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Quantitative Multicolor Super-Resolution Microscopy Reveals Tetherin HIV-1 Interaction


Virus assembly and interaction with host-cell proteins occur at length scales below the diffraction limit of visible light. Novel super-resolution microscopy techniques achieve nanometer resolution of fluorescently labeled molecules. The cellular restriction factor tetherin (also known as CD317, BST-2 or HM1.24) inhibits the release of human immunodeficiency virus 1 (HIV-1) through direct incorporation into viral membranes and is counteracted by the HIV-1 protein Vpu. For super-resolution analysis of HIV-1 and tetherin interactions, we established fluorescence labeling of HIV-1 proteins and tetherin that preserved HIV-1 particle formation and Vpu-dependent restriction, respectively. Multicolor super-resolution microscopy revealed important structural features of individual HIV-1 virions, virus assembly sites and their interaction with tetherin at the plasma membrane. Tetherin localization to micro-domains was dependent on both tetherin membrane anchors. Tetherin clusters containing on average 4 to 7 tetherin dimers were visualized at HIV-1 assembly sites. Combined biochemical and super-resolution analysis revealed that extended tetherin dimers incorporate both N-termini into assembling virus particles and restrict HIV-1 release. Neither tetherin domains nor HIV-1 assembly sites showed enrichment of the raft marker GM1. Together, our super-resolution microscopy analysis of HIV-1 interactions with tetherin provides new insights into the mechanism of tetherin-mediated HIV-1 restriction and paves the way for future studies of virus-host interactions.


Vyšlo v časopise: Quantitative Multicolor Super-Resolution Microscopy Reveals Tetherin HIV-1 Interaction. PLoS Pathog 7(12): e32767. doi:10.1371/journal.ppat.1002456
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002456

Souhrn

Virus assembly and interaction with host-cell proteins occur at length scales below the diffraction limit of visible light. Novel super-resolution microscopy techniques achieve nanometer resolution of fluorescently labeled molecules. The cellular restriction factor tetherin (also known as CD317, BST-2 or HM1.24) inhibits the release of human immunodeficiency virus 1 (HIV-1) through direct incorporation into viral membranes and is counteracted by the HIV-1 protein Vpu. For super-resolution analysis of HIV-1 and tetherin interactions, we established fluorescence labeling of HIV-1 proteins and tetherin that preserved HIV-1 particle formation and Vpu-dependent restriction, respectively. Multicolor super-resolution microscopy revealed important structural features of individual HIV-1 virions, virus assembly sites and their interaction with tetherin at the plasma membrane. Tetherin localization to micro-domains was dependent on both tetherin membrane anchors. Tetherin clusters containing on average 4 to 7 tetherin dimers were visualized at HIV-1 assembly sites. Combined biochemical and super-resolution analysis revealed that extended tetherin dimers incorporate both N-termini into assembling virus particles and restrict HIV-1 release. Neither tetherin domains nor HIV-1 assembly sites showed enrichment of the raft marker GM1. Together, our super-resolution microscopy analysis of HIV-1 interactions with tetherin provides new insights into the mechanism of tetherin-mediated HIV-1 restriction and paves the way for future studies of virus-host interactions.


Zdroje

1. NeilSJEastmanSWJouvenetNBieniaszPD 2006 HIV-1 Vpu promotes release and prevents endocytosis of nascent retrovirus particles from the plasma membrane. PLoS Pathog 2 e39

2. Van DammeNGoffDKatsuraCJorgensonRLMitchellR 2008 The interferon-induced protein BST-2 restricts HIV-1 release and is downregulated from the cell surface by the viral Vpu protein. Cell Host Microbe 3 245 252

3. JouvenetNNeilSJZhadinaMZangTKratovacZ 2009 Broad-spectrum inhibition of retroviral and filoviral particle release by tetherin. J Virol 83 1837 1844

4. SakumaTNodaTUrataSKawaokaYYasudaJ 2009 Inhibition of Lassa and Marburg virus production by tetherin. J Virol 83 2382 2385

5. MansouriMViswanathanKDouglasJLHinesJGustinJ 2009 Molecular mechanism of BST2/tetherin downregulation by K5/MIR2 of Kaposi's sarcoma-associated herpesvirus. J Virol 83 9672 9681

6. NeilSJZangTBieniaszPD 2008 Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451 425 430

7. JiaBSerra-MorenoRNeidermyerWRahmbergAMackeyJ 2009 Species-specific activity of SIV Nef and HIV-1 Vpu in overcoming restriction by tetherin/BST2. PLoS Pathog 5 e1000429

8. SauterDSchindlerMSpechtALandfordWNMunchJ 2009 Tetherin-driven adaptation of Vpu and Nef function and the evolution of pandemic and nonpandemic HIV-1 strains. Cell Host Microbe 6 409 421

9. GuptaRKMlcochovaPPelchen-MatthewsAPetitSJMattiuzzoG 2009 Simian immunodeficiency virus envelope glycoprotein counteracts tetherin/BST-2/CD317 by intracellular sequestration. Proc Natl Acad Sci U S A 106 20889 20894

10. Le TortorecANeilSJ 2009 Antagonism to and intracellular sequestration of human tetherin by the human immunodeficiency virus type 2 envelope glycoprotein. J Virol 83 11966 11978

11. KupzigSKorolchukVRollasonRSugdenAWildeA 2003 Bst-2/HM1.24 is a raft-associated apical membrane protein with an unusual topology. Traffic 4 694 709

12. HinzAMiguetNNatrajanGUsamiYYamanakaH 2010 Structural basis of HIV-1 tethering to membranes by the BST-2/tetherin ectodomain. Cell Host Microbe 7 314 323

13. Perez-CaballeroDZangTEbrahimiAMcNattMWGregoryDA 2009 Tetherin inhibits HIV-1 release by directly tethering virions to cells. Cell 139 499 511

14. HammondsJWangJJYiHSpearmanP 2010 Immunoelectron microscopic evidence for Tetherin/BST2 as the physical bridge between HIV-1 virions and the plasma membrane. PLoS Pathog 6 e1000749

15. FitzpatrickKSkaskoMDeerinckTJCrumJEllismanMH 2010 Direct restriction of virus release and incorporation of the interferon-induced protein BST-2 into HIV-1 particles. PLoS Pathog 6 e1000701

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

17. MitchellRSKatsuraCSkaskoMAFitzpatrickKLauD 2009 Vpu antagonizes BST-2-mediated restriction of HIV-1 release via beta-TrCP and endo-lysosomal trafficking. PLoS Pathog 5 e1000450

18. GoffinetCAllespachIHomannSTervoHMHabermannA 2009 HIV-1 antagonism of CD317 is species specific and involves Vpu-mediated proteasomal degradation of the restriction factor. Cell Host Microbe 5 285 297

19. MangeatBGers-HuberGLehmannMZuffereyMLubanJ 2009 HIV-1 Vpu neutralizes the antiviral factor Tetherin/BST-2 by binding it and directing its beta-TrCP2-dependent degradation. PLoS Pathog 5 e1000574

20. BieniaszPD 2009 The cell biology of HIV-1 virion genesis. Cell Host Microbe 5 550 558

21. BetzigEPattersonGHSougratRLindwasserOWOlenychS 2006 Imaging intracellular fluorescent proteins at nanometer resolution. Science 313 1642 1645

22. HessSTGirirajanTPMasonMD 2006 Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Biophys J 91 4258 4272

23. RustMJBatesMZhuangX 2006 Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods 3 793 795

24. HeilemannMvan de LindeSSchuttpelzMKasperRSeefeldtB 2008 Subdiffraction-resolution fluorescence imaging with conventional fluorescent probes. Angew Chem Int Ed Engl 47 6172 6176

25. BatesMHuangBDempseyGTZhuangX 2007 Multicolor super-resolution imaging with photo-switchable fluorescent probes. Science 317 1749 1753

26. ShroffHGalbraithCGGalbraithJAWhiteHGilletteJ 2007 Dual-color superresolution imaging of genetically expressed probes within individual adhesion complexes. Proc Natl Acad Sci U S A 104 20308 20313

27. HuangBBabcockHZhuangX 2010 Breaking the diffraction barrier: super-resolution imaging of cells. Cell 143 1047 1058

28. ManleySGilletteJMPattersonGHShroffHHessHF 2008 High-density mapping of single-molecule trajectories with photoactivated localization microscopy. Nat Methods 5 155 157

29. LarsonDRJohnsonMCWebbWWVogtVM 2005 Visualization of retrovirus budding with correlated light and electron microscopy. Proc Natl Acad Sci U S A 102 15453 15458

30. JouvenetNBieniaszPDSimonSM 2008 Imaging the biogenesis of individual HIV-1 virions in live cells. Nature 454 236 240

31. FlorsCHottaJUji-iHDedeckerPAndoR 2007 A stroboscopic approach for fast photoactivation-localization microscopy with Dronpa mutants. J Am Chem Soc 129 13970 13977

32. ChurchmanLSOktenZRockRSDawsonJFSpudichJA 2005 Single molecule high-resolution colocalization of Cy3 and Cy5 attached to macromolecules measures intramolecular distances through time. Proc Natl Acad Sci U S A 102 1419 1423

33. BriggsJAWilkTWelkerRKrausslichHGFullerSD 2003 Structural organization of authentic, mature HIV-1 virions and cores. EMBO J 22 1707 1715

34. CarlsonLAde MarcoAOberwinklerHHabermannABriggsJA 2010 Cryo electron tomography of native HIV-1 budding sites. PLoS Pathog 6 e1001173

35. ZhuPLiuJBessJJrChertovaELifsonJD 2006 Distribution and three-dimensional structure of AIDS virus envelope spikes. Nature 441 847 852

36. HessSTGouldTJGudhetiMVMaasSAMillsKD 2007 Dynamic clustered distribution of hemagglutinin resolved at 40 nm in living cell membranes discriminates between raft theories. Proc Natl Acad Sci U S A 104 17370 17375

37. LillemeierBFMortelmaierMAForstnerMBHuppaJBGrovesJT 2009 TCR and Lat are expressed on separate protein islands on T cell membranes and concatenate during activation. Nat Immunol 11 90 96

38. GreenfieldDMcEvoyALShroffHCrooksGEWingreenNS 2009 Self-organization of the Escherichia coli chemotaxis network imaged with super-resolution light microscopy. PLoS Biol 7 e1000137

39. AnnibalePVanniSScarselliMRothlisbergerURadenovicA 2011 Quantitative photo activated localization microscopy: unraveling the effects of photoblinking. PLoS One 6 e22678

40. WiedenmannJIvanchenkoSOswaldFSchmittFRockerC 2004 EosFP, a fluorescent marker protein with UV-inducible green-to-red fluorescence conversion. Proc Natl Acad Sci U S A 101 15905 15910

41. AnnibalePVanniSScarselliMRothlisbergerURadenovicA 2011 Identification of clustering artifacts in photoactivated localization microscopy. Nat Methods 8 527 528

42. JonesSAShimSHHeJZhuangX 2011 Fast, three-dimensional super-resolution imaging of live cells. Nat Methods 8 499 508

43. HeilemannMvan de LindeSMukherjeeASauerM 2009 Super-resolution imaging with small organic fluorophores. Angew Chem Int Ed Engl 48 6903 6908

44. SougratRBartesaghiALifsonJDBennettAEBessJW 2007 Electron tomography of the contact between T cells and SIV/HIV-1: implications for viral entry. PLoS Pathog 3 e63

45. IvanchenkoSGodinezWJLampeMKrausslichHGEilsR 2009 Dynamics of HIV-1 assembly and release. PLoS Pathog 5 e1000652

46. LeungKKimJOGaneshLKabatJSchwartzO 2008 HIV-1 assembly: viral glycoproteins segregate quantally to lipid rafts that associate individually with HIV-1 capsids and virions. Cell Host Microbe 3 285 292

47. HabermannAKrijnse-LockerJOberwinklerHEckhardtMHomannS 2010 CD317/tetherin is enriched in the HIV-1 envelope and downregulated from the plasma membrane upon virus infection. J Virol 84 4646 4658

48. MiyagiEAndrewAJKaoSStrebelK 2009 Vpu enhances HIV-1 virus release in the absence of Bst-2 cell surface down-modulation and intracellular depletion. Proc Natl Acad Sci U S A 106 2868 2873

49. RollasonRKorolchukVHamiltonCJepsonMBantingG 2009 A CD317/tetherin-RICH2 complex plays a critical role in the organization of the subapical actin cytoskeleton in polarized epithelial cells. J Cell Biol 184 721 736

50. AndrewAJKaoSStrebelK 2011 The C-terminal hydrophobic region in human BST-2/tetherin functions as a second transmembrane motif. J Biol Chem 286 39967 39981

51. Pais-CorreiaAMSachseMGuadagniniSRobbiatiVLasserreR 2009 Biofilm-like extracellular viral assemblies mediate HTLV-1 cell-to-cell transmission at virological synapses. Nat Med 16 83 89

52. MasuyamaNKuronitaTTanakaRMutoTHirotaY 2009 HM1.24 is internalized from lipid rafts by clathrin-mediated endocytosis through interaction with alpha-adaptin. J Biol Chem 284 15927 15941

53. NguyenDHHildrethJE 2000 Evidence for budding of human immunodeficiency virus type 1 selectively from glycolipid-enriched membrane lipid rafts. J Virol 74 3264 3272

54. OnoAFreedEO 2001 Plasma membrane rafts play a critical role in HIV-1 assembly and release. Proc Natl Acad Sci U S A 98 13925 13930

55. MiyagiEAndrewAKaoSYoshidaTStrebelK 2011 Antibody-mediated enhancement of HIV-1 and HIV-2 production from BST-2/tetherin+ cells. J Virol 85 11981 11994

56. LingwoodDSimonsK 2010 Lipid rafts as a membrane-organizing principle. Science 327 46 50

57. van ZantenTSGomezJManzoCCambiABucetaJ 2010 Direct mapping of nanoscale compositional connectivity on intact cell membranes. Proc Natl Acad Sci U S A 107 15437 15442

58. HogueIBGroverJRSoheilianFNagashimaKOnoA 2011 Gag Induces the Coalescence of Clustered Lipid Rafts and Tetraspanin-Enriched Microdomains at HIV-1 Assembly Sites on the Plasma Membrane. J Virol 85 9749 9766

59. KrementsovDNRassamPMargeatERoyNHSchneider-SchauliesJ 2010 HIV-1 assembly differentially alters dynamics and partitioning of tetraspanins and raft components. Traffic 11 1401 1414

60. NaldiniLBlomerUGallayPOryDMulliganR 1996 In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272 263 267

61. SchneiderRCampbellMNasioulasGFelberBKPavlakisGN 1997 Inactivation of the human immunodeficiency virus type 1 inhibitory elements allows Rev-independent expression of Gag and Gag/protease and particle formation. J Virol 71 4892 4903

62. AndoRMizunoHMiyawakiA 2004 Regulated fast nucleocytoplasmic shuttling observed by reversible protein highlighting. Science 306 1370 1373

63. HabuchiSTsutsuiHKochaniakABMiyawakiAvan OijenAM 2008 mKikGR, a monomeric photoswitchable fluorescent protein. PLoS One 3 e3944

64. ChudakovDMLukyanovSLukyanovKA 2007 Tracking intracellular protein movements using photoswitchable fluorescent proteins PS-CFP2 and Dendra2. Nat Protoc 2 2024 2032

65. SubachFVMalashkevichVNZencheckWDXiaoHFilonovGS 2009 Photoactivation mechanism of PAmCherry based on crystal structures of the protein in the dark and fluorescent states. Proc Natl Acad Sci U S A 106 21097 21102

66. WendyLMartinezARM 2008 Computational Statistics Handbook with MATLAB. Chapman & Hall/CRC

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Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

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