Gene Expression Patterns of Hemizygous and Heterozygous KIT Mutations Suggest Distinct Oncogenic Pathways: A Study in NIH3T3 Cell Lines and GIST Samples

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Bachet, Jean Baptiste ^a,b,c   Tabone Eglinger, Séverine ^d,g,h   Dessaux, Sophie ^d,g,h   Besse, Anthony ^d,g,h   Brahimi Adouane, Sabrina ^a,e   Emile, Jean François ^a,e   Blay, Jean Yves ^d,f   Alberti, Laurent ^d,f  

^a University of Versailles Saint Quentin en Yvelines   (France)

^b ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d UNIVERSITÉ DE LYON   (France)

^e HÔPITAL AMBROISE PARÉ   (France)

^f CENTRE LÉON BÉRARD   (France)

^g UNIVERSITÉ LYON 1   (France)

^h CENTRE DE RECHERCHE EN CANCÉROLOGIE DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; MEMBRANE PROTEIN; MICRORNA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN RGS 16; UNCLASSIFIED DRUG;

ADULT; AGED; ALLELE; ANIMAL CELL; ARTICLE; CARCINOGENESIS; CLINICAL ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO CELL; FEMALE; FIBROBLAST; GASTROINTESTINAL STROMAL TUMOR; GENE; GENE CLUSTER; GENE CONTROL; GENE DELETION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENE LOCATION; GENE MUTATION; HEMIZYGOSITY; HETEROZYGOSITY; HUMAN; KIT GENE; MALE; MOUSE; NONHUMAN; SIGNAL TRANSDUCTION;

ALLELES; ANALYSIS OF VARIANCE; ANIMALS; CLUSTER ANALYSIS; EXONS; GASTROINTESTINAL STROMAL TUMORS; GENE EXPRESSION REGULATION, NEOPLASTIC; HEMIZYGOTE; HETEROZYGOTE; HOMOZYGOTE; HUMANS; MICE; MICRORNAS; MUTATION; NIH 3T3 CELLS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PRINCIPAL COMPONENT ANALYSIS; PROTO-ONCOGENE PROTEINS C-KIT; RNA, MESSENGER;

EID: 84876084590     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0061103     Document Type: Article

References (64)

1. Cassier PA, Ducimetière F, Lurkin A, Ranchère-Vince D, Scoazec JY, et al. (2010) A prospective epidemiological study of new incident GISTs during two consecutive years in Rhône Alpes region: incidence and molecular distribution of GIST in a European region. Br J Cancer 13: 165-170.
2. Heinrich MC, Corless CL, Duensing A, McGreevey L, Chen CJ, et al. (2003) PDGFRA activating mutations in gastrointestinal stromal tumors. Science 299: 708-710.
3. Hirota S, Isozaki K, Moriyama Y, Hashimoto K, Nishida T, et al. (1998) Gain-of-function mutations of c-kit in human gastrointestinal stromal tumors. Science 279: 577-580.
4. Rubin BP, Heinrich MC, Corless CL, (2007) Gastrointestinal stromal tumour. Lancet 369: 1731-1741.
5. Bachet JB, Hostein I, Le Cesne A, Brahimi S, Beauchet A, et al. (2009) Prognosis and predictive value of KIT exon 11 deletion in GISTs. Br J Cancer 101: 7-11.
6. Corless CL, Fletcher JA, Heinrich MC, (2004) Biology of gastrointestinal tumors. J Clin Oncol 22: 3813-3825.
7. Emile JF, Théou N, Tabone S, Cortez A, Terrier P, et al. (2004) Clinicopathologic, phenotypic, and genotypic characteristics of gastrointestinal mesenchymal tumors. Clin Gastroenterol Hepatol 2: 597-605.
8. Blanke CD, Rankin C, Demetri GD, Ryan CW, von Mehren M, et al. (2008) Phase III randomized, intergroup trial assessing imatinib mesylate at two dose levels in patients with unresectable or metastatic gastrointestinal stromal tumors expressing the kit receptor tyrosine kinase: S0033. J Clin Oncol 26: 626-632.
9. DeMatteo RP, Ballman KV, Antonescu CR, Maki RG, Pisters PW, et al. (2009) Adjuvant imatinib mesylate after resection of localised, primary gastrointestinal stromal tumour: a randomised, double-blind, placebo-controlled trial. Lancet 373: 1097-1104.
10. Verweij J, Casali PG, Zalcberg J, LeCesne A, Reichardt P, et al. (2004) Progression-free survival in gastrointestinal stromal tumours with high-dose imatinib: randomised trial. Lancet 364: 1127-1134.
11. Debiec-Rychter M, Sciot R, Le Cesne A, Schlemmer M, Hohenberger P, et al. (2006) KIT mutations and dose selection for imatinib in patients with advanced gastrointestinal stromal tumours. Eur J Cancer 42: 1093-1103.
12. Heinrich MC, Corless CL, Demetri GD, Blanke CD, von Mehren M, et al. (2003) Kinase mutations and imatinib response in patients with metastatic gastrointestinal stromal tumor. J Clin Oncol 21: 4342-4349.
13. Emile JF, Bachet JB, Tabone-Eglinger S, Terrier P, Vignault JM, (2008) GIST with homozygous KIT exon 11 mutations. Lab Invest 88: 456-457.
14. Lasota J, vel Dobosz AJ, Wasag B, Wozniak A, Kraszewska E, et al. (2007) Presence of homozygous KIT exon 11 mutations is strongly associated with malignant clinical behavior in gastrointestinal stromal tumors. Lab Invest 87: 1029-1041.
15. Wallander ML, Willmore-Payne C, Layfield LJ, (2011) C-KIT and PDGFRA zygosity in gastrointestinal stromal tumors: Correlation with tumor site, tumor size, exon, and CD117 immunohistochemistry. Appl Immunohistochem Mol Morphol 19: 21-27.
16. Blume-Jensen P, Claesson-Welsh L, Siegbahn A, Zsebo KM, Westermark B, et al. (1991) Activation of the human c-kit product by ligand-induced dimerization mediates circular actin reorganization and chemotaxis. EMBO J 10: 4121-4128.
17. Mol CD, Dougan DR, Schneider TR, Skene RJ, Kraus ML, et al. (2004) Structural basis for the autoinhibition and STI-571 inhibition of c-Kit tyrosine kinase. J Biol Chem 279: 31655-31663.
18. Roskoski R, (2005) Structure and regulation of Kit protein-tyrosine kinase - the stem cell factor receptor. Biochem Biophys Res Commun 338: 1307-1315.
19. Tabone-Eglinger S, Subra F, El Sayadi H, Alberti L, Tabone E, et al. (2008) KIT mutations induce intracellular retention and activation of an immature form of the KIT protein in gastrointestinal stromal tumors. Clin Cancer Res 14: 2285-2294.
20. Xiang Z, Kreisel F, Cain J, Colson A, Tomasson MH, (2007) Neoplasia driven mutant c-KIT is mediated by intracellular, not plasma membrane, receptor signaling. Mol Cell Biol 27: 267-282.
21. Brahimi-Adouane S, Bachet JB, Tabone-Eglinger S, Subra F, Capron C, et al. (2012) Effects of endoplasmic reticulum stressors on maturation and signaling of hemizygous and heterozygous wild type and mutants forms of KIT. Mol Oncol (in press).
22. Casteran N, De Sepulveda P, Beslu N, Aoubala M, Letard S, et al. (2003) Signal transduction by several KIT juxtamembrane domain mutations. Oncogene 22: 4710-4722.
23. Pear WS, Miller JP, Xu L, Pui JC, Soffer B, et al. (1998) Efficient and rapid induction of a chronic myelogenous leukemia-like myeloproliferative disease in mice receiving P210 bcr/abl-transduced bone marrow. Blood 92: 3780-4003.
24. Emile JF, Lemoine A, Bienfait N, Terrier P, Azoulay D, et al. (2002) Length analysis of polymerase chain reaction products: a sensitive and reliable technique for the detection of mutations in KIT exon 11 in gastrointestinal stromal tumors. Diagn Mol Pathol 11: 107-112.
25. Gougelet A, Perez J, Pissaloux D, Besse A, Duc A, et al. (2011) miRNA Profiling: How to bypass the current difficulties in the diagnosis and treatment of sarcomas. Sarcoma 13: ID 460650.
26. Casali PG, Jost L, Reichardt P, Schlemmer M, Blay JY (2008) Gastrointestinal stromal tumors: ESMO clinical recommendations for diagnosis, treatment and follow-up. Ann Oncol (Suppl. 2): ii35-8.
27. Rubin BP, Antonescu CR, Scott-Browne JP, Comstock ML, Gu Y, et al. (2005) A knock-in mouse model of gastrointestinal stromal tumor harboring kit K641E. Cancer Res 2005 65: 6631-6639.
28. Sommer G, Agosti V, Ehlers I, Rossi F, Corbacioglu S, et al. (2003) Gastrointestinal stromal tumors in a mouse model by targeted mutation of the Kit receptor tyrosine kinase. Proc Natl Acad Sci U S A 100: 6706-6711.
29. Liang G, Bansal G, Xie Z, Druey KM, (2009) RGS16 inhibits breast cancer cell growth by mitigating phosphatidylinositol 3-kinase signaling. J Biol Chem 284: 21719-21727.
30. Kim JH, Lee JY, Lee KT, Lee JK, Lee KH, et al. (2010) RGS16 and FosB underexpressed in pancreatic cancer with lymph node metastasis promote tumor progression. Tumour Biol 31: 541-548.
31. Ceder R, Haig Y, Merne M, Hansson A, Zheng X, et al. (2012) Differentiation-promoting culture of competent and noncompetent keratinocytes identifies biomarkers for head and neck cancer. Am J Pathol 180: 457-472.
32. Mok SC, Bonome T, Vathipadiekal V, Bell A, Johnson ME, et al. (2009) A gene signature predictive for outcome in advanced ovarian cancer identifies a survival factor: microfibril-associated glycoprotein 2. Cancer Cell 16: 521-532.
33. Dumont AG, Yang Y, Reynoso D, Katz D, Trent JC, et al. (2012) Anti-tumor effects of the Notch pathway in gastrointestinal stromal tumors. Carcinogenesis 33: 1674-1683.
34. Albig AR, Becenti DJ, Roy TG, Schiemann WP, (2008) Microfibril-associate glycoprotein-2 (MAGP-2) promotes angiogenic cell sprouting by blocking notch signaling in endothelial cells. Microvasc Res 76: 7-14.
35. de Renzis S, Sönnichsen B, Zerial M, (2002) Divalent Rab effectors regulate the sub-compartmental organization and sorting of early endosomes. Nat Cell Biol 4: 124-133.
36. Yan GR, Xu SH, Tan ZL, Liu L, He QY, (2011) Global identification of miR-373-regulated genes in breast cancer by quantitative proteomics. Proteomics 11: 912-920.
37. Goebeler V, Poeter M, Zeuschner D, Gerke V, Rescher U, (2008) Annexin A8 regulates late endosome organization and function. Mol Biol Cell 19: 5267-5278.
38. Karanjawala ZE, Illei PB, Ashfaq R, Infante JR, Murphy K, et al. (2008) New markers of pancreatic cancer identified through differential gene expression analyses: claudin 18 and annexin A8. Am J Surg Pathol 32: 188-196.
39. Berthouze M, Venkataramanan V, Li Y, Shenoy SK, (2009) The deubiquitinases USP33 and USP20 coordinate beta2 adrenergic receptor recycling and resensitization. EMBO J 28: 1684-1696.
40. Buus R, Faronato M, Hammond DE, Urbé S, Claque MJ, (2009) Deubiquitinase activities required for hepatocyte growth factor-induced scattering of epithelial cells. Curr Biol 19: 1463-1466.
41. Lind GE, Danielsen SA, Ahlquist T, Merok MA, Andresen K, et al. (2011) Identification of an epigenetic biomarker with high sensitivity and specificity for colorectal cancer and adenomas. Mol Cancer 10: 85.
42. Wang Y, Yu Q, Cho AH, Rondeau G, Welsh J, et al. (2005) Survey of differentially methylated promoters in prostate cancer cell lines. Neoplasia 7: 748-760.
43. Davidson MR, Larsen JE, Yang IA, Hayward NK, Clarke BE, et al. (2010) MicroRNA-218 is deleted and downregulated in lung squamous cell carcinoma. PloS One 5: e12560.
44. Denk AE, Braig S, Schubert T, Bosserhoff AK, (2011) Slit3 inhibits activator protein 1-mediated migration of malignant melanoma cells. Int J Mol Med 28: 721-726.
45. Banerjee S, Dhar G, Haque I, Kambhampati S, Mehta S, et al. (2008) CCN5/WISP-2 expression in breast adenocarcinoma is associated with less frequent progression of the disease and suppresses the invasive phenotypes of tumor cells. Cancer Res 68: 7606-7612.
46. Davies SR, Davies ML, Sanders A, Parr C, Torkington J, et al. (2010) Differential expression of the CCN family member WISP-1, WISP-2 and WISP-3 in human colorectal cancer and the prognostic implications. Int J Oncol 36: 1129-1136.
47. Haydon RC, Deyrup A, Ishikawa A, Heck R, Jiang W, et al. (2002) Cytoplasmic and/or nuclear accumulation of the beta-catenin protein is a frequent event in human osteosarcoma. Int J Cancer 102: 338-342.
48. Hou CH, Chiang YC, Fong YC, Tang CH, (2011) Tang CH. WISP-1 increases MMP-2 expression and cell motility in human chondrosarcoma cells. Biochem Pharmacol 81: 1286-1295.
49. Nagai Y, Watanabe M, Ishikawa S, Karashima R, Kurashige J, et al. (2011) Clinical significance of Wnt-induced secreted protein-1 (WISP-1/CCN4) in esophageal squamous cell carcinoma. Anticancer Res 31: 991-997.
50. Clevers H, (2006) Wnt/beta-catenin signaling in development and disease. Cell 127: 469-480.
51. Vijayakumar S, Liu G, Rus IA, Yao S, Chen Y, et al. (2011) High frequency cano nical Wnt activation in multiple sarcoma subtypes drives proliferation through a TCF/β-catenin target gene, CDC25A. Cancer Cell 19: 601-612.
52. Bachet JB, Emile JF, (2010) Diagnostic criteria, specific mutations, and genetic predisposition in gastrointestinal stromal tumors. The Application Of Clinical Genetics 3: 85-101.
53. Jiang S, Li Y, Zhu YH, Wu XQ, Tanq J, et al. (2011) Intensive expression of UNC-51-like kinase 1 is a novel biomarker of poor prognosis in patients with esophageal squamous cell carcinoma. Cancer Sci 102: 1568-1575.
54. Haferlach C, Bacher U, Haferlach T, Dicker F, Alpermann T, et al. (2011) The inv(3)(q21q26)/t(3;3)(q21;q26) is frequently accompanied by alterations of the RUNX1, KRAS and NRAS and NF1 genes and mediates adverse prognosis both in MDS and in AML: a study in 39 cases of MDS or AML. Leukemia 25: 874-877.
55. Lennartsson J, Blume-Jensen P, Hermanson M, Pontén E, Carlberg M, et al. (1999) Phosphorylation of Shc by Src family kinases is necessary for stem cell factor receptor/c-kit mediated activation of the Ras/MAP kinase pathway and c-fos induction. Oncogene 18: 5546-5553.
56. Masson K, Heiss E, Band H, Rönnstrand L, (2006) Direct binding of Cbl to Tyr568 and Tyr936 of the stem cell factor receptor/c-KIT is required for ligand-induced ubiquination, internalization and degradation. Biochem J 399: 59-67.
57. Price DJ, Rivnay B, Fu Y, Jiang S, Avraham S, et al. (1997) Direct association of Csk homologous kinase (CHK) with the diphosphorylated site Tyr568/570 of the activated c-KIT in Megakaryocytes. J Biol Chem 272: 5915-5920.
58. Timokhina I, Kissel H, Stella G, Besmer P, (1998) Kit signaling through PI3-kinase and Src kinase pathways: an essential role for Rac1 and JNK activation in mast cell proliferation. EBMO J 17: 6250-6262.
59. Wollberg P, Lennartsson J, Gottfridsson E, Yoshimura A, Rönnstrand L, (2003) The adapter protein APS associates with the multifunctional docking sites Tyr-568 and Tyr-936 in c-Kit. Biochem J 370: 1033-1038.
60. Kozlowski M, Larose L, Lee F, Le DM, Rottapel R, et al. (1998) SHP-1 binds and negatively modulates the c-Kit receptor by interaction with Tyrosine 569 in the c-Kit juxtamembrane domain. Mol Cell Biol 18: 2089-2099.
61. Shivakrupa R, Linnekin D, (2005) Lyn contributes to regulation of multiple Kit-dependent signaling pathways in murine bone marrow mast cells. Cell Signal 17: 103-109.
62. Scholl S, Kirsch C, Böhmer FD, Klinger R, (2004) Signal transduction of c-Kit receptor tyrosine kinase in CHRF myeloid leukemia cells. J Cancer Res Clin Oncol 130: 711-718.
63. Emile JF, Stock N, Corless CL, Sciot R, Schildhaus HU, et al. (2009) Dotlike or Golgi-like KIT and PDGFRA Staining in GISTs. Am J Surg Pathol 33: 157-158.
64. Heinrich MC, Owzar K, Corless CL, Hollis D, Borden EC, et al. (2008) Correlation of kinase genotype and clinical outcome in the North American Intergroup Phase III trial of imatinib mesylate for treatment of advanced gastrointestinal stromal tumor: CALGB 150105 Study by Cancer and Leukemia Group B and Southwest Oncology Group. J Clin Oncol 26: 5360-5367.