Distribution of antinociceptive adenosine A1 receptors in the spinal cord dorsal horn, and relationship to primary afferents and neuronal subpopulations

Neuroscience

Volumn 121, Issue 4, 2003, Pages 907-916

  Schulte, G ^a   Robertson, B ^a   Fredholm, B B ^a   Delander, G E ^a   Shortland, P ^b   Molander, C ^a,c  

^a KAROLINSKA INSTITUTE   (Sweden)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Dorsal root ganglion; Nociception; Pain; Rat; Somatosensory system; Substantia gelatinosa

Indexed keywords

ADENOSINE A1 RECEPTOR; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; ANTINOCICEPTIVE AGENT; CALCITONIN GENE RELATED PEPTIDE RECEPTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMATE RECEPTOR; ISOLECTIN B4; METENKEPHALIN; MU OPIATE RECEPTOR; NITRIC OXIDE SYNTHASE; PARVALBUMIN; PROTEIN; PROTEIN KINASE C; RADIOLIGAND; RECEPTOR SUBUNIT; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; CELL SUBPOPULATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DORSAL RHIZOTOMY; FEMALE; GLIA CELL; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; LIGAND BINDING; NEUROCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SENSORY NERVE CELL; SPINAL CORD DORSAL HORN; THORACIC SPINAL CORD;

EID: 0142185330     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(03)00480-9     Document Type: Article

References (63)

1. Aimar P., Pasti L., Carmignoto G., Merighi A. Nitric oxide-producing islet cells modulate the release of sensory neuropeptides in the rat substantia gelatinosa. J Neurosci. 18:1998;10375-10388.
2. Antal M., Freund T.F., Polgar E. Calcium-binding proteins, parvalbumin- and calbindin-D 28k-immunoreactive neurons in the rat spinal cord and dorsal root ganglia a light and electron microscopic study. J Comp Neurol. 295:1990;467-484.
3. Antal M., Polgar E., Chalmers J., Minson J.B., Llewellyn-Smith I., Heizmann C.W., Somogyi P. Different populations of parvalbumin- and calbindin-D28k-immunoreactive neurons contain GABA and accumulate 3H-D-aspartate in the dorsal horn of the rat spinal cord. J Comp Neurol. 314:1991;114-124.
4. Arvidsson U., Riedl M., Chakrabarti S., Lee J.H., Nakano A.H., Dado R.J., Loh H.H., Law P.Y., Wessendorf M.W., Elde R. Distribution and targeting of a mu-opioid receptor (MOR1) in brain and spinal cord. J Neurosci. 15:1995;3328-3341.
5. Bao L., Wang H.F., Cai H.J., Tong Y.G., Jin S.X., Lu Y.J., Grant G., Hökfelt T., Zhang X. Peripheral axotomy induces only very limited sprouting of coarse myelinated afferents into inner lamina II of rat spinal cord. Eur J Neurosci. 16:2002;175-185.
6. Belfrage M., Sollevi A., Segerdahl M., Sjölund K.F., Hansson P. Systemic adenosine infusion alleviates spontaneous and stimulus evoked pain in patients with peripheral neuropathic pain. Anesth Analg. 81:1995;713-717.
7. 1 receptor-mediated inhibition of protein kinase A-induced calcitonin gene-related peptide release from rat trigeminal neurons. Mol Pharmacol. 59:2001;1533-1541.
8. 2 receptors of the substantia gelatinosa are located predominantly on intrinsic neurons an autoradiography study. J Pharmacol Exp Ther. 247:1988;757-764.
9. De Koninck Y., Salter M.W., Henry J.L. Substance P released endogenously by high-intensity sensory stimulation potentiates purinergic inhibition of nociceptive dorsal horn neurons induced by peripheral vibration. Neurosci Lett. 176:1994;128-132.
10. DeLander G.E., Hopkins C.J. Spinal adenosine modulates descending antinociceptive pathways stimulated by morphine. J Pharmacol Exp Ther. 239:1986;88-93.
11. Dolphin A.C., Forda S.R., Scott R.H. Calcium-dependent currents in cultured rat dorsal root ganglion neurones are inhibited by an adenosine analogue. J Physiol. 373:1986;47-61.
12. Ekblom A., Segerdahl M., Sollevi A. Adenosine increases the cutaneous heat pain threshold in healthy volunteers. Acta Anaesthesiol Scand. 39:1995;717-722.
13. Geiger J.D., LaBella F.S., Nagy J.I. Characterization and localization of adenosine receptors in rat spinal cord. J Neurosci. 4:1984;2303-2310.
14. Gilmore S.A., Sims T.J., Leiting J.E. Astrocytic reactions in spinal gray matter following sciatic axotomy. Glia. 3:1990;342-349.
15. 3H]cyclohexyladenosine. J Neurosci. 2:1982;1230-1241.
16. Gu J.G., MacDermott A.B. Activation of ATP P2X receptors elicits glutamate release from sensory neuron synapses. Nature. 389:1997;749-753.
17. Hajos F., Csillik B., Knyihar-Csillik E. Alterations in glial fibrillary acidic protein immunoreactivity in the upper dorsal horn of the rat spinal cord in the course of transganglionic degenerative atrophy and regenerative proliferation. Neurosci Lett. 117:1990;8-13.
18. Hökfelt T, Ljungdahl Å, Terenius L, Elde R, Nilsson G. (1977) Immunohistochemical analysis of peptide pathways possibly related to pain and analgesia: enkephalin and substance P. Proc Natl Acad Sci USA 74:3081-3085.
19. Holmgren M., Hedner J., Mellstrand T., Nordberg G., Hedner T. Characterization of the antinociceptive effects of some adenosine analogues in the rat. Naunyn Schmiedebergs Arch Pharmacol. 334:1986;290-293.
20. Jo Y.H., Schlichter R. Synaptic corelease of ATP and GABA in cultured spinal neurons. Nat Neurosci. 2:1999;241-245.
21. 2 adenosine receptor binding and on mRNA levels in rat brain. Naunyn Schmiedebergs Arch Pharmacol. 347:1993;407-414.
22. 1 receptor. Proc Natl Acad Sci USA. 98:2001;9407-9412.
23. Karlsten R., Gordh T., Post C. Local antinociceptive and hyperalgesic effects in the formalin test after peripheral administration of adenosine analogues in mice. Pharmacol Toxicol. 70:1992;434-438.
24. 1-adenosine receptor. Neurosci Lett. 121:1991;267-270.
25. Kemp T., Spike R.C., Watt C., Todd A.J. The mu-opioid receptor (MOR1) is mainly restricted to neurons that do not contain GABA or glycine in the superficial dorsal horn of the rat spinal cord. Neuroscience. 75:1996;1231-1238.
26. 1 adenosine receptor. Pain. 94:2001;315-324.
27. Lee Y.W., Yaksh T.L. Pharmacology of the spinal adenosine receptor which mediates the antiallodynic action of intrathecal adenosine agonists. J Pharmacol Exp Ther. 277:1996;1642-1648.
28. Li J., Perl E.R. Adenosine inhibition of synaptic transmission in the substantia gelatinosa. J Neurophysiol. 72:1994;1611-1621.
29. MacDonald R.L., Skerritt J.H., Werz M.A. Adenosine agonists reduce voltage-dependent calcium conductance of mouse sensory neurones in cell culture. J Physiol. 370:1986;75-90.
30. 1 adenosine receptor from rat brain. Mol Pharmacol. 40:1991;1-7.
31. Malmberg A.B., Chen C., Tonegawa S., Basbaum A.I. Preserved acute pain and reduced neuropathic pain in mice lacking PKCγ Science. 278:1997;279-283.
32. Mauborgne A., Polienor H., Hamon M., Cesselin F., Bourgoin S. Adenosine receptor-mediated control of in vitro release of pain-related neuropeptides from the rat spinal cord. Eur J Pharmacol. 441:2002;47-55.
33. Millan M.J. The induction of pain an integrative review. Prog Neurobiol. 57:1999;1-164.
34. Miller K.E., Seybold V.S. Comparison of met-enkephalin-, dynorphin A-, and neurotensin-immunoreactive neurons in the cat and rat spinal cords: I. Lumbar cord. J Comp Neurol. 255:1987;293-304.
35. Mori M., Kose A., Tsujino T., Tanaka C. Immunocytochemical localization of protein kinase C subspecies in the rat spinal cord light and electron microscopic study. J Comp Neurol. 299:1990;167-177.
36. Polgar E., Fowler J.H., McGill M.M., Todd A.J. The types of neuron which contain protein kinase C gamma in rat spinal cord. Brain Res. 833:1999;71-80.
37. Popratiloff A., Weinberg R.J., Rustioni A. AMPA receptor subunits underlying terminals of fine-caliber primary afferent fibers. J Neurosci. 16:1996;3363-3372.
38. Reeve A.J., Dickenson A.H. The roles of spinal adenosine receptors in the control of acute and more persistent nociceptive responses of dorsal horn neurones in the anaesthetized rat. Br J Pharmacol. 116:1995;2221-2228.
39. 1-adenosine receptor that is widely expressed in brain and spinal cord. Mol Endocrinol. 5:1991;1037-1048.
40. Reuss M.H., Reuss S. Nitric oxide synthase neurons in the rodent spinal cord: distribution, relation to Substance P fibers, and effects of dorsal rhizotomy. J Chem Neuroanat. 21:2002;181-196.
41. Salter M.W., De Koninck Y., Henry J.L. Physiological roles for adenosine and ATP in synaptic transmission in the spinal dorsal horn. Prog Neurobiol. 41:1993;125-156.
42. 1 receptors mediate the presynaptic inhibition of calcitonin gene-related peptide release by adenosine in the rat spinal cord. Eur J Pharmacol. 231:1993;139-142.
43. Sawynok J. Adenosine receptor activation and nociception. Eur J Pharmacol. 347:1998;1-11.
44. Sawynok J., Reid A., Poon A. Peripheral antinociceptive effect of an adenosine kinase inhibitor, with augmentation by an adenosine deaminase inhibitor, in the rat formalin test. Pain. 74:1998;75-81.
45. Segerdahl M., Ekblom A., Sjölund K.F., Belfrage M., Forsberg C., Sollevi A. Systemic adenosine attenuates touch evoked allodynia induced by mustard oil in humans. Neuroreport. 6:1995;753-756.
46. Segerdahl M., Sollevi A. Adenosine and pain relief: a clinical overview. Drug Development Research. 45:1998;151-158.
47. Silverman J.D., Kruger L. Lectin and neuropeptide labeling of separate populations of dorsal root ganglion neurons and asscoiated nociceptor thin axons in rat testis and cornea whole-mount preparations. Somatosens Res. 5:1988;259-267.
48. Sjölund K.F., Belfrage M., Karlsten R., Segerdahl M., Arner S., Gordh T., Sollevi A. Systemic adenosine infusion reduces the area of tactile allodynia in neuropathic pain following peripheral nerve injury a multi-centre, placebo-controlled study. Eur J Pain. 5:2001;199-207.
49. Sjölund K.F., Sollevi A., Segerdahl M., Lundeberg T. Intrathecal adenosine analog administration reduces substance P in cerebrospinal fluid along with behavioral effects that suggest antinociception in rats. Anesth Analg. 85:1997;627-632.
50. Spike R.C., Kerr R., Maxwell D.J., Todd A.J. GluR1 and GluR2/3 subunits of the AMPA-type glutamate receptor are associated with particular types of neurone in laminae I-III of the spinal dorsal horn of the rat. Eur J Neurosci. 10:1998;324-333.
51. Spike R.C., Puskar Z., Sakamoto H., Stewart W., Watt C., Todd A.J. MOR-1-immunoreactive neurons in the dorsal horn of the rat spinal cord evidence for nonsynaptic innervation by substance P-containing primary afferents and for selective activation by noxious thermal stimuli. Eur J Neurosci. 15:2002;1306-1316.
52. Stein V., Nicoll R.A. GABA generates excitement. Neuron. 37:2003;375-378.
53. Sudhof T.C. The synaptic vesicle cycle a cascade of protein-protein interactions. Nature. 375:1995;645-653.
54. Taiwo Y.O., Levine J.D. Direct cutaneous hyperalgesia induced by adenosine. Neuroscience. 38:1990;757-762.
55. Todd A.J., Spike R.C., Russell G., Johnston H.M. Immunohistochemical evidence that Met-enkephalin and GABA coexist in some neurones in rat dorsal horn. Brain Res. 584:1992;149-156.
56. Valtschanoff J.G., Weinberg R.J., Rustioni A. NADPH diaphorase in the spinal cord of rats. J Comp Neurol. 321:1992;209-222.
57. Wang H., Rivero-Melian C., Robertson B., Grant G. Transganglionic transport and binding of the isolectin B4 from Griffonia simplicifolia I in rat primary sensory neurons. Neuroscience. 62:1994;539-551.
58. Woolf C.J. Windup and central sensitization are not equivalent. Pain. 66:1996;105-108.
59. Woolf C.J., Shortland P., Coggeshall R.E. Peripheral nerve injury triggers central sprouting of myelinated afferents. Nature. 355:1992;75-78.
60. Woolf C.J., Shortland P., Reynolds M., Ridings J., Doubell T., Coggeshall R.E. Reorganization of central terminals of myelinated primary afferents in the rat dorsal horn following peripheral axotomy. J Comp Neurol. 360:1995;121-134.
61. Vulchanova L., Riedl M.S., Shuster S.J., Stone L.S., Hargreaves K.M., Buell G., Surprenant A., North R.A., Elde R. P2X3 is expressed by DRG neurons that terminate in inner lamina II. Eur J Neurosci. 10:1998;3470-3478.
62. Zhang X., de Araujo Lucas G., Elde R., Wiesenfeld-Hallin Z., Hökfelt T. Effect of morphine on cholecystokinin and mu-opioid receptor-like immunoreactivities in rat spinal dorsal horn neurons after peripheral axotomy and inflammation. Neuroscience. 95:2000;197-207.
63. Zhang X., Verge V., Wiesenfeld-Hallin Z., Ju G., Bredt D., Synder S.H., Hökfelt T. Nitric oxide synthase-like immunoreactivity in lumbar dorsal root ganglia and spinal cord of rat and monkey and effect of peripheral axotomy. J Comp Neurol. 335:1993;563-575.