Long-term exposure of gastrointestinal stromal tumor cells to sunitinib induces epigenetic silencing of the PTEN gene

International Journal of Cancer

Volumn 130, Issue 4, 2012, Pages 959-966

  Yang, Jing ^a   Ikezoe, Takayuki ^a   Nishioka, Chie ^a   Takezaki, Yuka ^a   Hanazaki, Kazuhiro ^a   Taguchi, Takahiro ^a   Yokoyama, Akihito ^a  

^a KOCHI UNIVERSITY   (Japan)

Author keywords

Akt; GIST; PTEN; sunitinib resistant

Indexed keywords

IMATINIB; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN KINASE B; SUNITINIB;

APOPTOSIS; ARTICLE; CANCER RESISTANCE; CONTROLLED STUDY; DNA METHYLATION; DOWN REGULATION; EPIGENETICS; GASTROINTESTINAL STROMAL TUMOR CELL; GENE; GENE SILENCING; GROWTH INHIBITION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; LONG TERM EXPOSURE; PHOSPHATASE AND TENSIN HOMOLOG DELETED ON CHROMOSOME TEN GENE; PRIORITY JOURNAL; PROMOTER REGION; TUMOR CELL;

ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; EPIGENESIS, GENETIC; GASTROINTESTINAL NEOPLASMS; GASTROINTESTINAL STROMAL TUMORS; HUMANS; INDOLES; PIPERAZINES; PTEN PHOSPHOHYDROLASE; PYRIMIDINES; PYRROLES;

EID: 83955161764     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.26095     Document Type: Article

References (39)

1. Fletcher CD, Berman JJ, Corless C, Gorstein F, Lasota J, Longley BJ, Miettinen M, O'Leary TJ, Remotti H, Rubin BP, Shmookler B, Sobin LH, et al,. Diagnosis of gastrointestinal stromal tumors: A consensus approach. Hum Pathol 2002; 33: 459-65. (Pubitemid 34747864)
2. Nilsson B, Bümming P, Meis-Kindblom JM, Odén A, Dortok A, Gustavsson B, Sablinska K, Kindblom LG,. Gastrointestinal stromal tumors: The incidence, prevalence, clinical course, and prognostication in the preimatinib mesylate eraâA population-based study in Western Sweden. Cancer 2005; 103: 821-9. (Pubitemid 40216412)
3. Tryggvason G, Gislason HG, Magnusson MK, Jonasson JG,. Gastrointestinal stromal tumors in Iceland, 1990-2003: The Icelandic GIST study, a population-based incidence and pathologic risk stratification study. Int J Cancer 2005; 117: 289-93. (Pubitemid 41377450)
4. DeMatteo RP, Lewis JJ, Leung D, Mudan SS, Woodruff JM, Brennan MF,. Two hundred gastrointestinal stromal tumors: Recurrence patterns and prognostic factors for survival. Ann Surg 2000; 231: 51-8. (Pubitemid 30043939)
5. Joensuu H, Roberts PJ, Sarlomo-Rikala M, Andersson LC, Tervahartiala P, Tuveson D, Silberman S, Capdeville R, Dimitrijevic S, Druker B, Demetri GD,. Effect of the tyrosine kinase inhibitor STI571 in a patient with a metastatic gastrointestinal stromal tumor. N Engl J Med 2001; 344: 1052-6. (Pubitemid 32267975)
6. Hirota S, Isozaki K, Moriyama Y, Hashimoto K, Nishida T, Ishiguro S, Kawano K, Hanada M, Kurata A, Takeda M, Muhammad Tunio G, Matsuzawa Y, et al,. Gain-of-function mutations of c-kit in human gastrointestinal stromal tumors. Science 1998; 279: 577-80. (Pubitemid 28067289)
7. Kindblom LG, Remotti HE, Aldenborg F, Meis-Kindblom JM,. Gastrointestinal pacemaker cell tumor (GIPACT): Gastrointestinal stromal tumors show phenotypic characteristics of the interstitial cells of Cajal. Am J Pathol 1998; 152: 1259-69. (Pubitemid 28221878)
8. Corless CL, McGreevey L, Haley A, Town A, Heinrich MC,. KIT mutations are common in incidental gastrointestinal stromal tumors one centimeter or less in size. Am J Pathol 2002; 160: 1567-72. (Pubitemid 34525636)
9. Galli SJ, Zsebo KM, Geissler EN,. The kit ligand, stem cell factor. Adv Immunol 1994; 55: 1-96.
10. Druker BJ, Tamura S, Buchdunger E, Ohno S, Segal GM, Fanning S, Zimmermann J, Lydon NB,. Effects of a selective inhibitor of the Abl tyrosine kinase on the growth of Bcr-Abl positive cells. Nat Med 1996; 2: 561-6.
11. Corless CL, Heinrich MC,. Molecular pathobiology of gastrointestinal stromal sarcomas. Annu Rev Pathol 2008; 3: 557-86. (Pubitemid 351488293)
12. Blanke CD, Demetri GD, von Mehren M, Heinrich MC, Eisenberg B, Fletcher JA, Corless CL, Fletcher CD, Roberts PJ, Heinz D, Wehre E, Nikolova Z, et al,. Long-term results from a randomised phase II trial of standard versus higher-dose imatinib mesylate for patients with unresectable or metastatic gastrointestinal stromal tumors expressing KIT. J Clin Oncol 2008; 26: 620-25. (Pubitemid 351264357)
13. Blanke CD, Rankin C, Demetri GD, Ryan CW, von Mehren M, Benjamin RS, Raymond AK, Bramwell VH, Baker LH, Maki RG, Tanaka M, Hecht JR, et al,. 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 2008; 26: 626-32. (Pubitemid 351264358)
14. Antonescu CR, Besmer P, Guo T, Arkun K, Hom G, Koryotowski B, Leversha MA, Jeffrey PD, Desantis D, Singer S, Brennan MF, Maki RG, et al,. Acquired resistance to imatinib in gastrointestinal stromal tumor occurs through secondary gene mutation. Clin Cancer Res 2005; 11: 4182-90. (Pubitemid 40791584)
15. Nishida T, Takahashi T, Nishitani A, Doi T, Shirao K, Komatsu Y, Nakajima K, Hirota S,. Japanese Study Group on GIST Sunitinib-resistant gastrointestinal stromal tumors harbor cis-mutations in the activation loop of the KIT gene. Int J Clin Oncol 2009; 14: 143-9.
16. Prenen H, Cools J, Mentens N, Folens C, Sciot R, Schöffski P, Van Oosterom A, Marynen P, Debiec-Rychter M,. Efficacy of the kinase inhibitor SU11248 against gastrointestinal stromal tumor mutants refractory to imatinib mesylate. Clin Cancer Res 2006; 12: 2622-7.
17. Carter TA, Wodicka LM, Shah NP, Velasco AM, Fabian MA, Treiber DK, Milanov ZV, Atteridge CE, Biggs WH, III, Edeen PT, Floyd M, Ford JM, et al,. Inhibition of drug-resistant mutants of ABL, KIT, and EGF receptor kinases. Proc Natl Acad Sci USA 2005; 102: 11011-16. (Pubitemid 41105984)
18. Demetri GD, van Oosterom AT, Garrett CR, Blackstein ME, Shah MH, Verweij J, McArthur G, Judson IR, Heinrich MC, Morgan JA, Desai J, Fletcher CD, et al,. Efficacy and safety of sunitinib in patients with advanced gastrointestinal stromal tumour after failure of imatinib: A randomized controlled trial. Lancet 2006; 368: 1329-38. (Pubitemid 44528723)
19. Skorski T, Kanakaraj P, Nieborowska-Skorska M, Ratajczak MZ, Wen SC, Zon G, Gewirtz AM, Perussia B, Calabretta B,. Phosphatidylinositol-3 kinase activity is regulated by BCR/ABL and is required for the growth of Philadelphia chromosome-positive cells. Blood 1995; 86: 726-36.
20. Bjornsti MA, Houghton PJ,. Lost in translation: Dysregulation of capdependent translation and cancer. Cancer Cell 2004; 5: 519-23. (Pubitemid 38748913)
21. Hay N, Sonenberg N,. Upsteam and downsteam of mTOR. Genes Dev 2004; 18: 1926-45.
22. Alvarez-Nuñez F, Bussaglia E, Mauricio D, Ybarra J, Vilar M, Lerma E, de Leiva A, Matias-Guiu X,. Thyroid Neoplasia Study Group. PTEN promoter methylation in sporadic thyroid carcinomas. Thyroid 2006; 16: 17-23. (Pubitemid 43346499)
23. Whang YE, Wu X, Suzuki H, Reiter RE, Tran C, Vessella RL, Said JW, Isaacs WB, Sawyers CL,. Inactivation of the tumor suppressor PTEN/MMAC1 in advanced human prostate cancer through loss of expression. Proc Natl Acad Sci USA 1998; 95: 5246-50. (Pubitemid 28208583)
24. Dahia PL, Aguiar RC, Alberta J, Kum JB, Caron S, Sill H, Marsh DJ, Ritz J, Freedman A, Stiles C, Eng C,. PTEN is inversely correlated with the cell survival factor Akt/PKB and is inactivated via multiple mechanismsin haematological malignancies. Hum Mol Genet 1999; 8: 185-93. (Pubitemid 29054260)
25. Salvesen HB, MacDonald N, Ryan A, Jacobs IJ, Lynch ED, Akslen LA, Das S,. PTEN methylation is associated with advanced stage and microsatellite instability in endometrial carcinoma. Int J Cancer 2001; 91: 22-6.
26. Taguchi T, Sonobe H, Toyonaga S, Yamasaki I, Shuin T, Takano A, Araki K, Akimaru K, Yuri K,. Conventional and molecular cytogenetic characterization of a new human cell line. GIST-T1, established from gastrointestinal stromal tumor. Lab Invest 2002; 82: 663-5. (Pubitemid 34522379)
27. Nishioka C, Ikezoe T, Yang J, Koeffler HP, Taguchi H,. Fludarabine induces apoptosis of human T-cell leukemia virus type 1-infected T cells via inhibition of the nuclear factor-kappaB signal pathway. Leukemia 2007; 21: 1044-9. (Pubitemid 46679439)
28. Ikezoe T, Yang Y, Nishioka C, Bandobashi K, Nakatani H, Taguchi T, Koeffler HP, Taguchi H,. Effect of SU11248 on gastrointestinal stromal tumor-T1 cells: Enhancement of growth inhibition via inhibition of 3-kinase/Akt/mammalian target of rapamycin signaling. Cancer Sci 2006; 97: 945-51. (Pubitemid 44151278)
29. Yang Y, Ikezoe T, Takeuchi T, Adachi Y, Ohtsuki Y, Takeuchi S, Koeffler HP, Taguchi H,. HIV-1 protease inhibitor induces growth arrest and apoptosis of human prostate cancer LNCaP cells in vitro and in vivo in conjunction with blockade of androgen receptor STAT3 and AKT signaling. Cancer Sci 2005; 96: 425-33. (Pubitemid 41179744)
30. Ikezoe T, Bandobashi K, Yang Y, Takeuchi S, Sekiguchi N, Sakai S, Koeffler HP, Taguchi H,. HIV-1 protease inhibitor ritonavir potentiates the effect of 1,25-dihydroxyvitamin D3 to induce growth arrest and differentiation of human myeloid leukemia cells via downregulation of CYP24. Leuk Res 2006; 30: 1005-11. (Pubitemid 43831188)
31. Bauer S, Duensing A, Demetri GD, Fletcher JA,. KIT oncogenic signaling mechanisms in imatinib-resistant gastrointestinal stromal tumor: PI3-kinase/Akt is a crucial survival pathway. Oncogene 2007; 26: 7560-68. (Pubitemid 350207707)
32. Abouantoun TJ, Castellino RC, MacDonald TJ,. Sunitinib induces. PTEN expression and inhibits. PDGFR signaling and migration of medulloblastoma cells. J Neurooncol 2011; 101: 215-26.
33. Noro R, Gemma A, Miyanaga A, Kosaihira S, Minegishi Y, Nara M, Kokubo Y, Seike M, Kataoka K, Matsuda K, Okano T, Yoshimura A, et al,. PTEN inactivation in lung cancer cells and the effect of its recovery on treatment with epidermal growth factor receptor tyrosine kinase inhibitors. Int J Oncol 2007; 31: 1157-63.
34. Kokubo Y, Gemma A, Noro R, Seike M, Kataoka K, Matsuda K, Okano T, Minegishi Y, Yoshimura A, Shibuya M, Kudoh S,. Reduction of PTEN protein and loss of epidermal growth factor receptor gene mutation in lung cancer with natural resistance to gefitinib (IRESSA). Br J Cancer 2005; 92: 1711-19. (Pubitemid 40756483)
35. Zhuang HQ, Wang J, Yuan ZY, Zhao LJ, Wang P, Wang CL,. The drug-resistance to gefitinib in PTEN low expression cancer cells is reversed by irradiation in vitro. J Exp Clin Cancer Res 2009; 28: 123.
36. Wu Z, Gioeli D, Conaway M, Weber MJ, Theodorescu D,. Restoration of PTEN expression alters the sensitivity of prostate cancer cells to EGFR inhibitors. Prostate 2008; 68: 935-44. (Pubitemid 351794158)
37. Ricci R, Maggiano N, Castri F, Rinelli A, Murazio M, Pacelli F, Potenza AE, Vecchio FM, Larocca LM,. Role of PTEN in gastrointestinal stromal tumor progression. Arch Pathol Lab Med 2004; 128: 421-5. (Pubitemid 38451129)
38. Nishioka C, Ikezoe T, Yang J, Yokoyama A,. Multitargeted tyrosine kinase inhibitor stimulates expression of IL-6 and activates JAK2/STAT5 signaling in acute myelogenous leukemia cells. Leukemia 2009; 23: 2304-8.
39. Nishioka C, Ikezoe T, Yang J, Yokoyama A,. Long-term exposure of leukemia cells to multi-targeted tyrosine kinase inhibitor induces activations of AKT. ERK and. STAT5 signaling via epigenetic silencing of the. PTEN gene. Leukemia 2010; 24: 1631-40.