Investigating the Substrate Specificity and Oligomerisation of the Leader Protease of Foot and Mouth Disease Virus using NMR

Journal of Molecular Biology

Volumn 373, Issue 4, 2007, Pages 1071-1087

  Cencic, Regina ^a   Mayer, Christina ^a   Juliano, Maria A ^b   Juliano, Luiz ^b   Konrat, Robert ^c   Kontaxis, Georg ^c   Skern, Tim ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^c UNIVERSITY OF VIENNA   (Austria)

Author keywords

cysteine proteinase; dimerisation; foot and mouth disease virus; protein synthesis inhibition; substrate recognition

Indexed keywords

PROTEINASE;

ARTICLE; BAY REGION BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SUBSTRATE; FOOT AND MOUTH DISEASE VIRUS; IONIC STRENGTH; MOLECULAR DYNAMICS; MOLECULAR RECOGNITION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN QUATERNARY STRUCTURE;

EUKARYOTA; FOOT-AND-MOUTH DISEASE VIRUS;

EID: 34848832896     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.08.061     Document Type: Article

References (52)

1. Guarné A., Tormo J., Kirchweger K., Pfistermueller D., Fita I., and Skern T. Structure of the foot-and-mouth disease virus leader protease: a papain-like fold adapted for self-processing and eIF4G recognition. EMBO J. 17 (1998) 7469-7479
2. Strebel K., and Beck E. A second protease of foot-and mouth disease virus. J. Virol. 58 (1986) 893-899
3. Medina M., Domingo E., Brangwyn J.K., and Belsham G.J. The two species of the foot-and-mouth disease virus leader protein, expressed individually, exhibit the same activities. Virology 194 (1993) 355-359
4. Cao X., Bergmann I.E., Fullkrug R., and Beck E. Functional analysis of the two alternative translation initiation sites of foot-and-mouth disease virus. J. Virol. 69 (1995) 560-563
5. Glaser W., Cencic R., and Skern T. Foot-and-mouth disease Leader proteinase: involvement of C-terminal residues in self-processing and cleavage of eIF4GI. J. Biol. Chem. 276 (2001) 35473-35481
6. Devaney M.A., Vakharia V.N., Lloyd R.E., Ehrenfeld E., and Grubman M.J. Leader protein of Foot-and-Mouth disease virus is required for cleavage of the p220 component of the cap-binding protein complex. J. Virol. 62 (1988) 4407-4409
7. Gradi A., Foeger N., Strong R., Svitkin Y.V., Sonenberg N., Skern T., and Belsham G. Cleavage of eukaryotic translation initiation factor 4GII within foot-and-mouth disease virus-infected cells: identification of the L-protease cleavage site in vitro. J. Virol. 78 (2004) 3271-3278
8. Lamphear B.J., Kirchweger R., Skern T., and Rhoads R.E. Mapping of functional domains in eukaryotic protein synthesis initiation factor 4G (eIF4G) with picornaviral proteases - implications for cap-dependent and cap- independent translational initiation. J. Biol. Chem. 270 (1995) 21975-21983
9. Belsham G.J., and Jackson R.R. Translation initiation on picornavirus RNA. In: Sonenberg N., Hershey J.W.B., and Mathews M.B. (Eds). Translational Control of Gene Expression vol. 39 (2000), Cold Spring Harbor Press, Cold Spring Harbor, NY 869-900
10. de Los Santos T., de Avila Botton S., Weiblen R., and Grubman M.J. The leader proteinase of foot-and-mouth disease virus inhibits the induction of beta interferon mRNA and blocks the host innate immune response. J. Virol. 80 (2006) 1906-1914
11. Brown C.C., Piccone M.E., Mason P.W., McKenna T.S., and Grubman M.J. Pathogenesis of wild-type and leaderless foot-and-mouth disease virus in cattle. J. Virol. 70 (1996) 5638-5641
12. Guarné A., Hampoelz B., Glaser W., Carpena X., Tormo J., Fita I., and Skern T. Structural and biochemical features distinguish the foot-and-mouth disease virus leader proteinase from other papain-like enzymes. J. Mol. Biol. 302 (2000) 1227-1240
13. Skern T., Fita I., and Guarne A. A structural model of picornavirus leader proteinases based on papain and bleomycin hydrolase. J. Gen. Virol. 79 (1998) 301-307
14. Foeger N., Kuehnel E., Cencic R., and Skern T. The binding of foot-and-mouth disease virus leader proteinase to eIF4GI involves conserved ionic interactions. FEBS J. 272 (2005) 2602-2611
15. Foeger N., Glaser W., and Skern T. Recognition of eukaryotic initiation factor 4G isoforms by picornaviral proteinases. J. Biol. Chem. 277 (2002) 44300-44309
16. Schlick P., Kronovetr J., Hampoelz B., and Skern T. Modulation of the electrostatic charge at the active site of foot-and-mouth-disease-virus leader proteinase, an unusual papain-like enzyme. Biochem. J. 363 (2002) 493-501
17. Lipari G., and Szabo A. Nuclear magnetic resonance relaxation in nucleic acid fragments: models for internal motion. Biochemistry 20 (1981) 6250-6256
18. Lipari G., and 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. 104 (1982) 4546-4559
19. Lipari G., and Szabo A. Model-free approach to the interpretation of nuclear magnetic-resonance relaxation in macromolecules. 2. Analysis of experimental results. J. Am. Chem. Soc. 104 (1982) 4559-4570
20. Tjandra N., and Bax A. Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium. Science 278 (1997) 1111-1114
21. Tjandra N., Omichinski J.G., Gronenborn A.M., Clore G.M., and Bax A. Use of dipolar 1H-15N and 1H-13C couplings in the structure determination of magnetically oriented macromolecules in solution. Nature Struct. Biol. 4 (1997) 732-738
22. Zweckstetter M., and Bax A. Prediction of sterically induced alignment in a dilute liquid crystalline phase: Aid to protein structure determination by NMR. J. Am. Chem. Soc. 122 (2000) 3791-3792
23. Zweckstetter M., Hummer G., and Bax A. Prediction of charge-induced molecular alignment of biomolecules dissolved in dilute liquid-crystalline phases. Biophys. J. 86 (2004) 3444-3460
24. Schwieters C.D., Kuszewski J.J., Tjandra N., and Clore G.M. The Xplor-NIH NMR molecular structure determination package. J. Magn. Reson. 160 (2003) 65-73
25. Kamphuis I.G., Kalk K.H., Swarte M.B., and Drenth J. Structure of papain refined at 1.65 Å resolution. J. Mol. Biol. 179 (1984) 233-256
26. Drenth J., Jansonius J.N., Koekoek R., Swen H.M., and Wolthers B.G. Structure of papain. Nature 218 (1968) 929-932
27. Oliveira V., Gatti R., Rioli V., Ferro E.S., Spisni A., Camargo A.C., et al. Temperature and salts effects on the peptidase activities of the recombinant metallooligopeptidases neurolysin and thimet oligopeptidase. Eur. J. Biochem. 269 (2002) 4326-4334
28. Kirchweger R., Ziegler E., Lamphear B.J., Waters D., Liebig H.D., Sommergruber W., et al. Foot-and-mouth disease virus leader proteinase: purification of the Lb form and determination of its cleavage site on eIF-4 gamma. J. Virol. 68 (1994) 5677-5684
29. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., and Bax A. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6 (1995) 277-293
30. Kay L.E., Ikura M., Tschudin R., and Bax A. Three-dimensional triple-resonance NMR-spectroscopy of isotopically enriched proteins. J. Magn. Reson. 89 (1990) 495-514
31. Grzesiek S., and Bax A. Amino acid type determination in the sequential assignment procedure of uniformly 13C/15N-enriched proteins. J. Biomol. NMR 3 (1993) 185-204
32. Grzesiek S., and Bax A. Correlating backbone amide and side-chain resonances in larger proteins by multiple relayed triple resonance NMR. J. Am. Chem. Soc. 114 (1992) 6291-6293
33. Wittekind M., and Mueller L. HNCACB, a high-sensitivity 3D NMR Experiment to correlate amide-proton and nitrogen resonances with the alpha- and beta-carbon resonances in proteins. J. Magn. Reson. ser. B 101 (1993) 201-205
34. 13C-labeled proteins. J. Magn. Reson. 97 (1992) 213-217
35. Kay L.E., Ikura M., and Bax A. Proton proton correlation via carbon carbon couplings - a 3-dimensional NMR approach for the assignment of aliphatic resonances in proteins labeled with carbon-13. J. Am. Chem. Soc. 112 (1990) 888-889
36. Marion D., Driscoll P.C., Kay L.E., Wingfield P.T., Bax A., Gronenborn A.M., and Clore G.M. Overcoming the overlap problem in the assignment of 1H NMR spectra of larger proteins by use of three-dimensional heteronuclear 1H-15N Hartmann-Hahn-multiple quantum coherence and nuclear Overhauser-multiple quantum coherence spectroscopy: application to interleukin 1 beta. Biochemistry 28 (1989) 6150-6156
37. Kuboniwa H., Grzesiek S., Delaglio F., and Bax A. Measurement of HN-H alpha J couplings in calcium-free calmodulin using new 2D and 3D water-flip-back methods. J. Biomol. NMR 4 (1994) 871-878
38. Bax A., Clore G.M., Driscoll P.C., Gronenborn A.M., Ikura M., and Kay L.E. Practical aspects of proton carbon carbon proton three-dimensional correlation spectroscopy of C-13-labeled proteins. J. Magn. Reson. 87 (1990) 620-627
39. Cornilescu G., Delaglio F., and Bax A. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 13 (1999) 289-302
40. Farrow N.A., Muhandiram R., Singer A.U., Pascal S.M., Kay C.M., Gish G., et al. Backbone dynamics of a free and phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation. Biochemistry 33 (1994) 5984-6003
41. Farrow N.A., Zhang O., Szabo A., Torchia D.A., and Kay L.E. Spectral density function mapping using 15N relaxation data exclusively. J. Biomol. NMR 6 (1995) 153-162
42. Ottiger M., Delaglio F., and Bax A. Measurement of J and dipolar couplings from simplified two-dimensional NMR spectra. J. Magn. Reson. 131 (1998) 373-378
43. Kraulis P.J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24 (1991) 946-950
44. Merritt E.A., and Murphy M.E. Raster3D version 2.0. a program for photorealistic molecular graphics. Acta Crystallog. sect. D 50 (1994) 869-873
45. Brunger A.T. Crystallographic refinement by simulated annealing. Application to a 2.8 Å resolution structure of aspartate aminotransferase. J. Mol. Biol. 203 (1988) 803-816
46. Nilges M., Gronenborn A.M., Brunger A.T., and Clore G.M. Determination of three-dimensional structures of proteins by simulated annealing with interproton distance restraints. Application to crambin, potato carboxypeptidase inhibitor, and barley proteinase inhibitor 2. Protein Eng. 2 (1988) 27-38
47. Brunger A.T. X-plor (Version 3.1) a System for X-ray Crystallography and NMR (1993), Yale University Press, New Haven
48. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallog. sect. D 54 (1998) 905-921
49. Koradi, R., Billeter, M., & Wuthrich, K. (1996). MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14, 51-5, 29-32.
50. Kuszewski J., Gronenborn A.M., and Clore G.M. Improving the packing and accuracy of NMR structures with a pseudopotential for the radius of gyration. J. Am. Chem. Soc. 121 (1999) 2337-2338
51. Clore G.M., Starich M.R., and Gronenborn A.M. Measurement of residual dipolar couplings of macromolecules aligned in the nematic phase of a colloidal suspension of rod-shaped viruses. J. Am. Chem. Soc. 120 (1998) 10571-10572
52. Dasso M.C., and Jackson R.J. Efficient initiation of mammalian mRNA translation at a CUG codon. Nucl. Acids Res. 17 (1989) 6485-6497