Calcitonin receptor-like receptor and receptor activity modifying protein 1 in the rat dorsal horn: Localization in glutamatergic presynaptic terminals containing opioids and adrenergic α2C receptors

Neuroscience

Volumn 148, Issue 1, 2007, Pages 250-265

  Marvizon J C G ^a   Perez O A ^a   Song, B ^a   Chen, W ^a   Bunnett, N W ^b   Grady, E F ^b   Todd, A J ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

adrenergic receptor; calcitonin gene related peptide; CGRP; colocalization; dynorphin; enkephalin

Indexed keywords

ADRENOMEDULLIN RECEPTOR; ALPHA 2C ADRENERGIC RECEPTOR; ANTIBODY; CALCITONIN GENE RELATED PEPTIDE; CALCITONIN GENE RELATED PEPTIDE RECEPTOR; CALCITONIN RECEPTOR LIKE RECEPTOR; ENKEPHALIN; ENKEPHALIN ANTIBODY; GLUTAMIC ACID; ISOPROPAMIDE IODIDE; OPIATE PEPTIDE; RECEPTOR ACTIVITY MODIFYING PROTEIN 1; RECEPTOR ACTIVITY MODIFYING PROTEIN 2; RECEPTOR ACTIVITY MODIFYING PROTEIN 3; SYNAPTOPHYSIN; UNCLASSIFIED DRUG; VESICULAR GLUTAMATE TRANSPORTER 2;

ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; CELL SURFACE; ELECTRON MICROSCOPY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; NERVE ENDING; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PUNCTA; QUANTITATIVE ANALYSIS; RAT; SENSORY NERVE; SPINAL CORD DORSAL HORN;

AFFERENT PATHWAYS; ANALGESICS, OPIOID; ANIMALS; BIOLOGICAL MARKERS; CALCITONIN GENE-RELATED PEPTIDE; GLUTAMIC ACID; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, IMMUNOELECTRON; NOCICEPTORS; POSTERIOR HORN CELLS; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; RATS, WISTAR; RECEPTORS, ADRENERGIC, ALPHA-2; RECEPTORS, CALCITONIN; SPINAL NERVE ROOTS; SYNAPTIC TRANSMISSION; SYNAPTOPHYSIN; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2;

EID: 34547787129     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2007.05.036     Document Type: Article

References (54)

1. Adamson P., Xiang J.Z., Mantzourides T., Brammer M.J., and Campbell I.C. Presynaptic alpha 2-adrenoceptor and kappa-opiate receptor occupancy promotes closure of neuronal (N-type) calcium channels. Eur J Pharmacol 174 (1989) 63-70
2. Arvidsson U., Riedl M., Chakrabarti S., Vulchanova L., Lee J.H., Nakano A.H., Lin X., Loh H.H., Law P.Y., and Wessendorf M.W. The kappa-opioid receptor is primarily postsynaptic: combined immunohistochemical localization of the receptor and endogenous opioids. Proc Natl Acad Sci U S A 92 (1995) 5062-5066
3. Bennett A.D., Chastain K.M., and Hulsebosch C.E. Alleviation of mechanical and thermal allodynia by CGRP(8-37) in a rodent model of chronic central pain. Pain 86 (2000) 163-175
4. Costes S.V., Daelemans D., Cho E.H., Dobbin Z., Pavlakis G., and Lockett S. Automatic and quantitative measurement of protein-protein colocalization in live cells. Biophys J 86 (2004) 3993-4003
5. Cottrell G.S., Roosterman D., Marvizon J.C., Song B., Wick E., Pikios S., Wong H., Berthelier C., Tang Y., Sternini C., Bunnett N.W., and Grady E.F. Localization of calcitonin receptor-like receptor and receptor activity modifying protein 1 in enteric neurons, dorsal root ganglia, and the spinal cord of the rat. J Comp Neurol 490 (2005) 239-255
6. Cuello A.C., Milstein C., Couture R., Wright B., Priestley J.V., and Jarvis J. Characterization and immunocytochemical application of monoclonal antibodies against enkephalins. J Histochem Cytochem 32 (1984) 947-957
7. De Felipe C., Herrero J.F., O'Brien J.A., Palmer J.A., Doyle C.A., Smith A.J., Laird J.M., Belmonte C., Cervero F., and Hunt S.P. Altered nociception, analgesia and aggression in mice lacking the receptor for substance P. Nature 392 (1998) 394-397
8. Dolphin A.C. G protein modulation of voltage-gated calcium channels. Pharmacol Rev 55 (2003) 607-627
9. Foord S.M., and Craig R.K. Isolation and characterisation of a human calcitonin-gene-related-peptide receptor. Eur J Biochem 170 (1987) 373-379
10. Franco-Cereceda A., Henke H., Lundberg J.M., Petermann J.B., Hokfelt T., and 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 8 (1987) 399-410
11. Garry M.G., Walton L.P., and Davis M.A. Capsaicin-evoked release of immunoreactive calcitonin gene-related peptide from the spinal cord is mediated by nitric oxide but not by cyclic GMP. Brain Res 861 (2000) 208-219
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., and Evans R.M. Calcitonin gene-related peptide immunoreactivity in the spinal cord of man and of eight other species. J Neurosci 4 (1984) 3101-3111
13. Gramsch C., Meo T., Riethmuller G., and Herz A. Binding characteristics of a monoclonal beta-endorphin antibody recognizing the N-terminus of opioid peptides. J Neurochem 40 (1983) 1220-1226
14. Hay D.L., Howitt S.G., Conner A.C., Schindler M., Smith D.M., and Poyner D.R. CL/RAMP2 and CL/RAMP3 produce pharmacologically distinct adrenomedullin receptors: a comparison of effects of adrenomedullin22-52, CGRP8-37 and BIBN4096BS. Br J Pharmacol 140 (2003) 477-486
15. Husmann K., Born W., Fischer J.A., and Muff R. Three receptor-activity-modifying proteins define calcitonin gene-related peptide or adrenomedullin selectivity of the mouse calcitonin-like receptor in COS-7 cells. Biochem Pharmacol 66 (2003) 2107-2115
16. Kawamura M., Kuraishi Y., Minami M., and Satoh M. Antinociceptive effect of intrathecally administered antiserum against calcitonin gene-related peptide on thermal and mechanical noxious stimuli in experimental hyperalgesic rats. Brain Res 497 (1989) 199-203
17. Knaus P., and Betz H. Mapping of a dominant immunogenic region of synaptophysin, a major membrane protein of synaptic vesicles. FEBS Lett 261 (1990) 358-360
18. Li J.L., Fujiyama F., Kaneko T., and Mizuno N. Expression of vesicular glutamate transporters, VGluT1 and VGluT2, in axon terminals of nociceptive primary afferent fibers in the superficial layers of the medullary and spinal dorsal horns of the rat. J Comp Neurol 457 (2003) 236-249
19. + channels in caudal raphe neurons. Neuroscience 82 (1998) 753-765
20. Ma W., Chabot J.G., and Quirion R. A role for adrenomedullin as a pain-related peptide in the rat. Proc Natl Acad Sci U S A 103 (2006) 16027-16032
21. Malcangio M., and Bowery N.G. Calcitonin gene-related peptide content, basal outflow and electrically-evoked release from monoarthritic rat spinal cord in vitro. Pain 66 (1996) 351-358
22. Mantyh P.W., DeMaster E., Malhotra A., Ghilardi J.R., Rogers S.D., Mantyh C.R., Liu H., Basbaum A.I., Vigna S.R., and Maggio J.E. Receptor endocytosis and dendrite reshaping in spinal neurons after somatosensory stimulation. Science 268 (1995) 1629-1632
23. Mantyh P.W., Rogers S.D., Honore P., Allen B.J., Ghilardi J.R., Li J., Daughters R.S., Lappi D.A., Wiley R.G., and Simone D.A. Inhibition of hyperalgesia by ablation of lamina I spinal neurons expressing the substance P receptor. Science 278 (1997) 275-279
24. Marvizon J.C.G., McRoberts J.A., Ennes H.S., Song B., Wang X., Jinton L., Corneliussen B., and Mayer E.A. Two NMDA receptors in rat dorsal root ganglia with different subunit composition and localization. J Comp Neurol 446 (2002) 325-341
25. Marvizon J.C., Song B., Grady E., and Bunnett N. CGRP receptors inhibit opioid release in the rat spinal cord. Soc Neurosci Abstr 982 (2005) 919
26. Marvizon J.C., Martinez V., Grady E.F., Bunnett N.W., and Mayer E.A. Neurokinin 1 receptor internalization in spinal cord slices induced by dorsal root stimulation is mediated by NMDA receptors. J Neurosci 17 (1997) 8129-8136
27. McLatchie L.M., Fraser N.J., Main M.J., Wise A., Brown J., Thompson N., Solari R., Lee M.G., and Foord S.M. RAMPs regulate the transport and ligand specificity of the calcitonin-receptor-like receptor. Nature 393 (1998) 333-339
28. Olave M.J., and Maxwell D.J. An investigation of neurones that possess the alpha 2C-adrenergic receptor in the rat dorsal horn. Neuroscience 115 (2002) 31-40
29. Olave M.J., and Maxwell D.J. Axon terminals possessing the alpha 2c-adrenergic receptor in the rat dorsal horn are predominantly excitatory. Brain Res 965 (2003) 269-273
30. Ribeiro-da-Silva A. Ultrastructural features of the colocalization of calcitonin gene related peptide with substance P or somatostatin in the dorsal horn of the spinal cord. Can J Physiol Pharmacol 73 (1995) 940-944
31. Ribeiro-da-Silva A., and Coimbra A. Two types of synaptic glomeruli and their distribution in laminae I-III of the rat spinal cord. J Comp Neurol 209 (1982) 176-186
32. Roh J., Chang C.L., Bhalla A., Klein C., and Hsu S.Y. Intermedin is a calcitonin/calcitonin gene-related peptide family peptide acting through the calcitonin receptor-like receptor/receptor activity-modifying protein receptor complexes. J Biol Chem 279 (2004) 7264-7274
33. Shindler K.S., and Roth K.A. Double immunofluorescent staining using two unconjugated primary antisera raised in the same species. J Histochem Cytochem 44 (1996) 1331-1335
34. Sillevis Smitt P.A., van der L.C., Vianney de Jong J.M., and Troost D. Tissue fixation methods alter the immunohistochemical demonstrability of neurofilament proteins, synaptophysin, and glial fibrillary acidic protein in human cerebellum. Acta Histochem 95 (1993) 13-21
35. Song B., and Marvizon J.C. Peptidases prevent mu-opioid receptor internalization in dorsal horn neurons by endogenously released opioids. J Neurosci 23 (2003) 1847-1858
36. Song B., and Marvizon J.C.G. Dorsal horn neurons firing at high frequency, but not primary afferents, release opioid peptides that produce μ-opioid receptor internalization in the rat spinal cord. J Neurosci 23 (2003) 9171-9184
37. Spike R.C., Watt C., Zafra F., and Todd A.J. An ultrastructural study of the glycine transporter GLYT2 and its association with glycine in the superficial laminae of the rat spinal dorsal horn. Neuroscience 77 (1997) 543-551
38. Spike R.C., Puskar Z., Sakamoto H., Stewart W., Watt C., and 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
39. Stangl D., Born W., and Fischer J.A. Characterization and photoaffinity labeling of a calcitonin gene-related peptide receptor solubilized from human cerebellum. Biochemistry 30 (1991) 8605-8611
40. Stone L.S., Broberger C., Vulchanova L., Wilcox G.L., Hokfelt T., Riedl M.S., and Elde R. Differential distribution of alpha(2A) and alpha(2C) adrenergic receptor immunoreactivity in the rat spinal cord. J Neurosci 18 (1998) 5928-5937
41. Stucky C.L., and Lewin G.R. Isolectin B(4)-positive and -negative nociceptors are functionally distinct. J Neurosci 19 (1999) 6497-6505
42. Todd A.J. GABA and glycine in synaptic glomeruli of the rat spinal dorsal horn. Eur J Neurosci 8 (1996) 2492-2498
43. Todd A.J., and Spike R.C. The localization of classical transmitters and neuropeptides within neurons in laminae I-III of the mammalian spinal dorsal horn. Prog Neurobiol 41 (1993) 609-645
44. Todd A.J., Hughes D.I., Polgar E., Nagy G.G., Mackie M., Ottersen O.P., and Maxwell D.J. The expression of vesicular glutamate transporters VGLUT1 and VGLUT2 in neurochemically defined axonal populations in the rat spinal cord with emphasis on the dorsal horn. Eur J Neurosci 17 (2003) 13-27
45. Traub R.J. The spinal contribution of substance P to the generation and maintenance of inflammatory hyperalgesia in the rat. Pain 67 (1996) 151-161
46. Tsou K., Khachaturian H., Akil H., and Watson S.J. Immunocytochemical localization of pro-opiomelanocortin-derived peptides in the adult rat spinal cord. Brain Res 378 (1986) 28-35
47. Tuchscherer M.M., and Seybold V.S. A quantitative study of the coexistence of peptides in varicosities within the superficial laminae of the dorsal horn of the rat spinal cord. J Neurosci 9 (1989) 195-205
48. Van Rossum D., Hanisch U.K., and Quirion R. Neuroanatomical localization, pharmacological characterization and functions of CGRP, related peptides and their receptors. Neurosci Biobehav Rev 21 (1997) 649-678
49. Wiesenfeld-Hallin Z., Hokfelt T., Lundberg J.M., Forssmann W.G., Reinecke M., Tschopp F.A., and Fischer J.A. Immunoreactive calcitonin gene-related peptide and substance P coexist in sensory neurons to the spinal cord and interact in spinal behavioral responses of the rat. Neurosci Lett 52 (1984) 199-204
50. Wimalawansa S.J., Gunasekera R.D., and Zhang F. Isolation, purification, and characterization of calcitonin gene-related peptide receptor. Peptides 14 (1993) 691-699
51. Wong H.C., Tache Y., Lloyd K.C., Yang H., Sternini C., Holzer P., and Walsh J.H. Monoclonal antibody to rat alpha-CGRP: production, characterization, and in vivo immunoneutralization activity. Hybridoma 12 (1993) 93-106
52. Ye Z., Wimalawansa S.J., and Westlund K.N. Receptor for calcitonin gene-related peptide: localization in the dorsal and ventral spinal cord. Neuroscience 92 (1999) 1389-1397
53. Yu L.C., Hansson P., and Lundeberg T. The calcitonin gene-related peptide antagonist CGRP8-37 increases the latency to withdrawal responses in rats. Brain Res 653 (1994) 223-230
54. Zhang L., Hoff A.O., Wimalawansa S.J., Cote G.J., Gagel R.F., and Westlund K.N. Arthritic calcitonin/alpha calcitonin gene-related peptide knockout mice have reduced nociceptive hypersensitivity. Pain 89 (2001) 265-273