Evolution and Phylogeny of Insect Endogenous Retroviruses

Overview

Journal BMC Evol Biol

Publisher Biomed Central

Specialty Biology

Date 2001 Oct 10

PMID 11591216

Citations 27

Authors

C Terzian

A Pelisson

A Bucheton

Affiliations

Soon will be listed here.

Abstract

Background: The genome of invertebrates is rich in retroelements which are structurally reminiscent of the retroviruses of vertebrates. Those containing three open reading frames (ORFs), including an env-like gene, may well be considered as endogenous retroviruses. Further support to this similarity has been provided by the ability of the env-like gene of DmeGypV (the Gypsy endogenous retrovirus of Drosophila melanogaster) to promote infection of Drosophila cells by a pseudotyped vertebrate retrovirus vector.

Results: To gain insights into their evolutionary story, a sample of thirteen insect endogenous retroviruses, which represents the largest sample analysed until now, was studied by computer-assisted comparison of the translated products of their gag, pol and env genes, as well as their LTR structural features. We found that the three phylogenetic trees based respectively on Gag, Pol and Env common motifs are congruent, which suggest a monophyletic origin for these elements.

Conclusions: We showed that most of the insect endogenous retroviruses belong to a major clade group which can be further divided into two main subgroups which also differ by the sequence of their primer binding sites (PBS). We propose to name IERV-K and IERV-S these two major subgroups of Insect Endogenous Retro Viruses (or Insect ERrantiVirus, according to the ICTV nomenclature) which respectively use Lys and Ser tRNAs to prime reverse transcription.

Citing Articles

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van Lopik J, Alizada A, Trapotsi M, Hannon G, Bornelov S, Nicholson B Nat Commun. 2023; 14(1):7337.

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References

Song S, Gerasimova T, Kurkulos M, Boeke J, Corces V . An env-like protein encoded by a Drosophila retroelement: evidence that gypsy is an infectious retrovirus. Genes Dev. 1994; 8(17):2046-57. DOI: 10.1101/gad.8.17.2046. View

Xiong Y, Eickbush T . Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J. 1990; 9(10):3353-62. PMC: 552073. DOI: 10.1002/j.1460-2075.1990.tb07536.x. View

Kim A, Terzian C, Santamaria P, Pelisson A, Purdhomme N, Bucheton A . Retroviruses in invertebrates: the gypsy retrotransposon is apparently an infectious retrovirus of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1994; 91(4):1285-9. PMC: 43142. DOI: 10.1073/pnas.91.4.1285. View

Tanda S, Mullor J, Corces V . The Drosophila tom retrotransposon encodes an envelope protein. Mol Cell Biol. 1994; 14(8):5392-401. PMC: 359058. DOI: 10.1128/mcb.14.8.5392-5401.1994. View

Bailey T, Elkan C . Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol. 1994; 2:28-36. View

Pelisson A, Song S, Prudhomme N, Smith P, Bucheton A, Corces V . Gypsy transposition correlates with the production of a retroviral envelope-like protein under the tissue-specific control of the Drosophila flamenco gene. EMBO J. 1994; 13(18):4401-11. PMC: 395367. DOI: 10.1002/j.1460-2075.1994.tb06760.x. View

Alberola T, de Frutos R . Molecular structure of a gypsy element of Drosophila subobscura (gypsyDs) constituting a degenerate form of insect retroviruses. Nucleic Acids Res. 1996; 24(5):914-23. PMC: 145713. DOI: 10.1093/nar/24.5.914. View

Page R . TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci. 1996; 12(4):357-8. DOI: 10.1093/bioinformatics/12.4.357. View

Ozers M, Friesen P . The Env-like open reading frame of the baculovirus-integrated retrotransposon TED encodes a retrovirus-like envelope protein. Virology. 1996; 226(2):252-9. DOI: 10.1006/viro.1996.0653. View

10.

Thompson J, Gibson T, Plewniak F, Jeanmougin F, Higgins D . The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1998; 25(24):4876-82. PMC: 147148. DOI: 10.1093/nar/25.24.4876. View

11.

Leblanc P, Desset S, Dastugue B, Vaury C . Invertebrate retroviruses: ZAM a new candidate in D.melanogaster. EMBO J. 1998; 16(24):7521-31. PMC: 1170351. DOI: 10.1093/emboj/16.24.7521. View

12.

Teysset L, Burns J, Shike H, Sullivan B, Bucheton A, Terzian C . A Moloney murine leukemia virus-based retroviral vector pseudotyped by the insect retroviral gypsy envelope can infect Drosophila cells. J Virol. 1998; 72(1):853-6. PMC: 109448. DOI: 10.1128/JVI.72.1.853-856.1998. View

13.

Zhang Z, Schaffer A, Miller W, Madden T, Lipman D, Koonin E . Protein sequence similarity searches using patterns as seeds. Nucleic Acids Res. 1998; 26(17):3986-90. PMC: 147803. DOI: 10.1093/nar/26.17.3986. View

14.

Steiner D . The proprotein convertases. Curr Opin Chem Biol. 1998; 2(1):31-9. DOI: 10.1016/s1367-5931(98)80033-1. View

15.

Whalen J, Grigliatti T . Molecular characterization of a retrotransposon in Drosophila melanogaster, nomad, and its relationship to other retrovirus-like mobile elements. Mol Gen Genet. 1999; 260(5):401-9. DOI: 10.1007/s004380050910. View

16.

Malik H, Eickbush T . Modular evolution of the integrase domain in the Ty3/Gypsy class of LTR retrotransposons. J Virol. 1999; 73(6):5186-90. PMC: 112568. DOI: 10.1128/JVI.73.6.5186-5190.1999. View

17.

Thompson J, Plewniak F, Poch O . A comprehensive comparison of multiple sequence alignment programs. Nucleic Acids Res. 1999; 27(13):2682-90. PMC: 148477. DOI: 10.1093/nar/27.13.2682. View

18.

Singh M, Berger B, Kim P . LearnCoil-VMF: computational evidence for coiled-coil-like motifs in many viral membrane-fusion proteins. J Mol Biol. 1999; 290(5):1031-41. PMC: 7125536. DOI: 10.1006/jmbi.1999.2796. View

19.

Lerat E, Capy P . Retrotransposons and retroviruses: analysis of the envelope gene. Mol Biol Evol. 1999; 16(9):1198-207. DOI: 10.1093/oxfordjournals.molbev.a026210. View

20.

Pearson M, Groten C, Rohrmann G . Identification of the lymantria dispar nucleopolyhedrovirus envelope fusion protein provides evidence for a phylogenetic division of the Baculoviridae. J Virol. 2000; 74(13):6126-31. PMC: 112111. DOI: 10.1128/jvi.74.13.6126-6131.2000. View