Genetic evidence that polysumoylation bypasses the need for a SUMO-targeted UB ligase

Genetics

Volumn 187, Issue 1, 2011, Pages 73-87

  Mullen, Janet R ^a   Das, Mukund ^a   Brill, Steven J ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN; PEPTIDASE; PROTEIN SLX5 SLX8; PROTEIN SUBUNIT; SUMO PROTEIN; UBIQUITIN PROTEIN LIGASE; ULP2 ISOPEPTIDASE; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; DNA DAMAGE; DNA REPLICATION; ENZYME ACTIVITY; GENE DELETION; GENOMIC INSTABILITY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; SPOROGENESIS; SUMOYLATION;

ALLELES; AMINO ACID SEQUENCE; ENDOPEPTIDASES; GENES, SUPPRESSOR; GENOMIC INSTABILITY; MOLECULAR SEQUENCE DATA; MUTATION; PHENOTYPE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUMO-1 PROTEIN; SUMOYLATION; UBIQUITIN-PROTEIN LIGASES;

SACCHAROMYCES CEREVISIAE;

EID: 78951471597     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.110.124347     Document Type: Article

References (46)

1. ADAMS, A., D. E. GOTTSCHLING, C. A. KAISER and T. STEARNS, 1997 Methods in Yeast Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
2. BACHANT, J., A. ALCASABAS, Y. BLAT, N. KLECKNER and S. J. ELLEDGE, 2002 The SUMO-1 isopeptidase Smt4 is linked to centromeric cohesion through SUMO-1 modification of DNA topoisomerase II. Mol. Cell 9: 1169-1182.
3. BURGESS, R. C., S. RAHMAN, M. LISBY, R. ROTHSTEIN and X. ZHAO, 2007 The Slx5-Slx8 complex affects sumoylation of DNA repair proteins and negatively regulates recombination. Mol. Cell. Biol. 27: 6153-6162.
4. BYLEBYL, G. R., I. BELICHENKO and E. S. JOHNSON, 2003 The SUMO isopeptidase Ulp2 prevents accumulation of SUMO chains in yeast. J. Biol. Chem. 278: 44113-44120.
5. CHEN, X. L., A. REINDLE and E. S. JOHNSON, 2005 Misregulation of 2 micron circle copy number in a SUMO pathway mutant. Mol. Cell. Biol. 25: 4311-4320.
6. CIECHANOVER, A., and A. L. SCHWARTZ, 1998 The ubiquitin-proteasome pathway: the complexity and myriad functions of proteins death. Proc. Natl. Acad. Sci. USA 95: 2727-2730.
7. DENUC, A., and G. MARFANY, 2010 SUMO and ubiquitin paths converge. Biochem. Soc. Trans. 38: 34-39.
8. DOBSON, M. J., A. J. PICKETT, S. VELMURUGAN, J. B. PINDER, L. A. BARRETT et al., 2005 The 2 micron plasmid causes cell death in Saccharomyces cerevisiae with a mutation in Ulp1 protease. Mol. Cell. Biol. 25: 4299-4310.
9. FU, C., K. AHMED, H. DING, X. DING, J. LAN et al., 2005 Stabilization of PML nuclear localization by conjugation and oligomerization of SUMO-3. Oncogene 24: 5401-5413.
10. GEOFFROY, M. C., and R. T. HAY, 2009 An additional role for SUMO in ubiquitin-mediated proteolysis. Nat. Rev. Mol. Cell Biol. 10: 564-568.
11. GULDENER, U., S.HECK, T. FIELDER, J. BEINHAUER and J.H.HEGEMANN, 1996 A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Res. 24: 2519-2524.
12. II, T., J. R.MULLEN, C. E. SLAGLE and S. J. BRILL, 2007 Stimulation of in vitro sumoylation by Slx5-Slx8: evidence for a functional interaction with the SUMO pathway. DNA Repair (Amst.) 6: 1679-1691.
13. JOHNSON, E. S., 2004 Protein modification by SUMO. Annu. Rev. Biochem. 73: 355-382.
14. KERSCHER, O., R. FELBERBAUM and M. HOCHSTRASSER, 2006 Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu. Rev. Cell Dev. Biol. 22: 159-180.
15. KOSOY, A., T. M. CALONGE, E. A. OUTWIN and M. J. O'CONNELL, 2007 Fission yeast Rnf4 homologs are required for DNA repair. J. Biol. Chem. 282: 20388-20394.
16. LALLEMAND-BREITENBACH, V., M. JEANNE, S. BENHENDA, R. NASR, M. LEI et al., 2008 Arsenic degrades PML or PML-RARalpha through a SUMO-triggered RNF4/ubiquitin-mediated pathway. Nat. Cell Biol. 10: 547-555.
17. LI, S. J., and M. HOCHSTRASSER, 1999 A new protease required for cell-cycle progression in yeast. Nature 398: 246-251. (Pubitemid 29142860)
18. LI, S. J., and M. HOCHSTRASSER, 2000 The yeast ULP2 (SMT4) gene encodes a novel protease specific for the ubiquitin-like Smt3 protein. Mol. Cell. Biol. 20: 2367-2377.
19. LI, S. J., and M. HOCHSTRASSER, 2003 The Ulp1 SUMO isopeptidase: distinct domains required for viability, nuclear envelope localization, and substrate specificity. J. Cell Biol. 160: 1069-1081.
20. LI, Y., H. WANG, S. WANG, D. QUON, Y. W. LIU et al., 2003 Positive and negative regulation of APP amyloidogenesis by sumoylation. Proc. Natl. Acad. Sci. USA 100: 259-264.
21. LIMA, C. D., and D. REVERTER, 2008 Structure of the human SENP7 catalytic domain and poly-SUMO deconjugation activities for SENP6 and SENP7. J. Biol. Chem. 283: 32045-32055.
22. MUKHOPADHYAY, D., and M. DASSO, 2007 Modification in reverse: the SUMO proteases. Trends Biochem. Sci. 32: 286-295.
23. MUKHOPADHYAY, D., F. AYAYDIN, N. KOLLI, S. H. TAN, T. ANAN et al., 2006 SUSP1 antagonizes formation of highly SUMO2/3-conjugated species. J. Cell Biol. 174: 939-949.
24. MULLEN, J. R., and S. J. BRILL, 2008 Activation of the Slx5-Slx8 ubiquitin ligase by poly-SUMO conjugates. J. Biol. Chem. 283: 19912-19921.
25. MULLEN, J. R., V. KALIRAMAN, S. S. IBRAHIM and S. J. BRILL, 2001 Requirement for three novel protein complexes in the absence of the Sgs1 DNA helicase in Saccharomyces cerevisiae. Genetics 157: 103-118.
26. MULLEN, J. R., C. F. CHEN and S. J. BRILL, 2010 Wss1 is a SUMO-dependent isopeptidase that interacts genetically with the Slx5-Slx8 SUMO-targeted Ub ligase. Mol. Cell. Biol. 30: 3737-3748.
27. PANSE, V. G., B. KUSTER, T. GERSTBERGER and E. HURT, 2003 Unconventional tethering of Ulp1 to the transport channel of the nuclear pore complex by karyopherins. Nat. Cell Biol. 5: 21-27.
28. PERRY, J. J., J. A. TAINER and M. N. BODDY, 2008 A SIM-ultaneous role for SUMO and ubiquitin. Trends Biochem. Sci. 33: 201-208.
29. PICKART, C. M., and D. FUSHMAN, 2004 Polyubiquitin chains: polymeric protein signals. Curr. Opin. Chem. Biol. 8: 610-616.
30. PRUDDEN, J., S. PEBERNARD, G. RAFFA, D. A. SLAVIN, J. J. PERRY et al., 2007 SUMO-targeted ubiquitin ligases in genome stability. EMBO J. 18: 4089-4101.
31. RAVID, T., and M. HOCHSTRASSER, 2008 Diversity of degradation signals in the ubiquitin-proteasome system. Nat. Rev. Mol. Cell Biol. 9: 679-690.
32. REID, R. J., I. SUNJEVARIC, W. P. VOTH, S. CICCONE, W. DU et al., 2008 Chromosome-scale genetic mapping using a set of 16 conditionally stable Saccharomyces cerevisiae chromosomes. Genetics 180: 1799-1808.
33. SCHWARTZ, D. C., R. FELBERBAUM and M. HOCHSTRASSER, 2007 The Ulp2 SUMO protease is required for cell division following termination of the DNA damage checkpoint. Mol. Cell. Biol. 27: 6948-6961.
34. SCHWIENHORST, I., E. S. JOHNSON and R. J. DOHMEN, 2000 SUMO conjugation and deconjugation. Mol. Gen. Genet. 263: 771-786.
35. SIKORSKI, R. S., and P. HIETER, 1989 A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 12: 19-27.
36. STRUNNIKOV, A. V., L. ARAVIND and E. V. KOONIN, 2001 Saccharomyces cerevisiae SMT4 encodes an evolutionarily conserved protease with a role in chromosome condensation regulation. Genetics 158: 95-107.
37. SUN, H., J. D. LEVERSON and T. HUNTER, 2007 Conserved function of RNF4 family proteins in eukaryotes: targeting a ubiquitin ligase to SUMOylated proteins. EMBO J. 18: 4102-4112.
38. TATHAM, M. H., E. JAFFRAY, O. A. VAUGHAN, J. M. DESTERRO, C. H. BOTTING et al., 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.
39. TATHAM, M. H., M. C. GEOFFROY, L. SHEN, A. PLECHANOVOVA, N. HATTERSLEY et al., 2008 RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation. Nat. Cell Biol. 10: 538-546.
40. UZUNOVA, K., K. GOTTSCHE, M. MITEVA, S. R. WEISSHAAR, C. GLANEMANN et al., 2007 Ubiquitin-dependent proteolytic control of SUMO conjugates. J. Biol. Chem. 282: 34167-34175.
41. WANG, Z., and G. PRELICH, 2009 Quality control of a transcriptional regulator by SUMO-targeted degradation. Mol. Cell. Biol. 29: 1694-1706.
42. WANG, Z., G. M. JONES and G. PRELICH, 2006 Genetic analysis connects SLX5 and SLX8 to the SUMO pathway in Saccharomyces cerevisiae. Genetics 172: 1499-1509.
43. XIE, Y., O. KERSCHER, M. B. KROETZ, H. F. MCCONCHIE, P. SUNG et al., 2007 The yeast HEX3-SLX8 heterodimer is a ubiquitin ligase stimulated by substrate sumoylation. J. Biol. Chem. 282: 34176-34184.
44. XIE, Y., E. M. RUBENSTEIN, T. MATT and M. HOCHSTRASSER, 2010 SUMO-independent in vivo activity of a SUMO-targeted ubiquitin ligase toward a short-lived transcription factor. Genes Dev. 24: 893-903.
45. XIONG, L., X. L. CHEN, H. R. SILVER, N. T. AHMED and E. S. JOHNSON, 2009 Deficient SUMO attachment to Flp recombinase leads to homologous recombination-dependent hyperamplification of the yeast 2 micron circle plasmid. Mol. Biol. Cell 20: 1241-1251.
46. ZHANG, C., T. M. ROBERTS, J. YANG, R. DESAI and G. W. BROWN, 2006 Suppression of genomic instability by SLX5 and SLX8 in Saccharomyces cerevisiae. DNA Repair (Amst.) 5: 336-346.