Essential role of stat3 in pi3k-induced oncogenic transformation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 32, 2011, Pages 13247-13252

  Hart, Jonathan R ^a   Liao, Lujian ^a   Yates III, John R ^a   Vogt, Peter K ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Oncogenic signaling; Tumor stroma; Tyrosine kinase

Indexed keywords

2 (1H INDAZOL 4 YL) 6 (4 METHANESULFONYL 1 PIPERAZINYLMETHYL) 4 MORPHOLINOTHIENO[3,2 D]PYRIMIDINE; 2 CYANO N (2,5 DIBROMOPHENYL) 3 HYDROXYCROTONAMIDE; N BENZYL 2 CYANO 3 (3,4 DIHYDROXYPHENYL)ACRYLAMIDE; PHOSPHATIDYLINOSITOL 3 KINASE; RAPAMYCIN; STAT3 PROTEIN; STEROID RECEPTOR COACTIVATOR 1;

ANIMAL CELL; ARTICLE; CANCER CELL CULTURE; CARCINOGENESIS; CELL TRANSFORMATION; CONTROLLED STUDY; FIBROBLAST; HUMAN; HUMAN CELL; INHIBITION KINETICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

AMIDES; ANIMALS; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; CLASS IA PHOSPHATIDYLINOSITOL 3-KINASE; FIBROBLASTS; GENES, DOMINANT; HUMANS; MICE; MUTANT PROTEINS; NITRILES; PHOSPHORYLATION; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR;

EID: 80052009547     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1110486108     Document Type: Article

References (53)

1. Shuai K., Stark G.R., Kerr I.M., Darnell J.E., Jr. (1993) A single phosphotyrosine residue of Stat91 required for gene activation by interferon-gamma. Science 261:1744-1746. (Pubitemid 23332925)
2. Zhong Z., Wen Z., Darnell J.E., Jr. (1994) Stat3: A STAT family member activated by tyrosine phosphorylation in response to epidermal growth factor and interleukin-6. Science 264:95-98. (Pubitemid 24144493)
3. Khan K.D., et al. (1993) Induction of the Ly-6A/E gene by interferon alpha/beta and gamma requires a DNA element to which a tyrosine-phosphorylated 91-kDa protein binds. Proc Natl Acad Sci USA 90:6806-6810.
4. Schindler C., Shuai K., Prezioso V.R., Darnell J.E., Jr. (1992) Interferon-dependent tyrosine phosphorylation of a latent cytoplasmic transcription factor. Science 257:809-813.
5. Shuai K., Schindler C., Prezioso V.R., Darnell J.E., Jr. (1992) Activation of transcription by IFN-gamma: Tyrosine phosphorylation of a 91-kD DNA binding protein. Science 258:1808-1812. (Pubitemid 23087351)
6. Schindler C., Fu X.Y., Improta T., Aebersold R., Darnell J.E., Jr. (1992) Proteins of transcription factor ISGF-3: One gene encodes the 91-and 84-kDa ISGF-3 proteins that are activated by interferon alpha. Proc Natl Acad Sci USA 89:7836-7839.
7. Sadowski H.B., Shuai K., Darnell J.E., Jr. Gilman M.Z. (1993) A common nuclear signal transduction pathway activated by growth factor and cytokine receptors. Science 261:1739-1744. (Pubitemid 23332924)
8. Schindler C., Darnell J.E., Jr. (1995) Transcriptional responses to polypeptide ligands: The JAK-STAT pathway. Annu Rev Biochem 64:621-651.
9. Bromberg J.F., Horvath C.M., Besser D., Lathem W.W., Darnell J.E., Jr. (1998) Stat3 activation is required for cellular transformation by v-src. Mol Cell Biol 18:2553-2558. (Pubitemid 28183425)
10. Yu H., Jove R. (2004) The STATs of cancer - New molecular targets come of age. Nat Rev Cancer 4:97-105. (Pubitemid 38198738)
11. Chiarle R., et al. (2005) Stat3 is required for ALK-mediated lymphomagenesis and provides a possible therapeutic target. Nat Med 11:623-629. (Pubitemid 40868302)
12. Poget M., Meyer R. (1976) Modification of a technic of reconstruction after total or subtotal resection of the lower lip (Translated from French) ORL J Otorhinolaryngol Relat Spec, 38(Suppl 1):127-132 .
13. Bromberg J.F., et al. (1999) Stat3 as an oncogene. Cell 98:295-303. (Pubitemid 29380565)
14. David M., et al. (1996) STAT activation by epidermal growth factor (EGF) and amphiregulin. Requirement for the EGF receptor kinase but not for tyrosine phosphorylation sites or JAK1. J Biol Chem 271:9185-9188.
15. Dudka A.A., Sweet S.M., Heath J.K. (2010) Signal transducers and activators of transcription- 3 binding to the fibroblast growth factor receptor is activated by receptor amplification. Cancer Res 70:3391-3401.
16. Zhang Y.W., Wang L.M., Jove R., Vande Woude G.F. (2002) Requirement of Stat3 signaling for HGF/SF-Met mediated tumorigenesis. Oncogene 21:217-226. (Pubitemid 34102130)
17. Ren Z., Schaefer T.S. (2002) ErbB-2 activates Stat3 alpha in a Src- and JAK2-dependent manner. J Biol Chem 277:38486-38493. (Pubitemid 35154707)
18. Gao S.P., et al. (2007) Mutations in the EGFR kinase domain mediate STAT3 activation via IL-6 production in human lung adenocarcinomas. J Clin Invest 117:3846-3856. (Pubitemid 350224094)
19. Iliopoulos D., Hirsch H.A., Struhl K. (2009) An epigenetic switch involving NF-kappaB, Lin28, Let-7 MicroRNA, and IL6 links inflammation to cell transformation. Cell 139:693-706.
20. Iwamoto T., et al. (2000) The JAK-inhibitor, JAB/SOCS-1 selectively inhibits cytokineinduced, but not v-Src induced JAK-STAT activation. Oncogene 19:4795-4801.
21. Spiekermann K., et al. (2002) Constitutive activation of STAT3 and STAT5 is induced by leukemic fusion proteins with protein tyrosine kinase activity and is sufficient for transformation of hematopoietic precursor cells. Exp Hematol 30:262-271. (Pubitemid 34203733)
22. Yu H., Kortylewski M., Pardoll D. (2007) Crosstalk between cancer and immune cells: Role of STAT3 in the tumour microenvironment. Nat Rev Immunol 7:41-51. (Pubitemid 46020826)
23. Niu G., et al. (2005) Role of Stat3 in regulating p53 expression and function. Mol Cell Biol 25:7432-7440. (Pubitemid 41170107)
24. Niu G., et al. (2002) Constitutive Stat3 activity up-regulates VEGF expression and tumor angiogenesis. Oncogene 21:2000-2008. (Pubitemid 34270888)
25. Wojcik E.J., et al. (2006) A novel activating function of c-Src and Stat3 on HGF transcription in mammary carcinoma cells. Oncogene 25:2773-2784.
26. Hart J.R., Liao L., Ueno L., Yates, J.R., 3rd, Vogt P.K. (2011) Protein expression profiles of C3H 10T1/2 murine fibroblasts and of isogenic cells transformed by the H1047R mutant of phosphoinositide 3-kinase (PI3K). Cell Cycle 10:971-976.
27. Su Z.Z., Sarkar D., Emdad L., Barral P.M., Fisher P.B. (2007) Central role of interferon regulatory factor-1 (IRF-1) in controlling retinoic acid inducible gene-I (RIG-I) expression. J Cell Physiol 213:502-510. (Pubitemid 47509733)
28. Dupuis S., et al. (2003) Impaired response to interferon-alpha/beta and lethal viral disease in human STAT1 deficiency. Nat Genet 33:388-391. (Pubitemid 36278855)
29. Nakaya T., et al. (2001) Gene induction pathways mediated by distinct IRFs during viral infection. Biochem Biophys Res Commun 283:1150-1156. (Pubitemid 32912888)
30. Sinibaldi D., et al. (2000) Induction of p21WAF1/CIP1 and cyclin D1 expression by the Src oncoprotein in mouse fibroblasts: Role of activated STAT3 signaling. Oncogene 19:5419-5427. (Pubitemid 32000908)
31. Kuhen K.L., Samuel C.E. (1997) Isolation of the interferon-inducible RNA-dependent protein kinase Pkr promoter and identification of a novel DNA element within the 5′-flanking region of human and mouse Pkr genes. Virology 227:119-130. (Pubitemid 27241061)
32. Shenoy A.R., et al. (2007) Emerging themes in IFN-gamma-induced macrophage immunity by the p47 and p65 GTPase families. Immunobiology 212:771-784. (Pubitemid 350246255)
33. Zhou J., et al. (2007) Activation of the PTEN/mTOR/STAT3 pathway in breast cancer stem-like cells is required for viability and maintenance. Proc Natl Acad Sci USA 104:16158-16163. (Pubitemid 350099378)
34. Yokogami K., Wakisaka S., Avruch J., Reeves S.A. (2000) Serine phosphorylation and maximal activation of STAT3 during CNTF signaling is mediated by the rapamycin target mTOR. Curr Biol 10:47-50. (Pubitemid 30057415)
35. Oh J., Julias J.G., Ferris A.L., Hughes S.H. (2002) Construction and characterization of a replication-competent retroviral shuttle vector plasmid. J Virol 76:1762-1768. (Pubitemid 34094623)
36. Abujamra A.L., et al. (2006) Leukemia virus long terminal repeat activates NFkappaB pathway by a TLR3-dependent mechanism. Virology 345:390-403. (Pubitemid 43189898)
37. Raynaud F.I., et al. (2009) Biological properties of potent inhibitors of class I phosphatidylinositide 3-kinases: From PI-103 through PI-540, PI-620 to the oral agent GDC-0941. Mol Cancer Ther 8:1725-1738.
38. Qiu Y., Kung H.J. (2000) Signaling network of the Btk family kinases. Oncogene 19:5651-5661.
39. Qiu Y., Robinson D., Pretlow T.G., Kung H.J. (1998) Etk/Bmx, a tyrosine kinase with a pleckstrin-homology domain, is an effector of phosphatidylinositol 3′-kinase and is involved in interleukin 6-induced neuroendocrine differentiation of prostate cancer cells. Proc Natl Acad Sci USA 95:3644-3649.
40. Tsai Y.T., et al. (2000) Etk, a Btk family tyrosine kinase, mediates cellular transformation by linking Src to STAT3 activation. Mol Cell Biol 20:2043-2054.
41. Uckun F.M., et al. (2007) Anti-breast cancer activity of LFM-A13, a potent inhibitor of Polo-like kinase (PLK). Bioorg Med Chem 15:800-814. (Pubitemid 44895504)
42. Mahajan S., et al. (1999) Rational design and synthesis of a novel anti-leukemic agent targeting Bruton's tyrosine kinase (BTK), LFM-A13 [alpha-cyano-beta-hydroxy-beta-methyl-N-(2, 5-dibromophenyl)propenamide]. J Biol Chem 274:9587-9599.
43. Wehinger J., et al. (1996) IL-10 induces DNA binding activity of three STAT proteins (Stat1, Stat3, and Stat5) and their distinct combinatorial assembly in the promoters of selected genes. FEBS Lett 394:365-370. (Pubitemid 26341476)
44. Wang C.G., et al. (2010) EZH2 and STAT6 expression profiles are correlated with colorectal cancer stage and prognosis. World J Gastroenterol 16:2421-2427.
45. Zhang W.J., et al. (2008) IL-4-induced Stat6 activities affect apoptosis and gene expression in breast cancer cells. Cytokine 42:39-47.
46. Das S., Roth C.P., Wasson L.M., Vishwanatha J.K. (2007) Signal transducer and activator of transcription-6 (STAT6) is a constitutively expressed survival factor in human prostate cancer. Prostate 67:1550-1564. (Pubitemid 47536154)
47. Vasudevan K.M., et al. (2009) AKT-independent signaling downstream of oncogenic PIK3CA mutations in human cancer. Cancer Cell 16:21-32.
48. Kang S., Denley A., Vanhaesebroeck B., Vogt P.K. (2006) Oncogenic transformation induced by the p110beta, -gamma, and -delta isoforms of class I phosphoinositide 3-kinase. Proc Natl Acad Sci USA 103:1289-1294. (Pubitemid 43191158)
49. Guryanova O.A., et al. (2011) Nonreceptor tyrosine kinase BMX maintains self-renewal and tumorigenic potential of glioblastoma stem cells by activating STAT3. Cancer Cell 19:498-511.
50. Thornberry N.A., et al. (1992) A novel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes. Nature 356:768-774.
51. Kang S., Bader A.G., Vogt P.K. (2005) Phosphatidylinositol 3-kinase mutations identified in human cancer are oncogenic. Proc Natl Acad Sci USA 102:802-807. (Pubitemid 40282746)
52. Bos T.J., et al. (1990) Efficient transformation of chicken embryo fibroblasts by c-Jun requires structural modification in coding and noncoding sequences. Genes Dev 4:1677-1687.
53. Duff R.G., Vogt P.K. (1969) Characteristics of two new avian tumor virus subgroups. Virology 39:18-30.