Metabolic stress evokes decreases in epithelial barrier function: Mechanistic insights from in vitro and in vivo model systems

Annals of the New York Academy of Sciences

Volumn 1165, Issue , 2009, Pages 327-337

  Lewis, Kimberley ^a   McKay, Derek M ^a,b  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

Bacteria; Cytokine; Inflammatory bowel disease; Intestine; T84 cells; Transcytosis

Indexed keywords

ADENOSINE TRIPHOSPHATE; INDOMETACIN; NONSTEROID ANTIINFLAMMATORY AGENT; TACROLIMUS; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; DISEASE MODEL; ENTERITIS; HUMAN; INTESTINE EPITHELIUM CELL; INTESTINE MUCOSA PERMEABILITY; MENTAL STRESS; METABOLIC STRESS; MONOLAYER CULTURE; NONHUMAN; PATHOGENESIS; PATHOPHYSIOLOGY; PERMEABILITY BARRIER; RELAPSE; RISK FACTOR; SMALL INTESTINE DISEASE; TRANSCYTOSIS;

EID: 67249112674     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1111/j.1749-6632.2009.04036.x     Document Type: Article

References (57)

1. Turner, J.R. 2006. Molecular basis of epithelial barrier regulation: from basic mechanisms to clinical application. Am. J. Pathol. 169: 1901-1909.
2. Bruewer, M., S. Samarin & A. Nusrat. 2006. Inflammatory bowel disease and the apical junctional complex. Ann. N. Y. Acad. Sci. 1072: 242-252.
3. Wallace, J.L. 1997. Nonsteroidal anti-inflammatory drugs and gastroenteropathy: the second hundred years. Gastroenterology 112: 1000-1016.
4. Hecht, G. 1995. Bugs and barriers: enteric pathogens exploit yet another epithelial function. News Physiol. Sci. 10: 160-166.
5. Weber, C.R. & J.R. Turner. 2007. Inflammatory bowel disease: is it really just another break in the wall? Gut 56: 6-8.
6. Soderholm, J.D., G. Olaison, K.H. Peterson, et al. 2002. Augmented increase in tight junction permeability by luminal stimuli in the non-inflamed ileum of Crohn's disease. Gut 50: 307-313.
7. Farhadi, A., A. Keshavarzian, L.D. van de Kar, et al. 2005. Heightened responses to stressors in patients with inflammatory bowel disease. Am. J. Gastroenterol. 100: 1796-1804.
8. Nazli, A., P.-C. Yang, J. Jury, et al. 2004. Epithelia under metabolic stress perceive commensal bacteria as a threat. Am. J. Pathol. 164: 947-957.
9. Xavier, R.J. & D.K. Podolsky. 2007. Unraveling the pathogenesis of inflammatory bowel disease. Nature 448: 427-434.
10. Grace, W.J. 1953. Life stress and regional enteritis. Gastroenterology 23: 542-553.
11. Mawdsley, J.E. & D.S. Rampton. 2005. Psychological stress in IBD: new insights into pathogenic and therapeutic implications. Gut 54: 1481-1491.
12. Mittermaier, C., C. Dejaco, T. Waldhoer, et al. 2004. Impact of depressive mood on relapse in patients with inflammatory bowel disease: a prospective 18-month follow-up study. Psychosom. Med. 66: 79-84.
13. Bernstein, C.N., J.R. Walker & L.A. Graff. 2006. On studying the connection between stress and IBD. Am. J. Gastroenterol. 101: 782-785.
14. Li, J., B. Norgard, D.H. Precht & J. Olsen. 2004. Psychological stress and inflammatory bowel disease: a follow-up study in parents who lost a child in Denmark. Am. J. Gastroenterol. 99: 1129-1133.
15. Vidal, A., E. Gomez-Gil, M. Sans, et al. 2006. Life events and inflammatory bowel disease relapse: a prospective study of patients enrolled in remission. Am. J. Gastroenterol. 101: 775-781.
16. Barclay, G. & L. Turnberg. 1987. Effect of psychological stress on salt and water transport in the human jejunum. Gastroenterology 93: 91-97.
17. Santos, J., E. Saperas, C. Nogueiras, et al. 1998. Release of mast cell mediators into the jejunum by cold pain stress in humans. Gastroenterology 114: 640-648.
18. Saunders, P.R., U. Kosecka, D.M. McKay & M.H. Perdue. 1994. Acute stressors stimulate ion secretion and increase epithelial permeability in rat intestine. Am. J. Physiol. (Gastrointest. Liver Physiol.) 267: G794-G799.
19. Meddings, J.B. & M.G. Swain. 2000. Environmental stress-induced gastrointestinal permeability is mediated by endogenous glucocorticoids in the rat. Gastroenterology 119: 1019-1028.
20. Barreau, F., L. Ferrier, J. Fioramonti, et al. 2004. Neonatal maternal deprivation triggers long term alterations in colonic epithelial barrier and mucosal immunity in rats. Gut 53: 501-506.
21. Soderholm, J.D. & M.H. Perdue. 2001. Stress and the gastrointestinal tract. II. Stress and intestinal barrier function. Am. J. Physiol. (Gastrointest. Liver Physiol.) 280: G7-G134.
22. Soderholm, J.D., P.-C. Yang, A. Vohra, et al. 2002. Chronic psychological stress induces epithelial barrier disruption, bacterial penetration and mucosal inflammation in the ileum and colon of naive rats. Gastroenterology 123: 1099-1108.
23. Somasundaram, S., G. Sigthorsson, R.J. Simpson, et al. 2000. Uncoupling of intestinal mitochondrial oxidative phosphorylation and inhibition of cyclooxygenase are required for the development of NSAID-enteropathy in the rat. Aliment. Pharm. Thera. 14: 639-650.
24. Atherton, C., J. Jones, B. McKaig, et al. 2004. Pharmacology and gastrointestinal safety of lumiracoxib, a novel cyclooxygenase-2 selective inhibitor: an integrated study. Clin. Gastroenterol. Hepatol. 2: 113-120.
25. Somasundaram, S., S. Rafi, G. Sigthorsson, et al. 1997. Mitochondrial damage: a possible mechanism of the "topical" phase of NSAID induced injury in the rat intestine. Gut 41: 344-353.
26. Basivireddy, J., A. Vasudevan, M. Jacob, et al. 2002. Indomethacin-induced mitochondrial dysfunction and oxidative stress in villous enterocytes. Biochem. Pharm. 64: 339-349.
27. Madsen, K., N. Yanchar, D. Sigalet, et al. 1995. FK506 increases permeability in rat intestine by inhibiting mitochondrial function. Gastroenterology 109: 107-114.
28. Gabe, S.M., I. Bjarnason, Z. Tolou-Ghamari, et al. 1998. The effect of tacrolimus (FK506) on intestinal barrier function and cellular energy production in humans. Gastroenterology 115: 67-74.
29. He, D., S.J. Hagen, C. Pothoulakis, et al. 2000. Clostridium difficile toxin A causes early damage to mitochondria in cultured cells. Gastroenterology 119: 139-150.
30. Humphrey, C.D., D.M. Montag & F.E. Pitteman. 1986. Morphologic observations of experimental Campylobacter jejuni infection in the hamster intestinal tract. Am. J. Pathol. 122: 152-159.
31. Zareie, M., J. Riff, K. Donato, et al. 2005. Novel effects of the prototype translocating Escherichia coli, strain C25 on intestinal epithelial structure and barrier function. Cell Microbiol. 7: 1782-1795.
32. Ma, C., M.E. Wickham, J.A. Guttman, et al. 2006. Citrobacter rodentium infection causes both mitochondrial dysfunction and intestinal epithelial barrier disruption in vivo: role of mitochondrial associated protein (Map). Cell Microbiol. 8: 1669-1686.
33. Dickman, K.G., S.J. Hempson, J. Anderson, et al. 2000. Rotavirus alters paracellular permeability and energy metabolism in Caco-2 cells. Am. J. Physiol (Gastrointest. Liver Physiol.) 279: G757-G766.
34. Gellerich, F.N., S. Trumbeckaite, J.R. Opalka, et al. 2002. Mitochondrial dysfunction in sepsis: evidence from bacteraemic baboons and endotoxaemic rabbits. Biosci. Rep. 22: 99-113.
35. Taylor, C.T., A.L. Dzus & S.P. Colgan. 1998. Autocrine regulation of epithelial permeability by hypoxia: role for polarized release of tumor necrosis factor a. Gastroenterology 114: 657-668.
36. 51Crethylenediaminetetraacetic acid is increased after bilateral lower extremity ischemia-reperfusion in the rat. Surgery 120: 547-553.
37. Ramachandran, A., A. Patram & K.A. Balasubramanian. 2001. Intestinal mitochondrial dysfunction in surgical stress. J. Surg. Res. 99: 120-128.
38. Frank, D.N., A.L. St. Amand, R.A. Feldman, et al. 2007. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc. Natl. Acad. Sci. USA 104: 13780-13785.
39. Manichanh, C., L. Rigottier-Gois, E. Bonnaud, et al. 2006. Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach. Gut 55: 205-211.
40. Barcenilla, A., S.E. Pryde, J.C. Martin, et al. 2000. Phylogenetic relationships of butyrate-producing bacteria from the human gut. Appl. Environ. Microbiol. 66: 1654-1661.
41. Segain, J.P., B.D. De La Raingeard, A. Bourreille, et al. 2000. Butyrate inhibits inflammatory responses through NFkB inhibition: implications for Crohn's disease. Gut 47: 397-403.
42. Mantena, S.K., A.L. King, K.K. Andringa, et al. 2008. Mitochondrial dysfunction and oxidative stress in the pathogenesis of alcohol- and obesity-induced fatty liver diseases. Free Radic. Biol. Med. 44: 1259-1272.
43. Tarnopolsky, M.A. & S. Raha. 2005. Mitochondrial myopathies: diagnosis, exercise intolerance, and treatment options. Med. Sci. Sports Exerc. 37: 2086-2093.
44. Nisoli, E., E. Clementi, C. Paolucci, et al. 2003. Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science 299: 896-899.
45. Sartor, R.B. 2008. Microbial influences in inflammatory bowel diseases. Gastroenterology 134: 577-594.
46. Rfeuille-Michaud, A., J. Boudeau, P. Bulois, et al. 2004. High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn's disease. Gastroenterology 127: 412-421.
47. Nazli, A., A. Wang, O. Steen, et al. 2006. Enterocyte cytoskeleton changes are crucial for enhanced translocation of commensal bacteria across metabolically stressed gut epithelia. Infect. Immunity 74: 192-201.
48. Lewis, K., J. Caldwell, V. Phan, et al. 2008. Decreased epithelial barrier function evoked by exposure to metabolic stress and nonpathogenic E. coli is enhanced by TNFα. Am. J. Physiol. (Gastrointest. Liver Physiol.) 294: G669-G678.
49. Philpott, D.J., D.M. McKay, P.M. Sherman & M.H. Perdue. 1996. Infection of T84 cells with en-teropathogenic Escherichia coli alters barrier and transport functions. Am. J. Physiol. (Gastrointest. Liver Physiol.) 270: G634-G645.
50. Soderholm, J.D., C. Streuker, P.-C. Yang, et al. 2004. Increased epithelial uptake of protein antigens in the ileum of Crohn's disease mediated by TNFa. Gut 53: 1813-1820.
51. McKay, D.M., J.L. Watson, A. Wang, et al. 2007. PI-3K is a critical mediator of interferon-γ-induced increases in enteric epithelial permeability. J. Pharmacol. Exp. Ther. 320: 1013-1022.
52. Clark, E., C. Hoare, J. Tanianis-Hughes, et al. 2005. Interferon-g induces translocation of commensal Escherichia coli across gut epithelial cells via a lipid raftmediated process. Gastroenterology 128: 1258-1267.
53. Schurmann, G., M. Bruwer, A. Klotz, et al. 1999. Transepithelial transport processes at the intestinal mucosa in inflammatory bowel disease. Int. J. Colorectal. Dis. 14: 41-46.
54. McKay, D.M. & A.W. Baird. 1999. Cytokine regulation of epithelial permeability and ion transport. Gut 44: 283-289.
55. Zareie, M., P.K. Singh, J. Irvine, et al. 2001. Monocyte/macrophage activation by normal bacteria and bacterial products: implications for epithelial pathophysiology in Crohn's disease. Am. J. Path. 158: 1101-1109.
56. Schmitz, H., M. Fromm, C.J. Bentzel, et al. 1999. Tumor necrosis factor-alpha (TNFa) regulates the epithelial barrier in the human intestinal cell line HT-29/B6. J. Cell Sci. 112: 137-146.
57. McKay, D.M., K. Croitor & M.H. Perdue. 1996. T cell-monocyte interactions regulate epithelial physiology in a co-culture model of inflammation. Am. J. Physiol.(Cell Physiol.) 270: C418-C428.