Cyclooxygenase-2 Promotes Human Cholangiocarcinoma Growth: Evidence for Cyclooxygenase-2-Independent Mechanism in Celecoxib-Mediated Induction of p21waf1/cip1 and p27kip1 and Cell Cycle Arrest

Cancer Research

Volumn 64, Issue 4, 2004, Pages 1369-1376

  Han, Chang ^a   Leng, Jing ^a,b   Demetris, A Jake ^a   Wu, Tong ^a,c  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b NANJING MEDICAL UNIVERSITY   (China)

^c PRESBYTERIAN UNIVERSITY HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELECOXIB; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 1B; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITOR; PROSTAGLANDIN E2; PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BILE DUCT CARCINOMA; CANCER GROWTH; CANCER INHIBITION; CELL CYCLE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL GROWTH; CONTROLLED STUDY; DOSE RESPONSE; DRUG MECHANISM; GENE OVEREXPRESSION; GROWTH REGULATION; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN EXPRESSION;

BILE DUCT NEOPLASMS; BILE DUCTS, INTRAHEPATIC; CELL CYCLE; CELL CYCLE PROTEINS; CELL LINE, TUMOR; CHOLANGIOCARCINOMA; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLIN-DEPENDENT KINASE INHIBITOR P27; CYCLINS; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITORS; CYCLOOXYGENASE INHIBITORS; DINOPROSTONE; HUMANS; ISOENZYMES; MEMBRANE PROTEINS; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; PYRAZOLES; SULFONAMIDES; TUMOR SUPPRESSOR PROTEINS;

EID: 1242271219     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-03-1086     Document Type: Article

References (69)

1. Gores, G. J. Cholangiocarcinoma: current concepts and insights. Hepatology, 37: 961-969, 2003.
2. Chariyalertsak, S., Sirikulchayanonta, V., Mayer, D., Kopp-Schneider, A., Furstenberger, G., Marks, F., and Muller-Decker, K. Aberrant cyclooxygenase isozyme expression in human intrahepatic cholangiocarcinoma. Gut, 48: 80-86, 2001.
3. Sirica, A. E., Lai, G. H., and Zhang, Z. Biliary cancer growth factor pathways, cyclo-oxygenase-2 and potential therapeutic strategies. J. Gastroenterol. Hepatol., 16: 363-372, 2001.
4. Endo, K., Yoon, B. I., Pairojkul, C., Demetris, A. J., and Sirica, A. E. ERBB-2 overexpression and cyclooxygenase-2 up-regulation in human cholangiocarcinoma and risk conditions. Hepatology, 36: 439-450, 2002.
5. Hayashi, N., Yamamoto, H., Hiraoka, N., Dono, K., Ito, Y., Okami, J., Kondo, M., Nagano, H., Umeshita, K., Sakon, M., Matsuura, N., Nakamori, S., and Monden, M. Differential expression of cyclooxygenase-2 (COX-2) in human bile duct epithelial cells and bile duct neoplasm. Hepatology, 34: 638-650, 2001.
6. Fitzpatrick, F. A., and Soberman, R. Regulated formation of eicosanoids. J. Clin. Investig., 107: 1347-1351, 2001.
7. Gupta, R. A., and Dubois, R. N. Colorectal cancer prevention and treatment by inhibition of cyclooxygenase-2. Nat. Rev. Cancer, 1: 11-21, 2001.
8. Fosslien, E. Molecular pathology of cyclooxygenase-2 in neoplasia. Ann. Clin. Lab. Sci., 30: 3-21, 2000.
9. Fournier, D. B., and Gordon, G. B. COX-2 and colon cancer: potential targets for chemoprevention. J. Cell. Biochem. Suppl., 34: 97-102, 2000.
10. Gately, S. The contributions of cyclooxygenase-2 to tumor angiogenesis. Cancer Metastasis Rev., 19: 19-27, 2000.
11. Williams, C. S., Mann, M., and DuBois, R. N. The role of cyclooxygenases in inflammation, cancer, and development. Oncogene, 18: 7908-7916, 1999.
12. Smith, W. L., and Langenbach, R. Why there are two cyclooxygenase isozymes. J. Clin. Investig., 107: 1491-1495, 2001.
13. Dubois, R. N., Abramson, S. B., Crofford, L., Gupta, R. A., Simon, L. S., Van De Putte, L. B., and Lipsky, P. E. Cyclooxygenase in biology and disease. FASEB J., 12: 1063-1073, 1998.
14. Levy, G. N. Prostaglandin H synthases, nonsteroidal anti-inflammatory drugs, and colon cancer. FASEB J., 11: 234-247, 1997.
15. Schreinemachers, D. M., and Everson, R. B. Aspirin use and lung, colon, and breast cancer incidence in a prospective study. Epidemiology, 5: 138-146, 1994.
16. Giovannucci, E., Egan, K. M., Hunter, D. J., Stampfer, M. J., Colditz, G. A., Willett, W. C., and Speizer, F. E. Aspirin and the risk of colorectal cancer in women. N. Engl. J. Med., 333: 609-614, 1995.
17. Taketo, M. M. Cyclooxygenase-2 inhibitors in tumorigenesis (part I). J. Natl. Cancer Inst., 90: 1529-1536, 1998.
18. Taketo, M. M. Cyclooxygenase-2 inhibitors in tumorigenesis (part II). J. Natl. Cancer Inst., 90: 1609-1620, 1998.
19. Marnett, L. J., and DuBois, R. N. COX-2: a target for colon cancer prevention. Annu. Rev. Pharmacol. Toxicol., 42: 55-80, 2002.
20. Thun, M. J., Henley, S. J., and Patrono, C. Nonsteroidal anti-inflammatory drugs as anticancer agents: mechanistic, pharmacologic, and clinical issues. J. Natl. Cancer Inst., 94: 252-266, 2002.
21. Tsujii, M., and DuBois, R. N. Alterations in cellular adhesion and apoptosis in epithelial cells overexpressing prostaglandin endoperoxide synthase 2. Cell, 83: 493-501, 1995.
22. DuBois, R. N., Shao, J., Tsujii, M., Sheng, H., and Beauchamp, R. D. G1 delay in cells overexpressing prostaglandin endoperoxide synthase-2. Cancer Res., 56: 733-737, 1996.
23. McGinty, A., Chang, Y. W., Sorokin, A., Bokemeyer, D., and Dunn, M. J. Cyclooxygenase-2 expression inhibits trophic withdrawal apoptosis in nerve growth factor-differentiated PC12 cells. J. Biol. Chem., 275: 12095-12101, 2000.
24. Lin, M. T., Lee, R. C., Yang, P. C., Ho, F. M., and Kuo, M. L. Cyclooxygenase-2 inducing McI-1-dependent survival mechanism in human lung adenocarcinoma CL1.0 cells. Involvement of phosphatidylinositol 3-kinase/Akt pathway. J. Biol. Chem., 276: 48997-49002, 2001.
25. Nzeako, U. C., Guicciardi, M. E., Yoon, J. H., Bronk, S. F., and Gores, G. J. COX-2 inhibits Fas-mediated apoptosis in cholangiocarcinoma cells. Hepatology, 35: 552-559, 2002.
26. Liu, C. H., Chang, S. H., Narko, K., Trifan, O. C., Wu, M. T., Smith, E., Haudenschild, C., Lane, T. F., and Hla, T. Overexpression of cyclooxygenase-2 is sufficient to induce tumorigenesis in transgenic mice. J. Biol. Chem., 276: 18563-18569, 2001.
27. Muller-Decker, K., Neufang, G., Berger, I., Neumann, M., Marks, F., and Furstenberger, G. Transgenic cyclooxygenase-2 overexpression sensitizes mouse skin for carcinogenesis. Proc. Natl. Acad. Sci. USA, 99: 12483-12488, 2002.
28. Oshima, M., Dinchuk, J. E., Kargman, S. L., Oshima, H., Hancock, B., Kwong, E., Trzaskos, J. M., Evans, J. F., and Taketo, M. M. Suppression of intestinal polyposis in Apc ä716 knockout mice by inhibition of cyclooxygenase 2 (COX-2). Cell, 87: 803-809, 1996.
29. Harris, R. E., Namboodiri, K. K., and Farrar, W. B. Nonsteroidal antiinflammatory drugs and breast cancer. Epidemiology, 7: 203-205, 1996.
30. Thun, M. J., Namboodiri, M. M., Calle, E. E., Flanders, W. D., and Heath, C. W., Jr. Aspirin use and risk of fatal cancer. Cancer Res., 53: 1322-1327, 1993.
31. Ziegler, J. Cancer and arthritis share underlying processes. J. Natl. Cancer Inst., 90: 802-803, 1998.
32. Labayle, D., Fischer, D., Vielh, P., Drouhin, F., Pariente, A., Bories, C., Duhamel, O., Trousset, M., and Attali, P. Sulindac causes regression of rectal polyps in familial adenomatous polyposis. Gastroenterology, 101: 635-639, 1991.
33. Giardiello, F. M., Hamilton, S. R., Krush, A. J., Piantadosi, S., Hylind, L. M., Celano, P., Booker, S. V., Robinson, C. R., and Offerhaus, G. J. Treatment of colonic and rectal adenomas with sulindac in familial adenomatous polyposis. N. Engl. J. Med., 328: 1313-1316, 1993.
34. Nugent, K. P., Farmer, K. C., Spigelman, A. D., Williams, C. B., and Phillips, R. K. Randomized controlled trial of the effect of sulindac on duodenal and rectal polyposis and cell proliferation in patients with familial adenomatous polyposis. Br. J. Surg., 80: 1618-1619, 1993.
35. Steinbach, G., Lynch, P. M., Phillips, R. K., Wallace, M. H., Hawk, E., Gordon, G. B., Wakabayashi, N., Saunders, B., Shen, Y., Fujimura, T., Su, L. K., and Levin, B. The effect of celecoxib, a cyclooxygenase-2 inhibitor, in familial adenomatous polyposis. N. Engl. J. Med., 342: 1946-1952, 2000.
36. Wu, T., Han, C., Lunz, J. G., 3rd, Michalopoulos, G., Shelhamer, J. H., and Demetris, A. J. Involvement of 85-kd cytosolic phospholipase A(2) and cyclooxygenase-2 in the proliferation of human cholangiocarcinoma cells. Hepatology, 36: 363-373, 2002.
37. Verburg, K. M., Maziasz, T. J., Weiner, E., Loose, L., Geis, G. S., and Isakson, P. C. Cox-2-specific inhibitors: definition of a new therapeutic concept. Am. J. Ther., 8: 49-64, 2001.
38. Patrono, C., Patrignani, P., and Garcia Rodriguez, L. A. Cyclooxygenase-selective inhibition of prostanoid formation: transducing biochemical selectivity into clinical read-outs. J. Clin. Investig., 108: 7-13, 2001.
39. Rigas, B., and Shiff, S. J. Is inhibition of cyclooxygenase required for the chemopreventive effect of NSAIDs in colon cancer? A model reconciling the current contradiction. Med. Hypotheses, 54: 210-215, 2000.
40. Piazza, G. A., Alberts, D. S., Hixson, L. J., Paranka, N. S., Li, H., Finn, T., Bogert, C., Guillen, J. M., Brendel, K., Gross, P. H., Sperl, G., Ritchie, J., Burt, R. W., Ellsworth, L., Ahnen, D. J., and Pamukcu, R. Sulindac sulfone inhibits azoxymethane-induced colon carcinogenesis in rats without reducing prostaglandin levels. Cancer Res., 57: 2909-2915, 1997.
41. Piazza, G. A., Rahm, A. L., Krutzsch, M., Sperl, G., Paranka, N. S., Gross, P. H., Brendel, K., Burt, R. W., Alberts, D. S., Pamukcu, R., et al. Antineoplastic drugs sulindac sulfide and sulfone inhibit cell growth by inducing apoptosis. Cancer Res., 55: 3110-3116, 1995.
42. Lim, J. T., Piazza, G. A., Han, E. K., Delohery, T. M., Li, H., Finn, T. S., Buttyan, R., Yamamoto, H., Sperl, G. J., Brendel, K., Gross, P. H., Pamukcu, R., and Weinstein, I. B. Sulindac derivatives inhibit growth and induce apoptosis in human prostate cancer cell lines. Biochem. Pharmacol., 58: 1097-1107, 1999.
43. Hanif, R., Pittas, A., Feng, Y., Koutsos, M. I., Qiao, L., Staiano-Coico, L., Shiff, S. I., and Rigas, B. Effects of nonsteroidal anti-inflammatory drugs on proliferation and on induction of apoptosis in colon cancer cells by a prostaglandin-independent pathway. Biochem. Pharmacol., 52: 237-245, 1996.
44. Williams, C. S., Watson, A. J., Sheng, H., Helou, R., Shao, J., and DuBois, R. N. Celecoxib prevents tumor growth in vivo without toxicity to normal gut: lack of correlation between in vitro and in vivo models. Cancer Res., 60: 6045-6051, 2000.
45. Arico, S., Pattingre, S., Bauvy, C., Gane, P., Barba, A., Codogno, P., and Ogier-Denis, E. Celecoxib induces apoptosis by inhibiting 3-phosphoinositide-dependent protein kinase-1 activity in the human colon cancer HT-29 cell line. J. Biol. Chem., 277: 27613-27621, 2002.
46. Grosch, S., Tegeder, I., Niederberger, E., Brautigam, L., and Geisslinger, G. COX-2 independent induction of cell cycle arrest and apoptosis in colon cancer cells by the selective COX-2 inhibitor celecoxib. FASEB J., 15: 2742-2744, 2001.
47. Harris, R. E., Alshafie, G. A., Abou-Issa, H., and Seibert, K. Chemoprevention of breast cancer in rats by celecoxib, a cyclooxygenase 2 inhibitor. Cancer Res., 60: 2101-2103, 2000.
48. Grubbs, C. J., Lubet, R. A., Koki, A. T., Leahy, K. M., Masferrer, J. L., Steele, V. E., Kelloff, G. J., Hill, D. L., and Seibert, K. Celecoxib inhibits N-butyl-N-(4-hydroxybutyl)-nitrosamine-induced urinary bladder cancers in male B6D2F1 mice and female Fischer-344 rats. Cancer Res., 60: 5599-5602, 2000.
49. Hsu, A. L., Ching, T. T., Wang, D. S., Song, X., Rangnekar, V. M., and Chen, C. S. The cyclooxygenase-2 inhibitor celecoxib induces apoptosis by blocking Akt activation in human prostate cancer cells independently of Bcl-2. J. Biol. Chem., 275: 11397-11403, 2000.
50. Waskewich, C., Blumenthal, R. D., Li, H., Stein, R., Goldenberg, D. M., and Burton, J. Celecoxib exhibits the greatest potency amongst cyclooxygenase (COX) inhibitors for growth inhibition of COX-2-negative hematopoietic and epithelial cell lines. Cancer Res., 62: 2029-2033, 2002.
51. Oshima, M., Murai, N., Kargman, S., Arguello, M., Luk, P., Kwong, E., Taketo, M. M., and Evans, J. F. Chemoprevention of intestinal polyposis in the Apcä716 mouse by rofecoxib, a specific cyclooxygenase-2 inhibitor. Cancer Res., 61: 1733-1740, 2001.
52. Jacoby, R. F., Seibert, K., Cole, C. E., Kelloff, G., and Lubet, R. A. The cyclooxygenase-2 inhibitor celecoxib is a potent preventive and therapeutic agent in the min mouse model of adenomatous polyposis. Cancer Res., 60: 5040-5044, 2000.
53. Chinery, R., Coffey, R. J., Graves-Deal, R., Kirkland, S. C., Sanchez, S. C., Zackert, W. E., Oates, J. A., and Morrow, J. D. Prostaglandin J2 and 15-deoxy-ä12, 14-prostaglandin J2 induce proliferation of cyclooxygenase-depleted colorectal cancer cells. Cancer Res., 59: 2739-2746, 1999.
54. Miyagiwa, M., Ichida, T., Tokiwa, T., Sato, J., and Sasaki, H. A new human cholangiocellular carcinoma cell line (HuCC-TI) producing carbohydrate antigen 1919 in serum-free medium. In Vitro Cell Dev. Biol., 25: 503-510, 1989.
55. Storto, P. D., Saidman, S. L., Demetris, A. J., Letessier, E., Whiteside, T. L., and Gollin, S. M. Chromosomal breakpoints in cholangiocarcinoma cell lines. Genes Chromosomes Cancer, 2: 300-310, 1990.
56. Shimizu, Y., Demetris, A. J., Gollin, S. M., Storto, P. D., Bedford, H. M., Altarac, S., Iwatsuki, S., Herberman, R. B., and Whiteside, T. L. Two new human cholangiocarcinoma cell lines and their cytogenetics and responses to growth factors, hormones, cytokines or immunologic effector cells. Int. J. Cancer, 52: 252-260, 1992.
57. Fiorentino, M., Altimari, A., D'Errico, A., Gabusi, E., Chieco, P., Masetti, M., and Grigioni, W. F. Low p27 expression is an independent predictor of survival for patients with either hilar or peripheral intrahepatic cholangiocarcinoma. Clin. Cancer Res., 7: 3994-3999, 2001.
58. Kang, Y. K., Kim, W. H., and Jang, J. J. Expression of G1-S modulators (p53, p16, p27, cyclin Dl, Rb) and Smad4/Dpc4 in intrahepatic cholangiocarcinoma. Hum. Pathol., 33: 877-883, 2002.
59. Taguchi, K., Aishima, S., Asayama, Y., Kajiyama, K., Kinukawa, N., Shimada, M., Sugimachi, K., and Tsuneyoshi, M. The role of p27kip1 protein expression on the biological behavior of intrahepatic cholangiocarcinoma. Hepatology, 33: 1118-1123, 2001.
60. Ito, Y., Takeda, T., Sasaki, Y., Sakon, M., Yamada, T., Ishiguro, S., Imaoka, S., Tsujimoto, M., and Matsuura, N. Expression and clinical significance of the G1-S modulators in intrahepatic cholangiocellular carcinoma. Oncology, 60: 242-251, 2001.
61. Grana, X., and Reddy, E. P. Cell cycle control in mammalian cells: role of cyclins, cyclin dependent kinases (CDKs), growth suppressor genes and cyclin-dependent kinase inhibitors (CKIs). Oncogene, 11: 211-219, 1995.
62. Lees, E. Cyclin dependent kinase regulation. Curr. Opin. Cell Biol., 7: 773-780, 1995.
63. Sherr, C. J., and Roberts, J. M. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev., 13: 1501-1512, 1999.
64. Harper, J. W., Adami, G. R., Wei, N., Keyomarsi, K., and Elledge, S. J. The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell, 75: 805-816, 1993.
65. Elledge, S. J. Cell cycle checkpoints: preventing an identity crisis. Science (Wash. DC), 274: 1664-1672, 1996.
66. Paulovich, A. G., Toczyski, D. P., and Hartwell, L. H. When checkpoints fail. Cell, 88: 315-321, 1997.
67. Hung, W. C., Chang, H. C., Pan, M. R., Lee, T. H., and Chuang, L. Y. Induction of p27(KIP1) as a mechanism underlying NS398-induced growth inhibition in human lung cancer cells. Mol. Pharmacol., 58: 1398-1403, 2000.
68. Han, C., Demetris, A. J., Michalopoulos, G. K., Zhan, Q., Shelhamer, J. H., and Wu, T. PPARgamma ligands inhibit cholangiocarcinoma cell growth through p53-dependent GADD45 and p21 pathway. Hepatology, 38: 167-177, 2003.
69. Todoroki, T. Chemotherapy for bile duct carcinoma in the light of adjuvant chemotherapy, to surgery. Hepatogastroenterology, 47: 644-649, 2000.