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Comparison of the mechanisms of nongenomic actions of thyroid hormone and steroid hormones

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Abstract

Steroids and thyroid hormone are thought primarily to act via binding to hormonespecific nuclear receptor superfamily members. The nuclear ligand-receptor complexes then initiate transcriptional activity. Actions of steroids and iodothyronines that are nongenomic or extranuclear in mechanism have been recognized recently and new insights into such mechanisms are available. Despite their distinct structures and biologic effects, the two families of hormones have similarities in the mechanisms of their nongenomic actions. That is, both steroids and thyroid hormone appear to interact with specific cell surface G protein-coupled receptors and to activate signal transducing kinases such as those involved in the mitogen-activated protein kinase (MAPK) pathway. Much is known about the ability of certain steroids such as estrogen and mineralocorticoids to increase [Ca2+]i acutely and stimulation of the MAPK cascade by L-T4 appears to depend upon a hormone-induced increase in [Ca2+]i via phosphoinositide pathway activation. At least in the case of iodothyronines, hormone activation of the MAPK pathway modulates the cellular activities of certain cytokines and growth factors. One of the two cell surface estrogen receptors (ERs) may be an expression of the same transcript as that for nuclear ER, whereas the mineralocorticoid and progesteronebinding proteins in the plasma membrane appear to be products of genes different from those of nuclear receptors. Iodothyronine structure-activity relationships at the plasma membrane binding site for thyroid hormone suggest that the cell surface receptor for T4 that also binds 3,5,3′-triiodo-L-T3 is different from the nuclear T3 receptor (TR). There are interfaces of nongenomic and genomic mechanisms for both steroids and thyroid hormone. For example, by nongenomic mechanisms, estrogen and thyroid hormone can promote serine phosphorylation, respectively, of nuclear ER and TR. Transcriptional activity of the nuclear receptor proteins can be altered by such phosphorylation.

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References

  1. Lowe W.L., Jr., Pestell R.G., Madison L.D., Jameson J.L. Mechanisms of hormone action. In: Jameson J.L., Collins F.S. (Eds.), Principles of molecular medicine. Humana Press, Totowa, 1998, p. 419.

    Chapter  Google Scholar 

  2. Beato M. Gene regulation by steroid hormones. Cell 1989, 56: 335–344.

    Article  CAS  PubMed  Google Scholar 

  3. Chin W.W., Yen P.M. Molecular mechanisms of nuclear thyroid hormone action. In: Braverman L.E. (Ed.), Contemporary endocrinology: Diseases of the thyroid. Humana Press, Totowa, 1997, p. 1.

    Google Scholar 

  4. Zhang J., Lazar M.A. The mechanism of action of thyroid hormones. Annu. Rev. Physiol. 2000, 62: 439–466.

    Article  CAS  PubMed  Google Scholar 

  5. Falkenstein E., Tillmann H.C., Christ M., Feuring M., Wehling M. Multiple actions of steroid hormones — A focus on rapid, nongenomic effects. Pharmacol. Rev. 2000, 52: 513–556.

    CAS  PubMed  Google Scholar 

  6. Davis P.J., Davis F.B. Nongenomic actions of thyroid hormone. In: Braverman L.E. (Ed.), Contemporary endocrinology: Diseases of the thyroid. Humana Press, Totowa, 1997, p. 17.

    Google Scholar 

  7. Incerpi S., Luly P., De Vito P., Farias R.N. Short-term effects of thyroid hormones on the Na/H antiport in L-6 myoblasts: high molecular specificity for 3,3′,5-triiodo-L-thyronine. Endocrinology 1999, 140: 683–689.

    CAS  PubMed  Google Scholar 

  8. Sakaguchi Y., Cui G., Sen L. Acute effects of thyroid hormone on inward rectifier potassium channel currents in guinea pig ventricular myocytes. Endocrinology 1996, 137: 4744–4751.

    CAS  PubMed  Google Scholar 

  9. Huang C.J., Geller H.M., Green W.L., Craelius W. Acute effects of thyroid hormone analogs on sodium currents in neonatal rat myocytes. J. Mol. Cell. Cardiol. 1999, 31: 881–893.

    Article  CAS  PubMed  Google Scholar 

  10. Zhu X.-G., Hanover J., Hager G., Cheng S.-Y. Hormoneinduced translocation of thyroid hormone receptors in living cells visualized using a receptor green fluorescent protein chimera. J. Biol. Chem. 1998, 273: 27058–27063.

    Article  CAS  PubMed  Google Scholar 

  11. Chen Y., Chen P.L., Chen, C.F., Sharp, Z.D., Lee W.H. Thyroid hormone, T3-dependent phosphorylation and translocation of Trip230 from the Golgi complex to the nucleus. Proc. Natl. Acad. Sci. USA 1999, 96: 4443–4448.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  12. Safran M., Farwell A.P., Leonard J.L. Thyroid hormone-dependent redistribution of the 55-kilodalton monomer of protein disulfide isomerase in cultured glial cells. Endocrinology 1992, 131: 2413–2418.

    CAS  PubMed  Google Scholar 

  13. Lin H.-Y., Thacore H.R., Davis F.B., Davis P.J. Potentiation by thyroxine of interferon-gamma-induced antiviral state requires PKA and PKC activities. Am. J. Physiol. 1996, 271: C1256–1261.

    CAS  PubMed  Google Scholar 

  14. Lin H.-Y., Davis F.B., Gordinier J.K., Martino L.J., Davis P.J. Thyroid hormone induces activation of mitogen-activated protein kinase in cultured cells. Am. J. Physiol. 1999, 276: C1014–C1024.

    CAS  PubMed  Google Scholar 

  15. Siegrist-Kaiser C., Juge-Aubry C., Tranter M., Ekenbarger D., Leonard J. Thyroxine-dependent modulation of actin polymerization in cultured astrocytes. A novel, extranuclear action of thyroid hormone. J. Biol. Chem. 1990, 265: 5296–5302.

    CAS  PubMed  Google Scholar 

  16. Davis P.J., Shih A., Lin H.-Y., Martino L.J., Davis F.B. Thyroxine promotes association of mitogen-activated protein kinase and nuclear thyroid hormone receptor (TR) and causes serine phosphorylation of TR. J. Biol. Chem. 2000, 275: 38032–38039.

    Article  CAS  PubMed  Google Scholar 

  17. Ebata S., Muto S., Okada K., Nemoto J., Amemiya M., Saito T., et al. Aldosterone activates Na+/H+ exchange in vascular smooth muscle cells by nongenomic and genomic mechanisms. Kidney Int. 56: 1400–1412.

  18. Ashizawa K., McPhie P., Lin K.H., Cheng S.-Y. An in vitro novel mechanism of regulating the activity of pyruvate kinase M2 by thyroid hormone and fructose 1,6-bisphosphate. Biochemistry 1991, 30: 7105–7111.

    Article  CAS  PubMed  Google Scholar 

  19. Arnold S., Goglia F., Kadenbach B. 3,5-Diiodothyronine binds to subunit Va of cytochrome-c oxidase and abolishes the allosteric inhibition of respiration by ATP. Eur. J. Biochem. 1998, 252: 325–330.

    Article  CAS  PubMed  Google Scholar 

  20. Sun Z.-Q., Ojamaa K., Coetzee W., Artman M., Klein I. Effects of thyroid hormone on action potential and repolarizing currents in rat ventricular myocytes. Amer. J. Physiol. 2000, 278: E302–E307.

    CAS  Google Scholar 

  21. Giguere A., Fortier S., Beaudry C., Gallo-Payet N., Bellabarba D. Effect of thyroid hormones on G proteins in synaptosomes of chick embryo. Endocrinology 1996, 137: 2558–2564.

    CAS  PubMed  Google Scholar 

  22. Lawrence W.D., Schoenl M., Davis P.J. Stimulation in vitro of rabbit erythrocyte cytosol phospholipid-dependent protein kinase activity. A novel action of thyroid hormone. J. Biol. Chem. 1989, 264: 4766–4768.

    CAS  PubMed  Google Scholar 

  23. Sundquist J., Blas S.D., Hogan J.E., Davis F.B., Davis P.J. The alpha 1-adrenergic receptor in human erythrocyte membranes mediates interaction in vitro of epinephrine and thyroid hormone at the membrane Ca(2+)-ATPase. Cell Signalling 1992, 4: 795–799.

    Article  CAS  PubMed  Google Scholar 

  24. Davis F.B., Moffett M.J., Davis P.J., Al Ogaily M.S., Blas S.D. Inositol phosphates modulate binding of thyroid hormone to human red cell membranes in vitro. J. Clin. Endocrinol. Metab. 1993, 77: 1427–1430.

    CAS  PubMed  Google Scholar 

  25. Davis F.B., Davis P.J., Blas S.D., Gombas D.Z. Inositol phosphates modulate human red blood cell Ca(2+)-adenosine triphosphatase activity in vitro by a guanine nucleotide regulatory protein. Metabolism 1995, 44: 865–868.

    Article  CAS  PubMed  Google Scholar 

  26. Smallwood J.I., Gugi B., Rasmussen H. Regulation of erythrocyte Ca2+ pump activity by protein kinase C. J. Biol. Chem. 1988, 263: 2195–2202.

    CAS  PubMed  Google Scholar 

  27. Galo M.G., Unates L.E., Farias R.N. Effect of membrane fatty acid composition on the action of thyroid hormones on (Ca2+ + Mg2+)-adenosine triphosphatase from rat erythrocyte. J. Biol. Chem. 1981, 256: 7113–7114.

    CAS  PubMed  Google Scholar 

  28. Mylotte K.M., Cody V., Davis P.J., Davis F.B., Blas S.D., Schoenl M. Milrinone and thyroid hormone stimulate myocardial membrane Ca2+-ATPase activity and share structural homologies. Proc. Natl. Acad. Sci. USA 1985, 82: 7974–7978.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. Warnick P.R., Davis P.J., Davis F.B., Cody V., Galindo J. Jr., Blas S.D. Rabbit skeletal muscle sarcoplasmic reticulum Ca(2+)-ATPase activity: stimulation in vitro by thyroid hormone analogues and bipyridines. Biochem. Biophys. Acta 1993, 1153: 184–190.

    Article  CAS  PubMed  Google Scholar 

  30. Christ M., Meyer C., Sippel K., Wehling M. Rapid aldosterone signaling in vascular smooth muscle cells: involvement of phospholipase C, diacylglycerol and protein kinase C alpha. Biochem. Biophys. Res. Commun. 1995, 213: 123–129.

    Article  CAS  PubMed  Google Scholar 

  31. Lin H.Y., Thacore H.R., Davis F.B., Davis P.J. Thyroid hormone analogues potentiate the antiviral action of interferon- gamma by two mechanisms. J. Cell. Physiol. 1996, 167: 269–276.

    Article  CAS  PubMed  Google Scholar 

  32. Lin H.Y., Yen P.M., Davis F.B., Davis P.J. Protein synthesis-dependent potentiation by thyroxine of antiviral activity of interferon-gamma. Am. J. Physiol. 1997, 273: C1225–C1232.

    CAS  PubMed  Google Scholar 

  33. Lin H.Y., Shih A., Davis F.B., Davis P.J. Thyroid hormone down regulates TGF-a-induced immediate-early gene expression via a PKA-dependent pathway. Proceedings of the 83rd Annual Meeting of the Endocrine Society, June, 2001.

    Google Scholar 

  34. Lin H.Y., Shih A., Davis F.B., Davis P.J. Thyroid hormone promotes the phosphorylation of STAT3 and potentiates the action of epidermal growth factor in cultured cells. Biochem. J. 1999, 338: 427–432.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  35. Schindler C., Darnell J.E. Jr. Transcriptional responses to polypeptide ligands: the JAK-STAT pathway. Annu. Rev. Biochem. 1995, 64: 621–651.

    Article  CAS  PubMed  Google Scholar 

  36. Horvath C.M., Darnell J.E. Jr. The antiviral state induced by alpha interferon and gamma interferon requires transcriptionally active Stat1 protein. J. Virol. 1996, 70: 647–650.

    CAS  PubMed Central  PubMed  Google Scholar 

  37. Kato S., Endoh H., Masuhiro Y., Kitamoto T., Uchiyama S., Sasaki H., et al. Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase. Science 1995, 270: 1491–1494.

    Article  CAS  PubMed  Google Scholar 

  38. Shih A., Lin H.Y., Davis F.B., Davis P.J. Thyroid hormone promotes serine phosphorylation of p53 by mitogen-activated protein kinase. Biochemistry 2001, 40: 2870–2878.

    Article  CAS  PubMed  Google Scholar 

  39. Puymirat J., Etongue-Mayer P., Dussault J. Thyroid hormones stabilize acetylcholinesterase mRNA in neuro-2A cells that overexpress the beta1 thyroid receptor. J. Biol. Chem. 1995, 270: 30651–30656.

    Article  CAS  PubMed  Google Scholar 

  40. Koenig R.J. Thyroid hormone receptor coactivators and corepressors. Thyroid 1998, 8: 703–713.

    Article  CAS  PubMed  Google Scholar 

  41. Vassy R., Nicolas P., Yin Y.L., Perret G.Y. Nongenomic effect of triiodothyronine on cell surface beta-adrenoceptors in cultured embryonic cardiac myocytes. Proc. Soc. Exp. Biol. Med. 1997, 214: 352–358.

    Article  CAS  PubMed  Google Scholar 

  42. Farwell A.P., DiBenedetto D.J., Leonard J.L. Thyroxine targets different pathways of internalization of type II iodothyronine 5′-deiodinase in astrocytes. J. Biol. Chem. 1993, 268: 5055–5062.

    CAS  PubMed  Google Scholar 

  43. Farwell A.P., Tranter M.P., Leonard J.L. Thyroxine-dependent regulation of integrin-laminin interactions in astrocytes. Endocrinology 1995, 136: 3909–3915.

    CAS  PubMed  Google Scholar 

  44. Zhang X.A., Bontrager A.L., Stipp C.S., Kraeft S.K., Bazzoni G., Chen L.B., et al. Phosphorylation of a conserved integrin alpha 3 QPSXXE motif regulates signaling, motility, and cytoskeletal engagement. Mol. Biol. Cell 2001, 12: 351–365.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  45. Boehme S.A., Sullivan S.K., Crowe P.D., Santos M., Conlon P.J., Sriramarao P., et al. Activation of mitogen-activated protein kinase regulates eotaxin-induced eosinophil migration. J. Immunol. 1999, 163: 1611–1618.

    CAS  PubMed  Google Scholar 

  46. Segal J., Ingbar S. Evidence that an increase in cytoplasmic calcium is the initiating event in certain plasma membranemediated responses to 3,5,3′-triiodothyronine in rat thymocytes. Endocrinology 1989, 124: 1949–1955.

    Article  CAS  PubMed  Google Scholar 

  47. Improta-Brears T., Whorton A.R., Codazzi F., York J.D., Meyer T., McDonnell D.P. Estrogen-induced activation of mitogen-activated protein kinase requires mobilization of intracellular calcium. Proc. Natl. Acad. Sci. USA 1999, 96: 4686–4691.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  48. Doolan C.M., Harvey B.J. Modulation of cytosolic protein kinase C and calcium ion activity by steroid hormones in rat distal colon. J. Biol. Chem. 1996, 271: 8763–8767.

    Article  CAS  PubMed  Google Scholar 

  49. Qiu J., Lou L.G., Huang X.Y., Lou S.J., Pei G., Chen Y.Z. Nongenomic mechanisms of glucocorticoid inhibition of nicotine-induced calcium influx in PC12 cells: involvement of protein kinase C. Endocrinology 1998, 139: 5103–5108.

    CAS  PubMed  Google Scholar 

  50. Lieberherr M., Grosse B., Machelon V. Phospholipase C-beta and ovarian sex steroids in pig granulosa cells. J. Cell. Biochem. 1999, 74: 50–60.

    Article  CAS  PubMed  Google Scholar 

  51. Machelon V., Nome F., Grosse B., Lieberherr M. Progesterone triggers rapid transmembrane calcium influx and/or calcium mobilization from endoplasmic reticulum, via a pertussis-insensitive G-protein in granulosa cells in relation to luteinization process. J. Cell. Biochem. 1996, 61: 619–628.

    Article  CAS  PubMed  Google Scholar 

  52. Machelon V., Nome F., Tesarik J. Nongenomic effects of androstenedione on human granulosa luteinizing cells. J. Clin. Endocrinol. Metab. 1998, 83: 263–269.

    Article  CAS  PubMed  Google Scholar 

  53. Harrison D.A., Carr D.W., Meizel S. Involvement of protein kinase A and A kinase anchoring protein in the progesterone- initiated human sperm acrosome reaction. Biol. Reprod. 2000, 62: 811–820.

    Article  CAS  PubMed  Google Scholar 

  54. Richards J.S. New signaling pathways for hormones and cyclic adenosine 3′,5′-monophosphate action in endocrine cells. Mol. Endocrinol. 2001, 15: 209–218.

    CAS  PubMed  Google Scholar 

  55. Christ M., Gunther A., Heck M., Schmidt B.M., Falkenstein E., Wehling M. Aldosterone, not estradiol, is the physiological agonist for rapid increases in cAMP in vascular smooth muscle cells. Circulation 1999, 99: 1485–1491.

    Article  CAS  PubMed  Google Scholar 

  56. Gekle M., Silbernagl S., Oberleithner H. The mineralocorticoid aldosterone activates a proton conductance in cultured kidney cells. Am. J. Physiol. 1997, 273: C1673–C1678.

    CAS  PubMed  Google Scholar 

  57. Sato A., Liu J.P., Funder J.W. Aldosterone rapidly represses protein kinase C activity in neonatal rat cardiomyocytes in vitro. Endocrinology 1997, 138: 3410–3416.

    Article  CAS  PubMed  Google Scholar 

  58. Muto S., Ebata S., Okada K., Saito T., Asano Y. Glucocorticoid modulates Na+/H+ exchange activity in vascular smooth muscle cells by nongenomic and genomic mechanisms. Kidney Int. 2000, 57: 2319–2333.

    Article  CAS  PubMed  Google Scholar 

  59. Lee H.W., Eghbali-Webb M. Estrogen enhances proliferative capacity of cardiac fibroblasts by estrogen receptor- and mitogen-activated protein kinase-dependent pathways. J. Mol. Cell. Cardiol. 1998, 30: 1359–1368.

    Article  CAS  PubMed  Google Scholar 

  60. Bayaa M., Booth R.A., Sheng Y., Liu X.J. The classical progesterone receptor mediates xenopus oocyte maturation through a nongenomic mechanism. Proc. Natl. Acad. Sci. USA 2000, 97: 12607–12612.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  61. Gerdes D., Wehling M., Leube B., Falkenstein E. Cloning and tissue expression of two putative steroid membrane receptors. Biol. Chem. 1998, 379: 907–911.

    CAS  PubMed  Google Scholar 

  62. Falkenstein E., Schmieding K., Lange A., Meyer C., Gerdes D., Welsch U., et al. Localization of a putative progesterone membrane binding protein in porcine hepatocytes. Cell. Mol. Biol. 1998, 44: 571–578.

    CAS  PubMed  Google Scholar 

  63. Nadal A., Ropero A.B., Laribi O., Maillet M., Fuentes E., Soria B. Nongenomic actions of estrogens and xeno-estrogens by binding at a plasma membrane receptor unrelated to estrogen receptor alpha and estrogen receptor beta. Proc. Natl. Acad. Sci. USA 2000, 97: 11603–11608.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  64. Razandi M., Pedram A., Greene G.L., Levin E.R. Cell membrane and nuclear estrogen receptors (ERs) originate from a single transcript: studies of ERalpha and ERbeta expressed in Chinese hamster ovary cells. Mol. Endocrinol. 1999, 13: 307–319.

    CAS  PubMed  Google Scholar 

  65. Goetz R.M., Thatte H.S., Prabhakar P., Cho M.R., Michel T., Golan D.E. Estradiol induces the calcium-dependent translocation of endothelial nitric oxide synthase. Proc. Natl. Acad. Sci. USA 1999, 96: 2788–2793.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  66. Koukouritaki S.B., Margioris A.N., Gravanis A., Hartig R., Stournaras C. Dexamethasone induces rapid actin assembly in human endometrial cells without affecting its synthesis. J. Cell. Biochem. 1997, 65: 492–500.

    Article  CAS  PubMed  Google Scholar 

  67. Koukouritaki S.B., Theodoropoulos P.A., Margioris A.N., Gravanis A., Stournaras C. Dexamethasone alters rapidly actin polymerization dynamics in human endometrial cells: evidence for nongenomic actions involving cAMP turnover. J. Cell. Biochem. 1996, 62: 251–261.

    Article  CAS  PubMed  Google Scholar 

  68. Luconi M., Muratori M., Forti G., Baldi E. Identification and characterization of a novel functional estrogen receptor on human sperm membrane that interferes with progesterone effects. J. Clin. Endocrinol. Metab. 1999, 84: 1670–1678.

    Article  CAS  PubMed  Google Scholar 

  69. Falkenstein E., Norman A.W., Wehling M. Mannheim classification of nongenomically initiated (rapid) steroid action( s). J. Clin. Endocrinol. Metab. 2000, 85: 2072–2075.

    Article  CAS  PubMed  Google Scholar 

  70. Bronson R.A., Peresleni T., Golightly M. Progesterone promotes the acrosome reaction in capacitated human spermatozoa as judged by flow cytometry and CD46 staining. Mol. Hum. Reprod. 1999, 5: 507–512.

    Article  CAS  PubMed  Google Scholar 

  71. Meizel S., Turner K.O. Progesterone acts at the plasma membrane of human sperm. Mol. Cell. Endocrinol. 1991, 77: R1–R5.

    Article  CAS  PubMed  Google Scholar 

  72. Osman R.A., Andria M.L., Jones A.D., Meizel S. Steroid induced exocytosis: the human sperm acrosome reaction. Biochem Biophys. Res. Commun. 1989, 160: 828–833.

    Article  CAS  PubMed  Google Scholar 

  73. Baldi E., Casano R., Falsetti C., Krausz C., Maggi M., Forti G. Intracellular calcium accumulation and responsiveness to progesterone in capacitating human spermatozoa. J. Androl. 1991, 12: 323–330.

    CAS  PubMed  Google Scholar 

  74. Turner K.O., Garcia M.A., Meizel S. Progesterone initiation of the human sperm acrosome reaction: the obligatory increase in intracellular calcium is independent of the chloride requirement. Mol. Cell. Endocrinol. 1994, 101: 221–225.

    Article  CAS  PubMed  Google Scholar 

  75. Blackmore P.F., Beebe S.J., Danforth D.R., Alexander N. Progesterone and 17alpha-hydroxyprogesterone. Novel stimulators of calcium influx in human sperm. J. Biol. Chem. 1990, 265: 1376–1380.

    CAS  PubMed  Google Scholar 

  76. Baldi E., Luconi M., Bonaccorsi L., Maggi M., Francavilla S., Gabriele A., et al. Nongenomic progesterone receptor on human spermatozoa: biochemical aspects and clinical implications. Steroids 1999, 64: 143–148.

    Article  CAS  PubMed  Google Scholar 

  77. Blackmore P.F., Neulen J., Lattanzio F., Beebe S.J. Cell surface-binding sites for progesterone mediate calcium uptake in human sperm. J. Biol. Chem. 1991, 266: 18655–18659.

    CAS  PubMed  Google Scholar 

  78. Meyer C., Schmid R., Scriba P.C., Wehling M. Purification and partial sequencing of high affinity progesterone-binding site(s) from porcine liver membranes. Eur. J. Biochem. 1996, 239: 726–731.

    Article  CAS  PubMed  Google Scholar 

  79. Falkenstein E., Meyer C., Eisen C., Scriba P.C., Wehling M. Full-length cDNA sequence of a progesterone membranebinding protein from porcine vascular smooth muscle cells. Biochem. Biophys. Res. Commun. 1996, 229: 86–89.

    Article  CAS  PubMed  Google Scholar 

  80. Blackmore P.F. Extragenomic actions of progesterone in human sperm and progesterone metabolites in human platelets. Steroids 1999, 64: 149–156.

    Article  CAS  PubMed  Google Scholar 

  81. Selmin O., Lucier G.W., Clark G.C., Tritscher A.M., Vanden Heuvel J.P., et al. Isolation and characterization of a novel gene induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin in rat liver. Carcinogenesis 1996, 17: 2609–2615.

    Article  CAS  PubMed  Google Scholar 

  82. Christ M., Eisen C., Aktas J., Theisen K., Wehling M. The inositol-1,4,5-trisphosphate system is involved in rapid effects of aldosterone in human mononuclear leukocytes. J. Clin. Endocrinol. Metab. 1993, 77: 1452–1457.

    CAS  PubMed  Google Scholar 

  83. Berridge M.J. Inositol trisphosphate and calcium signalling. Nature 1993, 361: 315–325.

    Article  CAS  PubMed  Google Scholar 

  84. Schneider M., Ulsenheimer A., Christ M., Wehling M. Nongenomic effects of aldosterone on intracellular calcium in porcine endothelial cells. Am. J. Physiol. 1997, 272: E616–E620.

    CAS  PubMed  Google Scholar 

  85. Wehling M., Ulsenheimer A., Schneider M., Neylon C., Christ M. Rapid effects of aldosterone on free intracellular calcium in vascular smooth muscle and endothelial cells: subcellular localization of calcium elevations by single cell imaging. Biochem. Biophys. Res. Commun. 1994, 204: 475–481.

    Article  CAS  PubMed  Google Scholar 

  86. Wehling M., Neylon C.B., Fullerton M., Bobik A., Funder J.W. Nongenomic effects of aldosterone on intracellular Ca2+ in vascular smooth muscle cells. Circ. Res. 1995, 76: 973–979.

    Article  CAS  PubMed  Google Scholar 

  87. Doolan C.M., Harvey B.J. Rapid effects of steroid hormones on free intracellular calcium in T84 colonic epithelial cells. Am. J. Physiol. 1996, 271: C1935–C1941.

    CAS  PubMed  Google Scholar 

  88. Haseroth K., Gerdes D., Berger S., Feuring M., Gunther A., Herbst C., et al. Rapid nongenomic effects of aldosterone in mineralocorticoid-receptor-knockout mice. Biochem. Biophys. Res. Commun. 1999, 266: 257–261.

    Article  CAS  PubMed  Google Scholar 

  89. Karim Z.G., Chambrey R., Chalumeau C., Defontaine N., Warnock D.G., Paillard M., et al. Regulation by PKC isoforms of Na(+)/H(+) exchanger in luminal membrane vesicles isolated from cortical tubules. Am. J. Physiol. 1999, 277: F773–F778.

    CAS  PubMed  Google Scholar 

  90. Moor A.N., Fliegel L. Protein kinase-mediated regulation of the Na+/H+ exchanger in the rat myocardium by mitogenactivated protein kinase-dependent pathways. J. Biol. Chem. 1999, 274: 22985–22992.

    Article  CAS  PubMed  Google Scholar 

  91. Sartori M., Ceolotto G., Semplicini A. MAPKinase and regulation of the sodium-proton exchanger in human red blood cell. Biochem. Biophys. Acta 1999, 1421: 140–148.

    Article  CAS  PubMed  Google Scholar 

  92. Gether U. Uncovering molecular mechanisms involved in activation of G protein-coupled receptors. Endocr. Rev. 2000, 21: 90–113.

    Article  CAS  PubMed  Google Scholar 

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  1. New York State Department of Health, Albany Medical College and the Wadsworth Center, MC-16, Albany, NY, 12208, USA

    P. J. Davis & F. B. Davis

  2. Departments of Endocrinology, University of Adelaide, Royal Adelaide Hospital, Adelaide, Australia

    H. C. Tillmann & M. Wehling

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Davis, P.J., Tillmann, H.C., Davis, F.B. et al. Comparison of the mechanisms of nongenomic actions of thyroid hormone and steroid hormones. J Endocrinol Invest 25, 377–388 (2002). https://doi.org/10.1007/BF03344022

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