Thymic microenvironment reconstitution after postnatal human thymus transplantation

Clinical Immunology

Volumn 140, Issue 3, 2011, Pages 244-259

  Li, Bin ^a   Li, Jie ^a   Devlin, Blythe H ^a   Markert, M Louise ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Cytokeratin; Progenitor epithelial cells; Thymopoiesis; Thymus transplantation

Indexed keywords

ANTIGEN; CORTICAL DENDRITIC RETICULUM ANTIGEN 2; CYTOKERATIN 14; EPITHELIAL CELL ADHESION MOLECULE; UNCLASSIFIED DRUG;

ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DIGEORGE SYNDROME; EPITHELIUM CELL; HUMAN; HUMAN TISSUE; MICROENVIRONMENT; PRIORITY JOURNAL; THYMOCYTE; THYMUS; THYMUS TRANSPLANTATION;

BIOPSY; CELL DIFFERENTIATION; DIGEORGE SYNDROME; HUMANS; INFANT; INFANT, NEWBORN; KERATIN-14; LYMPHOCYTE ACTIVATION; NERVE TISSUE PROTEINS; STEM CELLS; T-LYMPHOCYTES; THYMUS GLAND;

EID: 80051791491     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2011.04.004     Document Type: Article

References (61)

1. Hong R. The DiGeorge anomaly. Immunodefic. Rev. 1991, 3:1-14.
2. Markert M.L., Boeck A., Hale L.P., Kloster A.L., McLaughlin T.M., Batchvarova M.N., Douek D.C., Koup R.A., Kostyu D.D., Ward F.E., Rice H.E., Mahaffey S.M., Schiff S.E., Buckley R.H., Haynes B.F. Transplantation of thymus tissue in complete DiGeorge syndrome. N. Engl. J. Med. 1999, 341:1180-1189.
3. Markert M.L., Devlin B.H., Alexieff M.J., Li J., McCarthy E.A., Gupton S.E., Chinn I.K., Hale L.P., Kepler T.B., He M., Sarzotti M., Skinner M.A., Rice H.E., Hoehner J.C. Review of 54 patients with complete DiGeorge anomaly enrolled in protocols for thymus transplantation: outcome of 44 consecutive transplants. Blood 2007, 109:4539-4547.
4. Markert M.L., Kostyu D.D., Ward F.E., McLaughlin T.M., Watson T.J., Buckley R.H., Schiff S.E., Ungerleider R.M., Gaynor J.W., Oldham K.T., Mahaffey S.M., Ballow M., Driscoll D.A., Hale L.P., Haynes B.F. Successful formation of a chimeric human thymus allograft following transplantation of cultured postnatal human thymus. J. Immunol. 1997, 158:998-1005.
5. Markert M.L., Li J., Devlin B.H., Hoehner J.C., Rice H.E., Skinner M.A., Li Y.J., Hale L.P. Use of allograft biopsies to assess thymopoiesis after thymus transplantation. J. Immunol. 2008, 180:6354-6364.
6. Sprent J., Surh C.D. Knowing one's self: central tolerance revisited. Nat. Immunol. 2003, 4:303-304.
7. Zinkernagel R.M., Althage A., Waterfield E., Kindred B., Welsh R.M., Callahan G., Pincetl P. Restriction specificities, alloreactivity, and allotolerance expressed by T cells from nude mice reconstituted with H-2-compatible or -incompatible thymus grafts. J. Exp. Med. 1980, 151:376-399.
8. Goldrath A.W., Bevan M.J. Selecting and maintaining a diverse T-cell repertoire. Nature 1999, 402:255-262.
9. Starr T.K., Jameson S.C., Hogquist K.A. Positive and negative selection of T cells. Annu. Rev. Immunol. 2003, 21:139-176.
10. Manley N.R. Thymus organogenesis and molecular mechanisms of thymic epithelial cell differentiation. Semin. Immunol. 2000, 12:421-428.
11. Rodewald H.R., Kretzschmar K., Swat W., Takeda S. Intrathymically expressed c-kit ligand (stem cell factor) is a major factor driving expansion of very immature thymocytes in vivo. Immunity 1995, 3:313-319.
12. Kuo T. Cytokeratin profiles of the thymus and thymomas: histogenetic correlations and proposal for a histological classification of thymomas. Histopathology 2000, 36:403-414.
13. Gotter J., Brors B., Hergenhahn M., Kyewski B. Medullary epithelial cells of the human thymus express a highly diverse selection of tissue-specific genes colocalized in chromosomal clusters. J. Exp. Med. 2004, 199:155-166.
14. Mathis D., Benoist C. Aire. Annu. Rev. Immunol. 2009, 27:287-312.
15. Yano M., Kuroda N., Han H., Meguro-Horike M., Nishikawa Y., Kiyonari H., Maemura K., Yanagawa Y., Obata K., Takahashi S., Ikawa T., Satoh R., Kawamoto H., Mouri Y., Matsumoto M. Aire controls the differentiation program of thymic epithelial cells in the medulla for the establishment of self-tolerance. J. Exp. Med. 2008, 205:2827-2838.
16. Blackburn C.C., Manley N.R., Palmer D.B., Boyd R.L., Anderson G., Ritter M.A. One for all and all for one: thymic epithelial stem cells and regeneration. Trends Immunol. 2002, 23:391-395.
17. Blackburn C.C., Augustine C.L., Li R., Harvey R.P., Malin M.A., Boyd R.L., Miller J.F., Morahan G. The nu gene acts cell-autonomously and is required for differentiation of thymic epithelial progenitors. Proc. Natl. Acad. Sci. USA 1996, 93:5742-5746.
18. Nehls M., Kyewski B., Messerle M., Waldschutz R., Schuddekopf K., Smith A.J., Boehm T. Two genetically separable steps in the differentiation of thymic epithelium. Science 1996, 272:886-889.
19. Chin R.K., Lo J.C., Kim O., Blink S.E., Christiansen P.A., Peterson P., Wang Y., Ware C., Fu Y.X. Lymphotoxin pathway directs thymic Aire expression. Nat. Immunol. 2003, 4:1121-1127.
20. Xiao S., Su D.M., Manley N.R. Atypical memory phenotype T cells with low homeostatic potential and impaired TCR signaling and regulatory T cell function in Foxn1Delta/Delta mutant mice. J. Immunol. 2007, 179:8153-8163.
21. Itoi M., Tsukamoto N., Amagai T. Expression of Dll4 and CCL25 in Foxn1-negative epithelial cells in the post-natal thymus. Int. Immunol. 2007, 19:127-132.
22. Coffer P.J., Burgering B.M. Forkhead-box transcription factors and their role in the immune system. Nat. Rev. Immunol. 2004, 4:889-899.
23. Callan M.F., Fazou C., Yang H., Rostron T., Poon K., Hatton C., McMichael A.J. CD8(+) T-cell selection, function, and death in the primary immune response in vivo. J. Clin. Invest. 2000, 106:1251-1261.
24. Hetzer-Egger C., Schorpp M., Haas-Assenbaum A., Balling R., Peters H., Boehm T. Thymopoiesis requires Pax9 function in thymic epithelial cells. Eur. J. Immunol. 2002, 32:1175-1181.
25. Xu P.X., Zheng W., Laclef C., Maire P., Maas R.L., Peters H., Xu X. Eya1 is required for the morphogenesis of mammalian thymus, parathyroid and thyroid. Development 2002, 129:3033-3044.
26. Wallin J., Eibel H., Neubuser A., Wilting J., Koseki H., Balling R. Pax1 is expressed during development of the thymus epithelium and is required for normal T-cell maturation. Development 1996, 122:23-30.
27. Gillard G.O., Farr A.G. Features of medullary thymic epithelium implicate postnatal development in maintaining epithelial heterogeneity and tissue-restricted antigen expression. J. Immunol. 2006, 176:5815-5824.
28. Picker L.J., Treer J.R., Ferguson-Darnell B., Collins P.A., Buck D., Terstappen L.W. Control of lymphocyte recirculation in man: I. Differential regulation of the peripheral lymph node homing receptor L-selectin on T cells during the virgin to memory cell transition. J. Immunol. 1993, 150:1105-1121.
29. Markert M.L., Sarzotti M., Ozaki D.A., Sempowski G.D., Rhein M.E., Hale L.P., Le Deist F., Alexieff M.J., Li J., Hauser E.R., Haynes B.F., Rice H.E., Skinner M.A., Mahaffey S.M., Jaggers J., Stein L.D., Mill M.R. Thymus transplantation in complete DiGeorge syndrome: immunologic and safety evaluations in 12 patients. Blood 2003, 102:1121-1130.
30. Markert M.L., Alexieff M.J., Li J., Sarzotti M., Ozaki D.A., Devlin B.H., Sedlak D.A., Sempowski G.D., Hale L.P., Rice H.E., Mahaffey S.M., Skinner M.A. Postnatal thymus transplantation with immunosuppression as treatment for DiGeorge syndrome. Blood 2004, 104:2574-2581.
31. Hudson L.L., Markert M.L., Devlin B.H., Haynes B.F., Sempowski G.D. Human T cell reconstitution in DiGeorge syndrome and HIV-1 infection. Semin. Immunol. 2007, 19:297-309.
32. Davis C.M., McLaughlin T.M., Watson T.J., Buckley R.H., Schiff S.E., Hale L.P., Haynes B.F., Markert M.L. Normalization of the peripheral blood T cell receptor V beta repertoire after cultured postnatal human thymic transplantation in DiGeorge syndrome. J. Clin. Immunol. 1997, 17:167-175.
33. Hong R., Moore A.L. Organ culture for thymus transplantation. Transplantation 1996, 61:444-448.
34. Markert M.L., Devlin B.H., Chinn I.K., McCarthy E.A., Li Y.J. Factors affecting success of thymus transplantation for complete DiGeorge anomaly. Am. J. Transplant. 2008, 8:1729-1736.
35. Rice H.E., Skinner M.A., Mahaffey S.M., Oldham K.T., Ing R.J., Hale L.P., Markert M.L. Thymic transplantation for complete DiGeorge syndrome: medical and surgical considerations. J. Pediatr. Surg. 2004, 39:1607-1615.
36. Key G., Becker M.H., Baron B., Duchrow M., Schluter C., Flad H.D., Gerdes J. New Ki-67-equivalent murine monoclonal antibodies (MIB 1-3) generated against bacterially expressed parts of the Ki-67 cDNA containing three 62 base pair repetitive elements encoding for the Ki-67 epitope. Lab. Invest. 1993, 68:629-636.
37. Rouse R.V., Bolin L.M., Bender J.R., Kyewski B.A. Monoclonal antibodies reactive with subsets of mouse and human thymic epithelial cells. J. Histochem. Cytochem. 1988, 36:1511-1517.
38. Markert M.L., Devlin B.H., McCarthy E.A. Thymus transplantation. Clin. Immunol. 2010, 135:236-246.
39. Su D.M., Navarre S., Oh W.J., Condie B.G., Manley N.R. A domain of Foxn1 required for crosstalk-dependent thymic epithelial cell differentiation. Nat. Immunol. 2003, 4:1128-1135.
40. Blackburn C.C., Manley N.R. Developing a new paradigm for thymus organogenesis. Nat. Rev. Immunol. 2004, 4:278-289.
41. Rossi S.W., Jenkinson W.E., Anderson G., Jenkinson E.J. Clonal analysis reveals a common progenitor for thymic cortical and medullary epithelium. Nature 2006, 441:988-991.
42. Zhang L., Sun L., Zhao Y. Thymic epithelial progenitor cells and thymus regeneration: an update. Cell Res. 2007, 17:50-55.
43. Rossi S.W., Chidgey A.P., Parnell S.M., Jenkinson W.E., Scott H.S., Boyd R.L., Jenkinson E.J., Anderson G. Redefining epithelial progenitor potential in the developing thymus. Eur. J. Immunol. 2007, 37:2411-2418.
44. Bennett A.R., Farley A., Blair N.F., Gordon J., Sharp L., Blackburn C.C. Identification and characterization of thymic epithelial progenitor cells. Immunity 2002, 16:803-814.
45. Gill J., Malin M., Hollander G.A., Boyd R. Generation of a complete thymic microenvironment by MTS24(+) thymic epithelial cells. Nat. Immunol. 2002, 3:635-642.
46. Nijhof J.G., Braun K.M., Giangreco A., van Pelt C., Kawamoto H., Boyd R.L., Willemze R., Mullenders L.H., Watt F.M., de Gruijl F.R., van Ewijk W. The cell-surface marker MTS24 identifies a novel population of follicular keratinocytes with characteristics of progenitor cells. Development 2006, 133:3027-3037. (Cambridge, England).
47. Bleul C.C., Corbeaux T., Reuter A., Fisch P., Monting J.S., Boehm T. Formation of a functional thymus initiated by a postnatal epithelial progenitor cell. Nature 2006, 441:992-996.
48. Hikosaka Y., Nitta T., Ohigashi I., Yano K., Ishimaru N., Hayashi Y., Matsumoto M., Matsuo K., Penninger J.M., Takayanagi H., Yokota Y., Yamada H., Yoshikai Y., Inoue J., Akiyama T., Takahama Y. The cytokine RANKL produced by positively selected thymocytes fosters medullary thymic epithelial cells that express autoimmune regulator. Immunity 2008, 29:438-450.
49. Haynes B.F., Scearce R.M., Lobach D.F., Hensley L.L. Phenotypic characterization and ontogeny of mesodermal-derived and endocrine epithelial components of the human thymic microenvironment. J. Exp. Med. 1984, 159:1149-1168.
50. Lobach D.F., Haynes B.F. Ontogeny of the human thymus during fetal development. J. Clin. Immunol. 1987, 7:81-97.
51. Saito M., Kitamura H., Sugiyama K. A novel heptasialosyl c-series ganglioside in embryonic chicken brain: its structure and stage-specific expression. Biochim. Biophys. Acta 2002, 1571:18-26.
52. Haynes B.F., Shimizu K., Eisenbarth G.S. Identification of human and rodent thymic epithelium using tetanus toxin and monoclonal antibody A2B5. J. Clin. Invest. 1983, 71:9-14.
53. Popa I., Zubkova I., Medvedovic M., Romantseva T., Mostowski H., Boyd R., Zaitseva M. Regeneration of the adult thymus is preceded by the expansion of K5+K8+ epithelial cell progenitors and by increased expression of Trp63, cMyc and Tcf3 transcription factors in the thymic stroma. Int. Immunol. 2007, 19:1249-1260.
54. Cavadini P., Vermi W., Facchetti F., Fontana S., Nagafuchi S., Mazzolari E., Sediva A., Marrella V., Villa A., Fischer A., Notarangelo L.D., Badolato R. AIRE deficiency in thymus of 2 patients with Omenn syndrome. J. Clin. Invest. 2005, 115:728-732.
55. Finnish-German APECED Consortium An autoimmune disease, APECED, caused by mutations in a novel gene featuring two PHD-type zinc-finger domains. Nat. Genet. 1997, 17:399-403.
56. Ahonen P., Myllarniemi S., Sipila I., Perheentupa J. Clinical variation of autoimmune polyendocrinopathy-candidiasis-ectodermal dystrophy (APECED) in a series of 68 patients. N. Engl. J. Med. 1990, 322:1829-1836.
57. McLean-Tooke A., Spickett G.P., Gennery A.R. Immunodeficiency and autoimmunity in 22q11.2 deletion syndrome. Scand. J. Immunol. 2007, 66:1-7.
58. Nehls M., Pfeifer D., Schorpp M., Hedrich H., Boehm T. New member of the winged-helix protein family disrupted in mouse and rat nude mutations. Nature 1994, 372:103-107.
59. Pignata C., Gaetaniello L., Masci A.M., Frank J., Christiano A., Matrecano E., Racioppi L. Human equivalent of the mouse Nude/SCID phenotype: long-term evaluation of immunologic reconstitution after bone marrow transplantation. Blood 2001, 97:880-885.
60. Su D.M., Manley N.R. Hoxa3 and pax1 transcription factors regulate the ability of fetal thymic epithelial cells to promote thymocyte development. J. Immunol. 2000, 164:5753-5760.
61. Jenkinson W.E., Bacon A., White A.J., Anderson G., Jenkinson E.J. An epithelial progenitor pool regulates thymus growth. J. Immunol. 2008, 181:6101-6108.