Role of the ubiquitin-like protein Urm1 as a noncanonical lysine-directed protein modifier

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 5, 2011, Pages 1763-1770

  Van Der Veen, Annemarthe G ^a   Schorpp, Kenji ^b   Schlieker, Christian ^a,e   Buti, Ludovico ^a,c   Damon, Jadyn R ^a,d   Spooner, Eric ^a   Ploegh, Hidde L ^a,d   Jentsch, Stefan ^b  

^a WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^c NOVARTIS VACCINES AND DIAGNOSTICS   (Italy)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^e YALE UNIVERSITY   (United States)

Author keywords

Hydrogen peroxide; Nuclear transport; Posttranslational modification; Uba4; USP15

Indexed keywords

DIAMIDE; LYSINE; PEROXIREDOXIN; PROTEIN URM1; UBIQUITIN; UNCLASSIFIED DRUG;

ARTICLE; CELL DEATH; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEOMICS; SACCHAROMYCES CEREVISIAE;

CHROMATOGRAPHY, LIQUID; DIAMIDE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; HUMANS; LYSINE; OXIDATIVE STRESS; PROTEOMICS; SACCHAROMYCES CEREVISIAE PROTEINS; TANDEM MASS SPECTROMETRY; UBIQUITINATION; UBIQUITINS;

EUKARYOTA; MAMMALIA; PROKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 79952142375     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1014402108     Document Type: Article

References (40)

1. Furukawa K, Mizushima N, Noda T, Ohsumi Y (2000) A protein conjugation system in yeast with homology to biosynthetic enzyme reaction of prokaryotes. J Biol Chem 275:7462-7465. (Pubitemid 30159639)
2. Xu J, et al. (2006) Solution structure of Urm1 and its implications for the origin of protein modifiers. Proc Natl Acad Sci USA 103:11625-11630. (Pubitemid 44182502)
3. Singh S, et al. (2005) Three-dimensional structure of the AAH26994.1 protein from Mus musculus, a putative eukaryotic Urm1. Protein Sci 14:2095-2102. (Pubitemid 41132375)
4. Hochstrasser M (2009) Origin and function of ubiquitin-like proteins. Nature 458: 422-429.
5. Schulman BA, Harper JW (2009) Ubiquitin-like protein activation by E1 enzymes: The apex for downstream signalling pathways. Nat Rev Mol Cell Biol 10:319-331.
6. Varshavsky A (2005) Regulated protein degradation. Trends Biochem Sci 30:283-286.
7. Iyer LM, Burroughs AM, Aravind L (2006) The prokaryotic antecedents of the ubiquitin-signaling system and the early evolution of ubiquitin-like beta-grasp domains. Genome Biol 7:R60.1-R60.23.
8. Kessler D (2006) Enzymatic activation of sulfur for incorporation into biomolecules in prokaryotes. FEMS Microbiol Rev 30:825-840.
9. Schlieker CD, Van der Veen AG, Damon JR, Spooner E, Ploegh HL (2008) A functional proteomics approach links the ubiquitin-related modifier Urm1 to a tRNA modification pathway. Proc Natl Acad Sci USA 105:18255-18260.
10. Noma A, Sakaguchi Y, Suzuki T (2009) Mechanistic characterization of the sulfur-relay system for eukaryotic 2-thiouridine biogenesis at tRNA wobble positions. Nucleic Acids Res 37:1335-1352.
11. Nakai Y, Nakai M, Hayashi H (2008) Thio-modification of yeast cytosolic tRNA requires a ubiquitin-related system that resembles bacterial sulfur transfer systems. J Biol Chem 283:27469-27476.
12. Leidel S, et al. (2009) Ubiquitin-related modifier Urm1 acts as a sulphur carrier in thiolation of eukaryotic transfer RNA. Nature 458:228-232.
13. Pedrioli PG, Leidel S, Hofmann K (2008) Urm1 at the crossroad of modifications. 'Protein Modifications: Beyond the Usual Suspects' Review Series. EMBO Rep 9:1196-1202.
14. Marelja Z, Stöcklein W, Nimtz M, Leimkühler S (2008) A novel role for human Nfs1 in the cytoplasm: Nfs1 acts as a sulfur donor for MOCS3, a protein involved in molybdenum cofactor biosynthesis. J Biol Chem 283:25178-25185.
15. Schmitz J, et al. (2008) The sulfurtransferase activity of Uba4 presents a link between ubiquitin-like protein conjugation and activation of sulfur carrier proteins. Biochemistry 47:6479-6489. (Pubitemid 351874239)
16. Huang B, Lu J, Byström AS (2008) A genome-wide screen identifies genes required for formation of the wobble nucleoside 5-methoxycarbonylmethyl-2- thiouridine in Saccharomyces cerevisiae. RNA 14:2183-2194.
17. Dewez M, et al. (2008) The conserved Wobble uridine tRNA thiolase Ctu1-Ctu2 is required to maintain genome integrity. Proc Natl Acad Sci USA 105:5459-5464. (Pubitemid 351753885)
18. Björk GR, Huang B, Persson OP, Byström AS (2007) A conserved modified wobble nucleoside (mcm5s2U) in lysyl-tRNA is required for viability in yeast. RNA 13:1245-1255.
19. Goehring AS, Rivers DM, Sprague GF, Jr. (2003) Urmylation: A ubiquitin-like pathway that functions during invasive growth and budding in yeast. Mol Biol Cell 14:4329-4341. (Pubitemid 37444637)
20. Goehring AS, Rivers DM, Sprague GF, Jr. (2003) Attachment of the ubiquitin-related protein Urm1p to the antioxidant protein Ahp1p. Eukaryot Cell 2:930-936. (Pubitemid 37298706)
21. Rubio-Texeira M (2007) Urmylation controls Nil1p and Gln3p-dependent expression of nitrogen-catabolite repressed genes in Saccharomyces cerevisiae. FEBS Lett 581:541-550.
22. Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408:239-247.
23. Veal EA, Day AM, Morgan BA (2007) Hydrogen peroxide sensing and signaling. Mol Cell 26:1-14. (Pubitemid 46578115)
24. Igloi GL (1988) Interaction of tRNAs and of phosphorothioate-substituted nucleic acids with an organomercurial. Probing the chemical environment of thiolated residues by affinity electrophoresis. Biochemistry 27:3842-3849.
25. Tortorella D, et al. (1998) Dislocation of type I membrane proteins from the ER to the cytosol is sensitive to changes in redox potential. J Cell Biol 142:365-376. (Pubitemid 28361545)
26. Kinsland C, Taylor SV, Kelleher NL, McLafferty FW, Begley TP (1998) Overexpression of recombinant proteins with a C-terminal thiocarboxylate: Implications for protein semisynthesis and thiamin biosynthesis. Protein Sci 7:1839-1842. (Pubitemid 29133191)
27. Stewart M (2007) Molecular mechanism of the nuclear protein import cycle. Nat Rev Mol Cell Biol 8:195-208.
28. Kutay U, Bischoff FR, Kostka S, Kraft R, Görlich D (1997) Export of importin alpha from the nucleus is mediated by a specific nuclear transport factor. Cell 90:1061-1071. (Pubitemid 27408520)
29. Behrens P, Brinkmann U, Wellmann A (2003) CSE1L/CAS: Its role in proliferation and apoptosis. Apoptosis 8:39-44. (Pubitemid 36133136)
30. Kim HE, Jiang X, Du F, Wang X (2008) PHAPI, CAS, and Hsp70 promote apoptosome formation by preventing Apaf-1 aggregation and enhancing nucleotide exchange on Apaf-1. Mol Cell 30:239-247.
31. Tanaka T, Ohkubo S, Tatsuno I, Prives C (2007) hCAS/CSE1L associates with chromatin and regulates expression of select p53 target genes. Cell 130:638-650. (Pubitemid 47268061)
32. Agris PF, Vendeix FA, Graham WD (2007) tRNA's wobble decoding of the genome: 40 years of modification. J Mol Biol 366:1-13. (Pubitemid 46123342)
33. Chen C, Tuck S, Byström AS (2009) Defects in tRNA modification associated with neurological and developmental dysfunctions in Caenorhabditis elegans elongator mutants. PLoS Genet 5:e1000561.
34. Netzer N, et al. (2009) Innate immune and chemically triggered oxidative stress modifies translational fidelity. Nature 462:522-526.
35. Ling J, Söll D (2010) Severe oxidative stress induces protein mistranslation through impairment of an aminoacyl-tRNA synthetase editing site. Proc Natl Acad Sci USA 107:4028-4033.
36. Humbard MA, et al. (2010) Ubiquitin-like small archaeal modifier proteins (SAMPs) in Haloferax volcanii. Nature 463:54-60.
37. Dalle-Donne I, Rossi R, Colombo G, Giustarini D, Milzani A (2009) Protein Sglutathionylation: A regulatory device from bacteria to humans. Trends Biochem Sci 34:85-96.
38. Bossis G, Melchior F (2006) Regulation of SUMOylation by reversible oxidation of SUMO conjugating enzymes. Mol Cell 21:349-357. (Pubitemid 43163530)
39. Kodiha M, Tran D, Morogan A, Qian C, Stochaj U (2009) Dissecting the signaling events that impact classical nuclear import and target nuclear transport factors. PLoS ONE 4:e8420.
40. Ogryzko VV, Brinkmann E, Howard BH, Pastan I, Brinkmann U (1997) Antisense inhibition of CAS, the human homologue of the yeast chromosome segregation gene CSE1, interferes with mitosis in HeLa cells. Biochemistry 36:9493-9500. (Pubitemid 27346989)