Role of Ess1 in Growth, Morphogenetic Switching, and RNA Polymerase II Transcription in Candida albicans

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Samaranayake, Dhanushki ^a,b   Atencio, David ^c   Morse, Randall ^a,b   Wade, Joseph T ^a,b   Chaturvedi, Vishnu ^a,b   Hanes, Steven D ^a,b,c  

^a STATE UNIVERSITY OF NEW YORK   (United States)

^b WADSWORTH CENTER   (United States)

^c State University of New York Upstate Medical University: College of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PEPTIDYLPROLYL ISOMERASE PIN1; RNA POLYMERASE II; TRANSCRIPTOME;

ALLELE; ALPHA HELIX; ARTICLE; CANDIDA ALBICANS; CONTROLLED STUDY; ENZYME REGULATION; ESS1 GENE; FUNGAL GENE; FUNGAL STRAIN; FUNGUS GROWTH; GENE DOSAGE; GENE SWITCHING; GENETIC ASSOCIATION; MARKER GENE; MUTATIONAL ANALYSIS; NONHUMAN; PHENOTYPIC VARIATION; PROTEIN FUNCTION; RNA SEQUENCE; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; TRANSCRIPTION INITIATION; TRANSCRIPTION TERMINATION;

CANDIDA ALBICANS; PEPTIDYLPROLYL ISOMERASE; RNA POLYMERASE II;

EID: 84875012997     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0059094     Document Type: Article

References (88)

1. Schmid J, Tortorano AM, Jones G, Lazzarini C, Zhang N, et al. (2011) Increased mortality in young candidemia patients associated with presence of a Candida albicans general-purpose genotype. J Clinical Microbiol 49: 3250-3256.
2. Mean M, Marchetti O, Calandra T, (2008) Bench-to-bedside review: Candida infections in the intensive care unit. Critical Care 12: 204.
3. Pfaller MA, Messer SA, Moet GJ, Jones RN, Castanheira M, (2011) Candida bloodstream infections: comparison of species distribution and resistance to echinocandin and azole antifungal agents in Intensive Care Unit (ICU) and non-ICU settings in the SENTRY Antimicrobial Surveillance Program. 2008-2009Intern J Antimicrobial Agents 38: 65-69.
4. Yang YL, Leaw SN, Wang AH, Chen HT, Cheng WT, et al. (2011) Characterization of yeasts colonizing in healthy individuals. Medical Mycology 49: 103-106.
5. Gow NA, van de Veerdonk FL, Brown AJ, Netea MG, (2012) Candida albicans morphogenesis and host defence: discriminating invasion from colonization. Nat Rev Microbiol 10: 112-122.
6. Odds FC, (1994) Candida albicans, the life and times of a pathogenic yeast. J Med Vet Mycol 32 Suppl 1: 1-8.
7. Odds FC, (1994) Pathogenesis of Candida infections. J Am Acad Derm 31: S2-5.
8. Mavor AL, Thewes S, Hube B, (2005) Systemic fungal infections caused by Candida species: epidemiology, infection process and virulence attributes. Current Drug Targets 6: 863-874.
9. De Rosa FG, Garazzino S, Pasero D, Di Perri G, Ranieri VM, (2009) Invasive candidiasis and candidemia: new guidelines. Minerva Anestesiologica 75: 453-458.
10. Lai CC, Tan CK, Huang YT, Shao PL, Hsueh PR, (2008) Current challenges in the management of invasive fungal infections. J Infect Chemo 14: 77-85.
11. Schelenz S, Abdallah S, Gray G, Stubbings H, Gow I, et al. (2011) Epidemiology of oral yeast colonization and infection in patients with hematological malignancies, head neck and solid tumors. J Oral Path Med 40: 83-89.
12. Epstein JB, Hancock PJ, Nantel S, (2003) Oral candidiasis in hematopoietic cell transplantation patients: an outcome-based analysis. Oral Surg Med Path Rad Endo 96: 154-163.
13. Muller FM, Groll AH, Walsh TJ, (1999) Current approaches to diagnosis and treatment of fungal infections in children infected with human immuno deficiency virus. Eur J Pediatrics 158: 187-199.
14. Fridkin SK, Kaufman D, Edwards JR, Shetty S, Horan T, (2006) Changing incidence of Candida bloodstream infections among NICU patients in the United States. 1995-2004Pediatrics 117: 1680-1687.
15. Cassone A, Cauda R, (2012) Candida and candidiasis in HIV-infected patients: where commensalism, opportunistic behavior and frank pathogenicity lose their borders. AIDS 26: 1457-1472.
16. Jain A, Jain S, Rawat S, (2010) Emerging fungal infections among children: A review on its clinical manifestations, diagnosis, and prevention. J Pharm Bioallied Sci 2: 314-320.
17. Casalinuovo IA, Di Francesco P, Garaci E, (2004) Fluconazole resistance in Candida albicans: a review of mechanisms. Eur Rev Med Pharmacol Sci 8: 69-77.
18. Cannon RD, Lamping E, Holmes AR, Niimi K, Tanabe K, et al. (2007) Candida albicans drug resistance another way to cope with stress. Microbiology 153: 3211-3217.
19. Pitman SK, Drew RH, Perfect JR, (2011) Addressing current medical needs in invasive fungal infection prevention and treatment with new antifungal agents, strategies and formulations. Expert Opin Emerging Drugs. Epub Aug 17.
20. Huang M, Kao KC, (2012) May 21 Population dynamics and the evolution of antifungal drug resistance in Candida albicans. FEMS Micro Let epub.
21. Pfaller MA, Moet GJ, Messer SA, Jones RN, Castanheira M, (2011) Candida bloodstream infections: comparison of species distributions and antifungal resistance patterns in community-onset and nosocomial isolates in the SENTRY Antimicrobial Surveillance Program. 2008-2009Antimicrobial Agents Chemo 55: 561-566.
22. Vazquez JA, (2003) Combination antifungal therapy against Candida species: the new frontier-are we there yet? Medical Mycology 41: 355-368.
23. Kontoyiannis DP, Lewis RE, (2004) Toward more effective antifungal therapy: the prospects of combination therapy. British J Haematol 126: 165-175.
24. Agarwal AK, Tripathi SK, Xu T, Jacob MR, Li XC, et al. (2012) Exploring the molecular basis of antifungal synergies using genome-wide approaches. Frontiers Micro 3: 115.
25. Garbati MA, Alasmari FA, Al-Tannir MA, Tleyjeh IM, (2012) The role of combination antifungal therapy in the treatment of invasive aspergillosis: a systematic review. International J Infect Diseases 16: e76-81.
26. Del Pozo JL, Frances ML, Hernaez S, Serrera A, Alonso M, et al. (2011) Effect of amphotericin B alone or in combination with rifampicin or clarithromycin against Candida species biofilms. Intern J Artificial Organs 34: 766-770.
27. Mahboubi M, Ghazian Bidgoli F, (2010) In vitro synergistic efficacy of combination of amphotericin B with Myrtus communis essential oil against clinical isolates of Candida albicans. Phytomedicine 17: 771-774.
28. Edlich F, Fischer G, (2006) Pharmacological targeting of catalyzed protein folding: the example of peptide bond cis/trans isomerases. Handbook of Exp Pharma pp. 359-404.
29. Bell A, Monaghan P, Page AP, (2006) Peptidyl-prolyl cis-trans isomerases (immunophilins) and their roles in parasite biochemistry, host-parasite interaction and antiparasitic drug action. Intern J Parasit 36: 261-276.
30. Schiene C, Fischer G, (2000) Enzymes that catalyse the restructuring of proteins. Curr Opin Struct Biol 10: 40-45.
31. Schiene-Fischer C, Aumuller T, Fischer G, (2012) May 20 Peptide Bond cis/trans Isomerases: A Biocatalysis Perspective of Conformational Dynamics in Proteins. Topics in Curr Chem [Epub ahead of print] PMID pp. 21598101.
32. Arevalo-Rodriguez M, Wu X, Hanes SD, Heitman J, (2004) Prolyl isomerases in yeast. Front Biosci 9: 2420-2446.
33. Derkx PM, Madrid SM, (2001) The Aspergillus niger cypA gene encodes a cyclophilin that mediates sensitivity to the immunosuppressant cyclosporin A. Mol Genet Genomics 266: 527-536.
34. Cruz MC, Goldstein AL, Blankenship J, Del Poeta M, Perfect JR, et al. (2001) Rapamycin and less immunosuppressive analogs are toxic to Candida albicans and Cryptococcus neoformans via FKBP12-dependent inhibition of TOR. Antimicrobial Agents and Chemo 45: 3162-3170.
35. Cruz MC, Cavallo LM, Gorlach JM, Cox G, Perfect JR, et al. (1999) Rapamycin antifungal action is mediated via conserved complexes with FKBP12 and TOR kinase homologs in Cryptococcus neoformans. Mol Cell Biol 19: 4101-4112.
36. Bastidas RJ, Reedy JL, Morales-Johansson H, Heitman J, Cardenas ME, (2008) Signaling cascades as drug targets in model and pathogenic fungi. Curr Opin Investig Drugs 9: 856-864.
37. Baumgrass R, Zhang Y, Erdmann F, Thiel A, Weiwad M, et al. (2004) Substitution in position 3 of cyclosporin A abolishes the cyclophilin-mediated gain-of-function mechanism but not immunosuppression. J Biol Chem 279: 2470-2479.
38. Singh N, Heitman J, (2004) Antifungal attributes of immunosuppressive agents: new paradigms in management and elucidating the pathophysiologic basis of opportunistic mycoses in organ transplant recipients. Transplantation 77: 795-800.
39. Hani J, Stumpf G, Domdey H, (1995) PTF1 encodes an essential protein in Saccharomyces cerevisiae, which shows strong homology with a new putative family of PPIases. FEBS Lett 365: 198-202.
40. Ranganathan R, Lu KP, Hunter T, Noel JP, (1997) Structural and functional analysis of the mitotic rotamase Pin1 suggests substrate recognition is phosphorylation dependent. Cell 89: 875-886.
41. Hanes SD, Shank PR, Bostian KA, (1989) Sequence and mutational analysis of ESS1, a gene essential for growth in Saccharomyces cerevisiae. Yeast 5: 55-72.
42. Wu X, Wilcox CB, Devasahayam G, Hackett RL, Arevalo-Rodriguez M, et al. (2000) The Ess1 prolyl isomerase is linked to chromatin remodeling complexes and the general transcription machinery. EMBO J 19: 3727-3738.
43. Singh N, Ma Z, Gemmill T, Wu X, Rossettini A, Rabeler C, Beane O, DeFiglio H, Palumbo M, Morse R, Hanes, S D, (2009) The Ess1 prolyl isomerase is required for transcription termination of small non-coding regulatory RNAs via the Nrd1 pathway. Mol Cell 36: 255-266.
44. Wilcox CB, Rossettini A, Hanes SD, (2004) Genetic interactions with C-terminal domain (CTD) kinases and the CTD of RNA Pol II suggest a role for Ess1 in transcription initiation and elongation in Saccharomyces cerevisiae. Genetics 167: 93-105.
45. Xu YX, Hirose Y, Zhou XZ, Lu KP, Manley JL, (2003) Pin1 modulates the structure and function of human RNA polymerase II. Genes Dev 17: 2765-2776.
46. Krishnamurthy S, Ghazy MA, Moore C, Hampsey M, (2009) Functional interaction of the Ess1 prolyl isomerase with components of the RNA polymerase II initiation and termination machineries. Mol Cell Biol 29: 2925-2934.
47. Gemmill TR, Wu X, Hanes SD, (2005) Vanishingly low levels of Ess1 prolyl-isomerase activity are sufficient for growth in Saccharomyces cerevisiae. J Biol Chem 280: 15510-15517.
48. Morris DP, Phatnani HP, Greenleaf AL, (1999) Phospho-carboxyl-terminal domain binding and the role of a prolyl isomerase in pre-mRNA 3′-End formation. J Biol Chem 274: 31583-31587.
49. Ma Z, Atencio D, Barnes C, DeFiglio H, Hanes SD, (2012) Multiple Roles for the Ess1 Prolyl Isomerase in the RNA Polymerase II Transcription Cycle. Mol Cell Biol 32: 3594-3607.
50. Li Z, Li H, Devasahayam G, Gemmill T, Chaturvedi V, et al. (2005) The structure of the Candida albicans Ess1 prolyl isomerase reveals a well-ordered linker that restricts domain mobility. Biochemistry 44: 6180-6189.
51. Verdecia MA, Bowman ME, Lu KP, Hunter T, Noel JP, (2000) Structural basis for phosphoserine-proline recognition by group IV WW domains. Nat Struct Biol 7: 639-643.
52. Devasahayam G, Chaturvedi V, Hanes SD, (2002) The Ess1 prolyl isomerase is required for growth and morphogenetic switching in Candida albicans. Genetics 160: 37-48.
53. Ren P, Rossettini A, Chaturvedi V, Hanes SD, (2005) The Ess1 prolyl isomerase is dispensable for growth but required for virulence in Cryptococcus neoformans. Microbiology 151: 1593-1605.
54. Joseph JD, Daigle SN, Means AR, (2004) PINA is essential for growth and positively influences NIMA function in Aspergillus nidulans. J Biol Chem 279: 32373-32384.
55. Fonzi WA, Irwin MY, (1993) Isogenic strain construction and gene mapping in Candida albicans. Genetics 134: 717-728.
56. Lay J, Henry LK, Clifford J, Koltin Y, Bulawa CE, et al. (1998) Altered expression of selectable marker URA3 in gene-disrupted Candida albicans strains complicates interpretation of virulence studies. Infect Immun 66: 5301-5306.
57. 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. Euk Cell 3: 900-909.
58. Magee PT, Gale C, Berman J, Davis D, (2003) Molecular genetic and genomic approaches to the study of medically important fungi. Infect Infect Immun 71: 2299-2309.
59. Jones T, Federspiel NA, Chibana H, Dungan J, Kalman S, et al. (2004) The diploid genome sequence of Candida albicans. Proc Natl Acad Sci USA 101: 7329-7334.
60. Sanchez AA, Johnston DA, Myers C, Edwards JE Jr, Mitchell AP, et al. (2004) Relationship between Candida albicans virulence during experimental hematogenously disseminated infection and endothelial cell damage in vitro. Infect Immun 72: 598-601.
61. Klinke T, Rump A, Ponisch R, Schellenberger W, Muller EC, et al. (2008) Identification and characterization of CaApe2-a neutral arginine/alanine/leucine-specific metallo-aminopeptidase from Candida albicans. FEMS Yeast Res 8: 858-869.
62. Noble SM, Johnson AD, (2005) Strains and strategies for large-scale gene deletion studies of the diploid human fungal pathogen Candida albicans. Euk Cell 4: 298-309.
63. Moreno I, Martinez-Esparza M, Laforet LC, Sentandreu R, Ernst JF, et al. (2010) Dosage-dependent roles of the Cwt1 transcription factor for cell wall architecture, morphogenesis, drug sensitivity and virulence in Candida albicans. Yeast 27: 77-87.
64. Porta A, Ramon AM, Fonzi WA, (1999) PRR1, a homolog of Aspergillus nidulans palF, controls pH-dependent gene expression and filamentation in Candida albicans. J Bact 181: 7516-7523.
65. McNaughton L, Li Z, Van Roey P, Hanes SD, LeMaster DM, (2010) Restricted domain mobility in the Candida albicans Ess1 prolyl isomerase. Biochimica et biophysica acta 1804: 1537-1541.
66. Lu KP, Hanes SD, Hunter T, (1996) A human peptidyl-prolyl isomerase essential for regulation of mitosis. Nature 380: 544-547.
67. Mitrovich QM, Tuch BB, De La Vega FM, Guthrie C, Johnson AD, (2010) Evolution of yeast noncoding RNAs reveals an alternative mechanism for widespread intron loss. Science 330: 838-841.
68. Sellam A, Hogues H, Askew C, Tebbji F, van Het Hoog M, et al. (2010) Experimental annotation of the human pathogen Candida albicans coding and noncoding transcribed regions using high-resolution tiling arrays. Genome Biol 11: R71.
69. Schattner P, Decatur WA, Davis CA, Ares M Jr, Fournier MJ, et al. (2004) Genome-wide searching for pseudouridylation guide snoRNAs: analysis of the Saccharomyces cerevisiae genome. Nuc Acids Res 32: 4281-4296.
70. Lowe TM, Eddy SR, (1999) A computational screen for methylation guide snoRNAs in yeast. Science 283: 1168-1171.
71. Uhl MA, Biery M, Craig N, Johnson AD, (2003) Haploinsufficiency-based large-scale forward genetic analysis of filamentous growth in the diploid human fungal pathogen C. albicans. EMBO J 22: 2668-2678.
72. Cheng S, Nguyen MH, Zhang Z, Jia H, Handfield M, et al. (2003) Evaluation of the roles of four Candida albicans genes in virulence by using gene disruption strains that express URA3 from the native locus. Infec Imm 71: 6101-6103.
73. Sundstrom P, Cutler JE, Staab JF, (2002) Reevaluation of the role of HWP1 in systemic candidiasis by use of Candida albicans strains with selectable marker URA3 targeted to the ENO1 locus. Infec Imm 70: 3281-3283.
74. Sherman F, (1991) Getting started with Yeast, Ed Guthrie, C. and Fink, G. R. Meth in Enzymology 194: 1-21.
75. Wellington M, Rustchenko E, (2005) 5-Fluoro-orotic acid induces chromosome alterations in Candida albicans. Yeast 22: 57-70.
76. Ito H, Fukuda Y, Murata K, Kimura A, (1983) Transformation of intact yeast cells treated with alkali cations. J. Bact 153: 163-168.
77. Ramon AM, Fonzi WA, (2003) Diverged binding specificity of Rim101p, the Candida albicans ortholog of PacC. Eukaryotic Cell 2: 718-728.
78. Murad AM, Lee PR, Broadbent ID, Barelle CJ, Brown AJ, (2000) CIp10, an efficient and convenient integrating vector for Candida albicans. Yeast 16: 325-327.
79. Lloyd AT, Sharp PM, (1992) Evolution of codon usage patterns: the extent and nature of divergence between Candida albicans and Saccharomyces cerevisiae. Nuc Acids Res 20: 5289-5295.
80. Liu H, Kohler J, Fink GR, (1994) Suppression of hyphal formation in Candida albicans by mutation of a STE12 homolog. Science 266: 1723-1726.
81. Kadosh D, Johnson AD, (2005) Induction of the Candida albicans filamentous growth program by relief of transcriptional repression: a genome-wide analysis. Mol Biol Cell 16: 2903-2912.
82. Schmitt ME, Brown TA, Trumpower BL, (1990) A rapid and simple method for preparation of RNA from Saccharomyces cerevisiae. Nuc Acids Res 18: 3091-3092.
83. van het Hoog M, Rast TJ, Martchenko M, Grindle S, Dignard D, et al. (2007) Assembly of the Candida albicans genome into sixteen supercontigs aligned on the eight chromosomes. Genome Biol 8: R52.
84. Langmead B, Trapnell C, Pop M, Salzberg SL, (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
85. Trapnell C, Pachter L, Salzberg SL, (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 250: 1105-1111.
86. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079.
87. Yu C, Palumbo MJ, Lawrence CE, Morse RH, (2006) Contribution of the histone H3 and H4 amino termini to Gcn4p- and Gcn5p-mediated transcription in yeast. J Biol Chem 281: 9755-9764.
88. Sikorski RS, Hieter P, (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19-27.