Epithelial NF-κB enhances transmucosal fluid movement by altering tight junction protein composition after T cell activation

American Journal of Pathology

Volumn 176, Issue 1, 2010, Pages 158-167

  Tang, Yueming ^a   Clayburgh, Daniel R ^b   Mittal, Navdha ^a   Goretsky, Tatiana ^a   Dirisina, Ramanarao ^a   Zhang, Zheng ^a   Kron, Michelle ^a   Ivancic, David ^a   Katzman, Rebecca B ^a   Grimm, Gery ^a   Lee, Goo ^a   Fryer, Jonathan ^a   Nusrat, Asma ^c   Turner, Jerrold R ^b   Barrett, Terrence A ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALEXA; BOVINE SERUM ALBUMIN; CLAUDIN 1; DEXTRAN; FLUORESCENT DYE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MONOCLONAL ANTIBODY CD3; OCCLUDIN; PROTEIN ZO1; REPRESSOR PROTEIN; UNCLASSIFIED DRUG; I KAPPA B; MEMBRANE PROTEIN; NF KAPPAB INHIBITOR ALPHA; NF-KAPPAB INHIBITOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; DIARRHEA; ENZYME ACTIVATION; FLUID SHIFT; IMAGING; IMMUNOBLOTTING; IMMUNOCOMPETENT CELL; IN VIVO STUDY; INTERNALIZATION; INTRACELLULAR SPACE; MOLECULAR PROBE; MOUSE; NONHUMAN; PERFUSION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; TIGHT JUNCTION; TRANSGENIC MOUSE; WILD TYPE; ANIMAL; ANTIBODY SPECIFICITY; EPITHELIUM CELL; FLOW KINETICS; GENETICS; HUMAN; IMMUNOLOGY; INTESTINE; LYMPHOCYTE ACTIVATION; MACROMOLECULE; METABOLISM; MUCOSA; MUTATION; PATHOLOGY; PERMEABILITY; T LYMPHOCYTE;

ANIMALS; DIARRHEA; EPITHELIAL CELLS; HUMANS; I-KAPPA B PROTEINS; INTESTINES; LYMPHOCYTE ACTIVATION; MACROMOLECULAR SUBSTANCES; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; MUCOUS MEMBRANE; MUTATION; NF-KAPPA B; ORGAN SPECIFICITY; PERMEABILITY; RHEOLOGY; T-LYMPHOCYTES; TIGHT JUNCTIONS;

EID: 73949105149     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.090548     Document Type: Article

References (59)

1. Atreya I, Atreya R, Neurath MF: NF-kappaB in inflammatory bowel disease. J Intern Med 2008, 263:591-596
2. Podolsky DK: Inflammatory bowel disease. N Engl J Med 2002, 347:417-429
3. Clayburgh DR, Shen L, Turner JR: A porous defense: the leaky epithelial barrier in intestinal disease. Lab Invest 2004, 84:282-291
4. 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 1997, 273:C1378-C1385
5. Nusrat A, Parkos CA, Verkade P, Foley CS, Liang TW, Innis-Whitehouse W, Eastburn KK, Madara JL: Tight junctions are membrane microdomains. J Cell Sci 2000, 113 (Pt 10):1771-1781
6. Nusrat A, Turner JR, Madara JL: Molecular physiology and pathophysiology of tight junctions. IV Regulation of tight junctions by extracellular stimuli: nutrients, cytokines, and immune cells. Am J Physiol Gastrointest Liver Physiol 2000, 279:G851-G857
7. Macdonald TT, Monteleone G: Immunity, inflammation, and allergy in the gut. Science 2005, 307:1920-1925
8. 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
9. Ivanov AI, Nusrat A, Parkos CA: Endocytosis of the apical junctional complex: mechanisms and possible roles in regulation of epithelial barriers. Bioessays 2005, 27:356-365
10. Utech M, Ivanov AI, Samarin SN, Bruewer M, Turner JR, Mrsny RJ, Parkos CA, Nusrat A: Mechanism of IFN-gamma-induced endocytosis of tight junction proteins: myosin II-dependent vacuolarization of the apical plasma membrane. Mol Biol Cell 2005, 16:5040-5052
11. Shen L, Turner JR: Actin depolymerization disrupts tight junctions via caveolae-mediated endocytosis. Mol Biol Cell 2005, 16:3919-3936
12. 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
13. Chiba H, Kojima T, Osanai M, Sawada N: The significance of interferon-gamma-triggered internalization of tight-junction proteins in inflammatory bowel disease. Sci STKE 2006, 2006:pe1
14. Musch MW, Clarke LL, Mamah D, Gawenis LR, Zhang Z, Ellsworth W, Shalowitz D, Mittal N, Efthimiou P, Alnadjim Z, Hurst SD, Chang EB, Barrett TA: T cell activation causes diarrhea by increasing intestinal permeability and inhibiting epithelial Na+/K+-ATPase. J Clin Invest 2002, 110:1739-1747
15. Hollander D: Crohn's disease-a permeability disorder of the tight junction? Gut 1988, 29:1621-1624
16. Katz KD, Hollander D, Vadheim CM, McElree C, Delahunty T, Dadufalza VD, Krugliak P, Rotter JI: Intestinal permeability in patients with Crohn's disease and their healthy relatives. Gastroenterology 1989, 97:927-931
17. 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
18. Jobin C, Sartor RB: The I kappa B/NF-kappa B system: a key determinant of mucosalinflammation and protection. Am J Physiol Cell Physiol 2000, 278:C451-C462
19. Boivin MA, Roy PK, Bradley A, Kennedy JC, Rihani T, Ma TY: Mechanism of interferon-gamma-induced increase in T84 intestinal epithelial tight junction. J Interferon Cytokine Res 2009, 29:45-54
20. Al-Sadi R, Boivin M, Ma T: Mechanism of cytokine modulation of epithelial tight junction barrier. Front Biosci 2009, 14:2765-2778
21. Rogler G, Brand K, Vogl D, Page S, Hofmeister R, Andus T, Knuechel R, Baeuerle PA, Scholmerich J, Gross V: Nuclear factor kappaB is activated in macrophages and epithelial cells of inflamed intestinal mucosa. Gastroenterology 1998, 115:357-369
22. Shishodia S, Aggarwal BB: Nuclear factor-kappaB activation: a question of life or death. J Biochem Mol Biol 2002, 35:28-40
23. Schottelius AJ, Dinter H: Cytokines. NF-kappaB, microenvironment, intestinal inflammation and cancer. Cancer Treat Res 2006, 130:67-87
24. Kimura K, Teranishi S, Fukuda K, Kawamoto K, Nishida T: Delayed disruption of barrier function in cultured human corneal epithelial cells induced by tumor necrosis factor-alpha in a manner dependent on NF-kappaB. Invest Ophthalmol Vis Sci 2008, 49:565-571
25. Greten FR, Eckmann L, Greten TF, Park JM, Li ZW, Egan LJ, Kagnoff MF, Karin M: IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 2004, 118:285-296
26. Saam JR, Gordon JI: Inducible gene knockouts in the small intestinal and colonic epithelium. J Biol Chem 1999, 274:38071-38082
27. Voll RE, Jimi E, Phillips RJ, Barber DF, Rincon M, Hayday AC, Flavell RA, Ghosh S: NF-kappa B activation by the pre-T cell receptor serves as a selective survival signal in T lymphocyte development. Immunity 2000, 13:677-689
28. 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
29. Merger M, Viney JL, Borojevic R, Steele-Norwood D, Zhou P, Clark DA, Riddell R, Maric R, Podack ER, Croitoru K: Defining the roles of perforin. Fas/FasL, and tumour necrosis factor alpha in T cell induced mucosal damage in the mouse intestine. Gut 2002, 51:155-163
30. Radojevic N, McKay DM, Merger M, Vallance BA, Collins SM, Croitoru K: Characterization of enteric functional changes evoked by in vivo anti-CD3 T cell activation. Am J Physiol 1999, 276:R715-R723
31. Gossen M, Freundlieb S, Bender G, Muller G, Hillen W, Bujard H: Transcriptional activation by tetracyclines in mammalian cells. Science 1995, 268:1766-1769
32. He XC, Zhang J, Tong WG, Tawfik O, Ross J, Scoville DH, Tian Q, Zeng X, He X, Wiedemann LM, Mishina Y, Li L: BMP signaling inhibits intestinal stem cell self-renewal through suppression of Wnt-betacatenin signaling. Nat Genet 2004, 36:1117-1121
33. Janssen YM, Sen CK: Nuclear factor kappa B activity in response to oxidants and antioxidants. Methods Enzymol 1999, 300:363-374
34. Stappenbeck TS, Hooper LV, Manchester JK, Wong MH, Gordon JI: Laser capture microdissection of mouse intestine: characterizing mRNA and protein expression, and profiling intermediary metabolism in specified cell populations. Methods Enzymol 2002, 356:167-196
35. Zhang Z, Kaptanoglu L, Tang Y, Ivancic D, Rao SM, Luster A, Barrett TA, Fryer J: IP-10-induced recruitment of CXCR3 host T cells is required for small bowel allograft rejection. Gastroenterology 2004, 126:809-818
36. Sadowski DC, Meddings JB: Luminal nutrients alter tight-junction permeability in the rat jejunum: an in vivo perfusion model. Can J Physiol Pharmacol 1993, 71:835-839
37. Fihn BM, Sjoqvist A, Jodal M: Permeability of the rat small intestinal epithelium along the villus-crypt axis: effects of glucose transport. Gastroenterology 2000, 119:1029-1036
38. Grossmann J, Maxson JM, Whitacre CM, Orosz DE, Berger NA, Fiocchi C, Levine AD: New isolation technique to study apoptosis in human intestinal epithelial cells. Am J Pathol 1998, 153:53-62
39. Pajari AM, Rajakangas J, Paivarinta E, Kosma VM, Rafter J, Mutanen M: Promotion of intestinal tumor formation by inulin is associated with an accumulation of cytosolic beta-catenin in Min mice. Int J Cancer 2003, 106:653-660
40. Berglund JJ, Riegler M, Zolotarevsky Y, Wenzl E, Turner JR: Regulation of human jejunal transmucosal resistance and MLC phosphorylation by Na(+)-glucose cotransport. Am J Physiol Gastrointest Liver Physiol 2001, 281:G1487-G1493
41. Clayburgh DR, Rosen S, Witkowski ED, Wang F, Blair S, Dudek S, Garcia JG, Alverdy JC, Turner JR: A differentiation-dependent splice variant of myosin light chain kinase. MLCK1, regulates epithelial tight junction permeability. J Biol Chem 2004, 279:55506-55513
42. 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
43. 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
44. Chiba H, Osanai M, Murata M, Kojima T, Sawada N: Transmembrane proteins of tight junctions. Biochim Biophys Acta 2008, 1778:588-600
45. Perreault N, Beaulieu JF: Primary cultures of fully differentiated and pure human intestinal epithelial cells. Exp Cell Res 1998, 245:34-42
46. Jobin C, Morteau O, Han DS, Balfour Sartor R: Specific NF-kappaB blockade selectively inhibits tumour necrosis factor-alpha-induced COX-2 but not constitutive COX-1 gene expression in HT-29 cells. Immunology 1998, 95:537-543
47. Jobin C, Panja A, Hellerbrand C, Iimuro Y, Didonato J, Brenner DA, Sartor RB: Inhibition of proinflammatory molecule production by adenovirus-mediated expression of a nuclear factor kappaB super-repressor in human intestinal epithelial cells. J Immunol 1998, 160:410-418
48. Braegger CP, Nicholls S, Murch SH, Stephens S, MacDonald TT: Tumour necrosis factor alpha in stool as a marker of intestinal inflammation. Lancet 1992, 339:89-91
49. Murch SH, Braegger CP, Walker-Smith JA, MacDonald TT: Location of tumour necrosis factor alpha by immunohistochemistry in chronic inflammatory bowel disease. Gut 1993, 34:1705-1709
50. Van Deventer SJ: Tumour necrosis factor and Crohn's disease. Gut 1997, 40:443-448
51. Ricart E, Panaccione R, Loftus EV, Tremaine WJ, Sandborn WJ: Infliximab for Crohn's disease in clinical practice at the Mayo Clinic: the first 100 patients. Am J Gastroenterol 2001, 96:722-729
52. Bruewer M, Luegering A, Kucharzik T, Parkos CA, Madara JL, Hopkins AM, Nusrat A: Proinflammatory cytokines disrupt epithelial barrier function by apoptosis-independent mechanisms. J Immunol 2003, 171:6164 -6172
53. Ye D, Ma I, Ma TY: Molecular mechanism of tumor necrosis factoralpha modulation of intestinal epithelial tight junction barrier. Am J Physiol Gastrointest Liver Physiol 2006, 290:G496-G504
54. Peterson MD, Mooseker MS: Characterization of the enterocyte-like brush border cytoskeleton of the C2BBe clones of the human intestinal cell line Caco-2. J Cell Sci 1992, 102 (Pt 3):581-600
55. Graham WV, Wang F, Clayburgh DR, Cheng JX, Yoon B, Wang Y, Lin A, Turner JR: Tumor necrosis factor-induced long myosin light chain kinase transcription is regulated by differentiation-dependent signaling events. Characterization of the human long myosin light chain kinase promoter. J Biol Chem 2006, 281:26205-26215
56. Baldwin DN, Vanchinathan V, Brown PO, Theriot JA: A gene-expression program reflecting the innate immune response of cultured intestinal epithelial cells to infection by Listeria monocytogenes. Genome Biol 2003, 4:R2
57. Brown RC, Mark KS, Egleton RD, Huber JD, Burroughs AR, Davis TP: Protection against hypoxia-induced increase in blood-brain barrier permeability: role of tight junction proteins and NFkappaB. J Cell Sci 2003, 116:693-700
58. Nenci A, Becker C, Wullaert A, Gareus R, van Loo G, Danese S, Huth M, Nikolaev A, Neufert C, Madison B, Gumucio D, Neurath MF, Pasparakis M: Epithelial NEMO links innate immunity to chronic intestinal inflammation. Nature 2007, 446:557-561
59. Zaph C, Troy AE, Taylor BC, Berman-Booty LD, Guild KJ, Du Y, Yost EA, Gruber AD, May MJ, Greten FR, Eckmann L, Karin M, Artis D: Epithelial-cell- intrinsic IKK-beta expression regulates intestinal immune homeostasis. Nature 2007, 446:552-556