Tubulins interact with porcine and human S proteins of the genus Alphacoronavirus and support successful assembly and release of infectious viral particles

Virology

Volumn 497, Issue , 2016, Pages 185-197

  Rüdiger, Anna Theresa ^a   Mayrhofer, Peter ^b   Ma Lauer, Yue ^b   Pohlentz, Gottfried ^c   Müthing, Johannes ^c   von Brunn, Albrecht ^b   Schwegmann Weßels, Christel ^a  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

Assembly; Coronavirus; Incorporation; Interaction; Intracellular transport; Microtubule; Spike protein; TGEV; Viral infectivity

Indexed keywords

ALPHA TUBULIN; AMINO ACID; BETA TUBULIN; VIRUS SPIKE PROTEIN; VITRONECTIN; CORONAVIRUS SPIKE GLYCOPROTEIN; NOCODAZOLE; PROTEIN BINDING; TUBULIN;

ALPHACORONAVIRUS; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CORONAVIRIDAE; CYTOPLASM; DEPOLYMERIZATION; HOST CELL; HUMAN; HUMAN CELL; MICROTUBULE; NONHUMAN; PIG; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; TRANSMISSIBLE GASTROENTERITIS VIRUS; VIRION; VIRUS ASSEMBLY; VIRUS CELL INTERACTION; VIRUS PARTICLE; VIRUS STRAIN; ANIMAL; CELL LINE; CHEMISTRY; CORONAVIRIDAE INFECTION; DRUG EFFECTS; INTRACELLULAR SPACE; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; TRANSMISSIBLE GASTROENTERITIS OF SWINE; VIROLOGY; VIRUS RELEASE; VIRUS REPLICATION;

ANIMALS; CELL LINE; CORONAVIRIDAE; CORONAVIRIDAE INFECTIONS; GASTROENTERITIS, TRANSMISSIBLE, OF SWINE; HUMANS; INTRACELLULAR SPACE; NOCODAZOLE; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN TRANSPORT; SPIKE GLYCOPROTEIN, CORONAVIRUS; SWINE; TUBULIN; VIRUS ASSEMBLY; VIRUS RELEASE; VIRUS REPLICATION;

EID: 84979698229     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2016.07.022     Document Type: Article

References (77)

1. Alonso, C., Miskin, J., Hernaez, B., Fernandez-Zapatero, P., Soto, L., Canto, C., Rodriguez-Crespo, I., Dixon, L., Escribano, J.M., African swine fever virus protein p54 interacts with the microtubular motor complex through direct binding to light-chain dynein. J. Virol. 75 (2001), 9819–9827.
2. Babiss, L.E., Luftig, R.B., Weatherbee, J.A., Weihing, R.R., Ray, U.R., Fields, B.N., Reovirus serotypes 1 and 3 differ in their in vitro association with microtubules. J. Virol. 30 (1979), 863–874.
3. Belov, G.A., Altan-Bonnet, N., Kovtunovych, G., Jackson, C.L., Lippincott-Schwartz, J., Ehrenfeld, E., Hijacking components of the cellular secretory pathway for replication of poliovirus RNA. J. Virol. 81 (2007), 558–567.
4. Ben-Ze'ev, A., Horowitz, M., Skolnik, H., Abulafia, R., Laub, O., Aloni, Y., The metabolism of SV40 RNA is associated with the cytoskeletal framework. Virology 111 (1981), 475–487.
5. Beske, O., Reichelt, M., Taylor, M.P., Kirkegaard, K., Andino, R., Poliovirus infection blocks ERGIC-to-Golgi trafficking and induces microtubule-dependent disruption of the Golgi complex. J. Cell Sci. 120 (2007), 3207–3218.
6. Biswas, K., Das Sarma, J., Effect of microtubule disruption on neuronal spread and replication of demyelinating and nondemyelinating strains of mouse hepatitis virus in vitro. J. Virol. 88 (2014), 3043–3047.
7. Bosch, B.J., de Haan, C.A., Smits, S.L., Rottier, P.J., Spike protein assembly into the coronavirion: exploring the limits of its sequence requirements. Virology 334 (2005), 306–318.
8. Chinese, S.M.E.C., Molecular evolution of the SARS coronavirus during the course of the SARS epidemic in China. Science 303 (2004), 1666–1669.
9. Choe, S.S., Dodd, D.A., Kirkegaard, K., Inhibition of cellular protein secretion by picornaviral 3A proteins. Virology 337 (2005), 18–29.
10. Corman, V.M., Baldwin, H.J., Tateno, A.F., Zerbinati, R.M., Annan, A., Owusu, M., Nkrumah, E.E., Maganga, G.D., Oppong, S., Adu-Sarkodie, Y., Vallo, P., da Silva Filho, L.V., Leroy, E.M., Thiel, V., van der Hoek, L., Poon, L.L., Tschapka, M., Drosten, C., Drexler, J.F., Evidence for an ancestral association of human coronavirus 229E with bats. J. Virol. 89 (2015), 11858–11870.
11. Cudmore, S., Reckmann, I., Way, M., Viral manipulations of the actin cytoskeleton. Trends Microbiol. 5 (1997), 142–148.
12. Dewerchin, H.L., Desmarets, L.M., Noppe, Y., Nauwynck, H.J., Myosins 1 and 6, myosin light chain kinase, actin and microtubules cooperate during antibody-mediated internalisation and trafficking of membrane-expressed viral antigens in feline infectious peritonitis virus infected monocytes. Vet. Res., 45, 2014, 17.
13. Douglas, M.W., Diefenbach, R.J., Homa, F.L., Miranda-Saksena, M., Rixon, F.J., Vittone, V., Byth, K., Cunningham, A.L., Herpes simplex virus type 1 capsid protein VP26 interacts with dynein light chains RP3 and Tctex1 and plays a role in retrograde cellular transport. J. Biol. Chem. 279 (2004), 28522–28530.
14. Fokin, A.I., Brodsky, I.B., Burakov, A.V., Nadezhdina, E.S., Interaction of early secretory pathway and Golgi membranes with microtubules and microtubule motors. Biochemistry 79 (2014), 879–893.
15. Ge, X.Y., Li, J.L., Yang, X.L., Chmura, A.A., Zhu, G., Epstein, J.H., Mazet, J.K., Hu, B., Zhang, W., Peng, C., Zhang, Y.J., Luo, C.M., Tan, B., Wang, N., Zhu, Y., Crameri, G., Zhang, S.Y., Wang, L.F., Daszak, P., Shi, Z.L., Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor. Nature 503 (2013), 535–538.
16. 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. 74 (2000), 1566–1571.
17. Graham, R.L., Baric, R.S., Recombination, reservoirs, and the modular spike: mechanisms of coronavirus cross-species transmission. J. Virol. 84 (2010), 3134–3146.
18. Guan, Y., Zheng, B.J., He, Y.Q., Liu, X.L., Zhuang, Z.X., Cheung, C.L., Luo, S.W., Li, P.H., Zhang, L.J., Guan, Y.J., Butt, K.M., Wong, K.L., Chan, K.W., Lim, W., Shortridge, K.F., Yuen, K.Y., Peiris, J.S., Poon, L.L., Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science 302 (2003), 276–278.
19. Han, X., Li, Z., Chen, H., Wang, H., Mei, L., Wu, S., Zhang, T., Liu, B., Lin, X., Influenza virus A/Beijing/501/2009(H1N1) NS1 interacts with beta-tubulin and induces disruption of the microtubule network and apoptosis on A549 cells. PLoS One, 7, 2012, e48340.
20. Hara, Y., Hasebe, R., Sunden, Y., Ochiai, K., Honda, E., Sakoda, Y., Umemura, T., Propagation of swine hemagglutinating encephalomyelitis virus and pseudorabies virus in dorsal root ganglia cells. J. Vet. Med. Sci. 71 (2009), 595–601.
21. Heald, R., Nogales, E., Microtubule dynamics. J. Cell Sci. 115 (2002), 3–4.
22. Henry Sum, M.S., The involvement of microtubules and actin during the infection of Japanese encephalitis virus in neuroblastoma cell line, IMR32. Biomed. Res. Int., 2015, 2015, 695283.
23. Hsieh, M.J., White, P.J., Pouton, C.W., Interaction of viruses with host cell molecular motors. Curr. Opin. Biotechnol. 21 (2010), 633–639.
24. Hyde, J.L., Gillespie, L.K., Mackenzie, J.M., Mouse norovirus 1 utilizes the cytoskeleton network to establish localization of the replication complex proximal to the microtubule organizing center. J. Virol. 86 (2012), 4110–4122.
25. Jacob, Y., Badrane, H., Ceccaldi, P.E., Tordo, N., Cytoplasmic dynein LC8 interacts with lyssavirus phosphoprotein. J. Virol. 74 (2000), 10217–10222.
26. Johannsen, E., Luftig, M., Chase, M.R., Weicksel, S., Cahir-McFarland, E., Illanes, D., Sarracino, D., Kieff, E., Proteins of purified Epstein-Barr virus. Proc. Natl. Acad. Sci. USA 101 (2004), 16286–16291.
27. Kelkar, S.A., Pfister, K.K., Crystal, R.G., Leopold, P.L., Cytoplasmic dynein mediates adenovirus binding to microtubules. J. Virol. 78 (2004), 10122–10132.
28. Knoops, K., Swett-Tapia, C., van den Worm, S.H., Te Velthuis, A.J., Koster, A.J., Mommaas, A.M., Snijder, E.J., Kikkert, M., Integrity of the early secretory pathway promotes, but is not required for, severe acute respiratory syndrome coronavirus RNA synthesis and virus-induced remodeling of endoplasmic reticulum membranes. J. Virol. 84 (2010), 833–846.
29. Konan, K.V., Giddings, T.H. Jr., Ikeda, M., Li, K., Lemon, S.M., Kirkegaard, K., Nonstructural protein precursor NS4A/B from hepatitis C virus alters function and ultrastructure of host secretory apparatus. J. Virol. 77 (2003), 7843–7855.
30. Kuhl, A., Hoffmann, M., Muller, M.A., Munster, V.J., Gnirss, K., Kiene, M., Tsegaye, T.S., Behrens, G., Herrler, G., Feldmann, H., Drosten, C., Pohlmann, S., Comparative analysis of Ebola virus glycoprotein interactions with human and bat cells. J. Infect. Dis. 204:Suppl 3 (2011), S840–S849.
31. Kyhse-Andersen, J., Electroblotting of multiple gels: a simple apparatus without buffer tank for rapid transfer of proteins from polyacrylamide to nitrocellulose. J. Biochem. Biophys. Methods 10 (1984), 203–209.
32. Lanier, L.M., Volkman, L.E., Actin binding and nucleation by Autographa california M nucleopolyhedrovirus. Virology 243 (1998), 167–177.
33. Lau, S.K., Woo, P.C., Li, K.S., Huang, Y., Tsoi, H.W., Wong, B.H., Wong, S.S., Leung, S.Y., Chan, K.H., Yuen, K.Y., Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc. Natl. Acad. Sci. USA 102 (2005), 14040–14045.
34. Lenk, R., Penman, S., The cytoskeletal framework and poliovirus metabolism. Cell 16 (1979), 289–301.
35. Leopold, P.L., Pfister, K.K., Viral strategies for intracellular trafficking: motors and microtubules. Traffic 7 (2006), 516–523.
36. Li, W., Shi, Z., Yu, M., Ren, W., Smith, C., Epstein, J.H., Wang, H., Crameri, G., Hu, Z., Zhang, H., Zhang, J., McEachern, J., Field, H., Daszak, P., Eaton, B.T., Zhang, S., Wang, L.F., Bats are natural reservoirs of SARS-like coronaviruses. Science 310 (2005), 676–679.
37. Liu, C., Tang, J., Ma, Y., Liang, X., Yang, Y., Peng, G., Qi, Q., Jiang, S., Li, J., Du, L., Li, F., Receptor usage and cell entry of porcine epidemic diarrhea coronavirus. J. Virol. 89 (2015), 6121–6125.
38. Luby-Phelps, K., Cytoarchitecture and physical properties of cytoplasm: volume, viscosity, diffusion, intracellular surface area. Int Rev. Cytol. 192 (2000), 189–221.
39. Luftig, R.B., Does the cytoskeleton play a significant role in animal virus replication?. J. Theor. Biol. 99 (1982), 173–191.
40. Luftig, R.B., Weihing, R.R., Adenovirus binds to rat brain microtubules in vitro. J. Virol. 16 (1975), 696–706.
41. Miles, B.D., Luftig, R.B., Weatherbee, J.A., Weihing, R.R., Weber, J., Quantitation of the interaction between adenovirus types 2 and 5 and microtubules inside infected cells. Virology 105 (1980), 265–269.
42. Moffat, K., Knox, C., Howell, G., Clark, S.J., Yang, H., Belsham, G.J., Ryan, M., Wileman, T., Inhibition of the secretory pathway by foot-and-mouth disease virus 2 BCE protein is reproduced by coexpression of 2B with 2C, and the site of inhibition is determined by the subcellular location of 2C. J. Virol. 81 (2007), 1129–1139.
43. Muller, M.A., Raj, V.S., Muth, D., Meyer, B., Kallies, S., Smits, S.L., Wollny, R., Bestebroer, T.M., Specht, S., Suliman, T., Zimmermann, K., Binger, T., Eckerle, I., Tschapka, M., Zaki, A.M., Osterhaus, A.D., Fouchier, R.A., Haagmans, B.L., Drosten, C., Human coronavirus EMC does not require the SARS-coronavirus receptor and maintains broad replicative capability in mammalian cell lines. mBio, 3, 2012.
44. Nguyen, V.P., Hogue, B.G., Protein interactions during coronavirus assembly. J. Virol. 71 (1997), 9278–9284.
45. Nogales, E., Structural insights into microtubule function. Annu. Rev. Biochem. 69 (2000), 277–302.
46. Oostra, M., te Lintelo, E.G., Deijs, M., Verheije, M.H., Rottier, P.J., de Haan, C.A., Localization and membrane topology of coronavirus nonstructural protein 4: involvement of the early secretory pathway in replication. J. Virol. 81 (2007), 12323–12336.
47. Opstelten, D.J., Raamsman, M.J., Wolfs, K., Horzinek, M.C., Rottier, P.J., Envelope glycoprotein interactions in coronavirus assembly. J. Cell Biol. 131 (1995), 339–349.
48. Pasick, J.M., Kalicharran, K., Dales, S., Distribution and trafficking of JHM coronavirus structural proteins and virions in primary neurons and the OBL-21 neuronal cell line. J. Virol. 68 (1994), 2915–2928.
49. Payne, L.G., Kristensson, K., The effect of cytochalasin D and monensin on enveloped vaccinia virus release. Arch. Virol. 74 (1982), 11–20.
50. Pfefferle, S., Oppong, S., Drexler, J.F., Gloza-Rausch, F., Ipsen, A., Seebens, A., Muller, M.A., Annan, A., Vallo, P., Adu-Sarkodie, Y., Kruppa, T.F., Drosten, C., Distant relatives of severe acute respiratory syndrome coronavirus and close relatives of human coronavirus 229E in bats, Ghana. Emerg. Infect. Dis. 15 (2009), 1377–1384.
51. Ploubidou, A., Way, M., Viral transport and the cytoskeleton. Curr. Opin. Cell Biol. 13 (2001), 97–105.
52. Radtke, K., Dohner, K., Sodeik, B., Viral interactions with the cytoskeleton: a hitchhiker's guide to the cell. Cell Micro. 8 (2006), 387–400.
53. Raux, H., Flamand, A., Blondel, D., Interaction of the rabies virus P protein with the LC8 dynein light chain. J. Virol. 74 (2000), 10212–10216.
54. Risco, C., Muntion, M., Enjuanes, L., Carrascosa, J.L., Two types of virus-related particles are found during transmissible gastroenteritis virus morphogenesis. J. Virol. 72 (1998), 4022–4031.
55. Sakaguchi, T., Leser, G.P., Lamb, R.A., The ion channel activity of the influenza virus M2 protein affects transport through the Golgi apparatus. J. Cell Biol. 133 (1996), 733–747.
56. Sanlioglu, S., Benson, P.K., Yang, J., Atkinson, E.M., Reynolds, T., Engelhardt, J.F., Endocytosis and nuclear trafficking of adeno-associated virus type 2 are controlled by rac1 and phosphatidylinositol-3 kinase activation. J. Virol. 74 (2000), 9184–9196.
57. Satake, M., Luftig, R.B., Microtubule-depolymerizing agents inhibit Moloney murine leukaemia virus production. J. Gen. Virol. 58 (1982), 339–349.
58. 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. 279 (2004), 43661–43666.
59. Shi, Z., Hu, Z., A review of studies on animal reservoirs of the SARS coronavirus. Virus Res. 133 (2008), 74–87.
60. Simon, M., Johansson, C., Lundkvist, A., Mirazimi, A., Microtubule-dependent and microtubule-independent steps in Crimean-Congo hemorrhagic fever virus replication cycle. Virology 385 (2009), 313–322.
61. Sodeik, B., Mechanisms of viral transport in the cytoplasm. Trends Microbiol. 8 (2000), 465–472.
62. Sodeik, B., Ebersold, M.W., Helenius, A., Microtubule-mediated transport of incoming herpes simplex virus 1 capsids to the nucleus. J. Cell Biol. 136 (1997), 1007–1021.
63. Suikkanen, S., Aaltonen, T., Nevalainen, M., Valilehto, O., Lindholm, L., Vuento, M., Vihinen-Ranta, M., Exploitation of microtubule cytoskeleton and dynein during parvoviral traffic toward the nucleus. J. Virol. 77 (2003), 10270–10279.
64. Thyrock, A., Ossendorf, E., Stehling, M., Kail, M., Kurtz, T., Pohlentz, G., Waschbusch, D., Eggert, S., Formstecher, E., Muthing, J., Dreisewerd, K., Kins, S., Goud, B., Barnekow, A., A new Mint1 isoform, but not the conventional Mint1, interacts with the small GTPase Rab6. PLoS One, 8, 2013, e64149.
65. Trincone, A., Schwegmann-Wessels, C., Looking for a needle in a haystack: cellular proteins that may interact with the tyrosine-based sorting signal of the TGEV S protein. Virus Res. 202 (2015), 3–11.
66. Varnum, S.M., Streblow, D.N., Monroe, M.E., Smith, P., Auberry, K.J., Pasa-Tolic, L., Wang, D., Camp, D.G. 2nd, Rodland, K., Wiley, S., Britt, W., Shenk, T., Smith, R.D., Nelson, J.A., Identification of proteins in human cytomegalovirus (HCMV) particles: the HCMV proteome. J. Virol. 78 (2004), 10960–10966.
67. 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. 15 (1996), 2020–2028.
68. Verheije, M.H., Raaben, M., Mari, M., Te Lintelo, E.G., Reggiori, F., van Kuppeveld, F.J., Rottier, P.J., de Haan, C.A., Mouse hepatitis coronavirus RNA replication depends on GBF1-mediated ARF1 activation. PLoS Pathog., 4, 2008, e1000088.
69. Verkman, A.S., Solute and macromolecule diffusion in cellular aqueous compartments. Trends Biochem. Sci. 27 (2002), 27–33.
70. 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 11 (2011), 64–80.
71. Wang, M.Q., Kim, W., Gao, G., Torrey, T.A., Morse, H.C. 3rd, De Camilli, P., Goff, S.P., Endophilins interact with Moloney murine leukemia virus Gag and modulate virion production. J. Biol., 3, 2003, 4.
72. 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. 82 (2008), 2765–2771.
73. Woo, P.C., Lau, S.K., Huang, Y., Yuen, K.Y., Coronavirus diversity, phylogeny and interspecies jumping. Exp. Biol. Med. 234 (2009), 1117–1127.
74. Ye, G.J., Vaughan, K.T., Vallee, R.B., Roizman, B., The herpes simplex virus 1 U(L)34 protein interacts with a cytoplasmic dynein intermediate chain and targets nuclear membrane. J. Virol. 74 (2000), 1355–1363.
75. Zhang, X., Shi, H., Chen, J., Shi, D., Dong, H., Feng, L., Identification of the interaction between vimentin and nucleocapsid protein of transmissible gastroenteritis virus. Virus Res. 200 (2015), 56–63.
76. 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., 11, 2013, 31.
77. Zhao, S., Gao, J., Zhu, L., Yang, Q., Transmissible gastroenteritis virus and porcine epidemic diarrhoea virus infection induces dramatic changes in the tight junctions and microfilaments of polarized IPEC-J2 cells. Virus Res. 192 (2014), 34–45.