Hypoxia upregulates ovarian cancer invasiveness via the binding of HIF-1α to a hypoxia-induced, methylation-free hypoxia response element of S100A4 gene

International Journal of Cancer

Volumn 131, Issue 8, 2012, Pages 1755-1767

  Horiuchi, Akiko ^a   Hayashi, Takuma ^a   Kikuchi, Norihiko ^a   Hayashi, Akiko ^a   Fuseya, Chiho ^a   Shiozawa, Tanri ^a   Konishi, Ikuo ^b  

^a SHINSHU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

hypomethylation; hypoxia; ovarian carcinoma; S100A4

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; CANCER INVASION; CANCER PROGNOSIS; CARCINOMA CELL; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; EPIGENETICS; GENE EXPRESSION REGULATION; GENE LOCATION; HUMAN; HUMAN CELL; INTRON; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; ONCOGENE; OVARY CANCER; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN METHYLATION; S100A4 GENE; UPREGULATION;

ADENOCARCINOMA, CLEAR CELL; ADENOCARCINOMA, MUCINOUS; ANIMALS; ANOXIA; BLOTTING, WESTERN; CHROMATIN IMMUNOPRECIPITATION; CYSTADENOCARCINOMA, SEROUS; DNA METHYLATION; ENDOMETRIAL NEOPLASMS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; FOLLOW-UP STUDIES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMMUNOENZYME TECHNIQUES; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOPLASM INVASIVENESS; OVARIAN NEOPLASMS; OVARY; PROGNOSIS; REAL-TIME POLYMERASE CHAIN REACTION; RESPONSE ELEMENTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; S100 PROTEINS;

EID: 84865311262     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.27448     Document Type: Article

References (49)

1. Joyce JA,. Therapeutic targeting of the tumor microenvironment. Cancer Cell 2005; 7: 513-20. (Pubitemid 40799245)
2. Semenza GL,. Defining the role of hypoxia-inducible factor 1 in cancer biology and therapeutics. Oncogene 2010; 29: 625-34. (Epub 2009 Nov 30).
3. Harris AL,. Hypoxiaâ€"a key regulatory factor in tumour growth. Nat Rev Cancer 2002; 2: 38-47. (Pubitemid 37328806)
4. Graeber TG, Osmanian C, Jacks T, Housman DE, Koch CJ, Lowe SW, Giaccia AJ,. Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature 1996; 379: 88-91. (Pubitemid 26008141)
5. Rankin EB, Giaccia AJ,. The role of hypoxia-inducible factors in tumorigenesis. Cell Death Differ 2008; 15: 678-85. (Pubitemid 351405072)
6. Semenza GL,. Regulation of mammalian O2 homeostasis by hypoxia-inducible factor 1. Annu Rev Cell Dev Biol 1999; 15: 551-78. (Pubitemid 32250386)
7. Imai T, Horiuchi A, Wang C, Oka K, Ohira S, Nikaido T, Konishi I,. Hypoxia attenuates the expression of E-cadherin via up-regulation of SNAIL in ovarian carcinoma cells. Am J Pathol 2003; 163: 1437-47. (Pubitemid 37175091)
8. Horiuchi A, Imai T, Shimizu M, Oka K, Wang C, Nikaido T, Konishi I,. Hypoxia-induced changes in the expression of VEGF, HIF-1 alpha and cell cycle-related molecules in ovarian cancer cells. Anticancer Res 2002; 22: 2697-702. (Pubitemid 36069300)
9. Osada R, Horiuchi A, Kikuchi N, Yoshida J, Hayashi A, Ota M, Katsuyama Y, Melillo G, Konishi I,. Expression of hypoxia-inducible factor 1alpha, hypoxia-inducible factor 2alpha, and von Hippel-Lindau protein in epithelial ovarian neoplasms and allelic loss of von Hippel-Lindau gene: nuclear expression of hypoxia-inducible factor 1alpha is an independent prognostic factor in ovarian carcinoma. Hum Pathol 2007; 38: 1310-20. (Pubitemid 47247486)
10. Donato R,. S100: a multigenic family of calcium-modulated proteins of the EF-hand type with intracellular and extracellular functional roles. Int J Biochem Cell Biol 2001; 33: 637-68. (Pubitemid 32520962)
11. Boye K, Maelandsmo GM,. S100A4 and metastasis: a small actor playing many roles. Am J Pathol 2010; 176: 528-35.
12. Hiratsuka S, Nakamura K, Iwai S, Murakami M, Itoh T, Kijima H, Shipley JM, Senior RM, Shibuya M,. MMP9 induction by vascular endothelial growth factor receptor-1 is involved in lung-specific metastasis. Cancer Cell 2002; 2: 289-300. (Pubitemid 41043963)
13. Hiratsuka S, Watanabe A, Aburatani H, Maru Y,. Tumour-mediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis. Nat Cell Biol 2006; 8: 1369-75. (Pubitemid 44835111)
14. Harris MA, Yang H, Low BE, Mukherjee J, Guha A, Bronson RT, Shultz LD, Israel MA, Yun K,. Cancer stem cells are enriched in the side population cells in a mouse model of glioma. Cancer Res 2008; 68: 10051-9.
15. Kikuchi N, Horiuchi A, Osada R, Imai T, Wang C, Chen X, Konishi I,. Nuclear expression of S100A4 is associated with aggressive behavior of epithelial ovarian carcinoma: an important autocrine/paracrine factor in tumor progression. Cancer Sci 2006; 97: 1061-9. (Pubitemid 44322555)
16. Sato N, Maitra A, Fukushima N, van Heek NT, Matsubayashi H, Iacobuzio-Donahue CA, Rosty C, Goggins M,. Frequent hypomethylation of multiple genes overexpressed in pancreatic ductal adenocarcinoma. Cancer Res 2003; 63: 4158-66. (Pubitemid 36917941)
17. Xie R, Loose DS, Shipley GL, Xie S, Bassett RL, Jr., Broaddus RR,. Hypomethylation-induced expression of S100A4 in endometrial carcinoma. Mod Pathol 2007; 20: 1045-54. (Pubitemid 47429198)
18. Rehman I, Goodarzi A, Cross SS, Leiblich A, Catto JW, Phillips JT, Hamdy FC,. DNA methylation and immunohistochemical analysis of the S100A4 calcium binding protein in human prostate cancer. Prostate 2007; 67: 341-7. (Pubitemid 46341075)
19. Rosty C, Ueki T, Argani P, Jansen M, Yeo CJ, Cameron JL, Hruban RH, Goggins M,. Overexpression of S100A4 in pancreatic ductal adenocarcinomas is associated with poor differentiation and DNA hypomethylation. Am J Pathol 2002; 160: 45-50. (Pubitemid 34052264)
20. Tulchinsky E, Grigorian M, Tkatch T, Georgiev G, Lukanidin E,. Transcriptional regulation of the mts1 gene in human lymphoma cells: the role of DNA-methylation. Biochim Biophys Acta 1995; 1261: 243-8.
21. Lujambio A, Esteller M,. How epigenetics can explain human metastasis: a new role for microRNAs. Cell Cycle 2009; 8: 377-82.
22. Goelz SE, Vogelstein B, Hamilton SR, Feinberg AP,. Hypomethylation of DNA from benign and malignant human colon neoplasms. Science 1985; 228: 187-90. (Pubitemid 15117274)
23. Feinberg AP, Vogelstein B,. Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature 1983; 301: 89-92. (Pubitemid 13154475)
24. Jang SJ, Soria JC, Wang L, Hassan KA, Morice RC, Walsh GL, Hong WK, Mao L,. Activation of melanoma antigen tumor antigens occurs early in lung carcinogenesis. Cancer Res 2001; 61: 7959-63. (Pubitemid 33049388)
25. Ehrlich M,. DNA methylation in cancer: too much, but also too little. Oncogene 2002; 21: 5400-13. (Pubitemid 34983477)
26. Yanagawa N, Tamura G, Honda T, Endoh M, Nishizuka S, Motoyama T,. Demethylation of the synuclein gamma gene CpG island in primary gastric cancers and gastric cancer cell lines. Clin Cancer Res 2004; 10: 2447-51. (Pubitemid 38445705)
27. Kwapiszewska G, Wilhelm J, Wolff S, Laumanns I, Koenig IR, Ziegler A, Seeger W, Bohle RM, Weissmann N, Fink L,. Expression profiling of laser-microdissected intrapulmonary arteries in hypoxia-induced pulmonary hypertension. Respir Res 2005; 6: 109.
28. Tsuruo T, Hamilton TC, Louie KG, Behrens BC, Young RC, Ozols RF,. Collateral susceptibility of adriamycin-, melphalan- and cisplatin-resistant human ovarian tumor cells to bleomycin. Jpn J Cancer Res 1986; 77: 941-5. (Pubitemid 16006790)
29. Nitta M, Katabuchi H, Ohtake H, Tashiro H, Yamaizumi M, Okamura H,. Characterization and tumorigenicity of human ovarian surface epithelial cells immortalized by SV40 large T antigen. Gynecol Oncol 2001; 81: 10-7. (Pubitemid 32368071)
30. Horiuchi A, Imai T, Wang C, Ohira S, Feng Y, Nikaido T, Konishi I,. Up-regulation of small GTPases, RhoA and RhoC, is associated with tumor progression in ovarian carcinoma. Lab Invest 2003; 83: 861-70. (Pubitemid 36723695)
31. Horiuchi A, Nikaido T, Taniguchi S, Fujii S,. Possible role of calponin h1 as a tumor suppressor in human uterine leiomyosarcoma. J Natl Cancer Inst 1999; 91: 790-6. (Pubitemid 29239059)
32. Horiuchi A, Nikaido T, Ito K, Zhai Y, Orii A, Taniguchi S, Toki T, Fujii S,. Reduced expression of calponin h1 in leiomyosarcoma of the uterus. Lab Invest 1998; 78: 839-46. (Pubitemid 28347880)
33. Wang C, Horiuchi A, Imai T, Ohira S, Itoh K, Nikaido T, Katsuyama Y, Konishi I,. Expression of BRCA1 protein in benign, borderline, and malignant epithelial ovarian neoplasms and its relationship to methylation and allelic loss of the BRCA1 gene. J Pathol 2004; 202: 215-23. (Pubitemid 38208659)
34. Grzendowski M, Wolter M, Riemenschneider MJ, Knobbe CB, Schlegel U, Meyer HE, Reifenberger G, Stuhler K,. Differential proteome analysis of human gliomas stratified for loss of heterozygosity on chromosomal arms 1p and 19q. Neuro Oncol 2010; 12: 243-56.
35. Wenger RH, Gassmann M,. Oxygen(es) and the hypoxia-inducible factor-1. Biol Chem 1997; 378: 609-16. (Pubitemid 27361853)
36. Wilkins JF,. Genomic imprinting and methylation: epigenetic canalization and conflict. Trends Genet 2005; 21: 356-65. (Pubitemid 40726393)
37. Okano M, Xie S, Li E,. Dnmt2 is not required for de novo and maintenance methylation of viral DNA in embryonic stem cells. Nucleic Acids Res 1998; 26: 2536-40. (Pubitemid 28297362)
38. Dokun OY, Florl AR, Seifert HH, Wolff I, Schulz WA,. Relationship of SNCG, S100A4, S100A9 and LCN2 gene expression and DNA methylation in bladder cancer. Int J Cancer 2008; 123: 2798-807.
39. Liao SH, Zhao XY, Han YH, Zhang J, Wang LS, Xia L, Zhao KW, Zheng Y, Guo M, Chen GQ,. Proteomics-based identification of two novel direct targets of hypoxia-inducible factor-1 and their potential roles in migration/invasion of cancer cells. Proteomics 2009; 9: 3901-12.
40. Zhang R, Fu H, Chen D, Hua J, Hu Y, Sun K, Sun X,. Subcellular distribution of S100A4 and its transcriptional regulation under hypoxic conditions in gastric cancer cell line BGC823. Cancer Sci 2010; 101: 1141-6.
41. Wenger RH, Kvietikova I, Rolfs A, Camenisch G, Gassmann M,. Oxygen-regulated erythropoietin gene expression is dependent on a CpG methylation-free hypoxia-inducible factor-1 DNA-binding site. Eur J Biochem 1998; 253: 771-7. (Pubitemid 28223547)
42. Raspaglio G, Filippetti F, Prislei S, Penci R, De Maria I, Cicchillitti L, Mozzetti S, Scambia G, Ferlini C,. Hypoxia induces class III beta-tubulin gene expression by HIF-1alpha binding to its 3†flanking region. Gene 2008; 409: 100-8.
43. Shahrzad S, Bertrand K, Minhas K, Coomber BL,. Induction of DNA hypomethylation by tumor hypoxia. Epigenetics 2007; 2: 119-25. (Pubitemid 351682006)
44. Skowronski K, Dubey S, Rodenhiser D, Coomber B,. Ischemia dysregulates DNA methyltransferases and p16INK4a methylation in human colorectal cancer cells. Epigenetics 2010; 5: 547-56.
45. Peng DF, Kanai Y, Sawada M, Ushijima S, Hiraoka N, Kitazawa S, Hirohashi S,. DNA methylation of multiple tumor-related genes in association with overexpression of DNA methyltransferase 1 (DNMT1) during multistage carcinogenesis of the pancreas. Carcinogenesis 2006; 27: 1160-8. (Pubitemid 43985431)
46. Sato M, Horio Y, Sekido Y, Minna JD, Shimokata K, Hasegawa Y,. The expression of DNA methyltransferases and methyl-CpG-binding proteins is not associated with the methylation status of p14(ARF), p16(INK4a) and RASSF1A in human lung cancer cell lines. Oncogene 2002; 21: 4822-9. (Pubitemid 34879457)
47. Hsieh HL, Schafer BW, Weigle B, Heizmann CW,. S100 protein translocation in response to extracellular S100 is mediated by receptor for advanced glycation endproducts in human endothelial cells. Biochem Biophys Res Commun 2004; 316: 949-59. (Pubitemid 38368045)
48. Flatmark K, Pedersen KB, Nesland JM, Rasmussen H, Aamodt G, Mikalsen SO, Bjornland K, Fodstad O, Maelandsmo GM,. Nuclear localization of the metastasis-related protein S100A4 correlates with tumour stage in colorectal cancer. J Pathol 2003; 200: 589-95. (Pubitemid 36987307)
49. Saleem M, Kweon MH, Johnson JJ, Adhami VM, Elcheva I, Khan N, Bin Hafeez B, Bhat KM, Sarfaraz S, Reagan-Shaw S, Spiegelman VS, Setaluri V, et al. S100A4 accelerates tumorigenesis and invasion of human prostate cancer through the transcriptional regulation of matrix metalloproteinase 9. Proc Natl Acad Sci USA 2006; 103: 14825-30. (Pubitemid 44527813)