Activated Microglia Contribute to Convergent Nociceptive Inputs to Spinal Dorsal Horn Neurons and the Development of Neuropathic Pain

Neurochemical Research

Volumn 40, Issue 5, 2015, Pages 1000-1012

  Yamamoto, Yuya ^a   Terayama, Ryuji ^a,b   Kishimoto, Noriko ^a   Maruhama, Kotaro ^a,b   Mizutani, Masahide ^a,b   Iida, Seiji ^a,b   Sugimoto, Tomosada ^a,b  

^a OKAYAMA UNIVERSITY   (Japan)

^b OKAYAMA UNIVERSITY   (Japan)

Author keywords

c Fos; ERK; Microglia; Minocycline; Nerve injury; Spinal dorsal horn

Indexed keywords

ANIMAL; INJURIES; MALE; METABOLISM; MICROGLIA; NEURALGIA; PAIN MEASUREMENT; POSTERIOR HORN CELL; PROCEDURES; RAT; SPRAGUE DAWLEY RAT; TIBIAL NERVE;

ANIMALS; MALE; MICROGLIA; NEURALGIA; PAIN MEASUREMENT; POSTERIOR HORN CELLS; RATS; RATS, SPRAGUE-DAWLEY; TIBIAL NERVE;

EID: 84939942216     PISSN: 03643190     EISSN: 15736903     Source Type: Journal    
DOI: 10.1007/s11064-015-1555-8     Document Type: Article

References (55)

1. Zimmermann M (2001) Pathobiology of neuropathic pain. Eur J Pharmacol 429(1–3):23–37
2. Devor M, Wall PD (1978) Reorganisation of spinal cord sensory map after peripheral nerve injury. Nature 276(5683):75–76
3. Hylden JL, Nahin RL, Dubner R (1987) Altered responses of nociceptive cat lamina I spinal dorsal horn neurons after chronic sciatic neuroma formation. Brain Res 411(2):341–350
4. Lisney SJ (1983) Changes in the somatotopic organization of the cat lumbar spinal cord following peripheral nerve transection and regeneration. Brain Res 259(1):31–39
5. Markus H, Pomeranz B, Krushelnycky D (1984) Spread of saphenous somatotopic projection map in spinal cord and hypersensitivity of the foot after chronic sciatic denervation in adult rat. Brain Res 296(1):27–39
6. Sugimoto T, Ichikawa H, Hijiya H, Mitani S, Nakago T (1993) c-Fos expression by dorsal horn neurons chronically deafferented by peripheral nerve section in response to spared, somatotopically inappropriate nociceptive primary input. Brain Res 621(1):161–166
7. Nomura H, Ogawa A, Tashiro A, Morimoto T, Hu JW, Iwata K (2002) Induction of Fos protein-like immunoreactivity in the trigeminal spinal nucleus caudalis and upper cervical cord following noxious and non-noxious mechanical stimulation of the whisker pad of the rat with an inferior alveolar nerve transection. Pain 95(3):225–238
8. Fujisawa N, Terayama R, Yamaguchi D, Omura S, Yamashiro T, Sugimoto T (2012) Fos protein-like immunoreactive neurons induced by electrical stimulation in the trigeminal sensory nuclear complex of rats with chronically injured peripheral nerve. Exp Brain Res 219(2):191–201. doi:10.1007/s00221-012-3078-8
9. Terayama R, Kishimoto N, Yamamoto Y, Maruhama K, Tsuchiya H, Mizutani M, Iida S, Sugimoto T (2014) Convergent nociceptive input to spinal dorsal horn neurons after peripheral nerve injury. Neurochem Res. doi:10.1007/s11064-014-1484-y
10. Terayama R, Tsuchiya H, Omura S, Maruhama K, Mizutani M, Iida S, Sugimoto T (2014) Possible involvement of convergent nociceptive input to medullary dorsal horn neurons in intraoral hyperalgesia following peripheral nerve injury. Cell Mol Neurobiol. doi:10.1007/s10571-014-0137-7
11. Hains BC, Waxman SG (2006) Activated microglia contribute to the maintenance of chronic pain after spinal cord injury. J Neurosci 26(16):4308–4317
12. Tsuda M, Inoue K, Salter MW (2005) Neuropathic pain and spinal microglia: a big problem from molecules in “small” glia. Trends Neurosci 28(2):101–107. doi:10.1016/j.tins.2004.12.002
13. Tsuda M, Mizokoshi A, Shigemoto-Mogami Y, Koizumi S, Inoue K (2004) Activation of p38 mitogen-activated protein kinase in spinal hyperactive microglia contributes to pain hypersensitivity following peripheral nerve injury. Glia 45(1):89–95. doi:10.1002/glia.10308
14. Watkins LR, Milligan ED, Maier SF (2001) Glial activation: a driving force for pathological pain. Trends Neurosci 24(8):450–455
15. Watkins LR, Milligan ED, Maier SF (2001) Spinal cord glia: new players in pain. Pain 93(3):201–205
16. Terayama R, Omura S, Fujisawa N, Yamaai T, Ichikawa H, Sugimoto T (2008) Activation of microglia and p38 mitogen-activated protein kinase in the dorsal column nucleus contributes to tactile allodynia following peripheral nerve injury. Neuroscience 153(4):1245–1255. doi:10.1016/j.neuroscience.2008.03.041
17. Garrison CJ, Dougherty PM, Kajander KC, Carlton SM (1991) Staining of glial fibrillary acidic protein (GFAP) in lumbar spinal cord increases following a sciatic nerve constriction injury. Brain Res 565(1):1–7
18. Kalla R, Liu Z, Xu S, Koppius A, Imai Y, Kloss CU, Kohsaka S, Gschwendtner A, Moller JC, Werner A, Raivich G (2001) Microglia and the early phase of immune surveillance in the axotomized facial motor nucleus: impaired microglial activation and lymphocyte recruitment but no effect on neuronal survival or axonal regeneration in macrophage-colony stimulating factor-deficient mice. J Comp Neurol 436(2):182–201
19. Ledeboer A, Sloane EM, Milligan ED, Frank MG, Mahony JH, Maier SF, Watkins LR (2005) Minocycline attenuates mechanical allodynia and proinflammatory cytokine expression in rat models of pain facilitation. Pain 115(1–2):71–83. doi:10.1016/j.pain.2005.02.009
20. Raghavendra V, Tanga F, DeLeo JA (2003) Inhibition of microglial activation attenuates the development but not existing hypersensitivity in a rat model of neuropathy. J Pharmacol Exp Ther 306(2):624–630. doi:10.1124/jpet.103.052407
21. DeLeo JA, Yezierski RP (2001) The role of neuroinflammation and neuroimmune activation in persistent pain. Pain 90(1–2):1–6
22. Hanisch UK (2002) Microglia as a source and target of cytokines. Glia 40(2):140–155. doi:10.1002/glia.10161
23. Amin AR, Attur MG, Thakker GD, Patel PD, Vyas PR, Patel RN, Patel IR, Abramson SB (1996) A novel mechanism of action of tetracyclines: effects on nitric oxide synthases. Proc Natl Acad Sci USA 93(24):14014–14019
24. Tikka T, Fiebich BL, Goldsteins G, Keinanen R, Koistinaho J (2001) Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J Neurosci 21(8):2580–2588
25. Tikka TM, Koistinaho JE (2001) Minocycline provides neuroprotection against N-methyl-d-aspartate neurotoxicity by inhibiting microglia. J Immunol 166(12):7527–7533
26. Piao ZG, Cho IH, Park CK, Hong JP, Choi SY, Lee SJ, Lee S, Park K, Kim JS, Oh SB (2006) Activation of glia and microglial p38 MAPK in medullary dorsal horn contributes to tactile hypersensitivity following trigeminal sensory nerve injury. Pain 121(3):219–231. doi:10.1016/j.pain.2005.12.023
27. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL (1994) Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53(1):55–63
28. Dixon WJ (1980) Efficient analysis of experimental observations. Annu Rev Pharmacol Toxicol 20:441–462
29. Hargreaves K, Dubner R, Brown F, Flores C, Joris J (1988) A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32(1):77–88
30. Devor M, Govrin-Lippmann R (1983) Axoplasmic transport block reduces ectopic impulse generation in injured peripheral nerves. Pain 16(1):73–85
31. Hughes AS, Averill S, King VR, Molander C, Shortland PJ (2008) Neurochemical characterization of neuronal populations expressing protein kinase C gamma isoform in the spinal cord and gracile nucleus of the rat. Neuroscience 153(2):507–517. doi:10.1016/j.neuroscience.2008.01.082
32. Molander C, Hongpaisan J, Grant G (1992) Changing pattern of c-FOS expression in spinal cord neurons after electrical stimulation of the chronically injured sciatic nerve in the rat. Neuroscience 50(1):223–236
33. Shortland P, Molander C (1998) The time-course of abeta-evoked c-fos expression in neurons of the dorsal horn and gracile nucleus after peripheral nerve injury. Brain Res 810(1–2):288–293
34. Tokunaga A, Kondo E, Fukuoka T, Miki K, Dai Y, Tsujino H, Noguchi K (1999) Excitability of spinal cord and gracile nucleus neurons in rats with chronically injured sciatic nerve examined by c-fos expression. Brain Res 847(2):321–331
35. Swett JE, Woolf CJ (1985) The somatotopic organization of primary afferent terminals in the superficial laminae of the dorsal horn of the rat spinal cord. J Comp Neurol 231(1):66–77. doi:10.1002/cne.902310106
36. Terayama R, Fujisawa N, Yamaguchi D, Omura S, Ichikawa H, Sugimoto T (2011) Differential activation of mitogen-activated protein kinases and glial cells in the trigeminal sensory nuclear complex following lingual nerve injury. Neurosci Res 69:100–110. doi:10.1016/j.neures.2010.11.004
37. Inoue K (2002) Microglial activation by purines and pyrimidines. Glia 40(2):156–163. doi:10.1002/glia.10150
38. Inoue K (2006) The function of microglia through purinergic receptors: neuropathic pain and cytokine release. Pharmacol Ther 109(1–2):210–226. doi:10.1016/j.pharmthera.2005.07.001
39. Tsuda M, Shigemoto-Mogami Y, Koizumi S, Mizokoshi A, Kohsaka S, Salter MW, Inoue K (2003) P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature 424(6950):778–783
40. Wieseler-Frank J, Maier SF, Watkins LR (2005) Central proinflammatory cytokines and pain enhancement. Neurosignals 14(4):166–174
41. Zhuang ZY, Kawasaki Y, Tan PH, Wen YR, Huang J, Ji RR (2007) Role of the CX3CR1/p38 MAPK pathway in spinal microglia for the development of neuropathic pain following nerve injury-induced cleavage of fractalkine. Brain Behav Immun 21(5):642–651. doi:10.1016/j.bbi.2006.11.003
42. Lisney SJ, Devor M (1987) Afterdischarge and interactions among fibers in damaged peripheral nerve in the rat. Brain Res 415(1):122–136
43. Seltzer Z, Devor M (1979) Ephaptic transmission in chronically damaged peripheral nerves. Neurology 29(7):1061–1064
44. Cho IH, Lee MJ, Jang M, Gwak NG, Lee KY, Jung HS (2012) Minocycline markedly reduces acute visceral nociception via inhibiting neuronal ERK phosphorylation. Mol Pain 8:13. doi:10.1186/1744-8069-8-13
45. Mei XP, Xu H, Xie C, Ren J, Zhou Y, Zhang H, Xu LX (2011) Post-injury administration of minocycline: an effective treatment for nerve-injury induced neuropathic pain. Neurosci Res 70(3):305–312. doi:10.1016/j.neures.2011.03.012
46. Owolabi SA, Saab CY (2006) Fractalkine and minocycline alter neuronal activity in the spinal cord dorsal horn. FEBS Lett 580(18):4306–4310. doi:10.1016/j.febslet.2006.06.087
47. Padi SS, Kulkarni SK (2008) Minocycline prevents the development of neuropathic pain, but not acute pain: possible anti-inflammatory and antioxidant mechanisms. Eur J Pharmacol 601(1–3):79–87. doi:10.1016/j.ejphar.2008.10.018
48. Biggs JE, Lu VB, Stebbing MJ, Balasubramanyan S, Smith PA (2010) Is BDNF sufficient for information transfer between microglia and dorsal horn neurons during the onset of central sensitization? Mol Pain 6:44. doi:10.1186/1744-8069-6-44
49. Zhou LJ, Yang T, Wei X, Liu Y, Xin WJ, Chen Y, Pang RP, Zang Y, Li YY, Liu XG (2011) Brain-derived neurotrophic factor contributes to spinal long-term potentiation and mechanical hypersensitivity by activation of spinal microglia in rat. Brain Behav Immun 25(2):322–334. doi:10.1016/j.bbi.2010.09.025
50. Eriksson NP, Persson JK, Aldskogius H, Svensson M (1997) A quantitative analysis of the glial cell reaction in primary sensory termination areas following sciatic nerve injury and treatment with nerve growth factor in the adult rat. Exp Brain Res 114(3):393–404
51. Kreutzberg GW (1996) Microglia: a sensor for pathological events in the CNS. Trends Neurosci 19(8):312–318
52. Jin SX, Zhuang ZY, Woolf CJ, Ji RR (2003) p38 mitogen-activated protein kinase is activated after a spinal nerve ligation in spinal cord microglia and dorsal root ganglion neurons and contributes to the generation of neuropathic pain. J Neurosci 23(10):4017–4022
53. Wen YR, Suter MR, Kawasaki Y, Huang J, Pertin M, Kohno T, Berde CB, Decosterd I, Ji RR (2007) Nerve conduction blockade in the sciatic nerve prevents but does not reverse the activation of p38 mitogen-activated protein kinase in spinal microglia in the rat spared nerve injury model. Anesthesiology 107(2):312–321. doi:10.1097/01.anes.0000270759.11086.e7
54. Coull JA, Beggs S, Boudreau D, Boivin D, Tsuda M, Inoue K, Gravel C, Salter MW, De Koninck Y (2005) BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature 438(7070):1017–1021. doi:10.1038/nature04223
55. Coull JA, Boudreau D, Bachand K, Prescott SA, Nault F, Sik A, De Koninck P, De Koninck Y (2003) Trans-synaptic shift in anion gradient in spinal lamina I neurons as a mechanism of neuropathic pain. Nature 424(6951):938–942. doi:10.1038/nature01868