Role of dorsal vagal complex A2 noradrenergic neurons in hindbrain glucoprivic inhibition of the luteinizing hormone surge in the steroid-primed ovariectomized female rat: Effects of 5-thioglucose on A2 functional biomarker and AMPK activity

Neuroscience

Volumn 269, Issue , 2014, Pages 199-214

  Ibrahim, B A ^a   Briski, K P ^a  

^a UNIVERSITY OF LOUISIANA AT MONROE   (United States)

Author keywords

5 thioglucose; A2 noradrenergic neurons; AMPK; Estrogen receptor; Gonadotropin releasing hormone

Indexed keywords

ADENYLATE KINASE; ALPHA 2 ADRENERGIC RECEPTOR; DOPAMINE BETA MONOOXYGENASE; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; GLUCOSE TRANSPORTER 3; LUTEINIZING HORMONE; PROGESTERONE; PROTEIN FOS; THIOGLUCOSE; 5-THIO-D-GLUCOSE; ADENOSINE A2 RECEPTOR; ADRENERGIC RECEPTOR STIMULATING AGENT; ALPHA 1 ADRENERGIC RECEPTOR STIMULATING AGENT; BIOLOGICAL MARKER; CENTRAL NERVOUS SYSTEM AGENTS; ESTRADIOL; GLUCOSE; GONADORELIN; HORMONE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; METHOXAMINE; OXIDOPAMINE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; BRAIN NERVE CELL; CELL ACTIVITY; CELL STIMULATION; CONTROLLED STUDY; DISORDERS OF CARBOHYDRATE METABOLISM; DOWN REGULATION; ENZYME ACTIVATION; FEEDBACK SYSTEM; FEMALE; FUNCTIONAL ASSESSMENT; GLUCOPENIA; GLYCOLYSIS; HORMONE INHIBITION; LASER MICRODISSECTION; MOLECULAR DYNAMICS; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; RHOMBENCEPHALON; SEX HORMONE DETERMINATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ADRENERGIC NERVE CELL; ANALOGS AND DERIVATIVES; ANIMAL; DRUG EFFECTS; METABOLISM; NERVE CELL; OVARIECTOMY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ADRENERGIC AGENTS; ADRENERGIC ALPHA-1 RECEPTOR AGONISTS; ADRENERGIC NEURONS; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; BIOLOGICAL MARKERS; CENTRAL NERVOUS SYSTEM AGENTS; ESTRADIOL; FEMALE; GLUCOSE; GONADOTROPIN-RELEASING HORMONE; HORMONES; LUTEINIZING HORMONE; METHOXAMINE; NEURONS; OVARIECTOMY; OXIDOPAMINE; PROGESTERONE; RATS, SPRAGUE-DAWLEY; RECEPTORS, ADENOSINE A2; RHOMBENCEPHALON;

EID: 84898818352     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2014.02.015     Document Type: Article

References (56)

1. Barraclough C.A., Wise P.M. The role of catecholamines in the regulation of pituitary luteinizing hormone and follicle stimulating hormone secretion. Endocr Rev 1982, 3:91-119.
2. Briski K.P., Sylvester P.W. Effects of specific acute stressors on LH release in ovariectomized and ovariectomized estrogen-treated female rats. Neuroendocrinology 1988, 47:194-202.
3. Briski K.P., Vogel K.L. (Role of endogenous opioid peptides in central glucocorticoid receptor (GR)-induced decreases in circulating LH. Neuropeptides 1995, 28:175-181.
4. Briski K.P., Sylvester P.W. (Effects of the glucose antimetabolite, 2-deoxy-d-glucose (2-DG), on the LH surge and Fos expression by preoptic GnRH neurons in ovariectomized, steroid-primed rats. J Neuroendocrinol 1998, 10:769-776.
5. Briski K.P., Marshall E.S. (Caudal brainstem Fos expression is restricted to periventricular catecholaminergic loci following intraventricular administration of 2-deoxy-d-glucose. Exp Brain Res 2000, 133:547-551.
6. Briski K.P., Marshall E.S., Sylvester P.W. (Effects of estradiol on glucoprivic transactivation of catecholaminergic neurons in the female rat caudal brainstem. Neuroendocrinology 2001, 73(6):369-377.
7. Briski K.P., Kale A.Y., Vavaiya K.V. (Impact of recurring insulin-induced hypo-glycemia on corticotropin-releasing hormone, oxytocin, vasopressin, and glucokinase gene expression in hypothalamic paraventricular nucleus: role of type II glucocorticoid receptors. Exp Brain Res 2009, 195:499-507.
8. Briski K.P. Induction of cFos expression in hypothalamic dopaminergic neurons by the glucose antimetabolite, 2-deoxy-d-glucose: site-specific modulation by estradiol. NeuroReport 1997, 9:289-295.
9. Briski K.P., Koshy Cherian A., Genabai N.K., Vavaiya K.V. In situ coexpression of glucose and monocarboxylate transporter mRNAs in metabolic-sensitive dorsal vagal complex catecholaminergic neurons: transcriptional reactivity to insulin-induced hypoglycemia (IIH) and caudal hindbrain glucose or lactate repletion during IIH. Neuroscience 2009, 164:1152-1160.
10. Campbell R.E., Herbison A.E. Definition of brainstem afferents to gonadotropin-releasing hormone neurons in the mouse using conditional viral tract tracing. Endocrinology 2007, 148:5884-5890.
11. Castellano J.M., Roa J., Luque R.M., Diequez C., Aguilar E., Pinilla A., Tena-Sempere M. KiSS-1/kisspeptins and the metabolic control of reproduction: physiologic roles and putative physiopathological implications. Peptides 2009, 30:139-145.
12. Cheng X.B., Wen J.P., Yang J., Yang Y., Ning G., Li X.Y. GnRH secretion is inhibited by adiponectin through activation of AMP-activated protein kinase and extracellular signal-regulated kinase. Endocrine 2011, 39:6-12.
13. Cherian A., Briski K.P. Quantitative real-time RT PCR and high-sensitivity immunoblot analyses of laser-microdissected A2 noradrenergic neurons reveal adaptation of phosphoAMPK, glucokinase, substrate fuel transporter, and dopamine-beta-hydroxylase responses to intermediate insulin-induced hypoglycemia. J Neurosci Res 2011, 89:1114-1124.
14. Cherian A., Briski K.P. A2 noradrenergic nerve cell metabolic transducer and nutrient transporter adaptation to hypoglycemia: impact of estrogen. J Neurosci Res 2012, 90:1347-1358.
15. Christian C.A., Glidewell-Kenney C., Jameson J.L., Moenter S.M. (Classical estrogen receptor alpha signaling mediates negative and positive feedback on gonadotropin-releasing hormone neuron firing. Endocrinology 2008, 149:5328-5334.
16. Crosignani P.G. Nutrition and reproduction in women. The ESHRE Capri workshop. Hum Reprod Update 2006, 12:193-207.
17. Coyral-Castel S., Tosca L., Ferreira G., Jeanpierre E., Rame C., Lomet D., Caraty A., Monget P., Chabrolle C., Dupont J. The effect of AMP-activated kinase activation on gonadotrophin-releasing hormone secretion in GT1-7 cells and its potential role in hypothalamic regulation of the oestrous cyclicity in rats. J Neuroendocrinol 2008, 20:335-346.
18. Curran-Rauhut M.A., Petersen S.L. Oestradiol-dependent and -independent modulation of tyrosine hydroxylase mRNA levels in subpopulations of A1 and A2 neurones with oestrogen receptor (ER)α and ERβ gene expression. J Neuroendocrinol 2003, 15:296-303.
19. Demling J., Fuchs E., Baumert M., Wuttke W. Preoptic catecholamine, GABA, and glutamate release in ovariectomised and ovariectomised estogen-primed rats utilising a push-pull cannula technique. Neuroendocrinology 1985, 41:212-218.
20. Dungan H.M., Gottsch M.L., Zeng H., Gragerov A., Bergmann J.E., Vassilatis D.K., Clifton D.K., Steiner R.A. The role of kisspeptin-GPR54 signaling in the tonic regulation and surge release of gonadotropin-releasing hormone/luteinizing hormone. J Neurosci 2007, 27:12088-12095.
21. Fernandez-Galaz C., Dyer R.G., Herbison A.E. Analysis of brainstem A1 and A2 noradrenergic inputs to the preoptic area using microdialysis in the rat. Brain Res 1994, 636:227-232.
22. Gujar AD, Ibrahim BA, Tamrakar P, Briski KP (2012) Hindbrain nutrient status regulates hypothalamic AMPK activity and metabolic neurotransmitter expression. Soc Neurosci Abst 284.10/UU12, New Orleans, LA, October 13-17, 2012.
23. Haywood S.A., Simonian S.X., van der Beek E.M., Bicknell R.J., Herbison A.E. Fluctuating estrogen and progesterone receptor expression in brainstem norepinephrine neurons through the rat estrous cycle. Endocrinology 1999, 1407:3255-3263.
24. Herbison A.E. Noradrenergic regulation of cyclic GnRH secretion. Rev Reprod 1997, 2:1-6.
25. Honma K., Wuttke W. Norepinephrine and dopamine turnover rates in the medial preoptic area and the mediobasal hypothalamus of the rat brain after various endocrinological manipulations. Endocrinology 1980, 106:1848-1853.
26. Ibrahim B.A., Tamrakar P., Gujar A.D., Koshy Cherian A., Briski K.P. Caudal fourth ventricular AICAR regulates glucose and counterregulatory hormone profiles, dorsal vagal complex metabolo-sensory neuron function, and hypothalamic Fos expression. J Neurosci Res 2013, 91:1226-1238.
27. Irwin R.W., Yao J., Hamilton R.T., Cadenas E., Brinton R.D., Nilsen J. Progesterone and estrogen regulate oxidative metabolism in brain mitochondria. Endocrinology 2008, 149:3167-3175.
28. Jennes L., Jennes M.E., Purvis C., Nees M. c-fos expression in noradrenergic A2 neurons of the rat during the estrous cycle and after steroid hormone treatments. Brain Res 1992, 586:171-175.
29. Kalamatianos T., Grimshaw S.E., Poorun R., Hahn J.D., Coen C.W. Fasting reduces KiSS-1 expression in the anteroventral periventricular nucleus (AVPV): effects of fasting on the expression of KiSS-1 and neuropeptide Y in the AVPV or arcuate nucleus of female rats. J Neuroendocrinol 2008, 20:1089-1097.
30. Kale A.Y., Paranjape S.A., Briski K.P. (Intracerebroventricular administration of the nonsteroidal glucocorticoid receptor antagonist, CP472555, prevents exacerbation of hypo-glycemia during repeated insulin administration. Neuroscience 2006, 140:555-565.
31. Kostanyan A., Nazaryan K. Rat brain glycolysis regulation by estradiol-17 beta. Biochim Biophys Acta 1992, 1133:301-3-301-6.
32. Li A.J., Wang Q., Ritter S. Differential responsiveness of dopamine-beta-hydroxylase gene expression to glucoprivation in different catecholamine cell groups. Endocrinology 2006, 147:3428-3434.
33. Maharjan S., Serova L., Sabban E.L. Transcriptional regulation of tyrosine hydroxylase by estrogen: opposite effects with estrogen receptors alpha and beta and interactions with cyclic AMP. J Neurochem 2005, 93:1502-1514.
34. Messager S., Chatzidaki E.E., Ma D., Hendrick A.G., Zahn D., Dixon J., Thresher R.R., Malinge I., Lomet D., Carlton M.B., Colledge W.H., Caraty A., Aparicio S.A. Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proc Natl Acad Sci 2005, 102:1761-1776.
35. Micevych P., Sinchak K. The neurosteroid progesterone underlies estrogen positive feedback of the LH surge. Front Endocrinol 2011, 10.3389/fendo.2011.00090.
36. Mohankumar P.S., Thyagarajan S., Quadri S.K. Correlations of catecholamine release in the medial preoptic area with proestrous surge. Endocrinology 1994, 135:119-126.
37. Nilsen J., Brinton R.D. Mitochondria as therapeutic targets of estrogen action in the central nervous system. Curr Drug Targets CNS Neurol Disord 2004, 3:297-313.
38. Nilsen J., Irwin R.W., Gallaher T.K., Brinton R.D. Estadiol in vivo regulation of brain mitochondrial proteome. J Neurosci 2007, 27:14069-14077.
39. Ohkura S., Tanaka T., Nagatani S., Bucholtz D.C., Tsukamura H., Maeda K., Foster D.L. Central, but not peripheral, glucose-sensing mechanisms mediate glucoprivic suppression of pulsatile luteinizing hormone secretion in the sheep. Endocrinology 2000, 141:4472-4480.
40. Oomura Y., Yoshimatsu H. Neural network of glucose monitoring system. J Auton Nerv Syst 1984, 10:359-372.
41. Pacák K., Palkovits M. Stressor specificity of central neuroendocrine responses: implications for stress-related disorders. Endocr Rev 2001, 22:502-548.
42. Roland A.V., Moenter S.M. Regulation of gonadotropin-releasing hormone neurons by glucose. Trends Endocrinol Metab 2011, 22:443-449.
43. Ronnett G.V., Ramamurthy S., Kleman A.M., Landree L.E., Aja S. AMPK in the brain: its roles in energy balance and neuroprotection. J Neurochem 2009, 109:17-23.
44. Singh S.R., Briski K.P. Septopreoptic mu opioid receptor mediation of hindbrain gluco-privic inhibition of reproductive neuroendocrine function in the female rat. Endocrinology 2004, 145:5322-5331.
45. Smith J.T., Clifton D.K., Steiner R.A. Regulation of the neuroendocrine reproductive axis by kisspeptin-GPR54 signaling. Reproduction 2006, 131:623-630.
46. Szawka R.E., Poletini M.O., Leite C.M., Bernuci M.P., Kalil B.K., Mendonca L.B.D., Carolino R.O.G., Helena C.V.V., Bertram R., Franci C.R., Anselmo-Franci J.A. Release of norepinephrine in the preoptic area activates anteroventral periventricular nucleus neurons and stimulates the surge of luteinizing hormone. Endocrinology 2013, 154:363-374.
47. Tamrakar P, Ibrahim BA, Briski KP (2012) Estradiol is neuroprotective of hindbrain A2 noradrenergic metabolic sensory neurons during insulin-induced hypoglycemia. Soc Neurosci Abst 903.05/XX6, New Orleans, LA, October 13-17, 2012.
48. Vetrivelan R., Mallick H.N., Kumar V.M. Unmasking of alpha1 adrenoreceptor induced hypnogenic response from medial preoptic area. Physiol Behav 2005, 84:641-650.
49. Vetrivelan R., Mallick H.N., Kumar V.M. Sleep induction and temperature lowering by medial preoptic alpha(1) adrenergic receptors. Physiol Behav 2006, 87:707-713.
50. Wade G.N., Jones J.E. Neuroendocrinology of nutritional infertility. Am J Physiol 2004, 287:R1227-R1296.
51. Wade G.N., Schneider J.E. Metabolic fuels and reproduction in female mammals. Neurosci Biobehav Rev 1992, 16:235-272.
52. van den Buuse M., Versteeg D.H., De Jong W Role of dopamine in the development of spontaneous hypertension. Hypertension 1984, 6:899-905.
53. Wen J.P., Lu W.S., Yang J., Nie A.F., Cheng X.B., Yang Y., Ge Y., Li X.Y., Ning G. Globular adiponectin inhibits GnRH secretion from GT1-7 hypothalamic GnRH neurons by induction of hyperpolarization of membrane potential. Biochem Biophys Res Commun 2008, 371:756-761.
54. Wintermantel T.M., Campbell R.E., Porteous R., Bock D., Gröne H.J., Todman M.G., Korach K.S., Greiner E., Pérez C.A., Schülz G., Herbison A.E. Definition of estrogen receptor pathway critical for estrogen positive feedback to gonadotropin-releasing hormone neurons and fertility. Neuron 2006, 52:271-280.
55. Wright D.E., Jennes L. Origin of noradrenergic projections to GnRH perikarya-containing areas in the medial septum-diagonal band and preoptic area. Brain Res 1993, 621:272-278.
56. Zhang C., Bosch M., Levine J.E., Ronnekleiv O., Kelly M. GnRH neurons express KATP channels that are regulated by estrogen and responsive to glucose and metabolic inhibition. J Neurosci 2007, 27:10153-10164.