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Published in: Gut Pathogens 1/2014

Open Access 01-07-2014 | Research

Anti-inflammatory effects of Lactococcus lactis NCDO 2118 during the remission period of chemically induced colitis

Authors: Tessalia Diniz Luerce, Ana Cristina Gomes-Santos, Clarissa Santos Rocha, Thais Garcias Moreira, Déborah Nogueira Cruz, Luísa Lemos, Adna Luciana Sousa, Vanessa Bastos Pereira, Marcela de Azevedo, Kátia Moraes, Denise Carmona Cara, Jean Guy LeBlanc, Vasco Azevedo, Ana Maria Caetano Faria, Anderson Miyoshi

Published in: Gut Pathogens | Issue 1/2014

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Abstract

Background

Many probiotic bacteria have been described as promising tools for the treatment and prevention of inflammatory bowel diseases (IBDs). Most of these bacteria are lactic acid bacteria, which are part of the healthy human microbiota. However, little is known about the effects of transient bacteria present in normal diets, including Lactococcus lactis.

Methods

In the present study, we analysed the immunomodulatory effects of three L. lactis strains in vitro using intestinal epithelial cells. L. lactis NCDO 2118 was administered for 4 days to C57BL/6 mice during the remission period of colitis induced by dextran sodium sulphate (DSS).

Results

Only one strain, L. lactis NCDO 2118, was able to reduce IL-1β-induced IL-8 secretion in Caco-2 cells, suggesting a potential anti-inflammatory effect. Oral treatment using L. lactis NCDO 2118 resulted in a milder form of recurrent colitis than that observed in control diseased mice. This protective effect was not attributable to changes in secretory IgA (sIgA); however, NCDO 2118 administration was associated with an early increase in IL-6 production and sustained IL-10 production in colonic tissue. Mice fed L. lactis NCDO 2118 had an increased number of regulatory CD4+ T cells (Tregs) bearing surface TGF-β in its latent form (Latency-associated peptide-LAP) in the mesenteric lymph nodes and spleen.

Conclusions

Here, we identified a new probiotic strain with a potential role in the treatment of IBD, and we elucidated some of the mechanisms underlying its anti-inflammatory effect.
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Literature
2.
go back to reference LeBlanc JG, Aubry C, Cortes-Perez NG, de Moreno de LeBlanc A, Vergnolle N, Langella P, Azevedo V, Chatel J-M, Miyoshi A, Bermúdez-Humarán LG: Mucosal targeting of therapeutic molecules using genetically modified lactic acid bacteria: an update. FEMS Microbiol Lett. 2013, 344 (1): 1-9.CrossRefPubMed LeBlanc JG, Aubry C, Cortes-Perez NG, de Moreno de LeBlanc A, Vergnolle N, Langella P, Azevedo V, Chatel J-M, Miyoshi A, Bermúdez-Humarán LG: Mucosal targeting of therapeutic molecules using genetically modified lactic acid bacteria: an update. FEMS Microbiol Lett. 2013, 344 (1): 1-9.CrossRefPubMed
4.
go back to reference Marteau P: Ineffectiveness of Lactobacillus johnsonii LA1 for prophylaxis of postoperative recurrence in Crohn's disease: a randomised, double blind, placebo controlled GETAID trial. Gut. 2006, 55: 842-847.PubMedCentralCrossRefPubMed Marteau P: Ineffectiveness of Lactobacillus johnsonii LA1 for prophylaxis of postoperative recurrence in Crohn's disease: a randomised, double blind, placebo controlled GETAID trial. Gut. 2006, 55: 842-847.PubMedCentralCrossRefPubMed
5.
go back to reference Nielsen OH, Munck LK: Drug insight: aminosalicylates for the treatment of IBD. Nat Clin Pract Gastroenterol Hepatol. 2007, 4: 160-170.CrossRefPubMed Nielsen OH, Munck LK: Drug insight: aminosalicylates for the treatment of IBD. Nat Clin Pract Gastroenterol Hepatol. 2007, 4: 160-170.CrossRefPubMed
6.
go back to reference de Moreno de Leblanc A, Del Carmen S, Zurita-Turk M, Santos Rocha C, van de Guchte M, Azevedo V, Miyoshi A, LeBlanc JG: Importance of IL-10 modulation by probiotic microorganisms in gastrointestinal inflammatory diseases. ISRN Gastroenterol. 2011, 2011: 892971.PubMedCentralPubMed de Moreno de Leblanc A, Del Carmen S, Zurita-Turk M, Santos Rocha C, van de Guchte M, Azevedo V, Miyoshi A, LeBlanc JG: Importance of IL-10 modulation by probiotic microorganisms in gastrointestinal inflammatory diseases. ISRN Gastroenterol. 2011, 2011: 892971.PubMedCentralPubMed
7.
go back to reference Cronin M, Ventura M, Fitzgerald GF, van Sinderen D: Progress in genomics, metabolism and biotechnology of bifidobacteria. Int J Food Microbiol. 2011, 149: 4-18.CrossRefPubMed Cronin M, Ventura M, Fitzgerald GF, van Sinderen D: Progress in genomics, metabolism and biotechnology of bifidobacteria. Int J Food Microbiol. 2011, 149: 4-18.CrossRefPubMed
8.
go back to reference Wescombe PA, Heng NC, Burton JP, Chilcott CN, Tagg JR: Streptococcal bacteriocins and the case for Streptococcus salivarius as model oral probiotics. Future Microbiol. 2009, 4: 819-835.CrossRefPubMed Wescombe PA, Heng NC, Burton JP, Chilcott CN, Tagg JR: Streptococcal bacteriocins and the case for Streptococcus salivarius as model oral probiotics. Future Microbiol. 2009, 4: 819-835.CrossRefPubMed
10.
go back to reference Nanda Kumar NS, Balamurugan R, Jayakanthan K, Pulimood A, Pugazhendhi S, Ramakrishna BS: Probiotic administration alters the gut flora and attenuates colitis in mice administered dextran sodium sulfate. J Gastroenterol Hepatol. 2008, 23: 1834-1839.CrossRefPubMed Nanda Kumar NS, Balamurugan R, Jayakanthan K, Pulimood A, Pugazhendhi S, Ramakrishna BS: Probiotic administration alters the gut flora and attenuates colitis in mice administered dextran sodium sulfate. J Gastroenterol Hepatol. 2008, 23: 1834-1839.CrossRefPubMed
11.
go back to reference Castillo NA, DeMorenode LeBlanc A, de Moreno de LeBlanc AM, Galdeano C, Perdigón G: Comparative study of the protective capacity against Salmonella infection between probiotic and nonprobiotic Lactobacilli. J Appl Microbiol. 2013, 114: 861-876.CrossRefPubMed Castillo NA, DeMorenode LeBlanc A, de Moreno de LeBlanc AM, Galdeano C, Perdigón G: Comparative study of the protective capacity against Salmonella infection between probiotic and nonprobiotic Lactobacilli. J Appl Microbiol. 2013, 114: 861-876.CrossRefPubMed
12.
go back to reference Chai W, Burwinkel M, Wang Z, Palissa C, Esch B, Twardziok S, Rieger J, Wrede P, Schmidt MFG: Antiviral effects of a probiotic Enterococcus faecium strain against transmissible gastroenteritis coronavirus. Arch Virol. 2013, 158: 799-807.CrossRefPubMed Chai W, Burwinkel M, Wang Z, Palissa C, Esch B, Twardziok S, Rieger J, Wrede P, Schmidt MFG: Antiviral effects of a probiotic Enterococcus faecium strain against transmissible gastroenteritis coronavirus. Arch Virol. 2013, 158: 799-807.CrossRefPubMed
13.
go back to reference Isolauri E, Rautava S, Salminen S: Probiotics in the development and treatment of allergic disease. Gastroenterol Clin North Am. 2012, 41: 747-762.CrossRefPubMed Isolauri E, Rautava S, Salminen S: Probiotics in the development and treatment of allergic disease. Gastroenterol Clin North Am. 2012, 41: 747-762.CrossRefPubMed
14.
go back to reference Madsen K, Cornish A, Soper P, McKaigney C, Jijon H, Yachimec C, Doyle J, Jewell L, De Simone C: Probiotic bacteria enhance murine and human intestinal epithelial barrier function. Gastroenterology. 2001, 121: 580-591.CrossRefPubMed Madsen K, Cornish A, Soper P, McKaigney C, Jijon H, Yachimec C, Doyle J, Jewell L, De Simone C: Probiotic bacteria enhance murine and human intestinal epithelial barrier function. Gastroenterology. 2001, 121: 580-591.CrossRefPubMed
15.
go back to reference Reiff C, Kelly D: Inflammatory bowel disease, gut bacteria and probiotic therapy. Int J Med Microbiol. 2010, 300: 25-33.CrossRefPubMed Reiff C, Kelly D: Inflammatory bowel disease, gut bacteria and probiotic therapy. Int J Med Microbiol. 2010, 300: 25-33.CrossRefPubMed
16.
go back to reference Jijon HB, Panenka WJ, Madsen KL, Parsons HG: MAP kinases contribute to IL-8 secretion by intestinal epithelial cells via a posttranscriptional mechanism. Am J Physiol Cell Physiol. 2002, 283: C31-C41.CrossRefPubMed Jijon HB, Panenka WJ, Madsen KL, Parsons HG: MAP kinases contribute to IL-8 secretion by intestinal epithelial cells via a posttranscriptional mechanism. Am J Physiol Cell Physiol. 2002, 283: C31-C41.CrossRefPubMed
17.
go back to reference Di Giacinto C, Marinaro M, Sanchez M, Strober W, Boirivant M: Probiotics ameliorate recurrent Th1-mediated murine colitis by inducing IL-10 and IL-10-dependent TGF-beta-bearing regulatory cells. J Immunol. 2005, 174: 3237-3246.CrossRefPubMed Di Giacinto C, Marinaro M, Sanchez M, Strober W, Boirivant M: Probiotics ameliorate recurrent Th1-mediated murine colitis by inducing IL-10 and IL-10-dependent TGF-beta-bearing regulatory cells. J Immunol. 2005, 174: 3237-3246.CrossRefPubMed
18.
go back to reference Zhang L, Li N, Caicedo R, Neu J: Alive and dead Lactobacillus rhamnosus GG decrease tumor necrosis factor-alpha-induced interleukin-8 production in Caco-2 cells. J Nutr. 2005, 135: 1752-1756.PubMed Zhang L, Li N, Caicedo R, Neu J: Alive and dead Lactobacillus rhamnosus GG decrease tumor necrosis factor-alpha-induced interleukin-8 production in Caco-2 cells. J Nutr. 2005, 135: 1752-1756.PubMed
19.
go back to reference Riedel CU, Foata F, Philippe D, Adolfsson O, Eikmanns BJ, Blum S: Anti-inflammatory effects of bifidobacteria by inhibition of LPS-induced NF-kappaB activation. World J Gastroenterol. 2006, 12: 3729-3735.PubMedCentralPubMed Riedel CU, Foata F, Philippe D, Adolfsson O, Eikmanns BJ, Blum S: Anti-inflammatory effects of bifidobacteria by inhibition of LPS-induced NF-kappaB activation. World J Gastroenterol. 2006, 12: 3729-3735.PubMedCentralPubMed
20.
go back to reference Santos Rocha C, Lakhdari O, Blottière HM, Blugeon S, Sokol H, Bermudez-Humaran LG, Azevedo V, Miyoshi A, Doré J, Langella P, Maguin E, van de Guchte M: Anti-inflammatory properties of dairy lactobacilli. Inflamm Bowel Dis. 2012, 18: 657-666.CrossRefPubMed Santos Rocha C, Lakhdari O, Blottière HM, Blugeon S, Sokol H, Bermudez-Humaran LG, Azevedo V, Miyoshi A, Doré J, Langella P, Maguin E, van de Guchte M: Anti-inflammatory properties of dairy lactobacilli. Inflamm Bowel Dis. 2012, 18: 657-666.CrossRefPubMed
21.
go back to reference Kimoto H, Kurisaki J, Tsuji NM, Ohmomo S, Okamoto T: Lactococci as probiotic strains: adhesion to human enterocyte-like Caco-2 cells and tolerance to low pH and bile. Lett Appl Microbiol. 1999, 29: 313-316.CrossRefPubMed Kimoto H, Kurisaki J, Tsuji NM, Ohmomo S, Okamoto T: Lactococci as probiotic strains: adhesion to human enterocyte-like Caco-2 cells and tolerance to low pH and bile. Lett Appl Microbiol. 1999, 29: 313-316.CrossRefPubMed
22.
go back to reference Nishitani Y, Tanoue T, Yamada K, Ishida T, Yoshida M, Azuma T, Mizuno M: Lactococcus lactis subsp. cremoris FC alleviates symptoms of colitis induced by dextran sulfate sodium in mice. Int Immunopharmacol. 2009, 9: 1444-1451.CrossRefPubMed Nishitani Y, Tanoue T, Yamada K, Ishida T, Yoshida M, Azuma T, Mizuno M: Lactococcus lactis subsp. cremoris FC alleviates symptoms of colitis induced by dextran sulfate sodium in mice. Int Immunopharmacol. 2009, 9: 1444-1451.CrossRefPubMed
24.
go back to reference Hoffmann E, Dittrich-Breiholz O, Holtmann H, Kracht M: Multiple control of interleukin-8 gene expression. J Leukoc Biol. 2002, 72: 847-855.PubMed Hoffmann E, Dittrich-Breiholz O, Holtmann H, Kracht M: Multiple control of interleukin-8 gene expression. J Leukoc Biol. 2002, 72: 847-855.PubMed
27.
go back to reference Neurath MF, Pettersson S, Buschenfelde KH M z, Strober W: Local administration of antisense phosphorothioate oligonucleotides to the p65 subunit of NF-kappa B abrogates established experimental colitis in mice. Nat Med. 1996, 2: 998-1004.CrossRefPubMed Neurath MF, Pettersson S, Buschenfelde KH M z, Strober W: Local administration of antisense phosphorothioate oligonucleotides to the p65 subunit of NF-kappa B abrogates established experimental colitis in mice. Nat Med. 1996, 2: 998-1004.CrossRefPubMed
28.
go back to reference Ma D, Forsythe P, Bienenstock J: Live Lactobacillus rhamnosus [corrected] is essential for the inhibitory effect on tumor necrosis factor alpha-induced interleukin-8 expression. Infect Immun. 2004, 72: 5308-5314.PubMedCentralCrossRefPubMed Ma D, Forsythe P, Bienenstock J: Live Lactobacillus rhamnosus [corrected] is essential for the inhibitory effect on tumor necrosis factor alpha-induced interleukin-8 expression. Infect Immun. 2004, 72: 5308-5314.PubMedCentralCrossRefPubMed
29.
go back to reference Bai AP, Ouyang Q, Zhang W, Wang CH, Li SF: Probiotics inhibit TNF-alpha-induced interleukin-8 secretion of HT29 cells. World J Gastroenterol. 2004, 10: 455-457.PubMed Bai AP, Ouyang Q, Zhang W, Wang CH, Li SF: Probiotics inhibit TNF-alpha-induced interleukin-8 secretion of HT29 cells. World J Gastroenterol. 2004, 10: 455-457.PubMed
30.
go back to reference Malin M, Suomalainen H, Saxelin M, Isolauri E: Promotion of IgA immune response in patients with Crohn's disease by oral bacteriotherapy with Lactobacillus GG. Ann Nutr Metab. 1996, 40: 137-145.CrossRefPubMed Malin M, Suomalainen H, Saxelin M, Isolauri E: Promotion of IgA immune response in patients with Crohn's disease by oral bacteriotherapy with Lactobacillus GG. Ann Nutr Metab. 1996, 40: 137-145.CrossRefPubMed
31.
go back to reference O'Sullivan DJ: Screening of intestinal microflora for effective probiotic bacteria. J Agric Food Chem. 2001, 49: 1751-1760.CrossRefPubMed O'Sullivan DJ: Screening of intestinal microflora for effective probiotic bacteria. J Agric Food Chem. 2001, 49: 1751-1760.CrossRefPubMed
32.
go back to reference Okayasu I, Hatakeyama S, Yamada M, Ohkusa T, Inagaki Y, Nakaya R: A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology. 1990, 98: 694-702.PubMed Okayasu I, Hatakeyama S, Yamada M, Ohkusa T, Inagaki Y, Nakaya R: A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology. 1990, 98: 694-702.PubMed
33.
go back to reference Laroui H, Ingersoll SA, Liu HC, Baker MT, Ayyadurai S, Charania MA, Laroui F, Yan Y, Sitaraman SV, Merlin D: Dextran Sodium Sulfate (DSS) Induces Colitis in Mice by Forming Nano-Lipocomplexes with Medium-Chain Length Fatty Acids in the Colon. PLoS One. 2012, 7 (3): e32084.PubMedCentralCrossRefPubMed Laroui H, Ingersoll SA, Liu HC, Baker MT, Ayyadurai S, Charania MA, Laroui F, Yan Y, Sitaraman SV, Merlin D: Dextran Sodium Sulfate (DSS) Induces Colitis in Mice by Forming Nano-Lipocomplexes with Medium-Chain Length Fatty Acids in the Colon. PLoS One. 2012, 7 (3): e32084.PubMedCentralCrossRefPubMed
34.
go back to reference Kimoto H, Mizumachi K, Okamoto T, Kurisaki J: New Lactococcus strain with immunomodulatory activity: enhancement of Th1-type immune response. Microbiol Immunol. 2004, 48: 75-82.CrossRefPubMed Kimoto H, Mizumachi K, Okamoto T, Kurisaki J: New Lactococcus strain with immunomodulatory activity: enhancement of Th1-type immune response. Microbiol Immunol. 2004, 48: 75-82.CrossRefPubMed
35.
go back to reference 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. 2003, 10: 696-701.PubMedCentralPubMed 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. 2003, 10: 696-701.PubMedCentralPubMed
36.
go back to reference Podolsky DK: Mucosal immunity and inflammation. V. Innate mechanisms of mucosal defense and repair: the best offense is a good defense. Am J Physiol. 1999, 277: G495-G499.PubMed Podolsky DK: Mucosal immunity and inflammation. V. Innate mechanisms of mucosal defense and repair: the best offense is a good defense. Am J Physiol. 1999, 277: G495-G499.PubMed
37.
go back to reference Dann SM, Spehlmann ME, Hammond DC, Iimura M, Hase K, Choi LJ, Hanson E, Eckmann L: IL-6-dependent mucosal protection prevents establishment of a microbial niche for attaching/effacing lesion-forming enteric bacterial pathogens. J Immunol. 2008, 180: 6816-6826.PubMedCentralCrossRefPubMed Dann SM, Spehlmann ME, Hammond DC, Iimura M, Hase K, Choi LJ, Hanson E, Eckmann L: IL-6-dependent mucosal protection prevents establishment of a microbial niche for attaching/effacing lesion-forming enteric bacterial pathogens. J Immunol. 2008, 180: 6816-6826.PubMedCentralCrossRefPubMed
38.
go back to reference Grivennikov S, Karin E, Terzic J, Mucida D, Yu GY, Vallabhapurapu S, Scheller J, Rose-John S, Cheroutre H, Eckmann L, Karin M: IL-6 and STAT3 are required for survival of intestinal epithelial cells and development of colitis associated cancer. Cancer Cell. 2009, 16: 103-113.CrossRef Grivennikov S, Karin E, Terzic J, Mucida D, Yu GY, Vallabhapurapu S, Scheller J, Rose-John S, Cheroutre H, Eckmann L, Karin M: IL-6 and STAT3 are required for survival of intestinal epithelial cells and development of colitis associated cancer. Cancer Cell. 2009, 16: 103-113.CrossRef
39.
go back to reference Chalaris A, Adam N, Sina C, Rosenstiel P, Lehmann-Koch J, Schirmacher P, Hartmann D, Cichy J, Gavrilova O, Schreiber S, Jostock T, Matthews V, Hasler R, Becker C, Neurath MF, Reiss K, Saftig P, Scheller J, Rose-John S: Critical role of the disintegrin metalloprotease ADAM17 for intestinal inflammation and regeneration in mice. J Exp Med. 2010, 207: 1617-1624.PubMedCentralCrossRefPubMed Chalaris A, Adam N, Sina C, Rosenstiel P, Lehmann-Koch J, Schirmacher P, Hartmann D, Cichy J, Gavrilova O, Schreiber S, Jostock T, Matthews V, Hasler R, Becker C, Neurath MF, Reiss K, Saftig P, Scheller J, Rose-John S: Critical role of the disintegrin metalloprotease ADAM17 for intestinal inflammation and regeneration in mice. J Exp Med. 2010, 207: 1617-1624.PubMedCentralCrossRefPubMed
40.
go back to reference Scheller J, Chalaris A, Schmidt-Arras D, Rose-John S: The pro- and anti-inflammatory properties of the cytokine interleukin-6. Biochim Biophys Acta. 2011, 1813 (5): 878-888.CrossRefPubMed Scheller J, Chalaris A, Schmidt-Arras D, Rose-John S: The pro- and anti-inflammatory properties of the cytokine interleukin-6. Biochim Biophys Acta. 2011, 1813 (5): 878-888.CrossRefPubMed
41.
go back to reference Shen W, Durum SK: Synergy of IL-23 and Th17 cytokines: new light on inflammatory bowel disease. Neurochem Res. 2010, 35: 940-946.CrossRefPubMed Shen W, Durum SK: Synergy of IL-23 and Th17 cytokines: new light on inflammatory bowel disease. Neurochem Res. 2010, 35: 940-946.CrossRefPubMed
42.
go back to reference Ogawa A, Andoh A, Araki Y, Bamba T, Fujiyama Y: Neutralization of interleukin-17 aggravates dextran sulfate sodium-induced colitis in mice. Clin Immunol. 2004, 110: 55-62.CrossRefPubMed Ogawa A, Andoh A, Araki Y, Bamba T, Fujiyama Y: Neutralization of interleukin-17 aggravates dextran sulfate sodium-induced colitis in mice. Clin Immunol. 2004, 110: 55-62.CrossRefPubMed
43.
go back to reference Gomes-Santos AC, Moreira TG, Castro-Junior AB, Horta BC, Lemos L, Cruz DN, Guimarães MAF, Cara DC, McCafferty D-M, Faria AMC: New insights into the immunological changes in IL-10-deficient mice during the course of spontaneous inflammation in the gut mucosa. Clin Dev Immunol. 2012, 2012: 560817.PubMedCentralCrossRefPubMed Gomes-Santos AC, Moreira TG, Castro-Junior AB, Horta BC, Lemos L, Cruz DN, Guimarães MAF, Cara DC, McCafferty D-M, Faria AMC: New insights into the immunological changes in IL-10-deficient mice during the course of spontaneous inflammation in the gut mucosa. Clin Dev Immunol. 2012, 2012: 560817.PubMedCentralCrossRefPubMed
44.
go back to reference Bouma G, Strober W: The immunological and genetic basis of inflammatory bowel disease. Nat Rev Immunol. 2003, 3: 521-533.CrossRefPubMed Bouma G, Strober W: The immunological and genetic basis of inflammatory bowel disease. Nat Rev Immunol. 2003, 3: 521-533.CrossRefPubMed
46.
go back to reference Veltkamp C: Regulatory CD4 + CD25+ cells reverse imbalances in the T cell pool of bone marrow transplanted TGepsilon26 mice leading to the prevention of colitis. Gut. 2005, 54: 207-214.PubMedCentralCrossRefPubMed Veltkamp C: Regulatory CD4 + CD25+ cells reverse imbalances in the T cell pool of bone marrow transplanted TGepsilon26 mice leading to the prevention of colitis. Gut. 2005, 54: 207-214.PubMedCentralCrossRefPubMed
47.
go back to reference Chen W: Dendritic cells and (CD4+)CD25+ T regulatory cells: crosstalk between two professionals in immunity versus tolerance. Front Biosci. 2006, 11: 1360-1370.CrossRefPubMed Chen W: Dendritic cells and (CD4+)CD25+ T regulatory cells: crosstalk between two professionals in immunity versus tolerance. Front Biosci. 2006, 11: 1360-1370.CrossRefPubMed
49.
go back to reference Jeon SG, Kayama H, Ueda Y, Takahashi T, Asahara T, Tsuji H, Tsuji NM, Kiyono H, Ma JS, Kusu T, Okumura R, Hara H, Yoshida H, Yamamoto M, Nomoto K, Takeda K: Probiotic Bifidobacterium breve induces IL-10-producing Tr1 cells in the colon. PLoS Pathog. 2012, 8: e1002714.PubMedCentralCrossRefPubMed Jeon SG, Kayama H, Ueda Y, Takahashi T, Asahara T, Tsuji H, Tsuji NM, Kiyono H, Ma JS, Kusu T, Okumura R, Hara H, Yoshida H, Yamamoto M, Nomoto K, Takeda K: Probiotic Bifidobacterium breve induces IL-10-producing Tr1 cells in the colon. PLoS Pathog. 2012, 8: e1002714.PubMedCentralCrossRefPubMed
50.
go back to reference Miyoshi A, Jamet E, Commissaire J, Renault P, Langella P, Azevedo V: A xylose-inducible expression system for Lactococcus lactis. FEMS Microbiol Lett. 2004, 239: 205-212.CrossRefPubMed Miyoshi A, Jamet E, Commissaire J, Renault P, Langella P, Azevedo V: A xylose-inducible expression system for Lactococcus lactis. FEMS Microbiol Lett. 2004, 239: 205-212.CrossRefPubMed
51.
go back to reference Chopin A, Chopin MC, Moillo-Batt A, Langella P: Two plasmid-determined restriction and modification systems in Streptococcus lactis. Plasmid. 1984, 11: 260-263.CrossRefPubMed Chopin A, Chopin MC, Moillo-Batt A, Langella P: Two plasmid-determined restriction and modification systems in Streptococcus lactis. Plasmid. 1984, 11: 260-263.CrossRefPubMed
52.
go back to reference Gasson MJ: Plasmid complements of Streptococcus lactis NCDO 712 and other lactic streptococci after protoplast-induced curing. J Bacteriol. 1983, 154: 1-9.PubMedCentralPubMed Gasson MJ: Plasmid complements of Streptococcus lactis NCDO 712 and other lactic streptococci after protoplast-induced curing. J Bacteriol. 1983, 154: 1-9.PubMedCentralPubMed
53.
go back to reference Cooper HS, Murthy SN, Shah RS, Sedergran DJ: Clinicopathologic study of dextran sulfate sodium experimental murine colitis. Lab Invest. 1993, 69: 238-249.PubMed Cooper HS, Murthy SN, Shah RS, Sedergran DJ: Clinicopathologic study of dextran sulfate sodium experimental murine colitis. Lab Invest. 1993, 69: 238-249.PubMed
54.
go back to reference McCafferty DM, Sihota E, Muscara M, Wallace JL, Sharkey KA, Kubes P: Spontaneously developing chronic colitis in IL-10/iNOS double-deficient mice. Am J Physiol Gastrointest Liver Physiol. 2000, 279: G90-G99.PubMed McCafferty DM, Sihota E, Muscara M, Wallace JL, Sharkey KA, Kubes P: Spontaneously developing chronic colitis in IL-10/iNOS double-deficient mice. Am J Physiol Gastrointest Liver Physiol. 2000, 279: G90-G99.PubMed
Metadata
Title
Anti-inflammatory effects of Lactococcus lactis NCDO 2118 during the remission period of chemically induced colitis
Authors
Tessalia Diniz Luerce
Ana Cristina Gomes-Santos
Clarissa Santos Rocha
Thais Garcias Moreira
Déborah Nogueira Cruz
Luísa Lemos
Adna Luciana Sousa
Vanessa Bastos Pereira
Marcela de Azevedo
Kátia Moraes
Denise Carmona Cara
Jean Guy LeBlanc
Vasco Azevedo
Ana Maria Caetano Faria
Anderson Miyoshi
Publication date
01-07-2014
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2014
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/1757-4749-6-33

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