Solution structure and activation mechanism of ubiquitin-like small archaeal modifier proteins

Journal of Molecular Biology

Volumn 405, Issue 4, 2011, Pages 1040-1055

  Ranjan, Namit ^a   Damberger, Fred F ^a   Sutter, Markus ^a   Allain, Frédéric H T ^a   Weber Ban, Eilika ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

adenylation; E1 like SAMP activator (ELSA); NMR; SAMP; ubiquitin

Indexed keywords

ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE; ARCHAEAL PROTEIN; BACTERIAL PROTEIN; PROTEIN MOAD; SMALL ARCHAEAL MODIFIER PROTEIN; SULFUR; UBIQUITIN; UNCLASSIFIED DRUG;

ADENYLATION; ARCHAEBACTERIUM; ARTICLE; BETA SHEET; CARBOXY TERMINAL SEQUENCE; ELECTROSPRAY MASS SPECTROMETRY; HYDROPHOBICITY; METHANOSARCINA; METHANOSARCINA ACETIVORANS; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN STRUCTURE; SEQUENCE HOMOLOGY;

ARCHAEA; BACTERIA (MICROORGANISMS); EUKARYOTA; METHANOSARCINA ACETIVORANS;

EID: 79251595632     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.11.040     Document Type: Article

References (65)

1. Hershko A., and Ciechanover A. Mechanisms of intracellular protein breakdown Annu. Rev. Biochem. 51 1982 335 364
2. Hochstrasser M. Evolution and function of ubiquitin-like protein-conjugation systems Nat. Cell Biol. 2 2000 E153 E157
3. Hochstrasser M. Origin and function of ubiquitin-like proteins Nature 458 2009 422 429
4. Pickart C.M., and Fushman D. Polyubiquitin chains: polymeric protein signals Curr. Opin. Chem. Biol. 8 2004 610 616
5. Passmore L.A., and Barford D. Getting into position: the catalytic mechanisms of protein ubiquitylation Biochem. J. 379 2004 513 525
6. Schulman B.A., and Harper J.W. Ubiquitin-like protein activation by E1 enzymes: the apex for downstream signalling pathways Nat. Rev., Mol. Cell Biol. 10 2009 319 331
7. Robinson P.A., and Ardley H.C. Ubiquitin-protein ligases J. Cell Sci. 117 2004 5191 5194
8. Welchman R.L., Gordon C., and Mayer R.J. Ubiquitin and ubiquitin-like proteins as multifunctional signals Nat. Rev., Mol. Cell Biol. 6 2005 599 609
9. Lake M.W., Wuebbens M.M., Rajagopalan K.V., and Schindelin H. Mechanism of ubiquitin activation revealed by the structure of a bacterial MoeB-MoaD complex Nature 414 2001 325 329
10. Rudolph M.J., Wuebbens M.M., Rajagopalan K.V., and Schindelin H. Crystal structure of molybdopterin synthase and its evolutionary relationship to ubiquitin activation Nat. Struct. Biol. 8 2001 42 46
11. Schmitz J., Wuebbens M.M., Rajagopalan K.V., and Leimkuhler S. Role of the C-terminal Gly-Gly motif of Escherichia coli MoaD, a molybdenum cofactor biosynthesis protein with a ubiquitin fold Biochemistry 46 2007 909 916
12. Zhang W., Urban A., Mihara H., Leimkuhler S., Kurihara T., and Esaki N. IscS functions as a primary sulfur-donating enzyme by interacting specifically with MoeB and MoaD in the biosynthesis of molybdopterin in Escherichia coli J. Biol. Chem. 285 2010 2302 2308
13. Begley T.P., Xi J., Kinsland C., Taylor S., and McLafferty F. The enzymology of sulfur activation during thiamin and biotin biosynthesis Curr. Opin. Chem. Biol. 3 1999 623 629
14. Duda D.M., Walden H., Sfondouris J., and Schulman B.A. Structural analysis of Escherichia coli ThiF J. Mol. Biol. 349 2005 774 786
15. Lehmann C., Begley T.P., and Ealick S.E. Structure of the Escherichia coli ThiS-ThiF complex, a key component of the sulfur transfer system in thiamin biosynthesis Biochemistry 45 2006 11 19
16. Leonardi R., and Roach P.L. Thiamine biosynthesis in Escherichia coli: in vitro reconstitution of the thiazole synthase activity J. Biol. Chem. 279 2004 17054 17062
17. Wang C., Xi J., Begley T.P., and Nicholson L.K. Solution structure of ThiS and implications for the evolutionary roots of ubiquitin Nat. Struct. Biol. 8 2001 47 51
18. Leidel S., Pedrioli P.G., Bucher T., Brost R., Costanzo M., and Schmidt A. Ubiquitin-related modifier Urm1 acts as a sulphur carrier in thiolation of eukaryotic transfer RNA Nature 458 2009 228 232
19. Pedrioli P.G., Leidel S., and Hofmann K. Urm1 at the crossroad of modifications. 'Protein Modifications: Beyond the Usual Suspects' Review Series EMBO Rep. 9 2008 1196 1202
20. Schmitz J., Chowdhury M.M., Hanzelmann P., Nimtz M., Lee E.Y., Schindelin H., and Leimkuhler S. The sulfurtransferase activity of Uba4 presents a link between ubiquitin-like protein conjugation and activation of sulfur carrier proteins Biochemistry 47 2008 6479 6489
21. Xu J., Zhang J., Wang L., Zhou J., Huang H., and Wu J. Solution structure of Urm1 and its implications for the origin of protein modifiers Proc. Natl Acad. Sci. USA 103 2006 11625 11630
22. Burroughs A.M., Balaji S., Iyer L.M., and Aravind L. Small but versatile: the extraordinary functional and structural diversity of the beta-grasp fold Biol. Direct 2 2007 18
23. Burroughs A.M., Iyer L.M., and Aravind L. Natural history of the E1-like superfamily: implication for adenylation, sulfur transfer, and ubiquitin conjugation Proteins 75 2009 895 910
24. Iyer L.M., Burroughs A.M., and Aravind L. The prokaryotic antecedents of the ubiquitin-signaling system and the early evolution of ubiquitin-like beta-grasp domains Genome Biol. 7 2006 R60
25. Burns K.E., Liu W.T., Boshoff H.I., Dorrestein P.C., and Barry C.E. III Proteasomal protein degradation in Mycobacteria is dependent upon a prokaryotic ubiquitin-like protein J. Biol. Chem. 284 2009 3069 3075
26. Pearce M.J., Mintseris J., Ferreyra J., Gygi S.P., and Darwin K.H. Ubiquitin-like protein involved in the proteasome pathway of Mycobacterium tuberculosis Science 322 2008 1104 1107
27. Chen X., Solomon W.C., Kang Y., Cerda-Maira F., Darwin K.H., and Walters K.J. Prokaryotic ubiquitin-like protein pup is intrinsically disordered J. Mol. Biol. 392 2009 208 217
28. Liao S., Shang Q., Zhang X., Zhang J., Xu C., and Tu X. Pup, a prokaryotic ubiquitin-like protein, is an intrinsically disordered protein Biochem. J. 422 2009 207 215
29. Sutter M., Striebel F., Damberger F.F., Allain F.H., and Weber-Ban E. A distinct structural region of the prokaryotic ubiquitin-like protein (Pup) is recognized by the N-terminal domain of the proteasomal ATPase Mpa FEBS Lett. 583 2009 3151 3157
30. Striebel F., Imkamp F., Sutter M., Steiner M., Mamedov A., and Weber-Ban E. Bacterial ubiquitin-like modifier Pup is deamidated and conjugated to substrates by distinct but homologous enzymes Nat. Struct. Mol. Biol. 16 2009 647 651
31. Sutter M., Damberger F.F., Imkamp F., Allain F.H., and Weber-Ban E. Prokaryotic ubiquitin-like protein (Pup) is coupled to substrates via the side chain of its C-terminal glutamate J. Am. Chem. Soc. 132 2010 5610 5612
32. Humbard M.A., Miranda H.V., Lim J.M., Krause D.J., Pritz J.R., and Zhou G. Ubiquitin-like small archaeal modifier proteins (SAMPs) in Haloferax volcanii Nature 463 2010 54 60
33. 15N random coil NMR chemical shifts of the common amino acids. I. Investigations of nearest-neighbor effects J. Biomol. NMR 5 1995 67 81
34. Hiller S., Fiorito F., Wüthrich K., and Wider G. Automated projection spectroscopy (APSY) Proc. Natl Acad. Sci. USA 102 2005 10876 10881
35. Volk J., Herrmann T., and Wüthrich K. Automated sequence-specific protein NMR assignment using the memetic algorithm MATCH J. Biomol. NMR 41 2008 127 138
36. 13C chemical shift statistics J. Biomol. NMR 24 2002 149 154
37. Wüthrich K. NMR of Proteins and Nucleic Acids 1986 John Wiley & Sons New York, NY
38. 13C NMR chemical shifts can predict disulfide bond formation J. Biomol. NMR 18 2000 165 171
39. Herrmann T., Güntert P., and Wüthrich K. Protein NMR structure determination with automated NOE-identification in the NOESY spectra using the new software ATNOS J. Biomol. NMR 24 2002 171 189
40. Herrmann T., Güntert P., and Wüthrich K. Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA J. Mol. Biol. 319 2002 209 227
41. Güntert P., Mumenthaler C., and Wüthrich K. Torsion angle dynamics for NMR structure calculation with the new program DYANA J. Mol. Biol. 273 1997 283 298
42. Case, D. A., Darden, T. A., Cheatham, T. E., III, Simmerling, C. L., Wang, J., Duke, R. E. et al. (2006). AMBER 9, University of California, San Francisco, CA.
43. Koradi R., Billeter M., and Wüthrich K. MOLMOL: a program for display and analysis of macromolecular structures J. Mol. Graphicsics 14 1996 51 55
44. Laskowski R.A., MacArthur M.W., Moss D.S., and Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures J. Appl. Crystallogr. allogr. 26 1993 283 291
45. Dietmann S., Park J., Notredame C., Heger A., Lappe M., and Holm L. A fully automatic evolutionary classification of protein folds: Dali Domain Dictionary version 3 Nucleic Acids Res. 29 2001 55 57
46. Holm L., and Sander C. Protein structure comparison by alignment of distance matrices J. Mol. Biol. 233 1993 123 138
47. Guth E., Thommen M., and Weber-Ban E. Mycobacterial ubiquitin-like protein ligase PafA follows a two-step reaction pathway with a phosphorylated Pup intermediate J. Biol. Chem. 2010 Electronic publication ahead of print
48. Walsh C.T. Posttranslational Modification of Proteins: Expanding Nature's Inventory 2006 Roberts and Company Greenwood, CO
49. Wickliffe K., Williamson A., Jin L., and Rape M. The multiple layers of ubiquitin-dependent cell cycle control Chem. Rev. 109 2009 1537 1548
50. Morris J.R. More modifiers move on DNA damage Cancer Res. 70 2010 3861 3863
51. Thomson T.M., and Guerra-Rebollo M. Ubiquitin and SUMO signalling in DNA repair Biochem. Soc. Trans. 38 2010 116 131
52. Wilkinson K.A., and Henley J.M. Mechanisms, regulation and consequences of protein SUMOylation Biochem. J. 428 2010 133 145
53. Parry G., and Estelle M. Regulation of cullin-based ubiquitin ligases by the Nedd8/RUB ubiquitin-like proteins Semin. Cell Dev. Biol. 15 2004 221 229
54. Xirodimas D.P. Novel substrates and functions for the ubiquitin-like molecule NEDD8 Biochem. Soc. Trans. 36 2008 802 806
55. Daniels J.N., Wuebbens M.M., Rajagopalan K.V., and Schindelin H. Crystal structure of a molybdopterin synthase-precursor Z complex: insight into its sulfur transfer mechanism and its role in molybdenum cofactor deficiency Biochemistry 47 2008 615 626
56. Outten F.W., Wood M.J., Munoz F.M., and Storz G. The SufE protein and the SufBCD complex enhance SufS cysteine desulfurase activity as part of a sulfur transfer pathway for Fe-S cluster assembly in Escherichia coli J. Biol. Chem. 278 2003 45713 45719
57. Winget J.M., and Mayor T. The diversity of ubiquitin recognition: hot spots and varied specificity Mol. Cell 38 2010 627 635
58. Hecker C.M., Rabiller M., Haglund K., Bayer P., and Dikic I. Specification of SUMO1- and SUMO2-interacting motifs J. Biol. Chem. 281 2006 16117 16127
59. Talluri S., and Wagner G. An optimized 3D NOESY-HSQC J. Magn. Reson., Ser. B 112 1996 200 205
60. Hiller S., Joss R., and Wider G. Automated NMR assignment of protein side chain resonances using automated projection spectroscopy (APSY) J. Am. Chem. Soc. 130 2008 12073 12079
61. 13C-labeled proteins via scalar couplings J. Am. Chem. Soc. 115 1993 11054 11055
62. 1H]-NOE experiment J. Biomol. NMR 23 2002 23 33
63. Grzesiek S., and Bax A. The importance of not saturating water in protein NMR. Application to sensitivity enhancement and NOE measurements J. Am. Chem. Soc. 115 1993 12593 12594
64. Bai Y., Milne J.S., Mayne L., and Englander S.W. Primary structure effects on peptide group hydrogen exchange Proteins 17 1993 75 86
65. Keller R. The Computer-Aided Resonance Assignment Tutorial CARA 2004 Cantina Verlag Goldau, Switzerland