Home LiteratureArticle Details
PMID: 15776111 Published · ppublish English Journal Article

Age-dependent incidence, time course, and consequences of thymic renewal in adults.

The Journal of clinical investigation ·Vol. 115 ·No. 4 ·2005-04-00 ·Pages 930-9

Hakim FT, Memon SA, Cepeda R, Jones EC, Chow CK, Kasten-Sportes C, Odom J, Vance BA, Christensen BL, Mackall CL, Gress RE

Abstract

Homeostatic regulation of T cells involves an ongoing balance of new T cell generation, peripheral expansion, and turnover. The recovery of T cells when this balance is disrupted provides insight into the mechanisms that govern homeostasis. In a long-term, single cohort study, we assessed the role of thymic function after autologous transplant in adults, correlating serial computed tomography imaging of thymic size with concurrent measurements of peripheral CD4(+) T cell populations. We established the age-dependent incidence, time course, and duration of thymic enlargement in adults and demonstrated that these changes were correlated with peripheral recovery of naive CD45RA(+)CD62L(+) and signal-joint TCR rearrangement excision circle-bearing CD4(+) populations with broad TCR diversity. Furthermore, we demonstrated that renewed thymopoiesis was critical for the restoration of peripheral CD4(+) T cell populations. This recovery encompassed the recovery of normal CD4(+) T cell numbers, a low ratio of effector to central memory cells, and a broad repertoire of TCR Vbeta diversity among these memory cells. These data define the timeline and consequences of renewal of adult thymopoietic activity at levels able to quantitatively restore peripheral T cell populations. They further suggest that structural thymic regrowth serves as a basis for the regeneration of peripheral T cell populations.

MeSH Terms
Adult Age Factors Aged Breast Neoplasms/pathology CD4-Positive T-Lymphocytes/physiology Cohort Studies Female Homeostasis Humans Leukocyte Common Antigens/metabolism Middle Aged Receptors, Antigen, T-Cell/genetics,metabolism Statistics as Topic Thymus Gland/cytology,physiology,transplantation Time Factors Transplantation, Autologous
Chemicals
Receptors, Antigen, T-Cell Leukocyte Common Antigens
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Hakim Frances T
Experimental Transplantation and Immunology Branch, National Cancer Institute, NIH, Bethesda, Maryland 20892, USA. fhakim@helix.nih.gov
Memon Sarfraz A
Cepeda Rosemarie
Jones Elizabeth C
Chow Catherine K
Kasten-Sportes Claude
Odom Jeanne
Vance Barbara A
Christensen Barbara L
Mackall Crystal L
Gress Ronald E
References (60)
60 references, click to expand
  1. Stepwise development of thymic microenvironments in vivo is regulated by thymocyte subsets.
    Development. 2000 Apr;127(8):1583-91 PMID: 10725235
  2. Constraints on CD4 recovery postchemotherapy in adults: thymic insufficiency and apoptotic decline of expanded peripheral CD4 cells.
    Blood. 1997 Nov 1;90(9):3789-98 PMID: 9345067
  3. The role of the thymus in immune reconstitution in aging, bone marrow transplantation, and HIV-1 infection.
    Annu Rev Immunol. 2000;18:529-60 PMID: 10837068
  4. Increased apoptosis of peripheral blood T cells following allogeneic hematopoietic cell transplantation.
    Blood. 2000 Jun 15;95(12):3832-9 PMID: 10845917
  5. Longitudinal monitoring of immune reconstitution by CDR3 size spectratyping after T-cell-depleted allogeneic bone marrow transplant and the effect of donor lymphocyte infusions on T-cell repertoire.
    Blood. 2000 Jun 15;95(12):3990-5 PMID: 10845939
  6. Assessment of thymic output in adults after haematopoietic stem-cell transplantation and prediction of T-cell reconstitution.
    Lancet. 2000 May 27;355(9218):1875-81 PMID: 10866444
  7. Prolonged CD4 depletion after sequential autologous peripheral blood progenitor cell infusions in children and young adults.
    Blood. 2000 Jul 15;96(2):754-62 PMID: 10887145
  8. Naive T cells transiently acquire a memory-like phenotype during homeostasis-driven proliferation.
    J Exp Med. 2000 Aug 21;192(4):557-64 PMID: 10952725
  9. Il-7 and not stem cell factor reverses both the increase in apoptosis and the decline in thymopoiesis seen in aged mice.
    J Immunol. 2001 Feb 1;166(3):1524-30 PMID: 11160192
  10. Thymic hyperplasia after high-dose chemotherapy and autologous stem cell transplantation: incidence and significance in patients with breast cancer.
    AJR Am J Roentgenol. 1999 Nov;173(5):1341-4 PMID: 10541115
  11. Thymic size and lymphocyte restoration in patients with human immunodeficiency virus infection after 48 weeks of zidovudine, lamivudine, and ritonavir therapy.
    J Infect Dis. 2000 Jan;181(1):141-7 PMID: 10608760
  12. Leukemia inhibitory factor, oncostatin M, IL-6, and stem cell factor mRNA expression in human thymus increases with age and is associated with thymic atrophy.
    J Immunol. 2000 Feb 15;164(4):2180-7 PMID: 10657672
  13. High prevalence of thymic tissue in adults with human immunodeficiency virus-1 infection.
    J Clin Invest. 1998 Jun 1;101(11):2301-8 PMID: 9616201
  14. Thymic function in young/old chimeras: substantial thymic T cell regenerative capacity despite irreversible age-associated thymic involution.
    Eur J Immunol. 1998 Jun;28(6):1886-93 PMID: 9645370
  15. Interdependence of cortical thymic epithelial cell differentiation and T-lineage commitment.
    Proc Natl Acad Sci U S A. 1998 Sep 29;95(20):11822-7 PMID: 9751749
  16. Reconstitution of the T-cell compartment after bone marrow transplantation: restoration of the repertoire by thymic emigrants.
    Blood. 1998 Dec 1;92(11):4464-71 PMID: 9834254
  17. Changes in thymic function with age and during the treatment of HIV infection.
    Nature. 1998 Dec 17;396(6712):690-5 PMID: 9872319
  18. Development, organization and function of the thymic medulla in normal, immunodeficient or autoimmune mice.
    Semin Immunol. 1999 Feb;11(1):47-55 PMID: 9950751
  19. Immune reconstitution after bone marrow transplantation for combined immunodeficiencies: down-modulation of Bcl-2 and high expression of CD95/Fas account for increased susceptibility to spontaneous and activation-induced lymphocyte cell death.
    Bone Marrow Transplant. 1999 Mar;23(5):451-7 PMID: 10100558
  20. Serum levels of IL-7 in bone marrow transplant recipients: relationship to clinical characteristics and lymphocyte count.
    Bone Marrow Transplant. 1999 Apr;23(8):783-8 PMID: 10231140
  21. Generation of functional thymocytes in the human adult.
    Immunity. 1999 May;10(5):569-75 PMID: 10367902
  22. Persistent changes in the immune system 4-10 years after ABMT.
    Bone Marrow Transplant. 1999 Oct;24(8):873-8 PMID: 10516699
  23. Age-related change in the potential of bone marrow cells to repopulate the thymus and splenic T cells in mice.
    Cell Immunol. 1986 Jul;100(2):443-51 PMID: 3530503
  24. Evidence for thymic function in the elderly.
    Vaccine. 2000 Feb 25;18(16):1638-41 PMID: 10689141
  25. Factors affecting thymic function after allogeneic hematopoietic stem cell transplantation.
    Blood. 2001 Mar 1;97(5):1458-66 PMID: 11222394
  26. Interleukin-7 restores immunity in athymic T-cell-depleted hosts.
    Blood. 2001 Mar 15;97(6):1525-33 PMID: 11238086
  27. The human thymus during aging.
    Immunol Res. 2000;22(2-3):253-61 PMID: 11339360
  28. A potential role for interleukin-7 in T-cell homeostasis.
    Blood. 2001 May 15;97(10):2983-90 PMID: 11342421
  29. T-Cell recovery in adults and children following umbilical cord blood transplantation.
    Biol Blood Marrow Transplant. 2001;7(8):454-66 PMID: 11569891
  30. Administration of interleukin-7 after allogeneic bone marrow transplantation improves immune reconstitution without aggravating graft-versus-host disease.
    Blood. 2001 Oct 1;98(7):2256-65 PMID: 11568014
  31. Evidence for increased T cell turnover and decreased thymic output in HIV infection.
    J Immunol. 2001 Dec 1;167(11):6663-8 PMID: 11714838
  32. Cytokine-driven proliferation and differentiation of human naive, central memory, and effector memory CD4(+) T cells.
    J Exp Med. 2001 Dec 17;194(12):1711-9 PMID: 11748273
  33. Age-associated thymic atrophy is linked to a decline in IL-7 production.
    Exp Gerontol. 2002 Jan-Mar;37(2-3):455-63 PMID: 11772533
  34. 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. 2002 Feb 15;99(4):1458-64 PMID: 11830500
  35. T-cell receptor excision circle and T-cell dynamics after allogeneic stem cell transplantation are related to clinical events.
    Blood. 2002 May 1;99(9):3449-53 PMID: 11964316
  36. Current concepts of thymic aging.
    Springer Semin Immunopathol. 2002;24(1):7-22 PMID: 11974583
  37. Association between larger thymic size and higher thymic output in human immunodeficiency virus-infected patients receiving highly active antiretroviral therapy.
    J Infect Dis. 2002 Jun 1;185(11):1578-85 PMID: 12023763
  38. Molecular characterization of the mouse involuted thymus: aberrations in expression of transcription regulators in thymocyte and epithelial compartments.
    Int Immunol. 2002 Jul;14(7):813-22 PMID: 12096041
  39. Direct evidence for new T-cell generation by patients after either T-cell-depleted or unmodified allogeneic hematopoietic stem cell transplantations.
    Blood. 2002 Sep 15;100(6):2235-42 PMID: 12200390
  40. Changes in thymus volume in adult HIV-infected patients under HAART: correlation with the T-cell repopulation.
    Clin Exp Immunol. 2002 Oct;130(1):121-6 PMID: 12296862
  41. Proliferation and differentiation potential of human CD8+ memory T-cell subsets in response to antigen or homeostatic cytokines.
    Blood. 2003 Jun 1;101(11):4260-6 PMID: 12576317
  42. Identification of non-naïve CD4+CD45RA+ T cell subsets in adult allogeneic haematopoietic cell transplant recipients.
    Bone Marrow Transplant. 2003 Sep;32(6):609-16 PMID: 12953134
  43. Early reconstitution of the T-cell repertoire after non-myeloablative peripheral blood stem cell transplantation is from post-thymic T-cell expansion and is unaffected by graft-versus-host disease or mixed chimaerism.
    Br J Haematol. 2003 Sep;122(6):934-43 PMID: 12956764
  44. Comparison of thymic function-related markers to predict early CD4 T-cell repopulation in adult HIV-infected patients on HAART.
    Antivir Ther. 2003 Aug;8(4):289-94 PMID: 14518697
  45. Factors affecting reconstitution of the T cell compartment in allogeneic haematopoietic cell transplant recipients.
    Bone Marrow Transplant. 2003 Nov;32(10):1001-14 PMID: 14595388
  46. Increases in CD4+ T lymphocytes occur without increases in thymic size in HIV-infected subjects receiving interleukin-2 therapy.
    J Acquir Immune Defic Syndr. 2003 Nov 1;34(3):299-303 PMID: 14600575
  47. Evidence for adequate thymic function but impaired naive T-cell survival following allogeneic hematopoietic stem cell transplantation in the absence of chronic graft-versus-host disease.
    Blood. 2003 Dec 15;102(13):4600-7 PMID: 12933579
  48. Age-related changes in lymphocyte development and function.
    Nat Immunol. 2004 Feb;5(2):133-9 PMID: 14749784
  49. Central memory and effector memory T cell subsets: function, generation, and maintenance.
    Annu Rev Immunol. 2004;22:745-63 PMID: 15032595
  50. Regulation of thymus size by competition for stromal niches among early T cell progenitors.
    J Immunol. 2004 Aug 1;173(3):1604-11 PMID: 15265888
  51. Exogenous IL-7 increases recent thymic emigrants in peripheral lymphoid tissue without enhanced thymic function.
    Blood. 2004 Aug 15;104(4):1110-9 PMID: 15130942
  52. In vitro analysis of age-related changes in the developmental potential of bone marrow thymocyte progenitors.
    Eur J Immunol. 1990 Dec;20(12):2541-6 PMID: 1980109
  53. T-cell regeneration after bone marrow transplantation: differential CD45 isoform expression on thymic-derived versus thymic-independent progeny.
    Blood. 1993 Oct 15;82(8):2585-94 PMID: 7691265
  54. Turnover of naive- and memory-phenotype T cells.
    J Exp Med. 1994 Apr 1;179(4):1127-35 PMID: 8145034
  55. Circulating T cell repertoire complexity in normal individuals and bone marrow recipients analyzed by CDR3 size spectratyping. Correlation with immune status.
    J Immunol. 1994 May 15;152(10):5109-19 PMID: 8176227
  56. Age, thymopoiesis, and CD4+ T-lymphocyte regeneration after intensive chemotherapy.
    N Engl J Med. 1995 Jan 19;332(3):143-9 PMID: 7800006
  57. 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. 1996 Jun 15;156(12):4609-16 PMID: 8648103
  58. Enhancement of thymopoiesis after bone marrow transplant by in vivo interleukin-7.
    Blood. 1996 Sep 1;88(5):1887-94 PMID: 8781449
  59. Expanded CD4+ and CD8+ T cell clones in elderly humans.
    J Immunol. 1997 May 1;158(9):4493-9 PMID: 9127016
  60. Changes in T cell receptor repertoire associated with graft-versus-tumor effect and graft-versus-host disease in patients with relapsed multiple myeloma after donor lymphocyte infusion.
    Bone Marrow Transplant. 2000 Mar;25(6):623-32 PMID: 10734296
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
0021-9738
Published
2005-04-00
Epub
2005-00-17
Pages
930-9
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC1064981
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com