Naïve and memory cell turnover as drivers of CCR5-to-CXCR4 tropism switch in human immunodeficiency virus type 1: Implications for therapy

Journal of Virology

Volumn 80, Issue 2, 2006, Pages 802-809

  Ribeiro, Ruy M ^a   Hazenberg, Mette D ^b,c   Perelson, Alan S ^a   Davenport, Miles P ^d  

^a LOS ALAMOS NATIONAL LABORATORY   (United States)

^b SANQUIN RESEARCH   (Netherlands)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIRETROVIRUS AGENT; CHEMOKINE RECEPTOR; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CCR5 ANTAGONIST; CHEMOKINE RECEPTOR CXCR4;

ARTICLE; CD4 LYMPHOCYTE COUNT; CELL DIVISION; DISEASE COURSE; DRUG MECHANISM; GENE EXPRESSION; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MEMORY T LYMPHOCYTE; PHENOTYPE; PRIORITY JOURNAL; T LYMPHOCYTE; VIROGENESIS; VIRUS LOAD; VIRUS STRAIN;

ANTI-HIV AGENTS; CD4 LYMPHOCYTE COUNT; CD4-POSITIVE T-LYMPHOCYTES; CELL DIVISION; HIV INFECTIONS; HIV-1; HUMANS; IMMUNOLOGIC MEMORY; MODELS, IMMUNOLOGICAL; RECEPTORS, CCR5; RECEPTORS, CXCR4; TIME FACTORS; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 30344464412     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.80.2.802-809.2006     Document Type: Article

References (62)

1. Arron, S. T., R. M. Ribeiro, A. Gettie, R. Bohm, J. Blanchard, J. Yu, A. S. Perelson, D. D. Ho, and L. Zhang. 2005. Impact of thymectomy on the peripheral T cell pool in rhesus macaques before and after infection with simian immunodeficiency virus. Eur. J. Immunol. 35:46-55.
2. Benito, J. M., J. M. Zabay, J. Gil, M. Bermejo, A. Escudero, E. Sanchez, and E. Fernandez-Cruz. 1997. Quantitative alterations of the functionally distinct subsets of CD4 and CD8 T lymphocytes in asymptomatic HIV infection: changes in the expression of CD45RO, CD45RA, CD11b, CD38, HLA-DR, and CD25 antigens. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 14:128-135.
3. Berger, E. A., P. M. Murphy, and J. M. Farber. 1999. Chemokine receptors as HIV-1 coreceptors: roles in viral entry, tropism, and disease. Annu. Rev. Immunol. 17:657-700.
4. + T cell decline. Proc. Natl. Acad. Sci. USA 97:1269-1274.
5. Bleul, C. C., L. J. Wu, J. A. Hoxie, T. A. Springer, and C. R. Mackay. 1997. The HIV coreceptors CXCR4 and CCR5 are differentially expressed and regulated on human T lymphocytes. Proc. Natl. Acad. Sci. USA 94:1925- 1930.
6. - resting T cells cannot be infected de novo with HIV-1. Proc. Natl. Acad. Sci. USA 94:1361-1365.
7. Cohen Stuart, J. W., M. D. Hazebergh, D. Hamann, S. A. Otto, J. C. Borleffs, F. Miedema, C. A. Boucber, and R. J. de Boer. 2000. The dominant source of CD4+ and CD8+ T-cell activation in HIV infection is antigenic stimulation. J. Acquir. Immune Defic. Syndr. 25:203-211.
8. 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.
9. Davenport, M., J. Zaunders, M. Hazenberg, H. Schuitemaker, and R. van Rij. 2002. Cell turnover and cell tropism in HIV-1 infection. Trends Microbiol. 10:275-278.
10. De Boer, R. J., H. Mohri, D. D. Ho, and A. S. Perelson. 2003. Turnover rates of B cells, T cells, and NK cells in simian immunodeficiency virus-infected and uninfected rhesus macaques. J. Immunol. 170:2479-2487.
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. Delforge, M. L., C. Liesnard, L. Debaisieux, M. Tchetcheroff, C. M. Farber, and J. P. Van Vooren. 1995. In vivo inhibition of syncytium-inducing variants of HIV in patients treated with didanosine. AIDS 9:89-90.
13. Delobel, P., K. Sandres-Saune, M. Cazabat, C. Pasquier, B. Marchou, P. Massip, and J. Izopet. 2005. R5 to X4 switch of the predominant HIV-1 population in cellular reservoirs during effective highly active antiretroviral therapy. J. Acquir. Immune Defic. Syndr. 38:382-392.
14. de Roda Husman, A. M., H. Blaak, M. Brouwer, and H. Schuitemaker. 1999. CC chemokine receptor 5 cell-surface expression in relation to CC chemokine receptor 5 genotype and the clinical course of HIV-1 infection. J. Immunol. 163:4597-4603.
15. de Roda Husman, A. M., R. P. van Rij, H. Blaak, S. Broersen, and H. Schuitemaker. 1999. Adaptation to promiscuous usage of chemokine receptors is not a prerequisite for human immunodeficiency virus type 1 disease progression. J. Infect. Dis. 180:1106-1115.
16. Dummer, W., E. Ernst, E. LeRoy, D. S. Lee, and C. D. Surh. 2001. Autologous regulation of naive T cell homeostasis within the T cell compartment. J. Immunol. 166:2460-2468.
17. + T cells residing within human lymphoid tissues. Immunity 15:671-682.
18. Ercoli, L., L. Sarmali, E. Nicastri, G. Giannini, C. Galluzzo, S. Vella, and M. Andreoni. 1997. HIV phenotype switching during antiretroviral therapy: emergence of saquinavir-resistant strains with less cytopathogenicity. AIDS 11:1211-1217.
19. Farber, J. M., and E. A. Berger. 2002. HIV's response to a CCR5 inhibitor: I'd rather tighten than switch! Proc. Natl. Acad. Sci. USA 99:1749-1751.
20. Fry, T. J., E. Connick, J. Falloon, M. M. Lederman, D. J. Liewehr, J. Spritzler, S. M. Steinberg, L. V. Wood, R. Yarchoan, J. Zuckerman, A. Landay, and C. L. Mackall. 2001. A potential role for interleukin-7 in T-cell homeostasis. Blood 97:2983-2990.
21. Goldrath, A. W., L. Y. Bogatzki, and M. J. Bevan. 2000. Naive T cells transiently acquire a memory-like phenotype during homeostasis-driven proliferation. J. Exp. Med. 192:557-564.
22. + T cells in ex vivo-infected human lymphoid tissue. J. Virol. 74:8077-8084.
23. Hazenberg, M. D., J. W. Stuart, S. A. Otto, J. C. Borleffs, C. A. Boucher, R. J. de Boer, F. Miedema, and D. Hamann. 2000. T-cell division in human immunodeficiency virus (HIV)-1 infection is mainly due to immune activation: a longitudinal analysis in patients before and during highly active antiretroviral therapy (HAART). Blood 95:249-255.
24. Koot, M., I. P. Keet, A. H. Vos, R. E. de Goede, M. T. Roos, R. A. Coutinho, F. Miedema, P. T. Schellekens, and M. Tersmette. 1993. Prognostic value of HIV-1 syncytium-inducing phenotype for rate of CD4+ cell depletion and progression to AIDS. Ann. Intern. Med. 118:681-688.
25. Koot, M., A. B. Vantwout, N. A. Kootstra, R. E. Y. Degoede, M. Tersmette, and H. Schuitemaker. 1996. Relation between changes in cellular load, evolution of viral phenotype, and the clonal composition of virus populations in the course of human immunodeficiency virus type 1 infection. J. Infect. Dis. 173:349-354.
26. Lavie, A., I. Schlichting, I. R. Vetter, M. Konrad, J. Reinstein, and R. S. Goody. 1997. The bottleneck in AZT activation. Nat. Med. 3:922-924.
27. Li, Q., L. Duan, J. D. Estes, Z. M. Ma, T. Rourke, Y. Wang, C. Reilly, J. Carlis, C. J. Miller, and A. T. Haase. 2005. Peak SIV replication in resting memory CD4+ T cells depletes gut lamina propria CD4+ T cells. Nature 434:1148-1152.
28. Llano, A., J. Barretina, A. Gutierrez, J. Blanco, C. Cabrera, B. Clotet, and J. A. Este. 2001. Interleukin-7 in plasma correlates with CD4 T-cell depletion and may be associated with emergence of syncytium-inducing variants in human immunodeficiency virus type 1-positive individuals. J. Virol. 75:10319-10325.
29. Maas, J. J., S. J. Gange, H. Schuitemaker, R. A. Coutinho, R. van Leeuwen, and J. B. Margolick. 2000. Strong association between failure of T cell homeostasis and the syncytium-inducing phenotype among HIV-1-infected men in the Amsterdam Cohort Study. AIDS 14:1155-1161.
30. Margolick, J. B., A. Munoz, A. D. Donnenberg, L. P. Park, N. Galai, J. V. Giorgi, M. R. O'Gorman, and J. Ferbas. 1995. Failure of T-cell homeostasis preceding AIDS in HIV-1 infection. The Multicenter AIDS Cohort Study. Nat. Med. 1:674-680.
31. Mattapallil, J. J., D. C. Douek, B. Hill, Y. Nishimura, M. Martin, and M. Roederer. 2005. Massive infection and loss of memory CD4+ T cells in multiple tissues during acute SIV infection. Nature 434:1093-1097.
32. McCune, J. M., M. B. Hanley, D. Cesar, R. Halvorsen, R. Hoh, D. Schmidt, E. Wieder, S. Deeks, S. Siler, R. Neese, and M. Hellerstein. 2000. Factors influencing T-cell turnover in HIV-1-seropositive patients. J. Clin. Investig. 105:R1-R8.
33. McLean, A. R., and C. A. Michie. 1995. In vivo estimates of division and death rates of human T lymphocytes. Proc. Natl. Acad. Sci. USA 92:3707-3711.
34. Mohri, H., S. Bonhoeffer, S. Monard, A. S. Perelson, and D. D. Ho. 1998. Rapid turnover of T lymphocytes in SIV-infected rhesus macaques. Science 279:1223-1227.
35. Mosier, D. E., G. R. Picchio, R. J. Gulizia, R. Sabbe, P. Poignard, L. Picard, R. E. Offord, D. A. Thompson, and J. Wilken. 1999. Highly potent RANTES analogues either prevent CCR5-using human immunodeficiency virus type 1 infection in vivo or rapidly select for CXCR4-using variants. J. Virol. 73: 3544-3550.
36. Murali-Krishna, K., and R. Ahmed. 2000. Naive T cells masquerading as memory cells. J. Immunol. 165:1733-1737.
37. Ostrowski, M. A., S. J. Justement, A. Catanzaro, C. A. Hallahan, L. A. Ehler. S. B. Mizell, P. N. Kumar, J. A. Mican, T. W. Chun, and A. S. Fauci. 1998. Expression of chemokine receptors CXCR4 and CCR5 in HIV-1-infected and uninfected individuals. J. Immunol. 161:3195-3201.
38. Pastore, C., A. Ramos, and D. E. Mosier. 2004. Intrinsic obstacles to human immunodeficiency virus type 1 coreceptor switching. J. Virol. 78:7565-7574.
39. Perelson, A. S. 2002. Modelling viral and immune system dynamics. Nat. Rev. Immunol. 2:28-36.
40. Philpott, S., B. Weiser, K. Anastos, C. M. R. Kitchen, E. Robison, W. A. Meyer, H. S. Sacks, U. Mathur-Wagh, C. Brunner, and H. Burger. 2001. Preferential suppression of CXCR4-specific strains of HIV-1 by antiviral therapy. J. Clin. Investig. 107:431-438.
41. Regoes, R., and S. Bonhoeffer. 2005. The HIV coreceptor switch: a population dynamical perspective. Trends Microbiol. 13:269-277.
42. Regoes, R., and S. Bonhoeffer. 2002. HIV coreceptor usage and drug treatment. J. Theor. Biol. 217:443-457.
43. Ribeiro, R. M., H. Mohri, D. D. Ho, and A. S. Perelson. 2002. In vivo dynamics of T cell activation, proliferation, and death in HIV-1 infection: why are CD4+ but not CD8+ T cells depleted? Proc. Natl. Acad. Sci. USA 99:15572-15577.
44. Roederer, M., J. G. Dubs, M. T. Anderson, P. A. Raju, and L. A. Herzenberg. 1995. CD8 naive T cell counts decrease progressively in HIV-infected adults. J. Clin. Investig. 95:2061-2066.
45. + T lymphocyte turnover in simian immunodeficiency virus-infected macaques. Proc. Natl. Acad. Sci. USA 95:6388-6393.
46. Sachsenberg, N., A. S. Perelson, S. Yerly, G. A. Schockmel, D. Leduc, B. Hirschel, and L. Perrin. 1998. Turnover of CD4+ and CD8+ T lymphocytes in HIV-1 infection as measured by Ki-67 antigen. J. Exp. Med. 187:1295-1303.
47. Schacker, T., S. Little, E. Connick, K. Gebhard, Z. Q. Zhang, J. Krieger, J. Pryor, D. Havlir, J. K. Wong, R. T. Schooley, D. Richman, L. Corey, and A. T. Haase. 2001. Productive infection of T cells in lymphoid tissues during primary and early human immunodeficiency virus infection. J. Infect. Dis. 183:555-562.
48. Skrabal, K., V. Trouplin, B. Labrosse, V. Obry, F. Damond, A. J. Hance, F. Clavel, and F. Mammano. 2003. Impact of antiretroviral treatment on the tropism of HIV-1 plasma virus populations. AIDS 17:809-814.
49. Spijkerman, I., F. de Wolf, M. Langendem, H. Schuitemaker, and R. Coutinho. 1998. Emergence of syncytium-inducing human immunodeficiency virus type 1 variants coincides with a transient increase in viral RNA level and is an independent predictor for progression to AIDS. J. Infect. Dis. 178:397-403.
50. Stevenson, M., T. L. Stanwick, M. P. Dempsey, and C. A. Lamonica. 1990. HIV-1 replication is controlled at the level of T cell activation and proviral integration. EMBO J. 9:1551-1560.
51. Stoddart, C., S. Xu, J. Wojcik, J. L. Riley, and J. M. Strizki. 2003. Presented at the 10th Conference on Retroviruses and Opportunistic Infections, Boston, Mass.
52. Swingler, S., B. Brichacek, J. M. Jacque, C. Ulich, J. Zhou, and M. Stevenson. 2003. HIV-1 Nef intersects the macrophage CD40L signalling pathway to promote resting-cell infection. Nature 424:213-219.
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. van der Ende, M. E., M. Schutten, B. Raschdorff, G. Grosschupff, P. Racz, A. Osterhaus, and K. Tenner-Racz. 1999. CD4 T cells remain the major source of HIV-1 during end stage disease. AIDS 13:1015-1019.
55. van Rij, R. P., M. D. Hazenberg, B. H. van Benthem, S. A. Otto, M. Prins, F. Miedema, and H. Schuitemaker. 2003. Early viral load and CD4+ T cell count, but not percentage of CCR5+ or CXCR4+ CD4+ T cells, are associated with R5-to-X4 HIV type 1 virus evolution. AIDS Res. Hum. Retrovir. 19:389-398.
56. van Rij, R. P., J. A. Visser, R. M. van Praag, R. Rientsma, J. M. Prins, J. M. Lange, and H. Schuitemaker. 2002. Both RS and X4 human immunodeficiency virus type 1 variants persist during prolonged therapy with five antiretroviral drugs. J. Virol. 76:3054-3058.
57. van't Wout, A. B., N. A. Kootstra, G. A. Mulder-Kampinga, N. Albrecht-van Lent, H. J. Scherpbier, J. Veenstra, K. Boer, R. A. Coutinho, F. Miedema, and H. Schuitemaker. 1994. Macrophage-tropic variants initiate human immunodeficiency virus type 1 infection after sexual, parenteral, and vertical transmission. J. Clin. Investig. 94:2060-2067.
58. van't Wout, A. B., H. Blaak, L. J. Ran, M. Brouwer, C. Kuiken, and H. Schuitemaker. 1998. Evolution of syncytium-inducing and non-syncytium-inducing biological virus clones in relation to replication kinetics during the course of human immunodeficiency virus type 1 infection. J. Virol. 72:5099-5107.
59. Westby, M., J. Whitcomb, W. Huang, I. R. James, S. Abel, C. J. Petropoulos, M. Perros, and E. van der Ryst. 2003. Presented at the 11th Conference on Retroviruses and Opportunistic Infections, San Francisco, Calif..
60. Wolinsky, S. M., R. S. Veazey, K. J. Kunstman, P. J. Klasse, J. Dufour, A. J. Marozsan, M. S. Springer, and J. P. Moore. 2004. Effect of a CCR5 inhibitor on viral loads in macaques dual-infected with R5 and X4 primate immunodeficiency viruses. Virology 328:19-29.
61. Zack, J. A., S. J. Arrigo, S. R. Weitsman, A. S. Go, A. Haislip, and I. S. Y. Chen. 1990. HIV-1 entry into quiescent primary lymphocytes: molecular analysis reveals a labile latent early viral structure. Cell 61:213-222.
62. Zhang, Z., T. Schuler, M. Zupancic, S. Wietgrefe, K. A. Staskus, K. A. Reimann, T. A. Reinhart, M. Rogan, W. Cavert, C. J. Miller, R. S. Veazey, D. Notermans, S. Little, S. A. Danner, D. D. Richman, D. Havlir, J. Wong, H. L. Jordan, T. W. Schacker, P. Racz, K. Tenner-Racz, N. L. Letvin, S. Wolinsky, and A. T. Haase. 1999. Sexual transmission and propagation of SIV and HIV in resting and activated CD4+ T cells. Science 286:1353-1357.