Simultaneous quantification of recent thymic T-cell and bone marrow B-cell emigrants in patients with primary immunodeficiency undergone to stem cell transplantation

Clinical Immunology

Volumn 136, Issue 2, 2010, Pages 217-227

  Sottini, Alessandra ^a   Ghidini, Claudia ^a   Zanotti, Cinzia ^a   Chiarini, Marco ^a   Caimi, Luigi ^a   Lanfranchi, Arnalda ^b   Moratto, Daniele ^c   Porta, Fulvio ^b   Imberti, Luisa ^a  

^a Laboratorio di Biotecnologie   (Italy)

^b University of Brescia ^*  (Italy)

^c UNIVERSITY OF BRESCIA   (Italy)

Author keywords

Human stem cell transplantation; Immune reconstitution; Primary immunodeficiency

Indexed keywords

ARTICLE; B LYMPHOCYTE; CELL MATURATION; CELL MIGRATION; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; LYMPHOCYTOPOIESIS; MALE; PRESCHOOL CHILD; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; STEM CELL TRANSPLANTATION; T LYMPHOCYTE;

ADOLESCENT; ADULT; ANTIGENS, CD; B-LYMPHOCYTES; BONE MARROW CELLS; CASE-CONTROL STUDIES; CHILD; CHILD, PRESCHOOL; FEMALE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; INFANT; MALE; MIDDLE AGED; POLYMERASE CHAIN REACTION; SEVERE COMBINED IMMUNODEFICIENCY; T-LYMPHOCYTES; THYMUS GLAND; TIME FACTORS; YOUNG ADULT;

EID: 77954315400     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2010.04.005     Document Type: Article

References (50)

1. Fischer A., Notarangelo L.D. Combined immunodeficiencies. Immunologic disorders in infants and children 2004, 447-479. Elsevier Saunders, Philadelphia. E.R. Stiehm, H.D. Ochs, J.A. Winkelstein (Eds.).
2. Fischer A., Le Deist F., Hacein-Bey-Abina S., Andre-Schmutz I., Basile G.S., de Villartay J.P., Cavazzana-Calvo M. Severe combined immunodeficiency. A model disease for molecular immunology and therapy. Immunol. Rev. 2005, 203:98-109.
3. Buckley R.H., Schiff S.E., Schiff R.I., Markert L., Williams L.W., Roberts J.L., Myers L.A., Ward F.E. Hematopoietic stem-cell transplantation for the treatment of severe combined immunodeficiency. N. Engl. J. Med. 1999, 340:508-516.
4. Antoine C., Muller S., Cant A., Cavazzana-Calvo M., Veys P., Vossen J., Fasth A., Heilmann C., Wulffraat N., Seger R., Blanche S., Friedrich W., Abinun M., Davies G., Bredius R., Schulz A., Landais P., Fischer A. Long-term survival and transplantation of haemopoietic stem cells for immunodeficiencies: report of the European experience 1968-99. Lancet 2003, 361:553-560.
5. Grunebaum E., Mazzolari E., Porta F., Dallera D., Atkinson A., Reid B., Notarangelo L.D., Roifman C.M. Bone marrow transplantation for severe combined immune deficiency. JAMA 2006, 295:508-518.
6. Dror Y., Gallagher R., Wara D.W., Colombe B.W., Merino A., Benkerrou M., Cowan M.J. Immune reconstitution in severe combined immunodeficiency disease after lectin-treated, T-cell-depleted haplocompatible bone marrow transplantation. Blood 1993, 81:2021-2030.
7. Haddad E., Landais P., Friedrich W., Gerritsen B., Cavazzana-Calvo M., Morgan G., Bertrand Y., Fasth A., Porta F., Cant A., Espanol T., Muller S., Veys P., Vossen J., Fischer A. Long-term immune reconstitution and outcome after HLA-nonidentical T-cell-depleted bone marrow transplantation for severe combined immunodeficiency: a European retrospective study of 116 patients. Blood 1998, 91:3646-3653.
8. Sarzotti M., Patel D.D., Li X., Ozaki D.A., Cao S., Langdon S., Parrott R.E., Coyne K., Buckley R.H. T cell repertoire development in humans with SCID after nonablative allogeneic marrow transplantation. J. Immunol. 2003, 170:2711-2718.
9. Muller S.M., Kohn T., Schulz A.S., Debatin K.M., Friedrich W. Similar pattern of thymic-dependent T-cell reconstitution in infants with severe combined immunodeficiency after human leukocyte antigen (HLA)-identical and HLA-nonidentical stem cell transplantation. Blood 2000, 96:4344-4349.
10. Takeshita S., Toda M., Yamagishi H. Excision products of the T cell receptor gene support a progressive rearrangement model of the alpha/delta locus. EMBO J. 1989, 8:3261-3270.
11. Borghans J.A., Bredius R.G., Hazenberg M.D., Roelofs H., Jol-van der Zijde E.C., Heidt J., Otto S.A., Kuijpers T.W., Fibbe W.E., Vossen J.M., Miedema F., van Tol M.J. Early determinants of long-term T-cell reconstitution after hematopoietic stem cell transplantation for severe combined immunodeficiency. Blood 2006, 108:763-769.
12. Buckley R.H. Molecular defects in human severe combined immunodeficiency and approaches to immune reconstitution. Annu. Rev. Immunol. 2004, 22:625-655.
13. Roberts J.L., Lengi A., Brown S.M., Chen M., Zhou Y.J., O'Shea J.J., Buckley R.H. Janus kinase 3 (JAK3) deficiency: clinical, immunologic, and molecular analyses of 10 patients and outcomes of stem cell transplantation. Blood 2004, 103:2009-2018.
14. Haddad E., Le Deist F., Aucouturier P., Cavazzana-Calvo M., Blanche S., de Saint B.G., Fischer A. Long-term chimerism and B-cell function after bone marrow transplantation in patients with severe combined immunodeficiency with B cells: a single-center study of 22 patients. Blood 1999, 94:2923-2930.
15. van Zelm M.C., Szczepanski T., van der Burg M., van Dongen J.J.M. Replication history of B lymphocytes reveals homeostatic proliferation and extensive antigen-induced B cell expansion. J. Exp. Med. 2007, 204:645-655.
16. van Dongen J.J., Langerak A.W., Bruggemann M., Evans P.A., Hummel M., Lavender F.L., Delabesse E., Davi F., Schuuring E., Garcia-Sanz R., van Krieken J.H., Droese J., Gonzalez D., Bastard C., White H.E., Spaargaren M., Gonzalez M., Parreira A., Smith J.L., Morgan G.J., Kneba M., Macintyre E.A. Design and standardization of PCR primers and protocols for detection of clonal immunoglobulin and T-cell receptor gene recombinations in suspect lymphoproliferations: report of the BIOMED-2 Concerted Action BMH4-CT98-3936. Leukemia 2003, 17:2257-2317.
17. Chiarini M., Sottini A., Ghidini C., Zanotti C., Serana F., Rottoli M., Zaffaroni M., Bergamaschi R., Cordioli C., Capra R., Imberti L. Renewal of the T-cell compartment in multiple sclerosis patients treated with glatiramer acetate. Mult. Scler. 2010, 16:218-227.
18. Mazzolari E., Forino C., Guerci S., Imberti L., Lanfranchi A., Porta F., Notarangelo L.D. Long-term immune reconstitution and clinical outcome after stem cell transplantation for severe T-cell immunodeficiency. J. Allergy Clin. Immunol. 2007, 120:892-899.
19. Chen D.P., Tseng C.P., Tsai S.H., Wu T.L., Chang P.Y., Sun C.F. Systematic analysis of stutters to enhance the accuracy of chimerism testing. Ann. Clin. Lab. Sci. 2008, 38:264-272.
20. Douek D.C., Vescio R.A., Betts M.R., Brenchley J.M., Hill B.J., Zhang L., Berenson J.R., Collins R.H., Koup R.A. Assessment of thymic output in adults after haematopoietic stem-cell transplantation and prediction of T-cell reconstitution. Lancet 2000, 355:1875-1881.
21. Capra R., Sottini A., Cordioli C., Serana F., Chiarini M., Caimi L., Padovani A., Bergamaschi R., Imberti L. IFNbeta bioavailability in multiple sclerosis patients: MxA versus antibody-detecting assays. J. Neuroimmunol. 2007, 189:102-110.
22. Sottini A., Quiros-Roldan E., Albertini A., Primi D., Imberti L. Assessment of T-cell receptor beta-chain diversity by heteroduplex analysis. Hum. Immunol. 1996, 48:12-22.
23. Auletta J.J., Lazarus H.M. Immune restoration following hematopoietic stem cell transplantation: an evolving target. Bone Marrow Transplant. 2005, 35:835-857.
24. Douek D.C., McFarland R.D., Keiser P.H., Gage E.A., Massey J.M., Haynes B.F., Polis M.A., Haase A.T., Feinberg M.B., Sullivan J.L., Jamieson B.D., Zack J.A., Picker L.J., Koup R.A. Changes in thymic function with age and during the treatment of HIV infection. Nature 1998, 396:690-695.
25. Verschuren M.C., Wolvers-Tettero I.L., Breit T.M., Noordzij J., van Wering E.R., van Dongen J.J. Preferential rearrangements of the T cell receptor-delta-deleting elements in human T cells. J. Immunol. 1997, 158:1208-1216.
26. Beishuizen A., de Bruijn M.A., Pongers-Willemse M.J., Verhoeven M.A., van Wering E.R., Hahlen K., Breit T.M., Bruin-Versteeg S., Hooijkaas H., van Dongen J.J. Heterogeneity in junctional regions of immunoglobulin kappa deleting element rearrangements in B cell leukemias: a new molecular target for detection of minimal residual disease. Leukemia 1997, 11:2200-2207.
27. Graninger W.B., Goldman P.L., Morton C.C., O'Brien S.J., Korsmeyer S.J. The kappa-deleting element. Germline and rearranged, duplicated and dispersed forms. J. Exp. Med. 1988, 167:488-501.
28. Feddersen R.M., Martin D.J., Van Ness B.G. Novel recombinations of the IG kappa-locus that result in allelic exclusion. J. Immunol. 1990, 145:745-750.
29. Beishuizen A., Verhoeven M.A., Mol E.J., van Dongen J.J. Detection of immunoglobulin kappa light-chain gene rearrangement patterns by Southern blot analysis. Leukemia 1994, 8:2228-2236.
30. Perfetti V., Vignarelli M.C., Palladini G., Navazza V., Giachino C., Merlini G. Insights into the regulation of immunoglobulin light chain gene rearrangements via analysis of the kappa light chain locus in lambda myeloma. Immunology 2004, 112:420-427.
31. Fronkova E., Muzikova K., Mejstrikova E., Kovac M., Formankova R., Sedlacek P., Hrusak O., Stary J., Trka J. B-cell reconstitution after allogeneic SCT impairs minimal residual disease monitoring in children with ALL. Bone Marrow Transplant. 2008, 42:187-196.
32. Krenger W., Schmidlin H., Cavadini G., Hollander G.A. On the relevance of TCR rearrangement circles as molecular markers for thymic output during experimental graft-versus-host disease. J. Immunol. 2004, 172:7359-7367.
33. Ribeiro R.M., Perelson A.S. Determining thymic output quantitatively: using models to interpret experimental T-cell receptor excision circle (TREC) data. Immunol. Rev. 2007, 216:21-34.
34. Lorenzi A.R., Patterson A.M., Pratt A., Jefferson M., Chapman C.E., Ponchel F., Isaacs J.D. Determination of thymic function directly from peripheral blood: a validated modification to an established method. J. Immunol. Methods 2008, 339:185-194.
35. Pido-Lopez J., Imami N., Aspinall R. Both age and gender affect thymic output: more recent thymic migrants in females than males as they age. Clin. Exp. Immunol. 2001, 125:409-413.
36. Lorenzi A.R., Morgan T.A., Anderson A., Catterall J., Patterson A.M., Foster H.E., Isaacs J.D. Thymic function in juvenile idiopathic arthritis. Ann. Rheum. Dis. 2009, 68:983-990.
37. van Lent A.U., Dontje W., Nagasawa M., Siamari R., Bakker A.Q., Pouw S.M., Maijoor K.A., Weijer K., Cornelissen J.J., Blom B., Di Santo J.P., Spits H., Legrand N. IL-7 enhances thymic human T cell development in "human immune system" Rag2-/-IL-2Rgammac-/- mice without affecting peripheral T cell homeostasis. J. Immunol. 2009, 183:7645-7655.
38. Parrish Y.K., Baez I., Milford T.A., Benitez A., Galloway N., Rogerio J.W., Sahakian E., Kagoda M., Huang G., Hao Q.L., Sevilla Y., Barsky L.W., Zielinska E., Price M.A., Wall N.R., Dovat S., Payne K.J. IL-7 dependence in human B lymphopoiesis increases during progression of ontogeny from cord blood to bone marrow. J. Immunol. 2009, 182:4255-4266.
39. Fry T.J., Mackall C.L. Interleukin-7: master regulator of peripheral T-cell homeostasis?. Trends Immunol. 2001, 22:564-571.
40. Azevedo R.I., Soares M.V., Barata J.T., Tendeiro R., Serra-Caetano A., Victorino R.M., Sousa A.E. IL-7 sustains CD31 expression in human naive CD4+ T cells and preferentially expands the CD31+ subset in a PI3K-dependent manner. Blood 2009, 113:2999-3007.
41. Miklos D.B., Kim H.T., Zorn E., Hochberg E.P., Guo L., Mattes-Ritz A., Viatte S., Soiffer R.J., Antin J.H., Ritz J. Antibody response to DBY minor histocompatibility antigen is induced after allogeneic stem cell transplantation and in healthy female donors. Blood 2004, 103:353-359.
42. Miklos D.B., Kim H.T., Miller K.H., Guo L., Zorn E., Lee S.J., Hochberg E.P., Wu C.J., Alyea E.P., Cutler C., Ho V., Soiffer R.J., Antin J.H., Ritz J. Antibody responses to H-Y minor histocompatibility antigens correlate with chronic graft-versus-host disease and disease remission. Blood 2005, 105:2973-2978.
43. Cutler C., Miklos D., Kim H.T., Treister N., Woo S.B., Bienfang D., Klickstein L.B., Levin J., Miller K., Reynolds C., Macdonell R., Pasek M., Lee S.J., Ho V., Soiffer R., Antin J.H., Ritz J., Alyea E. Rituximab for steroid-refractory chronic graft-versus-host disease. Blood 2006, 108:756-762.
44. Di Martino D., Terranova M.P., Scuderi F., Di Michele P., Iacovone S., Scarso L., Dallorso S., Dini G., Morreale G., Valetto A. V(H)3 and V(H)6 immunoglobulin M repertoire reconstitution after hematopoietic stem-cell transplantation in children. Transplantation 2005, 79:98-107.
45. Storek J., King L., Ferrara S., Marcelo D., Saxon A., Braun J. Abundance of a restricted fetal B cell repertoire in marrow transplant recipients. Bone Marrow Transplant. 1994, 14:783-790.
46. Lum L.G. The kinetics of immune reconstitution after human marrow transplantation. Blood 1987, 69:369-380.
47. Atkinson K. Reconstruction of the haemopoietic and immune systems after marrow transplantation. Bone Marrow Transplant. 1990, 5:209-226.
48. Storek J., Saxon A. Reconstitution of B cell immunity following bone marrow transplantation. Bone Marrow Transplant. 1992, 9:395-408.
49. Raaphorst F.M. Reconstitution of the B cell repertoire after bone marrow transplantation does not recapitulate human fetal development. Bone Marrow Transplant. 1999, 24:1267-1272.
50. Marie-Cardine A., Divay F., Dutot I., Green A., Perdrix A., Boyer O., Contentin N., Tilly H., Tron F., Vannier J.P., Jacquot S. Transitional B cells in humans: characterization and insight from B lymphocyte reconstitution after hematopoietic stem cell transplantation. Clin. Immunol. 2008, 127:14-25.