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[Cancer Research 55, 1464-1472, April 1, 1995]
© 1995 American Association for Cancer Research

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Chemoprevention of Colon Carcinogenesis by Sulindac, a Nonsteroidal Anti-inflammatory Agent1

Chinthalapally V. Rao, Abraham Rivenson, Barbara Simi, Edith Zang, Gary Kelloff, Vernon Steele and Bandaru S. Reddy2

Divisions of Nutritional Carcinogenesis [C. V. R., B. S., B. S. R.], Pathology and Toxicology [A. R.], and Epidemiology [E. Z.], American Health Foundation, Valhalla, New York 10595, and Chemoprevention Branch, Division of Cancer Control and Prevention, National Cancer Institute, Bethesda, Maryland 20892 [G. K., V. S.]

Epidemiological and laboratory animal model studies have suggested that nonsteroidal anti-inflammatory drugs reduce the risk of development of colon cancer. The present study was designed to investigate the chemopreventive action of 160 and 320 ppm (equivalent to 40 and 80% maximum tolerated doses) sulindac, a nonsteroidal anti-inflammatory drug, fed during initiation and postinitiation stages and 320 ppm sulindac fed during promotion/progression stages of azoxymethane-induced colon carcinogenesis in male F344 rats. Also investigated was the modulating effect of this agent on the colonic mucosal and tumor phospholipase A2, phosphatidylinositol-specific phospholipase C, lipoxygenase, and cyclooxygenase activities. At 5 weeks of age, groups of male F344 rats were fed control diet or diets containing 160 and 320 ppm of sulindac. At 7 weeks of age, all animals except those in the vehicle-treated groups were given two weekly s.c. injections of azoxymethane at a dose rate of 15 mg/kg body weight/week. Animals intended for tumor promotion/progression study were administered 320 ppm of sulindac in diet starting at 14 weeks after a second azoxymethane treatment. All animals continued on their respective dietary regimen until the termination of the experiment at 52 weeks after the carcinogen treatment. Colonic tumors were evaluated histopathologically. Colonic mucosa and tumors were analyzed for phospholipase A2, phosphatidylinositol-specific phospholipase C, prostaglandin E2, cyclooxygenase, and lipoxygenase activities. The levels of sulindac and its metabolites in stomach, cecal, and fecal contents and in serum were analyzed. The results indicate that dietary sulindac at 160 and 320 ppm levels inhibited the incidence of invasive and nonivasive adenocarcinomas of the colon (P < 0.01–0.001) as well as their multiplicity (P < 0.01–0.0001) in a dose-dependent manner. Also, feeding sulindac during promotion/progression stages significantly suppressed the incidence (P < 0.0001) and multiplicity (P < 0.0001) of colonic adenocarcinomas. Dietary sulindac also suppressed the colon tumor volume by >52–62% compared to the control diet. Dietary sulindac significantly decreased the activities of phosphatidylinositol-specific phospholipase C (32–51%) and levels of prostaglandin E2 (>40%) in the colonic mucosa and tumors, but it had no significant (P > 0.05) effect on phospholipase A2 activity. The formation of cyclooxygenase metabolites, particularly prostaglandin E2, prostaglandin F2{alpha}, prostaglandin D2, 6-ketoprostaglandin F1{alpha}, and thromboxane B2, and lipoxygenase metabolites such as 8(S)- and 12(S)-hydroxyeicosatetraenoic acids were significantly reduced in colonic mucosa and tumors of animals fed 320 ppm sulindac. Also, animals fed 320 ppm sulindac showed increased levels of microbial metabolites of sulindac in cecal and fecal contents and in serum as compared to those fed 160 ppm sulindac. Although the exact mechanism by which sulindac inhibits colon tumorigenesis remains to be elucidated, it is likely that its chemopreventive action, at least in part, may be related to the modulation of arachidonic acid metabolism.

1 Supported by USPHS Grants CN85095-05 and CA17613 awarded by the National Cancer Institute.

2 To whom requests for reprints should be addressed.

Received 11/21/94. Accepted 2/ 2/95.




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CarcinogenesisHome page
C. V. Rao, I. Cooma, J. G.R. Rodriguez, B. Simi, K. El-Bayoumy, and B. S. Reddy
Chemoprevention of familial adenomatous polyposis development in the APCmin mouse model by 1,4-phenylene bis(methylene)selenocyanate
Carcinogenesis, April 1, 2000; 21(4): 617 - 621.
[Abstract] [Full Text] [PDF]


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FASEB J.Home page
R. ZEIDLER, M. CSANADY, O. GIRES, S. LANG, B. SCHMITT, and B. WOLLENBERG
Tumor cell-derived prostaglandin E2 inhibits monocyte function by interfering with CCR5 and Mac-1
FASEB J, April 1, 2000; 14(5): 661 - 668.
[Abstract] [Full Text]


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Cancer Res.Home page
R. F. Jacoby, C. E. Cole, K. Tutsch, M. A. Newton, G. Kelloff, E. T. Hawk, and R. A. Lubet
Chemopreventive Efficacy of Combined Piroxicam and Difluoromethylornithine Treatment of Apc Mutant Min Mouse Adenomas, and Selective Toxicity against Apc Mutant Embryos
Cancer Res., April 1, 2000; 60(7): 1864 - 1870.
[Abstract] [Full Text]


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Cancer Res.Home page
M. A. Rahman, D. K. Dhar, R. Masunaga, A. Yamanoi, H. Kohno, and N. Nagasue
Sulindac and Exisulind Exhibit a Significant Antiproliferative Effect and Induce Apoptosis in Human Hepatocellular Carcinoma Cell Lines
Cancer Res., April 1, 2000; 60(8): 2085 - 2089.
[Abstract] [Full Text]


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ChestHome page
P. A. Bunn Jr., A. Soriano, G. Johnson, and L. Heasley
New Therapeutic Strategies for Lung Cancer : Biology and Molecular Biology Come of Age
Chest, April 1, 2000; 117 (2009): 163S - 168S.
[Abstract] [Full Text] [PDF]


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Cancer Epidemiol. Biomarkers Prev.Home page
B. S. Reddy
Novel Approaches to the Prevention of Colon Cancer by Nutritional Manipulation and Chemoprevention
Cancer Epidemiol. Biomarkers Prev., March 1, 2000; 9(3): 239 - 247.
[Abstract] [Full Text]


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J. Biol. Chem.Home page
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]


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Am. J. Physiol. Gastrointest. Liver Physiol.Home page
T. A. de Jong, S. A. Skinner, C. Malcontenti-Wilson, D. Vogiagis, M. Bailey, I. R. van Driel, and P. E. O'Brien
Inhibition of rat colon tumors by sulindac and sulindac sulfone is independent of K-ras (codon 12) mutation
Am J Physiol Gastrointest Liver Physiol, February 1, 2000; 278(2): G266 - G272.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
B. S. Reddy, Y. Hirose, R. Lubet, V. Steele, G. Kelloff, S. Paulson, K. Seibert, and C. V. Rao
Chemoprevention of Colon Cancer by Specific Cyclooxygenase-2 Inhibitor, Celecoxib, Administered during Different Stages of Carcinogenesis
Cancer Res., January 1, 2000; 60(2): 293 - 297.
[Abstract] [Full Text]


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GutHome page
J J Keller, G J A Offerhaus, M Polak, S N Goodman, M L Zahurak, L M Hylind, S R Hamilton, and F M Giardiello
Rectal epithelial apoptosis in familial adenomatous polyposis patients treated with sulindac
Gut, December 1, 1999; 45(6): 822 - 828.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
K. Watanabe, T. Kawamori, S. Nakatsugi, T. Ohta, S. Ohuchida, H. Yamamoto, T. Maruyama, K. Kondo, F. Ushikubi, S. Narumiya, et al.
Role of the Prostaglandin E Receptor Subtype EP1 in Colon Carcinogenesis
Cancer Res., October 1, 1999; 59(20): 5093 - 5096.
[Abstract] [Full Text] [PDF]


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CarcinogenesisHome page
A. P. Pentland, J. W. Schoggins, G. A. Scott, K. N. M. Khan, and R. Han
Reduction of UV-induced skin tumors in hairless mice by selective COX-2 inhibition
Carcinogenesis, October 1, 1999; 20(10): 1939 - 1944.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
Y. Yamamoto, M.-J. Yin, K.-M. Lin, and R. B. Gaynor
Sulindac Inhibits Activation of the NF-kappa B Pathway
J. Biol. Chem., September 17, 1999; 274(38): 27307 - 27314.
[Abstract] [Full Text] [PDF]


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CarcinogenesisHome page
B. S. Reddy, T. Kawamori, R. Lubet, V. Steele, G. Kelloff, and C. V. Rao
Chemopreventive effect of S-methylmethane thiosulfonate and sulindac administered together during the promotion/progression stages of colon carcinogenesis
Carcinogenesis, August 1, 1999; 20(8): 1645 - 1648.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
B. S. Reddy, T. Kawamori, R. A. Lubet, V. E. Steele, G. J. Kelloff, and C. V. Rao
Chemopreventive Efficacy of Sulindac Sulfone against Colon Cancer Depends on Time of Administration during Carcinogenic Process
Cancer Res., July 1, 1999; 59(14): 3387 - 3391.
[Abstract] [Full Text] [PDF]


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Clin. Cancer Res.Home page
S. R. Ritland, J. A. Leighton, R. E. Hirsch, J. D. Morrow, A. L. Weaver, and S. J. Gendler
Evaluation of 5-Aminosalicylic Acid (5-ASA) for Cancer Chemoprevention: Lack of Efficacy against Nascent Adenomatous Polyps in the ApcMin Mouse
Clin. Cancer Res., April 1, 1999; 5(4): 855 - 863.
[Abstract] [Full Text] [PDF]


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CarcinogenesisHome page
H. Li, H. A.J. Schut, P. Conran, P. M. Kramer, R. A. Lubet, V. E. Steele, E. E. Hawk, G. J. Kelloff, and M. A. Pereira
Prevention by aspirin and its combination with {alpha}-difluoromethylornithine of azoxymethane-induced tumors, aberrant crypt foci and prostaglandin E2 levels in rat colon
Carcinogenesis, March 1, 1999; 20(3): 425 - 430.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
T. Kawamori, R. Lubet, V. E. Steele, G. J. Kelloff, R. B. Kaskey, and C. V. Rao
Chemopreventive Effect of Curcumin, a Naturally Occurring Anti-Inflammatory Agent, during the Promotion/Progression Stages of Colon Cancer
Cancer Res., February 1, 1999; 59(3): 597 - 601.
[Abstract] [Full Text] [PDF]


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ADRHome page
B.L. Lokeshwar, H.L. Houston-Clark, M.G. Selzer, N.L. Block, and L.M. Golub
Potential Application of a Chemically Modified Non-Antimicrobial Tetracycline (CMT-3) Against Metastatic Prostate Cancer
Advances in Dental Research, November 1, 1998; 12(1): 97 - 102.
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J. Biol. Chem.Home page
Z. Guan, S. Y. Buckman, A. P. Pentland, D. J. Templeton, and A. R. Morrison
Induction of Cyclooxygenase-2 by the Activated MEKK1 right-arrow SEK1/MKK4 right-arrow p38 Mitogen-activated Protein Kinase Pathway
J. Biol. Chem., May 22, 1998; 273(21): 12901 - 12908.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
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]


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J. Biol. Chem.Home page
L. E. Heasley, S. Thaler, M. Nicks, B. Price, K. Skorecki, and R. A. Nemenoff
Induction of Cytosolic Phospholipase A2 by Oncogenic Ras in Human Non-small Cell Lung Cancer
J. Biol. Chem., June 6, 1997; 272(23): 14501 - 14504.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
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]


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J. Pharmacol. Exp. Ther.Home page
P. C. Chulada and R. Langenbach
Differential Inhibition of Murine Prostaglandin Synthase-1 and -2 by Nonsteroidal Anti-Inflammatory Drugs Using Exogenous and Endogenous Sources of Arachidonic Acid
J. Pharmacol. Exp. Ther., February 1, 1997; 280(2): 606 - 613.
[Abstract] [Full Text]


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Proc. Natl. Acad. Sci. USAHome page
R. J. Coffey, C. J. Hawkey, L. Damstrup, R. Graves-Deal, V. C. Daniel, P. J. Dempsey, R. Chinery, S. C. Kirkland, R. N. DuBois, T. L. Jetton, et al.
Epidermal growth factor receptor activation induces nuclear targeting of cyclooxygenase-2, basolateral release of prostaglandins, and mitogenesis in polarizing colon cancer cells
PNAS, January 21, 1997; 94(2): 657 - 662.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
M. Murakami, H. Naraba, T. Tanioka, N. Semmyo, Y. Nakatani, F. Kojima, T. Ikeda, M. Fueki, A. Ueno, S. Oh-ishi, et al.
Regulation of Prostaglandin E2 Biosynthesis by Inducible Membrane-associated Prostaglandin E2 Synthase That Acts in Concert with Cyclooxygenase-2
J. Biol. Chem., October 13, 2000; 275(42): 32783 - 32792.
[Abstract] [Full Text] [PDF]




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