Translational Adaptation of Human Viruses to the Tissues They Infect

Overview

Journal Cell Rep

Publisher Cell Press

Specialties Biology
Cell Biology
Molecular Biology

Date 2021 Mar 17

PMID 33730572

Citations 16

Authors

Xavier Hernandez-Alias

Hannah Benisty

Martin H Schaefer

Luis Serrano

Affiliations

Soon will be listed here.

Abstract

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 502 human-infecting viruses and determine that tropism explains changes in codon usage. Using the tRNA abundances across 23 human tissues from The Cancer Genome Atlas (TCGA), we build an in silico model of translational efficiency that validates the correspondence of the viral codon usage with the translational machinery of their tropism. For instance, we detect that severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is specifically adapted to the upper respiratory tract and alveoli. Furthermore, this correspondence is specifically defined in early viral proteins. The observed tissue-specific translational efficiency could be useful for the development of antiviral therapies and vaccines.

Citing Articles

Computational Analysis of MDR1 Variants Predicts Effect on Cancer Cells via their Effect on mRNA Folding.

Gutman T, Tuller T PLoS Comput Biol. 2024; 20(12):e1012685.

PMID: 39724131 PMC: 11670953. DOI: 10.1371/journal.pcbi.1012685.

tRNA-Ser-UGA efficiently promotes the rapid release of duck hepatitis A virus from infected enterocytes and its remote dissemination to hepatocytes.

Ou X, Gou Y, Gong L, Lin X, Liu Y, Yang W Poult Sci. 2024; 104(2):104655.

PMID: 39708671 PMC: 11729666. DOI: 10.1016/j.psj.2024.104655.

Why HPV16? Why, now, HPV42? How the discovery of HPV42 in rare cancers provides an opportunity to challenge our understanding about the transition between health and disease for common members of the healthy microbiota.

Bravo I, Belkhir S, Paget-Bailly P FEMS Microbiol Rev. 2024; 48(6).

PMID: 39562287 PMC: 11644485. DOI: 10.1093/femsre/fuae029.

SARS-CoV-2 Displays a Suboptimal Codon Usage Bias for Efficient Translation in Human Cells Diverted by Hijacking the tRNA Epitranscriptome.

Eldin P, David A, Hirtz C, Battini J, Briant L Int J Mol Sci. 2024; 25(21).

PMID: 39519170 PMC: 11546939. DOI: 10.3390/ijms252111614.

mRNA Technology and Mucosal Immunization.

Toniolo A, Maccari G, Camussi G Vaccines (Basel). 2024; 12(6).

PMID: 38932399 PMC: 11209623. DOI: 10.3390/vaccines12060670.

References

Lorenz R, Bernhart S, Honer Zu Siederdissen C, Tafer H, Flamm C, Stadler P . ViennaRNA Package 2.0. Algorithms Mol Biol. 2011; 6:26. PMC: 3319429. DOI: 10.1186/1748-7188-6-26. View

Mioduser O, Goz E, Tuller T . Significant differences in terms of codon usage bias between bacteriophage early and late genes: a comparative genomics analysis. BMC Genomics. 2017; 18(1):866. PMC: 5683454. DOI: 10.1186/s12864-017-4248-7. View

Alexaki A, Kames J, Holcomb D, Athey J, Santana-Quintero L, Lam P . Codon and Codon-Pair Usage Tables (CoCoPUTs): Facilitating Genetic Variation Analyses and Recombinant Gene Design. J Mol Biol. 2019; 431(13):2434-2441. DOI: 10.1016/j.jmb.2019.04.021. View

Raj V, Mou H, Smits S, Dekkers D, Muller M, Dijkman R . Dipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC. Nature. 2013; 495(7440):251-4. PMC: 7095326. DOI: 10.1038/nature12005. View

Dos Reis M, Savva R, Wernisch L . Solving the riddle of codon usage preferences: a test for translational selection. Nucleic Acids Res. 2004; 32(17):5036-44. PMC: 521650. DOI: 10.1093/nar/gkh834. View

Pavon-Eternod M, David A, Dittmar K, Berglund P, Pan T, Bennink J . Vaccinia and influenza A viruses select rather than adjust tRNAs to optimize translation. Nucleic Acids Res. 2012; 41(3):1914-21. PMC: 3561966. DOI: 10.1093/nar/gks986. View

Wang K, Chen W, Zhang Z, Deng Y, Lian J, Du P . CD147-spike protein is a novel route for SARS-CoV-2 infection to host cells. Signal Transduct Target Ther. 2020; 5(1):283. PMC: 7714896. DOI: 10.1038/s41392-020-00426-x. View

Morgado S, Vicente A . Global Scenario of tRNA Genes and Their Organization in Virus Genomes. Viruses. 2019; 11(2). PMC: 6409571. DOI: 10.3390/v11020180. View

Zhou P, Yang X, Wang X, Hu B, Zhang L, Zhang W . A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature. 2020; 579(7798):270-273. PMC: 7095418. DOI: 10.1038/s41586-020-2012-7. View

10.

Li Y, Bai W, Hashikawa T . The neuroinvasive potential of SARS-CoV2 may play a role in the respiratory failure of COVID-19 patients. J Med Virol. 2020; 92(6):552-555. PMC: 7228394. DOI: 10.1002/jmv.25728. View

11.

Broszeit F, Tzarum N, Zhu X, Nemanichvili N, Eggink D, Leenders T . N-Glycolylneuraminic Acid as a Receptor for Influenza A Viruses. Cell Rep. 2019; 27(11):3284-3294.e6. PMC: 6750725. DOI: 10.1016/j.celrep.2019.05.048. View

12.

Athey J, Alexaki A, Osipova E, Rostovtsev A, Santana-Quintero L, Katneni U . A new and updated resource for codon usage tables. BMC Bioinformatics. 2017; 18(1):391. PMC: 5581930. DOI: 10.1186/s12859-017-1793-7. View

13.

Chan P, Lowe T . tRNAscan-SE: Searching for tRNA Genes in Genomic Sequences. Methods Mol Biol. 2019; 1962:1-14. PMC: 6768409. DOI: 10.1007/978-1-4939-9173-0_1. View

14.

Lauring A, Jones J, Andino R . Rationalizing the development of live attenuated virus vaccines. Nat Biotechnol. 2010; 28(6):573-9. PMC: 2883798. DOI: 10.1038/nbt.1635. View

15.

Stark T, Arnold J, Spector D, Yeo G . High-resolution profiling and analysis of viral and host small RNAs during human cytomegalovirus infection. J Virol. 2011; 86(1):226-35. PMC: 3255895. DOI: 10.1128/JVI.05903-11. View

16.

Bergman S, Tuller T . Widespread non-modular overlapping codes in the coding regions. Phys Biol. 2020; 17(3):031002. DOI: 10.1088/1478-3975/ab7083. View

17.

Chang S, Thomas M, Sova P, Green R, Palermo R, Katze M . Next-generation sequencing of small RNAs from HIV-infected cells identifies phased microrna expression patterns and candidate novel microRNAs differentially expressed upon infection. mBio. 2013; 4(1):e00549-12. PMC: 3560529. DOI: 10.1128/mBio.00549-12. View

18.

Zhao K, Gu W, Fang N, Saunders N, Frazer I . Gene codon composition determines differentiation-dependent expression of a viral capsid gene in keratinocytes in vitro and in vivo. Mol Cell Biol. 2005; 25(19):8643-55. PMC: 1265747. DOI: 10.1128/MCB.25.19.8643-8655.2005. View

19.

Weekes M, Tomasec P, Huttlin E, Fielding C, Nusinow D, Stanton R . Quantitative temporal viromics: an approach to investigate host-pathogen interaction. Cell. 2014; 157(6):1460-1472. PMC: 4048463. DOI: 10.1016/j.cell.2014.04.028. View

20.

Gogakos T, Brown M, Garzia A, Meyer C, Hafner M, Tuschl T . Characterizing Expression and Processing of Precursor and Mature Human tRNAs by Hydro-tRNAseq and PAR-CLIP. Cell Rep. 2017; 20(6):1463-1475. PMC: 5564215. DOI: 10.1016/j.celrep.2017.07.029. View