Mycobiology

The Korean Society of Mycology (한국균학회)
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Msi1-Like (MSIL) Proteins in Fungi

  • Yang, Dong-Hoon (Department of Biotechnology, Center for Fungal Pathogenesis, College of Life Science and Biotechnology, Yonsei University) ;
  • Maeng, Shinae (Department of Biotechnology, Center for Fungal Pathogenesis, College of Life Science and Biotechnology, Yonsei University) ;
  • Bahn, Yong-Sun (Department of Biotechnology, Center for Fungal Pathogenesis, College of Life Science and Biotechnology, Yonsei University)
  • Received : 2013.03.09
  • Accepted : 2013.03.11
  • Published : 2013.03.31
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Abstract

Msi1-like (MSIL) proteins, which are eukaryote-specific and contain a series of WD40 repeats, have pleiotropic roles in chromatin assembly, DNA damage repair, and regulation of nutrient/stress-sensing signaling pathways. In the fungal kingdom, the functions of MSIL proteins have been studied most intensively in the budding yeast model Saccharomyces cerevisiae, an ascomycete. Yet their functions are largely unknown in other fungi. Recently, an MSIL protein, Msl1, was discovered and functionally characterized in the pathogenic yeast Cryptococcus neoformans, a basidiomycete. Interestingly, MSIL proteins appear to have redundant and unique roles in both fungi, suggesting that MSIL proteins may have evolutionarily divergent roles in different parts of the fungal kingdom. In this review, we will describe the current findings regarding the role of MSIL proteins in fungi and discuss future directions for research on this topic.

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References

  1. Smith TF, Gaitatzes C, Saxena K, Neer EJ. The WD repeat: a common architecture for diverse functions. Trends Biochem Sci 1999;24:181-5. https://doi.org/10.1016/S0968-0004(99)01384-5
  2. Hennig L, Bouveret R, Gruissem W. MSI1-like proteins: an escort service for chromatin assembly and remodeling complexes. Trends Cell Biol 2005;15:295-302. https://doi.org/10.1016/j.tcb.2005.04.004
  3. Hayashi T, Fujita Y, Iwasaki O, Adachi Y, Takahashi K, Yanagida M. Mis16 and Mis18 are required for CENP-A loading and histone deacetylation at centromeres. Cell 2004; 118:715-29. https://doi.org/10.1016/j.cell.2004.09.002
  4. Verreault A, Kaufman PD, Kobayashi R, Stillman B. Nucleosomal DNA regulates the core-histone-binding subunit of the human Hat1 acetyltransferase. Curr Biol 1998;9:96-108.
  5. Ross JF, Liu X, Dynlacht BD. Mechanism of transcriptional repression of E2F by the retinoblastoma tumor suppressor protein. Mol Cell 1999;3:195-205. https://doi.org/10.1016/S1097-2765(00)80310-X
  6. Brehm A, Miska EA, McCance DJ, Reid JL, Bannister AJ, Kouzarides T. Retinoblastoma protein recruits histone deacetylase to repress transcription. Nature 1998;391:597-601. https://doi.org/10.1038/35404
  7. Luo RX, Postigo AA, Dean DC. Rb interacts with histone deacetylase to repress transcription. Cell 1998;92:463-73. https://doi.org/10.1016/S0092-8674(00)80940-X
  8. Magnaghi-Jaulin L, Groisman R, Naguibneva I, Robin P, Lorain S, Le Villain JP, Troalen F, Trouche D, Harel-Bellan A. Retinoblastoma protein represses transcription by recruiting a histone deacetylase. Nature 1998;391:601-5. https://doi.org/10.1038/35410
  9. Ferreira R, Magnaghi-Jaulin L, Robin P, Harel-Bellan A, Trouche D. The three members of the pocket proteins family share the ability to repress E2F activity through recruitment of a histone deacetylase. Proc Natl Acad Sci U S A 1998;95: 10493-8. https://doi.org/10.1073/pnas.95.18.10493
  10. Iavarone A, Massague J. E2F and histone deacetylase mediate transforming growth factor beta repression of cdc25A during keratinocyte cell cycle arrest. Mol Cell Biol 1999;19:916-22. https://doi.org/10.1128/MCB.19.1.916
  11. Stiegler P, De Luca A, Bagella L, Giordano A. The COOHterminal region of pRb2/p130 binds to histone deacetylase 1 (HDAC1), enhancing transcriptional repression of the E2Fdependent cyclin A promoter. Cancer Res 1998;58:5049-52.
  12. Ach RA, Taranto P, Gruissem W. A conserved family of WD- 40 proteins binds to the retinoblastoma protein in both plants and animals. Plant Cell 1997;9:1595-606. https://doi.org/10.1105/tpc.9.9.1595
  13. Kenzior AL, Folk WR. AtMSI4 and RbAp48 WD-40 repeat proteins bind metal ions. FEBS Lett 1998;440:425-9. https://doi.org/10.1016/S0014-5793(98)01500-2
  14. Hennig L, Taranto P, Walser M, Schonrock N, Gruissem W. Arabidopsis MSI1 is required for epigenetic maintenance of reproductive development. Development 2003;130:2555-65. https://doi.org/10.1242/dev.00470
  15. Ausin I, Alonso-Blanco C, Jarillo JA, Ruiz-Garcia L, Martinez- Zapater JM. Regulation of flowering time by FVE, a retinoblastoma-associated protein. Nat Genet 2004;36:162-6. https://doi.org/10.1038/ng1295
  16. Kim HJ, Hyun Y, Park JY, Park MJ, Park MK, Kim MD, Kim HJ, Lee MH, Moon J, Lee I, et al. A genetic link between cold responses and flowering time through FVE in Arabidopsis thaliana. Nat Genet 2004;36:167-71. https://doi.org/10.1038/ng1298
  17. Michaels SD, Amasino RM. Loss of FLOWERING LOCUS C activity eliminates the late-flowering phenotype of FRIGIDA and autonomous pathway mutations but not responsiveness to vernalization. Plant Cell 2001;13:935-41. https://doi.org/10.1105/tpc.13.4.935
  18. Luo M, Bilodeau P, Dennis ES, Peacock WJ, Chaudhury A. Expression and parent-of-origin effects for FIS2, MEA, and FIE in the endosperm and embryo of developing Arabidopsis seeds. Proc Natl Acad Sci U S A 2000;97:10637-42. https://doi.org/10.1073/pnas.170292997
  19. Dumbliauskas E, Lechner E, Jaciubek M, Berr A, Pazhouhandeh M, Alioua M, Cognat V, Brukhin V, Koncz C, Grossniklaus U, et al. The Arabidopsis CUL4-DDB1 complex interacts with MSI1 and is required to maintain MEDEA parental imprinting. Embo J 2011;30:731-43. https://doi.org/10.1038/emboj.2010.359
  20. Kaya H, Shibahara KI, Taoka KI, Iwabuchi M, Stillman B, Araki T. FASCIATA genes for chromatin assembly factor-1 in Arabidopsis maintain the cellular organization of apical meristems. Cell 2001;104:131-42. https://doi.org/10.1016/S0092-8674(01)00197-0
  21. Exner V, Taranto P, Schönrock N, Gruissem W, Hennig L. Chromatin assembly factor CAF-1 is required for cellular differentiation during plant development. Development 2006; 133:4163-72. https://doi.org/10.1242/dev.02599
  22. Jullien PE, Mosquna A, Ingouff M, Sakata T, Ohad N, Berger F. Retinoblastoma and its binding partner MSI1 control imprinting in Arabidopsis. PLoS Biol 2008;6:e194. https://doi.org/10.1371/journal.pbio.0060194
  23. Alexandre C, Möller-Steinbach Y, Schonrock N, Gruissem W, Hennig L. Arabidopsis MSI1 is required for negative regulation of the response to drought stress. Mol Plant 2009;2:675-87. https://doi.org/10.1093/mp/ssp012
  24. Yang DH, Maeng S, Strain AK, Floyd A, Nielsen K, Heitman J, Bahn YS. Pleiotropic roles of the Msi1-like protein Msl1 in Cryptococcus neoformans. Eukaryot Cell 2012;11:1482-95. https://doi.org/10.1128/EC.00261-12
  25. Neer EJ, Schmidt CJ, Nambudripad R, Smith TF. The ancient regulatory-protein family of WD-repeat proteins. Nature 1994;371:297-300. https://doi.org/10.1038/371297a0
  26. Smith TF. Diversity of WD-repeat proteins. Subcell Biochem 2008;48:20-30. https://doi.org/10.1007/978-0-387-09595-0_3
  27. Xu C, Min J. Structure and function of WD40 domain proteins. Protein Cell 2011;2:202-14. https://doi.org/10.1007/s13238-011-1018-1
  28. Stirnimann CU, Petsalaki E, Russell RB, Muller CW. WD40 proteins propel cellular networks. Trends Biochem Sci 2010; 35:565-74. https://doi.org/10.1016/j.tibs.2010.04.003
  29. Li D, Roberts R. WD-repeat proteins: structure characteristics, biological function, and their involvement in human diseases. Cell Mol Life Sci 2001;58:2085-97. https://doi.org/10.1007/PL00000838
  30. Loyola A, Almouzni G. Histone chaperones, a supporting role in the limelight. Biochim Biophys Acta 2004;1677:3-11. https://doi.org/10.1016/j.bbaexp.2003.09.012
  31. Kaufman PD, Kobayashi R, Stillman B. Ultraviolet radiation sensitivity and reduction of telomeric silencing in Saccharomyces cerevisiae cells lacking chromatin assembly factor-I. Genes Dev 1997;11:345-57. https://doi.org/10.1101/gad.11.3.345
  32. Smith S, Stillman B. Purification and characterization of CAF-I, a human cell factor required for chromatin assembly during DNA replication in vitro. Cell 1989;58:15-25. https://doi.org/10.1016/0092-8674(89)90398-X
  33. Shibahara K, Stillman B. Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin. Cell 1999;96:575-85. https://doi.org/10.1016/S0092-8674(00)80661-3
  34. Game JC, Kaufman PD. Role of Saccharomyces cerevisiae chromatin assembly factor-I in repair of ultraviolet radiation damage in vivo. Genetics 1999;151:485-97.
  35. Enomoto S, McCune-Zierath PD, Gerami-Nejad M, Sanders MA, Berman J. RLF2, a subunit of yeast chromatin assembly factor-I, is required for telomeric chromatin function in vivo. Genes Dev 1997;11:358-70. https://doi.org/10.1101/gad.11.3.358
  36. Tyler JK, Adams CR, Chen SR, Kobayashi R, Kamakaka RT, Kadonaga JT. The RCAF complex mediates chromatin assembly during DNA replication and repair. Nature 1999; 402:555-60. https://doi.org/10.1038/990147
  37. Kim JA, Haber JE. Chromatin assembly factors Asf1 and CAF-1 have overlapping roles in deactivating the DNA damage checkpoint when DNA repair is complete. Proc Natl Acad Sci U S A 2009;106:1151-6. https://doi.org/10.1073/pnas.0812578106
  38. Enomoto S, Berman J. Chromatin assembly factor I contributes to the maintenance, but not the re-establishment, of silencing at the yeast silent mating loci. Genes Dev 1998;12:219-32. https://doi.org/10.1101/gad.12.2.219
  39. Sharp JA, Fouts ET, Krawitz DC, Kaufman PD. Yeast histone deposition protein Asf1p requires Hir proteins and PCNA for heterochromatic silencing. Curr Biol 2001;11:463-73. https://doi.org/10.1016/S0960-9822(01)00140-3
  40. Sharp JA, Franco AA, Osley MA, Kaufman PD. Chromatin assembly factor I and Hir proteins contribute to building functional kinetochores in S. cerevisiae. Genes Dev 2002; 16:85-100. https://doi.org/10.1101/gad.925302
  41. Spellman PT, Sherlock G, Zhang MQ, Iyer VR, Anders K, Eisen MB, Brown PO, Botstein D, Futcher B. Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol Biol Cell 1998;9:3273-7. https://doi.org/10.1091/mbc.9.12.3273
  42. Pratt ZL, Drehman BJ, Miller ME, Johnston SD. Mutual interdependence of MSI1 (CAC3) and YAK1 in Saccharomyces cerevisiae. J Mol Biol 2007;368:30-43. https://doi.org/10.1016/j.jmb.2007.01.046
  43. Marheineke K, Krude T. Nucleosome assembly activity and intracellular localization of human CAF-1 changes during the cell division cycle. J Biol Chem 1998;273:15279-86. https://doi.org/10.1074/jbc.273.24.15279
  44. Zhu X, Demolis N, Jacquet M, Michaeli T. MSI1 suppresses hyperactive RAS via the cAMP-dependent protein kinase and independently of chromatin assembly factor-1. Curr Genet 2000;38:60-70. https://doi.org/10.1007/s002940000133
  45. Johnston SD, Enomoto S, Schneper L, McClellan MC, Twu F, Montgomery ND, Haney SA, Broach JR, Berman J. CAC3 (MSI1) suppression of RAS2G19V is independent of chromatin assembly factor I and mediated by NPR1. Mol Cell Biol 2001;21:1784-94. https://doi.org/10.1128/MCB.21.5.1784-1794.2001
  46. Ge Z, Wang H, Parthun MR. Nuclear Hat1p complex (NuB4) components participate in DNA repair-linked chromatin reassembly. J Biol Chem 2011;286:16790-9. https://doi.org/10.1074/jbc.M110.216846
  47. Poveda A, Pamblanco M, Tafrov S, Tordera V, Sternglanz R, Sendra R. Hif1 is a component of yeast histone acetyltransferase B, a complex mainly localized in the nucleus. J Biol Chem 2004;279:16033-43. https://doi.org/10.1074/jbc.M314228200
  48. Peserico A, Simone C. Physical and functional HAT/HDAC interplay regulates protein acetylation balance. J Biomed Biotechnol 2011;2011:371832.
  49. Parthun MR, Widom J, Gottschling DE. The major cytoplasmic histone acetyltransferase in yeast: links to chromatin replication and histone metabolism. Cell 1996;87:85-94. https://doi.org/10.1016/S0092-8674(00)81325-2
  50. Kelly TJ, Qin S, Gottschling DE, Parthun MR. Type B histone acetyltransferase Hat1p participates in telomeric silencing. Mol Cell Biol 2000;20:7051-8. https://doi.org/10.1128/MCB.20.19.7051-7058.2000
  51. Kleff S, Andrulis ED, Anderson CW, Sternglanz R. Identification of a gene encoding a yeast histone H4 acetyltransferase. J Biol Chem 1995;270:24674-7. https://doi.org/10.1074/jbc.270.42.24674
  52. Rosaleny LE, Antunez O, Ruiz-Garcia AB, Perez-Ortin JE, Tordera V. Yeast HAT1 and HAT2 deletions have different life-span and transcriptome phenotypes. FEBS Lett 2005; 579:4063-8. https://doi.org/10.1016/j.febslet.2005.06.028
  53. Suter B, Pogoutse O, Guo X, Krogan N, Lewis P, Greenblatt JF, Rine J, Emili A. Association with the origin recognition complex suggests a novel role for histone acetyltransferase Hat1p/Hat2p. BMC Biol 2007;5:38. https://doi.org/10.1186/1741-7007-5-38
  54. Ruggieri R, Tanaka K, Nakafuku M, Kaziro Y, Toh-e A, Matsumoto K. MSI1, a negative regulator of the RAS-cAMP pathway in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 1989;86:8778-82. https://doi.org/10.1073/pnas.86.22.8778
  55. Toda T, Uno I, Ishikawa T, Powers S, Kataoka T, Broek D, Cameron S, Broach J, Matsumoto K, Wigler M. In yeast, RAS proteins are controlling elements of adenylate cyclase. Cell 1985;40:27-36. https://doi.org/10.1016/0092-8674(85)90305-8
  56. Pan X, Heitman J. Cyclic AMP-dependent protein kinase regulates pseudohyphal differentiation in Saccharomyces cerevisiae. Mol Cell Biol 1999;19:4874-87. https://doi.org/10.1128/MCB.19.7.4874
  57. Sass P, Field J, Nikawa J, Toda T, Wigler M. Cloning and characterization of the high-affinity cAMP phosphodiesterase of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 1986;83:9303-7. https://doi.org/10.1073/pnas.83.24.9303
  58. Wilson RB, Tatchell K. SRA5 encodes the low-Km cyclic AMP phosphodiesterase of Saccharomyces cerevisiae. Mol Cell Biol 1988;8:505-10. https://doi.org/10.1128/MCB.8.1.505
  59. Robinson LC, Gibbs JB, Marshall MS, Sigal IS, Tatchell K. CDC25: a component of the RAS-adenylate cyclase pathway in Saccharomyces cerevisiae. Science 1987;235:1218-21. https://doi.org/10.1126/science.3547648
  60. Tanaka K, Nakafuku M, Satoh T, Marshall MS, Gibbs JB, Matsumoto K, Kaziro Y, Toh-e A. S. cerevisiae genes IRA1 and IRA2 encode proteins that may be functionally equivalent to mammalian ras GTPase activating protein. Cell 1990;60: 803-7. https://doi.org/10.1016/0092-8674(90)90094-U
  61. Ross EM, Wilkie TM. GTPase-activating proteins for heterotrimeric G proteins: regulators of G protein signaling (RGS) and RGS-like proteins. Annu Rev Biochem 2000;69: 795-827. https://doi.org/10.1146/annurev.biochem.69.1.795
  62. Cabrera-Vera TM, Vanhauwe J, Thomas TO, Medkova M, Preininger A, Mazzoni MR, Hamm HE. Insights into G protein structure, function, and regulation. Endocr Rev 2003; 24:765-81. https://doi.org/10.1210/er.2000-0026
  63. Fedor-Chaiken M, Deschenes RJ, Broach JR. SRV2, a gene required for RAS activation of adenylate cyclase in yeast. Cell 1990;61:329-40. https://doi.org/10.1016/0092-8674(90)90813-T
  64. Qian YW, Wang YC, Hollingsworth RE Jr, Jones D, Ling N, Lee EY. A retinoblastoma-binding protein related to a negative regulator of Ras in yeast. Nature 1993;364:648-52. https://doi.org/10.1038/364648a0
  65. Vandenbol M, Jauniaux JC, Grenson M. The Saccharomyces cerevisiae NPR1 gene required for the activity of ammoniasensitive amino acid permeases encodes a protein kinase homologue. Mol Gen Genet 1990;222:393-9. https://doi.org/10.1007/BF00633845
  66. Lorenz MC, Heitman J. The MEP2 ammonium permease regulates pseudohyphal differentiation in Saccharomyces cerevisiae. EMBO J 1998;17:1236-47. https://doi.org/10.1093/emboj/17.5.1236
  67. Garrett S, Broach J. Loss of Ras activity in Saccharomyces cerevisiae is suppressed by disruptions of a new kinase gene, YAKI, whose product may act downstream of the cAMPdependent protein kinase. Genes Dev 1989;3:1336-48. https://doi.org/10.1101/gad.3.9.1336
  68. Garrett S, Menold MM, Broach JR. The Saccharomyces cerevisiae YAK1 gene encodes a protein kinase that is induced by arrest early in the cell cycle. Mol Cell Biol 1991;11:4045-52. https://doi.org/10.1128/MCB.11.8.4045
  69. Smith A, Ward MP, Garrett S. Yeast PKA represses Msn2p/ Msn4p-dependent gene expression to regulate growth, stress response and glycogen accumulation. EMBO J 1998;17:3556-64. https://doi.org/10.1093/emboj/17.13.3556
  70. Zhang Z, Smith MM, Mymryk JS. Interaction of the E1A oncoprotein with Yak1p, a novel regulator of yeast pseudohyphal differentiation, and related mammalian kinases. Mol Biol Cell 2001;12:699-710. https://doi.org/10.1091/mbc.12.3.699
  71. Hartley AD, Ward MP, Garrett S. The Yak1 protein kinase of Saccharomyces cerevisiae moderates thermotolerance and inhibits growth by an Sch9 protein kinase-independent mechanism. Genetics 1994;136:465-74.
  72. Bahn YS, Xue C, Idnurm A, Rutherford JC, Heitman J, Cardenas ME. Sensing the environment: lessons from fungi. Nat Rev Microbiol 2007;5:57-69. https://doi.org/10.1038/nrmicro1578
  73. Kozubowski L, Lee SC, Heitman J. Signalling pathways in the pathogenesis of Cryptococcus. Cell Microbiol 2009;11:370-80. https://doi.org/10.1111/j.1462-5822.2008.01273.x
  74. Alspaugh JA, Cavallo LM, Perfect JR, Heitman J. RAS1 regulates filamentation, mating and growth at high temperature of Cryptococcus neoformans. Mol Microbiol 2000;36:352-65. https://doi.org/10.1046/j.1365-2958.2000.01852.x
  75. Maeng S, Ko YJ, Kim GB, Jung KW, Floyd A, Heitman J, Bahn YS. Comparative transcriptome analysis reveals novel roles of the Ras and cyclic AMP signaling pathways in environmental stress response and antifungal drug sensitivity in Cryptococcus neoformans. Eukaryot Cell 2010;9:360-78. https://doi.org/10.1128/EC.00309-09
  76. Taylor-Harding B, Binne UK, Korenjak M, Brehm A, Dyson NJ. p55, the Drosophila ortholog of RbAp46/RbAp48, is required for the repression of dE2F2/RBF-regulated genes. Mol Cell Biol 2004;24:9124-36. https://doi.org/10.1128/MCB.24.20.9124-9136.2004
  77. Tyler JK, Bulger M, Kamakaka RT, Kobayashi R, Kadonaga JT. The p55 subunit of Drosophila chromatin assembly factor 1 is homologous to a histone deacetylase-associated protein. Mol Cell Biol 1996;16:6149-59. https://doi.org/10.1128/MCB.16.11.6149
  78. Chu S, DeRisi J, Eisen M, Mulholland J, Botstein D, Brown PO, Herskowitz I. The transcriptional program of sporulation in budding yeast. Science 1998;282:699-705. https://doi.org/10.1126/science.282.5389.699
  79. Kennedy BK, Liu OW, Dick FA, Dyson N, Harlow E, Vidal M. Histone deacetylase-dependent transcriptional repression by pRB in yeast occurs independently of interaction through the LXCXE binding cleft. Proc Natl Acad Sci U S A 2001; 98:8720-5. https://doi.org/10.1073/pnas.151240898