Human Immunodeficiency Virus Type 1 Nef Activates p21-Activated Kinase Via Recruitment into Lipid Rafts

Journal of Virology

Volumn 78, Issue 8, 2004, Pages 4085-4097

  Krautkrämer, Ellen ^a   Giese, Simone I ^a   Gasteier, Judith E ^a   Muranyi, Walter ^a   Fackler, Oliver T ^a  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

NEF PROTEIN; PAK KINASE; PROTEIN CDC42; PROTEIN KINASE; PROTEIN P21; RAC PROTEIN; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ARTICLE; ENZYME ACTIVATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; LEUKEMIA CELL LINE; PRIORITY JOURNAL; PROTEIN TARGETING; SIGNAL TRANSDUCTION;

CDC42 GTP-BINDING PROTEIN; CELL LINE; ENZYME ACTIVATION; GENE PRODUCTS, NEF; HIV-1; HUMANS; JURKAT CELLS; MEMBRANE MICRODOMAINS; PROTEIN-SERINE-THREONINE KINASES; RAC GTP-BINDING PROTEINS; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 12144291075     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.8.4085-4097.2004     Document Type: Article

References (76)

1. Aiken, C., J. Konner, N. R. Landau, M. E. Lenburg, and D. Trono. 1994. Nef induces CD4 endocytosis: requirement for a critical dileucine motif in the membrane-proximal CD4 cytoplasmic domain. Cell 76:853-864.
2. Aiken, C., and D. Trono. 1995. Nef stimulates human immunodeficiency virus type 1 proviral DNA synthesis. J. Virol. 69:5048-5056.
3. Arora, V. K., R. P. Molina, J. L. Foster, J. L. Blakemore, J. Chernoff, B. L. Fredericksen, and J. V. Garcia. 2000. Lentivirus Nef specifically activates Pak2. J. Virol. 74:11081-11087.
4. Bagrodia, S., and R. A. Cerione. 1999. Pak to the future. Trends Cell Biol. 9:350-355.
5. Barabe, F., E. Rollet-Labelle, C. Gilbert, M. J. Fernandes, S. N. Naccache, and P. H. Naccache. 2002. Early events in the activation of Fc gamma RIIA in human neutrophils: stimulated insolubilization, translocation to detergent-resistant domains, and degradation of Fc gamma RIIA. J. Immunol. 168:4042-4049.
6. Baur, A. S., G. Sass, B. Laffert, D. Willbold, C. Cheng-Mayer, and B. M. Peterlin. 1997. The N terminus of Nef from HIV-1/SIV associates with a protein complex containing Lck and a serine kinase. Immunity 6:283-291.
7. Benson, R. E., A. Sanfridson, J. S. Ottinger, C. Doyle, and B. R. Cullen. 1993. Downregulation of cell-surface CD4 expression by simian immunodeficiency virus Nef prevents viral super infection. J. Exp. Med. 177:1561-1566.
8. Blagoveshchenskaya, A. D., L. Thomas, S. F. Feliciangeli, C. H. Hung, and G. Thomas. 2002. HIV-1 Nef downregulates MHC-I by a PACS-1- and PI3K-regulated ARF6 endocytic pathway. Cell 111:853-866.
9. Brown, D. A., and J. K. Rose. 1992. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68:533-544.
10. Bubeck Wardenburg, J., R. Pappu, J. Y. Bu, B. Mayer, J. Chernoff, D. Straus, and A. C. Chan. 1998. Regulation of PAK activation and the T-cell cytoskeleton by the linker protein SLP-76. Immunity 9:607-616.
11. Buchwald, G., E. Hostinova, M. G. Rudolph, A. Kraemer, A. Sickmann, H. E. Meyer, K. Scheffzek, and A. Wittinghofer. 2001. Conformational switch and role of phosphorylation in PAK activation. Mol. Cell. Biol. 21:5179-5189.
12. Carl, S., T. C. Greenough, M. Krumbiegel, M. Greenberg, J. Skowronski, J. L. Sullivan, and F. Kirchhoff. 2001. Modulation of different human immunodeficiency virus type 1 Nef functions during progression to AIDS. J. Virol. 75:3657-3665.
13. Chong, C., L. Tan, L. Lim, and E. Manser. 2001. The mechanism of PAK activation. Autophosphorylation events in both regulatory and kinase domains control activity. J. Biol. Chem. 276:17347-17353.
14. Collins, K. L., B. K. Chen, S. A. Kalams, B. D. Walker, and D. Baltimore. 1998. HIV-1 Nef protein protects infected primary cells against killing by cytotoxic T lymphocytes. Nature 391:397-401.
15. Daniels, R. H., and G. M. Bokoch. 1999. p21-activated protein kinase: a crucial component of morphological signaling? Trends Biochem. Sci. 24:350-355.
16. Deacon, N. J., A. Tsykin, A. Solomon, K. Smith, M. Ludford-Menting, D. J. Hooker, D. A. McPhee, A. L. Greenway, A. Ellett, C. Chatfield, et al. 1995. Genomic structure of an attenuated quasi species of HIV-1 from a blood transfusion donor and recipients. Science 270:988-991.
17. del Pozo, M. A., L. S. Price, N. B. Alderson, X. D. Ren, and M. A. Schwartz. 2000. Adhesion to the extracellular matrix regulates the coupling of the small GTPase Rac to its effector PAK. EMBO J. 19:2008-2014.
18. Du, Z., S. M. Lang, V. G. Sasseville, A. A. Lackner, P. O. Ilyinskii, M. D. Daniel, J. U. Jung, and R. C. Desrosiers. 1995. Identification of a nef allele that causes lymphocyte activation and acute disease in macaque monkeys. Cell 82:665-674.
19. Dustin, M. L., and A. C. Chan. 2000. Signaling takes shape in the immune system. Cell 103:283-294.
20. Dustin, M. L., and J. A. Cooper. 2000. The immunological synapse and the actin cytoskeleton: molecular hardware for T-cell signaling. Nat. Immunol. 1:23-29.
21. Fackler, O. T., and A. S. Baur. 2002. Live and let die: Nef functions beyond HIV replication. Immunity 16:493-497.
22. Fackler, O. T., X. Lu, J. A. Frost, M. Geyer, B. Jiang, W. Luo, A. Abo, A. S. Alberts, and B. M. Peterlin. 2000. p21-activated kinase 1 plays a critical role in cellular activation by Nef. Mol. Cell. Biol. 20:2619-2627.
23. Fackler, O. T., W. Luo, M. Geyer, A. S. Alberts, and B. M. Peterlin. 1999. Activation of Vav by Nef induces cytoskeletal rearrangements and downstream effector functions. Mol. Cell 3:729-739.
24. Fackler, O. T., and B. M. Peterlin. 2000. Endocytic entry of HIV-1. Curr. Biol. 10:1005-1008.
25. Fackler, O. T., D. Wolf, H. O. Weber, B. Laffert, P. D'Aloja, B. Schuler-Thurner, R. Geffin, K. Saksela, M. Geyer, B. M. Peterlin, G. Schuler, and A. S. Baur. 2001. A natural variability in the proline-rich motif of Nef modulates HIV-1 replication in primary T cells. Curr. Biol. 11:1294-1299.
26. Geyer, M., O. T. Fackler, and B. M. Peterlin. 2001. Structure-function relationships in HIV-1 Nef. EMBO Rep. 2:580-585.
27. Geyer, M., H. Yu, R. Mandic, T. Linnemann, Y. H. Zheng, O. T. Fackler, and B. M. Peterlin. 2002. Subunit H of the V-ATPase binds to the medium chain of adaptor protein complex 2 and connects Nef to the endocytic machinery. J. Biol. Chem. 277:28521-28529.
28. Greenberg, M. E., S. Bronson, M. Lock, M. Neumann, G. N. Pavlakis, and J. Skowronski. 1997. Co-localization of HIV-1 Nef with the AP-2 adaptor protein complex correlates with Nef-induced CD4 down-regulation. EMBO J. 16:6964-6976.
29. Hanna, Z., D. G. Kay, N. Rebai, A. Guimond, S. Jothy, and P. Jolicoeur. 1998. Nef harbors a major determinant of pathogenicity for an AIDS-like disease induced by HIV-1 in transgenic mice. Cell 95:163-175.
30. Hanna, Z., X. Weng, D. G. Kay, J. Poudrier, C. Lowell, and P. Jolicoeur. 2001. The pathogenicity of human immunodeficiency virus (HIV) type 1 Nef in CD4C/HIV transgenic mice is abolished by mutation of its SH3-binding domain, and disease development is delayed in the absence of Hck. J. Virol. 75:9378-9392.
31. Janes, P. W., S. C. Ley, and A. I. Magee. 1999. Aggregation of lipid rafts accompanies signaling via the T-cell antigen receptor. J. Cell Biol. 147:447-461.
32. Janes, P. W., S. C. Ley, A. I. Magee, and P. S. Kabouridis. 2000. The role of lipid rafts in T-cell antigen receptor (TCR) signaling. Semin. Immunol. 12:23-34.
33. Kirchhoff, F., T. C. Greenough, D. B. Brettler, J. L. Sullivan, and R. C. Desrosiers. 1995. Brief report: absence of intact nef sequences in a long-term survivor with nonprogressive HIV-1 infection. N. Engl. J. Med. 332:228-232.
34. Lama, J., A. Mangasarian, and D. Trono. 1999. Cell-surface expression of CD4 reduces HIV-1 infectivity by blocking Env incorporation in a Nef- and Vpu-inhibitable manner. Curr. Biol. 9:622-631.
35. Lang, S. M., A. J. Iafrate, C. Stahl-Hennig, E. M. Kuhn, T. Nisslein, F. J. Kaup, M. Haupt, G. Hunsmann, J. Skowronski, and F. Kirchhoff. 1997. Association of simian immunodeficiency virus Nef with cellular serine/threonine kinases is dispensable for the development of AIDS in rhesus macaques. Nat. Med. 3:860-865.
36. Le Gall, S., L. Erdtmann, S. Benichou, C. Berlioz-Torrent, L. Liu, R. Benarous, J. M. Heard, and O. Schwartz. 1998. Nef interacts with the mu subunit of clathrin adaptor complexes and reveals a cryptic sorting signal in MHC I molecules. Immunity 8:483-495.
37. Lei, M., W. Lu, W. Meng, M. C. Parrini, M. J. Eck, B. J. Mayer, and S. C. Harrison. 2000. Structure of PAK1 in an autoinhibited conformation reveals a multistage activation switch. Cell 102:387-397.
38. Liu, X., J. A. Schrager, G. D. Lange, and J. W. Marsh. 2001. HIV Nef-mediated cellular phenotypes are differentially expressed as a function of intracellular Nef concentrations. J. Biol. Chem. 276:32763-32770.
39. Lu, W., S. Katz, R. Gupta, and B. J. Mayer. 1997. Activation of Pak by membrane localization mediated by an SH3 domain from the adaptor protein Nck. Curr. Biol. 7:85-94.
40. Lu, W., and B. J. Mayer. 1999. Mechanism of activation of Pak1 kinase by membrane localization. Oncogene 18:797-806.
41. Lu, X., X. Wu, A. Plemenitas, H. Yu, E. T. Sawai, A. Abo, and B. M. Peterlin. 1996. CDC42 and Rac1 are implicated in the activation of the Nef-associated kinase and replication of HIV-1. Curr. Biol. 6:1677-1684.
42. Lu, X., H. Yu, S. H. Liu, F. M. Brodsky, and B. M. Peterlin. 1998. Interactions between HIV1 Nef and vacuolar ATPase facilitate the internalization of CD4. Immunity 8:647-656.
43. Luo, W., and B. M. Peterlin. 1997. Activation of the T-cell receptor signaling pathway by Nef from an aggressive strain of simian immunodeficiency virus. J. Virol. 71:9531-9537.
44. Manninen, A., M. Hiipakka, M. Vihinen, W. Lu, B. J. Mayer, and K. Saksela. 1998. SH3-Domain binding function of HIV-1 Nef is required for association with a PAK-related kinase. Virology 250:273-282.
45. Messmer, D., R. Ignatius, C. Santisteban, R. M. Steinman, and M. Pope. 2000. The decreased replicative capacity of simian immunodeficiency virus SIVmac239Delta(nef) is manifest in cultures of immature dendritic cells and T cells. J. Virol. 74:2406-2413.
46. Millan, J., M. C. Montoya, D. Sancho, F. Sanchez-Madrid, and M. A. Alonso. 2002. Lipid rafts mediate biosynthetic transport to the T lymphocyte uropod subdomain and are necessary for uropod integrity and function. Blood 99:978-984.
47. Montixi, C., C. Langlet, A. M. Bernard, J. Thimonier, C. Dubois, M. A. Wurbel, J. P. Chauvin, M. Pierres, and H. T. He. 1998. Engagement of T-cell receptor triggers its recruitment to low-density detergent-insoluble membrane domains. EMBO J. 17:5334-5348.
48. Nunn, M. F., and J. W. Marsh. 1996. Human immunodeficiency virus type 1 Nef associates with a member of the p21-activated kinase family. J. Virol. 70:6157-6161.
49. Parrini, M. C., M. Lei, S. C. Harrison, and B. J. Mayer. 2002. Pak1 kinase homodimers are autoinhibited in trans and dissociated upon activation by Cdc42 and Rac1. Mol. Cell 9:73-83.
50. Petit, C., F. Buseyne, C. Boccaccio, J. P. Abastado, J. M. Heard, and O. Schwartz. 2001. Nef is required for efficient HIV-1 replication in cocultures of dendritic cells and lymphocytes. Virology 286:225-236.
51. Piguet, V., Y. L. Chen, A. Mangasarian, M. Foti, J. L. Carpentier, and D. Trono. 1998. Mechanism of Nef-induced CD4 endocytosis: Nef connects CD4 with the mu chain of adaptor complexes. EMBO J. 17:2472-2481.
52. Piguet, V., L. Wan, C. Borel, A. Mangasarian, N. Demaurex, G. Thomas, and D. Trono. 2000. HIV-1 Nef protein binds to the cellular protein PACS-1 to downregulate class I major histocompatibility complexes. Nat. Cell Biol. 2:163-167.
53. Renkema, G. H., A. Manninen, D. A. Mann, M. Harris, and K. Saksela. 1999. Identification of the Nef-associated kinase as p21-activated kinase 2. Curr. Biol. 9:1407-1410.
54. Renkema, G. H., A. Manninen, and K. Saksela. 2001. 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. 75:2154-2160.
55. Renkema, G. H., K. Pulkkinen, and K. Saksela. 2002. Cdc42/Rac1-mediated activation primes PAK2 for superactivation by tyrosine phosphorylation. Mol. Cell. Biol. 22:6719-6725.
56. Resh, M. D. 1999. Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins. Biochim. Biophys. Acta 1451:1-16.
57. Ross, T. M., A. E. Oran, and B. R. Cullen. 1999. Inhibition of HIV-1 progeny virion release by cell-surface CD4 is relieved by expression of the viral Nef protein. Curr. Biol. 9:613-621.
58. Saksela, K., G. Cheng, and D. Baltimore. 1995. Proline-rich (PxxP) motifs in HIV-1 Nef bind to SH3 domains of a subset of Src kinases and are required for the enhanced growth of Nef+ viruses but not for down-regulation of CD4. EMBO J. 14:484-491.
59. Sawai, E. T., A. Baur, H. Struble, B. M. Peterlin, J. A. Levy, and C. Cheng-Mayer. 1994. Human immunodeficiency virus type 1 Nef associates with a cellular serine kinase in T lymphocytes. Proc. Natl. Acad. Sci. USA 91:1539-1543.
60. Sawai, E. T., A. S. Baur, B. M. Peterlin, J. A. Levy, and C. Cheng-Mayer. 1995. A conserved domain and membrane targeting of Nef from HIV and SIV are required for association with a cellular serine kinase activity. J. Biol. Chem. 270:15307-15314.
61. Sawai, E. T., I. H. Khan, P. M. Montbriand, B. M. Peterlin, C. Cheng-Mayer, and P. A. Luciw. 1996. Activation of PAK by HIV and SIV Nef: importance for AIDS in rhesus macaques. Curr. Biol. 6:1519-1527.
62. Schrager, J. A., and J. W. Marsh. 1999. HIV-1 Nef increases T-cell activation in a stimulus-dependent manner. Proc. Natl. Acad. Sci. USA 96:8167-8172.
63. Schwartz, O., V. Marechal, O. Danos, and J. M. Heard. 1995. Human immunodeficiency virus type 1 Nef increases the efficiency of reverse transcription in the infected cell. J. Virol. 69:4053-4059.
64. Schwartz, O., V. Marechal, S. Le Gall, F. Lemonnier, and J. M. Heard. 1996. Endocytosis of major histocompatibility complex class I molecules is induced by the HIV-1 Nef protein. Nat. Med. 2:338-342.
65. Simmons, A., V. Aluvihare, and A. McMichael. 2001. Nef triggers a transcriptional program in T cells imitating single-signal T-cell activation and inducing HIV virulence mediators. Immunity 14:763-777.
66. Simons, K., and D. Toomre. 2000. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1:31-39.
67. Stevenson, M., T. L. Stanwick, M. P. Dempsey, and C. A. Lamonica. 1990. HIV-1 replication is controlled at the level of T-cell activation and proviral integration. EMBO J. 9:1551-1560.
68. Swingler, S., A. Mann, J. Jacque, B. Brichacek, V. G. Sasseville, K. Williams, A. A. Lackner, E. N. Janoff, R. Wang, D. Fisher, and M. Stevenson. 1999. HIV-1 Nef mediates lymphocyte chemotaxis and activation by infected macrophages. Nat. Med. 5:997-1003.
69. Walk, S. F., M. Alexander, B. Maier, M. L. Hammarskjold, D. M. Rekosh, and K. S. Ravichandran. 2001. Design and use of an inducibly activated human immunodeficiency virus type 1 Nef to study immune modulation. J. Virol. 75:834-843.
70. Wang, J. K., E. Kiyokawa, E. Verdin, and D. Trono. 2000. The Nef protein of HIV-1 associates with rafts and primes T cells for activation. Proc. Natl. Acad. Sci. USA 97:394-399.
71. Wolf, D., V. Witte, B. Laffert, K. Blume, E. Stromer, S. Trapp, P. d'Aloja, A. Schurmann, and A. S. Baur. 2001. HIV-1 Nef associated PAK and PI3-kinases stimulate Akt-independent Bad-phosphorylation to induce anti-apoptotic signals. Nat. Med. 7:1217-1224.
72. Wu, Y., and J. W. Marsh. 2001. Selective transcription and modulation of resting T-cell activity by preintegrated HIV DNA. Science 293:1503-1506.
73. Xavier, R., T. Brennan, Q. Li, C. McCormack, and B. Seed. 1998. Membrane compartmentation is required for efficient T-cell activation. Immunity 8:723-732.
74. Zack, J. A., S. J. Arrigo, S. R. Weitsman, A. S. Go, A. Haislip, and I. S. Chen. 1990. HIV-1 entry into quiescent primary lymphocytes: molecular analysis reveals a labile, latent viral structure. Cell 61:213-222.
75. Zenke, F. T., C. C. King, B. P. Bohl, and G. M. Bokoch. 1999. Identification of a central phosphorylation site in p21-activated kinase regulating autoinhibition and kinase activity. J. Biol. Chem. 274:32565-32573.
76. Zheng, Y. H., A. Plemenitas, T. Linnemann, O. T. Fackler, and B. M. Peterlin. 2001. Nef increases infectivity of HIV via lipid rafts. Curr. Biol. 11:875-879.