A lysine-methionine exchange in a coronavirus surface protein transforms a retention motif into an endocytosis signal

Biological Chemistry

Volumn 395, Issue 6, 2014, Pages 657-665

  Paul, André ^a   Trincone, Anna ^a   Siewert, Sandra ^a   Herrler, Georg ^a   Schwegmann Weßels, Christel ^a  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

Author keywords

protein sorting; protein transport; TGEV S protein; tyrosine based sorting signal; VSV G protein

Indexed keywords

BIOTIN; LYSINE; METHIONINE; THROMBOSPONDIN; VIRUS ENVELOPE PROTEIN; VITRONECTIN;

AMINO ACID TRANSPORT; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL SURFACE; CORONAVIRUS; CYTOPLASM; ENDOCYTOSIS; GLYCOSYLATION; IMMUNOPRECIPITATION; INTERNALIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MOTIF; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; TRANSMISSIBLE GASTROENTERITIS VIRUS; VESICULAR STOMATITIS VIRUS; WESTERN BLOTTING; GENETIC TRANSFECTION; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT;

CORONAVIRUS; ENDOCYTOSIS; LYSINE; METHIONINE; PROTEIN TRANSPORT; TRANSFECTION;

EID: 84899792545     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2013-0282     Document Type: Article

References (42)

1. Borroto, A., Lama, J., Niedergang, F., Dautry-Varsat, A., Alarcon, B., and Alcover, A. (1999). The CD3 epsilon subunit of the TCR contains endocytosis signals. J. Immunol. 163, 25-31.
2. Cathomen, T., Buchholz, C.J., Spielhofer, P., and Cattaneo, R. (1995). Preferential initiation at the second AUG of the measles virus F mRNA: a role for the long untranslated region. Virology 214, 628-632.
3. Delmas, B., Gelfi, J., L'Haridon, R., Vogel, L.K., Sjostrom, H., Noren, O., and Laude, H. (1992). Aminopeptidase N is a major receptor for the entero-pathogenic coronavirus TGEV. Nature 357, 417-420.
4. Enjuanes, L. and van der Zeijst, B.A. (1995). Molecular basis of transmissible gastroenteritis virus epidemiology. In: The Coronaviridae, S.G. Siddell, ed. (New York: Plenum Press), pp. 337-376.
5. Escors, D., Ortego, J., Laude, H., and Enjuanes, L. (2001). The membrane M protein carboxy terminus binds to transmissible gastroenteritis coronavirus core and contributes to core stability. J. Virol. 75, 1312-1324.
6. Fischer, F., Stegen, C.F., Masters, P.S., and Samsonoff, W.A. (1998). Analysis of constructed E gene mutants of mouse hepatitis virus confirms a pivotal role for E protein in coronavirus assembly. J. Virol. 72, 7885-7894.
7. Gallagher, T.M. and Buchmeier, M.J. (2001). Coronavirus spike proteins in viral entry and pathogenesis. Virology 279, 371-374.
8. Gebauer, F., Posthumus, W.P., Correa, I., Sune, C., Smerdou, C., Sanchez, C.M., Lenstra, J.A., Meloen, R.H., and Enjuanes, L. (1991). Residues involved in the antigenic sites of transmissible gastroenteritis coronavirus S glycoprotein. Virology 183, 225-238.
9. Godet, M., Rasschaert, D., and Laude, H. (1991). Processing and antigenicity of entire and anchor-free spike glycoprotein S of coronavirus TGEV expressed by recombinant baculovirus. Virology 185, 732-740.
10. Godet, M., Grosclaude, J., Delmas, B., and Laude, H. (1994). Major receptor-binding and neutralization determinants are located within the same domain of the transmissible gastroenteritis virus (coronavirus) spike protein. J. Virol. 68, 8008-8016.
11. Granger, B.L., Green, S.A., Gabel, C.A., Howe, C.L., Mellman, I., and Helenius, A. (1990). Characterization and cloning of lgp110, a lysosomal membrane glycoprotein from mouse and rat cells. J. Biol. Chem. 265, 12036-12043.
12. Hanika, A., Larisch, B., Steinmann, E., Schwegmann-Wessels, C., Herrler, G., and Zimmer, G. (2005). Use of influenza C virus glycoprotein HEF for generation of vesicular stomatitis virus pseudotypes. J. Gen. Virol. 86, 1455-1465.
13. Howe, C.L., Granger, B.L., Hull, M., Green, S.A., Gabel, C.A., Helenius, A., and Mellman, I. (1988). Derived protein sequence, oligosaccharides, and membrane insertion of the 120-kDa lysosomal membrane glycoprotein (lgp120): identification of a highly conserved family of lysosomal membrane glycoproteins. Proc. Natl. Acad. Sci. USA 85, 7577-7581.
14. Krijnse-Locker, J., Ericsson, M., Rottier, P.J., and Griffiths, G. (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.
15. Letourneur, F. and Klausner, R.D. (1992). A novel di-leucine motif and a tyrosine-based motif independently mediate lysosomal targeting and endocytosis of CD3 chains. Cell 69, 1143-1157.
16. Mallabiabarrena, A., Fresno, M., and Alarcon, B. (1992). An endoplasmic reticulum retention signal in the CD3 epsilon chain of the T-cell receptor. Nature 357, 593-596.
17. Mallabiabarrena, A., Jimenez, M.A., Rico, M., and Alarcon, B. (1995). A tyrosine-containing motif mediates ER retention of CD3-epsilon and adopts a helix-turn structure. EMBO J. 14, 2257-2268.
18. McBride, C.E., Li, J., and Machamer, C.E. (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.
19. Moll, M., Klenk, H.D., Herrler, G., and Maisner, A. (2001). A single amino acid change in the cytoplasmic domains of measles virus glycoproteins H and F alters targeting, endocytosis, and cell fusion in polarized Madin-Darby canine kidney cells. J. Biol. Chem. 276, 17887-17894.
20. Narayanan, K., Maeda, A., Maeda, J., and Makino, S. (2000). Characterization of the coronavirus M protein and nucleocapsid interaction in infected cells. J. Virol. 74, 8127-8134.
21. Nishimura, N. and Balch, W.E. (1997). A di-acidic signal required for selective export from the endoplasmic reticulum. Science 277, 556-558.
22. Nishimura, N., Bannykh, S., Slabough, S., Matteson, J., Altschuler, Y., Hahn, K., and Balch, W.E. (1999). A di-acidic (DXE) code directs concentration of cargo during export from the endoplasmic reticulum. J. Biol. Chem. 274, 15937-15946.
23. Nishimura, N., Plutner, H., Hahn, K., and Balch, W.E. (2002). The delta subunit of AP-3 is required for efficient transport of VSV-G from the trans-Golgi network to the cell surface. Proc. Natl. Acad. Sci. USA 99, 6755-6760.
24. Opstelten, D.J., Raamsman, M.J., Wolfs, K., Horzinek, M.C., and Rottier, P.J. (1995). Envelope glycoprotein interactions in coronavirus assembly. J. Cell Biol. 131, 339-349.
25. Ortego, J., Ceriani, J.E., Patino, C., Plana, J., and Enjuanes, L. (2007). Absence of E protein arrests transmissible gastroenteritis coronavirus maturation in the secretory pathway. Virology 368, 296-308.
26. Penzes, Z., Gonzalez, J.M., Calvo, E., Izeta, A., Smerdou, C., Mendez, A., Sanchez, C.M., Sola, I., Almazan, F., and Enjuanes, L. (2001). Complete genome sequence of transmissible gastroenteritis coronavirus PUR46-MAD clone and evolution of the purdue virus cluster. Virus Genes 23, 105-118.
27. Rasband, W.S. (1997-2014). ImageJ, U. S. National Institutes of Health, Bethesda, Maryland, USA, http://imagej.nih.gov/ij/.
28. Rohrer, J., Schweizer, A., Russell, D., and Kornfeld, S. (1996). The targeting of Lamp1 to lysosomes is dependent on the spacing of its cytoplasmic tail tyrosine sorting motif relative to the membrane. J. Cell Biol. 132, 565-576.
29. Schwegmann-Wessels, C., Zimmer, G., Laude, H., Enjuanes, L., and Herrler, G. (2002). Binding of transmissible gastroenteritis coronavirus to cell surface sialoglycoproteins. J. Virol. 76, 6037-6043.
30. Schwegmann-Wessels, C., Al-Falah, M., Escors, D., Wang, Z., Zimmer, G., Deng, H., Enjuanes, L., Naim, H.Y., and Herrler, G. (2004). 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, 43661-43666.
31. Schwegmann-Wessels, C., Ren, X., and Herrler, G. (2006). Intracellular transport of the S proteins of coronaviruses. Adv. Exp. Med. Biol. 581, 271-275.
32. Schwegmann-Wessels, C., Bauer, S., Winter, C., Enjuanes, L., Laude, H., and Herrler, G. (2011). The sialic acid binding activity of the S protein facilitates infection by porcine transmissible gastroenteritis coronavirus. Virol. J. 8, 435.
33. Sevier, C.S., Weisz, O.A., Davis, M., and Machamer, C.E. (2000). Efficient export of the vesicular stomatitis virus G protein from the endoplasmic reticulum requires a signal in the cytoplasmic tail that includes both tyrosine-based and di-acidic motifs. Mol. Biol. Cell 11, 13-22.
34. Stephens, E.B., Compans, R.W., Earl, P., and Moss, B. (1986). Surface expression of viral glycoproteins is polarized in epithelial cells infected with recombinant vaccinia viral vectors. EMBO J. 5, 237-245.
35. Thomas, D.C. and Roth, M.G. (1994). The basolateral targeting signal in the cytoplasmic domain of glycoprotein G from vesicular stomatitis virus resembles a variety of intracellular targeting motifs related by primary sequence but having diverse targeting activities. J. Biol. Chem. 269, 15732-15739.
36. Tooze, J., Tooze, S., and Warren, G. (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.
37. Traub, L.M. (2005). Common principles in clathrin-mediated sorting at the Golgi and the plasma membrane. Biochim. Biophys. Acta 1744, 415-437.
38. Traub, L.M. (2009). Tickets to ride: selecting cargo for clathrinregulated internalization. Nat. Rev. Mol. Cell. Biol. 10, 583-596.
39. Vennema, H., Godeke, G.J., Rossen, J.W., Voorhout, W.F., Horzinek, M.C., Opstelten, D.J., and Rottier, P.J. (1996). Nucleocapsidindependent assembly of coronavirus-like particles by co-expression of viral envelope protein genes. EMBO J 15, 2020-2028.
40. Wehland, J., Willingham, M.C., Gallo, M.G., and Pastan, I. (1982). The morphologic pathway of exocytosis of the vesicular stomatitis virus G protein in cultured fibroblasts. Cell 28, 831-841.
41. Winter, C., Schwegmann-Wessels, C., Neumann, U., and Herrler, G. (2008). The spike protein of infectious bronchitis virus is retained intracellularly by a tyrosine motif. J. Virol. 82, 2765-2771.
42. Zimmer, G., Budz, L., and Herrler, G. (2001). Proteolytic activation of respiratory syncytial virus fusion protein. Cleavage at two furin consensus sequences. J. Biol. Chem. 276, 31642-31650.