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Neuroendocrine Regulation of Growth Hormone Secretion

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ABSTRACT

This article reviews the main findings that emerged in the intervening years since the previous volume on hormonal control of growth in the section on the endocrine system of the Handbook of Physiology concerning the intra‐ and extrahypothalamic neuronal networks connecting growth hormone releasing hormone (GHRH) and somatostatin hypophysiotropic neurons and the integration between regulators of food intake/metabolism and GH release. Among these findings, the discovery of ghrelin still raises many unanswered questions. One important event was the application of deconvolution analysis to the pulsatile patterns of GH secretion in different mammalian species, including Man, according to gender, hormonal environment and ageing. Concerning this last phenomenon, a great body of evidence now supports the role of an attenuation of the GHRH/GH/Insulin‐like growth factor‐1 (IGF‐1) axis in the control of mammalian aging. © 2016 American Physiological Society. Compr Physiol 6:687‐735, 2016.

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Figure 1. Figure 1. Contribution of feedback regulation to GH release. Ultrashort and short‐loop feedback mechanisms contribute largely to the generation of a single GH secretory event, modulating output over hours. This culminates in the ultradian pulsatile appearance of GH in circulation, defined by peaks and troughs in GH release. In turn, long‐loop feedback mechanisms contribute to the infradian regulation of secretion, modulating peak GH release and patterning over extended periods of time. Given homeostatic pressures (metabolic, reproductive, age associated), cross‐talk between short and long‐loop mechanisms (illustrated as white double arrows) ensure physiological GH secretion. For this, long‐loop feedback mechanisms will modulate ultradian responses, whereas ultradian patterns may impact infradian feedback.
Figure 2. Figure 2. Feedback mechanisms. The release of GH from the anterior pituitary gland is mediated through feedback mechanisms, acting on three levels. Somatostatin and GH release is controlled through ultrashort‐loop feedback (orange arrows), whereby somatostatin and GH modulates it own release. While ultrashort‐loop feedback is proposed for GHRH, evidence for this is not conclusive (illustrated by broken line arrow). GH pulsatility is regulated by short‐loop feedback between somatostatin, GHRH and GH (blue arrows). GH acts within the hypothalamus to stimulate somatostatin and possibly inhibit GHRH release in the median eminence (ME; note, for GHRH neurons, compelling evidence for GH feedback does not exist). Once released into portal circulation, somatostatin travels to the pituitary gland where it inhibits GH release, whereas GHRH stimulates GH release. In addition, somatostatin inhibits GHRH activity, and it is thought that GHRH neurons may stimulate somatostatin neuronal activity, and therefore somatostatin release. The release of GH relative to physiological demand is entrained through a number of peripheral factors. In this instance, long‐loop feedback (illustrated in green arrows) from insulin‐like growth factor‐1 (IGF‐1, produced in the liver in response to GH) results in the suppression of GH release through the stimulation of somatostatin release, and the inhibition of GH and GHRH release.
Figure 3. Figure 3. Interactions between somatostatin and GHRH that account for the pulsatile pattern of GH secretion. Comprehensive in vivo and in vitro assessment of the production and release of GH has resulted in the evolution of theory of peripheral and centrally mediated mechanisms that modulate the pulsatile release of GH. Periods of prevailing low levels of circulating GH (1) are associated with reduced somatostatin release into pituitary portal vasculature (2). The withdrawal of somatostatin inhibition of GHRH neurons (3) and somatotrophs (3) culminates in the release of GHRH into pituitary portal vasculature (4), and the stimulation of GH release (5). Periods of prevailing elevated levels of circulating GH (6) are associated with the activation of somatostatin‐expressing neurons (7) and inactivation of GHRH‐expressing neurons (7). The resulting rise in somatostatin activity contributes to the direct inhibition of GHRH‐neuronal activity (8) and the release of somatostatin into portal vasculature (8), culminating in reduced somatotroph activity (9) and the cessation of the release of GH into peripheral circulation (10). Complex interactions between central, pituitary and peripheral factors may disrupt these hypothalamic interactions, resulting in physiologically relevant GH release. Colored arrows indicate selective activation of mechanisms coupled with prevailing low/basal (left schematic) or elevated/peak (right schematic) levels of peripheral circulating GH. Green arrows indicate stimulatory pathways. Orange arrows indicate inhibitory pathways. Additional abbreviations: GHR, growth hormone receptor; SRIF‐R, somatostatin receptor; GHRH‐R, growth hormone releasing hormone receptor; PevN, periventricular nucleus; ArcN, arcuate nucleus; PG, pituitary gland.
Figure 4. Figure 4. Hypothalamic control—neuromodulators. The control of GH release from somatostatin and GHRH‐expressing neurons is mediated through interactions with hypothalamic neuromodulators. In this instance, dopamine (DA) and adrenaline [acting through selective activation of the α1‐receptor subtype (α1‐R)] stimulates somatostatin‐neuronal activity, thereby inhibiting GH release. Adrenaline [acting through selective activation of the α2‐receptor subtype (α2‐R)], serotonin (5‐HT), and acetylcholine (Ach) stimulate GH release, through inhibition of somatostatin‐expressing neurons. By comparison, activation of GHRH‐expressing neuronal activity by adrenaline (acting through selective activation of the α2‐R) and 5‐HT results in increased GH output. In turn, acting through select activation of the β2‐receptor subtype (β2‐R), adrenaline inhibits GH release by inhibiting GHRH‐neuronal activity. Stimulatory interactions are highlighted in green arrows. Inhibitory interactions are highlighted in orange arrows. Additional abbreviations: ME, median eminence.
Figure 5. Figure 5. Intrahypothalamic interactions—neuropeptides. Complex intrahypothalamic interactions control the activity of somatostatin‐expressing and GHRH‐expressing neurons, thereby regulating the pulsatile release of GH. Corticotrophin releasing hormone (CRH)‐expressing neurons within the paraventricular nucleus (PvN) stimulate somatostatin activity, thereby inhibiting GH release. This is modulated through activation of CRH‐expressing neurons by neuropeptide‐Y (NPY)‐expressing neurons within the arcuate nucleus (ArcN), acting through the Y‐1 (Y1‐R) and Y‐2 (Y2‐R) receptor subtypes. CRH activity is further modulated through activation of the melanocortin receptor subtype‐4 (MC4‐R). NPY‐expressing neurons further inhibit GH release through activation of somatostatin‐expressing neurons. Of interest, NPY‐expressing neurons may indirectly promote the release of GH through the activation of pro‐opiomelanocortin (POMC)‐expressing neurons, which inhibits somatostatin‐expressing neuronal activity. This control of GH release is further modulated through the stimulation of NPY‐expressing neurons by somatostatin (within the ArcN), and through activation of GHRH expressing neurons by low levels of somatostatin. Stimulatory interactions are highlighted in green arrows. Inhibitory interactions are highlighted in orange arrows. Additional abbreviations: ME, median eminence; SST1, somatostatin receptor subtype‐1, SST2, somatostatin receptor subtype‐2; SST3, somatostatin receptor subtype‐3; SST5, somatostatin receptor subtype‐5; Y1‐R, Neuropeptide‐Y specific receptor subtype‐1; Y2‐R, neuropeptide‐Y specific receptor subtype‐2; GAL‐R1, galanin receptor subtype‐1; GAL‐R2, galanin receptor subtype‐2; MC3R, melanocortin receptor subtype‐3.
Figure 6. Figure 6. Ghrelin acts within the hypothalamus and the anterior pituitary gland indirectly (through inhibiting somatostatin‐ and stimulating GHRH‐neuronal activity), and directly by stimulating somatotrophs, respectively. The actions of ghrelin are mediated through select activation of the GHS‐R. Actions of ghrelin on GH release may involve interactions with feeding circuits, specifically through neuropeptide‐Y (NPY)‐expressing neurons located within the arcuate nucleus (ArcN). Stimulatory interactions are highlighted in green arrows. Inhibitory interactions are highlighted in orange arrows. Additional abbreviations: ME, median eminence; PevN, periventricular nucleus; PvN, paraventricular nucleus; POMC, pro‐opiomelanocortin; GAL, galanin.
Figure 7. Figure 7. Differential GH secretory patterns between males and females. Mechanisms that promote GH output in adulthood are established during pubertal maturation. For males, this results in the establishment of adult‐specific GH release by 18 to 25 years of age, and the progressive decline in peak and total GH release with age. Differential patterns and amounts of GH release between males and females occur as a consequence of altered feedback to the hypothalamus and anterior pituitary gland, predominantly in response to circulating levels of estrogen. Increased circulating levels of estrogen are associated with an overall rise in peak amplitude, pulse frequency, and total GH release in females when compared to males. A further rise in peak and total GH release in females is observed during the follicular stage of the ovarian cycle, the period characterized by a rise in circulating levels of estrogen (peaking prior to ovulation). Feedback from placental‐derived GH to the anterior pituitary gland contributes to the suppression of maternal GH release during pregnancy. Resumption of maternal GH output following birth is critical for sustained milk production through prevention of involution of mammary gland tissue. Acting through direct mechanisms, or indirectly through insulin‐like growth factor‐1 (IGF‐1), GH is thought to further promote the transport of nutrients to maternal milk.


Figure 1. Contribution of feedback regulation to GH release. Ultrashort and short‐loop feedback mechanisms contribute largely to the generation of a single GH secretory event, modulating output over hours. This culminates in the ultradian pulsatile appearance of GH in circulation, defined by peaks and troughs in GH release. In turn, long‐loop feedback mechanisms contribute to the infradian regulation of secretion, modulating peak GH release and patterning over extended periods of time. Given homeostatic pressures (metabolic, reproductive, age associated), cross‐talk between short and long‐loop mechanisms (illustrated as white double arrows) ensure physiological GH secretion. For this, long‐loop feedback mechanisms will modulate ultradian responses, whereas ultradian patterns may impact infradian feedback.


Figure 2. Feedback mechanisms. The release of GH from the anterior pituitary gland is mediated through feedback mechanisms, acting on three levels. Somatostatin and GH release is controlled through ultrashort‐loop feedback (orange arrows), whereby somatostatin and GH modulates it own release. While ultrashort‐loop feedback is proposed for GHRH, evidence for this is not conclusive (illustrated by broken line arrow). GH pulsatility is regulated by short‐loop feedback between somatostatin, GHRH and GH (blue arrows). GH acts within the hypothalamus to stimulate somatostatin and possibly inhibit GHRH release in the median eminence (ME; note, for GHRH neurons, compelling evidence for GH feedback does not exist). Once released into portal circulation, somatostatin travels to the pituitary gland where it inhibits GH release, whereas GHRH stimulates GH release. In addition, somatostatin inhibits GHRH activity, and it is thought that GHRH neurons may stimulate somatostatin neuronal activity, and therefore somatostatin release. The release of GH relative to physiological demand is entrained through a number of peripheral factors. In this instance, long‐loop feedback (illustrated in green arrows) from insulin‐like growth factor‐1 (IGF‐1, produced in the liver in response to GH) results in the suppression of GH release through the stimulation of somatostatin release, and the inhibition of GH and GHRH release.


Figure 3. Interactions between somatostatin and GHRH that account for the pulsatile pattern of GH secretion. Comprehensive in vivo and in vitro assessment of the production and release of GH has resulted in the evolution of theory of peripheral and centrally mediated mechanisms that modulate the pulsatile release of GH. Periods of prevailing low levels of circulating GH (1) are associated with reduced somatostatin release into pituitary portal vasculature (2). The withdrawal of somatostatin inhibition of GHRH neurons (3) and somatotrophs (3) culminates in the release of GHRH into pituitary portal vasculature (4), and the stimulation of GH release (5). Periods of prevailing elevated levels of circulating GH (6) are associated with the activation of somatostatin‐expressing neurons (7) and inactivation of GHRH‐expressing neurons (7). The resulting rise in somatostatin activity contributes to the direct inhibition of GHRH‐neuronal activity (8) and the release of somatostatin into portal vasculature (8), culminating in reduced somatotroph activity (9) and the cessation of the release of GH into peripheral circulation (10). Complex interactions between central, pituitary and peripheral factors may disrupt these hypothalamic interactions, resulting in physiologically relevant GH release. Colored arrows indicate selective activation of mechanisms coupled with prevailing low/basal (left schematic) or elevated/peak (right schematic) levels of peripheral circulating GH. Green arrows indicate stimulatory pathways. Orange arrows indicate inhibitory pathways. Additional abbreviations: GHR, growth hormone receptor; SRIF‐R, somatostatin receptor; GHRH‐R, growth hormone releasing hormone receptor; PevN, periventricular nucleus; ArcN, arcuate nucleus; PG, pituitary gland.


Figure 4. Hypothalamic control—neuromodulators. The control of GH release from somatostatin and GHRH‐expressing neurons is mediated through interactions with hypothalamic neuromodulators. In this instance, dopamine (DA) and adrenaline [acting through selective activation of the α1‐receptor subtype (α1‐R)] stimulates somatostatin‐neuronal activity, thereby inhibiting GH release. Adrenaline [acting through selective activation of the α2‐receptor subtype (α2‐R)], serotonin (5‐HT), and acetylcholine (Ach) stimulate GH release, through inhibition of somatostatin‐expressing neurons. By comparison, activation of GHRH‐expressing neuronal activity by adrenaline (acting through selective activation of the α2‐R) and 5‐HT results in increased GH output. In turn, acting through select activation of the β2‐receptor subtype (β2‐R), adrenaline inhibits GH release by inhibiting GHRH‐neuronal activity. Stimulatory interactions are highlighted in green arrows. Inhibitory interactions are highlighted in orange arrows. Additional abbreviations: ME, median eminence.


Figure 5. Intrahypothalamic interactions—neuropeptides. Complex intrahypothalamic interactions control the activity of somatostatin‐expressing and GHRH‐expressing neurons, thereby regulating the pulsatile release of GH. Corticotrophin releasing hormone (CRH)‐expressing neurons within the paraventricular nucleus (PvN) stimulate somatostatin activity, thereby inhibiting GH release. This is modulated through activation of CRH‐expressing neurons by neuropeptide‐Y (NPY)‐expressing neurons within the arcuate nucleus (ArcN), acting through the Y‐1 (Y1‐R) and Y‐2 (Y2‐R) receptor subtypes. CRH activity is further modulated through activation of the melanocortin receptor subtype‐4 (MC4‐R). NPY‐expressing neurons further inhibit GH release through activation of somatostatin‐expressing neurons. Of interest, NPY‐expressing neurons may indirectly promote the release of GH through the activation of pro‐opiomelanocortin (POMC)‐expressing neurons, which inhibits somatostatin‐expressing neuronal activity. This control of GH release is further modulated through the stimulation of NPY‐expressing neurons by somatostatin (within the ArcN), and through activation of GHRH expressing neurons by low levels of somatostatin. Stimulatory interactions are highlighted in green arrows. Inhibitory interactions are highlighted in orange arrows. Additional abbreviations: ME, median eminence; SST1, somatostatin receptor subtype‐1, SST2, somatostatin receptor subtype‐2; SST3, somatostatin receptor subtype‐3; SST5, somatostatin receptor subtype‐5; Y1‐R, Neuropeptide‐Y specific receptor subtype‐1; Y2‐R, neuropeptide‐Y specific receptor subtype‐2; GAL‐R1, galanin receptor subtype‐1; GAL‐R2, galanin receptor subtype‐2; MC3R, melanocortin receptor subtype‐3.


Figure 6. Ghrelin acts within the hypothalamus and the anterior pituitary gland indirectly (through inhibiting somatostatin‐ and stimulating GHRH‐neuronal activity), and directly by stimulating somatotrophs, respectively. The actions of ghrelin are mediated through select activation of the GHS‐R. Actions of ghrelin on GH release may involve interactions with feeding circuits, specifically through neuropeptide‐Y (NPY)‐expressing neurons located within the arcuate nucleus (ArcN). Stimulatory interactions are highlighted in green arrows. Inhibitory interactions are highlighted in orange arrows. Additional abbreviations: ME, median eminence; PevN, periventricular nucleus; PvN, paraventricular nucleus; POMC, pro‐opiomelanocortin; GAL, galanin.


Figure 7. Differential GH secretory patterns between males and females. Mechanisms that promote GH output in adulthood are established during pubertal maturation. For males, this results in the establishment of adult‐specific GH release by 18 to 25 years of age, and the progressive decline in peak and total GH release with age. Differential patterns and amounts of GH release between males and females occur as a consequence of altered feedback to the hypothalamus and anterior pituitary gland, predominantly in response to circulating levels of estrogen. Increased circulating levels of estrogen are associated with an overall rise in peak amplitude, pulse frequency, and total GH release in females when compared to males. A further rise in peak and total GH release in females is observed during the follicular stage of the ovarian cycle, the period characterized by a rise in circulating levels of estrogen (peaking prior to ovulation). Feedback from placental‐derived GH to the anterior pituitary gland contributes to the suppression of maternal GH release during pregnancy. Resumption of maternal GH output following birth is critical for sustained milk production through prevention of involution of mammary gland tissue. Acting through direct mechanisms, or indirectly through insulin‐like growth factor‐1 (IGF‐1), GH is thought to further promote the transport of nutrients to maternal milk.
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Frederik J. Steyn, Virginie Tolle, Chen Chen, Jacques Epelbaum. Neuroendocrine Regulation of Growth Hormone Secretion. Compr Physiol 2016, 6: 687-735. doi: 10.1002/cphy.c150002