Poised for Contagion: Evolutionary Origins of the Infectious Abilities of Invertebrate Retroviruses

Harmit S. Malik; Steve Henikoff; Thomas H. Eickbush

doi:10.1101/gr.145000

journal article Open Access Sep 01, 2000

Poised for Contagion: Evolutionary Origins of the Infectious Abilities of Invertebrate Retroviruses

Harmit S. Malik

Steve Henikoff Thomas H. Eickbush

Genome Research Vol. 10 No. 9 pp. 1307-1318 · Cold Spring Harbor Laboratory

View at Publisher Save 10.1101/gr.145000

Abstract

Phylogenetic analyses suggest that long-terminal repeat (LTR) bearing retrotransposable elements can acquire additional open-reading frames that can enable them to mediate infection. Whereas this process is best documented in the origin of the vertebrate retroviruses and their acquisition of an envelope (env) gene, similar independent events may have occurred in insects, nematodes, and plants. The origins of env-like genes are unclear, and are often masked by the antiquity of the original acquisitions and by their rapid rate of evolution. In this report, we present evidence that in three other possible transitions of LTR retrotransposons to retroviruses, an envelope-like gene was acquired from a viral source. First, the gypsy and related LTR retrotransposable elements (the insect errantiviruses) have acquired their envelope-like gene from a class of insect baculoviruses (double-stranded DNA viruses with no RNA stage). Second, the Cer retroviruses in the Caenorhabditis elegans genome acquired their envelope gene from a Phleboviral (single ambisense-stranded RNA viruses) source. Third, the Tas retroviral envelope (Ascaris lumricoides) may have been obtained fromHerpesviridae (double-stranded DNA viruses, no RNA stage). These represent the only cases in which the env gene of a retrovirus has been traced back to its original source. This has implications for the evolutionary history of retroviruses as well as for the potential ability of all LTR-retrotransposable elements to become infectious agents.

Topics

No keywords indexed for this article. Browse by subject →

References

41

[1]

Gapped BLAST and PSI-BLAST: a new generation of protein database search programs

S. Altschul

Nucleic Acids Research 10.1093/nar/25.17.3389

[2]

10.1093/bioinformatics/14.1.48

[3]

10.1093/nar/27.1.260

[4]

Boeke J.D. Eickbush T.H. Sandmeyer S.B. Voytas D.F. (1999) in Virus Taxonomy: ICTV VIIth report. ed Murphy F.A. (Springer-Verlag, New York).

[5]

10.1101/gr.9.10.924

[6]

Britt "Human cytomegalovirus glycoproteins." Intervirology (1996) 10.1159/000150510

[7]

Clark "Phylogenetic analysis supports horizontal transfer of P transposable elements." Mol. Biol. Evol. (1994)

[8]

Coffin J.M. Hughes S.H. Varmus H.E. (1997) Retroviruses. (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York).

[9]

10.1046/j.1365-2583.2000.00167.x

[10]

Desset "Mobilization of two retroelements, ZAM and Idefix, in a novel unstable line of Drosophila melanogaster." Mol. Biol. Evol. (1999) 10.1093/oxfordjournals.molbev.a026038

[11]

10.1007/bf00366984

[12]

10.1016/0378-1119(94)90153-8

[13]

Friesen "Gene organization and transcription of TED, a lepidopteran retrotransposon integrated within the baculovirus genome." Mol. Cell. Biol. (1990)

[14]

10.1006/viro.1999.9894

[15]

10.1093/nar/28.1.228

[16]

Henikoff "Automated construction and graphical presentation of protein blocks from unaligned sequences." Gene (1995) 10.1016/0378-1119(95)00486-p

[17]

Ijkel "Sequence and organization of the Spodoptera exigua multicapsid nucleopolyhedrovirus genome." J. Gen. Virol. (1999) 10.1099/0022-1317-80-12-3289

[18]

10.1073/pnas.96.22.12621

[19]

Koonin "Diverse groups of plant RNA and DNA viruses share related movement proteins that may possess chaperone-like activity." J. Gen. Virol. (1991) 10.1099/0022-1317-72-12-2895

[20]

10.1006/viro.1998.9469

[21]

10.1073/pnas.95.12.6897

[22]

Lerat "Retrotransposons and retroviruses: Analysis of the envelope gene." Mol. Biol. Evol. (1999) 10.1093/oxfordjournals.molbev.a026210

[23]

Malik "Modular evolution of the integrase domain in the Ty3/Gypsy class of LTR retrotransposons." J. Virol. (1999) 10.1128/jvi.73.6.5186-5190.1999

[24]

Marin "Ty3/Gypsy retrotransposons (Metaviridae): Evolutionary perspectives derived from genome sequencing data." Mol. Biol. Evol. (2000) 10.1093/oxfordjournals.molbev.a026385

[25]

10.1093/protein/10.1.1

[26]

10.1006/viro.1998.9523

[27]

Pantazidis "The retrotransposon Osvaldo from Drosophila buzzatii displays all structural features of a functional retrovirus." Mol. Biol. Evol. (1999) 10.1093/oxfordjournals.molbev.a026180

[28]

Ramirez "Molecular biology of tenuiviruses, a remarkable group of plant viruses." J. Gen. Virol. (1994) 10.1099/0022-1317-75-3-467

[29]

Robertson "Multiple Mariner transposons in flatworms and hydras are related to those of insects." J. Hered. (1997) 10.1093/oxfordjournals.jhered.a023088

[30]

Prediction of Protein Secondary Structure at Better than 70% Accuracy

Burkhard Rost, Chris Sander

Journal of Molecular Biology 10.1006/jmbi.1993.1413

[31]

Saitou "The neighbor-joining method: A new method for reconstructing phylogenetic trees." Mol. Biol. Evol. (1987)

[32]

10.1093/bioinformatics/15.12.1000

[33]

10.1101/gad.8.17.2046

[34]

10.1126/science.1371365

[35]

Swofford D.L. (1999) PAUP*: phylogenetic analysis using parsimony and other methods. (Laboratory of Molecular Systematics, Smithsonisan Institute).

[36]

Takeya "Comparison between the viral transforming gene (src) of recovered avian sarcoma virus and its cellular homolog." Mol. Cell. Biol. (1981)

[37]

10.1093/nar/25.24.4876

[38]

Varmus H. Brown P. (1989) in Mobile DNA, eds Berg D.E. Howe M.M. (American Society for Microbiology, Washington, D.C.) pp 53â108.

[39]

Wright "Potential retroviruses in plants: Tat1 is related to a group of Arabidopsis thaliana Ty3/ gypsy retrotransposons that encode envelope-like proteins." Genetics (1998) 10.1093/genetics/149.2.703

[40]

10.1093/nar/21.9.2117

[41]

Xiong "Origin and evolution of retroelements based on their reverse transcriptase sequences." EMBO J. (1990) 10.1002/j.1460-2075.1990.tb07536.x

Cited By

283

Correlation in Expression between LTR Retrotransposons and Potential Host Cis-Targets during Infection of Antherea pernyi with ApNPV Baculovirus

Min Feng, Feifei Ren · 2019

Viruses

THE GENETICS AND GENOMICS OF THE SILKWORM, BOMBYX MORI

Marian R. Goldsmith, Toru Shimada · 2005

Annual Review of Entomology

The Sinbad retrotransposon from the genome of the human blood fluke, Schistosoma mansoni, and the distribution of related Pao-like elements

Claudia S Copeland, Victoria H Mann · 2005

BMC Evolutionary Biology

Transposable elements, gene creation and genome rearrangement in flowering plants

Jeffrey L Bennetzen · 2005

Current Opinion in Genetics & D...

Transposable elements and the evolution of genome size in eukaryotes

Margaret G. Kidwell · 2002

Genetica

New BEL-like LTR-retrotransposons in Fugu rubripes , Caenorhabditis elegans , and Drosophila melanogaster

Ian G Frame, John F Cutfield · 2001

Gene

Metrics

283

Citations

41

References

Details

Published: Sep 01, 2000
Vol/Issue: 10(9)
Pages: 1307-1318

Authors

Cite This Article

Harmit S. Malik, Steve Henikoff, Thomas H. Eickbush (2000). Poised for Contagion: Evolutionary Origins of the Infectious Abilities of Invertebrate Retroviruses. Genome Research, 10(9), 1307-1318. https://doi.org/10.1101/gr.145000

Poised for Contagion: Evolutionary Origins of the Infectious Abilities of Invertebrate Retroviruses

You May Also Like