HIV-1 particle assembly is driven by the structural protein Gag. Gag binds to and multimerizes on the inner leaflet of the plasma membrane, eventually resulting in formation of spherical particles. During virus spread among T cells, Gag accumulates to the plasma membrane domain that, together with target cell membrane, forms a cell junction known as the virological synapse. While Gag association with plasma membrane microdomains has been implicated in virus assembly and cell-to-cell transmission, recent studies suggest that, rather than merely accumulating to pre-existing microdomains, Gag plays an active role in reorganizing the microdomains via its multimerization activity. In this paper, we will discuss this emerging view of Gag microdomain interactions. Relationships between Gag multimerization and microdomain association will be further discussed in the context of Gag localization to T-cell uropods and virological synapses. 1. Introduction Microdomain-based compartmentalization of the plasma membrane is implicated in many aspects of the HIV-1 life cycle. In particular, during events in the late phase of the HIV-1 life cycle such as assembly and cell-to-cell transmission, these microdomains have been thought to serve as preformed platforms that facilitate concentration of viral components (e.g., Gag and Env) or delivery of these proteins to specific locations in cells. However, recent studies suggest that Gag is not a simple passenger of microdomains but rather plays an active role in reorganizing microdomains via its membrane-binding and multimerization activities. In this paper, we focus on recent findings on this active role played by Gag during microdomain association. In light of this new view, we will also discuss the implications of plasma membrane microdomains and large-scale domains in cell-to-cell transmission. Microdomains are also thought to affect virion infectivity, attachment of virions to target cells, and virus-cell fusion, in which they modulate distributions and/or activities of Env, Nef, and virus receptors. For these topics, interested readers are referred to more comprehensive papers published in recent years [1–5]. 2. HIV-1 Assembly at the Plasma Membrane The viral structural polyprotein Gag is necessary and sufficient for the assembly of virus-like particles. HIV-1 Gag is synthesized as a 55？kDa polyprotein composed of 4 major structural domains (and 2 spacer polypeptides), as defined by cleavage by the viral protease: matrix (MA), capsid (CA), nucleocapsid (NC), and p6. However, proteolytic cleavage occurs largely after
References
[1]
M.A. Checkley, B.G. Luttge, and E.O. Freed, “HIV-1 envelope glycoprotein biosynthesis, trafficking, and incorporation,” Journal of Molecular Biology, vol. 410, no. 4, pp. 582–608, 2011.
[2]
M. C. Johnson, “Mechanisms for env glycoprotein acquisition by retroviruses,” AIDS Research and Human Retroviruses, vol. 27, no. 3, pp. 239–247, 2011.
[3]
A. Ono, “Relationships between plasma membrane microdomains and HIV-1 assembly,” Biology of the Cell, vol. 102, no. 6, pp. 335–350, 2010.
[4]
M. Thali, “The roles of tetraspanins in HIV-1 replication,” Current Topics in Microbiology and Immunology, vol. 339, no. 1, pp. 85–102, 2009.
[5]
A. A. Waheed and E. O. Freed, “Lipids and membrane microdomains in HIV-1 replication,” Virus Research, vol. 143, no. 2, pp. 162–176, 2009.
[6]
C. S. Adamson and E. O. Freed, “Human immunodeficiency virus type 1 assembly, release, and maturation,” Advances in Pharmacology, vol. 55, pp. 347–387, 2007.
[7]
E. O. Balasubramaniam and M. Freed, “New Insights into HIV Assembly and Trafficking,” Physiology, vol. 26, no. 4, pp. 236–251, 2011.
[8]
M. Bryant and L. Ratner, “Myristoylation-dependent replication and assembly of human immunodeficiency virus 1,” Proceedings of the National Academy of Sciences of the United States of America, vol. 87, no. 2, pp. 523–527, 1990.
[9]
V. Chukkapalli, I. B. Hogue, V. Boyko, W. S. Hu, and A. Ono, “Interaction between the human immunodeficiency virus type 1 Gag matrix domain and phosphatidylinositol-(4,5)-bisphospnate is essential for efficient Gag membrane binding,” Journal of Virology, vol. 82, no. 5, pp. 2405–2417, 2008.
[10]
V. Chukkapalli, S. J. Oh, and A. Ono, “Opposing mechanisms involving RNA and lipids regulate HIV-1 Gag membrane binding through the highly basic region of the matrix domain,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 4, pp. 1600–1605, 2010.
[11]
A. K. Dalton, D. Ako-Adjei, P. S. Murray, D. Murray, and V. M. Vogt, “Electrostatic interactions drive membrane association of the human immunodeficiency virus type 1 Gag MA domain,” Journal of Virology, vol. 81, no. 12, pp. 6434–6445, 2007.
[12]
H. G. Gottlinger, J. G. Sodroski, and W. A. Haseltine, “Role of capsid precursor processing and myristoylation in morphogenesis and infectivity of human immunodeficiency virus type 1,” Proceedings of the National Academy of Sciences of the United States of America, vol. 86, no. 15, pp. 5781–5785, 1989.
[13]
C. P. Hill, D. Worthylake, D. P. Bancroft, A. M. Christensen, and W. I. Sundquist, “Crystal structures of the trimeric human immunodeficiency virus type 1 matrix protein: Implications for membrane association and assembly,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 7, pp. 3099–3104, 1996.
[14]
J. S. Saad, J. Miller, J. Tai, A. Kim, R. H. Ghanam, and M. F. Summers, “Structural basis for targeting HIV-1 Gag proteins to the plasma membrane for virus assembly,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 30, pp. 11364–11369, 2006.
[15]
N. Shkriabai, S. A. K. Datta, Z. Zhao, S. Hess, A. Rein, and M. Kvaratskhelia, “Interactions of HIV-1 Gag with assembly cofactors,” Biochemistry, vol. 45, no. 13, pp. 4077–4083, 2006.
[16]
W. Zhou, L. J. Parent, J. W. Wills, and M. D. Resh, “Identification of a membrane-binding domain within the amino-terminal region of human immunodeficiency virus type 1 Gag protein which interacts with acidic phospholipids,” Journal of Virology, vol. 68, no. 4, pp. 2556–2569, 1994.
[17]
V. Chukkapalli and A. Ono, “Molecular determinants that regulate plasma membrane association of HIV-1 Gag,” Journal of Molecular Biology, vol. 410, no. 4, pp. 512–524, 2011.
[18]
P. Spearman, R. Horton, L. Ratner, and I. Kuli-Zade, “Membrane binding of human immunodeficiency virus type 1 matrix protein in vivo supports a conformational myristyl switch mechanism,” Journal of Virology, vol. 71, no. 9, pp. 6582–6592, 1997.
[19]
W. Zhou and M. D. Resh, “Differential membrane binding of the human immunodeficiency virus type 1 matrix protein,” Journal of Virology, vol. 70, no. 12, pp. 8540–8548, 1996.
[20]
J. S. Saad, E. Loeliger, P. Luncsford et al., “Point mutations in the HIV-1 matrix protein turn off the myristyl switch,” Journal of Molecular Biology, vol. 366, no. 2, pp. 574–585, 2007.
[21]
C. Tang, E. Loeliger, P. Luncsford, I. Kinde, D. Beckett, and M. F. Summers, “Entropic switch regulates myristate exposure in the HIV-1 matrix protein,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 2, pp. 517–522, 2004.
[22]
A. Alfadhli, H. McNett, S. Tsagli, H.P. Bachinger, D.H. Peyton, and E. Barklis, “HIV-1 matrix protein binding to RNA,” Journal of Molecular Biology, vol. 410, no. 4, pp. 653–666, 2011.
[23]
A. Alfadhli, A. Still, and E. Barklis, “Analysis of human immunodeficiency virus type 1 matrix binding to membranes and nucleic acids,” Journal of Virology, vol. 83, no. 23, pp. 12196–12203, 2009.
[24]
S. A. K. Datta, F. Heinrich, S. Raghunandan et al., “HIV-1 Gag extension: conformational changes require simultaneous interaction with membrane and nucleic acid,” Journal of Molecular Biology, vol. 406, no. 2, pp. 205–214, 2011.
[25]
C. P. Jones, S. A. K. Datta, A. Rein, I. Rouzina, and K. Musier-Forsyth, “Matrix domain modulates HIV-1 Gag's nucleic acid chaperone activity via inositol phosphate binding,” Journal of Virology, vol. 85, no. 4, pp. 1594–1603, 2011.
[26]
S. A. K. Datta, Z. Zhao, P. K. Clark et al., “Interactions between HIV-1 Gag molecules in solution: an inositol phosphate-mediated switch,” Journal of Molecular Biology, vol. 365, no. 3, pp. 799–811, 2007.
[27]
T. R. Gamble, S. Yoo, F. F. Vajdos et al., “Structure of the carboxyl-terminal dimerization domain of the HIV-1 capsid protein,” Science, vol. 278, no. 5339, pp. 849–853, 1997.
[28]
I. B. Hogue, A. Hoppe, and A. Ono, “Quantitative fluorescence resonance energy transfer microscopy analysis of the human immunodeficiency virus type 1 Gag-Gag interaction: Relative contributions of the CA and NC domains and membrane binding,” Journal of Virology, vol. 83, no. 14, pp. 7322–7336, 2009.
[29]
U. K. Von Schwedler, K. M. Stray, J. E. Garrus, and W. I. Sundquist, “Functional surfaces of the human immunodeficiency virus type 1 capsid protein,” Journal of Virology, vol. 77, no. 9, pp. 5439–5450, 2003.
[30]
S. Campbell and A. Rein, “In vitro assembly properties of human immunodeficiency virus type 1 Gag protein lacking the p6 domain,” Journal of Virology, vol. 73, no. 3, pp. 2270–2279, 1999.
[31]
S. Campbell and V. M. Vogt, “Self-assembly in vitro of purified CA-NC proteins from Rous sarcoma virus and human immunodeficiency virus type 1,” Journal of Virology, vol. 69, no. 10, pp. 6487–6497, 1995.
[32]
A. Cimarelli, S. Sandin, S. H？glund, and J. Luban, “Basic residues in human immunodeficiency virus type 1 nucleocapsid promote virion assembly via interaction with RNA,” Journal of Virology, vol. 74, no. 7, pp. 3046–3057, 2000.
[33]
A. Khorchid, R. Halwani, M. A. Wainberg, and L. Kleiman, “Role of RNA in facilitating Gag/Gag-Pol interaction,” Journal of Virology, vol. 76, no. 8, pp. 4131–4137, 2002.
[34]
D. Muriaux, J. Mirro, D. Harvin, and A. Rein, “RNA is a structural element in retrovirus particles,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 9, pp. 5246–5251, 2001.
[35]
M. A. Accola, B. Strack, and H. G. G？ttlinger, “Efficient particle production by minimal Gag constructs which retain the carboxy-terminal domain of human immunodeficiency virus type 1 capsid-p2 and a late assembly domain,” Journal of Virology, vol. 74, no. 12, pp. 5395–5402, 2000.
[36]
R. M. Crist, S. A. K. Datta, A. G. Stephen et al., “Assembly properties of human immunodeficiency virus type 1 gag-leucine zipper chimeras: Implications for retrovirus assembly,” Journal of Virology, vol. 83, no. 5, pp. 2216–2225, 2009.
[37]
M. C. Johnson, H. M. Scobie, Y. M. Ma, and V. M. Vogt, “Nucleic acid-independent retrovirus assembly can be driven by dimerization,” Journal of Virology, vol. 76, no. 22, pp. 11177–11185, 2002.
[38]
K. C. Klein, J. C. Reed, M. Tanaka, V. T. Nguyen, S. Giri, and J. R. Lingappa, “HIV Gag-leucine zipper chimeras form ABCE1-containing intermediates and RNase-resistant immature capsids similar to those formed by wild-type HIV-1 Gag,” Journal of Virology, vol. 85, no. 14, pp. 7419–7435, 2011.
[39]
Y. Zhang, H. Qian, Z. Love, and E. Barklis, “Analysis of the assembly function of the human immunodeficiency virus type 1 gag protein nucleocapsid domain,” Journal of Virology, vol. 72, no. 3, pp. 1782–1789, 1998.
[40]
S. A. K. Datta, L. G. Temeselew, R. M. Crist et al., “On the role of the SP1 domain in HIV-1 particle assembly: a molecular switch?” Journal of Virology, vol. 85, no. 9, pp. 4111–4121, 2011.
[41]
J. A. G. Briggs and H.-G. Kr？usslich, “The molecular architecture of HIV,” Journal of Molecular Biology, vol. 410, no. 4, pp. 491–500, 2011.
[42]
I.B. Hogue, J.R. Grover, F. Soheilian, K. Nagashima, and A. Ono, “Gag induces the coalescence of clustered lipid rafts and tetraspanin-enriched microdomains at HIV-1 assembly sites on the plasma membrane,” Journal of Virology, vol. 85, no. 19, pp. 9749–9766, 2011.
[43]
E.R. Weiss and H. Gottlinger, “The role of cellular factors in promoting HIV budding,” Journal of Molecular Biology, vol. 410, no. 4, pp. 525–533, 2011.
[44]
A. Ono, “HIV-1 assembly at the plasma membrane: Gag trafficking and localization,” Future Virology, vol. 4, no. 3, pp. 241–257, 2009.
[45]
A. Pelchen-Matthews, B. Kramer, and M. Marsh, “Infectious HIV-1 assembles in late endosomes in primary macrophages,” Journal of Cell Biology, vol. 162, no. 3, pp. 443–455, 2003.
[46]
G. Raposo, M. Moore, D. Innes et al., “Human macrophages accumulate HIV-1 particles in MHC II compartments,” Traffic, vol. 3, no. 10, pp. 718–729, 2002.
[47]
A. E. Bennett, K. Narayan, D. Shi et al., “Ion-abrasion scanning electron microscopy reveals surface-connected tubular conduits in HIV-infected macrophages,” PLoS Pathogens, vol. 5, no. 9, Article ID e1000591, 2009.
[48]
H. Chu, J.-J. Wang, M. Qi et al., “The intracellular virus-containing compartments in primary human macrophages are largely inaccessible to antibodies and small molecules,” PLoS ONE, vol. 7, no. 5, Article ID e35297, 2012.
[49]
M. Deneka, A. Pelchen-Matthews, R. Byland, E. Ruiz-Mateos, and M. Marsh, “In macrophages, HIV-1 assembles into an intracellular plasma membrane domain containing the tetraspanins CD81, CD9, and CD53,” Journal of Cell Biology, vol. 177, no. 2, pp. 329–341, 2007.
[50]
M. Jouve, N. Sol-Foulon, S. Watson, O. Schwartz, and P. Benaroch, “HIV-1 buds and accumulates in “Nonacidic” endosomes of macrophages,” Cell Host and Microbe, vol. 2, no. 2, pp. 85–95, 2007.
[51]
H. Koppensteiner, C. Banning, C. Schneider, H. Hohenberg, and M. Schindler, “Macrophage internal HIV-1 is protected from neutralizing antibodies,” Journal of Virology, vol. 86, no. 5, pp. 2826–2836, 2012.
[52]
S. Welsch, F. Groot, H. G. Kr？usslich, O. T. Keppler, and Q. J. Sattentau, “Architecture and regulation of the HIV-1 assembly and holding compartment in macrophages,” Journal of Virology, vol. 85, no. 15, pp. 7922–7927, 2011.
[53]
S. Welsch, O. T. Keppler, A. Habermann, I. Allespach, J. Krijnse-Locker, and H. G. Kr？usslich, “HIV-1 buds predominantly at the plasma membrane of primary human macrophages,” PLoS Pathogens, vol. 3, no. 3, 2007.
[54]
A. M. Booth, Y. Fang, J. K. Fallon et al., “Exosomes and HIV Gag bud from endosome-like domains of the T cell plasma membrane,” Journal of Cell Biology, vol. 172, no. 6, pp. 923–935, 2006.
[55]
S. Nydegger, S. Khurana, D. N. Krementsov, M. Foti, and M. Thali, “Mapping of tetraspanin-enriched microdomains that can function as gateways for HIV-1,” Journal of Cell Biology, vol. 173, no. 5, pp. 795–807, 2006.
[56]
N. Jouvenet, S. J. Neil, C. Bess et al., “Plasma membrane is the site of productive HIV-1 particle assembly,” PLoS biology, vol. 4, no. 12, Article ID e435, 2006.
[57]
A. Finzi, A. Orthwein, J. Mercier, and E. A. Cohen, “Productive human immunodeficiency virus type 1 assembly takes place at the plasma membrane,” Journal of Virology, vol. 81, no. 14, pp. 7476–7490, 2007.
[58]
D. Lingwood and K. Simons, “Lipid rafts as a membrane-organizing principle,” Science, vol. 327, no. 5961, pp. 46–50, 2010.
[59]
J. Bhattacharya, A. Repik, and P. R. Clapham, “Gag regulates association of human immunodeficiency virus type 1 envelope with detergent-resistant membranes,” Journal of Virology, vol. 80, no. 11, pp. 5292–5300, 2006.
[60]
L. Ding, A. Derdowski, J. J. Wang, and P. Spearman, “Independent segregation of human immunodeficiency virus type 1 Gag protein complexes and lipid rafts,” Journal of Virology, vol. 77, no. 3, pp. 1916–1926, 2003.
[61]
J. Dou, J. J. Wang, X. Chen, H. Li, L. Ding, and P. Spearman, “Characterization of a myristoylated, monomeric HIV Gag protein,” Virology, vol. 387, no. 2, pp. 341–352, 2009.
[62]
C. Y. Gomez and T. J. Hope, “Mobility of human immunodeficiency virus type 1 Pr55Gag in living cells,” Journal of Virology, vol. 80, no. 17, pp. 8796–8806, 2006.
[63]
R. Halwani, A. Khorchid, S. Cen, and L. Kleiman, “Rapid localization of Gag/GagPol complexes to detergent-resistant membrane during the assembly of human immunodeficiency virus type 1,” Journal of Virology, vol. 77, no. 7, pp. 3973–3984, 2003.
[64]
K. Holm, K. Weclewicz, R. Hewson, and M. Suomalainen, “Human immunodeficiency virus type 1 assembly and lipid rafts: Pr55gag associates with membrane domains that are largely resistant to Brij98 but sensitive to triton X-100,” Journal of Virology, vol. 77, no. 8, pp. 4805–4817, 2003.
[65]
O. W. Lindwasser and M. D. Resh, “Multimerization of human immunodeficiency virus type 1 Gag promotes its localization to barges, raft-like membrane microdomains,” Journal of Virology, vol. 75, no. 17, pp. 7913–7924, 2001.
[66]
O. W. Lindwasser and M. D. Resh, “Myristoylation as a target for inhibiting HIV assembly: unsaturated fatty acids block viral budding,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 20, pp. 13037–13042, 2002.
[67]
D. H. Nguyen and J. E. K. Hildreth, “Evidence for budding of human immunodeficiency virus type 1 selectively from glycolipid-enriched membrane lipid rafts,” Journal of Virology, vol. 74, no. 7, pp. 3264–3272, 2000.
[68]
A. Ono and E. O. Freed, “Plasma membrane rafts play a critical role in HIV-1 assembly and release,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 24, pp. 13925–13930, 2001.
[69]
A. Ono, A. A. Waheed, and E. O. Freed, “Depletion of cellular cholesterol inhibits membrane binding and higher-order multimerization of human immunodeficiency virus type 1 Gag,” Virology, vol. 360, no. 1, pp. 27–35, 2007.
[70]
A. Ono, A. A. Waheed, A. Joshi, and E. O. Freed, “Association of human immunodeficiency virus type 1 Gag with membrane does not require highly basic sequences in the nucleocapsid: use of a novel Gag multimerization assay,” Journal of Virology, vol. 79, no. 22, pp. 14131–14140, 2005.
[71]
W. F. Pickl, F. X. Pimentel-Mui？ios, and B. Seed, “Lipid rafts and pseudotyping,” Journal of Virology, vol. 75, no. 15, pp. 7175–7183, 2001.
[72]
J. F. Hancock, “Lipid rafts: contentious only from simplistic standpoints,” Nature Reviews Molecular Cell Biology, vol. 7, no. 6, pp. 456–462, 2006.
[73]
H. Heerklotz, “Triton promotes domain formation in lipid raft mixtures,” Biophysical Journal, vol. 83, no. 5, pp. 2693–2701, 2002.
[74]
J. Kwik, S. Boyle, D. Fooksman, L. Margolis, M. P. Sheetz, and M. Edidin, “Membrane cholesterol, lateral mobility, and the phosphatidylinositol 4,5-bisphosphate-dependent organization of cell actin,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 2, pp. 13964–13969, 2003.
[75]
D. Lichtenberg, F. M. Go？i, and H. Heerklotz, “Detergent-resistant membranes should not be identified with membrane rafts,” Trends in Biochemical Sciences, vol. 30, no. 8, pp. 430–436, 2005.
[76]
S. Munro, “Lipid rafts: elusive or illusive?” Cell, vol. 115, no. 4, pp. 377–388, 2003.
[77]
G. Gri, B. Molon, S. Manes, T. Pozzan, and A. Viola, “The inner side of T cell lipid rafts,” Immunology Letters, vol. 94, no. 3, pp. 247–252, 2004.
[78]
T. Harder, P. Scheiffele, P. Verkade, and K. Simons, “Lipid domain structure of the plasma membrane revealed by patching of membrane components,” Journal of Cell Biology, vol. 141, no. 4, pp. 929–942, 1998.
[79]
P. W. Janes, S. C. Ley, and A. I. Magee, “Aggregation of lipid rafts accompanies signaling via the T cell antigen receptor,” Journal of Cell Biology, vol. 147, no. 2, pp. 447–461, 1999.
[80]
D. E. Shvartsman, M. Kotler, R. D. Tall, M. G. Roth, and Y. I. Henis, “Differently anchored influenza hemagglutinin mutants display distinct interaction dynamics with mutual rafts,” Journal of Cell Biology, vol. 163, no. 4, pp. 879–888, 2003.
[81]
A. V. Harrist, E. V. Ryzhova, T. Harvey, and F. González-Scarano, “Anx2 interacts with HIV-1 Gag at phosphatidylinositol (4,5) bisphosphate-containing lipid rafts and increases viral production in 293T cells,” PLoS ONE, vol. 4, no. 3, Article ID e5020, 2009.
[82]
D. N. Krementsov, P. Rassam, E. Margeat et al., “HIV-1 assembly differentially alters dynamics and partitioning of tetraspanins and raft components,” Traffic, vol. 11, no. 11, pp. 1401–1414, 2010.
[83]
E. O. Ono and A. Freed, The role of lipid rafts in virus replication, Elsevier, New York, NY, USA, 2005.
[84]
M. Lehmann, S. Rocha, B. Mangeat et al., “Quantitative multicolor super-resolution microscopy reveals tetherin HIV-1 interaction,” PLoS Pathogens, vol. 7, no. 12, Article ID e1002456, 2011.
[85]
R. C. Aloia, H. Tian, and F. C. Jensen, “Lipid composition and fluidity of the human immunodeficiency virus envelope and host cell plasma membranes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 11, pp. 5181–5185, 1993.
[86]
B. Brügger, B. Glass, P. Haberkant, I. Leibrecht, F. T. Wieland, and H. G. Kr？usslich, “The HIV lipidome: a raft with an unusual composition,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 8, pp. 2641–2646, 2006.
[87]
R. Chan, P. D. Uchil, J. Jin et al., “Retroviruses human immunodeficiency virus and murine leukemia virus are enriched in phosphoinositides,” Journal of Virology, vol. 82, no. 22, pp. 11228–11238, 2008.
[88]
E. Chertova, O. Chertov, L. V. Coren et al., “Proteomic and biochemical analysis of purified human immunodeficiency virus type 1 produced from infected monocyte-derived macrophages,” Journal of Virology, vol. 80, no. 18, pp. 9039–9052, 2006.
[89]
D. R. M. Graham, E. Chertova, J. M. Hilburn, L. O. Arthur, and J. E. K. Hildreth, “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, vol. 77, no. 15, pp. 8237–8248, 2003.
[90]
D. E. Ott, “Cellular proteins detected in HIV-1,” Reviews in Medical Virology, vol. 18, no. 3, pp. 159–175, 2008.
[91]
M. Saifuddin, C. J. Parker, M. E. Peeples et al., “Role of virion-associated glycosylphosphatidylinositol-linked proteins CD55 and CD59 in complement resistance of cell line-derived and primary isolates of HIV-1,” Journal of Experimental Medicine, vol. 182, no. 2, pp. 501–509, 1995.
[92]
Z. Mujawar, H. Rose, M. P. Morrow et al., “Human immunodeficiency virus impairs reverse cholesterol transport from macrophages.,” PLoS biology, vol. 4, no. 11, Article ID e365, 2006.
[93]
Y. H. Zheng, A. Plemenitas, C. J. Fielding, and B. M. Peterlin, “Nef increases the synthesis of and transports cholesterol to lipid rafts and HIV-1 progeny virions,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 14, pp. 8460–8465, 2003.
[94]
Y. H. Zheng, A. Plemenitas, T. Linnemann, O. T. Fackler, and B. M. Peterlin, “Nef increases infectivity of HIV via lipid rafts,” Current Biology, vol. 11, no. 11, pp. 875–879, 2001.
[95]
T. Nitta, Y. Kuznetsov, A. McPherson, and H. Fan, “Murine leukemia virus glycosylated Gag (gPr80gag) facilitates interferon-sensitive virus release through lipid rafts,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 3, pp. 1190–1195, 2010.
[96]
C. Dietrich, L. A. Bagatolli, Z. N. Volovyk et al., “Lipid rafts reconstituted in model membranes,” Biophysical Journal, vol. 80, no. 3, pp. 1417–1428, 2001.
[97]
M. Lorizate, B. Brügger, H. Akiyama et al., “Probing HIV-1 membrane liquid order by Laurdan staining reveals producer cell-dependent differences,” Journal of Biological Chemistry, vol. 284, no. 33, pp. 22238–22247, 2009.
[98]
S. Charrin, F. Le Naour, O. Silvie, P. E. Milhiet, C. Boucheix, and E. Rubinstein, “Lateral organization of membrane proteins: tetraspanins spin their web,” Biochemical Journal, vol. 420, no. 2, pp. 133–154, 2009.
[99]
M. Yá？ez-Mó, O. Barreiro, M. Gordon-Alonso, M. Sala-Valdés, and F. Sánchez-Madrid, “Tetraspanin-enriched microdomains: a functional unit in cell plasma membranes,” Trends in Cell Biology, vol. 19, no. 9, pp. 434–446, 2009.
[100]
F. Berditchevski, K. F. Tolias, K. Wong, C. L. Carpenter, and M. E. Hemler, “A novel link between integrins, transmembrane-4 superfamily proteins (CD63 and CD81), and phosphatidylinositol 4-kinase,” Journal of Biological Chemistry, vol. 272, no. 5, pp. 2595–2598, 1997.
[101]
P. Gluschankof, I. Mondor, H. R. Gelderblom, and Q. J. Sattentau, “Cell membrane vesicles are a major contaminant of gradient-enriched human immunodeficiency virus type-1 preparations,” Virology, vol. 230, no. 1, pp. 125–133, 1997.
[102]
S. Khurana, D. N. Krementsov, A. De Parseval, J. H. Elder, M. Foti, and M. Thali, “Human immunodeficiency virus type 1 and influenza virus exit via different membrane microdomains,” Journal of Virology, vol. 81, no. 22, pp. 12630–12640, 2007.
[103]
T. Meerloo, H. K. Parmentier, A. D. M. E. Osterhaus, J. Goudsmit, and H. J. Schuurman, “Modulation of cell surface molecules during HIV-1 infection of H9 cells. An immunoelectron microscopic study,” AIDS, vol. 6, no. 10, pp. 1105–1116, 1992.
[104]
T. Meerloo, M. A. Sheikh, A. C. Bloem et al., “Host cell membrane proteins on human immunodeficiency virus type 1 after in vitro infection of H9 cells and blood mononuclear cells. An immuno-electron microscopic study,” Journal of General Virology, vol. 74, no. 1, pp. 129–135, 1993.
[105]
D. G. Nguyen, A. Booth, S. J. Gould, and J. E. K. Hildreth, “Evidence that HIV budding in primary macrophages occurs through the exosome release pathway,” Journal of Biological Chemistry, vol. 278, no. 52, pp. 52347–52354, 2003.
[106]
R. J. Orentas and J. E. K. Hildreth, “Association of host cell surface adhesion receptors and other membrane proteins with HIV and SIV,” AIDS Research and Human Retroviruses, vol. 9, no. 11, pp. 1157–1165, 1993.
[107]
K. Sato, J. Aoki, N. Misawa et al., “Modulation of human immunodeficiency virus type 1 infectivity through incorporation of tetraspanin proteins,” Journal of Virology, vol. 82, no. 2, pp. 1021–1033, 2008.
[108]
B. Grigorov, V. Attuil-Audenis, F. Perugi et al., “A role for CD81 on the late steps of HIV-1 replication in a chronically infected T cell line,” Retrovirology, vol. 6, p. 28, 2009.
[109]
H. Chen, N. Dziuba, B. Friedrich et al., “A critical role for CD63 in HIV replication and infection of macrophages and cell lines,” Virology, vol. 379, no. 2, pp. 191–196, 2008.
[110]
D. N. Krementsov, J. Weng, M. Lambelé, N. H. Roy, and M. Thali, “Tetraspanins regulate cell-to-cell transmission of HIV-1,” Retrovirology, vol. 6, p. 64, 2009.
[111]
E. Ruiz-Mateos, A. Pelchen-Matthews, M. Deneka, and M. Marsh, “CD63 is not required for production of infectious human immunodeficiency virus type 1 in human macrophages,” Journal of Virology, vol. 82, no. 10, pp. 4751–4761, 2008.
[112]
Y. Fang, N. Wu, X. Gan, W. Yan, J. C. Morrell, and S. J. Gould, “Higher-order oligomerization targets plasma membrane proteins and HIV gag to exosomes.,” PLoS biology, vol. 5, no. 6, Article ID e158, 2007.
[113]
B. Shen, N. Wu, M. Yang, and S. J. Gould, “Protein targeting to exosomes/microvesicles by plasma membrane anchors,” Journal of Biological Chemistry, vol. 286, no. 16, pp. 14383–14395, 2011.
[114]
M. F. Langhorst, A. Reuter, and C. A. O. Stuermer, “Scaffolding microdomains and beyond: the function of reggie/flotillin proteins,” Cellular and Molecular Life Sciences, vol. 62, no. 19-20, pp. 2228–2240, 2005.
[115]
R. G. Parton and K. Simons, “The multiple faces of caveolae,” Nature Reviews Molecular Cell Biology, vol. 8, no. 3, pp. 185–194, 2007.
[116]
O. Barreiro, M. Zamai, M. Yá？ez-Mó et al., “Endothelial adhesion receptors are recruited to adherent leukocytes by inclusion in preformed tetraspanin nanoplatforms,” Journal of Cell Biology, vol. 183, no. 3, pp. 527–542, 2008.
[117]
S. Charrin, S. Manié, M. Oualid, M. Billard, C. Boucheix, and E. Rubinstein, “Differential stability of tetraspanin/tetraspanin interactions: role of palmitoylation,” FEBS Letters, vol. 516, no. 1–3, pp. 139–144, 2002.
[118]
C. Claas, C. S. Stipp, and M. E. Hemler, “Evaluation of prototype transmembrane 4 superfamily protein complexes and their relation to lipid rafts,” Journal of Biological Chemistry, vol. 276, no. 11, pp. 7974–7984, 2001.
[119]
C. Espenel, E. Margeat, P. Dosset et al., “Single-molecule analysis of CD9 dynamics and partitioning reveals multiple modes of interaction in the tetraspanin web,” Journal of Cell Biology, vol. 182, no. 4, pp. 765–776, 2008.
[120]
F. Le Naour, M. André, C. Boucheix, and E. Rubinstein, “Membrane microdomains and proteomics: lessons from tetraspanin microdomains and comparison with lipid rafts,” Proteomics, vol. 6, no. 24, pp. 6447–6454, 2006.
[121]
K. Gousset, S.D. Ablan, L.V. Coren et al., “Real-time visualization of HIV-1 GAG trafficking in infected macrophages,” PLoS Pathogens, vol. 4, no. 3, Article ID e1000015, 2008.
[122]
F. Groot, S. Welsch, and Q. J. Sattentau, “Efficient HIV-1 transmission from macrophages to T cells across transient virological synapses,” Blood, vol. 111, no. 9, pp. 4660–4663, 2008.
[123]
N. Sharova, C. Swingler, M. Sharkey, and M. Stevenson, “Macrophages archive HIV-1 virions for dissemination in trans,” EMBO Journal, vol. 24, no. 13, pp. 2481–2489, 2005.
[124]
J. F. Arrighi, M. Pion, E. Garcia et al., “DC-SIGN-mediated infectious synapse formation enhances X4 HIV-1 transmission from dendritic cells to T cells,” Journal of Experimental Medicine, vol. 200, no. 10, pp. 1279–1288, 2004.
[125]
R. L. Felts, K. Narayan, J. D. Estes et al., “3D visualization of HIV transfer at the virological synapse between dendritic cells and T cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 30, pp. 13336–13341, 2010.
[126]
E. Garcia, M. Pion, A. Pelchen-Matthews et al., “HIV-1 trafficking to the dendritic cell-T-cell infectious synapse uses a pathway of tetraspanin sorting to the immunological synapse,” Traffic, vol. 6, no. 6, pp. 488–501, 2005.
[127]
D. McDonald, L. Wu, S. M. Bohks, V. N. KewalRamani, D. Unutmaz, and T. J. Hope, “Recruitment of HIV and its receptors to dendritic cell-T cell junctions,” Science, vol. 300, no. 5623, pp. 1295–1297, 2003.
[128]
H. J. Yu, M. A. Reuter, and D. McDonald, “HIV traffics through a specialized, surface-accessible intracellular compartment during trans-infection of T cells by mature dendritic cells,” PLoS pathogens, vol. 4, no. 8, p. e1000134, 2008.
[129]
P. Chen, W. Hübner, M. A. Spinelli, and B. K. Chen, “Predominant mode of human immunodeficiency virus transfer between T cells is mediated by sustained Env-dependent neutralization-resistant virological synapses,” Journal of Virology, vol. 81, no. 22, pp. 12582–12595, 2007.
[130]
N. Martin, S. Welsch, C. Jolly, J. A. G. Briggs, D. Vaux, and Q. J. Sattentau, “Virological synapse-mediated spread of human immunodeficiency virus type 1 between T cells is sensitive to entry inhibition,” Journal of Virology, vol. 84, no. 7, pp. 3516–3527, 2010.
[131]
G. Bu, P. A. Morton, and A. L. Schwartz, “Receptor-mediated endocytosis of plasminogen activators,” Advances in Molecular and Cell Biology, vol. 8, no. C, pp. 87–131, 1994.
[132]
M. Sourisseau, N. Sol-Foulon, F. Porrot, F. Blanchet, and O. Schwartz, “Inefficient human immunodeficiency virus replication in mobile lymphocytes,” Journal of Virology, vol. 81, no. 2, pp. 1000–1012, 2007.
[133]
D. Mazurov, A. Ilinskaya, G. Heidecker, P. Lloyd, and D. Derse, “Quantitative comparison of HTLV-1 and HIV-1 cell-to-cell infection with new replication dependent vectors,” PLoS Pathogens, vol. 6, no. 2, Article ID e1000788, 2010.
[134]
T. Igakura, J. C. Stinchcombe, P. K. C. Goon et al., “Spread of HTLV-I between lymphocytes by virus-induced polarization of the cytoskeleton,” Science, vol. 299, no. 5613, pp. 1713–1716, 2003.
[135]
A. M. Pais-Correia, M. Sachse, S. Guadagnini et al., “Biofilm-like extracellular viral assemblies mediate HTLV-1 cell-to-cell transmission at virological synapses,” Nature Medicine, vol. 16, no. 1, pp. 83–89, 2010.
[136]
E. Majorovits, M. Nejmeddine, Y. Tanaka, G. P. Taylor, S. D. Fuller, and C. R. M. Bangham, “Human T-Lymphotropic Virus-1 visualized at the virological synapse by electron tomography,” PLoS ONE, vol. 3, no. 5, Article ID e2251, 2008.
[137]
J. Jin, N. M. Sherer, G. Heidecker, D. Derse, and W. Mothes, “Assembly of the murine leukemia virus is directed towards sites of cell-cell contact,” PLoS Biology, vol. 7, no. 7, Article ID e1000163, 2009.
[138]
N. M. Sherer, M. J. Lehmann, L. F. Jimenez-Soto, C. Horensavitz, M. Pypaert, and W. Mothes, “Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission,” Nature Cell Biology, vol. 9, no. 3, pp. 310–315, 2007.
[139]
N. M. Sherer and W. Mothes, “Cytonemes and tunneling nanotubules in cell-cell communication and viral pathogenesis,” Trends in Cell Biology, vol. 18, no. 9, pp. 414–420, 2008.
[140]
W. Mothes, N. M. Sherer, J. Jin, and P. Zhong, “Virus cell-to-cell transmission,” Journal of Virology, vol. 84, no. 17, pp. 8360–8368, 2010.
[141]
Q. Sattentau, “Avoiding the void: cell-to-cell spread of human viruses,” Nature Reviews Microbiology, vol. 6, no. 11, pp. 815–826, 2008.
[142]
A. Sigal, J.T. Kim, A.B. Balazs et al., “Cell-to-cell spread of HIV permits ongoing replication despite antiretroviral therapy,” Nature, vol. 477, no. 7362, pp. 95–99, 2011.
[143]
S. Sowinski, C. Jolly, O. Berninghausen et al., “Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission,” Nature Cell Biology, vol. 10, no. 2, pp. 211–219, 2008.
[144]
W. Hübner, G. P. McNerney, P. Chen et al., “Quantitative 3D video microscopy of HIV transfer across T cell virological synapses,” Science, vol. 323, no. 5922, pp. 1743–1747, 2009.
[145]
C. Jolly, K. Kashefi, M. Hollinshead, and Q. J. Sattentau, “HIV-1 Cell to cell transfer across an Env-induced, actin-dependent synapse,” Journal of Experimental Medicine, vol. 199, no. 2, pp. 283–293, 2004.
[146]
D. Rudnicka, J. Feldmann, F. Porrot et al., “Simultaneous cell-to-cell transmission of human immunodeficiency virus to multiple targets through polysynapses,” Journal of Virology, vol. 83, no. 12, pp. 6234–6246, 2009.
[147]
I. Puigdomènech, M. Massanella, N. Izquierdo-Useros et al., “HIV transfer between CD4 T cells does not require LFA-1 binding to ICAM-1 and is governed by the interaction of HIV envelope glycoprotein with CD4,” Retrovirology, vol. 5, p. 32, 2008.
[148]
G. Vasiliver-Shamis, M. Tuen, T. W. Wu et al., “Human immunodeficiency virus type 1 envelope gp120 induces a stop signal and virological synapse formation in noninfected CD4+ T cells,” Journal of Virology, vol. 82, no. 19, pp. 9445–9457, 2008.
[149]
M. Massanella, I. Puigdoménech, C. Cabrera et al., “Antigp41 antibodies fail to block early events of virological synapses but inhibit HIV spread between T cells,” AIDS, vol. 23, no. 2, pp. 183–188, 2009.
[150]
B.M. Dale, G.P. McNerney, D.L. Thompson et al., “Cell-to-cell transfer of HIV-1 via virological synapses leads to endosomal virion maturation that activates viral membrane fusion,” Cell Host and Microbe, vol. 10, no. 6, pp. 551–562, 2011.
[151]
C. Jolly, I. Mitar, and Q. J. Sattentau, “Adhesion molecule interactions facilitate human immunodeficiency virus type 1-induced virological synapse formation between T cells,” Journal of Virology, vol. 81, no. 24, pp. 13916–13921, 2007.
[152]
C. Jolly, I. Mitar, and Q. J. Sattentau, “Requirement for an intact T-cell actin and tubulin cytoskeleton for efficient assembly and spread of human immunodeficiency virus type 1,” Journal of Virology, vol. 81, no. 11, pp. 5547–5560, 2007.
[153]
M. Lehmann, D.S. Nikolic, and V. Piguet, “How HIV-1 takes advantage of the cytoskeleton during replication and cell-to-cell transmission,” Viruses, vol. 3, no. 9, pp. 1757–1776, 2011.
[154]
M. Nejmeddine and C. R. M. Bangham, “The HTLV-1 virological synapse,” Viruses, vol. 2, no. 7, pp. 1427–1447, 2010.
[155]
C. Jolly, S. Welsch, S. Michor, and Q.J. Sattentau, “The regulated secretory pathway in cd4+ t cells contributes to human immunodeficiency virus type-1 cell-to-cell spread at the virological synapse,” PLoS Pathogens, vol. 7, no. 9, Article ID e1002226, 2011.
[156]
N. Blanchard, V. Di Bartolo, and C. Hivroz, “In the immune synapse, ZAP-70 controls T cell polarization and recruitment of signaling proteins but not formation of the synaptic pattern,” Immunity, vol. 17, no. 4, pp. 389–399, 2002.
[157]
N. Sol-Foulon, M. Sourisseau, F. Porrot et al., “ZAP-70 kinase regulates HIV cell-to-cell spread and virological synapse formation,” EMBO Journal, vol. 26, no. 2, pp. 516–526, 2007.
[158]
G. N. Llewellyn, I. B. Hogue, J. R. Grover, and A. Ono, “Nucleocapsid promotes localization of HIV-1 gag to uropods that participate in virological synapses between T cells,” PLoS pathogens, vol. 6, no. 10, p. e1001167, 2010.
[159]
C. Jolly and Q. J. Sattentau, “Human immunodeficiency virus type 1 virological synapse formation in T cells requires lipid raft integrity,” Journal of Virology, vol. 79, no. 18, pp. 12088–12094, 2005.
[160]
C. Jolly and Q. J. Sattentau, “Human immunodeficiency virus type 1 assembly, budding, and cell-cell spread in T cells take place in tetraspanin-enriched plasma membrane domains,” Journal of Virology, vol. 81, no. 15, pp. 7873–7884, 2007.
[161]
J. Weng, D. N. Krementsov, S. Khurana, N. H. Roy, and M. Thali, “Formation of syncytia is repressed by tetraspanins in human immunodeficiency virus type 1-producing cells,” Journal of Virology, vol. 83, no. 15, pp. 7467–7474, 2009.
[162]
M. Bajénoff, J. G. Egen, L. Y. Koo et al., “Stromal cell networks regulate lymphocyte entry, migration, and territoriality in lymph nodes,” Immunity, vol. 25, no. 6, pp. 989–1001, 2006.
[163]
S. Hugues, L. Fetler, L. Bonifaz, J. Helft, F. Amblard, and S. Amigorena, “Distinct T cell dynamics in lymph nodes during the induction of tolerance and immunity,” Nature Immunology, vol. 5, no. 12, pp. 1235–1242, 2004.
[164]
T. R. Mempel, S. E. Henrickson, and U. H. Von Andrian, “T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases,” Nature, vol. 427, no. 6970, pp. 154–159, 2004.
[165]
M. J. Miller, S. H. Wei, M. D. Cahalan, and I. Parker, “Autonomous T cell trafficking examined in vivo with intravital two-photon microscopy,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 5, pp. 2604–2609, 2003.
[166]
M. J. Miller, S. H. Wei, I. Parker, and M. D. Cahalan, “Two-photon imaging of lymphocyte motility and antigen response in intact lymph node,” Science, vol. 296, no. 5574, pp. 1869–1873, 2002.
[167]
M. F. Krummel and I. Macara, “Maintenance and modulation of T cell polarity,” Nature Immunology, vol. 7, no. 11, pp. 1143–1149, 2006.
[168]
F. Sánchez-Madrid and M. A. Del Pozo, “Leukocyte polarization in cell migration and immune interactions,” EMBO Journal, vol. 18, no. 3, pp. 501–511, 1999.
[169]
F. Sánchez-Madrid and J. M. Serrador, “Bringing up the rear: defining the roles of the uropod,” Nature Reviews Molecular Cell Biology, vol. 10, no. 5, pp. 353–359, 2009.
[170]
W. Mcfarland and D. H. Heilman, “Lymphocyte foot appendage: its role in lymphocyte function and in immunological reactions,” Nature, vol. 205, no. 4974, pp. 887–888, 1965.
[171]
M.A. Del Pozo, C. Caba？as, M.C. Montoya, A. Ager, P. Sánchez-Mateos, and F. Sánchez-Madrid, “ICAMs redistributed by chemokines to cellular uropods as a mechanism for recruitment of T lymphocytes,” Journal of Cell Biology, vol. 137, no. 2, pp. 493–508, 1997.
[172]
B. Shen, Y. Fang, N. Wu, and S. J. Gould, “Biogenesis of the posterior pole is mediated by the exosome/microvesicle protein-sorting pathway,” Journal of Biological Chemistry, vol. 286, no. 51, pp. 44162–44176, 2011.
[173]
R. B. Taylor, W. P. Duffus, M. C. Raff, and S. de Petris, “Redistribution and pinocytosis of lymphocyte surface immunoglobulin molecules induced by anti-immunoglobulin antibody,” Nature: New biology, vol. 233, no. 42, pp. 225–229, 1971.
[174]
S. Kellie, B. Patel, E. J. Pierce, and D. R. Critchley, “Capping of cholera toxin-ganglioside GM1 complexes on mouse lymphocytes is accompanied by co-capping of alpha-actinin,” Journal of Cell Biology, vol. 97, no. 2, pp. 447–454, 1983.
[175]
T. Révész and M. Greaves, “Ligand-induced redistribution of lymphocyte membrane ganglioside GM1,” Nature, vol. 257, no. 5522, pp. 103–106, 1975.
[176]
J. H. Lee, T. Katakai, T. Hara, H. Gonda, M. Sugai, and A. Shimizu, “Roles of p-ERM and Rho-ROCK signalling in lymphocyte polarity and uropod formation,” Journal of Cell Biology, vol. 167, no. 2, pp. 327–337, 2004.
[177]
L. Y. W. Bourguignon and S. J. Singer, “Transmembrane interactions and the mechanism of capping of surface receptors by their specific ligands,” Proceedings of the National Academy of Sciences of the United States of America, vol. 74, no. 11, pp. 5031–5035, 1977.
[178]
Y. Cai, N. Biais, G. Giannone et al., “Nonmuscle myosin IIA-dependent force inhibits cell spreading and drives F-actin flow,” Biophysical Journal, vol. 91, no. 10, pp. 3907–3920, 2006.
[179]
B. F. Holifield, A. Ishihara, and K. Jacobson, “Comparative behavior of membrane protein-antibody complexes on motile fibroblasts: Implications for a mechanism of capping,” Journal of Cell Biology, vol. 111, no. 6, pp. 2499–2512, 1990.
[180]
G. F. Schreiner, K. Fujiwara, T. D. Pollard, and E. R. Unanue, “Redistribution of myosin accompanying capping of surface Ig,” Journal of Experimental Medicine, vol. 145, no. 5, pp. 1393–1398, 1977.
[181]
W. Shih and S. Yamada, “Myosin IIA dependent retrograde flow drives 3D cell migration,” Biophysical Journal, vol. 98, no. 8, pp. L29–L31, 2010.
[182]
B. Liu, R. Dai, C.-J. Tian, L. Dawson, R. Gorelick, and X.-F. Yu, “Interaction of the human immunedeficiency virus type 1 nucleocapsid with actin,” Journal of Virology, vol. 73, no. 4, pp. 2901–2908, 1999.
[183]
T. Wilk, B. Gowen, and S. D. Fuller, “Actin associates with the nucleocapsid domain of the human immunodeficiency virus Gag polyprotein,” Journal of Virology, vol. 73, no. 3, pp. 1931–1940, 1999.
[184]
S. C. Hatch, J. Archer, and S. Gummuluru, “Glycosphingolipid composition of Human Immunodeficiency Virus type 1 (HIV-1) particles is a crucial determinant for dendritic cell-mediated HIV-1 trans-infection,” Journal of Virology, vol. 83, no. 8, pp. 3496–3506, 2009.
[185]
S. McLaughlin and D. Murray, “Plasma membrane phosphoinositide organization by protein electrostatics,” Nature, vol. 438, no. 7068, pp. 605–611, 2005.
[186]
G. Van Den Bogaart, K. Meyenberg, H.J. Risselada et al., “Membrane protein sequestering by ionic protein-lipid interactions,” Nature, vol. 479, no. 7374, pp. 552–555, 2011.
