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 Letters

Volumn 583, Issue 9, 2009, Pages 1451-1456

  Oeemig, Jesper S ^a   Aranko, A Sesilja ^a   Djupsjöbacka, Janica ^a   Heinämäki, Kimmo ^a   Iwaï, Hideo ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Chemical modification; Intein; NMR spectroscopy; Nuclear spin relaxation; Protein ligation; Protein splicing; Protein trans splicing

Indexed keywords

DNAE INTEIN; INTEIN; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CHEMICAL MODIFICATION; EXPERIMENTAL MODEL; GENETIC VARIABILITY; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR DYNAMICS; NONHUMAN; NOSTOC; NOSTOC PUNCTIFORME; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTEIN STRUCTURE; SOLUTION AND SOLUBILITY;

AMINO ACID SEQUENCE; BASE SEQUENCE; DNA POLYMERASE III; DNA PRIMERS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; INTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NOSTOC; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION;

NOSTOC PUNCTIFORME;

EID: 67349189136     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2009.03.058     Document Type: Article

References (42)

1. Xu M.Q., and Evans Jr. T.C. Recent advances in protein splicing: manipulating proteins in vitro and in vivo. Curr. Opin. Biotechnol. 16 (2004) 440-446
2. Saleh L., and Perler F.B. Protein splicing in cis and in trans. Chem. Rec. 6 (2006) 183-193
3. Paulus H. Protein splicing and related forms of protein autoprocessing. Annu. Rev. Biochem. 69 (2000) 447-496
4. Wu H., Hu Z., and Liu X.Q. Protein trans-splicing by a split intein encoded in a split DnaE gene of Synechocystis sp. PCC6803. Proc. Natl. Acad. Sci. USA 95 (1998) 9226-9231
5. Mills K.V., Lew B.M., Jiang S., and Paulus H. Protein splicing in trans by purified N- and C-terminal fragments of the Mycobacterium tuberculosis RecA intein. Proc. Natl. Acad. Sci. USA 95 (1998) 3543-3548
6. Yamazaki T., Otomo T., Oda N., Kyogoku Y., Uegaki K., Ito N., Ishino Y., and Nakamura H. Segmental isotope labeling for protein NMR using peptide splicing. J. Am. Chem. Soc. 120 (1998) 5591-5592
7. Züger S., and Iwai H. Intein-based biosynthetic incorporation of unlabeled protein tags into isotopically labeled proteins for NMR studies. Nat. Biotechnol. 23 (2005) 736-740
8. Scott C.P., Abel-Santos E., Wall M., Wahnon D.C., and Benkovic S.J. Production of cyclic peptides and proteins in vivo. Proc. Natl. Acad. Sci. 24 (1999) 13638-13643
9. Evans T.C., Martin D., Kolly R., Panne D., Sun L., Ghosh I., Chen L.X., Benner J., Liu X.Q., and Xu M.Q. Protein trans-splicing and cyclization by a naturally split intein from the dnaE gene of Synechocystis species PCC6803. J. Biol. Chem. 275 (2000) 9091-9094
10. Iwai H., Lingel A., and Plückthun A. Cyclic green fluorescent protein produced in vivo using an artificially split PI-PfuI intein from Pyrococcus furiosus. J. Biol. Chem. 276 (2001) 16548-16554
11. Williams N.K., Prosselkov P., Liepinsh E., Line I., Sharipo A., Littler D.R., Curmi P.M., Otting G., and Dixon N.E. In vivo protein cyclization promoted by a circularly permuted Synechocystis sp. PCC6803 DnaB mini-intein. J. Biol. Chem. 277 (2002) 7790-7798
12. Mootz H.D., Blum E.S., Tyszkiewicz A.B., and Muir T.W. Conditional protein splicing: a new tool to control protein structure and function in vitro and in vivo. J. Am. Chem. Soc. 125 (2003) 10561-10569
13. Kurpiers T., and Mootz H.D. Regioselective cysteine bioconjugation by appending a labeled cystein tag to a protein by using protein splicing in trans. Angew. Chem. Int. Ed. Engl. 46 (2007) 5234-5237
14. Schwartz E.C., Saez L., Young M.W., and Muir T.W. Post-translational enzyme activation in an animal via optimized conditional protein splicing. Nat. Chem. Biol. 3 (2007) 50-54
15. Ludwig C., Pfeiff M., Linne U., and Mootz H.D. Ligation of a synthetic peptide to the N terminus of a recombinant protein using semisynthetic protein trans-splicing. Angew. Chem. Int. Ed. 45 (2006) 5218-5221
16. Iwai H., Züger S., Jin J., and Tam P.H. Highly efficient protein trans-splicing by a naturally split DnaE intein from Nostoc punctiforme. FEBS Lett. 580 (2006) 1853-1858
17. Otomo T., Teruya K., Uegaki K., Yamazaki T., and Kyogoku Y. Improved segmental isotope labeling of proteins and application to a larger protein. J. Biomol. NMR 14 (1999) 105-114
18. Aranko, A.S., Züger, S., Buchinger, E., and Iwaï, H. (2009) In vivo and in vitro protein ligation by naturally occurring and engineered split DnaE inteins, PLoS ONE 4, e5185.
19. Muona M., Aranko A.S., and Iwai H. Segmental isotopic labelling of a multi-domain protein by protein ligation using protein trans-splicing. ChemBioChem 9 (2008) 2958-2961
20. Iwai H., Aranko A.S., and Djupsjöbacka J. Protein ligation using protein trans-splicing. J. Pept. Sci. 14 Suppl. (2008) 183
21. Heinämäki, K., Oeemig, J.S., Djupsjöbacka, J. and Iwaï, H. (2009) NMR resonance assignment of DnaE intein from Nostoc punctiforme, Biomol. NMR assign, doi:10.1007/s12104-008-9137-1.
22. Farrow N.A., Muhandiram R., Singer A.U., Pascal S.M., Kay C.M., Gish G., Shoelson S.E., Pawson T., Forman-Kay J.D., and Kay L.E. Backbone dynamics of a free and phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation. Biochemistry 33 (1994) 5984-6003
23. Kay L.E., Nicholson L.K., Delaglio F., Bax A., and Torchia D.A. Pulse sequences for removal of the effects of cross correlation between dipolar and chemical-shift anisotropy relaxation mechanisms on the measurement of heteronuclear T1 and T2 values in proteins. J. Magn. Reson. 97 (1992) 359-375
24. Vranken W.F., Boucher W., Stevens T.J., Fogh R.H., Pajon A., Llinas M., Ulrich E.L., Markley J.L., Ionides J., and Laue E.D. The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins 59 (2005) 687-696
25. 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
26. 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
27. Pearlman D.A., Case D.A., Caldwell J.W., Ross W.S., Cheatham T.E., DeBolt S., Ferguson D., Seibel G., and Kollman P. AMBER, a package of computer programs for applying molecular mechanics, normal mode analysis, molecular dynamics and free energy calculations to simulate the structural and energetic properties of molecules. Comput. Phys. Commun. 91 (1995) 1-41
28. Cornell W.D., Cieplack P., Bayly C.I., Gould I.R., Merz K.M., Ferguson D.M., Spellmeyer D.C., Fox T., Caldwell J.W., and Kollman P.A. A 2nd generation force-field for the simulation of proteins, nucleic acids, and organic molecules. J. Am. Chem. Soc. 117 (1995) 5179-5197
29. Hall T.M., Porter J.A., Young K.E., Koonin E.V., Beachy P.A., and Leahy D.J. Crystal structure of a Hedgehog autoprocessing domain: homology between Hedgehog and self-splicing proteins. Cell 91 (1997) 85-97
30. Johnson M.A., Southworth M.W., Herrmann T., Brace L., Perler F.B., and Wüthrich K. NMR structure of a KlbA intein precursor from Methanococcus jannaschii. Protein Sci. 16 (2007) 1316-1328
31. Kay L.E., Torchia D.A., and Bax A. Backbone dynamics of proteins as studied by nitrogen-15 inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease. Biochemistry 128 (1989) 8972-8979
32. Clore G.M., Driscoll P.C., Wingfield P.T., and Gronenborn A.M. Analysis of the backbone dynamics of interleukin-1 beta using two-dimensional inverse detected heteronuclear 15N-1H NMR spectroscopy. Biochemistry 29 (1990) 7387-7401
33. 15N relaxation using inverse detected two-dimensional NMR spectroscopy: the central helix is flexible. Biochemistry 31 (1992) 5269-5278
34. 15N spin relaxation studies of protein mobility. Biochemistry 36 (1997) 7305-7312
35. Orekhov V.Yu., Nolde D.E., Golovanov A.P., Korzhnev D.M., and Arseniev A.S. Processing of heteronuclear NMR relaxation data with the new software DASHA. Appl. Magn. Reson. 9 (1995) 581-588
36. Sun W., Yang J., and Liu X.Q. Synthetic two-piece and three-piece split inteins for protein trans-splicing. J. Biol. Chem. 279 (2004) 35281-35286
37. Sun P., Ye S., Ferrandon S., Evans T.C., Xu M.Q., and Rao Z.H. 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. 353 (2005) 1093-1105
38. Martin D.D., Xu M.Q., and Evans Jr. T.C. Characterization of a naturally occurring trans-splicing intein from Synechocystis sp. PCC6803. Biochemistry 40 (2001) 1393-1402
39. Choi J.J., Nam K.H., Min B., Kim S.J., Söll D., and Kwon S.T. Protein trans-splicing and characterization of a split family B-type DNA polymerase from the hyperthermophilic archaeal parasite Nanoarchaeum equitans. J. Mol. Biol. 356 (2006) 1093-1106
40. Koradi R., Billeter M., and Wüthrich K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14 (1996) 51-55
41. 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. 26 (1993) 283-291
42. Morris A.L., MacArthur M.W., Hutchinson E.G., and Thornton J.M. Stereochemical quality of protein structure coordinates. Proteins 12 (1992) 345-364