Structural and Biochemical Analysis of Human Pathogenic Astrovirus Serine Protease at 2.0 Å Resolution

Journal of Molecular Biology

Volumn 387, Issue 5, 2009, Pages 1137-1152

  Speroni, Silvia ^a   Rohayem, Jacques ^b   Nenci, Simone ^a   Bonivento, Daniele ^a   Robel, Ivonne ^b   Barthel, Julia ^b   Luzhkov, Victor B ^c   Coutard, Bruno ^d   Canard, Bruno ^d   Mattevi, Andrea ^a  

^a UNIVERSITY OF PAVIA   (Italy)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^c UPPSALA UNIVERSITY   (Sweden)

^d Centre National de la Recherche Scientifique   (France)

Author keywords

astrovirus, serine protease, polyprotein, antiviral, catalytic triad

Indexed keywords

ASPARTIC ACID; GLUTAMINE; HISTIDINE; SERINE; SERINE PROTEINASE; WATER;

ARTICLE; ASTROVIRUS; BETA SHEET; BINDING SITE; CRYSTAL STRUCTURE; ELECTRIC POTENTIAL; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME CONFORMATION; ENZYME DEGRADATION; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SUBSTRATE; HYDROLYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; STRUCTURE ANALYSIS;

ASTROVIRIDAE; RNA VIRUSES;

EID: 63449095360     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.02.044     Document Type: Article

References (47)

1. Matsui S.M., Kiang D., Ginzton N., Chew T., and Geigenmüller-Gnirke U. Molecular biology of astroviruses: selected highlights. Novartis Found. Symp. 238 (2001) 219-233
2. Monroe S.S., Jiang B., Stine S.E., Koopmans M., and Glass R.I. Subgenomic RNA sequence of human astrovirus supports classification of Astroviridae as a new family of RNA viruses. J. Virol. 67 (1993) 3611-3614
3. Appleton H., and Higgins P.G. Viruses and gastroenteritis in infants. Lancet 1 (1975) 1297
4. Madeley C.R., and Cosgrove B.P. 28 nm particles in faeces in infantile gastroenteritis. Lancet 2 (1975) 451-452
5. Monroe S.S., Holmes J.L., and Belliot G.M. Molecular epidemiology of human astroviruses. Novartis Found. Symp. 238 (2001) 237-245
6. Gabbay Y.B., Chamone C.B., Nakamura L.S., Oliveira D.S., Abreu S.F., Cavalcante-Pepino E.L., et al. Characterization of an astrovirus genotype 2 strain causing an extensive outbreak of gastroenteritis among Maxakali Indians, Southeast Brazil. J. Clin. Virol. 37 (2006) 287-292
7. Lee T.W., and Kurtz J.B. Prevalence of human astrovirus serotypes in the Oxford region 1976-92, with evidence for two new serotypes. Epidemiol. Infect. 112 (1994) 187-193
8. Méndez-Toss M., Romero-Guido P., Munguía M.E., Méndez E., and Arias C.F. Molecular analysis of a serotype 8 human astrovirus genome. J. Gen. Virol. 81 (2000) 2891-2897
9. Bass D.M., and Qiu S. Proteolytic processing of the astrovirus capsid. J. Virol. 74 (2000) 1810-1814
10. Geigenmüller U., Chew T., Ginzton N.M., and Matsui S.N. Processing of nonstructural protein 1a of human astrovirus. J. Virol. 76 (2002) 2003-2008
11. Lewis T.L., and Matsui S.M. An astrovirus frameshift signal induces ribosomal frameshifting in vitro. Arch. Virol. 140 (1995) 1127-1135
12. Lewis T.L., Greenberg H.B., Herrmann J.E., Smith L.S., and Matsui S.M. Analysis of astrovirus serotype 1 RNA, identification of the viral RNA-dependent RNA polymerase motif, and expression of a viral structural protein. J. Virol. 68 (1994) 77-83
13. Marczinke B., Bloys A.J., Brown T.D., Willcocks M.M., Carter M.J., and Brierley I. The human astrovirus RNA-dependent RNA polymerase coding region is expressed by ribosomal frameshifting. J. Virol. 68 (1994) 5588-5595
14. Monroe S.S., Stine S.E., Gorelkin L., Herrmann J.E., Blacklow N.R., and Glass R.I. Temporal synthesis of proteins and RNAs during human astrovirus infection of cultured cells. J. Virol. 65 (1991) 641-648
15. Willcocks M.M., Boxall A.S., and Carter M.J. Processing and intracellular location of human astrovirus non-structural proteins. J. Gen. Virol. 80 (1999) 2607-2611
16. Willcocks M.M., Brown T.D., Madeley C.R., and Carter M.J. The complete sequence of a human astrovirus. J. Gen. Virol. 75 (1994) 1785-1788
17. Kiang D., and Matsui S.M. Proteolytic processing of a human astrovirus nonstructural protein. J. Gen. Virol. 83 (2002) 25-34
18. Berman H.M., Battistuz T., Bhat T.N., Bluhm W.F., Bourne P.E., Burkhardt K., et al. The Protein Data Bank. Acta Crystallogr. D 58 (2002) 899-907
19. Holm L., and Sander C. Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233 (1993) 123-138
20. Hasselblatt H., Kurzbauer R., Wilken C., Krojer T., Sawa J., Kurt J., et al. Regulation of the sigmaE stress response by DegS: how the PDZ domain keeps the protease inactive in the resting state and allows integration of different OMP-derived stress signals upon folding stress. Genes Dev. 21 (2007) 2659-2670
21. Li W., Srinivasula S.M., Chai J., Li P., Wu J.W., Zhang Z., et al. Structural insights into the pro-apoptotic function of mitochondrial serine protease HtrA2/Omi. Nature Struct. Biol. 9 (2002) 436-441
22. Gayathri P., Satheshkumar P.S., Prasad K., Nair S., Savithri H.S., and Murthy M.R. Crystal structure of the serine protease domain of Sesbania mosaic virus polyprotein and mutational analysis of residues forming the S1-binding pocket. Virology 346 (2006) 440-451
23. Matthews D.A., Dragovich P.S., Webber S.E., Fuhrman S.A., Patick A.K., Zalman L.S., et al. Structure-assisted design of mechanism-based irreversible inhibitors of human rhinovirus 3C protease with potent antiviral activity against multiple rhinovirus serotypes. Proc. Natl Acad. Sci. USA 96 (1999) 11000-11007
24. Bergmann E.M., Cherney M.M., Mckendrick J., Frormann S., Luo C., Malcolm B.A., et al. Crystal structure of an inhibitor complex of the 3C protease from hepatitis A virus (HAV) and implications for the polyprotein processing in HAV. Virology 265 (1999) 153-163
25. Sweeney T.R., Roqué-Rosell N., Birtley J.R., Leatherbarrow R.J., and Curry S. Structural and mutagenic analysis of foot-and-mouth disease virus 3C protease reveals the role of the beta-ribbon in proteolysis. J. Virol. 81 (2007) 115-124
26. Yan Y., Li Y., Munshi S., Sardana V., Cole J.L., Sardana M., et al. Complex of NS3 protease and NS4A peptide of BK strain hepatitis C virus: a 2.2 Å resolution structure in a hexagonal crystal form. Protein Sci. 7 (1998) 837-847
27. Zeitler C.E., Estes M.K., and Venkataram Prasad B.V. X-ray crystallographic structure of the Norwalk virus protease at 1.5 Å resolution. J. Virol. 80 (2006) 5050-5058
28. Bergmann E.M., Mosimann S.C., Chernaia M.M., Malcolm B.A., and James M.N. The refined crystal structure of the 3C gene product from hepatitis A virus: specific protease activity and RNA recognition. J. Virol. 71 (1997) 2436-2448
29. Yin J., Bergmann E.M., Cherney M.M., Lall M.S., Jain R.P., Vederas J.C., and James M.N. Dual modes of modification of hepatitis A virus 3C protease by a serine-derived beta-lactone: selective crystallization and formation of a functional catalytic triad in the active site. J. Mol. Biol. 354 (2005) 854-871
30. Yin J., Cherney M.M., Bergmann E.M., Zhang J., Huitema C., Pettersson H., et al. An episulfide cation (thiiranium ring) trapped in the active site of HAV 3C protease inactivated by peptide-based ketone inhibitors. J. Mol. Biol. 361 (2006) 673-686
31. Mosimann S.C., Cherney M.M., Sia S., Plotch S., and James M.N. Refined X-ray crystallographic structure of the poliovirus 3C gene product. J. Mol. Biol. 273 (1997) 1032-1047
32. Erlanger B.F., Kokowsky N., and Cohen W. The preparation and properties of two new chromogenic substrates of trypsin. Arch. Biochem. Biophys. 95 (1961) 271-278
33. Wirblich C., Sibilia M., Boniotti M.B., Rossi C., Thiel H.J., and Meyers G. 3C-Like protease of rabbit hemorrhagic disease virus: identification of cleavage sites in the ORF1 polyprotein and analysis of cleavage specificity. J. Virol. 69 (1995) 7159-7168
34. Coutard B., Gorbalenya A.E., Snijder E.J., Leontovich A.M., Poupon A., De Lamballerie X., et al. The VIZIER project: preparedness against pathogenic RNA viruses. Antivir. Res. 78 (2008) 37-46
35. Studier F.W. Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif. 41 (2005) 207-234
36. CCP4 (Collaborative Computational Project, Number 4). The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D 50 (1994) 760-763
37. Schneider T.R., and Sheldrick G.M. Substructure solution with SHELXD. Acta Crystallogr. D 58 (2002) 1772-1779
38. Bricogne G., Vonrhein C., Flensburg C., Schiltz M., and Paciorek W. Generation, representation and flow of phase information in structure determination: recent developments in and around SHARP 2.0. Acta Crystallogr. D 59 (2003) 2023-2030
39. Cowtan K.D., and Zhang K.Y. Density modification for macromolecular phase improvement. Prog. Biophys. Mol. Biol. 72 (1999) 245-270
40. Perrakis A., Harkiolaki M., Wilson K.S., and Lamzin V.S. ARP/wARP and molecular replacement. Acta Crystallogr. D 57 (2001) 1445-1450
41. Emsley P., and Cowtan K.D. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60 (2004) 2126-2132
42. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D 53 (1997) 240-255
43. Verdonk M.L., Cole J.C., Hartshorn M.J., Murray C.W., and Taylor R.D. Improved protein-ligand docking using GOLD. Proteins: Struct. Funct. Genet. 52 (2003) 609-623
44. Scheffler U., Rudolph W., Gebhardt J., and Rohayem J. Differential cleavage of the norovirus polyprotein precursor by two active forms of the viral protease. J. Gen. Virol. 88 (2007) 2013-2018
45. Gouet P., Robert X., and Courcelle E. ESPript/ENDscript: Extracting and rendering sequence and 3D information from atomic structures of proteins. Nucleic Acids Res. 31 (2003) 3320-3323
46. Baker N.A., Sept D., Joseph S., Holst M.J., and McCammon J.A. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl Acad. Sci. USA 98 (2001) 10037-10041
47. 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