Anti-inflammatory properties of Lactobacillus gasseri expressing manganese superoxide dismutase using the interleukin 10-deficient mouse model of colitis

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 293, Issue 4, 2007, Pages

  Carroll, Ian M ^a   Andrus, Jason M ^b   Bruno Bárcena, José M ^c   Klaenhammer, Todd R ^c   Hassan, Hosni M ^c   Threadgill, Deborah S ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b AUGUSTA STATE UNIVERSITY   (United States)

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Inflammatory bowel disease; Lactobacilli; Oxidative stress; Probiotic

Indexed keywords

ANTIOXIDANT; INTERLEUKIN 10; MANGANESE SUPEROXIDE DISMUTASE; PROBIOTIC AGENT; REACTIVE OXYGEN METABOLITE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; COLITIS; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; GENETIC TRANSCRIPTION; HISTOPATHOLOGY; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INNATE IMMUNITY; INTESTINE EPITHELIUM; LACTOBACILLUS GASSERI; MACROPHAGE; MALE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ASSAY; SCORING SYSTEM; SYMPTOM;

ANIMALS; ANTI-INFLAMMATORY AGENTS; COLITIS; COLON; CYCLOOXYGENASE 2; DISEASE MODELS, ANIMAL; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-10; LACTOBACILLUS; MICE; PEROXIDASE; PROBIOTICS; SPECIFIC PATHOGEN-FREE ORGANISMS; SUPEROXIDE DISMUTASE;

EID: 35348948953     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00132.2007     Document Type: Article

References (45)

1. Bleich A, Mahler M, Most C, Leiter EH, Liebler-Tenorio E, Elson CO, Hedrich HJ, Schlegelberger B, Sundberg JP. Refined histopathologic scoring system improves power to detect colitis QTL in mice. Mamm Genome 15: 865-871, 2004.
2. Bodor C, Matolcsy A, Bernath M. Elevated expression of Cu, Zn-SOD and Mn-SOD mRNA in inflamed dental pulp tissue. Int Endod J 40: 128-132, 2007.
3. Bruno-Barcena JM, Andrus JM, Libby SL, Klaenhammer TR, Hassan HM. Expression of a heterologous manganese superoxide dismutase gene in intestinal lactobacilli provides protection against hydrogen peroxide toxicity. Appl Environ Microbiol 70: 4702-4710, 2004.
4. Bruno-Barcena JM, Azcarate-Peril MA, Klaenhammer TR, Hassan HM. Marker-free chromosomal integration of the manganese superoxide dismutase gene (sodA) from Streptococcus thermophilus into Lactobacillus gasseri. FEMS Microbiol Lett 246: 91-101, 2005.
5. Deloris Alexander A, Orcutt RP, Henry JC, Baker J Jr, Bissahoyo AC, Threadgill DW. Quantitative PCR assays for mouse enteric flora reveal strain-dependent differences in composition that are influenced by the microenvironment. Mamm Genome 17: 1093-1104, 2006.
6. Fuller R. Probiotics in man and animals. J Appl Bacteriol 66: 365-378, 1989.
7. Garrido D, Suau A, Pochart P, Cruchet S, Gotteland M. Modulation of the fecal microbiota by the intake of a Lactobacillus johnsonii La1-containing product in human volunteers. FEMS Microbiol Lett 248: 249-256, 2005.
8. Heilig HG, Zoetendal EG, Vaughan EE, Marteau P, Akkermans AD, de Vos WM. Molecular diversity of Lactobacillus spp. and other lactic acid bacteria in the human intestine as determined by specific amplification of 16S ribosomal DNA. Appl Environ Microbiol 68: 114-123, 2002.
9. Huycke MM, Abrams V, Moore DR. Enterococcus faecalis produces extracellular superoxide and hydrogen peroxide that damages colonic epithelial cell DNA. Carcinogenesis 23: 529-536, 2002.
10. Keshavarzian A, Banan A, Farhadi A, Komanduri S, Mutlu E, Zhang Y, Fields JZ. Increases in free radicals and cytoskeletal protein oxidation and nitration in the colon of patients with inflammatory bowel disease. Gut 52: 720-728, 2003.
11. Kimball ES, Palmer JM, D'Andrea MR, Hornby PJ, Wade PR. Acute colitis induction by oil of mustard results in later development of an IBS-like accelerated upper GI transit in mice. Am J Physiol Gastrointest Liver Physiol 288: G1266-G1273, 2005.
12. Krieglstein CF, Cerwinka WH, Laroux FS, Salter JW, Russell JM, Schuermann G, Grisham MB, Ross CR, Granger DN. Regulation of murine intestinal inflammation by reactive metabolites of oxygen and nitrogen: divergent roles of superoxide and nitric oxide. J Exp Med 194: 1207-1218, 2001.
13. Kruidenier L, Kuiper I, van Duijn W, Marklund SL, van Hogezand RA, Lamers CB, Verspaget HW. Differential mucosal expression of three superoxide dismutase isoforms in inflammatory bowel disease. J Pathol 201: 7-16, 2003.
14. Kruidenier L, Kuiper I, Van Duijn W, Mieremet-Ooms MA, van Hogezand RA, Lamers CB, Verspaget HW. Imbalanced secondary mucosal antioxidant response in inflammatory bowel disease. J Pathol 201: 17-27, 2003.
15. Kruidenier L, van Meeteren ME, Kuiper I, Jaarsma D, Lamers CB, Zijlstra FJ, Verspaget HW. Attenuated mild colonic inflammation and improved survival from severe DSS-colitis of transgenic Cu/Zn-SOD mice. Free Radic Biol Med 34: 753-765, 2003.
16. Kruidenier L, Verspaget HW. Review article: oxidative stress as a pathogenic factor in inflammatory bowel disease - radicals or ridiculous? Aliment Pharmacol Ther 16: 1997-2015, 2002.
17. Lih-Brody L, Powell SR, Collier KP, Reddy GM, Cerchia R, Kahn E, Weissman GS, Katz S, Floyd RA, McKinley MJ, Fisher SE, Mullin GE. Increased oxidative stress and decreased antioxidant defenses in mucosa of inflammatory bowel disease. Dig Dis Sci 41: 2078 -2086, 1996.
18. Madsen KL, Doyle JS, Jewell LD, Tavernini MM, Fedorak RN. Lactobacillus species prevents colitis in interleukin 10 gene-deficient mice. Gastroenterology 116: 1107-1114, 1999.
19. McCarthy J, O'Mahony L, O'Callaghan L, Sheil B, Vaughan EE, Fitzsimons N, Fitzgibbon J, O'Sullivan GC, Kiely B, Collins JK, Shanahan F. Double blind, placebo controlled trial of two probiotic strains in interleukin 10 knockout mice and mechanistic link with cytokine balance. Gut 52: 975-980, 2003.
20. Montalto MC, Hart ML, Jordan JE, Wada K, Stahl GL. Role for complement in mediating intestinal nitric oxide synthase-2 and superoxide dismutase expression. Am J Physiol Gastrointest Liver Physiol 285: G197-G206, 2003.
21. Mulder TP, Verspaget HW, Janssens AR, de Bruin PA, Pena AS, Lamers CB. Decrease in two intestinal copper/zinc containing proteins with antioxidant function in inflammatory bowel disease. Gut 32: 1146-1150, 1991.
22. Murphy L, Dunne C, Kiely B, Shanahan F, O'Sullivan GC, Collins JK. In vivo assessment of potential probiotic Lactobacillus salivarius: evaluation of their establishment, persistence, and localisation in the murine gastrointestinal tract. Microbial Ecol Health Dis 11: 149-157, 1999.
23. O'Mahony L, Feeney M, O'Halloran S, Murphy L, Kiely B, Fitzgibbon J, Lee G, O'Sullivan G, Shanahan F, Collins JK. Probiotic impact on microbial flora, inflammation and tumour development in IL-10 knock-out mice. Aliment Pharmacol Ther 15: 1219-1225, 2001.
24. Osman N, Adawi D, Ahrne S, Jeppsson B, Molin G. Modulation of the effect of dextran sulfate sodium-induced acute colitis by the administration of different probiotic strains of Lactobacillus and Bifidobacterium. Dig Dis Sci 49: 320-327, 2004.
25. Pavan S, Desreumaux P, Mercenier A. Use of mouse models to evaluate the persistence, safety, and immune modulation capacities of lactic acid bacteria. Clin Diagn Lab Immunol 10: 696-701, 2003.
26. Pedrosa MC, Golner BB, Goldin BR, Barakat S, Dallal GE, Russell RM. Survival of yogurt-containing organisms and Lactobacillus gasseri (ADH) and their effect on bacterial enzyme activity in the gastrointestinal tract of healthy and hypochlorhydric elderly subjects. Am J Clin Nutr 61: 353-359, 1995.
27. Pena JA, Rogers AB, Ge Z, Ng V, Li SY, Fox JG, Versalovic J. Probiotic Lactobacillus spp. diminish Helicobacter hepaticus-induced inflammatory bowel disease in interleukin-10-deficient mice. Infect Immun 73: 912-920, 2005.
28. Peran L, Camuesco D, Comalada M, Nieto A, Concha A, Diaz-Ropero MP, Olivares M, Xaus J, Zarzuelo A, Galvez J. Preventative effects of a probiotic, Lactobacillus salivarius ssp. salivarius, in the TNBS model of rat colitis. World J Gastroenterol 11: 5185-5192, 2005.
29. Perdigon G, Nader de Macias ME, Alvarez S, Oliver G, Pesce de Ruiz Holgado AA. Prevention of gastrointestinal infection using immunobiological methods with milk fermented with Lactobacillus casei and Lactobacillus acidophilus. J Dairy Res 57: 255-264, 1990.
30. Pravda J. Radical induction theory of ulcerative colitis. World J Gastroenterol 11: 2371-2384, 2005.
31. Rogers AB, Boutin SR, Whary MT, Sundina N, Ge Z, Cormier K, Fox JG. Progression of chronic hepatitis and preneoplasia in Helicobacter hepaticus-infected A/JCr mice. Toxicol Pathol 32: 668-677, 2004.
32. Rolfe VE, Fortun PJ, Hawkey CJ, Bath-Hextall F. Probiotics for maintenance of remission in Crohn's disease. Cochrane Database Syst Rev 4: CD004826, 2006.
33. Sartor RB. Therapeutic manipulation of the enteric microflora in inflammatory bowel diseases: antibiotics, probiotics, and prebiotics. Gastroenterology 126: 1620-1633, 2004.
34. Segui J, Gil F, Gironella M, Alvarez M, Gimeno M, Coronel P, Closa D, Pique JM, Panes J. Down-regulation of endothelial adhesion molecules and leukocyte adhesion by treatment with superoxide dismutase is beneficial in chronic immune experimental colitis. Inflamm Bowel Dis 11: 872-882, 2005.
35. Segui J, Gironella M, Sans M, Granell S, Gil F, Gimeno M, Coronel P, Pique JM, Panes J. Superoxide dismutase ameliorates TNBS-induced colitis by reducing oxidative stress, adhesion molecule expression, and leukocyte recruitment into the inflamed intestine. J Leukoc Biol 76: 537-544, 2004.
36. Sheehan KM, Steele C, Sheahan K, O'Grady A, Leader MB, Murray FE, Kay EW. Association between cyclooxygenase-2-expressing macrophages, ulceration and microvessel density in colorectal cancer. Histopathology 46: 287-295, 2005.
37. Steidler L, Hans W, Schotte L, Neirynck S, Obermeier F, Falk W, Fiers W, Remaut E. Treatment of murine colitis by Lactococcus lactis secreting interleukin-10. Science 289: 1352-1355, 2000.
38. Steidler L, Robinson K, Chamberlain L, Schofield KM, Remaut E, Le Page RW, Wells JM. Mucosal delivery of murine interleukin-2 (IL-2) and IL-6 by recombinant strains of Lactococcus lactis coexpressing antigen and cytokine. Infect Immun 66: 3183-3189, 1998.
39. Steidler L, Neirynck S. Genetically modified probiotics. In: Probiotics and Prebiotics: Scientific Aspects, edited by Tannock GW. London: Caister Academic, 2005, p. 155-170.
40. Tannock GW. A special fondness for lactobacilli. Appl Environ Microbiol 70: 3189-3194, 2004.
41. Tannock GW, Munro K, Harmsen HJ, Welling GW, Smart J, Gopal PK. Analysis of the fecal microflora of human subjects consuming a probiotic product containing Lactobacillus rhamnosus DR20. Appl Environ Microbiol 66: 2578-2588, 2000.
42. Tirosh O, Pardo M, Schwartz B, Miskin R. Long-lived alphaMUPA transgenic mice show reduced SOD2 expression, enhanced apoptosis and reduced susceptibility to the carcinogen dimethylhydrazine. Mech Ageing Dev 126: 1262-1273, 2005.
43. Vandenbroucke K, Hans W, Van Huysse J, Neirynck S, Demetter P, Remaut E, Rottiers P, Steidler L. Active delivery of trefoil factors by genetically modified Lactococcus lactis prevents and heals acute colitis in mice. Gastroenterology 127: 502-513, 2004.
44. Vinderola G, Matar C, Perdigon G. Role of intestinal epithelial cells in immune effects mediated by gram-positive probiotic bacteria: involvement of toll-like receptors. Clin Diagn Lab Immunol 12: 1075-1084, 2005.
45. Zoetendal EG, Akkermans AD, De Vos WM. Temperature gradient gel electrophoresis analysis of 16S rRNA from human fecal samples reveals stable and host-specific communities of active bacteria. Appl Environ Microbiol 64: 3854-3859, 1998.