Cloning, expression, and characterization of two β-glucosidases from isoflavone glycoside-hydrolyzing Bacillus subtilis natto

Journal of Agricultural and Food Chemistry

Volumn 56, Issue 1, 2008, Pages 119-125

  Kuo, Lun Cheng ^a   Lee, Kung Ta ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

glucosidases; Bacillus subtilis natto; BglH; Isoflavone; YckE

Indexed keywords

CELLULASE; GLYCOSIDE; ISOFLAVONE DERIVATIVE; RECOMBINANT PROTEIN;

ARTICLE; BACILLUS SUBTILIS; ENZYMOLOGY; GENE EXPRESSION; GENETICS; HYDROLYSIS; KINETICS; METABOLISM; MOLECULAR CLONING;

BACILLUS SUBTILIS; CELLULASES; CLONING, MOLECULAR; GENE EXPRESSION; GLYCOSIDES; HYDROLYSIS; ISOFLAVONES; KINETICS; RECOMBINANT PROTEINS;

BACILLUS SUBTILIS; ESCHERICHIA COLI;

EID: 38549170356     PISSN: 00218561     EISSN: None     Source Type: Journal    
DOI: 10.1021/jf072287q     Document Type: Article

References (47)

1. Cappelletti, V.; Fioravanti, L.; Miodini, P.; Di Fronzo, G. Genistein blocks breast cancer cells in the G(2)M phase of the cell cycle. J. Cell Biochem. 2000, 14, 594-600.
2. Miura, T.; Yuan, L.; Sun, B.; Fujii, H.; Yoshida, M.; Wakame, K.; Kosuna, K. Isoflavone aglycon produced by culture of soybean extracts with basidiomycetes and its anti-angiogenic activity. Biosci. Biotechnol. Biochem. 2002, 66, 2626-2631.
3. Ravindranath, M. H.; Muthugounder, S.; Presser, N.; Viswanathan, S. Anticancer therapeutic potential of soy isoflavone, genistein. Adv. Exp. Med. Biol. 2004, 546, 121-165.
4. Anthony, M. S.; Clarkson, T. B.; Hughes, C. L.; Morgan, T. M.; Burke, G. L. Soybean isoflavones improve cardiovascular risk factors without affecting the reproductive system of peripubertal rhesus monkeys. J. Nutr. 1996, 126, 43-50.
5. Goodman-Gruen, D.; Kritz-Silverstein, D. Usual dietary isoflavone intake is associated with cardiovascular disease risk factors in postmenopausal women. J. Nutr. 2001, 131, 1202-1206.
6. Cotter, A.; Cashman, K. D. Genistein appears to prevent early postmenopausal bone loss as effectively as hormone replacement therapy. Nutr. Rev. 2003, 61, 346-351.
7. Weaver, C. M.; Cheong, J. M. Soy isoflavones and bone health: the relationship is still unclear. J. Nutr. 2005, 135, 1243-1247.
8. Joannou, G. E.; Kelly, G. E.; Reeder, A. Y.; Waring, M.; Nelson, C. A urinary profile study of dietary phytoestrogens. The identification and mode of metabolism of new isoflavonoids. J. Steroid Biochem. Mol. Biol. 1995, 54, 167-184.
9. Kelly, G. E.; Joannou, G. E.; Reeder, A. Y.; Nelson, C.; Waring, M. A. The variable metabolic response to dietary isoflavones in humans. Proc. Soc. Exp. Biol. Med. 1995, 208, 40-43.
10. Kawakami, Y.; Tsurugasaki, W.; Nakamura, S.; Osada, K. Comparison of regulative functions between dietary soy isoflavones aglycone and glucoside on lipid metabolism in rats fed cholesterol. J. Nutr. Biochem. 2005, 16, 205-212.
11. Hendrich, S. Bioavailability of isoflavones. J. Chromatogr., B Analyt. Technol. Biomed. Life Sci. 2002, 777, 203-210.
12. Setchell, K. D.; Brown, N. M.; Zimmer-Nechemias, L.; Brashear, W. T.; Wolfe, B. E.; Kirschner, A. S.; Heubi, J. E. Evidence for lack of absorption of soy isoflavone glycosides in humans, supporting the crucial role of intestinal metabolism for bioavailability. Am. J. Clin. Nutr. 2002, 76, 447-453.
13. Brown, J. P. Hydrolysis of glycosides and esters. In Role of the gut flora in toxicity and cancer; Rowland, I. R., Ed.; Academic: San Diego, 1998; pp 109-144.
14. Xu, X.; Harris, K. S.; Wang, H. J.; Murphy, P. A.; Hendrich, S. Bioavailability of soybean isoflavones depends upon gut microflora in women. J. Nutr. 1995, 125, 2307-2315.
15. Chiou, R. Y.; Cheng, S. L. Isoflavone transformation during soybean koji preparation and subsequent miso fermentation supplemented with ethanol and NaCl. J. Agric. Food Chem. 2001, 49, 3656-3660.
16. Ibe, S.; Kumada, K.; Yoshiba, M.; Onga, T. Production of natto which contains a high level of isoflavone aglycons. Nippon Shofuhin Kagaku Kogaku Kaishi 2001, 48, 27-34.
17. Toda, T.; Uesugi, T.; Hirai, K.; Nukaya, H.; Tauji, K.; Ishida, H. New 6-O-acyl isoflavone glycosides from soybeans fermented with Bacillus subtilis (natto). I. 6-O-succinylated isoflavone glycosides and their preventive effects on bone loss in ovariectomized rats fed a calcium-deficient diet. Biol. Pharm. Bull. 1999, 22, 1193-1201.
18. Slavin, J. L.; Karr, S. C.; Hutchins, A. M.; Lampe, J. W. Influence of soybean processing, habitual diet, and soy dose on urinary isoflavonoid excretion. Am. J. Clin. Nutr. 1998, 68, 1492-1495.
19. Tsangalis, D.; Ashton, J. F.; McGill, A. E.; Shah, N. P. Enzymic transformation of isoflavone phytoestrogens in soymilk by β-glucosidase- producing bifidobacteria. J. Food Sci. 2002, 67, 3104-3113.
20. Hessler, P. E.; Larsen, P. E.; Constantinou, A. I.; Schram, K. H.; Weber, J. M. Isolation of isoflavones from soy-based fermentations of the erythromycin-producing bacterium Saccharopolyspora erythraea. Appl. Microbiol. Biotechnol. 1997, 47, 398-404.
21. Esen, A. β-Glucosidase, overview. In β-Glucosidase: Biochemistry and Molecular Biology. Esen A., Ed.; American Chemical Society: Washinton, DC, 1993; pp 1-13.
22. Ghosh, P.; Pamment, N. B.; Martin, W. R. B. Simultaneous saccharification and fermentation of cellulose: Effect of beta-D-glucosidase activity and ethanol inhibition of cellulases. Enzyme Microb. Technol. 1982, 4, 425-430.
23. Lei, V.; Amoa-Awua, W. K.; Brimer, L. Degradation of cyanogenic glycosides by Lactobacillus plantarum strains from spontaneous cassava fermentation and other microorganisms. Int. J. Food Microbiol. 1999, 53, 169-184.
24. Marotti, I.; Bonetti, A.; Biavati, B.; Catizone, P.; Dinelli, G. Biotransformation of common bean (Phaseolus vulgaris L.) flavonoid glycosides by bifidobacterium species from human intestinal origin. J. Agric. Food Chem. 2007, 55, 3913-3919.
25. Kuo, L. C.; Cheng, W. Y.; Wu, R. Y.; Huang, C. J.; Lee, K. T. Hydrolysis of black soybean isoflavone glycosides by Bacillus subtilis natto. Appl. Microbiol. Biotechnol. 2006, 73, 314-320.
26. Choi, Y. B.; Kim, K. S.; Rhee, J. S. Hydrolysis of soybean isoflavone glucosides by lactic acid bacteria. Biotechnol. Lett. 2002, 24, 2113-2116.
27. Matsuda, S.; Norimoto, F.; Matsumoto, Y.; Ohba, R.; Teramoto, Y.; Ohta, N.; Ueda, S. Solubilization of a novel isoflavone glycosidehydrolyzing β-glucosidase from Lactobacillus casei subsp. rhamnosus. J. Ferment. Bioeng. 1994, 77, 439-441.
28. Sambrook, J.; Fritsch, E. F.; Maniatis, T. Molecular cloning; a laboratory manual, 2nd ed.; Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, 1989.
29. Wang, H. J.; Murphy, P. A. Isoflavone content in commercial soybean foods. J. Agric. Food Chem. 1994, 42, 1666-1673.
30. Kunst, F.; Ogasawara, N.; Moszer, I.; Albertini, A. M.; Alloni, G.; Azevedo, V.; Bertero, M. G.; Bessières, P.; Bolotin, A.; Borchert, S.; Borriss, R.; Boursier, L.; Brans, A.; Braun, M.; Brignell, S. C.; Bron, S.; Brouillet, S.; Bruschi, C. V.; Caldwell, B.; Capuano, V.; Carter, N. M.; Choi, S. K.; Codani, J. J.; Connerton, I. F.; Danchin, A.; et al. The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 1997, 390, 249-256.
31. Beguin, P. Molecular biology of cellulose degradation. Annu. Rev. Microbiol. 1990, 44, 219-248.
32. Gräbnitz, F.; Rücknagel, K. P.; Seiss, M.; Staudenbauer, W. L. Nucleotide sequence of the Clostridium thermocellum bglB gene encoding thermostable beta-glucosidase B: homology to fungal beta-glucosidases. Mol. Gen. Genet. 1989, 217, 70-76.
33. Baird, S. D.; Hefford, M. A.; Johnson, D. A.; Sung, W. L.; Yaguchi, M.; Seligy, V. L. The Glu residue in the conserved Asn-Glu-Pro sequence of two highly divergent endo-beta-1,4-glucanases is essential for enzymatic activity. Biochem. Biophys. Res. Commun. 1990, 169, 1035-1039.
34. Hashimoto, W.; Miki, H.; Nankai, H.; Sato, N.; Kawai, S.; Murata, K. Molecular cloning of two genes for β-D-glucosidase in Bacillus sp. GL1 and identification of one as a gellan-degrading enzyme. Arch. Biochem. Biophys. 1998, 360, 1-9.
35. Gekas, V.; Lopez-Levia, M. H. Hydrolysis of lactose. Process Biochem. 1985, 20, 2-12.
36. Paavilainen, S.; Hellman, J.; Korpela, T. Purification, characterization, gene cloning, and sequencing of a new beta-glucosidase from Bacillus circulans subsp. alkalophilus. Appl. Environ. Microbiol. 1993, 59, 927-32.
37. Patchett, M. L.; Daniel, R. M.; Morgan, H. W. Purification and properties of a stable β-glucosidase from an extremely thermophilic anaerobic bacterium. Biochem. J. 1987, 243, 779-787.
38. Krüger, S.; Hecker, M. Regulation of the putative bglPH operon for aryl-β-glucoside utilization in Bacillus subtilis. J. Bacteriol. 1995, 177, 5590-5597.
39. Krüger, S.; Gertz, S.; Hecker, M. Transcriptional analysis of bglPH expression in Bacillus subtilis: evidence for two distinct pathways mediating catabolite repression. J. Bacteriol. 1996, 178, 2637-2644.
40. Minami, Y.; Kanafuji, T.; Miura, K. Purification and characterization of a β-glucosidase from Polygonum tinctorium, which catalyzes preferentially the hydrolysis of indican. Biosci. Biotechnol. Biochem. 1996, 60, 147-149.
41. Yang, L.; Ning, Z. S.; Shi, C. Z.; Chang, Z. Y.; Huan, L. Y. Purification and characterization of an isoflavone-conjugates-hydrolyzing β-glucosidase from endophytic bacterium. J. Agric. Food Chem. 2004, 52, 1940-1944.
42. Hsieh, M. C.; Graham, T. L. Partial purification and characterization of a soybean β-glucosidase with high specific activity towards isoflavone conjugates. Phytochemistry 2001, 58, 995-1005.
43. Hosel, W.; Barz, W. β-glucosidase from Cicer Arietinum L.: purification and properties of isoflavone 7-O-glucoside-specific β-glucosidases. Eur. J. Biochem. 1975, 57, 607-616.
44. Setlow, B.; Cabrera-Hernandez, A.; Cabrera-Martinez, R. M.; Setlow, P. Identification of aryl-phospho-β-D-glucosidases in Bacillus subtilis. Arch. Microbiol. 2004, 181, 60-67.
45. Bhatia, Y.; Mishra, S.; Bisaria, V. S. Micorbial β-glucosidasees: cloning, properties and applications. Crit. Rev. Biotechnol. 2002, 22, 375-407.
46. Ridgway, T. J.; Tucker, G. A. Prospects for the production and use of new improved dietary oestrogens for cardioprotection. Biochem. Soc. Trans. 1997, 25, 59-63.
47. Briante, R.; Patumi, M.; Febbraio, F.; Nucci, R. Production of highly purified hydroxytyrosol from Olea europaea leaf extract biotransformed by hyperthermophilic beta-glycosidase. J. Biotechnol. 2004, 111, 67-77.