Sphingolipid biosynthetic pathway genes FEN1 and SUR4 modulate amphotericin B resistance

Antimicrobial Agents and Chemotherapy

Volumn 58, Issue 4, 2014, Pages 2409-2414

  Sharma, Sushma ^a,b   Alfatah, Md ^a   Bari, Vinay K ^a   Rawal, Yashpal ^a   Paul, Sanjoy ^a,c   Ganesan, K ^a  

^a INSTITUTE OF MICROBIAL TECHNOLOGY   (India)

^b UMEÅ UNIVERSITY   (Sweden)

^c UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHOTERICIN B; PHYTOSPHINGOSINE; SPHINGOLIPID; THERMOZYMOCIDIN;

ANTIFUNGAL RESISTANCE; ANTIFUNGAL SUSCEPTIBILITY; ARTICLE; BIOSYNTHESIS; CANDIDA ALBICANS; CANDIDA GLABRATA; CLAVISPORA LUSITANIAE; CONTROLLED STUDY; DRUG POTENTIATION; FEN1 GENE; FUNGAL GENE; FUNGAL STRAIN; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; ORTHOLOGY; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; SUR4 GENE;

AMPHOTERICIN B; ANTIFUNGAL AGENTS; BIOSYNTHETIC PATHWAYS; FUNGAL PROTEINS; MICROBIAL SENSITIVITY TESTS; SACCHAROMYCES CEREVISIAE; SPHINGOLIPIDS;

EID: 84896987395     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02130-13     Document Type: Article

References (59)

1. Andes DR, Safdar N, Baddley JW, Playford G, Reboli AC, Rex JH, Sobel JD, Pappas PG, Kullberg BJ, Mycoses Study Group. 2012. Impact of treatment strategy on outcomes in patients with candidemia and other forms of invasive candidiasis: a patient-level quantitative review of randomized trials. Clin. Infect. Dis. 54:1110-1122. http://dx.doi.org/10.1093/cid/cis021.
2. Pfaller M, Neofytos D, Diekema D, Azie N, Meier-Kriesche HU, Quan SP, Horn D. 2012. Epidemiology and outcomes of candidemia in 3648 patients: data from the Prospective Antifungal Therapy (PATH Alliance) registry, 2004-2008. Diagn. Microbiol. Infect. Dis. 74:323-331. http://dx.doi.org/10.1016/j. diagmicrobio.2012.10.003.
3. Pfaller MA, Diekema DJ. 2007. Epidemiology of invasive candidiasis: a persistent public health problem. Clin. Microbiol. Rev. 20:133-163. http://dx.doi.org/10.1128/CMR.00029-06. (Pubitemid 46167771)
4. Warnock DW. 2007. Trends in the epidemiology of invasive fungal infections. Nihon Ishinkin Gakkai Zasshi 48:1-12. http://dx.doi.org/10.3314/ jjmm.48.1.
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(Suppl 6):S389-S393. http://dx.doi.org/10.1086/430923. (Pubitemid 41266739)
6. Pfaller MA, Diekema DJ. 2004. Rare and emerging opportunistic fungal pathogens: concern for resistance beyond Candida albicans and Aspergillus fumigatus. J. Clin. Microbiol. 42:4419-4431. http://dx.doi.org/10.1128/JCM.42. 10.4419-4431.2004. (Pubitemid 39362350)
7. Silva S, Negri M, Henriques M, Oliveira R, Williams DW, Azeredo J. 2012. Candida glabrata, Candida parapsilosis and Candida tropicalis: biology, epidemiology, pathogenicity and antifungal resistance. FEMS Microbiol. Rev. 36:288-305. http://dx.doi.org/10.1111/j.1574-6976.2011.00278.x.
8. Akins RA, Sobel JD. 2009. Antifungal targets, mechanisms of action, and resistance in Candida albicans, p 347-409. In Mayers DL (ed), Antimicrobial drug resistance. Humana Press, New York, NY.
9. Anderson JB. 2005. Evolution of antifungal-drug resistance: mechanisms and pathogen fitness. Nat. Rev. Microbiol. 3:547-556. http://dx.doi.org/10.1038/ nrmicro1179. (Pubitemid 40903878)
10. Shapiro RS, Robbins N, Cowen LE. 2011. Regulatory circuitry governing fungal development, drug resistance, and disease. Microbiol. Mol. Biol. Rev. 75:213-267. http://dx.doi.org/10.1128/MMBR.00045-10.
11. Shaughnessy EMO, Lyman CA, Walsh TJ. 2009. Amphotericin B: polyene resistance mechanisms, p 295-305. In Mayers DL (ed), Antimicrobial drug resistance. Humana Press, New York, NY.
12. Laniado-Laborin R, Cabrales-Vargas MN. 2009. Amphotericin B: side effects and toxicity. Rev. Iberoam. Micol. 26:223-227. http://dx.doi.org/10.1016/j. riam.2009.06.003.
13. Gray KC, Palacios DS, Dailey I, Endo MM, Uno BE, Wilcock BC, Burke MD. 2012. Amphotericin primarily kills yeast by simply binding ergosterol. Proc. Natl. Acad. Sci. U. S. A. 109:2234-2239. http://dx.doi.org/10.1073/pnas. 1117280109.
14. Hull CM, Bader O, Parker JE, Weig M, Gross U, Warrilow AG, Kelly DE, Kelly SL. 2012. Two clinical isolates of Candida glabrata exhibiting reduced sensitivity to amphotericin B both harbor mutations in ERG2. Antimicrob. Agents Chemother. 56:6417-6421. http://dx.doi.org/10.1128/AAC.01145-12.
15. Martel CM, Parker JE, Bader O, Weig M, Gross U, Warrilow AG, Kelly DE, Kelly SL. 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. http://dx.doi.org/10.1128/AAC.00303-10.
16. 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. http://dx.doi.org/10.1128/AAC.47.8.2404-2412.2003. (Pubitemid 36919437)
17. Vandeputte P, Tronchin G, Larcher G, Ernoult E, Berges T, Chabasse D, Bouchara JP. 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. http://dx.doi.org/10.1128/AAC.00423- 08.
18. 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. http://dx.doi.org/10.1128/AAC.47.9.2717-2724.2003. (Pubitemid 37040239)
19. Bagnat M, Chang A, Simons K. 2001. Plasma membrane proton ATPase Pma1p requires raft association for surface delivery in yeast. Mol. Biol. Cell 12:4129-4138. http://dx.doi.org/10.1091/mbc.12.12.4129. (Pubitemid 34001097)
20. Bagnat M, Keranen S, Shevchenko A, Simons K. 2000. Lipid rafts function in biosynthetic delivery of proteins to the cell surface in yeast. Proc. Natl. Acad. Sci. U. S. A. 97:3254-3259. http://dx.doi.org/10.1073/pnas.97.7.3254. (Pubitemid 30183288)
21. Ikonen E. 2001. Roles of lipid rafts in membrane transport. Curr. Opin. Cell Biol. 13:470-477. http://dx.doi.org/10.1016/S0955-0674(00)00238-6. (Pubitemid 32709771)
22. Simons K, Sampaio JL. 2011. Membrane organization and lipid rafts. Cold Spring Harb. Perspect. Biol. 3:a004697. http://dx.doi.org/10.1101/cshperspect. a004697.
23. Simons K, Ikonen E. 1997. Functional rafts in cell membranes. Nature 387:569-572. http://dx.doi.org/10.1038/42408. (Pubitemid 27248754)
24. Brown DA, London E. 1998. Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 14:111-136. http://dx.doi.org/10.1146/ annurev.cellbio.14.1.111. (Pubitemid 29001451)
25. Mukhopadhyay K, Prasad T, Saini P, Pucadyil TJ, Chattopadhyay A, Prasad R. 2004. Membrane sphingolipid-ergosterol interactions are important determinants of multidrug resistance in Candida albicans. Antimicrob. Agents Chemother. 48:1778-1787. http://dx.doi.org/10.1128/AAC.48.5.1778-1787.2004. (Pubitemid 38544389)
26. Pasrija R, Panwar SL, Prasad R. 2008. Multidrug transporters CaCdr1p and CaMdr1p of Candida albicans display different lipid specificities: both ergosterol and sphingolipids are essential for targeting of CaCdr1p to membrane rafts. Antimicrob. Agents Chemother. 52:694-704. http://dx.doi.org/10.1128/AAC. 00861-07. (Pubitemid 351170846)
27. Guan XL, Souza CM, Pichler H, Dewhurst G, Schaad O, Kajiwara K, Wakabayashi H, Ivanova T, Castillon GA, Piccolis M, Abe F, Loewith R, Funato K, Wenk MR, Riezman H. 2009. Functional interactions between sphingolipids and sterols in biological membranes regulating cell physiology. Mol. Biol. Cell 20:2083-2095. http://dx.doi.org/10.1091/mbc.E08-11-1126.
28. Breslow DK, Weissman JS. 2010. Membranes in balance: mechanisms of sphingolipid homeostasis. Mol. Cell 40:267-279. http://dx.doi.org/10.1016/j. molcel.2010.10.005.
29. Hannich JT, Umebayashi K, Riezman H. 2011. Distribution and functions of sterols and sphingolipids. Cold Spring Harb. Perspect. Biol. 3:pii a004762. http://dx.doi.org/10.1101/cshperspect.a004762.
30. Clinical and Laboratory Standards Institute. 2008. Reference method for broth dilution antifungal susceptibility testing of yeasts; approved standard - 3rd ed. CLSI document M27-A3. Clinical and Laboratory Standards Institute, Wayne, PA.
31. Giaever G, Chu AM, Ni L, Connelly C, Riles L, Veronneau S, Dow S, Lucau-Danila A, Anderson K, Andre B, Arkin AP, Astromoff A, El-Bakkoury M, Bangham R, Benito R, Brachat S, Campanaro S, Curtiss M, Davis K, Deutschbauer A, Entian KD, Flaherty P, Foury F, Garfinkel DJ, Gerstein M, Gotte D, Guldener U, Hegemann JH, Hempel S, Herman Z, Jaramillo DF, Kelly DE, Kelly SL, Kotter P, LaBonte D, Lamb DC, Lan N, Liang H, Liao H, Liu L, Luo C, Lussier M, Mao R, Menard P, Ooi SL, Revuelta JL, Roberts CJ, Rose M, Ross-Macdonald P, Scherens B, et al. 2002. Functional profiling of the Saccharomyces cerevisiae genome. Nature 418:387-391. http://dx.doi.org/10.1038/nature00935. (Pubitemid 34826834)
32. Han G, Gable K, Kohlwein SD, Beaudoin F, Napier JA, Dunn TM. 2002. The Saccharomyces cerevisiae YBR159w gene encodes the 3-ketoreductase of the microsomal fatty acid elongase. J. Biol. Chem. 277:35440-35449. http://dx.doi.org/10.1074/jbc.M205620200.
33. Obeid LM, Okamoto Y, Mao C. 2002. Yeast sphingolipids: metabolism and biology. Biochim. Biophys. Acta 1585:163-171. http://dx.doi.org/10.1016/S1388- 1981(02)00337-2. (Pubitemid 36092081)
34. Arthington-Skaggs BA, Jradi H, Desai T, Morrison CJ. 1999. Quantitation of ergosterol content: novel method for determination of fluconazole susceptibility of Candida albicans. J. Clin. Microbiol. 37:3332-3337. (Pubitemid 29455229)
35. Enloe B, Diamond A, Mitchell AP. 2000. A single-transformation gene function test in diploid Candida albicans. J. Bacteriol. 182:5730-5736. http://dx.doi.org/10.1128/JB.182.20.5730-5736.2000.
36. Brand A, MacCallum DM, Brown AJ, Gow NA, Odds FC. 2004. Ectopic expression of URA3 can influence the virulence phenotypes and proteome of Candida albicans but can be overcome by targeted reintegration of URA3 at the RPS10 locus. Eukaryot. Cell 3:900-909. http://dx.doi.org/10.1128/EC.3.4.900-909. 2004. (Pubitemid 39098866)
37. Lay J, Henry LK, Clifford J, Koltin Y, Bulawa CE, Becker JM. 1998. Altered expression of selectable marker URA3 in gene-disrupted Candida albicans strains complicates interpretation of virulence studies. Infect. Immun. 66:5301-5306. (Pubitemid 29044623)
38. Staab JF, Sundstrom P. 2003. URA3 as a selectable marker for disruption and virulence assessment of Candida albicans genes. Trends Microbiol. 11:69-73. http://dx.doi.org/10.1016/S0966-842X(02)00029-X. (Pubitemid 36207502)
39. Noble SM, Johnson AD. 2005. Strains and strategies for large-scale gene deletion studies of the diploidhumanfungalpathogen Candida albicans. Eukaryot. Cell 4:298-309. http://dx.doi.org/10.1128/EC.4.2.298-309.2005. (Pubitemid 40257130)
40. Carter Z, Delneri D. 2010. New generation of loxP-mutated deletion cassettes for the genetic manipulation of yeast natural isolates. Yeast 27:765-775. http://dx.doi.org/10.1002/yea.1774.
41. Dennison PMJ, Ramsdale M, Manson CL, Brown AJP. 2005. Gene disruption in Candida albicans using a synthetic, codon-optimised CreloxP system. Fungal Genet. Biol. 42:737-748. http://dx.doi.org/10.1016/j.fgb.2005.05.006. (Pubitemid 41188172)
42. Revardel E, Bonneau M, Durrens P, Aigle M. 1995. Characterization of a new gene family developing pleiotropic phenotypes upon mutation in Saccharomyces cerevisiae. Biochim. Biophys. Acta 1263:261-265. http://dx.doi.org/10.1016/ 0167-4781(95)00124-Y.
43. Dickson RC. 2008. New insights into sphingolipid metabolism and function in budding yeast. J. Lipid Res. 49:909-921. http://dx.doi.org/10.1194/jlr. R800003-JLR200.
44. Miyake Y, Kozutsumi Y, Nakamura S, Fujita T, Kawasaki T. 1995. Serine palmitoyltransferase is the primary target of a sphingosine-like immunosuppressant, ISP-1/myriocin. Biochem. Biophys. Res. Commun. 211:396-403. http://dx.doi.org/10.1006/bbrc.1995.1827.
45. Sun Y, Taniguchi R, Tanoue D, Yamaji T, Takematsu H, Mori K, Fujita T, Kawasaki T, Kozutsumi Y. 2000. Sli2 (Ypk1), a homologue of mammalian protein kinase SGK, is a downstream kinase in the sphingolipidmediated signaling pathway of yeast. Mol. Cell. Biol. 20:4411-4419. http://dx.doi.org/10.1128/MCB.20.12. 4411-4419.2000. (Pubitemid 30346635)
46. Oh CS, Toke DA, Mandala S, Martin CE. 1997. ELO2 and ELO3, homologues of the Saccharomyces cerevisiae ELO1 gene, function in fatty acid elongation and are required for sphingolipid formation. J. Biol. Chem. 272:17376-17384. http://dx.doi.org/10.1074/jbc.272.28.17376. (Pubitemid 27311164)
47. Denic V, Weissman JS. 2007. A molecular caliper mechanism for determining very long-chain fatty acid length. Cell 130:663-677. http://dx.doi.org/10.1016/ j.cell.2007.06.031. (Pubitemid 47268053)
48. Chung JH, Lester RL, Dickson RC. 2003. Sphingolipid requirement for generation of a functional v1 component of the vacuolar ATPase. J. Biol. Chem. 278:28872-28881. http://dx.doi.org/10.1074/jbc.M300943200. (Pubitemid 36935798)
49. David D, Sundarababu S, Gerst JE. 1998. Involvement of long chain fatty acid elongation in the trafficking of secretory vesicles in yeast. J. Cell Biol. 143:1167-1182. http://dx.doi.org/10.1083/jcb.143.5.1167. (Pubitemid 28559820)
50. Dickson RC, Lester RL. 1999. Metabolism and selected functions of sphingolipids in the yeast Saccharomyces cerevisiae. Biochim. Biophys. Acta 1438:305-321. http://dx.doi.org/10.1016/S1388-1981(99)00068-2. (Pubitemid 29301720)
51. Gaigg B, Toulmay A, Schneiter R. 2006. Very long-chain fatty acid-containing lipids rather than sphingolipids per se are required for raft association and stable surface transport of newly synthesized plasma membrane ATPase in yeast. J. Biol. Chem. 281:34135-34145. http://dx.doi.org/10.1074/jbc. M603791200. (Pubitemid 46036622)
52. Ejsing CS, Sampaio JL, Surendranath V, Duchoslav E, Ekroos K, Klemm RW, Simons K, Shevchenko A. 2009. Global analysis of the yeast lipidome by quantitative shotgun mass spectrometry. Proc. Natl. Acad. Sci. U. S. A. 106:2136-2141. http://dx.doi.org/10.1073/pnas.0811700106.
53. Klose C, Ejsing CS, Garcia-Saez AJ, Kaiser HJ, Sampaio JL, Surma MA, Shevchenko A, Schwille P, Simons K. 2010. Yeast lipids can phase-separate into micrometer-scale membrane domains. J. Biol. Chem. 285: 30224-30232. http://dx.doi.org/10.1074/jbc.M110.123554.
54. Ziolkowska NE, Christiano R, Walther TC. 2012. Organized living: formation mechanisms and functions of plasma membrane domains in yeast. Trends Cell Biol. 22:151-158. http://dx.doi.org/10.1016/j.tcb.2011.12.002.
55. Healey KR, Katiyar SK, Raj S, Edlind TD. 2012. CRS-MIS in Candida glabrata: sphingolipids modulate echinocandin-Fks interaction. Mol. Microbiol. 86:303-313. http://dx.doi.org/10.1111/j.1365-2958.2012.08194.x.
56. Winston F, Dollard C, Ricupero-Hovasse SL. 1995. Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C. Yeast 11:53-55. http://dx.doi.org/10.1002/yea.320110107.
57. Cormack BP, Ghori N, Falkow S. 1999. An adhesin of the yeast pathogen Candida glabrata mediating adherence to human epithelial cells. Science 285:578-582. http://dx.doi.org/10.1126/science.285.5427.578.
58. Young LY, Lorenz MC, Heitman J. 2000. A STE12 homolog is required for mating but dispensable for filamentation in Candida lusitaniae. Genetics 155:17-29. (Pubitemid 30257107)
59. Fonzi WA, Irwin MY. 1993. Isogenic strain construction and gene mapping in Candida albicans. Genetics 134:717-728. (Pubitemid 23193572)