T cell immune reconstitution following lymphodepletion

Seminars in Immunology

Volumn 19, Issue 5, 2007, Pages 318-330

  Williams, Kirsten M ^a   Hakim, Frances T ^a   Gress, Ronald E ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

GVHD; Homeostatic peripheral expansion; Immune reconstitution; Immunotherapy; Lymphopenia; Thymopoiesis; Thymus

Indexed keywords

ANTINEOPLASTIC AGENT; ANTIRETROVIRUS AGENT; IMMUNOSUPPRESSIVE AGENT; INTERLEUKIN 15; INTERLEUKIN 21; INTERLEUKIN 7; KERATINOCYTE GROWTH FACTOR; T LYMPHOCYTE RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; TUMOR VACCINE;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; AGING; ALLOGENEIC STEM CELL TRANSPLANTATION; ANTINEOPLASTIC ACTIVITY; CANCER CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL MATURATION; CELLULAR IMMUNITY; CYTOKINE PRODUCTION; DISEASE COURSE; DRUG MECHANISM; DRUG MEGADOSE; GRAFT VERSUS HOST REACTION; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HOMEOSTASIS; HUMAN; IMMUNE DEFICIENCY; IMMUNE RESPONSE; LYMPHOCYTE COUNT; LYMPHOCYTE DEPLETION; LYMPHOCYTE PROLIFERATION; LYMPHOCYTOPENIA; LYMPHOCYTOPOIESIS; MELANOMA; NONHUMAN; PATHOGENESIS; REGULATORY MECHANISM; REVIEW; T LYMPHOCYTE ACTIVATION; THYMUS;

ANIMALS; CYTOKINES; CYTOTOXICITY, IMMUNOLOGIC; GRAFT VS HOST DISEASE; HOMEOSTASIS; HUMANS; INTERLEUKIN-15; INTERLEUKIN-7; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DEPLETION; LYMPHOPOIESIS; T-LYMPHOCYTES; T-LYMPHOCYTES, REGULATORY; THYMUS GLAND; TRANSFORMING GROWTH FACTOR BETA;

EID: 36549014534     PISSN: 10445323     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.smim.2007.10.004     Document Type: Review

References (145)

1. Hakim F.T., Cepeda R., Kaimei S., Mackall C.L., McAtee N., Zujewski J., et al. Constraints on CD4 recovery postchemotherapy in adults: thymic insufficiency and apoptotic decline of expanded peripheral CD4 cells. Blood 90 9 (1997) 3789-3798
2. Mackall C.L., Stein D., Fleisher T.A., Brown M.R., Hakim F.T., Bare C.V., et al. Prolonged CD4 depletion after sequential autologous peripheral blood progenitor cell infusions in children and young adults. Blood 96 2 (2000) 754-762
3. Nordoy T., Husebekk A., Aaberge I.S., Jenum P.A., Samdal H.H., Flugsrud L.B., et al. Humoral immunity to viral and bacterial antigens in lymphoma patients 4-10 years after high-dose therapy with ABMT Serological responses to revaccinations according to EBMT guidelines. Bone Marrow Transplant 28 7 (2001) 681-687
4. Small T.N., Papadopoulos E.B., Boulad F., Black P., Castro-Malaspina H., Childs B.H., et al. Comparison of immune reconstitution after unrelated and related T-cell-depleted bone marrow transplantation: effect of patient age and donor leukocyte infusions. Blood 93 2 (1999) 467-480
5. King C., Ilic A., Koelsch K., and Sarvetnick N. Homeostatic expansion of T cells during immune insufficiency generates autoimmunity. Cell 117 2 (2004) 265-277
6. Parkman R., Cohen G., Carter S.L., Weinberg K.I., Masinsin B., Guinan E., et al. Successful immune reconstitution decreases leukemic relapse and improves survival in recipients of unrelated cord blood transplantation. Biol Blood Marrow Transplant 12 9 (2006) 919-927
7. Dudley M.E., Wunderlich J.R., Robbins P.F., Yang J.C., Hwu P., Schwartzentruber D.J., et al. Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 298 5594 (2002) 850-854
8. Dummer W., Niethammer A.G., Baccala R., Lawson B.R., Wagner N., Reisfeld R.A., et al. T cell homeostatic proliferation elicits effective antitumor autoimmunity. J Clin Invest 110 2 (2002) 185-192
9. Gattinoni L., Finkelstein S.E., Klebanoff C.A., Antony P.A., Palmer D.C., Spiess P.J., et al. Removal of homeostatic cytokine sinks by lymphodepletion enhances the efficacy of adoptively transferred tumor-specific CD8+ T cells. J Exp Med 202 7 (2005) 907-912
10. Wrzesinski C., Paulos C.M., Gattinoni L., Palmer D.C., Kaiser A., Yu Z., et al. Hematopoietic stem cells promote the expansion and function of adoptively transferred antitumor CD8 T cells. J Clin Invest 117 2 (2007) 492-501
11. Mackall C.L., and Gress R.E. Pathways of T-cell regeneration in mice and humans: implications for bone marrow transplantation and immunotherapy. Immunol Rev 157 (1997) 61-72
12. Mackall C.L., Fleisher T.A., Brown M.R., Andrich M.P., Chen C.C., Feuerstein I.M., et al. Age, thymopoiesis, and CD4+ T-lymphocyte regeneration after intensive chemotherapy. N Engl J Med 332 3 (1995) 143-149
13. Mackall C.L., Granger L., Sheard M.A., Cepeda R., and Gress R.E. T-cell regeneration after bone marrow transplantation: differential CD45 isoform expression on thymic-derived versus thymic-independent progeny. Blood 82 8 (1993) 2585-2594
14. Hakim F.T., Memon S.A., Cepeda R., Jones E.C., Chow C.K., Kasten-Sportes C., et al. Age-dependent incidence, time course, and consequences of thymic renewal in adults. J Clin Invest 115 4 (2005) 930-939
15. Ge Q., Hu H., Eisen H.N., and Chen J. Different contributions of thymopoiesis and homeostasis-driven proliferation to the reconstitution of naive and memory T cell compartments. Proc Natl Acad Sci USA 99 5 (2002) 2989-2994
16. Douek D.C., Vescio R.A., Betts M.R., Brenchley J.M., Hill B.J., Zhang L., et al. Assessment of thymic output in adults after haematopoietic stem-cell transplantation and prediction of T-cell reconstitution. Lancet 355 9218 (2000) 1875-1881
17. Douek D.C., McFarland R.D., Keiser P.H., Gage E.A., Massey J.M., Haynes B.F., et al. Changes in thymic function with age and during the treatment of HIV infection. Nature 396 6712 (1998) 690-695
18. Wu C.J., Chillemi A., Alyea E.P., Orsini E., Neuberg D., Soiffer R.J., et al. Reconstitution of T-cell receptor repertoire diversity following T-cell depleted allogeneic bone marrow transplantation is related to hematopoietic chimerism. Blood 95 1 (2000) 352-359
19. Klein A.K., Patel D.D., Gooding M.E., Sempowski G.D., Chen B.J., Liu C., et al. T-Cell recovery in adults and children following umbilical cord blood transplantation. Biol Blood Marrow Transplant 7 8 (2001) 454-466
20. Lewin S.R., Heller G., Zhang L., Rodrigues E., Skulsky E., van den Brink M.R., et al. Direct evidence for new T-cell generation by patients after either T-cell-depleted or unmodified allogeneic hematopoietic stem cell transplantations. Blood 100 6 (2002) 2235-2242
21. Fredrickson G.G., and Basch R.S. Early thymic regeneration after irradiation. Dev Comp Immunol 18 3 (1994) 251-263
22. Sfikakis P.P., Gourgoulis G.M., Moulopoulos L.A., Kouvatseas G., Theofilopoulos A.N., and Dimopoulos M.A. Age-related thymic activity in adults following chemotherapy-induced lymphopenia. Eur J Clin Invest 35 6 (2005) 380-387
23. Smith K.Y., Valdez H., Landay A., Spritzler J., Kessler H.A., Connick E., et al. Thymic size and lymphocyte restoration in patients with human immunodeficiency virus infection after 48 weeks of zidovudine, lamivudine, and ritonavir therapy. J Infect Dis 181 1 (2000) 141-147
24. Teixeira L., Valdez H., McCune J.M., Koup R.A., Badley A.D., Hellerstein M.K., et al. Poor CD4 T cell restoration after suppression of HIV-1 replication may reflect lower thymic function. AIDS 15 14 (2001) 1749-1756
25. Dion M.L., Poulin J.F., Bordi R., Sylvestre M., Corsini R., Kettaf N., et al. HIV infection rapidly induces and maintains a substantial suppression of thymocyte proliferation. Immunity 21 6 (2004) 757-768
26. Fallen P.R., McGreavey L., Madrigal J.A., Potter M., Ethell M., Prentice H.G., et al. Factors affecting reconstitution of the T cell compartment in allogeneic haematopoietic cell transplant recipients. Bone Marrow Transplant 32 10 (2003) 1001-1014
27. Haynes B.F., Markert M.L., Sempowski G.D., Patel D.D., and Hale L.P. The role of the thymus in immune reconstitution in aging, bone marrow transplantation, and HIV-1 infection. Annu Rev Immunol 18 (2000) 529-560
28. Mackall C.L., Punt J.A., Morgan P., Farr A.G., and Gress R.E. Thymic function in young/old chimeras: substantial thymic T cell regenerative capacity despite irreversible age-associated thymic involution. Eur J Immunol 28 6 (1998) 1886-1893
29. Sarzotti M., Patel D.D., Li X., Ozaki D.A., Cao S., Langdon S., et al. T cell repertoire development in humans with SCID after nonablative allogeneic marrow transplantation. J Immunol 170 5 (2003) 2711-2718
30. Nordoy T., Kolstad A., Endresen P., Holte H., Kvaloy S., Kvalheim G., et al. Persistent changes in the immune system 4-10 years after ABMT. Bone Marrow Transplant 24 8 (1999) 873-878
31. Storek J., Joseph A., Espino G., Dawson M.A., Douek D.C., Sullivan K.M., et al. Immunity of patients surviving 20 to 30 years after allogeneic or syngeneic bone marrow transplantation. Blood 98 13 (2001) 3505-3512
32. Almeida A.R., Borghans J.A., and Freitas A.A. T cell homeostasis: thymus regeneration and peripheral T cell restoration in mice with a reduced fraction of competent precursors. J Exp Med 194 5 (2001) 591-599
33. Min H., Montecino-Rodriguez E., and Dorshkind K. Reduction in the developmental potential of intrathymic T cell progenitors with age. J Immunol 173 1 (2004) 245-250
34. Heng T.S., Goldberg G.L., Gray D.H., Sutherland J.S., Chidgey A.P., and Boyd R.L. Effects of castration on thymocyte development in two different models of thymic involution. J Immunol 175 5 (2005) 2982-2993
35. Talvensarri K., Clave E., Douay C., Rabian C., Garderet L., Busson M., et al. A broad T-cell repertoire diversity and an efficient thymic function indicate a favorable long-term immune reconstitution after cord blood stem cell transplantation. Blood 99 4 (2002) 1458-1464
36. Chen B.J., Cui X., Sempowski G.D., Domen J., and Chao N.J. Hematopoietic stem cell dose correlates with the speed of immune reconstitution after stem cell transplantation. Blood 103 11 (2004) 4344-4352
37. Zakrzewski J.L., Kochman A.A., Lu S.X., Terwey T.H., Kim T.D., Hubbard V.M., et al. Adoptive transfer of T-cell precursors enhances T-cell reconstitution after allogeneic hematopoietic stem cell transplantation. Nat Med 12 9 (2006) 1039-1047
38. Peschon J.J., Morrissey P.J., Grabstein K.H., Ramsdell F.J., Maraskovsky E., Gliniak B.C., et al. Early lymphocyte expansion is severely impaired in interleukin 7 receptor-deficient mice. J Exp Med 180 5 (1994) 1955-1960
39. Andrew D., and Aspinall R. Age-associated thymic atrophy is linked to a decline in IL-7 production. Exp Gerontol 37 2-3 (2002) 455-463
40. Phillips J.A., Brondstetter T.I., English C.A., Lee H.E., Virts E.L., and Thoman M.L. IL-7 gene therapy in aging restores early thymopoiesis without reversing involution. J Immunol 173 8 (2004) 4867-4874
41. Bolotin E., Smogorzewska M., Smith S., Widmer M., and Weinberg K. Enhancement of thymopoiesis after bone marrow transplant by in vivo interleukin-7. Blood 88 5 (1996) 1887-1894
42. Mackall C.L., Fry T.J., Bare C., Morgan P., Galbraith A., and Gress R.E. IL-7 increases both thymic-dependent and thymic-independent T-cell regeneration after bone marrow transplantation. Blood 97 5 (2001) 1491-1497
43. Li A., Zhang Q., Jiang J., Yuan G., Feng Y., Hao J., et al. Co-transplantation of bone marrow stromal cells transduced with IL-7 gene enhances immune reconstitution after allogeneic bone marrow transplantation in mice. Gene Ther 13 15 (2006) 1178-1187
44. Chu Y.W., Memon S.A., Sharrow S.O., Hakim F.T., Eckhaus M., Lucas P.J., et al. Exogenous IL-7 increases recent thymic emigrants in peripheral lymphoid tissue without enhanced thymic function. Blood 104 4 (2004) 1110-1119
45. Adachi Y., Tokuda N., Sawada T., and Fukumoto T. Semiquantitative detection of cytokine messages in X-irradiated and regenerating rat thymus. Radiat Res 163 4 (2005) 400-407
46. Alpdogan O., Hubbard V.M., Smith O.M., Patel N., Lu S., Goldberg G.L., et al. Keratinocyte growth factor (KGF) is required for postnatal thymic regeneration. Blood 107 6 (2006) 2453-2460
47. Rossi S., Blazar B.R., Farrell C.L., Danilenko D.M., Lacey D.L., Weinberg K.I., et al. Keratinocyte growth factor preserves normal thymopoiesis and thymic microenvironment during experimental graft-versus-host disease. Blood 100 2 (2002) 682-691
48. Rossi S.W., Jeker L.T., Ueno T., Kuse S., Keller M.P., Zuklys S., et al. Keratinocyte growth factor (KGF) enhances postnatal T-cell development via enhancements in proliferation and function of thymic epithelial cells. Blood (2007) 109
49. Napolitano L.A., Lo J.C., Gotway M.B., Mulligan K., Barbour J.D., Schmidt D., et al. Increased thymic mass and circulating naive CD4 T cells in HIV-1-infected adults treated with growth hormone. AIDS 16 8 (2002) 1103-1111
50. Savino W., Postel-Vinay M.C., Smaniotto S., and Dardenne M. The thymus gland: a target organ for growth hormone. Scand J Immunol 55 5 (2002) 442-452
51. Polgreen L., Steiner M., Dietz C.A., Manivel J.C., and Petryk A. Thymic hyperplasia in a child treated with growth hormone. Growth Horm IGF Res 17 1 (2007) 41-46
52. Olsen N.J., Olson G., Viselli S.M., Gu X., and Kovacs W.J. Androgen receptors in thymic epithelium modulate thymus size and thymocyte development. Endocrinology 142 3 (2001) 1278-1283
53. Sutherland J.S., Goldberg G.L., Hammett M.V., Uldrich A.P., Berzins S.P., Heng T.S., et al. Activation of thymic regeneration in mice and humans following androgen blockade. J Immunol 175 4 (2005) 2741-2753
54. Goldberg G.L., Sutherland J.S., Hammet M.V., Milton M.K., Heng T.S., Chidgey A.P., et al. Sex steroid ablation enhances lymphoid recovery following autologous hematopoietic stem cell transplantation. Transplantation 80 11 (2005) 1604-1613
55. Roux E., Dumont-Girard F., Starobinski M., Siegrist C.A., Helg C., Chapuis B., et al. Recovery of immune reactivity after T-cell-depleted bone marrow transplantation depends on thymic activity. Blood 96 6 (2000) 2299-2303
56. Dumont-Girard F., Roux E., van Lier R.A., Hale G., Helg C., Chapuis B., et al. Reconstitution of the T-cell compartment after bone marrow transplantation: restoration of the repertoire by thymic emigrants. Blood 92 11 (1998) 4464-4471
57. Muraro P.A., and Douek D.C. Renewing the T cell repertoire to arrest autoimmune aggression. Trends Immunol 27 2 (2006) 61-67
58. Fry T.J., and Mackall C.L. The many faces of IL-7: from lymphopoiesis to peripheral T cell maintenance. J Immunol 174 11 (2005) 6571-6576
59. Hazenberg M.D., Otto S.A., de Pauw E.S., Roelofs H., Fibbe W.E., Hamann D., et al. T-cell receptor excision circle and T-cell dynamics after allogeneic stem cell transplantation are related to clinical events. Blood 99 9 (2002) 3449-3453
60. Bellucci R., Alyea E.P., Weller E., Chillemi A., Hochberg E., Wu C.J., et al. Immunologic effects of prophylactic donor lymphocyte infusion after allogeneic marrow transplantation for multiple myeloma. Blood 99 12 (2002) 4610-4617
61. Hochberg E.P., Chillemi A.C., Wu C.J., Neuberg D., Canning C., Hartman K., et al. Quantitation of T-cell neogenesis in vivo after allogeneic bone marrow transplantation in adults. Blood 98 4 (2001) 1116-1121
62. Schluns K.S., Kieper W.C., Jameson S.C., and Lefrancois L. Interleukin-7 mediates the homeostasis of naive and memory CD8 T cells in vivo. Nat Immunol 1 5 (2000) 426-432
63. Tan J.T., Dudl E., LeRoy E., Murray R., Sprent J., Weinberg K.I., et al. IL-7 is critical for homeostatic proliferation and survival of naive T cells. Proc Natl Acad Sci USA 98 15 (2001) 8732-8737
64. Fry T.J., Christensen B.L., Komschlies K.L., Gress R.E., and Mackall C.L. Interleukin-7 restores immunity in athymic T-cell-depleted hosts. Blood 97 6 (2001) 1525-1533
65. Fry T.J., Moniuszko M., Creekmore S., Donohue S.J., Douek D.C., Giardina S., et al. IL-7 therapy dramatically alters peripheral T-cell homeostasis in normal and SIV-infected nonhuman primates. Blood 101 6 (2003) 2294-2299
66. Moniuszko M., Fry T., Tsai W.P., Morre M., Assouline B., Cortez P., et al. Recombinant interleukin-7 induces proliferation of naive macaque CD4+ and CD8+ T cells in vivo. J Virol 78 18 (2004) 9740-9749
67. Rosenberg S.A., Sportes C., Ahmadzadeh M., Fry T.J., Ngo L.T., Schwarz S.L., et al. IL-7 administration to humans leads to expansion of CD8+ and CD4+ cells but a relative decrease of CD4+ T-regulatory cells. J Immunother 29 3 (2006) 313-319
68. Li W.Q., Jiang Q., Khaled A.R., Keller J.R., and Durum S.K. Interleukin-7 inactivates the pro-apoptotic protein Bad promoting T cell survival. J Biol Chem 279 28 (2004) 29160-29166
69. Schober S.L., Kuo C.T., Schluns K.S., Lefrancois L., Leiden J.M., and Jameson S.C. Expression of the transcription factor lung Kruppel-like factor is regulated by cytokines and correlates with survival of memory T cells in vitro and in vivo. J Immunol 163 7 (1999) 3662-3667
70. Sasson S.C., Zaunders J.J., Zanetti G., King E.M., Merlin K.M., Smith D.E., et al. Increased plasma interleukin-7 level correlates with decreased CD127 and Increased CD132 extracellular expression on T cell subsets in patients with HIV-1 infection. J Infect Dis 193 4 (2006) 505-514
71. Vassena L., Proschan M., Fauci A.S., and Lusso P. Interleukin 7 reduces the levels of spontaneous apoptosis in CD4+ and CD8+ T cells from HIV-1-infected individuals. Proc Natl Acad Sci USA 104 7 (2007) 2355-2360
72. Park J.H., Yu Q., Erman B., Appelbaum J.S., Montoya-Durango D., Grimes H.L., et al. Suppression of IL7Ralpha transcription by IL-7 and other prosurvival cytokines: a novel mechanism for maximizing IL-7-dependent T cell survival. Immunity 21 2 (2004) 289-302
73. Bolotin E., Annett G., Parkman R., and Weinberg K. Serum levels of IL-7 in bone marrow transplant recipients: relationship to clinical characteristics and lymphocyte count. Bone Marrow Transplant 23 8 (1999) 783-788
74. Fry T.J., Connick E., Falloon J., Lederman M.M., Liewehr D.J., Spritzler J., et al. A potential role for interleukin-7 in T-cell homeostasis. Blood 97 10 (2001) 2983-2990
75. Kennedy M.K., Glaccum M., Brown S.N., Butz E.A., Viney J.L., Embers M., et al. Reversible defects in natural killer and memory CD8 T cell lineages in interleukin 15-deficient mice. J Exp Med 191 5 (2000) 771-780
76. Schluns K.S., Williams K., Ma A., Zheng X.X., and Lefrancois L. Cutting edge: requirement for IL-15 in the generation of primary and memory antigen-specific CD8 T cells. J Immunol 168 10 (2002) 4827-4831
77. Lodolce J.P., Boone D.L., Chai S., Swain R.E., Dassopoulos T., Trettin S., et al. IL-15 receptor maintains lymphoid homeostasis by supporting lymphocyte homing and proliferation. Immunity 9 5 (1998) 669-676
78. Yajima T., Yoshihara K., Nakazato K., Kumabe S., Koyasu S., Sad S., et al. IL-15 regulates CD8+ T cell contraction during primary infection. J Immunol 176 1 (2006) 507-515
79. Li Y., Zhi W., Wareski P., and Weng N.P. IL-15 activates telomerase and minimizes telomere loss and may preserve the replicative life span of memory CD8+ T cells in vitro. J Immunol 174 7 (2005) 4019-4024
80. Anichini A., Scarito A., Molla A., Parmiani G., and Mortarini R. Differentiation of CD8+ T cells from tumor-invaded and tumor-free lymph nodes of melanoma patients: role of common gamma-chain cytokines. J Immunol 171 4 (2003) 2134-2141
81. Cooley S., June C.H., Schoenberger S.P., and Miller J.S. Adoptive therapy with T Cells/NK Cells. Biol Blood Marrow Transplant 13 Suppl. 1 (2007) 33-42
82. Chik K.W., Li K., Pong H., Shing M.M., Li C.K., and Yuen P.M. Elevated serum interleukin-15 level in acute graft-versus-host disease after hematopoietic cell transplantation. J Pediatr Hematol Oncol 25 12 (2003) 960-964
83. Mackall C.L., Fleisher T.A., Brown M.R., Andrich M.P., Chen C.C., Feuerstein I.M., et al. Distinctions between CD8+ and CD4+ T-cell regenerative pathways result in prolonged T-cell subset imbalance after intensive chemotherapy. Blood 89 10 (1997) 3700-3707
84. Ferrari V., Cacere C.R., Machado C.M., Pannuti C.S., Dulley F.L., Barros J.C., et al. Distinct patterns of regeneration of central memory, effector memory and effector TCD8+ cell subsets after different hematopoietic cell transplant types: possible influence in the recovery of anti-cytomegalovirus immune response and risk for its reactivation. Clin Immunol 119 3 (2006) 261-271
85. Geginat J., Lanzavecchia A., and Sallusto F. Proliferation and differentiation potential of human CD8+ memory T-cell subsets in response to antigen or homeostatic cytokines. Blood 101 11 (2003) 4260-4266
86. Judge A.D., Zhang X., Fujii H., Surh C.D., and Sprent J. Interleukin 15 controls both proliferation and survival of a subset of memory-phenotype CD8(+) T cells. J Exp Med 196 7 (2002) 935-946
87. Zeng R., Spolski R., Finkelstein S.E., Oh S., Kovanen P.E., Hinrichs C.S., et al. Synergy of IL-21 and IL-15 in regulating CD8+ T cell expansion and function. J Exp Med 201 1 (2005) 139-148
88. Moroz A., Eppolito C., Li Q., Tao J., Clegg C.H., and Shrikant P.A. IL-21 enhances and sustains CD8+ T cell responses to achieve durable tumor immunity: comparative evaluation of IL-2, IL-15, and IL-21. J Immunol 173 2 (2004) 900-909
89. Lucas P.J., Kim S.J., Melby S.J., and Gress R.E. Disruption of T cell homeostasis in mice expressing a T cell-specific dominant negative transforming growth factor beta II receptor. J Exp Med 191 7 (2000) 1187-1196
90. Lucas P.J., McNeil N., Hilgenfeld E., Choudhury B., Kim S.J., Eckhaus M.A., et al. Transforming growth factor-beta pathway serves as a primary tumor suppressor in CD8+ T cell tumorigenesis. Cancer Res 64 18 (2004) 6524-6529
91. Lucas P.J., Kim S.J., Mackall C.L., Telford W.G., Chu Y.W., Hakim F.T., et al. Dysregulation of IL-15-mediated T-cell homeostasis in TGF-beta dominant-negative receptor transgenic mice. Blood 108 8 (2006) 2789-2795
92. Ahmadzadeh M., and Rosenberg S.A. TGF-beta 1 attenuates the acquisition and expression of effector function by tumor antigen-specific human memory CD8 T cells. J Immunol 174 9 (2005) 5215-5223
93. Liu W., Putnam A.L., Xu-Yu Z., Szot G.L., Lee M.R., Zhu S., et al. CD127 expression inversely correlates with FoxP3 and suppressive function of human CD4+ T reg cells. J Exp Med 203 7 (2006) 1701-1711
94. Sakaguchi S., Ono M., Setoguchi R., Yagi H., Hori S., Fehervari Z., et al. Foxp3+ CD25+ CD4+ natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol Rev 212 (2006) 8-27
95. Ku C.C., Murakami M., Sakamoto A., Kappler J., and Marrack P. Control of homeostasis of CD8+ memory T cells by opposing cytokines. Science 288 5466 (2000) 675-678
96. Kamimura D., Ueda N., Sawa Y., Hachida S., Atsumi T., Nakagawa T., et al. Evidence of a novel IL-2/15R beta-targeted cytokine involved in homeostatic proliferation of memory CD8+ T cells. J Immunol 173 10 (2004) 6041-6049
97. Kursar M., Bonhagen K., Fensterle J., Kohler A., Hurwitz R., Kamradt T., et al. Regulatory CD4+CD25+ T cells restrict memory CD8+ T cell responses. J Exp Med 196 12 (2002) 1585-1592
98. Almeida A.R., Legrand N., Papiernik M., and Freitas A.A. Homeostasis of peripheral CD4+ T cells: IL-2R alpha and IL-2 shape a population of regulatory cells that controls CD4+ T cell numbers. J Immunol 169 9 (2002) 4850-4860
99. Shen S., Ding Y., Tadokoro C.E., Olivares-Villagomez D., and Camps-Ramirez M. Control of homeostatic proliferation by regulatory T cells. J Clin Invest 115 12 (2005) 3517-3526
100. Nguyen V.H., Zeiser R., and Negrin R.S. Role of naturally arising regulatory T cells in hematopoietic cell transplantation. Biol Blood Marrow Transplant 12 10 (2006) 995-1009
101. Rezvani K., Mielke S., Ahmadzadeh M., Kilical Y., Savani B.N., Zeilah J., et al. High donor FOXP3-positive regulatory T-cell (Treg) content is associated with a low risk of GVHD following HLA-matched allogeneic SCT. Blood 108 4 (2006) 1291-1297
102. Zhang H., Chua K.S., Guimond M., Kapoor V., Brown M.V., Fleisher T.A., et al. Lymphopenia and interleukin-2 therapy alter homeostasis of CD4+CD25+ regulatory T cells. Nat Med 11 11 (2005) 1238-1243
103. Mackall C.L., Bare C.V., Granger L.A., Sharrow S.O., Titus J.A., and Gress R.E. 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 12 (1996) 4609-4616
104. Min B., McHugh R., Sempowski G.D., Mackall C., Foucras G., and Paul W.E. Neonates support lymphopenia-induced proliferation. Immunity 18 1 (2003) 131-140
105. Min B., and Paul W.E. Endogenous proliferation: burst-like CD4 T cell proliferation in lymphopenic settings. Semin Immunol 17 3 (2005) 201-207
106. Kieper W.C., Troy A., Burghardt J.T., Ramsey C., Lee J.Y., Jiang H.Q., et al. Recent immune status determines the source of antigens that drive homeostatic T cell expansion. J Immunol 174 6 (2005) 3158-3163
107. Chalandon Y., Degermann S., Villard J., Arlettaz L., Kaiser L., Vischer S., et al. Pretransplantation CMV-specific T cells protect recipients of T-cell-depleted grafts against CMV-related complications. Blood 107 1 (2006) 389-396
108. Ganepola S., Gentilini C., Hilbers U., Lange T., Rieger K., Hofmann J., et al. Patients at high risk for CMV infection and disease show delayed CD8+ T-cell immune recovery after allogeneic stem cell transplantation. Bone Marrow Transplant 39 5 (2007) 293-299
109. Peggs K.S., Verfuerth S., Pizzey A., Khan N., Moss P., Goldstone A.H., et al. Reconstitution of T-cell repertoire after autologous stem cell transplantation: influence of CD34 selection and cytomegalovirus infection. Biol Blood Marrow Transplant 9 3 (2003) 198-205
110. Ma J., Urba W.J., Si L., Wang Y., Fox B.A., and Hu H.M. Anti-tumor T cell response and protective immunity in mice that received sublethal irradiation and immune reconstitution. Eur J Immunol 33 8 (2003) 2123-2132
111. Borrello I., Sotomayor E.M., Rattis F.M., Cooke S.K., Gu L., and Levitsky H.I. Sustaining the graft-versus-tumor effect through posttransplant immunization with granulocyte-macrophage colony-stimulating factor (GM-CSF)-producing tumor vaccines. Blood 95 10 (2000) 3011-3019
112. Antony P.A., Paulos C.M., Ahmadzadeh M., Akpinarli A., Palmer D.C., Sato N., et al. Interleukin-2-dependent mechanisms of tolerance and immunity in vivo. J Immunol 176 9 (2006) 5255-5266
113. Kochenderfer J.N., Chien C.D., Simpson J.L., and Gress R.E. Synergism between CpG-containing oligodeoxynucleotides and IL-2 causes dramatic enhancement of vaccine-elicited CD8+ T cell responses. J Immunol 177 12 (2006) 8860-8873
114. Pasare C., and Medzhitov R. Toll pathway-dependent blockade of CD4+CD25+ T cell-mediated suppression by dendritic cells. Science 299 5609 (2003) 1033-1036
115. Oh S., Berzofsky J.A., Burke D.S., Waldmann T.A., and Perera L.P. Coadministration of HIV vaccine vectors with vaccinia viruses expressing IL-15 but not IL-2 induces long-lasting cellular immunity. Proc Natl Acad Sci USA 100 6 (2003) 3392-3397
116. Di Carlo E., Comes A., Orengo A.M., Rosso O., Meazza R., Musiani P., et al. IL-21 induces tumor rejection by specific CTL and IFN-gamma-dependent CXC chemokines in syngeneic mice. J Immunol 172 3 (2004) 1540-1547
117. Dudley M.E., Wunderlich J.R., Yang J.C., Sherry R.M., Topalian S.L., Restifo N.P., et al. Adoptive cell transfer therapy following non-myeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma. J Clin Oncol 23 10 (2005) 2346-2357
118. Robbins P.F., Dudley M.E., Wunderlich J., El-Gamil M., Li Y.F., Zhou J., et al. Cutting edge: persistence of transferred lymphocyte clonotypes correlates with cancer regression in patients receiving cell transfer therapy. J Immunol 173 12 (2004) 7125-7130
119. Shen X., Zhou J., Hathcock K.S., Robbins P., Powell Jr. D.J., Rosenberg S.A., et al. Persistence of tumor infiltrating lymphocytes in adoptive immunotherapy correlates with telomere length. J Immunother 30 1 (2007) 123-129
120. Ahmadzadeh M., and Rosenberg S.A. IL-2 administration increases CD4+ CD25(hi) Foxp3+ regulatory T cells in cancer patients. Blood 107 6 (2006) 2409-2414
121. Morgan R.A., Dudley M.E., Wunderlich J.R., Hughes M.S., Yang J.C., Sherry R.M., et al. Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 314 5796 (2006) 126-129
122. Hakim F.T., and Mackall C. Immunopathogenesis of graft vs host disease. In: Ferrara J., and Burakoff A. (Eds). Graft-versus-host disease (1996), Marcel Dekker, New York 257-289
123. Muluk S.C., Hakim F.T., and Shearer G.M. Regulation of graft-versus-host-reaction by Mlsa-reactive donor T cells. Eur J Immunol 22 8 (1992) 1967-1973
124. van den Brink M.R., Moore E., Ferrara J.L., and Burakoff S.J. Graft-versus-host-disease-associated thymic damage results in the appearance of T cell clones with anti-host reactivity. Transplantation 69 3 (2000) 446-449
125. Hakim F.T., Sharrow S.O., Payne S., and Shearer G.M. Repopulation of host lymphohematopoietic systems by donor cells during graft-versus-host reaction in unirradiated adult F1 mice injected with parental lymphocytes. J Immunol 146 7 (1991) 2108-2115
126. Sinha M.L., Fry T.J., Fowler D.H., Miller G., and Mackall C.L. Interleukin 7 worsens graft-versus-host disease. Blood 100 7 (2002) 2642-2649
127. Alpdogan O., Schmaltz C., Muriglan S.J., Kappel B.J., Perales M.A., Rotolo J.A., et al. Administration of interleukin-7 after allogeneic bone marrow transplantation improves immune reconstitution without aggravating graft-versus-host disease. Blood 98 7 (2001) 2256-2265
128. Gendelman M., Hecht T., Logan B., Vodanovic-Jankovic S., Komorowski R., and Drobyski W.R. Host conditioning is a primary determinant in modulating the effect of IL-7 on murine graft-versus-host disease. J Immunol 172 5 (2004) 3328-3336
129. Blaser B.W., Roychowdhury S., Kim D.J., Schwind N.R., Bhatt D., Yuan W., et al. Donor-derived IL-15 is critical for acute allogeneic graft-versus-host disease. Blood 105 2 (2005) 894-901
130. Alpdogan O., Eng J.M., Muriglan S.J., Willis L.M., Hubbard V.M., Tjoe K.H., et al. Interleukin-15 enhances immune reconstitution after allogeneic bone marrow transplantation. Blood 105 2 (2005) 865-873
131. Roychowdhury S., Blaser B.W., Freud A.G., Katz K., Bhatt D., Ferketich A.K., et al. IL-15 but not IL-2 rapidly induces lethal xenogeneic graft-versus-host disease. Blood 106 7 (2005) 2433-2435
132. Kumaki S., Minegishi M., Fujie H., Sasahara Y., Ohashi Y., Tsuchiya S., et al. Prolonged secretion of IL-15 in patients with severe forms of acute graft-versus-host disease after allogeneic bone marrow transplantation in children. Int J Hematol 67 3 (1998) 307-312
133. Via C.S., Shanley J.D., and Shearer G.M. Synergistic effect of murine cytomegalovirus on the induction of acute graft-vs.-host disease involving MHC class I differences only. Analysis of in vitro T cell function. J Immunol 145 10 (1990) 3283-3289
134. Levy R.B., Jones M., and Cray C. HSV-1 enhances GvHR-associated parent anti-F1 alloreactivity in vivo and in vitro. Cell Immunol 129 1 (1990) 1-12
135. Trenado A., Sudres M., Tang Q., Maury S., Charlotte F., Gregoire S., et al. Ex vivo-expanded CD4+CD25+ immunoregulatory T cells prevent graft-versus-host-disease by inhibiting activation/differentiation of pathogenic T cells. J Immunol 176 2 (2006) 1266-1273
136. Taylor P.A., Lees C.J., and Blazar B.R. The infusion of ex vivo activated and expanded CD4(+)CD25(+) immune regulatory cells inhibits graft-versus-host disease lethality. Blood 99 10 (2002) 3493-3499
137. Nguyen V.H., Zeiser R., Dasilva D.L., Chang D.S., Beilhack A., Contag C.H., et al. In vivo dynamics of regulatory T-cell trafficking and survival predict effective strategies to control graft-versus-host disease following allogeneic transplantation. Blood 109 6 (2007) 2649-2656
138. Hollander G.A., Widmer B., and Burakoff S.J. Loss of normal thymic repertoire selection and persistence of autoreactive T cells in graft vs. host disease. J Immunol 152 4 (1994) 1609-1617
139. Desbarats J., and Lapp W.S. Thymic selection and thymic major histocompatibility complex class II expression are abnormal in mice undergoing graft-versus-host reactions. J Exp Med 178 3 (1993) 805-814
140. Ghayur T., Seemayer T.A., Xenocostas A., and Lapp W.S. Complete sequential regeneration of graft-vs.-host-induced severely dysplastic thymuses. Implications for the pathogenesis of chronic graft-vs.-host disease. Am J Pathol 133 1 (1988) 39-46
141. Hauri-Hohl M.M., Keller M.P., Gill J., Hafen K., Pachlatko E., Boulay T., et al. Donor T-cell alloreactivity against host thymic epithelium limits T-cell development after bone marrow transplantation. Blood 109 9 (2007) 4080-4088
142. Watanabe N., Wang Y.H., Lee H.K., Ito T., Wang Y.H., Cao W., et al. Hassall's corpuscles instruct dendritic cells to induce CD4+CD25+ regulatory T cells in human thymus. Nature 436 7054 (2005) 1181-1185
143. Jimenez M., Martinez C., Ercilla G., Carreras E., Urbano-Ispizua A., Aymerich M., et al. Clinical factors influencing T-cell receptor excision circle (TRECs) counts following allogeneic stem cell transplantation in adults. Transpl Immunol 16 1 (2006) 52-59
144. Weinberg K., Blazar B.R., Wagner J.E., Agura E., Hill B.J., Smogorzewska M., et al. Factors affecting thymic function after allogeneic hematopoietic stem cell transplantation. Blood 97 5 (2001) 1458-1466
145. Olkinuora H., Talvensaari K., Kaartinen T., Siitonen S., Saarinen-Pihkala U., Partanen J., et al. T cell regeneration in pediatric allogeneic stem cell transplantation. Bone Marrow Transplant 39 3 (2007) 149-156