Lipid composition and fluidity of the human immunodeficiency virus envelope and host cell plasma membranes (original) (raw)

Abstract

Previous studies have indicated that human immunodeficiency virus (HIV) is enclosed with a lipid envelope similar in composition to cell plasma membranes and to other viruses. Further, the fluidity, as measured by spin resonance spectroscopy, is low and the viral envelope is among the most highly ordered membranes analyzed. However, the relationship between viral envelope lipids and those of the host cell is not known. Here we demonstrate that the phospholipids within the envelopes of HIV-1RF and HIV-2-L are similar to each other but significantly different from their respective host cell surface membranes. Further, we demonstrate that the cholesterol-to-phospholipid molar ratio of the viral envelope is approximately 2.5 times that of the host cell surface membranes. Consistent with the elevated cholesterol-to-phospholipid molar ratio, the viral envelopes of HIV-1RF and HIV-2-L were shown to be 7.5% and 10.5% more ordered than the plasma membranes of their respective host cells. These data demonstrate that HIV-1 and HIV-2-L select specific lipid domains within the surface membrane of their host cells through which to emerge during viral maturation.

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Selected References

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  1. Aloia R. C., Jensen F. C., Curtain C. C., Mobley P. W., Gordon L. M. Lipid composition and fluidity of the human immunodeficiency virus. Proc Natl Acad Sci U S A. 1988 Feb;85(3):900–904. doi: 10.1073/pnas.85.3.900. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Antonian L., Shinitzky M., Samuel D., Lippa A. S. AL721, a novel membrane fluidizer. Neurosci Biobehav Rev. 1987 Winter;11(4):399–413. doi: 10.1016/s0149-7634(87)80010-6. [DOI] [PubMed] [Google Scholar]
  3. Asano K., Asano A. Binding of cholesterol and inhibitory peptide derivatives with the fusogenic hydrophobic sequence of F-glycoprotein of HVJ (Sendai virus): possible implication in the fusion reaction. Biochemistry. 1988 Feb 23;27(4):1321–1329. doi: 10.1021/bi00404a035. [DOI] [PubMed] [Google Scholar]
  4. Barenholz Y., Moore N. F., Wagner R. R. Enveloped viruses as model membrane systems: microviscosity of vesicular stomatitis virus and host cell membranes. Biochemistry. 1976 Aug 10;15(16):3563–3570. doi: 10.1021/bi00661a026. [DOI] [PubMed] [Google Scholar]
  5. Boland J. D., Tweto J. Cellular fractionation and isolation of the plasma membrane of Burkitt's lymphoma cells. Biochim Biophys Acta. 1980 Aug 14;600(3):713–729. doi: 10.1016/0005-2736(80)90475-7. [DOI] [PubMed] [Google Scholar]
  6. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
  7. Brugh M., Jr Butylated hydroxytoluene protects chickens exposed to Newcastle disease virus. Science. 1977 Sep 23;197(4310):1291–1292. doi: 10.1126/science.897670. [DOI] [PubMed] [Google Scholar]
  8. Curtain C. C., Looney F. D., Marchalonis J. J., Raison J. K. Changes in lipid ordering and state of aggregation in lymphocyte plasma membranes after exposure to mitogens. J Membr Biol. 1978 Dec 29;44(3-4):211–232. doi: 10.1007/BF01944222. [DOI] [PubMed] [Google Scholar]
  9. Curtain C. C., Looney F. D., Smelstorius J. A. Lipid domain formation and ligand-induced lymphocyte membrane changes. Biochim Biophys Acta. 1980 Feb 15;596(1):43–56. doi: 10.1016/0005-2736(80)90169-8. [DOI] [PubMed] [Google Scholar]
  10. David A. E. Lipid composition of Sindbis virus. Virology. 1971 Dec;46(3):711–720. doi: 10.1016/0042-6822(71)90073-0. [DOI] [PubMed] [Google Scholar]
  11. Ferber E., Resch K., Wallach D. F., Imm W. Isolation and characterization of lymphocyte plasma membranes. Biochim Biophys Acta. 1972 May 9;266(2):494–504. doi: 10.1016/0005-2736(72)90105-8. [DOI] [PubMed] [Google Scholar]
  12. Garry R. F., Bishop J. M., Parker S., Westbrook K., Lewis G., Waite M. R. Na+ and K+ concentrations and the regulation of protein synthesis in Sindbis virus-infected chick cells. Virology. 1979 Jul 15;96(1):108–120. doi: 10.1016/0042-6822(79)90177-6. [DOI] [PubMed] [Google Scholar]
  13. Garry R. F., Bostick D. A., Schram R., Waite M. R. The ratio of plasma membrane cholesterol to phospholipid and the inhibition of Sindbis virus maturation by low NaCl medium. J Gen Virol. 1985 May;66(Pt 5):1171–1177. doi: 10.1099/0022-1317-66-5-1171. [DOI] [PubMed] [Google Scholar]
  14. Getchell J. P., Hicks D. R., Svinivasan A., Heath J. L., York D. A., Malonga M., Forthal D. N., Mann J. M., McCormick J. B. Human immunodeficiency virus isolated from a serum sample collected in 1976 in Central Africa. J Infect Dis. 1987 Nov;156(5):833–837. doi: 10.1093/infdis/156.5.833. [DOI] [PubMed] [Google Scholar]
  15. Gordon L. M., Jensen F. C., Curtain C. C., Mobley P. W., Aloia R. C. Thermotropic lipid phase separation in the human immunodeficiency virus. Biochim Biophys Acta. 1988 Aug 18;943(2):331–342. doi: 10.1016/0005-2736(88)90565-2. [DOI] [PubMed] [Google Scholar]
  16. Horowitz B., Piët M. P., Prince A. M., Edwards C. A., Lippin A., Walakovits L. A. Inactivation of lipid-enveloped viruses in labile blood derivatives by unsaturated fatty acids. Vox Sang. 1988;54(1):14–20. doi: 10.1111/j.1423-0410.1988.tb01606.x. [DOI] [PubMed] [Google Scholar]
  17. Jett M., Seed T. M., Jamieson G. A. Isolation and characterization of plasma membranes and intact nuclei from lymphoid cells. J Biol Chem. 1977 Mar 25;252(6):2134–2142. [PubMed] [Google Scholar]
  18. Keith A. D., Arruda D., Snipes W., Frost P. The antiviral effectiveness of butylated hydroxytoluene on herpes cutaneous infections in hairless mice. Proc Soc Exp Biol Med. 1982 Jun;170(2):237–244. doi: 10.3181/00379727-170-41425. [DOI] [PubMed] [Google Scholar]
  19. Kim K. S., Moon H. M., Sapienza V., Carp R. I., Pullarkat R. Inactivation of cytomegalovirus and Semliki Forest virus by butylated hydroxytoluene. J Infect Dis. 1978 Jul;138(1):91–94. doi: 10.1093/infdis/138.1.91. [DOI] [PubMed] [Google Scholar]
  20. Kinne-Saffran E., Kinne R. K. Membrane isolation: strategy, techniques, markers. Methods Enzymol. 1989;172:3–17. doi: 10.1016/s0076-6879(89)72004-8. [DOI] [PubMed] [Google Scholar]
  21. Klenk H. D., Choppin P. W. Lipids of plasma membranes of monkey and hamster kidney cells and of parainfluenza virions grown in these cells. Virology. 1969 Jun;38(2):255–268. doi: 10.1016/0042-6822(69)90367-5. [DOI] [PubMed] [Google Scholar]
  22. Klenk H. D., Choppin P. W. Plasma membrane lipids and parainfluenza virus assembly. Virology. 1970 Apr;40(4):939–947. doi: 10.1016/0042-6822(70)90140-6. [DOI] [PubMed] [Google Scholar]
  23. Konopka K., Davis B. R., Düzgüneş N. HIV-1 infection of a non-CD4-expressing variant of HUT-78 cells: lack of inhibition by Leu3A antibodies and enhancement by cationic DOTMA liposomes. Adv Exp Med Biol. 1991;300:97–110. doi: 10.1007/978-1-4684-5976-0_7. [DOI] [PubMed] [Google Scholar]
  24. Konopka K., Davis B. R., Larsen C. E., Alford D. R., Debs R. J., Düzgüneş N. Liposomes modulate human immunodeficiency virus infectivity. J Gen Virol. 1990 Dec;71(Pt 12):2899–2907. doi: 10.1099/0022-1317-71-12-2899. [DOI] [PubMed] [Google Scholar]
  25. Kundrot C. E., Spangler E. A., Kendall D. A., MacDonald R. C., MacDonald R. I. Sendai virus-mediated lysis of liposomes requires cholesterol. Proc Natl Acad Sci U S A. 1983 Mar;80(6):1608–1612. doi: 10.1073/pnas.80.6.1608. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Landsberger F. R., Compans R. W. Effect of membrane protein on lipid bilayer structure: a spin-label electron spin resonance study of vesicular stomatitis virus. Biochemistry. 1976 Jun 1;15(11):2356–2360. doi: 10.1021/bi00656a017. [DOI] [PubMed] [Google Scholar]
  27. Lenard J., Compans R. W. The membrane structure of lipid-containing viruses. Biochim Biophys Acta. 1974 Apr 8;344(1):51–94. doi: 10.1016/0304-4157(74)90008-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Lyte M., Shinitzky M. A special lipid mixture for membrane fluidization. Biochim Biophys Acta. 1985 Jan 10;812(1):133–138. doi: 10.1016/0005-2736(85)90530-9. [DOI] [PubMed] [Google Scholar]
  29. McSharry J. J., Wagner R. R. Lipid composition of purified vesicular stomatitis viruses. J Virol. 1971 Jan;7(1):59–70. doi: 10.1128/jvi.7.1.59-70.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Moore N. F., Patzer E. J., Shaw J. M., Thompson T. E., Wagner R. R. Interaction of vesicular stomatitis virus with lipid vesicles: depletion of cholesterol and effect on virion membrane fluidity and infectivity. J Virol. 1978 Aug;27(2):320–329. doi: 10.1128/jvi.27.2.320-329.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Pal R., Barenholz Y., Wagner R. R. Depletion and exchange of cholesterol from the membrane of vesicular stomatitis virus by interaction with serum lipoproteins or poly(vinylpyrrolidone) complexed with bovine serum albumin. Biochemistry. 1981 Feb 3;20(3):530–539. doi: 10.1021/bi00506a014. [DOI] [PubMed] [Google Scholar]
  32. Patzer E. J., Moore N. F., Barenholz Y., Shaw J. M., Wagner R. R. Lipid organization of the membrane of vesicular stomatitis virus. J Biol Chem. 1978 Jul 10;253(13):4544–4550. [PubMed] [Google Scholar]
  33. Phalen T., Kielian M. Cholesterol is required for infection by Semliki Forest virus. J Cell Biol. 1991 Feb;112(4):615–623. doi: 10.1083/jcb.112.4.615. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Quigley J. P., Rifkin D. B., Reich E. Phospholipid composition of Rous sarcoma virus, host cell membranes and other enveloped RNA viruses. Virology. 1971 Oct;46(1):106–116. doi: 10.1016/0042-6822(71)90010-9. [DOI] [PubMed] [Google Scholar]
  35. Renkonen O., Käräinen L., Simons K., Gahmberg C. G. The lipid class composition of Semliki forest virus and plasma membranes of the host cells. Virology. 1971 Nov;46(2):318–326. doi: 10.1016/0042-6822(71)90033-x. [DOI] [PubMed] [Google Scholar]
  36. Resnick L., Veren K., Salahuddin S. Z., Tondreau S., Markham P. D. Stability and inactivation of HTLV-III/LAV under clinical and laboratory environments. JAMA. 1986 Apr 11;255(14):1887–1891. [PubMed] [Google Scholar]
  37. Rouser G., Fkeischer S., Yamamoto A. Two dimensional then layer chromatographic separation of polar lipids and determination of phospholipids by phosphorus analysis of spots. Lipids. 1970 May;5(5):494–496. doi: 10.1007/BF02531316. [DOI] [PubMed] [Google Scholar]
  38. Sarin P. S., Gallo R. C., Scheer D. I., Crews F., Lippa A. S. Effects of a novel compound (AL 721) on HTLV-III infectivity in vitro. N Engl J Med. 1985 Nov 14;313(20):1289–1290. doi: 10.1056/NEJM198511143132011. [DOI] [PubMed] [Google Scholar]
  39. Slosberg B. N., Montelaro R. C. A comparison of the mobilities and thermal transitions of retrovirus lipid envelopes and host cell plasma membranes by electron spin resonance spectroscopy. Biochim Biophys Acta. 1982 Jul 28;689(2):393–402. doi: 10.1016/0005-2736(82)90274-7. [DOI] [PubMed] [Google Scholar]
  40. Tibbits G. F., Sasaki M., Ikeda M., Shimada K., Tsuruhara T., Nagatomo T. Characterization of rat myocardial sarcolemma. J Mol Cell Cardiol. 1981 Dec;13(12):1051–1061. doi: 10.1016/0022-2828(81)90295-9. [DOI] [PubMed] [Google Scholar]
  41. Weiner N. Regulation of norepinephrine biosynthesis. Annu Rev Pharmacol. 1970;10:273–290. doi: 10.1146/annurev.pa.10.040170.001421. [DOI] [PubMed] [Google Scholar]
  42. White J., Helenius A. pH-dependent fusion between the Semliki Forest virus membrane and liposomes. Proc Natl Acad Sci U S A. 1980 Jun;77(6):3273–3277. doi: 10.1073/pnas.77.6.3273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Young J. D., Young G. P., Cohn Z. A., Lenard J. Interaction of enveloped viruses with planar bilayer membranes: observations on Sendai, influenza, vesicular stomatitis, and Semliki Forest viruses. Virology. 1983 Jul 15;128(1):186–194. doi: 10.1016/0042-6822(83)90329-x. [DOI] [PubMed] [Google Scholar]