Polymodality in Nociceptive Neurons: Experimental Models of Chemotransduction

  • Carlos Belmonte
  • Juana Gallar
  • Laura G. Lopez-Briones
  • Miguel A. Pozo
Part of the NATO ASI Series book series (volume 79)

Abstract

Transduction of chemical changes in the environment is present in all levels of living organisms, from protozoa to man. In bacteria, chemotransduction mediates a modification of flagellar motion that biases the individual cell’s random displacement, leading to an accumulation if the chemical cue is an attractant or to a dispersion in the case of a repellent. Likewise, in metazoans chemotransduction is involved in chemical detection of nutrients and mates, and triggers also behavioral mechanisms to approach or escape the stimulus72.

Keywords

Fatigue Histamine Prostaglandin Acetylcholine PGE2 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    ANTON, F., EUCHNER, I. and HANDWERKER, H.O. (1992) Psychophysical examination of pain induced by defined CO2 pulses applied to the nasal mucosa. Pain 49, 53–60.PubMedCrossRefGoogle Scholar
  2. 2.
    AKAIKE, N., KRISHTAL, OA. and MARUYAMA, T. (1990) Proton-induced current in frog isolated dorsal root ganglion cells. J. Neurophysiol. 805–813.Google Scholar
  3. 3.
    Baccaglini, P.I. and Hogan, P.G. (1983) Some rat sensory neurons in culture express characteristics of differentiated pain sensory cells. Proc. Natl. Acad. Sci. USA. 80, 594–598.PubMedCrossRefGoogle Scholar
  4. 4.
    Belmonte, C., Gallar, J., Pozo, M.A. and Rebollo, I. (1991) Excitation by irritant chemical substances of sensory afferent units in the cat’s cornea. J. Physiol. 437, 709–725.PubMedGoogle Scholar
  5. 5.
    Belmonte, C. and Giraldez, F. (1981) Responses of cat corneal sensory receptors to mechanical and thermal stimulation. J. Physiol. 321, 355–368.PubMedGoogle Scholar
  6. 6.
    Bessou, P. and Perl, E.R. (1969) Response of cutaneous sensory units with unmyelinated fibers to noxious stimuli. J. Neurophysiol. 32, 1025–1043.PubMedGoogle Scholar
  7. 7.
    Beuerman, R.W. and Tanelian, D.L. Corneal pain evoked by thermal stimulation. Pain 1979; 7: 1–14.PubMedCrossRefGoogle Scholar
  8. 8.
    Bevan, S. and Yeats, J. (1991) Protons activate a cation conductance in a sub-population of rat dorsal root ganglion neurones. J. Physiol. 433, 145–161.PubMedGoogle Scholar
  9. 9.
    Blumberg, H. and Jänig, W. (1984) Discharge pattern of afferent fibers from a neuroma. Pain 20, 335–353.PubMedCrossRefGoogle Scholar
  10. 10.
    Burgess, G.M., Mullaney, I., McNeill, M., Dunn, P. and Rang, H.P. (1989) Second messengers involved in the action on bradykinin on cultured sensory neurons. J. Neurosci. 9, 3314–3325.PubMedGoogle Scholar
  11. 11.
    Cervero, F. (1982) Afferent activity evoked by natural stimulation of the biliary system in the ferret. Pain 13, 137–151.PubMedCrossRefGoogle Scholar
  12. 12.
    Chahl, L.A. (1991) Antidromic vasodilatation and neurogenic inflammation. In: Novel Peripheral Neurotransmitters, ed. C. Bell. Pergamon Press.Google Scholar
  13. 13.
    Chang-Ling, T. (1989) Sensitivity and neural organization of the cat cornea. Invest. Ophthalmol. Vis. Sci. 30, 1075–1082.Google Scholar
  14. 14.
    Chen, X., Pozo, M.A., Baeza, M., Gallar, J. and Belmonte, C. (1993) Stimulation of corneal nerve fibers by CO2: a method to measure corneal sensitivity. Invest. Ophthalmol. Vis. Sci. (suppl. ARVO Meeting).Google Scholar
  15. 15.
    Devor, M. (1991) Neuropathic pain and injured nerve: peripheral mechanisms. Br. Med. Bull. 47, 619–630.PubMedGoogle Scholar
  16. 16.
    Dray, A., Bettaney, J., Foster, P. and Perkins, M.N. (1988) Bradykinin-induced stimulation of afferent fibres is mediated through protein kinase C. Neurosci. Lett. 91, 301–307.PubMedCrossRefGoogle Scholar
  17. 17.
    Dray, A., Forbes, C.A. and Burgess, G.M. (1990) Ruthenium red blocks the capsaicin-induced increase of intracellular calcium and activation of membrane currents in sensory neurons as well as the activation of peripheral nociceptors in vitro. Neurosci. Lett. 110, 52–59.PubMedCrossRefGoogle Scholar
  18. 18.
    Dray, A. and Wood, J.N. (1991) Nonopioid molecular signaling mechanisms involved in nociception and antinociception. In: Towards a New Pharmacotherapy of Pain. eds. A. I. Basbaum, J.M. Besso. John Wiley & Sons Ltd.Google Scholar
  19. 19.
    Fjällbrant, N. and Iggo, A. (1961) The effect of histamine, 5-hydroxytryptamine and acetylcholine on cutaneous afferent fibres. J. Physiol. 156, 5788–590.Google Scholar
  20. 20.
    Gallar, J. and Belmonte, C. (1990) Modulation by prostaglandins of nervous activity in corneal nociceptors. Invest. Ophthalmol. Vis. Sci. 31, (suppl): 514.Google Scholar
  21. 21.
    Gallar, J., Pozo, M.A. and Belmonte, C. Unpublished results.Google Scholar
  22. 22.
    Gallar, J., Pozo, M.A., Tuckett R.P. and Belmonte, C. (1993) Response of unmyelinated fibres to mechanical, thermal and chemical stimulation of the cat’s cornea. J. Physiol. 468, 609–622.PubMedGoogle Scholar
  23. 23.
    Garcia De La Rubia, P., Gonzalez, G.G., Gallar, J. and Belmonte, C. (1993) Attenuation of anterior segment inflammation by blockade of sensory nerves with calcium antagonist diltiazem. Invest. Ophthalmol. Vis. Sci (in press).Google Scholar
  24. 24.
    Gonzalez, G.G., Gallar, J. and Belmonte, C. (1992) Polymodal nociceptors and neurogenic inflammation in the cornea. Exp Eye Res. 55 (suppl. 1), S53.CrossRefGoogle Scholar
  25. 25.
    Gonzalez, G.G., Garcia, De La Rubia, P., Gallar, J. and Belmonte, C. Reduction of capsaicin-induced ocular pain and neurogenic inflammation. Invest. Ophthalmol. Vis. Sci. (submitted).Google Scholar
  26. 26.
    Grubb, B.D., Birrell, G.J., McQuenn, D.S. and Iggo, A. (1991) The role of PGE2 in the sensitization of mechanoreceptors in normal and inflamed ankle joints of the rat. Exp. Brain Res. 84, 383–392.PubMedCrossRefGoogle Scholar
  27. 27.
    Häbler, H.J., Jänig, W. and Koltzenburg, M. (1990) Activation of unmyelinated afferent fibres by mechanical stimuli and inflammation of the urinary bladder in the cat. J. Physiol. 425, 545–562.PubMedGoogle Scholar
  28. 28.
    Handwerker, H.O. (1991) What peripheral mechanisms contribute to nociceptive transmission and hyperalgesia?. In: Towards a New Pharmacology of Pain. eds. A. I. Basbaum, J.-M. Besson. John Wiley & Sons.Google Scholar
  29. 29.
    Handwerker, H.O. and Reeh, P.W. (1991) Pain and inflammation. Proc. VIth World Congress on Pain. 59–70.Google Scholar
  30. 30.
    Hartung, M., Leah, J. and Zimmermann, M. (1989) The excitation of cutaneous nerve endings in a neuroma by capsaicin. Brain Res. 499, 363–366.PubMedCrossRefGoogle Scholar
  31. 31.
    Haynes, L.W. (1992) Block of the cyclic GMP-gated channel of vertebrate rod and cone photoreceptors by I-cis-diltiazem. J. Gen. Physiol. 100, 783–801.PubMedCrossRefGoogle Scholar
  32. 32.
    Hunt, S.P., Pini, A. and Evan, G. (1987) Induction of c-fos-like protein in spinal cord neurons following sensory stimulation. Nature 328, 632–634.PubMedCrossRefGoogle Scholar
  33. 33.
    Jancso, N., Jancso-Gabor, A., Szolcsányi, J. (1968) The role of sensory nerve endings in neurogenic inflammation induced by human skin and in the eye and paw of the rat. Br. J. Pharmacol. Chemother. 33, 32–41.PubMedGoogle Scholar
  34. 34.
    Kanaka, R., Schaible, H.G. and Schmidt, R.F. (1985) Activation of fine articular afferent units by bradykinin. Brain Res. 327, 81–90.PubMedCrossRefGoogle Scholar
  35. 35.
    Kaupp, U.B. (1991) The cyclic nucleotide-gated channels of vertebrate photoreceptors and olfactory epithelium. Trends Neurosci. 14, 150–157.PubMedCrossRefGoogle Scholar
  36. 36.
    Kaupp, U.B. and Kock, K.W. (1992) Role of cGMP and Ca2+ in vertebrate photoreceptor excitation and adaptation. Ann. rev. Physiol. 54, 153–175.CrossRefGoogle Scholar
  37. 37.
    Keele, C.A. (1962) The common chemical sense and its receptors. Arch. Int. Pharmacodyn. 139, 547–57.PubMedGoogle Scholar
  38. 38.
    Kenins, P. (1982) Response of single nerve fibers to capsaicin applied to the skin. Neurosci Lett. 29, 83–88.PubMedCrossRefGoogle Scholar
  39. 39.
    Kenshalo, D.R. (1960) Comparison of thermal sensitivity of the forehead, lip, conjunctiva and cornea. J. Appl. Physiol. 15, 987–991.PubMedGoogle Scholar
  40. 40.
    Kessler, W., Kirchhoff, C., Reeh, P.W. and Handwerker, H.O. (1992) Excitation of cutaneous afferent nerve endings in vitro by a combination of inflammatory mediators and conditioning effect of substance P. Exp. Brain Res. 91, 467–476.PubMedCrossRefGoogle Scholar
  41. 41.
    Kirchhoff, C., Jung, S., Reeh, P.W. and Handwerker, HO. (1990) Carragenaan inflammation increases bradykinin sensitivity of rat cutaneous nociceptors. Neurosci. Lett. 111, 206–210.PubMedCrossRefGoogle Scholar
  42. 42.
    Kirchhoff, C., Leah, J.D., Jung, S. and Reeh, P.W. (1992) Excitation of cutaneous sensory nerve endings in the rat by 4-aminopyridine and tetraethylammonium. J. Neurophysiol. 67, 125–131.PubMedGoogle Scholar
  43. 43.
    Konnerth, A., Lux, H.D. and Morad, M. (1987) Proton-induced transformation of calcium channel in chick dorsal root ganglion cells. J. Physiol. 386, 603–633.PubMedGoogle Scholar
  44. 44.
    Kumazawa, T. and Mizumura, K. (1977) Thin-fibre receptors responding to mechanical, chemical and thermal stimulation in the skeletal muscle of the dog. J. Physiol. 273, 179–194.PubMedGoogle Scholar
  45. 45.
    Kumazawa, T. and Mizumura, K. (1980) Chemical responses of polymodal receptors of the scrotal contents in dogs. J. Physiol. 299, 219–232.PubMedGoogle Scholar
  46. 46.
    Kumazawa, T, and Perl, E.R. (1977) Primate cutaneous sensory units with unmyelinated (C) afferent fibers. J. Neurophysiol. 40, 1325–1338.PubMedGoogle Scholar
  47. 47.
    Lang, E., Novak, A., Reeh, P. and Handwerker, H.O. (1990) Chemosensitivity of fine afferents from rat skin in vitro. J. Neurophysiol. 63, 887–901.PubMedGoogle Scholar
  48. 48.
    Lindahl O. (1961) Experimental skin pain induced by injection of water-soluble substances in humans. Acta Physiol. Scand. 179, (suppl.), 1–89.Google Scholar
  49. 49.
    López-Briones, L.G., García-Hirschfeld, J., Valdeolmillos, M. and Belmonte, C. (1993) Calcium transients produced by pH changes and capsaicin in cultured trigeminal neurons, (in preparation).Google Scholar
  50. 50.
    Lynn, B. and Baranowski, R.A. (1987) Comparison of the relative numbers and properties of cutaneous nociceptive afferents in different mammalian species. In: Fine afferent nerve fibers and pain. eds. R.F. Schmidt et al. VCH Publishers.Google Scholar
  51. 51.
    Maggi, C.A. (1991) Capsaicin and primary afferent neurons: from basic science to human therapy?. J. Auton Nerv. Sys. 33, 1–14.CrossRefGoogle Scholar
  52. 52.
    Martinez, S. and Belmonte, C. C-fos expression in trigeminal nucleus neurones after chemical irritation of the cornea: reduction by selective blockade of nociceptor’s chemosensitivity. Eur. J. Neurosci. (submitted).Google Scholar
  53. 53.
    Mense, S. (1977) Nervous outflow from skeletal muscle following chemical noxious stimulation. J Physiol. 267, 75–88.PubMedGoogle Scholar
  54. 54.
    Mizumura, K., Sato, J. and Kumazawa, T. (1987) Effects of prostaglandins and other putative chemical intermediaries on the activity of canine testicular polymodal receptors studied in vitro. Pflügers Arch. 408, 565–572.PubMedCrossRefGoogle Scholar
  55. 55.
    Nicholls, J.G. and Baylor, DA. (1968) Specific modalities and receptive fields of sensory neurons in CNS of the leech. J. Neurophysiol. 31, 740–756.PubMedGoogle Scholar
  56. 56.
    Pastor, J.E., Soria, B. and Belmonte, C. (1993) Nociceptive responses in the N neuron of the leech. Proc. 16th Meeting of the European Neuroscience Association, Madrid.Google Scholar
  57. 57.
    Pozo, M.A., Gallego, R., Gallar, J. and Belmonte, C. (1992) Blockade by calcium antagonists of chemical excitation and sensitization of polymodal nociceptors in the cat’s cornea. J. Physiol. 450, 179–189.PubMedGoogle Scholar
  58. 58.
    Rang, H.P., Bevan, S. and Dray, A. (1991) Chemical activation of nociceptive peripheral neurones. Br. Med. Bull. 47 (3), 534–548.PubMedGoogle Scholar
  59. 59.
    Rebollo, I. and Belmonte, C. (1988) Effects of substance P and SP-antagonists on the neural activity of corneal sensory fibers. Proc. 8th International Congress of Eye Research. 110.Google Scholar
  60. 60.
    Reeh, P.W. (1986) Sensory receptors in mammalian skin in an in vitro preparation. Neurosci. Lett. 66, 141–146.PubMedCrossRefGoogle Scholar
  61. 61.
    Rivera, L., Gallar, J., Pozo, M.A. and Belmonte, C. (1993) Chemical responses of sensory neuromas: an ‘in vitro’ study. Proc. 16th Meeting of the European Neuroscience Association.Google Scholar
  62. 62.
    Sato, J., Mizumura, K. and Kumazawa, T. (1989) Effects of ionic calcium on the response of canine testicular polymodal receptors to algesic substances. J. Neurophysiol. 62, 119–125.PubMedGoogle Scholar
  63. 63.
    Schaible, H.G. and Schmidt, RF. (1985) Effects of an experimental arthritis on the sensory properties of fine articular nerves. J. Neurophysiol. 54, 1109–1122.PubMedGoogle Scholar
  64. 64.
    Schaible, H.G. and Schmidt, R.F. (1988) Direct observation of the sensitization of articular afferents during an experimental arthritis. In: Pain Research and Clinical Management, vol 3, Proc. VIth World Congress on Pain. eds. R. Dubner et al. Elsevier.Google Scholar
  65. 65.
    Schaible, H.G. and Schmidt, R.F. (1988) Excitation and sensitization of fine articular afferents from cat’s knee joint by prostaglandin E2. J. Physiol. 403, 91–104.PubMedGoogle Scholar
  66. 66.
    Silver, W.L. and Finger, T.E. (1991) The trigeminal system. In: Smell and Taste in Health and Disease, eds. T.V. Getchell et al. Raven Press.Google Scholar
  67. 67.
    Steen, K.H., Reeh, P.W., Anton, F. and Handwerker, H.O. (1992) Protons selectively induce lasting excitation and sensitization to mechanical stimulation of nociceptors in rat skin, in vitro. J. Neurosci. 12, 86–95.PubMedGoogle Scholar
  68. 68.
    Stone, R.A., Kuwayama, Y. and Laties, A.M. (1987) Regulatory peptides in the eye. Experiential, 791–800.PubMedCrossRefGoogle Scholar
  69. 69.
    Szolcsányi, J. (1987) Selective responsiveness of polymodal nociceptors of the rabbit ear to capsaicin, bradykinin and ultra-violet irradiation. J. Physiol. 388, 9–23.PubMedGoogle Scholar
  70. 70.
    Szolcsányi, J., Anton, F., Reeh, P. and Handwerker, H.O. (1988) Selective excitation by capsaicin of mechano-heat sensitive nociceptors in rat skin. Brain Res. 446, 262–268.PubMedCrossRefGoogle Scholar
  71. 71.
    Van Essen, D.C. (1973) The contribution of membrane hyperpolarization to adaptation and conduction block in sensory neurones of the leech. J. Physiol. 230, 509–534.PubMedGoogle Scholar
  72. 72.
    Van Houten, J. (1991) Chemosensory transduction in Paramecium. In: Biology of chemotactic response, eds. J. Armitage and J. Lackie. Cambridge University Press.Google Scholar
  73. 73.
    Weelk, E., Leah, J.D. and Zimmermann, M. (1990) Characteristics of A- and C-fibers ending in a sensory nerve neuroma in the rat. J. Neurophysiol. 63, 759–766.Google Scholar
  74. 74.
    Wood, J.N., Bevan, S.J., Coote, P.R., Dunn, P.M., Harmar, A., Hogan, P., Larchman, D.S., Morrison, C., Rougon, G., Theveniau, M. and Wheatley, S. (1990) Novel cell lines display properties of nociceptive sensory neurons. Proc. R. Soc. Lond. B. 241, 187–194.CrossRefGoogle Scholar
  75. 75.
    WOOD, J.N., WINTER, J., JAMES, I.F., RANG, H.P., YEATS, J. and BEVAN, S. (1988) Capsaicin-induced ion fluxes in dorsal root ganglion cells in culture. J. Neurosci. 8, 3208–3220.PubMedGoogle Scholar
  76. 76.
    WOOLF, C.J. and WALTERS, E.T. (1991) Common patterns of plasticity contributing to nociceptive sensitization in mammals and Aplysia. Trends Neurosci. 14 (2), 74–78.PubMedCrossRefGoogle Scholar
  77. 77.
    ZIMMERMANN, M. and KORSCHORKE, G.M. (1987) Chemosensitivity of nerve sprouts in experimental neuroma of cutaneous nerves of the cat. In: Fine afferent nerve fibers and pain. EDS. r.f. Schmidt RF et al. VCH Publishers.Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1994

Authors and Affiliations

  • Carlos Belmonte
    • 1
  • Juana Gallar
    • 1
  • Laura G. Lopez-Briones
    • 1
  • Miguel A. Pozo
    • 1
  1. 1.Departamento de Fisiologia and Instituto de NeurocienciasUniversidad de AlicanteAlicanteSpain

Personalised recommendations