Molecular cloning, characterization and comparison of bile salt hydrolases from Lactobacillus johnsonii PF01

Journal of Applied Microbiology

Volumn 114, Issue 1, 2013, Pages 121-133

  Chae, J P ^a   Valeriano, V D ^a   Kim, G B ^b   Kang, D K ^a  

^a Dankook University   (South Korea)

^b Chung Ang University   (South Korea)

Author keywords

Bile salt hydrolase; Glyco conjugated bile salts; Lactobacillus johnsonii; Substrate specificity; Tauro conjugated bile salts

Indexed keywords

BINDING SITES; BODY FLUIDS; CLONING; ESCHERICHIA COLI; GENE EXPRESSION; HYDROLASES; HYDROLYSIS; OLIGONUCLEOTIDES; POLYMERASE CHAIN REACTION;

BILE SALT HYDROLASE; CONJUGATED BILE SALTS; GLYCO-CONJUGATED BILE SALT; HYDROLASE GENE; LACTOBACILLUS JOHNSONII; MOLECULAR CLONING; OLIGONUCLEOTIDE PRIMERS; SUBSTRATE SPECIFICITY; TAURO-CONJUGATED BILE SALT;

SALTS;

AGAROSE; BILE SALT; HYDROLASE; NITRILOTRIACETIC ACID; PENICILLIN V;

BACTERIUM; CLONE; ENZYME ACTIVITY; GENE EXPRESSION; MOLECULAR ANALYSIS; MUTAGENICITY; PH; POLYMERASE CHAIN REACTION; SALT; SUBSTRATE;

ARTICLE; BACTERIAL GENE; BINDING SITE; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME PURIFICATION; ENZYME SPECIFICITY; ESCHERICHIA COLI; EXPRESSION VECTOR; GENE AMPLIFICATION; GENE EXPRESSION; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS GASSERI; LACTOBACILLUS JOHNSONII; MOLECULAR CLONING; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; PH; POLYMERASE CHAIN REACTION; TEMPERATURE;

ESCHERICHIA COLI; LACTOBACILLUS JOHNSONII;

EID: 84871106689     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.12027     Document Type: Article

References (68)

1. Ahn, Y.T., Lim, K.L., Ryu, J.C., Kang, D.-K., Ham, J.S., Jang, Y.H. and Kim, H.U. (2002) Characterization of Lactobacillus acidophilus isolated from piglets and chicken. Asian-Aust J Anim Sci 15, 1790-1797.
2. Anderson, J.W. and Gilliland, S.E. (1999) Effect of fermented milk (yogurt) containing Lactobacillus acidophilus L1 on serum cholesterol in hypercholesterolemic humans. J Am Coll Nutr 18, 43-50.
3. Batta, A.K., Salen, G. and Shefer, S. (1984) Substrate specificity of cholylglycine hydrolase for the hydrolysis of bile acid conjugates. J Biol Chem 259, 15035-15039.
4. Begley, M., Gahan, C.G.M. and Hill, C. (2004) The interaction between bacteria and bile. FEMS Microbiol Rev 29, 625-651.
5. Begley, M., Hill, C. and Gahan, C.G.M. (2006) Bile salt hydrolase activity in probiotics. Appl Environ Microbiol 72, 1729-1738.
6. Bernstein, C., Bernstein, H., Payne, C.M., Dvorakova, K. and Garewal, H. (2005) Bile acids as carcinogens in human gastrointestinal cancers. Mutat Res 589, 47-65.
7. Berr, F., Kullak-Ublick, G.A., Paumgartner, G., Munzing, W. and Hylemon, P.B. (1996) 7α-dehydroxylating bacteria enhance deoxycholic acid input and cholesterol saturation of bile in patients with gallstones. Gastroenterology 111, 1611-1620.
8. Berwal, S.K., Sreejith, R.K. and Pal, J.K. (2010) Distance between RBS and AUG plays an important role in overexpression of recombinant proteins. Anal Biochem 405, 275-277.
9. Burr, T., Mitchell, J., Kolb, A., Minchin, S. and Busby, S. (2000) DNA sequence elements located immediately upstream of the -10 hexamer in Escherichia coli promoters: a systematic study. Nucleic Acids Res 28, 1864-1870.
10. Chikai, T., Nakao, H. and Uchida, K. (1987) Deconjugation of bile acids by human intestinal bacteria implanted in germ-free rats. Lipids 22, 669-671.
11. Chothia, C. and Lesk, A.M. (1986) The relation between the divergence of sequence and structure in proteins. EMBO J 5, 823-826.
12. Christiaens, H., Leer, R.J., Pouwels, P.H. and Verstraete, W. (1992) Cloning and expression of a conjugated bile acid hydrolase gene from Lactobacillus plantarum by using a direct plate assay. Appl Environ Microbiol 58, 3792-3798.
13. Coleman, J.P. and Hudson, L.L. (1995) Cloning and characterization of a conjugated bile acid hydrolase gene from Clostridium perfringens. Appl Environ Microbiol 61, 2514-2520.
14. Corzo, G. and Gilliland, S.E. (1999) Bile salt hydrolase activity of three strains of Lactobacillus acidophilus. J Dairy Sci 82, 472-480.
15. De Smet, I., Van Hoorde, L., Vande Woestyne, M., Christiaens, H. and Verstraete, W. (1995) Significance of bile salt hydrolytic activities of lactobacilli. J Appl Bacteriol 79, 292-301.
16. De Smet, I., De Boever, P. and Verstraete, W. (1998) Cholesterol lowering in pigs through enhanced bacterial bile salt hydrolase activity. Br J Nutr 79, 185-194.
17. Elkins, C.A. and Savage, D.C. (1998) Identification of genes encoding conjugated bile salt hydrolase and transport in Lactobacillus johnsonii 100-100. J Bacteriol 180, 4344-4349.
18. Elkins, C.A., Moser, S.A. and Savage, D.C. (2001) Genes encoding bile salt hydrolases and conjugated bile salt transporters in Lactobacillus johnsonii 100-100 and other Lactobacillus species. Microbiology 147, 3403-3412.
19. Eyssen, H. (1973) Role of gut microflora in metabolism of lipids and sterols. Proc Nutr Soc 32, 59-63.
20. Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S., Wilkins, M.R., Appel, R.D. and Bairoch, A. (2005) Protein identification and analysis tools on the ExPASy server. In The Proteomics Protocols Handbook ed. Walker, J.M. pp. 571-607. Totowa, NJ: Humana Press.
21. Ha, C.-G., Cho, J.-K., Lee, C.-H., Chai, Y.-G., Ha, Y.-A. and Shin, S.-H. (2006) Cholesterol lowering effect of Lactobacillus plantarum isolated from human feces. J Microbiol Biotechnol 16, 1201-1209.
22. Hofmann, A.F. (1989) Concepts of biliary secretion. Dig Dis Sci 34, 16S-20S.
23. Jiang, J., Hang, X., Zhang, M., Liu, X., Li, D. and Yang, H. (2010) Diversity of bile salt hydrolase activities in different lactobacilli toward human bile salts. Ann Microbiol 60, 81-88.
24. Kabsch, W., Kabsch, H. and Eisenberg, D. (1976) Packing in a new crystalline form of glutamine synthetase from Escherichia coli. J Mol Biol 100, 283-291.
25. Kaczanowski, S. and Zielenkiewicz, P. (2010) Why similar protein sequences encode similar three-dimensional structures? Theor Chem Acc 125, 543-550.
26. Kandell, R.L. and Bernstein, C. (1991) Bile salt/acid induction of DNA damage in bacterial and mammalian cells: implications for colon cancer. Nutr Cancer 16, 227-238.
27. Kim, G.-B. and Lee, B.H. (2005) Biochemical and molecular insights into bile salt hydrolase in the gastrointestinal microflora: a review. Asian-Aust J Anim Sci 18, 1505-1512.
28. Kim, G.-B., Yi, S.H. and Lee, B.H. (2004) Purification and characterization of three different types of bile salt hydrolases from Bifidobacterium strains. J Dairy Sci 87, 258-266.
29. Kim, G.-B., Brochet, M. and Lee, B.H. (2005) Cloning and characterization of a bile salt hydrolase (bsh) from Bifidobacterium adolescentis. Biotechnol Lett 27, 817-822.
30. Krieger, E., Nabuurs, S.B. and Vriend, G. (2003) Homology modeling. In Structural Bioinformatics ed. Bourne, P.E. and Weissig, H. pp. 507-521. Hoboken: John Wiley & Sons.
31. Kumar, R.S., Brannigan, J.A., Pundle, A., Prabhune, A., Dodson, G.G. and Suresh, C.G. (2004) Expression, purification, crystallization, and preliminary X-ray diffraction analysis of conjugated bile salt hydrolase from Bifidobacterium longum. Acta Crystallogr D Biol Crystallogr 60, 1665-1667.
32. Kumar, R.S., Brannigan, J.A., Prabhune, A.A., Pundle, A.V., Dodson, G.G., Dodson, E.G. and Suresh, C.G. (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.
33. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of the bacteriophage T4. Nature, 227, 680-685.
34. Lambert, J.M., Bongers, R.S., De Vos, W.M. and Kleerebezem, M. (2008) Functional analysis of four bile salt hydrolase and penicillin acylase family members in Lactobacillus plantarum WCFS1. Appl Environ Microbiol 74, 4719-4726.
35. Larsen, C.T., Sorum, C., Hansen, J.F., Jensen, H.A. and Rasmussen, V. (2000) Blood pressure level and relation to other cardiovascular risk factors in male hypertensive patients without clinical evidence of ischemic heart disease. Blood Press 9, 91-97.
36. Lee, J., Kim, Y., Yun, H.S., Kim, J.G., Oh, S. and Kim, S.H. (2010) Genetic and proteomic analysis of factors affecting serum cholesterol reduction by Lactobacillus acidophilus A4. Appl Environ Microbiol 76, 4829-4835.
37. Lee, J.H., Chae, J.P., Lee, J.Y., Lim, J.S., Kim, G.-B., Ham, J.S., Chun, J. and Kang, D.-K. (2011) Genome sequence of Lactobacillus johnsonii PF01, isolated from piglet feces. J Bacteriol 193, 5030-5031.
38. Liong, M.-T. (2008) Roles of probiotics and prebiotics in colon cancer prevention: postulated mechanisms and in-vivo evidence. Int J Mol Sci 9, 854-863.
39. Liong, M.-T. and Shah, N.P. (2005) Bile salt deconjugation ability, bile salt hydrolase activity and cholesterol co-precipitation ability of lactobacilli strains. Int Dairy J 15, 391-398.
40. Low-Beer, T.S. and Nutter, S. (1978) Colonic bacterial activity, biliary cholesterol saturation, and pathogenesis of gallstones. Lancet, ii, 1063-1065.
41. Lundeen, S.G. and Savage, D.C. (1990) Characterization and purification of bile salt hydrolase from Lactobacillus sp. strain 100-100. J Bacteriol 172, 4171-4177.
42. Lundeen, S.G. and Savage, D.C. (1992) Characterization of an extracellular factor that stimulates bile salt hydrolase activity in Lactobacillus sp. strain 100-100. FEMS Microbiol Lett 94, 121-126.
43. Mamianett, A., Garrido, D., Carducci, C.N. and Vescina, M.C. (1999) Fecal bile acid excretion pattern profile in gallstone patients. Medicina 59, 269-273.
44. McAuliffe, O., Cano, R.J. and Klaenhammer, T.R. (2005) Genetic analysis of two bile salt hydrolase activities in Lactobacillus acidophilus NCFM. Appl Environ Microbiol 71, 4925-4929.
45. McCracken, A. and Timms, P. (1999) Efficiency of transcription from promoter sequence variants in Lactobacillus is both strain and context dependent. J Bacteriol 181, 6569-6572.
46. Moser, S.A. and Savage, D.C. (2001) Bile salt hydrolase activity and resistance to toxicity of conjugated bile salts are unrelated properties in Lactobacilli. Appl Environ Microbiol 67, 3476-3480.
47. Nagengast, F.M., Grobben, M.J. and Van Munster, I.P. (1995) Role of bile acids in colorectal carcinogenesis. Eur J Cancer 31, 1067-1070.
48. Nguyen, T.D.T., Kang, J.H. and Lee, M.S. (2007) Characterization of Lactobacillus plantarum PH04, a potential probiotic bacterium with cholesterol-lowering effects. Int J Food Microbiol 113, 358-361.
49. Oh, H.-K., Lee, J.Y., Lim, S.J., Kim, M.J., Kim, G.-B., Kim, J.H., Hong, S.-K. and Kang, D.-K. (2008) Molecular cloning and characterization of a bile salt hydrolase from Lactobacillus acidophilus PF01. J Microbiol Biotechnol 18, 449-456.
50. Ohara, T., Yoshino, K. and Kitajima, M. (2010) Possibility of preventing colorectal carcinogenesis with probiotics. Hepatogastroenterology 57, 1411-1415.
51. Oinonen, C. and Rouvinen, J. (2000) Structural comparison of Ntn-hydrolases. Protein Sci 9, 2329-2337.
52. Park, S.Y., Ko, Y.T., Jeong, H.K., Yang, J.O., Chung, H.S., Kim, Y.B. and Ji, G.E. (1996) Effect of various lactic acid bacteria on the serum cholesterol levels in rats and resistance to acid, bile and antibiotics. Korean J Microbiol Biotechnol 24, 304-310.
53. Park, Y.H., Kim, J.G., Shin, Y.W., Kim, S.H. and Hwang, K.Y. (2007) Effect of dietary inclusion of Lactobacillus acidophilus ATCC 43121 on cholesterol metabolism in rats. J Microbiol Biotechnol 17, 655-662.
54. Patel, A.K., Singhania, R.R., Pandey, A. and Chinkolar, S.B. (2010) Probiotic bile salt hydrolase: current developments and perspectives. Appl Biochem Biotechnol 162, 166-180.
55. Ridlon, J.M., Kang, D.-J. and Hylemon, P.B. (2006) Bile salt biotransformations by human intestinal bacteria. J Lipid Res 47, 241-259.
56. Rossocha, M., Schultz-Heienbrok, R., Von Moeller, H., Coleman, J.P. and Saenger, W. (2005) Conjugated bile acid hydrolase is a tetrameric n-terminal thiol hydrolase with specific recognition of its cholyl but not of its tauryl product. Biochemistry 44, 5739-5748.
57. Russell, D.W. (2003) The enzymes, regulation, and genetics of bile acid synthesis. Annu Rev Biochem 72, 137-174.
58. Sambrook, J. and Russell, D.W. (2001) Molecular Cloning. A Laboratory Manual, 3rd edn. New York, NY: Cold Spring Harbor Laboratory Press.
59. Sander, C. and Schneider, R. (1991) Database of homology-derived protein structures and the structural meaning of sequence alignment. Proteins 9, 56-58.
60. Shin, Y.-R., Lim, K.B., Chae, J.P. and Kang, D.K. (2011) Characterization of anti-Listerial substance produced by Lactobacillus salivarius LCH1227. Korean J Food Sci Ani Resour 31, 609-616.
61. Tanaka, H., Doesburg, K., Iwasaki, T. and Mierau, I. (1999) Screening of lactic acid bacteria for bile salt hydrolase activity. J Dairy Sci 82, 2530-2535.
62. Tanaka, H., Kok, H.J. and Mierau, I. (2000) Bile salt hydrolase of Bifidobacterium longum: biochemical and genetic characterization. Appl Environ Microbiol 66, 2502-2512.
63. Tannock, G.W. (1995) Microecology of the gastrointestinal tract in relation to lactic acid bacteria. Int Dairy J 5, 1059-1070.
64. Taranto, M.P., Sesma, F. and Font de Valdez, G. (1999) Localization and primary characterization of bile salt hydrolase from Lactobacillus reuteri. Biotechnol Lett 21, 935-938.
65. Thompson, J.D., Higgins, D.G. and Gibson, T.J. (1994) Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673-4680.
66. Tikkanen, R., Riikonen, A., Oinonen, C., Rouvinen, J. and Peltonen, L. (1996) Functional analyses of active site residues of human lysosomal aspartylglucosaminidase: implications for catalytic mechanism and autocatalytic activation. EMBO J 15, 2954-2960.
67. Veysey, M.J., Thomas, L.A., Mallet, A.I., Jenkins, P.J., Besser, G.M., Wass, J.A., Murphy, G.M. and Dowling, R.H. (1999) Prolonged large bowel transit increases serum deoxycholic acid: a risk factor for octreotide induced gallstones. Gut 44, 675-681.
68. Yip, K.Y., Utz, L., Sitwell, S., Hu, X., Sidhu, S.S., Turk, B.E., Gerstein, M. and Kim, P.M. (2011) Identification of specificity determining residues in peptide recognition domains using an information theoretical approach applied to large-scale binding maps. BMC Biol 9, 53.