IL-1β-induced increase in intestinal epithelial tight junction permeability is mediated by MEKK-1 activation of canonical NF-κB pathway

American Journal of Pathology

Volumn 177, Issue 5, 2010, Pages 2310-2322

  Al Sadi, Rana ^a   Ye, Dongmei ^a   Said, Hamid M ^a   Ma, Thomas Y ^a  

^a NONE

Author keywords

[No Author keywords available]

Indexed keywords

I KAPPA B KINASE; I KAPPA B KINASE ALPHA; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MYOSIN LIGHT CHAIN; PROTEIN KINASE; PROTEIN NIK; PROTEIN P100; PROTEIN P52; SYNAPTOTAGMIN I; UNCLASSIFIED DRUG; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE 1; MYOSIN LIGHT CHAIN KINASE; NF KAPPA B KINASE; NF-KAPPA B KINASE; PROTEIN SERINE THREONINE KINASE; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR RELA;

ANIMAL CELL; ARTICLE; CELL PERMEABILIZATION; CELL STRAIN CACO 2; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME INHIBITION; GENE; GENE ACTIVATION; IN VITRO STUDY; INFLAMMATION; INTESTINE EPITHELIUM; MLCK GENE; MONOLAYER CULTURE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; TIGHT JUNCTION; CELL MEMBRANE PERMEABILITY; CYTOLOGY; GENETICS; HUMAN; INTESTINE MUCOSA; METABOLISM; PHYSIOLOGY;

CACO-2 CELLS; CELL MEMBRANE PERMEABILITY; HUMANS; I-KAPPA B KINASE; INTERLEUKIN-1BETA; INTESTINAL MUCOSA; MAP KINASE KINASE KINASE 1; MAP KINASE KINASE KINASES; MYOSIN-LIGHT-CHAIN KINASE; NF-KAPPA B P52 SUBUNIT; PROTEIN-SERINE-THREONINE KINASES; RNA, SMALL INTERFERING; TIGHT JUNCTIONS; TRANSCRIPTION FACTOR RELA;

EID: 78149291807     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.100371     Document Type: Article

References (55)

1. Hollander D, Vadheim CM, Brettholz E, Petersen GM, Delahunty T, Rotter JI: Increased intestinal permeability in patients with Crohn's disease and their relatives. A possible etiologic factor. Ann Intern Med 1986, 105:883-885
2. Ma TY, Anderson, JM: Tight junctions and the intestinal barrier. In: Physiology of the Gastrointestinal Tract. Burlington, MA, Elsevier Academic Press, 2006, pp1559-1594
3. DeMeo MT, Mutlu EA, Keshavarzian A, Tobin MC: Intestinal permeation and gastrointestinal disease. J Clin Gastroenterol 2002, 34:385-396
4. Hecht G, Koutsouris A, Pothoulakis C, LaMont JT, Madara JL: Clostridium difficile toxin B disrupts the barrier function of T84 monolayers. Gastroenterology 1992, 102:416-423
5. Turner JR: Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 2009, 9:799-809
6. Hollander D: Crohn's disease - a permeability disorder of the tight junction? Gut 1988, 29:1621-1624
7. Capaldo CT, Nusrat A: Cytokine regulation of tight junctions. Biochim Biophys Acta 2009, 1788:864-871
8. May GR, Sutherland LR, Meddings JB: Is small intestinal permeability really increased in relatives of patients with Crohn's disease? Gastroenterology 1993, 104:1627-1632
9. Dinarello CA: The interleukin-1 family: 10 years of discovery. FASEB J 1994, 8:1314-1325
10. Dinarello CA: Biologic basis for interleukin-1 in disease. Blood 1996, 87:2095-2147
11. Ligumsky M, Simon PL, Karmeli F, Rachmilewitz D: Role of interleukin 1 in inflammatory bowel disease-enhanced production during active disease. Gut 1990, 31:686-689
12. Nakamura M, Saito H, Kasanuki J, Tamura Y, Yoshida S: Cytokine production in patients with inflammatory bowel disease. Gut 1992, 33:933-937
13. Reinecker HC, Steffen M, Witthoeft T, Pflueger I, Schreiber S, MacDermott RP, Raedler A: Enhanced secretion of tumour necrosis factor-alpha. IL-6, and IL-1 beta by isolated lamina propria mononuclear cells from patients with ulcerative colitis and Crohn's disease. Clin Exp Immunol 1993, 94:174-181
14. Carty E, De Brabander M, Feakins RM, Rampton DS: Measurement of in vivo rectal mucosal cytokine and eicosanoid production in ulcerative colitis using filter paper. Gut 2000, 46:487-492
15. Cominelli F, Pizarro TT: Interleukin-1 and interleukin-1 receptor antagonist in inflammatory bowel disease, Aliment Pharmacol Ther 1996, 10 (Suppl 2):49 -53; discussion 54
16. Mittal RD, Bid HK, Ghoshal UC: IL-1 receptor antagonist (IL-1Ra) gene polymorphism in patients with inflammatory bowel disease in India. Scand J Gastroenterol 2005, 40:827-831
17. Heresbach D, Alizadeh M, Dabadie A, Le Berre N, Colombel JF, Yaouanq J, Bretagne JF, Semana G: Significance of interleukin-1beta and interleukin-1 receptor antagonist genetic polymorphism in inflammatory bowel diseases. Am J Gastroenterol 1997, 92:1164-1169
18. Nemetz A, Nosti-Escanilla MP, Molnar T, Kope A, Kovacs A, Feher J, Tulassay Z, Nagy F, Garcia-Gonzalez MA, Pena AS: IL1B gene polymorphisms influence the course and severity of inflammatory bowel disease. Immunogenetics 1999, 49:527-531
19. Cominelli F, Nast CC, Clark BD, Schindler R, Lierena R, Eysselein VE, Thompson RC, Dinarello CA: Interleukin 1 (IL-1) gene expression, synthesis, and effect of specific IL-1 receptor blockade in rabbit immune complex colitis. J Clin Invest 1990, 86:972-980
20. Cominelli F, Nast CC, Duchini A, Lee M: Recombinant interleukin-1 receptor antagonist blocks the proinflammatory activity of endogenous interleukin-1 in rabbit immune colitis. Gastroenterology 1992, 103:65-71
21. Al-Sadi R, Ye D, Dokladny K, Ma TY: Mechanism of IL-1beta-induced increase in intestinal epithelial tight junction permeability. J Immunol 2008, 180:5653-5661
22. Al-Sadi RM, Ma TY: IL-1beta causes an increase in intestinal epithelial tight junction permeability. J Immunol 2007, 178:4641-4649
23. Ma TY, Iwamoto GK, Hoa NT, Akotia V, Pedram A, Boivin MA, Said HM: TNF-alpha-induced increase in intestinal epithelial tight junction permeability requires NF-kappa B activation. Am J Physiol Gastrointest Liver Physiol 2004, 286:G367-G376
24. Madara JL, Stafford J: Interferon-gamma directly affects barrier function of cultured intestinal epithelial monolayers. J Clin Invest 1989, 83:724-727
25. Bruewer M, Utech M, Ivanov AI, Hopkins AM, Parkos CA, Nusrat A: Interferon-gamma induces internalization of epithelial tight junction proteins via a macropinocytosis-like process. FASEB J 2005, 19:923-933
26. Marano CW, Lewis SA, Garulacan LA, Soler AP, Mullin JM: Tumor necrosis factor-alpha increases sodium and chloride conductance across the tight junction of CACO-2 BBE, a human intestinal epithelial cell line. J Membr Biol 1998, 161:263-274
27. Wang F, Graham WV, Wang Y, Witkowski ED, Schwarz BT, Turner JR: Interferon-gamma and tumor necrosis factor-alpha synergize to induce intestinal epithelial barrier dysfunction by up-regulating myosin light chain kinase expression. Am J Pathol 2005, 166:409-419
28. Al-Sadi R, Boivin M, Ma T: Mechanism of cytokine modulation of epithelial tight junction barrier. Front Biosci 2009, 14:2765-2778
29. Clayburgh DR, Barrett TA, Tang Y, Meddings JB, Van Eldik LJ, Watterson DM, Clarke LL, Mrsny RJ, Turner JR: Epithelial myosin light chain kinase-dependent barrier dysfunction mediates T cell activation-induced diarrhea in vivo. J Clin Invest 2005, 115:2702-2715
30. Clayburgh DR, Musch MW, Leitges M, Fu YX, Turner JR: Coordinated epithelial NHE3 inhibition and barrier dysfunction are required for TNF-mediated diarrhea in vivo. J Clin Invest 2006, 116:2682-2694
31. Arrieta MC, Madsen K, Doyle J, Meddings J: Reducing small intestinal permeability attenuates colitis in the IL10 gene-deficient mouse. Gut 2009, 58:41-48
32. Madsen KL, Malfair D, Gray D, Doyle JS, Jewell LD, Fedorak RN: Interleukin-10 gene-deficient mice develop a primary intestinal permeability defect in response to enteric microflora. Inflamm Bowel Dis 1999, 5:262-270
33. Ferrier L, Mazelin L, Cenac N, Desreumaux P, Janin A, Emilie D, Colombel JF, Garcia-Villar R, Fioramonti J, Bueno L: Stress-induced disruption of colonic epithelial barrier: role of interferon-gamma and myosin light chain kinase in mice. Gastroenterology 2003, 125: 795-804
34. Miehsler W, Puspok A, Oberhuber T, Vogelsang H: Impact of different therapeutic regimens on the outcome of patients with Crohn's disease of the upper gastrointestinal tract. Inflamm Bowel Dis 2001, 7:99-105
35. Wild GE, Waschke KA, Bitton A, Thomson AB: The mechanisms of prednisone inhibition of inflammation in Crohn's disease involve changes in intestinal permeability, mucosal TNFalpha production and nuclear factor kappa B expression. Aliment Pharmacol Ther 2003, 18:309-317
36. Wyatt J, Vogelsang H, Hubl W, Waldhoer T, Lochs H: Intestinal permeability and the prediction of relapse in Crohn's disease. Lancet 1993, 341:1437-1439
37. Thalhamer T, McGrath MA, Harnett MM: MAPKs and their relevance to arthritis and inflammation. Rheumatology (Oxford) 2008, 47:409-414
38. Symons A, Beinke S, Ley SC: MAP kinase kinase kinases and innate immunity. Trends Immunol 2006, 27:40-48
39. Dunne A, O'Neill LA: The interleukin-1 receptor/Toll-like receptor superfamily: signal transduction during inflammation and host defense. Sci STKE 2003, 2003:re3
40. Li Q, Engelhardt JF: Interleukin-1beta induction of NFkappaB is partially regulated by H2O2-mediated activation of NFkappaB-inducing kinase. J Biol Chem 2006, 281:1495-1505
41. Takeuchi J, Hirota K, Itoh T, Shinkura R, Kitada K, Yodoi J, Namba T, Fukuda K: Thioredoxin inhibits tumor necrosis factor- or interleukin-1-induced NF-kappaB activation at a level upstream of NF-kappaB-inducing kinase. Antioxid Redox Signal 2000, 2:83-92
42. Kim YJ, Hwang SY, Oh ES, Oh S, Han IO: IL-1beta, an immediate early protein secreted by activated microglia, induces iNOS/NO in C6 astrocytoma cells through p38 MAPK and NF-kappaB pathways. J Neurosci Res 2006, 84:1037-1046
43. Oetjen E, Blume R, Cierny I, Schlag C, Kutschenko A, Kratzner R, Stein R, Knepel W: Inhibition of MafA transcriptional activity and human insulin gene transcription by interleukin-1beta and mitogen-activated protein kinase kinase kinase in pancreatic islet beta cells. Diabetologia 2007, 50:1678-1687
44. Ye D, Ma I, Ma TY: Molecular mechanism of tumor necrosis factor-alpha modulation of intestinal epithelial tight junction barrier. Am J Physiol Gastrointest Liver Physiol 2006, 290:G496-G504
45. Pomerantz JL, Baltimore D: Two pathways to NF-kappaB. Mol Cell 2002, 10:693-695
46. Baldwin AS Jr: The NF-kappa B and I kappa B proteins: new discoveries and insights, Annu Rev Immunol 1996, 14:649-683
47. Aliaga JC, Deschenes C, Beaulieu JF, Calvo EL, Rivard N: Requirement of the MAP kinase cascade for cell cycle progression and differentiation of human intestinal cells. Am J Physiol 1999, 277: G631-G641
48. Magro F, Fraga S, Ribeiro T, Soares-da-Silva P: Intestinal Na+-K+-ATPase activity and molecular events downstream of interferon-gamma receptor stimulation. Br J Pharmacol 2004, 142:1281-1292
49. Sun Z, Wang X, Lasson A, Borjesson A, Leveau P, Haraldsen P, Andersson R: Roles of platelet-activating factor, interleukin-1beta and interleukin-6 in intestinal barrier dysfunction induced by mesenteric arterial ischemia and reperfusion. J Surg Res 1999, 87:90-100
50. Barreau F, Ferrier L, Fioramonti J, Bueno L: Neonatal maternal deprivation triggers long term alterations in colonic epithelial barrier and mucosal immunity in rats. Gut 2004, 53:501-506
51. Zarnegar B, Yamazaki S, He JQ, Cheng G: Control of canonical NF-kappaB activation through the NIK-IKK complex pathway. Proc Natl Acad Sci USA 2008, 105:3503-3508
52. Karin M, Delhase M: The I kappa B kinase (IKK) and NF-kappa B: key elements of proinflammatory signalling. Semin Immunol 2000, 12:85-98
53. Ma TY, Boivin MA, Ye D, Pedram A, Said HM: Mechanism of TNF-{alpha} modulation of Caco-2 intestinal epithelial tight junction barrier: role of myosin light-chain kinase protein expression. Am J Physiol Gastrointest Liver Physiol 2005, 288:G422-G430
54. Ma TY, Hoa NT, Tran DD, Bui V, Pedram A, Mills S, Merryfield M: Cytochalasin B modulation of Caco-2 tight junction barrier: role of myosin light chain kinase. Am J Physiol Gastrointest Liver Physiol 2000, 279:G875-G885
55. Madara JL, Barenberg D, Carlson S: Effects of cytochalasin D on occluding junctions of intestinal absorptive cells: further evidence that the cytoskeleton may influence paracellular permeability and junctional charge selectivity. J Cell Biol 1986, 102:2125-2136