Interaction of coronavirus nucleocapsid protein with the 5′‐ and 3′‐ends of the coronavirus genome is involved in genome circularization and negative‐strand RNA synthesis

Synthesis of the negative‐strand ((−)‐strand) counterpart is the first step of coronavirus (CoV) replication; however, the detailed mechanism of the early event and the factors involved remain to be determined. Here, using bovine coronavirus (BCoV)‐defective interfering (DI) RNA, we showed that (a)...

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Published inThe FEBS journal Vol. 286; no. 16; pp. 3222 - 3239
Main Authors Lo, Chen‐Yu, Tsai, Tsung‐Lin, Lin, Chao‐Nan, Lin, Ching‐Hung, Wu, Hung‐Yi
Format Journal Article
LanguageEnglish
Published England Blackwell Publishing Ltd 01.08.2019
John Wiley and Sons Inc
Subjects
(−)‐strand synthesis
Affinity
Animals
binding capacity
Bovine coronavirus
Cattle
Circularity
cis‐acting element
Coronaviridae
coronavirus
Coronavirus, Bovine - genetics
Coronavirus, Bovine - growth & development
Coronaviruses
dissociation
genome
genome circularization
Genome, Viral - genetics
Genomes
N protein
nucleocapsid
nucleocapsid protein
nucleocapsid proteins
Nucleocapsid Proteins - genetics
Nucleocapsids
Nucleotides
Original
Poly A - genetics
Polyadenine
Polyadenylation
Polynucleotides
Proteins
regulatory sequences
Replication
RNA
RNA - biosynthesis
RNA - genetics
RNA, Messenger - genetics
RNA, Viral - genetics
RNA-binding protein
RNA-binding proteins
RNA-Binding Proteins - genetics
Synthesis
Transcription
Virus Replication - genetics
genome circularization
replication
coronavirus
nucleocapsid protein
(−)-strand synthesis
cis-acting element
Online AccessGet full text

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Abstract Synthesis of the negative‐strand ((−)‐strand) counterpart is the first step of coronavirus (CoV) replication; however, the detailed mechanism of the early event and the factors involved remain to be determined. Here, using bovine coronavirus (BCoV)‐defective interfering (DI) RNA, we showed that (a) a poly(A) tail with a length of 15 nucleotides (nt) was sufficient to initiate efficient (−)‐strand RNA synthesis and (b) substitution of the poly(A) tail with poly(U), (C) or (G) only slightly decreased the efficiency of (−)‐strand synthesis. The findings indicate that in addition to the poly(A) tail, other factors acting in trans may also participate in (−)‐strand synthesis. The BCoV nucleocapsid (N) protein, an RNA‐binding protein, was therefore tested as a candidate. Based on dissociation constant (Kd) values, it was found that the binding affinity between N protein, but not poly(A)‐binding protein, and the 3′‐terminal 55 nt plus a poly(A), poly(U), poly(C) or poly(G) tail correlates with the efficiency of (−)‐strand synthesis. Such an association was also evidenced by the binding affinity between the N protein and 5′‐ and 3′‐terminal cis‐acting elements important for (−)‐strand synthesis. Further analysis demonstrated that N protein can act as a bridge to facilitate interaction between the 5′‐ and 3′‐ends of the CoV genome, leading to circularization of the genome. Together, the current study extends our understanding of the mechanism of CoV (−)‐strand RNA synthesis through involvement of N protein and genome circularization and thus may explain why the addition of N protein in trans is required for efficient CoV replication. In the initial stage of coronavirus (CoV) (−)‐strand RNA synthesis, binding of the CoV N protein to the 5′‐ and 3′‐terminal structures of (+)‐strand CoV genome leads to circularization of the genome, serving as a platform to recruit cellular proteins and viral replicase proteins including RNA‐dependent RNA polymerase. This then initiates (−)‐strand RNA synthesis.
AbstractList Synthesis of the negative‐strand ((−)‐strand) counterpart is the first step of coronavirus (CoV) replication; however, the detailed mechanism of the early event and the factors involved remain to be determined. Here, using bovine coronavirus (BCoV)‐defective interfering (DI) RNA, we showed that (a) a poly(A) tail with a length of 15 nucleotides (nt) was sufficient to initiate efficient (−)‐strand RNA synthesis and (b) substitution of the poly(A) tail with poly(U), (C) or (G) only slightly decreased the efficiency of (−)‐strand synthesis. The findings indicate that in addition to the poly(A) tail, other factors acting in trans may also participate in (−)‐strand synthesis. The BCoV nucleocapsid (N) protein, an RNA‐binding protein, was therefore tested as a candidate. Based on dissociation constant (Kd) values, it was found that the binding affinity between N protein, but not poly(A)‐binding protein, and the 3′‐terminal 55 nt plus a poly(A), poly(U), poly(C) or poly(G) tail correlates with the efficiency of (−)‐strand synthesis. Such an association was also evidenced by the binding affinity between the N protein and 5′‐ and 3′‐terminal cis‐acting elements important for (−)‐strand synthesis. Further analysis demonstrated that N protein can act as a bridge to facilitate interaction between the 5′‐ and 3′‐ends of the CoV genome, leading to circularization of the genome. Together, the current study extends our understanding of the mechanism of CoV (−)‐strand RNA synthesis through involvement of N protein and genome circularization and thus may explain why the addition of N protein in trans is required for efficient CoV replication. In the initial stage of coronavirus (CoV) (−)‐strand RNA synthesis, binding of the CoV N protein to the 5′‐ and 3′‐terminal structures of (+)‐strand CoV genome leads to circularization of the genome, serving as a platform to recruit cellular proteins and viral replicase proteins including RNA‐dependent RNA polymerase. This then initiates (−)‐strand RNA synthesis.
Synthesis of the negative‐strand ((−)‐strand) counterpart is the first step of coronavirus (CoV) replication; however, the detailed mechanism of the early event and the factors involved remain to be determined. Here, using bovine coronavirus (BCoV)‐defective interfering (DI) RNA, we showed that (a) a poly(A) tail with a length of 15 nucleotides (nt) was sufficient to initiate efficient (−)‐strand RNA synthesis and (b) substitution of the poly(A) tail with poly(U), (C) or (G) only slightly decreased the efficiency of (−)‐strand synthesis. The findings indicate that in addition to the poly(A) tail, other factors acting in trans may also participate in (−)‐strand synthesis. The BCoV nucleocapsid (N) protein, an RNA‐binding protein, was therefore tested as a candidate. Based on dissociation constant (K d ) values, it was found that the binding affinity between N protein, but not poly(A)‐binding protein, and the 3′‐terminal 55 nt plus a poly(A), poly(U), poly(C) or poly(G) tail correlates with the efficiency of (−)‐strand synthesis. Such an association was also evidenced by the binding affinity between the N protein and 5′‐ and 3′‐terminal cis ‐acting elements important for (−)‐strand synthesis. Further analysis demonstrated that N protein can act as a bridge to facilitate interaction between the 5′‐ and 3′‐ends of the CoV genome, leading to circularization of the genome. Together, the current study extends our understanding of the mechanism of CoV (−)‐strand RNA synthesis through involvement of N protein and genome circularization and thus may explain why the addition of N protein in trans is required for efficient CoV replication. In the initial stage of coronavirus (CoV) (−)‐strand RNA synthesis, binding of the CoV N protein to the 5′‐ and 3′‐terminal structures of (+)‐strand CoV genome leads to circularization of the genome, serving as a platform to recruit cellular proteins and viral replicase proteins including RNA‐dependent RNA polymerase. This then initiates (−)‐strand RNA synthesis.
Synthesis of the negative‐strand ((−)‐strand) counterpart is the first step of coronavirus (CoV) replication; however, the detailed mechanism of the early event and the factors involved remain to be determined. Here, using bovine coronavirus (BCoV)‐defective interfering (DI) RNA, we showed that (a) a poly(A) tail with a length of 15 nucleotides (nt) was sufficient to initiate efficient (−)‐strand RNA synthesis and (b) substitution of the poly(A) tail with poly(U), (C) or (G) only slightly decreased the efficiency of (−)‐strand synthesis. The findings indicate that in addition to the poly(A) tail, other factors acting in trans may also participate in (−)‐strand synthesis. The BCoV nucleocapsid (N) protein, an RNA‐binding protein, was therefore tested as a candidate. Based on dissociation constant (Kd) values, it was found that the binding affinity between N protein, but not poly(A)‐binding protein, and the 3′‐terminal 55 nt plus a poly(A), poly(U), poly(C) or poly(G) tail correlates with the efficiency of (−)‐strand synthesis. Such an association was also evidenced by the binding affinity between the N protein and 5′‐ and 3′‐terminal cis‐acting elements important for (−)‐strand synthesis. Further analysis demonstrated that N protein can act as a bridge to facilitate interaction between the 5′‐ and 3′‐ends of the CoV genome, leading to circularization of the genome. Together, the current study extends our understanding of the mechanism of CoV (−)‐strand RNA synthesis through involvement of N protein and genome circularization and thus may explain why the addition of N protein in trans is required for efficient CoV replication.
Synthesis of the negative-strand ((-)-strand) counterpart is the first step of coronavirus (CoV) replication; however, the detailed mechanism of the early event and the factors involved remain to be determined. Here, using bovine coronavirus (BCoV)-defective interfering (DI) RNA, we showed that (a) a poly(A) tail with a length of 15 nucleotides (nt) was sufficient to initiate efficient (-)-strand RNA synthesis and (b) substitution of the poly(A) tail with poly(U), (C) or (G) only slightly decreased the efficiency of (-)-strand synthesis. The findings indicate that in addition to the poly(A) tail, other factors acting in trans may also participate in (-)-strand synthesis. The BCoV nucleocapsid (N) protein, an RNA-binding protein, was therefore tested as a candidate. Based on dissociation constant (Kd ) values, it was found that the binding affinity between N protein, but not poly(A)-binding protein, and the 3'-terminal 55 nt plus a poly(A), poly(U), poly(C) or poly(G) tail correlates with the efficiency of (-)-strand synthesis. Such an association was also evidenced by the binding affinity between the N protein and 5'- and 3'-terminal cis-acting elements important for (-)-strand synthesis. Further analysis demonstrated that N protein can act as a bridge to facilitate interaction between the 5'- and 3'-ends of the CoV genome, leading to circularization of the genome. Together, the current study extends our understanding of the mechanism of CoV (-)-strand RNA synthesis through involvement of N protein and genome circularization and thus may explain why the addition of N protein in trans is required for efficient CoV replication.Synthesis of the negative-strand ((-)-strand) counterpart is the first step of coronavirus (CoV) replication; however, the detailed mechanism of the early event and the factors involved remain to be determined. Here, using bovine coronavirus (BCoV)-defective interfering (DI) RNA, we showed that (a) a poly(A) tail with a length of 15 nucleotides (nt) was sufficient to initiate efficient (-)-strand RNA synthesis and (b) substitution of the poly(A) tail with poly(U), (C) or (G) only slightly decreased the efficiency of (-)-strand synthesis. The findings indicate that in addition to the poly(A) tail, other factors acting in trans may also participate in (-)-strand synthesis. The BCoV nucleocapsid (N) protein, an RNA-binding protein, was therefore tested as a candidate. Based on dissociation constant (Kd ) values, it was found that the binding affinity between N protein, but not poly(A)-binding protein, and the 3'-terminal 55 nt plus a poly(A), poly(U), poly(C) or poly(G) tail correlates with the efficiency of (-)-strand synthesis. Such an association was also evidenced by the binding affinity between the N protein and 5'- and 3'-terminal cis-acting elements important for (-)-strand synthesis. Further analysis demonstrated that N protein can act as a bridge to facilitate interaction between the 5'- and 3'-ends of the CoV genome, leading to circularization of the genome. Together, the current study extends our understanding of the mechanism of CoV (-)-strand RNA synthesis through involvement of N protein and genome circularization and thus may explain why the addition of N protein in trans is required for efficient CoV replication.
Synthesis of the negative‐strand ((−)‐strand) counterpart is the first step of coronavirus (CoV) replication; however, the detailed mechanism of the early event and the factors involved remain to be determined. Here, using bovine coronavirus (BCoV)‐defective interfering (DI) RNA, we showed that (a) a poly(A) tail with a length of 15 nucleotides (nt) was sufficient to initiate efficient (−)‐strand RNA synthesis and (b) substitution of the poly(A) tail with poly(U), (C) or (G) only slightly decreased the efficiency of (−)‐strand synthesis. The findings indicate that in addition to the poly(A) tail, other factors acting in trans may also participate in (−)‐strand synthesis. The BCoV nucleocapsid (N) protein, an RNA‐binding protein, was therefore tested as a candidate. Based on dissociation constant (K d ) values, it was found that the binding affinity between N protein, but not poly(A)‐binding protein, and the 3′‐terminal 55 nt plus a poly(A), poly(U), poly(C) or poly(G) tail correlates with the efficiency of (−)‐strand synthesis. Such an association was also evidenced by the binding affinity between the N protein and 5′‐ and 3′‐terminal cis ‐acting elements important for (−)‐strand synthesis. Further analysis demonstrated that N protein can act as a bridge to facilitate interaction between the 5′‐ and 3′‐ends of the CoV genome, leading to circularization of the genome. Together, the current study extends our understanding of the mechanism of CoV (−)‐strand RNA synthesis through involvement of N protein and genome circularization and thus may explain why the addition of N protein in trans is required for efficient CoV replication.
Synthesis of the negative-strand ((-)-strand) counterpart is the first step of coronavirus (CoV) replication; however, the detailed mechanism of the early event and the factors involved remain to be determined. Here, using bovine coronavirus (BCoV)-defective interfering (DI) RNA, we showed that (a) a poly(A) tail with a length of 15 nucleotides (nt) was sufficient to initiate efficient (-)-strand RNA synthesis and (b) substitution of the poly(A) tail with poly(U), (C) or (G) only slightly decreased the efficiency of (-)-strand synthesis. The findings indicate that in addition to the poly(A) tail, other factors acting in trans may also participate in (-)-strand synthesis. The BCoV nucleocapsid (N) protein, an RNA-binding protein, was therefore tested as a candidate. Based on dissociation constant (K ) values, it was found that the binding affinity between N protein, but not poly(A)-binding protein, and the 3'-terminal 55 nt plus a poly(A), poly(U), poly(C) or poly(G) tail correlates with the efficiency of (-)-strand synthesis. Such an association was also evidenced by the binding affinity between the N protein and 5'- and 3'-terminal cis-acting elements important for (-)-strand synthesis. Further analysis demonstrated that N protein can act as a bridge to facilitate interaction between the 5'- and 3'-ends of the CoV genome, leading to circularization of the genome. Together, the current study extends our understanding of the mechanism of CoV (-)-strand RNA synthesis through involvement of N protein and genome circularization and thus may explain why the addition of N protein in trans is required for efficient CoV replication.
Author Lin, Chao‐Nan
Lin, Ching‐Hung
Tsai, Tsung‐Lin
Wu, Hung‐Yi
Lo, Chen‐Yu
AuthorAffiliation 1 Graduate Institute of Veterinary Pathobiology College of Veterinary Medicine National Chung Hsing University Taichung Taiwan
2 Department of Veterinary Medicine National Pingtung University of Science and Technology Neipu Pingtung Taiwan
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Issue 16
Keywords genome circularization
replication
coronavirus
nucleocapsid protein
(−)-strand synthesis
cis-acting element
Language English
License 2019 Federation of European Biochemical Societies.
This article is being made freely available through PubMed Central as part of the COVID-19 public health emergency response. It can be used for unrestricted research re-use and analysis in any form or by any means with acknowledgement of the original source, for the duration of the public health emergency.
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Snippet Synthesis of the negative‐strand ((−)‐strand) counterpart is the first step of coronavirus (CoV) replication; however, the detailed mechanism of the early...
Synthesis of the negative-strand ((-)-strand) counterpart is the first step of coronavirus (CoV) replication; however, the detailed mechanism of the early...
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wiley
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StartPage 3222
SubjectTerms (−)‐strand synthesis
Affinity
Animals
binding capacity
Bovine coronavirus
Cattle
Circularity
cis‐acting element
Coronaviridae
coronavirus
Coronavirus, Bovine - genetics
Coronavirus, Bovine - growth & development
Coronaviruses
dissociation
genome
genome circularization
Genome, Viral - genetics
Genomes
N protein
nucleocapsid
nucleocapsid protein
nucleocapsid proteins
Nucleocapsid Proteins - genetics
Nucleocapsids
Nucleotides
Original
Poly A - genetics
Polyadenine
Polyadenylation
Polynucleotides
Proteins
regulatory sequences
Replication
RNA
RNA - biosynthesis
RNA - genetics
RNA, Messenger - genetics
RNA, Viral - genetics
RNA-binding protein
RNA-binding proteins
RNA-Binding Proteins - genetics
Synthesis
Transcription
Virus Replication - genetics
Title Interaction of coronavirus nucleocapsid protein with the 5′‐ and 3′‐ends of the coronavirus genome is involved in genome circularization and negative‐strand RNA synthesis
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Ffebs.14863
https://www.ncbi.nlm.nih.gov/pubmed/31034708
https://www.proquest.com/docview/2274950515
https://www.proquest.com/docview/2217492973
https://www.proquest.com/docview/2388788950
https://pubmed.ncbi.nlm.nih.gov/PMC7164124
Volume 286
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