Role for CD21 in the establishment of an extracellular HIV reservoir in lymphoid tissues

Journal of Immunology

Volumn 178, Issue 11, 2007, Pages 6968-6974

  Ho, Jason ^a   Moir, Susan ^a   Kulik, Liudmila ^b   Malaspina, Angela ^a   Donoghue, Eileen T ^a   Miller, Natalie J ^a   Wang, Wei ^a   Chun, Tae Wook ^a   Fauci, Anthony S ^a   Holers, V Michael ^b  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIGEN; COMPLEMENT COMPONENT C3D RECEPTOR; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; LIGAND; MONOCLONAL ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY SPECIFICITY; ARTICLE; CELL LYSATE; CONTROLLED STUDY; FOLLICULAR DENDRITIC CELL; HUMAN IMMUNODEFICIENCY VIRUS; IN VITRO STUDY; KNOCKOUT MOUSE; LYMPHOID TISSUE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; VIRION;

EID: 34249806714     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.178.11.6968     Document Type: Article

References (52)

1. Pantaleo, G., C. Graziosi, J. F. Demarest, L. Butini, M. Montroni, C. H. Fox, J. M. Orenstein, D. P. Kotler, and A. S. Fauci. 1993. HIV infection is active and progressive in lymphoid tissue during the clinically latent stage of disease. Nature 362: 355-358.
2. Embretson, J., M. Zupancic, J. L. Ribas, A. Burke, P. Racz, K. Tenner-Racz, and A. T. Haase. 1993. Massive covert infection of helper T lymphocytes and macrophages by HIV during the incubation period of AIDS. Nature 362: 359-362.
3. Heath, S. L., J. G. Tew, A. K. Szakal, and G. F. Burton. 1995. Follicular dendritic cells and human immunodeficiency virus infectivity. Nature 377: 740-744.
4. + T cell demographics and dynamics in lymphatic tissues. Annu. Rev. Immunol. 17: 625-656.
5. Pope, M., and A. T. Haase. 2003. Transmission, acute HIV-1 infection and the quest for strategies to prevent infection. Nat. Med. 9: 847-852.
6. Park, C. S., and Y. S. Choi. 2005. How do follicular dendritic cells interact intimately with B cells in the germinal centre. Immunology 114: 2-10.
7. Kosco-Vilbois, M. H. 2003. Are follicular dendritic cells really good for nothing. Nat. Rev. Immunol. 3: 764-769.
8. Rosenberg, Y. J., M. G. Lewis, and M. H. Kosco-Vilbois. 1998. Enhanced follicular dendritic cell-B cell interaction in HIV and SIV infections and its potential role in polyclonal B cell activation. Dev. Immunol. 6: 61-70.
9. Rademakers, L. H., H. J. Schuurman, J. F. de Frankrijker, and A. Van Ooyen. 1992. Cellular composition of germinal centers in lymph nodes after HIV-1 infection: evidence for an inadequate support of germinal center B lymphocytes by follicular dendritic cells. Clin. Immunol. Immunopathol. 62: 148-159.
10. Yamanaka, H., K. Teruya, M. Tanaka, Y. Kikuchi, T. Takahashi, S. Kimura, and S. Oka. 2005. Efficacy and immunologic responses to influenza vaccine in HIV-1-infected patients. J. Acquir. Immune Defic. Syndr. 39: 167-173.
11. Malaspina, A., S. Moir, S. M. Orsega, J. Vasquez, N. J. Miller, E. T. Donoghue, S. Kottilil, M. Gezmu, D. Follmann, G. M. Vodeiko, et al. 2005. Compromised B cell responses to influenza vaccination in HIV-infected individuals. J. Infect. Dis. 191: 1442-1450.
12. Tasker, S. A., M. R. Wallace, J. B. Rubins, W. B. Paxton, J. O'Brien, and E. N. Janoff. 2002. Reimmunization with 23-valent pneumococcal vaccine for patients infected with human immunodeficiency virus type 1: clinical, immunologic, and virologic responses. Clin. Infect. Dis. 34: 813-821.
13. + cell depletion. J. Infect. Dis. 188: 1794-1803.
14. Kacani, L., W. M. Prodinger, G. M. Sprinzl, M. G. Schwendinger, M. Spruth, H. Stoiber, S. Döpper, 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.
15. Moir, S., A. Malaspina, Y. Li, T. W. Chun, T. Lowe, J. Adelsberger, M. Baseler, L. A. Ehler, S. Liu, R. T. Davey, Jr., et al. 2000. B cells of HIV-1-infected patients bind virions through CD21-complement interactions and transmit infectious virus to activated T cells. J. Exp. Med. 192: 637-646.
16. + T cells and circulating in plasma. J. Virol. 76: 8855-8863.
17. 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.
18. Guthridge, J. M., K. Young, M. G. Gipson, M. R. Sarrias, G. Szakonyi, X. S. Chen, A. Malaspina, E. Donoghue, J. A. James, J. D. Lambris, et al. 2001. Epitope mapping using the X-ray crystallographic structure of complement receptor type 2 (CR2)/CD21: identification of a highly inhibitory monoclonal antibody that directly recognizes the CR2-C3d interface. J. Immunol. 167: 5758-5766.
19. Abacioglu, Y. H., T. R. Fouts, J. D. Laman, E. Claassen, S. H. Pincus, J. P. Moore, C. A. Roby, R. Kamin-Lewis, and G. K. Lewis. 1994. Epitope mapping and topology of baculovirus-expressed HIV-1 gp160 determined with a panel of murine monoclonal antibodies. AIDS Res. Hum. Retroviruses 10: 371-381.
20. Chesebro, B., and K. Wehrly. 1988. Development of a sensitive quantitative focal assay for human immunodeficiency virus infectivity. J. Virol. 62: 3779-3788.
21. Thiriart, C., M. Francotte, J. Cohen, C. Collignon, A. Delers, S. Kummert, C. Molitor, D. Gilles, P. Roelants, F. van Wijnendaele, et al. 1989. Several antigenic determinants exposed on the gp120 moiety of HIV-1 gp160 are hidden on the mature gp120. J. Immunol. 143: 1832-1836.
22. Chen, H., T. J. Boyle, M. H. Malim, B. R. Cullen, and H. K. Lyerly. 1992. Derivation of a biologically contained replication system for human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. USA 89: 7678-7682.
23. Molina, H., V. M. Holers, B. Li, Y. Fung, S. Mariathasan, J. Goellner, J. Strauss-Schoenberger, R. W. Karr, and D. D. Chaplin. 1996. Markedly impaired humoral immune response in mice deficient in complement receptors 1 and 2. Proc. Natl. Acad. Sci. USA 93: 3357-3361.
24. Sukumar, S., A. K. Szakal, and J. G. Tew. 2006. Isolation of functionally active murine follicular dendritic cells. J. Immunol. Methods 313: 81-95.
25. Molina, H., C. Brenner, S. Jacobi, J. Gorka, J. C. Carel, T. Kinoshita, and V. M. Holers. 1991. Analysis of Epstein-Barr virus-binding sites on complement receptor 2 (CR2/CD21) using human-mouse chimeras and peptides: at least two distinct sites are necessary for ligand-receptor interaction. J. Biol. Chem. 266: 12173-12179.
26. Peltz, G. A., M. L. Trounstine, and K. W. Moore. 1988. Cloned and expressed human Fc receptor for IgG mediates anti-CD3-dependent lymphoproliferation. J. Immunol. 141: 1891-1896.
27. + T cells in viremic versus aviremic HIV-infected individuals. Proc. Natl. Acad. Sci. USA 100: 1908-1913.
28. Azeredo da Silveira, S., S. Kikuchi, L. Fossati-Jimack, T. Moll, T. Saito, J. S. Verbeek, M. Botto, M. J. Walport, M. Carroll, and S. Izui. 2002. Complement activation selectively potentiates the pathogenicity of the IgG2b and IgG3 isotypes of a high affinity anti-erythrocyte autoantibody. J. Exp. Med. 195: 665-672.
29. Klaus, G. G., M. B. Pepys, K. Kitajima, and B. A. Askonas. 1979. Activation of mouse complement by different classes of mouse antibody. Immunology 38: 687-695.
30. Neuberger, M. S., and K. Rajewsky. 1981. Activation of mouse complement by monoclonal mouse antibodies. Eur. J. Immunol. 11: 1012-1016.
31. 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.
32. Qin, D., J. Wu, K. A. Vora, J. V. Ravetch, A. K. Szakal, T. Manser, and J. G. Tew. 2000. Fcγ receptor IIB on follicular dendritic cells regulates the B cell recall response. J. Immunol. 164: 6268-6275.
33. Banki, Z., L. Kacani, P. Rusert, M. Pruenster, D. Wilflingseder, B. Falkensammer, H. J. Stellbrink, J. van Lunzen, A. Trkola, M. P. Dierich, and H. Stoiber. 2005. Complement dependent trapping of infectious HIV in human lymphoid tissues. AIDS 19: 481-486.
34. Heyman, B., E. J. Wiersma, and T. Kinoshita. 1990. In vivo inhibition of the antibody response by a complement receptor-specific monoclonal antibody. J. Exp. Med. 172: 665-668.
35. 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, et al. 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.
36. Schacker, T., S. Little, E. Connick, K. Gebhard-Mitchell, Z. Q. Zhang, J. Krieger, J. Pryor, D. Havlir, J. K. Wong, D. Richman, et al. 2000. Rapid accumulation of human immunodeficiency virus (HIV) in lymphatic tissue reservoirs during acute and early HIV infection: implications for timing of antiretroviral therapy. J. Infect. Dis. 181: 354-357.
37. + T cells. Science 286: 1353-1357.
38. Stahl-Hennig, C., R. M. Steinman, K. Tenner-Racz, M. Pope, N. Stolte, K. Mätz-Rensing, G. Grobschupff, B. Raschdorff, G. Hunsmann, and P. Racz. 1999. Rapid infection of oral mucosal-associated lymphoid tissue with simian immunodeficiency virus. Science 285: 1261-1265.
39. Baskin, G. B., L. N. Martin, M. Murphey-Corb, F. S. Hu, D. Kuebler, and B. Davison. 1995. Distribution of SIV in lymph nodes of serially sacrificed rhesus monkeys. AIDS Res. Hum. Retroviruses 11: 273-285.
40. Chakrabarti, L., P. Isola, M. C. Cumont, M. A. Claessens-Maire, M. Hurtrel, L. Montagnier, and B. Hurtrel. 1994. Early stages of simian immunodeficiency virus infection in lymph nodes: evidence for high viral load and successive populations of target cells. Am. J. Pathol. 144: 1226-1237.
41. Joling, P., L. J. Bakker, J. A. Van Strijp, T. Meerloo, L. de Graaf, M. E. Dekker, J. Goudsmit, J. Verhoef, and H. J. Schuurman. 1993. Binding of human immunodeficiency virus type-1 to follicular dendritic cells in vitro is complement dependent. J. Immunol. 150: 1065-1073.
42. Ji, X., H. Gewurz, and G. T. Spear. 2005. Mannose binding lectin (MBL) and HIV. Mol. Immunol. 42: 145-152.
43. Taruishi, M., K. Terashima, Z. Dewan, N. Yamamoto, S. Ikeda, D. Kobayashi, Y. Eishi, M. Yamazaki, T. Furusaka, M. Sugimoto, et al. 2004. Role of follicular dendritic cells in the early HIV-1 infection: in vitro model without specific antibody. Microbiol. Immunol. 48: 693-702.
44. Molina, H., W. Wong, T. Kinoshita, C. Brenner, S. Foley, and V. M. Holers. 1992. Distinct receptor and regulatory properties of recombinant mouse complement receptor. 1 (CR1) and Crry, the two genetic homologues of human CR1. J. Exp. Med. 175: 121-129.
45. Holers, V. M., T. Kinoshita, and H. Molina. 1992. The evolution of mouse and human complement C3-binding proteins: divergence of form but conservation of function. Immunol. Today 13: 231-236.
46. Molina, H. 2002. Update on complement in the pathogenesis of systemic lupus erythematosus. Curr. Opin. Rheumatol. 14: 492-497.
47. Spear, G. T., B. L. Sullivan, D. M. Takefman, A. L. Landay, and T. F. Lint. 1991. Human immunodeficiency virus (HIV)-infected cells and free virus directly activate the classical complement pathway in rabbit, mouse and guinea-pig sera; activation results in virus neutralization by virolysis. Immunology 73: 377-382.
48. Stoiber, H., C. Speth, and M. P. Dierich. 2003. Role of complement in the control of HIV dynamics and pathogenesis. Vaccine 21(Suppl. 2): S77-S82.
49. Manderson, A. P., M. C. Pickering, M. Botto, M. J. Walport, and C. R. Parish. 2001. Continual low-level activation of the classical complement pathway. J. Exp. Med. 194: 747-756.
50. Huber, M., M. Fischer, B. Misselwitz, A. Manrique, H. Kuster, B. Niederost, R. Weber, V. von Wyl, H. F. Gunthard, and A. Trkola. 2006. Complement lysis activity in autologous plasma is associated with lower viral loads during the acute phase of HIV-1 infection. PLoS Med. 3: e441.
51. Carroll, M. C. 2004. The complement system in regulation of adaptive immunity. Nat. Immunol. 5: 981-986.
52. Hlavacek, W. S., N. I. Stilianakis, D. W. Notermans, S. A. Danner, and A. S. Perelson. 2000. Influence of follicular dendritic cells on decay of HIV during antiretroviral therapy. Proc. Natl. Acad. Sci. USA 97: 10966-10971.