Somatostatin triggers rhythmic electrical firing in hypothalamic GHRH neurons

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Osterstock, Guillaume ^a,b   Mitutsova, Violeta ^a,b   Barre, Alexander ^a,b   Granier, Manon ^a,b   Fontanaud, Pierre ^a,b   Chazalon, Marine ^a,b   Carmignac, Danielle ^c   Robinson, Iain C A F ^c   Low, Malcolm J ^d   Plesnila, Nikolaus ^e   Hodson, David J ^f,g,h   Mollard, Patrice ^a,b   Méry, Pierre François ^a,b  

^a INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

^b UNIV MONTPELLIER   (France)

^c NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^e ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^f HAMMERSMITH HOSPITAL   (United Kingdom)

^g UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^h Birmingham Women s Hospital NHS Foundation Trust   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN COUPLED INWARDLY RECTIFYING POTASSIUM CHANNEL; GROWTH HORMONE RELEASING FACTOR; SOMATOSTATIN;

ACTION POTENTIAL; ANIMAL; ANTAGONISTS AND INHIBITORS; FEMALE; HYPOTHALAMUS; KNOCKOUT MOUSE; MALE; METABOLISM; MOUSE; PATCH CLAMP TECHNIQUE; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; FEMALE; G PROTEIN-COUPLED INWARDLY-RECTIFYING POTASSIUM CHANNELS; GROWTH HORMONE-RELEASING HORMONE; HYPOTHALAMUS; MALE; MICE; MICE, KNOCKOUT; PATCH-CLAMP TECHNIQUES; SOMATOSTATIN;

EID: 84969812048     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep24394     Document Type: Article

References (58)

1. Robinson, I. C. A. F. & Hindmarsh, P. C. The growth hormone secretory pattern and structural growth. Handbook of Physiology 5, 329-396 (1999).
2. Stanley, S. et al. Profiling of Glucose-Sensing Neurons Reveals that GHRH Neurons Are Activated by Hypoglycemia. Cell metabolism 18, 596-607 (2013).
3. Adams, J. M. et al. Somatostatin Is Essential for the Sexual Dimorphism of GH Secretion, Corticosteroid-Binding Globulin Production, and Corticosterone Levels in Mice. Endocrinology 156, 1052-1065 (2015).
4. Farhy, L. S., Bowers, C. Y. & Veldhuis, J. D. Model-projected mechanistic bases for sex differences in growth hormone regulation in humans. Am J Physiol Regul Integr Comp Physiol 292, R1577-1593 (2007).
5. Farhy, L. S. & Veldhuis, J. D. Putative GH pulse renewal: periventricular somatostatinergic control of an arcuate-nuclear somatostatin and GH-releasing hormone oscillator. Am J Physiol Regul Integr Comp Physiol 286, R1030-1042 (2004).
6. MacGregor, D. J. & Leng, G. Modelling the hypothalamic control of growth hormone secretion. J Neuroendocrinol 17, 788-803 (2005).
7. Wagner, C., Caplan, S. R. & Tannenbaum, G. S. Interactions of ghrelin signaling pathways with the GH neuroendocrine axis: a new and experimentally tested model. Journal of molecular endocrinology 43, 105-119 (2009).
8. Baccam, N. et al. Dual-level afferent control of growth hormone-releasing hormone (GHRH) neurons in GHRH-green fluorescent protein transgenic mice. J Neurosci 27, 1631-1641 (2007).
9. Osterstock, G. et al. Ghrelin stimulation of growth hormone-releasing hormone neurons is direct in the arcuate nucleus. Plos One 5, e9159 (2010).
10. Bouyer, K. et al. Sexually dimorphic distribution of sst2A somatostatin receptors on growth hormone-releasing hormone neurons in mice. Endocrinology 147, 2670-2674 (2006).
11. Israelian, Z. et al. Multiple defects in counterregulation of hypoglycemia in modestly advanced type 2 diabetes mellitus. Metabolism: clinical and experimental 55, 593-598 (2006).
12. Mangan, S. & Alon, U. Structure and function of the feed-forward loop network motif. Proc Natl Acad Sci USA 100, 11980-11985 (2003).
13. Low, M. J. et al. Somatostatin is required for masculinization of growth hormone-regulated hepatic gene expression but not of somatic growth. The Journal of clinical investigation 107, 1571-1580 (2001).
14. Bonnefont, X. et al. Revealing the large-scale network organization of growth hormone-secreting cells. Proc Natl Acad Sci USA 102, 16880-16885 (2005).
15. Brunner, E., Domhof, S. & Langer, F. Nonparametric analysis of longitudinal data in factorial experiments. (John Wiley & Sons, Inc., 2002).
16. Yang, S. K., Steyn, F. & Chen, C. Influence of membrane ion channel in pituitary somatotrophs by hypothalamic regulators. Cell Calcium 51, 231-239 (2012).
17. Guyon, A. et al. Complex effects of stromal cell-derived factor-1 alpha on melanin-concentrating hormone neuron excitability. Eur J Neurosci 21, 701-710 (2005).
18. Sun, Q. Q., Huguenard, J. R. & Prince, D. A. Somatostatin inhibits thalamic network oscillations in vitro: actions on the GABAergic neurons of the reticular nucleus. J Neurosci 22, 5374-5386 (2002).
19. Mollard, P., Vacher, P., Dufy, B. & Barker, J. L. Somatostatin blocks Ca2+ action potential activity in prolactin-secreting pituitary tumor cells through coordinate actions on K+ and Ca2+ conductances. Endocrinology 123, 721-732 (1988).
20. Giustina, A. & Veldhuis, J. D. Pathophysiology of the neuroregulation of growth hormone secretion in experimental animals and the human. Endocr Rev 19, 717-797 (1998).
21. Lanneau, C. et al. Somatostatin receptor subtypes sst1 and sst2 elicit opposite effects on the response to glutamate of mouse hypothalamic neurones: an electrophysiological and single cell RT-PCR study. Eur J Neurosci 10, 204-212 (1998).
22. Viollet, C. et al. Distinct patterns of expression and physiological effects of sst1 and sst2 receptor subtypes in mouse hypothalamic neurons and astrocytes in culture. J Neurochem 68, 2273-2280 (1997).
23. Hannon, J. P. et al. Drug design at peptide receptors: somatostatin receptor ligands. Journal of molecular neuroscience: MN 18, 15-27 (2002).
24. Lanneau, C. et al. Involvement of the Sst1 somatostatin receptor subtype in the intrahypothalamic neuronal network regulating growth hormone secretion: an in vitro and in vivo antisense study. Endocrinology 141, 967-979 (2000).
25. Stroh, T., van Schouwenburg, M. R., Beaudet, A. & Tannenbaum, G. S. Subcellular dynamics of somatostatin receptor subtype 1 in the rat arcuate nucleus: receptor localization and synaptic connectivity vary in parallel with the ultradian rhythm of growth hormone secretion. J Neurosci 29, 8198-8205 (2009).
26. Lanneau, C. et al. Somatostatin modulation of excitatory synaptic transmission between periventricular and arcuate hypothalamic nuclei in vitro. J Neurophysiol 84, 1464-1474 (2000).
27. Balthasar, N. et al. Growth hormone-releasing hormone (GHRH) neurons in GHRH-enhanced green fluorescent protein transgenic mice: a ventral hypothalamic network. Endocrinology 144, 2728-2740 (2003).
28. Thoss, V. S., Perez, J., Probst, A. & Hoyer, D. Expression of five somatostatin receptor mRNAs in the human brain and pituitary. Naunyn-Schmiedeberg's archives of pharmacology 354, 411-419 (1996).
29. Pfeffer, C. K. et al. Inhibition of inhibition in visual cortex: the logic of connections between molecularly distinct interneurons. Nat Neurosci 16, 1068-1076 (2013).
30. Orosz, G., Moehlis, J. & Murray, R. M. Controlling biological networks by time-delayed signals. Philos Trans A Math Phys Eng Sci 368, 439-454 (2010).
31. Pinto, S. et al. Rapid rewiring of arcuate nucleus feeding circuits by leptin. Science 304, 110-115 (2004).
32. Steyn, F. J. Nutrient Sensing Overrides Somatostatin and Growth Hormone-Releasing Hormone to Control Pulsatile Growth Hormone Release. J Neuroendocrinol 27, 577-587 (2015).
33. Getting, P. A. Emerging principles governing the operation of neural networks. Annu Rev Neurosci 12, 185-204 (1989).
34. Alon, U. Network motifs: theory and experimental approaches. Nat Rev Genet 8, 450-461 (2007).
35. Milo, R. et al. Superfamilies of evolved and designed networks. Science 303, 1538-1542 (2004).
36. Milo, R. et al. Network motifs: simple building blocks of complex networks. Science 298, 824-827 (2002).
37. Sekido, R. & Lovell-Badge, R. Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 453, 930-934 (2008).
38. Shen-Orr, S. S., Milo, R., Mangan, S. & Alon, U. Network motifs in the transcriptional regulation network of Escherichia coli. Nat Genet 31, 64-68 (2002).
39. Song, S. et al. Highly nonrandom features of synaptic connectivity in local cortical circuits. PLoS Biol 3, e68 (2005).
40. Sporns, O. & Kotter, R. Motifs in brain networks. Plos Biol 2, e369 (2004).
41. Jansson, J. O., Eden, S. & Isaksson, O. Sexual dimorphism in the control of growth hormone secretion. Endocr Rev 6, 128-150 (1985).
42. Jansson, J. O. et al. Imprinting of growth hormone secretion, body growth, and hepatic steroid metabolism by neonatal testosterone. Endocrinology 117, 1881-1889 (1985).
43. Mode, A. et al. Association between plasma level of growth hormone and sex differentiation of hepatic steroid metabolism in the rat. Endocrinology 111, 1692-1697 (1982).
44. Mode, A., Norstedt, G., Eneroth, P. & Gustafsson, J. A. Purification of liver feminizing factor from rat pituitaries and demonstration of its identity with growth hormone. Endocrinology 113, 1250-1260 (1983).
45. Feifel, D. & Vaccarino, F. J. Growth hormone-regulatory peptides (GHRH and somatostatin) and feeding: a model for the integration of central and peripheral function. Neuroscience and biobehavioral reviews 18, 421-433 (1994).
46. Okada, K. et al. Intracerebroventricular administration of the growth hormone-releasing peptide KP-102 increases food intake in free-feeding rats. Endocrinology 137, 5155-5158 (1996).
47. Bartanusz, V. et al. Local gamma-aminobutyric acid and glutamate circuit control of hypophyseotrophic corticotropin-releasing factor neuron activity in the paraventricular nucleus of the hypothalamus. Eur J Neurosci 19, 777-782 (2004).
48. Herman, J. P., Tasker, J. G., Ziegler, D. R. & Cullinan, W. E. Local circuit regulation of paraventricular nucleus stress integration: glutamate-GABA connections. Pharmacol Biochem Behav 71, 457-468 (2002).
49. Hrabovszky, E. & Liposits, Z. Novel aspects of glutamatergic signalling in the neuroendocrine system. J Neuroendocrinol 20, 743-751 (2008).
50. Hrabovszky, E. et al. Glutamatergic and GABAergic innervation of human gonadotropin-releasing hormone-I neurons. Endocrinology 153, 2766-2776 (2012).
51. Maeda, K. et al. Neurobiological mechanisms underlying GnRH pulse generation by the hypothalamus. Brain Res 1364, 103-115 (2010).
52. Mercer, A. J., Hentges, S. T., Meshul, C. K. & Low, M. J. Unraveling the central proopiomelanocortin neural circuits. Frontiers in neuroscience 7, 19 (2013).
53. Doslikova, B. et al. 5-HT2C receptor agonist anorectic efficacy potentiated by 5-HT1B receptor agonist coapplication: an effect mediated via increased proportion of pro-opiomelanocortin neurons activated. J Neurosci 33, 9800-9804 (2013).
54. Caplan, S. R., Tannenbaum, G. S. & Johnstone, R. M. An enzymatic model of the growth hormone-releasing hormone oscillator incorporating neuronal synchronization. J Theor Biol 264, 984-989 (2010).
55. Edelman, G. M. & Gally, J. A. Degeneracy and complexity in biological systems. Proc Natl Acad Sci USA 98, 13763-13768 (2001).
56. Marder, E. & Taylor, A. L. Multiple models to capture the variability in biological neurons and networks. Nat Neurosci 14, 133-138 (2011).
57. Herbison, A. E. et al. Gonadotropin-releasing hormone neuron requirements for puberty, ovulation, and fertility. Endocrinology 149, 597-604 (2008).
58. Mayer, C. & Boehm, U. Female reproductive maturation in the absence of kisspeptin/GPR54 signaling. Nat Neurosci 14, 704-710 (2011).