Experimental Hematology
Volume 38, Issue 3 , Pages 222-232.e2 , March 2010

Auto-reconstitution of the T-cell compartment by radioresistant hematopoietic cells following lethal irradiation and bone marrow transplantation

  • Nabil Bosco

      Affiliations

    • Department of Biomedicine, Group of Developmental and Molecular Immunology, University of Basel, Basel, Switzerland
  • ,
  • Lee Kim Swee

      Affiliations

    • Department of Biomedicine, Group of Developmental and Molecular Immunology, University of Basel, Basel, Switzerland
  • ,
  • Angèle Bénard

      Affiliations

    • Department of Biomedicine, Group of Developmental and Molecular Immunology, University of Basel, Basel, Switzerland
  • ,
  • Rhodri Ceredig

      Affiliations

    • Department of Biomedicine, Group of Developmental and Molecular Immunology, University of Basel, Basel, Switzerland
    • REMEDI, NCBES, Department of Physiology, National University of Galway, Ireland
  • ,
  • Antonius Rolink

      Affiliations

    • Department of Biomedicine, Group of Developmental and Molecular Immunology, University of Basel, Basel, Switzerland
    • Corresponding Author InformationOffprint requests to: Antonius Rolink, Ph.D., Department of Biomedicine, Group of Developmental and Molecular Immunology, University of Basel, Mattenstrasse 28, 4058 Basel, Switzerland

Received 7 September 2009 ,Revised 24 November 2009 ,Accepted 23 December 2009.

References 

  1. Gress RE, Komanduri KV, Einsele H, Cooper LJ. Lymphoid reconstruction and vaccines. Biol Blood Marrow Transplant. 2007;13:17–22
  2. Hakim FT, Gress RE. Reconstitution of the lymphocyte compartment after lymphocyte depletion: a key issue in clinical immunology. Eur J Immunol. 2005;35:3099–3102
  3. Chalandon Y, Degermann S, Villard J, et al. Pretransplantation CMV-specific T cells protect recipients of T-cell-depleted grafts against CMV-related complications. Blood. 2006;107:389–396
  4. Benard A, Ceredig R, Rolink AG. Regulatory T cells control autoimmunity following syngeneic bone marrow transplantation. Eur J Immunol. 2006;36:2324–2335
  5. Anderson BE, McNiff JM, Matte C, Athanasiadis I, Shlomchik WD, Shlomchik MJ. Recipient CD4+ T cells that survive irradiation regulate chronic graft-versus-host disease. Blood. 2005;104:1565–1573
  6. Komatsu N, Hori S. Full restoration of peripheral Foxp3+ regulatory T cell pool by radioresistant host cells in scurfy bone marrow chimeras. Proc Natl Acad Sci U S A. 2007;104:8959–8964
  7. Schleussner C, Ceredig R. Analysis of intraepithelial lymphocytes from major histocompatibility complex (MHC)-deficient mice: no evidence for a role of MHC class II antigens in the positive selection of V delta 4+ gamma delta T cells. Eur J Immunol. 1993;23:1615–1622
  8. Bosco N, Agenes F, Ceredig R. Effects of increasing IL-7 availability on lymphocytes during and after lymphopenia-induced proliferation. J Immunol. 2005;175:162–170
  9. Bosco N, Agenes F, Rolink AG, Ceredig R. Peripheral T cell lymphopenia and concomitant enrichment in naturally arising regulatory T cells: the case of the pre-Talpha gene-deleted mouse. J Immunol. 2006;177:5014–5023
  10. Balciunaite G, Ceredig R, Rolink AG. The earliest subpopulation of mouse thymocytes contains potent T, significant macrophage, and natural killer cell but no B-lymphocyte potential. Blood. 2005;105:1930–1936
  11. Balciunaite G, Ceredig R, Fehling HJ, Zuniga-Pflucker JC, Rolink AG. The role of Notch and IL-7 signaling in early thymocyte proliferation and differentiation. Eur J Immunol. 2005;35:1292–1300
  12. Bosco N, Ceredig R, Rolink A. Transient decrease in interleukin-7 availability arrests B lymphopoiesis during pregnancy. Eur J Immunol. 2008;38:381–390
  13. Ceredig R, Rauch M, Balciunaite G, Rolink AG. Increasing Flt3L availability alters composition of a novel bone marrow lymphoid progenitor compartment. Blood. 2006;108:1216–1222
  14. Tough DF, Sprent J. Turnover of naive- and memory-phenotype T cells. J Exp Med. 1994;179:1127–1135
  15. Penit C, Ezine S. Cell proliferation and thymocyte subset reconstitution in sublethally irradiated mice: compared kinetics of endogenous and intrathymically transferred progenitors. Proc Natl Acad Sci U S A. 1989;86:5547–5551
  16. Ceredig R, MacDonald HR. Phenotypic and functional properties of murine thymocytes. II. Quantitation of host- and donor-derived cytolytic T lymphocyte precursors in regenerating radiation bone marrow chimeras. J Immunol. 1982;128:614–620
  17. Kadish JL, Basch RS. Thymic regeneration after lethal irradiation evidence for an intra-thymic radioresistant T cell precursor. J Immunol. 1975;114:452–458
  18. Sharrow SO, Singer A, Hammerling U, Mathieson BJ. Phenotypic characterization of early events of thymus repopulation in radiation bone marrow chimeras. Transplantation. 1983;35:355–362
  19. Maillard I, Schwarz BA, Sambandam A, et al. Notch-dependent T-lineage commitment occurs at extrathymic sites following bone marrow transplantation. Blood. 2006;107:3511–3519
  20. Domen J, Gandy KL, Weissman IL. Systemic overexpression of BCL-2 in the hematopoietic system protects transgenic mice from the consequences of lethal irradiation. Blood. 1998;91:2272–2282
  21. Roord ST, de Jager W, Boon L, et al. Autologous bone marrow transplantation in autoimmune arthritis restores immune homeostasis through CD4+CD25+Foxp3+ regulatory T cells. Blood. 2008;111:5233–5241
  22. Bayer AL, Jones M, Chirinos J, et al. Host CD4+CD25+ T cells can expand and comprise a major component of the Treg compartment after experimental HCT. Blood. 2009;113:733–743
  23. Bourgeois C, Stockinger B. CD25+CD4+ regulatory T cells and memory T cells prevent lymphopenia-induced proliferation of naive T cells in transient states of lymphopenia. J Immunol. 2006;177:4558–4566
  24. Gladstone DE, Golightly MG, Brannagan TH. High dose cyclophosphamide preferentially targets naive T (CD45/CD4/RA+) cells in CIDP and MS patients. J Neuroimmunol. 2007;190:121–126
  25. Walzer T, Arpin C, Beloeil L, Marvel J. Differential in vivo persistence of two subsets of memory phenotype CD8 T cells defined by CD44 and CD122 expression levels. J Immunol. 2002;168:2704–2711
  26. Avigan D, Pirofski LA, Lazarus HM. Vaccination against infectious disease following hematopoietic stem cell transplantation. Biol Blood Marrow Transplant. 2001;7:171–183
  27. Gangappa S, Kokko KE, Carlson LM, et al. Immune responsiveness and protective immunity after transplantation. Transpl Int. 2001;21:293–303
  28. Ljungman P, Engelhard D, de la Camara R, et al. Vaccination of stem cell transplant recipients: recommendations of the Infectious Diseases Working Party of the EBMT. Bone Marrow Transplant. 2005;35:737–746
  29. Parkman R. Antigen-specific immunity following hematopoietic stem cell transplantation. Blood Cells Mol Dis. 2008;40:91–93
  30. Patel SR, Ortin M, Cohen BJ, et al. Revaccination with measles, tetanus, poliovirus, Haemophilus influenzae type B, meningococcus C, and pneumococcus vaccines in children after hematopoietic stem cell transplantation. Clin Infect Dis. 2007;44:625–634
  31. Bredemeyer AL, Helmink BA, Innes CL, et al. DNA double-strand breaks activate a multi-functional genetic program in developing lymphocytes. Nature. 2008;456:819–823
  32. Jeggo PA, Lobrich M. Contribution of DNA repair and cell cycle checkpoint arrest to the maintenance of genomic stability. DNA Repair (Amst). 2006;5:1192–1198
  33. Lobrich M, Jeggo PA. The impact of a negligent G2/M checkpoint on genomic instability and cancer induction. Nat Rev Cancer. 2007;7:861–869
  34. Pawlik TM, Keyomarsi K. Role of cell cycle in mediating sensitivity to radiotherapy. Int J Radiat Oncol Biol Phys. 2004;59:928–942
  35. Burdelya LG, Krivokrysenko VI, Tallant TC, et al. An agonist of toll-like receptor 5 has radioprotective activity in mouse and primate models. Science. 2008;320:226–230
  36. Akiyama M. Late effects of radiation on the human immune system: an overview of immune response among the atomic-bomb survivors. Int J Radiat Biol. 1995;68:497–508
  37. Michie CA, McLean A, Alcock C, Beverley PC. Lifespan of human lymphocyte subsets defined by CD45 isoforms. Nature. 1992;360:264–265
  38. Boyman O, Ramsey C, Kim DM, Sprent J, Surh CD. IL-7/Anti-IL-7 mAb complexes restore T cell development and induce homeostatic T cell expansion without lymphopenia. J Immunol. 2008;180:7265–7275

PII: S0301-472X(09)00487-1

doi: 10.1016/j.exphem.2009.12.006

Experimental Hematology
Volume 38, Issue 3 , Pages 222-232.e2 , March 2010