Glutamatergic phenotype of glucagon-like peptide 1 neurons in the caudal nucleus of the solitary tract in rats

Brain Structure and Function

Volumn 220, Issue 5, 2015, Pages 3011-3022

  Zheng, H ^a   Stornetta, R L ^b   Agassandian, K ^a   Rinaman, Linda ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Bed nucleus of the stria terminals; Confocal microscopy; Electron microscopy; Glutamate; In situ hybridization; Paraventricular nucleus of the hypothalamus; VGLUT2

Indexed keywords

GLUCAGON LIKE PEPTIDE 1; HYDROGEN PEROXIDE; VESICULAR GLUTAMATE TRANSPORTER; VESICULAR GLUTAMATE TRANSPORTER 2; GLUTAMIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY LABELING; ARTICLE; BRAIN REGION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRON MICROSCOPY; FLUORESCENCE IN SITU HYBRIDIZATION; GLUTAMATERGIC SYNAPSE; HYPOTHALAMUS; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; IN SITU HYBRIDIZATION; MALE; MICROSCOPY; NERVE CELL; NERVE ENDING; NONHUMAN; PARABRACHIAL NUCLEUS; PERIAQUEDUCTAL GRAY MATTER; PHASEOLUS VULGARIS; PHENOTYPE; PRIORITY JOURNAL; RAT; ROOM TEMPERATURE; SECRETORY CELL; ANIMAL; METABOLISM; NERVE TRACT; SOLITARY TRACT NUCLEUS; SPRAGUE DAWLEY RAT; SYNAPSE; SYNAPSE VESICLE;

ANIMALS; GLUCAGON-LIKE PEPTIDE 1; GLUTAMIC ACID; HYPOTHALAMUS; MALE; NEURAL PATHWAYS; NEURONS; PHENOTYPE; PRESYNAPTIC TERMINALS; RATS, SPRAGUE-DAWLEY; SOLITARY NUCLEUS; SYNAPSES; SYNAPTIC VESICLES;

EID: 84940579032     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-014-0841-6     Document Type: Article

References (63)

1. Acuna-Goycolea C, van den Pol A (2004) Glucagon-like peptide 1 excites hypocretin/orexin neurons by direct and indirect mechanisms: implications for viscera-mediated arousal. J Neurosci 24(37):8141–8152. doi:10.1523/JNEUROSCI.1607-04.2004
2. Crestani CC, Alves FH, Gomes FV, Resstel LB, Correa FM, Herman JP (2013) Mechanisms in the bed nucleus of the stria terminalis involved in control of autonomic and neuroendocrine functions: a review. Curr Neuropharmacol 11(2):141–159. doi:10.2174/1570159X11311020002
3. Donahey JC, van Dijk G, Woods SC, Seeley RJ (1998) Intraventricular GLP-1 reduces short- but not long-term food intake or body weight in lean and obese rats. Brain Res 779(1–2):75–83
4. Doyle S, Pyndiah S, De Gois S, Erickson JD (2010) Excitation-transcription coupling via calcium/calmodulin-dependent protein kinase/ERK1/2 signaling mediates the coordinate induction of VGLUT2 and Narp triggered by a prolonged increase in glutamatergic synaptic activity. J Biol Chem 285(19):14366–14376. doi:10.1074/jbc.M109.080069
5. El Mestikawy S, Wallen-Mackenzie A, Fortin GM, Descarries L, Trudeau LE (2011) From glutamate co-release to vesicular synergy: vesicular glutamate transporters. Nat Rev Neurosci 12(4):204–216. doi:10.1038/nrn2969
6. Flak JN, Ostrander MM, Tasker JG, Herman JP (2009) Chronic stress-induced neurotransmitter plasticity in the PVN. J Comp Neurol 517(2):156–165. doi:10.1002/cne.22142
7. Fremeau RT Jr, Troyer MD, Pahner I, Nygaard GO, Tran CH, Reimer RJ, Bellocchio EE, Fortin D, Storm-Mathisen J, Edwards RH (2001) The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 31(2):247–260
8. Griffin GD, Ferri-Kolwicz SL, Reyes BA, Van Bockstaele EJ, Flanagan-Cato LM (2010) Ovarian hormone-induced reorganization of oxytocin-labeled dendrites and synapses lateral to the hypothalamic ventromedial nucleus in female rats. J Comp Neurol 518(22):4531–4545. doi:10.1002/cne.22470
9. Gulpinar MA, Bozkurt A, Coskun T, Ulusoy NB, Yegen BC (2000) Glucagon-like peptide (GLP-1) is involved in the central modulation of fecal output in rats. Am J Physiol Gastrointest Liver Physiol 278:G924–G929
10. 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. J Neurosci Res 16(1):97–107. doi:10.1002/jnr.490160110
11. Hayashi M, Morimoto R, Yamamoto A, Moriyama Y (2003) Expression and localization of vesicular glutamate transporters in pancreatic islets, upper gastrointestinal tract, and testis. J Histochem Cytochem 51(10):1375–1390
12. Hayes MR (2012) Neuronal and intracellular signaling pathways mediating GLP-1 energy balance and glycemic effects. Physiol Behav 106(3):413–416. doi:10.1016/j.physbeh.2012.02.017
13. Herzog E, Gilchrist J, Gras C, Muzerelle A, Ravassard P, Giros B, Gaspar P, El Mestikawy S (2004) Localization of VGLUT3, the vesicular glutamate transporter type 3, in the rat brain. Neuroscience 123(4):983–1002
14. Johnson J, Sherry DM, Liu X, Fremeau RT Jr, Seal RP, Edwards RH, Copenhagen DR (2004) Vesicular glutamate transporter 3 expression identifies glutamatergic amacrine cells in the rodent retina. J Comp Neurol 477(4):386–398. doi:10.1002/cne.20250
15. Kaneko T, Fujiyama F, Hioki H (2002) Immunohistochemical localization of candidates for vesicular glutamate transporters in the rat brain. J Comp Neurol 444(1):39–62
16. Kinzig KP, D’Alessio DA, Herman JP, Sakai RR, Vahl TP, Figueiredo HF, Murphy EK, Seeley RJ (2003) CNS glucagon-like peptide-1 receptors mediate endocrine and anxiety responses to interoceptive and psychogenic stressors. J Neurosci 23(15):6163–6170
17. Larsen PJ, Tang-Christensen M, Holst JJ, Orskov C (1997a) Distribution of glucagon-like peptide-1 and other preproglucagon-derived peptides in rat hypothalamus and brainstem. Neuroscience 77(1):257–270
18. Larsen PJ, Tang-Christensen M, Jessop DS (1997b) Central administration of glucagon-like peptide-1 activates hypothalamic neuroendocrine neurons in the rat. Endocrinology 138(10):4445–4455
19. Liguz-Lecznar M, Skangiel-Kramska J (2007) Vesicular glutamate transporters (VGLUTs): the three musketeers of glutamatergic system. Acta Neurobiol Exp (Wars) 67(3):207–218
20. Maniscalco JW, Kreisler AD, Rinaman L (2012) Satiation and stress-induced hypophagia: examining the role of hindbrain neurons expressing prolactin-releasing peptide or glucagon-like peptide 1. Front Neurosci 6:199. doi:10.3389/fnins.2012.00199
21. Meeran K, O’Shea D, Edwards CMB, Turton MD, Heath MM, Gunn I, Abusnana S, Rossi M, Small CJ, Goldstone AP, Taylor GM, Sunter D, Steere J, Choi SJ, Ghatei MA, Bloom SR (1999) Repeated intracerebroventricular administration of glucagon-like peptide-1-(7-26) amide or exendin-(9-39) alters body weight in the rat. Endocrinology 140(1):244–250
22. Merchenthaler I, Lane M, Shughrue P (1999) Distribution of pre-pro-glucagon and glucagon-like peptide-1 receptor messenger RNAs in the rat central nervous system. J Comp Neurol 403(2):261–280
23. Mietlicki-Baase EG, Ortinski PI, Rupprecht LE, Olivos DR, Alhadeff AL, Pierce RC, Hayes MR (2013) The food intake-suppressive effects of glucagon-like peptide-1 receptor signaling in the ventral tegmental area are mediated by AMPA/kainate receptors. Am J Physiol Endocrinol Metab 305(11):E1367–E1374. doi:10.1152/ajpendo.00413.2013
24. Moller C, Sommer W, Thorsell A, Rimondini R, Heilig M (2002) Anxiogenic-like action of centrally administered glucagon-like peptide-1 in a punished drinking test. Prog Neuropsychopharmacol Bol Psychiatry 26(1):119–122
25. Moriyama Y, Yamamoto A (2004) Glutamatergic chemical transmission: look! Here, there, and anywhere. J Biochem 135(2):155–163
26. Myers B, Mark Dolgas C, Kasckow J, Cullinan WE, Herman JP (2013) Central stress-integrative circuits: forebrain glutamatergic and GABAergic projections to the dorsomedial hypothalamus, medial preoptic area, and bed nucleus of the stria terminalis. Brain Struct Funct. doi:10.1007/s00429-013-0566-y
27. Nakade Y, Tsukamoto K, Pappas TN, Takahashi T (2006) Central glucagon-like peptide 1 delays solid gastric emptying via central CRF and peripheral sympathetic pathways in rats. Brain Res 1111:117–121
28. Nakade Y, Tsukamoto K, Iwa M, Pappas TN, Takahashi T (2007) Glucagon-like peptide 1 accelerates colonic transit via central CRF and peripheral vagal pathways in conscious rats. Auton Neurosci 131(1–2):50–56
29. Noh J, Seal RP, Garver JA, Edwards RH, Kandler K (2010) Glutamate co-release at GABA/glycinergic synapses is crucial for the refinement of an inhibitory map. Nat Neurosci 13(2):232–238. doi:10.1038/nn.2478
30. O’Shea D, Gunn I, Chen X, Bloom S, Herbert J (1996) A role for central glucagon-like peptide-1 in temperature regulation. Neuroreport 7:830–832
31. Reimer R, Edwards R (2004) Organic anion transport is the primary function of the SLC17/type I phosphate transporter family. Pflugers Arch Gesamte Physiol Menschen Tiere 447(5):629–635
32. Riediger T, Eisele N, Scheel C, Lutz TA (2010) Effects of glucagon-like peptide 1 and oxyntomodulin on neuronal activity of ghrelin-sensitive neurons in the hypothalamic arcuate nucleus. Am J Physiol Regul Integr Comp Physiol 298(4):R1061–R1067. doi:10.1152/ajpregu.00438.2009
33. Rinaman L (1999a) A functional role for central glucagon-like peptide-1 receptors in lithium chloride-induced anorexia. Am J Physiol 277:R1537–R1540
34. Rinaman L (1999b) Interoceptive stress activates glucagon-like peptide-1 neurons that project to the hypothalamus. Am J Physiol 277:R582–R590
35. Rinaman L (2010) Ascending projections from the caudal visceral nucleus of the solitary tract to brain regions involved in food intake and energy expenditure. Brain Res 1350:18–34
36. Rinaman L (2011) Hindbrain noradrenergic A2 neurons: diverse roles in autonomic, endocrine, cognitive, and behavioral functions. Am J Physiol Regul Integr Comp Physiol 300(2):R222–R235. doi:10.1152/ajpregu.00556.2010
37. Rinaman L, Comer J (2000) Antagonism of central glucagon-like peptide-1 receptors enhances lipopolysaccharide-induced fever. Auton Neurosci Basic Clin 85:98–101
38. Sandoval DA, Bagnol D, Woods SC, D’Alessio DA, Seeley RJ (2008) Arcuate glucagon-like peptide 1 receptors regulate glucose homeostasis but not food intake. Diabetes 57:2046–2054
39. Sarkar S, Fekete C, Legradi G, Lechan RM (2003) Glucagon-like peptide-1 (7-36) amide (GLP-1) nerve terminals densely innervate corticotropin-releasing hormone neurons in the hypothalamic paraventricular nucleus. Brain Res 985:163–168
40. Sawchenko PE, Swanson LW (1982) The organization of noradrenergic pathways from the brainstem to the paraventricular and supraoptic nuclei in the rat. Brain Res Rev 4:275–325
41. Schafer MK, Varoqui H, Defamie N, Weihe E, Erickson JD (2002) Molecular cloning and functional identification of mouse vesicular glutamate transporter 3 and its expression in subsets of novel excitatory neurons. J Biol Chem 277(52):50734–50748. doi:10.1074/jbc.M206738200
42. Schick RR, Zimmermann JP, Walde TV, Schusdziarra V (2003) Glucagon-like peptide 1-(7-36) amide acts at lateral and medial hypothalamic sites to suppress feeding in rats. Am J Physiol Regul Integr Comp Physiol 284:R1427–R1435
43. Schone C, Burdakov D (2012) Glutamate and GABA as rapid effectors of hypothalamic “peptidergic” neurons. Front Behav Neurosci 6:81. doi:10.3389/fnbeh.2012.00081
44. Seeley RJ, Blake K, Rushing PA, Benoit S, Eng J, Woods SC, D’Alessio D (2000) The role of CNS glucagon-like peptide-1 (7-36) amide receptors in mediating the visceral illness effects of lithium chloride. J Neurosci 20(4):1616–1621
45. Stornetta RL, Sevigny CP, Guyenet PG (2002a) Vesicular glutamate transporter DNPI/VGLUT2 mRNA is present in C1 and several other groups of brainstem catecholaminergic neurons. J Comp Neurol 444(3):191–206
46. Stornetta RL, Sevigny CP, Schreihofer AM, Rosin DL, Guyenet PG (2002b) Vesicular glutamate transporter DNPI/VGLUT2 is expressed by both C1 adrenergic and nonaminergic presympathetic vasomotor neurons of the rat medulla. J Comp Neurol 444:207–220
47. Tang-Christensen M, Vrang N, Larsen PJ (2001) Glucagon-like peptide containing pathways in the regulation of feeding behaviour. Int J Obes 25(suppl 5):S42–S47
48. Thiele TE, Seeley RJ, D’Alessio D, Eng J, Bernstein IL, Woods SC, van Dijk G (1998) Central infusion of glucagon-like peptide-1-(7-36) amide (GLP-1) receptor antagonist attenuates lithium chloride-induced c-Fos induction in rat brainstem. Brain Res 801(1–2):164–170
49. Todd AJ, Hughes DI, Polgar E, Nagy GG, Mackie M, Ottersen OP, Maxwell DJ (2003) The expression of vesicular glutamate transporters VGLUT1 and VGLUT2 in neurochemically defined axonal populations in the rat spinal cord with emphasis on the dorsal horn. Eur J Neurosci 17(1):13–27
50. Turton MD, O’Shea D, Gunn I, Beak SA, Edwards CM, Meeran K, Choi SJ, Taylor GM, Heath MM, Lambert PD, Wilding JP, Smith DM, Ghatei MA, Herbert J, Bloom SR (1996) A role for glucagon-like peptide-1 in the central regulation of feeding. Nature 379(6560):69–72
51. Uehara S, Jung SK, Morimoto R, Arioka S, Miyaji T, Juge N, Hiasa M, Shimizu K, Ishimura A, Otsuka M, Yamamoto A, Maechler P, Moriyama Y (2006) Vesicular storage and secretion of l-glutamate from glucagon-like peptide 1-secreting clonal intestinal L cells. J Neurochem 96(2):550–560. doi:10.1111/j.1471-4159.2005.03575.x
52. 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(7):1301–1319. doi:10.1002/cne.22571
53. van Dijk G, Thiele TE (1999) Glucagon-like peptide-1 (7-36) amide: a central regulator of satiety and interoceptive stress. Neuropeptides 33(3):406–414
54. Varoqui H, Schafer MK, Zhu H, Weihe E, Erickson JD (2002) Identification of the differentiation-associated Na +/PI transporter as a novel vesicular glutamate transporter expressed in a distinct set of glutamatergic synapses. J Neurosci 22(1):142–155
55. Vrang N, Grove K (2011) The brainstem preproglucagon system in a non-human primate (Macaca mulatta). Brain Res 1397:28–37. doi:10.1016/j.brainres.2011.05.002
56. Vrang N, Phifer CB, Corkern MM, Berthoud HR (2003) Gastric distension induces c-Fos in medullary GLP-1/2-containing neurons. Am J Physiol Regul Integr Comp Physiol 285(2):R470–R478. doi:10.1152/ajpregu.00732.2002
57. Vrang N, Hansen M, Larsen PJ, Tang-Christensen M (2007) Characterization of brainstem preproglucagon projections to the paraventricular and dorsomedial hypothalamic nuclei. Brain Res 1149:118–126
58. Wan S, Browning KN, Travagli RA (2007) Glucagon-like peptide-1 modulates synaptic transmission to identified pancreas-projecting vagal motoneurons. Peptides 28(11):2184–2191
59. Weston M, Wang H, Stornetta RL, Sevigny CP, Guyenet PG (2003) Fos expression by glutamatergic neurons of the solitary tract nucleus after phenylephrine-induced hypertension in rats. J Comp Neurol 460(4):525–541. doi:10.1002/cne.10663
60. Zheng H, Cai L, Rinaman L (2014) Distribution of glucagon-like peptide 1-immunopositive neurons in human caudal medulla. Brain Struct Funct. doi:10.1007/s00429-014-0714-z
61. Ziegler DR, Cullinan WE, Herman JP (2002) Distribution of vesicular glutamate transporter mRNA in rat hypothalamus. J Comp Neurol 448(3):217–229. doi:10.1002/cne.10257
62. Ziegler DR, Cullinan WE, Herman JP (2005) Organization and regulation of paraventricular nucleus glutamate signaling systems: N-methyl-d-aspartate receptors. J Comp Neurol 484(1):43–56. doi:10.1002/cne.20445
63. Ziegler DR, Edwards MR, Ulrich-Lai YM, Herman JP, Cullinan WE (2012) Brainstem origins of glutamatergic innervation of the rat hypothalamic paraventricular nucleus. J Comp Neurol 520(11):2369–2394. doi:10.1002/cne.23043