Kinetics of histatin proteolysis in whole saliva and the effect on bioactive domains with metal-binding, antifungal, and wound-healing properties

FASEB Journal

Volumn 23, Issue 8, 2009, Pages 2691-2701

  Sun, Xiuli ^a   Salih, Erdjan ^a   Oppenheim, Frank G ^a   Helmerhorst, Eva J ^a  

^a BOSTON UNIVERSITY   (United States)

Author keywords

Enzymes; Oral; Proteins; Proteolytic; Proteomics

Indexed keywords

ENZYME; HISTATIN; HISTATIN 1; HISTATIN 3; HISTATIN 5; HYDROGEN; HYDROGEN 15; HYDROGEN 18; METAL; POTASSIUM 11; POTASSIUM 13; POTASSIUM 17; POTASSIUM DERIVATIVE; UNCLASSIFIED DRUG; YTTRIUM; YTTRIUM 10; YTTRIUM 24; ANTIFUNGAL AGENT; HTN1 PROTEIN, HUMAN; HTN3 PROTEIN, HUMAN; PEPTIDE FRAGMENT; PEPTIDE HYDROLASE;

ANTIFUNGAL ACTIVITY; ARTICLE; ELECTROSPRAY MASS SPECTROMETRY; ENVIRONMENT; KINETICS; MATHEMATICAL MODEL; METAL BINDING; MONITORING; MOUTH CAVITY; PREDICTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SALIVA; SUPERNATANT; TANDEM MASS SPECTROMETRY; WOUND HEALING; AMINO ACID SEQUENCE; BINDING SITE; CHEMISTRY; GENETICS; HUMAN; IN VITRO STUDY; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANTIFUNGAL AGENTS; BINDING SITES; HISTATINS; HUMANS; KINETICS; METALS; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PEPTIDE HYDROLASES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SALIVA; SEQUENCE HOMOLOGY, AMINO ACID; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TANDEM MASS SPECTROMETRY; WOUND HEALING;

EID: 68849122288     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-131045     Document Type: Article

References (42)

1. Lopez-Otin, C., and Matrisian, L. M. (2007) Emerging roles of proteases in tumour suppression. Nat. Rev. Cancer 7, 800-808 (Pubitemid 47463671)
2. Overall, C. M., and Blobel, C. P. (2007) In search of partners: linking extracellular proteases to substrates. Nat. Rev. Mol. Cell Biol. 8, 245-257
3. Rudney, J. D. (1995) Does variability in salivary protein concentrations influence oral microbial ecology and oral health? Crit. Rev. Oral Biol. Med. 6, 343-367
4. Nakamura, M., and Slots, J. (1983) Salivary enzymes. Origin and relationship to periodontal disease. J. Periodontal Res. 18, 559-569 (Pubitemid 14153608)
5. Watanabe, T., Ohata, N., Morishita, M., and Iwamoto, Y. (1981) Correlation between the protease activities and the number of epithelial cells in human saliva. J. Dent. Res. 60, 1039-1044 (Pubitemid 11037988)
6. Germaine, G. R., Tellefson, L. M., and Johnson, G. L. (1978) Whole saliva proteases: development of methods for determination of origins. Adv. Exp. Med. Biol. 107, 849-858
7. Helmerhorst, E. J., Alagl, A. S., Siqueira, W. L., and Oppenheim, F. G. (2006) Oral fluid proteolytic effects on histatin 5 structure and function. Arch. Oral Biol. 51, 1061-1070
8. Castagnola, M., Inzitari, R., Rossetti, D. V., Olmi, C., Cabras, T., Piras, V., Nicolussi, P., Sanna, M. T., Pellegrini, M., Giardina, B., and Messana, I. (2004) A cascade of 24 histatins (histatin 3 fragments) in human saliva: suggestions for a pre-secretory sequential cleavage pathway. J. Biol. Chem. 279, 41436-41443 (Pubitemid 39313584)
9. Helmerhorst, E. J., Sun, X., Salih, E., and Oppenheim, F. G. (2008) Identification of Lys-Pro-Gln as a novel cleavage site specificity of saliva-associated proteases. J. Biol. Chem. 283, 19957-19966
10. Messana, I., Cabras, T., Pisano, E., Sanna, M. T., Olianas, A., Manconi, B., Pellegrini, M., Paludetti, G., Scarano, E., Fiorita, A., Agostino, S., Contucci, A. M., Calo, L., Picciotti, P. M., Manni, A., Bennick, A., Vitali, A., Fanali, C., Inzitari, R., and Castagnola, M. (2008) Trafficking and postsecretory events responsible for the formation of secreted human salivary peptides: a proteomics approach. Mol. Cell. Proteomics 7, 911-926 (Pubitemid 351737091)
11. Vitorino, R., Lobo, M. J., Duarte, J. A., Ferrer-Correia, A. J., Domingues, P. M., and Amado, F. M. (2004) Analysis of salivary peptides using HPLC-electrospray mass spectrometry. Biomed. Chromatogr. 18, 570-575 (Pubitemid 39335041)
12. Oppenheim, F. G., Yang, Y. C., Diamond, R. D., Hyslop, D., Offner, G. D., and Troxler, R. F. (1986) The primary structure and functional characterization of the neutral histidine-rich polypeptide from human parotid secretion. J. Biol. Chem. 261, 1177-1182
13. Grogan, J., McKnight, C. J., Troxler, R. F., and Oppenheim, F. G. (2001) Zinc and copper bind to unique sites of histatin 5. FEBS Lett. 491, 76-80 (Pubitemid 32172005)
14. Melino, S., Gallo, M., Trotta, E., Mondello, F., Paci, M., and Petruzzelli, R. (2006) Metal-binding and nuclease activity of an antimicrobial peptide analogue of the salivary histatin 5. Biochemistry 45, 15373-15383 (Pubitemid 46032462)
15. 2+ ions selectively induce antimicrobial salivary peptide histatin-5 to fuse negatively charged vesicles. Identification and characterization of a zincbinding motif present in the functional domain. Biochemistry 38, 9626-9633
16. Gusman, H., Lendenmann, U., Grogan, J., Troxler, R. F., and Oppenheim, F. G. (2001) Is salivary histatin 5 a metallopeptide? Biochim. Biophys. Acta 1545, 86-95 (Pubitemid 32124810)
17. Freedman, A. (1996) Taste for zinc. Lancet 348, 1592
18. Gusman, H., Travis, J., Helmerhorst, E. J., Potempa, J., Troxler, R. F., and Oppenheim, F. G. (2001) Salivary histatin 5 is an inhibitor of both host and bacterial enzymes implicated in periodontal disease. Infect. Immun. 69, 1402-1408 (Pubitemid 32187587)
19. Oppenheim, F. G., Xu, T., McMillian, F. M., Levitz, S. M., Diamond, R. D., Offner, G. D., and Troxler, R. F. (1988) Histatins, a novel family of histidine-rich proteins in human parotid secretion: isolation, characterization, primary structure, and fungistatic effects on Candida albicans. J. Biol. Chem. 263, 7472-7477 (Pubitemid 18147029)
20. Amerongen, A. V., and Veerman, E. C. (2002) Saliva - the defender of the oral cavity. Oral Dis. 8, 12-22
21. Xu, T., Levitz, S. M., Diamond, R. D., and Oppenheim, F. G. (1991) Anticandidal activity of major human salivary histatins. Infect. Immun. 59, 2549-2554
22. Rothstein, D. M., Helmerhorst, E. J., Spacciapoli, P., Oppenheim, F. G., and Friden, P. (2002) Histatin-derived peptides: potential agents to treat localised infections. Exp. Opin. Emerg. Drugs 7, 47-59 (Pubitemid 34650914)
23. Rothstein, D. M., Spacciapoli, P., Tran, L. T., Xu, T., Roberts, F. D., Dalla Serra, M., Buxton, D. K., Oppenheim, F. G., and Friden, P. (2001) Anticandida activity is retained in P-113, a 12-amino-acid fragment of histatin 5. Antimicrob. Agents Chemother. 45, 1367-1373 (Pubitemid 32374104)
24. Oudhoff, M. J., Bolscher, J. G., Nazmi, K., Kalay, H., van't Hof, W., Amerongen, A. V., and Veerman, E. C. (2008) Histatins are the major wound-closure stimulating factors in human saliva as identified in a cell culture assay. FASEB J. 22, 3805-3812
25. Baum, B. J., Bird, J. L., and Longton, R. W. (1977) Polyacrylamide gel electrophoresis of human salivary histidine-richpolypeptides. J. Dent. Res. 56, 1115-1118 (Pubitemid 8239868)
26. Flora, B., Gusman, H., Helmerhorst, E. J., Troxler, R. F., and Oppenheim, F. G. (2001) A new method for the isolation of histatins 1, 3, and 5 from parotid secretion using zinc precipitation. Protein Expr. Purif. 23, 198-206 (Pubitemid 32930997)
27. Payne, J. B., Iacono, V. J., Crawford, I. T., Lepre, B. M., Bernzweig, E., and Grossbard, B. L. (1991) Selective effects of histidine-rich polypeptides on the aggregation and viability of Streptococcus mutans and Streptococcus sanguis. Oral Microbiol. Immunol. 6, 169-176
28. Baum, B. J., Bird, J. L., Millar, D. B., and Longton, R. W. (1976) Studies on histidine-rich polypeptides from human parotid saliva. Arch. Biochem. Biophys. 177, 427-436 (Pubitemid 8012812)
29. Dawes, C. (2004) How much saliva is enough for avoidance of xerostomia? Caries Res. 38, 236-240 (Pubitemid 38716215)
30. Gusman, H., Leone, C., Helmerhorst, E. J., Nunn, M., Flora, B., Troxler, R. F., and Oppenheim, F. G. (2004) Human salivary gland-specific daily variations in histatin concentrations determined by a novel quantitation technique. Arch. Oral Biol. 49, 11-22 (Pubitemid 38161736)
31. Campese, M., Sun, X., Bosch, J. A., Oppenheim, F. G., and Helmerhorst, E. J. (2009) Concentration and fate of histatins and acidic proline-rich proteins in the oral environment. [E-pub ahead of print] Arch Oral Biol. 10.1016/j.archoralbio. 2008.11.010
32. Vitorino, R., Lobo, M. J., Ferrer-Correira, A. J., Dubin, J. R., Tomer, K. B., Domingues, P. M., and Amado, F. M. (2004) Identification of human whole saliva protein components using proteomics. Proteomics 4, 1109-1115 (Pubitemid 38445969)
33. Helmerhorst, E. J., and Oppenheim, F. G. (2007) Saliva: a dynamic proteome. J. Dent. Res. 86, 680-693
34. Brewer, D., Hunter, H., and Lajoie, G. (1998) NMR studies of the antimicrobial salivary peptides histatin 3 and histatin 5 in aqueous and nonaqueous solutions. Biochem. Cell Biol. 76, 247-256 (Pubitemid 29102009)
35. Bruno, L. S., Li, X., Wang, L., Soares, R. V., Siqueira, C. C., Oppenheim, F. G., Troxler, R. F., and Offner, G. D. (2005) Two-hybrid analysis of human salivary mucin MUC7 interactions. Biochim. Biophys. Acta 1746, 65-72 (Pubitemid 41484087)
36. Iontcheva, I., Oppenheim, F. G., Offner, G. D., and Troxler, R. F. (2000) Molecular mapping of statherin- and histatinbinding domains in human salivary mucin MG1 (MUC5B) by the yeast two-hybrid system. J. Dent. Res. 79, 732-739 (Pubitemid 32507644)
37. Vitorino, R., Calheiros-Lobo, M. J., Williams, J., Ferrer-Correia, A. J., Tomer, K. B., Duarte, J. A., Domingues, P. M., and Amado, F. M. (2007) Peptidomic analysis of human acquired enamel pellicle. Biomed. Chromatogr. 21, 1107-1117 (Pubitemid 350200889)
38. Li, J., Helmerhorst, E. J., Troxler, R. F., and Oppenheim, F. G. (2004) Identification of in vivo pellicle constituents by analysis of serum immune responses. J. Dent. Res. 83, 60-64 (Pubitemid 41756860)
39. Armstrong, W. G. (1968) Origin and nature of the acquired pellicle. Proc. R. Soc. Med. 61, 923-930
40. Zahradnik, R. T., Moreno, E. C., and Burke, E. J. (1976) Effect of salivary pellicle on enamel subsurface demineralization in vitro. J. Dent. Res. 55, 664-670
41. Sorsa, T., Tjaderhane, L., and Salo, T. (2004) Matrix metalloproteinases (MMPs) in oral diseases. Oral Dis. 10, 311-318 (Pubitemid 39564343)
42. Sun, X., Salih, E., Oppenheim, F. G., and Helmerhorst, E. J. (2009) Activity-based mass spectrographic characterization of proteases and inhibitors in human saliva. Proteomics Clin. Appl. In press