Histone H4 dosage modulates DNA damage response in the pathogenic yeast Candida glabrata via homologous recombination pathway
Autoři:
Kundan Kumar aff001; Romila Moirangthem aff001; Rupinder Kaur aff001
Působiště autorů:
Laboratory of Fungal Pathogenesis, Centre for DNA Fingerprinting and Diagnostics, Hyderabad, Telangana, India
aff001; Graduate studies, Manipal Academy of Higher Education, Manipal, Karnataka, India
aff002
Vyšlo v časopise:
Histone H4 dosage modulates DNA damage response in the pathogenic yeast Candida glabrata via homologous recombination pathway. PLoS Genet 16(3): e32767. doi:10.1371/journal.pgen.1008620
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008620
Souhrn
Candida glabrata, a nosocomial fungal bloodstream pathogen, causes significant morbidity and mortality in hospitals worldwide. The ability to replicate in macrophages and survive a high level of oxidative stress contributes to its virulence in the mammalian host. However, the role of DNA repair and recombination mechanisms in its pathobiology is still being discovered. Here, we have characterized the response of C. glabrata to the methyl methanesulfonate (MMS)-induced DNA damage. We found that the MMS exposure triggered a significant downregulation of histone H4 transcript and protein levels, and that, the damaged DNA was repaired by the homologous recombination (HR) pathway. Consistently, the reduced H4 gene dosage was associated with increased HR frequency and elevated resistance to MMS. The genetic analysis found CgRad52, a DNA strand exchange-promoter protein of the HR system, to be essential for this MMS resistance. Further, the tandem-affinity purification and mass spectrometry analysis revealed a substantially smaller interactome of H4 in MMS-treated cells. Among 23 identified proteins, we found the WD40-repeat protein CgCmr1 to interact genetically and physically with H4, and regulate H4 levels, HR pathway and MMS stress survival. Controlling H4 levels tightly is therefore a regulatory mechanism to survive MMS stress in C. glabrata.
Klíčová slova:
DNA damage – DNA repair – DNA-binding proteins – Gene expression – Histones – Homologous recombination – Chromatin – Saccharomyces cerevisiae
Zdroje
1. Ehrenhofer-Murray AE. Chromatin dynamics at DNA replication, transcription and repair. Eur J Biochem. 2004;271: 2335–49. doi: 10.1111/j.1432-1033.2004.04162.x 15182349
2. Hauer MH, Gasser SM. Chromatin and nucleosome dynamics in DNA damage and repair. Genes Dev. 2017;31: 2204–2221. doi: 10.1101/gad.307702.117 29284710
3. Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature. 1997;389: 251–60. doi: 10.1038/38444 9305837
4. Meeks-Wagner D, Hartwell LH. Normal stoichiometry of histone dimer sets is necessary for high fidelity of mitotic chromosome transmission. Cell. 1986;44: 43–52. doi: 10.1016/0092-8674(86)90483-6 3510079
5. MacAlpine DM, Almouzni G. Chromatin and DNA replication. Cold Spring Harb Perspect Biol. 2013;5: a010207. doi: 10.1101/cshperspect.a010207 23751185
6. Smith MM, Murray K. Yeast H3 and H4 histone messenger RNAs are transcribed from two non-allelic gene sets. J Mol Biol. 1983;169: 641–61. doi: 10.1016/s0022-2836(83)80163-6 6313932
7. Eriksson PR, Ganguli D, Nagarajavel V, Clark DJ. Regulation of histone gene expression in budding yeast. Genetics. 2012;191: 7–20. doi: 10.1534/genetics.112.140145 22555441
8. Hentschel CC, Birnstiel ML. The organization and expression of histone gene families. Cell. 1981;25: 301–13. doi: 10.1016/0092-8674(81)90048-9 6793234
9. Montagna MT, Lovero G, Borghi E, Amato G, Andreoni S, Campion L, et al. Candidemia in intensive care unit: a nationwide prospective observational survey (GISIA-3 study) and review of the European literature from 2000 through 2013. Eur Rev Med Pharmacol Sci. 2014;18: 661–74. 24668706
10. Chakrabarti A, Sood P, Rudramurthy SM, Chen S, Kaur H, Capoor M, et al. Incidence, characteristics and outcome of ICU-acquired candidemia in India. Intensive Care Med. 2015;41: 285–95. doi: 10.1007/s00134-014-3603-2 25510301
11. Pfaller MA, Diekema DJ, Turnidge JD, Castanheira M, Jones RN. Twenty years of the SENTRY antifungal surveillance program: results for Candida Species from 1997–2016. Open forum Infect Dis. 2019;6: S79–S94. doi: 10.1093/ofid/ofy358 30895218
12. Klevay MJ, Ernst EJ, Hollanbaugh JL, Miller JG, Pfaller MA, Diekema DJ. Therapy and outcome of Candida glabrata versus Candida albicans bloodstream infection. Diagn Microbiol Infect Dis. 2008;60: 273–7. doi: 10.1016/j.diagmicrobio.2007.10.001 18024053
13. Moran C, Grussemeyer CA, Spalding JR, Benjamin DK, Reed SD. Candida albicans and non-albicans bloodstream infections in adult and pediatric patients: comparison of mortality and costs. Pediatr Infect Dis J. 2009;28: 433–5. doi: 10.1097/INF.0b013e3181920ffd 19319021
14. Moran C, Grussemeyer CA, Spalding JR, Benjamin DK, Reed SD. Comparison of costs, length of stay, and mortality associated with Candida glabrata and Candida albicans bloodstream infections. Am J Infect Control. 2010;38: 78–80. doi: 10.1016/j.ajic.2009.06.014 19836856
15. Fidel PL, Vazquez JA, Sobel JD. Candida glabrata: review of epidemiology, pathogenesis, and clinical disease with comparison to C. albicans. Clin Microbiol Rev. 1999;12: 80–96. 9880475
16. Li L, Dongari-Bagtzoglou A. Oral epithelium-Candida glabrata interactions in vitro. Oral Microbiol Immunol. 2007;22: 182–7. doi: 10.1111/j.1399-302X.2007.00342.x 17488444
17. Makanjuola O, Bongomin F, Fayemiwo SA. An update on the roles of non-albicans Candida Species in Vulvovaginitis. J fungi. 2018;4: 121. doi: 10.3390/jof4040121 30384449
18. Kumar K, Askari F, Sahu MS, Kaur R. Candida glabrata: a lot more than meets the eye. Microorganisms. 2019;7: 39. doi: 10.3390/microorganisms7020039 30704135
19. Dujon B, Sherman D, Fischer G, Durrens P, Casaregola S, Lafontaine I, et al. Genome evolution in yeasts. Nature. 2004;430: 35–44. doi: 10.1038/nature02579 15229592
20. Smith MM, Andrésson OS. DNA sequences of yeast H3 and H4 histone genes from two non-allelic gene sets encode identical H3 and H4 proteins. J Mol Biol. 1983;169: 663–90. doi: 10.1016/s0022-2836(83)80164-8 6355483
21. Smith MM, Stirling VB. Histone H3 and H4 gene deletions in Saccharomyces cerevisiae. J Cell Biol. 1988;106: 557–66. doi: 10.1083/jcb.106.3.557 3279046
22. Jandric Z, Schüller C. Stress response in Candida glabrata: pieces of a fragmented picture. Future Microbiol. 2011;6: 1475–84. doi: 10.2217/fmb.11.131 22122443
23. Roetzer A, Gabaldón T, Schüller C. From Saccharomyces cerevisiae to Candida glabrata in a few easy steps: important adaptations for an opportunistic pathogen. FEMS Microbiol Lett. 2011;314: 1–9. doi: 10.1111/j.1574-6968.2010.02102.x 20846362
24. Rai MN, Balusu S, Gorityala N, Dandu L, Kaur R. Functional genomic analysis of Candida glabrata-macrophage interaction: role of chromatin remodeling in virulence. PLoS Pathog. 2012;8: e1002863. doi: 10.1371/journal.ppat.1002863 22916016
25. Kaur R, Ma B, Cormack BP. A family of glycosylphosphatidylinositol-linked aspartyl proteases is required for virulence of Candida glabrata. Proc Natl Acad Sci. 2007;104: 7628–33. doi: 10.1073/pnas.0611195104 17456602
26. Seider K, Brunke S, Schild L, Jablonowski N, Wilson D, Majer O, et al. The facultative intracellular pathogen Candida glabrata subverts macrophage cytokine production and phagolysosome maturation. J Immunol. 2011;187: 3072–86. doi: 10.4049/jimmunol.1003730 21849684
27. Zacchi LF, Selmecki AM, Berman J, Davis DA. Low dosage of histone H4 leads to growth defects and morphological changes in Candida albicans. PLoS One. 2010;5: e10629. doi: 10.1371/journal.pone.0010629 20498713
28. Kim UJ, Han M, Kayne P, Grunstein M. Effects of histone H4 depletion on the cell cycle and transcription of Saccharomyces cerevisiae. EMBO J. 1988;7: 2211–9. 3046933
29. Gabaldón T, Martin T, Marcet-Houben M, Durrens P, Bolotin-Fukuhara M, Lespinet O, et al. Comparative genomics of emerging pathogens in the Candida glabrata clade. BMC Genomics. 2013;14: 623. doi: 10.1186/1471-2164-14-623 24034898
30. He Q, Yu C, Morse RH. Dispersed mutations in histone H3 that affect transcriptional repression and chromatin structure of the CHA1 promoter in Saccharomyces cerevisiae. Eukaryot Cell. 2008;7: 1649–60. doi: 10.1128/EC.00233-08 18658255
31. Tercero JA, Diffley JFX. Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature. 2001;412: 553–557. doi: 10.1038/35087607 11484057
32. Fry RC, Begley TJ, Samson LD. Genome-wide responses to DNA-damaging agents. Annu Rev Microbiol. 2005;59: 357–77. doi: 10.1146/annurev.micro.59.031805.133658 16153173
33. Kinner A, Wu W, Staudt C, Iliakis G. Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res. 2008;36: 5678–94. doi: 10.1093/nar/gkn550 18772227
34. Cormack BP, Falkow S. Efficient homologous and illegitimate recombination in the opportunistic yeast pathogen Candida glabrata. Genetics. 1999;151: 979–87. 10049916
35. Corrigan MW, Kerwin-Iosue CL, Kuczmarski AS, Amin KB, Wykoff DD. The fate of linear DNA in Saccharomyces cerevisiae and Candida glabrata: the role of homologous and non-homologous end joining. PLoS One. 2013;8: e69628. doi: 10.1371/journal.pone.0069628 23894512
36. Ueno K, Uno J, Nakayama H, Sasamoto K, Mikami Y, Chibana H. Development of a highly efficient gene targeting system induced by transient repression of YKU80 expression in Candida glabrata. Eukaryot Cell. 2007;6: 1239–47. doi: 10.1128/EC.00414-06 17513567
37. Rosas-Hernández LL, Juárez-Reyes A, Arroyo-Helguera OE, De Las Peñas A, Pan S-J, Cormack BP, et al. yKu70/yKu80 and Rif1 regulate silencing differentially at telomeres in Candida glabrata. Eukaryot Cell. 2008;7: 2168–78. doi: 10.1128/EC.00228-08 18836091
38. New JH, Sugiyama T, Zaitseva E, Kowalczykowski SC. Rad52 protein stimulates DNA strand exchange by Rad51 and replication protein A. 1998;391: 407–10. doi: 10.1038/34950 9450760
39. Clark-Adams CD, Norris D, Osley MA, Fassler JS, Winston F. Changes in histone gene dosage alter transcription in yeast. Genes Dev. 1988;2: 150–9. doi: 10.1101/gad.2.2.150 2834270
40. Gossett AJ, Lieb JD. In vivo effects of histone H3 depletion on nucleosome occupancy and position in Saccharomyces cerevisiae. PLoS Genet. 2012;8: e1002771. doi: 10.1371/journal.pgen.1002771 22737086
41. Wyrick JJ, Holstege FC, Jennings EG, Causton HC, Shore D, Grunstein M, et al. Chromosomal landscape of nucleosome-dependent gene expression and silencing in yeast. Nature. 1999;402: 418–21. doi: 10.1038/46567 10586882
42. Fan Y, Nikitina T, Zhao J, Fleury TJ, Bhattacharyya R, Bouhassira EE, et al. Histone H1 depletion in mammals alters global chromatin structure but causes specific changes in gene regulation. Cell. 2005;123: 1199–212. doi: 10.1016/j.cell.2005.10.028 16377562
43. De Las Peñas A, Pan S-J, Castaño I, Alder J, Cregg R, Cormack BP. 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. doi: 10.1101/gad.1121003 12952896
44. de Groot PWJ, Bader O, de Boer AD, Weig M, Chauhan N. Adhesins in human fungal pathogens: glue with plenty of stick. Eukaryot Cell. 2013;12: 470–81. doi: 10.1128/EC.00364-12 23397570
45. Turgeon M-O, Perry NJS, Poulogiannis G. DNA Damage, Repair, and Cancer Metabolism. Front Oncol. 2018;8: 15. doi: 10.3389/fonc.2018.00015 29459886
46. Formosa T, Eriksson P, Wittmeyer J, Ginn J, Yu Y, Stillman DJ. Spt16-Pob3 and the HMG protein Nhp6 combine to form the nucleosome-binding factor SPN. EMBO J. 2001;20: 3506–17. doi: 10.1093/emboj/20.13.3506 11432837
47. Jamai A, Puglisi A, Strubin M. Histone chaperone Spt16 promotes redeposition of the original h3-h4 histones evicted by elongating RNA polymerase. Mol Cell. 2009;35: 377–83. doi: 10.1016/j.molcel.2009.07.001 19683500
48. Hewawasam G, Shivaraju M, Mattingly M, Venkatesh S, Martin-Brown S, Florens L, et al. Psh1 is an E3 ubiquitin ligase that targets the centromeric histone variant Cse4. Mol Cell. 2010;40: 444–54. doi: 10.1016/j.molcel.2010.10.014 21070970
49. Choi D-H, Kwon S-H, Kim J-H, Bae S-H. Saccharomyces cerevisiae Cmr1 protein preferentially binds to UV-damaged DNA in vitro. J Microbiol. 2012;50: 112–8. doi: 10.1007/s12275-012-1597-4 22367945
50. Gallina I, Colding C, Henriksen P, Beli P, Nakamura K, Offman J, et al. Cmr1/WDR76 defines a nuclear genotoxic stress body linking genome integrity and protein quality control. Nat Commun. 2015;6: 6533. doi: 10.1038/ncomms7533 25817432
51. Tkach JM, Yimit A, Lee AY, Riffle M, Costanzo M, Jaschob D, et al. Dissecting DNA damage response pathways by analysing protein localization and abundance changes during DNA replication stress. Nat Cell Biol. 2012;14: 966–76. doi: 10.1038/ncb2549 22842922
52. Prado F, Aguilera A. Partial depletion of histone H4 increases homologous recombination-mediated genetic instability. Mol Cell Biol. 2005;25: 1526–36. doi: 10.1128/MCB.25.4.1526-1536.2005 15684401
53. Liang D, Burkhart SL, Singh RK, Kabbaj MHM, Gunjan A. Histone dosage regulates DNA damage sensitivity in a checkpoint-independent manner by the homologous recombination pathway. Nucleic Acids Res. 2012;40: 9604–9620. doi: 10.1093/nar/gks722 22850743
54. Gilmore JM, Sardiu ME, Venkatesh S, Stutzman B, Peak A, Seidel CW, et al. Characterization of a Highly Conserved Histone Related Protein, Ydl156w, and Its Functional Associations Using Quantitative Proteomic Analyses. Mol Cell Proteomics. 2012;11: M111.011544. doi: 10.1074/mcp.M111.011544 22199229
55. Jelinsky SA, Samson LD. Global response of Saccharomyces cerevisiae to an alkylating agent. Proc Natl Acad Sci. 1999;96: 1486–91. doi: 10.1073/pnas.96.4.1486 9990050
56. Gasch AP, Huang M, Metzner S, Botstein D, Elledge SJ, Brown PO. Genomic expression responses to DNA-damaging agents and the regulatory role of the yeast ATR homolog Mec1p. Mol Biol Cell. 2001;12: 2987–3003. doi: 10.1091/mbc.12.10.2987 11598186
57. Borah S, Shivarathri R, Kaur R. The Rho1 GTPase-activating protein CgBem2 is required for survival of azole stress in Candida glabrata. J Biol Chem. 2011;286: 34311–34324. doi: 10.1074/jbc.M111.264671 21832071
58. Edgar R. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002;30: 207–210. doi: 10.1093/nar/30.1.207 11752295
59. Perez-Riverol Y, Csordas A, Bai J, Bernal-Llinares M, Hewapathirana S, Kundu DJ, et al. The PRIDE database and related tools and resources in 2019: improving support for quantification data. Nucleic Acids Res. 2019;47: D442–D450. doi: 10.1093/nar/gky1106 30395289
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