Localization of central cannabinoid CB1 receptor messenger RNA in neuronal subpopulations of rat dorsal root ganglia: A double-label in situ hybridization study

Neuroscience

Volumn 90, Issue 3, 1999, Pages 923-931

  Hohmann, A G ^a   Herkenham, M ^a  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

Anandamide; CGRP; Digoxigenin; Dorsal root ganglia; Somatostatin; Substance P

Indexed keywords

ALPHA CALCITONIN GENE RELATED PEPTIDE; CANNABINOID RECEPTOR; DIGOXIGENIN; HORMONE PRECURSOR; MESSENGER RNA; NEUROPEPTIDE; PREPROTACHYKININ; SOMATOSTATIN; SUBSTANCE P; SULFUR 35;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL SIZE; CELL SUBPOPULATION; CONTROLLED STUDY; IN SITU HYBRIDIZATION; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SPINAL GANGLION;

ANIMALS; CALCITONIN GENE-RELATED PEPTIDE; GANGLIA, SPINAL; HISTOCYTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; NEURONS; PHENOTYPE; PROTEIN PRECURSORS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CANNABINOID; RECEPTORS, DRUG; RNA, MESSENGER; SOMATOSTATIN; TACHYKININS; TISSUE DISTRIBUTION;

EID: 0032940633     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(98)00524-7     Document Type: Article

References (61)

1. Amara S. G., Arriza J. L., Leff S. E., Swanson L. W., Evans R. M., Rosenfeld M. G. Expression in brain of a messenger RNA encoding a novel neuropeptide homologous to calcitonin gene-related peptide. Science. 229:1985;1094-1097.
2. Basbaum A. I., Gautron M., Jazat F., Mayes M., Guilbaud G. The spectrum of fiber loss in a model of neuropathic pain in the rat: an electron microscopic study. Pain. 47:1991;359-367.
3. Bennett G. J., Xie Y. K. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain. 33:1988;87-107.
4. Buckley N. E., Hansson S., Harta G., Mezey E. Expression of the CB1 and CB2 receptor messenger RNAs during embryonic development in the rat. Neuroscience. 82:1998;1131-1149.
5. Calzà L., Pozza M., Zanni M., Manzini C. U., Manzini E., Hökfelt T. Peptide plasticity in primary sensory neurons and spinal cord during adjuvant-induced arthritis in the rat: an immunocytochemical and in situ hybridization study. Neuroscience. 82:1998;575-589.
6. Carlton S. M., Dougherty P. M., Pover C. M., Coggeshall R. E. Neuroma formation and numbers of axons in a rat model of experimental peripheral neuropathy. Neurosci. Lett. 131:1991;88-92.
7. Deadwyler S. A., Hampson R. E., Mu J., Whyte A., Childers S. Cannabinoids modulate voltage sensitive potassium A-current in hippocampal neurons via a cAMP-dependent process. J. Pharmac. exp. Ther. 273:1995;734-743.
8. Galeazza M. T., Garry M. G., Yost H. J., Strait K. A., Hargreaves K. M., 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.
9. Gautron M., Jazat F., Ratinahirana H., Hauw J. J., Guilbaud G. Alterations in myelinated fibres in the sciatic nerve of rats after constriction: possible relationships between the presence of abnormal small myelinated fibres and pain-related behaviour. Neurosci. Lett. 111:1990;28-33.
10. Gerfen C. R., Engber T. M., Mahan L. C., Susel Z., Chase T. N., Monsma F. J. Jr., Sibley D. R. D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. Science. 250:1990;1429-1432.
11. Gerfen C. R., Young W. S. III Distribution of striatonigral and striatopallidal peptidergic neurons in both patch and matrix compartments: an in situ hybridization histochemistry and fluorescent retrograde tracing study. Brain Res. 460:1988;161-167.
12. Gibson S. J., Polak J. M., Bloom S. R., Sabate I. M., Mulderry P. M., Ghatei M. A., McGregor G. P., Morrison J. F., Kelly J. S., Evans R. M., Rosenfeld M. G. Calcitonin gene-related peptide immunoreactivity in the spinal cord of man and of eight other species. J. Neurosci. 4:1984;3101-3111.
13. Gifford A. N., Ashby C. R. Jr. Electrically evoked acetylcholine release from hippocampal slices is inhibited by the cannabinoid receptor agonist, WIN 55212-2, and is potentiated by the cannabinoid antagonist, SR 141716A. J. Pharmac. exp. Ther. 277:1996;1431-1436.
14. Gifford A. N., Samiian L., Gatley S. J., Ashby C. R. Jr. Examination of the effect of the cannabinoid receptor agonist, CP 55,940, on electrically evoked transmitter release from rat brain slices. Eur. J. Pharmac. 324:1997;187-192.
15. Goodman R. H., Montminy M. R., Low M. J., Habener J. F. Biosynthesis of rat preprosomatostatin. Adv. exp. Med. Biol. 188:1985;31-47.
16. Herkenham M., Lynn A. B., de Costa B. R., Richfield E. K. Neuronal localization of cannabinoid receptors in the basal ganglia of the rat. Brain Res. 547:1991;267-274.
17. Herkenham M., Lynn A. B., Johnson M. R., Melvin L. S., de Costa B. R., Rice K. C. Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J. Neurosci. 11:1991;563-583.
18. Herzberg U., Eliav E., Bennett G. J., Kopin I. J. The analgesic effects of R(+)-WIN 55,212-2 mesylate, a high affinity cannabinoid agonist, in a rat model of neuropathic pain. Neurosci. Lett. 221:1997;157-160.
19. Hohmann A. G., Herkenham M. Regulation of cannabinoid and mu opioid receptor binding sites following neonatal capsaicin treatment. Neurosci. Lett. 252:1998;13-16.
20. Hohmann A. G., Martin W. J., Tsou K., Walker J. M. Inhibition of noxious stimulus-evoked activity of spinal cord dorsal horn neurons by the cannabinoid WIN55,212-2. Life Sci. 56:1995;2111-2118.
21. Hohmann A. G., Tsou K., Walker J. M. Cannabinoid modulation of wide dynamic range neurons in the lumbar dorsal horn of the rat by spinally administered WIN55,212-2. Neurosci. Lett. 257:1998;119-122.
22. Ishac E. J., Jiang L., Lake K. D., Varga K., Abood M. E., Kunos G. Inhibition of exocytotic noradrenaline release by presynaptic cannabinoid CB1 receptors on peripheral sympathetic nerves. Br. J. Pharmac. 118:1996;2023-2028.
23. Kajander K. C., Bennett G. J. Onset of a painful peripheral neuropathy in rat: a partial and differential deafferentation and spontaneous discharge in A-β and A-δ primary afferent neurons. J. Neurophysiol. 68:1992;734-744.
24. Kiyama H., Emson P. C. Distribution of somatostatin mRNA in the rat nervous system as visualized by a novel non-radioactive in situ hybridization histochemistry procedure. Neuroscience. 38:1990;223-244.
25. Krause J. E., Chirgwin J. M., Carter M. S., Xu Z. S., Hershey A. D. Three rat preprotachykinin mRNAs encode the neuropeptides substance P and neurokinin A. Proc. natn. Acad. Sci. U.S.A. 84:1987;881-885.
26. Lawson S. N. Neuropeptides in morphologically and functionally identified primary afferent neurons in dorsal root ganglia: substance P, CGRP and somatostatin. Prog. Brain Res. 104:1995;161-173.
27. Lawson S. N. Peptides and cutaneous polymodal nociceptor neurones. Prog. Brain Res. 113:1996;369-385.
28. Lichtman A. H., Martin B. R. Spinal and supraspinal components of cannabinoid-induced antinociception. J. Pharmac. exp. Ther. 258:1991;517-523.
29. Mackie K., Hille B. Cannabinoids inhibit N-type calcium channels in neuroblastoma-glioma cells. Proc. natn. Acad. Sci. U.S.A. 89:1992;3825-3829.
30. Mackie K., Lai Y., Westenbroek R., Mitchell R. Cannabinoids activate an inwardly rectifying potassium conductance and inhibit Q-type calcium currents in AtT20 cells transfected with rat brain cannabinoid receptor. J. Neurosci. 15:1995;6552-6561.
31. Maekawa K., Minami M., Masuda T., Satoh M. Expression of μ- and κ-, but not δ-, opioid receptor mRNAs is enhanced in the spinal dorsal horn of the arthritic rats. Pain. 64:1996;365-371.
32. Mailleux P., Vanderhaeghen J. J. Distribution of neuronal cannabinoid receptor in the adult rat brain: a comparative receptor binding radioautography and in situ hybridization histochemistry. Neuroscience. 48:1992;655-668.
33. Mailleux P., Vanderhaeghen J. J. Localization of cannabinoid receptor in the human developing and adult basal ganglia. Higher levels in the striatonigral neurons. Neurosci. Lett. 148:1992;173-176.
34. Martin W. J., Hohmann A. G., Walker J. M. Suppression of noxious stimulus-evoked activity in the ventral posterolateral nucleus of the thalamus by a cannabinoid agonist: correlation between electrophysiological and antinociceptive effects. J. Neurosci. 16:1996;6601-6611.
35. Matsuda L. A., Bonner T. I., Lolait S. J. Localization of cannabinoid receptor mRNA in rat brain. J. comp. Neurol. 327:1993;535-550.
36. Matsuda L. A., Lolait S. J., Brownstein M. J., Young A. C., Bonner T. I. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature. 346:1990;561-564.
37. McCarthy P. W., Lawson S. N. Cell type and conduction velocity of rat primary sensory neurons with substance P-like immunoreactivity. Neuroscience. 28:1989;745-753.
38. McCarthy P. W., Lawson S. N. Cell type and conduction velocity of rat primary sensory neurons with calcitonin gene-related peptide-like immunoreactivity. Neuroscience. 34:1990;623-632.
39. Miller M. A., Kolb P. E., Raskind M. A. A method for simultaneous detection of multiple mRNAs using digoxigenin and radioisotopic cRNA probes. J. Histochem. Cytochem. 41:1993;1741-1750.
40. Minami M., Maekawa K., Yabuuchi K., Satoh M. Double in situ hybridization study on coexistence of μ-, δ- and κ-opioid receptor mRNAs with preprotachykinin A mRNA in the rat dorsal root ganglia. Brain Res. molec. Brain Res. 30:1995;203-210.
41. Nagy J. I., Hunt S. P. Fluoride-resistant acid phosphatase-containing neurones in dorsal root ganglia are separate from those containing substance P or somatostatin. Neuroscience. 7:1982;89-97.
42. Nahin R. L., Ren K., De Leon M., Ruda M. Primary sensory neurons exhibit altered gene expression in a rat model of neuropathic pain. Pain. 58:1994;95-108.
43. Noguchi K., Senba E., Morita Y., Sato M., Tohyama M. Co-expression of alpha-CGRP and beta-CGRP mRNAs in the rat dorsal root ganglion cells. Neurosci. Lett. 108:1990;1-5.
44. Paxinos G. and Watson C. (1986) The Rat Brain in Stereotaxic Coordinates, 2nd edn. Academic, Sydney.
45. Priestley J. V., Rethelyi M., Lund P. K. Semi-quantitative analysis of somatostatin mRNA distribution in the rat central nervous system using in situ hybridization. J. chem. Neuroanat. 4:1991;131-153.
46. Réthelyi M., Metz C. B., Lund P. K. Distribution of neurons expressing calcitonin gene-related peptide mRNAs in the brain stem, spinal cord and dorsal root ganglia of rat and guinea-pig. Neuroscience. 29:1989;225-239.
47. Richardson J. D., Aanonsen L., Hargreaves K. M. Antihyperalgesic effects of spinal cannabinoids. Eur. J. Pharmac. 345:1998;145-153.
48. Richardson J. D., Aanonsen L., Hargreaves K. M. Hypoactivity of the spinal cannabinoid system results in NMDA-dependent hyperalgesia. J. Neurosci. 18:1998;451-457.
49. Richardson J. D., Kilo S., Hargreaves K. M. Cannabinoids reduce hyperalgesia and inflammation via interaction with peripheral CB1 receptors. Pain. 75:1998;111-119.
50. Shen M., Piser T. M., Seybold V. S., Thayer S. A. Cannabinoid receptor agonists inhibit glutamatergic synaptic transmission in rat hippocampal cultures. J. Neurosci. 16:1996;4322-4334.
51. Tal M., Eliav E. Abnormal discharge originates at the site of nerve injury in experimental constriction neuropathy (CCI) in the rat. Pain. 64:1996;511-518.
52. Thorat S. N., Bhargava H. N. Effects of NMDA receptor blockade and nitric oxide synthase inhibition on the acute and chronic actions of delta 9-tetrahydrocannabinol in mice. Brain Res. 667:1994;77-82.
53. Tsou K., Brown S., Sanudo-Pena M. C., Mackie K., Walker J. M. Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience. 83:1998;393-411.
54. Tsou K., Lowitz K. A., Hohmann A. G., Martin W. J., Hathaway C. B., Bereiter D. A., Walker J. M. Suppression of noxious stimulus-evoked expression of FOS protein-like immunoreactivity in rat spinal cord by a selective cannabinoid agonist. Neuroscience. 70:1996;791-798.
55. Twitchell W., Brown S., Mackie K. Cannabinoids inhibit N- and P/Q-type calcium channels in cultured rat hippocampal neurons. J. Neurophysiol. 78:1997;43-50.
56. Uhl G. R., Sasek C. A. Somatostatin mRNA: regional variation in hybridization densities in individual neurons. J. Neurosci. 6:1986;3258-3264.
57. Wanaka A., Shiotani Y., Kiyama H., Matsuyama T., Kamada T., Shiosaka S., Tohyama M. Glutamate-like immunoreactive structures in primary sensory neurons in the rat detected by a specific antiserum against glutamate. Expl Brain Res. 65:1987;691-694.
58. Warden M. K., Young W. S. III Distribution of cells containing mRNAs encoding substance P and neurokinin B in the rat central nervous system. J. comp. Neurol. 272:1988;90-113.
59. Whitfield H. J. Jr., Brady L. S., Smith M. A., Mamalaki E., Fox R. J., Herkenham M. Optimization of cRNA probe in situ hybridization methodology for localization of glucocorticoid receptor mRNA in rat brain: a detailed protocol. Cell. molec. Neurobiol. 10:1990;145-157.
60. Yaksh T. L. The antinociceptive effects of intrathecally administered levonantradol and desacetyllevonantradol in the rat. J. clin. Pharmac. 21:1981;334S-340S.
61. Yin K. J. Distribution of somatostatin mRNA containing neurons in the primary pain relaying nuclei of the rat. Anat. Rec. 241:1995;579-584.