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Retroviruses Human Immunodeficiency Virus and Murine Leukemia Virus Are Enriched in Phosphoinositides
Open accessAbstract
Retroviruses acquire a lipid envelope during budding from the membrane of their hosts. Therefore, the composition of this envelope can provide important information about the budding process and its location. Here, we present mass spectrometry analysis of the lipid content of human immunodeficiency virus type 1 (HIV-1) and murine leukemia virus (MLV). The results of this comprehensive survey found that the overall lipid content of these viruses mostly matched that of the plasma membrane, which was considerably different from the total lipid content of the cells. However, several lipids are enriched in comparison to the composition of the plasma membrane: (i) cholesterol, ceramide, and GM3; and (ii) phosphoinositides, phosphorylated derivatives of phosphatidylinositol. Interestingly, microvesicles, which are similar in size to viruses and are also released from the cell periphery, lack phosphoinositides, suggesting a different budding mechanism/location for these particles than for retroviruses. One phosphoinositide, phosphatidylinositol 4,5-bisphosphate [PI(4,5)P 2 ], has been implicated in membrane binding by HIV Gag. Consistent with this observation, we found that PI(4,5)P 2 was enriched in HIV-1 and that depleting this molecule in cells reduced HIV-1 budding. Analysis of mutant virions mapped the enrichment of PI(4,5)P 2 to the matrix domain of HIV Gag. Overall, these results suggest that HIV-1 and other retroviruses bud from cholesterol-rich regions of the plasma membrane and exploit matrix/PI(4,5)P 2 interactions for particle release from cells.
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“In HIV-1, (PIP2) is roughly three times more concentrated in the viral membrane compared to the plasma membrane”
From Beyond reverse transcription: molecular mechanisms and emerging paradigms in retroviral replication (2026) · cites this paper as Chan et al. 2008
In the citing paper
“virus particles harbor three times more PIP2 molecules than Gag molecules”
From Beyond reverse transcription: molecular mechanisms and emerging paradigms in retroviral replication (2026) · cites this paper as Chan et al. 2008
Citations
Cites
A RAPID METHOD OF TOTAL LIPID EXTRACTION AND PURIFICATION
Bligh, E. G., & Dyer, W. J. (1959) · Canadian Journal of Biochemistry and Physiology · doi:10.1139/o59-099 · Cited by 54,751
Ceramide Triggers Budding of Exosome Vesicles into Multivesicular Endosomes
Trajković, K., Hsu, C., Chiantia, S., Rajendran, L., Wenzel, D., Wieland, F., Schwille, P., Brügger, B., & Simons, M. (2008) · Science · doi:10.1126/science.1153124 · Cited by 3,760
How proteins produce cellular membrane curvature
Zimmerberg, J. J., & Kozlov, M. M. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1784 · Cited by 1,321
Escola, J.-M., Kleijmeer, M. J., Stoorvogel, W., Griffith, J. M., Yoshie, O., & Geuze, H. J. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.32.20121 · Cited by 1,228
Proteomic and Biochemical Analyses of Human B Cell-derived Exosomes
Wubbolts, R., Leckie, R. S., Veenhuizen, P. T. M., Schwarzmann, G., Möbius, W., Hoernschemeyer, J., Slot, J.-W., Geuze, H. J., & Stoorvogel, W. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m207550200 · Cited by 886
Brügger, B., Erben, G., Sandhoff, R., Wieland, F., & Lehmann, W. D. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.6.2339 · Cited by 882
Nguyen, D., & Hildreth, J. E. K. (2000) · Journal of Virology · doi:10.1128/jvi.74.7.3264-3272.2000 · Cited by 788
PI(3,4,5)P 3 and PI(4,5)P 2 Lipids Target Proteins with Polybasic Clusters to the Plasma Membrane
Heo, W. D., Inoue, T., Park, W. S., Kim, M. L., Park, B. O., Wandless, T. J., & Meyer, T. (2006) · Science · doi:10.1126/science.1134389 · Cited by 773
Derdeyn, C. A., Decker, J. M., Sfakianos, J. N., Wu, X., O’Brien, W. A., Ratner, L., Kappes, J. C., Shaw, G. M., & Hunter, E. (2000) · Journal of Virology · doi:10.1128/jvi.74.18.8358-8367.2000 · Cited by 743
The HIV lipidome: A raft with an unusual composition
Brügger, B., Glass, B., Haberkant, P., Leibrecht, I., Wieland, F., & Kräusslich, H. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0511136103 · Cited by 730
CD95 Signaling via Ceramide-rich Membrane Rafts
Grassmé, H., Jekle, A., Riehle, A., Schwarz, H., Berger, J., Sandhoff, K., Kolesnick, R., & Gulbins, E. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m101207200 · Cited by 637
Merrill, A. H., Sullards, M. C., Allegood, J. C., Kelly, S. L., & Wang, E. L. (2005) · Methods · doi:10.1016/j.ymeth.2005.01.009 · Cited by 594
Morita, E., & Sundquist, W. I. (2004) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.20.010403.102350 · Cited by 594
Lipid rafts and membrane dynamics
Rajendran, L., & Simons, K. (2005) · Journal of Cell Science · doi:10.1242/jcs.01681 · Cited by 590
Gerrit van, M. E. E. R. (2005) · The EMBO Journal · doi:10.1038/sj.emboj.7600798 · Cited by 584
Phosphatidylinositol (4,5) bisphosphate regulates HIV-1 Gag targeting to the plasma membrane
Ono, A., Ablan, S. D., Lockett, S. J., Nagashima, K., & Freed, E. O. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0405596101 · Cited by 553
Structural basis for targeting HIV-1 Gag proteins to the plasma membrane for virus assembly
Saad, J. S., Miller, J., Tai, J., Kim, A., Ghanam, R. H., & Summers, M. F. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0602818103 · Cited by 545
Fld1p, a functional homologue of human seipin, regulates the size of lipid droplets in yeast
Fei, W., Shui, G., Gaëta, B. A., Du, X., Kuerschner, L., Li, P., Brown, A. J., Wenk, M. R., Parton, R. G., & Yang, H. (2008) · The Journal of Cell Biology · doi:10.1083/jcb.200711136 · Cited by 470
Self-citationAloia, R. C., Tian, H., & Jensen, F. C. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.11.5181 · Cited by 451
Ceramide Selectively Displaces Cholesterol from Ordered Lipid Domains (Rafts)
Megha, M., & London, E. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m309992200 · Cited by 431
Visualization of Retroviral Replication in Living Cells Reveals Budding into Multivesicular Bodies
Sherer, N. M., Lehmann, M. J., Soto, L. F. J., Ingmundson, A., Horner, S. M., Cicchetti, G., Allen, P. G., Pypaert, M., Cunningham, J. M., & Mothes, W. (2003) · Traffic · doi:10.1034/j.1600-0854.2003.00135.x · Cited by 416
Self-citationMattila, P. K., Pykäläinen, A., Saarikangas, J., Paavilainen, V. O., Vihinen, H., Jokitalo, E., & Lappalainen, P. (2007) · Journal of Cell Biology · doi:10.1083/jcb.200609176 · Cited by 405
Actin- and myosin-driven movement of viruses along filopodia precedes their entry into cells
Lehmann, M. J., Sherer, N. M., Marks, C. B., Pypaert, M., & Mothes, W. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200503059 · Cited by 403
Self-citationITOH, T., & DECAMILLI, P. (2006) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2006.06.015 · Cited by 361
Plasma Membrane Is the Site of Productive HIV-1 Particle Assembly
Jouvenet, N., Neil, S. J. D., Bess, C., Johnson, M. C., Virgen, C. A., Simon, S. M., & Bieniasz, P. D. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040435 · Cited by 358
Deneka, M., Pelchen–Matthews, A., Byland, R., Ruíz-Mateos, E., & Marsh, M. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200609050 · Cited by 355
The eloquent ape: genes, brains and the evolution of language
Fisher, S. E., & Marcus, G. (2005) · Nature Reviews Genetics · doi:10.1038/nrg1747 · Cited by 354
Human Immunodeficiency Virus Impairs Reverse Cholesterol Transport from Macrophages
Mujawar, Z., Rose, H. M., Morrow, M. P., Pushkarsky, T., Dubrovsky, L., Mukhamedova, N., Fu, Y., Dart, A. M., Orenstein, J. M., Bobryshev, Y. V., et al. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040365 · Cited by 335
Receptor Activation Alters Inner Surface Potential During Phagocytosis
Yeung, T., Terebiznik, M., Yu, L., Silvius, J., Abidi, W. M., Philips, M., Levine, T., Kapus, A., & Grinstein, S. (2006) · Science · doi:10.1126/science.1129551 · Cited by 329
Ceramide-enriched membrane domains
Bollinger, C. R., Teichgräber, V., & Gulbins, E. (2005) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2005.09.001 · Cited by 325
Electrostatic Sequestration of PIP2 on Phospholipid Membranes by Basic/Aromatic Regions of Proteins
Gambhir, A., Hangyás-Mihályné, G., Zaitseva, I., Cafiso, D. S., Wang, J., Murray, D., Pentyala, S., Smith, S. O., & McLaughlin, S. (2004) · Biophysical Journal · doi:10.1016/s0006-3495(04)74278-2 · Cited by 318
Role of the basic domain of human immunodeficiency virus type 1 matrix in macrophage infection
Freed, E. O., Englund, G., & Martin, M. A. (1995) · Journal of Virology · doi:10.1128/jvi.69.6.3949-3954.1995 · Cited by 301
HIV-1 Buds Predominantly at the Plasma Membrane of Primary Human Macrophages
Welsch, S., Keppler, O. T., Habermann, A., Allespach, I., Krijnse‐Locker, J., & Kräusslich, H. (2007) · PLoS Pathogens · doi:10.1371/journal.ppat.0030036 · Cited by 272
Phosphoinositide profiling in complex lipid mixtures using electrospray ionization mass spectrometry
Wenk, M. R., Lucast, L. J., Paolo, G. D., Romanelli, A. J., Suchy, S. F., Nussbaum, R. L., Cline, G. W., Shulman, G. I., McMurray, W. J., & Camilli, P. V. D. (2003) · Nature Biotechnology · doi:10.1038/nbt837 · Cited by 268
Self-citationChukkapalli, V., Hogue, I. B., Boyko, V., Hu, W.-S., & Ono, A. (2008) · Journal of Virology · doi:10.1128/jvi.01614-07 · Cited by 268
Mapping of tetraspanin-enriched microdomains that can function as gateways for HIV-1
Nydegger, S., Khurana, S., Krementsov, D. N., Foti, M., & Thali, M. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200508165 · Cited by 257
Host factors exploited by retroviruses
Goff, S. P. (2007) · Nature Reviews Microbiology · doi:10.1038/nrmicro1541 · Cited by 247
Lipid rafts: now you see them, now you don't
Shaw, A. S. (2006) · Nature Immunology · doi:10.1038/ni1405 · Cited by 240
Jolly, C. L., & Sattentau, Q. J. (2007) · Journal of Virology · doi:10.1128/jvi.01845-06 · Cited by 212
Kinetics of intracellular transport and sorting of lysosomal membrane and plasma membrane proteins.
Green, S. A., Zimmer, K. ‐., Griffiths, G. W., & Mellman, I. (1987) · The Journal of Cell Biology · doi:10.1083/jcb.105.3.1227 · Cited by 200
Palmitoylation of the HIV-1 envelope glycoprotein is critical for viral infectivity
Rousso, I. Y., Mixon, M. B., Chen, B. K., & Kim, P. S. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.240459697 · Cited by 189
Nef increases infectivity of HIV via lipid rafts
Zheng, Y., Plemenitaš, A., Linnemann, T., Fackler, O., & Peterlin, B. M. (2001) · Current Biology · doi:10.1016/s0960-9822(01)00237-8 · Cited by 151
Role of Lipid Rafts in Virus Replication
Ono, A., & Freed, E. O. (2005) · Advances in virus research · doi:10.1016/s0065-3527(05)64010-9 · Cited by 150
Phospholipid composition of Rous sarcoma virus, host cell membranes and other enveloped RNA viruses
Quigley, J. P., Rifkin, D. B., & Reich, E. (1971) · Virology · doi:10.1016/0042-6822(71)90010-9 · Cited by 133
Yu, C. R., Alterman, M. A., & Dobrowsky, R. T. (2005) · Journal of Lipid Research · doi:10.1194/jlr.m500060-jlr200 · Cited by 133
Rudner, L. A., Nydegger, S., Coren, L. V., Nagashima, K., Thali, M., & Ott, D. E. (2005) · Journal of Virology · doi:10.1128/jvi.79.7.4055-4065.2005 · Cited by 127
Self-citationAnalyzing phosphoinositides and their interacting proteins
Rusten, T. E., & Stenmark, H. (2006) · Nature Methods · doi:10.1038/nmeth867 · Cited by 126
Do lipid rafts mediate virus assembly and pseudotyping?
Briggs, J. A. G., Wilk, T., & Fuller, S. D. (2003) · Journal of General Virology · doi:10.1099/vir.0.18779-0 · Cited by 126
Dalton, A. K., Ako-Adjei, D., Murray, P. S., Murray, D., & Vogt, V. M. (2007) · Journal of Virology · doi:10.1128/jvi.02757-06 · Cited by 118
Productive Human Immunodeficiency Virus Type 1 Assembly Takes Place at the Plasma Membrane
Finzi, A., Orthwein, A., Mercier, J., & Cohen, É. A. (2007) · Journal of Virology · doi:10.1128/jvi.00308-07 · Cited by 111
Ivanova, P. T., Cerda, B. A., Horn, D. M., Cohen, J. S., McLafferty, F. W., & Brown, H. A. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.131195098 · Cited by 109
Ono, A., Waheed, A. A., & Freed, E. O. (2006) · Virology · doi:10.1016/j.virol.2006.10.011 · Cited by 106
Ceramide, a target for antiretroviral therapy
Finnegan, C. M., Rawat, S. S., Puri, A., Wang, J. M., Ruscetti, F. W., & Blumenthal, R. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0402874101 · Cited by 105
Murray, P. S., Li, Z., Wang, J., Tang, C. L., Honig, B. H., & Murray, D. (2005) · Structure · doi:10.1016/j.str.2005.07.010 · Cited by 98
Sensitive profiling of chemically diverse bioactive lipids
Shui, G., Bendt, A. K., Pethe, K., Dick, T., & Wenk, M. R. (2007) · Journal of Lipid Research · doi:10.1194/jlr.m700060-jlr200 · Cited by 90
Self-citationBhattacharya, J., Repik, A., & Clapham, P. R. (2006) · Journal of Virology · doi:10.1128/jvi.01469-05 · Cited by 82
Pessin, J. E., & Gläser, M. (1980) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)70525-0 · Cited by 74
Trubey, C. M., Chertova, E. N., Coren, L. V., Hilburn, J. M., Hixson, C. V., Nagashima, K., Lifson, J. D., & Ott, D. E. (2003) · Journal of Virology · doi:10.1128/jvi.77.23.12699-12709.2003 · Cited by 64
Self-citationLipid studies of Rous sarcoma virus and host cell membranes
Quigley, J. P., Rifkin, D. B., & Reich, E. (1972) · Virology · doi:10.1016/0042-6822(72)90406-0 · Cited by 57
Stolz, D. B., & Jacobsonf, B. S. (1992) · Journal of Cell Science · doi:10.1242/jcs.103.1.39 · Cited by 56
Finnegan, C. M., Rawat, S. S., Cho, E. H., Guiffre, D. L., Lockett, S., Merrill, A. H., & Blumenthal, R. (2007) · Journal of Virology · doi:10.1128/jvi.02553-06 · Cited by 56
Ott, D. E., Nigida, S. M., Henderson, L. E., & Arthur, L. O. (1995) · Journal of Virology · doi:10.1128/jvi.69.4.2443-2450.1995 · Cited by 37
Self-citationBarsov, E. V., Payne, W. S., & Hughes, S. H. (2001) · Journal of Virology · doi:10.1128/jvi.75.11.4973-4983.2001 · Cited by 27
Mason, P. W., & Jacobson, B. S. (1985) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/0005-2736(85)90096-3 · Cited by 22
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HIV-1 assembly, budding, and maturation
Sundquist, W. I., & Krausslich, H.-G. (2012) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a006924 · Cited by 814
Holland, W. L., Bikman, B. T., Wang, L.-P., Yuguang, G., Sargent, K. M., Bulchand, S., Knotts, T. A., Shui, G., Clegg, D. J., Wenk, M. R., et al. (2011) · Journal of Clinical Investigation · doi:10.1172/jci43378 · Cited by 705
Self-citationComprehensive analysis of lipids in biological systems by liquid chromatography-mass spectrometry
Čajka, T., & Fiehn, O. (2014) · TrAC Trends in Analytical Chemistry · doi:10.1016/j.trac.2014.04.017 · Cited by 683
HIV-1 assembly, release and maturation
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Metadata
- Authors
- Chan, R., Uchil, P. D., Jin, J., Shui, G., Ott, D. E., Mothes, W., & Wenk, M. R.
- Affiliations
- National University of Singapore (SG)
- Yale University (US)
- National Cancer Institute (US)
- Corresponding author
- Wenk, Markus R.
- Venue
- Journal of Virology
- Publisher
- American Society for Microbiology
- Published
- 2008-11-15
- Volume
- 82
- Issue
- 22
- Pages
- 11228-11238
- ISSN
- 0022-538X (ISSN-L)
- 1098-5514
- PMC
- PMC2573248
- OpenAlex
- W2081618928
- Cited by
- 282
- References
- 65
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 10 · 2023: 8 · 2022: 9 · 2021: 13 · 2020: 10 · 2019: 12 · 2018: 12 · 2017: 7 · 2016: 18 · 2015: 20 · 2014: 23 · 2013: 26 · 2012: 31
- FWCI
- 8.34
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Virology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- National University of Singapore (submittedVersion)
- Funders
- National University of Singapore
- National Institutes of Health (n01co12400-79-0-22)
- Biomedical Research Council
- National Cancer Institute (N01-CO-012400, ND1-CO-12400, R01CA098727)
- National Institute of Allergy and Infectious Diseases (R21AI065284)
- H2020 European Research Council
- Topics
- Life Sciences › Immunology and Microbiology › Virology › HIV Research and Treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Lipid Membrane Structure and Behavior
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Keywords
- retroviruses, HIV-1, murine leukemia virus, phosphoinositides, phosphatidylinositol 4,5-bisphosphate, viral budding, plasma membrane, cholesterol, ceramide, GM3 ganglioside, microvesicles, HIV Gag, matrix domain, membrane binding
- MeSH terms
- Animals, Cell Line, Cell Membrane, Cytoplasm, Humans, Lipids, Leukemia Virus, Murine, Phosphatidylinositols, Mass Spectrometry, HIV-1, Secretory Vesicles, Rats, gag Gene Products, Human Immunodeficiency Virus
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