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Research article

Food Microbiology and Biotechnology

Protective Effects of a Novel Probiotic Strain of Lactobacillus plantarum JSA22 from Traditional Fermented Soybean Food Against Infection by Salmonella enterica Serovar Typhimurium

Jeong Seon Eom 1, Jin Song 1 and Hye Sun Choi 1*

Department of Agro-food Resources, National Academy of Agricultural Science, Jeollabuk-do 565-851, Republic of Korea

Received: January 6, 2015; Accepted: January 20, 2015

J. Microbiol. Biotechnol. 2015; 25(4): 479-491

Published April 28, 2015 https://doi.org/10.4014/jmb.1501.01006

Copyright © The Korean Society for Microbiology and Biotechnology.

Abstract

Lactobacillus species have been shown to enhance intestinal epithelial barrier function, modulate host immune responses, and suppress the growth of pathogenic bacteria, yeasts, molds, and viruses. Thus, lactobacilli have been used as probiotics for treating various diseases, including intestinal disorders, and as biological preservatives in the food and agricultural industries. However, the molecular mechanisms used by lactobacilli to suppress pathogenic bacterial infections have been poorly characterized. We previously isolated Lactobacillus plantarum JSA22 from buckwheat sokseongjang, a traditional Korean fermented soybean food, which possessed high enzymatic, fibrinolytic, and broad-spectrum antimicrobial activity against foodborne pathogens. In this study, we investigated the effects of L. plantarum JSA22 on the growth of S. Typhimurium and S. Typhimurium-induced cytotoxicity by stimulating the host immune response in intestinal epithelial cells. The results showed that coincubation of S. Typhimurium and L. plantarum JSA22 with intestinal epithelial cells suppressed S. Typhimurium infection, S. Typhimurium-induced NF-κB activation, and IL-8 production, and lowered the phosphorylation of both Akt and p38. These data indicated that L. plantarum JSA22 has probiotic properties, and can inhibit S. Typhimurium infection of intestinal epithelial cells. Our findings can be used to develop therapeutic and prophylactic agents against pathogenic bacteria.

Keywords

Lactobacillus plantarum JSA22, Salmonella Typhimurium, probiotic, intestinal epithelial cells, prophylactic agents

References

  1. Ahn YJ, Choi HS. 2014. Potential probiotic properties of exopolysaccharide producing lactic acid bacteria isolated from fermented soybean product. J. Korean Soc. Food Sci. Nutr. 43: 749-755.
    CrossRef
  2. Behnsen J, Deriu E, Sassone-Cors M, Raffatellu M. 2013. Probiotics: properties, examples, and specific applications. Cold Spring Harbor Perspect. Med. 3: a010074.
    Pubmed PMC CrossRef
  3. Boirivant M, Strober W. 2007. The mechanism of action of probiotics. Curr. Opin. Gastroenterol. 23: 679-692.
    Pubmed CrossRef
  4. Collado MC, Sanz Y. 2007. Induction of acid resistance in Bifidobacterium: a mechanism for improving desirable traits of potentially probiotic strains. J. Appl. Microbiol. 103: 1147-1157.
    Pubmed CrossRef
  5. Das JK, Mishra D, Ray P, Tripathy P, Beuria TK, Singh N , Suar M. 2013. In vitro evaluation of anti-infective activity of a Lactobacillus plantarum strain against Salmonella enterica serovar Enteritidis. Gut Pathog. 5: 11.
    Pubmed PMC CrossRef
  6. Del Re B, Sgorbati B, Miglioli M, Palenzona D. 2000. Adhesion, autoaggregation and hydrophobicity of 13 strains of Bifidobacterium longum. Lett. Appl. Microbiol. 31: 438-442.
    Pubmed CrossRef
  7. Ewaschuk JB, Naylor JM, Chirino-Trejo M, Zello GA. 2004. Lactobacillus rhamnosus strain GG is a potential probiotic for calves. Can. J. Vet. Res. 68: 249-253.
    Pubmed PMC
  8. Fabrega A, Vila J. 2013. Salmonella enterica serovar Typhimurium skills to succeed in the host: virulence and regulation. Clin. Microbiol. Rev. 26: 308-341.
    Pubmed PMC CrossRef
  9. Gantois I, Ducatelle R , P asmans F , Haesebrouck F, Hautefort I, Thompson A, et al. 2006. Butyrate specifically down-regulates Salmonella pathogenicity island 1 gene expression. Appl. Environ. Microbiol. 72: 946-949.
    Pubmed PMC CrossRef
  10. Guard-Bouldin J, Morales CA, Frye JG, Gast RK, Musgrove M. 2007. Detection of Salmonella enterica subpopulations by phenotype microarray antibiotic resistance patterns. Appl. Environ. Microbiol. 73: 7753-7756.
    Pubmed PMC CrossRef
  11. Ingham CJ, Beerthuyzen M, van Hylckama Vlieg J. 2008. Population heterogeneity of Lactobacillus plantarum WCFS1 microcolonies in response to and recovery from acid stress. Appl. Environ. Microbiol. 74: 7750-7758.
    Pubmed PMC CrossRef
  12. Iqbal M Z, Qadir M I, Hussain T , Janbaz KH, Khan YH, Ahmad B. 2014. Probiotics and their beneficial effects against various diseases. Pak. J. Pharm. Sci. 27: 405-415.
    Pubmed
  13. Jang SE, Hyam SR, Han MJ, Kim S Y, Lee B G, Kim D H. 2013. Lactobacillus brevis G-101 ameliorates colitis in mice by inhibiting NF-kappaB, MAPK and AKT pathways and by polarizing M1 macrophages to M2-like macrophages. J. Appl. Microbiol. 115: 888-896.
    Pubmed CrossRef
  14. Johnson GL, Lapadat R. 2002. Mitogen-activated protein kinase p athways mediated b y ERK, JNK, and p 38 p rotein kinases. Science 298: 1911-1912.
    Pubmed CrossRef
  15. Kailasapathy K, Chin J. 2000. Survival and therapeutic potential of probiotic organisms with reference to Lactobacillus acidophilus and Bifidobacterium spp. Immunol. Cell Biol. 78: 80-88.
    Pubmed CrossRef
  16. Karlsson M, Scherbak N, Reid G, Jass J. 2012. Lactobacillus rhamnosus GR-1 enhances NF-kappaB activation in Escherichia coli-stimulated urinary bladder cells through TLR4. BMC Microbiol. 12: 15.
    Pubmed PMC CrossRef
  17. Kaushik JK, Kumar A , Duary RK, Mohanty AK, Grover S, Batish VK. 2009. Functional and probiotic attributes of an indigenous isolate of Lactobacillus plantarum. PloS One 4: e8099.
    Pubmed PMC CrossRef
  18. Kim GB, Lee BH. 2005. Biochemical and molecular insights into bile salt hydrolase in the gastrointestinal microflora A review. Asian Australas. J. Anim. 18: 1505-1512.
    CrossRef
  19. Kotzamanidis C, Kourelis A, Litopoulou-Tzanetaki E, Tzanetakis N , Yiangou M . 2010. E valuation of a dhesion capacity, cell surface traits and immunomodulatory activity of presumptive probiotic Lactobacillus strains. Int. J. Food Microbiol. 140: 154-163.
    Pubmed CrossRef
  20. Kuijl C, Savage NDL, Marsman M, Tuin AW, Janssen L, Egan DA, et al. 2007. Intracellular bacterial growth is controlled by a kinase network around PKB/AKT1. Nature 450: 725-730.
    Pubmed CrossRef
  21. Kumar RS, Brannigan JA, Prabhune AA, Pundle AV, Dodson GG, Dodson EJ, Suresh CG. 2006. Structural and functional analysis of a conjugated bile salt hydrolase from Bifidobacterium longum reveals an evolutionary relationship with penicillin V acylase. J. Biol. Chem. 281: 32516-32525.
    Pubmed CrossRef
  22. Lee D J, Drongowski RA, Coran A G, Harmon C M. 2 000. Evaluation of probiotic treatment in a neonatal animal model. Pediatr. Surg. Int. 16: 237-242.
    Pubmed CrossRef
  23. Lee JJ, Kwon H, Lee JH, Kim DG, Jung SH, Ma JY. 2014. Fermented soshiho-tang with Lactobacillus plantarum enhances the antiproliferative activity in vascular smooth muscle cell. BMC Complement. Altern. Med. 14: 78.
    Pubmed PMC CrossRef
  24. Lim SM, Ahn DH. 2012. Factors affecting adhesion of lactic acid bacteria to Caco-2 cells and inhibitory effect on infection of Salmonella Typhimurium. J. Microbiol. Biotechnol. 22: 1731-1739.
    Pubmed CrossRef
  25. Lin YP, Thibodeaux CH, Pena JA, Ferry GD, Versalovic J. 2008. Probiotic Lactobacillus reuteri suppress proinflammatory cytokines via c-Jun. Inflamm. Bowel Dis. 14: 1068-1083.
    Pubmed CrossRef
  26. Liong MT. 2008. Roles of probiotics and prebiotics in colon cancer prevention: postulated mechanisms and in-vivo evidence. Int. J. Mol. Sci. 9: 854-863.
    Pubmed PMC CrossRef
  27. Morita H, He F, Fuse T, Ouwehand AC, Hashimoto H, Hosoda M, et al. 2002. Adhesion of lactic acid bacteria to Caco-2 cells and their effect on cytokine secretion. Microbiol. Immunol. 46: 293-297.
    Pubmed CrossRef
  28. Myllyluoma E, Ahonen AM, Korpela R, Vapaatalo H, Kankuri E. 2008. Effects of multispecies probiotic combination on Helicobacter pylori infection in vitro. Clin. Vaccine Immunol. 15: 1472-1482.
    Pubmed PMC CrossRef
  29. Ogunshe AA, Omotoso MA, Bello VB. 2011. The in vitro antimicrobial activities of metabolites from Lactobacillus strains on Candida species implicated in Candida vaginitis. Malays. J. Med. Sci. 18: 13-25.
    Pubmed PMC
  30. Pena JA, Versalovic J. 2003. Lactobacillus rhamnosus GG decreases TNF-alpha production in lipopolysaccharide-activated murine macrophages by a contact-independent mechanism. Cell Microbiol. 5: 277-285.
    Pubmed CrossRef
  31. Peral MC, Rachid MM, Gobbato NM, Huaman Martinez MA, Valdez JC. 2010. Interleukin-8 production by polymorphonuclear leukocytes from patients with chronic infected leg ulcers treated with Lactobacillus plantarum. Clin. Microbiol. Infect. 16:281-286.
    Pubmed CrossRef
  32. Perrett CA, Zhou DG. 2013. Salmonella type III effector SopB modulates host cell exocytosis. Emerg. Microbes Infect. 2: e32.
    Pubmed PMC CrossRef
  33. Pieper GM, Olds C, Hilton G, Lindholm PF, Adams MB, Roza AM. 2001. Antioxidant treatment inhibits activation of myocardial nuclear factor kappa B and inhibits nitrosylation of myocardial heme protein in cardiac transplant rejection. Antioxid. Redox Signal. 3: 81-88.
    Pubmed CrossRef
  34. Ribeiro VB, Lincopan N, Landgraf M, Franco BD, Destro MT. 2011. Characterization of class 1 integrons and antibiotic resistance genes in multidrug-resistant Salmonella enterica isolates from foodstuff and related sources. Braz. J. Microbiol. 42: 685-692.
    Pubmed PMC CrossRef
  35. Roselli M, Finamore A, Britti MS, Konstantinov SR, Smidt H, de Vos WM, Mengheri E. 2007. The novel porcine Lactobacillus sobrius strain protects intestinal cells from enterotoxigenic Escherichia coli K88 infection and prevents membrane barrier damage. J. Nutr. 137: 2709-2716.
    Pubmed
  36. Saarinen M, Ekman P , I keda M, Virtala M , Gronberg A, Yu DTY, et al. 2002. Invasion of Salmonella into human intestinal epithelial cells is modulated by HLA-B27. Rheumatology 41: 651-657.
    Pubmed CrossRef
  37. Tan Z , H uang M , Puga A, Xia Y . 2004. A critical r ole for MAP kinases in the control of Ah receptor complex activity. Toxicol. Sci. 82: 80-87.
    Pubmed CrossRef
  38. Thirabunyanon M, Thongwittaya N. 2012. Protection activity of a novel probiotic strain of Bacillus subtilis against Salmonella Enteritidis infection. Res. Vet. Sci. 93: 74-81.
    Pubmed CrossRef
  39. Wang S, Kotamraju S, Konorev E, Kalivendi S, Joseph J, Kalyanaraman B. 2002. Activation of nuclear factor-kappaB during doxorubicin-induced apoptosis in endothelial cells and myocytes is pro-apoptotic: the role of hydrogen peroxide. Biochem. J. 367: 729-740.
    Pubmed PMC CrossRef
  40. Xu H, Jeong HS, Lee HY, Ahn J. 2009. Assessment of cell surface properties and adhesion potential of selected probiotic strains. Lett. Appl. Microbiol. 49: 434-442.
    Pubmed CrossRef
  41. Yan F, Polk DB. 2002. Probiotic bacterium prevents cytokineinduced apoptosis in intestinal epithelial cells. J. Biol. Chem. 277: 50959-50965.
    Pubmed PMC CrossRef
  42. Yang X, B risbin J, Yu H, Wang Q, Y in F , Zhang Y , et al. 2014. Selected lactic acid-producing bacterial isolates with the capacity to reduce Salmonella translocation and virulence gene expression in chickens. PloS One 9: e93022.
    Pubmed PMC CrossRef
  43. Yu Z, Zhang X, Li S, Li C, Li D, Yang Z. 2013. Evaluation of probiotic properties of Lactobacillus plantarum strains isolated from Chinese sauerkraut. World J. Microbiol. Biotechnol. 29:489-498.
    Pubmed CrossRef
  44. Zago M, Fornasari ME, Carminati D, Burns P, Suarez V, Vinderola G, et al. 2011. Characterization and probiotic potential of Lactobacillus plantarum strains isolated from cheeses. Food Microbiol. 28: 1033-1040.
    Pubmed CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2015; 25(4): 479-491

Published online April 28, 2015 https://doi.org/10.4014/jmb.1501.01006

Copyright © The Korean Society for Microbiology and Biotechnology.

Protective Effects of a Novel Probiotic Strain of Lactobacillus plantarum JSA22 from Traditional Fermented Soybean Food Against Infection by Salmonella enterica Serovar Typhimurium

Jeong Seon Eom 1, Jin Song 1 and Hye Sun Choi 1*

Department of Agro-food Resources, National Academy of Agricultural Science, Jeollabuk-do 565-851, Republic of Korea

Received: January 6, 2015; Accepted: January 20, 2015

Abstract

Lactobacillus species have been shown to enhance intestinal epithelial barrier function,
modulate host immune responses, and suppress the growth of pathogenic bacteria, yeasts,
molds, and viruses. Thus, lactobacilli have been used as probiotics for treating various
diseases, including intestinal disorders, and as biological preservatives in the food and
agricultural industries. However, the molecular mechanisms used by lactobacilli to suppress
pathogenic bacterial infections have been poorly characterized. We previously isolated
Lactobacillus plantarum JSA22 from buckwheat sokseongjang, a traditional Korean fermented
soybean food, which possessed high enzymatic, fibrinolytic, and broad-spectrum antimicrobial
activity against foodborne pathogens. In this study, we investigated the effects of L. plantarum
JSA22 on the growth of S. Typhimurium and S. Typhimurium-induced cytotoxicity by
stimulating the host immune response in intestinal epithelial cells. The results showed that coincubation
of S. Typhimurium and L. plantarum JSA22 with intestinal epithelial cells
suppressed S. Typhimurium infection, S. Typhimurium-induced NF-κB activation, and IL-8
production, and lowered the phosphorylation of both Akt and p38. These data indicated that
L. plantarum JSA22 has probiotic properties, and can inhibit S. Typhimurium infection of
intestinal epithelial cells. Our findings can be used to develop therapeutic and prophylactic
agents against pathogenic bacteria.

Keywords: Lactobacillus plantarum JSA22, Salmonella Typhimurium, probiotic, intestinal epithelial cells, prophylactic agents

References

  1. Ahn YJ, Choi HS. 2014. Potential probiotic properties of exopolysaccharide producing lactic acid bacteria isolated from fermented soybean product. J. Korean Soc. Food Sci. Nutr. 43: 749-755.
    CrossRef
  2. Behnsen J, Deriu E, Sassone-Cors M, Raffatellu M. 2013. Probiotics: properties, examples, and specific applications. Cold Spring Harbor Perspect. Med. 3: a010074.
    Pubmed KoreaMed CrossRef
  3. Boirivant M, Strober W. 2007. The mechanism of action of probiotics. Curr. Opin. Gastroenterol. 23: 679-692.
    Pubmed CrossRef
  4. Collado MC, Sanz Y. 2007. Induction of acid resistance in Bifidobacterium: a mechanism for improving desirable traits of potentially probiotic strains. J. Appl. Microbiol. 103: 1147-1157.
    Pubmed CrossRef
  5. Das JK, Mishra D, Ray P, Tripathy P, Beuria TK, Singh N , Suar M. 2013. In vitro evaluation of anti-infective activity of a Lactobacillus plantarum strain against Salmonella enterica serovar Enteritidis. Gut Pathog. 5: 11.
    Pubmed KoreaMed CrossRef
  6. Del Re B, Sgorbati B, Miglioli M, Palenzona D. 2000. Adhesion, autoaggregation and hydrophobicity of 13 strains of Bifidobacterium longum. Lett. Appl. Microbiol. 31: 438-442.
    Pubmed CrossRef
  7. Ewaschuk JB, Naylor JM, Chirino-Trejo M, Zello GA. 2004. Lactobacillus rhamnosus strain GG is a potential probiotic for calves. Can. J. Vet. Res. 68: 249-253.
    Pubmed KoreaMed
  8. Fabrega A, Vila J. 2013. Salmonella enterica serovar Typhimurium skills to succeed in the host: virulence and regulation. Clin. Microbiol. Rev. 26: 308-341.
    Pubmed KoreaMed CrossRef
  9. Gantois I, Ducatelle R , P asmans F , Haesebrouck F, Hautefort I, Thompson A, et al. 2006. Butyrate specifically down-regulates Salmonella pathogenicity island 1 gene expression. Appl. Environ. Microbiol. 72: 946-949.
    Pubmed KoreaMed CrossRef
  10. Guard-Bouldin J, Morales CA, Frye JG, Gast RK, Musgrove M. 2007. Detection of Salmonella enterica subpopulations by phenotype microarray antibiotic resistance patterns. Appl. Environ. Microbiol. 73: 7753-7756.
    Pubmed KoreaMed CrossRef
  11. Ingham CJ, Beerthuyzen M, van Hylckama Vlieg J. 2008. Population heterogeneity of Lactobacillus plantarum WCFS1 microcolonies in response to and recovery from acid stress. Appl. Environ. Microbiol. 74: 7750-7758.
    Pubmed KoreaMed CrossRef
  12. Iqbal M Z, Qadir M I, Hussain T , Janbaz KH, Khan YH, Ahmad B. 2014. Probiotics and their beneficial effects against various diseases. Pak. J. Pharm. Sci. 27: 405-415.
    Pubmed
  13. Jang SE, Hyam SR, Han MJ, Kim S Y, Lee B G, Kim D H. 2013. Lactobacillus brevis G-101 ameliorates colitis in mice by inhibiting NF-kappaB, MAPK and AKT pathways and by polarizing M1 macrophages to M2-like macrophages. J. Appl. Microbiol. 115: 888-896.
    Pubmed CrossRef
  14. Johnson GL, Lapadat R. 2002. Mitogen-activated protein kinase p athways mediated b y ERK, JNK, and p 38 p rotein kinases. Science 298: 1911-1912.
    Pubmed CrossRef
  15. Kailasapathy K, Chin J. 2000. Survival and therapeutic potential of probiotic organisms with reference to Lactobacillus acidophilus and Bifidobacterium spp. Immunol. Cell Biol. 78: 80-88.
    Pubmed CrossRef
  16. Karlsson M, Scherbak N, Reid G, Jass J. 2012. Lactobacillus rhamnosus GR-1 enhances NF-kappaB activation in Escherichia coli-stimulated urinary bladder cells through TLR4. BMC Microbiol. 12: 15.
    Pubmed KoreaMed CrossRef
  17. Kaushik JK, Kumar A , Duary RK, Mohanty AK, Grover S, Batish VK. 2009. Functional and probiotic attributes of an indigenous isolate of Lactobacillus plantarum. PloS One 4: e8099.
    Pubmed KoreaMed CrossRef
  18. Kim GB, Lee BH. 2005. Biochemical and molecular insights into bile salt hydrolase in the gastrointestinal microflora A review. Asian Australas. J. Anim. 18: 1505-1512.
    CrossRef
  19. Kotzamanidis C, Kourelis A, Litopoulou-Tzanetaki E, Tzanetakis N , Yiangou M . 2010. E valuation of a dhesion capacity, cell surface traits and immunomodulatory activity of presumptive probiotic Lactobacillus strains. Int. J. Food Microbiol. 140: 154-163.
    Pubmed CrossRef
  20. Kuijl C, Savage NDL, Marsman M, Tuin AW, Janssen L, Egan DA, et al. 2007. Intracellular bacterial growth is controlled by a kinase network around PKB/AKT1. Nature 450: 725-730.
    Pubmed CrossRef
  21. Kumar RS, Brannigan JA, Prabhune AA, Pundle AV, Dodson GG, Dodson EJ, Suresh CG. 2006. Structural and functional analysis of a conjugated bile salt hydrolase from Bifidobacterium longum reveals an evolutionary relationship with penicillin V acylase. J. Biol. Chem. 281: 32516-32525.
    Pubmed CrossRef
  22. Lee D J, Drongowski RA, Coran A G, Harmon C M. 2 000. Evaluation of probiotic treatment in a neonatal animal model. Pediatr. Surg. Int. 16: 237-242.
    Pubmed CrossRef
  23. Lee JJ, Kwon H, Lee JH, Kim DG, Jung SH, Ma JY. 2014. Fermented soshiho-tang with Lactobacillus plantarum enhances the antiproliferative activity in vascular smooth muscle cell. BMC Complement. Altern. Med. 14: 78.
    Pubmed KoreaMed CrossRef
  24. Lim SM, Ahn DH. 2012. Factors affecting adhesion of lactic acid bacteria to Caco-2 cells and inhibitory effect on infection of Salmonella Typhimurium. J. Microbiol. Biotechnol. 22: 1731-1739.
    Pubmed CrossRef
  25. Lin YP, Thibodeaux CH, Pena JA, Ferry GD, Versalovic J. 2008. Probiotic Lactobacillus reuteri suppress proinflammatory cytokines via c-Jun. Inflamm. Bowel Dis. 14: 1068-1083.
    Pubmed CrossRef
  26. Liong MT. 2008. Roles of probiotics and prebiotics in colon cancer prevention: postulated mechanisms and in-vivo evidence. Int. J. Mol. Sci. 9: 854-863.
    Pubmed KoreaMed CrossRef
  27. Morita H, He F, Fuse T, Ouwehand AC, Hashimoto H, Hosoda M, et al. 2002. Adhesion of lactic acid bacteria to Caco-2 cells and their effect on cytokine secretion. Microbiol. Immunol. 46: 293-297.
    Pubmed CrossRef
  28. Myllyluoma E, Ahonen AM, Korpela R, Vapaatalo H, Kankuri E. 2008. Effects of multispecies probiotic combination on Helicobacter pylori infection in vitro. Clin. Vaccine Immunol. 15: 1472-1482.
    Pubmed KoreaMed CrossRef
  29. Ogunshe AA, Omotoso MA, Bello VB. 2011. The in vitro antimicrobial activities of metabolites from Lactobacillus strains on Candida species implicated in Candida vaginitis. Malays. J. Med. Sci. 18: 13-25.
    Pubmed KoreaMed
  30. Pena JA, Versalovic J. 2003. Lactobacillus rhamnosus GG decreases TNF-alpha production in lipopolysaccharide-activated murine macrophages by a contact-independent mechanism. Cell Microbiol. 5: 277-285.
    Pubmed CrossRef
  31. Peral MC, Rachid MM, Gobbato NM, Huaman Martinez MA, Valdez JC. 2010. Interleukin-8 production by polymorphonuclear leukocytes from patients with chronic infected leg ulcers treated with Lactobacillus plantarum. Clin. Microbiol. Infect. 16:281-286.
    Pubmed CrossRef
  32. Perrett CA, Zhou DG. 2013. Salmonella type III effector SopB modulates host cell exocytosis. Emerg. Microbes Infect. 2: e32.
    Pubmed KoreaMed CrossRef
  33. Pieper GM, Olds C, Hilton G, Lindholm PF, Adams MB, Roza AM. 2001. Antioxidant treatment inhibits activation of myocardial nuclear factor kappa B and inhibits nitrosylation of myocardial heme protein in cardiac transplant rejection. Antioxid. Redox Signal. 3: 81-88.
    Pubmed CrossRef
  34. Ribeiro VB, Lincopan N, Landgraf M, Franco BD, Destro MT. 2011. Characterization of class 1 integrons and antibiotic resistance genes in multidrug-resistant Salmonella enterica isolates from foodstuff and related sources. Braz. J. Microbiol. 42: 685-692.
    Pubmed KoreaMed CrossRef
  35. Roselli M, Finamore A, Britti MS, Konstantinov SR, Smidt H, de Vos WM, Mengheri E. 2007. The novel porcine Lactobacillus sobrius strain protects intestinal cells from enterotoxigenic Escherichia coli K88 infection and prevents membrane barrier damage. J. Nutr. 137: 2709-2716.
    Pubmed
  36. Saarinen M, Ekman P , I keda M, Virtala M , Gronberg A, Yu DTY, et al. 2002. Invasion of Salmonella into human intestinal epithelial cells is modulated by HLA-B27. Rheumatology 41: 651-657.
    Pubmed CrossRef
  37. Tan Z , H uang M , Puga A, Xia Y . 2004. A critical r ole for MAP kinases in the control of Ah receptor complex activity. Toxicol. Sci. 82: 80-87.
    Pubmed CrossRef
  38. Thirabunyanon M, Thongwittaya N. 2012. Protection activity of a novel probiotic strain of Bacillus subtilis against Salmonella Enteritidis infection. Res. Vet. Sci. 93: 74-81.
    Pubmed CrossRef
  39. Wang S, Kotamraju S, Konorev E, Kalivendi S, Joseph J, Kalyanaraman B. 2002. Activation of nuclear factor-kappaB during doxorubicin-induced apoptosis in endothelial cells and myocytes is pro-apoptotic: the role of hydrogen peroxide. Biochem. J. 367: 729-740.
    Pubmed KoreaMed CrossRef
  40. Xu H, Jeong HS, Lee HY, Ahn J. 2009. Assessment of cell surface properties and adhesion potential of selected probiotic strains. Lett. Appl. Microbiol. 49: 434-442.
    Pubmed CrossRef
  41. Yan F, Polk DB. 2002. Probiotic bacterium prevents cytokineinduced apoptosis in intestinal epithelial cells. J. Biol. Chem. 277: 50959-50965.
    Pubmed KoreaMed CrossRef
  42. Yang X, B risbin J, Yu H, Wang Q, Y in F , Zhang Y , et al. 2014. Selected lactic acid-producing bacterial isolates with the capacity to reduce Salmonella translocation and virulence gene expression in chickens. PloS One 9: e93022.
    Pubmed KoreaMed CrossRef
  43. Yu Z, Zhang X, Li S, Li C, Li D, Yang Z. 2013. Evaluation of probiotic properties of Lactobacillus plantarum strains isolated from Chinese sauerkraut. World J. Microbiol. Biotechnol. 29:489-498.
    Pubmed CrossRef
  44. Zago M, Fornasari ME, Carminati D, Burns P, Suarez V, Vinderola G, et al. 2011. Characterization and probiotic potential of Lactobacillus plantarum strains isolated from cheeses. Food Microbiol. 28: 1033-1040.
    Pubmed CrossRef