Biphasic modulation by galanin of excitatory synaptic transmission in substantia gelatinosa neurons of adult rat spinal cord slices

Journal of Neurophysiology

Volumn 105, Issue 5, 2011, Pages 2337-2349

  Yue, Hai Yuan ^a   Fujita, Tsugumi ^a   Kumamoto, Eiichi ^a  

^a SAGA UNIVERSITY   (Japan)

Author keywords

Pain; Patch clamp; Spinal dorsal horn

Indexed keywords

CALCIUM ION; GALANIN; GALANIN RECEPTOR 2; GALANIN RECEPTOR 3; GLUTAMIC ACID; GLYCINE RECEPTOR; LANTHANUM; VOLTAGE GATED CALCIUM CHANNEL;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CITRIC ACID CYCLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; EVOKED SPINAL CORD RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; GABAERGIC TRANSMISSION; HYPERPOLARIZATION; LUMBOSACRAL SPINE; MALE; MEMBRANE STEADY POTENTIAL; NEUROMODULATION; NEUROTRANSMITTER RELEASE; NONHUMAN; PATCH CLAMP; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT; SLOW INWARD CURRENT; SPINAL CORD NERVE CELL; SPINAL GANGLION; STIMULUS RESPONSE; SUBSTANTIA GELATINOSA; SYNAPTIC TRANSMISSION; VOLTAGE CLAMP; WHOLE CELL;

ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; EXCITATORY POSTSYNAPTIC POTENTIALS; GALANIN; MALE; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD; SUBSTANTIA GELATINOSA; SYNAPTIC TRANSMISSION;

EID: 79956265881     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00991.2010     Document Type: Article

References (63)

1. Alier KA, Chen Y, Sollenberg UE, Langel Ü, Smith PA. Selective stimulation of GalR1 and GalR2 in rat substantia gelatinosa reveals a cellular basis for the anti-and pro-nociceptive actions of galanin. Pain 137: 138-146, 2008.
2. Ataka T, Kumamoto E, Shimoji K, Yoshimura M. Baclofen inhibits more effectively C-afferent than Aδ-afferent glutamatergic transmission in substantia gelatinosa neurons of adult rat spinal cord slices. Pain 86: 273-282, 2000.
3. Berger A, Lang R, Moritz K, Santic R, Hermann A, Sperl W, Kofler B. Galanin receptor subtype GalR2 mediates apoptosis in SH-SY5Y neuroblastoma cells. Endocrinology 145: 500-507, 2004.
4. Branchek TA, Smith KE, Gerald C, Walker MW. Galanin receptor subtypes. Trends Pharmacol Sci 21: 109-116, 2000.
5. Brumovsky P, Mennicken F, O'Donnell D, Hökfelt T. Differential distribution and regulation of galanin receptors-1 and-2 in the rat lumbar spinal cord. Brain Res 1085: 111-120, 2006.
6. Carlton SM, Hargett GL. Colocalization of metabotropic glutamate receptors in rat dorsal root ganglion cells. J Comp Neurol 501: 780-789, 2007.
7. Cartmell J, Schoepp DD. Regulation of neurotransmitter release by metabotropic glutamate receptors. J Neurochem 75: 889-907, 2000.
8. Ch'ng JLC, Christofides ND, Anand P, Gibson SJ, Allen YS, Su HC, Tatemoto K, Morrison JFB, Polak JM, Bloom SR. Distribution of galanin immunoreactivity in the central nervous system and the responses of galanin-containing neuronal pathways to injury. Neuroscience 16: 343-354, 1985.
9. Coull JAM, Boudreau D, Bachand K, Prescott SA, Nault F, Sik A, de Koninck P, de Koninck Y. Trans-synaptic shift in anion gradient in spinal lamina I neurons as a mechanism of neuropathic pain. Nature 424: 938-942, 2003.
10. Cridland RA, Henry JL. Effects of intrathecal administration of neuropeptides on a spinal nociceptive reflex in the rat: VIP, galanin, CGRP, TRH, somatostatin and angiotensin II. Neuropeptides 11: 23-32, 1988.
11. Florén A, Land T, Langel Ü. Galanin receptor subtypes and ligand binding. Neuropeptides 34: 331-337, 2000.
12. Fujita T, Kumamoto E. Inhibition by endomorphin-1 and endomorphin-2 of excitatory transmission in adult rat substantia gelatinosa neurons. Neuroscience 139: 1095-1105, 2006.
13. Fujita T, Liu T, Nakatsuka T, Kumamoto E. Proteinase-activated receptor-1 activation presynaptically enhances spontaneous glutamatergic excitatory transmission in adult rat substantia gelatinosa neurons. J Neurophysiol 102: 312-319, 2009.
14. Fürst S. Transmitters involved in antinociception in the spinal cord. Brain Res Bull 48: 129-141, 1999.
15. Grudt TJ, Perl ER. Correlations between neuronal morphology and electrophysiological features in the rodent superficial dorsal horn. J Physiol 540: 189-207, 2002.
16. Gu JG, MacDermott AB. Activation of ATP P2X receptors elicits glutamate release from sensory neuron synapses. Nature 389: 749-753, 1997.
17. Hökfelt T. Galanin and its receptors: introduction to the Third International Symposium, San Diego, California, USA, 21-22 October 2004. Neuropeptides 39: 125-142, 2005.
18. Holmes FE, Bacon A, Pope RJP, Vanderplank PA, Kerr NCH, Sukumaran M, Pachnis V, Wynick D. Transgenic overexpression of galanin in the dorsal root ganglia modulates pain-related behavior. Proc Natl Acad Sci USA 100: 6180-6185, 2003.
19. 2+ current in the RINm5f cell line. Proc Natl Acad Sci USA 88: 8744-8748, 1991.
20. Hori Y, Endo K, Takahashi T. Presynaptic inhibitory action of enkephalin on excitatory transmission in superficial dorsal horn of rat spinal cord. J Physiol 450: 673-685, 1992.
21. Jhamandas JH, Harris KH, MacTavish D, Jassar BS. Novel excitatory actions of galanin on rat cholinergic basal forebrain neurons: implications for its role in Alzheimer's disease. J Neurophysiol 87: 696-704, 2002.
22. Ji RR, Zhang X, Zhang Q, Dagerlind Å, Nilsson S, Wiesenfeld-Hallin Z, Hökfelt T. Central and peripheral expression of galanin in response to inflammation. Neuroscience 68: 563-576, 1995.
23. Kai A, Ono K, Kawano H, Honda E, Nakanishi O, Inenaga K. Galanin inhibits neural activity in the subfornical organ in rat slice preparation. Neuroscience 143: 769-777, 2006.
24. 2 Adrenoceptormediated presynaptic inhibition of primary afferent glutamatergic transmission in rat substantia gelatinosa neurons. Anesthesiology 98: 682-689, 2003.
25. 2+ currents in adult, acutely dissociated dorsal root ganglion neurons. Eur J Neurosci 18: 2957-2966, 2003.
26. Kohno T, Kumamoto E, Higashi H, Shimoji K, Yoshimura M. Actions of opioids on excitatory and inhibitory transmission in substantia gelatinosa of adult rat spinal cord. J Physiol 518: 803-813, 1999.
27. Kohno T. A role of spinal inhibition in neuropathic pain. In: Cellular and Molecular Mechanisms for the Modulation of Nociceptive Transmission in the Peripheral and Central Nervous Systems, edited by Kumamoto E. Kerala, India: Research Signpost, 2007, p. 131-145.
28. Kuraishi Y, Kawamura M, Yamaguchi T, Houtani T, Kawabata S, Futaki S, Fujii N, Satoh M. Intrathecal injections of galanin and its antiserum affect nociceptive response of rat to mechanical, but not thermal, stimuli. Pain 44: 321-324, 1991.
29. Landry M, Bouali-Benazzouz R, André C, Shi TJS, Léger C, Nagy F, Hökfelt T. Galanin receptor 1 is expressed in a subpopulation of glutamatergic interneurons in the dorsal horn of the rat spinal cord. J Comp Neurol 499: 391-403, 2006.
30. Lang R, Gundlach AL, Kofler B. The galanin peptide family: receptor pharmacology, pleiotropic biological actions, and implications in health and disease. Pharmacol Ther 115: 177-207, 2007.
31. Lao LJ, Kawasaki Y, Yang K, Fujita T, Kumamoto E. Modulation by adenosine of Aδ and C primary-afferent glutamatergic transmission in adult rat substantia gelatinosa neurons. Neuroscience 125: 221-231, 2004.
32. 1 adenosine receptor. Pain 94: 315-324, 2001.
33. Li J, Perl ER. Adenosine inhibition of synaptic transmission in the substantia gelatinosa. J Neurophysiol 72: 1611-1621, 1994.
34. Liebel JT, Swandulla D, Zeilhofer HU. Modulation of excitatory synaptic transmission by nociceptin in superficial dorsal horn neurones of the neonatal rat spinal cord. Br J Pharmacol 121: 425-432, 1997.
35. Liu HX, Brumovsky P, Schmidt R, Brown W, Payza K, Hodzic L, Pou C, Godbout C, Hökfelt T. Receptor subtype-specific pronociceptive and analgesic actions of galanin in the spinal cord: selective actions via GalR1 and GalR2 receptors. Proc Natl Acad Sci USA 98: 9960-9964, 2001.
36. Liu HX, Hökfelt T. The participation of galanin in pain processing at the spinal level. Trends Pharmacol Sci 23: 468-474, 2002.
37. Liu T, Fujita T, Kawasaki Y, Kumamoto E. Regulation by equilibrative nucleoside transporter of adenosine outward currents in adult rat spinal dorsal horn neurons. Brain Res Bull 64: 75-83, 2004.
38. 2 activation enhances inhibitory synaptic transmission in rat substantia gelatinosa neurons. J Neurophysiol 99: 1274-1284, 2008.
39. Lundström L, Sollenberg U, Brewer A, Kouya PF, Zheng K, Xu XJ, Sheng X, Robinson JK, Wiesenfeld-Hallin Z, Xu ZQ, Hökfelt T, Bartfai T, Langel Ü. A galanin receptor subtype 1 specific agonist. Int J Peptide Res Ther 11: 17-27, 2005.
40. Luo C, Kumamoto E, Furue H, Chen J, Yoshimura M. Anandamide inhibits excitatory transmission to rat substantia gelatinosa neurones in a manner different from that of capsaicin. Neurosci Lett 321: 17-20, 2002a.
41. Luo C, Kumamoto E, Furue H, Chen J, Yoshimura M. Nociceptin inhibits excitatory but not inhibitory transmission to substantia gelatinosa neurones of adult rat spinal cord. Neuroscience 109: 349-358, 2002b.
42. Luo C, Kumamoto E, Furue H, Yoshimura M. Nociceptin-induced outward current in substantia gelatinosa neurones of the adult rat spinal cord. Neuroscience 108: 323-330, 2001.
43. Mennicken F, Hoffert C, Pelletier M, Ahmad S, O'Donnell D. Restricted distribution of galanin receptor 3 (GalR3) mRNA in the adult rat central nervous system. J Chem Neuroanat 24: 257-268, 2002.
44. Moore KA, Kohno T, Karchewski LA, Scholz J, Baba H, Woolf CJ. Partial peripheral nerve injury promotes a selective loss of GABAergic inhibition in the superficial dorsal horn of the spinal cord. J Neurosci 22: 6724-6731, 2002.
45. Nakatsuka T, Ataka T, Kumamoto E, Tamaki T, Yoshimura M. Alteration in synaptic inputs through C-afferent fibers to substantia gelatinosa neurons of the rat spinal dorsal horn during postnatal development. Neuroscience 99: 549-556, 2000.
46. North RA, Yoshimura M. The actions of noradrenaline on neurones of the rat substantia gelatinosa in vitro. J Physiol 349: 43-55, 1984.
47. O'Donnell D, Ahmad S, Wahlestedt C, Walker P. Expression of the novel galanin receptor subtype GALR2 in the adult rat CNS: distinct distribution from GALR1. J Comp Neurol 409: 469-481, 1999.
48. Parsons RL, Mulvaney JM, Merriam LA. Galanin activates an inwardly rectifying potassium conductance and inhibits a voltage-dependent calcium conductance in mudpuppy parasympathetic neurons. Ann NY Acad Sci 863: 156-169, 1998.
49. Scanziani M, Salin PA, Vogt KE, Malenka RC, Nicoll RA. Use-dependent increases in glutamate concentration activate presynaptic metabotropic glutamate receptors. Nature 385: 630-634, 1997.
50. Sharkey LM, Madamba SG, Siggins GR, Bartfai T. Galanin alters GABAergic neurotransmission in the dorsal raphe nucleus. Neurochem Res 33: 285-291, 2008.
51. Skofitsch G, Jacobowitz DM. Galanin-like immunoreactivity in capsaicin sensitive sensory neurons and ganglia. Brain Res Bull 15: 191-195, 1985.
52. Tamura K, Palmer JM, Winkelmann CK, Wood JD. Mechanism of action of galanin on myenteric neurons. J Neurophysiol 60: 966-979, 1988.
53. Tatemoto K, Rökaeus Å, Jörnvall H, McDonald TJ, Mutt V. Galanin-a novel biologically active peptide from porcine intestine. FEBS Lett 164: 124-128, 1983.
54. Waters SM, Krause JE. Distribution of galanin-1,-2 and-3 receptor messenger RNAs in central and peripheral rat tissues. Neuroscience 95: 265-271, 2000.
55. Wiesenfeld-Hallin Z, Villar MJ, Hökfelt T. The effects of intrathecal galanin and C-fiber stimulation on the flexor reflex in the rat. Brain Res 486: 205-213, 1989.
56. Willis WD Jr, Coggeshall RE. Sensory Mechanisms of the Spinal Cord (2nd ed.). New York: Plenum, 1991, p. 94-115.
57. Wu SY, Ohtubo Y, Brailoiu GC, Dun NJ. Effects of endomorphin on substantia gelatinosa neurons in rat spinal cord slices. Br J Pharmacol 140: 1088-1096, 2003.
58. Yang K, Fujita T, Kumamoto E. Adenosine inhibits GABAergic and glycinergic transmission in adult rat substantia gelatinosa neurons. J Neurophysiol 92: 2867-2877, 2004.
59. Yang K, Kumamoto E, Furue H, Li YQ, Yoshimura M. Action of capsaicin on dorsal root-evoked synaptic transmission to substantia gelatinosa neurons in adult rat spinal cord slices. Brain Res 830: 268-273, 1999.
60. Yang K, Li YQ. Origins of spontaneous and noxious stimuli-evoked miniature EPSCs in substantia gelatinosa. Neuroreport 12: 39-42, 2001.
61. Yau WM, Dorsett JA, Youther ML. Evidence for galanin as an inhibitory neuropeptide on myenteric cholinergic neurons in the guinea pig small intestine. Neurosci Lett 72: 305-308, 1986.
62. Yoshimura M, North RA. Substantia gelatinosa neurones hyperpolarized in vitro by enkephalin. Nature 305: 529-530, 1983.
63. 2 activation by melittin enhances spontaneous glutamatergic excitatory transmission in rat substantia gelatinosa neurons. Neuroscience 135: 485-495, 2005