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Vol. 52, Issue 4, 513-556, December 2000

Multiple Actions of Steroid Hormones---A Focus on Rapid, Nongenomic Effects

Elisabeth Falkenstein, Hanns-Christian Tillmann, Michael Christ, Martin Feuring and Martin Wehling1

Institute of Clinical Pharmacology, Faculty for Clinical Medicine at Mannheim, University of Heidelberg, Mannheim, Germany

I. Introduction and Historical Development
II. How Do Steroids Act?
    A. Genomic Steroid Action
    B. Nongenomic Steroid Action
III. Steroid Receptors Mediating Genomic and Nongenomic Steroid Action
    A. Receptors Responsible for Genomic Steroid Action
        1. Structural Features of Steroid Hormone Receptors.
        2. Genomic Steroid Hormone Action.
        3. Steroid Hormone-Responsive Elements.
        4. Steroid-Induced Initiation of Transcription.
        5. Alternative, Including Nontranscriptional Actions of Ligand-Steroid Hormone Receptor Complexes.
    B. Receptors Responsible for Nongenomic Steroid Action
        1. Classic Intracellular Receptors (Classification AIIa).
        2. Nonclassic Steroid Receptors---No Coagonist Required (Classification AIIb).
        3. Nonclassic Steroid Receptors---Coagonist-Mediated Steroid Action (Classification BIIb).
        4. No Receptor Involved---Direct Nongenomic Action (Classification AI).
IV. Steroid Groups
    A. Gonadal Steroids
        1. Progesterone.
            a. Rapid Effects of Progesterone.
            b. Progesterone Receptors for Rapid Signaling.
        2. Estrogens.
            a. Rapid Effects of Estrogens.
            b. Estrogen Receptors for Rapid Signaling.
        3. Androgens.
            a. Rapid Effects of Androgens.
            b. Androgen Receptors for Rapid Signaling.
    B. Glucocorticoids
        1. Rapid Effects of Glucocorticoids.
        2. Glucocorticoid Receptors for Rapid Signaling.
    C. Mineralocorticoids
        1. Rapid Effects of Mineralocorticoids.
        2. Mineralocorticoid Receptors for Rapid Signaling.
    D. Neuroactive Steroids
        1. Rapid Effects of Neuroactive Steroids.
        2. Neurosteroid Receptors for Rapid Signaling.
            a. gamma -Aminobutyric AcidA Receptor.
            b. N-Methyl-D-aspartate Receptor.
            c. Sigma1 Receptor.
            d. 5-Hydroxytryptamine Type 3 Receptor.
            e. Glycine Receptor.
    E. Vitamin D3
        1. Rapid Effects of Vitamin D3.
        2. Vitamin D3 Receptors for Rapid Signaling.
    F. Triiodothyronine
        1. Rapid Effects of Triiodothyronine.
        2. Triiodothyronine Receptors for Rapid Signaling.
V. Two-Step Model for Steroid Action
VI. Clinical Perspectives
    A. Cardiovascular Pharmacology
    B. Reproductive Pharmacology
    C. Endocrinological Pharmacology
    D. Neuro-/Psychopharmacology
VII. Conclusions and Outlook
Acknowledgments
References

According to the traditional model, steroid hormones bind to intracellular receptors and subsequently modulate transcription and protein synthesis, thus triggering genomic events finally responsible for delayed effects. Based upon similarities in molecular structure, specific receptors for steroids, vitamin D3 derivatives, thyroid hormone, retinoids, and a variety of orphan receptors are considered to represent a superfamily of steroid receptors. In addition, very rapid effects of steroids mainly affecting intracellular signaling have been widely recognized that are clearly incompatible with the genomic model. These rapid, nongenomic steroid actions are likely to be transmitted via specific membrane receptors. Evidence for nongenomic steroid effects and distinct receptors involved is presented for all steroid groups including related compounds like vitamin D3 and thyroid hormones. The physiological and clinical relevance of these rapid effects is still largely unclear, but their existence in vivo has been clearly shown in various settings including human studies. Drugs that specifically affect nongenomic steroid action may find applications in various clinical areas such as cardiovascular and central nervous disorders, electrolyte homeostasis, and infertility. In addition to a short description of genomic steroid action, this review pays particular attention to the current knowledge and important results on the mechanisms of nongenomic steroid action. The modes of action are discussed in relation to their potential physiological or pathophysiological relevance and with regard to a cross-talk between genomic and nongenomic responses.

1 Address for correspondence: Dr. Martin Wehling, Institute of Clinical Pharmacology, University Hospital Mannheim, Theodor-Kutzer-Ufer 1-3, 68135 Mannheim, Germany. E-mail: martin.wehling{at}kpha.ma.uni-heidelberg.de

0031-6997/00/5204-0513$03.00/0
PHARMACOLOGICAL REVIEWS
Copyright © 2000 by The American Society for Pharmacology and Experimental Therapeutics


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D. Susic, J. Varagic, J. Ahn, L. C. Matavelli, and E. D. Frohlich
Beneficial Cardiovascular Actions of Eplerenone in the Spontaneously Hypertensive Rat
Journal of Cardiovascular Pharmacology and Therapeutics, July 1, 2005; 10(3): 197 - 203.
[Abstract] [PDF]

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 JCBHome page
T. Kino, A. Tiulpakov, T. Ichijo, L. Chheng, T. Kozasa, and G. P. Chrousos
G protein {beta} interacts with the glucocorticoid receptor and suppresses its transcriptional activity in the nucleus
J. Cell Biol., June 20, 2005; 169(6): 885 - 896.
[Abstract] [Full Text] [PDF]

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 J Mol EndocrinolHome page
Y. Kazeto, R. Goto-Kazeto, P. Thomas, and J. M Trant
Molecular characterization of three forms of putative membrane-bound progestin receptors and their tissue-distribution in channel catfish, Ictalurus punctatus
J. Mol. Endocrinol., June 1, 2005; 34(3): 781 - 791.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
A. M. Vertino, C. M. Bula, J.-R. Chen, M. Almeida, L. Han, T. Bellido, S. Kousteni, A. W. Norman, and S. C. Manolagas
Nongenotropic, Anti-Apoptotic Signaling of 1{alpha},25(OH)2-Vitamin D3 and Analogs through the Ligand Binding Domain of the Vitamin D Receptor in Osteoblasts and Osteocytes: MEDIATION BY Src, PHOSPHATIDYLINOSITOL 3-, AND JNK KINASES
J. Biol. Chem., April 8, 2005; 280(14): 14130 - 14137.
[Abstract] [Full Text] [PDF]

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 CirculationHome page
M. M. Bachschmid and B. van der Loo
A New "Sunshine" in the Vasculature?
Circulation, April 5, 2005; 111(13): 1571 - 1573.
[Full Text] [PDF]

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 Am. J. Physiol. Gastrointest. Liver Physiol.Home page
T. Radanovic, C. A. Wagner, H. Murer, and J. Biber
Regulation of Intestinal Phosphate Transport I. Segmental expression and adaptation to low-Pi diet of the type IIb Na+-Pi cotransporter in mouse small intestine
Am J Physiol Gastrointest Liver Physiol, March 1, 2005; 288(3): G496 - G500.
[Abstract] [Full Text] [PDF]

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 J Mol EndocrinolHome page
J. S Lewis, T J Thomas, R. G Pestell, C. Albanese, M. A Gallo, and T. Thomas
Differential effects of 16{alpha}-hydroxyestrone and 2-methoxyestradiol on cyclin D1 involving the transcription factor ATF-2 in MCF-7 breast cancer cells
J. Mol. Endocrinol., February 1, 2005; 34(1): 91 - 105.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
M. Candolfi, G. Jaita, V. Zaldivar, S. Zarate, L. Ferrari, D. Pisera, M. G. Castro, and A. Seilicovich
Progesterone Antagonizes the Permissive Action of Estradiol on Tumor Necrosis Factor-{alpha}-Induced Apoptosis of Anterior Pituitary Cells
Endocrinology, February 1, 2005; 146(2): 736 - 743.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
P. Thomas, Y. Pang, E. J. Filardo, and J. Dong
Identity of an Estrogen Membrane Receptor Coupled to a G Protein in Human Breast Cancer Cells
Endocrinology, February 1, 2005; 146(2): 624 - 632.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
P. Capuano, T. Radanovic, C. A. Wagner, D. Bacic, S. Kato, Y. Uchiyama, R. St.-Arnoud, H. Murer, and J. Biber
Intestinal and renal adaptation to a low-Pi diet of type II NaPi cotransporters in vitamin D receptor- and 1{alpha}OHase-deficient mice
Am J Physiol Cell Physiol, February 1, 2005; 288(2): C429 - C434.
[Abstract] [Full Text] [PDF]

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 Arterioscler. Thromb. Vasc. Bio.Home page
P.E. Norman and J.T. Powell
Vitamin D, Shedding Light on the Development of Disease in Peripheral Arteries
Arterioscler Thromb Vasc Biol, January 1, 2005; 25(1): 39 - 46.
[Abstract] [Full Text] [PDF]

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 BloodHome page
L. Moro, S. Reineri, D. Piranda, D. Pietrapiana, P. Lova, A. Bertoni, A. Graziani, P. Defilippi, I. Canobbio, M. Torti, et al.
Nongenomic effects of 17{beta}-estradiol in human platelets: potentiation of thrombin-induced aggregation through estrogen receptor {beta} and Src kinase
Blood, January 1, 2005; 105(1): 115 - 121.
[Abstract] [Full Text] [PDF]

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 Proc Am Thorac SocHome page
C. Stellato
Post-transcriptional and Nongenomic Effects of Glucocorticoids
Proceedings of the ATS, November 1, 2004; 1(3): 255 - 263.
[Abstract] [Full Text] [PDF]

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 Exp. Biol. Med.Home page
T. R. Chakraborty and A. C. Gore
Aging-Related Changes in Ovarian Hormones, Their Receptors, and Neuroendocrine Function
Experimental Biology and Medicine, November 1, 2004; 229(10): 977 - 987.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
L. Moro, E. Marra, F. Capuano, and M. Greco
Thyroid Hormone Treatment of Hypothyroid Rats Restores the Regenerative Capacity and the Mitochondrial Membrane Permeability Properties of the Liver after Partial Hepatectomy
Endocrinology, November 1, 2004; 145(11): 5121 - 5128.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
E. Unni, S. Sun, B. Nan, M. J. McPhaul, B. Cheskis, M. A. Mancini, and M. Marcelli
Changes in Androgen Receptor Nongenotropic Signaling Correlate with Transition of LNCaP Cells to Androgen Independence
Cancer Res., October 1, 2004; 64(19): 7156 - 7168.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
O. Guzeloglu Kayisli, U. A. Kayisli, G. Luleci, and A. Arici
In Vivo and In Vitro Regulation of Akt Activation in Human Endometrial Cells Is Estrogen Dependent
Biol Reprod, September 1, 2004; 71(3): 714 - 721.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
C. Fix, C. Jordan, P. Cano, and W. H. Walker
Testosterone activates mitogen-activated protein kinase and the cAMP response element binding protein transcription factor in Sertoli cells
PNAS, July 27, 2004; 101(30): 10919 - 10924.
[Abstract] [Full Text] [PDF]

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 CirculationHome page
A. Mano, T. Tatsumi, J. Shiraishi, N. Keira, T. Nomura, M. Takeda, S. Nishikawa, S. Yamanaka, S. Matoba, M. Kobara, et al.
Aldosterone Directly Induces Myocyte Apoptosis Through Calcineurin-Dependent Pathways
Circulation, July 20, 2004; 110(3): 317 - 323.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
A. Arif, P. Vasanthi, I. A. Hansen, K. Scheller, and A. Dutta-Gupta
The Insect Hemolymph Protein HP19 Mediates the Nongenomic Effect of Ecdysteroids on Acid Phosphatase Activity
J. Biol. Chem., July 2, 2004; 279(27): 28000 - 28008.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
I. Bossis, S. Nishimura, M. Muchow, and T. E. Porter
Pituitary Expression of Type I and Type II Glucocorticoid Receptors during Chicken Embryonic Development and Their Involvement in Growth Hormone Cell Differentiation
Endocrinology, July 1, 2004; 145(7): 3523 - 3531.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
A. M. Braun and P. Thomas
Biochemical Characterization of a Membrane Androgen Receptor in the Ovary of the Atlantic Croaker (Micropogonias undulatus)
Biol Reprod, July 1, 2004; 71(1): 146 - 155.
[Abstract] [Full Text] [PDF]

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 CirculationHome page
A. Skyschally, M. Haude, H. Dorge, M. Thielmann, A. Duschin, A. van de Sand, I. Konietzka, A. Buchert, S. Aker, P. Massoudy, et al.
Glucocorticoid Treatment Prevents Progressive Myocardial Dysfunction Resulting From Experimental Coronary Microembolization
Circulation, May 18, 2004; 109(19): 2337 - 2342.
[Abstract] [Full Text] [PDF]

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 J. Exp. Biol.Home page
R. S. Farrar and K. J. Rodnick
Sex-dependent effects of gonadal steroids and cortisol on cardiac contractility in rainbow trout
J. Exp. Biol., May 15, 2004; 207(12): 2083 - 2093.
[Abstract] [Full Text] [PDF]

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 J. Am. Soc. Nephrol.Home page
C. Le Moellic, A. Ouvrard-Pascaud, C. Capurro, F. Cluzeaud, M. Fay, F. Jaisser, N. Farman, and M. Blot-Chabaud
Early Nongenomic Events in Aldosterone Action in Renal Collecting Duct Cells: PKC{alpha} Activation, Mineralocorticoid Receptor Phosphorylation, and Cross-Talk with the Genomic Response
J. Am. Soc. Nephrol., May 1, 2004; 15(5): 1145 - 1160.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
A. R. Beker-van Woudenberg, H. T.A. van Tol, B. A.J. Roelen, B. Colenbrander, and M. M. Bevers
Estradiol and Its Membrane-Impermeable Conjugate (Estradiol-Bovine Serum Albumin) During In Vitro Maturation of Bovine Oocytes: Effects on Nuclear and Cytoplasmic Maturation, Cytoskeleton, and Embryo Quality
Biol Reprod, May 1, 2004; 70(5): 1465 - 1474.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. Baron, M. Manin, C. Beaudoin, L. Leotoing, Y. Communal, G. Veyssiere, and L. Morel
Androgen Receptor Mediates Non-genomic Activation of Phosphatidylinositol 3-OH Kinase in Androgen-sensitive Epithelial Cells
J. Biol. Chem., April 9, 2004; 279(15): 14579 - 14586.
[Abstract] [Full Text] [PDF]

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 Endocr. Rev.Home page
C. A. Heinlein and C. Chang
Androgen Receptor in Prostate Cancer
Endocr. Rev., April 1, 2004; 25(2): 276 - 308.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
D. Auboeuf, D. H. Dowhan, Y. K. Kang, K. Larkin, J. W. Lee, S. M. Berget, and B. W. O'Malley
Differential recruitment of nuclear receptor coactivators may determine alternative RNA splice site choice in target genes
PNAS, February 24, 2004; 101(8): 2270 - 2274.
[Abstract] [Full Text] [PDF]

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 Circ. Res.Home page
A. Huang, D. Sun, Z. Wu, C. Yan, M. A. Carroll, H. Jiang, J. R. Falck, and G. Kaley
Estrogen Elicits Cytochrome P450--Mediated Flow-Induced Dilation of Arterioles in NO Deficiency: Role of PI3K-Akt Phosphorylation in Genomic Regulation
Circ. Res., February 6, 2004; 94(2): 245 - 252.
[Abstract] [Full Text] [PDF]

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 FASEB J.Home page
B. BARTHOLOME, C. M. SPIES, T. GABER, S. SCHUCHMANN, T. BERKI, D. KUNKEL, M. BIENERT, A. RADBRUCH, G.-R. BURMESTER, R. LAUSTER, et al.
Membrane glucocorticoid receptors (mGCR) are expressed in normal human peripheral blood mononuclear cells and up-regulated after in vitro stimulation and in patients with rheumatoid arthritis
FASEB J, January 1, 2004; 18(1): 70 - 80.
[Abstract] [Full Text] [PDF]

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 J. Neurophysiol.Home page
P. V. Lovell, J. T. King, and D. P. McCobb
Acute Modulation of Adrenal Chromaffin Cell BK Channel Gating and Cell Excitability by Glucocorticoids
J Neurophysiol, January 1, 2004; 91(1): 561 - 570.
[Abstract] [Full Text]

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 J. Lipid Res.Home page
S. Lamon-Fava and D. Micherone
Regulation of apoA-I gene expression: mechanism of action of estrogen and genistein
J. Lipid Res., January 1, 2004; 45(1): 106 - 112.
[Abstract] [Full Text] [PDF]

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 Exp. Biol. Med.Home page
C. S. Watson and B. Gametchu
Proteins of Multiple Classes May Participate in Nongenomic Steroid Actions
Experimental Biology and Medicine, December 1, 2003; 228(11): 1272 - 1281.
[Abstract] [Full Text] [PDF]

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 J. Pharmacol. Exp. Ther.Home page
M. C. Farach-Carson and P. J. Davis
Steroid Hormone Interactions with Target Cells: Cross Talk between Membrane and Nuclear Pathways
J. Pharmacol. Exp. Ther., December 1, 2003; 307(3): 839 - 845.
[Abstract] [Full Text] [PDF]


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