Mechanisms and regulation of RNA virus recombination
Keywords:
RNA viruses, retroviruses, replicative recombination, nonreplicative recombination, template switching, recombination hotspotsAbstract
This review attempts to summarize the most important data concerning of molecular mechanisms and regulation of the viral recombination. Two mechanisms are responsible for RNA virus recombination, specifically replicative recombination based on replicase template switching and nonreplicative joining among fragments of viral origin. Retroviruses recombination occurs during DNA synthesis, whereby reverse transcriptase undergoes template switching between the two copackaged RNAs, However numerous questions about molecular mechanisms of RNA recombination remain unanswered. RNA recombination is one of the driving forces of genetic variability and virus evolution. But significant differences in recombination frequency were observed among various RNA viruses and retroviruses. We do not understand conclusively why the frequency of RNA recombination varies so much among RNA viruses but the data summarized in this review support the hypothesis according to which not only selection forces plays a role in the determination of the recombination rate.Numerous virus and host factors were found to affect the rate of viral RNA recombinants and the distribution of recombination breakpoints.
References
Weaver SC., Kang W., Shirako Y., Rumenapf T., Strauss EG., Strauss JH. Recombinational history and molecular evolution of western equine encephalomyelitis complex alphaviruses // J. Virol. 1997. Vol.71. Р.613-636.
Jackwood MW., Hall D., Handel A. Molecular evolution and emergence of avian gammacoronaviruses // Infect. Genet. Evol. 2012. Vol.12(6). P.1305-1316.
Lefeuvre P., Moriones E. Recombination as a motor of host switches and virus emergence: geminiviruses as case studies // Curr. Opin. Virol. 2015. Vol.10. P.14–19.
Koonin EV., Dolja VV., Krupovic M. Origins and evolution of viruses of eukaryotes // The ultimate modularity Virology. 2015. Vol.479–480. P.2-25.
Khatchikian D., Orlich M., Rott R. Increased viral pathogenicity after insertion of a 28S ribosomal RNA sequence into the haemagglutinin gene of an influenza virus // Nature. 1989. Vol.340. Р.156–157.
Malim MH., Emerman M. HIV-1 sequence variation: drift, shift, and attenuation // Cell. 2001. Vol.104. P.469–472.
Nora T., Charpentier C., Tenaillon O., Hoede C., Clavel F., Hance A.J. Contribution of recombination to the evolution of human immunodeficiency viruses expressing resistance to antiretroviral treatment // J. Virol. 2007. Vol.81. P.7620-7628.
Krupovic M., Dolja VV., Koonin EV. Plant viruses of the Amalgaviridae family evolved via recombination between viruses with double-stranded and negative-strand RNA genomes // Biol Direct. 2015. Vol.10. P.12.
Qin XC., Shi M., Tian JH., Lin XD., Gao DY., He JR., Wang JB., Li CX., Kang YJ., Yu B., Zhou DJ., Xu J., Plyusnin A., Holmes EC., Zhang YZ. A tick-borne segmented RNA virus contains genome segments derived from unsegmented viral ancestors // Proc. Natl. Acad. Sci. U S A. 2014. Vol.111. P.6744-6753.
Diemer GS. Stedman KM. A novel virus genome discovered in an extreme environment suggests recombination between unrelated groups of RNA and DNA viruses // Biol. Direct. 2012. Vol.7. P.13.
Krupovic M., Koonin EV. Evolution of eukaryotic single-stranded DNA viruses of the Bidnaviridae family from genes of four other groups of widely different viruses // Sci. Rep. 2014. Vol.4. P. 5347.
Simon-Loriere E., Holmes EC. Why do RNA viruses recombine? // Nat. Rev. Microbiol. 2011. Vol.9. P.617-643.
Nagy PD., Bujarski JJ. Targeting the site of RNA-RNA recombination in brome mosaic virus with antisense sequences // Proc. Natl. Acad. Sci. U.S.A. 1993. Vol.90. P.6390–6394.
Sztuba-Solinska J., Fanning SW., Horn JR., Bujarski JJ. Mutations in the coat protein-binding cis-acting RNA motifs debilitate RNA recombination of Brome mosaic virus // Virus Res. 2012. Vol.170. P.138–149.
Khatchikian D., Orlich M., Rott R. Increased viral pathogenicity after insertion of a 28S ribosomal RNA sequence into the haemagglutinin gene of an influenza virus //Nature. 1989. Vol.340. P.156–157.
Woo PC., Lau SK., Huang Y., Yuen KY. Coronavirus diversity, phylogeny and interspecies jumping // Exp. Biol. Med. (Maywood). 2009. Vol. 234. P.1117-1144.
Taucher C., Berger A., Mandl CW. A trans-complementing recombination trap demonstrates a lowpropensity of flaviviruses for intermolecular recombination // J. Virol. 2010. Vol.84. P.599–611.
Lukashev AN. Recombination among picornaviruses // Rev. Med. Virol. 2010. Vol.20. P.327–337.
Simmonds P., Welch J. Frequency and dynamics of recombination within different species of human enteroviruses // J. Virol. 2006. Vol.80(1). P.483-576.
Urbanowicz A. [et al.] Homologous crossovers among molecules of brome mosaic bromovirus RNA1 or RNA2 segments in vivo // J. Virol. 2005. Vol.79. P.5732–5742.
Gibbs A., Ohshima K. Potyviruses and the digital revolution // Annu Rev. Phytopathol. 2010. Vol.48. P.205–223.
Desbiez C., Lecoq H. Evidence for multiple intraspecific recombinants in natural populations of Watermelon mosaic virus (WMV, Potyvirus) // Arch Virol. 2008. Vol.153(9). P.1749-1803.
Tanne E. Occurrence of a DNA sequence of a non-retro RNA virus in a host plant genome and its expression: evidence for recombination between viral and host RNAs // Virology. 2005. Vol.332. P. 614-636.
Gallei A., Pankraz A., Thiel H-J., Becher P. RNA recombination in vivo in the absence of viral replication // J. Virol. 2004. Vol.78. P.6271–6281.
Gmyl AP. [et al.] Nonreplicative RNA recombination in poliovirus. J. Virol. 73:8958–8965. Gmyl AP, Korshenko SA, Belousov EV, Khitrina EV, Agol VI. 2003. Nonreplicative homologous RNA recombination: promiscuous joining of RNA pieces? // RNA. 1999. Vol. 9. P.1221–1231.
Scheel TKH. [et al.] Productive Homologous and Non-homologous Recombination of Hepatitis C Virus in Cell Culture // PLoS Pathog. 2013. Vol.9. P.e1003228.
Kleine Büning M., Meyer D., Austermann-Busch S., Roman-Sosa G., Rümenapf T., Becher P. Nonreplicative RNA Recombination of an Animal Plus-Strand RNA Virus in the Absence of Efficient Translation of Viral Proteins // Genome Biol Evol. 2017. Vol.9(4). P.817-829.
Li WM., Barnes T., Lee CH. Endoribonucleases--enzymes gaining spotlight in mRNA metabolism // FEBS J. 2010. Vol.277. P.627–641.
Beckham CJ., Parker R. P bodies, stress granules, and viral life cycles // Cell. Host. Microbe. 2008. Vol.3. P.206–212.
Monroe SS., Schlesinger S. RNAs from two independently isolated defective interfering particles of Sindbis virus contain a cellular tRNA sequence at their 5' ends // Proc. Natl. Acad. Sci. US A. 1983. Vol.80. P.3279-3362.
Becher P., Tautz N. RNA recombination in pestiviruses: cellular RNA sequences in viral genomes highlight the role of host factors for viral persistence and lethal disease // RNA Biol. 2011. Vol.8. P.216–224.
Koonin EV., Dolja VV., Krupovic M. Origins and Evolution of Viruses of Eukaryotes: The Ultimate Modularity // Virology. 2015. Vol. 479-480. P. 2–25.
Krupovic M., Dolja VV., Koonin EV. Plant Viruses of the Amalgaviridae Family Evolved via Recombination Between Viruses with Double-Stranded and Negative-Strand RNA Genomes // Biology Direct. 2015. Vol.10. P. 12.
Zhuang, J., Jetzt AE., Sun G., Yu H., Klarmann G., Ron Y., Preston BD., Dougherty JP. Human immunodeficiency virus type 1 recombination: Rate, fidelity, and putative hot spots // J. Virol. 2002. Vol.76. P.11273–11282.
Delviks-Frankenberry K., Galli A., Nikolaitchik O., Mens H., Pathak VK., Hu WS. Mechanisms and factors that influence high frequency retroviral recombination // Viruses. 2011. Vol.3. P.1650–1680.
Rhodes T., Wargo H., Hu W-S. High rates of human immunodeficiency virus type 1 recombination: near-random segregation of markers one kilobase apart in one round of viral replication // J. Virol. 2003. Vol.77. P.11193–11200.
Flynn JA., An W., King SR., Telesnitsky A. Nonrandom dimerization of murine leukemia virus genomic RNAs // J. Virol. 2004. Vol.78. P. 12129–12139.
Anderson JA., Pathak VK., Hu WS. Effect of the murine leukemia virus extended packaging signal on the rates and locations of retroviral recombination // J. Virol. 2000. Vol.74. P. 6953–6963.
Webster B., Ott M., Greene WC. Evasion of superinfection exclusion and elimination of primary viral RNA by an adapted strain of hepatitis C virus // J. Virol. 2013. Vol.87. P.13354–13369.
Jung A., Maier R., Vartanian JP., Bocharov G., Jung V., Fischer U., Meese E., Wain-Hobson S., Meyerhans, A. Recombination: Multiply infected spleen cells in HIV patients // Nature. 2002. Vol.418. P. 144.
Hu WS., Temin HM. Genetic consequences of packaging two RNA genomes in one retroviral particle: Pseudodiploidy and high rate of genetic recombination // Proc. Natl. Acad. Sci. USA. 1990. Vol.87. P.1556–1616.
Dang Q., Chen J., Unutmaz D., Coffin JM., Pathak VK., Powell D. [et al.] Nonrandom HIV-1 infection and double infection via direct and cell-mediated pathways // Proc. Natl. Acad. Sci. USA. 2004. Vol.101. P.632–639.
Haqqani AA., Marek SL., Kumar J., Davenport M., Wang H., Tilton JC. Central memory CD4+ T cells are preferential targets of double infection by HIV-1 // Virol J. 2015. Vol.12. P.184.
Moore MD., Nikolaitchik OA., Chen J., Hammarskjöld ML., Rekosh D., Hu WS. Probing the HIV-1 genomic RNA trafficking pathway and dimerization by genetic recombination and single virion analyses // PLoS Pathog. 2009. Vol.5. P.e1000627.
Song R., Kafaie J., Yang L., Laughrea M. HIV-1 viral RNA is selected in the form of monomers that dimerize in a three-step proteasedependent process. The DIS of stem-loop 1 initiates viral RNA dimerization // J. Mol. Biol. 2007. Vol.371. P.1084–1098.
Piekna-Przybylska D., Sharma G., Bambara RA. Mechanism of HIV-1 RNA dimerization in the central region of the genome and significance for viral evolution // J. Biol. Chem. 2013. Vol.288(33). P.24140-24190.
Lizna M., Tahir A., Farah Mustafa. Cross- and Co-Packaging of Retroviral RNAs and Their Consequences // Viruses. 2016. Vol.8(10). P.E276.
Yin PD., Hu WS. RNAs from genetically distinct retroviruses can copackage and exchange genetic information in vivo // J. Virol. 1997. Vol.71. P.6237–6242.
Yang S., Temin HM. A double hairpin structure is necessary for the efficient encapsidation of spleen necrosis virus retroviral RNA //EMBO J. 1994. Vol.13. P.713–726.
Motomura K., Chen J., Hu W.-S. Genetic Recombination between Human Immunodeficiency Virus Type 1 (HIV-1) and HIV-2, Two Distinct Human Lentiviruses // J. Virol. 2008. Vol.82. P.1923–1933.
Malik HS., Henikoff S., Eickbush TH. Poised for contagion: evolutionary origins of the infectious abilities of invertebrate retroviruses // Genome Res. 2000. Vol.10. P.1307–1325.
Ribet D., Harper F., Dupressoir A., Dewannieux M., Pierron G., Heidmann T. An infectious progenitor for the murine IAP retrotransposon: emergence of an intracellular genetic parasite from an ancient retrovirus // Genome Res. 2008. Vol.18. P.597–609.
Tan S., Cardoso-Moreira M., Shi W., Zhang D., Huang J., Mao Y., Jia H., Zhang Y., Chen C., Shao Y., Leng L., Liu Z., Huang X., Long M., Zhang YE. LTR-mediated retroposition as a mechanism of RNA-based duplication in metazoans // Genome Res. 2016. Vol. 26. P.1663-1675.
Takebe Y., Telesnitsky A. Evidence for the acquisition of multi-drug resistance in an HIV-1 clinical isolate via human sequence transduction // Virology. 2006. Vol.351. P.1-6.
Megens S., Vaira D., De Baets G., Dekeersmaeker N., Schrooten Y., Li G., Schymkowitz J., Rousseau F., Vandamme AM., Moutschen M. [et al.] Horizontal gene transfer from human host to HIV-1 reverse transcriptase confers drug resistance and partly compensates for replication deficits // Virology. 2014. Vol.456. P. 310–318.
Muriaux D., Rein A. Encapsidation and transduction of cellular genes by retroviruses // Front Biosci. 2003. Vol.8. P. d135-177.
Collett MS., Erikson RL. Protein kinase activity associated with the avian sarcoma virus src gene product // Proc. Natl. Acad. Sci. USA. 1978. Vol.75. P.2021–2024.
Bujarski JJ. Genetic recombination in plant-infecting messenger-sense RNA viruses: overview and research perspectives // Front Plant. Sci. 2013. Vol.26(4). P.68.
Mine A., Okuno T. Composition of plant virus RNA replicase complexes. Curr. Opin. Virol. 2012. Vol.2. P. 663–669.
Prasanth KR., Kovalev N., de Castro Martín IF., Baker J., Nagy PD. Screening a yeast library of temperature-sensitive mutants reveals a role for actin in tombusvirus RNA recombination // Virology. 2016. Vol.489. P.233-275.
Cheng CP., Serviene E., Nagy PD. Suppression of viral RNA recombination by a host exoribonuclease // J. Virol. 2006. Vol.80. P.2631–2640.
Cheng CP., Jaag HM., Jonczyk M., Serviene E., Nagy PD. Expression of the Arabidopsis Xrn4p 5'-3' exoribonuclease facilitates degradation of tombusvirus RNA and promotes rapid emergence of viral variants in plants // Virology. 2007. Nov 25. Vol.368(2). P.238-286.
Jaag HM., Pogany J., Nagy PD. A host Ca2+/Mn2+ ion pump is a factor in the emergence of viralRNA recombinants // Cell Host Microbe. 2010. Vol. 7. P.74–81.
Chuang C., Barajas D., Qin J., Nagy PD. Inactivation of the host lipin gene accelerates RNA virus replication through viral exploitation of the expanded endoplasmic reticulum membrane // PLoS Pathog. 2014. Vol.10 (2). P. e1003944.
Smyth RP., Davenport MP., Mak J. The origin of genetic diversity in hiv-1 // Virus Res. 2012. Vol.169. P. 415–429.
Nguyen LA., Kim DH., Daly MB., Allan KC., Kim B. Host SAMHD1 protein promotes HIV-1 recombination in macrophages // J. Biol. Chem. 2014. Vol.289(5). P.2489-2575.
Cromer D., Schlub TE., Smyth RP., Grimm AJ., Chopra A., Mallal S., Davenport MP., Mak J. HIV-1 Mutation and Recombination Rates Are Different in Macrophages and T-cells // Viruses. 2016. Vol.8(4). P.118.
Simmonds P. Recombination and selection in the evolution of picornaviruses and other mammalian positive-stranded RNA viruses // J. Virol. 2006. Vol.80. P.11124 –11140.
Duggal R., Wimmer E. Genetic Recombination of Poliovirus in Vitro and in Vivo: Temperature-Dependent Alteration of Crossover Sites // Virology. 1999. Vol.258. P.30–41.
Runckel C., Westesson O., Andino R., DeRisi JL. Identification and manipulation of the molecular determinants influencing poliovirus recombination // PLoS Pathog. 2013. Vol.9(2). P.e1003164.
Muslin C., Joffret M-L., Pelletier I., Blondel B., Delpeyroux F. Evolution and Emergence of Enteroviruses through Intra- and Inter-species Recombination: Plasticity and Phenotypic Impact of Modular Genetic Exchanges in the 5’ Untranslated Region // PLoS Pathog. 2015. Vol. 11(11). P. e1005266.
Simon-Loriere E., Martin DP., Weeks KM., Negroni M. RNA structures facilitate recombination-mediated gene swapping in HIV-1 // J. Virol. 2010. Vol.84. P. 12675–12682.
Smyth RP., Schlub TE., Grimm AJ., Waugh C., Ellenberg P., Chopra A., Mallal S., Cromer D., Mak J., Davenport MP. Identifying recombination hot spots in the HIV-1 genome // J. Virol. 2014. Vol.88. P.2891-2902.
Jackie E. Mahar, Karin Bok, Kim Y. Green, Carl D. Kirkwooda. The Importance of Intergenic Recombination in Norovirus GII.3 Evolution // J. Virol. 2013. Vol.87(7). P.3687-3698.
Tsimpidis M., Bachoumis G., Mimouli K., Kyriakopoulou Z., Robertson DL., Markoulatos P., Amoutzias GD. T-RECs: rapid and large-scale detection of recombination events among different evolutionary lineages of viral genomes // BMC Bioinformatics. 2017. Vol.18(1). P.13.
Wierzchoslawski R., Dzianott A., Bujarski J. Dissecting the requirement for subgenomic promoter sequences by RNA recombination of brome mosaic virus in vivo: evidence for functional separation of transcription and recombination // J. Virol. 2004. Vol.78. P. 8552–8564.
Kolondam B., Rao P., Sztuba-Solinska J., Weber PH., Dzianott A., Johns MA., Bujarski JJ. Co-infection with two strains of Brome mosaic bromovirus reveals common RNA recombination sites in different hosts // Virus. Evol. 2015. Vol. 1(1). P.vev021.
Downloads
How to Cite
Issue
Section
License
Copyright (c) 2019 Annals of Mechnikov's Institute
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 Unported License.
