Genome-wide analysis identifies MEN1 and MAX mutations and a neuroendocrine-like molecular heterogeneity in Quadruple WT GIST

Molecular Cancer Research

Volumn 15, Issue 5, 2017, Pages 553-562

  Pantaleo, Maria A ^a,b   Urbini, Milena ^b   Indio, Valentina ^b   Ravegnini, Gloria ^b   Nannini, Margherita ^a   De Luca, Matilde ^b   Tarantino, Giuseppe ^b   Angelini, Sabrina ^b   Gronchi, Alessandro ^c   Vincenzi, Bruno ^d   Grignani, Giovanni ^e   Colombo, Chiara ^c   Fumagalli, Elena ^c   Gatto, Lidia ^a   Saponara, Maristella ^a   Ianni, Manuela ^b   Paterini, Paola ^b   Santini, Donatella ^f   Pirini, M Giulia ^f   Ceccarelli, Claudio ^a   Altimari, Annalisa ^f   Gruppioni, Elisa ^f   Renne, Salvatore L ^c   Collini, Paola ^c   Stacchiotti, Silvia ^c   Brandi, Giovanni ^a   Casali, Paolo G ^c   Pinna, Antonio D ^a   Astolfi, Annalisa ^b   Biasco, Guido ^a,b   more..

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c NATIONAL CANCER INSTITUTE   (Italy)

^d UNIVERSITY CAMPUS BIO MEDICO   (Italy)

^e CANDIOLO CANCER INSTITUTE   (Italy)

^f F Addarii Institute of Oncology   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR RECEPTOR 1; G PROTEIN COUPLED RECEPTOR; GENOMIC DNA; MICRORNA; MULTIPLE ENDOCRINE NEOPLASIA TYPE 1 PROTEIN; MYC ASSOCIATED FACTOR X PROTEIN; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PROTEIN; PROTEIN P53; SUCCINATE DEHYDROGENASE; TRANSCRIPTOME; UNCLASSIFIED DRUG; ASCL1 PROTEIN, HUMAN; BASIC HELIX LOOP HELIX LEUCINE ZIPPER TRANSCRIPTION FACTOR; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; MAX PROTEIN, HUMAN; MEN1 PROTEIN, HUMAN; ONCOPROTEIN; TP53 PROTEIN, HUMAN;

ADULT; AGED; ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; FEMALE; GASTROINTESTINAL STROMAL TUMOR; GENE MUTATION; GENE OVEREXPRESSION; GENOME ANALYSIS; HUMAN; HUMAN TISSUE; MALE; MIDDLE AGED; NEUROENDOCRINE TUMOR; PRIORITY JOURNAL; QUADRUPLE WILD TYPE GASTROINTESTINAL STROMAL TUMOR; RNA SEQUENCE; RNA TRANSCRIPTION; SOMATIC MUTATION; TRANSCRIPTOMICS; WHOLE EXOME SEQUENCING; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; MUTATION; PROCEDURES; SEQUENCE ANALYSIS;

ADULT; AGED; BASIC HELIX-LOOP-HELIX LEUCINE ZIPPER TRANSCRIPTION FACTORS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; FEMALE; GASTROINTESTINAL STROMAL TUMORS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOME-WIDE ASSOCIATION STUDY; HUMANS; MALE; MICRORNAS; MIDDLE AGED; MUTATION; PROTO-ONCOGENE PROTEINS; SEQUENCE ANALYSIS, RNA; TUMOR SUPPRESSOR PROTEIN P53; WHOLE EXOME SEQUENCING;

EID: 85018324511     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-16-0376     Document Type: Article

References (46)

1. Corless CL, Barnett CM, Heinrich MC. Gastrointestinal stromal tumours: origin and molecular oncology. Nat Rev Cancer 2011;11:865-78.
2. Miettinen M, Wang ZF, Sarlomo-Rikala M, Osuch C, Rutkowski P, Lasota J. Succinate dehydrogenase-deficient GISTs: a clinicopathologic, immunohistochemical, and molecular genetic study of 66 gastric GISTs with predilection to young age. Am J Surg Pathol 2011;35:1712-21.
3. Gill AJ, Chou A, Vilain R, Clarkson A, Lui M, Jin R, et al. Immunohistochemistry for SDHB divides gastrointestinal stromal tumors (GISTs) into 2 distinct types. Am J Surg Pathol 2010;34:636-44.
4. Janeway KA, Kim SY, Lodish M, Nose V, Rustin P, Gaal J, et al. Defects in succinate dehydrogenase in gastrointestinal stromal tumors lacking KIT and PDGFRA mutations. Proc Natl Acad Sci USA 2011;108:314-8.
5. Pantaleo MA, Astolfi A, Urbini M, Nannini M, Paterini P, Indio V, et al. Analysis of all subunits, SDHA, SDHB, SDHC, SDHD, of the succinate dehydrogenase complex in KIT/PDGFRA wild-type GIST. EurJ Hum Genet 2014;22:32-9.
6. Pantaleo MA, Astolfi A, Indio V, Moore R, Thiessen N, Heinrich MC, et al. SDHA loss-of-function mutations in KIT-PDGFRA wild-type gastrointestinal stromal tumors identified by massively parallel sequencing. J Natl Cancer Inst 2011;103:983-7.
7. Miettinen M, Killian JK, Wang ZF, Lasota J, Lau C, Jones L, et al. Immunohistochemical loss of succinate dehydrogenase subunit A (SDHA) in gastrointestinal stromal tumors (GISTs) signals SDHA germline mutation. Am J Surg Pathol 2013;37:234-40.
8. Killian JK, Kim SY, Miettinen M, Smith C, Merino M, Tsokos M, et al. Succinate dehydrogenase mutation underlies global epigenomic divergence in gastrointestinal stromal tumor. Cancer Discov 2013;6:648-57.
9. Mason EF, Hornick JL. Succinate dehydrogenase deficiency is associated with decreased 5-hydroxymethylcytosine production in gastrointestinal stromal tumors: implications for mechanisms of tumorigenesis. Mod Pathol 2013;26:1492-7.
10. Killian JK, Miettinen M, Walker RL, Wang Y, Zhu YJ, Waterfall JJ, et al. Recurrent epimutation of SDHC in gastrointestinal stromal tumors. Sci Transl Med 2014;6:268ra177.
11. Urbini M, Astolfi A, Indio V, Heinrich MC, Corless CL, Nannini M, et al. SDHC methylation in gastrointestinal stromal tumors (GIST): a case report. BMC Med Genet 2015;28;16:87.
12. Kelly L, Bryan K, Kim SY, Janeway KA, Killian JK, Schildhaus HU, et al. Post-transcriptional dysregulation by miRNAs is implicated in the pathogenesis of gastrointestinal stromal tumor [GIST]. PLoS One 2013;8:e64102.
13. Pantaleo MA, Lolli C, Nannini M, Astolfi A, Indio V, Saponara M, et al. Good survival outcome of metastatic SDH-deficient gastrointestinal stromal tumors harboring SDHA mutations. Genet Med 2015;17:391-5.
14. Nannini M, Astolfi A, Paterini P, Urbini M, Santini D, Catena F, et al. Expression of IGF-1 receptor in KIT/PDGF receptor-a wild-type gastrointestinal stromal tumors with succinate dehydrogenase complex dysfunction. Future Oncol 2013;9:121-6.
15. Belinsky MG, Rink L, Flieder DB, Jahromi MS, Schiffman JD, Godwin AK, et al. Overexpression of insulin-like growth factor 1 receptor and frequent mutational inactivation of SDHA in wild-type SDHB-negative gastrointestinal stromal tumors. Genes Chromosomes Cancer 2013;52:214-24.
16. Pasini B, McWhinney SR, Bei T, Matyakhina L, Stergiopoulos S, Muchow M, et al. Clinical and molecular genetics of patients with the Carney-Stratakis syndrome and germline mutations of the genes coding for the succinate dehydrogenase subunits SDHB, SDHC, and SDHD. Eur J Hum Genet 2008;16:79-88.
17. Zhang L, Smyrk TC, Young WF Jr, Stratakis CA, Carney JA. Gastric stromal tumors in Carney triad are different clinically, pathologically, and behaviourally from sporadic gastric gastrointestinal stromal tumors: findings in 104 cases. Am J Surg Pathol 2010;34:53-64.
18. Haller F, Moskalev EA, Faucz FR, Barthelmeß S, Wiemann S, Bieg M, et al. Aberrant DNA hypermethylation of SDHC: a novel mechanism of tumor development in Carney triad. Endocr Relat Cancer 2014;21:567-77.
19. Daniels M, Lurkin I, Pauli R, Erbstösser E, Hildebrandt U, Hellwig K, et al. Spectrum of KIT/PDGFRA/BRAF mutations and phosphatidylinositol-3-kinase pathway gene alterations in gastrointestinal stromal tumors (GIST). Cancer Lett 2011;312:43-54.
20. Bajor J. Gastrointestinal stromal tumors in patients with type 1 neurofibromatosis. Clin Exp Med J 2009;3:247-54.
21. Pantaleo MA, Nannini M, Corless CL, Heinrich MC. Quadruple wildtype (WT) GIST: defining the subset of GISTs that lack abnormalities of KIT, PDGFRA, SDH, and the RAS signalling pathway. Cancer Med 2015;4:101-3.
22. Nannini M, Astolfi A, Urbini M, Indio V, Santini D, Heinrich MC, et al. Integrated genomic study of quadruple-WT GIST (KIT/PDGFRA/SDH/RAS pathway wild-type GIST). BMC Cancer 2014;14:685.
23. Belinsky MG, Rink L, Cai KQ, Capuzzi SJ, Hoang Y, Chien J, et al. Somatic loss of function mutations inneurofibromin1and MYC associated factor X genes identified by exome-wide sequencing in a wild-type GIST case. BMC Cancer 2015;15:887.
24. Gasparotto D, Rossi S, Polano M, Tamborini E, Lorenzetto E, Sbaraglia M, et al. Quadruple-negative GIST is a sentinel for unrecognized Neurofibromatosis Type 1 syndrome. Clin Cancer Res 2016; Jul. 7. pii: clincanres. 0152.2016.
25. Brenca M, Rossi S, Polano M, Gasparotto D, Zanatta L, Racanelli D, et al. Transcriptome sequencing identifies ETV6-NTRK3 as a gene fusion involved in GIST. J Pathol 2015;238:543-9.
26. Boikos SA, Pappo AS, Killian JK, LaQuaglia MP, Weldon CB, George S, et al. Molecular subtypes of KIT/PDGFRA wild-type gastrointestinal stromal tumors: a report from the National Institutes of Health Gastrointestinal Stromal Tumor Clinic. JAMA Oncol 2016;2:922-8.
27. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 2013;14:R36.
28. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009;25:1754-60.
29. Cingolani P, Platts A, Wang le L, Coon M, Nguyen T, Wang L, et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly (Austin). 2012;6:80-92.
30. Chen H, Biel MA, Borges MW, Thiagalingam A, Nelkin BD, Baylin SB, et al. Tissue-specific expression of human achaete-scute homologue-1 in neuroendocrine tumors: transcriptional regulation by dual inhibitory regions. Cell Growth Differ 1997;8:677-86.
31. Frattini V, Trifonov V, Chan JM, Castano A, Lia M, Abate F, et al. The integrated landscape of driver genomic alterations in glioblastoma. Nat Genet 2013;45:1141-9.
32. Muller PA, Vousden KH. P53 mutations in cancer. Nat Cell Biol 2013;15:2-8.
33. Zong L, Chen P, Xu Y. Correlation between P53 expression and malignant risk of gastrointestinal stromal tumors: evidence from 9 studies. Eur J Surg Oncol 2012;38:189-95.
34. Giusti F, Marini F, Brandi ML. Multiple Endocrine Neoplasia Type 1. 2005 Aug. 31 [updated 2015 Feb. 12]. In: Pagon RA, Adam MP, Ardinger HH, Wallace SE, Amemiya A, Bean LJH, Bird TD, Fong CT, Mefford HC, Smith RJH, Stephens K, editors. GeneReviews [Internet]. Seattle (WA): University of Washington, Seattle; 1993-2016.
35. Minetti M, Grossman A. Somatic and germline mutations in NETs: Implications fortheir diagnosis and management. Best Pract Res Clin Endocrinol Metab 2016;30:115-27.
36. Beadling C, Patterson J, Justusson E, Nelson D, Pantaleo MA, Hornick JL, et al. Gene expression of the IGF pathway family distinguishes subsets of gastrointestinal stromal tumors wild type for KIT and PDGFRA. Cancer Med 2013;2:21-31.
37. Pantaleo MA, Astolfi A, Nannini M, Ceccarelli C, Formica S, Santini D, et al. Differential expression of neural markers in KIT and PDGFRA wild-type gastrointestinal stromal tumours. Histopathology 2011;59:1071-80.
38. Kim MS, Chung NG, Kang MR, Yoo NJ, Lee SH. Genetic and expressional alterations of CHD genes in gastric and colorectal cancers. Histopathology 2011;58:660-8.
39. Gonzalez-Perez A, Jene-Sanz A, Lopez-Bigas N. The mutational landscape of chromatin regulatory factors across 4, 623 tumor samples. Genome Biol 2013;14:r106
40. Yang YJ, Song TY, Park J, Lee J, Lim J, Jang H, et al. Menin mediates epigenetic regulation via histone H3 lysine 9 methylation. Cell Death Dis 2013;4:e583.
41. BouchardC, DittrichO, KiermaierA, DohmannK, MenkelA, EilersM, et al. Regulation of cyclin D2 gene expression by the Myc/Max/Mad network: Myc-dependent TRRAP recruitment and histone acetylation at the cyclin D2 promoter. Genes Dev 2001;15:2042-7.
42. Nopparat J, Zhang J, Lu JP, Chen YH, Zheng D, Neufer PD, et al. d-Catenin, a Wnt/b-catenin modulator, reveals inducible mutagenesis promoting cancer cell survival adaptation and metabolic reprogramming. Oncogene 2015;34:1542-52.
43. Yoshida T, Hisamoto T, Akiba J, Koga H, Nakamura K, Tokunaga Y, et al. Spreds, inhibitors of the Ras/ERK signal transduction, are dysregulated in human hepatocellular carcinoma and linked to the malignant phenotype of tumors. Oncogene 2006;25:6056-66.
44. Agelopoulos K, Richter GH, Schmidt E, Dirksen U, von Heyking K, Moser B, et al. Deep sequencing in conjunction with expression and functional analyses reveals activation of FGFR1 in Ewing Sarcoma. Clin Cancer Res 2015;21:4935-46.
45. Shi E, Wang K, Ross JR, Tang C-M, Harismendy O, Ali S, et al. Comprehensive genomic profiling of quadruple (KIT/PDGFRA/SDH/RAS pathway) wild-type gastrointestinal stromal tumors. CTOS 2015. Paper 030.
46. Heinrich MC, Kang G, Warrick A, Corless CL, Beadling C. Oncogenic receptor tyrosine kinase (RTK) translocations in a subset of quadruple wild-type gastrointestinal stromal tumors (GIST). J Clin Oncol 34, 2016 (suppl; abstr 11012).