Fitness Trade-offs Restrict the Evolution of Resistance to Amphotericin B

PLoS Biology

Volumn 11, Issue 10, 2013, Pages

  Vincent, Benjamin Matteson ^a,b   Lancaster, Alex Kelvin ^b,c   Scherz Shouval, Ruth ^b   Whitesell, Luke ^b   Lindquist, Susan ^a,b  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHOTERICIN B; HEAT SHOCK PROTEIN 90;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIFUNGAL RESISTANCE; ARTICLE; CANDIDA ALBICANS; CANDIDIASIS; CELL KILLING; CONTROLLED STUDY; ERG11 GENE; ERG2 GENE; ERG3 GENE; ERG6 GENE; FEVER; FUNGAL GENE; FUNGAL STRAIN; FUNGAL VIRULENCE; GENOME ANALYSIS; IN VITRO STUDY; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; OXIDATIVE STRESS; PHENOTYPIC VARIATION; SEQUENCE ANALYSIS;

AMPHOTERICIN B; ANIMALS; BIOLOGICAL EVOLUTION; CANDIDA ALBICANS; CANDIDIASIS; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, FUNGAL; ERGOSTEROL; FUNGAL PROTEINS; GENETIC FITNESS; HOST-PATHOGEN INTERACTIONS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; MICE; MICROBIAL SENSITIVITY TESTS; MICROBIAL VIABILITY; MUTATION; REPRODUCIBILITY OF RESULTS; STRESS, PHYSIOLOGICAL; VIRULENCE;

EID: 84886633433     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001692     Document Type: Article

References (61)

1. Tibayrenc M, Ayala FJ, (2012) Reproductive clonality of pathogens: a perspective on pathogenic viruses, bacteria, fungi, and parasitic protozoa. Proc Natl Acad Sci U S A 109: E3305-3313.
2. Xu J, Ramos AR, Vilgalys R, Mitchell TG, (2000) Clonal and spontaneous origins of fluconazole resistance in Candida albicans. J Clin Microbiol 38: 1214-1220.
3. Brown GD, Denning DW, Gow NA, Levitz SM, Netea MG, et al. (2012) Hidden killers: human fungal infections. Sci Transl Med 4: 165rv113.
4. Pfaller M, Neofytos D, Diekema D, Azie N, Meier-Kriesche HU, et al. (2012) Epidemiology and outcomes of candidemia in 3648 patients: data from the Prospective Antifungal Therapy (PATH Alliance(R)) registry, 2004-2008. Diagn Microbiol Infect Dis 74: 323-331.
5. Odds FC, Brown AJ, Gow NA, (2003) Antifungal agents: mechanisms of action. Trends Microbiol 11: 272-279.
6. Gallis HA, Drew RH, Pickard WW, (1990) Amphotericin B: 30 years of clinical experience. Rev Infect Dis 12: 308-329.
7. Brajtburg J, Powderly WG, Kobayashi GS, Medoff G, (1990) Amphotericin B: current understanding of mechanisms of action. Antimicrob Agents Chemother 34: 183-188.
8. 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: 2234-2239.
9. Paterson PJ, Seaton S, Prentice HG, Kibbler CC, (2003) Treatment failure in invasive aspergillosis: susceptibility of deep tissue isolates following treatment with amphotericin B. J Antimicrob Chemother 52: 873-876.
10. Vermes A, Guchelaar HJ, Dankert J, (2000) Flucytosine: a review of its pharmacology, clinical indications, pharmacokinetics, toxicity and drug interactions. J Antimicrob Chemother 46: 171-179.
11. Pfaller MA, Espinel-Ingroff A, Canton E, Castanheira M, Cuenca-Estrella M, et al. (2012) Wild-type MIC distributions and epidemiological cutoff values for amphotericin B, flucytosine, and itraconazole and Candida spp. as determined by CLSI broth microdilution. J Clin Microbiol 50: 2040-2046.
12. Mora-Duarte J, Betts R, Rotstein C, Colombo AL, Thompson-Moya L, et al. (2002) Comparison of caspofungin and amphotericin B for invasive candidiasis. N Engl J Med 347: 2020-2029.
13. Garcia-Effron G, Kontoyiannis DP, Lewis RE, Perlin DS, (2008) Caspofungin-resistant Candida tropicalis strains causing breakthrough fungemia in patients at high risk for hematologic malignancies. Antimicrob Agents Chemother 52: 4181-4183.
14. 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.
15. Pfeiffer CD, Garcia-Effron G, Zaas AK, Perfect JR, Perlin DS, et al. (2010) Breakthrough invasive candidiasis in patients on micafungin. J Clin Microbiol 48: 2373-2380.
16. Sanglard D, Odds FC, (2002) Resistance of Candida species to antifungal agents: molecular mechanisms and clinical consequences. Lancet Infect Dis 2: 73-85.
17. Walker LA, Gow NA, Munro CA, (2010) Fungal echinocandin resistance. Fungal Genet Biol 47: 117-126.
18. White TC, Marr KA, Bowden RA, (1998) Clinical, cellular, and molecular factors that contribute to antifungal drug resistance. Clin Microbiol Rev 11: 382-402.
19. Kelly SL, Lamb DC, Kelly DE, Manning NJ, Loeffler J, et al. (1997) Resistance to fluconazole and cross-resistance to amphotericin B in Candida albicans from AIDS patients caused by defective sterol delta5,6-desaturation. FEBS Lett 400: 80-82.
20. Martel CM, Parker JE, Bader O, Weig M, Gross U, et al. (2010) A clinical isolate of Candida albicans with mutations in ERG11 (encoding sterol 14alpha-demethylase) and ERG5 (encoding C22 desaturase) is cross resistant to azoles and amphotericin B. Antimicrob Agents Chemother 54: 3578-3583.
21. Sanglard D, Ischer F, Parkinson T, Falconer D, Bille J, (2003) Candida albicans mutations in the ergosterol biosynthetic pathway and resistance to several antifungal agents. Antimicrob Agents Chemother 47: 2404-2412.
22. Hull CM, Bader O, Parker JE, Weig M, Gross U, et al. (2012) Two clinical isolates of Candida glabrata exhibiting reduced sensitivity to amphotericin B both harbor mutations in ERG2. Antimicrob Agents Chemother 56: 6417-6421.
23. Vandeputte P, Tronchin G, Larcher G, Ernoult E, Berges T, et al. (2008) A nonsense mutation in the ERG6 gene leads to reduced susceptibility to polyenes in a clinical isolate of Candida glabrata. Antimicrob Agents Chemother 52: 3701-3709.
24. Young LY, Hull CM, Heitman J, (2003) Disruption of ergosterol biosynthesis confers resistance to amphotericin B in Candida lusitaniae. Antimicrob Agents Chemother 47: 2717-2724.
25. Cowen LE, Lindquist S, (2005) Hsp90 potentiates the rapid evolution of new traits: drug resistance in diverse fungi. Science 309: 2185-2189.
26. Borkovich KA, Farrelly FW, Finkelstein DB, Taulien J, Lindquist S, (1989) hsp82 is an essential protein that is required in higher concentrations for growth of cells at higher temperatures. Mol Cell Biol 9: 3919-3930.
27. Jarosz DF, Lindquist S, (2010) Hsp90 and environmental stress transform the adaptive value of natural genetic variation. Science 330: 1820-1824.
28. Whitesell L, Santagata S, Lin NU, (2012) Inhibiting HSP90 to treat cancer: a strategy in evolution. Curr Mol Med 12: 1108-1124.
29. Cowen LE, Singh SD, Kohler JR, Collins C, Zaas AK, et al. (2009) Harnessing Hsp90 function as a powerful, broadly effective therapeutic strategy for fungal infectious disease. Proc Natl Acad Sci U S A 106: 2818-2823.
30. Singh SD, Robbins N, Zaas AK, Schell WA, Perfect JR, et al. (2009) Hsp90 governs echinocandin resistance in the pathogenic yeast Candida albicans via calcineurin. PLoS Pathog 5: e1000532 doi:10.1371/journal.ppat.1000532.
31. LaFayette SL, Collins C, Zaas AK, Schell WA, Betancourt-Quiroz M, et al. (2010) PKC signaling regulates drug resistance of the fungal pathogen Candida albicans via circuitry comprised of Mkc1, calcineurin, and Hsp90. PLoS Pathog 6: e1001069 doi: 10.1371/journal.ppat.1001069.
32. Taipale M, Krykbaeva I, Koeva M, Kayatekin C, Westover KD, et al. (2012) Quantitative analysis of HSP90-client interactions reveals principles of substrate recognition. Cell 150: 987-1001.
33. Karababa M, Valentino E, Pardini G, Coste AT, Bille J, et al. (2006) CRZ1, a target of the calcineurin pathway in Candida albicans. Mol Microbiol 59: 1429-1451.
34. Jia Y, Tang RJ, Wang L, Zhang X, Wang Y, et al. (2012) Calcium-activated-calcineurin reduces the In vitro and In vivo sensitivity of fluconazole to Candida albicans via Rta2p. PLoS One 7: e48369 doi: 10.1371/journal.pone.0048369.
35. Diezmann S, Michaut M, Shapiro RS, Bader GD, Cowen LE, (2012) Mapping the Hsp90 genetic interaction network in Candida albicans reveals environmental contingency and rewired circuitry. PLoS Genet 8: e1002562 doi:10.1371/journal.pgen.1002562.
36. Sussman A, Huss K, Chio LC, Heidler S, Shaw M, et al. (2004) Discovery of cercosporamide, a known antifungal natural product, as a selective Pkc1 kinase inhibitor through high-throughput screening. Eukaryot Cell 3: 932-943.
37. Arana DM, Alonso-Monge R, Du C, Calderone R, Pla J, (2007) Differential susceptibility of mitogen-activated protein kinase pathway mutants to oxidative-mediated killing by phagocytes in the fungal pathogen Candida albicans. Cell Microbiol 9: 1647-1659.
38. Miramon P, Dunker C, Windecker H, Bohovych IM, Brown AJ, et al. (2012) Cellular responses of Candida albicans to phagocytosis and the extracellular activities of neutrophils are critical to counteract carbohydrate starvation, oxidative and nitrosative stress. PLoS One 7: e52850 doi:10.1371/journal.pone.0052850.
39. Lo HJ, Kohler JR, DiDomenico B, Loebenberg D, Cacciapuoti A, et al. (1997) Nonfilamentous C. albicans mutants are avirulent. Cell 90: 939-949.
40. Mitchell AP, (1998) Dimorphism and virulence in Candida albicans. Curr Opin Microbiol 1: 687-692.
41. Miyazaki T, Miyazaki Y, Izumikawa K, Kakeya H, Miyakoshi S, et al. (2006) Fluconazole treatment is effective against a Candida albicans erg3/erg3 mutant in vivo despite in vitro resistance. Antimicrob Agents Chemother 50: 580-586.
42. Chau AS, Gurnani M, Hawkinson R, Laverdiere M, Cacciapuoti A, et al. (2005) Inactivation of sterol Delta5,6-desaturase attenuates virulence in Candida albicans. Antimicrob Agents Chemother 49: 3646-3651.
43. Vale-Silva LA, Coste AT, Ischer F, Parker JE, Kelly SL, et al. (2012) Azole resistance by loss of function of the sterol Delta(5),(6)-desaturase gene (ERG3) in Candida albicans does not necessarily decrease virulence. Antimicrob Agents Chemother 56: 1960-1968.
44. Park BJ, Arthington-Skaggs BA, Hajjeh RA, Iqbal N, Ciblak MA, et al. (2006) Evaluation of amphotericin B interpretive breakpoints for Candida bloodstream isolates by correlation with therapeutic outcome. Antimicrob Agents Chemother 50: 1287-1292.
45. Rex JH, Pfaller MA, Barry AL, Nelson PW, Webb CD, (1995) Antifungal susceptibility testing of isolates from a randomized, multicenter trial of fluconazole versus amphotericin B as treatment of nonneutropenic patients with candidemia. NIAID Mycoses Study Group and the Candidemia Study Group. Antimicrob Agents Chemother 39: 40-44.
46. Read AF, Lynch PA, Thomas MB, (2009) How to make evolution-proof insecticides for malaria control. PLoS Biol 7: e1000058 doi:10.1371/journal.pbio.1000058.
47. Altman MD, Ali A, Reddy GS, Nalam MN, Anjum SG, et al. (2008) HIV-1 protease inhibitors from inverse design in the substrate envelope exhibit subnanomolar binding to drug-resistant variants. J Am Chem Soc 130: 6099-6113.
48. Li XZ, Nikaido H, (2009) Efflux-mediated drug resistance in bacteria: an update. Drugs 69: 1555-1623.
49. Nakashima R, Sakurai K, Yamasaki S, Nishino K, Yamaguchi A, (2011) Structures of the multidrug exporter AcrB reveal a proximal multisite drug-binding pocket. Nature 480: 565-569.
50. Zhou T, Commodore L, Huang WS, Wang Y, Thomas M, et al. (2011) Structural mechanism of the Pan-BCR-ABL inhibitor ponatinib (AP24534): lessons for overcoming kinase inhibitor resistance. Chem Biol Drug Des 77: 1-11.
51. Li H, Durbin R, (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
52. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, et al. (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43: 491-498.
53. Thorvaldsdottir H, Robinson JT, Mesirov JP, (2012) Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform.
54. Fields Development Team (2006). fields: Tools for Spatial Data. National Center for Atmospheric Research, Boulder, CO. http://www.image.ucar.edu/GSP/Software/Fields/index.shtml.
55. Arthington-Skaggs BA, Warnock DW, Morrison CJ, (2000) Quantitation of Candida albicans ergosterol content improves the correlation between in vitro antifungal susceptibility test results and in vivo outcome after fluconazole treatment in a murine model of invasive candidiasis. Antimicrob Agents Chemother 44: 2081-2085.
56. Noble SM, Johnson AD, (2005) Strains and strategies for large-scale gene deletion studies of the diploid human fungal pathogen Candida albicans. Eukaryot Cell 4: 298-309.
57. Blankenship JR, Wormley FL, Boyce MK, Schell WA, Filler SG, et al. (2003) Calcineurin is essential for Candida albicans survival in serum and virulence. Eukaryot Cell 2: 422-430.
58. Nauseef WM, (2007) Isolation of human neutrophils from venous blood. Methods Mol Biol 412: 15-20.
59. Ermert D, Niemiec MJ, Rohm M, Glenthoj A, Borregaard N, et al. (2013) Candida albicans escapes from mouse neutrophils. J Leukoc Biol 94: 223-236.
60. Uppuluri P, Chaturvedi AK, Srinivasan A, Banerjee M, Ramasubramaniam AK, et al. (2010) Dispersion as an important step in the Candida albicans biofilm developmental cycle. PLoS Pathog 6: e1000828 doi: 10.1371/journal.ppat.1000828.
61. White TC, (1997) Increased mRNA levels of ERG16, CDR, and MDR1 correlate with increases in azole resistance in Candida albicans isolates from a patient infected with human immunodeficiency virus. Antimicrob Agents Chemother 41: 1482-1487.