Evolution of a Species-Specific Determinant within Human CRM1 that Regulates the Post-transcriptional Phases of HIV-1 Replication

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The human immunodeficiency virus type-1 (HIV-1) Rev protein regulates the nuclear export of intron-containing viral RNAs by recruiting the CRM1 nuclear export receptor. Here, we employed a combination of functional and phylogenetic analyses to identify and characterize a species-specific determinant within human CRM1 (hCRM1) that largely overcomes established defects in murine cells to the post-transcriptional stages of the HIV-1 life cycle. hCRM1 expression in murine cells promotes the cytoplasmic accumulation of intron-containing viral RNAs, resulting in a substantial stimulation of the net production of infectious HIV-1 particles. These stimulatory effects require a novel surface-exposed element within HEAT repeats 9A and 10A, discrete from the binding cleft previously shown to engage Rev's leucine-rich nuclear export signal. Moreover, we show that this element is a unique feature of higher primate CRM1 proteins, and discuss how this sequence has evolved from a non-functional, ancestral sequence.

Vyšlo v časopise: Evolution of a Species-Specific Determinant within Human CRM1 that Regulates the Post-transcriptional Phases of HIV-1 Replication. PLoS Pathog 7(11): e32767. doi:10.1371/journal.ppat.1002395
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002395

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1. KirchhoffF 2010 Immune evasion and counteraction of restriction factors by HIV-1 and other primate lentiviruses. Cell Host Microbe 8 55 67

2. van MaanenMSuttonRE 2003 Rodent models for HIV-1 infection and disease. Curr HIV Res 1 121 130

3. ClaytonLKHusseyRESteinbrichRRamachandranHHusainY 1988 Substitution of murine for human CD4 residues identifies amino acids critical for HIV-gp120 binding. Nature 335 363 366

4. LandauNRWartonMLittmanDR 1988 The envelope glycoprotein of the human immunodeficiency virus binds to the immunoglobulin-like domain of CD4. Nature 334 159 162

5. FengYBroderCCKennedyPEBergerEA 1996 HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 272 872 877

6. GarberMEWeiPKewalRamaniVNMayallTPHerrmannCH 1998 The interaction between HIV-1 Tat and human cyclin T1 requires zinc and a critical cysteine residue that is not conserved in the murine CycT1 protein. Genes Dev 12 3512 3527

7. WeiPGarberMEFangSMFischerWHJonesKA 1998 A novel CDK9-associated C-type cyclin interacts directly with HIV-1 Tat and mediates its high-affinity, loop-specific binding to TAR RNA. Cell 92 451 462

8. BieniaszPDCullenBR 2000 Multiple blocks to human immunodeficiency virus type 1 replication in rodent cells. J Virol 74 9868 9877

9. MarianiRRutterGHarrisMEHopeTJKrausslichHG 2000 A block to human immunodeficiency virus type 1 assembly in murine cells. J Virol 74 3859 3870

10. ZhangJXDiehlGELittmanDR 2008 Relief of preintegration inhibition and characterization of additional blocks for HIV replication in primary mouse T cells. PLoS One 3 e2035

11. SwansonCMMalimMH 2006 Retrovirus RNA trafficking: from chromatin to invasive genomes. Traffic 7 1440 1450

12. CullenBR 2003 Nuclear mRNA export: insights from virology. Trends Biochem Sci 28 419 424

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

14. HuttenSKehlenbachRH 2007 CRM1-mediated nuclear export: to the pore and beyond. Trends Cell Biol 17 193 201

15. ChenBKRoussoIShimSKimPS 2001 Efficient assembly of an HIV-1/MLV Gag-chimeric virus in murine cells. Proc Natl Acad Sci U S A 98 15239 15244

16. ReedMMarianiRSheppardLPekrunKLandauNR 2002 Chimeric human immunodeficiency virus type 1 containing murine leukemia virus matrix assembles in murine cells. J Virol 76 436 443

17. TronoDBaltimoreD 1990 A human cell factor is essential for HIV-1 Rev action. EMBO J 9 4155 4160

18. ShererNMSwansonCMPapaioannouSMalimMH 2009 Matrix mediates the functional link between human immunodeficiency virus type 1 RNA nuclear export elements and the assembly competency of Gag in murine cells. J Virol 83 8525 8535

19. SwansonCMPufferBAAhmadKMDomsRWMalimMH 2004 Retroviral mRNA nuclear export elements regulate protein function and virion assembly. EMBO J 23 2632 2640

20. HatziioannouTMartin-SerranoJZangTBieniaszPD 2005 Matrix-induced inhibition of membrane binding contributes to human immunodeficiency virus type 1 particle assembly defects in murine cells. J Virol 79 15586 15589

21. JinJSturgeonTChenCWatkinsSCWeiszOA 2007 Distinct intracellular trafficking of equine infectious anemia virus and human immunodeficiency virus type 1 Gag during viral assembly and budding revealed by bimolecular fluorescence complementation assays. J Virol 81 11226 11235

22. BrayMPrasadSDubayJWHunterEJeangKT 1994 A small element from the Mason-Pfizer monkey virus genome makes human immunodeficiency virus type 1 expression and replication Rev-independent. Proc Natl Acad Sci U S A 91 1256 1260

23. CoskunAKvan MaanenMNguyenVSuttonRE 2006 Human chromosome 2 carries a gene required for production of infectious human immunodeficiency virus type 1. J Virol 80 3406 3415

24. Nagai-FukatakiMOhashiTHashimotoIKimuraTHakataY 2011 Nuclear and cytoplasmic effects of human CRM1 on HIV-1 production in rat cells. Genes Cells 16 203 216

25. OkadaHZhangXBen FofanaINagaiMSuzukiH 2009 Synergistic effect of human CycT1 and CRM1 on HIV-1 propagation in rat T cells and macrophages. Retrovirology 6 43

26. SwansonCMShererNMMalimMH 2010 SRp40 and SRp55 promote the translation of unspliced human immunodeficiency virus type 1 RNA. J Virol 84 6748 6759

27. BieniaszPDGrdinaTABogerdHPCullenBR 1998 Recruitment of a protein complex containing Tat and cyclin T1 to TAR governs the species specificity of HIV-1 Tat. EMBO J 17 7056 7065

28. MalimMHMcCarnDFTileyLSCullenBR 1991 Mutational definition of the human immunodeficiency virus type 1 Rev activation domain. Journal of virology 65 4248 4254

29. WinslowBJTronoD 1993 The blocks to human immunodeficiency virus type 1 Tat and Rev functions in mouse cell lines are independent. J Virol 67 2349 2354

30. AdamsonCSFreedEO 2007 Human immunodeficiency virus type 1 assembly, release, and maturation. Adv Pharmacol 55 347 387

31. SaadJSMillerJTaiJKimAGhanamRH 2006 Structural basis for targeting HIV-1 Gag proteins to the plasma membrane for virus assembly. Proc Natl Acad Sci U S A 103 11364 11369

32. TangCLoeligerELuncsfordPKindeIBeckettD 2004 Entropic switch regulates myristate exposure in the HIV-1 matrix protein. Proc Natl Acad Sci U S A 101 517 522

33. PaillartJCGottlingerHG 1999 Opposing effects of human immunodeficiency virus type 1 matrix mutations support a myristyl switch model of gag membrane targeting. J Virol 73 2604 2612

34. Perez-CaballeroDHatziioannouTMartin-SerranoJBieniaszPD 2004 Human immunodeficiency virus type 1 matrix inhibits and confers cooperativity on gag precursor-membrane interactions. J Virol 78 9560 9563

35. DongXBiswasASuelKEJacksonLKMartinezR 2009 Structural basis for leucine-rich nuclear export signal recognition by CRM1. Nature 458 1136 1141

36. MoneckeTGuttlerTNeumannPDickmannsAGorlichD 2009 Crystal structure of the nuclear export receptor CRM1 in complex with Snurportin1 and RanGTP. Science 324 1087 1091

37. GuttlerTMadlTNeumannPDeichselDCorsiniL 2010 NES consensus redefined by structures of PKI-type and Rev-type nuclear export signals bound to CRM1. Nat Struct Mol Biol 17 1367 1376

38. KoyamaMMatsuuraY 2010 An allosteric mechanism to displace nuclear export cargo from CRM1 and RanGTP by RanBP1. EMBO J 29 2002 2013

39. PerelmanPJohnsonWERoosCSeuanezHNHorvathJE 2011 A molecular phylogeny of living primates. PLoS Genet 7 e1001342

40. GuptaRKHueSSchallerTVerschoorEPillayD 2009 Mutation of a single residue renders human tetherin resistant to HIV-1 Vpu-mediated depletion. PLoS Pathog 5 e1000443

41. McNattMWZangTHatziioannouTBartlettMFofanaIB 2009 Species-specific activity of HIV-1 Vpu and positive selection of tetherin transmembrane domain variants. PLoS Pathog 5 e1000300

42. SawyerSLEmermanMMalikHS 2004 Ancient adaptive evolution of the primate antiviral DNA-editing enzyme APOBEC3G. PLoS Biol 2 E275

43. SawyerSLWuLIEmermanMMalikHS 2005 Positive selection of primate TRIM5alpha identifies a critical species-specific retroviral restriction domain. Proc Natl Acad Sci U S A 102 2832 2837

44. HurstLD 2002 The Ka/Ks ratio: diagnosing the form of sequence evolution. Trends Genet 18 486

45. ParaskevaEIzaurraldeEBischoffFRHuberJKutayU 1999 CRM1-mediated recycling of snurportin 1 to the cytoplasm. J Cell Biol 145 255 264

46. AskjaerPJensenTHNilssonJEnglmeierLKjemsJ 1998 The specificity of the CRM1-Rev nuclear export signal interaction is mediated by RanGTP. J Biol Chem 273 33414 33422

47. HakataYYamadaMShidaH 2003 A multifunctional domain in human CRM1 (exportin 1) mediates RanBP3 binding and multimerization of human T-cell leukemia virus type 1 Rex protein. Mol Cell Biol 23 8751 8761

48. NemergutMELindsayMEBrownawellAMMacaraIG 2002 Ran-binding protein 3 links Crm1 to the Ran guanine nucleotide exchange factor. J Biol Chem 277 17385 17388

49. EnglmeierLFornerodMBischoffFRPetosaCMattajIW 2001 RanBP3 influences interactions between CRM1 and its nuclear protein export substrates. EMBO reports 2 926 932

50. LindsayMEHolaskaJMWelchKPaschalBMMacaraIG 2001 Ran-binding protein 3 is a cofactor for Crm1-mediated nuclear protein export. J Cell Biol 153 1391 1402

51. MertzJASimperMSLozanoMMPayneSMDudleyJP 2005 Mouse mammary tumor virus encodes a self-regulatory RNA export protein and is a complex retrovirus. J Virol 79 14737 14747

52. IndikSGunzburgWHSalmonsBRouaultF 2005 A novel, mouse mammary tumor virus encoded protein with Rev-like properties. Virology 337 1 6

53. TileyLSMadoreSJMalimMHCullenBR 1992 The VP16 transcription activation domain is functional when targeted to a promoter-proximal RNA sequence. Genes Dev 6 2077 2087

54. WodrichHSchambachAKrausslichHG 2000 Multiple copies of the Mason-Pfizer monkey virus constitutive RNA transport element lead to enhanced HIV-1 Gag expression in a context-dependent manner. Nucleic Acids Res 28 901 910

55. YiRBogerdHPCullenBR 2002 Recruitment of the Crm1 nuclear export factor is sufficient to induce cytoplasmic expression of incompletely spliced human immunodeficiency virus mRNAs. J Virol 76 2036 2042

56. SheehyAMGaddisNCChoiJDMalimMH 2002 Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 418 646 650

57. PlattEJWehrlyKKuhmannSEChesebroBKabatD 1998 Effects of CCR5 and CD4 cell surface concentrations on infections by macrophagetropic isolates of human immunodeficiency virus type 1. J Virol 72 2855 2864

58. GaddisNCChertovaESheehyAMHendersonLEMalimMH 2003 Comprehensive investigation of the molecular defect in vif-deficient human immunodeficiency virus type 1 virions. J Virol 77 5810 5820

59. EvanGILewisGKRamsayGBishopJM 1985 Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol Cell Biol 5 3610 3616

60. DutheilNHenckaertsEKohlbrennerELindenRM 2009 Transcriptional analysis of the adeno-associated virus integration site. J Virol 83 12512 12525

61. PriceMNDehalPSArkinAP 2009 FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26 1641 1650

62. YangZ 1997 PAML: a program package for phylogenetic analysis by maximum likelihood. CABIOS 13 555 556

63. WangDZhangYZhangZZhuJYuJ 2010 KaKs_Calculator 2.0: a toolkit incorporating gamma-series methods and sliding window strategies. Genomics Proteomics Bioinformatics 8 77 80

64. PondSLFrostSDMuseSV 2005 HyPhy: hypothesis testing using phylogenies. Bioinformatics 21 676 679

65. ZhangJNielsenRYangZ 2005 Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol 22 2472 2479

66. DaughertyMDLiuBFrankelAD 2010 Structural basis for cooperative RNA binding and export complex assembly by HIV Rev. Nat Struct Mol Biol 17 1337 1342

67. GruterPTaberneroCvon KobbeCSchmittCSaavedraC 1998 TAP, the human homolog of Mex67p, mediates CTE-dependent RNA export from the nucleus. Mol Cell 1 649 659