The P-113 fragment of histatin 5 requires a specific peptide sequence for intracellular translocation in Candida albicans, which is independent of cell wall binding

Antimicrobial Agents and Chemotherapy

Volumn 52, Issue 2, 2008, Pages 497-504

  Woong, Sik Jang ^a   Xuewei, Serene Li ^a   Sun, Jianing N ^a   Edgerton, Mira ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANE PROTEIN; GLUTAMINE; HISTATIN 5; LYSINE; PROTEIN SSA2; SODIUM CHLORIDE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; CANDIDA ALBICANS; CELL KILLING; CELL WALL; CELLULAR DISTRIBUTION; CYTOSOL; FUNGAL CELL; FUNGAL STRAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN MICROARRAY; SSA2 GENE; WILD TYPE;

AMINO ACID SEQUENCE; ANTIMICROBIAL CATIONIC PEPTIDES; BIOLOGICAL TRANSPORT, ACTIVE; CANDIDA ALBICANS; CELL WALL; CYTOSOL; FUNGAL PROTEINS; HISTATINS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; MOLECULAR SEQUENCE DATA;

EID: 38649127564     PISSN: 00664804     EISSN: None     Source Type: Journal    
DOI: 10.1128/AAC.01199-07     Document Type: Article

References (40)

1. Ahmad, M., M. Piludu, F. G. Oppenheim, E. J. Heimerhorst, and A. R. Hand. 2004. Immunocytochemical localization of histatins in human salivary glands. J. Histochem. Cytochem. 52:361-370.
2. Aouida, M., A. Leduc, R. Poulin, and D. Ramotar. 2005. AGP2 encodes the major permease for high affinity polyamine import in Saccharomyces cerevisiae. J. Biol. Chem. 280:24267-24276.
3. Baev, D., X. S. Li, J. Dong, P. Keng, and M. Edgerton. 2002. Human salivary histatin 5 causes disordered volume regulation and cell cycle arrest in Candida albicans. Infect. Immun. 70:4777-4784.
4. Baev, D., A. Rivetta, S. Vylkova, J. N. Sun, G. F. Zeng, C. L. Slayman, and M. Edgerton. 2004. The TRK1 potassium transporter is the critical effector for killing of Candida albicans by the cationic protein, histatin 5. J. Biol. Chem. 279:55060-55072.
5. Breinig, F., T. Sendzik, K. Eisfeld, and M. J. Schmitt. 2006. Dissecting toxin immunity in virus-infected killer yeast uncovers an intrinsic strategy of self-protection. Proc. Natl. Acad. Sci. USA 103:3810-3815.
6. Brewer, D., and G. Lajoie. 2002. Structure-based design of potent histatin analogues. Biochemistry 41:5526-5536.
7. Castagnola, M., R. Inzitari, D. V. Rossetti, C. Olmi, T. Cabras, V. Piras, P. Nicolussi, M. T. Sanna, M. Pellegrini, B. Giardina, and I. Messana. 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.
8. Den Hertog, A. L., H. W. Wong Fong Sang, R. Kraayenhof, J. G. Bolscher, W. Van't Hof, E. C. Veerman, and A. V. Nieuw Amerongen. 2004. Interactions of histatin 5 and histatin 5-derived peptides with liposome membranes: surface effects, translocation and permeabilization. Biochem. J. 379:665-672.
9. de Repentigny, L., D. Lewandowski, and P. Jolicoeur. 2004. Immunopathogenesis of oropharyngeal candidiasis in human immunodeficiency virus infection. Clin. Microbiol. Rev. 17:729-759.
10. Dong, J., S. Vylkova, X. S. Li, and M. Edgerton. 2003. Calcium blocks fungicidal activity of human salivary histatin 5 through disruption of binding with Candida albicans. J. Dent. Res. 82:748-752.
11. Driscoll, J., C. Duan, Y. Zuo, T. Xu, R. Troxler, and F. G. Oppenheim. 1996. Candidacidal activity of human salivary histatin recombinant variants produced by site-directed mutagenesis. Gene 177:29-34.
12. Eckert, R., J. He, D. K. Yarbrough, F. Qi, M. H. Anderson, and W. Shi. 2006. Targeted killing of Streptococcus mutans by a pheromone-guided "smart" antimicrobial peptide. Antimicrob. Agents Chemother. 50:3651-3657.
13. Edgerton, M., S. E. Koshlukova, T. E. Lo, B. G. Chrzan, R. M. Straubinger, and P. A. Raj. 1998. Candidacidal activity of salivary histatins. Identification of a histatin 5-binding protein on Candida albicans. J. Biol. Chem. 273:20438-20447.
14. Eisfeld, K., F. Riffer, J. Mentges, and M. J. Schmitt. 2000. Endocytotic uptake and retrograde transport of a virally encoded killer toxin in yeast. Mol. Microbiol. 37:926-940.
15. Fotos, P. G., and J. W. Hellstein. 1992. Candida and candidosis. Epidemiology, diagnosis and therapeutic management. Dent. Clin. N. Am. 36:857-878.
16. Giacometti, A., O. Cirioni, W. Kamysz, G. D'Amato, C. Silvestri, M. S. Del Prete, A. Licci, A. Riva, J. Lukasiak, and G. Scalise. 2005. In vitro activity of the histatin derivative P-113 against multidrug-resistant pathogens responsible for pneumonia in immunocompromised patients. Antimicrob. Agents Chemother. 49:1249-1252.
17. Gyurko, C., U. Lendenmann, R. F. Troxler, and F. G. Oppenheim. 2000. Candida albicans mutants deficient in respiration are resistant to the small cationic salivary antimicrobial peptide histatin 5. Antimicrob. Agents Chemother. 44:348-354.
18. Hardt, M., L. R. Thomas, S. E. Dixon, G. Newport, N. Agabian, A. Prakobphol, S. C. Hall, H. E. Witkowska, and S. J. Fisher. 2005. Toward defining the human parotid gland salivary proteome and peptidome: identification and characterization using 2D SDS-PAGE, ultrafiltration, HPLC, and mass spectrometry. Biochemistry 44:2885-2899.
19. Haveman, C. W., and S. W. Redding. 1998. Dental management and treatment of xerostomic patients. Tex. Dent. J. 115:43-56.
20. Heimerhorst, E. J., I. M. Reijnders, W. van't Hof, I. Simoons-Smit, E. C. Veerman, and A. V. Amerongen. 1999. Amphotericin B- and fluconazole-resistant Candida spp., Aspergillus fumigatus, and other newly emerging pathogenic fungi are susceptible to basic antifungal peptides. Antimicrob. Agents Chemother. 43:702-704.
21. Jang, W. S., H. K. Kim, K. Y. Lee, S. A. Kim, Y. S. Han, and I. H. Lee. 2006. Antifungal activity of synthetic peptide derived from halocidin, antimicrobial peptide from the tunicate, Halocynthia aurantium. FEBS Lett. 580:1490-1496.
22. Koshlukova, S. E., T. L. Lloyd, M. W. Araujo, and M. Edgerton. 1999. Salivary histatin 5 induces non-lytic release of ATP from Candida albicans leading to cell death. J. Biol. Chem. 274:18872-18879.
23. Li, X. S., M. S. Reddy, D. Baev, and M. Edgerton. 2003. Candida albicans Ssa1/2p is the cell envelope binding protein for human salivary histatin 5. J. Biol. Chem. 278:28553-28561.
24. Li, X. S., J. N. Sun, K. Okamoto-Shibayama, and M. Edgerton. 2006. Candida albicans cell wall Ssa proteins bind and facilitate import of salivary histatin 5 required for toxicity. J. Biol. Chem. 281:22453- 22463.
25. Ramirez-Amador, V., S. Silverman, Jr., P. Mayer, M. Tyler, and J. Quivey. 1997. Candidal colonization and oral candidiasis in patients undergoing oral and pharyngeal radiation therapy. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 84:149-153.
26. Redding, S. W., R. C. Zellars, W. R. Kirkpatrick, R. K. McAtee, M. A. Caceres, A. W. Fothergill, J. L. Lopez-Ribot, C. W. Bailey, M. G. Rinaldi, and T. F. Patterson. 1999. Epidemiology of oropharyngeal Candida colonization and infection in patients receiving radiation for head and neck cancer. J. Clin. Microbiol. 37:3896-3900.
27. Rothstein, D. M., P. Spacciapoli, L. T. Tran, T. Xu, F. D. Roberts, M. Dalla Serra, D. K. Buxton, F. G. Oppenheim, and P. Friden. 2001. Anticandida activity is retained in P-113, a 12-amino-acid fragment of histatin 5. Antimicrob. Agents Chemother. 45:1367-1373.
28. Ruissen, A. L., J. Groenink, E. J. Heimerhorst, E. Walgreen-Weterings, W. Van't Hof, E. C. Veerman, and A. V. Nieuw Amerongen. 2001. Effects of histatin 5 and derived peptides on Candida albicans. Biochem. J. 356:361-368.
29. Schagger, H., and G. von Jagow. 1987. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166:368-379.
30. Silverman, S., Jr., L. Luangjarmekorn, and D. Greenspan. 1984. Occurrence of oral Candida in irradiated head and neck cancer patients. J. Oral Med. 39:194-196.
31. Tam, J. P., Y. A. Lu, and J. L. Yang. 2002. Correlations of cationic charges with salt sensitivity and microbial specificity of cystine-stabilized beta-strand antimicrobial peptides. J. Biol. Chem. 277:50450-50456.
32. Tsai, H., and L. A. Bobek. 1998. Human salivary histatins: promising antifungal therapeutic agents. Crit. Rev. Oral Biol. Med. 9:480-497.
33. Tsai, H., and L. A. Bobek. 1997. Studies of the mechanism of human salivary histatin-5 candidacidal activity with histatin-5 variants and azole-sensitive and -resistant Candida species. Antimicrob. Agents Chemother. 41:2224-2228.
34. Uemura, T., K. Kashiwagi, and K. Igarashi. 2007. Polyamine uptake by DUR3 and SAM3 in Saccharomyces cerevisiae. J. Biol. Chem. 282:7733-7741.
35. Uemura, T., K. Kashiwagi, and K. Igarashi. 2005. Uptake of putrescine and spermidine by Gap1p on the plasma membrane in Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 328:1028-1033.
36. Vanden Bossche, H., D. W. Warnock, B. Dupont, D. Kerridge, S. Sen Gupta, L. Improvisi, P. Marichal, F. C. Odds, F. Provost, and O. Ronin. 1994. Mechanisms and clinical impact of antifungal drug resistance. J. Med. Vet. Mycol. 32:189-202.
37. Vylkova, S., N. Nayyar, W. Li, and M. Edgerton. 2007. Human beta-defensins kill Candida albicans in an energy-dependent and salt-sensitive manner without causing membrane disruption. Antimicrob. Agents Chemother. 51:154-161.
38. Xu, T., S. M. Levitz, R. D. Diamond, and F. G. Oppenheim. 1991. Anticandidal activity of major human salivary histatins. Infect. Immun. 59:2549-2554.
39. Xu, Y., I. Ambudkar, H. Yamagisbi, W. Swaim, T. J. Walsh, and B. C. O'Connell. 1999. Histatin 3-mediated killing of Candida albicans: effect of extracellular salt concentration on binding and internalization. Antimicrob. Agents Chemother. 43:2256-2262.
40. Zhu, J., P. W. Luther, Q. Leng, and A. J. Mixson. 2006. Synthetic histidine-rich peptides inhibit Candida species and other fungi in vitro: role of endocytosis and treatment implications. Antimicrob. Agents Chemother. 50:2797-2805.