The Journal of Pain
Volume 11, Issue 6 , Pages 588-599 , June 2010

Spinal Nerve Ligation in Mouse Upregulates TRPV1 Heat Function in Injured IB4-Positive Nociceptors

  • Daniel Vilceanu

      Affiliations

    • Department of Cell Biology, Neurobiology, and Anatomy, Medical College of Wisconsin, Milwaukee, Wisconsin
  • ,
  • Prisca Honore

      Affiliations

    • Neuroscience Research, Global Pharmaceutical Research and Development, Abbott Laboratories, Abbott Park, Illinois
  • ,
  • Quinn H. Hogan

      Affiliations

    • Department of Anesthesiology, Medical College of Wisconsin, Milwaukee, Wisconsin
  • ,
  • Cheryl L. Stucky

      Affiliations

    • Department of Cell Biology, Neurobiology, and Anatomy, Medical College of Wisconsin, Milwaukee, Wisconsin
    • Corresponding Author InformationAddress reprint requests to Dr Cheryl L. Stucky, Department of Cell Biology, Neurobiology, and Anatomy, Medical College of Wisconsin, 8701 Watertown Plank Road, Milwaukee, WI 53226-0509.

Received 8 January 2009 ,Revised 23 September 2009 ,Accepted 29 September 2009.

References 

  1. Albers KM, Woodbury CJ, Ritter AM, Davis BM, Koerber HR. Glial cell-line-derived neurotrophic factor expression in skin alters the mechanical sensitivity of cutaneous nociceptors. J Neurosci. 2006;26:2981–2990
  2. Amaya F, Shimosato G, Nagano M, Ueda M, Hashimoto S, Tanaka Y, et al. NGF and GDNF differentially regulate TRPV1 expression that contributes to development of inflammatory thermal hyperalgesia. Eur J Neurosci. 2004;20:2303–2310
  3. Bennett DL, Michael GJ, Ramachandran N, Munson JB, Averill S, Yan Q, et al. A distinct subgroup of small DRG cells express GDNF receptor components and GDNF is protective for these neurons after nerve injury. J Neurosci. 1998;18:3059–3072
  4. Bernardini N, Neuhuber W, Reeh PW, Sauer SK. Morphological evidence for functional capsaicin receptor expression and calcitonin gene-related peptide exocytosis in isolated peripheral nerve axons of the mouse. Neuroscience. 2004;126:585–590
  5. Braz JM, Nassar MA, Wood JN, Basbaum AI. Parallel “pain” pathways arise from subpopulations of primary afferent nociceptor. Neuron. 2005;47:787–793
  6. Breese NM, George AC, Pauers LE, Stucky CL. Peripheral inflammation selectively increases TRPV1 function in IB4-positive sensory neurons from adult mouse. Pain. 2005;115:37–49
  7. Campbell JN, Meyer RA. Mechanisms of neuropathic pain. Neuron. 2006;52:77–92
  8. 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
  9. 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
  10. Caterina MJ, Rosen TA, Tominaga M, Brake AJ, Julius D. A capsaicin-receptor homologue with a high threshold for noxious heat. Nature. 1999;398:436–441
  11. Cheng W, Yang F, Takanishi CL, Zheng J. Thermosensitive TRPV channel subunits coassemble into heteromeric channels with intermediate conductance and gating properties. J Gen Physiol. 2007;129:191–207
  12. 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
  13. Dirajlal S, Pauers LE, Stucky CL. Differential response properties of IB(4)-positive and -negative unmyelinated sensory neurons to protons and capsaicin. J Neurophysiol. 2003;89:513–524
  14. Dittert I, Benedikt J, Vyklicky L, Zimmermann K, Reeh PW, Vlachova V. Improved superfusion technique for rapid cooling or heating of cultured cells under patch-clamp conditions. J Neurosci Methods. 2006;151:178–185
  15. Djouhri L, Koutsikou S, Fang X, McMullan S, Lawson SN. Spontaneous pain, both neuropathic and inflammatory, is related to frequency of spontaneous firing in intact C-fiber nociceptors. J Neurosci. 2006;26:1281–1292
  16. El Kouhen R, Surowy CS, Bianchi BR, Neelands TR, McDonald HA, Niforatos W, et al. A-425619 [1-isoquinolin-5-yl-3-(4-trifluoromethyl-benzyl)-urea], a novel and selective transient receptor potential type V1 receptor antagonist, blocks channel activation by vanilloids, heat, and acid. J Pharmacol Exp Ther. 2005;314:400–409
  17. Fang X, McMullan S, Lawson SN, Djouhri L. Electrophysiological differences between nociceptive and non-nociceptive dorsal root ganglion neurones in the rat in vivo. J Physiol. 2005;565:927–943
  18. Fukuoka T, Tokunaga A, Tachibana T, Dai Y, Yamanaka H, Noguchi K. VR1, but not P2X(3), increases in the spared L4 DRG in rats with L5 spinal nerve ligation. Pain. 2002;99:111–120
  19. Guler AD, Lee H, Iida T, Shimizu I, Tominaga M, Caterina M. Heat-evoked activation of the ion channel, TRPV4. J Neurosci. 2002;22:6408–6414
  20. Hammarberg H, Piehl F, Cullheim S, Fjell J, Hokfelt T, Fried K. GDNF mRNA in Schwann cells and DRG satellite cells after chronic sciatic nerve injury. Neuroreport. 1996;7:857–860
  21. Hammond DL, Ackerman L, Holdsworth R, Elzey B. Effects of spinal nerve ligation on immunohistochemically identified neurons in the L4 and L5 dorsal root ganglia of the rat. J Comp Neurol. 2004;475:575–589
  22. Hargreaves K, Dubner R, Brown F, Flores C, Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain. 1988;32:77–88
  23. Hellwig N, Albrecht N, Harteneck C, Schultz G, Schaefer M. Homo- and heteromeric assembly of TRPV channel subunits. J Cell Sci. 2005;118:917–928
  24. Honore P, Wismer CT, Mikusa J, Zhu CZ, Zhong C, Gauvin DM, et al. A-425619 [1-isoquinolin-5-yl-3-(4-trifluoromethyl-benzyl)-urea], a novel transient receptor potential type V1 receptor antagonist, relieves pathophysiological pain associated with inflammation and tissue injury in rats. J Pharmacol Exp Ther. 2005;314:410–421
  25. Hudson LJ, Bevan S, Wotherspoon G, Gentry C, Fox A, Winter J. VR1 protein expression increases in undamaged DRG neurons after partial nerve injury. Eur J Neurosci. 2001;13:2105–2114
  26. Hwang SW, Cho H, Kwak J, Lee SY, Kang CJ, Jung J, et al. Direct activation of capsaicin receptors by products of lipoxygenases: Endogenous capsaicin-like substances. Proc Natl Acad Sci USA. 2000;97:6155–6160
  27. Kim SH, Chung JM. An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain. 1992;50:355–363
  28. Koerber HR, Druzinsky RE, Mendell LM. Properties of somata of spinal dorsal root ganglion cells differ according to peripheral receptor innervated. J Neurophysiol. 1988;60:1584–1596
  29. LaMotte RH. Acutely dissociated sensory neurons: normal or neuropathic? Focus on: “Dissociation of dorsal root ganglion neurons induces hyperexcitability that is maintained by increased responsiveness to cAMP and cGMP.”. J Neurophysiol. 2007;97:1–2
  30. 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
  31. Lee H, Caterina MJ. TRPV channels as thermosensory receptors in epithelial cells. Pflugers Arch. 2005;451:160–167
  32. Li L, Zhou XF. Pericellular Griffonia simplicifolia I isolectin B4-binding ring structures in the dorsal root ganglia following peripheral nerve injury in rats. J Comp Neurol. 2001;439:259–274
  33. Liedtke W, Choe Y, Marti-Renom MA, Bell AM, Denis CS, Sali A, et al. Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell. 2000;103:525–535
  34. Liu CN, Wall PD, Ben-Dor E, Michaelis M, Amir R, Devor M. Tactile allodynia in the absence of C-fiber activation: Altered firing properties of DRG neurons following spinal nerve injury. Pain. 2000;85:503–521
  35. Lu J, Zhou XF, Rush RA. Small primary sensory neurons innervating epidermis and viscera display differential phenotype in the adult rat. Neurosci Res. 2001;41:355–363
  36. Lyfenko A, Vlachova V, Vyklicky L, Dittert I, Kress M, Reeh PW. The effects of excessive heat on heat-activated membrane currents in cultured dorsal root ganglia neurons from neonatal rat. Pain. 2002;95:207–214
  37. Ma C, Shu Y, Zheng Z, Chen Y, Yao H, Greenquist KW, et al. Similar electrophysiological changes in axotomized and neighboring intact dorsal root ganglion neurons. J Neurophysiol. 2003;89:1588–1602
  38. Macrae WA. Chronic post-surgical pain: 10 years on. Br J Anaesth. 2008;101:77–86
  39. Macrae WA. Chronic pain after surgery. Br J Anaesth. 2001;87:88–98
  40. Mandadi S, Sokabe T, Shibasaki K, Katanosaka K, Mizuno A, Moqrich A, et al. TRPV3 in keratinocytes transmits temperature information to sensory neurons via ATP. Pflugers Arch. 2009;458:1093–1102
  41. Michael GJ, Priestley JV. Differential expression of the mRNA for the vanilloid receptor subtype 1 in cells of the adult rat dorsal root and nodose ganglia and its downregulation by axotomy. J Neurosci. 1999;19:1844–1854
  42. Moalem G, Tracey DJ. Immune and inflammatory mechanisms in neuropathic pain. Brain Res Rev. 2006;51:240–264
  43. Molliver DC, Wright DE, Leitner ML, Parsadanian AS, Doster K, Wen D, et al. IB4-binding DRG neurons switch from NGF to GDNF dependence in early postnatal life. Neuron. 1997;19:849–861
  44. Nakatsuka T, Furue H, Yoshimura M, Gu JG. Activation of central terminal vanilloid receptor-1 receptors and alpha beta-methylene-ATP-sensitive P2X receptors reveals a converged synaptic activity onto the deep dorsal horn neurons of the spinal cord. J Neurosci. 2002;22:1228–1237
  45. Naveilhan P, ElShamy WM, Ernfors P. Differential regulation of mRNAs for GDNF and its receptors Ret and GDNFR alpha after sciatic nerve lesion in the mouse. Eur J Neurosci. 1997;9:1450–1460
  46. Nicol GD, Cui M. Enhancement by prostaglandin E2 of bradykinin activation of embryonic rat sensory neurones. J Physiol. 1994;480:485–492
  47. Peier AM, Reeve AJ, Andersson DA, Moqrich A, Earley TJ, Hergarden AC, et al. A heat-sensitive TRP channel expressed in keratinocytes. Science. 2002;296:2046–2049
  48. Pomonis JD, Harrison JE, Mark L, Bristol DR, Valenzano KJ, Walker K. N-(4-Tertiarybutylphenyl)-4-(3-cholorphyridin-2-yl)tetrahydropyrazine -1(2H)-carbox-amide (BCTC), a novel, orally effective vanilloid receptor 1 antagonist with analgesic properties, II: In vivo characterization in rat models of inflammatory and neuropathic pain. J Pharmacol Exp Ther. 2003;306:387–393
  49. Rashid MH, Inoue M, Kondo S, Kawashima T, Bakoshi S, Ueda H. Novel expression of vanilloid receptor 1 on capsaicin-insensitive fibers accounts for the analgesic effect of capsaicin cream in neuropathic pain. J Pharmacol Exp Ther. 2003;304:940–948
  50. Rigaud M, Gemes G, Barabas ME, Chernoff DI, Abram SE, Stucky CL, et al. Species and strain differences in rodent sciatic nerve anatomy: Implications for studies of neuropathic pain. Pain. 2008;136:188–201
  51. Ritter AM, Mendell LM. Somal membrane properties of physiologically identified sensory neurons in the rat: Effects of nerve growth factor. J Neurophysiol. 1992;68:2033–2041
  52. Sikand P, Premkumar LS. Potentiation of glutamatergic synaptic transmission by protein kinase C-mediated sensitization of TRPV1 at the first sensory synapse. J Physiol. 2007;581:631–647
  53. Smith GD, Gunthorpe MJ, Kelsell RE, Hayes PD, Reilly P, Facer P, et al. TRPV3 is a temperature-sensitive vanilloid receptor-like protein. Nature. 2002;418:186–190
  54. Stucky CL, Lewin GR. Isolectin B(4)-positive and -negative nociceptors are functionally distinct. J Neurosci. 1999;19:6497–6505
  55. Sugiura S, Lahav R, Han J, Kou SY, Banner LR, de Pablo F, et al. Leukaemia inhibitory factor is required for normal inflammatory responses to injury in the peripheral and central nervous systems in vivo and is chemotactic for macrophages in vitro. Eur J Neurosci. 2000;12:457–466
  56. Sugiura T, Tominaga M, Katsuya H, Mizumura K. Bradykinin lowers the threshold temperature for heat activation of vanilloid receptor 1. J Neurophysiol. 2002;88:544–548
  57. Sukhotinsky I, Ben-Dor E, Raber P, Devor M. Key role of the dorsal root ganglion in neuropathic tactile hypersensibility. Eur J Pain. 2004;8:135–143
  58. Swett JE, Torigoe Y, Elie VR, Bourassa CM, Miller PG. Sensory neurons of the rat sciatic nerve. Exp Neurol. 1991;114:82–103
  59. 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
  60. Vulchanova L, Olson TH, Stone LS, Riedl MS, Elde R, Honda CN. Cytotoxic targeting of isolectin IB4-binding sensory neurons. Neuroscience. 2001;108:143–155
  61. Koltzenburg M, McMahon S. Wall and Melzack's Textbook of Pain. 5th ed.. Philadelphia, PA: Elsevier; 2006;pp 905-927
  62. Wang C, Hu HZ, Colton CK, Wood JD, Zhu MX. An alternative splicing product of the murine trpv1 gene dominant negatively modulates the activity of TRPV1 channels. J Biol Chem. 2004;279:37423–37430
  63. 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
  64. Wu G, Ringkamp M, Hartke TV, Murinson BB, Campbell JN, Griffin JW, et al. Early onset of spontaneous activity in uninjured C-fiber nociceptors after injury to neighboring nerve fibers. J Neurosci. 2001;21:RC140
  65. Zheng JH, Walters ET, Song XJ. Dissociation of dorsal root ganglion neurons induces hyperexcitability that is maintained by increased responsiveness to cAMP and cGMP. J Neurophysiol. 2007;97:15–25
  66. Zimmermann K, Leffler A, Fischer MM, Messlinger K, Nau C, Reeh PW. The TRPV1/2/3 activator 2-aminoethoxydiphenyl borate sensitizes native nociceptive neurons to heat in wildtype but not TRPV1 deficient mice. Neuroscience. 2005;135:1277–1284
  67. Zwick M, Davis BM, Woodbury CJ, Burkett JN, Koerber HR, Simpson JF, et al. Glial cell line-derived neurotrophic factor is a survival factor for isolectin B4-positive, but not vanilloid receptor 1-positive, neurons in the mouse. J Neurosci. 2002;22:4057–4065
  68. Zygmunt PM, Petersson J, Andersson DA, Chuang H, Sorgard M, Di Marzo V, et al. Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature. 1999;400:452–457
  69. Zylka MJ, Rice FL, Anderson DJ. Topographically distinct epidermal nociceptive circuits revealed by axonal tracers targeted to Mrgprd. Neuron. 2005;45:17–25

 Supported by NIH grant NS40538 (to C.L.S.).

PII: S1526-5900(09)00773-1

doi: 10.1016/j.jpain.2009.09.018

The Journal of Pain
Volume 11, Issue 6 , Pages 588-599 , June 2010