Purpurin triggers caspase-independent apoptosis in Candida dubliniensis biofilms

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Tsang, Paul Wai Kei ^a   Wong, Alan Pak Kin ^a   Yang, Hai Ping ^a   Li, Ngai For ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRAQUINONES; APOPTOSIS; BIOFILMS; CANDIDA; DRUG RESISTANCE, FUNGAL; IN SITU NICK-END LABELING; MICROSCOPY, ELECTRON, SCANNING; REACTIVE OXYGEN SPECIES; STATISTICS, NONPARAMETRIC;

EID: 84893485001     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0086032     Document Type: Article

References (52)

1. Parize P, Rammaert B, Lortholary O (2012) Emerging invasive fungal diseases in transplantation. Curr Infect Dis Rep 14: 668-675. doi:10.1007/s11908-012-0296-y. PubMed: 23065419.
2. Garcia-Vidal C, Viasus D, Carratalà J (2013) Pathogenesis of invasive fungal infections. Curr Opin Infect Dis 26: 270-276. doi:10.1097/QCO.0b013e32835fb920. PubMed: 23449139.
3. Hundalani S, Pammi M (2013) Invasive fungal infections in newborns and current management strategies. Expert Rev Anti Infect Ther 11:709-721. doi:10.1586/14787210.2013.811925. PubMed: 23829639.
4. Corner BE, Magee PT (1997) Candida pathogenicity: unravelling the threads of infection. Curr Biol 7: R691-R694. doi:10.1016/S0960-9822(06)00357-5. PubMed: 9382797. (Pubitemid 27493108)
5. Wenzel RP, Gennings C (2005) Bloodstream infections due to Candida species in the intensive care unit: identifying especially high-risk patients to determine prevention strategies. Clin Infect Dis 41: S389-S393. doi:10.1086/430923. PubMed: 16108005. (Pubitemid 41266739)
6. Bustamante CI (2005) Treatment of Candida infection: a view from the trenches! Curr Opin Infect Dis 18: 490-495. doi:10.1097/01.qco.0000191516.43792. 61. PubMed: 16258321.
7. Miceli MH, Díaz JA, Lee SA (2011) Emerging opportunistic yeast infections. Lancet Infect Dis 11: 142-151. doi:10.1016/S1473-3099(10)70218-8. PubMed: 21272794.
8. Bassetti M, Righi E, Costa A, Fasce R, Molinari MP et al. (2006) Epidemiological trends in nosocomial candidemia in intensive care. BMC Infect Dis 6: 21. doi:10.1186/1471-2334-6-21. PubMed: 16472387.
9. Colombo AL, Nucci M, Salomão R, Branchini ML, Richtmann R et al. (1999) High rate of non-albicans candidemia in Brazilian tertiary care hospitals. Diagn Microbiol Infect Dis 34: 281-286. doi:10.1016/S0732-8893(99) 00042-5. PubMed: 10459478.
10. Dimopoulos G, Ntziora F, Rachiotis G, Armaganidis A, Falagas ME (2008) Candida albicans versus non-albicans intensive care unit-acquired bloodstream infections: differences in risk factors and outcome. Anesth Analg 106: 523-529. doi:10.1213/ane.0b013e3181607262. PubMed: 18227310. (Pubitemid 351156678)
11. Chow JK, Golan Y, Ruthazer R, Karchmer AW, Carmeli Y et al. (2008) Factors associated with candidemia caused by non-albicans Candida species versus Candida albicans in the intensive care unit. Clin Infect Dis 46: 1206-1213. doi:10.1086/529435. PubMed: 18444857. (Pubitemid 351589904)
12. Sullivan DJ, Moran GP, Coleman DC (2005) Candida dubliniensis: ten years on. FEMS Microbiol Lett 253: 9-17. doi:10.1016/j.femsle.2005.09.015. PubMed: 16213674. (Pubitemid 41605389)
13. Willis AM, Coulter WA, Sullivan DJ, Coleman DC, Hayes JR et al. (2000) Isolation of Candida dubliniensis from insulin-using diabetes mellitus patients. J Oral Pathol Med 29: 86-90. doi:10.1034/j.1600-0714.2000.290206.x. PubMed: 10718404. (Pubitemid 30104872)
14. Polacheck I, Strahilevitz J, Sullivan D, Donnelly S, Salkin IF et al. (2000) Recovery of Candida dubliniensis from non-human immunodeficiency virus-infected patients in Israel. J Clin Microbiol 38:170-174. PubMed: 10618082. (Pubitemid 30043283)
15. Jabra-Rizk MA, Johnson JK, Forrest G, Mankes K, Meiller TF et al. (2005) Prevalence of Candida dubliniensis fungemia at a large teaching hospital. Clin Infect Dis 41: 1064-1067. doi:10.1086/432943. PubMed: 16142677. (Pubitemid 41368235)
16. Sullivan DJ, Moran GP, Pinjon E, Al-Mosaid A, Stokes C et al. (2004) Comparison of the epidemiology, drug resistance mechanisms, and virulence of Candida dubliniensis and Candida albicans. FEMS Yeast Res 4: 369-376. doi:10.1016/S1567-1356(03)00240-X. PubMed: 14734017. (Pubitemid 38156201)
17. Moran GP, Sullivan DJ, Henman MC, McCreary CE, Harrington BJ et al. (1997) Antifungal drug susceptibilities of oral Candida dubliniensis isolates from human immunodeficiency virus (HIV)-infected and non-infected subjects and generation of stable fluconazole-resistant derivatives in vitro. Antimicrob Agents Chemother 41: 617-623. PubMed: 9056003. (Pubitemid 27098414)
18. Fanci R (2009) Breakthrough Candida dubliniensis fungemia in an acute myeloid leukemia patient during voriconazole therapy successfully treated with caspofungin. J Chemother 21: 105-107. PubMed: 19297283.
19. Kang K, Fong WP, Tsang PWK (2010) Novel antifungal activity of purpurin against Candida species in vitro. Med Mycol 48: 904-911. doi:10.3109/ 13693781003739351. PubMed: 20392152.
20. Tsang PWK, Bandara HMHN, Fong WP (2012) Purpurin suppresses Candida albicans biofilm formation and hyphal development. PLOS ONE 7: e50866. doi:10.1371/journal.pone.0050866. PubMed: 23226409.
21. Jackson AP, Gamble JA, Yeomans T, Moran GP, Saunders D et al. (2009) Comparative genomics of the fungal pathogens Candida dubliniensis and Candida albicans. Genome Res 19: 2231-2244. doi:10.1101/gr.097501.109. PubMed: 19745113.
22. Moran GP, Coleman DC, Sullivan DJ (2012) Candida albicans versus Candida dubliniensis: why is C. albicans more pathogenic? Int J Microbiol 2012: 205921
23. Pannanusorn S, Fernandez V, Römling U (2013) Prevalence of biofilm formation in clinical isolates of Candida species causing bloodstream infection. Mycoses 56: 264-272. doi:10.1111/myc.12014. PubMed: 23113805.
24. Ramage G, Vande Walle K, Wickes BL, López-Ribot JL (2001) Biofilm formation by Candida dubliniensis. J Clin Microbiol 39: 3234-3240. doi:10.1128/JCM.39.9.3234-3240.2001. PubMed: 11526156. (Pubitemid 32830320)
25. Ásmundsdóttir LR, Erlendsdóttir H, Agnarsson BA, Gottfredsson M (2009) The important of strain variation in virulence of Candida dubliniensis and Candida albicans: results of a blinded histopathological study of invasive candidiasis. Clin Microbiol Infect 15:576-585. doi:10.1111/j.1469- 0691.2009.02840.x. PubMed: 19604278.
26. Lorenz MC, Bender JA, Fink GR (2004) Transcriptional response of Candida albicans upon internalization by macrophages. Eukaryot Cell 3: 1076-1087. doi:10.1128/EC.3.5.1076-1087.2004. PubMed: 15470236. (Pubitemid 39385215)
27. ten Cate JM, Klis FM, Pereira-Cenci T, Crielaard W, de Groot PW (2009) Molecular and cellular mechanisms that lead to Candida biofilm formation. J Dent Res 88: 105-115. doi:10.1177/0022034508329273. PubMed: 19278980.
28. Dongari-Bagtzoglou A (2008) Pathogenesis of mucosal biofilms infections: challenges and progress. Expert Rev Anti Infect Ther 6:201-208. doi:10.1586/14787210.6.2.201. PubMed: 18380602.
29. Ruhnke M (2006) Epidemiology of Candida albicans infections and role of non-Candida albicans yeasts. Curr Drug Targets 7: 495-504. doi:10.2174/ 138945006776359421. PubMed: 16611037.
30. Khan Z, Ahmad S, Joseph L, Chandy R (2012) Candida dubliniensis: an appraisal of its clinical significance as a bloodstream pathogen. PLOS ONE 7: e32952. doi:10.1371/journal.pone.0032952. PubMed: 22396802.
31. Shirtliff ME, Krom BP, Meijering RA, Peters BM, Zhu J et al. (2009) Farnesol-induced apoptosis in Candida albicans. Antimicrob Agents Chemother 53: 2392-2401. doi:10.1128/AAC.01551-08. PubMed: 19364863.
32. 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: 14327-14332. doi:10.1073/pnas.2332326100. PubMed: 14623979. (Pubitemid 37499236)
33. + efflux. Antimicrob Agents Chemother 52: 4081-4088. doi:10.1128/AAC.01597-07. PubMed: 18710913.
34. Al-Dhaheri RS, Douglas LJ (2010) Apoptosis in Candida biofilms exposed to amphotericin B. J Med Microbiol 59: 149-157. doi:10.1099/jmm.0.015784-0. PubMed: 19892857.
35. Keyhani E, Khavari-Nejad S, Keyhani J, Attar F (2009) Acriflavine-mediated apoptosis and necrosis in yeast Candida utilis. Ann N Y Acad Sci 1171: 284-291. doi:10.1111/j.1749-6632.2009.04682.x. PubMed: 19723067.
36. Kang K, Wong KS, Fong WP, Tsang PWK (2011) Metergoline-induced cell death in Candida krusei. Fungal Biol 115: 302-309. doi:10.1016/j.funbio.2011.01.001. PubMed: 21354537.
37. Pradelli LA, Bénéteau M, Ricci JE (2010) Mitochondrial control of caspase-dependent and -independent cell death. Cell Mol Life Sci 67:1589-1597. doi:10.1007/s00018-010-0285-y. PubMed: 20151314.
38. Estaquier J, Vallette F, Vayssiere JL, Mignotte B (2012) The mitochondrial pathways of apoptosis. Adv Exp Med Biol 942: 157-183. doi:10.1007/978-94-007-2869-1-7. PubMed: 22399422.
39. Borutaite V (2010) Mitochondria as decision-makers in cell death. Environ Mol Mutagen 51: 406-416. PubMed: 20209625.
40. Karbowski M (2010) Mitochondria on guard: role of mitochondrial fusion and fission in the regulation of apoptosis. Adv Exp Med Biol 687:131-142. doi:10.1007/978-1-4419-6706-0-8. PubMed: 20919642.
41. Cao YY, Huang S, Dai B, Zhu Z, Lu H et al. (2009) Candida albicans cells lacking CaMCA1-encoded metacaspase show resistance to oxidative stress-induced death and change in energy metabolism. Fungal Genet Biol 46: 183-189. doi:10.1016/j.fgb.2008.11.001. PubMed: 19049890.
42. Pozniakovsky AI, Knorre DA, Markova OV, Hyman AA, Skulachev VP et al. (2005) Role of mitochondria in the pheromone- and amiodarone-induced programmed cell death of yeast. J Cell Biol 168: 257-267. doi:10.1083/jcb.200408145. PubMed: 15657396.
43. Madeo F, Herker E, Wissing S, Jungwirth H et al. (2004) Apoptosis in yeast. Curr Opin Microbiol 7: 655-660. doi:10.1016/j.mib.2004.10.012. PubMed: 15556039. (Pubitemid 39536293)
44. Ramsdale M (2008) Programmed cell death in pathogenic fungi. Biochim Biophys Acta 1783: 1369-1380. doi:10.1016/j.bbamcr.2008.01.021. PubMed: 18294459.
45. Kang K, Fong WP, Tsang PWK (2010) Antifungal activity of baicalein against Candida krusei does not involve apoptosis. Mycopathologia 170: 391-396. doi:10.1007/s11046-010-9341-2. PubMed: 20614252.
46. Madeo F, Herker E, Maldener C, Wissing S, Lächelt S et al. (2002) A caspase-related protease regulates apoptosis in yeast. Mol Cell 9:911-917. doi:10.1016/S1097-2765(02)00501-4. PubMed: 11983181. (Pubitemid 34454900)
47. Barroso G, Taylor S, Morshedi M, Manzur F, Gaviño F et al. (2006) Mitochondrial membrane potential integrity and plasma membrane translocation of phosphatidylserine as early apoptotic markers: a comparison of two different sperm subpopulations. Fertil Steril 85:149-154. doi:10.1016/j.fertnstert.2005. 06.046. PubMed: 16412746. (Pubitemid 43063438)
48. Odds FC, Brown AJ, Gow NA (2003) Antifungal agents: mechanism of action. Trends Microbiol 11: 272-279. doi:10.1016/S0966-842X(03)00117-3. PubMed: 12823944.
49. Ghannoum MA, Rice LB (1999) Antifungal agents: mode of action, mechanisms of resistance, and correlation of these mechanisms with bacterial resistance. Clin Microbiol Rev 12: 501-517. PubMed: 10515900. (Pubitemid 29484744)
50. Zhang J, Heitman J, Chen YL (2012) Comparative analysis of calcineurin signaling between Candida dubliniensis and Candida albicans. Commun Integr Biol 5: 122-126. doi:10.4161/cib.18833. PubMed: 22808313.
51. Moran GP (2012) Transcript profiling reveals rewiring of iron assimilation gene expression in Candida albicans and Candida dubliniensis. FEMS Yeast Res 12: 918-923. doi:10.1111/j.1567-1364.2012.00841.x. PubMed: 22888912.
52. Bandara HMHN, Lam OL, Watt RM, Jin LJ, Samaranayake LP (2010) Bacterial lipopolysaccharides variably modulate in vitro biofilm formation of Candida species. J Med Microbiol 59: 1225-1234. doi:10.1099/jmm.0.021832-0. PubMed: 20576747.