The hepatitis B virus X protein promotes tumor cell invasion by inducing membrane-type matrix metalloproteinase-1 and cyclooxygenase-2 expression

Journal of Clinical Investigation

Volumn 110, Issue 12, 2002, Pages 1831-1838

  Lara Pezzi, Enrique ^a   Victoria Gómez Gaviro, Maria ^a   Gálvez, Beatriz G ^a   Mira, Emilia ^b   Iñiguez, Miguel A ^c   Fresno, Manuel ^c   Carlos Martinez A ^b   Arroyo, Alicia G ^a   López Cabrera, Manuel ^a  

^a HOSPITAL UNIVERSITARIO DE LA PRINCESA   (Spain)

^b CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^c CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLSALICYLIC ACID; BB 3103; CYCLOOXYGENASE 2; DIMETHYL SULFOXIDE; DOXYCYCLINE; GELATINASE A; INDOMETACIN; INTERSTITIAL COLLAGENASE; MATRIX METALLOPROTEINASE INHIBITOR; MELOXICAM; N (2 CYCLOHEXYLOXY 4 NITROPHENYL)METHANESULFONAMIDE; PROTEIN X; TETRACYCLINE DERIVATIVE; TRANSCRIPTION FACTOR NFAT; VIRUS PROTEIN;

ARTICLE; CANCER INVASION; CANCER RECURRENCE; DISEASE ASSOCIATION; ENZYME ACTIVATION; ENZYME ACTIVITY; HEPATITIS B; HEPATITIS B VIRUS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL CARCINOMA; METASTASIS; NONHUMAN; PRIORITY JOURNAL; PROGNOSIS; PROMOTER REGION; PROTEIN EXPRESSION; TRANSCRIPTION INITIATION; TUMOR CELL; UPREGULATION;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; CARCINOMA, HEPATOCELLULAR; CHICK EMBRYO; CULTURE MEDIA, SERUM-FREE; CYCLOOXYGENASE 2; ENZYME ACTIVATION; ENZYME INHIBITORS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, REPORTER; HEPATITIS B ANTIGENS; HUMANS; ISOENZYMES; LIVER NEOPLASMS; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASES, MEMBRANE-ASSOCIATED; MEMBRANE PROTEINS; METALLOENDOPEPTIDASES; NEOPLASM INVASIVENESS; PROGNOSIS; PROMOTER REGIONS (GENETICS); PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; TRANS-ACTIVATION (GENETICS); TRANS-ACTIVATORS; TUMOR CELLS, CULTURED; UP-REGULATION;

EID: 0036955336     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI200215887     Document Type: Article

References (34)

1. Schafer, D.F., and Sorrell, M.F. 1999. Hepatocellular carcinoma. Lancet. 353:1253-1257.
2. Feitelson, M.A., and Duan, L.-X. 1997. Hepatitis B virus X antigen in the pathogenesis of chronic infections and the development of hepatocellular carcinoma. Am. J. Pathol. 150:1141-1157.
3. Su, Q., et al. 1998. Expression of hepatitis B virus X protein in HBV-infected human livers and hepatocellular carcinomas. Hepatology. 27:1109-1120.
4. Kim, C.M., et al. 1991. HBx gene of hepatitis B virus induces liver cancer in transgenic mice. Nature. 351:317-320.
5. Slagle, B.L., Lee, T.H., Medina, D., Finegold, M.J., and Butel, J.S. 1996. Increased sensitivity to the hepatocarcinogen diethylnitrosamine in transgenic mice carrying the hepatitis B virus X gene. Mol. Carcinog. 15:261-269.
6. Terradillos, O., et al. 1997. The hepatitis B virus X gene potentiates c-myc-induced liver oncogenesis in transgenic mice. Oncogene. 14:395-404.
7. Kekulé, A., Lauer, U., Weiss, L., Luber, B., and Hofsschneider, P. 1993. Hepatitis B virus transactivator HBx uses a tumour promoter signalling pathway. Nature. 361:742-745.
8. Shih, W.L., Kuo, M.L., Chuang, S.E., Cheng, A.L., and Doong, S.L. 2000. Hepatitis B virus X protein inhibits transforming growth factor-beta-induced apoptosis through the activation of phosphatidylinositol 3-kinase pathway. J. Biol. Chem. 275:25858-25864.
9. Werb, Z. 1997. ECM and cell surface proteolysis: Regulating cellular ecology. Cell. 91:439-442.
10. Harada, T., et al. 1998. Membrane-type matrix metalloproteinase-1 (MT1-MMP) gene is overexpressed in highly invasive hepatocellular carcinoma. J. Hepatol. 28:231-239.
11. Théret, N., et al. 2001. Increased extracellular matrix remodelling is associated with tumor progression in human hepatocellular carcinoma. Hepatology. 34:82-88.
12. Tsujii, M., Kawano, S., and DuBois, R.N. 1997. Cyclooxygenase-2 expression in human colon cancer cells increases metastatic potential. Proc. Natl. Acad. Sci. USA. 94:3336-3340.
13. Williams, C.S., Mann, M., and DuBois, R.N. 1999. The role of cyclooxygenases in inflammation, cancer and development. Oncogene. 18:7908-7916.
14. Koga, H., et al. 1999. Expression of cyclooxygenase-2 in human hepatocellular carcinoma: Relevance to tumor dedifferentiation. Hepatology. 29:688-696.
15. Liu, C.H., et al. 2001. Overexpression of cyclooxygenase-2 is sufficient to induce tumorigenesis in transgenic mice. J. Biol. Chem. 276:18563-18569.
16. Lara-Pezzi, E., et al. 2001. Effect of the hepatitis B virus HBx protein on integrin-mediated adhesion to and migration on extracellular matrix. J. Hepatol. 34:409-415.
17. Lara-Pezzi, E., et al. 2001. The hepatitis B virus X protein (HBx) induces a migratory phenotype in a CD44-dependent manner: Possible role of HBx in invasion and metastasis. Hepatology. 33:1270-1281.
18. Lara-Pezzi, E., Roche, S., Andrisani, O.M., Sanchez-Madrid, F.,and Lopez-Cabrera, M. 2001. The hepatitis B virus HBx protein induces adherens junction disruption in a src-dependent manner. Oncogene. 20:3323-3331.
19. Lee, J.S., and Thorgeirsson, S.S. 2002. Functional and genomic implications of global gene expression profiles in cell lines from human hepatocellular cancer. Hepatology. 35:1134-1143.
20. Wang, W., London, W.T., Lega, L., and Feitelson, M.A. 1991. HBxAg in the liver from carrier patients with chronic hepatitis and cirrhosis. Hepatology. 14:29-37.
21. Tarn, C., Bilodeau, M.L., Hullinger, R.L., and Andrisani, O.M. 1999. Differential immediate early gene expression in conditional hepatitis B virus pX-transforming versus nontransforming hepatocyte cell lines. J. Biol. Chem. 274:2327-2336.
22. Gálvez, B.G., Matías-Román, S., Albar, J.P., Sánchez-Madrid, F., and Arroyo, A.G. 2001. Membrane type 1-matrix metalloproteinase is activated during migration of human endothelial cells and modulates endothelial motility and matrix remodeling. J. Biol. Chem. 276:37491-37500.
23. Mira, E., Lacalle, R.A., Gómez-Moutón, C., Leonardo, E., and Mañés, S. 2002. Quantitative determination of tumor cell intravasation in a real-time polymerase chain reaction-based assay. Clin. Exp. Metastasis. 19:313-318.
24. Iñiguez, M.A., Martínez-Martínez, S., Punzón, C., Redondo, J.M., and Fresno, M. 2000. An essential role of the nuclear factor of activated T cells in the regulation of the expression of the cyclooxygenase-2 gene in human T lymphocytes. J. Biol. Chem. 275:23627-23635.
25. Lara-Pezzi, E., Armesilla, A.L., Majano, P.L., Redondo, J.M., and Lopez-Cabrera, M. 1998. The hepatitis B virus X protein activates nuclear factor of activated T cells (NF-AT) by a cyclosporin A-sensitive pathway. EMBOJ. 17:7066-7077.
26. Kajita, M., et al. 2001. Membrane-type 1 matrix metalloproteinase cleaves CD44 and promotes cell migration. J. Cell Biol. 153:893-904.
27. Hotary, K., Allen, E., Punturieri, A., Yana, L., and Weiss, S.J. 2000. Regulation of cell invasion and morphogenesis in a three-dimensional type I collagen matrix by membrane-type matrix metalloproteinases 1, 2 and 3. J. Cell Biol. 149:1309-1323.
28. Dohadwala, M., et al. 2001. Non-small cell lung cancer cyclooxygenase-2-dependent invasion is mediated by CD44. J. Biol. Chem. 276:20809-20812.
29. Tsujii, M., et al. 1998. Cyclooxygenase regulates angiogenesis induced by colon cancer cells. Cell. 93:705-716.
30. Majano, P.L., et al. 1998. Inducible nitric oxide synthase expression in chronic viral hepatitis. J. Clin. Invest. 101:1343-1352.
31. Yoo, Y.D., et al. 1996. Regulation of transforming growth factor-β1 expression by the hepatitis B virus (HBV) X transactivator. J. Clin. Invest. 97:388-395.
32. Giambartolomei, S., et al. 1999. Nonsteroidal anti-inflammatory drug metabolism potentiates interferon alfa signaling by increasing STAT1 phosphorylation. Hepatology. 30:510-516.
33. Bouchard, M.J., Wang, L.H., and Schneider, R.J. 2001. Calcium signaling by HBx protein in hepatitis B virus DNA replication. Science. 294:2376-2378.
34. Waris, G., Huh, K.-W., and Siddiqui, A. 2001. Mitochondrially associated hepatitis B virus X protein constitutively activates transcription factors STAT-3 and NF-κB via oxidative stress. Mol. Cell. Biol. 21:7721-7730.