Crystal structure-based exploration of the important role of Arg106 in the RNA-binding domain of human coronavirus OC43 nucleocapsid protein

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1834, Issue 6, 2013, Pages 1054-1062

  Chen, I Jung ^a   Yuann, Jeu Ming P ^b   Chang, Yu Ming ^c   Lin, Shing Yen ^a   Zhao, Jincun ^d   Perlman, Stanley ^d   Shen, Yo Yu ^a   Huang, Tai Huang ^e   Hou, Ming Hon ^a  

^a NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^b MING CHUAN UNIVERSITY   (Taiwan)

^c INSTITUTE OF BIOLOGICAL CHEMISTRY   (Taiwan)

^d UNIVERSITY OF IOWA   (United States)

^e INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

Author keywords

Arginine106; Coronaviruses; Nucleocapsid protein; RNA binding; Virus replication; X ray crystallography

Indexed keywords

ARG106 PROTEIN; HUMAN CORONAVIRUS OC43 PROTEIN; NUCLEOCAPSID PROTEIN; UNCLASSIFIED DRUG; VIRUS RNA;

ARTICLE; CORONAVIRUS; CRYSTAL STRUCTURE; MOLECULAR DOCKING; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; RNA BINDING; SIMULATION; SITE DIRECTED MUTAGENESIS; VIRUS REPLICATION;

AMINO ACID SEQUENCE; CORONAVIRUS OC43, HUMAN; CRYSTALLOGRAPHY, X-RAY; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NUCLEOCAPSID PROTEINS; PROTEIN STRUCTURE, TERTIARY; RNA, VIRAL; RNA-BINDING PROTEINS; SEQUENCE ALIGNMENT;

CORONAVIRUS;

EID: 84878105608     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2013.03.003     Document Type: Article

References (61)

1. J.R. St-Jean, H. Jacomy, M. Desforges, A. Vabret, F. Freymuth, and P.J. Talbot Human respiratory coronavirus OC43: Genetic stability and neuroinvasion J. Virol. 78 2004 8824 8834
2. A. Vabret, T. Mourez, S. Gouarin, J. Petitjean, and F. Freymuth An outbreak of coronavirus OC43 respiratory infection in Normandy, France Clin. Infect. Dis. 36 2003 985 989
3. H.M. El-Sahly, R.L. Atmar, W.P. Glezen, and S.B. Greenberg Spectrum of clinical illness in hospitalized patients with "common cold" virus infections Clin. Infect. Dis. 31 2000 96 100
4. A. Gagneur, J. Sizun, S. Vallet, M.C. Legr, B. Picard, and P.J. Talbot Coronavirus-related nosocomial viral respiratory infections in a neonatal and paediatric intensive care unit: A prospective study J. Hosp. Infect. 51 2002 59 64
5. R.P. Wenzel, J.O. Hendley, J.A. Davies, and J.M. Gwaltney Jr. Coronavirus infections in military recruits. Three-year study with coronavirus strains OC43 and 229E Am. Rev. Respir. Dis. 109 1974 621 624
6. N. Arbour, R. Day, J. Newcombe, and P.J. Talbot Neuroinvasion by human respiratory coronaviruses J. Virol. 74 2000 8913 8921
7. Q. Leng, and Z. Bentwich A novel coronavirus and SARS N. Engl. J. Med. 349 2003 709
8. B.G. Hogue, and D.A. Brian Structural proteins of human respiratory coronavirus OC43 Virus Res. 5 1986 131 144
9. M.M. Lai, and D. Cavanagh The molecular biology of coronaviruses Adv. Virus Res. 48 1997 1 100
10. J.A. Hiscox RNA viruses: Hijacking the dynamic nucleolus Nat. Rev. Microbiol. 5 2007 119 127
11. S.A. Stohlman, J.O. Fleming, C.D. Patton, and M.M. Lai Synthesis and subcellular localization of the murine coronavirus nucleocapsid protein Virology 130 1983 527 532
12. J.H. You, M.L. Reed, B.K. Dove, and J.A. Hiscox Three-dimensional reconstruction of the nucleolus using meta-confocal microscopy in cells expressing the coronavirus nucleoprotein Adv. Exp. Med. Biol. 581 2006 313 318
13. R.S. Baric, G.W. Nelson, J.O. Fleming, R.J. Deans, J.G. Keck, N. Casteel, and S.A. Stohlman Interactions between coronavirus nucleocapsid protein and viral RNAs: Implications for viral transcription J. Virol. 62 1988 4280 4287
14. P.S. Masters, M.M. Parker, C.S. Ricard, C. Duchala, M.F. Frana, K.V. Holmes, and L.S. Sturman Structure and function studies of the nucleocapsid protein of mouse hepatitis virus Adv. Exp. Med. Biol. 276 1990 239 246
15. K. Pyrc, M.F. Jebbink, B. Berkhout, and L. van der Hoek Genome structure and transcriptional regulation of human coronavirus NL63 Virol. J. 1 2004 7
16. T.K. Tang, M.P. Wu, S.T. Chen, M.H. Hou, M.H. Hong, F.M. Pan, H.M. Yu, J.H. Chen, C.W. Yao, and A.H. Wang Biochemical and immunological studies of nucleocapsid proteins of severe acute respiratory syndrome and 229E human coronaviruses Proteomics 5 2005 925 937
17. L. Du, G. Zhao, Y. Lin, C. Chan, Y. He, S. Jiang, C. Wu, D.Y. Jin, K.Y. Yuen, Y. Zhou, and B.J. Zheng Priming with rAAV encoding RBD of SARS-CoV S protein and boosting with RBD-specific peptides for T cell epitopes elevated humoral and cellular immune responses against SARS-CoV infection Vaccine 26 2008 1644 1651
18. P.K. Hsieh, S.C. Chang, C.C. Huang, T.T. Lee, C.W. Hsiao, Y.H. Kou, I.Y. Chen, C.K. Chang, T.H. Huang, and M.F. Chang Assembly of severe acute respiratory syndrome coronavirus RNA packaging signal into virus-like particles is nucleocapsid dependent J. Virol. 79 2005 13848 13855
19. S.A. Kopecky-Bromberg, L. Martinez-Sobrido, M. Frieman, R.A. Baric, and P. Palese Severe acute respiratory syndrome coronavirus open reading frame (ORF) 3b, ORF 6, and nucleocapsid proteins function as interferon antagonists J. Virol. 81 2007 548 557
20. M. Surjit, B. Liu, V.T. Chow, and S.K. Lal The nucleocapsid protein of severe acute respiratory syndrome-coronavirus inhibits the activity of cyclin-cyclin-dependent kinase complex and blocks S phase progression in mammalian cells J. Biol. Chem. 281 2006 10669 10681
21. S. Zuniga, I. Sola, J.L. Moreno, P. Sabella, J. Plana-Duran, and L. Enjuanes Coronavirus nucleocapsid protein is an RNA chaperone Virology 357 2007 215 227
22. K.H. Chan, V.C. Cheng, P.C. Woo, S.K. Lau, L.L. Poon, Y. Guan, W.H. Seto, K.Y. Yuen, and J.S. Peiris Serological responses in patients with severe acute respiratory syndrome coronavirus infection and cross-reactivity with human coronaviruses 229E, OC43, and NL63 Clin. Diagn. Lab. Immunol. 12 2005 1317 1321
23. T. Mourez, A. Vabret, Y. Han, J. Dina, L. Legrand, S. Corbet, and F. Freymuth Baculovirus expression of HCoV-OC43 nucleocapsid protein and development of a Western blot assay for detection of human antibodies against HCoV-OC43 J. Virol. Methods 139 2007 175 180
24. F.Y. Liang, L.C. Lin, T.H. Ying, C.W. Yao, T.K. Tang, Y.W. Chen, and M.H. Hou Immunoreactivity characterisation of the three structural regions of the human coronavirus OC43 nucleocapsid protein by Western blot: Implications for the diagnosis of coronavirus infection J. Virol. Methods 187 2013 413 420
25. C.K. Chang, S.C. Sue, T.H. Yu, C.M. Hsieh, C.K. Tsai, Y.C. Chiang, S.J. Lee, H.H. Hsiao, W.J. Wu, W.L. Chang, C.H. Lin, and T.H. Huang Modular organization of SARS coronavirus nucleocapsid protein J. Biomed. Sci. 13 2006 59 72
26. C.Y. Chen, C.K. Chang, Y.W. Chang, S.C. Sue, H.I. Bai, L. Riang, C.D. Hsiao, and T.H. Huang Structure of the SARS coronavirus nucleocapsid protein RNA-binding dimerization domain suggests a mechanism for helical packaging of viral RNA J. Mol. Biol. 368 2007 1075 1086
27. H. Fan, A. Ooi, Y.W. Tan, S. Wang, S. Fang, D.X. Liu, and J. Lescar The nucleocapsid protein of coronavirus infectious bronchitis virus: Crystal structure of its N-terminal domain and multimerization properties Structure 13 2005 1859 1868
28. H. Jayaram, H. Fan, B.R. Bowman, A. Ooi, J. Jayaram, E.W. Collisson, J. Lescar, and B.V. Prasad X-ray structures of the N- and C-terminal domains of a coronavirus nucleocapsid protein: Implications for nucleocapsid formation J. Virol. 80 2006 6612 6620
29. K.A. Spencer, and J.A. Hiscox Characterisation of the RNA binding properties of the coronavirus infectious bronchitis virus nucleocapsid protein amino-terminal region FEBS Lett. 580 2006 5993 5998
30. Y.S. Lo, S.Y. Lin, S.M. Wang, C.T. Wang, Y.L. Chiu, T.H. Huang, and M.H. Hou Oligomerization of the carboxyl terminal domain of the human coronavirus 229E nucleocapsid protein FEBS Lett. 587 2013 120 127
31. S.M. Kuo, H.W. Kao, M.H. Hou, C.H. Wang, S.H. Lin, and H.L. Su Evolution of infectious bronchitis virus in Taiwan: Positively selected sites in the nucleocapsid protein and their effects on RNA-binding activity Vet. Microbiol. 162 2013 408 418
32. P.S. Masters Localization of an RNA-binding domain in the nucleocapsid protein of the coronavirus mouse hepatitis virus Arch. Virol. 125 1992 141 160
33. G.W. Nelson, and S.A. Stohlman Localization of the RNA-binding domain of mouse hepatitis virus nucleocapsid protein J. Gen. Virol. 74 Pt 9 1993 1975 1979
34. D. Peng, C.A. Koetzner, T. McMahon, Y. Zhu, and P.S. Masters Construction of murine coronavirus mutants containing interspecies chimeric nucleocapsid proteins J. Virol. 69 1995 5475 5484
35. H. Chen, A. Gill, B.K. Dove, S.R. Emmett, C.F. Kemp, M.A. Ritchie, M. Dee, and J.A. Hiscox Mass spectroscopic characterization of the coronavirus infectious bronchitis virus nucleoprotein and elucidation of the role of phosphorylation in RNA binding by using surface plasmon resonance J. Virol. 79 2005 1164 1179
36. K.A. Spencer, M. Dee, P. Britton, and J.A. Hiscox Role of phosphorylation clusters in the biology of the coronavirus infectious bronchitis virus nucleocapsid protein Virology 370 2008 373 381
37. K.S. Saikatendu, J.S. Joseph, V. Subramanian, B.W. Neuman, M.J. Buchmeier, R.C. Stevens, and P. Kuhn Ribonucleocapsid formation of severe acute respiratory syndrome coronavirus through molecular action of the N-terminal domain of N protein J. Virol. 81 2007 3913 3921
38. M. Takeda, C.K. Chang, T. Ikeya, P. Guntert, Y.H. Chang, Y.L. Hsu, T.H. Huang, and M. Kainosho Solution structure of the c-terminal dimerization domain of SARS coronavirus nucleocapsid protein solved by the SAIL-NMR method J. Mol. Biol. 380 2008 608 622
39. I.M. Yu, M.L. Oldham, J. Zhang, and J. Chen Crystal structure of the severe acute respiratory syndrome (SARS) coronavirus nucleocapsid protein dimerization domain reveals evolutionary linkage between corona- and arteriviridae J. Biol. Chem. 281 2006 17134 17139
40. T. Kamahora, L.H. Soe, and M.M. Lai Sequence analysis of nucleocapsid gene and leader RNA of human coronavirus OC43 Virus Res. 12 1989 1 9
41. H.C. Hung, C.L. Liu, J.T. Hsu, J.T. Horng, M.Y. Fang, S.Y. Wu, S.H. Ueng, M.Y. Wang, C.W. Yaw, and M.H. Hou Development of an anti-influenza drug screening assay targeting nucleoproteins with tryptophan fluorescence quenching Anal. Chem. 84 2012 6391 6399
42. J. Newman Expanding screening space through the use of alternative reservoirs in vapor-diffusion experiments Acta Crystallogr. D Biol. Crystallogr. 61 2005 490 493
43. I.J. Chen, C.C. Chou, C.L. Liu, C.C. Lee, L.S. Kan, and M.H. Hou Crystallization and preliminary X-ray diffraction analysis of the N-terminal domain of human coronavirus OC43 nucleocapsid protein Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 66 2010 815 818
44. J. Newman Novel buffer systems for macromolecular crystallization Acta Crystallogr. D Biol. Crystallogr. 60 2004 610 612
45. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276 1997 307 326
46. B.W. Matthews Solvent content of protein crystals J. Mol. Biol. 33 1968 491 497
47. M. Sugahara, Y. Asada, K. Shimizu, H. Yamamoto, N.K. Lokanath, H. Mizutani, B. Bagautdinov, Y. Matsuura, M. Taketa, Y. Kageyama, N. Ono, Y. Morikawa, Y. Tanaka, H. Shimada, T. Nakamoto, M. Sugahara, M. Yamamoto, and N. Kunishima High-throughput crystallization-to-structure pipeline at RIKEN SPring-8 Center J. Struct. Funct. Genomics 9 2008 21 28
48. A. Vagin, and A. Teplyakov Molecular replacement with MOLREP Acta Crystallogr. D Biol. Crystallogr. 66 2010 22 25
49. A.T. Brunger, 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 Crystallography & NMR system: A new software suite for macromolecular structure determination Acta Crystallogr. D Biol. Crystallogr. 54 1998 905 921
50. C. Dominguez, R. Boelens, and A.M. Bonvin HADDOCK: A protein-protein docking approach based on biochemical or biophysical information J. Am. Chem. Soc. 125 2003 1731 1737
51. S.C. Keane, P. Liu, J.L. Leibowitz, and D.P. Giedroc Functional transcriptional regulatory sequence (TRS) RNA binding and helix destabilizing determinants of murine hepatitis virus (MHV) nucleocapsid (N) protein J. Biol. Chem. 287 2012 7063 7073
52. N.E. Grossoehme, L. Li, S.C. Keane, P. Liu, C.E. Dann III, J.L. Leibowitz, and D.P. Giedroc Coronavirus N protein N-terminal domain (NTD) specifically binds the transcriptional regulatory sequence (TRS) and melts TRS-cTRS RNA duplexes J. Mol. Biol. 394 2009 544 557
53. Y.W. Tan, S. Fang, H. Fan, J. Lescar, and D.X. Liu Amino acid residues critical for RNA-binding in the N-terminal domain of the nucleocapsid protein are essential determinants for the infectivity of coronavirus in cultured cells Nucleic Acids Res. 34 2006 4816 4825
54. L. Pewe, H. Zhou, J. Netland, C. Tangudu, H. Olivares, L. Shi, D. Look, T. Gallagher, and S. Perlman A severe acute respiratory syndrome-associated coronavirus-specific protein enhances virulence of an attenuated murine coronavirus J. Virol. 79 2005 11335 11342
55. Q. Huang, L. Yu, A.M. Petros, A. Gunasekera, Z. Liu, N. Xu, P. Hajduk, J. Mack, S.W. Fesik, and E.T. Olejniczak Structure of the N-terminal RNA-binding domain of the SARS CoV nucleocapsid protein Biochemistry 43 2004 6059 6063
56. Y. Ma, X. Tong, X. Xu, X. Li, Z. Lou, and Z. Rao Structures of the N- and C-terminal domains of MHV-A59 nucleocapsid protein corroborate a conserved RNA-protein binding mechanism in coronavirus Protein Cell 1 2010 688 697
57. C.K. Chang, Y.L. Hsu, Y.H. Chang, F.A. Chao, M.C. Wu, Y.S. Huang, C.K. Hu, and T.H. Huang Multiple nucleic acid binding sites and intrinsic disorder of severe acute respiratory syndrome coronavirus nucleocapsid protein: Implications for ribonucleocapsid protein packaging J. Virol. 83 2009 2255 2264
58. C.Y. Huang, Y.L. Hsu, W.L. Chiang, and M.H. Hou Elucidation of the stability and functional regions of the human coronavirus OC43 nucleocapsid protein Protein Sci. 18 2009 2209 2218
59. G.W. Nelson, S.A. Stohlman, and S.M. Tahara High affinity interaction between nucleocapsid protein and leader/intergenic sequence of mouse hepatitis virus RNA J. Gen. Virol. 81 2000 181 188
60. J. Pan, X. Peng, Y. Gao, Z. Li, X. Lu, Y. Chen, M. Ishaq, D. Liu, M.L. Dediego, L. Enjuanes, and D. Guo Genome-wide analysis of protein-protein interactions and involvement of viral proteins in SARS-CoV replication PLoS One 3 2008 e3299
61. J.S. Peiris, C.M. Chu, V.C. Cheng, K.S. Chan, I.F. Hung, L.L. Poon, K.I. Law, B.S. Tang, T.Y. Hon, C.S. Chan, K.H. Chan, J.S. Ng, B.J. Zheng, W.L. Ng, R.W. Lai, Y. Guan, and K.Y. Yuen Clinical progression and viral load in a community outbreak of coronavirus-associated SARS pneumonia: A prospective study Lancet 361 2003 1767 1772