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Research article
Food Microbiology and Biotechnology
Factors Affecting Adhesion of Lactic Acid Bacteria to Caco-2 Cells and Inhibitory Effect on Infection of Salmonella Typhimurium
1Department of Food Nutrition and Science, Tongmyong University, Busan 608-735, Korea, 1Department of Food Science and Technology, Pukyong National University, Busan 608-737, Korea
Received: August 22, 2012; Accepted: September 6, 2012
J. Microbiol. Biotechnol. 2012; 22(12): 1731-1739
Published December 28, 2012 https://doi.org/10.4014/jmb.1208.08049
Copyright © The Korean Society for Microbiology and Biotechnology.
Abstract
In this study, seven strains isolated from mustard leaf
kimchi were screened for their tolerance to simulated
gastric and bile juices, the adhesive properties to Caco-2
cells, and the inhibition ability of Salmonella Typhimurium
ATCC 29631 adhesion. Lactobacillus acidophilus GK20,
Lactobacillus paracasei GK74, and Lactobacillus plantarum
GK81, which were resistant to bile as well as gastric juices,
possessed high bile-salt hydrolase (BSH) activity towards
both sodium glycocholate and sodium taurocholate. The
strongest in vitro adherence of 53.96 ± 4.49% was exhibited
by L. plantarum GK81 followed by L. acidophilus GK20
with adhesion levels of 40.72 ± 9.46%. The adhesion of
these strains was significantly (p < 0.05) reduced after
exposure to pepsin and heating for 30 min at 80oC.
Addition of Ca2+ led to a significant (p < 0.05) increase of
the adhesion of L. acidophilus GK20, but the adhesion
ability of L. plantarum GK81 was not different from the
control by the addition of calcium. In the competition and
exclusion experiment, the adhesion inhibition of S.
Typhimurium by L. plantarum GK81 strain was much
higher than the other strains. Moreover, the exclusion
inhibition of S. Typhimurium by L. acidophilus GK20 was
considerably high, although the inhibition activity of this
strain was lower than L. plantarum GK81.
Keywords
adhesion, Caco-2 cells, probiotics, Salmonella typhimurium
References
- Baptissart, M., A. Vega, S. Maqdasy, F. Caira, S. Baron, J. A. Lobaccaro, and D. H. Volle. 2012. Bile acids: From digestion to cancers. Biochimie 94: 1-14.
- Begley, M., C. Hill, and C. G. M. Gahan. 2006. Bile salt hydrolase activity in probiotics. Appl. Environ. Microbiol. 72:1729-1738.
- Bernet, M. F., D. Brassart, J. R. Neeser, and A. L. Servin. 1994. Lactobacillus acidophilus LA1 binds to cultured human intestinal cell lines and inhibits cell attachment and cell invasion by enterovirulent bacteria. Gut 35: 483-489.
- Chauviere, G., M. H. Coconnier, S. Kerneis, J. Fourniat, and A. L. Servin. 1992. Adhesion of Lactobacillus acidophilus strain LB to human enterocyte-like Caco-2 cells. J. Gen. Microbiol. 138: 1689-1696.
- Chen, X., J. Xu, J. Shuai, J. Chen, Z. Zhang, and W. Fang. 2007. The S-layer proteins of Lactobacillus crispatus strains ZJ001 is responsible for competitive exclusion against Escherichia coli O157:H7 and Salmonella Typhimurium. Int. J. Food Microbiol. 115: 307-312.
- De Smet, I., L. Van Hoorde, M. Vande Woestyne, H. Christiaens, and W. Verstrate. 1995. Significance of bile salt hydrolytic activities of lactobacilli. J. Appl. Bacteriol. 79: 292301.
- Forestier, C., C. De Champs, C. Vatoux, and B. Jolie. 2000. Probiotic activities of Lactobacillus casei rhamnosus: In vitro adherence to intestinal cells and antimicrobial properties. Res. Microbiol. 152: 167-173.
- Fuller, R. 1989. Probiotics in man and animals. J. Appl. Bacteriol. 66: 365-378.
- Granato, D., F. Perotti, I. Masserey, M. Rouvet, M. Golliard, A. Servin, and D. Brassart. 1999. Cell surface-associated lipoteichoic acid acts as an adhesion factor for attachment of Lactobacillus johnsonii La1 to human enterocyte-like Caco-2 cells. Appl. Environ. Microbiol. 35: 1071-1077.
- Greene, J. D. and T. R. Klaenhammer. 1994. Factors involved in adherence of lactobacilli to human Caco-2 cells. Appl. Environ. Microbiol. 60: 4487-4494.
- Gueimonde, M., L. Jalonen, F. He, M. Hiramatus, and S. Salminen. 2006. Adhesion and competitive inhibition and displacement of human enteropathogens by selected lactobacilli. Food Res. Int. 39: 467-471.
- Jensen, H., S. Grimmer, K. Naterstad, and L. Axelsson. 2012. In vitro testing of commercial and potential probiotic lactic acid bacteria. Int. J. Food Microbiol. 153: 216-222.
- Kos, B., J. Suskovic, S. Vukovic, M. Simpraga, J. Frece, and S. Matosic. 2003. Adhesion and aggregation ability of probiotic strain Lactobacillus acidophilus M92. J. Appl. Microbiol. 94:981-987.
- Larsen, N., P. Nissen, and W. G. T. Willats. 2007. The effect of calcium ions on adhesion and competitive exclusion of Lactobacillus ssp. and E. coli O138. Int. J. Food Microbiol. 114: 113-119.
- Li, G. 2012. Intestinal probiotics: Interactions with bile salts and reduction of cholesterol. Procedia Environ. Sci. 12: 1180-1186.
- Lim, S. M. 2010. Resistance to reactive oxygen species and antioxidant activities of some strains of lactic acid bacteria from the mustard leaf kimchi. Kor. J. Microbiol. 46: 375-382.
- Lim, S. M. 2011. Bile salts degradation and cholesterol assimilation ability of Pediococcus pentosaceus MLK isolated from mustard leaf kimchi. Kor. J. Microbiol. 47: 231-240.
- Lim, S. M. and D. S. Im. 2012. Inhibitory effects of antagonistic compounds produced from Lactobacillus brevis MLK27 on adhesion of Listeria monocytogenes KCTC 3569 to HT-29 cells. Food Sci. Biotechnol. 21: 775-784.
- Liong, M. T. and N. P. Shah. 2005. Bile salt deconjugation ability, bile salt hydrolase activity and cholesterol co-precipitation ability of lactobacilli strains. Int. Dairy J. 15: 391-398.
- Lorca, G. L. and G. F. de Valdez. 2001. A low-pH-inducible, stationary-phase acid tolerance response in Lactobacillus acidophilus CRL 639. Curr. Microbiol. 42: 21-25.
- Morata, A. V. I., S. N. Gonzalez, and G. Oliver. 1999. Study of adhesion of Lactobacillus casei CRL 431 to ileal intestinal cells of mice. J. Food Prot. 62: 1430-1434.
- Oelschlaeger, T. A. 2010. Mechanisms of probiotic actions – A review. Int. J. Med. Microbiol. 300: 57-62.
- Ouwehand, A. C., E. M. Tuomola, S. Tolkko, and S. Salminen. 2001. Assessment of adhesion properties of novel probiotic strains to human intestinal mucus. Int. J. Food Microbiol. 64:119-126.
- Ouwehand, A. C., P. V. Kirjavainen, M. M. Gronlund, E. Isolauri, and S. J. Salminen. 1999. Adhesion of probiotic microorganisms to intestinal mucus. Int. Dairy J. 9: 623-630.
- Patel, H. M., S. S. Pandiella, R. H. Wang, and C. Webb. 2004. Influence of malt, wheat, and barley extract on the bile tolerance of selected strains of lactobacilli. Food Microbiol. 21:83-89.
- Reid, G., A. L. Servin, A. W. Bruce, and H. J. Busscher. 1993. Adhesion of three Lactobacillus strains to human urinary and intestinal epithelial cells. Microbios 75: 57-65.
- Reid, G., J. Howard, and B. S. Gan. 2001. Can bacterial interference prevent infection? Trends Microbiol. 9: 424-428.
- Saarel, M., G. Mogensen, R. Fonden, J. Matto, and T. MattilaSandholm. 2000. Probiotic bacteria: Safety, functional and technological properties. J. Biotechnol. 84: 197-215.
- Schar-Zammaretti, P. and J. Ubbink. 2003. The cell wall of lactic acid bacteria: Surface constituents and macromolecular conformations. Biophys. J. 85: 4076-4092.
- Schillinger, U., C. Guigas, and W. H. Holzapfel. 2005. In vitro adherence and other properties of lactobacilli used in probiotic yoghurt-like products. Int. Dairy J. 15: 1289-1297.
- Servin, A. L. and M. H. Coconnier. 2003. Adhesion of probiotic strains to the intestinal mucosa and interaction with pathogens. Best Pract. Res. Clin. Gastroenterol. 17: 741-754.
- Sun, J., G. W. Le, Y. H. Shi, and G. W. Su. 2007. Factors involved in binding of Lactobacillus plantarum Lp6 to rat small intestinal mucus. Lett. Appl. Microbiol. 44: 79-85.
- Tuomola, E. M., A. C. Ouwehand, and S. J. Salminen. 2000. Chemical, physical and enzymatic pre-treatments of probiotic lactobacilli alter their adhesion to human intestinal mucus glycoproteins. Int. J. Food Microbiol. 60: 75-81.
- Tuomola, E., R. Crittenden, M. Playne, E. Isolauri, and S. Salminen. 2001. Quality assurance criteria for probiotic bacteria. Am. J. Clin. Nutr. 73: 393S-398S.
- Velez, M. P., S. C. De Keersmaecker, and J. Vanderleyden. 2007. Adherence factors of Lactobacillus in the human gastrointestinal tract. FEMS Microbiol. Lett. 276: 140-148.
- Vinderola, C. G. and J. A. Reinheimer. 2003. Lactic acid starter and probiotic bacteria: A comparative “in vitro” study of probiotic characteristics and biological barrier resistance. Food Res. Int. 36: 895-904.
- Von Wright, A., T. Vilpponen-Salmela, M. P. Llopis, K. Collins, B. Kiely, F. Shanahan, and C. Dunne. 2002. The survival and colonic adhesion of Bifidobacterium infantis in patients with ulcerative colitis. Int. Dairy J. 12: 197-200.
- Zarate, G., A. V. Morata, C. A. Perez, and S. Gonzalez. 2002. Some factors affecting the adherence of probiotic Propionibacterium acidipropionici CRL 1198 to intestinal epithelial cells. Can. J. Microbiol. 48: 449-457.
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Research article
J. Microbiol. Biotechnol. 2012; 22(12): 1731-1739
Published online December 28, 2012 https://doi.org/10.4014/jmb.1208.08049
Copyright © The Korean Society for Microbiology and Biotechnology.
Factors Affecting Adhesion of Lactic Acid Bacteria to Caco-2 Cells and Inhibitory Effect on Infection of Salmonella Typhimurium
Sung-Mee Lim 1* and Dong-Hyun Ahn 2
1Department of Food Nutrition and Science, Tongmyong University, Busan 608-735, Korea, 1Department of Food Science and Technology, Pukyong National University, Busan 608-737, Korea
Received: August 22, 2012; Accepted: September 6, 2012
Abstract
In this study, seven strains isolated from mustard leaf
kimchi were screened for their tolerance to simulated
gastric and bile juices, the adhesive properties to Caco-2
cells, and the inhibition ability of Salmonella Typhimurium
ATCC 29631 adhesion. Lactobacillus acidophilus GK20,
Lactobacillus paracasei GK74, and Lactobacillus plantarum
GK81, which were resistant to bile as well as gastric juices,
possessed high bile-salt hydrolase (BSH) activity towards
both sodium glycocholate and sodium taurocholate. The
strongest in vitro adherence of 53.96 ± 4.49% was exhibited
by L. plantarum GK81 followed by L. acidophilus GK20
with adhesion levels of 40.72 ± 9.46%. The adhesion of
these strains was significantly (p < 0.05) reduced after
exposure to pepsin and heating for 30 min at 80oC.
Addition of Ca2+ led to a significant (p < 0.05) increase of
the adhesion of L. acidophilus GK20, but the adhesion
ability of L. plantarum GK81 was not different from the
control by the addition of calcium. In the competition and
exclusion experiment, the adhesion inhibition of S.
Typhimurium by L. plantarum GK81 strain was much
higher than the other strains. Moreover, the exclusion
inhibition of S. Typhimurium by L. acidophilus GK20 was
considerably high, although the inhibition activity of this
strain was lower than L. plantarum GK81.
Keywords: adhesion, Caco-2 cells, probiotics, Salmonella typhimurium
References
- Baptissart, M., A. Vega, S. Maqdasy, F. Caira, S. Baron, J. A. Lobaccaro, and D. H. Volle. 2012. Bile acids: From digestion to cancers. Biochimie 94: 1-14.
- Begley, M., C. Hill, and C. G. M. Gahan. 2006. Bile salt hydrolase activity in probiotics. Appl. Environ. Microbiol. 72:1729-1738.
- Bernet, M. F., D. Brassart, J. R. Neeser, and A. L. Servin. 1994. Lactobacillus acidophilus LA1 binds to cultured human intestinal cell lines and inhibits cell attachment and cell invasion by enterovirulent bacteria. Gut 35: 483-489.
- Chauviere, G., M. H. Coconnier, S. Kerneis, J. Fourniat, and A. L. Servin. 1992. Adhesion of Lactobacillus acidophilus strain LB to human enterocyte-like Caco-2 cells. J. Gen. Microbiol. 138: 1689-1696.
- Chen, X., J. Xu, J. Shuai, J. Chen, Z. Zhang, and W. Fang. 2007. The S-layer proteins of Lactobacillus crispatus strains ZJ001 is responsible for competitive exclusion against Escherichia coli O157:H7 and Salmonella Typhimurium. Int. J. Food Microbiol. 115: 307-312.
- De Smet, I., L. Van Hoorde, M. Vande Woestyne, H. Christiaens, and W. Verstrate. 1995. Significance of bile salt hydrolytic activities of lactobacilli. J. Appl. Bacteriol. 79: 292301.
- Forestier, C., C. De Champs, C. Vatoux, and B. Jolie. 2000. Probiotic activities of Lactobacillus casei rhamnosus: In vitro adherence to intestinal cells and antimicrobial properties. Res. Microbiol. 152: 167-173.
- Fuller, R. 1989. Probiotics in man and animals. J. Appl. Bacteriol. 66: 365-378.
- Granato, D., F. Perotti, I. Masserey, M. Rouvet, M. Golliard, A. Servin, and D. Brassart. 1999. Cell surface-associated lipoteichoic acid acts as an adhesion factor for attachment of Lactobacillus johnsonii La1 to human enterocyte-like Caco-2 cells. Appl. Environ. Microbiol. 35: 1071-1077.
- Greene, J. D. and T. R. Klaenhammer. 1994. Factors involved in adherence of lactobacilli to human Caco-2 cells. Appl. Environ. Microbiol. 60: 4487-4494.
- Gueimonde, M., L. Jalonen, F. He, M. Hiramatus, and S. Salminen. 2006. Adhesion and competitive inhibition and displacement of human enteropathogens by selected lactobacilli. Food Res. Int. 39: 467-471.
- Jensen, H., S. Grimmer, K. Naterstad, and L. Axelsson. 2012. In vitro testing of commercial and potential probiotic lactic acid bacteria. Int. J. Food Microbiol. 153: 216-222.
- Kos, B., J. Suskovic, S. Vukovic, M. Simpraga, J. Frece, and S. Matosic. 2003. Adhesion and aggregation ability of probiotic strain Lactobacillus acidophilus M92. J. Appl. Microbiol. 94:981-987.
- Larsen, N., P. Nissen, and W. G. T. Willats. 2007. The effect of calcium ions on adhesion and competitive exclusion of Lactobacillus ssp. and E. coli O138. Int. J. Food Microbiol. 114: 113-119.
- Li, G. 2012. Intestinal probiotics: Interactions with bile salts and reduction of cholesterol. Procedia Environ. Sci. 12: 1180-1186.
- Lim, S. M. 2010. Resistance to reactive oxygen species and antioxidant activities of some strains of lactic acid bacteria from the mustard leaf kimchi. Kor. J. Microbiol. 46: 375-382.
- Lim, S. M. 2011. Bile salts degradation and cholesterol assimilation ability of Pediococcus pentosaceus MLK isolated from mustard leaf kimchi. Kor. J. Microbiol. 47: 231-240.
- Lim, S. M. and D. S. Im. 2012. Inhibitory effects of antagonistic compounds produced from Lactobacillus brevis MLK27 on adhesion of Listeria monocytogenes KCTC 3569 to HT-29 cells. Food Sci. Biotechnol. 21: 775-784.
- Liong, M. T. and N. P. Shah. 2005. Bile salt deconjugation ability, bile salt hydrolase activity and cholesterol co-precipitation ability of lactobacilli strains. Int. Dairy J. 15: 391-398.
- Lorca, G. L. and G. F. de Valdez. 2001. A low-pH-inducible, stationary-phase acid tolerance response in Lactobacillus acidophilus CRL 639. Curr. Microbiol. 42: 21-25.
- Morata, A. V. I., S. N. Gonzalez, and G. Oliver. 1999. Study of adhesion of Lactobacillus casei CRL 431 to ileal intestinal cells of mice. J. Food Prot. 62: 1430-1434.
- Oelschlaeger, T. A. 2010. Mechanisms of probiotic actions – A review. Int. J. Med. Microbiol. 300: 57-62.
- Ouwehand, A. C., E. M. Tuomola, S. Tolkko, and S. Salminen. 2001. Assessment of adhesion properties of novel probiotic strains to human intestinal mucus. Int. J. Food Microbiol. 64:119-126.
- Ouwehand, A. C., P. V. Kirjavainen, M. M. Gronlund, E. Isolauri, and S. J. Salminen. 1999. Adhesion of probiotic microorganisms to intestinal mucus. Int. Dairy J. 9: 623-630.
- Patel, H. M., S. S. Pandiella, R. H. Wang, and C. Webb. 2004. Influence of malt, wheat, and barley extract on the bile tolerance of selected strains of lactobacilli. Food Microbiol. 21:83-89.
- Reid, G., A. L. Servin, A. W. Bruce, and H. J. Busscher. 1993. Adhesion of three Lactobacillus strains to human urinary and intestinal epithelial cells. Microbios 75: 57-65.
- Reid, G., J. Howard, and B. S. Gan. 2001. Can bacterial interference prevent infection? Trends Microbiol. 9: 424-428.
- Saarel, M., G. Mogensen, R. Fonden, J. Matto, and T. MattilaSandholm. 2000. Probiotic bacteria: Safety, functional and technological properties. J. Biotechnol. 84: 197-215.
- Schar-Zammaretti, P. and J. Ubbink. 2003. The cell wall of lactic acid bacteria: Surface constituents and macromolecular conformations. Biophys. J. 85: 4076-4092.
- Schillinger, U., C. Guigas, and W. H. Holzapfel. 2005. In vitro adherence and other properties of lactobacilli used in probiotic yoghurt-like products. Int. Dairy J. 15: 1289-1297.
- Servin, A. L. and M. H. Coconnier. 2003. Adhesion of probiotic strains to the intestinal mucosa and interaction with pathogens. Best Pract. Res. Clin. Gastroenterol. 17: 741-754.
- Sun, J., G. W. Le, Y. H. Shi, and G. W. Su. 2007. Factors involved in binding of Lactobacillus plantarum Lp6 to rat small intestinal mucus. Lett. Appl. Microbiol. 44: 79-85.
- Tuomola, E. M., A. C. Ouwehand, and S. J. Salminen. 2000. Chemical, physical and enzymatic pre-treatments of probiotic lactobacilli alter their adhesion to human intestinal mucus glycoproteins. Int. J. Food Microbiol. 60: 75-81.
- Tuomola, E., R. Crittenden, M. Playne, E. Isolauri, and S. Salminen. 2001. Quality assurance criteria for probiotic bacteria. Am. J. Clin. Nutr. 73: 393S-398S.
- Velez, M. P., S. C. De Keersmaecker, and J. Vanderleyden. 2007. Adherence factors of Lactobacillus in the human gastrointestinal tract. FEMS Microbiol. Lett. 276: 140-148.
- Vinderola, C. G. and J. A. Reinheimer. 2003. Lactic acid starter and probiotic bacteria: A comparative “in vitro” study of probiotic characteristics and biological barrier resistance. Food Res. Int. 36: 895-904.
- Von Wright, A., T. Vilpponen-Salmela, M. P. Llopis, K. Collins, B. Kiely, F. Shanahan, and C. Dunne. 2002. The survival and colonic adhesion of Bifidobacterium infantis in patients with ulcerative colitis. Int. Dairy J. 12: 197-200.
- Zarate, G., A. V. Morata, C. A. Perez, and S. Gonzalez. 2002. Some factors affecting the adherence of probiotic Propionibacterium acidipropionici CRL 1198 to intestinal epithelial cells. Can. J. Microbiol. 48: 449-457.
