This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Saved Citations Download to citation manager Request Permissions Request Reprints Add to My Marked Citations Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Citing Articles via Scopus Google Scholar Articles by Cowman, R.A. Articles by Baron, S.S. Search for Related Content PubMed PubMed Citation Articles by Cowman, R.A. Articles by Baron, S.S. Social Bookmarking                         What's this?

Pathway for Uptake and Degradation of X-Prolyl Tripeptides in Streptococcus mutans VA-29R and Streptococcus sanguis ATCC 10556

Dental Research Unit, Department of Veterans Affairs Medical Center, Miami, Florida 33125, Department of Medicine, University of Miami School of Medicine, Miami, Florida 33124

S.S. Baron

Dental Research Unit, Department of Veterans Affairs Medical Center, Miami, Florida 33125

The growth of Streptococcus mutans and Streptococcus sanguis in the oral environment requires that these micro-organisms be able to degrade salivary proteins and to assimilate the resulting peptides as an amino nitrogen source. Our research is aimed at the definition of the proteolytic enzyme systems in these oral streptococci which allow them to utilize such substrates. In the present work, the nature of the hydrolytic activity expressed by S. mutans VA-29R and S. sanguis ATCC 10556 against X-Pro-4-nitroanilide and X-Pro-Y tripeptide substrates was investigated. This activity was predominantly associated with a cytoplasmic dipeptidyl peptidase which preferentially catalyzes the release of an N-terminal dipeptide from substrates in which proline is the penultimate residue. These streptococci also possess a second cytoplasmic peptidase, pepD, which catalyzes the hydrolysis of X-Pro dipeptides. We found that Gly-Pro-Ala or Ala-Pro-Gly were transported into the bacterial cells only when an energy source such as glucose was present. Peptide uptake was time-dependent, and selective exodus of peptide-derived amino acids from the bacterial cells occurred during peptide uptake. Results from these studies provide evidence that S. mutans VA-29R and S. sanguis ATCC 10556 possess a pathway for the complete degradation of X-Pro tripeptides. Transport of the peptides into cells prior to hydrolysis provides an efficient way by which all amino acids of a peptide may be obtained at an energy expense equivalent to that associated with the transport of just one amino acid. In light of the abundance of proline in salivary polypeptides, this degradative pathway could be an important component in the proteolytic pathway for salivary polypeptide utilization in these oral streptococci.

Key Words: dipeptidyl peptidases • oral streptococci • tripeptides • transport

REFERENCES

• Andersson C., Sund M.-L, Linder L. (1984). Peptide utilization by oral streptococci. Infect Immun 43:555-560.[Abstract/Free Full Text]
• Bennick A., Cannon M., Madapallimattam G. (1979). The nature of the hydroxyapatite-binding site in salivary acidic proline-rich proteins. Biochem J 183:115-126.[Medline] [Order article via Infotrieve]
• Bunick FJ, Kashket S. (1981). Enolases from fluoride-sensitive and fluoride-resistant streptococci. Infect Immun 34:856-863.[Abstract/Free Full Text]
• Chassy BM (1976). A gentle method for the lysis of oral streptococci. Biochem Biophys Res Commun 68:603-608.[CrossRef][Medline] [Order article via Infotrieve]
• Cowman RA, Baron SS (1990). Influence of hydrophobicity on oligopeptide utilization by oral streptococci. J Dent Res 69:1847-1851.
• Cowman RA, Baron SS (1991). Studies on the subcellular localization of protease and arylaminopeptidase activities in Streptococcus sanguis ATCC 10556. J Dent Res 70:1508-1515.
• Cowman RA, Baron SS (1993). Comparison of aminopeptidase activities in four strains of mutans group oral streptococci. Infect Immun 61:182-186.[Abstract/Free Full Text]
• Cowman RA, Perrella MM, Fitzgerald RJ (1976). Caseinolytic and glycoprotein hydrolase activity of Streptococcus mutans. J Dent Res 55:391-399.
• Cowman RA, Fitzgerald RJ, Perrella MM, Cornell AH (1977). Human saliva as a nitrogen source for oral streptococci. Caries Res 11:1-8.[Medline] [Order article via Infotrieve]
• Cowman RA, Schaefer SJ, Fitzgerald RJ (1979). Specificity of utilization of human salivary proteins for growth by oral streptococci. Caries Res 13:181-189.[Medline] [Order article via Infotrieve]
• Cowman RA, Baron SS, Fitzgerald RJ, Stuchell RE, Mandel ID (1983). Comparative growth responses of oral streptococci on mixed saliva or the separate submandibular and parotid secretions from caries-active and caries-free individuals. J Dent Res 62:946-951.
• Exterkate FA (1984). Location of peptidases outside and inside the membrane of Streptococcus cremoris. Appl Environ Microbiol 47:177-183.[Abstract/Free Full Text]
• Floderus E., Andersson C., Linder L., Sund M.-L (1987). Aminopeptidase activity in strains of oral streptococci. Oral Microbiol Immunol 2:117-120.[Medline] [Order article via Infotrieve]
• Foucaud C., Kunji ER, Hagting A., Richard J., Konings WN, Desmazeaud M., et al. (1995). Specificity of peptide transport systems in Lactococcus lactis: Evidence for a third system which transports hydrophobic di- and tripeptides. J Bacteriol 177:4652-4657.[Abstract/Free Full Text]
• Fukasawa KM, Harada M. (1981). Purification and properties of dipeptidyl peptidase IV from Streptococcus mitis ATCC 9811. Arch Biochem Biophys 210:230-237.[CrossRef][Medline] [Order article via Infotrieve]
• Hagting A., Kunji ER, Leenhouts KJ, Poolman B., Konings WN (1994). The di- and tripeptide transport protein of Lactococcus lactis. A new type of bacterial peptide transporter. J Biol Chem 269:11391-11399.[Abstract/Free Full Text]
• Harada M., Hiraoka BY, Mogi M., Fukasawa K., Fukasawa KM (1988). High-performance liquid chromatographic separation of peptides possessing a proline residue in the amino-terminal penultimate position, and their products generated by enzymatic hydrolysis. J Chromatog 424:129-135.[Medline] [Order article via Infotrieve]
• Homer KA, Patel R., Beighton D. (1993). Effects of N-acetylglucosamine on carbohydrate fermentation by Streptococcus mutans NCTC 10449 and Streptococcus sobrinus SL-1. Infect Immun 61:295-302.[Abstract/Free Full Text]
• Jenkinson HF, Baker RA, Tannock GW (1996). A binding-lipoprotein-dependent oligopeptide transport system in Streptococcus gordonii essential for uptake of hexa- and heptapeptides. J Bacteriol 178:68-77.[Abstract/Free Full Text]
• Kunji ER, Smid EJ, Plapp R., Poolman B., Konings WN (1993). Di-tripeptides and oligopeptides are taken up via distinct transport mechanisms in Lactococcus lactis. J Bacteriol 175:2052-2059.[Abstract/Free Full Text]
• Kousvelari EE, Baratz RS, Burke B., Oppenheim FG (1980). Immunochemical identification and determination of proline-rich proteins in salivary secretions, enamel pellicle, and glandular tissue specimens. J Dent Res 59:1430-1438.
• Lloyd RJ, Pritchard GG (1991). Characterization of X-prolyl dipeptidyl aminopeptidase from Lactococcus lactis subsp. lactis. J Gen Microbiol 137:49-55.[Abstract/Free Full Text]
• Meyer J., Jordi R. (1987). Purification and characterization of X-prolyl-dipeptidylaminopeptidase from Lactococcus lactis and from Streptococcus thermophilus. J Dairy Sci 70:738-745.[Abstract/Free Full Text]
• Mineyama R., Saito K. (1991). Purification and characterization of dipeptidyl peptidase IV from Streptococcus salivarius HHT. Microbios 68:37-52.
• Payne JW (1977). Transport and hydrolysis of peptides by microorganisms. In: Peptide transport and hydrolysis. Ciba Foundation Symposium 50 (new series). Payne JW, Mathews D, editors. Amsterdam: Elsevier Publishers, pp. 305-333.
• Payne JW, Bell G. ( 1979). Direct determination of the properties of peptide transport systems in Escherichia coli, using a fluorescent-labeling procedure. J Bacteriol 137:447-455.[Abstract/Free Full Text]
• Perinpanayagam HE, Van Wuyckhuyse BC, Ji ZS, Tabak LA (1995). Characterization of low-molecular-weight peptides in human parotid saliva. J Dent Res 74:345-350.
• Poolman B., Konings WN (1988). Relation of growth of Streptococcus cremoris to amino acid transport. J Bacteriol 170:700-707.[Abstract/Free Full Text]
• Rogers AH, Pfennig AL, Gully NJ, Zilm PS ( 1991). Factors affecting peptide catabolism by oral streptococci. Oral Microbiol Immunol 6:72-75.[Medline] [Order article via Infotrieve]
• Rogers AH, Zilm PS, Gully NJ, Pfennig AL (1990). Some aspects of protease production by a strain of Streptococcus sanguis. Oral Microbiol Immunol 5:72-76.[Medline] [Order article via Infotrieve]
• Smith K., Beighton D. (1987). Proteolytic activities in the supragingival plaque of monkeys (Macaca fascicularis). Arch Oral Biol 32:473-476.[Medline] [Order article via Infotrieve]
• Smid EJ, Plapp R., Konings WM (1989). Peptide uptake is essential for growth of Lactococcus lactis on the milk protein casein. J Bacteriol 171:6135-6140.[Abstract/Free Full Text]
• Tang-Larsen J., Claesson R., Edlund M-B., Carlsson J. (1995). Competition for peptides and amino acids among periodontal bacteria. J Periodont Res 30:390-395.[CrossRef][Medline] [Order article via Infotrieve]
• Thoma RS, Crimmins DL (1991). Automated phenylthiocarbamyl amino acid analysis of carboxypeptidase/aminopeptidase digests and acid hydrolysates. J Chromatog 537:153-165.[Medline] [Order article via Infotrieve]
• Thomas TD, Jarvis BD, Skipper NA (1974). Localization of proteinase(s) near the cell surface of Streptococcus lactis. J Bacteriol 118:329-333.[Abstract/Free Full Text]
• Van Boven A., Konings WN (1986). Energetics of leucylleucine hydrolysis in Streptococcus cremoris Wg2. Appl Environ Microbiol 51:95-100.[Abstract/Free Full Text]
• Zevaco C., Monnet V., Gripon J.-C (1990). Intracellular X-prolyl dipeptidyl peptidase from Lactococcus lactis spp. lactis: Purification and properties. J Appl Bacteriol 68:357-366.

Journal of Dental Research, Vol. 76, No. 8, 1477-1484 (1997)
DOI: 10.1177/00220345970760081001


CiteULike    Complore    Connotea    Del.icio.us    Digg    Reddit    Technorati    Twitter    What's this?

This article has been cited by other articles:

				C. Wickstrom, M. C. Herzberg, D. Beighton, and G. Svensater Proteolytic degradation of human salivary MUC5B by dental biofilms Microbiology, September 1, 2009; 155(9): 2866 - 2872. [Abstract] [Full Text] [PDF]

				A. C. L. Len, D. W. S. Harty, and N. A. Jacques Stress-responsive proteins are upregulated in Streptococcus mutans during acid tolerance Microbiology, May 1, 2004; 150(5): 1339 - 1351. [Abstract] [Full Text] [PDF]

				J. M. Goldstein, D. Nelson, T. Kordula, J. A. Mayo, and J. Travis Extracellular Arginine Aminopeptidase from Streptococcus gordonii FSS2 Infect. Immun., February 1, 2002; 70(2): 836 - 843. [Abstract] [Full Text] [PDF]

				J. M. Goldstein, A. Banbula, T. Kordula, J. A. Mayo, and J. Travis Novel Extracellular x-Prolyl Dipeptidyl-Peptidase (DPP) from Streptococcus gordonii FSS2: an Emerging Subfamily of Viridans Streptococcal x-Prolyl DPPs Infect. Immun., September 1, 2001; 69(9): 5494 - 5501. [Abstract] [Full Text] [PDF]

				Z. E. Juarez and M. W. Stinson An Extracellular Protease of Streptococcus gordonii Hydrolyzes Type IV Collagen and Collagen Analogues Infect. Immun., January 1, 1999; 67(1): 271 - 278. [Abstract] [Full Text] [PDF]

This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Saved Citations Download to citation manager Request Permissions Request Reprints Add to My Marked Citations Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Citing Articles via Scopus Google Scholar Articles by Cowman, R.A. Articles by Baron, S.S. Search for Related Content PubMed PubMed Citation Articles by Cowman, R.A. Articles by Baron, S.S. Social Bookmarking                         What's this?