Human pangenome: far-reaching implications in precision medicine

Yingyan Yu, Hongzhuan Chen

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Front. Med. ›› 2024, Vol. 18 ›› Issue (2) : 403-409. DOI: 10.1007/s11684-023-1039-1
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Human pangenome: far-reaching implications in precision medicine

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Yingyan Yu, Hongzhuan Chen. Human pangenome: far-reaching implications in precision medicine. Front. Med., 2024, 18(2): 403‒409 https://doi.org/10.1007/s11684-023-1039-1

References

[1]
Liao WW, Asri M, Ebler J, Doerr D, Haukness M, Hickey G, Lu S, Lucas JK, Monlong J, Abel HJ, Buonaiuto S, Chang XH, Cheng H, Chu J, Colonna V, Eizenga JM, Feng X, Fischer C, Fulton RS, Garg S, Groza C, Guarracino A, Harvey WT, Heumos S, Howe K, Jain M, Lu TY, Markello C, Martin FJ, Mitchell MW, Munson KM, Mwaniki MN, Novak AM, Olsen HE, Pesout T, Porubsky D, Prins P, Sibbesen JA, Sirén J, Tomlinson C, Villani F, Vollger MR, Antonacci-Fulton LL, Baid G, Baker CA, Belyaeva A, Billis K, Carroll A, Chang PC, Cody S, Cook DE, Cook-Deegan RM, Cornejo OE, Diekhans M, Ebert P, Fairley S, Fedrigo O, Felsenfeld AL, Formenti G, Frankish A, Gao Y, Garrison NA, Giron CG, Green RE, Haggerty L, Hoekzema K, Hourlier T, Ji HP, Kenny EE, Koenig BA, Kolesnikov A, Korbel JO, Kordosky J, Koren S, Lee H, Lewis AP, Magalhães H, Marco-Sola S, Marijon P, McCartney A, McDaniel J, Mountcastle J, Nattestad M, Nurk S, Olson ND, Popejoy AB, Puiu D, Rautiainen M, Regier AA, Rhie A, Sacco S, Sanders AD, Schneider VA, Schultz BI, Shafin K, Smith MW, Sofia HJ, Abou Tayoun AN, Thibaud-Nissen F, Tricomi FF, Wagner J, Walenz B, Wood JMD, Zimin AV, Bourque G, Chaisson MJP, Flicek P, Phillippy AM, Zook JM, Eichler EE, Haussler D, Wang T, Jarvis ED, Miga KH, Garrison E, Marschall T, Hall IM, Li H, Paten B. A draft human pangenome reference. Nature 2023; 617(7960): 312–324
CrossRef Google scholar
[2]
Gao Y, Yang X, Chen H, Tan X, Yang Z, Deng L, Wang B, Kong S, Li S, Cui Y, Lei C, Wang Y, Pan Y, Ma S, Sun H, Zhao X, Shi Y, Yang Z, Wu D, Wu S, Zhao X, Shi B, Jin L, Hu Z, Lu Y, Chu J, Ye K, Xu S. A pangenome reference of 36 Chinese populations. Nature 2023; 619(7968): 112–121
CrossRef Google scholar
[3]
Li R, Li Y, Zheng H, Luo R, Zhu H, Li Q, Qian W, Ren Y, Tian G, Li J, Zhou G, Zhu X, Wu H, Qin J, Jin X, Li D, Cao H, Hu X, Blanche H, Cann H, Zhang X, Li S, Bolund L, Kristiansen K, Yang H, Wang J, Wang J. Building the sequence map of the human pan-genome. Nat Biotechnol 2010; 28(1): 57–63
CrossRef Google scholar
[4]
Watson JD, Crick FH. Molecular structure of nucleic acids; a structure for deoxyribose nucleic acid. Nature 1953; 171(4356): 737–738
CrossRef Google scholar
[5]
Wilkins MH, Stokes AR, Wilson HR. Molecular structure of deoxypentose nucleic acids. Nature 1953; 171(4356): 738–740
CrossRef Google scholar
[6]
Franklin RE, Gosling RG. Molecular configuration in sodium thymonucleate. Nature 1953; 171(4356): 740–741
CrossRef Google scholar
[7]
Attar N. Raymond Gosling: the man who crystallized genes. Genome Biol 2013; 14(4): 402
CrossRef Google scholar
[8]
Edsall JT. Nobel Prize: two Britons, American share 1962 Award for Genetic Code Achievement. Science 1962; 138(3539): 498–500
CrossRef Google scholar
[9]
Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 1977; 74(12): 5463–5467
CrossRef Google scholar
[10]
Olson MV. The human genome project. Proc Natl Acad Sci USA 1993; 90(10): 4338–4344
CrossRef Google scholar
[11]
Chen Z, Zhang S. Chinese Human Genome Project-opportunity and challenge. Chin J Med Genet (Zhonghua YiXue YiChuanXue ZaZhi) 1998; 15(4): 195–197
[12]
Han ZG, Zhao GP, Chen Z. Transcriptome study in China. C R Biol 2003; 326(10–11): 949–957
CrossRef Google scholar
[13]
Collins FS, Morgan M, Patrinos A. The Human Genome Project: lessons from large-scale biology. Science 2003; 300(5617): 286–290
CrossRef Google scholar
[14]
Garver KL, Garver B. The Human Genome Project and eugenic concerns. Am J Hum Genet 1994; 54(1): 148–158
[15]
Jarvie T. Next generation sequencing technologies. Drug Discov Today Technol 2005; 2(3): 255–260
CrossRef Google scholar
[16]
Goodwin S, McPherson JD, McCombie WR. Coming of age: ten years of next-generation sequencing technologies. Nat Rev Genet 2016; 17(6): 333–351
CrossRef Google scholar
[17]
International Human Genome Sequencing Consortium. Finishing the euchromatic sequence of the human genome. Nature 2004; 431(7011): 931–945
CrossRef Google scholar
[18]
Schneider VA, Graves-Lindsay T, Howe K, Bouk N, Chen HC, Kitts PA, Murphy TD, Pruitt KD, Thibaud-Nissen F, Albracht D, Fulton RS, Kremitzki M, Magrini V, Markovic C, McGrath S, Steinberg KM, Auger K, Chow W, Collins J, Harden G, Hubbard T, Pelan S, Simpson JT, Threadgold G, Torrance J, Wood JM, Clarke L, Koren S, Boitano M, Peluso P, Li H, Chin CS, Phillippy AM, Durbin R, Wilson RK, Flicek P, Eichler EE, Church DM. Evaluation of GRCh38 and de novo haploid genome assemblies demonstrates the enduring quality of the reference assembly. Genome Res 2017; 27(5): 849–864
CrossRef Google scholar
[19]
Audano PA, Sulovari A, Graves-Lindsay TA, Cantsilieris S, Sorensen M, Welch AE, Dougherty ML, Nelson BJ, Shah A, Dutcher SK, Warren WC, Magrini V, McGrath SD, Li YI, Wilson RK, Eichler EE. Characterizing the major structural variant alleles of the human genome. Cell 2019; 176(3): 663–675.e19
CrossRef Google scholar
[20]
Yang X, Lee WP, Ye K, Lee C. One reference genome is not enough. Genome Biol 2019; 20(1): 104
CrossRef Google scholar
[21]
Golicz AA, Bayer PE, Bhalla PL, Batley J, Edwards D. Pangenomics comes of age: from bacteria to plant and animal applications. Trends Genet 2020; 36(2): 132–145
CrossRef Google scholar
[22]
Tettelin H, Masignani V, Cieslewicz MJ, Donati C, Medini D, Ward NL, Angiuoli SV, Crabtree J, Jones AL, Durkin AS, Deboy RT, Davidsen TM, Mora M, Scarselli M, Margarit y Ros I, Peterson JD, Hauser CR, Sundaram JP, Nelson WC, Madupu R, Brinkac LM, Dodson RJ, Rosovitz MJ, Sullivan SA, Daugherty SC, Haft DH, Selengut J, Gwinn ML, Zhou L, Zafar N, Khouri H, Radune D, Dimitrov G, Watkins K, O’Connor KJ, Smith S, Utterback TR, White O, Rubens CE, Grandi G, Madoff LC, Kasper DL, Telford JL, Wessels MR, Rappuoli R, Fraser CM. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial “pan-genome”. Proc Natl Acad Sci USA 2005; 102(39): 13950–13955
CrossRef Google scholar
[23]
Wang W, Mauleon R, Hu Z, Chebotarov D, Tai S, Wu Z, Li M, Zheng T, Fuentes RR, Zhang F, Mansueto L, Copetti D, Sanciangco M, Palis KC, Xu J, Sun C, Fu B, Zhang H, Gao Y, Zhao X, Shen F, Cui X, Yu H, Li Z, Chen M, Detras J, Zhou Y, Zhang X, Zhao Y, Kudrna D, Wang C, Li R, Jia B, Lu J, He X, Dong Z, Xu J, Li Y, Wang M, Shi J, Li J, Zhang D, Lee S, Hu W, Poliakov A, Dubchak I, Ulat VJ, Borja FN, Mendoza JR, Ali J, Li J, Gao Q, Niu Y, Yue Z, Naredo MEB, Talag J, Wang X, Li J, Fang X, Yin Y, Glaszmann JC, Zhang J, Li J, Hamilton RS, Wing RA, Ruan J, Zhang G, Wei C, Alexandrov N, McNally KL, Li Z, Leung H. Genomic variation in 3010 diverse accessions of Asian cultivated rice. Nature 2018; 557(7703): 43–49
CrossRef Google scholar
[24]
Gong Y, Li Y, Liu X, Ma Y, Jiang L. A review of the pangenome: how it affects our understanding of genomic variation, selection and breeding in domestic animals?. J Anim Sci Biotechnol 2023; 14(1): 73
CrossRef Google scholar
[25]
Venter JC, Adams MD, Myers EW, Li PW, Mural RJ, Sutton GG, Smith HO, Yandell M, Evans CA, Holt RA, Gocayne JD, Amanatides P, Ballew RM, Huson DH, Wortman JR, Zhang Q, Kodira CD, Zheng XH, Chen L, Skupski M, Subramanian G, Thomas PD, Zhang J, Gabor Miklos GL, Nelson C, Broder S, Clark AG, Nadeau J, McKusick VA, Zinder N, Levine AJ, Roberts RJ, Simon M, Slayman C, Hunkapiller M, Bolanos R, Delcher A, Dew I, Fasulo D, Flanigan M, Florea L, Halpern A, Hannenhalli S, Kravitz S, Levy S, Mobarry C, Reinert K, Remington K, Abu-Threideh J, Beasley E, Biddick K, Bonazzi V, Brandon R, Cargill M, Chandramouliswaran I, Charlab R, Chaturvedi K, Deng Z, Di Francesco V, Dunn P, Eilbeck K, Evangelista C, Gabrielian AE, Gan W, Ge W, Gong F, Gu Z, Guan P, Heiman TJ, Higgins ME, Ji RR, Ke Z, Ketchum KA, Lai Z, Lei Y, Li Z, Li J, Liang Y, Lin X, Lu F, Merkulov GV, Milshina N, Moore HM, Naik AK, Narayan VA, Neelam B, Nusskern D, Rusch DB, Salzberg S, Shao W, Shue B, Sun J, Wang Z, Wang A, Wang X, Wang J, Wei M, Wides R, Xiao C, Yan C, Yao A, Ye J, Zhan M, Zhang W, Zhang H, Zhao Q, Zheng L, Zhong F, Zhong W, Zhu S, Zhao S, Gilbert D, Baumhueter S, Spier G, Carter C, Cravchik A, Woodage T, Ali F, An H, Awe A, Baldwin D, Baden H, Barnstead M, Barrow I, Beeson K, Busam D, Carver A, Center A, Cheng ML, Curry L, Danaher S, Davenport L, Desilets R, Dietz S, Dodson K, Doup L, Ferriera S, Garg N, Gluecksmann A, Hart B, Haynes J, Haynes C, Heiner C, Hladun S, Hostin D, Houck J, Howland T, Ibegwam C, Johnson J, Kalush F, Kline L, Koduru S, Love A, Mann F, May D, McCawley S, McIntosh T, McMullen I, Moy M, Moy L, Murphy B, Nelson K, Pfannkoch C, Pratts E, Puri V, Qureshi H, Reardon M, Rodriguez R, Rogers YH, Romblad D, Ruhfel B, Scott R, Sitter C, Smallwood M, Stewart E, Strong R, Suh E, Thomas R, Tint NN, Tse S, Vech C, Wang G, Wetter J, Williams S, Williams M, Windsor S, Winn-Deen E, Wolfe K, Zaveri J, Zaveri K, Abril JF, Guigó R, Campbell MJ, Sjolander KV, Karlak B, Kejariwal A, Mi H, Lazareva B, Hatton T, Narechania A, Diemer K, Muruganujan A, Guo N, Sato S, Bafna V, Istrail S, Lippert R, Schwartz R, Walenz B, Yooseph S, Allen D, Basu A, Baxendale J, Blick L, Caminha M, Carnes-Stine J, Caulk P, Chiang YH, Coyne M, Dahlke C, Deslattes Mays A, Dombroski M, Donnelly M, Ely D, Esparham S, Fosler C, Gire H, Glanowski S, Glasser K, Glodek A, Gorokhov M, Graham K, Gropman B, Harris M, Heil J, Henderson S, Hoover J, Jennings D, Jordan C, Jordan J, Kasha J, Kagan L, Kraft C, Levitsky A, Lewis M, Liu X, Lopez J, Ma D, Majoros W, McDaniel J, Murphy S, Newman M, Nguyen T, Nguyen N, Nodell M, Pan S, Peck J, Peterson M, Rowe W, Sanders R, Scott J, Simpson M, Smith T, Sprague A, Stockwell T, Turner R, Venter E, Wang M, Wen M, Wu D, Wu M, Xia A, Zandieh A, Zhu X. The sequence of the human genome. Science 2001; 291(5507): 1304–1351
CrossRef Google scholar
[26]
Llamas B, Narzisi G, Schneider V, Audano PA, Biederstedt E, Blauvelt L, Bradbury P, Chang X, Chin CS, Fungtammasan A, Clarke WE, Cleary A, Ebler J, Eizenga J, Sibbesen JA, Markello CJ, Garrison E, Garg S, Hickey G, Lazo GR, Lin MF, Mahmoud M, Marschall T, Minkin I, Monlong J, Musunuri RL, Sagayaradj S, Novak AM, Rautiainen M, Regier A, Sedlazeck FJ, Siren J, Souilmi Y, Wagner J, Wrightsman T, Yokoyama TT, Zeng Q, Zook JM, Paten B, Busby B. A strategy for building and using a human reference pangenome. F1000 Res 2019; 8: 1751
CrossRef Google scholar
[27]
Duan Z, Qiao Y, Lu J, Lu H, Zhang W, Yan F, Sun C, Hu Z, Zhang Z, Li G, Chen H, Xiang Z, Zhu Z, Zhao H, Yu Y, Wei C. HUPAN: a pan-genome analysis pipeline for human genomes. Genome Biol 2019; 20(1): 149
CrossRef Google scholar
[28]
Li H, Feng X, Chu C. The design and construction of reference pangenome graphs with minigraph. Genome Biol 2020; 21(1): 265
CrossRef Google scholar
[29]
Eizenga JM, Novak AM, Sibbesen JA, Heumos S, Ghaffaari A, Hickey G, Chang X, Seaman JD, Rounthwaite R, Ebler J, Rautiainen M, Garg S, Paten B, Marschall T, Sirén J, Garrison E. Pangenome graphs. Annu Rev Genomics Hum Genet 2020; 21(1): 139–162
CrossRef Google scholar
[30]
Garg S, Balboa R, Kuja J. Chromosome-scale haplotype-resolved pangenomics. Trends Genet 2022; 38(11): 1103–1107
CrossRef Google scholar
[31]
Massarat A, Gymrek M, McStay B, Jónsson H. Human pangenome supports analysis of complex genomic regions. Nature 2023; 617(7960): 256–258
CrossRef Google scholar
[32]
Yu Y, Zhang Z, Dong X, Yang R, Duan Z, Xiang Z, Li J, Li G, Yan F, Xue H, Jiao D, Lu J, Lu H, Zhang W, Wei Y, Fan S, Li J, Jia J, Zhang J, Ji J, Liu P, Lu H, Zhao H, Chen S, Wei C, Chen H, Zhu Z. Pangenomic analysis of Chinese gastric cancer. Nat Commun 2022; 13(1): 5412
CrossRef Google scholar
[33]
Yoshida T, Yatabe Y, Kato K, Ishii G, Hamada A, Mano H, Sunami K, Yamamoto N, Kohno T. The evolution of cancer genomic medicine in Japan and the role of the National Cancer Center Japan. Cancer Biol Med 2023; 3: j.issn.2095-3941.2023.0036
CrossRef Google scholar
[34]
Stewart OA, Wu F, Chen Y. The role of gastric microbiota in gastric cancer. Gut Microbes 2020; 11(5): 1220–1230
CrossRef Google scholar
[35]
Cancer Genome Atlas Research Network. Comprehensive molecular characterization of gastric adenocarcinoma. Nature 2014; 513(7517): 202–209
CrossRef Google scholar
[36]
Yu Y, Wei C. A powerful HUPAN on a pan-genome study: significance and perspectives. Cancer Biol Med 2020; 17(1): 1–5
CrossRef Google scholar
[37]
Watson CM, Crinnion LA, Simmonds J, Camm N, Adlard J, Bonthron DT. Long-read nanopore sequencing enables accurate confirmation of a recurrent PMS2 insertion-deletion variant located in a region of complex genomic architecture. Cancer Genet 2021; 256–257: 122–126
CrossRef Google scholar
[38]
Pareek CS, Smoczynski R, Tretyn A. Sequencing technologies and genome sequencing. J Appl Genet 2011; 52(4): 413–435
CrossRef Google scholar
[39]
Venkatesan BM, Bashir R. Nanopore sensors for nucleic acid analysis. Nat Nanotechnol 2011; 6(10): 615–624
CrossRef Google scholar
[40]
Ozsolak F. Third-generation sequencing techniques and applications to drug discovery. Expert Opin Drug Discov 2012; 7(3): 231–243
CrossRef Google scholar
[41]
Tsai CM, Riestra AM, Ali SR, Fong JJ, Liu JZ, Hughes G, Varki A, Nizet V. Siglec-14 enhances NLRP3-inflammasome activation in macrophages. J Innate Immun 2020; 12(4): 333–343
CrossRef Google scholar
[42]
Angata T, Hayakawa T, Yamanaka M, Varki A, Nakamura M. Discovery of Siglec-14, a novel sialic acid receptor undergoing concerted evolution with Siglec-5 in primates. FASEB J 2006; 20(12): 1964–1973
CrossRef Google scholar
[43]
Yamanaka M, Kato Y, Angata T, Narimatsu H. Deletion polymorphism of SIGLEC14 and its functional implications. Glycobiology 2009; 19(8): 841–846
CrossRef Google scholar
[44]
Varki A. Colloquium paper: uniquely human evolution of sialic acid genetics and biology. Proc Natl Acad Sci USA 2010; 107(Suppl 2): 8939–8946
CrossRef Google scholar
[45]
Yu Y, Peng W. Recent progress in targeting the sialylated glycan-SIGLEC axis in cancer immunotherapy. Cancer Biol Med 2023; 20(5): 369–384
CrossRef Google scholar
[46]
Lin YL, Pavlidis P, Karakoc E, Ajay J, Gokcumen O. The evolution and functional impact of human deletion variants shared with archaic hominin genomes. Mol Biol Evol 2015; 32(4): 1008–1019
CrossRef Google scholar
[47]
Cavalli M, Diamanti K, Dang Y, Xing P, Pan G, Chen X, Wadelius C. The thioesterase ACOT1 as a regulator of lipid metabolism in type 2 diabetes detected in a multi-omics study of human liver. OMICS 2021; 25(10): 652–659
CrossRef Google scholar

Acknowledgments

We thank the High Performance Computing Center (HPCC) at Shanghai Jiao Tong University for the computation. This work was supported by grants from the Shanghai Science and Technology Committee (No. 20DZ2201900), the National Natural Science Foundation of China (No. 82072602), the Innovation Foundation of Translational Medicine of Shanghai Jiao Tong University School of Medicine (No. TM202001), and the Collaborative Innovation Center for Clinical and Translational Science by Chinese Ministry of Education & Shanghai Municipal Government (Nos. CCTS-2022202 and CCTS-202302). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Compliance with ethics guidelines

YingyanYu and Hongzhuan Chen declare no conflicts of interest. This article does not involve a research protocol requiring approval by a relevant institutional review board or ethics committee.

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