Estrogen differentially modulates the cannabinoid- induced presynaptic inhibition of amino acid neurotransmission in proopiomelanocortin neurons of the arcuate nucleus

Neuroendocrinology

Volumn 84, Issue 2, 2007, Pages 123-137

  Nguyen, Que Huong ^a   Wagner, Edward J ^a,b  

^a Western University of Health Sciences   (United States)

^b WESTERN UNIVERSITY OF HEALTH SCIENCES   (United States)

Author keywords

Aminobutyric acid; CB1 receptor; Electrophysiology; Estrogen; Glutamate; Proopiomelanocortin

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; AMINO ACID; CANNABINOID; CANNABINOID 1 RECEPTOR; CANNABINOID RECEPTOR AFFECTING AGENT; ESTRADIOL BENZOATE; ESTROGEN; IONOTROPIC RECEPTOR ANTAGONIST; PROOPIOMELANOCORTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; ELECTROSTIMULATION; ENDOCRINE FUNCTION; ESTROGEN ACTIVITY; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; GABAERGIC TRANSMISSION; GUINEA PIG; HORMONAL REGULATION; HYPOTHALAMUS; INHIBITORY POSTSYNAPTIC POTENTIAL; NEUROTRANSMISSION; NONHUMAN; OVARIECTOMY; PATCH CLAMP; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL;

ANIMALS; ARCUATE NUCLEUS; ELECTRIC STIMULATION; ESTRADIOL; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GUINEA PIGS; NEURAL INHIBITION; NEURONS; PATCH-CLAMP TECHNIQUES; PIPERIDINES; PRESYNAPTIC TERMINALS; PRO-OPIOMELANOCORTIN; PYRAZOLES; RECEPTOR, CANNABINOID, CB1; RECEPTORS, GABA-A; RECEPTORS, GLUTAMATE; STATISTICS, NONPARAMETRIC;

EID: 33846417285     PISSN: 00283835     EISSN: None     Source Type: Journal    
DOI: 10.1159/000096996     Document Type: Article

References (62)

1. Murphy LL, Muñoz RM, Adrian BA, Villanúa MA: Function of cannabinoid receptors in the neuroendocrine regulation of hormone secretion. Neurobiol Dis 1998;5:432-446.
2. Horvath TL: Endocannabinoids and the regulation of body fat: the smoke is clearing. J Clin Invest 2003;113:323-326.
3. 9-tetrahydrocannabinol produces a differential time related responsiveness on proenkephalin, proopiomelanocortin and corticotropin releasing factor gene expression in the hypothalamus and pituitary gland of the rat. Neuropharmacology 1999;38:433-439.
4. Corchero J, Fuentes JA, Manzanares J: Chronic treatment with CP-55,940 regulates corticotropin releasing factor and proopiomelanocortin gene expression in the hypothalamus and pituitary gland of the rat. Life Sci 1999;64:905-911.
5. Di S, Malcher-Lopes R, Halmos KC, Tasker JG: Nongenomic glucocorticoid inhibition via endocannabinoid release in the hypothalamus: a fast feedback mechanism. J Neurosci 2003;23:4850-4857.
6. Cota D, Marsicano G, Tschöp M, Grübler Y, Flachskamm C, Schubert M, Auer D, Yassouridis A, Thöne-Reineke C, Ortmann S, Tomassoni F, Cervino C, Nisoli E, Linthhorst ACE, Pasquali R, Lutz B, Stalla GK, Pagotto U: The endogenous cannabinoid system affects energy balance via central orexigenic drive and peripheral lipogenesis. J Clin Invest 2003;112:423-431.
7. Di Marzo V, Goparahu SK, Wang L, Liu J, Bátkai S, Járai Z, Fezza F, Miura GI, Palmiter RD, Sugiura T, Kunos G: Leptin-regulated endocannabinoids are involved in maintaining food intake. Nature 2001;410:822-825.
8. Hildebrandt AL, Kelly-Sullivan DM, Black SC: Antiobesity effects of chronic CB1 receptor antagonist treatment in diet-induced obese mice. Eur J Pharmacol 2003;462:125-132.
9. Akesson TR, Micevych PE: Endogenous opioid-immunoreactive neurons of the ventromedial hypothalamic nucleus concentrate estrogen in male and female rats. J Neurosci Res 1991;28:359-366.
10. Morrell JI, McGinty JF, Pfaff DW: A subset of β-endorphin- or dynorphin-containing neurons in the medial basal hypothalamus accumulates estradiol. Neuroendocrinology 1985;41:417-426.
11. Cheung S, Hammer RP: Gonadal steroid hormone regulation of proopiomelanocortin gene expression in arcuate neurons that innervate the medial preoptic area of the rat. Neuroendocrinology 1995;62:283-292.
12. Thornton JE, Loose MD, Kelly MJ, Rönnekleiv OK: Effects of estrogen on the number of neurons expressing β-endorphin in the medial basal hypothalamus of the female guinea pig. J Comp Neurol 1994;341:68-77.
13. Diano S, Naftolin F, Horvath TL: Gonadal steroids target AMPA glutamate receptor-containing neurons in the rat hypothalamus, septum and amygdala: a morphological and biochemical study. Endocrinology 1997;138:778-789.
14. Wagner EJ, Moore KE, Lookingland KJ: Sexual differences in N-methyl-D-aspartate receptor-mediated regulation of tuberoinfundibular dopaminergic neurons in the rat. Brain Res 1993;611:139-146.
15. Wagner EJ, Manzanares J, Moore KE, Lookingland KJ: Neurochemical evidence that estrogen-induced suppression of kappa-opioid-receptor-mediated regulation of tuberoinfundibular dopaminergic neurons is prolactin-independent. Neuroendocrinology 1994;59:197-201.
16. B-mediated hyperpolarization of hypothalamic arcuate neurons. J Neurosci 1992;12:2745-2750.
17. Lagrange AH, Ronnekleiv OK, Kelly MJ: The potency of μ-opioid hyperpolarization of hypothalamic arcuate neurons is rapidly attenuated by 17β-estradiol. J Neurosci 1994;14:6196-6204.
18. + channel activity in hypothalamic neurons involved in the control of the reproductive axis. Steroids 2002;67:447-456.
19. Sinchak K, Micevych PE: Progesterone blockade of estrogen activation of μ-opioid receptors regulates reproductive behavior. J Neurosci 2001;21:5723-5729.
20. 9-tetrahydrocannabinol in the hypothalamus of the rat. Neuroendocrinology 2001;74:185-192.
21. Mackie K, Lai Y, Westenbroek R, Mitchell R: Cannabinoids activate an inwardly rectifying potassium conductance and inhibit Q-type calcium currents in AtT20 cells transfected with rat brain cannabinoid receptor. J Neurosci 1995;15:6552-6561.
22. Garcia DE, Brown S, Hille B, Mackie K: Protein kinase C disrupts cannabinoid actions by phosphorylation of the CB1 cannabinoid receptor. J Neurosci 1998;18:2834-2841.
23. Henry DJ, Chavkin C: Activation of inwardly rectifying potassium channels (GIRK1) by co-expressed rat brain cannabinoid receptors in Xenopus oocytes. Neurosci Lett 1995;186:91-94.
24. McAllister SD, Griffin G, Satin LS, Abood ME: Cannabinoid receptors can activate and inhibit G protein-coupled inwardly rectifying potassium channels in a Xenopus oocyte expression system. J Pharmacol Exp Ther 1999;291:618-626.
25. Deadwyler SA, Hampson RE, Mu J, Whyte A, Childers S: Cannabinoids modulate voltage sensitive potassium A-current in hippocampal neurons via a cAMP-dependent process. J Pharmacol Exp Ther 1995;273:734-743.
26. Mu J, Zhuang S-Y, Kirby MT, Hampson RE, Deadwyler SA: Cannabinoid receptors differentially modulate potassium A and D currents in hippocampal neurons in culture. J Pharmacol Exp Ther 1999;291:893-902.
27. + current in neurons of the mammalian hypothalamus. J Neurophysiol 2005;94:2983-2986.
28. Khasabova IA, Harding-Rose C, Simone DA, Seybold VS: Differential effects of CB1 and opioid agonists on two populations of adult rat dorsal root ganglion neurons. J Neurosci 2004;24:1744-1753.
29. Caulfield MP, Brown DA: Cannabinoid receptor agonists inhibit Ca current in NG108-15 neuroblastoma cells via a pertussis toxin-sensitive mechanism. Br J Pharmacol 1992;106:231-232.
30. Ho BY, Stadnicka A, Prather PL, Buckley AR, Current LL, Bosnjak ZJ, Kwok WM: Cannabinoid CB1 receptor-mediated inhibition of prolactin release and signaling mechanisms in GH4C1 cells. Endocrinology 2000;141:1675-1685.
31. Auclair N, Otani S, Soubrie P, Crepel F: Cannabinoids modulate synaptic strength and plasticity at glutamatergic synapses of rat prefrontal cortex pyramidal neurons. J Neurophysiol 2000;83:3287-3293.
32. Shen MX, Piser TM, Seybold VS, Thayer SA: Cannabinoid receptor agonists inhibit glutamatergic synaptic transmission in rat hippocampal cultures. J Neurosci 1996;16:4322-4334.
33. Straiker AJ, Borden CR, Sullivan JM: G-protein α subunit isoforms couple differentially to receptors that mediate presynaptic inhibition at rat hippocampal synapses. J Neurosci 2002;22:2460-2468.
34. Vaughan CW, Connor M, Bagley EE, Christie MJ: Actions of cannabinoids on membrane properties and synaptic transmission in rat periaqueductal gray neurons in vitro. Mol Pharmacol 2000;57:288-295.
35. Derbenev AV, Stuart TC, Smith BN: Cannabinoids suppress synaptic input to neurones of the rat dorsal motor nucleus of the vagus nerve. J Physiol 2004;559:923-938.
36. Tsou K, Mackie K, Sañudo-Peña MC, Walker JM: Cannabinoid CB1 receptors are localized primarily on cholecystokinin-containing GABAergic interneurons in the rat hippocampal formation. Neuroscience 1999;93:969-975.
37. Katona I, Sperlágh B, Sík A, Käfalvi A, Vizi ES, Mackie K, Freund TF: Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J Neurosci 1999;19:4544-4558.
38. Hoffman AF, Lupica CR: Direct actions of cannabinoids on synaptic transmission in the nucleus accumbens: a comparison with opioids. J Neurophysiol 2001;85:72-83.
39. Khachaturian H, Lewis ME, Shafer MKH, Watson SJ: Anatomy of the CNS opioid systems. Trends Neurosci 1985;8:111-119.
40. Naftolin F, Leranth C, Horvath TL, Garcia-Segura LM: Potential neuronal mechanisms of estrogen actions in synaptogenesis and synaptic plasticity. Cell Mol Neurobiol 1996;16:213-223.
41. Yang ZY, Copolov DL, Lim AT: Glutamate enhances the adenylyl cyclase-cAMP system-induced beta-endorphin secretion and POMC mRNA expression in rat hypothalamic neurons in culture: NMDA receptor-mediated modulation. Brain Res 1995;692:129-136.
42. Hentges ST, Nishiyama M, Overstreet LS, Stenzel-Poore M, Williams JT, Low MJ: GABA release from proopiomelanocortin neurons. J Neurosci 2004;24:1578-1583.
43. Hentges ST, Low MJ, Williams JT: Differential regulation of synaptic inputs by constitutively released endocannabinoids and exogenous cannabinoids. J Neurosci 2005;25:9746-9751.
44. Condon TP, Dykshoorn-Bosch MA, Kelly MJ: Episodic luteinizing-hormone release in the ovariectomized female guinea pig: rapid inhibition by estrogen. Biol Reprod 1988;38:121-126.
45. Qiu J, Bosch MA, Tobias SC, Grandy DK, Scanlan TS, Rønnekleiv OK, Kelly MJ: Rapid signaling of estrogen in hypothalamic neurons involves a novel G-protein-coupled estrogen receptor that activates protein kinase C. J Neurosci 2003;23:9529-9540.
46. Adams IB, Martin BR: Cannabis: pharmacology and toxicology in animals and humans. Addiction 1996;91:1585-1614.
47. Hillard CJ, Manna S, Greenberg MJ, Dicamelli R, Ross RA, Stevenson LA, Murphy V, Pertwee RG, Campbell WB: Synthesis and characterization of potent and selective agonists of the neuronal cannabinoid receptor (CB1). J Pharmacol Exp Ther 1999;289:1427-1433.
48. Ronnekleiv OK, Loose MD, Erickson KR, Kelly MJ: A method for immunocytochemical identification of biocytin-labeled neurons following intracellular recording. Biotechniques 1990;9:432-438.
49. Horvath TL: The hardship of obesity: a soft-wired hypothalamus. Nat Neurosci 2005;8:561-565.
50. Decavel C, van den Pol AN: Converging GABA- and glutamate-immunoreactive axons make synaptic contact with identified hypothalamic neurosecretory neurons. J Comp Neurol 1992;316:104-116.
51. Brann DW, Mahesh VB: Excitatory amino acid neurotransmission: evidence for a role in neuroendocrine regulation. Trends Endocrinol Metab 1992;3:122-126.
52. Appleyard SM, Bailey TW, Doyle MW, Jin YH, Smart JL, Low MJ, Andresen MC: Proopiomelanocortin neurons in nucleus tractus solitarius are activated by visceral afferents: regulation by cholecystokinin and opioids. J Neurosci 2005;25:3578-3585.
53. Decavel C, van den Pol AN: GABA: a dominant neurotransmitter in the hypothalamus. J Comp Neurol 1990;302:1019-1037.
54. Melis M, Perra S, Muntoni AL, Pillolla G, Lutz B, Marsicano G, Di Marzo V, Gessa GL, Pistis M: Prefrontal cortex stimulation induces 2-arachidonoyl-glycerol-mediated suppression of excitation in dopamine neurons. J Neurosci 2004;24:10707-10715.
55. Ohno-Shosaku T, Tsubokawa H, Mizushima I, Yoneda N, Zimmer A, Kano M: Presynaptic cannabinoid sensitivity is a major determinant of depolarization-induced retrograde suppression at hippocampal synapses. J Neurosci 2002;22:3864-3872.
56. Gu Q, Moss RL: 17β-Estradiol potentiates kainate-induced currents via activation of the cAMP cascade. J Neurosci 1996;16:3620-3629.
57. Bocchiaro CM, Saywell SA, Feldman JL: Dynamic modulation of inspiratory drive currents by protein kinase A and protein phosphatases in functionally active motoneurons. J Neurosci 2003;23:1099-1103.
58. Ingram SL, Vaughan CW, Bagley EE, Connor M, Christie MJ: Enhanced opioid efficacy in opioid dependence is caused by an altered signal transduction pathway. J Neurosci 1998;18:10269-10276.
59. Tavalin SJ, Colledge M, Hell JW, Langeberg LK, Huganir RL, Scott JD: Regulation of GluR1 by the A-kinase anchoring protein 79 (AKAP79) signaling complex shares properties with long-term depression. J Neurosci 2002;22:3044-3051.
60. Krishek BJ, Xie X, Blackstone C, Huganir RL, Moss SJ, Smart TG: Regulation of GABA(A) receptor function by protein kinase C phosphorylation. Neuron 1994;12:1081-1095.
61. 9-tetrahydrocannabinol during the follicular phase of the rhesus monkey (Macaca mulatta). J Clin Endocrinol Metab 1981;52:50-55.
62. McCaffrey TA, Czaja JA: Diverse effects of estradiol-17β: concurrent suppression of appetite, blood pressure and vascular reactivity in conscious, unrestrained animals. Physiol Behav 1989;45:649-657.