NMR characterization of foldedness for the production of E3 RING domains

Journal of Structural Biology

Volumn 172, Issue 1, 2010, Pages 120-127

  Huang, Anding ^a   de Jong, Rob N ^a   Folkers, Gert E ^a   Boelens, Rolf ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Imidazole; NMR; Protein purification; RING E3; Zinc finger

Indexed keywords

IMIDAZOLE; UBIQUITIN PROTEIN LIGASE E3; ZINC FINGER PROTEIN;

AFFINITY CHROMATOGRAPHY; ARTICLE; HETERONUCLEAR SINGLE QUANTUM COHERENCE; IMMOBILIZED METAL AFFINITY CHROMATOGRAPHY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PURIFICATION; PROTEIN STRUCTURE; PROTON TRANSPORT; SOLUBILITY; ZINC FINGER MOTIF;

CHROMATOGRAPHY, AFFINITY; CYSTEINE; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GLUTATHIONE TRANSFERASE; HISTIDINE; HUMANS; IMIDAZOLES; MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN FOLDING; PROTEIN STABILITY; RECOMBINANT FUSION PROTEINS; RING FINGER DOMAINS; SOLUBILITY; UBIQUITIN-PROTEIN LIGASES; ZINC;

EID: 77956191339     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2010.07.014     Document Type: Article

References (59)

1. Aravind L., Koonin E.V. The U box is a modified RING finger - a common domain in ubiquitination. Curr. Biol. 2000, 10:R132-R134.
2. Bagby S., Tong K.I., Liu D., Alattia J.R., Ikura M. The button test: a small scale method using microdialysis cells for assessing protein solubility at concentrations suitable for NMR. J. Biomol. NMR 1997, 10:279-282.
3. Borden K.L., Freemont P.S. The RING finger domain: a recent example of a sequence-structure family. Curr. Opin. Struct. Biol. 1996, 6:395-401.
4. Brzovic P.S., Klevit R.E. Ubiquitin transfer from the E2 perspective: why is UbcH5 so promiscuous?. Cell Cycle 2006, 5:2867-2873.
5. Cavanagh, J., Fairbrother, W.J., Palmer III A.G., Skelton, N.J., Rance, M., 2007. Protein NMR Spectroscopy, second ed. Principles and Practice.
6. Christensen D.E., Brzovic P.S., Klevit R.E. E2-BRCA1 RING interactions dictate synthesis of mono or specific polyubiquitin chain linkages. Nat. Struct. Mol. Biol. 2007, 14:941-948.
7. de Jong R.N., Daniels M.A., Kaptein R., Folkers G.E. Enzyme free cloning for high throughput gene cloning and expression. J. Struct. Funct. Genomics 2006, 7:109-118.
8. Deshaies R.J., Joazeiro C.A. RING domain E3 ubiquitin ligases. Ann. Rev. Biochem. 2009, 78:399-434.
9. Edsall J.T., Felsenfeld G., Goodman D.S., Gurd F.R.N. The association of imidazole with the ions of zinc and cupric copper. J. Am. Chem. Soc. 1954, 76(11):3054-3061.
10. Ericsson U.B., Hallberg B.M., Detitta G.T., Dekker N., Nordlund P. Thermofluor-based high-throughput stability optimization of proteins for structural studies. Anal. Biochem. 2006, 357:289-298.
11. Esposito D., Chatterjee D.K. Enhancement of soluble protein expression through the use of fusion tags. Curr. Opin. Biotechnol. 2006, 17:353-358.
12. Folkers G.E., van Buuren B.N., Kaptein R. Expression screening, protein purification and NMR analysis of human protein domains for structural genomics. J. Struct. Funct. Genomics 2004, 5:119-131.
13. Freemont P.S. The RING finger. A novel protein sequence motif related to the zinc finger. Ann. NY Acad. Sci. 1993, 684:174-192.
14. Galvao-Botton L.M., Katsuyama A.M., Guzzo C.R., Almeida F.C., Farah C.S., Valente A.P. High-throughput screening of structural proteomics targets using NMR. FEBS Lett. 2003, 552:207-213.
15. Golovanov A.P., Hautbergue G.M., Wilson S.A., Lian L.Y. A simple method for improving protein solubility and long-term stability. J. Am. Chem. Soc. 2004, 126:8933-8939.
16. Hammarstrom M., Hellgren N., van Den Berg S., Berglund H., Hard T. Rapid screening for improved solubility of small human proteins produced as fusion proteins in Escherichia coli. Protein Sci. 2002, 11:313-321.
17. Hammarstrom M., Woestenenk E.A., Hellgren N., Hard T., Berglund H. Effect of N-terminal solubility enhancing fusion proteins on yield of purified target protein. J. Struct. Funct. Genomics 2006, 7:1-14.
18. Hanzawa H., de Ruwe M.J., Albert T.K., van Der Vliet P.C., Timmers H.T., Boelens R. The structure of the C4C4 ring finger of human NOT4 reveals features distinct from those of C3HC4 RING fingers. J. Biol. Chem. 2001, 276:10185-10190.
19. Huang A., de Jong R.N., Wienk H., Winkler G.S., Timmers H.T., Boelens R. E2-c-Cbl recognition is necessary but not sufficient for ubiquitination activity. J. Mol. Biol. 2009, 385:507-519.
20. Huth J.R., Bewley C.A., Jackson B.M., Hinnebusch A.G., Clore G.M., Gronenborn A.M. Design of an expression system for detecting folded protein domains and mapping macromolecular interactions by NMR. Protein Sci. 1997, 6:2359-2364.
21. Jansson M., Li Y.C., Jendeberg L., Anderson S., Montelione B.T., Nilsson B. High-level production of uniformly 15N- and 13C-enriched fusion proteins in Escherichia coli. J. Biomol. NMR 1996, 7:131-141.
22. Jensen D.R., Woytovich C., Li M., Duvnjak P., Cassidy M.S., Frederick R.O., Bergeman L.F., Peterson F.C., Volkman B.F. Rapid, robotic, small-scale protein production for NMR screening and structure determination. Protein Sci. 2010, 19:570-578.
23. Joazeiro C.A., Wing S.S., Huang H., Leverson J.D., Hunter T., Liu Y.C. The tyrosine kinase negative regulator c-Cbl as a RING-type, E2-dependent ubiquitin-protein ligase. Science 1999, 286:309-312.
24. Kandias N.G., Chasapis C.T., Bentrop D., Episkopou V., Spyroulias G.A. High yield expression and NMR characterization of Arkadia E3 ubiquitin ligase RING-H2 finger domain. Biochem. Biophys. Res. Commun. 2009, 378:498-502.
25. Katoh S., Hong C., Tsunoda Y., Murata K., Takai R., Minami E., Yamazaki T., Katoh E. High precision NMR structure and function of the RING-H2 finger domain of EL5, a rice protein whose expression is increased upon exposure to pathogen-derived oligosaccharides. J. Biol. Chem. 2003, 278:15341-15348.
26. Kigawa T., Yabuki T., Matsuda N., Matsuda T., Nakajima R., Tanaka A., Yokoyama S. Preparation of Escherichia coli cell extract for highly productive cell-free protein expression. J. Struct. Funct. Genomics 2004, 5:63-68.
27. LaVallie E.R., DiBlasio E.A., Kovacic S., Grant K.L., Schendel P.F., McCoy J.M. A thioredoxin gene fusion expression system that circumvents inclusion body formation in the E. coli cytoplasm. Biotechnology (NY) 1993, 11:187-193.
28. Lepre C.A., Moore J.M. Microdrop screening: a rapid method to optimize solvent conditions for NMR spectroscopy of proteins. J. Biomol. NMR 1998, 12:493-499.
29. Lorick K.L., Jensen J.P., Weissman A.M. Expression, purification, and properties of the Ubc4/5 family of E2 enzymes. Methods Enzymol. 2005, 398:54-68.
30. Lovering R., Hanson I.M., Borden K.L., Martin S., O'Reilly N.J., Evan G.I., Rahman D., Pappin D.J., Trowsdale J., Freemont P.S. Identification and preliminary characterization of a protein motif related to the zinc finger. Proc. Natl. Acad. Sci. USA 1993, 90:2112-2116.
31. Makowski G.S., Sunderman F.W. The interactions of zinc, nickel, and cadmium with Xenopus transcription factor IIIA, assessed by equilibrium dialysis. J. Inorg. Biochem. 1992, 48:107-119.
32. Markson, G., Kiel, C., Hyde, A.R., Brown, S., Charalabous, P., Bremm, A., Semple, J., Woodsmith, J., Duley, S., Salehi-Ashtiani, K., Vidal, M., Komander, D., Serrano, L., Lehner, P., Sanderson, C., 2009. Analysis of the human E2 ubiquitin conjugating enzyme protein interaction network. Genome Res.
33. Montelione, G.T., Zheng, D., Huang, Y.J., Gunsalus, K.C., Szyperski, T., 2000. Protein NMR spectroscopy in structural genomics. Nat. Struct. Biol. 7 (Suppl.), 982-985.
34. Montelione G.T., Arrowsmith C., Girvin M.E., Kennedy M.A., Markley J.L., Powers R., Prestegard J.H., Szyperski T. Unique opportunities for NMR methods in structural genomics. J. Struct. Funct. Genomics 2009, 10:101-116.
35. Morita E.H., Sawasaki T., Tanaka R., Endo Y., Kohno T. A wheat germ cell-free system is a novel way to screen protein folding and function. Protein Sci. 2003, 12:1216-1221.
36. Newman R.H., Carpenter E., Freemont P.S., Blundell T.L., Parker P.J. Microcrystals of the beta 1 isoenzyme of protein kinase C: an electron microscopic study. Biochem. J. 1994, 298(Pt 2):391-393.
37. Nieba L., Nieba-Axmann S.E., Persson A., Hamalainen M., Edebratt F., Hansson A., Lidholm J., Magnusson K., Karlsson A.F., Pluckthun A. BIACORE analysis of histidine-tagged proteins using a chelating NTA sensor chip. Anal. Biochem. 1997, 252:217-228.
38. Notenboom V., Hibbert R.G., van Rossum-Fikkert S.E., Olsen J.V., Mann M., Sixma T.K. Functional characterization of Rad18 domains for Rad6, ubiquitin, DNA binding and PCNA modification. Nucleic Acids Res. 2007, 35:5819-5830.
39. Ohi M.D., Vander Kooi C.W., Rosenberg J.A., Chazin W.J., Gould K.L. Structural insights into the U-box, a domain associated with multi-ubiquitination. Nat. Struct. Biol. 2003, 10:250-255.
40. Page R., Peti W., Wilson I.A., Stevens R.C., Wuthrich K. NMR screening and crystal quality of bacterially expressed prokaryotic and eukaryotic proteins in a structural genomics pipeline. Proc. Natl. Acad. Sci. USA 2005, 102:1901-1905.
41. Peti W., Page R., Moy K., O'Neil-Johnson M., Wilson I.A., Stevens R.C., Wuthrich K. Towards miniaturization of a structural genomics pipeline using micro-expression and microcoil NMR. J. Struct. Funct. Genomics 2005, 6:259-267.
42. Rehm T., Huber R., Holak T.A. Application of NMR in structural proteomics: screening for proteins amenable to structural analysis. Structure 2002, 10:1613-1618.
43. Reich S., Puckey L.H., Cheetham C.L., Harris R., Ali A.A., Bhattacharyya U., Maclagan K., Powell K.A., Prodromou C., Pearl L.H., Driscoll P.C., Savva R. Combinatorial domain hunting: an effective approach for the identification of soluble protein domains adaptable to high-throughput applications. Protein Sci. 2006, 15:2356-2365.
44. Rossi P., Swapna G.V., Huang Y.J., Aramini J.M., Anklin C., Conover K., Hamilton K., Xiao R., Acton T.B., Ertekin A., Everett J.K., Montelione G.T. A microscale protein NMR sample screening pipeline. J. Biomol. NMR 2010, 46:11-22.
45. Smith D.B., Johnson K.S. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene 1988, 67:31-40.
46. Sobhanifar S., Reckel S., Junge F., Schwarz D., Kai L., Karbyshev M., Lohr F., Bernhard F., Dotsch V. Cell-free expression and stable isotope labelling strategies for membrane proteins. J. Biomol. NMR 2010, 46:33-43.
47. Sundberg, R.J., Martin, R.B., 1974. Interactions of histidine and other imidazole derivatives with transition metal ions in chemical and biological systems. Chem. Rev. 74 (4).
48. van Wijk S.J., de Vries S.J., Kemmeren P., Huang A., Boelens R., Bonvin A.M., Timmers H.T. A comprehensive framework of E2-RING E3 interactions of the human ubiquitin-proteasome system. Mol. Syst. Biol. 2009, 5:295.
49. Vinarov D.A., Lytle B.L., Peterson F.C., Tyler E.M., Volkman B.F., Markley J.L. Cell-free protein production and labeling protocol for NMR-based structural proteomics. Nat. Methods 2004, 1:149-153.
50. Wishart D.S., Sykes B.D. Chemical shifts as a tool for structure determination. Methods Enzymol. 1994, 239:363-392.
51. Woestenenk E.A., Hammarstrom M., Hard T., Berglund H. Screening methods to determine biophysical properties of proteins in structural genomics. Anal. Biochem. 2003, 318:71-79.
52. Woestenenk E.A., Hammarstrom M., van den Berg S., Hard T., Berglund H. His tag effect on solubility of human proteins produced in Escherichia coli: a comparison between four expression vectors. J. Struct. Funct. Genomics 2004, 5:217-229.
53. Wüthrich K. NMR of Proteins and Nucleic Acids 1986, Wiley, New York.
54. Yee A., Pardee K., Christendat D., Savchenko A., Edwards A.M., Arrowsmith C.H. Structural proteomics: toward high-throughput structural biology as a tool in functional genomics. Acc. Chem. Res. 2003, 36:183-189.
55. Yee A., Chang X., Pineda-Lucena A., Wu B., Semesi A., Le B., Ramelot T., Lee G.M., Bhattacharyya S., Gutierrez P., Denisov A., Lee C.H., Cort J.R., Kozlov G., Liao J., Finak G., Chen L., Wishart D., Lee W., McIntosh L.P., Gehring K., Kennedy M.A., Edwards A.M., Arrowsmith C.H. An NMR approach to structural proteomics. Proc. Natl. Acad. Sci. USA 2002, 99:1825-1830.
56. Yokoyama S. Protein expression systems for structural genomics and proteomics. Curr. Opin. Chem. Biol. 2003, 7:39-43.
57. Zhang Q., Horst R., Geralt M., Ma X., Hong W.X., Finn M.G., Stevens R.C., Wuthrich K. Microscale NMR screening of new detergents for membrane protein structural biology. J. Am. Chem. Soc. 2008, 130:7357-7363.
58. Zhou P., Wagner G. Overcoming the solubility limit with solubility-enhancement tags: successful applications in biomolecular NMR studies. J. Biomol. NMR 2010, 46:23-31.
59. Zhou P., Lugovskoy A.A., Wagner G. A solubility-enhancement tag (SET) for NMR studies of poorly behaving proteins. J. Biomol. NMR 2001, 20:11-14.