Literature DB >> 22529376

Env-less endogenous retroviruses are genomic superspreaders.

Gkikas Magiorkinis1, Robert J Gifford, Aris Katzourakis, Joris De Ranter, Robert Belshaw.   

Abstract

Endogenous retroviruses (ERVs) differ from typical retroviruses in being inherited through the host germline and therefore are a unique combination of pathogen and selfish genetic element. Some ERV lineages proliferate by infecting germline cells, as do typical retroviruses, whereas others lack the env gene required for virions to enter cells and thus behave like retrotransposons. We wished to know what factors determined the relative abundance of different ERV lineages, so we analyzed ERV loci recovered from 38 mammal genomes by in silico screening. By modeling the relationship between proliferation and replication mechanism in detail within one group, the intracisternal A-type particles (IAPs), and performing simple correlations across all ERV lineages, we show that when ERVs lose the env gene their proliferation within that genome is boosted by a factor of ∼30. We also show that ERV abundance follows the Pareto principle or 20/80 rule, with ∼20% of lineages containing 80% of the loci. This rule is observed in many biological systems, including infectious disease epidemics, where commonly ∼20% of the infected individuals are responsible for 80% of onward infection. We thus borrow simple epidemiological and ecological models and show that retrotransposition and loss of env is the trait that leads endogenous retroviruses to becoming genomic superspreaders that take over a significant proportion of their host's genome.

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Year:  2012        PMID: 22529376      PMCID: PMC3358877          DOI: 10.1073/pnas.1200913109

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  46 in total

1.  The Distribution of Abundance in Neutral Communities.

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Journal:  Am Nat       Date:  2000-05       Impact factor: 3.926

2.  Poised for contagion: evolutionary origins of the infectious abilities of invertebrate retroviruses.

Authors:  H S Malik; S Henikoff; T H Eickbush
Journal:  Genome Res       Date:  2000-09       Impact factor: 9.043

Review 3.  The evolution, distribution and diversity of endogenous retroviruses.

Authors:  Robert Gifford; Michael Tristem
Journal:  Virus Genes       Date:  2003-05       Impact factor: 2.332

4.  Long-term reinfection of the human genome by endogenous retroviruses.

Authors:  Robert Belshaw; Vini Pereira; Aris Katzourakis; Gillian Talbot; Jan Paces; Austin Burt; Michael Tristem
Journal:  Proc Natl Acad Sci U S A       Date:  2004-03-25       Impact factor: 11.205

5.  Heterogeneities in the transmission of infectious agents: implications for the design of control programs.

Authors:  M E Woolhouse; C Dye; J F Etard; T Smith; J D Charlwood; G P Garnett; P Hagan; J L Hii; P D Ndhlovu; R J Quinnell; C H Watts; S K Chandiwana; R M Anderson
Journal:  Proc Natl Acad Sci U S A       Date:  1997-01-07       Impact factor: 11.205

6.  Mutation rates in mammalian genomes.

Authors:  Sudhir Kumar; Sankar Subramanian
Journal:  Proc Natl Acad Sci U S A       Date:  2002-01-15       Impact factor: 11.205

7.  Identification and characterization of novel human endogenous retrovirus families by phylogenetic screening of the human genome mapping project database.

Authors:  M Tristem
Journal:  J Virol       Date:  2000-04       Impact factor: 5.103

8.  Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu.

Authors:  Stuart J D Neil; Trinity Zang; Paul D Bieniasz
Journal:  Nature       Date:  2008-01-16       Impact factor: 49.962

9.  Epidemiology: dimensions of superspreading.

Authors:  Alison P Galvani; Robert M May
Journal:  Nature       Date:  2005-11-17       Impact factor: 49.962

10.  Tetherin inhibits HIV-1 release by directly tethering virions to cells.

Authors:  David Perez-Caballero; Trinity Zang; Alaleh Ebrahimi; Matthew W McNatt; Devon A Gregory; Marc C Johnson; Paul D Bieniasz
Journal:  Cell       Date:  2009-10-30       Impact factor: 41.582

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  53 in total

Review 1.  Studies of endogenous retroviruses reveal a continuing evolutionary saga.

Authors:  Jonathan P Stoye
Journal:  Nat Rev Microbiol       Date:  2012-05-08       Impact factor: 60.633

Review 2.  Border collies of the genome: domestication of an autonomous retrovirus-like transposon.

Authors:  M Joan Curcio
Journal:  Curr Genet       Date:  2018-06-21       Impact factor: 3.886

Review 3.  Immune responses to endogenous retroelements: taking the bad with the good.

Authors:  George Kassiotis; Jonathan P Stoye
Journal:  Nat Rev Immunol       Date:  2016-04       Impact factor: 53.106

Review 4.  Transmission, Evolution, and Endogenization: Lessons Learned from Recent Retroviral Invasions.

Authors:  Alex D Greenwood; Yasuko Ishida; Sean P O'Brien; Alfred L Roca; Maribeth V Eiden
Journal:  Microbiol Mol Biol Rev       Date:  2017-12-13       Impact factor: 11.056

Review 5.  Long Terminal Repeats: From Parasitic Elements to Building Blocks of the Transcriptional Regulatory Repertoire.

Authors:  Peter J Thompson; Todd S Macfarlan; Matthew C Lorincz
Journal:  Mol Cell       Date:  2016-06-02       Impact factor: 17.970

6.  Exploring the effects of immunity and life history on the dynamics of an endogenous retrovirus.

Authors:  R K Kanda; M Tristem; T Coulson
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2013-08-12       Impact factor: 6.237

7.  Genome-wide characterization of endogenous retroviruses in the bat Myotis lucifugus reveals recent and diverse infections.

Authors:  Xiaoyu Zhuo; Mina Rho; Cédric Feschotte
Journal:  J Virol       Date:  2013-05-29       Impact factor: 5.103

8.  Genome-Wide Screening of Retroviral Envelope Genes in the Nine-Banded Armadillo (Dasypus novemcinctus, Xenarthra) Reveals an Unfixed Chimeric Endogenous Betaretrovirus Using the ASCT2 Receptor.

Authors:  Sébastien Malicorne; Cécile Vernochet; Guillaume Cornelis; Baptiste Mulot; Frédéric Delsuc; Odile Heidmann; Thierry Heidmann; Anne Dupressoir
Journal:  J Virol       Date:  2016-08-26       Impact factor: 5.103

9.  Distribution, Diversity, and Evolution of Endogenous Retroviruses in Perissodactyl Genomes.

Authors:  Henan Zhu; Robert James Gifford; Pablo Ramiro Murcia
Journal:  J Virol       Date:  2018-11-12       Impact factor: 5.103

10.  A novel recombinant retrovirus in the genomes of modern birds combines features of avian and mammalian retroviruses.

Authors:  Jamie E Henzy; Robert J Gifford; Welkin E Johnson; John M Coffin
Journal:  J Virol       Date:  2013-12-18       Impact factor: 5.103

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