Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Epigenetic Control of Oxidative Stresses by Histone Acetyltransferases in Candida albicans

  • Kim, Jueun (Department of Molecular Bioscience, College of Biomedical Science, Kangwon National University) ;
  • Park, Shinae (Department of Molecular Bioscience, College of Biomedical Science, Kangwon National University) ;
  • Lee, Jung-Shin (Department of Molecular Bioscience, College of Biomedical Science, Kangwon National University)
  • Received : 2017.07.13
  • Accepted : 2017.11.15
  • Published : 2018.02.28
Download PDF
⟨ Previous Next ⟩

Abstract

Candida albicans is a major pathogenic fungus in humans, and meets at first the innate immune cells, such as macrophages, in its host. One important strategy of the host cell to kill C. albicans is to produce reactive oxygen species (ROS) by the macrophages. In response to ROS produced by the macrophages, C. albicans operates its defense mechanisms against them by expressing its oxidative stress response genes. Although there have been many research studies explaining the specific transcription factors and the expression of the oxidative stress genes in C. albicans, the regulation of the oxidative stress genes by chromatin structure is little known. Epigenetic regulation by the chromatin structure is very important for the regulation of eukaryotic gene expression, including the chromatin structure dynamics by histone modifications. Among various histone modifications, histone acetylation is reported for its direct relationship to the regulation of gene expression. Recent studies reported that histone acetyltransferases regulate genes to respond to the oxidative stress in C. albicans. In this review, we introduce all histone acetyltransferases that C. albicans contains and some papers that explain how histone acetyltransferases participate in the oxidative stress response in C. albicans.

Keywords

References

  1. Berman J, Sudbery PE. 2002. Candida albicans: a molecular revolution built on lessons from budding yeast. Nat. Rev. Genet. 3: 918-932.
  2. de Nadal E, Ammerer G, Posas F. 2011. Controlling gene expression in response to stress. Nat. Rev. Genet. 12: 833-845. https://doi.org/10.1038/nrg3055
  3. van Dijk EL, Auger H, Jaszczyszyn Y, Thermes C. 2014. Ten years of next-generation sequencing technology. Trends Genet. 30: 418-426. https://doi.org/10.1016/j.tig.2014.07.001
  4. Wang Z, Gerstein M, Snyder M. 2009. RNA-Seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet. 10: 57-63. https://doi.org/10.1038/nrg2484
  5. Enguita JF, Costa CM, Fusco-Almeida M, Mendes-Giannini J, Leitao LA. 2016. Transcriptomic crosstalk between fungal invasive pathogens and their host cells: opportunities and challenges for next-generation sequencing methods. J. Fungi 2: 7. https://doi.org/10.3390/jof2010007
  6. Dantas DA, Day A, Ikeh M, Kos I, Achan B, Quinn J. 2015. Oxidative stress responses in the human fungal pathogen, Candida albicans. Biomolecules 5: 142-165.
  7. Baek Y, Kim Y, Yim H, Kang S. 2004. Disruption of ${\gamma}$-glutamylcysteine synthetase results in absolute glutathione auxotrophy and apoptosis in Candida albicans. FEBS Lett. 556: 47-52. https://doi.org/10.1016/S0014-5793(03)01363-2
  8. Komalapriya C, Kaloriti D, Tillmann AT, Yin Z, Herrero-de-Dios C, Jacobsen MD, et al. 2015. Integrative model of oxidative stress adaptation in the fungal pathogen Candida albicans. PLoS One 10: e0137750 https://doi.org/10.1371/journal.pone.0137750
  9. Hwang C, Rhie G, Oh J, Huh W, Y im H, Kang S. 2002. Copper- and zinc-containing superoxide dismutase (Cu/ZnSOD) is required for the protection of Candida albicans against oxidative stresses and the expression of its full virulence. Microbiology 148: 3705-3713.
  10. Wysong DR, Christin L, Sugar AM, Robbins PW, Diamond RD. 1998. Cloning and sequencing of a Candida albicans catalase gene and effects of disruption of this gene. Infect. Immun. 66: 1953-1961.
  11. Kornberg RD. 1974. Chromatin structure: a repeating unit of histones and DNA. Science 184: 868. https://doi.org/10.1126/science.184.4139.868
  12. Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ. 1997. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389: 251-260. https://doi.org/10.1038/38444
  13. Bannister AJ, Kouzarides T. 2011. Regulation of chromatin by histone modifications. Cell Res. 21: 381-395. https://doi.org/10.1038/cr.2011.22
  14. Grunstein M. 1997. Histone acetylation in chromatin structure and transcription. Nature 389: 349-352.
  15. Marmorstein R, Zhou M. 2014. Writers and readers of histone acetylation: structure, mechanism, and inhibition. Cold Spring Harb. Perspect. Biol. 6: a018762.
  16. Shahbazian MD, Grunstein M. 2007. Functions of sitespecific histone acetylation and deacetylation. Annu. Rev. Biochem. 76: 75-100. https://doi.org/10.1146/annurev.biochem.76.052705.162114
  17. Roth SY, Denu JM, Allis CD. 2001. Histone acetyltransferases. Annu. Rev. Biochem. 70: 81-120. https://doi.org/10.1146/annurev.biochem.70.1.81
  18. Sterner DE, Berger SL. 2000. Acetylation of histones and transcription-related factors. Microbiol. Mol. Biol. Rev. 64: 435-459. https://doi.org/10.1128/MMBR.64.2.435-459.2000
  19. Sellam A, Askew C, Epp E, Lavoie H, Whiteway M, Nantel A. 2009. Genome-wide mapping of the coactivator Ada2p yields insight into the functional roles of SAGA/ADA complex in Candida albicans. Mol. Biol. Cell 20: 2389-2400. https://doi.org/10.1091/mbc.e08-11-1093
  20. da Rosa L, Boyartchuk VL, Zhu LJ, Kaufman PD. 2010. Histone acetyltransferase Rtt109 is required for Candida albicans pathogenesis. Proc. Natl. Acad. Sci. USA 107: 1594-1599. https://doi.org/10.1073/pnas.0912427107
  21. Tscherner M, Zwolanek F, Jenull S, Sedlazeck FJ, Petryshyn A, Frohner IE, et al. 2015. The Candida albicans histone acetyltransferase Hat1 regulates stress resistance and virulence via distinct chromatin assembly pathways. PLoS Pathog. 11: e1005218. https://doi.org/10.1371/journal.ppat.1005218
  22. Lee KK, Workman JL. 2007. Histone acetyltransferase complexes: one size doesn't fit all. Nat. Rev. Mol. Cell Biol. 8: 284-295. https://doi.org/10.1038/nrm2145
  23. Chang P, Fan X, Chen J. 2015. Function and subcellular localization of Gcn5, a histone acetyltransferase in Candida albicans. Fungal Genet. Biol. 81: 132-141. https://doi.org/10.1016/j.fgb.2015.01.011
  24. Sudbery PE. 2011. Growth of Candida albicans hyphae. Nat. Rev. Microbiol. 9: 737-748. https://doi.org/10.1038/nrmicro2636
  25. Lu Y, Su C, Mao X, Raniga PP, Liu H, Chen J. 2008. Efg1-mediated recruitment of NuA4 to promoters is required for hypha-specific Swi/Snf binding and activation in Candida albicans. Mol. Biol. Cell 19: 4260-4272.
  26. Wang X, Chang P, Ding J, Chen J. 2013. Distinct and redundant roles of the two MYST histone acetyltransferases Esa1 and Sas2 in cell growth and morphogenesis of Candida albicans. Eukaryot. Cell 12: 438-449. https://doi.org/10.1128/EC.00275-12
  27. Osada S, Sutton A, Muster N, Brown CE, Yates JR, Sternglanz R, Workman JL. 2001. The yeast SAS (something about silencing) protein complex contains a MYST-type putative acetyltransferase and functions with chromatin assembly factor ASF1. Genes Dev. 15: 3155-3168. https://doi.org/10.1101/gad.907201
  28. Shia W, Osada S, Florens L, Swanson SK, Washburn MP, Workman JL. 2005. Characterization of the yeast trimeric-SAS acetyltransferase complex. J. Biol. Chem. 280: 11987-11994.
  29. Kimura A, Umehara T, Horikoshi M. 2002. Chromosomal gradient of histone acetylation established by Sas2p and Sir2p functions as a shield against gene silencing. Nat. Genet. 32: 370-377. https://doi.org/10.1038/ng993
  30. Suka N, Luo K, Grunstein M. 2002. Sir2p and Sas2p opposingly regulate acetylation of yeast histone H4 lysine16 and spreading of heterochromatin. Nat. Genet. 32: 378-383.
  31. Tscherner M, Stappler E, Hnisz D, Kuchler K. 2012. The histone acetyltransferase Hat1 facilitates DNA damage repair and morphogenesis in Candida albicans. Mol. Microbiol. 86: 1197-1214. https://doi.org/10.1111/mmi.12051
  32. Schneider J, Bajwa P, Johnson FC, Bhaumik SR, Shilatifard A. 2006. Rtt109 is required for proper H3K56 acetylation: a chromatin mark associated with the elongating RNA polymerase II. J. Biol. Chem. 281: 37270-37274.
  33. Driscoll R, Hudson A, Jackson SP. 2007. Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. Science 315: 649. https://doi.org/10.1126/science.1135862
  34. Wittschieben BO, Otero G, de Bizemont T, Fellows J, Erdjument-Bromage H, Ohba R, et al. 1999. A novel histone acetyltransferase is an integral subunit of elongating RNA polymerase II holoenzyme. Mol. Cell 4: 123-128. https://doi.org/10.1016/S1097-2765(00)80194-X
  35. Li F, Lu J, Han Q, Zhang G, Huang B. 2005. The Elp3 subunit of human Elongator complex is functionally similar to its counterpart in yeast. Mol. Genet. Genomics 273: 264-272. https://doi.org/10.1007/s00438-005-1120-2
  36. Angus-Hill ML, Dutnall RN, Tafrov ST, Sternglanz R, Ramakrishnan V. 1999. Crystal structure of the histone acetyltransferase Hpa2: a tetrameric member of the Gcn5-related N-acetyltransferase superfamily. J. Mol. Biol. 294: 1311-1325.
  37. Grant PA, Duggan L, Cote J, Roberts SM, Brownell JE, Candau R, et al. 1997. Yeast Gcn5 functions in two multisubunit complexes to acetylate nucleosomal histones: characterization of an Ada complex and the SAGA (Spt/Ada) complex. Genes Dev. 11: 1640-1650. https://doi.org/10.1101/gad.11.13.1640
  38. Candau R, Z hou JX, Allis C D, Berger SL. 1997. H istone acetyltransferase activity and interaction with ADA2 are critical for GCN5 function in vivo. EMBO J. 16: 555-565. https://doi.org/10.1093/emboj/16.3.555
  39. Larschan E, Winston F. 2001. The S. cerevisiae SAGA complex functions in vivo as a coactivator for transcriptional activation by Gal4. Genes Dev. 15: 1946-1956. https://doi.org/10.1101/gad.911501
  40. Wang Y, Cao Y, Jia X, Cao Y, Gao P, Fu X, et al. 2006. Cap1p is involved in multiple pathways of oxidative stress response in Candida albicans. Free Rad. Biol. Med. 40: 1201-1209. https://doi.org/10.1016/j.freeradbiomed.2005.11.019
  41. Moye-Rowley W. 2003. Regulation of the transcriptional response to oxidative stress in fungi: similarities and differences. Eukaryot. Cell 2: 381-389. https://doi.org/10.1128/EC.2.3.381-389.2003
  42. Ramirez-Zavala B, Mogavero S, Scholler E, Sasse C, Rogers PD, Morschhauser J. 2014. SAGA/ADA complex subunit Ada2 is required for Cap1- but not Mrr1-mediated upregulation of the Candida albicans multidrug efflux pump MDR1. Antimicrob. Agents Chemother. 58: 5102-5110. https://doi.org/10.1128/AAC.03065-14
  43. Poveda A, Pamblanco M, Tafrov S, Tordera V, Sternglanz R, Sendra R. 2004. Hif1 is a component of yeast histone acetyltransferase B, a complex mainly localized in the nucleus. J. Biol. Chem. 279: 16033-16043. https://doi.org/10.1074/jbc.M314228200
  44. Ge Z, Wang H, Parthun MR. 2011. Nuclear Hat1p complex (NuB4) components participate in DNA repair-linked chromatin reassembly. J. Biol. Chem. 286: 16790-16799. https://doi.org/10.1074/jbc.M110.216846
  45. Verzijlbergen KF, van Welsem T, Sie D, Lenstra TL, Turner DJ, Holstege FCP, et al. 2011. A barcode screen for epigenetic regulators reveals a role for the NuB4/HAT-B histone acetyltransferase complex in histone turnover. PLoS Genet. 7: e1002284. https://doi.org/10.1371/journal.pgen.1002284
  46. Mahalingaiah PKS, Ponnusamy L, Singh KP. 2016. Oxidative stress-induced epigenetic changes associated with malignant transformation of human kidney epithelial cells. Oncotarget 8: 11127-11143.
  47. Bennett CB, Lewis LK, Karthikeyan G, Lobachev KS, Jin YH, Sterling JF, et al. 2001. Genes required for ionizing radiation resistance in yeast. Nat. Genet. 29: 426-434. https://doi.org/10.1038/ng778
  48. Dahlin JL, Chen X, Walters MA, Zhang Z. 2015. Histonemodifying enzymes, histone modifications and histone chaperones in nucleosome assembly: lessons learned from Rtt109 histone acetyltransferases. Crit. Rev. Biochem. Mol. Biol. 50: 31-53. https://doi.org/10.3109/10409238.2014.978975
  49. Li S, Shogren-Knaak M. 2009. The Gcn5 bromodomain of the SAGA complex facilitates cooperative and cross-tail acetylation of nucleosomes. J. Biol. Chem. 284: 9411-9417. https://doi.org/10.1074/jbc.M809617200
  50. Suka N, Suka Y, Carmen AA, Wu J, Grunstein M. 2001. Highly specific antibodies determine histone acetylation site usage in yeast heterochromatin and euchromatin. Mol. Cell 8: 473-479. https://doi.org/10.1016/S1097-2765(01)00301-X
  51. Millar CB, Xu F, Zhang K, Grunstein M. 2006. Acetylation of H2AZ Lys 14 is associated with genome-wide gene activity in yeast. Genes Dev. 20: 711-722. https://doi.org/10.1101/gad.1395506
  52. Morris SA, Rao B, Garcia BA, Hake SB, Diaz RL, Shabanowitz J, et al. 2007. Identification of histone H3 lysine 36 acetylation as a highly conserved histone modification. J. Biol. Chem. 282: 7632-7640. https://doi.org/10.1074/jbc.M607909200
  53. Searle NE, Torres-Machorro A, Pillus L. 2017. Chromatin regulation by the NuA4 acetyltransferase complex is mediated by essential interactions between enhancer of polycomb (Epl1) and Esa1. Genetics 205: 1125. https://doi.org/10.1534/genetics.116.197830
  54. Allard S, Utley RT, Savard J, Clarke A, Grant P, Brandl CJ, et al. 1999. NuA4, an essential transcription adaptor/histone H4 acetyltransferase complex containing Esa1p and the ATM-related cofactor Tra1p. EMBO J. 18: 5108. https://doi.org/10.1093/emboj/18.18.5108
  55. Keogh M, Mennella TA, Sawa C, Berthelet S, Krogan NJ, Wolek A, et al. 2006. The Saccharomyces cerevisiae histone H2A variant Htz1 is acetylated by NuA4. Genes Dev. 20: 660-665. https://doi.org/10.1101/gad.1388106
  56. Meijsing SH, Ehrenhofer-Murray A. 2001. The silencing complex SAS-I links histone acetylation to the assembly of repressed chromatin by CAF-I and Asf1 in Saccharomyces cerevisiae. Genes Dev. 15: 3169-3182. https://doi.org/10.1101/gad.929001
  57. John S, Howe L, Tafrov ST, Grant PA, Sternglanz R, Workman JL. 2000. The Something About Silencing protein, Sas3, is the catalytic subunit of NuA3, a yTAFII30-containing HAT complex that interacts with the Spt16 subunit of the yeast CP (Cdc68/Pob3)-FACT complex. Genes Dev. 14: 1196-1208.
  58. Taverna SD, Ilin S, Rogers RS, Tanny JC, Lavender H, Li H, et al. 2006. Yng1 PHD finger binding to H3 trimethylated at K4 promotes NuA3 HAT activity at K14 of H3 and transcription at a subset of targeted ORFs. Mol. Cell 24: 785-796.
  59. Gilbert TM, McDaniel SL, Byrum SD, Cades JA, Dancy BCR, Wade H, et al. 2014. A PWWP domain-containing protein targets the NuA3 acetyltransferase complex via histone H3 lysine 36 trimethylation to coordinate transcriptional elongation at coding regions. Mol. Cell. Proteomics 13: 2883-2895. https://doi.org/10.1074/mcp.M114.038224
  60. Parthun MR, Widom J, Gottschling DE. 1996. The major cytoplasmic histone acetyltransferase in yeast: links to chromatin replication and histone metabolism. Cell 87: 85-94. https://doi.org/10.1016/S0092-8674(00)81325-2
  61. Winkler GS, Kristjuhan A, Erdjument-Bromage H, Tempst P, Svejstrup JQ. 2002. Elongator is a histone H3 and H4 acetyltransferase important for normal histone acetylation levels in vivo. Proc. Natl. Acad. Sci. USA 99: 3517-3522. https://doi.org/10.1073/pnas.022042899
  62. Sampath V, Liu B, Tafrov S, Srinivasan M, Rieger R, Chen EI, Sternglanz R. 2013. Biochemical characterization of Hpa2 and Hpa3, two small closely related acetyltransferases from Saccharomyces cerevisiae. J. Biol. Chem. 288: 21506-21513. https://doi.org/10.1074/jbc.M113.486274
  63. Han J, Zhou H, Horazdovsky B, Zhang K, Xu R, Zhang Z. 2007. Rtt109 acetylates histone H3 lysine 56 and functions in DNA replication. Science 315: 653. https://doi.org/10.1126/science.1133234

Cited by

  1. The Fungal Histone Acetyl Transferase Gcn5 Controls Virulence of the Human Pathogen Candida albicans through Multiple Pathways vol.9, pp.None, 2018, https://doi.org/10.1038/s41598-019-45817-5
  2. Histone deacetylase inhibitor attenuates experimental fungal keratitis in mice vol.9, pp.None, 2019, https://doi.org/10.1038/s41598-019-46361-y
  3. Update of Vulvovaginal Candidiasis in Pregnant and Non-pregnant Patients vol.13, pp.4, 2018, https://doi.org/10.1007/s12281-019-00357-3
  4. Histone acetylation/deacetylation in Candida albicans and their potential as antifungal targets vol.15, pp.11, 2020, https://doi.org/10.2217/fmb-2019-0343