Salivary histatin 5 internalization by translocation, but not endocytosis, is required for fungicidal activity in Candida albicans

Molecular Microbiology

Volumn 77, Issue 2, 2010, Pages 354-370

  Jang, Woong Sik ^a   Bajwa, Jashanjot Singh ^a   Sun, Jianing N ^a   Edgerton, Mira ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AZIDE; BETA GLUCAN; CARBOHYDRATE; CARBONYL CYANIDE CHLOROPHENYLHYDRAZONE; HISTATIN 5; LAMINARAN; MANNAN; PUSTULAN; SIALIC ACID; SODIUM CHLORIDE; SORBITOL; UNCLASSIFIED DRUG; BETA-1,3-GLUCAN; HISTATIN; HTN3 PROTEIN, HUMAN; PROPIDIUM IODIDE;

ARTICLE; CANDIDA ALBICANS; CELL PH; CELL VACUOLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOSOL; CYTOTOXICITY; ENDOCYTOSIS; FUNGAL CELL; FUNGICIDAL ACTIVITY; INTERNALIZATION; MEMBRANE BINDING; MEMBRANE DAMAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CARBOHYDRATE INTERACTION; CELL WALL; CYTOPLASM; HUMAN; METABOLISM; PROTEIN TRANSPORT;

CANDIDA ALBICANS;

BETA-GLUCANS; CANDIDA ALBICANS; CELL WALL; CYTOPLASM; ENDOCYTOSIS; HISTATINS; HUMANS; PROPIDIUM; PROTEIN TRANSPORT; SODIUM CHLORIDE; SORBITOL; VACUOLES;

EID: 77954352198     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07210.x     Document Type: Article

References (53)

1. Aouida, M., Page, N., Leduc, A., Peter, M. Ramotar, D. (2004) A genome-wide screen in Saccharomyces cerevisiae reveals altered transport as a mechanism of resistance to the anticancer drug bleomycin. Cancer Res 64 : 1102 1109.
2. Aouida, M., Leduc, A., Poulin, R. Ramotar, D. (2005) AGP2 encodes the major permease for high affinity polyamine import in Saccharomyces cerevisiae. J Biol Chem 280 : 24267 24276.
3. Arcuino, G., Lin, J.H., Takano, T., Liu, C., Jiang, L., Gao, Q., et al. (2002) Intercellular calcium signaling mediated by point-source burst release of ATP. Proc Natl Acad Sci USA 99 : 9840 9845.
4. Baev, D., Li, X.S., Dong, J., Keng, P. Edgerton, M. (2002) Human salivary histatin 5 causes disordered volume regulation and cell cycle arrest in Candida albicans. Infect Immun 70 : 4777 4784.
5. Baev, D., Rivetta, A., Li, X.S., Vylkova, S., Bashi, E., Slayman, C.L. Edgerton, M. (2003) Killing of Candida albicans by human salivary histatin 5 is modulated, but not determined, by the potassium channel TOK1. Infect Immun 71 : 3251 3260.
6. Baev, D., Rivetta, A., Vylkova, S., Sun, J.N., Zeng, G.F., Slayman, C.L. Edgerton, M. (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.
7. Bensen, E.S., Filler, S.G. Berman, J. (2002) A forkhead transcription factor is important for true hyphal as well as yeast morphogenesis in Candida albicans. Eukaryot Cell 1 : 787 798.
8. Castagnola, M., Inzitari, R., Rossetti, D.V., Olmi, C., Cabras, T., Piras, V., et al. (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.
9. Chaffin, W.L., Lopez-Ribot, J.L., Casanova, M., Gozalbo, D. Martinez, J.P. (1998) Cell wall and secreted proteins of Candida albicans: identification, function, and expression. Microbiol Mol Biol Rev 62 : 130 180.
10. Den Hertog, A.L., Wong Fong Sang, H.W., Kraayenhof, R., Bolscher, J.G., Van't Hof, W., Veerman, E.C. Nieuw Amerongen, A.V. (2004) Interactions of histatin 5 and histatin 5-derived peptides with liposome membranes: surface effects, translocation and permeabilization. Biochem J 379 : 665 672.
11. Dielbandhoesing, S.K., Zhang, H., Caro, L.H., van der Vaart, J.M., Klis, F.M., Verrips, C.T. Brul, S. (1998) Specific cell wall proteins confer resistance to nisin upon yeast cells. Appl Environ Microbiol 64 : 4047 4052.
12. Edgerton, M., Koshlukova, S.E., Lo, T.E., Chrzan, B.G., Straubinger, R.M. Raj, P.A. (1998) Candidacidal activity of salivary histatins. Identification of a histatin 5-binding protein on Candida albicans. J Biol Chem 273 : 20438 20447.
13. Efe, J.A., Botelho, R.J. Emr, S.D. (2005) The Fab1 phosphatidylinositol kinase pathway in the regulation of vacuole morphology. Curr Opin Cell Biol 17 : 402 408.
14. Fonzi, W.A. Irwin, M.Y. (1993) Isogenic strain construction and gene mapping in Candida albicans. Genetics 134 : 717 728.
15. Ghosh, M., Shen, J. Rosen, B.P. (1999) Pathways of As(III) detoxification in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 96 : 5001 5006.
16. Gow, N.A., Netea, M.G., Munro, C.A., Ferwerda, G., Bates, S., Mora-Montes, H.M., et al. (2007) Immune recognition of Candida albicans beta-glucan by dectin-1. J Infect Dis 196 : 1565 1571.
17. Gyurko, C., Lendenmann, U., Troxler, R.F. Oppenheim, F.G. (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. Harris, M., Mora-Montes, H.M., Gow, N.A. Coote, P.J. (2009) Loss of mannosylphosphate from Candida albicans cell wall proteins results in enhanced resistance to the inhibitory effect of a cationic antimicrobial peptide via reduced peptide binding to the cell surface. Microbiology 155 : 1058 1070.
19. Helmerhorst, E.J., Breeuwer, P., van't Hof, W., Walgreen-Weterings, E., Oomen, L.C., Veerman, E.C., et al. (1999) The cellular target of histatin 5 on Candida albicans is the energized mitochondrion. J Biol Chem 274 : 7286 7291.
20. Helmerhorst, E.J., Troxler, R.F. Oppenheim, F.G. (2001) The human salivary peptide histatin 5 exerts its antifungal activity through the formation of reactive oxygen species. Proc Natl Acad Sci USA 98 : 14637 14642.
21. Helmerhorst, E.J., Venuleo, C., Beri, A. Oppenheim, F.G. (2005) Candida glabrata is unusual with respect to its resistance to cationic antifungal proteins. Yeast 22 : 705 714.
22. Hoffmann, J.A., Kafatos, F.C., Janeway, C.A. Ezekowitz, R.A. (1999) Phylogenetic perspectives in innate immunity. Science 284 : 1313 1318.
23. Hohmann, S. (2002) Osmotic stress signaling and osmoadaptation in yeasts. Microbiol Mol Biol Rev 66 : 300 372.
24. Jang, W.S., Kim, H.K., Lee, K.Y., Kim, S.A., Han, Y.S. Lee, I.H. (2006) Antifungal activity of synthetic peptide derived from halocidin, antimicrobial peptide from the tunicate, Halocynthia aurantium. FEBS Lett 580 : 1490 1496.
25. Jang, W.S., Li, X.S., Sun, J.N. Edgerton, M. (2008) 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. Antimicrob Agents Chemother 52 : 497 504.
26. Johnston, D.A., Eberle, K.E., Sturtevant, J.E. Palmer, G.E. (2009) Role for endosomal and vacuolar GTPases in Candida albicans pathogenesis. Infect Immun 77 : 2343 2355.
27. Kapteyn, J.C., Hoyer, L.L., Hecht, J.E., Muller, W.H., Andel, A., Verkleij, A.J., et al. (2000) The cell wall architecture of Candida albicans wild-type cells and cell wall-defective mutants. Mol Microbiol 35 : 601 611.
28. Koshlukova, S.E., Lloyd, T.L., Araujo, M.W. Edgerton, M. (1999) Salivary histatin 5 induces non-lytic release of ATP from Candida albicans leading to cell death. J Biol Chem 274 : 18872 18879.
29. Koshlukova, S.E., Araujo, M.W., Baev, D. Edgerton, M. (2000) Released ATP is an extracellular cytotoxic mediator in salivary histatin 5-induced killing of Candida albicans. Infect Immun 68 : 6848 6856.
30. Li, S.C. Kane, P.M. (2009) The yeast lysosome-like vacuole: endpoint and crossroads. Biochim Biophys Acta 1793 : 650 663.
31. Li, X.S., Sun, J.N., Okamoto-Shibayama, K. Edgerton, M. (2006) Candida albicans cell wall ssa proteins bind and facilitate import of salivary histatin 5 required for toxicity. J Biol Chem 281 : 22453 22463.
32. Lu, C.F., Montijn, R.C., Brown, J.L., Klis, F., Kurjan, J., Bussey, H. Lipke, P.N. (1995) Glycosyl phosphatidylinositol-dependent cross-linking of alpha-agglutinin and beta 1,6-glucan in the Saccharomyces cerevisiae cell wall. J Cell Biol 128 : 333 340.
33. MacRobbie, E.A. (2006) Osmotic effects on vacuolar ion release in guard cells. Proc Natl Acad Sci USA 103 : 1135 1140.
34. Maddi, A., Bowman, S.M. Free, S.J. (2009) Trifluoromethanesulfonic acid-based proteomic analysis of cell wall and secreted proteins of the ascomycetous fungi Neurospora crassa and Candida albicans. Fungal Genet Biol 46 : 768 781.
35. Martinez, J.P., Gil, M.L., Lopez-Ribot, J.L. Chaffin, W.L. (1998) Serologic response to cell wall mannoproteins and proteins of Candida albicans. Clin Microbiol Rev 11 : 121 141.
36. Mochon, A.B. Liu, H. (2008) The antimicrobial peptide histatin-5 causes a spatially restricted disruption on the Candida albicans surface, allowing rapid entry of the peptide into the cytoplasm. PLoS Pathog 4 : e1000190.
37. Oberholzer, U., Marcil, A., Leberer, E., Thomas, D.Y. Whiteway, M. (2002) Myosin I is required for hypha formation in Candida albicans. Eukaryot Cell 1 : 213 228.
38. Oberholzer, U., Nantel, A., Berman, J. Whiteway, M. (2006) Transcript profiles of Candida albicans cortical actin patch mutants reflect their cellular defects: contribution of the Hog1p and Mkc1p signaling pathways. Eukaryot Cell 5 : 1252 1265.
39. Oppenheim, F.G., Xu, T., McMillian, F.M., Levitz, S.M., Diamond, R.D., Offner, G.D. 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.
40. Palmer, G.E., Kelly, M.N. Sturtevant, J.E. (2007) Autophagy in the pathogen Candida albicans. Microbiology 153 : 51 58.
41. Peschel, A., Otto, M., Jack, R.W., Kalbacher, H., Jung, G. Gotz, F. (1999) Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J Biol Chem 274 : 8405 8410.
42. Pina-Vaz, C., Sansonetty, F., Rodrigues, A.G., Costa-Oliveira, S., Tavares, C. Martinez-de-Oliveira, J. (2001) Cytometric approach for a rapid evaluation of susceptibility of Candida strains to antifungals. Clin Microbiol Infect 7 : 609 618.
43. Raj, P.A., Edgerton, M. Levine, M.J. (1990) Salivary histatin 5: dependence of sequence, chain length, and helical conformation for candidacidal activity. J Biol Chem 265 : 3898 3905.
44. Stevens, H.C. Nichols, J.W. (2007) The proton electrochemical gradient across the plasma membrane of yeast is necessary for phospholipid flip. J Biol Chem 282 : 17563 17567.
45. Sun, J.N., Li, W., Jang, W.S., Nayyar, N., Sutton, M.D. Edgerton, M. (2008) Uptake of the antifungal cationic peptide Histatin 5 by Candida albicans Ssa2p requires binding to non-conventional sites within the ATPase domain. Mol Microbiol 70 : 1246 1260.
46. Uemura, T., Kashiwagi, K. Igarashi, K. (2007) Polyamine uptake by DUR3 and SAM3 in Saccharomyces cerevisiae. J Biol Chem 282 : 7733 7741.
47. Veerman, E.C., Nazmi, K., Van't Hof, W., Bolscher, J.G., Den Hertog, A.L. Nieuw Amerongen, A.V. (2004) Reactive oxygen species play no role in the candidacidal activity of the salivary antimicrobial peptide histatin 5. Biochem J 381 : 447 452.
48. Veerman, E.C., Valentijn-Benz, M., Nazmi, K., Ruissen, A.L., Walgreen-Weterings, E., van Marle, J., et al. (2007) Energy depletion protects Candida albicans against antimicrobial peptides by rigidifying its cell membrane. J Biol Chem 282 : 18831 18841.
49. Vylkova, S., Jang, W.S., Li, W., Nayyar, N. Edgerton, M. (2007) Histatin 5 initiates osmotic stress response in Candida albicans via activation of the Hog1 mitogen-activated protein kinase pathway. Eukaryot Cell 6 : 1876 1888.
50. Weisman, L.S. (2003) Yeast vacuole inheritance and dynamics. Annu Rev Genet 37 : 435 460.
51. Wheeler, R.T., Kombe, D., Agarwala, S.D. Fink, G.R. (2008) Dynamic, morphotype-specific Candida albicans beta-glucan exposure during infection and drug treatment. PLoS Pathog 4 : e1000227.
52. Xu, Y., Ambudkar, I., Yamagishi, H., Swaim, W., Walsh, T.J. O'Connell, B.C. (1999) Histatin 3-mediated killing of Candida albicans: effect of extracellular salt concentration on binding and internalization. Antimicrob Agents Chemother 43 : 2256 2262.
53. Yeaman, M.R. Yount, N.Y. (2003) Mechanisms of antimicrobial peptide action and resistance. Pharmacol Rev 55 : 27 55.