Thymic nurse cells exhibit epithelial progenitor phenotype and create unique extra-cytoplasmic membrane space for thymocyte selection

Cellular Immunology

Volumn 261, Issue 2, 2010, Pages 81-92

  Hendrix, Tonya M ^a   Chilukuri, Rajendra V E ^a   Martinez, Marcia ^b   Olushoga, Zachariah ^a   Blake, Andrew ^a   Brohi, Moazzam ^a   Walker, Christopher ^a   Samms, Michael ^a   Guyden, Jerry C ^a  

^a CITY COLLEGE OF NEW YORK   (United States)

^b TUSKEGEE UNIVERSITY   (United States)

Author keywords

Cytokeratins; Epithelial progenitor; Heterotypic internalization; Membrane extensions; MHC restriction; Thymic nurse cell; Trp 63

Indexed keywords

CYTOKERATIN 5; CYTOKERATIN 8; LYMPHOCYTE ANTIGEN RECEPTOR; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR TRP 63; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL AGGREGATION; CELL FUNCTION; CELL INTERACTION; CELL SELECTION; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EPITHELIUM CELL; IMMUNOHISTOLOGY; LIPID RAFT; MEMBRANE FORMATION; MICROENVIRONMENT; MOUSE; NONHUMAN; NURSE CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL; THYMOCYTE;

ANIMALS; CELL COMMUNICATION; CELL MEMBRANE; EPITHELIAL CELLS; INTRACELLULAR SPACE; KERATINS; MAJOR HISTOCOMPATIBILITY COMPLEX; MICE; MICE, INBRED C57BL; PHENOTYPE; STEM CELLS; THYMUS GLAND;

EID: 77649187909     PISSN: 00088749     EISSN: 10902163     Source Type: Journal    
DOI: 10.1016/j.cellimm.2009.11.004     Document Type: Article

References (50)

1. Overholtzer M., Brugge J.S. The cell biology of cell-in-cell structures. Nat. Rev. Mol. Cell Biol. 2008, 9:796-809.
2. Wekerle H., Ketelsen U.P. Thymic nurse cells-Ia-bearing epithelium involved in T-lymphocyte differentiation?. Nature 1980, 283:402-404.
3. Wekerle H., Ketelsen U.P., Ernst M. Thymic nurse cells. Lymphoepithelial cell complexes in murine thymuses: morphological and serological characterization. J. Exp. Med. 1980, 151:925-944.
4. Ritter M.A., Sauvage C.A., Cotmore S.F. The human thymus microenvironment: in vivo identification of thymic nurse cells and other antigenically-distinct subpopulations of epithelial cells. Immunology 1981, 44:439-446.
5. Boyd R.L., Oberhuber G., Hala K., Wick G. Obese strain (OS) chickens with spontaneous autoimmune thyroiditis have a deficiency in thymic nurse cells. J. Immunol. 1984, 132:718-724.
6. Flano E., Alvarez F., Lopez-Fierro P., Razquin B.E., Villena A.J., Zapata A.G. In vitro and in situ characterization of fish thymic nurse cells. Dev. Immunol. 1996, 5:17-24.
7. Romano N., Taverne-Thiele A.J., Fanelli M., Baldassini M.R., Abelli L., Mastrolia L., Van Muiswinkel W.B., Rombout J.H. Ontogeny of the thymus in a teleost fish, Cyprinus carpio L.: developing thymocytes in the epithelial microenvironment. Dev. Comp. Immunol. 1999, 23:123-137.
8. Mohammad M.G., Chilmonczyk S., Birch D., Aladaileh S., Raftos D., Joss J. Anatomy and cytology of the thymus in juvenile Australian lungfish, Neoceratodus forsteri. J. Anat. 2007, 211:784-797.
9. Andrews P., Boyd R.L., Shortman K. The limited immunocompetence of thymocytes within murine thymic nurse cells. Eur. J. Immunol. 1985, 15:1043-1048.
10. Kyewski B.A., Kaplan H.S. Lymphoepithelial interactions in the mouse thymus: phenotypic and kinetic studies on thymic nurse cells. J. Immunol. 1982, 128:2287-2294.
11. + thymocytes from apoptosis. Cell. Mol. Biol. (Noisy-le-grand) 1995, 41:1099-1111.
12. + thymocytes. Cell. Immunol. 1992, 140:495-506.
13. Pezzano M., King K.D., Philp D.D., Adeyemi A., Gardiner B., Yang J., Samms M., Boto W., Guyden J.C. A thymic nurse cell-specific monoclonal antibody. Cell. Immunol. 1998, 185:123-133.
14. Philp D., Pezzano M., Li Y., Omene C., Boto W., Guyden J. The binding, internalization, and release of thymocytes by thymic nurse cells. Cell. Immunol. 1993, 148:301-315.
15. Surh C.D., Sprent J. T-cell apoptosis detected in situ during positive and negative selection in the thymus. Nature 1994, 372:100-103.
16. Robey E., Fowlkes B.J. Selective events in T cell development. Annu. Rev. Immunol. 1994, 12:675-705.
17. von Boehmer H., Kisielow P. Self-nonself discrimination by T cells. Science 1990, 248:1369-1373.
18. Peterson P., Org T., Rebane A. Transcriptional regulation by AIRE: molecular mechanisms of central tolerance. Nat. Rev. Immunol. 2008, 8:948-957.
19. Su M.A., Anderson M.S. Aire: an update. Curr. Opin. Immunol. 2004, 16:746-752.
20. Derbinski J., Schulte A., Kyewski B., Klein L. Promiscuous gene expression in medullary thymic epithelial cells mirrors the peripheral self. Nat. Immunol. 2001, 2:1032-1039.
21. Hansenne I., Louis C., Martens H., Dorban G., Charlet-Renard C., Peterson P., Geenen V. Aire and Foxp3 expression in a particular microenvironment for T cell differentiation. Neuroimmunomodulation 2009, 16:35-44.
22. Samms M., Philp D., Emanus F., Osuji O., Pezzano M., Guyden J.C. Lysosomal-mediated degradation of apoptotic thymocytes within thymic nurse cells. Cell. Immunol. 1999, 197:108-115.
23. 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.
24. Pezzano M., Li Y., Yang Y.M., Guyden J. The immortalization of thymic nurse cells by SV40 virus. Cell. Immunol. 1991, 133:434-445.
25. + epithelial cell progenitors and by increased expression of Trp63, cMyc and Tcf3 transcription factors in the thymic stroma. Int. Immunol. 2007, 19:1249-1260.
26. Senoo M., Pinto F., Crum C.P., McKeon F. p63 is essential for the proliferative potential of stem cells in stratified epithelia. Cell 2007, 129:523-536.
27. Lorenz R.G., Allen P.M. Thymic cortical epithelial cells can present self-antigens in vivo. Nature 1989, 337:560-562.
28. Werlen G., Hausmann B., Naeher D., Palmer E. Signaling life and death in the thymus: timing is everything. Science 2003, 299:1859-1863.
29. Delgado P., Fernandez E., Dave V., Kappes D., Alarcon B. CD3delta couples T-cell receptor signalling to ERK activation and thymocyte positive selection. Nature 2000, 406:426-430.
30. 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.
31. 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.
32. Brelinska R., Warchol J.B. Thymic nurse cells: their functional ultrastructure. Microsc. Res. Tech. 1997, 38:250-266.
33. Anderson G., Jenkinson E.J. Lymphostromal interactions in thymic development and function. Nat. Rev. Immunol. 2001, 1:31-40.
34. Hogquist K.A., Bevan M.J. The nature of the peptide/MHC ligand involved in positive selection. Semin. Immunol. 1996, 8:63-68.
35. Boehm T., Scheu S., Pfeffer K., Bleul C.C. Thymic medullary epithelial cell differentiation, thymocyte emigration, and the control of autoimmunity require lympho-epithelial cross talk via LTbetaR. J. Exp. Med. 2003, 198:757-769.
36. Anderson M.S., Venanzi E.S., Klein L., Chen Z., Berzins S.P., Turley S.J., von Boehmer H., Bronson R., Dierich A., Benoist C., Mathis D. Projection of an immunological self shadow within the thymus by the aire protein. Science 2002, 298:1395-1401.
37. McCaughtry T.M., Baldwin T.A., Wilken M.S., Hogquist K.A. Clonal deletion of thymocytes can occur in the cortex with no involvement of the medulla. J. Exp. Med. 2008, 205:2575-2584.
38. Klein L., Kyewski B. Self-antigen presentation by thymic stromal cells: a subtle division of labor. Curr. Opin. Immunol. 2000, 12:179-186.
39. Goldman K.P., Park C.S., Kim M., Matzinger P., Anderson C.C. Thymic cortical epithelium induces self tolerance. Eur. J. Immunol. 2005, 35:709-717.
40. Spain L.M., Berg L.J. Developmental regulation of thymocyte susceptibility to deletion by " self" -peptide. J. Exp. Med. 1992, 176:213-223.
41. Janes P.W., Ley S.C., Magee A.I., Kabouridis P.S. The role of lipid rafts in T cell antigen receptor (TCR) signalling. Semin. Immunol. 2000, 12:23-34.
42. Magee T., Pirinen N., Adler J., Pagakis S.N., Parmryd I. Lipid rafts: cell surface platforms for T cell signaling. Biol. Res. 2002, 35:127-131.
43. Fischer A.M., Katayama C.D., Pages G., Pouyssegur J., Hedrick S.M. The role of erk1 and erk2 in multiple stages of T cell development. Immunity 2005, 23:431-443.
44. Sohn S.J., Thompson J., Winoto A. Apoptosis during negative selection of autoreactive thymocytes. Curr. Opin. Immunol. 2007, 19:510-515.
45. Pezzano M., Philp D., Stephenson S., Li Y., Reid V., Maitta R., Guyden J.C. Positive selection by thymic nurse cells requires IL-1 beta and is associated with an increased Bcl-2 expression. Cell. Immunol. 1996, 169:174-184.
46. von Boehmer H. Developmental biology of T cells in T cell-receptor transgenic mice. Annu. Rev. Immunol. 1990, 8:531-556.
47. Martinez M., Samms M., Hendrix T.M., Adeosun O., Pezzano M., Guyden J.C. Thymic nurse cell multicellular complexes in HY-TCR transgenic mice demonstrate their association with MHC restriction. Exp. Biol. Med. (Maywood) 2007, 232:780-788.
48. + thymocytes. Nature 1988, 333:742-746.
49. Teh H.S., Kisielow P., Scott B., Kishi H., Uematsu Y., Bluthmann H., von Boehmer H. Thymic major histocompatibility complex antigens and the alpha beta T-cell receptor determine the CD4/CD8 phenotype of T cells. Nature 1988, 335:229-233.
50. Zuklys S., Balciunaite G., Agarwal A., Fasler-Kan E., Palmer E., Hollander G.A. Normal thymic architecture and negative selection are associated with Aire expression, the gene defective in the autoimmune-polyendocrinopathy-candidiasis-ectodermal dystrophy (APECED). J. Immunol. 2000, 165:1976-1983.