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Neuroendocrine Regulation of Hydromineral Homeostasis

Andre de Souza Mecawi, Silvia Graciela Ruginsk, Lucila Leico Kagohara Elias, Wamberto Antonio Varanda, Jose Antunes‐Rodrigues

10.1002/cphy.c140031

Source: Volume 5, Issue 3, July 2015

Published online: June 2015

Full Article on Wiley Online Library



ABSTRACT

Since the crucial evolutionary change from an aqueous to a terrestrial environment, all living organisms address the primordial task of equilibrating the ingestion/production of water and electrolytes (primarily sodium) with their excretion. In mammals, the final route for the excretion of these elements is mainly through the kidneys, which can eliminate concentrated or diluted urine according to the requirements. Despite their primary role in homeostasis, the kidneys are not able to recover water and solutes lost through other systems. Therefore, the selective stimulation or inhibition of motivational and locomotor behavior becomes essential to initiate the search and acquisition of water and/or sodium from the environment. Indeed, imbalances affecting the osmolality and volume of body fluids are dramatic challenges to the maintenance of hydromineral homeostasis. In addition to behavioral changes, which are integrated in the central nervous system, most of the systemic responses recruited to restore hydroelectrolytic balance are accomplished by coordinated actions of the cardiovascular, autonomic and endocrine systems, which determine the appropriate renal responses. The activation of sequential and redundant mechanisms (involving local and systemic factors) produces accurate and self‐limited effector responses. From a physiological point of view, understanding the mechanisms underlying water and sodium balance is intriguing and of great interest for the biomedical sciences. Therefore, the present review will address the biophysical, evolutionary and historical perspectives concerning the integrative neuroendocrine control of hydromineral balance, focusing on the major neural and endocrine systems implicated in the control of water and sodium balance. © 2015 American Physiological Society. Compr Physiol 5:1465‐1516, 2015.

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Figure 1. Figure 1. Primary paths for water and sodium management in the adult organism. The main input signal is rendered by water and sodium ingestion in liquids and food, although some water can also be produced by endogenous metabolism. The principal route for water and sodium excretion takes place in the kidneys. However, water can be lost during humidification of the inspired air and also through sweating. Sweat contains sodium (although sodium concentrations in sweat are smaller than in the plasma). Reproduced with the permission from Ruginsk and coworkers (2015) (399).
Figure 2. Figure 2. A simple device to estimate the osmotic pressure of a solution. Thistle tube 1 contains 10 mmol/L sucrose; tube 2 contains 50 mmol/L sucrose, tube 3 contains 100 mmol/L sucrose, and tube 4 contains 50 mmol/L NaCl. Arrows indicate the final level of solution in the tubes.
Figure 3. Figure 3. Osmotic coefficients for solutions of Sucrose and NaCl against their molal concentration. Data for NaCl was obtained from Appendix 8.10, Table 1 (page 483) and for sucrose from Appendix 8.6 Table 1 (page 478) from Robson and Stockes (1968) (397).
Figure 4. Figure 4. Swelling and shrinkage of rabbit cardiac myocytes when exposed to an isosmotic solution (330 mosm/L—marked as 1T in the graph), to a hyposmotic solution (165 mosm/L—marked as 0.5T in the graph) and to a hyperosmotic solution (660 mosm/L—marked as 2T in the graph). Axes in the figure were redrawn from the original to improve resolution. Reproduced with the permission from Suleymanian and Baumgarten (1996) (459).
Figure 5. Figure 5. Volume changes induced in red blood cells of cow, human, rat, and mouse by exposure to a 250 mmol/L urea inward directed gradient. Cells were initially bathed in PBS and urea added at time zero. The temporal evolution of volume decrease was estimated by measuring the intensity of scattered light. Axes in the figure were redrawn from the original to improve resolution.Traces of interest reproduced with permission from Liu and co‐workers (2011) (274).
Figure 6. Figure 6. Time course of the column height (or pressure) for a membrane impermeable to sucrose and permeable to urea. Experimental arrangement as in Figure 1. Arrows indicate the maximum pressure difference achieved in each case.
Figure 7. Figure 7. Increased osmotic water permeability of Channel‐forming integral protein of 28 kDa (CHIP28) RNA‐injected Xenopus oocytes. After 72 h, control‐injected and CHIP28 RNA‐injected (10 ng) oocytes were transferred from 200 mosM to 70 mosM modified Barth's buffer, and changes in size were observed by videomicroscopy. (A) Osmotic swelling of representative control‐injected (open circles) and CHIP28 RNA‐injected (filled squares) oocytes. Time of rupture is denoted (X). (B) Photos of injected oocytes at indicated times. Oocytes injected with CHIP28 RNA (3 min) or control (5 min) are denoted 3/5. Reproduced with the permission from Preston and coworkers (1992) (376).
Figure 8. Figure 8. Transduction mechanism of osmorreceptor neurons. (A) Representative tracing from a magnocellular neuron membrane voltage variation in response to hyperosmolality (depolarization and increased action‐potential firing) and hypo‐osmolality (hyperpolarization and reduced action‐potential firing); (B) graph showing the inverse correlation between extracellular fluid (ECF) osmolality and magnocellular neuron volume (nV, normalized to control volume); (C) diagram showing the magnocellular neurons changing ionic strength in response to hypotonic and hypertonic environments; (D) demonstration of the restoration of cell volume through suction applied to the recording pipette is able to reverse the reduction on cationic membrane conductance (G) caused by a hypo‐osmotic stimulus in osmorreceptor neurons. (E) Conversely, demonstration of the restoration of cell volume through increased pipette pressure is able to reverse the increase in cationic membrane conductance caused by a hyperosmotic stimulus. Reproduced with the permission from Bourque (2008) (57).
Figure 9. Figure 9. Schematic organization of lamina terminalis (LT) structures. The LT is composed by dorsal (D) and ventral (V) parts of the median preoptic nucleus (MnPO) and two other CVOs, the subfornical organ (SFO) and the organum vasculosum of the lamina terminalis (OVLT). The OVLT and the ventral (V) portion of MnPO, together with both the preoptic periventricular region and the anterior periventricular hypothalamic area, constitute the anteroventral region of the third cerebral ventricle (AV3V). The LT nuclei are interconnected by the MnPO, which presents bidirectional projections between both the SFO and OVLT (dashed arrows in black). The LT nuclei are also hardly connected with other brain areas related to the control of sympathetic activity and neuro‐humoral and behavioral responses (arrows in gray).
Figure 10. Figure 10. Sagittal illustration showing the main rat brain nucleus and connections related to the neural regulation of hydromineral balance. We can see the complex interconnections among the lamina terminalis nuclei [organum vasculosum of the lamina terminalis (OVLT), subfornical organ (SFO) and median preoptic nucleus (MnPO)], paraventricular (PVN) and supraoptic (SON) hypothalamic nucleus, midbrain dorsal raphe (DRN) and lateral parabrachial nucleus (LPBN), medullary nucleus of the solitary tract (NTS), area postrema (AP), caudal ventral lateral medulla (CVLM), and rostral ventral lateral medulla (RVLM). The blood‐borne signals (ANG II, ANP, OXT, AVP, Na+, and osmolality) are monitored by the circumventricular organs that responsible for transmitting these informations to others brain nuclei. Conversely, most of the peripheral afferents (baroreceptors, chemoreceptors, osmoreceptors, volume receptors and gustatory information) reach the NTS through the vagus and/or glossopharyngeal nerve, which redistribute this information to several brain areas. Finally, all humoral and sensory signals constitute multimodal information that are accurately integrated by the central nervous system, which use several neuroendocrine systems (neurohypophyseal, renin‐angiotensin, sympathetic, and atrial natriuretic peptides systems) to control the extracellular volume and osmolality. ac, anterior commissural nucleus; ANG II, angiotensin II; ANP, atrial natriuretic peptide; AVP, vasopressin; oc, optic chiasm; OXT, oxytocin. Modified with permission from Bourque (2008) (57).
Figure 11. Figure 11. Diagram representing several mechanisms implied in the neuroendocrine control of hydromineral balance mediated by organum vasculosum of the lamina terminalis (OVLT) and subfornical organ (SFO). (A) The circumventricular organs (CVOs) are devoided of blood‐brain barrier (BBB) and, consequently, they are able to sense circulating factors that are unable to cross the BBB, such as plasma angiotensin II (ANG II) acting on the CVOs ANG II type 1 receptors (AT1) receptors; (B) The OVLT and SFO also express all components of the renin‐angiotensin system, which constitute the sources of brain ANG II synthesis, release and action as a neurotransmitter/neuromodulator; (C) OVLT and SFO are the primary brain site responsible for detecting changes in plasma osmolality, mechanism which seems to be mediated by the plasma membrane transient receptor potencial vanilloid (TRPV) receptors located in the osmorreceptors neurons; (D) the participation of glial cells in the central Na+‐sensory mechanisms mediated by sodium sensors channels (Nax) channels expressed in the CVOs are responsible for monitoring plasma and cerebrospinal fluid Na+ concentrations; (E) The OVLT and SFO also receives projections from several brain areas related to the control of hydromineral and cardiovascular balance; (F) the lamina terminalis process and redistribute all collected information to other brain areas related to the neuroendocrine control of hydromineral balance. Thus, the lamina terminalis is a key part of the neuroendocrine control of thirst, sodium appetite, arterial pressure, sympathetic activity, renal function and neurohypophyseal vasopressin (AVP) and oxytocin (OXT) secretion. ACE, angiotensin converting enzyme; Agt, angiotensinogen; R1/R2/R3, different receptors for various neurotransmitters.
Figure 12. Figure 12. Photomicrographs presenting immunoreactive AVP (red) and OXT (green) neurons in the supraoptic nucleus of euhydrated, water‐restricted or salt‐loaded rats (A1‐C2). Merge images, exhibiting the colocalization of OXT and AVP in the same neuron (yellow) (A3‐C3). Scale bar = 25 μm. OC = optic chiasm. In D are the number of immunoreactive neurons observed in each experimental condition (** P < 0.005). Reproduced with the permission from Da Silva and co‐workers (2015) (102).
Figure 13. Figure 13. Schematic organization of the PVN [gray (magnocellular) or white (parvocellular) areas delimited by dashed lines] and SON (black areas). The anterior parvocellular subpopulation (PaAP), which coexists with the anterior commissural (AC) magnocellular group, and the periventricular group (PeP), which lies adjacently to the third ventricle walls throughout the rostrocaudal extent of the PVN, are not shown here. Cir, circular accessory group; f, fornix; PaDC, dorsomedial cap of the PVN; PaLM, lateral magnocellular area of the PVN; PaMM, medial magnocellular area of the PVN; PaMP, medial parvocellular group of the PVN; PaPo, posterior parvocellular group of the PVN; PaV, ventral parvocellular part of the PVN; PeM, periventricular magnocellular group of the PVN; SOR, residual SON. Based on the organization revised by Armstrong (1995) (31).
Figure 14. Figure 14. Schematic diagram showing the modulation of the lateral parabrachial nucleus (LPBN) inhibitory mechanism by different neurotransmitters and its interaction with forebrain facilitatory mechanisms involved in the control of sodium intake. 5‐HT, serotonin; ANG II, angiotensin II; AP, area postrema; CCK, cholecystokinin; CRH, corticotrophin‐releasing hormone; OVLT, OVLT organum vasculosum of the lamina terminalis; SFO, subfornical organ; NTS, nucleus of the solitary tract. Reproduced with the permission from Menani and co‐workers (2014) (314).
Figure 15. Figure 15. Diagram representing the combined effects of volume and osmolality changes in vasopressin (AVP) plasma concentrations (arbitrary units). Under basal conditions AVP plasma concentrations are hypervolemia can further reduce these values. Conversely, hypovolemia (greater than 10% of blood volume) increases AVP secretion, although the main factor stimulating the secretion of this peptide is hyperosmolality. With decreased blood volume, the set point for hyperosmolality‐induced increase in AVP secretion is shifted to a lower plasma osmolality and the slope is increased. Increase in blood volume produces the opposite effects. Max: maximum. Reproduced with the permission from Koeppen and Stanton (2013) (246).
Figure 16. Figure 16. Diagram representing the effects of volume and osmolality changes in oxytocin (OXT) and atrial natriuretic peptide (ANP) plasma concentrations. Increases in extracellular fluid (ECF) volume or venous return enhance the release of natriuretic peptides, particularly ANP, from the heart. ANP then stimulates the release of OXT from the neurohypophysis (upper panel). These two hormones act synergistically to increase renal sodium excretion. These responses are observed following both isotonic and hypertonic increases in ECF volume, with this latter experimental situation producing a greater effect on ANP and OXT release. Under decreased ECF volume (with unchanged ECF osmolality), ANP release is suppressed and OXT release is stimulated (lower panel).
Figure 17. Figure 17. Diagram representing the cascade of renin‐angiotensin system components formation, enzymes involved in these processes and target receptors to each peptide.
Figure 18. Figure 18. Diagram demonstrating the intracellular pathway activated by AT1 receptors. The AT1 receptor is coupled to a Gq protein which activate the phospholipase C (PLC) enzyme, responsible for cleave the phosphatidylinositol bisphosphate (PIP2, a plasma membrane phospholipid) producing inositol 3‐phosphate (IP3) and diacilglicerol (DAG). The IP3 is responsible for increase intracellular Ca2+ concentration, while the DAG activates the protein kinase C (PKC). Additionally, AT1 receptors activate several other pathways, such as mitogen‐activated protein kinase (MAPKs) pathway which include extracellular regulated kinase types 1 and 2 (ERK 1/2), and its effect can be dependent or independent (mediated by β‐arretin) of Gq protein activation. Daniels and co‐workers (2005; 2009) demonstrated that ANG II‐induced thirst is depent of PKC pathway activation, while ANG II‐induced sodium appetite is depent of MAPK pathway activation, demonstrating that thirst and sodium appetite induced by ANG II are processed by distinct intracellular pathways (106,107). Src, kinase protein family; Ras, GTPase.
Figure 19. Figure 19. Schematic representation of the main actions of atrial natriuretic peptide (ANP) on body fluid homeostasis. The dashed lines represent inhibitory actions of ANP on: (i) the release of vasopressin (AVP) by the neurohypophysis; (ii) the production and release of aldosterone (Aldo) from the medullar portion of the adrenal gland; (iii) the production and release of renin (Ren) from the renal juxtamedular apparatus; and (iv) the release of norepinephrine (Nor) from sympathetic terminals innervating blood vessels. ANP actions decreasing Ren activity produce the impairment of the conversion of the precursor angiotensinogen to angiotensin I (ANG I) and, consequently, decrease angiotensin II (ANG II) production. The combined effects of decreased ANG II, AVP, and Nor release contribute to ANP‐induced vasodilation, although a direct action of ANP decreasing vascular resistance has been already recognized. The reduced ANG II production and secretion is also involved in the diminished production of Aldo.
Figure 20. Figure 20. Atrial natriuretic peptide (ANP) binds to NPRA and NPRC, which are expressed by the basolateral membrane of tubular cells. The binding of ANP or other natriuretic peptides to NPRC produces the internalization of the ligand‐receptor complex, which is then degraded or recycled. NPRA, in turn, exhibits an intracellular guanylyl cyclase (GS) domain. ANP binding to NPRA stimulates the production of cyclic monophosphate of guanosine (cGMP), which is responsible for the natriuretic effect of ANP, characterized by the closing of epithelial Na+ channels (ENaCs) located in the apical membrane of distal tubular cells. The activity of the enzyme phosphodiesterase (PD), which converts cGMP to GMP, may be increased by angiotensin II (ANG II) increased circulating levels, thus reducing ANP‐mediated natriuretic effects. This mechanism is particularly involved in the pathogenesis of congestive heart failure.
Figure 21. Figure 21. Scheme presenting potential consequences of diverse environmental factors (lifestyle, hydromineral balance and/or challenges, neuroendocrine disturbances, dietary composition, and drug use) at various stages of developmental programing of thirst and sodium appetite, and also the predisposition to pathological conditions such as hypertension and/or kidney damage. Reproduced with the permission (graphical abstract) from Mecawi and co‐workers (2015) (312).
Figure 22. Figure 22. The effects of estradiol cypionate (EC, 10 or 40 μg/kg) on the activation of neurohypophyseal systems in response to hemorrhage in OVX rats. In A and B are showed, respectively, the plasma vasopressin and oxytocin levels in basal condition and after hemorrhage. The number of animals/group is shown in the respective bar. * P < 0.05, ** P < 0.01, and *** P < 0.001 between basal and hemorrhage levels. +P < 0.05, ++P < 0.01, and +++P < 0.001 between the OVX‐oil and OVX‐EC groups. In C are showed representative photomicrographs (coronal sections) of the SON showing c‐Fos/AVP immunoreactive neurons in sham or hemorrhage rats pretreated with oil or EC. In detail, the SON is shown in a small magnification. Scale bar: 100 μm. Reproduced with the permission from Mecawi and coworkers (2011) (313).


Figure 1. Primary paths for water and sodium management in the adult organism. The main input signal is rendered by water and sodium ingestion in liquids and food, although some water can also be produced by endogenous metabolism. The principal route for water and sodium excretion takes place in the kidneys. However, water can be lost during humidification of the inspired air and also through sweating. Sweat contains sodium (although sodium concentrations in sweat are smaller than in the plasma). Reproduced with the permission from Ruginsk and coworkers (2015) (399).


Figure 2. A simple device to estimate the osmotic pressure of a solution. Thistle tube 1 contains 10 mmol/L sucrose; tube 2 contains 50 mmol/L sucrose, tube 3 contains 100 mmol/L sucrose, and tube 4 contains 50 mmol/L NaCl. Arrows indicate the final level of solution in the tubes.


Figure 3. Osmotic coefficients for solutions of Sucrose and NaCl against their molal concentration. Data for NaCl was obtained from Appendix 8.10, Table 1 (page 483) and for sucrose from Appendix 8.6 Table 1 (page 478) from Robson and Stockes (1968) (397).


Figure 4. Swelling and shrinkage of rabbit cardiac myocytes when exposed to an isosmotic solution (330 mosm/L—marked as 1T in the graph), to a hyposmotic solution (165 mosm/L—marked as 0.5T in the graph) and to a hyperosmotic solution (660 mosm/L—marked as 2T in the graph). Axes in the figure were redrawn from the original to improve resolution. Reproduced with the permission from Suleymanian and Baumgarten (1996) (459).


Figure 5. Volume changes induced in red blood cells of cow, human, rat, and mouse by exposure to a 250 mmol/L urea inward directed gradient. Cells were initially bathed in PBS and urea added at time zero. The temporal evolution of volume decrease was estimated by measuring the intensity of scattered light. Axes in the figure were redrawn from the original to improve resolution.Traces of interest reproduced with permission from Liu and co‐workers (2011) (274).


Figure 6. Time course of the column height (or pressure) for a membrane impermeable to sucrose and permeable to urea. Experimental arrangement as in Figure 1. Arrows indicate the maximum pressure difference achieved in each case.


Figure 7. Increased osmotic water permeability of Channel‐forming integral protein of 28 kDa (CHIP28) RNA‐injected Xenopus oocytes. After 72 h, control‐injected and CHIP28 RNA‐injected (10 ng) oocytes were transferred from 200 mosM to 70 mosM modified Barth's buffer, and changes in size were observed by videomicroscopy. (A) Osmotic swelling of representative control‐injected (open circles) and CHIP28 RNA‐injected (filled squares) oocytes. Time of rupture is denoted (X). (B) Photos of injected oocytes at indicated times. Oocytes injected with CHIP28 RNA (3 min) or control (5 min) are denoted 3/5. Reproduced with the permission from Preston and coworkers (1992) (376).


Figure 8. Transduction mechanism of osmorreceptor neurons. (A) Representative tracing from a magnocellular neuron membrane voltage variation in response to hyperosmolality (depolarization and increased action‐potential firing) and hypo‐osmolality (hyperpolarization and reduced action‐potential firing); (B) graph showing the inverse correlation between extracellular fluid (ECF) osmolality and magnocellular neuron volume (nV, normalized to control volume); (C) diagram showing the magnocellular neurons changing ionic strength in response to hypotonic and hypertonic environments; (D) demonstration of the restoration of cell volume through suction applied to the recording pipette is able to reverse the reduction on cationic membrane conductance (G) caused by a hypo‐osmotic stimulus in osmorreceptor neurons. (E) Conversely, demonstration of the restoration of cell volume through increased pipette pressure is able to reverse the increase in cationic membrane conductance caused by a hyperosmotic stimulus. Reproduced with the permission from Bourque (2008) (57).


Figure 9. Schematic organization of lamina terminalis (LT) structures. The LT is composed by dorsal (D) and ventral (V) parts of the median preoptic nucleus (MnPO) and two other CVOs, the subfornical organ (SFO) and the organum vasculosum of the lamina terminalis (OVLT). The OVLT and the ventral (V) portion of MnPO, together with both the preoptic periventricular region and the anterior periventricular hypothalamic area, constitute the anteroventral region of the third cerebral ventricle (AV3V). The LT nuclei are interconnected by the MnPO, which presents bidirectional projections between both the SFO and OVLT (dashed arrows in black). The LT nuclei are also hardly connected with other brain areas related to the control of sympathetic activity and neuro‐humoral and behavioral responses (arrows in gray).


Figure 10. Sagittal illustration showing the main rat brain nucleus and connections related to the neural regulation of hydromineral balance. We can see the complex interconnections among the lamina terminalis nuclei [organum vasculosum of the lamina terminalis (OVLT), subfornical organ (SFO) and median preoptic nucleus (MnPO)], paraventricular (PVN) and supraoptic (SON) hypothalamic nucleus, midbrain dorsal raphe (DRN) and lateral parabrachial nucleus (LPBN), medullary nucleus of the solitary tract (NTS), area postrema (AP), caudal ventral lateral medulla (CVLM), and rostral ventral lateral medulla (RVLM). The blood‐borne signals (ANG II, ANP, OXT, AVP, Na+, and osmolality) are monitored by the circumventricular organs that responsible for transmitting these informations to others brain nuclei. Conversely, most of the peripheral afferents (baroreceptors, chemoreceptors, osmoreceptors, volume receptors and gustatory information) reach the NTS through the vagus and/or glossopharyngeal nerve, which redistribute this information to several brain areas. Finally, all humoral and sensory signals constitute multimodal information that are accurately integrated by the central nervous system, which use several neuroendocrine systems (neurohypophyseal, renin‐angiotensin, sympathetic, and atrial natriuretic peptides systems) to control the extracellular volume and osmolality. ac, anterior commissural nucleus; ANG II, angiotensin II; ANP, atrial natriuretic peptide; AVP, vasopressin; oc, optic chiasm; OXT, oxytocin. Modified with permission from Bourque (2008) (57).


Figure 11. Diagram representing several mechanisms implied in the neuroendocrine control of hydromineral balance mediated by organum vasculosum of the lamina terminalis (OVLT) and subfornical organ (SFO). (A) The circumventricular organs (CVOs) are devoided of blood‐brain barrier (BBB) and, consequently, they are able to sense circulating factors that are unable to cross the BBB, such as plasma angiotensin II (ANG II) acting on the CVOs ANG II type 1 receptors (AT1) receptors; (B) The OVLT and SFO also express all components of the renin‐angiotensin system, which constitute the sources of brain ANG II synthesis, release and action as a neurotransmitter/neuromodulator; (C) OVLT and SFO are the primary brain site responsible for detecting changes in plasma osmolality, mechanism which seems to be mediated by the plasma membrane transient receptor potencial vanilloid (TRPV) receptors located in the osmorreceptors neurons; (D) the participation of glial cells in the central Na+‐sensory mechanisms mediated by sodium sensors channels (Nax) channels expressed in the CVOs are responsible for monitoring plasma and cerebrospinal fluid Na+ concentrations; (E) The OVLT and SFO also receives projections from several brain areas related to the control of hydromineral and cardiovascular balance; (F) the lamina terminalis process and redistribute all collected information to other brain areas related to the neuroendocrine control of hydromineral balance. Thus, the lamina terminalis is a key part of the neuroendocrine control of thirst, sodium appetite, arterial pressure, sympathetic activity, renal function and neurohypophyseal vasopressin (AVP) and oxytocin (OXT) secretion. ACE, angiotensin converting enzyme; Agt, angiotensinogen; R1/R2/R3, different receptors for various neurotransmitters.


Figure 12. Photomicrographs presenting immunoreactive AVP (red) and OXT (green) neurons in the supraoptic nucleus of euhydrated, water‐restricted or salt‐loaded rats (A1‐C2). Merge images, exhibiting the colocalization of OXT and AVP in the same neuron (yellow) (A3‐C3). Scale bar = 25 μm. OC = optic chiasm. In D are the number of immunoreactive neurons observed in each experimental condition (** P < 0.005). Reproduced with the permission from Da Silva and co‐workers (2015) (102).


Figure 13. Schematic organization of the PVN [gray (magnocellular) or white (parvocellular) areas delimited by dashed lines] and SON (black areas). The anterior parvocellular subpopulation (PaAP), which coexists with the anterior commissural (AC) magnocellular group, and the periventricular group (PeP), which lies adjacently to the third ventricle walls throughout the rostrocaudal extent of the PVN, are not shown here. Cir, circular accessory group; f, fornix; PaDC, dorsomedial cap of the PVN; PaLM, lateral magnocellular area of the PVN; PaMM, medial magnocellular area of the PVN; PaMP, medial parvocellular group of the PVN; PaPo, posterior parvocellular group of the PVN; PaV, ventral parvocellular part of the PVN; PeM, periventricular magnocellular group of the PVN; SOR, residual SON. Based on the organization revised by Armstrong (1995) (31).


Figure 14. Schematic diagram showing the modulation of the lateral parabrachial nucleus (LPBN) inhibitory mechanism by different neurotransmitters and its interaction with forebrain facilitatory mechanisms involved in the control of sodium intake. 5‐HT, serotonin; ANG II, angiotensin II; AP, area postrema; CCK, cholecystokinin; CRH, corticotrophin‐releasing hormone; OVLT, OVLT organum vasculosum of the lamina terminalis; SFO, subfornical organ; NTS, nucleus of the solitary tract. Reproduced with the permission from Menani and co‐workers (2014) (314).


Figure 15. Diagram representing the combined effects of volume and osmolality changes in vasopressin (AVP) plasma concentrations (arbitrary units). Under basal conditions AVP plasma concentrations are hypervolemia can further reduce these values. Conversely, hypovolemia (greater than 10% of blood volume) increases AVP secretion, although the main factor stimulating the secretion of this peptide is hyperosmolality. With decreased blood volume, the set point for hyperosmolality‐induced increase in AVP secretion is shifted to a lower plasma osmolality and the slope is increased. Increase in blood volume produces the opposite effects. Max: maximum. Reproduced with the permission from Koeppen and Stanton (2013) (246).


Figure 16. Diagram representing the effects of volume and osmolality changes in oxytocin (OXT) and atrial natriuretic peptide (ANP) plasma concentrations. Increases in extracellular fluid (ECF) volume or venous return enhance the release of natriuretic peptides, particularly ANP, from the heart. ANP then stimulates the release of OXT from the neurohypophysis (upper panel). These two hormones act synergistically to increase renal sodium excretion. These responses are observed following both isotonic and hypertonic increases in ECF volume, with this latter experimental situation producing a greater effect on ANP and OXT release. Under decreased ECF volume (with unchanged ECF osmolality), ANP release is suppressed and OXT release is stimulated (lower panel).


Figure 17. Diagram representing the cascade of renin‐angiotensin system components formation, enzymes involved in these processes and target receptors to each peptide.


Figure 18. Diagram demonstrating the intracellular pathway activated by AT1 receptors. The AT1 receptor is coupled to a Gq protein which activate the phospholipase C (PLC) enzyme, responsible for cleave the phosphatidylinositol bisphosphate (PIP2, a plasma membrane phospholipid) producing inositol 3‐phosphate (IP3) and diacilglicerol (DAG). The IP3 is responsible for increase intracellular Ca2+ concentration, while the DAG activates the protein kinase C (PKC). Additionally, AT1 receptors activate several other pathways, such as mitogen‐activated protein kinase (MAPKs) pathway which include extracellular regulated kinase types 1 and 2 (ERK 1/2), and its effect can be dependent or independent (mediated by β‐arretin) of Gq protein activation. Daniels and co‐workers (2005; 2009) demonstrated that ANG II‐induced thirst is depent of PKC pathway activation, while ANG II‐induced sodium appetite is depent of MAPK pathway activation, demonstrating that thirst and sodium appetite induced by ANG II are processed by distinct intracellular pathways (106,107). Src, kinase protein family; Ras, GTPase.


Figure 19. Schematic representation of the main actions of atrial natriuretic peptide (ANP) on body fluid homeostasis. The dashed lines represent inhibitory actions of ANP on: (i) the release of vasopressin (AVP) by the neurohypophysis; (ii) the production and release of aldosterone (Aldo) from the medullar portion of the adrenal gland; (iii) the production and release of renin (Ren) from the renal juxtamedular apparatus; and (iv) the release of norepinephrine (Nor) from sympathetic terminals innervating blood vessels. ANP actions decreasing Ren activity produce the impairment of the conversion of the precursor angiotensinogen to angiotensin I (ANG I) and, consequently, decrease angiotensin II (ANG II) production. The combined effects of decreased ANG II, AVP, and Nor release contribute to ANP‐induced vasodilation, although a direct action of ANP decreasing vascular resistance has been already recognized. The reduced ANG II production and secretion is also involved in the diminished production of Aldo.


Figure 20. Atrial natriuretic peptide (ANP) binds to NPRA and NPRC, which are expressed by the basolateral membrane of tubular cells. The binding of ANP or other natriuretic peptides to NPRC produces the internalization of the ligand‐receptor complex, which is then degraded or recycled. NPRA, in turn, exhibits an intracellular guanylyl cyclase (GS) domain. ANP binding to NPRA stimulates the production of cyclic monophosphate of guanosine (cGMP), which is responsible for the natriuretic effect of ANP, characterized by the closing of epithelial Na+ channels (ENaCs) located in the apical membrane of distal tubular cells. The activity of the enzyme phosphodiesterase (PD), which converts cGMP to GMP, may be increased by angiotensin II (ANG II) increased circulating levels, thus reducing ANP‐mediated natriuretic effects. This mechanism is particularly involved in the pathogenesis of congestive heart failure.


Figure 21. Scheme presenting potential consequences of diverse environmental factors (lifestyle, hydromineral balance and/or challenges, neuroendocrine disturbances, dietary composition, and drug use) at various stages of developmental programing of thirst and sodium appetite, and also the predisposition to pathological conditions such as hypertension and/or kidney damage. Reproduced with the permission (graphical abstract) from Mecawi and co‐workers (2015) (312).


Figure 22. The effects of estradiol cypionate (EC, 10 or 40 μg/kg) on the activation of neurohypophyseal systems in response to hemorrhage in OVX rats. In A and B are showed, respectively, the plasma vasopressin and oxytocin levels in basal condition and after hemorrhage. The number of animals/group is shown in the respective bar. * P < 0.05, ** P < 0.01, and *** P < 0.001 between basal and hemorrhage levels. +P < 0.05, ++P < 0.01, and +++P < 0.001 between the OVX‐oil and OVX‐EC groups. In C are showed representative photomicrographs (coronal sections) of the SON showing c‐Fos/AVP immunoreactive neurons in sham or hemorrhage rats pretreated with oil or EC. In detail, the SON is shown in a small magnification. Scale bar: 100 μm. Reproduced with the permission from Mecawi and coworkers (2011) (313).
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Article Title: Neuroendocrine Regulation of Hydromineral Homeostasis
 

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Andre de Souza Mecawi, Silvia Graciela Ruginsk, Lucila Leico Kagohara Elias, Wamberto Antonio Varanda, Jose Antunes‐Rodrigues. Neuroendocrine Regulation of Hydromineral Homeostasis. Compr Physiol 2015, 5: 1465-1516. doi: 10.1002/cphy.c140031