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The Multifaceted Mineralocorticoid Receptor

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Abstract

The primary adrenal cortical steroid hormones, aldosterone, and the glucocorticoids cortisol and corticosterone, act through the structurally similar mineralocorticoid (MR) and glucocorticoid receptors (GRs). Aldosterone is crucial for fluid, electrolyte, and hemodynamic homeostasis and tissue repair; the significantly more abundant glucocorticoids are indispensable for energy homeostasis, appropriate responses to stress, and limiting inflammation. Steroid receptors initiate gene transcription for proteins that effect their actions as well as rapid non‐genomic effects through classical cell signaling pathways. GR and MR are expressed in many tissues types, often in the same cells, where they interact at molecular and functional levels, at times in synergy, others in opposition. Thus the appropriate balance of MR and GR activation is crucial for homeostasis. MR has the same binding affinity for aldosterone, cortisol, and corticosterone. Glucocorticoids activate MR in most tissues at basal levels and GR at stress levels. Inactivation of cortisol and corticosterone by 11β‐HSD2 allows aldosterone to activate MR within aldosterone target cells and limits activation of the GR. Under most conditions, 11β‐HSD1 acts as a reductase and activates cortisol/corticosterone, amplifying circulating levels. 11β‐HSD1 and MR antagonists mitigate inappropriate activation of MR under conditions of oxidative stress that contributes to the pathophysiology of the cardiometabolic syndrome; however, MR antagonists decrease normal MR/GR functional interactions, a particular concern for neurons mediating cognition, memory, and affect. © 2014 American Physiological Society. Compr Physiol 4:965‐994, 2014.

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Figure 1. Figure 1. Aldosterone action. Aldosterone, cortisol, and corticosterone act through the mineralocorticoid receptor for which they have similar binding affinity to initiate transcriptional effects that take more than 3 h or rapid nongenomic effects that occur in seconds to minutes. The glucocorticoid receptor has similar slow transcriptional and rapid nongenomic effects in response to glucocorticoids, but not endogenous levels of aldosterone. Aldosterone, but not cortisol or corticosterone, activates GPR30(GPER) at physiological concentrations. Estrogen has not been demonstrated to activate GPER at physiological concentrations.
Figure 2. Figure 2. Microsomal 11β‐Hydroxysteroid dehydrogenases 1 and 2 provide prereceptor ligand specificity for MR and GR. 11β‐HSD1, a reductase in most tissues, requires NADPH to convert cortisone and 11‐dehydrocorticosterone to cortisol and corticosterone with a Km ∼1 to 3 μmol/L. In the presence of NADP+ or absence of hexose‐6‐phosphate dehydrogenase to regenerate NADPH, 11β‐HSD1 is a dehydrogenase. 11β‐HSD2 is a unidirectional NAD+‐dependent dehydrogenase which converts cortisol and corticosterone to the inactive cortisone and 11‐dehydrocorticosterone, Km ∼15 nmol/L. Aldosterone is not a substrate for the enzymes. Net dehydrogenase activity within the cell decreases glucocorticoid binding to the MR and GR and provides extrinsic specificity for aldosterone binding to the MR. Reductase activity increases glucocorticoid binding to both receptors.
Figure 3. Figure 3. MR and GR act as ligand activated transcription factors that reside primarily in the cytoplasm bound to chaperone and scaffolding proteins when not bound to an agonist. Upon ligand binding they are transported to the nucleus where they form homodimers and heterodimers that bind hormone response elements on the chromosomes and associate with coactivator and corepressor proteins to modulate the transcription of effector proteins. Some chaperone and co‐activator proteins bind both receptors. MR and GR associated with the plasma membrane within caveoli initiate rapid nonnuclear effects through classic cell signaling mechanisms. 11β‐HSD enzymes within the endoplasmic reticulum (not depicted) modulate glucocorticoid concentrations for both the GR and MR. Interactions between receptors occur at multiple levels.


Figure 1. Aldosterone action. Aldosterone, cortisol, and corticosterone act through the mineralocorticoid receptor for which they have similar binding affinity to initiate transcriptional effects that take more than 3 h or rapid nongenomic effects that occur in seconds to minutes. The glucocorticoid receptor has similar slow transcriptional and rapid nongenomic effects in response to glucocorticoids, but not endogenous levels of aldosterone. Aldosterone, but not cortisol or corticosterone, activates GPR30(GPER) at physiological concentrations. Estrogen has not been demonstrated to activate GPER at physiological concentrations.


Figure 2. Microsomal 11β‐Hydroxysteroid dehydrogenases 1 and 2 provide prereceptor ligand specificity for MR and GR. 11β‐HSD1, a reductase in most tissues, requires NADPH to convert cortisone and 11‐dehydrocorticosterone to cortisol and corticosterone with a Km ∼1 to 3 μmol/L. In the presence of NADP+ or absence of hexose‐6‐phosphate dehydrogenase to regenerate NADPH, 11β‐HSD1 is a dehydrogenase. 11β‐HSD2 is a unidirectional NAD+‐dependent dehydrogenase which converts cortisol and corticosterone to the inactive cortisone and 11‐dehydrocorticosterone, Km ∼15 nmol/L. Aldosterone is not a substrate for the enzymes. Net dehydrogenase activity within the cell decreases glucocorticoid binding to the MR and GR and provides extrinsic specificity for aldosterone binding to the MR. Reductase activity increases glucocorticoid binding to both receptors.


Figure 3. MR and GR act as ligand activated transcription factors that reside primarily in the cytoplasm bound to chaperone and scaffolding proteins when not bound to an agonist. Upon ligand binding they are transported to the nucleus where they form homodimers and heterodimers that bind hormone response elements on the chromosomes and associate with coactivator and corepressor proteins to modulate the transcription of effector proteins. Some chaperone and co‐activator proteins bind both receptors. MR and GR associated with the plasma membrane within caveoli initiate rapid nonnuclear effects through classic cell signaling mechanisms. 11β‐HSD enzymes within the endoplasmic reticulum (not depicted) modulate glucocorticoid concentrations for both the GR and MR. Interactions between receptors occur at multiple levels.
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Elise Gomez‐Sanchez, Celso E. Gomez‐Sanchez. The Multifaceted Mineralocorticoid Receptor. Compr Physiol 2014, 4: 965-994. doi: 10.1002/cphy.c130044