Distribution and characterisation of Glucagon-like peptide-1 receptor expressing cells in the mouse brain

Molecular Metabolism

Volumn 4, Issue 10, 2015, Pages 718-731

  Cork, Simon C ^a   Richards, James E ^a   Holt, Marie K ^a   Gribble, Fiona M ^b   Reimann, Frank ^b   Trapp, Stefan ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Channelrhodopsin; Electrophysiology; GLP 1; Glucagon like peptide 1 receptor; PPG; Preproglucagon

Indexed keywords

CAPSID PROTEIN; CRE RECOMBINASE; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; INCRETIN; PARVALBUMIN; PREPROGLUCAGON;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; BRAIN CORTEX; CATECHOLAMINERGIC SYSTEM; CIRCUMVENTRICULAR ORGAN; CONTROLLED STUDY; HIPPOCAMPUS; HYPOTHALAMUS NUCLEUS; IMMUNOCOMPETENT CELL; IN VIVO STUDY; MOUSE; NONHUMAN; PARAVENTRICULAR THALAMIC NUCLEUS; PATCH CLAMP TECHNIQUE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; ROSTRAL VENTROLATERAL MEDULLA; SOLITARY TRACT NUCLEUS; VIRAL GENE DELIVERY SYSTEM;

EID: 84942198303     PISSN: None     EISSN: 22128778     Source Type: Journal    
DOI: 10.1016/j.molmet.2015.07.008     Document Type: Article

References (48)

1. Llewellyn-Smith I.J., Reimann F., Gribble F.M., Trapp S. Preproglucagon neurons project widely to autonomic control areas in the mouse brain. Neuroscience 2011, 180:111-121.
2. Hisadome K., Reimann F., Gribble F.M., Trapp S. Leptin directly depolarizes preproglucagon neurons in the nucleus tractus solitarius: electrical properties of glucagon-like peptide 1 neurons. Diabetes 2010, 59:1890-1898.
3. Trapp S., Richards J.E. The gut hormone glucagon-like peptide-1 produced in brain: is this physiologically relevant?. Current Opinion in Pharmacology 2013, 13:964-969.
4. Vrang N., Larsen P.J. Preproglucagon derived peptides GLP-1, GLP-2 and oxyntomodulin in the CNS: role of peripherally secreted and centrally produced peptides. Progress in Neurobiology 2010, 92:442-462.
5. Turton M.D., O'Shea D., Gunn I., Beak S.A., Edwards C.M., Meeran K., et al. A role for glucagon-like peptide-1 in the central regulation of feeding. Nature 1996, 379:69-72.
6. During M.J., Cao L., Zuzga D.S., Francis J.S., Fitzsimons H.L., Jioa X., et al. Glucagon-like peptide-1 receptor is involved in learning and neuroprotection. Nature Medicine 2003, 1173-1179.
7. Yamamoto H., Lee C.E., Marcus J.N., Williams T.D., Overton J.M., Lopez M.E., et al. Glucagon-like peptide-1 receptor stimulation increases blood pressure and heart rate and activates autonomic regulatory neurons. The Journal of Clinical Investigation 2002, 110:43-52.
8. Cabou C., Campistron G., Marsollier N., Leloup C., Cruciani-Guglielmacci C., Penicaud L., et al. Brain glucagon-like peptide-1 regulates arterial blood flow, heart rate, and insulin sensitivity. Diabetes 2008, 57:2577-2587.
9. Lockie S.H., Heppner K.M., Chaudhary N., Chabenne J.R., Morgan D.A., Veyrat-Durebex C., et al. Direct control of brown adipose tissue thermogenesis by central nervous system glucagon-like peptide-1 receptor signaling. Diabetes 2012, 61:2753-2762.
10. Dickson S.L., Shirazi R.H., Hansson C., Bergquist F., Nissbrandt H., Skibicka K.P. The glucagon-like peptide 1 (GLP-1) analogue, exendin-4, decreases the rewarding value of food: a new role for mesolimbic GLP-1 receptors. Journal of Neuroscience 2012, 32:4812-4820.
11. Mietlicki-Baase E.G., Ortinski P.I., Rupprecht L.E., Olivos D.R., Alhadeff A.L., Pierce R.C., et al. The food intake-suppressive effects of glucagon-like peptide-1 receptor signaling in the ventral tegmental area are mediated by AMPA/kainate receptors. American Journal of Physiology, Endocrinology and Metabolism 2013, 305:E1367-1374.
12. Mietlicki-Baase E.G., Ortinski P.I., Reiner D.J., Sinon C.G., McCutcheon J.E., Pierce R.C., et al. Glucagon-like peptide-1 receptor activation in the nucleus accumbens core suppresses feeding by increasing glutamatergic AMPA/kainate signaling. The Journal of Neuroscience 2014, 34:6985-6992.
13. Llewellyn-Smith I.J., Gnanamanickam G.J., Reimann F., Gribble F.M., Trapp S. Preproglucagon (PPG) neurons innervate neurochemically identified autonomic neurons in the mouse brainstem. Neuroscience 2013, 229:130-143.
14. Merchenthaler I., Lane M., Shughrue P. Distribution of pre-pro-glucagon and glucagon-like peptide-1 receptor messenger RNAs in the rat central nervous system. Journal of Comparative Neurology 1999, 403:261-280.
15. Heppner K.M., Kirigiti M., Secher A., Paulsen S.J., Buckingham R., Pyke C., et al. Expression and distribution of glucagon-like peptide-1 receptor mRNA, protein and binding in the male nonhuman primate (Macaca mulatta) brain. Endocrinology 2015, 156:255-267.
16. Richards P., Parker H.E., Adriaenssens A.E., Hodgson J.M., Cork S.C., Trapp S., et al. Identification and characterization of GLP-1 receptor-expressing cells using a new transgenic mouse model. Diabetes 2014, 63:1224-1233.
17. Luche H., Weber O., Nageswara Rao T., Blum C., Fehling H.J. Faithful activation of an extra-bright red fluorescent protein in "knock-in" Cre-reporter mice ideally suited for lineage tracing studies. European Journal of Immunology 2007, 37:43-53.
18. Murray A.J., Sauer J.F., Riedel G., McClure C., Ansel L., Cheyne L., et al. Parvalbumin-positive CA1 interneurons are required for spatial working but not for reference memory. Nature Neuroscience 2011, 14:297-299.
19. Yamamoto H., Kishi T., Lee C.E., Choi B.J., Fang H., Hollenberg A.N., et al. Glucagon-like peptide-1-responsive catecholamine neurons in the area postrema link peripheral glucagon-like peptide-1 with central autonomic control sites. The Journal of Neuroscience 2003, 23:2939-2946.
20. Llewellyn-Smith I.J., Marina N., Manton R.N., Reimann F., Gribble F.M., Trapp S. Spinally projecting preproglucagon axons preferentially innervate sympathetic preganglionic neurons. Neuroscience 2015, 284:872-887.
21. Drucker D.J. Incretin action in the pancreas: potential promise, possible perils, and pathological pitfalls. Diabetes 2013, 62:3316-3323.
22. Aroor A., Nistala R. Tissue-specific expression of GLP1R in Mice: Is the problem of antibody nonspecificity solved?. Diabetes 2014, 63:1182-1184.
23. Larsen P.J., Tang-Christensen M., Holst J.J., Orskov C. Distribution of glucagon-like peptide-1 and other preproglucagon-derived peptides in the rat hypothalamus and brainstem. Neuroscience 1997, 77:257-270.
24. Tauchi M., Zhang R., D'Alessio D.A., Stern J.E., Herman J.P. Distribution of glucagon-like peptide-1 immunoreactivity in the hypothalamic paraventricular and supraoptic nuclei. Journal of Chemical Neuroanatomy 2008, 36:144-149.
25. Alhadeff A.L., Rupprecht L.E., Hayes M.R. GLP-1 neurons in the nucleus of the solitary tract project directly to the ventral tegmental area and nucleus accumbens to control for food intake. Endocrinology 2012, 153:647-658.
26. Vrang N., Grove K. The brainstem preproglucagon system in a non-human primate (Macaca mulatta). Brain Research 2011, 1397:28-37.
27. Zheng H., Cai L., Rinaman L. Distribution of glucagon-like peptide 1-immunopositive neurons in human caudal medulla. Brain Structure & Function 2015, 220:1213-1219.
28. Sandoval D.A., Bagnol D., Woods S.C., D'Alessio D.A., Seeley R.J. Arcuate glucagon-like peptide 1 receptors regulate glucose homeostasis but not food intake. Diabetes 2008, 57:2046-2054.
29. Sisley S., Gutierrez-Aguilar R., Scott M., D'Alessio D.A., Sandoval D.A., Seeley R.J. Neuronal GLP1R mediates liraglutide's anorectic but not glucose-lowering effect. Journal of Clinical Investigation 2014, 124:2456-2463.
30. Knauf C., Cani P.D., Kim D.H., Iglesias M.A., Chabo C., Waget A., et al. Role of central nervous system glucagon-like Peptide-1 receptors in enteric glucose sensing. Diabetes 2008, 57:2603-2612.
31. Harasta A.E., Power J.M., von Jonquieres G., Karl T., Drucker D.J., Housley G.D., et al. Septal Glucagon-Like Peptide 1 Receptor Expression Determines Suppression of Cocaine-Induced Behavior. Neuropsychopharmacology 2015, 40:1969-1978.
32. Gu G., Roland B., Tomaselli K., Dolman C.S., Lowe C., Heilig J.S. Glucagon-like peptide-1 in the rat brain: distribution of expression and functional implication. Journal of Comparative Neurology 2013, 521:2235-2261.
33. Beiroa D., Imbernon M., Gallego R., Senra A., Herranz D., Villarroya F., et al. GLP-1 agonism stimulates brown adipose tissue thermogenesis and browning through hypothalamic AMPK. Diabetes 2014, 63:3346-3358.
34. Dossat A.M., Lilly N., Kay K., Williams D.L. Glucagon-like peptide 1 receptors in nucleus accumbens affect food intake. Journal of Neuroscience 2011, 31:14453-14457.
35. Dossat A.M., Diaz R., Gallo L., Panagos A., Kay K., Williams D.L. Nucleus accumbens GLP-1 receptors influence meal size and palatability. American Journal of Physiology - Endocrinology and Metabolism 2013, 304:E1314-E1320.
36. Alvarez E., Roncero I., Chowen J.A., Thorens B., Blazquez E. Expression of the glucagon-like peptide-1 receptor gene in rat brain. Journal of Neurochemistry 1996, 66:920-927.
37. Chowen J.A., de Fonseca F.R., Alvarez E., Navarro M., Garcia-Segura L.M., Blazquez E. Increased glucagon-like peptide-1 receptor expression in glia after mechanical lesion of the rat brain. Neuropeptides 1999, 33:212-215.
38. Gong N., Xiao Q., Zhu B., Zhang C.Y., Wang Y.C., Fan H., et al. Activation of spinal glucagon-like peptide-1 receptors specifically suppresses pain hypersensitivity. The Journal of Neuroscience 2014, 34:5322-5334.
39. Lovatt D., Nedergaard M. The astrocyte transcriptome. Neuroglia 2012, Oxford University Press. H. Kettenmann, B.R. Ransom (Eds.).
40. Luiten P.G., ter Horst G.J., Karst H., Steffens A.B. The course of paraventricular hypothalamic efferents to autonomic structures in medulla and spinal cord. Brain Research 1985, 329:374-378.
41. Larsen P.J., Moller M., Mikkelsen J.D. Efferent projections from the periventricular and medial parvicellular subnuclei of the hypothalamic paraventricular nucleus to circumventricular organs of the rat: a Phaseolus vulgaris-leucoagglutinin (PHA-L) tracing study. Journal of Comparative Neurology 1991, 306:462-479.
42. Geerling J.C., Shin J.W., Chimenti P.C., Loewy A.D. Paraventricular hypothalamic nucleus: axonal projections to the brainstem. Journal of Comparative Neurology 2010, 518:1460-1499.
43. Rogers R.C., Hermann G.E. Gastric-vagal solitary neurons excited by paraventricular nucleus microstimulation. Journal of the Autonomic Nervous System 1985, 14:351-362.
44. Oka J.I., Goto N., Kameyama T. Glucagon-like peptide-1 modulates neuronal activity in the rat's hippocampus. Neuroreport 1999, 10:1643-1646.
45. Hsu T.M., Hahn J.D., Konanur V.R., Lam A., Kanoski S.E. Hippocampal GLP-1 receptors influence food intake, meal size, and effort-based responding for food through volume transmission. Neuropsychopharmacology 2015, 40:327-337.
46. Goke R., Larsen P.J., Mikkelsen J.D., Sheikh S.P. 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 1995, 7:2294-2300.
47. Kieffer T.J., McIntosh C.H., Pederson R.A. Degradation of glucose-dependent insulinotropic polypeptide and truncated glucagon-like peptide 1 in vitro and in vivo by dipeptidyl peptidase IV. Endocrinology 1995, 136:3585-3596.
48. Zac-Varghese S., Trapp S., Richards P., Sayers S., Sun G., Bloom S.R., et al. The Peutz-Jeghers kinase LKB1 suppresses polyp growth from intestinal cells of a proglucagon-expressing lineage in mice. Disease Models & Mechanisms 2014, 7:1275-1286.