Capsaicin-evoked iCGRP release from human dental pulp: A model system for the study of peripheral neuropeptide secretion in normal healthy tissue

Pain

Volumn 144, Issue 3, 2009, Pages 253-261

  Fehrenbacher, Jill C ^a   Sun, Xiaoling X ^a   Locke, Erin E ^a   Henry, Michael A ^a   Hargreaves, Kenneth M ^a,b  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^b Mays Cancer Center at UT Health San Antonio   (United States)

Author keywords

Analgesia; Calcitonin gene related peptide; Capsaicin; Clinical trial; Dental pulp; Exocytosis; Human; MOR; Morphine; Neuropeptide release; Pain; Sensory neuron; Translational studies; TRPV1

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; CALCIUM; CAPSAICIN; ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; NEUROPEPTIDE; PHORBOL 13 ACETATE 12 MYRISTATE; PROSTAGLANDIN E2; VANILLOID RECEPTOR 1;

ADULT; ARTICLE; CONCENTRATION RESPONSE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME ASSAY; ENZYME IMMUNOASSAY; EXOCYTOSIS; EXTRACELLULAR CALCIUM; FEMALE; HUMAN; HUMAN EXPERIMENT; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN VITRO STUDY; INFORMED CONSENT; MALE; MEDIATOR; MOLAR TOOTH; NERVE CELL; NOCICEPTIVE RECEPTOR; NONHUMAN; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; SENSORY NERVE; SENSORY NERVE CELL; TACHYPHYLAXIS; TOOTH EXTRACTION; TOOTH PULP;

ADOLESCENT; ADULT; BIOLOGICAL ASSAY; BIOPSY; CALCITONIN GENE-RELATED PEPTIDE; CAPSAICIN; DENTAL PULP; DINOPROSTONE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENKEPHALIN, ALA(2)-MEPHE(4)-GLY(5)-; FEMALE; HUMANS; IMMUNOENZYME TECHNIQUES; MALE; MIDDLE AGED; MODELS, BIOLOGICAL; MODELS, NEUROLOGICAL; NOCICEPTORS; PAIN; RECEPTORS, OPIOID, MU; SENSORY RECEPTOR CELLS; SENSORY SYSTEM AGENTS; TETRADECANOYLPHORBOL ACETATE; TRPV CATION CHANNELS; YOUNG ADULT;

EID: 67649502331     PISSN: 03043959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pain.2009.03.027     Document Type: Article

References (84)

1. Alexander SP, Mathie A, Peters JA. Guide to receptors and channels, 2nd edition. Br J Pharmacol 2006;147(Suppl 3):S1-168.
2. Alvarado L.T., Perry G.M., Hargreaves K.M., and Henry M.A. TRPM8 axonal expression is decreased in painful human teeth with irreversible pulpitis and cold hyperalgesia. J Endod 33 (2007) 1167-1171
3. Andreeva L., and Rang H.P. Effect of bradykinin and prostaglandins on the release of calcitonin gene-related peptide-like immunoreactivity from the rat spinal cord in vitro. Br J Pharmacol 108 (1993) 185-190
4. Aubrun F., Salvi N., Coriat P., and Riou B. Sex- and age-related differences in morphine requirements for postoperative pain relief. Anesthesiology 103 (2005) 156-160
5. Baad-Hansen L., Jensen T.S., and Svensson P. A human model of intraoral pain and heat hyperalgesia. J Orofac Pain 17 (2003) 333-340
6. Barrett A.C., Smith E.S., and Picker M.J. Capsaicin-induced hyperalgesia and mu-opioid-induced antihyperalgesia in male and female Fischer 344 rats. J Pharmacol Exp Ther 307 (2003) 237-245
7. Bartok R.E., and Craft R.M. Sex differences in opioid antinociception. J Pharmacol Exp Ther 282 (1997) 769-778
8. Berg K.A., Patwardhan A.M., Sanchez T.A., Silva Y.M., Hargreaves K.M., and Clarke W.P. Rapid modulation of micro-opioid receptor signaling in primary sensory neurons. J Pharmacol Exp Ther 321 (2007) 839-847
9. Bevan S., Hothi S., Hughes G., James I.F., Rang H.P., Shah K., Walpole C.S., and Yeats J.C. Capsazepine: a competitive antagonist of the sensory neurone excitant capsaicin. Br J Pharmacol 107 (1992) 544-552
10. Bevan S., and Szolcsanyi J. Sensory neuron-specific actions of capsaicin: mechanisms and applications. Trends Pharmacol Sci 11 (1990) 330-333
11. Bhatnagar M., Cintra A., Tinner B., Agnati L.F., Kerezoudis N., Edwall L., and Fuxe K. Neurotensin-like immunoreactivity in odontoblasts and their processes in rat maxillary molar teeth and the effect of pulpotomy. Regul Pept 58 (1995) 141-147
12. Brodin E., Gazelius B., Panopoulos P., and Olgart L. Morphine inhibits substance P release from peripheral sensory nerve endings. Acta Physiol Scand 117 (1983) 567-570
13. Byers M.R. Dynamic plasticity of dental sensory nerve structure and cytochemistry. Arch Oral Biol 39 Suppl (1994) 13S-21S
14. Byers M.R., and Taylor P.E. Effect of sensory denervation on the response of rat molar pulp to exposure injury. J Dent Res 72 (1993) 613-618
15. Carruthers A.M., Sellers L.A., Jenkins D.W., Jarvie E.M., Feniuk W., and Humphrey P.P. Adenosine A(1) receptor-mediated inhibition of protein kinase A-induced calcitonin gene-related peptide release from rat trigeminal neurons. Mol Pharmacol 59 (2001) 1533-1541
16. Caterina M.J., Leffler A., Malmberg A.B., Martin W.J., Trafton J., Petersen-Zeitz K.R., Koltzenburg M., Basbaum A.I., and Julius D. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288 (2000) 306-313
17. Cepeda M.S., and Carr D.B. Women experience more pain and require more morphine than men to achieve a similar degree of analgesia. Anesth Analg 97 (2003) 1464-1468
18. Chang H.M., Berde C.B., Holz G.G.t., Steward G.F., and Kream R.M. Sufentanil, morphine, met-enkephalin, and kappa-agonist (U-50, 488 H) inhibit substance P release from primary sensory neurons: a model for presynaptic spinal opioid actions. Anesthesiology 70 (1989) 672-677
19. Chang M.C., Chen Y.J., Tai T.F., Tai M.R., Li M.Y., Tsai Y.L., Lan W.H., Wang Y.L., and Jeng J.H. Cytokine-induced prostaglandin E2 production and cyclooxygenase-2 expression in dental pulp cells: downstream calcium signalling via activation of prostaglandin EP receptor. Int Endod J 39 (2006) 819-826
20. Chia Y.Y., Chow L.H., Hung C.C., Liu K., Ger L.P., and Wang P.N. Gender and pain upon movement are associated with the requirements for postoperative patient-controlled iv analgesia: a prospective survey of 2298 chinese patients. Can J Anaesth 49 (2002) 249-255
21. Cholewinski A., Burgess G.M., and Bevan S. The role of calcium in capsaicin-induced desensitization in rat cultured dorsal root ganglion neurons. Neuroscience 55 (1993) 1015-1023
22. Chuang H.H., Prescott E.D., Kong H., Shields S., Jordt S.E., Basbaum A.I., Chao M.V., and Julius D. Bradykinin and nerve growth factor release the capsaicin receptor from Ptdins(4, 5)P2-mediated inhibition. Nature 411 (2001) 957-962
23. Cicero T.J., Nock B., and Meyer E.R. Gender-related differences in the antinociceptive properties of morphine. J Pharmacol Exp Ther 279 (1996) 767-773
24. Cook C.D., and Nickerson M.D. Nociceptive sensitivity and opioid antinociception and antihyperalgesia in freund's adjuvant-induced arthritic male and female rats. J Pharmacol Exp Ther 313 (2005) 449-459
25. Davis A.J., and Perkins M.N. Substance P and capsaicin-induced mechanical hyperalgesia in the rat knee joint; the involvement of bradykinin B1 and B2 receptors. Br J Pharmacol 118 (1996) 2206-2212
26. Davis J.B., Gray J., Gunthorpe M.J., Hatcher J.P., Davey P.T., Overend P., Harries M.H., Latcham J., Clapham C., Atkinson K., Hughes S.A., Rance K., Grau E., Harper A.J., Pugh P.L., Rogers D.C., Bingham S., Randall A., and Sheardown S.A. Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 405 (2000) 183-187
27. Docherty R.J., Yeats J.C., Bevan S., and Boddeke H.W. Inhibition of calcineurin inhibits the desensitization of capsaicin-evoked currents in cultured dorsal root ganglion neurones from adult rats. Pflugers Arch 431 (1996) 828-837
28. Donnerer J., Schuligoi R., and Amann R. Time-course of capsaicin-evoked release of calcitonin gene-related peptide from rat spinal cord in vitro. Effect of concentration and modulation by ruthenium red. Regul Pept 37 (1992) 27-37
29. Duyk G. Attrition and translation. Science 302 (2003) 603-605
30. Escott K.J., Beattie D.T., Connor H.E., and Brain S.D. The modulation of the increase in rat facial skin blood flow observed after trigeminal ganglion stimulation. Eur J Pharmacol 284 (1995) 69-76
31. Fehrenbacher J.C., Taylor C.P., and Vasko M.R. Pregabalin and gabapentin reduce release of substance P and CGRP from rat spinal tissues only after inflammation or activation of protein kinase C. Pain 105 (2003) 133-141
32. Ferreira S.H., and Nakamura M. Ii - prostaglandin hyperalgesia: the peripheral analgesic activity of morphine, enkephalins and opioid antagonists. Prostaglandins 18 (1979) 191-200
33. Fillingim R.B., and Gear R.W. Sex differences in opioid analgesia: clinical and experimental findings. Eur J Pain 8 (2004) 413-425
34. Flores C.M., Leong A.S., Dussor G.O., Harding-Rose C., Hargreaves K.M., and Kilo S. Capsaicin-evoked CGRP release from rat buccal mucosa: development of a model system for studying trigeminal mechanisms of neurogenic inflammation. Eur J Neurosci 14 (2001) 1113-1120
35. Franco-Cereceda A. Prostaglandins and CGRP release from cardiac sensory nerves. Naunyn Schmiedebergs Arch Pharmacol 340 (1989) 180-184
36. Geppetti P., Del Bianco E., Tramontana M., Vigano T., Folco G.C., Maggi C.A., Manzini S., and Fanciullacci M. Arachidonic acid and bradykinin share a common pathway to release neuropeptide from capsaicin-sensitive sensory nerve fibers of the guinea pig heart. J Pharmacol Exp Ther 259 (1991) 759-765
37. Goodis H.E., Poon A., and Hargreaves K.M. Tissue pH and temperature regulate pulpal nociceptors. J Dent Res 85 (2006) 1046-1049
38. Hargreaves K.M., Jackson D.L., and Bowles W.R. Adrenergic regulation of capsaicin-sensitive neurons in dental pulp. J Endod 29 (2003) 397-399
39. Hingtgen C.M., and Vasko M.R. Prostacyclin enhances the evoked-release of substance P and calcitonin gene-related peptide from rat sensory neurons. Brain Res 655 (1994) 51-60
40. Holzer P. Local effector functions of capsaicin-sensitive sensory nerve endings: involvement of tachykinins, calcitonin gene-related peptide and other neuropeptides. Neuroscience 24 (1988) 739-768
41. Jaber L., Swaim W.D., and Dionne R.A. Immunohistochemical localization of mu-opioid receptors in human dental pulp. J Endod 29 (2003) 108-110
42. Jeske N.A., Patwardhan A.M., Gamper N., Price T.J., Akopian A.N., and Hargreaves K.M. Cannabinoid WIN 55, 212-2 regulates TRPV1 phosphorylation in sensory neurons. J Biol Chem 281 (2006) 32879-32890
43. Ji R.R., Samad T.A., Jin S.X., Schmoll R., and Woolf C.J. P38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron 36 (2002) 57-68
44. Ji Y., Murphy A.Z., and Traub R.J. Sex differences in morphine-induced analgesia of visceral pain are supraspinally and peripherally mediated. Am J Physiol Regul Integr Comp Physiol 291 (2006) R307-R314
45. Joris J.L., Dubner R., and Hargreaves K.M. Opioid analgesia at peripheral sites: a target for opioids released during stress and inflammation?. Anesth Analg 66 (1987) 1277-1281
46. Julius D., and Basbaum A.I. Molecular mechanisms of nociception. Nature 413 (2001) 203-210
47. Kest B., Sarton E., and Dahan A. Gender differences in opioid-mediated analgesia: animal and human studies. Anesthesiology 93 (2000) 539-547
48. Kilo S., Harding-Rose C., Hargreaves K.M., and Flores C.M. Peripheral CGRP release as a marker for neurogenic inflammation: a model system for the study of neuropeptide secretion in rat paw skin. Pain 73 (1997) 201-207
49. Koplas P.A., Rosenberg R.L., and Oxford G.S. The role of calcium in the desensitization of capsaicin responses in rat dorsal root ganglion neurons. J Neurosci 17 (1997) 3525-3537
50. Kuraishi Y., Hirota N., Sato Y., Hino Y., Satoh M., and Takagi H. Evidence that substance P and somatostatin transmit separate information related to pain in the spinal dorsal horn. Brain Res 325 (1985) 294-298
51. Lawson S.N., McCarthy P.W., and Prabhakar E. Electrophysiological properties of neurones with CGRP-like immunoreactivity in rat dorsal root ganglia. J Comp Neurol 365 (1996) 355-366
52. Levine J.D., and Taiwo Y.O. Involvement of the mu-opiate receptor in peripheral analgesia. Neuroscience 32 (1989) 571-575
53. Lipton J.A., Ship J.A., and Larach-Robinson D. Estimated prevalence and distribution of reported orofacial pain in the United States. J Am Dent Assoc 124 (1993) 115-121
54. Liu L., and Simon S.A. Capsaicin-induced currents with distinct desensitization and Ca2+ dependence in rat trigeminal ganglion cells. J Neurophysiol 75 (1996) 1503-1514
55. Luo S., Perry G.M., Levinson S.R., and Henry M.A. NaV1.7 expression is increased in painful human dental pulp. Mol Pain 4 (2008) 16
56. Miller P.L., and Ernst A.A. Sex differences in analgesia: a randomized trial of mu versus kappa opioid agonists. South Med J 97 (2004) 35-41
57. Morgan C.R., Rodd H.D., Clayton N., Davis J.B., and Boissonade F.M. Vanilloid receptor 1 expression in human tooth pulp in relation to caries and pain. J Orofac Pain 19 (2005) 248-260
58. Moriyama T., Iida T., Kobayashi K., Higashi T., Fukuoka T., Tsumura H., Leon C., Suzuki N., Inoue K., Gachet C., Noguchi K., and Tominaga M. Possible involvement of P2Y2 metabotropic receptors in ATP-induced transient receptor potential vanilloid receptor 1-mediated thermal hypersensitivity. J Neurosci 23 (2003) 6058-6062
59. Morton C.R., and Hutchison W.D. Release of sensory neuropeptides in the spinal cord: studies with calcitonin gene-related peptide and galanin. Neuroscience 31 (1989) 807-815
60. Ngom P.I., Dubray C., Woda A., and Dallel R. A human oral capsaicin pain model to assess topical anesthetic-analgesic drugs. Neurosci Lett 316 (2001) 149-152
61. Okamoto K., Tashiro A., Hirata H., and Bereiter D.A. Differential modulation of TMJ neurons in superficial laminae of trigeminal subnucleus caudalis/upper cervical cord junction region of male and cycling female rats by morphine. Pain 114 (2005) 203-211
62. Patwardhan A.M., Berg K.A., Akopain A.N., Jeske N.A., Gamper N., Clarke W.P., and Hargreaves K.M. Bradykinin-induced functional competence and trafficking of the delta-opioid receptor in trigeminal nociceptors. J Neurosci 25 (2005) 8825-8832
63. Patwardhan A.M., Diogenes A., Berg K.A., Fehrenbacher J.C., Clarke W.P., Akopian A.N., and Hargreaves K.M. PAR-2 agonists activate trigeminal nociceptors and induce functional competence in the delta opioid receptor. Pain 125 (2006) 114-124
64. Pol O., and Puig M.M. Expression of opioid receptors during peripheral inflammation. Curr Top Med Chem 4 (2004) 51-61
65. Renton T., Yiangou Y., Baecker P.A., Ford A.P., and Anand P. Capsaicin receptor VR1 and ATP purinoceptor P2X3 in painful and nonpainful human tooth pulp. J Orofac Pain 17 (2003) 245-250
66. Ruparel N.B., Patwardhan A.M., Akopian A.N., and Hargreaves K.M. Homologous and heterologous desensitization of capsaicin and mustard oil responses utilize different cellular pathways in nociceptors. Pain 135 (2008) 271-279
67. Schafer M., Imai Y., Uhl G.R., and Stein C. Inflammation enhances peripheral mu-opioid receptor-mediated analgesia, but not mu-opioid receptor transcription in dorsal root ganglia. Eur J Pharmacol 279 (1995) 165-169
68. Southall M.D., Michael R.L., and Vasko M.R. Intrathecal NSAIDs attenuate inflammation-induced neuropeptide release from rat spinal cord slices. Pain 78 (1998) 39-48
69. Southall M.D., and Vasko M.R. Prostaglandin E(2)-mediated sensitization of rat sensory neurons is not altered by nerve growth factor. Neurosci Lett 287 (2000) 33-36
70. Stein C., Schafer M., and Machelska H. Attacking pain at its source: new perspectives on opioids. Nat Med 9 (2003) 1003-1008
71. Suarez-Roca H., Abdullah L., Zuniga J., Madison S., and Maixner W. Multiphasic effect of morphine on the release of substance P from rat trigeminal nucleus slices. Brain Res 579 (1992) 187-194
72. Suarez-Roca H., and Maixner W. Morphine produces a biphasic modulation of substance P release from cultured dorsal root ganglion neurons. Neurosci Lett 194 (1995) 41-44
73. Sugiuar T., Bielefeldt K., and Gebhart G.F. TRPV1 function in mouse colon sensory neurons is enhanced by metabotropic 5-hydroxytryptamine receptor activation. J Neurosci 24 (2004) 9521-9530
74. Sun R.Q., Lawand N.B., and Willis W.D. The role of calcitonin gene-related peptide (CGRP) in the generation and maintenance of mechanical allodynia and hyperalgesia in rats after intradermal injection of capsaicin. Pain 104 (2003) 201-208
75. Svensson P., Arendt-Nielsen L., Bjerring P., Bak P., Hjorth T., and Troest T. Human mastication modulated by experimental trigeminal and extra-trigeminal painful stimuli. J Oral Rehabil 23 (1996) 838-848
76. Szolcsanyi J. Forty years in capsaicin research for sensory pharmacology and physiology. Neuropeptides 38 (2004) 377-384
77. Taylor P.E., Byers M.R., and Redd P.E. Sprouting of CGRP nerve fibers in response to dentin injury in rat molars. Brain Res 461 (1988) 371-376
78. Ulrich-Lai Y.M., Flores C.M., Harding-Rose C.A., Goodis H.E., and Hargreaves K.M. Capsaicin-evoked release of immunoreactive calcitonin gene-related peptide from rat trigeminal ganglion: evidence for intraganglionic neurotransmission. Pain 91 (2001) 219-226
79. Urban L., and Dray A. Capsazepine, a novel capsaicin antagonist, selectively antagonises the effects of capsaicin in the mouse spinal cord in vitro. Neurosci Lett 134 (1991) 9-11
80. Vasko M.R. Prostaglandin-induced neuropeptide release from spinal cord. Prog Brain Res 104 (1995) 367-380
81. Vasko M.R., Zirkelbach S.L., and Waite K.J. Prostaglandins stimulate the release of substance P from rat spinal cord slices. Prog Pharmacol Clin Pharmacol 10 (1993) 69-89
82. Vetter I., Wyse B.D., Monteith G.R., Roberts-Thomson S.J., and Cabot P.J. The mu opioid agonist morphine modulates potentiation of capsaicin-evoked TRPV1 responses through a cyclic AMP-dependent protein kinase A pathway. Mol Pain 2 (2006) 22
83. Voets T., Droogmans G., Wissenbach U., Janssens A., Flockerzi V., and Nilius B. The principle of temperature-dependent gating in cold- and heat-sensitive TRP channels. Nature 430 (2004) 748-754
84. Zollner C., Shaqura M.A., Bopaiah C.P., Mousa S., Stein C., and Schafer M. Painful inflammation-induced increase in mu-opioid receptor binding and G-protein coupling in primary afferent neurons. Mol Pharmacol 64 (2003) 202-210