PIM kinase isoform specific regulation of MIG6 expression and EGFR signaling in prostate cancer cells

Oncotarget

Volumn 2, Issue 12, 2011, Pages 1134-1144

  Siu, Allan ^a,b   Virtanen, Carl ^c   Jongstra, Jan ^a,b  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

EGFR; Gefitinib; M 110; MIG6; PIM 1; Prostate cancer

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; GEFITINIB; IMIDAZOLE DERIVATIVE; MIG 6 PROTEIN, HUMAN; MIG-6 PROTEIN, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE; ONCOPROTEIN; PIM2 PROTEIN, HUMAN; PIM3 PROTEIN, HUMAN; PROTEIN KINASE PIM 1; PROTEIN SERINE THREONINE KINASE; PYRIDAZINE DERIVATIVE; QUINAZOLINE DERIVATIVE; SGI 1776; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SMALL INTERFERING RNA; TUMOR SUPPRESSOR PROTEIN;

ARTICLE; CELL PROLIFERATION; DRUG ANTAGONISM; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MALE; METABOLISM; PROSTATE TUMOR; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL LINE, TUMOR; CELL PROLIFERATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMIDAZOLES; MALE; MAP KINASE SIGNALING SYSTEM; PROSTATIC NEOPLASMS; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-PIM-1; PYRIDAZINES; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; RNA INTERFERENCE; RNA, SMALL INTERFERING; TUMOR SUPPRESSOR PROTEINS;

EID: 84862986683     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.386     Document Type: Article

References (55)

1. Nawijn MC, Alendar A, Berns A. For better or for worse: the role of Pim oncogenes in tumorigenesis. Nat Rev Cancer. 2011; 11:23-34.
2. Cibull TL, Jones TD, Li L, Eble JN, Ann Baldridge L, Malott SR, Luo Y, Cheng L. Overexpression of Pim-1 during progression of prostatic adenocarcinoma. J Clin Pathol. 2006; 59:285-288.
3. Dai H, Li R, Wheeler T, Diaz de Vivar A, Frolov A, Tahir S, Agoulnik I, Thompson T, Rowley D, Ayala G. Pim- 2 upregulation: biological implications associated with disease progression and perinueral invasion in prostate cancer. Prostate. 2005; 65:276-286.
4. Beier UH, Weise JB, Laudien M, Sauerwein H, Gorogh T. Overexpression of Pim-1 in head and neck squamous cell carcinomas. International journal of oncology. 2007; 30:1381-1387.
5. Guo S, Mao X, Chen J, Huang B, Jin C, Xu Z, Qiu S. Overexpression of Pim-1 in bladder cancer. J Exp Clin Cancer Res. 2010; 29:161.
6. Li YY, Popivanova BK, Nagai Y, Ishikura H, Fujii C, Mukaida N. Pim-3, a proto-oncogene with serine/threonine kinase activity, is aberrantly expressed in human pancreatic cancer and phosphorylates bad to block bad-mediated apoptosis in human pancreatic cancer cell lines. Cancer Res. 2006; 66:6741-6747.
7. Popivanova BK, Li YY, Zheng H, Omura K, Fujii C, Tsuneyama K, Mukaida N. Proto-oncogene, Pim-3 with serine/threonine kinase activity, is aberrantly expressed in human colon cancer cells and can prevent Bad-mediated apoptosis. Cancer Sci. 2007; 98:321-328.
8. Wu Y, Wang YY, Nakamoto Y, Li YY, Baba T, Kaneko S, Fujii C, Mukaida N. Accelerated hepatocellular carcinoma development in mice expressing the Pim-3 transgene selectively in the liver. Oncogene. 2010; 29:2228-2237.
9. Chen WW, Chan DC, Donald C, Lilly MB, Kraft AS. Pim family kinases enhance tumor growth of prostate cancer cells. Mol Cancer Res. 2005; 3:443-451.
10. Morishita D, Katayama R, Sekimizu K, Tsuruo T, Fujita N. Pim kinases promote cell cycle progression by phosphorylating and down-regulating p27Kip1 at the transcriptional and posttranscriptional levels. Cancer Res. 2008; 68:5076-5085.
11. Wang Z, Bhattacharya N, Mixter PF, Wei W, Sedivy J, Magnuson NS. Phosphorylation of the cell cycle inhibitor p21Cip1/WAF1 by Pim-1 kinase. Biochim Biophys Acta. 2002; 1593:45-55.
12. Bachmann M, Moroy T. The serine/threonine kinase Pim- 1. Int J Biochem Cell Biol. 2005; 37:726-730.
13. Aho TL, Sandholm J, Peltola KJ, Mankonen HP, Lilly M, Koskinen PJ. Pim-1 kinase promotes inactivation of the pro-apoptotic Bad protein by phosphorylating it on the Ser112 gatekeeper site. FEBS Lett. 2004; 571:43-49.
14. Gu JJ, Wang Z, Reeves R, Magnuson NS. PIM1 phosphorylates and negatively regulates ASK1-mediated apoptosis. Oncogene. 2009.
15. Isaac M, Siu A, Jongstra J. The oncogenic PIM kinase family regulates drug resistance through multiple mechanisms. Drug Resist Updat. 2011; 14:203-211.
16. Chang M, Kanwar N, Feng E, Siu A, Liu X, Ma D, Jongstra J. PIM kinase inhibitors downregulate STAT3(Tyr705) phosphorylation. Mol Cancer Ther. 2010; 9:2478-2487.
17. Haura EB, Turkson J, Jove R. Mechanisms of disease: Insights into the emerging role of signal transducers and activators of transcription in cancer. Nat Clin Pract Oncol. 2005; 2:315-324.
18. Horinaga M, Okita H, Nakashima J, Kanao K, Sakamoto M, Murai M. Clinical and pathologic significance of activation of signal transducer and activator of transcription 3 in prostate cancer. Urology. 2005; 66:671-675.
19. Clark J, Edwards S, Feber A, Flohr P, John M, Giddings I, Crossland S, Stratton MR, Wooster R, Campbell C, Cooper CS. Genome-wide screening for complete genetic loss in prostate cancer by comparative hybridization onto cDNA microarrays. Oncogene. 2003; 22:1247-1252.
20. Hynes NE, Lane HA. ERBB receptors and cancer: the complexity of targeted inhibitors. Nat Rev Cancer. 2005; 5:341-354.
21. Peraldo-Neia C, Migliardi G, Mello-Grand M, Montemurro F, Segir R, Pignochino Y, Cavalloni G, Torchio B, Mosso L, Chiorino G, Aglietta M. Epidermal Growth Factor Receptor (EGFR) mutation analysis, gene expression profiling and EGFR protein expression in primary prostate cancer. BMC Cancer. 2011; 11:31.
22. Shah RB, Ghosh D, Elder JT. Epidermal growth factor receptor (ErbB1) expression in prostate cancer progression: correlation with androgen independence. Prostate. 2006; 66:1437-1444.
23. Di Lorenzo G, Tortora G, D'Armiento FP, De Rosa G, Staibano S, Autorino R, D'Armiento M, De Laurentiis M, De Placido S, Catalano G, Bianco AR, Ciardiello F. Expression of epidermal growth factor receptor correlates with disease relapse and progression to androgen-independence in human prostate cancer. Clin Cancer Res. 2002; 8:3438-3444.
24. Segatto O, Anastasi S, Alema S. Regulation of epidermal growth factor receptor signalling by inducible feedback inhibitors. J Cell Sci. 2011; 124:1785-1793.
25. Anastasi S, Baietti MF, Frosi Y, Alema S, Segatto O. The evolutionarily conserved EBR module of RALT/MIG6 mediates suppression of the EGFR catalytic activity. Oncogene. 2007; 26:7833-7846.
26. Zhang X, Pickin KA, Bose R, Jura N, Cole PA, Kuriyan J. Inhibition of the EGF receptor by binding of MIG6 to an activating kinase domain interface. Nature. 2007; 450:741- 744.
27. Frosi Y, Anastasi S, Ballaro C, Varsano G, Castellani L, Maspero E, Polo S, Alema S, Segatto O. A two-tiered mechanism of EGFR inhibition by RALT/MIG6 via kinase suppression and receptor degradation. J Cell Biol. 2010; 189:557-571.
28. Ying H, Zheng H, Scott K, Wiedemeyer R, Yan H, Lim C, Huang J, Dhakal S, Ivanova E, Xiao Y, Zhang H, Hu J, Stommel JM, Lee MA, Chen AJ, Paik JH et al. Mig-6 controls EGFR trafficking and suppresses gliomagenesis. Proc Natl Acad Sci U S A. 2010; 107:6912-6917.
29. Dang CV, O'Donnell KA, Zeller KI, Nguyen T, Osthus RC, Li F. The c-Myc target gene network. Semin Cancer Biol. 2006; 16:253-264.
30. Zeller KI, Zhao X, Lee CW, Chiu KP, Yao F, Yustein JT, Ooi HS, Orlov YL, Shahab A, Yong HC, Fu Y, Weng Z, Kuznetsov VA, Sung WK, Ruan Y, Dang CV et al. Global mapping of c-Myc binding sites and target gene networks in human B cells. Proc Natl Acad Sci U S A. 2006; 103:17834-17839.
31. Zippo A, De Robertis A, Serafini R, Oliviero S. PIM1- dependent phosphorylation of histone H3 at serine 10 is required for MYC-dependent transcriptional activation and oncogenic transformation. Nat Cell Biol. 2007; 9:932-944.
32. Delpuech O, Griffiths B, East P, Essafi A, Lam EW, Burgering B, Downward J, Schulze A. Induction of Mxi1- SR alpha by FOXO3a contributes to repression of Myc-dependent gene expression. Mol Cell Biol. 2007; 27:4917- 4930.
33. Brandt TL, Fraser DJ, Leal S, Halandras PM, Kroll AR, Kroll DJ. c-Myb trans-activates the human DNA topoisomerase IIalpha gene promoter. J Biol Chem. 1997; 272:6278-6284.
34. Quintana AM, Liu F, O'Rourke JP, Ness SA. Identification and Regulation of c-Myb Target Genes in MCF-7 Cells. BMC Cancer. 2011; 11:30.
35. Baniwal SK, Khalid O, Gabet Y, Shah RR, Purcell DJ, Mav D, Kohn-Gabet AE, Shi Y, Coetzee GA, Frenkel B. Runx2 transcriptome of prostate cancer cells: insights into invasiveness and bone metastasis. Mol Cancer. 2010; 9:258.
36. Wotton S, Terry A, Kilbey A, Jenkins A, Herzyk P, Cameron E, Neil JC. Gene array analysis reveals a common Runx transcriptional programme controlling cell adhesion and survival. Oncogene. 2008; 27:5856-5866.
37. Anastasi S, Fiorentino L, Fiorini M, Fraioli R, Sala G, Castellani L, Alema S, Alimandi M, Segatto O. Feedback inhibition by RALT controls signal output by the ErbB network. Oncogene. 2003; 22:4221-4234.
38. Hackel PO, Gishizky M, Ullrich A. Mig-6 is a negative regulator of the epidermal growth factor receptor signal. Biol Chem. 2001; 382:1649-1662.
39. Mumenthaler SM, Ng PY, Hodge A, Bearss D, Berk G, Kanekal S, Redkar S, Taverna P, Agus DB, Jain A. Pharmacologic inhibition of Pim kinases alters prostate cancer cell growth and resensitizes chemoresistant cells to taxanes. Mol Cancer Ther. 2009; 8:2882-2893.
40. Rojas M, Yao S, Lin YZ. Controlling epidermal growth factor (EGF)-stimulated Ras activation in intact cells by a cell-permeable peptide mimicking phosphorylated EGF receptor. J Biol Chem. 1996; 271:27456-27461.
41. Chou TC, Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Advances in enzyme regulation. 1984; 22:27-55.
42. Grundler R, Brault L, Gasser C, Bullock AN, Dechow T, Woetzel S, Pogacic V, Villa A, Ehret S, Berridge G, Spoo A, Dierks C, Biondi A, Knapp S, Duyster J, Schwaller J. Dissection of PIM serine/threonine kinases in FLT3-ITD-induced leukemogenesis reveals PIM1 as regulator of CXCL12-CXCR4-mediated homing and migration. J Exp Med. 2009; 206:1957-1970.
43. Hammerman PS, Fox CJ, Birnbaum MJ, Thompson CB. Pim and Akt oncogenes are independent regulators of hematopoietic cell growth and survival. Blood. 2005; 105:4477-4483.
44. Aho TL, Sandholm J, Peltola KJ, Ito Y, Koskinen PJ. Pim-1 kinase phosphorylates RUNX family transcription factors and enhances their activity. BMC Cell Biol. 2006; 7:21.
45. Kim HR, Oh BC, Choi JK, Bae SC. Pim-1 kinase phosphorylates and stabilizes RUNX3 and alters its subcellular localization. J Cell Biochem. 2008; 105:1048- 1058.
46. Macdonald A, Campbell DG, Toth R, McLauchlan H, Hastie CJ, Arthur JS. Pim kinases phosphorylate multiple sites on Bad and promote 14-3-3 binding and dissociation from Bcl-XL. BMC Cell Biol. 2006; 7:1.
47. Fiorini M, Ballaro C, Sala G, Falcone G, Alema S, Segatto O. Expression of RALT, a feedback inhibitor of ErbB receptors, is subjected to an integrated transcriptional and post-translational control. Oncogene. 2002; 21:6530-6539.
48. Normanno N, De Luca A, Bianco C, Strizzi L, Mancino M, Maiello MR, Carotenuto A, De Feo G, Caponigro F, Salomon DS. Epidermal growth factor receptor (EGFR) signaling in cancer. Gene. 2006; 366:2-16.
49. Canil CM, Moore MJ, Winquist E, Baetz T, Pollak M, Chi KN, Berry S, Ernst DS, Douglas L, Brundage M, Fisher B, McKenna A, Seymour L. Randomized phase II study of two doses of gefitinib in hormone-refractory prostate cancer: a trial of the National Cancer Institute of Canada- Clinical Trials Group. J Clin Oncol. 2005; 23:455-460.
50. Pezaro C, Rosenthal MA, Gurney H, Davis ID, Underhill C, Boyer MJ, Kotasek D, Solomon B, Toner GC. An open-label, single-arm phase two trial of gefitinib in patients with advanced or metastatic castration-resistant prostate cancer. Am J Clin Oncol. 2009; 32:338-341.
51. Lorusso PM. Phase I studies of ZD1839 in patients with common solid tumors. Semin Oncol. 2003; 30:21-29.
52. Fiorentino L, Pertica C, Fiorini M, Talora C, Crescenzi M, Castellani L, Alema S, Benedetti P, Segatto O. Inhibition of ErbB-2 mitogenic and transforming activity by RALT, a mitogen-induced signal transducer which binds to the ErbB-2 kinase domain. Mol Cell Biol. 2000; 20:7735-7750.
53. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 2004; 5:R80.
54. Benjamini Y, Hochberg Y.J R Statistical Soc. 1995; 8:289- 300.
55. Skehan P, Storeng R, Scudiero D, Monks A, McMahon J, Vistica D, Warren JT, Bokesch H, Kenney S, Boyd MR. New colorimetric cytotoxicity assay for anticancer-drug screening. J Natl Cancer Inst. 1990; 82:1107-1112.