Immunohistochemical localization of histamine H3 receptors in rodent skin, dorsal root ganglia, superior cervical ganglia, and spinal cord: Potential antinociceptive targets

Pain

Volumn 129, Issue 1-2, 2007, Pages 76-92

  Cannon, Keri E ^a   Chazot, Paul L ^b   Hann, Victoria ^b   Shenton, Fiona ^b   Hough, Lindsay B ^a   Rice, Frank L ^a  

^a ALBANY MEDICAL COLLEGE   (United States)

^b DURHAM UNIVERSITY   (United Kingdom)

Author keywords

A fibers; A fibers; Arterial innervation; Calcitonin gene related peptide; H3 receptors; Histamine; Sensory innervation; Substance P

Indexed keywords

ACID SENSING ION CHANNEL; ACID SENSING ION CHANNEL 3; CALCITONIN GENE RELATED PEPTIDE; CATION CHANNEL; HISTAMINE H3 RECEPTOR; NEUROFILAMENT PROTEIN; SUBSTANCE P; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; CONTROLLED STUDY; FEMALE; HAIR FOLLICLE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; KERATINOCYTE; KNOCKOUT MOUSE; MALE; MERKEL CELL; MOUSE; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; RAT; SKIN; SPINAL CORD; SPINAL CORD DORSAL HORN; SPINAL GANGLION; SUPERIOR CERVICAL GANGLION; VIBRISSA;

ANIMALS; GANGLIA, SPINAL; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, HISTAMINE H3; SKIN; SUPERIOR CERVICAL GANGLION;

EID: 34047249428     PISSN: 03043959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pain.2006.09.039     Document Type: Article

References (74)

1. Abercrombie M. Estimation of nuclear population from microtome sections. Anat Rec 94 (1946) 239-247
2. 3) of histamine receptors. Nature 302 (1983) 832-837
3. 3-receptors. Nature 327 (1987) 117-123
4. Bar-Shavit Z., Goldman R., Stabinsky Y., Gottlieb P., Fridkin M., Teichberg V.I., and Blumberg S. Enhancement of phagocytosis - a newly found activity of Substance P residing in its N-terminal tetrapeptide. Biochem Biophys Res Commun 94 (1980) 1445-1451
5. Beck P.W., Handwerker H.O., and Zimmermann M. Nervous outflow from the cat's foot during noxious radiant heat stimulation. Brain Res 67 (1974) 373-386
6. Brain S.D., and Williams T.J. Interactions between tachykinins and calcitonin gene-related peptide lead to the modulation of oedema formation and blood flow in rat skin. Br J Pharmacol 97 (1989) 77-82
7. Brain S.D., Cambridge H., Hughes S.R., and Wilsoncroft P. Evidence that calcitonin gene-related peptide contributes to inflammation in skin and joint. Ann NY Acad Sci 657 (1992) 412-419
8. Burgess P.R., and Perl E.R. Myelinated afferent fibres responding specifically to noxious stimulation of the skin. J Physiol 190 (1967) 541-562
9. 3 receptors. J Pain 6 (2005) 193-200
10. 3 receptors inhibits mechanical nociception. Eur J Pharmacol 470 (2003) 139-147
11. 3 histamine receptor in the mouse brain. Neuroreport 12 (2001) 259-262
12. Chen J., Liu C., and Lovenberg T.W. Molecular and pharmacological characterization of the mouse histamine H(3) receptor. Eur J Pharmacol 467 (2003) 57-65
13. 3 receptor. Biochem J 355 (2001) 279-288
14. Delaunois A., Gustin P., Garbarg M., and Ansay M. Modulation of acetylcholine, capsaicin and substance P effects by histamine H3 receptors in isolated perfused rabbit lungs. Eur J Pharmacol 277 (1995) 243-250
15. Dimitriadou V., Rouleau A., Dam Trung T.M., Newlands G.J., Miller H.R., Luffau G., Schwartz J.C., and Garbarg M. Functional relationship between mast cells and C-sensitive nerve fibres evidenced by histamine H3-receptor modulation in rat lung and spleen. Clin Sci (Lond) 87 (1994) 151-163
16. Dimitriadou V., Rouleau A., Trung T., Newlands G.J., Miller H.R., Luffau G., Schwartz J.C., and Garbarg M. Functional relationships between sensory nerve fibers and mast cells of dura mater in normal and inflammatory conditions. Neuroscience 77 (1997) 829-839
17. 3 receptor isoforms with different brain expression and signaling properties. Mol Pharmacol 59 (2001) 1-8
18. Fitzsimons C., Engel N., Duran H., Policastro L., Cricco G., Martin G., Molinari B., and Rivera E. Histamine production in mouse epidermal keratinocytes is regulated during cellular differentiation. Inflamm Res 50 (2001) S100-S101
19. Fundin B.T., Arvidsson J., Aldskogius H., Johansson O., Rice S.N., and Rice F.L. Comprehensive immunofluorescence and lectin binding analysis of intervibrissal fur innervation in the mystacial pad of the rat. J Comp Neurol 385 (1997) 185-206
20. Fundin B.T., Pfaller K., and Rice F.L. Different distribution of the sensory and autonomic innervation among the microvasculature of the rat mystacial pad. J Comp Neurol 389 (1997) 545-568
21. Fünfschilling U., Ng Y.-G., Zang K., Miyazaki J.K., Reichardt L.F., and Rice F.L. TrkC kinase expression in distinct subsets of cutaneous trigeminal innervation and non-neuronal cells. J Comp Neurol 480 (2004) 392-414
22. Godlewski G., Malinowska B., Buczko W., and Schlicker E. Inhibitory H3 receptors on sympathetic nerves of the pithed rat: activation by endogenous histamine and operation in spontaneously hypertensive rats. Naunyn Schmiedebergs Arch Pharmacol 355 (1997) 261-266
23. Godlewski G., Malinowska B., Schlicker E., and Bucher B. Identification of histamine H3 receptors in the tail artery from normotensive and spontaneously hypertensive rats. J Cardiovasc Pharmacol 29 (1997) 801-807
24. Hartung H.-P., Wolters K., and Tokya K.V. Substance P binding properties and studies on cellular responses in guinea-pig macrophages. J Immunol 136 (1986) 3856-3863
25. Helme R.D., and Andrews P.V. The effect of nerve lesions on the inflammatory response to injury. J Neurosci Res 13 (1985) 453-459
26. Heron A., Rouleau A., Cochois V., Pillot C., Schwartz J.C., and Arrang J.M. Expression analysis of the histamine H(3) receptor in developing rat tissues. Mech Dev 105 (2001) 167-173
27. Hossen M.A., Sugimoto Y., Kayasuga R., and Kamei C. Involvement of histamine H3 receptors in scratching behaviour in mast cell-deficient mice. Br J Dermatol 149 (2003) 17-22
28. Hough L.B. Genomics meets histamine receptors: new subtypes, new receptors. Mol Pharmacol 59 (2001) 1-5
29. Hough L.B., and Leurs R. Histamine. In: Siegel G., Agranoff B., Albers R., Fisher S., and Uhler M. (Eds). Basic neurochemistry. 7nd ed. (2006), Williams and Wilkins, Lippincott 249-266
30. 2 cannabinoid receptor activation produces antinociception by stimulating peripheral release of endogenous opioids. Proc Natl Acad Sci USA 102 (2005) 3093-3098
31. 3-receptor-mediated inhibition of calcitonin gene-related peptide release from cardiac C fibers. A regulatory negative-feedback loop. Circ Res 78 (1996) 863-869
32. Ishikawa S., and Sperelakis N. A novel class (H3) of histamine receptors on perivascular nerve terminals. Nature 327 (1987) 158-160
33. Johnson A.R., and Erdos E.G. Release of histamine from mast cells by vasoactive peptides. Proc Soc Exp Biol Med 142 (1973) 1252-1256
34. Ju G., Hokfelt T., Brodin E., Fahrenkrug J., Fischer J.A., Frey P., Elde R.P., and Brown J.C. Primary sensory neurons of the rat showing calcitonin gene-related peptide immunoreactivity and their relation to substance P-, somatostatin-, galanin-, vasoactive intestinal polypeptide- and cholecystokinin-immunoreactive ganglion cells. Cell Tissue Res 247 (1987) 417-431
35. 3 receptor in the developing CNS and brown fat suggests novel roles for histamine. Mol Cell Neurosci 24 (2003) 614-622
36. Khodorova A., Navarro B., Jouaville L.S., Murphy J.E., Rice F.L., Mazurkiewicz J.E., Long-Woodward D., Stoffel M., Strichartz G.R., Yukhananov R., and Davar G. Endothelin-B receptor activation triggers an endogenous analgesic cascade at sites of peripheral injury. Nat Med 9 (2003) 1055-1061
37. 3 receptor activation inhibits sympathetic-cholinergic responses in cats. Eur J Pharmacol 257 (1994) 109-115
38. 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
39. Lawson S.N., Crepps B., and Perl E.R. Calcitonin gene-related peptide immunoreactivity and afferent receptive properties of dorsal root ganglion neurones in guinea-pigs. J Physiol 540 (2002) 989-1002
40. Lembeck F., and Holzer P. Substance P as neurogenic mediator of antidromic vasodilation and neurogenic plasma extravasation. Naunyn Schmiedebergs Arch Pharmacol 352 (1979) 201-205
41. Light A.R., and Perl E.R. Spinal termination of functionally identified primary afferent neurons with slowly conducting myelinated fibers. J Comp Neurol 186 (1979) 133-150
42. 3 receptor. Mol Pharmacol 55 (1999) 1101-1107
43. McCarthy P.W., and 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
44. Mobarakeh J.I., Sakurada S., Katsuyama S., Kutsuwa M., Kuramasu A., Lin Z.Y., Watanabe T., Hashimoto Y., and Yanai K. Role of histamine H(1) receptor in pain perception: a study of the receptor gene knockout mice. Eur J Pharmacol 391 (2000) 81-89
45. Mobarakeh J.I., Nalwalk J.W., Watanabe T., Sakurada S., Hoffmann M., Leurs R., Timmerman H., Silos-Santiago I., Yanai K., and Hough L.B. Improgan antinociception does not require neuronal histamine or histamine receptors. Brain Res 974 (2003) 146-152
46. Molderings G.J., Weissenborn G., Schlicker E., Likungu J., and Gothert M. Inhibition of noradrenaline release from the sympathetic nerves of the human saphenous vein by presynaptic histamine H3 receptors. Naunyn Schmiedebergs Arch Pharmacol 346 (1992) 46-50
47. Molliver D.C., Immke D.C., Fierro L., Paré M., Rice F.L., and McCleskey E.W. ASIC3, an acid-sensing ion channel, is expressed in metaboreceptive sensory neurons. Mol Pain 1 (2004) 35
48. Nemmar A., Delaunois A., Beckers J.F., Sulon J., Bloden S., and Gustin P. Modulatory effect of imetit, a histamine H3 receptor agonist, on C-fibers, cholinergic fibers and mast cells in rabbit lungs in vitro. Eur J Pharmacol 371 (1999) 23-30
49. 3 receptors. Eur J Pharmacol 273 (1995) 83-88
50. 2-receptor antagonists in acute inflammation. Biochem Soc Trans 8 (1980) 150-155
51. 2- receptors in cutaneous inflammation in the guinea-pig produced by histamine and mast cell degranulation. Br J Pharmacol 69 (1980) 615-623
52. Paré M., Elde R., Mazurkiewicz J.E., Smith A.M., and Rice F.L. The Meissner corpuscle revised: a multiafferented mechanoreceptor with nociceptor immunochemical properties. J Neurosci 21 (2001) 7236-7246
53. Paré M., Smith A.M., and Rice F.L. Distribution and terminal arborizations of cutaneous mechanoreceptors in the glabrous finger pads of the monkey. J Comp Neurol 445 (2002) 347-359
54. Payan D.G., Levine J.D., and Goetzl E.J. Modulation of immunity and hypersensitivity by sensory neuropeptides. J Immunol 132 (1984) 1601-1604
55. Pillot C., Heron A., Cochois V., Tardivel-Lacombe J., Ligneau X., Schwartz J.C., and Arrang J.M. A detailed mapping of the histamine H(3) receptor and its gene transcripts in rat brain. Neuroscience 114 (2002) 173-193
56. 3 receptors in rat brain areas. Neuroscience 52 (1993) 169-189
57. Price M.P., McIlwrath S.L., Xie J., Cheng C., Qiao J., Tarr D.E., Sluka K.A., Brennan T.J., Lewin G.R., and Welsh M.J. The DRASIC cation channel contributes to the detection of cutaneous touch and acid stimuli in mice. Neuron 32 (2001) 1071-1083
58. Rice F.L., and Rasmusson D.D. Innervation of the digit on the forepaw of the raccoon. J Comp Neurol 417 (2000) 467-490
59. Rice F.L., Fundin B.T., Arvidsson J., Aldskogius H., and Johansson O. Comprehensive immunofluorescence and lectin binding analysis of vibrissal follicle sinus complex innervation in the mystacial pad of the rat. J Comp Neurol 385 (1997) 149-184
60. Rice F.L., Albers K.M., Davis B.M., Silos-Santiago I., Wilkinson G.A., LeMaster A.M., Ernfors P.J., Smeyne R.J., Aldskogius H., Phillips H.S., Barbacid M., DeChiara T.M., Yancopoulos G.D., Dunne C.E., and Fundin B.T. Differential effects of various neurotrophin and trk receptor deletions on the unmyelinated innervation of the epidermis in the whisker pad of the mouse. Develop Biol 198 (1998) 57-81
61. Ringkamp M., Peng Y.B., Wu G., Hartke T.V., Campbell J.N., and Meyer R.A. Capsaicin responses in heat-sensitive and heat-insensitive A-fiber nociceptors. J Neurosci 21 (2001) 4460-4468
62. 3 receptor agonist prodrug. J Pharmacol Exp Ther 281 (1997) 1085-1094
63. Rouleau A., Stark H., Schunack W., and Schwartz J.C. Anti-inflammatory and antinociceptive properties of BP 2-94, a histamine H(3)-receptor agonist prodrug. J Pharmacol Exp Ther 295 (2000) 219-225
64. 3 receptor: evidence for multiple isoforms. J Neurochem 90 (2004) 1331-1338
65. Saito A., Kimura S., and Goto K. Calcitonin gene-related peptide as potential neurotransmitter in guinea-pig right atrium. Am J Physiol 250 (1986) H693-H698
66. Saria A. Substance P in sensory nerve fibers contributes to the development of oedema in the rat hindpaw after thermal injury. Br J Pharmacol 323 (1984) 341-342
67. Schmelz M., Schmidt R., Bickel A., Handwerker H.O., and Torebjork H.E. Specific C-receptors for itch in human skin. J Neurosci 17 (1997) 8003-8008
68. Shenton F.C., Hann V., and Chazot P.L. Evidence for native and cloned H3 histamine receptor higher oligomers. Inflammation Res 54 Suppl. 1 (2005) 548-549
69. Sugimoto Y., Iba Y., Nakamura Y., Kayasuga R., and Kamei C. Pruritus-associated response mediated by cutaneous histamine H3 receptors. Clin Exp Allergy 34 (2004) 456-459
70. Szolcsanyi J., Anton F., Reeh P.W., and Handwerker H.O. Selective excitation by capsaicin of mechano-heat sensitive nociceptors in rat skin. Brain Res 446 (1988) 262-268
71. Tardivel-Lacombe J., Rouleau A., Heron A., Morisset S., Pillot C., Cochois V., Schwartz J.C., and Arrang J.M. Cloning and cerebral expression of the guinea pig histamine H3 receptor: evidence for two isoforms. Neuroreport 11 (2000) 755-759
72. Wellendorph P., Goodman M.W., Burstein E.S., Nash N.R., Brann M.R., and Weiner D.M. Molecular cloning and pharmacology of functionally distinct isoforms of the human histamine H(3) receptor. Neuropharmacology 42 (2002) 929-940
73. Yeomans D.C., and Proudfit H.K. Nociceptive responses to high and low rates of noxious cutaneous heating are mediated by different nociceptors in the rat: electrophysiological evidence. Pain 68 (1996) 141-150
74. Zylka M.J., Rice F.L., and Anderson D.J. Axonal tracers targeted to Mrgprd define a nociceptive circuit with exclusive peripheral projections to the epidermis. Neuron 45 (2005) 17-25