SUMO-independent in vivo activity of a SUMO-targeted ubiquitin ligase toward a short-lived transcription factor

Genes and Development

Volumn 24, Issue 9, 2010, Pages 893-903

  Xie, Yang ^b   Rubenstein, Eric M ^a   Matt, Tanja ^c   Hochstrasser, Mark ^a  

^a YALE UNIVERSITY   (United States)

^b NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^c UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Proteasome; STUbL; SUMO; Transcription factor; Ubiquitin

Indexed keywords

RING FINGER PROTEIN; SUMO PROTEIN; TRANSCRIPTION FACTOR; UBIQUITIN CONJUGATING ENZYME; UBIQUITIN PROTEIN LIGASE;

ARTICLE; CONJUGATION; DEGRADATION; IN VIVO STUDY; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN TARGETING; TURNOVER TIME; UBIQUITINATION; YEAST;

AMINO ACID SEQUENCE; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; MOLECULAR SEQUENCE DATA; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 77951806546     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1906510     Document Type: Article

References (48)

1. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K., ed. 1989. Current protocols in molecular biology. Wiley, New York.
2. Bays NW, Gardner RG, Seelig LP, Joazeiro CA, Hampton RY. 2001. Hrd1p/Der3p is a membrane-anchored ubiquitin ligase required for ER-associated degradation. Nat Cell Biol 3: 24-29.
3. Chen P, Hochstrasser M. 1995. Biogenesis, structure, and function of the yeast 20S proteasome. EMBO J 14: 2620-2630.
4. Chen P, Johnson P, Sommer T, Jentsch S, Hochstrasser M. 1993. Multiple ubiquitin-conjugating enzymes participate in the in vivo degradation of the yeast MATα2 repressor. Cell 74: 357-369. (Pubitemid 23221711)
5. Deng M, Hochstrasser M. 2006. Spatially regulated ubiquitin ligation by an ER/nuclear membrane ligase. Nature 443: 827-831. (Pubitemid 44622689)
6. Gelperin DM, White MA, Wilkinson ML, Kon Y, Kung LA, Wise KJ, Lopez-Hoyo N, Jiang L, Piccirillo S, Yu H, et al. 2005. Biochemical and genetic analysis of the yeast proteome with a movable ORF collection. Genes & Dev 19: 2816-2826. (Pubitemid 41739967)
7. Geoffroy MC, Hay RT. 2009. An additional role for SUMO in ubiquitin-mediated proteolysis. Nat Rev Mol Cell Biol 10: 564-568.
8. Goldstein AL, McCusker JH. 1999. Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15: 1541-1553.
9. Guthrie C, Fink GR. 1991. Guide to yeast genetics and molecular biology. Academic Press, San Diego.
10. Hannich JT, Lewis A, Kroetz MB, Li SJ, Heide H, Emili A, Hochstrasser M. 2005. Defining the SUMO-modified proteome by multiple approaches in Saccharomyces cerevisiae. J Biol Chem 280: 4102-4110. (Pubitemid 40288574)
11. Heck JW, Cheung SK, Hampton RY. 2010. Cytoplasmic protein quality control degradation mediated by parallel actions of the E3 ubiquitin ligases Ubr1 and San1. Proc Natl Acad Sci 107: 1106-1111.
12. Hecker CM, Rabiller M, Haglund K, Bayer P, Dikic I. 2006. Specification of SUMO1- and SUMO2-interacting motifs. J Biol Chem 281: 16117-16127.
13. Heideker J, Perry JJ, Boddy MN. 2009. Genome stability roles of SUMO-targeted ubiquitin ligases. DNA Repair (Amst) 8: 517-524.
14. Herskowitz I. 1985. Master regulatory loci in yeast and λ. Cold Spring Harb Symp Quant Biol 50: 565-574.
15. Hochstrasser M, Varshavsky A. 1990. In vivo degradation of a transcriptional regulator: The yeast α2 repressor. Cell 61: 697-708.
16. Hochstrasser M, Ellison MJ, Chau V, Varshavsky A. 1991. The short-lived MATα2 transcriptional regulator is ubiquitinated in vivo. Proc Natl Acad Sci 88: 4606-4610. (Pubitemid 21914590)
17. Joazeiro CA, Weissman AM. 2000. RING finger proteins: Mediators of ubiquitin ligase activity. Cell 102: 549-552.
18. Johnson ES. 2004. Protein modification by SUMO. Annu Rev Biochem 73: 355-382.
19. Johnson PR, Swanson R, Rakhilina L, Hochstrasser M. 1998. Degradation signal masking by heterodimerization of MATα2 and MATa1 blocks their mutual destruction by the ubiquitin-proteasome pathway. Cell 94: 217-227. (Pubitemid 28348009)
20. Kerscher O. 2007. SUMO junction - What's your function? New insights through SUMO-interacting motifs EMBO Rep 8: 550-555.
21. Kerscher O, Felberbaum R, Hochstrasser M. 2006. Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol 22: 159-180.
22. Lallemand-Breitenbach V, Jeanne M, Benhenda S, Nasr R, Lei M, Peres L, Zhou J, Zhu J, Raught B, de The H. 2008. Arsenic degrades PML or PML-RARα through a SUMO-triggered RNF4/ubiquitin-mediated pathway. Nat Cell Biol 10: 547-555. (Pubitemid 351627374)
23. Laney JD, Hochstrasser M. 2003. Ubiquitin-dependent degradation of the yeast Matα2 repressor enables a switch in developmental state. Genes & Dev 17: 2259-2270. (Pubitemid 37128641)
24. Laney JD, Mobley EF, Hochstrasser M. 2006. The short-lived Matα2 transcriptional repressor is protected from degradation in vivo by interactions with its corepressors Tup1 and Ssn6. Mol Cell Biol 26: 371-380.
25. Mead J, Zhong H, Acton TB, Vershon AK. 1996. The yeast α2 and Mcm1 proteins interact through a region similar to a motif found in homeodomain proteins of higher eukaryotes. Mol Cell Biol 16: 2135-2143. (Pubitemid 26123734)
26. Mullen JR, Brill SJ. 2008. Activation of the Slx5-Slx8 ubiquitin ligase by poly-small ubiquitin-like modifier conjugates. J Biol Chem 283: 19912-19921.
27. Mullen JR, Kaliraman V, Ibrahim SS, Brill SJ. 2001. Requirement for three novel protein complexes in the absence of the Sgs1 DNA helicase in Saccharomyces cerevisiae. Genetics 157: 103-118.
28. Muratani M, Tansey WP. 2003. How the ubiquitin-proteasome system controls transcription. Nat Rev Mol Cell Biol 4: 192-201. (Pubitemid 36288041)
29. Perry JJ, Tainer JA, Boddy MN. 2008. A SIM-ultaneous role for SUMO and ubiquitin. Trends Biochem Sci 33: 201-208.
30. Pickart CM. 2001. Mechanisms underlying ubiquitination. Annu Rev Biochem 70: 503-533.
31. Prudden J, Pebernard S, Raffa G, Slavin DA, Perry JJ, Tainer JA, McGowan CH, Boddy MN. 2007. SUMO-targeted ubiquitin ligases in genome stability. EMBO J 26: 4089-4101. (Pubitemid 47462097)
32. Prudden J, Perry JJ, Arvai AS, Tainer JA, Boddy MN. 2009. Molecular mimicry of SUMO promotes DNA repair. Nat Struct Mol Biol 16: 509-516.
33. Ravid T, Hochstrasser M. 2007. Autoregulation of an E2 enzyme by ubiquitin-chain assembly on its catalytic residue. Nat Cell Biol 9: 422-427. (Pubitemid 46511075)
34. Ravid T, Hochstrasser M. 2008. Degradation signal diversity in the ubiquitin-proteasome system. Nat Rev Mol Cell Biol 9: 679-690.
35. Ravid T, Kreft SG, Hochstrasser M. 2006. Membrane and soluble substrates of the Doa10 ubiquitin ligase are degraded by distinct pathways. EMBO J 25: 533-543. (Pubitemid 43237660)
36. Schwienhorst I, Johnson ES, Dohmen RJ. 2000. SUMO conjugation and deconjugation. Mol Gen Genet 263: 771-786.
37. Song J, Durrin LK, Wilkinson TA, Krontiris TG, Chen Y. 2004. Identification of a SUMO-binding motif that recognizes SUMO-modified proteins. Proc Natl Acad Sci 101: 14373-14378. (Pubitemid 39346756)
38. Song J, Zhang Z, Hu W, Chen Y. 2005. Small ubiquitin-like modifier (SUMO) recognition of a SUMO binding motif: A reversal of the bound orientation. J Biol Chem 280: 40122-40129. (Pubitemid 41779147)
39. Sun H, Leverson JD, Hunter T. 2007. Conserved function of RNF4 family proteins in eukaryotes: Targeting a ubiquitin ligase to SUMOylated proteins. EMBO J 26: 4102-4112. (Pubitemid 47462098)
40. Swanson R, Locher M, Hochstrasser M. 2001. A conserved ubiquitin ligase of the nuclear envelope/endoplasmic reticulum that functions in both ER-associated and Matα2 repressor degradation. Genes & Dev 15: 2660-2674. (Pubitemid 32988877)
41. Tan S, Richmond TJ. 1998. Crystal structure of the yeast MATα2/MCM1/DNA ternary complex. Nature 391: 660-666. (Pubitemid 28113205)
42. Tatham MH, Geoffroy MC, Shen L, Plechanovova A, Hattersley N, Jaffray EG, Palvimo JJ, Hay RT. 2008. RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation. Nat Cell Biol 10: 538-546. (Pubitemid 351627373)
43. Uzunova K, Gottsche K, Miteva M, Weisshaar SR, Glanemann C, Schnellhardt M, Niessen M, Scheel H, Hofmann K, Johnson ES, et al. 2007. Ubiquitin-dependent proteolytic control of SUMO conjugates. J Biol Chem 282: 34167-34175. (Pubitemid 350159437)
44. Wang Z, Prelich G. 2009. Quality control of a transcriptional regulator by SUMO-targeted degradation. Mol Cell Biol 29: 1694-1706.
45. Wilcox AJ, Laney JD. 2009. A ubiquitin-selective AAA-ATPase mediates transcriptional switching by remodeling a repressor-promoter DNA complex. Nat Cell Biol 11: 1481-1486.
46. Xie Y, Kerscher O, Kroetz MB, McConchie HF, Sung P, Hochstrasser M. 2007. The yeast Hex3.Slx8 heterodimer is a ubiquitin ligase stimulated by substrate sumoylation. J Biol Chem 282: 34176-34184. (Pubitemid 350159438)
47. Yang L, Mullen JR, Brill SJ. 2006. Purification of the yeast Slx5-Slx8 protein complex and characterization of its DNA-binding activity. Nucleic Acids Res 34: 5541-5551. (Pubitemid 44742442)
48. Zhang C, Roberts TM, Yang J, Desai R, Brown GW. 2006. Suppression of genomic instability by SLX5 and SLX8 in Saccharomyces cerevisiae. DNA Repair (Amst) 5: 336-346. (Pubitemid 43247600)