Transport of the intracisternal A-type particle Gag polyprotein to the endoplasmic reticulum is mediated by the signal recognition particle

Journal of Virology

Volumn 77, Issue 11, 2003, Pages 6293-6304

  Fehrmann, Frauke ^a,d   Jung, Martin ^c   Zimmermann, Richard ^c   Kräusslich, Hans Georg ^a,b  

^a LEIBNIZ INSTITUTE FOR EXPERIMENTAL VIROLOGY   (Germany)

^b UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^c SAARLAND UNIVERSITY   (Germany)

^d NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENVELOPE PROTEIN; GAG PROTEIN; PROLACTIN; PROPROLACTIN; PROTEIN PRECURSOR; SIGNAL PEPTIDE; SIGNAL RECOGNITION PARTICLE; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; DEFECTIVE VIRUS; ENDOPLASMIC RETICULUM; FLOTATION; IN VITRO STUDY; INTRACELLULAR TRANSPORT; INTRACISTERNAL A TYPE PARTICLE; MEMBRANE BINDING; MICROSOME MEMBRANE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN INTERACTION; PROTEIN TRANSPORT; PROTEOLIPOSOME; RETROVIRUS; RNA TRANSLATION; SEDIMENTATION; SIGNAL TRANSDUCTION; VIRUS PARTICLE;

AMINO ACID SEQUENCE; ENDOPLASMIC RETICULUM; GENE PRODUCTS, GAG; GENES, INTRACISTERNAL A-PARTICLE; INTRACELLULAR MEMBRANES; MEMBRANE PROTEINS; MICROSOMES; MOLECULAR SEQUENCE DATA; POLYPROTEINS; PROTEIN BIOSYNTHESIS; PROTEOLIPIDS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECEPTORS, PEPTIDE; SIGNAL RECOGNITION PARTICLE;

EID: 0037955874     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.11.6293-6304.2003     Document Type: Article

References (76)

1. Adam, S. A., R. S. Marr, and L. Gerace. 1990. Nuclear protein import in permeabilized mammalian cells requires soluble cytoplasmic factors. J. Cell Biol. 111:807-816.
2. Anderson, D. J., K. E. Mostov, and G. Blobel. 1983. Mechanisms of integration of de novo-synthesized polypeptides into membranes: signal-recognition particle is required for integration into microsomal membranes of calcium ATPase and of lens MP26 but not of cytochrome b5. Proc. Natl. Acad. Sci. USA 80:7249-7253.
3. Aota, S., T. Gojobori, K. Shigesada, H. Ozeki, and T. Ikemura. 1987. Nucleotide sequence and molecular evolution of mouse retrovirus-like IAP elements. Gene 56:1-12.
4. Blobel, G., and B. Dobberstein. 1975. Transfer to proteins across membranes. II. Reconstitution of functional rough microsomes from heterologous components. J. Cell Biol. 67:852-862.
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., and L. Ratner. 1990. Myristoylation-dependent replication and assembly of human immunodeficiency virus 1. Proc Natl. Acad. Sci. USA 87:523-527.
7. Bucher, D. J., I. G. Kharitonenkov, J. A. Zakomirdin, V. B. Grigoriev, S. M. Klimenko, and J. F. Davis. 1980. Incorporation of influenza virus M-protein into liposomes. J. Virol. 36:586-590.
8. Chong, L. D., and J. K. Rose. 1994. Interactions of normal and mutant vesicular stomatitis virus matrix proteins with the plasma membrane and nucleocapsids. J. Virol. 68:441-447.
9. Chong, L. D., and J. K. Rose. 1993. Membrane association of functional vesicular stomatitis virus matrix protein in vivo. J. Virol. 67:407-414.
10. Connolly, T., and R. Gilmore. 1989. The signal recognition particle receptor mediates the GTP-dependent displacement of SRP from the signal sequence of the nascent polypeptide. Cell 57:599-610.
11. Corsi, A. K., and R. Schekman. 1996. Mechanism of polypeptide translocation into the endoplasmic reticulum. J. Biol. Chem. 271:30299-30302.
12. Deshaies, R. J., S. L. Sanders, D. A. Feldheim, and R. Schekman. 1991. Assembly of yeast Sec proteins involved in translocation into the endoplasmic reticulum into a membrane-bound multisubunit complex. Nature 349:806-808.
13. Deshaies, R. J., and R. Schekman. 1987. A yeast mutant defective at an early stage in import of secretory protein precursors into the endoplasmic reticulum. J. Cell Biol. 105:633-645.
14. Dorner, A. J., F. Bonneville, R. Kriz, K. Kelleher, K. Bean, and R. J. Kaufman. 1991. Molecular cloning and characterization of a complete Chinese hamster provirus related to intracisternal A particle genomes. J. Virol. 65:4713-4719.
15. Eisenberg, D. 1984. Three-dimensional structure of membrane and surface proteins. Annu. Rev. Biochem. 53:595-623.
16. Facke, M., A. Janetzko, R. L. Shoeman, and H. G. Krausslich. 1993. A large deletion in the matrix domain of the human immunodeficiency virus gag gene redirects virus particle assembly from the plasma membrane to the endoplasmic reticulum. J. Virol. 67:4972-4980.
17. Fehrmann, F., R. Welker, and H. G. Krausslich. 1997. Intracisternal A-type particles express their proteinase in a separate reading frame by translational frameshifting, similar to D-type retroviruses. Virology 235:352-359.
18. Fries, E., and J. E. Rothman. 1980. Transport of vesicular stomatitis virus glycoprotein in a cell-free extract. Proc. Natl. Acad. Sci. USA 77:3870-3874.
19. Fuller, S. D., T. Wilk, B. E. Gowen, H. G. Krausslich, and V. M. Vogt. 1997. Cryo-electron microscopy reveals ordered domains in the immature HIV-1 particle. Curr. Biol. 7:729-738.
20. Gorlich, D., E. Hartmann, S. Prehn, and T. A. Rapoport. 1992. A protein of the endoplasmic reticulum involved early in polypeptide translocation. Nature 357:47-52.
21. Gorlich, D., and T. A. Rapoport. 1993. Protein translocation into proteoliposomes reconstituted from purified components of the endoplasmic reticulum membrane. Cell 75:615-630.
22. Gottlinger, H. G., J. G. Sodroski, and W. A. Haseltine. 1989. Role of capsid precursor processing and myristoylation in morphogenesis and infectivity of human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. USA 86:5781-5785.
23. Gregoriades, A., and B. Frangione. 1981. Insertion of influenza M protein into the viral lipid bilayer and localization of site of insertion. J. Virol. 40:323-328.
24. 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.
25. Hauser, S., G. Bacher, B. Dobberstein, and H. Lutcke. 1995. A complex of the signal sequence binding protein and the SRP RNA promotes translocation of nascent proteins. EMBO J. 14:5485-5493.
26. Henderson, L. E., H. C. Krutzsch, and S. Oroszlan. 1983. Myristyl amino-terminal acylation of murine retrovirus proteins: an unusual post-translational proteins modification. Proc. Natl. Acad. Sci. USA 80:339-343.
27. High, S., and B. Dobberstein. 1991. The signal sequence interacts with the methionine-rich domain of the 54-kD protein of signal recognition particle. J. Cell Biol. 113:229-233.
28. Hill, C. P., D. Worthylake, D. P. Bancroft, A. M. Christensen, and W. I. Sundquist. 1996. Crystal structures of the trimeric human immunodeficiency virus type 1 matrix protein: implications for membrane association and assembly. Proc. Natl. Acad. Sci. USA 93:3099-3104.
29. Hull, J. D., R. Gilmore, and R. A. Lamb. 1988. Integration of a small integral membrane protein, M2, of influenza virus into the endoplasmic reticulum: analysis of the internal signal-anchor domain of a protein with an ectoplasmic NH2 terminus. J. Cell Biol. 106:1489-1498.
30. Krausslich, H. G., and R. Welker. 1996. Intracellular transport of retroviral capsid components. Curr. Top. Microbiol. Immunol. 214:25-63.
31. Kretzschmar, E., M. Bui, and J. K. Rose. 1996. Membrane association of influenza virus matrix protein does not require specific hydrophobic domains or the viral glycoproteins. Virology 220:37-45.
32. Kuff, E. L., and K. K. Lueders. 1988. The intracisternal A-particle gene family: structure and functional aspects. Adv. Cancer Res. 51:183-276.
33. Lenard, J., and R. Vanderoef. 1990. Localization of the membrane-associated region of vesicular stomatitis virus M protein at the N terminus, using the hydrophobic, photoreactive probe 125I-TID. J. Virol. 64:3486-3491.
34. Li, P., J. Beckwith, and H. Inouye. 1988. Alteration of the amino terminus of the mature sequence of a periplasmic protein can severely affect protein export in Escherichia coli. Proc. Natl. Acad. Sci. USA 85:7685-7689.
35. 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,
36. Luftig, R. B., and L. D. Lupo. 1994. Viral interactions with the host-cell cytoskeleton: the role of retroviral proteases. Trends Microbiol. 2:178-182.
37. Meyer, D. I., E. Krause, and B. Dobberstein. 1982. Secretory protein translocation across membranes-the role of the "docking protein". Nature 297:647-650.
38. Mietz, J. A., Z. Grossman, K. K. Lueders, and E. L. Kuff. 1987. Nucleotide sequence of a complete mouse intracisternal A-particle genome: relationship to known aspects of particle assembly and function. J. Virol. 61:3020-3029.
39. Monier, S., P. Van Luc, G. Kreibich, D. D. Sabatini, and M. Adesnik. 1988. Signals for the incorporation and orientation of cytochrome P450 in the endoplasmic reticulum membrane. J. Cell Biol. 107:457-470.
40. Moss, B., O. Elroy-Stein, T. Mizukami, W. A. Alexander, and T. R. Fuerst. 1990. Product review. New mammalian expression vectors. Nature 348:91-92.
41. Muller, G., and R. Zimmermann. 1987. Import of honeybee prepromelittin into the endoplasmic reticulum: structural basis for independence of SRP and docking protein. EMBO J. 6:2099-2107.
42. Nguyen, D. H., and J. E. Hildreth. 2000. Evidence for budding of human immunodeficiency virus type 1 selectively from glycolipid-enriched membrane lipid rafts. J. Virol. 74:3264-3272.
43. Nilsson, I., P. Whitley, and G. von Heijne. 1994. The COOH-terminal ends of internal signal and signal-anchor sequences are positioned differently in the ER translocase. J. Cell Biol. 126:1127-1132.
44. Ogden, J. R., R. Pal, and R. R. Wagner. 1986. Mapping regions of the matrix protein of vesicular stomatitis virus which bind to ribonucleocapsids, liposomes, and monoclonal antibodies. J. Virol. 58:860-868.
45. Ono, A., and E. O. Freed. 2001. Plasma membrane rafts play a critical role in HIV-1 assembly and release. Proc. Natl. Acad. Sci. USA 98:13925-13930.
46. Ono, M., H. Toh, T. Miyata, and T. Awaya. 1985. Nucleotide sequence of the Syrian hamster intracisternal A-particle gene: close evolutionary relationship of type A particle gene to types B and D oncovirus genes. J. Virol. 55:387-394.
47. Panzner, S., L. Dreier, E. Hartmann, S. Kostka, and T. A. Rapoport. 1995. Posttranslational protein transport in yeast reconstituted with a purified complex of Sec proteins and Kar2p. Cell 81:561-570.
48. Parent, L. J., C. B. Wilson, M. D. Resh, and J. W. Wills. 1996. Evidence for a second function of the MA sequence in the Rous sarcoma virus Gag protein. J. Virol. 70:1016-1026.
49. Parks, G. D., and R. A. Lamb. 1993. Role of NH2-terminal positively charged residues in establishing membrane protein topology. J. Biol. Chem. 268:19101-19109.
50. Parks, G. D., and R. A. Lamb. 1991. Topology of eukaryotic type II membrane proteins: importance of N-terminal positively charged residues flanking the hydrophobic domain. Cell 64:777-787.
51. Pietschmann, T., M. Heinkelein, M. Heldmann, H. Zentgraf, A. Rethwilm, and D. Lindemann. 1999. Foamy virus capsids require the cognate envelope protein for particle export. J. Virol. 73:2613-2621.
52. Rao, Z., A. S. Belyaev, E. Fry, P. Roy, I. M. Jones, and D. I. Stuart. 1995. Crystal structure of SIV matrix antigen and implications for virus assembly. Nature 378:743-747.
53. Rapoport, T. A., M. M. Rolls, and B. Jungnickel. 1996. Approaching the mechanism of protein transport across the ER membrane. Curr. Opin. Cell Biol. 8:499-504.
54. Rein, A., M. R. McClure, N. R. Rice, R. B. Luftig, and A. M. 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.
55. Reuss, F. U., and H. C. Schaller. 1991. cDNA sequence and genomic characterization of intracisternal A-particle-related retroviral elements containing an envelope gene. J. Virol. 65:5702-5709.
56. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual., 2 ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
57. Schatz, P. J., and J. Beckwith. 1990. Genetic analysis of protein export in Escherichia coli. Annu. Rev. Genet. 24:215-248.
58. Schlenstedt, G., G. H. Gudmundsson, H. G. Boman, and R. Zimmermann. 1990. A large presecretory protein translocates both cotranslationally, using signal recognition particle and ribosome, and post-translationally, without these ribonucleoparticles, when synthesized in the presence of mammalian microsomes. J. Biol. Chem. 265:13960-13968.
59. Schlenstedt, G., G. H. Gudmundsson, H. G. Boman, and R. Zimmermann. 1992. Structural requirements for transport of preprocecropinA and related presecretory proteins into mammalian microsomes. J. Biol. Chem. 267:24328-24332.
60. Szczesna-Skorupa, E., N. Browne, D. Mead, and B. Kemper. 1988. Positive charges at the NH2 terminus convert the membrane-anchor signal peptide of cytochrome P-450 to a secretory signal peptide. Proc. Natl. Acad. Sci. USA 85:738-742.
61. von Heijne, G. 1990. The signal peptide. J. Membr. Biol. 115:195-201.
62. von Heijne, G. 1985. Signal sequences. The limits of variation. J. Mol. Biol. 184:99-105.
63. von Heijne, G. 1986. Towards a comparative anatomy of N-terminal topogenic protein sequences. J. Mol. Biol. 189:239-242.
64. von Heijne, G., and Y. Gavel. 1988. Topogenic signals in integral membrane proteins. Eur. J. Biochem. 174:671-678.
65. Walter, P., and G. Blobel. 1981. Translocation of proteins across the endoplasmic reticulum III. Signal recognition protein (SRP) causes signal sequence-dependent and site-specific arrest of chain elongation that is released by microsomal membranes. J. Cell Biol. 91:557-561.
66. Walter, P., and G. Blobel. 1981. Translocation of proteins across the endoplasmic reticulum. II. Signal recognition protein (SRP) mediates the selective binding to microsomal membranes of in-vitro-assembled polysomes synthesizing secretory protein. J. Cell Biol. 91:551-556.
67. Walter, P., I. Ibrahimi, and G. Blobel. 1981. Translocation of proteins across the endoplasmic reticulum. I. Signal recognition protein (SRP) binds to in-vitro-assembled polysomes synthesizing secretory protein. J. Cell Biol. 91:545-550.
68. Walter, P., and A. E. Johnson. 1994. Signal sequence recognition and protein targeting to the endoplasmic reticulum membrane. Annu. Rev. Cell Biol. 10:87-119.
69. Watts, C., W. Wickner, and R. Zimmermann. 1983. M13 procoat and a pre-immunoglobulin share processing specificity but use different membrane receptor mechanisms. Proc. Natl. Acad. Sci. USA 80:2809-2813.
70. Welker, R., A. Janetzko, and H. G. Krausslich. 1997. Plasma membrane targeting of chimeric intracisternal A-type particle polyproteins leads to particle release and specific activation of the viral proteinase. J. Virol. 71:5209-5217.
71. Wickner, W., and M. R. Leonard. 1996. Escherichia coli preprotein translocase. J. Biol. Chem. 271:29514-29516.
72. Wilk, T., I. Gross, B. E. Gowen, T. Rutten, F. de Haas, R. Welker, H. G. Krausslich, P. Boulanger, and S. D. Fuller. 2001. Organization of immature human immunodeficiency virus type 1. J. Virol. 75:759-771.
73. Yamane, K., and S. Mizushima. 1988. Introduction of basic amino acid residues after the signal peptide inhibits protein translocation across the cytoplasmic, membrane of Escherichia coli. Relation to the orientation of membrane proteins. J. Biol. Chem. 263:19690-19696.
74. Zakowski, J. J., W. A. Petri, Jr., and R. R. Wagner. 1981. Role of matrix protein in assembling the membrane of vesicular stomatitis virus: reconstitution of matrix protein with negatively charged phospholipid vesicles. Biochemistry 20:3902-3907.
75. Zhao, H., B. Lindqvist, H. Garoff, C. H. von Bonsdorff, and P. Liljestrom. 1994. A tyrosine-based motif in the cytoplasmic domain of the alphavirus envelope protein is essential for budding. EMBO J. 13:4204-4211.
76. 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.