Evolution and Distribution of Class II-Related Endogenous Retroviruses

ABSTRACT Endogenous retroviruses (ERVs) are widespread in vertebrate genomes and have been loosely grouped into “classes” on the basis of their phylogenetic relatedness to the established genera of exogenous retroviruses. Four of these genera—the lentiviruses, alpharetroviruses, betaretroviruses, and deltaretroviruses—form a well-supported clade in retroviral phylogenies, and ERVs that group with these genera have been termed class II ERVs. We used PCR amplification and sequencing of retroviral fragments from more than 130 vertebrate taxa to investigate the evolution of the class II retroviruses in detail. We confirm that class II retroviruses are largely confined to mammalian and avian hosts and provide evidence for a major novel group of avian retroviruses, and we identify additional members of both the alpha- and the betaretrovirus genera. Phylogenetic analyses demonstrated that the avian and mammalian viruses form distinct monophyletic groups, implying that interclass transmission has occurred only rarely during the evolution of the class II retroviruses. In contrast to previous reports, the lentiviruses clustered as sister taxa to several endogenous retroviruses derived from rodents and insectivores. This topology was further supported by the shared loss of both the class II PR-Pol frameshift site and the class II retrovirus G-patch domain.

[1]  Michael P. Cummings,et al.  PAUP* [Phylogenetic Analysis Using Parsimony (and Other Methods)] , 2004 .

[2]  L. N. van de Lagemaat,et al.  Multiple Groups of Endogenous Betaretroviruses in Mice, Rats, and Other Mammals , 2004, Journal of Virology.

[3]  J. McDonald,et al.  Long terminal repeat retrotransposons of Mus musculus , 2004, Genome Biology.

[4]  John P. Huelsenbeck,et al.  MrBayes 3: Bayesian phylogenetic inference under mixed models , 2003, Bioinform..

[5]  Colin N. Dewey,et al.  Initial sequencing and comparative analysis of the mouse genome. , 2002 .

[6]  Jean-Michel Hatt,et al.  Identification and Characterization of Two Closely Related Unclassifiable Endogenous Retroviruses in Pythons ( Python molurus and Python curtus ) , 2022 .

[7]  Richard A. Goldstein,et al.  rtREV: An Amino Acid Substitution Matrix for Inference of Retrovirus and Reverse Transcriptase Phylogeny , 2002, Journal of Molecular Evolution.

[8]  B. Berkhout,et al.  Codon and amino acid usage in retroviral genomes is consistent with virus-specific nucleotide pressure. , 2002, AIDS research and human retroviruses.

[9]  Mouse Genome Sequencing Consortium.  Initial sequencing and comparative analysis of the mouse genome , 2002, Nature.

[10]  Philippe Dessen,et al.  Identification, Phylogeny, and Evolution of Retroviral Elements Based on Their Envelope Genes , 2001, Journal of Virology.

[11]  R. Wilkins,et al.  Endogenous Type D Retrovirus in a Marsupial, the Common Brushtail Possum (Trichosurus vulpecula) , 2001, Journal of Virology.

[12]  D. Mindell,et al.  Evolution and Characterization of Tetraonine Endogenous Retrovirus: a New Virus Related to Avian Sarcoma and Leukosis Viruses , 2001, Journal of Virology.

[13]  J. V. Moran,et al.  Initial sequencing and analysis of the human genome. , 2001, Nature.

[14]  International Human Genome Sequencing Consortium.  Initial sequencing and analysis of the human genome , 2001, Nature.

[15]  D. Mager,et al.  Novel Mouse Type D Endogenous Proviruses and ETn Elements Share Long Terminal Repeat and Internal Sequences , 2000, Journal of Virology.

[16]  D. Mindell,et al.  Cospeciation and Horizontal Transmission of Avian Sarcoma and Leukosis Virus gag Genes in Galliform Birds , 2000, Journal of Virology.

[17]  Michael Tristem,et al.  Identification and Characterization of Novel Human Endogenous Retrovirus Families by Phylogenetic Screening of the Human Genome Mapping Project Database , 2000, Journal of Virology.

[18]  M. V. Regenmortel,et al.  Virus taxonomy: classification and nomenclature of viruses. Seventh report of the International Committee on Taxonomy of Viruses. , 2000 .

[19]  E. Koonin,et al.  G-patch: a new conserved domain in eukaryotic RNA-processing proteins and type D retroviral polyproteins. , 1999, Trends in biochemical sciences.

[20]  T. Heidmann,et al.  ERV-L Elements: a Family of Endogenous Retrovirus-Like Elements Active throughout the Evolution of Mammals , 1999, Journal of Virology.

[21]  James Cook,et al.  Interclass Transmission and Phyletic Host Tracking in Murine Leukemia Virus-Related Retroviruses , 1999, Journal of Virology.

[22]  A. Brunt,et al.  Virus Taxonomy. Seventh Report of the International Committee on Taxomony of Viruses , 1999 .

[23]  E. Herniou,et al.  Retroviral Diversity and Distribution in Vertebrates , 1998, Journal of Virology.

[24]  Thomas L. Madden,et al.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. , 1997, Nucleic acids research.

[25]  J. Stoye,et al.  Retrotransposons, Endogenous Retroviruses, and the Evolution of Retroelements , 1997 .

[26]  C. Petropoulos.  Retroviral Taxonomy, Protein Structures, Sequences, and Genetic Maps , 1997 .

[27]  Peter K. Vogt,et al.  Historical Introduction to the General Properties of Retroviruses , 1997 .

[28]  S. Hecht,et al.  Distribution of endogenous type B and type D sheep retrovirus sequences in ungulates and other mammals. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[29]  M. Tristem.  Amplification of divergent retroelements by PCR. , 1996, BioTechniques.

[30]  P. Štrop,et al.  Cloning, Bacterial Expression, and Characterization of the Mason-Pfizer Monkey Virus Proteinase (*) , 1995, The Journal of Biological Chemistry.

[31]  D. Mager,et al.  Endogenous Human Retroviruses , 1994 .

[32]  G. Quérat,et al.  Nucleotide sequence of the jaagsiekte retrovirus, an exogenous and endogenous type D and B retrovirus of sheep and goats , 1992, Journal of virology.

[33]  T. Eickbush,et al.  Origin and evolution of retroelements based upon their reverse transcriptase sequences. , 1990, The EMBO journal.

[34]  M. A. McClure,et al.  Origins and Evolutionary Relationships of Retroviruses , 1989, The Quarterly review of biology.

[35]  M. A. McClure,et al.  Sequence comparisons of retroviral proteins: relative rates of change and general phylogeny. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[36]  K. Lueders,et al.  The intracisternal A-particle gene family: structure and functional aspects. , 1988, Advances in cancer research.

[37]  G. Peters,et al.  Complete nucleotide sequence of a milk-transmitted mouse mammary tumor virus: two frameshift suppression events are required for translation of gag and pol , 1987, Journal of virology.

[38]  W. Gilbert,et al.  Nucleotide sequence of rous sarcoma virus , 1983, Cell.

[39]  W. S. Hayward,et al.  Pheasant virus: new class of ribodeoxyvirus. , 1976, Proceedings of the National Academy of Sciences of the United States of America.

[40]  P. Vogt,et al.  RNA tumor viruses of pheasants: characterization of avian leukosis subgroups F and G. , 1974, Virology.