Kainate receptors are primarily postsynaptic to SP-containing axon terminals in the trigeminal dorsal horn

Brain Research

Volumn 1184, Issue 1, 2007, Pages 149-159

  Hegarty, Deborah M ^a   Mitchell, Jennifer L ^a   Swanson, Kristin C ^a   Aicher, Sue A ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Electron microscopy; Glutamate receptor; Immunocytochemistry; Kainate receptor; Nociception; Substance P

Indexed keywords

KAINIC ACID RECEPTOR;

ARTICLE; ELECTRON MICROSCOPY; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; NERVE ENDING; NOCICEPTION; PRIORITY JOURNAL; SPINAL CORD DORSAL HORN;

ANIMALS; MALE; MICROSCOPY, IMMUNOELECTRON; POSTERIOR HORN CELLS; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, KAINIC ACID; SUBSTANCE P; SYNAPSES; TRIGEMINAL NUCLEUS, SPINAL;

RATTUS;

EID: 36349001813     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2007.09.070     Document Type: Article

References (74)

1. Advokat C., and Rutherford D. Selective antinociceptive effect of excitatory amino acid antagonists in intact and acute spinal rats. Pharmacol. Biochem. Behav. 51 (1995) 855-860
2. Afrah A.W., Fiska A., Gjerstad J., Gustafsson H., Tjolsen A., Olgart L., Stiller C.O., Hole K., and Brodin E. Spinal substance P release in vivo during the induction of long-term potentiation in dorsal horn neurons. Pain 96 (2002) 49-55
3. Aicher S.A., Sharma S., Cheng P.Y., and Pickel V.M. The N-methyl-d-aspartate (NMDA) receptor is postsynaptic to substance P-containing axon terminals in the rat superficial dorsal horn. Brain Res. 772 (1997) 71-81
4. Aicher S.A., Punnoose A., and Goldberg A. mu-Opioid receptors often colocalize with the substance P receptor (NK1) in the trigeminal dorsal horn. J. Neurosci. 20 (2000) 4345-4354
5. Aicher S.A., Sharma S., Cheng P.Y., Liu-Chen L.Y., and Pickel V.M. Dual ultrastructural localization of mu-opiate receptors and substance p in the dorsal horn. Synapse 36 (2000) 12-20
6. Aicher S.A., Mitchell J.L., Swanson K.C., and Zadina J.E. Endomorphin-2 axon terminals contact mu-opioid receptor-containing dendrites in trigeminal dorsal horn. Brain Res. 977 (2003) 190-198
7. Allen B.J., Rogers S.D., Ghilardi J.R., Menning P.M., Kuskowski M.A., Basbaum A.I., Simone D.A., and Mantyh P.W. Noxious cutaneous thermal stimuli induce a graded release of endogenous substance P in the spinal cord: imaging peptide action in vivo. J. Neurosci. 17 (1997) 5921-5927
8. Barber R.P., Vaughn J.E., Slemmon J.R., Salvaterra P.M., Roberts E., and Leeman S.E. The origin, distribution and synaptic relationships of substance P axons in rat spinal cord. J. Comp. Neurol. 184 (1979) 331-351
9. Battaglia G., and Rustioni A. Coexistence of glutamate and substance P in dorsal root ganglion neurons of the rat and monkey. J. Comp. Neurol. 277 (1988) 302-312
10. Blackburn-Munro G., Bomholt S.F., and Erichsen H.K. Behavioural effects of the novel AMPA/GluR5 selective receptor antagonist NS1209 after systemic administration in animal models of experimental pain. Neuropharmacology 47 (2004) 351-362
11. Brodin E., Linderoth B., Gazelius B., and Ungerstedt U. In vivo release of substance P in cat dorsal horn studied with microdialysis. Neurosci. Lett. 76 (1987) 357-362
12. Calcutt N.A., Stiller C., Gustafsson H., and Malmberg A.B. Elevated substance-P-like immunoreactivity levels in spinal dialysates during the formalin test in normal and diabetic rats. Brain Res. 856 (2000) 20-27
13. Cao Y.Q., Mantyh P.W., Carlson E.J., Gillespie A.M., Epstein C.J., and Basbaum A.I. Primary afferent tachykinins are required to experience moderate to intense pain. Nature 392 (1998) 390-394
14. Chan J., Aoki C., and Pickel V.M. Optimization of differential immunogold-silver and peroxidase labeling with maintenance of ultrastructure in brain sections before plastic embedding. J. Neurosci. Methods 33 (1990) 113-127
15. Coggeshall R.E., and Carlton S.M. Ultrastructural analysis of NMDA, AMPA, and kainate receptors on unmyelinated and myelinated axons in the periphery. J. Comp. Neurol. 391 (1998) 78-86
16. Cuello A.C., Galfre G., and Milstein C. Detection of substance P in the central nervous system by a monoclonal antibody. Proc. Natl. Acad. Sci. U. S. A. 76 (1979) 3532-3536
17. De Biasi S., and Rustioni A. Glutamate and substance P coexist in primary afferent terminals in the superficial laminae of spinal cord. Proc. Natl. Acad. Sci. U. S. A. 85 (1988) 7820-7824
18. DeKoninck Y., Ribeiro-Da-Silva A., Henry J.L., and Cuello A.C. Spinal neurons exhibiting a specific nociceptive response receive abundant substance P-containing synaptic contacts. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 5073-5077
19. Dougherty P.M., and Willis W.D. Enhancement of spinothalamic neuron responses to chemical and mechanical stimuli following combined micro-iontophoretic application of N-methyl-d-aspartic acid and substance P. Pain 47 (1991) 85-93
20. Dougherty P.M., Palecek J., Zorn S., and Willis W.D. Combined application of excitatory amino acids and substance P produces long-lasting changes in responses of primate spinothalamic tract neurons. Brain Res. Brain Res. Rev. 18 (1993) 227-246
21. Drake C.T., Aicher S.A., Montalmant F.L., and Milner T.A. Redistribution of mu-opioid receptors in C1 adrenergic neurons following chronic administration of morphine. Exp. Neurol. 196 (2005) 365-372
22. Dubner R., and Bennett G.J. Spinal and trigeminal mechanisms of nociception. Annu. Rev. Neurosci. 6 (1983) 381-418
23. Duggan A.W., Hendry I.A., Morton C.R., Hutchison W.D., and Zhao Z.Q. Cutaneous stimuli releasing immunoreactive substance P in the dorsal horn of the cat. Brain Res. 451 (1988) 261-273
24. Frerking M., and Nicoll R.A. Synaptic kainate receptors. Curr. Opin. Neurobiol. 10 (2000) 342-351
25. Galeazza M.T., Garry M.G., Yost H.J., Strait K.A., Hargreaves K.M., and Seybold V.S. Plasticity in the synthesis and storage of substance P and calcitonin gene-related peptide in primary afferent neurons during peripheral inflammation. Neuroscience 66 (1995) 443-458
26. Go V.L., and Yaksh T.L. Release of substance P from the cat spinal cord. J. Physiol. 391 (1987) 141-167
27. Hokfelt T., Kellerth J.O., Nilsson G., and Pernow B. Substance p: localization in the central nervous system and in some primary sensory neurons. Science 190 (1975) 889-890
28. Hollmann M., and Heinemann S. Cloned glutamate receptors. Annu. Rev. Neurosci. 17 (1994) 31-108
29. Honore P., Menning P.M., Rogers S.D., Nichols M.L., Basbaum A.I., Besson J.M., and Mantyh P.W. Spinal substance P receptor expression and internalization in acute, short-term, and long-term inflammatory pain states. J. Neurosci. 19 (1999) 7670-7678
30. Huettner J.E. Glutamate receptor channels in rat DRG neurons: activation by kainate and quisqualate and blockade of desensitization by Con A. Neuron 5 (1990) 255-266
31. Huntley G.W., Rogers S.W., Moran T., Janssen W., Archin N., Vickers J.C., Cauley K., Heinemann S.F., and Morrison J.H. Selective distribution of kainate receptor subunit immunoreactivity in monkey neocortex revealed by a monoclonal antibody that recognizes glutamate receptor subunits GluR5/6/7. J. Neurosci. 13 (1993) 2965-2981
32. Hutchins B., Spears R., Hinton R.J., and Harper R.P. Calcitonin gene-related peptide and substance P immunoreactivity in rat trigeminal ganglia and brainstem following adjuvant-induced inflammation of the temporomandibular joint. Arch. Oral Biol. 45 (2000) 335-345
33. Hwang S.J., Pagliardini S., Rustioni A., and Valtschanoff J.G. Presynaptic kainate receptors in primary afferents to the superficial laminae of the rat spinal cord. J. Comp. Neurol. 436 (2001) 275-289
34. Jaskolski F., Coussen F., and Mulle C. Subcellular localization and trafficking of kainate receptors. Trends Pharmacol. Sci. 26 (2005) 20-26
35. Jessell T.M., and Iversen L.L. Opiate analgesics inhibit substance P release from rat trigeminal nucleus. Nature 268 (1977) 549-551
36. Jessell T., Tsunoo A., Kanazawa I., and Otsuka M. Substance P: depletion in the dorsal horn of rat spinal cord after section of the peripheral processes of primary sensory neurons. Brain Res. 168 (1979) 247-259
37. Kerchner G.A., Wilding T.J., Li P., Zhuo M., and Huettner J.E. Presynaptic kainate receptors regulate spinal sensory transmission. J. Neurosci. 21 (2001) 59-66
38. Kerchner G.A., Wilding T.J., Huettner J.E., and Zhuo M. Kainate receptor subunits underlying presynaptic regulation of transmitter release in the dorsal horn. J. Neurosci. 22 (2002) 8010-8017
39. Kuraishi Y., Hirota N., Sato Y., Hanashima N., Takagi H., and Satoh M. Stimulus specificity of peripherally evoked substance P release from the rabbit dorsal horn in situ. Neuroscience 30 (1989) 241-250
40. Levine J.D., Fields H.L., and Basbaum A.I. Peptides and the primary afferent nociceptor. J. Neurosci. 13 (1993) 2273-2286
41. Li P., Wilding T.J., Kim S.J., Calejesan A.A., Huettner J.E., and Zhuo M. Kainate-receptor-mediated sensory synaptic transmission in mammalian spinal cord. Nature 397 (1999) 161-164
42. Ljungdahl A., Hokfelt T., and Nilsson G. Distribution of substance P-like immunoreactivity in the central nervous system of the rat-I. Cell bodies and nerve terminals. Neuroscience 3 (1978) 861-943
43. Lucifora S., Willcockson H.H., Lu C.R., Darstein M., Phend K.D., Valtschanoff J.G., and Rustioni A. Presynaptic low- and high-affinity kainate receptors in nociceptive spinal afferents. Pain 120 (2006) 97-105
44. Ma W., Ribeiro-Da-Silva A., De K.Y., Radhakrishnan V., Cuello A.C., and Henry J.L. Substance P and enkephalin immunoreactivities in axonal boutons presynaptic to physiologically identified dorsal horn neurons. An ultrastructural multiple-labelling study in the cat. Neuroscience 77 (1997) 793-811
45. Malcangio M., Ramer M.S., Jones M.G., and McMahon S.B. Abnormal substance P release from the spinal cord following injury to primary sensory neurons. Eur. J. Neurosci. 12 (2000) 397-399
46. McCarson K.E., and Goldstein B.D. Release of substance P into the superficial dorsal horn following nociceptive activation of the hindpaw of the rat. Brain Res. 568 (1991) 109-115
47. Mjellem-Joly N., Lund A., Berge O.G., and Hole K. Potentiation of a behavioural response in mice by spinal coadministration of substance P and excitatory amino acid agonists. Neurosci. Lett. 133 (1991) 121-124
48. Nasstrom J., Karlsson U., and Post C. Antinociceptive actions of different classes of excitatory amino acid receptor antagonists in mice. Eur. J. Pharmacol. 212 (1992) 21-29
49. Neubert J.K., Maidment N.T., Matsuka Y., Adelson D.W., Kruger L., and Spigelman I. Inflammation-induced changes in primary afferent-evoked release of substance P within trigeminal ganglia in vivo. Brain Res. 871 (2000) 181-191
50. Nishiyama T., Gyermek L., Lee C., Kawasaki-Yatsugi S., and Yamaguchi T. The spinal antinociceptive effects of a novel competitive AMPA receptor antagonist, YM872, on thermal or formalin-induced pain in rats. Anesth. Analg. 89 (1999) 143-147
51. Okano K., Kuraishi Y., and Satoh M. Involvement of spinal substance P and excitatory amino acids in inflammatory hyperalgesia in rats. Jpn. J. Pharmacol. 76 (1998) 15-22
52. Peters A., Palay S.L., and Webster H.D. The Fine Structure of the Nervous System: Neurons and Their Supporting Cells (1991), Oxford, New York
53. Petralia R.S., Wang Y.X., and Wenthold R.J. Histological and ultrastructural localization of the kainate receptor subunits, KA2 and GluR6/7, in the rat nervous system using selective antipeptide antibodies. J. Comp. Neurol. 349 (1994) 85-110
54. Pickel V.M., Reis D.J., and Leeman S.E. Ultrastructural localization of substance P in neurons of rat spinal cord. Brain Res. 122 (1977) 534-540
55. Pinheiro P., and Mulle C. Kainate receptors. Cell Tissue Res. 326 (2006) 457-482
56. Priestley J.V., Somogyi P., and Cuello A.C. Immunocytochemical localization of substance P in the spinal trigeminal nucleus of the rat: a light and electron microscopic study. J. Comp. Neurol. 211 (1982) 31-49
57. Randic M., Jiang M.C., Rusin K.I., Cerne R., and Kolaj M. Interactions between excitatory amino acids and tachykinins and long-term changes of synaptic responses in the rat spinal dorsal horn. Regul. Pept. 46 (1993) 418-420
58. Ribeiro-Da-Silva A., Pioro E.P., and Cuello A.C. Substance P- and enkephalin-like immunoreactivities are colocalized in certain neurons of the substantia gelatinosa of the rat spinal cord: an ultrastructural double-labeling study. J. Neurosci. 11 (1991) 1068-1080
59. Ruscheweyh R., and Sandkuhler J. Role of kainate receptors in nociception. Brain Res. Brain Res. Rev. 40 (2002) 215-222
60. Rusin K.I., Jiang M.C., Cerne R., and Randic M. Interactions between excitatory amino acids and tachykinins in the rat spinal dorsal horn. Brain Res. Bull. 30 (1993) 329-338
61. Sahara Y., Noro N., Iida Y., Soma K., and Nakamura Y. Glutamate receptor subunits GluR5 and KA-2 are coexpressed in rat trigeminal ganglion neurons. J. Neurosci. 17 (1997) 6611-6620
62. Samsam M., Covenas R., Ahangari R., Yajeya J., Narvaez J.A., and Tramu G. Alterations in neurokinin A-, substance P- and calcitonin gene-related peptide immunoreactivities in the caudal trigeminal nucleus of the rat following electrical stimulation of the trigeminal ganglion. Neurosci. Lett. 261 (1999) 179-182
63. Schaible H.G., Jarrott B., Hope P.J., and Duggan A.W. Release of immunoreactive substance P in the spinal cord during development of acute arthritis in the knee joint of the cat: a study with antibody microprobes. Brain Res. 529 (1990) 214-223
64. Schaible H.G., Ebersberger A., Peppel P., Beck U., and Messlinger K. Release of immunoreactive substance P in the trigeminal brain stem nuclear complex evoked by chemical stimulation of the nasal mucosa and the dura mater encephali-a study with antibody microprobes. Neuroscience 76 (1997) 273-284
65. Simmons R.M., Li D.L., Hoo K.H., Deverill M., Ornstein P.L., and Iyengar S. Kainate GluR5 receptor subtype mediates the nociceptive response to formalin in the rat. Neuropharmacology 37 (1998) 25-36
66. Sluka K.A., Dougherty P.M., Sorkin L.S., Willis W.D., and Westlund K.N. Neural changes in acute arthritis in monkeys: III. Changes in substance P, calcitonin gene-related peptide and glutamate in the dorsal horn of the spinal cord. Brain Res. Brain Res. Rev. 17 (1992) 29-38
67. Snijdelaar D.G., Dirksen R., Slappendel R., and Crul B.J. Substance P. Eur. J. Pain 4 (2000) 121-135
68. Sugimoto T., Fujiyoshi Y., Xiao C., He Y.F., and Ichikawa H. Central projection of calcitonin gene-related peptide (CGRP)- and substance P (SP)-immunoreactive trigeminal primary neurons in the rat. J. Comp. Neurol. 378 (1997) 425-442
69. Szekely J.I., Kedves R., Mate I., Torok K., and Tarnawa I. Apparent antinociceptive and anti-inflammatory effects of GYKI 52466. Eur. J. Pharmacol. 336 (1997) 143-154
70. Tallaksen-Greene S.J., Young A.B., Penney J.B., and Beitz A.J. Excitatory amino acid binding sites in the trigeminal principal sensory and spinal trigeminal nuclei of the rat. Neurosci. Lett. 141 (1992) 79-83
71. Willis W.D. The Pain System: The Neural Basis of Nociceptive Transmission in the Mammalian Nervous System (1985), Karger, Paris
72. Yaksh T.L., Jessell T.M., Gamse R., Mudge A.W., and Leeman S.E. Intrathecal morphine inhibits substance P release from mammalian spinal cord in vivo. Nature 286 (1980) 155-157
73. Yaksh T.L., Michener S.R., Bailey J.E., Harty G.J., Lucas D.L., Nelson D.K., Roddy D.R., and Go V.L. Survey of distribution of substance P, vasoactive intestinal polypeptide, cholecystokinin, neurotensin, Met-enkephalin, bombesin and PHI in the spinal cord of cat, dog, sloth and monkey. Peptides 9 (1988) 357-372
74. Zeng J., Thomson L.M., Aicher S.A., and Terman G.W. Primary afferent NMDA receptors increase dorsal horn excitation and mediate opiate tolerance in neonatal rats. J. Neurosci. 26 (2006) 12033-12042