Baseline resistance of primary human immunodeficiency virus type 1 strains to the CXCR4 inhibitor AMD3100

Journal of Virology

Volumn 82, Issue 23, 2008, Pages 11695-11704

  Harrison, Jessamina E ^a   Lynch, Jonathan B ^a   Sierra, Luz Jeannette ^a   Blackburn, Leslie A ^a   Ray, Neelanjana ^a   Collman, Ronald G ^a   Doms, Robert W ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APLAVIROC; CHEMOKINE RECEPTOR CXCR4; PLERIXAFOR;

ARTICLE; CONTROLLED STUDY; DRUG INHIBITION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SENSITIVITY ANALYSIS; VIRUS IDENTIFICATION; VIRUS RESISTANCE;

ANIMALS; CELLS, CULTURED; DRUG RESISTANCE, VIRAL; HETEROCYCLIC COMPOUNDS; HIV ENVELOPE PROTEIN GP120; HIV FUSION INHIBITORS; HIV-1; QUAIL; RECEPTORS, CCR5; RECEPTORS, CXCR4;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 56449131382     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01303-08     Document Type: Article

References (61)

1. Alexander, W. A., B. Moss, and T. R. Fuerst. 1992. Regulated expression of foreign genes in vaccinia virus under the control of bacteriophage T7 RNA polymerase and the Escherichia coli lac repressor. J. Virol. 66:2934-2942.
2. Boyer, P. L., S. G. Sarafianos, P. K. Clark, E. Arnold, and S. H. Hughes. 2006. Why do HIV-1 and HIV-2 use different pathways to develop AZT resistance? PLoS Pathog. 2:e10.
3. Briz, V., E. Poveda, and V. Soriano. 2006. HIV entry inhibitors: mechanisms of action and resistance pathways. J. Antimicrob. Chemother. 57:619-627.
4. Cho, M. W., M. K. Lee, M. C. Carney, J. F. Berson, R. W. Doms, and M. A. Martin. 1998. Identification of determinants on a dualtropic human immunodeficiency virus type 1 envelope glycoprotein that confer usage of CXCR4. J. Virol. 72:2509-2515.
5. Cho, M. W., R. Shibata, and M. A. Martin. 1996. Infection of chimpanzee peripheral blood mononuclear cells by human immunodeficiency virus type 1 requires cooperative interaction between multiple variable regions of gp120. J. Virol. 70:7318-7321.
6. De Clercq, E. 2003. The bicyclam AMD3100 story. Nat. Rev. Drug Discov. 2:581-587.
7. De Clercq, E., N. Yamamoto, R. Pauwels, J. Balzarini, M. Witvrouw, K. De Vreese, Z. Debyser, B. Rosenwirth, P. Peichl, R. Datema, et al. 1994. Highly potent and selective inhibition of human immunodeficiency virus by the bicyclam derivative JM3100. Antimicrob. Agents Chemother. 38:668-674.
8. de Vreese, K., V. Kofler-Mongold, C. Leutgeb, V. Weber, K. Vermeire, S. Schacht, J. Anne, E. de Clercq, R. Datema, and G. Werner. 1996. The molecular target of bicyclams, potent inhibitors of human immunodeficiency virus replication. J. Virol. 70:689-696.
9. De Vreese, K., I. Van Nerum, K. Vermeire, J. Anne, and E. De Clercq. 1997. Sensitivity of human immunodeficiency virus to bicyclam derivatives is influenced by the three-dimensional structure of gp120. Antimicrob. Agents Chemother. 41:2616-2620.
10. 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 Clercq, and J. P. Moore. 1998. AMD3100, a small molecule inhibitor of HIV-1 entry via the CXCR4 co-receptor. Nat. Med. 4:72-77.
11. Endres, M. J., P. R. Clapham, M. Marsh, M. Ahuja, J. D. Turner, A. McKnight, J. F. Thomas, B. Stoebenau-Haggarty, S. Choe, P. J. Vance, T. N. Wells, C. A. Power, S. S. Sutterwala, R. W. Doms, N. R. Landau, and J. A. Hoxie. 1996. CD4-independent infection by HIV-2 is mediated by fusin/CXCR4. Cell 87:745-756.
12. Este, J. A., and A. Telenti. 2007. HIV entry inhibitors. Lancet 370:81-88.
13. 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.
14. Fricker, S. P., V. Anastassov, J. Cox, M. C. Darkes, O. Grujic, S. R. Idzan, J. Labrecque, G. Lau, R. M. Mosi, K. L. Nelson, L. Qin, Z. Santucci, and R. S. Wong. 2006. Characterization of the molecular pharmacology of AMD3100: a specific antagonist of the G-protein coupled chemokine receptor, CXCR4. Biochem. Pharmacol. 72:588-596.
15. Gaschen, B., J. Taylor, K. Yusim, B. Foley, F. Gao, D. Lang, V. Novitsky, B. Haynes, B. H. Hahn, T. Bhattacharya, and B. Korber. 2002. Diversity considerations in HIV-1 vaccine selection. Science 296:2354-2360.
16. Ghaffari, G., D. L. Tuttle, D. Briggs, B. R. Burkhardt, D. Bhatt, W. A. Andiman, J. W. Sleasman, and M. M. Goodenow. 2005. Complex determinants in human immunodeficiency virus type 1 envelope gp120 mediate CXCR4-dependent infection of macrophages. J. Virol. 79:13250-13261.
17. Glushakova, S., Y. Yi, J. C. Grivel, A. Singh, D. Schols, E. De Clercq, R. G. Collman, and L. Margolis. 1999. Preferential coreceptor utilization and cytopathicity by dual-tropic HIV-1 in human lymphoid tissue ex vivo. J. Clin. Investig. 104:R7-R11.
18. Goodenow, M. M., and R. G. Collman. 2006. HIV-1 coreceptor preference is distinct from target cell tropism: a dual-parameter nomenclature to define viral phenotypes. J. Leukoc. Biol. 80:965-972.
19. Gorry, P. R., R. L. Dunfee, M. E. Mefford, K. Kunstman, T. Morgan, J. P. Moore, J. R. Mascola, K. Agopian, G. H. Holm, A. Mehle, J. Taylor, M. Farzan, H. Wang, P. Ellery, S. J. Willey, P. R. Clapham, S. M. Wolinsky, S. M. Crowe, and D. Gabuzda. 2007. Changes in the V3 region of gp120 contribute to unusually broad coreceptor usage of an HIV-1 isolate from a CCR5 Delta32 heterozygote. Virology 362:163-178.
20. Harrigan, P. R., J. S. Montaner, S. A. Wegner, W. Verbiest, V. Miller, R. Wood, and B. A. Larder. 2001. World-wide variation in HIV-1 phenotypic susceptibility in untreated individuals: biologically relevant values for resistance testing. AIDS 15:1671-1677.
21. Hartley, O., P. J. Klasse, Q. J. Sattentau, and J. P. Moore. 2005. V3: HIV's switch-hitter. AIDS Res. Hum Retrovir. 21:171-189.
22. Heil, M. L., J. M. Decker, J. N. Sfakianos, G. M. Shaw, E. Hunter, and C. A. Derdeyn. 2004. Determinants of human immunodeficiency virus type 1 baseline susceptibility to the fusion inhibitors enfuvirtide and T-649 reside outside the peptide interaction site. J. Virol. 78:7582-7589.
23. Hendrix, C. W., A. C. Collier, M. M. Lederman, D. Schols, R. B. Pollard, S. Brown, J. B. Jackson, R. W. Coombs, M. J. Glesby, C. W. Flexner, G. J. Bridger, K. Badel, R. T. MacFarland, G. W. Henson, and G. Calandra. 2004. Safety, pharmacokinetics, and antiviral activity of AMD3100, a selective CXCR4 receptor inhibitor, in HIV-1 infection. J. Acquir. Immune Defic. Syndr. 37:1253-1262.
24. Hoffman, T. L., E. B. Stephens, O. Narayan, and R. W. Doms. 1998. HIV type I envelope determinants for use of the CCR2b, CCR3, STRL33, and APJ coreceptors. Proc. Natl. Acad. Sci. USA 95:11360-11365.
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. Igarashi, T., O. K. Donau, H. Imamichi, M. J. Dumaurier, R. Sadjadpour, R. J. Plishka, A. Buckler-White, C. Buckler, A. F. Suffredini, H. C. Lane, J. P. Moore, and M. A. Martin. 2003. Macrophage-tropic simian/human immunodeficiency virus chimeras use CXCR4, not CCR5, for infections of rhesus macaque peripheral blood mononuclear cells and alveolar macrophages. J. Virol. 77:13042-13052.
27. Ketas, T. J., S. E. Kuhmann, A. Palmer, J. Zurita, W. He, S. K. Ahuja, P. J. Klasse, and J. P. Moore. 2007. Cell surface expression of CCR5 and other host factors influence the inhibition of HIV-1 infection of human lymphocytes by CCR5 ligands. Virology 364:281-290.
28. Kim, Y. B., M. K. Lee, D. P. Han, and M. W. Cho. 2001. Development of a safe and rapid neutralization assay using murine leukemia virus pseudotyped with HIV type 1 envelope glycoprotein lacking the cytoplasmic domain. AIDS Res. Hum. Retrovir. 17:1715-1724.
29. Kuhmann, S. E., P. Pugach, K. J. Kunstman, J. Taylor, R. L. Stanfield, A. Snyder, J. M. Strizki, J. Riley, B. M. Baroudy, I. A. Wilson, B. T. Korber, S. M. Wolinsky, and J. P. Moore. 2004. Genetic and phenotypic analyses of human immunodeficiency virus type 1 escape from a small-molecule CCR5 inhibitor. J. Virol. 78:2790-2807.
30. Laakso, M. M., F. H. Lee, B. Haggarty, C. Agrawal, K. M. Nolan, M. Biscone, J. Romano, A. P. Jordan, G. J. Leslie, E. G. Meissner, L. Su, J. A. Hoxie, and R. W. Doms. 2007. V3 loop truncations in HIV-1 envelope impart resistance to coreceptor inhibitors and enhanced sensitivity to neutralizing antibodies. PLoS Pathog. 3:e117.
31. Labrosse, B., J. L. Labernardiere, E. Dam, V. Trouplin, K. Skrabal, F. Clavel, and F. Mammano. 2003. Baseline susceptibility of primary human immunodeficiency virus type 1 to entry inhibitors. J. Virol. 77:1610-1613.
32. 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.
33. Lee, B., M. Sharron, L. J. Montaner, D. Weissman, and R. W. Doms. 1999. Quantification of CD4, CCR5, and CXCR4 levels on lymphocyte subsets, dendritic cells, and differentially conditioned monocyte-derived macrophages. Proc. Natl. Acad. Sci. USA 96:5215-5220.
34. Lin, G., A. Bertolotti-Ciarlet, B. Haggarty, J. Romano, K. M. Nolan, G. J. Leslie, A. P. Jordan, C. C. Huang, P. D. Kwong, R. W. Doms, and J. A. Hoxie. 2007. Replication-competent variants of human immunodeficiency virus type 2 lacking the V3 loop exhibit resistance to chemokine receptor antagonists. J. Virol. 81:9956-9966.
35. Maeda, K., H. Nakata, Y. Koh, T. Miyakawa, H. Ogata, Y. Takaoka, S. Shibayama, K. Sagawa, D. Fukushima, J. Moravek, Y. Koyanagi, and H. Mitsuya. 2004. Spirodiketopiperazine-based CCR5 inhibitor which preserves CC-chemokine/CCR5 interactions and exerts potent activity against R5 human immunodeficiency virus type 1 in vitro. J. Virol. 78:8654-8662.
36. Malkevitch, N., D. H. McDermott, Y. Yi, J. C. Grivel, D. Schols, E. De Clercq, P. M. Murphy, S. Glushakova, R. G. Collman, and L. Margolis. 2001. Coreceptor choice and T cell depletion by R5, X4, and R5X4 HIV-1 variants in CCR5-deficient (CCR5delta32) and normal human lymphoid tissue. Virology. 281:239-247.
37. Marozsan, A. J., S. E. Kuhmann, T. Morgan, C. Herrera, E. Rivera-Troche, S. Xu, B. M. Baroudy, J. Strizki, and J. P. Moore. 2005. Generation and properties of a human immunodeficiency virus type 1 isolate resistant to the small molecule CCR5 inhibitor, SCH-417690 (SCH-D). Virology 338:182-199.
38. Meissner, E. G., K. M. Duus, F. Gao, X. F. Yu, and L. Su. 2004. Characterization of a thymus-tropic HIV-1 isolate from a rapid progressor: role of the envelope. Virology 328:74-88.
39. Melikyan, G. B., R. M. Markosyan, H. Hemmati, M. K. Delmedico, D. M. Lambert, and F. S. Cohen. 2000. Evidence that the transition of HIV-1 gp41 into a six-helix bundle, not the bundle configuration, induces membrane fusion. J. Cell Biol. 151:413-423.
40. Molla, A., M. Korneyeva, Q. Gao, S. Vasavanonda, P. J. Schipper, H. M. Mo, M. Markowitz, T. Chernyavskiy, P. Niu, N. Lyons, A. Hsu, G. R. Granneman, D. D. Ho, C. A. Boucher, J. M. Leonard, D. W. Norbeck, and D. J. Kempf. 1996. Ordered accumulation of mutations in HIV protease confers resistance to ritonavir. Nat. Med. 2:760-766.
41. Moore, J. P., S. G. Kitchen, P. Pugach, and J. A. Zack. 2004. The CCR5 and CXCR4 coreceptors - central to understanding the transmission and pathogenesis of human immunodeficiency virus type 1 infection. AIDS Res. Hum. Retrovir. 20:111-126.
42. Nolan, K. M., A. P. Jordan, and J. A. Hoxie. 2008. Effects of partial deletions within the human immunodeficiency virus type 1 V3 loop on coreceptor tropism and sensitivity to entry inhibitors. J. Virol. 82:664-673.
43. Platt, E. J., J. P. Durnin, and D. Kabat. 2005. Kinetic factors control efficiencies of cell entry, efficacies of entry inhibitors, and mechanisms of adaptation of human immunodeficiency virus. J. Virol. 79:4347-4356.
44. Pugach, P., A. J. Marozsan, T. J. Ketas, E. L. Landes, J. P. Moore, and S. E. Kuhmann. 2007. HIV-1 clones resistant to a small molecule CCR5 inhibitor use the inhibitor-bound form of CCR5 for entry. Virology 361:212-228.
45. 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. Parmentier, and R. G. Collman. 1997. Role of CCR5 in infection of primary macrophages and lymphocytes by macrophage-tropic strains of human immunodeficiency virus: resistance to patient-derived and prototype isolates resulting from the delta ccr5 mutation. J. Virol. 71:3219-3227.
46. Ray, N., and R. W. Doms. 2006. HIV-1 coreceptors and their inhibitors. Curr. Top. Microbiol. Immunol. 303:97-120.
47. Ray, N., J. E. Harrison, L. A. Blackburn, J. N. Martin, S. G. Deeks, and R. W. Doms. 2007. Clinical resistance to enfuvirtide does not affect susceptibility of human immunodeficiency virus type 1 to other classes of entry inhibitors. J. Virol. 81:3240-3250.
48. Reeves, J. D., S. A. Gallo, N. Ahmad, J. L. Miamidian, P. E. Harvey, M. Sharron, S. Pohlmann, J. N. Sfakianos, C. A. Derdeyn, R. Blumenthal, E. Hunter, and R. W. Doms. 2002. Sensitivity of HIV-1 to entry inhibitors correlates with envelope/coreceptor affinity, receptor density, and fusion kinetics. Proc. Natl. Acad. Sci. USA 99:16249-16254.
49. Reynes, J., P. Portales, M. Segondy, V. Baillat, P. Andre, O. Avinens, M. C. Picot, J. Clot, J. F. Eliaou, and P. Corbeau. 2001. CD4 T cell surface CCR5 density as a host factor in HIV-1 disease progression. AIDS 15:1627-1634.
50. Rucker, J., B. J. Doranz, A. L. Edinger, D. Long, J. F. Berson, and R. W. Doms. 1997. Cell-cell fusion assay to study role of chemokine receptors in human immunodeficiency virus type 1 entry. Methods Enzymol. 288:118-133.
51. Schols, D., J. A. Este, G. Henson, and E. De Clercq. 1997. Bicyclams, a class of potent anti-HIV agents, are targeted at the HIV coreceptor fusin/CXCR-4. Antivir. Res. 35:147-156.
52. 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.
53. Shibata, R., M. D. Hoggan, C. Broscius, G. Englund, T. S. Theodore, A. Buckler-White, L. O. Arthur, Z. Israel, A. Schultz, H. C. Lane, et al. 1995. Isolation and characterization of a syncytium-inducing, macrophage/T-cell line-tropic human immunodeficiency virus type 1 isolate that readily infects chimpanzee cells in vitro and in vivo. J. Virol. 69:4453-4462.
54. Shieh, J. T., J. Martin, G. Baltuch, M. H. Malim, and F. Gonzalez-Scarano. 2000. Determinants of syncytium formation in microglia by human immunodeficiency virus type 1: role of the V1/V2 domains. J. Virol. 74:693-701.
55. Smyth, R. J., Y. Yi, A. Singh, and R. G. Collman. 1998. Determinants of entry cofactor utilization and tropism in a dualtropic human immunodeficiency virus type 1 primary isolate. J. Virol. 72:4478-4484.
56. Trkola, A., T. Dragic, J. Arthos, J. M. Binley, W. C. Olson, G. P. Allaway, C. Cheng-Mayer, J. Robinson, P. J. Maddon, and J. P. Moore. 1996. CD4-dependent, antibody-sensitive interactions between HIV-1 and its co-receptor CCR-5. Nature 384:184-187.
57. Westby, M., C. Smith-Burchnell, J. Mori, M. Lewis, M. Mosley, M. Stockdale, P. Dorr, G. Ciaramella, and M. Perros. 2007. Reduced maximal inhibition in phenotypic susceptibility assays indicates that viral strains resistant to the CCR5 antagonist maraviroc utilize inhibitor-bound receptor for entry. J. Virol. 81:2359-2371.
58. Wu, L., W. A. Paxton, N. Kassam, N. Ruffing, J. B. Rottman, N. Sullivan, H. Choe, J. Sodroski, W. Newman, R. A. Koup, and C. R. Mackay. 1997. CCR5 levels and expression pattern correlate with infectability by macrophagetropic HIV-1, in vitro. J. Exp. Med. 185:1681-1691.
59. Yi, Y., S. N. Isaacs, D. A. Williams, I. Frank, D. Schols, E. De Clercq, D. L. Kolson, and R. G. Collman. 1999. Role of CXCR4 in cell-cell fusion and infection of monocyte-derived macrophages by primary human immunodeficiency virus type 1 (HIV-1) strains: two distinct mechanisms of HIV-1 dual tropism. J. Virol. 73:7117-7125.
60. Yi, Y., C. Lee, Q. H. Liu, B. D. Freedman, and R. G. Collman. 2004. Chemokine receptor utilization and macrophage signaling by human immunodeficiency virus type 1 gp120: implications for neuropathogenesis. J. Neurovirol 10(Suppl. 1):91-96.
61. Yi, Y., F. Shaheen, and R. G. Collman. 2005. Preferential use of CXCR4 by R5X4 human immunodeficiency virus type 1 isolates for infection of primary lymphocytes. J. Virol. 79:1480-1486.