Bryostatin-1 Stimulates the Transcription of Cyclooxygenase-2: Evidence for an Activator Protein-1-Dependent Mechanism

Clinical Cancer Research

Volumn 9, Issue 13, 2003, Pages 5036-5043

  De Lorenzo, Mariana S ^a   Yamaguchi, Kentaro ^a   Subbaramaiah, Kotha ^a   Dannenberg, Andrew J ^a,b  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b NEW YORK PRESBYTERIAN HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRYOSTATIN 1; CYCLOOXYGENASE 2; MACROLIDE; MITOGEN ACTIVATED PROTEIN KINASE; PROSTAGLANDIN; PROSTAGLANDIN E2; PROTEIN C FOS; PROTEIN C JUN; PROTEIN KINASE C; RETINOIC ACID; TRANSCRIPTION FACTOR AP 1;

ANTINEOPLASTIC ACTIVITY; ARTICLE; BRYOZOA; BUGULA NERITINA; CANCER CELL CULTURE; CONTROLLED STUDY; CYCLIC AMP RESPONSIVE ELEMENT; DOSE RESPONSE; DRUG ANTAGONISM; DRUG MECHANISM; GEL MOBILITY SHIFT ASSAY; GENE INDUCTION; HUMAN; HUMAN CELL; MACROPHAGE; MYALGIA; PAIN; PRIORITY JOURNAL; PROMOTER REGION; PROSTAGLANDIN SYNTHESIS; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ANTINEOPLASTIC AGENTS; BETA-GALACTOSIDASE; BLOTTING, NORTHERN; BLOTTING, WESTERN; CELL LINE, TUMOR; CYCLIC AMP; CYCLOOXYGENASE 2; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; ISOENZYMES; LACTONES; MACROLIDES; MACROPHAGES; MEMBRANE PROTEINS; MODELS, CHEMICAL; MODELS, GENETIC; PLASMIDS; PROMOTER REGIONS (GENETICS); PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; PROTEIN BINDING; PROTEIN KINASE C; RNA, MESSENGER; TIME FACTORS; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTION, GENETIC; TRANSFECTION; TRETINOIN;

EID: 0142188127     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (61)

1. Smith, W. L., Garavito, R. M., and DeWitt, D. L. Prostaglandin endoperoxide H synthases (cyclooxygenases)-1 and -2. J. Biol. Chem., 271: 33157-33160, 1996.
2. Kujubu, D. A., Fletcher, B. S., Varnum, B. C., Lim, R. W., and Herschman, H. R. TIS10, a phorbol ester tumor promoter-inducible mRNA from Swiss 3T3 cells, encodes a novel prostaglandin synthase/cyclooxygenase homologue. J. Biol. Chem., 266: 12866-12872, 1991.
3. Jones, D. A., Carlton, D. P., McIntyre, T. M., Zimmerman, G. A., and Prescott, S. M. Molecular cloning of human prostaglandin endoperoxide synthase type II and demonstration of expression in response to cytokines. J. Biol. Chem., 268: 9049-9054, 1993.
4. DuBois, R. N., Awad, J., Morrow, J., Roberts, L. J., and Bishop, P. R. Regulation of eicosanoid production and mitogenesis in rat intestinal epithelial cells by transforming growth factor α and phorbol ester. J. Clin. Investig., 93: 493-498, 1994.
5. Inoue, H., Yokoyama, C., Hara, S., Tone, Y., and Tanabe, T. Transcriptional regulation of human prostaglandin-endoperoxide synthase-2 gene by lipopolysaccharide and phorbol ester in vascular endothelial cells. Involvement of both nuclear factor for interleukin-6 expression site and cAMP response element. J. Biol. Chem., 270: 24965-24971, 1995.
6. Simmons, D. L., Levy, D. B., Yannoni, Y., and Erikson, R. L. Identification of a phorbol ester-repressible v-src-inducible gene. Proc. Natl. Acad. Sci. USA, 86: 1178-1182, 1989.
7. Subbaramaiah, K., Telang, N., Ramonetti, J. T., Araki, R., DeVito, B., Weksler, B. B., and Dannenberg, A. J. Transcription of cyclooxygenase-2 is enhanced in transformed mammary epithelial cells. Cancer Res., 56: 4424-4429, 1996.
8. Mestre, J. R., Subbaramaiah, K., Sacks, P. G., Schantz, S. P., Tanabe, T., Inoue, H., and Dannenberg, A. J. Retinoids suppress epidermal growth factor-induced transcription of cyclooxygenase-2 in human oral squamous carcinoma cells. Cancer Res., 57: 2890-2895, 1997.
9. Anderson, G. D., Hauser, S. D., McGarity, K. L., Bremer, M. E., Isakson, P. C., and Gregory, S. A. Selective inhibition of cyclooxygenase (COX)-2 reverses inflammation and expression of COX-2 and interleukin 6 in rat adjuvant arthritis. J. Clin. Investig., 97: 2672-2679, 1996.
10. Lipsky, P. E., and Isakson, P. C. Outcome of specific COX-2 inhibition in rheumatoid arthritis. J. Rheumatol., 49: 9-14, 1997.
11. Sabino, M. A., Ghilardi, J. R., Jongen, J. L. M., Keyser, C. P., Luger, N. M., Mach, D. B., Peters, C. M., Rogers, S. D., Schwei, M. J., de Felipe, C., and Mantyh, P. W. Simultaneous reduction in cancer pain, bone destruction, and tumor growth by selective inhibition of cyclooxygenase-2. Cancer Res., 62: 7343-7349, 2002.
12. Subbaramaiah, K., and Dannenberg, A. J. Cyclooxygenase 2: a molecular target for cancer prevention and treatment. Trends. Pharmacol. Sci., 24: 96-102, 2003.
13. Crofford, L. J., Wilder, R. L., Ristimaki, A. P., Sano, H., Remmers, E. F., Epps, H. R., and Hla, T. Cyclooxygenase-1 and -2 expression in rheumatoid synovial tissues. Effects of interleukin-1β, phorbol ester, and corticosteroids. J. Clin. Investig., 93: 1095-1101, 1994.
14. Samad, T. A., Moore, K. A., Sapirstein, A., Billet, S., Allchorne, A., Poole, S., Bonventre, J. V., and Woolf, C. J. Interleukin-1β-mediated induction of Cox-2 in the CNS contributes to inflammatory pain hypersensitivity. Nature (Lond.), 410: 471-475, 2001.
15. Eberhart, C. E., Coffey, R. J., Radhika, A., Giardiello, F. M., Ferrenbach, S., and DuBois, R. N. Up-regulation of cyclooxygenase 2 gene expression in human colorectal adenomas and adenocarcinomas. Gastroenterology, 107: 1183-1188, 1994.
16. Ristimaki, A., Honkanen, N., Jankala, H., Sipponen, P., and Harkonen, M. Expression of cyclooxygenase-2 in human gastric carcinoma. Cancer Res., 57: 1276-1280, 1997.
17. Parrett, M. L., Harris, R. E., Joarder, F. S., Ross, M. S., Clausen, K. P., and Robertson, F. M. Cyclooxygenase-2 expression in human breast cancer. Int. J. Oncol., 10: 503-507, 1997.
18. Chan, G., Boyle, J. O., Yang, E. K., Zhang, F., Sacks, P. G., Shah, J. P., Edelstein, D., Soslow, R. A., Koki, A. T., Woerner, B. M., Masferrer, J. L., and Dannenberg, A. J. Cyclooxygenase-2 expression is up-regulated in squamous cell carcinoma of the head and neck. Cancer Res., 59: 991-994, 1999.
19. Tucker, O. N., Dannenberg, A. J., Yang, E. K., Zhang, F., Teng, L., Daly, J. M., Soslow, R. A., Masferrer, J. L., Woerner, B. M., Koki, A. T., and Fahey, T. J. Cyclooxygenase-2 expression is up-regulated in human pancreatic cancer. Cancer Res., 59: 987-990, 1999.
20. Kulkarni, S., Rader, J. S., Zhang, F., Liapis, H., Koki, A. T., Masferrer, J. L., Subbaramaiah, K., and Dannenberg, A. J. Cyclooxygenase-2 is overexpressed in human cervical cancer. Clin. Cancer Res., 7: 429-434, 2001.
21. 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.
22. Δ716 knockout mice by inhibition of cyclooxygenase 2 (COX-2). Cell, 87: 803-809, 1996.
23. Tiano, H. F., Loftin, C. D., Akunda, J., Lee, C. A., Spalding, J., Sessoms, A., Dunson, D. B., Rogan, E. G., Morham, S. G., Smart, R. C., and Langenbach, R. Deficiency of either cyclooxygenase(COX)-1 or COX-2 alters epidermal differentiation and reduces mouse skin tumorigenesis. Cancer Res., 62: 3395-3401, 2002.
24. Kawamori, T., Rao, C. V., Seibert, K., and Reddy, B. S. Chemopreventive activity of celecoxib, a specific cyclooxygenase-2 inhibitor, against colon carcinogenesis. Cancer Res., 58: 409-412, 1998.
25. Fischer, S. M., Lo H-H., Gordon, G. B., Seibert, K., Kelloff, G., Lubet, R. A., and Conti, C. C. Chemopreventive activity of celecoxib, a specific cyclooxygenase-2 inhibitor, and indomethacin against ultravioler light-induced skin carcinogenesis. Mol. Carcinog., 25: 231-240, 1999.
26. Sheng, H., Shao, J., Kirkland, S. C., Isakson, P., Coffey, R. J., Morrow, J., Beauchamp, R. D., and DuBois, R. N. Inhibition of human colon cancer cell growth by selective inhibition of cyclooxygenase-2. J. Clin. Investig., 99: 2254-2259, 1997.
27. Sawaoka, H., Kawano, S., Tsuji, S., Tsujii, M., Gunawan, E. S., Takei, Y., Nagano, K., and Hori, M. Cyclooxygenase-2 inhibitors suppress the growth of gastric cancer xenografts via induction of apoptosis in nude mice. Am. J. Physiol., 274: G1061-G1067, 1998.
28. 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.
29. Steinbach, G., Lynch, P. M., Phillips, R. K. S., 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.
30. 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.
31. 2 in human colon cancer cells. Cancer Res., 58: 362-366, 1998.
32. 2 increases growth and motility of colorectal carcinoma cells. J. Biol. Chem., 276: 18075-18081, 2001.
33. Ben-Av, P., Crofford, L. J., Wilder, R. L., and Hla, T. Induction of vascular endothelial growth factor expression in synovial fibroblasts by prostaglandin E and interleukin-1: a potential mechanism for inflammatory angiogenesis. FEBS Lett., 372: 83-87, 1995.
34. Tsujii, M., Kawano, S., Tsuji, S., Sawaoka, H., Hori, M., and DuBois, R. N. Cyclooxygenase regulates angiogenesis induced by colon cancer cells. Cell, 93: 705-716, 1998.
35. Tsujii, M., Kawano, S., and DuBois, R. N. Cyclooxygenase-2 expression in human colon cancer cells increases metastatic potential. Proc. Natl. Acad. Sci. USA, 94: 3336-3340, 1997.
36. Dohadwala, M., Luo, J., Zhu, L., Lin, Y., Dougherty, G. J., Sharma, S., Huang, M., Pold, M., Batra, R. K., and Dubinett, S. M. Non-small cell lung cancer cyclooxygenase-2-dependent invasion is mediated by CD44. J. Biol. Chem., 276: 20809-20812, 2001.
37. Pettit, G. R., Herald, C. L., Doubek, D. L., Herald, D. L., Arnold, E., and Clardy, J. Isolation and structure of bryostatin-1. J. Am. Chem. Soc., 104: 6846-6848, 1982.
38. Pettit, G. R., Herald, C. L., and Hogan, F. Biosynthetic products for anticancer drug design and treatment: the bryostatins. In: B. C. Baguley and D. J. Kerr (eds.), Anticancer Drug Development, pp. 203-235. New York: Academic Press, 2001.
39. Hornung, R. L., Pearson, J. W., Beckwith, M., and Longo, D. L. Preclinical evaluation of bryostatin as an anticancer agent against several murine tumor cell lines: in vitro versus in vivo activity. Cancer Res., 52: 101-107, 1992.
40. Schuchter, L. M., Esa, A. H., May, S., Laulis, M. K., Pettit, G. R., and Hess, A. D. Successful treatment of murine melanoma with bryostatin-1. Cancer Res., 51: 682-687, 1991.
41. Mohammad, R. M., Al-Katib, A., Pettit, G. R., and Sensenbrenner, L. L. Successful treatment of human Waldenstrom's macroglobulinemia with combination biological and chemotherapy agents. Cancer Res., 54: 165-168, 1994.
42. Mohammad, R. M., Wall, N. R., Dutcher, J. A., and Al-Katib, A. M. The addition of bryostatin 1 to cyclophosphamide, doxorubicin, vincristine and prednisone (CHOP) chemotherapy improves response in a CHOP-resistant human diffuse large cell lymphoma xenograft model. Clin. Cancer Res., 6: 4950-4956, 2000.
43. Clamp, A., and Jayson, G. C. The clinical development of the bryostatins. Anticancer Drugs, 13: 673-683, 2002.
44. Prendiville, J., Crowther, D., Thatcher, N., Woll, P. J., Fox, B. W., McGown, A., Testa, N., Stern, P., McDermott, R., Potter, M., and Pettit, G. R. A Phase I study of intravenous bryostatin 1 in patients with advanced cancer. Br. J. Cancer, 68: 418-424, 1993.
45. Kraft, A. S., Smith, J. B., and Berkow, R. L. Bryostatin, an activator of the calcium phospholipid-dependent protein kinase, blocks phorbol ester-induced differentiation of human promyelocytic leukemia cells HL-60. Proc. Natl. Acad. Sci. USA, 83: 1334-1338, 1986.
46. 4 pituitary cells. J. Biol. Chem., 261: 17073-17080, 1986.
47. Shimada, Y., Imamura, M., Wagata, T., Yamaguchi, N., and Tobe, T. Characterization of 21 newly established esophageal cancer cell lines. Cancer (Phila.), 69: 277-284, 1992.
48. Sacks, P. G., Parnes, S. M., Gallick, G. E., Mansouri, Z., Lichtner, R., Satya-Prakash, K. L., Pathak, S., and Parsons, D. F. Establishment and characterization of two new squamous cell carcinoma cell lines derived from tumors of the head and neck. Cancer Res., 48: 2858-2866, 1988.
49. Yoshimatsu, K., Altorki, N. K., Golijanin, D., Zhang, F., Jakobsson, P-J., Dannenberg, A. J., and Subbaramaiah, K. Inducible prostaglandin E synthase is overexpressed in non-small cell lung cancer. Clin. Cancer Res., 7: 2669-2674, 2001.
50. Fujita, J., Mestre, J. R., Zeldis, J. B., Subbaramaiah, K., and Dannenberg, A. J. Thalidomide and its analogues inhibit lipopolysaccharide-mediated induction of cyclooxygenase-2. Clin. Cancer Res., 7: 3349-3355, 2001.
51. Denizot, F., and Lang, R. Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J. Immunol. Methods, 89: 271-277, 1986.
52. Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randell, R. J. Protein measurement with the Folin phenol reagent. J. Biol. Chem., 193: 265-275, 1951.
53. Laemmli, U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (Lond.), 227: 680-685, 1970.
54. Towbin, H., Staehelin, T., and Gordon, J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA, 76: 4350-4354, 1979.
55. Subbaramaiah, K., Chung, W. J., and Dannenberg, A. J. Ceramide regulates the transcription of cyclooxygenase-2. Evidence for involvement of extracellular signal-regulated kinase/c-Jun N-terminal kinase and p38 mitogen-activated protein kinase pathways. J. Biol. Chem., 273: 32943-32949, 1998.
56. Mestre, J. R., Subbaramaiah, K., Sacks, P. G., Schantz, S. P., Tanabe, T., Inoue, H., and Dannenberg, A. J. Retinoids suppress phorbol ester-mediated induction of cyclooxygenase-2. Cancer Res., 57: 1081-1085, 1997.
57. Subbaramaiah, K., Cole, P. A., and Dannenberg, A. J. Retinoids and carnosol suppress cyclooxygenase-2 transcription by CREB-binding protein/p300-dependent and -independent mechanisms. Cancer Res., 62: 2522-2530, 2002.
58. Zhang, F., Subbaramaiah, K., Altorki, N., and Dannenberg, A. J. Dihydroxy bile acids activate the transcription of cyclooxygenase-2. J. Biol. Chem., 273: 2424-2428, 1998.
59. Subbaramaiah, K., Hart, J. C., Norton, L., and Dannenberg, A. J. Microtubule-interfering agents stimulate the transcription of cyclooxygenase-2. J. Biol. Chem., 275: 14838-14845, 2000.
60. Kralova, J., Liss, A. S., Bargmann, W., and Bose, H. R. AP-1 factors play an important role in transformation induced by the v-rel oncogene. Mol. Cell. Biol., 18: 2997-3009, 1998.
61. Young, M. R., Li, J. J., Rincon, M., Flavell, R. A., Sathyanarayana, B. K., Hunziker, R., and Colburn, N. Transgenic mice demonstrate AP-1 (activator protein-1) transactivation is required for tumor promotion. Proc. Natl. Acad. Sci. USA, 96: 9827-9832, 1999.