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Transcription of Cyclooxygenase-2 Is Enhanced in Transformed Mammary Epithelial Cells¹

Department of Medicine, Cornell University Medical College [K. S., J. T. R., B. D., B. B. W., A. J. D.] and Strang Cancer Prevention Center [K. S., N. T., J. T. R., R. A., A. J. D.], New York, New York 10021

Cancers form more prostaglandins than the normal tissues from which they arise. Cyclooxygenase-2 (prostaglandin H synthase-2, PGHS-2, EC 1.14.99.1), an enzyme that catalyzes the formation of prostaglandins from arachidonic acid, is inducible in epithelial cells. We investigated whether transformation of mammary cells was associated with up-regulation of Cox-2 as a basis for increased production of prostaglandin E₂ (PGE₂) by these cells. This hypothesis was tested in two pairs of mammary cell lines between which the mode of transformation (viral versus oncogene) differed. Virally transformed RIII/Pr1 cells, which are highly tumorigenic in mice, produced markedly increased amounts of PGE₂ compared to virally initiated RIII/MG cells, a weakly tumorigenic strain. Cox-2 mRNA and protein were increased concomitantly in RIII/Pr1 cells. Similarly, Ras-induced transformation of C57/MG cells resulted in increased levels of Cox-2 mRNA and protein and increased production of PGE₂. Nuclear run-offs revealed increased rates of Cox-2 transcription in the virally transformed and oncogene-transformed cell lines. Transient transfection experiments demonstrated that the oncogenes src and ras up-regulated Cox-2 promoter activity. Src-mediated up-regulation of Cox-2 promoter activity was suppressed by dominant negative ras. Our data indicate that cellular transformation is associated with enhanced transcription of Cox-2 and increased production of PGE₂.

¹ This work was supported by Department of Army Grant DAMD 17-94-J4208 (to N. T.), NIH Grants CA68136 (to A. J. D.) and PO1CA29502 (to N. T.), and a NIH SCOR in Thrombosis HL 18828 (to B. B. W.).

² To whom requests for reprints should be addressed, at Division of Digestive Diseases, Room F-231, The New York Hospital-Cornell Medical Center, New York, NY 10021.

Received 4/29/96. Accepted 8/ 1/96.

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				A.-L. Hsu, T.-T. Ching, D.-S. Wang, X. Song, V. M. Rangnekar, and C.-S. Chen The Cyclooxygenase-2 Inhibitor Celecoxib Induces Apoptosis by Blocking Akt Activation in Human Prostate Cancer Cells Independently of Bcl-2 J. Biol. Chem., April 6, 2000; 275(15): 11397 - 11403. [Abstract] [Full Text] [PDF]

				M. B. Sporn and N. Suh Chemoprevention of cancer Carcinogenesis, March 1, 2000; 21(3): 525 - 530. [Abstract] [Full Text] [PDF]

				H. Sheng, J. Shao, D. A. Dixon, C. S. Williams, S. M. Prescott, R. N. DuBois, and R. D. Beauchamp Transforming Growth Factor-beta 1 Enhances Ha-ras-induced Expression of Cyclooxygenase-2 in Intestinal Epithelial Cells via Stabilization of mRNA J. Biol. Chem., February 25, 2000; 275(9): 6628 - 6635. [Abstract] [Full Text] [PDF]

				Z. Yan, K. Subbaramaiah, T. Camilli, F. Zhang, T. Tanabe, T. A. McCaffrey, A. J. Dannenberg, and B. B. Weksler Benzo[a]pyrene Induces the Transcription of Cyclooxygenase-2 in Vascular Smooth Muscle Cells. EVIDENCE FOR THE INVOLVEMENT OF EXTRACELLULAR SIGNAL-REGULATED KINASE AND NF-kappa B J. Biol. Chem., February 18, 2000; 275(7): 4949 - 4955. [Abstract] [Full Text] [PDF]

				M. T. Yip-Schneider, D. S. Barnard, S. D. Billings, L. Cheng, D. K. Heilman, A. Lin, S. J. Marshall, P. L. Crowell, M. S. Marshall, and C. J. Sweeney Cyclooxygenase-2 expression in human pancreatic adenocarcinomas Carcinogenesis, February 1, 2000; 21(2): 139 - 146. [Abstract] [Full Text] [PDF]

				C.-J. Yuan, A. K. Mandal, Z. Zhang, and A. B. Mukherjee Transcriptional Regulation of Cyclooxygenase-2 Gene Expression: Novel Effects of Nonsteroidal Anti-Inflammatory Drugs Cancer Res., February 1, 2000; 60(4): 1084 - 1091. [Abstract] [Full Text]

				D. Wolfle, S. Marotzki, D. Dartsch, W. Schafer, and H. Marquardt Induction of cyclooxygenase expression and enhancement of malignant cell transformation by 2,3,7,8-tetrachlorodibenzo- p-dioxin Carcinogenesis, January 1, 2000; 21(1): 15 - 21. [Abstract] [Full Text] [PDF]

				H. Matsuura, M. Sakaue, K. Subbaramaiah, H. Kamitani, T. E. Eling, A. J. Dannenberg, T. Tanabe, H. Inoue, J. Arata, and A. M. Jetten Regulation of Cyclooxygenase-2 by Interferon gamma and Transforming Growth Factor alpha in Normal Human Epidermal Keratinocytes and Squamous Carcinoma Cells. ROLE OF MITOGEN-ACTIVATED PROTEIN KINASES J. Biol. Chem., October 8, 1999; 274(41): 29138 - 29148. [Abstract] [Full Text] [PDF]

				L. W. Slice, J. H. Walsh, and E. Rozengurt Galpha 13 Stimulates Rho-dependent Activation of the Cyclooxygenase-2 Promoter J. Biol. Chem., September 24, 1999; 274(39): 27562 - 27566. [Abstract] [Full Text] [PDF]

				P. Michaluart, J. L. Masferrer, A. M. Carothers, K. Subbaramaiah, B. S. Zweifel, C. Koboldt, J. R. Mestre, D. Grunberger, P. G. Sacks, T. Tanabe, et al. Inhibitory Effects of Caffeic Acid Phenethyl Ester on the Activity and Expression of Cyclooxygenase-2 in Human Oral Epithelial Cells and in a Rat Model of Inflammation Cancer Res., May 1, 1999; 59(10): 2347 - 2352. [Abstract] [Full Text] [PDF]

				H. Achiwa, Y. Yatabe, T. Hida, T. Kuroishi, K.-i. Kozaki, S. Nakamura, M. Ogawa, T. Sugiura, T. Mitsudomi, and T. Takahashir Prognostic Significance of Elevated Cyclooxygenase 2 Expression in Primary, Resected Lung Adenocarcinomas Clin. Cancer Res., May 1, 1999; 5(5): 1001 - 1005. [Abstract] [Full Text] [PDF]

				K. Subbaramaiah, N. Altorki, W. J. Chung, J. R. Mestre, A. Sampat, and A. J. Dannenberg Inhibition of Cyclooxygenase-2 Gene Expression by p53 J. Biol. Chem., April 16, 1999; 274(16): 10911 - 10915. [Abstract] [Full Text] [PDF]

				O. N. Tucker, A. J. Dannenberg, E. K. Yang, F. Zhang, L. Teng, J. M. Daly, R. A. Soslow, J. L. Masferrer, B. M. Woerner, A. T. Koki, et al. Cyclooxygenase-2 Expression Is Up-Regulated in Human Pancreatic Cancer Cancer Res., March 1, 1999; 59(5): 987 - 990. [Abstract] [Full Text] [PDF]

				G. Chan, J. O. Boyle, E. K. Yang, F. Zhang, P. G. Sacks, J. P. Shah, D. Edelstein, R. A. Soslow, A. T. Koki, B. M. Woerner, et al. Cyclooxygenase-2 Expression Is Up-Regulated in Squamous Cell Carcinoma of the Head and Neck Cancer Res., March 1, 1999; 59(5): 991 - 994. [Abstract] [Full Text] [PDF]

				F. Zhang, N. K. Altorki, J. R. Mestre, K. Subbaramaiah, and A. J. Dannenberg Curcumin inhibits cyclooxygenase-2 transcription in bile acid- and phorbol ester-treated human gastrointestinal epithelial cells Carcinogenesis, March 1, 1999; 20(3): 445 - 451. [Abstract] [Full Text] [PDF]

				K. Subbaramaiah, W. J. Chung, and A. J. Dannenberg 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., December 4, 1998; 273(49): 32943 - 32949. [Abstract] [Full Text] [PDF]

				Y. Kim and S. M. Fischer Transcriptional Regulation of Cyclooxygenase-2 in Mouse Skin Carcinoma Cells. REGULATORY ROLE OF CCAAT/ENHANCER-BINDING PROTEINS IN THE DIFFERENTIAL EXPRESSION OF CYCLOOXYGENASE-2 IN NORMAL AND NEOPLASTIC TISSUES J. Biol. Chem., October 16, 1998; 273(42): 27686 - 27694. [Abstract] [Full Text] [PDF]

				K. Subbaramaiah, W. J. Chung, P. Michaluart, N. Telang, T. Tanabe, H. Inoue, M. Jang, J. M. Pezzuto, and A. J. Dannenberg Resveratrol Inhibits Cyclooxygenase-2 Transcription and Activity in Phorbol Ester-treated Human Mammary Epithelial Cells J. Biol. Chem., August 21, 1998; 273(34): 21875 - 21882. [Abstract] [Full Text] [PDF]

				H. Sheng, C. S. Williams, J. Shao, P. Liang, R. N. DuBois, and R. D. Beauchamp Induction of Cyclooxygenase-2 by Activated Ha-ras Oncogene in Rat-1 Fibroblasts and the Role of Mitogen-activated Protein Kinase Pathway J. Biol. Chem., August 21, 1998; 273(34): 22120 - 22127. [Abstract] [Full Text] [PDF]

				F. Zhang, K. Subbaramaiah, N. Altorki, and A. J. Dannenberg Dihydroxy Bile Acids Activate the Transcription of Cyclooxygenase-2 J. Biol. Chem., January 23, 1998; 273(4): 2424 - 2428. [Abstract] [Full Text] [PDF]

				B. J. Ledwith, C. J. Pauley, L. K. Wagner, C. L. Rokos, D. W. Alberts, and S. Manam Induction of Cyclooxygenase-2 Expression by Peroxisome Proliferators and Non-tetradecanoylphorbol 12,13-Myristate-type Tumor Promoters in Immortalized Mouse Liver Cells J. Biol. Chem., February 7, 1997; 272(6): 3707 - 3714. [Abstract] [Full Text] [PDF]

				J. Shao, H. Sheng, R. N. DuBois, and R. D. Beauchamp Oncogenic Ras-mediated Cell Growth Arrest and Apoptosis are Associated with Increased Ubiquitin-dependent Cyclin D1 Degradation J. Biol. Chem., July 21, 2000; 275(30): 22916 - 22924. [Abstract] [Full Text] [PDF]

				J. Shao, H. Sheng, H. Inoue, J. D. Morrow, and R. N. DuBois Regulation of Constitutive Cyclooxygenase-2 Expression in Colon Carcinoma Cells J. Biol. Chem., October 20, 2000; 275(43): 33951 - 33956. [Abstract] [Full Text] [PDF]