The role of molecular profiling in adrenocortical carcinoma.
adrenocortical cancer
biomarkers
precision medicine
prognosis
targeted treatment
Journal
Clinical endocrinology
ISSN: 1365-2265
Titre abrégé: Clin Endocrinol (Oxf)
Pays: England
ID NLM: 0346653
Informations de publication
Date de publication:
10 2022
10 2022
Historique:
revised:
18
10
2021
received:
07
09
2021
accepted:
23
10
2021
pubmed:
10
11
2021
medline:
14
9
2022
entrez:
9
11
2021
Statut:
ppublish
Résumé
Adrenocortical carcinoma (ACC) is a rare, aggressive cancer with still partially unknown pathogenesis, heterogenous clinical behaviour and no effective treatment for advanced stages. Therefore, there is an urgent clinical unmet need for better prognostication strategies, innovative therapies and significant improvement of the management of the individual patients. In this review, we summarize available studies on molecular prognostic markers and markers predictive of response to standard therapies as well as newly proposed drug targets in sporadic ACC. We include in vitro studies and available clinical trials, focusing on alterations at the DNA, RNA and epigenetic levels. We also discuss the potential of biomarkers to be implemented in a clinical routine workflow for improved ACC patient care.
Types de publication
Journal Article
Review
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
460-472Informations de copyright
© 2021 The Authors. Clinical Endocrinology published by John Wiley & Sons Ltd.
Références
Kerkhofs TM, Verhoeven RH, Van der Zwan JM, et al. Adrenocortical carcinoma: a population-based study on incidence and survival in the Netherlands since 1993. Eur J Cancer. 2013;49(11):2579-2586.
Else T, Kim AC, Sabolch A, et al. Adrenocortical carcinoma. Endocr Rev. 2014;35(2):282-326.
Fassnacht M, Dekkers OM, Else T, et al. European Society of Endocrinology Clinical Practice Guidelines on the management of adrenocortical carcinoma in adults, in collaboration with the European Network for the Study of Adrenal Tumors. Eur J Endocrinol. 2018;179(4):G1-G46.
Fassnacht M, Johanssen S, Quinkler M, et al. Limited prognostic value of the 2004 International Union Against Cancer staging classification for adrenocortical carcinoma: proposal for a Revised TNM Classification. Cancer. 2009;115(2):243-250.
Fassnacht M, Assie G, Baudin E, et al. Adrenocortical carcinomas and malignant phaeochromocytomas: ESMO-EURACAN Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2020;31(11):1476-1490.
Assie G, Letouze E, Fassnacht M, et al. Integrated genomic characterization of adrenocortical carcinoma. Nat Genet. 2014;46(6):607-612.
Zheng S, Cherniack AD, Dewal N, et al. Comprehensive pan-genomic characterization of adrenocortical carcinoma. Cancer Cell. 2016;30(2):363.
Lippert J, Appenzeller S, Liang R, et al. Targeted molecular analysis in adrenocortical carcinomas: a strategy toward improved personalized prognostication. J Clin Endocrinol Metab. 2018;103(12):4511-4523.
Assie G, Jouinot A, Fassnacht M, et al. Value of molecular classification for prognostic assessment of adrenocortical carcinoma. JAMA Oncol. 2019;5(10):1440-1447.
Fassnacht M, Terzolo M, Allolio B, et al. Combination chemotherapy in advanced adrenocortical carcinoma. N Engl J Med. 2012;366(23):2189-2197.
Mohan DR, Lerario AM, Hammer GD. Therapeutic targets for adrenocortical carcinoma in the genomics era. J Endocr Soc. 2018;2(11):1259-1274.
Altieri B, Ronchi CL, Kroiss M, Fassnacht M. Next-generation therapies for adrenocortical carcinoma. Best Pract Res Clin Endocrinol Metab. 2020;34(3):101434.
Kamilaris CDC, Hannah-Shmouni F, Stratakis CA. Adrenocortical tumorigenesis: Lessons from genetics. Best Pract Res Clin Endocrinol Metab. 2020;34(3):101428.
Jouinot A, Bertherat J. Diseases predisposing to adrenocortical malignancy (Li-Fraumeni syndrome, beckwith-wiedemann syndrome, and carney complex). Exp Suppl. 2019;111:149-169.
Petr EJ, Else T. Adrenocortical carcinoma (ACC): when and why should we consider germline testing? Presse Med. 2018;47(7-8 Pt 2):e119-e125.
Yano T, Linehan M, Anglard P, et al. Genetic changes in human adrenocortical carcinomas. J Natl Cancer Inst. 1989;81(7):518-523.
Henry I, Jeanpierre M, Couillin P, et al. Molecular definition of the 11p15.5 region involved in Beckwith-Wiedemann syndrome and probably in predisposition to adrenocortical carcinoma. Hum Genet. 1989;81(3):273-277.
Gicquel C, Bertagna X, Gaston V, et al. Molecular markers and long-term recurrences in a large cohort of patients with sporadic adrenocortical tumors. Cancer Res. 2001;61(18):6762-6767.
Kjellman M, Kallioniemi OP, Karhu R, et al. Genetic aberrations in adrenocortical tumors detected using comparative genomic hybridization correlate with tumor size and malignancy. Cancer Res. 1996;56(18):4219-4223.
Barreau O, de Reynies A, Wilmot-Roussel H, et al. Clinical and pathophysiological implications of chromosomal alterations in adrenocortical tumors: an integrated genomic approach. J Clin Endocrinol Metab. 2012;97(2):E301-E311.
Ronchi CL, Sbiera S, Leich E, et al. Single nucleotide polymorphism array profiling of adrenocortical tumors--evidence for an adenoma carcinoma sequence? PLoS One. 2013;8(9):e73959.
Stephan EA, Chung TH, Grant CS, et al. Adrenocortical carcinoma survival rates correlated to genomic copy number variants. Mol Cancer Ther. 2008;7(2):425-431.
Juhlin CC, Goh G, Healy JM, et al. Whole-exome sequencing characterizes the landscape of somatic mutations and copy number alterations in adrenocortical carcinoma. J Clin Endocrinol Metab. 2015;100(3):E493-E502.
Libe R, Groussin L, Tissier F, et al. Somatic TP53 mutations are relatively rare among adrenocortical cancers with the frequent 17p13 loss of heterozygosity. Clin Cancer Res. 2007;13(3):844-850.
Gicquel C, Bertagna X, Schneid H, et al. Rearrangements at the 11p15 locus and overexpression of insulin-like growth factor-II gene in sporadic adrenocortical tumors. J Clin Endocrinol Metab. Jun 1994;78(6):1444-1453.
Rechache NS, Wang Y, Stevenson HS, et al. DNA methylation profiling identifies global methylation differences and markers of adrenocortical tumors. J Clin Endocrinol Metab. 2012;97(6):E1004-E1013.
Barreau O, Assie G, Wilmot-Roussel H, et al. Identification of a CpG island methylator phenotype in adrenocortical carcinomas. J Clin Endocrinol Metab. 2013;98(1):E174-E184.
Jouinot A, Assie G, Libe R, et al. DNA methylation Is an independent prognostic marker of survival in adrenocortical cancer. J Clin Endocrinol Metab. 2017;102(3):923-932.
Mohan DR, Lerario AM, Else T, et al. Targeted assessment of G0S2 methylation identifies a rapidly recurrent, routinely fatal molecular subtype of adrenocortical carcinoma. Clin Cancer Res. 2019;25(11):3276-3288.
Giordano TJ, Thomas DG, Kuick R, et al. Distinct transcriptional profiles of adrenocortical tumors uncovered by DNA microarray analysis. Am J Pathol. 2003;162(2):521-531.
de Fraipont F, El Atifi M, Cherradi N, et al. Gene expression profiling of human adrenocortical tumors using complementary deoxyribonucleic acid microarrays identifies several candidate genes as markers of malignancy. J Clin Endocrinol Metab. 2005;90(3):1819-1829.
Giordano TJ, Kuick R, Else T, et al. Molecular classification and prognostication of adrenocortical tumors by transcriptome profiling. Clin Cancer Res. 2009;15(2):668-676.
de Reynies A, Assie G, Rickman DS, et al. Gene expression profiling reveals a new classification of adrenocortical tumors and identifies molecular predictors of malignancy and survival. J Clin Oncol. 2009;27(7):1108-1115.
Ragazzon B, Libe R, Gaujoux S, et al. Transcriptome analysis reveals that p53 and {beta}-catenin alterations occur in a group of aggressive adrenocortical cancers. Cancer Res. 2010;70(21):8276-8281.
Fragoso MC, Almeida MQ, Mazzuco TL, et al. Combined expression of BUB1B, DLGAP5, and PINK1 as predictors of poor outcome in adrenocortical tumors: validation in a Brazilian cohort of adult and pediatric patients. Eur J Endocrinol. 2012;166(1):61-67.
Calin GA, Dumitru CD, Shimizu M, et al. Frequent deletions and down-regulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci U S A. 2002;99(24):15524-15529.
Soon PS, Tacon LJ, Gill AJ, et al. miR-195 and miR-483-5p Identified as predictors of poor prognosis in adrenocortical cancer. Clin Cancer Res. 2009;15(24):7684-7692.
Schmitz KJ, Helwig J, Bertram S, et al. Differential expression of microRNA-675, microRNA-139-3p and microRNA-335 in benign and malignant adrenocortical tumours. J Clin Pathol. 2011;64(6):529-535.
Chabre O, Libe R, Assie G, et al. Serum miR-483-5p and miR-195 are predictive of recurrence risk in adrenocortical cancer patients. Endocr Relat Cancer. 2013;20(4):579-594.
Salvianti F, Canu L, Poli G, et al. New insights in the clinical and translational relevance of miR483-5p in adrenocortical cancer. Oncotarget. 2017;8(39):65525-65533.
Oreglia M, Sbiera S, Fassnacht M, et al. Early postoperative circulating miR-483-5p Is a prognosis marker for adrenocortical cancer. Cancers (Basel). 2020;12(3).
Ozata DM, Caramuta S, Velazquez-Fernandez D, et al. The role of microRNA deregulation in the pathogenesis of adrenocortical carcinoma. Endocr Relat Cancer. 2011;18(6):643-655.
McGranahan N, Swanton C. Clonal Heterogeneity and tumor evolution: past, present, and the future. Cell. 2017;168(4):613-628.
Mazor T, Pankov A, Song JS, Costello JF. Intratumoral heterogeneity of the epigenome. Cancer Cell. 2016;29(4):440-451.
Vatrano S, Volante M, Duregon E, et al. Detailed genomic characterization identifies high heterogeneity and histotype-specific genomic profiles in adrenocortical carcinomas. Mod Pathol. 2018;31(8):1257-1269.
Gara SK, Lack J, Zhang L, Harris E, Cam M, Kebebew E. Metastatic adrenocortical carcinoma displays higher mutation rate and tumor heterogeneity than primary tumors. Nat Commun. 2018;9(1):4172.
Jouinot A, Lippert J, Fassnacht M, et al. Intratumor heterogeneity of prognostic DNA-based molecular markers in adrenocortical carcinoma. Endocr Connect. 2020;9(7):705-714.
Volante M, Terzolo M, Fassnacht M, et al. Ribonucleotide reductase large subunit (RRM1) gene expression may predict efficacy of adjuvant mitotane in adrenocortical cancer. Clin Cancer Res. 2012;18(12):3452-3461.
Jordheim LP, Seve P, Tredan O, Dumontet C. The ribonucleotide reductase large subunit (RRM1) as a predictive factor in patients with cancer. Lancet Oncol. 2011;12(7):693-702.
Fassnacht M, Libe R, Kroiss M, Allolio B. Adrenocortical carcinoma: a clinician's update. Nat Rev Endocrinol. 2011;7(6):323-335.
Puglisi S, Calabrese A, Basile V, et al. Mitotane concentrations influence outcome in patients with advanced adrenocortical carcinoma. Cancers (Basel). 2020;12(3).
D'Avolio A, De Francia S, Basile V, et al. Influence of the CYP2B6 polymorphism on the pharmacokinetics of mitotane. Pharmacogenet Genomics. 2013;23(6):293-300.
Altieri B, Sbiera S, Herterich S, et al. Effects of germline CYP2W1*6 and CYP2B6*6 single nucleotide polymorphisms on mitotane treatment in adrenocortical carcinoma: a multicenter ENSAT study. Cancers (Basel). 2020;12(2).
Ronchi CL, Sbiera S, Kraus L, et al. Expression of excision repair cross complementing group 1 and prognosis in adrenocortical carcinoma patients treated with platinum-based chemotherapy. Endocr Relat Cancer. 2009;16(3):907-918.
Laufs V, Altieri B, Sbiera S, et al. ERCC1 as predictive biomarker to platinum-based chemotherapy in adrenocortical carcinomas. Eur J Endocrinol. 2018;178(2):181-188.
Henning JEK, Deutschbein T, Altieri B, et al. Gemcitabine-based chemotherapy in adrenocortical carcinoma: a multicenter study of efficacy and predictive factors. J Clin Endocrinol Metab. 2017;102(11):4323-4332.
Le Tourneau C, Hoimes C, Zarwan C, et al. Avelumab in patients with previously treated metastatic adrenocortical carcinoma: phase 1b results from the JAVELIN solid tumor trial. J Immunother Cancer. 2018;6(1):111.
Carneiro BA, Konda B, Costa RB, et al. Nivolumab in metastatic adrenocortical carcinoma: results of a phase 2 trial. J Clin Endocrinol Metab. 2019;104(12):6193-6200.
Habra MA, Stephen B, Campbell M, et al. Phase II clinical trial of pembrolizumab efficacy and safety in advanced adrenocortical carcinoma. J Immunother Cancer. 2019;7(1):253.
Raj N, Zheng Y, Kelly V, et al. PD-1 Blockade in advanced adrenocortical carcinoma. J Clin Oncol. 2020;38(1):71-80.
Fassnacht M, Berruti A, Baudin E, et al. Linsitinib (OSI-906) versus placebo for patients with locally advanced or metastatic adrenocortical carcinoma: a double-blind, randomised, phase 3 study. Lancet Oncol. 2015;16(4):426-435.
De Martino MC, Al Ghuzlan A, Aubert S, et al. Molecular screening for a personalized treatment approach in advanced adrenocortical cancer. J Clin Endocrinol Metab. 2013;98(10):4080-4088.
Hadjadj D, Kim SJ, Denecker T, et al. A hypothesis-driven approach identifies CDK4 and CDK6 inhibitors as candidate drugs for treatments of adrenocortical carcinomas. Aging (Albany NY). 2017;9(12):2695-2716.
Fiorentini C, Fragni M, Tiberio GAM, et al. Palbociclib inhibits proliferation of human adrenocortical tumor cells. Endocrine. 2018;59(1):213-217.
Liang R, Weigand I, Lippert J, et al. Targeted gene expression profile reveals CDK4 as therapeutic target for selected patients with adrenocortical carcinoma. Front Endocrinol (Lausanne). 2020;11:219.
Nilubol N, Boufraqech M, Zhang L, et al. Synergistic combination of flavopiridol and carfilzomib targets commonly dysregulated pathways in adrenocortical carcinoma and has biomarkers of response. Oncotarget. 2018;9(68):33030-33042.
Doghman M, Cazareth J, Lalli E. The T cell factor/beta-catenin antagonist PKF115-584 inhibits proliferation of adrenocortical carcinoma cells. J Clin Endocrinol Metab. 2008;93(8):3222-3225.
Leal LF, Bueno AC, Gomes DC, Abduch R, de Castro M, Antonini SR. Inhibition of the Tcf/beta-catenin complex increases apoptosis and impairs adrenocortical tumor cell proliferation and adrenal steroidogenesis. Oncotarget. 2015;6(40):43016-43032.
Kaminskas E, Farrell AT, Wang YC, Sridhara R, Pazdur R. FDA drug approval summary: azacitidine (5-azacytidine, Vidaza) for injectable suspension. Oncologist. 2005;10(3):176-182.
Steensma DP. Decitabine treatment of patients with higher-risk myelodysplastic syndromes. Leuk Res. 2009;33(Suppl_2):S12-S17.
Gao ZH, Suppola S, Liu J, Heikkila P, Janne J, Voutilainen R. Association of H19 promoter methylation with the expression of H19 and IGF-II genes in adrenocortical tumors. J Clin Endocrinol Metab. 2002;87(3):1170-1176.
Liu J, Li XD, Vaheri A, Voutilainen R. DNA methylation affects cell proliferation, cortisol secretion and steroidogenic gene expression in human adrenocortical NCI-H295R cells. J Mol Endocrinol. 2004;33(3):651-662.
Suh I, Weng J, Fernandez-Ranvier G, et al. Antineoplastic effects of decitabine, an inhibitor of DNA promoter methylation, in adrenocortical carcinoma cells. Arch Surg. Mar 2010;145(3):226-232.
Fonseca AL, Kugelberg J, Starker LF, et al. Comprehensive DNA methylation analysis of benign and malignant adrenocortical tumors. Genes Chromosomes Cancer. 2012;51(10):949-960.
Strauss J, Figg WD. Using epigenetic therapy to overcome chemotherapy resistance. Anticancer Res. 2016;36(1):1-4.
Heneghan HM, Miller N, Kerin MJ. MiRNAs as biomarkers and therapeutic targets in cancer. Curr Opin Pharmacol. 2010;10(5):543-550.
Libe R, Borget I, Ronchi CL, et al. Prognostic factors in stage III-IV adrenocortical carcinomas (ACC): an European Network for the Study of Adrenal Tumor (ENSAT) study. Ann Oncol. Oct 2015;26(10):2119-2125.
Hantel C, Shapiro I, Poli G, et al. Targeting heterogeneity of adrenocortical carcinoma: evaluation and extension of preclinical tumor models to improve clinical translation. Oncotarget. 2016;7(48):79292-79304.
Kiseljak-Vassiliades K, Zhang Y, Bagby SM, et al. Development of new preclinical models to advance adrenocortical carcinoma research. Endocr Relat Cancer. 2018;25(4):437-451.
Landwehr LS, Schreiner J, Appenzeller S, et al. A novel patient-derived cell line of adrenocortical carcinoma shows a pathogenic role of germline MUTYH mutation and high tumour mutational burden. Eur J Endocrinol. 2021;184(6):823-835.