Characterization of the pattern of αs1- and β-casein breakdown and release of a bioactive peptide by a cell envelope proteinase from Lactobacillus delbrueckii subsp. lactis CRL 581

Applied and Environmental Microbiology

Volumn 74, Issue 12, 2008, Pages 3682-3689

  Hebert, Elvira María ^a   Mamone, Gianfranco ^b   Picariello, Gianluca ^b   Raya, Raúl R ^a   Savoy, Graciela ^a   Ferranti, Pasquale ^c   Addeo, Francesco ^c  

^a CENTRO DE REFERENCIA PARA LACTOBACILOS CERELA CONICET   (Argentina)

^b CNR   (Italy)

^c UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDS; AGRICULTURAL PRODUCTS; AMINATION; AMINES; AMINO ACIDS; CARBOHYDRATES; CARBON; DAIRY PRODUCTS; FOOD ADDITIVES; HEALTH; ORGANIC ACIDS; ORGANIC COMPOUNDS; POLYMER BLENDS; PROTEINS; WELL STIMULATION;

ACTIVITY LEVELS; CARBON SOURCES; CASAMINO ACIDS; CASITONE; CELL ENVELOPES; DI-PEPTIDES; FERMENTED MILKS; GROWTH MEDIUM; LACTOBACILLUS DELBRUECKII SUBSP. LACTIS; MILK PROTEINS; ORGANOLEPTIC PROPERTIES; OSMOLITES; SYNTHESIS (OF CHIRAL IONIC LIQUIDS); TRI-PEPTIDES; YEAST EXTRACT (YE);

ENZYME ACTIVITY;

AGAR; BACTERIAL PROTEIN; BETA CASEIN; CASAMINO ACID; CASEIN; DIPEPTIDE; GLYCINE; LEUCYLLEUCINE; OSMOLITE; PROLINE; PROTEINASE; CARBOHYDRATE; CARBON; LIPID; PEPTIDE; PEPTIDE HYDROLASE; VEGETABLE PROTEIN;

BACTERIUM; ENZYME ACTIVITY; NUTRITION; PEPTIDE; PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIUM CULTURE; CULTURE MEDIUM; ENZYME ACTIVITY; LACTOBACILLUS DELBRUECKII; MASS SPECTROMETRY; NONHUMAN; PEPTIDE ANALYSIS; PROTEIN ANALYSIS; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; CHEMISTRY; ENZYME SPECIFICITY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; ISOLATION AND PURIFICATION; KINETICS; METABOLISM; MOLECULAR GENETICS; SEQUENCE ANALYSIS;

BACTERIA (MICROORGANISMS); LACTOBACILLUS DELBRUECKII SUBSP. LACTIS;

AMINO ACID SEQUENCE; CARBOHYDRATES; CARBON; CASEINS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CULTURE MEDIA; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; KINETICS; LACTOBACILLUS DELBRUECKII; LIPIDS; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; PEPTIDE HYDROLASES; PEPTIDES; SEQUENCE ANALYSIS, PROTEIN; SUBSTRATE SPECIFICITY; VEGETABLE PROTEINS;

EID: 45749128307     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.00247-08     Document Type: Article

References (45)

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. USA 102:3906-3912.
2. Caira, S., P. Ferranti, M. Gatti, M. E. Fornasari, F. Barone, S. Lilla, G. Mucchetti, G. Picariello, L. Chianese, E. Neviani, and F. Addeo. 2003. Synthetic peptides as substrate for assaying the proteolytic activity of Lactobacillus helveticus. J. Dairy Res. 70:315-325.
3. den Hengst, C. D., S. A. van Hijum, J. M. Geurts, A. Nauta, J. Kok, and O. P. Kuipers. 2005. The Lactococcus lactis CodY regulon: identification of a conserved cis-regulatory element. J. Biol. Chem. 280:34332-34342.
4. Exterkate, F. A. 1990. Differences in short peptide-substrate cleavage by two cell-envelope-located serine proteinases of Lactococcus lactis subsp. cremoris are related to secondary binding specificity. Appl. Microbiol. Biotechnol. 33:401-406.
5. Exterkate, F. A., A. C. Alting, and P. G. Bruinenberg. 1993. Diversity of cell envelope proteinase specificity among strains of Lactococcus lactis and its relationship to charge characteristics of the substrate-binding region. Appl. Environ. Microbiol. 59:3640-3647.
6. Fox, P. F., and J. M. Wallace. 1997. Formation of flavor compounds in cheese. Adv. Appl. Microbiol. 45:17-85.
7. Fuglsang, A., D. Nilsson, and N. C. Nyborg. 2002. Cardiovascular effects of fermented milk containing angiotensin-converting enzyme inhibitors evaluated in permanently catheterized, spontaneously hypertensive rats. Appl. Environ. Microbiol. 68:3566-3569.
8. Gilbert, C., D. Atlan, B. Blanc, R. Portalier, J. E. Germond, L. Lapierre, and B. Mollet. 1996. A new cell surface proteinase: sequencing and analysis of the prtB gene from Lactobacillus delbrueckii subsp. bulgaricus. J. Bacteriol. 178:3059-3065.
9. Guedon, E., P. Serror, S. D. Ehrlich, P. Renault, and C. Delorme. 2001. Pleiotropic transcriptional repressor CodY senses the intracellular pool of branched-chain amino acids in Lactococcus lactis. Mol. Microbiol. 40:1227-1239.
10. Guedon, E., P. Renault, S. D. Ehrlich, and C. Delorme. 2001. Transcriptional pattern of genes coding for the proteolytic system of Lactococcus lactis and evidence for coordinated regulation of key enzymes by peptide supply. J. Bacteriol. 183:3614-3622.
11. Guedon, E., B. Sperandio, N. Pons, S. D. Ehrlich, and P. Renault. 2005. Overall control of nitrogen metabolism in Lactococcus lactis by CodY, and possible models for CodY regulation in Firmicutes. Microbiology 151:3895-3909.
12. Hartmann, R., and H. Meisel. 2007. Food-derived peptides with biological activity: from research to food applications. Curr. Opin. Biotechnol. 18:163-169.
13. Hata, Y., M. Yamamoto, M. Ohni, K. Nakajima, Y. Nakamura, and T. Takano. 1996. A placebo-controlled study of the effect of sour milk on blood pressure in hypertensive subjects. Am. J. Clin. Nutr. 64:767-771.
14. Hebert, E. M., R. R. Raya, and G. S. De Giori. 2000. Nutritional requirements and nitrogen-dependent regulation of proteinase activity of Lactobacillus helveticus CRL 1062. Appl. Environ. Microbiol. 66:5316-5321.
15. Hebert, E. M., R. R. Raya, and G. S. de Giori. 2002. Modulation of the cell-surface proteinase activity of thermophilic lactobacilli by the peptide supply. Curr. Microbiol. 45:385-389.
16. Hebert, E. M., R. R. Raya, and G. S. de Giori. 2004. Nutritional requirements of Lactobacillus delbrueckii subsp. lactis in a chemically defined medium. Curr. Microbiol. 49:341-345.
17. Holck, A., and H. Naes. 1992. Cloning, sequencing and expression of the gene encoding the cell-envelope-associated proteinase from Lactobacillus paracasei subsp. paracasei NCDO151. J. Gen. Microbiol. 138:1353-1364.
18. Hugenholtz, J., F. A. Exterkate, and W. N. Konings. 1984. The proteolytic systems of Streptococcus cremoris: an immunological analysis. Appl. Environ. Microbiol. 48:1105-1110.
19. Jauhiainen, T., H. Vapaatalo, T. Poussa, S. Kyronpalo, M. Rasmussen, and R. Korpela. 2005. Lactobacillus helveticus fermented milk lowers blood pressure in hypertensive subjects in 24-h ambulatory blood pressure measurement. Am. J. Hypertens. 18:1600-1605.
20. Juillard, V., H. Laan, E. R. S. Kunji, C. M. Jeronimus-Stratingh, A. P. Bruins, and W. N. Konings. 1995. The extracellular PI-type proteinase of Lactococcus lactis hydrolyzes β-casein into more than one hundred different oligopeptides. J. Bacteriol. 177:3472-3478.
21. Kandler, O., and N. Weiss. 1986. Regular, non-sporing gram-positive rods, p. 1208-1234. In P. H. A. Sneath, N. S. Mair, M. E. Sharpe, and J. G. Holt (ed.), Bergey's manual of systematic bacteriology, vol. 1. Williams and Wilkins, Baltimore, MD.
22. Kunji, E. R. S., I. Mierau, A. Hagting, B. Poolman, and W. N. Konings. 1996. The proteolytic systems of lactic acid bacteria. Antonie van Leeuwenhoek 70:187-221.
23. Kunji, E. R., G. Fang, C. M. Jeronimus-Stratingh, A. P. Bruins, B. Poolman, and W. N. Konings. 1998. Reconstruction of the proteolytic pathway for use of β-casein by Lactococcus lactis. Mol. Microbiol. 27:1107-1118.
24. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
25. Laloi, P., D. Atlan, B. Blanc, C. Gilbert, and R. Portalier. 1991. Cell-wall-associated proteinase of Lactobacillus delbrueckii subsp. bulgaricus CNRZ 397: differential extraction, purification and properties of the enzyme. Appl. Microbiol. Biotechnol. 36:196-204.
26. Law, J., and A. Haandrikman. 1997. Proteolytic enzymes of lactic acid bacteria. Int. Dairy J. 7:1-11.
27. Martín-Hernández, M. C., A. C. Alting, and F. A. Exterkate. 1994. Purification and characterization of the mature, membrane-associated cell-envelope proteinase of Lactobacillus helveticus L89. Appl. Microbiol. Biotechnol. 40:828-834.
28. Marugg, J. D., W. Meijer, R. Van Kranenburg, P. Laverman, P. G. Bruinenberg, and W. M. D. Vos. 1995. Medium-dependent regulation of proteinase gene expression in Lactococcus lactis: control of transcription initiation by specific dipeptides. J. Bacteriol. 177:2982-2989.
29. Meijer, W., J. D. Marugg, and J. Hugenholtz. 1996. Regulation of proteolytic enzyme activity in Lactococcus lactis. Appl. Environ. Microbiol. 62:156-161.
30. Meisel, H. 2004. Multifunctional peptides encrypted in milk proteins. Biofactors 21:55-61.
31. Miladinov, N., O. P. Kuipers, and L. Topisirovic. 2001. Casitone-mediated expression of the prtP and prtM genes in Lactococcus lactis subsp. lactis BGIS29. Arch. Microbiol. 177:54-61.
32. Morishita, T., Y. Deguchi, M. Yajima, T. Sakurai, and T. Yura. 1981. Multiple nutritional requirements of lactobacilli: genetic lesions affecting amino acid biosynthetic pathways. J. Bacteriol. 148:64-71.
33. Pastar, I., I. Tonic, N. Golic, M. Kojic, R. van Kranenburg, M. Kleerebezem, L. Topisirovic, and G. Jovanovic. 2003. Identification and genetic characterization of a novel proteinase, PrtR, from the human isolate Lactobacillus rhamnosus BGT10. Appl. Environ. Microbiol. 69:5802-5811.
34. Pederson, J. A., G. J. Mileski, B. C. Weimer, and J. L. Steele. 1999. Genetic characterization of a cell envelope-associated proteinase from Lactobacillus helveticus CNRZ32. J. Bacteriol. 181:4592-4597.
35. Petranovic, D., E. Guedon, B. Sperandio, C. Delorme, D. Ehrlich, and P. Renault. 2004. Intracellular effectors regulating the activity of the Lactococcus lactis CodY pleiotropic transcription regulator. Mol. Microbiol. 53:613-621.
36. Savijoki, K., H. Ingmer, and P. Varmanen. 2006. Proteolytic systems of lactic acid bacteria. Appl. Microbiol. Biotechnol. 71:394-406.
37. Scolari, G., M. Vescovo, C. Zacconi, and F. Vescovi. 2006. Extraction and partial characterization of proteolytic activities from the cell surface of Lactobacillus helveticus Zuc2. J. Dairy Sci. 89:3800-3809.
38. Singh, T. K., N. D. Young, M. Drake, and K. R. Cadwallader. 2005. Production and sensory characterization of a bitter peptide from β-casein. J. Agric. Food Chem. 53:1185-1189.
39. Smeianov, V. V., P. Wechter, J. R. Broadbent, J. E. Hughes, B. T. Rodriguez, T. K. Christensen, Y. Ardo, and J. L. Steele. 2007. Comparative high-density microarray analysis of gene expression during growth of Lactobacillus helveticus in milk versus rich culture medium. Appl. Environ. Microbiol. 73:2661-2672.
40. Sridhar, V. R., J. E. Hughes, D. L. Welker, J. R. Broadbent, and J. L. Steele. 2005. Identification of endopeptidase genes from the genomic sequence of Lactobacillus helveticus CNRZ32 and the role of these genes in hydrolysis of model bitter peptides. Appl. Environ. Microbiol. 71:3025-3032.
41. Thomas, T. D. 1975. Tagatose-1,6-diphosphate activation of lactate dehydrogenase from Streptococcus cremoris. Biochem. Biophys. Res. Commun. 63:1035-1042.
42. Thomas, T. D., and O. E. Mills. 1981. Proteolytic enzymes of starter bacteria. Neth. Milk Dairy J. 35:255-273.
43. Tsakalidou, E., R. Anastasiou, I. Vandenberghe, J. Van Beeumen, and G. Kalantzopoulos. 1999. Cell-wall-bound proteinase of Lactobacillus delbrueckii subsp. lactis ACA-DC 178: characterization and specificity for β-casein. Appl. Environ. Microbiol. 65:2035-2040.
44. Yamamoto, N., A. Akino, and T. Takano. 1993. Purification and specifity of a cell-wall-associated proteinase from Lactobacillus helveticus CP790. J. Biochem. 114:740-745.
45. Zevaco, C., and J.-C. Gripon. 1988. Properties and specificity of a cell-wall proteinase from Lactobacillus helveticus. Lait 68:393-408.