Advertisement

Regulation of Apoptosis via Steroid Receptors

  • M. Iwata
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 200)

Abstract

Steroid hormones play essential roles in a variety of physiological processes including embryonic development, sexual differentiation and maturation, and metamorphosis. The homeostatic regulation of metabolism and cell turnover that determines tissue sizes and shapes are also under the influence of these hormones. Apoptosis is involved in many of these phenomena, The pharmacological or surgical manipulation of animals to change steroid levels often causes involution or enlargement of certain tissues partly through the enhancement or inhibition of apoptosis. For example, an elevation of blood glucocorticoid level, by an injection of glucocorticoids or by excessive stress, causes thymus involution due to apoptosis in cortical immature thymocytes (Claman 1972). By contrast, adrenalectomy of mice causes not only depletion of glucocorticoids from the plasma but also a marked increase in the thymus size (Shortman and Jackson 1974). Glucocorticoid-induced apoptosis is dependent on the binding of glucocorticoids to glucocorticoid hormone receptors (GRs), which is also required in the general effects of steroids (Duval et al. 1984). The steroid receptors such as GR, mineralcorticoid receptors, progesterone receptors, androgen receptors, and estrogen receptors are members of a superfamily of ligand-inducible transcription factors. The steroid receptor superfamily also includes retinoic acid receptors, thyroid hormone receptors, vitamin D3 receptors, ecdysone receptors, and COUP transcription factor. They are related to v-erbA oncogene.

Keywords

Retinoic Acid Okadaic Acid Palatal Shelf Thymic Selection Thymocyte Apoptosis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alegre M, Vandenabeele P, Flamand V, Moser M, Leo O, Abramowicz D, Urbain J, Fiers W, Goldman M (1990) Hypothermia and hypoglycemia induced by anti-CD3 monoclonal antibody in mice: role of tumor necrosis factor. Eur J Immunol 20: 707–710PubMedCrossRefGoogle Scholar
  2. Allbritton NL, Verret CR, Wolley RC, Eisen HN (1988) Calcium ion concentrations and DNA fragmentation in target cell destruction by murine cytotoxic T lymphocytes. J Exp Med 167: 514–527PubMedCrossRefGoogle Scholar
  3. Allen PM (1994) Peptides in positive and negative selection: a delicate balance. Cell 76: 593–596PubMedCrossRefGoogle Scholar
  4. Alnemri ES, Litwack G (1990) Activation of internucleosomal DNA cleavage in human CEM lymphocytes by glucocorticoid and novobiocin evidence for a non-Ca2+-requiring mechanism(s). J Biol Chem 265: 17323–17333PubMedGoogle Scholar
  5. Bansal N, Houle AG, Melnykovych G (1990) Dexamethasone-induced killing of neoplastic cells of lymphoid derivation: lack of early calcium involvement. J Cell Physiol 143: 105–109PubMedCrossRefGoogle Scholar
  6. Barr IG, Khalid BAK, Pearce P, Toh BH, Bartlett PF, Scollay RG, Funder JW (1982) Dihydrotestosterone and estradiol deplete corticosensitive thymocytes lacking in receptors for these hormones. J Immunol 128: 2825–2828PubMedGoogle Scholar
  7. Bonner JJ (1984) The H-2 genetic complex, dexamethasone-induced cleft palate and other craniofacial anomalies. Curr Top Dev Biol 19: 193–215PubMedCrossRefGoogle Scholar
  8. Breedlove SM (1992) Sexual dimorphism in the vertebrate nervous system. J Neurosci 12: 4133–4142PubMedGoogle Scholar
  9. Brown OG, Sun XM, Cohen GM (1993) Dexamethasone-induced apoptosis involves cleavage of DNA to large fragments prior to internucleosomal fragmentation. J Biol Chem 268: 3037–3039PubMedGoogle Scholar
  10. Buttke TM, Sandstrom PA (1994) Oxidative stress as a mediator of apoptosis. Immunol Today 15: 7–10PubMedCrossRefGoogle Scholar
  11. Carrera AC, Baker C, Roberts TM, Pardoll DM (1992) Tyrosine kinase triggering in thymocytes undergoing positive selection. Eur J Immunol 22: 2289–2294PubMedCrossRefGoogle Scholar
  12. Claman HN (1972) Corticosteroids and lymphoid cells. N Engl J Med 287: 388–397PubMedCrossRefGoogle Scholar
  13. Cohen JJ, Duke RC (1984) Glucocorticoid activation of a calcium-dependent endonuclease in thymocyte nuclei leads to cell death. J Immunol 132: 38–42PubMedGoogle Scholar
  14. Cohen GM, Sun XM, Snowden RT, Dinsdale D, Skilleter DN (1992) Key morphological features of apoptosis may occur in the absence of internucleosomal DNA fragmentation. Biochem J 286: 331–334PubMedGoogle Scholar
  15. Deckers CLP, Lyons AB, Samuel K, Sanderson A, Maddy AH (1993) Alternative pathways of apoptosis induced by methylprednisolone and valinomycin analyzed by flow cytometry. Exp Cell Res 208: 362–370PubMedCrossRefGoogle Scholar
  16. Durant S (1986) In vivo effects of catecholamines and glucacorticoids on mouse thymic cAMP content and thymolysis. Cell Immunol 102: 136–143PubMedCrossRefGoogle Scholar
  17. Duval D, Durant S, Homo-Delarche F (1984) Effect of antiglucocorticoids on dexamethasone-induced inhibition of uridine incorporation and cell lysis in isolated mouse thymocytes. J Steroid Biochem 20: 283–287PubMedCrossRefGoogle Scholar
  18. Egerton M, Scollay R, Shortman K (1990) Kinetics of mature T-cell development in the thymus. Proc Natl Acad Sci USA 87: 2579–2582PubMedCrossRefGoogle Scholar
  19. Ferran C, Sheeha K, Dy M, Schreiber R, Merite S, Landais P, Noel LH, Grau G, Bluestone J, Bach JF, Chatenoud L (1990) Cytokine-related syndrome following injection of anti-CD3 monoclonal antibody further evidence for transient in vivo T cell activation. Eur J Immunol 20: 509–515PubMedCrossRefGoogle Scholar
  20. Fine JS, Kruisbeek AM (1991) The role of LFA-1/ICAM-1 interactions during murine lymphocyte development. J Immunol 147: 2852–2859PubMedGoogle Scholar
  21. Flomerfelt FA, Briehl MM, Dowd DR, Dieken ES, Miesfeld RL (1993) Elevated glutathione S-transferase gene expression is an early event during steroid-induced lymphocyte apoptosis. J Cell Physiol 154: 573–581PubMedCrossRefGoogle Scholar
  22. Goldman AS (1984) Biochemical mechanism of glucocorticoid and phenytoin-induced cleft palate. Curr Top Dev Biol 19: 217–239PubMedCrossRefGoogle Scholar
  23. Gonzalo JA, Gonzalez-Garcia A, Martinez A C, Kroemer G (1993) Glucocorticoid mediated control of the activation and clonal detetion of peripheral T cells in vivo. J Exp Med 177: 1239–1246PubMedCrossRefGoogle Scholar
  24. Gonzalo JA, Gonzalez-Garcia A, Kalland T, Hedlund G, Martinez AC, Kroemer G (1994) Linomide inhibits programmed cell death of peripheral T cells in vivo. Eur J Immunol 24: 48–52PubMedCrossRefGoogle Scholar
  25. Gupta C, Katsumata M, Goldman AS, Herold R, Piddington R (1984) Glucocorticoid induced phospholipase A2 inhibitory proteins mediate glucocorticoid teratogenicity in vitro. Proc Natl Acad USA 81: 1140–1143CrossRefGoogle Scholar
  26. Hockenbery DM, Oltval ZN, Yin XM, Milliman CL, Korsmeyer SJ (1993) Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 75: 241–251PubMedCrossRefGoogle Scholar
  27. Homo F, Duval D, Hatzfeld J, Evrard C (1980) Glucocorticoid sensitive and resistant cell populations in the mouse thymus. J Steroid Biochem 13: 135–143PubMedCrossRefGoogle Scholar
  28. Hoshino J, Beckmann G, Kroger H (1993) 3-Aminobenzamide protects the mouse thymocytes in vitro from dexamethasone-mediated apoptotic cell death and cytolysis without changing DNA strand breakage. J Steroid Biochem Mol Biol 44: 113–119PubMedCrossRefGoogle Scholar
  29. Hugo P, Boyd RL, Waanders GA, Scollay R (1991) CD4+CD8+CD3high thymocytes appear transiently during ontogeny: evidence from phenotypic and functional studies. Eur J Immunol 21: 2655–2660PubMedCrossRefGoogle Scholar
  30. Iseki R, Mukai M, Iwata M (1991) Regulation of T lymphocyte apoptosis: Signals for the antagonism between activation- and glucocorticoid-induced death. J Immunol 147: 4286–4292PubMedGoogle Scholar
  31. Iseki R, Kudo Y, Iwata M (1993) Early mobilization of Ca2+ is not required for glucocorticoid-induced apoptosis in thymocytes. J Immunol 151: 5198–5207PubMedGoogle Scholar
  32. Iwata M, Hanaoka S, Sato K (1991) Rescue of thymocytes and T cell hybridomas from glucocorticoid-induced apoptosis by stimulation via the T cell receptor/CD3 complex: a possible in vitro model for positive selection of the T cell repertoire. Eur J Immunol 21: 643–648PubMedCrossRefGoogle Scholar
  33. Iwata M, Mukai M, Nakai Y, Iseki R (1992) Retinoic acids inhibit activation-induced apoptosis in T cell hybridomas and thymocytes. J Immunol 149: 3302–3308PubMedGoogle Scholar
  34. Iwata M, Iseki R. Kudo Y (1993) Regulation of thymocyte apoptosis: glucocorticoid-induced death and its inhibition by T-cell receptor/CD3 complex-mediated stimulation. In: Lavin ML, Waiters D (ed) Programmed cell death: the cellular and molecular biology of apoptosis. Harwood Academic Publishers, Chur, Switzerland, pp 31–44Google Scholar
  35. Iwata M, Iseki R, Sato K, Tozawa Y, Ohoka Y (1994) Involvement of protein kinase C-ε in glucocorticoid induced apoptosis in thymocytes. Int Immunol 6: 431–438PubMedCrossRefGoogle Scholar
  36. Jondal M, Okret S, McConkey D (1993) Killing of immature CD4+CD8+ thymocytes in vivo by anti-CD3 or 5′-(N-ethyl)-carboxamido adenosine is blocked by glucocorticoid receptor antagonist RU-486. Eur J Immunol 23: 1246–1250PubMedCrossRefGoogle Scholar
  37. Jones DP, McConkey DJ, Nicotera P, Orrenius S (1989) Calcium-activated DNA fragmentation in rat liver nuclei. J Biol Chem 264: 6398–6403PubMedGoogle Scholar
  38. Kaiser N, Edelman IS (1977) Calcium dependence of glucocorticoid-induced lymphocytolysis. Proc Natl Acad Sci USA 74: 638–642PubMedCrossRefGoogle Scholar
  39. Konishi M, Akutagawa E (1985) Neuronal growth, atrophy and death in a sexually dimorphic song nucleus in the zebra finch brain. Nature 315: 145–147PubMedCrossRefGoogle Scholar
  40. Kyprianou N, English HF, Davidson NE, Isaacs JT (1991) Programmed cell death during regression of the MCF-7 human breast cancer following estrogen ablation. Cancer Res 51: 162–166PubMedGoogle Scholar
  41. Leger JG, Montpetit ML, Tenniswood MP (1987) Characterization and cloning of androgen-repressed mRNAs from rat ventral prostate. Biochem Biophys Res Commun 147: 196–203PubMedCrossRefGoogle Scholar
  42. MacDonald HR, Hengartner H, Pedrezzini T (1988) Intrathymic deletion of self-reactive cells prevented by neonatal anti-CD4 antibody treatment. Nature 335: 174–176PubMedCrossRefGoogle Scholar
  43. Malkovsky M, Medawar PB, Thatcher DR, Toy J, Hunt R, Rayfield LS, Dore C (1985) Acquired immunological tolerance of foreign cells is impaired by recombinant interleukin 2 or vitamin A acetate. Proc Natl Acad Sci USA 82: 536–538PubMedCrossRefGoogle Scholar
  44. McCarthy SA, Cacchione RN, Mainwaring MS, Cairns JS (1992) The effects of immunosuppressive drugs on the regulation of activation-induced apoptotic cell death in thymocytes. Transplantation 54: 543–547PubMedCrossRefGoogle Scholar
  45. McConkey DJ, Nicotera P, Hartzell P, Bellomo G, Wyllie AH, Orrenius S (1989) Glucocorticoids activate a suicide process in thymocytes through an elevation of cytosolic Ca2+ concentration. Arch Biochem Biophys 269: 365–370PubMedCrossRefGoogle Scholar
  46. McConkey DJ, Orrenius S, Jondal M (1990) Agents that elevates cAMP stimulate DNA fragmentation in thymocytes. J Immunol 145: 1227–1230PubMedGoogle Scholar
  47. McConkey DJ, Orrenius S, Okret S, Jondal M (1993) Cycic AMP potentiates glueocorticoid-induced endogenous endonuclease activation in thymocytes. FASEB J 7: 580–585PubMedGoogle Scholar
  48. Murakami S, Arai Y (1989) Neuronal death in the developing sexulally dimorphic periventricular nucleus of the preoptic area in the female rat: effect of neonatal androgen treatment. Neurosci Lett 102: 185–190PubMedCrossRefGoogle Scholar
  49. Nicholson ML, Young DA (1979) Independence of the lethal actions of glucocorticoids on lymphoid cells from possible hormone effects on calcium uptake. J Supramol Struct 10: 165–174PubMedCrossRefGoogle Scholar
  50. Nicotera P, Bellomo G, Orrenius S (1992) Calcium-mediated mechanisms in chemically induced cell death. Annu Rev Pharmacol Toxicol 32: 449–470PubMedCrossRefGoogle Scholar
  51. Nordeen EJ, Nordeen KW, Sengelaub DR, Arnold AP (1985) Androgens prevent normally occurring cell death in a sexually dimorphic spinal nucleus. Science 229: 671–673PubMedCrossRefGoogle Scholar
  52. Ohoka Y, Nakai Y, Mukai M, Iwata M (1993) Okadaic acid inhibits glucocorticoid-induced apoptosis in T cell hybridomas at its late stage. Biochem Biophys Res Commun 197: 916–921PubMedCrossRefGoogle Scholar
  53. Ojeda F, Guarda MI, Maldonado C, Foich H (1990) Protein kinase C involvement in thymocyte apoptosis induced by hydrocortisone. Cell Immunol 125: 535–539PubMedCrossRefGoogle Scholar
  54. Owens GP, Hahn WE, Cohen JJ (1991) Identification of mRNAs associated with programmed cell death in immature thymocytes. Mol Cell Biol 11: 4177–4188PubMedGoogle Scholar
  55. Perandones CE, Illiera VA, Peckham D, Stunz LL, Ashman RF (1993) Regulation of apoptosis in vitro in mature murine spleen T cells. J Immunol 151: 3521–3529PubMedGoogle Scholar
  56. Pla M, Zakany J, Fachet J (1976) H-2 influence on corticosteroid effects on thymus cells. Folia Biol (Praha) 22: 49–50Google Scholar
  57. Pratt RM, Kim CS, Grove RI (1984) Role of glucocorticoids and epidermal growth factor in normal and abnormal palatal devetopment. Curr Top Dev Biol 19: 81–101PubMedCrossRefGoogle Scholar
  58. Pratt WB, Sanchez ER, Bresnick EH, Meshinchi S, Scherrer LC, Dalman FC, Welsh MJ (1989) Interaction of the glucocorticoid receptor with Mr 90,000 heat shock protein: An evolving model of ligand-mediated receptor transformation and translocation. Cancer Res [Suppl] 49: 2222s–2229sPubMedGoogle Scholar
  59. Preston RR (1990) A magnesium current in Paramecium. Science 250: 285–288PubMedCrossRefGoogle Scholar
  60. Punt JA, Hosono M, Hashimoto Y (1993) CD4+/CD8- thymocytes dominate the fetal thymus treated with a combination of anti-T cell receptor-β and anti-CD4 antibodies. J Immunol 151: 1290–1302PubMedGoogle Scholar
  61. Ramakrishnan N, Catravas GN (1992) N-(2-mercaptoethyl)-1,3-propanediamine (WR-1065) protects thymocytes from programed cell death. J Immunol 148: 1817–1821PubMedGoogle Scholar
  62. Ramsdell F, Fowlkes BJ (1989) Engagement of CD4 and CD8 accessory molecules is required for T-cell maturation. J Immunol 143: 1467–1471PubMedGoogle Scholar
  63. Saltzman AG, Hiipakka RA, Chang C, Liao S (1987) Androgen repression of the production of a 29-Kilodalton protein and its mRNA in the rat ventral prostate. J Biol Chem 262: 432–437PubMedGoogle Scholar
  64. Schraufstatter IU, Hyslop PA, Hinshaw DB, Spragg RG, Sklar LA, Cochrane CG (1986) Hydrogen peroxide-induced injury of cells and its prevention by inhibitors of poly(ADP-ribose) polymerase. Proc Natl Acad Sci USA 83: 4908–4912PubMedCrossRefGoogle Scholar
  65. Schwartz LM, Osborne BA (1993) Programmed cell death, apoptosis and killer genes. Immunol Today 14: 582–590PubMedCrossRefGoogle Scholar
  66. Schwartzman RA, Cidlowski JA (1993) Mechanism of tissue-specific induction of intemucleosomal deoxyribonucleic acid cleavage activity and apoptosis by glucocorticoids. Endocrinology 133: 591–599PubMedCrossRefGoogle Scholar
  67. Shi Y, Sahai BM, Green DR (1989) Cyclosporin A inhibits activation-induced death in T cell hybridomas and in thymocytes. Nature 339: 625–626PubMedCrossRefGoogle Scholar
  68. Shi Y, Glynn JM, Guilbert LJ, Cotter TG, Bissonnette RP, Green DR (1992) Role for c-myc in activation-induced apoptotic cell death in T cell hybridomas. Science 257: 212–214PubMedCrossRefGoogle Scholar
  69. Shortman K, Jackson H (1974) The differentiation of T lymphocytes. 1. Proliferation kinetics and interrelationships of subpopulations of mouse thymus cells. Cell Immunol 12: 230–246PubMedCrossRefGoogle Scholar
  70. Sloviter RS, Sollas AL, Dean E, Noubort S (1993) Adrenalectomy-induced granule cell degeneration in the rat hippocampal dentate gyrus: characterization of an in vivo model of controlled neuronal death. J Comparative Neurol 330: 324–336CrossRefGoogle Scholar
  71. Sun DY, Jiang S, Zheng LM, Ojcius DM, Young JDE (1994) Separate metabolic pathways teading to DNA fragmentation and apoptotic chromatin condensation. J Exp Med 179: 559–568PubMedCrossRefGoogle Scholar
  72. Suzuki K, Kizaki H, Tadakuma T, Ishimura Y (1990) 12-O-tetradecanoylphorbol 13-acetate potentiates the action of cAMP in inducing DNA cleavage in thymocytes. Biochem Biophys Res Commun 171: 827–831PubMedCrossRefGoogle Scholar
  73. Tyan ML (1979) Genetic control of hydrocortisone induced thymus atrophy. Immunogenetics 8: 177–181CrossRefGoogle Scholar
  74. Wilson JD, George FW, Griffen JE (1981) The harmonal control of sexual development. Science 211: 1278–1284PubMedCrossRefGoogle Scholar
  75. Wyllie AH (1980) Glucocorticoid-induced thymocyte apoptosis is associated with endogenous ondonuclease activation. Nature 284: 555–556PubMedCrossRefGoogle Scholar
  76. Wyllie AH, Kerr JFR, Currie AR (1980) Cell death: the significance of apoptosis. Int Rev Cytol 68: 251–306PubMedCrossRefGoogle Scholar
  77. Wyllie AH, Morris RG, Smith AL, Dunlop D (1984) Chromatin cleavage in apoptosis: association with condensed chromatin morphology and dependence on macromolecular synthesis. J Pathol 142: 67–77PubMedCrossRefGoogle Scholar
  78. Yang Y, Vacchio MS, Ashwell JD (1993) 9-c/s-Retinoic acid inhibits activation-driven T-cell apoptosis: implication for retinoid X receptor involvement in thymocyte development. Proc Natl Acad Sci USA 90: 6170–6174PubMedCrossRefGoogle Scholar
  79. Zacharchuk CM, Mercep M, Chakraborti PK, Simons SS, Ashwell JD (1990) Programmed T lymphocyte death: cell activation- and steroid-induced pathways are mutually antagonistic. J Immunol 145: 4037–4045PubMedGoogle Scholar
  80. Zubiaga AM, Munoz E, Huber BT (1992) IL-4 and IL-2 selectively rescue Th cell subsets from glucocorticoid-induced apoptosis. J Immunol 149: 107–112PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1995

Authors and Affiliations

  • M. Iwata
    • 1
  1. 1.Mitsubishi Kasei Institute of Life SciencesMachida-shi, Tokyo, 194Japan

Personalised recommendations