HIF-2α mediates hypoxia-induced LIF expression in human colorectal cancer cells

Oncotarget

Volumn 6, Issue 6, 2015, Pages 4406-4417

  Wu, Lihua ^a,b   Yu, Haiyang ^a   Zhao, Yuhan ^a   Zhang, Cen ^a   Wang, Jiabei ^a   Yue, Xuetian ^a   Yang, Qifeng ^a,c   Hu, Wenwei ^a  

^a RUTGERS CANCER INSTITUTE OF NEW JERSEY   (United States)

^b ZHEJIANG UNIVERSITY   (China)

^c SHANDONG UNIVERSITY   (China)

Author keywords

HIF 2 ; Hypoxia; Hypoxia responsive element; Leukemia inhibitory factor

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; LEUKEMIA INHIBITORY FACTOR; SMALL INTERFERING RNA; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; ENDOTHELIAL PAS DOMAIN-CONTAINING PROTEIN 1; LIF PROTEIN, HUMAN;

ARTICLE; CELL HYPOXIA; COLORECTAL CANCER CELL LINE; CONTROLLED STUDY; GENE EXPRESSION; GENE INDUCTION; GENE SILENCING; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; LIF GENE; ONCOGENE; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; BIOSYNTHESIS; COLORECTAL TUMOR; GENE EXPRESSION REGULATION; METABOLISM; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL HYPOXIA; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LEUKEMIA INHIBITORY FACTOR;

EID: 84924234545     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3017     Document Type: Article

References (41)

1. Metcalf D. The unsolved enigmas of leukemia inhibitory factor. Stem cells. 2003; 21:5-14.
2. Williams RL, Hilton DJ, Pease S, Willson TA, Stewart CL, Gearing DP, Wagner EF, Metcalf D, Nicola NA, Gough NM. Myeloid leukaemia inhibitory factor maintains the developmental potential of embryonic stem cells. Nature. 1988; 336:684-687.
3. Stewart CL, Kaspar P, Brunet LJ, Bhatt H, Gadi I, Kontgen F, Abbondanzo SJ. Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature. 1992; 359:76-79.
4. Hu W, Feng Z, Teresky AK, Levine AJ. p53 regulates maternal reproduction through LIF. Nature. 2007; 450:721-724.
5. Kang HJ, Feng Z, Sun Y, Atwal G, Murphy ME, Rebbeck TR, Rosenwaks Z, Levine AJ, Hu W. Single-nucleotide polymorphisms in the p53 pathway regulate fertility in humans. Proc Natl Acad Sci U S A. 2009; 106:9761-9766.
6. Gearing DP. The leukemia inhibitory factor and its receptor. Advances in immunology. 1993; 53:31-58.
7. Heinrich PC, Behrmann I, Haan S, Hermanns HM, Muller-Newen G, Schaper F. Principles of interleukin (IL)-6-type cytokine signalling and its regulation. The Biochemical journal. 2003; 374:1-20.
8. Li X, Yang Q, Yu H, Wu L, Zhao Y, Zhang C, Yue X, Liu Z, Wu H, Haffty BG, Feng Z, Hu W. LIF promotes tumorigenesis and metastasis of breast cancer through the AKT-mTOR pathway. Oncotarget. 2014; 5:788-801.
9. Gearing DP, Gough NM, King JA, Hilton DJ, Nicola NA, Simpson RJ, Nice EC, Kelso A, Metcalf D. Molecular cloning and expression of cDNA encoding a murine myeloid leukaemia inhibitory factor (LIF). EMBO J. 1987; 6:3995-4002.
10. Fitzgerald JS, Tsareva SA, Poehlmann TG, Berod L, Meissner A, Corvinus FM, Wiederanders B, Pfitzner E, Markert UR, Friedrich K. Leukemia inhibitory factor triggers activation of signal transducer and activator of transcription 3, proliferation, invasiveness, and altered protease expression in choriocarcinoma cells. The international journal of biochemistry & cell biology. 2005; 37:2284-2296.
11. Quaglino A, Schere-Levy C, Romorini L, Meiss RP, Kordon EC. Mouse mammary tumors display Stat3 activation dependent on leukemia inhibitory factor signaling. Breast cancer research: BCR. 2007; 9:R69.
12. Suman P, Shembekar N, Gupta SK. Leukemia inhibitory factor increases the invasiveness of trophoblastic cells through integrated increase in the expression of adhesion molecules and pappalysin 1 with a concomitant decrease in the expression of tissue inhibitor of matrix metalloproteinases. Fertil Steril. 2013; 99:533-542.
13. Maruta S, Takiguchi S, Ueyama M, Kataoka Y, Oda Y, Tsuneyoshi M, Iguchi H. A role for leukemia inhibitory factor in melanoma-induced bone metastasis. Clinical & experimental metastasis. 2009; 26:133-141.
14. Wysoczynski M, Miekus K, Jankowski K, Wanzeck J, Bertolone S, Janowska-Wieczorek A, Ratajczak J, Ratajczak MZ. Leukemia inhibitory factor: a newly identified metastatic factor in rhabdomyosarcomas. Cancer Res. 2007; 67:2131-2140.
15. McKenzie RC, Szepietowski J. Cutaneous leukemia inhibitory factor and its potential role in the development of skin tumors. Dermatologic surgery: official publication for American Society for Dermatologic Surgery [et al]. 2004; 30:279-290.
16. Penuelas S, Anido J, Prieto-Sanchez RM, Folch G, Barba I, Cuartas I, Garcia-Dorado D, Poca MA, Sahuquillo J, Baselga J, Seoane J. TGF-beta increases glioma-initiating cell self-renewal through the induction of LIF in human glioblastoma. Cancer Cell. 2009; 15:315-327.
17. Yu H, Yue X, Zhao Y, Li X, Wu L, Zhang C, Liu Z, Lin K, Xu-Monette ZY, Young KH, Liu J, Shen Z, Feng Z, Hu W. LIF negatively regulates tumour-suppressor p53 through Stat3/ID1/MDM2 in colorectal cancers. Nature communications. 2014; 5:5218.
18. Liu SC, Tsang NM, Chiang WC, Chang KP, Hsueh C, Liang Y, Juang JL, Chow KP, Chang YS. Leukemia inhibitory factor promotes nasopharyngeal carcinoma progression and radioresistance. J Clin Invest. 2013; 123:5269-5283.
19. Lu X, Kang Y. Hypoxia and hypoxia-inducible factors: master regulators of metastasis. Clinical cancer research: an official journal of the American Association for Cancer Research. 2010; 16:5928-5935.
20. Wade M, Wahl GM. Targeting Mdm2 and Mdmx in cancer therapy: better living through medicinal chemistry? Mol Cancer Res. 2009; 7:1-11.
21. Marine JC, Dyer MA, Jochemsen AG. MDMX: from bench to bedside. J Cell Sci. 2007; 120:371-378.
22. Brannon AR, Vakiani E, Sylvester BE, Scott SN, McDermott G, Shah RH, Kania K, Viale A, Oschwald DM, Vacic V, Emde AK, Cercek A, Yaeger R, Kemeny NE, Saltz LB, Shia J, et al. Comparative sequencing analysis reveals high genomic concordance between matched primary and metastatic colorectal cancer lesions. Genome biology. 2014; 15:454.
23. Loboda A, Jozkowicz A, Dulak J. HIF-1 versus HIF-2-is one more important than the other? Vascular pharmacology. 2012; 56:245-251.
24. Kimura H, Weisz A, Kurashima Y, Hashimoto K, Ogura T, D'Acquisto F, Addeo R, Makuuchi M, Esumi H. Hypoxia response element of the human vascular endothelial growth factor gene mediates transcriptional regulation by nitric oxide: control of hypoxia-inducible factor-1 activity by nitric oxide. Blood. 2000; 95:189-197.
25. Raval RR, Lau KW, Tran MG, Sowter HM, Mandriota SJ, Li JL, Pugh CW, Maxwell PH, Harris AL, Ratcliffe PJ. Contrasting properties of hypoxia-inducible factor 1 (HIF-1) and HIF-2 in von Hippel-Lindau-associated renal cell carcinoma. Mol Cell Biol. 2005; 25:5675-5686.
26. Kimber SJ. Leukaemia inhibitory factor in implantation and uterine biology. Reproduction. 2005; 130:131-145.
27. Albrengues J, Bourget I, Pons C, Butet V, Hofman P, Tartare-Deckert S, Feral CC, Meneguzzi G, Gaggioli C. LIF mediates proinvasive activation of stromal fibroblasts in cancer. Cell reports. 2014; 7:1664-1678.
28. Feng Z, Zhang C, Kang HJ, Sun Y, Wang H, Naqvi A, Frank AK, Rosenwaks Z, Murphy ME, Levine AJ, Hu W. Regulation of female reproduction by p53 and its family members. FASEB J. 2011; 25:2245-2255.
29. Levine AJ, Hu W, Feng Z. The P53 pathway: what questions remain to be explored? Cell Death Differ. 2006; 13:1027-1036.
30. Vousden KH, Prives C. Blinded by the Light: The Growing Complexity of p53. Cell. 2009; 137:413-431.
31. Hainaut P, Hernandez T, Robinson A, Rodriguez-Tome P, Flores T, Hollstein M, Harris CC, Montesano R. IARC Database of p53 gene mutations in human tumors and cell lines: updated compilation, revised formats and new visualisation tools. Nucleic Acids Res. 1998; 26:205-213.
32. Rankin EB, Giaccia AJ. The role of hypoxia-inducible factors in tumorigenesis. Cell Death Differ. 2008; 15:678-685.
33. Hu CJ, Sataur A, Wang L, Chen H, Simon MC. The N-terminal transactivation domain confers target gene specificity of hypoxia-inducible factors HIF-1alpha and HIF-2alpha. Molecular biology of the cell. 2007; 18:4528-4542.
34. Lau KW, Tian YM, Raval RR, Ratcliffe PJ, Pugh CW. Target gene selectivity of hypoxia-inducible factor-alpha in renal cancer cells is conveyed by post-DNA-binding mechanisms. British journal of cancer. 2007; 96:1284-1292.
35. Hu CJ, Wang LY, Chodosh LA, Keith B, Simon MC. Differential roles of hypoxia-inducible factor 1alpha (HIF-1alpha) and HIF-2alpha in hypoxic gene regulation. Mol Cell Biol. 2003; 23:9361-9374.
36. Wang V, Davis DA, Haque M, Huang LE, Yarchoan R. Differential gene up-regulation by hypoxia-inducible factor-1alpha and hypoxia-inducible factor-2alpha in HEK293T cells. Cancer Res. 2005; 65:3299-3306.
37. Gordan JD, Bertout JA, Hu CJ, Diehl JA, Simon MC. HIF-2alpha promotes hypoxic cell proliferation by enhancing c-myc transcriptional activity. Cancer Cell. 2007; 11:335-347.
38. Covello KL, Kehler J, Yu H, Gordan JD, Arsham AM, Hu CJ, Labosky PA, Simon MC, Keith B. HIF-2alpha regulates Oct-4: effects of hypoxia on stem cell function, embryonic development, and tumor growth. Genes Dev. 2006; 20:557-570.
39. Holmquist-Mengelbier L, Fredlund E, Lofstedt T, Noguera R, Navarro S, Nilsson H, Pietras A, Vallon-Christersson J, Borg A, Gradin K, Poellinger L, Pahlman S. Recruitment of HIF-1alpha and HIF-2alpha to common target genes is differentially regulated in neuroblastoma: HIF-2alpha promotes an aggressive phenotype. Cancer Cell. 2006; 10:413-423.
40. Luo W, Zhong J, Chang R, Hu H, Pandey A, Semenza GL. Hsp70 and CHIP selectively mediate ubiquitination and degradation of hypoxia-inducible factor (HIF)-1alpha but Not HIF-2alpha. J Biol Chem. 2010; 285:3651-3663.
41. Yoshimura H, Dhar DK, Kohno H, Kubota H, Fujii T, Ueda S, Kinugasa S, Tachibana M, Nagasue N. Prognostic impact of hypoxia-inducible factors 1alpha and 2alpha in colorectal cancer patients: correlation with tumor angiogenesis and cyclooxygenase-2 expression. Clinical cancer research: an official journal of the American Association for Cancer Research. 2004; 10:8554-8560.