PAIN
Volume 141, Issue 1 , Pages 41-51 , January 2009

Trpv1 mediates spontaneous firing and heat sensitization of cutaneous primary afferents after plantar incision

  • Ratan K. Banik

      Affiliations

    • Departments of Anesthesia and Pharmacology, University of Iowa Hospitals and Clinics, Iowa City, IA, USA
    • Pain Research Program, NJ Neuroscience Institute and Seton Hall University School of Graduate Medical Education, JFK Medical Center, 65 James St., Edison, NJ, USA
    • Corresponding Author InformationCorresponding author. Address: Pain Research Program, NJ Neuroscience Institute and Seton Hall University School of Graduate Medical Education, JFK Medical Center, Edison, NJ 08820, USA. Tel.: +1 732 321 7000x68567/68535; fax: +1 732 744 5821.
    • ,
  • Timothy J. Brennan

      Affiliations

    • Departments of Anesthesia and Pharmacology, University of Iowa Hospitals and Clinics, Iowa City, IA, USA

Received 27 May 2008 ,Revised 11 September 2008 ,Accepted 7 October 2008.

References 

  1. Caterina MJ, Julius D. Sense and specificity: a molecular identity for nociceptors. Curr Opin Neurobiol. 1999;9:525–530
  2. Tominaga M, Caterina MJ, Malmberg AB, Rosen TA, Gilbert H, Skinner K, et al. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron. 1998;21:531–543
  3. Caterina MJ, Julius D. The vanilloid receptor: a molecular gateway to the pain pathway. Annu Rev Neurosci. 2001;24:487–517
  4. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature. 1997;389:816–824
  5. Tillman DB, Treede RD, Meyer RA, Campbell JN. Response of C fibre nociceptors in the anaesthetized monkey to heat stimuli: correlation with pain threshold in humans. J Physiol. 1995;485:767–774
  6. Davis JB, Gray J, Gunthorpe MJ, Hatcher JP, Davey PT, Overend P, et al. Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature. 2000;405:183–187
  7. Woodbury CJ, Zwick M, Wang S, Lawson JJ, Caterina MJ, Koltzenburg M, et al. Nociceptors lacking TRPV1 and TRPV2 have normal heat responses. J Neurosci. 2004;24:6410–6415
  8. Pingle SC, Matta JA, Ahern GP. Capsaicin receptor: TRPV1 a promiscuous TRP channel. Handbook Exp Pharmacol. 2007;155–171
  9. Woo YC, Park SS, Subieta AR, Brennan TJ. Changes in tissue pH and temperature after incision indicate acidosis may contribute to postoperative pain. Anesthesiology. 2004;101:468–475
  10. Chuang HH, Prescott ED, Kong H, Shields S, Jordt SE, Basbaum AI, et al. Bradykinin and nerve growth factor release the capsaicin receptor from PtdIns(4, 5)P2-mediated inhibition. Nature. 2001;411:957–962
  11. Ji RR, Samad TA, Jin SX, Schmoll R, Woolf CJ. P38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron. 2002;36:57–68
  12. Zhang X, Huang J, McNaughton PA. NGF rapidly increases membrane expression of TRPV1 heat-gated ion channels. EMBO J. 2005;24:4211–4223
  13. Pogatzki EM, Gebhart GF, Brennan TJ. Characterization of Adelta- and C-fibers innervating the plantar rat hindpaw one day after an incision. J Neurophysiol. 2002;87:721–731
  14. Banik RK, Brennan TJ. Spontaneous discharge and increased heat sensitivity of rat C-fiber nociceptors are present in vitro after plantar incision. Pain. 2004;112:204–213
  15. Pogatzki-Zahn EM, Shimizu I, Caterina M, Raja SN. Heat hyperalgesia after incision requires TRPV1 and is distinct from pure inflammatory pain. Pain. 2005;115:296–307
  16. Reeh PW, Petho G. Nociceptor excitation by thermal sensitization – a hypothesis. Prog Brain Res. 2000;129:39–50
  17. Banik RK, Subieta R, Brennan TJ. TrpV1 in primary afferent terminals mediates plantar incision-induced heat hyperalgesia. 35th Annual Meeting of Society for Neuroscience, Washington, DC: SFN online; 2005.
  18. Banik RK, Woo YC, Park SS, Brennan TJ. Strain and sex influence on pain sensitivity after plantar incision in the mouse. Anesthesiology. 2006;105:1246–1253
  19. Pogatzki EM, Raja SN. A mouse model of incisional pain. Anesthesiology. 2003;99:1023–1027
  20. Banik RK, Brennan TJ. Sensitization of primary afferents to mechanical and heat stimuli after incision in a novel in vitro mouse glabrous skin-nerve preparation. Pain. 2008;138:380–391
  21. Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, et al. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science. 2000;288:306–313
  22. Patapoutian A, Peier AM, Story GM, Viswanath V. ThermoTRP channels and beyond: mechanisms of temperature sensation. Nat Rev Neurosci. 2003;4:529–539
  23. Bolcskei K, Helyes Z, Szabo A, Sandor K, Elekes K, Nemeth J, et al. Investigation of the role of TRPV1 receptors in acute and chronic nociceptive processes using gene-deficient mice. Pain. 2005;117:368–376
  24. Kanai Y, Hara T, Imai A, Sakakibara A. Differential involvement of TRPV1 receptors at the central and peripheral nerves in CFA-induced mechanical and thermal hyperalgesia. J Pharm Pharmacol. 2007;59:733–738
  25. Barton NJ, McQueen DS, Thomson D, Gauldie SD, Wilson AW, Salter DM, et al. Attenuation of experimental arthritis in TRPV1R knockout mice. Exp Mol Pathol. 2006;81:166–170
  26. Georgopoulos AP. Functional properties of primary afferent units probably related to pain mechanisms in primate glabrous skin. J Neurophysiol. 1976;39:71–83
  27. Treede RD, Meyer RA, Raja SN, Campbell JN. Evidence for two different heat transduction mechanisms in nociceptive primary afferents innervating monkey skin. J Physiol 1995;483:747–58.
  28. Granovsky Y, Matre D, Sokolik A, Lorenz J, Casey KL. Thermoreceptive innervation of human glabrous and hairy skin: a contact heat evoked potential analysis. Pain. 2005;115:238–247
  29. Lawson JJ, McIlwrath SL, Woodbury CJ, Davis BM, Koerber HR. TRPV1 unlike TRPV2 is restricted to a subset of mechanically insensitive cutaneous nociceptors responding to heat. J Pain. 2008;9:298–308
  30. Kress M, Koltzenburg M, Reeh PW, Handwerker HO. Responsiveness and functional attributes of electrically localized terminals of cutaneous C-fibers in vivo and in vitro. J Neurophysiol. 1992;68:581–595
  31. Meyer RA, Davis KD, Cohen RH, Treede RD, Campbell JN. Mechanically insensitive afferents (MIAs) in cutaneous nerves of monkey. Brain Res. 1991;561:252–261
  32. Handwerker HO, Kilo S, Reeh PW. Unresponsive afferent nerve fibres in the sural nerve of the rat. J Physiol. 1991;435:229–242
  33. Schmelz M, Schmidt R, Ringkamp M, Handwerker HO, Torebjork HE. Sensitization of insensitive branches of C nociceptors in human skin. J Physiol. 1994;480:389–394
  34. Kumazawa T. The polymodal receptor: biowarning and defense system. In:  Kumazawa T,  Kruger L,  Mizumura K editor. The polymodal receptor: A gateway to pathological pain. Elsevier; 1996;
  35. Tominaga M, Caterina MJ. Thermosensation and pain. J Neurobiol. 2004;61:3–12
  36. Banik RK, Subieta AR, Wu CR, Brennan TJ. Increased nerve growth factor after rat plantar incision contributes to guarding behavior and heat hyperalgesia. Pain. 2005;117:68–76
  37. Wu C, Boustany L, Liang H, Brennan TJ. Nerve growth factor expression after plantar incision in the rat. Anesthesiology. 2007;107:128–135
  38. Koc M, Tez M, Yoldas O, Dizen H, Gocmen E. Cooling for the reduction of postoperative pain: prospective randomized study. Hernia. 2006;10:184–186
  39. Saito N, Horiuchi H, Kobayashi S, Nawata M, Takaoka K. Continuous local cooling for pain relief following total hip arthroplasty. J Arthroplasty. 2004;19:334–337
  40. Fader DJ, Sax DS, Hamilton TA. Quantifying postoperative pain reduction using the dynamic cooling device to treat pediatric patients with port-wine stains. Arch Dermatol. 2000;136:1416–1417
  41. Fountas KN, Kapsalaki EZ, Johnston KW, Smisson HF, Vogel RL, Robinson JS, et al. Postoperative lumbar microdiscectomy pain. Minimalization by irrigation and cooling. Spine. 1999;24:1958–1960
  42. Brandner B, Munro B, Bromby LM, Hetreed M. Evaluation of the contribution to postoperative analgesia by local cooling of the wound. Anaesthesia. 1996;51:1021–1025
  43. Munst P, Bonnaire F, Kuner EH. The effect of postoperative cold therapy in joint surgery using a new cooling device. Unfallchirurgie. 1988;14:224–230
  44. Reeh PW, Kocher L, Jung S. Does neurogenic inflammation alter the sensitivity of unmyelinated nociceptors in the rat?. Brain Res. 1986;384:42–50
  45. LaMotte RH, Lundberg LE, Torebjork HE. Pain. Hyperalgesia and activity in nociceptive C units in humans after intradermal injection of capsaicin J Physiol. 1992;448:749–764
  46. Kichko TI, Reeh PW. Why cooling is beneficial: non-linear temperature-dependency of stimulated iCGRP release from isolated rat skin. Pain. 2004;110:215–219

PII: S0304-3959(08)00602-7

doi: 10.1016/j.pain.2008.10.004

PAIN
Volume 141, Issue 1 , Pages 41-51 , January 2009

Article Tools

* Image Usage & Resolution