Genes involved in protein glycosylation determine the activity and cell internalization of the antifungal peptide PAF26 in Saccharomyces cerevisiae

Fungal Genetics and Biology

Volumn 58-59, Issue , 2013, Pages 105-115

  Harries, Eleonora ^a,b   Carmona, Lourdes ^a   Muñoz, Alberto ^b   Ibeas, José I ^c   Read, Nick D ^b,d   Gandía, Mónica ^a   Marcos, Jose F ^a  

^a INSTITUTO DE AGROQUÍMICA Y TECNOLOGÍA DE ALIMENTOS CSIC   (Spain)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c Departamento de Biología Molecular e Ingeniería Bioquímica   (Spain)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Antimicrobial peptide; Cell wall; Cell penetrating peptide; Histatins; Melittin; Protein glycosylation

Indexed keywords

GLYCOPEPTIDASE; HEXAPEPTIDE; MANNOSYLTRANSFERASE; PAF 26; POLYPEPTIDE ANTIBIOTIC AGENT; TUNICAMYCIN; UNCLASSIFIED DRUG;

ALG5 GENE; AMINO ACID SEQUENCE; ANTIMICROBIAL ACTIVITY; ARTICLE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; EOS1 GENE; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; FUNGAL CELL WALL; FUNGAL GENE; FUNGAL GENETICS; FUNGAL STRAIN; FUNGUS CULTURE; GENE DELETION; GENE DISRUPTION; GENOTYPE; MINIMUM INHIBITORY CONCENTRATION; MNN1 GENE; MNN4 GENE; MNN5 GENE; NONHUMAN; PMT1 GENE; PMT2 GENE; PMT3 GENE; PMT4 GENE; PMT5 GENE; PMT6 GENE; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; PROTEIN LOCALIZATION; PROTOPLAST; SACCHAROMYCES CEREVISIAE;

FUNGI; SACCHAROMYCES CEREVISIAE;

ANTIMICROBIAL PEPTIDE; CELL WALL; CELL-PENETRATING PEPTIDE; HISTATINS; MELITTIN; PROTEIN GLYCOSYLATION;

ANTIFUNGAL AGENTS; CELL WALL; GLYCOSYLATION; OLIGOPEPTIDES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84884590595     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2013.08.004     Document Type: Article

References (63)

1. Arroyo J., Hutzler J., Bermejo C., Ragni E., Garcia-Cantalejo J., Botias P., Piberger H., Schott A., Sanz A.B., Strahl S. Functional and genomic analyses of blocked protein O-mannosylation in baker's yeast. Mol. Microbiol. 2011, 79:1529-1546.
2. Bai C., Xu X.L., Chan F.Y., Lee R.T.H., Wang Y. MNN5 encodes an iron-regulated α-1,2-mannosyltransferase important for protein glycosylation, cell wall integrity, morphogenesis and virulence in Candida albicans. Eukaryot. Cell 2006, 5:238-247.
3. Bou Zeidan, M., Carmona, L., Zara, S., Marcos, J.F., in press. FLO11 gene is involved in the interaction of flor strains of Saccharomyces cerevisiae with a biofilm-promoting synthetic hexapeptide. Appl. Environ. Microbiol. 79, 2013, doi:10.1128/AEM.01647-13.
4. Brogden K.A. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria?. Nat. Rev. Microbiol. 2005, 3:238-250.
5. Cantero P.D., Ernst J.F. Damage to the glycoshield activates PMT-directed O-mannosylation via the Msb2-Cek1 pathway in Candida albicans. Mol. Microbiol. 2011, 80:715-725.
6. Cantero P.D., Lengsfeld C., Prill S.K.H., Subanovic M., Roman E., Pla J., Ernst J.F. Transcriptional and physiological adaptation to defective protein-O-mannosylation in Candida albicans. Mol. Microbiol. 2007, 64:1115-1128.
7. Carmona L., Gandía M., López-García B., Marcos J.F. Sensitivity of Saccharomyces cerevisiae to the cell-penetrating antifungal peptide PAF26 correlates with endogenous nitric oxide (NO) production. Biochem. Biophys. Res. Commun. 2012, 417:56-61.
8. de Nadal E., Real F.X., Posas F. Mucins, osmosensors in eukaryotic cells?. Trends Cell Biol. 2007, 17:571-574.
9. Deshpande N., Wilkins M.R., Packer N., Nevalainen H. Protein glycosylation pathways in filamentous fungi. Glycobiology 2008, 18:626-637.
10. Duncan V.M.S., O'Neil D.A. Commercialization of antifungal peptides. Fungal Biol. Rev. 2013, 26:156-165.
11. Elbein A.D. Inhibitors of the biosynthesis and processing of N-linked oligosaccharide chains. Annu. Rev. Biochem. 1987, 56:497-534.
12. Fernández-Álvarez A., Elías-Villalobos A., Ibeas J.I. The O-mannosyltransferase PMT4 is essential for normal appressorium formation and penetration in Ustilago maydis. Plant Cell. 2009, 21:3397-3412.
13. Gamberi T., Cavalieri D., Magherini F., Mangoni L., De Filippo C., Borro M., Gentile G., Simmaco M., Modesti A. An integrated analysis of the effects of Esculentin 1-21 on Saccharomyces cerevisiae. Biochim. Biophys. Acta - Prot. Proteom. 2007, 1774:688-700.
14. Gentzsch M., Tanner W. The PMT gene family: protein O-glycosylation in Saccharomyces cerevisiae is vital. EMBO J. 1996, 15:5752-5759.
15. Gentzsch M., Tanner W. Protein-O-glycosylation in yeast: protein-specific mannosyltransferases. Glycobiology 1997, 7:481-486.
16. Girrbach V., Strahl S. Members of the evolutionarily conserved PMT family of protein O-mannosyltransferases form distinct protein complexes among themselves. J. Biol. Chem. 2003, 278:12554-12562.
17. Hancock R.E.W., Sahl H.G. Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat. Biotechnol. 2006, 24:1551-1557.
18. Harris M., Mora-Montes H.M., Gow N.A.R., Coote P.J. 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. Microbiol. SGM 2009, 155:1058-1070.
19. Heesen S.t., Lehle L., Weissmann A., Aebi M. Isolation of the ALG5 locus encoding the UDP-glucose:dolichyl-phosphate glucosyltransferase from Saccharomyces cerevisiae. Eur. J. Biochem. 1994, 224:71-79.
20. Henriques S.T., Melo M.N., Castanho M.A.R.B. Cell-penetrating peptides and antimicrobial peptides: how different are they?. Biochem. J. 2006, 399:1-7.
21. Ibeas J.I., Lee H., Damsz B., Prasad D.T., Pardo J.M., Hasegawa P.M., Bressan R.A., Narasimhan M.L. Fungal cell wall phosphomannans facilitate the toxic activity of a plant PR-5 protein. Plant J. 2000, 23:375-383.
22. Jang W.S., Li X.W.S., Sun J.N.N., Edgerton M. 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. 2008, 52:497-504.
23. Jang W.S., Bajwa J.S., Sun J.N., Edgerton M. Salivary histatin 5 internalization by translocation, but not endocytosis, is required for fungicidal activity in Candida albicans. Mol. Microbiol. 2010, 77:354-370.
24. Kimura T., Komiyama T., Furuichi Y., Iimura Y., Karita S., Sakka K., Ohmiya K. N-glycosylation is involved in the sensitivity of Saccharomyces cerevisiae to HM-1 killer toxin secreted from Hansenula mrakii IFO 0895. Appl. Microbiol. Biotechnol. 1999, 51:176-184.
25. Klis F.M., Boorsma A., de Groot P.W.J. Cell wall construction in Saccharomyces cerevisiae. Yeast 2006, 23:185-202.
26. Koo J.C., Lee B., Young M.E., Koo S.C., Cooper J.A., Baek D., Lim C.O., Lee S.Y., Yun D.J., Cho M.J. Pn-AMP1, a plant defense protein, induces actin depolarization in yeasts. Plant Cell Physiol. 2004, 45:1669-1680.
27. Lehle L., Strahl S., Tanner W. Protein glycosylation, conserved from yeast to man: a model organism helps elucidate congenital human diseases. Angew. Chem. Int. Ed. 2006, 45:6802-6818.
28. Lesage G., Sdicu A.M., Menard P., Shapiro J., Hussein S., Bussey H. Analysis of beta-1,3-glucan assembly in Saccharomyces cerevisiae using a synthetic interaction network and altered sensitivity to caspofungin. Genetics 2004, 167:35-49.
29. Lien E.C., Nagiec M.J., Dohlman H.G. Proper protein glycosylation promotes mitogen-activated protein kinase signal fidelity. Biochemistry 2013, 52:115-124.
30. López-García B., Pérez-Payá E., Marcos J.F. Identification of novel hexapeptides bioactive against phytopathogenic fungi through screening of a synthetic peptide combinatorial library. Appl. Environ. Microbiol. 2002, 68:2453-2460.
31. López-García B., Gandía M., Muñoz A., Carmona L., Marcos J.F. A genomic approach highlights common and diverse effects and determinants of susceptibility on the yeast Saccharomyces cerevisiae exposed to distinct antimicrobial peptides. BMC Microbiol. 2010, 10:289.
32. Lussier M., Gentzsch M., Sdicu A.M., Bussey H., Tanner W. Protein O-glycosylation in yeast. The PMT2 gene specifies a second protein O-mannosyltransferase that functions in addition to the PMT1-encoded activity. J. Biol. Chem. 1995, 270:2770-2775.
33. Marcos J.F., Gandía M. Antimicrobial peptides: to membranes and beyond. Expert Opin. Drug Discov. 2009, 4:659-671.
34. Marcos J.F., Muñoz A., Pérez-Payá E., Misra S., López-García B. Identification and rational design of novel antimicrobial peptides for plant protection. Annu. Rev. Phytopathol. 2008, 46:273-301.
35. Marcos J.F., Gandía M., Harries E., Carmona L., Muñoz A. Antifungal peptides: exploiting non-lytic mechanisms and cell penetration properties. Small Wonders: Peptides for Disease Control 2012, 337-357. American Chemical Society. K. Rajasekaran, J.W. Cary, J. Jaynes, E. Montesinos (Eds.).
36. Markovich S., Yekutiel A., Shalit I., Shadkchan Y., Osherov N. Genomic approach to identification of mutations affecting caspofungin susceptibility in Saccharomyces cerevisiae. Antimicrob. Agents Chemother. 2004, 48:3871-3876.
37. Mochon A.B., Liu H.P. 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. 2008, 4:e1000190.
38. Morton C.O., Hayes A., Wilson M., Rash B.M., Oliver S.G., Coote P. Global phenotype screening and transcript analysis outlines the inhibitory mode(s) of action of two amphibian-derived, α-helical, cationic peptides on Saccharomyces cerevisiae. Antimicrob. Agents Chemother. 2007, 51:3948-3959.
39. Mouyna I., Kniemeyer O., Jank T., Loussert C., Mellado E., Aimanianda V., Beauvais A., Wartenberg D., Sarfati J., Bayry J., Prevost M.C., Brakhage A.A., Strahl S., Huerre M., Latge J.P. Members of protein O-mannosyltransferase family in Aspergillus fumigatus differentially affect growth, morphogenesis and viability. Mol. Microbiol. 2010, 76:1205-1221.
40. Muñoz A., López-García B., Marcos J.F. Studies on the mode of action of the antifungal hexapeptide PAF26. Antimicrob. Agents Chemother. 2006, 50:3847-3855.
41. Muñoz A., Marcos J.F., Read N.D. Concentration-dependent mechanisms of cell penetration and killing by the de novo designed antifungal hexapeptide PAF26. Mol. Microbiol. 2012, 85:89-106.
42. Muñoz A., Gandía M., Harries E., Carmona L., Read N.D., Marcos J.F. Understanding the mechanism of action of cell-penetrating antifungal peptides using the rationally designed hexapeptide PAF26 as a model. Fungal Biol. Rev. 2013, 26:146-155.
43. Muñoz A., Harries E., Contreras-Valenzuela A., Carmona L., Read N.D., Marcos J.F. Two functional motifs define the interaction, internalization and toxicity of the cell-penetrating antifungal peptide PAF26 on fungal cells. PLoS ONE 2013, 8:e54813.
44. Munro C.A., Bates S., Buurman E.T., Hughes H.B., MacCallum D.M., Bertram G., Atrih A., Ferguson M.A.J., Bain J.M., Brand A., Hamilton S., Westwater C., Thomson L.M., Brown A.J.P., Odds F.C., Gow N.A.R. Mnt1p and Mnt2p of Candida albicans are partially redundant α-1,2-mannosyltransferases that participate in O-linked mannosylation and are required for adhesion and virulence. J. Biol. Chem. 2005, 280:1051-1060.
45. Nakamura T., Ando A., Takagi H., Shima J. EOS1, whose deletion confers sensitivity to oxidative stress, is involved in N-glycosylation in Saccharomyces cerevisiae Biochem. Biophys. Res. Commun. 2007, 353:293-298.
46. Nakamura T., Takahashi S., Takagi H., Shima J. Multicopy suppression of oxidant-sensitive eos1 mutation by IZH2 in Saccharomyces cerevisiae and the involvement of Eos1in zinc homeostasis. FEMS Yeast Res. 2010, 10:259-269.
47. Peters B.M., Shirtliff M.E., Jabra-Rizk M.A. Antimicrobial peptides: primeval molecules or future drugs?. PLoS Pathog. 2010, 6:e1001067.
48. Petit J., Boisseau P., Arveiler B. Glucanex: a cost-effective yeast lytic enzyme. Trends Genet. 1994, 10:4-5.
49. Prill S.K.H., Klinkert B., Timpel C., Gale C.A., Schroppel K., Ernst J.F. PMT family of Candida albicans: five protein mannosyltransferase isoforms affect growth, morphogenesis and antifungal resistance. Mol. Microbiol. 2005, 55:546-560.
50. Rayner J.C., Munro S. Identification of the MNN2 and MNN5 mannosyltransferases required for forming and extending the mannose branches of the outer chain mannans of Saccharomyces cerevisiae. J. Biol. Chem. 1998, 273:26836-26843.
51. Schirawski J., Böhnert H.U., Steinberg G., Snetselaar K., Adamikowa L., Kahmann R. Endoplasmic reticulum glucosidase II is required for pathogenicity of Ustilago maydis. Plant Cell. 2005, 17:3532-3543.
52. Steiner H., Hultmark D., Engstrom A., Bennich H., Boman H.G. Sequence and specificity of 2 anti-bacterial proteins involved in insect immunity. Nature 1981, 292:246-248.
53. Strahl-Bolsinger S., Gentzsch M., Tanner W. Protein O-mannosylation. Biochim. Biophys. Acta 1999, 1426:297-307.
54. Sun J.N.N., Li W.S., Jang W.S., Nayyar N., Sutton M.D., Edgerton M. Uptake of the antifungal cationic peptide Histatin 5 by Candida albicans Ssa2p requires binding to non-conventional sites within the ATPase domain. Mol. Microbiol. 2008, 70:1246-1260.
55. Szafranski-Schneider E., Swidergall M., Cottier F., Tielker D., Roman E., Pla J., Ernst J.F. Msb2 shedding protects Candida albicans against antimicrobial peptides. PLoS Pathog. 2012, 8:e1002501.
56. Tatebayashi K., Tanaka K., Yang H.Y., Yamamoto K., Matsushita Y., Tomida T., Imai M., Saito H. Transmembrane mucins Hkr1 and Msb2 are putative osmosensors in the SHO1 branch of yeast HOG pathway. EMBO J. 2007, 26:3521-3533.
57. Terwillinger T.C., Eisenberg D. The structure of melittin. II. Interpretation of the structure. J. Biol. Chem. 1982, 257:6016-6022.
58. van der Weerden N.L., Hancock R.E.W., Anderson M.A. Permeabilization of fungal hyphae by the plant defensin NaD1 occurs through a cell wall-dependent process. J. Biol. Chem. 2010, 285:37513-37520.
59. Vylkova S., Jang W.S., Li W.S., Nayyar N., Edgerton M. Histatin 5 initiates osmotic stress response in Candida albicans via activation of the Hog1 mitogen-activated protein kinase pathway. Eukaryot. Cell 2007, 6:1876-1888.
60. Yang H.Y., Tatebayashi K., Yamamoto K., Saito H. Glycosylation defects activate filamentous growth Kss1 MAPK and inhibit osmoregulatory Hog1 MAPK. EMBO J. 2009, 28:1380-1391.
61. Yeaman M.R., Yount N.Y. Mechanisms of antimicrobial peptide action and resistance. Pharmacol. Rev. 2003, 55:27-55.
62. Zasloff M. Antimicrobial peptides of multicellular organisms. Nature 2002, 415:389-395.
63. Zhou H., Hu H.Y., Zhang L.J., Li R.Y., Ouyang H.M., Ming J., Jin C. O-mannosyltransferase 1 in Aspergillus fumigatus (AfPmt1p) is crucial for cell wall integrity and conidium morphology, especially at an elevated temperature. Eukaryot. Cell 2007, 6:2260-2268.