Functional roles of aggregation-promoting-like factor in stress tolerance and adherence of lactobacillus acidophilus NCFM

Applied and Environmental Microbiology

Volumn 76, Issue 15, 2010, Pages 5005-5012

  Goh, Yong Jun ^a   Klaenhammer, Todd R ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SHAPES; COAGGREGATION; DELETION MUTANTS; DIGESTIVE TRACT; GASTRIC JUICE; GENOME ANALYSIS; IN-CELL; IN-SILICO; IN-VITRO; INTESTINAL EPITHELIAL CELLS; INTESTINAL MUCOSA; LACTOBACILLUS ACIDOPHILUS; PATHOGENIC BACTERIUM; QUANTITATIVE PCR; REFERENCE STRAINS; REVERSE TRANSCRIPTASES; SECRETED PROTEIN; SELF AGGREGATION; SODIUM DODECYL SULFATE; STATIONARY PHASE; STRESS TOLERANCE; SURVIVAL RATE;

BACTERIA; BODY FLUIDS; CELL CULTURE; DIGESTIVE SYSTEM; GENES; SODIUM; SODIUM SULFATE;

PROTEINS;

ADHESIN; ANTIINFECTIVE AGENT; DETERGENT; DODECYL SULFATE SODIUM; FIBRONECTIN; MUCIN; PROTEIN BINDING;

BACTERIUM; BIOASSAY; CYTOLOGY; GROWTH RATE; MORPHOLOGY; MUTAGENICITY; PHENOTYPE; POLYMERASE CHAIN REACTION; PROTEIN; REAL TIME; SURVIVAL;

ARTICLE; BACTERIUM ADHERENCE; BILE; CHEMISTRY; DRUG EFFECT; EPITHELIUM CELL; GENE DELETION; GENE EXPRESSION PROFILING; GENETICS; LACTOBACILLUS ACIDOPHILUS; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; MOLECULAR WEIGHT; PHYLOGENY; PHYSIOLOGY; PROTEIN BINDING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; STOMACH JUICE; DRUG EFFECTS; TOXICITY;

ADHESINS, BACTERIAL; ANTI-BACTERIAL AGENTS; BACTERIAL ADHESION; BILE; DETERGENTS; EPITHELIAL CELLS; FIBRONECTINS; GASTRIC JUICE; GENE DELETION; GENE EXPRESSION PROFILING; LACTOBACILLUS ACIDOPHILUS; MICROBIAL VIABILITY; MOLECULAR WEIGHT; MUCINS; PHYLOGENY; PROTEIN BINDING; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY, AMINO ACID; SODIUM DODECYL SULFATE;

BACTERIA (MICROORGANISMS); LACTOBACILLUS; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS ACIDOPHILUS NCFM;

EID: 77955588375     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00030-10     Document Type: Article

References (48)

1. Altermann, E., W. M. Russell, M. A. Azcarate-Peril, R. Barrangou, B. L. Buck, O. McAuliffe, N. Souther, A. Dobson, T. Duong, M. Callanan, S. Lick, A. Hamrick, R. Cano, and T. R. Klaenhammer. 2005. Complete genome sequence of the probiotic lactic acid bacterium Lactobacillus acidophilus NCFM. Proc. Natl. Acad. Sci. U. S. A. 102: 3906-3912.
2. Azcarate-Peril, M. A., E. Altermann, R. L. Hoover-Fitzula, R. J. Cano, and T. R. Klaenhammer. 2004. Identification and inactivation of genetic loci involved with Lactobacillus acidophilus acid tolerance. Appl. Environ. Microbiol. 70: 5315-5322.
3. Azcarate-Peril, M. A., J. M. Bruno-Barcena, H. M. Hassan, and T. R. Klaenhammer. 2006. Transcriptional and functional analysis of oxalyl-coenzyme A (CoA) decarboxylase and formyl-CoA transferase genes from Lactobacillus acidophilus. Appl. Environ. Microbiol. 72: 1891-1899.
4. Azcarate-Peril, M. A., O. McAuliffe, E. Altermann, S. Lick, W. M. Russell, and T. R. Klaenhammer. 2005. Microarray analysis of a two-component regulatory system involved in acid resistance and proteolytic activity in Lactobacillus acidophilus. Appl. Environ. Microbiol. 71: 5794-5804.
5. Azcarate-Peril, M. A., R. Talion, and T. R. Klaenhammer. 2009. Temporal gene expression and probiotic attributes of Lactobacillus acidophilus during growth in milk. J. Dairy Sci. 92: 870-886.
6. Barefoot, S. F., and T. R. Klaenhammer. 1983. Detection and activity of lactacin B, a bacteriocin produced by Lactobacillus acidophilus. Appl. Environ. Microbiol. 45: 1808-1815.
7. Barrangou, R., E. Altermann, R. Hutkins, R. Cano, and T. R. Klaenhammer. 2003. Functional and comparative genomic analyses of an operon involved in fructooligosaccharide utilization by Lactobacillus acidophilus. Proc. Natl. Acad. Sci. U. S. A. 100: 8957-8962.
8. Barrangou, R., M. A. Azcarate-Peril, T. Duong, S. B. Conners, R. M. Kelly, and T. R. Klaenhammer. 2006. Global analysis of carbohydrate utilization by Lactobacillus acidophilus using cDNA microarrays. Proc. Natl. Acad. Sci. U. S. A. 103: 3816-3821.
9. Bendtsen, J. D., H. Nielsen, G. von Heijne, and S. Brunak. 2004. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340: 783-795.
10. Boris, S., J. E. Suarez, and C. Barbes. 1997. Characterization of the aggregation promoting factor from Lactobacillus gasseri, a vaginal isolate. J. Appl. Microbiol. 83: 413-420.
11. Buck, B. L., E. Altermann, T. Svingerud, and T. R. Klaenhammer. 2005. Functional analysis of putative adhesion factors in Lactobacillus acidophilus NCFM. Appl. Environ. Microbiol. 71: 8344-8351.
12. Bujnakova, D., and V. Kmet. 2002. Aggregation of animal lactobacilli with 0157 enterohemorrhagic Escherichia coli. J. Vet. Med. B Infect. Dis. Vet. Public Health 49: 152-154.
13. Cesena, C., L. Morelli, M. Alander, T. Siljander, E. Tuomola, S. Salminen, T. Mattila-Sandholm, T. Vilpponen-Salmela, and A. von Wright. 2001. Lactobacillus crispatus and its nonaggregating mutant in human colonization trials. J. Dairy Sci. 84: 1001-1010.
14. Charteris, W. P., P. M. Kelly, L. Morelli, and J. K. Collins. 1998. Development and application of an in vitro methodology to determine the transit tolerance of potentially probiotic Lactobacillus and Bifidobacterium species in the upper human gastrointestinal tract. J. Appl. Microbiol. 84: 759-768.
15. Collado, M. C., J. Meriluoto, and S. Salminen. 2008. Adhesion and aggregation properties of probiotic and pathogen strains. Eur. Food Res. Technol. 226: 1065-1073.
16. Collado, M. C., J. Meriluoto, and S. Salminen. 2007. Role of commercial probiotic strains against human pathogen adhesion to intestinal mucus. Lett. Appl. Microbiol. 45: 454-460.
17. Dobson, A. E., R. B. Sanozky-Dawes, and T. R. Klaenhammer. 2007. Identification of an operon and inducing peptide involved in the production of lactacin B by Lactobacillus acidophilus. J. Appl. Microbiol. 103: 1766-1778.
18. Engelbrektson, A. L., J. R. Korzenik, M. E. Sanders, B. G. Clement, G. Lever, T. R. Klaenhammer, and C. L. Kitts. 2006. Analysis of treatment effects on the microbial ecology of the human intestine. FEMS Microbiol. Ecol. 57: 239-250.
19. Felis, G. E., F. Dellaglio, and S. Torriani. 2009. Taxonomy of probiotic microorganisms, p. 591-637. In D. Charalampopoulos and R. A. Rastall (ed.), Prebiotics and probiotics science and technology, vol. 1. Springer, New York, NY.
20. Foligne, B., S. Nutten, C. Grangette, V. Dennin, D. Goudercourt, S. Poiret, J. Dewulf, D. Brassart, A. Mercenier, and B. Pot. 2007. Correlation between in vitro and in vivo immunomodulatory properties of lactic acid bacteria. World J. Gastroenterol. 13: 236-243.
21. Frece, J., B. Kos, I. K. Svetec, Z. Zgaga, V. Mrsa, and J. Suskovic. 2005. Importance of S-layer proteins in probiotic activity of Lactobacillus acidophilus M92. J. Appl. Microbiol. 98: 285-292.
22. Giffard, P. M., and N. A. Jacques. 1994. Definition of a fundamental repeating unit in streptococcal glucosyltransferase glucan-binding regions and related sequences. J. Dent. Res. 73: 1133-1141.
23. Goh, Y. J., M. A. Azcarate-Peril, S. O'Flaherty, E. Durmaz, F. Valence, J. Jardin, S. Lortal, and T. R. Klaenhammer. 2009. Development and application of a upp-based counterselective gene replacement system for the study of the S-layer protein SlpX of Lactobacillus acidophilus NCFM. Appl. Environ. Microbiol. 75: 3093-3105.
24. Goh, Y. J., C. Zhang, A. K. Benson, V. Schlegel, J. H. Lee, and R. W. Hutkins. 2006. Identification of a putative operon involved in fructooligosaccharide utilization by Lactobacillus paracasei. Appl. Environ. Microbiol. 72: 7518-7530.
25. Horton, R. M., H. D. Hunt, S. N. Ho, J. K. Pullen, and L. R. Pease. 1989. Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77: 61-68.
26. Jankovic, I., M. Ventura, V. Meylan, M. Rouvet, M. Elli, and R. Zink. 2003. Contribution of aggregation-promoting factor to maintenance of cell shape in Lactobacillus gasseri 4B2. J. Bacteriol. 185: 3288-3296.
27. Kim, H. S., and S. E. Gilliland. 1983. Lactobacillus acidophilus as a dietaiy adjunct for milk to aid lactose digestion in humans. J. Dairy Sci. 66: 959-966.
28. Kimmel, S. A., and R. F. Roberts. 1998. Development of a growth medium suitable for exopolysaccharide production by Lactobacillus delbmeckii ssp. bulgaricus RR. Int. J. Food Microbiol. 40: 87-92.
29. Klaenhammer, T. R., and W. M. Russell. 2000. Species of the Lactobacillus acidophilus complex, p. 1151-1157. In R. K. Robinson, C. Batt, and P. D. Patel (ed.), Encyclopedia of food microbiology, vol. 2. Academic Press, San Diego, CA.
30. Larkin, M. A., G. Blackshields, N. P. Brown, R. Chenna, P. A. McGettigan, H. McWilliam, F. Valentin, I. M. Wallace, A. Wilm, R. Lopez, J. D. Thompson, T. J. Gibson, and D. G. Higgins. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
31. Law, J., G. Buist, A. Haandrikman, J. Kok, G. Venema, and K. Leenhouts. 1995. A system to generate chromosomal mutations in Lactococcus lactis which allows fast analysis of targeted genes. J. Bacteriol. 177: 7011-7018.
32. Leyer, G. J., S. Li, M. E. Mubasher, C. Reifer, and A. C. Ouwehand. 2009. Probiotic effects on cold and influenza-like symptom incidence and duration in children. Pediatrics 124: el72-el79.
33. Lozo, J., B. Jovcic, M. Kojic, M. Dalgalarrondo, J. M. Chobert, T. Haertle, and L. Topisirovic. 2007. Molecular characterization of a novel bacteriocin and an unusually large aggregation factor of Lactobacillus paracasei subsp. paracasei BGSJ2-8, a natural isolate from homemade cheese. Curr. Microbiol. 55: 266-271.
34. Marcotte, H., S. Ferrari, C. Cesena, L. Hammarstrom, L. Morelli, G. Pozzi, and M. R. Oggioni. 2004. The aggregation-promoting factor of Lactobacillus crispatus M247 and its genetic locus. J. Appl. Microbiol. 97: 749-756.
35. Narimatsu, M., Y. Noiri, S. Itoh, N. Noguchi, T. Kawahara, and S. Ebisu. 2004. Essential role for the gtfA gene encoding a putative glycosyltransferase in the adherence of Porphyromonas gingivalis. Infect. Immun. 72: 2698-2702.
36. Paineau, D., D. Carcano, G. Leyer, S. Darquy, M. A. Alyanakian, G. Simoneau, J. F. Bergmann, D. Brassart, F. Bornet, and A. C. Ouwehand. 2008. Effects of seven potential probiotic strains on specific immune responses in healthy adults: a double-blind, randomized, controlled trial. FEMS Immunol. Med. Microbiol. 53: 107-113.
37. Pfeiler, E. A., M. A. Azcarate-Peril, and T. R. Klaenhammer. 2007. Characterization of a novel bile-inducible operon encoding a two-component regulatory system in Lactobacillus acidophilus. J. Bacteriol. 189: 4624-4634.
38. Pfeiler, E. A., and T. R. Klaenhammer. 2009. Role of transporter proteins in bile tolerance of Lactobacillus acidophilus. Appl. Environ. Microbiol. 75: 6013-6016.
39. Reniera, R., P. Cocconcelli, V. Bottazzi, and L. Morelli. 1992. High frequency of conjugation in Lactobacillus mediated by an aggregation-promoting factor. J. Gen. Microbiol. 138: 763-768.
40. Roos, S., S. Lindgren, and H. Jonsson. 1999. Autoaggregation of Lactobacillus reuteri is mediated by a putative DEAD-box helicase. Mol. Microbiol. 32: 427-436.
41. T surface protein Cpf mediating coaggregation with and aggregation among pathogens. Appl. Environ. Microbiol. 70: 7078-7085.
42. Siciliano, R. A., G. Cacace, M. F. Mazzeo, L. Morelli, M. Elli, M. Rossi, and A. Malorni. 2008. Proteomic investigation of the aggregation phenomenon in Lactobacillus crispatus. Biochim. Biophys. Acta 1784: 335-342.
43. Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24: 1596-1599.
44. Turner, M. S., L. M. Hafner, T. Walsh, and P. M. Giffard. 2004. Identification and characterization of the novel LysM domain-containing surface protein Sep from Lactobacillus fermentum BR11 and its use as a peptide fusion partner in Lactobacillus and Lactococcus. Appl. Environ. Microbiol. 70: 3673-3680.
45. Ventura, M., I. Jankovic, D. C. Walker, R. D. Pridmore, and R. Zink. 2002. Identification and characterization of novel surface proteins in Lactobacillus johnsonii and Lactobacillus gasseri. Appl. Environ. Microbiol. 68: 6172-6181.
46. Voltan, S., I. Castagliuolo, M. Elli, S. Longo, P. Brun, R. D'Inca, A. Porzionato, V. Macchi, G. Palu, G. C. Sturniolo, L. Morelli, and D. Martines. 2007. Aggregating phenotype in Lactobacillus crispatus determines intestinal colonization and TLR2 and TLR4 modulation in murine colonic mucosa. Clin. Vaccine Immunol. 14: 1138-1148.
47. Walter, J., C. Schwab, D. M. Loach, M. G. Ganzle, and G. W. Tannock. 2008. Glucosyltransferase A (GtfA) and inulosucrase (Inu) of Lactobacillus reuteri TMW1.106 contribute to cell aggregation, in vitro biofilm formation, and colonization of the mouse gastrointestinal tract. Microbiology 154: 72-80.
48. Yamaguchi, T., K. Kasamo, M. Chuman, M. Machigashira, M. Inoue, and T. Sueda. 1998. Preparation and characterization of an Actinomyces naeslundii aggregation factor that mediates coaggregation with Porphyromonas gingivalis. J. Periodontal Res. 33: 460-468.