TRIMCyps are anti-retroviral proteins that have arisen independently in New World and Old World primates. All TRIMCyps comprise a CypA domain fused to the tripartite domains of TRIM5α but they have distinct lentiviral specificities, conferring HIV-1 restriction in New World owl monkeys and HIV-2 restriction in Old World rhesus macaques. Here we provide evidence that Asian macaque TRIMCyps have acquired changes that switch restriction specificity between different lentiviral lineages, resulting in species-specific alleles that target different viruses. Structural, thermodynamic and viral restriction analysis suggests that a single mutation in the Cyp domain, R69H, occurred early in macaque TRIMCyp evolution, expanding restriction specificity to the lentiviral lineages found in African green monkeys, sooty mangabeys and chimpanzees. Subsequent mutations have enhanced restriction to particular viruses but at the cost of broad specificity. We reveal how specificity is altered by a scaffold mutation, E143K, that modifies surface electrostatics and propagates conformational changes into the active site. Our results suggest that lentiviruses may have been important pathogens in Asian macaques despite the fact that there are no reported lentiviral infections in current macaque populations.
Vyšlo v časopise: Conformational Adaptation of Asian Macaque TRIMCyp Directs Lineage Specific Antiviral Activity. PLoS Pathog 6(8): e32767. doi:10.1371/journal.ppat.1001062 Kategorie: Research Article prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1001062
1. RandallRE
GoodbournS
2008 Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J Gen Virol 89 1 47
2. SawyerSL
EmermanM
MalikHS
2004 Ancient adaptive evolution of the primate antiviral DNA-editing enzyme APOBEC3G. PLoS Biol 2 E275
3. SawyerSL
WuLI
2005 Positive selection of primate TRIM5alpha identifies a critical species-specific retroviral restriction domain. Proc Natl Acad Sci U S A 102 2832 2837
4. GuptaRK
HueS
SchallerT
VerschoorE
PillayD
2009 Mutation of a single residue renders human tetherin resistant to HIV-1 Vpu-mediated depletion. PLoS Pathog 5 e1000443
5. McNattMW
ZangT
HatziioannouT
BartlettM
FofanaIB
2009 Species-specific activity of HIV-1 Vpu and positive selection of tetherin transmembrane domain variants. PLoS Pathog 5 e1000300
6. Van ValenL
1973 A new evolutonary law. Evolutionary Theory 1 1 30
7. HuthoffH
TowersGJ
2008 Restriction of retroviral replication by APOBEC3G/F and TRIM5α. Trends Microbiol 16 612 619
8. PatersonS
VogvillT
BucklingA
BenmayorR
SpiersAJ
2010 Antagonistic coevolution accelerates molecular evolution. Nature in press
9. StremlauM
OwensCM
PerronMJ
KiesslingM
AutissierP
2004 The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 427 848 853
10. StremlauM
WelikalaS
SodroskiJ
2005 Species-specific variation in the B30.2(SPRY) domain of TRIM5alpha determines the potency of human immunodeficiency virus restriction. J Virol 79 3139 3145
11. Perez-CaballeroD
YangA
CowanS
BieniaszPD
2005 Human Tripartite Motif 5{alpha} Domains Responsible for Retrovirus Restriction Activity and Specificity. J Virol 79 8969 8978
12. YapMW
NisoleS
StoyeJP
2005 A Single Amino Acid Change in the SPRY Domain of Human Trim5alpha Leads to HIV-1 Restriction. Curr Biol 15 73 78
13. StremlauM
PerronM
LeeM
LiY
SongB
2006 Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5alpha restriction factor. Proc Natl Acad Sci U S A 103 5514 5519
14. WuX
AndersonJL
CampbellEM
JosephAM
HopeTJ
2006 Proteasome inhibitors uncouple rhesus TRIM5alpha restriction of HIV-1 reverse transcription and infection. Proc Natl Acad Sci U S A 103 7465 7470
15. RoldCJ
AikenC
2008 Proteasomal degradation of TRIM5alpha during retrovirus restriction. PLoS Pathog 4 e1000074
16. TowersGJ
2007 The control of viral infection by tripartite motif proteins and cyclophilin A. Retrovirology 4 40
17. LangelierCR
SandrinV
EckertDM
ChristensenDE
ChandrasekaranV
2008 Biochemical characterization of a recombinant TRIM5alpha protein that restricts human immunodeficiency virus type 1 replication. J Virol 82 11682 11694
18. SoaresEA
MenezesAN
SchragoCG
MoreiraMA
BonvicinoCR
2010 Evolution of TRIM5alpha B30.2 (SPRY) domain in New World primates. Infect Genet Evol 10 246 253
19. YlinenL
KeckesovaZ
WilsonSJ
RanasingheS
2005 Differential restriction of HIV-2 and SIVmac by TRIM5alpha alleles. J Virol 79 11580 11587
20. SayahDM
SokolskajaE
BerthouxL
LubanJ
2004 Cyclophilin A retrotransposition into TRIM5 explains owl monkey resistance to HIV-1. Nature 430 569 573
21. YapMW
DoddingMP
2006 Trim-cyclophilin A fusion proteins can restrict human immunodeficiency virus type 1 infection at two distinct phases in the viral life cycle. J Virol 80 4061 4067
22. WilsonSJ
WebbBL
YlinenLM
HeeneyJL
2008 Independent evolution of an antiviral TRIMCyp in rhesus macaques. Proc Natl Acad Sci U S A 105 3557 3562
23. VirgenCA
KratovacZ
2008 Independent genesis of chimeric TRIM5-cyclophilin proteins in two primate species. Proc Natl Acad Sci U S A 105 3563 3568
24. BrennanG
KozyrevY
HuSL
2008 TRIMCyp expression in Old World primates Macaca nemestrina and Macaca fascicularis. Proc Natl Acad Sci U S A 105 3569 3574
25. NewmanRM
HallL
KirmaierA
PozziLA
PeryE
2008 Evolution of a TRIM5-CypA splice isoform in old world monkeys. PLoS Pathog 4 e1000003
26. LiaoCH
KuangYQ
LiuHL
ZhengYT
SuB
2007 A novel fusion gene, TRIM5-Cyclophilin A in the pig-tailed macaque determines its susceptibility to HIV-1 infection. Aids 21 Suppl 8 S19 26
27. YinL
BoussardS
AllanJ
1998 The HIV type 1 replication block in nonhuman primates is not explained by differences in cyclophilin A primary structure. AIDS Res Hum Retroviruses 14 95 97
28. HirschVM
OlmstedRA
Murphey-CorbM
PurcellRH
JohnsonPR
1989 An African primate lentivirus (SIVsm) closely related to HIV-2. Nature 339 389 392
29. GaoF
BailesE
RobertsonDL
ChenY
RodenburgC
1999 Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature 397 436 441
30. PriceAJ
MarzettaF
LammersM
YlinenLMJ
2009 Active site remodelling switches HIV specificity of antiretroviral TRIMCyp. Nature Struct Mol Biol 16 1036 1042
31. McEwanWA
HosieMJ
2009 Truncation of TRIM5 in the Feliformia explains the absence of retroviral restriction in cells of the domestic cat. J Virol 83 8270 8275
32. IkedaY
CollinsMK
RadcliffePA
MitrophanousKA
TakeuchiY
2002 Gene transduction efficiency in cells of different species by HIV and EIAV vectors. Gene Ther 9 932 938
33. HatziioannouT
GoffSP
2003 Restriction of multiple divergent retroviruses by Lv1 and Ref1. EMBO J 22 385 394
34. YlinenLM
GiffordRJ
SmithTP
2006 Isolation of an Active Lv1 Gene from Cattle Indicates that Tripartite Motif Protein-Mediated Innate Immunity to Retroviral Infection Is Widespread among Mammals. J Virol 80 7332 7338
35. GambleTR
VajdosFF
YooS
WorthylakeDK
HouseweartM
1996 Crystal structure of human cyclophilin A bound to the amino-terminal domain of HIV-1 capsid. Cell 87 1285 1294
36. LiJ
HanK
XingJ
KimHS
RogersJ
2009 Phylogeny of the macaques (Cercopithecidae: Macaca) based on Alu elements. Gene 448 242 249
37. FooteJ
MilsteinC
1991 Kinetic maturation of an immune response. Nature 352 530 532
38. FooteJ
WinterG
1992 Antibody framework residues affecting the conformation of the hypervariable loops. J Mol Biol 224 487 499
39. JamesLC
RoversiP
TawfikDS
2003 Antibody multispecificity mediated by conformational diversity. Science 299 1362 1367
40. KatzourakisA
TristemM
PybusOG
2007 From the Cover: Discovery and analysis of the first endogenous lentivirus. Proc Natl Acad Sci U S A 104 6261 6265
41. KeckesovaZ
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
42. ApetreiC
KaurA
LercheNW
MetzgerM
PandreaI
2005 Molecular epidemiology of simian immunodeficiency virus SIVsm in U.S. primate centers unravels the origin of SIVmac and SIVstm. J Virol 79 8991 9005
43. ApetreiC
GormusB
SilvestriG
2006 Kuru experiments triggered the emergence of pathogenic SIVmac. Aids 20 317 321
44. VergneL
BourgeoisA
Mpoudi-NgoleE
MougnutouR
MbuagbawJ
2003 Biological and genetic characteristics of HIV infections in Cameroon reveals dual group M and O infections and a correlation between SI-inducing phenotype of the predominant CRF02_AG variant and disease stage. Virology 310 254 266
45. da SilvaZJ
OliveiraI
AndersenA
DiasF
RodriguesA
2008 Changes in prevalence and incidence of HIV-1, HIV-2 and dual infections in urban areas of Bissau, Guinea-Bissau: is HIV-2 disappearing? Aids 22 1195 1202
46. GiffordRJ
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
47. ZuffereyR
NagyD
MandelRJ
NaldiniL
TronoD
1997 Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nature Biotech 15 871 875
48. BainbridgeJW
StephensC
ParsleyK
DemaisonC
HalfyardA
2001 In vivo gene transfer to the mouse eye using an HIV-based lentiviral vector; efficient long-term transduction of corneal endothelium and retinal pigment epithelium. Gene Ther 8 1665 1668
49. GriffinSD
AllenJF
LeverAM
2001 The major human immunodeficiency virus type 2 (HIV-2) packaging signal is present on all HIV-2 RNA species: cotranslational RNA encapsidation and limitation of Gag protein confer specificity. J Virol 75 12058 12069
50. PoeschlaEM
Wong-StaalF
LooneyDJ
1998 Efficient transduction of nondividing human cells by feline immunodeficiency virus lentiviral vectors. Nat Med 4 354 357
51. BesnierC
TowersG
2002 Restriction of lentivirus in monkeys. Proc Natl Acad Sci U S A 99 11920 11925
52. PasseriniLD
2006 Retroviral Restriction Factors Fv1 and TRIM5{alpha} Act Independently and Can Compete for Incoming Virus before Reverse Transcription. J Virol 80 2100 2105
53. ZhangF
Perez-CaballeroD
DerseD
2006 Antiretroviral potential of human tripartite motif-5 and related proteins. Virology
54. ZhengL
BaumannU
ReymondJL
2004 An efficient one-step site-directed and site-saturation mutagenesis protocol. Nucleic Acids Res 32 e115
55. 1994 The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50 760 763
Zvýšte si kvalifikáciu online z pohodlia domova
Nemáte účet? Registrujte sa
Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.
