The transmembrane domain of the severe acute respiratory syndrome coronavirus ORF7b protein is necessary and sufficient for its retention in the Golgi complex

Journal of Virology

Volumn 82, Issue 19, 2008, Pages 9477-9491

  Schaecher, Scott R ^a   Diamond, Michael S ^a   Pekosz, Andrew ^b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; MUTANT PROTEIN; SEVERE ACUTE RESPIRATORY SYNDROME CORONAVIRUS OPEN READING FRAME 7B PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; GOLGI COMPLEX; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; SARS CORONAVIRUS;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD4; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GOLGI APPARATUS; HUMANS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; SARS VIRUS; SEQUENCE HOMOLOGY, AMINO ACID; VERO CELLS; VIRAL PROTEINS;

SARS CORONAVIRUS;

EID: 52649182178     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00784-08     Document Type: Article

References (86)

1. Afzelius, B. A. 1994. Ultrastructure of human nasal epithelium during an episode of coronavirus infection. Virchows Arch. 424:295-300.
2. Andersson, A. M., L. Melin, A. Bean, and R. F. Pettersson. 1997. A retention signal necessary and sufficient for Golgi localization maps to the cytoplasmic tail of a Bunyaviridae (Uukuniemi virus) membrane glycoprotein. J. Virol. 71:4717-4727.
3. Bosshart, H., J. Humphrey, E. Deignan, J. Davidson, J. Drazba, L. Yuan, V. Oorschot, P. J. Peters, and J. S. Bonifacino. 1994. The cytoplasmic domain mediates localization of furin to the trans-Golgi network en route to the endosomal/lysosomal system. J. Cell Biol. 126:1157-1172.
4. Bretscher, M. S., and S. Munro. 1993. Cholesterol and the Golgi apparatus. Science 261:1280-1281.
5. Colley, K. J. 1997. Golgi localization of glycosyltransferases: more questions than answers. Glycobiology 7:1-13.
6. Corse, E., and C. E. Machamer. 2002. The cytoplasmic tail of infectious bronchitis virus E protein directs Golgi targeting. J. Virol. 76:1273-1284.
7. Dea, S., S. Garzon, H. Strykowski, and P. Tijssen. 1989. Ultrastructure and protein A-gold immunolabelling of HRT-18 cells infected with turkey enteric coronavirus. Vet. Microbiol. 20:21-33.
8. de Haan, C. A., and P. J. Rottier. 2005. Molecular interactions in the assembly of coronaviruses. Adv. Virus Res. 64:165-230.
9. Garoff, H., R. Hewson, and D. J. Opstelten. 1998. Virus maturation by budding. Microbiol. Mol. Biol. Rev. 62:1171-1190.
10. Geng, H., Y.-M. Liu, W.-S. Chan, A. W.-I. Lo, D. M.-Y. Au, M. M.-Y. Waye, and Y.-Y. Ho. 2005. The putative protein 6 of the severe acute respiratory syndrome-associated coronavirus: expression and functional characterization. FEBS Lett. 579:6763-6768.
11. Gerrard, S. R., and S. T. Nichol. 2002. Characterization of the Golgi retention motif of Rift Valley fever virus G(N) glycoprotein. J. Virol. 76:12200-12210.
12. Griffiths, G., and P. Rottier. 1992. Cell biology of viruses that assemble along the biosynthetic pathway. Semin. Cell Biol. 3:367-381.
13. Huang, C., N. Ito, C. T. Tseng, and S. Makino. 2006. Severe acute respiratory syndrome coronavirus 7a accessory protein is a viral structural protein. J. Virol. 80:7287-7294.
14. Huang, C., C. J. Peters, and S. Makino. 2007. Severe acute respiratory syndrome coronavirus accessory protein 6 is a virion-associated protein and is released from 6 protein-expressing cells. J. Virol. 81:5423-5426.
15. Ito, N., E. C. Mossel, K. Narayanan, V. L. Popov, C. Huang, T. Inoue, C. J. Peters, and S. Makino. 2005. Severe acute respiratory syndrome coronavirus 3a protein is a viral structural protein. J. Virol. 79:3182-3186.
16. Jackson, M. R., T. Nilsson, and P. A. Peterson. 1990. Identification of a consensus motif for retention of transmembrane proteins in the endoplasmic reticulum. EMBO J. 9:3153-3162.
17. Klumperman, J., J. K. Locker, A. Meijer, M. C. Horzinek, H. J. Geuze, and P. J. Rottier. 1994. Coronavirus M proteins accumulate in the Golgi complex beyond the site of virion budding. J. Virol. 68:6523-6534.
18. Kopecky-Bromberg, S. A., L. Martinez-Sobrido, and P. Palese. 2006. 7a protein of severe acute respiratory syndrome coronavirus inhibits cellular protein synthesis and activates p38 mitogen-activated protein kinase. J. Virol. 80:785-793.
19. Krijnse-Locker, J., M. Ericsson, P. J. Rottier, and G. Griffiths. 1994. Characterization of the budding compartment of mouse hepatitis virus: evidence that transport from the RER to the Golgi complex requires only one vesicular transport step. J. Cell Biol. 124:55-70.
20. Kuismanen, E., K. Hedman, J. Saraste, and R. F. Pettersson. 1982. Uukuniemi virus maturation: accumulation of virus particles and viral antigens in the Golgi complex. Mol. Cell. Biol. 2:1444-1458.
21. Landolt-Marticorena, C., K. A. Williams, C. M. Deber, and R. A. Reithmeier. 1993. Non-random distribution of amino acids in the transmembrane segments of human type I single span membrane proteins. J. Mol. Biol. 229:602-608.
22. Liao, Y., Q. Yuan, J. Torres, J. P. Tam, and D. X. Liu. 2006. Biochemical and functional characterization of the membrane association and membrane permeabilizing activity of the severe acute respiratory syndrome coronavirus envelope protein. Virology 349:264-275.
23. Lim, K. P., and D. X. Liu. 2001. The missing link in coronavirus assembly. Retention of the avian coronavirus infectious bronchitis virus envelope protein in the pre-Golgi compartments and physical interaction between the envelope and membrane proteins. J. Biol. Chem. 276:17515-17523.
24. Locker, J. K., G. Griffiths, M. C. Horzinek, and P. J. Rottier. 1992. O-glycosylation of the coronavirus M protein. Differential localization of sialyltransferases in N- and O-linked glycosylation. J. Biol. Chem. 267:14094-14101.
25. Locker, J. K., J. Klumperman, V. Oorschot, M. C. Horzinek, H. J. Geuze, and P. J. Rottier. 1994. The cytoplasmic tail of mouse hepatitis virus M protein is essential but not sufficient for its retention in the Golgi complex. J. Biol. Chem. 269:28263-28269.
26. Lontok, E., E. Corse, and C. E. Machamer. 2004. Intracellular targeting signals contribute to localization of coronavirus spike proteins near the virus assembly site. J. Virol. 78:5913-5922.
27. Lundbaek, J. A., O. S. Andersen, T. Werge, and C. Nielsen. 2003. Cholesterol-induced protein sorting: an analysis of energetic feasibility. Biophys. J. 84:2080-2089.
28. Ma, J., and K. J. Colley. 1996. A disulfide-bonded dimer of the Golgi beta-galactoside alpha2,6-sialyltransferase is catalytically inactive yet still retains the ability to bind galactose. J. Biol. Chem. 271:7758- 7766.
29. Machamer, C. E., M. G. Grim, A. Esquela, S. W. Chung, M. Rolls, K. Ryan, and A. M. Swift. 1993. Retention of a eis Golgi protein requires polar residues on one face of a predicted alpha-helix in the transmembrane domain. Mol. Biol. Cell 4:695-704.
30. Machamer, C. E., S. A. Mentone, J. K. Rose, and M. G. Farquhar. 1990. The E1 glycoprotein of an avian coronavirus is targeted to the cis Golgi complex. Proc. Natl. Acad. Sci. USA 87:6944-6948.
31. Machamer, C. E., and J. K. Rose. 1987. A specific transmembrane domain of a coronavirus E1 glycoprotein is required for its retention in the Golgi region. J. Cell Biol. 105:1205-1214.
32. Mackenzie, J. M., and E. G. Westaway. 2001. Assembly and maturation of the flavivirus Kunjin virus appear to occur in the rough endoplasmic reticulum and along the secretory pathway, respectively. J. Virol. 75:10787-10799.
33. Marra, M. A., S. J. M. Jones, C. R. Astell, R. A. Holt, A. Brooks-Wilson, Y. S. N. Butterfield, J. Khattra, J. K. Asano, S. A. Barber, S. Y. Chan, A. Cloutier, S. M. Coughlin, D. Freeman, N. Girn, O. L. Griffith, S. R. Leach, M. Mayo, H. McDonald, S. B. Montgomery, P. K. Pandoh, A. S. Petrescu, A. G. Robertson, J. E. Schein, A. Siddiqui, D. E. Smailus, J. M. Stott, G. S. Yang, F. Plummer, A. Andonov, H. Artsob, N. Bastien, K. Bernard, T. F. Booth, D. Bowness, M. Czub, M. Drebot, L. Fernando, R. Flick, M. Garbutt, M. Gray, A. Grolla, S. Jones, H. Feldmann, A. Meyers, A. Kabani, Y. Li, S. Normand, U. Stroher, G. A. Tipples, S. Tyler, R. Vogrig, D. Ward, B. Watson, R. C. Brunham, M. Krajden, M. Petric, D. M. Skowronski, C. Upton, and R. L. Roper. 2003. The genome sequence of the SARS-associated coronavirus. Science 300:1399-1404.
34. Masters, P. S. 2006. The molecular biology of coronaviruses. Adv. Virus Res. 66:193-292.
35. Matsuoka, Y., S. Y. Chen, and R. W. Compans. 1991. Bunyavirus protein transport and assembly. Curr. Top. Microbiol. Immunol. 169:161-179.
36. Matsuoka, Y., S. Y. Chen, and R. W. Compans. 1994. A signal for Golgi retention in the bunyavirus G1 glycoprotein. J. Biol. Chem. 269:22565-22573.
37. McBride, C. E., J. Li, and C. E. Machamer. 2007. The cytoplasmic tail of the severe acute respiratory syndrome coronavirus spike protein contains a novel endoplasmic reticulum retrieval signal that binds COPI and promotes interaction with membrane protein. J. Virol. 81:2418-2428.
38. Mhamdi, M., A. Funk, H. Hohenberg, H. Will, and H. Sirma. 2007. Assembly and budding of a hepatitis B virus is mediated by a novel type of intracellular vesicles. Hepatology 46:95-106.
39. Mihindukulasuriya, K. A., G. Wu, J. St. Leger, R. W. Nordhausen, and D. Wang. 2008. Identification of a novel coronavirus from a beluga whale using a panviral microarray. J. Virol. 82:5084-5088.
40. Mukhopadhyay, S., R. J. Kuhn, and M. G. Rossmann. 2005. A structural perspective of the flavivirus life cycle. Nat. Rev. Microbiol. 3:13-22.
41. Munro, S. 1995. An investigation of the role of transmembrane domains in Golgi protein retention. EMBO J. 14:4695-4704.
42. Munro, S. 1998. Localization of proteins to the Golgi apparatus. Trends Cell Biol. 8:11-15.
43. Munro, S. 1991. Sequences within and adjacent to the transmembrane segment of alpha-2,6-sialyltransferase specify Golgi retention. EMBO J. 10:3577-3588.
44. Nal, B., C. Chan, F. Kien, L. Siu, J. Tse, K. Chu, J. Kam, I. Staropoli, B. Crescenzo-Chaigne, N. Escriou, S. van der Werf, K.-Y. Yuen, and R. Altmeyer. 2005. Differential maturation and subcellular localization of severe acute respiratory syndrome coronavirus surface proteins S, M and E. J. Gen. Virol. 86:1423-1434.
45. Nelson, C. A., A. Pekosz, C. A. Lee, M. S. Diamond, and D. H. Fremont. 2005. Structure and intracellular targeting of the SARS-coronavirus Orf7a accessory protein. Structure (Cambridge) 13:75-85.
46. Nilsson, T., M. H. Hoe, P. Slusarewicz, C. Rabouille, R. Watson, F. Hunte, G. Watzele, E. G. Berger, and G. Warren. 1994. Kin recognition between medial Golgi enzymes in HeLa cells. EMBO J. 13:562-574.
47. Nilsson, T., P. Slusarewicz, M. H. Hoe, and G. Warren. 1993. Kin recognition. A model for the retention of Golgi enzymes. FEBS Lett. 330:1-4.
48. Niwa, H., K. Yamamura, and J. Miyazaki. 1991. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108:193- 199.
49. Padhan, K., C. Tanwar, A. Hussain, P. Y. Hui, M. Y. Lee, C. Y. Cheung, J. S. Peiris, and S. Jameel. 2007. Severe acute respiratory syndrome coronavirus Orf3a protein interacts with caveolin. J. Gen. Virol. 88:3067-3077.
50. Paterson, R. G., and R. A. Lamb. 1993. The molecular biology of influenza viruses and paramyxoviruses, p. 35-73. In A. J. Davison and R. M. Elliott (ed.), Molecular virology: a practical approach. Oxford University Press, Oxford, United Kingdom.
51. Pewe, L., H. Zhou, J. Netland, C. Tangudu, H. Olivares, L. Shi, D. Look, T. Gallagher, and S. Perlman. 2005. A severe acute respiratory syndrome-associated coronavirus-specific protein enhances virulence of an attenuated murine coronavirus. J. Virol 79:11335-11342.
52. Qinfen, Z., C. Jinming, H. Xiaojun, Z. Huanying, H. Jicheng, F. Ling, L. Kunpeng, and Z. Jingqiang. 2004. The life cycle of SARS coronavirus in Vero E6 cells. J. Med. Virol. 73:332-337.
53. Raamsman, M. J., J. K. Locker, A. de Hooge, A. A. de Vries, G. Griffiths, H. Vennema, and P. J. Rottier. 2000. Characterization of the coronavirus mouse hepatitis virus strain A59 small membrane protein E. J. Virol. 74:2333-2342.
54. Risco, C., M. Muntion, L. Enjuanes, and J. L. Carrascosa. 1998. Two types of virus-related particles are found during transmissible gastroenteritis virus morphogenesis. J. Virol. 72:4022-4031.
55. Rodgers, W. 2002. Making membranes green: construction and characterization of GFP-fusion proteins targeted to discrete plasma membrane domains. BioTechniqaes 32:1044-1046, 1048, 1050-1051.
56. Roingeard, P., and C. Hourioux. 2008. Hepatitis C virus core protein, lipid droplets and steatosis. J. Viral Hepat. 15:157-164.
57. Rota, P. A., M. S. Oberste, S. S. Monroe, W. A. Nix, R. Campagnoli, J. P. Icenogle, S. Penaranda, B. Bankamp, K. Maher, M.-H. Chen, S. Tong, A. Tamin, L. Lowe, M. Frace, J. L. DeRisi, Q. Chen, D. Wang, D. D. Erdman, T. C. T. Peret, C. Burns, T. G. Ksiazek, P. E. Rollin, A. Sanchez, S. Liffick, B. Holloway, J. Limor, K. McCaustland, M. Olsen-Rasmussen, R. Fouchier, S. Gunther, A. D. M. E. Osterhaus, C. Drosten, M. A. Pallansch, L. J. Anderson, and W. J. Bellini. 2003. Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science 300:1394-1399.
58. Rottier, P. J., and J. K. Rose. 1987. Coronavirus E1 glycoprotein expressed from cloned cDNA localizes in the Golgi region. J. Virol. 61:2042-2045.
59. Ruan, W., V. Becker, U. Klingmuller, and D. Langosch. 2004. The interface between self-assembling erythropoietin receptor transmembrane segments corresponds to a membrane-spanning leucine zipper. J. Biol. Chem. 279: 3273-3279.
60. Salanueva, I. J., J. L. Carrascosa, and C. Risco. 1999. Structural maturation of the transmissible gastroenteritis coronavirus. J. Virol. 73:7952-7964.
61. Schaecher, S. R., J. M. Mackenzie, and A. Pekosz. 2007. The ORF7b protein of severe acute respiratory syndrome coronavirus (SARS-CoV) is expressed in virus-infected cells and incorporated into SARS-CoV particles. J. Virol. 81:718-731.
62. Schaecher, S. R., E. Touchette, J. Schriewer, R. M. Buller, and A. Pekosz. 2007. Severe acute respiratory syndrome coronavirus gene 7 products contribute to virus-induced apoptosis. J. Virol. 81:11054-11068.
63. Schmaljohn, C., and J. Hooper. 2001. Bunyaviridae: the viruses and their replication, p. 1581-1602. In P. M. H. D. M. Knipe, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, and S. E. Straus (ed.), Fields virology, 4th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
64. Schweizer, A., J. Rohrer, H. P. Hauri, and S. Kornfeld. 1994. Retention of p63 in an ER-Golgi intermediate compartment depends on the presence of all three of its domains and on its ability to form oligomers. J. Cell Biol. 126:25-39.
65. Shen, S., P. S. Lin, Y. C. Chao, A. Zhang, X. Yang, S. G. Lim, W. Hong, and Y. J. Tan. 2005. The severe acute respiratory syndrome coronavirus 3a is a novel structural protein. Biochem. Biophys. Res. Commun. 330:286-292.
66. Shi, X., D. F. Lappin, and R. M. Elliott. 2004. Mapping the Golgi targeting and retention signal of Bunyamwera virus glycoproteins. J. Virol. 78:10793-10802.
67. Shin, J., R. L. Dunbrack, Jr., S. Lee, and J. L. Strominger. 1991. Signals for retention of transmembrane proteins in the endoplasmic reticulum studied with CD4 truncation mutants. Proc. Natl. Acad. Sci. USA 88:1918-1922.
68. Sims, A. C., R. S. Baric, B. Yount, S. E. Burkett, P. L. Collins, and R. J. Pickles. 2005. Severe acute respiratory syndrome coronavirus infection of human ciliated airway epithelia: role of ciliated cells in viral spread in the conducting airways of the lungs. J. Virol. 79:15511-15524.
69. Stertz, S., M. Reichelt, M. Spiegel, T. Kuri, L. Martinez-Sobrido, A. Garcia-Sastre, F. Weber, and G. Kochs. 2007. The intracellular sites of early replication and budding of SARS-coronavirus. Virology 361:304-315.
70. Swift, A. M., and C. E. Machamer. 1991. A Golgi retention signal in a membrane-spanning domain of coronavirus E1 protein. J. Cell Biol. 115:19-30.
71. 2 ion channel activity is essential for efficient replication in tissue culture. J. Virol. 76:1391-1399.
72. Tan, Y.-J., E. Teng, S. Shen, T. H. P. Tan, P.-Y. Goh, B. C. Fielding, E.-E. Ooi, H.-C. Tan, S. G. Lim, and W. Hong. 2004. A novel severe acute respiratory syndrome coronavirus protein, U274, is transported to the cell surface and undergoes endocytosis. J. Virol. 78:6723-6734.
73. Teasdale, R. D., and M. R. Jackson. 1996. Signal-mediated sorting of membrane proteins between the endoplasmic reticulum and the Golgi apparatus. Annu. Rev. Cell Dev. Biol. 12:27-54.
74. Teasdale, R. D., F. Matheson, and P. A. Gleeson. 1994. Post-translational modifications distinguish cell surface from Golgi-retained beta 1,4 galactosyltransferase molecules. Golgi localization involves active retention. Glycobiology 4:917-928.
75. Thiel, V., K. A. Ivanov, A. Putics, T. Hertzig, B. Schelle, S. Bayer, B. Weissbrich, E. J. Snijder, H. Rabenau, H. W. Doerr, A. E. Gorbalenya, and J. Ziebuhr. 2003. Mechanisms and enzymes involved in SARS coronavirus genome expression. J. Gen. Virol. 84:2305-2315.
76. Tooze, J., S. Tooze, and G. Warren. 1984. Replication of coronavirus MHV-A59 in sac- cells: determination of the first site of budding of progeny virions. Eur. J. Cell Biol. 33:281-293.
77. Tooze, J., and S. A. Tooze. 1985. Infection of AtT20 murine pituitary tumour cells by mouse hepatitis virus strain A59: virus budding is restricted to the Golgi region. Eur. J. Cell Biol. 37:203-212.
78. Tooze, J., S. A. Tooze, and S. D. Fuller. 1987. Sorting of progeny coronavirus from condensed secretory proteins at the exit from the trans-Golgi network of AtT20 cells. J. Cell Biol. 105:1215-1226.
79. Voorhees, P., E. Deignan, E. van Donselaar, J. Humphrey, M. S. Marks, P. J. Peters, and J. S. Bonifacino. 1995. An acidic sequence within the cytoplasmic domain of furin functions as a determinant of trans-Golgi network localization and internalization from the cell surface. EMBO J. 14:4961-4975.
80. Watanabe, T., E. M. Sorensen, A. Naito, M. Schott, S. Kim, and P. Ahlquist. 2007. Involvement of host cellular multivesicular body functions in hepatitis B virus budding. Proc. Natl. Acad. Sci. USA 104:10205-10210.
81. Weisz, O. A., A. M. Swift, and C. E. Machamer. 1993. Oligomerization of a membrane protein correlates with its retention in the Golgi complex. J. Cell Biol. 122:1185-1196.
82. Yamaguchi, N., and M. N. Fukuda. 1995. Golgi retention mechanism of beta-1,4-galactosyltransferase. Membrane-spanning domain-dependent homodimerization and association with alpha- and beta-tubulins. J. Biol. Chem. 270:12170-12176.
83. Ye, Y., and B. G. Hogue. 2007. Role of the coronavirus E viroporin protein transmembrane domain in virus assembly. J. Virol. 81:3597-3607.
84. Yount, B., K. M. Curtis, E. A. Fritz, L. E. Hensley, P. B. Jahrling, E. Prentice, M. R. Denison, T. W. Geisbert, and R. S. Baric. 2003. Reverse genetics with a full-length infectious cDNA of severe acute respiratory syndrome coronavirus. Proc. Natl. Acad. Sci. USA 100:12995-13000.
85. Yount, B., R. S. Roberts, A. C. Sims, D. Deming, M. B. Frieman, J. Sparks, M. R. Denison, N. Davis, and R. S. Baric. 2005. Severe acute respiratory syndrome coronavirus group-specific open reading frames encode nonessential functions for replication in cell cultures and mice. J. Virol. 79:14909-14922.
86. Zhu, Z., Y. Hao, M. D. Gershon, R. T. Ambron, and A. A. Gershon. 1996. Targeting of glycoprotein I (gE) of varicella-zoster virus to the trans-Golgi network by an AYRV sequence and an acidic amino acid-rich patch in the cytosolic domain of the molecule. J. Virol. 70:6563-6575.