Molecular mechanism of desensitization of the chemokine receptor CCR-5: Receptor signaling and internalization are dissociable from its role as an HIV-1 co-receptor

EMBO Journal

Volumn 16, Issue 15, 1997, Pages 4606-4616

  Aramori, Ichiro ^a   Zhang, Jie ^a   Ferguson, Stephen S G ^a   Bieniasz, Paul D ^a   Cullen, Bryan R ^a   Caron, Marc G ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Chemokine receptors; Desensitization; HIV 1 co receptor; Internalization; Phosphorylation

Indexed keywords

BETA ARRESTIN; CELL RECEPTOR; CHEMOKINE RECEPTOR; CYCLIC AMP; FORSKOLIN; GUANINE NUCLEOTIDE BINDING PROTEIN; PERTUSSIS TOXIN; PHOSPHOTRANSFERASE; UNCLASSIFIED DRUG;

ARTICLE; CHEMOTAXIS; CONTROLLED STUDY; DESENSITIZATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; INTERNALIZATION; LEUKOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; T LYMPHOCYTE;

ARRESTINS; BINDING, COMPETITIVE; CELL LINE; GTP-BINDING PROTEINS; HIV INFECTIONS; HIV-1; HUMANS; KINETICS; MUTATION; PHOSPHORYLATION; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, CCR5; RECEPTORS, CYTOKINE; RECEPTORS, HIV; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TRANSFECTION;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 0030812438     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.15.4606     Document Type: Article

References (63)

1. Alkhatib, G., Combadiere, C. Broder, C.C., Feng, Y., Kennedy, P.E., Murphy, P.M. and Berger, E.A. (1996) CC CKR5: a RANTES, MIP-1α, MIP-1β receptor as a fusion cofactor for macrophage-tropic HIV-1. Science, 272, 1955-1958.
2. Arriza, J.L., Dawson, T.M., Simerly, R.B., Martin, L.J., Caron, M.G., Snyder, S.H. and Lefkowitz, R.J. (1992) The G-protein-coupled receptor kinases βARK1 and βARK2 are widely distributed at synapses in rat brain. J. Neurosci., 12, 4045-4055.
3. Atchison, R.E., Gosling, J., Monteclaro, F.S., Franci, C., Digilio, L., Charo, I.F. and Goldsmith, M.A. (1996) Multiple extracellular elements of CCR5 and HIV-1 entry: dissociation from response to chemokines. Science, 274, 1924-1926.
4. Attramadal, H., Arriza, J.L., Aoki, C., Dawson, T.M., Codina, J., Kwatra, M.M., Snyder, S.H., Caron, M.G. and Lefkowitz, R.J. (1992) β-Arrestin2, a novel member of the arrestin/β-arrestin gene family. J. Biol. Chem., 267, 17882-17890.
5. 2-adrenergic receptor sequestration. J. Biol. Chem., 269, 2790-2795.
6. Berger, J., Hauber, J., Hauber, R., Geiger, R. and Cullen, B.R. (1988) Secreted placental alkaline phosphatase: a powerful new quantitative indicator of gene expression in eukaryotic cells. Gene, 66, 1-10.
7. Bieniasz, P.D., Fridell, R.A., Aramori, I., Ferguson, S.S.G., Caron, M.G. and Cullen, B.R. (1997) HIV-1 induced cell fusion is mediated by multiple regions within both the viral envelope and the CCR-5 co-receptor. EMBO J., 16, 2599-2609.
8. Bleul, C.C, Farzan, M., Choe, H., Parolin, C., Clark-Lewis, I., Sodroski, J. and Springer, T.A. (1996) The lymphocyte chemoattractant SDF-1 is a ligand for LESTR/fusin and blocks HIV-1 entry. Nature, 382, 829-833.
9. Choe, H. et al. (1996) The β-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates. Cell, 85, 1135-1148.
10. Chuang, T.T, Sallese, M., Ambrosini, G., Parruti, G. and De Blasi, A. (1992) High expression of β-adrenergic receptor kinase in human peripheral blood leukocytes. Isoproterenol and platelet activating factor can induce kinase translocation. J. Biol. Chem., 267, 6886-6892.
11. Clapham, P.R., Blanc, D. and Weiss, R.A. (1991) Specific cell surface requirements for the infection of CD4-positive cells by human immunodeficiency virus types 1 and 2 and by simian immunodeficiency virus. Virology, 181, 703-715.
12. + T cells. Science, 270, 1811-1815.
13. Cocchi, F., DeVico, A.L., Garzino-Demo, A., Cara, A., Gallo, R.C. and Lusso, P. (1996) The V3 domain of the HIV-1 gp120 envelope glycoprotein is critical for chemokine-mediated blockade of infection. Nature Med., 2, 1244-1247.
14. Cullen, B.R. (1987) Use of eukaryotic expression technology in the functional analysis of cloned genes. Methods Enzymol., 152, 684-704.
15. Deng, H. et al. (1996) Identification of a major co-receptor for primary isolates of HIV-1. Nature, 381, 661-666.
16. Doranz, B.J., Rucker, J., Yi, Y., Smyth, R.J., Samson, M., Peiper, S.C., Parmentier, M., Collman, R.G. and Doms, R. (1996) A dual-tropic primary HIV-1 isolate that uses fusin and the β-chemokine receptors CKR-5, CKR-3, and CKR-2b as fusion cofactors. Cell, 85, 1149-1158.
17. + cells is mediated by the chemokine receptor CC-CKR-5. Nature, 381, 667-673.
18. D'Souza, M.P. and Harden, V.A. (1996) Chemokines and HIV-1 second receptors. Confluence of two fields generates optimism in AIDS research. Nature Med., 2, 1293-1300.
19. Farzan, M., Choe, H., Martin, K.A., Sun, Y., Sidelko, M., Mackay, C.R., Gerard, N.P., Sodroski, J. and Gerard, C. (1997) HIV-1 entry and macrophage inflamatory protein-1β-mediated signaling are independent functions of the chemokine receptor CCR5. J. Biol. Chem., 272, 6854-6857.
20. Feng, Y., Broder, C.C. Kennedy, P.E. and Berger, E.A. (1996) HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science, 272, 872-877.
21. 2-adrenergic receptor sequestration. Rescue of a sequestration-defective mutant receptor by βARK1. J. Biol. Chem., 270, 24782-24789.
22. Ferguson, S.S.G., Zhang, J., Barak, L.S. and Caron, M.G. (1996a) G-protein-coupled receptor kinases and arrestins: regulators of G-protein-coupled receptor sequestration. Biochem. Soc. Trans., 24, 953-959.
23. Ferguson, S.S.G., Barak, L.S., Zhang, J. and Caron, M.G. (1996b) G-protein-coupled receptor regulation: role of G-protein-coupled receptor kinases and arrestins. Can. J. Physiol. Pharmacol., 74, 1095-1011.
24. Ferguson, S.S.G., Downey, W.E., Colapietro, A.-M., Barak, L.S., Ménard, L. and Caron, M.G. (1996c) Role of β-arrestin in mediating agonist-promoted G protein-coupled receptor internalization. Science, 271, 363-366.
25. Franci, C., Gosling, J., Tsou, C.-L., Coughlin, S.R., and Charo, I.F. (1996) Phosphorylation by a G protein-coupled kinase inhibits signaling and promotes internalization of the monocyte chemoattractant protein-1 receptor. J. Immunol., 157, 5606-5612.
26. 1-adrenergic receptor. Involvement of G protein-coupled receptor kinases and cAMP-dependent protein kinase. J. Biol. Chem., 270, 17953-17961.
27. Gartner, S., Markovitz, P. Markovitz, D., Kaplan, M., Gallo, R. and Popovic, M. (1986) The role of mononuclear phagocytes in HTLV-III/LAV infection. Science, 233, 215-219.
28. Gilman, A.G. (1987) G proteins: transducers of receptor-generated signals. Ann. Rev. Biochem., 56, 615-649.
29. 2-adrenergic receptor. Nature, 383, 447-450.
30. 2-adrenergic and m2 muscarinic cholinergic receptors. J. Biol. Chem., 270, 720-731.
31. Hunyady, L., Bor, M., Baukal, A.J., Balla, T. and Catt, K.J. (1995) A conserved NPLFY sequence contributes to agonist binding and signal transduction but is not an internalization signal for the angiotensin type 1 angiotensin II receptor. J. Biol. Chem., 270, 9702-9709.
32. Hwang, S.S., Boyle, T.J., Lyerly, H.K. and Cullen, B.R. (1991) Identification of the envelope V3 loop as the primary determinant of cell tropism in HIV-1. Science, 253, 71-74.
33. Ishikawa, Y., Katsushika, S., Chen, L., Halnon, N.J., Kawabe, J. and Homcy, C.J. (1992) Isolation and characterization of a novel cardiac adenylylcyclase cDNA. J. Biol. Chem., 267, 13553-13557.
34. 2-adrenergic receptor dephosphorylation by vesicular acidification. J. Biol. Chem., 272, 5-8.
35. Lapham, C.K., Ouyang, J., Chandrasekhar, B., Nguyen, N.Y., Dimitrov, D.S. and Golding, H. (1996) Evidence for cell-surface association between fusin and the CD4-gp120 complex in human cell lines. Science, 274, 602-605.
36. 2-adrenergic receptor and rhodopsin systems. J. Biol. Chem., 267, 8558-8564.
37. + T-cell clone (PM1): failure to downregulate CD4 and to interfere with cell-line-tropic HIV-1. J. Virol., 69, 3712-3720.
38. Maddon, P.J., Dalgleish, A.G., McDougal, J.S., Clapham, P.R., Weiss, R.A. and Axel, R. (1986) The T4 gene encodes the AIDS virus receptor and is expressed in the immune system and the brain. Cell, 47, 333-348.
39. 2-adrenergic receptor facilitate sequestration. Biochemistry, 35, 4155-4160.
40. 2-adrenergic receptor sequestration: intracellular complement of βARK and βarrestin determine kinetics of internalization. Mol. Pharmacol., 51, 800-808.
41. Murphy, P.M. (1994) The molecular biology of leukocyte chemoattractant receptors. Annu. Rev. Immunol., 12, 593-633.
42. Neote, K., DiGregorio, D., Mak, J.Y., Horuk, R. and Schall, T.J. (1993) Molecular cloning, functional expression, and signaling characteristics of a C-C chemokine receptor. Cell. 72, 415-425.
43. Oberlin, E. et al. (1996) The CXC chemokine SDF-1 is the ligand for LESTR/fusin and prevents infection by T-cell-line-adapted HIV-1. Nature, 382, 833-835.
44. O'Brien, W.A., Koyanagi, Y. Namazie, A., Zhao, J.-Q., Diagne, A., Idler, K., Zack, J.A. and Chen, I.S.Y. (1990) HIV-1 tropism for mononuclear phagocytes can be determined by regions of gp120 outside the CD4-binding domain. Nature, 348, 69-73.
45. Oppermann, M., Freedman, N.J., Alexander, R.W. and Lefkowitz, R.J. (1996) Phosphoryration of the type 1A angiotensin II receptor by G protein-coupled receptor kinases and protein kinase C. J. Biol. Chem., 271, 13266-13272.
46. Oravecz, T., Pall, M. and Norcross, M.A. (1996) β-Chemokine inhibition of a monocytotropic HIV-1 infection. Interference with a postbinding fusion step. J. Immunol., 157, 1329-1332.
47. Parruti, G., Ambrosini, G., Sallese, M. and De Blasi, A. (1993) Comparative analysis of β-adrenergic receptor kinase and β-arrestm mRNA expression in human cells. J. Receptor Res., 13, 609-618.
48. Power, C.A. and Wells, T.N.C. (1996) Cloning and characterization of human chemokine receptors. Trends Pharmacol. Sci. 17, 209-213.
49. Premont, R.T., Koch, W.J., Inglese, J. and Lefkowitz, R.J. (1994) Identification, purification and characterization of GRK5, a member of the family of G protein-coupled receptor kinases. J. Biol. Chem., 269, 6832-6841.
50. Premont, R.T. Inglese, J. and Lefkowitz, R.J. (1995) Protein kinases that phosphorylate activated G protein-coupled receptors. FASEB J., 9, 175-182.
51. Raport, C.J., Gosling, J., Schweickart, V.L., Gray, P.W. and Charo, I.F. (1996) Molecular cloning and functional characterization of a novel human CC chemokine receptor (CCR5) for RANTES, MIP-1β, and MIP-1α. J. Biol. Chem., 71, 17161-17166.
52. Roth, N.S., Carapbell, P.T., Caron, M.G., Lefkowitz, R.J. and Lohse, M.J. (1991) Comparative rates of desensitization of β-adrenergic receptors by the β-adrenergic receptor kinase and the cyclic AMP-dependent protein kinase. Proc. Natl Acad. Sci. USA, 88, 6201-6204.
53. Rucker, J. et al. (1996) Regions in beta-chemokine receptors CCR5 and CCR2B that determine HIV-1 cofactor specificity. Cell, 87, 437-446.
54. 3H]cAMP in cell monolayers, cell suspensions, and tissue slices. Methods Enzymol., 195, 22-28.
55. Samson, M., Labbe, O., Mollereau, C., Vassart, G. and Parmentier, M. (1996) Molecular cloning and functional expression of a new human CC-chemokine receptor gene. Biochemistry, 35, 3362-3367.
56. Shigemoto, R., Yokota, Y., Tsuchida, K. and Nakanishi, S. (1990) Cloning and expression of a rat neuromedin K receptor cDNA. J. Biol. Chem., 265, 623-628.
57. nY motif present in the gastrin-releasing peptide receptor is not a general sequestration sequence J. Biol. Chem., 269, 21755-21762.
58. Tiberi, M., Nash, S.R., Bertrand, L., Lefkowitz, R.J. and Caron, M.G. (1996) Differential regulation of dopamine D1A receptor responsiveness by various G protein-coupled receptor kinases. J. Biol. Chem., 271, 3771-3778.
59. Trkola, A. et al. (1996) CD4-dependent, antibody-sensitive interactions between HIV-1 and its co-receptor CCR-5. Nature, 384, 184-187.
60. Ui, M. (1984) Islet-activating protein, pertussis toxin: a probe for functions of the inhibitory guanine nucleotide regulatory component of adenylate cyclase. Trends Pharmacol. Sci., 5, 277-279.
61. Wang, J.M., Sherry, B., Fivash, M.J., Kelvin, D.J. and Oppenheim, J.J. (1993) Human recombinant macrophage inflammatory protein-1α and -β and monocyte chemotactic and activating factor utilze common unique receptors on human monocytes. J. Immunol. 150, 3022-3029.
62. Wu, L. et al. (1996) CD4-induced interaction of primary HIV-1 gp120 glycoproteins with the chemokine receptor CCR-5 Nature 384 179-183.
63. Zhang, J., Ferguson, S.S.G., Barak, L.S., Ménard, L. and Caron, M.G. (1996) Dynamin and β-arrestin reveal distinct mechanisms for G protein-coupled receptor internalization. J. Biol. Chem., 271, 18302-18305.