Sulindac and its metabolites induce carcinogen metabolizing enzymes in human colon cancer cells

International Journal of Cancer

Volumn 122, Issue 5, 2008, Pages 990-998

  Ciolino, Henry P ^a   Bass, Sara E ^b   MacDonald, Christopher J ^c   Cheng, Robert Y S ^c   Yeh, Grace Chao ^c  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b SAIC FREDERICK INC   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Aryl hydrocarbon receptor (AhR); Cytochrome P450 1A1 (CYP1A1); NAD(P)H:quinone oxidoreductase (NQO1); Sulindac; Sulindac sulfide

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; CARCINOGEN; CYTOCHROME P450 1A1; CYTOCHROME P450 1A2; CYTOCHROME P450 1B1; DACTINOMYCIN; DRUG METABOLITE; GLUCURONOSYLTRANSFERASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; MESSENGER RNA; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE:QUINONE OXIDOREDUCTASE; NONSTEROID ANTIINFLAMMATORY AGENT; OXIDOREDUCTASE; POLYCYCLIC AROMATIC HYDROCARBON; SULINDAC; SULINDAC SULFIDE; SULINDAC SULFONE; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; CYTOCHROME P450; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE);

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL CULTURE; CANCER PREVENTION; CELL STRAIN CACO 2; CHROMATIN IMMUNOPRECIPITATION; COLON CANCER; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYP1A1 GENE; DRUG POTENCY; ENZYME ACTIVITY; GENE; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IN VIVO STUDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; UPREGULATION; BIOSYNTHESIS; COLON TUMOR; DRUG EFFECT; IMMUNOPRECIPITATION; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; COLONIC NEOPLASMS; CYTOCHROME P-450 CYP1A1; CYTOCHROME P-450 ENZYME SYSTEM; GLUCURONOSYLTRANSFERASE; HUMANS; IMMUNOPRECIPITATION; NAD(P)H DEHYDROGENASE (QUINONE); RECEPTORS, ARYL HYDROCARBON; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SULINDAC; TRANSCRIPTION, GENETIC;

EID: 38749111818     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.23218     Document Type: Article

References (78)

1. Edwards BK, Brown ML, Wingo PA, Howe HL, Ward E, Ries LA, Schrag D, Jamison PM, Jemal A, Wu XC, Friedman C, Harlan L, et al. Annual report to the nation on the status of cancer, 1975-2002, featuring population-based trends in cancer treatment. J Natl Cancer Inst 2005;97:1407-27.
2. Thun MJ, Henley SJ, Patrono C. Nonsteroidal anti-inflammatory drugs as anticancer agents: mechanistic, pharmacologic, and clinical issues. J Natl Cancer Inst 2002;94:252-66.
3. Ruegg C, Zaric J, Stupp R. Non steroidal anti-inflammatory drugs and COX-2 inhibitors as anti-cancer therapeutics: hypes, hopes and reality. Ann Med 2003;35:476-87.
4. Whelton A, Stout RL, Spilman PS, Klassen DK. Renal effects of Ibuprofen, piroxicam, and sulindac in patients with asymptomatic renal failure. A prospective, randomized, crossover comparison. Ann Intern Med 1990;112:568-76.
5. Kishimoto Y, Yashima K, Morisawa T, Ohishi T, Marumoto A, Sano A, Idobe-Fujii Y, Miura N, Shiota G, Murawaki Y, Hasegawa J. Effects of long-term administration of sulindac on APC mRNA and apoptosis in colons of rats treated with azoxymethane. J Cancer Res Clin Oncol 2002;128:589-95.
6. Winde G, Schmid KW, Schlegel W, Fischer R, Osswald H, Bunte H. Complete reversion and prevention of rectal adenomas in colectomized patients with familial adenomatous polyposis by rectal low-dose sulindac maintenance treatment. Advantages of a low-dose nonsteroidal anti-inflammatory drug regimen in reversing adenomas exceeding 33 months. Dis Colon Rectum 1995;38:813-30.
7. Pepin P, Bouchard L, Nicole P, Castonguay A. Effects of sulindac and oltipraz on the tumorigenicity of 4-(methylnitrosamino)1-(3-pyridyl)-1-butanone in A/J mouse lung. Carcinogenesis 1992;13:341-8.
8. Cruz-Correa M, Hylind LM, Romans KE, Booker SV, Giardiello FM. Long-term treatment with sulindac in familial adenomatous polyposis: a prospective cohort study. Gastroenterology 2002;122:641-5.
9. Labayle D, Fischer D, Vielh P, Drouhin F, Pariente A, Bories C, Duhamel O, Trousset M, Attali P. Sulindac causes regression of rectal polyps in familial adenomatous polyposis. Gastroenterology 1991;101:635-9.
10. Giardiello FM, Offerhaus JA, Tersmette AC, Hylind LM, Krush AJ, Brensinger JD, Booker SV, Hamilton SR. Sulindac induced regression of colorectal adenomas in familial adenomatous polyposis: evaluation of predictive factors. Gut 1996;38:578-81.
11. Giardiello FM, Spannhake EW, DuBois RN, Hylind LM, Robinson CR, Hubbard WC, Hamilton SR, Yang VW. Prostaglandin levels in human colorectal mucosa: effects of sulindac in patients with familial adenomatous polyposis. Dig Dis Sci 1998;43:311-6.
12. Giardiello FM, Casero RA, Jr, Hamilton SR, Hylind LM, Trimbath JD, Geiman DE, Judge KR, Hubbard W, Offerhaus GJ, Yang VW. Prostanoids, ornithine decarboxylase, and polyamines in primary chemoprevention of familial adenomatous polyposis. Gastroenterology 2004;126:425-31.
13. Hisamuddin IM, Wehbi MA, Schmotzer B, Easley KA, Hylind LM, Giardiello FM, Yang VW. Genetic polymorphisms of flavin monooxygenase 3 in sulindac-induced regression of colorectal adenomas in familial adenomatous polyposis. Cancer Epidemiol Biomarkers Prev 2005;14:2366-9.
14. Hisamuddin IM, Wehbi MA, Chao A, Wyre HW, Hylind LM, Giardiello FM, Yang VW. Genetic polymorphisms of human flavin monooxygenase 3 in sulindac-mediated primary chemoprevention of familial adenomatous polyposis. Clin Cancer Res 2004;10:8357-62.
15. Giardiello FM, Hamilton SR, Krush AJ, Piantadosi S, Hylind LM, Celano P, Booker SV, Robinson CR, Offerhaus GJ. Treatment of colonic and rectal adenomas with sulindac in familial adenomatous polyposis. N Engl J Med 1993;328:1313-6.
16. Chiu CH, McEntee MF, Whelan J. Sulindac causes rapid regression of preexisting tumors in Min/+ mice independent of prostaglandin biosynthesis. Cancer Res 1997;57:4267-73.
17. Deguchi A, Thompson WJ, Weinstein IB. Activation of protein kinase G is sufficient to induce apoptosis and inhibit cell migration in colon cancer cells. Cancer Res 2004;64:3966-73.
18. Zhang L, Yu J, Park BH, Kinzler KW, Vogelstein B. Role of BAX in the apoptotic response to anticancer agents. Science 2000;290:989-92.
19. He TC, Chan TA, Vogelstein B, Kinzler KW. PPARdelta is an APC-regulated target of nonsteroidal anti-inflammatory drugs. Cell 1999;99:335-45.
20. Yamamoto Y, Yin MJ, Lin KM, Gaynor RB. Sulindac inhibits activation of the NF-kappaB pathway. J Biol Chem 1999;274:27307-14.
21. Sawaoka H, Tsuji S, Tsujii M, Gunawan ES, Sasaki Y, Kawano S, Hori M. Cyclooxygenase inhibitors suppress angiogenesis and reduce tumor growth in vivo. Lab Invest 1999;79:1469-77.
22. Skopinska-Rozewska E, Piazza GA, Sommer E, Pamukcu R, Barcz E, Filewska M, Kupis W, Caban R, Rudzinski P, Bogdan J, Mlekodaj S, Sikorska E. Inhibition of angiogenesis by sulindac and its sulfone metabolite (FGN-1): a potential mechanism for their antineoplastic properties. Int J Tissue React 1998;20:85-9.
23. van Lieshout EM, Tiemessen DM, Peters WH, Jansen JB. Effects of nonsteroidal anti-inflammatory drugs on glutathione S-transferases of the rat digestive tract. Carcinogenesis 1997;18:485-90.
24. Van Lieshout EM, Tiemessen DM, Roelofs HM, Peters WH. Nonsteroidal anti-inflammatory drugs enhance glutathione S-transferase theta levels in rat colon. Biochim Biophys Acta 1998;1381:305-11.
25. Patten EJ, DeLong MJ. Effects of sulindac, sulindac metabolites, and aspirin on the activity of detoxification enzymes in HT-29 human colon adenocarcinoma cells. Cancer Lett 1999;147:95-100.
26. Zhang X, Morham SG, Langenbach R, Young DA. Malignant transformation and antineoplastic actions of nonsteroidal antiinflammatory drugs (NSAIDs) on cyclooxygenase-null embryo fibroblasts. J Exp Med 1999;190:451-9.
27. Hanif R, Pittas A, Feng Y, Koutsos MI, Qiao L, Staiano-Coico L, Shiff SI, 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 1996;52:237-45.
28. Thompson HJ, Jiang C, Lu J, Mehta RG, Piazza GA, Paranka NS, Pamukcu R, Ahnen DJ. Sulfone metabolite of sulindac inhibits mammary carcinogenesis. Cancer Res 1997;57:267-71.
29. Duperron C, Castonguay A. Chemopreventive efficacies of aspirin and sulindac against lung tumorigenesis in A/J mice. Carcinogenesis 1997;18:1001-6.
30. Castonguay A, Rioux N. Inhibition of lung tumourigenesis by sulindac: comparison of two experimental protocols. Carcinogenesis 1997;18:491-6.
31. Moorghen M, Ince P, Finney KJ, Sunter JP, Appleton DR, Watson AJ. A protective effect of sulindac against chemically-induced primary colonic tumours in mice. J Pathol 1988;156:341-7.
32. Rao CV, Rivenson A, Simi B, Zang E, Kelloff G, Steele V, Reddy BS. Chemoprevention of colon carcinogenesis by sulindac, a nonsteroidal anti-inflammatory agent. Cancer Res 1995;55:1464-72.
33. Reddy BS, Kawamori T, Lubet RA, Steele VE, Kelloff GJ, Rao CV. Chemopreventive efficacy of sulindac sulfone against colon cancer depends on time of administration during carcinogenic process. Cancer Res 1999;59:3387-91.
34. Ciolino HP, MacDonald CJ, Memon OS, Bass SE, Yeh GC. Sulindac regulates the aryl hydrocarbon receptor-mediated expression of Phase 1 metabolic enzymes in vivo and in vitro. Carcinogenesis 2006;27:1586-92.
35. Buesen R, Mock M, Seidel A, Jacob J, Lampen A. Interaction between metabolism and transport of benzo[a]pyrene and its metabolites in enterocytes. Toxicol Appl Pharmacol 2002;183:168-78.
36. Daujat M, Charrasse S, Fabre I, Lesca P, Jounaidi Y, Larroque C, Poellinger L, Maurel P. Induction of CYP1A1 gene by benzimidazole derivatives during Caco-2 cell differentiation. Evidence for an aryl-hydrocarbon receptor-mediated mechanism. Eur J Biochem 1996;237:642-52.
37. Lampen A, Ebert B, Stumkat L, Jacob J, Seidel A. Induction of gene expression of xenobiotic metabolism enzymes and ABC-transport proteins by PAH and a reconstituted PAH mixture in human Caco-2 cells. Biochim Biophys Acta 2004;1681:38-46.
38. Harper PA, Prokipcak RD, Bush LE, Golas CL, Okey AB. Detection and characterization of the Ah receptor for 2,3,7,8-tetrachlorodibenzo- p-dioxin in the human colon adenocarcinoma cell line LS180. Arch Biochem Biophys 1991;290:27-36.
39. Li W, Harper PA, Tang BK, Okey AB. Regulation of cytochrome P450 enzymes by aryl hydrocarbon receptor in human cells: CYP1A2 expression in the LS180 colon carcinoma cell line after treatment with 2,3,7,8-tetrachlorodibenzo-p- dioxin or 3-methylcholanthrene. Biochem Pharmacol 1998;56:599-612.
40. Tsuchiya Y, Nakajima M, Itoh S, Iwanari M, Yokoi T. Expression of aryl hydrocarbon receptor repressor in normal human tissues and inducibility by polycyclic aromatic hydrocarbons in human tumor-derived cell lines. Toxicol Sci 2003;72:253-9.
41. MacDonald CJ, Ciolino HP, Yeh GC. Dibenzoylmethane modulates aryl hydrocarbon receptor function and expression of cytochromes P450 1A1, 1A2, and 1B1. Cancer Res 2001;61:3919-24.
42. Dohr O, Vogel C, Abel J. Different response of 2,3,7,8- tetrachlorodibenzo-p-dioxin (TCDD)-sensitive genes in human breast cancer MCF-7 and MDA-MB 231 cells. Arch Biochem Biophys 1995;321:405-12.
43. Chung I, Bresnick E. 3-Methylcholanthrene-mediated induction of cytochrome P4501A2 in human hepatoma HepG2 cells as quantified by the reverse transcription-polymerase chain reaction. Arch Biochem Biophys 1994;314:75-81.
44. Elferink CJ, Reiners JJ, Jr. Quantitative RT-PCR on CYP1A1 heterogeneous nuclear RNA: a surrogate for the in vitro transcription run-on assay. Biotechniques 1996;20:470-7.
45. Guigal N, Seree E, Nguyen QB, Charvet B, Desobry A, Barra Y. Serum induces a transcriptional activation of CYP1A1 gene in HepG2 independently of the AhR pathway. Life Sci 2001;68:2141-50.
46. Hestermann EV, Brown M. Agonist and chemopreventative ligands induce differential transcriptional cofactor recruitment by aryl hydrocarbon receptor. Mol Cell Biol 2003;23:7920-5.
47. Prochaska HJ, Santamaria AB, Talalay P. Rapid detection of inducers of enzymes that protect against carcinogens. Proc Natl Acad Sci USA 1992;89:2394-8.
48. Doostdar H, Burke MD, Mayer RT. Bioflavonoids: selective substrates and inhibitors for cytochrome P450 CYP1A and CYP1B1. Toxicology 2000;144:31-8.
49. Korashy HM, El-Kadi AO. Regulatory mechanisms modulating the expression of cytochrome P450 1A1 gene by heavy metals. Toxicol Sci 2005;88:39-51.
50. Denison MS, Nagy SR. Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals. Annu Rev Pharmacol Toxicol 2003;43:309-34.
51. Talalay P, Fahey JW. Phytochemicals from cruciferous plants protect against cancer by modulating carcinogen metabolism. J Nutr 2001;131 (Suppl 11):3027S-3033S.
52. Yeh GC, Daschner PJ, Lopaczynska J, MacDonald CJ, Ciolino HP. Modulation of glucose-6-phosphate dehydrogenase activity and expression is associated with aryl hydrocarbon resistance in vitro. J Biol Chem 2001;276:34708-13.
53. Ebert B, Seidel A, Lampen A. Identification of BCRP as transporter of benzo[a]pyrene conjugates metabolically formed in Caco-2 cells and its induction by Ah-receptor agonists. Carcinogenesis 2005;26:1754-63.
54. Uno S, Dalton TP, Derkenne S, Curran CP, Miller ML, Shertzer HG, Nebert DW. Oral exposure to benzo[a]pyrene in the mouse: detoxication by inducible cytochrome P450 is more important than metabolic activation. Mol Pharmacol 2004;65:1225-37.
55. Nebert DW, Dalton TP, Okey AB, Gonzalez FJ. Role of aryl hydrocarbon receptor-mediated induction of the CYP1 enzymes in environmental toxicity and cancer. J Biol Chem 2004;279:23847-50.
56. Uno S, Dalton TP, Shertzer HG, Genter MB, Warshawsky D, Talaska G, Nebert DW. Benzo[a]pyrene-induced toxicity: paradoxical protection in Cyplal(-/-) knockout mice having increased hepatic BaP-DNA adduct levels. Biochem Biophys Res Commun 2001;289:1049-56.
57. Wattenberg LW, Loub WD. Inhibition of polycyclic aromatic hydrocarbon-induced neoplasia by naturally occurring indoles. Cancer Res 1978;38:1410-3.
58. Grubbs CJ, Steele VE, Casebolt T, Juliana MM, Eto I, Whitaker LM, Dragnev KH, Kelloff GJ, Lubet RL. Chemoprevention of chemically-induced mammary carcinogenesis by indole-3-carbinol. Anticancer Res 1995;15:709-16.
59. Miao W, Hu L, Kandouz M, Batist G. Oltipraz is a bifunctional inducer activating both phase I and phase II drug-metabolizing enzymes via the xenobiotic responsive element. Mol Pharmacol 2003;64:346-54.
60. Guyonnet D, Belloir C, Suschetet M, Siess MH, Le Bon AM. Mechanisms of protection against aflatoxin B(1) genotoxicity in rats treated by organosulfur compounds from garlic. Carcinogenesis 2002;23:1335-41.
61. Bonnesen C, Eggleston IM, Hayes JD. Dietary indoles and isothiocyanates that are generated from cruciferous vegetables can both stimulate apoptosis and confer protection against DNA damage in human colon cell lines. Cancer Res 2001;61:6120-30.
62. Manson MM, Hudson EA, Ball HW, Barrett MC, Clark HL, Judah DJ, Verschoyle RD, Neal GE. Chemoprevention of aflatoxin B1-induced carcinogenesis by indole-3-carbinol in rat liver - predicting the outcome using early biomarkers. Carcinogenesis 1998;19:1829-36.
63. Fang JL, Beland FA, Doerge DR, Wiener D, Guillemette C, Marques MM, Lazarus P. Characterization of benzo(a)pyrene-trans-7,8-dihydrodiol glucuronidation by human tissue microsomes and overexpressed UDP-glucuronosyltransferase enzymes. Cancer Res 2002;62:1978-86.
64. Joseph P, Jaiswal AK. NAD(P)H:quinone oxidoreductase 1 (DT diaphorase) specifically prevents the formation of benzo[a]pyrene quinone-DNA adducts generated by cytochrome P4501A1 and P450 reductase. Proc Natl Acad Sci USA 1994;91:8413-17.
65. Sundberg K, Dreij K, Seidel A, Jernstrom B. Glutathione conjugation and DNA adduct formation of dibenzo[a,1]pyrene and benzo[a]pyrene diol epoxides in V79 cells stably expressing different human glutathione transferases. Chem Res Toxicol 2002;15:170-9.
66. Itoh K, Wakabayashi N, Katoh Y, Ishii T, Igarashi K, Engel JD, Yamamoto M. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev 1999;13:76-86.
67. Kwak MK, Wakabayashi N, Kensler TW. Chemoprevention through the Keap1-Nrf2 signaling pathway by phase 2 enzyme inducers. Mutat Res 2004;555:133-48.
68. Rushmore TH, King RG, Paulson KE, Pickett CB. Regulation of glutathione S-transferase Ya subunit gene expression: identification of a unique xenobiotic-responsive element controlling inducible expression by planar aromatic compounds. Proc Natl Acad Sci USA 1990;87:3826-30.
69. Favreau LV, Pickett CB. Transcriptional regulation of the rat NAD(P)H:quinone reductase gene, identification of regulatory elements controlling basal level expression and inducible expression by planar aromatic compounds and phenolic antioxidants. J Biol Chem 1991;266:4556-61.
70. Emi Y, Ikushiro S, Iyanagi T. Xenobiotic responsive element-mediated transcriptional activation in the UDP-glucuronosyltransferase family 1 gene complex. J Biol Chem 1996;271:3952-8.
71. Cho JS, Chang MS, Rho HM. Transcriptional activation of the human Cu/Zn superoxide dismutase gene by 2,3,7,8-tetrachlorodibenzo-p-dioxin through the xenobiotic-responsive element. Mol Genet Genomics 2001;266:133-41.
72. Ma Q, Kinneer K, Bi Y, Chan JY, Kan YW. Induction of murine NAD(P)H:quinone oxidoreductase by 2,3,7,8-tetrachlorodibenzo-p-dioxin requires the CNC (cap 'n' collar) basic leucine zipper transcription factor Nrf2 (nuclear factor erythroid 2-related factor 2): cross-interaction between AhR (aryl hydrocarbon receptor) and Nrf2 signal transduction. Biochem J 2004;377 (Part 1):205-13.
73. Miao W, Hu L, Kandouz M, Hamilton D, Batist G. A cell-based system to identify and characterize the molecular mechanism of drug-metabolizing enzyme (DME) modulators. Biochem Pharmacol 2004;67:1897-905.
74. Miao W, Hu L, Scrivens PJ, Batist G. Transcriptional regulation of NF-E2 p45-related factor (NRF2) expression by the aryl hydrocarbon receptor-xenobiotic response element signaling pathway: direct cross-talk between phase I and II drug-metabolizing enzymes. J Biol Chem 2005;280:20340-8.
75. Denison MS, Phelan D, Winter GM, Ziccardi MH. Carbaryl, a carbamate insecticide, is a ligand for the hepatic Ah (dioxin) receptor. Toxicol Appl Pharmacol 1998;152:406-14.
76. Taylor MT, Lawson KR, Ignatenko NA, Marek SE, Stringer DE, Skovan BA, Gerner EW. Sulindac sulfone inhibits K-ras-dependent cyclooxygenase-2 expression in human colon cancer cells. Cancer Res 2000;60:6607-10.
77. Rice PL, Beard KS, Driggers LJ, Ahnen DJ. Inhibition of extracellular-signal regulated kinases 1/2 is required for apoptosis of human colon cancer cells in vitro by sulindac metabolites. Cancer Res 2004;64:8148-51.
78. Witta SE, Gustafson DL, Pierson AS, Menter A, Holden SN, Basche M, Persky M, O'Bryant CL, Zeng C, Baron A, Long ME, Gibbs A, et al. A phase I and pharmacokinetic study of exisulind and docetaxel in patients with advanced solid tumors. Clin Cancer Res 2004;10:7229-37.