EBV latent membrane protein 1 up-regulates hypoxia-inducible factor 1α through Siah1-mediated down-regulation of prolyl hydroxylases 1 and 3 in nasopharyngeal epithelial cells

Cancer Research

Volumn 66, Issue 20, 2006, Pages 9870-9877

  Kondo, Satoru ^a,c   Seo, So Young ^b   Yoshizaki, Tomokazu ^c   Wakisaka, Naohiro ^c   Furukawa, Mitsuru ^c   Joab, Irene ^d   Jang, Kyung Lib ^a,b   Pagano, Joseph S ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b Pusan National University   (South Korea)

^c KANAZAWA UNIVERSITY   (Japan)

^d INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; LATENT MEMBRANE PROTEIN 1; ONCOPROTEIN; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; PROTEIN SIAH 1; PROTEIN SIAH 2; TUMOR SUPPRESSOR PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; VON HIPPEL LINDAU PROTEIN;

ANGIOGENESIS; ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; CYTOPLASM; DOWN REGULATION; EPITHELIUM CELL; EPSTEIN BARR VIRUS; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; NASOPHARYNX; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STABILITY; UPREGULATION;

BREAST NEOPLASMS; CELL LINE, TUMOR; CELL NUCLEUS; CYTOPLASM; DOWN-REGULATION; EPITHELIAL CELLS; EPSTEIN-BARR VIRUS INFECTIONS; HELA CELLS; HERPESVIRUS 4, HUMAN; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; NASOPHARYNX; NUCLEAR PROTEINS; PROCOLLAGEN-PROLINE DIOXYGENASE; TRANSFECTION; UBIQUITIN-PROTEIN LIGASES; UP-REGULATION; VIRAL MATRIX PROTEINS;

EID: 33750537081     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-06-1679     Document Type: Article

References (51)

1. Rickinson AB, Kieff E. Epstein-Barr virus. In: Knipe DM, Howley PM, editors. Virology. 4th ed. Philadelphia: Lippincott Williams and Wilkins; 2001. p. 2575-627.
2. Pagano JS, Blaser M, Buendia MA, et al. Infectious agents and cancer: criteria for a causal relation. Semin Cancer Biol 2004;14:453-71.
3. Yoshizaki T, Sato H, Furukawa M, Pagano JS. The expression of matrix metalloproteinase 9 is enhanced by Epstein-Barr virus latent membrane protein 1. Proc Natl Acad U S A 1998;95:3621-6.
4. Wakisaka N, Murono S, Yoshizaki T, Furukawa M, Pagano JS. Epstein-Barr virus latent membrane protein 1 induces and causes release of fibroblast growth factor-2, Cancer Res 2002;22:6337-44.
5. Kim KR, Yoshizaki T, Miyamori H, et al. Transformation of Madin-Darby canine kidney (MDCK) epithelial cells by Epstein-Barr virus latent membrane protein 1 (LMP1) induces expression of Ets1 and invasive growth. Oncogene 2002;19:1764-71.
6. Kondo S, Wakisaka N, Schell MJ, et al. Epstein-Barr virus latent membrane protein 1 induces the matrix metalloproteinase-1 promoter via an Ets binding site formed by a single nucleotide polymorphism: enhanced susceptibility to nasopharyngeal carcinoma. Int J Cancer 2005;115:368-76.
7. Murono S, Inoue H, Tanabe T, et al. Induction of cyclooxygenase-2 by Epstein-Barr virus latent membrane protein 1 is involved in vascular endothelial growth factor production in nasopharyngeal carcinoma cells. Proc Natl Acad U S A 2001;98:6905-10.
8. Wakisaka N, Kondo S, Yoshizaki T, Murono S, et al. Epstein-Barr virus latent membrane protein 1 induces synthesis of hypoxia-inducible factor 1. Mol Cell Biol 2004;24:5223-34.
9. 2 tension. Proc Natl Acad Sci U S A 1995;92:5510-4.
10. 2 tension. Am J Physiol 1996;271:1172-80.
11. Wang V, Davis DA, Haque M, Huang LE, Yarchoan R. Differential gene up-regulation by hypoxia-inducible factor-1 and hypoxia-inducible factor-2α in HEK293T cells. Cancer Res 2005;65:3299-306.
12. Masson N, Ratcliffe PJ. HIF prolyl and asparaginyl hydroxylases in the biological response to intracellular O(2) levels. J Cell Sci 2003;116:3041-9.
13. Bruick RK, McKnight SL. A conserved family of prolyl-4-hydroxylases that modify HIF. Science 2001;294: 1337-40.
14. 2, and the 3 PHDs: how animal cells signal hypoxia to nucleus. Cell 2001;107:1-3.
15. 2 sensing. Science 2001;292:464-8.
16. 2-regulated prolyl hydroxylation. Science 2001;292:468-72.
17. Maxwell PH, Wiesener MS, Chang GW, et al. The tumor suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 1999;399:271-5.
18. Carthew RW, Rubin GM. Seven in absentia, a gene required for specification of R7 cell fate in the Drosophila eye. Cell 1990;63:561-77.
19. Della NG, Senior PV, Bowtell DD. Isolation and characterisation of murine homologues of the Drosophlia seven in absentia gene (sina). Development 1993;117: 1333-43.
20. Hu G, Chung YL, Glover T, Valentine V, et al. Characterization of human homologs of the Drosophila seven in absentia (sina) gene. Genomics 1997;11:2701-14.
21. Hu G, Zhang S, Vidal M, et al. Mammalian homologs of seven in absentia regulate DCC via the ubiquitin-proteasome pathway. Genes Dev 1997;11:2701-14.
22. Liu J, Stevens J, Rote CA, et al. Siah-1 mediates a novel β-catenin degradation pathway linking p53 to the adenomatous polyposis coli protein. Mol Cell 2001;7: 927-36.
23. Tanikawa J, Ichikawa-Iwata E, Kanei-Ishii C, et al. p53 suppresses the c-Myb-induced activation of heat shock transcription factor 3. J Biol Chem 2000;275:15578-85.
24. Nakayama K, Frew IJ, Hagensen M, et al. Siah2 regulates stability of prolyl-hydroxylases, controls HIF1 abundance, and modulates physiological responses to hypoxia. Cell 2004;117:941-52.
25. Jang KL, Shackelford J, Seo SY, Pagano JS. Up-regulation of β-catenin by a viral oncogene correlates with inhibition of the seven in absentia homolog 1 in B lymphoma cells. Proc Natl Acad Sci U S A 2005;102: 18431-6.
26. Contreras-Brodin BA Anvret M, Imreh S, et al. B cell phenotype-dependent expression of the Epstein-Barr virus nuclear antigens EBNA-2 to EBNA-6: studies with somatic cell hybrids. J Gen Virol 1991;72:3025-33.
27. Takimoto T, Sato H, Ogura H, Glaser R. Superinfection of epithelial hybrid cells (D98/HR-1, NPC-KT, and A2L/AH) with Epstein-Barr virus and the relationship to the C3d receptor. Cancer Res 1986;46:2085-7.
28. Zhang L, Wu L, Hong K, Pagano JS. Intracellular signaling molecules activated by Epstein-Barr virus for induction of interferon regulatory factor 7. J Virol 2001; 75:12393-401.
29. Yue W, Davenport MG, Shackelford J, Pagano JS. Mitosis-specific hyperphosphorylation of Epstein-Barr virus nuclear antigen 2 suppresses its function. J Virol 2004;78:3542-52.
30. Yoshizaki T, Wakisaka N, Pagano JS. Epstein-Barr Virus, Invasion and metastasis, chapter 12. In: E. Robertson, editor. Epstein-Barr virus. Norfolk (United Kingdom): Caister Academic Press; 2005. pp 171-96.
31. Arbach H, Viglasky V, Lefeu F, et al. Epstein-Barr virus (EBV) genome and expression in breast cancer tissue: effect of EBV infection of breast cancer cells on resistance to paclitaxed (Taxol). J Virol 2006;80:845-53.
32. Curran JA, Laverty FS, Campbell D, Macdiarmid J, Wilson JB. Epstein-Barr virus encoded latent membrane protein-1 induces epithelial cell proliferation and sensitizes transgenic mice to chemical carcinogenesis. Cancer Res 1994;61:6730-8.
33. Matsuzawa S, Takayama S, Froesch BA, Zapata JM, Reed JC. p53-inducible human homologue of Drosophila seven in absentia (Siah) inhibits cell growth: suppression by BAG-1. EMBO J 1998;17:2736-47.
34. Roperch J, Lethrone F, Prieur S, et al. SIAH-1 promotes apoptosis and tumor suppression through a network involving the regulation of protein folding, unfolding, and trafficking: identification of common effectors with p53 and p21. Proc Natl Acad U S A 1999; 96:8070-3.
35. Wang D, Liebowitz D, Kieff E. An EBV membrane protein expressed in immortalized lymphocytes transforms established rodent cells. Cell 1985;43:831-40.
36. Dawson CW, Rickinson AB, Young LS. Epstein-Barr virus latent membrane protein inhibits human epithelial cell differentiation. Nature 1990;344:777-80.
37. Fahraeus R, Rymo L, Rhim SJ, Klein G. Morphological transformation of human keratinocytes expressing the LMP gene of Epstein-Barr virus. Nature 1990;345:447-9.
38. Kulwichit W, Edwards RH, Davenport EM, et al. Expression of the Epstein-Barr virus latent membrane protein 1 induces B cell lymphoma in transgenic mice. Proc Natl Acad U S A 1998;95:11963-8.
39. Page EL, Robitaille GA, Pouyssegur J, Richard DE. Induction of hypoxia-inducible factor-1α by transcriptional and translational mechanisms. J Biol Chem 2002; 277:48403-9.
40. Metzen E, Berchner-Pfannschmidt U, Stengel P, et al. Intracellular localization of human HIF-1 α hydroxylases: implications for oxygen sensing. J Cell Sci 2003; 116:1319-26.
41. Appenhoff RJ, Tian Y-M, Raval RR, et al. Differential regulation of the prolyl hydroxylases PDH1, PHD2, and PHD3 in the regulation of hypoxia-inducible factor. J Biol Chem 2004;279:38458-65.
42. Berra E, Benizri E, Ginouvès A, Volmat V, Roux D, Pouysségur J. HIF prolyl-hydroxylase 2 is the key oxygen sensor setting low steady-state levels of HIF-1α in normoxia. EMBO J 2003;22:4082-90.
43. Xu Z, Sproul A, Wang W, Kukekov N, Greene LA. Siah1 interacts with the scaffold protein POSH to promote JNK activation and apoptosis. J Biol Chem 2006;281:303-12.
44. Wan J, Sun L, Mendoza JW, et al. Elucidation of the c-Jun N-terminal kinase pathway mediated by Estein-Barr virus-encoded latent membrane protein 1. Mol Cell Biol 2004;24:192-9.
45. Shackelford J, Maier C, Pagano JS. Epstein-Barr virus activates β-catenin in type III latently infected B lymphocyte lines: association with deubiquitinating enzymes. Proc Natl Acad Sci U S A 2003;100:15572-6.
46. 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 1α. Cancer Res 2000;60:4873-80.
47. Moon EJ, Jeong CH, Kim KR et al. Hepatitis B virus X protein induces angiogenesis by stabilizing hypoxia-inducible factor-1. FASEB J 2004;18:382-4.
48. Nemani M, Linares-Cruz G, Bruzzoni-Giovanelli H, et al. Activation of the human homologue of the Drosophila sina gene in apoptosis and tumor suppression. Proc Natl Acad Sci U S A 1996;93:9039-42.
49. Medhioub M, Vaury C, Hamelin R, Thomas G. Lack of somatic mutation in the coding sequence of SIAH1 in tumors hemizygous for this candidate tumor suppressor gene. Int J Cancer 2000;87:794-7.
50. Johnsen SA, Subramaniam M, Monroe DG, Janknecht R, Spelsberg TC. Modulation of transforming growth factor β(TGFβ)/Smad transcriptional responses through targeted degradation of TGFβ-inducible early gene-1 by human seven in absentia homologue. J Biol Chem 2002;277:30754-9.
51. Shibata D, Reale Lavin P, Silverman M, et al. The DCC protein and prognosis in colorectal cancer. N Engl J Med 1996;335:1727-32.