Genetics of Gastrointestinal Stromal Tumors A Heterogeneous Family of Tumors?

Surgical Pathology Clinics

Volumn 8, Issue 3, 2015, Pages 515-524

  Patil, Deepa T ^a   Rubin, Brian P ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

Author keywords

BRAF; GIST; KIT; PDGFRA; Succinate dehydrogenase

Indexed keywords

B RAF KINASE; IMATINIB; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; STEM CELL FACTOR; SUCCINATE DEHYDROGENASE; BRAF PROTEIN, HUMAN; SDHB PROTEIN, HUMAN; STEM CELL FACTOR RECEPTOR;

BRAF GENE; CARNEY COMPLEX; CARNEY STRATAKIS SYNDROME; DISEASE ACTIVITY; DISEASE ASSOCIATION; ENZYME ACTIVITY; ENZYME DEFECT; ENZYME DEFICIENCY; FAMILIAL CANCER; GASTROINTESTINAL STROMAL TUMOR; GENE MUTATION; GENETIC DISORDER; GENETIC HETEROGENEITY; GENOTYPE; HUMAN; KIT GENE; MOLECULAR GENETICS; MOLECULAR PATHOLOGY; NEUROFIBROMATOSIS; NONHUMAN; PDGFRA GENE; PRIORITY JOURNAL; REVIEW; SYNDROME; CHEMODECTOMA; CHONDROMA; DEFICIENCY; GENETICS; LEIOMYOSARCOMA; LUNG TUMOR; MUTATION; NEUROFIBROMATOSIS TYPE 1; PARAGANGLIOMA; PATHOLOGY; STOMACH TUMOR;

CHONDROMA; GASTROINTESTINAL STROMAL TUMORS; GENOTYPE; HUMANS; LEIOMYOSARCOMA; LUNG NEOPLASMS; MUTATION; NEOPLASTIC SYNDROMES, HEREDITARY; NEUROFIBROMATOSIS 1; PARAGANGLIOMA; PARAGANGLIOMA, EXTRA-ADRENAL; PROTO-ONCOGENE PROTEINS B-RAF; PROTO-ONCOGENE PROTEINS C-KIT; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR ALPHA; STOMACH NEOPLASMS; SUCCINATE DEHYDROGENASE;

EID: 84940957971     PISSN: 18759181     EISSN: 18759157     Source Type: Journal    
DOI: 10.1016/j.path.2015.05.006     Document Type: Review

References (59)

1. Hirota S., Isozaki K., Moriyama Y., et al. Gain-of-function mutations of c-kit in human gastrointestinal stromal tumors. Science 1998, 279:577-580.
2. Sommer G., Agosti V., Ehlers I., et al. Gastrointestinal stromal tumors in a mouse model by targeted mutation of the Kit receptor tyrosine kinase. Proc Natl Acad Sci U S A 2003, 100:6706-6711.
3. Rubin B.P., Antonescu C.R., Scott-Browne J.P., et al. A knock-in mouse model of gastrointestinal stromal tumor harboring kit K641E. Cancer Res 2005, 65:6631-6639.
4. Lasota J., Corless C.L., Heinrich M.C., et al. Clinicopathologic profile of gastrointestinal stromal tumors (GISTs) with primary KIT exon 13 or exon 17 mutations: a multicenter study on 54 cases. Mod Pathol 2008, 21:476-484.
5. van Nederveen F.H., Gaal J., Favier J., et al. An immunohistochemical procedure to detect patients with paraganglioma and phaeochromocytoma with germline SDHB, SDHC, or SDHD gene mutations: a retrospective and prospective analysis. Lancet Oncol 2009, 10:764-771.
6. Gill A.J., Chou A., Vilain R.E., et al. "Pediatric-type" gastrointestinal stromal tumors are SDHB negative ("type 2") GISTs. Am J Surg Pathol 2011, 35:1245-1247. [author reply: 1247-8].
7. Gaal J., Stratakis C.A., Carney J.A., et al. SDHB immunohistochemistry: a useful tool in the diagnosis of Carney-Stratakis and Carney triad gastrointestinal stromal tumors. Mod Pathol 2011, 24:147-151.
8. Janeway K.A., Kim S.Y., Lodish M., et al. Defects in succinate dehydrogenase in gastrointestinal stromal tumors lacking KIT and PDGFRA mutations. Proc Natl Acad Sci U S A 2011, 108:314-318.
9. Miettinen M., Wang Z.F., Sarlomo-Rikala M., et al. 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, 35:1712-1721.
10. Doyle L.A., Nelson D., Heinrich M.C., et al. Loss of succinate dehydrogenase subunit B (SDHB) expression is limited to a distinctive subset of gastric wild-type gastrointestinal stromal tumours: a comprehensive genotype-phenotype correlation study. Histopathology 2012, 61:801-809.
11. Agaram N.P., Wong G.C., Guo T., et al. Novel V600E BRAF mutations in imatinib-naive and imatinib-resistant gastrointestinal stromal tumors. Genes Chromosomes Cancer 2008, 47:853-859.
12. Agaimy A., Terracciano L.M., Dirnhofer S., et al. V600E BRAF mutations are alternative early molecular events in a subset of KIT/PDGFRA wild-type gastrointestinal stromal tumours. J Clin Pathol 2009, 62:613-616.
13. Hostein I., Faur N., Primois C., et al. BRAF mutation status in gastrointestinal stromal tumors. Am J Clin Pathol 2010, 133:141-148.
14. Miranda C., Nucifora M., Molinari F., et al. KRAS and BRAF mutations predict primary resistance to imatinib in gastrointestinal stromal tumors. Clin Cancer Res 2012, 18:1769-1776.
15. Maertens O., Prenen H., Debiec-Rychter M., et al. Molecular pathogenesis of multiple gastrointestinal stromal tumors in NF1 patients. Hum Mol Genet 2006, 15:1015-1023.
16. Heinrich M.C., Corless C.L., Demetri G.D., et al. Kinase mutations and imatinib response in patients with metastatic gastrointestinal stromal tumor. J Clin Oncol 2003, 21:4342-4349.
17. Corless C.L., Fletcher J.A., Heinrich M.C. Biology of gastrointestinal stromal tumors. J Clin Oncol 2004, 22:3813-3825.
18. Martin J., Poveda A., Llombart-Bosch A., et al. Deletions affecting codons 557-558 of the c-KIT gene indicate a poor prognosis in patients with completely resected gastrointestinal stromal tumors: a study by the Spanish Group for Sarcoma Research (GEIS). J Clin Oncol 2005, 23:6190-6198.
19. Heinrich M.C., Maki R.G., Corless C.L., et al. Primary and secondary kinase genotypes correlate with the biological and clinical activity of sunitinib in imatinib-resistant gastrointestinal stromal tumor. J Clin Oncol 2008, 26:5352-5359.
20. Miettinen M., Sobin L.H., Lasota J. Gastrointestinal stromal tumors of the stomach: a clinicopathologic, immunohistochemical, and molecular genetic study of 1765 cases with long-term follow-up. Am J Surg Pathol 2005, 29:52-68.
21. Miettinen M., Makhlouf H., Sobin L.H., et al. Gastrointestinal stromal tumors of the jejunum and ileum: a clinicopathologic, immunohistochemical, and molecular genetic study of 906 cases before imatinib with long-term follow-up. Am J Surg Pathol 2006, 30:477-489.
22. Lux M.L., Rubin B.P., Biase T.L., et al. KIT extracellular and kinase domain mutations in gastrointestinal stromal tumors. Am J Surg Pathol 2000, 156:791-795.
23. Kunstlinger H., Huss S., Merkelbach-Bruse S., et al. Gastrointestinal stromal tumors with KIT exon 9 mutations: Update on genotype-phenotype correlation and validation of a high-resolution melting assay for mutational testing. Am J Surg Pathol 2013, 37:1648-1659.
24. Gastrointestinal stromal tumor meta-analysis group (metaGIST) Comparison of two doses of imatinib for the treatment of unresectable or metastatic gastrointestinal stromal tumors: a meta-analysis of 1,640 patients. J Clin Oncol 2010, 28:1247-1253.
25. Stenman G., Eriksson A., Claesson-Welsh L. Human PDGFA receptor gene maps to the same region on chromosome 4 as the KIT oncogene. Genes Chromosomes Cancer 1989, 1:155-158.
26. Heinrich M.C., Corless C.L., Duensing A., et al. PDGFRA activating mutations in gastrointestinal stromal tumors. Science 2003, 299:708-710.
27. Neuhann T.M., Mansmann V., Merkelbach-Bruse S., et al. A novel germline KIT mutation (p.L576P) in a family presenting with juvenile onset of multiple gastrointestinal stromal tumors, skin hyperpigmentations, and esophageal stenosis. Am J Surg Pathol 2013, 37:898-905.
28. Ponti G., Luppi G., Martorana D., et al. Gastrointestinal stromal tumor and other primary metachronous or synchronous neoplasms as a suspicion criterion for syndromic setting. Oncol Rep 2010, 23:437-444.
29. Nishida T., Hirota S., Taniguchi M., et al. Familial gastrointestinal stromal tumours with germline mutation of the KIT gene. Nat Genet 1998, 19:323-324.
30. Burgoyne A.M., Somaiah N., Sicklick J.K. Gastrointestinal stromal tumors in the setting of multiple tumor syndromes. Curr Opin Oncol 2014, 26:408-414.
31. O'Riain C., Corless C.L., Heinrich M.C., et al. Gastrointestinal stromal tumors: insights from a new familial GIST kindred with unusual genetic and pathologic features. Am J Surg Pathol 2005, 29:1680-1683.
32. Kleinbaum E.P., Lazar A.J., Tamborini E., et al. Clinical, histopathologic, molecular and therapeutic findings in a large kindred with gastrointestinal stromal tumor. Int J Cancer 2008, 122:711-718.
33. Li F.P., Fletcher J.A., Heinrich M.C., et al. Familial gastrointestinal stromal tumor syndrome: phenotypic and molecular features in a kindred. J Clin Oncol 2005, 23:2735-2743.
34. Agarwal R., Robson M. Inherited predisposition to gastrointestinal stromal tumor. Hematol Oncol Clin North Am 2009, 23:1-13. vii.
35. Boikos S.A., Stratakis C.A. The genetic landscape of gastrointestinal stromal tumor lacking KIT and PDGFRA mutations. Endocrine 2014, 47:401-408.
36. Selak M.A., Armour S.M., MacKenzie E.D., et al. Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-alpha prolyl hydroxylase. Cancer Cell 2005, 7:77-85.
37. Killian J.K., Kim S.Y., Miettinen M., et al. Succinate dehydrogenase mutation underlies global epigenomic divergence in gastrointestinal stromal tumor. Cancer Discov 2013, 3:648-657.
38. Lasota J., Wang Z., Kim S.Y., et al. Expression of the receptor for type i insulin-like growth factor (IGF1R) in gastrointestinal stromal tumors: an immunohistochemical study of 1078 cases with diagnostic and therapeutic implications. Am J Surg Pathol 2013, 37:114-119.
39. Mahadevan D., Theiss N., Morales C., et al. Novel receptor tyrosine kinase targeted combination therapies for imatinib-resistant gastrointestinal stromal tumors (GIST). Oncotarget 2015, 6(4):1954-1966.
40. Killian J.K., Miettinen M., Walker R.L., et al. Recurrent epimutation of SDHC in gastrointestinal stromal tumors. Sci Transl Med 2014, 6:268ra177.
41. Miettinen M., Lasota J. Histopathology of gastrointestinal stromal tumor. J Surg Oncol 2011, 104:865-873.
42. Doyle L.A., Hornick J.L. Gastrointestinal stromal tumours: from KIT to succinate dehydrogenase. Histopathology 2014, 64:53-67.
43. Pappo A.S., Janeway K., Laquaglia M., et al. Special considerations in pediatric gastrointestinal tumors. J Surg Oncol 2011, 104:928-932.
44. Janeway K.A., Pappo A. Treatment guidelines for gastrointestinal stromal tumors in children and young adults. J Pediatr Hematol Oncol 2012, 34(Suppl 2):S69-S72.
45. Pasini B., McWhinney S.R., Bei T., 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.
46. Carney J.A. Gastric stromal sarcoma, pulmonary chondroma, and extra-adrenal paraganglioma (Carney Triad): natural history, adrenocortical component, and possible familial occurrence. Mayo Clin Proc 1999, 74:543-552.
47. Carney J.A., Stratakis C.A. Familial paraganglioma and gastric stromal sarcoma: a new syndrome distinct from the Carney triad. Am J Med Genet 2002, 108:132-139.
48. Matyakhina L., Bei T.A., McWhinney S.R., et al. Genetics of Carney triad: recurrent losses at chromosome 1 but lack of germline mutations in genes associated with paragangliomas and gastrointestinal stromal tumors. J Clin Endocrinol Metab 2007, 92:2938-2943.
49. Haller F., Moskalev E.A., Faucz F.R., et al. Aberrant DNA hypermethylation of SDHC: a novel mechanism of tumor development in Carney triad. Endocr Relat Cancer 2014, 21:567-577.
50. Oudijk L., Gaal J., Korpershoek E., et al. SDHA mutations in adult and pediatric wild-type gastrointestinal stromal tumors. Mod Pathol 2013, 26:456-463.
51. Wagner A.J., Remillard S.P., Zhang Y.X., et al. Loss of expression of SDHA predicts SDHA mutations in gastrointestinal stromal tumors. Mod Pathol 2013, 26:289-294.
52. Miettinen M., Killian J.K., Wang Z.F., et al. Immunohistochemical loss of succinate dehydrogenase subunit A (SDHA) in gastrointestinal stromal tumors (GISTs) signals SDHA germline mutation. Am J Surg Pathol 2013, 37:234-240.
53. Capper D., Preusser M., Habel A., et al. Assessment of BRAF V600E mutation status by immunohistochemistry with a mutation-specific monoclonal antibody. Acta Neuropathol 2011, 122:11-19.
54. Patil D., Shuang M., Konishi M., et al. Utility of BRAF V600E mutation-specific immunohistochemistry in detecting BRAF V600E-mutated gastrointestinal stromal tumors 2015, American Journal of Clinical Pathology, in press.
55. Daniels M., Lurkin I., Pauli R., 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.
56. Rubin B.P., Heinrich M.C., Corless C.L. Gastrointestinal stromal tumour. Lancet 2007, 369:1731-1741.
57. Takazawa Y., Sakurai S., Sakuma Y., et al. Gastrointestinal stromal tumors of neurofibromatosis type I (von Recklinghausen's disease). Am J Surg Pathol 2005, 29:755-763.
58. Pantaleo M.A., Nannini M., Corless C.L., et al. Quadruple wild-type (WT) GIST: defining the subset of GIST that lacks abnormalities of KIT, PDGFRA, SDH, or RAS signaling pathways. Cancer Med 2015, 4:101-103.
59. Miettinen M., Lasota J. Gastrointestinal stromal tumors: pathology and prognosis at different sites. Semin Diagn Pathol 2006, 23:70-83.