Characterization of the follicular dendritic cell reservoir of human immunodeficiency virus type 1

Journal of Virology

Volumn 82, Issue 11, 2008, Pages 5548-5561

  Keele, Brandon F ^a,d   Tazi, Loubna ^b   Gartner, Suzanne ^c   Liu, Yiling ^c   Burgon, Trever B ^a,e   Estes, Jacob D ^a,f   Thacker, Tyler C ^a,g   Crandall, Keith A ^b   McArthur, Justin C ^c   Burton, Gregory F ^a  

^a Brigham Young University   (United States)

^b BRIGHAM YOUNG UNIVERSITY   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d University of Alabama at Birmingham   (United States)

^e STANFORD UNIVERSITY   (United States)

^f NATIONAL CANCER INSTITUTE   (United States)

^g AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BLOOD SAMPLING; CD4+ T LYMPHOCYTE; COCULTURE; FOLLICULAR DENDRITIC CELL; GENETIC VARIABILITY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN TISSUE; HYPOTHESIS; MICROBIAL COLONIZATION; PHYLOGENY; POPULATION GENETIC PARAMETERS; PRIORITY JOURNAL; VIRUS DETECTION; VIRUS REPLICATION;

CD4-POSITIVE T-LYMPHOCYTES; COCULTURE TECHNIQUES; DENDRITIC CELLS, FOLLICULAR; GENOTYPE; HIV INFECTIONS; HIV-1; HUMANS; MUTATION; PHYLOGENY; VIRAL PROTEINS; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; MURINAE;

EID: 43949092756     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00124-08     Document Type: Article

References (62)

1. Armstrong, J. A. 1991. Ultrastructure and significance of the lymphoid tissue lesions in HIV infection, p. 69-82. In P. Racz, C. D. Dijkstra, and J. C. Gluckman (ed.), Accessory cells in HIV and other retroviral infections. Karger, Basel, Switzerland.
2. Biberfeld, P., A. Porwit, G. Biberfield, M. Harper, A. Bodner, and R. Gallo. 1988. Lymphadenopathy in HIV (HTLV-III LAV) infected subjects: the role of virus and follicular dendritic cells. Cancer Detect. Prev. 12:217-224.
3. Blankson, J. N., D. Persaud, and R. F. Siliciano. 2002. The challenge of viral reservoirs in HIV-1 infection. Annu. Rev. Med. 53:557-593.
4. Burton, G. F., A. Masuda, S. L. Heath, B. A. Smith, J. G. Tew, and A. K. Szakal. 1997. Follicular dendritic cells (FDC) in retroviral infection: host/pathogen perspectives. Immunol. Rev. 156:185-197.
5. Chun, T. W., L. Carruth, D. Finzi, X. Shen, J. A. DiGiuseppe, H. Taylor, M. Hermankova, K. Chadwick, J. Margolick, T. C. Quinn, Y. H. Kuo, R. Brookmeyer, M. A. Zeiger, P. Barditch-Crovo, and R. F. Siliciano. 1997. Quantification of latent tissue reservoirs and total body viral load in HIV-1 infection. Nature 387:183-188.
6. Chun, T. W., and A. S. Fauci. 1999. Latent reservoirs of HIV: obstacles to the eradication of virus. Proc. Natl. Acad. Sci. USA 96:10958-10961.
7. Chun, T. W., L. Stuyver, S. B. Mizell, L. A. Ehler, J. A. Mican, M. Baseler, A. L. Lloyd, M. A. Nowak, and A. S. Fauci. 1997. Presence of an inducible HIV-1 latent reservoir during highly active antiretroviral therapy. Proc. Natl. Acad. Sci. USA 94:13193-13197.
8. Clement, M., D. Posada, and K. A. Crandall. 2000. TCS: a computer program to estimate gene genealogies. Mol. Ecol. 9:1657-1659.
9. Collman, R. G., C. F. Perno, S. M. Crowe, M. Stevenson, and L. J. Montaner. 2003. HIV and cells of macrophage/dendritic lineage and other non-T cell reservoirs: new answers yield new questions. J. Leukoc. Biol. 74:631-634.
10. Crandall, K. A., and A. R. Templeton. 1999. Statistical approaches to detecting recombination, p. 153-176. In K. A. Crandall (ed.), The evolution of HIV. The Johns Hopkins University Press, Baltimore, MD.
11. Dumaurier, M. J., S. Gratton, S. Wain-Hobson, and R. Cheynier. 2005. The majority of human immunodeficiency virus type 1 particles present within splenic germinal centres are produced locally. J. Gen. Virol. 86:3369-3373.
12. Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783-791.
13. Felsenstein, J. 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. J. Mol. Evol. 17:368-376.
14. Finzi, D., J. Blankson, J. D. Siliciano, J. B. Margolick, K. Chadwick, T. Pierson, K. Smith, J. Lisziewicz, F. Lori, C. Flexner, T. C. Quinn, R. E. Chaisson, E. Rosenberg, B. Walker, S. Gange, J. Gallant, and R. F. Siliciano. 1999. Latent infection of CD4+ T cells provides a mechanism for lifelong persistence of HIV-1, even in patients on effective combination therapy. Nat. Med. 5:512-517.
15. Finzi, D., M. Hermankova, T. Pierson, L. M. Carruth, C. Buck, R. E. Chaisson, T. C. Quinn, K. Chadwick, J. Margolick, R. Brookmeyer, J. Gallant, M. Markowitz, D. D. Ho, D. D. Richman, and R. F. Siliciano. 1997. Identification of a reservoir for HIV-1 in patients on highly active antiretroviral therapy. Science 278:1295-1300.
16. Fox, C. H., K. Tenner-Racz, P. Racz, A. Firpo, P. A. Rizzo, and A. S. Fauci. 1991. Lymphoid germinal centers are reservoirs of human immunodeficiency virus type 1 RNA. J. Infect. Dis. 164:1051-1057.
17. García, J. A., L. E. Soto-Ramirez, G. Cocho, T. Govezensky, and M. V. Jose. 2006. HIV-1 dynamics at different time scales under antiretroviral therapy. J. Theor. Biol. 238:220-229.
18. Guindon, S., and O. Gascuel. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52:696-704.
19. Haase, A. T. 1999. Population biology of HIV-1 infection: viral and CD4+ T cell demographics and dynamics in lymphatic tissues. Annu. Rev. Immunol. 17:625-656.
20. Haase, A. T., K. Henry, M. Zupancic, G. Sedgewick, R. A. Faust, H. Melroe, W. Cavert, K. Gebhard, K. Staskus, Z.-Q. Zhang, P. Dailey, H. H. Balfour, Jr., A. Erice, and A. S. Perelson. 1996. Quantitative image analysis of HIV-1 infection in lymphoid tissue. Science 274:985-989.
21. Heath, S. L., J. G. Tew, J. G. Tew, A. K. Szakal, and G. F. Burton. 1995. Follicular dendritic cells and human immunodeficiency virus infectivity. Nature 377:740-744.
22. Helm, S. L., G. F. Burton, A. K. Szakal, and J. G. Tew. 1995. Follicular dendritic cells and the maintenance of IgE responses. Eur. J. Immunol. 25:2362-2369.
23. Huelsenbeck, J. P., B. Larget, R. E. Miller, and F. Ronquist. 2002. Potential applications and pitfalls of Bayesian inference of phytogeny. Syst. Biol. 51:673-688.
24. Kacani, L., W. M. Prodinger, G. M. Sprinzl, M. G. Schwendinger, M. Spruth, H. Stoiber, S. Dopper, S. Steinhuber, F. Steindl, and M. P. Dierich. 2000. Detachment of human immunodeficiency virus type 1 from germinal centers by blocking complement receptor type 2. J. Virol. 74:7997-8002.
25. Kay, M. S. 2003. Silent, but deadly - eliminating reservoirs of latent HIV. Trends Biotechnol. 21:420-423.
26. Klaus, G. G. B., J. H. Humphrey, A. Kunkl, and D. W. Dongworth. 1980. The follicular dendritic cell: its role in antigen presentation in the generation of immunological memory. Immunol. Rev. 53:3-28.
27. Kuhner, M. K. 2006. LAMARC 2.0: maximum likelihood and Bayesian estimation of population parameters. Bioinformatics 22:768-770.
28. Lampert, I. A., J. B. Schofield, P. Amlot, and S. Van Noorden. 1993. Protection of germinal centres from complement attack: decay-accelerating factor (DAF) is a constitutive protein on follicular dendritic cells. A study in reactive and neoplastic follicles. J. Pathol. 170:115-120.
29. Laurence, J. 1993. Reservoirs of HIV infection or carriage: monocytic, dendritic, follicular dendritic, and B cells. Ann. N. Y. Acad. Sci. 693:52-64.
30. Liu, Y., X. P. Tang, J. C. McArthur, J. Scott, and S. Gartner. 2000. Analysis of human immunodeficiency virus type 1 gp160 sequences from a patient with HIV dementia: evidence for monocyte trafficking into brain. J. Neurovirol. 6(Suppl. 1):S70-S81.
31. Mandel, T. E., R. P. Phipps, A. Abbot, and J. G. Tew. 1980. The follicular dendritic cell: long term antigen retention during immunity. Immunol. Rev. 53:29-59.
32. Meltzer, M. S., M. Nakamura, B. D. Hansen, J. A. Turpin, D. C. Kalter, and H. E. Gendelman. 1990. Macrophages as susceptible targets for HIV infection, persistent viral reservoirs in tissue, and key immunoregulatory cells that control levels of virus replication and extent of disease. AIDS Res. Hum. Retrovir. 6:967-971.
33. Müller, V., A. F. Maree, and R. J. De Boer. 2001. Release of virus from lymphoid tissue affects human immunodeficiency virus type 1 and hepatitis C virus kinetics in the blood. J. Virol. 75:2597-2603.
34. Nickle, D. C., M. A. Jensen, D. Shriner, S. J. Brodie, L. M. Frenkel, J. E. Mittler, and J. I. Mullins. 2003. Evolutionary indicators of human immunodeficiency virus type 1 reservoirs and compartments. J. Virol. 77:5540-5546.
35. Nickle, D. C., D. Shriner, J. E. Mittler, L. M. Frenkel, and J. I. Mullins. 2003. Importance and detection of virus reservoirs and compartments of HIV infection. Curr. Opin. Microbiol. 6:410-416.
36. Orenstein, J. M., C. Fox, K. Tenner-Racz, and P. Racz. 1997. Is HIV found in the cytoplasm of dendritic cells? Am. J. Pathol. 151:1173-1176.
37. Pantaleo, G., O. J. Cohen, T. Schacker, M. Vaccarezza, C. Graziosi, G. P. Rizzardi, J. Kahn, C. H. Fox, S. M. Schnittman, D. H. Schwartz, L. Corey, and A. S. Fauci. 1998. Evolutionary pattern of human immunodeficiency virus (HIV) replication and distribution in lymph nodes following primary infection: implications for antiviral therapy. Nat. Med. 4:341-345.
38. Perelson, A. S., P. Essunger, Y. Cao, M. Vesanen, A. Hurley, K. Saksela, M. Markowitz, and D. D. Ho. 1997. Decay characteristics of HIV-1-infected compartments during combination therapy. Nature 387:188-191.
39. Pierson, T., J. McArthur, and R. F. Siliciano. 2000. Reservoirs for HIV-1: mechanisms for viral persistence in the presence of antiviral immune responses and antiretroviral therapy. Annu. Rev. Immunol. 18:665-708.
40. Pomerantz, R. J. 2003. Reservoirs, sanctuaries, and residual disease: the hiding spots of HIV-1. HIV Clin. Trials 4:137-143.
41. Posada, D., and T. R. Buckley. 2004. Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst. Biol. 53:793-808.
42. Posada, D., and K. A. Crandall. 2001. Intraspecific gene genealogies: trees grafting into networks. Trends Ecol. Evol. 16:37-45.
43. Posada, D., and K. A. Crandall. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817-818.
44. Posada, D., and K. A. Crandall. 2002. The effect of recombination on the accuracy of phylogeny estimation. J. Mol. Evol. 54:396-402.
45. Racz, P., K. Tenner-Racz, and H. Schmidt. 1989. Follicular dendritic cells in HIV-induced lymphadenopathy and AIDS. APMIS Suppl. 8:16-23.
46. Robertson, D. L., B. H. Hahn, and P. M. Sharp. 1995. Recombination in AIDS viruses. J. Mol. Evol. 40:249-259.
47. Robertson, D. L., P. M. Sharp, F. E. McCutchan, and B. H. Hahn. 1995. Recombination in HIV-1. Nature 374:124-126.
48. Ronquist, F., and J. P. Huelsenbeck. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574.
49. Saksena, N. K., and S. J. Potter. 2003. Reservoirs of HIV-1 in vivo: implications for antiretroviral therapy. AIDS Rev. 5:3-18.
50. Schierup, M. H., and J. Hein. 2000. Consequences of recombination on traditional phylogenetic analysis. Genetics 156:879-891.
51. Siliciano, R. F. 1999. Latency and reservoirs for HIV-1. AIDS 13(Suppl. A):S49-S58.
52. Smith, B. A., S. Gartner, Y. Liu, A. S. Perelson, N. I. Stilianakis, B. F. Keele, T. M. Kerkering, A. Ferreira-Gonzalez, A. K. Szakal, J. G. Tew, and G. F. Burton. 2001. Persistence of infectious HIV on follicular dendritic cells. J. Immunol. 166:690-696.
53. Smith-Franklin, B. A., B. F. Keele, J. G. Tew, S. Gartner, A. K. Szakal, J. D. Estes, T. C. Thacker, and G. F. Burton. 2002. Follicular dendritic cells and the persistence of HIV infectivity: the role of antibodies and Fcγ receptors. J. Immunol. 168:2408-2414.
54. Stoiber, H., A. Clivio, and M. P. Dierich. 1997. Role of complement in HIV infection. Annu. Rev. Immunol. 15:649-674.
55. Szakal, A. K., and M. G. Hanna, Jr. 1968. The ultrastructure of antigen localization and virus-like particles in mouse spleen germinal centers. Exp. Mol. Pathol. 8:75-89.
56. Szakal, A. K., M. H. Kosco, and J. G. Tew. 1989. Microanatomy of lymphoid tissue during the induction and maintenance of humoral immune responses: structure function relationships. Annu. Rev. Immunol. 7:91-109.
57. Temin, H. M. 1991. Sex and recombination in retroviruses. Trends Genet. 7:71-74.
58. Tenner-Racz, K., and P. Racz. 1995. Follicular dendritic cells initiate and maintain infection of the germinal centers by human immunodeficiency virus. Curr. Top. Microbiol. Immunol. 201:141-159:141- 159.
59. Tew, J. G., and T. E. Mandel. 1979. Prolonged antigen half-life in the lymphoid follicles of specifically immunized mice. Immunology 37:69-76.
60. Tew, J. G., J. Wu, D. Qin, S. Helm, G. F. Burton, and A. K. Szakal. 1997. Follicular dendritic cells and presentation of antigen and costimulatory signals to B cells. Immunol. Rev. 156:39-52.
61. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882.
62. Wong, J. K., M. Hezareh, H. F. Gunthard, D. V. Havlir, C. C. Ignacio, C. A. Spina, and D. D. Richman. 1997. Recovery of replication-competent HIV, despite prolonged suppression of plasma viremia. Science 278:1291-1295.