Proteogenomics: decoding cancer in multiple dimensions

Qian Liu , Yimin Chen , Hu Zhou

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MedScience ›› DOI: 10.1007/s11684-026-1222-2
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Proteogenomics: decoding cancer in multiple dimensions
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Abstract

A key challenge in cancer precision oncology is the limited ability of genomic analyses to accurately predict changes in protein expression or function, even though proteins serve as the main targets of numerous modern therapies. Bridging this gap necessitates precise quantification of proteins and their post-translational modifications (PTMs). Recent advances in mass spectrometry (MS)-based proteomics now enable large-scale, quantitative characterization of proteins and PTMs in tumor tissues. To link genomic aberrations to cancer phenotypes, the emerging field of proteogenomics integrates proteomic data, including PTMs, with genomic, epigenomic, and transcriptomic information. This comprehensive approach offers a deeper understanding of cancer biology at multiple levels. This review highlights recent advancements in MS-based proteomics, key discoveries in cancer proteogenomics, and the transformative potential of this field in decoding the complexities of cancer across diverse dimensions.

Keywords

proteogenomics / proteomics / cancer / precision oncology / multi-omics

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Qian Liu, Yimin Chen, Hu Zhou. Proteogenomics: decoding cancer in multiple dimensions. MedScience DOI:10.1007/s11684-026-1222-2

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References

[1]

Hanahan D , Weinberg RA . Hallmarks of cancer: the next generation. Cell 2011; 144(5): 646–674

[2]

Vogelstein B , Papadopoulos N , Velculescu VE , Zhou S , Diaz LA Jr , Kinzler KW . Cancer genome landscapes. Science 2013; 339(6127): 1546–1558

[3]

Druker BJ , Talpaz M , Resta DJ , Peng B , Buchdunger E , Ford JM , Lydon NB , Kantarjian H , Capdeville R , Ohno-Jones S , Sawyers CL . Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N Engl J Med 2001; 344(14): 1031–1037

[4]

Piccart-Gebhart MJ , Procter M , Leyland-Jones B , Goldhirsch A , Untch M , Smith I , Gianni L , Baselga J , Bell R , Jackisch C , Cameron D , Dowsett M , Barrios CH , Steger G , Huang CS , Andersson M , Inbar M , Lichinitser M , Láng I , Nitz U , Iwata H , Thomssen C , Lohrisch C , Suter TM , Rüschoff J , Suto T , Greatorex V , Ward C , Straehle C , McFadden E , Dolci MS , Gelber RD; Herceptin Adjuvant (HERA) Trial Study Team . Trastuzumab after adjuvant chemotherapy in HER2-positive breast cancer. N Engl J Med 2005; 353(16): 1659–1672

[5]

Cooper AJ , Sequist LV , Lin JJ . Third-generation EGFR and ALK inhibitors: mechanisms of resistance and management. Nat Rev Clin Oncol 2022; 19(8): 499–514

[6]

Blum A , Wang P , Zenklusen JC . SnapShot: TCGA-analyzed tumors. Cell 2018; 173(2): 530

[7]

Hyman DM , Taylor BS , Baselga J . Implementing genome-driven oncology. Cell 2017; 168(4): 584–599

[8]

Gillette MA , Satpathy S , Cao S , Dhanasekaran SM , Vasaikar SV , Krug K , Petralia F , Li Y , Liang WW , Reva B , Krek A , Ji J , Song X , Liu W , Hong R , Yao L , Blumenberg L , Savage SR , Wendl MC , Wen B , Li K , Tang LC , MacMullan MA , Avanessian SC , Kane MH , Newton CJ , Cornwell M , Kothadia RB , Ma W , Yoo S , Mannan R , Vats P , Kumar-Sinha C , Kawaler EA , Omelchenko T , Colaprico A , Geffen Y , Maruvka YE , da Veiga Leprevost F , Wiznerowicz M , Gümüş ZH , Veluswamy RR , Hostetter G , Heiman DI , Wyczalkowski MA , Hiltke T , Mesri M , Kinsinger CR , Boja ES , Omenn GS , Chinnaiyan AM , Rodriguez H , Li QK , Jewell SD , Thiagarajan M , Getz G , Zhang B , Fenyö D , Ruggles KV , Cieslik MP , Robles AI , Clauser KR , Govindan R , Wang P , Nesvizhskii AI , Ding L , Mani DR , Carr SA; Clinical Proteomic Tumor Analysis Consortium . Proteogenomic characterization reveals therapeutic vulnerabilities in lung adenocarcinoma. Cell 2020; 182(1): 200–225.e35

[9]

Clark DJ , Dhanasekaran SM , Petralia F , Pan J , Song X , Hu Y , da Veiga Leprevost F , Reva B , Lih TM , Chang HY , Ma W , Huang C , Ricketts CJ , Chen L , Krek A , Li Y , Rykunov D , Li QK , Chen LS , Ozbek U , Vasaikar S , Wu Y , Yoo S , Chowdhury S , Wyczalkowski MA , Ji J , Schnaubelt M , Kong A , Sethuraman S , Avtonomov DM , Ao M , Colaprico A , Cao S , Cho KC , Kalayci S , Ma S , Liu W , Ruggles K , Calinawan A , Gümüş ZH , Geiszler D , Kawaler E , Teo GC , Wen B , Zhang Y , Keegan S , Li K , Chen F , Edwards N , Pierorazio PM , Chen XS , Pavlovich CP , Hakimi AA , Brominski G , Hsieh JJ , Antczak A , Omelchenko T , Lubinski J , Wiznerowicz M , Linehan WM , Kinsinger CR , Thiagarajan M , Boja ES , Mesri M , Hiltke T , Robles AI , Rodriguez H , Qian J , Fenyö D , Zhang B , Ding L , Schadt E , Chinnaiyan AM , Zhang Z , Omenn GS , Cieslik M , Chan DW , Nesvizhskii AI , Wang P , Zhang H; Clinical Proteomic Tumor Analysis Consortium . Integrated proteogenomic characterization of clear cell renal cell carcinoma. Cell 2019; 179(4): 964–983.e31

[10]

Liu Q , Zhang J , Guo C , Wang M , Wang C , Yan Y , Sun L , Wang D , Zhang L , Yu H , Hou L , Wu C , Zhu Y , Jiang G , Zhu H , Zhou Y , Fang S , Zhang T , Hu L , Li J , Liu Y , Zhang H , Zhang B , Ding L , Robles AI , Rodriguez H , Gao D , Ji H , Zhou H , Zhang P . Proteogenomic characterization of small cell lung cancer identifies biological insights and subtype-specific therapeutic strategies. Cell 2024; 187(1): 184–203.e28

[11]

Zhang B , Wang J , Wang X , Zhu J , Liu Q , Shi Z , Chambers MC , Zimmerman LJ , Shaddox KF , Kim S , Davies SR , Wang S , Wang P , Kinsinger CR , Rivers RC , Rodriguez H , Townsend RR , Ellis MJ , Carr SA , Tabb DL , Coffey RJ , Slebos RJ , Liebler DC; NCI CPTAC . Proteogenomic characterization of human colon and rectal cancer. Nature 2014; 513(7518): 382–387

[12]

Zhang B , Whiteaker JR , Hoofnagle AN , Baird GS , Rodland KD , Paulovich AG . Clinical potential of mass spectrometry-based proteogenomics. Nat Rev Clin Oncol 2019; 16(4): 256–268

[13]

Zizmare L , Hofmann U , Jarboui MA , Klose F , Fraschka S , Matthes J , Krüger M , Schaeffeler E , Schwab M , Ueffing M , Pichler BJ , Boldt K , Casadei N , Trautwein C . Cryogenic mouse tissue homogenization as an alternative to fresh-frozen biopsy use for genomics, transcriptomics, proteomics and metabolomics. Sci Rep 2025; 15(1): 20254

[14]

Daugaard I , Kjeldsen TE , Hager H , Hansen LL , Wojdacz TK . The influence of DNA degradation in formalin-fixed, paraffin-embedded (FFPE) tissue on locus-specific methylation assessment by MS-HRM. Exp Mol Pathol 2015; 99(3): 632–640

[15]

Chung JY , Braunschweig T , Hewitt SM . Optimization of recovery of RNA from formalin-fixed, paraffin-embedded tissue. Diagn Mol Pathol 2006; 15(4): 229–236

[16]

Wei L , Dugas M , Sandmann S . SimFFPE and FilterFFPE: improving structural variant calling in FFPE samples. Gigascience 2021; 10(9): giab065

[17]

Meggendorfer M , Jobanputra V , Wrzeszczynski KO , Roepman P , de Bruijn E , Cuppen E , Buttner R , Caldas C , Grimmond S , Mullighan CG , Elemento O , Rosenquist R , Schuh A , Haferlach T . Analytical demands to use whole-genome sequencing in precision oncology. Semin Cancer Biol 2022; 84: 16–22

[18]

Huang C , Chen L , Savage SR , Eguez RV , Dou Y , Li Y , da Veiga Leprevost F , Jaehnig EJ , Lei JT , Wen B , Schnaubelt M , Krug K , Song X , Cieślik M , Chang HY , Wyczalkowski MA , Li K , Colaprico A , Li QK , Clark DJ , Hu Y , Cao L , Pan J , Wang Y , Cho KC , Shi Z , Liao Y , Jiang W , Anurag M , Ji J , Yoo S , Zhou DC , Liang WW , Wendl M , Vats P , Carr SA , Mani DR , Zhang Z , Qian J , Chen XS , Pico AR , Wang P , Chinnaiyan AM , Ketchum KA , Kinsinger CR , Robles AI , An E , Hiltke T , Mesri M , Thiagarajan M , Weaver AM , Sikora AG , Lubiński J , Wierzbicka M , Wiznerowicz M , Satpathy S , Gillette MA , Miles G , Ellis MJ , Omenn GS , Rodriguez H , Boja ES , Dhanasekaran SM , Ding L , Nesvizhskii AI , El-Naggar AK , Chan DW , Zhang H , Zhang B; Clinical Proteomic Tumor Analysis Consortium . Proteogenomic insights into the biology and treatment of HPV-negative head and neck squamous cell carcinoma. Cancer Cell 2021; 39(3): 361–379.e16

[19]

Dou Y , Kawaler EA , Cui Zhou D , Gritsenko MA , Huang C , Blumenberg L , Karpova A , Petyuk VA , Savage SR , Satpathy S , Liu W , Wu Y , Tsai CF , Wen B , Li Z , Cao S , Moon J , Shi Z , Cornwell M , Wyczalkowski MA , Chu RK , Vasaikar S , Zhou H , Gao Q , Moore RJ , Li K , Sethuraman S , Monroe ME , Zhao R , Heiman D , Krug K , Clauser K , Kothadia R , Maruvka Y , Pico AR , Oliphant AE , Hoskins EL , Pugh SL , Beecroft SJI , Adams DW , Jarman JC , Kong A , Chang HY , Reva B , Liao Y , Rykunov D , Colaprico A , Chen XS , Czekański A , Jędryka M , Matkowski R , Wiznerowicz M , Hiltke T , Boja E , Kinsinger CR , Mesri M , Robles AI , Rodriguez H , Mutch D , Fuh K , Ellis MJ , DeLair D , Thiagarajan M , Mani DR , Getz G , Noble M , Nesvizhskii AI , Wang P , Anderson ML , Levine DA , Smith RD , Payne SH , Ruggles KV , Rodland KD , Ding L , Zhang B , Liu T , Fenyö D; Clinical Proteomic Tumor Analysis Consortium . Proteogenomic characterization of endometrial carcinoma. Cell 2020; 180(4): 729–748.e26

[20]

Kim KH , Migliozzi S , Koo H , Hong JH , Park SM , Kim S , Kwon HJ , Ha S , Garofano L , Oh YT , D’Angelo F , Kim CI , Kim S , Lee JY , Kim J , Hong J , Jang EH , Mathon B , Di Stefano AL , Bielle F , Laurenge A , Nesvizhskii AI , Hur EM , Yin J , Shi B , Kim Y , Moon KS , Kwon JT , Lee SH , Lee SH , Gwak HS , Lasorella A , Yoo H , Sanson M , Sa JK , Park CK , Nam DH , Iavarone A , Park JB . Integrated proteogenomic characterization of glioblastoma evolution. Cancer Cell 2024; 42(3): 358–377.e8

[21]

Pena SDJ , Tarazona-Santos E . Clinical genomics and precision medicine. Genet Mol Biol 2022; 45(3): e20220150

[22]

Zhao Y , Fang LT , Shen TW , Choudhari S , Talsania K , Chen X , Shetty J , Kriga Y , Tran B , Zhu B , Chen Z , Chen W , Wang C , Jaeger E , Meerzaman D , Lu C , Idler K , Ren L , Zheng Y , Shi L , Petitjean V , Sultan M , Hung T , Peters E , Drabek J , Vojta P , Maestro R , Gasparotto D , Kõks S , Reimann E , Scherer A , Nordlund J , Liljedahl U , Foox J , Mason CE , Xiao C , Hong H , Xiao W . Whole genome and exome sequencing reference datasets from a multi-center and cross-platform benchmark study. Sci Data 2021; 8(1): 296

[23]

Belkadi A , Bolze A , Itan Y , Cobat A , Vincent QB , Antipenko A , Shang L , Boisson B , Casanova JL , Abel L . Whole-genome sequencing is more powerful than whole-exome sequencing for detecting exome variants. Proc Natl Acad Sci USA 2015; 112(17): 5473–5478

[24]

Minoche AE , Lundie B , Peters GB , Ohnesorg T , Pinese M , Thomas DM , Zankl A , Roscioli T , Schonrock N , Kummerfeld S , Burnett L , Dinger ME , Cowley MJ . ClinSV: clinical grade structural and copy number variant detection from whole genome sequencing data. Genome Med 2021; 13(1): 32

[25]

Bartha Á , Győrffy B . Comprehensive outline of whole exome sequencing data analysis tools available in clinical oncology. Cancers (Basel) 2019; 11(11): 1725

[26]

Wirka RC , Pjanic M , Quertermous T . Advances in transcriptomics: investigating cardiovascular disease at unprecedented resolution. Circ Res 2018; 122(9): 1200–1220

[27]

Molbert N , Ghanavi HR , Johansson T , Mostadius M , Hansson MC . An evaluation of DNA extraction methods on historical and roadkill mammalian specimen. Sci Rep 2023; 13(1): 13080

[28]

Sultan M , Amstislavskiy V , Risch T , Schuette M , Dökel S , Ralser M , Balzereit D , Lehrach H , Yaspo ML . Influence of RNA extraction methods and library selection schemes on RNA-seq data. BMC Genomics 2014; 15(1): 675

[29]

Xiang H , Luo R , Wang Y , Yang B , Xu S , Huang W , Tang S , Fang R , Chen L , Zhu N , Yu Z , Akesu S , Wei C , Xu C , Zhou Y , Gu J , Zhao J , Hou Y , Ding C . Proteogenomic insights into the biology and treatment of pan-melanoma. Cell Discov 2024; 10(1): 78

[30]

Xu N , Yao Z , Shang G , Ye D , Wang H , Zhang H , Qu Y , Xu F , Wang Y , Qin Z , Zhu J , Zhang F , Feng J , Tian S , Liu Y , Zhao J , Hou J , Guo J , Hou Y , Ding C . Integrated proteogenomic characterization of urothelial carcinoma of the bladder. J Hematol Oncol 2022; 15(1): 76

[31]

Liu J , Cao S , Imbach KJ , Gritsenko MA , Lih TM , Kyle JE , Yaron-Barir TM , Binder ZA , Li Y , Strunilin I , Wang YT , Tsai CF , Ma W , Chen L , Clark NM , Shinkle A , Naser Al Deen N , Caravan W , Houston A , Simin FA , Wyczalkowski MA , Wang LB , Storrs E , Chen S , Illindala R , Li YD , Jayasinghe RG , Rykunov D , Cottingham SL , Chu RK , Weitz KK , Moore RJ , Sagendorf T , Petyuk VA , Nestor M , Bramer LM , Stratton KG , Schepmoes AA , Couvillion SP , Eder J , Kim YM , Gao Y , Fillmore TL , Zhao R , Monroe ME , Southard-Smith AN , Li YE , Jui-Hsien Lu R , Johnson JL , Wiznerowicz M , Hostetter G , Newton CJ , Ketchum KA , Thangudu RR , Barnholtz-Sloan JS , Wang P , Fenyö D , An E , Thiagarajan M , Robles AI , Mani DR , Smith RD , Porta-Pardo E , Cantley LC , Iavarone A , Chen F , Mesri M , Nasrallah MP , Zhang H , Resnick AC , Chheda MG , Rodland KD , Liu T , Ding L; Philadelphia Coalition for a Cure; Clinical Proteomic Tumor Analysis Consortium . Multi-scale signaling and tumor evolution in high-grade gliomas. Cancer Cell 2024; 42(7): 1217–1238.e19

[32]

Li GX , Chen L , Hsiao Y , Mannan R , Zhang Y , Luo J , Petralia F , Cho H , Hosseini N , Leprevost FDV , Calinawan A , Li Y , Anand S , Dagar A , Geffen Y , Kumar-Sinha C , Chugh S , Le A , Ponce S , Guo S , Zhang C , Schnaubelt M , Al Deen NN , Chen F , Caravan W , Houston A , Hopkins A , Newton CJ , Wang X , Polasky DA , Haynes S , Yu F , Jing X , Chen S , Robles AI , Mesri M , Thiagarajan M , An E , Getz GA , Linehan WM , Hostetter G , Jewell SD , Chan DW , Wang P , Omenn GS , Mehra R , Ricketts CJ , Ding L , Chinnaiyan AM , Cieslik MP , Dhanasekaran SM , Zhang H , Nesvizhskii AI; Clinical Proteomic Tumor Analysis Consortium . Comprehensive proteogenomic characterization of rare kidney tumors. Cell Rep Med 2024; 5(5): 101547

[33]

Cao L , Huang C , Cui Zhou D , Hu Y , Lih TM , Savage SR , Krug K , Clark DJ , Schnaubelt M , Chen L , da Veiga Leprevost F , Eguez RV , Yang W , Pan J , Wen B , Dou Y , Jiang W , Liao Y , Shi Z , Terekhanova NV , Cao S , Lu RJ , Li Y , Liu R , Zhu H , Ronning P , Wu Y , Wyczalkowski MA , Easwaran H , Danilova L , Mer AS , Yoo S , Wang JM , Liu W , Haibe-Kains B , Thiagarajan M , Jewell SD , Hostetter G , Newton CJ , Li QK , Roehrl MH , Fenyö D , Wang P , Nesvizhskii AI , Mani DR , Omenn GS , Boja ES , Mesri M , Robles AI , Rodriguez H , Bathe OF , Chan DW , Hruban RH , Ding L , Zhang B , Zhang H; Clinical Proteomic Tumor Analysis Consortium . Proteogenomic characterization of pancreatic ductal adenocarcinoma. Cell 2021; 184(19): 5031–5052.e26

[34]

Ribarska T , Bjørnstad PM , Sundaram AYM , Gilfillan GD . Optimization of enzymatic fragmentation is crucial to maximize genome coverage: a comparison of library preparation methods for Illumina sequencing. BMC Genomics 2022; 23(1): 92

[35]

Chen R , Im H , Snyder M . Whole-exome enrichment with the Agilent SureSelect Human All Exon Platform. Cold Spring Harb Protoc 2015; 2015(7): 626–633

[36]

Rio DCAres M JrHannon GJNilsen TW. Enrichment of poly(A)+ mRNA using immobilized oligo(dT). Cold Spring Harb Protoc 2010; 2010(7): pdb. prot5454 doi:10.1101/pdb.prot5454

[37]

Andrzejewska-Romanowska A , Tykwińska E , Śledziński P , Pachulska-Wieczorek K . A comparative analysis of mRNA enrichment strategies and guidance for improving their efficiency. Sci Rep 2025; 15(1): 17890

[38]

Su Q , Wang J , Kang K , Niu Y , Li S , Gou D . Critical view on oligo(dT)-based RNA-seq: bias arising, modeling, and mitigating. Genetics 2024; 226(3): iyad190

[39]

Baldwin A , Morris AR , Mukherjee N . An easy, cost-effective, and scalable method to deplete human ribosomal RNA for RNA-seq. Curr Protoc 2021; 1(6): e176

[40]

Wahl A , Huptas C , Neuhaus K . Comparison of rRNA depletion methods for efficient bacterial mRNA sequencing. Sci Rep 2022; 12(1): 5765

[41]

Picelli S , Faridani OR , Björklund AK , Winberg G , Sagasser S , Sandberg R . Full-length RNA-seq from single cells using Smart-seq2. Nat Protoc 2014; 9(1): 171–181

[42]

Zhu YY , Machleder EM , Chenchik A , Li R , Siebert PD . Reverse transcriptase template switching: a SMART approach for full-length cDNA library construction. Biotechniques 2001; 30(4): 892–897

[43]

Isaic A , Motofelea N , Hoinoiu T , Motofelea AC , Leancu IC , Stan E , Gheorghe SR , Dutu AG , Crintea A . Next-generation sequencing: a review of its transformative impact on cancer diagnosis, treatment, and resistance management. Diagnostics (Basel) 2025; 15(19): 2425

[44]

Head SR , Komori HK , LaMere SA , Whisenant T , Van Nieuwerburgh F , Salomon DR , Ordoukhanian P . Library construction for next-generation sequencing: overviews and challenges. Biotechniques 2014; 56(2): 61–77

[45]

Bentz ML , Clines C , Padilla J , Horn C , Lee J , Sheth M . High-throughput PacBio library preparation and sequencing techniques for genomic DNA and TNA. Front Genet 2025; 16: 1587691

[46]

Weirather JL , de Cesare M , Wang Y , Piazza P , Sebastiano V , Wang XJ , Buck D , Au KF . Comprehensive comparison of Pacific Biosciences and Oxford Nanopore Technologies and their applications to transcriptome analysis. F1000 Res 2017; 6: 100

[47]

Schoffman H , Levin Y , Itzhaki-Alfia A , Tselekovits L , Gonen L , Vainer GW , Hout-Siloni G , Barshack I , Cohen ZR , Margalit N , Shahar T . Comparison of matched formalin-fixed paraffin embedded and fresh frozen meningioma tissue reveals bias in proteomic profiles. Proteomics 2022; 22(21): e2200085

[48]

Weist S , Brunkau C , Wittke J , Eravci M , Broedel O , Krause E , Stephanowitz H , Eravci S , Baumgartner A . Effects of thawing, refreezing and storage conditions of tissue samples and protein extracts on 2-DE spot intensity. Proteomics 2010; 10(7): 1515–1521

[49]

Xie R , Chung JY , Ylaya K , Williams RL , Guerrero N , Nakatsuka N , Badie C , Hewitt SM . Factors influencing the degradation of archival formalin-fixed paraffin-embedded tissue sections. J Histochem Cytochem 2011; 59(4): 356–365

[50]

Satpathy S , Jaehnig EJ , Krug K , Kim BJ , Saltzman AB , Chan DW , Holloway KR , Anurag M , Huang C , Singh P , Gao A , Namai N , Dou Y , Wen B , Vasaikar SV , Mutch D , Watson MA , Ma C , Ademuyiwa FO , Rimawi MF , Schiff R , Hoog J , Jacobs S , Malovannaya A , Hyslop T , Clauser KR , Mani DR , Perou CM , Miles G , Zhang B , Gillette MA , Carr SA , Ellis MJ . Microscaled proteogenomic methods for precision oncology. Nat Commun 2020; 11(1): 532

[51]

Friedrich C , Schallenberg S , Kirchner M , Ziehm M , Niquet S , Haji M , Beier C , Neudecker J , Klauschen F , Mertins P . Comprehensive micro-scaled proteome and phosphoproteome characterization of archived retrospective cancer repositories. Nat Commun 2021; 12(1): 3576

[52]

Coscia F , Doll S , Bech JM , Schweizer L , Mund A , Lengyel E , Lindebjerg J , Madsen GI , Moreira JM , Mann M . A streamlined mass spectrometry-based proteomics workflow for large-scale FFPE tissue analysis. J Pathol 2020; 251(1): 100–112

[53]

Buczak K , Kirkpatrick JM , Truckenmueller F , Santinha D , Ferreira L , Roessler S , Singer S , Beck M , Ori A . Spatially resolved analysis of FFPE tissue proteomes by quantitative mass spectrometry. Nat Protoc 2020; 15(9): 2956–2979

[54]

Li L , Jiang D , Liu H , Guo C , Zhang Q , Li X , Chen X , Chen Z , Feng J , Tan S , Huang W , Huang J , Xu C , Liu CY , Yu W , Hou Y , Ding C . Comprehensive proteogenomic profiling reveals the molecular characteristics of colorectal cancer at distinct stages of progression. Cancer Res 2024; 84(17): 2888–2910

[55]

Hu Z , Wu Z , Liu W , Ning Y , Liu J , Ding W , Fan J , Cai S , Li Q , Li W , Yang X , Dou Y , Wang W , Peng W , Lu F , Zhuang X , Qin T , Kang X , Feng C , Xu Z , Lv Q , Wang Q , Wang C , Wang X , Wang Z , Wang J , Jiang J , Wang B , Mills GB , Ma D , Gao Q , Li K , Chen G , Chen X , Sun C . Proteogenomic insights into early-onset endometrioid endometrial carcinoma: predictors for fertility-sparing therapy response. Nat Genet 2024; 56(4): 637–651

[56]

Li L , Jiang D , Liu H , Guo C , Zhao R , Zhang Q , Xu C , Qin Z , Feng J , Liu Y , Wang H , Chen W , Zhang X , Li B , Bai L , Tian S , Tan S , Yu Z , Chen L , Huang J , Zhao JY , Hou Y , Ding C . Comprehensive proteogenomic characterization of early duodenal cancer reveals the carcinogenesis tracks of different subtypes. Nat Commun 2023; 14(1): 1751

[57]

Li L , Jiang D , Zhang Q , Liu H , Xu F , Guo C , Qin Z , Wang H , Feng J , Liu Y , Chen W , Zhang X , Bai L , Tian S , Tan S , Xu C , Song Q , Liu Y , Zhong Y , Chen T , Zhou P , Zhao JY , Hou Y , Ding C . Integrative proteogenomic characterization of early esophageal cancer. Nat Commun 2023; 14(1): 1666

[58]

Piehowski PD , Petyuk VA , Sontag RL , Gritsenko MA , Weitz KK , Fillmore TL , Moon J , Makhlouf H , Chuaqui RF , Boja ES , Rodriguez H , Lee JSH , Smith RD , Carrick DM , Liu T , Rodland KD . Residual tissue repositories as a resource for population-based cancer proteomic studies. Clin Proteomics 2018; 15(1): 26

[59]

Irving JA , Cain G , Parr A , Howard M , Angus B , Cattan AR . OCT embedded sections of pathological specimens as a source of high quality RNA for reverse transcriptase/polymerase chain reaction. J Clin Pathol 1996; 49(3): 258–259

[60]

Turbett GR , Sellner LN . The use of optimal cutting temperature compound can inhibit amplification by polymerase chain reaction. Diagn Mol Pathol 1997; 6(5): 298–303

[61]

Shah P , Zhang B , Choi C , Yang S , Zhou J , Harlan R , Tian Y , Zhang Z , Chan DW , Zhang H . Tissue proteomics using chemical immobilization and mass spectrometry. Anal Biochem 2015; 469: 27–33

[62]

Zhao X , Huffman KE , Fujimoto J , Canales JR , Girard L , Nie G , Heymach JV , Wistuba II , Minna JD , Yu Y . Quantitative proteomic analysis of optimal cutting temperature (OCT) embedded core-needle biopsy of lung cancer. J Am Soc Mass Spectrom 2017; 28(10): 2078–2089

[63]

Krug K , Jaehnig EJ , Satpathy S , Blumenberg L , Karpova A , Anurag M , Miles G , Mertins P , Geffen Y , Tang LC , Heiman DI , Cao S , Maruvka YE , Lei JT , Huang C , Kothadia RB , Colaprico A , Birger C , Wang J , Dou Y , Wen B , Shi Z , Liao Y , Wiznerowicz M , Wyczalkowski MA , Chen XS , Kennedy JJ , Paulovich AG , Thiagarajan M , Kinsinger CR , Hiltke T , Boja ES , Mesri M , Robles AI , Rodriguez H , Westbrook TF , Ding L , Getz G , Clauser KR , Fenyö D , Ruggles KV , Zhang B , Mani DR , Carr SA , Ellis MJ , Gillette MA; Clinical Proteomic Tumor Analysis Consortium . Proteogenomic landscape of breast cancer tumorigenesis and targeted therapy. Cell 2020; 183(5): 1436–1456.e31

[64]

Mertins P , Mani DR , Ruggles KV , Gillette MA , Clauser KR , Wang P , Wang X , Qiao JW , Cao S , Petralia F , Kawaler E , Mundt F , Krug K , Tu Z , Lei JT , Gatza ML , Wilkerson M , Perou CM , Yellapantula V , Huang KL , Lin C , McLellan MD , Yan P , Davies SR , Townsend RR , Skates SJ , Wang J , Zhang B , Kinsinger CR , Mesri M , Rodriguez H , Ding L , Paulovich AG , Fenyö D , Ellis MJ , Carr SA; NCI CPTAC . Proteogenomics connects somatic mutations to signalling in breast cancer. Nature 2016; 534(7605): 55–62

[65]

Raj-Kumar PK , Lin X , Liu T , Sturtz LA , Gritsenko MA , Petyuk VA , Sagendorf TJ , Deyarmin B , Liu J , Praveen-Kumar A , Wang G , McDermott JE , Shukla AK , Moore RJ , Monroe ME , Webb-Robertson BM , Hooke JA , Fantacone-Campbell L , Mostoller B , Kvecher L , Kane J , Melley J , Somiari S , Soon-Shiong P , Smith RD , Mural RJ , Rodland KD , Shriver CD , Kovatich AJ , Hu H . Proteogenomic characterization of difficult-to-treat breast cancer with tumor cells enriched through laser microdissection. Breast Cancer Res 2024; 26(1): 76

[66]

Vasaikar S , Huang C , Wang X , Petyuk VA , Savage SR , Wen B , Dou Y , Zhang Y , Shi Z , Arshad OA , Gritsenko MA , Zimmerman LJ , McDermott JE , Clauss TR , Moore RJ , Zhao R , Monroe ME , Wang YT , Chambers MC , Slebos RJC , Lau KS , Mo Q , Ding L , Ellis M , Thiagarajan M , Kinsinger CR , Rodriguez H , Smith RD , Rodland KD , Liebler DC , Liu T , Zhang B; Clinical Proteomic Tumor Analysis Consortium . Proteogenomic analysis of human colon cancer reveals new therapeutic opportunities. Cell 2019; 177(4): 1035–1049.e19

[67]

Dou Y , Katsnelson L , Gritsenko MA , Hu Y , Reva B , Hong R , Wang YT , Kolodziejczak I , Lu RJ , Tsai CF , Bu W , Liu W , Guo X , An E , Arend RC , Bavarva J , Chen L , Chu RK , Czekański A , Davoli T , Demicco EG , DeLair D , Devereaux K , Dhanasekaran SM , Dottino P , Dover B , Fillmore TL , Foxall M , Hermann CE , Hiltke T , Hostetter G , Jędryka M , Jewell SD , Johnson I , Kahn AG , Ku AT , Kumar-Sinha C , Kurzawa P , Lazar AJ , Lazcano R , Lei JT , Li Y , Liao Y , Lih TM , Lin TT , Martignetti JA , Masand RP , Matkowski R , McKerrow W , Mesri M , Monroe ME , Moon J , Moore RJ , Nestor MD , Newton C , Omelchenko T , Omenn GS , Payne SH , Petyuk VA , Robles AI , Rodriguez H , Ruggles KV , Rykunov D , Savage SR , Schepmoes AA , Shi T , Shi Z , Tan J , Taylor M , Thiagarajan M , Wang JM , Weitz KK , Wen B , Williams CM , Wu Y , Wyczalkowski MA , Yi X , Zhang X , Zhao R , Mutch D , Chinnaiyan AM , Smith RD , Nesvizhskii AI , Wang P , Wiznerowicz M , Ding L , Mani DR , Zhang H , Anderson ML , Rodland KD , Zhang B , Liu T , Fenyö D; Clinical Proteomic Tumor Analysis Consortium . Proteogenomic insights suggest druggable pathways in endometrial carcinoma. Cancer Cell 2023; 41(9): 1586–1605.e15

[68]

McDermott JE , Arshad OA , Petyuk VA , Fu Y , Gritsenko MA , Clauss TR , Moore RJ , Schepmoes AA , Zhao R , Monroe ME , Schnaubelt M , Tsai CF , Payne SH , Huang C , Wang LB , Foltz S , Wyczalkowski M , Wu Y , Song E , Brewer MA , Thiagarajan M , Kinsinger CR , Robles AI , Boja ES , Rodriguez H , Chan DW , Zhang B , Zhang Z , Ding L , Smith RD , Liu T , Rodland KD; Clinical Proteomic Tumor Analysis Consortium . Proteogenomic characterization of ovarian HGSC implicates mitotic kinases, replication stress in observed chromosomal instability. Cell Rep Med 2020; 1(1): 100004

[69]

Hu Y , Pan J , Shah P , Ao M , Thomas SN , Liu Y , Chen L , Schnaubelt M , Clark DJ , Rodriguez H , Boja ES , Hiltke T , Kinsinger CR , Rodland KD , Li QK , Qian J , Zhang Z , Chan DW , Zhang H; Clinical Proteomic Tumor Analysis Consortium . Integrated proteomic and glycoproteomic characterization of human high-grade serous ovarian carcinoma. Cell Rep 2020; 33(3): 108276

[70]

Zhang H , Liu T , Zhang Z , Payne SH , Zhang B , McDermott JE , Zhou JY , Petyuk VA , Chen L , Ray D , Sun S , Yang F , Chen L , Wang J , Shah P , Cha SW , Aiyetan P , Woo S , Tian Y , Gritsenko MA , Clauss TR , Choi C , Monroe ME , Thomas S , Nie S , Wu C , Moore RJ , Yu KH , Tabb DL , Fenyö D , Bafna V , Wang Y , Rodriguez H , Boja ES , Hiltke T , Rivers RC , Sokoll L , Zhu H , Shih IM , Cope L , Pandey A , Zhang B , Snyder MP , Levine DA , Smith RD , Chan DW , Rodland KD; CPTAC Investigators . Integrated proteogenomic characterization of human high-grade serous ovarian cancer. Cell 2016; 166(3): 755–765

[71]

Sinha A , Huang V , Livingstone J , Wang J , Fox NS , Kurganovs N , Ignatchenko V , Fritsch K , Donmez N , Heisler LE , Shiah YJ , Yao CQ , Alfaro JA , Volik S , Lapuk A , Fraser M , Kron K , Murison A , Lupien M , Sahinalp C , Collins CC , Tetu B , Masoomian M , Berman DM , van der Kwast T , Bristow RG , Kislinger T , Boutros PC . The proteogenomic landscape of curable prostate cancer. Cancer Cell 2019; 35(3): 414–427.e6

[72]

Macklin A , Khan S , Kislinger T . Recent advances in mass spectrometry based clinical proteomics: applications to cancer research. Clin Proteomics 2020; 17(1): 17

[73]

Li X , Wang W , Chen J . Recent progress in mass spectrometry proteomics for biomedical research. Sci China Life Sci 2017; 60(10): 1093–1113

[74]

Zhu W , Smith JW , Huang CM . Mass spectrometry-based label-free quantitative proteomics. J Biomed Biotechnol 2010; 2010: 840518

[75]

Bateman NW , Goulding SP , Shulman NJ , Gadok AK , Szumlinski KK , MacCoss MJ , Wu CC . Maximizing peptide identification events in proteomic workflows using data-dependent acquisition (DDA). Mol Cell Proteomics 2014; 13(1): 329–338

[76]

Qu N , Chen D , Ma B , Zhang L , Wang Q , Wang Y , Wang H , Ni Z , Wang W , Liao T , Xiang J , Wang Y , Jin S , Xue D , Wu W , Wang Y , Ji Q , He H , Piao HL , Shi R . Integrated proteogenomic and metabolomic characterization of papillary thyroid cancer with different recurrence risks. Nat Commun 2024; 15(1): 3175

[77]

Tanaka A , Ogawa M , Zhou Y , Namba K , Hendrickson RC , Miele MM , Li Z , Klimstra DS , Buckley PG , Gulcher J , Wang JY , Roehrl MHA . Proteogenomic characterization of primary colorectal cancer and metastatic progression identifies proteome-based subtypes and signatures. Cell Rep 2024; 43(2): 113810

[78]

Qu Y , Feng J , Wu X , Bai L , Xu W , Zhu L , Liu Y , Xu F , Zhang X , Yang G , Lv J , Chen X , Shi GH , Wang HK , Cao DL , Xiang H , Li L , Tan S , Gan HL , Sun MH , Qiu J , Zhang H , Zhao JY , Ye D , Ding C . A proteogenomic analysis of clear cell renal cell carcinoma in a Chinese population. Nat Commun 2022; 13(1): 2052

[79]

Nassiri F , Liu J , Patil V , Mamatjan Y , Wang JZ , Hugh-White R , Macklin AM , Khan S , Singh O , Karimi S , Corona RI , Liu LY , Chen CY , Chakravarthy A , Wei Q , Mehani B , Suppiah S , Gao A , Workewych AM , Tabatabai G , Boutros PC , Bader GD , de Carvalho DD , Kislinger T , Aldape K , Zadeh G . A clinically applicable integrative molecular classification of meningiomas. Nature 2021; 597(7874): 119–125

[80]

Xu JY , Zhang C , Wang X , Zhai L , Ma Y , Mao Y , Qian K , Sun C , Liu Z , Jiang S , Wang M , Feng L , Zhao L , Liu P , Wang B , Zhao X , Xie H , Yang X , Zhao L , Chang Y , Jia J , Wang X , Zhang Y , Wang Y , Yang Y , Wu Z , Yang L , Liu B , Zhao T , Ren S , Sun A , Zhao Y , Ying W , Wang F , Wang G , Zhang Y , Cheng S , Qin J , Qian X , Wang Y , Li J , He F , Xiao T , Tan M . Integrative proteomic characterization of human lung adenocarcinoma. Cell 2020; 182(1): 245–261.e17

[81]

Chahrour O , Cobice D , Malone J . Stable isotope labelling methods in mass spectrometry-based quantitative proteomics. J Pharm Biomed Anal 2015; 113: 2–20

[82]

Thompson A , Schäfer J , Kuhn K , Kienle S , Schwarz J , Schmidt G , Neumann T , Johnstone R , Mohammed AK , Hamon C . Tandem mass tags: a novel quantification strategy for comparative analysis of complex protein mixtures by MS/MS. Anal Chem 2003; 75(8): 1895–1904

[83]

Gao Q , Zhu H , Dong L , Shi W , Chen R , Song Z , Huang C , Li J , Dong X , Zhou Y , Liu Q , Ma L , Wang X , Zhou J , Liu Y , Boja E , Robles AI , Ma W , Wang P , Li Y , Ding L , Wen B , Zhang B , Rodriguez H , Gao D , Zhou H , Fan J . Integrated proteogenomic characterization of HBV-related hepatocellular carcinoma. Cell 2019; 179(2): 561–577.e22

[84]

Lehtiö J , Arslan T , Siavelis I , Pan Y , Socciarelli F , Berkovska O , Umer HM , Mermelekas G , Pirmoradian M , Jönsson M , Brunnström H , Brustugun OT , Purohit KP , Cunningham R , Foroughi Asl H , Isaksson S , Arbajian E , Aine M , Karlsson A , Kotevska M , Gram Hansen C , Drageset Haakensen V , Helland Å , Tamborero D , Johansson HJ , Branca RM , Planck M , Staaf J , Orre LM . Proteogenomics of non-small cell lung cancer reveals molecular subtypes associated with specific therapeutic targets and immune evasion mechanisms. Nat Cancer 2021; 2(11): 1224–1242

[85]

Satpathy S , Krug K , Jean Beltran PM , Savage SR , Petralia F , Kumar-Sinha C , Dou Y , Reva B , Kane MH , Avanessian SC , Vasaikar SV , Krek A , Lei JT , Jaehnig EJ , Omelchenko T , Geffen Y , Bergstrom EJ , Stathias V , Christianson KE , Heiman DI , Cieslik MP , Cao S , Song X , Ji J , Liu W , Li K , Wen B , Li Y , Gümüş ZH , Selvan ME , Soundararajan R , Visal TH , Raso MG , Parra ER , Babur Ö , Vats P , Anand S , Schraink T , Cornwell M , Rodrigues FM , Zhu H , Mo CK , Zhang Y , da Veiga Leprevost F , Huang C , Chinnaiyan AM , Wyczalkowski MA , Omenn GS , Newton CJ , Schurer S , Ruggles KV , Fenyö D , Jewell SD , Thiagarajan M , Mesri M , Rodriguez H , Mani SA , Udeshi ND , Getz G , Suh J , Li QK , Hostetter G , Paik PK , Dhanasekaran SM , Govindan R , Ding L , Robles AI , Clauser KR , Nesvizhskii AI , Wang P , Carr SA , Zhang B , Mani DR , Gillette MA; Clinical Proteomic Tumor Analysis Consortium . A proteogenomic portrait of lung squamous cell carcinoma. Cell 2021; 184(16): 4348–4371.e40

[86]

Park SJ , Ju S , Goh SH , Yoon BH , Park JL , Kim JH , Lee S , Lee SJ , Kwon Y , Lee W , Park KC , Lee GK , Park SY , Kim S , Kim SY , Han JY , Lee C . Proteogenomic characterization reveals estrogen signaling as a target for never-smoker lung adenocarcinoma patients without EGFR or ALK alterations. Cancer Res 2024; 84(9): 1491–1503

[87]

Wang LB , Karpova A , Gritsenko MA , Kyle JE , Cao S , Li Y , Rykunov D , Colaprico A , Rothstein JH , Hong R , Stathias V , Cornwell M , Petralia F , Wu Y , Reva B , Krug K , Pugliese P , Kawaler E , Olsen LK , Liang WW , Song X , Dou Y , Wendl MC , Caravan W , Liu W , Cui Zhou D , Ji J , Tsai CF , Petyuk VA , Moon J , Ma W , Chu RK , Weitz KK , Moore RJ , Monroe ME , Zhao R , Yang X , Yoo S , Krek A , Demopoulos A , Zhu H , Wyczalkowski MA , McMichael JF , Henderson BL , Lindgren CM , Boekweg H , Lu S , Baral J , Yao L , Stratton KG , Bramer LM , Zink E , Couvillion SP , Bloodsworth KJ , Satpathy S , Sieh W , Boca SM , Schürer S , Chen F , Wiznerowicz M , Ketchum KA , Boja ES , Kinsinger CR , Robles AI , Hiltke T , Thiagarajan M , Nesvizhskii AI , Zhang B , Mani DR , Ceccarelli M , Chen XS , Cottingham SL , Li QK , Kim AH , Fenyö D , Ruggles KV , Rodriguez H , Mesri M , Payne SH , Resnick AC , Wang P , Smith RD , Iavarone A , Chheda MG , Barnholtz-Sloan JS , Rodland KD , Liu T , Ding L; Clinical Proteomic Tumor Analysis Consortium . Proteogenomic and metabolomic characterization of human glioblastoma. Cancer Cell 2021; 39(4): 509–528.e20

[88]

Li C , Sun YD , Yu GY , Cui JR , Lou Z , Zhang H , Huang Y , Bai CG , Deng LL , Liu P , Zheng K , Wang YH , Wang QQ , Li QR , Wu QQ , Liu Q , Shyr Y , Li YX , Chen LN , Wu JR , Zhang W , Zeng R . Integrated omics of metastatic colorectal cancer. Cancer Cell 2020; 38(5): 734–747.e9

[89]

Li Y , Lih TM , Dhanasekaran SM , Mannan R , Chen L , Cieslik M , Wu Y , Lu RJ , Clark DJ , Kołodziejczak I , Hong R , Chen S , Zhao Y , Chugh S , Caravan W , Naser Al Deen N , Hosseini N , Newton CJ , Krug K , Xu Y , Cho KC , Hu Y , Zhang Y , Kumar-Sinha C , Ma W , Calinawan A , Wyczalkowski MA , Wendl MC , Wang Y , Guo S , Zhang C , Le A , Dagar A , Hopkins A , Cho H , Leprevost FDV , Jing X , Teo GC , Liu W , Reimers MA , Pachynski R , Lazar AJ , Chinnaiyan AM , Van Tine BA , Zhang B , Rodland KD , Getz G , Mani DR , Wang P , Chen F , Hostetter G , Thiagarajan M , Linehan WM , Fenyö D , Jewell SD , Omenn GS , Mehra R , Wiznerowicz M , Robles AI , Mesri M , Hiltke T , An E , Rodriguez H , Chan DW , Ricketts CJ , Nesvizhskii AI , Zhang H , Ding L; Clinical Proteomic Tumor Analysis Consortium . Histopathologic and proteogenomic heterogeneity reveals features of clear cell renal cell carcinoma aggressiveness. Cancer Cell 2023; 41(1): 139–163.e17

[90]

Blackburn K , Mbeunkui F , Mitra SK , Mentzel T , Goshe MB . Improving protein and proteome coverage through data-independent multiplexed peptide fragmentation. J Proteome Res 2010; 9(7): 3621–3637

[91]

Meier F , Park MA , Mann M . Trapped ion mobility spectrometry and parallel accumulation-serial fragmentation in proteomics. Mol Cell Proteomics 2021; 20: 100138

[92]

Kuster B , Tüshaus J , Bayer FP . A new mass analyzer shakes up the proteomics field. Nat Biotechnol 2024; 42(12): 1796–1797

[93]

Fíla J , Honys D . Enrichment techniques employed in phosphoproteomics. Amino Acids 2012; 43(3): 1025–1047

[94]

Li S , Yuan L , Xu ZY , Xu JL , Chen GP , Guan X , Pan GZ , Hu C , Dong J , Du YA , Yang LT , Ni MW , Jiang RB , Zhu X , Lv H , Xu HD , Zhang SJ , Qin JJ , Cheng XD . Integrative proteomic characterization of adenocarcinoma of esophagogastric junction. Nat Commun 2023; 14(1): 778

[95]

Pino JC , Posso C , Joshi SK , Nestor M , Moon J , Hansen JR , Hutchinson-Bunch C , Gritsenko MA , Weitz KK , Watanabe-Smith K , Long N , McDermott JE , Druker BJ , Liu T , Tyner JW , Agarwal A , Traer E , Piehowski PD , Tognon CE , Rodland KD , Gosline SJC . Mapping the proteogenomic landscape enables prediction of drug response in acute myeloid leukemia. Cell Rep Med 2024; 5(1): 101359

[96]

Chowdhury S , Kennedy JJ , Ivey RG , Murillo OD , Hosseini N , Song X , Petralia F , Calinawan A , Savage SR , Berry AB , Reva B , Ozbek U , Krek A , Ma W , da Veiga Leprevost F , Ji J , Yoo S , Lin C , Voytovich UJ , Huang Y , Lee SH , Bergan L , Lorentzen TD , Mesri M , Rodriguez H , Hoofnagle AN , Herbert ZT , Nesvizhskii AI , Zhang B , Whiteaker JR , Fenyo D , McKerrow W , Wang J , Schürer SC , Stathias V , Chen XS , Barcellos-Hoff MH , Starr TK , Winterhoff BJ , Nelson AC , Mok SC , Kaufmann SH , Drescher C , Cieslik M , Wang P , Birrer MJ , Paulovich AG . Proteogenomic analysis of chemo-refractory high-grade serous ovarian cancer. Cell 2023; 186(16): 3476–3498.e35

[97]

Zhang H , Bai L , Wu XQ , Tian X , Feng J , Wu X , Shi GH , Pei X , Lyu J , Yang G , Liu Y , Xu W , Anwaier A , Zhu Y , Cao DL , Xu F , Wang Y , Gan HL , Sun MH , Zhao JY , Qu Y , Ye D , Ding C . Proteogenomics of clear cell renal cell carcinoma response to tyrosine kinase inhibitor. Nat Commun 2023; 14(1): 4274

[98]

Shi W , Wang Y , Xu C , Li Y , Ge S , Bai B , Zhang K , Wang Y , Zheng N , Wang J , Wang S , Ji G , Li J , Nie Y , Liang W , Wu X , Cui J , Wang Y , Chen L , Zhao Q , Shen L , He F , Qin J , Ding C . Multilevel proteomic analyses reveal molecular diversity between diffuse-type and intestinal-type gastric cancer. Nat Commun 2023; 14(1): 835

[99]

Cho SY , Hwang H , Kim YH , Yoo BC , Han N , Kong SY , Baek MJ , Kim KH , Lee MR , Park JG , Han SS , Lee WJ , Park C , Park JB , Kim JY , Park SJ , Woo SM . Refining classification of cholangiocarcinoma subtypes via proteogenomic integration reveals new therapeutic prospects. Gastroenterology 2023; 164(7): 1293–1309

[100]

Thingholm TE , Larsen MR . Phosphopeptide enrichment by immobilized metal affinity chromatography. Methods Mol Biol 2016; 1355: 123–133

[101]

Ruprecht B , Koch H , Medard G , Mundt M , Kuster B , Lemeer S . Comprehensive and reproducible phosphopeptide enrichment using iron immobilized metal ion affinity chromatography (Fe-IMAC) columns. Mol Cell Proteomics 2015; 14(1): 205–215

[102]

Cantin GT , Shock TR , Park SK , Madhani HD , Yates JR 3rd . Optimizing TiO2-based phosphopeptide enrichment for automated multidimensional liquid chromatography coupled to tandem mass spectrometry. Anal Chem 2007; 79(12): 4666–4673

[103]

Matheron L , van den Toorn H , Heck AJ , Mohammed S . Characterization of biases in phosphopeptide enrichment by Ti4+-immobilized metal affinity chromatography and TiO2 using a massive synthetic library and human cell digests. Anal Chem 2014; 86(16): 8312–8320

[104]

Yue X , Schunter A , Hummon AB . Comparing multistep immobilized metal affinity chromatography and multistep TiO2 methods for phosphopeptide enrichment. Anal Chem 2015; 87(17): 8837–8844

[105]

Yu YQ , Fournier J , Gilar M , Gebler JC . Phosphopeptide enrichment using microscale titanium dioxide solid phase extraction. J Sep Sci 2009; 32(8): 1189–1199

[106]

Yu LR , Veenstra T . Phosphopeptide enrichment using offline titanium dioxide columns for phosphoproteomics. Methods Mol Biol 2013; 1002: 93–103

[107]

Labots M , van der Mijn JC , Beekhof R , Piersma SR , de Goeij-de Haas RR , Pham TV , Knol JC , Dekker H , van Grieken NCT , Verheul HMW , Jiménez CR . Phosphotyrosine-based-phosphoproteomics scaled-down to biopsy level for analysis of individual tumor biology and treatment selection. J Proteomics 2017; 162: 99–107

[108]

Bergström Lind S , Molin M , Savitski MM , Emilsson L , Aström J , Hedberg L , Adams C , Nielsen ML , Engström A , Elfineh L , Andersson E , Zubarev RA , Pettersson U . Immunoaffinity enrichments followed by mass spectrometric detection for studying global protein tyrosine phosphorylation. J Proteome Res 2008; 7(7): 2897–2910

[109]

Zou L , Wang Y , Wang X , Yang X , Zhang Q , Zheng Q . Stable isotope labeling-based two-step derivatization strategy for analysis of phosphopeptides. J Proteomics 2024; 297: 105128

[110]

Yang SS , Chang YJ , Zhang H , Yu X , Shang W , Chen GQ , Chen DDY , Gu ZY . Enrichment of phosphorylated peptides with metal-organic framework nanosheets for serum profiling of diabetes and phosphoproteomics analysis. Anal Chem 2018; 90(22): 13796–13805

[111]

Jiang D , Wu S , Li Y , Qi R , Liu J . Cobalt phthalocyanine-modified magnetic metal-organic frameworks for specific enrichment of phosphopeptides. ACS Biomater Sci Eng 2024; 10(6): 3739–3746

[112]

Liu M , Torsetnes SB , Wierzbicka C , Jensen ON , Sellergren B , Irgum K . Selective enrichment of phosphorylated peptides by monolithic polymers surface imprinted with bis-imidazolium moieties by UV-initiated cryopolymerization. Anal Chem 2019; 91(15): 10188–10196

[113]

Qiu W , Evans CA , Landels A , Pham TK , Wright PC . Phosphopeptide enrichment for phosphoproteomic analysis—a tutorial and review of novel materials. Anal Chim Acta 2020; 1129: 158–180

[114]

Shang S , Liu J , Hua F . Protein acylation: mechanisms, biological functions and therapeutic targets. Signal Transduct Target Ther 2022; 7(1): 396

[115]

Diallo I , Seve M , Cunin V , Minassian F , Poisson JF , Michelland S , Bourgoin-Voillard S . Current trends in protein acetylation analysis. Expert Rev Proteomics 2019; 16(2): 139–159

[116]

Yu J , Gui X , Zou Y , Liu Q , Yang Z , An J , Guo X , Wang K , Guo J , Huang M , Zhou S , Zuo J , Chen Y , Deng L , Yuan G , Li N , Song Y , Jia J , Zeng J , Zhao Y , Liu X , Du X , Liu Y , Wang P , Zhang B , Ding L , Robles AI , Rodriguez H , Zhou H , Shao Z , Wu L , Gao D . A proteogenomic analysis of cervical cancer reveals therapeutic and biological insights. Nat Commun 2024; 15(1): 10114

[117]

Svinkina T , Gu H , Silva JC , Mertins P , Qiao J , Fereshetian S , Jaffe JD , Kuhn E , Udeshi ND , Carr SA . Deep, quantitative coverage of the lysine acetylome using novel anti-acetyl-lysine antibodies and an optimized proteomic workflow. Mol Cell Proteomics 2015; 14(9): 2429–2440

[118]

Gritsenko MA , Tsai CF , Kim H , Liu T . Automated immunoprecipitation workflow for comprehensive acetylome analysis. Methods Mol Biol 2024; 2823: 173–191

[119]

Xu W , Zhao S . Generation and characterization of pan-specific anti-acetyllysine antibody. Methods Mol Biol 2013; 981: 137–150

[120]

Deng L , Meng T , Chen L , Wei W , Wang P . The role of ubiquitination in tumorigenesis and targeted drug discovery. Signal Transduct Target Ther 2020; 5(1): 11

[121]

Steger M , Karayel Ö , Demichev V . Ubiquitinomics: History, methods, and applications in basic research and drug discovery. Proteomics 2022; 22(15-16): e2200074

[122]

Sahu I , Zhu H , Buhrlage SJ , Marto JA . Proteomic approaches to study ubiquitinomics. Biochim Biophys Acta Gene Regul Mech 2023; 1866(2): 194940

[123]

Xu G , Paige JS , Jaffrey SR . Global analysis of lysine ubiquitination by ubiquitin remnant immunoaffinity profiling. Nat Biotechnol 2010; 28(8): 868–873

[124]

Akimov V , Barrio-Hernandez I , Hansen SVF , Hallenborg P , Pedersen AK , Bekker-Jensen DB , Puglia M , Christensen SDK , Vanselow JT , Nielsen MM , Kratchmarova I , Kelstrup CD , Olsen JV , Blagoev B . UbiSite approach for comprehensive mapping of lysine and N-terminal ubiquitination sites. Nat Struct Mol Biol 2018; 25(7): 631–640

[125]

Davies CW , Vidal SE , Phu L , Sudhamsu J , Hinkle TB , Chan Rosenberg S , Schumacher FR , Zeng YJ , Schwerdtfeger C , Peterson AS , Lill JR , Rose CM , Shaw AS , Wertz IE , Kirkpatrick DS , Koerber JT . Antibody toolkit reveals N-terminally ubiquitinated substrates of UBE2W. Nat Commun 2021; 12(1): 4608

[126]

Stes E , Laga M , Walton A , Samyn N , Timmerman E , De Smet I , Goormachtig S , Gevaert K . A COFRADIC protocol to study protein ubiquitination. J Proteome Res 2014; 13(6): 3107–3113

[127]

Hart GW , Copeland RJ . Glycomics hits the big time. Cell 2010; 143(5): 672–676

[128]

Vajaria BN , Patel PS . Glycosylation: a hallmark of cancer. Glycoconj J 2017; 34(2): 147–156

[129]

Xu S , Xu X , Wu R . Deciphering the properties and functions of glycoproteins using quantitative proteomics. J Proteome Res 2023; 22(6): 1571–1588

[130]

Dong W , Chen L , Jia L , Chen Z , Shen J , Li P , Sun S . Maximal performance of intact N-glycopeptide enrichment using sequential HILIC and MAX columns. Anal Bioanal Chem 2023; 415(26): 6431–6439

[131]

Yang W , Shah P , Hu Y , Toghi Eshghi S , Sun S , Liu Y , Zhang H . Comparison of enrichment methods for intact N- and O-linked glycopeptides using strong anion exchange and hydrophilic interaction liquid chromatography. Anal Chem 2017; 89(21): 11193–11197

[132]

Mun DG , Bhin J , Kim S , Kim H , Jung JH , Jung Y , Jang YE , Park JM , Kim H , Jung Y , Lee H , Bae J , Back S , Kim SJ , Kim J , Park H , Li H , Hwang KB , Park YS , Yook JH , Kim BS , Kwon SY , Ryu SW , Park DY , Jeon TY , Kim DH , Lee JH , Han SU , Song KS , Park D , Park JW , Rodriguez H , Kim J , Lee H , Kim KP , Yang EG , Kim HK , Paek E , Lee S , Lee SW , Hwang D . Proteogenomic characterization of human early-onset gastric cancer. Cancer Cell 2019; 35(1): 111–124.e10

[133]

Li H , Sun L , Gao P , Hu H . Lactylation in cancer: current understanding and challenges. Cancer Cell 2024; 42(11): 1803–1807

[134]

Chen J , Huang Z , Chen Y , Tian H , Chai P , Shen Y , Yao Y , Xu S , Ge S , Jia R . Lactate and lactylation in cancer. Signal Transduct Target Ther 2025; 10(1): 38

[135]

Yang Z , Yan C , Ma J , Peng P , Ren X , Cai S , Shen X , Wu Y , Zhang S , Wang X , Qiu S , Zhou J , Fan J , Huang H , Gao Q . Lactylome analysis suggests lactylation-dependent mechanisms of metabolic adaptation in hepatocellular carcinoma. Nat Metab 2023; 5(1): 61–79

[136]

Duan Y , Zhan H , Wang Q , Li B , Gao H , Liu D , Xu Q , Gao X , Liu Z , Gao P , Wei G , Wang Y . Integrated lactylome characterization reveals the molecular dynamics of protein regulation in gastrointestinal cancers. Adv Sci (Weinh) 2024; 11(35): e2400227

[137]

Yang J , Yu X , Xiao M , Xu H , Tan Z , Lei Y , Guo Y , Wang W , Xu J , Shi S , Yu X . Histone lactylation-driven feedback loop modulates cholesterol-linked immunosuppression in pancreatic cancer. Gut 2025; 74(11): 1859–1872

[138]

Chen YJ , Roumeliotis TI , Chang YH , Chen CT , Han CL , Lin MH , Chen HW , Chang GC , Chang YL , Wu CT , Lin MW , Hsieh MS , Wang YT , Chen YR , Jonassen I , Ghavidel FZ , Lin ZS , Lin KT , Chen CW , Sheu PY , Hung CT , Huang KC , Yang HC , Lin PY , Yen TC , Lin YW , Wang JH , Raghav L , Lin CY , Chen YS , Wu PS , Lai CT , Weng SH , Su KY , Chang WH , Tsai PY , Robles AI , Rodriguez H , Hsiao YJ , Chang WH , Sung TY , Chen JS , Yu SL , Choudhary JS , Chen HY , Yang PC , Chen YJ . Proteogenomics of non-smoking lung cancer in East Asia delineates molecular signatures of pathogenesis and progression. Cell 2020; 182(1): 226–244.e17

[139]

Petralia F , Tignor N , Reva B , Koptyra M , Chowdhury S , Rykunov D , Krek A , Ma W , Zhu Y , Ji J , Calinawan A , Whiteaker JR , Colaprico A , Stathias V , Omelchenko T , Song X , Raman P , Guo Y , Brown MA , Ivey RG , Szpyt J , Guha Thakurta S , Gritsenko MA , Weitz KK , Lopez G , Kalayci S , Gümüş ZH , Yoo S , da Veiga Leprevost F , Chang HY , Krug K , Katsnelson L , Wang Y , Kennedy JJ , Voytovich UJ , Zhao L , Gaonkar KS , Ennis BM , Zhang B , Baubet V , Tauhid L , Lilly JV , Mason JL , Farrow B , Young N , Leary S , Moon J , Petyuk VA , Nazarian J , Adappa ND , Palmer JN , Lober RM , Rivero-Hinojosa S , Wang LB , Wang JM , Broberg M , Chu RK , Moore RJ , Monroe ME , Zhao R , Smith RD , Zhu J , Robles AI , Mesri M , Boja E , Hiltke T , Rodriguez H , Zhang B , Schadt EE , Mani DR , Ding L , Iavarone A , Wiznerowicz M , Schürer S , Chen XS , Heath AP , Rokita JL , Nesvizhskii AI , Fenyö D , Rodland KD , Liu T , Gygi SP , Paulovich AG , Resnick AC , Storm PB , Rood BR , Wang P; Children’s Brain Tumor Network; Clinical Proteomic Tumor Analysis Consortium . Integrated proteogenomic characterization across major histological types of pediatric brain cancer. Cell 2020; 183(7): 1962–1985.e31

[140]

Dong L , Lu D , Chen R , Lin Y , Zhu H , Zhang Z , Cai S , Cui P , Song G , Rao D , Yi X , Wu Y , Song N , Liu F , Zou Y , Zhang S , Zhang X , Wang X , Qiu S , Zhou J , Wang S , Zhang X , Shi Y , Figeys D , Ding L , Wang P , Zhang B , Rodriguez H , Gao Q , Gao D , Zhou H , Fan J . Proteogenomic characterization identifies clinically relevant subgroups of intrahepatic cholangiocarcinoma. Cancer Cell 2022; 40(1): 70–87.e15

[141]

Dong B , Xu JY , Huang Y , Guo J , Dong Q , Wang Y , Li N , Liu Q , Zhang M , Pan Q , Wang H , Jiang J , Chen B , Shen D , Ma Y , Zhai L , Zhang J , Li J , Xue W , Tan M , Qin J . Integrative proteogenomic profiling of high-risk prostate cancer samples from Chinese patients indicates metabolic vulnerabilities and diagnostic biomarkers. Nat Cancer 2024; 5(9): 1427–1447

[142]

Zhang Q , Xu X , Jiang D , Wang Y , Wang H , Zhu J , Tang S , Wang R , Zhao S , Li K , Feng J , Xiang H , Yao Z , Xu N , Fang R , Guo W , Liu Y , Hou Y , Ding C . Integrated proteogenomic characterization of ampullary adenocarcinoma. Cell Discov 2025; 11(1): 2

[143]

Qin Z , Jiang D , Yu Z , Li L , Xu W , Xu C , Song Q , Sun X , Li L , Guo W , Pu Y , Feng J , Liu Y , Wang H , Wang L , Qu Y , He F , Qin J , Tan L , Zhao JY , Yang W , Hou Y , Ding C . Proteogenomic characterization reveals that lipid droplet formation promotes esophageal squamous cell cancer progression. Sci Transl Med 2025; 17(802): eadt0214

[144]

Jayavelu AK , Wolf S , Buettner F , Alexe G , Häupl B , Comoglio F , Schneider C , Doebele C , Fuhrmann DC , Wagner S , Donato E , Andresen C , Wilke AC , Zindel A , Jahn D , Splettstoesser B , Plessmann U , Münch S , Abou-El-Ardat K , Makowka P , Acker F , Enssle JC , Cremer A , Schnütgen F , Kurrle N , Chapuy B , Löber J , Hartmann S , Wild PJ , Wittig I , Hübschmann D , Kaderali L , Cox J , Brüne B , Röllig C , Thiede C , Steffen B , Bornhäuser M , Trumpp A , Urlaub H , Stegmaier K , Serve H , Mann M , Oellerich T . The proteogenomic subtypes of acute myeloid leukemia. Cancer Cell 2022; 40(3): 301–317.e12

[145]

Ramberger E , Sapozhnikova V , Ng YLD , Dolnik A , Ziehm M , Popp O , Sträng E , Kull M , Grünschläger F , Krüger J , Benary M , Müller S , Gao X , Murgai A , Haji M , Schmidt A , Lutz R , Nogai A , Braune J , Laue D , Langer C , Khandanpour C , Bassermann F , Döhner H , Engelhardt M , Straka C , Hundemer M , Beule D , Haas S , Keller U , Einsele H , Bullinger L , Knop S , Mertins P , Krönke J . The proteogenomic landscape of multiple myeloma reveals insights into disease biology and therapeutic opportunities. Nat Cancer 2024; 5(8): 1267–1284

[146]

Yoon KA , Kim Y , Jung SY , Ryu JS , Kim KH , Lee EG , Chae H , Kwon Y , Kim J , Park JB , Kong SY . Proteogenomic analysis dissects early-onset breast cancer patients with prognostic relevance. Exp Mol Med 2024; 56(11): 2382–2394

[147]

Jaehnig EJ , Fernandez-Martinez A , Vashist TD , Holt MV , Williams L , Lei JT , Moon CI , Kim BJ , Dou Y , Zhao H , Korchina V , Gibbs RA , Muzny DM , Doddapaneni H , Perou CM , Carey LA , Robles AI , Hyslop T , Wen Y , McCart L , Krek A , Petralia F , Miles G , Kavuri SM , Gillette MA , Mani DR , Carr SA , Zhang B , Ellis MJ , Satpathy S , Anurag M . Proteogenomic analysis of the CALGB 40601 (Alliance) HER2+ breast cancer neoadjuvant trial reveals resistance biomarkers. Cell Rep Med 2025; 6(6): 102154

[148]

Xu G , Yu J , Lyu J , Zhan M , Xu J , Huang M , Zhao R , Li Y , Zhu J , Feng J , Tan S , Ran P , Su Z , Liu X , Zhao J , Zhang H , Xu C , Chang J , Hou Y , Ding C . Proteogenomic landscape of breast ductal carcinoma reveals tumor progression characteristics and therapeutic targets. Adv Sci (Weinh) 2024; 11(46): e2401041

[149]

Hyeon DY , Nam D , Shin HJ , Jeong J , Jung E , Cho SY , Shin DH , Ku JL , Baek HJ , Yoo CW , Hong EK , Lim MC , Lee SJ , Bae YK , Kim JK , Bae J , Choi W , Kim SJ , Back S , Kang C , Madar IH , Kim H , Kim S , Kim DK , Kang J , Park GW , Park KS , Shin Y , Kim SS , Jung K , Hwang D , Lee SW , Kim JY . Proteogenomic characterization of molecular and cellular targets for treatment-resistant subtypes in locally advanced cervical cancers. Mol Cancer 2025; 24(1): 77

[150]

Deng M , Ran P , Chen L , Wang Y , Yu Z , Cai K , Feng J , Qin Z , Yin Y , Tan S , Liu Y , Xu C , Shi G , Ji Y , Zhao JY , Zhou J , Fan J , Hou Y , Ding C . Proteogenomic characterization of cholangiocarcinoma. Hepatology 2023; 77(2): 411–429

[151]

Qu Y , Pei X , Feng J , Yan X , Zhang L , Wang J , Yao X , Bian J , Gan Y , Gan H , Jiang X , Yang P , Cai M , Li L , Wu X , Jing W , Zhang C , Zhao J , Zhang H , Shi G , Zhou X , Ye D , Ding C . Proteogenomic analysis identifies clinically relevant subgroups of collecting duct carcinoma. Research (Wash D C) 2025; 8: 0859

[152]

Yanovich-Arad G , Ofek P , Yeini E , Mardamshina M , Danilevsky A , Shomron N , Grossman R , Satchi-Fainaro R , Geiger T . Proteogenomics of glioblastoma associates molecular patterns with survival. Cell Rep 2021; 34(9): 108787

[153]

Wang Y , Luo R , Zhang X , Xiang H , Yang B , Feng J , Deng M , Ran P , Sujie A , Zhang F , Zhu J , Tan S , Xie T , Chen P , Yu Z , Li Y , Jiang D , Zhang X , Zhao JY , Hou Y , Ding C . Proteogenomics of diffuse gliomas reveal molecular subtypes associated with specific therapeutic targets and immune-evasion mechanisms. Nat Commun 2023; 14(1): 505

[154]

Liu Z , Wu Y , Xu H , Wang M , Weng S , Pei D , Chen S , Wang W , Yan J , Cui L , Duan J , Zhao Y , Wang Z , Ma Z , Li R , Duan W , Qiu Y , Su D , Li S , Liu H , Li W , Ma C , Yu M , Yu Y , Chen T , Fu J , Zhen Y , Yu B , Ji Y , Zheng H , Liang D , Liu X , Yan D , Han X , Wang F , Li ZC , Zhang Z . Multimodal fusion of radio-pathology and proteogenomics identify integrated glioma subtypes with prognostic and therapeutic opportunities. Nat Commun 2025; 16(1): 3510

[155]

Stewart PA , Welsh EA , Slebos RJC , Fang B , Izumi V , Chambers M , Zhang G , Cen L , Pettersson F , Zhang Y , Chen Z , Cheng CH , Thapa R , Thompson Z , Fellows KM , Francis JM , Saller JJ , Mesa T , Zhang C , Yoder S , DeNicola GM , Beg AA , Boyle TA , Teer JK , Ann Chen Y , Koomen JM , Eschrich SA , Haura EB . Proteogenomic landscape of squamous cell lung cancer. Nat Commun 2019; 10(1): 3578

[156]

Zhang H , Liu C , Wang S , Wang Q , Feng X , Jiang H , Xiao L , Luo C , Zhang L , Hou F , Zhou M , Deng Z , Li H , Zhang Y , Su X , Li G . Proteogenomic analysis of air-pollution-associated lung cancer reveals prevention and therapeutic opportunities. eLife 2024; 13: RP95453

[157]

Su H , Chen L , Wu J , Cheng Z , Li J , Ren Y , Xu J , Dang Y , Zheng M , Cao Y , Gao J , Dai C , Hu X , Xie H , Chen J , Luo T , Zhu J , Wu C , Sha W , Chen C , Liu H . Proteogenomic characterization reveals tumorigenesis and progression of lung cancer manifested as subsolid nodules. Nat Commun 2025; 16(1): 2414

[158]

Zhang Z , Wu X , Bao S , Sun X , Yang F , Zhang Y , Yang Z , Zhang L , Chen R , Xing P , Li J , Zhou M , Yang L . Proteogenomic characterization of high-grade lung neuroendocrine carcinoma deciphers molecular diversity and potential biomarkers of different histological subtypes in Chinese population. Research (Wash D C) 2025; 8: 0671

[159]

Wu CS , Li HP , Hsieh CH , Lin YT , Yi-Feng Chang I , Chung AK , Huang Y , Ueng SH , Hsiao YC , Chien KY , Luo JD , Chen CH , Liao WC , Hung JL , Yuan SN , OuYang CN , Chiang WF , Chien CY , Chuang HC , Chu LJ , Liu H , Yang CY , Robles AI , Rodriguez H , Lin HH , Yang HY , Hsueh C , Chang KP , Yu JS , Chang YS . Integrated multi-omics analyses of oral squamous cell carcinoma reveal precision patient stratification and personalized treatment strategies. Cancer Lett 2025; 614: 217482

[160]

Wang Z , Yu H , Bao W , Qu M , Wang Y , Zhang L , Liu X , Liu C , He M , Li J , Dong Z , Zhang Y , Yang B , Hou J , Xu C , Wang L , Li X , Gao X , Yang C . Proteomic and phosphoproteomic landscape of localized prostate cancer unveils distinct molecular subtypes and insights into precision therapeutics. Proc Natl Acad Sci USA 2024; 121(40): e2402741121

[161]

Ou W , Zhang XX , Li B , Tuo Y , Lin RX , Liu PF , Guo JP , Un HC , Li MH , Lei JH , Gao XJ , Zheng FF , Chen LW , Long LL , Wang ZR . Integrated proteogenomic characterization of localized prostate cancer identifies biological insights and subtype-specific therapeutic strategies. Nat Commun 2025; 16(1): 3189

[162]

Hyeon DY , Nam D , Han Y , Kim DK , Kim G , Kim D , Bae J , Back S , Mun DG , Madar IH , Lee H , Kim SJ , Kim H , Hyun S , Kim CR , Choi SA , Kim YR , Jeong J , Jeon S , Choo YW , Lee KB , Kwon W , Choi S , Goo T , Park T , Suh YA , Kim H , Ku JL , Kim MS , Paek E , Park D , Jung K , Baek SH , Jang JY , Hwang D , Lee SW . Proteogenomic landscape of human pancreatic ductal adenocarcinoma in an Asian population reveals tumor cell-enriched and immune-rich subtypes. Nat Cancer 2023; 4(2): 290–307

[163]

Tong Y , Sun M , Chen L , Wang Y , Li Y , Li L , Zhang X , Cai Y , Qie J , Pang Y , Xu Z , Zhao J , Zhang X , Liu Y , Tian S , Qin Z , Feng J , Zhang F , Zhu J , Xu Y , Lou W , Ji Y , Zhao J , He F , Hou Y , Ding C . Proteogenomic insights into the biology and treatment of pancreatic ductal adenocarcinoma. J Hematol Oncol 2022; 15(1): 168

[164]

Ji S , Cao L , Gao J , Du Y , Ye Z , Lou X , Liu F , Zhang Y , Xu J , Shi X , Wang H , Li P , Li Y , Chen H , Yang Z , Gao S , Zhang W , Huang D , Ni S , Wei M , Wang F , Wang Y , Ding T , Jing D , Fan G , Gong Z , Lu R , Qin Y , Chen J , Xu X , Wang P , Zhang B , Ding L , Robles AI , Rodriguez H , Chang DK , Hruban RH , Gao D , Gao D , Jin G , Zhou H , Wu J , Yu X . Proteogenomic characterization of non-functional pancreatic neuroendocrine tumors unravels clinically relevant subgroups. Cancer Cell 2025; 43(4): 776–796.e14

[165]

Zhang F , Zhang Q , Zhu J , Yao B , Ma C , Qiao N , He S , Ye Z , Wang Y , Han R , Feng J , Wang Y , Qin Z , Ma Z , Li K , Zhang Y , Tian S , Chen Z , Tan S , Wu Y , Ran P , Wang Y , Ding C , Zhao Y . Integrated proteogenomic characterization across major histological types of pituitary neuroendocrine tumors. Cell Res 2022; 32(12): 1047–1067

[166]

Zhang Q , Xu Z , Han R , Wang Y , Ye Z , Zhu J , Cai Y , Zhang F , Zhao J , Yao B , Qin Z , Qiao N , Huang R , Feng J , Wang Y , Rui W , He F , Zhao Y , Ding C . Proteogenomic characterization of skull-base chordoma. Nat Commun 2024; 15(1): 8338

[167]

Pan Z , Tan Z , Xu N , Yao Z , Zheng C , Shang J , Xie L , Xu J , Wang J , Jiang L , Zhu X , Yu D , Li Y , Che Y , Gong Y , Qin Z , Zhang Y , Zou X , Xu T , Guo Z , Jin T , Guo T , Wang W , Chen W , Sun Y , Wang W , Peng X , Yin C , Ding C , Huang P , Ge M . Integrative proteogenomic characterization reveals therapeutic targets in poorly differentiated and anaplastic thyroid cancers. Nat Commun 2025; 16(1): 3601

[168]

Shi X , Sun Y , Shen C , Zhang Y , Shi R , Zhang F , Liao T , Lv G , Zhu Z , Jiao L , Li P , Xu T , Qu N , Huang N , Hu J , Zhang T , Gu Y , Qin G , Guan H , Pu W , Li Y , Geng X , Zhang Y , Chen T , Huang S , Zhang Z , Ge S , Wang W , Xu W , Yu P , Lu Z , Wang Y , Guo L , Wang Y , Guo T , Ji Q , Wei W . Integrated proteogenomic characterization of medullary thyroid carcinoma. Cell Discov 2022; 8(1): 120

[169]

Yao Z , Xu N , Shang G , Wang H , Tao H , Wang Y , Qin Z , Tan S , Feng J , Zhu J , Ma F , Tian S , Zhang Q , Qu Y , Hou J , Guo J , Zhao J , Hou Y , Ding C . Proteogenomics of different urothelial bladder cancer stages reveals distinct molecular features for papillary cancer and carcinoma in situ. Nat Commun 2023; 14(1): 5670

[170]

Cheng C , Zhang L , Chang X , Chen K , He T , Shi J , Lv F , Pan L , Wu Y , Cheng Q , Ren D , Guo Y , Zhang W , Wang H , Shi T , Li J , Ni X , Wu Y , Jin Y , Wu Z . Integrative proteogenomic characterization of Wilms tumor. Nat Commun 2025; 16(1): 7715

[171]

Gaujoux R , Seoighe C . A flexible R package for nonnegative matrix factorization. BMC Bioinformatics 2010; 11(1): 367

[172]

Yuan Y , Van Allen EM , Omberg L , Wagle N , Amin-Mansour A , Sokolov A , Byers LA , Xu Y , Hess KR , Diao L , Han L , Huang X , Lawrence MS , Weinstein JN , Stuart JM , Mills GB , Garraway LA , Margolin AA , Getz G , Liang H . Assessing the clinical utility of cancer genomic and proteomic data across tumor types. Nat Biotechnol 2014; 32(7): 644–652

[173]

Wang J , Mouradov D , Wang X , Jorissen RN , Chambers MC , Zimmerman LJ , Vasaikar S , Love CG , Li S , Lowes K , Leuchowius KJ , Jousset H , Weinstock J , Yau C , Mariadason J , Shi Z , Ban Y , Chen X , Coffey RJC , Slebos RJC , Burgess AW , Liebler DC , Zhang B , Sieber OM . Colorectal cancer cell line proteomes are representative of primary tumors and predict drug sensitivity. Gastroenterology 2017; 153(4): 1082–1095

[174]

Schneider JL , Lin JJ , Shaw AT . ALK-positive lung cancer: a moving target. Nat Cancer 2023; 4(3): 330–343

[175]

Farshidfar F , Zheng S , Gingras MC , Newton Y , Shih J , Robertson AG , Hinoue T , Hoadley KA , Gibb EA , Roszik J , Covington KR , Wu CC , Shinbrot E , Stransky N , Hegde A , Yang JD , Reznik E , Sadeghi S , Pedamallu CS , Ojesina AI , Hess JM , Auman JT , Rhie SK , Bowlby R , Borad MJ; Cancer Genome Atlas Network; Zhu AX , Stuart JM , Sander C , Akbani R , Cherniack AD , Deshpande V , Mounajjed T , Foo WC , Torbenson MS , Kleiner DE , Laird PW , Wheeler DA , McRee AJ , Bathe OF , Andersen JB , Bardeesy N , Roberts LR , Kwong LN . Integrative genomic analysis of cholangiocarcinoma identifies distinct IDH-mutant molecular profiles. Cell Rep 2017; 19(13): 2878–2880

[176]

Karremann M , Gielen GH , Hoffmann M , Wiese M , Colditz N , Warmuth-Metz M , Bison B , Claviez A , van Vuurden DG , von Bueren AO , Gessi M , Kühnle I , Hans VH , Benesch M , Sturm D , Kortmann RD , Waha A , Pietsch T , Kramm CM . Diffuse high-grade gliomas with H3 K27M mutations carry a dismal prognosis independent of tumor location. Neuro-oncol 2018; 20(1): 123–131

[177]

Jiang Y , Sun A , Zhao Y , Ying W , Sun H , Yang X , Xing B , Sun W , Ren L , Hu B , Li C , Zhang L , Qin G , Zhang M , Chen N , Zhang M , Huang Y , Zhou J , Zhao Y , Liu M , Zhu X , Qiu Y , Sun Y , Huang C , Yan M , Wang M , Liu W , Tian F , Xu H , Zhou J , Wu Z , Shi T , Zhu W , Qin J , Xie L , Fan J , Qian X , He F; Chinese Human Proteome Project (CNHPP) Consortium . Proteomics identifies new therapeutic targets of early-stage hepatocellular carcinoma. Nature 2019; 567(7747): 257–261

[178]

Chen F , Zhang Y , Gibbons DL , Deneen B , Kwiatkowski DJ , Ittmann M , Creighton CJ . Pan-cancer molecular classes transcending tumor lineage across 32 cancer types, multiple data platforms, and over 10, 000 cases. Clin Cancer Res 2018; 24(9): 2182–2193

[179]

Chen F , Chandrashekar DS , Varambally S , Creighton CJ . Pan-cancer molecular subtypes revealed by mass-spectrometry-based proteomic characterization of more than 500 human cancers. Nat Commun 2019; 10(1): 5679

[180]

Zhang Y , Chen F , Chandrashekar DS , Varambally S , Creighton CJ . Proteogenomic characterization of 2002 human cancers reveals pan-cancer molecular subtypes and associated pathways. Nat Commun 2022; 13(1): 2669

[181]

Li Y , Porta-Pardo E , Tokheim C , Bailey MH , Yaron TM , Stathias V , Geffen Y , Imbach KJ , Cao S , Anand S , Akiyama Y , Liu W , Wyczalkowski MA , Song Y , Storrs EP , Wendl MC , Zhang W , Sibai M , Ruiz-Serra V , Liang WW , Terekhanova NV , Rodrigues FM , Clauser KR , Heiman DI , Zhang Q , Aguet F , Calinawan AP , Dhanasekaran SM , Birger C , Satpathy S , Zhou DC , Wang LB , Baral J , Johnson JL , Huntsman EM , Pugliese P , Colaprico A , Iavarone A , Chheda MG , Ricketts CJ , Fenyö D , Payne SH , Rodriguez H , Robles AI , Gillette MA , Kumar-Sinha C , Lazar AJ , Cantley LC , Getz G , Ding L; Clinical Proteomic Tumor Analysis Consortium . Pan-cancer proteogenomics connects oncogenic drivers to functional states. Cell 2023; 186(18): 3921–3944.e25

[182]

Bagaev A , Kotlov N , Nomie K , Svekolkin V , Gafurov A , Isaeva O , Osokin N , Kozlov I , Frenkel F , Gancharova O , Almog N , Tsiper M , Ataullakhanov R , Fowler N . Conserved pan-cancer microenvironment subtypes predict response to immunotherapy. Cancer Cell 2021; 39(6): 845–865.e7

[183]

Petralia F , Ma W , Yaron TM , Caruso FP , Tignor N , Wang JM , Charytonowicz D , Johnson JL , Huntsman EM , Marino GB , Calinawan A , Evangelista JE , Selvan ME , Chowdhury S , Rykunov D , Krek A , Song X , Turhan B , Christianson KE , Lewis DA , Deng EZ , Clarke DJB , Whiteaker JR , Kennedy JJ , Zhao L , Segura RL , Batra H , Raso MG , Parra ER , Soundararajan R , Tang X , Li Y , Yi X , Satpathy S , Wang Y , Wiznerowicz M , González-Robles TJ , Iavarone A , Gosline SJC , Reva B , Robles AI , Nesvizhskii AI , Mani DR , Gillette MA , Klein RJ , Cieslik M , Zhang B , Paulovich AG , Sebra R , Gümüş ZH , Hostetter G , Fenyö D , Omenn GS , Cantley LC , Ma'ayan A , Lazar AJ , Ceccarelli M , Wang P; Clinical Proteomic Tumor Analysis Consortium . Pan-cancer proteogenomics characterization of tumor immunity. Cell 2024; 187(5): 1255–1277.e27

[184]

Zhang Z , Chen L , Chen H , Zhao J , Li K , Sun J , Zhou M . Pan-cancer landscape of T-cell exhaustion heterogeneity within the tumor microenvironment revealed a progressive roadmap of hierarchical dysfunction associated with prognosis and therapeutic efficacy. EBioMedicine 2022; 83: 104207

[185]

Sheng D , Jin C , Yue K , Yue M , Liang Y , Xue X , Li P , Zhao G , Zhang L . Pan-cancer atlas of tumor-resident microbiome, immunity and prognosis. Cancer Lett 2024; 598: 217077

[186]

Geffen Y , Anand S , Akiyama Y , Yaron TM , Song Y , Johnson JL , Govindan A , Babur Ö , Li Y , Huntsman E , Wang LB , Birger C , Heiman DI , Zhang Q , Miller M , Maruvka YE , Haradhvala NJ , Calinawan A , Belkin S , Kerelsky A , Clauser KR , Krug K , Satpathy S , Payne SH , Mani DR , Gillette MA , Dhanasekaran SM , Thiagarajan M , Mesri M , Rodriguez H , Robles AI , Carr SA , Lazar AJ , Aguet F , Cantley LC , Ding L , Getz G; Clinical Proteomic Tumor Analysis Consortium . Pan-cancer analysis of post-translational modifications reveals shared patterns of protein regulation. Cell 2023; 186(18): 3945–3967.e26

[187]

Elmas A , Tharakan S , Jaladanki S , Galsky MD , Liu T , Huang KL . Pan-cancer proteogenomic investigations identify post-transcriptional kinase targets. Commun Biol 2021; 4(1): 1112

[188]

Sengupta S , Sun SQ , Huang KL , Oh C , Bailey MH , Varghese R , Wyczalkowski MA , Ning J , Tripathi P , McMichael JF , Johnson KJ , Kandoth C , Welch J , Ma C , Wendl MC , Payne SH , Fenyö D , Townsend RR , Dipersio JF , Chen F , Ding L . Integrative omics analyses broaden treatment targets in human cancer. Genome Med 2018; 10(1): 60

[189]

Zhou Y , Lih TM , Pan J , Höti N , Dong M , Cao L , Hu Y , Cho KC , Chen SY , Eguez RV , Gabrielson E , Chan DW , Zhang H , Li QK . Proteomic signatures of 16 major types of human cancer reveal universal and cancer-type-specific proteins for the identification of potential therapeutic targets. J Hematol Oncol 2020; 13(1): 170

[190]

Savage SR , Yi X , Lei JT , Wen B , Zhao H , Liao Y , Jaehnig EJ , Somes LK , Shafer PW , Lee TD , Fu Z , Dou Y , Shi Z , Gao D , Hoyos V , Gao Q , Zhang B . Pan-cancer proteogenomics expands the landscape of therapeutic targets. Cell 2024; 187(16): 4389–4407.e15

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