Severe acute respiratory syndrome coronavirus ORF7a inhibits bone marrow stromal antigen 2 virion tethering through a novel mechanism of glycosylation interference

Journal of Virology

Volumn 89, Issue 23, 2015, Pages 11820-11833

  Taylor, Justin K ^a   Coleman, Christopher M ^a   Postel, Sandra ^a   Sisk, Jeanne M ^a   Bernbaum, John G ^b   Venkataraman, Thiagarajan ^a   Sundberg, Eric J ^a   Frieman, Matthew B ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CONCANAMYCIN A; LYMPHOCYTE ANTIGEN; NONSTRUCTURAL PROTEIN 1; PAPAIN LIKE PROTEASE; PROTEIN BST 2; PROTEIN ORF6; PROTEIN ORF7A; UNCLASSIFIED DRUG; VIRUS PROTEIN; 3C-LIKE PROTEASE, SARS CORONAVIRUS; BST2 PROTEIN, HUMAN; CYSTEINE PROTEINASE; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; LEUKOCYTE ANTIGEN; NSP1 PROTEIN, SARS CORONAVIRUS; PRIMER DNA; RNA DIRECTED RNA POLYMERASE; VIRAL PROTEIN;

ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SARS CORONAVIRUS; VIRION; VIRUS GENOME; VIRUS INHIBITION; VIRUS RELEASE; VIRUS REPLICATION; AFFINITY CHROMATOGRAPHY; ANIMAL; CHLOROCEBUS AETHIOPS; CONFOCAL MICROSCOPY; ELECTRON MICROSCOPY; FLOW CYTOMETRY; GENETICS; GLYCOSYLATION; HEK293 CELL LINE; MOLECULAR CLONING; OPEN READING FRAME; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEVERE ACUTE RESPIRATORY SYNDROME; VERO CELL LINE; VIROLOGY; VIRUS ATTACHMENT;

ANIMALS; ANTIGENS, CD; CERCOPITHECUS AETHIOPS; CHROMATOGRAPHY, AFFINITY; CLONING, MOLECULAR; CYSTEINE ENDOPEPTIDASES; DNA PRIMERS; FLOW CYTOMETRY; GLYCOSYLATION; GPI-LINKED PROTEINS; HEK293 CELLS; HUMANS; IMMUNOPRECIPITATION; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; OPEN READING FRAMES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA REPLICASE; SARS VIRUS; SEVERE ACUTE RESPIRATORY SYNDROME; VERO CELLS; VIRAL NONSTRUCTURAL PROTEINS; VIRAL PROTEINS; VIRION; VIRUS ATTACHMENT;

EID: 84949652761     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02274-15     Document Type: Article

References (55)

1. World Health Organization. 2003. WHO summary of probable SARS cases with onset of illness from 1 November 2002 to 31 July 2003. World Health Organization, Geneva, Switzerland.
2. Drosten C, Preiser W, Günther S, Schmitz H, Doerr HW. 2003. Severe acute respiratory syndrome: identification of the etiological agent. Trends Mol Med 9:325-327. http://dx.doi.org/10.1016/S1471-4914(03)00133-3.
3. Marra MA, Jones SJM, Astell CR, Holt RA, Brooks-Wilson A, Butterfield YSN, Khattra J, Asano JK, Barber SA, Chan SY, Cloutier A, Coughlin SM, Freeman D, Girn N, Griffith OL, Leach SR, Mayo M, McDonald H, Montgomery SB, Pandoh PK, Petrescu AS, Robertson AG, Schein JE, Siddiqui A, Smailus DE, Stott JM, Yang GS, Plummer F, Andonov A, Artsob H, Bastien N, Bernard K, Booth TF, 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 GA, Tyler S, et al. 2003. The genome sequence of the SARS-associated coronavirus. Science 300:1399-1404. http://dx.doi.org/10.1126/science.1085953.
4. Li W, Moore MJ, Vasilieva N, Sui J, Wong SK, Berne MA, Somasundaran M, Sullivan JL, Luzuriaga K, Greenough TC, Choe H, Farzan M. 2003. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 426:450-454. http://dx.doi.org/10.1038/nature02145.
5. Rota PA, Oberste MS, Monroe SS, Nix WA, Campagnoli R, Icenogle JP, Peñaranda S, Bankamp B, Maher K, Chen M-H, Tong S, Tamin A, Lowe L, Frace M, DeRisi JL, Chen Q, Wang D, Erdman DD, Peret TCT, Burns C, Ksiazek TG, Rollin PE, Sanchez A, Liffick S, Holloway B, Limor J, McCaustland K, Olsen-Rasmussen M, Fouchier R, Günther S, Osterhaus ADME, Drosten C, Pallansch MA, Anderson LJ, Bellini WJ. 2003. Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science 300:1394-1399. http://dx.doi.org/10.1126/science.1085952.
6. Frieman M, Yount B, Heise M, Kopecky-Bromberg SA, Palese P, Baric RS. 2007. Severe acute respiratory syndrome coronavirus ORF6 antagonizes STAT1 function by sequestering nuclear import factors on the rough endoplasmic reticulum/Golgi membrane. J Virol 81:9812-9824. http://dx.doi.org/10.1128/JVI.01012-07.
7. Kopecky-Bromberg SA, Martínez-Sobrido L, Frieman M, Baric RA, Palese P. 2007. Severe acute respiratory syndrome coronavirus open reading frame (ORF) 3b, ORF 6, and nucleocapsid proteins function as interferon antagonists. J Virol 81:548-557. http://dx.doi.org/10.1128/JVI.01782-06.
8. Wathelet MG, Orr M, Frieman MB, Baric RS. 2007. Severe acute respiratory syndrome coronavirus evades antiviral signaling: role of nsp1 and rational design of an attenuated strain. J Virol 81:11620-11633. http://dx.doi.org/10.1128/JVI.00702-07.
9. Nelson CA, Pekosz A, Lee CA, Diamond MS, Fremont DH. 2005. Structure and intracellular targeting of the SARS-coronavirus Orf7a accessory protein. Structure 13:75-85. http://dx.doi.org/10.1016/j.str.2004.10.010.
10. Schaecher SR, Touchette E, Schriewer J, Buller M, Pekosz A. 2007. Severe acute respiratory syndrome coronavirus gene 7 products contribute to virus-induced apoptosis. J Virol 81:11054-11068. http://dx.doi.org/10.1128/JVI.01266-07.
11. Frieman MB, Yount B, Sims AC, Deming DJ, Morrison TE, Sparks J, Denison M, Heise M, Baric RS. 2006. SARS coronavirus accessory ORFs encode luxury functions. Adv Exp Med Biol 581:149-152. http://dx.doi.org/10.1007/978-0-387-33012-9_26.
12. Yount B, Roberts RS, Sims AC, Deming D, Frieman MB, Sparks J, Denison MR, Davis N, Baric RS. 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.http://dx.doi.org/10.1128/JVI.79.23.14909-14922.2005.
13. Schaecher SR, Touchette E, Schriewer J, Buller RM, Pekosz A. 2007. Severe acute respiratory syndrome coronavirus gene 7 products contribute to virus-induced apoptosis. J Virol 81:11054-11068. http://dx.doi.org/10.1128/JVI.01266-07.
14. Tan Y-J, Fielding BC, Goh P-Y, Shen S, Tan THP, Lim SG, Hong W. 2004. Overexpression of 7a, a protein specifically encoded by the severe acute respiratory syndrome coronavirus, induces apoptosis via a caspasedependent pathway. J Virol 78:14043-14047. http://dx.doi.org/10.1128/JVI.78.24.14043-14047.2004.
15. Tan Y-X, Tan THP, Lee MJR, Tham P-Y, Gunalan V, Druce J, Birch C, Catton M, Fu NY, Yu VC, Tan Y-J. 2007. Induction of apoptosis by the severe acute respiratory syndrome coronavirus 7a protein is dependent on its interaction with the Bcl-XL protein. J Virol 81:6346-6355. http://dx.doi.org/10.1128/JVI.00090-07.
16. Tang X, Li G, Vasilakis N, Zhang Y, Shi Z, Zhong Y, Wang L-F, Zhang S. 2009. Differential stepwise evolution of SARS coronavirus functional proteins in different host species. BMC Evol Biol 9:52. http://dx.doi.org/10.1186/1471-2148-9-52.
17. Goto T, Kennel SJ, Abe M, Takishita M, Kosaka M, Solomon A, Saito S. 1994. A novel membrane antigen selectively expressed on terminally differentiated human B cells. Blood 84:1922-1930.
18. Ishikawa J, Kaisho T, Tomizawa H, Lee BO, Kobune Y, Inazawa J, Oritani K, Itoh M, Ochi T, Ishihara K, Hirano T. 1995. Molecular cloning and chromosomal mapping of a bone marrow stromal cell surface gene, BST2, that may be involved in pre-B-cell growth. Genomics 26:527-534.http://dx.doi.org/10.1016/0888-7543(95)80171-H.
19. Blasius AL, Giurisato E, Cella M, Schreiber RD, Shaw AS, Colonna M. 2006. Bone marrow stromal cell antigen 2 is a specific marker of type I IFN-producing cells in the naive mouse, but a promiscuous cell surface antigen following IFN stimulation. J Immunol 177:3260-3265. http://dx.doi.org/10.4049/jimmunol.177.5.3260.
20. Kupzig S, Korolchuk V, Rollason R, Sugden A, Wilde A, Banting G. 2003. Bst-2/HM1.24 is a raft-associated apical membrane protein with an unusual topology. Traffic 4:694-709. http://dx.doi.org/10.1034/j.1600-0854.2003.00129.x.
21. Ohtomo T, Sugamata Y, Ozaki Y, Ono K, Yoshimura Y, Kawai S, Koishihara Y, Ozaki S, Kosaka M, Hirano T, Tsuchiya M. 1999. Molecular cloning and characterization of a surface antigen preferentially overexpressed on multiple myeloma cells. Biochem Biophys ResCommun 258:583-591. http://dx.doi.org/10.1006/bbrc.1999.0683.
22. Swiecki M, Scheaffer SM, Allaire M, Fremont DH, Colonna M, Brett TJ. 2011. Structural and biophysical analysis of BST-2/tetherin ectodomains reveals an evolutionary conserved design to inhibit virus release. J Biol Chem 286:2987-2997. http://dx.doi.org/10.1074/jbc. M110.190538.
23. Jones PH, Maric M, Madison MN, Maury W, Roller RJ, Okeoma CM. 2013. BST-2/tetherin-mediated restriction of chikungunya (CHIKV) VLP budding is counteracted by CHIKV non-structural protein 1 (nsP1). Virology 438:37-49. http://dx.doi.org/10.1016/j.virol.2013.01.010.
24. Radoshitzky SR, Dong L, Chi X, Clester JC, Retterer C, Spurgers K, Kuhn JH, Sandwick S, Ruthel G, Kota K, Boltz D, Warren T, Kranzusch PJ, Whelan SPJ, Bavari S. 2010. Infectious Lassa virus, but not filoviruses, is restricted by BST-2/tetherin. J Virol 84:10569-10580. http://dx.doi.org/10.1128/JVI.00103-10.
25. Blondeau C, Pelchen-Matthews A, Mlcochova P, Marsh M, Milne RSB, Towers GJ. 2013. Tetherin restricts herpes simplex virus type 1 and is antagonised by glycoprotein M. J Virol 87:13124-13133. http://dx.doi.org/10.1128/JVI.02250-13.
26. Bampi C, Rasga L, Roux L. 2013. Antagonism to human BST-2/tetherin by Sendai virus glycoproteins. J Gen Virol 94:1211-1219. http://dx.doi.org/10.1099/vir.0.051771-0.
27. Neil SJD, Zang T, Bieniasz PD. 2008. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451:425-430. http://dx.doi.org/10.1038/nature06553.
28. Fitzpatrick K, Skasko M, Deerinck TJ, Crum J, Ellisman MH, Guatelli J. 2010. Direct restriction of virus release and incorporation of the interferon-induced protein BST-2 into HIV-1 particles. PLoS Pathog 6:e1000701. http://dx.doi.org/10.1371/journal.ppat.1000701.
29. Perez-Caballero D, Zang T, Ebrahimi A, McNatt MW, Gregory DA, Johnson MC, Bieniasz PD. 2009. Tetherin inhibits HIV-1 release by directly tethering virions to cells. Cell 139:499-511. http://dx.doi.org/10.1016/j.cell.2009.08.039.
30. Andrew AJ, Miyagi E, Kao S, Strebel K. 2009. The formation of cysteinelinked dimers of BST-2/tetherin is important for inhibition of HIV-1 virus release but not for sensitivity to Vpu. Retrovirology 6:80. http://dx.doi.org/10.1186/1742-4690-6-80.
31. Galão RP, Le Tortorec A, Pickering S, Kueck T, Neil SJD. 2012. Innate sensing of HIV-1 assembly by tetherin induces NFκB-dependent proinflammatory responses. Cell Host Microbe 12:633-644. http://dx.doi.org/10.1016/j.chom.2012.10.007.
32. Douglas JL, Viswanathan K, McCarroll MN, Gustin JK, Früh K, Moses AV. 2009. Vpu directs the degradation of the human immunodeficiency virus restriction factor BST-2/tetherin via a βTrCP-dependent mechanism. J Virol 83:7931-7947. http://dx.doi.org/10.1128/JVI.00242-09.
33. Mangeat B, Gers-Huber G, Lehmann M, Zufferey M, Luban J, Piguet V. 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. http://dx.doi.org/10.1371/journal.ppat.1000574.
34. Mitchell RS, Katsura C, Skasko MA, Fitzpatrick K, Lau D, Ruiz A, Stephens EB, Margottin-Goguet F, Benarous R, Guatelli JC. 2009. Vpu antagonizes BST-2-mediated restriction of HIV-1 release via β-TrCP and endo-lysosomal trafficking. PLoS Pathog 5:e1000450. http://dx.doi.org/10.1371/journal.ppat.1000450.
35. Gupta RK, Mlcochova P, Pelchen-Matthews A, Petit SJ, Mattiuzzo G, Pillay D, Takeuchi Y, Marsh M, Towers GJ. 2009. Simian immunodeficiency virus envelope glycoprotein counteracts tetherin/BST-2/CD317 by intracellular sequestration. Proc Natl Acad SciUSA106:20889-20894. http://dx.doi.org/10.1073/pnas.0907075106.
36. Le Tortorec A, Neil SJ. 2009. Antagonism to and intracellular sequestration of human tetherin by the human immunodeficiency virus type 2 envelope glycoprotein. J Virol 83:11966-11978. http://dx.doi.org/10.1128/JVI.01515-09.
37. Wang S-M, Huang K-J, Wang C-T. 2014. BST2/CD317 counteracts human coronavirus 229E productive infection by tethering virions at the cell surface. Virology 449:287-296. http://dx.doi.org/10.1016/j.virol.2013.11.030.
38. Zhang F, Wilson SJ, Landford WC, Virgen B, Gregory D, Johnson MC, Munch J, KirchhoffF, Bieniasz PD, Hatziioannou T. 2009. Nef proteins from simian immunodeficiency viruses are tetherin antagonists. Cell Host Microbe 6:54-67. http://dx.doi.org/10.1016/j.chom.2009.05.008.
39. Kaletsky RL, Francica JR, Agrawal-Gamse C, Bates P. 2009. Tetherinmediated restriction of filovirus budding is antagonized by the Ebola glycoprotein. Proc Natl Acad Sci U S A 106:2886-2891. http://dx.doi.org/10.1073/pnas.0811014106.
40. Stertz S, Reichelt M, Spiegel M, Kuri T, Martínez-Sobrido L, García-Sastre A, Weber F, Kochs G. 2007. The intracellular sites of early replication and budding of SARS-coronavirus. Virology 361:304-315. http://dx.doi.org/10.1016/j.virol.2006.11.027.
41. Yount B, Curtis KM, Fritz EA, Hensley LE, Jahrling PB, Prentice E, Denison MR, Geisbert TW, Baric RS. 2003. Reverse genetics with a full-length infectious cDNA of severe acute respiratory syndrome coronavirus. Proc Natl Acad Sci U S A 100:12995-13000. http://dx.doi.org/10.1073/pnas.1735582100.
42. Sims AC, Baric RS, Yount B, Burkett SE, Collins PL, Pickles RJ. 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. http://dx.doi.org/10.1128/JVI.79.24.15511-15524.2005.
43. Pewe L, Zhou H, Netland J, Tangudu C, Olivares H, Shi L, Look D, Gallagher T, Perlman S. 2005. A severe acute respiratory syndromeassociated coronavirus-specific protein enhances virulence of an attenuated murine coronavirus. J Virol 79:11335-11342. http://dx.doi.org/10.1128/JVI.79.17.11335-11342.2005.
44. Tangudu C, Olivares H, Netland J, Perlman S, Gallagher T. 2007. Severe acute respiratory syndrome coronavirus protein 6 accelerates murine coronavirus infections. J Virol 81:1220-1229. http://dx.doi.org/10.1128/JVI.01515-06.
45. Frieman M, Ratia K, Johnston RE, Mesecar AD, Baric RS. 2009. Severe acute respiratory syndrome coronavirus papain-like protease ubiquitin-like domain and catalytic domain regulate antagonism of IRF3 and NF-kappaB signaling. J Virol 83:6689-6705. http://dx.doi.org/10.1128/JVI.02220-08.
46. Barretto N, Jukneliene D, Ratia K, Chen Z, Mesecar AD, Baker SC. 2005. The papain-like protease of severe acute respiratory syndrome coronavirus has deubiquitinating activity. J Virol 79:15189-15198. http://dx.doi.org/10.1128/JVI.79.24.15189-15198.2005.
47. Clementz MA, Chen Z, Banach BS, Wang Y, Sun L, Ratia K, Baez-Santos YM, Wang J, Takayama J, Ghosh AK, Li K, Mesecar AD, Baker SC. 2010. Deubiquitinating and interferon antagonism activities of coronavirus papain-like proteases. J Virol 84:4619-4629. http://dx.doi.org/10.1128/JVI.02406-09.
48. Kamitani W, Narayanan K, Huang C, Lokugamage K, Ikegami T, Ito N, Kubo H, Makino S. 2006. Severe acute respiratory syndrome coronavirus nsp1 protein suppresses host gene expression by promoting host mRNA degradation. Proc Natl Acad SciUSA103:12885-12890. http://dx.doi.org/10.1073/pnas.0603144103.
49. Devaraj SG, Wang N, Chen Z, Chen Z, Tseng M, Barretto N, Lin R, Peters CJ, Tseng CT, Baker SC, Li K. 2007. Regulation of IRF-3-dependent innate immunity by the papain-like protease domain of the severe acute respiratory syndrome coronavirus. J Biol Chem 282:32208-32221.http://dx.doi.org/10.1074/jbc. M704870200.
50. Basu D, Walkiewicz MP, Frieman M, Baric RS, Auble DT, Engel DA. 2009. Novel influenza virus NS1 antagonists block replication and restore innate immune function. J Virol 83:1881-1891. http://dx.doi.org/10.1128/JVI.01805-08.
51. Van Damme N, GoffD, Katsura C, Jorgenson RL, Mitchell R, Johnson MC, Stephens EB, Guatelli J. 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. http://dx.doi.org/10.1016/j.chom.2008.03.001.
52. Hoa XD, Kirk AG, Tabrizian M. 2007. Towards integrated and sensitive surface plasmon resonance biosensors: a review of recent progress. Biosens Bioelectron 23:151-160. http://dx.doi.org/10.1016/j.bios.2007.07.001.
53. McNatt MW, Zang T, Hatziioannou T, Bartlett M, Ben Fofana I, Johnson WE, Neil SJD, Bieniasz PD. 2009. Species-specific activity of HIV-1 Vpu and positive selection of tetherin transmembrane domain variants. PLoS Pathog 5:e1000300. http://dx.doi.org/10.1371/journal.ppat.1000300.
54. Mansouri M, Viswanathan K, Douglas JL, Hines J, Gustin J, Moses AV, Früh K. 2009. Molecular mechanism of BST2/tetherin downregulation by K5/MIR2 of Kaposi's sarcoma-associated herpesvirus. J Virol 83:9672-9681.http://dx.doi.org/10.1128/JVI.00597-09.
55. Jia HP, Look DC, Shi L, Hickey M, Pewe L, Netland J, Farzan M, Wohlford-Lenane C, Perlman S, McCray PB, Jr. 2005. ACE2 receptor expression and severe acute respiratory syndrome coronavirus infection depend on differentiation of human airway epithelia. J Virol 79:14614-14621.http://dx.doi.org/10.1128/JVI.79.23.14614-14621.2005.