Entamoeba histolytica exacerbates epithelial tight junction permeability and proinflammatory responses in Muc2-/- mice

American Journal of Pathology

Volumn 182, Issue 3, 2013, Pages 852-865

  Kissoon Singh, Vanessa ^a   Moreau, France ^a   Trusevych, Elizabeth ^a   Chadee, Kris ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CLAUDIN 2; CYSTEINE PROTEINASE; GAMMA INTERFERON; INTERLEUKIN 13; MUCIN 2; OCCLUDIN; PROTEIN ZO1; SERUM ALBUMIN; TIGHT JUNCTION PROTEIN; TUMOR NECROSIS FACTOR ALPHA; VIRULENCE FACTOR;

AMOEBOZOA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CYTOKINE RELEASE; DISEASE EXACERBATION; ENTAMOEBA HISTOLYTICA; EPITHELIUM; EXUDATE; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INFECTION SENSITIVITY; INFLAMMATION; INNATE IMMUNITY; MEMBRANE PERMEABILITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; TIGHT JUNCTION;

ANIMALS; BLOOD CELLS; COLON; ENTAMOEBA HISTOLYTICA; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; GOBLET CELLS; HUMANS; INFLAMMATION MEDIATORS; INTESTINES; MICE; MICE, INBRED C57BL; MUCIN-2; PERMEABILITY; TIGHT JUNCTION PROTEINS; TIGHT JUNCTIONS; VIRULENCE FACTORS;

EID: 84874512496     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2012.11.035     Document Type: Article

References (48)

1. D. Moncada, and K. Chadee Production, structure, and function of gastrointestinal mucins. Infections of the gastrointestinal tract M.J. Blaser, R.L. Guerrant, P.D. Smith, J.I. Ravdin, H.B. Greenberg, ed 2 2002 Lippincott Williams & Wilkins Philadelphia 57 79
2. M.E. Johansson, M. Phillipson, J. Petersson, A. Velcich, L. Holm, and G.C. Hansson The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria Proc Natl Acad Sci USA 105 2008 15064 15069
3. H. Kindon, C. Pothoulakis, L. Thim, K. Lynch-Devaney, and D.K. Podolsky Trefoil peptide protection of intestinal epithelial barrier function: cooperative interaction with mucin glycoprotein Gastroenterology 109 1995 516 523
4. S.N. Nie, X.M. Qian, X.H. Wu, S.Y. Yang, W.J. Tang, B.H. Xu, F. Huang, X. Lin, D.Y. Sun, H.C. Sun, and Z.S. Li Role of TFF in healing of stress-induced gastric lesions World J Gastroenterol 9 2003 1772 1776
5. P. Dharmani, V. Srivastava, V. Kissoon-Singh, and K. Chadee Role of intestinal mucins in innate host defense mechanisms against pathogens J Innate Immun 1 2009 123 135
6. V. Strugala, P.W. Dettmar, and J.P. Pearson Thickness and continuity of the adherent colonic mucus barrier in active and quiescent ulcerative colitis and Crohn's disease Int J Clin Pract 62 2008 762 769
7. A. Velcich, W. Yang, J. Heyer, A. Fragale, C. Nicholas, S. Viani, R. Kucherlapati, M. Lipkin, K. Yang, and L. Augenlicht Colorectal cancer in mice genetically deficient in the mucin Muc2 Science 295 2002 1726 1729
8. V. Kissoon-Singh, L. Mortimer, and K. Chadee Entamoeba histolytica cathepsin-like enzymes: interactions with the host gut Adv Exp Med Biol 712 2011 62 83
9. Amoebiasis Wkly Epidemiol Rec 72 1997 97 100
10. A. Belley, and K. Chadee Prostaglandin E(2) stimulates rat and human colonic mucin exocytosis via the EP(4) receptor Gastroenterology 117 1999 1352 1362
11. P. Dharmani, P. Leung, and K. Chadee Tumor necrosis factor-alpha and Muc2 mucin play major roles in disease onset and progression in dextran sodium sulphate-induced colitis PLoS One 6 2011 e25058
12. M.U. Göttke, K. Keller, A. Belley, R.M. Garcia, M.A. Hollingsworth, D.R. Mack, and K. Chadee Functional heterogeneity of colonic adenocarcinoma mucins for inhibition of Entamoeba histolytica adherence to target cells J Eukaryot Microbiol 45 1998 17S 23S
13. C. Caballero-Franco, K. Keller, C. De Simone, and K. Chadee The VSL#3 probiotic formula induces mucin gene expression and secretion in colonic epithelial cells Am J Physiol Gastrointest Liver Physiol 292 2007 G315 G322
14. A. Belley, K. Keller, J. Grove, and K. Chadee Interaction of LS174T human colon cancer cell mucins with Entamoeba histolytica: an in vitro model for colonic disease Gastroenterology 111 1996 1484 1492
15. Y. Naito, K. Katada, T. Takagi, H. Tsuboi, M. Kuroda, O. Handa, S. Kokura, N. Yoshida, H. Ichikawa, and T. Yoshikawa Rosuvastatin reduces rat intestinal ischemia-reperfusion injury associated with the preservation of endothelial nitric oxide synthase protein World J Gastroenterol 12 2006 2024 2030
16. A. Giulietti, L. Overbergh, D. Valckx, B. Decallonne, R. Bouillon, and C. Mathieu An overview of real-time quantitative PCR: applications to quantify cytokine gene expression Methods 25 2001 386 401
17. Luo Y, Xiao W, Zhu X, Mao Y, Liu X, Chen X, Huang J, Tang S, Rizzolo LJ: Differential expression of claudins in retinas during normal development and the angiogenesis of oxygen-induced retinopathy. Invest Ophthalmol Vis Sci 52:7556-7564
18. J.L. Roxas, A. Koutsouris, A. Bellmeyer, S. Tesfay, S. Royan, K. Falzari, A. Harris, H. Cheng, K.J. Rhee, and G. Hecht Enterohemorrhagic E. coli alters murine intestinal epithelial tight junction protein expression and barrier function in a Shiga toxin independent manner Lab Invest 90 2010 1152 1168
19. H. Kakutani, M. Kondoh, M. Fukasaka, H. Suzuki, T. Hamakubo, and K. Yagi Mucosal vaccination using claudin-4-targeting Biomaterials 31 2010 5463 5471
20. A. Willems, S.R. Batlouni, A. Esnal, J.V. Swinnen, P.T. Saunders, R.M. Sharpe, L.R. França, K. De Gendt, and G. Verhoeven Selective ablation of the androgen receptor in mouse Sertoli cells affects Sertoli cell maturation, barrier formation and cytoskeletal development PLoS One 5 2010 e14168
21. M. Lejeune, P. Leung, P.L. Beck, and K. Chadee Role of EP4 receptor and prostaglandin transporter in prostaglandin E2-induced alteration in colonic epithelial barrier integrity Am J Physiol Gastrointest Liver Physiol 299 2010 G1097 G1105
22. H. Zhao, H. Zhang, H. Wu, H. Li, L. Liu, J. Guo, C. Li, D.Q. Shih, and X. Zhang Protective role of 1,25(OH)2 vitamin D3 in the mucosal injury and epithelial barrier disruption in DSS-induced acute colitis in mice BMC Gastroenterol 12 2012 57
23. K. Chadee, W.A. Petri Jr., D.J. Innes, and J.I. Ravdin Rat and human colonic mucins bind to and inhibit adherence lectin of Entamoeba histolytica J Clin Invest 80 1987 1245 1254
24. S.K. Tse, and K. Chadee Biochemical characterization of rat colonic mucins secreted in response to Entamoeba histolytica Infect Immun 60 1992 1603 1612
25. M. Van der Sluis, B.A. De Koning, A.C. De Bruijn, A. Velcich, J.P. Meijerink, J.B. Van Goudoever, H.A. Buller, J. Dekker, I. Van Seuningen, I.B. Renes, and A.W. Einerhand Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection Gastroenterology 131 2006 117 129
26. L. Mortimer, and K. Chadee The immunopathogenesis of Entamoeba histolytica Exp Parasitol 126 2010 366 380
27. A.M. Marchiando, L. Shen, W.V. Graham, C.R. Weber, B.T. Schwarz, J.R. Austin 2nd, D.R. Raleigh, Y. Guan, A.J. Watson, M.H. Montrose, and J.R. Turner Caveolin-1-dependent occludin endocytosis is required for TNF-induced tight junction regulation in vivo J Cell Biol 189 2010 111 126
28. Y. Hou, L. Mortimer, and K. Chadee Entamoeba histolytica cysteine proteinase 5 binds integrin on colonic cells and stimulates NFkappaB-mediated pro-inflammatory responses J Biol Chem 285 2010 35497 35504
29. M.E. Lidell, D.M. Moncada, K. Chadee, and G.C. Hansson Entamoeba histolytica cysteine proteases cleave the MUC2 mucin in its C-terminal domain and dissolve the protective colonic mucus gel Proc Natl Acad Sci USA 103 2006 9298 9303
30. C.C. Waterhouse, and A.W. Stadnyk Rapid expression of IL-1beta by intestinal epithelial cells in vitro Cell Immunol 193 1999 1 8
31. B.A. de Koning, M. Sluis, D.J. Lindenbergh-Kortleve, A. Velcich, R. Pieters, H.A. Büller, A.W. Einerhand, and I.B. Renes Methotrexate-induced mucositis in mucin 2-deficient mice J Cell Physiol 210 2007 144 152
32. M.E. Johansson, J.K. Gustafsson, K.E. Sjöberg, J. Petersson, L. Holm, H. Sjövall, and G.C. Hansson Bacteria penetrate the inner mucus layer before inflammation in the dextran sulfate colitis model PLoS One 5 2010 e12238
33. H. Schmitz, M. Fromm, C.J. Bentzel, P. Scholz, K. Detjen, J. Mankertz, H. Bode, H.J. Epple, E.O. Riecken, and J.D. Schulzke Tumor necrosis factor-alpha (TNFalpha) regulates the epithelial barrier in the human intestinal cell line HT-29/B6 J Cell Sci 112 1999 137 146
34. J.L. Madara, and J. Stafford Interferon-gamma directly affects barrier function of cultured intestinal epithelial monolayers J Clin Invest 83 1989 724 727
35. M. Bruewer, A. Luegering, T. Kucharzik, C.A. Parkos, J.L. Madara, A.M. Hopkins, and A. Nusrat Proinflammatory cytokines disrupt epithelial barrier function by apoptosis-independent mechanisms J Immunol 171 2003 6164 6172
36. M. Amasheh, I. Grotjohann, S. Amasheh, A. Fromm, J.D. Söderholm, M. Zeitz, M. Fromm, and J.D. Schulzke Regulation of mucosal structure and barrier function in rat colon exposed to tumor necrosis factor alpha and interferon gamma in vitro: a novel model for studying the pathomechanisms of inflammatory bowel disease cytokines Scand J Gastroenterol 44 2009 1226 1235
37. S. Blazquez, C. Zimmer, G. Guigon, J.C. Olivo-Marin, N. Guillén, and E. Labruyère Human tumor necrosis factor is a chemoattractant for the parasite Entamoeba histolytica Infect Immun 74 2006 1407 1411
38. Z. Zhang, S. Mahajan, X. Zhang, and S.L. Stanley Jr. Tumor necrosis factor alpha is a key mediator of gut inflammation seen in amebic colitis in human intestine in the SCID mouse-human intestinal xenograft model of disease Infect Immun 71 2003 5355 5359
39. K.M. Peterson, J. Shu, P. Duggal, R. Haque, D. Mondal, and W.A. Petri Jr. Association between TNF-alpha and Entamoeba histolytica diarrhea Am J Trop Med Hyg 82 2010 620 625
40. L. Shen, C.R. Weber, D.R. Raleigh, D. Yu, and J.R. Turner Tight junction pore and leak pathways: a dynamic duo Annu Rev Physiol 73 2011 283 309
41. K.S. Bergstrom, V. Kissoon-Singh, D.L. Gibson, C. Ma, M. Montero, H.P. Sham, N. Ryz, T. Huang, A. Velcich, B.B. Finlay, K. Chadee, and B.A. Vallance Muc2 protects against lethal infectious colitis by disassociating pathogenic and commensal bacteria from the colonic mucosa PLoS Pathog 6 2010 e1000902
42. D.N. Szakál, H. Gyorffy, A. Arató, A. Cseh, K. Molnár, M. Papp, A. Dezsofi, and G. Veres Mucosal expression of claudins 2, 3 and 4 in proximal and distal part of duodenum in children with coeliac disease Virchows Arch 456 2010 245 250
43. S. Amasheh, M. Fromm, and D. Gunzel Claudins of intestine and nephron-a correlation of molecular tight junction structure and barrier function Acta Physiol (Oxf) 201 2011 133 140
44. S. Prasad, R. Mingrino, K. Kaukinen, K.L. Hayes, R.M. Powell, T.T. MacDonald, and J.E. Collins Inflammatory processes have differential effects on claudins 2, 3 and 4 in colonic epithelial cells Lab Invest 85 2005 1139 1162
45. 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
46. 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
47. C.M. Van Itallie, O.R. Colegio, and J.M. Anderson The cytoplasmic tails of claudins can influence tight junction barrier properties through effects on protein stability J Membr Biol 199 2004 29 38
48. A. Leroy, T. Lauwaet, G. De Bruyne, M. Cornelissen, and M. Mareel Entamoeba histolytica disturbs the tight junction complex in human enteric T84 cell layers FASEB J 14 2000 1139 1146