#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Endogenous Viral Elements in Animal Genomes


Integration into the nuclear genome of germ line cells can lead to vertical inheritance of retroviral genes as host alleles. For other viruses, germ line integration has only rarely been documented. Nonetheless, we identified endogenous viral elements (EVEs) derived from ten non-retroviral families by systematic in silico screening of animal genomes, including the first endogenous representatives of double-stranded RNA, reverse-transcribing DNA, and segmented RNA viruses, and the first endogenous DNA viruses in mammalian genomes. Phylogenetic and genomic analysis of EVEs across multiple host species revealed novel information about the origin and evolution of diverse virus groups. Furthermore, several of the elements identified here encode intact open reading frames or are expressed as mRNA. For one element in the primate lineage, we provide statistically robust evidence for exaptation. Our findings establish that genetic material derived from all known viral genome types and replication strategies can enter the animal germ line, greatly broadening the scope of paleovirological studies and indicating a more significant evolutionary role for gene flow from virus to animal genomes than has previously been recognized.


Vyšlo v časopise: Endogenous Viral Elements in Animal Genomes. PLoS Genet 6(11): e32767. doi:10.1371/journal.pgen.1001191
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1001191

Souhrn

Integration into the nuclear genome of germ line cells can lead to vertical inheritance of retroviral genes as host alleles. For other viruses, germ line integration has only rarely been documented. Nonetheless, we identified endogenous viral elements (EVEs) derived from ten non-retroviral families by systematic in silico screening of animal genomes, including the first endogenous representatives of double-stranded RNA, reverse-transcribing DNA, and segmented RNA viruses, and the first endogenous DNA viruses in mammalian genomes. Phylogenetic and genomic analysis of EVEs across multiple host species revealed novel information about the origin and evolution of diverse virus groups. Furthermore, several of the elements identified here encode intact open reading frames or are expressed as mRNA. For one element in the primate lineage, we provide statistically robust evidence for exaptation. Our findings establish that genetic material derived from all known viral genome types and replication strategies can enter the animal germ line, greatly broadening the scope of paleovirological studies and indicating a more significant evolutionary role for gene flow from virus to animal genomes than has previously been recognized.


Zdroje

1. BenvenisteRE

TodaroGJ

1974 Evolution of C-type viral genes: inheritance of exogenously acquired viral genes. Nature 252 456 459

2. JaenischR

1976 Germ line integration and Mendelian transmission of the exogenous Moloney leukemia virus. Proc Natl Acad Sci U S A 73 1260 1264

3. BejaranoER

KhashoggiA

WittyM

LichtensteinC

1996 Integration of multiple repeats of geminiviral DNA into the nuclear genome of tobacco during evolution. Proc Natl Acad Sci U S A 93 759 764

4. HerniouE

MartinJ

MillerK

CookJ

WilkinsonM

1998 Retroviral diversity and distribution in vertebrates. J Virol 72 5955 5966

5. TristemM

2000 Identification and characterization of novel human endogenous retrovirus families by phylogenetic screening of the human genome mapping project database. J Virol 74 3715 3730

6. CrochuS

CookS

AttouiH

CharrelRN

De ChesseR

2004 Sequences of flavivirus-related RNA viruses persist in DNA form integrated in the genome of Aedes spp. mosquitoes. J Gen Virol 85 1971 1980

7. TangKF

LightnerDV

2006 Infectious hypodermal and hematopoietic necrosis virus (IHHNV)-related sequences in the genome of the black tiger prawn Penaeus monodon from Africa and Australia. Virus Res 118 185 191

8. StaginnusC

Richert-PoggelerKR

2006 Endogenous pararetroviruses: two-faced travelers in the plant genome. Trends Plant Sci 11 485 491

9. BezierA

AnnaheimM

HerbiniereJ

WetterwaldC

GyapayG

2009 Polydnaviruses of braconid wasps derive from an ancestral nudivirus. Science 323 926 930

10. TaylorDJ

BruennJ

2009 The evolution of novel fungal genes from non-retroviral RNA viruses. BMC Biol 7 88

11. HorieM

HondaT

SuzukiY

KobayashiY

DaitoT

2010 Endogenous non-retroviral RNA virus elements in mammalian genomes. Nature 463 84 87

12. LanderES

LintonLM

BirrenB

NusbaumC

ZodyMC

2001 Initial sequencing and analysis of the human genome. Nature 409 860 921

13. SperberG

LovgrenA

ErikssonNE

BenachenhouF

BlombergJ

2009 RetroTector online, a rational tool for analysis of retroviral elements in small and medium size vertebrate genomic sequences. BMC Bioinformatics 10 Suppl 6 S4

14. MalikHS

HenikoffS

EickbushTH

2000 Poised for contagion: evolutionary origins of the infectious abilities of invertebrate retroviruses. Genome Res 10 1307 1318

15. MaoriE

TanneE

SelaI

2007 Reciprocal sequence exchange between non-retro viruses and hosts leading to the appearance of new host phenotypes. Virology 362 342 349

16. ShafritzDA

ShouvalD

ShermanHI

HadziyannisSJ

KewMC

1981 Integration of hepatitis B virus DNA into the genome of liver cells in chronic liver disease and hepatocellular carcinoma. Studies in percutaneous liver biopsies and post-mortem tissue specimens. N Engl J Med 305 1067 1073

17. BernsKI

LindenRM

1995 The cryptic life style of adeno-associated virus. Bioessays 17 237 245

18. ArbuckleJH

MedveczkyMM

LukaJ

HadleySH

LuegmayrA

2010 The latent human herpesvirus-6A genome specifically integrates in telomeres of human chromosomes in vivo and in vitro. Proc Natl Acad Sci U S A 107 5563 5568

19. ZhdanovVM

1975 Integration of viral genomes. Nature 256 471 473

20. KlenermanP

HengartnerH

ZinkernagelRM

1997 A non-retroviral RNA virus persists in DNA form. Nature 390 298 301

21. GeukingMB

WeberJ

DewannieuxM

GorelikE

HeidmannT

2009 Recombination of retrotransposon and exogenous RNA virus results in nonretroviral cDNA integration. Science 323 393 396

22. TaylorDJ

LeachRW

BruennJ

2010 Filoviruses are ancient and integrated into mammalian genomes. BMC Evol Biol 10 193

23. RibetD

HarperF

DupressoirA

DewannieuxM

PierronG

2008 An infectious progenitor for the murine IAP retrotransposon: emergence of an intracellular genetic parasite from an ancient retrovirus. Genome Res 18 597 609

24. KazazianHHJr

2004 Mobile elements: drivers of genome evolution. Science 303 1626 1632

25. DunlapKA

PalmariniM

VarelaM

BurghardtRC

HayashiK

2006 Endogenous retroviruses regulate periimplantation placental growth and differentiation. Proc Natl Acad Sci U S A 103 14390 14395

26. DupressoirA

VernochetC

BawaO

HarperF

PierronG

2009 Syncytin-A knockout mice demonstrate the critical role in placentation of a fusogenic, endogenous retrovirus-derived, envelope gene. Proc Natl Acad Sci U S A 106 12127 12132

27. GiffordR

TristemM

2003 The evolution, distribution and diversity of endogenous retroviruses. Virus Genes 26 291 316

28. EmermanM

MalikHS

2010 Paleovirology–modern consequences of ancient viruses. PLoS Biol 8 e1000301 doi:10.1371/journal.pbio.1000301

29. CharlestonMA

RobertsonDL

2002 Preferential host switching by primate lentiviruses can account for phylogenetic similarity with the primate phylogeny. Syst Biol 51 528 535

30. HolmesEC

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

31. KatzourakisA

TristemM

PybusOG

GiffordRJ

2007 Discovery and analysis of the first endogenous lentivirus. Proc Natl Acad Sci U S A 104 6261 6265

32. SimmondsP

SmithDB

1999 Structural constraints on RNA virus evolution. J Virol 73 5787 5794

33. BelshawR

GardnerA

RambautA

PybusOG

2008 Pacing a small cage: mutation and RNA viruses. Trends Ecol Evol 23 188 193

34. GibbsAJ

FargetteD

Garcia-ArenalF

GibbsMJ

2010 Time–the emerging dimension of plant virus studies. J Gen Virol 91 13 22

35. KeckesovaZ

YlinenLM

TowersGJ

GiffordRJ

KatzourakisA

2009 Identification of a RELIK orthologue in the European hare (Lepus europaeus) reveals a minimum age of 12 million years for the lagomorph lentiviruses. Virology 384 7 11

36. EsnaultC

MaestreJ

HeidmannT

2000 Human LINE retrotransposons generate processed pseudogenes. Nat Genet 24 363 367

37. PrestiRM

ZhaoG

BeattyWL

MihindukulasuriyaKA

da RosaAP

2009 Quaranfil, Johnston Atoll, and Lake Chad viruses are novel members of the family Orthomyxoviridae. J Virol 83 11599 11606

38. AttouiH

Mohd JaafarF

BelhouchetM

TaoS

ChenB

2006 Liao ning virus, a new Chinese seadornavirus that replicates in transformed and embryonic mammalian cells. J Gen Virol 87 199 208

39. RoizD

VazquezA

SecoMP

TenorioA

RizzoliA

2009 Detection of novel insect flavivirus sequences integrated in Aedes albopictus (Diptera: Culicidae) in Northern Italy. Virol J 6 93

40. SamulskiRJ

ZhuX

XiaoX

BrookJD

HousmanDE

1991 Targeted Integration of adeno-associated virus (AAV) into human chromosome 19. Embo Journal 10 3941 3950

41. KotinRM

LindenRM

BernsKI

1992 Characterization of a preferred site on human chromosome 19q for integration of adeno-associated virus DNA by non-homologous recombination. EMBO J 11 5071 5078

42. Bininda-EmondsOR

CardilloM

JonesKE

MacPheeRD

BeckRM

2007 The delayed rise of present-day mammals. Nature 446 507 512

43. FavaroP

DowneyHD

ZhouJS

WrightJF

HauckB

2009 Host and vector-dependent effects on the risk of germline transmission of AAV vectors. Mol Ther 17 1022 1030

44. TownerJS

AmmanBR

SealyTK

CarrollSA

ComerJA

2009 Isolation of genetically diverse Marburg viruses from Egyptian fruit bats. PLoS Pathog 5 e1000536 doi:10.1371/journal.ppat.1000536

45. BarretteRW

MetwallySA

RowlandJM

XuL

ZakiSR

2009 Discovery of swine as a host for the Reston ebolavirus. Science 325 204 206

46. SmithJM

HaighJ

1974 The hitch-hiking effect of a favourable gene. Genet Res 23 23 35

47. TarlintonR

MeersJ

YoungP

2008 Biology and evolution of the endogenous koala retrovirus. Cell Mol Life Sci 65 3413 3421

48. BelshawR

DawsonAL

Woolven-AllenJ

ReddingJ

BurtA

2005 Genomewide screening reveals high levels of insertional polymorphism in the human endogenous retrovirus family HERV-K(HML2): implications for present-day activity. J Virol 79 12507 12514

49. GiordanoR

MagnanoAR

ZaccagniniG

PittoggiC

MoscufoN

2000 Reverse transcriptase activity in mature spermatozoa of mouse. J Cell Biol 148 1107 1113

50. MartinJ

HerniouE

CookJ

O'NeillRW

TristemM

1999 Interclass transmission and phyletic host tracking in murine leukemia virus-related retroviruses. J Virol 73 2442 2449

51. LiL

KapoorA

SlikasB

BamideleOS

WangC

2010 Multiple diverse circoviruses infect farm animals and are commonly found in human and chimpanzee feces. J Virol 84 1674 1682

52. VictoriaJG

KapoorA

DupuisK

SchnurrDP

DelwartEL

2008 Rapid identification of known and new RNA viruses from animal tissues. PLoS Pathog 4 e1000163 doi:10.1371/journal.ppat.1000163

53. LiL

VictoriaJG

WangC

JonesM

FellersGM

2010 Bat guano virome: predominance of dietary viruses from insects and plants plus novel mammalian viruses. J Virol 84 6955 6965

54. BestS

Le TissierP

TowersG

StoyeJP

1996 Positional cloning of the mouse retrovirus restriction gene Fv1. Nature 382 826 829

55. ArnaudF

CaporaleM

VarelaM

BiekR

ChessaB

2007 A paradigm for virus-host coevolution: sequential counter-adaptations between endogenous and exogenous retroviruses. PLoS Pathog 3 e170 doi:10.1371/journal.ppat.0030170

56. KooninEV

2010 Taming of the shrewd: novel eukaryotic genes from RNA viruses. BMC Biol 8 2

57. van der OostJ

JoreMM

WestraER

LundgrenM

BrounsSJ

2009 CRISPR-based adaptive and heritable immunity in prokaryotes. Trends Biochem Sci 34 401 407

58. BelshawR

KatzourakisA

2005 BlastAlign: a program that uses blast to align problematic nucleotide sequences. Bioinformatics 21 122 123

59. EdgarRC

2004 MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32 1792 1797

60. StamatakisA

2006 RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22 2688 2690

61. AbascalF

ZardoyaR

PosadaD

2005 ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21 2104 2105

62. RambautA

GrasslyNC

1997 Seq-Gen: an application for the Monte Carlo simulation of DNA sequence evolution along phylogenetic trees. Comput Appl Biosci 13 235 238

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2010 Číslo 11
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
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

#ADS_BOTTOM_SCRIPTS#