Targeting of moloney murine leukemia virus gag precursor to the site of virus budding

Journal of Cell Biology

Volumn 135, Issue 6 II, 1996, Pages 1841-1852

  Suomalainen, Maarit ^a,c   Hultenby, Kjell ^b   Garoff, Henrik ^a  

^a Department of Bioscience at Novum ^*  (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

^c UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

MONENSIN; VIRUS PROTEIN;

ARTICLE; CELL FRACTIONATION; CELL MEMBRANE; CELL SURFACE; CYTOPLASM; DNA VIRUS; LIPOPROTEIN BLOOD LEVEL; MEMBRANE VESICLE; MURINE LEUKEMIA VIRUS; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; RETROVIRUS; SEMLIKI FOREST ALPHAVIRUS;

ANTIVIRAL AGENTS; BIOLOGICAL TRANSPORT; BREFELDIN A; CELL MEMBRANE; COLD; CYCLOPENTANES; ENDOPEPTIDASES; GENE EXPRESSION REGULATION, VIRAL; GENE PRODUCTS, GAG; GENOME, VIRAL; IONOPHORES; KINETICS; MICROSCOPY, ELECTRON; MOLONEY MURINE LEUKEMIA VIRUS; MONENSIN; PROTEIN PRECURSORS; RECOMBINANT PROTEINS; SEMLIKI FOREST VIRUS; SUBCELLULAR FRACTIONS; VIRUS REPLICATION;

EID: 0030446526     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.135.6.1841     Document Type: Article

References (67)

1. Aliperti, G., and M.J. Schlesinger. 1978. Evidence for an autoprotease activity of Sindbis virus capsid protein. Virology. 90:366-369.
2. Allison, S.L., K. Stadier, C.W. Mandl, C. Kunz, and F.X. Heinz. 1995. Synthesis and secretion of recombinant tick-borne encephalitis virus protein E in soluble and particulate form. J. Virol. 69:5816-5820.
3. Braakman, I., J. Helenius, and A. Helenius. 1992. Role of ATP and disulphide bonds during protein folding in the endoplasmic reliculum. Nature (Lond.). 356:260-262.
4. Brew, K., J. Shaper, K.W.Q. Olsen, I.O. Trayer, and R.L. Hill. 1975. Cross-linking of the components of lactose synthctase with dimethylpimelimidate. J. Biol. Chem. 250:1434-1444.
5. Bruss, V., and D. Ganem. 1991. The role of envelope proteins in hepatitis B virus assembly. Proc. Natl. Acad. Sci. USA. 88:1059-1063.
6. Bryant, M. L., and L. Ratner. 1990. Myristylation-dependent replication and assembly of Human immunodeficiency virus 1. Proc. Natl. Acad. Sci. USA. 87:523-527.
7. Collawn, J.F., M. Stangel, L.A. Kuhn, V. Esekogwu, S. Jing, I.S. Trowbridge, and J.A. Tainer. 1990. Transferrin receptor internalization sequence YXRF implicates a light turn as the structural recognition motif for endocytosis. Cell. 63:1061-1072.
8. de Curtis, I., and K. Simons. 1988. Dissection of Semliki Forest virus glycoprotein delivery from the trans-Golgi network to the cell surface in permeabilized BHK cells. Proc. Natl. Acad. Sci. USA. 85:8052-8056.
9. Delchambre, M., D. Gheysen, D. Thines, C. Thiriart, E. Jacobs, E. Verdin, M. Horth, A. Burny, and F. Bex. 1989. The GAG precursor of Simian Immunodeficiency virus assembles into virus-like particles. EMBO (Eur. Mol. Biol. Organ.) J. 8:2653-2660.
10. Devaney, E., and K. E. Howell. 1985. Immuno-isolation of a plasma membrane fraction from the Fao cell. EMBO (Eur. Mol. Biol. Organ.) J. 4:3123-3130.
11. Donaldson, J.G., D. Finazzi, and R.D. Klausner. 1992. Brefeldin A inhibits Golgi-catalyzed exchange of guanine nucleotide onto ARF proteins. Nature (Lond.). 360:350-352.
12. Gheysen, D., E. Jacobs, F. de Frosta, C. Thiriart, M. Francotte, D. Thines, and M. De Wilde. 1989. Assembly and release of HIV-1 precursor Pr55gag virus-like particles from recombinant Baculovirus-infected cells. Cell. 59:103-112.
13. Gielkens, A. L. J., M. H. L. Salden, and H. Bloemendal. 1974. Virus-specific messenger RNA on free and membrane-bound polyribosomes from cells infected with Rauscher leukemia virus. Proc. Natl. Acad. Sci. USA. 71:1093-1097.
14. Gielkens, A.L.J., D. Van Zaane, H.P.J. Bloemers, and H. Bloemendal. 1976. Synthesis of Rauscher murine leukemia virus-specific polypeptides in vitro. Proc. Natl. Acad. Sci. USA. 73:356-360.
15. Griffiths, G., and K. Simons. 1986. The trans-Golgi Network: sorting at the exit site of the Golgi complex. Science (Wash. DC).. 234:438-443.
16. Griffiths, G., P. Quinn, and G. Warren. 1983. Dissection of the Golgi complex. I. Monensin inhibits the transport of viral membrane proteins from medial to trans-Golgi cisternae in baby hamster kidney cells infected with Semliki Forest virus. J. Cell Biol. 96:835-850.
17. Hansen, M., L. Jelinek, R. S. Jones, J. Slegeman-Olsen, and E. Barklis. 1993. Assembly and composition of intracellular particles formed by Moloney murine leukemia virus. J. Virol. 67:5163-5174.
18. Hansen, M., L. Jelinek, S. Whiting, and E. Barklis. 1990. Transport and assembly of gag proteins into Moloney murine leukemia virus. J. Virol. 64:5306-5316.
19. Hare, J.F., and E. Lee. 1989. Metabolic behavior of cell surface biotinylated proteins. J. Cell Biol. 28:574-580.
20. Helms, J.B., and J.E. Rothman. 1992. Inhibition by brefeldin A of a Golgi membrane enzyme that catalyzed exchange of guanine nucleotide bound to ARF. Nature (Lond.).. 360:352-354.
21. Johnson, D.R., R.S. Bhatnagar, L.J. Knoll, and J.I. Gordon. 1994. Genetic and biochemical studies of protein N-myristylation. Annu. Rev Biochem. 63:869-914.
22. Kääriäinen, L., K. Simons, and C.-H. von Bonsdorff. 1969. Studies in subviral components of Semliki Forest virus. Annu. Med. Exp. Biol. Fenn. 47:235-248.
23. Klausner, R.D., J.G. Donaldson, and J. Lippincott-Schwartz. 1992. Brefeldin A: insights into the control of membrane traffic and organelle structure. J. Cell Biol. 116:1071-1080.
24. Konishi, E., S. Pincus, E. Paoletti, W.W. Laegreid, R.E. Shope, and P.W. Mason. 1992. Mice immunized with a subviral particle containing the Japanese encephalitis virus prM/M and E proteins are protected from lethal JEV infection. Virology. 188:714-720.
25. Krijnse-Locker, J., M. Ericsson, P.J.M. Rottier, and G. Griffiths. 1994. Characterization of the budding compartment of Mouse Hepatitis virus: evidence that transport from RER to the Golgi complex requires only one vesicular transport step. J. Cell Biol. 124:55-70.
26. Krishna, N.K., R.A. Weldon, and J.W. Wills. 1996. Transport and processing of the Rous sarcoma virus Gag protein in the endoplasmic reticulum. J. Virol. 70:1570-1579.
27. Lahtinen, U., B. Dahllöf, and J. Saraste. 1992. Characterization of a 58 kDa cis-Golgi protein in pancreatic exocrine cells. J. Cell Sci. 103:321-333.
28. V-STC). Proc. Natl. Acad. Sci. USA. 78:1624-1628.
29. Liljeström, P., and H. Garoff. 1991. Internally located cleavable signal sequences direct the formation of Semliki Forest virus membrane proteins from a polyprotein precursor. J. Virol. 65:147-154.
30. Liljestrom, P., and H. Garoff. 1991. A new generation of animal cell expression vectors based on the Semliki Forest virus replicon. Bio/Technology. 9:1356-1361.
31. Lisanti, M.P., A. Le Bivic, M. Sargiacomo, and E. Rodriguez-Boulan. 1989. Steady-slate distribution and biogenesis of endogenous Madin-Darby canine kidney glycoproteins: evidence for intracellular sorting and polarized cell surface delivery. J. Cell Biol. 109:2117-2127.
32. Lodge, R., H. Göttlinger, D. Gabuzda, E.A. Cohen, and G. Lemay. 1994. The intracytoplasmic domain of gp41 mediates polarized budding of Human immunodeficiency virus type 1 in MDCK cells. J. Virol. 68:4857-4861.
33. Lopez, S., J.-S. Yao, R.J. Kuhn, E.G. Strauss, and J.H. Strauss. 1994. Nucleocapsid-glycoprotein interactions required for assembly of alphaviruses. J. Virol. 68:1316-1323.
34. Mason, P.W., S. Pincus, M.J. Fournier, T.L. Mason, R.E. Shope, and E. Paoletti. 1991. Japanese Encephalitis virus-vaccinia recombinants produce paniculate forms of the structural membrane proteins and induce high levels of protection against JEV infection. Virology. 180:294-305.
35. McLaughlin, S., and A. Aderem. 1995. The myristoyl-electrostatic switch: a modulator of reversible protein-membrane interactions. TIBS. 20:272-276.
36. Mebatsion, T., M. König, and K.-K. Conzelmann. 1996. Budding of rabies virus particles in the absence of the spike glycoprotein. Cell. 84:941-951.
37. Melancon, P., and H. Garoff. 1987. Processing of the Semliki Forest virus structural polyprotein: role of the capsid protease. J. Virol. 61:1301-1309.
38. Neefjes, J.J., T. Henegveld, O. Toi, and H.L. Ploegh. 1990. Intracellular interactions of transferrin and its receptor during biosynthesis. J. Cell Biol. 111:1383-1392.
39. Op den Kamp, J.A.F. 1979. Lipid asymmetry of membranes. Annu. Rev. Biochem. 48:47-71.
40. Orci, L., B.S. Click, and J.E. Rothman, 1986. A new type of coaled vesicular carrier that appears not to contain clathrin: is possible role in protein transport within the Golgi stack. Cell. 46:171-184.
41. Owens, R.J., J.W. Duhay, E. Hunter, and R.W. Compans. 1991. Human immunodeficiency virus envelope protein determines the site of virus release in polarized epithelial cells. Proc. Natl. Acad. Sci. USA. 88:3987-3991.
42. Pal, R., R.C. Gallo, and M.G. Sarngadharan. 1988. Processing of the structural proteins of human immunodeficiency virus type 1 in the presence of monensin and cerulenin. Proc. Natl. Acad. Sci. USA. 85:9283-9286.
43. Pal, R., S. Mumbauer, G.M. Hoke, A. Takatsuki, and M.G. Sarngadharan. 1991. Brefeldin A inhibits the processing and secretion of envelope glycoproteins of human immunodeficiency virus type 1. AIDS Res. Human Retrovir. 7:707-712.
44. 2-terminal sequence of the avian oncovirus Gag precursor polyprolein (Pr76gag). Virology. 91:423-433.
45. Peranen, J., K. Takkinen, N. Kalkkinen, and L. Kääriäinen. 1988. Semliki Forest virus-specific non-structural protein nsP3 is a phosphoprolein. J. Gen. Virol. 69:2165-2178.
46. Pettersson, R.F. 1991. Protein localisation and virus assembly at intracellular membranes. Curr. Top. Microbiol. & Immunol. 170:67-110.
47. Rein, A., M. McClure, N. Rice, R. Luftig, and A. Schultz. 1986. Myristylation site in Pr65gag is essential for virus particle formation by Moloney murine leukemia virus. Proc. Natl. Acad. Sci. USA. 83:7246-7250.
48. Rhee, S., H. Hui, and E. Hunter. 1990. Preassembled eapsids of type D retroviruses contain a signal sufficient for targeting specifically to the plasma membrane. J. Virol. 64:3844-3852.
49. Saraste, J., G.E. Palade, and M. Gist Farquhar. 1986. Temperature-sensitive steps in the transport of secretory proteins through the Golgi complex in exocrine pancreatic cells. Proc. Natl. Acad. Sci. USA. 83:6425-6429.
50. Simon, K., V.R. Lingappa, and D. Ganem. 1988. Secreted Hepatitis B surface antigen polypeptides are derived from a transmembrane precursor. J. Cell Biol. 107:2163-2168.
51. Sjoberg, E.M., M. Suomalainen, and H. Garoft. 1994. A significantly improved Semliki Forest virus expression system based on translation enhancer segments from the viral eapsid gene. Bio/Technology. 12:1127-1131.
52. St. Johnston, D. 1995. The intracellular localization of messenger RNAs. Cell. 81:161-170.
53. Suomalainen, M., and H. Garoff. 1994. Incorporation of homologous and heterologous proteins into the envelope of Moloney murine leukemia virus. J. Virol. 68:4879-4889.
54. Suomalainen, M., P. Liljeströ, and H. Garoff. 1992. Spike protein-nucleocapsid interactions drive the hudding of alphaviruses. J. Virol. 66:4737-4747.
55. Tartakoff, A.M. 1983. Pertubation of vesicular traffic with the carboxylic ionophore monensin. Cell. 32:1026-1028.
56. Towler, D.A., J.I. Gordon, S.P. Adams, and L. Glaser. 1988. The biology and enzymology of eukaryotic protein acylation. Annu. Rev. Biochem. 57:69-99.
57. van Meer, G. 1989. Lipid traffic in animal cells. Annu. Rev. Cell Biol. 5:247-275.
58. Vennema, H., G.-J. Godeke, J.W.A. Rossen, W.F. Voorhout, M.C. Horzinck, D.-J.E. Opstelten, and P.J.M. Rottier. 1996. Nucleocapsid-independent assembly of coronavirus-like particles by co-expression of viral envelope protein genes. EURO (Eur. Mol. Biol. Organ.) J. 15:2020-2028.
59. Wahlberg, J.M., W.A. Boere, and H. Garoff. 1989. The helerodimeric association between the membrane proteins of Semliki Forest virus changes its sensitivity to mildly acidic pH during virus maturation. J. Virol. 63:4991-4997.
60. Wilhelm, J.E., and R.D. Vale. 1993. RNA on the move: the RNA localisation pathway. J. Cell Biol. 123:269-274.
61. Wills, J.W., and R.C. Craven. 1991. Form, function, and use of relroviral Gag proteins. AIDS. 5:639-654.
62. Wills, J.W., R.C. Craven, and J.A. Achacoso. 1989. Creation and expression of myristylated forms of Rous sarcoma virus Gag protein in mammalian cells. J. Virol. 63:4331-4343.
63. Yamshchikov, V.F., and R.W. Compans. 1993. Regulation of the late events in flavivirus protein processing and maturation. Virology. 192:38-51.
64. Yuan, X., X. Yu, T.-H. Lee, and M. Essex. 1993. Mutations in the N-terminal region of Human immunodeficiency virus type I matrix protein block intracellular transport of the Gag precursor. J. Virol. 67:6387-6394.
65. Zhao, H., B. Lindqvist, H. Garoff, A. Salminen, C.-H. von Bonsdorff, and P. Liljeström. 1994. A tyrosine-based motif in the cytoplasmic domain of the alphavirus envelope protein is essential lor budding. EMBO (Eur. Mol. Biol. Organ.) J. 13:4204-4211.
66. Zhou, W., L.J. Parent, J.W. Wills, and M.D. Resh. 1994. Identification of a membrane-binding domain within the amino-terminal region of human immunodeficiency virus type 1 Gag protein which interacts with acidic phospholipids. J. Virol. 68:2556-2569.
67. Ziemiecki, A., H. Garoff, and K. Simons. 1980. Formation of the Semliki Forest virus membrane glycoprotein complexes in the infected cell. J. Gen. Virol. 50:111-123.