Sensitivity of Saccharomyces cerevisiae to the cell-penetrating antifungal peptide PAF26 correlates with endogenous nitric oxide (NO) production

Biochemical and Biophysical Research Communications

Volumn 417, Issue 1, 2012, Pages 56-61

  Carmona, Lourdes ^a   Gandía, Mónica ^a   López García, Belén ^a,b   Marcos, Jose F ^a  

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

^b CSIC   (Spain)

Author keywords

Antifungal mechanism; Antimicrobial peptide; Nitric oxide; Reactive oxygen species; Saccharomyces cerevisiae

Indexed keywords

ANTIFUNGAL AGENT; ARGININE; CELL PENETRATING PEPTIDE; HEXAPEPTIDE; HYDROGEN PEROXIDE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; PAF 26; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR YAP1; UNCLASSIFIED DRUG;

ANTIFUNGAL ACTIVITY; ANTIFUNGAL RESISTANCE; ANTIFUNGAL SUSCEPTIBILITY; ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; FUNGAL CELL; FUNGAL STRAIN; FUNGUS GROWTH; GENE DELETION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE;

ANTIFUNGAL AGENTS; ARGINASE; DRUG RESISTANCE, FUNGAL; ENZYME INHIBITORS; GENE DELETION; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; OLIGOPEPTIDES; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS;

FUNGI; SACCHAROMYCES CEREVISIAE;

EID: 84855800455     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2011.11.050     Document Type: Article

References (40)

1. Zasloff M. Antimicrobial peptides of multicellular organisms. Nature 2002, 415:389-395.
2. Hancock R.E.W., Sahl H.G. Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat. Biotechnol. 2006, 24:1551-1557.
3. Marcos J.F., Muñoz A., Pérez-Payá E., Misra S., López-García B. Identification and rational design of novel antimicrobial peptides for plant protection. Ann. Rev. Phytopathol. 2008, 46:273-301.
4. Brogden K.A. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria?. Nat. Rev. Microbiol. 2005, 3:238-250.
5. Yount N.Y., Bayer A.S., Xiong Y.Q., Yeaman M.R. Advances in antimicrobial peptide immunobiology. Biopolymers 2006, 84:435-458.
6. Marcos J.F., Gandía M. Antimicrobial peptides: to membranes and beyond. Expert Opin. Drug Discov. 2009, 4:659-671.
7. Nicolas P. Multifunctional host defense peptides: intracellular-targeting antimicrobial peptides. FEBS J. 2009, 276:6483-6496.
8. 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.
9. Narasimhan M.L., Damsz B., Coca M.A., Ibeas J.I., Yun D.J., Pardo J.M., Hasegawa P.M., Bressan R.A. A plant defense response effector induces microbial apoptosis. Mol. Cell 2001, 8:921-930.
10. Leiter E., Szappanos H., Oberparleiter C., Kaiserer L., Csernoch L., Pusztahelyi T., Emri T., Pócsi I., Salvenmoser W., Marx F. Antifungal protein PAF severely affects the integrity of the plasma membrane of Aspergillus nidulans and induces an apoptosis-like phenotype. Antimicrob. Agents Chemother. 2005, 49:2445-2453.
11. Morton C.O., dos Santos S.C., Coote P. An amphibian-derived, cationic, a-helical antimicrobial peptide kills yeast by caspase-independent but AIF-dependent programmed cell death. Mol. Microbiol. 2007, 65:494-507.
12. + efflux. Antimicrob. Agents Chemother. 2008, 52:4081-4088.
13. Park C., Lee D.G. Melittin induces apoptotic features in Candida albicans. Biochem. Biophys. Res. Commun. 2010, 394:170-172.
14. Hwang B., Hwang J.S., Lee J., Lee D.G. The antimicrobial peptide, psacotheasin induces reactive oxygen species and triggers apoptosis in Candida albicans. Biochem. Biophys. Res. Commun. 2011, 405:267-271.
15. Mello E.O., Ribeiro S.F.F., Carvalho A.O., Santos I.S., Da Cunha M., Santa-Catarina C., Gomes V.M. Antifungal activity of PvD1 defensin involves plasma membrane permeabilization, inhibition of medium acidification, and induction of ROS in fungi cells. Curr. Microbiol. 2011, 62:1209-1217.
16. Aerts A.M., François I.E.J.A., Meert E.M.K., Li Q.T., Cammue B.P.A., Thevissen K. The antifungal activity of RsAFP2, a plant defensin from Raphanus sativus, involves the induction of reactive oxygen species in Candida albicans. J. Mol. Microbiol. Biotechnol. 2007, 13:243-247.
17. Lupetti A., Paulusma-Annema A., Senesi S., Campa M., van Dissel J.T., Nibbering P.H. Internal thiols and reactive oxygen species in candidacidal activity exerted by an N-terminal peptide of human lactoferrin. Antimicrob. Agents Chemother. 2002, 46:1634-1639.
18. Maurya I.K., Pathak S., Sharma M., Sanwal H., Chaudhary P., Tupe S., Deshpande M., Chauhan V.S., Prasad R. Antifungal activity of novel synthetic peptides by accumulation of reactive oxygen species (ROS) and disruption of cell wall against Candida albicans. Peptides 2011, 32:1732-1740.
19. Helmerhorst E.J., Troxler R.F., Oppenheim F.G. The human salivary peptide histatin 5 exerts its antifungal activity through the formation of reactive oxygen species. Proc. Natl. Acad. Sci. U S A 2001, 98:14637-14642.
20. Veerman E.C.I., Nazmi K., van Hof W., Bolscher J.G.M., den Hertog A.L., Amerongen A.V.N. Reactive oxygen species play no role in the candidacidal activity of the salivary antimicrobial peptide histatin 5. Biochem. J. 2004, 381:447-452.
21. Fang F.C. Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat. Rev. Microbiol. 2004, 2:820-832.
22. 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.
23. López-García B., Ubhayasekera W., Gallo R.L., Marcos J.F. Parallel evaluation of antimicrobial peptides derived from the synthetic PAF26 and the human LL37. Biochem. Biophys. Res. Commun. 2007, 356:107-113.
24. 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.
25. 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.
26. Osório N.S., Carvalho A., Almeida A.J., Padilla-Lopez S., Leao C., Laranjinha J., Ludovico P., Pearce D.A., Rodrigues F. Nitric oxide signaling is disrupted in the yeast model for batten disease. Mol. Biol. Cell 2007, 18:2755-2767.
27. Almeida B., Buttner S., Ohlmeier S., Silva A., Mesquita A., Sampaio-Marques B., Osório N.S., Kollau A., Mayer B., Leao C., Laranjinha J., Rodrigues F., Madeo F., Ludovico P. NO-mediated apoptosis in yeast. J. Cell Sci. 2007, 120:3279-3288.
28. Rodrigues-Pousada C., Menezes R.A., Pimentel C. The Yap family and its role in stress response. Yeast 2010, 27:245-258.
29. Kuge S., Jones N. Yap1 dependent activation of Trx2 is essential for the response of Saccharomyces cerevisiae to oxidative stress by hydroperoxides. EMBO J. 1994, 13:655-664.
30. 2 sensing through oxidation of the Yap1 transcription factor. EMBO J. 2000, 19:5157-5166.
31. Wood M.J., Storz G., Tjandra N. Structural basis for redox regulation of Yap1 transcription factor localization. Nature 2004, 430:917-921.
32. 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.
33. Horan S., Bourges I., Meunier B. Transcriptional response to nitrosative stress in Saccharomyces cerevisiae. Yeast 2006, 23:519-535.
34. Chiang K.T., Switzer C.H., Akali K.O., Fukuto J.M. The role of oxygen and reduced oxygen species in nitric oxide-mediated cytotoxicity: studies in the yeast Saccharomyces cerevisiae model system. Toxicol. Appl. Pharmacol. 2000, 167:30-36.
35. Domitrovic T., Palhano F.L., Barja-Fidalgo C., DeFreitas M., Orlando M.T.D., Fernandes P.M.B. Role of nitric oxide in the response of Saccharomyces cerevisiae cells to heat shock and high hydrostatic pressure. FEMS Yeast Res. 2003, 3:341-346.
36. Kig C., Temizkan G. Nitric oxide as a signaling molecule in the fission yeast Schizosaccharomyces pombe. Protoplasma 2009, 238:59-66.
37. Lushchak O.V., Inoue Y., Lushchak V.I. Regulatory protein yap1 is involved in response of yeast Saccharomyces cerevisiae to nitrosative stress. Biochemistry (Moscow) 2010, 75:629-635.
38. Tillmann A., Gow N.A., Brown A.J. Nitric oxide and nitrosative stress tolerance in yeast. Biochem. Soc. Trans. 2011, 39:219-223.
39. 2 and thiol-reactive chemicals signaling. Free Radic. Biol. Med. 2003, 35:889-900.
40. Coleman S.T., Epping E.A., Steggerda S.M., Moye-Rowley W.S. Yap1p activates gene transcription in an oxidant-specific fashion. Mol. Cell. Biol. 1999, 19:8302-8313.