The Journal of Pain
Volume 8, Issue 8 , Pages 637-649 , August 2007

Diabetes-Induced Chemogenic Hypoalgesia Is Paralleled by Attenuated Stimulus-Induced Fos Expression in the Spinal Cord of Diabetic Mice

Received 11 November 2006 ,Revised 22 February 2007 ,Accepted 6 April 2007.

References 

  1. Abbadie C, Lombard MC, Morain F, Besson J-M. Fos-like immunoreactivity in the rat superficial dorsal horn induced by formalin injection in the forepaw: Effects of dorsal rhizotomies. Brain Res. 1992;578:17–25
  2. Abbadie C, Taylor BK, Peterson MA, Basbaum AI. Differential contribution of the two phases of the formalin test to the pattern of c-fos expression in the rat spinal cord: Studies with remifentanil and lidocaine. Pain. 1997;69:101–110
  3. Akkina SK, Patterson CL, Wright DE. GDNF rescues nonpeptidergic unmyelinated primary afferents in streptozotocin-treated diabetic mice. Exp Neurol. 2001;167:173–182
  4. Bon K, Wilson SG, Mogil JS, Roberts WJ. Genetic evidence for the correlation of deep dorsal horn Fos protein immunoreactivity with tonic formalin pain behavior. J Pain. 2002;3:181–189
  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. Calcutt NA. Experimental models of painful diabetic neuropathy. J Neurosurg Sci. 2004;220:137–139
  7. Calcutt NA, Jorge MC, Yaksh TL, Chaplan SR. Tactile allodynia and formalin hyperalgesia in streptozotocin-diabetic rats: Effects of insulin, aldose reductase inhibition and lidocaine. Pain. 1996;68:293–299
  8. Calcutt NA, Stiller C, Gustafsson H, Malmberg AB. Elevated substance-P-like immunoreactivity levels in spinal dialysates during the formalin test in normal and diabetic rats. Brain Res. 2000;856:20–27
  9. Cesena RM, Calcutt NA. Gabapentin prevents hyperalgesia during the formalin test in diabetic rats. Neurosci Lett. 1999;262:101–104
  10. Chen SR, Pan HL. Hypersensitivity of spinothalamic tract neurons associated with diabetic neuropathic pain in rats. J Neurophysiol. 2002;87:2726–2733
  11. Chen YS, Chung SS, Chung SK. Noninvasive monitoring of diabetes-induced cutaneous nerve fiber loss and hypoalgesia in thy1-YFP transgenic mice. Diabetes. 2005;54(11):3112–3118
  12. Christianson JA, Riekhof JT, Wright DE. Restorative effects of neurotrophin treatment on diabetes-induced cutaneous axon loss in mice. Exp Neurol. 2003;179:188–189
  13. Christianson JA, Ryals JM, McCarson KE, Wright DE. Beneficial actions of neurotrophin treatment on diabetes-induced hypoalgesia in mice. J Pain. 2003;4:493–504
  14. Ciruela A, Dixon AK, Bramwell S, Gonzalez MI, Pinnock RD, Lee K. Identification of MEK1 as a novel target for the treatment of neuropathic pain. Br J Pharmacol. 2003;138:751–756
  15. Dualhac L, Mallet C, Courteix C, Etienne M, Duroux E, Privat AM, et al. Diabetes-induced mechanical hyperalgesia involves spinal MAPKs activation in neurons and microglia via NMDA-dependent mechanisms. Mol Pharmacol. 2006;70:1246–1254
  16. Freshwater JD, Svensson CI, Malmberg AB, Calcutt NA. Elevated spinal cyclooxygenase and prostaglandin release during hyperalgesia in diabetic rats. Diabetes. 2002;51:2249–2255
  17. Genuth S. Insights from the diabetes control and complications trial/epidemiology of diabetes interventions and complications study on the use of intensive glycemic treatment to reduce the risk of complications of type 1 diabetes. Endocrine Practice. 2006;12:34-31
  18. Hermann DN, Griffen JW, Hauer P, Cornblath DR, McArthur JC. Epidermal nerve fiber density and sural nerve morphometry in peripheral neuropathies. Neurology. 1999;53:1634–1640
  19. Hirai A, Yasuda H, Joko M, Maeda T, Kikkawa R. Evaluation of diabetic neuropathy through the quantitation of cutaneous nerves. J Neurol Sci. 2000;172:55–62
  20. Hunt SP, Pini A, Evan G. Induction of c-fos-like protein in spinal cord neurons following sensory stimulation. Nature. 1987;328:632–634
  21. Hylden JL, Wilcox GL. Intrathecal morphine in mice: A new technique. Eur J Pharmacol. 1980;67:313–316
  22. Jaffey PB, Gelman BB. Increased vulnerability to demyelination in streptozotocin diabetic rats. J Comp Neurol. 1996;373:55–61
  23. Kamei J, Ohhashi Y, Aoki T, Kasuya Y. Streptozotocin-induced diabetes in mice reduces the nociceptive threshold, as recognized after application of noxious mechanical stimuli but not of thermal stimuli. Pharmacol Biochem Behav. 1991;39:541–544
  24. Kamei J, Hitosugi H, Kasuya Y. Formalin-induced nociceptive responses in diabetic mice. Neurosci Lett. 1993;149:161–164
  25. Kamei J, Zushida K, Morita K, Sasaki M, Tanaka S. Role of vanilloid VR1 receptor in thermal allodynia and hyperalgesia in diabetic mice. Eur J Pharmacol. 2001;422:83–86
  26. Kennedy WR, Wendelschafer-Crabb G, Johnson T. Quantitation of epidermal nerves in diabetic neuropathy. Neurology. 1996;47:1042–1048
  27. Kennedy JM, Zochodne DW. The regenerative deficit of peripheral nerves in experimental diabetes: Its extent, timing and possible mechanisms. 2000;123:2118–2129
  28. Konrad RJ, Mikolaenko I, Tolar JF, Liu K, Kudlow JE. The potential mechanism of the diabetogenic action of streptozotocin: inhibition of pancreatic beta-cell O-GlcNAc-selective N-acetyl-beta-D-glucosaminidase. Biochem J. 2001;356:31–41
  29. Lauria G, Lombardi R, Borgna M, Penza P, Bianchi R, Savino C, et al. Intraepidermal nerve fiber density in rat foot pad: Neuropathologic-neurophysiologic correlation. J Peripher Nerv Syst. 2005;10:202–208
  30. Leinninger GM, Feldman EL. Insulin-like growth factors in the treatment of neurological disease. Endocr Dev. 2005;9:135–159
  31. Leinninger GM, Vincent AM, Feldman EL. The role of growth factors in diabetic peripheral neuropathy. J Peripher Nerv Syst. 2004;9:26–53
  32. Low PA, Dotson RM. Symptomatic treatment of painful neuropathy. JAMA. 1998;280:1863–1864
  33. McCall WD, Tanner KD, Levine JD. Formalin induces biphasic activity in C-fibers in the rat. Neurosci Lett. 1996;208:45–48
  34. McCarthy BG, Hsieh ST, Stocks A, Hauer P, Macko C, Cornblath DR, et al. Cutaneous innervation in sensory neuropathies: Evaluation by skin biopsy. Neurology. 1995;45:1848–1855
  35. Morgado C, Tavares IF. Baseline c-fos expression in the spinal dorsal horn neurons of streptozotocin diabetic rats. Soc Neurosci Abst. 2006;43:10
  36. Murray CW, Porreca F, Cowan A. Methodological refinements to the mouse paw formalin test: An animal model of tonic pain. J Pharmacol Methods. 1988;20:175–186
  37. Pertovaara A, Wei H, Kalmari J, Ruotsalainen M. Pain behavior and response properties of spinal dorsal horn neurons following experimental diabetic neuropathy in the rat: Modulation by nitecapone, a COMT inhibitor with antioxidant properties. Exp Neurol. 2001;167:425–434
  38. Polydefkis M, Hauer P, Sheth S, Sirdofsky M, Griffin JW, McArthur JC. The time course of epidermal nerve fiber regeneration: Studies in normal controls and in people with diabetes, with and without neuropathy. Brain. 2004;127:1606–1615
  39. Presley RW, Menetrey D, Levine JD, Basbaum AI. Systemic morphine suppresses noxious stimulus-evoked Fos protein-like immunoreactivity in the rat spinal cord. J Neurosci. 1990;10:323–333
  40. Puig S, Sorkin LS. Formalin-evoked activity in identified primary afferent fibers: Systemic lidocaine suppresses phase-2 activity. Pain. 1996;64:345–355
  41. Purves TD, Tomlinson DR. Diminished transcription factor survival signals in dorsal root ganglia in rats with streptozotocin-induced diabetes. Ann N Y Acad Sci. 2002;973:472–476
  42. Quattrini C, Tesfaye S. Understanding the impact of painful diabetic neuropathy. Diabetes Metab Res Rev. 2003;19(Suppl 1):S2–S8
  43. Schmader K. Epidemiology and impact on quality of life of postherpetic neuralgia and painful diabetic neuropathy. Clin J Pain. 2002;18:350–354
  44. Sinnreich M, Taylor BV, Dyck PJB. Diabetic neuropathies: Classification, clinical features, and pathophysiological basis. Neurologist. 2005;11:63–79
  45. Sorensen L, Molyneaux L, Yue DK. Insensate vs. painful diabetic neuropathy: The effects of height, gender, ethnicity and glycaemic control. Diabetes Res Clin Pract. 2002;57:45–51
  46. Takeshita N, Yamaguchi I. Insulin attenuates formalin-induced nociceptive response in mice through a mechanism that is deranged by diabetes mellitus. J Pharmacol Exp Ther. 1997;281:315–321
  47. Thomas PK. Diabetic neuropathy: Mechanisms and future treatment options. J Neurol Neurosurg Psychiatry. 1999;67:277–281
  48. Tomiyama M, Furusawa K, Kamijo M, Kimura T, Matsunaga M, Baba M. Upregulation of mRNAs coding for AMPA and NMDA receptor subunits and metabotropic glutamate receptors in the dorsal horn of the spinal cord in a rat model of diabetes mellitus. Brain Res Mol Brain Res. 2005;136:275–281
  49. Walwyn WM, Matsuka Y, Arai D, Bloom DC, Lam H, Tran C, et al. HSV-1 mediated NGF delivery delays nociceptive deficits in a genetic model of diabetic neuropathy. Exp Neurol. 2006;198:260–270
  50. Wang ZC, Dohle JF, Friemann J, Green BS. Prevention of high- and low-dose STZ-induced diabetes with d-glucose and 5-thio-d-glucose. Diabetes. 1993;42:420–428
  51. Wright DE, Ryals JM, Johnson MS, Smittkamp SE. Discrete neuropathic symptoms in the peripheral nervous system of a Type 2 model of diabetes: db/db mice. Soc. Neurosci Abstract. 2006;443:13
  52. Zochodne DW. Neurotrophins and other growth factors in diabetic neuropathy. Semin Neurol. 1996;16:153–161

 Supported by NIH grant R01NS43314 (D.E.W.).

PII: S1526-5900(07)00643-8

doi: 10.1016/j.jpain.2007.04.004

The Journal of Pain
Volume 8, Issue 8 , Pages 637-649 , August 2007