Putative roles of neuropeptides in vagal afferent signaling

Physiology and Behavior

Volumn 136, Issue , 2014, Pages 155-169

  de Lartigue, Guillaume ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cardiovascular; CART; Food intake; Glutamate; Gut brain signaling; MCH; Nucleus of the solitary tract (NTS); Respiratory; Satiation; Vagus nerve

Indexed keywords

4 AMINOBUTYRIC ACID; COCAINE AND AMPHETAMINE REGULATED TRANSCRIPT PEPTIDE; GLUTAMIC ACID; MELANIN CONCENTRATING HORMONE; NEUROKININ A; NEUROPEPTIDE; NEUROTRANSMITTER; NITRIC OXIDE; SUBSTANCE P;

BREATHING; CARDIOVASCULAR FUNCTION; FEEDING; HUMAN; NERVE CELL; NONHUMAN; NUTRITIONAL STATUS; PHYSIOLOGY; REVIEW; SATIETY; SENSORY NERVE; SOLITARY TRACT NUCLEUS; VAGAL AFFERENT NEURON; VAGUS NERVE; ANIMAL; EATING; METABOLISM; SENSORY NERVE CELL; SIGNAL TRANSDUCTION;

ANIMALS; EATING; HUMANS; NEURONS, AFFERENT; NEUROPEPTIDES; SIGNAL TRANSDUCTION; VAGUS NERVE;

EID: 84917730302     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2014.03.011     Document Type: Review

References (214)

1. Ewart W.R., Jones M.V., King B.F. Central origin of vagal nerve fibres innervating the fundus and corpus of the stomach in rat. J Auton Nerv Syst 1988, 25:219-231.
2. Berthoud H.R., Kressel M., Neuhuber W.L. An anterograde tracing study of the vagal innervation of rat liver, portal vein and biliary system. Anat Embryol 1992, 186:431-442.
3. Berthoud H.R., Neuhuber W.L. Functional and chemical anatomy of the afferent vagal system. Autonomic neuroscience: basic & clinical 2000, 85:1-17.
4. Broussard D.L., Altschuler S.M. Brainstem viscerotopic organization of afferents and efferents involved in the control of swallowing. Am J Med 2000, 108(Suppl. 4a):79S-86S.
5. Hornby P.J. Receptors and transmission in the brain-gut axis II. Excitatory amino acid receptors in the brain-gut axis. Am J Physiol Gastrointest Liver Physiol 2001, 280:G1055-G1060.
6. Travagli R.A., Hermann G.E., Browning K.N., Rogers R.C. Brainstem circuits regulating gastric function. Annu Rev Physiol 2006, 68:279-305.
7. Zheng H., Patterson L.M., Morrison C., Banfield B.W., Randall J.A., Browning K.N., et al. Melanin concentrating hormone innervation of caudal brainstem areas involved in gastrointestinal functions and energy balance. Neuroscience 2005, 135:611-625.
8. Ritter R.C. A tale of two endings: modulation of satiation by NMDA receptors on or near central and peripheral vagal afferent terminals. Physiol Behav 2011, 105:94-99.
9. Julio-Pieper M., Flor P.J., Dinan T.G., Cryan J.F. Exciting times beyond the brain: metabotropic glutamate receptors in peripheral and non-neural tissues. Pharmacol Rev 2011, 63:35-58.
10. Kline D.D. Plasticity in glutamatergic NTS neurotransmission. Respir Physiol Neurobiol 2008, 164:105-111.
11. Lawrence A.J. Neurotransmitter mechanisms of rat vagal afferent neurons. Clin Exp Pharmacol Physiol 1995, 22:869-873.
12. Saha S., Batten T.F., McWilliam P.N. Glutamate-immunoreactivity in identified vagal afferent terminals of the cat: a study combining horseradish peroxidase tracing and postembedding electron microscopic immunogold staining. Exp Physiol 1995, 80:193-202.
13. Schaffar N., Rao H., Kessler J.P., Jean A. Immunohistochemical detection of glutamate in rat vagal sensory neurons. Brain Res 1997, 778:302-308.
14. Talman W.T., Perrone M.H., Reis D.J. Evidence for L-glutamate as the neurotransmitter of baroreceptor afferent nerve fibers. Science 1980, 209:813-815.
15. Lachamp P., Crest M., Kessler J.P. Vesicular glutamate transporters type 1 and 2 expression in axon terminals of the rat nucleus of the solitary tract. Neuroscience 2006, 137:73-81.
16. Corbett E.K., Sinfield J.K., McWilliam P.N., Deuchars J., Batten T.F. Differential expression of vesicular glutamate transporters by vagal afferent terminals in rat nucleus of the solitary tract: projections from the heart preferentially express vesicular glutamate transporter 1. Neuroscience 2005, 135:133-145.
17. Cai Y., Hay M., Bishop V.S. Synaptic connections and interactions between area postrema and nucleus tractus solitarius. Brain Res 1996, 724:121-124.
18. Schaffar N., Pio J., Jean A. Selective retrograde labeling of primary vagal afferent cell-bodies after injection of [3H]D-aspartate into the rat nucleus tractus solitarii. Neurosci Lett 1990, 114:253-258.
19. Granata A.R., Sved A.F., Reis D.J. In vivo release by vagal stimulation of L-[3H] glutamic acid in the nucleus tractus solitarius preloaded with L-[3H] glutamine. Brain Res Bull 1984, 12:5-9.
20. Allchin R.E., Batten T.F., McWilliam P.N., Vaughan P.F. Electrical stimulation of the vagus increases extracellular glutamate recovered from the nucleus tractus solitarii of the cat by in vivo microdialysis. Exp Physiol 1994, 79:265-268.
21. Jin Y.H., Bailey T.W., Li B.Y., Schild J.H., Andresen M.C. Purinergic and vanilloid receptor activation releases glutamate from separate cranial afferent terminals in nucleus tractus solitarius. J Neurosci 2004, 24:4709-4717.
22. Slattery J.A., Page A.J., Dorian C.L., Brierley S.M., Blackshaw L.A. Potentiation of mouse vagal afferent mechanosensitivity by ionotropic and metabotropic glutamate receptors. J Physiol 2006, 577:295-306.
23. Dietrich W.D., Lowry O.H., Loewy A.D. The distribution of glutamate, GABA and aspartate in the nucleus tractus solitarius of the cat. Brain Res 1982, 237:254-260.
24. Perrone M.H. Biochemical evidence that L-glutamate is a neurotransmitter of primary vagal afferent nerve fibers. Brain Res 1981, 230:283-293.
25. Sved A.F., Backes M.G. Neuroanatomical evidence that vagal afferent nerves do not possess a high affinity uptake system for glutamate. J Auton Nerv Syst 1992, 38:219-229.
26. Sved A.F. Lack of change in high affinity glutamate uptake in nucleus tractus solitarius following removal of the nodose ganglion. Brain Res Bull 1986, 16:325-329.
27. Sved A.F., Curtis J.T. Amino acid neurotransmitters in nucleus tractus solitarius: an in vivo microdialysis study. J Neurochem 1993, 61:2089-2098.
28. Hollmann M., Heinemann S. Cloned glutamate receptors. Annu Rev Neurosci 1994, 17:31-108.
29. Cartmell J., Schoepp D.D. Regulation of neurotransmitter release by metabotropic glutamate receptors. J Neurochem 2000, 75:889-907.
30. Ambalavanar R., Ludlow C.L., Wenthold R.J., Tanaka Y., Damirjian M., Petralia R.S. Glutamate receptor subunits in the nucleus of the tractus solitarius and other regions of the medulla oblongata in the cat. J Comp Neurol 1998, 402:75-92.
31. Broussard D.L., Wiedner E.B., Li X., Altschuler S.M. NMDAR1 mRNA expression in the brainstem circuit controlling esophageal peristalsis. Brain Res Mol Brain Res 1994, 27:329-332.
32. Austgen J.R., Fong A.Y., Foley C.M., Mueller P.J., Kline D.D., Heesch C.M., et al. Expression of Group I metabotropic glutamate receptors on phenotypically different cells within the nucleus of the solitary tract in the rat. Neuroscience 2009, 159:701-716.
33. Andresen M.C., Yang M.Y. Non-NMDA receptors mediate sensory afferent synaptic transmission in medial nucleus tractus solitarius. Am J Physiol 1990, 259:H1307-H1311.
34. Glaum S.R., Miller R.J. Metabotropic glutamate receptors mediate excitatory transmission in the nucleus of the solitary tract. J Neurosci 1992, 12:2251-2258.
35. Gordon F.J., Leone C. Non-NMDA receptors in the nucleus of the tractus solitarius play the predominant role in mediating aortic baroreceptor reflexes. Brain Res 1991, 568:319-322.
36. Aylwin M.L., Horowitz J.M., Bonham A.C. NMDA receptors contribute to primary visceral afferent transmission in the nucleus of the solitary tract. J Neurophysiol 1997, 77:2539-2548.
37. Bednar I., Qian M., Qureshi G.A., Kallstrom L., Johnson A.E., Carrer H., et al. Glutamate inhibits ingestive behaviour. J Neuroendocrinol 1994, 6:403-408.
38. Burns G.A., Ritter R.C. The non-competitive NMDA antagonist MK-801 increases food intake in rats. Pharmacol Biochem Behav 1997, 56:145-149.
39. Burns G.A., Fleischmann L.G., Ritter R.C. MK-801 interferes with nutrient-related signals for satiation. Appetite 1998, 30:1-12.
40. Burns G.A., Ritter R.C. Visceral afferent participation in delayed satiation following NMDA receptor blockade. Physiol Behav 1998, 65:361-366.
41. Covasa M., Ritter R.C., Burns G.A. Reduction of food intake by intestinal macronutrient infusion is not reversed by NMDA receptor blockade. Am J Physiol Regul Integr Comp Physiol 2000, 278:R345-R351.
42. Covasa M., Ritter R.C., Burns G.A. NMDA receptor blockade attenuates CCK-induced reduction of real feeding but not sham feeding. Am J Physiol Regul Integr Comp Physiol 2004, 286:R826-R831.
43. Berthoud H., Patterson L.M., Morales S., Zheng H. Additive satiety-delaying effects of capsaicin-induced visceral deafferentation and NMDA receptor blockade suggest separate pathways. Pharmacol Biochem Behav 2000, 67:371-375.
44. Treece B.R., Ritter R.C., Burns G.A. Lesions of the dorsal vagal complex abolish increases in meal size induced by NMDA receptor blockade. Brain Res 2000, 872:37-43.
45. Covasa M., Ritter R.C., Burns G.A. NMDA receptor participation in control of food intake by the stomach. Am J Physiol Regul Integr Comp Physiol 2000, 278:R1362-R1368.
46. Shinozaki H., Gotoh Y., Ishida M. Selective N-methyl-D-aspartate (NMDA) antagonists increase gastric motility in the rat. Neurosci Lett 1990, 113:56-61.
47. Covasa M., Hung C.Y., Ritter R.C., Burns G.A. Intracerebroventricular administration of MK-801 increases food intake through mechanisms independent of gastric emptying. Am J Physiol Regul Integr Comp Physiol 2004, 287:R1462-R1467.
48. Treece B.R., Covasa M., Ritter R.C., Burns G.A. Delay in meal termination follows blockade of N-methyl-D-aspartate receptors in the dorsal hindbrain. Brain Res 1998, 810:34-40.
49. Guard D.B., Swartz T.D., Ritter R.C., Burns G.A., Covasa M. Blockade of hindbrain NMDA receptors containing NR2 subunits increases sucrose intake. Am J Physiol Regul Integr Comp Physiol 2009, 296:R921-R928.
50. Hung C.Y., Covasa M., Ritter R.C., Burns G.A. Hindbrain administration of NMDA receptor antagonist AP-5 increases food intake in the rat. Am J Physiol Regul Integr Comp Physiol 2006, 290:R642-R651.
51. Wright J., Campos C., Herzog T., Covasa M., Czaja K., Ritter R.C. Reduction of food intake by cholecystokinin requires activation of hindbrain NMDA-type glutamate receptors. Am J Physiol Regul Integr Comp Physiol 2011, 301:R448-R455.
52. Gillespie B.R., Burns G.A., Ritter R.C. NMDA channels control meal size via central vagal afferent terminals. Am J Physiol Regul Integr Comp Physiol 2005, 289:R1504-R1511.
53. Campos C.A., Wright J.S., Czaja K., Ritter R.C. CCK-induced reduction of food intake and hindbrain MAPK signaling are mediated by NMDA receptor activation. Endocrinology 2012, 153:2633-2646.
54. Balland B., Lachamp P., Kessler J.P., Tell F. Silent synapses in developing rat nucleus tractus solitarii have AMPA receptors. J Neurosci 2008, 28:4624-4634.
55. Berthoud H.R., Earle T., Zheng H., Patterson L.M., Phifer C. Food-related gastrointestinal signals activate caudal brainstem neurons expressing both NMDA and AMPA receptors. Brain Res 2001, 915:143-154.
56. Mazzone S.B., Canning B.J. Central nervous system control of the airways: pharmacological implications. Curr Opin Pharmacol 2002, 2:220-228.
57. Machado B.H., Mauad H., Chianca Junior D.A., Haibara A.S., Colombari E. Autonomic processing of the cardiovascular reflexes in the nucleus tractus solitarii. Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas / Sociedade Brasileira de Biofisica 1997, 30:533-543. [et al.].
58. Machado B.H. Neurotransmission of the cardiovascular reflexes in the nucleus tractus solitarii of awake rats. Ann N Y Acad Sci 2001, 940:179-196.
59. Smeraski C.A., Dunwiddie T.V., Diao L., Finger T.E. Excitatory amino acid neurotransmission in the primary gustatory nucleus of the goldfish Carassius auratus. Ann N Y Acad Sci 1998, 855:442-449.
60. Meldrum B.S. Glutamate as a neurotransmitter in the brain: review of physiology and pathology. J Nutr 2000, 130:1007S-1015S.
61. Schwartz N.E., Alford S. Physiological activation of presynaptic metabotropic glutamate receptors increases intracellular calcium and glutamate release. J Neurophysiol 2000, 84:415-427.
62. Eulenburg V., Gomeza J. Neurotransmitter transporters expressed in glial cells as regulators of synapse function. Brain Res Rev 2010, 63:103-112.
63. Polson J.W., Dampney R.A., Boscan P., Pickering A.E., Paton J.F. Differential baroreflex control of sympathetic drive by angiotensin II in the nucleus tractus solitarii. Am J Physiol Regul Integr Comp Physiol 2007, 293:R1954-R1960.
64. Altschuler S.M., Bao X.M., Bieger D., Hopkins D.A., Miselis R.R. Viscerotopic representation of the upper alimentary tract in the rat: sensory ganglia and nuclei of the solitary and spinal trigeminal tracts. J Comp Neurol 1989, 283:248-268.
65. Ciriello J., Schultz C.G., Roder S. Collateral axonal projections from ventrolateral medullary non-catecholaminergic neurons to central nucleus of the amygdala. Brain Res 1994, 663:346-351.
66. Schwarz J., Burguet J., Rampin O., Fromentin G., Andrey P., Tome D., et al. Three-dimensional macronutrient-associated Fos expression patterns in the mouse brainstem. PLoS One 2010, 5:e8974.
67. Paton J.F. The Sharpey-Schafer prize lecture: nucleus tractus solitarii: integrating structures. Exp Physiol 1999, 84:815-833.
68. Bailey T.W., Hermes S.M., Whittier K.L., Aicher S.A., Andresen M.C. A-type potassium channels differentially tune afferent pathways from rat solitary tract nucleus to caudal ventrolateral medulla or paraventricular hypothalamus. J Physiol 2007, 582:613-628.
69. Ruppersberg J.P.K.E., Schwepfer R. The mechanism of magnesium block of NMDA receptors. Semin Neurosci 1994, 6:87-96.
70. Kullmann D.M., Asztely F. Extrasynaptic glutamate spillover in the hippocampus: evidence and implications. Trends Neurosci 1998, 21:8-14.
71. Chen C.Y., Bonham A.C. Glutamate suppresses GABA release via presynaptic metabotropic glutamate receptors at baroreceptor neurones in rats. J Physiol 2005, 562:535-551.
72. Gilbey M.P., Jordan D., Richter D.W., Spyer K.M. Synaptic mechanisms involved in the inspiratory modulation of vagal cardio-inhibitory neurones in the cat. J Physiol 1984, 356:65-78.
73. Hokfelt T., Broberger C., Xu Z.Q., Sergeyev V., Ubink R., Diez M. Neuropeptides-an overview. Neuropharmacology 2000, 39:1337-1356.
74. Mens W.B., Witter A., van Wimersma Greidanus T.B. Penetration of neurohypophyseal hormones from plasma into cerebrospinal fluid (CSF): half-times of disappearance of these neuropeptides from CSF. Brain Res 1983, 262:143-149.
75. Fried G., Terenius L., Hokfelt T., Goldstein M. Evidence for differential localization of noradrenaline and neuropeptide Y in neuronal storage vesicles isolated from rat vas deferens. J Neurosci 1985, 5:450-458.
76. Zhu P.C., Thureson-Klein A., Klein R.L. Exocytosis from large dense cored vesicles outside the active synaptic zones of terminals within the trigeminal subnucleus caudalis: a possible mechanism for neuropeptide release. Neuroscience 1986, 19:43-54.
77. Verhage M., McMahon H.T., Ghijsen W.E., Boomsma F., Scholten G., Wiegant V.M., et al. Differential release of amino acids, neuropeptides, and catecholamines from isolated nerve terminals. Neuron 1991, 6:517-524.
78. Thureson-Klein A., Klein R.L., Zhu P.C. Exocytosis from large dense cored vesicles as a mechanism for neuropeptide release in the peripheral and central nervous system. Scan Electron Microsc 1986, 179-187.
79. Thureson-Klein A.K., Klein R.L. Exocytosis from neuronal large dense-cored vesicles. Int Rev Cytol 1990, 121:67-126.
80. Hartmann M., Heumann R., Lessmann V. Synaptic secretion of BDNF after high-frequency stimulation of glutamatergic synapses. EMBO J 2001, 20:5887-5897.
81. van de Bospoort R., Farina M., Schmitz S.K., de Jong A., de Wit H., Verhage M., et al. Munc13 controls the location and efficiency of dense-core vesicle release in neurons. J Cell Biol 2012, 199:883-891.
82. de Lartigue G., Dimaline R., Varro A., Dockray G.J. Cocaine- and amphetamine-regulated transcript: stimulation of expression in rat vagal afferent neurons by cholecystokinin and suppression by ghrelin. J Neurosci 2007, 27:2876-2882.
83. Broberger C., Holmberg K., Kuhar M.J., Hokfelt T. Cocaine- and amphetamine-regulated transcript in the rat vagus nerve: A putative mediator of cholecystokinin-induced satiety. Proc Natl Acad Sci U S A 1999, 96:13506-13511.
84. Zheng H., Patterson L.M., Berthoud H.R. CART in the dorsal vagal complex: sources of immunoreactivity and effects on Fos expression and food intake. Brain Res 2002, 957:298-310.
85. Koylu E.O., Couceyro P.R., Lambert P.D., Kuhar M.J. Cocaine- and amphetamine-regulated transcript peptide immunohistochemical localization in the rat brain. J Comp Neurol 1998, 391:115-132.
86. De Lartigue G., Dimaline R., Varro A., Raybould H., De la Serre C.B., Dockray G.J. Cocaine- and amphetamine-regulated transcript mediates the actions of cholecystokinin on rat vagal afferent neurons. Gastroenterology 2010, 138:1479-1490.
87. de Lartigue G., Lur G., Dimaline R., Varro A., Raybould H., Dockray G.J. EGR1 Is a target for cooperative interactions between cholecystokinin and leptin, and inhibition by ghrelin, in vagal afferent neurons. Endocrinology 2010, 151:3589-3599.
88. Kristensen P., Judge M.E., Thim L., Ribel U., Christjansen K.N., Wulff B.S., et al. Hypothalamic CART is a new anorectic peptide regulated by leptin. Nature 1998, 393:72-76.
89. Vrang N., Tang-Christensen M., Larsen P.J., Kristensen P. Recombinant CART peptide induces c-Fos expression in central areas involved in control of feeding behaviour. Brain Res 1999, 818:499-509.
90. Asakawa A., Inui A., Yuzuriha H., Nagata T., Kaga T., Ueno N., et al. Cocaine-amphetamine-regulated transcript influences energy metabolism, anxiety and gastric emptying in mice. Horm Metab Res 2001, 33:554-558.
91. Stanley S.A., Small C.J., Murphy K.G., Rayes E., Abbott C.R., Seal L.J., et al. Actions of cocaine- and amphetamine-regulated transcript (CART) peptide on regulation of appetite and hypothalamo-pituitary axes in vitro and in vivo in male rats. Brain Res 2001, 893:186-194.
92. Lambert P.D., Couceyro P.R., McGirr K.M., Dall Vechia S.E., Smith Y., Kuhar M.J. CART peptides in the central control of feeding and interactions with neuropeptide Y. Synapse 1998, 29:293-298.
93. Okumura T., Yamada H., Motomura W., Kohgo Y. Cocaine-amphetamine-regulated transcript (CART) acts in the central nervous system to inhibit gastric acid secretion via brain corticotropin-releasing factor system. Endocrinology 2000, 141:2854-2860.
94. Tebbe J.J., Ortmann E., Schumacher K., Monnikes H., Kobelt P., Arnold R., et al. Cocaine- and amphetamine-regulated transcript stimulates colonic motility via central CRF receptor activation and peripheral cholinergic pathways in fed, conscious rats. Neurogastroenterol Motil 2004, 16:489-496.
95. Zheng H., Patterson C., Berthoud H.R. Fourth ventricular injection of CART peptide inhibits short-term sucrose intake in rats. Brain Res 2001, 896:153-156.
96. Aja S., Robinson B.M., Mills K.J., Ladenheim E.E., Moran T.H. Fourth ventricular CART reduces food and water intake and produces a conditioned taste aversion in rats. Behav Neurosci 2002, 116:918-921.
97. Aja S., Sahandy S., Ladenheim E.E., Schwartz G.J., Moran T.H. Intracerebroventricular CART peptide reduces food intake and alters motor behavior at a hindbrain site. Am J Physiol Regul Integr Comp Physiol 2001, 281:R1862-R1867.
98. de Lartigue G.D.R.A., Raybould H.E. Neuropeptide transmitters released from VAN into the NTS play an important role in regulating food intake. Appetite 2011, 57:S12-S13.
99. de Lartigue G. Cocaine- and amphetamine-regulated transcript (CART) derived from vagal afferent neurons is required for satiation. Neurogastroenterol Motility 2013, 25:1.
100. Heldsinger A., Lu Y., Zhou S.Y., Wu X., Grabauskas G., Song I., et al. Cocaine- and amphetamine-regulated transcript is the neurotransmitter regulating the action of cholecystokinin and leptin on short-term satiety in rats. Am J Physiol Gastrointest Liver Physiol 2012, 303:G1042-G1051.
101. Hsun Lin H., Chiu H.Y., Lai C.C. Potentiation of spinal N-methyl-D-aspartate-mediated nociceptive transmission by cocaine-regulated and amphetamine-regulated transcript peptide in rats. Neuroreport 2005, 16:253-257.
102. Burdyga G., Varro A., Dimaline R., Thompson D.G., Dockray G.J. Feeding-dependent depression of melanin-concentrating hormone and melanin-concentrating hormone receptor-1 expression in vagal afferent neurones. Neuroscience 2006, 137:1405-1415.
103. Burdyga G., Varro A., Dimaline R., Thompson D.G., Dockray G.J. Ghrelin receptors in rat and human nodose ganglia: putative role in regulating CB-1 and MCH receptor abundance. Am J Physiol Gastrointest Liver Physiol 2006, 290:G1289-G1297.
104. Qu D., Ludwig D.S., Gammeltoft S., Piper M., Pelleymounter M.A., Cullen M.J., et al. A role for melanin-concentrating hormone in the central regulation of feeding behaviour. Nature 1996, 380:243-247.
105. Nair S.G., Adams-Deutsch T., Pickens C.L., Smith D.G., Shaham Y. Effects of the MCH1 receptor antagonist SNAP 94847 on high-fat food-reinforced operant responding and reinstatement of food seeking in rats. Psychopharmacology (Berl) 2009, 205:129-140.
106. Segal-Lieberman G., Bradley R.L., Kokkotou E., Carlson M., Trombly D.J., Wang X., et al. Melanin-concentrating hormone is a critical mediator of the leptin-deficient phenotype. Proc Natl Acad Sci U S A 2003, 100:10085-10090.
107. Chen Y., Hu C., Hsu C.K., Zhang Q., Bi C., Asnicar M., et al. Targeted disruption of the melanin-concentrating hormone receptor-1 results in hyperphagia and resistance to diet-induced obesity. Endocrinology 2002, 143:2469-2477.
108. Marsh D.J., Weingarth D.T., Novi D.E., Chen H.Y., Trumbauer M.E., Chen A.S., et al. Melanin-concentrating hormone 1 receptor-deficient mice are lean, hyperactive, and hyperphagic and have altered metabolism. Proc Natl Acad Sci U S A 2002, 99:3240-3245.
109. Bittencourt J.C., Presse F., Arias C., Peto C., Vaughan J., Nahon J.L., et al. The melanin-concentrating hormone system of the rat brain: an immuno- and hybridization histochemical characterization. J Comp Neurol 1992, 319:218-245.
110. Hervieu G.J., Cluderay J.E., Harrison D., Meakin J., Maycox P., Nasir S., et al. The distribution of the mRNA and protein products of the melanin-concentrating hormone (MCH) receptor gene, slc-1, in the central nervous system of the rat. Eur J Neurosci 2000, 12:1194-1216.
111. Skofitsch G., Jacobowitz D.M., Zamir N. Immunohistochemical localization of a melanin concentrating hormone-like peptide in the rat brain. Brain Res Bull 1985, 15:635-649.
112. Zamir N., Skofitsch G., Jacobowitz D.M. Distribution of immunoreactive melanin-concentrating hormone in the central nervous system of the rat. Brain Res 1986, 373:240-245.
113. Zamir N., Skofitsch G., Bannon M.J., Jacobowitz D.M. Melanin-concentrating hormone: unique peptide neuronal system in the rat brain and pituitary gland. Proc Natl Acad Sci U S A 1986, 83:1528-1531.
114. Bresson J.L., Clavequin M.C., Fellmann D., Bugnon C. Human hypothalamic neuronal system revealed with a salmon melanin-concentrating hormone (MCH) antiserum. Neurosci Lett 1989, 102:39-43.
115. Burdyga G., Varro A., Dimaline R., Thompson D.G., Dockray G.J. Expression of cannabinoid CB1 receptors by vagal afferent neurons: kinetics and role in influencing neurochemical phenotype. Am J Physiol Gastrointest Liver Physiol 2010, 299:G63-G69.
116. Vallee R.B., Bloom G.S. Mechanisms of fast and slow axonal transport. Annu Rev Neurosci 1991, 14:59-92.
117. Hammerschlag R., Stone G.C., Bolen F.A., Lindsey J.D., Ellisman M.H. Evidence that all newly synthesized proteins destined for fast axonal transport pass through the Golgi apparatus. J Cell Biol 1982, 93:568-575.
118. Gibbins I.L., Furness J.B., Costa M. Pathway-specific patterns of the co-existence of substance P, calcitonin gene-related peptide, cholecystokinin and dynorphin in neurons of the dorsal root ganglia of the guinea-pig. Cell Tissue Res 1987, 248:417-437.
119. McMahon S.B., Gibson S. Peptide expression is altered when afferent nerves reinnervate inappropriate tissue. Neurosci Lett 1987, 73:9-15.
120. Gamse R., Lembeck F., Cuello A.C. Substance P in the vagus nerve Immunochemical and immunohistochemical evidence for axoplasmic transport. Naunyn Schmiedebergs Arch Pharmacol 1979, 306:37-44.
121. Lundberg J.M., Hokfelt T., Nilsson G., Terenius L., Rehfeld J., Elde R., et al. Peptide neurons in the vagus, splanchnic and sciatic nerves. Acta Physiol Scand 1978, 104:499-501.
122. Lorez H.P., Haeusler G., Aeppli L. Substance P neurones in medullary baroreflex areas and baroreflex function of capsaicin-treated rats Comparison with other primary afferent systems. Neuroscience 1983, 8:507-523.
123. Gillis R.A., Helke C.J., Hamilton B.L., Norman W.P., Jacobowitz D.M. Evidence that substance P is a neurotransmitter of baro- and chemoreceptor afferents in nucleus tractus solitarius. Brain Res 1980, 181:476-481.
124. Helke C.J., Goldman W., Jacobowitz D.M. Demonstration of substance P in aortic nerve afferent fibers by combined use of fluorescent retrograde neuronal labeling and immunocytochemistry. Peptides 1980, 1:359-364.
125. Morilak D.A., Morris M., Chalmers J. Release of substance P in the nucleus tractus solitarius measured by in vivo microdialysis: response to stimulation of the aortic depressor nerves in rabbit. Neurosci Lett 1988, 94:131-137.
126. Potts J.T., Fuchs I.E. Naturalistic activation of barosensitive afferents release substance P in the nucleus tractus solitarius of the cat. Brain Res 2001, 893:155-164.
127. Danks J.A., Rothman R.B., Cascieri M.A., Chicchi G.G., Liang T., Herkenham M. A comparative autoradiographic study of the distributions of substance P and eledoisin binding sites in rat brain. Brain Res 1986, 385:273-281.
128. Helke C.J., Shults C.W., Chase T.N., O'Donohue T.L. Autoradiographic localization of substance P receptors in rat medulla: effect of vagotomy and nodose ganglionectomy. Neuroscience 1984, 12:215-223.
129. Maley B.E., Sasek C.A., Seybold V.S. Substance P binding sites in the nucleus tractus solitarius of the cat. Peptides 1988, 9:1301-1306.
130. Segu L., Lanoir J., Puizillout J.J. Up-regulation of substance P binding sites in the vagus nerve projection area of the cat brainstem after nodosectomy. A quantitative autoradiographic study. J Chem Neuroanat 1991, 4:447-459.
131. Paton J.F. Importance of neurokinin-1 receptors in the nucleus tractus solitarii of mice for the integration of cardiac vagal inputs. Eur J Neurosci 1998, 10:2261-2275.
132. Chan J.Y., Barnes C.D., Chan S.H. Tonic enhancement of the sensitivity of baroreceptor reflex response by endogenous substance P in the rat. Regul Pept 1990, 29:199-213.
133. Kubo T., Kihara M. Blood pressure modulation by substance P in the rat nucleus tractus solitarius. Brain Res 1987, 413:379-383.
134. Riley J., Lin L.H., Chianca D.A., Talman W.T. Ablation of NK1 receptors in rat nucleus tractus solitarii blocks baroreflexes. Hypertension 2002, 40:823-826.
135. Hall M.E., Miley F.B., Stewart J.M. Cardiovascular effects of substance P peptides in the nucleus of the solitary tract. Brain Res 1989, 497:280-290.
136. Haeusler G., Osterwalder R. Evidence suggesting a transmitter or neuromodulatory role for substance P at the first synapse of the baroreceptor reflex. Naunyn Schmiedebergs Arch Pharmacol 1980, 314:111-121.
137. Talman W.T., Reis D.J. Baroreflex actions of substance P microinjected into the nucleus tractus solitarii in rat: a consequence of local distortion. Brain Res 1981, 220:402-407.
138. Cowan A.R., Dean C., Bago M., Seagard J.L. Potentiation of non-N-methyl-D-aspartate receptor-induced changes in blood pressure by substance P in rats. Neurosci Lett 2000, 278:161-164.
139. Hall M.E., Greer R.A., Stewart J.M. Effects of L-glutamate, substance P and substance P(1-7) on cardiovascular regulation in the nucleus tractus solitarius. Regul Pept 1993, 46:102-109.
140. Nozaki K., Moskowitz M.A., Maynard K.I., Koketsu N., Dawson T.M., Bredt D.S., et al. Possible origins and distribution of immunoreactive nitric oxide synthase-containing nerve fibers in cerebral arteries. J Cereb Blood Flow Metab 1993, 13:70-79.
141. Lawrence A.J., Jarrott B. Neurochemical modulation of cardiovascular control in the nucleus tractus solitarius. Prog Neurobiol 1996, 48:21-53.
142. Yamamoto Y., Henrich M., Snipes R.L., Kummer W. Altered production of nitric oxide and reactive oxygen species in rat nodose ganglion neurons during acute hypoxia. Brain Res 2003, 961:1-9.
143. Ruggiero D.A., Mtui E.P., Otake K., Anwar M. Central and primary visceral afferents to nucleus tractus solitarii may generate nitric oxide as a membrane-permeant neuronal messenger. J Comp Neurol 1996, 364:51-67.
144. Lin L.H., Cassell M.D., Sandra A., Talman W.T. Direct evidence for nitric oxide synthase in vagal afferents to the nucleus tractus solitarii. Neuroscience 1998, 84:549-558.
145. Lawrence A.J., Castillo-Melendez M., McLean K.J., Jarrott B. The distribution of nitric oxide synthase-, adenosine deaminase- and neuropeptide Y-immunoreactivity through the entire rat nucleus tractus solitarius: Effect of unilateral nodose ganglionectomy. J Chem Neuroanat 1998, 15:27-40.
146. Lin L.H., Talman W.T. Vesicular glutamate transporters and neuronal nitric oxide synthase colocalize in aortic depressor afferent neurons. J Chem Neuroanat 2006, 32:54-64.
147. Lewis S.J., Ohta H., Machado B., Bates J.N., Talman W.T. Microinjection of S-nitrosocysteine into the nucleus tractus solitarii decreases arterial pressure and heart rate via activation of soluble guanylate cyclase. Eur J Pharmacol 1991, 202:135-136.
148. Machado B.H., Bonagamba L.G. Microinjection of S-nitrosocysteine into the nucleus tractus solitarii of conscious rats decreases arterial pressure but L-glutamate does not. Eur J Pharmacol 1992, 221:179-182.
149. Harada S., Tokunaga S., Momohara M., Masaki H., Tagawa T., Imaizumi T., et al. Inhibition of nitric oxide formation in the nucleus tractus solitarius increases renal sympathetic nerve activity in rabbits. Circ Res 1993, 72:511-516.
150. Lin L.H., Edwards R.H., Fremeau R.T., Fujiyama F., Kaneko T., Talman W.T. Localization of vesicular glutamate transporters and neuronal nitric oxide synthase in rat nucleus tractus solitarii. Neuroscience 2004, 123:247-255.
151. Di Paola E.D., Nistico M.J.V.,.G. L-Glutamate evokes the release of an endothelium-derived relaxing factor-like substance from the rat nucleus tractus solitarius. J Cardiovasc Pharmacol 1991, 17:S269-S272.
152. Lo W.C., Lin H.C., Ger L.P., Tung C.S., Tseng C.J. Cardiovascular effects of nitric oxide and N-methyl-D-aspartate receptors in the nucleus tractus solitarii of rats. Hypertension 1997, 30:1499-1503.
153. Talman W.T., Dragon D.N., Ohta H., Lin L.H. Nitroxidergic influences on cardiovascular control by NTS: A link with glutamate. Ann N Y Acad Sci 2001, 940:169-178.
154. Dias A.C.R., Colombari E., Mifflin S.W. Effect of nitric oxide on excitatory amino acid-evoked discharge of neurons in NTS. Am J Physiol Heart C 2003, 284:H234-H240.
155. Stoyanova I.I. Gamma-aminobutiric acid immunostaining in trigeminal, nodose and spinal ganglia of the cat. Acta Histochem 2004, 106:309-314.
156. Catelli J.M., Giakas W.J., Sved A.F. GABAergic mechanisms in nucleus tractus solitarius alter blood pressure and vasopressin release. Brain Res 1987, 403:279-289.
157. van Giersbergen P.L., Palkovits M., De Jong W. Involvement of neurotransmitters in the nucleus tractus solitarii in cardiovascular regulation. Physiol Rev 1992, 72:789-824.
158. Kubo T., Kihara M. Evidence for gamma-aminobutyric acid receptor-mediated modulation of the aortic baroreceptor reflex in the nucleus tractus solitarii of the rat. Neurosci Lett 1988, 89:156-160.
159. Bousquet P., Feldman J., Bloch R., Schwartz J. Evidence for a neuromodulatory role of GABA at the first synapse of the baroreceptor reflex pathway Effects of GABA derivatives injected into the NTS. Naunyn Schmiedebergs Arch Pharmacol 1982, 319:168-171.
160. Persson B. A hypertensive response to baclofen in the nucleus tractus solitarii in rats. J Pharm Pharmacol 1981, 33:226-231.
161. Sved A.F., Tsukamoto K. Tonic stimulation of GABAB receptors in the nucleus tractus solitarius modulates the baroreceptor reflex. Brain Res 1992, 592:37-43.
162. Vargas K.J., Terunuma M., Tello J.A., Pangalos M.N., Moss S.J., Couve A. The availability of surface GABA B receptors is independent of gamma-aminobutyric acid but controlled by glutamate in central neurons. J Biol Chem 2008, 283:24641-24648.
163. Helke C.J., Hill K.M. Immunohistochemical study of neuropeptides in vagal and glossopharyngeal afferent neurons in the rat. Neuroscience 1988, 26:539-551.
164. Helke C.J., Niederer A.J. Studies on the coexistence of substance P with other putative transmitters in the nodose and petrosal ganglia. Synapse 1990, 5:144-151.
165. Nagashima A., Takano Y., Tateishi K., Matsuoka Y., Hamaoka T., Kamiya H. Cardiovascular roles of tachykinin peptides in the nucleus tractus solitarii of rats. Brain Res 1989, 487:392-396.
166. Fischer A., McGregor G.P., Saria A., Philippin B., Kummer W. Induction of tachykinin gene and peptide expression in guinea pig nodose primary afferent neurons by allergic airway inflammation. J Clin Invest 1996, 98:2284-2291.
167. Mazzone S.B., Geraghty D.P. Respiratory actions of tachykinins in the nucleus of the solitary tract: effect of neonatal capsaicin pretreatment. Br J Pharmacol 2000, 129:1132-1139.
168. Mazzone S.B., Geraghty D.P. Respiratory actions of tachykinins in the nucleus of the solitary tract: characterization of receptors using selective agonists and antagonists. Br J Pharmacol 2000, 129:1121-1131.
169. Bongianni F., Mutolo D., Cinelli E., Pantaleo T. Neurokinin receptor modulation of respiratory activity in the rabbit. Eur J Neurosci 2008, 27:3233-3243.
170. Rusin K.I., Jiang M.C., Cerne R., Randic M. Interactions between excitatory amino acids and tachykinins in the rat spinal dorsal horn. Brain Res Bull 1993, 30:329-338.
171. Joad J.P., Sekizawa S., Chen C.Y., Bonham A.C. Air pollutants and cough. Pulm Pharmacol Ther 2007, 20:347-354.
172. Bauman N.M., Wang D., Luschei E.S., Talman W.T. Effect of substance P injection into the nucleus tractus solitarius of rats on cricothyroid and thyroarytenoid motor activity and cardiovascular and respiratory systems. Ann Otol Rhinol Laryngol 2002, 111:875-883.
173. Joad J.P., Munch P.A., Bric J.M., Evans S.J., Pinkerton K.E., Chen C.Y., et al. Passive smoke effects on cough and airways in young guinea pigs: role of brainstem substance P. Am J Respir Crit Care Med 2004, 169:499-504.
174. Mazzone S.B., McGovern A.E. Immunohistochemical characterization of nodose cough receptor neurons projecting to the trachea of guinea pigs. Cough 2008, 4:9.
175. Mascarucci P., Perego C., Terrazzino S., De Simoni M.G. Glutamate release in the nucleus tractus solitarius induced by peripheral lipopolysaccharide and interleukin-1 beta. Neuroscience 1998, 86:1285-1290.
176. Furukawa N., Hatano M., Fukuda H., Koga T. Non-N-methyl-D-aspartate receptors may mediate the transmission of emetic signals between visceral vagal afferents and the solitary nucleus in dogs. Neurosci Lett 1998, 258:53-56.
177. Page A.J., O'Donnell T.A., Cooper N.J., Young R.L., Blackshaw L.A. Nitric oxide as an endogenous peripheral modulator of visceral sensory neuronal function. J Neurosci 2009, 29:7246-7255.
178. Palouzier B., Barrit-Chamoin M.C., Portalier P., Ternaux J.P. Cholinergic neurons in the rat nodose ganglia. Neurosci Lett 1987, 80:147-152.
179. Ternaux J.P., Falempin M., Palouzier B., Chamoin M.C., Portalier P. Presence of cholinergic neurons in the vagal afferent system: biochemical and immunohistochemical approaches. J Auton Nerv Syst 1989, 28:233-242.
180. Cheng P.W., Lu P.J., Chen S.R., Ho W.Y., Cheng W.H., Hong L.Z., et al. Central nicotinic acetylcholine receptor involved in Ca(2+) -calmodulin-endothelial nitric oxide synthase pathway modulated hypotensive effects. Br J Pharmacol 2011, 163:1203-1213.
181. Giacobini E., Nore B. Dopa-decarboxylase in autonomic and sensory ganglia of the cat. Acta Physiol Scand 1971, 82:209-217.
182. Katz D.M., Markey K.A., Goldstein M., Black I.B. Expression of catecholaminergic characteristics by primary sensory neurons in the normal adult rat in vivo. Proc Natl Acad Sci U S A 1983, 80:3526-3530.
183. Kummer W., Bachmann S., Neuhuber W.L., Hanze J., Lang R.E. Tyrosine-hydroxylase-containing vagal afferent neurons in the rat nodose ganglion are independent from neuropeptide-Y-containing populations and project to esophagus and stomach. Cell Tissue Res 1993, 271:135-144.
184. Granata A.R., Woodruff G.N. Dopaminergic mechanisms in the nucleus tractus solitarius and effects on blood pressure. Brain Res Bull 1982, 8:483-488.
185. Gaudin-Chazal G., Portalier P., Barrit M.C., Puizillout J.J. Serotonin-like immunoreactivity in paraffin-sections of the nodose ganglia of the cat. Neurosci Lett 1982, 33:169-172.
186. Thor K.B., Hill K.M., Harrod C., Helke C.J. Immunohistochemical and biochemical analysis of serotonin and substance P colocalization in the nucleus tractus solitarii and associated afferent ganglia of the rat. Synapse 1988, 2:225-231.
187. Nosjean A., Compoint C., Buisseret-Delmas C., Orer H.S., Merahi N., Puizillout J.J., et al. Serotonergic projections from the nodose ganglia to the nucleus tractus solitarius: an immunohistochemical and double labeling study in the rat. Neurosci Lett 1990, 114:22-26.
188. Itoh H., Bunag R.D. Cardiovascular and sympathetic effects of injecting serotonin into the nucleus tractus solitarius in rats. J Pharmacol Exp Ther 1991, 256:1147-1153.
189. Voss M.D., De Castro D., Lipski J., Pilowsky P.M., Jiang C. Serotonin immunoreactive boutons form close appositions with respiratory neurons of the dorsal respiratory group in the cat. J Comp Neurol 1990, 295:208-218.
190. Czyzyk-Krzeska M.F., Bayliss D.A., Seroogy K.B., Millhorn D.E. Gene expression for peptides in neurons of the petrosal and nodose ganglia in rat Experimental brain research. Exp Hirnforsch Exp Cereb 1991, 83:411-418.
191. Kummer W., Fischer A., Kurkowski R., Heym C. The sensory and sympathetic innervation of guinea-pig lung and trachea as studied by retrograde neuronal tracing and double-labelling immunohistochemistry. Neuroscience 1992, 49:715-737.
192. Franco-Cereceda A., Henke H., Lundberg J.M., Petermann J.B., Hokfelt T., Fischer J.A. Calcitonin gene-related peptide (CGRP) in capsaicin-sensitive substance P-immunoreactive sensory neurons in animals and man: distribution and release by capsaicin. Peptides 1987, 8:399-410.
193. Torrealba F. Calcitonin gene-related peptide immunoreactivity in the nucleus of the tractus solitarius and the carotid receptors of the cat originates from peripheral afferents. Neuroscience 1992, 47:165-173.
194. Springall D.R., Cadieux A., Oliveira H., Su H., Royston D., Polak J.M. Retrograde tracing shows that CGRP-immunoreactive nerves of rat trachea and lung originate from vagal and dorsal root ganglia. J Auton Nerv Syst 1987, 20:155-166.
195. Uddman R., Grunditz T., Luts A., Desai H., Fernstrom G., Sundler F. Distribution and origin of the peripheral innervation of rat cervical esophagus. Dysphagia 1995, 10:203-212.
196. Lutz T.A., Senn M., Althaus J., Del Prete E., Ehrensperger F., Scharrer E. Lesion of the area postrema/nucleus of the solitary tract (AP/NTS) attenuates the anorectic effects of amylin and calcitonin gene-related peptide (CGRP) in rats. Peptides 1998, 19:309-317.
197. Lundberg J.M., Dahlstrom A., Larsson I., Petterson G., Ahlman H., Kewenter J. Efferent innervation of the small intestine by adrenergic neurons from the cervical sympathetic and stellate ganglia, studied by retrograde transport of peroxidase. Acta Physiol Scand 1978, 104:33-42.
198. Dockray G.J., Gregory R.A., Tracy H.J., Zhu W.Y. Transport of cholecystokinin-octapeptide-like immunoreactivity toward the gut in afferent vagal fibres in cat and dog. J Physiol 1981, 314:501-511.
199. Mantyh P.W., Hunt S.P. Neuropeptides are present in projection neurones at all levels in visceral and taste pathways: from periphery to sensory cortex. Brain Res 1984, 299:297-312.
200. Broberger C., Holmberg K., Shi T.J., Dockray G., Hokfelt T. Expression and regulation of cholecystokinin and cholecystokinin receptors in rat nodose and dorsal root ganglia. Brain Res 2001, 903:128-140.
201. Philippe C., Cuber J.C., Bosshard A., Rampin O., Laplace J.P., Chayvialle J.A. Galanin in porcine vagal sensory nerves: immunohistochemical and immunochemical study. Peptides 1990, 11:989-993.
202. Calingasan N.Y., Ritter S. Presence of galanin in rat vagal sensory neurons: evidence from immunohistochemistry and in situ hybridization. J Auton Nerv Syst 1992, 40:229-238.
203. Page A.J., Slattery J.A., O'Donnell T,.A., Cooper N.J., Young R.L., Blackshaw L.A. Modulation of gastro-oesophageal vagal afferents by galanin in mouse and ferret. J Physiol 2005, 563:809-819.
204. Koegler F.H., Ritter S. Galanin injection into the nucleus of the solitary tract stimulates feeding in rats with lesions of the paraventricular nucleus of the hypothalamus. Physiol Behav 1998, 63:521-527.
205. Harfstrand A., Fuxe K., Melander T., Hokfelt T., Agnati L.F. Evidence for a cardiovascular role of central galanin neurons: focus on interactions with alpha 2-adrenergic and neuropeptide Y mechanisms. J Cardiovasc Pharmacol 1987, 10(Suppl. 12):S199-S204.
206. Ferrari M.F., Coelho E.F., Farizatto K.L., Chadi G., Fior-Chadi D.R. Modulation of tyrosine hydroxylase, neuropeptide y, glutamate, and substance p in Ganglia and brain areas involved in cardiovascular control after chronic exposure to nicotine. Int J Hypertens 2011, 2011:216464.
207. Martinez V., Rivier J., Coy D., Tache Y. Intracisternal injection of somatostatin receptor 5-preferring agonists induces a vagal cholinergic stimulation of gastric emptying in rats. J Pharmacol Exp Ther 2000, 293:1099-1105.
208. Helke C.J., Rabchevsky A. Axotomy alters putative neurotransmitters in visceral sensory neurons of the nodose and petrosal ganglia. Brain Res 1991, 551:44-51.
209. Zhuo H., Sinclair C., Helke C.J. Plasticity of tyrosine hydroxylase and vasoactive intestinal peptide messenger RNAs in visceral afferent neurons of the nodose ganglion upon axotomy-induced deafferentation. Neuroscience 1994, 63:617-626.
210. Zhuo H., Lewin A.C., Phillips E.T., Sinclair C.M., Helke C.J. Inhibition of axoplasmic transport in the rat vagus nerve alters the numbers of neuropeptide and tyrosine hydroxylase messenger RNA-containing and immunoreactive visceral afferent neurons of the nodose ganglion. Neuroscience 1995, 66:175-187.
211. Saade N.E., Abdallah L.E., Barada K.A., Atweh S.F., Nassar C.F. Effects of intracerebral injections of VIP on jejunal alanine absorption and gastric acid secretion in rats. Regul Pept 1995, 55:269-276.
212. Sekizawa S., Joad J.P., Bonham A.C. Substance P presynaptically depresses the transmission of sensory input to bronchopulmonary neurons in the guinea pig nucleus tractus solitarii. J Physiol 2003, 552:547-559.
213. Martin J.L., Jenkins V.K., Hsieh H.Y., Balkowiec A. Brain-derived neurotrophic factor in arterial baroreceptor pathways: implications for activity-dependent plasticity at baroafferent synapses. J Neurochem 2009, 108:450-464.
214. Hsieh H.Y., Robertson C.L., Vermehren-Schmaedick A., Balkowiec A. Nitric oxide regulates BDNF release from nodose ganglion neurons in a pattern-dependent and cGMP-independent manner. J Neurosci Res 2010, 88:1285-1297.