Heterosexual transmission of human immunodeficiency virus type 1 subtype C: Macrophage tropism, alternative coreceptor use, and the molecular anatomy of CCR5 utilization

Journal of Virology

Volumn 83, Issue 16, 2009, Pages 8208-8220

  Isaacman Beck, Jesse ^a   Hermann, Emilia A ^a   Yi, Yanjie ^a   Ratcliffe, Sarah J ^a   Mulenga, Joseph ^c   Allen, Susan ^b   Hunter, Eric ^b   Derdeyn, Cynthia A ^b   Collman, Ronald G ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b EMORY UNIVERSITY   (United States)

^c Zambia Blood Transfusion Service   (Zambia)

Author keywords

[No Author keywords available]

Indexed keywords

APELIN RECEPTOR; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CCR2B; CHEMOKINE RECEPTOR CCR3; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CCR8; CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR6; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 15; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN;

ARTICLE; CD4+ T LYMPHOCYTE; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE TRANSMISSION; FEMALE; HETEROSEXUALITY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; INFECTION; MACROPHAGE; MALE; PRIORITY JOURNAL; SENSITIVITY ANALYSIS; SEXUAL TRANSMISSION; TARGET CELL;

CELL LINE; CELLS, CULTURED; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; FEMALE; HETEROSEXUALITY; HIV INFECTIONS; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; MACROPHAGES; MALE; PROSPECTIVE STUDIES; RECEPTORS, CCR5; RECEPTORS, HIV; ZAMBIA;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 67749118313     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00296-09     Document Type: Article

References (56)

1. Abebe, A., D. Demissie, J. Goudsmit, M. Brouwer, C. L. Kuiken, G. Pollakis, H. Schuitemaker, A. L. Fontanet, and T. F. R. 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. Allen, S., J. Meinzen-Derr, M. Kautzman, I. Zulu, S. Trask, U. Fideli, R. Musonda, F. Kasolo, F. Gao, and A. Haworth. 2003. Sexual behavior of HIV discordant couples after HIV counseling and testing. AIDS 17:733-740.
3. Baribaud, F., T. G. Edwards, M. Sharron, A. Brelot, N. Heveker, K. Price, F. Mortari, M. Alizon, M. Tsang, and R. W. Doms. 2001. Antigenically distinct conformations of CXCR4. J. Virol. 75:8957-8967.
4. Bieniasz, P. D., R. A. Fridell, I. Aramori, S. S. G. Ferguson, M. G. Caron, and B. R. Cullen. 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.
5. Björndal, 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.
6. Björndal, 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.
7. Blanpain, C., J. M. Vanderwinden, J. Cihak, V. Wittamer, E. Le Poul, H. Issafras, M. Stangassinger, G. Vassart, S. Marullo, D. Schlondorff, M. Parmentier, and M. Mack. 2002. Multiple active states and oligomerization of CCR5 revealed by functional properties of monoclonal antibodies. Mol. Biol. Cell 13:723-737.
8. Chohan, B., D. Lang, M. Sagar, B. Korber, L. Lavreys, B. Richardson, and J. Overbaugh. 2005. Selection for human immunodeficiency virus type 1 envelope glycosylation variants with shorter V1-V2 loop sequences occurs during transmission of certain genetic subtypes and may impact viral RNA levels. J. Virol. 79:6528-6531.
9. Cilliers, T., J. Nhlapo, M. Coetzer, D. Orlovic, T. Ketas, W. C. Olson, J. P. Moore, A. Trkola, and L. Morris. 2003. The CCR5 and CXCR4 coreceptors are both used by human immunodeficiency virus type 1 primary isolates from subtype C. J. Virol. 77:4449-4456.
10. Cilliers, T., S. Willey, W. M. Sullivan, T. Patience, P. Pugach, M. Coetzer, M. Papathanasopoulos, J. P. Moore, A. Trkola, P. Clapham, and L. Morris. 2005. Use of alternate coreceptors on primary cells by two HIV-1 isolates. Virology 339:136-144.
11. Coetzer, M., T. Cilliers, L. H. Ping, R. Swanstrom, and L. Morris. 2006. Genetic characteristics of the V3 region associated with CXCR4 usage in HIV-1 subtype C isolates. Virology 356:95-105.
12. Connor, R. I., B. K. Chen, S. Choe, and N. R. Landau. 1995. Vpr is required for efficient replication of human immunodeficiency virus type-1 in mononuclear phagocytes. Virology 206:935-944.
13. 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.
14. + T lymphocytes are preferentially recruited to the ileum in Crohn's disease. Gut 53:1287-1294.
15. Derdeyn, C. A., J. M. Decker, F. Bibollet-Ruche, J. L. Mokili, M. Muldoon, S. A. Denham, M. L. Heil, F. Kasolo, R. Musonda, B. H. Hahn, G. M. Shaw, B. T. Korber, S. Allen, and E. Hunter. 2004. Envelope-constrained neutralization-sensitive HIV-1 after heterosexual transmission. Science 303:2019-2022.
16. Dragic, T. 2001. An overview of the determinants of CCR5 and CXCR4 co-receptor function. J. Gen. Virol. 82:1807-1814.
17. Farzan, M., T. Mirzabekov, P. Kolchinsky, R. Wyatt, M. Cayabyab, N. P. Gerard, C. Gerard, J. Sodroski, and H. Choe. 1999. Tyrosine sulfation of the amino terminus of CCR5 facilitates HIV-1 entry. Cell 96:667-676.
18. Gorry, P. R., J. Sterjovski, M. Churchill, K. Witlox, L. Gray, A. Cunningham, and S. Wesselingh. 2004. The role of viral coreceptors and enhanced macrophage tropism in human immunodeficiency virus type 1 disease progression. Sex. Health 1:23-34.
19. Gottlieb, G. S., L. Heath, D. C. Nickle, K. G. Wong, S. E. Leach, B. Jacobs, S. Gezahegne, A. B. van 't Wout, L. P. Jacobson, J. B. Margolick, and J. I. Mullins. 2008. HIV-1 variation before seroconversion in men who have sex with men: analysis of acute/early HIV infection in the multicenter AIDS cohort study. J. Infect. Dis. 197:1011-1015.
20. Gray, L., J. Sterjovski, M. Churchill, P. Ellery, N. Nasr, S. R. Lewin, S. M. Crowe, S. L. Wesselingh, A. L. Cunningham, and P. R. Gorry. 2005. Uncoupling coreceptor usage of human immunodeficiency virus type 1 (HIV-1) from macrophage tropism reveals biological properties of CCR5-restricted HIV-1 isolates from patients with acquired immunodeficiency syndrome. Virology 337:384-398.
21. Guthrie, B. L., G. de Bruyn, and C. Farquhar. 2007. HIV-1-discordant couples in sub-Saharan Africa: explanations and implications for high rates of discordancy. Curr. HIV Res. 5:416-429.
22. Haaland, R. E., P. A. Hawkins, J. Salazar-Gonzalez, A. Johnson, A. Tichacek, E. Karita, O. Manigart, J. Mulenga, B. F. Keele, G. M. Shaw, B. H. Hahn, S. A. Allen, C. A. Derdeyn, and E. Hunter. 2009. Inflammatory genital infections mitigate a severe genetic bottleneck in heterosexual transmission of subtype A and C HIV-1. PLoS Pathog. 5:e1000274.
23. Hu, Q., K. B. Napier, J. O. Trent, Z. Wang, S. Taylor, G. E. Griffin, S. C. Peiper, and R. J. Shattock. 2005. Restricted variable residues in the Cterminal segment of HIV-1 V3 loop regulate the molecular anatomy of CCR5 utilization. J. Mol. Biol. 350:699-712.
24. Hu, Q. X., J. O. Trent, G. D. Tomaras, Z. X. Wang, J. L. Murray, S. M. Conolly, J. M. Navenot, A. P. Barry, M. L. Greenberg, and S. C. Peiper. 2000. Identification of ENV determinants in V3 that influence the molecular anatomy of CCR5 utilization. J. Mol. Biol. 302:359-375.
25. Huang, C. C., S. N. Lam, P. Acharya, M. Tang, S. H. Xiang, S. S. Hussan, R. L. Stanfield, J. Robinson, J. Sodroski, I. A. Wilson, R. Wyatt, C. A. Bewley, and P. D. Kwong. 2007. Structures of the CCR5 N terminus and of a tyrosine-sulfated antibody with HIV-1 gp120 and CD4. Science 317:1930-1934.
26. Keele, B. F., E. E. Giorgi, J. F. Salazar-Gonzalez, J. M. Decker, K. T. Pham, M. G. Salazar, C. Sun, T. Grayson, S. Wang, H. Li, X. Wei, C. Jiang, J. L. Kirchherr, F. Gao, J. A. Anderson, L. H. Ping, R. Swanstrom, G. D. Tomaras, W. A. Blattner, P. A. Goepfert, J. M. Kilby, M. S. Saag, E. L. Delwart, M. P. Busch, M. S. Cohen, D. C. Montefiori, B. F. Haynes, B. Gaschen, G. S. Athreya, H. Y. Lee, N. Wood, C. Seoighe, A. S. Perelson, T. Bhattacharya, B. T. Korber, B. H. Hahn, and G. M. Shaw. 2008. Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc. Natl. Acad. Sci. USA 105:7552-7557.
27. Labrosse, B., C. Treboute, A. Brelot, and M. Alizon. 2001. Cooperation of the V1/V2 and V3 domains of human immunodeficiency virus type 1 gp120 for interaction with the CXCR4 receptor. J. Virol. 75:5457-5464.
28. Learn, G. H., D. Muthui, S. J. Brodie, T. Zhu, K. Diem, J. I. Mullins, and L. Corey. 2002. Virus population homogenization following acute human immunodeficiency virus type 1 infection. J. Virol. 76:11953-11959.
29. Lee, B., M. Sharron, C. Blanpain, B. J. Doranz, J. Vakili, P. Setoh, E. Berg, G. Liu, H. R. Guy, S. R. Durell, M. Parmentier, C. N. Chang, K. Price, M. Tsang, and R. W. Doms. 1999. Epitope mapping of CCR5 reveals multiple conformational states and distinct but overlapping structures involved in chemokine and coreceptor function. J. Biol. Chem. 274:9617-9626.
30. Lee, S., H. L. Tiffany, L. King, P. M. Murphy, H. Golding, and M. B. Zaitseva. 2000. CCR8 on human thymocytes functions as a human immunodeficiency virus type 1 coreceptor. J. Virol. 74:6946-6952.
31. Li, M., J. F. Salazar-Gonzalez, C. A. Derdeyn, L. Morris, C. Williamson, J. E. Robinson, J. M. Decker, Y. Li, M. G. Salazar, V. R. Polonis, K. Mlisana, S. A. Karim, K. Hong, K. M. Greene, M. Bilska, J. Zhou, S. Allen, E. Chomba, J. Mulenga, C. Vwalika, F. Gao, M. Zhang, B. T. Korber, E. Hunter, B. H. Hahn, and D. C. Montefiori. 2006. Genetic and neutralization properties of subtype C human immunodeficiency virus type 1 molecular env clones from acute and early heterosexually acquired infections in Southern Africa. J. Virol. 80:11776-11790.
32. Liu, R., W. A. Paxton, S. Choe, D. Ceradini, S. R. Martin, R. Horuk, M. E. MacDonald, H. Stuhlmann, R. A. Koup, and N. R. Landau. 1996. Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply-exposed individuals to HIV-1 infection. Cell 86:367-377.
33. Liu, Y., M. E. Curlin, K. Diem, H. Zhao, A. K. Ghosh, H. Zhu, A. S. Woodward, J. Maenza, C. E. Stevens, J. Stekler, A. C. Collier, I. Genowati, W. Deng, R. Zioni, L. Corey, T. Zhu, and J. I. Mullins. 2008. Env length and N-linked glycosylation following transmission of human immunodeficiency virus type 1 subtype B viruses. Virology 374:229-233.
34. Long, E. M., H. L. Martin, Jr., J. K. Kreiss, S. M. Rainwater, L. Lavreys, D. J. Jackson, J. Rakwar, K. Mandaliya, and J. Overbaugh. 2000. Gender differences in HIV-1 diversity at time of infection. Nat. Med. 6:71-75.
35. Margolis, L., and R. Shattock. 2006. Selective transmission of CCR5-utilizing HIV-1: the "gatekeeper" problem resolved? Nat. Rev. Microbiol. 4:312-317.
36. McClure, C. P., P. J. Tighe, R. A. Robins, D. Bansal, C. A. Bowman, M. Kingston, and J. K. Ball. 2005. HIV coreceptor and chemokine ligand gene expression in the male urethra and female cervix. AIDS 19:1257-1265.
37. + cells. Nat. Med. 8:150-156.
38. Morris, L., T. Cilliers, H. Bredell, M. Phoswa, and D. J. Martin. 2001. CCR5 is the major coreceptor used by HIV-1 subtype C isolates from patients with active tuberculosis. AIDS Res. Hum. Retrovir. 17:697-701.
39. Ndung'u, T., E. Sepako, M. F. McLane, F. Chand, K. Bedi, S. Gaseitsiwe, F. Doualla-Bell, T. Peter, I. Thior, S. M. Moyo, P. B. Gilbert, V. A. Novitsky, and M. Essex. 2006. HIV-1 subtype C in vitro growth and coreceptor utilization. Virology 347:247-260.
40. O'Doherty, U., W. J. Swiggard, and M. H. Malim. 2000. Human immunodeficiency virus type 1 spinoculation enhances infection through virus binding. J. Virol. 74:10074-10080.
41. Patterson, B. K., A. Landay, J. Andersson, C. Brown, H. Behbahani, D. Jiyamapa, Z. Burki, D. Stanislawski, M. A. Czerniewski, and P. Garcia. 1998. Repertoire of chemokine receptor expression in the female genital tract: implications for human immunodeficiency virus transmission. Am. J. Pathol. 153:481-490.
42. Peters, P. J., W. M. Sullivan, M. J. Duenas-Decamp, J. Bhattacharya, C. Ankghuambom, R. Brown, K. Luzuriaga, J. Bell, P. Simmonds, J. Ball, and P. R. Clapham. 2006. Non-macrophage-tropic human immunodeficiency virus type 1 R5 envelopes predominate in blood, lymph nodes, and semen: implications for transmission and pathogenesis. J. Virol. 80:6324-6332.
43. Reece, J. C., A. J. Handley, E. J. Anstee, W. A. Morrison, S. M. Crowe, and P. U. Cameron. 1998. HIV-1 selection by epidermal dendritic cells during transmission across human skin. J. Exp. Med. 187:1623-1631.
44. Ritola, K., C. D. Pilcher, S. A. Fiscus, N. G. Hoffman, J. A. Nelson, K. M. Kitrinos, C. B. Hicks, J. J. Eron, Jr., and R. Swanstrom. 2004. Multiple V1/V2 env variants are frequently present during primary infection with human immunodeficiency virus type 1. J. Virol. 78:11208-11218.
45. Rizzuto, C. D., R. Wyatt, N. Hernández-Ramos, Y. Sun, P. D. Kwong, W. A. Hendrickson, and J. Sodroski. 1998. A conserved HIV gp120 glycoprotein structure involved in chemokine receptor binding. Science 280:1949-1953.
46. Roos, M. T. L., J. M. A. Lange, R. E. Y. de Goede, R. A. Coutinho, P. T. A. Schellekens, F. Miedema, and M. Tersmette. 1992. Viral phenotype and immune response in primary human immunodeficiency virus type 1 infection. J. Infect. Dis. 165:427-432.
47. Rucker, J., A. L. Edinger, M. Sharron, M. Samson, B. Lee, J. F. Berson, Y. Yi, B. Margulies, R. G. Collman, B. J. Doranz, M. Parmentier, and R. W. Doms. 1997. Utilization of chemokine receptors, orphan receptors, and herpesvirus-encoded receptors by diverse human and simian immunodeficiency viruses. J. Virol. 71:8999-9007.
48. Rucker, J., M. Samson, B. J. Doranz, F. Libert, J. F. Berson, Y. Yi, R. J. Smyth, R. G. Collman, C. C. Broder, G. Vassart, R. W. Doms, and M. Parmentier. 1996. Regions in beta-chemokine receptors CCR5 and CCR2b that determine HIV-1 cofactor specificity. Cell 87:437-446.
49. Samson, M., F. Libert, B. J. Doranz, J. Rucker, C. Liesnard, C. M. Farber, S. Saragosti, C. Lapoumeroulie, J. Cogniaux, C. Forceille, G. Muyldermans, C. Verhofstede, G. Bortonboy, M. Georges, T. Imai, S. Rana, Y. Yi, R. J. Smyth, R. G. Collman, R. W. Doms, G. Vassart, and M. Parmentier. 1996. Resistance to HIV-1 infection of Caucasian individuals bearing mutant alleles of the CCR5 chemokine receptor gene. Nature 382:722-725.
50. 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.
51. Shimizu, N., Y. Soda, K. Kanbe, H. Y. Liu, A. Jinno, T. Kitamura, and H. Hoshino. 1999. An orphan G protein-coupled receptor, GPR1, acts as a coreceptor to allow replication of human immunodeficiency virus types 1 and 2 in brain-derived cells. J. Virol. 73:5231-5239.
52. Singh, A., Y. Yi, S. N. Isaacs, D. L. Kolson, and R. G. Collman. 2001. Concordant utilization of macrophage entry coreceptors by related variants within an HIV type 1 primary isolate viral swarm. AIDS Res. Hum. Retrovir. 17:957-963.
53. Soler, D., T. R. Chapman, L. R. Poisson, L. Wang, J. Cote-Sierra, M. Ryan, A. McDonald, S. Badola, E. Fedyk, A. J. Coyle, M. R. Hodge, and R. Kolbeck. 2006. CCR8 expression identifies CD4 memory T cells enriched for FOXP3+ regulatory and Th2 effector lymphocytes. J. Immunol. 177:6940- 6951.
54. Tokizawa, S., N. Shimizu, H. Y. Liu, D. Y. Fang, Y. Haraguchi, T. Oite, and H. Hoshino. 2000. Infection of mesangial cells with HIV and SIV: identifi-cation of GPR1 as a coreceptor. Kidney Int. 58:607-617.
55. Zhu, T., H. Mo, N. Wang, D. S. Nam, Y. Cao, R. A. Koup, and D. D. Ho. 1993. Genotypic and phenotypic characterization of HIV-1 patients with primary infection. Science 261:1179-1181.
56. Zhu, T. F., N. Wang, A. Carr, D. S. Nam, R. Moor-Jankowski, D. A. Cooper, and D. D. Ho. 1996. Genetic characterization of human immunodeficiency virus type 1 in blood and genital secretions: evidence for viral compartmentalization and selection during sexual transmission. J. Virol. 70:3098-3107.