Physiological and molecular triggers for SARS-CoV membrane fusion and entry into host cells

Virology

Volumn 517, Issue , 2018, Pages 3-8

  Millet, Jean Kaoru ^a   Whittaker, Gary R ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

Calcium; Coronavirus; Endosomes; Fusion peptide; SARS; Spike protein; Virus entry

Indexed keywords

CORE PROTEIN; CORONAVIRUS S FUSION PEPTIDE; UNCLASSIFIED DRUG; VIRUS FUSION PROTEIN; CORONAVIRUS SPIKE GLYCOPROTEIN; VIRUS ENVELOPE PROTEIN;

ARTICLE; CYTOLOGY; GENE LOCATION; HOST CELL; MEMBRANE FUSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SARS-RELATED CORONAVIRUS; SIGNAL TRANSDUCTION; VIRUS ENTRY; CELL MEMBRANE; CHEMISTRY; HUMAN; PHYSIOLOGY; SARS CORONAVIRUS;

CELL MEMBRANE; HUMANS; MEMBRANE FUSION; SARS VIRUS; SPIKE GLYCOPROTEIN, CORONAVIRUS; VIRAL ENVELOPE PROTEINS; VIRUS INTERNALIZATION;

EID: 85038832920     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2017.12.015     Document Type: Article

References (72)

1. Apellaniz, B., Huarte, N., Largo, E., Nieva, J.L., The three lives of viral fusion peptides. Chem. Phys. Lipids 181 (2014), 40–55.
2. Basso, L.G., Vicente, E.F., Crusca, E. Jr., Cilli, E.M., Costa-Filho, A.J., SARS-CoV fusion peptides induce membrane surface ordering and curvature. Sci. Rep., 6, 2016, 37131.
3. Belouzard, S., Chu, V.C., Whittaker, G.R., Activation of the SARS coronavirus spike protein via sequential proteolytic cleavage at two distinct sites. Proc. Natl. Acad. Sci. 106 (2009), 5871–5876.
4. Belouzard, S., Millet, J.K., Licitra, B.N., Whittaker, G.R., Mechanisms of coronavirus cell entry mediated by the viral spike protein. Viruses 4 (2012), 1011–1033.
5. Bertram, S., Dijkman, R., Habjan, M., Heurich, A., Gierer, S., Glowacka, I., Welsch, K., Winkler, M., Schneider, H., Hofmann-Winkler, H., Thiel, V., Pöhlmann, S., TMPRSS2 activates the human coronavirus 229E for cathepsin-independent host cell entry and is expressed in viral target cells in the respiratory epithelium. J. Virol. 87 (2013), 6150–6160.
6. Bertram, S., Glowacka, I., Muller, M.A., Lavender, H., Gnirss, K., Nehlmeier, I., Niemeyer, D., He, Y., Simmons, G., Drosten, C., Soilleux, E.J., Jahn, O., Steffen, I., Pöhlmann, S., Cleavage and activation of the SARS-coronavirus spike-protein by human airway trypsin-like protease. J. Virol. 85 (2011), 13363–13372.
7. Bosch, B.J., van der Zee, R., de Haan, C.A.M., Rottier, P.J.M., The coronavirus spike protein is a class I virus fusion protein: structural and functional characterization of the fusion core complex. J. Virol. 77 (2003), 8801–8811.
8. Boulant, S., Stanifer, M., Lozach, P.Y., Dynamics of virus-receptor interactions in virus binding, signaling, and endocytosis. Viruses 7 (2015), 2794–2815.
9. Burkard, C., Verheije, M.H., Wicht, O., van Kasteren, S.I., van Kuppeveld, F.J., Haagmans, B.L., Pelkmans, L., Rottier, P.J.M., Bosch, B.J., de Haan, C.A.M., Coronavirus cell entry occurs through the endo-/lysosomal pathway in a proteolysis-dependent manner. PLoS Pathog., 10, 2014, e1004502.
10. Chernomordik, L.V., Kozlov, M.M., Mechanics of membrane fusion. Nat. Struct. Mol. Biol. 15 (2008), 675–683.
11. Colman, P.M., Lawrence, M.C., The structural biology of type I viral membrane fusion. Nat. Rev. Mol. Cell Biol. 4 (2003), 309–319.
12. Costello, D.A., Millet, J.K., Hsia, C.Y., Whittaker, G.R., Daniel, S., Single particle assay of coronavirus membrane fusion with proteinaceous receptor-embedded supported bilayers. Biomaterials 34 (2013), 7895–7904.
13. de Groot, R.J., Cowley, J.A., Enjuanes, L., Faaberg, K.S., Perlman, S., Rottier, P.J.M., Snijder, E.J., Ziebuhr, J., Gorbalenya, A.E., Order - Nidovirales. King, A.M.Q., Adams, M.J., Carstens, E.B., Lefkowitz, E.J., (eds.) Virus Taxonomy, 2012, Elsevier, San Diego, 784–794.
14. Delos, S.E., Brecher, M.B., Chen, Z., Melder, D.C., Federspiel, M.J., White, J.M., Cysteines flanking the internal fusion peptide are required for the avian sarcoma/leukosis virus glycoprotein to mediate the lipid mixing stage of fusion with high efficiency. J. Virol. 82 (2008), 3131–3134.
15. Dube, M., Etienne, L., Fels, M., Kielian, M., Calcium-dependent rubella virus fusion occurs in early endosomes. J. Virol. 90 (2016), 6303–6313.
16. Dube, M., Rey, F.A., Kielian, M., Rubella virus: first calcium-requiring viral fusion protein. PLoS Pathog., 10, 2014, e1004530.
17. Earnest, J.T., Hantak, M.P., Li, K., McCray, P.B. Jr., Perlman, S., Gallagher, T., The tetraspanin CD9 facilitates MERS-coronavirus entry by scaffolding host cell receptors and proteases. PLoS Pathog., 13, 2017, e1006546.
18. Epand, R.M., Fusion peptides and the mechanism of viral fusion. Biochim. Biophys. Acta (BBA) - Biomembr. 1614 (2003), 116–121.
19. Ge, M., Freed, J.H., Fusion peptide from influenza hemagglutinin increases membrane surface order: an electron-spin resonance study. Biophys. J. 96 (2009), 4925–4934.
20. Ge, M., Freed, J.H., Two conserved residues are important for inducing highly ordered membrane domains by the transmembrane domain of influenza hemagglutinin. Biophys. J. 100 (2011), 90–97.
21. Gierer, S., Bertram, S., Kaup, F., Wrensch, F., Heurich, A., Kramer-Kuhl, A., Welsch, K., Winkler, M., Meyer, B., Drosten, C., Dittmer, U., von Hahn, T., Simmons, G., Hofmann, H., Pöhlmann, S., The spike-protein of the emerging betacoronavirus EMC uses a novel coronavirus receptor for entry, can be activated by TMPRSS2 and is targeted by neutralizing antibodies. J. Virol. 87 (2013), 5502–5511.
22. Glowacka, I., Bertram, S., Müller, M.A., Allen, P., Soilleux, E., Pfefferle, S., Steffen, I., Tsegaye, T.S., He, Y., Gnirss, K., Niemeyer, D., Schneider, H., Drosten, C., Pöhlmann, S., Evidence that TMPRSS2 activates the severe acute respiratory syndrome coronavirus spike protein for membrane fusion and reduces viral control by the humoral immune response. J. Virol. 85 (2011), 4122–4134.
23. Graham, R.L., Donaldson, E.F., Baric, R.S., A decade after SARS: strategies for controlling emerging coronaviruses. Nat. Rev. Microbiol. 11 (2013), 836–848.
24. Grove, J., Marsh, M., The cell biology of receptor-mediated virus entry. J. Cell Biol. 195 (2011), 1071–1082.
25. Gui, M., Song, W., Zhou, H., Xu, J., Chen, S., Xiang, Y., Wang, X., Cryo-electron microscopy structures of the SARS-CoV spike glycoprotein reveal a prerequisite conformational state for receptor binding. Cell Res. 27 (2017), 119–129.
26. Guillen, J., Kinnunen, P.K.J., Villalain, J., Membrane insertion of the three main membranotropic sequences from SARS-CoV S2 glycoprotein. Biochim. Biophys. Acta (BBA) - Biomembr. 1778 (2008), 2765–2774.
27. Guillen, J., Perez-Berna, A.J., Moreno, M.R., Villalain, J., Identification of the membrane-active regions of the severe acute respiratory syndrome coronavirus spike membrane glycoprotein using a 16/18-mer peptide scan: implications for the viral fusion mechanism. J. Virol. 79 (2005), 1743–1752.
28. Guillén, J., Pérez-Berná, A.J., Moreno, M.R., Villalaín, J., A Second SARS-CoV S2 Glycoprotein Internal Membrane-Active Peptide. Biophysical Characterization and Membrane Interaction. Biochemistry 47 (2008), 8214–8224.
29. Harrison, S.C., Viral membrane fusion. Nat. Struct. Mol. Biol. 15 (2008), 690–698.
30. Harrison, S.C., Viral membrane fusion. Virology 479–480 (2015), 498–507.
31. Hofmann, H., Pöhlmann, S., Cellular entry of the SARS coronavirus. Trends Microbiol. 12 (2004), 466–472.
32. Hulswit, R.J., de Haan, C.A., Bosch, B.J., Coronavirus spike protein and tropism changes. Adv. Virus Res. 96 (2016), 29–57.
33. Huotari, J., Helenius, A., Endosome maturation. EMBO J. 30 (2011), 3481–3500.
34. Inoue, Y., Tanaka, N., Tanaka, Y., Inoue, S., Morita, K., Zhuang, M., Hattori, T., Sugamura, K., Clathrin-dependent entry of severe acute respiratory syndrome coronavirus into target cells expressing ACE2 with the cytoplasmic tail deleted. J. Virol. 81 (2007), 8722–8729.
35. Jeffers, S.A., Tusell, S.M., Gillim-Ross, L., Hemmila, E.M., Achenbach, J.E., Babcock, G.J., Thomas, W.D. Jr., Thackray, L.B., Young, M.D., Mason, R.J., Ambrosino, D.M., Wentworth, D.E., Demartini, J.C., Holmes, K.V., CD209L (L-SIGN) is a receptor for severe acute respiratory syndrome coronavirus. Proc. Natl. Acad. Sci. USA 101 (2004), 15748–15753.
36. Kirchdoerfer, R.N., Cottrell, C.A., Wang, N., Pallesen, J., Yassine, H.M., Turner, H.L., Corbett, K.S., Graham, B.S., McLellan, J.S., Ward, A.B., Pre-fusion structure of a human coronavirus spike protein. Nature 531 (2016), 118–121.
37. Lai, A.L., Freed, J.H., HIV gp41 fusion peptide increases membrane ordering in a cholesterol-dependent fashion. Biophys. J. 106 (2014), 172–181.
38. Lai, A.L., Freed, J.H., The Interaction between Influenza HA Fusion Peptide and Transmembrane Domain Affects Membrane Structure. Biophys. J. 109 (2015), 2523–2536.
39. Lai, A.L., Li, Y., Tamm, L.K., Interplay of Proteins and Lipids in Virus Entry by Membrane Fusion, Protein–Lipid Interactions. 2005, Wiley-VCH Verlag GmbH & Co. KGaA, 279–303.
40. Lai, A.L., Millet, J.K., Daniel, S., Freed, J.H., Whittaker, G.R., The SARS-CoV fusion peptide forms an extended bipartite fusion platform that perturbs membrane order in a calcium-dependent manner. J. Mol. Biol. 429 (2017), 3875–3892.
41. Li, W., Moore, M.J., Vasilieva, N., Sui, J., Wong, S.K., Berne, M.A., Somasundaran, M., Sullivan, J.L., Luzuriaga, K., Greenough, T.C., Choe, H., Farzan, M., Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 426 (2003), 450–454.
42. Luzio, J.P., Bright, N.A., Pryor, P.R., The role of calcium and other ions in sorting and delivery in the late endocytic pathway. Biochem. Soc. Trans. 35 (2007), 1088–1091.
43. Madu, I.G., Belouzard, S., Whittaker, G.R., SARS-coronavirus spike S2 domain flanked by cysteine residues C822 and C833 is important for activation of membrane fusion. Virology 393 (2009), 265–271.
44. Madu, I.G., Roth, S.L., Belouzard, S., Whittaker, G.R., Characterization of a highly conserved domain within the severe acute respiratory syndrome coronavirus spike protein S2 domain with characteristics of a viral fusion peptide. J. Virol. 83 (2009), 7411–7421.
45. Mahajan, M., Bhattacharjya, S., NMR structures and localization of the potential fusion peptides and the pre-transmembrane region of SARS-CoV: implications in membrane fusion. Biochim. Biophys. Acta 1848 (2015), 721–730.
46. Marsh, M., Helenius, A., Virus entry: open sesame. Cell 124 (2006), 729–740.
47. Matsuyama, S., Nagata, N., Shirato, K., Kawase, M., Takeda, M., Taguchi, F., Efficient activation of the severe acute respiratory syndrome coronavirus spike protein by the transmembrane protease TMPRSS2. J. Virol. 84 (2010), 12658–12664.
48. Matsuyama, S., Taguchi, F., Two-step conformational changes in a coronavirus envelope glycoprotein mediated by receptor binding and proteolysis. J. Virol. 83 (2009), 11133–11141.
49. Matsuyama, S., Ujike, M., Morikawa, S., Tashiro, M., Taguchi, F., Protease-mediated enhancement of severe acute respiratory syndrome coronavirus infection. Proc. Natl. Acad. Sci. 102 (2005), 12543–12547.
50. Millet, J.K., Whittaker, G.R., Host cell entry of Middle East respiratory syndrome coronavirus after two-step, furin-mediated activation of the spike protein. Proc. Natl. Acad. Sci. 111 (2014), 15214–15219.
51. Millet, J.K., Whittaker, G.R., Host cell proteases: critical determinants of coronavirus tropism and pathogenesis. Virus Res. 202 (2015), 120–134.
52. Mingo, R.M., Simmons, J.A., Shoemaker, C.J., Nelson, E.A., Schornberg, K.L., D'Souza, R.S., Casanova, J.E., White, J.M., Ebola virus and severe acute respiratory syndrome coronavirus display late cell entry kinetics: evidence that transport to NPC1+ endolysosomes is a rate-defining step. J. Virol. 89 (2015), 2931–2943.
53. Nash, T.C., Buchmeier, M.J., Entry of mouse hepatitis virus into cells by endosomal and nonendosomal pathways. Virology 233 (1997), 1–8.
54. Petit, C.M., Melancon, J.M., Chouljenko, V.N., Colgrove, R., Farzan, M., Knipe, D.M., Kousoulas, K.G., Genetic analysis of the SARS-coronavirus spike glycoprotein functional domains involved in cell-surface expression and cell-to-cell fusion. Virology 341 (2005), 215–230.
55. Pinello, J.F., Lai, A.L., Millet, J.K., Cassidy-Hanley, D., Freed, J.H., Clark, T.G., Structure-function studies link class II viral fusogens with the ancestral gamete fusion protein HAP2. Curr. Biol.: CB 27 (2017), 651–660.
56. Reinke, L.M., Spiegel, M., Plegge, T., Hartleib, A., Nehlmeier, I., Gierer, S., Hoffmann, M., Hofmann-Winkler, H., Winkler, M., Pohlmann, S., Different residues in the SARS-CoV spike protein determine cleavage and activation by the host cell protease TMPRSS2. PLoS One, 12, 2017, e0179177.
57. Scott, C.C., Gruenberg, J., Ion flux and the function of endosomes and lysosomes: pH is just the start. Bioessays 33 (2010), 103–110.
58. Shulla, A., Heald-Sargent, T., Subramanya, G., Zhao, J., Perlman, S., Gallagher, T., A transmembrane serine protease is linked to the severe acute respiratory syndrome coronavirus receptor and activates virus entry. J. Virol. 85 (2011), 873–882.
59. Simmons, G., Gosalia, D.N., Rennekamp, A.J., Reeves, J.D., Diamond, S.L., Bates, P., Inhibitors of cathepsin L prevent severe acute respiratory syndrome coronavirus entry. Proc. Natl. Acad. Sci. USA 102 (2005), 11876–11881.
60. Simmons, G., Reeves, J.D., Rennekamp, A.J., Amberg, S.M., Piefer, A.J., Bates, P., Characterization of severe acute respiratory syndrome-associated coronavirus (SARS-CoV) spike glycoprotein-mediated viral entry. Proc. Natl. Acad. Sci. 101 (2004), 4240–4245.
61. Stadler, K., Ha, H.R., Ciminale, V., Spirli, C., Saletti, G., Schiavon, M., Bruttomesso, D., Bigler, L., Follath, F., Pettenazzo, A., Baritussio, A., Amiodarone alters late endosomes and inhibits SARS coronavirus infection at a post-endosomal level. Am. J. Respir. Cell Mol. Biol. 39 (2008), 142–149.
62. Sun, X., Belouzard, S., Whittaker, G.R., Molecular architecture of the bipartite fusion loops of vesicular stomatitis virus glycoprotein G, a class III viral fusion protein. J. Biol. Chem. 283 (2008), 6418–6427.
63. Tamm, L.K., Han, X., Viral fusion peptides: a tool set to disrupt and connect biological membranes. Biosci. Rep., 20, 2000, 501.
64. Tamm, L.K., Han, X., Li, Y., Lai, A.L., Structure and function of membrane fusion peptides. Biopolymers 66 (2002), 249–260.
65. Walls, A.C., Tortorici, M.A., Bosch, B.-J., Frenz, B., Rottier, P.J.M., DiMaio, F., Rey, F.A., Veesler, D., Cryo-electron microscopy structure of a coronavirus spike glycoprotein trimer. Nature 531 (2016), 114–117.
66. Walls, A.C., Tortorici, M.A., Frenz, B., Snijder, J., Li, W., Rey, F.A., DiMaio, F., Bosch, B.-J., Veesler, D., Glycan shield and epitope masking of a coronavirus spike protein observed by cryo-electron microscopy. Nat. Struct. Mol. Biol. 23 (2016), 899–905.
67. Wang, H., Yang, P., Liu, K., Guo, F., Zhang, Y., Zhang, G., Jiang, C., SARS coronavirus entry into host cells through a novel clathrin- and caveolae-independent endocytic pathway. Cell Res. 18 (2008), 290–301.
68. White, J.M., Delos, S.E., Brecher, M., Schornberg, K., Structures and mechanisms of viral membrane fusion proteins: multiple variations on a common theme. Crit. Rev. Biochem. Mol. Biol. 43 (2008), 189–219.
69. White, J.M., Whittaker, G.R., Fusion of enveloped viruses in endosomes. Traffic 17 (2016), 593–614.
70. Woo, P.C., Lau, S.K., Huang, Y., Yuen, K.Y., Coronavirus diversity, phylogeny and interspecies jumping. Exp. Biol. Med. 234 (2009), 1117–1127.
71. Yuan, Y., Cao, D., Zhang, Y., Ma, J., Qi, J., Wang, Q., Lu, G., Wu, Y., Yan, J., Shi, Y., Zhang, X., Gao, G.F., Cryo-EM structures of MERS-CoV and SARS-CoV spike glycoproteins reveal the dynamic receptor binding domains. Nat. Commun., 8, 2017, 15092.
72. Zhang, H., Wang, G., Li, J., Nie, Y., Shi, X., Lian, G., Wang, W., Yin, X., Zhao, Y., Qu, X., Ding, M., Deng, H., Identification of an antigenic determinant on the S2 domain of the severe acute respiratory syndrome coronavirus spike glycoprotein capable of inducing neutralizing antibodies. J. Virol. 78 (2004), 6938–6945.