Roles of TRPV1 and neuropeptidergic receptors in dorsal root reflex-mediated neurogenic inflammation induced by intradermal injection of capsaicin

Molecular Pain

Volumn 3, Issue , 2007, Pages

  Lin, Qing ^a   Li, Dingge ^a   Xu, Xijin ^a   Zou, Xiaoju ^a,b   Fang, Li ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

^b NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BICUCULLINE; CALCITONIN GENE RELATED PEPTIDE; CAPSAICIN; CAPSAZEPINE; NEUROKININ 1 RECEPTOR; NEUROPEPTIDE RECEPTOR; SPANTIDE; SUBSTANCE P; VANILLOID RECEPTOR 1; 4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; ANALGESIC AGENT; CALCITONIN GENE RELATED PEPTIDE (8 37); CALCITONIN GENE-RELATED PEPTIDE (8-37); DRUG DERIVATIVE; PEPTIDE FRAGMENT; TRPV1 PROTEIN, RAT; UNCLASSIFIED DRUG; VANILLOID RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DORSAL ROOT; HINDLIMB; MALE; NEUROGENIC INFLAMMATION; NOCICEPTIVE RECEPTOR; NONHUMAN; PERIPHERAL EDEMA; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECRETION; RAT; RHIZOTOMY; VASODILATATION; ANIMAL; CHEMICALLY INDUCED DISORDER; DRUG EFFECT; DRUG POTENTIATION; EDEMA; INTRADERMAL DRUG ADMINISTRATION; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; REFLEX; SPINAL ROOT;

ANALGESICS; ANIMALS; BICUCULLINE; CALCITONIN GENE-RELATED PEPTIDE; CAPSAICIN; EDEMA; GABA ANTAGONISTS; INJECTIONS, INTRADERMAL; NEUROGENIC INFLAMMATION; PEPTIDE FRAGMENTS; RATS; RECEPTORS, NEUROKININ-1; REFLEX; SPINAL NERVE ROOTS; SUBSTANCE P; TRPV CATION CHANNELS; VASODILATION;

EID: 37849045582     PISSN: 17448069     EISSN: None     Source Type: Journal    
DOI: 10.1186/1744-8069-3-30     Document Type: Article

References (68)

1. Richardson JD Vasko MR Cellular mechanisms of neurogenic inflammation J Pharmacol Exp Ther 2002, 302:839-845 10.1124/jpet.102.032797 12183638
2. Willis WD Coggeshall RE Sensory mechanisms of the spinal cord New York: Plenum 2004
3. Herbert MK Holzer P Neurogenic inflammation. II. pathophysiology and clinical implications Anasthesiol Intensivmed Notfallmed Schmerzther 2002, 37:386-394 10.1055/s-2002-32701 12101511
4. Jancso N Jancso-Gabor A Szolcsanyi J Direct evidence for neurogenic inflammation and its prevention by denervation and pretreatment with capsaicin Br J Pharmacol 1967, 31:138-151
5. Holzer P Capsaicin: Cellular targets, mechanisms of action, and selectivity for thin sensory neurons Pharmacol Rev 1991, 43:143-201 1852779
6. Holzer P Capsaicin-sensitive nerves in the control of vascular effector mechanisms Capsaicin in the Study of Pain London: Academic Press Wood JN 1993:191-218
7. Szolcsanyi J Neurogenic inflammation: Reevaluation of axon reflex theory Neurogenic inflammation New York: CRC Press Geppetti P, Holzer P 1996:33-42
8. Wall PD The textbook of Pain London: W.B. Saunders, 1999
9. Cervero F Laird JM Mechanisms of touch-evoked pain (allodynia): A new model Pain 1996, 68:13-23 10.1016/S0304-3959(96)03165-X 9251994
10. Rudomin P Schmidt RF Presynaptic inhibition in the vertebral spinal cord revisited Exp Brain Res 1999, 129:1-37 10.1007/s002210050933 10550500
11. Willis WD Dorsal root potentials and dorsal root reflexes: A double-edged sword Exp Brain Res 1999, 124:395-421 10.1007/s002210050637 10090653
12. Eccles JC Schmidt RF Willis WD Pharmacological studies on presynaptic inhibition J Physiol (Lond) 1963, 168:500-530 1359437 14067941
13. Willis WD Sluka KA Rees H Westlund KN A contribution of dorsal root reflexes to peripheral inflammation Presynaptic inhibition and neural control New York: Oxford University Press Rudomin P, Romo R, Mendell LM 1998:407-423
14. Cervero F Laird JM Garcia-Nicas E Secondary hyperalgesia and presynaptic inhibition: An update Eur J Pain 2003, 7:345-351 10.1016/ S1090-3801(03)00047-8 12821405
15. Lin Q A contribution of dorsal root reflexes to neurogenic inflammation and pain Experimental Pathological Pain: From Molecules to Brain Functions Beijing: Science Press Chen J, Chen, CAN, Han JS, Willis WD 2003:36-56
16. Lin Q Cervero F Schmelz M Pathophysiology of neurogenic inflammation Proceedings of the 11th World Congress on Pain Seattle: IASP Press Flor H, Kalso E, Dostrovsky JO 2006:155-168
17. Lin Q Wu J Willis WD Dorsal root reflexes and cutaneous neurogenic inflammation following intradermal injection of capsaicin in rats J Neurophysiol 1999, 82:2602-2611 10561430
18. Lin Q Zou X Willis WD Aδ and C primary afferents convey dorsal root reflexes after intradermal injection of capsaicin in rats J Neurophysiol 2000, 84:2695-2698 11068011
19. +-2Cl- cotransporter in the development of capsaicin-induced neurogenic inflammation J Neurophysiol 2006, 95:3553-3561 10.1152/jn.01091.2005 16709721
20. Garcia-Nicas E Laird J Cervero F Vasodilatation in hyperalgesic rat skin evoked by stimulation of afferent Aβ-fibers: Further evidence for a role of dorsal root reflexes in allodynia Pain 2001, 94:283-291 10.1016/ S0304-3959(01)00365-7 11731065
21. Weng H-R Dougherty PM Response properties of dorsal root reflexes in cutaneous C fibers before and after intradermal capsaicin injection in rats Neuroscience 2005, 132:823-831 10.1016/j.neuroscience.2005.01.039 15837142
22. 2 but not substance P release induced by antidromic nerve stimulation from rat skin in vitro Neuroscience 1999, 89:303-310 10.1016/S0306-4522(98)00280-2 10051237
23. Lam FY Ferrell WR Acute inflammation in the rat knee joint attenuates sympathetic vasoconstriction but enhances neuropeptides-mediated vasodilation assessed by laser doppler perfusion imaging Neuroscience 1993, 52:443-449 10.1016/0306-4522(93)90170-K 7680789
24. Lewin GR Lisney SJW Mendell LM Neonatal anti-NGF treatment reduces the A delta and C fiber evoked vasodilator responses in rat skin: Evidence that nociceptor afferents mediate antidromic dilatation Eur J Neurosci 1992, 4:1213-1218 10.1111/j.1460-9568.1992.tb00146.x 12106384
25. Lewin GR Ritter AM Mendell LM On the role of nerve growth factor in the development of myelinated nociceptors J Neurosci 1992, 12:1896-1905 1578276
26. Scott DT Lam FY Ferrell WR Acute-inflammation enhances substance P-induced plasma-protein extravasation in the rat knee joint Regul Pept 1992, 39:227-235 10.1016/0167-0115(92)90543-4 1279754
27. Lin Q Ren Y Zou X Fang L Willis WD Dorsal root reflexes mediate neuropeptide - induced cutaneous inflammation following intradermal injection of capsaicin [abstract] Society for Neuroscience San Diego 2004 Program No. 290.12.
28. Lin Q Zou X Fang L Willis WD Sympathetic modulation of acute cutaneous flare induced by intradermal injection of capsaicin in anesthetized rats J Neurophysiol 2003, 89:853-861 10.1152/jn.00568.2002 12574463
29. Wang J Ren Y Zou X Fang L Willis WD Lin Q Sympathetic influence on capsaicin-evoked enhancement of dorsal root reflexes in rats J Neurophysiol 2004, 92:2017-2026 10.1152/jn.00145.2004 15163667
30. Gibbins IL Furness JB Costa M MacIntyre I Hillyard CJ Girgis S Co-localization of calcitonin gene-related peptide-like immunoreactivity with substance P in cutaneous, vascular and visceral sensory neurons of guinea pig Neurosci Lett 1985, 57:125-130 10.1016/0304-3940(85)90050-3 2412189
31. Gibbins IL Wattchow D Coventry B Immunohistochemically identified populations of calcitonin gene-related peptide-immunoreactive (CGRP-IR) axons in human skin Brain Res 1987, 414:143-148 10.1016/ 0006-8993(87)91335-7 2441798
32. Alvarez FJ Cervantes C Blasco I Villalba R Martinez-Murillo R Polak JM Rodrigo J Presence of calcitonin gene-related peptide (CGRP) and substance P (SP) immunoreactivity in intraepidermal free nerve endings of cat skin Brain Res 1988, 442:391-395 10.1016/0006-8993(88)91532-6 2453251
33. Ishida-Yamamoto A Senba E Tohyama M Distribution and fine structure of calcitonin gene-related peptide-like immunoreactive nerve fibers in the rat skin Brain Res 1989, 491:93-101 10.1016/0006-8993(89)90090-5 2788478
34. Kruger L Silverman JD Mantyh PW Sternini C Brecha NC Peripheral patterns of calcitonin-gene-related peptide general somatic sensory innervation: cutaneous and deep terminations J Comp Neurol 1989, 280:291-302 10.1002/ cne.902800210 2784448
35. O'Brien C Woolf CJ Fitzgerald M Lindsay RM Molander C Differences in the chemical expression of rat primary afferent neurons which innervate skin, muscle or joint Neuroscience 1989, 32:493-502 10.1016/ 0306-4522(89)90096-1 2555742
36. Kilo S Harding-Rose C Hargreaves KM Flores CM Peripheral CGRP release as a marker for neurogenic inflammation: A model system for the study of neuropeptide secretion in rat paw skin Pain 1997, 73:201-207 10.1016/ S0304-3959(97)00108-5 9415506
37. Kessler F Habelt C Averbeck B Reeh PW Kress M Heat-induced release of CGRP from isolated rat skin and effects of bradykinin and the protein kinase C activator PMA Pain 1999, 83:289-295 10.1016/ S0304-3959(99)00108-6 10534601
38. Brain SD Cambridge H Hughes SR Wilsoncroft P Evidence that clacitonin-gene-related peptide contributes to inflammation in the skin and joint Ann NY Acad Sci 1992, 657:412-419 10.1111/ j.1749-6632.1992.tb22787.x 1637097
39. Ferrell WR Russell JW Extravasation in the knee induced by antidromic stimulation of articular C fibre afferents of the anaenesthetized cat Nature 1986, 284:351-353
40. Holzer P Local effector functions of capsaicin-sensitive sensory nerve endings: Involvement of tachykinins and other neuropeptides Neuroscience 1988, 24:739-768 10.1016/0306-4522(88)90064-4 3288903
41. Louis SM Jamieson A Russell NJ Dockray GJ The role of substance P and calcitonin gene-related peptide in neurogenic plasma extravasation and vasodilatation in the rat Neuroscience 1989, 32:581-586 10.1016/ 0306-4522(89)90281-9 2481241
42. Brain SD Sensory neuropeptides in the skin Neurogenic Inflammation New York: CRC Geppetti P, Holzer P 1996:229-245
43. Maggi CA The pharmacological modulation of neurotransmitter release Capsaicin in the study of pain London:ACademic Press Wood JN 1993:161-189
44. Caterina MJ Julius D The vanilloid receptor: A molecular gateway to the pain pathway Ann Rev Neurosci 2001, 24:487-517 10.1146/ annurev.neuro.24.1.487 11283319
45. Ren Y Zou X Fang L Lin Q Sympathetic modulation of activity in Aδ and C-primary nociceptive afferents after intradermal injection of capsaicin in rats J Neurophysiol 2005, 93:365-377 10.1152/jn.00804.2004 15371497
46. Go VLW Yaksh TL Release of substance P from the cat spinal cord J Physiol (Lond) 1987, 391:141-167 1192207 2451003
47. Zhang Y Malmberg AB Yaksh TL Sjolund B Sundler F Hakanson R Capsaicin-evoked release of pituitary adenylate cyclase activating peptide (PACAP) and calcitonin gene-related peptide (CGRP) from rat spinal cord in vivo Regul Pept 1997, 69:83-87 10.1016/ S0167-0115(97)02133-2 9178350
48. Szallasi A Blumberg PM Vanilloid (capsaicin) receptors and mechanisms Pharmacol Rev 1999, 51:159-211 10353985
49. deGroot J Zhou S Carlton SM Peripheral glutamate release in the hindpaw following low and high intensity sciatic stimulation NeuroReport 2000, 11:497-502 10.1097/00001756-200002280-00014 10718302
50. Pedersen-Bjergaard U Nielsen LB Jensen K Edvinsson L Jansen I Olesen J Algesia and local responses induced by neurokinin A and substance P in human skin and temporal muscle Peptides 1989, 10:1147-1152 10.1016/ 0196-9781(89)90006-5 2482964
51. Zhou S Bonasera L Carlton SM Peripheral administration of NMDA, AMPA or KA results in pain behaviors in rats NeuroReport 1996, 7:895-900 8724668
52. Du J Koltzenburg M Carlton SM Glutamate-induced excitation and sensitization of nociceptors in rat glabrous skin Pain 2001, 89:187-198 10.1016/S0304-3959(00)00362-6 11166475
53. Beirith A Santos ARS Calixto JB Mechanisms underlying the nociception and paw oedema caused by injection of glutamate into the mouse paw Brain Res 2002, 924:219-228 10.1016/S0006-8993(01)03240-1 11750907
54. Bayliss WM On the origin from the spinal cord of vasodilator fibres of the hind limb, and on the nature of these fibres J Physiol (Lond) 1901, 26:173-209 1540518 16992575
55. Szolcsanyi J Antidromic vasodilatation and neurogenic inflammation Agents Actions 1988, 23:4-11 10.1007/BF01967170 2965495
56. Jänig W Lisney SJW Small diameter mylinated afferents produce vasodilatation but not plasms extravasation in rat skin J Physiol (Lond) 1989, 415:477-486 1189187 2640468
57. Dickenson AH Dray A Selective antagonism of capsaicin by capsazepine: evidence for a spinal receptor site in capsaicin-induced antinociception Br J Pharmacol 1991, 104:1045-1049 1810591
58. Kwak JY Jung JY Hwang SW Lee WT Oh U A capsaicin-receptor antagonist, capsazepine, reduces inflammation-induced hyperalgesic responses in the rat: Evidence for an endogenous capsaicin-like substnace Neuroscience 1998, 86:619-626 10.1016/S0306-4522(98)00012-8 9881874
59. Walker KM Urban L Medhurst SJ Patel S Panesar M Fox AJ Mcintyre P The VR1 antagonist capsazepine reverses mechanical hyperalgesia in models of inflammatory and neuropathic pain J Pharmacol Ther 2003, 304:56-62 10.1124/jpet.102.042010
60. Lin Q Wu J Willis WD Neurogenic inflammation following intradermal injection of capsaicin is partially mediated by dorsal root reflexes Proceedings of the 9th World Congress on Pain: Progress in pain research and management Seattle:IASP Press Devor M, Rowbotham MC, Wiesenfeld-Hallin Z 2000:259-266
61. Lin Q Zou X Ren Y Wang J Fang L Willis WD Involvement of peripheral neuropeptide Y receptors in sympathetic modulation of acute cutaneous flare induced by intradermal capsaicin Neuroscience 2004, 123:337-347 10.1016/j.neuroscience.2003.09.017 14698742
62. Silverman DG Jotkowitz AB Freemer M Gutter V O'Connor TZ Braverman IM Peripheral assessment of phenylephrine-induced vasoconstriction by laser Doppler flowmetry and its potential relevance to homeostatic mechanisms Circulation 1994, 90:23-26 8026002
63. Rees H Sluka KA Westlund KN Willis WD The role of glutamate and GABA receptors in the generation of dorsal root reflexes by acute arthritis in the anaesthetized rat J Physiol (Lond) 1995, 484:437-445 1157905 7602536
64. Garcia-Nicas E Laird JM Cervero F Sensitization of nociceptor-specific neurons by capsaicin or mustard oil: Effect of GABAA-receptor blockade Proceedings of the 10th World Congress on Pain Seattle:IASP Press Dostrovsky JO, Carr DB, Koltzenburg M 2003;327-335
65. Hughes SR Brain SD A calcitonin gene-related peptide (CGRP) antagonist (CGRP8-37) inhibits microvascular responses induced by CGRP and capsaicin in skin Br J Pharmacol 1991, 104:738-742 1797334
66. Plourde V St.-Pierre S Quirion R Calcitonin gene-related peptide in viscerosensitive response to colorectal distension in rats Am J Physiol 1997, 273:G191-G196 9252526
67. Sakurada T Yamada T Tan-No K Manome Y Sakurada S Differential effects of substance P analogs on neurokinin 1 receptor agonists in the mouse spinal cord J Pharmacol Exp Ther 1991, 259:205-210 1717679
68. Rosen A Zhang Y-X Lund I Lundeberg T Yu L-C Substance P microinjected into the periaqueductal gray matter induces antinociception and is released following morphine administration Brain Res 2004, 1001:87-94 10.1016/j.brainres.2003.11.060 14972657