Skip to main content
Top
Published in: Virchows Archiv 4/2004

01-10-2004 | Review Article

Cyclooxygenase-2 and its role in colorectal cancer development

Authors: Dominique Wendum, Joëlle Masliah, Germain Trugnan, Jean-François Fléjou

Published in: Virchows Archiv | Issue 4/2004

Login to get access

Abstract

Cyclooxygenase 2 (COX-2), also called prostaglandin endoperoxide synthase 2, is involved in colorectal tumor development. This review deals with particular questions raised in this field such as the mechanisms of COX-2 related tumor promotion, the role of the different types of cells (epithelial and interstitial) expressing COX-2, the factors that trigger COX-2 induction, and the clinical potential of selective COX-2 inhibitors to treat or prevent colorectal tumors. Several mechanisms of COX-2 related tumor promotion have been identified. Some are dependent on prostaglandin E2 production (such as induction of cell proliferation, angiogenenis or local immunosuppression, inhibition of apoptosis, increase in cell motility) and others are not (such as carcinogen activation or malondialdehyde production). COX-2 expression has been demonstrated in epithelial cells of colorectal cancers and adenomas and also in interstitial cells. These cells correspond to macrophages and/or fibroblasts and endothelial cells. COX-2 expression in these interstitial cells participates in tumor development. Factors or events that trigger COX-2 expression include oncogene activation, antioncogene inactivation, cytokines, growth factors, some fatty acids, bile salts, and mucins. Finally, selective COX-2 inhibitors may be effective in preventing or treating colorectal adenomas or carcinomas. However, their real efficiency and the cost/benefit balance are currently evaluated, and no definite conclusion can be made at the moment.
Literature
1.
go back to reference Aaltonen LA, Peltomaki P, Mecklin JP, Jarvinen H, Jass JR, Green JS, Lynch HT, Watson P, Tallqvist G, Juhola M et al. (1994) Replication errors in benign and malignant tumors from hereditary nonpolyposis colorectal cancer patients. Cancer Res 54:1645–1648PubMed Aaltonen LA, Peltomaki P, Mecklin JP, Jarvinen H, Jass JR, Green JS, Lynch HT, Watson P, Tallqvist G, Juhola M et al. (1994) Replication errors in benign and malignant tumors from hereditary nonpolyposis colorectal cancer patients. Cancer Res 54:1645–1648PubMed
2.
go back to reference Araki Y, Okamura S, Hussain SP, Nagashima M, He P, Shiseki M, Miura K, Harris CC (2003) Regulation of cyclooxygenase-2 expression by the Wnt and ras pathways. Cancer Res 63:728–734PubMed Araki Y, Okamura S, Hussain SP, Nagashima M, He P, Shiseki M, Miura K, Harris CC (2003) Regulation of cyclooxygenase-2 expression by the Wnt and ras pathways. Cancer Res 63:728–734PubMed
3.
go back to reference Arvind P, Papavassiliou ED, Tsioulias GJ, Qiao L, Lovelace CI, Duceman B, Rigas B (1995) Prostaglandin E2 down-regulates the expression of HLA-DR antigen in human colon adenocarcinoma cell lines. Biochemistry 34:5604–5609 Arvind P, Papavassiliou ED, Tsioulias GJ, Qiao L, Lovelace CI, Duceman B, Rigas B (1995) Prostaglandin E2 down-regulates the expression of HLA-DR antigen in human colon adenocarcinoma cell lines. Biochemistry 34:5604–5609
4.
go back to reference Bamba H, Ota S, Kato A, Adachi A, Itoyama S, Matsuzaki F (1999) High expression of cyclooxygenase-2 in macrophages of human colonic adenoma. Int J Cancer 83:470–475CrossRefPubMed Bamba H, Ota S, Kato A, Adachi A, Itoyama S, Matsuzaki F (1999) High expression of cyclooxygenase-2 in macrophages of human colonic adenoma. Int J Cancer 83:470–475CrossRefPubMed
5.
go back to reference Becerra CR, Frenkel EP, Ashfaq R, Gaynor RB (2003) Increased toxicity and lack of efficacy of Rofecoxib in combination with chemotherapy for treatment of metastatic colorectal cancer: a phase II study. Int J Cancer 105:868–872CrossRefPubMed Becerra CR, Frenkel EP, Ashfaq R, Gaynor RB (2003) Increased toxicity and lack of efficacy of Rofecoxib in combination with chemotherapy for treatment of metastatic colorectal cancer: a phase II study. Int J Cancer 105:868–872CrossRefPubMed
6.
go back to reference Benamouzig R, Deyra J, Martin A, Girard B, Jullian E, Piednoir B, Couturier D, Coste T, Little J, Chaussade S (2003) Daily soluble aspirin and prevention of colorectal adenoma recurrence: one-year results of the APACC trial. Gastroenterology 125:328–336CrossRefPubMed Benamouzig R, Deyra J, Martin A, Girard B, Jullian E, Piednoir B, Couturier D, Coste T, Little J, Chaussade S (2003) Daily soluble aspirin and prevention of colorectal adenoma recurrence: one-year results of the APACC trial. Gastroenterology 125:328–336CrossRefPubMed
7.
go back to reference Cao Y, Pearman AT, Zimmerman GA, McIntyre TM, Prescott SM (2000) Intracellular unesterified arachidonic acid signals apoptosis. Proc Natl Acad Sci U S A 97:11280–11285CrossRefPubMed Cao Y, Pearman AT, Zimmerman GA, McIntyre TM, Prescott SM (2000) Intracellular unesterified arachidonic acid signals apoptosis. Proc Natl Acad Sci U S A 97:11280–11285CrossRefPubMed
8.
go back to reference Chan TA, Morin PJ, Vogelstein B, Kinzler KW (1998) Mechanisms underlying nonsteroidal antiinflammatory drug-mediated apoptosis. Proc Natl Acad Sci U S A 95:681–686CrossRefPubMed Chan TA, Morin PJ, Vogelstein B, Kinzler KW (1998) Mechanisms underlying nonsteroidal antiinflammatory drug-mediated apoptosis. Proc Natl Acad Sci U S A 95:681–686CrossRefPubMed
9.
go back to reference Chandrasekharan NV, Dai H, Roos KL, Evanson NK, Tomsik J, Elton TS, Simmons DL (2002) COX-3, a cyclooxygenase-1 variant inhibited by acetaminophen and other analgesic/antipyretic drugs: cloning, structure, and expression. Proc Natl Acad Sci U S A 99:13926–13931. Epub 12002 Sep 13919CrossRefPubMed Chandrasekharan NV, Dai H, Roos KL, Evanson NK, Tomsik J, Elton TS, Simmons DL (2002) COX-3, a cyclooxygenase-1 variant inhibited by acetaminophen and other analgesic/antipyretic drugs: cloning, structure, and expression. Proc Natl Acad Sci U S A 99:13926–13931. Epub 12002 Sep 13919CrossRefPubMed
10.
go back to reference Chapple KS, Cartwright EJ, Hawcroft G, Tisbury A, Bonifer C, Scott N, Windsor AC, Guillou PJ, Markham AF, Coletta PL, Hull MA (2000) Localization of cyclooxygenase-2 in human sporadic colorectal adenomas. Am J Pathol 156:545–553PubMed Chapple KS, Cartwright EJ, Hawcroft G, Tisbury A, Bonifer C, Scott N, Windsor AC, Guillou PJ, Markham AF, Coletta PL, Hull MA (2000) Localization of cyclooxygenase-2 in human sporadic colorectal adenomas. Am J Pathol 156:545–553PubMed
11.
go back to reference Chulada PC, Thompson MB, Mahler JF, Doyle CM, Gaul BW, Lee C, Tiano HF, Morham SG, Smithies O, Langenbach R (2000) Genetic disruption of Ptgs-1, as well as Ptgs-2, reduces intestinal tumorigenesis in Min mice. Cancer Res 60:4705–4708PubMed Chulada PC, Thompson MB, Mahler JF, Doyle CM, Gaul BW, Lee C, Tiano HF, Morham SG, Smithies O, Langenbach R (2000) Genetic disruption of Ptgs-1, as well as Ptgs-2, reduces intestinal tumorigenesis in Min mice. Cancer Res 60:4705–4708PubMed
12.
go back to reference Cianchi F, Cortesini C, Bechi P, Fantappie O, Messerini L, Vannacci A, Sardi I, Baroni G, Boddi V, Mazzanti R, Masini E (2001) Up-regulation of cyclooxygenase 2 gene expression correlates with tumor angiogenesis in human colorectal cancer. Gastroenterology 121:1339–1347PubMed Cianchi F, Cortesini C, Bechi P, Fantappie O, Messerini L, Vannacci A, Sardi I, Baroni G, Boddi V, Mazzanti R, Masini E (2001) Up-regulation of cyclooxygenase 2 gene expression correlates with tumor angiogenesis in human colorectal cancer. Gastroenterology 121:1339–1347PubMed
13.
go back to reference Daniel TO, Liu H, Morrow JD, Crews BC, Marnett LJ (1999) Thromboxane A2 is a mediator of cyclooxygenase-2-dependent endothelial migration and angiogenesis. Cancer Res 59:4574–4577PubMed Daniel TO, Liu H, Morrow JD, Crews BC, Marnett LJ (1999) Thromboxane A2 is a mediator of cyclooxygenase-2-dependent endothelial migration and angiogenesis. Cancer Res 59:4574–4577PubMed
14.
go back to reference Deviere J (2002) Do selective cyclo-oxygenase inhibitors eliminate the adverse events associated with nonsteroidal anti-inflammatory drug therapy? Eur J Gastroenterol Hepatol 14:S29–S33PubMed Deviere J (2002) Do selective cyclo-oxygenase inhibitors eliminate the adverse events associated with nonsteroidal anti-inflammatory drug therapy? Eur J Gastroenterol Hepatol 14:S29–S33PubMed
15.
go back to reference Dinchuk JE, Car BD, Focht RJ, Johnston JJ, Jaffee BD, Covington MB, Contel NR, Eng VM, Collins RJ, Czerniak PM et al. (1995) Renal abnormalities and an altered inflammatory response in mice lacking cyclooxygenase II. Nature 378:406–409CrossRefPubMed Dinchuk JE, Car BD, Focht RJ, Johnston JJ, Jaffee BD, Covington MB, Contel NR, Eng VM, Collins RJ, Czerniak PM et al. (1995) Renal abnormalities and an altered inflammatory response in mice lacking cyclooxygenase II. Nature 378:406–409CrossRefPubMed
16.
go back to reference Dixon DA, Tolley ND, King PH, Nabors LB, McIntyre TM, Zimmerman GA, Prescott SM (2001) Altered expression of the mRNA stability factor HuR promotes cyclooxygenase-2 expression in colon cancer cells. J Clin Invest 108:1657–1665CrossRefPubMed Dixon DA, Tolley ND, King PH, Nabors LB, McIntyre TM, Zimmerman GA, Prescott SM (2001) Altered expression of the mRNA stability factor HuR promotes cyclooxygenase-2 expression in colon cancer cells. J Clin Invest 108:1657–1665CrossRefPubMed
17.
go back to reference Eberhart CE, Coffey RJ, Radhika A, Giardiello FM, Ferrenbach S, DuBois RN (1994) Up-regulation of cyclooxygenase 2 gene expression in human colorectal adenomas and adenocarcinomas. Gastroenterology 107:1183–1188PubMed Eberhart CE, Coffey RJ, Radhika A, Giardiello FM, Ferrenbach S, DuBois RN (1994) Up-regulation of cyclooxygenase 2 gene expression in human colorectal adenomas and adenocarcinomas. Gastroenterology 107:1183–1188PubMed
18.
go back to reference Einspahr JG, Krouse RS, Yochim JM, Danenberg PV, Danenberg KD, Bhattacharyya AK, Martinez ME, Alberts DS (2003) Association between Cyclooxygenase expression and colorectal adenoma characteristics. Cancer Res 63:3891–3893PubMed Einspahr JG, Krouse RS, Yochim JM, Danenberg PV, Danenberg KD, Bhattacharyya AK, Martinez ME, Alberts DS (2003) Association between Cyclooxygenase expression and colorectal adenoma characteristics. Cancer Res 63:3891–3893PubMed
19.
go back to reference Elder DJ, Baker JA, Banu NA, Moorghen M, Paraskeva C (2002) Human colorectal adenomas demonstrate a size-dependent increase in epithelial cyclooxygenase-2 expression. J Pathol 198:428–434CrossRefPubMed Elder DJ, Baker JA, Banu NA, Moorghen M, Paraskeva C (2002) Human colorectal adenomas demonstrate a size-dependent increase in epithelial cyclooxygenase-2 expression. J Pathol 198:428–434CrossRefPubMed
20.
go back to reference Elder DJ, Halton DE, Crew TE, Paraskeva C (2000) Apoptosis induction and cyclooxygenase-2 regulation in human colorectal adenoma and carcinoma cell lines by the cyclooxygenase-2-selective non-steroidal anti-inflammatory drug NS-398. Int J Cancer 86:553–560CrossRefPubMed Elder DJ, Halton DE, Crew TE, Paraskeva C (2000) Apoptosis induction and cyclooxygenase-2 regulation in human colorectal adenoma and carcinoma cell lines by the cyclooxygenase-2-selective non-steroidal anti-inflammatory drug NS-398. Int J Cancer 86:553–560CrossRefPubMed
21.
go back to reference Fenwick SW, Toogood GJ, Lodge JP, Hull MA (2003) The effect of the selective cyclooxygenase-2 inhibitor rofecoxib on human colorectal cancer liver metastases. Gastroenterology 125:716–729CrossRefPubMed Fenwick SW, Toogood GJ, Lodge JP, Hull MA (2003) The effect of the selective cyclooxygenase-2 inhibitor rofecoxib on human colorectal cancer liver metastases. Gastroenterology 125:716–729CrossRefPubMed
22.
go back to reference Gallo O, Schiavone N, Papucci L, Sardi I, Magnelli L, Franchi A, Masini E, Capaccioli S (2003) Down-regulation of nitric oxide synthase-2 and cyclooxygenase-2 pathways by p53 in squamous cell carcinoma. Am J Pathol 163:723–732PubMed Gallo O, Schiavone N, Papucci L, Sardi I, Magnelli L, Franchi A, Masini E, Capaccioli S (2003) Down-regulation of nitric oxide synthase-2 and cyclooxygenase-2 pathways by p53 in squamous cell carcinoma. Am J Pathol 163:723–732PubMed
23.
go back to reference Giardiello FM, Hamilton SR, Krush AJ, Piantadosi S, Hylind LM, Celano P, Booker SV, Robinson CR, Offerhaus GJ (1993) Treatment of colonic and rectal adenomas with sulindac in familial adenomatous polyposis. N Engl J Med 328:1313–1316CrossRefPubMed Giardiello FM, Hamilton SR, Krush AJ, Piantadosi S, Hylind LM, Celano P, Booker SV, Robinson CR, Offerhaus GJ (1993) Treatment of colonic and rectal adenomas with sulindac in familial adenomatous polyposis. N Engl J Med 328:1313–1316CrossRefPubMed
24.
go back to reference Giovannucci E, Egan KM, Hunter DJ, Stampfer MJ, Colditz GA, Willett WC, Speizer FE (1995) Aspirin and the risk of colorectal cancer in women. N Engl J Med 333:609–614CrossRefPubMed Giovannucci E, Egan KM, Hunter DJ, Stampfer MJ, Colditz GA, Willett WC, Speizer FE (1995) Aspirin and the risk of colorectal cancer in women. N Engl J Med 333:609–614CrossRefPubMed
25.
go back to reference Giovannucci E, Rimm EB, Stampfer MJ, Colditz GA, Ascherio A, Willett WC (1994) Aspirin use and the risk for colorectal cancer and adenoma in male health professionals. Ann Intern Med 121:241–246PubMed Giovannucci E, Rimm EB, Stampfer MJ, Colditz GA, Ascherio A, Willett WC (1994) Aspirin use and the risk for colorectal cancer and adenoma in male health professionals. Ann Intern Med 121:241–246PubMed
26.
go back to reference Glinghammar B, Rafter J (2001) Colonic luminal contents induce cyclooxygenase 2 transcription in human colon carcinoma cells. Gastroenterology 120:401–410PubMed Glinghammar B, Rafter J (2001) Colonic luminal contents induce cyclooxygenase 2 transcription in human colon carcinoma cells. Gastroenterology 120:401–410PubMed
27.
go back to reference Gomez Cerezo J, Lubomirov Hristov R, Carcas Sansuan AJ, Vazquez Rodriguez JJ (2003) Outcome trials of COX-2 selective inhibitors: global safety evaluation does not promise benefits. Eur J Clin Pharmacol 59:169–175PubMed Gomez Cerezo J, Lubomirov Hristov R, Carcas Sansuan AJ, Vazquez Rodriguez JJ (2003) Outcome trials of COX-2 selective inhibitors: global safety evaluation does not promise benefits. Eur J Clin Pharmacol 59:169–175PubMed
28.
go back to reference d’Halluin PN, Turlin B, Polard E, Dinasquet M, Pagenault M, Rioux N, Gosselin M, Bretagne JF, Heresbach D (2003) [Selective COX-2 inhibitor-associated colitis: two case reports]. Gastroenterol Clin Biol 27:932–935PubMed d’Halluin PN, Turlin B, Polard E, Dinasquet M, Pagenault M, Rioux N, Gosselin M, Bretagne JF, Heresbach D (2003) [Selective COX-2 inhibitor-associated colitis: two case reports]. Gastroenterol Clin Biol 27:932–935PubMed
29.
go back to reference Hanif R, Pittas A, Feng Y, Koutsos MI, Qiao L, Staiano-Coico L, Shiff SI, Rigas B (1996) Effects of nonsteroidal anti-inflammatory drugs on proliferation and on induction of apoptosis in colon cancer cells by a prostaglandin-independent pathway. Biochem Pharmacol 52:237–245CrossRefPubMed Hanif R, Pittas A, Feng Y, Koutsos MI, Qiao L, Staiano-Coico L, Shiff SI, Rigas B (1996) Effects of nonsteroidal anti-inflammatory drugs on proliferation and on induction of apoptosis in colon cancer cells by a prostaglandin-independent pathway. Biochem Pharmacol 52:237–245CrossRefPubMed
30.
go back to reference Hao X, Bishop AE, Wallace M, Wang H, Willcocks TC, Maclouf J, Polak JM, Knight S, Talbot IC (1999) Early expression of cyclo-oxygenase-2 during sporadic colorectal carcinogenesis. J Pathol 187:295–301CrossRefPubMed Hao X, Bishop AE, Wallace M, Wang H, Willcocks TC, Maclouf J, Polak JM, Knight S, Talbot IC (1999) Early expression of cyclo-oxygenase-2 during sporadic colorectal carcinogenesis. J Pathol 187:295–301CrossRefPubMed
31.
go back to reference Hasegawa K, Ichikawa W, Fujita T, Ohno R, Okusa T, Yoshinaga K, Sugihara K (2001) Expression of cyclooxygenase-2 (COX-2) mRNA in human colorectal adenomas. Eur J Cancer 37:1469–1474CrossRefPubMed Hasegawa K, Ichikawa W, Fujita T, Ohno R, Okusa T, Yoshinaga K, Sugihara K (2001) Expression of cyclooxygenase-2 (COX-2) mRNA in human colorectal adenomas. Eur J Cancer 37:1469–1474CrossRefPubMed
32.
go back to reference Hull MA, Booth JK, Tisbury A, Scott N, Bonifer C, Markham AF, Coletta PL (1999) Cyclooxygenase 2 is up-regulated and localized to macrophages in the intestine of Min mice. Br J Cancer 79:1399–1405CrossRefPubMed Hull MA, Booth JK, Tisbury A, Scott N, Bonifer C, Markham AF, Coletta PL (1999) Cyclooxygenase 2 is up-regulated and localized to macrophages in the intestine of Min mice. Br J Cancer 79:1399–1405CrossRefPubMed
33.
go back to reference Inaba T, Sano H, Kawahito Y, Hla T, Akita K, Toda M, Yamashina I, Inoue M, Nakada H (2003) Induction of cyclooxygenase-2 in monocyte/macrophage by mucins secreted from colon cancer cells. Proc Natl Acad Sci U S A 100:2736–2741. Epub 2003 Feb 2721CrossRefPubMed Inaba T, Sano H, Kawahito Y, Hla T, Akita K, Toda M, Yamashina I, Inoue M, Nakada H (2003) Induction of cyclooxygenase-2 in monocyte/macrophage by mucins secreted from colon cancer cells. Proc Natl Acad Sci U S A 100:2736–2741. Epub 2003 Feb 2721CrossRefPubMed
34.
go back to reference Jacoby RF, Seibert K, Cole CE, Kelloff G, Lubet RA (2000) The cyclooxygenase-2 inhibitor celecoxib is a potent preventive and therapeutic agent in the min mouse model of adenomatous polyposis. Cancer Res 60:5040–5044PubMed Jacoby RF, Seibert K, Cole CE, Kelloff G, Lubet RA (2000) The cyclooxygenase-2 inhibitor celecoxib is a potent preventive and therapeutic agent in the min mouse model of adenomatous polyposis. Cancer Res 60:5040–5044PubMed
35.
go back to reference Jones DA, Carlton DP, McIntyre TM, Zimmerman GA, Prescott SM (1993) Molecular cloning of human prostaglandin endoperoxide synthase type II and demonstration of expression in response to cytokines. J Biol Chem 268:9049–9054PubMed Jones DA, Carlton DP, McIntyre TM, Zimmerman GA, Prescott SM (1993) Molecular cloning of human prostaglandin endoperoxide synthase type II and demonstration of expression in response to cytokines. J Biol Chem 268:9049–9054PubMed
36.
go back to reference Karnes WE Jr, Shattuck-Brandt R, Burgart LJ, DuBois RN, Tester DJ, Cunningham JM, Kim CY, McDonnell SK, Schaid DJ, Thibodeau SN (1998) Reduced COX-2 protein in colorectal cancer with defective mismatch repair. Cancer Res 58:5473–5477PubMed Karnes WE Jr, Shattuck-Brandt R, Burgart LJ, DuBois RN, Tester DJ, Cunningham JM, Kim CY, McDonnell SK, Schaid DJ, Thibodeau SN (1998) Reduced COX-2 protein in colorectal cancer with defective mismatch repair. Cancer Res 58:5473–5477PubMed
37.
go back to reference Kawamori T, Rao CV, Seibert K, Reddy BS (1998) Chemopreventive activity of celecoxib, a specific cyclooxygenase-2 inhibitor, against colon carcinogenesis. Cancer Res 58:409–412PubMed Kawamori T, Rao CV, Seibert K, Reddy BS (1998) Chemopreventive activity of celecoxib, a specific cyclooxygenase-2 inhibitor, against colon carcinogenesis. Cancer Res 58:409–412PubMed
38.
go back to reference Kojima M, Morisaki T, Uchiyama A, Doi F, Mibu R, Katano M, Tanaka M (2001) Association of enhanced cyclooxygenase-2 expression with possible local immunosuppression in human colorectal carcinomas. Ann Surg Oncol 8:458–465CrossRefPubMed Kojima M, Morisaki T, Uchiyama A, Doi F, Mibu R, Katano M, Tanaka M (2001) Association of enhanced cyclooxygenase-2 expression with possible local immunosuppression in human colorectal carcinomas. Ann Surg Oncol 8:458–465CrossRefPubMed
39.
go back to reference Lim H, Paria BC, Das SK, Dinchuk JE, Langenbach R, Trzaskos JM, Dey SK (1997) Multiple female reproductive failures in cyclooxygenase 2-deficient mice. Cell 91:197–208CrossRefPubMed Lim H, Paria BC, Das SK, Dinchuk JE, Langenbach R, Trzaskos JM, Dey SK (1997) Multiple female reproductive failures in cyclooxygenase 2-deficient mice. Cell 91:197–208CrossRefPubMed
40.
go back to reference Lin E, Morris JS, Ayers GD (2002) Effect of celecoxib on capecitabine-induced hand-foot syndrome and antitumor activity. Oncology (Huntingt) 16:31–37 Lin E, Morris JS, Ayers GD (2002) Effect of celecoxib on capecitabine-induced hand-foot syndrome and antitumor activity. Oncology (Huntingt) 16:31–37
41.
go back to reference Meade EA, McIntyre TM, Zimmerman GA, Prescott SM (1999) Peroxisome proliferators enhance cyclooxygenase-2 expression in epithelial cells. J Biol Chem 274:8328–8334CrossRefPubMed Meade EA, McIntyre TM, Zimmerman GA, Prescott SM (1999) Peroxisome proliferators enhance cyclooxygenase-2 expression in epithelial cells. J Biol Chem 274:8328–8334CrossRefPubMed
42.
go back to reference Morham SG, Langenbach R, Loftin CD, Tiano HF, Vouloumanos N, Jennette JC, Mahler JF, Kluckman KD, Ledford A, Lee CA et al. (1995) Prostaglandin synthase 2 gene disruption causes severe renal pathology in the mouse. Cell 83:473–482CrossRefPubMed Morham SG, Langenbach R, Loftin CD, Tiano HF, Vouloumanos N, Jennette JC, Mahler JF, Kluckman KD, Ledford A, Lee CA et al. (1995) Prostaglandin synthase 2 gene disruption causes severe renal pathology in the mouse. Cell 83:473–482CrossRefPubMed
43.
go back to reference Oshima M, Dinchuk JE, Kargman SL, Oshima H, Hancock B, Kwong E, Trzaskos JM, Evans JF, Taketo MM (1996) Suppression of intestinal polyposis in Apc delta716 knockout mice by inhibition of cyclooxygenase 2 (COX-2). Cell 87:803–809CrossRefPubMed Oshima M, Dinchuk JE, Kargman SL, Oshima H, Hancock B, Kwong E, Trzaskos JM, Evans JF, Taketo MM (1996) Suppression of intestinal polyposis in Apc delta716 knockout mice by inhibition of cyclooxygenase 2 (COX-2). Cell 87:803–809CrossRefPubMed
44.
go back to reference Oshima M, Murai N, Kargman S, Arguello M, Luk P, Kwong E, Taketo MM, Evans JF (2001) Chemoprevention of intestinal polyposis in the Apcdelta716 mouse by rofecoxib, a specific cyclooxygenase-2 inhibitor. Cancer Res 61:1733–1740PubMed Oshima M, Murai N, Kargman S, Arguello M, Luk P, Kwong E, Taketo MM, Evans JF (2001) Chemoprevention of intestinal polyposis in the Apcdelta716 mouse by rofecoxib, a specific cyclooxygenase-2 inhibitor. Cancer Res 61:1733–1740PubMed
45.
go back to reference Pai R, Soreghan B, Szabo IL, Pavelka M, Baatar D, Tarnawski AS (2002) Prostaglandin E2 transactivates EGF receptor: a novel mechanism for promoting colon cancer growth and gastrointestinal hypertrophy. Nat Med 8:289–293CrossRefPubMed Pai R, Soreghan B, Szabo IL, Pavelka M, Baatar D, Tarnawski AS (2002) Prostaglandin E2 transactivates EGF receptor: a novel mechanism for promoting colon cancer growth and gastrointestinal hypertrophy. Nat Med 8:289–293CrossRefPubMed
46.
go back to reference Phillips RK, Wallace MH, Lynch PM, Hawk E, Gordon GB, Saunders BP, Wakabayashi N, Shen Y, Zimmerman S, Godio L, Rodrigues-Bigas M, Su LK, Sherman J, Kelloff G, Levin B, Steinbach G (2002) A randomised, double blind, placebo controlled study of celecoxib, a selective cyclooxygenase 2 inhibitor, on duodenal polyposis in familial adenomatous polyposis. Gut 50:857–860CrossRefPubMed Phillips RK, Wallace MH, Lynch PM, Hawk E, Gordon GB, Saunders BP, Wakabayashi N, Shen Y, Zimmerman S, Godio L, Rodrigues-Bigas M, Su LK, Sherman J, Kelloff G, Levin B, Steinbach G (2002) A randomised, double blind, placebo controlled study of celecoxib, a selective cyclooxygenase 2 inhibitor, on duodenal polyposis in familial adenomatous polyposis. Gut 50:857–860CrossRefPubMed
47.
go back to reference Piazza GA, Alberts DS, Hixson LJ, Paranka NS, Li H, Finn T, Bogert C, Guillen JM, Brendel K, Gross PH, Sperl G, Ritchie J, Burt RW, Ellsworth L, Ahnen DJ, Pamukcu R (1997) Sulindac sulfone inhibits azoxymethane-induced colon carcinogenesis in rats without reducing prostaglandin levels. Cancer Res 57:2909–2915PubMed Piazza GA, Alberts DS, Hixson LJ, Paranka NS, Li H, Finn T, Bogert C, Guillen JM, Brendel K, Gross PH, Sperl G, Ritchie J, Burt RW, Ellsworth L, Ahnen DJ, Pamukcu R (1997) Sulindac sulfone inhibits azoxymethane-induced colon carcinogenesis in rats without reducing prostaglandin levels. Cancer Res 57:2909–2915PubMed
48.
go back to reference Prescott SM, White RL (1996) Self-promotion? Intimate connections between APC and prostaglandin H synthase-2. Cell 87:783–786CrossRefPubMed Prescott SM, White RL (1996) Self-promotion? Intimate connections between APC and prostaglandin H synthase-2. Cell 87:783–786CrossRefPubMed
49.
go back to reference Rao M, Yang W, Seifalian AM, Winslet MC (2004) Role of cyclooxygenase-2 in the angiogenesis of colorectal cancer. Int J Colorectal Dis 19:1–11 Rao M, Yang W, Seifalian AM, Winslet MC (2004) Role of cyclooxygenase-2 in the angiogenesis of colorectal cancer. Int J Colorectal Dis 19:1–11
50.
go back to reference Rigas B, Goldman IS, Levine L (1993) Altered eicosanoid levels in human colon cancer. J Lab Clin Med 122:518–523PubMed Rigas B, Goldman IS, Levine L (1993) Altered eicosanoid levels in human colon cancer. J Lab Clin Med 122:518–523PubMed
51.
go back to reference Sandler RS, Halabi S, Baron JA, Budinger S, Paskett E, Keresztes R, Petrelli N, Pipas JM, Karp DD, Loprinzi CL, Steinbach G, Schilsky R (2003) A randomized trial of aspirin to prevent colorectal adenomas in patients with previous colorectal cancer. N Engl J Med 348:883–890CrossRefPubMed Sandler RS, Halabi S, Baron JA, Budinger S, Paskett E, Keresztes R, Petrelli N, Pipas JM, Karp DD, Loprinzi CL, Steinbach G, Schilsky R (2003) A randomized trial of aspirin to prevent colorectal adenomas in patients with previous colorectal cancer. N Engl J Med 348:883–890CrossRefPubMed
52.
go back to reference Sano H, Kawahito Y, Wilder RL, Hashiramoto A, Mukai S, Asai K, Kimura S, Kato H, Kondo M, Hla T (1995) Expression of cyclooxygenase-1 and -2 in human colorectal cancer. Cancer Res 55:3785–3789PubMed Sano H, Kawahito Y, Wilder RL, Hashiramoto A, Mukai S, Asai K, Kimura S, Kato H, Kondo M, Hla T (1995) Expression of cyclooxygenase-1 and -2 in human colorectal cancer. Cancer Res 55:3785–3789PubMed
53.
go back to reference Seno H, Oshima M, Ishikawa TO, Oshima H, Takaku K, Chiba T, Narumiya S, Taketo MM (2002) Cyclooxygenase 2- and prostaglandin E (2) receptor EP (2)-dependent angiogenesis in Apc (Delta716) mouse intestinal polyps. Cancer Res 62:506–511PubMed Seno H, Oshima M, Ishikawa TO, Oshima H, Takaku K, Chiba T, Narumiya S, Taketo MM (2002) Cyclooxygenase 2- and prostaglandin E (2) receptor EP (2)-dependent angiogenesis in Apc (Delta716) mouse intestinal polyps. Cancer Res 62:506–511PubMed
54.
go back to reference Shao J, Sheng H, Inoue H, Morrow JD, DuBois RN (2000) Regulation of constitutive cyclooxygenase-2 expression in colon carcinoma cells. J Biol Chem 275:33951–33956CrossRefPubMed Shao J, Sheng H, Inoue H, Morrow JD, DuBois RN (2000) Regulation of constitutive cyclooxygenase-2 expression in colon carcinoma cells. J Biol Chem 275:33951–33956CrossRefPubMed
55.
go back to reference Shattuck-Brandt RL, Varilek GW, Radhika A, Yang F, Washington MK, DuBois RN (2000) Cyclooxygenase 2 expression is increased in the stroma of colon carcinomas from IL-10 (-/-) mice. Gastroenterology 118:337–345PubMed Shattuck-Brandt RL, Varilek GW, Radhika A, Yang F, Washington MK, DuBois RN (2000) Cyclooxygenase 2 expression is increased in the stroma of colon carcinomas from IL-10 (-/-) mice. Gastroenterology 118:337–345PubMed
56.
go back to reference Sheng H, Shao J, Hooton EB, Tsujii M, DuBois RN, Beauchamp RD (1997) Cyclooxygenase-2 induction and transforming growth factor beta growth inhibition in rat intestinal epithelial cells. Cell Growth Differ 8:463–470PubMed Sheng H, Shao J, Hooton EB, Tsujii M, DuBois RN, Beauchamp RD (1997) Cyclooxygenase-2 induction and transforming growth factor beta growth inhibition in rat intestinal epithelial cells. Cell Growth Differ 8:463–470PubMed
57.
go back to reference Sheng H, Shao J, Morrow JD, Beauchamp RD, DuBois RN (1998) Modulation of apoptosis and Bcl-2 expression by prostaglandin E2 in human colon cancer cells. Cancer Res 58:362–366PubMed Sheng H, Shao J, Morrow JD, Beauchamp RD, DuBois RN (1998) Modulation of apoptosis and Bcl-2 expression by prostaglandin E2 in human colon cancer cells. Cancer Res 58:362–366PubMed
58.
go back to reference Sheng H, Shao J, Dubois RN (2001) K-Ras-mediated increase in cyclooxygenase 2 mRNA stability involves activation of the protein kinase B1. Cancer Res 61:2670–2675PubMed Sheng H, Shao J, Dubois RN (2001) K-Ras-mediated increase in cyclooxygenase 2 mRNA stability involves activation of the protein kinase B1. Cancer Res 61:2670–2675PubMed
59.
go back to reference Sheng H, Shao J, Washington MK, DuBois RN (2001) Prostaglandin E2 increases growth and motility of colorectal carcinoma cells. J Biol Chem 276:18075–18081CrossRefPubMed Sheng H, Shao J, Washington MK, DuBois RN (2001) Prostaglandin E2 increases growth and motility of colorectal carcinoma cells. J Biol Chem 276:18075–18081CrossRefPubMed
60.
go back to reference Shiff SJ, Rigas B (1997) Nonsteroidal anti-inflammatory drugs and colorectal cancer: evolving concepts of their chemopreventive actions. Gastroenterology 113:1992–1998PubMed Shiff SJ, Rigas B (1997) Nonsteroidal anti-inflammatory drugs and colorectal cancer: evolving concepts of their chemopreventive actions. Gastroenterology 113:1992–1998PubMed
61.
go back to reference Silverstein FE, Faich G, Goldstein JL, Simon LS, Pincus T, Whelton A, Makuch R, Eisen G, Agrawal NM, Stenson WF, Burr AM, Zhao WW, Kent JD, Lefkowith JB, Verburg KM, Geis GS (2000) Gastrointestinal toxicity with celecoxib vs nonsteroidal anti-inflammatory drugs for osteoarthritis and rheumatoid arthritis: the CLASS study: a randomized controlled trial. Celecoxib Long-term Arthritis Safety Study. JAMA 284:1247–1255CrossRefPubMed Silverstein FE, Faich G, Goldstein JL, Simon LS, Pincus T, Whelton A, Makuch R, Eisen G, Agrawal NM, Stenson WF, Burr AM, Zhao WW, Kent JD, Lefkowith JB, Verburg KM, Geis GS (2000) Gastrointestinal toxicity with celecoxib vs nonsteroidal anti-inflammatory drugs for osteoarthritis and rheumatoid arthritis: the CLASS study: a randomized controlled trial. Celecoxib Long-term Arthritis Safety Study. JAMA 284:1247–1255CrossRefPubMed
62.
go back to reference Sinicrope FA, Lemoine M, Xi L, Lynch PM, Cleary KR, Shen Y, Frazier ML (1999) Reduced expression of cyclooxygenase 2 proteins in hereditary nonpolyposis colorectal cancers relative to sporadic cancers. Gastroenterology 117:350–358PubMed Sinicrope FA, Lemoine M, Xi L, Lynch PM, Cleary KR, Shen Y, Frazier ML (1999) Reduced expression of cyclooxygenase 2 proteins in hereditary nonpolyposis colorectal cancers relative to sporadic cancers. Gastroenterology 117:350–358PubMed
63.
go back to reference Smith WL, Garavito RM, DeWitt DL (1996) Prostaglandin endoperoxide H synthases (cyclooxygenases)-1 and -2. J Biol Chem 271:33157–33160CrossRefPubMed Smith WL, Garavito RM, DeWitt DL (1996) Prostaglandin endoperoxide H synthases (cyclooxygenases)-1 and -2. J Biol Chem 271:33157–33160CrossRefPubMed
64.
go back to reference Smith WL, DeWitt DL, Garavito RM (2000) Cyclooxygenases: structural, cellular, and molecular biology. Annu Rev Biochem 69:145–182CrossRefPubMed Smith WL, DeWitt DL, Garavito RM (2000) Cyclooxygenases: structural, cellular, and molecular biology. Annu Rev Biochem 69:145–182CrossRefPubMed
65.
go back to reference Sonoshita M, Takaku K, Oshima M, Sugihara K, Taketo MM (2002) Cyclooxygenase-2 expression in fibroblasts and endothelial cells of intestinal polyps. Cancer Res 62:6846–6849PubMed Sonoshita M, Takaku K, Oshima M, Sugihara K, Taketo MM (2002) Cyclooxygenase-2 expression in fibroblasts and endothelial cells of intestinal polyps. Cancer Res 62:6846–6849PubMed
66.
go back to reference Steinbach G, Lynch PM, Phillips RK, Wallace MH, Hawk E, Gordon GB, Wakabayashi N, Saunders B, Shen Y, Fujimura T, Su LK, Levin B (2000) The effect of celecoxib, a cyclooxygenase-2 inhibitor, in familial adenomatous polyposis. N Engl J Med 342:1946–1952CrossRefPubMed Steinbach G, Lynch PM, Phillips RK, Wallace MH, Hawk E, Gordon GB, Wakabayashi N, Saunders B, Shen Y, Fujimura T, Su LK, Levin B (2000) The effect of celecoxib, a cyclooxygenase-2 inhibitor, in familial adenomatous polyposis. N Engl J Med 342:1946–1952CrossRefPubMed
67.
go back to reference Subbaramaiah K, Altorki N, Chung WJ, Mestre JR, Sampat A, Dannenberg AJ (1999) Inhibition of cyclooxygenase-2 gene expression by p53. J Biol Chem 274:10911–10915CrossRefPubMed Subbaramaiah K, Altorki N, Chung WJ, Mestre JR, Sampat A, Dannenberg AJ (1999) Inhibition of cyclooxygenase-2 gene expression by p53. J Biol Chem 274:10911–10915CrossRefPubMed
68.
go back to reference Thun MJ, Henley SJ, Patrono C (2002) Nonsteroidal anti-inflammatory drugs as anticancer agents: mechanistic, pharmacologic, and clinical issues. J Natl Cancer Inst 94:252–266CrossRefPubMed Thun MJ, Henley SJ, Patrono C (2002) Nonsteroidal anti-inflammatory drugs as anticancer agents: mechanistic, pharmacologic, and clinical issues. J Natl Cancer Inst 94:252–266CrossRefPubMed
69.
go back to reference Tiano HF, Loftin CD, Akunda J, Lee CA, Spalding J, Sessoms A, Dunson DB, Rogan EG, Morham SG, Smart RC, Langenbach R (2002) Deficiency of Either Cyclooxygenase (COX)-1 or COX-2 Alters Epidermal Differentiation and Reduces Mouse Skin Tumorigenesis. Cancer Res 62:3395–3401PubMed Tiano HF, Loftin CD, Akunda J, Lee CA, Spalding J, Sessoms A, Dunson DB, Rogan EG, Morham SG, Smart RC, Langenbach R (2002) Deficiency of Either Cyclooxygenase (COX)-1 or COX-2 Alters Epidermal Differentiation and Reduces Mouse Skin Tumorigenesis. Cancer Res 62:3395–3401PubMed
70.
go back to reference Tomozawa S, Nagawa H, Tsuno N, Hatano K, Osada T, Kitayama J, Sunami E, Nita ME, Ishihara S, Yano H, Tsuruo T, Shibata Y, Muto T (1999) Inhibition of haematogenous metastasis of colon cancer in mice by a selective COX-2 inhibitor, JTE-522. Br J Cancer 81:1274–1279CrossRefPubMed Tomozawa S, Nagawa H, Tsuno N, Hatano K, Osada T, Kitayama J, Sunami E, Nita ME, Ishihara S, Yano H, Tsuruo T, Shibata Y, Muto T (1999) Inhibition of haematogenous metastasis of colon cancer in mice by a selective COX-2 inhibitor, JTE-522. Br J Cancer 81:1274–1279CrossRefPubMed
71.
go back to reference Tsujii M, DuBois RN (1995) Alterations in cellular adhesion and apoptosis in epithelial cells overexpressing prostaglandin endoperoxide synthase 2. Cell 83:493–501CrossRefPubMed Tsujii M, DuBois RN (1995) Alterations in cellular adhesion and apoptosis in epithelial cells overexpressing prostaglandin endoperoxide synthase 2. Cell 83:493–501CrossRefPubMed
72.
go back to reference Tsujii M, Kawano S, DuBois RN (1997) Cyclooxygenase-2 expression in human colon cancer cells increases metastatic potential. Proc Natl Acad Sci U S A 94:3336–3340CrossRefPubMed Tsujii M, Kawano S, DuBois RN (1997) Cyclooxygenase-2 expression in human colon cancer cells increases metastatic potential. Proc Natl Acad Sci U S A 94:3336–3340CrossRefPubMed
73.
go back to reference Tsujii M, Kawano S, Tsuji S, Sawaoka H, Hori M, DuBois RN (1998) Cyclooxygenase regulates angiogenesis induced by colon cancer cells. Cell 93:705–716CrossRefPubMed Tsujii M, Kawano S, Tsuji S, Sawaoka H, Hori M, DuBois RN (1998) Cyclooxygenase regulates angiogenesis induced by colon cancer cells. Cell 93:705–716CrossRefPubMed
74.
go back to reference Waddell WR, Ganser GF, Cerise EJ, Loughry RW (1989) Sulindac for polyposis of the colon. Am J Surg 157:175–179CrossRefPubMed Waddell WR, Ganser GF, Cerise EJ, Loughry RW (1989) Sulindac for polyposis of the colon. Am J Surg 157:175–179CrossRefPubMed
75.
go back to reference Wallace JL, Bak A, McKnight W, Asfaha S, Sharkey KA, MacNaughton WK (1998) Cyclooxygenase 1 contributes to inflammatory responses in rats and mice: implications for gastrointestinal toxicity. Gastroenterology 115:101–109PubMed Wallace JL, Bak A, McKnight W, Asfaha S, Sharkey KA, MacNaughton WK (1998) Cyclooxygenase 1 contributes to inflammatory responses in rats and mice: implications for gastrointestinal toxicity. Gastroenterology 115:101–109PubMed
76.
go back to reference Wallace JL, Chapman K, McKnight W (1999) Limited anti-inflammatory efficacy of cyclo-oxygenase-2 inhibition in carrageenan-airpouch inflammation. Br J Pharmacol 126:1200–1204PubMed Wallace JL, Chapman K, McKnight W (1999) Limited anti-inflammatory efficacy of cyclo-oxygenase-2 inhibition in carrageenan-airpouch inflammation. Br J Pharmacol 126:1200–1204PubMed
77.
go back to reference Wendum D, Boelle PY, Rigau V, Sebbagh N, Olschwang S, Mourra N, Parc R, Trugnan G, Masliah J, Flejou JF (2003) Mucinous colon carcinomas with microsatellite instability have a lower microvessel density and lower vascular endothelial growth factor expression. Virchows Arch 442:111–117PubMed Wendum D, Boelle PY, Rigau V, Sebbagh N, Olschwang S, Mourra N, Parc R, Trugnan G, Masliah J, Flejou JF (2003) Mucinous colon carcinomas with microsatellite instability have a lower microvessel density and lower vascular endothelial growth factor expression. Virchows Arch 442:111–117PubMed
78.
go back to reference Wendum D, Svrcek M, Rigau V, Boelle PY, Sebbagh N, Parc R, Masliah J, Trugnan G, Flejou JF (2003) COX-2, inflammatory secreted PLA2, and cytoplasmic PLA2 protein expression in small bowel adenocarcinomas compared with colorectal adenocarcinomas. Mod Pathol 16:130–136CrossRefPubMed Wendum D, Svrcek M, Rigau V, Boelle PY, Sebbagh N, Parc R, Masliah J, Trugnan G, Flejou JF (2003) COX-2, inflammatory secreted PLA2, and cytoplasmic PLA2 protein expression in small bowel adenocarcinomas compared with colorectal adenocarcinomas. Mod Pathol 16:130–136CrossRefPubMed
79.
go back to reference Williams CS, Tsujii M, Reese J, Dey SK, DuBois RN (2000) Host cyclooxygenase-2 modulates carcinoma growth. J Clin Invest 105:1589–1594PubMed Williams CS, Tsujii M, Reese J, Dey SK, DuBois RN (2000) Host cyclooxygenase-2 modulates carcinoma growth. J Clin Invest 105:1589–1594PubMed
80.
go back to reference Yao M, Kargman S, Lam EC, Kelly CR, Zheng Y, Luk P, Kwong E, Evans JF, Wolfe MM (2003) Inhibition of cyclooxygenase-2 by rofecoxib attenuates the growth and metastatic potential of colorectal carcinoma in mice. Cancer Res 63:586–592PubMed Yao M, Kargman S, Lam EC, Kelly CR, Zheng Y, Luk P, Kwong E, Evans JF, Wolfe MM (2003) Inhibition of cyclooxygenase-2 by rofecoxib attenuates the growth and metastatic potential of colorectal carcinoma in mice. Cancer Res 63:586–592PubMed
Metadata
Title
Cyclooxygenase-2 and its role in colorectal cancer development
Authors
Dominique Wendum
Joëlle Masliah
Germain Trugnan
Jean-François Fléjou
Publication date
01-10-2004
Publisher
Springer-Verlag
Published in
Virchows Archiv / Issue 4/2004
Print ISSN: 0945-6317
Electronic ISSN: 1432-2307
DOI
https://doi.org/10.1007/s00428-004-1105-2

Other articles of this Issue 4/2004

Virchows Archiv 4/2004 Go to the issue

Announcements

October 2004