Effect of B-cell depletion on viral replication and clinical outcome of simian immunodeficiency virus infection in a natural host

Journal of Virology

Volumn 83, Issue 20, 2009, Pages 10347-10357

  Gaufin, Thaidra ^a   Pattison, Melissa ^a   Gautam, Rajeev ^a   Stoulig, Crystal ^a   Dufour, Jason ^a   MacFarland, Jeanne ^a   Mandell, Daniel ^a   Tatum, Coty ^a   Marx, Matthew H ^a   Ribeiro, Ruy M ^b   Montefiori, David ^c   Apetrei, Cristian ^a,d,f   Pandrea, Ivona ^a,e,f  

^a TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

^b LOS ALAMOS NATIONAL LABORATORY   (United States)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d TULANE UNIVERSITY   (United States)

^e TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD20 ANTIGEN; CD79A ANTIGEN; NEUTRALIZING ANTIBODY; RITUXIMAB;

ACUTE DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; B LYMPHOCYTE; BLOOD; CD4+ T LYMPHOCYTE; CERCOPITHECIDAE; CHRONIC DISEASE; COMPARATIVE STUDY; CONTROLLED STUDY; GERMINAL CENTER; HISTOLOGY; HOST; IMMUNE RESPONSE; INTESTINE; LYMPH NODE; MUCOSA; NONHUMAN; OUTCOME ASSESSMENT; PEYER PATCH; PRIORITY JOURNAL; SEROCONVERSION; SIMIAN IMMUNODEFICIENCY VIRUS; TREATMENT DURATION; VIRUS INFECTION; VIRUS LOAD; VIRUS REPLICATION;

ACUTE DISEASE; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, MONOCLONAL, MURINE-DERIVED; ANTIBODIES, VIRAL; ANTIGENS, CD20; B-LYMPHOCYTES; CERCOPITHECUS AETHIOPS; CHRONIC DISEASE; FLOW CYTOMETRY; IMMUNOLOGIC FACTORS; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DEPLETION; MONKEY DISEASES; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS REPLICATION;

ANIMALIA; CERCOPITHECUS AETHIOPS; MACACA MULATTA; PRIMATES; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 70349733184     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00880-09     Document Type: Article

References (76)

1. Allan, J. S., J. Strauss, and D. W. Buck. 1990. Enhancement of SIV infection with soluble receptor molecules. Science 247:1084-1088. (Pubitemid 20102466)
2. Anolik, J. H., D. Campbell, R. E. Felgar, F. Young, I. Sanz, J. Rosenblatt, and R. J. Looney. 2003. The relationship of FcγRIIIa genotype to degree of B cell depletion by rituximab in the treatment of systemic lupus erythematosus. Arthritis Rheum. 48:455-459.
3. Barry, A. P., G. Silvestri, J. T. Safrit, B. Sumpter, N. Kozyr, H. M. McClure, S. I. Staprans, and M. B. Feinberg. 2007. Depletion of CD8+ cells in sooty mangabey monkeys naturally infected with simian immunodeficiency virus reveals limited role for immune control of virus replication in a natural host species. J. Immunol. 178:8002-8012.
4. Brenchley, J. M., D. A. Price, T. W. Schacker, T. E. Asher, G. Silvestri, S. Rao, Z. Kazzaz, O. Lambotte, D. Altmann, B. R. Blazar, B. Rodriguez, L. Teixeira-Johnson, A. Landay, J. N. Martin, F. M. Hecht, L. J. Picker, M. Lederman, S. G. Deeks, and D. C. Douek. 2006. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat. Med. 12:1365-1371.
5. Cartron, G., L. Dacheux, G. Salles, P. Solal-Celigny, P. Bardos, P. Colombat, and H. Watier. 2002. Therapeutic activity of humanized anti-CD20 monoclonal antibody and polymorphism in IgG Fc receptor FcγRIIIa gene. Blood 99:754-758. (Pubitemid 34525533)
6. Chakrabarti, L. A. 2004. The paradox of simian immunodeficiency virus infection in sooty mangabeys: active viral replication without disease progression. Front. Biosci. 9:521-539.
7. Colombat, P., G. Salles, N. Brousse, P. Eftekhari, P. Soubeyran, V. Delwail, E. Deconinck, C. Haioun, C. Foussard, C. Sebban, A. Stamatoullas, N. Milpied, F. Boue, B. Taillan, P. Lederlin, A. Najman, C. Thieblemont, F. Montestruc, A. Mathieu-Boue, A. Benzohra, and P. Solal-Celigny. 2001. Rituximab (anti-CD20 monoclonal antibody) as single first-line therapy for patients with follicular lymphoma with a low tumor burden: clinical and molecular evaluation. Blood 97:101-106. (Pubitemid 32061248)
8. Crooks, E. T., P. L. Moore, D. Richman, J. Robinson, J. A. Crooks, M. Franti, N. Schulke, and J. M. Binley. 2005. Characterizing anti-HIV monoclonal antibodies and immune sera by defining the mechanism of neutralization. Hum. Antibodies 14:101-113.
9. Cumont, M. C., O. Diop, B. Vaslin, C. Elbim, L. Viollet, V. Monceaux, S. Lay, G. Silvestri, R. Le Grand, M. Muller-Trutwin, B. Hurtrel, and J. Estaquier. 2008. Early divergence in lymphoid tissue apoptosis between pathogenic and nonpathogenic simian immunodeficiency virus infections of nonhuman primates. J. Virol. 82:1175-1184.
10. De Milito, A. 2004. B lymphocyte dysfunctions in HIV infection. Curr. HIV Res. 2:11-21.
11. 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. (Pubitemid 38393277)
12. Diop, O. M., A. Gueye, M. Dias-Tavares, C. Kornfeld, A. Faye, P. Ave, M. Huerre, S. Corbet, F. Barre-Sinoussi, and M. C. Muller-Trutwin. 2000. High levels of viral replication during primary simian immunodeficiency virus SIVagm infection are rapidly and strongly controlled in African green monkeys. J. Virol. 74:7538-7547.
13. Dunham, R., P. Pagliardini, S. Gordon, B. Sumpter, J. Engram, A. Moanna, M. Paiardini, J. N. Mandl, B. Lawson, S. Garg, H. M. McClure, Y. X. Xu, C. Ibegbu, K. Easley, N. Katz, I. Pandrea, C. Apetrei, D. L. Sodora, S. I. Staprans, M. B. Feinberg, and G. Silvestri. 2006. The AIDS resistance of naturally SIV-infected sooty mangabeys is independent of cellular immunity to the virus. Blood 108:209-217. (Pubitemid 43990631)
14. Favre, D., S. Lederer, B. Kanwar, Z. M. Ma, S. Proll, Z. Kasakow, J. Mold, L. Swainson, J. D. Barbour, C. R. Baskin, R. Palermo, I. Pandrea, C. J. Miller, M. G. Katze, and J. M. McCune. 2009. Critical loss of the balance between Th17 and T regulatory cell populations in pathogenic SIV infection. Plos Pathog. 5:e1000295.
15. Flynn, N. M., D. N. Forthal, C. D. Harro, F. N. Judson, K. H. Mayer, and M. F. Para. 2005. Placebo-controlled phase 3 trial of a recombinant glycoprotein 120 vaccine to prevent HIV-1 infection. J. Infect. Dis. 191:654-665.
16. Frost, S. D., T. Wrin, D. M. Smith, S. L. Kosakovsky Pond, Y. Liu, E. Paxinos, C. Chappey, J. Galovich, J. Beauchaine, C. J. Petropoulos, S. J. Little, and D. D. Richman. 2005. Neutralizing antibody responses drive the evolution of human immunodeficiency virus type 1 envelope during recent HIV infection. Proc. Natl. Acad. Sci. USA 102:18514-18519.
17. Fuentes-Panana, E. M., G. Bannish, and J. G. Monroe. 2004. Basal B-cell receptor signaling in B lymphocytes: mechanisms of regulation and role in positive selection, differentiation, and peripheral survival. Immunol. Rev. 197:26-40.
18. Gaufin, T., R. Gautam, M. Kasheta, R. M. Ribeiro, E. Ribka, M. Barnes, M. Pattison, C. Tatum, J. MacFarland, D. Montefiori, A. Kaur, I. Pandrea, and C. Apetrei. 2009. Limited ability of humoral immune responses in control of viremia during infection with a neutralization-sensitive SIV strain. Blood 113:4250-4261.
19. Gicheru, M. M., M. Otsyula, P. Spearman, B. S. Graham, C. J. Miller, H. L. Robinson, N. L. Haigwood, and D. C. Montefiori. 1999. Neutralizing antibody responses in Africa green monkeys naturally infected with simian immunodeficiency virus (SIVagm). J. Med. Primatol. 28:97-104.
20. Giorgi, J. V., L. E. Hultin, J. A. McKeating, T. D. Johnson, B. Owens, L. P. Jacobson, R. Shih, J. Lewis, D. J. Wiley, J. P. Phair, S. M. Wolinsky, and R. Detels. 1999. Shorter survival in advanced human immunodeficiency virus type 1 infection is more closely associated with T lymphocyte activation than with plasma virus burden or virus chemokine coreceptor usage. J. Infect. Dis. 179:859-870.
21. Gordon, S., N. R. Klatt, J. M. Milush, J. Engram, R. M. Dunham, M. Paiardini, E. A. Strobert, C. Apetrei, I. Pandrea, S. Staprans, D. L. Sodora, and G. Silvestri. 2007. Severe depletion of mucosal CD4+ T cells in AIDS-free SIV-infected sooty mangabeys. J. Immunol. 179:3026-3034.
22. Hainsworth, J. D., H. A. Burris III, L. H. Morrissey, S. Litchy, D. C. Scullin, Jr., J. D. Bearden III, P. Richards, and F. A. Greco. 2000. Rituximab monoclonal antibody as initial systemic therapy for patients with low-grade non-Hodgkin lymphoma. Blood 95:3052-3056.
23. Hazenberg, M. D., S. A. Otto, B. H. van Benthem, M. T. Roos, R. A. Coutinho, J. M. Lange, D. Hamann, M. Prins, and F. Miedema. 2003. Persistent immune activation in HIV-1 infection is associated with progression to AIDS. AIDS 17:1881-1888.
24. Hirsch, V. M. 2004. What can natural infection of African monkeys with simian immunodeficiency virus tell us about the pathogenesis of AIDS? AIDS Rev. 6:40-53.
25. Hirsch, V. M., B. J. Campbell, E. Bailes, R. Goeken, C. Brown, W. R. Elkins, M. Axthelm, M. Murphey-Corb, and P. M. Sharp. 1999. Characterization of a novel simian immunodeficiency virus (SIV) from L'Hoest monkeys (Cercopithecus l'hoesti): implications for the origins of SIVmnd and other primate lentiviruses. J. Virol. 73:1036-1045.
26. Hirsch, V. M., and P. R. Johnson. 1994. Pathogenic diversity of simian immunodeficiency viruses. Virus Res. 32:183-203. (Pubitemid 24147716)
27. Hunziker, L., M. Recher, A. J. Macpherson, A. Ciurea, S. Freigang, H. Hengartner, and R. M. Zinkernagel. 2003. Hypergammaglobulinemia and autoantibody induction mechanisms in viral infections. Nat. Immunol. 4:343-349.
28. Kaur, A., L. Alexander, S. I. Staprans, L. Denekamp, C. L. Hale, H. M. McClure, M. B. Feinberg, R. C. Desrosiers, and R. P. Johnson. 2001. Emergence of cytotoxic T lymphocyte escape mutations in nonpathogenic simian immunodeficiency virus infection. Eur. J. Immunol. 31:3207-3217.
29. Kaur, A., J. Yang, D. Hempel, L. Gritz, G. P. Mazzara, H. McClure, and R. P. Johnson. 2000. Identification of multiple simian immunodeficiency virus (SIV)-specific CTL epitopes in sooty mangabeys with natural and experimentally acquired SIV infection. J. Immunol. 164:934-943. (Pubitemid 30043720)
30. Kornfeld, C., M. J. Ploquin, I. Pandrea, A. Faye, R. Onanga, C. Apetrei, V. Poaty-Mavoungou, P. Rouquet, J. Estaquier, L. Mortara, J. F. Desoutter, C. Butor, R. Le Grand, P. Roques, F. Simon, F. Barre-Sinoussi, O. M. Diop, and M. C. Muller-Trutwin. 2005. Antiinflammatory profiles during primary SIV infection in African green monkeys are associated with protection against AIDS. J. Clin. Investig. 115:1082-1091.
31. Liossis, S. N., and P. P. Sfikakis. 2008. Rituximab-induced B cell depletion in autoimmune diseases: potential effects on T cells. Clin. Immunol. 127: 280-285.
32. Malaspina, A., S. Moir, S. Kottilil, C. W. Hallahan, L. A. Ehler, S. Liu, M. A. Planta, T. W. Chun, and A. S. Fauci. 2003. Deleterious effect of HIV-1 plasma viremia on B cell costimulatory function. J. Immunol. 170:5965-5972. (Pubitemid 36682576)
33. Mandl, J. N., A. P. Barry, T. H. Vanderford, N. Kozyr, R. Chavan, S. Klucking, F. J. Barrat, R. L. Coffman, S. I. Staprans, and M. B. Feinberg. 2008. Divergent TLR7 and TLR9 signaling and type I interferon production distinguish pathogenic and nonpathogenic AIDS virus infections. Nat. Med. 14:1077-1087.
34. Mascola, J. R. 2002. Passive transfer studies to elucidate the role of antibody- mediated protection against HIV-1. Vaccine 20:1922-1925.
35. Mascola, J. R., G. Stiegler, T. C. VanCott, H. Katinger, C. B. Carpenter, C. E. Hanson, H. Beary, D. Hayes, S. S. Frankel, D. L. Birx, and M. G. Lewis. 2000. Protection of macaques against vaginal transmission of a pathogenic HIV-1/SIV chimeric virus by passive infusion of neutralizing antibodies. Nat. Med. 6:207-210.
36. McMichael, A. J. 2006. HIV vaccines. Annu. Rev. Immunol. 24:227-255.
37. + Tlymphocyte apoptosis and bystander T-cell activation in rhesus macaques and sooty mangabeys during acute simian immunodeficiency virus infection. J. Virol. 83:572-583.
38. Miller, C. J., M. Genesca, K. Abel, D. Montefiori, D. Forthal, K. Bost, J. Li, D. Favre, and J. M. McCune. 2007. Antiviral antibodies are necessary for control of simian immunodeficiency virus replication. J. Virol. 81:5024-5035. (Pubitemid 46744414)
39. Moir, S., K. M. Ogwaro, A. Malaspina, J. Vasquez, E. T. Donoghue, C. W. Hallahan, S. Liu, L. A. Ehler, M. A. Planta, S. Kottilil, T. W. Chun, and A. S. Fauci. 2003. Perturbations in B cell responsiveness to CD4+ T cell help in HIV-infected individuals. Proc. Natl. Acad. Sci. USA 100:6057-6062.
40. Montefiori, D. C. 2004. Evaluating neutralizing antibodies against HIV, SIV and SHIV in a luciferase reporter gene assay. In J. E. Coligan, A. M. Kruisbeek, D. H. Margulies, E. M. Shevach, W. Strober, and R. Coico (ed.), Current protocols in immunology. John Wiley & Sons, Hoboken, NJ.
41. National Research Council. 1996. Guide for the care and use of laboratory animals. National Academy Press, Washington, DC.
42. Norley, S., and R. Kurth. 2004. The role of the immune response during SIVagm infection of the African green monkey natural host. Front Biosci. 9:550-564. (Pubitemid 39043734)
43. Norley, S. G., G. Kraus, J. Ennen, J. Bonilla, H. Konig, and R. Kurth. 1990. Immunological studies of the basis for the apathogenicity of simian immunodeficiency virus from African green monkeys. Proc. Natl. Acad. Sci. USA 87:9067-9071.
44. + cell numbers during the early phase of experimental infection with simian immunodeficiency virus SIVmnd-1 in Mandrillus sphinx. J. Virol. 76:10256-10263.
45. Onanga, R., S. Souquiere, M. Makuwa, A. Mouinga-Ondeme, F. Simon, C. Apetrei, and P. Roques. 2006. Primary simian immunodeficiency virus SIVmnd-2 infection in mandrills (Mandrillus sphinx). J. Virol. 80:3303-3309.
46. Pandrea, I., C. Apetrei, J. Dufour, N. Dillon, J. Barbercheck, M. Metzger, B. Jacquelin, R. Bohm, P. A. Marx, F. Barre-Sinoussi, V. M. Hirsch, M. C. Muller-Trutwin, A. A. Lackner, and R. Veazey. 2006. Simian immunodeficiency virus (SIV) SIVagm.sab infection of Caribbean African green monkeys: new model of the study of SIV pathogenesis in natural hosts. J. Virol. 80:4858-4867.
47. Pandrea, I., C. Apetrei, S. Gordon, J. Barbercheck, J. Dufour, R. Bohm, B. Sumpter, P. Roques, P. A. Marx, V. M. Hirsch, A. Kaur, A. A. Lackner, R. S. Veazey, and G. Silvestri. 2007. Paucity of CD4+CCR5+ T cells is a typical feature of natural SIV hosts. Blood 109:1069-1076.
48. Pandrea, I., R. Gautam, R. Ribeiro, J. M. Brenchley, I. F. Butler, M. Pattison, T. Rasmussen, P. A. Marx, G. Silvestri, A. A. Lackner, A. S. Perelson, D. C. Douek, R. S. Veazey, and C. Apetrei. 2007. Acute loss of intestinal CD4+ T cells is not predictive of SIV virulence. J. Immunol. 179:3035-3046.
49. Pandrea, I., C. Kornfeld, M. J.-I. Ploquin, C. Apetrei, A. Faye, P. Rouquet, P. Roques, F. Simon, F. Barré-Sinoussi, M. C. Müller-Trutwin, and O. M. Diop. 2005. Impact of viral factors on very early in vivo replication profiles in SIVagm-infected African green monkeys. J. Virol. 79:6249-6259.
50. Pandrea, I., R. Onanga, C. Kornfeld, P. Rouquet, O. Bourry, S. Clifford, P. T. Telfer, K. Abernethy, L. T. White, P. Ngari, M. Muller-Trutwin, P. Roques, P. A. Marx, F. Simon, and C. Apetrei. 2003. High levels of SIVmnd-1 replication in chronically infected Mandrillus sphinx. Virology 317:119-127. (Pubitemid 37522233)
51. Pandrea, I., R. M. Ribeiro, R. Gautam, T. Gaufin, M. Pattison, M. Barnes, C. Monjure, C. Stoulig, G. Silvestri, M. Miller, A. S. Perelson, and C. Apetrei. 2008. Simian immunodeficiency virus SIVagm dynamics in African green monkeys. J. Virol. 82:3713-3724.
52. Pandrea, I., G. Silvestri, R. Onanga, R. S. Veazey, P. A. Marx, V. M. Hirsch, and C. Apetrei. 2006. Simian immunodeficiency viruses replication dynamics in African non-human primate hosts: common patterns and species-specific differences. J. Med. Primatol. 35:194-201.
53. Pandrea, I., D. L. Sodora, G. Silvestri, and C. Apetrei. 2008. Into the wild: simian immunodeficiency virus (SIV) infection in natural hosts. Trends Immunol. 29:419-428.
54. Parren, P. W., P. A. Marx, A. J. Hessell, A. Luckay, J. Harouse, C. Cheng- Mayer, J. P. Moore, and D. R. Burton. 2001. Antibody protects macaques against vaginal challenge with a pathogenic R5 simian/human immunodeficiency virus at serum levels giving complete neutralization in vitro. J. Virol. 75:8340-8347.
55. Richman, D. D., T. Wrin, S. J. Little, and C. J. Petropoulos. 2003. Rapid evolution of the neutralizing antibody response to HIV type 1 infection. Proc. Natl. Acad. Sci. USA 100:4144-4149.
56. Rogers, K. A., F. Scinicariello, and R. Attanasio. 2006. IgG Fc receptor III homologues in nonhuman primate species: genetic characterization and ligand interactions. J. Immunol. 177:3848-3856.
57. Schmitz, J. E., M. J. Kuroda, S. Santra, M. A. Simon, M. A. Lifton, W. Lin, R. Khunkhun, M. Piatak, J. D. Lifson, G. Grosschupff, R. S. Gelman, P. Racz, K. Tenner-Racz, K. A. Mansfield, N. L. Letvin, D. C. Montefiori, and K. A. Reimann. 2003. Effect of humoral immune responses on controlling viremia during primary infection of rhesus monkeys with simian immunodeficiency virus. J. Virol. 77:2165-2173.
58. Sfikakis, P. P., J. N. Boletis, S. Lionaki, V. Vigklis, K. G. Fragiadaki, A. Iniotaki, and H. M. Moutsopoulos. 2005. Remission of proliferative lupus nephritis following B cell depletion therapy is preceded by down-regulation of the T cell costimulatory molecule CD40 ligand: an open-label trial. Arthritis Rheum. 52:501-513.
59. Shirai, A., M. Cosentino, S. F. Leitman-Klinman, and D. M. Klinman. 1992. Human immunodeficiency virus infection induces both polyclonal and virus-specific B cell activation. J. Clin. Investig. 89:561-566.
60. Siegel, F., R. Kurth, and S. Norley. 1995. Neither whole inactivated virus immunogen nor passive immunoglobulin transfer protects against SIVagm infection in the African green monkey natural host. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 8:217-226.
61. Silvestri, G. 2005. Naturally SIV-infected sooty mangabeys: are we closer to understanding why they do not develop AIDS? J. Med. Primatol. 34:243-252.
62. Silvestri, G., A. Fedanov, S. Germon, N. Kozyr, W. J. Kaiser, D. A. Garber, H. McClure, M. B. Feinberg, and S. I. Staprans. 2005. Divergent host responses during primary simian immunodeficiency virus SIVsm infection of natural sooty mangabey and nonnatural rhesus macaque hosts. J. Virol. 79:4043-4054. (Pubitemid 40388344)
63. Silvestri, G., D. L. Sodora, R. A. Koup, M. Paiardini, S. P. O'Neil, H. M. McClure, S. I. Staprans, and M. B. Feinberg. 2003. Nonpathogenic SIV infection of sooty mangabeys is characterized by limited bystander immunopathology despite chronic high-level viremia. Immunity 18:441-452. (Pubitemid 36351522)
64. Simon, F., S. Souquiere, F. Damond, A. Kfutwah, M. Makuwa, E. Leroy, P. Rouquet, J. L. Berthier, J. Rigoulet, A. Lecu, P. T. Telfer, I. Pandrea, J. C. Plantier, F. Barre-Sinoussi, P. Roques, M. C. Muller-Trutwin, and C. Apetrei. 2001. Synthetic peptide strategy for the detection of and discrimination among highly divergent primate lentiviruses. AIDS Res. Hum. Retrovir. 17:937-952.
65. Sousa, A. E., J. Carneiro, M. Meier-Schellersheim, Z. Grossman, and R. M. Victorino. 2002. CD4 T cell depletion is linked directly to immune activation in the pathogenesis of HIV-1 and HIV-2 but only indirectly to the viral load. J. Immunol. 169:3400-3406.
66. Titanji, K., F. Chiodi, R. Bellocco, D. Schepis, L. Osorio, C. Tassandin, G. Tambussi, S. Grutzmeier, L. Lopalco, and A. De Milito. 2005. Primary HIV-1 infection sets the stage for important B lymphocyte dysfunctions. AIDS 19:1947-1955. (Pubitemid 41669018)
67. Titanji, K., A. De Milito, A. Cagigi, R. Thorstensson, S. Grutzmeier, A. Atlas, B. Hejdeman, F. P. Kroon, L. Lopalco, A. Nilsson, and F. Chiodi. 2006. Loss of memory B cells impairs maintenance of long-term serologic memory during HIV-1 infection. Blood 108:1580-1587. (Pubitemid 44316125)
68. Tokunaga, M., K. Saito, D. Kawabata, Y. Imura, T. Fujii, S. Nakayamada, S. Tsujimura, M. Nawata, S. Iwata, T. Azuma, T. Mimori, and Y. Tanaka. 2007. Efficacy of rituximab (anti-CD20) for refractory systemic lupus erythematosus involving the central nervous system. Ann. Rheum. Dis. 66:470-475.
69. Treon, S. P., M. Hansen, A. R. Branagan, S. Verselis, C. Emmanouilides, E. Kimby, S. R. Frankel, N. Touroutoglou, B. Turnbull, K. C. Anderson, D. G. Maloney, and E. A. Fox. 2005. Polymorphisms in FcγRIIIA (CD16) receptor expression are associated with clinical response to rituximab in Waldenstrom's macroglobulinemia. J. Clin. Oncol. 23:474-481.
70. Vallerskog, T., I. Gunnarsson, M. Widhe, A. Risselada, L. Klareskog, R. van Vollenhoven, V. Malmstrom, and C. Trollmo. 2007. Treatment with rituximab affects both the cellular and the humoral arm of the immune system in patients with SLE. Clin. Immunol. 122:62-74.
71. VandeWoude, S., and C. Apetrei. 2006. Going wild: Lessons from T-lymphotropic naturally occurring lentiviruses. Clin. Microbiol. Rev. 19:728-762.
72. Veazey, R. S., R. J. Shattock, M. Pope, J. C. Kirijan, J. Jones, Q. Hu, T. Ketas, P. A. Marx, P. J. Klasse, D. R. Burton, and J. P. Moore. 2003. Prevention of virus transmission to macaque monkeys by a vaginally applied monoclonal antibody to HIV-1 gp120. Nat. Med. 9:343-346.
73. + T-lymphocyte responses to simian immunodeficiency virus (SIV) are a consistent feature of natural SIV infection in sooty mangabeys. J. Virol. 80:2771-2783.
74. Watkins, D. I., D. R. Burton, E. G. Kallas, J. P. Moore, and W. C. Koff. 2008. Nonhuman primate models and the failure of the Merck HIV-1 vaccine in humans. Nat. Med. 14:617-621.
75. Wei, X., J. M. Decker, S. Wang, H. Hui, J. C. Kappes, X. Wu, J. F. Salazar- Gonzalez, M. G. Salazar, J. M. Kilby, M. S. Saag, N. L. Komarova, M. A. Nowak, B. H. Hahn, P. D. Kwong, and G. M. Shaw. 2003. Antibody neutralization and escape by HIV-1. Nature 422:307-312.
76. Zahn, R. C., M. D. Rett, B. Korioth-Schmitz, Y. Sun, A. P. Buzby, S. Goldstein, C. R. Brown, R. A. Byrum, G. J. Freeman, N. L. Letvin, V. M. Hirsch, and J. E. Schmitz. 2008. Simian immunodeficiency virus (SIV)- specific CD8+ T cell responses in chronically SIVagm-infected vervet African green monkeys. J. Virol. 82:11577-11588.