PAIN
Volume 109, Issue 3 , Pages 471-480 , June 2004

Absence of an association between axotomy-induced changes in sodium currents and excitability in DRG neurons from the adult rat

  • Natasha M. Flake

      Affiliations

    • Department of Biomedical Sciences, Dental School, University of Maryland at Baltimore, Baltimore, MD 21201, USA
  • ,
  • Eric Lancaster

      Affiliations

    • Program in Neuroscience, University of Maryland at Baltimore, Baltimore, MD 21201, USA
  • ,
  • Daniel Weinreich

      Affiliations

    • Program in Neuroscience, University of Maryland at Baltimore, Baltimore, MD 21201, USA
    • Department of Pharmacology and Experimental Therapeutics, University of Maryland at Baltimore, Baltimore, MD 21201, USA
  • ,
  • Michael S Gold

      Affiliations

    • Department of Biomedical Sciences, Dental School, University of Maryland at Baltimore, Baltimore, MD 21201, USA
    • Program in Neuroscience, University of Maryland at Baltimore, Baltimore, MD 21201, USA
    • Department of Anatomy and Neurobiology, Medical School, University of Maryland at Baltimore, Baltimore, MD 21201, USA
    • Corresponding Author InformationCorresponding author. Address: Dental School, University of Maryland, 666 W. Baltimore St., Room 5-A-12 HHH, Baltimore, MD 21201, USA. Tel.: +1-410-706-0909; fax: +1-410-706-4172

Received 12 August 2003 ,Revised 4 February 2004 ,Accepted 23 February 2004.

References 

  1. Abdulla FA, Smith PA. Axotomy- and autotomy-induced changes in Ca2+ and K+ channel currents of rat dorsal root ganglion neurons. J Neurophysiol. 2001;85:644–658
  2. Abdulla FA, Smith PA. Axotomy- and autotomy-induced changes in the excitability of rat dorsal root ganglion neurons. J Neurophysiol. 2001;85:630–643
  3. Abdulla FA, Smith PA. Changes in Na(+) channel currents of rat dorsal root ganglion neurons following axotomy and axotomy-induced autotomy. J Neurophysiol. 2002;88:2518–2529
  4. Akopian AN, Souslova V, England S, Okuse K, Ogata N, Ure J, et al. The tetrodotoxin-resistant sodium channel SNS has a specialized function in pain pathways. Nat Neurosci. 1999;2:541–548
  5. Baccei ML, Kocsis JD. Voltage-gated calcium currents in axotomized adult rat cutaneous afferent neurons. J Neurophysiol. 2000;83:2227–2238
  6. Benson CJ, Eckert SP, McCleskey EW. Acid-evoked currents in cardiac sensory neurons: a possible mediator of myocardial ischemic sensation. Circ Res. 1999;84:921–928
  7. Black JA, Cummins TR, Plumpton C, Chen YH, Hormuzdiar W, Clare JJ, et al. Upregulation of a silent sodium channel after peripheral, but not central, nerve injury in DRG neurons. J Neurophysiol. 1999;82:2776–2785
  8. Boucher TJ, Okuse K, Bennett DL, Munson JB, Wood JN, McMahon SB. Potent analgesic effects of GDNF in neuropathic pain states. Science. 2000;290:124–127
  9. Cummins TR, Waxman SG. Downregulation of tetrodotoxin-resistant sodium currents and upregulation of a rapidly repriming tetrodotoxin-sensitive sodium current in small spinal sensory neurons after nerve injury. J Neurosci. 1997;17:3503–3514
  10. Decosterd I, Ji RR, Abdi S, Tate S, Woolf CJ. The pattern of expression of the voltage-gated sodium channels Na(v)1.8 and Na(v)1.9 does not change in uninjured primary sensory neurons in experimental neuropathic pain models. Pain. 2002;96:269–277
  11. Devor M. Neuropathic pain: what do we do with all these theories?. Acta Anaesthesiol Scand. 2001;45:1121–1127
  12. Devor M, Seltzer Z. Pathophysiology of damaged nerves in relation to chronic pain. In:  Wall PD,  Melzack R editor. Textbook of pain. London: Harcourt; 1999;
  13. Dib-Hajj S, Black JA, Felts P, Waxman SG. Down-regulation of transcripts for Na channel alpha-SNS in spinal sensory neurons following axotomy. Proc Natl Acad Sci USA. 1996;93:14950–14954
  14. Dib-Hajj SD, Black JA, Cummins TR, Kenney AM, Kocsis JD, Waxman SG. Rescue of alpha-SNS sodium channel expression in small dorsal root ganglion neurons after axotomy by nerve growth factor in vivo [in process citation]. J Neurophysiol. 1998;79:2668–2676
  15. Dib-Hajj SD, Fjell J, Cummins TR, Zheng Z, Fried K, LaMotte R, et al. Plasticity of sodium channel expression in DRG neurons in the chronic constriction injury model of neuropathic pain. Pain. 1999;83:591–600
  16. Eriksson J, Fried K. Expression of the sodium channel transcripts Na(v)1.8 and Na(v)1.9 in injured dorsal root ganglion neurons of interferon-gamma or interferon-gamma receptor deficient mice. Neurosci Lett. 2003;338:242–246
  17. Everill B, Kocsis JD. Nerve injury reduces total potassium conductance of two of three identified currents in adult cutaneous afferent dorsal root ganglion neurons. Soc Neurosci Abs. 1997;23:1745
  18. Everill B, Cummins TR, Waxman SG, Kocsis JD. Sodium currents of large (Abeta-type) adult cutaneous afferent dorsal root ganglion neurons display rapid recovery from inactivation before and after axotomy. Neuroscience. 2001;106:161–169
  19. Fukuoka T, Noguchi K. Contribution of the spared primary afferent neurons to the pathomechanisms of neuropathic pain. Mol Neurobiol. 2002;26:57–67
  20. Gold MS, Dastmalchi S, Levine JD. Co-expression of nociceptor properties in dorsal root ganglion neurons from the adult rat in vitro. Neuroscience. 1996;71:265–275
  21. Gold MS, Reichling DB, Shuster MJ, Levine JD. Hyperalgesic agents increase a tetrodotoxin-resistant Na+ current in nociceptors. Proc Natl Acad Sci USA. 1996;93:1108–1112
  22. Gold MS, Zhang L, Wrigley DL, Traub RJ. Prostaglandin E(2) modulates TTX-R I(Na) in rat colonic sensory neurons. J Neurophysiol. 2002;88:1512–1522
  23. Gold MS, Weinreich D, Kim CS, Wang R, Treanor J, Porreca F, et al. Redistribution of Na(V)1.8 in uninjured axons enables neuropathic pain. J Neurosci. 2003;23:158–166
  24. Ishikawa K, Tanaka M, Black JA, Waxman SG. Changes in expression of voltage-gated potassium channels in dorsal root ganglion neurons following axotomy. Muscle Nerve. 1999;22:502–507
  25. Kim CH, Oh Y, Chung JM, Chung K. The changes in expression of three subtypes of TTX sensitive sodium channels in sensory neurons after spinal nerve ligation. Brain Res Mol Brain Res. 2001;95:153–161
  26. Kim CH, Oh Y, Chung JM, Chung K. Changes in three subtypes of tetrodotoxin sensitive sodium channel expression in the axotomized dorsal root ganglion in the rat. Neurosci Lett. 2002;323:125–128
  27. Lai J, Gold MS, Kim CS, Biana D, Ossipov MH, Hunter JC, et al. Inhibition of neuropathic pain by decreased expression of the tetrodotoxin-resistant sodium channel, NaV1.8. Pain. 2002;95:143–152
  28. Lancaster E, Weinreich D. Sodium currents in vagotomized primary afferent neurones of the rat. J Physiol. 2001;536:445–458
  29. Lancaster E, Oh EJ, Weinreich D. Vagotomy decreases excitability in primary vagal afferent somata. J Neurophysiol. 2001;85:247–253
  30. Lancaster E, Oh EJ, Gover T, Weinreich D. Calcium and calcium-activated currents in vagotomized rat primary vagal afferent neurons. J Physiol. 2002;540:543–556
  31. Leffler A, Cummins TR, Dib-Hajj SD, Hormuzdiar WN, Black JA, Waxman SG. GDNF and NGF reverse changes in repriming of TTX-sensitive Na(+) currents following axotomy of dorsal root ganglion neurons. J Neurophysiol. 2002;88:650–658
  32. Novakovic SD, Tzoumaka E, McGivern JG, Haraguchi M, Sangameswaran L, Gogas KR, et al. Distribution of the tetrodotoxin-resistant sodium channel PN3 in rat sensory neurons in normal and neuropathic conditions. J Neurosci. 1998;18:2174–2187
  33. Okuse K, Chaplan SR, McMahon SB, Luo ZD, Calcutt NA, Scott BP, et al. Regulation of expression of the sensory neuron-specific sodium channel SNS in inflammatory and neuropathic pain. Mol Cell Neurosci. 1997;10:196–207
  34. Rizzo MA, Kocsis JD, Waxman SG. Selective loss of slow and enhancement of fast Na+ currents in cutaneous afferent dorsal root ganglion neurones following axotomy. Neurobiol Dis. 1995;2:87–96
  35. Rush AM, Brau ME, Elliott AA, Elliott JR. Electrophysiological properties of sodium current subtypes in small cells from adult rat dorsal root ganglia. J Physiol (Lond). 1998;511:771–789
  36. Waxman SG, Cummins TR, Black JA, Dib-Hajj S. Diverse functions and dynamic expression of neuronal sodium channels. Novartis Found Symp. 2002;241:34–51 discussion 51–60
  37. 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
  38. Xiao HS, Huang QH, Zhang FX, Bao L, Lu YJ, Guo C, et al. Identification of gene expression profile of dorsal root ganglion in the rat peripheral axotomy model of neuropathic pain. Proc Natl Acad Sci USA. 2002;99:8360–8365
  39. Zhang JM, Donnelly DF, Song XJ, Lamotte RH. Axotomy increases the excitability of dorsal root ganglion cells with unmyelinated axons. J Neurophysiol. 1997;78:2790–2794

PII: S0304-3959(04)00116-2

doi: 10.1016/j.pain.2004.02.024

PAIN
Volume 109, Issue 3 , Pages 471-480 , June 2004