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Dopamine and Renal Function and Blood Pressure Regulation

Ines Armando, Van Anthony M. Villar, Pedro A. Jose

10.1002/cphy.c100032

Source: Volume 1, Issue 3, July 2011

Published online: July 2011

Full Article on Wiley Online Library



Abstract

Dopamine is an important regulator of systemic blood pressure via multiple mechanisms. It affects fluid and electrolyte balance by its actions on renal hemodynamics and epithelial ion and water transport and by regulation of hormones and humoral agents. The kidney synthesizes dopamine from circulating or filtered l‐DOPA independently from innervation. The major determinants of the renal tubular synthesis/release of dopamine are probably sodium intake and intracellular sodium. Dopamine exerts its actions via two families of cell surface receptors, D1‐like receptors comprising D1R and D5R, and D2‐like receptors comprising D2R, D3R, and D4R, and by interactions with other G protein‐coupled receptors. D1‐like receptors are linked to vasodilation, while the effect of D2‐like receptors on the vasculature is variable and probably dependent upon the state of nerve activity. Dopamine secreted into the tubular lumen acts mainly via D1‐like receptors in an autocrine/paracrine manner to regulate ion transport in the proximal and distal nephron. These effects are mediated mainly by tubular mechanisms and augmented by hemodynamic mechanisms. The natriuretic effect of D1‐like receptors is caused by inhibition of ion transport in the apical and basolateral membranes. D2‐like receptors participate in the inhibition of ion transport during conditions of euvolemia and moderate volume expansion. Dopamine also controls ion transport and blood pressure by regulating the production of reactive oxygen species and the inflammatory response. Essential hypertension is associated with abnormalities in dopamine production, receptor number, and/or posttranslational modification. © 2011 American Physiological Society. Compr Physiol 1:1075‐1117, 2011.

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Figure 1. Figure 1.

Distribution of the dopamine receptor subtypes along the nephron. OS: outer stripe; IS: inner stripe (composite from several mammals, including humans).
Figure 2. Figure 2.

D1R and D3R colocalization in renal proximal tubule cells from WKY rats. The cells were washed, fixed, and immunostained for D1R and D3R receptors. Basal colocalization appears as discreet yellow areas in the merge image of FITC‐tagged D1R (pseudocolored green) and Alexa 568‐tagged D3R (pseudocolored red).
Figure 3. Figure 3.

Proposed schema of dopamine signaling in renal proximal tubule cells during salt‐replete states. The dopaminergic response to conditions of salt repletion presumably involves both D1R and D3R acting synergistically; other dopamine receptors may take part in the physiological response, as well. During these conditions, the dopaminergic system is activated and the intrarenally produced dopamine occupies both D1 and D3 receptors (dopamine affinity for the dopamine receptors: D3R≥D4R>D5R>D2R>D1R). The D1R, mediated by Gαs, activates adenylyl cyclase, leading to increased intracellular cAMP/PKA, which, in turn, inhibits sodium transport in the renal proximal tubule cells and promotes natriuresis. Concurrently, the occupation of D3R by dopamine leads to increased Gβγ, which targets the C1b domain of adenylyl cyclases (other than adenylyl cyclase V, the preferred target of D3R‐associated Gαi) to augment the synthesis of cAMP mediated by D1R (and thus, the inhibition of sodium transport, green arrow), and to Gαi3 to directly inhibit NHE3 activity (GαS can also directly inhibit NHE3). Adenylyl cyclase isoforms IV, V, and VIII are not expressed in the proximal tubules. D3R can also couple to Gαs to abet the adenylyl cyclase activity by itself (green arrow). During prolonged periods of salt repletion (blue arrow), the D3R upregulates the expression of D1R and ETB to ensure continued natriuresis, and downregulates AT1R expression, directly by itself and indirectly through D1R, to attenuate its anti‐natriuretic effects. Hence, the D1R and D3R work in concert to promote natriuresis during salt‐replete states. Dopamine may work in the same manner in other nephron segments, however, the processes involved in these segments are still not completely worked out.
Figure 4. Figure 4.

AT1R is ubiquitinated and the ubiquitination of AT1R is initiated at the plasma membrane. Ubiquitination of the enhanced green fluorescence (EGF)‐tagged human AT1R is initiated at the plasma membrane in HEK293 cells heterologously expressing the human AT1R and human D5R. In vehicle‐treated cells, AT1R (pseudocolored green) is mainly at the membrane but is also observed in the cytoplasm. Ubiquitin (pseudocolored blue) and the proteasome marker, p44S10 (pseudocolored red) are scattered throughout the cytoplasm. The D5R agonist fenoldopam promotes the colocalization of AT1R, p44S10, and ubiquitin at the plasma membrane. The changes in color indicate colocalization: yellow = colocalization of AT1R and p44S10; cyan = colocalization of AT1R and ubiquitin; magenta = colocalization of p44S10 and ubiquitin; white = colocalization of AT1R, ubiquitin, and p44S10. The merging of the line drawings, red, green, and/or blue also depicts the colocalization of the different proteins. Scale bars are shown in vehicle‐treated cells.
Figure 5. Figure 5.

D3R and ETB interaction in Wistar‐Kyoto (WKY) rat renal proximal tubule cells. Renal proximal tubule cells from WKY rats grown on cover slips were treated for 30 min with a D3R agonist (PD128907), D3R antagonist (GR103691), ETB antagonist (BQ788), vehicle (PBS), or a combination of the D3R agonist with either antagonist after a 1‐h serum starvation. The cell membrane was labeled with the cell‐impermeant EZ‐link sulfo‐NHS‐SS‐Biotin for 30 min on ice. The cells were then fixed and permeabilized, double‐immunostained for D3R and ETB, and counterstained with FITC‐conjugated avidin to label the cell membrane. Images were obtained for D3R (pseudocolored red), ETB (pseudocolored green), cell membrane (pseudocolored blue) and the nucleus (pseudocolored magenta), via laser confocal microscopy. Under basal condition, both receptors are found at the cell membrane, with negligible colocalization. D3R activation results in the internalization of both receptors and in increased colocalization (yellow punctate areas in inset image; white arrows). No changes in the distribution or extent of colocalization are observed with either D3R or ETB antagonist treatment alone, or as co‐treatment.
Figure 6. Figure 6.

Signal transduction of a dopamine receptor. Upon ligand binding to the dopamine receptor (DR), the cognate G protein dissociates into Gα and Gβγ subunits. The Gβγ recruits G protein‐coupled receptor kinase that then phosphorylates/modifies the receptor. This covalent modification of the receptor prevents it from interacting with G proteins and allows it to associate with other proteins, for example, β‐arrestins, clathrin, and dynamin, to facilitate its endocytosis. Depending on the receptor subtype, the Gα subunit either activates or inhibits adenylyl cyclase to increase or decrease cAMP levels to promote specific downstream signaling pathways.
Figure 7. Figure 7.

D1R and GRK4 interaction in human renal proximal tubule cells. The interaction between D1R and GRK4 was evaluated through confocal microscopy and bimolecular fluorescence complementation (BiFC) assay in human renal proximal tubule cells (hPTCs). Top: serum‐starved hPTCs grown on cover slips were treated with the D1‐like receptor agonist fenoldopam (1 μM, 5 min), fixed and permeabilized, double immunostained for D1R and GRK4, and observed via laser scanning confocal microscopy. At basal conditions, the receptor (red) is distributed mostly at the cytoplasm and partially at the plasma membrane, while GRK4 (green) is localized in both the cytoplasm and cell membrane. Fenoldopam treatment promotes the redistribution of both proteins to the perinuclear area, where colocalization (yellow) is observed the most. Bottom: to confirm these observations, BiFC assay was performed in hPTCs. This technique is based on the in situ formation of a fluorescent complex when two nonfluorescent fragments of a fluorophore are brought together by the interaction between the proteins tagged with the fragments and thus allows the visualization of protein‐protein interaction in cells with neither the need to disrupt subcellular compartmentalization nor the use of exogenous fluorophore‐labeled antibodies. hPTCs heterologously expressing D1R tagged with the n‐terminus of EYFP and GRK4 tagged with the c‐terminus of the same fluorophore shows minimal fluorescent signal (pseudocolored green) at the basal state. Fenoldopam treatment markedly increases the signal at the perinuclear area.
Figure 8. Figure 8.

D3R and GRK4 interaction in human renal proximal tubule cells. Top: human renal proximal tubule cells (hPTCs) grown on cover slips were serum‐starved for 1 h and treated with the D3R agonist PD128907 (1 μM) at the indicated duration of treatment. The cell membrane was labeled with a membrane‐impermeant biotin, after which the cells were fixed and permeabilized, and double immunostained for D3R (pseudocolored red) and GRK4 (pseudocolored green). The membrane (pseudocolored blue) was probed with Cy3‐conjugated avidin. The distribution and co‐localization of the proteins of D3R (pseudocolored red) and GRK4 (pseudocolored green) were evaluated by laser scanning confocal microscopy. Both the receptor and GRK4 are distributed in both the cell membrane (CM, pseudocolored blue) and the cytoplasm under basal conditions. Receptor activation promoted the internalization and colocalization (yellow in merge and inset images) of D3R and GRK4 at the perinuclear area. Bottom: hPTCs were double‐transfected with D3R and GRK4 tagged with the c‐ and n‐termini of the fluorescent protein EYFP, respectively. The cells were grown for 48 h post‐transfection, serum‐starved for 2 h, stimulated with the D3R agonist PD128907 (1 μM) at the indicated time points, and then prepared for confocal microscopy. The cell membrane (CM) was biotinylated with a membrane‐impermeant biotin to allow visualization (pseudocolored red) and co‐localization with the BiFC signal (pseudocolored green). Colocalization of the BiFC signal with the CM is indicated by yellow punctate areas in merge images. An overlay of the BiFC signal and the nucleus (pseudocolored blue) is shown to indicate intracellular distribution. Under basal conditions, minimal BiFC signal is observed at the CM and cytoplasm. D3R stimulation markedly enhanced the interaction of the receptor and GRK4, which is observed in both the CM and perinuclear area. Untransfected cells treated with the D3R agonist for 5 min were used as negative control (control). Scale bar = 10 μm.
Figure 9. Figure 9.

GRK4 Structure. Schematic representation of the structure of GRK4 with the polymorphisms. The positions of the GRK4 gene variants associated with hypertension are shown in red. The numbers represent amino acid residues in GRK4.
Figure 10. Figure 10.

Differential effect of GRK4 wild‐type versus variants on blood pressure regulation. Stimulation of D1R and D3R by dopamine leads to receptor phosphorylation/modification by wild‐type GRK4, which in turn results in decreased sodium reabsorption in the proximal tubule (and other nephron segments) and increased sodium excretion (natriuresis) and normal blood pressure. The D3R keeps the AT1R expression in check. In the presence of GRK4 sequence variants, there is inherent uncoupling of the dopamine receptors with their cognate G proteins and hyperphosphorylation of the receptors, resulting in increased sodium reabsorption and retention, and consequently to high blood pressure. A dysfunction of the D3R could presumably lead to increased AT1R expression, which further exacerbates the retention of sodium in the body.


Figure 1.

Distribution of the dopamine receptor subtypes along the nephron. OS: outer stripe; IS: inner stripe (composite from several mammals, including humans).



Figure 2.

D1R and D3R colocalization in renal proximal tubule cells from WKY rats. The cells were washed, fixed, and immunostained for D1R and D3R receptors. Basal colocalization appears as discreet yellow areas in the merge image of FITC‐tagged D1R (pseudocolored green) and Alexa 568‐tagged D3R (pseudocolored red).



Figure 3.

Proposed schema of dopamine signaling in renal proximal tubule cells during salt‐replete states. The dopaminergic response to conditions of salt repletion presumably involves both D1R and D3R acting synergistically; other dopamine receptors may take part in the physiological response, as well. During these conditions, the dopaminergic system is activated and the intrarenally produced dopamine occupies both D1 and D3 receptors (dopamine affinity for the dopamine receptors: D3R≥D4R>D5R>D2R>D1R). The D1R, mediated by Gαs, activates adenylyl cyclase, leading to increased intracellular cAMP/PKA, which, in turn, inhibits sodium transport in the renal proximal tubule cells and promotes natriuresis. Concurrently, the occupation of D3R by dopamine leads to increased Gβγ, which targets the C1b domain of adenylyl cyclases (other than adenylyl cyclase V, the preferred target of D3R‐associated Gαi) to augment the synthesis of cAMP mediated by D1R (and thus, the inhibition of sodium transport, green arrow), and to Gαi3 to directly inhibit NHE3 activity (GαS can also directly inhibit NHE3). Adenylyl cyclase isoforms IV, V, and VIII are not expressed in the proximal tubules. D3R can also couple to Gαs to abet the adenylyl cyclase activity by itself (green arrow). During prolonged periods of salt repletion (blue arrow), the D3R upregulates the expression of D1R and ETB to ensure continued natriuresis, and downregulates AT1R expression, directly by itself and indirectly through D1R, to attenuate its anti‐natriuretic effects. Hence, the D1R and D3R work in concert to promote natriuresis during salt‐replete states. Dopamine may work in the same manner in other nephron segments, however, the processes involved in these segments are still not completely worked out.



Figure 4.

AT1R is ubiquitinated and the ubiquitination of AT1R is initiated at the plasma membrane. Ubiquitination of the enhanced green fluorescence (EGF)‐tagged human AT1R is initiated at the plasma membrane in HEK293 cells heterologously expressing the human AT1R and human D5R. In vehicle‐treated cells, AT1R (pseudocolored green) is mainly at the membrane but is also observed in the cytoplasm. Ubiquitin (pseudocolored blue) and the proteasome marker, p44S10 (pseudocolored red) are scattered throughout the cytoplasm. The D5R agonist fenoldopam promotes the colocalization of AT1R, p44S10, and ubiquitin at the plasma membrane. The changes in color indicate colocalization: yellow = colocalization of AT1R and p44S10; cyan = colocalization of AT1R and ubiquitin; magenta = colocalization of p44S10 and ubiquitin; white = colocalization of AT1R, ubiquitin, and p44S10. The merging of the line drawings, red, green, and/or blue also depicts the colocalization of the different proteins. Scale bars are shown in vehicle‐treated cells.



Figure 5.

D3R and ETB interaction in Wistar‐Kyoto (WKY) rat renal proximal tubule cells. Renal proximal tubule cells from WKY rats grown on cover slips were treated for 30 min with a D3R agonist (PD128907), D3R antagonist (GR103691), ETB antagonist (BQ788), vehicle (PBS), or a combination of the D3R agonist with either antagonist after a 1‐h serum starvation. The cell membrane was labeled with the cell‐impermeant EZ‐link sulfo‐NHS‐SS‐Biotin for 30 min on ice. The cells were then fixed and permeabilized, double‐immunostained for D3R and ETB, and counterstained with FITC‐conjugated avidin to label the cell membrane. Images were obtained for D3R (pseudocolored red), ETB (pseudocolored green), cell membrane (pseudocolored blue) and the nucleus (pseudocolored magenta), via laser confocal microscopy. Under basal condition, both receptors are found at the cell membrane, with negligible colocalization. D3R activation results in the internalization of both receptors and in increased colocalization (yellow punctate areas in inset image; white arrows). No changes in the distribution or extent of colocalization are observed with either D3R or ETB antagonist treatment alone, or as co‐treatment.



Figure 6.

Signal transduction of a dopamine receptor. Upon ligand binding to the dopamine receptor (DR), the cognate G protein dissociates into Gα and Gβγ subunits. The Gβγ recruits G protein‐coupled receptor kinase that then phosphorylates/modifies the receptor. This covalent modification of the receptor prevents it from interacting with G proteins and allows it to associate with other proteins, for example, β‐arrestins, clathrin, and dynamin, to facilitate its endocytosis. Depending on the receptor subtype, the Gα subunit either activates or inhibits adenylyl cyclase to increase or decrease cAMP levels to promote specific downstream signaling pathways.



Figure 7.

D1R and GRK4 interaction in human renal proximal tubule cells. The interaction between D1R and GRK4 was evaluated through confocal microscopy and bimolecular fluorescence complementation (BiFC) assay in human renal proximal tubule cells (hPTCs). Top: serum‐starved hPTCs grown on cover slips were treated with the D1‐like receptor agonist fenoldopam (1 μM, 5 min), fixed and permeabilized, double immunostained for D1R and GRK4, and observed via laser scanning confocal microscopy. At basal conditions, the receptor (red) is distributed mostly at the cytoplasm and partially at the plasma membrane, while GRK4 (green) is localized in both the cytoplasm and cell membrane. Fenoldopam treatment promotes the redistribution of both proteins to the perinuclear area, where colocalization (yellow) is observed the most. Bottom: to confirm these observations, BiFC assay was performed in hPTCs. This technique is based on the in situ formation of a fluorescent complex when two nonfluorescent fragments of a fluorophore are brought together by the interaction between the proteins tagged with the fragments and thus allows the visualization of protein‐protein interaction in cells with neither the need to disrupt subcellular compartmentalization nor the use of exogenous fluorophore‐labeled antibodies. hPTCs heterologously expressing D1R tagged with the n‐terminus of EYFP and GRK4 tagged with the c‐terminus of the same fluorophore shows minimal fluorescent signal (pseudocolored green) at the basal state. Fenoldopam treatment markedly increases the signal at the perinuclear area.



Figure 8.

D3R and GRK4 interaction in human renal proximal tubule cells. Top: human renal proximal tubule cells (hPTCs) grown on cover slips were serum‐starved for 1 h and treated with the D3R agonist PD128907 (1 μM) at the indicated duration of treatment. The cell membrane was labeled with a membrane‐impermeant biotin, after which the cells were fixed and permeabilized, and double immunostained for D3R (pseudocolored red) and GRK4 (pseudocolored green). The membrane (pseudocolored blue) was probed with Cy3‐conjugated avidin. The distribution and co‐localization of the proteins of D3R (pseudocolored red) and GRK4 (pseudocolored green) were evaluated by laser scanning confocal microscopy. Both the receptor and GRK4 are distributed in both the cell membrane (CM, pseudocolored blue) and the cytoplasm under basal conditions. Receptor activation promoted the internalization and colocalization (yellow in merge and inset images) of D3R and GRK4 at the perinuclear area. Bottom: hPTCs were double‐transfected with D3R and GRK4 tagged with the c‐ and n‐termini of the fluorescent protein EYFP, respectively. The cells were grown for 48 h post‐transfection, serum‐starved for 2 h, stimulated with the D3R agonist PD128907 (1 μM) at the indicated time points, and then prepared for confocal microscopy. The cell membrane (CM) was biotinylated with a membrane‐impermeant biotin to allow visualization (pseudocolored red) and co‐localization with the BiFC signal (pseudocolored green). Colocalization of the BiFC signal with the CM is indicated by yellow punctate areas in merge images. An overlay of the BiFC signal and the nucleus (pseudocolored blue) is shown to indicate intracellular distribution. Under basal conditions, minimal BiFC signal is observed at the CM and cytoplasm. D3R stimulation markedly enhanced the interaction of the receptor and GRK4, which is observed in both the CM and perinuclear area. Untransfected cells treated with the D3R agonist for 5 min were used as negative control (control). Scale bar = 10 μm.



Figure 9.

GRK4 Structure. Schematic representation of the structure of GRK4 with the polymorphisms. The positions of the GRK4 gene variants associated with hypertension are shown in red. The numbers represent amino acid residues in GRK4.



Figure 10.

Differential effect of GRK4 wild‐type versus variants on blood pressure regulation. Stimulation of D1R and D3R by dopamine leads to receptor phosphorylation/modification by wild‐type GRK4, which in turn results in decreased sodium reabsorption in the proximal tubule (and other nephron segments) and increased sodium excretion (natriuresis) and normal blood pressure. The D3R keeps the AT1R expression in check. In the presence of GRK4 sequence variants, there is inherent uncoupling of the dopamine receptors with their cognate G proteins and hyperphosphorylation of the receptors, resulting in increased sodium reabsorption and retention, and consequently to high blood pressure. A dysfunction of the D3R could presumably lead to increased AT1R expression, which further exacerbates the retention of sodium in the body.

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Article Title: Dopamine and Renal Function and Blood Pressure Regulation
 

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Ines Armando, Van Anthony M. Villar, Pedro A. Jose. Dopamine and Renal Function and Blood Pressure Regulation. Compr Physiol 2011, 1: 1075-1117. doi: 10.1002/cphy.c100032