Looking for a needle in a haystack: Cellular proteins that may interact with the tyrosine-based sorting signal of the TGEV S protein

Virus Research

Volumn 202, Issue , 2015, Pages 3-11

  Trincone, Anna ^a,b   Schwegmann Weßels, Christel ^a  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b Centre for Pharmacology and Toxicology Institute for Pharmaco and Toxicogenomics   (Germany)

Author keywords

Assembly; Cellular interaction candidates; Coronavirus; Filamin A; Spike protein; TGEV

Indexed keywords

CELL PROTEIN; FILAMIN A; PROTEIN S; PROTEOME; VIRUS PROTEIN; VITRONECTIN; CORONAVIRUS SPIKE GLYCOPROTEIN; FILAMIN; PROTEIN BINDING;

ARTICLE; CORONAVIRUS INFECTION; HUMAN; IMMUNOFLUORESCENCE TEST; MASS SPECTROMETRY; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; TRANSMISSIBLE GASTROENTERITIS VIRUS; VIRUS CELL INTERACTION; ANIMAL; HOST PATHOGEN INTERACTION; METABOLISM; PHYSIOLOGY;

CORONAVIRUS; TRANSMISSIBLE GASTROENTERITIS VIRUS;

ANIMALS; FILAMINS; HOST-PATHOGEN INTERACTIONS; HUMANS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; SPIKE GLYCOPROTEIN, CORONAVIRUS; TRANSMISSIBLE GASTROENTERITIS VIRUS;

EID: 84930045228     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2014.11.029     Document Type: Article

References (85)

1. Aschenbrenner L., Lee T., Hasson T. Myo6 facilitates the translocation of endocytic vesicles from cell peripheries. Mol. Biol. Cell 2003, 14:2728-2743.
2. Backes P., Quinkert D., Reiss S., Binder M., Zayas M., Rescher U., Gerke V., Bartenschlager R., Lohmann V. Role of annexin A2 in the production of infectious hepatitis C virus particles. J. Virol. 2010, 84:5775-5789.
3. Beaton A.R., Rodriguez J., Reddy Y.K., Roy P. The membrane trafficking protein calpactin forms a complex with bluetongue virus protein NS3 and mediates virus release. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:13154-13159.
4. Bost A.G., Prentice E., Denison M.R. Mouse hepatitis virus replicase protein complexes are translocated to sites of M protein accumulation in the ERGIC at late times of infection. Virology 2001, 285:21-29.
5. Calvo E., Escors D., Lopez J.A., Gonzalez J.M., Alvarez A., Arza E., Enjuanes L. Phosphorylation and subcellular localization of transmissible gastroenteritis virus nucleocapsid protein in infected cells. J. Gen. Virol. 2005, 86:2255-2267.
6. Cantin R., Methot S., Tremblay M.J. Plunder and stowaways: incorporation of cellular proteins by enveloped viruses. J. Virol. 2005, 79:6577-6587.
7. Cao Z., Han Z., Shao Y., Geng H., Kong X., Liu S. Proteomic analysis of chicken embryonic trachea and kidney tissues after infection in ovo by avian infectious bronchitis coronavirus. Proteome Sci. 2011, 9:11.
8. Cao Z., Han Z., Shao Y., Liu X., Sun J., Yu D., Kong X., Liu S. Proteomics analysis of differentially expressed proteins in chicken trachea and kidney after infection with the highly virulent and attenuated coronavirus infectious bronchitis virus in vivo. Proteome Sci. 2012, 10:24.
9. Chertova E., Chertov O., Coren L.V., Roser J.D., Trubey C.M., Bess J.W., Sowder R.C., Barsov E., Hood B.L., Fisher R.J., Nagashima K., Conrads T.P., Veenstra T.D., Lifson J.D., Ott D.E. Proteomic and biochemical analysis of purified human immunodeficiency virus type 1 produced from infected monocyte-derived macrophages. J. Virol. 2006, 80:9039-9052.
10. Cohen J.R., Lin L.D., Machamer C.E. Identification of a Golgi complex-targeting signal in the cytoplasmic tail of the severe acute respiratory syndrome coronavirus envelope protein. J. Virol. 2011, 85:5794-5803.
11. Cooper J., Liu L., Woodruff E.A., Taylor H.E., Goodwin J.S., D'Aquila R.T., Spearman P., Hildreth J.E., Dong X. Filamin A protein interacts with human immunodeficiency virus type 1 Gag protein and contributes to productive particle assembly. J. Biol. Chem. 2011, 286:28498-28510.
12. Corse E., Machamer C.E. Infectious bronchitis virus E protein is targeted to the Golgi complex and directs release of virus-like particles. J. Virol. 2000, 74:4319-4326.
13. Corse E., Machamer C.E. The cytoplasmic tail of infectious bronchitis virus E protein directs Golgi targeting. J. Virol. 2002, 76:1273-1284.
14. Corse E., Machamer C.E. The cytoplasmic tails of infectious bronchitis virus E and M proteins mediate their interaction. Virology 2003, 312:25-34.
15. Cudmore S., Reckmann I., Way M. Viral manipulations of the actin cytoskeleton. Trends Microbiol. 1997, 5:142-148.
16. Cunningham C.C., Gorlin J.B., Kwiatkowski D.J., Hartwig J.H., Janmey P.A., Byers H.R., Stossel T.P. Actin-binding protein requirement for cortical stability and efficient locomotion. Science 1992, 255:325-327.
17. de Haan C.A., Smeets M., Vernooij F., Vennema H., Rottier P.J. Mapping of the coronavirus membrane protein domains involved in interaction with the spike protein. J. Virol. 1999, 73:7441-7452.
18. de Haan C.A., Vennema H., Rottier P.J. Assembly of the coronavirus envelope: homotypic interactions between the M proteins. J. Virol. 2000, 74:4967-4978.
19. Del Valle-Perez B., Martinez V.G., Lacasa-Salavert C., Figueras A., Shapiro S.S., Takafuta T., Casanovas O., Capella G., Ventura F., Vinals F. Filamin B plays a key role in vascular endothelial growth factor-induced endothelial cell motility through its interaction with Rac-1 and Vav-2. J. Biol. Chem. 2010, 285:10748-10760.
20. Donnelly S.R., Moss S.E. Annexins in the secretory pathway. Cell. Mol. Life Sci. 1997, 53:533-538.
21. Emmott E., Munday D., Bickerton E., Britton P., Rodgers M.A., Whitehouse A., Zhou E.M., Hiscox J.A. The cellular interactome of the coronavirus infectious bronchitis virus nucleocapsid protein and functional implications for virus biology. J. Virol. 2013, 87:9486-9500.
22. Emmott E., Rodgers M.A., Macdonald A., McCrory S., Ajuh P., Hiscox J.A. Quantitative proteomics using stable isotope labeling with amino acids in cell culture reveals changes in the cytoplasmic, nuclear, and nucleolar proteomes in Vero cells infected with the coronavirus infectious bronchitis virus. Mol. Cell Proteomics 2010, 9:1920-1936.
23. Emmott E., Smith C., Emmett S.R., Dove B.K., Hiscox J.A. Elucidation of the avian nucleolar proteome by quantitative proteomics using SILAC and changes in cells infected with the coronavirus infectious bronchitis virus. Proteomics 2010, 10:3558-3562.
24. Escors D., Ortego J., Laude H., Enjuanes L. The membrane M protein carboxy terminus binds to transmissible gastroenteritis coronavirus core and contributes to core stability. J. Virol. 2001, 75:1312-1324.
25. Godeke G.J., de Haan C.A., Rossen J.W., Vennema H., Rottier P.J. Assembly of spikes into coronavirus particles is mediated by the carboxy-terminal domain of the spike protein. J. Virol. 2000, 74:1566-1571.
26. Gov N.S., Gopinathan A. Dynamics of membranes driven by actin polymerization. Biophys. J. 2006, 90:454-469.
27. Greber U.F., Way M. A superhighway to virus infection. Cell 2006, 124:741-754.
28. Harrist A.V., Ryzhova E.V., Harvey T., Gonzalez-Scarano F. Anx2 interacts with HIV-1 Gag at phosphatidylinositol (4,5) bisphosphate-containing lipid rafts and increases viral production in 293T cells. PLoS ONE 2009, 4:e5020.
29. Hay J.C., Klumperman J., Oorschot V., Steegmaier M., Kuo C.S., Scheller R.H. Localization, dynamics, and protein interactions reveal distinct roles for ER and Golgi SNAREs. J. Cell Biol. 1998, 141:1489-1502.
30. He R., Leeson A., Ballantine M., Andonov A., Baker L., Dobie F., Li Y., Bastien N., Feldmann H., Strocher U., Theriault S., Cutts T., Cao J., Booth T.F., Plummer F.A., Tyler S., Li X. Characterization of protein-protein interactions between the nucleocapsid protein and membrane protein of the SARS coronavirus. Virus Res. 2004, 105:121-125.
31. Hiscox J.A., Wurm T., Wilson L., Britton P., Cavanagh D., Brooks G. The coronavirus infectious bronchitis virus nucleoprotein localizes to the nucleolus. J. Virol. 2001, 75:506-512.
32. Jeon Y.J., Choi J.S., Lee J.Y., Yu K.R., Ka S.H., Cho Y., Choi E.J., Baek S.H., Seol J.H., Park D., Bang O.S., Chung C.H. Filamin B serves as a molecular scaffold for type I interferon-induced c-Jun NH2-terminal kinase signaling pathway. Mol. Biol. Cell 2008, 19:5116-5130.
33. Jiang X.S., Tang L.Y., Dai J., Zhou H., Li S.J., Xia Q.C., Wu J.R., Zeng R. Quantitative analysis of severe acute respiratory syndrome (SARS)-associated coronavirus-infected cells using proteomic approaches: implications for cellular responses to virus infection. Mol. Cell. Proteomics 2005, 4:902-913.
34. Jimenez-Baranda S., Gomez-Mouton C., Rojas A., Martinez-Prats L., Mira E., Ana Lacalle R., Valencia A., Dimitrov D.S., Viola A., Delgado R., Martinez A.C., Manes S. Filamin-A regulates actin-dependent clustering of HIV receptors. Nat. Cell Biol. 2007, 9:838-846.
35. Kaelin W.G., Pallas D.C., DeCaprio J.A., Kaye F.J., Livingston D.M. Identification of cellular proteins that can interact specifically with the T/E1A-binding region of the retinoblastoma gene product. Cell 1991, 64:521-532.
36. Kanters E., van Rijssel J., Hensbergen P.J., Hondius D., Mul F.P., Deelder A.M., Sonnenberg A., van Buul J.D., Hordijk P.L. Filamin B mediates ICAM-1-driven leukocyte transendothelial migration. J. Biol. Chem. 2008, 283:31830-31839.
37. Kim H., Nakamura F., Lee W., Hong C., Perez-Sala D., McCulloch C.A. Regulation of cell adhesion to collagen via beta1 integrins is dependent on interactions of filamin A with vimentin and protein kinase C epsilon. Exp. Cell Res. 2010, 316:1829-1844.
38. Kirchhausen T. Three ways to make a vesicle. Nat. Rev. Mol. Cell Biol. 2000, 1:187-198.
39. Klaile E., Muller M.M., Kannicht C., Singer B.B., Lucka L. CEACAM1 functionally interacts with filamin A and exerts a dual role in the regulation of cell migration. J. Cell Sci. 2005, 118:5513-5524.
40. Klumperman J., Locker J.K., Meijer A., Horzinek M.C., Geuze H.J., Rottier P.J. Coronavirus M proteins accumulate in the Golgi complex beyond the site of virion budding. J. Virol. 1994, 68:6523-6534.
41. Kong Q., Xue C., Ren X., Zhang C., Li L., Shu D., Bi Y., Cao Y. Proteomic analysis of purified coronavirus infectious bronchitis virus particles. Proteome Sci. 2010, 8:29.
42. Krempl C., Herrler G. Sialic acid binding activity of transmissible gastroenteritis coronavirus affects sedimentation behavior of virions and solubilized glycoproteins. J. Virol. 2001, 75:844-849.
43. Krijnse-Locker J., Ericsson M., Rottier P.J., Griffiths G. 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. 1994, 124:55-70.
44. Lim K.P., Liu D.X. 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. 2001, 276:17515-17523.
45. Liu G., Thomas L., Warren R.A., Enns C.A., Cunningham C.C., Hartwig J.H., Thomas G. Cytoskeletal protein ABP-280 directs the intracellular trafficking of furin and modulates proprotein processing in the endocytic pathway. J. Cell Biol. 1997, 139:1719-1733.
46. Locker J.K., Klumperman J., Oorschot V., Horzinek M.C., Geuze H.J., Rottier P.J. The cytoplasmic tail of mouse hepatitis virus M protein is essential but not sufficient for its retention in the Golgi complex. J. Biol. Chem. 1994, 269:28263-28269.
47. Machamer C.E., Mentone S.A., Rose J.K., Farquhar M.G. The E1 glycoprotein of an avian coronavirus is targeted to the cis Golgi complex. Proc. Natl. Acad. Sci. U.S.A. 1990, 87:6944-6948.
48. McBride C.E., Li J., Machamer C.E. 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. 2007, 81:2418-2428.
49. McBride C.E., Machamer C.E. A single tyrosine in the severe acute respiratory syndrome coronavirus membrane protein cytoplasmic tail is important for efficient interaction with spike protein. J. Virol. 2010, 84:1891-1901.
50. Moss S.E., Morgan R.O. The annexins. Genome Biol. 2004, 5:219.
51. 2+ and calmodulin regulate the binding of filamin A to actin filaments. J. Biol. Chem. 2005, 280:32426-32433.
52. Nakamura F., Stossel T.P., Hartwig J.H. The filamins: organizers of cell structure and function. Cell. Adhes. Migr. 2011, 5:160-169.
53. Neuman B.W., Joseph J.S., Saikatendu K.S., Serrano P., Chatterjee A., Johnson M.A., Liao L., Klaus J.P., Yates J.R., Wuthrich K., Stevens R.C., Buchmeier M.J., Kuhn P. Proteomics analysis unravels the functional repertoire of coronavirus nonstructural protein 3. J. Virol. 2008, 82:5279-5294.
54. Nguyen V.P., Hogue B.G. Protein interactions during coronavirus assembly. J. Virol. 1997, 71:9278-9284.
55. Nogales A., Marquez-Jurado S., Galan C., Enjuanes L., Almazan F. Transmissible gastroenteritis coronavirus RNA-dependent RNA polymerase and nonstructural proteins 2, 3, and 8 are incorporated into viral particles. J. Virol. 2012, 86:1261-1266.
56. Ohta Y., Suzuki N., Nakamura S., Hartwig J.H., Stossel T.P. The small GTPase RalA targets filamin to induce filopodia. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:2122-2128.
57. Orlinick J.R., Chao M.V. Interactions of cellular polypeptides with the cytoplasmic domain of the mouse Fas antigen. J. Biol. Chem. 1996, 271:8627-8632.
58. Paul A., Trincone A., Siewert S., Herrler G., Schwegmann-Wessels C. A lysine-methionine exchange in a coronavirus surface protein transforms a retention motif into an endocytosis signal. Biol. Chem. 2014, 395:657-665.
59. Pfefferle S., Schopf J., Kogl M., Friedel C.C., Muller M.A., Carbajo-Lozoya J., Stellberger T., von Dall'Armi E., Herzog P., Kallies S., Niemeyer D., Ditt V., Kuri T., Zust R., Pumpor K., Hilgenfeld R., Schwarz F., Zimmer R., Steffen I., Weber F., Thiel V., Herrler G., Thiel H.J., Schwegmann-Wessels C., Pohlmann S., Haas J., Drosten C., von Brunn A. The SARS-coronavirus-host interactome: identification of cyclophilins as target for pan-coronavirus inhibitors. PLoS Pathog. 2011, 7:e1002331.
60. Ploubidou A., Way M. Viral transport and the cytoskeleton. Curr. Opin. Cell Biol. 2001, 13:97-105.
61. Popowicz G.M., Schleicher M., Noegel A.A., Holak T.A. Filamins: promiscuous organizers of the cytoskeleton. Trends Biochem. Sci. 2006, 31:411-419.
62. Radtke K., Dohner K., Sodeik B. Viral interactions with the cytoskeleton: a hitchhiker's guide to the cell. Cell. Microbiol. 2006, 8:387-400.
63. Rowland R.R., Chauhan V., Fang Y., Pekosz A., Kerrigan M., Burton M.D. Intracellular localization of the severe acute respiratory syndrome coronavirus nucleocapsid protein: absence of nucleolar accumulation during infection and after expression as a recombinant protein in vero cells. J. Virol. 2005, 79:11507-11512.
64. Ryzhova E.V., Vos R.M., Albright A.V., Harrist A.V., Harvey T., Gonzalez-Scarano F. Annexin 2: a novel human immunodeficiency virus type 1 Gag binding protein involved in replication in monocyte-derived macrophages. J. Virol. 2006, 80:2694-2704.
65. Sambrook J., Russell D.W. Detection of protein-protein interactions using the GST fusion protein pulldown technique. CSH Protoc. 2006, 2006.
66. Schwegmann-Wessels C., Al-Falah M., Escors D., Wang Z., Zimmer G., Deng H., Enjuanes L., Naim H.Y., 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. 2004, 279:43661-43666.
67. Shaw M.L., Stone K.L., Colangelo C.M., Gulcicek E.E., Palese P. Cellular proteins in influenza virus particles. PLoS Pathog. 2008, 4:e1000085.
68. 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. U.S.A. 2004, 101:4240-4245.
69. Smith D.B., Johnson K.S. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene 1988, 67:31-40.
70. Stahlhut M., van Deurs B. Identification of filamin as a novel ligand for caveolin-1: evidence for the organization of caveolin-1-associated membrane domains by the actin cytoskeleton. Mol. Biol. Cell 2000, 11:325-337.
71. Sverdlov M., Shinin V., Place A.T., Castellon M., Minshall R.D. Filamin A regulates caveolae internalization and trafficking in endothelial cells. Mol. Biol. Cell 2009, 20:4531-4540.
72. Timani K.A., Liao Q., Ye L., Zeng Y., Liu J., Zheng Y., Yang X., Lingbao K., Gao J., Zhu Y. Nuclear/nucleolar localization properties of C-terminal nucleocapsid protein of SARS coronavirus. Virus Res. 2005, 114:23-34.
73. Tooze J., Tooze S., Warren G. Replication of coronavirus MHV-A59 in sac-cells: determination of the first site of budding of progeny virions. Eur. J. Cell Biol. 1984, 33:281-293.
74. Tseng Y., An K.M., Esue O., Wirtz D. The bimodal role of filamin in controlling the architecture and mechanics of F-actin networks. J. Biol. Chem. 2004, 279:1819-1826.
75. Vennema H., Godeke G.J., Rossen J.W., Voorhout W.F., Horzinek M.C., Opstelten D.J., Rottier P.J. Nucleocapsid-independent assembly of coronavirus-like particles by co-expression of viral envelope protein genes. EMBO J. 1996, 15:2020-2028.
76. Vogels M.W., van Balkom B.W., Kaloyanova D.V., Batenburg J.J., Heck A.J., Helms J.B., Rottier P.J., de Haan C.A. Identification of host factors involved in coronavirus replication by quantitative proteomics analysis. Proteomics 2011, 11:64-80.
77. Volpicelli-Daley L.A., Li Y., Zhang C.J., Kahn R.A. Isoform-selective effects of the depletion of ADP-ribosylation factors 1-5 on membrane traffic. Mol. Biol. Cell 2005, 16:4495-4508.
78. von Brunn A., Teepe C., Simpson J.C., Pepperkok R., Friedel C.C., Zimmer R., Roberts R., Baric R., Haas J. Analysis of intraviral protein-protein interactions of the SARS coronavirus ORFeome. PLoS ONE 2007, 2:e459.
79. Wang J., Fang S., Xiao H., Chen B., Tam J.P., Liu D.X. Interaction of the coronavirus infectious bronchitis virus membrane protein with beta-actin and its implication in virion assembly and budding. PLoS ONE 2009, 4:e4908.
80. Winter C., Schwegmann-Wessels C., Neumann U., Herrler G. The spike protein of infectious bronchitis virus is retained intracellularly by a tyrosine motif. J. Virol. 2008, 82:2765-2771.
81. Wurm T., Chen H., Hodgson T., Britton P., Brooks G., Hiscox J.A. Localization to the nucleolus is a common feature of coronavirus nucleoproteins, and the protein may disrupt host cell division. J. Virol. 2001, 75:9345-9356.
82. You J., Dove B.K., Enjuanes L., DeDiego M.L., Alvarez E., Howell G., Heinen P., Zambon M., Hiscox J.A. Subcellular localization of the severe acute respiratory syndrome coronavirus nucleocapsid protein. J. Gen. Virol. 2005, 86:3303-3310.
83. Zhang X., Shi H., Chen J., Shi D., Li C., Feng L. EF1A interacting with nucleocapsid protein of transmissible gastroenteritis coronavirus and plays a role in virus replication. Vet. Microbiol. 2014, 172:443-448.
84. Zhang X., Shi H.Y., Chen J.F., Shi D., Lang H.W., Wang Z.T., Feng L. Identification of cellular proteome using two-dimensional difference gel electrophoresis in ST cells infected with transmissible gastroenteritis coronavirus. Proteome Sci. 2013, 11:31.
85. Zhou B., Liu J., Wang Q., Liu X., Li X., Li P., Ma Q., Cao C. The nucleocapsid protein of severe acute respiratory syndrome coronavirus inhibits cell cytokinesis and proliferation by interacting with translation elongation factor 1alpha. J. Virol. 2008, 82:6962-6971.