Thymic nurse cells: A microenvironment for thymocyte development and selection

International Review of Cytology

Volumn 223, Issue , 2002, Pages 1-37

  Guyden, Jerry C ^a   Pezzano, Mark ^a  

^a CITY COLLEGE OF NEW YORK   (United States)

Author keywords

Autoimmunity; Macrophage; MHC restriction; Neuroendocrine; T cell development; Thymic nurse cell

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; INTERLEUKIN 1BETA; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MEROSIN; NEUROPEPTIDE; T LYMPHOCYTE RECEPTOR; VERY LATE ACTIVATION ANTIGEN 6;

ANTIGEN PRESENTATION; ANTIGEN RECOGNITION; APOPTOSIS; AUTOIMMUNITY; CELL SELECTION; CELLULAR DISTRIBUTION; HUMAN; IMMUNOLOGICAL TOLERANCE; LYMPHOCYTE DIFFERENTIATION; MACROPHAGE; MAJOR HISTOCOMPATIBILITY COMPLEX RESTRICTION; MICROENVIRONMENT; NEUROIMMUNOLOGY; NONHUMAN; NURSE CELL; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; THYMOCYTE;

ANIMALIA;

EID: 0037282442     PISSN: 00747696     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0074-7696(05)23001-2     Document Type: Review

References (150)

1. Adkins, B., Tidmarsh, G. F., and Weissman, I. L. (1988). Normal thymic cortical epithelial cells developmentally regulate the expression of a B-lineage transformation-associated antigen. Immunogenetics 27, 180-186.
2. Aguilar, L. K., Aguilar-Cordova, E., Cartwright, J., Jr., and Belmont, J. W. (1994). Thymic nurse cells are sites of thymocyte apoptosis. J. Immunol. 152, 2645-2651.
3. Albert, M. L., Sauter, B., and Bhardwaj, N. (1998). Dendritic cells acquire antigen from apoptotic cells and induce class I-restricted CTLs. Nature 392, 86-89.
4. Andrews, P., and Boyd, R. L. (1985). The murine thymic nurse cell: An isolated thymic microenvironment. Eur. J. Immunol. 15, 36-42.
5. Andrews, P., Boyd, R. L., and Shortman, K. (1985). The limited immunocompetence of thymocytes within murine thymic nurse cells. Eur. J. Immunol. 15, 1043-1048.
6. Bellone, M., Iezzi, G., Rovere, P., Galati, G., Ronchetti, A., Protti, M. P., Davoust, J., Rugarli, C., and Manfredi, A. A. (1997). Processing of engulfed apoptotic bodies yields T cell epitopes. J. Immunol. 159, 5391-5399.
7. Besedovsky, H. O., and del Rey, A. (1996). Immune-neuro-endocrine interactions: Facts and hypotheses. Endocr. Rev. 17, 64-102.
8. Bevan, M. J. (1977). In a radiation chimaera, host H-2 antigens determine immune responsiveness of donor cytotoxic cells. Nature 269, 417-418.
9. Blalock, J. E. (1994). The syntax of immune-neuroendocrine communication. Immunol. Today 15, 504-511.
10. Bodey, B., Bodey, B., Jr., Siegel, S. E., and Kaiser, H. E. (2000). The role of the reticulo-epithelial (RE) cell network in the immuno-neuroendocrine regulation of intrathymic lymphopoiesis. Anticancer Res. 20, 1871-1888.
11. Boudreau, N., Sympson, C. J., Werb, Z., and Bissell, M. J. (1995). Suppression of ICE and apoptosis in mammary epithelial cells by extracellular matrix. Science 267, 891-893.
12. Boyd, R. L., Oberhuber, G., Hala, K., and Wick, G. (1984). Obese strain (OS) chickens with spontaneous autoimmune thyroiditis have a deficiency in thymic nurse cells. J. Immunol. 132, 718-724.
13. Boyd, R. L., Tucek, C. L., Godfrey, D. I., Izon, D. J., Wilson, T. J., Davidson, N. J., Bean, A. G., Ladyman, H. M., Ritter, M. A., and Hugo, P. (1993). The thymic microenvironment. Immunol. Today 14, 445-459.
14. Brelinska, R. (1989). Thymic nurse cells: Division of thymocytes within complexes. Cell Tissue Res. 258, 637-643.
15. Brelinska, R., and Warchol, J. B. (1997). Thymic nurse cells: their functional ultrastructure. Microsc. Res. Tech. 38, 250-266.
16. Brooks, P. C., Montgomery, A. M., Rosenfeld, M., Reisfeld, R. A., Hu, T., Klier, G., and Cheresh, D. A. (1994). Integrin alpha v beta 3 antagonists promote tumor regression by inducing apoptosis of angiogenic blood vessels. Cell 79, 1157-1164.
17. Brunet, J. F., Hirsch, M. R., Naquet, P., Uberla, K., Diamantstein, T., Lipinski, M., and Goridis, C. (1989). Developmentally regulated expression of the neural cell adhesion molecule (NCAM) by mouse thymocytes. Eur. J. Immunol. 19, 837-841.
18. Casciola-Rosen, L. A., Anhalt, G., and Rosen, A. (1994). Autoantigens targeted in systemic lupus erythematosus are clustered in two populations of surface structures on apoptotic keratinocytes. J. Exp. Med. 179, 1317-1330.
19. Ceredig, R., Dialynas, D. P., Fitch, F. W., and MacDonald, H. R. (1983). Precursors of T cell growth factor producing cells in the thymus: Ontogeny, frequency, and quantitative recovery in a subpopulation of phenotypically mature thymocytes defined by monoclonal antibody GK-1.5. J. Exp. Med. 158, 1654-1671.
20. Clark, R., Strasser, J., McCabe, S., Robbins, K., and Jardieu, P. (1993). Insulin-like growth factor-1 stimulation of lymphopoiesis. J. Clin. Invest. 92, 540-548.
21. Cordes, U., Pedersen, M., Bastholm, L., Nielsen, M., and Werdelin, O. (1997). Murine thymic nurse cells express ICAM-1 on caveolar and vacuolar membranes. Scand. J. Immunol. 46, 344-348.
22. Couture, C., Patel, P. C., and Potworowski, E. F. (1990). A novel thymic epithelial adhesion molecule. Eur. J. Immunol. 20, 2769-2773.
23. de Carvalho, L. C., Wick, G., and Roitt, I. M. (1981). Requirement of T cells for the development of spontaneous autoimmune thyroiditis in obese strain (OS) chickens. J. Immunol. 126, 750-753.
24. Defresne, M. P., Humblet, C., Rongy, A. M., Greimers, R., and Boniver, J. (1990). Effect of interferongamma and tumor necrosis factor-alpha on lymphoepithelial interactions within thymic nurse cells. Eur. J. Immunol. 20, 429-432.
25. Defresne, M. P., Nabarra, B., van Vliet, E., Willemsen, R., van Dongen, H., and van Ewijk, W. (1994). The ER-TR4 monoclonal antibody recognizes murine thymic epithelial cells (type 1) and inhibits their capacity to interact with immature thymocytes: Immuno-electron microscopic and functional studies. Histochemistry 101, 355-363.
26. de Waal Malefijt, R., Leene, W., Roholl, P. J., Wormmeester, J., and Hoeben, K. A. (1986). T cell differentiation within thymic nurse cells. Lab. Invest. 55, 25-34.
27. Dipasquale, B., and Tridente, G. (1991). Immunohistochemical characterization of nurse cells in normal human thymus. Histochemistry 96, 499-503.
28. Doi, H., Nakagawa, S., Nagata, K., Hata, M., Kasahara, S., Sakata, T., Suzuki, R., Nanno, M., Sugamura, K., and Itoh, T. (1991). Murine thymic nurse cell clone supports the growth of fetal thymocytes in the presence of interleukin 2. Eur. J. Immunol. 21, 783-792.
29. Doukas, J., Mordes, J. P., Swymer, C., Niedzwiecki, D., Mason, R., Rozing, J., Rossini, A. A., and Greiner, D. L. (1994). Thymic epithelial defects and predisposition to autoimmune disease in BB rats. Am. J. Pathol. 145, 1517-1525.
30. Duijvestijn, A. M., Schutte, R., Kohler, Y. G., Korn, C., and Hoefsmit, E. C. (1983). Characterization of the population of phagocytic cells in thymic cell suspensions. A morphological and cytochemical study. Cell Tissue Res. 231, 313-323.
31. Elands, J., Resink, A., and De Kloet, E. R. (1990). Neurohypophyseal hormone receptors in the rat thymus, spleen, and lymphocytes. Endocrinology 126, 2703-2710.
32. Ezaki, T., Matsuno, K., and Kotani, M. (1991). Thymic nurse cells (TNC) in spontaneous thymoma BUF/Mna rats as a model to study their roles in T-cell development. Immunology 73, 151-158.
33. Fehling, H. J., and von Boehmer, H. (1997). Early alpha beta T cell development in the thymus of normal and genetically altered mice. Curr. Opin. Immunol. 9, 263-275.
34. Flano, E., Alvarez, F., Lopez-Fierro, P., Razquin, B. E., Villena, A. J., and Zapata, A. G. (1996). In vitro and in situ characterization of fish thymic nurse cells. Dev. Immunol. 5, 17-24.
35. Fowlkes, B. J., Edison, L., Mathieson, B. J., and Chused, T. M. (1985). Early T lymphocytes. Differentiation in vivo of adult intrathymic precursor cells. J. Exp. Med. 162, 802-822.
36. Frisch, S. M., and Francis, H. (1994). Disruption of epithelial cell-matrix interactions induces apoptosis. J. Cell Biol. 1249, 619-626.
37. Fujiwara, H., Ogata, M., Mizushima, Y., Tatsumi, Y., Takai, Y., and Hamaoka, T. (1990). Proliferation and differentiation of immature thymocytes induced by a thymic stromal cell clone. Thymus 16, 159-172.
38. Gao, X., Nishimura, T., Takeuchi, Y., Sudo, T., and Habu, S. (1993). Thymic nurse cell clone supports the differentiation of CD4-8-thymocytes into CD4+8+ thymocytes in vitro. Immunol. Lett. 35, 169-175.
39. Geenen, V., Defresne, M. P., Robert, F., Legros, J. J., Franchimont, P., and Boniver, J. (1988). The neurohormonal thymic microenvironment: Immunocytochemical evidence that thymic nurse cells are neuroendocrine cells. Neuroendocrinology 47, 365-368.
40. Geenen, V., Cormann, N., Benhida, A., Martens, H., Achour, I., Defresne, M. P., and Robert, F. (1992a). The thymic repertoire of neuroendocrine self antigens and the central immune tolerance of neuroendocrine functions. Eur. J. Med. 1, 158-165.
41. Geenen, V., Robert, F., Martens, H., De Groote, D., and Franchimont, P. (1992b). The thymic education of developing T cells in self neuroendocrine principles. J. Endocrinol. Invest. 15, 621-629.
42. Geenen, V., Achour, I., Robert, F., Vandersmissen, E., Sodoyez, J. C., Defresne, M. P., Boniver, J., Lefebvre, P. J., and Franchimont, P. (1993a). Evidence that insulin-like growth factor 2 (IGF2) is the dominant thymic peptide of the insulin superfamily. Thymus 21, 115-127.
43. Geenen, V., Vandersmissen, E., Cormann-Goffin, N., Martens, H., Legros, J. J., Degiovanni, G., Benhida, A., Martial, J., and Franchimont, P. (1993b). Membrane translocation and relationship with MHC class I of a human thymic neurophysin-like protein. Thymus 22, 55-66.
44. Geenen, V., Kecha, O., and Martens, H. (1998). Thymic expression of neuroendocrine self-peptide precursors: Role in T cell survival and self-tolerance. J. Neuroendocrinol. 10, 811-822.
45. Geenen, V., Martens, H., Brilot, F., Renard, C., Franchimont, D., and Kecha, O. (2000). Thymic neuroendocrine self-antigens. Role in T-cell development and central T-cell self-tolerance. Ann. N. Y. Acad. Sci. 917, 710-723.
46. Geenen, V., Kecha, O., Brilot, F., Hansenne, I., Renard, C., and Martens, H. (2001). Thymic T-cell tolerance of neuroendocrine functions: Physiology and pathophysiology. Cell. Mol. Biol. (Noisy-le-grand) 47, 179-188.
47. Gilligan, H. M., Bredy, B., Brady, H. R., Hebert, M. J., Slayter, H. S., Xu, Y., Rauch, J., Shia, M. A., Koh, J. S., and Levine, J. S. (1996). Antineutrophil cytoplasmic autoantibodies interact with primary granule constituents on the surface of apoptotic neutrophils in the absence of neutrophil priming. J. Exp. Med. 184, 2231-2241.
48. Hartwell, D. W., Fenton, M. J., Levine, J. S., and Beller, D. I. (1995). Aberrant cytokine regulation in macrophages from young autoimmune-prone mice: Evidence that the intrinsic defect in MRL macrophage IL-1 expression is transcriptionally controlled. Mol. Immunol. 32, 743-751.
49. Haynes, B. F., Shimizu, K., and Eisenbarth, G. S. (1983). Identification of human and rodent thymic epithelium using tetanus toxin and monoclonal antibody A2B5. J. Clin. Invest. 71, 9-14.
50. Hinton, P. S., Peterson, C. A., Dahly, E. M., and Ney, D. M. (1998). IGF-I alters lymphocyte survival and regeneration in thymus and spleen after dexamethasone treatment. Am. J. Physiol. 274, R912-920.
51. Hiramine, C., Hojo, K., Koseto, M., Nakagawa, T., and Mukasa, A. (1990). Establishment of a murine thymic epithelial cell line capable of inducing both thymic nurse cell formation and thymocyte apoptosis. Lab. Invest. 62, 41-54.
52. Hiramine, C., Nakagawa, T., Miyauchi, A., and Hojo, K. (1996). Thymic nurse cells as the site of thymocyte apoptosis and apoptotic cell clearance in the thymus of cyclophosphamide-treated mice. Lab. Invest. 75, 185-201.
53. Hirokawa, K., Utsuyama, M., Moriizumi, E., and Handa, S. (1986). Analysis of the thymic microenvironment by monoclonal antibodies with special reference to thymic nurse cells. Thymus 8, 349-360.
54. Hoffman, R. W. (2001). T cells in the pathogenesis of systemic lupus erythematosus. Front. Biosci. 6, D1369-1378.
55. Holtfreter, H. B., and Cohen, N. (1987). In vitro behavior of thymic nurse cell-like complexes from mechanically and enzymatically dissociated frog tadpole thymuses. Am. J. Anat. 179, 342-355.
56. Hugo, P., Kappler, J. W., Godfrey, D. I., and Marrack, P. C. (1994). Thymic epithelial cell lines that mediate positive selection can also induce thymocyte clonal deletion. J. Immunol. 152, 1022-1031.
57. Imachi, H., Murao, K., Hiramine, C., Sayo, Y., Sato, M., Hosokawa, H., Ishida, T., Kodama, T., Quehenberger, O., Steinberg, D., and Takahara, J. (2000). Human scavenger receptor B1 is involved in recognition of apoptotic thymocytes by thymic nurse cells. Lab. Invest. 80, 263-270.
58. Imura, H., Nakao, K., Shimatsu, A., Ogawa, Y., Sando, T., Fujisawa, I., and Yamabe, H. (1993). Lymphocytic infundibuloneurohypophysitis as a cause of central diabetes insipidus. N. Engl. J. Med. 329, 683-689.
59. Itoh, T., Doi, H., Chin, S., Nishimura, T., and Kasahara, S. (1988). Establishment of mouse thymic nurse cell clones from a spontaneous BALB/c thymic tumor. Eur. J. Immunol. 18, 821-824.
60. Iwao, M., Fukada, S., Harada, T., Tsujikawa, K., Yagita, H., Hiramine, C., Miyagoe, Y., Takeda, S., and Yamamoto, H. (2000). Interaction of merosin (laminin 2) with very late activation antigen-6 is necessary for the survival of CD4+ CD8+ immature thymocytes. Immunology 99, 481-488.
61. Jason, J. M., and Janeway, C. A., Jr. (1984). In vitro cultivation of nonlymphoid thymic cells: Morphological and immunological characterization. Clin. Immunol. Immunopathol. 30, 214-226.
62. Kanazawa, S., Ilic, D., Hashiyama, M., Noumura, T., Yamamoto, T., Suda, T., and Aizawa, S. (1996a). p59fyn-p125FAK cooperation in development of CD4+CD8+ thymocytes. Blood 87, 865-870.
63. Kanazawa, S., Ilic, D., Hashiyama, M., Okada, M., Noumura, T., Aizawa, S., and Suda, T. (1996b). Impaired development of CD4+ CD8+ thymoyctes by csk-'knock-in' into fyn locus. Oncogene 13, 199-204.
64. Kecha, O., Martens, H., Franchimont, N., Achour, I., Hazee-Hagelstein, M. T, Charlet-Renard, C., Geenen, V., and Winkler, R. (1999). Characterization of the insulin-like growth factor axis in the human thymus. J. Neuroendocrinol. 11, 435-440.
65. Kecha, O., Brilot, F., Martens, H., Franchimont, N., Renard, C., Greimers, R., Defresne, M. P., Winkler, R., and Geenen, V. (2000). Involvement of insulin-like growth factors in early T cell development: A study using fetal thymic organ cultures. Endocrinology 141, 1209-1217.
66. Kim, M. G., Lee, G., Lee, S. K., Lolkema, M., Yim, J., Hong, S. H., and Schwartz, R. H. (2000). Epithelial cell-specific laminin 5 is required for survival of early thymocytes. J. Immunol. 165, 192-201.
67. Koh, J. S., and Levine, J. S. (1997). Apoptosis and autoimmunity. Curr Opin. Nephrol. Hypertens. 6, 259-266.
68. Koh, J. S., Wang, Z., and Levine, J. S. (2000). Cytokine dysregulation induced by apoptotic cells is a shared characteristic of murine lupus. J. Immunol. 165, 4190-4201.
69. Kooijman, R., van Buul-Offers, S. C., Scholtens, L. E., Schuurman, H. J., Van den Brande, L. J., and Zegers, B. J. (1995a). T cell development in insulin-like growth factor-II transgenic mice. J. Immunol. 154, 5736-5745.
70. Kooijman, R. K., Scholtens, L. E., Rijkers, G. T., and Zegers, B. J. (1995b). Differential expression of type I insulin-like growth factor receptors in different stages of human T cells. Eur. J. Immunol. 25, 931-935.
71. Krieger, M. (1997). The other side of scavenger receptors: pattern recognition for host defense. Curr. Opin. Lipidol. 8, 275-280.
72. Kumamoto, K., Matsuura, T., Amagai, T., and Kawata, M. (1995). Oxytocin-producing and vasopressin-producing eosinophils in the mouse spleen: Immunohistochemical, immuno-electron-microscopic and in situ hybridization studies. Cell Tissue Res. 281, 1-10.
73. Kyewski, B. A., and Kaplan, H. S. (1982). Lymphoepithelial interactions in the mouse thymus: Phenotypic and kinetic studies on thymic nurse cells. J. Immunol. 128, 2287-2294.
74. Lahoud, M., Vremec, D., Boyd, R. L., and Shortman, K. (1993). Characterization of thymic nurse-cell lymphocytes, using an improved procedure for nurse-cell isolation. Dev. Immunol. 3, 103-112.
75. Lepesant, H., Reggio, H., Pierres, M., and Naquet, P. (1990). Mouse thymic epithelial cell lines interact with and select a CD3lowCD4+CD8+ thymocyte subset through an LFA-1-dependent adhesion-deadhesion mechanism. Int. Immunol. 2, 1021-1032.
76. Levine, J. S., Koh, J. S., Hartwell, D., and Beller, D. I. (1998). Adhesion elicits an intrinsic defect in interleukin-1 expression by macrophages from autoimmune-prone MRL mice. J. Autoimmun. 11, 141-150.
77. Li, Y., Pezzano, M., Philp, D., Reid, V., and Guyden, J. (1992). Thymic nurse cells exclusively bind and internalize CD4+CD8+ thymocytes. Cell. Immunol. 140, 495-506.
78. Lind, E. F., Prockop, S. E., Porritt, H. E., and Petrie, H. T. (2001). Mapping precursor movement through the postnatal thymus reveals specific microenvironments supporting defined stages of early lymphoid development. J. Exp. Med. 194, 127-134.
79. Lo, D., Ron, Y., and Sprent, J. (1986). Induction of MHC-restricted specificity and tolerance in the thymus. Immunol. Res. 5, 221-232.
80. Lorenz, R. G., and Allen, P. M. (1989a). Thymic cortical epithelial cells can present self-antigens in vivo. Nature 337, 560-562.
81. Lorenz, R. G., and Allen, P. M. (1989b). Thymic cortical epithelial cells lack full capacity for antigen presentation. Nature 340, 557-559.
82. Madden, K. S., and Felten, D. L. (1995). Experimental basis for neural-immune interactions. Physiol. Rev. 75, 77-106.
83. Martens, H., Robert, F., and Legros, J. J. (1992). Expression of functional neurohypophysial peptide receptors by murine immature and cytotoxic T cell lines. Prog. NeuroEndocrin. Immunol. 5, 31-39.
84. Martens, H., Kecha, O., and Charlet-Renard, C. (1997). Neurohypophysial peptides stimulate the phosphorylation of pre-T cell focal adhesion kinases. Neuroedocrinology 67, 282-289.
85. Montgomery, A. M., Reisfeld, R. A., and Cheresh, D. A. (1994). Integrin alpha v beta 3 rescues melanoma cells from apoptosis in three-dimensional dermal collagen. Proc. Natl. Acad. Sci. USA 91, 8856-8860.
86. Murao, K., Terpstra, V., Green, S. R., Kondratenko, N., Steinberg, D., and Quehenberger, O. (1997). Characterization of CLA-1, a human homologue of rodent scavenger receptor BI, as a receptor for high density lipoprotein and apoptotic thymocytes. J. Biol. Chem. 272, 17551-17557.
87. Nakashima, M., Mori, K., Maeda, K., Kishi, H., Hirata, K., Kawabuchi, M., and Watanabe, T. (1990). Selective elimination of double-positive immature thymocytes by a thymic epithelial cell line. Eur. J. Immunol. 20, 47-53.
88. Naquet, P., Naspetti, M., and Boyd, R. (1999). Development, organization and function of the thymic medulla in normal, immunodeficient or autoimmune mice. Semin. Immunol. 11, 47-55.
89. Nishimura, T., Takeuchi, Y., Ichimura, Y., Gao, X. H., Akatsuka, A., Tamaoki, N., Yagita, H., Okumura, K., and Habu, S. (1990). Thymic stromal cell clone with nursing activity supports the growth and differentiation of murine CD4+8+ thymocytes in vitro. J. Immunol. 145, 4012-4017.
90. Nonoyama, S., Nakayama, M., Shiohara, T., and Yata, J. (1989). Only dull CD3+ thymocytes bind to thymic epithelial cells. The binding is elicited by both CD2/LFA-3 and LFA-1/ICAM-1 interactions. Eur. J. Immunol. 19, 1631-1635.
91. Nossal, G. J. (1983). Cellular mechanisms of immunologic tolerance. Annu. Rev. Immunol. 1, 33-62.
92. Ohashi, P. S., Pircher, H., Burki, K., Zinkernagel, R. M., and Hengartner, H. (1990). Distinct sequence of negative or positive selection implied by thymocyte T-cell receptor densities. Nature 346, 861-863.
93. Oliveira-dos-Santos, A. J., Rieker-Geley, T., Recheis, H., and Wick, G. (1997). Murine thymic nurse cells and rosettes: Analysis of adhesion molecule expression using confocal microscopy and a simplified enrichment method. J. Histochem. Cytochem. 45, 1293-1297.
94. Owen, J. J., and Jenkinson, E. J. (1984). Early events in T lymphocyte genesis in the fetal thymus. Am. J. Anat. 170, 301-310.
95. Pearson, A. M. (1996). Scavenger receptors in innate immunity. Curr. Opin. Immunol. 8, 20-28.
96. Penninger, J., and Wick, G. (1992). Thymic nurse cell lymphocytes react against self major histocompatibility complex. Eur. J. Immunol. 22, 79-83.
97. Penninger, J., Rieker, T., Romani, N., Klima, J., Salvenmoser, W., Dietrich, H., Stossel, H., and Wick, G. (1994). Ultrastructural analysis of thymic nurse cell epithelium. Eur. J. Immunol. 24, 222-228.
98. Pezzano, M., Li, Y., Yang, Y. M., and Guyden, J. (1991). The immortalization of thymic nurse cells by SV40 virus. Cell. Immunol. 133, 434-445.
99. Pezzano, M., Li, Y., Philp, D., Omene, C., Cantey, M., Saunders, G., and Guyden, J. C. (1995). Thymic nurse cell rescue of early CD4+CD8+ thymocytes from apoptosis. Cell. Mol. Biol. (Noisy-le-grand) 41, 1099-1111.
100. Pezzano, M., Philp, D., Stephenson, S., Li, Y., Reid, V., Maitta, R., and Guyden, J. C. (1996). Positive selection by thymic nurse cells requires IL-1 beta and is associated with an increased Bcl-2 expression. Cell. Immunol. 169, 174-184.
101. Pezzano, M., King, K. D., Philp, D. D., Adeyemi, A., Gardiner, B., Yang, J., Samms, M., Boto, W., and Guyden, J. C. (1998). A thymic nurse cell-specific monoclonal antibody. Cell. Immunol. 185, 123-133.
102. Pezzano, M., Samms, M., and Guyden, J. C. (2001). TNF and Fas-induced apoptosis during negative selection in thymic nurse cells. Ethn. Dis. 11, 154-156.
103. Philp, D., Pezzano, M., Li, Y., Omene, C., Boto, W., and Guyden, J. (1993). The binding, internalization, and release of thymocytes by thymic nurse cells. Cell. Immunol. 148, 301-315.
104. Platt, N., Suzuki, H., Kurihara, Y., Kodama, T., and Gordon, S. (1996). Role for the class A macrophage scavenger receptor in the phagocytosis of apoptotic thymocytes in vitro. Proc. Natl. Acad. Sci. USA 93, 12456-12460.
105. Price, B. E., Rauch, J., Shia, M. A., Walsh, M. T., Lieberthal, W., Gilligan, H. M., O'Laughlin, T., Koh, J. S., and Levine, J. S. (1996). Anti-phospholipid autoantibodies bind to apoptotic, but not viable, thymocytes in a beta 2-glycoprotein I-dependent manner. J. Immunol. 157, 2201-2208.
106. Rebai, N., and Malissen, B. (1983). Structural and genetic analyses of HLA class I molecules using monoclonal xenoantibodies. Tissue Antigens 22, 107-117.
107. Reppert, S. M., and Uhl, G. R. (1987). Vasopressin messenger ribonucleic acid in supraoptic and suprachiasmatic nuclei: Appearance and circadian regulation during development. Endocrinology 120, 2483-2487.
108. Ritter, M. A., Sauvage, C. A., and Cotmore, S. F. (1981). The human thymus microenvironment: In vivo identification of thymic nurse cells and other antigenically-distinct subpopulations of epithelial cells. Immunology 44, 439-446.
109. Robert, F. R., Martens, H., Cormann, N., Benhida, A., Schoenen, J., and Geenen, V. (1992). The recognition of hypothalamo-neurohypophysial functions by developing T cells. Dev. Immunol. 2, 131-140.
110. Robey, E., and Fowlkes, B. J. (1994). Selective events in T cell development. Annu. Rev. Immunol. 12, 675-705.
111. Samms, M., Philp, D., Emanus, F., Osuji, O., Pezzano, M., and Guyden, J. C. (1999). Lysosomal-mediated degradation of apoptotic thymocytes within thymic nurse cells. Cell. Immunol. 197, 108-115.
112. Samms, M., Martinez, M., Fousse, S., Pezzano, M., and Guyden, J. C. (2001). Circulating macrophages as well as developing thymocytes are enclosed within thymic nurse cells. Cell. Immunol. 212,16-23.
113. Savill, J., Fadok, V., Henson, P., and Haslett, C. (1993). Phagocyte recognition of cells undergoing apoptosis. Immunol. Today 14, 131-136.
114. Savino, W., and Dardenne, M. (1995). Immune-neuroendocrine interactions. Immunol. Today 16, 318-322.
115. Savino, W., and Dardenne, M. (2000). Neuroendocrine control of thymus physiology. Endocr. Rev. 21, 412-443.
116. Savino, W., Boitard, C., Bach, J. F., and Dardenne, M. (1991). Studies on the thymus in nonobese diabetic mouse. I. Changes in the microenvironmental compartments. Lab. Invest. 64, 405-417.
117. Scherbaum, W. A., and Bottazzo, G. F. (1983). Autoantibodies to vasopressin cells in idiopathic diabetes insipidus: Evidence for an autoimmune variant. Lancet 1, 897-901.
118. Scollay, R., and Shortman, K. (1985). Identification of early stages of T lymphocyte development in the thymus cortex and medulla. J. Immunol. 134, 3632-3642.
119. Scupoli, M. T., Fiorini, E., Marchisio, P. C., Poffe, O., Tagliabue, E., Brentegani, M., Tridente, G., and Ramarli, D. (2000). Lymphoid adhesion promotes human thymic epithelial cell survival via NF-(kappa)B activation. J. Cell Sci. 113(Pt 1), 169-177.
120. Shortman, K., and Wu, L. (1996). Early T lymphocyte progenitors. Annu. Rev. Immunol. 14, 29-47.
121. Singer, K. H., Denning, S. M., Whichard, L. P., and Haynes, B. F. (1990). Thymocyte LFA-1 and thymic epithelial cell ICAM-1 molecules mediate binding of activated human thymocytes to thymic epithelial cells. J. Immunol. 144, 2931-2939.
122. Speiser, D. E., Lees, R. K., Hengartner, H., Zinkernagel, R. M., and MacDonald, H. R. (1989a). Positive and negative selection of T cell receptor V beta domains controlled by distinct cell populations in the thymus. J. Exp. Med. 170, 2165-2170.
123. Speiser, D. E., Schneider, R., Hengartner, H., MacDonald, H. R., and Zinkernagel, R. M. (1989b). Clonal deletion of self-reactive T cells in irradiation bone marrow chimeras and neonatally tolerant mice. Evidence for intercellular transfer of Mlsa. J. Exp. Med. 170, 595-600.
124. Sundler, F., Carraway, R. E., Hakanson, R., Alumets, J., and Dubois, M. P. (1978). Immunoreactive neurotensin and somatostatin in the chicken thymus. A chemical and histochemical study. Cell Tissue Res. 194, 367-376.
125. Surh, C. D., and Sprent, J. (1994). T-cell apoptosis detected in situ during positive and negative selection in the thymus. Nature 372, 100-103.
126. Takeoka, Y., Whitmer, K. J., Chen, S. Y., Ansari, A. A., Boyd, R. L., Shultz, L. D., Suehiro, S., and Gershwin, M. E. (1995a). Thymic epithelial cell abnormalities in (NZB H-2u)Fmice. Clin. Immunol. Immunopathol. 76, 297-307.
127. Takeoka, Y., Yoshida, S. H., Van de Water, J., Boyd, R., Suehiro, S., Ansari, A. A., and Gershwin, M. E. (1995b). Thymic microenvironmental abnormalities in MRL/MP-pr/lpr, BXSB/MpJ Yaa and C3H HeJ-gld/gld mice. J. Autoimmun. 8, 145-161.
128. Takeoka, Y., Chen, S. Y., Boyd, R. L., Tsuneyama, K., Taguchi, N., Morita, S., Yago, H., Suehiro, S., Ansari, A. A., Shultz, L. D., and Gershwin, M. E. (1997). A comparative analysis of the murine thymic microenvironment in normal, autoimmune, and immunodeficiency states. Dev. Immunol. 5, 79-89.
129. Takeoka, Y., Taguchi, N., Shultz, L., Boyd, R. L., Naiki, M., Ansari, A. A., and Gershwin, M. E. (1999). Apoptosis and the thymic microenvironment in murine lupus. J. Autoimmun. 13, 325-334.
130. Tatsumi, Y., Kumanogoh, A., Saitoh, M., Mizushima, Y., Kimura, K., Suzuki, S., Yagi, H., Horiuchi, A., Ogata, M., Hamaoka, T., et al. (1990). Differentiation of thymocytes from CD3-CD4-CD8-through CD3-CD4-CD8+ into more mature stages induced by a thymic stromal cell clone. Proc. Natl. Acad. Sci. USA 87, 2750-2754.
131. Thomas-Vaslin, V., Damotte, D., Coltey, M., Le Douarin, N. M., Coutinho, A., and Salaun, J. (1997). Abnormal T cell selection on nod thymic epithelium is sufficient to induce autoimmune manifestations in C57BL/6 athymic nude mice. Proc. Natl. Acad. Sci. USA 94, 4598-4603.
132. Toussaint-Demylle, D., Scheiff, J. M., and Haumont, S. (1990). Thymic nurse cells: Morphological study during their isolation from murine thymus. Cell Tissue Res. 261, 115-123.
133. van de Wijngaert, F. P., Rademakers, L. H., Schuurman, H. J., de Weger, R. A., and Kater, L. (1983). Identification and in situ localization of the "thymic nurse cell" in man. J. Immunol. 130, 2348-2351.
134. van Ewijk, W. (1988). Cell surface topography of thymic microenvironments. Lab. Invest. 59, 579-590.
135. van Ewijk, W. (1991). T-cell differentiation is influenced by thymic microenvironments. Annu. Rev. Immunol. 9, 591-615.
136. van Ewijk, W., van Soest, P. L., and van den Engh, G. J. (1981). Fluorescence analysis and anatomic distribution of mouse T lymphocyte subsets defined by monoclonal antibodies to the antigens Thy-1, Lyt-1, Lyt-2, and T-200. J. Immunol. 127, 2594-2604.
137. van Ewijk, W., Hollander, G., Terhorst, C., and Wang, B. (2000). Stepwise development of thymic microenvironments in vivo is regulated by thymocyte subsets. Development 127, 1583-1591.
138. Vanneste, Y., Thome, A. N., Vandersmissen, E., Charlet, C., Franchimont, D., Martens, H., Lhiaubet, A. M., Schimpff, R. M., Rostene, W., and Geenen, V. (1997). Identification of neurotensin-related peptides in human thymic epithelial cell membranes and relationship with major histocompatibility complex class I molecules. J. Neuroimmunol. 76, 161-166.
139. van Vliet, E., Melis, M., and van Ewijk, W. (1984). Immunohistology of thymic nurse cells. Cell. Immunol. 87, 101-109.
140. Verland, S., and Gammeltoft, S. (1989). Functional receptors for insulin-like growth factors I and II in rat thymocytes and mouse thymoma cells. Mol. Cell. Endocrinol. 67, 207-216.
141. Vicente, A., Varas, A., Moreno, J., Sacedon, R., Jimenez, E., and Zapata, A. G. (1995). Ontogeny of rat thymic macrophages. Phenotypic characterization and possible relationships between different cell subsets. Immunology 85, 99-105.
142. Villa-Verde, D. M., Lagrota-Candido, J. M., Vannier-Santos, M. A., Chammas, R., Brentani, R. R., and Savino, W. (1994). Extracellular matrix components of the mouse thymus microenvironment. IV. Modulation of thymic nurse cells by extracellular matrix ligands and receptors. Eur. J. Immunol. 24, 659-664.
143. Watanabe, Y., Naiki, M., Wilson, T., Godfrey, D., Chiang, B. L., Boyd, R., Ansari, A., and Gershwin, M. E. (1993). Thymic microenvironmental abnormalities and thymic selection in NZB.H-2bm12 mice. J. Immunol. 150, 4702-4712.
144. Weissman, I. L. (1985). Thymic lymphocyte differentiation and thymic leukemogenesis. Int. J. Radiat. Oncol. Biol. Phys. 11, 57-64.
145. Wekerle, H., and Ketelsen, U. P. (1980). Thymic nurse cells - Ia-bearing epithelium involved in T-lymphocyte differentiation? Nature 283, 402-404.
146. Wekerle, H., Ketelsen, U. P., and Ernst, M. (1980). Thymic nurse cells. Lymphoepithelial cell complexes in murine thymuses: Morphological and serological characterization. J. Exp. Med. 151, 925-944.
147. Whitlock, C. A., Tidmarsh, G. F., Muller-Sieburg, C., and Weissman, I. L. (1987). Bone marrow stromal cell lines with lymphopoietic activity express high levels of a pre-B neoplasia-associated molecule. Cell 48, 1009-1021.
148. Wick, G., Boyd, R., Hala, K., Thunold, S., and Kofler, H. (1982). Pathogenesis of spontaneous autoimmune thyroiditis in obese strain (OS) chickens. Clin. Exp. Immunol. 47, 1-18.
149. Wicker, L. S., Todd, J. A., and Peterson, L. B. (1995). Genetic control of autoimmune diabetes in the NOD mouse. Annu. Rev. Immunol. 13, 179-200.
150. Wiemann, M., and Ehret, G. (1993). Subcellular localization of immunoreactive oxytocin within thymic epithelial cells of the male mouse. Cell Tissue Res. 273, 79-87.