Cited by 1,010Regulation of Appetite and ObesityAdipokines, Inflammation, and Metabolic DiseasesHypothalamic control of reproductive hormones

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STAT3 signalling is required for leptin regulation of energy balance but not reproduction

Bates, Sarah H., Stearns, Walter H., Dundon, Trevor A., Schubert, Markus, Tso, Annette W. K., Wang, Yongping, Banks, Alexander S., Lavery, Hugh J., Haq, Asma K., Maratos-Flier, Eleftheria, Neel, Benjamin G., Schwartz, Michael W., Myers, Martin G.·2003·Nature

DOI 10.1038/nature01388

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Abstract

Secretion of leptin from adipocytes communicates body energy status to the brain by activating the leptin receptor long form (LRb). LRb regulates energy homeostasis and neuroendocrine function; the absence of LRb in db/db mice results in obesity, impaired growth, infertility and diabetes. Tyr 1138 of LRb mediates activation of the transcription factor STAT3 during leptin action. To investigate the contribution of STAT3 signalling to leptin action in vivo, we replaced the gene encoding the leptin receptor (lepr) in mice with an allele coding for a replacement of Tyr 1138 in LRb with a serine residue (lepr(S1138)) that specifically disrupts the LRb-STAT3 signal. Here we show that, like db/db mice, lepr(S1138) homozygotes (s/s) are hyperphagic and obese. However, whereas db/db mice are infertile, short and diabetic, s/s mice are fertile, long and less hyperglycaemic. Furthermore, hypothalamic expression of neuropeptide Y (NPY) is elevated in db/db mice but not s/s mice, whereas the hypothalamic melanocortin system is suppressed in both db/db and s/s mice. LRb-STAT3 signalling thus mediates the effects of leptin on melanocortin production and body energy homeostasis, whereas distinct LRb signals regulate NPY and the control of fertility, growth and glucose homeostasis.

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Background
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Background
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Background
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Result
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Background
An allelic series for the leptin receptor gene generated by CRE and FLP recombinase
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“In addition, a Y1138S point mutation in the murine LEPR-B abrogates STAT-3 protein phosphorylation and fully recapitulates the obese phenotype observed in Leprdb/db and Lepob/ob mice (Bates et al. 2003).”
Background
The role of leptin-->STAT3 signaling in neuroendocrine function: an integrative perspective
Bates, S. H., & Myers, M. G. (2004) · Journal of Molecular Medicine · doi:10.1007/s00109-003-0494-z · Cited by 81
Self-citation
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“The s/s mice bearing disruption of the LepRb–STAT3 pathway (Bates et al., 2003) also displayed unaltered hepatic sympathetic response to leptin indicating that STAT3 is not involved in the control of liver sympathetic outflow by leptin.”
BackgroundMethodInfluential
Signal Transducer and Activator of Transcription-3 Is Required in Hypothalamic Agouti-Related Protein/Neuropeptide Y Neurons for Normal Energy Homeostasis
Gong, L., Yao, F., Hockman, K., Heng, H. H., Morton, G. J., Takeda, K., Akira, S., Low, M. J., Rubinstein, M., & MacKenzie, R. G. (2008) · Endocrinology · doi:10.1210/en.2007-0945 · Cited by 80
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Self-citation
Leptin signaling in neurotensin neurons involves STAT, MAP kinases ERK1/2, and p38 through c‐Fos and ATF1
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“The mechanisms involved in alternative leptin signaling in the hypothalamus are poorly understood, although it is accepted that other important pathways are necessary for all of the diverse functions ascribed to leptin (9).”
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“Defective leptin JAK2-STAT3 signaling in the hypothalamus is involved in the development of central leptin resistance in highsaturated-fat diet-induced obesity in rodents [38].”
Background
Glut2‐dependent glucose‐sensing controls thermoregulation by enhancing the leptin sensitivity of NPY and POMC neurons
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“Similarly, mice with a knockout of STAT3, an essential component of leptin receptor intracellular signaling (28, 29), or with genetic inactivation of MC4R (30) also have reduced thermogenesis and increased body weight.”
Background
Dietary Components in the Development of Leptin Resistance
Vasselli, J. R., Scarpace, P. J., Harris, R. B. S., & Banks, W. A. (2013) · Advances in Nutrition · doi:10.3945/an.112.003152 · Cited by 87
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“The Jak ⁄STAT3 pathway is essential for leptin regulation of energy homeostasis, but not for the control of reproductive function, growth or glucose homeostasis.(9)”
Background
The Acute-Phase Protein Orosomucoid Regulates Food Intake and Energy Homeostasis via Leptin Receptor Signaling Pathway
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“Disruption of the STAT3-binding site on LepR resulted in hyperphagia and obesity (46).”
Background
Puberty in Mice and Rats
Prévot, V. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-397175-3.00030-2 · Cited by 79
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“This is compatible with the role of pSTAT3 signaling in the metabolic effects of endogenous leptin, as proposed previously [33,34].”
Background
Leptin Induces Phosphorylation of Neuronal Nitric Oxide Synthase in Defined Hypothalamic Neurons
Donato, J., Frazão, R., Fukuda, M., Vianna, C. R., & Elias, C. F. (2010) · Endocrinology · doi:10.1210/en.2010-0651 · Cited by 76
“Leptin induces pSTAT3-ir in neurons expressing NADPHd activity To identify the NOergic neurons directly responsive to leptin, we assessed coexpression of NADPHd activity as a marker for NO production (36–38, 43) and leptin-induced pSTAT3-ir as a maker for direct leptin action (40, 48, 49).”
Method
Structural insights into the mechanism of leptin receptor activation
Saxton, R. A., Caveney, N. A., Moya-Garzón, M. D., Householder, K. D., Rodriguez, G. E., Burdsall, K. A., Long, J. Z., & García, K. C. (2023) · Nature Communications · doi:10.1038/s41467-023-37169-6 · Cited by 84
Neuronal deletion of Lepr elicits diabesity in mice without affecting cold tolerance or fertility
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“For instance, Lepr homozygotes, with a single amino acid mutation in the STAT3 signaling portion of LEPR-B, are fertile despite their extreme obesity, which may be attributed to 40% reduced NPY levels compared with db/db mice (4).”
Background
Suppression of leptin-induced hypothalamic JAK/STAT signalling and feeding response during pregnancy in the mouse
Ladyman, S. R., Fieldwick, D., & Grattan, D. R. (2012) · Reproduction · doi:10.1530/rep-12-0112 · Cited by 77
“There are currently seven members of the STAT family (Darnell 1997), and it is well established that in the hypothalamus, leptin acts through STAT3 to suppress food intake (Bates et al. 2003).”
Background
Possible Integrative Actions of Leptin and Insulin Signaling in the Hypothalamus Targeting Energy Homeostasis
Thon, M., Hosoi, T., & Ozawa, K. (2016) · Frontiers in Endocrinology · doi:10.3389/fendo.2016.00138 · Cited by 75
“Nuclear phospho-STAT3 acts as a transcription factor for STAT3-targeted genes (20, 21).”
Background
Spinal interleukin-10 produces antinociception in neuropathy through microglial β-endorphin expression, separated from antineuroinflammation
Wu, H., Mao, X.-F., Tang, X.-Q., Ali, U., Apryani, E., Liu, H., Li, X., & Wang, Y. (2018) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2018.06.015 · Cited by 75
“In addition, NSC74859 totally blocked IL-10-stimulated βendorphin expression, consistent with the previous findings that STAT3 was an effective inducer of POMC expression in COS-7 cell lines (Scully and Rosenfeld, 2002; Bates et al., 2003).”
Self-citation
Leptin Stimulates Neuropeptide Y and Cocaine Amphetamine-Regulated Transcript Coexpressing Neuronal Activity in the Dorsomedial Hypothalamus in Diet-Induced Obese Mice
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“NPY neurons in the DMH are leptin sensitive in DIO mice Since ARH NPY neurons express a signaling form of leptin receptor ObRb (Bates et al., 2003), we investigated the presence of leptin signaling in DMH NPY neurons in DIO mice.”
Background
Hypothalamic S1P/S1PR1 axis controls energy homeostasis
Silva, V. R. R., Micheletti, T. O., Pimentel, G. D., Katashima, C. K., Lenhare, L., Morari, J., Mendes, M. C. S., Razolli, D. S., Rocha, G. Z., de Souza, C. T., et al. (2014) · Nature Communications · doi:10.1038/ncomms5859 · Cited by 77
“Accumulating number of studies have demonstrated that hypothalamic STAT3 tyrosine 705 phosphorylation precedes STAT3 DNA binding, promoting transcriptional activation of the POMC promoter, induced by anorexigenic factors, including leptin 2,21–23 or cytokines 24–26 .”
Proanthocyanidins potentiate hypothalamic leptin/STAT3 signalling and Pomc gene expression in rats with diet-induced obesity
Ibars, M., Ardid‐Ruiz, A., Suárez, M., Muguerza, B., Bladé, C., & Aragonès, G. (2016) · International Journal of Obesity · doi:10.1038/ijo.2016.169 · Cited by 77
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Development of Diabesity in Mice with Neuronal Deletion of Shp2 Tyrosine Phosphatase
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“Two key long-term regulators of energy balance, the adiposity negative feedback signals, insulin and leptin, signal via a range of intracellular signal transduction mechanisms, including PI3K-Akt and JAK-STAT pathways [8,27,53–55].”
Background
Leptin receptor modulation of adiposity and fertility
Israel, D. D., & Chua, S. C. (2009) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2009.07.004 · Cited by 74
“As previously mentioned, it appears that the transcriptional effects of leptin receptor signaling are not necessary for leptin's modulatory effects on GnRH neurons since ablation of STAT3 activation by LEPR does not impose infertility in Y1138S LEPR-B mutant females [19].”
BackgroundResult
Insulin secretory defects and impaired islet architecture in pancreatic β-cell-specific STAT3 knockout mice
Gorogawa, S.-I., Fujitani, Y., Kaneto, H., Hazama, Y., Watada, H., Miyamoto, Y., Takeda, K., Akira, S., Magnuson, M. A., Yamasaki, Y., et al. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.05.095 · Cited by 71
Transplanted Hypothalamic Neurons Restore Leptin Signaling and Ameliorate Obesity in db/db Mice
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“The phosphorylation and nuclear translocation of STAT3 is a well characterized leptin signaling response (24-26).”
Background
New Pharmacological Perspectives for the Leptin Receptor in the Treatment of Obesity
Roujeau, C., Jockers, R., & Dam, J. (2014) · Frontiers in Endocrinology · doi:10.3389/fendo.2014.00167 · Cited by 71
“Proc Natl Acad Sci U S A (2011) 108(16):6585–90.”
Background
Regulation of Proopiomelanocortin Gene Expression
Jenks, B. G. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2008.03620.x · Cited by 70
Insulin Receptor Substrate 4 Couples the Leptin Receptor to Multiple Signaling Pathways
Wauman, J., de Smet, A.-S., Catteeuw, D., Belsham, D. D., & Tavernier, J. H. (2007) · Molecular Endocrinology · doi:10.1210/me.2007-0414 · Cited by 69
Impaired hypothalamic insulin signaling in CUMS rats: Restored by icariin and fluoxetine through inhibiting CRF system
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Chronic AMP-kinase activation with AICAR reduces adiposity by remodeling adipocyte metabolism and increasing leptin sensitivity
Gaidhu, M. P., Frontini, A., Hung, S., Pistor, K., Cinti, S., & Ceddia, R. B. (2011) · Journal of Lipid Research · doi:10.1194/jlr.m015354 · Cited by 70
Roles of leptin, adiponectin and resistin in the transcriptional regulation of steroidogenic genes contributing to decreased Leydig cells function in obesity
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“The Ob-Rb isoform has three conserved tyrosine residues (Y985, Y1077 and Y1138 according to mouse receptor sequence) important for cytoplasmic signal transduction (Figure 1).”
BackgroundInfluential
Adipokines that link obesity and diabetes to the hypothalamus
Ahima, R. S., Qi, Y., & Singhal, N. S. (2006) · Progress in brain research · doi:10.1016/s0079-6123(06)53009-2 · Cited by 72
Neuroendocrine and metabolic effects of adipocyte-derived hormones
Jackson, M. B., & Ahima, R. S. (2006) · Clinical Science · doi:10.1042/cs20050243 · Cited by 68
Targeting Intermediary Metabolism in the Hypothalamus as a Mechanism to Regulate Appetite
Lopaschuk, G. D., Ussher, J. R., & Jaswal, J. S. (2010) · Pharmacological Reviews · doi:10.1124/pr.109.002428 · Cited by 71
“Likewise, mice with STAT3 signaling abrogated via mutation of tyrosine residue 1178 to alanine in the leptin receptor have a phenotype mimicking the hyperphagia and obesity observed in leptin receptor-deficient db/db mice (Bates et al., 2003).”
Background
Insights into amylin–leptin synergy
Trevaskis, J. L., Parkes, D. G., & Roth, J. D. (2010) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2010.03.006 · Cited by 69
Exercise and diabetes have opposite effects on the assembly and O-GlcNAc modification of the mSin3A/HDAC1/2 complex in the heart
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“Tibia length was also significantly reduced in db mice at the 4 week time point, consistent with previous reports of reduced linear skeletal growth in db mice [50,51].”
Systematic analysis of dopamine receptor genes (DRD1–DRD5) in antipsychotic-induced weight gain
Müller, D., Zai, C. C. H., Sicard, M. N., Remington, E., de Souza, R. P., Tiwari, A. K., Hwang, R., Likhodi, O., Shaikh, S. A., Freeman, N., et al. (2010) · The Pharmacogenomics Journal · doi:10.1038/tpj.2010.65 · Cited by 69
Neuroendocrine integration of nutritional signals on reproduction
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Central leptin gene therapy fails to overcome leptin resistance associated with diet-induced obesity
Wilsey, J. T., Zolotukhin, S., Prima, V., & Scarpace, P. J. (2003) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00193.2003 · Cited by 67
“on energy homeostasis and the anorexic/thermogenic melanocortin system (2).”
Background
Leptin Regulates Neointima Formation After Arterial Injury Through Mechanisms Independent of Blood Pressure and the Leptin Receptor/STAT3 Signaling Pathways Involved in Energy Balance
Bodary, P. F., Shen, Y., Öhman, M. K., Bahrou, K. L., Vargas, F. B., Cudney, S. S., Wickenheiser, K. J., Myers, M. G., & Eitzman, D. T. (2006) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000252068.89775.ee · Cited by 67
Self-citation
Leptin regulated calcium channels of neuropeptide Y and proopiomelanocortin neurons by activation of different signal pathways
Wang, J.-H., Wang, F., Yang, M., Yu, D., Wu, W., Liu, J., Ma, L., Cai, F., & Chen, J. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.04.079 · Cited by 66
High Circulating Leptin Receptors with Normal Leptin Sensitivity in Liver-specific Insulin Receptor Knock-out (LIRKO) Mice
Cohen, S. E., Kokkotou, E. G., Biddinger, S. B., Kondo, T., Gebhardt, R., Kratzsch, J., Mantzoros, C. S., & Kahn, C. R. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m704053200 · Cited by 67
Leptin resistance and obesity in mice with deletion of methyl-CpG-binding protein 2 (MeCP2) in hypothalamic pro-opiomelanocortin (POMC) neurons
Wang, X., Lacza, Z., Sun, Y. E., & Han, W. (2013) · Diabetologia · doi:10.1007/s00125-013-3072-0 · Cited by 67
“Deficits in JAK2/STAT3 signalling in POMC neurons are associated with reduced Pomc expression, leptin resistance and obesity [11, 12].”
mTORC1 signaling in energy balance and metabolic disease
Catania, C., Binder, E., & Cota, D. (2010) · International Journal of Obesity · doi:10.1038/ijo.2010.208 · Cited by 68
Intrauterine growth restriction alters term fetal baboon hypothalamic appetitive peptide balance
Li, C., McDonald, T. J., Wu, G., Nijland, M. J., & Nathanielsz, P. W. (2013) · Journal of Endocrinology · doi:10.1530/joe-13-0012 · Cited by 64
“…(Nijland et al. 2010) that IUGR increases fetal ARH glucocorticoid receptor (GR) expression; and iv) as STAT3 inhibits the orexigenic peptide NPY (Bates et al. 2003, Diano et al. 2011), IUGR http://joe.endocrinology-journals.org 2013 Society for Endocrinology DOI: 10.1530/JOE-13-0012 Printed in…”
BackgroundInfluential
Deficiency of leptin receptor in myeloid cells disrupts hypothalamic metabolic circuits and causes body weight increase
Gao, Y., Vidal-Itriago, A., Milanova, I. V., Korpel, N. L., Kalsbeek, M. J. T., Tom, R. Z., Kalsbeek, A., Hofmann, S. M., & Yi, C. (2017) · Molecular Metabolism · doi:10.1016/j.molmet.2017.11.003 · Cited by 64
“Leptin receptor deficiency in myeloid cells decreases POMC neurons projecting from ARC to PVN In the hypothalamus of LepR flþ/þ Cx3cr1 Creþ/- mice, a significant decrease of POMC-ir neuron number was found in the ARC (Figure 3A1, B1, C), with a trend for increased AGRP-ir compared to WT mice (Figure 3A2, B2, D).”
BackgroundInfluential
Green Tea Polyphenol (−)-Epigallocatechin Gallate (EGCG) Attenuates Neuroinflammation in Palmitic Acid-Stimulated BV-2 Microglia and High-Fat Diet-Induced Obese Mice
Mao, L., Hochstetter, D., Yao, L., Zhao, Y., Zhou, J., Wang, Y., & Xu, P. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20205081 · Cited by 63
Self-citation
Tyrosine-dependent and -independent actions of leptin receptor in control of energy balance and glucose homeostasis
Jiang, L., You, J., Yu, X., Gonzalez, L., Yu, Y., Wang, Q. A., Yang, G., Li, W., Cai, L., & Liu, Y. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0804589105 · Cited by 61
“Similar to the reported findings in the s/s mice (8) with targeted substitution mutation at Tyr1138 by serine, replacement by phenylalanine of all 3 tyrosines or Tyr1138 within Ob-Rb abolished leptin-stimulated phosphorylation of STAT3 in the hypothalamus (Fig.”
BackgroundResultInfluential
Leptin receptor 170 kDa (OB‐R170) protein expression is reduced in obese human skeletal muscle: a potential mechanism of leptin resistance
Fuentes, T., Ara, I., Guadalupe‐Grau, A., Larsen, S., Stallknecht, B. M., Olmedillas, H., Santana, A., Helge, J. W., Calbet, J. A. L., & Guerra, B. (2009) · Experimental Physiology · doi:10.1113/expphysiol.2009.049270 · Cited by 64
“Leptin may also downregulate leptin signalling in the target tissues by inducing the protein suppressor of cytokine signalling 3 (SOCS3), which blunts JAK2/STAT3-dependent leptin signalling (Bjørbæk et al. 2000) and causes leptin resistance in the skeletal muscle (Steinberg et al. 2006c).”
BackgroundInfluential
Leptin action via LepR-b Tyr1077 contributes to the control of energy balance and female reproduction
Patterson, C. M., Villanueva, E. C., Greenwald-Yarnell, M. L., Rajala, M. W., Gonzalez, I. E., Saini, N., Jones, J. C., & Myers, M. G. (2012) · Molecular Metabolism · doi:10.1016/j.molmet.2012.05.001 · Cited by 60
Self-citation
The PI3K signaling pathway mediates the biological effects of leptin.
Donato, J., Frazão, R., & Elias, C. (2010) · Arquivos brasileiros de endocrinologia e metabologia · doi:10.1590/s0004-27302010000700002 · Cited by 53
Roles of leptin and resistin in metabolism, reproduction, and leptin resistance
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A complex interaction pattern of CIS and SOCS2 with the leptin receptor
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The evidence of metabolic-improving effect of metformin in Ay/a mice with genetically-induced melanocortin obesity and the contribution of hypothalamic mechanisms to this effect
Derkach, K. V., Zakharova, I. O., Zorina, I. I., Bakhtyukov, A. A., Romanova, I. V., Bayunova, L. V., & Shpakov, A. O. (2019) · PLoS ONE · doi:10.1371/journal.pone.0213779 · Cited by 60
Ligand-Induced Architecture of the Leptin Receptor Signaling Complex
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“…a class I cytokine, is secreted from adipose tissue at levels that are proportional to body fat, and after crossing the blood-brain barrier it engages the leptin receptor (LEP-R) in order to modulate energy expenditure and food intake (Bates et al., 2003; Halaas et al., 1995; Morton et al., 2005).”
The proinflammatory cytokines IL‐1β and TNF‐α modulate corneal epithelial wound healing through p16Ink4a suppressing STAT3 activity
Wang, X., Zhang, S., Dong, M., Li, Y., Zhou, Q., & Yang, L. (2020) · Journal of Cellular Physiology · doi:10.1002/jcp.29823 · Cited by 60
“Signal transducer and activator of transcription 3 (STAT3) is a transcription factor that is activated by a variety of cytokines, such as the IL‐6 family of cytokines, epidermal growth factor, and leptin (Bates et al., 2003; Darnell, Kerr, & Stark, 1994; Johnson et al., 2018; Vaisse et al., 1996).”
Background
Evidence for Central Regulation of Glucose Metabolism
Carey, M., Kehlenbrink, S., & Hawkins, M. A. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.r113.506782 · Cited by 65
“2 subunit of the KATP channel (E23K variant) are at increased risk of developing T2DM over their lifetimes, although studies of E23K homozygotes with normal glucose tolerance raised an intriguing conundrum as these subjects appeared more insulin-sensitive than control subjects.”
BackgroundInfluential
Control of food intake and muscle wasting in cachexia
Amitani, M. S., Asakawa, A., Amitani, H., & Inui, A. (2013) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2013.07.016 · Cited by 62
Incendiary Leptin
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Enhancement of Bovine oocyte maturation by leptin is accompanied by an upregulation in mRNA expression of leptin receptor isoforms in cumulus cells
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“Furthermore, it has been suggested that leptin signaling through the STAT3 pathway is not required for reproduction since mice with disrupted ObR-b STAT3 signaling are obese yet fertile (Bates et al., 2003).”
Background
TNF-α Up-Regulates Protein Level and Cell Surface Expression of the Leptin Receptor by Stimulating Its Export via a PKC-Dependent Mechanism
Gan, L., Guo, K., Cremona, M. L., McGraw, T. E., Leibel, R. L., & Zhang, Y. (2012) · Endocrinology · doi:10.1210/en.2012-1510 · Cited by 59
Neuroendocrine Regulation of Metabolism
Cornejo, M. P., Hentges, S. T., Maliqueo, M. A., Coirini, H., Becú‐Villalobos, D., & Elias, C. F. (2016) · Journal of Neuroendocrinology · doi:10.1111/jne.12395 · Cited by 56
“Humans and mice with loss-of-function mutations in leptin (LEP/Lep) or leptin receptor (LEPR/Lepr) genes are obese and infertile (86–88).”
Suppression of food intake by Glp1r/Lepr-coexpressing neurons prevents obesity in mouse models
Rupp, A. C., Tomlinson, A. J., Affinati, A. H., Yacawych, W. T., Duensing, A. M., True, C., Lindsley, S. R., Kirigiti, M. A., MacKenzie, A., Polex-Wolf, J., et al. (2023) · Journal of Clinical Investigation · doi:10.1172/jci157515 · Cited by 55
“Indeed, not only do KO Glp1r mice exhibit normal energy expenditure (suggesting normal sympathetic tone and thyroid function), but also we routinely breed KO Glp1r mice (data not shown), which is not possible with KO mice (40).”
Self-citation
LRb signals act within a distributed network of leptin‐responsive neurones to mediate leptin action
Leinninger, G. M., & Myers, M. G. (2008) · Acta Physiologica · doi:10.1111/j.1748-1716.2007.01784.x · Cited by 56
“However, important differences exist between the phenotypes of s/s mice (missing only the LRb-STAT3 signal) and db/db mice (devoid of all leptin signals) (Bates et al. 2003).”
BackgroundInfluentialSelf-citation
Role of Leptin-Mediated Colonic Inflammation in Defense against Clostridium difficile Colitis
Madan, R., Guo, X., Naylor, C., Buonomo, E. L., Mackay, D., Noor, Z., CONCANNON, P. J., Scully, K. W., Pramoonjago, P., Kolling, G. L., et al. (2013) · Infection and Immunity · doi:10.1128/iai.00972-13 · Cited by 56
Leptin Receptors
Cottrell, E. C., & Mercer, J. G. (2011) · Handbook of experimental pharmacology · doi:10.1007/978-3-642-24716-3_1 · Cited by 56
Molecular connectomics reveals a glucagon-like peptide 1-sensitive neural circuit for satiety
Webster, A. N., Becker, J. J., Li, C., Schwalbe, D. C., Kerspern, D., Karolczak, E. O., Bundon, C. B., Onoharigho, R., Crook, M. E., Jalil, M., et al. (2024) · Nature Metabolism · doi:10.1038/s42255-024-01168-8 · Cited by 53
“To account for differences in cell responsiveness across tissue slices, we also calculated the percentage of responding cells per slice 58–60 .”
Molecular basis of insulin resistance: the role of IRS and Foxo1 in the control of diabetes mellitus and its complications
Guo, S. (2013) · Drug Discovery Today Disease Mechanisms · doi:10.1016/j.ddmec.2013.06.003 · Cited by 56
Phenotypic effects of an induced mutation of the ObRa isoform of the leptin receptor
Li, Z., Ceccarini, G., Eisenstein, M., Tan, K., & Friedman, J. M. (2013) · Molecular Metabolism · doi:10.1016/j.molmet.2013.07.007 · Cited by 58
“This conclusion is consistent with prior reports that point mutations in the C terminus of ObRb also interfere with leptin action [20–22].”
BackgroundResult
Deregulation of inflammatory response in the diabetic condition is associated with increased ischemic brain injury
Kim, E., Tolhurst, A. T., & Cho, S. (2014) · Journal of Neuroinflammation · doi:10.1186/1742-2094-11-83 · Cited by 56
Regulation of energy homeostasis by peripheral signals
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Anorexigenic Hormones Leptin, Insulin, and α-Melanocyte-Stimulating Hormone Directly Induce Neurotensin (NT) Gene Expression in Novel NT-Expressing Cell Models
Cui, H., Cai, F., & Belsham, D. D. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2269-05.2005 · Cited by 55
“This suggests that there is a STAT3-independent pathway, specifically used to control NPY neuron responsiveness to leptin (Bates et al., 2003), which may also mediate the response seen with NT. Alternatively, high levels of leptin may disrupt the signaling machinery leading to a response similar to…”
BackgroundInfluential
Neither Signal Transducer and Activator of Transcription 3 (STAT3) or STAT5 Signaling Pathways Are Required for Leptin's Effects on Fertility in Mice
Singireddy, A. V., Inglis, M. A., Zuure, W. A., Kim, J. S., & Anderson, G. M. (2013) · Endocrinology · doi:10.1210/en.2013-1109 · Cited by 54
Blockade of IL-6 signaling exacerbates liver injury and suppresses antiapoptotic gene expression in methionine choline-deficient diet-Fed db/db mice
Yamaguchi, K., Itoh, Y., Yokomizo, C., Nishimura, T., Niimi, T., Umemura, A., Fujii, H., Okanoue, T., & Yoshikawa, T. (2011) · Laboratory Investigation · doi:10.1038/labinvest.2011.2 · Cited by 55
Mechanistic insight into high-fat diet-induced metabolic inflammation in the arcuate nucleus of the hypothalamus
Ullah, R., Rauf, N., Nabi, G., Shen, Y., Yu-Dong, Z., & Fu, J. (2021) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2021.112012 · Cited by 64
Control of T Cell Metabolism by Cytokines and Hormones
Bishop, E. L., Gudgeon, N. H., & Dimeloe, S. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.653605 · Cited by 56
Hypothalamic endoplasmic reticulum stress as a key mediator of obesity‐induced leptin resistance
Ye, Z., Liu, G., Guo, J., & Su, Z. (2018) · Obesity Reviews · doi:10.1111/obr.12673 · Cited by 54
“anti-obesity effect of leptin by suppressing appetite and enhancing energy expenditure (119).”
Background
Organizational actions of metabolic hormones
Bouret, S. G. (2013) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2013.01.001 · Cited by 52
“Although LepRb ? pSTAT3 represents a crucial mediator of leptin action on energy balance in mature animals (Bates et al., 2003), this signaling pathway is not solely required to mediate the neurodevelopmental action of leptin.”
Hormonal Gut–Brain Signaling for the Treatment of Obesity
Roh, E., & Choi, K. M. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24043384 · Cited by 61
“Leptin stimulates the transcriptional activity of POMC, whereas the dominant negative expression of STAT3 suppresses this activity, indicating that LepRb–STAT3 signaling mediates the effects of leptin on energy metabolism [47].”
BackgroundInfluential
Endogenous leptin receptor signaling in the medial nucleus tractus solitarius affects meal size and potentiates intestinal satiation signals
Kanoski, S. E., Zhao, S., Guarnieri, D. J., Dileone, R., Yan, J., Jonghe, B. C. D., Bence, K. K., Hayes, M. R., & Grill, H. J. (2012) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00205.2012 · Cited by 52
“Leptin-induced activation of signal transducer and activator of transcription 3 (pSTAT3), a transcription factor critical in the LepRb-mediated control of energy balance (1), is substantially more robust in the mNTS than in the AP (25, 35, 39).”
Background
Oestradiol and Diet Modulate Energy Homeostasis and Hypothalamic Neurogenesis in the Adult Female Mouse
Bless, E. P., Reddy, T. P., Acharya, K. D., Beltz, B. S., & Tetel, M. J. (2014) · Journal of Neuroendocrinology · doi:10.1111/jne.12206 · Cited by 49
Goldfish Leptin-AI and Leptin-AII: Function and Central Mechanism in Feeding Control
Yan, A., Chen, T., Chen, S., Chun-hua, R. E. N., Hu, C.-Q., Cai, Y.-M., Liu, F., & Tang, D. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17060783 · Cited by 51
“A study in tilapia showed that mouse leptin cannot promote STAT-3 signaling in the tilapia lepR-transfected COS7 cells, and STAT-3 signaling is necessary for leptin regulation of appetite [41].”
Background

Authors: Bates, S. H., Stearns, W. H., Dundon, T. A., Schubert, M., Tso, A. W. K., Wang, Y., Banks, A. S., Lavery, H. J., Haq, A. K., Maratos-Flier, E., Neel, B. G., Schwartz, M. W., & Myers, M. G.
Affiliations: Joslin Diabetes Center (US)
Beth Israel Deaconess Medical Center (US)
University of Washington (US)
Corresponding author: Myers, Martin G.
ORCID: Schubert, Markus
Wang, Yongping
Banks, Alexander S.
Lavery, Hugh J.
Neel, Benjamin G.
Schwartz, Michael W.
Myers, Martin G.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2003-02
Volume: 421
Issue: 6925
Pages: 856-859
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature01388
OpenAlex: W2103270369
Semantic Scholar: 25ab9d73ec0d0c8fc3c6ec167cccbfe002d52c52
Cited by: 1,010
References: 25
Citations by year: 2026: 12 · 2025: 14 · 2024: 19 · 2023: 21 · 2022: 34 · 2021: 35 · 2020: 50 · 2019: 32 · 2018: 46 · 2017: 35 · 2016: 48 · 2015: 52 · 2014: 66 · 2013: 67 · 2012: 54
FWCI: 20.53
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
RePEc: Research Papers in Economics (submittedVersion)
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 › Reproductive Medicine › Hypothalamic control of reproductive hormones
Keywords: STAT3 signaling, leptin, leptin receptor, energy homeostasis, obesity, fertility, neuropeptide Y, melanocortin system, hypothalamus, glucose homeostasis, db/db mice, hyperphagia, insulin resistance
MeSH terms: Alleles, alpha-MSH, Animals, Blood Glucose, Body Weight, Cell Line, Diabetes Mellitus, DNA-Binding Proteins, Energy Metabolism, Female, Homeostasis, Humans, Infertility, Male, Neuropeptide Y, Obesity, Phenotype, Receptors, Cell Surface, Reproduction, RNA, Messenger, Signal Transduction, Trans-Activators, Leptin, Estrous Cycle, STAT3 Transcription Factor, Mice, Receptors, Leptin

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STAT3 signalling is required for leptin regulation of energy balance but not reproduction

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