Involvement of the Rac1-IRSp53-Wave2-Arp2/3 signaling pathway in HIV-1 Gag particle release in CD4 T cells

Journal of Virology

Volumn 89, Issue 16, 2015, Pages 8162-8181

  Thomas, Audrey ^b,d   Mariani Floderer, Charlotte ^b   López Huertas, Maria Rosa ^c,d   Gros, Nathalie ^b   Hamard Péron, Elise ^d   Favard, Cyril ^b   Ohlmann, Theophile ^a,d   Alcamí, José ^c   Muriaux, Delphine ^b,d  

^a CENTRE INTERNATIONAL DE RECHERCHE EN INFECTIOLOGIE   (France)

^b University of Montpellier I and II   (France)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

^d UNIVERSITÉ DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN RELATED PROTEIN 2-3 COMPLEX; F ACTIN; GAG PROTEIN; INSULIN RECEPTOR SUBSTRATE; INSULIN RECEPTOR SUBSTRATE P53; PROTEIN WAVE2; RAC1 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; BAIAP2 PROTEIN, HUMAN; NERVE PROTEIN; RAC1 PROTEIN, HUMAN; WASF2 PROTEIN, HUMAN; WISKOTT ALDRICH SYNDROME PROTEIN;

ARTICLE; BIOASSAY; CD4+ T LYMPHOCYTE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; GLISA; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; MEMBRANE FLOTATION ASSAY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN POLYMERIZATION; PROTEIN SECRETION; SIGNAL TRANSDUCTION; VIROGENESIS; VIRUS ATTACHMENT; VIRUS PARTICLE; VIRUS REPLICATION; JURKAT CELL LINE; METABOLISM;

HUMAN IMMUNODEFICIENCY VIRUS 1;

ACTIN-RELATED PROTEIN 2-3 COMPLEX; CD4-POSITIVE T-LYMPHOCYTES; GENE PRODUCTS, GAG; HIV-1; HUMANS; JURKAT CELLS; NERVE TISSUE PROTEINS; RAC1 GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; WISKOTT-ALDRICH SYNDROME PROTEIN FAMILY;

EID: 84938099466     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00469-15     Document Type: Article

References (85)

1. Corbin A, Grigorov B, Roingeard P, Darlix J, Muriaux D. 2008. Revisiting HIV-1 assembly. Med Sci (Paris) 24:49-55. (In French.) http://dx.doi.org/10.1051/medsci/200824149.
2. Grigorov B, Arcanger F, Roingeard P, Darlix J, Muriaux D. 2006. Assembly of infectious HIV-1 in human epithelial and T-lymphoblastic cell lines. J Mol Biol 359:848-862. http://dx.doi.org/10.1016/j.jmb.2006.04.017.
3. Joshi A, Ablan SD, Soheilian F, Nagashima K, Freed EO. 2009. Evidence that productive human immunodeficiency virus type 1 assembly can occur in an intracellular compartment. J Virol 83:5375-5387. http://dx.doi.org/10.1128/JVI.00109-09.
4. Jouve M, Sol-Foulon N, Watson S, Schwartz O, Benaroch P. 2007. HIV-1 buds and accumulates in "nonacidic" endosomes of macrophages. Cell Host Microbe 2:85-95. http://dx.doi.org/10.1016/j.chom.2007.06.011.
5. Ono A, Freed EO. 2004. Cell-type-dependent targeting of human immunodeficiency virus type 1 assembly to the plasma membrane and the multivesicular body. J Virol 78:1552-1563. http://dx.doi.org/10.1128/JVI.78.3.1552-1563.2004.
6. Kutluay SB, Bieniasz PD. 2010. Analysis of the initiating events in HIV-1 particle assembly and genome packaging. PLoS Pathog 6:e1001200. http://dx.doi.org/10.1371/journal.ppat.1001200.
7. Muriaux D, Darlix J. 2010. Properties and functions of the nucleocapsid protein in virus assembly. RNA Biol 7:744-753. http://dx.doi.org/10.4161/rna.7.6.14065.
8. Ono A. 2010. Relationships between plasma membrane microdomains and HIV-1 assembly. Biol Cell 102:335-350. http://dx.doi.org/10.1042/BC20090165.
9. Dussupt V, Javid MP, Abou-Jaoudé G, Jadwin JA, de La Cruz J, Nagashima K, Bouamr F. 2009. The nucleocapsid region of HIV-1 Gag cooperates with the PTAP and LYPXnL late domains to recruit the cellular machinery necessary for viral budding. PLoS Pathog 5:e1000339. http://dx.doi.org/10.1371/journal.ppat.1000339.
10. von Schwedler UK, Stuchell M, Müller B, Ward DM, Chung H, Morita E, Wang HE, Davis T, He G, Cimbora DM, Scott A, Kräusslich H, Kaplan J, Morham SG, Sundquist WI. 2003. The protein network of HIV budding. Cell 114:701-713. http://dx.doi.org/10.1016/S0092-8674(03)00714-1.
11. Chen K, Bachtiar I, Piszczek G, Bouamr F, Carter C, Tjandra N. 2008. Solution NMR characterizations of oligomerization and dynamics of equine infectious anemia virus matrix protein and its interaction with PIP2. Biochemistry 47:1928-1937. http://dx.doi.org/10.1021/bi701984h.
12. Chukkapalli V, Hogue IB, Boyko V, Hu W, 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. http://dx.doi.org/10.1128/JVI.01614-07.
13. 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. http://dx.doi.org/10.1073/pnas.0908661107.
14. Hamard-Peron E, Muriaux D. 2011. Retroviral matrix and lipids, the intimate interaction. Retrovirology 8:15. http://dx.doi.org/10.1186/1742-4690-8-15.
15. Hamard-Peron E, Juillard F, Saad JS, Roy C, Roingeard P, Summers MF, Darlix JL, Picart C, Muriaux D. 2010. Targeting of murine leukemia virus gag to the plasma membrane is mediated by PI(4,5)P2/PS and a polybasic region in the matrix. J Virol 84:503-515. http://dx.doi.org/10.1128/JVI.01134-09.
16. Inlora J, Chukkapalli V, Derse D, Ono A. 2011. Gag localization and virus-like particle release mediated by the matrix domain of human Tlymphotropic virus type 1 Gag are less dependent on phosphatidylinositol-(4,5)-bisphosphate than those mediated by the matrix domain of HIV-1 Gag. J Virol 85:3802-3810. http://dx.doi.org/10.1128/JVI.02383-10.
17. Kerviel A, Thomas A, Chaloin L, Favard C, Muriaux D. 2013. Virus assembly and plasma membrane domains: which came first? Virus Res 171:332-340. http://dx.doi.org/10.1016/j.virusres.2012.08.014.
18. 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. http://dx.doi.org/10.1073/pnas.0405596101.
19. Prchal J, Srb P, Hunter E, Ruml T, Hrabal R. 2012. The structure of myristoylated Mason-Pfizer monkey virus matrix protein and the role of phosphatidylinositol-(4,5)-bisphosphate in its membrane binding. J Mol Biol 423:427-438. http://dx.doi.org/10.1016/j.jmb.2012.07.021.
20. Saad JS, Ablan SD, Ghanam RH, Kim A, Andrews K, Nagashima K, Soheilian F, Freed EO, Summers MF. 2008. Structure of the myristylated human immunodeficiency virus type 2 matrix protein and the role of phosphatidylinositol-(4,5)-bisphosphate in membrane targeting. J Mol Biol 382:434-447. http://dx.doi.org/10.1016/j.jmb.2008.07.027.
21. Brügger B, Glass B, Haberkant P, Leibrecht I, Wieland FT, Kräusslich H. 2006. The HIV lipidome: a raft with an unusual composition. Proc Natl Acad Sci U S A 103:2641-2646. http://dx.doi.org/10.1073/pnas.0511136103.
22. Dick RA, Goh SL, Feigenson GW, Vogt VM. 2012. HIV-1 Gag protein can sense the cholesterol and acyl chain environment in model membranes. Proc Natl Acad Sci U S A 109:18761-18766. http://dx.doi.org/10.1073/pnas.1209408109.
23. 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. http://dx.doi.org/10.1128/JVI.74.7.3264-3272.2000.
24. 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. http://dx.doi.org/10.1073/pnas.241320298.
25. Grigorov B, Attuil-Audenis V, Perugi F, Nedelec M, Watson S, Pique C, Darlix J, 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. http://dx.doi.org/10.1186/1742-4690-6-28.
26. Jolly C, Sattentau QJ. 2007. Human immunodeficiency virus type 1 assembly, budding, and cell-cell spread in T cells take place in tetraspaninenriched plasma membrane domains. J Virol 81:7873-7884. http://dx.doi.org/10.1128/JVI.01845-06.
27. Thali M. 2011. Tetraspanin functions during HIV-1 and influenza virus replication. Biochem Soc Trans 39:529-531. http://dx.doi.org/10.1042/BST0390529.
28. Keller H, Kräusslich H, Schwille P. 2013. Multimerizable HIV Gag derivative binds to the liquid-disordered phase in model membranes. Cell Microbiol 15:237-247. http://dx.doi.org/10.1111/cmi.12064.
29. Ridley A. 2011. Life at the leading edge. Cell 145:1012-1022. http://dx.doi.org/10.1016/j.cell.2011.06.010.
30. Ott DE, Coren LV, Kane BP, Busch LK, Johnson DG, Sowder RC, II, Chertova EN, Arthur LO, Henderson LE. 1996. Cytoskeletal proteins inside human immunodeficiency virus type 1 virions. J Virol 70:7734-7743.
31. Ott DE, Coren LV, Johnson DG, Kane BP, Sowder RC, II, Kim YD, Fisher RJ, Zhou XZ, Lu KP, Henderson LE. 2000. Actin-binding cellular proteins inside human immunodeficiency virus type 1. Virology 266:42-51. http://dx.doi.org/10.1006/viro.1999.0075.
32. Liu B, Dai R, Tian CJ, Dawson L, Gorelick R, Yu XF. 1999. Interaction of the human immunodeficiency virus type 1 nucleocapsid with actin. J Virol 73:2901-2908.
33. Wilk T, Gowen B, Fuller SD. 1999. Actin associates with the nucleocapsid domain of the human immunodeficiency virus Gag polyprotein. J Virol 73:1931-1940.
34. Gladnikoff M, Shimoni E, Gov NS, Rousso I. 2009. Retroviral assembly and budding occur through an actin-driven mechanism. Biophys J 97: 2419-2428. http://dx.doi.org/10.1016/j.bpj.2009.08.016.
35. Rahman SA, Koch P, Weichsel J, Godinez WJ, Schwarz U, Rohr K, Lamb DC, Kräusslich H, Müller B. 2014. Investigating the role of F-actin in human immunodeficiency virus assembly by live-cell microscopy. J Virol 88:7904-7914. http://dx.doi.org/10.1128/JVI.00431-14.
36. Jolly C, Mitar I, Sattentau QJ. 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. http://dx.doi.org/10.1128/JVI.01469-06.
37. Muriaux D, Darlix JL, Cimarelli A. 2004. Targeting the assembly of the human immunodeficiency virus type I. Curr Pharm Des 10:3725-3739. http://dx.doi.org/10.2174/1381612043382701.
38. Sasaki H, Nakamura M, Ohno T, Matsuda Y, Yuda Y, Nonomura Y. 1995. Myosin-actin interaction plays an important role in human immunodeficiency virus type 1 release from host cells. Proc Natl Acad Sci U S A 92:2026-2030. http://dx.doi.org/10.1073/pnas.92.6.2026.
39. Cooper J, Liu L, Woodruff EA, Taylor HE, Goodwin JS, D'Aquila RT, Spearman P, Hildreth JEK, Dong X. 2011. Filamin A protein interacts with human immunodeficiency virus type 1 Gag protein and contributes to productive particle assembly. J Biol Chem 286:28498-28510. http://dx.doi.org/10.1074/jbc.M111.239053.
40. Wen X, Ding L, Wang J, Qi M, Hammonds J, Chu H, Chen X, Hunter E, Spearman P. 2014. ROCK1 and LIM kinase modulate retrovirus particle release and cell-cell transmission events. J Virol 88:6906-6921. http://dx.doi.org/10.1128/JVI.00023-14.
41. Chen C, Jin J, Rubin M, Huang L, Sturgeon T, Weixel KM, Stolz DB, Watkins SC, Bamburg JR, Weisz OA, Montelaro RC. 2007. Association of gag multimers with filamentous actin during equine infectious anemia virus assembly. Curr HIV Res 5:315-323. http://dx.doi.org/10.2174/157016207780636542.
42. Chen C, Weisz OA, Stolz DB, Watkins SC, Montelaro RC. 2004. Differential effects of actin cytoskeleton dynamics on equine infectious anemia virus particle production. J Virol 78:882-891. http://dx.doi.org/10.1128/JVI.78.2.882-891.2004.
43. Lehmann M, Nikolic DS, Piguet V. 2011. How HIV-1 takes advantage of the cytoskeleton during replication and cell-to-cell transmission. Viruses 3:1757-1776. http://dx.doi.org/10.3390/v3091757.
44. Stolp B, Abraham L, Rudolph JM, Fackler OT. 2010. Lentiviral Nef proteins utilize PAK2-mediated deregulation of cofilin as a general strategy to interfere with actin remodeling. J Virol 84:3935-3948. http://dx.doi.org/10.1128/JVI.02467-09.
45. Stolp B, Reichman-Fried M, Abraham L, Pan X, Giese SI, Hannemann S, Goulimari P, Raz E, Grosse R, Fackler OT. 2009. HIV-1 Nef interferes with host cell motility by deregulation of cofilin. Cell Host Microbe 6:174-186. http://dx.doi.org/10.1016/j.chom.2009.06.004.
46. Nobile C, Rudnicka D, Hasan M, Aulner N, Porrot F, Machu C, Renaud O, Prévost M, Hivroz C, Schwartz O, Sol-Foulon N. 2010. HIV-1 Nef inhibits ruffles, induces filopodia, and modulates migration of infected lymphocytes. J Virol 84:2282-2293. http://dx.doi.org/10.1128/JVI.02230-09.
47. Chichili GR, Rodgers W. 2009. Cytoskeleton-membrane interactions in membrane raft structure. Cell Mol Life Sci 66:2319-2328. http://dx.doi.org/10.1007/s00018-009-0022-6.
48. Sechi AS, Wehland J. 2000. The actin cytoskeleton and plasma membrane connection: PtdIns(4,5)P(2) influences cytoskeletal protein activity at the plasma membrane. J Cell Sci 113(Part 21):3685-3695.
49. Tybulewicz VLJ, Henderson RB. 2009. Rho family GTPases and their regulators in lymphocytes. Nat Rev Immunol 9:630-644. http://dx.doi.org/10.1038/nri2606.
50. Heasman SJ, Ridley AJ. 2008. Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat Rev Mol Cell Biol 9:690-701. http://dx.doi.org/10.1038/nrm2476.
51. Burbach BJ, Medeiros RB, Mueller KL, Shimizu Y. 2007. T-cell receptor signaling to integrins. Immunol Rev 218:65-81. http://dx.doi.org/10.1111/j.1600-065X.2007.00527.x.
52. Knaus UG, Bokoch GM. 1998. The p21Rac/Cdc42-activated kinases (PAKs). Int J Biochem Cell Biol 30:857-862. http://dx.doi.org/10.1016/S1357-2725(98)00059-4.
53. Takenawa T, Miki H. 2001. Wasp and wave family proteins: key molecules for rapid rearrangement of cortical actin filaments and cell movement. J Cell Sci 114:1801-1809.
54. Vicente-Manzanares M, Rey M, Pérez-Martínez M, Yáñez-Mó M, Sancho D, Cabrero JR, Barreiro O, de la Fuente H, Itoh K, Sánchez-Madrid F. 2003. The RhoA effector mDia is induced during T cell activation and regulates actin polymerization and cell migration in T lymphocytes. J Immunol 171:1023-1034. http://dx.doi.org/10.4049/jimmunol.171.2.1023.
55. Audoly G, Popoff MR, Gluschankof P. 2005. Involvement of a small GTP binding protein in HIV-1 release. Retrovirology 2:48. http://dx.doi.org/10.1186/1742-4690-2-48.
56. Watanabe T, Urano E, Miyauchi K, Ichikawa R, Hamatake M, Misawa N, Sato K, Ebina H, Koyanagi Y, Komano J. 2012. The hematopoietic cell-specific Rho GTPase inhibitor ARHGDIB/D4GDI limits HIV type 1 replication. AIDS ResHumRetroviruses 28:913-922. http://dx.doi.org/10.1089/aid.2011.0180.
57. Fackler OT, Lu X, Frost JA, Geyer M, Jiang B, Luo W, Abo A, Alberts AS, Peterlin BM. 2000. p21-activated kinase 1 plays a critical role in cellular activation by Nef. Mol Cell Biol 20:2619-2627. http://dx.doi.org/10.1128/MCB.20.7.2619-2627.2000.
58. Abou-Kheir W, Isaac B, Yamaguchi H, Cox D. 2008. Membrane targeting of wave2 is not sufficient for wave2-dependent actin polymerization: a role for irsp53 in mediating the interaction between rac and wave2. J Cell Sci 121:379-390. http://dx.doi.org/10.1242/jcs.010272.
59. Lee SH, Dominguez R. 2010. Regulation of actin cytoskeleton dynamics in cells. Mol Cells 29:311-325. http://dx.doi.org/10.1007/s10059-010-0053-8.
60. Harmon B, Campbell N, Ratner L. 2010. Role of Abl kinase and the Wave2 signaling complex in HIV-1 entry at a post-hemifusion step. PLoS Pathog 6:e1000956. http://dx.doi.org/10.1371/journal.ppat.1000956.
61. Zufferey R, Nagy D, Mandel RJ, Naldini L, Trono D. 1997. Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat Biotechnol 15:871-875. http://dx.doi.org/10.1038/nbt0997-871.
62. 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.
63. Thomas CL, Steel J, Prestwich GD, Schiavo G. 1999. Generation of phosphatidylinositol-specific antibodies and their characterization. Biochem Soc Trans 27:648-652.
64. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254. http://dx.doi.org/10.1016/0003-2697(76)90527-3.
65. Gao Y, Dickerson JB, Guo F, Zheng J, Zheng Y. 2004. Rational design and characterization of a Rac GTPase-specific small molecule inhibitor. Proc Natl Acad Sci U S A 101:7618-7623. http://dx.doi.org/10.1073/pnas.0307512101.
66. López-Huertas MR, Callejas S, Abia D, Mateos E, Dopazo A, Alcamí J, Coiras M. 2010. Modifications in host cell cytoskeleton structure and function mediated by intracellular HIV-1 Tat protein are greatly dependent on the second coding exon. Nucleic Acids Res 38:3287-3307. http://dx.doi.org/10.1093/nar/gkq037.
67. Harmon B, Ratner L. 2008. Induction of the Galpha(q) signaling cascade by the human immunodeficiency virus envelope is required for virus entry. J Virol 82:9191-9205. http://dx.doi.org/10.1128/JVI.00424-08.
68. Pontow SE, Heyden NV, Wei S, Ratner L. 2004. Actin cytoskeletal reorganizations and coreceptor-mediated activation of rac during human immunodeficiency virus-induced cell fusion. J Virol 78:7138-7147. http://dx.doi.org/10.1128/JVI.78.13.7138-7147.2004.
69. Halstead JR, Savaskan NE, van den Bout I, Van Horck F, Hajdo-Milasinovic A, Snell M, Keune W, Ten Klooster J, Hordijk PL, Divecha N. 2010. Rac controls PIP5K localisation and PtdIns(4,5)P2 synthesis, which modulates vinculin localisation and neurite dynamics. J Cell Sci 123:3535-3546. http://dx.doi.org/10.1242/jcs.062679.
70. Weernink PAO, Meletiadis K, Hommeltenberg S, Hinz M, Ishihara H, Schmidt M, Jakobs KH. 2004. Activation of type I phosphatidylinositol 4-phosphate 5-kinase isoforms by the Rho GTPases RhoA, Rac1, and Cdc42. J Biol Chem 279:7840-7849. http://dx.doi.org/10.1074/jbc.M312737200.
71. Goode BL, Eck MJ. 2007. Mechanism and function of formins in the control of actin assembly. Annu Rev Biochem 76:593-627. http://dx.doi.org/10.1146/annurev.biochem.75.103004.142647.
72. Lebensohn AM, Kirschner MW. 2009. Activation of the wave complex by coincident signals controls actin assembly. Mol Cell 36:512-524. http://dx.doi.org/10.1016/j.molcel.2009.10.024.
73. Lu X, Wu X, Plemenitas A, Yu H, Sawai ET, Abo A, Peterlin BM. 1996. CDC42 and Rac1 are implicated in the activation of the Nef-associated kinase and replication of HIV-1. Curr Biol 6:1677-1684. http://dx.doi.org/10.1016/S0960-9822(02)70792-6.
74. Rauch S, Pulkkinen K, Saksela K, Fackler OT. 2008. Human immunodeficiency virus type 1 nef recruits the guanine exchange factor vav1 via an unexpected interface into plasma membrane microdomains for association with p21-activated kinase 2 activity. J Virol 82:2918-2929. http://dx.doi.org/10.1128/JVI.02185-07.
75. Jouvenet N, Neil SJD, Bess C, Johnson MC, Virgen CA, Simon SM, Bieniasz PD. 2006. Plasma membrane is the site of productive HIV-1 particle assembly. PLoS Biol 4:e435. http://dx.doi.org/10.1371/journal.pbio.0040435.
76. Mariani C, Desdouits M, Favard C, Benaroch P, Muriaux DM. 2014. Role of Gag and lipids during HIV-1 assembly in CD4(+) T cells and macrophages. Front Microbiol 5:312. http://dx.doi.org/10.3389/fmicb.2014.00312.
77. Gowrishankar K, Ghosh S, Saha S, Rumamol C, Mayor S, Rao M. 2012. Active remodeling of cortical actin regulates spatiotemporal organization of cell surface molecules. Cell 149:1353-1367. http://dx.doi.org/10.1016/j.cell.2012.05.008.
78. Spear M, Guo J, Turner A, Yu D, Wang W, Meltzer B, He S, Hu X, Shang H, Kuhn J, Wu Y. 2014. HIV-1 triggers WAVE2 phosphorylation in primary CD4 T cells and macrophages, mediating Arp2/3-dependent nuclear migration. J Biol Chem 289:6949-6959. http://dx.doi.org/10.1074/jbc.M113.492132.
79. Loomis RJ, Holmes DA, Elms A, Solski PA, Der CJ, Su L. 2006. Citron kinase, a RhoA effector, enhances HIV-1 virion production by modulating exocytosis. Traffic 7:1643-1653. http://dx.doi.org/10.1111/j.1600-0854.2006.00503.x.
80. Tybulewicz VLJ, Ardouin L, Prisco A, Reynolds LF. 2003. Vav1: a key signal transducer downstream of the TCR. Immunol Rev 192:42-52. http://dx.doi.org/10.1034/j.1600-065X.2003.00032.x.
81. Fackler OT, Luo W, Geyer M, Alberts AS, Peterlin BM. 1999. Activation of vav by nef induces cytoskeletal rearrangements and downstream effector functions. Mol Cell 3:729-739. http://dx.doi.org/10.1016/S1097-2765(01)80005-8.
82. García-Bernal D, Parmo-Cabañas M, Dios-Esponera A, Samaniego R, Hernán de la Ossa DH-P, Teixidó J. 2009. Chemokine-induced Zap70 kinase-mediated dissociation of the Vav1-talin complex activates alpha4beta1 integrin for T cell adhesion. Immunity 31:953-964. http://dx.doi.org/10.1016/j.immuni.2009.09.021.
83. Sol-Foulon N, Sourisseau M, Porrot F, Thoulouze M, Trouillet C, Nobile C, Blanchet F, di Bartolo V, Noraz N, Taylor N, Alcover A, Hivroz C, Schwartz O. 2007. Zap-70 kinase regulates HIV cell-to-cell spread and virological synapse formation. EMBO J 26:516-526. http://dx.doi.org/10.1038/sj.emboj.7601509.
84. Carlson L, de Marco A, Oberwinkler H, Habermann A, Briggs JAG, Kräusslich H, Grünewald K. 2010. Cryo electron tomography of native HIV-1 budding sites. PLoS Pathog 6:e1001173. http://dx.doi.org/10.1371/journal.ppat.1001173.
85. Stauffer S, Rahman SA, de Marco A, Carlson L, Glass B, Oberwinkler H, Herold N, Briggs JAG, Müller B, Grünewald K, Kräusslich H. 2014. The nucleocapsid domain of Gag is dispensable for actin incorporation into HIV-1 and for association of viral budding sites with cortical F-actin. J Virol 88:7893-7903. http://dx.doi.org/10.1128/JVI.00428-14.