Palmitoylation of the cysteine-rich endodomain of the SARS-coronavirus spike glycoprotein is important for spike-mediated cell fusion

Virology

Volumn 360, Issue 2, 2007, Pages 264-274

  Petit, Chad M ^a,b   Chouljenko, Vladimir N ^a,b   Iyer, Arun ^a,b   Colgrove, Robin ^c   Farzan, Michael ^d   Knipe, David M ^c   Kousoulas, K G ^a,b  

^a Division of Biotechnology and Molecular Medicine (BIOMMED)   (United States)

^b LOUISIANA STATE UNIVERSITY   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Coronavirus; Cysteine rich; Fusion; SARS; Spike

Indexed keywords

ALANINE; AMINO ACID; CYSTEINE; GLYCOPROTEIN; MUTANT PROTEIN; PALMITIC ACID DERIVATIVE; SPIKE GLYCOPROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL FUSION; CELL SURFACE; CYTOPLASM; MEMBRANE FUSION; MOLECULE; MUTAGENESIS; NONHUMAN; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN TRANSPORT; SARS CORONAVIRUS; STATISTICAL SIGNIFICANCE; TRANSIENT TRANSFECTION; WILD TYPE;

AMINO ACID SEQUENCE; ANIMALS; CELL FUSION; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; CYSTEINE; IMMUNOHISTOCHEMISTRY; ISOTOPE LABELING; MEMBRANE FUSION; MEMBRANE GLYCOPROTEINS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PALMITIC ACID; PROTEIN PROCESSING, POST-TRANSLATIONAL; SARS VIRUS; TRITIUM; VERO CELLS; VIRAL ENVELOPE PROTEINS;

CORONAVIRUS; SARS CORONAVIRUS;

EID: 33947601361     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2006.10.034     Document Type: Article

References (69)

1. Abraham S., Kienzle T.E., Lapps W., and Brian D.A. Deduced sequence of the bovine coronavirus spike protein and identification of the internal proteolytic cleavage site. Virology 176 1 (1990) 296-301
2. Aiyar A., Xiang Y., and Leis J. Site-directed mutagenesis using overlap extension PCR. Methods Mol. Biol. 57 (1996) 177-191
3. Anand K., Ziebuhr J., Wadhwani P., Mesters J.R., and Hilgenfeld R. Coronavirus main proteinase (3CLpro) structure: basis for design of anti-SARS drugs. Science 300 5626 (2003) 1763-1767
4. Bagai S., and Lamb R.A. Truncation of the COOH-terminal region of the paramyxovirus SV5 fusion protein leads to hemifusion but not complete fusion. J. Cell Biol. 135 1 (1996) 73-84
5. Baker K.A., Dutch R.E., Lamb R.A., and Jardetzky T.S. Structural basis for paramyxovirus-mediated membrane fusion. Mol. Cell 3 3 (1999) 309-319
6. Binns M.M., Boursnell M.E., Cavanagh D., Pappin D.J., and Brown T.D. Cloning and sequencing of the gene encoding the spike protein of the coronavirus IBV. J. Gen. Virol. 66 Pt 4 (1985) 719-726
7. Bos E.C., Heijnen L., Luytjes W., and Spaan W.J. Mutational analysis of the murine coronavirus spike protein: effect on cell-to-cell fusion. Virology 214 2 (1995) 453-463
8. Bos E.C., Luytjes W., and Spaan W.J. The function of the spike protein of mouse hepatitis virus strain A59 can be studied on virus-like particles: cleavage is not required for infectivity. J. Virol. 71 12 (1997) 9427-9433
9. Bosch B.J., van der Zee R., de Haan C.A., and Rottier P.J. The coronavirus spike protein is a class I virus fusion protein: structural and functional characterization of the fusion core complex. J. Virol. 77 16 (2003) 8801-8811
10. Broer R., Boson B., Spaan W., Cosset F.L., and Corver J. Important role for the transmembrane domain of severe acute respiratory syndrome coronavirus spike protein during entry. J. Virol. 80 3 (2006) 1302-1310
11. Cavanagh D. The Coronavirus Surface Glycoprotein (1995), Plenum Press Inc., New York, NY
12. Chang K.W., Sheng Y., and Gombold J.L. Coronavirus-induced membrane fusion requires the cysteine-rich domain in the spike protein. Virology 269 1 (2000) 212-224
13. de Groot R.J., Luytjes W., Horzinek M.C., van der Zeijst B.A., Spaan W.J., and Lenstra J.A. Evidence for a coiled-coil structure in the spike proteins of coronaviruses. J. Mol. Biol. 196 4 (1987) 963-966
14. Delmas B., Gelfi J., L'Haridon R., Vogel L.K., Sjostrom H., Noren O., and Laude H. Aminopeptidase N is a major receptor for the entero-pathogenic coronavirus TGEV. Nature 357 6377 (1992) 417-420
15. Drosten C., Gunther S., Preiser W., van der Werf S., Brodt H.R., Becker S., Rabenau H., Panning M., Kolesnikova L., Fouchier R.A., Berger A., Burguiere A.M., Cinatl J., Eickmann M., Escriou N., Grywna K., Kramme S., Manuguerra J.C., Muller S., Rickerts V., Sturmer M., Vieth S., Klenk H.D., Osterhaus A.D., Schmitz H., and Doerr H.W. Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N Engl. J. Med. 348 20 (2003) 1967-1976
16. Eckert D.M., and Kim P.S. Mechanisms of viral membrane fusion and its inhibition. Annu. Rev. Biochem. 70 (2001) 777-810
17. Gabuzda D.H., Lever A., Terwilliger E., and Sodroski J. Effects of deletions in the cytoplasmic domain on biological functions of human immunodeficiency virus type 1 envelope glycoproteins. J. Virol. 66 6 (1992) 3306-3315
18. Glick B.S., and Rothman J.E. Possible role for fatty acyl-coenzyme A in intracellular protein transport. Nature 326 6110 (1987) 309-312
19. Godeke G.J., de Haan C.A., Rossen J.W., Vennema H., and Rottier P.J. Assembly of spikes into coronavirus particles is mediated by the carboxy-terminal domain of the spike protein. J. Virol. 74 3 (2000) 1566-1571
20. Gombold J.L., Hingley S.T., and Weiss S.R. Fusion-defective mutants of mouse hepatitis virus A59 contain a mutation in the spike protein cleavage signal. J. Virol. 67 8 (1993) 4504-4512
21. Hirokawa T., Boon-Chieng S., and Mitaku S. SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics 14 4 (1998) 378-379
22. Holmes K.V. SARS-associated coronavirus. N Engl. J. Med. 348 20 (2003) 1948-1951
23. Ingallinella P., Bianchi E., Finotto M., Cantoni G., Eckert D.M., Supekar V.M., Bruckmann C., Carfi A., and Pessi A. Structural characterization of the fusion-active complex of severe acute respiratory syndrome (SARS) coronavirus. Proc. Natl. Acad. Sci. U. S. A. 101 23 (2004) 8709-8714
24. Jin H., Subbarao K., Bagai S., Leser G.P., Murphy B.R., and Lamb R.A. Palmitylation of the influenza virus hemagglutinin (H3) is not essential for virus assembly or infectivity. J. Virol. 70 3 (1996) 1406-1414
25. Kielian M. Class II virus membrane fusion proteins. Virology 344 1 (2006) 38-47
26. Krokhin O., Li Y., Andonov A., Feldmann H., Flick R., Jones S., Stroeher U., Bastien N., Dasuri K.V., Cheng K., Simonsen J.N., Perreault H., Wilkins J., Ens W., Plummer F., and Standing K.G. Mass spectrometric characterization of proteins from the SARS virus: a preliminary report. Mol. Cell. Proteomics 2 5 (2003) 346-356
27. Ksiazek T.G., Erdman D., Goldsmith C.S., Zaki S.R., Peret T., Emery S., Tong S., Urbani C., Comer J.A., Lim W., Rollin P.E., Dowell S.F., Ling A.E., Humphrey C.D., Shieh W.J., Guarner J., Paddock C.D., Rota P., Fields B., DeRisi J., Yang J.Y., Cox N., Hughes J.M., LeDuc J.W., Bellini W.J., and Anderson L.J. A novel coronavirus associated with severe acute respiratory syndrome. N Engl. J. Med. 348 20 (2003) 1953-1966
28. Kunkel F., and Herrler G. Structural and functional analysis of the surface protein of human coronavirus OC43. Virology 195 1 (1993) 195-202
29. Lescar J., Roussel A., Wien M.W., Navaza J., Fuller S.D., Wengler G., and Rey F.A. The Fusion glycoprotein shell of Semliki Forest virus: an icosahedral assembly primed for fusogenic activation at endosomal pH. Cell 105 1 (2001) 137-148
30. 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., and Farzan M. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 426 6965 (2003) 450-454
31. Lontok E., Corse E., and Machamer C.E. Intracellular targeting signals contribute to localization of coronavirus spike proteins near the virus assembly site. J. Virol. 78 11 (2004) 5913-5922
32. Luytjes W., Sturman L.S., Bredenbeek P.J., Charite J., van der Zeijst B.A., Horzinek M.C., and Spaan W.J. Primary structure of the glycoprotein E2 of coronavirus MHV-A59 and identification of the trypsin cleavage site. Virology 161 2 (1987) 479-487
33. Marra M.A., Jones S.J., Astell C.R., Holt R.A., Brooks-Wilson A., Butterfield Y.S., Khattra J., Asano J.K., Barber S.A., Chan S.Y., Cloutier A., Coughlin S.M., Freeman D., Girn N., Griffith O.L., Leach S.R., Mayo M., McDonald H., Montgomery S.B., Pandoh P.K., Petrescu A.S., Robertson A.G., Schein J.E., Siddiqui A., Smailus D.E., Stott J.M., Yang G.S., Plummer F., Andonov A., Artsob H., Bastien N., Bernard K., Booth T.F., Bowness D., Czub M., Drebot M., Fernando L., Flick R., Garbutt M., Gray M., Grolla A., Jones S., Feldmann H., Meyers A., Kabani A., Li Y., Normand S., Stroher U., Tipples G.A., Tyler S., Vogrig R., Ward D., Watson B., Brunham R.C., Krajden M., Petric M., Skowronski D.M., Upton C., and Roper R.L. The Genome sequence of the SARS-associated coronavirus. Science 300 5624 (2003) 1399-1404
34. Melikyan G.B., Markosyan R.M., Hemmati H., Delmedico M.K., Lambert D.M., and Cohen F.S. Evidence that the transition of HIV-1 gp41 into a six-helix bundle, not the bundle configuration, induces membrane fusion. J. Cell Biol. 151 2 (2000) 413-423
35. Mounir S., and Talbot P.J. Molecular characterization of the S protein gene of human coronavirus OC43. J. Gen. Virol. 74 Pt 9 (1993) 1981-1987
36. Naim H.Y., Amarneh B., Ktistakis N.T., and Roth M.G. Effects of altering palmitylation sites on biosynthesis and function of the influenza virus hemagglutinin. J. Virol. 66 12 (1992) 7585-7588
37. 1, a new type of viral glycoprotein. J. Mol. Biol. 153 4 (1981) 993-1010
38. Parker S.E., Gallagher T.M., and Buchmeier M.J. Sequence analysis reveals extensive polymorphism and evidence of deletions within the E2 glycoprotein gene of several strains of murine hepatitis virus. Virology 173 2 (1989) 664-673
39. Peiris J.S., Lai S.T., Poon L.L., Guan Y., Yam L.Y., Lim W., Nicholls J., Yee W.K., Yan W.W., Cheung M.T., Cheng V.C., Chan K.H., Tsang D.N., Yung R.W., Ng T.K., and Yuen K.Y. Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet 361 9366 (2003) 1319-1325
40. Petit C.M., Melancon J.M., Chouljenko V.N., Colgrove R., Farzan M., Knipe D.M., and Kousoulas K.G. Genetic analysis of the SARS-coronavirus spike glycoprotein functional domains involved in cell-surface expression and cell-to-cell fusion. Virology (2005) 215-230
41. Ponimaskin E., and Schmidt M.F. Acylation of viral glycoproteins: structural requirements for palmitoylation of transmembrane proteins. Biochem. Soc. Trans. 23 3 (1995) 565-568
42. Raabe T., Schelle-Prinz B., and Siddell S.G. Nucleotide sequence of the gene encoding the spike glycoprotein of human coronavirus HCV 229E. J. Gen. Virol. 71 Pt 5 (1990) 1065-1073
43. Rasschaert D., and Laude H. The predicted primary structure of the peplomer protein E2 of the porcine coronavirus transmissable gastroenteritis virus. J. Gen. Virol. 68 Pt 7 (1987) 1883-1890
44. Rose J.K., Adams G.A., and Gallione C.J. The presence of cysteine in the cytoplasmic domain of the vesicular stomatitis virus glycoprotein is required for palmitate addition. Proc. Natl. Acad. Sci. U. S. A. 81 7 (1984) 2050-2054
45. Rota P.A., Oberste M.S., Monroe S.S., Nix W.A., Campagnoli R., Icenogle J.P., Penaranda S., Bankamp B., Maher K., Chen M.H., Tong S., Tamin A., Lowe L., Frace M., DeRisi J.L., Chen Q., Wang D., Erdman D.D., Peret T.C., Burns C., Ksiazek T.G., Rollin P.E., Sanchez A., Liffick S., Holloway B., Limor J., McCaustland K., Olsen-Rasmussen M., Fouchier R., Gunther S., Osterhaus A.D., Drosten C., Pallansch M.A., Anderson L.J., and Bellini W.J. Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science 300 5624 (2003) 1394-1399
46. Russell C.J., Jardetzky T.S., and Lamb R.A. Membrane fusion machines of paramyxoviruses: capture of intermediates of fusion. EMBO J. 20 15 (2001) 4024-4034
47. Sainz Jr. B., Rausch J.M., Gallaher W.R., Garry R.F., and Wimley W.C. Identification and characterization of the putative fusion peptide of the severe acute respiratory syndrome-associated coronavirus spike protein. J. Virol. 79 11 (2005) 7195-7206
48. Schlesinger M.J., Veit M., and Schmidt M.F. Palmitoylation of cellular and viral proteins. In: Schlesinger M.J. (Ed). Lipid Modification of Proteins (1993), CRC Press, Boca Raton, FL 1-19
49. Schmidt M.F. Fatty acylation of proteins. Biochim. Biophys. Acta 988 3 (1989) 411-426
50. Schroth-Diez B., Ponimaskin E., Reverey H., Schmidt M.F., and Herrmann A. Fusion activity of transmembrane and cytoplasmic domain chimeras of the influenza virus glycoprotein hemagglutinin. J. Virol. 72 1 (1998) 133-141
51. Schwegmann-Wessels C., Al-Falah M., Escors D., Wang Z., Zimmer G., Deng H., Enjuanes L., Naim H.Y., and Herrler G. A novel sorting signal for intracellular localization is present in the S protein of a porcine coronavirus but absent from severe acute respiratory syndrome-associated coronavirus. J. Biol. Chem. 279 42 (2004) 43661-43666
52. Sefton B.M., and Buss J.E. The covalent modification of eukaryotic proteins with lipid. J. Cell Biol. 104 6 (1987) 1449-1453
53. Sergel T., and Morrison T.G. Mutations in the cytoplasmic domain of the fusion glycoprotein of Newcastle disease virus depress syncytia formation. Virology 210 2 (1995) 264-272
54. Seth S., Vincent A., and Compans R.W. Mutations in the cytoplasmic domain of a paramyxovirus fusion glycoprotein rescue syncytium formation and eliminate the hemagglutinin-neuraminidase protein requirement for membrane fusion. J. Virol. 77 1 (2003) 167-178
55. Skehel J.J., and Wiley D.C. Coiled coils in both intracellular vesicle and viral membrane fusion. Cell 95 7 (1998) 871-874
56. Snijder E.J., Bredenbeek P.J., Dobbe J.C., Thiel V., Ziebuhr J., Poon L.L., Guan Y., Rozanov M., Spaan W.J., and Gorbalenya A.E. Unique and conserved features of genome and proteome of SARS-coronavirus, an early split-off from the coronavirus group 2 lineage. J. Mol. Biol. 331 5 (2003) 991-1004
57. Song H.C., Seo M.Y., Stadler K., Yoo B.J., Choo Q.L., Coates S.R., Uematsu Y., Harada T., Greer C.E., Polo J.M., Pileri P., Eickmann M., Rappuoli R., Abrignani S., Houghton M., and Han J.H. Synthesis and characterization of a native, oligomeric form of recombinant severe acute respiratory syndrome coronavirus spike glycoprotein. J. Virol. 78 19 (2004) 10328-10335
58. Stauber R., Pfleiderera M., and Siddell S. Proteolytic cleavage of the murine coronavirus surface glycoprotein is not required for fusion activity. J. Gen. Virol. 74 Pt 2 (1993) 183-191
59. Sturman L.S., Holmes K.V., and Behnke J. Isolation of coronavirus envelope glycoproteins and interaction with the viral nucleocapsid. J. Virol. 33 1 (1980) 449-462
60. Tong S., Li M., Vincent A., Compans R.W., Fritsch E., Beier R., Klenk C., Ohuchi M., and Klenk H.D. Regulation of fusion activity by the cytoplasmic domain of a paramyxovirus F protein. Virology 301 2 (2002) 322-333
61. Tsai J.C., Zelus B.D., Holmes K.V., and Weiss S.R. The N-terminal domain of the murine coronavirus spike glycoprotein determines the CEACAM1 receptor specificity of the virus strain. J. Virol. 77 2 (2003) 841-850
62. van Berlo M.F., van den Brink W.J., Horzinek M.C., and van der Zeijst B.A. Fatty acid acylation of viral proteins in murine hepatitis virus-infected cells. Brief report. Arch. Virol. 95 1-2 (1987) 123-128
63. Waning D.L., Russell C.J., Jardetzky T.S., and Lamb R.A. Activation of a paramyxovirus fusion protein is modulated by inside-out signaling from the cytoplasmic tail. Proc. Natl. Acad. Sci. U. S. A. 101 25 (2004) 9217-9222
64. Wu X.D., Shang B., Yang R.F., Yu H., Ma Z.H., Shen X., Ji Y.Y., Lin Y., Wu Y.D., Lin G.M., Tian L., Gan X.Q., Yang S., Jiang W.H., Dai E.H., Wang X.Y., Jiang H.L., Xie Y.H., Zhu X.L., Pei G., Li L., Wu J.R., and Sun B. The spike protein of severe acute respiratory syndrome (SARS) is cleaved in virus infected Vero-E6 cells. Cell Res. 14 5 (2004) 400-406
65. Yao Q., and Compans R.W. Differences in the role of the cytoplasmic domain of human parainfluenza virus fusion proteins. J. Virol. 69 11 (1995) 7045-7053
66. Ye R., Montalto-Morrison C., and Masters P.S. Genetic analysis of determinants for spike glycoprotein assembly into murine coronavirus virions: distinct roles for charge-rich and cysteine-rich regions of the endodomain. J. Virol. 78 18 (2004) 9904-9917
67. Ying W., Hao Y., Zhang Y., Peng W., Qin E., Cai Y., Wei K., Wang J., Chang G., Sun W., Dai S., Li X., Zhu Y., Li J., Wu S., Guo L., Dai J., Wan P., Chen T., Du C., Li D., Wan J., Kuai X., Li W., Shi R., Wei H., Cao C., Yu M., Liu H., Dong F., Wang D., Zhang X., Qian X., Zhu Q., and He F. Proteomic analysis on structural proteins of severe acute respiratory syndrome coronavirus. Proteomics 4 2 (2004) 492-504
68. Zelus B.D., Schickli J.H., Blau D.M., Weiss S.R., and Holmes K.V. Conformational changes in the spike glycoprotein of murine coronavirus are induced at 37 degrees C either by soluble murine CEACAM1 receptors or by pH 8. J. Virol. 77 2 (2003) 830-840
69. Zurcher T., Luo G., and Palese P. Mutations at palmitoylation sites of the influenza virus hemagglutinin affect virus formation. J. Virol. 68 9 (1994) 5748-5754