Detection of human immunodeficiency virus type 1 Nef and CD4 physical interaction in living human cells by using bioluminescence resonance energy transfer

Journal of Virology

Volumn 79, Issue 13, 2005, Pages 8629-8636

  Cluet, David ^a   Bertsch, Christophe ^a,b   Beyer, Christian ^a   Gloeckler, Liliane ^a   Erhardt, Mathieu ^a,c   Gut, Jean Pierre ^a   Galzi, Jean Luc ^a   Aubertin, Anne Marie ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b UNIVERSITÉ DE HAUTE ALSACE   (France)

^c INST DE BIOL MOLEC DES PLANTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; NEF PROTEIN;

ARTICLE; BIOLUMINESCENCE RESONANCE ENERGY TRANSFER; COMPLEX FORMATION; CONTROLLED STUDY; CYTOPLASM; DOWN REGULATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; VIRUS DETECTION; VIRUS VIRULENCE;

ANTIGENS, CD; ANTIGENS, CD4; BACTERIAL PROTEINS; BINDING SITES; CD4-POSITIVE T-LYMPHOCYTES; CELL LINE; GENE PRODUCTS, NEF; GENES, REPORTER; HIV-1; HUMANS; KIDNEY; LUMINESCENT MEASUREMENTS; LUMINESCENT PROTEINS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 20744447725     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.13.8629-8636.2005     Document Type: Article

References (56)

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. Alexander, L., Z. Du, M. Rosenzweig, J. U. Jung, and R. C. Desrosiers. 1997. A role for natural simian immunodeficiency virus and human immunodeficiency virus type 1 nef alleles in lymphocyte activation. J. Virol. 71:6094-6099.
3. Alexander, M., Y. Bor, K. S. Ravichandran, M.-L. Hammarsjöld, and D. Rekosh. 2004. 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. J. Virol. 78: 1685-1696.
4. Angers, S., A. Salahpour, E. Joly, S. Hilairet, D. Chelsky, M. Dennis, and M. Bouvier. 2000. Detection of β2-adrenergic receptor dimerization in living cells using bioluminescence resonance energy transfer (BRET). Proc. Natl. Acad. Sci. USA 97:3684-3689.
5. Arold, S., F. Hoh, S. Domergue, C. Birk, M. A. Delsuc, M. Jullien, and C. Dumas. 2000. Characterization and molecular basis of the oligomeric structure of HIV-1 Nef protein. Protein Sci. 9:1137-1148.
6. Bell, I., T. M. Schaefer, R. P. Trible, A. Amedee, and T. A. Reinhart. 2001. Down-modulation of the costimulatory molecule, CD28, is a conserved activity of multiple SIV Nefs and is dependent on histidine 196 of Nef. Virology 283:148-158.
7. Bell, I., C. Ashman, J. Maughan, E. Hooker, F. Cook, and T. A. Reinhart. 1998. Association of simian immunodeficiency virus Nef with the T-cell receptor (TCR) zeta chain leads to TCR down-modulation. J. Gen. Virol. 79:2717-2727.
8. Benichou, S., M. Bomsel, M. Bodeus, H. Durand, M. Doute, F. Letourneur, J. Camonis, and R. Benarous. 1994. Physical interaction of the HIV-1 Nef protein with beta-COP, a component of non-clathrin-coated vesicles essential for membrane traffic. J. Biol. Chem. 269:30073-30076.
9. Bentham, M., S. Mazaleyrat, and M. Harris. 2003. The di-leucine motif in the cytoplasmic tail of CD4 is not required for binding to human immunodeficiency virus type 1 Nef, but is critical for CD4 down-modulation. J. Gen. Virol. 84:2705-2713.
10. Boute, N., K. Pernet, and T. Issad. 2001. Monitoring the activation state of the insulin receptor using bioluminescence resonance energy transfer. Mol. Pharmacol. 60:640-645.
11. Bresnahan, P. A., W. Yonemoto, S. Ferrell, D. Williams-Herman, R. Geleziunas, and W. C. Greene. 1998. A dileucine motif in HIV-1 Nef acts as an internalization signal for CD4 downregulation and binds the AP-1 clathrin adaptor. Curr. Biol. 8:1235-1238.
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. Chen, Y.-L., D. Trono, and D. Camaur. 1998. The proteolytic cleavage of human immunodeficiency virus type 1 Nef does not correlate with its ability to stimulate virion infectivity. J. Virol. 72:3178-3184.
14. Cheng, Z.-J., and L. J. Miller. 2001. Agonist-dependent dissociation of oligomeric complexes of G protein-coupled cholecystokinin receptors demonstrated in living cells using bioluminescence resonance energy transfer. J. Biol. Chem. 276:48040-48047.
15. Chowers, M. Y., C. A. Spina, T. J. Kwoh, N. J. S. Fitch, D. D. Richman, and J. C. Guatelli. 1994. Optimal infectivity in vitro of human immunodeficiency virus type 1 requires an intact nef gene. J. Virol. 68:2906-2914.
16. Craig, H. M., T. R. Reddy, N. L. Riggs, P. P. Dao, and J. C. Guatelli. 2000. 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 271:9-17.
17. Deacon, N. J., A. Tsykin, A. Solomon, K. Smith, M. Ludford-Menting, D. J. Hooker, D. A. McPhee, A. L. Greenway, A. Ellett, and C. Chatfield. 1995. Genomic structure of an attenuated quasi species of HIV-1 from a blood transfusion donor and recipients. Science 270:988-991.
18. Garcia, J. V., and A. D. Miller. 1991. Serine phosphorylation-independent downregulation of cell-surface CD4 by nef. Nature 350:508-511.
19. Geleziunas, R., W. Xhu, K. Takeda, H. Ichijo, and W. C. Green. 2001. HIV-1 Nef inhibits ASK1-dependent death signalling providing a potential mechanism for protecting the infecting host cell. Nature 410:834-838.
20. 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 AP-2 and connects Nef to the endocytic machinery. J. Biol. Chem. 277: 28521-28529.
21. + T-cell depletion in human lymphoid tissue ex vivo. J. Virol. 75:10113-10117.
22. 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. 16:10113-10117.
23. Grzesiek, S., S. J. Stahl, P. T. Wingfield, and A. Bax. 1996. The CD4 determinant for downregulation by HIV-1 Nef directly binds to Nef. Mapping of the Nef binding surface by NMR. Biochemistry 35:10256-10261.
24. Harris, M. P., and J. C. Neil. 1994. Myristoylation-dependent binding of HIV-1 Nef to CD4. J. Mol. Biol. 241:136-142.
25. Hua, J., W. Blair, R. Truant, and B. R. Cullen. 1997. Identification of regions in HIV-1 Nef required for efficient downregulation of cell surface CD4. Virology 231:231-238.
26. Janvier, K., H. Craig, S. Le Gall, R. Benarous, J. Guatelli, O. Schwartz, and S. Benichou. 2001. Nef-induced CD4 downregulation: a diacidic sequence in human immunodeficiency virus type 1 Nef does not function as a protein sorting motif through direct binding to β-COP. J. Virol. 75:3971-3976.
27. Jason, J., and K. L. Inge. 2001. Modulation of CD8 and CD3 by HIV or HIV antigens. J. Immunol. 53:259-267.
28. Kestler, H. W., III, D. J. Ringler, K. Mori, D. L. Panicali, P. K. Sehgal, M. D. Daniel, and R. C. Desrosiers. 1991. Importance of the nef gene for maintenance of high virus loads and for development of AIDS. Cell 65:651-652.
29. Kienzle, N., J. Freund, H. R. Kalbitzer, and N. Mueller-Lantzsch. 1993. Oligomerization of the Nef protein from human immunodeficiency virus (HIV) type 1. Eur. J. Biochem. 214:451-457.
30. 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.
31. Liu, X. L., N. Heveker, O. T. Fackler, S. Arold, S. Le Gall, K. Janvier, B. M. Peterlin, C. Dumas, O. Schwartz, S. Benichou, and R. Benarous. 2000. Mutation of a conserved residue (D123) required for oligomerization of human immunodeficiency virus type 1 Nef protein abolishes interaction with human thioesterase and results in impairment of Nef biological functions. J. Virol. 74:5310-5319.
32. Lock, M., M. E. Greenberg, A. J. Iafrate, T. Swigut, J. Muench, F. Kirchhoff, N. Shohdy, and J. Skowronski. 1999. Two elements target SIV Nef to the AP-2 clathrin adaptor complex, but only one is required for the induction of CD4 endocytosis. EMBO J. 18:2722-2733.
33. Lundquist, C. A., M. Tobiume, J. Zhou, D. Unutmaz, and C. Aiken. 2002. Nef-mediated downregulation of CD4 enhances human immunodeficency virus type 1 replication in primary T lymphocytes. J. Virol. 76:4625-4633.
34. Mandic, R., O. T. Fackler, M. Geyer, T. Linnemann, Y. H. Zheng, and B. M. Peterlin. 2001. Negative factor from SIV binds to the catalytic subunit of the V-ATPase to internalize CD4 and to increase viral infectivity. Mol. Biol. Cell 12:463-473.
35. Mangasarian, A., V. Piguet, J.-K. Wang, Y.-L. Chen, and D. Trono. 1999. Nef-induced CD4 and major histocompatibility complex class I (MHC-I) down regulation are governed by distinct determinants: N-terminal alpha helix and proline repeat of Nef selectively regulate MHC-I trafficking. J. Virol. 73:1964-1973.
36. McVey, M., D. Ramsay, E. Kellett, S. Rees, S. Wilson, A. J. Pope, and G. Milligan. 2001. Monitoring receptor oligomerization using time-resolved fluorescence resonance energy transfer and bioluminescence resonance energy transfer. J. Biol. Chem. 276:14092-14099.
37. Miller, M. D., M. T. Warmerdam, I. Gaston, W. C. Greene, and M. B. Feinberg. 1994. The human immunodeficiency virus-1 nef gene product: a positive factor for viral infection and replication in primary lymphocytes and macrophages. J. Exp Med. 179:101-113.
38. 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 μ chain of adaptor complexes. EMBO J. 17:2472-2481.
39. Piguet, V., F. Gu, M. Foti, N. Demaurex, J. Gruenberg, J.-L. Carpentier, and D. Trono. 1999. Nef-induced CD4 degradation: a diacidic-based motif in Nef functions as a lysosomal targetting signal through the binding of β-COP in endosomes. Cell 97:63-73.
40. Poulin, L., and J. A. Levy. 1992. The HIV-1 nef gene product is associated with phosphorylation of a 46 kD cellular protein. AIDS 6:787-791.
41. Preusser, A., L. Briese, A. Baur, and D. Willbord. 2001. Direct in vitro binding of full-length human immunodeficiency virus type 1 Nef protein to CD4 cytoplasmic domain. J. Virol. 75:3960-3964.
42. Rossi, F., A. Gallina, and G. Milanesi. 1996. Nef-CD4 physical interaction sensed with the yeast two-hybrid system. Virology 217:397-403.
43. Salvi, R., A. R. Garbuglia, A. Di Caro, S. Pulciani, F. Montella, and A. Benedetto. 1998. Grossly defective nef gene sequences in a human immunodeficiency virus type 1 seropositive long-term nonprogressor. J. Virol. 72: 3646-3657.
44. 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.
45. Schaeffer, E., R. Geleziunas, and W. C. Greene. 2001. Human immunodeficiency type 1 Nef functions at the level of virus entry by enhancing cytoplasmic delivery of virions. J. Virol. 75:2993-3000.
46. Schwartz, O., V. Marechal, S. Le Gall, F. Lemmonier, and J.-M. Heard. 1996. Endocytosis of major histocompatibility complex class I molecules is induced by the HIV-1 Nef protein. Nat. Med. 2:338-341.
47. 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.
48. Sol-Foulon, N., C. Esnault, Y. Pecherancier, F. Porrot, P. Metais-Cunha, F. Bachelerie, and O. Schwartz. 2004. The effects of Nef on CD4 surface expression and viral infectivity in lymphoid cells are independent of rafts. J. Biol. Chem. 279:31398-31408.
49. Spina, C. A., T. J. Kwoh, M. Y. Chowers, J. C. Guatelli, and D. D. Richman. 1994. The importance of nef in the induction of human immunodeficiency virus type 1 replication from primary quiescent CD4 lymphocytes. J. Exp. Med. 179:115-123.
50. Swigut, T., N. Shohdy, and J. Skowronski. 2001. Mechanism for down-regulation of CD28 by Nef. EMBO J. 20:1593-1604.
51. Valenzuela-Fernandez, A., T. Palanche, A. Amara, A. Magerus, R. Altmeyer, T. Delaunay, J. L. Virelizier, F. Baleux, J. L. Galzi, and F. Arenzana-Seisdedos. 2001. Optimal inhibition of X4 HIV isolates by the CXC chemokine stromal cell-derived factor 1 alpha requires interaction with cell surface heparan sulfate proteoglycans. J. Biol. Chem. 276:26550-26558.
52. Vollmer, J. Y., P. Alix, A. Chollet, K. Takeda, and J. L. Galzi. 1999. Subcellular compartimentalization of activation and desensitization of responses mediated by NK2 neurokinin receptors. J. Biol. Chem. 274:37915-37922.
53. Willard-Gallo, K. E., M. Furtado, A. Burny, and S. M. Wolinsky. 2001 Down-modulation of TCR/CD3 surface complexes after HIV-1 infection is associated with differential expression of the viral regulatory genes. Eur. J. Immunol. 31:969-979.
54. Wolf, D., V. Witte, B. Laffert, K. Blume, E. Stromer, S. Trapp, P. D'Aloja, A. Schürmann, and A. S. Baur. 2001. HIV-1 Nef associated PAK and PI3-kinases stimulate Akt-independent Bad-phosphorylation to induce antiapoptotic signals. Nat. Med. 7:1217-1224.
55. Xu, Y., D. W. Piston, and C. H. Johnson. 1999. A bioluminescence resonance energy transfer (BRET) system: application to interacting circadian clock proteins. Proc. Natl. Acad. Sci. USA 96:151-156.
56. Zhou, J., and C. Aiken. 2001. Nef enhances human immunodeficiency virus type 1 infectivity resulting from intervirion fusion: evidence supporting a role for Nef at the virion envelope. J. Virol. 75:5851-5859.