Diagnostic, prognostic, and therapeutic implications of genetic profiling in pleural mesothelioma

Ahmed Sadek , Assunta De Rienzo , Raphael Bueno

Journal of Cancer Metastasis and Treatment ›› 2023, Vol. 9 : 26

PDF
Journal of Cancer Metastasis and Treatment ›› 2023, Vol. 9:26 DOI: 10.20517/2394-4722.2023.17
review-article

Diagnostic, prognostic, and therapeutic implications of genetic profiling in pleural mesothelioma

Author information +
History +
PDF

Abstract

Pleural mesothelioma (PM) is an aggressive malignancy of the pleural lining that typically arises secondary to asbestos exposure. With the advent of next-generation sequencing, major progress has been made in the molecular characterization of pleural mesothelioma over the past three decades. However, these advances have been largely unable to identify effective targeted therapies for PM. Additionally, there remains an absence of accepted gold-standard consensus for staging and treatment, which partly explains the overall poor outcomes in patients with PM. In recent years, genetic profiling of PM tumors has proved to be an effective tool in the diagnosis and prognosis of PM. Genomic sequencing has identified several potential targets for the development of novel therapeutics in PM. This review summarizes the progress in diagnosis, prognosis, and therapeutics derived by genomics and tumor profiling of PM tumors.

Keywords

Pleural mesothelioma / gene-profiling / next generation sequencing / gene ratio profiling / tumor biomarkers / targeted therapies

Cite this article

Download citation ▾
Ahmed Sadek, Assunta De Rienzo, Raphael Bueno. Diagnostic, prognostic, and therapeutic implications of genetic profiling in pleural mesothelioma. Journal of Cancer Metastasis and Treatment, 2023, 9: 26 DOI:10.20517/2394-4722.2023.17

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Maciá S. Mesothelioma: intechopen; 2020. Available from: https://www.intechopen.com/books/10130 [Last accessed on 29 June 2023]

[2]

Carbone M,Alexander HR Jr.Mesothelioma: scientific clues for prevention, diagnosis, and therapy.CA Cancer J Clin2019;69:402-29 PMCID:PMC8192079

[3]

Bueno R,Goldstein LD.Comprehensive genomic analysis of malignant pleural mesothelioma identifies recurrent mutations, gene fusions and splicing alterations.Nat Genet2016;48:407-16

[4]

Lapidot M,Bueno R.New concepts in the treatment of malignant pleural mesothelioma.J Thorac Dis2018;10:1283-5 PMCID:PMC5906329

[5]

Bianchi C.Malignant mesothelioma: global incidence and relationship with asbestos.Ind Health2007;45:379-87

[6]

De Rienzo A,Yeap BY.Gender-specific molecular and clinical features underlie malignant pleural mesothelioma.Cancer Res2016;76:319-28 PMCID:PMC4715909

[7]

Herndon JE,Chahinian AP,Suzuki Y.Factors predictive of survival among 337 patients with mesothelioma treated between 1984 and 1994 by the Cancer and Leukemia Group B.Chest1998;113:723-31

[8]

Blum Y,Quetel L.Dissecting heterogeneity in malignant pleural mesothelioma through histo-molecular gradients for clinical applications.Nat Commun2019;10:1333 PMCID:PMC6430832

[9]

Borchert S,Schmeller J.Gene expression profiling of homologous recombination repair pathway indicates susceptibility for olaparib treatment in malignant pleural mesothelioma in vitro.BMC Cancer2019;19:108 PMCID:PMC6354412

[10]

Yap TA,Popat S.Novel insights into mesothelioma biology and implications for therapy.Nat Rev Cancer2017;17:475-88

[11]

Yeap BY,Gill RR.Mesothelioma risk score: a new prognostic pretreatment, clinical-molecular algorithm for malignant pleural mesothelioma.J Thorac Oncol2021;16:1925-35 PMCID:PMC8557128

[12]

Carbone M,Testa JR.The pathogenesis of mesothelioma.Semin Oncol2002;29:2-17

[13]

Dacic S.Pleural mesothelioma classification-update and challenges.Mod Pathol2022;35:51-6

[14]

Physicians RCo. National mesothelioma audit report 2018 (for the audit period 2014-16). London: Royal College of Physicians; 2018.

[15]

Galateau Salle F,Tirode F.Comprehensive molecular and pathologic evaluation of transitional mesothelioma assisted by deep learning approach: a multi-institutional study of the international mesothelioma panel from the MESOPATH reference center.J Thorac Oncol2020;15:1037-53 PMCID:PMC8864581

[16]

Sugarbaker DJ. Sugarbaker’s adult chest surgery. New York: McGraw-Hill Education; 2020.

[17]

Husain AN,Ordóñez NG.Guidelines for pathologic diagnosis of malignant mesothelioma 2017 update of the consensus statement from the international mesothelioma interest group.Arch Pathol Lab Med2018;142:89-108

[18]

Chirieac LR,Foo WC.Diagnostic value of biopsy sampling in predicting histology in patients with diffuse malignant pleural mesothelioma.Cancer2019;125:4164-71 PMCID:PMC7341068

[19]

Paajanen J,Bueno R.Contemporary issues in the surgical management of pleural mesothelioma.J Surg Oncol2023;127:343-54 PMCID:PMC9839311

[20]

Jean D,Le Pimpec-Barthes F,Jaurand MC.Molecular changes in mesothelioma with an impact on prognosis and treatment.Arch Pathol Lab Med2012;136:277-93

[21]

Severson DT,Bueno R.Mesothelioma in the age of “Omics”: before and after The Cancer Genome Atlas.J Thorac Cardiovasc Surg2020;160:1078-83.e2 PMCID:PMC9026567

[22]

Hmeljak J,Hoadley KA.Integrative molecular characterization of malignant pleural mesothelioma.Cancer Discov2018;8:1548-65

[23]

Murakami H,Taniguchi T.LATS2 is a tumor suppressor gene of malignant mesothelioma.Cancer Res2011;71:873-83

[24]

Bott M,Taylor BS.The nuclear deubiquitinase BAP1 is commonly inactivated by somatic mutations and 3p21.1 losses in malignant pleural mesothelioma.Nat Genet2011;43:668-72 PMCID:PMC4643098

[25]

Nasu M,Pastorino S.High incidence of somatic BAP1 alterations in sporadic malignant mesothelioma.J Thorac Oncol2015;10:565-76 PMCID:PMC4408084

[26]

Wang LM,Wang JL.Diagnostic accuracy of BRCA1-associated protein 1 in malignant mesothelioma: a meta-analysis.Oncotarget2017;8:68863-72 PMCID:PMC5620303

[27]

Ascoli V,Vatrano S.Mesothelioma families without inheritance of a BAP1 predisposing mutation.Cancer Genet2016;209:381-7

[28]

Guo Z,Zhang X.Improving the accuracy of mesothelioma diagnosis in china.J Thorac Oncol2017;12:714-23

[29]

Righi L,Vatrano S.BRCA1-associated protein 1 (BAP1) immunohistochemical expression as a diagnostic tool in malignant pleural mesothelioma classification: a large retrospective study.J Thorac Oncol2016;11:2006-17

[30]

Bhattacharya S,Maiti TK.Cancer associated missense mutations in BAP1 catalytic domain induce amyloidogenic aggregation: a new insight in enzymatic inactivation.Sci Rep2015;5:18462 PMCID:PMC4683529

[31]

Ventii KH,Friedrich KL.BRCA1-associated protein-1 is a tumor suppressor that requires deubiquitinating activity and nuclear localization.Cancer Res2008;68:6953-62 PMCID:PMC2736608

[32]

Carbone M,Pass HI,Testa JR.BAP1 and cancer.Nat Rev Cancer2013;13:153-9 PMCID:PMC3792854

[33]

Cigognetti M,Fisogni S.BAP1 (BRCA1-associated protein 1) is a highly specific marker for differentiating mesothelioma from reactive mesothelial proliferations.Mod Pathol2015;28:1043-57

[34]

Cozzi I,Rullo E.Loss of BRCA1-associated protein 1 (BAP1) expression is useful in diagnostic cytopathology of malignant mesothelioma in effusions.Diagn Cytopathol2018;46:9-14

[35]

Farzin M,Clarkson A.Loss of expression of BAP1 predicts longer survival in mesothelioma.Pathology2015;47:302-7

[36]

Hida T,Matsumoto S.BAP1 immunohistochemistry and p16 FISH results in combination provide higher confidence in malignant pleural mesothelioma diagnosis: ROC analysis of the two tests.Pathol Int2016;66:563-70

[37]

Hida T,Matsumoto S.Immunohistochemical detection of MTAP and BAP1 protein loss for mesothelioma diagnosis: Comparison with 9p21 FISH and BAP1 immunohistochemistry.Lung Cancer2017;104:98-105

[38]

De Rienzo A,Hung YP.Large-scale analysis of BAP1 expression reveals novel associations with clinical and molecular features of malignant pleural mesothelioma.J Pathol2021;253:68-79 PMCID:PMC7756745

[39]

Illei PB,Zakowski MF.Homozygous deletion of CDKN2A and codeletion of the methylthioadenosine phosphorylase gene in the majority of pleural mesotheliomas.Clin Cancer Res2003;9:2108-13

[40]

Illei PB,Rusch VW.The use of CDKN2A deletion as a diagnostic marker for malignant mesothelioma in body cavity effusions.Cancer2003;99:51-6

[41]

McGregor SM,Minor A.BAP1 immunohistochemistry has limited prognostic utility as a complement of CDKN2A (p16) fluorescence in situ hybridization in malignant pleural mesothelioma.Hum Pathol2017;60:86-94

[42]

Chapel DB,Berg K.MTAP immunohistochemistry is an accurate and reproducible surrogate for CDKN2A fluorescence in situ hybridization in diagnosis of malignant pleural mesothelioma.Mod Pathol2020;33:245-54

[43]

Chapel DB,Hornick JL.Correlation of methylthioadenosine phosphorylase (MTAP) protein expression with MTAP and CDKN2A copy number in malignant pleural mesothelioma.Histopathology2021;78:1032-42

[44]

Gordon GJ,Hsiao LL.Translation of microarray data into clinically relevant cancer diagnostic tests using gene expression ratios in lung cancer and mesothelioma.Cancer Res2002;62:4963-7

[45]

Gordon GJ.Transcriptional profiling of mesothelioma using microarrays.Lung Cancer2005;49 Suppl 1:S99-103

[46]

De Rienzo A,Yeap BY.Sequential binary gene ratio tests define a novel molecular diagnostic strategy for malignant pleural mesothelioma.Clin Cancer Res2013;19:2493-502 PMCID:PMC3644001

[47]

Gordon GJ,Hsiao LL.Using gene expression ratios to predict outcome among patients with mesothelioma.J Natl Cancer Inst2003;95:598-605

[48]

Gordon GJ,Yeap BY.Four-gene expression ratio test for survival in patients undergoing surgery for mesothelioma.J Natl Cancer Inst2009;101:678-86 PMCID:PMC2677573

[49]

Abakay O,Palanci Y.The value of inflammatory parameters in the prognosis of malignant mesothelioma.J Int Med Res2014;42:554-65

[50]

Brims FJ,Duffus I.A novel clinical prediction model for prognosis in malignant pleural mesothelioma using decision tree analysis.J Thorac Oncol2016;11:573-82

[51]

Curran D,Therasse P,Postmus PE.Prognostic factors in patients with pleural mesothelioma: the European Organization for Research and Treatment of Cancer experience.J Clin Oncol1998;16:145-52

[52]

Kao SC,Henderson DW.Low calretinin expression and high neutrophil-to-lymphocyte ratio are poor prognostic factors in patients with malignant mesothelioma undergoing extrapleural pneumonectomy.J Thorac Oncol2011;6:1923-9

[53]

Kao SC,Harvie R.High blood neutrophil-to-lymphocyte ratio is an indicator of poor prognosis in malignant mesothelioma patients undergoing systemic therapy.Clin Cancer Res2010;16:5805-13

[54]

Kao SC,Chatfield M.Validation of prognostic factors in malignant pleural mesothelioma: a retrospective analysis of data from patients seeking compensation from the New South Wales Dust Diseases Board.Clin Lung Cancer2013;14:70-7

[55]

Özyürek BA,Özdemirel ,Kaplan B.Relation between neutrophil/lymphocyte ratio and primary tumor metabolic activity in patients with malign pleural mesothelioma.Clin Respir J2018;12:646-51

[56]

O'Brien J,Zayed Y.Overview of MicroRNA biogenesis, mechanisms of actions, and circulation.Front Endocrinol2018;9:402 PMCID:PMC6085463

[57]

Sethi S,Sethi S.MicroRNAs in personalized cancer therapy.Clin Genet2014;86:68-73

[58]

Goto Y,Kondo Y.Epigenetic profiles distinguish malignant pleural mesothelioma from lung adenocarcinoma.Cancer Res2009;69:9073-82

[59]

Shin VY.MiRNA as potential biomarkers and therapeutic targets for gastric cancer.World J Gastroenterol2014;20:10432-9 PMCID:PMC4130850

[60]

Chandra V,Mittal B.MicroRNA aberrations: an emerging field for gallbladder cancer management.World J Gastroenterol2016;22:1787-99 PMCID:PMC4724610

[61]

Guo J,Xiao B.Differential expression of microRNA species in human gastric cancer versus non-tumorous tissues.J Gastroenterol Hepatol2009;24:652-7

[62]

Guo Y,Zhang L.Distinctive microRNA profiles relating to patient survival in esophageal squamous cell carcinoma.Cancer Res2008;68:26-33

[63]

Han YQ,Zheng WQ.Diagnostic value of microRNAs for malignant pleural mesothelioma: a mini-review.Thorac Cancer2021;12:8-12 PMCID:PMC7779186

[64]

Andersen M,Ravn J,Andersen CB.Diagnostic potential of miR-126, miR-143, miR-145, and miR-652 in malignant pleural mesothelioma.J Mol Diagn2014;16:418-30

[65]

Pass HI,Ivanov S.hsa-miR-29c* is linked to the prognosis of malignant pleural mesothelioma.Cancer Res2010;70:1916-24 PMCID:PMC2831149

[66]

Busacca S,De Cecco L.MicroRNA signature of malignant mesothelioma with potential diagnostic and prognostic implications.Am J Respir Cell Mol Biol2010;42:312-9

[67]

Cavallari I,Sharova E,Ciminale V.Liquid biopsy in malignant pleural mesothelioma: state of the art, pitfalls, and perspectives.Front Oncol2019;9:740 PMCID:PMC6705182

[68]

Merker JD,Compton C.Circulating tumor DNA analysis in patients with cancer: american society of clinical oncology and college of american pathologists joint review.Arch Pathol Lab Med2018;142:1242-53

[69]

Cavalleri T,Favero C.Plasmatic extracellular vesicle microRNAs in malignant pleural mesothelioma and asbestos-exposed subjects suggest a 2-miRNA signature as potential biomarker of disease.PLoS One2017;12:e0176680 PMCID:PMC5417506

[70]

Birnie KA,Musk AWB.MicroRNA signatures in malignant pleural mesothelioma effusions.Dis Markers2019;2019:8628612 PMCID:PMC6701424

[71]

Burt BM,Lenge De Rosen V.Soluble mesothelin-related peptides to monitor recurrence after resection of pleural mesothelioma.Ann Thorac Surg2017;104:1679-87

[72]

Martinson LJ,Dawson AG.Abstract 1349: personalized circulating tumor DNA profiling in malignant pleural mesothelioma.Cancer Res2019;79:1349

[73]

Hylebos M,Pauwels P,van Meerbeeck JP.Tumor-specific genetic variants can be detected in circulating cell-free DNA of malignant pleural mesothelioma patients.Lung Cancer2018;124:19-22

[74]

Wu L,Yun H.Prognostic value of EMT gene signature in malignant mesothelioma.Int J Mol Sci2023;24:4264 PMCID:PMC10001510

[75]

Canino C,Marcato P,Pass HI.A STAT3-NFkB/DDIT3/CEBPβ axis modulates ALDH1A3 expression in chemoresistant cell subpopulations.Oncotarget2015;6:12637-53 PMCID:PMC4494963

[76]

Cioce M,Pass HI.Insights into intra-tumoral heterogeneity: transcriptional profiling of chemoresistant MPM cell subpopulations reveals involvement of NFkB and DNA repair pathways and contributes a prognostic signature.Int J Mol Sci2021;22:12071 PMCID:PMC8585077

[77]

Janes SM,Fennell DA.Perspectives on the treatment of malignant pleural mesothelioma.N Engl J Med2021;385:1207-18

[78]

Friedberg JS,Tsao AS.A Proposed system toward standardizing surgical-based treatments for malignant pleural mesothelioma, from the joint national cancer institute-international association for the study of lung cancer-mesothelioma applied research foundation taskforce.J Thorac Oncol2019;14:1343-53

[79]

Lapidot M,Mazzola E.Pleurectomy decortication in the treatment of malignant pleural mesothelioma: encouraging results and novel prognostic implications based on experience in 355 consecutive patients.Ann Surg2022;275:1212-20

[80]

Järvinen T,Ilonen I.Hyperthermic intrathoracic chemoperfusion for malignant pleural mesothelioma: systematic review and meta-analysis.Cancers2021;13:3637 PMCID:PMC8307465

[81]

Sanmamed MF.Inducible expression of B7-H1 (PD-L1) and its selective role in tumor site immune modulation.Cancer J2014;20:256-61 PMCID:PMC4455021

[82]

Peters S,Cornelissen R.First-line nivolumab plus ipilimumab versus chemotherapy in patients with unresectable malignant pleural mesothelioma: 3-year outcomes from CheckMate 743.Ann Oncol2022;33:488-99

[83]

Forde PM,Sun Z.Durvalumab with platinum-pemetrexed for unresectable pleural mesothelioma: survival, genomic and immunologic analyses from the phase 2 PrE0505 trial.Nat Med2021;27:1910-20 PMCID:PMC8604731

[84]

Lee HS,Ramineni M.A phase II window of opportunity study of neoadjuvant PD-L1 versus PD-L1 plus CTLA-4 blockade for patients with malignant pleural mesothelioma.Clin Cancer Res2023;29:548-59 PMCID:PMC9898180

[85]

Baas P,Nowak AK.First-line nivolumab plus ipilimumab in unresectable malignant pleural mesothelioma (CheckMate 743): a multicentre, randomised, open-label, phase 3 trial.Lancet2021;397:375-86

[86]

Hinz TK.Translating mesothelioma molecular genomics and dependencies into precision oncology-based therapies.Semin Cancer Biol2020;61:11-22

[87]

Paajanen J,De Rienzo A.The rocky road from preclinical findings to successful targeted therapy in pleural mesothelioma.Int J Mol Sci2022;23:13422 PMCID:PMC9658134

[88]

Duan R,Guo W.EZH2: a novel target for cancer treatment.J Hematol Oncol2020;13:104 PMCID:PMC7385862

[89]

Zauderer MG,Le Moulec S.EZH2 inhibitor tazemetostat in patients with relapsed or refractory, BAP1-inactivated malignant pleural mesothelioma: a multicentre, open-label, phase 2 study.Lancet Oncol2022;23:758-67

[90]

Fennell DA,Mohammed S.Rucaparib in patients with BAP1-deficient or BRCA1-deficient mesothelioma (MiST1): an open-label, single-arm, phase 2a clinical trial.Lancet Respir Med2021;9:593-600

[91]

ali A,Lee J.Phase II trial of the PARP inhibitor, niraparib, in BAP1 and other DNA damage response (DDR) pathway deficient neoplasms (NCT03207347).J Clin Oncol2020;38:e22061

[92]

Fennell DA,Mohammed S.Abemaciclib in patients with p16ink4A-deficient mesothelioma (MiST2): a single-arm, open-label, phase 2 trial.Lancet Oncol2022;23:374-81

[93]

Sato T.NF2/merlin inactivation and potential therapeutic targets in mesothelioma.Int J Mol Sci2018;19:988 PMCID:PMC5979333

[94]

Shapiro IM,Vidal CM.Merlin deficiency predicts FAK inhibitor sensitivity: a synthetic lethal relationship.Sci Transl Med2014;6:237ra68 PMCID:PMC4165339

[95]

Fennell DA,Taylor P.Maintenance defactinib versus placebo after first-line chemotherapy in patients with merlin-stratified pleural mesothelioma: COMMAND-a double-blind, randomized, phase II study.J Clin Oncol2019;37:790-8

[96]

Knelson EH,Tarannum M.Activation of tumor-cell STING primes NK-cell therapy.Cancer Immunol Res2022;10:947-61 PMCID:PMC9357206

[97]

Lapidot M,Weisberg EL.Essential role of the histone lysine demethylase KDM4A in the biology of malignant pleural mesothelioma (MPM).Br J Cancer2021;125:582-92 PMCID:PMC8368004

[98]

Birnie KA,Thompson PJ,Mutsaers SE.Targeting microRNA to improve diagnostic and therapeutic approaches for malignant mesothelioma.Oncotarget2017;8:78193-207 PMCID:PMC5652849

[99]

Tomasetti M,Staffolani S.MicroRNA-126 suppresses mesothelioma malignancy by targeting IRS1 and interfering with the mitochondrial function.Antioxid Redox Signal2014;21:2109-25 PMCID:PMC4215384

[100]

Monaco F,Vodret S.Force-feeding malignant mesothelioma stem-cell like with exosome-delivered miR-126 induces tumour cell killing.Transl Oncol2022;20:101400 PMCID:PMC8956928

[101]

Monaco F,Alessandrini F.Exosomal transfer of miR-126 promotes the anti-tumour response in malignant mesothelioma: Role of miR-126 in cancer-stroma communication.Cancer Lett2019;463:27-36

[102]

Bandi N,Gugger M.miR-15a and miR-16 are implicated in cell cycle regulation in a Rb-dependent manner and are frequently deleted or down-regulated in non-small cell lung cancer.Cancer Res2009;69:5553-9

[103]

Bonci D,Musumeci M.The miR-15a-miR-16-1 cluster controls prostate cancer by targeting multiple oncogenic activities.Nat Med2008;14:1271-7

[104]

van Zandwijk N,Kao SC.Safety and activity of microRNA-loaded minicells in patients with recurrent malignant pleural mesothelioma: a first-in-man, phase 1, open-label, dose-escalation study.Lancet Oncol2017;18:1386-96

[105]

Reid G,Kirschner MB.Restoring expression of miR-16: a novel approach to therapy for malignant pleural mesothelioma.Ann Oncol2013;24:3128-35

[106]

El-Deiry WS,Lenz HJ.The current state of molecular testing in the treatment of patients with solid tumors, 2019.CA Cancer J Clin2019;69:305-43 PMCID:PMC6767457

[107]

Hiltbrunner S,Sokol ES,Felley-Bosco E.Genomic landscape of pleural and peritoneal mesothelioma tumours.Br J Cancer2022;127:1997-2005 PMCID:PMC9681755

[108]

Gordon GJ,Godfrey PA.Validation of genomics-based prognostic tests in malignant pleural mesothelioma.Clin Cancer Res2005;11:4406-14 PMCID:PMC1488818

[109]

Xu D,Schmid RA.Therapeutic landscape of malignant pleural mesothelioma: collateral vulnerabilities and evolutionary dependencies in the spotlight.Front Oncol2020;10:579464 PMCID:PMC7538645

AI Summary AI Mindmap
PDF

55

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/