Probiotics prevent intestinal barrier dysfunction in acute pancreatitis in rats via induction of ileal mucosal glutathione biosynthesis

PLoS ONE

Volumn 4, Issue 2, 2009, Pages

  Lutgendorff, Femke ^a,b   Nijmeijer, Rian M ^b   Sandström, Per A ^a   Trulsson, Lena M ^a   Magnusson, Karl Eric ^a   Timmerman, Harro M ^b   van Minnen, L Paul ^b   Rijkers, Ger T ^b   Gooszen, Hein G ^b   Akkermans, Louis M A ^b   Söderholm, Johan D ^a  

^a LINKÖPING UNIVERSITY   (Sweden)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CERULETIDE; CLAUDIN 1; CLAUDIN 2; ECOLOGIC 641; EDETIC ACID; GAP JUNCTION PROTEIN; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE; GLYCODEOXYCHOLIC ACID; LIPID; MESSENGER RNA; OCCLUDIN; PLACEBO; PROBIOTIC AGENT; UNCLASSIFIED DRUG;

ACUTE PANCREATITIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ESCHERICHIA COLI K 12; GENE EXPRESSION; GLUTATHIONE METABOLISM; ILEUM MUCOSA; IMMUNOFLUORESCENCE MICROSCOPY; INTESTINE BARRIER DYSFUNCTION; INTESTINE FUNCTION DISORDER; LIPID PEROXIDATION; MALE; NONHUMAN; OXIDATIVE STRESS; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RAT; TIGHT JUNCTION;

ANIMALIA; RATTUS;

EID: 84875496739     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0004512     Document Type: Article

References (47)

1. Deitch EA, Dayal SD (2006) Intensive care unit management of the trauma patient. Crit Care Med 34: 2294-2301.
2. Clark JA, Coopersmith CM (2007) Intestinal crosstalk: a new paradigm for understanding the gut as the "motor" of critical illness. Shock 28: 384-393.
3. Ammori BJ (2003) Role of the gut in the course of severe acute pancreatitis. Pancreas 26: 122-129.
4. Deitch EA, Xu D, Franko L, Ayala A, Chaudry IH (1994) Evidence favoring the role of the gut as a cytokine-generating organ in rats subjected to hemorrhagic shock. Shock 1: 141-145.
5. Katsube T, Tsuji H, Onoda M (2007) Nitric oxide attenuates hydrogen peroxide-induced barrier disruption and protein tyrosine phosphorylation in monolayers of intestinal epithelial cell. Biochim Biophys Acta 1773: 794-803.
6. Basuroy S, Seth A, Elias B, Naren AP, Rao R (2006) MAPK interacts with occludin and mediates EGF-induced prevention of tight junction disruption by hydrogen peroxide. Biochem J 393: 69-77.
7. Van Itallie CM, Anderson JM (2006) Claudins and epithelial paracellular transport. Annu Rev Physiol 68: 403-429.
8. Wu B, Qiu W, Wang P, Yu H, Cheng T, et al. (2007) p53 independent induction of PUMA mediates intestinal apoptosis in response to ischaemia-reperfusion. Gut 56: 645-654.
9. Yasuda T, Takeyama Y, Ueda T, Shinzeki M, Sawa H, et al. (2006) Breakdown of intestinal mucosa via accelerated apoptosis increases intestinal permeability in experimental severe acute pancreatitis. J Surg Res 135: 18-26.
10. Heller F, Florian P, Bojarski C, Richter J, Christ M, et al. (2005) Interleukin-13 is the key effector Th2 cytokine in ulcerative colitis that affects epithelial tight junctions, apoptosis, and cell restitution. Gastroenterology 129: 550-564.
11. Abreu MT, Palladino AA, Arnold ET, Kwon RS, McRoberts JA (2000) Modulation of barrier function during Fas-mediated apoptosis in human intestinal epithelial cells. Gastroenterology 119: 1524-1536.
12. Coopersmith CM, Stromberg PE, Dunne WM, Davis CG, Amiot DM, et al. (2002) Inhibition of intestinal epithelial apoptosis and survival in a murine model of pneumonia-induced sepsis. JAMA 287: 1716-1721.
13. Yasuda T, Takeyama Y, Ueda T, Shinzeki M, Kishi S, Sawa, et al. (2007) Protective effect of caspase inhibitor on intestinal integrity in experimental severe acute pancreatitis. J Surg Res.
14. Hotchkiss RS, Schmieg RE Jr, Swanson PE, Freeman BD, Tinsley KW, et al. (2000) Rapid onset of intestinal epithelial and lymphocyte apoptotic cell death in patients with trauma and shock. Crit Care Med 28: 3207-3217.
15. Tomson FL, Koutsouris A, Viswanathan VK, Turner JR, Savkovic SD, et al. (2004) Differing roles of protein kinase C-zeta in disruption of tight junction barrier by enteropathogenic and enterohemorrhagic Escherichia coli. Gastroenterology 127: 859-869.
16. Kohler JE, Zaborina O, Wu L, Wang Y, Bethel C, Chen, et al. (2005) Components of intestinal epithelial hypoxia activate the virulence circuitry of Pseudomonas. Am J Physiol Gastrointest Liver Physiol 288: G1048-G1054.
17. Ding Y, Choi KJ, Kim JH, Han X, Piao Y, et al. (2008) Endogenous hydrogen peroxide regulates glutathione redox via nuclear factor erythroid 2-related factor 2 downstream of phosphatidylinositol 3-kinase during muscle differentiation. Am J Pathol 172: 1529-1541.
18. Solis WA, Dalton TP, Dieter MZ, Freshwater S, Harrer JM, et al. (2002) Glutamate-cysteine ligase modifier subunit: mouse Gclm gene structure and regulation by agents that cause oxidative stress. Biochem Pharmacol 63: 1739-1754.
19. Guarner F, Malagelada JR (2003) Gut flora in health and disease. Lancet 361: 512-519.
20. Peran L, Camuesco D, Comalada M, Nieto A, Concha A, et al. (2006) Lactobacillus fermentum, a probiotic capable to release glutathione, prevents colonic inflammation in the TNBS model of rat colitis. Int J Colorectal Dis 21: 737-746.
21. Alberda C, Gramlich L, Meddings J, Field C, McCargar L, et al. (2007) Effects of probiotic therapy in critically ill patients: a randomized, double-blind, placebo-controlled trial. Am J Clin Nutr 85: 816-823.
22. Timmerman HM, Niers LE, Ridwan BU, Koning CJ, Mulder L, et al. (2007) Design of a multispecies probiotic mixture to prevent infectious complications in critically ill patients. Clin Nutr 26: 450-459.
23. van Minnen LP, Timmerman HM, Lutgendorff F, Verheem A, Harmsen W, et al. (2007) Modification of intestinal flora with multispecies probiotics reduces bacterial translocation and improves clinical course in a rat model of acute pancreatitis. Surgery 141: 470-480.
24. Besselink MG, van Santvoort HC, Buskens E, Boermeester MA, van Goor H, et al. (2008) Probiotic prophylaxis in predicted severe acute pancreatitis: a randomised, double-blind, placebo-controlled trial. Lancet 371: 651-659.
25. Schmidt J, Rattner DW, Lewandrowski K, Compton CC, Mandavilli U, et al. (1992) A better model of acute pancreatitis for evaluating therapy. Ann Surg 215: 44-56.
26. Velin AK, Ericson AC, Braaf Y, Wallon C, Soderholm JD (2004) Increased antigen and bacterial uptake in follicle associated epithelium induced by chronic psychological stress in rats. Gut 53: 494-500.
27. Grass GM, Sweetana SA (1988) In vitro measurement of gastrointestinal tissue permeability using a new diffusion cell. Pharm Res 5: 372-376.
28. Wan CP, Park CS, Lau BH (1993) A rapid and simple microfluorometric phagocytosis assay. J Immunol Methods 162: 1-7.
29. Trulsson LM, Gasslander T, Sundqvist T, Svanvik J (2002) The influence of nitric oxide on basal and cholecystokinin-8-induced proliferation and apoptosis in the rat pancreas. Regul Pept 106: 97-104.
30. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
31. Chiu CJ, McArdle AH, Brown R, Scott HJ, Gurd FN (1970) Intestinal mucosal lesion in low-flow states. I. A morphological, hemodynamic, and metabolic reappraisal. Arch Surg 101: 478-483.
32. Spormann H, Sokolowski A, Letko G (1989) Effect of temporary ischemia upon development and histological patterns of acute pancreatitis in the rat. Pathol Res Pract 184: 507-513.
33. Gaitonde MK (1967) A spectrophotometric method for the direct determination of cysteine in the presence of other naturally occurring amino acids. Biochem J 104: 627-633.
34. White CC, Viernes H, Krejsa CM, Botta D, Kavanagh TJ (2003) Fluorescence-based microtiter plate assay for glutamate-cysteine ligase activity. Anal Biochem 318: 175-180.
35. Hagen TM, Wierzbicka GT, Bowman BB, Aw TY, Jones DP (1990) Fate of dietary glutathione: disposition in the gastrointestinal tract. Am J Physiol 259: G530-G535.
36. Meister A, Anderson ME (1983) Glutathione. Annu Rev Biochem 52: 711-760.
37. Lu SC (2008) Regulation of glutathione synthesis. Mol Aspects Med.
38. Musenga A, Mandrioli R, Bonifazi P, Kenndler E, Pompei A, et al. (2007) Sensitive and selective determination of glutathione in probiotic bacteria by capillary electrophoresis-laser induced fluorescence. Anal Bioanal Chem 387: 917-924.
39. Peran L, Sierra S, Comalada M, Lara-Villoslada F, Bailon E, et al. (2007) A comparative study of the preventative effects exerted by two probiotics, Lactobacillus reuteri and Lactobacillus fermentum, in the trinitrobenzenesulfonic acid model of rat colitis. Br J Nutr 97: 96-103.
40. Zeissig S, Burgel N, Gunzel D, Richter J, Mankertz J, et al. (2007) 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.
41. Yan F, Cao H, Cover TL, Whitehead R, Washington MK, et al. (2007) Soluble proteins produced by probiotic bacteria regulate intestinal epithelial cell survival and growth. Gastroenterology 132: 562-575.
42. Resta-Lenert S, Barrett KE (2002) Enteroinvasive bacteria alter barrier and transport properties of human intestinal epithelium: role of iNOS and COX-2. Gastroenterology 122: 1070-1087.
43. Rau B, Poch B, Gansauge F, Bauer A, Nussler AK, et al. (2000) Pathophysiologic role of oxygen free radicals in acute pancreatitis: initiating event or mediator of tissue damage? Ann Surg 231: 352-360.
44. Siriwardena AK, Mason JM, Balachandra S, Bagul A, Galloway S, et al. (2007) Randomised, double blind, placebo controlled trial of intravenous antioxidant (n-acetylcysteine, selenium, vitamin C) therapy in severe acute pancreatitis. Gut 56: 1439-1444.
45. Sugawara G, Nagino M, Nishio H, Ebata T, Takagi K, et al. (2006) Perioperative synbiotic treatment to prevent postoperative infectious complications in biliary cancer surgery: a randomized controlled trial. Ann Surg 244: 706-714.
46. Kruis W, Fric P, Pokrotnieks J, Lukas M, Fixa B, et al. (2004) Maintaining remission of ulcerative colitis with the probiotic Escherichia coli Nissle 1917 is as effective as with standard mesalazine. Gut 53: 1617-1623.
47. Gionchetti P, Rizzello F, Venturi A, Brigidi P, Matteuzzi D, et al. (2000) Oral bacteriotherapy as maintenance treatment in patients with chronic pouchitis: a double-blind, placebo-controlled trial. Gastroenterology 119: 305-309.