An Antimicrobial Peptidomimetic Induces Mucorales Cell Death through Mitochondria-Mediated Apoptosis

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Barbu, E Magda ^a   Shirazi, Fazal ^a   McGrath, Danielle M ^a,d   Albert, Nathaniel ^a   Sidman, Richard L ^b,c   Pasqualini, Renata ^a   Arap, Wadih ^a,e   Kontoyiannis, Dimitrios P ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^d TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

^e UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; CYSTYLVALYLARGINYLALANYLCYSTEINE; FLUCONAZOLE; LYSYLLEUCYLALANYLLYSYLLEUCYLLYSINE; PEPTIDOMIMETIC AGENT; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ANTIFUNGAL SUSCEPTIBILITY; APOPTOSIS; ARTICLE; BACTERIAL CELL; CELL DAMAGE; CELL DEATH; CELL VACUOLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; FUNGAL SPORE GERMINATION; FUNGAL VIABILITY; FUNGICIDAL ACTIVITY; IN VITRO STUDY; MEMBRANE DEPOLARIZATION; MINIMUM FUNGICIDAL CONCENTRATION; MINIMUM INHIBITORY CONCENTRATION; MITOCHONDRIAL MEMBRANE; MITOCHONDRION SWELLING; NONHUMAN; RHIZOPUS ORYZAE;

ACETYLCYSTEINE; AMINO ACID MOTIFS; ANTIMICROBIAL CATIONIC PEPTIDES; APOPTOSIS; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICROBIAL SENSITIVITY TESTS; MICROBIAL VIABILITY; MITOCHONDRIA; MUCORALES; MUCORMYCOSIS; PEPTIDOMIMETICS; REACTIVE OXYGEN SPECIES; SPORES, FUNGAL;

EID: 84884829581     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076981     Document Type: Article

References (48)

1. Kontoyiannis DP, Lewis RE, (2006) Invasive Zygomycosis: update on pathogenesis, clinical manifestations, and management. Infect Dis Clin North Am 20(3):: 581-607. doi:10.1016/j.idc.2006.06.003. PubMed: 16984870.
2. Pfaller MA, (2012) Antifungal drug resistance: mechanisms, epidemiology, and consequences for treatment. Am J Med 125 (1 Suppl)():: S3-13. doi:10.1016/j.amjmed.2011.05.012. PubMed: 22196207.
3. Ostrosky-Zeichner L, (2012) Invasive mycoses: diagnostic challenges. Am J Med 125 (1 Suppl)():: S14-S24. doi:10.1016/j.amjmed.2011.10.008. PubMed: 22196205.
4. Gray KC, Palacios DS, Dailey I, Endo MM, Uno BE, et al. (2012) Amphotericin primarily kills yeast by simply binding ergosterol. Proc Natl Acad Sci U S A 109(7):: 2234-2239. doi:10.1073/pnas.1117280109. PubMed: 22308411.
5. Hof H, (2006) A new, broad-spectrum azole antifungal: posaconazole--mechanisms of action and resistance, spectrum of activity. Mycoses 49 (Suppl 1):: 2-6. doi:10.1111/j.1439-0507.2006.01295.x. PubMed: 16961575.
6. Ma LJ, Ibrahim AS, Skory C, Grabherr MG, Burger G, et al. (2009) Genomic analysis of the basal lineage fungus Rhizopus oryzae reveals a whole-genome duplication. PLOS Genet 5(7):: e1000549. PubMed: 19578406.
7. Jenssen H, Hamill P, Hancock RE, (2006) Peptide antimicrobial agents. Clin Microbiol Rev 19(3):: 491-511. doi:10.1128/CMR.00056-05. PubMed: 16847082.
8. Marr AK, Gooderham WJ, Hancock RE, (2006) Antibacterial peptides for therapeutic use: obstacles and realistic outlook. Curr Opin Pharmacol 6(5):: 468-472. doi:10.1016/j.coph.2006.04.006. PubMed: 16890021.
9. Matejuk A, Leng Q, Begum MD, Woodle MC, Scaria P, et al. (2010) Peptide-based antifungal therapies against emerging infections. Drugs Future 35(3):: 197. PubMed: 20495663.
10. Peters BM, Shirtliff ME, Jabra-Rizk MA, (2010) Antimicrobial peptides: primeval molecules or future drugs? PLOS Pathog 6(10):: e1001067.
11. Maloy WL, Kari UP, (1995) Structure-activity studies on magainins and other host defense peptides. Biopolymers 37: 105-122. doi:10.1002/bip.360370206. PubMed: 7893944.
12. Bessalle R, Kapitkovsky A, Gorea A, Shalit I, Fridkin M, (1990) All-D-magainin: chirality, antimicrobial activity and proteolytic resistance. FEBS Lett 274(1-2):: 151-155. doi:10.1016/0014-5793(90)81351-N. PubMed: 2253768.
13. Porter EA, Wang X, Lee HS, Weisblum B, Gellman SH, (2000) Non-haemolytic beta-amino-acid oligomers. Nature 404: 565. doi:10.1038/35007145. PubMed: 10766230.
14. Ellerby HM, Arap W, Ellerby LM, Kain R, Andrusiak R, et al. (1999) Anti-cancer activity of targeted pro-apoptotic peptides. Nat Med 5(9):: 1032-1038. doi:10.1038/12469. PubMed: 10470080.
15. Arap W, Haedicke W, Bernasconi M, Kain R, Rajotte D, et al. (2002) Targeting the prostate for destruction through a vascular address. Proc Natl Acad Sci U S A 99(3):: 1527-1531. doi:10.1073/pnas.241655998. PubMed: 11830668.
16. Lahdenranta J, Sidman RL, Pasqualini R, Arap W, (2007) Treatment of hypoxia-induced retinopathy with targeted proapoptotic peptidomimetic in a mouse model of disease. FASEB J 21(12):: 3272-3278. doi:10.1096/fj.07-8273com. PubMed: 17513561.
17. Zurita AJ, Troncoso P, Cardó-Vila M, Logothetis CJ, Pasqualini R, et al. (2004) Combinatorial screenings in patients: the interleukin-11 receptor alpha as a candidate target in the progression of human prostate cancer. Cancer Res 64(2):: 435-439. doi:10.1158/0008-5472.CAN-03-2675. PubMed: 14744752.
18. Kolonin MG, Saha PK, Chan L, Pasqualini R, Arap W, (2004) Reversal of obesity by targeted ablation of adipose tissue. Nat Med 10(6):: 625-632. doi:10.1038/nm1048. PubMed: 15133506.
19. Cardó-Vila M, Giordano RJ, Sidman RL, Bronk LF, Fan Z, et al. (2010) From combinatorial peptide selection to drug prototype (II): targeting the epidermal growth factor receptor pathway. Proc Natl Acad Sci U S A 107(11):: 5118-5123. doi:10.1073/pnas.0915146107. PubMed: 20190183.
20. Giordano RJ, Cardó-Vila M, Salameh A, Anobom CD, Zeitlin BD, et al. (2010) From combinatorial peptide selection to drug prototype (I): targeting the vascular endothelial growth factor receptor pathway. Proc Natl Acad Sci U S A 107(11):: 5112-5117. doi:10.1073/pnas.0915141107. PubMed: 20190181.
21. Barnhart KF, Christianson DR, Hanley PW, Driessen WH, Bernacky BJ, et al. (2011) A peptidomimetic targeting white fat causes weight loss and improved insulin resistance in obese monkeys. Sci Transl Med 3(108):: 108-112.
22. Onuchic JN, Jennings PA, Ben-Jacob E, (2013) Learning from cancer how to defeat bacteria. Proc Natl Acad Sci U S A 110(9):: 3212-3213. doi:10.1073/pnas.1222882110. PubMed: 23407166.
23. McGrath DM, Barbu EM, Driessen WH, Lasco TM, Tarrand JJ, et al. (2013) Mechanism of action and initial evaluation of a membrane active all-D-enantiomer antimicrobial peptidomimetic. Proc Natl Acad Sci U S A 110(9):: 3477-3482. doi:10.1073/pnas.1221924110. PubMed: 23345420.
24. Ben-Ami R, Lewis RE, Tarrand J, Leventakos K, Kontoyiannis DP, (2010) Antifungal activity of colistin against mucorales species in vitro and in a murine model of Rhizopus oryzae pulmonary infection. Antimicrob Agents Chemother 54(1):: 484-490. doi:10.1128/AAC.00956-09. PubMed: 19858263.
25. Clinical and Laboratory Standards Institute (2012) Performance standards for antimicrobial susceptibility testing. Document M100-S19. Available: http://www.clsi.org/. Accessed May1, 2013.
26. Vitale RG, Meis JF, Mouton JW, Verweij PE, (2003) Evaluation of the post-antifungal effect (PAFE) of amphotericin B and nystatin against 30 zygomycetes using two different media. J Antimicrob Chemother 52(1):: 65-70. doi:10.1093/jac/dkg285. PubMed: 12775672.
27. Meletiadis J, Mouton JW, Meis JF, Bouman BA, Donnelly JP, et al. (2001) Colorimetric assay for antifungal susceptibility testing of Aspergillus species. J Clin Microbiol 39(9):: 3402-3408. doi:10.1128/JCM.39.9.3402-3408.2001. PubMed: 11526191.
28. Antachopoulos C, Meletiadis J, Roilides E, Sein T, Walsh TJ, (2006) Rapid susceptibility testing of medically important zygomycetes by XTT assay. J Clin Microbiol 44(2):: 553-560. doi:10.1128/JCM.44.2.553-560.2006. PubMed: 16455912.
29. Higgins DL, Chang R, Debabov DV, Leung J, Wu T, et al. (2005) Telavancin, a multifunctional lipoglycopeptide, disrupts both cell wall synthesis and cell membrane integrity in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 49(3):: 1127-1134. doi:10.1128/AAC.49.3.1127-1134.2005. PubMed: 15728913.
30. Vida TA, Emr SD, (1995) A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J Cell Biol 128(5):: 779-792. doi:10.1083/jcb.128.5.779. PubMed: 7533169.
31. Phillips AJ, Sudbery I, Ramsdale M, (2003) Apoptosis induced by environmental stresses and amphotericin B in Candida albicans. Proc Natl Acad Sci U S A 100(24):: 14327-14332. doi:10.1073/pnas.2332326100. PubMed: 14623979.
32. Shirazi F, Kontoyiannis DP, (2013) Mitochondrial respiratory pathways inhibition in Rhizopus oryzae potentiates activity of posaconazole and itraconazole via apoptosis. PLOS ONE 8(5):: e63393. doi:10.1371/journal.pone.0063393. PubMed: 23696824.
33. Zoratti M, Szabò I, (1995) The mitochondrial permeability transition. Biochim Biophys Acta 1241(2):: 139-176. doi:10.1016/0304-4157(95)00003-A. PubMed: 7640294.
34. Niimi K, Harding DR, Parshot R, King A, Lun DJ, et al. (2004) Chemosensitization of fluconazole resistance in Saccharomyces cerevisiae and pathogenic fungi by a D-octapeptide derivative. Antimicrob Agents Chemother 48(4):: 1256-1271. doi:10.1128/AAC.48.4.1256-1271.2004. PubMed: 15047528.
35. Wu XZ, Cheng AX, Sun LM, Sun SJ, Lou HX, (2009) Plagiochin E, an antifungal bis(bibenzyl), exerts its antifungal activity through mitochondrial dysfunction-induced reactive oxygen species accumulation in Candida albicans. Biochim Biophys Acta 1790(8):: 439-447. PubMed: 19446008.
36. Grove SN, Bracker CE, (1970) Protoplasmic organization of hyphal tips among fungi: Vesicles and Spitzenkörper. J Bacteriol 104(2):: 989-1009. PubMed: 4099103.
37. Kirimura K, Ogawa S, Hattori T, Kino K, (2006) Expression analysis of alternative oxidase gene (aox1) with enhanced green fluorescent protein as marker in citric acid-producing Aspergillus niger. J Biosci Bioeng 102(3):: 210-214. doi:10.1263/jbb.102.210. PubMed: 17046535.
38. Madeo F, Fröhlich E, Ligr M, Grey M, Sigrist SJ, et al. (1999) Oxygen stress: a regulator of apoptosis in yeast. J Cell Biol 145(4):: 757-767. doi:10.1083/jcb.145.4.757. PubMed: 10330404.
39. Cho J, Lee DG, (2011) The characteristic region of arenicin-1 involved with a bacterial membrane targeting mechanism. Biochem Biophys Res Commun 405(3):: 422-427. doi:10.1016/j.bbrc.2011.01.046. PubMed: 21241661.
40. Uren AG, O'Rourke K, Aravind LA, Pisabarro MT, Seshagiri S, et al. (2000) Identification of paracaspases and metacaspases: two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma. Mol Cell 6(4):: 961-967. doi:10.1016/S1097-2765(05)00086-9. PubMed: 11090634.
41. Tsiatsiani L, Van Breusegem F, Gallois P, Zavialov A, Lam E, et al. (2011) Metacaspases. Cell Death Differ 18(8):: 1279-1288. doi:10.1038/cdd.2011.66. PubMed: 21597462.
42. Simon HU, Haj-Yehia A, Levi-Schaffer F, (2000) Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 5(5):: 415-418. doi:10.1023/A:1009616228304. PubMed: 11256882.
43. Hwang B, Hwang JS, Lee J, Lee DG, (2011) The antimicrobial peptide, psacotheasin induces reactive oxygen species and triggers apoptosis in Candida albicans. Biochem Biophys Res Commun 405(2):: 267-271. doi:10.1016/j.bbrc.2011.01.026. PubMed: 21219857.
44. Perrone GG, Tan SX, Dawes IW, (2008) Reactive oxygen species and yeast apoptosis. Biochim Biophys Acta 1783(7):: 1354-1368. doi:10.1016/j.bbamcr.2008.01.023. PubMed: 18298957.
45. Tian J, Ban X, Zeng H, He J, Chen Y, et al. (2012) The mechanism of antifungal action of essential oil from dill (Anethum graveolens L.) on Aspergillus flavus. PLOS ONE 7(1):: e30147. doi:10.1371/journal.pone.0030147. PubMed: 22272289.
46. Farina C, Marchesi G, Passera M, Diliberto C, Russello G, et al. (2012) In vitro activity of Amphotericin B against zygomycetes isolated from deep mycoses: a comparative study between incubation in aerobic and hyperbaric atmosphere. Med Mycol 50(4):: 427-432. doi:10.3109/13693786.2011.614964. PubMed: 21954953.
47. Weber SU, Koch A, Kankeleit J, Schewe JC, Siekmann U, et al. (2009) Hyperbaric oxygen induces apoptosis via a mitochondrial mechanism. Apoptosis 14(1):: 97-107. doi:10.1007/s10495-008-0280-z. PubMed: 19052874.
48. Lionakis MS, Lahdenranta J, Sun J, Liu W, Lewis RE, et al. (2005) Development of a ligand-directed approach to study the pathogenesis of invasive aspergillosis. Infect Immun 73(11):: 7747-7758. doi:10.1128/IAI.73.11.7747-7758.2005. PubMed: 16239579.