The CCR5 and CXCR4 coreceptors are both used by human immunodeficiency virus type 1 primary isolates from subtype C

Journal of Virology

Volumn 77, Issue 7, 2003, Pages 4449-4456

  Cilliers, Tonie ^a   Nhlapo, Jabulani ^a   Coetzer, Mia ^a   Orlovic, Dragana ^b   Ketas, Thomas ^c   Olson, William C ^c   Moore, John P ^d   Trkola, Alexandra ^e   Morri, Lynn ^a  

^a NATIONAL INSTITUTE FOR COMMUNICABLE DISEASES   (South Africa)

^b Sizwe Tropical Diseases Hospital   (South Africa)

^c A Subsidiary of Lantheus Holdings   (United States)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

^e UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

1,1' [1,4 PHENYLENEBIS(METHYLENE)]BIS(1,4,8,11 TETRAAZACYCLOTETRADECANE); CHEMOKINE RECEPTOR CCR3; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CCR6; CHEMOKINE RECEPTOR CXCR4; PRO 140; RANTES; RECEPTOR BLOCKING AGENT; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ARTICLE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MALE; MONONUCLEAR CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; VIRUS ISOLATION; VIRUS REPLICATION; VIRUS TRANSMISSION;

ACQUIRED IMMUNODEFICIENCY SYNDROME; ADULT; AMINO ACID SEQUENCE; ANTI-HIV AGENTS; ANTIBODIES, MONOCLONAL; CELL LINE; FEMALE; HETEROCYCLIC COMPOUNDS; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV-1; HUMANS; MALE; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; RANTES; RECEPTORS, CCR5; RECEPTORS, CXCR4; RECEPTORS, HIV; SEQUENCE HOMOLOGY, AMINO ACID; SOUTH AFRICA; TRANSFECTION; VIRUS REPLICATION;

EID: 0037379188     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.7.4449-4456.2003     Document Type: Article

References (64)

1. Abebe, A., D. Demissie, J. Goudsmit, M. Brouwer, C. L. Kuiken, G. Pollakis, H. Schuitemaker, A. L. Fontanet, and T. F. Rinke de Wit. 1999. HIV-1 subtype C syncytium- and non-syncytium-inducing phenotypes and coreceptor usage among Ethiopian patients with AIDS. AIDS 13:1305-1311.
2. Baba, M., O. Nishimura, N. Kanzaki, M. Okamoto, H. Sawada, Y. Iizawa, M. Shiraishi, Y. Aramaki, K. Okonogi, Y. Ogawa, K. Meguro, and M. Fujino. 1999. A small-molecule, nonpeptide CCR5 antagonist with highly potent and selective anti-HIV-1 activity. Proc. Natl. Acad. Sci. USA 96:5698-5703.
3. Bjorndal, A., H. Deng, M. Jansson, J. R. Fiore, C. Colognesi, A. Karlsson, J. Albert, G. Scarlatti, D. R. Littman, and E. M. Fenyo. 1997. Coreceptor usage of primary human immunodeficiency virus type 1 isolates varies according to biological phenotype. J. Virol. 71:7478-7487.
4. Bjorndal, A., A. Sonnerborg, C. Tscherning, J. Albert, and E. M. Fenyo. 1999. Phenotypic characteristics of human immunodeficiency virus type 1 subtype C isolates of Ethiopian AIDS patients. AIDS Res. Hum. Retrovir. 15:647-653.
5. Blackard, J. T., B. Renjifo, W. Fawzi, E. Hertzmark, G. Msamanga, D. Mwakagile, D. Hunter, D. Spiegelman, N. Sharghi, C. Kagoma, and M. Essex. 2001. HIV-1 LTR subtype and perinatal transmission. Virology 287:261-265.
6. Bredell, H., C. Williamson, P. Sonnenberg, D. J. Martin, and L. Morris. 1998. Genetic characterization of HIV type 1 from migrant workers in three South African gold mines. AIDS Res. Hum. Retrovir. 14:677-684.
7. Cecilia, D., S. S. Kulkarni, S. P. Tripathy, R. R. Gangakhedkar, R. S. Paranjape, and D. A. Gadkari. 2000. Absence of coreceptor switch with disease progression in human immunodeficiency virus infections in India. Virology 271:253-258.
8. Chan, S. Y., R. F. Speck, C. Power, S. L. Gaffen, B. Chesebro, and M. A. Goldsmith. 1999. V3 recombinants indicate a central role for CCR5 as a coreceptor in tissue infection by human immunodeficiency virus type 1. J. Virol. 73:2350-2358.
9. Clerici, M., S. Butto, M. Lukwiya, M. Saresella, S. Declich, D. Trabattoni, C. Pastori, S. Piconi, C. Fracasso, M, Fabiani, P, Ferrante, G, Rizzardini, and L. Lopalco, et al. 2000. Immune activation in Africa is environmentally-driven and is associated with upregulation of CCR5. AIDS 14:2083-2092.
10. Connor, R. I., K. E. Sheridan, D. Ceradini, S. Choe, and N. R. Landau. 1997. Change in coreceptor use correlates with disease progression in HIV-1-infected individuals. J. Exp. Med. 185:621-628.
11. De Jong, J. J., A. De Ronde, W. Keulen, M. Tersmette, and J. Goudsmit. 1992. Minimal requirements for the human immunodeficiency virus type 1 V3 domain to support the syncytium-inducing phenotype: analysis by single amino acid substitution. J. Virol. 66:6777-6780.
12. De Jong, J. J., J. Goudsmit, W. Keulen, B. Klaver, W. Krone, M. Tersmette, and A. de Ronde. 1992. Human immunodeficiency virus type 1 clones chimeric for the envelope V3 domain differ in syncytium formation and replication capacity. J. Virol. 66:757-765.
13. De Wolf, F., E. Hogervorst, J. Goudsmit, E. M. Fenyo, H. Rubsamen-Waigmann, H. Holmes, B. Galvao-Castro, E. Karita, C. Wasi, S. D. Sempala, et al. 1994. Syncytium-inducing and non-syncytium-inducing capacity of human immunodeficiency virus type 1 subtypes other than B: phenotypic and genotypic characteristics. AIDS Res. Hum. Retrovir. 10:1387-1400.
14. Deng, H. K., D. Unutmaz, V. N. KewalRamani, and D. R. Littman. 1997. Expression cloning of new receptors used by simian and human immunodeficiency viruses. Nature 388:296-300.
15. Doms, R. W., and S. C. Peiper. 1997. Unwelcomed guests with master keys: how HIV uses chemokine receptors for cellular entry. Virology 235:179-190.
16. Donzella, G. A., D. Schols, S. W. Lin, J. A. Este, K. A. Nagashima, P. J. Maddon, G. P. Allaway, T. P. Sakmar, G. Henson, E. De Clereq, and J. P. Moore. 1998. AMD3100, a small molecule inhibitor of HIV-1 entry via the CXCR4 co-receptor. Nat. Med. 4:72-77.
17. Dragic, T., A. Trkola, D. A. Thompson, E. G. Cormier, F. A. Kajumo, E. Maxwell, S. W. Lin, W. Ying, S. O. Smith, T. P. Sakmar, and J. P. Moore. 2000. A binding pocket for a small molecule inhibitor of HIV-1 entry within the transmembrane helices of CCR5. Proc. Natl. Acad. Sci. USA 97:5639-5644.
18. Edinger, A. L., T. L. Hoffman, M. Sharron, B. Lee, B. O'Dowd, and R. W. Doms. 1998. Use of GPR1, GPR15, and STRL33 as coreceptors by diverse human immunodeficiency virus type 1 and simian immunodeficiency virus envelope proteins. Virology 249:367-378.
19. Elbeik, T., W. G. Alvord, R. Trichavaroj, M. de Souza, R. Dewar, A. Brown, D. Chernoff, N. L. Michael, P. Nassos, K. Hadley, and V. L. Ng. 2002. Comparative analysis of HIV-1 viral load assays on subtype quantification: Bayer Versant HIV-1 RNA 3.0 versus Roche Amplicor HIV-1 Monitor version 1.5. J. Acquir. Immune Defic. Syndr. 29:330-339.
20. Essex, M. 1999. Human immunodeficiency viruses in the developing world. Adv. Virus Res. 53:71-88.
21. Farzan, M., H. Choe, K. Martin, L. Marcon, W. Hofmann, G. Karlsson, Y. Sun, P. Barrett, N. Marchand, N. Sullivan, N. Gerard, C. Gerard, and J. Sodroski. 1997. Two orphan seven-transmembrane segment receptors which are expressed in CD4-positive cells support simian immunodeficiency virus infection. J. Exp. Med. 186:405-411.
22. Fraziano, M., G. Cappelli, M. Santucci, F. Mariani, M. Amicosante, M. Casarini, S. Giosue, A. Bisetti, and V. Colizzi. 1999. Expression of CCR5 is increased in human monocyte-derived macrophages and alveolar macrophages in the course of in vivo and in vitro Mycobacterium tuberculosis infection. AIDS Res. Hum. Retrovir. 15:869-874.
23. Gaschen, B., B. Korber, and B. Foley. 1999. Part VII. Global variation in the V3 region. Los Alamos National Laboratory, Los Alamos, N.M. http://hiv-web.lan.gov/content/hiv-db/HTML/99compendium.html.
24. Gouws, E., B. G. Williams, H. W. Sheppard, B. Enge, and S. A. Karim. 2002. High incidence of HIV-1 in South Africa using a standardized algorithm for recent HIV seroconversion. J. Acquir. Immune Defic. Syndr. 29:531-535.
25. Hendrix, C. W., C. Flexner, R. T. MacFarland, C. Giandomenico, E. J. Fuchs, E. Redpath, G. Bridger, and G. W. Henson. 2000. Pharmacokinetics and safety of AMD-3100, a novel antagonist of the CXCR-4 chemokine receptor, in human volunteers. Antimicrob. Agents Chemother. 44:1667-1673.
26. Hoffman, N. G., F. Seiller-Moiseiwitsch, J. Ahn, J. M. Walker, and R. Swanstrom. 2002. Variability in the human immunodeficiency virus type 1 gp120 Env protein linked to phenotype-associated changes in the V3 loop. J. Virol. 76:3852-3864.
27. Hoffman, T. L., and R. W. Doms. 1999. HIV-1 envelope determinants for cell tropism and chemokine receptor use. Mol. Membr. Biol. 16:57-65.
28. Ivanoff, L. A., J. W. Dubay, J. F. Morris, S. J. Roberts, L. Gutshall, E. J. Sternberg, E. Hunter, T. J. Matthews, and S. R. Petteway, Jr. 1992. V3 loop region of the HIV-1 gp120 envelope protein is essential for virus infectivity. Virology 187:423-432.
29. LaBranche, C. C., G. Galasso, J. P. Moore, D. P. Bolognesi, M. S. Hirsch, and S. M. Hammer. 2001. HIV fusion and its inhibition. Antivir. Res. 50:95-115.
30. Menu, E., J. M. Reynes, M. C. Muller-Trutwin, L. Guillemot, P. Versmisse, M. Chiron, S. An, V. Trouplin, P. Charneau, H. Fleury, F. Barre-Sinoussi, and F. F. Sainte Marie. 1999. Predominance of CCR5-dependent HIV-1 subtype E isolates in Cambodia. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 20:481-487.
31. Michael, N. L., G. Chang, L. G. Louie, J. R. Mascola, D. Dondero, D. L. Birx, and H. W. Sheppard. 1997. The role of viral phenotype and CCR-5 gene defects in HIV-1 transmission and disease progression. Nat. Med. 3:338-340.
32. Milich, L., B. H. Margolin, and R. Swanstrom. 1997. Patterns of amino acid variability in NSI-like and SI-like V3 sequences and a linked change in the CD4-binding domain of the HIV-1 Env protein. Virology 239:108-118.
33. Moore, J. P., and M. Stevenson. 2000. New targets for inhibitors of HIV-1 replication. Nat. Rev. Mol. Cell. Biol. 1:40-49.
34. Morris, L., T. Cilliers, H. Bredell, M. Phoswa, and O. Martin. 2001. CCR5 is the major coreceptor used by HIV-1 subtype C isolates from patients with active tuberculosis. AIDS Res. Human Retrovir. 17:697-701.
35. Ndung'u, T., B. Renjifo, and M. Essex. 2001. Construction and analysis of an infectious human immunodeficiency virus type 1 subtype C molecular clone. J. Virol. 75:4964-4972.
36. Olson, W. C., G. E. Rabut, K. A. Nagashima, D. N. Tran, D. J. Anselma, S. P. Monard, J. P. Segal, D. A. Thompson, F. Kajumo, Y. Guo, J. P. Moore, P. J. Maddon, and T. Dragic. 1999. Differential inhibition of human immunodeficiency virus type 1 fusion, gp120 binding, and CC-chemokine activity by monoclonal antibodies to CCR5. J. Virol. 73:4145-4155.
37. Papathanasopoulos, M., T. Cilliers, L. Morris, J. Mokili, W. Dowling, D. Birx, and F. McCutchan. 2002. Full-length genome analysis of HIV-1 subtype C utilizing CXCR4 and intersubtype recombinants isolated in South Africa. AIDS Res. Hum. Retrovir. 18:879-886.
38. Ping, L. H., J. A. Nelson, I. F. Hoffman, J. Schock, S. L. Lamers, M. Goodman, P. Vernazza, P. Kazembe, M. Maida, D. Zimba, M. M. Goodenow, J. J. Eron, Jr., S. A. Fiscus, M. S. Cohen, and R. Swanstrom. 1999. Characterization of V3 sequence heterogeneity in subtype C human immunodeficiency virus type 1 isolates from Malawi: underrepresentation of X4 variants. J. Virol. 73:6271-6281.
39. Pohlmann, S., M. Krumbiegel, and F. Kirchhoff. 1999. Coreceptor usage of BOB/GPR15 and Bonzo/STRL33 by primary isolates of human immunodeficiency virus type 1. J. Gen. Virol. 80:1241-1251.
40. Rana, S., G. Besson, D. G. Cook, J. Rucker, R. J. Smyth, Y. Yi, J. D. Turner, H. H. Guo, J. G. Du, S. C. Peiper, E. Lavi, M. Samson, F. Libert, C. Liesnard, G. Vassart, R. W. Doms, M. Parmentler, and R. G. Collman. 1997. Role of CCR5 in infection of primary macrophages and lymphocytes by macrophagetropic strains of human immunodeficiency virus: resistance to patient-derived and prototype isolates resulting from the delta CCR5 mutation. J. Virol. 71:3219-3227.
41. Richman, D. D., and S. A. Bozzette. 1994. The impact of the syncytium-inducing phenotype of human immunodeficiency virus on disease progression. J. Infect. Dis. 169:968-974.
42. Scarlatti, G., E. Tresoldi, A. Bjorndal, R. Fredriksson, C. Colognesi, H. K. Deng, M. S. Malnati, A. Plebani, A. G. Siccardi, D. R. Littman, E. M. Fenyo, and P. Lusso. 1997. In vivo evolution of HIV-1 co-receptor usage and sensitivity to chemokine-mediated suppression. Nat. Med. 3:1259-1265.
43. Schols, D., S. Struyf, J. Van Damme, J. A. Este, G. Henson, and E. De Clercq. 1997. Inhibition of T-tropic HIV strains by selective antagonization of the chemokine receptor CXCR4. J. Exp. Med. 186:1383-1388.
44. Schwarz, M., T. N. Wells, and A. E. Proudfoot. 2001. Chemokine receptors the next therapeutic target for HIV? Recept. Channels 7:417-428.
45. Sharron, M., S. Pohlmann, K. Price, E. Lolis, M. Tsang, F. Kirchhoff, R. W. Doms, and B. Lee. 2000. Expression and coreceptor activity of STRL33/Bonzo on primary peripheral blood lymphocytes. Blood 96:41-49.
46. Shimizu, N., Y. Haraguchi, Y. Takeuchi, Y. Soda, K. Kanbe, and H. Hoshino. 1999. Changes in and discrepancies between cell tropisms and coreceptor uses of human immunodeficiency virus type 1 induced by single point mutations at the V3 tip of the env protein. Virology 259:324-333.
47. Strizki, J. M., S. Xu, N. E. Wagner, L. Wojcik, J. Liu, Y. Hou, M. Endres, A. Palani, S. Shapiro, J. W. Clader, W. J. Greenlee, J. R. Tagat, S. McCombie, K. Cox, A. B. Fawzi, C. C. Chou, C. Pugliese-Sivo, L. Davies, M. E. Moreno, D. D. Ho, A. Trkola, C. A. Stoddart, J. P. Moore, G. R. Reyes, and B. M. Baroudy. 2001. SCH-C (SCH 351125), an orally bioavailable, small molecule antagonist of the chemokine receptor CCR5, is a potent inhibitor of HIV-1 infection in vitro and in vivo. Proc. Natl. Acad. Sci. USA 98:12718-12723.
48. Sutthent, R., K. Chokephaibulkit, D. Piyasujabul, N. Vanprapa, A. Roog-pisuthipong, and P. Chaisilwatana. 2002. Effect of perinatal short-course zidovudine on the clinical and virological manifestations of HIV-1 subtype E infection in infants. J. Clin. Virol. 25:47-56.
49. Sutthent, R., K. Sumrangsurp, P. Wirachsilp, P. Chaisilwattana, A. Roong-pisuthipong, P. Chaiyakul, P. Nooma, M. Houda, and P. Warachit. 2001. Diversity of HIV-1 subtype E in semen and cervicovaginal secretion. J. Hum. Virol. 4:260-268.
50. Swanson, P., V. Soriano, S. G. Devare, and J. Hackett, Jr. 2001. Comparative performance of three viral load assays on human immunodeficiency virus type 1 (HIV-1) isolates representing group M (subtypes A to G) and group O: LCx HIV RNA quantitative, AMPLICOR HIV-1 MONITOR version 1.5, and Quantiplex HIV-1 RNA version 3.0. J. Clin. Microbiol. 39:862-870.
51. Tien, P. C., T. Chiu, A. Latif, S. Ray, M. Batra, C. H. Contag, L. Zejena, M. Mbizvo, E. L. Delwart, J. I. Mullins, and D. A. Katzenstein. 1999. Primary subtype C HIV-1 infection in Harare, Zimbabwe. J. Acquit. Immune Defic. Syndr. Hum. Retrovirol. 20:147-153.
52. Trkola, A., T. J. Ketas, K. A. Nagashima, L. Zhao, T. Cilliers, L. Morris, J. P. Moore, P. J. Maddon, and W. C. Olson. 2001. Potent, broad-spectrum inhibition of human immunodeficiency virus type 1 by the CCR5 monoclonal antibody PRO 140. J. Virol. 75:579-588.
53. Trkola, A., S. E. Kuhmann, J. M. Strizki, E. Maxwell, T. Ketas, T. Morgan, P. Pugach, S. Xu, L. Wojcik, J. Tagat, A. Palani, S. Shapiro, J. W. Clader, S. McCombie, G. R. Reyes, B. M. Baroudy, and J. P. Moore. 2002. HIV-1 escape from a small molecule, CCR5-specific entry inhibitor does not involve CXCR4 use. Proc. Natl. Acad. Sci. USA 99:395-400.
54. Trkola, A., J. Matthews, C. Gordon, T. Ketas, and J. P. Moore. 1999. A cell line-based neutralization assay for primary human immunodeficiency virus type 1 isolates that use either the CCR5 or the CXCR4 coreceptor. J. Virol. 73:8966-8974.
55. Trkola, A., W. A. Paxton, S. P. Monard, J. A. Hoxie, M. A. Siani, D. A. Thompson, L. Wu, C. R. Mackay, R. Horuk, and J. P. Moore. 1998. Genetic subtype-independent inhibition of human immunodeficiency virus type 1 replication by CC and CXC chemokines. J. Virol. 72:396-404.
56. Unutmaz, D., W. Xiang, M. J. Sunshine, J. Campbell, E. Butcher, and D. R. Littman. 2000. The primate lentiviral receptor Bonzo/STRL33 is coordinately regulated with CCR5 and its expression pattern is conserved between human and mouse. J. Immunol. 165:3284-3292.
57. Utaipat, U., A. Duerr, D. L. Rudolph, C. Yang, S. T. Butera, D. Lupo, T. Pisell, A. Tangmunkongvorakul, N. Kamtorn, N. Nantachit, T. Nagachinta, V. Suriyanon, V. Robison, K. E. Nelson, N. Sittisombut, and R. B. Lal. 2002. Coreceptor utilization of HIV type 1 subtype E viral isolates from Thai men with HIV type 1-infected and uninfected wives. AIDS Res. Hum. Retrovir. 18:1-11.
58. Van Harmelen, J. H., E. Van der Ryst, A. S. Loubser, D. York, S. Madurai, S. Lyons, R. Wood, and C. Williamson. 1999. A predominantly HIV type 1 subtype C-restricted epidemic in South African urban populations. AIDS Res. Hum. Retrovir. 15:395-398.
59. Willlamson, C., S. A. Loubser, B. Brice, G. Joubert, T. Smit, R. Thomas, M. Visagie, M. Cooper, and E. van der Ryst. 2000. Allelic frequencies of host genetic variants influencing susceptibility to HIV-1 infection and disease in South African populations. AIDS 14:449-451.
60. Wu, L., G. LaRosa, N. Kassam, C. J. Gordon, H. Heath, N. Ruffing, H. Chen, J. Humblias, M. Samson, M. Parmentier, J. P. Moore, and C. R. Mackay. 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.
61. Xiao, L., D. L. Rudolph, S. M. Owen, T. J. Spira, and R. B. Lal. 1998. Adaptation to promiscuous usage of CC and CXC-chemokine coreceptors in vivo correlates with HIV-1 disease progression. AIDS 12:F137-F143.
62. Zhang, Y., B. Lou, R. B. Lal, A. Gettie, P. A. Marx, and J. P. Moore. 2000. Use of inhibitors to evaluate coreceptor usage by simian and simian/human immunodeficiency viruses and human immunodeficiency virus type 2 in primary cells. J. Virol. 74:6893-6910.
63. Zhang, Y. J., T. Dragic, Y. Cao, L. Kostrikis, D. S. Kwon, D. R. Littman, V. N. KewalRamani, and J. P. Moore. 1998. Use of coreceptors other than CCR5 by non-syncytium-inducing adult and pediatric isolates of human immunodeficiency virus type 1 is rare in vitro. J. Virol. 72:9337-9344.
64. Zhang, Y. J., and J. P. Moore. 1999. Will multiple coreceptors need to be targeted by inhibitors of human immunodeficiency virus type 1 entry? J. Virol. 73:3443-3448.