Population biology of HIV-1 infection: Viral and CD4+ T cell demographics and dynamics in lymphatic tissues

Annual Review of Immunology

Volumn 17, Issue , 1999, Pages 625-656

  Haase, A T ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Follicular dendritic cells; Immune depletion and restoration; In situ hybridization and in situ PCR; Quantitative image analysis; Treatment; Virus production

Indexed keywords

ANTIRETROVIRUS AGENT;

ANIMAL CELL; CELL DENSITY; CELL POPULATION; DENDRITIC CELL; DISEASE COURSE; HELPER CELL; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IN SITU HYBRIDIZATION; LYMPHOCYTE COUNT; LYMPHOID TISSUE; MODEL; MOLECULAR DYNAMICS; NONHUMAN; PERSISTENT INFECTION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE SUBPOPULATION; VIRUS REPLICATION;

ADULT; ANIMALS; ANTI-HIV AGENTS; APOPTOSIS; CD4-POSITIVE T-LYMPHOCYTES; CELL DIVISION; DENDRITIC CELLS; HEMATOPOIESIS; HIV INFECTIONS; HIV-1; HOMEOSTASIS; HUMANS; LYMPHOID TISSUE; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME;

EID: 0032971372     PISSN: 07320582     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.immunol.17.1.625     Document Type: Review

References (158)

1. Quinn TC. 1996. Global burden of the HIV pandemic. Lancet 348:99-106
2. Tenner-Racz K, Racz P, Gluckman JC, Popovic M. 1988. Cell-free HIV in lymph nodes of patients with persistent generalized lymphadenopathy and AIDS. N. Engl. J. Med. 318:49-50
3. Tenner-Racz K, Racz P, Gartner S, Ramsauer J, Dietrich M, Gluckman JC, Popovic M. 1989. Ultrastructural analysis of germinal centers in lymph nodes of patients with HIV-1-induced persistent generalized lymphadenopathy: evidence for persistence of infection. In Progress in AIDS Pathology, ed. H Rotterdam, SC Sommers, P Racz, PR Meyer, pp 29-40. New York: Field and Wood
4. Tenner-Racz K, Racz P, Schmidt H, Dietrich M, Kern P, Louie A, Gartner S, Popovic M. 1988. Immunohistochemical, electron microscopic and in situ hybridization evidence for the involvement of lymphatics in the spread of HIV-1. AIDS 2:299-309
5. Parmentier HK, van Wichen D, Sie-Go DMDS, Goudsmit J, Borleffs JCC, Schuurman HJ. 1990. HIV-1 infection and virus production in follicular dendritic cells in lymph nodes. Am. J. Pathol. 137:247-51
6. Pantaleo G, Grazioso C, Butini L, Pizzo PA, Schnittman SM, Kotler DP, Fauci AS. 1991. Lymphoid organs function as major reservoirs for human immunodeficiency virus, Proc. Natl. Acad. Sci. USA 88:9838-42
7. Fox CH, Tenner-Racz K, Racz P, Firpo A, Pizzo PA, Fauci AS. 1991. Lymphoid germinal centers are reservoirs of human immunodeficiency virus type I RNA. J. Infect. Dis. 164:1051-57
8. Spiegel H, Herbst H, Niedobitek G, Foss HD, Stein H. 1992. Follicular dendritic cells are a major reservoir for human immunodeficiency virus type I in lymphoid tissues facilitating infection of CD4+ T-helper cells. Am. J. Path. 140:15-22
9. Embretson J, Zupancic M, Ribas JL, Burke A, Racz P, Tenner-Racz K, Haase AT. 1993. Massive covert infection of helper T lymphocytes and macrophages by HIV during the incubation period of AIDS. Nature 362:359-62
10. Pantaleo G, Graziosi C, Demarest JF, Butini L, Montroni M, Fox CH, Orenstein JM, Kotler DP, Fauci AS. 1993. HIV infection is active and progressive in lymphoid tissue during the clinically latent stage of disease. Nature 362:355-9
11. Haase AT, Henry K, Zupancic M, Sedgewick G, Faust RA, Melroe H, Cavert W, Gebhard K, Staskus K, Zhang ZQ, Daily PJ, Balfour HH, Erice A, Perelson AS. 1996. Quantitative image analysis of HIV-1 infection in lymphoid tissue. Science 274:985-9
12. Daar ES, Moudgil T, Meyer RD, Ho DD. 1991. Transient high levels of viremia in patients with primary human immunodeficiency virus type I infection. N. Engl. J. Med. 324:961-4
13. Clark SJ, Saag MS, Decker WD, Campbell-Hill S, Roberson JL, Veldkamp PJ, Kappes JC, Hahn BH, Shaw GM. 1991. High titers of cytopathic virus in plasma of patients with symptomatic primary HIV-1 infection. N. Engl. J. Med. 324:954-60
14. Cooper DA, Gold J, Maclean P, Donovan B, Finlayson R, Barnes TG, Michelmore HM, Brooke P, Penny R. 1985. Acute AIDS retrovirus infection: definition of a clinical illness associated with serocon-version. Lancet 1:537-10
15. Ho DD, Sarngadharan MG, Resnick L, DiMarzo-Veronese F, Rota TR, Hirsch MS. 1985. Primary human T-lymphotropic virus type III infection. Ann. Intern. Med. 103:880-83
16. Henrard DR, Daar E, FarzadeganH, Clark SJ, Phillips J, Shaw GM, Busch MP. 1995. Virologie and immunologic characterization of symptomatic and asymptomatic primary HIV-1 infection. J. Acquir. Immune Defic. Syndr. 9:305-10
17. Schacker TW, Hughes JP, Shea T, Coombs RW, Corey L. 1998. Biological and virologic characteristics of primary HIV infection. Ann. Intern. Med, 128:613-20
18. Koup RA, Safrit JR, Cao Y, Andrews CA, McLeod G, Borkowsky W, Farthing C, Ho DD. Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J. Virol. 68:4650-55
19. Pantaleo G, Graziosi C, Fauci AS. 1993. The immunopathogcnesis of human immunodeficiency virus infection. N. Engl. J. Med. 328:327-35
20. Mellors JW, Rinaldo CR, Gupta P, White RM, Todd JA, Kingsley LA. Prognosis in HIV-1 infection predicted by the quantity of virus in plasma. Science: 272:1167-70
21. Wei X, Ghosh SK, Taylor ME, Johnson VA, Emini KA, Deutsch P, Lifson JD, Bonhoeffer S, Nowak MA, Hahn BH, Saag MS, Shaw GM. 1995. Viral dynamics in human immunodeficiency virus type I infection. Nature 373:117-22
22. Ho DD, Neumann AU, Perelson AS, Chen W, Leonard JM, Markowitz M. 1995. Rapid turnover of plasma virions and CD4 lymphocytes in HIV-1 infection. Nature 373:123-26
23. Cavert W, Notermans DW, Staskus K, Wietgrefe SW, Zupancic M, Gebhard K, Henry K, Zhang ZQ, Mills R, McDade H, Schuwirth CM, Goudsmit J, Danner SA, Haase AT. 1997. Kinetics of response in lymphoid tissues to antiretroviral therapy of HIV-1 infection. Science 276:960-64
24. Finzi D, Hermankova M, Pierson T, Carruth LM, Buck C, Chaisson RE, Quinn TC, Chadwick K, Margolick J, Brookmeyer R, Gallant J, Markowitz M, Ho DD, Richman DD, Siliciano RF. 1997. Identification of a reservoir for HIV-1 in patients on highly active antiretroviral therapy. Science 278:1295-1300
25. Wong JK, Hezareh M, Gunthard HF, Havlir DV, Ignacio CC, Spina CA, Richman DD. 1997. Recovery of replicationcompetent HIV despite prolonged suppression of plasma viremia. Science 278: 1291-95
26. Chun TW, Stuyver L, Mizell SB, Ehler LA, Mican JAM, Baseler M, Lloyd AL, Nowak MA, Fauci AS. 1997. Presence of an inducible HIV-1 latent reservoir during highly active antiretroviral therapy. Proc. Natl. Acad. Sci. USA 94:13193-97
27. Autran B, Carcelain G, Li TS, Blanc C, Mathez D, Tubiana R, Katlama C, Debre P, Leibowitch J. 1997. Positive effects of combined antiretroviral therapy on CD4+ T cell homeostasis and function in advanced HIV disease. Science 277:112 16
28. Zhang ZQ, Notermans DW, Sedgewick G, Cavert W, Wietgrefe S, Zupancic M, Gebhard K, Henry K, Boies L, Chen Z, Jenkins M, Mills R, McDade H, Goodwin C, Schuwirth CM, Danner SA, Haase AT. 1998. Kinetics of CD4+ T cell repopulation of lymphoid tissues after treatment of HIV-1 infection. Proc. Natl. Acad. Sci. USA 95:1154-59
29. Li TS, Tubiana R, Katlama C, Calvez, Ait Mohand H, Autran B. 1998. Long lasting recovery in CD4+ T cell function mirrors viral load reduction after highly active anti-retroviral therapy in patients with advanced HIV disease. Lancet 351:1682-86
30. Komanduri KV, Viswanathan MN, Wieder ED, Schmidt DK, Bredt BM, Jacobson MA, McCune JM. 1998. Restoration of cytomegalovirus-specific CD4+ T lymphocyte responses after ganciclovir and highly active antiretroviral therapy in individuals infected with HIV-1. Nature Med. 4:953-56
31. Palella FJ, Delaney KM, Moorman AC, Loveless MO, Fuhrer J, Satten GA, Aschman DJ, Holmberg SD, HIV Outpatient Study Investigators. 1998. Declining morbidity and mortality among patients with advanced human immunodeficiency virus infection. N. Engl. J. Med. 338, 853-60
32. Miller CJ, Alexander NJ, Vogel P, Anderson J, Marx PA. 1992. Mechanism of genital transmission of SIV: a hypothesis based on transmission studies and the location of SIV in the genital tract of chronically infected female rhesus macaques. J. Med. Primatol. 21,65-68
33. Spira AI, Marx PA, Patterson BK, Mahoney J, Koup RA, Wolinsky SM, Ho DD. 1996. Cellular targets of infection and route of viral dissemination after an intravaginal inoculation of simian immunodeficiency virus into rhesus macaques. J. Exp. Med. 183,215-25
34. Marx PA, Spira AI, Gettie A, Dailey PJ, Veazey RS, Lackner AA, Mahoney CJ, Miller CJ, Claypool LE, Ho DD, Alexander NJ. 1996. Progesterone implants enhance SIV vaginal transmission and early virus load. Nature Med. 2:1084 89
35. Veazey RS, DeMaria M, Chalifoux LV, Shvelz DE, Pauley DR, Knight HL, Rosenzweig M, Johnson RP, Desrosiers RC, Lackner AA. 1998. Gastrointestinal tract as a major site of CD4+ T cell depletion and viral replication in SIV infection. Science 280:427-31
36. Reinhart TA, Rogan MJ, Huddleston D, Rausch DM, Eiden LE, Haase AT. 1997. Simian immunodeficiency virus burden in tissue and cellular compartments during clinical latency and AIDS, J. Infect. Dis. 176:1198-1208
37. Reimann KA, Tenner-Racz K, Racz P, Montefiori DC, Yasutomi Y, Lin W. Ransil BJ, Letvin NL. 1994. Immunopathogenic events in acute infection of rhesus monkeys with simian immunodeficiency virus of macaques. J. Virol. 68: 2362-70
38. Chakrabarti L, Cumont MC, Montagnier L, Hurtrel B. 1994. Variable course of primary simian immunodeficiency virus infection in lymph nodes: relation to disease progression. J. Virol. 68:6634-42
39. Chakrabarti L, Isola P, Cumont MC, Claessens-Maire MA, Hurtrel M, Montagniew L, Hurtrel B. 1994. Early states of simian immunodeficiency virus infection in lymph nodes: evidence for high viral load and successive populations of target cells. Am. J. Pathol. 144:1226-36
40. Orenstein JM, Fox C, Wahl SM. 1997. Macrophages as a source of HIV during opportunistic infections. Science 276: 1857-61
41. Prankel SS, Wenig BM, Burke AP, Mannan P, Thompson LDR, Ahbondanzo SL, Nelson AM, Pope M, Steinman RM. 1996. Replication of HIV-1 in dendritic cell-derived syncytia at the mucosal surface of the adenoid. Science 272:115-17
42. Frankel SS, Tenner-Ratz K, Raez P, Wenig BM, Hansen CH, Heffner D, Nelson AM, Pope M, Steinman RM. 1997. Active replication of HIV-1 at the lymphoepithelial surface of the tonsil. Am. J. Pathol. 151:89-96
43. McIlroy D, Autran B, Cheynier R, WainHohson S, Clauvel JP, Oksenhendler E, Debre P, Hosmalin A. 1995. Infection frequency of dendritic cells and CD4+ T lymphocytes in spleens of human immunodeficiency virus-positive patients. J. Virol. 69:4737-45
44. Livingstone WJ, Moore M, Innes D, Bell JE, Simmonds P, the Edinburgh Heterosexual Transmission Study Group. 1996. Frequent infection of peripheral blood CD8 positive T-lymphocytes with HIV-1. Lancet 348:649-54
45. Stanley SK, McCune JM, Kaneshima H, Justement JS, Sullivan M, Boone E, Baseler M, Adelsberger J, Bonyhadi M, Orenstein J, Fox CH, Fauci AS. 1993. Human immunodeficiency virus infection of the human thymus and disruption of the thymic microenvironment in the SCID hu mouse. J. Exp. Med. 178:1151-63
46. Jamieson BD, Uitlenhogaart CH, Schmid I, Zack JA. 1997. High viral burden and rapid CD4 + cell depletion in human immunodeficiency virus type 1-infected SCID-hu mice suggest direct viral killing of thymocytes in vivo. J. Virol. 71:8245-53
47. Kitchen SG, Uittenbogaart CH, Zack JA. 1997. Mechanism of human immunodeficiency virus type I localization in CD4 negative thymocytes: differentiation from a CD4-positive precursor allows productive infection. J. Virol. 71: 5713-22
48. Lee S, Goldstein H, Baseler M, Adelsberger J, Golding H. 1997. Human immunodeficiency virus type I infection of mature CD3hiCD8+ thymocytes. J. Virol. 71:6671-76
49. Flamand L. Crowley RW, Lusso P, Colombini Hatch S, Margolis DM, Gallo RC. 1998. Activation of CD8+ T lymphocytes through the T cell receptor turns on CD4 gene expression: implications for HIV pathogenesis. Proc. Natl. Acad. Sci. USA 95:3111 16
50. Yang LP, Riley JL, Carroll RG, June CH, Hoxie J, Patterson BK, Ohshima Y, Hodes RJ, Delespess G. 1998. Productive infection of neonatal CD8+ T lymphocytes by HIV-1. J. Exp. Med. 187:1139-44
51. Hufert FT, van Lunzen J, Janossy G, Bertram S, Schmitz J, Haller O, Racz. P, von Laer D. 1997. Germinal centre CD4+ T cells are an important site of HIV replication in vivo. AIDS 11:849-57
52. Klaus GGB, Humphrey JH, Kunkl A, Dongwonh DW. 1980. The follicular dendritic cell: its role in antigen presentation in the generation of immunological memory, Immunol. Rev. 53:3-28
53. Tew JG, Kosco MH, Szakal AK. 1989. The alternative antigen pathway. Immunol. Today 10:229-32
54. Szakal AK, Kosco MH, Smith JP, Tew JG. 1991. Kinetic and ultrastructural aspects of the antigen transport FDC-iccosome-B cell axis. In Accessory Cells in HIV and Other Retroviral Infections, ed. P Racz, CD Dijkstra, JC Gluckman, pp 29-13. Basel, Switzerland: Karger
55. Szakal AK, Kosco MH, Tew JG. 1988. A novel in vivo follicular dendritic celldependent iccosoine-mediated mechanism for delivery of antigen to antigenprocessing cells, J. Immunol. 140:341-53
56. Burton GF, Conrad DH, Szakal AK, Tew JG. 1993. Follicular dendritic cells and B cell costimulation. J. Immunol. 150:31-38
57. Spear GT, Landay AL, Sullivan BL, Dittel B, Lint TF. 1990. Activation of complement on the surface of cells infected by human immunodeficiency virus. J. Immunol 144:1490-96
58. Spear CT, Takefman DM, Sullivan BL, Landay AL, Zolla-Pazner S. 1993. Complement activation by human monoclonal antibodies to human immunodeficiency virus. J. Virol. 67:53 59
59. Joling P, Bakker LJ, Van Strijp JAG, Meerloo T, de Graaf L, Dekker MEM, Goudsmit J, Verhoef J, Schuurman HJ. 1993. Binding of human immunodeficiency virus type-I to follicular dendritic cells in vitro is complement dependent. J. Immunol. 150:1065-73
60. Armstrong JA, Home R. 1984. Follicular dendritic cells and virus-like particles in ATDS-related Iymphadenopathy. Lancet 2:370-72
61. Tsunoda R, Hashimoto K, Baba M, Shigeta S, Sugai N. 1996. Follicular dendritic cells in vitro are not susceptible to infection by HIV-1. AIDS 10:595-602
62. Reinhart TA, Rogan MJ, Viglianti GA, Rausch DM, Eiden LE, Haase AT. 1997. A new approach to investigating the relationship between productive infection and cytopathicity in vivo. Nature Med. 3:218-21
63. Heath SL, Tew JG, Tew JG, Szakal AK, Burton GF. 1995. Follicular dendritic cells and human immunodeficiency virus infectivity. Nature 377:740-44
64. Haase AT, Retzel EF, Staskus KA. 1990. Amplification and detection of lentiviral DNA inside cells. Proc. Natl. Acad. Sci. USA 87:4971-75
65. Chun TW, Carruth L, Finzi D, Shen X, DiGuiseppe JA, Taylor H, Hermankova M, Chadwick K, Margolick J, Quinn TC, Kuo YH, Brookmeyer R, Zeiger MA, Barditch-Crovo P, Siliciano RF. 1997. Quantification of latent tissue reservoirs and total body viral load in HIV-1 infection. Nature 387:183-98
66. Chun TW, Finzi D, Margolick J, Chadwick K, Schwart D, Siliciano RF. 1995. In vivo fate of HIV-1-infected T cells: quantitative analysis of the transition to stable latency. Nature Med, 1:1284-90
67. Sanchez G, Xu X, Chermann JC, Hirsch I. 1997. Accumulation of defective viral genomes in peripheral blood mononuclear cells of human immunodeficiency virus type I-infected individuals. J. Virol. 71:2233-10
68. Brinchmann JE, Albert J, Vandal F. 1991. Few infected CD4+ T cells but a high proportion of replication-competent provirus copies in asymptomatic human immunodeficiency virus type I infection. J. Virol. 65:2019-23
69. Drinker CK, Yoffey JM. 1941. Lymphatics, lymph, and lymphoid tissue: their physiological and clinical significance. In Lymphatics, Lymph, and Lymphoid Tissue, pp. 11-18. Cambridge, MA: Harvard Univ. Press
70. Chun TW. Engel D, Berrey MM, Shea T, Corey L, Fauci AS. 1998. Early establishment of a pool of latently infected, resting CD4+ T cells during primary HIV-1 infection. Proc. Natl. Acad. Sci. USA 95: 8869-73
71. Haase AT, Stowring L, Harris JD, Traynor B, Ventura P, Peluso R, Brahic M. 1982. Visna DNA synthesis and the tempo of infection in vitro. Virology 119:399-410
72. Walker CM, Moody DJ, Stites DP, Levy JA. 1986. CD8+ lymphocytes can control HIV infection in vitro by suppressing virus replication. Science 234:1563-66
73. Pal R, Garzino Demo A, Markham PD, Burns J, Brown M, Gallo RC, DeVico AL. 1997. Inhibition of HIV-1 infection by the β-chemokine MDC. Science 278:695-98
74. Borrow P, Lewicki H, Hahn BH, Shaw GM, Oldstone MBA. 1994. Virus-specific CD8+ cytotoxic T-lymphocyte activity-associated with control of viremia in primary human immunodeficiency virus type I infection, J. Virol. 68:6103-10
75. Kannagi M, Masuda T, Hattori T, Kanoh T, Nasu K, Yamamoto N, Harada S. 1990. Interference with human immunodeficiency (HIV) replication by CD8+ T cells in peripheral blood leukocytes of asymptomatic HIV carriers in vitro. J. Virol. 64:3399 406
76. Perelson AS, Neumann AU, Markowitz M, Leonard JM, Ho DD. 1996. HIV-I dynamics in vivo: Virion clearance rate, infected cell life-span, and viral generation time. Science 271:1582-86
77. Perelson AS, Essunger P, Cao Y, Vesanen M, Hurley A, Saksela K, Markowitz M, Ho DD. 1997. Decay characteristics of HIV-1-infected compartments during combination therapy. Nature 387:188-91
78. Grossman Z. Feinberg MB, Paul WE. 1998. Multiple modes of cellular activation and virus transmission in HIV infection: a role for chronically and latently infected cells in sustaining viral replication, Proc. Natl. Acad. Sci. USA 95:6314-19
79. Cheynier R, Hanrichwark S, Hadida F, Pelletier K, Oksenhendler E, Autran B, Wain-Hobson S. 1994. HIV and T cell expansion in splenic white pulps is accompanied by infiltration of HIV-1 specific cytotoxic T lymphocytes. Cell 78:2705 14
80. Reinhart TA, Rogan MJ, Amedec AM, Murphey-Corb M, Rausch DM, Eiden LE, Haase AT. 1998. Tracking members of the simian immunodeficiency virus deltaB670 quasispecies population in vivo at single-cell resolution. J. Virol. 72:113-20
81. Spear GT, ,Sullivan BL, Landay AL, Lint TF. 1990. Neutralization of human immunodeficiency virus type I by complement occurs by viral lysis. J. Virol. 64: 5869-73
82. Smith JP, Kosco MH, Tew JG, Szakal AK. 1988. Thy-1 positive tangible body macrophages (TBM) in mouse lymph nodes. Anal. Rec. 222:380-90
83. Pomerantz RJ, Trono D, Feinberg MB, Baltimore D. 1990. Cells nonproductively infected with HIV-1 exhibit an aberrant pattern of viral RNA expression: a molecular model for latency. Cell 61:1271 -76
84. Seshamma T, Bagasra O, Trono D, Baltimore D, Pomerantz RJ. 1992. Blocked early-stage latency in the peripheral blood cells of certain individuals infected with human immunodeficiency virus type 1. Proc. Natl Acad. Sci. USA 89:10663-67
85. Pomerantz RJ, Seshamma T, Trono D. 1992. Efficient replication of human immunodeficiency virus type I requires a threshold level of Rev: potential implications for latency. J. Virol. 66:1809-13
86. Adams M, Sharmeen L, Kimpton J, Romeo JM, Garcia JV, Peterlin BM, Groudine M, Emerman M. 1994. Cellular latency in human immunodeficiency virus-infected individuals with high CD4 levels can be detected by the presence of promoter-proximal transcripts. Proc. Natl. Acad. Sci. USA 91:3862 66
87. Lafeuillade A, Poggi C, Profizi N, Tamalet C, Costes O. 1996. Human immunodeficiency virus type I kinetics in lymph nodes compared with plasma. J. Infect. Dis. 174:404-7
88. Lafeuillade A, Poggi C, Profizi N, Tamalet C, Profizi N. 1997. Human immunodeficiency virus type I dynamics in different lymphoid tissue compartments. J. Infect. Dis. 176:804-6
89. Tamalet C, Lafeuillade A, Fantini J, Poggi C, Yahi N. 1997. Quantification of HIV-1 viral load in lymphoid and blood cells: assessment during four-drug combination therapy. AIDS 11:895-901
90. Wong JK, Gunthard HF, Havlir DV, Zhang JQ, Haase AT, Ignacio CC, Kwok S, Emini E, Richman DD. 1997. Reduction of HIV-1 in blood and lymph nodes following potent antirelroviral therapy and the virologie correlates of treatment failure. Proc. Natl. Acad. Sci. USA 94:12574-79
91. Gunthard HF, Wong JK, lgnacio CC, Guatell JC, Riggs NL, Havlir DV, Richman DD. 1998. Human immunodefi-ciency virus replication and genotypic resistance in blood and lymph nodes after a year of potent antiretroviral therapy. J. Virol. 72:2422-28
92. Mackall CL, Hakim FT, Gress RE. 1997. T-cell regeneration: all repertoires are not created equal. Immunol. Today 18:245-51
93. Mackall CL, Gress RE. 1997. Thymic aging and T-cell regeneration, Immunol. Rev. 160:91-102
94. Mackall CL, Granger L, Sheard MA, Cepeda R, Cress RF. 1993. T-cell regeneration after bone marrow transplantation: differential CD45 isoform expression on thymic-derived versus thymic-independent progeny. Blood 82:2585-94
95. Steinmann GG. 1986. Changes in the human thymus during aging. Curr. Top. Pathol. 75:43-88
96. Prevot S, Audouis J, Andre-Bougaran J, Griffais R, Le Tourneau A, Fournier JG, Biebold J. 1992. Thymic pseudotumorous enlargement due to follicular hyperplasia in a human immunodeficiency virus sero-positive patient. Am. J. Clin. Pathol. 97:420-25
97. Burke AP, Anderson D, Benson W, Turnicky R, Mannan P, Liang YH, Smialek J, Virmani R. 1995. Localization of human immunodeficiency virus 1 RNA in thymic tissues from asymptomatic drug addicts. Arch. Pathol. Lab. Med. 119:36-41
98. Mackall CL, Fleisher TA, Brown MR, Andrich MP, Chen CC, Feuerstein JM, Horowitz ME, Magrath IT, Shad AT, Steinberg SM, Wexler LH, Gress RE. 1995. Age, thymopoiesis, and CD4+ T-lymphocyte regeneration after intensive chemotherapy. N. Engl. J. Med. 332:143-49
99. Lindsey JW, Hodgkinson S, Mehta R, Mitchell D, Enzmann D, Steinman L. 1994. Repeated treatment with chimeric anti-CD4 antibody in multiple sclerosis. Ann. Neurol. 36:183-89
100. Mackall CL, Fleisher TA, Brown MR, Andrich MP, Chen CC, Feuerstein IM, Magrath IT, Wexler LH, Dimitrov DS, Gress RE. 1997. Distinctions between CD8+ and CD4+ T-cell regenerative pathways result in prolonged T-cell subset imbalance after intensive chemotherapy. Blood 89:3700-7
101. Mackall CL, Hakim FT, Cress RE. 1997. Restoration of T-cell homeostasis af 1er T-cell depletion. Semin. in Immunol. 9:339-46
102. Hakim FT, Cepeda R, Kaimei S, Mackall CL, McAtee N, Zujcwski J, Cowan K. Cress RE. 1997. Constraints on CD4 recovery postehemotherapy in adults: thymic insufficiency and apoptotic decline of expanded peripheral CD4 cells. Blood 90:3789-98
103. Mackall CL, Bare CV, Granger LA, Sharrow SO, Titus JA, Gross RE. 1996. Thymic-independent T cell regeneration occurs via antigen-driven expansion of peripheral T cells resulting in a repertoire that is limited in diversity and prone to skewing. J. Immunol. 156:4609 16
104. Mackall CL, Gress RE. 1997. Pathways of T-cell regeneration in mice and humans: implications for bone marrow transplantation and immunotherapy, Immunol. Rev. 157:61-72
105. Bell EB, Sparshott SM. 1990. Interconversion of CD45R subsets of CD4 T cells in vivo. Nature 348:163-66
106. McLean AR, Michie CA. 1995. In vivo estimates of division and death rates of human T lymphocytes. Proc. Natl. Acad. Sci. USA 92:3707-11
107. Picker LJ, Treer JR, Ferguson-Darnell, Collins PA, Buck D, Terstappen LWMM. 1993. Control of lymphocyte recirculation in man. J. Immunol. 150:1105-2
108. Clegg CH, Rulffes JT, Wallace PM, Haugen HS. 1996. Regulation of an extrathymic T-cell development pathway by oncostatin M. Nature 384:261-63
109. Zheng B, Han S, Zhu Q, Goldsby R, Kelsoe G. 1996. Alternative pathways for the selection of antigen-specific peripheral T cells. Nature 384:263-66
110. Butcher EC, Picker LJ. 1996. Lymphocyte homing and homeostasis. Science 272:60-66
111. Freitas AA, Rocha BB. 1993 Lymphocyte lifespans: homeostasis, selection and competition. Immunol. Today 14:25-29
112. Kuo CT, Veselits ML, Leiden JM. 1997. LKLF: a transcriptional regulator of single-positive T cell quiescence and survival. Science 277:1986 90
113. Tanchot C, Lemonnier FA, Beramau B, Freitas AA, Rocha B. 1997. Differential requirements for survival and proliferation of CD8 naive or memory T cells. Science 276:2057-62
114. Markiewicz MA, Girao C, Opferman JT, Sun J, Hu Q, Agulnik AA, Bishop CE, Thompson CB, Ashton-Rickardt PG. 1998. Long term T cell memory requires the surface expression of selfpeptide/major histocompatibility complex molecules, Proc. Natl. Acad. Sci. USA 95:3065-70
115. Rocha B, Dautigny N, Pereira Pablo. 1989. Peripheral T lymphocytes: expansion potential and homeostatic regulation of pool sizes and CD4/CD8 ratios in vivo. Eur, J. Immunol. 19:905-1
116. Westermann J, Pabst R. 1990. Lymphocyte subsets in the blood: a diagnostic window on the lymphoid system? Immunol. Today 11:406-10
117. Pabst R. 1988. The spleen in lymphocyte migration. Immunol. Today 9:43-45
118. Fleury S, de Boer RJ, Rizzardi GP, Wolthers KC, Otto SA, Welbon CC, Graziosi C, Knabenhans C, Soudeyns H, Bart PA, Gallant S, Corpataux JM, Gillet M, Meylan P, Schnyder P, Meuwly JY, Spreen W, Glauser MP, Miedema F, Pantaleo G. 1998. Limited CD4+ T cell renewal in early HIV-1 infection: effect of highly active antirctroviral therapy. Nature Med. 4:794-801
119. Trepel F. 1974. Number and distribution of lymphocytes in man. A critical mass. Klin. Wschr.52:511-15
120. Chou CC, Gudeman V, OŌRourke S, lsacescu V, Detels R, Williams GJ, Mitsuyasu, Giorgi JV. 1994. Phenotypically defined memory CD4+ cells are not selectively decreased in chronic HIV disease. J. Acquir. Immune Defic. Syndr. 7: 665-75
121. Roederer M, Dubs JG, Anderson MT, RaJu PA, Herzenberg LA, Herzenberg LA. 1995. CD8 naive T cell counts decrease progressively in HIV-infected adults. J. Clin. Invest. 95:2061-66
122. Janossy G, Bofill M, Rowe D, Muir J, Beverlcy PCL. 1989. The tissue distribution of T lymphocytes expressing different CD45 polypcptides. J. Immunol. 66: 517-25
123. Collins JA, Schandl CA, Young KK, Vesely J, Willingham MC. 1997. Major DNA fragmentation is a late event in apoptosis. J. Histochem. Cytochem. 45:923-34
124. Rosok BI, Bostad L, Voltersvik P, Bjerknes R, Olofsson J, Asjo B, Brinchmann JE. 1996. Reduced CD4 cell counts in blood do not reflect CD4 cell depletion in tonsillar tissue in asymptomatic HIV-1 infection. AIDS 10:F35-F38
125. Rosenberg YJ, Zack PM, White BD, Papermaster SF, Elkins WR, Eddy GA, Lewis MG. 1993. Decline in the CD4+ lymphocyte population in the blood of SIV-infected macaques is not reflected in lymph nodes. AIDS Res. Hum. Retroviruses 9:639-46
126. Mosier DE. 1995. HIV results in the frame. CD4+ cell turnover. Nature 375: 193-94
127. Sprent J, Tough D. 1995. HIV results in the frame. CD4+ cell turnover. Nature 375:194
128. Grossman Z, Herberman RB. 1997. T-cell homeostasis in HIV infection is neither failing nor blind: modified cell counts reflect an adaptive response of the host. Nature Med. 3:486-90
129. Rosenberg YJ, Anderson AO, Pabst R. 1998. HIV-induced decline in blood CD4/CD8 ratios: viral killing or altered lymphocyte trafficking? Immunol. Today 19:10-17
130. Pakker NG, Notermans DW, de Boer RJ, Roos MT, de Wolf F, Hill A, Leonard JM, Danner SA, Miedema F, Schellekens PT. 1998. Biphasic kinetics of peripheral blood T cells after triple combination therapy in HIV-1 infection: a composite of redistribution and proliferation. Nature Med. 4:145-46
131. Lafeuillade A, Chouraqui M, Hittinger G, Poggi C, Delbeke E. 1997. Lymph node expansion of CD4+ lymphocytes during antiretroviral therapy. J. Infect, Dis. 176:1378-82
132. Sachsenberg N, Perelson AS, Yerly S, Schockmel GA, Leduc D, Hirschel B, Perrin L. 1998. Turnover of CD4+ and CD8+ T lymphocytes in HIV-1 infection as measured by Ki-67 antigen. J. Exp. Med. 187:1295-1303
133. Lane HC, Depper JM, Greene WC, Whalen G, Waldmann TA, Fauci AS. 1985. Qualitative analysis of immune function in patients with the acquired immunodeficiency syndrome. Evidence for a selective defect in soluble antigen recognition. N. Engl. J. Med. 313:79-84
134. Rosenzweig M, DeMaria M, Harper DM, Friedrich S, Jain RK, Johnson RP. 1998. Increased rates of CD4+ and CD8+ T lymphocyte turnover in simian immunodeficiency virus-infected macaques. Proc. Natl. Acad. Sci. USA 95:6388 93
135. Mohri H, Bonhoeffer S, Monard S, Perelson AS, Ho DD. 1998. Rapid turnover of T lymphocytes in SIV-infected rhesus macaques. Science 279:1223-27
136. Wolthers KC, Wisman GBA, Otto SA, de Roda Husman AM, Schaft N, de Wolf F, Goudsmil J, Coutinho RA, van der Zee AG, Meyaard L, Miedema F. 1996. T cell telomere length in HIV-1 infection: no evidence for increased CD4+ T cell turnover. Science 274:1543-47
137. Palmer LD, Weng N, Levine BL, June CH, Lane C, Hodes RJ. 1997. Telomere length, telomerase activity, and replicative potential in HIV infection: analysis of CD4+ and CD8+ T cells from HIV-discordant monozygotic twins. J. Exp, Med. 185:1381-86
138. Muro-Cacho CA, Pantaleo G, Fauci AS. 1995. Analysis of apoptosis in lymph nodes of HIV-infected persons. J. Immunol 154:5555-66
139. Banda NK, Bernier J, Kurahara DK, Kurrle R, Haigwood N, Sekaly RP, Finkel TH. 1992. Crosslinking CD4 by human immunodeficiency virus gpI20 primes T cells for activation-induced apoptosis, J, Exp.Med. 176:1099-106
140. Sunila I, Vaccarezza M, Pantalco G, Fauci AS, Orenstein JM. 1997. gpI20 is present on the plasma membrane of apoptotic CD4 cells prepared from lymph nodes of HIV-1-infected individuals: an immunoelectron microscopic study, AIDS 11:27-32
141. Finkel TH, Tudor Williams G, Banda NK, Cotton MF, Curiel T, Monks C, Baba TW, Ruprecht RM, Kupfer A. 1995. Apoptosis occurs predominantly in bystander cells and not in productively infected cells of HIV- and SIV-infected lymph nodes. Nature Med. 1: 129-34
142. Connors M, Kovacs JA, Krevat S, Gea Banacloche JC, Sneller MC, Flanigan M, Metcalf JA, Walker RF, Falloon J, Baseler M, Stevens R, Feuerstein T, Masur H, Lane HC. 1997. HIV infection induces changes in CD4+ T-cell phenotype and depletions within the CD4+ T-cell repertoire that are not immediately restored by antiviral or immune-based therapies. Nature Med. 3:703-4
143. Gorochov G, Neumann AU, Kereveur A, Parizot C, Li T, Katlama C, Karmochkine M, Raguin G, Autran B, Debre P. 1998. Perturbation of CD4+ and CD8+ T-cell repertoires during progression to AIDS and regulation of the CD4+ repertoire during antiviral therapy. Nature Med. 4:215-21
144. McCune JM, Loftus R, Schmidt DK, Carroll P, Webster D, Swor-Yim LB, Francis IR, Gross BH, Grant RM. 1998. High prevalence of thymic tissue in adults with human immunodeficiency virus-1 infection. J. Clin. Invest. 101:2301 8
145. Schuurman HJ, Krone WJA, Broekhuizen R, van Baarlen J, van Veen P, Goldstein AL, Huber J, Goudsmit J. 1989. The thymus in acquired immune deficiency syndrome. Am. J. Pathol. 134:1329 -38
146. Withers-Ward ES, Amado RG, Koka PS, Jamieson BD, Kaplan AH, Chen ISY, Zack JA. 1997. Transient renewal of thymopoiesis in HIV-infected human thymic implants following antiviral therapy. Nature Med. 3:1102-9
147. Linder J. 1987. The thymus gland in secondary immunodeficiency. Arch. Pathol. Lab. Med. 111:1118-22
148. Seemayer TA, Laroche AC, Russo P, Malebranche R, Arnoux E, Guerin JM, Pierre G, Dupuy JM, Gartner JG, Lapp WS, Spira TJ, Elie R. 1984. Precocious thymic involution manifest by epithelial injury in the acquired immune deficiency syndrome. Hum. Pathol. 15:469-74
149. Grody WW, Fligiel S, Nacim F. 1985. Thymus involution in the acquired immune deficiency syndrome. Am. J. Clin. Pathol. 84:85-95
150. Heitger A, Neu N, Kern H, Panzer-Grumayer ER, Greinix H, Nachbaur D, Niederwieser D, Fink FM. 1997. Essential role of the thymus to reconstitute naive (CD45RA+) T-helper cells after human allogeneic bone marrow transplantation. Blood 90:850-57
151. Bonyhadi ML, Rabin L, Salimi S, Brown DA, Kosek J, McCune JM, Kaneshima H. 1993. HIV induces thymus depletion in vivo. Nature 363:728-32
152. Jenkins M, Hanley MB, Moreno MB, Wieder E, McCune JM. 1998. Human immunodeficiency virus-1 infection interrupts thymopoiesis and multilineage hematopoiesis in vivo. Blood 91:2672-78
153. Zauli G, Re MC, Visani G, Furlini G, Mazza P, Vignoli M, La Placa M. 1992. Evidence for a human immunodeficiency virus type I-mediated suppression of uninfected hematopoietic (CD34+) cells in AIDS patients. J. Infect. Dis. 166:710-16
154. Koka PS, Fraser JK, Bryson Y, Bristol GC, Aldrovandi GM, Daar KS, Zack JA. 1998. Human immunodeficiency virus inhibits multilineage hematopoiesis in vivo. J. Virol. 72:5121-27
155. Davis BR, Schwanz DH, Marx JC, Johnson CE, Berry JM, Lyding J, Merigan TC, Zander A. 1991. Absent or rare human immunodeficiency virus infection of bone marrow stem/progenitor cells in vivo, J. Virol. 65:1985-90
156. Walthers HG, Schuitemaker H, Miedeina F. 1998. Rapid CD4+ T cell turnover in HIV-1 infection: a paradigm revisited. Immunol. Todav 19:44-48
157. Carroll L. 1871. Through the Looking-Glass. Now York: MacMillan
158. Mackall CL, Punt JA, Morgan P, FanAG, Gress RE. 1998. Thymic function in young/old chimeras: substantial thymic T cell regenerative capacity despite irreversible age-associated thymic involution. 28:1886-93