Parallel Germline Infiltration of a Lentivirus in Two Malagasy Lemurs


Retroviruses normally infect the somatic cells of their host and are transmitted horizontally, i.e., in an exogenous way. Occasionally, however, some retroviruses can also infect and integrate into the genome of germ cells, which may allow for their vertical inheritance and fixation in a given species; a process known as endogenization. Lentiviruses, a group of mammalian retroviruses that includes HIV, are known to infect primates, ruminants, horses, and cats. Unlike many other retroviruses, these viruses have not been demonstrably successful at germline infiltration. Here, we report on the discovery of endogenous lentiviral insertions in seven species of Malagasy lemurs from two different genera—Cheirogaleus and Microcebus. Combining molecular clock analyses and cross-species screening of orthologous insertions, we show that the presence of this endogenous lentivirus in six species of Microcebus is the result of one endogenization event that occurred about 4.2 million years ago. In addition, we demonstrate that this lentivirus independently infiltrated the germline of Cheirogaleus and that the two endogenization events occurred quasi-simultaneously. Using multiple proviral copies, we derive and characterize an apparently full length and intact consensus for this lentivirus. These results provide evidence that lentiviruses have repeatedly infiltrated the germline of prosimian species and that primates have been exposed to lentiviruses for a much longer time than what can be inferred based on sequence comparison of circulating lentiviruses. The study sets the stage for an unprecedented opportunity to reconstruct an ancestral primate lentivirus and thereby advance our knowledge of host–virus interactions.


Vyšlo v časopise: Parallel Germline Infiltration of a Lentivirus in Two Malagasy Lemurs. PLoS Genet 5(3): e32767. doi:10.1371/journal.pgen.1000425
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1000425

Souhrn

Retroviruses normally infect the somatic cells of their host and are transmitted horizontally, i.e., in an exogenous way. Occasionally, however, some retroviruses can also infect and integrate into the genome of germ cells, which may allow for their vertical inheritance and fixation in a given species; a process known as endogenization. Lentiviruses, a group of mammalian retroviruses that includes HIV, are known to infect primates, ruminants, horses, and cats. Unlike many other retroviruses, these viruses have not been demonstrably successful at germline infiltration. Here, we report on the discovery of endogenous lentiviral insertions in seven species of Malagasy lemurs from two different genera—Cheirogaleus and Microcebus. Combining molecular clock analyses and cross-species screening of orthologous insertions, we show that the presence of this endogenous lentivirus in six species of Microcebus is the result of one endogenization event that occurred about 4.2 million years ago. In addition, we demonstrate that this lentivirus independently infiltrated the germline of Cheirogaleus and that the two endogenization events occurred quasi-simultaneously. Using multiple proviral copies, we derive and characterize an apparently full length and intact consensus for this lentivirus. These results provide evidence that lentiviruses have repeatedly infiltrated the germline of prosimian species and that primates have been exposed to lentiviruses for a much longer time than what can be inferred based on sequence comparison of circulating lentiviruses. The study sets the stage for an unprecedented opportunity to reconstruct an ancestral primate lentivirus and thereby advance our knowledge of host–virus interactions.


Zdroje

1. HahnBH

ShawGM

De CockKM

SharpPM

2000 AIDS as a zoonosis: scientific and public health implications. Science 287 607 14

2. WorobeyM

GemmelM

TeuwenDE

HaselkornT

KunstmanK

2008 Direct evidence of extensive diversity of HIV-1 in Kinshasa by 1960. Nature 455 661 4

3. HolmesEC

2003 Molecular clocks and the puzzle of RNA virus origins. J Virol 77 3893 3897

4. GiffordRJ

2006 Evolution at the host-retrovirus interface. Bioessays 28 1153 1156

5. CoffinJM

HughesSH

VarmusHE

1997 Retroviruses. Cold Spring Harbor Press 843

6. GiffordR

TristemM

2003 The evolution, distribution and diversity of endogenous retroviruses. Virus Genes 26 291 315

7. LöwerR

LöwerJ

KurthR

1996 The viruses in all of us: characteristics and biological significance of human endogenous retrovirus sequences. Proc Natl Acad Sci U S A 93 5177 84

8. StoyeJP

2006 Koala retrovirus: a genome invasion in real time. Genome Biol 7 241

9. KatzourakisA

TristemM

PybusOG

GiffordRJ

2007 Discovery and analysis of the first endogenous lentivirus. Proc Natl Acad Sci U S A 104 6261 5

10. KeckesovaZ

YlinenLM

TowersGJ

GiffordRJ

KatzourakisA

2008 Identification of a RELIK orthologue in the European hare (Lepus europaeus) reveals a minimum age of 12 million years for the lagomorph lentiviruses. Virology. In press

11. van der LooW

AbrantesJ

EstevesPJ

2008 Sharing of endogenous lentiviral gene fragments among leporid lineages separated for more than 12 million years. J Virol. In press

12. GiffordRJ

KatzourakisA

TristemM

PybusOG

WintersM

2008 A transitional endogenous lentivirus from the genome of a basal primate and implications for lentivirus evolution. Proc Natl Acad Sci U S A 105 20362 20367

13. HughesJF

CoffinJM

2004 Human endogenous retrovirus K solo-LTR formation and insertional polymorphisms: implications for human and viral evolution. Proc Natl Acad Sci U S A 101 1668 72

14. TaylorBS

SobieszczykME

McCutchanFE

HammerSM

2008 The challenge of HIV-1 subtype diversity. N Engl J Med 358 1590 602

15. HopeTJ

1997 Viral RNA export. Chem Biol 4 335 344

16. PollardVW

MalimMH

1998 The HIV-1 Rev protein. Annu Rev Microbiol 52 491 532

17. TristemM

MarshallC

KarpasA

PetrikJ

HillF

1990 Origin of vpx in lentiviruses. Nature 347 341 342

18. SharpPM

BailesE

StevensonM

EmermanM

HahnBH

1996 Gene acquisition in HIV and SIV. Nature 383 586 7

19. TristemM

PurvisA

QuickeDLJ

1998 Complex evolutionary history of primate lentiviral vpr genes. Virology 240 232 237

20. PathakVK

HuWS

1997 “Might as well jump!” Template switching by retroviral reverse transcriptase, defective genome formation, and recombination. Semin Virol 8 141 150

21. GrovesC

2005 Order primates.

WilsonDE

ReederDM

Mammal's species of the world. John Hopkins University press 111 119

22. PouxC

MadsenO

MarquardE

VietesDR

de JongWW

VencesM

2005 Asynchronous colonization of Madagascar by the four endemic clades of primates, tenrecs, carnivores, and rodents as inferred from nuclear genes. Syst Biol 54 719 730

23. HorvathJE

WeisrockDW

EmbrySL

FiorentinoI

BalhoffJP

2008 Development and application of a phylogenomic toolkit: Resolving the evolutionary history of Madagascar's lemurs. Genome Res 18 489 499

24. PaceJKII

GilbertC

ClarkMS

FeschotteC

2008 Repeated horizontal transfer of a DNA transposon in mammals and other tetrapods. Proc Natl Acad Sci U S A 105 17023 17028

25. HughesJF

CoffinJM

2005 Human endogenous retroviral elements as indicators of ectopic recombination events in the primate genome. Genetics 171 1183 94

26. HeckmanKL

MarianiCL

RasoloarisonR

YoderAD

2007 Multiple nuclear loci reveal patterns of incomplete lineage sorting and complex species history within western mouse lemurs (Microcebus). Mol Phylogenet Evol 43 353 367

27. LiWH

TanimuraM

SharpPM

1988 Rates and dates of divergence between AIDS virus nucleotide sequences. Mol Biol Evol 5 313 330

28. StoreyM

MahoneyJJ

SaundersAD

DuncanRA

KelleySP

1995 Timing of hot spot-related volcanism and the breakup of Madagascar and India. Science 267 852 855

29. SchwabD

GanzhornJU

2004 Distribution, population structure and habitat use of Microcebus berthae compared to those of other sympatric Cheirogalids. Int J Primatol 25 307 330

30. RasoloarisonR

GoodmanSM

GanzhornJU

2000 A taxonomic revision of mouse lemurs (Microcebus) occurring in the western portion of Madagascar. Int J Primatol 21 963 1019

31. SondgerothK

BlitvichB

BlairC

TerweeJ

JungeR

2007 Assessing flavivirus, lentivirus, and herpesvirus exposure in free-ranging ring-tailed lemurs in southwestern Madagascar. J Wildl Dis 43 40 47

32. TowersGJ

2007 The control of viral infection by tripartite motif proteins and cyclophilin A. Retrovirology 4 40

33. Goila-GaurR

StrebelK

2008 HIV-1 Vif, APOBEC, and intrinsic immunity. Retrovirology 5 51

34. HallT

2004 BioEdit version 5.0.6. Available: http://www.mbio.ncsu.edu/BioEdit/bioedit.html

35. HuelsenbeckJP

RonquistF

2001 MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17 754 755

36. GuindonS

GascuelO

2003 A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52 696 704

37. NylanderJAA

2004 MrModeltest v2. Program distributed by the author Evolutionary Biology Centre, Uppsala University

38. DimmicMW

RestJS

MindellDP

GoldsteinRA

2002 rtREV: an amino acid substitution matrix for inference of retrovirus and reverse transcriptase phylogeny. J Mol Evol 55 65 73

39. TamuraK

DudleyJ

NeiM

KumarS

2007 MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24 1596 1599

40. KuikenC

LeitnerT

FoleyB

HahnB

MarxP

2008 HIV Sequence Compendium 2008 Los Alamos, New Mexico Los Alamos National Laboratory, Theoretical Biology and Biophysics LA-UR 08-03719. Available: http://www.hiv.lanl.gov/

41. YangZ

YoderAD

2003 Comparison of likelihood and Bayesian methods for estimating divergence times using multiple gene loci and calibration points, with application to a radiation of cute-looking mouse lemur species. Syst Biol 52 705 716

42. TheisC

ReederJ

GiegerichR

2008 KnotInFrame: prediction of -1 ribosomal frameshift events. Nucleic Acids Res 36 6013 20

Štítky
Genetika Reprodukčná medicína
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa