Interplay of the fungal sumoylation network for control of multicellular development

Molecular Microbiology

Volumn 90, Issue 5, 2013, Pages 1125-1145

  Harting, Rebekka ^a   Bayram, Özgür ^a   Laubinger, Karen ^a,b   Valerius, Oliver ^a   Braus, Gerhard H ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b Deutsche Forschungsgemeinschaft   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; METHYLTRANSFERASE; NEDD8 PROTEIN; PEPTIDASE; PROTEIN AOSA; PROTEIN CCLA; PROTEIN DENA; PROTEIN SETA; PROTEIN UBCN; PROTEIN ULPA; PROTEIN ULPB; SUMO PROTEIN; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG;

ARTICLE; ASPERGILLUS NIDULANS; CONTROLLED STUDY; ENZYME ACTIVITY; FUNGAL DEVELOPMENT; HISTONE MODIFICATION; NEDDYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SUMOYLATION; UBIQUITINATION;

ASPERGILLUS; FUNGI;

ASPERGILLUS NIDULANS; CARRIER PROTEINS; FUNGAL PROTEINS; GENES, FUNGAL; HYPHAE; METHYLTRANSFERASES; PEPTIDE HYDROLASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; SUMOYLATION; TRANSCRIPTION FACTORS; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITINS;

EID: 84888366615     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12421     Document Type: Article

References (95)

1. Acquaviva, L., Szekvolgyi, L., Dichtl, B., Dichtl, B.S., de La Roche Saint Andre, C., Nicolas, A., and Geli, V. (2013) The COMPASS subunit Spp1 links histone methylation to initiation of meiotic recombination. Science 339: 215-218.
2. Adams, T.H., Wieser, J.K., and Yu, J.H. (1998) Asexual sporulation in Aspergillus nidulans. Microbiol Mol Biol Rev 62: 35-54.
3. Alseth, I., Eide, L., Pirovano, M., Rognes, T., Seeberg, E., and Bjoras, M. (1999) The Saccharomyces cerevisiae homologues of endonuclease III from Escherichia coli, Ntg1 and Ntg2, are both required for efficient repair of spontaneous and induced oxidative DNA damage in yeast. Mol Cell Biol 19: 3779-3787.
4. Arnaud, M.B., Cerqueira, G.C., Inglis, D.O., Skrzypek, M.S., Binkley, J., Chibucos, M.C., etal. (2012) The Aspergillus Genome Database (AspGD): recent developments in comprehensive multispecies curation, comparative genomics and community resources. Nucleic Acids Res 40: D653-D659.
5. Bayer, P., Arndt, A., Metzger, S., Mahajan, R., Melchior, F., Jaenicke, R., and Becker, J. (1998) Structure determination of the small ubiquitin-related modifier SUMO-1. J Mol Biol 280: 275-286.
6. Bayram, O., and Braus, G.H. (2012) Coordination of secondary metabolism and development in fungi: the velvet family of regulatory proteins. FEMS Microbiol Rev 36: 1-24.
7. Bayram, O., Krappmann, S., Ni, M., Bok, J.W., Helmstaedt, K., Valerius, O., etal. (2008) VelB/VeA/LaeA complex coordinates light signal with fungal development and secondary metabolism. Science 320: 1504-1506.
8. Bayram, O., Bayram, O.S., Ahmed, Y.L., Maruyama, J., Valerius, O., Rizzoli, S.O., etal. (2012) The Aspergillus nidulans MAPK module AnSte11-Ste50-Ste7-Fus3 controls development and secondary metabolism. PLoS Genet 8: e1002816.
9. Bernier-Villamor, V., Sampson, D.A., Matunis, M.J., and Lima, C.D. (2002) Structural basis for E2-mediated SUMO conjugation revealed by a complex between ubiquitin-conjugating enzyme Ubc9 and RanGAP1. Cell 108: 345-356.
10. Bernstein, B.E., Humphrey, E.L., Erlich, R.L., Schneider, R., Bouman, P., Liu, J.S., etal. (2002) Methylation of histone H3 Lys 4 in coding regions of active genes. Proc Natl Acad Sci USA 99: 8695-8700.
11. Bertani, G. (1951) Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J Bacteriol 62: 293-300.
12. Bok, J.W., and Keller, N.P. (2004) LaeA, a regulator of secondary metabolism in Aspergillus spp. Eukaryot Cell 3: 527-535.
13. Bok, J.W., Chiang, Y.M., Szewczyk, E., Reyes-Dominguez, Y., Davidson, A.D., Sanchez, J.F., etal. (2009) Chromatin-level regulation of biosynthetic gene clusters. Nat Chem Biol 5: 462-464.
14. Bok, J.W., Soukup, A.A., Chadwick, E., Chiang, Y.M., Wang, C.C., and Keller, N.P. (2013) VeA and MvlA repression of the cryptic orsellinic acid gene cluster in Aspergillus nidulans involves histone 3 acetylation. Mol Microbiol 89: 963-974.
15. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
16. Braus, G.H., Krappmann, S., and Eckert, S.E. (2002) Sexual development in ascomycetes: fruit body formation of Aspergillus nidulans. In Molecular Biology of Fungal Development. Osiewacz, H.D. (ed.). New York, Basel: Marcel Decker, Inc., pp. 215-244.
17. Braus, G.H., Irniger, S., and Bayram, O. (2010) Fungal development and the COP9 signalosome. Curr Opin Microbiol 13: 672-676.
18. Briggs, S.D., Bryk, M., Strahl, B.D., Cheung, W.L., Davie, J.K., Dent, S.Y., etal. (2001) Histone H3 lysine 4 methylation is mediated by Set1 and required for cell growth and rDNA silencing in Saccharomyces cerevisiae. Genes Dev 15: 3286-3295.
19. Bruner, S.D., Nash, H.M., Lane, W.S., and Verdine, G.L. (1998) Repair of oxidatively damaged guanine in Saccharomyces cerevisiae by an alternative pathway. Curr Biol 8: 393-403.
20. Bylebyl, G.R., Belichenko, I., and Johnson, E.S. (2003) The SUMO isopeptidase Ulp2 prevents accumulation of SUMO chains in yeast. J Biol Chem 278: 44113-44120.
21. Cherry, J.M., Hong, E.L., Amundsen, C., Balakrishnan, R., Binkley, G., Chan, E.T., etal. (2012) Saccharomyces Genome Database: the genomics resource of budding yeast. Nucleic Acids Res 40: D700-D705.
22. Christmann, M., Schmaler, T., Gordon, C., Huang, X., Bayram, O., Schinke, J., etal. (2013) Control of multicellular development by the physically interacting deneddylases DEN1/DenA and COP9 Signalosome. PLoS Genet 9: e1003275.
23. Dorval, V., and Fraser, P.E. (2007) SUMO on the road to neurodegeneration. Biochim Biophys Acta 1773: 694-706.
24. Dou, H., Huang, C., Van Nguyen, T., Lu, L.S., and Yeh, E.T. (2011) SUMOylation and de-SUMOylation in response to DNA damage. FEBS Lett 585: 2891-2896.
25. Eckert, S.E., Kubler, E., Hoffmann, B., and Braus, G.H. (2000) The tryptophan synthase-encoding trpB gene of Aspergillus nidulans is regulated by the cross-pathway control system. Mol Gen Genet 263: 867-876.
26. Eissenberg, J.C., and Shilatifard, A. (2010) Histone H3 lysine 4 (H3K4) methylation in development and differentiation. Dev Biol 339: 240-249.
27. Ferreira, H.C., Luke, B., Schober, H., Kalck, V., Lingner, J., and Gasser, S.M. (2011) The PIAS homologue Siz2 regulates perinuclear telomere position and telomerase activity in budding yeast. Nat Cell Biol 13: 867-874.
28. Geiss-Friedlander, R., and Melchior, F. (2007) Concepts in sumoylation: a decade on. Nat Rev Mol Cell Biol 8: 947-956.
29. Gerke, J., Bayram, O., and Braus, G.H. (2012) Fungal S-adenosylmethionine synthetase and the control of development and secondary metabolism in Aspergillus nidulans. Fungal Genet Biol 49: 443-454.
30. Giles, S.S., Soukup, A.A., Lauer, C., Shaaban, M., Lin, A., Oakley, B.R., etal. (2011) Cryptic Aspergillus nidulans antimicrobials. Appl Environ Microbiol 77: 3669-3675.
31. Gill, G. (2005) Something about SUMO inhibits transcription. Curr Opin Genet Dev 15: 536-541.
32. Gnad, F., Ren, S., Cox, J., Olsen, J.V., Macek, B., Oroshi, M., and Mann, M. (2007) PHOSIDA (phosphorylation site database): management, structural and evolutionary investigation, and prediction of phosphosites. Gen Biol 8: R250.
33. Gnad, F., Gunawardena, J., and Mann, M. (2011) PHOSIDA 2011: the posttranslational modification database. Nucleic Acids Res 39: D253-D260.
34. Guo, D., Li, M., Zhang, Y., Yang, P., Eckenrode, S., Hopkins, D., etal. (2004) A functional variant of SUMO4, a new I kappa B alpha modifier, is associated with type 1 diabetes. Nat Genet 36: 837-841.
35. Hagiwara, D., Asano, Y., Marui, J., Furukawa, K., Kanamaru, K., Kato, M., etal. (2007) The SskA and SrrA response regulators are implicated in oxidative stress responses of hyphae and asexual spores in the phosphorelay signaling network of Aspergillus nidulans. Biosci Biotechnol Biochem 71: 1003-1014.
36. Hicks, J., Lockington, R.A., Strauss, J., Dieringer, D., Kubicek, C.P., Kelly, J., and Keller, N. (2001) RcoA has pleiotropic effects on Aspergillus nidulans cellular development. Mol Microbiol 39: 1482-1493.
37. Inoue, H., Nojima, H., and Okayama, H. (1990) High efficiency transformation of Escherichia coli with plasmids. Gene 96: 23-28.
38. Johnson, E.S., and Blobel, G. (1997) Ubc9p is the conjugating enzyme for the ubiquitin-like protein Smt3p. J Biol Chem 272: 26799-26802.
39. Johnson, E.S., and Gupta, A.A. (2001) An E3-like factor that promotes SUMO conjugation to the yeast septins. Cell 106: 735-744.
40. Johnson, E.S., Schwienhorst, I., Dohmen, R.J., and Blobel, G. (1997) The ubiquitin-like protein Smt3p is activated for conjugation to other proteins by an Aos1p/Uba2p heterodimer. EMBO J 16: 5509-5519.
41. Käfer, E. (1977) Meiotic and mitotic recombination in Aspergillus and its chromosomal aberrations. Adv Genet 19: 33-131.
42. Kerscher, O. (2007) SUMO junction-what's your function? New insights through SUMO-interacting motifs. EMBO Rep 8: 550-555.
43. Krappmann, S., Jung, N., Medic, B., Busch, S., Prade, R.A., and Braus, G.H. (2006) The Aspergillus nidulans F-box protein GrrA links SCF activity to meiosis. Mol Microbiol 61: 76-88.
44. Kurepa, J., Walker, J.M., Smalle, J., Gosink, M.M., Davis, S.J., Durham, T.L., etal. (2003) The small ubiquitin-like modifier (SUMO) protein modification system in Arabidopsis. Accumulation of SUMO1 and -2 conjugates is increased by stress. J Biol Chem 278: 6862-6872.
45. Lara-Ortiz, T., Riveros-Rosas, H., and Aguirre, J. (2003) Reactive oxygen species generated by microbial NADPH oxidase NoxA regulate sexual development in Aspergillus nidulans. Mol Microbiol 50: 1241-1255.
46. Li, S.J., and Hochstrasser, M. (1999) A new protease required for cell-cycle progression in yeast. Nature 398: 246-251.
47. Li, S.J., and Hochstrasser, M. (2000) The yeast ULP2 (SMT4) gene encodes a novel protease specific for the ubiquitin-like Smt3 protein. Mol Cell Biol 20: 2367-2377.
48. Lipkowitz, S., and Weissman, A.M. (2011) RINGs of good and evil: RING finger ubiquitin ligases at the crossroads of tumour suppression and oncogenesis. Nat Rev Cancer 11: 629-643.
49. Lyst, M.J., and Stancheva, I. (2007) A role for SUMO modification in transcriptional repression and activation. Biochem Soc Trans 35: 1389-1392.
50. Mabey Gilsenan, J., Cooley, J., and Bowyer, P. (2012) CADRE: the Central Aspergillus Data REpository 2012. Nucleic Acids Res 40: D660-D666.
51. Matic, I., van Hagen, M., Schimmel, J., Macek, B., Ogg, S.C., Tatham, M.H., etal. (2008) In vivo identification of human small ubiquitin-like modifier polymerization sites by high accuracy mass spectrometry and an in vitro to in vivo strategy. Mol Cell Proteomics 7: 132-144.
52. Matunis, M.J., Wu, J., and Blobel, G. (1998) SUMO-1 modification and its role in targeting the Ran GTPase-activating protein, RanGAP1, to the nuclear pore complex. J Cell Biol 140: 499-509.
53. Mukhopadhyay, D., and Dasso, M. (2007) Modification in reverse: the SUMO proteases. Trends Biochem Sci 32: 286-295.
54. Mullen, J.R., Chen, C.F., and Brill, S.J. (2010) Wss1 is a SUMO-dependent isopeptidase that interacts genetically with the Slx5-Slx8 SUMO-targeted ubiquitin ligase. Mol Cell Biol 30: 3737-3748.
55. Nacerddine, K., Lehembre, F., Bhaumik, M., Artus, J., Cohen-Tannoudji, M., Babinet, C., etal. (2005) The SUMO pathway is essential for nuclear integrity and chromosome segregation in mice. Dev Cell 9: 769-779.
56. Nahlik, K., Dumkow, M., Bayram, O., Helmstaedt, K., Busch, S., Valerius, O., etal. (2010) The COP9 signalosome mediates transcriptional and metabolic response to hormones, oxidative stress protection and cell wall rearrangement during fungal development. Mol Microbiol 78: 964-979.
57. Nayak, T., Szewczyk, E., Oakley, C.E., Osmani, A., Ukil, L., Murray, S.L., etal. (2006) A versatile and efficient gene-targeting system for Aspergillus nidulans. Genetics 172: 1557-1566.
58. Oberegger, H., Zadra, I., Schoeser, M., and Haas, H. (2000) Iron starvation leads to increased expression of Cu/Zn-superoxide dismutase in Aspergillus. FEBS Lett 485: 113-116.
59. Palvimo, J.J. (2007) PIAS proteins as regulators of small ubiquitin-related modifier (SUMO) modifications and transcription. Biochem Soc Trans 35: 1405-1408.
60. Pickett, M., Gwynne, D.I., Buxton, F.P., Elliott, R., Davies, R.W., Lockington, R.A., etal. (1987) Cloning and characterization of the aldA gene of Aspergillus nidulans. Gene 51: 217-226.
61. Praefcke, G.J., Hofmann, K., and Dohmen, R.J. (2012) SUMO playing tag with ubiquitin. Trends Biochem Sci 37: 23-31.
62. Punt, P.J., and van den Hondel, C.A. (1992) Transformation of filamentous fungi based on hygromycin B and phleomycin resistance markers. Methods Enzymol 216: 447-457.
63. Quevillon, E., Silventoinen, V., Pillai, S., Harte, N., Mulder, N., Apweiler, R., and Lopez, R. (2005) InterProScan: protein domains identifier. Nucleic Acids Res 33: W116-W120.
64. Rodriguez, M.S., Dargemont, C., and Hay, R.T. (2001) SUMO-1 conjugation in vivo requires both a consensus modification motif and nuclear targeting. J Biol Chem 276: 12654-12659.
65. Roguev, A., Schaft, D., Shevchenko, A., Pijnappel, W.W., Wilm, M., Aasland, R., and Stewart, A.F. (2001) The Saccharomyces cerevisiae Set1 complex includes an Ash2 homologue and methylates histone 3 lysine 4. EMBO J 20: 7137-7148.
66. Saracco, S.A., Miller, M.J., Kurepa, J., and Vierstra, R.D. (2007) Genetic analysis of SUMOylation in Arabidopsis: conjugation of SUMO1 and SUMO2 to nuclear proteins is essential. Plant Physiol 145: 119-134.
67. Sarikaya Bayram, O., Bayram, O., Valerius, O., Park, H.S., Irniger, S., Gerke, J., etal. (2010) LaeA control of velvet family regulatory proteins for light-dependent development and fungal cell-type specificity. PLoS Genet 6: e1001226.
68. Semighini, C.P., and Harris, S.D. (2008) Regulation of apical dominance in Aspergillus nidulans hyphae by reactive oxygen species. Genetics 179: 1919-1932.
69. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68: 850-858.
70. Sims, R.J., 3rd, Millhouse, S., Chen, C.F., Lewis, B.A., Erdjument-Bromage, H., Tempst, P., etal. (2007) Recognition of trimethylated histone H3 lysine 4 facilitates the recruitment of transcription postinitiation factors and pre-mRNA splicing. Mol Cell 28: 665-676.
71. Skilton, A., Ho, J.C., Mercer, B., Outwin, E., and Watts, F.Z. (2009) SUMO chain formation is required for response to replication arrest in S.pombe. PLoS ONE 4: e6750.
72. Spektor, T.M., Congdon, L.M., Veerappan, C.S., and Rice, J.C. (2011) The UBC9 E2 SUMO conjugating enzyme binds the PR-Set7 histone methyltransferase to facilitate target gene repression. PLoS ONE 6: e22785.
73. Sterner, D.E., Nathan, D., Reindle, A., Johnson, E.S., and Berger, S.L. (2006) Sumoylation of the yeast Gcn5 protein. Biochemistry 45: 1035-1042.
74. Szewczyk, E., Nayak, T., Oakley, C.E., Edgerton, H., Xiong, Y., Taheri-Talesh, N., etal. (2006) Fusion PCR and gene targeting in Aspergillus nidulans. Nat Protoc 1: 3111-3120.
75. Szewczyk, E., Chiang, Y.M., Oakley, C.E., Davidson, A.D., Wang, C.C., and Oakley, B.R. (2008) Identification and characterization of the asperthecin gene cluster of Aspergillus nidulans. Appl Environ Microbiol 74: 7607-7612.
76. Takahashi, Y., Kahyo, T., Toh, E.A., Yasuda, H., and Kikuchi, Y. (2001) Yeast Ull1/Siz1 is a novel SUMO1/Smt3 ligase for septin components and functions as an adaptor between conjugating enzyme and substrates. J Biol Chem 276: 48973-48977.
77. Tanaka, K., Nishide, J., Okazaki, K., Kato, H., Niwa, O., Nakagawa, T., etal. (1999) Characterization of a fission yeast SUMO-1 homologue, pmt3p, required for multiple nuclear events, including the control of telomere length and chromosome segregation. Mol Cell Biol 19: 8660-8672.
78. Tatham, M.H., Jaffray, E., Vaughan, O.A., Desterro, J.M., Botting, C.H., Naismith, J.H., and Hay, R.T. (2001) Polymeric chains of SUMO-2 and SUMO-3 are conjugated to protein substrates by SAE1/SAE2 and Ubc9. J Biol Chem 276: 35368-35374.
79. Tesfaigzi, J., Smith-Harrison, W., and Carlson, D.M. (1994) A simple method for reusing Western blots on PVDF membranes. Biotechniques 17: 268-269.
80. Todd, R.B., Hynes, M.J., and Andrianopoulos, A. (2006) The Aspergillus nidulans rcoA gene is required for veA-dependent sexual development. Genetics 174: 1685-1688.
81. Uzunova, K., Gottsche, K., Miteva, M., Weisshaar, S.R., Glanemann, C., Schnellhardt, M., etal. (2007) Ubiquitin-dependent proteolytic control of SUMO conjugates. J Biol Chem 282: 34167-34175.
82. Vargas-Perez, I., Sanchez, O., Kawasaki, L., Georgellis, D., and Aguirre, J. (2007) Response regulators SrrA and SskA are central components of a phosphorelay system involved in stress signal transduction and asexual sporulation in Aspergillus nidulans. Eukaryot Cell 6: 1570-1583.
83. van der Veen, A.G., and Ploegh, H.L. (2012) Ubiquitin-like proteins. Annu Rev Biochem 81: 323-357.
84. Wang, C.Y., and She, J.X. (2008) SUMO4 and its role in type 1 diabetes pathogenesis. Diabetes Metab Res Rev 24: 93-102.
85. Wang, J. (2011) Cardiac function and disease: emerging role of small ubiquitin-related modifier. Wiley Interdiscip Rev Syst Biol Med 3: 446-457.
86. Wang, Y., and Dasso, M. (2009) SUMOylation and deSUMOylation at a glance. J Cell Sci 122: 4249-4252.
87. Watson, I.R., Irwin, M.S., and Ohh, M. (2011) NEDD8 pathways in cancer, Sine Quibus Non. Cancer Cell 19: 168-176.
88. Wohlschlegel, J.A., Johnson, E.S., Reed, S.I., and Yates, J.R., 3rd (2004) Global analysis of protein sumoylation in Saccharomyces cerevisiae. J Biol Chem 279: 45662-45668.
89. Wong, K.H., Todd, R.B., Oakley, B.R., Oakley, C.E., Hynes, M.J., and Davis, M.A. (2008) Sumoylation in Aspergillus nidulans: sumO inactivation, overexpression and live-cell imaging. Fungal Genet Biol 45: 728-737.
90. Wood, A., Schneider, J., and Shilatifard, A. (2005) Cross-talking histones: implications for the regulation of gene expression and DNA repair. Biochem Cell Biol 83: 460-467.
91. Wood, V., Harris, M.A., McDowall, M.D., Rutherford, K., Vaughan, B.W., Staines, D.M., etal. (2012) PomBase: a comprehensive online resource for fission yeast. Nucleic Acids Res 40: D695-D699.
92. Woodcock, D.M., Crowther, P.J., Doherty, J., Jefferson, S., DeCruz, E., Noyer-Weidner, M., etal. (1989) Quantitative evaluation of Escherichia coli host strains for tolerance to cytosine methylation in plasmid and phage recombinants. Nucleic Acids Res 17: 3469-3478.
93. von Zeska Kress, M.R., Harting, R., Bayram, O., Christmann, M., Irmer, H., Valerius, O., etal. (2012) The COP9 signalosome counteracts the accumulation of cullin SCF ubiquitin E3 RING ligases during fungal development. Mol Microbiol 83: 1162-1177.
94. Zhao, J. (2007) Sumoylation regulates diverse biological processes. Cell Mol Life Sci 64: 3017-3033.
95. Zhao, X., and Blobel, G. (2005) A SUMO ligase is part of a nuclear multiprotein complex that affects DNA repair and chromosomal organization. Proc Natl Acad Sci USA 102: 4777-4782.