Nef-induced CD4 endocytosis in human immunodeficiency virus type 1 host cells: Role of p56lck kinase

Journal of Virology

Volumn 83, Issue 14, 2009, Pages 7117-7128

  Laguette, Nadine ^a,b   Brégnard, Christelle ^a,b   Bouchet, Jérôme ^a,b   Benmerah, Alexandre ^a,b   Benichou, Serge ^a,b   Basmaciogullari, Stéphane ^a,b  

^a INSTITUT COCHIN   (France)

^b INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; MUTANT PROTEIN; NEF PROTEIN; PROTEIN KINASE LCK; PROTEIN P56;

ARTICLE; BONE MARROW CULTURE; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME ANALYSIS; HOST CELL; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INTERNALIZATION; LYMPHOID CELL LINE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; VIRUS CELL INTERACTION;

AMINO ACID SEQUENCE; ANTIGENS, CD4; CELL LINE; DOWN-REGULATION; ENDOCYTOSIS; GENE EXPRESSION; HIV INFECTIONS; HIV-1; HUMANS; LYMPHOCYTE SPECIFIC PROTEIN TYROSINE KINASE P56(LCK); LYMPHOCYTES; MOLECULAR SEQUENCE DATA; NEF GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; PROTEIN BINDING;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 67650410034     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01648-08     Document Type: Article

References (75)

1. Aiken, C. 1997. Pseudotyping human immunodeficiency virus type 1 (HIV-1) by the glycoprotein of vesicular stomatitis virus targets HIV-1 entry to an endocytic pathway and suppresses both the requirement for Nef and the sensitivity to cyclosporin A. J. Virol. 71:5871-5877.
2. 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.
3. Arganaraz, E. R., M. Schindler, F. Kirchhoff, M. J. Cortes, and J. Lama. 2003. Enhanced CD4 down-modulation by late stage HIV-1 nef alleles is associated with increased Env incorporation and viral replication. J. Biol. Chem. 278:33912-33919.
4. Basmaciogullari, S., B. Pacheco, S. Bour, and J. Sodroski. 2006. Specific interaction of CXCR4 with CD4 and CD8alpha: functional analysis of the CD4/CXCR4 interaction in the context of HIV-1 envelope glycoprotein-mediated membrane fusion. Virology 353:52-67.
5. 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.
6. Birch, M. R., J. C. Learmont, W. B. Dyer, N. J. Deacon, J. J. Zaunders, N. Saksena, A. L. Cunningham, J. Mills, and J. S. Sullivan. 2001. An examination of signs of disease progression in survivors of the Sydney Blood Bank Cohort (SBBC). J. Clin. Virol. 22:263-270.
7. 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.
8. Bour, S., C. Perrin, and K. Strebel. 1999. Cell surface CD4 inhibits HIV-1 particle release by interfering with Vpu activity. J. Biol. Chem. 274:33800-33806.
9. 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.
10. Burtey, A., J. Z. Rappoport, J. Bouchet, S. Basmaciogullari, J. Guatelli, S. M. Simon, S. Benichou, and A. Benmerah. 2007. Dynamic interaction of HIV-1 Nef with the clathrin-mediated endocytic pathway at the plasma membrane. Traffic 8:61-76.
11. 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.
12. Chaudhuri, R., O. W. Lindwasser, W. J. Smith, J. H. Hurley, and J. S. Bonifacino. 2007. Downregulation of CD4 by human immunodeficiency virus type 1 Nef is dependent on clathrin and involves direct interaction of Nef with the AP2 clathrin adaptor. J. Virol. 81:3877-3890.
13. Chowers, M. Y., C. A. Spina, T. J. Kwoh, N. J. 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.
14. Cluet, D., C. Bertsch, C. Beyer, L. Gloeckler, M. Erhardt, J. P. Gut, J. L. Galzi, and A. M. Aubertin. 2005. Detection of human immunodeficiency virus type 1 Nef and CD4 physical interaction in living human cells by using bioluminescence resonance energy transfer. J. Virol. 79:8629-8636.
15. Coleman, S. H., N. Van Damme, J. R. Day, C. M. Noviello, D. Hitchin, R. Madrid, S. Benichou, and J. C. Guatelli. 2005. Leucine-specific, functional interactions between human immunodeficiency virus type 1 Nef and adaptor protein complexes. J. Virol. 79:2066-2078.
16. Collins, K. L., and D. Baltimore. 1999. HIV's evasion of the cellular immune response. Immunol. Rev. 168:65-74.
17. Dyer, W. B., A. F. Geczy, S. J. Kent, L. B. McIntyre, S. A. Blasdall, J. C. Learmont, and J. S. Sullivan. 1997. Lymphoproliferative immune function in the Sydney Blood Bank Cohort, infected with natural nef/long terminal repeat mutants, and in other long-term survivors of transfusion-acquired HIV-1 infection. AIDS 11:1565-1574.
18. Foti, M., L. Cartier, V. Piguet, D. P. Lew, J. L. Carpentier, D. Trono, and K. H. Krause. 1999. The HIV Nef protein alters Ca(2+) signaling in myelomonocytic cells through SH3-mediated protein-protein interactions. J. Biol. Chem. 274:34765-34772.
19. Foti, M., A. Mangasarian, V. Piguet, D. P. Lew, K. H. Krause, D. Trono, and J. L. Carpentier. 1997. Nef-mediated clathrin-coated pit formation. J. Cell Biol. 139:37-47.
20. Garcia, J. V., and A. D. Miller. 1991. Serine phosphorylation- independent downregulation of cell-surface CD4 by nef. Nature 350:508-511.
21. Geleziunas, R., S. Bour, and M. A. Wainberg. 1994. Cell surface down-modulation of CD4 after infection by HIV-1. FASEB J. 8:593-600.
22. Geyer, M., O. T. Fackler, and B. M. Peterlin. 2001. Structure-function relationships in HIV-1 Nef. EMBO Rep. 2:580-585.
23. Goldsmith, M. A., M. T. Warmerdam, R. E. Atchison, M. D. Miller, and W. C. Greene. 1995. Dissociation of the CD4 downregulation and viral infectivity enhancement functions of human immunodeficiency virus type 1 Nef. J. Virol. 69:4112-4121.
24. Gratton, S., X. J. Yao, S. Venkatesan, E. A. Cohen, and R. P. Sekaly. 1996. Molecular analysis of the cytoplasmic domain of CD4: overlapping but non-competitive requirement for lck association and down-regulation by Nef. J. Immunol. 157:3305-3311.
25. Greenberg, M., L. DeTulleo, I. Rapoport, J. Skowronski, and T. Kirchhausen. 1998. A dileucine motif in HIV-1 Nef is essential for sorting into clathrin-coated pits and for downregulation of CD4. Curr. Biol. 8:1239-1242.
26. 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.
27. Greene, W. C., and B. M. Peterlin. 2002. Charting HIV's remarkable voyage through the cell: basic science as a passport to future therapy. Nat. Med. 8:673-680.
28. Greenway, A., A. Azad, J. Mills, and D. McPhee. 1996. Human immunodeficiency virus type 1 Nef binds directly to Lck and mitogen-activated protein kinase, inhibiting kinase activity. J. Virol. 70:6701-6708.
29. 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.
30. Haller, C., S. Rauch, and O. T. Fackler. 2007. HIV-1 Nef employs two distinct mechanisms to modulate Lck subcellular localization and TCR induced actin remodeling. PLoS ONE 2:e1212.
31. 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 beta-COP. J. Virol. 75:3971-3976.
32. Jin, Y. J., C. Y. Cai, X. Zhang, H. T. Zhang, J. A. Hirst, and S. J. Burakoff. 2005. HIV Nef-mediated CD4 down-regulation is adaptor protein complex 2 dependent. J. Immunol. 175:3157-3164.
33. Jin, Y. J., X. Zhang, J. G. Boursiquot, and S. J. Burakoff. 2004. CD4 phosphorylation partially reverses Nef down-regulation of CD4. J. Immunol. 173:5495-5500.
34. Kim, Y. H., S. H. Chang, J. H. Kwon, and S. S. Rhee. 1999. HIV-1 Nef plays an essential role in two independent processes in CD4 down-regulation: dissociation of the CD4-p56(lck) complex and targeting of CD4 to lysosomes. Virology 257:208-219.
35. Klatzmann, D., E. Champagne, S. Chamaret, J. Gruest, D. Guetard, T. Hercend, J. C. Gluckman, and L. Montagnier. 1984. T-lymphocyte T4 molecule behaves as the receptor for human retrovirus LAV. Nature 312:767-768.
36. 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.
37. Learmont, J. C., A. F. Geczy, J. Mills, L. J. Ashton, C. H. Raynes-Greenow, R. J. Garsia, W. B. Dyer, L. McIntyre, R. B. Oelrichs, D. I. Rhodes, N. J. Deacon, and J. S. Sullivan. 1999. Immunologic and virologic status after 14 to 18 years of infection with an attenuated strain of HIV-1. A report from the Sydney Blood Bank Cohort. N. Engl. J. Med. 340:1715-1722.
38. 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.
39. Lindwasser, O. W., W. J. Smith, R. Chaudhuri, P. Yang, J. H. Hurley, and J. S. Bonifacino. 2008. A diacidic motif in human immunodeficiency virus type 1 Nef is a novel determinant of binding to AP-2. J. Virol. 82:1166-1174.
40. Luo, T., S. J. Anderson, and J. V. Garcia. 1996. Inhibition of Nef- and phorbol ester-induced CD4 degradation by macrolide antibiotics. J. Virol. 70:1527-1534.
41. Luo, T., J. R. Downing, and J. V. Garcia. 1997. Induction of phosphorylation of human immunodeficiency virus type 1 Nef and enhancement of CD4 downregulation by phorbol myristate acetate. J. Virol. 71:2535-2539.
42. Lynch, G. W., S. Turville, B. Carter, A. J. Sloane, A. Chan, N. Muljadi, S. Li, L. Low, P. Armati, R. Raison, H. Zoellner, P. Williamson, A. Cunningham, and W. B. Church. 2006. Marked differences in the structures and protein associations of lymphocyte and monocyte CD4: resolution of a novel CD4 isoform. Immunol. Cell Biol. 84:154-165.
43. Madrid, R., K. Janvier, D. Hitchin, J. Day, S. Coleman, C. Noviello, J. Bouchet, A. Benmerah, J. Guatelli, and S. Benichou. 2005. Nef-induced alteration of the early/recycling endosomal compartment correlates with enhancement of HIV-1 infectivity. J. Biol. Chem. 280:5032-5044.
44. Mangasarian, A., M. Foti, C. Aiken, D. Chin, J. L. Carpentier, and D. Trono. 1997. The HIV-1 Nef protein acts as a connector with sorting pathways in the Golgi and at the plasma membrane. Immunity 6:67-77.
45. Marracci, G. H., W. E. Marquardt, A. Strehlow, G. P. McKeon, J. Gross, D. C. Buck, L. B. Kozell, and D. N. Bourdette. 2006. Lipoic acid downmodulates CD4 from human T lymphocytes by dissociation of p56(Lck). Biochem. Biophys. Res. Commun. 344:963-971.
46. Matlin, K. S., H. Reggio, A. Helenius, and K. Simons. 1982. Pathway of vesicular stomatitis virus entry leading to infection. J. Mol. Biol. 156:609-631.
47. Miller, M. D., M. T. Warmerdam, K. A. Page, M. B. Feinberg, and W. C. Greene. 1995. Expression of the human immunodeficiency virus type 1 (HIV-1) nef gene during HIV-1 production increases progeny particle infectivity independently of gp160 or viral entry. J. Virol. 69:579-584.
48. Parolini, I., S. Topa, M. Sorice, A. Pace, P. Ceddia, E. Montesoro, A. Pavan, M. P. Lisanti, C. Peschle, and M. Sargiacomo. 1999. Phorbol ester-induced disruption of the CD4-Lck complex occurs within a detergent-resistant microdomain of the plasma membrane. Involvement of the translocation of activated protein kinase C isoforms. J. Biol. Chem. 274:14176-14187.
49. Pelchen-Matthews, A., J. E. Armes, and M. Marsh. 1989. Internalization and recycling of CD4 transfected into HeLa and NIH3T3 cells. EMBO J. 8:3641-3649.
50. Pelchen-Matthews, A., I. Boulet, D. R. Littman, R. Fagard, and M. Marsh. 1992. The protein tyrosine kinase p56lck inhibits CD4 endocytosis by preventing entry of CD4 into coated pits. J. Cell Biol. 117:279-290.
51. Pelchen-Matthews, A., R. P. da Silva, M. J. Bijlmakers, N. Signoret, S. Gordon, and M. Marsh. 1998. Lack of p56lck expression correlates with CD4 endocytosis in primary lymphoid and myeloid cells. Eur. J. Immunol. 28:3639-3647.
52. Pelchen-Matthews, A., I. J. Parsons, and M. Marsh. 1993. Phorbol ester-induced downregulation of CD4 is a multistep process involving dissociation from p56lck, increased association with clathrin-coated pits, and altered endosomal sorting. J. Exp. Med. 178:1209-1222.
53. Pham, H. M., E. R. Arganaraz, B. Groschel, D. Trono, and J. Lama. 2004. Lentiviral vectors interfering with virus-induced CD4 down-modulation potently block human immunodeficiency virus type 1 replication in primary lymphocytes. J. Virol. 78:13072-13081.
54. 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.
55. 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 targeting signal through the binding of beta-COP in endosomes. Cell 97:63-73.
56. Pitcher, C., S. Honing, A. Fingerhut, K. Bowers, and M. Marsh. 1999. Cluster of differentiation antigen 4 (CD4) endocytosis and adaptor complex binding require activation of the CD4 endocytosis signal by serine phosphorylation. Mol. Biol. Cell 10:677-691.
57. Preusser, A., L. Briese, A. S. Baur, and D. Willbold. 2001. Direct in vitro binding of full-length human immunodeficiency virus type 1 Nef protein to CD4 cytoplasmic domain. J. Virol. 75:3960-3964.
58. Rhee, S. S., and J. W. Marsh. 1994. Human immunodeficiency virus type 1 Nef-induced down-modulation of CD4 is due to rapid internalization and degradation of surface CD4. J. Virol. 68:5156-5163.
59. Robinson, M. S. 2004. Adaptable adaptors for coated vesicles. Trends Cell Biol. 14:167-174.
60. Rose, J. J., K. Janvier, S. Chandrasekhar, R. P. Sekaly, J. S. Bonifacino, and S. Venkatesan. 2005. CD4 down-regulation by HIV-1 and simian immunodeficiency virus (SIV) Nef proteins involves both internalization and intracellular retention mechanisms. J. Biol. Chem. 280:7413-7426.
61. Salghetti, S., R. Mariani, and J. Skowronski. 1995. Human immunodeficiency virus type 1 Nef and p56lck protein-tyrosine kinase interact with a common element in CD4 cytoplasmic tail. Proc. Natl. Acad. Sci. USA 92:349-353.
62. Sanfridson, A., B. R. Cullen, and C. Doyle. 1994. The simian immunodeficiency virus Nef protein promotes degradation of CD4 in human T cells. J. Biol. Chem. 269:3917-3920.
63. Schindler, M., J. Munch, and F. Kirchhoff. 2005. Human immunodeficiency virus type 1 inhibits DNA damage-triggered apoptosis by a Nef-independent mechanism. J. Virol. 79:5489-5498.
64. Schindler, M., S. Wurfl, P. Benaroch, T. C. Greenough, R. Daniels, P. Easterbrook, M. Brenner, J. Munch, and F. Kirchhoff. 2003. Down-modulation of mature major histocompatibility complex class II and up-regulation of invariant chain cell surface expression are well-conserved functions of human and simian immunodeficiency virus nef alleles. J. Virol. 77:10548-10556.
65. Schwartz, O., V. Marechal, B. Friguet, F. Arenzana-Seisdedos, and J. M. Heard. 1998. Antiviral activity of the proteasome on incoming human immunodeficiency virus type 1. J. Virol. 72:3845-3850.
66. Shin, J., C. Doyle, Z. Yang, D. Kappes, and J. L. Strominger. 1990. Structural features of the cytoplasmic region of CD4 required for internalization. EMBO J. 9:425-434.
67. Shin, J., R. L. Dunbrack, Jr., S. Lee, and J. L. Strominger. 1991. Phosphorylation-dependent down-modulation of CD4 requires a specific structure within the cytoplasmic domain of CD4. J. Biol. Chem. 266:10658-10665.
68. Sleckman, B. P., J. Shin, V. E. Igras, T. L. Collins, J. L. Strominger, and S. J. Burakoff. 1992. Disruption of the CD4-p56lck complex is required for rapid internalization of CD4. Proc. Natl. Acad. Sci. USA 89:7566-7570.
69. 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.
70. Stewart, S. J., J. Fujimoto, and R. Levy. 1986. Human T lymphocytes and monocytes bear the same Leu-3(T4) antigen. J. Immunol. 136:3773-3778.
71. Stoddart, C. A., R. Geleziunas, S. Ferrell, V. Linquist-Stepps, M. E. Moreno, C. Bare, W. Xu, W. Yonemoto, P. A. Bresnahan, J. M. McCune, and W. C. Greene. 2003. Human immunodeficiency virus type 1 Nef-mediated downregulation of CD4 correlates with Nef enhancement of viral pathogenesis. J. Virol. 77:2124-2133.
72. Thoulouze, M. I., N. Sol-Foulon, F. Blanchet, A. Dautry-Varsat, O. Schwartz, and A. Alcover. 2006. Human immunodeficiency virus type-1 infection impairs the formation of the immunological synapse. Immunity 24:547-561.
73. Turner, J. M., M. H. Brodsky, B. A. Irving, S. D. Levin, R. M. Perlmutter, and D. R. Littman. 1990. Interaction of the unique N-terminal region of tyrosine kinase p56lck with cytoplasmic domains of CD4 and CD8 is mediated by cysteine motifs. Cell 60:755-765.
74. Wei, B. L., P. W. Denton, E. O'Neill, T. Luo, J. L. Foster, and J. V. Garcia. 2005. Inhibition of lysosome and proteasome function enhances human immunodeficiency virus type 1 infection. J. Virol. 79:5705-5712.
75. Wildum, S., M. Schindler, J. Munch, and F. Kirchhoff. 2006. Contribution of Vpu, Env, and Nef to CD4 down-modulation and resistance of human immunodeficiency virus type 1-infected T cells to superinfection. J. Virol. 80:8047-8059.