Dissimilation of synonymous codon usage bias in virus–host coevolution due to translational selection

Chen, F; Wu, Peng; Deng, S.Z.; Zhang, H; Hou, Yiling; Hu, Zheng; Zhang, J; Chen, X; Yang, Jinfu

doi:10.1038/s41559-020-1124-7

Cited by 90 publications

(113 citation statements)

References 69 publications

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“…The consumption of specific tRNAs for the virus replication could thus be an alternative to controlling host protein synthesis machinery as well as generating deleterious collateral effects on the function of the host cells. Recent evidence supports the idea that high codon usage similarity between virus and host can lead to a deleterious effect on the host (Chen et al, 2020). Furthermore, Chen et al (2020) have shown that codon composition of highly expressed viral genes regulates the tRNA availability, affecting the decoding time of codons in the infected cells.…”

Section: Introductionmentioning

confidence: 77%

“…Recent evidence supports the idea that high codon usage similarity between virus and host can lead to a deleterious effect on the host (Chen et al, 2020). Furthermore, Chen et al (2020) have shown that codon composition of highly expressed viral genes regulates the tRNA availability, affecting the decoding time of codons in the infected cells. In this manner the viral infection can convert abundant codons into scarce codons, reshaping the human codon optimality pattern.…”

Section: Introductionmentioning

confidence: 77%

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SARS-CoV-2 Codon Usage Bias Downregulates Host Expressed Genes With Similar Codon Usage

Alonso

Diambra

2020

Front. Cell Dev. Biol.

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Severe acute respiratory syndrome has spread quickly throughout the world and was declared a pandemic by the World Health Organization (WHO). The pathogenic agent is a new coronavirus (SARS-CoV-2) that infects pulmonary cells with great effectiveness. In this study we focus on the codon composition for the viral protein synthesis and its relationship with the protein synthesis of the host. Our analysis reveals that SARS-CoV-2 preferred codons have poor representation of G or C nucleotides in the third position, a characteristic which could result in an unbalance in the tRNAs pools of the infected cells with serious implications in host protein synthesis. By integrating this observation with proteomic data from infected cells, we observe a reduced translation rate of host proteins associated with highly expressed genes and that they share the codon usage bias of the virus. The functional analysis of these genes suggests that this mechanism of epistasis can contribute to understanding how this virus evades the immune response and the etiology of some deleterious collateral effect as a result of the viral replication. In this manner, our finding contributes to the understanding of the SARS-CoV-2 pathogeny and could be useful for the design of a vaccine based on the live attenuated strategy.

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Section: Introductionmentioning

confidence: 77%

Section: Introductionmentioning

confidence: 77%

SARS-CoV-2 Codon Usage Bias Downregulates Host Expressed Genes With Similar Codon Usage

Alonso

Diambra

2020

Front. Cell Dev. Biol.

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“…because having codon usage similar to their host would allow them to replicate faster due to better translation efficiency of their mRNA(s) 11 . However, it is worth noting that viral codon usage often does not closely resemble the codon usage of their hosts 12,13 , a phenomenon that is not well understood.…”

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confidence: 99%

Sequence analysis of SARS-CoV-2 genome reveals features important for vaccine design

Kames

Holcomb

Kimchi

et al. 2020

Sci Rep

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As the SARS-CoV-2 pandemic is rapidly progressing, the need for the development of an effective vaccine is critical. A promising approach for vaccine development is to generate, through codon pair deoptimization, an attenuated virus. This approach carries the advantage that it only requires limited knowledge specific to the virus in question, other than its genome sequence. Therefore, it is well suited for emerging viruses, for which we may not have extensive data. We performed comprehensive in silico analyses of several features of SARS-CoV-2 genomic sequence (e.g., codon usage, codon pair usage, dinucleotide/junction dinucleotide usage, RNA structure around the frameshift region) in comparison with other members of the coronaviridae family of viruses, the overall human genome, and the transcriptome of specific human tissues such as lung, which are primarily targeted by the virus. Our analysis identified the spike (S) and nucleocapsid (N) proteins as promising targets for deoptimization and suggests a roadmap for SARS-CoV-2 vaccine development, which can be generalizable to other viruses.

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“…On the other hand, given the similarity of SARS-CoV-2 SDA with the phylogenetically closest bat coronavirus, it seems that a translational selection to increase SDA would have acted before the putative zoonosis from bats or other intermediate hosts. Furthermore, in agreement with the highest translational potential of SARS-CoV-2 in their target tissues, a recent model of viral tropism suggested that a tradeoff exists between the efficiency of viral translation and the translational load on the host, indicating that an improved codon usage can make the difference between symptomatic and natural hosts 51 .…”

Section: Discussionmentioning

confidence: 60%

Translational adaptation of human viruses to the tissues they infect

Hernandez‐Alias

Schaefer

Serrano

2020

Preprint

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Viruses need to hijack the translational machinery of the host cell for a productive infection to happen. However, given the dynamic landscape of tRNA pools among tissues, it is unclear whether different viruses infecting different tissues have adapted their codon usage toward their tropism. Here, we collect the coding sequences of over 500 human-infecting viruses and determine that tropism explains changes in codon usage. Using an in silico model of translational efficiency, we validate the correspondence of the viral codon usage with the translational machinery of their tropism. In particular, we propose that the improved translational adaptation to the upper respiratory airways of the pandemic agent SARS-CoV-2 coronavirus could enhance its transmissibility. Furthermore, this correspondence is specifically defined in early viral proteins, as upon infection cells undergo reprogramming of tRNA pools that favors the translation of late counterparts.

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Dissimilation of synonymous codon usage bias in virus–host coevolution due to translational selection

Cited by 90 publications

References 69 publications

SARS-CoV-2 Codon Usage Bias Downregulates Host Expressed Genes With Similar Codon Usage

SARS-CoV-2 Codon Usage Bias Downregulates Host Expressed Genes With Similar Codon Usage

Sequence analysis of SARS-CoV-2 genome reveals features important for vaccine design

Translational adaptation of human viruses to the tissues they infect

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