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Receptor-mediated regional sympathetic nerve activation by leptin.
Open accessAbstract
Leptin is a peptide hormone produced by adipose tissue which acts centrally to decrease appetite and increase energy expenditure. Although leptin increases norepinephrine turnover in thermogenic tissues, the effects of leptin on directly measured sympathetic nerve activity to thermogenic and other tissues are not known. We examined the effects of intravenous leptin and vehicle on sympathetic nerve activity to brown adipose tissue, kidney, hindlimb, and adrenal gland in anesthetized Sprague-Dawley rats. Intravenous infusion of mouse leptin over 3 h (total dose 10-1,000 microg/kg) increased plasma concentrations of immunoreactive murine leptin up to 50-fold. Leptin slowly increased sympathetic nerve activity to brown adipose tissue (+286+/-64% at 1,000 microg/kg; P = 0.002). Surprisingly, leptin infusion also produced gradual increases in renal sympathetic nerve activity (+228+/-63% at 1,000 microg/kg; P = 0.0008). The effect of leptin on sympathetic nerve activity was dose dependent, with a threshold dose of 100 microg/kg. Leptin also increased sympathetic nerve activity to the hindlimb (+287+/-60%) and adrenal gland (388+/-171%). Despite the increase in overall sympathetic nerve activity, leptin did not increase arterial pressure or heart rate. Leptin did not change plasma glucose and insulin concentrations. Infusion of vehicle did not alter sympathetic nerve activity. Obese Zucker rats, known to possess a mutation in the gene for the leptin receptor, were resistant to the sympathoexcitatory effects of leptin, despite higher achieved plasma leptin concentrations. These data demonstrate that leptin increases thermogenic sympathetic nerve activity and reveal an unexpected stimulatory effect of leptin on overall sympathetic nerve traffic.
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In the citing paper
“These findings are in contrast to the effect of leptin administration on increase natriuresis (49, 50) and sympathetic activity (51) in normal, nonobese leptin-resistant Zucker rats (51).”
From The role of falling leptin levels in the neuroendocrine and metabolic adaptation to short-term starvation in healthy men (2003) · cites this paper as [51]
Experimental — accuracy not yet measuredIn the citing paper
“Plasma leptin concentration is highly correlated with SNA activity123, and acute leptin infusions increase SNA in the brown adipose tissue, adrenal glands and kidneys of rodents124.”
From Obesity, kidney dysfunction and hypertension: mechanistic links (2019) · cites this paper as [124]
In the citing paper
“acute leptin administration in rodents increased SNS activity in brown adipose tissue (BAT), the adrenal gland, and the kidneys84.”
From Obesity-Induced Hypertension: Interaction of Neurohumoral and Renal Mechanisms (2015) · cites this paper as [84]
In the citing paper
“Acute leptin administration in rodents and humans increases renal and muscle SNS activity [45, 46] while chronic increases in plasma leptin levels, comparable to those found in severe obesity, caused sustained increases in BP and HR in rodents despite causing weight loss which would normally reduce BP [47].”
From Role of the brain melanocortins in blood pressure regulation (2017) · cites this paper as [45]
In the citing paper
“In addition its effects on appetite and metabolism, leptin acts in the brain to produce receptor-mediated increases in regional sympathetic activity91.”
From The Sympathetic Nervous System Alterations in Human Hypertension (2015) · cites this paper as [91]
In the citing paper
“Leptin is a potent appetite suppressant and, like insulin, stimulates the SNS.24,25”
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“Murine studies also found that leptin increased renal sympathetic nerve activity in a dose-dependent manner [37,38].”
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“R: Corticotropin-releasing factor receptor subtype 1, 2 CART: Cocaine- and amphetamine-regulated transcript GOAT: Ghrelin-O-acyl-transferase 3T3-L1: Preadipocytes GPR39: G-protein-coupled receptor 39 GLP-1: Glucagon-like peptide-1 IGF-1: Insulin growth factor 1 NTS: Nucleus tractus solitarius SNS: Sympathetic nervous…”
BackgroundInfluentialObesity, hypertension, and sympathetic nervous system activity
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“Leptin, a novel protein hormone produced almost exclusively by adipose tissue has been recently described in detail [ 48 ,49].”
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“Surprisingly, leptin also caused a significant and dose-dependent increase in sympathetic nerve activity to the kidneys, hindlimb, and adrenal glands [15].”
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“Similarly, intravenous or intracerebroventricular injection of leptin was found to induce a slow but progressive increase in sympathetic nerve activity in peripheral tissues (25,26), whereas intracerebroventricular injection of a-melanocyte–stimulating hormone (a-MSH) resulted in immediate activation of sympathetic ne…”
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Peripheral injection of risperidone, an atypical antipsychotic, alters the bodyweight gain of rats
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Self-citationCafeteria Diet Increases Fat Mass and Chronically Elevates Lumbar Sympathetic Nerve Activity in Rats
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“For example, obese hypertensive patients have increased muscle sympathetic nerve activity (SNA) compared with lean controls,1 and weight loss causes marked reductions in SNA.2 In addition, experimental animals and humans fed high-fat diets show increases in renal and muscle SNA.3–7 This sympathetic overactivity, cause…”
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Strategies for the Delivery of Leptin to the CNS
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“But leptin also has effects on brain maturation, bone density, immunity, reproduction, angiogenesis, hemodynamics, breathing, sympathetic nerve activity, the BBB transporter of urocortin, and insulin-associated liver functions (Cohen et al., 1996; Haynes et al., 1997; Bouloumié et al., 1998; Ahima et al., 1999; O’Donn…”
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“These effects of leptin on energy expenditure may be secondary to activation of the sympathetic nervous system because leptin administration activates the sympathetic nervous system in rodents (15) and in nonhuman primates (16).”
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Role of the Paraventricular Nucleus of the Hypothalamus in the Sympathoexcitatory Effects of Leptin
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Self-citationLeptin production during early starvation in lean and obese women
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“Leptin signaling in the CNS results in a decrease in food intake and an increase in energy expenditure,(3) in part, by enhancing sympathetic activity to thermogenic brown adipose tissue (BAT).(4) In addition to its role in central energy control, leptin increases sympathetic nerve activity (SNA) to organs involved in…”
BackgroundSelf-citationMetabolic responses to leptin in obese db/db mice are strain dependent
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“These are thought to be centrally mediated responses (22) and may not be present in mice lacking ObRb.”
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“We and others have shown that intravenous and intracerebroventricular leptin administration increases SNA measured by direct nerve recording in lumbar nerves (10, 12, 13) and nerve fibers to IBAT (12, 13).”
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Synergy of sibutramine and low-dose leptin in treatment of diet-induced obesity in rats
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“…of food intake and energy homeostasis (Zhang et al. 1994), has been shown to modulate HPA axis activity (Morimoto et al. 2000), SNS activity (Haynes et al. 1997), and the release of proinflammatory cytokines (Lappas et al. 2005), implying that it has the potential to modify the stress…”
BackgroundLeptin‐Induced Endothelial Dysfunction Is Mediated by Sympathetic Nervous System Activity
Wang, J., Wang, H., Luo, W., Guo, C., Wang, J., Chen, Y. E., Chang, L., & Eitzman, D. T. (2013) · Journal of the American Heart Association · doi:10.1161/jaha.113.000299 · Cited by 57
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Briley, L. P., & Szczech, L. A. M. (2006) · Seminars in Dialysis · doi:10.1111/j.1525-139x.2006.00119.x · Cited by 58
Heritability of plasma leptin levels
Narkiewicz, K., Szczęch, R., Winnicki, M., Chrostowska, M., Pawłowski, R., Łysiak−Szydłowska, W., Choe, I., Kato, M., Sivitz, W. I., Krupa-Wojciechowska, B., et al. (1999) · Journal of Hypertension · doi:10.1097/00004872-199917010-00005 · Cited by 56
Self-citationBivariate genetic analysis of fasting insulin and glucose levels
Snieder, H., Boomsma, D. I., van Doornen, L. J. P., & Neale, M. C. (1999) · Genetic Epidemiology · doi:10.1002/(sici)1098-2272(1999)16:4 · Cited by 56
Role of the hypothalamic arcuate nucleus in cardiovascular regulation
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Evidence for lower sympathetic nerve activity in young adults with low birth weight
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Leptin in pediatrics: A hormone from adipocyte that wheels several functions in children
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“Leptin and cardiovascular system Leptin possesses potent vascular effects and participates in the regulation of sympathetic tone and arterial blood pressure through central as well as peripheral actions.[93]”
BackgroundEndothelial effects of leptin: Implications in health and diseases
Rahmouni, K., & Haynes, W. G. (2005) · Current Diabetes Reports · doi:10.1007/s11892-005-0020-5 · Cited by 53
“The investigation of the potential vasodilator action of leptin was triggered by the observation that acute intravenous administration of leptin does not increase arterial pressure in rats despite the robust increase in sympathetic outflow, which suggested that leptin may have a peripheral vasodilator action that oppo…”
BackgroundSelf-citationEndothelin-1 Stimulates Leptin Production in Adipocytes
Xiong, Y., Tanaka, H., Richardson, J. A., Williams, S. C., Slaughter, C. A., Nakamura, M., Chen, J., & Yanagisawa, M. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m103478200 · Cited by 54
Role of adipokines in obesity‐associated hypertension
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“In contrast, short-term peripheral leptin administration did not affect blood pressure neither in anesthetized (Haynes et al. 1997) nor in conscious rats (Gardiner et al. 2000, Rahmouni et al. 2005a).”
BackgroundLeptin as a Key between Obesity and Cardiovascular Disease
Kang, K., Ok, M., & Lee, S. (2020) · Journal of Obesity & Metabolic Syndrome · doi:10.7570/jomes20120 · Cited by 53
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Chronic Kidney Disease, Obesity, and Hypertension: The Role of Leptin and Adiponectin
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“Studies conducted in murine models have shown how hyperexpression of lectin increases the activity of sympathetic nervous system, leading to an upregulation of blood pressure and an increase of urinary catecholamine excretion [31, 35].”
BackgroundCentral Leptin Infusion Attenuates the Cardiovascular and Metabolic Effects of Fasting in Rats
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“After 3 days of baseline measurement, the rats were assigned to 1 of 4 groups (n55 to 6/group): (1) ICV saline‐ad libitum, ( 2 ) ICV leptin‐ad libitum, (3) ICV saline‐fasting/refeeding, and (4) ICV leptin‐fasting/refeeding.”
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G protein-coupled receptor 12 deficiency results in dyslipidemia and obesity in mice
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Altered regulation of the rostral ventrolateral medulla in hypertensive obese Zucker rats
Huber, D. A., & Schreihofer, A. M. (2011) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00075.2011 · Cited by 49
Direct measurement of renal sympathetic nervous activity in high-fat diet-related hypertensive rats
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Induction of Uncoupling Protein Expression in Brown and White Adipose Tissue by Leptin
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Integration of sensory information via central thermoregulatory leptin targets
Rezai-Zadeh, K. P., & Münzberg, H. (2013) · Physiology & Behavior · doi:10.1016/j.physbeh.2013.02.014 · Cited by 52
“In rodents, leptin deficiency is associated with BAT atrophy and low UCP1 expression, thus compromising BAT-derived heat production [27, 28] and exogenous leptin injections stimulate sympathetic BAT inputs [29].”
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“The VMH has been described as having both an inhibitory and an excitatory effect on the cardiovascular system (Bunag & Inoue, 1985; Hirasawa et al. 1996).”
BackgroundLeptin and insulin homeostasis in epilepsy: Relation to weight adverse conditions
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Leptin Potentiates Thermogenic Sympathetic Responses to Hypothermia
Hausberg, M., Morgan, D. A., Mitchell, J., Sivitz, W. I., Mark, A. L., & Haynes, W. G. (2002) · Diabetes · doi:10.2337/diabetes.51.8.2434 · Cited by 48
Self-citationHypertension in obesity: is leptin the culprit?
Simonds, S. E., & Cowley, M. A. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.01.004 · Cited by 50
Metadata
- Authors
- Haynes, W. G., Morgan, D. A., Walsh, S. A., Mark, A. L., & Sivitz, W. I.
- Affiliations
- University of Iowa (US)
- Venue
- Journal of Clinical Investigation
- Published
- 1997-07-15
- Volume
- 100
- Issue
- 2
- Pages
- 270-278
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC508189
- OpenAlex
- W2061340727
- Cited by
- 979
- References
- 29
- Citations by year
- 2026: 7 · 2025: 12 · 2024: 17 · 2023: 11 · 2022: 14 · 2021: 17 · 2020: 15 · 2019: 13 · 2018: 11 · 2017: 31 · 2016: 29 · 2015: 25 · 2014: 44 · 2013: 34 · 2012: 43
- FWCI
- 14.77
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Clinical Investigation (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- U.S. Department of Veterans Affairs
- Wellcome Trust
- National Institutes of Health (5p50hl044546-05, 5r29hl043514-05)
- National Heart, Lung, and Blood Institute (HL-43514, HL-44546)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK-25295, P30DK025295)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
- Health Sciences › Medicine › Physiology (medical) › Adipose Tissue and Metabolism
- Keywords
- leptin, sympathetic activity, brown adipose tissue, renal sympathetic nerve activity, adrenal gland, thermogenesis, leptin receptor, Zucker fatty rats, norepinephrine, energy homeostasis
- MeSH terms
- Action Potentials, Adrenal Glands, Animals, Blood Glucose, Adipose Tissue, Brown, Disease Models, Animal, Hemodynamics, Hindlimb, Insulin, Kidney, Male, Obesity, Proteins, Rats, Zucker, Sympathetic Nervous System, Rats, Sprague-Dawley, Leptin, Rats
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