Structure and dynamics of coxsackievirus B4 2A proteinase, an enyzme involved in the etiology of heart disease

Journal of Virology

Volumn 80, Issue 3, 2006, Pages 1451-1462

  Baxter, Nicola J ^a   Roetzer, Andreas ^c   Liebig, Hans Dieter ^b   Sedelnikova, Svetlana E ^a   Hounslow, Andrea M ^a   Skern, Tim ^c   Waltho, Jonathan P ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b Axon Neuroscience Forschungs und Entwicklungs GmbH   (Austria)

^c Vienna Biocenter   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

COXSACKIEVIRUS B4 2A PROTEINASE; CYSTEINE PROTEINASE; DYSTROPHIN; INITIATION FACTOR 4G; UNCLASSIFIED DRUG; VIRUS ENZYME;

ANIMAL CELL; ANIMAL TISSUE; ANTIGEN PRESENTATION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; COXSACKIE VIRUS B4; CYTOSKELETON; ENZYME ACTIVE SITE; ENZYME STRUCTURE; HEART DISEASE; MOLECULAR MODEL; MOLECULAR RECOGNITION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PICORNAVIRUS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; RHINOVIRUS; SEROTYPING; STRUCTURE ANALYSIS; VIRUS REPLICATION;

AMINO ACID SEQUENCE; CARDIOMYOPATHY, DILATED; CATALYTIC DOMAIN; COXSACKIEVIRUS INFECTIONS; CYSTEINE ENDOPEPTIDASES; ELECTROSTATICS; ENTEROVIRUS B, HUMAN; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; RHINOVIRUS; SEQUENCE HOMOLOGY, AMINO ACID; THERMODYNAMICS; VIRAL PROTEINS;

ANIMALIA; COXSACKIEVIRUS; EUKARYOTA; HUMAN RHINOVIRUS SP.; PICORNAVIRIDAE; RHINOVIRUS;

EID: 31144434119     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.80.3.1451-1462.2006     Document Type: Article

References (62)

1. Baboonian, C., M. J. Davies, J. C. Booth, and W. J. McKenna. 1997. Coxsackie B viruses and human heart disease. Curr. Top. Microbiol. Immunol. 223:31-52.
2. Badorff, C., N. Berkely, S. Mehrotra, J. W. Talhouk, R. E. Rhoads, and K. U. Knowlton. 2000. Enteroviral protease 2A directly cleaves dystrophin and is inhibited by a dystrophin-based substrate analogue. J. Biol. Chem. 275:11191-11197.
3. Badorff, C., G.-H. Lee, B. J. Lamphear, M. E. Martone, K. P. Campbell, R. E. Rhoads, and K. U. Knowlton. 1999. Enteroviral protease 2A cleaves dystrophin: evidence of cytoskeletal disruption in an acquired cardiomyopathy. Nat. Med. 5:320-326.
4. Barbato, G., D. O. Cicero, M. C. Nardi, C. Steinkühler, R. Cortese, R. De Francesco, and R. Bazzo. 1999. The solution structure of the N-terminal proteinase domain of the hepatitis C virus (HCV) NS3 protein provides new insights into its activation and catalytic mechanism. J. Mol. Biol. 289:371-384.
5. Barbato, G., D. O. Cicero, F. Cordier, F. Narjes, B. Gerlach, S. Sambucini, S. Grzesiek, V. G. Matassa, R. De Francesco, and R. Bazzo. 2000. Inhibitor binding induces active site stabilization of the HCV NS3 protein serine protease domain. EMBO J. 19:1195-1206.
6. 13C-enriched proteins. J. Magn. Reson. 88:425-431.
7. Belsham, G. J., and N. Sonenberg. 1996. RNA-protein interactions in regulation of picornavirus RNA translation. Microbiol. Rev. 60:499-511.
8. 7a. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
9. Bradley, C. A., J. C. Padovan, T. L. Thompson, C. A. Benoit, B. T. Chait, and R. E. Rhoads. 2002. Mass spectrometric analysis of the N terminus of translational initiation factor eIF4G-1 reveals novel isoforms. J. Biol. Chem. 277:12559-12571.
10. Brunger, A. T. 1992. X-PLOR version 3.1: a system for X-ray crystallography and NMR. Yale University Press, New Haven, Conn.
11. Brunger, A. T., P. D. Adams, G. M. Clore, W. L. Delano, P. Gros, R. W. Grosse-Kunstleve, J.-S. Jiang, J. Kuszewski, M. Nilges, N. S. Pannu, R. J. Read, L. M. Rice, T. Simonson, and G. L. Warren. 1998. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D 54:905-921.
12. Byrd, M. P., M. Zamora, and R. E. Lloyd. 2002. Generation of multiple isoforms of eukaryotic translation initiation factor 4GI by use of alternate translation initiation codons. Mol. Cell. Biol. 22:4499-4511.
13. Cavanagh, J., W. J. Fairbrother, A. G. Palmer, and N. J. Skelton. 1995. Protein NMR spectroscopy: principles and practice. Academic Press, Inc., San Diego, Calif.
14. Chen, J., and K. R. Chien. 1999. Complexity in simplicity: monogenic disorders and complex cardiomyopathies. J. Clin. Investig. 103:1483-1485.
15. 13C labeled proteins. J. Magn. Reson. 97:213-217.
16. Cornilescu, G., F. Delaglio, and A. Bax. 1999. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 13:289-302.
17. DeLano, W. L. 2002. The PyMOL molecular graphics system. DeLano Scientific LLC, San Carlos, Calif. [Online.] http://www.pymol.org.
18. Etchison, D., S. C. Milburn, I. Edery, N. Sonenberg, and J. W. B. Hershey. 1982. Inhibition of HeLa cell protein synthesis following poliovirus infection correlates with the proteolysis of a 220 kDa polypeptide associated with eukaryotic initiation factor 3 and a cap binding protein complex. J. Biol. Chem. 257:14806-14810.
19. Ferrin, T. E., C. C. Huang, L. E. Jarvis, and R. Langridge. 1988. The MIDAS display system. J. Mol. Graph. 6:13-27.
20. pro recognition of eukaryotic initiation factor 4GI. Involvement of an exosite. J. Biol. Chem. 278:33200-33207.
21. Glaser, W., and T. Skern. 2000. Extremely efficient cleavage of eIF4G by picornaviral proteinases L and 2A in vitro. FEBS Lett. 480:151-155.
22. pro: relationship to self-cleavage and role of zinc. J. Virol. 77:5021-5025.
23. Gradi, A., Y. V. Svitkin, H. Imataka, and N. Sonenberg. 1998. Proteolysis of human eukaryotic initiation translation factor eIF4GII, but not eIF4GI, coincides with the shutoff of host protein synthesis after poliovirus infection. Proc. Natl. Acad. Sci. USA 95:11089-11094.
24. Grzesiek, S., and A. Bax. 1992. Improved 3D triple-resonance NMR techniques applied to a 31 kDa protein. J. Magn. Reson. 96:432-440.
25. 15N-enriched proteins. J. Biomol. NMR 3:185-204.
26. Hentze, M. W. 1997. eIF4G-a multipurpose ribosome adaptor. Science 275:500-501.
27. Kerekatte, V., B. D. Keiper, C. Badorff, A. Cai, K. U. Knowlton, and R. E. Rhoads. 1999. Cleavage of poly(A)-binding protein by coxsackievirus 2A protease in vitro and in vivo: another mechanism for host protein synthesis shutoff? J. Virol. 73:709-717.
28. Koenig, M., A. P. Monaco, and L. M. Kunkel. 1988. The complete sequence of dystrophin predicts a rod-shaped cytoskeletal protein. Cell 53:219-226.
29. 15N NMR spectroscopy. Biochemistry 31:4856-4866.
30. Kraulis, P. J. 1991. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24:946-950.
31. Lamphear, B. J., R. Kirchweger, T. Skern, and R. E. Rhoads. 1995. 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. 270:21975-21983.
32. Laskowski, R. A., J. A. C. Rullmann, M. W. MacArthur, R. Kaptein, and J. M. Thornton. 1996. AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8:477-486.
33. Liebig, H.-D., E. Ziegler, R. Van, K. Hartmuth, H. Klump, H. Kowalski, D. Blaas, W. Sommergruber, L. Frasel, B. Lamphear, R. Rhoads, E. Kuechler, and T. Skern. 1993. Purification of two picornaviral 2A proteinases: interaction with eIF-4γ and influence on in vitro translation. Biochemistry 32:7581-7588.
34. Malhotra, S. B., K. A. Hart, H. J. Klamut, N. S. Thomas, S. E. Bodrug, A. Burghes, M. Bobrow, P. S. Harper, M. W. Thompson, et al. 1988. Frameshift deletions in patients with Duchenne and Becker muscular dystrophy. Science 242:755-759.
35. Martin, J. R., F. A. Mulder, Y. Karimi-Nejad, J. van der Zwan, M. Mariani, D. Schipper, and R. Boelens. 1997. The solution structure of serine protease PB92 from Bacillus alcalophilus presents a rigid fold with a flexible substrate-binding site. Structure 5:521-532.
36. McCoy, M. A., M. M. Senior, J. J. Gesell, L. Ramanathan, and D. F. Wyss. 2001. Solution structure and dynamics of the single-chain hepatitis C virus NS3 protease NS4A cofactor complex. J. Mol. Biol. 305:1099-1110.
37. Merrit, E. A., and D. J. Bacon. 1997. Raster3D: photorealistic molecular graphics. Methods Enzymol. 277:505-524.
38. 13C labeling. Biochemistry 28:7510-7516.
39. Nicholls, A., K. A. Sharp, and B. Honig. 1991. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 11:281-296.
40. Nigro, G., L. I. Comi, L. Politano, and R. J. Bain. 1990. The incidence and evolution of cardiomyopathy in Duchenne muscular dystrophy. Int. J. Cardiol. 26:271-277.
41. Omichinski, J. G., G. M. Clore, E. Appella, K. Sakaguchi, and A. M. Gronenborn. 1990. High-resolution three-dimensional structure of a single zinc finger from a human enhancer binding protein in solution. Biochemistry 29:9324-9334.
42. 2O. J. Magn. Reson. B 103:197-201.
43. Pestova, T. V., V. G. Kolupaeva, I. B. Lomakin, E. V. Pilipenko, I. N. Shatsky, V. I. Agol, and C. U. T. Hellen. 2001. Molecular mechanisms of translation initiation in eukaryotes. Proc. Natl. Acad. Sci. USA 98:7029-7036.
44. Petersen, J. F. W., M. M. Cherney, H.-D. Liebig, T. Skern, E. Kuechler, and M. N. G. James. 1999. The structure of the 2A proteinase from a common cold virus: a proteinase responsible for the shut-off of host-cell protein synthesis. EMBO J. 18:5463-5475.
45. Read, R. J., M. Fujinaga, A. R. Sielecki, and M. N. G. James. 1983. Structure of the complex of Streptomyces griseus protease B and the third domain of the turkey ovomucoid inhibitor at 1.8 Å resolution. Biochemistry 22:4420-4433.
46. Reed, M. A. C., A. M. Hounslow, K. H. Sze, I. G. Barsukov, L. L. P. Hosszu, A. R. Clarke, C. J. Craven, and J. P. Waltho. 2003. Effects of domain dissection on the folding and stability of the 43 kDa protein PGK probed by NMR. J. Mol. Biol. 330:1189-1201.
47. Sachs, A. B., P. Sarnow, and M. W. Hentz. 1997. Starting at the beginning, middle and end: translation initiation in eukaryotes. Cell 89:831-838.
48. Sarkany, Z., T. Skern, and L. Polgar. 2000. Characterization of the active site thiol group of rhinovirus 2A proteinase. FEBS Lett. 481:289-292.
49. Sauter, N. K., T. Mau, S. D. Rader, and D. A. Agard. 1998. Structure of α-lytic protease complexed with its pro region. Nat. Struct. Biol. 5:945-950.
50. Skern, T., B. Hampoelz, E. Bergmann, A. Guarné, J. Petersen, I. Fita, and M. N. G. James. 2002. Structure and function of picornaviral proteinases, p. 199-212. In B. Semler and E. Wimmer (ed.), Molecular biology of picornaviruses. ASM Press, Washington, D.C.
51. Sole, M. J., and P. Liu. 1993. Viral myocarditis: a paradigm for understanding the pathogenesis and treatment of dilated cardiomyopathy. J. Am. Coll. Cardiol. 22:99A-105A.
52. Sommergruber, W., H. Ahorn, A. Zoephel, I. Maurer-Fogy, F. Fessl, G. Schnorrenberg, H.-D. Liebig, D. Blaas, E. Kuechler, and T. Skern. 1992. Cleavage specificity on synthetic peptide substrates of human rhinovirus 2 proteinase 2A. J. Biol. Chem. 267:22639-22644.
53. Sommergruber, W., H. Ahorn, H. Klump, J. Seipelt, A. Zoephel, F. Fessl, E. Krystek, D. Blaas, E. Kuechler, H.-D. Liebig, and T. Skern. 1994. 2A proteinases of Coxsackie- and Rhinovirus cleave peptides derived from eIF-4γ via a common recognition motif. Virology 198:741-745.
54. Sommergruber, W., C. Casari, F. Fessl, J. Seipelt, and T. Skern. 1994. The 2A proteinase of human rhinovirus is a zinc containing enzyme. Virology 204:815-818.
55. Straub, V., and K. P. Campbell. 1997. Muscular dystrophies and the dystrophin-glycoprotein complex. Curr. Opin. Neurol. 10:168-175.
56. Towbin, J. A., J. F. Hejtmancik, P. Brink, B. Gelb, X. M. Zhu, J. S. Chamberlain, E. R. McCabe, and M. Swift. 1993. X-linked dilated cardiomyopathy. Molecular genetic evidence of linkage to the Duchenne muscular dystrophy dystrophin gene at the Xp21 locus. Circulation 87:1854-1865.
57. Toyoda, H., M. J. H. Nicklin, M. G. Murray, C. W. Anderson, J. J. Dunn, F. W. Studier, and E. Wimmer. 1986. A second virus-encoded proteinase involved in proteolytic processing of poliovirus polyprotein. Cell 45:761-770.
58. Voss, T., R. Meyer, and W. Sommergruber. 1995. Spectroscopic characterisation of rhinoviral 2A: Zn is essential for the structural integrity. Protein Sci. 4:2526-2531.
59. 13C protein by homonuclear broadband decoupling. J. Magn. Reson. 98:428-435.
60. 1H TOCSY experiment for assignment of aromatic ring resonances and selective identitication of tyrosine ring resonances in proteins: description and application to photoactive yellow protein. J. Biomol. NMR 9:313-316.
61. Wittekind, M., and L. Mueller. 1993. 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. B 101:201-205.
62. Xiong, D., G.-H. Lee, C. Badorff, A. Dorner, S. Lee, P. Wolf, and K. U. Knowlton. 2002. Dystrophin deficiency markedly increases enterovirus-induced cardiomyopathy: a genetic predisposition to viral heart disease. Nat. Med. 8:872-877.