Genetically engineered immunomodulatory Streptococcus thermophilus strains producing antioxidant enzymes exhibit enhanced anti-inflammatory activities

Applied and Environmental Microbiology

Volumn 80, Issue 3, 2014, Pages 869-877

  del Carmen, Silvina ^a   de LeBlanc, Alejandra de Moreno ^a   Martin, Rebeca ^b   Chain, Florian ^b   Langella, Philippe ^b   Bermúdez Humarán, Luis G ^b   LeBlanc, Jean Guy ^a,c  

^a CENTRO DE REFERENCIA PARA LACTOBACILOS CERELA CONICET   (Argentina)

^b UMR1319 MICALIS   (France)

^c Universidad Nacional de Tucuman UNT Facultad de Medicina   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-INFLAMMATORY ACTIVITY; ANTI-INFLAMMATORY EFFECTS; ANTIOXIDANT PROPERTIES; LACTIC ACID BACTERIA; LACTOBACILLUS DELBRUECKII; MACROSCOPIC AND MICROSCOPIC; STREPTOCOCCUS THERMOPHILUS STRAINS; SUPEROXIDE DISMUTASES;

ANTIOXIDANTS; BACTERIA; DISEASES; ENZYMES; GENES; MIXTURES; OXYGEN;

MAMMALS;

ANTIOXIDANT; BACTERIUM; CARBOXYLIC ACID; DIGESTIVE SYSTEM DISORDER; DISEASE TREATMENT; GENE EXPRESSION; GENETIC ENGINEERING; IMMUNE SYSTEM; MEDICINE; PROTEIN; RODENT;

ANTIOXIDANT; CATALASE; CYTOKINE; IMMUNOLOGIC FACTOR; SUPEROXIDE DISMUTASE; TRINITROBENZENESULFONIC ACID;

ANIMAL; ARTICLE; CELL CULTURE; CHEMICALLY INDUCED DISORDER; COLITIS; DISEASE MODEL; GENETICS; IMMUNOLOGY; INFLAMMATION; METABOLIC ENGINEERING; METABOLISM; MICROBIOLOGY; MONONUCLEAR CELL; MOUSE; PATHOLOGY; SECRETION (PROCESS); STREPTOCOCCUS THERMOPHILUS;

ANIMALS; ANTIOXIDANTS; CATALASE; CELLS, CULTURED; COLITIS; CYTOKINES; DISEASE MODELS, ANIMAL; IMMUNOLOGIC FACTORS; INFLAMMATION; LEUKOCYTES, MONONUCLEAR; METABOLIC ENGINEERING; MICE; STREPTOCOCCUS THERMOPHILUS; SUPEROXIDE DISMUTASE; TRINITROBENZENESULFONIC ACID;

EID: 84892957370     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03296-13     Document Type: Article

References (33)

1. LeBlanc JG, de Moreno de LeBlanc A. 2013. Crohn's disease: etiology, diagnosis and treatment options, 1st ed. Nova Science Publishers, Inc., Hauppauge, NY.
2. FAO/WHO. 2001. Expert consultation on evaluation of health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Cordoba, Argentina, 1 to 4 October 2001. WHO, Geneva, Switzerland.
3. LeBlanc JG, del Carmen S, Zurita Turk M, Alvarenga Lima F, Santos Pontes D, Miyoshi A, Azevedo V, de Moreno de LeBlanc A. 2013. Mechanisms involved in the anti-inflammatory properties of native and genetically engineered lactic acid bacteria. Anti-Infect. Agents 11:59-69. http://dx.doi.org/10.2174/10059.
4. Sheil B, Shanahan F, O'Mahony L. 2007. Probiotic effects on inflammatory bowel disease. J. Nutr. 137:819S-824S.
5. de Moreno de LeBlanc A, Chaves S, Perdigon G. 2009. Effect of yoghurt on the cytokine profile using a murine model of intestinal inflammation. Eur. J. Inflam. 7:97-109.
6. Chaves S, Perdigon G, de Moreno de LeBlanc A. 2011. Yoghurt consumption regulates the immune cells implicated in acute intestinal inflammation and prevents the recurrence of the inflammatory process in a mouse model. J. Food Prot. 74:801-811. http://dx.doi.org/10.4315/0362-028X.JFP-10-375.
7. Bruno-Barcena JM, Andrus JM, Libby SL, Klaenhammer TR, Hassan HM. 2004. Expression of a heterologous manganese superoxide dismutase gene in intestinal lactobacilli provides protection against hydrogen peroxide toxicity. Appl. Environ. Microbiol. 70:4702-4710. http://dx.doi .org/10.1128/AEM.70.8.4702-4710.2004.
8. Carroll IM, Andrus JM, Bruno-Barcena JM, Klaenhammer TR, Hassan HM, Threadgill DS. 2007. Anti-inflammatory properties of Lactobacillus gasseri expressing manganese superoxide dismutase using the interleukin 10-deficient mouse model of colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 293:G729-738. http://dx.doi.org/10.1152/ajpgi.00132.2007.
9. Han W, Mercenier A, Ait-Belgnaoui A, Pavan S, Lamine F, van Kleerebezem SIIM, Salvador-Cartier C, Hisbergues M, Bueno L, Theodorou V, Fioramonti J. 2006. Improvement of an experimental colitis in rats by lactic acid bacteria producing superoxide dismutase. Inflamm. Bowel Dis. 12:1044-1052. http://dx.doi.org/10.1097/01.mib.0000235101.09231.9e.
10. Watterlot L, Rochat T, Sokol H, Cherbuy C, Bouloufa I, Lefèvre F, Gratadoux JJ, Honvo-Hueto E, Chilmonczyk S, Blugeon S. 2010. Intragastric administration of a superoxide dismutase-producing recombinant Lactobacillus casei BL23 strain attenuates DSS colitis in mice. Int. J. Food Microbiol. 144:35-41. http://dx.doi.org/10.1016/j.ijfoodmicro.2010.03 .037.
11. Castillo NA, Perdigon G, de Moreno de Leblanc A. 2011. Oral administration of a probiotic Lactobacillus modulates cytokine production and TLR expression improving the immune response against Salmonella enterica serovar Typhimurium infection in mice. BMC Microbiol. 11:177. http://dx.doi.org/10.1186/1471-2180-11-177.
12. de Moreno de LeBlanc A, Perdigón G. 2004. Yogurt feeding inhibits promotion and progression of experimental colorectal cancer. Med. Sci. Monit. 10:BR96-BR104.
13. del Carmen S, Zurita-Turk M, Alvarenga Lima F, Coelho dos Santos JS, Leclercq SY, Chatel J-M, Azevedo V, de Moreno de LeBlanc A, Miyoqhi A, LeBlanc JG. 2013. A novel interleukin-10 DNA mucosal delivery system attenuates intestinal inflammation in a mouse model. Eur. J. Inflamm. 11:641-655.
14. Holo H, Nes IF. 1989. High-frequency transformation, by electroporation, of Lactococcus lactis subsp. cremoris grown with glycine in osmotically stabilized media. Appl. Environ. Microbiol. 55:3119-3123.
15. O'Sullivan TF, Fitzgerald GF. 1999. Electrotransformation of industrial strains of Streptococcus thermophilus. J. Appl. Microbiol. 86:275-283. http: //dx.doi.org/10.1046/j.1365-2672.1999.00657.x.
16. Rochat T, Gratadoux JJ, Gruss A, Corthier G, Maguin E, Langella P, van de Guchte M. 2006. Production of a heterologous nonheme catalase by Lactobacillus casei: an efficient tool for removal of H2O2 and protection of Lactobacillus bulgaricus from oxidative stress in milk. Appl. Environ. Microbiol. 72:5143-5149. http://dx.doi.org/10.1128/AEM.00482-06.
17. 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. http://dx.doi.org/10.1016/0003-2697(76)90527-3.
18. LeBlanc JG, del Carmen S, Miyoshi A, Azevedo V, Sesma F, Langella P, Bermudez-Humaran LG, Watterlot L, Perdigon G, de Moreno de LeBlanc A. 2011. Use of superoxide dismutase and catalase producing lactic acid bacteria in TNBS induced Crohn's disease in mice. J. Biotechnol. 151:287-293. http://dx.doi.org/10.1016/j.jbiotec.2010.11.008.
19. LeBlanc JG, Garro MS, Silvestroni A, Connes C, Piard JC, Sesma F, Savoy de Giori G. 2004. Reduction of α-galactooligosaccharides in soyamilk by Lactobacillus fermentum CRL 722: in vitro and in vivo evaluation of fermented soya milk. J. Appl. Microbiol. 97:876-881. http://dx.doi.org /10.1111/j.1365-2672.2004.02389.x.
20. Foligne B, Nutten S, Grangette C, Dennin V, Goudercourt D, Poiret S, Dewulf J, Brassart D, Mercenier A, Pot B. 2007. Correlation between in vitro and in vivo immunomodulatory properties of lactic acid bacteria. World J. Gastroenterol. 13:236-243. http://dx.doi.org/10.1186/1471-2180-11-177.
21. Jung C, Hugot JP, Barreau F. 2010. Peyer's patches: the immune sensors of the intestine. Int. J. Inflam. 2010:823710. http://dx.doi.org/10.4061 /2010/823710.
22. Kruidenier L, Verspaget HW. 2002. Review article: oxidative stress as a pathogenic factor in inflammatory bowel disease, radicals or ridiculous? Aliment. Pharmacol. Ther. 16:1997-2015. http://dx.doi.org/10.1046/j .1365-2036.2002.01378.x.
23. Kruidenier L, van Meeteren ME, Kuiper I, Jaarsma D, Lamers CB, Zijlstra FJ, Verspaget HW. 2003. Attenuated mild colonic inflammation and improved survival from severe DSS-colitis of transgenic Cu/Zn-SOD mice. Free Radic. Biol. Med. 34:753-765. http://dx.doi.org/10.1016/S0891-5849(02)01426-0.
24. 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. 1996. Increased oxidative stress and decreased antioxidant defenses in mucosa of inflammatory bowel disease. Dig. Dis. Sci. 41:2078-2086. http: //dx.doi.org/10.1007/BF02093613.
25. Rochat T, Bermudez-Humaran L, Gratadoux JJ, Fourage C, Hoebler C, Corthier G, Langella P. 2007. Anti-inflammatory effects of Lactobacillus casei BL23 producing or not a manganese-dependent catalase on DSSinduced colitis in mice. Microb. Cell Fact. 6:22. http://dx.doi.org/10.1186 /1475-2859-6-22.
26. Van de Guchte M, Penaud S, Grimaldi C, Barbe V, ryson B Nicolas KP, Robert C, Oztas S, Mangenot S, Couloux A. 2006. The complete genome sequence of Lactobacillus bulgaricus reveals extensive and ongoing reductive evolution. Proc. Natl. Acad. Sci. U. S. A. 103:9274-9279. http://dx.doi .org/10.1073/pnas.0603024103.
27. Chang S, Hassan H. 1997. Characterization of superoxide dismutase in Streptococcus thermophilus. Appl. Environ. Microbiol. 63:3732-3735.
28. Grompone G, Martorell P, Llopis S, González N, Genovés S, Mulet AP, Fernández-Calero T, iscornia T Bollati-Fogolín IM, Chambaud I, Foligne B, Montserrat A, Ramón D. 2012. Anti-inflammatory Lactobacillus rhamnosus CNCM I-3690 strain protects against oxidative stress and increases lifespan in Caenorhabditis elegans. PLoS One 7:e52493. http://dx .doi.org/10.1371/journal.pone.0052493.
29. Braat H, Rottiers P, Hommes DW, Huyghebaert N, Remaut E, Remon JP, van Deventer SJ, Neirynck S, Peppelenbosch MP, Steidler L. 2006. A phase I trial with transgenic bacteria expressing interleukin-10 in Crohn's disease. Clin. Gastroenterol. Hepatol. 4:754-759. http://dx.doi .org/10.1016/j.cgh.2006.03.028.
30. Limaye SA, Haddad RI, Cilli F, Sonis ST, Colevas AD, Brennan MT, Hu KS, Murphy BA. 2013. Phase 1b, multicenter, single blinded, placebocontrolled, sequential dose escalation study to assess the safety and tolerability of topically applied AG013 in subjects with locally advanced head and neck cancer receiving induction chemotherapy. Cancer 119:4268-4276. http://dx.doi.org/10.1002/cncr.28365.
31. Reference deleted.
32. Kechaou N, Chain F, Gratadoux JJ, Blugeon S, Bertho N, Chevalier C, Le Goffic R, Courau S, Molimard P, Chatel JM, Langella P, Bermúdez-Humarán LG. 2013. Identification of one novel candidate probiotic Lactobacillus plantarum strain active against influenza virus infection in mice by a large-scale screening. Appl. Environ. Microbiol. 79:1491-1499. http: //dx.doi.org/10.1128/AEM.03075-12.
33. Fu L, Kong J, Sun Z, Zhang L, Zhang X, Guo T. 2013. Enhancing the oxidative resistance of yoghurt starter bacteria with heterologous catalase expression in Streptococcus thermophilus. Int. Dairy J. 30:68-72. http://dx .doi.org/10.1016/j.idairyj.2012.11.012.