Skip to main content
Top
Published in: BMC Immunology 1/2014

Open Access 01-12-2014 | Research article

Immunobiotic Lactobacillus jensenii as immune-health promoting factor to improve growth performance and productivity in post-weaning pigs

Authors: Yoshihito Suda, Julio Villena, Yu Takahashi, Shoichi Hosoya, Yohsuke Tomosada, Kohichiro Tsukida, Tomoyuki Shimazu, Hisashi Aso, Masanori Tohno, Mitsuharu Ishida, Seiya Makino, Shuji Ikegami, Haruki Kitazawa

Published in: BMC Immunology | Issue 1/2014

Login to get access

Abstract

Background

Immunoregulatory probiotics (immunobiotics) have been proposed to improve piglets’ immune system to avoid intestinal infections and reduce unproductive inflammation after weaning. Previously, it was demonstrated that Lactobacillus jensenii TL2937 (LjTL2937) attenuated the inflammatory response triggered by activation of Toll-like receptor 4 (TLR-4) in porcine intestinal epithelial (PIE) cells and antigen presenting cells (APCs) from porcine Peyer’s patches (PP).

Objective

In view of the critical importance of PIE-APCs interactions in the regulation of intestinal immune responses, we aimed to examine the effect of LjTL2937 on activation patterns of APCs from swine PPs in co-cultures with PIE cells. In addition, we investigated whether LjTL2937 was able to beneficially modulate intestinal immunity of piglets after weaning to improve immune-health status.

Results

Stimulation of PIE-APCs co-cultures with LjTL2937 increased the expression of MHC-II, CD80/86, IL-10, and Bcl-3 in CD172a+CD11R1- and CD172a+CD11R1high APCs. In addition, the TL2937 strain caused the upregulation of three negative regulators of TLR4 in PIE cells: MKP-1, Bcl-3 and A20. These changes significantly reduced the inflammatory response triggered by TLR4 activation in PIE-APCs co-cultures. The in vivo experiments using castrated male piglets (crossbreeding (LWD) with Landrace (L), Large Yorkshire (W) and Duroc (D))of 3 weeks of age demonstrated that feeding with LjTL2937 significantly reduced blood complement activity and C reactive protein concentrations while no changes were observed in blood leukocytes, ratio of granulocytes to lymphocyte numbers, macrophages’ activity and antibody levels. In addition, treatment with LjTL2937 significantly improved growth performance and productivity, and increased carcass quality.

Conclusions

We demonstrated that the use of immunobiotics strains like LjTL2937, as supplemental additives for piglets feedings, could be used as a strategy to maintain and improve intestinal homeostasis; that is important for the development of the pig and for health and performance throughout the productive life of the animal.
Appendix
Available only for authorised users
Literature
1.
go back to reference Blecha J: Immunology. Biology of Domestic Pigs. Edited by: Pand WG, Mersmand HJ. 2001, Ithaca, NY, USA: Cornell University, 688-711. Blecha J: Immunology. Biology of Domestic Pigs. Edited by: Pand WG, Mersmand HJ. 2001, Ithaca, NY, USA: Cornell University, 688-711.
2.
go back to reference McCracken BA, Gaskins HR, Ruwekaiser PJ, Klasing KC, Jewell DE: Diet-dependent and diet-independent metabolic responses underlie growth stasis of pigs at weaning. J Nutr. 1995, 125: 2838-2845.PubMed McCracken BA, Gaskins HR, Ruwekaiser PJ, Klasing KC, Jewell DE: Diet-dependent and diet-independent metabolic responses underlie growth stasis of pigs at weaning. J Nutr. 1995, 125: 2838-2845.PubMed
3.
go back to reference McCracken BA, Spurlock ME, Roos MA, Zuckermann FA, Gaskins HR: Weaning anorexia may contribute to local inflammation in the pig- let small intestine. J Nutr. 1999, 129: 613-619.PubMed McCracken BA, Spurlock ME, Roos MA, Zuckermann FA, Gaskins HR: Weaning anorexia may contribute to local inflammation in the pig- let small intestine. J Nutr. 1999, 129: 613-619.PubMed
4.
go back to reference Pié S, Lallès JP, Blazy F, Laffitte J, Sève B, Oswald IP: Weaning is associated with an upregulation of expression of inflammatory cytokines in the intestine of piglets. J Nutr. 2004, 134: 641-647.PubMed Pié S, Lallès JP, Blazy F, Laffitte J, Sève B, Oswald IP: Weaning is associated with an upregulation of expression of inflammatory cytokines in the intestine of piglets. J Nutr. 2004, 134: 641-647.PubMed
5.
go back to reference Williams BA, Verstegen MWA, Tamminga S: Fermentation in the large intestine of single-stomached animals and its relationship to animal health. Nutr Res Rev. 2001, 14: 207-227.PubMedCrossRef Williams BA, Verstegen MWA, Tamminga S: Fermentation in the large intestine of single-stomached animals and its relationship to animal health. Nutr Res Rev. 2001, 14: 207-227.PubMedCrossRef
6.
go back to reference McDermott PF, Walker RD, White DG: Antimicrobials: modes of action and mechanisms of resistance. Int J Toxicol. 2003, 22: 135-143.PubMedCrossRef McDermott PF, Walker RD, White DG: Antimicrobials: modes of action and mechanisms of resistance. Int J Toxicol. 2003, 22: 135-143.PubMedCrossRef
7.
go back to reference Kemper N: Veterinary antibiotics in the aquatic and terrestrial environment. Ecol Indicators. 2003, 8: 1-13.CrossRef Kemper N: Veterinary antibiotics in the aquatic and terrestrial environment. Ecol Indicators. 2003, 8: 1-13.CrossRef
8.
go back to reference Deng J, Li Y, Zhang J, Yang Q: Co-administration of Bacillus subtilis RJGP16 and Lactobacillus salivarius B1 strongly enhances the intestinal mucosal immunity of piglets. Res Vet Sci. 2012, In press Deng J, Li Y, Zhang J, Yang Q: Co-administration of Bacillus subtilis RJGP16 and Lactobacillus salivarius B1 strongly enhances the intestinal mucosal immunity of piglets. Res Vet Sci. 2012, In press
9.
go back to reference Shimazu T, Villena J, Tohno M, Fujie H, Hosoya S, Shimosato T, Aso H, Suda Y, Kawai Y, Saito T, Makino S, Ikegami S, Itoh H, Kitazawa H: Immunobiotic Lactobacillus jensenii elicit anti-inflammatory activity in porcine intestinal epithelial cells by modulating negative regulators of the toll-like receptor signaling pathway. Infect Immun. 2012, 80: 276-288.PubMedPubMedCentralCrossRef Shimazu T, Villena J, Tohno M, Fujie H, Hosoya S, Shimosato T, Aso H, Suda Y, Kawai Y, Saito T, Makino S, Ikegami S, Itoh H, Kitazawa H: Immunobiotic Lactobacillus jensenii elicit anti-inflammatory activity in porcine intestinal epithelial cells by modulating negative regulators of the toll-like receptor signaling pathway. Infect Immun. 2012, 80: 276-288.PubMedPubMedCentralCrossRef
10.
go back to reference Villena J, Suzuki R, Fujie H, Chiba E, Takahashi T, Shimazu T, Aso H, Ohwada S, Suda Y, Ikegami S, Itoh H, Alvarez S, Saito T, Kitazawa H: Immunobiotic Lactobacillus jensenii modulates toll-like receptor 4-induced inflammatory response via negative regulation in porcine antigen presenting cells. Clin Vaccine Immunol. 2012, 19: 1038-1053.PubMedPubMedCentralCrossRef Villena J, Suzuki R, Fujie H, Chiba E, Takahashi T, Shimazu T, Aso H, Ohwada S, Suda Y, Ikegami S, Itoh H, Alvarez S, Saito T, Kitazawa H: Immunobiotic Lactobacillus jensenii modulates toll-like receptor 4-induced inflammatory response via negative regulation in porcine antigen presenting cells. Clin Vaccine Immunol. 2012, 19: 1038-1053.PubMedPubMedCentralCrossRef
11.
go back to reference Villena J, Kitazawa H: Role of Toll-Like Receptors in the Modulation of Intestinal Inflammation by Immunobiotics. Probiotics: Immunobiotics and Immunogenics. Edited by: Kitazawa H, Villena J, Alvarez A. 2013, Boca Raton, Florida, U.S.A: Science Publishers, CRC Press, Taylor & Francis Group company, 89-127.CrossRef Villena J, Kitazawa H: Role of Toll-Like Receptors in the Modulation of Intestinal Inflammation by Immunobiotics. Probiotics: Immunobiotics and Immunogenics. Edited by: Kitazawa H, Villena J, Alvarez A. 2013, Boca Raton, Florida, U.S.A: Science Publishers, CRC Press, Taylor & Francis Group company, 89-127.CrossRef
12.
go back to reference Villena J, Aso H, Alvarez S, Kitazawa H: Porcine Toll-Like Receptors and Their Crosstalk With Immunobiotics: Impact in the Regulation of gut Inflammatory Immunity. Probiotics: Sources, Types and Health Benefits. Edited by: Smith A, Jones CJ. 2012, Hauppauge, New York, U.S.A: Nova, 53-83. Villena J, Aso H, Alvarez S, Kitazawa H: Porcine Toll-Like Receptors and Their Crosstalk With Immunobiotics: Impact in the Regulation of gut Inflammatory Immunity. Probiotics: Sources, Types and Health Benefits. Edited by: Smith A, Jones CJ. 2012, Hauppauge, New York, U.S.A: Nova, 53-83.
13.
go back to reference Rescigno M, Lopatin U, Chieppa M: Interactions among dendritic cells, macrophages, and epithelial cells in the gut: implications for immune tolerance. Curr Opin Immunol. 2008, 20: 669-675.PubMedCrossRef Rescigno M, Lopatin U, Chieppa M: Interactions among dendritic cells, macrophages, and epithelial cells in the gut: implications for immune tolerance. Curr Opin Immunol. 2008, 20: 669-675.PubMedCrossRef
14.
go back to reference Westendorf AM, Fleissner D, Hansen W, Buer J: T cells, dendritic cells and epithelial cells in intestinal homeostasis. Int J Med Microbiol. 2010, 300: 11-18.PubMedCrossRef Westendorf AM, Fleissner D, Hansen W, Buer J: T cells, dendritic cells and epithelial cells in intestinal homeostasis. Int J Med Microbiol. 2010, 300: 11-18.PubMedCrossRef
15.
go back to reference Rimoldi M, Chieppa M, Salucci V, Avogadri F, Sonzogni A, Sampietro GM, Nespoli A, Viale G, Allavena P, Rescigno M: Intestinal immune homeostasis is regulated by the crosstalk between epithelial cells and dendritic cells. Nat Immunol. 2005, 6: 507-514.PubMedCrossRef Rimoldi M, Chieppa M, Salucci V, Avogadri F, Sonzogni A, Sampietro GM, Nespoli A, Viale G, Allavena P, Rescigno M: Intestinal immune homeostasis is regulated by the crosstalk between epithelial cells and dendritic cells. Nat Immunol. 2005, 6: 507-514.PubMedCrossRef
16.
go back to reference Hershberg RM, Mayer LF: Antigen processing and presentation by intestinal epithelial cells-polarity and complexity. Immunol Today. 2000, 21: 123-128.PubMedCrossRef Hershberg RM, Mayer LF: Antigen processing and presentation by intestinal epithelial cells-polarity and complexity. Immunol Today. 2000, 21: 123-128.PubMedCrossRef
17.
go back to reference Blumberg RS: Inflammation in the intestinal tract: pathogenesis and treatment. Digest Dis. 2009, 27: 455-464.CrossRef Blumberg RS: Inflammation in the intestinal tract: pathogenesis and treatment. Digest Dis. 2009, 27: 455-464.CrossRef
18.
go back to reference Fujie H, Villena J, Tohno M, Morie K, Simazu T, Aso H, Suda Y, Iwabuchi N, Xiao J, Iwatsuki K, Kawai Y, Saito T, Kitazawa H: Toll-like receptor-2 activating bifidobacteria strains differentially regulate inflammatory cytokines in porcine intestinal epithelial cell culture system: finding new anti-inflammatory immunobiotics. FEMS Immunol Med Microbiol. 2011, 63: 129-139.PubMedCrossRef Fujie H, Villena J, Tohno M, Morie K, Simazu T, Aso H, Suda Y, Iwabuchi N, Xiao J, Iwatsuki K, Kawai Y, Saito T, Kitazawa H: Toll-like receptor-2 activating bifidobacteria strains differentially regulate inflammatory cytokines in porcine intestinal epithelial cell culture system: finding new anti-inflammatory immunobiotics. FEMS Immunol Med Microbiol. 2011, 63: 129-139.PubMedCrossRef
19.
go back to reference Hosoya S, Villena J, Simazu T, Tohno M, Fujie H, Chiba E, Shimaosato T, Aso H, Suda Y, Kawai Y, Saito T, Alvarez S, Ikegami S, Itoh H, Kitazawa H: Immunobiotic lactic acid bacteria beneficially regulate immune response triggered by poly(I:C) in porcine intestinal epithelial cells. Vet Res. 2011, 42: 111-PubMedPubMedCentralCrossRef Hosoya S, Villena J, Simazu T, Tohno M, Fujie H, Chiba E, Shimaosato T, Aso H, Suda Y, Kawai Y, Saito T, Alvarez S, Ikegami S, Itoh H, Kitazawa H: Immunobiotic lactic acid bacteria beneficially regulate immune response triggered by poly(I:C) in porcine intestinal epithelial cells. Vet Res. 2011, 42: 111-PubMedPubMedCentralCrossRef
20.
go back to reference Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT: The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem. 2009, 55: 611-622.PubMedCrossRef Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT: The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem. 2009, 55: 611-622.PubMedCrossRef
21.
go back to reference Nygard AB, Jorgensen CB, Cirera S, Fredholm M: M: Selection of reference genes for gene expression studies in pig tissues using SYBR green qPCR. BMC Mol Biol. 2007, 8: 67-PubMedPubMedCentralCrossRef Nygard AB, Jorgensen CB, Cirera S, Fredholm M: M: Selection of reference genes for gene expression studies in pig tissues using SYBR green qPCR. BMC Mol Biol. 2007, 8: 67-PubMedPubMedCentralCrossRef
22.
go back to reference Tomosada Y, Villena J, Murata K, Chiba E, Shimazu T, Aso H, Iwabuchi N, Xiao J, Saito T, Kitazawa H: Immunoregulatory effect of bifidobacteria strains in porcine intestinal epithelial cells trough modulation of ubiquitin-editing enzyme A20 expression. PLoS One. 2013, 8: e59259-PubMedPubMedCentralCrossRef Tomosada Y, Villena J, Murata K, Chiba E, Shimazu T, Aso H, Iwabuchi N, Xiao J, Saito T, Kitazawa H: Immunoregulatory effect of bifidobacteria strains in porcine intestinal epithelial cells trough modulation of ubiquitin-editing enzyme A20 expression. PLoS One. 2013, 8: e59259-PubMedPubMedCentralCrossRef
23.
go back to reference Takanashi N, Tomosada Y, Villena J, Murata K, Takahashi T, Chiba E, Tohno M, Shimazu T, Aso H, Suda Y, Ikegami S, Itoh H, Kawai Y, Saito T, Alvarez S, Kitazawa H: Advanced application of bovine intestinal epithelial cell line for evaluating regulatory effect of lactobacilli against heat-killed enterotoxigenic Escherichia coli-mediated inflammation. BMC Microbiol. 2013, 13: 54-PubMedPubMedCentralCrossRef Takanashi N, Tomosada Y, Villena J, Murata K, Takahashi T, Chiba E, Tohno M, Shimazu T, Aso H, Suda Y, Ikegami S, Itoh H, Kawai Y, Saito T, Alvarez S, Kitazawa H: Advanced application of bovine intestinal epithelial cell line for evaluating regulatory effect of lactobacilli against heat-killed enterotoxigenic Escherichia coli-mediated inflammation. BMC Microbiol. 2013, 13: 54-PubMedPubMedCentralCrossRef
24.
go back to reference Fritz JH, Le Bourhis L, Magalhaes JG, Philpott DJ: Innate immune recognition at the epithelial barrier drives adaptive immunity: APCs take the back seat. Trends Immunol. 2007, 29: 41-49.PubMedCrossRef Fritz JH, Le Bourhis L, Magalhaes JG, Philpott DJ: Innate immune recognition at the epithelial barrier drives adaptive immunity: APCs take the back seat. Trends Immunol. 2007, 29: 41-49.PubMedCrossRef
25.
go back to reference Liu YJ, Soumelis V, Watanabe N, Ito T, Wang YH, Malefyt Rde W, Omori M, Zhou B, Ziegler SF: TSLP: an epithelial cell cytokine that regulates T cell differentiation by conditioning dendritic cell maturation. Ann Rev Immunol. 2007, 25: 193-219.CrossRef Liu YJ, Soumelis V, Watanabe N, Ito T, Wang YH, Malefyt Rde W, Omori M, Zhou B, Ziegler SF: TSLP: an epithelial cell cytokine that regulates T cell differentiation by conditioning dendritic cell maturation. Ann Rev Immunol. 2007, 25: 193-219.CrossRef
26.
go back to reference Kuwata H, Watanabe Y, Miyoshi H, Yamamoto M, Kaisho T, Takeda K, Akira S: IL-10-inducible Bcl-3 negatively regulates LPS- induced TNF-alpha production in macrophages. Blood. 2003, 102: 4123-4129.PubMedCrossRef Kuwata H, Watanabe Y, Miyoshi H, Yamamoto M, Kaisho T, Takeda K, Akira S: IL-10-inducible Bcl-3 negatively regulates LPS- induced TNF-alpha production in macrophages. Blood. 2003, 102: 4123-4129.PubMedCrossRef
27.
go back to reference Lalles JP, Boudry G, Favier C, Le Floc’h N, Luron I, Montagne L, Oswald IP, Piel S, Sève B: Gut function and dysfunction in young pigs: physiology. Anim Res. 2004, 53: 301-316.CrossRef Lalles JP, Boudry G, Favier C, Le Floc’h N, Luron I, Montagne L, Oswald IP, Piel S, Sève B: Gut function and dysfunction in young pigs: physiology. Anim Res. 2004, 53: 301-316.CrossRef
28.
go back to reference Lalle’s JP, Bosia P, Smidta H, Stokes CR: Nutritional management of gut health in pigs around weaning. Proceed Nutr Soc. 2007, 66: 260-268.CrossRef Lalle’s JP, Bosia P, Smidta H, Stokes CR: Nutritional management of gut health in pigs around weaning. Proceed Nutr Soc. 2007, 66: 260-268.CrossRef
29.
go back to reference Chowdhury SR, King DE, Willing BP, Band MR, Beever JE, Lane AB, Loor JJ, Marini JC, Rund LA, Schook LB, Van Kessel AG, Gaskins HR: Transcriptome profiling of the small intestinal epithelium in germfree versus conventional piglets. BMC Genomics. 2007, 8: 215-PubMedPubMedCentralCrossRef Chowdhury SR, King DE, Willing BP, Band MR, Beever JE, Lane AB, Loor JJ, Marini JC, Rund LA, Schook LB, Van Kessel AG, Gaskins HR: Transcriptome profiling of the small intestinal epithelium in germfree versus conventional piglets. BMC Genomics. 2007, 8: 215-PubMedPubMedCentralCrossRef
30.
go back to reference Li XQ, Zhu YH, Zhang HF, Yue Y, Cai ZX, Lu QP, Zhang L, Weng XG, Zhang FJ, Zhou D, Yang JC, Wang JF: Risks associated with high-dose Lactobacillus rhamnosus in an Escherichia coli model of piglet diarrhoea: intestinal microbiota and immune imbalances. PLoS One. 2012, 7: e40666-PubMedPubMedCentralCrossRef Li XQ, Zhu YH, Zhang HF, Yue Y, Cai ZX, Lu QP, Zhang L, Weng XG, Zhang FJ, Zhou D, Yang JC, Wang JF: Risks associated with high-dose Lactobacillus rhamnosus in an Escherichia coli model of piglet diarrhoea: intestinal microbiota and immune imbalances. PLoS One. 2012, 7: e40666-PubMedPubMedCentralCrossRef
31.
go back to reference Deng J, Li Y, Zhang J, Yang Q: Co-administration of Bacillus subtilis RJGP16 and Lactobacillus salivarius B1 strongly enhances the intestinal mucosal immunity of piglets. Res Vet Science. 2013, 94: 62-68.CrossRef Deng J, Li Y, Zhang J, Yang Q: Co-administration of Bacillus subtilis RJGP16 and Lactobacillus salivarius B1 strongly enhances the intestinal mucosal immunity of piglets. Res Vet Science. 2013, 94: 62-68.CrossRef
32.
go back to reference Herfel TM, Jacobi SK, Lin X, Jouni ZE, Chichlowski M, Stahl CH, Odle J: Dietary supplementation of Bifidobacterium longum strain AH1206 increases its cecal abundance and elevates intestinal interleukin-10 expression in the neonatal piglet. Food Chem Toxicol. 2013, 60: 116-122.PubMedCrossRef Herfel TM, Jacobi SK, Lin X, Jouni ZE, Chichlowski M, Stahl CH, Odle J: Dietary supplementation of Bifidobacterium longum strain AH1206 increases its cecal abundance and elevates intestinal interleukin-10 expression in the neonatal piglet. Food Chem Toxicol. 2013, 60: 116-122.PubMedCrossRef
33.
go back to reference Chiba E, Tomosada Y, Vizoso-Pinto MG, Takahashi T, Tsukida K, Kitazawa H, Avarez S, Villena J: Immunobiotic Lactobacillus rhamnosus improves resistance of infant mice against respiratory syncytial virus infection. Int Immunopharmacol. 2013, 17: 373-382.PubMedCrossRef Chiba E, Tomosada Y, Vizoso-Pinto MG, Takahashi T, Tsukida K, Kitazawa H, Avarez S, Villena J: Immunobiotic Lactobacillus rhamnosus improves resistance of infant mice against respiratory syncytial virus infection. Int Immunopharmacol. 2013, 17: 373-382.PubMedCrossRef
34.
go back to reference Salva S, Villena J, Alvarez S: Diferential immunomodulatory activity of Lactobacillus rhamnosus strains isolated from goat milk: impact on intestinal and respiratory infections. Int J Food Microbiol. 2010, 141: 82-89.PubMedCrossRef Salva S, Villena J, Alvarez S: Diferential immunomodulatory activity of Lactobacillus rhamnosus strains isolated from goat milk: impact on intestinal and respiratory infections. Int J Food Microbiol. 2010, 141: 82-89.PubMedCrossRef
35.
go back to reference Murata K, Tomosada Y, Villena J, Chiba E, Shimazu T, Aso H, Suda Y, Iwabuchi N, Xiao J, Saito T, Kitazawa H: Bifidobacterium breve MCC-117 induces tolerance in porcine intestinal epithelial cells: study of the mechanisms involved in the immunoregulatory effect. Biosci Microbiot Food Helath. 2014, 33: 1-10.CrossRef Murata K, Tomosada Y, Villena J, Chiba E, Shimazu T, Aso H, Suda Y, Iwabuchi N, Xiao J, Saito T, Kitazawa H: Bifidobacterium breve MCC-117 induces tolerance in porcine intestinal epithelial cells: study of the mechanisms involved in the immunoregulatory effect. Biosci Microbiot Food Helath. 2014, 33: 1-10.CrossRef
Metadata
Title
Immunobiotic Lactobacillus jensenii as immune-health promoting factor to improve growth performance and productivity in post-weaning pigs
Authors
Yoshihito Suda
Julio Villena
Yu Takahashi
Shoichi Hosoya
Yohsuke Tomosada
Kohichiro Tsukida
Tomoyuki Shimazu
Hisashi Aso
Masanori Tohno
Mitsuharu Ishida
Seiya Makino
Shuji Ikegami
Haruki Kitazawa
Publication date
01-12-2014
Publisher
BioMed Central
Published in
BMC Immunology / Issue 1/2014
Electronic ISSN: 1471-2172
DOI
https://doi.org/10.1186/1471-2172-15-24

Other articles of this Issue 1/2014

BMC Immunology 1/2014 Go to the issue