KLF5 promotes hypoxia-induced survival and inhibits apoptosis in non-small cell lung cancer cells via HIF-1α

International Journal of Oncology

Volumn 45, Issue 4, 2014, Pages 1507-1514

  Li, Xiaochen ^a   Liu, Xiansheng ^a   Xu, Yongjian ^a   Liu, Jin ^a   Xie, Min ^a   Ni, Wang ^a   Chen, Shixin ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Cell survival; HIF 1 ; Hypoxia; KLF5; Lung cancer

Indexed keywords

CASPASE 3; CYCLIN B1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; KRUPPEL LIKE FACTOR 5; SMALL INTERFERING RNA; SURVIVIN; HIF1A PROTEIN, HUMAN; KLF5 PROTEIN, HUMAN; KRUPPEL LIKE FACTOR;

A549 CELL LINE; APOPTOSIS; ARTICLE; CELL CLONING; CELL HYPOXIA; CELL PROLIFERATION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; GENE SILENCING; HUMAN; HUMAN CELL; HYPOXIC CELL; IMMUNOPRECIPITATION; LUNG NON SMALL CELL CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; TUMOR PROMOTION; UPREGULATION; GENE EXPRESSION REGULATION; GENETICS; LUNG TUMOR; METABOLISM; NON SMALL CELL LUNG CANCER; PATHOLOGY; TUMOR CELL LINE;

APOPTOSIS; CARCINOMA, NON-SMALL-CELL LUNG; CELL HYPOXIA; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; KRUPPEL-LIKE TRANSCRIPTION FACTORS; LUNG NEOPLASMS;

EID: 84907463121     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2014.2544     Document Type: Article

References (54)

1. Estimated Incidence, Mortality and Prevalence Worldwide in 2012. http://globocan.iarc.fr/Pages/fact-sheets-cancer.aspx Accessed Mar 27, 2014.
2. Evan GI and Vousden KH: Proliferation, cell cycle and apoptosis in cancer. Nature 411: 342-348, 2001. (Pubitemid 32467043)
3. Wilson WR and Hay MP: Targeting hypoxia in cancer therapy. Nature reviews. Cancer 11: 393-410, 2011.
4. Brahimi-Horn MC, Chiche J and Pouyssegur J: Hypoxia and cancer. J Mol Med 85: 1301-1307, 2007. (Pubitemid 50004093)
5. Zhang H, Okamoto M, Panzhinskiy E, Zawada WM and Das M: PKC delta/midkine pathway drives hypoxia-induced proliferation and differentiation of human lung epithelial cells. Am J Physiol Cell Physiol 306: C648-C658, 2014.
6. Vaporidi K, Tsatsanis C, Georgopoulos D and Tsichlis PN: Effects of hypoxia and hypercapnia on surfactant protein expression proliferation and apoptosis in A549 alveolar epithelial cells. Life Sci 78: 284-293, 2005. (Pubitemid 41570199)
7. Zagzag D, Zhong H, Scalzitti JM, Laughner E, Simons JW and Semenza GL: Expression of hypoxia-inducible factor 1alpha in brain tumors: association with angiogenesis, invasion, and progression. Cancer 88: 2606-2618, 2000. (Pubitemid 30331970)
8. Volm M and Koomagi R: Hypoxia-inducible factor (HIF-1) and its relationship to apoptosis and proliferation in lung cancer. Anticancer Res 20: 1527-1533, 2000. (Pubitemid 30628160)
9. Wang Q, Li LH, Gao GD, et al: HIF-1alpha up-regulates NDRG1 expression through binding to NDRG1 promoter, leading to proliferation of lung cancer A549 cells. Mol Biol Rep 40: 3723-3729, 2013.
10. Luo F, Liu X, Yan N, et al: Hypoxia-inducible transcription factor-1alpha promotes hypoxia-induced A549 apoptosis via a mechanism that involves the glycolysis pathway. BMC Cancer 6: 26, 2006.
11. Chi JT, Wang Z, Nuyten DS, et al: Gene expression programs in response to hypoxia: cell type specificity and prognostic significance in human cancers. PLoS Med 3: e47, 2006.
12. Kim WY and Kaelin WG: Role of VHL gene mutation in human cancer. J Clin Oncol 22: 4991-5004, 2004. (Pubitemid 46646218)
13. Sermeus A and Michiels C: Reciprocal influence of the p53 and the hypoxic pathways. Cell Death Dis 2: e164, 2011.
14. Lee SJ, No YR, Dang DT, et al: Regulation of hypoxia-inducible factor 1alpha (HIF-1alpha) by lysophosphatidic acid is dependent on interplay between p53 and Kruppel-like factor 5. J Biol Chem 288: 25244-25253, 2013.
15. Park SY, Jeong KJ, Lee J, et al: Hypoxia enhances LPA-induced HIF-1alpha and VEGF expression: their inhibition by resveratrol. Cancer Lett 258: 63-69, 2007. (Pubitemid 47600493)
16. Schumpelick VH-PB and Schackert HK: Chirurgisches Forum und DGAV Forum. Springer, Berlin, 2009.
17. Meyer SE, Hasenstein JR, Baktula A, et al: Kruppel-like factor 5 is not required for K-RasG12D lung tumorigenesis, but represses ABCG2 expression and is associated with better disease-specific survival. Am J Pathol 177: 1503-1513, 2010.
18. Tong D, Czerwenka K, Heinze G, et al: Expression of KLF5 is a prognostic factor for disease-free survival and overall survival in patients with breast cancer. Clin Cancer Res 12: 2442-2448, 2006.
19. Budihardjo I, Oliver H, Lutter M, Luo X and Wang X: Biochemical pathways of caspase activation during apoptosis. Annu Rev Cell Dev Biol 15: 269-290, 1999. (Pubitemid 32250377)
20. Ambrosini G, Adida C and Altieri DC: A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nat Med 3: 917-921, 1997. (Pubitemid 27353455)
21. Harris AL: Hypoxia - a key regulatory factor in tumour growth. Nature reviews. Cancer 2: 38-47, 2002.
22. Graves EE, Maity A and Le QT: The tumor microenvironment in non-small-cell lung cancer. Semin Rad Oncol 20: 156-163, 2010.
23. Cui J, Mao X, Olman V, Hastings PJ and Xu Y: Hypoxia and miscoupling between reduced energy efficiency and signaling to cell proliferation drive cancer to grow increasingly faster. J Mol Cell Biol 4: 174-176, 2012.
24. Bruick RK: Oxygen sensing in the hypoxic response pathway: regulation of the hypoxia-inducible transcription factor. Genes Dev 17: 2614-2623, 2003.
25. Lenihan CR and Taylor CT: The impact of hypoxia on cell death pathways. Biochem Soc Trans 41: 657-663, 2013.
26. Hu Y, Liu J and Huang H: Recent agents targeting HIF-1alpha for cancer therapy. J Cell Biochem 114: 498-509, 2013.
27. Diakiw SM, D'Andrea RJ and Brown AL: The double life of KLF5: opposing roles in regulation of gene-expression, cellular function, and transformation. IUBMB Life 65: 999-1011, 2013.
28. Nandan MO, Chanchevalap S, Dalton WB and Yang VW: Kruppel-like factor 5 promotes mitosis by activating the cyclin B1/Cdc2 complex during oncogenic Ras-mediated transformation. FEBS Lett 579: 4757-4762, 2005. (Pubitemid 41218659)
29. Reed JC: Dysregulation of apoptosis in cancer. J Clin Oncol 17: 2941-2953, 1999.
30. Ghavami S, Hashemi M, Ande SR, et al: Apoptosis and cancer: mutations within caspase genes. J Med Genet 46: 497-510, 2009.
31. Krepela E, Dankova P, Moravcikova E, et al: Increased expression of inhibitor of apoptosis proteins, survivin and XIAP, in non-small cell lung carcinoma. Int J Oncol 35: 1449-1462, 2009.
32. Zhu N, Gu L, Findley HW, et al: KLF5 interacts with p53 in regulating survivin expression in acute lymphoblastic leukemia. J Biol Chem 281: 14711-14718, 2006. (Pubitemid 43855176)
33. Yun YJ, Li SH, Cho YS, Park JW and Chun YS: Survivin mediates prostate cell protection by HIF-1alpha against zinc toxicity. Prostate 70: 1179-1188, 2010.
34. Van Hoecke M, Prigent-Tessier AS, Garnier PE, et al: Evidence of HIF-1 functional binding activity to caspase-3 promoter after photothrombotic cerebral ischemia. Mol Cell Neurosci 34: 40-47, 2007. (Pubitemid 46026929)
35. Majumder PK, Febbo PG, Bikoff R, et al: mTOR inhibition reverses Akt-dependent prostate intraepithelial neoplasia through regulation of apoptotic and HIF-1-dependent pathways. Nat Med 10: 594-601, 2004. (Pubitemid 38796850)
36. Zhong H, Chiles K, Feldser D, et al: Modulation of hypoxia-inducible factor 1alpha expression by the epidermal growth factor/phosphatidylinositol 3-kinase/PTEN/AKT/FRAP pathway in human prostate cancer cells: implications for tumor angiogenesis and therapeutics. Cancer Res 60: 1541-1545, 2000. (Pubitemid 30183422)
37. Park JH, Lee JY, Shin DH, Jang KS, Kim HJ and Kong G: Loss of Mel-18 induces tumor angiogenesis through enhancing the activity and expression of HIF-1alpha mediated by the PTEN/PI3K/Akt pathway. Oncogene 30: 4578-4589, 2011.
38. Zhang M, Ma Q, Hu H, et al: Stem cell factor/c-kit signaling enhances invasion of pancreatic cancer cells via HIF-1alpha under normoxic condition. Cancer Lett 303: 108-117, 2011.
39. Sodhi A, Montaner S, Patel V, et al: The Kaposi's sarcoma-associated herpes virus G protein-coupled receptor up-regulates vascular endothelial growth factor expression and secretion through mitogen-activated protein kinase and p38 pathways acting on hypoxia-inducible factor 1alpha. Cancer Res 60: 4873-4880, 2000.
40. Fukuda R, Hirota K, Fan F, Jung YD, Ellis LM and Semenza GL: Insulin-like growth factor 1 induces hypoxia-inducible factor 1-mediated vascular endothelial growth factor expression, which is dependent on MAP kinase and phosphatidylinositol 3-kinase signaling in colon cancer cells. J Biol Chem 277: 38205-38211, 2002. (Pubitemid 35154674)
41. Semenza GL: Targeting HIF-1 for cancer therapy. Nat Rev Cancer 3: 721-732, 2003.
42. Zundel W, Schindler C, Haas-Kogan D, et al: Loss of PTEN facilitates HIF-1-mediated gene expression. Genes Dev 14: 391-396, 2000. (Pubitemid 30131884)
43. Liu R, Zheng HQ, Zhou Z, Dong JT and Chen C: KLF5 promotes breast cell survival partially through fibroblast growth factor-binding protein 1-pERK-mediated dual specificity MKP-1 protein phosphorylation and stabilization. J Biol Chem 284: 16791-16798, 2009.
44. Schofield CJ and Ratcliffe PJ: Oxygen sensing by HIF hydroxylases. Nat Rev Mol Cell Biol 5: 343-354, 2004. (Pubitemid 38579472)
45. Forsythe JA, Jiang BH, Iyer NV, et al: Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 16: 4604-4613, 1996. (Pubitemid 26272112)
46. Melillo G, Musso T, Sica A, Taylor LS, Cox GW and Varesio L: A hypoxia-responsive element mediates a novel pathway of activation of the inducible nitric oxide synthase promoter. J Exp Med 182: 1683-1693, 1995.
47. Feldser D, Agani F, Iyer NV, Pak B, Ferreira G and Semenza GL: Reciprocal positive regulation of hypoxia-inducible factor 1alpha and insulin-like growth factor 2. Cancer Res 59: 3915-3918, 1999. (Pubitemid 29393552)
48. Lofstedt T, Jogi A, Sigvardsson M, et al: Induction of ID2 expression by hypoxia-inducible factor-1: a role in dedifferentiation of hypoxic neuroblastoma cells. J Biol Chem 279: 39223-39231, 2004. (Pubitemid 39258183)
49. Yee Koh M, Spivak-Kroizman TR and Powis G: HIF-1 regulation: not so easy come, easy go. Trends Biochem Sci 33: 526-534, 2008.
50. Zou C, Yu S, Xu Z, et al: ERRalpha augments HIF-1 signalling by directly interacting with HIF-1alpha in normoxic and hypoxic prostate cancer cells. J Pathol 233: 61-73, 2014.
51. Jung JE, Kim HS, Lee CS, et al: STAT3 inhibits the degradation of HIF-1alpha by pVHL-mediated ubiquitination. Exp Mol Med 40: 479-485, 2008. (Pubitemid 352789087)
52. Minet E, Mottet D, Michel G, et al: Hypoxia-induced activation of HIF-1: role of HIF-1alpha-Hsp90 interaction. FEBS Lett 460: 251-256, 1999. (Pubitemid 29495950)
53. Ohh M, Park CW, Ivan M, et al: Ubiquitination of hypoxia-inducible factor requires direct binding to the beta-domain of the von Hippel-Lindau protein. Nat Cell Biol 2: 423-427, 2000.
54. Mori A, Moser C, Lang SA, et al: Upregulation of Kruppel-like factor 5 in pancreatic cancer is promoted by interleukin-1beta signaling and hypoxia-inducible factor-1alpha. Mol Cancer Res 7: 1390-1398, 2009.