Leptin differentially increases sympathetic nerve activity and its baroreflex regulation in female rats: Role of oestrogen

Journal of Physiology

Volumn 593, Issue 7, 2015, Pages 1633-1647

  Shi, Zhigang ^a   Brooks, Virginia L ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERMEDIN; ESTROGEN; LEPTIN; MELANOCORTIN 3 RECEPTOR; MELANOCORTIN 4 RECEPTOR; N ACETYL ALPHA INTERMEDIN[4-10]CYCLO[4 NORLEUCINE 5 ASPARTIC ACID 7 [3 (2 NAPHTHYL)ALANINE] 10 LYSINAMIDE]; ESTRADIOL; INSULIN; INTERMEDIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIESTRUS; FEMALE; HEART RATE; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; MALE; MEAN ARTERIAL PRESSURE; NONHUMAN; OVARIECTOMY; PRESSORECEPTOR REFLEX; PRIORITY JOURNAL; PROESTRUS; RAT; SEX DIFFERENCE; SYMPATHETIC TONE; ANIMAL; ANTAGONISTS AND INHIBITORS; BLOOD; DRUG EFFECTS; ESTRUS CYCLE; INNERVATION; KIDNEY; LUMBOSACRAL REGION; PHYSIOLOGY; SPLANCHNIC NERVE; SPRAGUE DAWLEY RAT;

ANIMALS; BAROREFLEX; ESTRADIOL; ESTROGENS; ESTROUS CYCLE; FEMALE; INSULIN; KIDNEY; LEPTIN; LUMBOSACRAL REGION; MALE; MELANOCYTE-STIMULATING HORMONES; OVARIECTOMY; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; RATS, SPRAGUE-DAWLEY; RECEPTOR, MELANOCORTIN, TYPE 3; RECEPTOR, MELANOCORTIN, TYPE 4; SPLANCHNIC NERVES;

EID: 84925958858     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2014.284638     Document Type: Article

References (74)

1. Ainslie DA, Morris MJ, Wittert G, Turnbull H, Proietto J & Thorburn AW (2001). Estrogen deficiency causes central leptin insensitivity and increased hypothalamic neuropeptide Y. Int J Obes Relat Metab Disord 25, 1680-1688.
2. Allison MA, Ix JH, Morgan C, McClelland RL, Rifkin D, Shimbo D & Criqui MH (2013). Higher leptin is associated with hypertension: the Multi-Ethnic Study of Atherosclerosis. J Hum Hypertens 27, 617-622.
3. Anglin JC & Brooks VL (2003). Tyrosine hydroxylase and norepinephrine transporter in sympathetic ganglia of female rats vary with reproductive state 1. Auton Neurosci 105, 8-15.
4. Berkelaar M, Eekhoff EM, Simonis-Bik AM, Boomsma DI, Diamant M, Ijzerman RG, Dekker JM, 't Hart LM & de Geus EJ (2013). Effects of induced hyperinsulinaemia with and without hyperglycaemia on measures of cardiac vagal control. Diabetologia 56, 1436-1443.
5. Bohler HC Jr, Tracer H, Merriam GR & Petersen SL (1991). Changes in proopiomelanocortin messenger ribonucleic acid levels in the rostral periarcuate region of the female rat during the estrous cycle. Endocrinology 128, 1265-1269.
6. Brown LM, Gent L, Davis K & Clegg DJ (2010). Metabolic impact of sex hormones on obesity. Brain Res 1350, 77-85.
7. Carter JR, Fu Q, Minson CT & Joyner MJ (2013). Ovarian cycle and sympathoexcitation in premenopausal women. Hypertension 61, 395-399.
8. Cassaglia PA, Hermes SM, Aicher SA & Brooks VL (2011). Insulin acts in the arcuate nucleus to increase lumbar sympathetic nerve activity and baroreflex function in rats. J Physiol 589, 1643-1662.
9. Cassaglia PA, Shi Z, Li B, Reis WL, Clute-Reinig NM, Stern JE & Brooks VL (2014). Neuropeptide Y acts in the paraventricular nucleus to suppress sympathetic nerve activity and its baroreflex regulation. J Physiol 592, 1655-1675.
10. Clegg DJ, Brown LM, Woods SC & Benoit SC (2006). Gonadal hormones determine sensitivity to central leptin and insulin. Diabetes 55, 978-987.
11. Clegg DJ, Riedy CA, Smith KA, Benoit SC & Woods SC (2003). Differential sensitivity to central leptin and insulin in male and female rats. Diabetes 52, 682-687.
12. De Meersman RE, Zion AS, Giardina EG, Weir JP, Lieberman JS & Downey JA (1998). Estrogen replacement, vascular distensibility, and blood pressures in postmenopausal women. Am J Physiol 274, H1539-H1544.
13. Dhillon SS & Belsham DD (2011). Estrogen inhibits NPY secretion through membrane-associated estrogen receptor (ER)-α in clonal, immortalized hypothalamic neurons. Int J Obes (Lond) 35, 198-207.
14. Diano S, Kalra SP, Sakamoto H & Horvath TL (1998). Leptin receptors in estrogen receptor-containing neurons of the female rat hypothalamus. Brain Res 812, 256-259.
15. Dunbar JC & Lu H (1999). Leptin-induced increase in sympathetic nervous and cardiovascular tone is mediated by proopiomelanocortin (POMC) products. Brain Res Bull 50, 215-221.
16. Ellacott KL & Cone RD (2004). The central melanocortin system and the integration of short- and long-term regulators of energy homeostasis. Recent Prog Horm Res 59, 395-408.
17. Esler M, Straznicky N, Eikelis N, Masuo K, Lambert G & Lambert E (2006). Mechanisms of sympathetic activation in obesity-related hypertension. Hypertension 48, 787-796.
18. Fungfuang W, Nakada T, Nakao N, Terada M, Yokosuka M, Gizurarson S, Hau J, Moon C & Saito TR (2013a). Serum leptin concentrations, leptin mRNA expression, and food intake during the estrous cycle in rats. Lab Anim Res 29, 1-6.
19. Fungfuang W, Terada M, Komatsu N, Moon C & Saito TR (2013b). Effects of estrogen on food intake, serum leptin levels and leptin mRNA expression in adipose tissue of female rats. Lab Anim Res 29, 168-173.
20. Gao Q & Horvath TL (2008). Cross-talk between estrogen and leptin signaling in the hypothalamus. Am J Physiol Endocrinol Metab 294, E817-E826.
21. Goldman RK, Azar AS, Mulvaney JM, Hinojosa-Laborde C, Haywood JR & Brooks VL (2009). Baroreflex sensitivity varies during the rat estrous cycle: role of gonadal steroids. Am J Physiol Regul Integr Comp Physiol 296, R1419-R1426.
22. Goldstein DS, Levinson P & Keiser HR (1983). Plasma and urinary catecholamines during the human ovulatory cycle. Am J Obstet Gynecol 146, 824-829.
23. Gonzalez C, Diaz F & Alonso A (2008). Neuroprotective effects of estrogens: cross-talk between estrogen and intracellular insulin signalling. Infect Disord Drug Targets 8, 65-67.
24. Goodman RL (1978). A quantitative analysis of the physiological role of estradiol and progesterone in the control of tonic and surge secretion of luteinizing hormone in the rat. Endocrinology 102, 142-150.
25. Greenfield JR (2011). Melanocortin signalling and the regulation of blood pressure in human obesity. J Neuroendocrinol 23, 186-193.
26. Hall JE, da Silva AA, do Carmo JM, Dubinion J, Hamza S, Munusamy S, Smith G & Stec DE (2010). Obesity-induced hypertension: role of sympathetic nervous system, leptin, and melanocortins. J Biol Chem 285, 17271-17276.
27. Hart EC, Charkoudian N, Wallin BG, Curry TB, Eisenach J & Joyner MJ (2011). Sex and ageing differences in resting arterial pressure regulation: the role of the β-adrenergic receptors. J Physiol 589, 5285-5297.
28. Haynes WG, Morgan DA, Djalali A, Sivitz WI & Mark AL (1999). Interactions between the melanocortin system and leptin in control of sympathetic nerve traffic. Hypertension 33, 542-547.
29. He XR, Wang W, Crofton JT & Share L (1999). Effects of 17β-estradiol on the baroreflex control of sympathetic activity in conscious ovariectomized rats. Am J Physiol 277, R493-R498.
30. He Z, Zhang SS, Meng Q, Li S, Zhu HH, Raquil MA, Alderson N, Zhang H, Wu J, Rui L, Cai D & Feng GS (2012). Shp2 controls female body weight and energy balance by integrating leptin and estrogen signals. Mol Cell Biol 32, 1867-1878.
31. Kelly MJ & Qiu J (2010). Estrogen signaling in hypothalamic circuits controlling reproduction. Brain Res 1364, 44-52.
32. Kim A, Deo SH, Fisher JP & Fadel PJ (2012). Effect of sex and ovarian hormones on carotid baroreflex resetting and function during dynamic exercise in humans. J Appl Physiol (1985) 112, 1361-1371.
33. Kimura M, Irahara M, Yasui T, Saito S, Tezuka M, Yamano S, Kamada M & Aono T (2002). The obesity in bilateral ovariectomized rats is related to a decrease in the expression of leptin receptors in the brain. Biochem Biophys Res Commun 290, 1349-1353.
34. Kneale BJ, Chowienczyk PJ, Brett SE, Coltart DJ & Ritter JM (2000). Gender differences in sensitivity to adrenergic agonists of forearm resistance vasculature. J Am Coll Cardiol 36, 1233-1238.
35. Lambert E, Straznicky N, Eikelis N, Esler M, Dawood T, Masuo K, Schlaich M & Lambert G (2007). Gender differences in sympathetic nervous activity: influence of body mass and blood pressure. J Hypertens 25, 1411-1419.
36. Li B, Shi Z, Cassaglia PA & Brooks VL (2013). Leptin acts in the forebrain to differentially influence baroreflex control of lumbar, renal, and splanchnic sympathetic nerve activity and heart rate. Hypertension 61, 812-819.
37. Mallamaci F, Cuzzola F, Tripepi G, Cutrupi S, Parlongo S, Tripepi R & Zoccali C (2000). Gender-dependent differences in plasma leptin in essential hypertension. Am J Hypertens 13, 914-920.
38. Marsh AJ, Fontes MA, Killinger S, Pawlak DB, Polson JW & Dampney RA (2003). Cardiovascular responses evoked by leptin acting on neurons in the ventromedial and dorsomedial hypothalamus. Hypertension 42, 488-493.
39. Meli R, Pacilio M, Raso GM, Esposito E, Coppola A, Nasti A, Di Carlo C, Nappi C & Di Carlo R (2004). Estrogen and raloxifene modulate leptin and its receptor in hypothalamus and adipose tissue from ovariectomized rats. Endocrinology 145, 3115-3121.
40. Mercer AJ, Hentges ST, Meshul CK & Low MJ (2013). Unraveling the central proopiomelanocortin neural circuits. Front Neurosci 7, 19.
41. Minson CT, Halliwill JR, Young TM & Joyner MJ (2000). Influence of the menstrual cycle on sympathetic activity, baroreflex sensitivity, and vascular transduction in young women. Circulation 101, 862-868.
42. Mohamed MK, El Mas MM & Abdel-Rahman AA (1999). Estrogen enhancement of baroreflex sensitivity is centrally mediated. Am J Physiol 276, R1030-R1037.
43. Montanaro MS, Allen AM & Oldfield BJ (2005). Structural and functional evidence supporting a role for leptin in central neural pathways influencing blood pressure in rats. Exp Physiol 90, 689-696.
44. Muntzel MS, Morgan DA, Mark AL & Johnson AK (1994). Intracerebroventricular insulin produces nonuniform regional increases in sympathetic nerve activity. Am J Physiol 267, R1350-R1355.
45. O'Donohue TL & Jacobowitz DM (1980). Studies of alpha-MSH-containing nerves in the brain. Prog Biochem Pharmacol 16, 69-83.
46. Olofsson LE, Pierce AA & Xu AW (2009). Functional requirement of AgRP and NPY neurons in ovarian cycle-dependent regulation of food intake. Proc Natl Acad Sci USA 106, 15932-15937.
47. Pamidimukkala J, Taylor JA, Welshons WV, Lubahn DB & Hay M (2003). Estrogen modulation of baroreflex function in conscious mice. Am J Physiol Regul Integr Comp Physiol 284, R983-R989.
48. Paxinos G & Watson C (2007). The Rat Brain in Sterotaxic Coordinates, 6th edn. Academic Press, San Diego.
49. 2-adrenoceptor subtype gene expression in cafeteria diet-induced hypertension and consequences of neonatal androgenization. J Pharmacol Exp Ther 302, 525-531.
50. Pratchayasakul W, Chattipakorn N & Chattipakorn SC (2014). Estrogen restores brain insulin sensitivity in ovariectomized non-obese rats, but not in ovariectomized obese rats. Metabolism 63, 851-859.
51. Pricher MP, Freeman KL & Brooks VL (2008). Insulin in the brain increases gain of baroreflex control of heart rate and lumbar sympathetic nerve activity. Hypertension 51, 514-520.
52. 2C receptor signaling in hypothalamic proopiomelanocortin neurons: role in energy homeostasis in females. Mol Pharmacol 72, 885-896.
53. Rahmouni K & Morgan DA (2007). Hypothalamic arcuate nucleus mediates the sympathetic and arterial pressure responses to leptin. Hypertension 49, 647-652.
54. Rahmouni K, Morgan DA, Morgan GM, Liu X, Sigmund CD, Mark AL & Haynes WG (2004). Hypothalamic PI3K and MAPK differentially mediate regional sympathetic activation to insulin. J Clin Invest 114, 652-658.
55. Rahmouni K, Sigmund CD, Haynes WG & Mark AL (2009). Hypothalamic ERK mediates the anorectic and thermogenic sympathetic effects of leptin. Diabetes 58, 536-542.
56. Resko JA, Ellinwood WE, Pasztor LM & Buhl AE (1980). Sex steroids in the umbilical circulation of fetal rhesus monkeys from the time of gonadal differentiation. J Clin Endocrinol Metab 50, 900-905.
57. Roepke TA, Qiu J, Smith AW, Ronnekleiv OK & Kelly MJ (2011). Fasting and 17β-estradiol differentially modulate the M-current in neuropeptide Y neurons. J Neurosci 31, 11825-11835.
58. Roselli CE, Ellinwood WE & Resko JA (1984). Regulation of brain aromatase activity in rats. Endocrinology 114, 192-200.
59. Roselli CE, Horton LE & Resko JA (1985). Distribution and regulation of aromatase activity in the rat hypothalamus and limbic system. Endocrinology 117, 2471-2477.
60. Saeki Y, Atogami F, Takahashi K & Yoshizawa T (1997). Reflex control of autonomic function induced by posture change during the menstrual cycle. J Auton Nerv Syst 66, 69-74.
61. Saleh MC, Connell BJ & Saleh TM (2000). Autonomic and cardiovascular reflex responses to central estrogen injection in ovariectomized female rats. Brain Res 879, 105-114.
62. Saleh TM & Connell BJ (1999). Centrally mediated effect of 17β-estradiol on parasympathetic tone in male rats. Am J Physiol 276, R474-R481.
63. Saleh TM & Connell BJ (2000). 17β-estradiol modulates baroreflex sensitivity and autonomic tone of female rats. J Auton Nerv Syst 80, 148-161.
64. Shimizu H, Shimomura Y, Nakanishi Y, Futawatari T, Ohtani K, Sato N & Mori M (1997). Estrogen increases in vivo leptin production in rats and human subjects. J Endocrinol 154, 285-292.
65. Siani A, Strazzullo P, Giorgione N, De Leo A & Mancini M (1990). Insulin-induced increase in heart rate and its prevention by propranolol. Eur J Clin Pharmacol 38, 393-395.
66. Smith AW, Bosch MA, Wagner EJ, Ronnekleiv OK & Kelly MJ (2013). The membrane estrogen receptor ligand STX rapidly enhances GABAergic signaling in NPY/AgRP neurons: role in mediating the anorexigenic effects of 17β-estradiol. Am J Physiol Endocrinol Metab 305, E632-E640.
67. Tanaka M, Sato M, Umehara S & Nishikawa T (2003). Influence of menstrual cycle on baroreflex control of heart rate: comparison with male volunteers. Am J Physiol Regul Integr Comp Physiol 285, R1091-R1097.
68. Tank J, Heusser K, Diedrich A, Hering D, Luft FC, Busjahn A, Narkiewicz K & Jordan J (2008). Influences of gender on the interaction between sympathetic nerve traffic and central adiposity. J Clin Endocrinol Metab 93, 4974-4978.
69. Ulrich-Lai YM, Jones KR, Ziegler DR, Cullinan WE & Herman JP (2011). Forebrain origins of glutamatergic innervation to the rat paraventricular nucleus of the hypothalamus: differential inputs to the anterior versus posterior subregions. J Comp Neurol 519, 1301-1319.
70. Vongpatanasin W, Tuncel M, Mansour Y, Arbique D & Victor RG (2001). Transdermal estrogen replacement therapy decreases sympathetic activity in postmenopausal women. Circulation 103, 2903-2908.
71. Williams KW, Margatho LO, Lee CE, Choi M, Lee S, Scott MM, Elias CF & Elmquist JK (2010). Segregation of acute leptin and insulin effects in distinct populations of arcuate proopiomelanocortin neurons. J Neuroscie 30, 2472-2479.
72. Wise PM, Scarbrough K, Weiland NG & Larson GH (1990). Diurnal pattern of proopiomelanocortin gene expression in the arcuate nucleus of proestrous, ovariectomized, and steroid-treated rats: a possible role in cyclic luteinizing hormone secretion. Mol Endocrinol 4, 886-892.
73. Ye ZY & Li DP (2011). Activation of the melanocortin-4 receptor causes enhanced excitation in presympathetic paraventricular neurons in obese Zucker rats. Regul Pept 166, 112-120.
74. Zhang ZH & Felder RB (2004). Melanocortin receptors mediate the excitatory effects of blood-borne murine leptin on hypothalamic paraventricular neurons in rat. Am J Physiol Regul Integr Comp Physiol 286, R303-R310.