Adaptive Evolution of Includes Retroviral Insertion and Positive Selection at Two Clusters of Residues Flanking the Substrate Groove

English version České info

Mouse APOBEC3 (mA3) is a cytidine deaminase with antiviral activity. mA3 is linked to the Rfv3 virus resistance factor, a gene responsible for recovery from infection by Friend murine leukemia virus, and mA3 allelic variants differ in their ability to restrict mouse mammary tumor virus. We sequenced mA3 genes from 38 inbred strains and wild mouse species, and compared the mouse sequence and predicted structure with human APOBEC3G (hA3G). An inserted sequence was identified in the virus restrictive C57BL strain allele that disrupts a splice donor site. This insertion represents the long terminal repeat of the xenotropic mouse gammaretrovirus, and was acquired in Eurasian mice that harbor xenotropic retrovirus. This viral regulatory sequence does not alter splicing but is associated with elevated mA3 expression levels in spleens of laboratory and wild-derived mice. Analysis of Mus mA3 coding sequences produced evidence of positive selection and identified 10 codons with very high posterior probabilities of having evolved under positive selection. Six of these codons lie in two clusters in the N-terminal catalytically active cytidine deaminase domain (CDA), and 5 of those 6 codons are polymorphic in Rfv3 virus restrictive and nonrestrictive mice and align with hA3G CDA codons that are critical for deaminase activity. Homology models of mA3 indicate that the two selected codon clusters specify residues that are opposite each other along the predicted CDA active site groove, and that one cluster corresponds to an hAPOBEC substrate recognition loop. Substitutions at these clustered mA3 codons alter antiviral activity. This analysis suggests that mA3 has been under positive selection throughout Mus evolution, and identified an inserted retroviral regulatory sequence associated with enhanced expression in virus resistant mice and specific residues that modulate antiviral activity.

Vyšlo v časopise: Adaptive Evolution of Includes Retroviral Insertion and Positive Selection at Two Clusters of Residues Flanking the Substrate Groove. PLoS Pathog 6(7): e32767. doi:10.1371/journal.ppat.1000974
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1000974

Souhrn

Zdroje

1. LillyF

1967 Susceptibility to two strains of Friend leukemia virus in mice. Science 155 461 462

2. BestS

LeTissierP

TowersG

StoyeJP

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

3. YanY

Buckler-WhiteA

WollenbergK

KozakCA

2009 Origin, antiviral function and evidence for positive selection of the gammaretrovirus restriction gene Fv1 in the genus Mus. Proc Natl Acad Sci U S A 106 3259 3263

4. KeckesovaZ

YlinenLM

TowersGJ

2004 The human and African green monkey Trim5α genes encode Ref1 and Lv1 retroviral restriction factor activities. Proc Natl Acad Sci U S A 101 10780 10785

5. StremlauM

OwensCM

PerronMJ

KiesslingM

AutissierP

2004 The cytoplasmic body component Trim5α restricts HIV-1 infection in Old World monkeys. Nature 427 848 853

6. TareenSU

SawyerSL

MalikHS

EmermanM

2008 An expanded clade of rodent Trim5 genes. Virology 385 473 483

7. Goila-GaurR

StrebelK

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

8. HarrisRS

BishopKN

SheehyAM

CraigHM

Petersen-MahrtSK

2003 DNA deamination mediates innate immunity to retroviral infection. Cell 113 803 809

9. NewmanENC

HolmesRK

CraigHM

KleinKC

LingappaJR

2005 Antiviral function of APOBEC3G can be dissociated from cytidine deaminase activity. Curr Biol 15 166 170

10. TakedaE

Tsuji-KawaharaS

SakamotoM

LangloisM-A

NeubergerMS

2008 Mouse APOBEC3 restricts Friend leukemia virus infection and pathogenesis in vivo. J Virol 82 10998 11008

11. KaoS

KhanMA

MiyagiE

PlishkaR

Buckler-WhiteA

2003 The human immunodeficiency virus type 1 Vif protein reduces intracellular expression and inhibits packaging of APOBEC3G (CEM15), a cellular inhibitor of virus infectivity. J Virol 77 11398 11407

12. EsnaultC

HeidmannO

DelebecqueF

DewannieuxM

RibetD

2005 APOBEC3G cytidine deaminase inhibits retrotransposition of endogenous retroviruses. Nature 433 430 433

13. MarianiR

ChenD

SchrofelbauerB

NavarroF

KonigR

2003 Species-specific exclusion of APOBEC3G from HIV-1 virions by Vif. Cell 114 21 31

14. OkeomaCM

LovsinN

PeterlinBM

RossSR

2007 APOBEC3 inhibits mouse mammary tumour virus replication in vivo. Nature 445 927 930

15. MiklMC

WattIN

LuM

ReikW

DaviesSL

2005 Mice deficient in APOBEC2 and APOBEC3. Mol Cell Biol 25 7270 7277

16. JernP

StoyeJP

CoffinJM

2007 Role of APOBEC3 in genetic diversity among endogenous murine leukemia viruses. PLoS Genet 3 2014 2022

17. SantiagoML

MontanoM

BenitezR

MesserRJ

YonemotoW

2008 Apobec3 encodes Rfv3, a gene influencing neutralizing antibody control of retrovirus infection. Science 321 1343 1346

18. ChesebroB

WehrlyK

1979 Identification of a non-H-2 gene (Rfv-3) influencing recovery from viremia and leukemia induced by Friend virus complex. Proc Natl Acad Sci U S A 76 425 429

19. DoigD

ChesebroB

1979 Anti-Friend virus antibody is associated with recovery from viremia and loss of viral leukemia cell-surface antigens in leukemic mice. Identification of Rfv-3 as a gene locus influencing antibody production. J Exp Med 150 10 19

20. SuperHJ

HasenkrugKJ

SimmonsS

BrooksDM

KonzekR

1999 Fine mapping of the Friend retrovirus resistance gene, Rfv3, on mouse chromosome 15. J Virol 73 7848 7852

21. OkeomaCM

PetersenJ

RossSR

2009 Expression of murine APOBEC3 alleles in different mouse strains and their effect on mouse mammary tumor virus infection. J Virol 83 3029 3038

22. HakataY

LandauNR

2006 Reversed functional organization of mouse and human APOBEC3 cytidine deaminase domains. J Biol Chem 281 366624 36631

23. LaRueRS

AndresdottirV

BlanchardY

ConticelloSG

DerseD

2009 Guidelines for naming nonprimate APOBEC3 genes and proteins. J Virol 83 494 497

24. ElderJH

GautschJW

JensenFC

LernerRA

ChusedTM

1980 Differential expression of two distinct xenotropic viruses in NZB mice. Clin Immunol Immunopath 15 493 501

25. O'NeillRR

BucklerCE

TheodoreTS

MartinMA

RepaskeR

1985 Envelope and long terminal repeat sequences of a cloned infectious NZB xenotropic murine leukemia virus. J Virol 53 100 106

26. BeckJA

LloydS

HafezparastM

Lennon-PierceM

EppigJT

2000 Geneologies of mouse inbred strains. Nat Genet 24 23 25

27. YangH

BellTA

ChurchillGA

de VillenaFP-M

2007 On the subspecific origin of the laboratory mouse. Nature Genet 39 1100 1107

28. YangZ

1997 PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13 555 556

29. LundriganBL

JansaSA

TuckerPK

2002 Phylogenetic relationships in the genus Mus, based on paternally, maternally, and biparentally inherited characters. Syst Biol 51 410 431

30. VeyrunesF

DobignyG

YangF

O'BrienPCM

CatalanJ

2006 Phylogenomics of the genus Mus (Rodentia: Muridae); extensive genome repatterning is not restricted to the house mouse. Proc R Soc B 273 2925 2934

31. ShandilyaSMD

NalamMNL

NalivaikaEA

GrossPJ

ValesanoJC

2010 Crystal structure of the APOBEC3G catalytic domain reveals potential oligomerization interfaces. Structure 18 28 38

32. HoldenLG

ProchnowC

ChangYP

BransteitterR

ChelicoL

2008 Crystal structure of the anti-viral APOBEC3G catalytic domain and functional implications. Nature 456 121 124

33. ChenK-M

HarjesE

GrossPJ

FahmyA

LuY

2008 Structure of the DNA deaminase domain of the HIV-1 restriction factor APOBEC3G. Nature 452 116 119

34. ChenK-M

MartemyanovaN

LuY

ShindoK

MatsuoH

2007 Extensive mutagenesis experiments corroborate a structural model for the DNA deaminase domain of APOBEC3G. FEBS Lett 581 4761 4766

35. MaksakovaIA

RomanishMT

GagnierL

DunnCA

van de LagemaatLN

2006 Retroviral elements and their hosts: insertional mutagenesis in the mouse germ line. PLoS Genet 2 0001 0010

36. AbuduA

Takaori-KondoA

IsumiT

ShirakawaK

KobayashiM

2006 Murine retrovirus escapes from murine APOBEC3 via two distinct novel mechanisms. Curr Biol 16 1565 1570

37. EastJ

TillyRJ

TuffreyM

HarveyJJ

1978 The early appearance and subsequent distribution of murine leukaemia virus in NZB embryos. Int J Cancer 22 495 502

38. KozakCA

O'NeillRR

1987 Diverse wild mouse origins of xenotropic, mink cell focus-forming and two types of ecotropic proviral genes. J Virol 61 3082 3088

39. YanY

KnoperRC

KozakCA

2007 Wild mouse variants of envelope genes of xenotropic/polytropic mouse gammaretroviruses and their XPR1 receptors elucidate receptor determinants of virus entry. J Virol 81 10550 10557

40. YanY

LiuQ

KozakCA

2009 Six host range variants of the xenotropic/polytropic gammaretrovirsues define determinants for entry in the XPR1 receptor. Retrovirology 6 87

41. StockingC

KozakCA

2008 Murine endogenous retroviruses. Cell Mol Life Sci 65 3383 3398

42. KohliRM

AbramsSR

GajulaKS

MaulRW

GearhartPJ

2009 A portable hot spot recognition loop transfers sequence preferences from APOBEC family members to activation-induced cytidine deaminase. J Biol Chem 284 22898 22904

43. LangloisMA

BealeRCL

ConticelloSG

NeubergerMS

2005 Mutational comparison of the single-domained APOBEC3C and double-domained APOBEC3F/G anti-retroviral cytidine deaminases provides insight into their DNA target site specificities. Nucleic Acids Res 33 1913 1923

44. LarijaniM

MartinA

2007 Single-stranded DNA structure and positional context of the target cytidine determine the enzymatic efficiency of AID. Mol Cell Biol 27 8038 8048

45. JonssonSR

HacheG

StengleinMD

FahrenkrugSC

AndresdottirV

2006 Evolutionarily conserved and non-conserved retrovirus restriction activities of artiodactyl APOBEC3F proteins. Nucleic Acids Res 34 5683 5694

46. SawyerSL

EmermanM

MalikHS

2004 Ancient adaptive evolution of the primate antiviral DNA-editing enzyme APOBEC3G. PLoS Biol 2 1278 1285

47. BrowneEP

LittmanDR

2008 Species-specific restriction of Apobec3-mediated hypermutation. J Virol 82 1305 1313

48. LanderMR

ChattopadhyaySK

1984 A Mus dunni cell line that lacks sequences closely related to endogenous murine leukemia viruses and can be infected by ecotropic, amphotropic, xenotropic, and mink cell focus-forming viruses. J Virol 52 695 698

49. HartleyJW

RoweWP

1975 Clonal cell lines from a feral mouse embryo which lack host-range restrictions for murine leukemia viruses. Virology 65 128 134

50. ClementsGB

FenyoEM

KleinG

1976 In vitro derived mouse A9 cell clones differing in malignancy: analysis by somatic cell hybridization with YACIR lymphoma cell clones. Proc Natl Acad Sci U S A 73 2004 2007

51. NRC 1996 Guide for the care and use of laboratory animals Washington, D.C. National Academies Press

52. PortisJL

McAteeFJ

KaymanSC

1992 Infectivity of retroviral DNA in vivo. J Acquired Immune Deficiency Syndrome 12 1272 3

53. RoweWP

PughWE

HartleyJW

1970 Plaque assay techniques for murine leukemia viruses. Virology 42 1136 1139

54. WuT

LeeCG

Buckler-WhiteA

KozakCA

2002 Genetic control of a mouse serum lipoprotein factor that inactivates murine leukemia viruses: evaluation of apolipoprotein F as a candidate. J Virol 76 2279 2286

55. EdgarRC

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

56. FelsensteinJ

2004 PHYLIP (Phylogenetic Inference Package) version 3.6 Seattle Distributed by the author. Department of Genome Sciences, University of Washington

57. BielawskiJP

YangZ

2005 Maximum likelihood methods for detecting adaptive protein evolution.

NielsenR

Statistical Methods in Molecular Evolution New York Springer-Verlag 103 124

58. YangZ

WongWSW

NielsenR