Nucleocapsid protein-dependent assembly of the RNA packaging signal of Middle East respiratory syndrome coronavirus

Journal of Biomedical Science

Volumn 25, Issue 1, 2018, Pages

  Hsin, Wei Chen ^a   Chang, Chan Hua ^a   Chang, Chi You ^a   Peng, Wei Hao ^a   Chien, Chung Liang ^a   Chang, Ming Fu ^a   Chang, Shin C ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

MERS CoV; Nucleocapsid protein; RNA packaging signal

Indexed keywords

MESSENGER RNA; NUCLEOCAPSID PROTEIN; NUCLEOTIDE; VIRAL PROTEIN; VIRUS RNA;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BIOINFORMATICS; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ELECTRON MICROSCOPY; EMBRYO; HEK293T CELL LINE; HUH-7 CELL LINE; HUMAN; HUMAN CELL; MIDDLE EAST RESPIRATORY SYNDROME; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN RNA BINDING; RNA PACKAGING; RNA SEQUENCE; RNA STRUCTURE; SARS CORONAVIRUS; SIGNAL TRANSDUCTION; VIRUS ASSEMBLY; VIRUS GENOME; VIRUS MORPHOGENESIS; GENETICS; HEK293 CELL LINE; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE;

CELL LINE, TUMOR; HEK293 CELLS; HUMANS; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; NUCLEOCAPSID PROTEINS; RNA, MESSENGER; RNA, VIRAL; VIRUS ASSEMBLY;

EID: 85047405559     PISSN: 10217770     EISSN: 14230127     Source Type: Journal    
DOI: 10.1186/s12929-018-0449-x     Document Type: Article

References (38)

1. Zaki AM, van Boheemen S, Bestebroer TM, Osterhaus AD, Fouchier RA. Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med. 2012;367:1814-20.
2. Raj VS, Mou H, Smits SL, Dekkers DH, Muller MA, Dijkman R, Muth D, Demmers JA, Zaki A, Fouchier RA, Thiel V, Drosten C, Rottier PJ, Osterhaus AD, Bosch BJ, Haagmans BL. Dipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC. Nature. 2013;495:251-4.
3. Lu G, Hu Y, Wang Q, Qi J, Gao F, Li Y, Zhang Y, Zhang W, Yuan Y, Bao J, Zhang B, Shi Y, Yan J, Gao GF. Molecular basis of binding between novel human coronavirus MERS-CoV and its receptor CD26. Nature. 2013;500:227-31.
4. Pasternak AO, Spaan WJ, Snijder EJ. Nidovirus transcription: how to make sense.? J Gen Virol. 2006;87:1403-21.
5. Stadler K, Masignani V, Eickmann M, Becker S, Abrignani S, Klenk HD, Rappuoli R. SARS - beginning to understand a new virus. Nat Rev Microbiol. 2003;1:209-18.
6. Dires B, Dawo F. Review on Middle East respiratory syndrome. Open Acc Lib J. 2015;2:e1749.
7. Boscarino J, Logan H, Lacny J, Gallagher T. Envelope protein palmitoylations are crucial for murine coronavirus assembly. J Virol. 2008;82:2989-99.
8. de Haan CA, Vennema H, Rottier PJ. Assembly of the coronavirus envelope: homotypic interactions between the M proteins. J Virol. 2000;74:4967-78.
9. Vennema H, Godeke GJ, Rossen JW, Voorhout WF, Horzinek MC, Opstelten DJ, Rottier PJ. Nucleocapsid-independent assembly of coronavirus-like particles by co-expression of viral envelope protein genes. EMBO J. 1996;15:2020-8.
10. Chang CK, Lo SC, Wang YS, Hou MH. Recent insights into the development of therapeutics against coronavirus diseases by targeting N protein. Drug Discov Today. 2016;21:562-72.
11. Kuo L, Koetzner CA, Hurst KR, Masters PS. Recognition of the murine coronavirus genomic RNA packaging signal depends on the second RNA-binding domain of the nucleocapsid protein. J Virol. 2014;88:4451-65.
12. Molenkamp R, Spaan WJM. Identification of a specific interaction between the coronavirus mouse hepatitis virus A59 nucleocapsid protein and packaging signal. Virology. 1997;239:78-86.
13. Fosmire JA, Hwang K, Makino S. Identification and characterization of a coronavirus packaging signal. J Virol. 1992;66:3522-30.
14. Kuo L, Masters PS. Functional analysis of the murine coronavirus genomic RNA packaging signal. J Virol. 2013;87:5182-92.
15. Woo K, Joo M, Narayanan K, Kim KH, Makino S. Murine coronavirus packaging signal confers packaging to nonviral RNA. J Virol. 1997;71:824-7.
16. Cologna R, Hogue BG. Identification of a bovine coronavirus packaging signal. J Virol. 2000;74:580-3.
17. Chen SC, van den Born E, van den Worm SH, Pleij CW, Snijder EJ, Olsthoorn RC. New structure model for the packaging signal in the genome of group IIa coronaviruses. J Virol. 2007;81:6771-4.
18. Chen SC, Olsthoorn RC. Group-specific structural features of the 5'-proximal sequences of coronavirus genomic RNAs. Virology. 2010;401:29-41.
19. Hsieh PK, Chang SC, Huang CC, Lee TT, Hsiao CW, Kou YH, Chen IY, Chang CK, Huang TH, Chang MF. Assembly of severe acute respiratory syndrome coronavirus RNA packaging signal into virus-like particles is nucleocapsid dependent. J Virol. 2005;79:13848-55.
20. Escors D, Izeta A, Capiscol C, Enjuanes L. Transmissible gastroenteritis coronavirus packaging signal is located at the 5′ end of the virus genome. J Virol. 2003;77:7890-902.
21. Morales L, Mateos-Gomez PA, Capiscol C, del Palacio L, Enjuanes L, Sola I. Transmissible gastroenteritis coronavirus genome packaging signal is located at the 5′ end of the genome and promotes viral RNA incorporation into virions in a replication-independent process. J Virol. 2013;87:11579-90.
22. Penzes Z, Tibbles K, Shaw K, Britton P, Brown TD, Cavanagh D. Characterization of a replicating and packaged defective RNA of avian coronavirus infectious bronchitis virus. Virology. 1994;203:286-93.
23. Dalton K, Casais R, Shaw K, Stirrups K, Evans S, Britton P, Brown TD, Cavanagh D. Cis-acting sequences required for coronavirus infectious bronchitis virus defective-RNA replication and packaging. J Virol. 2001;75:125-33.
24. Narayanan K, Chen CJ, Maeda J, Makino S. Nucleocapsid-independent specific viral RNA packaging via viral envelope protein and viral RNA signal. J Virol. 2003;77:2922-7.
25. Narayanan K, Makino S. Cooperation of an RNA packaging signal and a viral envelope protein in coronavirus RNA packaging. J Virol. 2001;75:9059-67.
26. Kuo L, Koetzner C, Masters PS. A key role for the carboxy-terminal tail of the murine coronavirus nucleocapsid protein in coordination of genome packaging. Virology. 2016;494:100-7.
27. Chang MF, Sun CY, Chen CJ, Chang SC. Functional motifs of delta antigen essential for RNA binding and replication of hepatitis delta virus. J Virol. 1993;67:2529-36.
28. Chang CK, Hou MH, Chang CF, Hsiao CD, Huang TH. The SARS coronavirus nucleocapsid protein - forms and functions. Antivir Res. 2014;103:39-50.
29. Papageorgiou N, Lichière J, Baklouti A, Ferron F, Sévajol M, Canard B, Coutard B. Structural characterization of the N-terminal part of the MERS-CoV nucleocapsid by X-ray diffraction and small-angle X-ray scattering. Acta Crystallogr D Struct Biol. 2016;72:192-202.
30. Saikatendu KS, Joseph JS, Subramanian V, Neuman BW, Buchmeier MJ, Stevens RC, Kuhn P. Ribonucleocapsid formation of severe acute respiratory syndrome coronavirus through molecular action of the N-terminal domain of N protein. J Virol. 2007;81:3913-21.
31. Chen CY, Chang CK, Chang YW, Sue SC, Bai HI, Riang L, Hsiao CD, Huang TH. Structure of the SARS coronavirus nucleocapsid protein RNA-binding dimerization domain suggests a mechanism for helical packaging of viral RNA. J Mol Biol. 2007;368:1075-86.
32. Luo H, Chen J, Chen K, Shen X, Jiang H. Carboxyl terminus of severe acute respiratory syndrome coronavirus nucleocapsid protein: self-association analysis and nucleic acid binding characterization. Biochemistry. 2006;45:11827-35.
33. Takeda M, Chang CK, Ikeya T, Güntert P, Chang YH, Hsu YL, Huang TH, Kainosho M. Solution structure of the C-terminal dimerization domain of SARS coronavirus nucleocapsid protein solved by the SAIL-NMR method. J Mol Biol. 2008;380:608-22.
34. Yu IM, Gustafson CL, Diao J, Burgner JW II, Li Z, Zhang J, Chen J. Recombinant severe acute respiratory syndrome (SARS) coronavirus nucleocapsid protein forms a dimer through its C-terminal domain. J Biol Chem. 2005;280:23280-6.
35. Chang CK, Hsu YL, Chang YH, Chao FA, Wu MC, Huang YS, Hu CK, Huang TH. Multiple nucleic acid binding sites and intrinsic disorder of severe acute respiratory syndrome coronavirus nucleocapsid protein: implications for ribonucleocapsid protein packaging. J Virol. 2009;83:2255-64.
36. Chang CK, Sue SC, Yu TH, Hsieh CM, Tsai CK, Chiang YC, Lee SJ, Hsiao HH, Wu WJ, Chang WL, Lin CH, Huang TH. Modular organization of SARS coronavirus nucleocapsid protein. J Biomed Sci. 2006;13:59-72.
37. Hurst K, Koetzner C, Masters P. Identification of in vivo interacting domains of the murine coronavirus nucleocapsid protein. J Virol. 2009;83:7221-34.
38. Ma Y, Tong X, Xu X, Li X, Lou Z, Rao Z. Structures of the N- and C-terminal domains of MHV-A59 nucleocapsid protein corroborate a conserved RNA-protein binding mechanism in coronavirus. Protein Cell. 2010;1:688-97.