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

Journal of Virology

Volumn 77, Issue 15, 2003, Pages 8237-8248

  Graham, David R M ^a   Chertova, Elena ^b   Hilburn, Joanne M ^b   Arthur, Larry O ^b   Hildreth, James E K ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SAIC FREDERICK INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; BETA CYCLODEXTRIN; CAPSID PROTEIN; CHOLESTEROL; ENVELOPE PROTEIN; EZRIN; GAG PROTEIN; GLYCOSYLPHOSPHATIDYLINOSITOL; INTEGRASE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MATRIX PROTEIN; MOESIN; NUCLEOCAPSID PROTEIN; RNA DIRECTED DNA POLYMERASE; VIRUS GLYCOPROTEIN; VIRUS RNA;

ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; LIPID MEMBRANE; NONHUMAN; PERMEABILITY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SIMIAN IMMUNODEFICIENCY VIRUS; VIRION; VIRUS ASSEMBLY; VIRUS ENVELOPE; VIRUS INACTIVATION; VIRUS INFECTIVITY; VIRUS MORPHOLOGY; VIRUS PARTICLE;

BETA-CYCLODEXTRINS; CAPSID PROTEINS; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CHOLESTEROL; CYCLODEXTRINS; HIV-1; HUMANS; MEMBRANE MICRODOMAINS; MICROSCOPY, ELECTRON; SIMIAN IMMUNODEFICIENCY VIRUS; TUMOR CELLS, CULTURED; VIRION; VIRUS INACTIVATION;

EID: 0037771098     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.15.8237-8248.2003     Document Type: Article

References (62)

1. Aloia, R. C., F. C. Jensen, C. C. Curtain, P. W. Mobley, and L. M. Gordon. 1988. Lipid composition and fluidity of the human immunodeficiency virus. Proc. Natl. Acad. Sci. USA 85:900-904.
2. Arthur, L. O., J. W. Bess, Jr., E. N. Chertova, J. L. Rossio, M. T. Esser, R. E. Benveniste, L. E. Henderson, and J. D. Lifson. 1998. Chemical inactivation of retroviral infectivity by targeting nucleocapsid protein zinc fingers: a candidate SIV vaccine. AIDS Res. Hum. Retrovir. 14:S311-S319.
3. Benveniste, R. E., D. Raben, R. W. Hill, W. B. Knott, J. E. Drummond, L. O. Arthur, P. B. Jahrling, W. R. Morton, L. E. Henderson, and G. Heidecker. 1989. Molecular characterization and comparison of simian immunodeficiency virus isolates from macaques, mangabeys, and African green monkeys. J. Med. Primatol. 18:287-303.
4. Bess, J. W., Jr., R. J. Gorelick, W. J. Bosche, L. E. Henderson, and L. O. Arthur. 1997. Microvesicles are a source of contaminating cellular proteins found in purified HIV-1 preparations. Virology 230:134-144.
5. Bess, J. W., Jr., P. J. Powell, H. J. Issaq, L. J. Schumack, M. K. Grimes, L. E. Henderson, and L. O. Arthur. 1992. Tightly bound zinc in human immunodeficiency virus type 1, human T-cell leukemia virus type I, and other retroviruses. J. Virol. 66:840-847.
6. Brown, D. 2002. Structure and function of membrane rafts. Int. J. Med. Microbiol. 291:433-437.
7. Brown, D. A., and E. London. 2000. Structure and function of sphingolipid-and cholesterol-rich membrane rafts. J. Biol. Chem. 275:17221-17224.
8. Bukrinskaya, A., B. Brichacek, A. Mann, and M. Stevenson. 1998. Establishment of a functional human immunodeficiency virus type 1 (HIV-1) reverse transcription complex involves the cytoskeleton. J. Exp. Med. 188:2113-2125.
9. Campbell, S. M., S. M. Crowe, and J. Mak. 2002. Virion-associated cholesterol is critical for the maintenance of HIV-1 structure and infectivity. AIDS 16:2253-2261.
10. Chertova, E., J. W. Bess, Jr., B. J. Crise, I. R. Sowder, 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.
11. Craven, R. C., A. E. Leure-duPree, R. A. Weldon, Jr., and J. W. Wills. 1995. Genetic analysis of the major homology region of the Rous sarcoma virus Gag protein. J. Virol. 69:4213-4227.
12. Esser, M. T., D. R. Graham, L. V. Coren, C. M. Trubey, J. W. Bess, Jr., L. O. Arthur, D. E. Ott, and J. D. Lifson. 2001. Differential incorporation of CD45, CD80 (B7-1), CD86 (B7-2), and major histocompatibility complex class I and II molecules into human immunodeficiency virus type 1 virions and microvesicles: implications for viral pathogenesis and immune regulation. J. Virol. 75:6173-6182.
13. Freed, E. O. 2002. Viral late domains. J. Virol. 76:4679-4687.
14. 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.
15. Garrus, J. E., U. K. von Schwedler, O. W. Pornillos, S. G. Morham, K. H. Zavitz, H. E. Wang, D. A. Wettstein, 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.
16. Gonda, M. A., S. A. Aaronson, N. Ellmore, V. H. Zeve, and K. Nagashima. 1976. Ultrastructural studies of surface features of human normal and tumor cells in tissue culture by scanning and transmission electron microscopy. J. Natl. Cancer Inst. 56:245-263.
17. Gordon, L. M., F. C. Jensen, C. C. Curtain, P. W. Mobley, and R. C. Aloia. 1988. Thermotropic lipid phase separation in the human immunodeficiency virus. Biochim. Biophys. Acta 943:331-342.
18. Gottlinger, H. G., T. Dorfman, J. G. Sodroski, and W. A. Haseltine. 1991. Effect of mutations affecting the p6 gag protein on human immunodeficiency virus particle release. Proc. Natl. Acad. Sci. USA 88:3195-3199.
19. Greene, W. C., and B. M. Peterlin. 2002. Charting HIV's remarkable voyage through the cell: basic science as a passport to future therapy. Nat. Med. 8:673-680.
20. Guyader, M., E. Kiyokawa, L. Abrami, P. Turelli, and D. Trono. 2002. Role for human immunodeficiency virus type 1 membrane cholesterol in viral internalization. J. Virol. 76:10356-10364.
21. Haynes, M. P., M. C. Phillips, and G. H. Rothblat. 2000. Efflux of cholesterol from different cellular pools. Biochemistry 39:4508-4517.
22. Hermida-Matsumoto, L., and M. D. Resh. 2000. Localization of human immunodeficiency virus type 1 Gag and Env at the plasma membrane by confocal imaging. J. Virol. 74:8670-8679.
23. Iyengar, S., J. E. Hildreth, and D. H. Schwartz. 1998. Actin-dependent receptor colocalization required for human immunodeficiency virus entry into host cells. J. Virol. 72:5251-5255.
24. Khanna, K. V., K. J. Whaley, L. Zeitlin, T. R. Moench, K. Mehrazar, R. A. Cone, Z. Liao, J. E. Hildreth, T. E. Hoen, L. Shultz, and R. B. Markham. 2002. Vaginal transmission of cell-associated HIV-1 in the mouse is blocked by a topical, membrane-modifying agent. J. Clin. Investig. 109:205-211.
25. Kilsdonk, E. P., P. G. Yancey, G. W. Stoudt, F. W. Bangerter, W. J. Johnson, M. C. Phillips, and G. H. Rothblat. 1995. Cellular cholesterol efflux mediated by cyclodextrins. J. Biol. Chem. 270:17250-17256.
26. Kim, J. T., E. M. Kim, K. H. Lee, J. E. Choi, B. H. Jhun, and J. W. Kim. 2002. Leucine zipper domain of HIV-1 gp41 interacted specifically with alpha-catenin. Biochem. Biophys. Res. Commun. 291:1239-1244.
27. Kozak, S. L., J. M. Heard, and D. Kabat. 2002. Segregation of CD4 and CXCR4 into distinct lipid microdomains in T lymphocytes suggests a mechanism for membrane destabilization by human immunodeficiency virus. J. Virol. 76:1802-1815.
28. Leitinger, B., and N. Hogg. 2002. The involvement of lipid rafts in the regulation of integrin function. J. Cell Sci. 115:963-972.
29. 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.
30. + lymphocytes in control of simian immunodeficiency virus infection and resistance to rechallenge after transient early antiretroviral treatment. J. Virol. 75:10187-10199.
31. Lindwasser, O. W., and M. D. Resh. 2001. Multimerization of human immunodeficiency virus type 1 Gag promotes its localization to barges, raft-like membrane microdomains. J. Virol. 75:7913-7924.
32. Liu, B., R. Dai, C. J. Tian, L. Dawson, R. Gorelick, and X. F. Yu. 1999. Interaction of the human immunodeficiency virus type 1 nucleocapsid with actin. J. Virol. 73:2901-2908.
33. London, E., and D. A. Brown. 2000. Insolubility of lipids in triton X-100: physical origin and relationship to sphingolipid/holesterol membrane domains (rafts). Biochim. Biophys. Acta 1508:182-195.
34. Lub, M., Y. van Kooyk, S. J. van Vliet, and C. G. Figdor. 1997. Dual role of the actin cytoskeleton in regulating cell adhesion mediated by the integrin lymphocyte function-associated molecule-1. Mol. Biol. Cell 8:341-351.
35. 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.
36. Nakamura, M., H. Okada, H. Sasaki, K. Yoshida, M. Kamada, N. Okada, M. Terada, and T. Ohno. 1996. Quantification of the CD55 and CD59, membrane inhibitors of complement on HIV-1 particles as a function of complement-mediated virolysis. Microbiol. Immunol. 40:561-567.
37. 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.
38. Nguyen, D. H., Z. Liao, J. T. Buckley, and J. E. Hildreth. 1999. The channel-forming toxin aerolysin neutralizes human immunodeficiency virus type 1. Mol. Microbiol. 33:659-666.
39. Nguyen, D. H., and D. Taub. 2002. CXCR4 function requires membrane cholesterol: implications for HIV infection. J. Immunol. 168:4121-4126.
40. 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.
41. Orentas, R. J., and J. E. Hildreth. 1993. Association of host cell surface adhesion receptors and other membrane proteins with HIV and SIV. AIDS Res. Hum. Retrovir. 9:1157-1165.
42. Ott, D. E. 1997. Cellular proteins in HIV virions. Rev. Med. Virol. 7:167-180.
43. Ott, D. E., L. V. Coren, D. G. Johnson, B. P. Kane, R. C. Sowder II, Y. D. Kim, R. J. Fisher, X. Z. Zhou, K. P. Lu, and L. E. Henderson. 2000. Actin-binding cellular proteins inside human immunodeficiency virus type 1. Virology 266:42-51.
44. Ott, D. E., L. V. Coren, B. P. Kane, L. K. Busch, D. G. Johnson, R. C. Sowder II, E. N. Chertova, L. O. Arthur, and L. E. Henderson. 1996. Cytoskeletal proteins inside human immunodeficiency virus type 1 virions. J. Virol. 70:7734-7743.
45. Ott, D. E., S. M. Nigida, Jr., L. E. Henderson, and L. O. Arthur. 1995. The majority of cells are superinfected in a cloned cell line that produces high levels of human immunodeficiency virus type 1 strain MN. J. Virol. 69:2443-2450.
46. Palmer, E., M. L. Martin, C. Goldsmith, and W. Switzer. 1988. Ultrastructure of human immunodeficiency virus type 2. J. Gen. Virol. 69:1425-1429.
47. + T cells. J. Virol. 76:4709-4722.
48. Reed, L. J., and H. Muench. 1938. A simple method of estimating fifty percent endpoints. Am. J. Hyg. 27:493-497.
49. Rey, O., J. Canon, and P. Krogstad. 1996. HIV-1 Gag protein associates with F-actin present in microfilaments. Virology 220:530-534.
50. Roos, J. W., M. F. Maughan, Z. Liao, J. E. Hildreth, and J. E. Clements. 2000. LuSIV cells: a reporter cell line for the detection and quantitation of a single cycle of HIV and SIV replication. Virology 273:307-315.
51. Rossio, J. L., M. T. Esser, K. Suryanarayana, D. K. Schneider, J. W. Bess, Jr., G. M. Vasquez, T. A. Wiltrout, E. Chertova, M. K. Grimes, Q. Sattentau, L. O. Arthur, L. E. Henderson, and J. D. Lifson. 1998. Inactivation of human immunodeficiency virus type 1 infectivity with preservation of conformational and functional integrity of virion surface proteins. J. Virol. 72:7992-8001.
52. Sasaki, H., M. Nakamura, T. Ohno, Y. Matsuda, Y. Yuda, and Y. Nonomura. 1995. Myosin-actin interaction plays an important role in human immunodeficiency virus type 1 release from host cells. Proc. Natl. Acad. Sci. USA 92:2026-2030.
53. Shoeman, R. L., C. Kesselmier, E. Mothes, B. Honer, and P. Traub. 1991. Non-viral cellular substrates for human immunodeficiency virus type 1 protease. FEBS Lett. 278:199-203.
54. Shoeman, R. L., C. Sachse, B. Honer, E. Mothes, M. Kaufmann, and P. Traub. 1993. Cleavage of human and mouse cytoskeletal and sarcomeric proteins by human immunodeficiency virus type 1 protease: actin, desmin, myosin, and tropomyosin. Am. J. Pathol. 142:221-230.
55. Suryanarayana, K., T. A. Wiltrout, G. M. Vasquez, V. M. Hirsch, and J. D. Lifson. 1998. Plasma SIV RNA viral load determination by real-time quantification of product generation in reverse transcriptase-polymerase chain reaction. AIDS Res. Hum. Retrovir. 14:183-189.
56. Tomasselli, A. G., J. O. Hui, L. Adams, J. Chosay, D. Lowery, B. Greenberg, A. Yem, M. R. Deibel, H. Zurcher-Neely, and R. L. Heinrikson. 1991. Actin, troponin C, Alzheimer amyloid precursor protein and pro-interleukin 1β as substrates of the protease from human immunodeficiency virus. J. Biol. Chem. 266:14548-14553.
57. Viard, M., I. Parolini, M. Sargiacomo, K. Fecchi, C. Ramoni, S. Ablan, F. W. Ruscetti, J. M. Wang, and R. Blumenthal. 2002. Role of cholesterol in human immunodeficiency virus type 1 envelope protein-mediated fusion with host cells. J. Virol. 76:11584-11595.
58. Wilk, T., B. Gowen, and S. D. Fuller. 1999. Actin associates with the nucleocapsid domain of the human immunodeficiency virus Gag polyprotein. J. Virol. 73:1931-1940.
59. Yancey, P. G., W. V. Rodrigueza, E. P. Kilsdonk, G. W. Stoudt, W. J. Johnson, M. C. Phillips, and G. H. Rothblat. 1996. Cellular cholesterol efflux mediated by cyclodextrins: demonstration of kinetic pools and mechanism of efflux. J. Biol. Chem. 271:16026-16034.
60. Yong, W. H., S. Wyman, and J. A. Levy. 1990. Optimal conditions for synthesizing complementary DNA in the HIV-1 endogenous reverse transcriptase reaction. AIDS 4:199-206.
61. Zhang, H., G. Dornadula, and R. J. Pomerantz. 1996. Endogenous reverse transcription of human immunodeficiency virus type 1 in physiological microenviroments: an important stage for viral infection of nondividing cells. J. Virol. 70:2809-2824.
62. Zhang, H., L. Wang, S. Kao, I. P. Whitehead, M. J. Hart, B. Liu, K. Duus, K. Burridge, C. J. Der, and L. Su. 1999. Functional interaction between the cytoplasmic leucine-zipper domain of HIV-1 gp41 and p115-RhoGEF. Curr. Biol. 9:1271-1274.