Respiratory deficiency enhances the sensitivity of the pathogenic fungus Candida to photodynamic treatment

Photochemistry and Photobiology

Volumn 84, Issue 5, 2008, Pages 1141-1148

  Chabrier Roselló, Yeissa ^a   Foster, Thomas H ^a   Mitra, Soumya ^a   Haidaris, Constantine G ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIFUNGAL AGENT; PHOTOFRIN II; PHOTOSENSITIZING AGENT; PORPHYRIN; TETRA(3 N METHYLPYRIDYL)PORPHINE; TETRA(3-N-METHYLPYRIDYL)PORPHINE;

ARTICLE; BIOFILM; CANDIDA ALBICANS; CANDIDA GLABRATA; DRUG EFFECT; FUNGUS HYPHAE; GENETICS; METABOLISM; MICROBIOLOGICAL EXAMINATION; MITOCHONDRION; MUTATION; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PATHOGENICITY; PHOTOCHEMOTHERAPY;

ANTIFUNGAL AGENTS; BIOFILMS; CANDIDA ALBICANS; CANDIDA GLABRATA; DIHEMATOPORPHYRIN ETHER; HYPHAE; MICROBIAL SENSITIVITY TESTS; MITOCHONDRIA; MUTATION; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PHOTOCHEMOTHERAPY; PHOTOSENSITIZING AGENTS; PORPHYRINS;

CANDIDA; CANDIDA ALBICANS; CANDIDA GLABRATA; FUNGI; TETRA;

EID: 50849125739     PISSN: 00318655     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1751-1097.2007.00280.x     Document Type: Article

References (64)

1. Odds, F. C. (1988) Candida and Candidosis. Bailliere Tindall, London.
2. Cannon, R. D., A. R. Holmes, A. B. Mason B. C. Monk (1995) Oral Candida: Clearance, colonization, or candidiasis? J. Dent. Res. 74, 1152 1161.
3. Wenzel, R. P. (1995) Nosocomial candidemia: Risk factors and attributable mortality. Clin. Infect. Dis. 20, 1531 1534.
4. Fidel Jr., P. L., J. A. Vazquez J. D. Sobel (1999) Candida glabrata: Review of epidemiology, pathogenesis, and clinical disease with comparison to C. albicans. Clin. Microbiol. Rev. 12, 80 96.
5. Barchiesi, F., M. Maracci, B. Radi, D. Arzeni, I. Baldassarri, A. Giacometti G. Scalise (2002) Point prevalence, microbiology and fluconazole susceptibility patterns of yeast isolates colonizing the oral cavities of HIV-infected patients in the era of highly active antiretroviral therapy. J. Antimicrob. Chemother. 50, 999 1002.
6. Powderly, W. G. (1992) Mucosal candidiasis caused by non-albicans species of Candida in HIV-positive patients. AIDS 6, 593 606.
7. Johnson, E. M., D. W. Warnock, J. Luker, S. R. Porter C. Scully (1995) Emergence of azole drug resistance in Candida species from HIV-infected patients receiving prolonged fluconazole therapy for oral candidosis. J. Antimicrob. Chemother. 35, 103 114.
8. Dougherty, T. J., C. J. Gomer, B. W. Henderson, G. Jori, D. Kessel, M. Korbelik, J. Moan Q. Peng (1998) Photodynamic therapy. J. Nat'l Cancer Inst. 90, 889 905.
9. Brown, S. B., E. A. Brown I. Walker (2004) The present and future role of photodynamic therapy in cancer treatment. Lancet Oncol. 5, 497 508.
10. Mennel, S., I. Barbazetto, C. H. Meyer, S. Peter M. Stur (2007) Ocular photodynamic therapy - Standard applications and new indications (part 1). Review of the literature and personal experience. Ophthalmologica 221, 216 226.
11. Morton, C. A., S. B. Brown, S. Collins, S. Ibbotson, H. Jenkinson, H. Kurwa, K. Langmack, K. McKenna, H. Moseley, A. D. Pearse, M. Stringer, D. K. Taylor, G. Wong L. E. Rhodes (2002) Guidelines for topical photodynamic therapy: Report of a workshop of the British Photodermatology Group. Br. J. Dermatol. 146, 552 567.
12. Trauner, K. B., R. Gandour-Edwards, M. Bamberg, S. Shortkroff, C. Sledge T. Hasan (1998) Photodynamic synovectomy using benzoporphyrin derivative in an antigen-induced arthritis model for rheumatoid arthritis. Photochem. Photobiol. 67, 133 139.
13. Jori, G., C. Fabris, M. Soncin, S. Ferro, O. Coppellotti, D. Dei, L. Fantetti, G. Chiti G. Roncucci (2006) Photodynamic therapy in the treatment of microbial infections: Basic principles and perspective applications. Lasers Surg. Med. 38, 468 481.
14. Friedberg, J. S., C. Skema, E. D. Baum, J. Burdick, S. A. Vinogradov, D. F. Wilson, A. D. Horan I. Nachamkin (2001) In vitro effects of photodynamic therapy on Aspergillus fumigatus. J. Antimicrob. Chemother. 48, 105 107.
15. Smijs, T. G. H. J. Schuitmaker (2003) Photodynamic inactivation of the dermatophyte Trichophyton rubrum. Photochem. Photobiol. 77, 556 560.
16. Bliss, J. M., C. E. Bigelow, T. H. Foster C. G. Haidaris (2004) Susceptibility of Candida species to photodynamic effects of Photofrin. Antimicrob. Agents Chemother. 48, 2000 2006.
17. Chabrier-Rosellò, Y., T. H. Foster, N. Perez-Nazario, S. Mitra C. G. Haidaris (2005) Sensitivity of Candida albicans germ tubes and biofilms to Photofrin-mediated phototoxicity. Antimicrob. Agents Chemother. 49, 1 8.
18. Bertoloni, G., E. Reddi, M. Gatta, C. Burlini G. Jori (1989) Factors influencing the haematoporphyrin-sensitized photoinactivation of Candida albicans. J. Gen. Microbiol. 135, 957 966.
19. Wilson, M. N. Mia (1993) Sensitisation of Candida albicans to killing by low-power laser light. J. Oral Pathol. Med. 22, 354 357.
20. Zeina, B., J. Greenman, W. M. Purcell B. Das (2001) Killing of cutaneous microbial species by photodynamic therapy. Br. J. Dermatol. 144, 274 278.
21. Lambrechts, S. A. G., M. C. G. Aalders J. Van Marle (2005) Mechanistic study of the photodynamic activation of Candida albicans by a cationic porphyrin. Antimicrob. Agents Chemother. 49, 2026 2034.
22. Teichert, M. C., J. W. Jones, M. N. Usacheva M. A. Biel (2002) Treatment of oral candidiasis with methylene blue-mediated photodynamic therapy in an immunodeficient murine model. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endodont. 93, 155 160.
23. Helmerhorst, E. J., C. Venuleo, A. Beri F. G. Oppenheim (2005) Candida glabrata is unusual with respect to its resistance to cationic antifungal agents. Yeast 22, 705 714.
24. Odds, F. C. (1993) Resistance of yeasts to azole-derivative antifungals. J. Antimicrob. Chemother. 31, 463 471.
25. Traven, A., J. M. Wong, D. Xu, M. Sopta C. J. Ingles (2001) Interorganellar communication. Altered nuclear gene expression profiles in a yeast mitochondrial DNA mutant. J. Biol. Chem. 276, 4020 4027.
26. Cheng, S., C. J. Clancy, K. T. Nguyen, W. Clapp M. H. Nguyen (2007) A Candida albicans petite mutant strain with uncoupled oxidative phosphorylation overexpresses MDR1 and has diminished susceptibility to fluconazole and voriconazole. Antimicrob. Agents Chemother. 51, 1855 1858.
27. Brun, S., C. Aubry, O. Lima, R. Filmon, T. Berges, D. Chabasse J. P. Bouchara (2003) Relationships between respiration and susceptibility to azole antifungals in Candida glabrata. Antimicrob. Agents Chemother. 47, 847 853.
28. Slonimski, P. P., G. Perrodin J. H. Croft (1968) Ethidium bromide induced mutation of yeast mitochondria: Complete transformation of cells into respiratory deficient non-chromosomal "petites". Biochem. Biophys. Res. Commun. 30, 232 239.
29. Gyurko, C., U. Lendenmann, R. F. Troxler F. G. Oppenheim (2000) Candida albicans mutants deficient in respiration are resistant to the small cationic salivary antimicrobial peptide histatin 5. Antimicrob. Agents Chemother. 44, 348 354.
30. Cheng, S., C. J. Clancy, Z. Zhang, B. Hao, W. Wang, K. A. Iczkowski, M. A. Pfaller M. H. Nguyen (2007) Uncoupling of oxidative phosphorylation enables Candida albicans to resist killing by phagocytes and persist in tissue. Cell. Microbiol. 9, 492 501.
31. Morrow, B., H. Ramsey D. R. Soll (1994) Regulation of phase-specific genes in the more general switching system of Candida albicans strain 3153A. J. Med. Vet. Mycol. 32, 287 294.
32. Vargas, K., P. W. Wertz, D. Drake, B. Morrow D. R. Soll (1994) Differences in adhesion of Candida albicans 3153A cells exhibiting switch phenotypes to buccal epithelium and stratum corneum. Infect. Immun. 62, 1328 1335.
33. Kurtz, M. B., M. W. Cortelyou D. R. Kirsch (1986) Integrative transformation of Candida albicans, using a cloned Candida ADE2 gene. Mol. Cell. Biol. 6, 142 149.
34. Rogers, P. D. K. S. Barker (2003) Genome-wide expression profile analysis reveals coordinately regulated genes associated with stepwise acquisition of azole resistance in Candida albicans clinical isolates. Antimicrob. Agents Chemother. 47, 1220 1227.
35. White, T. C., K. A. Marr R. A. Bowden (1998) Clinical, cellular, and molecular factors that contribute to antifungal drug resistance. Clin. Microbiol. Rev. 11, 382 402.
36. Chandra, J., D. M. Kuhn, P. K. Mukherjee, L. L. Hoyer, T. McCormick M. A. Ghannoum (2001) Biofilm formation by the fungal pathogen Candida albicans: Development, architecture, and drug resistance. J. Bacteriol. 183, 5385 5394.
37. Meshulam, T., S. M. Levitz, L. Christin R. D. Diamond (1995) A simplified new assay for assessment of fungal cell damage with the tetrazolium dye, (2,3)-bis-(2-methoxy-4-nitro-5-sulphenyl)-(2H)-tetrazolium-5-carboxanilide (XTT). J. Infect. Dis. 172, 1153 1156.
38. NCCLS 2002) Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts; Approved Standard-Second Edition. NCCLS Document M27-A2, NCCLS, Wayne, PA.
39. Jori, G. (2006) Photodynamic therapy of microbial infections: State of the art and perspectives. J. Environ. Pathol. Toxicol. Oncol. 25, 505 519.
40. Reddi, E., M. Ceccon, G. Valduga, G. Jori, J. C. Bommer, F. Elisei, L. Latterini U. Mazzucato (2002) Photophysical properties and antibacterial activity of meso-substituted cationic porphyrins. Photochem. Photobiol. 75, 462 470.
41. Brun, S., T. Berges, P. Poupard, C. Vauzelle-Moreau, G. Renier, D. Chabasse J. P. Bouchara (2004) Mechanisms of azole resistance in petite mutants of Candida glabrata. Antimicrob. Agents Chemother. 48, 1788 1796.
42. Pfaller, M. A., S. A. Messer, R. J. Hollis, R. N. Jones D. J. Diekema (2002) In vitro activities of ravuconazole and voriconazole compared with those of four approved systemic antifungal agents against 6,970 clinical isolates of Candida spp. Antimicrob. Agents Chemother. 46, 1723 1727.
43. Kaur, R., I. Castano B. P. Cormack (2004) Functional genomic analysis of fluconazole susceptibility in the pathogenic yeast Candida glabrata: Roles of calcium signaling and mitochondria. Antimicrob. Agents Chemother. 48, 1600 1613.
44. Bouchara, J. P., R. Zouhair, S. Le Boudouil, G. Renier, R. Filmon, D. Chabasse, J. N. Hallet A. Defontaine (2000) In-vivo selection of an azole-resistant petite mutant of Candida glabrata. J. Med. Microbiol. 49, 977 984.
45. Tsai, H. F., A. A. Krol, K. E. Sarti J. E. Bennett (2006) Candida glabrata PDR1, a transcriptional regulator of a pleiotropic drug resistance network, mediates azole resistance in clinical isolates and petite mutants. Antimicrob. Agents Chemother. 50, 1384 1392.
46. Helmerhorst, E. J., C. Venuleo, D. Sanglard F. G. Oppenheim (2006) Roles of cellular respiration, CgCDR1, and CgCDR2 in Candida glabrata resistance to histatin 5. Antimicrob. Agents Chemother. 50, 1100 1103.
47. Vermitsky, J. P., K. D. Earhart, W. L. Smith, R. Homayouni, T. D. Edlind P. D. Rogers (2006) Pdr1 regulates multidrug resistance in Candida glabrata: Gene disruption and genome-wide expression studies. Mol. Microbiol. 61, 704 722.
48. Akins, R. A. (2005) An update on antifungal targets and mechanisms of resistance in Candida albicans. Med. Mycol. 43, 285 318.
49. Kohli, A., Smriti, K. Mukhopadhyay, A. Rattan R. Prasad (2002) In vitro low-level resistance to azoles in Candida albicans is associated with changes in membrane lipid fluidity and asymmetry. Antimicrob. Agents Chemother. 46, 1046 1052.
50. Kan, V. L., A. Geber J. E. Bennett (1996) Enhanced oxidative killing of azole-resistant Candida glabrata strains with ERG11 deletion. Antimicrob. Agents Chemother. 40, 1717 1719.
51. Kobayashi, D., K. Kondo, N. Uehara, S. Otokozawa, N. Tsuji, A. Yagihashi N. Watanabe (2002) Endogenous reactive oxygen species is an important mediator of miconazole antifungal effect. Antimicrob. Agents Chemother. 46, 3113 3117.
52. Evans, I. H., E. S. Diala, A. Earl D. Wilkie (1980) Mitochondrial control of cell surface characteristics in Saccharomyces cerevisiae. Biochim. Biophys. Acta 602, 201 206.
53. Lussier, M., A. M. White, J. Sheraton, T. di Paolo, J. Treadwell, S. B. Southard, C. I. Horenstein, J. Chen-Weiner, A. F. Ram, J. C. Kapteyn, T. W. Roemer, D. H. Vo, D. C. Bondoc, J. Hall, W. W. Zhong, A. M. Sdicu, J. Davies, F. M. Klis, P. W. Robbins H. Bussey (1997) Large scale identification of genes involved in cell surface biosynthesis and architecture in Saccharomyces cerevisiae. Genetics 147, 435 450.
54. Brun, S., F. Dalle, P. Saulnier, G. Renier, A. Bonnin, D. Chabasse J. P. Bouchara (2005) Biological consequences of petite mutations in Candida glabrata. J. Antimicrob. Chemother. 56, 307 314.
55. Wauters, T., D. Iserentant H. Verachtert (2001) Sensitivity of Saccharomyces cerevisiae to tannic acid is due to iron deprivation. Can. J. Microbiol. 47, 290 293.
56. Perrone, G. G., C. M. Grant I. W. Dawes (2005) Genetic and environmental factors influencing glutathione homeostasis in Saccharomyces cerevisiae. Mol. Biol. Cell 16, 218 230.
57. Kontoyiannis, D. P. (2000) Modulation of fluconazole sensitivity by the interaction of mitochondria and erg3p in Saccharomyces cerevisiae. J. Antimicrob. Chemother. 46, 191 197.
58. Zhong, Q. M. L. Greenberg (2005) Deficiency in mitochondrial anionic phospholipid synthesis impairs cell wall biogenesis. Biochem. Soc. Trans. 33, 1158 1161.
59. Ouedraogo, G. D. R. W. Redmond (2003) Secondary reactive oxygen species extend the range of photosensitization effects in cells: DNA damage produced via initial membrane photosensitization. Photochem. Photobiol. 77, 192 203.
60. Gralla, E. B. D. J. Kosman (1992) Molecular genetics of superoxide dismutases in yeasts and related fungi. Adv. Genet. 30, 251 319.
61. Chauhan, N., J. P. Latge R. Calderone (2006) Signalling and oxidant adaptation in Candida albicans and Aspergillus fumigatus. Nat. Rev. Microbiol. 4, 435 444.
62. Moradas-Ferreira, P., V. Costa, P. Piper W. Mager (1996) The molecular defences against reactive oxygen species in yeast. Mol. Microbiol. 19, 651 658.
63. Temple, M. D., G. G. Perrone I. W. Dawes (2005) Complex cellular responses to reactive oxygen species. Trends Cell Biol. 15, 319 326.
64. Thorpe, G. W., C. S. Fong, N. Alic, V. J. Higgins I. W. Dawes (2004) Cells have distinct mechanisms to maintain protection against different reactive oxygen species: Oxidative-stress-response genes. Proc. Natl Acad. Sci. USA 101, 6564 6569.