Glucocorticoids attenuate the central sympathoexcitatory actions of insulin

Journal of Neurophysiology

Volumn 112, Issue 10, 2014, Pages 2597-2604

  Steiner, Jennifer L ^a   Bardgett, Megan E ^a   Wolfgang, Lawrence ^a   Lang, Charles H ^a   Stocker, Sean D ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

Akt; Arcuate nucleus; Dexamethasone; Mtor; Sympathetic nerve activity

Indexed keywords

3 AMINO 2 (3 CARBOXYPROPYL) 6 (4 METHOXYPHENYL)PYRIDAZINIUM BROMIDE; DEXAMETHASONE; GLUCOCORTICOID; INSULIN; PROTEIN KINASE B; PROTEIN S6; 4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; MECHANISTIC TARGET OF RAPAMYCIN COMPLEX 1; MULTIPROTEIN COMPLEX; PYRIDAZINE DERIVATIVE; TARGET OF RAPAMYCIN KINASE;

ADRENERGIC TRANSMISSION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; BRAIN NERVE CELL; CENTRAL SYMPATHOEXCITATORY ACTION; CONTROLLED STUDY; ENZYME ACTIVATION; HYPOTHALAMUS; MALE; NERVE CELL INHIBITION; NERVE STIMULATION; NEUROMODULATION; NONHUMAN; PROTEIN INDUCTION; RAT; SCIATIC NERVE; SENSORY NERVE; SYMPATHETIC BLOCKING; WESTERN BLOTTING; ANIMAL; BLOOD PRESSURE; DRUG EFFECTS; ELECTROSTIMULATION; LUMBAR VERTEBRA; METABOLISM; PHYSIOLOGY; SENSORY NERVE CELL; SPRAGUE DAWLEY RAT;

ANIMALS; ARCUATE NUCLEUS OF HYPOTHALAMUS; BLOOD PRESSURE; DEXAMETHASONE; ELECTRIC STIMULATION; GABA ANTAGONISTS; GLUCOCORTICOIDS; INSULIN; LUMBAR VERTEBRAE; MALE; MULTIPROTEIN COMPLEXES; NEURONS, AFFERENT; PYRIDAZINES; RATS, SPRAGUE-DAWLEY; SCIATIC NERVE; TOR SERINE-THREONINE KINASES;

EID: 84910151414     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00514.2014     Document Type: Article

References (46)

1. Akabayashi A, Watanabe Y, Wahlestedt C, McEwen BS, Paez X, Leibowitz SF. Hypothalamic neuropeptide Y, its gene expression and receptor activity: relation to circulating corticosterone in adrenalectomized rats. Brain Res 665: 201–212, 1994.
2. Anderson EA, Hoffman RP, Balon TW, Sinkey CA, Mark AL. Hyperinsulinemia produces both sympathetic neural activation and vasodilation in normal humans. J Clin Invest 87: 2246–2252, 1991.
3. Aronsson M, Fuxe K, Dong Y, Agnati LF, Okret S, Gustafsson JA. Localization of glucocorticoid receptor mRNA in the male rat brain by in situ hybridization. Proc Natl Acad Sci USA 85: 9331–9335, 1988.
4. Bardgett ME, McCarthy JJ, Stocker SD. Glutamatergic receptor activation in the rostral ventrolateral medulla mediates the sympathoexcitatory response to hyperinsulinemia. Hypertension 55: 284–290, 2010.
5. Baura GD, Foster DM, Kaiyala K, Porte D Jr, Kahn SE, Schwartz MW. Insulin transport from plasma into the central nervous system is inhibited by dexamethasone in dogs. Diabetes 45: 86–90, 1996.
6. Begg DP, Woods SC. The central insulin system and energy balance. Handb Exp Pharmacol 111–129, 2012.
7. Broberger C, Visser TJ, Kuhar MJ, Hokfelt T. Neuropeptide Y innervation and neuropeptide-Y-Y1-receptor-expressing neurons in the paraventricular hypothalamic nucleus of the mouse. Neuroendocrinology 70: 295–305, 1999.
8. Cassaglia PA, Hermes SM, Aicher SA, Brooks VL. Insulin acts in the arcuate nucleus to increase lumbar sympathetic nerve activity and baroreflex function in rats. J Physiol 589: 1643–1662, 2011.
9. Cassaglia PA, Shi Z, Li B, Reis WL, Clute-Reinig NM, Stern JE, Brooks VL. Neuropeptide Y acts in the paraventricular nucleus to suppress sympathetic nerve activity and its baroreflex regulation. J Physiol 592: 1655–1675, 2014.
10. Geer EB, Islam J, Buettner C. Mechanisms of glucocorticoid-induced insulin resistance: focus on adipose tissue function and lipid metabolism. Endocrinol Metab Clin North Am 43: 75–102, 2014.
11. Gudbjornsdottir S, Friberg P, Elam M, Attvall S, Lonnroth P, Wallin BG. The effect of metformin and insulin on sympathetic nerve activity, norepinephrine spillover and blood pressure in obese, insulin resistant, normoglycemic, hypertensive men. Blood Press 3: 394–403, 1994.
12. Harlan SM, Guo DF, Morgan DA, Fernandes-Santos C, Rahmouni K. Hypothalamic mTORC1 signaling controls sympathetic nerve activity and arterial pressure and mediates leptin effects. Cell Metab 17: 599–606, 2013.
13. Hill JW, Williams KW, Ye C, Luo J, Balthasar N, Coppari R, Cowley MA, Cantley LC, Lowell BB, Elmquist JK. Acute effects of leptin require PI3K signaling in hypothalamic proopiomelanocortin neurons in mice. J Clin Invest 118: 1796–1805, 2008.
14. Inoki K, Li Y, Zhu T, Wu J, Guan KL. TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat Cell Biol 4: 648–657, 2002.
15. Kalsbeek A, Bruinstroop E, Yi CX, Klieverik LP, La Fleur SE, Fliers E. Hypothalamic control of energy metabolism via the autonomic nervous system. Ann NY Acad Sci 1212: 114–129, 2010.
16. Kawabe T, Kawabe K, Sapru HN. Cardiovascular responses to chemical stimulation of the hypothalamic arcuate nucleus in the rat: role of the hypothalamic paraventricular nucleus. PLoS One 7: e45180, 2012.
17. Luckett BS, Frielle JL, Wolfgang L, Stocker SD. Arcuate nucleus injection of an anti-insulin affibody prevents the sympathetic response to insulin. Am J Physiol Heart Circ Physiol 304: H1538–H1546, 2013.
18. Marks JL, Porte D Jr, Stahl WL, Baskin DG. Localization of insulin receptor mRNA in rat brain by in situ hybridization. Endocrinology 127: 3234–3236, 1990.
19. McEwen BS, De Kloet ER, Rostene W. Adrenal steroid receptors and actions in the nervous system. Physiol Rev 66: 1121–1188, 1986.
20. Morgan DA, Balon TW, Ginsberg BH, Mark AL. Nonuniform regional sympathetic nerve responses to hyperinsulinemia in rats. Am J Physiol Regul Integr Comp Physiol 264: R423–R427, 1993.
21. Morgan DA, Rahmouni K. Differential effects of insulin on sympathetic nerve activity in agouti obese mice. J Hypertens 28: 1913–1919, 2010.
22. Mori H, Inoki K, Munzberg H, Opland D, Faouzi M, Villanueva EC, Ikenoue T, Kwiatkowski D, MacDougald OA, Myers MG Jr, Guan KL. Critical role for hypothalamic mTOR activity in energy balance. Cell Metab 9: 362–374, 2009.
23. Morimoto M, Morita N, Ozawa H, Yokoyama K, Kawata M. Distribution of glucocorticoid receptor immunoreactivity and mRNA in the rat brain: an immunohistochemical and in situ hybridization study. Neurosci Res 26: 235–269, 1996.
24. Muntzel M, Beltz T, Mark AL, Johnson AK. Anteroventral third ventricle lesions abolish lumbar sympathetic responses to insulin. Hypertension 23: 1059–1062, 1994a.
25. Muntzel MS, Morgan DA, Mark AL, Johnson AK. Intracerebroventricular insulin produces nonuniform regional increases in sympathetic nerve activity. Am J Physiol Regul Integr Comp Physiol 267: R1350–R1355, 1994b.
26. Niswender KD, Morrison CD, Clegg DJ, Olson R, Baskin DG, Myers MG Jr, Seeley RJ, Schwartz MW. Insulin activation of phosphatidylinositol 3-kinase in the hypothalamic arcuate nucleus: a key mediator of insulininduced anorexia. Diabetes 52: 227–231, 2003.
27. Norman AW, Mizwicki MT, Norman DP. Steroid-hormone rapid actions, membrane receptors and a conformational ensemble model. Nat Rev Drug Discov 3: 27–41, 2004.
28. Obici S, Feng Z, Karkanias G, Baskin DG, Rossetti L. Decreasing hypothalamic insulin receptors causes hyperphagia and insulin resistance in rats. Nat Neurosci 5: 566–572, 2002.
29. Peterson RT, Beal PA, Comb MJ, Schreiber SL. FKBP12-rapamycinassociated protein (FRAP) autophosphorylates at serine 2481 under translationally repressive conditions. J Biol Chem 275: 7416–7423, 2000.
30. Pricher MP, Freeman KL, Brooks VL. Insulin in the brain increases gain of baroreflex control of heart rate and lumbar sympathetic nerve activity. Hypertension 51: 514–520, 2008.
31. Qiu J, Zhang C, Borgquist A, Nestor CC, Smith AW, Bosch MA, Ku S, Wagner EJ, Ronnekleiv OK, Kelly MJ. Insulin excites anorexigenic proopiomelanocortin neurons via activation of canonical transient receptor potential channels. Cell Metab 19: 682–693, 2014.
32. Rahmouni K, Haynes WG, Morgan DA, Mark AL. Role of melanocortin-4 receptors in mediating renal sympathoactivation to leptin and insulin. J Neurosci 23: 5998–6004, 2003.
33. Rahmouni K, Morgan DA, Morgan GM, Liu X, Sigmund CD, Mark AL, Haynes WG. Hypothalamic PI3K and MAPK differentially mediate regional sympathetic activation to insulin. J Clin Invest 114: 652–658, 2004.
34. Ruzzin J, Wagman AS, Jensen J. Glucocorticoid-induced insulin resistance in skeletal muscles: defects in insulin signalling and the effects of a selective glycogen synthase kinase-3 inhibitor. Diabetologia 48: 2119–2130, 2005.
35. Sancak Y, Thoreen CC, Peterson TR, Lindquist RA, Kang SA, Spooner E, Carr SA, Sabatini DM. PRAS40 is an insulin-regulated inhibitor of the mTORC1 protein kinase. Mol Cell 25: 903–915, 2007.
36. Scherrer U, Vollenweider P, Randin D, Jequier E, Nicod P, Tappy L. Suppression of insulin-induced sympathetic activation and vasodilation by dexamethasone in humans. Circulation 88: 388–394, 1993.
37. Shah OJ, Anthony JC, Kimball SR, Jefferson LS. Glucocorticoids oppose translational control by leucine in skeletal muscle. Am J Physiol Endocrinol Metab 279: E1185–E1190, 2000.
38. Shimizu H, Arima H, Ozawa Y, Watanabe M, Banno R, Sugimura Y, Ozaki N, Nagasaki H, Oiso Y. Glucocorticoids increase NPY gene expression in the arcuate nucleus by inhibiting mTOR signaling in rat hypothalamic organotypic cultures. Peptides 31: 145–149, 2010.
39. Simmonds SS, Lay J, Stocker SD. Dietary salt intake exaggerates sympathetic reflexes and increases blood pressure variability in normotensive rats. Hypertension 64: 583–589, 2014.
40. Soliman GA, Acosta-Jaquez HA, Dunlop EA, Ekim B, Maj NE, Tee AR, Fingar DC. mTOR Ser-2481 autophosphorylation monitors mTORC-specific catalytic activity and clarifies rapamycin mechanism of action. J Biol Chem 285: 7866–7879, 2010.
41. Stocker SD, Smith CA, Kimbrough CM, Stricker EM, Sved AF. Elevated dietary salt suppresses renin secretion but not thirst evoked by arterial hypotension in rats. Am J Physiol Regul Integr Comp Physiol 284: R1521–R1528, 2003.
42. Ward KR, Bardgett JF, Wolfgang L, Stocker SD. Sympathetic response to insulin is mediated by melanocortin 3/4 receptors in the hypothalamic paraventricular nucleus. Hypertension 57: 435–441, 2011.
43. Werther GA, Hogg A, Oldfield BJ, McKinley MJ, Figdor R, Allen AM, Mendelsohn FA. Localization and characterization of insulin receptors in rat brain and pituitary gland using in vitro autoradiography and computerized densitometry. Endocrinology 121: 1562–1570, 1987.
44. Williams KW, Margatho LO, Lee CE, Choi M, Lee S, Scott MM, Elias CF, Elmquist JK. Segregation of acute leptin and insulin effects in distinct populations of arcuate proopiomelanocortin neurons. J Neurosci 30: 2472–2479, 2010.
45. Yi CX, Foppen E, Abplanalp W, Gao Y, Alkemade A, la Fleur SE, Serlie MJ, Fliers E, Buijs RM, Tschop MH, Kalsbeek A. Glucocorticoid signaling in the arcuate nucleus modulates hepatic insulin sensitivity. Diabetes 61: 339–345, 2012.
46. Young CN, Deo SH, Chaudhary K, Thyfault JP, Fadel PJ. Insulin enhances the gain of arterial baroreflex control of muscle sympathetic nerve activity in humans. J Physiol 588: 3593–3603, 2010.