Palmitoylation of the murine leukemia virus envelope glycoprotein transmembrane subunits

Virology

Volumn 221, Issue 1, 1996, Pages 87-97

  Yang, Chinglai ^a,b   Compans, Richard W ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROXYLAMINE; MEMBRANE PROTEIN; MERCAPTOETHANOL; PALMITIC ACID; PROTEIN PRECURSOR; PROTEIN SUBUNIT; VIRUS ENVELOPE PROTEIN; VIRUS GLYCOPROTEIN;

ACYLATION; ARTICLE; CELL LINE; CONTROLLED STUDY; GENE MUTATION; HUMAN; HUMAN CELL; HYDROLYSIS; ISOTOPE LABELING; MURINE LEUKEMIA VIRUS; NONHUMAN; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN MODIFICATION; SITE DIRECTED MUTAGENESIS; THIN LAYER CHROMATOGRAPHY; VIRUS RECOMBINANT;

EID: 0030198535     PISSN: 00426822     EISSN: None     Source Type: Journal    
DOI: 10.1006/viro.1996.0355     Document Type: Article

References (54)

1. Alvarez, E., Girones, N., and Davis, R. J. (1990). Inhibition of the receptor-mediated endocytosis of diferric transferrin is associated with the covalent modification of the transferrin receptor with palmitic acid. J. Biol. Chem. 265, 16644-16655.
2. Bonatti, S., Migliaccio, G., and Simons, K. (1989). Palmitylation of viral membrane glycoprotein takes place after exit from the endoplasmic reticulum. J. Biol. Chem. 264, 12590-12595.
3. Brewer, C. B., and Roth, M. G. (1991). A single amino acid change in the cytoplasmic domain alters the polarized delivery of influenza virus hemagglutinin. J. Cell Biol. 114, 413-421.
4. Cadwallader, K. A., Paterson, H., MacDonald, S. G., and Hancock, J. F. (1994). N-terminally myristoylated Ras proteins require palmitoylation or a polybasic domain for plasma membrane localization. Mol. Cell. Biol. 14, 4722-4730.
5. Casey, P. J. (1995). Protein lipidation in cell signaling. Science 268, 221-225.
6. Crise, B., and Rose, J. K. (1992). Identification of palmitoylation sites on CD4, the human immunodeficiency virus receptor. J. Biol. Chem. 267, 13593-13597.
7. Dickson, C., Eisenmann, R., Fan, H., Hunter, E., and Teich, N. (1982). Protein biosynthesis and assembly. In "RNA Tumor Viruses" (R. A. Weiss, N. Teich, H. E. Varmus, and J. M. Coffin, Eds.), pp. 513-648. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
8. Eason, M. G., Jacinto, M. T., Theiss, C. T., and Liggett, S. B. (1994). The palmitoylated cysteine of the cytoplasmic tail of a2A-adrenergic receptors confers subtype-specific agonist-promoted downregulation. Proc. Natl. Acad. Sci. USA 91, 11178-11182.
9. Fuerst, T. R., Niles, E. G., Studier, F. W., and Moss, B. (1986). Eukaryotic transient-expression system based on recombinant vaccinia virus that synthesizes bacteriophage T7 RNA polymerase. Proc. Natl. Acad. Sci. USA 83, 8122-8126.
10. Gallaher, W. R. (1987). Detection of a fusion peptide sequence in the transmembrane protein of the human immunodeficiency virus. Cell 50, 327-328.
11. Gebhardt, A., Bosch, J. V., Ziemiecki, A., and Friis, R. R. (1984). Rous sarcoma virus p19 and gp35 can be chemically crosslinked to high molecular weight complexes. J. Mol. Biol. 174, 297-317.
12. Green, N., Shinnick, T. M., Witte, O., Ponticelli, A., Sutcliffe, J. G., and Lerner, R. A. (1981). Sequence-specific antibodies show that maturation of Moloney leukemia virus envelope polyprotein involves removal of a COOH-terminal peptide. Proc. Natl. Acad. Sci. USA 78, 6023-6027.
13. Hackett, M., Guo, L., Shabanowitz, Z., Hunt, D. F., and Hewlett, E. G. (1994). Internal lysine palmitoylation in adenylate cyclase toxin from Bordetella pertussis. Science 266, 433-435.
14. Hallenberger, S., Bosch, V., Angliker, H., Shaw, E., Klenk, H.-D., and Garten, W. (1992). Inhibition of furin-mediated cleavage activation of HIV-1 glycoprotein gp160. Nature 360, 358-361.
15. Ivanova, L., and Schlesinger, M. J. (1993). Site-directed mutations in the Sindbis virus E2 glycoprotein identify palmitoylation sites and affect virus budding. J. Virol. 67, 2546-2551.
16. James, G., and Olson, E. N. (1990). Fatty acylated proteins as components of intracellular signaling pathways. Biochemistry 29, 2623-2634.
17. Kaufman, J. R., Krangel, M. S., and Strominger, J. L. (1984). Cysteines in the transmembrane region of major histocompatibility complex antigens are fatty acylated via thioester bonds. J. Biol. Chem. 259, 7230-7238.
18. Koenig, B., Arendt, A., McDowell, J. H., Kahlert, M., Hargrave, P. A., and Hofman, K. P. (1989). Three cytoplasmic loops of rhodopsin interact with transducin. Proc. Natl. Acad. Sci. USA 86, 6878-6882.
19. Kozarsky, K., Penman, M., Basiripour, L., Haseltine, W., Sodroski, J., and Krieger, M. (1989). Glycosylation and processing of the human immunodeficiency virus type 1 envelope protein. J. AIDS 2, 163-169.
20. Kunkel, T. A. (1985). Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc. Natl. Acad. Sci. USA 82, 488-492.
21. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 277, 680-685.
22. McGlade, C. J., Tremblay, M. L., Yee, S.-P., Ross, R., and Branton, P. E. (1987). Acylation of the 176R (19-kilodalton) early region 1B protein of human adenovirus type-5. J. Virol. 61, 3227-3234.
23. Morrison, T., and Portner, A. (1991). Structure, function, and intracellular processing of the glycoproteins of Paramyxoviridae. In "The Paramyxoviruses." Plenum, New York.
24. Mumby, S. M., Kleuss, C., and Gilman, A. G. (1994). Receptor regulation of G-protein palmitoylation. Proc. Natl. Acad. Sci. USA 91, 2800-2804.
25. Naeve, C. W., and Williams, D. (1990). Fatty acids on the A/Japan/305/ 57 influenza virus hemagglutinin have a role in membrane fusion. EMBO J. 9, 3857-3866.
26. Naim, H. Y., Amarneh, B., Ktistakis, N. T., and Roth, M. G. (1992). Effects of altering palmitylation sites on biosynthesis and function of the influenza virus hemagglutinin. J. Virol. 66, 7585-7588.
27. O'Dowd, B. F., Hnatowich, M., Caron, M. G., Lefkowitz, R. J., and Bouvier, M. (1989). Palmitoylation of the human b2-adrenergic receptor. J. Biol. Chem. 264, 7564-7569.
28. Oliff, A., Linemeyer, D., Ruscetti, S., Lowe, R., Lowy, D. R., and Scolnick, E. (1980). Subgenomic fragment of molecularly cloned Friend murine leukemia virus DNA contains the gene(s) responsible for Friend murine leukemia virus-induced diseases. J. Virol. 35, 924-936.
29. Owens R. J., Burke, C., and Rose J. K. (1994). Mutations in the membrane-spanning domain of the human immunodeficiency virus envelope glycoprotein that affect fusion activity. J. Virol. 68, 570-574.
30. lck. J. Biol. Chem. 268, 8669-8674.
31. Pinter, A., and Honnen, W. J. (1988). O-linked glycosylation of retroviral envelope gene products. J. Virol. 62, 1016-1021.
32. Ragheb, J. A., and Anderson, W. F. (1994). pH-independent murine leukemia virus ecotropic envelope-mediated cell fusion: Implications for the role of the R peptide and p12E TM in viral entry. J. Virol. 68, 3220-3231.
33. Rein, A., Mirro, J., Gordon-Haynes, J. A., Ernst, S. M., and Nagashima, K. (1994). Function of the cytoplasmic domain of a retroviral transmembrane protein: p15E-p2E cleavage activates the membrane fusion capability of the murine leukemia virus Env protein. J. Virol. 68, 1773-1781.
34. Resh, M. D. (1994). Myristylation and palmitylation of Src family members: The fats of the matter. Cell 76, 411-413.
35. Rose, J. K., Adams, G. A., and Gallione, C. J. (1984). The presence of cysteine in the cytoplasmic domain of the vesicular stomatitis virus glycoprotein is required for palmitate addition. Proc. Natl. Acad. Sci. USA 81, 2050-2054.
36. Sanger, F., Nicklen, S., and Coulson, A. R. (1977). DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74, 5463-5468.
37. Schmidt, M. F. G., and Schlesinger, M. J. (1980). Relation of fatty acid attachment to the translation and maturation of vesicular stomatitis and Sindbis virus membrane glycoproteins. J. Biol. Chem. 255, 3334-3339.
38. Schmidt, M. F. G., and Lambrecht, B. (1985). On the structure of the acyl linkage and function of fatty acyl chains in the influenza virus haemagglutinin and the glycoproteins of Semliki Forest virus. J. Gen. Virol. 66, 2635-2647.
39. Schmidt, M., Schmidt, M. F. G., and Rott, R. (1988). Chemical identification of cysteine as palmitoylation site in a transmembrane protein (Semliki Forest virus E1). J. Biol. Chem. 263, 18635-18639.
40. Schmidt, M. F. G. (1989). Fatty acylation of proteins. Biochim. Biophys. Acta 988, 411-426.
41. Sefton, B. M., and Buss, J. E. (1987). The covalent modification of eukaryotic proteins with lipid. J. Cell Biol. 104, 1449-1453.
42. Simpson, D. A., and Lamb, R. A. (1992). Alterations to influenza virus hemagglutinin cytoplasmic tail modulate virus infectivity. J. Virol. 66, 790-803.
43. Spies, C. P., and Compans, R. W. (1994). Effects of cytoplasmic domain length on cell surface expression and syncytium-forming capacity of the simian immunodeficiency virus envelope glycoprotein. Virology 203, 8-19.
44. Spies, C. P., Ritter, G. D., Jr., Mulligan, M. J., and Compans, R. W. (1994). Truncation of the cytoplasmic domain of the simian immunodeficiency virus envelope glycoprotein alters conformation of the external domain. J. Virol. 68, 585-591.
45. Srinivas, R. V., and Compans, R. W. (1983). Membrane association and defective transport of spleen focus forming virus glycoproteins. J. Biol. Chem. 258, 14718-14724.
46. Stanley, P., Packman, L. C., Koyonakis, V., and Huges, C. (1994). Fatty acylation of two internal lysine residues required for the toxic activity of Escherichia coli hemolysin. Science 266, 1992-1996.
47. Sugrue, R. J., Belshe, R. B., and Hay, A. J. (1990). Palmitoylation of the influenza A virus M2 protein. Virology 179, 51-56.
48. Veit, M., Schmidt, M. F. G., and Rott, R. (1989). Different palmitoylation of paramyxovirus glycoproteins. Virology 168, 173-176.
49. Veit, M., Kretzschmar, E., Kuroda, K., Garten, W., Schmidt, M. F. G., Klenk, H.-D., and Rott, R. (1991). Site-specific mutagenesis identifies three cysteine residues in the cytoplasmic tail as acylation sites of influenza virus hemagglutinin. J. Virol. 65, 2491-2500.
50. Wedegaertner, P. B., Chu, D. H., Wilson, P. T., Leviz, M. J., and Bourne, H. R. (1993). Palmitoylation is required for signaling functions and membrane attachment of Gq alpha and Gs alpha. J Biol. Chem. 268, 25001-25008.
51. Willey, R. L., Bonifacino, J. S., Potts, B. J., Martin, M. A., and Klausner, R. D. (1988). Biosynthesis, cleavage and degradation of the human immunodeficiency virus 1 envelope glycoprotein gp160. Proc. Natl. Acad. Sci. USA 85, 9580-9584.
52. Witte, O. N., and Wirth, D. F. (1979). Structure of the murine leukemia virus envelope glycoprotein precursor. J. Virol. 29, 735-743.
53. Yang, C., and Compans, R. W. (1996). Analysis of the cell fusion activities of chimeric simian immunodeficiency virus-murine leukemia virus envelope proteins: Inhibitory effects of the R peptide. J. Virol. 70, 248-254.
54. Zurcher, T., Luo, G., and Palese, P. (1994). Mutations at palmitylation sites of the influenza virus hemagglutinin affect virus formation. J. Virol. 68, 5748-5754.