Structural Basis for Tetherin Antagonism as a Barrier to Zoonotic Lentiviral Transmission

Cell Host and Microbe

Volumn 26, Issue 3, 2019, Pages 359-368.e8

  Buffalo, Cosmo Z ^a   Stürzel, Christina M ^b   Heusinger, Elena ^b   Kmiec, Dorota ^b   Kirchhoff, Frank ^b   Hurley, James H ^a,c   Ren, Xuefeng ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY HOSPITAL ULM   (Germany)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

adaptor protein; clathrin; cryo EM; HIV; host factor restriction; hydrogen deuterium exchange; SIV; tetherin; trafficking

Indexed keywords

BETA ADAPTIN; BONE MARROW STROMAL ANTIGEN 2; CD3 ANTIGEN; CD4 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NEF PROTEIN; TRANSCRIPTION FACTOR AP 2; VIRUS ENVELOPE PROTEIN; ADAPTOR PROTEIN; ANTIMICROBIAL CATIONIC PEPTIDE; AP2B1 PROTEIN, HUMAN; HLA ANTIGEN CLASS 1; MEMBRANE PROTEIN; SERINC5 PROTEIN, HUMAN;

AMINO TERMINAL SEQUENCE; ARTICLE; CERCOCEBUS ATYS; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; DOWN REGULATION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN INTERACTION; PROTEIN STRUCTURE; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; SURFACE PROPERTY; VIRUS TRANSMISSION; ZOONOSIS; ALPHA HELIX; ANIMAL; BINDING SITE; CELL MEMBRANE; CHEMISTRY; DRUG EFFECT; HEK293 CELL LINE; LENTIVIRUS INFECTION; METABOLISM; MOLECULAR MODEL; PRIMARY CELL CULTURE; PROTEIN DOMAIN; PROTEIN FOLDING; SEQUENCE ALIGNMENT; VIRION; VIROLOGY;

ADAPTOR PROTEIN COMPLEX 2; ADAPTOR PROTEIN COMPLEX BETA SUBUNITS; ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; BINDING SITES; BONE MARROW STROMAL ANTIGEN 2; CD3 COMPLEX; CD4 ANTIGENS; CELL MEMBRANE; CRYOELECTRON MICROSCOPY; DOWN-REGULATION; GENE PRODUCTS, NEF; HEK293 CELLS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; LENTIVIRUS INFECTIONS; MEMBRANE PROTEINS; MODELS, MOLECULAR; PRIMARY CELL CULTURE; PROTEIN CONFORMATION; PROTEIN CONFORMATION, ALPHA-HELICAL; PROTEIN FOLDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; SEQUENCE ALIGNMENT; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VIRION; ZOONOSES;

EID: 85071288828     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2019.08.002     Document Type: Article

References (64)

1. Adams, P.D., Afonine, P.V., Bubkóczi, G., Chen, V.B., Davis, I.W., Echols, N., Headd, J.J., Hung, L.-W., Kapral, G.J., Gross-Kunstleve, R.W., et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66 (2010), 213–221.
2. Afonine, P.V., Poon, B.K., Read, R.J., Sobolev, O.V., Terwilliger, T.C., Urzhumtsev, A., Adams, P.D., Real-space refinement in PHENIX for cryo-EM and Crystallography. Acta Crystallogr. Struct. Biol. 74 (2018), 531–544.
3. Aiken, C., Konner, J., Landau, N.R., Lenburg, M.E., Trono, D., Nef induces CD4 endocytosis: requirement for a critical dileucine motif in the membrane-proximal CD4 cytoplasmic domain. Cell 76 (1994), 853–864.
4. Barad, B.A., Echols, N., Wang, R.Y., Cheng, Y., DiMaio, F., Adams, P.D., Fraser, J.S., EMRinger: side chain-directed model and map validation for 3D cryo-electron microscopy. Nat. Methods 12 (2015), 943–946.
5. Braun, E., Hotter, D., Koepke, L., Zech, F., Groß, R., Sparrer, K.M.J., Müller, J.A., Pfaller, C.K., Heusinger, E., Wombacher, R., et al. Guanylate-Binding Proteins 2 and 5 Exert Broad Antiviral Activity by Inhibiting Furin-Mediated Processing of Viral Envelope Proteins. Cell Rep 27 (2019), 2092–2104.
6. Bresnahan, P.A., Yonemoto, W., Ferrell, S., Williams-Herman, D., Geleziunas, R., Greene, W.C., A dileucine motif in HIV-1 Nef acts as an internalization signal for CD4 downregulation and binds the AP-1 clathrin adaptor. Curr. Biol. 8 (1998), 1235–1238.
7. Canagarajah, B.J., Ren, X., Bonifacino, J.S., Hurley, J.H., The clathrin adaptor complexes as a paradigm for membrane-associated allostery. Protein Sci. 22 (2013), 517–529.
8. Chaudhuri, R., Lindwasser, O.W., Smith, W.J., Hurley, J.H., Bonifacino, J.S., Downregulation of CD4 by human immunodeficiency virus type 1 Nef is dependent on clathrin and involves direct interaction of Nef with the AP2 clathrin adaptor. J. Virol. 81 (2007), 3877–3890.
9. Collins, D.R., Collins, K.L., HIV-1 accessory proteins adapt cellular adaptors to facilitate immune evasion. PLoS Pathog., 10, 2014, e1003851.
10. Craig, H.M., Pandori, M.W., Guatelli, J.C., Interaction of HIV-1 Nef with the cellular dileucine-based sorting pathway is required for CD4 down-regulation and optimal viral infectivity. Proc. Natl. Acad. Sci. USA 95 (1998), 11229–11234.
11. Davis, I.W., Leaver-Fay, A., Chen, V.B., Block, J.N., Kapral, G.J., Wang, X., Murray, L.W., Arendall, W.B. 3rd, Snoeyink, J., Richardson, J.S., et al. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35 (2007), W375–W383.
12. Du, Y., Fluorescence polarization assay to quantify protein-protein interactions in an HTS format. Methods Mol. Biol. 1278 (2015), 529–544.
13. DuBridge, R.B., Tang, P., Hsia, H.C., Leong, P.M., Miller, J.H., Calos, M.P., Analysis of mutation in human cells by using an Epstein-Barr virus shuttle system. Mol. Cell. Biol. 7 (1987), 379–387.
14. Emsley, P., Lohkamp, B., Scott, W.G., Cowtan, K., Features and development of coot. Acta Crystallogr. D Biol. Crystallogr. 66 (2010), 486–501.
15. Fouchier, R.A., Meyer, B.E., Simon, J.H., Fischer, U., Malim, M.H., HIV-1 infection of non-dividing cells: evidence that the amino-terminal basic region of the viral matrix protein is important for Gag processing but not for post-entry nuclear import. EMBO J. 16 (1997), 4531–4539.
16. Heusinger, E., Deppe, K., Sette, P., Krapp, C., Kmiec, D., Kluge, S.F., Marx, P.A., Apetrei, C., Kirchhoff, F., Sauter, D., Preadaptation of simian immunodeficiency virus SIVsmm facilitated env-mediated counteraction of human tetherin by human immunodeficiency virus type 2. J. Virol., 92, 2018.
17. Hoover, D.M., Lubkowski, J., DNAWorks: an automated method for designing oligonucleotides for PCR-based gene synthesis. Nucleic Acids Res., 30, 2002, e43.
18. Jackson, L.P., Kelly, B.T., McCoy, A.J., Gaffry, T., James, L.C., Collins, B.M., Höning, S., Evans, P.R., Owen, D.J., A large-scale conformational change couples membrane recruitment to cargo binding in the AP2 clathrin adaptor complex. Cell 141 (2010), 1220–1229.
19. Jia, B., Serra-Moreno, R., Neidermyer, W., Rahmberg, A., Mackey, J., Fofana, I.B., Johnson, W.E., Westmoreland, S., Evans, D.T., Species-specific activity of SIV Nef and HIV-1 Vpu in overcoming restriction by tetherin/BST2. PLoS Pathog., 5, 2009, e1000429.
20. Jia, X., Singh, R., Homann, S., Yang, H., Guatelli, J., Xiong, Y., Structural basis of evasion of cellular adaptive immunity by HIV-1 Nef. Nat. Struct. Mol. Biol. 19 (2012), 701–706.
21. Jia, X., Weber, E., Tokarev, A., Lewinski, M., Rizk, M., Suarez, M., Guatelli, J., Xiong, Y., Structural basis of HIV-1 Vpu-mediated BST2 antagonism via hijacking of the clathrin adaptor protein complex 1. Elife, 3, 2014, e02362.
22. Joas, S., Parrish, E.H., Gnanadurai, C.W., Lump, E., Stürzel, C.M., Parrish, N.F., Learn, G.H., Sauermann, U., Neumann, B., Rensing, K.M., et al. Species-specific host factors rather than virus-intrinsic virulence determine primate lentiviral pathogenicity. Nat. Commun., 9, 2018, 1371.
23. Kimanius, D., Forsberg, B.O., Scheres, S.H., Lindahl, E., Accelerated cryo-EM structure determination with parallelisation using GPUs in RELION-2. Elife, 5, 2016.
24. Kluge, S.F., Mack, K., Iyer, S.S., Pujol, F.M., Heigele, A., Learn, G.H., Usmani, S.M., Sauter, D., Joas, S., Hotter, D., et al. Nef proteins of epidemic HIV-1 group O strains antagonize human tetherin. Cell Host Microbe 16 (2014), 639–650.
25. Kmiec, D., Akbil, B., Ananth, S., Hotter, D., Sparrer, K.M.J., Stürzel, C.M., Trautz, B., Ayouba, A., Peeters, M., Yao, Z., et al. SIVcol Nef counteracts SERINC5 by promoting its proteasomal degradation but does not efficiently enhance HIV-1 replication in human CD4+ T cells and lymphoid tissue. PLoS Pathog., 14, 2018, e1007269.
26. Kueck, T., Foster, T.L., Weinelt, J., Sumner, J.C., Pickering, S., Neil, S.J., Serine phosphorylation of HIV-1 Vpu and its binding to tetherin regulates interaction with clathrin adaptors. PLoS Pathog., 11, 2015, e1005141.
27. Le Gall, S., Erdtmann, L., Benichou, S., Berlioz-Torrent, C., Liu, L., Benarous, R., Heard, J.M., Schwartz, O., Nef interacts with the mu subunit of clathrin adaptor complexes and reveals a cryptic sorting signal in MHC I molecules. Immunity 8 (1998), 483–495.
28. Le Tortorec, A., Neil, S.J., Antagonism to and intracellular sequestration of human tetherin by the human immunodeficiency virus type 2 envelope glycoprotein. J. Virol. 83 (2009), 11966–11978.
29. Leonard, J.A., Filzen, T., Carter, C.C., Schaefer, M., Collins, K.L., HIV-1 Nef disrupts intracellular trafficking of major histocompatibility complex class I, CD4, CD8, and CD28 by distinct pathways that share common elements. J. Virol. 85 (2011), 6867–6881.
30. Mack, K., Starz, K., Sauter, D., Langer, S., Bibollet-Ruche, F., Learn, G.H., Stürzel, C.M., Leoz, M., Plantier, J.C., Geyer, M., et al. Efficient Vpu-mediated tetherin antagonism by an HIV-1 group O strain. J. Virol., 91, 2017.
31. Malim, M.H., Bieniasz, P.D., HIV restriction factors and mechanisms of evasion. Cold Spring Harb. Perspect. Med., 2, 2012, a006940.
32. Manrique, S., Sauter, D., Horenkamp, F.A., Lülf, S., Yu, H., Hotter, D., Anand, K., Kirchhoff, F., Geyer, M., Endocytic sorting motif interactions involved in Nef-mediated downmodulation of CD4 and CD3. Nat. Commun., 8, 2017, 442.
33. Moerke, N.J., Fluorescence polarization (FP) assays for monitoring peptide-protein or nucleic acid-protein binding. Curr. Protoc. Chem. Biol. 1 (2009), 1–15.
34. Morris, K.L., Buffalo, C.Z., Stürzel, C.M., Heusinger, E., Kirchhoff, F., Ren, X., Hurley, J.H., HIV-1 nefs are cargo-sensitive AP-1 trimerization switches in tetherin downregulation. Cell 174 (2018), 659–671.
35. Münch, J., Rajan, D., Schindler, M., Specht, A., Rücker, E., Novembre, F.J., Nerrienet, E., Müller-Trutwin, M.C., Peeters, M., Hahn, B.H., et al. Nef-mediated enhancement of virion infectivity and stimulation of viral replication are fundamental properties of primate lentiviruses. J. Virol. 81 (2007), 13852–13864.
36. Neil, S.J., Zang, T., Bieniasz, P.D., Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451 (2008), 425–430.
37. Olsen, S.K., Lima, C.D., Structure of a ubiquitin E1-E2 complex: insights to E1-E2 thioester transfer. Mol. Cell 49 (2013), 884–896.
38. Pereira, E.A., daSilva, L.L., HIV-1 nef: taking control of protein trafficking. Traffic 17 (2016), 976–996.
39. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C., Ferrin, T.E., UCSF Chimera–a visualization system for exploratory research and analysis. J. Comput. Chem. 25 (2004), 1605–1612.
40. Platt, E.J., Wehrly, K., Kuhmann, S.E., Chesebro, B., Kabat, D., Effects of CCR5 and CD4 cell surface concentrations on infections by macrophagetropic isolates of human immunodeficiency virus type 1. J. Virol. 72 (1998), 2855–2864.
41. Punjani, A., Rubinstein, J.L., Fleet, D.J., Brubaker, M.A., cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination. Nat. Methods 14 (2017), 290–296.
42. Ren, X., Farías, G.G., Canagarajah, B.J., Bonifacino, J.S., Hurley, J.H., Structural basis for recruitment and activation of the AP-1 clathrin adaptor complex by Arf1. Cell 152 (2013), 755–767.
43. Ren, X., Park, S.Y., Bonifacino, J.S., Hurley, J.H., How HIV-1 Nef hijacks the AP-2 clathrin adaptor to downregulate CD4. Elife, 3, 2014, e01754.
44. Rohou, A., Grigorieff, N., CTFFIND4: fast and accurate defocus estimation from electron micrographs. J. Struct. Biol. 192 (2015), 216–221.
45. Rosa, A., Chande, A., Ziglio, S., De Sanctis, V., Bertorelli, R., Goh, S.L., McCauley, S.M., Nowosielska, A., Antonarakis, S.E., Luban, J., et al. HIV-1 Nef promotes infection by excluding SERINC5 from virion incorporation. Nature 526 (2015), 212–217.
46. Sauter, D., Kirchhoff, F., Key viral adaptations preceding the AIDS pandemic. Cell Host Microbe 25 (2019), 27–38.
47. Sauter, D., Schindler, M., Specht, A., Landford, W.N., Münch, J., Kim, K.A., Votteler, J., Schubert, U., Bibollet-Ruche, F., Keele, B.F., et al. Tetherin-driven adaptation of Vpu and Nef function and the evolution of pandemic and nonpandemic HIV-1 strains. Cell Host Microbe 6 (2009), 409–421.
48. Scheres, S.H., RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180 (2012), 519–530.
49. Schindler, M., Münch, J., Kutsch, O., Li, H., Santiago, M.L., Bibollet-Ruche, F., Müller-Trutwin, M.C., Novembre, F.J., Peeters, M., Courgnaud, V., et al. Nef-mediated suppression of T cell activation was lost in a lentiviral lineage that gave rise to HIV-1. Cell 125 (2006), 1055–1067.
50. Schmökel, J., Li, H., Bailes, E., Schindler, M., Silvestri, G., Hahn, B.H., Apetrei, C., Kirchhoff, F., Conservation of Nef function across highly diverse lineages of SIVsmm. Retrovirology, 6, 2009, 36.
51. Schmökel, J., Sauter, D., Schindler, M., Leendertz, F.H., Bailes, E., Dazza, M.C., Saragosti, S., Bibollet-Ruche, F., Peeters, M., Hahn, B.H., et al. The presence of a vpu gene and the lack of Nef-mediated downmodulation of T cell receptor-CD3 are not always linked in primate lentiviruses. J. Virol. 85 (2011), 742–752.
52. Schouest, B., Weiler, A.M., Janaka, S.K., Myers, T.A., Das, A., Wilder, S.C., Furlott, J., Baddoo, M., Flemington, E.K., Rakasz, E.G., et al. Maintenance of AP-2-dependent functional activities of nef restricts pathways of immune escape from CD8 T lymphocyte responses. J. Virol., 92, 2018.
53. Selleck, W., Tan, S., Recombinant protein complex expression in E. coli. Curr. Protoc. Protein Sci., 21, 2008 Chapter 5, Unit 5.
54. Serra-Moreno, R., Zimmermann, K., Stern, L.J., Evans, D.T., Tetherin/BST-2 antagonism by Nef depends on a direct physical interaction between Nef and tetherin, and on clathrin-mediated endocytosis. PLoS Pathog., 9, 2013, e1003487.
55. Sheffield, P., Garrard, S., Derewenda, Z., Overcoming expression and purification problems of RhoGDI using a family of “parallel” expression vectors. Protein Expr. Purif. 15 (1999), 34–39.
56. Shen, Q.T., Ren, X., Zhang, R., Lee, I.H., Hurley, J.H., HIV-1 Nef hijacks clathrin coats by stabilizing AP-1:Arf1 polygons. Science, 350, 2015, aac5137.
57. Traub, L.M., Bonifacino, J.S., Cargo recognition in clathrin-mediated endocytosis. Cold Spring Harb. Perspect. Biol., 5, 2013, a016790.
58. Usami, Y., Wu, Y., Göttlinger, H.G., SERINC3 and SERINC5 restrict HIV-1 infectivity and are counteracted by Nef. Nature 526 (2015), 218–223.
59. Wildum, S., Schindler, M., Münch, J., Kirchhoff, F., Contribution of Vpu, Env, and Nef to CD4 down-modulation and resistance of human immunodeficiency virus type 1-infected T cells to superinfection. J. Virol. 80 (2006), 8047–8059.
60. Zhang, F., Landford, W.N., Ng, M., McNatt, M.W., Bieniasz, P.D., Hatziioannou, T., SIV Nef proteins recruit the AP-2 complex to antagonize Tetherin and facilitate virion release. PLoS Pathog., 7, 2011, e1002039.
61. Zhang, F., Wilson, S.J., Landford, W.C., Virgen, B., Gregory, D., Johnson, M.C., Munch, J., Kirchhoff, F., Bieniasz, P.D., Hatziioannou, T., Nef proteins from simian immunodeficiency viruses are tetherin antagonists. Cell Host Microbe 6 (2009), 54–67.
62. Zhang, K., Gctf: real-time CTF determination and correction. J. Struct. Biol. 193 (2016), 1–12.
63. Zheng, S.Q., Palovcak, E., Armache, J.P., Verba, K.A., Cheng, Y., Agard, D.A., MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14 (2017), 331–332.
64. Zivanov, J., Nakane, T., Forsberg, B.O., Kimanius, D., Hagen, W.J., Lindahl, E., Scheres, S.H., New tools for automated high-resolution cryo-EM structure determination in RELION-3. Elife, 7, 2018.