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Published in: Journal of Endocrinological Investigation 5/2018

01-05-2018 | Review

Adrenocortical carcinoma: the dawn of a new era of genomic and molecular biology analysis

Authors: R. Armignacco, G. Cantini, L. Canu, G. Poli, T. Ercolino, M. Mannelli, M. Luconi

Published in: Journal of Endocrinological Investigation | Issue 5/2018

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Abstract

Over the last decade, the development of novel and high penetrance genomic approaches to analyze biological samples has provided very new insights in the comprehension of the molecular biology and genetics of tumors. The use of these techniques, consisting of exome sequencing, transcriptome, miRNome, chromosome alteration, genome, and epigenome analysis, has also been successfully applied to adrenocortical carcinoma (ACC). In fact, the analysis of large cohorts of patients allowed the stratification of ACC with different patterns of molecular alterations, associated with different outcomes, thus providing a novel molecular classification of the malignancy to be associated with the classical pathological analysis. Improving our knowledge about ACC molecular features will result not only in a better diagnostic and prognostic accuracy, but also in the identification of more specific therapeutic targets for the development of more effective pharmacological anti-cancer approaches. In particular, the specific molecular alteration profiles identified in ACC may represent targetable events by the use of already developed or newly designed drugs enabling a better and more efficacious management of the ACC patient in the context of new frontiers of personalized precision medicine.
Literature
1.
go back to reference Libé R (2015) Adrenocortical carcinoma (ACC): diagnosis, prognosis, and treatment. Dev Biol 3:45 Libé R (2015) Adrenocortical carcinoma (ACC): diagnosis, prognosis, and treatment. Dev Biol 3:45
2.
go back to reference Else T, Kim AC, Sabolch A, Raymond VM, Kandathil A, Caoili EM, Jolly S, Miller BS, Giordano TJ, Hammer GD (2014) Adrenocortical carcinoma. Endocr Rev 35:282–326CrossRefPubMed Else T, Kim AC, Sabolch A, Raymond VM, Kandathil A, Caoili EM, Jolly S, Miller BS, Giordano TJ, Hammer GD (2014) Adrenocortical carcinoma. Endocr Rev 35:282–326CrossRefPubMed
3.
go back to reference Erdogan I, Deutschbein T, Jurowich C, Kroiss M, Ronchi C, Quinkler M, Waldmann J, Willenberg HS, Beuschlein F, Fattener C, Klose S, Heidemeier A, Brix D, Fenske W, Hahner S, Reibetanz J, Allolio B, Fassnacht M, German Adrenocortical Carcinoma Study Group (2013) The role of surgery in the management of recurrent adrenocortical carcinoma. J Clin Endocrinol Metab 98:181–191CrossRefPubMed Erdogan I, Deutschbein T, Jurowich C, Kroiss M, Ronchi C, Quinkler M, Waldmann J, Willenberg HS, Beuschlein F, Fattener C, Klose S, Heidemeier A, Brix D, Fenske W, Hahner S, Reibetanz J, Allolio B, Fassnacht M, German Adrenocortical Carcinoma Study Group (2013) The role of surgery in the management of recurrent adrenocortical carcinoma. J Clin Endocrinol Metab 98:181–191CrossRefPubMed
4.
go back to reference Terzolo M, Angeli A, Fassnacht M, Daffara F, Tauchmanova L, Conton PA, Rossetto R, Buci L, Sperone P, Grossrubatscher E, Reimondo G, Bollito E, Papotti M, Saeger W, Hahner S, Koschker AC, Arvat E, Ambrosi B, Loli P, Lombardi G, Mannelli M, Bruzzi P, Mantero F, Allolio B, Dogliotti L, Berruti A (2007) Adjuvant mitotane treatment for adrenocortical carcinoma. New Engl J Med 356:2372–2380CrossRefPubMed Terzolo M, Angeli A, Fassnacht M, Daffara F, Tauchmanova L, Conton PA, Rossetto R, Buci L, Sperone P, Grossrubatscher E, Reimondo G, Bollito E, Papotti M, Saeger W, Hahner S, Koschker AC, Arvat E, Ambrosi B, Loli P, Lombardi G, Mannelli M, Bruzzi P, Mantero F, Allolio B, Dogliotti L, Berruti A (2007) Adjuvant mitotane treatment for adrenocortical carcinoma. New Engl J Med 356:2372–2380CrossRefPubMed
5.
go back to reference Stigliano A, Chiodini I, Giordano R, Faggiano A, Canu L, Della Casa S, Loli P, Luconi M, Mantero F, Terzolo M (2016) Management of adrenocortical carcinoma: a consensus statement of the Italian Society of Endocrinology (SIE). J Endocrinol Invest 39:103–121CrossRefPubMed Stigliano A, Chiodini I, Giordano R, Faggiano A, Canu L, Della Casa S, Loli P, Luconi M, Mantero F, Terzolo M (2016) Management of adrenocortical carcinoma: a consensus statement of the Italian Society of Endocrinology (SIE). J Endocrinol Invest 39:103–121CrossRefPubMed
6.
go back to reference Weiss LM, Medeiros LJ, Vickery AL Jr (1989) Pathologic features of prognostic significance in adrenocortical carcinoma. Am J Surg Pathol 13:202–206CrossRefPubMed Weiss LM, Medeiros LJ, Vickery AL Jr (1989) Pathologic features of prognostic significance in adrenocortical carcinoma. Am J Surg Pathol 13:202–206CrossRefPubMed
7.
go back to reference van’t Sant HP, Bouvy ND, Kazemier G, Bonjer HJ, Hop WC, Feelders RA, de Herder WW, de Krijger RR (2007) The prognostic value of two different histopathological scoring systems for adrenocortical carcinomas. Histopathology 51:239–245CrossRef van’t Sant HP, Bouvy ND, Kazemier G, Bonjer HJ, Hop WC, Feelders RA, de Herder WW, de Krijger RR (2007) The prognostic value of two different histopathological scoring systems for adrenocortical carcinomas. Histopathology 51:239–245CrossRef
8.
go back to reference Duregon E, Cappellesso R, Maffeis V, Zaggia B, Ventura L, Berruti A, Terzolo M, Fassina A, Volante M, Papotti M (2017) Validation of the prognostic role of the “Helsinki Score” in 225 cases of adrenocortical carcinoma. Hum Pathol 62:1–7CrossRefPubMed Duregon E, Cappellesso R, Maffeis V, Zaggia B, Ventura L, Berruti A, Terzolo M, Fassina A, Volante M, Papotti M (2017) Validation of the prognostic role of the “Helsinki Score” in 225 cases of adrenocortical carcinoma. Hum Pathol 62:1–7CrossRefPubMed
9.
go back to reference Libé R, Borget I, Ronchi CL, Zaggia B, Kroiss M, Kerkhofs T, Bertherat J, Volante M, Quinkler M, Chabre O, Bala M, Tabarin A, Beuschlein F, Vezzosi D, Deutschbein T, Borson-Chazot F, Hermsen I, Stell A, Fottner C, Leboulleux S, Hahner S, Mannelli M, Berruti A, Haak H, Terzolo M, Fassnacht M, Baudin E, ENSAT Network (2015) Prognostic factors in stage III–IV adrenocortical carcinomas (ACC): an European Network for the Study of Adrenal Tumor (ENSAT) study. Ann Oncol 2015(26):2119–2125CrossRef Libé R, Borget I, Ronchi CL, Zaggia B, Kroiss M, Kerkhofs T, Bertherat J, Volante M, Quinkler M, Chabre O, Bala M, Tabarin A, Beuschlein F, Vezzosi D, Deutschbein T, Borson-Chazot F, Hermsen I, Stell A, Fottner C, Leboulleux S, Hahner S, Mannelli M, Berruti A, Haak H, Terzolo M, Fassnacht M, Baudin E, ENSAT Network (2015) Prognostic factors in stage III–IV adrenocortical carcinomas (ACC): an European Network for the Study of Adrenal Tumor (ENSAT) study. Ann Oncol 2015(26):2119–2125CrossRef
10.
go back to reference Fassnacht M, Johanssen S, Quinkler M, Bucsky P, Willenberg HS, Beuschlein F, Terzolo M, Mueller HH, Hahner S, Allolio B, German Adrenocortical Carcinoma Registry Group, European Network for the Study of Adrenal Tumors (2009) Limited prognostic value of the 2004 International Union Against Cancer staging classification for adrenocortical carcinoma: proposal for a Revised TNM Classification. Cancer 115:243–250CrossRefPubMed Fassnacht M, Johanssen S, Quinkler M, Bucsky P, Willenberg HS, Beuschlein F, Terzolo M, Mueller HH, Hahner S, Allolio B, German Adrenocortical Carcinoma Registry Group, European Network for the Study of Adrenal Tumors (2009) Limited prognostic value of the 2004 International Union Against Cancer staging classification for adrenocortical carcinoma: proposal for a Revised TNM Classification. Cancer 115:243–250CrossRefPubMed
11.
go back to reference Beuschlein F, Weigel J, Saeger W, Kroiss M, Wild V, Daffara F, Libé R, Ardito A, Al Ghuzlan A, Quinkler M, Oßwald A, Ronchi CL, de Krijger R, Feelders RA, Waldmann J, Willenberg HS, Deutschbein T, Stell A, Reincke M, Papotti M, Baudin E, Tissier F, Haak HR, Loli P, Terzolo M, Allolio B, Müller HH, Fassnacht M (2015) Major prognostic role of Ki67 in localized adrenocortical carcinoma after complete resection. J Clin Endocrinol Metab 100:841–849CrossRefPubMed Beuschlein F, Weigel J, Saeger W, Kroiss M, Wild V, Daffara F, Libé R, Ardito A, Al Ghuzlan A, Quinkler M, Oßwald A, Ronchi CL, de Krijger R, Feelders RA, Waldmann J, Willenberg HS, Deutschbein T, Stell A, Reincke M, Papotti M, Baudin E, Tissier F, Haak HR, Loli P, Terzolo M, Allolio B, Müller HH, Fassnacht M (2015) Major prognostic role of Ki67 in localized adrenocortical carcinoma after complete resection. J Clin Endocrinol Metab 100:841–849CrossRefPubMed
12.
go back to reference Ronchi CL, Di Dalmazi G, Faillot S, Sbiera S, Assié G, Weigand I, Calebiro D, Schwarzmayr T, Appenzeller S, Rubin B et al (2016) Genetic landscape of sporadic unilateral adrenocortical adenomas without PRKACA p.Leu206Arg mutation. J Clin Endocrinol Metab 101:3526–3538CrossRefPubMed Ronchi CL, Di Dalmazi G, Faillot S, Sbiera S, Assié G, Weigand I, Calebiro D, Schwarzmayr T, Appenzeller S, Rubin B et al (2016) Genetic landscape of sporadic unilateral adrenocortical adenomas without PRKACA p.Leu206Arg mutation. J Clin Endocrinol Metab 101:3526–3538CrossRefPubMed
13.
go back to reference Ronchi CL, Sbiera S, Leich E, Henzel K, Rosenwald A, Allolio B, Fassnacht M (2013) Single nucleotide polymorphism array profiling of adrenocortical tumors—evidence for an adenoma carcinoma sequence? PLoS ONE 8:e73959CrossRefPubMedPubMedCentral Ronchi CL, Sbiera S, Leich E, Henzel K, Rosenwald A, Allolio B, Fassnacht M (2013) Single nucleotide polymorphism array profiling of adrenocortical tumors—evidence for an adenoma carcinoma sequence? PLoS ONE 8:e73959CrossRefPubMedPubMedCentral
14.
go back to reference Heaton JH, Wood MA, Kim AC, Lima LO, Barlaskar FM, Almeida MQ, Fragoso MC, Kuick R, Lerario AM, Simon DP et al (2012) Progression to adrenocortical tumorigenesis in mice and humans through insulin like growth factor 2 and β-catenin. Am J Pathol 181:1017–1033CrossRefPubMedPubMedCentral Heaton JH, Wood MA, Kim AC, Lima LO, Barlaskar FM, Almeida MQ, Fragoso MC, Kuick R, Lerario AM, Simon DP et al (2012) Progression to adrenocortical tumorigenesis in mice and humans through insulin like growth factor 2 and β-catenin. Am J Pathol 181:1017–1033CrossRefPubMedPubMedCentral
15.
go back to reference Drelon C, Berthon A, Ragazzon B, Tissier F, Bandiera R, Sahut-Barnola I, de Joussineau C, Batisse-Lignier M, Lefrançois-Martinez AM, Bertherat J et al (2012) Analysis of the role of Igf2 in adrenal tumour development in transgenic mouse models. PLoS ONE 2012(7):e44171CrossRef Drelon C, Berthon A, Ragazzon B, Tissier F, Bandiera R, Sahut-Barnola I, de Joussineau C, Batisse-Lignier M, Lefrançois-Martinez AM, Bertherat J et al (2012) Analysis of the role of Igf2 in adrenal tumour development in transgenic mouse models. PLoS ONE 2012(7):e44171CrossRef
16.
go back to reference Belmihoub I, Silvera S, Sibony M, Dousset B, Legmann P, Bertagna X, Bertherat J, Assié G (2017) From benign adrenal incidentaloma to adrenocortical carcinoma: an exceptional random event. Eur J Endocrinol 176:K15–K19CrossRefPubMed Belmihoub I, Silvera S, Sibony M, Dousset B, Legmann P, Bertagna X, Bertherat J, Assié G (2017) From benign adrenal incidentaloma to adrenocortical carcinoma: an exceptional random event. Eur J Endocrinol 176:K15–K19CrossRefPubMed
17.
go back to reference Juhlin CC, Goh G, Healy JM, Fonseca AL, Scholl UI, Stenman A, Kunstman JW, Brown TC, Overton JD, Mane SM, Nelson-Williams C, Bäckdahl M, Suttorp AC, Haase M, Choi M, Schlessinger J, Rimm DL, Höög A, Prasad ML, Korah R, Larsson C, Lifton RP, Carling T (2015) Whole-exome sequencing characterizes the landscape of somatic mutations and copy number alterations in adrenocortical carcinoma. J Clin Endocrinol Metab 100:E493–E502CrossRefPubMed Juhlin CC, Goh G, Healy JM, Fonseca AL, Scholl UI, Stenman A, Kunstman JW, Brown TC, Overton JD, Mane SM, Nelson-Williams C, Bäckdahl M, Suttorp AC, Haase M, Choi M, Schlessinger J, Rimm DL, Höög A, Prasad ML, Korah R, Larsson C, Lifton RP, Carling T (2015) Whole-exome sequencing characterizes the landscape of somatic mutations and copy number alterations in adrenocortical carcinoma. J Clin Endocrinol Metab 100:E493–E502CrossRefPubMed
18.
go back to reference Assié G, Letouzé E, Fassnacht M, Jouinot A, Luscap W, Barreau O, Omeiri H, Rodriguez S, Perlemoine K, René-Corail F, Elarouci N, Sbiera S, Kroiss M, Allolio B, Waldmann J, Quinkler M, Mannelli M, Mantero F, Papathomas T, De Krijger R, Tabarin A, Kerlan V, Baudin E, Tissier F, Dousset B, Groussin L, Amar L, Clauser E, Bertagna X, Ragazzon B, Beuschlein F, Libé R, de Reyniès A, Bertherat J (2014) Integrated genomic characterization of adrenocortical carcinoma. Nat Genet 46:607–612CrossRefPubMed Assié G, Letouzé E, Fassnacht M, Jouinot A, Luscap W, Barreau O, Omeiri H, Rodriguez S, Perlemoine K, René-Corail F, Elarouci N, Sbiera S, Kroiss M, Allolio B, Waldmann J, Quinkler M, Mannelli M, Mantero F, Papathomas T, De Krijger R, Tabarin A, Kerlan V, Baudin E, Tissier F, Dousset B, Groussin L, Amar L, Clauser E, Bertagna X, Ragazzon B, Beuschlein F, Libé R, de Reyniès A, Bertherat J (2014) Integrated genomic characterization of adrenocortical carcinoma. Nat Genet 46:607–612CrossRefPubMed
19.
go back to reference Zheng S, Cherniack AD, Dewal N, Moffitt RA, Danilova L, Murray BA, Lerario AM, Else T, Knijnenburg TA, Ciriello G, Kim S, Assie G, Morozova O, Akbani R, Shih J, Hoadley KA, Choueiri TK, Waldmann J, Mete O, Robertson AG, Wu HT, Raphael BJ, Shao L, Meyerson M, Demeure MJ, Beuschlein F, Gill AJ, Sidhu SB, Almeida MQ, Fragoso MC, Cope LM, Kebebew E, Habra MA, Whitsett TG, Bussey KJ, Rainey WE, Asa SL, Bertherat J, Fassnacht M, Wheeler DA, CancerGenome Atlas Research Network, Hammer GD, Giordano TJ, Verhaak RG (2016) Comprehensive pan-genomic characterization of adrenocortical carcinoma. Cancer Cell 9(29):723–736CrossRef Zheng S, Cherniack AD, Dewal N, Moffitt RA, Danilova L, Murray BA, Lerario AM, Else T, Knijnenburg TA, Ciriello G, Kim S, Assie G, Morozova O, Akbani R, Shih J, Hoadley KA, Choueiri TK, Waldmann J, Mete O, Robertson AG, Wu HT, Raphael BJ, Shao L, Meyerson M, Demeure MJ, Beuschlein F, Gill AJ, Sidhu SB, Almeida MQ, Fragoso MC, Cope LM, Kebebew E, Habra MA, Whitsett TG, Bussey KJ, Rainey WE, Asa SL, Bertherat J, Fassnacht M, Wheeler DA, CancerGenome Atlas Research Network, Hammer GD, Giordano TJ, Verhaak RG (2016) Comprehensive pan-genomic characterization of adrenocortical carcinoma. Cancer Cell 9(29):723–736CrossRef
20.
go back to reference Faillot S, Assié G (2016) ENDOCRINE TUMORS: the genomics of adrenocortical tumors. Eur J Endocrinol 174:R249–R265CrossRefPubMed Faillot S, Assié G (2016) ENDOCRINE TUMORS: the genomics of adrenocortical tumors. Eur J Endocrinol 174:R249–R265CrossRefPubMed
21.
go back to reference Giordano TJ, Thomas DG, Kuick R, Lizyness M, Misek DE, Smith AL, Sanders D, Aljundi RT, Gauger PG, Thompson NW, Taylor JM, Hanash SM (2003) Distinct transcriptional profiles of adrenocortical tumors uncovered by DNA microarray analysis. Am J Pathol 162:521–531CrossRefPubMedPubMedCentral Giordano TJ, Thomas DG, Kuick R, Lizyness M, Misek DE, Smith AL, Sanders D, Aljundi RT, Gauger PG, Thompson NW, Taylor JM, Hanash SM (2003) Distinct transcriptional profiles of adrenocortical tumors uncovered by DNA microarray analysis. Am J Pathol 162:521–531CrossRefPubMedPubMedCentral
22.
go back to reference Giordano TJ, Kuick R, Else T, Gauger PG, Vinco M, Bauersfeld J, Sanders D, Thomas DG, Doherty G, Hammer G (2009) Molecular classification and prognostication of adrenocortical tumors by transcriptome profiling. Clin Cancer Res 15:668–676CrossRefPubMedPubMedCentral Giordano TJ, Kuick R, Else T, Gauger PG, Vinco M, Bauersfeld J, Sanders D, Thomas DG, Doherty G, Hammer G (2009) Molecular classification and prognostication of adrenocortical tumors by transcriptome profiling. Clin Cancer Res 15:668–676CrossRefPubMedPubMedCentral
23.
go back to reference deFraipont F, ElAtifi M, Cherradi N, Le Moigne G, Defaye G, Houlgatte R, Bertherat J, Bertagna X, Plouin PF, Baudin E, Berr F, Gicquel C, Chabre O, Feige JJ (2005) Gene expression profiling of human adrenocortical tumors using complementary deoxyribonucleic acid microarrays identifies several candidate genes as markers of malignancy. J Clin Endocrinol Metab 90:1819–1829CrossRef deFraipont F, ElAtifi M, Cherradi N, Le Moigne G, Defaye G, Houlgatte R, Bertherat J, Bertagna X, Plouin PF, Baudin E, Berr F, Gicquel C, Chabre O, Feige JJ (2005) Gene expression profiling of human adrenocortical tumors using complementary deoxyribonucleic acid microarrays identifies several candidate genes as markers of malignancy. J Clin Endocrinol Metab 90:1819–1829CrossRef
24.
go back to reference deReyniès A, Assié G, Rickman DS, Tissier F, Groussin L, René-Corail F, Dousset B, Bertagna X, Clauser E, Bertherat J (2009) Gene expression profiling reveals a new classification of adrenocortical tumors and identifies molecular predictors of malignancy and survival. J Clin Oncol 27:1108–1115CrossRef deReyniès A, Assié G, Rickman DS, Tissier F, Groussin L, René-Corail F, Dousset B, Bertagna X, Clauser E, Bertherat J (2009) Gene expression profiling reveals a new classification of adrenocortical tumors and identifies molecular predictors of malignancy and survival. J Clin Oncol 27:1108–1115CrossRef
25.
go back to reference Soon PS, Tacon LJ, Gill AJ, Bambach CP, Sywak MS, Campbell PR, Yeh MW, Wong SG, Clifton-Bligh RJ, Robinson BG, Sidhu SB (2009) miR-195 and miR-483-5p identified as predictors of poor prognosis in adrenocortical cancer. Clin Cancer Res 15:7684–7692CrossRefPubMed Soon PS, Tacon LJ, Gill AJ, Bambach CP, Sywak MS, Campbell PR, Yeh MW, Wong SG, Clifton-Bligh RJ, Robinson BG, Sidhu SB (2009) miR-195 and miR-483-5p identified as predictors of poor prognosis in adrenocortical cancer. Clin Cancer Res 15:7684–7692CrossRefPubMed
26.
go back to reference Wang C, Sun Y, Wu H, Zhao D, Chen J (2014) Distinguishing adrenalcortical carcinomas and adenomas: a study of clinicopathological features and biomarkers. Histopathology 64:567–576CrossRefPubMed Wang C, Sun Y, Wu H, Zhao D, Chen J (2014) Distinguishing adrenalcortical carcinomas and adenomas: a study of clinicopathological features and biomarkers. Histopathology 64:567–576CrossRefPubMed
27.
go back to reference Ragazzon B, Libé R, Gaujoux S, Assié G, Fratticci A, Launay P, Clauser E, Bertagna X, Tissier F, de Reyniès A, Bertherat J (2010) Transcriptome analysis reveals that p53 and{beta}-catenin alterations occur in a group of aggressive adrenocortical cancers. Cancer Res 70:8276–8281CrossRefPubMed Ragazzon B, Libé R, Gaujoux S, Assié G, Fratticci A, Launay P, Clauser E, Bertagna X, Tissier F, de Reyniès A, Bertherat J (2010) Transcriptome analysis reveals that p53 and{beta}-catenin alterations occur in a group of aggressive adrenocortical cancers. Cancer Res 70:8276–8281CrossRefPubMed
28.
go back to reference Ragazzon B, Assié G, Bertherat J (2011) Transcriptome analysis of adrenocortical cancers: from molecular classification to the identification of new treatments. Endocr Relat Cancer 18:15–27CrossRef Ragazzon B, Assié G, Bertherat J (2011) Transcriptome analysis of adrenocortical cancers: from molecular classification to the identification of new treatments. Endocr Relat Cancer 18:15–27CrossRef
29.
go back to reference Assié G, Guillaud-Bataille M, Ragazzon B, Bertagna X, Bertherat J, Clauser E (2010) The pathophysiology, diagnosis and prognosis of adrenocortical tumors revisited by transcriptome analyses. Trends Endocrinol Metab 21:325–334CrossRefPubMed Assié G, Guillaud-Bataille M, Ragazzon B, Bertagna X, Bertherat J, Clauser E (2010) The pathophysiology, diagnosis and prognosis of adrenocortical tumors revisited by transcriptome analyses. Trends Endocrinol Metab 21:325–334CrossRefPubMed
30.
go back to reference Fragoso MC, Almeida MQ, Mazzuco TL, Mariani BM, Brito LP, Gonçalves TC, Alencar GA, Lima Lde O, Faria AM, Bourdeau I, Lucon AM, Freire DS, Latronico AC, Mendonca BB, Lacroix A, Lerario AM (2012) 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 166:61–67CrossRefPubMed Fragoso MC, Almeida MQ, Mazzuco TL, Mariani BM, Brito LP, Gonçalves TC, Alencar GA, Lima Lde O, Faria AM, Bourdeau I, Lucon AM, Freire DS, Latronico AC, Mendonca BB, Lacroix A, Lerario AM (2012) 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 166:61–67CrossRefPubMed
31.
go back to reference Kulis M, Esteller M (2010) DNA methylation and cancer. Adv Genet 70:27–56PubMed Kulis M, Esteller M (2010) DNA methylation and cancer. Adv Genet 70:27–56PubMed
32.
go back to reference Kalari S, Pfeifer GP (2010) Identification of driver and passenger DNA methylation in cancer by epigenomic analysis. Adv Genet 70:277–308PubMedPubMedCentral Kalari S, Pfeifer GP (2010) Identification of driver and passenger DNA methylation in cancer by epigenomic analysis. Adv Genet 70:277–308PubMedPubMedCentral
33.
go back to reference Rechache NS, Wang Y, Stevenson HS, Killian JK, Edelman DC, Merino M, Zhang L, Nilubol N, Stratakis CA, Meltzer PS, Kebebew E (2012) DNA methylation profiling identifies global methylation differences and markers of adrenocortical tumors. J Clin Endocrinol Metab 97(6):E1004–E1013CrossRefPubMedPubMedCentral Rechache NS, Wang Y, Stevenson HS, Killian JK, Edelman DC, Merino M, Zhang L, Nilubol N, Stratakis CA, Meltzer PS, Kebebew E (2012) DNA methylation profiling identifies global methylation differences and markers of adrenocortical tumors. J Clin Endocrinol Metab 97(6):E1004–E1013CrossRefPubMedPubMedCentral
34.
go back to reference Fonseca AL, Kugelberg J, Starker LF, Scholl U, Choi M, Hellman P, Åkerström G, Westin G, Lifton RP, Björklund P, Carling T (2012) Comprehensive DNA methylation analysis of benign and malignant adrenocortical tumors. Genes Chromosomes Cancer 51:949–960CrossRefPubMed Fonseca AL, Kugelberg J, Starker LF, Scholl U, Choi M, Hellman P, Åkerström G, Westin G, Lifton RP, Björklund P, Carling T (2012) Comprehensive DNA methylation analysis of benign and malignant adrenocortical tumors. Genes Chromosomes Cancer 51:949–960CrossRefPubMed
35.
go back to reference Barreau O, Assié G, Wilmot-Roussel H, Ragazzon B, Baudry C, Perlemoine K, René-Corail F, Bertagna X, Dousset B, Hamzaoui N, Tissier F, de Reynies A, Bertherat J (2013) Identification of a CpG island methylator phenotype in adrenocortical carcinomas. J Clin Endocrinol Metab 98:E174–E184CrossRefPubMed Barreau O, Assié G, Wilmot-Roussel H, Ragazzon B, Baudry C, Perlemoine K, René-Corail F, Bertagna X, Dousset B, Hamzaoui N, Tissier F, de Reynies A, Bertherat J (2013) Identification of a CpG island methylator phenotype in adrenocortical carcinomas. J Clin Endocrinol Metab 98:E174–E184CrossRefPubMed
36.
go back to reference Creemers SG, van Koetsveld PM, van Kemenade FJ, Papathomas TG, Franssen GJ, Dogan F, Eekhoff EM, van der Valk P, de Herder WW, Janssen JA, Feelders RA, Hofland LJ (2016) Methylation of IGF2 regulatory regions to diagnose adrenocortical carcinomas. Endocr Relat Cancer 23:727–737CrossRefPubMed Creemers SG, van Koetsveld PM, van Kemenade FJ, Papathomas TG, Franssen GJ, Dogan F, Eekhoff EM, van der Valk P, de Herder WW, Janssen JA, Feelders RA, Hofland LJ (2016) Methylation of IGF2 regulatory regions to diagnose adrenocortical carcinomas. Endocr Relat Cancer 23:727–737CrossRefPubMed
37.
go back to reference Jouinot A, Assie G, Libe R, Fassnacht M, Papathomas T, Barreau O, DE LA Villeon B, Faillot S, Hamzaoui N, Neou M, Perlemoine K, Rene-Corail F, Rodriguez S, Sibony M, Tissier F, Dousset B, Sbiera S, Ronchi C, Kroiss M, Korpershoek E, DE Krijger R, Waldmann J, Bartsch DK, Quinkler M, Haissaguerre M, Tabarin A, Chabre O, Sturm N, Luconi M, Mantero F, Mannelli M, Cohen R, Kerlan V, Touraine P, Barrande G, Groussin L, Bertagna X, Baudin E, Amar L, Beuschlein F, Clauser E, Coste J, Bertherat J (2017) DNA methylation is an independent prognostic marker of survival in adrenocortical cancer. J Clin Endocrinol Metab 102:923–932PubMed Jouinot A, Assie G, Libe R, Fassnacht M, Papathomas T, Barreau O, DE LA Villeon B, Faillot S, Hamzaoui N, Neou M, Perlemoine K, Rene-Corail F, Rodriguez S, Sibony M, Tissier F, Dousset B, Sbiera S, Ronchi C, Kroiss M, Korpershoek E, DE Krijger R, Waldmann J, Bartsch DK, Quinkler M, Haissaguerre M, Tabarin A, Chabre O, Sturm N, Luconi M, Mantero F, Mannelli M, Cohen R, Kerlan V, Touraine P, Barrande G, Groussin L, Bertagna X, Baudin E, Amar L, Beuschlein F, Clauser E, Coste J, Bertherat J (2017) DNA methylation is an independent prognostic marker of survival in adrenocortical cancer. J Clin Endocrinol Metab 102:923–932PubMed
38.
go back to reference Cherradi N (2016) microRNAs as potential biomarkers in adrenocortical cancer: progress and challenges. Front Endocrinol (Lausanne) 6:195 Cherradi N (2016) microRNAs as potential biomarkers in adrenocortical cancer: progress and challenges. Front Endocrinol (Lausanne) 6:195
39.
go back to reference Lerario AM, Moraitis A, Hammer GD (2014) Genetics and epigenetics of adrenocortical tumors. Mol Cell Endocrinol 386:67–84CrossRefPubMed Lerario AM, Moraitis A, Hammer GD (2014) Genetics and epigenetics of adrenocortical tumors. Mol Cell Endocrinol 386:67–84CrossRefPubMed
40.
go back to reference Igaz P, Igaz I, Nagy Z, Nyírő G, Szabó PM, Falus A, Patócs A, Rácz K (2015) MicroRNAs in adrenal tumors: relevance for pathogenesis, diagnosis, and therapy. Cell Mol Life Sci 72:417–428CrossRefPubMed Igaz P, Igaz I, Nagy Z, Nyírő G, Szabó PM, Falus A, Patócs A, Rácz K (2015) MicroRNAs in adrenal tumors: relevance for pathogenesis, diagnosis, and therapy. Cell Mol Life Sci 72:417–428CrossRefPubMed
41.
go back to reference Patterson EE, Holloway AK, Weng J, Fojo T, Kebebew E (2011) MicroRNA profiling of adrenocortical tumors reveals miR-483 as a marker of malignancy. Cancer 117:1630–1639CrossRefPubMed Patterson EE, Holloway AK, Weng J, Fojo T, Kebebew E (2011) MicroRNA profiling of adrenocortical tumors reveals miR-483 as a marker of malignancy. Cancer 117:1630–1639CrossRefPubMed
42.
go back to reference Özata DM, Caramuta S, Velázquez-Fernández D, Akçakaya P, Xie H, Höög A, Zedenius J, Bäckdahl M, Larsson C, Lui WO (2011) The role of microRNA deregulation in the pathogenesis of adrenocortical carcinoma. Endocr Relat Cancer 18:643–655CrossRefPubMedPubMedCentral Özata DM, Caramuta S, Velázquez-Fernández D, Akçakaya P, Xie H, Höög A, Zedenius J, Bäckdahl M, Larsson C, Lui WO (2011) The role of microRNA deregulation in the pathogenesis of adrenocortical carcinoma. Endocr Relat Cancer 18:643–655CrossRefPubMedPubMedCentral
43.
go back to reference Chabre O, Libé R, Assie G, Barreau O, Bertherat J, Bertagna X, Feige JJ, Cherradi N (2013) Serum miR-483-5p and miR-195 are predictive of recurrence risk in adrenocortical cancer patients. Endocr Relat Cancer 120:579–594 Chabre O, Libé R, Assie G, Barreau O, Bertherat J, Bertagna X, Feige JJ, Cherradi N (2013) Serum miR-483-5p and miR-195 are predictive of recurrence risk in adrenocortical cancer patients. Endocr Relat Cancer 120:579–594
44.
go back to reference Tömböl Z, Szabó PM, Molnár V, Wiener Z, Tölgyesi G, Horányi J, Riesz P, Reismann P, Patócs A, Likó I, Gaillard RC, Falus A, Rácz K, Igaz P (2009) Integrative molecular bioinformatics study of human adrenocortical tumors: microRNA, tissue-specific target prediction, and pathway analysis. Endocr Relat Cancer 16:895–906CrossRefPubMed Tömböl Z, Szabó PM, Molnár V, Wiener Z, Tölgyesi G, Horányi J, Riesz P, Reismann P, Patócs A, Likó I, Gaillard RC, Falus A, Rácz K, Igaz P (2009) Integrative molecular bioinformatics study of human adrenocortical tumors: microRNA, tissue-specific target prediction, and pathway analysis. Endocr Relat Cancer 16:895–906CrossRefPubMed
45.
go back to reference Schmitz KJ, Helwig J, Bertram S, Sheu SY, Suttorp AC, Seggewiss J, Willscher E, Walz MK, Worm K, Schmid KW (2011) Differential expression of microRNA-675, microRNA-139-3p and microRNA-335 in benign and malignant adrenocortical tumours. J Clin Pathol 64:529–535CrossRefPubMedPubMedCentral Schmitz KJ, Helwig J, Bertram S, Sheu SY, Suttorp AC, Seggewiss J, Willscher E, Walz MK, Worm K, Schmid KW (2011) Differential expression of microRNA-675, microRNA-139-3p and microRNA-335 in benign and malignant adrenocortical tumours. J Clin Pathol 64:529–535CrossRefPubMedPubMedCentral
46.
go back to reference Szabó DR, Luconi M, Szabó PM, Tóth M, Szücs N, Horányi J, Nagy Z, Mannelli M, Patócs A, Rácz K, Igaz P (2014) Analysis of circulating microRNAs in adrenocortical tumors. Lab Invest 94:331–339CrossRefPubMed Szabó DR, Luconi M, Szabó PM, Tóth M, Szücs N, Horányi J, Nagy Z, Mannelli M, Patócs A, Rácz K, Igaz P (2014) Analysis of circulating microRNAs in adrenocortical tumors. Lab Invest 94:331–339CrossRefPubMed
47.
go back to reference Assié G, Jouinot A, Bertherat J (2014) The ‘omics’ of adrenocortical tumours for personalized medicine. Nat Rev Endocrinol 10:215–228CrossRefPubMed Assié G, Jouinot A, Bertherat J (2014) The ‘omics’ of adrenocortical tumours for personalized medicine. Nat Rev Endocrinol 10:215–228CrossRefPubMed
48.
go back to reference Pantel K, Alix-Panabières C (2013) Real-time liquid biopsy in cancer patients: fact or fiction? Cancer Res 73:6384–6388CrossRefPubMed Pantel K, Alix-Panabières C (2013) Real-time liquid biopsy in cancer patients: fact or fiction? Cancer Res 73:6384–6388CrossRefPubMed
49.
go back to reference Alix-Panabières C, Pantel K (2016) Clinical applications of circulating tumor cells and circulating tumor DNA as liquid biopsy. Cancer Discov 6:479–491CrossRefPubMed Alix-Panabières C, Pantel K (2016) Clinical applications of circulating tumor cells and circulating tumor DNA as liquid biopsy. Cancer Discov 6:479–491CrossRefPubMed
50.
go back to reference Riethdorf S, Wikman H, Pantel K (2008) Review: biological relevance of disseminated tumor cells in cancer patients. Int J Cancer 123:1991–2006CrossRefPubMed Riethdorf S, Wikman H, Pantel K (2008) Review: biological relevance of disseminated tumor cells in cancer patients. Int J Cancer 123:1991–2006CrossRefPubMed
51.
go back to reference Pinzani P, Scatena C, Salvianti F, Corsini E, Canu L, Poli G, Paglierani M, Piccini V, Pazzagli M, Nesi G, Mannelli M, Luconi M (2013) Detection of circulating tumor cells in patients with adrenocortical carcinoma: a monocentric preliminary study. J Clin Endocrinol Metab 98:3731–3738CrossRefPubMed Pinzani P, Scatena C, Salvianti F, Corsini E, Canu L, Poli G, Paglierani M, Piccini V, Pazzagli M, Nesi G, Mannelli M, Luconi M (2013) Detection of circulating tumor cells in patients with adrenocortical carcinoma: a monocentric preliminary study. J Clin Endocrinol Metab 98:3731–3738CrossRefPubMed
52.
go back to reference Salvianti F, Canu L, Poli G, Armignacco R, Scatena C, Cantini G, Di Franco A, Gelmini S, Ercolino T, Pazzagli M, Nesi G, Mannelli M, Pinzani P, Luconi M (2017) New insights in the clinical and translational relevance of miR483-5p in adrenocortical cancer. Oncotarget 8:65525–65533CrossRefPubMedPubMedCentral Salvianti F, Canu L, Poli G, Armignacco R, Scatena C, Cantini G, Di Franco A, Gelmini S, Ercolino T, Pazzagli M, Nesi G, Mannelli M, Pinzani P, Luconi M (2017) New insights in the clinical and translational relevance of miR483-5p in adrenocortical cancer. Oncotarget 8:65525–65533CrossRefPubMedPubMedCentral
53.
go back to reference Perge P, Butz H, Pezzani R, Bancos I, Nagy Z, Pálóczi K, Nyírő G, Decmann Á, Pap E, Luconi M, Mannelli M, Buzás EI, Tóth M, Boscaro M, Patócs A, Igaz P (2017) Evaluation and diagnostic potential of circulating extracellular vesicle-associated microRNAs in adrenocortical tumors. Sci Rep 14(7):5474CrossRef Perge P, Butz H, Pezzani R, Bancos I, Nagy Z, Pálóczi K, Nyírő G, Decmann Á, Pap E, Luconi M, Mannelli M, Buzás EI, Tóth M, Boscaro M, Patócs A, Igaz P (2017) Evaluation and diagnostic potential of circulating extracellular vesicle-associated microRNAs in adrenocortical tumors. Sci Rep 14(7):5474CrossRef
54.
go back to reference Creemers SG, Esther Korpershoek E, Atmodimedjo PN, Dinjens WNM, van Koetsveld PM, Feelders RA, Hofland LJ (2017) Identification of mutations in cell-free circulating tumor DNA in adrenocortical carcinoma: a case series. J Clin Endocrinol Metab 102:3611–3615CrossRefPubMed Creemers SG, Esther Korpershoek E, Atmodimedjo PN, Dinjens WNM, van Koetsveld PM, Feelders RA, Hofland LJ (2017) Identification of mutations in cell-free circulating tumor DNA in adrenocortical carcinoma: a case series. J Clin Endocrinol Metab 102:3611–3615CrossRefPubMed
56.
go back to reference Batth IS, Mitra A, Manier S, Ghobrial IM, Menter D, Kopetz S, Li S (2017) Circulating tumor markers: harmonizing the yin and yang of CTCs and ctDNA for precision medicine. Ann Oncol 28:468–477PubMed Batth IS, Mitra A, Manier S, Ghobrial IM, Menter D, Kopetz S, Li S (2017) Circulating tumor markers: harmonizing the yin and yang of CTCs and ctDNA for precision medicine. Ann Oncol 28:468–477PubMed
57.
58.
go back to reference Fassnacht M, Terzolo M, Allolio B, Baudin E, Haak H, Berruti A, Welin S, Schade-Brittinger C, Lacroix A, Jarzab B, Sorbye H, Torpy DJ, Stepan V, Schteingart DE, Arlt W, Kroiss M et al (2012) Combination chemotherapy in advanced adrenocortical carcinoma. N Engl J Med 366:2189–2197CrossRefPubMed Fassnacht M, Terzolo M, Allolio B, Baudin E, Haak H, Berruti A, Welin S, Schade-Brittinger C, Lacroix A, Jarzab B, Sorbye H, Torpy DJ, Stepan V, Schteingart DE, Arlt W, Kroiss M et al (2012) Combination chemotherapy in advanced adrenocortical carcinoma. N Engl J Med 366:2189–2197CrossRefPubMed
59.
go back to reference Costa R, Carneiro BA, Tavora F, Pai SG, Kaplan JB, Chae YK, Chandra S, Kopp PA, Giles FJ (2016) The challenge of developmental therapeutics for adrenocortical carcinoma. Oncotarget 7:46734–46749PubMedPubMedCentral Costa R, Carneiro BA, Tavora F, Pai SG, Kaplan JB, Chae YK, Chandra S, Kopp PA, Giles FJ (2016) The challenge of developmental therapeutics for adrenocortical carcinoma. Oncotarget 7:46734–46749PubMedPubMedCentral
60.
go back to reference De Martino MC, Al Ghuzlan A, Aubert S, Assié G, Scoazec JY, Leboulleux S, Do Cao C, Libè R, Nozières C, Lombès M, Pattou F, Borson-Chazot F, Hescot S, Mazoyer C, Young J, Borget I, Colao A, Pivonello R, Soria JC, Bertherat J, Schlumberger M, Lacroix L, Baudin E (2013) Molecular screening for a personalized treatment approach in advanced adrenocortical cancer. J Clin Endocrinol Metab 98:4080–4088CrossRefPubMed De Martino MC, Al Ghuzlan A, Aubert S, Assié G, Scoazec JY, Leboulleux S, Do Cao C, Libè R, Nozières C, Lombès M, Pattou F, Borson-Chazot F, Hescot S, Mazoyer C, Young J, Borget I, Colao A, Pivonello R, Soria JC, Bertherat J, Schlumberger M, Lacroix L, Baudin E (2013) Molecular screening for a personalized treatment approach in advanced adrenocortical cancer. J Clin Endocrinol Metab 98:4080–4088CrossRefPubMed
61.
go back to reference Ross JS, Wang K, Rand JV, Gay L, Presta MJ, Sheehan CE, Ali SM, Elvin JA, Labrecque E, Hiemstra C, Buell J, Otto GA, Yelensky R, Lipson D, Morosini D, Chmielecki J, Miller VA, Stephens PJ (2014) Next-generation sequencing of adrenocortical carcinoma reveals new routes to targeted therapies. J Clin Pathol 67:968–973CrossRefPubMedPubMedCentral Ross JS, Wang K, Rand JV, Gay L, Presta MJ, Sheehan CE, Ali SM, Elvin JA, Labrecque E, Hiemstra C, Buell J, Otto GA, Yelensky R, Lipson D, Morosini D, Chmielecki J, Miller VA, Stephens PJ (2014) Next-generation sequencing of adrenocortical carcinoma reveals new routes to targeted therapies. J Clin Pathol 67:968–973CrossRefPubMedPubMedCentral
62.
go back to reference Creemers SG, Hofland LJ, Korpershoek E, Franssen GJ, van Kemenade FJ, de Herder WW, Feelders RA (2016) Future directions in the diagnosis and medical treatment of adrenocortical carcinoma. Endocr Relat Cancer 23(1):R43–R69PubMed Creemers SG, Hofland LJ, Korpershoek E, Franssen GJ, van Kemenade FJ, de Herder WW, Feelders RA (2016) Future directions in the diagnosis and medical treatment of adrenocortical carcinoma. Endocr Relat Cancer 23(1):R43–R69PubMed
64.
go back to reference Terzolo M, Zaggia B, Allasino B, De Francia S (2014) Practical treatment using mitotane for adrenocortical carcinoma. Curr Opin Endocrinol Diabetes Obes 21:159–165CrossRefPubMed Terzolo M, Zaggia B, Allasino B, De Francia S (2014) Practical treatment using mitotane for adrenocortical carcinoma. Curr Opin Endocrinol Diabetes Obes 21:159–165CrossRefPubMed
65.
go back to reference Anastas JN, Moon RT (2013) WNT signalling pathways as therapeutic targets in cancer. Nat Rev Cancer 13:11–26CrossRefPubMed Anastas JN, Moon RT (2013) WNT signalling pathways as therapeutic targets in cancer. Nat Rev Cancer 13:11–26CrossRefPubMed
Metadata
Title
Adrenocortical carcinoma: the dawn of a new era of genomic and molecular biology analysis
Authors
R. Armignacco
G. Cantini
L. Canu
G. Poli
T. Ercolino
M. Mannelli
M. Luconi
Publication date
01-05-2018
Publisher
Springer International Publishing
Published in
Journal of Endocrinological Investigation / Issue 5/2018
Electronic ISSN: 1720-8386
DOI
https://doi.org/10.1007/s40618-017-0775-y

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