Glucagon-like peptide-1 control of GnRH secretion in female sheep

in Journal of Endocrinology
Authors:
Leila Arbabi Neuroscience Program, Monash Biomedicine Discovery Institute and Department of Physiology, Monash University, Melbourne, Victoria, Australia

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Qun Li Neuroscience Program, Monash Biomedicine Discovery Institute and Department of Physiology, Monash University, Melbourne, Victoria, Australia

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Belinda A Henry Metabolism, Diabetes and Obesity Program, Monash Biomedicine Discovery Institute and Department of Physiology, Monash University, Melbourne, Victoria, Australia

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Iain J Clarke Neuroscience Program, Monash Biomedicine Discovery Institute and Department of Physiology, Monash University, Melbourne, Victoria, Australia

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Correspondence should be addressed to I J Clarke: iain.clarke@monash.edu

†(I J Clarke is now at Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Parkville, Victoria, Australia)

DOI:
https://doi.org/10.1530/JOE-20-0335
Volume/Issue:
Volume 248: Issue 3
Article Type:
Research Article
Page Range:
325–335
Online Publication Date:
Mar 2021
Copyright:
© 2021 Society for Endocrinology 2021
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The role of glucagon-like peptide-1 (GLP-1) on gonadotropin-releasing hormone (GnRH) secretion was investigated in ovariectomised (OVX) ewes, in which GnRH and luteinising hormone (LH) secretion had been restrained by treatment with oestrogen and progesterone. Guide tubes for microinjection were placed above the median eminence (ME) and the animals were allowed to recover for 1 month. Jugular venous blood samples were taken via cannulae at 10 min intervals. Vehicle (50 nL) was injected into the ME at 2 h, followed by injection of GLP-1 ((7-36)-amide – 0.5 or 1 nmol) or its receptor agonist, exendin-4 (0.5 nmol) at 4 h (n = 5). Plasma LH levels were quantified as a surrogate measure of GnRH secretion. GLP-1 microinjection into the ME elicited a large amplitude LH pulse in jugular plasma, the effect was greater at the higher dose. Exendin-4 microinjection caused a large, sustained increase in plasma LH levels. To determine how GLP-1 might exert an effect on GnRH secretion, we employed double labelled in situ hybridisation, with RNAScope, for co-localisation of the GLP-1 receptor (GLP-1R) in GnRH, Kisspeptin and NPY cells in the hypothalami of three ewes in the luteal phase of the estrous cycle. GLP1R expression was clearly visible but the receptor was not expressed in GNRH1 or NPY expressing neurons and was visualised in <5% of KISS1 expressing neurons. We conclude that GLP-1 may act at the level of the secretory terminals of GnRH neurons in the ME to stimulate GnRH secretion, the pathway through which such effect is manifested remains unknown.

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Print ISSN:
0022-0795
Online ISSN:
1479-6805
Copyright:
© 2021 Society for Endocrinology 2021
Page(s):
11
Article Type:
Research Article
Received Date:
22 Dec 2020
Accepted Date:
12 Jan 2020
Print Publication Date:
01 Mar 2021
Online Publication Date:
Mar 2021
Keywords:
glucagon-like peptide-1; gonadotropin-releasing hormone; hypothalamus; sheep

  • Alvarez E, Martínez MD, Roncero I, Chowen JA, García‐Cuartero B, Gispert JD, Sanz C, Vázquez P, Maldonado A, De Cáceres Jet al. 2005 The expression of GLP‐1 receptor mRNA and protein allows the effect of GLP‐1 on glucose metabolism in the human hypothalamus and brainstem. Journal of Neurochemistry 92 798–806. (https://doi.org/10.1111/j.1471-4159.2004.02914.x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ast J, Arvaniti A, Fine NHF, Nasteska D, Ashford FB, Stamataki Z, Koszegi Z, Bacon A, Jones BJ & Lucey MA et al. 2020 Super-resolution microscopy compatible fluorescent probes reveal endogenous glucagon-like peptide-1 receptor distribution and dynamics. Nature Communications 11 467. (https://doi.org/10.1038/s41467-020-14309-w)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Balland E, Dam J, Langlet F, Caron E, Steculorum S, Messina A, Rasika S, Falluel-Morel A, Anouar Y & Dehouck B et al. 2014 Hypothalamic tanycytes are an ERK-gated conduit for leptin into the brain. Cell Metabolism 19 293–301. (https://doi.org/10.1016/j.cmet.2013.12.015)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Barker-Gibb ML & Clarke IJ 2000 Effect of season on neuropeptide Y and galanin within the hypothalamus of the ewe in relation to plasma luteinizing hormone concentrations and the breeding season: an immunohistochemical analysis. Journal of Neuroendocrinology 12 618–626. (https://doi.org/10.1046/j.1365-2826.2000.00514.x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Beak SA, Heath MM, Small CJ, Morgan DG, Ghatei MA, Taylor AD, Buckingham JC, Bloom SR & Smith DM 1998 Glucagon-like peptide-1 stimulates luteinizing hormone-releasing hormone secretion in a rodent hypothalamic neuronal cell line. Journal of Clinical Investigation 101 1334–1341. (https://doi.org/10.1172/JCI610)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Burger HG, Lee VW & Rennie GC 1972 A generalized computer program for the treatment of data front competitive protein-binding assays including radioimmunoassays. Journal of Laboratory and Clinical Medicine 80 302–312.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Clarke IJ 2014 Interface between metabolic balance and reproduction in ruminants: focus on the hypothalamus and pituitary. Hormones and Behavior 66 15–40. (https://doi.org/10.1016/j.yhbeh.2014.02.005)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Clarke IJ 2015 Hypothalamus as an endocrine organ. Comprehensive Physiology 5 217–253. (https://doi.org/10.1002/cphy.c140019)

  • Clarke IJ & Cummins JT 1982 The temporal relationship between gonadotropin releasing hormone (GnRH) and luteinizing hormone (LH) secretion in ovariectomized ewes. Endocrinology 111 1737–1739. (https://doi.org/10.1210/endo-111-5-1737)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Clarke IJ, Campbell R, Smith JT, Prevot V & Wray S 2012 Neuroendocrine control of reproduction. In Handbook of Neuroendocrinology, pp. 197–235. Amsterdam, Netherlands: Elsevier. (https://doi.org/10.1016/B978-0-12-375097-6.10009-5)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • D’Alessio D, Lu W, Sun W, Zheng S, Yang Q, Seeley R, Woods SC & Tso P 2007 Fasting and postprandial concentrations of GLP-1 in intestinal lymph and portal plasma: evidence for selective release of GLP-1 in the lymph system. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology 293 R2163–R 2169. (https://doi.org/10.1152/ajpregu.00911.2006)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • d’Anglemont de Tassigny X, Fagg LA, Carlton MB & Colledge WH 2008 Kisspeptin can stimulate gonadotropin-releasing hormone (GnRH) release by a direct action at GnRH nerve terminals. Endocrinology 149 3926–3932. (https://doi.org/10.1210/en.2007-1487)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Dar MS, Chapman 3rd WH, Pender JR, Drake 3rd AJ, O’Brien K, Tanenberg RJ, Dohm GL & Pories WJ 2012 GLP-1 response to a mixed meal: what happens 10 years after Roux-en-Y gastric bypass (RYGB)? Obesity Surgery 22 1077–1083. (https://doi.org/10.1007/s11695-012-0624-1)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Deacon CF, Nauck MA, Toft-Nielsen M, Pridal L, Willms B & Holst JJ 1995 Both subcutaneously and intravenously administered glucagon-like peptide I are rapidly degraded from the NH2-terminus in type II diabetic patients and in healthy subjects. Diabetes 44 1126–1131. (https://doi.org/10.2337/diab.44.9.1126)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Doyle ME & Egan JM 2007 Mechanisms of action of glucagon-like peptide 1 in the pancreas. Pharmacology and Therapeutics 113 546–593. (https://doi.org/10.1016/j.pharmthera.2006.11.007)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Drucker DJ & Nauck MA 2006 The incretin system: glucagon-like peptide-1 receptor agonists and dipeptidyl peptidase-4 inhibitors in type 2 diabetes. Lancet 368 1696–1705. (https://doi.org/10.1016/S0140-6736(06)69705-5)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ezzat A, Pereira A & Clarke IJ 2015 Kisspeptin is a component of the pulse generator for GnRH secretion in female sheep but not the pulse generator. Endocrinology 156 1828–1837. (https://doi.org/10.1210/en.2014-1756)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Farkas I, Vastagh C, Farkas E, Balint F, Skrapits K, Hrabovszky E, Fekete C & Liposits Z 2016 Glucagon-like peptide-1 excites firing and increases GABAergic miniature postsynaptic currents (mPSCs) in gonadotropin-releasing hormone (GnRH) neurons of the male mice via activation of nitric oxide (NO) and suppression of endocannabinoid signaling pathways. Frontiers in Cellular Neuroscience 10 214. (https://doi.org/10.3389/fncel.2016.00214)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Garcia-Caceres C, Balland E, Prevot V, Luquet S, Woods SC, Koch M, Horvath TL, Yi CX, Chowen JA & Verkhratsky A et al. 2019 Role of astrocytes, microglia, and tanycytes in brain control of systemic metabolism. Nature Neuroscience 22 7–14. (https://doi.org/10.1038/s41593-018-0286-y)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Garcia-Segura LM, Lorenz B & DonCarlos LL 2008 The role of glia in the hypothalamus: implications for gonadal steroid feedback and reproductive neuroendocrine output. Reproduction 135 419–429. (https://doi.org/10.1530/REP-07-0540)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Goke R, Larsen PJ, Mikkelsen JD & Sheikh SP 1995 Distribution of GLP-1 binding sites in the rat brain: evidence that exendin-4 is a ligand of brain GLP-1 binding sites. European Journal of Neuroscience 7 2294–2300. (https://doi.org/10.1111/j.1460-9568.1995.tb00650.x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Goodman RL, Legan SJ, Ryan KD, Foster DL & Karsch FJ 1980 Two effects of estradiol that normally contribute to the control of tonic LH secretion in the ewe. Biology of Reproduction 23 415–422. (https://doi.org/10.1095/biolreprod23.2.415)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hamra AH, Massri YG, Marcek JM & Wheaton JE 1986 Plasma progesterone levels in ewes treated with progesterone-controlled internal drug-release dispensers, implants and sponges. Animal Reproduction Science 11 187–194. (https://doi.org/10.1016/0378-4320(86)90120-X)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Han VK, Hynes MA, Jin C, Towle AC, Lauder JM & Lund PK 1986 Cellular localization of proglucagon/glucagon-like peptide I messenger RNAs in rat brain. Journal of Neuroscience Research 16 97–107. (https://doi.org/10.1002/jnr.490160110)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Henry BA, Goding JW, Tilbrook AJ, Dunshea FR & Clarke IJ 2001 Intracerebroventricular infusion of leptin elevates the secretion of luteinising hormone without affecting food intake in long-term food-restricted sheep, but increases growth hormone irrespective of bodyweight. Journal of Endocrinology 168 67–77. (https://doi.org/10.1677/joe.0.1680067)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Heppner KM, Baquero AF, Bennett CM, Lindsley SR, Kirigiti MA, Bennett B, Bosch MA, Mercer AJ, Ronnekleiv OK & True C et al. 2017 GLP-1R signaling directly activates arcuate nucleus kisspeptin action in brain slices but does not rescue luteinizing hormone inhibition in ovariectomized mice During negative energy balance. Eneuro 4 ENEURO.0198-16.2016. (https://doi.org/10.1523/ENEURO.0198-16.2016)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Herde MK, Iremonger KJ, Constantin S & Herbison AE 2013 GnRH neurons elaborate a long-range projection with shared axonal and dendritic functions. Journal of Neuroscience 33 12689–12697. (https://doi.org/10.1523/JNEUROSCI.0579-13.2013)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Holst JJ 2007 The physiology of glucagon-like peptide 1. Physiological Reviews 87 1409–1439. (https://doi.org/10.1152/physrev.00034.2006)

  • Iremonger KJ, Porteous R & Herbison AE 2017 Spike and neuropeptide-dependent mechanisms control GnRH neuron nerve terminal Ca(2+) over diverse time scales. Journal of Neuroscience 37 3342–3351. (https://doi.org/10.1523/JNEUROSCI.2925-16.2017)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Jeibmann A, Zahedi S, Simoni M, Nieschlag E & Byrne MM 2005 Glucagon‐like peptide‐1 reduces the pulsatile component of testosterone secretion in healthy males. European Journal of Clinical Investigation 35 565–572. (https://doi.org/10.1111/j.1365-2362.2005.01542.x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Jin SL, Han VK, Simmons JG, Towle AC, Lauder JM & Lund PK 1988 Distribution of glucagonlike peptide I (GLP‐I), glucagon, and glicentin in the rat brain: an immunocytochemical study. Journal of Comparative Neurology 271 519–532. (https://doi.org/10.1002/cne.902710405)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Karsch FJ, Cummins JT, Thomas GB & Clarke IJ 1987 Steroid feedback inhibition of pulsatile secretion of gonadotropin-releasing hormone in the ewe. Biology of Reproduction 36 1207–1218. (https://doi.org/10.1095/biolreprod36.5.1207)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Katsurada K, Maejima Y, Nakata M, Kodaira M, Suyama S, Iwasaki Y, Kario K & Yada T 2014 Endogenous GLP-1 acts on paraventricular nucleus to suppress feeding: projection from nucleus tractus solitarius and activation of corticotropin-releasing hormone, nesfatin-1 and oxytocin neurons. Biochemical and Biophysical Research Communications 451 276–281. (https://doi.org/10.1016/j.bbrc.2014.07.116)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kreymann B, Ghatei MA, Burnet P, Williams G, Kanse S, Diani AR & Bloom SR 1989 Characterization of glucagon-like peptide-1-(7–36) amide in the hypothalamus. Brain Research 502 325–331. (https://doi.org/10.1016/0006-8993(89)90628-8)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Larsen PJ, Tang-Christensen M, Holst JJ & Orskov C 1997 Distribution of glucagon-like peptide-1 and other preproglucagon-derived peptides in the rat hypothalamus and brainstem. Neuroscience 77 257–270. (https://doi.org/10.1016/s0306-4522(96)00434-4)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Lee VW, Cumming IA, De Kretser DM, Findlay JK, Hudson B & Keogh EJ 1976 Regulation of gonadotrophin secretion in rams from birth to sexual maturity. I. Plasma LH, FSH and testosterone levels. Journal of Reproduction and Fertility 46 1–6. (https://doi.org/10.1530/jrf.0.0460001)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Liu H, Schultz CG, De Blasio MJ, Peura AM, Heinemann GK, Harryanto H, Hunter DS, Wooldridge AL, Kind KL & Giles LC et al. 2015 Effect of placental restriction and neonatal exendin-4 treatment on postnatal growth, adult body composition, and in vivo glucose metabolism in the sheep. American Journal of Physiology: Endocrinology and Metabolism 309 E589–E600. (https://doi.org/10.1152/ajpendo.00487.2014)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Llewellyn-Smith IJ, Reimann F, Gribble FM & Trapp S 2011 Preproglucagon neurons project widely to autonomic control areas in the mouse brain. Neuroscience 180 111–121. (https://doi.org/10.1016/j.neuroscience.2011.02.023)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • MacLusky NJ, Cook S, Scrocchi L, Shin J, Kim J, Vaccarino F, Asa SL & Drucker DJ 2000 Neuroendocrine function and response to stress in mice with complete disruption of glucagon-like Peptide-1 receptor signaling. Endocrinology 141 752–762. (https://doi.org/10.1210/endo.141.2.7326)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mojsov S, Heinrich G, Wilson IB, Ravazzola M, Orci L & Habener JF 1986 Preproglucagon gene expression in pancreas and intestine diversifies at the level of post-translational processing. Journal of Biological Chemistry 261 11880–11889. (https://doi.org/10.1016/S0021-9258(18)67324-7)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Moore AM, Prescott M, Czieselsky K, Desroziers E, Yip SH, Campbell RE & Herbison AE 2018 Synaptic innervation of the GnRH neuron distal dendron in female mice. Endocrinology 159 3200–3208. (https://doi.org/10.1210/en.2018-00505)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ogilvie KM, Held Hales K, Roberts ME, Hales DB & Rivier C 1999 The inhibitory effect of intracerebroventricularly injected interleukin 1beta on testosterone secretion in the rat: role of steroidogenic acute regulatory protein. Biology of Reproduction 60 527–533. (https://doi.org/10.1095/biolreprod60.2.527)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Outeirino-Iglesias V, Romani-Perez M, Gonzalez-Matias LC, Vigo E & Mallo F 2015 GLP-1 increases preovulatory LH source and the number of mature follicles, as well as synchronizing the onset of puberty in female rats. Endocrinology 156 4226–4237. (https://doi.org/10.1210/en.2014-1978)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Outeiriño-Iglesias V, Romaní-Pérez M, González-Matías LC, Vigo E & Mallo F 2015 GLP-1 increases pre-ovulatory LH source and the number of mature follicles, as well as synchronizing the onset of puberty in female rats. Endocrinology 156 2014–1978.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Prevot V, Dehouck B, Sharif A, Ciofi P, Giacobini P & Clasadonte J 2018 The versatile tanycyte: a hypothalamic integrator of reproduction and energy metabolism. Endocrine Reviews 39 333–368. (https://doi.org/10.1210/er.2017-00235)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Relling AE, Reynolds CK & Loerch SC 2011 Effect of feeding fat or intrajugular infusion of glucagon-like peptide-1 and cholecystokinin on dry matter intake, digestibility, and digesta rate of passage in growing wethers. Journal of Animal Science 89 168–178. (https://doi.org/10.2527/jas.2010-2976)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Renner E, Puskas N, Dobolyi A & Palkovits M 2012 Glucagon-like peptide-1 of brainstem origin activates dorsomedial hypothalamic neurons in satiated rats. Peptides 35 14–22. (https://doi.org/10.1016/j.peptides.2012.02.018)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Richards P, Parker HE, Adriaenssens AE, Hodgson JM, Cork SC, Trapp S, Gribble FM & Reimann F 2014 Identification and characterization of GLP-1 receptor-expressing cells using a new transgenic mouse model. Diabetes 63 1224–1233. (https://doi.org/10.2337/db13-1440)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Runge S, Schimmer S, Oschmann J, Schiodt CB, Knudsen SM, Jeppesen CB, Madsen K, Lau J, Thogersen H & Rudolph R 2007 Differential structural properties of GLP-1 and exendin-4 determine their relative affinity for the GLP-1 receptor N-terminal extracellular domain. Biochemistry 46 5830–5840. (https://doi.org/10.1021/bi062309m)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Sandoval DA & D’Alessio DA 2015 Physiology of proglucagon peptides: role of glucagon and GLP-1 in health and disease. Physiological Reviews 95 513–548. (https://doi.org/10.1152/physrev.00013.2014)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Secher A, Jelsing J, Baquero AF, Hecksher-Sorensen J, Cowley MA, Dalboge LS, Hansen G, Grove KL, Pyke C & Raun K et al. 2014 The arcuate nucleus mediates GLP-1 receptor agonist liraglutide-dependent weight loss. Journal of Clinical Investigation 124 4473–4488. (https://doi.org/10.1172/JCI75276)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Selvage DJ & Rivier C 2003 Importance of the paraventricular nucleus of the hypothalamus as a component of a neural pathway between the brain and the testes that modulates testosterone secretion independently of the pituitary. Endocrinology 144 594–598. (https://doi.org/10.1210/en.2002-220781)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Shimizu I, Hirota M, Ohboshi C & SHIMA K 1987 Identification and localization of glucagon-like peptide-1 and its receptor in rat brain. Endocrinology 121 1076–1082. (https://doi.org/10.1210/endo-121-3-1076)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Small CJ, Stanley SA & Bloom SR 2002 Appetite control and reproduction: leptin and beyond. Seminars in Reproductive Medicine 20 389–398. (https://doi.org/10.1055/s-2002-36712)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Smith JT, Clay CM, Caraty A & Clarke IJ 2007 KiSS-1 messenger ribonucleic acid expression in the hypothalamus of the ewe is regulated by sex steroids and season. Endocrinology 148 1150–1157. (https://doi.org/10.1210/en.2006-1435)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Smith JT, Li Q, Pereira A & Clarke IJ 2009 Kisspeptin neurons in the ovine arcuate nucleus and preoptic area are involved in the preovulatory luteinizing hormone surge. Endocrinology 150 5530–5538. (https://doi.org/10.1210/en.2009-0712)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Timper K, Del Rio-Martin A, Cremer AL, Bremser S, Alber J, Giavalisco P, Varela L, Heilinger C, Nolte H & Trifunovic A et al. 2020 GLP-1 receptor signaling in astrocytes regulates fatty acid oxidation, mitochondrial integrity, and function. Cell Metabolism 31 1189 .e13–1205.e13. (https://doi.org/10.1016/j.cmet.2020.05.001)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Turton MD, O’shea D, Gunn I, Beak SA, Edwards CM, Meeran K, Choi SJ, Taylor GM, Heath MM & Lambert PD et al. 1996 A role for glucagon-like peptide-1 in the central regulation of feeding. Nature 379 69–72. (https://doi.org/10.1038/379069a0)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Yun SP, Kam TI, Panicker N, Kim S, Oh Y, Park JS, Kwon SH, Park YJ, Karuppagounder SS & Park H et al. 2018 Block of A1 astrocyte conversion by microglia is neuroprotective in models of Parkinson’s disease. Nature Medicine 24 931–938. (https://doi.org/10.1038/s41591-018-0051-5)

    • PubMed
    • Search Google Scholar
    • Export Citation