Proteomic analysis of HIV-1 Nef cellular binding partners reveals a role for exocyst complex proteins in mediating enhancement of intercellular nanotube formation

Retrovirology

Volumn 9, Issue , 2012, Pages

  Mukerji, Joya ^a,b   Olivieri, Kevin C ^a   Misra, Vikas ^a   Agopian, Kristin A ^a,b   Gabuzda, Dana ^a,b  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Exocyst complex; Fluorescence confocal microscopy; HIV; Intercellular nanotubes; Nef; Pak2 kinase

Indexed keywords

EXOCYST; EXOCYST COMPLEX COMPONENT 1; EXOCYST COMPLEX COMPONENT 2; EXOCYST COMPLEX COMPONENT 3; EXOCYST COMPLEX COMPONENT 4; EXOCYST COMPLEX COMPONENT 6; NEF PROTEIN; P21 ACTIVATED KINASE 2; UNCLASSIFIED DRUG; EXOC2 PROTEIN, HUMAN; MUTANT PROTEIN; NEF PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; P21 ACTIVATED KINASE; PAK2 PROTEIN, HUMAN; VESICULAR TRANSPORT PROTEIN;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; ENDOCYTOSIS; EXOCYTOSIS; FUNCTIONAL PROTEOMICS; LEUKEMIA CELL LINE; NUCLEOTIDE SEQUENCE; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; TANDEM MASS SPECTROMETRY; BIOLOGICAL MODEL; CELL LINE; GENETICS; HUMAN; METABOLISM; PROTEIN BINDING; PROTEOMICS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

CELL LINE; HUMANS; MODELS, BIOLOGICAL; MUTANT PROTEINS; NEF GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; P21-ACTIVATED KINASES; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN INTERACTION MAPS; PROTEOMICS; VESICULAR TRANSPORT PROTEINS;

EID: 84862197035     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-9-33     Document Type: Article

References (94)

1. Arhel NJ, Kirchhoff F: Implications of nef: host cell interactions in viral persistence and progression to AIDS. Curr Top Microbiol Immunol 2010, 339:147-175.
2. Foster J, Garcia JV: HIV-1 Nef: at the crossroads. Retrovirology 2008, 5:84.
3. Peterlin BM, Trono D: Hide, shield and strike back: how HIV-infected cells avoid immune eradication. Nat Rev Immunol 2003, 3:97-107.
4. Roeth JF, Collins KL: Human immunodeficiency virus type 1 Nef: adapting to intracellular trafficking pathways. Microbiol Mol Biol Rev 2006, 70:548-563.
5. Wei BL, Arora VK, Foster JL, Sodora DL, Garcia JV: vivo analysis of Nef function. Curr HIV Res 2003, 1:41-50.
6. Fenard D, Yonemoto W, de Noronha C, Cavrois M, Williams SA, Greene WC: Nef is physically recruited into the immunological synapse and potentiates T cell activation early after TCR engagemen. J Immunol (Baltimore, Md: 1950) 2005, 175:6050-6057.
7. Schrager JA, Marsh JW: HIV-1 Nef increases T cell activation in a stimulus-dependent manner. Proceedings of the National Academy of Sciences of the United States 1999, 96:8167-8172.
8. Simmons A, Aluvihare V, McMichael A: Nef triggers a transcriptional program in T cells imitating single-signal T cell activation and inducing HIV virulence mediators. Immunity 2001, 14:763-777.
9. Costa LJ, Chen N, Lopes A, Aguiar RS, Tanuri A, Plemenitas A, Peterlin BM: Interactions between Nef and AIP1 proliferate multivesicular bodies and facilitate egress of HIV-1. Retrovirology 2006, 3:33.
10. Peterlin BM: Nef: out and in? Nat Immunol 2006, 7:229-230.
11. Stumptner-Cuvelette P, Jouve M, Helft J, Dugast M, Glouzman AS, Jooss K, Raposo G, Benaroch P: Human immunodeficiency virus-1 Nef expression induces intracellular accumulation of multivesicular bodies and major histocompatibility complex class II complexes: potential role of phosphatidylinositol 3-kinase. Mol Biol Cell 2003, 14:4857-4870.
12. Rudnicka D, Schwartz O: Intrusive HIV-1-infected cells. Nat Immunol 2009, 10:933-934.
13. Xu W, Santini PA, Sullivan JS, He B, Shan M, Ball SC, Dyer WB, Ketas TJ, Chadburn A, Cohen-gould L, et al: HIV-1 evades virus-specific IgG2 and IgA responses by targeting systemic and intestinal B cells via long-range intercellular conduits. Nat Publishing Group 2009, 10:1008-1017.
14. da Silva LL, Sougrat R, Burgos PV, Janvier K, Mattera R, Bonifacino JS: Human immunodeficiency virus type 1 Nef protein targets CD4 to the multivesicular body pathway. J Virol 2009, 83:6578-6590.
15. Jin YJ, Cai CY, Zhang X, Zhang HT, Hirst JA, Burakoff SJ: HIV Nef-mediated CD4 down-regulation is adaptor protein complex 2 dependent. J Immunol 2005, 175:3157-3164.
16. Lindwasser OW, Smith WJ, Chaudhuri R, Yang P, Hurley JH, Bonifacino JS: A diacidic motif in human immunodeficiency virus type 1 Nef is a novel determinant of binding to AP-2. J Virol 2008, 82:1166-1174.
17. Jager S, Cimermancic P, Gulbahce N, Johnson JR, McGovern KE, Clarke SC, Shales M, Mercenne G, Pache L, Li K, et al: Global landscape of HIV-human protein complexes. Nature 2012, 481:365-370.
18. Craig HM, Reddy TR, Riggs NL, Dao PP, Guatelli JC: Interactions of HIV-1 nef with the mu subunits of adaptor protein complexes 1, 2, and 3: role of the dileucine-based sorting motif. Virology 2000, 271:9-17.
19. Blagoveshchenskaya AD, Thomas L, Feliciangeli SF, Hung CH, Thomas G: HIV-1 Nef downregulates MHC-I by a PACS-1- and PI3K-regulated ARF6 endocytic pathway. Cell 2002, 111:853-866.
20. Piguet V, Wan L, Borel C, Mangasarian A, Demaurex N, Thomas G, Trono D: HIV-1 Nef protein binds to the cellular protein PACS-1 to downregulate class I major histocompatibility complexes. Nat Cell Biol 2000, 2:163-167.
21. Simons M, Raposo G: Exosomes-vesicular carriers for intercellular communication. Curr Opin Cell Biol 2009, 21:575-581.
22. Ali SA, Huang MB, Campbell PE, Roth WW, Campbell T, Khan M, Newman G, Villinger F, Powell MD, Bond VC: Genetic characterization of HIV type 1 Nef-induced vesicle secretion. AIDS Res Hum Retroviruses 2010, 26:173-192.
23. Campbell TD, Khan M, Huang MB, Bond VC, Powell MD: HIV-1 Nef protein is secreted into vesicles that can fuse with target cells and virions. Ethn Dis 2008, 18(S2):14-19.
24. Lenassi M, Cagney G, Liao M, Vaupotic T, Bartholomeeusen K, Cheng Y, Krogan NJ, Plemenitas A, Peterlin BM: HIV Nef is secreted in exosomes and triggers apoptosis in bystander CD4+ T cells. Traffic (Copenhagen, Denmark) 2010, 11:110-122.
25. Muratori C, Cavallin LE, Kratzel K, Tinari A, Muratori C, Cavallin LE, Kratzel K, Tinari AA, Fais S, D'Aloja P, Federico M, Vullo V, Fomina A, et al: Massive secretion by T cells is caused by HIV Nef in infected cells and by Nef transfer to bystander cells. Cell Host Microbe 2009, 6:218-230.
26. Shelton MN, Huang MB, Ali SA, Powell MD, Bond VC: Secretion modification region-derived peptide disrupts HIV-1 Nef's interaction with mortalin and blocks virus and Nef exosome release. JVirol 2012, 86:406-419.
27. Raymond AD, Campbell-Sims TC, Khan M, Lang M, Huang MB, Bond VC, Powell MD: HIV Type 1 Nef is released from infected cells in CD45(+) microvesicles and is present in the plasma of HIV-infected individuals. AIDS Res Human Retroviruses 2011, 27:167-178.
28. Arora VK, Molina RP, Foster JL, Blakemore JL, Chernoff J, Fredericksen BL, Garcia JV: Lentivirus Nef specifically activates Pak2. JVirol 2000, 74:11081-11087.
29. Janardhan A, Swigut T, Hill B, Myers MP, Skowronski J: HIV-1 Nef binds the DOCK2-ELMO1 complex to activate rac and inhibit lymphocyte chemotaxis. PLoS Biol 2004, 2:E6.
30. Krautkramer E, Giese SI, Gasteier JE, Muranyi W, Fackler OT: Human immunodeficiency virus type 1 Nef activates p21-activated kinase via recruitment into lipid rafts. J Virol 2004, 78:4085-4097.
31. Pulkkinen K, Renkema GH, Kirchhoff F, Saksela K: Nef associates with p21-activated kinase 2 in a p21-GTPase-dependent dynamic activation complex within lipid rafts. J Virol 2004, 78:12773-12780.
32. Renkema GH, Manninen A, Saksela K: Human immunodeficiency virus type 1 Nef selectively associates with a catalytically active subpopulation of p21-activated kinase 2 (PAK2) independently of PAK2 binding to Nck or beta-PIX. J Virol 2001, 75:2154-2160.
33. Olivieri KC, Mukerji J, Gabuzda D: Nef-mediated enhancement of cellular activation and human immunodeficiency virus type 1 replication in primary T cells is dependent on association with p21-activated kinase 2. Retrovirology 2011, 8:64.
34. Brown A, Wang X, Sawai E, Cheng-Mayer C: Activation of the PAK-related kinase by human immunodeficiency virus type 1 Nef in primary human peripheral blood lymphocytes and macrophages leads to phosphorylation of a PIX-p95 complex. J Virol 1999, 73:9899-9907.
35. Fackler OT, Luo W, Geyer M, Alberts AS, Peterlin BM: Activation of Vav by Nef induces cytoskeletal rearrangements and downstream effector functions. Mol Cell 1999, 3:729-739.
36. Linnemann T, Zheng YH, Mandic R, Peterlin BM: Interaction between Nef and phosphatidylinositol-3-kinase leads to activation of p21-activated kinase and increased production of HIV. Virology 2002, 294:246-255.
37. Rauch S, Pulkkinen K, Saksela K, Fackler OT: 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 2008, 82:2918-2929.
38. Arold S, Franken P, Strub MP, Hoh F, Benichou S, Benarous R, Dumas C: The crystal structure of HIV-1 Nef protein bound to the Fyn kinase SH3 domain suggests a role for this complex in altered T cell receptor signaling. Structure 1997, 5:1361-1372.
39. Greenway A, Azad A, Mills J, McPhee D: Human immunodeficiency virus type 1 Nef binds directly to Lck and mitogen-activated protein kinase, inhibiting kinase activity. J Virol 1996, 70:6701-6708.
40. Chu PC, Wu J, Liao XC, Pardo J, Zhao H, Li C, Mendenhall MK, Pali E, Shen M, Yu S, et al: A novel role for p21-activated protein kinase 2 in T cell activation. J Immunol 2004, 172:7324-7334.
41. Fackler OT, Alcover A, Schwartz O: Modulation of the immunological synapse: a key to HIV-1 pathogenesis? Nat Rev Immunol 2007, 7:310-317.
42. Haller C, Fackler OT: HIV-1 at the immunological and T-lymphocytic virological synapse. Biol Chem 2008, 389:1253-1260.
43. Yokosuka T, Sakata-Sogawa K, Kobayashi W, Hiroshima M, Hashimoto-Tane A, Tokunaga M, Dustin ML, Saito T: Newly generated T cell receptor microclusters initiate and sustain T cell activation by recruitment of Zap70 and SLP-76. Nat Immunol 2005, 6:1253-1262.
44. Blanchard N, Lankar D, Faure F, Regnault A, Dumont C, Raposo G, Hivroz C: TCR activation of human T cells induces the production of exosomes bearing the TCR/CD3/zeta complex. J Immunol 2002, 168:3235-3241.
45. Haller C, Rauch S, Fackler OT: HIV-1 Nef employs two distinct mechanisms to modulate Lck subcellular localization and TCR induced actin remodeling. PLoS One 2007, 2:e1212.
46. Haller C, Rauch S, Michel N, Hannemann S, Lehmann MJ, Keppler OT, Fackler OT: The HIV-1 pathogenicity factor Nef interferes with maturation of stimulatory T-lymphocyte contacts by modulation of N-Wasp activity. J Biol Chem 2006, 281:19618-19630.
47. Arhel N, Lehmann M, Clauss K, Nienhaus GU, Piguet V, Kirchhoff F: The inability to disrupt the immunological synapse between infected human T cells and APCs distinguishes HIV-1 from most other primate lentiviruses. J Clin Invest 2009, 119:2965-2975.
48. Petit C, Buseyne F, Boccaccio C, Abastado J-P, Heard J-M, Schwartz O: Nef Is Required for Efficient HIV-1 Replication in Cocultures of Dendritic Cells and Lymphocytes. Virology 2001, 286:225-236.
49. Izquierdo-useros N, Naranjo-go M, Archer J, Hatch SC, Erkizia I, Puertas MC, Connor JH, Ferna MT, Moore L: Capture and transfer of HIV-1 particles by mature dendritic cells converges with the exosome-dissemination pathway. Blood 2009, 113:2732-2741.
50. Sherer NM, Mothes W: Cytonemes and tunneling nanotubules in cell-cell communication and viral pathogenesis. Trends Cell Biol 2008, 18:414-420.
51. Sowinski S, Jolly C, Berninghausen O, Purbhoo MA, Chauveau A, Kohler K, Oddos S, Eissmann P, Brodsky FM, Hopkins C, et al: Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission. Nat Cell Biol 2008, 10:211-219.
52. Van den Broeke C, Radu M, Chernoff J, Favoreel HW: An emerging role for p21-activated kinases (Paks) in viral infections. Trends Cell Biol 2010, 20:160-169.
53. Agopian K, Wei BL, Garcia JV, Gabuzda D: A hydrophobic binding surface on the human immunodeficiency virus type 1 Nef core is critical for association with p21-activated kinase 2. J Virol 2006, 80:3050-3061.
54. Wang JK, Kiyokawa E, Verdin E, Trono D: The Nef protein of HIV-1 associates with rafts and primes T cells for activation. Proc Natl Acad Sci USA 2000, 97:394-399.
55. Sowa ME, Bennett EJ, Gygi SP, Harper JW: Defining the Human Deubiquitinating Enzyme Interaction Landscape. Cell 2009, 138:389-403.
56. Jackson PK: Navigating the Deubiquitinating Proteome with a CompPASS. Cell 2009, 138:222-224.
57. The UniProt Consortium: The Universal Protein Resource (UniProt) in 2010. Nucl Acids Res 2010, 38:D142-D148.
58. He B, Guo W: The exocyst complex in polarized exocytosis. Curr Opin Cell Biol 2009, 21:537-542.
59. Munson M, Novick P: The exocyst defrocked, a framework of rods revealed. Nat Struct Mol Biol 2006, 13:577-581.
60. Fortin JF, Barat C, Beausejour Y, Barbeau B, Tremblay MJ: Hyper-responsiveness to stimulation of human immunodeficiency virus-infected CD4+ T cells requires Nef and Tat virus gene products and results from higher NFAT, NF-kappaB, and AP-1 induction. J Biol Chem 2004, 279:39520-39531.
61. Witte V, Laffert B, Gintschel P, Krautkramer E, Blume K, Fackler OT, Baur AS: Induction of HIV transcription by Nef involves Lck activation and protein kinase C theta raft recruitment leading to activation of ERK1/2 but not NF kappa B. J Immunol 2008, 181:8425-8432.
62. Tuosto L, Marinari B, Andreotti M, Federico M, Piccolella E: Vav exchange factor counteracts the HIV-1 Nef-mediated decrease of plasma membrane GM1 and NF-AT activity in T cells. Eur J Immunol 2003, 33:2186-2196.
63. Lipschutz JH, Lingappa VR, Mostov KE: The exocyst affects protein synthesis by acting on the translocation machinery of the endoplasmic reticulum. J Biol Chem 2003, 278:20954-20960.
64. von Mering C, Jensen LJ, Snel B, Hooper SD, Krupp M, Foglierini M, Jouffre N, Huynen MA, Bork P: STRING: known and predicted protein-protein associations, integrated and transferred across organisms. Nucleic Acids Res 2005, 33:D433-D437.
65. Fielding AB, Schonteich E, Matheson J, Wilson G, Yu X, Hickson GR, Srivastava S, Baldwin SA, Prekeris R, Gould GW: Rab11-FIP3 and FIP4 interact with Arf6 and the exocyst to control membrane traffic in cytokinesis. EMBO J 2005, 24:3389-3399.
66. Hase K, Kimura S, Takatsu H, Ohmae M, Kawano S, Kitamura H, Ito M, Watarai H, Hazelett CC, Yeaman C, Ohno H: M-Sec promotes membrane nanotube formation by interacting with Ral and the exocyst complex. Nat Cell Biol 2009, 11:1427-1432.
67. Sowinski S, Alakoskela JM, Jolly C, Davis DM: Optimized methods for imaging membrane nanotubes between T cells and trafficking of HIV-1. Methods 2010, 53:27-33.
68. Ndolo T, George M, Nguyen H, Dandekar S: Expression of simian immunodeficiency virus Nef protein in CD4+ T cells leads to a molecular profile of viral persistence and immune evasion. Virology 2006, 353:374-387.
69. Hyrcza MD, Kovacs C, Loutfy M, Halpenny R, Heisler L, Yang S, Wilkins O, Ostrowski M, Der SD: Distinct transcriptional profiles in ex vivo CD4+ and CD8+ T cells are established early in human immunodeficiency virus type 1 infection and are characterized by a chronic interferon response as well as extensive transcriptional changes in CD8+ T cells. J Virol 2007, 81:3477-3486.
70. Madrid R, Janvier K, Hitchin D, Day J, Coleman S, Noviello C, Bouchet J, Benmerah A, Guatelli J, Benichou S: Nef-induced alteration of the early/ recycling endosomal compartment correlates with enhancement of HIV-1 infectivity. J Biol Chem 2005, 280:5032-5044.
71. ZhaoZ-S,LimJP,NgY-W,LimL,ManserE: The GIT-associated kinase PAK targets to the centrosome and regulates Aurora-A. Mol Cell 2005, 20:237-249.
72. Moskalenko S, Tong C, Rosse C, Mirey G, Formstecher E, Daviet L, Camonis J, White MA: Ral GTPases regulate exocyst assembly through dual subunit interactions. J Biol Chem 2003, 278:51743-51748.
73. Lim K-H, Brady DC, Kashatus DF, Ancrile BB, Der CJ, Cox AD, Counter CM: Aurora-A phosphorylates, activates, and relocalizes the small GTPase RalA. Mol Cell Biol 2010, 30:508-523.
74. Hertzog M, Chavrier P: Cell polarity during motile processes: keeping on track with the exocyst complex. Biochem J 2011, 433:403-409.
75. Zuo X, Zhang J, Zhang Y, Hsu SC, Zhou D, Guo W: Exo70 interacts with the Arp2/3 complex and regulates cell migration. Nat Cell Biol 2006, 8:1383-1388.
76. Grant BD, Donaldson JG: Pathways and mechanisms of endocytic recycling. Nat Rev Mol Cell Biol 2009, 10:597-608.
77. Chaudhry A, Das SR, Jameel S, George A, Bal V, Mayor S, Rath S: HIV-1 Nef induces a Rab11-dependent routing of endocytosed immune costimulatory proteins CD80 and CD86 to the Golgi. Traffic (Copenhagen, Denmark) 2008, 9:1925-1935.
78. Zhang XM, Ellis S, Sriratana A, Mitchell CA, Rowe T: Sec15 is an effector for the Rab11 GTPase in mammalian cells. J Biol Chem 2004, 279:43027-43034.
79. Alexander M, Bor YC, Ravichandran KS, Hammarskjold ML, Rekosh D: Human immunodeficiency virus type 1 Nef associates with lipid rafts to downmodulate cell surface CD4 and class I major histocompatibility complex expression and to increase viral infectivity. JVirol 2004, 78:1685-1696.
80. Balasubramanian N, Meier JA, Scott DW, Norambuena A, White MA, Schwartz MA: RalA-Exocyst Complex Regulates Integrin-Dependent Membrane Raft Exocytosis and Growth Signaling. Curr Biol 2010, 20:75-79.
81. Zhou H, Xu M, Huang Q, Gates AT, Zhang XD, Castle JC, Stec E, Ferrer M, Strulovici B, Hazuda DJ, Espeseth AS: Genome-scale RNAi screen for host factors required for HIV replication. Cell Host Microbe 2008, 4:495-504.
82. Brass AL, Dykxhoorn DM, Benita Y, Yan N, Engelman A, Xavier RJ, Lieberman J, Elledge SJ: Identification of host proteins required for HIV infection through a functional genomic screen. Science 2008, 319:921-926.
83. Baldari CT, Rosenbaum J: Intraflagellar transport: it's not just for cilia anymore. Curr Opin Cell Biol 2010, 22:75-80.
84. Griffiths GM, Tsun A, Stinchcombe JC: The immunological synapse: a focal point for endocytosis and exocytosis. J Cell Biol 2010, 189:399-406.
85. Zuo X, Guo W, Lipschutz JH: The Exocyst Protein Sec10 Is Necessary for Primary Ciliogenesis and Cystogenesis In Vitro. Mol Biol Cell 2009, 20:2522-2529.
86. Théry C, Ostrowski M, Segura E: Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 2009, 9:581-593.
87. Gousset K, Zurzolo C: Tunnelling nanotubes: a highway for prion spreading? Prion 2009, 3:94-98.
88. Sattentau Q: Avoiding the void: cell-to-cell spread of human viruses. Nat Rev Microbiol 2008, 6:815-826.
89. Wilson AA, Kwok LW, Hovav AH, Ohle SJ, Little FF, Fine A, Kotton DN: Sustained expression of alpha1-antitrypsin after transplantation of manipulated hematopoietic stem cells. Am J Respir Cell Mol Biol 2008, 39:133-141.
90. Zufferey R, Nagy D, Mandel RJ, Naldini L, Trono D: Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat Biotechnol 1997, 15:871-875.
91. Rho HM, Poiesz B, Ruscetti FW, Gallo RC: Characterization of the reverse transcriptase from a new retrovirus (HTLV) produced by a human cutaneous T-cell lymphoma cell line. Virology 1981, 112:355-360.
92. Konig R, Zhou Y, Elleder D, Diamond TL, Bonamy GM, Irelan JT, Chiang CY, Tu BP, De Jesus PD, Lilley CE, et al: Global analysis of host-pathogen interactions that regulate early-stage HIV-1 replication. Cell 2008, 135:49-60.
93. Yeung ML, Houzet L, Yedavalli VS, Jeang KT: A genome-wide short hairpin RNA screening of jurkat T-cells for human proteins contributing to productive HIV-1 replication. J Biol Chem 2009, 284:19463-19473.
94. VENNY: An interactive tool for comparing lists with Venn Diagrams. [http://bioinfogp.cnb.csic.es/tools/venny/index.html].