Backbone dynamics and global effects of an activating mutation in minimized Mtu RecA inteins

Journal of Molecular Biology

Volumn 400, Issue 4, 2010, Pages 755-767

  Du, Zhenming ^a   Liu, Yangzhong ^b   Ban, David ^a   Lopez, Maria M ^c   Belfort, Marlene ^d   Wang, Chunyu ^a,c  

^a RENSSELAER POLYTECHNIC INSTITUTE   (United States)

^b UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^c RENSSELAER POLYTECHNIC INSTITUTE   (United States)

^d WADSWORTH CENTER   (United States)

Author keywords

Chemical exchange; Hydrogen exchange; Intein; Protein dynamics; Protein splicing

Indexed keywords

ASPARAGINE; HISTIDINE; INTEIN; NITROGEN 15; RECA PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; DEUTERIUM HYDROGEN EXCHANGE; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN PROCESSING; PROTEIN STABILITY; PROTON NUCLEAR MAGNETIC RESONANCE;

MYCOBACTERIUM TUBERCULOSIS;

EID: 77954386029     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.05.044     Document Type: Article

References (50)

1. Paulus H. Protein splicing and related forms of protein autoprocessing. Annu. Rev. Biochem. 2000, 69:447-496.
2. Kwon Y., Coleman M.A., Camarero J.A. Selective immobilization of proteins onto solid supports through split-intein-mediated protein trans-splicing. Angew. Chem. Int. Ed. 2006, 118:1758-1761.
3. Seyedsayamdost M.R., Yee C.S., Reece S.Y., Nocera D.G., Stubbe J. pH rate profiles of FnY356-R2s (n=2, 3, 4) in Escherichia coli ribonucleotide reductase: evidence that Y356 is a redox-active amino acid along the radical propagation pathway. J. Am. Chem. Soc. 2006, 128:1562-1568.
4. Evans T.C., Benner J., Xu M.-Q. The cyclization and polymerization of bacterially expressed proteins using modified self-splicing inteins. J. Biol. Chem. 1999, 274:18359-18363.
5. Zueger S., Iwai H. Intein-based biosynthetic incorporation of unlabeled protein tags into isotopically labeled proteins for NMR studies. Nat. Biotechnol. 2005, 23:736-740.
6. Romanelli A., Shekhtman A., Cowburn D., Muir T.W. Semisynthesis of a segmental isotopically labeled protein splicing precursor: NMR evidence for an unusual peptide bond at the N-extein-intein junction. Proc. Natl Acad. Sci. USA 2004, 101:6397-6402.
7. Paulus H. Protein splicing inhibitors as a new class of antimycobacterial agents. Drugs Future 2007, 32:973-984.
8. Wood D.W., Wu W., Belfort G., Derbyshire V., Belfort M. A genetic system yields self-cleaving inteins for bioseparations. Nat. Biotechnol. 1999, 17:889-892.
9. Derbyshire V., Wood D.W., Wu W., Dansereau J.T., Dalgaard J.Z., Belfort M. Genetic definition of a protein-splicing domain: functional mini-inteins support structure predictions and a model for intein evolution. Proc. Natl Acad. Sci. USA 1997, 94:11466-11471.
10. Hiraga K., Derbyshire V., Dansereau J.T., Van Roey P., Belfort M. Minimization and stabilization of the Mycobacterium tuberculosis recA intein. J. Mol. Biol. 2005, 354:916-926.
11. Shemella P., Pereira B., Zhang Y., Van Roey P., Belfort G., Garde S., Nayak S.K. Mechanism for intein C-terminal cleavage: a proposal from quantum mechanical calculations. Biophys. J. 2007, 92:847-853.
12. Van Roey P., Pereira B., Li Z., Hiraga K., Belfort M., Derbyshire V. Crystallographic and mutational studies of Mycobacterium tuberculosis recA mini-inteins suggest a pivotal role for a highly conserved aspartate residue. J. Mol. Biol. 2007, 367:162-173.
13. 15N NMR assignments of an engineered intein based on Mycobacterium tuberculosis RecA. Biomol. NMR Assign. 2008, 2:111-113.
14. a shift mechanism. J. Am. Chem. Soc. 2009, 131:11581-11589.
15. Buskirk A.R., Ong Y.-C., Gartner Z.J., Liu D.R. Directed evolution of ligand dependence: small-molecule-activated protein splicing. Proc. Natl Acad. Sci. USA 2004, 101:10505-10510.
16. Pereira B., Jain S., Garde S. Quantifying the protein core flexibility through analysis of cavity formation. J. Chem. Phys. 2006, 124:74704.
17. 19F NMR studies. J. Mol. Biol. 2005, 345:599-610.
18. Perler F.B. InBase: the Intein Database. Nucleic Acids Res. 2002, 30:383-384.
19. Heinamaki K., Oeemig J.S., Djupsjobacka J., Iwai H. NMR resonance assignment of DnaE intein from Nostoc punctiforme. Biomol. NMR Assign. 2009, 3:41-43.
20. Hiraga K., Soga I., Dansereau J.T., Pereira B., Derbyshire V., Du Z., et al. Selection and structure of hyperactive inteins: peripheral changes relayed to the catalytic center. J. Mol. Biol. 2009, 393:1106-1117.
21. Johnson M.A., Southworth M.W., Herrmann T., Brace L., Perler F.B., Wuthrich K. NMR structure of a KlbA intein precursor from Methanococcus jannaschii. Protein Sci. 2007, 16:1316-1328.
22. Oeemig J.S., Aranko A.S., Djupsjobacka J., Heinamaki K., Iwai H. Solution structure of DnaE intein from Nostoc punctiforme: structural basis for the design of a new split intein suitable for site-specific chemical modification. FEBS Lett. 2009, 583:1451-1456.
23. Palmer A.G. NMR probes of molecular dynamics: overview and comparison with other techniques. Annu. Rev. Biophys. Biomol. Struct. 2001, 30:129-155.
24. Goodman J.L., Pagel M.D., Stone M.J. Relationships between protein structure and dynamics from a database of NMR-derived backbone order parameters. J. Mol. Biol. 2000, 295:963-978.
25. De Alba E., Baber J.L., Tjandra N. The use of residual dipolar coupling in concert with backbone relaxation rates to identify conformational exchange by NMR. J. Am. Chem. Soc. 1999, 121:4282-4283.
26. Carr H.Y., Purcell E.M. Effects of diffusion on free precession in nuclear magnetic resonance experiments. Phys. Rev. 1954, 94:630-638.
27. Meiboom S., Gill D. Modified spin-echo method for measuring nuclear relaxation times. Rev. Sci. Instrum. 1958, 29:688-691.
28. Wagner G., Pardi A., Wuethrich K. Hydrogen bond length and proton NMR chemical shifts in proteins. J. Am. Chem. Soc. 1983, 105:5948-5949.
29. Goodey N.M., Benkovic S.J. Allosteric regulation and catalysis emerge via a common route. Nat. Chem. Biol. 2008, 4:474-482.
30. Lockless S.W., Muir T.W. Traceless protein splicing utilizing evolved split inteins. Proc. Natl Acad. Sci. USA 2009, 106:10999-11004.
31. Hvidt A., Nielsen S.O. Hydrogen exchange in proteins. Adv. Protein Chem. 1966, 21:287-386.
32. Russell B.S., Zhong L., Bigotti M.G., Cutruzzola F., Bren K.L. Backbone dynamics and hydrogen exchange of Pseudomonas aeruginosa ferricytochrome c551. J. Biol. Inorg. Chem. 2003, 8:156-166.
33. Savard P.Y., Gagne S.M. Backbone dynamics of TEM-1 determined by NMR: evidence for a highly ordered protein. Biochemistry 2006, 45:11414-11424.
34. Sun P., Ye S., Ferrandon S., Evans T.C., Xu M.-Q., Rao Z. Crystal structures of an intein from the split dnaE gene of Synechocystis sp. PCC6803 reveal the catalytic model without the penultimate histidine and the mechanism of zinc ion inhibition of protein splicing. J. Mol. Biol. 2005, 353:1093-1105.
35. Bai Y., Milne J.S., Mayne L., Englander S.W. Primary structure effects on peptide group hydrogen exchange. Proteins 1993, 17:75-86.
36. Englander S.W., Kallenbach N.R. Hydrogen exchange and structural dynamics of proteins and nucleic acids. Q. Rev. Biophys. 1983, 16:521-655.
37. Chou J.J., Gaemers S., Howder B., Louis J.M., Bax A. A simple apparatus for generating stretched polyacrylamide gels, yielding uniform alignment of proteins and detergent micelles. J. Biomol. NMR 2001, 21:377-382.
38. Ottiger M., Delaglio F., Bax A. Measurement of J and dipolar couplings from simplified two-dimensional NMR spectra. J. Magn. Reson. 1998, 131:373-378.
39. Zweckstetter M., Bax A. Prediction of sterically induced alignment in a dilute liquid crystalline phase: aid to protein structure determination by NMR. J. Am. Chem. Soc. 2000, 122:3791-3792.
40. 15N NMR relaxation. Biochemistry 1994, 33:5984-6003.
41. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., Bax A. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 1995, 6:277-293.
42. Lipari G., Szabo A. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules: 1. Theory and range of validity. J. Am. Chem. Soc. 1982, 104:4546-4559.
43. Lipari G., Szabo A. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules: 2. Analysis of experimental results. J. Am. Chem. Soc. 1982, 104:4559-4570.
44. Clore G.M., Szabo A., Bax A., Kay L.E., Driscoll P.C., Gronenborn A.M. Deviations from the simple two-parameter model-free approach to the interpretation of nitrogen-15 nuclear magnetic relaxation of proteins. J. Am. Chem. Soc. 1990, 112:4989-4991.
45. Cole R., Loria J.P. FAST-Modelfree: a program for rapid automated analysis of solution NMR spin-relaxation data. J. Biomol. NMR 2003, 26:203-213.
46. Loria J.P., Rance M., Palmer A.G. A relaxation-compensated Carr-Purcell-Meiboom-Gill sequence for characterizing chemical exchange by NMR spectroscopy. J. Am. Chem. Soc. 1999, 121:2331-2332.
47. Tollinger M., Skrynnikov N.R., Mulder F.A., Forman-Kay J.D., Kay L.E. Slow dynamics in folded and unfolded states of an SH3 domain. J. Am. Chem. Soc. 2001, 123:11341-11352.
48. 2 upon the Carr-Purcell pulse separation. J. Magn. Reson. 1972, 6:89-105.
49. Korzhnev D.M., Salvatella X., Vendruscolo M., Di Nardo A.A., Davidson A.R., Dobson C.M., Kay L.E. Low-populated folding intermediates of Fyn SH3 characterized by relaxation dispersion NMR. Nature 2004, 430:586-590.
50. Rao N.S., Legault P., Muhandiram D.R., Greenblatt J., Battiste J.L., Williamson J.R., Kay L.E. NMR pulse schemes for the sequential assignment of arginine side-chain H[epsilon]protons. J. Magn. Reson. Ser. B 1996, 113:272.