Nucleocapsid Promotes Localization of HIV-1 Gag to Uropods That Participate in Virological Synapses between T Cells
T cells adopt a polarized morphology in lymphoid organs, where cell-to-cell transmission of HIV-1 is likely frequent. However, despite the importance of understanding virus spread in vivo, little is known about the HIV-1 life cycle, particularly its late phase, in polarized T cells. Polarized T cells form two ends, the leading edge at the front and a protrusion called a uropod at the rear. Using multiple uropod markers, we observed that HIV-1 Gag localizes to the uropod in polarized T cells. Infected T cells formed contacts with uninfected target T cells preferentially via HIV-1 Gag-containing uropods compared to leading edges that lack plasma-membrane-associated Gag. Cell contacts enriched in Gag and CD4, which define the virological synapse (VS), are also enriched in uropod markers. These results indicate that Gag-laden uropods participate in the formation and/or structure of the VS, which likely plays a key role in cell-to-cell transmission of HIV-1. Consistent with this notion, a myosin light chain kinase inhibitor, which disrupts uropods, reduced virus particle transfer from infected T cells to target T cells. Mechanistically, we observed that Gag copatches with antibody-crosslinked uropod markers even in non-polarized cells, suggesting an association of Gag with uropod-specific microdomains that carry Gag to uropods. Finally, we determined that localization of Gag to the uropod depends on higher-order clustering driven by its NC domain. Taken together, these results support a model in which NC-dependent Gag accumulation to uropods establishes a preformed platform that later constitutes T-cell-T-cell contacts at which HIV-1 virus transfer occurs.
Vyšlo v časopise:
Nucleocapsid Promotes Localization of HIV-1 Gag to Uropods That Participate in Virological Synapses between T Cells. PLoS Pathog 6(10): e32767. doi:10.1371/journal.ppat.1001167
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1001167
Souhrn
T cells adopt a polarized morphology in lymphoid organs, where cell-to-cell transmission of HIV-1 is likely frequent. However, despite the importance of understanding virus spread in vivo, little is known about the HIV-1 life cycle, particularly its late phase, in polarized T cells. Polarized T cells form two ends, the leading edge at the front and a protrusion called a uropod at the rear. Using multiple uropod markers, we observed that HIV-1 Gag localizes to the uropod in polarized T cells. Infected T cells formed contacts with uninfected target T cells preferentially via HIV-1 Gag-containing uropods compared to leading edges that lack plasma-membrane-associated Gag. Cell contacts enriched in Gag and CD4, which define the virological synapse (VS), are also enriched in uropod markers. These results indicate that Gag-laden uropods participate in the formation and/or structure of the VS, which likely plays a key role in cell-to-cell transmission of HIV-1. Consistent with this notion, a myosin light chain kinase inhibitor, which disrupts uropods, reduced virus particle transfer from infected T cells to target T cells. Mechanistically, we observed that Gag copatches with antibody-crosslinked uropod markers even in non-polarized cells, suggesting an association of Gag with uropod-specific microdomains that carry Gag to uropods. Finally, we determined that localization of Gag to the uropod depends on higher-order clustering driven by its NC domain. Taken together, these results support a model in which NC-dependent Gag accumulation to uropods establishes a preformed platform that later constitutes T-cell-T-cell contacts at which HIV-1 virus transfer occurs.
Zdroje
1. BajenoffM
EgenJG
KooLY
LaugierJP
BrauF
2006 Stromal cell networks regulate lymphocyte entry, migration, and territoriality in lymph nodes. Immunity 25 989 1001
2. HuguesS
FetlerL
BonifazL
HelftJ
AmblardF
2004 Distinct T cell dynamics in lymph nodes during the induction of tolerance and immunity. Nat Immunol 5 1235 1242
3. MempelTR
HenricksonSE
Von AndrianUH
2004 T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature 427 154 159
4. MillerMJ
WeiSH
CahalanMD
ParkerI
2003 Autonomous T cell trafficking examined in vivo with intravital two-photon microscopy. Proc Natl Acad Sci U S A 100 2604 2609
5. MillerMJ
WeiSH
ParkerI
CahalanMD
2002 Two-photon imaging of lymphocyte motility and antigen response in intact lymph node. Science 296 1869 1873
6. MrassP
TakanoH
NgLG
DaxiniS
LasaroMO
2006 Random migration precedes stable target cell interactions of tumor-infiltrating T cells. J Exp Med 203 2749 2761
7. AdamsonCS
FreedEO
2007 Human immunodeficiency virus type 1 assembly, release, and maturation. Adv Pharmacol 55 347 387
8. AlfadhliA
StillA
BarklisE
2009 Analysis of human immunodeficiency virus type 1 matrix binding to membranes and nucleic acids. J Virol 83 12196 12203
9. BryantM
RatnerL
1990 Myristoylation-dependent replication and assembly of human immunodeficiency virus 1. Proc Natl Acad Sci U S A 87 523 527
10. ChanR
UchilPD
JinJ
ShuiG
OttDE
2008 Retroviruses human immunodeficiency virus and murine leukemia virus are enriched in phosphoinositides. J Virol 82 11228 11238
11. ChukkapalliV
HogueIB
BoykoV
HuWS
OnoA
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
12. ChukkapalliV
OhSJ
OnoA
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
13. DaltonAK
Ako-AdjeiD
MurrayPS
MurrayD
VogtVM
2007 Electrostatic interactions drive membrane association of the human immunodeficiency virus type 1 Gag MA domain. J Virol 81 6434 6445
14. GottlingerHG
SodroskiJG
HaseltineWA
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
15. HillCP
WorthylakeD
BancroftDP
ChristensenAM
SundquistWI
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
16. OnoA
AblanSD
LockettSJ
NagashimaK
FreedEO
2004 Phosphatidylinositol (4,5) bisphosphate regulates HIV-1 Gag targeting to the plasma membrane. Proc Natl Acad Sci U S A 101 14889 14894
17. SaadJS
MillerJ
TaiJ
KimA
GhanamRH
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
18. ShkriabaiN
DattaSA
ZhaoZ
HessS
ReinA
2006 Interactions of HIV-1 Gag with assembly cofactors. Biochemistry 45 4077 4083
19. TangC
LoeligerE
LuncsfordP
KindeI
BeckettD
2004 Entropic switch regulates myristate exposure in the HIV-1 matrix protein. Proc Natl Acad Sci U S A 101 517 522
20. ZhouW
ParentLJ
WillsJW
ReshMD
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
21. BurnistonMT
CimarelliA
ColganJ
CurtisSP
LubanJ
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
22. DattaSA
CurtisJE
RatcliffW
ClarkPK
CristRM
2007 Conformation of the HIV-1 Gag protein in solution. J Mol Biol 365 812 824
23. DattaSA
ZhaoZ
ClarkPK
TarasovS
AlexandratosJN
2007 Interactions between HIV-1 Gag molecules in solution: an inositol phosphate-mediated switch. J Mol Biol 365 799 811
24. EhrlichLS
AgrestaBE
CarterCA
1992 Assembly of recombinant human immunodeficiency virus type 1 capsid protein in vitro. J Virol 66 4874 4883
25. FrankeEK
YuanHE
BossoltKL
GoffSP
LubanJ
1994 Specificity and sequence requirements for interactions between various retroviral Gag proteins. J Virol 68 5300 5305
26. GambleTR
YooS
VajdosFF
von SchwedlerUK
WorthylakeDK
1997 Structure of the carboxyl-terminal dimerization domain of the HIV-1 capsid protein. Science 278 849 853
27. GrossI
HohenbergH
HuckhagelC
KrausslichHG
1998 N-Terminal extension of human immunodeficiency virus capsid protein converts the in vitro assembly phenotype from tubular to spherical particles. J Virol 72 4798 4810
28. HogueIB
HoppeA
OnoA
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
29. JoshiA
NagashimaK
FreedEO
2006 Mutation of dileucine-like motifs in the human immunodeficiency virus type 1 capsid disrupts virus assembly, gag-gag interactions, gag-membrane binding, and virion maturation. J Virol 80 7939 7951
30. LiH
DouJ
DingL
SpearmanP
2007 Myristoylation is required for human immunodeficiency virus type 1 Gag-Gag multimerization in mammalian cells. J Virol 81 12899 12910
31. MomanyC
KovariLC
ProngayAJ
KellerW
GittiRK
1996 Crystal structure of dimeric HIV-1 capsid protein. Nat Struct Biol 3 763 770
32. von SchwedlerUK
StrayKM
GarrusJE
SundquistWI
2003 Functional surfaces of the human immunodeficiency virus type 1 capsid protein. J Virol 77 5439 5450
33. ZhangWH
HockleyDJ
NermutMV
MorikawaY
JonesIM
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 Pt 4 743 751
34. D'SouzaV
SummersMF
2005 How retroviruses select their genomes. Nat Rev Microbiol 3 643 655
35. CampbellS
ReinA
1999 In vitro assembly properties of human immunodeficiency virus type 1 Gag protein lacking the p6 domain. J Virol 73 2270 2279
36. CampbellS
VogtVM
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
37. CimarelliA
SandinS
HoglundS
LubanJ
2000 Basic residues in human immunodeficiency virus type 1 nucleocapsid promote virion assembly via interaction with RNA. J Virol 74 3046 3057
38. DawsonL
YuXF
1998 The role of nucleocapsid of HIV-1 in virus assembly. Virology 251 141 157
39. DerdowskiA
DingL
SpearmanP
2004 A novel fluorescence resonance energy transfer assay demonstrates that the human immunodeficiency virus type 1 Pr55Gag I domain mediates Gag-Gag interactions. J Virol 78 1230 1242
40. HusebyD
BarklisRL
AlfadhliA
BarklisE
2005 Assembly of human immunodeficiency virus precursor gag proteins. J Biol Chem 280 17664 17670
41. SandefurS
SmithRM
VarthakaviV
SpearmanP
2000 Mapping and characterization of the N-terminal I domain of human immunodeficiency virus type 1 Pr55(Gag). J Virol 74 7238 7249
42. SandefurS
VarthakaviV
SpearmanP
1998 The I domain is required for efficient plasma membrane binding of human immunodeficiency virus type 1 Pr55Gag. J Virol 72 2723 2732
43. ZabranskyA
HunterE
SakalianM
2002 Identification of a minimal HIV-1 gag domain sufficient for self-association. Virology 294 141 150
44. DemirovDG
FreedEO
2004 Retrovirus budding. Virus Res 106 87 102
45. Martin-SerranoJ
ZangT
BieniaszPD
2003 Role of ESCRT-I in retroviral budding. J Virol 77 4794 4804
46. MoritaE
SundquistWI
2004 Retrovirus budding. Annu Rev Cell Dev Biol 20 395 425
47. KrummelMF
MacaraI
2006 Maintenance and modulation of T cell polarity. Nat Immunol 7 1143 1149
48. Sanchez-MadridF
del PozoMA
1999 Leukocyte polarization in cell migration and immune interactions. Embo J 18 501 511
49. Sanchez-MadridF
SerradorJM
2009 Bringing up the rear: defining the roles of the uropod. Nat Rev Mol Cell Biol 10 353 359
50. Alonso-LebreroJL
SerradorJM
Dominguez-JimenezC
BarreiroO
LuqueA
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
51. ItohS
SusukiC
TakeshitaK
NagataK
TsujiT
2007 Redistribution of P-selectin glycoprotein ligand-1 (PSGL-1) in chemokine-treated neutrophils: a role of lipid microdomains. J Leukoc Biol 81 1414 1421
52. RatnerS
SherrodWS
LichlyterD
1997 Microtubule retraction into the uropod and its role in T cell polarization and motility. J Immunol 159 1063 1067
53. ChenP
HubnerW
SpinelliMA
ChenBK
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
54. NguyenDH
HildrethJE
2000 Evidence for budding of human immunodeficiency virus type 1 selectively from glycolipid-enriched membrane lipid rafts. J Virol 74 3264 3272
55. Pearce-PrattR
MalamudD
PhillipsDM
1994 Role of the cytoskeleton in cell-to-cell transmission of human immunodeficiency virus. J Virol 68 2898 2905
56. PerottiME
TanX
PhillipsDM
1996 Directional budding of human immunodeficiency virus from monocytes. J Virol 70 5916 5921
57. PhillipsDM
1994 The role of cell-to-cell transmission in HIV infection. AIDS 8 719 731
58. ChertovaE
ChertovO
CorenLV
RoserJD
TrubeyCM
2006 Proteomic and biochemical analysis of purified human immunodeficiency virus type 1 produced from infected monocyte-derived macrophages. J Virol 80 9039 9052
59. FaisS
CapobianchiMR
AbbateI
CastillettiC
GentileM
1995 Unidirectional budding of HIV-1 at the site of cell-to-cell contact is associated with co-polarization of intercellular adhesion molecules and HIV-1 viral matrix protein. Aids 9 329 335
60. Gomez-MoutonC
AbadJL
MiraE
LacalleRA
GallardoE
2001 Segregation of leading-edge and uropod components into specific lipid rafts during T cell polarization. Proc Natl Acad Sci U S A 98 9642 9647
61. JollyC
SattentauQJ
2005 Human immunodeficiency virus type 1 virological synapse formation in T cells requires lipid raft integrity. J Virol 79 12088 12094
62. OnoA
FreedEO
2005 Role of lipid rafts in virus replication. Adv Virus Res 64 311 358
63. del PozoMA
Sanchez-MateosP
NietoM
Sanchez-MadridF
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
64. SerradorJM
NietoM
Alonso-LebreroJL
del PozoMA
CalvoJ
1998 CD43 interacts with moesin and ezrin and regulates its redistribution to the uropods of T lymphocytes at the cell-cell contacts. Blood 91 4632 4644
65. TibaldiEV
SalgiaR
ReinherzEL
2002 CD2 molecules redistribute to the uropod during T cell scanning: implications for cellular activation and immune surveillance. Proc Natl Acad Sci U S A 99 7582 7587
66. DimitrovDS
WilleyRL
SatoH
ChangLJ
BlumenthalR
1993 Quantitation of human immunodeficiency virus type 1 infection kinetics. J Virol 67 2182 2190
67. HubnerW
McNerneyGP
ChenP
DaleBM
GordonRE
2009 Quantitative 3D video microscopy of HIV transfer across T cell virological synapses. Science 323 1743 1747
68. MartinN
WelschS
JollyC
BriggsJA
VauxD
2010 Virological synapse-mediated spread of human immunodeficiency virus type 1 between T cells is sensitive to entry inhibition. J Virol 84 3516 3527
69. MazurovD
IlinskayaA
HeideckerG
LloydP
DerseD
2010 Quantitative comparison of HTLV-1 and HIV-1 cell-to-cell infection with new replication dependent vectors. PLoS Pathog 6 e1000788
70. SatoH
OrensteinJ
DimitrovD
MartinM
1992 Cell-to-cell spread of HIV-1 occurs within minutes and may not involve the participation of virus particles. Virology 186 712 724
71. SourisseauM
Sol-FoulonN
PorrotF
BlanchetF
SchwartzO
2007 Inefficient human immunodeficiency virus replication in mobile lymphocytes. J Virol 81 1000 1012
72. AlfsenA
YuH
Magerus-ChatinetA
SchmittA
BomselM
2005 HIV-1-infected blood mononuclear cells form an integrin- and agrin-dependent viral synapse to induce efficient HIV-1 transcytosis across epithelial cell monolayer. Mol Biol Cell 16 4267 4279
73. ArrighiJF
PionM
GarciaE
EscolaJM
van KooykY
2004 DC-SIGN-mediated infectious synapse formation enhances X4 HIV-1 transmission from dendritic cells to T cells. J Exp Med 200 1279 1288
74. GarciaE
PionM
Pelchen-MatthewsA
CollinsonL
ArrighiJF
2005 HIV-1 trafficking to the dendritic cell-T-cell infectious synapse uses a pathway of tetraspanin sorting to the immunological synapse. Traffic 6 488 501
75. GoussetK
AblanSD
CorenLV
OnoA
SoheilianF
2008 Real-time visualization of HIV-1 GAG trafficking in infected macrophages. PLoS Pathog 4 e1000015
76. GrootF
WelschS
SattentauQJ
2008 Efficient HIV-1 transmission from macrophages to T cells across transient virological synapses. Blood 111 4660 4663
77. IgakuraT
StinchcombeJC
GoonPK
TaylorGP
WeberJN
2003 Spread of HTLV-I between lymphocytes by virus-induced polarization of the cytoskeleton. Science 299 1713 1716
78. JollyC
KashefiK
HollinsheadM
SattentauQJ
2004 HIV-1 cell to cell transfer across an Env-induced, actin-dependent synapse. J Exp Med 199 283 293
79. McDonaldD
WuL
BohksSM
KewalRamaniVN
UnutmazD
2003 Recruitment of HIV and its receptors to dendritic cell-T cell junctions. Science 300 1295 1297
80. RudnickaD
FeldmannJ
PorrotF
WietgrefeS
GuadagniniS
2009 Simultaneous cell-to-cell transmission of human immunodeficiency virus to multiple targets through polysynapses. J Virol 83 6234 6246
81. ShererNM
LehmannMJ
Jimenez-SotoLF
HorensavitzC
PypaertM
2007 Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission. Nat Cell Biol 9 310 315
82. SowinskiS
JollyC
BerninghausenO
PurbhooMA
ChauveauA
2008 Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission. Nat Cell Biol 10 211 219
83. WangJH
WellsC
WuL
2008 Macropinocytosis and cytoskeleton contribute to dendritic cell-mediated HIV-1 transmission to CD4+ T cells. Virology 381 143 154
84. YuHJ
ReuterMA
McDonaldD
2008 HIV traffics through a specialized, surface-accessible intracellular compartment during trans-infection of T cells by mature dendritic cells. PLoS Pathog 4 e1000134
85. MajorovitsE
NejmeddineM
TanakaY
TaylorGP
FullerSD
2008 Human T-lymphotropic virus-1 visualized at the virological synapse by electron tomography. PLoS One 3 e2251
86. Pais-CorreiaAM
SachseM
GuadagniniS
RobbiatiV
LasserreR
2010 Biofilm-like extracellular viral assemblies mediate HTLV-1 cell-to-cell transmission at virological synapses. Nat Med 16 83 89
87. ShererNM
MothesW
2008 Cytonemes and tunneling nanotubules in cell-cell communication and viral pathogenesis. Trends Cell Biol 18 414 420
88. JinJ
ShererNM
HeideckerG
DerseD
MothesW
2009 Assembly of the murine leukemia virus is directed towards sites of cell-cell contact. PLoS Biol 7 e1000163
89. Vasiliver-ShamisG
TuenM
WuTW
StarrT
CameronTO
2008 Human immunodeficiency virus type 1 envelope gp120 induces a stop signal and virological synapse formation in noninfected CD4+ T cells. J Virol 82 9445 9457
90. Vasiliver-ShamisG
ChoMW
HioeCE
DustinML
2009 Human immunodeficiency virus type 1 envelope gp120-induced partial T-cell receptor signaling creates an F-actin-depleted zone in the virological synapse. J Virol 83 11341 11355
91. PuigdomenechI
MassanellaM
CabreraC
ClotetB
BlancoJ
2009 On the steps of cell-to-cell HIV transmission between CD4 T cells. Retrovirology 6 89
92. SattentauQ
2008 Avoiding the void: cell-to-cell spread of human viruses. Nat Rev Microbiol 6 815 826
93. HallerC
FacklerOT
2008 HIV-1 at the immunological and T-lymphocytic virological synapse. Biol Chem 389 1253 1260
94. PiguetV
SattentauQ
2004 Dangerous liaisons at the virological synapse. J Clin Invest 114 605 610
95. Sol-FoulonN
SourisseauM
PorrotF
ThoulouzeMI
TrouilletC
2007 ZAP-70 kinase regulates HIV cell-to-cell spread and virological synapse formation. Embo J 26 516 526
96. JollyC
MitarI
SattentauQJ
2007 Adhesion molecule interactions facilitate human immunodeficiency virus type 1-induced virological synapse formation between T cells. J Virol 81 13916 13921
97. ArthosJ
CicalaC
MartinelliE
MacleodK
Van RykD
2008 HIV-1 envelope protein binds to and signals through integrin alpha4beta7, the gut mucosal homing receptor for peripheral T cells. Nat Immunol 9 301 309
98. KinashiT
KatagiriK
2004 Regulation of lymphocyte adhesion and migration by the small GTPase Rap1 and its effector molecule, RAPL. Immunol Lett 93 1 5
99. HubnerW
ChenP
Del PortilloA
LiuY
GordonRE
2007 Sequence of human immunodeficiency virus type 1 (HIV-1) Gag localization and oligomerization monitored with live confocal imaging of a replication-competent, fluorescently tagged HIV-1. J Virol 81 12596 12607
100. OnoA
OrensteinJM
FreedEO
2000 Role of the Gag matrix domain in targeting human immunodeficiency virus type 1 assembly. J Virol 74 2855 2866
101. ZhouW
ReshMD
1996 Differential membrane binding of the human immunodeficiency virus type 1 matrix protein. J Virol 70 8540 8548
102. RuggieroE
BonaR
MuratoriC
FedericoM
2008 Virological consequences of early events following cell-cell contact between human immunodeficiency virus type 1-infected and uninfected CD4+ cells. J Virol 82 7773 7789
103. PuigdomenechI
MassanellaM
Izquierdo-UserosN
Ruiz-HernandezR
CurriuM
2008 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 5 32
104. BlancoJ
BoschB
Fernandez-FiguerasMT
BarretinaJ
ClotetB
2004 High level of coreceptor-independent HIV transfer induced by contacts between primary CD4 T cells. J Biol Chem 279 51305 51314
105. OnoA
FreedEO
2001 Plasma membrane rafts play a critical role in HIV-1 assembly and release. Proc Natl Acad Sci U S A 98 13925 13930
106. DingL
DerdowskiA
WangJJ
SpearmanP
2003 Independent segregation of human immunodeficiency virus type 1 Gag protein complexes and lipid rafts. J Virol 77 1916 1926
107. HolmK
WeclewiczK
HewsonR
SuomalainenM
2003 Human immunodeficiency virus type 1 assembly and lipid rafts: Pr55(gag) associates with membrane domains that are largely resistant to Brij98 but sensitive to Triton X-100. J Virol 77 4805 4817
108. LindwasserOW
ReshMD
2001 Multimerization of human immunodeficiency virus type 1 Gag promotes its localization to barges, raft-like membrane microdomains. J Virol 75 7913 7924
109. NydeggerS
KhuranaS
KrementsovDN
FotiM
ThaliM
2006 Mapping of tetraspanin-enriched microdomains that can function as gateways for HIV-1. J Cell Biol 173 795 807
110. BoothAM
FangY
FallonJK
YangJM
HildrethJE
2006 Exosomes and HIV Gag bud from endosome-like domains of the T cell plasma membrane. J Cell Biol 172 923 935
111. GrigorovB
Attuil-AudenisV
PerugiF
NedelecM
WatsonS
2009 A role for CD81 on the late steps of HIV-1 replication in a chronically infected T cell line. Retrovirology 6 28
112. BruggerB
GlassB
HaberkantP
LeibrechtI
WielandFT
2006 The HIV lipidome: a raft with an unusual composition. Proc Natl Acad Sci U S A 103 2641 2646
113. JollyC
SattentauQJ
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
114. KrementsovDN
WengJ
LambeleM
RoyNH
ThaliM
2009 Tetraspanins regulate cell-to-cell transmission of HIV-1. Retrovirology 6 64
115. ManesS
MiraE
Gomez-MoutonC
LacalleRA
KellerP
1999 Membrane raft microdomains mediate front-rear polarity in migrating cells. Embo J 18 6211 6220
116. RossyJ
SchlichtD
EngelhardtB
NiggliV
2009 Flotillins interact with PSGL-1 in neutrophils and, upon stimulation, rapidly organize into membrane domains subsequently accumulating in the uropod. PLoS One 4 e5403
117. FabbriM
Di MeglioS
GaglianiMC
ConsonniE
MolteniR
2005 Dynamic partitioning into lipid rafts controls the endo-exocytic cycle of the alphaL/beta2 integrin, LFA-1, during leukocyte chemotaxis. Mol Biol Cell 16 5793 5803
118. PieriniLM
MaxfieldFR
2001 Flotillas of lipid rafts fore and aft. Proc Natl Acad Sci U S A 98 9471 9473
119. HarderT
ScheiffeleP
VerkadeP
SimonsK
1998 Lipid domain structure of the plasma membrane revealed by patching of membrane components. J Cell Biol 141 929 942
120. JanesPW
LeySC
MageeAI
1999 Aggregation of lipid rafts accompanies signaling via the T cell antigen receptor. J Cell Biol 147 447 461
121. GriG
MolonB
ManesS
PozzanT
ViolaA
2004 The inner side of T cell lipid rafts. Immunol Lett 94 247 252
122. LingwoodD
RiesJ
SchwilleP
SimonsK
2008 Plasma membranes are poised for activation of raft phase coalescence at physiological temperature. Proc Natl Acad Sci U S A 105 10005 10010
123. MederD
MorenoMJ
VerkadeP
VazWL
SimonsK
2006 Phase coexistence and connectivity in the apical membrane of polarized epithelial cells. Proc Natl Acad Sci U S A 103 329 334
124. ShvartsmanDE
KotlerM
TallRD
RothMG
HenisYI
2003 Differently anchored influenza hemagglutinin mutants display distinct interaction dynamics with mutual rafts. J Cell Biol 163 879 888
125. FreedEO
MartinMA
1996 Domains of the human immunodeficiency virus type 1 matrix and gp41 cytoplasmic tail required for envelope incorporation into virions. J Virol 70 341 351
126. MammanoF
KondoE
SodroskiJ
BukovskyA
GottlingerHG
1995 Rescue of human immunodeficiency virus type 1 matrix protein mutants by envelope glycoproteins with short cytoplasmic domains. J Virol 69 3824 3830
127. AkariH
FukumoriT
AdachiA
2000 Cell-dependent requirement of human immunodeficiency virus type 1 gp41 cytoplasmic tail for Env incorporation into virions. J Virol 74 4891 4893
128. MurakamiT
FreedEO
2000 Genetic evidence for an interaction between human immunodeficiency virus type 1 matrix and alpha-helix 2 of the gp41 cytoplasmic tail. J Virol 74 3548 3554
129. MurakamiT
FreedEO
2000 The long cytoplasmic tail of gp41 is required in a cell type-dependent manner for HIV-1 envelope glycoprotein incorporation into virions. Proc Natl Acad Sci U S A 97 343 348
130. Lopez-VergesS
CamusG
BlotG
BeauvoirR
BenarousR
2006 Tail-interacting protein TIP47 is a connector between Gag and Env and is required for Env incorporation into HIV-1 virions. Proc Natl Acad Sci U S A 103 14947 14952
131. WymaDJ
KotovA
AikenC
2000 Evidence for a stable interaction of gp41 with Pr55(Gag) in immature human immunodeficiency virus type 1 particles. J Virol 74 9381 9387
132. MassanellaM
PuigdomenechI
CabreraC
Fernandez-FiguerasMT
AucherA
2009 Antigp41 antibodies fail to block early events of virological synapses but inhibit HIV spread between T cells. AIDS 23 183 188
133. FackeM
JanetzkoA
ShoemanRL
KrausslichHG
1993 A large deletion in the matrix domain of the human immunodeficiency virus gag gene redirects virus particle assembly from the plasma membrane to the endoplasmic reticulum. J Virol 67 4972 4980
134. FreedEO
OrensteinJM
Buckler-WhiteAJ
MartinMA
1994 Single amino acid changes in the human immunodeficiency virus type 1 matrix protein block virus particle production. J Virol 68 5311 5320
135. YuanX
YuX
LeeTH
EssexM
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
136. Hermida-MatsumotoL
ReshMD
2000 Localization of human immunodeficiency virus type 1 Gag and Env at the plasma membrane by confocal imaging. J Virol 74 8670 8679
137. CannonPM
MatthewsS
ClarkN
BylesED
IourinO
1997 Structure-function studies of the human immunodeficiency virus type 1 matrix protein, p17. J Virol 71 3474 3483
138. ReilH
BukovskyAA
GelderblomHR
GottlingerHG
1998 Efficient HIV-1 replication can occur in the absence of the viral matrix protein. Embo J 17 2699 2708
139. OnoA
2009 HIV-1 Assembly at the Plasma Membrane: Gag Trafficking and Localization. Future Virol 4 241 257
140. DouJ
WangJJ
ChenX
LiH
DingL
2009 Characterization of a myristoylated, monomeric HIV Gag protein. Virology 387 341 352
141. CristRM
DattaSA
StephenAG
SoheilianF
MirroJ
2009 Assembly properties of human immunodeficiency virus type 1 Gag-leucine zipper chimeras: implications for retrovirus assembly. J Virol 83 2216 2225
142. AccolaMA
StrackB
GottlingerHG
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
143. ZhangY
QianH
LoveZ
BarklisE
1998 Analysis of the assembly function of the human immunodeficiency virus type 1 gag protein nucleocapsid domain. J Virol 72 1782 1789
144. GilletteJM
LarochelleA
DunbarCE
Lippincott-SchwartzJ
2009 Intercellular transfer to signalling endosomes regulates an ex vivo bone marrow niche. Nat Cell Biol 11 303 311
145. JollyC
MitarI
SattentauQJ
2007 Requirement for an intact T-cell actin and tubulin cytoskeleton for efficient assembly and spread of human immunodeficiency virus type 1. J Virol 81 5547 5560
146. SeveauS
KellerH
MaxfieldFR
PillerF
Halbwachs-MecarelliL
2000 Neutrophil polarity and locomotion are associated with surface redistribution of leukosialin (CD43), an antiadhesive membrane molecule. Blood 95 2462 2470
147. BraunJ
FujiwaraK
PollardTD
UnanueER
1978 Two distinct mechanisms for redistribution of lymphocyte surface macromolecules. I. Relationship to cytoplasmic myosin. J Cell Biol 79 409 418
148. KammerGM
WalterEI
MedofME
1988 Association of cytoskeletal re-organization with capping of the complement decay-accelerating factor on T lymphocytes. J Immunol 141 2924 2928
149. FangY
WuN
GanX
YanW
MorrellJC
2007 Higher-order oligomerization targets plasma membrane proteins and HIV gag to exosomes. PLoS Biol 5 e158
150. FisherRJ
ReinA
FivashM
UrbanejaMA
Casas-FinetJR
1998 Sequence-specific binding of human immunodeficiency virus type 1 nucleocapsid protein to short oligonucleotides. J Virol 72 1902 1909
151. HancockJF
2006 Lipid rafts: contentious only from simplistic standpoints. Nat Rev Mol Cell Biol 7 456 462
152. FujitaA
ChengJ
FujimotoT
2009 Segretation of GM1 and GM3 clusters in the cell membrane depends on the intact actin cytoskeleton. Biochim Biophys Acta 1791 388 396
153. KatagiriK
MaedaA
ShimonakaM
KinashiT
2003 RAPL, a Rap1-binding molecule that mediates Rap1-induced adhesion through spatial regulation of LFA-1. Nat Immunol 4 741 748
154. MorinNA
OakesPW
HyunYM
LeeD
ChinYE
2008 Nonmuscle myosin heavy chain IIA mediates integrin LFA-1 de-adhesion during T lymphocyte migration. J Exp Med 205 195 205
155. SmithA
CarrascoYR
StanleyP
KiefferN
BatistaFD
2005 A talin-dependent LFA-1 focal zone is formed by rapidly migrating T lymphocytes. J Cell Biol 170 141 151
156. DeschambeaultJ
LalondeJP
Cervantes-AcostaG
LodgeR
CohenEA
1999 Polarized human immunodeficiency virus budding in lymphocytes involves a tyrosine-based signal and favors cell-to-cell viral transmission. J Virol 73 5010 5017
157. AdachiA
GendelmanHE
KoenigS
FolksT
WilleyR
1986 Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J Virol 59 284 291
158. ZachariasDA
ViolinJD
NewtonAC
TsienRY
2002 Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 296 913 916
159. NagaiT
IbataK
ParkES
KubotaM
MikoshibaK
2002 A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat Biotechnol 20 87 90
160. RizzoMA
SpringerGH
GranadaB
PistonDW
2004 An improved cyan fluorescent protein variant useful for FRET. Nat Biotechnol 22 445 449
161. FreedEO
MartinMA
1995 The role of human immunodeficiency virus type 1 envelope glycoproteins in virus infection. J Biol Chem 270 23883 23886
162. YeeJK
FriedmannT
BurnsJC
1994 Generation of high-titer pseudotyped retroviral vectors with very broad host range. Methods Cell Biol 43 Pt A 99 112
163. NietoM
FradeJM
SanchoD
MelladoM
MartinezAC
1997 Polarization of chemokine receptors to the leading edge during lymphocyte chemotaxis. J Exp Med 186 153 158
164. WilkinsonPC
NewmanI
1994 Chemoattractant activity of IL-2 for human lymphocytes: a requirement for the IL-2 receptor beta-chain. Immunology 82 134 139
165. GoeblNA
BabbeyCM
Datta-MannanA
WitcherDR
WroblewskiVJ
2008 Neonatal Fc receptor mediates internalization of Fc in transfected human endothelial cells. Mol Biol Cell 19 5490 5505
166. LachmanovichE
ShvartsmanDE
MalkaY
BotvinC
HenisYI
2003 Co-localization analysis of complex formation among membrane proteins by computerized fluorescence microscopy: application to immunofluorescence co-patching studies. J Microsc 212 122 131
167. HoppeA
ChristensenK
SwansonJA
2002 Fluorescence resonance energy transfer-based stoichiometry in living cells. Biophys J 83 3652 3664
168. NegulescuPA
KrasievaTB
KhanA
KerschbaumHH
CahalanMD
1996 Polarity of T cell shape, motility, and sensitivity to antigen. Immunity 4 421 430
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
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