Cox-2 Is Regulated by Toll-Like Receptor-4 (TLR4) Signaling: Role in Proliferation and Apoptosis in the Intestine

Gastroenterology

Volumn 131, Issue 3, 2006, Pages 862-877

  Fukata, Masayuki ^a   Chen, Anli ^a   Klepper, Arielle ^a   Krishnareddy, Suneeta ^a   Vamadevan, Arunan S ^a   Thomas, Lisa S ^d   Xu, Ruliang ^b   Inoue, Hiroyasu ^e   Arditi, Moshe ^c   Dannenberg, Andrew J ^f   Abreu, Maria T ^a  

^a Division of Gastroenterology   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c Section of Infectious Diseases   (United States)

^d BURNS AND ALLEN RESEARCH INSTITUTE   (United States)

^e NARA WOMEN'S UNIVERSITY   (Japan)

^f NEW YORK PRESBYTERIAN HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BROXURIDINE; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITOR; EPIDERMAL GROWTH FACTOR RECEPTOR; INDOMETACIN; MYELOID DIFFERENTIATION FACTOR 88; PROSTAGLANDIN E2; SMALL INTERFERING RNA; TOLL LIKE RECEPTOR 4;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROLIFERATION; COLITIS; CONTROLLED STUDY; ENZYME REGULATION; FEMALE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; INTESTINE; INTESTINE EPITHELIUM CELL; MALE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROSTAGLANDIN SYNTHESIS; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING; WILD TYPE;

EID: 33748271299     PISSN: 00165085     EISSN: None     Source Type: Journal    
DOI: 10.1053/j.gastro.2006.06.017     Document Type: Article

References (72)

1. Hooper L.V., Stappenbeck T.S., Hong C.V., and Gordon J.I. Angiogenins: a new class of microbicidal proteins involved in innate immunity. Nat Immunol 4 (2003) 269-273
2. Abrams G.D., Bauer H., and Sprinz H. Influence of the normal flora on mucosal morphology and cellular renewal in the ileum. A comparison of germ-free and conventional mice. Lab Invest 12 (1963) 355-364
3. Pull S.L., Doherty J.M., Mills J.C., Gordon J.I., and Stappenbeck T.S. Activated macrophages are an adaptive element of the colonic epithelial progenitor niche necessary for regenerative responses to injury. Proc Natl Acad Sci U S A 102 (2005) 99-104
4. Kitajima S., Morimoto M., Sagara E., Shimizu C., and Ikeda Y. Dextran sodium sulfate-induced colitis in germ-free IQI/Jic mice. Exp Anim 50 (2001) 387-395
5. Sartor R.B. Clinical applications of advances in the genetics of IBD. Rev Gastroenterol Disord 3 (2003) S9-S17
6. Kim S.C., Tonkonogy S.L., Albright C.A., Tsang J., Balish E.J., Braun J., Huycke M.M., and Sartor R.B. Variable phenotypes of enterocolitis in interleukin 10-deficient mice monoassociated with two different commensal bacteria. Gastroenterology 128 (2005) 891-906
7. Pasare C., and Medzhitov R. Toll-like receptors: linking innate and adaptive immunity. Adv Exp Med Biol 560 (2005) 11-18
8. Poltorak A., He X., Smirnova I., Liu M.Y., Huffel C.V., Du X., Birdwell D., Alejos E., Silva M., Galanos C., Freudenberg M., Ricciardi-Castagnoli P., Layton B., and Beutler B. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282 (1998) 2085-2088
9. Hoshino K., Takeuchi O., Kawai T., Sanjo H., Ogawa T., Takeda Y., Takeda K., and Akira S. Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J Immunol 162 (1999) 3749-3752
10. Travassos L.H., Girardin S.E., Philpott D.J., Blanot D., Nahori M.A., Werts C., and Boneca I.G. Toll-like receptor 2-dependent bacterial sensing does not occur via peptidoglycan recognition. EMBO Rep 5 (2004) 1000-1006
11. Sato S., Sanjo H., Takeda K., Ninomiya-Tsuji J., Yamamoto M., Kawai T., Matsumoto K., Takeuchi O., and Akira S. Essential function for the kinase TAK1 in innate and adaptive immune responses. Nat Immunol 6 (2005) 1087-1095
12. Cario E., Gerken G., and Podolsky D.K. Toll-like receptor 2 enhances ZO-1-associated intestinal epithelial barrier integrity via protein kinase C. Gastroenterology 127 (2004) 224-238
13. Vora P., Youdim A., Thomas L.S., Fukata M., Tesfay S.Y., Lukasek K., Michelsen K.S., Wada A., Hirayama T., Arditi M., and Abreu M.T. Beta-defensin-2 expression is regulated by TLR signaling in intestinal epithelial cells. J Immunol 173 (2004) 5398-5405
14. Rakoff-Nahoum S., Paglino J., Eslami-Varzaneh F., Edberg S., and Medzhitov R. Recognition of commensal microflora by Toll-like receptors is required for intestinal homeostasis. Cell 118 (2004) 229-241
15. Fukata M., Michelsen K.S., Eri R., Thomas L.S., Hu B., Lukasek K., Nast C.C., Lechago J., Xu R., Naiki Y., Soliman A., Arditi M., and Abreu M.T. Toll-like receptor-4 is required for intestinal response to epithelial injury and limiting bacterial translocation in a murine model of acute colitis. Am J Physiol 288 (2005) G1055-G1065
16. Araki A., Kanai T., Ishikura T., Makita S., Uraushihara K., Iiyama R., Totsuka T., Takeda K., Akira S., and Watanabe M. MyD88-deficient mice develop severe intestinal inflammation in dextran sodium sulfate colitis. J Gastroenterol 40 (2005) 16-23
17. Backlund M.G., Mann J.R., Holla V.R., Buchanan F.G., Tai H.H., Musiek E.S., Milne G.L., Katkuri S., and DuBois R.N. 15-Hydroxyprostaglandin dehydrogenase is down-regulated in colorectal cancer. J Biol Chem 280 (2005) 3217-3223
18. Subbaramaiah K., Yoshimatsu K., Scherl E., Das K.M., Glazier K.D., Golijanin D., Soslow R.A., Tanabe T., Naraba H., and Dannenberg A.J. Microsomal prostaglandin E synthase-1 is overexpressed in inflammatory bowel disease. Evidence for involvement of the transcription factor Egr-1. J Biol Chem 279 (2004) 12647-12658
19. Otani T., Yamaguchi K., Scherl E., Du B., Tai H.H., Greifer M., Petrovic L., Daikoku T., Dey S.K., Subbaramaiah K., and Dannenberg A.J. Levels of NAD(+)-dependent 15-hydroxyprostaglandin dehydrogenase are reduced in inflammatory bowel disease: evidence for involvement of TNF-alpha. Am J Physiol 290 (2006) G361-G368
20. Newberry R.D., McDonough J.S., Stenson W.F., and Lorenz R.G. Spontaneous and continuous cyclooxygenase-2-dependent prostaglandin E2 production by stromal cells in the murine small intestine lamina propria: directing the tone of the intestinal immune response. J Immunol 166 (2001) 4465-4472
21. Riehl T., Cohn S., Tessner T., Schloemann S., and Stenson W.F. Lipopolysaccharide is radioprotective in the mouse intestine through a prostaglandin-mediated mechanism. Gastroenterology 118 (2000) 1106-1116
22. Morteau O., Morham S.G., Sellon R., Dieleman L.A., Langenbach R., Smithies O., and Sartor R.B. Impaired mucosal defense to acute colonic injury in mice lacking cyclooxygenase-1 or cyclooxygenase-2. J Clin Invest 105 (2000) 469-478
23. Wang D., Buchanan F.G., Wang H., Dey S.K., and DuBois R.N. Prostaglandin E2 enhances intestinal adenoma growth via activation of the Ras-mitogen-activated protein kinase cascade. Cancer Res 65 (2005) 1822-1829
24. Holla V.R., Wang D., Brown J.R., Mann J.R., Katkuri S., and DuBois R.N. Prostaglandin E2 regulates the complement inhibitor CD55/decay-accelerating factor in colorectal cancer. J Biol Chem 280 (2005) 476-483
25. Atreya R., Mudter J., Finotto S., Mullberg J., Jostock T., Wirtz S., Schutz M., Bartsch B., Holtmann M., Becker C., Strand D., Czaja J., Schlaak J.F., Lehr H.A., Autschbach F., Schurmann G., Nishimoto N., Yoshizaki K., Ito H., Kishimoto T., Galle P.R., Rose-John S., and Neurath M.F. Blockade of interleukin 6 trans signaling suppresses T-cell resistance against apoptosis in chronic intestinal inflammation: evidence in Crohn disease and experimental colitis in vivo. Nat Med 6 (2000) 583-588
26. Cooper H.S., Murthy S.N., Shah R.S., and Sedergran D.J. Clinicopathologic study of dextran sulfate sodium experimental murine colitis. Lab Invest 69 (1993) 238-249
27. Siegmund B., Lehr H.A., and Fantuzzi G. Leptin: a pivotal mediator of intestinal inflammation in mice. Gastroenterology 122 (2002) 2011-2025
28. Moss S.F., and Holt P.R. Apoptosis in the intestine. Gastroenterology 111 (1996) 567-568
29. Inoue H., Nanayama T., Hara S., Yokoyama C., and Tanabe T. The cyclic AMP response element plays an essential role in the expression of the human prostaglandin-endoperoxide synthase 2 gene in differentiated U937 monocytic cells. FEBS Lett 350 (1994) 51-54
30. 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 (1995) 24965-24971
31. Mukherji M. Phosphoproteomics in analyzing signaling pathways. Expert Rev Proteomics 2 (2005) 117-128
32. Irish J.M., Hovland R., Krutzik P.O., Perez O.D., Bruserud O., Gjertsen B.T., and Nolan G.P. Single cell profiling of potentiated phospho-protein networks in cancer cells. Cell 118 (2004) 217-228
33. Rhee S.H., and Hwang D. Murine Toll-like receptor 4 confers lipopolysaccharide responsiveness as determined by activation of NF kappa B and expression of the inducible cyclooxygenase. J Biol Chem 275 (2000) 34035-34040
34. Suzuki M., Hisamatsu T., and Podolsky D.K. Gamma interferon augments the intracellular pathway for lipopolysaccharide (LPS) recognition in human intestinal epithelial cells through coordinated up-regulation of LPS uptake and expression of the intracellular Toll-like receptor 4-MD-2 complex. Infect Immun 71 (2003) 3503-3511
35. Yoshimatsu K., Golijanin D., Paty P.B., Soslow R.A., Jakobsson P.J., DeLellis R.A., Subbaramaiah K., and Dannenberg A.J. Inducible microsomal prostaglandin E synthase is overexpressed in colorectal adenomas and cancer. Clin Cancer Res 7 (2001) 3971-3976
36. Backlund M.G., Mann J.R., and Dubois R.N. Mechanisms for the prevention of gastrointestinal cancer: the role of prostaglandin E2. Oncology 69 Suppl 1 (2005) 28-32
37. Meyer T.A., Noguchi Y., Ogle C.K., Tiao G., Wang J.J., Fischer J.E., and Hasselgren P.O. Endotoxin stimulates interleukin-6 production in intestinal epithelial cells. A synergistic effect with prostaglandin E2. Arch Surg 129 (1994) 1290-1295
38. Longo W.E., Damore L.J., Mazuski J.E., Smith G.S., Panesar N., and Kaminski D.L. The role of cyclooxygenase-1 and cyclooxygenase-2 in lipopolysaccharide and interleukin-1 stimulated enterocyte prostanoid formation. Mediators Inflamm 7 (1998) 85-91
39. Grossman E.M., Longo W.E., Mazuski J.E., Panesar N., and Kaminski D.L. Role of cytoplasmic and secretory phospholipase A2 in intestinal epithelial cell prostaglandin E2 formation. Int J Surg Investig 1 (2000) 467-476
40. Newberry R.D., McDonough J.S., Stenson W.F., and Lorenz R.G. Spontaneous and continuous cyclooxygenase-2-dependent prostaglandin E2 production by stromal cells in the murine small intestine lamina propria: directing the tone of the intestinal immune response. J Immunol 166 (2001) 4465-4472
41. Singer I.I., Kawka D.W., Schloemann S., Tessner T., Riehl T., and Stenson W.F. Cyclooxygenase 2 is induced in colonic epithelial cells in inflammatory bowel disease. Gastroenterology 115 (1998) 297-306
42. Watson A.J., Chu S., Sieck L., Gerasimenko O., Bullen T., Campbell F., McKenna M., Rose T., and Montrose M.H. Epithelial barrier function in vivo is sustained despite gaps in epithelial layers. Gastroenterology 129 (2005) 902-912
43. Stern L.E., Erwin C.R., O'Brien D.P., Huang F., and Warner B.W. Epidermal growth factor is critical for intestinal adaptation following small bowel resection. Microsc Res Tech 51 (2000) 138-148
44. Podolsky D.K. Mechanisms of regulatory peptide action in the gastrointestinal tract: trefoil peptides. J Gastroenterol 35 Suppl 12 (2000) 69-74
45. Wu R., Abramson A.L., Shikowitz M.J., Dannenberg A.J., and Steinberg B.M. Epidermal growth factor-induced cyclooxygenase-2 expression is mediated through phosphatidylinositol-3 kinase, not mitogen-activated protein/extracellular signal-regulated kinase kinase, in recurrent respiratory papillomas. Clin Cancer Res 11 (2005) 6155-6161
46. Dannenberg A.J., Lippman S.M., Mann J.R., Subbaramaiah K., and DuBois R.N. Cyclooxygenase-2 and epidermal growth factor receptor: pharmacologic targets for chemoprevention. J Clin Oncol 23 (2005) 254-266
47. Pai R., Soreghan B., Szabo I.L., Pavelka M., Baatar D., and Tarnawski A.S. Prostaglandin E2 transactivates EGF receptor: a novel mechanism for promoting colon cancer growth and gastrointestinal hypertrophy. Nat Med 8 (2002) 289-293
48. Tessner T.G., Muhale F., Riehl T.E., Anant S., and Stenson W.F. Prostaglandin E2 reduces radiation-induced epithelial apoptosis through a mechanism involving AKT activation and bax translocation. J Clin Invest 114 (2004) 1676-1685
49. Jiang D., Liang J., Fan J., Yu S., Chen S., Luo Y., Prestwich G.D., Mascarenhas M.M., Garg H.G., Quinn D.A., Homer R.J., Goldstein D.R., Bucala R., Lee P.J., Medzhitov R., and Noble P.W. Regulation of lung injury and repair by Toll-like receptors and hyaluronan. Nat Med 11 (2005) 1173-1179
50. Ruemmele F.M., Beaulieu J.F., Dionne S., Levy E., Seidman E.G., Cerf-Bensussan N., and Lentze M.J. Lipopolysaccharide modulation of normal enterocyte turnover by Toll-like receptors is mediated by endogenously produced tumour necrosis factor alpha. Gut 51 (2002) 842-848
51. Grishin A.V., Wang J., Hackam D.J., Qureshi F., Upperman J.S., Zamora R., and Ford H.R. p38 MAP kinase mediates endotoxin-induced expression of cyclooxygenase-2 in enterocytes. Surgery 136 (2004) 329-335
52. Grishin A.V., Wang J., Potoka D.A., Hackam D.J., Upperman J.S., Boyle P., Zamora R., and Ford H.R. Lipopolysaccharide induces cyclooxygenase-2 in intestinal epithelium via a noncanonical p38 MAPK pathway. J Immunol 176 (2006) 580-588
53. Tessner T.G., Cohn S.M., Schloemann S., and Stenson W.F. Prostaglandins prevent decreased epithelial cell proliferation associated with dextran sodium sulfate injury in mice. Gastroenterology 115 (1998) 874-882
54. Wang D., Wang H., Shi Q., Katkuri S., Walhi W., Desvergne B., Das S.K., Dey S.K., and DuBois R.N. Prostaglandin E(2) promotes colorectal adenoma growth via transactivation of the nuclear peroxisome proliferator-activated receptor delta. Cancer Cell 6 (2004) 285-295
55. Kabashima K., Saji T., Murata T., Nagamachi M., Matsuoka T., Segi E., Tsuboi K., Sugimoto Y., Kobayashi T., Miyachi Y., Ichikawa A., and Narumiya S. The prostaglandin receptor EP4 suppresses colitis, mucosal damage and CD4 cell activation in the gut. J Clin Invest 109 (2002) 883-893
56. Buchanan F.G., Wang D., Bargiacchi F., and DuBois R.N. Prostaglandin E2 regulates cell migration via the intracellular activation of the epidermal growth factor receptor. J Biol Chem 278 (2003) 35451-35457
57. Konturek P.K., Brzozowski T., Konturek S.J., and Dembinski A. Role of epidermal growth factor, prostaglandin, and sulfhydryls in stress-induced gastric lesions. Gastroenterology 99 (1990) 1607-1615
58. Romano M., Polk W.H., Awad J.A., Arteaga C.L., Nanney L.B., Wargovich M.J., Kraus E.R., Boland C.R., and Coffey R.J. Transforming growth factor alpha protection against drug-induced injury to the rat gastric mucosa in vivo. J Clin Invest 90 (1992) 2409-2421
59. Playford R.J., and Wright N.A. Why is epidermal growth factor present in the gut lumen?. Gut 38 (1996) 303-305
60. Egger B., Buchler M.W., Lakshmanan J., Moore P., and Eysselein V.E. Mice harboring a defective epidermal growth factor receptor (waved-2) have an increased susceptibility to acute dextran sulfate-induced colitis. Scand J Gastroenterol 35 (2000) 1181-1187
61. Carty E., De Brabander M., Feakins R.M., and Rampton D.S. Measurement of in vivo rectal mucosal cytokine and eicosanoid production in ulcerative colitis using filter paper. Gut 46 (2000) 487-492
62. Sharon P., Ligumsky M., Rachmilewitz D., and Zor U. Role of prostaglandins in ulcerative colitis. Enhanced production during active disease and inhibition by sulfasalazine. Gastroenterology 75 (1978) 638-640
63. Wiercinska-Drapalo A., Flisiak R., and Prokopowicz D. Effects of ulcerative colitis activity on plasma and mucosal prostaglandin E2 concentration. Prostaglandins Other Lipid Mediat 58 (1999) 159-165
64. Sheehan K.M., O'Connell F., O'Grady A., Conroy R.M., Leader M.B., Byrne M.F., Murray F.E., and Kay E.W. The relationship between cyclooxygenase-2 expression and characteristics of malignant transformation in human colorectal adenomas. Eur J Gastroenterol Hepatol 16 (2004) 619-625
65. Konturek P.C., Kania J., Burnat G., Hahn E.G., and Konturek S.J. Prostaglandins as mediators of COX-2 derived carcinogenesis in gastrointestinal tract. J Physiol Pharmacol 56 Suppl 5 (2005) 57-73
66. Wang D., Mann J.R., and DuBois R.N. The role of prostaglandins and other eicosanoids in the gastrointestinal tract. Gastroenterology 128 (2005) 1445-1461
67. Castellone M.D., Teramoto H., Williams B.O., Druey K.M., and Gutkind J.S. Prostaglandin E2 promotes colon cancer cell growth through a Gs-axin-beta-catenin signaling axis. Science 310 (2005) 1504-1510
68. Malecka-Panas E., Kordek R., Biernat W., Tureaud J., Liberski P.P., and Majumdar A.P. Differential activation of total and EGF receptor (EGF-R) tyrosine kinase (tyr-k) in the rectal mucosa in patients with adenomatous polyps, ulcerative colitis and colon cancer. Hepatogastroenterology 44 (1997) 435-440
69. Matuk R., Crawford J., Abreu M.T., Targan S.R., Vasiliauskas E.A., and Papadakis K.A. The spectrum of gastrointestinal toxicity and effect on disease activity of selective cyclooxygenase-2 inhibitors in patients with inflammatory bowel disease. Inflamm Bowel Dis 10 (2004) 352-356
70. Sandborn W., Stenson W., Brynskov J., Steidle G., and Robbins J. Safety of celecoxib in patients with ulcerative colitis in remission: a randomized, double-blind, placebo-controlled study. Clin Gastroenterol Hepatol 4 (2006) 157-159
71. Velayos F.S., Terdiman J.P., and Walsh J.M. Effect of 5-aminosalicylate use on colorectal cancer and dysplasia risk: a systematic review and metaanalysis of observational studies. Am J Gastroenterol 100 (2005) 1345-1353
72. Matula S., Croog V., Itzkowitz S., Harpaz N., Bodian C., Hossain S., and Ullman T. Chemoprevention of colorectal neoplasia in ulcerative colitis: the effect of 6-mercaptopurine. Clin Gastroenterol Hepatol 3 (2005) 1015-1021