Interleukin-18 facilitates neutrophil transmigration via myosin light chain kinase-dependent disruption of occludin, without altering epithelial permeability

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 302, Issue 3, 2012, Pages

  Lapointe, Tamia K ^a   Buret, Andre G ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Inflammatory bowel disease; Neutrophil transepithelial migration

Indexed keywords

1 (5 CHLORO 1 NAPHTHALENESULFONYL)HEXAHYDRO 1H 1,4 DIAZEPINE; 3 (4 METHYLPHENYLSULFONYL) 2 PROPENENITRILE; CLAUDIN 4; CLAUDIN 5; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 18; MYOSIN LIGHT CHAIN KINASE; OCCLUDIN; PROTEIN ZO1; UVOMORULIN;

ARTICLE; CELL MIGRATION; CELL STRAIN CACO 2; COLON MUCOSA; ENTERITIS; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; INTESTINE FUNCTION; INTESTINE MUCOSA PERMEABILITY; NEUTROPHIL; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN DEPLETION; TIGHT JUNCTION;

AZEPINES; CACO-2 CELLS; CADHERINS; CARDIAC MYOSINS; CLAUDINS; DEXTRANS; ELECTRIC IMPEDANCE; EPITHELIAL CELLS; ESCHERICHIA COLI; FLUORESCEIN-5-ISOTHIOCYANATE; GENE EXPRESSION; HUMANS; INTERLEUKIN-18; INTESTINAL MUCOSA; MEMBRANE PROTEINS; MYOSIN LIGHT CHAINS; MYOSIN-LIGHT-CHAIN KINASE; N-FORMYLMETHIONINE LEUCYL-PHENYLALANINE; NEUTROPHILS; NF-KAPPA B; NITRILES; PERMEABILITY; PHOSPHOPROTEINS; PHOSPHORYLATION; SULFONES; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION;

EID: 84856141443     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00202.2011     Document Type: Article

References (64)

1. Adachi O, Kawai T, Takeda K, Matsumoto M, Tsutsui H, Sakagami M, Nakanishi K, Akira S. Targeted disruption of the MyD88 gene results in loss of IL-1-and IL-18-mediated function. Immunity 9: 143-150, 1998.
2. Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell 124: 783-801, 2006.
3. Al-Sadi R, Ye D, Dokladny K, Ma TY. Mechanism of IL-1 -induced increase in intestinal epithelial tight junction permeability. J Immunol 180: 5653-5661, 2008.
4. Al-Sadi RM, Ma TY. IL-1 causes an increase in intestinal epithelial tight junction permeability. J Immunol 178: 4641-4649, 2007.
5. Balda MS, Whitney JA, Flores C, Gonzalez S, Cereijido M, Matter K. Functional dissociation of paracellular permeability and transepithelial electrical resistance and disruption of the apical-basolateral intramem-brane diffusion barrier by expression of a mutant tight junction membrane protein. J Cell Biol 134: 1031-1049, 1996.
6. Blair SA, Kane SV, Clayburgh DR, Turner JR. Epithelial myosin light chain kinase expression and activity are upregulated in inflammatory bowel disease. Lab Invest 86: 191-201, 2006.
7. Bruewer M, Utech M, Ivanov A, Hopkins A, Parkos C, Nusrat A. Interferon-γ induces internalization of epithelial tight junction proteins via a macropinocytosis-like process. FASEB J 19: 923-933, 2005.
8. Chin AC, Parkos CA. Neutrophil transepithelial migration and epithelial barrier function in IBD: potential targets for inhibiting neutrophil trafficking. Ann NY Acad Sci 1072: 276-287, 2006.
9. Chun J, Prince A. TLR2-induced calpain cleavage of epithelial junctional proteins facilitates leukocyte transmigration. Cell Host Microbe 5: 47-58, 2009.
10. Ciccocioppo R, Finamore A, Ara C, Di Sabatino A, Mengheri E, Corazza GR. Altered expression, localization, and phosphorylation of epithelial junctional proteins in celiac disease. Am J Clin Pathol 125: 502-511, 2006.
11. 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 activa-tion-induced diarrhea in vivo. J Clin Invest 115: 2702-2715, 2005.
12. 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 116: 2682-2694, 2006.
13. Dogan A, Wang ZD, Spencer J. E-cadherin expression in intestinal epithelium. J Clin Pathol 48: 143-146, 1995.
14. Dransfield I, Stocks SC, Haslett C. Regulation of cell adhesion molecule expression and function associated with neutrophil apoptosis. Blood 85: 3264-3273, 1995.
15. Edelblum K, Shen L, Marchiando A, Wang Y, Sperling A, Turner J. Occludin regulates intraepithelial lymphocyte migration in vivo (Abstract). Gastroenterology 140: S132, 2011.
16. Edens HA, Levi BP, Jaye DL, Walsh S, Reaves TA, Turner JR, Nusrat A, Parkos CA. Neutrophil transepithelial migration: evidence for sequential, contact-dependent signaling events and enhanced paracellular permeability independent of transjunctional migration. J Immunol 169: 476-486, 2002.
17. Fedwick JP, Lapointe TK, Meddings JB, Sherman PM, Buret AG. Helicobacter pylori activates myosin light-chain kinase to disrupt claudin-4 and claudin-5 and increase epithelial permeability. Infect Immun 73: 7844-7852, 2005.
18. Furuse M, Fujita K, Hiiragi T, Fujimoto K, Tsukita S. Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. J Cell Biol 141: 1539-1550, 1998.
19. Furuse M, Itoh M, Hirase T, Nagafuchi A, Yonemura S, Tsukita S. Direct association of occludin with ZO-1 and its possible involvement in the localization of occludin at tight junctions. J Cell Biol 127: 1617-1626, 1994.
20. Gassler N, Rohr C, Schneider A, Kartenbeck J, Bach A, Obermuller N, Otto HF, Autschbach F. Inflammatory bowel disease is associated with changes of enterocytic junctions. Am J Physiol Gastrointest Liver Physiol 281: G216-G228, 2001.
21. Huber D, Balda MS, Matter K. Occludin modulates transepithelial migration of neutrophils. J Biol Chem 275: 5773-5778, 2000.
22. Itoh M, Furuse M, Morita K, Kubota K, Saitou M, Tsukita S. Direct binding of three tight junction-associated MAGUKs, ZO-1, ZO-2, and ZO-3, with the COOH termini of claudins. J Cell Biol 147: 1351-1363, 1999.
23. Ivanov AI, Nusrat A, Parkos CA. Endocytosis of epithelial apical junctional proteins by a clathrin-mediated pathway into a unique storage compartment. Mol Biol Cell 15: 176-188, 2004.
24. Kanai T, Watanabe M, Okazawa A, Nakamaru K, Okamoto M, Naganuma M, Ishii H, Ikeda M, Kurimoto M, Hibi T. Interleukin 18 is a potent proliferative factor for intestinal mucosal lymphocytes in Crohn's disease. Gastroenterology 119: 1514-1523, 2000.
25. Kanai T, Watanabe M, Okazawa A, Sato T, Yamazaki M, Okamoto S, Ishii H, Totsuka T, Iiyama R, Okamoto R, Ikeda M, Kurimoto M, Takeda K, Akira S, Hibi T. Macrophage-derived IL-18-mediated intestinal inflammation in the murine model of Crohn's disease. Gastroenterology 121: 875-888, 2001.
26. Karayiannakis AJ, Syrigos KN, Efstathiou J, Valizadeh A, Noda M, Playford RJ, Kmiot W, Pignatelli M. Expression of catenins and E-cadherin during epithelial restitution in inflammatory bowel disease. J Pathol 185: 413-418, 1998.
27. Keller TC 3rd, Mooseker MS. Ca2_-calmodulin-dependent phosphorylation of myosin and its role in brush border contraction in vitro. J Cell Biol 95: 943-959, 1982.
28. Kohka H, Yoshino T, Iwagaki H, Sakuma I, Tanimoto T, Matsuo Y, Kurimoto M, Orita K, Akagi T, Tanaka N. Interleukin-18/interferon-_-inducing factor, a novel cytokine, up-regulates ICAM-1 (CD54) expression in KG-1 cells. J Leukoc Biol 64: 519-527, 1998.
29. Kucharzik T, Walsh SV, Chen J, Parkos CA, Nusrat A. Neutrophil transmigration in inflammatory bowel disease is associated with differential expression of epithelial intercellular junction proteins. Am J Pathol 159: 2001-2009, 2001.
30. Lamb-Rosteski JM, Kalischuk LD, Inglis GD, Buret AG. Epidermal growth factor inhibits Campylobacter jejuni-induced claudin-4 disruption, loss of epithelial barrier function, and Escherichia coli translocation. Infect Immun 76: 3390-3398, 2008.
31. Lapointe TK, O'Connor PM, Jones NL, Menard D, Buret AG. Interleukin-1 receptor phosphorylation activates Rho kinase to disrupt human gastric tight junctional claudin-4 during Helicobacter pylori infection. Cell Microbiol 12: 692-703, 2010.
32. Leach ST, Messina I, Lemberg DA, Novick D, Rubenstein M, Day AS. Local and systemic interleukin-18 and interleukin-18-binding protein in children with inflammatory bowel disease. Inflamm Bowel Dis 14: 68-74, 2008.
33. Lee JK, Kim SH, Lewis EC, Azam T, Reznikov LL, Dinarello CA. Differences in signaling pathways by IL-1_ and IL-18. Proc Natl Acad Sci USA 101: 8815-8820, 2004.
34. Lee WY, Chin AC, Voss S, Parkos CA. In vitro neutrophil transepithelial migration. Methods Mol Biol 341: 205-215, 2006.
35. Leon AJ, Gomez E, Garrote JA, Bernardo D, Barrera A, Marcos JL, Fernandez-Salazar L, Velayos B, Blanco-Quiros A, Arranz E. High levels of proinflammatory cytokines, but not markers of tissue injury, in unaffected intestinal areas from patients with IBD. Mediators Inflamm 2009: 580450, 2009.
36. Magness ST, Jijon H, Van Houten Fisher N, Sharpless NE, Brenner DA, Jobin C. In vivo pattern of lipopolysaccharide and anti-CD3-induced NF-_B activation using a novel gene-targeted enhanced GFP reporter gene mouse. J Immunol 173: 1561-1570, 2004.
37. Marchiando AM, Shen L, Graham WV, Weber CR, Schwarz BT, Austin JR 2nd, Raleigh DR, Guan Y, Watson AJ, Montrose MH, Turner JR. Caveolin-1-dependent occludin endocytosis is required for TNF-induced tight junction regulation in vivo. J Cell Biol 189: 111-126, 2010.
38. McCarthy KM, Skare IB, Stankewich MC, Furuse M, Tsukita S, Rogers RA, Lynch RD, Schneeberger EE. Occludin is a functional component of the tight junction. J Cell Sci 109: 2287-2298, 1996.
39. Monteleone G, Trapasso F, Parrello T, Biancone L, Stella A, Iuliano R, Luzza F, Fusco A, Pallone F. Bioactive IL-18 expression is upregulated in Crohn's disease. J Immunol 163: 143-147, 1999.
40. Nash S, Stafford J, Madara JL. Effects of polymorphonuclear leukocyte transmigration on the barrier function of cultured intestinal epithelial monolayers. J Clin Invest 80: 1104-1113, 1987.
41. Nusrat A, Brown GT, Tom J, Drake A, Bui TT, Quan C, Mrsny RJ. Multiple protein interactions involving proposed extracellular loop domains of the tight junction protein occludin. Mol Biol Cell 16: 1725-1734, 2005.
42. Nusrat A, Parkos CA, Liang TW, Carnes DK, Madara JL. Neutrophil migration across model intestinal epithelia: monolayer disruption and subsequent events in epithelial repair. Gastroenterology 113: 1489-1500, 1997.
43. O'Hara JR, Buret AG. Mechanisms of intestinal tight junctional disruption during infection. Front Biosci 13: 7008-7021, 2008.
44. Parkos CA, Colgan SP, Delp C, Arnaout MA, Madara JL. Neutrophil migration across a cultured epithelial monolayer elicits a biphasic resistance response representing sequential effects on transcellular and paracellular pathways. J Cell Biol 117: 757-764, 1992.
45. Parkos CA, Colgan SP, Madara JL. Interactions of neutrophils with epithelial cells: lessons from the intestine. J Am Soc Nephrol 5: 138-152, 1994.
46. Parsons PE, Sugahara K, Cott GR, Mason RJ, Henson PM. The effect of neutrophil migration and prolonged neutrophil contact on epithelial permeability. Am J Pathol 129: 302-312, 1987.
47. Pierce JW, Schoenleber R, Jesmok G, Best J, Moore SA, Collins T, Gerritsen ME. Novel inhibitors of cytokine-induced I_B_ phosphorylation and endothelial cell adhesion molecule expression show anti-inflammatory effects in vivo. J Biol Chem 272: 21096-21103, 1997.
48. Pizarro TT, Michie MH, Bentz M, Woraratanadharm J, Smith MF Jr, Foley E, Moskaluk CA, Bickston SJ, Cominelli F. IL-18, a novel immunoregulatory cytokine, is up-regulated in Crohn's disease: expression and localization in intestinal mucosal cells. J Immunol 162: 6829-6835, 1999.
49. Prasad S, Mingrino R, Kaukinen K, Hayes KL, Powell RM, Mac-Donald TT, Collins JE. Inflammatory processes have differential effects on claudins 2, 3 and 4 in colonic epithelial cells. Lab Invest 85: 1139-1162, 2005.
50. Reuter BK, Pizarro TT. Role of the IL-18 system and other members of the IL-1R/TLR superfamily in innate mucosal immunity and the pathogenesis of inflammatory bowel disease: friend or foe? Eur J Immunol 34: 2347-2355, 2004.
51. Saitou M, Fujimoto K, Doi Y, Itoh M, Fujimoto T, Furuse M, Takano H, Noda T, Tsukita S. Occludin-deficient embryonic stem cells can differentiate into polarized epithelial cells bearing tight junctions. J Cell Biol 141: 397-408, 1998.
52. Saitou M, Furuse M, Sasaki H, Schulzke JD, Fromm M, Takano H, Noda T, Tsukita S. Complex phenotype of mice lacking occludin, a component of tight junction strands. Mol Biol Cell 11: 4131-4142, 2000.
53. Shen L, Turner JR. Actin depolymerization disrupts tight junctions via caveolae-mediated endocytosis. Mol Biol Cell 16: 3919-3936, 2005.
54. Siegmund B, Fantuzzi G, Rieder F, Gamboni-Robertson F, Lehr HA, Hartmann G, Dinarello CA, Endres S, Eigler A. Neutralization of interleukin-18 reduces severity in murine colitis and intestinal IFN-_ and TNF-_ production. Am J Physiol Regul Integr Comp Physiol 281: R1264-R1273, 2001.
55. Sivakumar PV, Westrich GM, Kanaly S, Garka K, Born TL, Derry JM, Viney JL. Interleukin 18 is a primary mediator of the inflammation associated with dextran sulphate sodium induced colitis: blocking interleukin 18 attenuates intestinal damage. Gut 50: 812-820, 2002.
56. Ten Hove T, Corbaz A, Amitai H, Aloni S, Belzer I, Graber P, Drillenburg P, van Deventer SJ, Chvatchko Y, Te Velde AA. Blockade of endogenous IL-18 ameliorates TNBS-induced colitis by decreasing local TNF-_ production in mice. Gastroenterology 121: 1372-1379, 2001.
57. Turner JR, Rill BK, Carlson SL, Carnes D, Kerner R, Mrsny RJ, Madara JL. Physiological regulation of epithelial tight junctions is associated with myosin light-chain phosphorylation. Am J Physiol Cell Physiol 273: C1378-C1385, 1997.
58. Utech M, Mennigen R, Bruewer M. Endocytosis and recycling of tight junction proteins in inflammation. J Biomed Biotechnol 2010: 484987, 2010.
59. Wirtz S, Becker C, Blumberg R, Galle PR, Neurath MF. Treatment of T cell-dependent experimental colitis in SCID mice by local administration of an adenovirus expressing IL-18 antisense mRNA. J Immunol 168: 411-420, 2002.
60. Wittchen ES, Haskins J, Stevenson BR. Protein interactions at the tight junction. Actin has multiple binding partners, and ZO-1 forms independent complexes with ZO-2 and ZO-3. J Biol Chem 274: 35179-35185, 1999.
61. Wong V, Gumbiner BM. A synthetic peptide corresponding to the extracellular domain of occludin perturbs the tight junction permeability barrier. J Cell Biol 136: 399-409, 1997.
62. Wroblewski LE, Shen L, Ogden S, Romero-Gallo J, Lapierre LA, Israel DA, Turner JR, Peek RM Jr. Helicobacter pylori dysregulation of gastric epithelial tight junctions by urease-mediated myosin II activation. Gastroenterology 136: 236-246, 2009.
63. Yu AS, McCarthy KM, Francis SA, McCormack JM, Lai J, Rogers RA, Lynch RD, Schneeberger EE. Knockdown of occludin expression leads to diverse phenotypic alterations in epithelial cells. Am J Physiol Cell Physiol 288: C1231-C1241, 2005.
64. Zeissig S, Burgel N, Gunzel D, Richter J, Mankertz J, Wahnschaffe U, Kroesen AJ, Zeitz M, Fromm M, Schulzke JD. Changes in expression and distribution of claudin 2, 5 and 8 lead to discontinuous tight junctions and barrier dysfunction in active Crohn's disease. Gut 56: 61-72, 2007.