TNF-α Modulation of Intestinal Tight Junction Permeability Is Mediated by NIK/IKK-α Axis Activation of the Canonical NF-κB Pathway

American Journal of Pathology

Volumn 186, Issue 5, 2016, Pages 1151-1165

  Al Sadi, Rana ^a   Guo, Shuhong ^a   Ye, Dongmei ^a   Rawat, Manmeet ^a   Ma, Thomas Y ^a  

^a UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

I KAPPA B KINASE ALPHA; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTOR RELB; TUMOR NECROSIS FACTOR ALPHA; CARDIAC MYOSIN LIGHT CHAIN KINASE, HUMAN; I KAPPA B KINASE; MAP3K1 PROTEIN, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE 1; MYOSIN LIGHT CHAIN KINASE; RELA PROTEIN, MOUSE; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; GENE ACTIVATION; GENE ACTIVITY; GENE EXPRESSION; MOUSE; NONHUMAN; PERMEABILITY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TIGHT JUNCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; CACO-2 CELL LINE; CELL CULTURE; GENETIC TRANSFECTION; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY; PROMOTER REGION; SMALL INTESTINE;

ANIMALS; CACO-2 CELLS; CELLS, CULTURED; HUMANS; I-KAPPA B KINASE; INTESTINE, SMALL; MAP KINASE KINASE KINASE 1; MAP KINASE SIGNALING SYSTEM; MICE; MYOSIN-LIGHT-CHAIN KINASE; NF-KAPPA B; NF-KAPPA B P50 SUBUNIT; NF-KAPPA B P52 SUBUNIT; PERMEABILITY; PROMOTER REGIONS, GENETIC; RNA, SMALL INTERFERING; TIGHT JUNCTIONS; TRANSCRIPTION FACTOR RELA; TRANSFECTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84964054466     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2015.12.016     Document Type: Article

References (86)

1. D. Hollander Intestinal permeability, leaky gut, and intestinal disorders Curr Gastroenterol Rep 1 1999 410 416
2. T.Y. Ma, and J.M. Anderson Tight junctions and the intestinal barrier Physiology of the Gastrointestinal Tract 2012 Elsevier Academic Press Burlington, MA 1043 1088
3. R. Al-Sadi, M. Boivin, and T. Ma Mechanism of cytokine modulation of epithelial tight junction barrier Front Biosci (Landmark Ed) 14 2009 2765 2778
4. R.M. Al-Sadi, and T.Y. Ma IL-1beta causes an increase in intestinal epithelial tight junction permeability J Immunol 178 2007 4641 4649
5. T.Y. Ma, M.A. Boivin, D. Ye, A. Pedram, and H.M. Said 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 288 2005 G422 G430
6. A. Nusrat, J.R. Turner, and J.L. Madara 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 279 2000 G851 G857
7. R.J. Kennedy, M. Hoper, K. Deodhar, P.J. Erwin, S.J. Kirk, and K.R. Gardiner Interleukin 10-deficient colitis: new similarities to human inflammatory bowel disease Br J Surg 87 2000 1346 1351
8. E. Mazzon, D. Puzzolo, A.P. Caputi, and S. Cuzzocrea Role of IL-10 in hepatocyte tight junction alteration in mouse model of experimental colitis Mol Med 8 2002 353 366
9. M.C. Arrieta, K. Madsen, J. Doyle, and J. Meddings Reducing small intestinal permeability attenuates colitis in the IL10 gene-deficient mouse Gut 58 2009 41 48
10. B.M. Paterson, K.M. Lammers, M.C. Arrieta, A. Fasano, and J.B. Meddings The safety, tolerance, pharmacokinetic and pharmacodynamic effects of single doses of AT-1001 in coeliac disease subjects: a proof of concept study Aliment Pharmacol Ther 26 2007 757 766
11. D. Rittirsch, M.A. Flierl, B.A. Nadeau, D.E. Day, M.S. Huber-Lang, J.J. Grailer, F.S. Zetoune, A.V. Andjelkovic, A. Fasano, and P.A. Ward Zonulin as prehaptoglobin2 regulates lung permeability and activates the complement system Am J Physiol Lung Cell Mol Physiol 304 2013 L863 L872
12. Y. Feng, and D.H. Teitelbaum Tumour necrosis factor - induced loss of intestinal barrier function requires TNFR1 and TNFR2 signaling in a mouse model of total parenteral nutrition J Physiol 591 2013 3709 3723
13. D. Hollander Crohn's disease, TNF-alpha, and the leaky gut. The chicken or the egg? Am J Gastroenterol 97 2002 1867 1868
14. I. Kirman, R.L. Whelan, and O.H. Nielsen Infliximab: mechanism of action beyond TNF-alpha neutralization in inflammatory bowel disease Eur J Gastroenterol Hepatol 16 2004 639 641
15. A. Shetty, and A. Forbes Pharmacogenomics of response to anti-tumor necrosis factor therapy in patients with Crohn's disease Am J Pharmacogenomics 2 2002 215 221
16. R. Al-Sadi, S. Guo, D. Ye, and T.Y. Ma TNF-alpha modulation of intestinal epithelial tight junction barrier is regulated by ERK1/2 activation of Elk-1 Am J Pathol 183 2013 1871 1884
17. T.Y. Ma, G.K. Iwamoto, N.T. Hoa, V. Akotia, A. Pedram, M.A. Boivin, and H.M. Said TNF-alpha-induced increase in intestinal epithelial tight junction permeability requires NF-kappa B activation Am J Physiol Gastrointest Liver Physiol 286 2004 G367 G376
18. G. Schulze-Tanzil, O. Al-Sadi, E. Wiegand, W. Ertel, C. Busch, B. Kohl, and T. Pufe The role of pro-inflammatory and immunoregulatory cytokines in tendon healing and rupture: new insights Scand J Med Sci Sports 21 2011 337 351
19. D. Ye, S. Guo, R. Al-Sadi, and T.Y. Ma MicroRNA regulation of intestinal epithelial tight junction permeability Gastroenterology 141 2011 1323 1333
20. P. Suenaert, V. Bulteel, L. Lemmens, M. Noman, B. Geypens, G. Van Assche, K. Geboes, J.L. Ceuppens, and P. Rutgeerts Anti-tumor necrosis factor treatment restores the gut barrier in Crohn's disease Am J Gastroenterol 97 2002 2000 2004
21. W.J. Sandborn Clinical perspectives in Crohn's disease. Moving forward with anti-TNF-alpha therapy: current needs and future treatments Rev Gastroenterol Disord 7 Suppl 2 2007 S23 S35
22. M.M. Lawson, A.G. Thomas, and A.K. Akobeng Tumour necrosis factor alpha blocking agents for induction of remission in ulcerative colitis Cochrane Database Syst Rev 2006 CD005112
23. D. Ye, I. Ma, and T.Y. Ma Molecular mechanism of tumor necrosis factor-alpha modulation of intestinal epithelial tight junction barrier Am J Physiol Gastrointest Liver Physiol 290 2006 G496 G504
24. M. Karin, and E. Gallagher TNFR signaling: ubiquitin-conjugated TRAFfic signals control stop-and-go for MAPK signaling complexes Immunol Rev 228 2009 225 240
25. N.L. Malinin, M.P. Boldin, A.V. Kovalenko, and D. Wallach MAP3K-related kinase involved in NF-kappaB induction by TNF, CD95 and IL-1 Nature 385 1997 540 544
26. S. Nemoto, J.A. DiDonato, and A. Lin Coordinate regulation of IkappaB kinases by mitogen-activated protein kinase kinase kinase 1 and NF-kappaB-inducing kinase Mol Cell Biol 18 1998 7336 7343
27. H. Li, and X. Lin Positive and negative signaling components involved in TNFalpha-induced NF-kappaB activation Cytokine 41 2008 1 8
28. J.Y. Kim, M. Morgan, D.G. Kim, J.Y. Lee, L. Bai, Y. Lin, Z.G. Liu, and Y.S. Kim TNFalpha induced noncanonical NF-kappaB activation is attenuated by RIP1 through stabilization of TRAF2 J Cell Sci 124 2011 647 656
29. B. Zarnegar, S. Yamazaki, J.Q. He, and G. Cheng Control of canonical NF-kappaB activation through the NIK-IKK complex pathway Proc Natl Acad Sci U S A 105 2008 3503 3508
30. P. Ramakrishnan, W. Wang, and D. Wallach Receptor-specific signaling for both the alternative and the canonical NF-kappaB activation pathways by NF-kappaB-inducing kinase Immunity 21 2004 477 489
31. A.S. Baldwin Jr. The NF-kappa B and I kappa B proteins: new discoveries and insights Annu Rev Immunol 14 1996 649 683
32. J.L. Pomerantz, and D. Baltimore Two pathways to NF-kappaB Mol Cell 10 2002 693 695
33. R.E. Simmonds, and B.M. Foxwell Signalling, inflammation and arthritis: NF-kappaB and its relevance to arthritis and inflammation Rheumatology (Oxford) 47 2008 584 590
34. D. Widera, I. Mikenberg, M. Elvers, C. Kaltschmidt, and B. Kaltschmidt Tumor necrosis factor alpha triggers proliferation of adult neural stem cells via IKK/NF-kappaB signaling BMC Neurosci 7 2006 64
35. S.C. Sun The noncanonical NF-kappaB pathway Immunol Rev 246 2012 125 140
36. R. Al-Sadi, D. Ye, H.M. Said, and T.Y. Ma IL-1beta-induced increase in intestinal epithelial tight junction permeability is mediated by MEKK-1 activation of canonical NF-kappaB pathway Am J Pathol 177 2010 2310 2322
37. R. Al-Sadi, D. Ye, K. Dokladny, and T.Y. Ma Mechanism of IL-1beta-induced increase in intestinal epithelial tight junction permeability J Immunol 180 2008 5653 5661
38. B.R. Achyut, A. Srivastava, S. Bhattacharya, and B. Mittal Genetic association of interleukin-1beta (-511C/T) and interleukin-1 receptor antagonist (86 bp repeat) polymorphisms with Type 2 diabetes mellitus in North Indians Clin Chim Acta 377 2007 163 169
39. R. Al-Sadi, S. Guo, K. Dokladny, M.A. Smith, D. Ye, A. Kaza, D.M. Watterson, and T.Y. Ma Mechanism of interleukin-1beta induced-increase in mouse intestinal permeability in vivo J Interferon Cytokine Res 32 2012 474 484
40. R. Al-Sadi, S. Guo, D. Ye, K. Dokladny, T. Alhmoud, L. Ereifej, H.M. Said, and T.Y. Ma Mechanism of IL-1beta modulation of intestinal epithelial barrier involves p38 kinase and activating transcription factor-2 activation J Immunol 190 2013 6596 6606
41. R. Al-Sadi, K. Khatib, S. Guo, D. Ye, M. Youssef, and T. Ma Occludin regulates macromolecule flux across the intestinal epithelial tight junction barrier Am J Physiol Gastrointest Liver Physiol 300 2011 G1054 G1064
42. D. Ye, and T.Y. Ma Cellular and molecular mechanisms that mediate basal and tumour necrosis factor-alpha-induced regulation of myosin light chain kinase gene activity J Cell Mol Med 12 2008 1331 1346
43. M.H. Holtmann, and M.F. Neurath Anti-TNF strategies in stenosing and fistulizing Crohn's disease Int J Colorectal Dis 20 2005 1 8
44. L. Dinesen, and S. Travis Targeting nanomedicines in the treatment of Crohn's disease: focus on certolizumab pegol (CDP870) Int J Nanomedicine 2 2007 39 47
45. G. Lapadula, A. Marchesoni, A. Armuzzi, C. Blandizzi, R. Caporali, S. Chimenti, R. Cimaz, L. Cimino, P. Gionchetti, G. Girolomoni, P. Lionetti, A. Marcellusi, F.S. Mennini, and C. Salvarani Adalimumab in the treatment of immune-mediated diseases Int J Immunopathol Pharmacol 27 2014 33 48
46. H. Nakano, M. Shindo, S. Sakon, S. Nishinaka, M. Mihara, H. Yagita, and K. Okumura Differential regulation of IkappaB kinase alpha and beta by two upstream kinases, NF-kappaB-inducing kinase and mitogen-activated protein kinase/ERK kinase kinase-1 Proc Natl Acad Sci U S A 95 1998 3537 3542
47. T. Lernbecher, U. Muller, and T. Wirth Distinct NF-kappa B/Rel transcription factors are responsible for tissue-specific and inducible gene activation Nature 365 1993 767 770
48. C.S. Duckett, N.D. Perkins, T.F. Kowalik, R.M. Schmid, E.S. Huang, A.S. Baldwin Jr., and G.J. Nabel Dimerization of NF-KB2 with RelA(p65) regulates DNA binding, transcriptional activation, and inhibition by an I kappa B-alpha (MAD-3) Mol Cell Biol 13 1993 1315 1322
49. A.R. Brasier The NF-kappaB regulatory network Cardiovasc Toxicol 6 2006 111 130
50. A. Israel The IKK complex, a central regulator of NF-kappaB activation Cold Spring Harb Perspect Biol 2 2010 a000158
51. S.C. Sun, and S.C. Ley New insights into NF-kappaB regulation and function Trends Immunol 29 2008 469 478
52. A.P. Grech, M. Amesbury, T. Chan, S. Gardam, A. Basten, and R. Brink TRAF2 differentially regulates the canonical and noncanonical pathways of NF-kappaB activation in mature B cells Immunity 21 2004 629 642
53. S.J. de Jong, J.C. Albrecht, M. Schmidt, I. Muller-Fleckenstein, and B. Biesinger Activation of noncanonical NF-kappaB signaling by the oncoprotein Tio J Biol Chem 285 2010 16495 16503
54. J.C. Lo, S. Basak, E.S. James, R.S. Quiambo, M.C. Kinsella, M.L. Alegre, F. Weih, G. Franzoso, A. Hoffmann, and Y.X. Fu Coordination between NF-kappaB family members p50 and p52 is essential for mediating LTbetaR signals in the development and organization of secondary lymphoid tissues Blood 107 2006 1048 1055
55. Z.B. Yilmaz, D.S. Weih, V. Sivakumar, and F. Weih RelB is required for Peyer's patch development: differential regulation of p52-RelB by lymphotoxin and TNF EMBO J 22 2003 121 130
56. F.S. Lee, R.T. Peters, L.C. Dang, and T. Maniatis MEKK1 activates both IkappaB kinase alpha and IkappaB kinase beta Proc Natl Acad Sci U S A 95 1998 9319 9324
57. Q. Zhao, and F.S. Lee Mitogen-activated protein kinase/ERK kinase kinases 2 and 3 activate nuclear factor-kappaB through IkappaB kinase-alpha and IkappaB kinase-beta J Biol Chem 274 1999 8355 8358
58. X. Li, P.E. Massa, A. Hanidu, G.W. Peet, P. Aro, A. Savitt, S. Mische, J. Li, and K.B. Marcu IKKalpha, IKKbeta, and NEMO/IKKgamma are each required for the NF-kappa B-mediated inflammatory response program J Biol Chem 277 2002 45129 45140
59. D.M. Rothwarf, E. Zandi, G. Natoli, and M. Karin IKK-gamma is an essential regulatory subunit of the IkappaB kinase complex Nature 395 1998 297 300
60. H.J. Dyson, and E.A. Komives Role of disorder in IkappaB-NFkappaB interaction IUBMB Life 64 2012 499 505
61. M.L. Scott, T. Fujita, H.C. Liou, G.P. Nolan, and D. Baltimore The p65 subunit of NF-kappa B regulates I kappa B by two distinct mechanisms Genes Dev 7 1993 1266 1276
62. P.B. Shambharkar, M. Blonska, B.P. Pappu, H. Li, Y. You, H. Sakurai, B.G. Darnay, H. Hara, J. Penninger, and X. Lin Phosphorylation and ubiquitination of the IkappaB kinase complex by two distinct signaling pathways EMBO J 26 2007 1794 1805
63. H. Suzuki, T. Chiba, M. Kobayashi, M. Takeuchi, K. Furuichi, and K. Tanaka In vivo and in vitro recruitment of an IkappaBalpha-ubiquitin ligase to IkappaBalpha phosphorylated by IKK, leading to ubiquitination Biochem Biophys Res Commun 256 1999 121 126
64. F. Mercurio, B.W. Murray, A. Shevchenko, B.L. Bennett, D.B. Young, J.W. Li, G. Pascual, A. Motiwala, H. Zhu, M. Mann, and A.M. Manning IkappaB kinase (IKK)-associated protein 1, a common component of the heterogeneous IKK complex Mol Cell Biol 19 1999 1526 1538
65. F. Mercurio, H. Zhu, B.W. Murray, A. Shevchenko, B.L. Bennett, J. Li, D.B. Young, M. Barbosa, M. Mann, A. Manning, and A. Rao IKK-1 and IKK-2: cytokine-activated IkappaB kinases essential for NF-kappaB activation Science 278 1997 860 866
66. N. Kanarek, and Y. Ben-Neriah Regulation of NF-kappaB by ubiquitination and degradation of the IkappaBs Immunol Rev 246 2012 77 94
67. Z.J. Chen Ubiquitin signalling in the NF-kappaB pathway Nat Cell Biol 7 2005 758 765
68. T. Maruyama, H. Fukushima, K. Nakao, M. Shin, H. Yasuda, F. Weih, T. Doi, K. Aoki, N. Alles, K. Ohya, R. Hosokawa, and E. Jimi Processing of the NF-kappa B2 precursor p100 to p52 is critical for RANKL-induced osteoclast differentiation J Bone Miner Res 25 2010 1058 1067
69. R.E. Amir, H. Haecker, M. Karin, and A. Ciechanover Mechanism of processing of the NF-kappa B2 p100 precursor: identification of the specific polyubiquitin chain-anchoring lysine residue and analysis of the role of NEDD8-modification on the SCF(beta-TrCP) ubiquitin ligase Oncogene 23 2004 2540 2547
70. R. Al-Sadi, D. Ye, H.M. Said, and T.Y. Ma Cellular and molecular mechanism of interleukin-1beta modulation of Caco-2 intestinal epithelial tight junction barrier J Cell Mol Med 15 2011 970 982
71. T.Y. Ma, D. Nguyen, V. Bui, H. Nguyen, and N. Hoa Ethanol modulation of intestinal epithelial tight junction barrier Am J Physiol 276 1999 G965 G974
72. K. Suzuki, and K. Takahashi Actin filament assembly and actin-myosin contractility are necessary for anchorage- and EGF-dependent activation of phospholipase Cgamma J Cell Physiol 189 2001 64 71
73. T.Y. Ma, D. Tran, N. Hoa, D. Nguyen, M. Merryfield, and A. Tarnawski Mechanism of extracellular calcium regulation of intestinal epithelial tight junction permeability: role of cytoskeletal involvement Microsc Res Tech 51 2000 156 168
74. S.A. Blair, S.V. Kane, D.R. Clayburgh, and J.R. Turner Epithelial myosin light chain kinase expression and activity are upregulated in inflammatory bowel disease Lab Invest 86 2006 191 201
75. D.R. Clayburgh, S. Rosen, E.D. Witkowski, F. Wang, S. Blair, S. Dudek, J.G. Garcia, J.C. Alverdy, and J.R. Turner A differentiation-dependent splice variant of myosin light chain kinase, MLCK1, regulates epithelial tight junction permeability J Biol Chem 279 2004 55506 55513
76. M. Suzuki, T. Nagaishi, M. Yamazaki, M. Onizawa, T. Watabe, Y. Sakamaki, S. Ichinose, M. Totsuka, S. Oshima, R. Okamoto, M. Shimonaka, H. Yagita, T. Nakamura, and M. Watanabe Myosin light chain kinase expression induced via tumor necrosis factor receptor 2 signaling in the epithelial cells regulates the development of colitis-associated carcinogenesis PLoS One 9 2014 e88369
77. M. Utech, A.I. Ivanov, S.N. Samarin, M. Bruewer, J.R. Turner, R.J. Mrsny, C.A. Parkos, and A. Nusrat Mechanism of IFN-gamma-induced endocytosis of tight junction proteins: myosin II-dependent vacuolarization of the apical plasma membrane Mol Biol Cell 16 2005 5040 5052
78. M. Adli, E. Merkhofer, P. Cogswell, and A.S. Baldwin IKKalpha and IKKbeta each function to regulate NF-kappaB activation in the TNF-induced/canonical pathway PLoS One 5 2010 e9428
79. J.A. DiDonato IKK alpha on center stage Sci STKE 2001 2001 pe1
80. E. Mathes, E.L. O'Dea, A. Hoffmann, and G. Ghosh NF-kappaB dictates the degradation pathway of IkappaBalpha EMBO J 27 2008 1357 1367
81. F.S. Zetoune, A.R. Murthy, Z. Shao, T. Hlaing, M.G. Zeidler, Y. Li, and C. Vincenz A20 inhibits NF-kappa B activation downstream of multiple Map3 kinases and interacts with the I kappa B signalosome Cytokine 15 2001 282 298
82. J.H. Je, J.Y. Lee, K.J. Jung, B. Sung, E.K. Go, B.P. Yu, and H.Y. Chung NF-kappaB activation mechanism of 4-hydroxyhexenal via NIK/IKK and p38 MAPK pathway FEBS Lett 566 2004 183 189
83. X. Jiang, N. Takahashi, K. Ando, T. Otsuka, T. Tetsuka, and T. Okamoto NF-kappa B p65 transactivation domain is involved in the NF-kappa B-inducing kinase pathway Biochem Biophys Res Commun 301 2003 583 590
84. Q. Wang, R. Dziarski, C.J. Kirschning, M. Muzio, and D. Gupta Micrococci and peptidoglycan activate TLR2 - >MyD88 - >IRAK - >TRAF - >NIK - >IKK - >NF-kappaB signal transduction pathway that induces transcription of interleukin-8 Infect Immun 69 2001 2270 2276
85. C. Schmidt, B. Peng, Z. Li, G.M. Sclabas, S. Fujioka, J. Niu, M. Schmidt-Supprian, D.B. Evans, J.L. Abbruzzese, and P.J. Chiao Mechanisms of proinflammatory cytokine-induced biphasic NF-kappaB activation Mol Cell 12 2003 1287 1300
86. Y. Xia, S. Chen, Y. Wang, N. Mackman, G. Ku, D. Lo, and L. Feng RelB modulation of IkappaBalpha stability as a mechanism of transcription suppression of interleukin-1alpha (IL-1alpha), IL-1beta, and tumor necrosis factor alpha in fibroblasts Mol Cell Biol 19 1999 7688 7696