Hindbrain glucoprivation effects on gastric vagal reflex circuits and gastric motility in the rat are suppressed by the astrocyte inhibitor fluorocitrate

Journal of Neuroscience

Volumn 34, Issue 32, 2014, Pages 10488-10496

  Hermann, Gerlinda E ^a   Viard, Edouard ^a   Rogers, Richard C ^a  

^a PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

Author keywords

Astrocytes; Dorsal motor nucleus; Fluorocitrate; Solitary nucleus; Vago vagal reflex

Indexed keywords

ASTROCYTES; DORSAL MOTOR NUCLEUS; FLUOROCITRATE; SOLITARY NUCLEUS; VAGO-VAGAL REFLEX;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; CITRATES; DEOXYGLUCOSE; ENZYME INHIBITORS; GASTROINTESTINAL MOTILITY; GLUCOSE; INSULIN; NEURONS; RATS; REFLEX; RHOMBENCEPHALON; VAGUS NERVE;

EID: 84905695105     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1406-14.2014     Document Type: Article

References (56)

1. Adachi A, Kobashi M, Funahashi M (1995) Glucose-responsive neurons in the brainstem. Obes Res 3:735S-740S. CrossRef Medline
2. Andrew S. F, Dinh TT, Ritter S (2007) Localized glucoprivation of hindbrain sites elicits corticosterone and glucagon secretion. Am J Physiol Regul Integr Comp Physiol 292:R1792-R1798. CrossRef Medline
3. Araque A., Parpura V, Sanzgiri RP, Haydon PG (1999) Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci 22:208-215. CrossRef Medline
4. Arnold S. (2005) Estrogen suppresses the impact of glucose deprivation on astrocytic calcium levels and signaling independently of the nuclear estrogen receptor. Neurobiol Dis 20:82-92. CrossRef Medline
5. Beaumont W. (1833) Experiments and observations on the gastric juice. F.P. Allen, Plattsburgh.
6. Bernard C. (1855) Lecons de physiologie experimentale appliques á la medecine, pp 296-313. Paris: Bailliere.
7. Buelke-Sam J., Holson JF, Bazare JJ, Young JF (1978) Comparative stability of physiological parameters during sustained anesthesia in rats. Lab Anim Sci 28:157-162. Medline
8. Bulatao E., Carlson A (1924) Contributions to the physiology of the stomach: influence of experimental changes in blood sugar level on gastric hunger contractions. Am J Physiol 69:107-115.
9. Cannon W. B, Washburn AL (1912) An explanation of hunger. Am J Physiol 29:441-454.
10. Cato R. K, Flanagan LM, Verbalis JG, Stricker EM (1990) Effects of glucoprivation on gastric motility and pituitary oxytocin secretion in rats. Am J Physiol 259:R447-R452. Medline
11. Chen C. H, Stephens RL Jr, Rogers RC (1997) PYY and NPY: control of gastric motility via action on Y1 and Y2 receptors in the DVC. Neurogastroenterol Motil 9:109-116. CrossRef Medline
12. Dallaporta M., Himmi T, Perrin J, Orsini JC (1999) Solitary tract nucleus sensitivity to moderate changes in glucose level. Neuroreport 10:2657-2660. CrossRef Medline
13. Dallaporta M., Perrin J, Orsini JC (2000) Involvement of adenosine triphosphate-sensitive K+ channels in glucose-sensing in the rat solitary tract nucleus. Neurosci Lett 278:77-80. CrossRef Medline
14. Edling Y., Ingelman-Sundberg M, Simi A (2007) Glutamate activates c-fos in glial cells via a novel mechanism involving the glutamate receptor subtype mGlu5 and the transcriptional repressor DREAM. Glia 55:328-340. CrossRef Medline
15. Erlichman J. S, Leiter JC (2010) Glia modulation of the extracellular milieu as a factor in central CO2 chemosensitivity and respiratory control. J Appl Physiol 108:1803-1811. CrossRef Medline
16. Erlichman J. S, Li A, Nattie EE (1998) Ventilatory effects of glial dysfunction in a rat brain stem chemoreceptor region. J Appl Physiol 85:1599-1604. Medline
17. Fellin T., Sul JY, D'Ascenzo M, Takano H, Pascual O, Haydon PG (2006) Bidirectional astrocyte-neuron communication: the many roles of glutamate and ATP. Novartis Found Symp 276:208-217. CrossRef Medline
18. Granneman J., Friedman MI (1983) Feeding after recovery from 2-deoxyglucose injection: cerebral and peripheral factors. Am J Physiol 244:R383-R388. Medline
19. Hassel B., Paulsen RE, Johnsen A, Fonnum F (1992) Selective inhibition of glial cell metabolism in vivo by fluorocitrate. Brain Res 576:120-124. CrossRef Medline
20. Hermann G., Rogers RC (1995) Tumor necrosis factor-alpha in the dorsal vagal complex suppresses gastric motility. Neuroimmunomodulation 2:74-81. CrossRef Medline
21. Hermann G. E, Rogers RC (2009) TNF activates astrocytes and catecholaminergic neurons in the solitary nucleus: implications for autonomic control. Brain Res 1273:72-82. CrossRef Medline
22. Hermann G. E, Tovar CA, Rogers RC (2002) LPS-induced suppression of gastric motility relieved by TNFR:Fc construct in dorsal vagal complex. Am J Physiol Gastrointest Liver Physiol 283:G634-G639. CrossRef Medline
23. Hermann G. E, Travagli RA, Rogers RC (2006) Esophageal-gastric relaxation reflex in rat: dual control of peripheral nitrergic and cholinergic transmission. Am J Physiol Regul Integr Comp Physiol 290:R1570-R1576. CrossRef Medline
24. Hermann G. E, Van Meter MJ, Rood JC, Rogers RC (2009) Proteinaseactivated receptors in the nucleus of the solitary tract: evidence for glialneural interactions in autonomic control of the stomach. J Neurosci 29: 9292-9300. CrossRef Medline
25. Hoffman G. E, Smith MS, Verbalis JG (1993) c-Fos and related immediate early gene products as markers of activity in neuroendocrine systems. Front Neuroendocrinol 14:173-213. CrossRef Medline
26. Kahlert S., Reiser G (2000) Requirement of glycolytic and mitochondrial energy supply for loading of Ca(2+) stores and InsP(3)-mediated Ca(2+) signaling in rat hippocampus astrocytes. J Neurosci Res 61:409-420. CrossRef Medline
27. Martín E. D, Fernández M, Perea G, Pascual O, Haydon PG, Araque A, Ceña V (2007) Adenosine released by astrocytes contributes to hypoxia-induced modulation of synaptic transmission. Glia 55:36-45. CrossRef Medline
28. Marty N., Dallaporta M, Foretz M, Emery M, Tarussio D, Bady I, Binnert C, Beermann F., Thorens B (2005) Regulation of glucagon secretion by glucose transporter type 2 (glut2) and astrocyte-dependent glucose sensors. J Clin Invest 115:3545-3553. CrossRef Medline
29. Marty N., Dallaporta M, Thorens B (2007) Brain glucose sensing, counterregulation, and energy homeostasis. Physiology 22:241-251. CrossRef Medline
30. McCann M. J, Rogers RC (1990) Oxytocin excites gastric-related neurones in rat dorsal vagal complex. J Physiol 428:95-108. Medline
31. McCann M. J, Rogers RC (1992) Impact of antral mechanoreceptor activation on the vago-vagal reflex in the rat: functional zonation of responses. J Physiol 453:401-411. Medline
32. McCann M. J, Rogers RC (1994) Functional and chemical neuroanatomy of a gastric vago-vagal reflex. In: Innervation of the gut: pathophysiological implications (Taché Y, Wingate DL, Burks TF, eds), pp 81-92. Boca Raton, FL: CRC.
33. McCann M. J, Hermann GE, Rogers RC (1988) Dorsal medullary serotonin and gastric motility: enhancement of effects by thyrotropin-releasing hormone. J Auton Nerv Syst 25:35-40. CrossRef Medline
34. McDougal D. H, Hermann GE, Rogers RC (2013) Astrocytes in the nucleus of the solitary tract are activated by low glucose or glucoprivation: evidence for glial involvement in glucose homeostasis. Front Neurosci 7:249. CrossRef Medline
35. Mizuno Y., Oomura Y (1984) Glucose responding neurons in the nucleus tractus solitarius of the rat: in vitro study. Brain Res 307:109-116. CrossRef Medline
36. Novin D., Vander Weele DA, Rezek M (1973) Infusion of 2-deoxy-D-glucose into the hepatic-portal system causes eating: evidence for peripheral glucoreceptors. Science 181:858-860. CrossRef Medline
37. Ormsbee H. S 3rd, Bass P (1976) Gastroduodenal motor gradients in the dog after pyloroplasty. Am J Physiol 230:389-397. Medline
38. Pascual O., Casper KB, Kubera C, Zhang J, Revilla-Sanchez R, Sul JY, Takano H, Moss S. J, McCarthy K, Haydon PG (2005) Astrocytic purinergic signaling coordinates synaptic networks. Science 310:113-116. CrossRef Medline
39. Pavlov I. P (1910) The centrifugal (efferent) nerves to the gastric glands and of the pancreas. In: The work of the digestive glands, Ed 2, pp 48-59. Philadelphia: Charles Griffin.
40. Richter C. P (1941) Increased dextrose appetite of normal rats treated with insulin. Am J Physiol 135:781-787.
41. Ritter R. C, Roelke M, Neville M (1978) Glucoprivic feeding behavior in absence of other signs of glucoprivation. Am J Physiol 234:E617-E621. Medline
42. Ritter S., Llewellyn-Smith I, Dinh TT (1998) Subgroups of hindbrain catecholamine neurons are selectively activated by 2-deoxy-D-glucose induced metabolic challenge. Brain Res 805:41-54. CrossRef Medline
43. Ritter S., Dinh TT, Zhang Y (2000) Localization of hindbrain glucoreceptive sites controlling food intake and blood glucose. Brain Res 856:37-47. CrossRef Medline
44. Rogers R. C, Hermann GE (1987) Oxytocin, oxytocin antagonist, TRH, and hypothalamic paraventricular nucleus stimulation effects on gastric motility. Peptides 8:505-513. CrossRef Medline
45. Rogers R. C, McCann MJ (1989) Effects of TRH on the activity of gastric inflation-related neurons in the solitary nucleus in the rat. Neurosci Lett 104:71-76. CrossRef Medline
46. Rogers R. C, Viard E, Hermann GE (2013) CXCL12 sensitizes vago-vagal reflex neurons in the dorsal medulla. Brain Res 1492:46-52. CrossRef Medline
47. Rogers R. C, Hermann GE (2012) Brainstem control of gastric function. In: Physiology of the gastrointestinal tract, Ed 4 (Johnson LR, ed), pp 861-892. New York: Elsevier.
48. Schemann M., Grundy D (1992) Electrophysiological identification of vagally innervated enteric neurons in guinea pig stomach. Am J Physiol 263:G709-G718. Medline
49. Swanson R. A, Graham SH (1994) Fluorocitrate and fluoroacetate effects on astrocyte metabolism in vitro. Brain Res 664:94-100. CrossRef Medline
50. Taché Y., Garrick T, Raybould H (1990) Central nervous system action of peptides to influence gastrointestinal motor function. Gastroenterology 98:517-528. Medline
51. Thorens B. (2001) GLUT2 in pancreatic and extra-pancreatic glucodetection (review). Mol Membr Biol 18:265-273. CrossRef Medline
52. Verkhratsky A., Rodríguez JJ, Parpura V (2012) Calcium signalling in astroglia. Mol Cell Endocrinol 353:45-56. CrossRef Medline
53. Viard E., Rogers RC, Hermann GE (2012) Systemic cholecystokinin amplifies vago-vagal reflex responses recorded in vagal motor neurones. J Physiol 590:631-646. CrossRef Medline
54. Yettefti K., Orsini JC, el Ouazzani T, Himmi T, Boyer A, Perrin J (1995) Sensitivity of nucleus tractus solitarius neurons to induced moderate hyperglycemia, with special reference to catecholaminergic regions. J Auton Nerv Syst 51:191-197. CrossRef Medline
55. Young J. K, Baker JH, Montes MI (2000) The brain response to 2-deoxy glucose is blocked by a glial drug. Pharmacol Biochem Behav 67:233-239. CrossRef Medline
56. Zhang Q., Haydon PG (2005) Roles for gliotransmission in the nervous system. J Neural Transm 112:121-125. CrossRef Medline