Tyrosine sulfation of the amino terminus of CCR5 facilitates HIV-1 entry

Cell

Volumn 96, Issue 5, 1999, Pages 667-676

  Farzan, Michael ^a   Mirzabekov, Tajib ^a   Kolchinsky, Peter ^a   Wyatt, Richard ^a   Cayabyab, Mark ^a   Gerard, Norma P ^a,c   Gerard, Craig ^a,c   Sodroski, Joseph ^a,b   Choe, Hyeryun ^a,c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR; CHEMOKINE RECEPTOR CCR5; GUANINE NUCLEOTIDE BINDING PROTEIN; VIRUS RECEPTOR;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; NONHUMAN; PRIORITY JOURNAL; RECEPTOR INTRINSIC ACTIVITY; SIMIAN IMMUNODEFICIENCY VIRUS; SULFATION; VIRUS INFECTIVITY;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; PRIMATES; RNA VIRUSES; SIMIAE; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 0033525590     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)80577-2     Document Type: Article

References (56)

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. Bundgaard, J.R., Vuust, J., and Rehfeld, J.F. (1997). New consensus features for tyrosine O-sulfation determined by mutational analysis. J. Biol. Chem. 272, 21700-21705.
3. Carlsson, S.R., Sasaki, H., and Fukuda, M. (1986). Structural variations of O-linked oligosaccharides present in leukosialin isolated from erythroid, myeloid, and T-lymphoid cell lines. J. Biol. Chem. 261, 12787-12795.
4. Choe, H., Farzan, M., Sun, Y., Sullivan, N., Rollins, B., Ponath, P.D., Wu, L., Mackay, C.R., LaRosa, G., Newman, W., et al. (1996). The beta-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates. Cell 85, 1135-1148.
5. Choe, H., Farzan, M., Konkel, M., Martin, K., Sun, Y., Marcon, L., Cayabyab, M., Berman, M., Dorf, M.E., Gerard, N., Gerard, C., and Sodroski, J. (1998a). The orphan seven-transmembrane receptor apj supports the entry of primary T-cell-line-tropic and dualtropic human immunodeficiency virus type 1. J. Virol. 72, 6113-6118.
6. Choe, H., Martin, K.A., Farzan, M., Sodroski, J., Gerard, N.P., and Gerard, C. (1998b). Structural interactions between chemokine receptors, gp120 Env and CD4. Semin. Immunol. 10, 249-257.
7. - T cells. Science 270, 1811-1815.
8. Connor, R.I., Sheridan, K.E., Ceradini, D., Choe, S., and Landau, N.R. (1997). Change in coreceptor use correlates with disease progression in HIV-1-infected individuals. J. Exp. Med. 185, 621-628.
9. Deng, H., Liu, R., Ellmeier, W., Choe, S., Unutmaz, D., Burkhart, M., Di Marzio, P., Marmon, S., Sutton, R.E., Hill, C.M., et al. (1996). Identification of a major co-receptor for primary isolates of HIV-1. Nature 381, 661-666.
10. Deng, H.K., Unutmaz, D., KewalRamani, V.N., and Littman, D.R. (1997). Expression cloning of new receptors used by simian and human immunodeficiency viruses. Nature 388, 296-300.
11. Doms, R.W., and Peiper, S.C. (1997). Unwelcomed guests with master keys: how HIV uses chemokine receptors for cellular entry. Virology 235, 179-190.
12. Doranz, B.J., Rucker, J., Yi, Y., Smyth, R.J., Samson, M., Peiper, S.C., Parmentier, M., Collman, R.G., and Doms, R.W. (1996). A dualtropic primary HIV-1 isolate that uses fusin and the beta-chemokine receptors CKR-5, CKR-3, and CKR-2b as fusion cofactors. Cell 85, 1149-1158.
13. + cells is mediated by the chemokine receptor CC- CKR-5. Nature 381, 667-673.
14. Dragic, T., Trkola, A., Lin, S.W., Nagashima, K.A., Kajumo, F., Zhao, L., Olson, W.C., Wu, L., Mackay, C.R., Allaway, G.P., et al. (1998). Amino-terminal substitutions in the CCR5 coreceptor impair gp120 binding and human immunodeficiency virus type 1 entry. J. Virol. 72, 279-285.
15. Este, J.A., Schols, D., De Vreese, K., Van Laethem, K., Vandamme, A.M., Desmyter, J., and De Clercq, E. (1997). Development of resistance of human immunodeficiency virus type 1 to dextran sulfate associated with the emergence of specific mutations in the envelope gp120 glycoprotein. Mol. Pharmacol. 52, 98-104.
16. Farzan, M., Choe, H., Martin, K., Marcon, L., Hofmann, W., Karlsson, G., Sun, Y., Barrett, P., Marchand, N., Sullivan, N., et al. (1997a). Two orphan seven-transmembrane segment receptors which are expresed in CD4-positive cells support simian immunodeficiency virus infection. J. Exp. Med. 186, 405-411.
17. Farzan, M., Choe, H., Martin, K.A., Sun, Y., Sidelko, M., Mackay, C.R., Gerard, N.P., Sodroski, J., and Gerard, C. (1997b). HIV-1 entry and macrophage inflammatory protein-1beta-mediated signaling are independent functions of the chemokine receptor CCR5. J. Biol. Chem. 272, 6854-6857.
18. Farzan, M., Choe, H., Vaca, L., Martin, K., Sun, Y., Desjardins, E., Ruffing, N., Wu, L., Wyatt, R., Gerard, N., Gerard, C., and Sodroski, J. (1998). A tyrosine-rich region in the N terminus of CCR5 is important for human immunodeficiency virus type 1 entry and mediates an association between gp120 and CCR5. J. Virol. 72, 1160-1164.
19. eng, 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.
20. Fukuda, M., Carlsson, S.R., Klock, J.C., and Dell, A. (1986). Structures of O-linked oligosaccharides isolated from normal granulocytes, chronic myelogenous leukemia cells, and acute myelogenous leukemia cells. J. Biol. Chem. 261, 12796-12806.
21. Gerard, C., and Gerard, N.P. (1994). The pro-inflammatory seven-transmembrane segment receptors of the leukocyte. Curr. Opin. Immunol. 6, 140-145.
22. Gong, W., Howard, O.M., Turpin, J.A., Grimm, M.C., Ueda, H., Gray, P.W., Raport, C.J., Oppenheim, J.J., and Wang, J.M. (1998). Monocyte chemotactic protein-2 activates CCR5 and blocks CD4/CCR5-mediated HIV-1 entry/replication. J. Biol. Chem. 273, 4289-4292.
23. Horuk, R., Hesselgesser, J., Zhou, Y., Faulds, D., Halks-Miller, M., Harvey, S., Taub, D., Samson, M., Parmentier, M., Rucker, J., Doranz, B.J., and Doms, R.W. (1998). The CC chemokine I-309 inhibits CCR8-dependent infection by diverse HIV-1 strains. J. Biol. Chem. 273, 386-391.
24. Huttner, W.B. (1984). Determination and occurrence of tyrosine O-sulfate in proteins. Methods Enzymol. 107, 200-223.
25. Huttner, W.B. (1988). Tyrosine sulfation and the secretory pathway. Annu. Rev. Physiol. 50, 363-376.
26. 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.
27. Kwong, P.D., Wyatt, R., Robinson, J., Sweet, R.W., Sodroski, J., and Hendrickson, W.A. (1998). Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human. Nature 393, 648-659.
28. Liao, F., Alkhatib, G., Peden, K.W., Sharma, G., Berger, E.A., and Farber, J.M. (1997). STRL33, a novel chemokine receptor-like protein, functions as a fusion cofactorfor both macrophage-tropic and T cell line-tropic HIV-1. J. Exp. Med. 185, 2015-2023.
29. Littman, D.R. (1998). Chemokine receptors: keys to AIDS pathogenesis? Cell 93, 677-680.
30. Luster, A.D., Greenberg, S.M., and Leder, P. (1995). The IP-10 chemokine binds to a specific cell surface heparan sulfate site shared with platelet factor 4 and inhibits endothelial cell proliferation. J. Exp. Med. 182, 219-231.
31. Mintz, K.P., Fisher, L.W., Grzesik, W.J., Hascall, V.C., and Midura, R.J. (1994). Chlorate-induced inhibition of tyrosine sulfation on bone sialoprotein synthesized by a rat osteoblast-like cell line (UMR 106-01 BSP). J. Biol. Chem. 269, 4845-4852.
32. Mondor, I., Ugolini, S., and Sattentau, Q.J. (1998). Human immunodeficiency virus type 1 attachment to HeLa CD4 cells is CD4 independent and gp120 dependent and requires cell surface heparans. J. Virol. 72, 3623-3634.
33. Monteclaro, F.S., and Charo, I.F. (1996). The amino-terminal extracellular domain of the MCP-1 receptor, but not the RANTES MIP-1alpha receptor, confers chemokine selectivity. Evidence for a two-step mechanism for MCP-1 receptor activation. J. Biol. Chem. 271, 19084-19092.
34. Oravecz, T., Pall, M., Wang, J., Roderiquez, G., Ditto, M., and Norcross, M.A. (1997). Regulation of anti-HIV-1 activity of RANTES by heparan sulfate proteoglycans. J. Immunol. 159, 4587-4592.
35. Pleskoff, O., Treboute, C., Brelot, A., Heveker, N., Seman, M., and Alizon, M. (1997). Identification of a chemokine receptor encoded by human cytomegalovirus as a cofactor for HIV-1 entry. Science 276, 1874-1878.
36. Pouyani, T., and Seed, B. (1995). PSGL-1 recognition of P-selectin is controlled by a tyrosine sulfation consensus at the PSGL-1 amino terminus. Cell 83, 333-343.
37. Premack, B.A., and Schall, T.J. (1996). Chemokine receptors: gateways to inflammation and infection. Nat. Med. 2, 1174-1178.
38. Rabut, G.E., Konner, J.A., Kajumo, F., Moore, J.P., and Dragic, T. (1998). Alanine substitutions of polar and nonpolar residues in the amino-terminal domain of CCR5 differently impair entry of macrophage and dualtropic isolates of human immunodeficiency virus type 1. J. Virol. 72, 3464-3468.
39. 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-1beta, and MIP-1alpha. J. Biol. Chem. 271, 17161-17166.
40. Rizzuto, C.D., Wyatt, R., Hernandez-Ramos, N., Sun, Y., Kwong, P.D., Hendrickson, W.A., and Sodroski, J. (1998). A conserved HIV gp120 glycoprotein structure involved in chemokine receptor binding. Science 280, 1949-1953.
41. Roderiquez, G., Oravecz, T., Yanagishita, M., Bou-Habib, D.C., Mostowski, H., and Norcross, M.A. (1995). Mediation of human immunodeficiency virus type 1 binding by interaction of cell surface heparan sulfate proteoglycans with the V3 region of envelope gp120-gp41. J. Virol. 69, 2233-2239.
42. Rosenquist, G.L, and Nicholas, H.B., Jr. (1993). Analysis of sequence requirements for protein tyrosine sulfation. Protein Sci. 2, 215-222.
43. Ross, T.M., Bieniasz, P.D., and Cullen, B.R. (1998). Multiple residues contribute to the inability of murine CCR-5 to function as a coreceptor for macrophage-tropic human immunodefiency virus type 1 isololates. J. Virol. 72, 1918-1924.
44. Rucker, J., Samson, M., Doranz, B.J., Libert, F., Berson, J.F., Yi, Y., Smyth, R.J., Collman, R.G., Broder, C.C., Vassart, G., Doms, R.W., and Parmentier, M. (1996). Regions in beta-chemokine receptors CCR5 and CCR2b that determine HIV-1 cofactor specificity. Cell 87, 437-446.
45. Rucker, J., Edinger, A.L., Sharron, M., Samson, M., Lee, B., Berson, J., Yi, Y., Margulies, B., Collman, R.G., Doranz, B.J., Parmentier, M., and Doms, R.W. (1997). Utilization of chemokine receptors, orphan receptors, and herpesvirus-encoded receptors by diverse human and simian immunodeficiency viruses. J. Virol. 71, 8999-9007.
46. 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.
47. Samson, M., LaRosa, G., Libert, F., Paindavoine, P., Detheux, M., Vassart, G., and Parmentier, M. (1997). The second extracellular loop of CCR5 is the major determinant of ligand specificity. J. Biol. Chem. 272, 24934-24941.
48. Tanaka, Y., Adams, D.H., Hubscher, S., Hirano, H., Siebenlist, U., and Shaw, S. (1993). T-cell adhesion induced by proteoglycanimmobilized cytokine MIP-1 beta. Nature 361, 79-82.
49. Trkola, A., Dragic, T., Arthos, J., Binley, J.M., Olson, W.C., Allaway, G.P., Cheng-Mayer, C., Robinson, J., Maddon, P.J., and Moore, J.P. (1996). CD4-dependent, antibody-sensitive interactions between HIV-1 and its co-receptor CCR-5. Nature 384, 184-187.
50. Wang, W.K., Dudek, T., Zhao, Y.J., Brumblay, H.G., Essex, M., and Lee, T.H. (1998). CCR5 coreceptor utilization involves a highly conserved arginine residue of HIV type 1 gp120. Proc. Natl. Acad. Sci. USA 95, 5740-5745.
51. Webb, L.M., Ehrengruber, M.U., Clark-Lewis, I., Baggiolini, M., and Rot, A. (1993). Binding to heparan sulfate or heparin enhances neutrophil responses to interleukin 8. Proc. Natl. Acad. Sci. USA 90, 7158-7162.
52. Wu, L., Gerard, N.P., Wyatt, R., Choe, H., Paralin, C., Ruffing, N., Borsetti, A., Cardosa, A.A., Desjardin, E., Newman, W., Gerard, C., and Sodroski, J. (1996). CD4-induced interactions of primary HIV-1 gp120 glycoproteins with the chemokine receptor CCR-5. Nature 184, 179-183.
53. Wu, L., LaRosa, G., Kassam, N., Gordon, C.J., Heath, H., Ruffing, N., Chen, H., Humblias, J., Samson, M., Parmentier, M., Moore, J.P., and Mackay, C.R. (1997). Interaction of chemokine receptor CCR5 with its ligands: multiple domains for HIV-1 gp120 binding and a single domain for chemokine binding. J. Exp. Med. 186, 1373-1381.
54. Wyatt, R., Kwong, P.D., Desjardins, E., Sweet, R.W., Robinson, J., Hendrickson, W.A., and Sodroski, J.G. (1998). The antigenic structure of the HIV gp120 envelope glycoprotein. Nature 393, 705-711.
55. Yang, D.W., Ohta, Y., Yamaguchi, S., Tsukada, Y., Haraguchi, Y., Hoshino, H., Amagai, H., and Kobayashi, I. (1996). Sulfated colominic acid: an antiviral agent that inhibits the human immunodeficiency virus type 1 in vitro. Antiviral Res. 31, 95-104.
56. Zhang, J.L., Choe, H., Dezube, B.J., Farzan, M., Sharma, P.L., Zhou, X.C., Chen, L.B., Ono, M., Gillies, S., Wu, Y., Sodroski, J.G., and Crumpacker, C.S. (1998). The bis-azo compound FP-21399 inhibits HIV-1 replication by preventing viral entry. Virology 244, 530-541.