Local and regional chromatin silencing in Candida glabrata: Consequences for adhesion and the response to stress

FEMS Yeast Research

Volumn 15, Issue 6, 2015, Pages

  De Las Peñas, Alejandro ^a   Juárez Cepeda, Jacqueline ^a   López Fuentes, Eunice ^a   Briones Martín del Campo, Marcela ^a   Gutiérrez Escobedo, Guadalupe ^a   Castaño, Irene ^a  

^a INSTITUTO POTOSINO DE INVESTIGACIÓN CIENTÍFICA Y TECNOLÓGICA   (Mexico)

Author keywords

Hst1; Sir2; Sirtuins; Subtelomeric region; Telomeres

Indexed keywords

ADHESIN; DNA BINDING PROTEIN; HISTONE DEACETYLASE; HST1 PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE; RAP1 PROTEIN; SIRTUIN 1; SIRTUIN 4; SUM1 PROTEIN; UNCLASSIFIED DRUG; XENOBIOTIC AGENT; YKU PROTEIN; CHROMATIN; FUNGAL PROTEIN;

ADHESION; BINDING AFFINITY; BINDING SITE; CANDIDA GLABRATA; CHROMATIN; COMPLEX FORMATION; DEACETYLATION; EPIGENETICS; FUNGAL GENE; FUNGAL VIRULENCE; GENE EXPRESSION REGULATION; GENE INTERACTION; GENE SILENCING; MOLECULAR RECOGNITION; NONHUMAN; OXIDATIVE STRESS; PROMOTER REGION; PROTEIN DOMAIN; REPRESSOR GENE; SHORT SURVEY; SIGNAL TRANSDUCTION; ANIMAL; CELL ADHESION; GENETIC EPIGENESIS; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PROTEIN PROTEIN INTERACTION;

ANIMALS; CANDIDA GLABRATA; CELL ADHESION; CHROMATIN; DNA-BINDING PROTEINS; EPIGENESIS, GENETIC; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; HISTONE DEACETYLASES; HOST-PATHOGEN INTERACTIONS; HUMANS; PROTEIN INTERACTION MAPS; STRESS, PHYSIOLOGICAL;

EID: 84949214078     PISSN: 15671356     EISSN: 15671364     Source Type: Journal    
DOI: 10.1093/femsyr/fov056     Document Type: Short Survey

References (65)

1. Briones-Martin-Del-Campo M, Orta-Zavalza E, Canas-Villamar I, et al. The superoxide dismutases of Candida glabrata protect against oxidative damage and are required for lysine biosynthesis, DNA integrity and chronological life survival. Microbiology 2015;161:300-10.
2. Brunke S, Hube B. Two unlike cousins: Candida albicans and C. glabrata infection strategies. Cell Microbiol 2013;15:701-8.
3. Buhler M, Gasser SM. Silent chromatin at the middle and ends: lessons from yeasts. EMBO J 2009;28:2149-61.
4. Butler G, RasmussenMD, LinMF, et al. Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 2009;459:657-62.
5. Castano I, Pan SJ, Zupancic M, et al. Telomere length control and transcriptional regulation of subtelomeric adhesins in Candida glabrata. Mol Microbiol 2005;55:1246-58.
6. Cockell MM, Perrod S, Gasser SM. Analysis of Sir2p domains required for rDNA and telomeric silencing in Saccharomyces cerevisiae. Genetics 2000;154:1069-83.
7. Cohn M, McEachern MJ, Blackburn EH. Telomeric sequence diversity within the genus Saccharomyces. Curr Genet 1998;33:83-91.
8. Cormack BP, Falkow S. Efficient homologous and illegitimate recombination in the opportunistic yeast pathogen Candida glabrata. Genetics 1999;151:979-87.
9. Cormack BP, Ghori N, Falkow S. An adhesin of the yeast pathogen Candida glabrata mediating adherence to human epithelial cells. Science 1999;285:578-82.
10. Courey AJ, Jia S. Transcriptional repression: the long and the short of it. Genes Dev 2001;15:2786-96.
11. Cuellar-Cruz M, Briones-Martin-del-Campo M, Canas-Villamar I, et al. High resistance to oxidative stress in the fungal pathogen Candida glabrata is mediated by a single catalase, Cta1p, and is controlled by the transcription factors Yap1p, Skn7p, Msn2p, and Msn4p. Eukaryot Cell 2008;7: 814-25.
12. De Las Penas A, Pan SJ, Castano I, et al. Virulence-related surface glycoproteins in the yeast pathogen Candida glabrata are encoded in subtelomeric clusters and subject to RAP1-and SIR-dependent transcriptional silencing. Genes Dev 2003;17: 2245-58.
13. Domergue R, Castano I, De Las Penas A, et al. Nicotinic acid limitation regulates silencing of Candida adhesins during UTI. Science 2005;308:866-70.
14. Ellahi A, Thurtle DM, Rine J. The chromatin and transcriptional landscape of native Saccharomyces cerevisiae telomeres and subtelomeric domains. Genetics 2015;200:505-21.
15. Fabre E, Muller H, Therizols P, et al. Comparative genomics in hemiascomycete yeasts: evolution of sex, silencing, and subtelomeres. Mol Biol Evol 2005;22:856-73.
16. Fourel G, Revardel E, Koering CE, et al. Cohabitation of insulators and silencing elements in yeast subtelomeric regions. EMBO J 1999;18:2522-37.
17. Fox CA, McConnell KH. Toward biochemical understanding of a transcriptionally silenced chromosomal domain in Saccharomyces cerevisiae. J Biol Chem 2005;280:8629-32.
18. Froyd CA, Rusche LN. The duplicated deacetylases Sir2 and Hst1 subfunctionalized by acquiring complementary inactivating mutations. Mol Cell Biol 2011;31:3351-65.
19. Gabaldon T, Martin T, Marcet-Houben M, et al. Comparative genomics of emerging pathogens in the Candida glabrata clade. BMC Genomics 2013;14:623.
20. Gallegos-Garcia V, Pan SJ, Juarez-Cepeda J, et al. A novel downstream regulatory element cooperates with the silencing machinery to repress EPA1 expression in Candida glabrata. Genetics 2012;190:1285-97.
21. Gasser SM, Cockell MM. The molecular biology of the SIR proteins. Gene 2001;279:1-16.
22. Gordon JL, Byrne KP, Wolfe KH. Additions, losses, and rearrangements on the evolutionary route froma reconstructed ancestor to the modern Saccharomyces cerevisiae genome. PLoS Genet 2009;5:e1000485.
23. Gottschling DE, Aparicio OM, Billington BL, et al. Position effect at S. cerevisiae telomeres: reversible repression of Pol II transcription. Cell 1990;63:751-62.
24. Gravel S, Larrivee M, Labrecque P, et al. Yeast Ku as a regulator of chromosomal DNA end structure. Science 1998;280:741-4.
25. Greiss S, Gartner A. Sirtuin/Sir2 phylogeny, evolutionary considerations and structural conservation. Mol Cells 2009;28: 407-15.
26. Gutierrez-Escobedo G, Orta-Zavalza E, Castano I, et al. Role of glutathione in the oxidative stress response in the fungal pathogen Candida glabrata. Curr Genet 2013; 59:91-106.
27. Halliwell S, Smith MCA, Muston P, et al. Heterogeneous expression of the virulence-related adhesin Epa1 between individual cells and strains of the pathogen Candida glabrata. Eukaryot Cell 2012;11:141-50.
28. Hecht A, Laroche T, Strahl-Bolsinger S, et al. Histone H3 and H4 N-termini interact with SIR3 and SIR4 proteins: a molecular model for the formation of heterochromatin in yeast. Cell 1995;80:583-92.
29. Imai S, Guarente L. Ten years of NAD-dependent SIR2 family deacetylases: implications for metabolic diseases. Trends Pharmacol Sci 2010;31:212-20.
30. Iraqui I, Garcia-Sanchez S, Aubert S, et al. The Yak1p kinase controls expression of adhesins and biofilm formation in Candida glabrata in a Sir4p-dependent pathway. Mol Microbiol 2005;55:1259-71.
31. Juarez-Cepeda J, Orta-Zavalza E, Canas-Villamar I, et al. The EPA2 adhesin encoding gene is responsive to oxidative stress in the opportunistic fungal pathogen Candida glabrata. Curr Genet 2015. DOI:10.1007/s00294-015-0473-2.
32. Juarez-Reyes A, Ramirez-Zavaleta CY, Medina-Sanchez L, et al. A protosilencer of subtelomeric gene expression in Candida glabrata with unique properties. Genetics 2012;190:101-11.
33. Kachouri-Lafond R, Dujon B, Gilson E, et al. Large telomerase RNA, telomere length heterogeneity and escape from senescence in Candida glabrata. FEBS Lett 2009;583:3605-10.
34. Kaur R, Ma B, Cormack BP. A family of glycosylphosphatidylinositol-linked aspartyl proteases is required for virulence of Candida glabrata. Proc Natl Acad Sci USA 2007;104:7628-33.
35. Kraneveld EA, de Soet JJ, Deng DM, et al. Identification and differential gene expression of adhesin-like wall proteins in Candida glabrata biofilms. Mycopathologia 2011;172:415-27.
36. Loney ER, Inglis PW, Sharp S, et al. Repressive and non-repressive chromatin at native telomeres in Saccharomyces cerevisiae. Epigenetics Chromatin 2009;2:18.
37. Lu SP, Lin SJ. Regulation of yeast sirtuins by NAD(+) metabolism and calorie restriction. Biochim Biophys Acta 2010;1804:1567-75.
38. Ma B, Pan SJ, Domergue R, et al. High-affinity transporters for NAD(+) precursors in Candida glabrata are regulated by Hst1 and induced in response to niacin limitation. Mol Cell Biol 2009;29:4067-79.
39. Ma B, Pan SJ, Zupancic ML, et al. Assimilation of NAD(+) precursors in Candida glabrata. Mol Microbiol 2007;66:14-25.
40. Martinez-Jimenez V, Ramirez-Zavaleta CY, Orta-Zavalza E, et al. Sir3 polymorphisms in Candida glabrata clinical isolates. Mycopathologia 2013;175:207-19.
41. McCord R, Pierce M, Xie J, et al. Rfm1, a novel tethering factor required to recruit the Hst1 histone deacetylase for repression of middle sporulation genes. Mol Cell Biol 2003;23:2009-16.
42. Muller H, Hennequin C, Gallaud J, et al. The asexual yeast Candida glabrata maintains distinct a and alpha haploid mating types. Eukaryot Cell 2008;7:848-58.
43. Muller H, Hennequin C, Dujon B, Fairhead C. Ascomycetes: the Candida MAT Locus: comparing the MAT in the genomes of hemiascomycetous yeasts. In: Heitman J, Kronstad JW, Taylor JW, et al. (eds). Sex in Fungi: Molecular Determination and Evolutionary Implications. Washington, DC: ASM Press, 2007, pp. 247-66.
44. Mundy RD, Cormack B. Expression of Candida glabrata Adhesins after Exposure to Chemical Preservatives. J Infect Dis 2009;199:1891-8.
45. Orta-Zavalza E, Guerrero-Serrano G, Gutierrez-Escobedo G, et al. Local silencing controls the oxidative stress response and the multidrug resistance in Candida glabrata. Mol Microbiol 2013;88:1135-48.
46. PfallerMA, Messer SA, Moet GJ, et al. 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 (2008-2009). Int J Antimicrob Agents 2011;38:65-9.
47. Pryde FE, Louis EJ. Limitations of silencing at native yeast telomeres. EMBO J 1999;18:2538-50.
48. Rai MN, Balusu S, Gorityala N, et al. Functional genomic analysis of Candida glabrata-macrophage interaction: role of chromatin remodeling in virulence. PLoS Pathog 2012;8: e1002863.
49. Ramirez-Zavaleta CY, Salas-Delgado GE, De Las Penas A, et al. Subtelomeric silencing of the MTL3 locus of Candida glabrata requires yKu70, yKu80, and Rif1 proteins. Eukaryot Cell 2010;9:1602-11.
50. Renauld H, Aparicio OM, Zierath PD, et al. Silent domains are assembled continuously from the telomere and are defined by promoter distance and strength, and by SIR3 dosage. Genes Dev 1993;7:1133-45.
51. Richardson M, Lass-Florl C. Changing epidemiology of systemic fungal infections. Clin Microbiol Infect 2008;14:5-24.
52. Roetzer A, Gratz N, Kovarik P, et al. Autophagy supports Candida glabrata survival during phagocytosis. Cell Microbiol 2010;12:199-216.
53. Roetzer A, Gregori C, Jennings AM, et al. Candida glabrata environmental stress response involves Saccharomyces cerevisiae Msn2/4 orthologous transcription factors. Mol Microbiol 2008;69:603-20.
54. Roetzer A, Klopf E, Gratz N, et al. Regulation of Candida glabrata oxidative stress resistance is adapted to host environment. FEBS Lett 2011;585:319-27.
55. Rosas-Hernandez LL, Juarez-Reyes A, Arroyo-Helguera OE, et al. yKu70/yKu80 and Rif1 regulate silencing differentially at telomeres in Candida glabrata. Eukaryot Cell 2008;7:2168-78.
56. Rusche LN, Kirchmaier AL, Rine J. The establishment, inheritance, and function of silenced chromatin in Saccharomyces cerevisiae. Annu Rev Biochem 2003;72:481-516.
57. Saijo T, Miyazaki T, Izumikawa K, et al. Skn7p is involved in oxidative stress response and virulence of Candida glabrata. Mycopathologia 2010;169:81-90.
58. Seider K, Brunke S, Schild L, et al. The facultative intracellular pathogen Candida glabrata subverts macrophage cytokine production and phagolysosome maturation. J Immunol 2011;187:3072-86.
59. Srikantha T, Lachke SA, Soll DR. Three mating type-like loci in Candida glabrata. Eukaryot Cell 2003;2:328-40.
60. Strahl-Bolsinger S, Hecht A, Luo K, et al. SIR2 and SIR4 interactions differ in core and extended telomeric heterochromatin in yeast. Genes Dev 1997;11:83-93.
61. Thurtle DM, Rine J. The molecular topography of silenced chromatin in Saccharomyces cerevisiae. Genes Dev 2014;28: 245-58.
62. Wright JH, Gottschling DE, Zakian VA. Saccharomyces telomeres assume a non-nucleosomal chromatin structure. Genes Dev 1992;6:197-210.
63. Xie J, Pierce M, Gailus-Durner V, et al. Sum1 and Hst1 repress middle sporulation-specific gene expression during mitosis in Saccharomyces cerevisiae. EMBO J 1999;18:6448-54.
64. Yanez-Carrillo P, Robledo-Marquez KA, Ramirez-Zavaleta CY, et al. The mating type-like loci of Candida glabrata. Rev Iberoam Micol 2014;31:30-4.
65. Zill OA, Rine J. Interspecies variation reveals a conserved repressor of alpha-specific genes in Saccharomyces yeasts. Genes Dev 2008;22:1704-16.