ACTH controls thymocyte homeostasis independent of glucocorticoids

FASEB Journal

Volumn 29, Issue 6, 2015, Pages 2526-2534

  Talaber, Gergely ^a   Tuckermann, Peter Jan ^b   Okret, Sam ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF ULM   (Germany)

Author keywords

Adrenalectomy; Glucocorticoid receptor ablation; Glucocorticoid resistance; Thymus

Indexed keywords

CORTICOTROPIN; GLUCOCORTICOID; MELANOCORTIN RECEPTOR; MELANOCORTIN RECEPTOR SUBTYPE 2; UNCLASSIFIED DRUG; DLL4 PROTEIN, MOUSE; GLUCOCORTICOID RECEPTOR; MELANOCORTIN 2 RECEPTOR; MEMBRANE PROTEIN; SIGNAL PEPTIDE;

ADAPTIVE IMMUNITY; ADRENALECTOMY; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; CORTICOTROPIN RELEASE; DENDRITIC CELL; EPITHELIUM; HOMEOSTASIS; HOUSEKEEPING GENE; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; KNOCKOUT MOUSE; MOUSE; NONHUMAN; ORGAN CULTURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA ISOLATION; THYMOCYTE; THYMUS; ADRENAL GLAND; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECTS; EMBRYOLOGY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; GENETICS; METABOLISM; ORGAN CULTURE TECHNIQUE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SURGERY; TRANSGENIC MOUSE;

MUS;

ADRENAL GLANDS; ADRENALECTOMY; ADRENOCORTICOTROPIC HORMONE; ANIMALS; APOPTOSIS; CELL PROLIFERATION; CELLS, CULTURED; GENE EXPRESSION; GLUCOCORTICOIDS; HOMEOSTASIS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROSCOPY, FLUORESCENCE; ORGAN CULTURE TECHNIQUES; RECEPTOR, MELANOCORTIN, TYPE 2; RECEPTORS, GLUCOCORTICOID; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; THYMOCYTES; THYMUS GLAND;

EID: 84933565887     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-268508     Document Type: Article

References (42)

1. Shah, D. K., and Zúñiga-Pflücker, J. C. (2014) An overview of the intrathymic intricacies of T cell development. J. Immunol. 192, 4017-4023
2. Klein, L., Kyewski, B., Allen, P. M., and Hogquist, K. A. (2014) Positive and negative selection of the T cell repertoire: what thymocytes see (and don't see). Nat. Rev. Immunol. 14, 377-391
3. Boehm, T., and Swann, J. B. (2013) Thymus involution and regeneration: two sides of the same coin? Nat. Rev. Immunol. 13, 831-838
4. Herold, M. J., McPherson, K. G., and Reichardt, H. M. (2006) Glucocorticoids in T cell apoptosis and function. Cell. Mol. Life Sci. 63, 60-72
5. Rocha, B. (1985) The effects of stress in normal and adrenalectomized mice. Eur. J. Immunol. 15, 1131-1135
6. Jaffe, H. L. (1924) The influence of the suprarenal gland on the thymus: III. Stimulation of the growth of the thymus gland following double suprarenalectomy in young rats. J. Exp. Med. 40, 753-759
7. Jaffe, H. L. (1924) The influence of the suprarenal gland on the thymus: II. Direct evidence of regeneration of the involuted thymus following double suprarenalectomy in the rat. J. Exp. Med. 40, 619-625
8. Jaffe, H. L. (1924) The influence of the suprarenal gland on the thymus: I. Regeneration of the thymus following double suprarenalectomy in the rat. J. Exp. Med. 40, 325-342
9. Padgett, E. L., Sibley, D. A., and Jerrells, T. R. (2000) Effect of adrenalectomy on ethanol-associated changes in lymphocyte cell numbers and subpopulations in thymus, spleen, and gutassociated lymphoid tissues. Int. J. Immunopharmacol. 22, 285-298
10. Kawiak, J., Hoser, G., Malendowicz, L. K., Miks, B., and Skurzak, H. (1996) Thymocyte and splenocyte subpopulations in normal and leukemia-bearing mice after adrenalectomy. Folia Histochem. Cytobiol. 34, 75-78
11. Wiegers, G. J., Knoflach, M., Böck, G., Niederegger, H., Dietrich, H., Falus, A., Boyd, R., and Wick, G. (2001) CD4(+)CD8(+)TCR (low) thymocytes express low levels of glucocorticoid receptors while being sensitive to glucocorticoid-induced apoptosis. Eur. J. Immunol. 31, 2293-2301
12. Berki, T., Pálinkás, L., Boldizsár, F., and Németh, P. (2002) Glucocorticoid (GC) sensitivity and GC receptor expression differ in thymocyte subpopulations. Int. Immunol. 14, 463-469
13. Kyrou, I., and Tsigos, C. (2009) Stress hormones: physiological stress and regulation of metabolism. Curr. Opin. Pharmacol. 9, 787-793
14. Bornstein, S. R., and Chrousos, G. P. (1999) Clinical review 104: adrenocorticotropin (ACTH)- and non-ACTH-mediated regulation of the adrenal cortex: neural and immune inputs. J. Clin. Endocrinol. Metab. 84, 1729-1736
15. Xing, Y., Parker, C. R., Edwards, M., and Rainey, W. E. (2010) ACTH is a potent regulator of gene expression in human adrenal cells. J. Mol. Endocrinol. 45, 59-68
16. Hoeflich, A., and Bielohuby, M. (2009) Mechanisms of adrenal gland growth: signal integration by extracellular signal regulated kinases1/2. J. Mol. Endocrinol. 42, 191-203
17. Zaidi, M., Sun, L., Robinson, L. J., Tourkova, I. L., Liu, L., Wang, Y., Zhu, L. L., Liu, X., Li, J., Peng, Y., Yang, G., Shi, X., Levine, A., Iqbal, J., Yaroslavskiy, B. B., Isales, C., and Blair, H. C. (2010) ACTH protects against glucocorticoid-induced osteonecrosis of bone. Proc. Natl. Acad. Sci. USA 107, 8782-8787
18. Benjamins, J. A., Nedelkoska, L., Bealmear, B., and Lisak, R. P. (2013) ACTH protects mature oligodendroglia from excitotoxic and inflammation-related damage in vitro. Glia 61, 1206-1217
19. Si, J., Ge, Y., Zhuang, S., Wang, L. J., Chen, S., and Gong, R. (2013) Adrenocorticotropic hormone ameliorates acute kidney injury by steroidogenic-dependent and -independent mechanisms. Kidney Int. 83, 635-646
20. Pazirandeh, A., Xue, Y., Rafter, I., Sjovall, J., Jondal, M., and Okret, S. (1999) Paracrine glucocorticoid activity produced by mouse thymic epithelial cells. FASEB J. 13, 893-901
21. Qiao, S., Okret, S., and Jondal, M. (2009) Thymocyte-synthesized glucocorticoids play a role in thymocyte homeostasis and are down-regulated by adrenocorticotropic hormone. Endocrinology 150, 4163-4169
22. Vacchio, M. S., Papadopoulos, V., and Ashwell, J. D. (1994) Steroid production in the thymus: implications for thymocyte selection. J. Exp. Med. 179, 1835-1846
23. Talabér, G., Jondal, M., and Okret, S. (2013) Extra-adrenal glucocorticoid synthesis: immune regulation and aspects on local organ homeostasis. Mol. Cell. Endocrinol. 380, 89-98
24. Taves, M. D., Gomez-Sanchez, C. E., and Soma, K. K. (2011) Extra-adrenal glucocorticoids and mineralocorticoids: evidence for local synthesis, regulation, and function. Am. J. Physiol. Endocrinol. Metab. 301, E11-E24
25. Liddicoat, D. R., Purton, J. F., Cole, T. J., and Godfrey, D. I. (2014) Glucocorticoid-mediated repression of T-cell receptor signalling is impaired in glucocorticoid receptor exon 2-disrupted mice. Immunol. Cell Biol. 92, 148-155
26. Tuckermann, J. P., Kleiman, A., Moriggl, R., Spanbroek, R., Neumann, A., Illing, A., Clausen, B. E., Stride, B., Förster, I., Habenicht, A. J., Reichardt, H. M., Tronche, F., Schmid, W., and Schütz, G. (2007) Macrophages and neutrophils are the targets for immune suppression by glucocorticoids in contact allergy. J. Clin. Invest. 117, 1381-1390
27. Farr, A., Nelson, A., Truex, J., and Hosier, S. (1991) Epithelial heterogeneity in the murine thymus: a cell surface glycoprotein expressed by subcapsular and medullary epithelium. J. Histochem. Cytochem. 39, 645-653
28. Gavet, O., and Pines, J. (2010) Progressive activation of CyclinB1- Cdk1 coordinates entry to mitosis. Dev. Cell 18, 533-543
29. Cooray, S. N., and Clark, A. J. (2011) Melanocortin receptors and their accessory proteins. Mol. Cell. Endocrinol. 331, 215-221
30. Hozumi, K., Mailhos, C., Negishi, N., Hirano, K., Yahata, T., Ando, K., Zuklys, S., Holländer, G. A., Shima, D. T., and Habu, S. (2008) Delta-like 4 is indispensable in thymic environment specific for T cell development. J. Exp. Med. 205, 2507-2513
31. Stojić-Vukanić, Z., Rauski, A., Kosec, D., Radojević, K., Pilipović, I., and Leposavić, G. (2009) Dysregulation of T-cell development in adrenal glucocorticoid-deprived rats. Exp. Biol. Med. (Maywood) 234, 1067-1074
32. Pruett, S. B., and Padgett, E. L. (2004) Thymus-derived glucocorticoids are insufficient for normal thymus homeostasis in the adult mouse. BMC Immunol. 5, 24
33. Batanero, E., de Leeuw, F. E., Jansen, G. H., van Wichen, D. F., Huber, J., and Schuurman, H. J. (1992) The neural and neuroendocrine component of the human thymus. II. Hormone immunoreactivity. Brain Behav. Immun. 6, 249-264
34. Wu, L., and Shortman, K. (2005) Heterogeneity of thymic dendritic cells. Semin. Immunol. 17, 304-312
35. Esashi, E., Sekiguchi, T., Ito, H., Koyasu, S., and Miyajima, A. (2003) Cutting edge: a possible role for CD4+ thymic macrophages as professional scavengers of apoptotic thymocytes. J. Immunol. 171, 2773-2777
36. Gray, D. H., Tull, D., Ueno, T., Seach, N., Classon, B. J., Chidgey, A., McConville, M. J., and Boyd, R. L. (2007) A unique thymic fibroblast population revealed by the monoclonal antibody MTS-15. J. Immunol. 178, 4956-4965
37. García-Peydró, M., de Yébenes, V. G., and Toribio, M. L. (2006) Notch1 and IL-7 receptor interplay maintains proliferation of human thymic progenitors while suppressing non-T cell fates. J. Immunol. 177, 3711-3720
38. Ferrero, I., Koch, U., Claudinot, S., Favre, S., Radtke, F., Luther, S. A., and MacDonald, H. R. (2013) DL4-mediated Notch signaling is required for the development of fetal ab and gd T cells. Eur. J. Immunol. 43, 2845-2853
39. Johnson, E. W., Hughes, Jr., T. K., and Smith, E. M. (2001) ACTH receptor distribution and modulation among murine mononuclear leukocyte populations. J. Biol. Regul. Homeost. Agents 15, 156-162
40. Vezys, V., Masopust, D., Kemball, C. C., Barber, D. L., O'Mara, L. A., Larsen, C. P., Pearson, T. C., Ahmed, R., and Lukacher, A. E. (2006) Continuous recruitment of naive T cells contributes to heterogeneity of antiviral CD8 T cells during persistent infection. J. Exp. Med. 203, 2263-2269
41. Ferrando-Martínez, S., Romero-Sánchez, M. C., Solana, R., Delgado, J., de la Rosa, R., Muñoz-Fernández, M. A., Ruiz-Mateos, E., and Leal, M. (2013) Thymic function failure and C-reactive protein levels are independent predictors of allcause mortality in healthy elderly humans. Age (Dordr.) 35, 251-259
42. Weyand, C. M., Fulbright, J. W., and Goronzy, J. J. (2003) Immunosenescence, autoimmunity, and rheumatoid arthritis. Exp. Gerontol. 38, 833-841