Structural analysis of membrane-bound retrovirus capsid proteins

EMBO Journal

Volumn 16, Issue 6, 1997, Pages 1199-1213

  Barklis, Eric ^a   McDermott, Jason ^a   Wilkens, Stephan ^b   Schabtach, Eric ^b   Schmid, M F ^c   Fuller, Stephen ^d   Karanjia, Sonya ^a   Love, Zachary ^a   Jones, Russell ^a   Rui, Yuanjui ^e   Zhao, Xiumin ^e   Thompson, David ^e  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b UNIVERSITY OF OREGON   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^e PURDUE UNIVERSITY   (United States)

Author keywords

Electron microscopy; Image analysis; Lipid monolayer; Retrovirus

Indexed keywords

CAPSID PROTEIN; CORE PROTEIN; ENVELOPE PROTEIN; GAG PROTEIN; LIPID; MEMBRANE PROTEIN; NICKEL; PHOSPHATIDYLCHOLINE;

ANIMAL CELL; ARTICLE; ATOMIC ABSORPTION SPECTROMETRY; CHELATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; LIPID MONOLAYER; MOLONEY LEUKEMIA ONCOVIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN STRUCTURE; RETROVIRUS; VIRUS ASSEMBLY; VIRUS PARTICLE;

AMINO ACID SEQUENCE; ANIMALS; CAPSID; CHELATING AGENTS; COS CELLS; CRYSTALLIZATION; GENE PRODUCTS, GAG; LIPIDS; MEMBRANES, ARTIFICIAL; MICROSCOPY, ELECTRON; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; MOLONEY MURINE LEUKEMIA VIRUS; NICKEL; RETROVIRIDAE PROTEINS; TRANSFECTION;

ANIMALIA; MIRIDAE; MOLONEY MURINE LEUKEMIA VIRUS; MURINAE; ONCOVIRINAE; UNIDENTIFIED RETROVIRUS;

EID: 0030987083     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.6.1199     Document Type: Article

References (64)

1. Avila-Sakar, A.J. and Chiu, W. (1996) Visualization of β sheets and side chain clusters in 2-dimensional periodic arrays of streptavidin on phospholipid monolayers by electron crystallography. Biophys. J., 70, 57-68.
2. Baldwin, J., Henderson, R., Beckman, E. and Zemlin, F. (1988) Images of purple membrane at 2.8 A° resolution obtained by cryo-electron microscopy. J. Mol. Biol., 202, 585-591.
3. Campbell, S. and Vogt, V. (1995) Self-assembly in vitro of purified CA-NC proteins from Rous sarcoma virus and human immunodeficiency virus type 1. J. Virol., 69, 6487-6497.
4. Celia, H., Hoermann, L., Schultz, P., Lebeau, L., Mallouh, V., Wigley, D., Wang, J., Mioskowski, C. and Oudet, P. (1994) Three-dimensional model of Escherichia coli gyrase B subunit crystallized in two-dimensions on novobiocin-linked phospholipid films. J. Mol. Biol., 236, 618-628.
5. Chazal, N., Carriere, C., Gay, B. and Boulanger, P. (1994) Phenotypic characterization of insertion mutants of the human immunodeficiency virus type 1 Gag precursor expressed in recombinant baculovirus-infected cells. J. Virol., 68, 111-122.
6. Chesebro, B., Britt, W., Evans, L., Wehrly, K., Nishio, J. and Cloyd, M. (1983) Characterization of monoclonal antibodies reactive with murine leukemia viruses: use in analysis of strains of Friend MCF and Friend ecotropic murine leukemia viruses. Virology, 127, 134-148.
7. Choi, H.-K., Tong, L., Minor, W., Dumas, P., Boege, U., Rossmann, M. and Wengler, G. (1991) Structure of Sindbis virus core protein reveals a chymotrypsin-like serine proteinase and the organization of the virion. Nature, 354, 37-43.
8. Clish, C., Peyton, D. and Barklis, E. (1996) Spectroscopic study of an HIV-1 capsid protein major homology region peptide analog. FEBS Lett., 378, 43-47.
9. Craven, R., Leure-duPree, A., Erdie, C., Wilson, C. and Wills, J. (1995) Genetic analysis of the major homology region of the Rous sarcoma virus Gag protein. J. Virol., 69, 4213-4227.
10. Crawford, S. and Goff, S. (1984) Mutations in Gag proteins p12 and p15 of Moloney murine leukemia virus block early stages of infection. J. Virol., 49, 909-917.
11. Darst, S., Ahlers, M., Meller, P., Kubalek, E., Blankenburg, R., Ribi, H., Ringsdorf, H. and Kornberg, R. (1991a) Two-dimensional crystals of streptavidin on biotinylated lipid layers and their interactions with biotinylated macromolecules. Biophys. J., 59, 387-396.
12. Darst, S., Edwards, A., Kubalek, E. and Kornberg, R. (1991b) Three-dimensional structure of yeast RNA polymerase II at 16 Å resolution. Cell, 66, 121-128.
13. Dietrich, C., Schmitt, L. and Tampe, R. (1995) Molecular organization of histidine-tagged biomolecules at self-assembled lipid interfaces using a novel class of chelator lipids. Proc. Natl Acad. Sci. USA, 92, 9014-9018.
14. Dietrich, C., Boscheinen, O., Scharf, K., Schmitt, L. and Tampe, R. (1996) Functional immobilization of a DNA-binding protein at a membrane interface via histidine tag and synthetic chelator lipids. Biochemistry, 35, 1100-1105.
15. Ehrlich, L., Agresta, B. and Carter, C. (1992) Assembly of recombinant human immunodeficiency virus type 1 capsid protein in vitro. J. Virol., 66, 4874-4883.
16. Erickson, H., Voter, W. and Leonard, K. (1978) Image reconstruction in electron microscopy: enhancement of periodic structure by optical filtering. Methods Enzymol., 49, 39-63.
17. Faecke, M., Janetzko, A., Shoeman, R. and Krausslich, H. (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.
18. Frank, J., Radermacher, M., Wagenknecht, T. and Verschoor, A. (1988) Studying ribosome structure by electron microscopy and computer-image processing. Methods Enzymol., 164, 3-35.
19. Frey, W., Schief, W., Pack, D., Chen, C., Chilkot, A., Stayton, P., Vogel, V. and Arnold, F. (1996) Two-dimensional protein crystallization via metal-ion coordination by naturally occurring surface histidines. Proc. Natl Acad. Sci. USA, 93, 4937-4941.
20. Fuller, S.D., Capaldi, R. and Henderson, R. (1979) Structure of cytochrome c oxidase in deoxycholate-derived two-dimensional crystals. J. Mol. Biol., 134, 305-327.
21. Fuller, S.D., Berriman, J., Butcher, S. and Gowen, B. (1995) Low pH induces swiveling of the glycoprotein heterodimers in the Semliki Forest virus spike complex. Cell, 81, 715-725.
22. Fuller, S.D., Butcher, S.J., Cheng, R.H. and Baker, T.S. (1996) Three-dimensional reconstruction of icosohedral particles: the uncommon line. J. Struct. Biol., 116, 48-55.
23. Geoghegan, W. and Ackerman, A. (1977) Adsorption of horseradish peroxidase, ovomucoid and anti-immunoglobulin to colloidal gold for the indirect detection of concanavalin A, wheat germ agglutinin and goat anti-human immunoglobulin G on cell surfaces at the electron microscopic level: a new method, theory and application. J. Histochem. Cytochem., 25, 1187-1200.
24. Gitti, R., Lee, B., Walker, J., Summers, M., Yoo, S. and Sundquist, W.I. (1996) Structure of the amino-terminal core domain of the HIV-1 capsid protein. Science, 273, 231-235.
25. Hansen, M. and Barklis, E. (1995) Structural interactions between retroviral Gag proteins examined by cysteine crosslinking. J. Virol., 69, 1150-1159.
26. Hansen, M., Jelinek, L., Whiting, S. and Barklis, E. (1990) Transport and assembly of Gag proteins into Moloney murine leukemia virus. J. Virol., 64, 5306-5316.
27. Hansen, M., Jelinek, L., Jones, R., Stegeman-Olsen, J. and Barklis, E. (1993) Assembly and composition of intracellular particles formed by Moloney murine leukemia virus. J. Virol., 67, 5163-5174.
28. Henderson, R., Baldwin, J., Ceska, T., Zemlin, F., Beckmann, E. and Downing, K. (1990) Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. J. Mol. Biol., 213, 899-929.
29. Hill, C., Worthylake, D., Bancroft, D., Christensen, A. and Sundquist, W. (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.
30. Hochuli, E., Dobeli, H. and Schacher, A. (1987) New metal chelate adsorbent selective for proteins and peptides containing neighbouring histidine residues. J. Chromatogr., 411, 177-184.
31. Horisberger, M. and Clerc, M.-F. (1985) Labelling of colloidal gold with protein A. Histochemistry, 82, 219-223.
32. Jones, T., Blaug, G., Hansen, M. and Barklis, E. (1990) Assembly of Gag-β-galactosidase proteins into retrovirus particles. J. Virol., 64, 2265-2279.
33. Klikova, M., Rhee, S., Hunter, E. and Ruml, T. (1995) Efficient in vivo and in vitro assembly of retroviral capsids from Gag precursor proteins expressed in bacteria. J. Virol., 69, 1830-1839.
34. Kubalek, E., Le Grice, S. and Brown, P. (1995) Two-dimensional crystallization of histidine-tagged HIV-1 reverse transcriptase promoted by a novel nickel-chelating lipid. J. Struct. Biol., 113, 117-123.
35. Kuhlbrandt, W., Wang, D.M. and Fujiyhoshi, Y. (1994) Atomic model of plant light-harvesting complex by electron crystallography. Nature, 367, 614-621.
36. Leis, J. et al. (1988) Standardized and simplified nomenclature for proteins common to all retroviruses. J. Virol., 62, 1808-1809.
37. Mammano, F., Ohagen, A., Hoglund, S. and Gottlinger, H. (1994) Role of the major homology region of the human immunodeficiency virus type 1 in virion morphogenesis. J. Virol., 68, 4927-4936.
38. Maniatis, T., Fritsch, E. and Sambrook, J. (1982) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
39. Matthews, S. et al. (1994) Structural similarity between the p17 matrix protein of HIV-1 and interferon-gamma. Nature, 370, 666-668.
40. McDermott, J., Farrell, L., Ross, R. and Barklis, E. (1996) Structural analysis of human immunodeficiency virus type 1 Gag protein interactions using cysteine-specific reagents. J. Virol., 70, 5106-5114.
41. Momany, C. et al. (1996) Crystal structure of dimeric HIV-1 capsid protein. Nature Struct. Biol., 3, 763-770.
42. 1H NMR. EMBO J., 11, 3059-3065.
43. Nermut, M., Hockley, D., Jowett, J., Jones, I., Garreau, M. and Thomas, D. (1994) Fullerene-like organization of HIV Gag protein shell in virus-like particles produced by recombinant baculovirus. Virology, 198, 288-296.
44. Ng, K., Pack, D., Sasaki, D. and Arnold, F. (1995) Engineering protein-lipid interactions: targeting of histidine-tagged proteins to metal-chelating lipid monolayers. Langmuir, 11, 4048-4055.
45. Olofsson, A., Mallouh, V. and Brisson, A. (1994) Two-dimensional structure of membrane-bound annexin V at 8 Å resolution. J. Struct. Biol., 113, 199-205.
46. Rein, A., McClure, M., Rice, N., Luftif, R. and Schultz, A. (1986) Myristylation site in Pr65Gag is essential for virus particle formation by Moloney murine leukemia virus. Proc. Natl Acad. Sci. USA, 83, 7246-7250.
47. Salmon, E. and DeRosier, D. (1981) A surveying optical diffractometer. J. Microsc., 123, 239-247.
48. Schmitt, L., Dietrich, C. and Tampe, R. (1994) Synthesis and characterization of chelator-lipids for reversible immobilization of engineered proteins at self-assembled lipid interfaces. J. Am. Chem. Soc., 116, 8485-8491.
49. Schmid, M., Dargahi, R. and Tam, M. (1993) SPECTRA: a system for processing electron images of crystals. Ultramicroscopy, 48, 251-264.
50. Shaw, A., Rothnagel, R., Chen, D., Ramig, R., Chiu, W. and Prasad, B. (1993) Three-dimensional visualization of the rotavirus hemagglutinin structure. Cell, 74, 693-701.
51. Shinnick, T., Lerner, R. and Sutcliffe, J. (1981) Nucleotide sequence of Moloney murine leukemia virus. Nature, 293, 543-548.
52. Spearman, P., Wang, J., Van der Heyden, N. and Ratner, L. (1994) Identification of human immunodeficiency virus type 1 Gag protein domains essential to membrane binding and particle assembly. J. Virol., 68, 3232-3242.
53. Srinivasakumar, N., Hammarskjold, M. and Rekosh, D. (1995) Characterization of deletion mutations in the capsid region of human immunodeficiency virus type 1 that affect particle formation and Gagpol precursor incorporation. J. Virol., 69, 6106-6114.
54. Stewart, L., Schatz, G. and Vogt, V. (1990) Properties of avian retrovirus particles defective in viral protease. J. Virol., 64, 5076-5092.
55. Thompson, D., Svendsen, C., DiMeglio, C. and Anderson, V. (1994) Synthesis of chiral diether and tetraether phopholipids. Regiospecific ring opening of epoxides derived from asymmetric epoxidation. J. Org. Chem., 59, 2945-2955.
56. Unwin, P.N.T. and Henderson, R. (1975) Molecular structure determination by electron microscopy of unstained crystalline specimens. J. Mol. Biol., 94, 425-440.
57. Uzgiris, E. and Kornberg, R. (1983) Two-dimensional crystallization technique for imaging macromolecules with application to antigen-antibody-complement complexes. Nature, 301, 125-129.
58. Wang, C., Zhang, Y., McDermott, J. and Barklis, E. (1993) Conditional infectivity of a human immunodeficiency virus matrix domain deletion mutant. J. Virol., 67, 5550-5561.
59. Wang, C., Stegeman-Olsen, J., Zhang, Y. and Barklis, E. (1994) Assembly of HIV Gag-β-galactosidase fusion proteins into virus particles. Virology, 200, 524-534.
60. Weiss, R., Teich, N., Varmus, H. and Coffin, J. (1984) RNA Tumor Viruses. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
61. Wills, J., Craven, R., Weldon, R., Nelle, T. and Erdie, C. (1994) An assembly domain of the Rous sarcoma virus Gag protein required late in budding. J. Virol., 68, 6605-6618.
62. Yu, X., Yuan, X., Matsuda, Z., Lee, T. and Essex, M. (1992) The matrix protein of HIV-1 is required for incorporation of viral envelope protein into mature virions. J. Virol., 66, 5667-5670.
63. Zhang, Y. and Barklis, E. (1995) Nucleocapsid protein effects on the specificity of retrovirus RNA encapsidation. J. Virol., 69, 5716-5722.
64. Zhao, X., Rui, Y. Thompson, D. and Barklis, E. (1994) Interfacial crystallization of HIV capsid protein arrays. American Chemical Society 46th Southeast Regional Meeting, Abstract 73.