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Vanilloid receptor-mediated hyperalgesia and desensitization

  • Zoltán Sándor
  • Arpad Szallasi
Part of the Progress in Inflammation Research book series (PIR)

Keywords

Nerve Growth Factor Dorsal Root Ganglion Dorsal Root Ganglion Neuron Thermal Hyperalgesia Vanilloid Receptor 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Jancsó N, Jancsó A (1949) Desensitization of sensory nerve endings [in Hungarian]. Kísérletes Orvostudomány 2(Suppl): 15Google Scholar
  2. 2.
    Buck SH, Burks TF (1986) The neuropharmacology of capsaicin: a review of some recent observations. Pharmacol Rev 38: 179–226PubMedGoogle Scholar
  3. 3.
    Holzer P (1991) Capsaicin: cellular targets, mechanisms of action, and selectivity for thin sensory neurons. Pharmacol Rev 43: 143–120PubMedGoogle Scholar
  4. 4.
    Szallasi A, Blumberg PM (1999) Vanilloid (capsaicin) receptors and mechanisms. Pharmacol Rev 51: 159–212PubMedGoogle Scholar
  5. 5.
    Szallasi A (2002) Vanilloid (capsaicin) receptors in health and disease. Am J Clin Pathol 118: 110–121PubMedGoogle Scholar
  6. 6.
    Szallasi A, Fowler CJ (2002) After a decade of intravesical vanilloid therapy: still more questions than answers. Lancet Neurol 1: 167–172PubMedGoogle Scholar
  7. 7.
    Szolcsányi J, Jancsó-Gábor A (1976) Sensory effects of capsaicin congeners. Part II: Importance of chemical structure and pungency in desensitizing activity of capsaicintype compounds. Arzneimittelforschung (Drug Res) 26: 33–37PubMedGoogle Scholar
  8. 8.
    Walpole CSJ, Wrigglesworth R (1993) Structural requirements for capsaicin agonists and antagonists. In: JN Wood (ed): Capsaicin in the Study of Pain. Academic Press, San Diego, 63–82Google Scholar
  9. 9.
    Szallasi A, Blumberg PM (1990) Specific binding of resiniferatoxin, an ultrapotent capsaicin analog, by dorsal root ganglion membranes. Brain Res 524: 106–111PubMedCrossRefGoogle Scholar
  10. 10.
    Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389: 816–824PubMedGoogle Scholar
  11. 11.
    Roberts JC, Davis JB, Benham CD (2004) [3H]Resiniferatoxin autoradiography in the CNS of wild-type and TRPV1 null mice defines TRPV1 (VR-1) protein distribution. Brain Res 995: 176–183PubMedCrossRefGoogle Scholar
  12. 12.
    Caterina MJ, Julius D (2001) The vanilloid receptor: a molecular gateway to the pain pathway. Annu Rev Neurosci 24: 487–514PubMedCrossRefGoogle Scholar
  13. 13.
    Jordt SE, McKemy DD, Julius D (2003) Lessons from peppers and peppermint: the molecular logic of thermosensation. Curr Opin Neurobiol 13: 487–492PubMedCrossRefGoogle Scholar
  14. 14.
    Di Marzo V, Blumberg PM, Szallasi A (2002) Endovanilloid signaling in pain. Curr Opin Neurobiol 12: 372–380PubMedGoogle Scholar
  15. 15.
    Huang SM, Bisogno T, Trevisani M, Al-Hayani A, De Petrocellis L, Fezza M, Petros TJ, Krey FJ, Chu CI, Miller JD et al (2002) An endogenous capsaicin-like substance with high potency at recombinant and native vanilloid VR1 receptors. Proc Natl Acad Sci USA 99: 8400–8405PubMedGoogle Scholar
  16. 16.
    Chu CJ, Huang SM, De Petrocellis L, Bisogno T, Ewing SA, Miller JD, Zipkin RE, Daddario N, Appendino G, Di Marzo V et al (2003) N-oleoyldopamine, a novel endogenous capsaicin-like lipid that produces hyperalgesia. J Biol Chem 278: 13633–13639PubMedCrossRefGoogle Scholar
  17. 17.
    Szolcsányi J, Sándor Z, Pethö G, Varga A, Bölcskei K, Almási R, Riedl Z, Hajos G, Czéh G (2004) Direct evidence for activation and desensitization of the capsaicin receptor by N-oleoyldopamine on TRPV1-transfected cell line, in gene deleted mice, and in the rat. Neurosci Lett 361: 155–158PubMedGoogle Scholar
  18. 18.
    Trevisani M. Smart D, Gunthorpe MJ, Tognetto M, Barbieri M, Campi B, Amadesi S, Grey J, Jerman JC, Brough SJ et al (2002) Ethanol elicits and potentiates nociceptor responses via the vanilloid receptor-1. Nat Neurosci 5: 546–551PubMedCrossRefGoogle Scholar
  19. 19.
    Liu L, Zhu W, Zhang ZS, Yang T, Grant A, Oxford G, Simon SA (2004) Nicotine inhibits voltage-dependent sodium channels and sensitizes vanilloid receptors. J Neurophysiol 91: 1482–1491PubMedGoogle Scholar
  20. 20.
    Inoue K, Koizumi S, Fiziwara S, Denda S, Inoue K, Denda M (2002) Functional vanilloid receptors in cultured normal human epidermal keratinocytes. Biochem Biophys Res Commun 291: 124–129PubMedCrossRefGoogle Scholar
  21. 21.
    Southall MD, Li T, Gharibova LS, Pei Y, Nicol GD, Travers JB (2003) Activation of epidermal vanilloid receptor-1 induces release of proinflammatory mediators in human keratinocytes. J Pharmacol Exp Ther 304: 217–222PubMedCrossRefGoogle Scholar
  22. 22.
    Birder LA, Kanai AJ, De Groat WC, Kiss S, Nealan ML, Burke NE, Dineley KE, Watkins S, Reynolds IJ, Caterina M (2001) Vanilloid receptor expression suggests a sensory role for urinary bladder epithelial cells. Proc Natl Acad Sci USA 98: 13396–13401PubMedCrossRefGoogle Scholar
  23. 23.
    Kato S, Aihara E, Nakamura A, Xin H, Matsui H, Kohama K, Takeuchi I (2003) Expression of vanilloid receptors in rat gastric epithelial cells: role in cellular protection. Biochem Pharmacol 66: 1115–1121PubMedCrossRefGoogle Scholar
  24. 24.
    Stander S, Moormann C, Schumacher M, Buddenkotte J, Artuc M, Shpakovitch V, Brzoska T, Lippert U, Henz BM, Luger TA et al (2004) Expression of the vanilloid receptor subtype 1 in cutaneous sensory nerve fibers, mast cells, and epithelial cells of appendage structures. Exp Dermatol 13: 129–139PubMedCrossRefGoogle Scholar
  25. 25.
    Reilly CA, Taylor JL, Lanza DL, Carr BA, Crouch DJ, Yost GS (2003) Capsaicinoids cause inflammation and epithelial cell death through activation of vanilloid receptors. Toxicol Sci 73: 170–181PubMedCrossRefGoogle Scholar
  26. 26.
    Chen CW, Lee ST, Wu WT, Fu WM, Ho FM, Lin WW (2003) Signal transduction for inhibition of iducible nitric oxide synthase and cyclooxygenase-2 induction by capsaicin and related analogs in macrophages. Br J Pharmacol 140: 1077–1087PubMedGoogle Scholar
  27. 27.
    Heiner I, Eisfeld J, Halaszovich CR, Wehage E, Jungling E, Zitt C, Luckhoff A (2003) Expression profile of the transient receptor potential (TRP) family in neutrophil granulocytes: evidence for currents through long TRP channel 2 induced by ADP-ribose and NAD. Biochem J 371: 1045–1053PubMedCrossRefGoogle Scholar
  28. 28.
    Simone DA, Ngeow JYF, Putterman GJ, LaMotte RH (1987) Hyperalgesia to heat after intradermal injection of capsaicin. Brain Res 418: 201–203PubMedCrossRefGoogle Scholar
  29. 29.
    Simone DA, Baumann TF, LaMotte RH (1989) Dose-dependent pain and mechanical hyperalgesia in humans after intradermal injection of capsaicin. Pain 38: 99–107PubMedCrossRefGoogle Scholar
  30. 30.
    Torebjörk HE, Lundberg JM, LaMotte RH (1992) Central changes in processing of mechanoreceptive input in capsaicin-induced secondary hyperalgesia in humans. J Physiol 448: 765–780PubMedGoogle Scholar
  31. 31.
    Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, Koltzenburg M, Basbaum AI, Julius D (2000) Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288: 306–313PubMedCrossRefGoogle Scholar
  32. 32.
    Davis JB, Gray J, Gunthorpe MJ, Hatcher JP, Davey PT, Overend P, Harries MH, Latcham J, Clapham C, Atkinson K et al (2000) Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 405:183–187PubMedCrossRefGoogle Scholar
  33. 33.
    Jordt SE, Tominaga M, Julius D (2000) Acid potentiation of the capsaicin receptor determined by a key extracellular site. Proc Natl Acad Sci USA 97: 8134–8139PubMedCrossRefGoogle Scholar
  34. 34.
    Reeh PW, Kress M (2001) Molecular physiology of proton transduction in nociceptors. Curr Opin Pharmacol 1: 45–51PubMedGoogle Scholar
  35. 35.
    Kuzhikandathil EV, Wang H, Szabo T, Morozowa N, Blumberg PM, Oxford GS (2001) Functional analysis of capsaicin receptor (vanilloid receptor subtype 1) multimerizationand agonist responseiveness using a dominant negative mutation. J Neurosci 21: 8697–8706PubMedGoogle Scholar
  36. 36.
    Jordt SE, Julius D (2002) Molecular basis for species-specific sensitivity to “hot” chili peppers. Cell 108: 421–430PubMedCrossRefGoogle Scholar
  37. 37.
    Ryu S, Liu B, Qin F (2003) Low pH potentiates both capsaicin binding and channel gating of VR1 receptors. J Gen Physiol 122: 45–61PubMedCrossRefGoogle Scholar
  38. 38.
    Vellani V, Mapplebeck S, Moriondo A, Davis JB, McNaughton PA (2001) Protein kinase C activation potentiates gating of the vanilloid receptor VR1 by capsaicin, protons, heat nand anandamide. J Physiol 534: 813–825PubMedCrossRefGoogle Scholar
  39. 39.
    Amadesi S, Nie J, Vergnolle N, Cottrell GS, Grady EF, Trevisiani M, Manni C, Geppetti P, McRoberts JA, Ennes H et al (2004) Protease-activated receptor 2 sensitizes the capsaicin receptor transient receptor potential vanilloid receptor 1 to induced hyperalgesia. J Neurosci 24: 4300–4312PubMedCrossRefGoogle Scholar
  40. 40.
    Ossovskaya VS, Bunnett NW (2003) Protease-activated receptors: contribution to physiology and disease. J Physiol 552: 589–601Google Scholar
  41. 41.
    Kawao N, Ikeda H, Kitano T, Kuroda R, Sekiguchi F, Kataoka K, Kamanaka Y, Kawataba A (2004) Modulation of capsaicin-evoked visceral pain and referred hyperalgesia by protease-activated receptors 1 and 2. J Pharmacol Sci 94: 277–285PubMedCrossRefGoogle Scholar
  42. 42.
    Numazaki M, Tominaga T, Toyooka H, Tominaga M (2002) Direct phosphorilation of capsaicin receptor VR1 by protein kinase Ce and identification of two target serine residues. J Biol Chem 277: 13375–13378PubMedCrossRefGoogle Scholar
  43. 43.
    Malmberg AB, Chen C, Tonegawa S, Basbaum AI (1997) Preserved acute pain and reduced neuropathic pain in mice lacking PKC©. Science 278: 279–283PubMedCrossRefGoogle Scholar
  44. 44.
    Khasar SG, Lin YH, Martin A, Dadgar J, McMahon T, Wang D, Hundle B, Aley KO, Isenberg W, McCarter G et al (1999) A novel nociceptor signaling pathway revealed in protein kinase C epsilon mutant mice. Neuron 24: 253–260PubMedCrossRefGoogle Scholar
  45. 45.
    Zhou Y, Li GD, Zhao ZQ (2003) State-dependent phosphorylation of epsilon isozyme of prtein kinase C in adult rat dorsal root ganaglia after inflammation and nerve injury. J Neurochem 85: 571–580PubMedCrossRefGoogle Scholar
  46. 46.
    Levine JD, Reichling DB (1999) Peripheral mechanisms of inflammatory pain. In: PD Wall, R Melzack (eds): Textbook of pain. Churchill Livingstone, Edinburgh, 59–84Google Scholar
  47. 47.
    Bhave G, Zhu W, Wang H, Brasier DJ, Oxford GS, Gereau RW (2002) cAMP-dependent protein kinase regulates desensitization of the capsaicin receptor (VR1) by direct phosphorylation. Neuron 35: 721–731PubMedCrossRefGoogle Scholar
  48. 48.
    Rathee PK, Distler C, Obreja O, Neuhuber W, Wang GK, Wang SY, Nau C, Kress M (2002) PKA/AKAP/VR-1 module: A common link of Gs-mediated signaling to thermal hyperalgesia. J Neurosci 22: 4740–4745PubMedGoogle Scholar
  49. 49.
    Jung J, Shin JS, Lee SY, Hwang SW, Koo J, Cho H, Oh U (2004) Phosphorylation of vanilloid receptor 1 by Ca2+/calmodulin-dependent kinase II regulates its vanilloid binding. J Biol Chem 279: 7048–7054PubMedGoogle Scholar
  50. 50.
    Rosenbaum T, Gordon-Shaag A, Munari M, Gordon SE (2004) Ca2+/calmodulin modulates TRPV1 activation by capsaicin. J Gen Physiol 123: 53–62PubMedCrossRefGoogle Scholar
  51. 51.
    Mandadi S, Numazaki M, Tominaga M, Bhat MB, Armati PJ, Roufogalis BD (2004) Activation of protein kinase C reverses capsaicin-induced calcium-dependent desensitization of TRPV1 ion channels. Cell Calcium 35: 471–478PubMedCrossRefGoogle Scholar
  52. 52.
    Galoyan SM, Petruska JC, Mendell LM (2003) Mechanissm of sensitization of the response of single dorsal root ganglion cells from adult rat to noxious heat. Eur J Neurosci 18: 535–541PubMedCrossRefGoogle Scholar
  53. 53.
    Lázár J, Szabó T, Marincsák R, Kovács L, Blumberg PM, Bíró T (2004) sensitization of recombinant vanilloid receptor-1 by various neurotrophic factors. Life Sci 75: 153–163PubMedGoogle Scholar
  54. 54.
    Winston J, Toma H, Shenoy M, Pasricha PJ (2001) Nerve growth factor regulates VR-1 mRNA in cultures of adult dorsal root ganglion neurons. Pain 89: 181–186PubMedCrossRefGoogle Scholar
  55. 55.
    Dai Y, Iwata K, Fukuota T, Kondo E, Tokunaga A, Yamanaka H, Tachibana T, Noguchi, K (2002) Phosphorylation of extracellular signal-regulated kinase in primary afferent neurons by noxious stimuli and its involvement in peripheral sensitization. J Neurosci 22: 7737–7745PubMedGoogle Scholar
  56. 56.
    Hu HJ, Bhave G, Gereau RW (2002) Prostaglandin and protein kinase A-dependent modulation of vanilloid receptor function by metabotropic glutamate receptor 5: potential mechanism for thermal hyperalgesia. J Neurosci 22: 7444–7452PubMedGoogle Scholar
  57. 57.
    Yang D, Gereau RQ (2002) Peripheral group II metabotropic glutamate receptors (mGluR2/3) regulate prostaglandin E2-mediated sensitization of capsaicin responses and thermal nociception. J Neurosci 22: 6388–6393PubMedGoogle Scholar
  58. 58.
    Cortright DN, Szallasi A (2004) Biochemical pharmacology of the vanilloid receptor TRPV1. Eur J Biochem 271: 1814–1819PubMedCrossRefGoogle Scholar
  59. 59.
    Morenilla-Palao C, Planells-Cases R, Garcia-Sanz N, Ferrer-Montiel A (2004) Regulated exocytosis contributes to protein kinase C potentiation of vanilloid receptor activity. J Biol Chem 279: 25665–25672PubMedCrossRefGoogle Scholar
  60. 60.
    Chuang HH, Prescott ED, Kong H, Shields S, Jordt SE, Basbaum AI, Chao MV, Julius D (2002) Bradykinin and nerve growth factor release the capsaicin receptor from PtdIns(4,5)P2-mediated inhibition. Nature 411: 957–962Google Scholar
  61. 61.
    Prescott ED, Julius D (2003) A modular PIP2 binding site as a determinant of capsaicin receptor sensitivity. Science 300: 1284–1288PubMedCrossRefGoogle Scholar
  62. 62.
    Crandall M, Kwash J, Yu W, White G (2002) Activation of protein kinase C sensitizes human VR1 to capsaicin and to moderate decreases in pH at physiological temperatures in Xenopus oocytes. Pain 98: 109–117PubMedCrossRefGoogle Scholar
  63. 63.
    Shin J, Cho H, Hwang SW, Jung J, Shin CY, Lee SY, Kim SH, Lee MG, Choi YH, Kim J et al (2002) Bradykinin-12-lipoxygenase-VR1 signaling pathway for inflammatory hyperalgesia. Proc Natl Acad Sci USA 99: 10150–10155PubMedGoogle Scholar
  64. 64.
    Sugiura T, Tominaga M, Katsuya H, Mizumura K (2002) Bradykinin lowers the threshold temperature for heat activation of vanilloid receptor 1. J Neurophysiol 88: 544–548PubMedGoogle Scholar
  65. 65.
    Carlton SM, Coggeshall RE (2001) Peripheral capsaicin receptors increase in the inflamed rat hindpaw: a possible mechanism for peripheral sensitization. Neurosci Lett 310: 53–56PubMedCrossRefGoogle Scholar
  66. 66.
    Rashid H, Inoue M, Kondo S, Kawashima T, Bakoshi S, Ueda H (2003) Novel expression of vanilloid receptor 1 on capsaicin-insensitive fibers acoounts for the analgesic effect of capsaicin cream in neuropathic pain. J Pharmacol Exp Ther 304: 940–948PubMedGoogle Scholar
  67. 67.
    Kamei J, Zushida K, Morita K, Sasaki M, Tanaka SI (2001) Role of vanilloid VR1 receptor in thermal allodynia and hyperalgesia in diabetic mice. Eur J Pharmacol 422: 83–86PubMedCrossRefGoogle Scholar
  68. 68.
    Jancsó N (1955) Speicherung. Stoffanreicherung in Retikuloendothelial und in der Niere. Akadémiai kiadó, BudapestGoogle Scholar
  69. 69.
    Szolcsányi J (1993) Actions of capsaicin on sensory receptors. In: JN Woods (ed): Capsaicin in the study of pain. Academic Press, San Diego, 1–26Google Scholar
  70. 70.
    Docherty RJ, Yeats JC, Bevan S, Boddeke HW (1996) Inhibition of calcineurin inhibits the desensitization of capsaicin-evoked currents in cultured dorsal root ganglion neurons from adult rats. Pflugers Arch 431: 828–837PubMedCrossRefGoogle Scholar
  71. 71.
    Piper AS, Yeats JC, Bevan S, Docherty RJ (1999) A study of the voltage dependence of capsaicin-activated membrane currents in rat sensory neurons before and after acute desensitization. J Physiol 518: 721–733PubMedCrossRefGoogle Scholar
  72. 72.
    Cholewinski A, Burgess GM, Bevan S (1993) The role of calcium in capsaicin-induced desensitization in rat cultured dorsal root ganglion neurons. Neuroscience 55: 101CrossRefGoogle Scholar
  73. 73.
    Koplas PA, Rosenberg RL, Oxford GS (1997) The role of calcium in the desensitization of capsaicin responses in rat dorsal root ganglion neurons. J Neurosci 17: 3525–3537PubMedGoogle Scholar
  74. 74.
    Numazaki M, Tominaga T, Takeuchi K, Murayama N, Toyooka H, Tominaga M (2003) Structural determinant of TRPV1 desensitization interacts with calmodulin. Proc Natl Acad Sci USA 100: 8002–8006PubMedCrossRefGoogle Scholar
  75. 75.
    Kenins P (1982) Responses of single nerve fibres to capsaicin applied to the skin. Neurosci Lett 29: 83–88PubMedCrossRefGoogle Scholar
  76. 76.
    He X, Schepelmann K, Schaible HG, Schmidt RF (1990) Capsaicin inhibits responses of fine afferents from the knee joint of the cat to mechanical and chemical stimuli. Brain Res 530: 147–150PubMedCrossRefGoogle Scholar
  77. 77.
    Szolcsányi J (1977) A pharmacological approach to elucidation of the role of different nerve fibres and receptor endings in mediation of pain. J Physiol (Paris) 73: 251–259Google Scholar
  78. 78.
    Dray A, Hankins MW, Yeats JC (1989) Desensitization and capsaicin-induced release of substance P-like immunoreactivity from guinea-pig ureter in vitro. Neuroscience 31: 479–483PubMedCrossRefGoogle Scholar
  79. 79.
    Dray A, Bettaney J, Forster P (1989) Capsaicin desensitization of peripheral nociceptive fibres does not impair sensitivity to other noxious stimuli. Neurosci Lett 99: 50–54PubMedCrossRefGoogle Scholar
  80. 80.
    Dray A, Bettaney J, Forster P (1990) Actions of capsaicin on peripheral nociceptors of the neonatal rat spinal cord-tail in vitro: dependence of extracellular ions and independence of second messengers. Br J Pharmacol 101: 727–733PubMedGoogle Scholar
  81. 81.
    Lang E, Novak A, Reeh PW, Handwerker HO (1990) Chemosensitivity of fine afferents from rat skin in vitro. J Neurophysiol 63: 887–901PubMedGoogle Scholar
  82. 82.
    Szolcsányi J. (1987) Selective responsiveness of polymodal nociceptors of the rabbit ear to capsaicin, bradykinin and ultra-violet irradiation. J Physiol 388: 9–23PubMedGoogle Scholar
  83. 83.
    Belmonte C, Gallar J, Pozo MA, Rebollo I (1991) Excitation by irritant chemical substances of sensory afferent units in the cat’s cornea. J Physiol 437: 709–725PubMedGoogle Scholar
  84. 84.
    Balla Z, Szöke E, Czéh G, Szolcsányi J (2001) Effect of capsaicin on voltage-gated currents of trigeminal neurons in cell culture and slice preparations. Acta Physiol Hung 88: 173–196PubMedGoogle Scholar
  85. 85.
    Liu L, Oortgiesen M, Li L, Simon SA (2001) Capsaicin inhibits activation of voltagegated sodium currents in capsaicin-sensitive trigeminal ganglion neurons. J Neurophysiol 85: 745–758PubMedGoogle Scholar
  86. 86.
    Su X, Wachtel RE, Gebhart GF (1999) Capsaicin sensitivity and voltage-gated sodium currents in colon sensory neurons from rat dorsal root ganglia. Am J Physiol Gastrointest Liver Physiol 277: G1180–G1188Google Scholar
  87. 87.
    Blair NT, Bean BP (2003) Role of tetrodotoxin-resistant Na+ current slow inactivation in adaptation of action potential firing in small-diameter dorsal root ganglion neurons. J Neurosci 23: 10338–10350PubMedGoogle Scholar
  88. 88.
    Wood JN, Coote PR, Minhas A, McNiel M, Mullany I, Burgess G (1989) Capsaicininduced ion fluxes increase cGMP but not cAMP levels in rat sensory neurons in culture. J Neurosci 53: 1203–1211Google Scholar
  89. 89.
    Marban E, Yamagishi T, Tomaselli GF (1998) Structure and function of voltage-gated sodium channels. J Physiol 508: 647–657PubMedCrossRefGoogle Scholar
  90. 90.
    Kehl SJ (1994) Block by capsaicin of voltage-gated K+ currents in melanotrophs of the rat pituitary. Br J Pharmacol 112: 616–624PubMedGoogle Scholar
  91. 91.
    Bleakman D, Brorson JR, Miller RJ (1990) The effect of capsaicin on voltage-gated calcium currents and calcium signals in cultured dorsal root ganglion cells. Br J Pharmacol 101: 423–431PubMedGoogle Scholar
  92. 92.
    Docherty RJ, Robertson B, Bevan S (1991) Capsaicin causes prolonged inhibition of voltage-activated calcium currents in adult rat dorsal root ganglion neurons in culture. Neuroscience 40: 513–521PubMedCrossRefGoogle Scholar
  93. 93.
    Brand L, Berman E, Schwen R, Loomans M, Janusz J, Bohne R, Maddin C, Gardner J, Lahann T, Farmer R et al (1987) NE-19550: a novel, orally active anti-inflammatory analgesic. Drugs Exp Clin Res 13: 259–265PubMedGoogle Scholar
  94. 94.
    Brand LM, Skare KL, Loomans ME, Reller HH, Schwen RJ, Lade DA, Bohne RL, Maddin CS, Moorehead DP, Fanelli R et al (1990) Anti-inflammatory pharmacology and mechanism of the orally active capsaicin analogs, NE-19550 and NE-28345. Agents Actions 31: 329–340PubMedCrossRefGoogle Scholar
  95. 95.
    Dray A, Bettaney J, Rueff A, Walpole C, Wrigglesworth R (1990) NE-19550 and NE-21610, antinociceptive capsaicin analogues: studies on nociceptive fibres of the neonatal rat tail in vitro. Eur J Pharmacol 181: 289–293PubMedCrossRefGoogle Scholar
  96. 96.
    Wrigglesworth R, Walpole CS, Bevan S, Campbell EA, Dray A, Hughes GA, James I, Masdin KJ, Winter J (1996) Analogues of capsaicin with agonist activity as novel analgesic agents: structure-activity studies. 4. Potent, orally active analgesics. J Med Chem 39: 4942–4951PubMedCrossRefGoogle Scholar
  97. 97.
    Taylor DC, Pierau FK, Szolcsányi J (1985) Capsaicin-induced inhibition of axoplasmic transport is prevented by nerve growth factor. Cell Tissue Res 240: 569–573PubMedCrossRefGoogle Scholar
  98. 98.
    Taylor DC, Pierau FK, Szolcsányi J (1984) Long lasting inhibition of horseradish peroxidase (HRP) transport in sensory nerves induced by capsaicin pretreatment of the receptive field. Brain Res 298: 45–49PubMedCrossRefGoogle Scholar
  99. 99.
    Miller MS, Buck SH, Sipes IG, Yamamura HI, Burks TF (1982) Regulation of substance P by nerve growth factor: disruption by capsaicin. Brain Res 250: 193–196PubMedCrossRefGoogle Scholar
  100. 100.
    Farkas-Szallasi T, Lundberg JM, Wiesenfeld-Hallin Z, Hökfelt T, Szallasi A (1995) Increased levels of GMAP, VIP and nitric oxide synthase, and their mRNAs, in lumbar dorsal root ganglia of the rat following systemic resiniferatoxin treatment. Neuroreport 6: 2230–2234PubMedGoogle Scholar
  101. 101.
    Xu XJ, Farkas-Szallasi T, Lundberg JM, Hökfelt T, Wiesenfeld-Hallin Z, Szallasi A (1997) Effects of the capsaicin analogue resiniferatoxin on spinal nociceptive mechanisms in the rat: behavioral, electrophysiological and in situ hybridization studies. Brain Res 752: 52–60PubMedCrossRefGoogle Scholar
  102. 102.
    Szallasi A, Blumberg PM (1992) Vanilloid receptor loss in rat sensory ganglia associated with long term desensitization to resiniferatoxin. Neurosci Lett 140: 51–54PubMedCrossRefGoogle Scholar
  103. 103.
    Szallasi A, Nilsson S, Farkas-Szallasi T, Blumberg PM, Hökfelt T, Lundberg JM (1995) Vanilloid (capsaicin) receptors in the rat: distribution in the brain, regional differences in the spinal cord, axonal transport to the periphery, and depletion by systemic vanilloid treatment. Brain Res 703: 175–183PubMedCrossRefGoogle Scholar
  104. 104.
    Farkas-Szallasi T, Bennett GJ, Blumberg PM, Hökfelt T, Lundberg JM, Szallasi A. (1996) Vanilloid receptor loss is independent of the messenger plasticity that follows systemic resiniferatoxin administration. Brain Res 719: 213–218PubMedGoogle Scholar
  105. 105.
    Goso C, Piovacari G, Szallasi A (1993) Resiniferatoxin-induced loss of vanilloid receptors is reversible in the urinary bladder but not in the spinal cord of the rat. Neurosci Lett 162: 197–200PubMedCrossRefGoogle Scholar
  106. 106.
    Szolcsányi J, Jancsó-Gábor A, Joó F (1975) Functional and fine structural characteristics of the sensory neuron blocking effect of capsaicin. Naunyn Schmiedebergs Arch Pharmacol 287: 157–169PubMedGoogle Scholar
  107. 107.
    Dedov VN, Mandadi S, Armati PJ, Verkhratsky A (2001) Capsaicin-induced depolarisation of mitochondria in dorsal root ganglion neurons is enhanced by vanilloid receptors. Neuroscience 103: 219–226PubMedCrossRefGoogle Scholar
  108. 108.
    Szolcsányi J, Joó F, Jancsó-Gábor A (1971) Mitochondrial changes in preoptic neurons after capsaicin desensitization of the hypothalamic thermodetectors in rats. Nature 229: 116–117PubMedGoogle Scholar
  109. 109.
    Szöke E, Czéh G, Szolcsányi J, Seress L (2002) Neonatal anandamide treatment results in prolonged mitochondrial damage in the vanilloid receptor type 1-immunoreactive B-type neurons of the rat trigeminal ganglion. Neuroscience 115: 805–814PubMedGoogle Scholar
  110. 110.
    Szöke E, Seress L, Szolcsányi J. (2002) Neonatal capsaicin treatment results in prolonged mitochondrial damage and delayed cell death of B cells in the rat trigeminal ganglia. Neuroscience 113: 925–937PubMedGoogle Scholar
  111. 111.
    Chard PS, Bleakman D, Savidge JR, Miller RJ (1995) Capsaicin-induced neurotoxicity in cultured dorsal root ganglion neurons: involvement of calcium-activated proteases. Neuroscience 65: 1099–1108PubMedCrossRefGoogle Scholar
  112. 112.
    Chung K, Klein CM, Coggeshall RE (1990) The receptive part of the primary afferent axon is most vulnerable to systemic capsaicin in adult rats. Brain Res 511: 222–226PubMedCrossRefGoogle Scholar
  113. 113.
    Chung K, Schwen RJ, Coggeshall RE (1985) Ureteral axon damage following subcutaneous administration of capsaicin in adult rats. Neurosci Lett 53: 221–226PubMedCrossRefGoogle Scholar
  114. 114.
    Simone DA, Nolano M, Johnson T, Wendelschafer-Crabb G, Kennedy WR (1998) Intradermal injection of capsaicin in humans produces degeneration and subsequent reinnervation of epidermal nerve fibers: correlation with sensory function. J Neurosci 18: 8947–8959PubMedGoogle Scholar
  115. 115.
    Nolano M, Simone DA, Wendelschafer-Crabb G, Johnson T, Hazen E, Kennedy WR (1999) Topical capsaicin in humans: parallel loss of epidermal nerve fibers and pain sensation. Pain 81: 135–145PubMedCrossRefGoogle Scholar
  116. 116.
    Wood JN, Winter J, James IF, Rang HP, Yeats J, Bevan S (1988) Capsaicin-induced ion fluxes in dorsal root ganglion cells in culture. J Neurosci 8: 3208–3220PubMedGoogle Scholar
  117. 117.
    Jeftinija S, Liu F, Jeftinija K, Urban L (1992) Effect of capsaicin and resiniferatoxin on peptidergic neurons in cultured dorsal root ganglion. Regul Pept 39: 123–135PubMedCrossRefGoogle Scholar
  118. 118.
    Karai L, Brown DC, Mannes AJ, Connelly ST, Brown J, Gandal M, Wellish OM, Neubert JK, Oláh Z, Iadarola MJ (2004) Deletion of vanilloid receptor-1 expressing primary afferent neurons for pain control. J Clin Invest 113: 1344–1352PubMedCrossRefGoogle Scholar
  119. 119.
    Oláh Z, Szabó T, Karai L, Hough C, Fields RD, Caudle RM, Blumberg PM, Iadarola MJ (2001) Ligand-induced dynamic membrane changes and cell deletion conferred by vanilloid receptor 1. J Biol Chem 276: 11021–11030PubMedGoogle Scholar
  120. 120.
    Jancsó G, Király E, Jancsó-Gábor A (1977) Pharmacologically induced selective degeneration of chemosensitive primary sensory neurons. Nature 270: 741–743PubMedGoogle Scholar
  121. 121.
    Jancsó G, Király E (1981) Sensory neurotoxins: chemically induced selective destruction of primary sensory neurons. Brain Res 210: 83–89PubMedGoogle Scholar
  122. 122.
    Otten U, Lorez HP, Businger F (1983) Nerve growth factor antagonizes the neurotoxic action of capsaicin on primary sensory neurons. Nature 301: 515–517PubMedCrossRefGoogle Scholar
  123. 123.
    Ruit KG, Elliott JL, Osborne PA, Yan Q, Snider WD (1992) Selective dependence of mammalian dorsal root ganglion neurons on nerve growth factor during embryonic development. Neuron 8:573–587PubMedCrossRefGoogle Scholar
  124. 124.
    Mendell LM (1999) Neurotrophin action on sensory neurons in adults: an extension of the neurotrophic hypothesis. Pain 6: S127–S132PubMedGoogle Scholar
  125. 125.
    Winter J, Woolf C, Lynn B (1993) Degenerative and regenerative responses of sensory neurons to capsaicin-induced damage. In: JN Woods (ed): Capsaicin in the Study of Pain. Academic Press, San Diego, 139–160Google Scholar
  126. 126.
    Welk E, Fleischer E, Petsche U, Handwerker HO (1984) Afferent C-fibres in rats after neonatal capsaicin treatment. Pflügers Arch 400: 66–71PubMedCrossRefGoogle Scholar
  127. 127.
    Fukuoka T, Tokunaga A, Tachibana T, Dai Y, Yamanaka H, Noguchi K (2002) VR1, but not P2X(3), increases in the spared L4 DRG in rats with L5 spinal nerve ligation. Pain 99: 111–120PubMedCrossRefGoogle Scholar
  128. 128.
    HHudson LJ, Bevan S, Wotherspoon G, Gentry C, Fox A, Winter J (2001) VR1 protein expression increases in undamaged DRG neurons after partial nerve injury. Eur J Neurosci 13: 2105–2114Google Scholar
  129. 129.
    Pini A, Lynn B (1991) C-fibre function during the 6 weeks following brief application of capsaicin to a cutaneous nerve in the rat. Eur J Neurosci 3: 274–284PubMedGoogle Scholar
  130. 130.
    Pini A, Baranowski R, Lynn B (1990) Long-term reduction in the number of C-fibre nociceptors following capsaicin treatment of a cutaneous nerve in adult rats. Eur J Neurosci 2: 89–97PubMedGoogle Scholar
  131. 131.
    Jancsó G, Lawson SN (1990) Transganglionic degeneration of capsaicin-sensitive C-fiber primary afferent terminals. Neuroscience 39: 501–511PubMedGoogle Scholar
  132. 132.
    Joó F, Szolcsányi J, Jancsó-Gábor A (1969) Mitochondrial alterations in the spinal ganglion cells of the rat accompanying the long-lasting sensory disturbance induced by capsaicin. Life Sci 8: 621–626PubMedGoogle Scholar
  133. 133.
    Chiba T, Masuko S, Kawano H (1986) Correlation of mitochondrial swelling after capsaicin treatment and substance P and somatostatin immunoreactivity in small neurons of dorsal root ganglion in the rat. Neurosci Lett 64: 311–316PubMedCrossRefGoogle Scholar
  134. 134.
    Hoyes AD, Barber P (1981) Degeneration of axons in the ureteric and duodenal nerve plexuses of the adult rat following in vivo treatment with capsaicin. Neurosci Lett 25: 19–24PubMedCrossRefGoogle Scholar
  135. 135.
    Pethö G, Szolcsányi J (1996) Excitation of central and peripheral terminals of primary afferent neurons by capsaicin in vivo. Life Sci 58: 47–53Google Scholar
  136. 136.
    Caterina MJ, Rosen TA, Tominaga M, Brake AJ, Julius D (1999) A capsaicin receptor homologue with a high threshold for noxious heat. Nature 398: 436–441PubMedGoogle Scholar
  137. 137.
    Szallasi A, Appendino G (2004) Vanilloid receptor TRPV1 antagonists as the next generation of painkillers. Are we putting the cart before the horse? J Med Chem 47: 2717–2712PubMedCrossRefGoogle Scholar

Copyright information

© Birkhäuser Verlag Basel/Switzerland 2005

Authors and Affiliations

  • Zoltán Sándor
    • 1
  • Arpad Szallasi
    • 2
  1. 1.Department of Pharmacology and Pharmacotherapy, Faculty of MedicineUniversity of PécsPécsHungary
  2. 2.Department of PathologyMonmouth Medical CenterLong BranchUSA

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