HIV-1 gag associates with specific uropod-directed microdomains in a manner dependent on its MA highly basic region

Journal of Virology

Volumn 87, Issue 11, 2013, Pages 6441-6454

  Llewellyn, G Nicholas ^a,b   Grover, Jonathan R ^a   Olety, Balaji ^a   Ono, Akira ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD59 ANTIGEN; GAG PROTEIN; HERMES ANTIGEN; INTERCELLULAR ADHESION MOLECULE 1; INTERCELLULAR ADHESION MOLECULE 3; LEUKOSIALIN; P SELECTIN GLYCOPROTEIN LIGAND 1; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE;

ARTICLE; CONTROLLED STUDY; DIMERIZATION; HUMAN IMMUNODEFICIENCY VIRUS 1; MATRIX; NONHUMAN; PLASMID; POLARIZATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; UROPOD DIRECTED MICRODOMAIN; VIRUS RELEASE;

CELL ADHESION MOLECULES; CELL LINE; CELL POLARITY; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV INFECTIONS; HIV-1; HUMANS; MEMBRANE MICRODOMAINS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; T-LYMPHOCYTES;

EID: 84878166615     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00040-13     Document Type: Article

References (106)

1. Chen P, Hubner W, Spinelli MA, Chen BK. 2007. Predominant mode of human immunodeficiency virus transfer between T cells is mediated by sustained Env-dependent neutralization-resistant virological synapses. J. Virol. 81:12582-12595.
2. Dimitrov DS, Willey RL, Sato H, Chang LJ, Blumenthal R, Martin MA. 1993. Quantitation of human immunodeficiency virus type 1 infection kinetics. J. Virol. 67:2182-2190.
3. Hübner W, McNerney GP, Chen P, Dale BM, Gordon RE, Chuang FYS, Li XD, Asmuth DM, Huser T, Chen BK. 2009. Quantitative 3D video microscopy of HIV transfer across T cell virological synapses. Science 323:1743-1747.
4. Martin N, Welsch S, Jolly C, Briggs JAG, Vaux D, Sattentau QJ. 2010. Virological synapse-mediated spread of human immunodeficiency virus type 1 between T cells is sensitive to entry inhibition. J. Virol. 84:3516-3527.
5. Mazurov D, Ilinskaya A, Heidecker G, Lloyd P, Derse D. 2010. Quantitative comparison of HTLV-1 and HIV-1 cell-to-cell infection with new replication dependent vectors. PLoS Pathog. 6:e1000788. doi: 10.1371/journal.ppat.1000788.
6. Jolly C, Kashefi K, Hollinshead M, Sattentau QJ. 2004. HIV-1 cell to cell transfer across an Env-induced, actin-dependent synapse. J. Exp. Med. 199:283-293.
7. Igakura T, Stinchcombe JC, Goon PK, Taylor GP, Weber JN, Griffiths GM, Tanaka Y, Osame M, Bangham CR. 2003. Spread of HTLV-I between lymphocytes by virus-induced polarization of the cytoskeleton. Science 299:1713-1716.
8. Sewald X, Gonzalez DG, Haberman AM, Mothes W. 2012. In vivo imaging of virological synapses. Nat. Commun. 3:1320.
9. Murooka TT, Deruaz M, Marangoni F, Vrbanac VD, Seung E, von Andrian UH, Tager AM, Luster AD, Mempel TR. 2012. HIV-infected T cells are migratory vehicles for viral dissemination. Nature 490:283-287.
10. Bajénoff M, Egen JG, Koo LY, Laugier JP, Brau F, Glaichenhaus N, Germain RN. 2006. Stromal cell networks regulate lymphocyte entry, migration, and territoriality in lymph nodes. Immunity 25:989-1001.
11. Hugues S, Fetler L, Bonifaz L, Helft J, Amblard F, Amigorena S. 2004. Distinct T cell dynamics in lymph nodes during the induction of tolerance and immunity. Nat. Immunol. 5:1235-1242.
12. Miller MJ, Wei SH, Cahalan MD, Parker I. 2003. Autonomous T cell trafficking examined in vivo with intravital two-photon microscopy. Proc. Natl. Acad. Sci. U. S. A. 100:2604-2609.
13. Miller MJ, Wei SH, Parker I, Cahalan MD. 2002. Two-photon imaging of lymphocyte motility and antigen response in intact lymph node. Science 296:1869-1873.
14. Mrass P, Takano H, Ng LG, Daxini S, Lasaro MO, Iparraguirre A, Cavanagh LL, von Andrian UH, Ertl HC, Haydon PG, Weninger W. 2006. Random migration precedes stable target cell interactions of tumor-infiltrating T cells. J. Exp. Med. 203:2749-2761.
15. Alonso-Lebrero JL, Serrador JM, Dominguez-Jimenez C, Barreiro O, Luque A, del Pozo MA, Snapp K, Kansas G, Schwartz-Albiez R, Furthmayr H, Lozano F, Sanchez-Madrid F. 2000. Polarization and interaction of adhesion molecules P-selectin glycoprotein ligand 1 and intercellular adhesion molecule 3 with moesin and ezrin in myeloid cells. Blood 95:2413-2419.
16. Sánchez-Madrid F, del Pozo MA. 1999. Leukocyte polarization in cell migration and immune interactions. EMBO J. 18:501-511.
17. Rosenman SJ, Ganji AA, Tedder TF, Gallatin WM. 1993. Syn-capping of human T lymphocyte adhesion/activation molecules and their redistribution during interaction with endothelial cells. J. Leukoc. Biol. 53:1-10.
18. del Pozo MA, Sánchez-Mateos P, Nieto M, Sánchez-Madrid F. 1995. Chemokines regulate cellular polarization and adhesion receptor redistribution during lymphocyte interaction with endothelium and extracellular matrix. Involvement of cAMP signaling pathway. J. Cell Biol. 131: 495-508.
19. Serrador JM, Urzainqui A, Alonso-Lebrero JL, Cabrero JR, Montoya MC, Vicente-Manzanares M, Yanez-Mo M, Sanchez-Madrid F. 2002. A juxta-membrane amino acid sequence of P-selectin glycoprotein ligand-1 is involved in moesin binding and ezrin/radixin/moesin-directed targeting at the trailing edge of migrating lymphocytes. Eur. J. Immunol. 32:1560-1566.
20. McFarland W, Heilman DH. 1965. Lymphocyte foot appendage: its role in lymphocyte function and in immunological reactions. Nature 205: 887-888.
21. del Pozo MA, Cabanas C, Montoya MC, Ager A, Sanchez-Mateos P, Sanchez-Madrid F. 1997. ICAMs redistributed by chemokines to cellular uropods as a mechanism for recruitment of T lymphocytes. J. Cell Biol. 137:493-508.
22. Sánchez-Madrid F, Serrador JM. 2009. Bringing up the rear: defining the roles of the uropod. Nat. Rev. Mol. Cell Biol. 10:353-359.
23. Llewellyn GN, Hogue IB, Grover JR, Ono A. 2010. Nucleocapsid promotes localization of HIV-1 gag to uropods that participate in virological synapses between T cells. PLoS Pathog. 6:e1001167. doi:10.1371/journal.ppat.1001167.
24. Balasubramaniam M, Freed EO. 2011. New insights into HIV assembly and trafficking. Physiology (Bethesda) 26:236-251.
25. Bieniasz PD. 2009. The cell biology of HIV-1 virion genesis. Cell Host Microbe 5:550-558.
26. Chukkapalli V, Ono A. 2011. Molecular determinants that regulate plasma membrane association of HIV-1 Gag. J. Mol. Biol. 410:512-524.
27. Datta SA, Zhao Z, Clark PK, Tarasov S, Alexandratos JN, Campbell SJ, Kvaratskhelia M, Lebowitz J, Rein A. 2007. Interactions between HIV-1 Gag molecules in solution: an inositol phosphate-mediated switch. J. Mol. Biol. 365:799-811.
28. Gamble TR, Yoo SH, Vajdos FF, von Schwedler UK, Worthylake DK, Wang H, McCutcheon JP, Sundquist WI, Hill CP. 1997. Structure of the carboxyl-terminal dimerization domain of the HIV-1 capsid protein. Science 278:849-853.
29. Hogue IB, Hoppe A, Ono A. 2009. 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. J. Virol. 83:7322-7336.
30. von Schwedler UK, Stray KM, Garrus JE, Sundquist WI. 2003. Functional surfaces of the human immunodeficiency virus type 1 capsid protein. J. Virol. 77:5439-5450.
31. Zhang WH, Hockley DJ, Nermut MV, Morikawa Y, Jones IM. 1996. Gag-Gag interactions in the C-terminal domain of human immunodeficiency virus type 1 p24 capsid antigen are essential for Gag particle assembly. J. Gen. Virol. 77:743-751.
32. Burniston MT, Cimarelli A, Colgan J, Curtis SP, Luban J. 1999. Human immunodeficiency virus type 1 Gag polyprotein multimerization requires the nucleocapsid domain and RNA and is promoted by the capsid-dimer interface and the basic region of matrix protein. J. Virol. 73:8527-8540.
33. Campbell S, Vogt VM. 1995. Self-assembly in vitro of purified Ca-Nc proteins from Rous sarcoma virus and human immunodeficiency virus type 1. J. Virol. 69:6487-6497.
34. Cimarelli A, Sandin S, Hoglund S, Luban J. 2000. Basic residues in human immunodeficiency virus type 1 nucleocapsid promote virion assembly via interaction with RNA. J. Virol. 74:3046-3057.
35. Dawson L, Yu XF. 1998. The role of nucleocapsid of HIV-1 in virus assembly. Virology 251:141-157.
36. Campbell S, Rein A. 1999. In vitro assembly properties of human immunodeficiency virus type 1 Gag protein lacking the p6 domain. J. Virol. 73:2270-2279.
37. Muriaux D, Mirro J, Harvin D, Rein A. 2001. RNA is a structural element in retrovirus particles. Proc. Natl. Acad. Sci. U. S. A. 98:5246-5251.
38. D'Souza V, Summers MF. 2005. How retroviruses select their genomes. Nat. Rev. Microbiol. 3:643-655.
39. Weiss ER, Gottlinger H. 2011. The role of cellular factors in promoting HIV budding. J. Mol. Biol. 410:525-533.
40. Bryant M, Ratner L. 1990. Myristoylation-dependent replication and assembly of human immunodeficiency virus 1. Proc. Natl. Acad. Sci. U. S. A. 87:523-527.
41. Göttlinger HG, Sodroski JG, Haseltine WA. 1989. Role of capsid precursor processing and myristoylation in morphogenesis and infectivity of human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. U. S. A. 86:5781-5785.
42. Tang C, Loeliger E, Luncsford P, Kinde I, Beckett D, Summers MF. 2004. Entropic switch regulates myristate exposure in the HIV-1 matrix protein. Proc. Natl. Acad. Sci. U. S. A. 101:517-522.
43. Zhou W, Resh MD. 1996. Differential membrane binding of the human immunodeficiency virus type 1 matrix protein. J. Virol. 70:8540-8548.
44. Dalton AK, Ako-Adjei D, Murray PS, Murray D, Vogt VM. 2007. Electrostatic interactions drive membrane association of the human immunodeficiency virus type 1 Gag MA domain. J. Virol. 81:6434-6445.
45. Zhou WJ, Parent LJ, Wills JW, Resh MD. 1994. Identification of a membrane-binding domain within the amino-terminal region of human immunodeficiency virus type 1 Gag protein which interacts with acidic phospholipids. J. Virol. 68:2556-2569.
46. Yuan X, Yu XF, Lee TH, Essex M. 1993. Mutations in the N-terminal region of human immunodeficiency virus type 1 matrix protein block intracellular transport of the Gag precursor. J. Virol. 67:6387-6394.
47. Ono A, Orenstein JM, Freed EO. 2000. Role of the gag matrix domain in targeting human immunodeficiency virus type 1 assembly. J. Virol. 74:2855-2866.
48. Chukkapalli V, Oh SJ, Ono A. 2010. Opposing mechanisms involving RNA and lipids regulate HIV-1 Gag membrane binding through the highly basic region of the matrix domain. Proc. Natl. Acad. Sci. U. S. A. 107:1600-1605.
49. Hill CP, Worthylake D, Bancroft DP, Christensen AM, Sundquist WI. 1996. Crystal structures of the trimeric human immunodeficiency virus type 1 matrix protein: implications for membrane association and assembly. Proc. Natl. Acad. Sci. U. S. A. 93:3099-3104.
50. Chukkapalli V, Hogue IB, Boyko V, Hu WS, Ono A. 2008. Interaction between the human immunodeficiency virus type 1 Gag matrix domain and phosphatidylinositol-(4,5)-bisphosphate is essential for efficient gag membrane binding. J. Virol. 82:2405-2417.
51. Ono A, Ablan SD, Lockett SJ, Nagashima K, Freed EO. 2004. Phosphatidylinositol (4,5) bisphosphate regulates HIV-1 gag targeting to the plasma membrane. Proc. Natl. Acad. Sci. U. S. A. 101:14889-14894.
52. Saad JS, Miller J, Tai J, Kim A, Ghanam RH, Summers MF. 2006. Structural basis for targeting HIV-1 Gag proteins to the plasma membrane for virus assembly. Proc. Natl. Acad. Sci. U. S. A. 103:11364-11369.
53. Alfadhli A, Still A, Barklis E. 2009. Analysis of human immunodefi-ciency virus type 1 matrix binding to membranes and nucleic acids. J. Virol. 83:12196-12203.
54. Chan R, Uchil PD, Jin J, Shui G, Ott DE, Mothes W, Wenk MR. 2008. Retroviruses human immunodeficiency virus and murine leukemia virus are enriched in phosphoinositides. J. Virol. 82:11228-11238.
55. Shkriabai N, Datta SA, Zhao Z, Hess S, Rein A, Kvaratskhelia M. 2006. Interactions of HIV-1 Gag with assembly cofactors. Biochemistry 45: 4077-4083.
56. Hogue IB, Llewellyn GN, Ono A. 2012. Dynamic association between HIV-1 Gag and membrane domains. Mol. Biol. Int. 2012:979765.
57. Lindwasser OW, Resh MD. 2001. Multimerization of human immunodeficiency virus type 1 Gag promotes its localization to barges, raft-like membrane microdomains. J. Virol. 75:7913-7924.
58. Nguyen DH, Hildreth JE. 2000. Evidence for budding of human immunodeficiency virus type 1 selectively from glycolipid-enriched membrane lipid rafts. J. Virol. 74:3264-3272.
59. Ono A, Freed EO. 2001. Plasma membrane rafts play a critical role in HIV-1 assembly and release. Proc. Natl. Acad. Sci. U. S. A. 98:13925-13930.
60. Lingwood D, Simons K. 2010. Lipid rafts as a membrane-organizing principle. Science 327:46-50.
61. Nydegger S, Khurana S, Krementsov DN, Foti M, Thali M. 2006. Mapping of tetraspanin-enriched microdomains that can function as gateways for HIV-1. J. Cell Biol. 173:795-807.
62. Booth AM, Fang Y, Fallon JK, Yang JM, Hildreth JE, Gould SJ. 2006. Exosomes and HIV Gag bud from endosome-like domains of the T cell plasma membrane. J. Cell Biol. 172:923-935.
63. Thali M. 2009. The roles of tetraspanins in HIV-1 replication. Curr. Top. Microbiol. Immunol. 339:85-102.
64. Claas C, Stipp CS, Hemler ME. 2001. Evaluation of prototype transmembrane 4 superfamily protein complexes and their relation to lipid rafts. J. Biol. Chem. 276:7974-7984.
65. Charrin S, Le Naour F, Silvie O, Milhiet PE, Boucheix C, Rubinstein E. 2009. Lateral organization of membrane proteins: tetraspanins spin their web. Biochem. J. 420:133-154.
66. Hogue IB, Grover JR, Soheilian F, Nagashima K, Ono A. 2011. Gag induces the coalescence of clustered lipid rafts and tetraspanin-enriched microdomains at HIV-1 assembly sites on the plasma membrane. J. Virol. 85:9749-9766.
67. Ley K, Zhang H. 2008. Dances with leukocytes: how tetraspaninenriched microdomains assemble to form endothelial adhesive platforms. J. Cell Biol. 183:375-376.
68. Barreiro O, Zamai M, Yanez-Mo M, Tejera E, Lopez-Romero P, Monk PN, Gratton E, Caiolfa VR, Sanchez-Madrid F. 2008. Endothelial adhesion receptors are recruited to adherent leukocytes by inclusion in preformed tetraspanin nanoplatforms. J. Cell Biol. 183:527-542.
69. Espenel C, Margeat E, Dosset P, Arduise C, Le Grimellec C, Royer CA, Boucheix C, Rubinstein E, Milhiet PE. 2008. Single-molecule analysis of CD9 dynamics and partitioning reveals multiple modes of interaction in the tetraspanin web. J. Cell Biol. 182:765-776.
70. Krementsov DN, Rassam P, Margeat E, Roy NH, Schneider-Schaulies J, Milhiet PE, Thali M. 2010. HIV-1 assembly differentially alters dynamics and partitioning of tetraspanins and raft components. Traffic 11:1401-1414.
71. Shen B, Fang Y, Wu N, Gould SJ. 2011. Biogenesis of the posterior pole is mediated by the exosome/microvesicle protein-sorting pathway. J. Biol. Chem. 286:44162-44176.
72. Fang Y, Wu N, Gan X, Yan W, Morrell JC, Gould SJ. 2007. Higherorder oligomerization targets plasma membrane proteins and HIV gag to exosomes. PLoS Biol. 5:e158. doi:10.1371/journal.pbio.0050158.
73. Lehmann MJ, Sherer NM, Marks CB, Pypaert M, Mothes W. 2005. Actin-and myosin-driven movement of viruses along filopodia precedes their entry into cells. J. Cell Biol. 170:317-325.
74. Sherer NM, Jin J, Mothes W. 2010. Directional spread of surfaceassociated retroviruses regulated by differential virus-cell interactions. J. Virol. 84:3248-3258.
75. Grover JR, Llewellyn GN, Soheilian F, Nagashima K, Veatch SL, Ono A. 2013. Roles played by capsid-dependent induction of membrane curvature and Gag-ESCRT interactions in tetherin recruitment to HIV-1 assembly sites. J. Virol. 87:4650-4664.
76. Accola MA, Strack B, Gottlinger HG. 2000. 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. J. Virol. 74:5395-5402.
77. Adachi A, Gendelman HE, Koenig S, Folks T, Willey R, Rabson A, Martin MA. 1986. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol. 59:284-291.
78. Kong LB, An D, Ackerson B, Canon J, Rey O, Chen IS, Krogstad P, Stewart PL. 1998. Cryoelectron microscopic examination of human immunodeficiency virus type 1 virions with mutations in the cyclophilin A binding loop. J. Virol. 72:4403-4407.
79. Auerbach MR, Brown KR, Kaplan A, de Las Nueces D, Singh IR. 2006. A small loop in the capsid protein of Moloney murine leukemia virus controls assembly of spherical cores. J. Virol. 80:2884-2893.
80. Crist RM, Datta SA, Stephen AG, Soheilian F, Mirro J, Fisher RJ, Nagashima K, Rein A. 2009. Assembly properties of human immunodeficiency virus type 1 Gag-leucine zipper chimeras: implications for retrovirus assembly. J. Virol. 83:2216-2225.
81. Zhang Y, Qian H, Love Z, Barklis E. 1998. Analysis of the assembly function of the human immunodeficiency virus type 1 gag protein nucleocapsid domain. J. Virol. 72:1782-1789.
82. Klein KC, Reed JC, Tanaka M, Nguyen VT, Giri S, Lingappa JR. 2011. HIV Gag-leucine zipper chimeras form ABCE1-containing intermediates and RNase-resistant immature capsids similar to those formed by wild-type HIV-1 Gag. J. Virol. 85:7419-7435.
83. Ono A, Waheed AA, Joshi A, Freed EO. 2005. 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. J. Virol. 79:14131-14140.
84. Guo XF, Roldan A, Hu J, Wainberg MA, Liang C. 2005. Mutation of the SP1 sequence impairs both multimerization and membrane-binding activities of human immunodeficiency virus type 1 Gag. J. Virol. 79:1803-1812.
85. Ono A, Freed EO. 1999. Binding of human immunodeficiency virus type 1 Gag to membrane: role of the matrix amino terminus. J. Virol. 73:4136-4144.
86. Saad JS, Loeliger E, Luncsford P, Liriano M, Tai J, Kim A, Miller J, Joshi A, Freed EO, Summers MF. 2007. Point mutations in the HIV-1 matrix protein turn off the myristyl switch. J. Mol. Biol. 366:574-585.
87. Liu J, Deng Y, Zheng Q, Cheng CS, Kallenbach NR, Lu M. 2006. A parallel coiled-coil tetramer with offset helices. Biochemistry 45:15224-15231.
88. Dou J, Wang JJ, Chen X, Li H, Ding L, Spearman P. 2009. Characterization of a myristoylated, monomeric HIV Gag protein. Virology 387: 341-352.
89. Langhorst MF, Reuter A, Stuermer CA. 2005. Scaffolding microdomains and beyond: the function of reggie/flotillin proteins. Cell. Mol. Life Sci. 62:2228-2240.
90. Parton RG, Simons K. 2007. The multiple faces of caveolae. Nat. Rev. Mol. Cell Biol. 8:185-194.
91. Ursell TS, Klug WS, Phillips R. 2009. Morphology and interaction between lipid domains. Proc. Natl. Acad. Sci. U. S. A. 106:13301-13306.
92. van den Bogaart G, Meyenberg K, Risselada HJ, Amin H, Willig KI, Hubrich BE, Dier M, Hell SW, Grubmuller H, Diederichsen U, Jahn R. 2011. Membrane protein sequestering by ionic protein-lipid interactions. Nature 479:552-555.
93. Grigorov B, Attuil-Audenis V, Perugi F, Nedelec M, Watson S, Pique C, Darlix JL, Conjeaud H, Muriaux D. 2009. A role for CD81 on the late steps of HIV-1 replication in a chronically infected T cell line. Retrovirology 6:28. doi:10.1186/1742-4690-6-28.
94. Jolly C, Sattentau QJ. 2005. Human immunodeficiency virus type 1 virological synapse formation in T cells requires lipid raft integrity. J. Virol. 79:12088-12094.
95. Jolly C, Sattentau QJ. 2007. Human immunodeficiency virus type 1 assembly, budding, and cell-cell spread in T cells take place in tetraspanin-enriched plasma membrane domains. J. Virol. 81:7873-7884.
96. Krementsov DN, Weng J, Lambele M, Roy NH, Thali M. 2009. Tetraspanins regulate cell-to-cell transmission of HIV-1. Retrovirology 6:64. doi:10.1186/1742-4690-6-64.
97. Rudnicka D, Feldmann J, Porrot F, Wietgrefe S, Guadagnini S, Prevost MC, Estaquier J, Haase AT, Sol-Foulon N, Schwartz O. 2009. Simultaneous cell-to-cell transmission of human immunodeficiency virus to multiple targets through polysynapses. J. Virol. 83:6234-6246.
98. Lindwasser OW, Resh MD. 2002. Myristoylation as a target for inhibiting HIV assembly: unsaturated fatty acids block viral budding. Proc. Natl. Acad. Sci. U. S. A. 99:13037-13042.
99. Ono A. 2010. Relationships between plasma membrane microdomains and HIV-1 assembly. Biol. Cell 102:335-350.
100. Mazurov D, Ilinskaya A, Heidecker G, Filatov A. 2012. Role of O-glycosylation and expression of CD43 and CD45 on the surfaces of effector T cells in human T cell leukemia virus type 1 cell-to-cell infection. J. Virol. 86:2447-2458.
101. Biggins JE, Biesinger T, Yu Kimata MT, Arora R, Kimata JT. 2007. ICAM-3 influences human immunodeficiency virus type 1 replication in CD4() T cells independent of DC-SIGN-mediated transmission. Virology 364:383-394.
102. Zacharias DA, Violin JD, Newton AC, Tsien RY. 2002. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 296:913-916.
103. McLaughlin S, Murray D. 2005. Plasma membrane phosphoinositide organization by protein electrostatics. Nature 438:605-611.
104. Chan J, Dick RA, Vogt VM. 2011. Rous sarcoma virus gag has no specific requirement for phosphatidylinositol-(4,5)-bisphosphate for plasma membrane association in vivo or for liposome interaction in vitro. J. Virol. 85:10851-10860.
105. Kusumi A, Suzuki KG, Kasai RS, Ritchie K, Fujiwara TK. 2011. Hierarchical mesoscale domain organization of the plasma membrane. Trends Biochem. Sci. 36:604-615.
106. Ciani B, Bjelic S, Honnappa S, Jawhari H, Jaussi R, Payapilly A, Jowitt T, Steinmetz MO, Kammerer RA. 2010. Molecular basis of coiled-coil oligomerization-state specificity. Proc. Natl. Acad. Sci. U. S. A. 107: 19850-19855.