Atomic Force Microscopy Investigation of Human Immunodeficiency Virus (HIV) and HIV-Infected Lymphocytes

Journal of Virology

Volumn 77, Issue 22, 2003, Pages 11896-11909

  Kuznetsov, Y G ^a   Victoria, J G ^a   Robinson Jr , W E ^a   McPherson, A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 [(3 CHOLAMIDOPROPYL)DIMETHYLAMMONIO] 1 PROPANESULFONIC ACID; DETERGENT; DODECYL SULFATE SODIUM; GLYCOPROTEIN GP 120; MATRIX PROTEIN; MEMBRANE PROTEIN; MONOMER; NUCLEIC ACID; POLYSORBATE 20; PROTEINASE INHIBITOR;

ARTICLE; ATOMIC FORCE MICROSCOPY; CELL CYCLE; CELL LINE; CONCENTRATION RESPONSE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNOFLUORESCENCE; LYMPHOCYTE; PRIORITY JOURNAL; PROGENY; THICKNESS; VIRION; VIRUS CAPSID; VIRUS ENVELOPE; VIRUS PARTICLE;

CELL LINE; DETERGENTS; HIV; HIV ENVELOPE PROTEIN GP120; HUMANS; LYMPHOCYTES; MICROSCOPY, ATOMIC FORCE; PROTEASE INHIBITORS; VIRION;

EID: 0242300211     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.22.11896-11909.2003     Document Type: Article

References (73)

1. Baker, T. S., N. H. Olson, and S. D. Fuller. 1999. Adding the third dimension to virus life cycles: three-dimensional reconstruction of icosahedral viruses from cryo-electron micrographs. Microbiol. Mol. Biol. Rev. 63:862-922.
2. Bennett, V. 1982. The molecular basis for membrane-cytoskeleton association in human erythrocytes. J. Cell. Biochem. 18:49-65.
3. Berger, E. A. 1998. And the best picture is-the HIV gp envelope, please! Nat. Struct. Biol. 5:671-674.
4. Bolognesi, D. P., R. C. Montelaro, H. Frank, and W. Schafer. 1978. Assembly of C-type oncornaviruses. A model. Science 199:183-186.
5. Braet, F., D. Vermijlen, V. Bossuyt, R. De Zanger, and E. Wisse. 2001. Early detection of cytotoxic events between hepatic natural killer cells and colon carcinoma cells as probed with the atomic force microscope. Ultramicroscopy 89:265-273.
6. Briggs, J. A. G., T. Wilk, R. Welker, H.-G. Krausslich, and S. D. Fuller. 2003. Structural organization of authentic, mature HIV-1 virions and cores. EMBO J. 22:1707-1715.
7. Bustamante, C., and D. Keller. 1995. Scanning force microscopy in biology. Phys. Today 48:32-38.
8. Chan, D. C., J. M. Fass, E. A. Berger, and P. S. Kim. 1997. Core structure of gp41 from the HIV envelope glycoprotein. Cell 89:263-273.
9. Chertova, E., J. W. Bess, Jr., B. J. Crise, R. C. Sowder II, T. M. Schaden, J. M. Hilburn, J. A. Hoxie, R. E. Benveniste, J. D. Lifson, L. E. Henderson, and L. O. Arthur. 2002. Envelope glycoprotein incorporation, not shedding of surface envelope glycoprotein (gp120/SU), is the primary determinant of SU content of purified human immunodeficiency virus type 1 and simian immunodeficiency virus. J. Virol. 76:5315-5325.
10. Coffin, J. M., S. H. Hughes, and H. E. Varmus (ed.). 1997. Retroviruses. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
11. Craven, R. C., and L. J. Parent. 1996. Dynamic interactions of the Gag polyprotein. Curr. Top. Microbiol. Immunol. 214:65-94.
12. Demirov, D. G., A. Ono, J. M. Orenstein, and E. O. Freed. 2002. Overexpression of the N-terminal domain of TSG101 inhibits HIV-1 budding by blocking late domain function. Proc. Natl. Acad. Sci. USA 99:955-960.
13. Demirov, D. G., J. M. Orenstein, and E. O. Freed. 2002. The late domain of human immunodeficiency virus type 1 p6 promotes virus release in a cell type-dependent manner. Virology 76:105-117.
14. Donnadieu, E., V. Lang, G. Bismuth, W. Ellmeier, O. Acuto, F. Michel, and A. Trautmann. 2001. Differential roles of Lck and Itk in T cell response to antigen recognition revealed by calcium imaging and electron microscopy. J. Immunol. 166:5540-5549.
15. Fass, D. R., R. A. Davey, C. A. Hamson, P. S. Kim, J. M. Cunningham, and J. M. Berger. 1997. Structure of a murine leukemia virus receptor-binding glycoprotein at 2.0 angstrom resolution. Science 277:1662-1666.
16. Frankel, A. D., and J. A. T. Young. 1998. HIV-1: fifteen proteins and an RNA. Annu. Rev. Biochem. 67:1-25.
17. Fuller, S. D., T. Wilk, B. E. Gown, 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.
18. Ganser, B. K., S. Li, V. Y. Klishko, J. T. Finch, and W. I. Sundquist. 1999. Assembly and analysis of conical models for the HIV-1 core. Science 283:80-82.
19. Garrus, J. E., U. K. von Schwedler, O. W. Pornillos, S. G. Morham, K. H. Zavitz, H. E. Wang, D. A. Wettstain, K. M. Stray, M. Cote, R. L. Rich, D. G. Myszka, and W. I. Sundquist. 2001. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107:55-65.
20. Gelderblom, H. R. 1991. Assembly and morphology of HIV: potential effect of structure on viral function. AIDS 5:617-637.
21. Gelderblom, H. R., H. Reuphe, T. Winkel, R. Kunze, and G. Pauli. 1987. MHC-antigens: constituents of the envelopes of human and simian immunodeficiency virus. Z. Naturforsch. Sect. C 42:1328-1334.
22. Graham, D. R. M., E. Chertova, J. M. Hilburn, L. O. Arthur, and J. E. Hildreth. 2003. Cholesterol depletion of human immunodeficiency virus type 1 and simian immunodeficiency virus with β-cyclodextrin inactivates and permeabilizes the virions: evidence for virion-associated lipid rafts. J. Virol. 77:8237-8248.
23. Grewe, C., A. Beck, and H. R. Gelderblom. 1990. HIV: early virus-cell interactions. J. Acquir. Immun. Defic. Syndr. 3:965-974.
24. Hansma, H. G., K. J. Kim, D. E. Laney, R. A. Garcia, M. Argaman, M. J. Allen, and S. M. Parsons. 1997. Properties of biomolecules measured from atomic force microscope images: a review. J. Struct. Biol. 119:99-108.
25. Hartwig, J. H., and M. DeSisto. 1991. The cytoskeleton of the resting human blood platelet: structure of the membrane skeleton and its attachment to actin filaments. J. Cell Biol. 112:407-425.
26. Henderson, L. E., H. C. Krutzsch, and S. Oroszlan. 1983. Myristyl amino-terminal acylation of murine retrovirus proteins: an unusual post-translational protein modification. Proc. Natl. Acad. Sci. USA 80:339-343.
27. 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.
28. Hockley, D. J., M. V. Nermut, C. Grief, J. B. Jowett, and I. M. Jones. 1994. Comparative morphology of Gag protein structures produced by mutants of the gag gene of human immunodeficiency virus type 1. J. Gen. Virol. 75:2985-2987.
29. Hogland, S., L. G. Ofverstedt, A. Nilson, H. Lundquist, H. R. Gelderblom, M. Ozel, and U. Skoglund. 1992. Spatial visualization of the maturing HIV-1 core and its linkage to the envelope. AIDS Res. Hum. Retrovir. 8:1-7.
30. Huang, Y., J. Mak, Q. Cao, Z. Liz, M. A. Wainberg, and L. Kleiman. 1994. Incorporation of excess wild-type and mutant tRNA(2Lys) into human immunodeficiency virus type 1. J. Virol. 68:7676-7683.
31. Jiang, M., J. Mak, A. Ladha, E. Cohen, M. Klein, B. Rovinski, and L. Kleiman. 1993. Identification of tRNAs incorporated into wild-type and mutant human immunodeficiency virus type 1. J. Virol. 67:3246-3253.
32. King, P. J., and W. E. Robinson, Jr. 1998. Resistance to the anti-human immunodeficiency virus type 1 compound L-chicoric acid results from a single mutation at amino acid 140 of integrase. J. Virol. 72:8420-8424.
33. Kotov, A., J. Zhou, P. Flicker, and C. Aiken. 1999. Association of Nef with the human immunodeficiency virus type 1 core. J. Virol. 73:8824-8830.
34. Kuznetsov, Y. G., S. Datta, N. H. Kothari, A. Greenwood, H. Fan, and A. McPherson. 2002. Atomic force microscopy investigation of fibroblasts infected with wild type and mutant murine leukemic virus (MuLV). Biophys. J. 83:3665-3674.
35. Kuznetsov, Y. G., A. J. Malkin, R. W. Lucas, and A. McPherson. 2000. Atomic force microscopy studies of icosahedral virus crystal growth. Colloids Surf. B Biointerfaces 19:333-346.
36. Kuznetsov, Y. G., A. J. Malkin, R. W. Lucas, M. Plomp, and A. McPherson. 2001. Imaging of viruses by atomic force microscopy. J. Gen. Virol. 82:2025-2034.
37. Kuznetsov, Y. G., A. J. Malkin, and A. McPherson. 1997. Atomic force microscopy studies of living cells: visualization of motility, division, aggregation, transformation, and apoptosis. J. Struct. Biol. 120:180-191.
38. Kwong, P. D., R. Wyatt, J. Robinson, R. W. Sweet, J. Sodroski, and W. A. Hendrickson. 1998. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393:648-659.
39. Lee, Y.-M., and X. F. Yu. 1998. Identification and characterization of virus assembly intermediate complexes in HIV-1-infected CD4+ T cells. Virology 243:78-93.
40. Liao, Z., L. M. Cimakasky, R. Hampton, D. H. Nguyen, and J. E. Hildreth. 2001. Lipid rafts and HIV pathogenesis: host membrane cholesterol is required for infection by HIV type 1. AIDS Res. Hum. Retrovir. 17:1009-1019.
41. Lucas, R. W., Y. G. Kuznetsov, S. B. Larson, and A. McPherson. 2001. Crystallization of Brome mosaic virus and T=1 Brome mosaic virus particles following a structural transition. Virology 286:290-303.
42. Malkin, A. J., Y. G. Kuznetsov, R. W. Lucas, and A. McPherson. 1999. Surface processes in the crystallization of turnip yellow mosaic virus visualized by atomic force microscopy. J. Struct. Biol. 127:35-43.
43. Malkin, A. J., A. McPherson, and P. D. Gershon. 2003. Structure of intracellular mature vaccinia virus visualized by in situ AFM. J. Virol. 77:6332-6340.
44. Martin-Serrano, J., T. Zang, and P. D. Bieniasz. 2003. Role of ESCRT-1 in retroviral budding. Virology 77:4794-4804.
45. Momany, C., L. C. Kovari, A. J. Prongay, W. Keller, R. K. Gitti, B. M. Lee, A. E. Gorbaleny, L. Tong, J. McClure, L. S. Ehrlich, M. F. Summers, C. Carter, and M. G. Rossmann. 1996. Crystal structure of dimeric HIV-1 capsid protein. Nat. Struct. Biol. 3:763-771.
46. Moore, J. P. 1997. Coreceptors: implications for HIV pathogenesis and therapy. Science 276:51-52.
47. Morikawa, Y., M. Shibuya, T. Gotoa, and K. Sano. 2000. In vitro processing of human immunodeficiency virus type 1 gag virus-like particles. Virology 272:366-374.
48. Morris, V. J. 1994. Biological applications of scanning probe microscopies. Prog. Biophys. Mol. Biol. 61:131-185.
49. Neagu, C., K. O. Vanderwerf, C. A. J. Putman, Y. M. Kraan, B. G. Degrooth, N. F. Vanhulst, and J. Greve. 1994. Analysis of immunolabeled cells by atomic force microscopy, optical microscopy, and flow cytometry. J. Struct. Biol. 112:32-40.
50. Nermut, M. V., C. Grief, S. Haskmi, and D. J. Hockley. 1993. Further evidence of icosahedral symmetry in human and simian immunodeficiency virus. AIDS Res. Hum. Retrovir. 9:929-938.
51. Nguyen, D. H., and J. K. Hildreth. 2000. Evidence for budding of human immunodeficiency virus type 1 selectively from glycolipid-enriched membrane lipid rafts. J. Virol. 74:3264-3272.
52. Ott, D. E., L. V. Coren, D. G. Johnson, R. C. Sowder II, L. O. Arthur, and L. E. Henderson. 1995. Analysis and localization of cyclophilin A found in the virions of human immunodeficiency virus type 1 MN strain. AIDS Res. Hum. Retrovir. 11:1003-1006.
53. Parker, S. D., J. S. Wall, and E. Hunter. 2001. Analysis of Mason-Pfizer monkey virus Gag particles by scanning transmission electron microscopy. J. Virol. 75:9543-9548.
54. Perotti, M. E., X. Tan, and D. M. Phillips. 1996. Directional budding of human immunodeficiency virus from monocytes. Virology 70:5916-5921.
55. Plomp, M., M. K. Rice, E. K. Wagner, A. McPherson, and A. J. Malkin. 2002. Rapid visualization at high resolution of pathogens by atomic force microscopy: structural studies of herpes simplex virus-1. Am. J. Pathol. 160:1959-1966.
56. Pornillos, O. W., S. L. Alam, R. L. Rich, D. G. Myszka, D. R. Davis, and W. I. Sundquist. 2002. Structure and functional interactions of the Tsg101 UEV domain. EMBO J. 21:2397-2406.
57. Pralle, A., P. Keller, E. L. Florin, K. Simons, and J. K. H. Horber. 2000. Sphingolipid-cholesterol rafts diffuse as small entities in the plasma membrane of mammalian cells. J. Cell Biol. 148:997-1007.
58. Rein, A., M. R. McClure, N. R. Rice, R. B. Luftig, and A. M. Schultz. 1986. Myristylation site in Pr65 Gag is essential for virus particle formation by Moloney murine leukemia virus. Proc. Natl. Acad. Sci. USA 83:7246-7250.
59. Robinson, W. E., Jr., D. C. Montefiori, D. H. Gillespie, and W. M. Mitchell. 1989. Complement-mediated, antibody-dependent enhancement of human immunodeficiency virus type 1 (HIV-1) infection in vitro increases HIV-1 RNA and protein synthesis and infectious virus production. J. Acquir. Immun. Defic. Syndr. 2:33-42.
60. Sakaue, M., and K. Taniguchi. 2001. Imaging of the lectin-labeled cell surface of human lymphocytes by the use of atomic force microscope. J. Vet. Med. Sci. 63:223-225.
61. Schutz, G. J., G. Kada, V. P. Pastushenko, and H. Schindler. 2000. Properties of lipid microdomains in the muscle cell membrane visualized by single molecule microscopy. EMBO J. 19:892-901.
62. Shibata-Seki, T., W. Watanabe, and J. Masai. 1994. Imaging of cells with atomic force microscopy operating at a "tapping mode." J. Vac. Sci. Technol. B 12:1530-1534.
63. Shiraishi, T. 2001. Myristoylation of human immunodeficiency virus type 1 gag protein is required for efficient env protein transportation to the surface of cells. Biochem. Biophys. Res. Commun. 282:1201-1205.
64. Turner, B. G., and M. F. Summers. 1999. Structural biology of HIV. J. Mol. Biol. 285:1-32.
65. Varma, R., and S. Mayor. 1998. GPI-anchored proteins are organized in submicron domains at the cell surface. Nature 394:798-801.
66. Vogt, V. M. 1997. Retroviral virions and genomes, p. 27-69. In J. M. Coffin, S. H. Hughes, and H. E. Varmus (ed.), Retroviruses, vol. 1. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
67. Weissenhorn, W., A. Dessen, S. C. Harrison, J. J. Skehel, and D. C. Wiley. 1997. Atomic structure of the ectodomain from HIV-1 gp41. Nature 387:426-430.
68. Weldon, R. A., and E. Hunter. 1997. Molecular requirements for retrovirus assembly, p. 280. In W. Chin. R. M. Burnett, and R. L. Garcea (ed.), Structural biology of viruses. Oxford University Press, Oxford, United Kingdom.
69. Wilk, T. 2000. The intact retroviral Env glycoprotein of human foamy virus is a trimer. J. Virol. 74:2885-2891.
70. Wilk, T., I. Gross, B. E. Gowen, T. Rutten, D. H. Felix, 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.
71. Wyatt, R., and J. Sodroski. 1998. The HIV-1 envelope glycoproteins: fusogens, antigens and immunogens. Science 280:1884-1888.
72. Gag in immature human immunodeficiency virus type 1 particles. J. Virol. 74:9381-9387.
73. Yeager, M., E. M. Wilson-Kubalek, S. G. Weiner, P. O. Brown, and A. Rein. 1998. Supramolecular organization of immature and mature murine leukemia virus revealed by electron cryo-microscopy: implications for retroviral assembly mechanisms. Proc. Natl. Acad. Sci. USA 95:7299-7304.