Role of glia in neuropathic pain

Frontiers in Bioscience - Landmark

Volumn 19, Issue 5, 2014, Pages 798-807

  Liu, Fangting ^a   Yuan, Hongbin ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Glia; Inflammation; Neuropathic pain; Review

Indexed keywords

GLIA; HUMAN; NEURALGIA; PATHOPHYSIOLOGY; PHYSIOLOGY; REVIEW;

HUMANS; NEURALGIA; NEUROGLIA;

EID: 84904299519     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/4247     Document Type: Review

References (119)

1. Baron R: Mechanisms of disease: neuropathic pain - a clinical perspective. Nat Clin Pract Neurol 2,95-106 (2006)
2. Jha MK, Jeon S, Suk K: Glia as a Link between Neuroinflammation and Neuropathic Pain. Immune Netw 12,41-7 (2012)
3. Mika J, Zychowska M, Popiolek-Barczyk K, Rojewska E, Przewlocka B: Importance of glial activation in neuropathic pain. Eur J Pharmacol 716,106-19 (2013)
4. Baron R: Neuropathic pain: a clinical perspective. Handb Exp Pharmacol 3-30 (2009)
5. Birklein F: Mechanisms of neuropathic pain and their importance in Fabry disease. Acta Paediatr Suppl 91,34-7 (2002)
6. Chiang CY, Dostrovsky JO, Iwata K, Sessle BJ: Role of glia in orofacial pain. Neuroscientist 17,303-20 (2011)
7. Chiang CY, Sessle BJ, Dostrovsky JO: Role of astrocytes in pain. Neurochem Res 37,2419-31 (2012)
8. Tsuda M, Beggs S, Salter MW, Inoue K: Microglia and intractable chronic pain. Glia 61,55-61 (2013)
9. Inoue K, Tsuda M: The role of microglia and ATP receptors in a mechanism of neuropathic pain. Nihon Yakurigaku Zasshi 127,14-7 (2006)
10. Lu B, Yao J, Lei W, Xiao C, Sun JL: Role of the CX3CR1/ERK5 pathway in spinal microglia for the development of neuropathic pain. Zhonghua Yi Xue Za Zhi 93,1997-2000 (2013)
11. Gao YJ, Ji RR: Targeting astrocyte signaling for chronic pain. Neurotherapeutics 7,482-93 (2010)
12. Tsuda M, Inoue K: Role of molecules expressed in spiral microglia in neuropathic pain. Nihon Shinkei Seishin Yakurigaku Zasshi 26,57-61 (2006)
13. Hansson E, Ronnback L: Glial neuronal signaling in the central nervous system. FASEB J 17,341-8 (2003)
14. Ji RR, Kawasaki Y, Zhuang ZY, Wen YR, Decosterd I: Possible role of spinal astrocytes in maintaining chronic pain sensitization: review of current evidence with focus on bFGF/JNK pathway. Neuron Glia Biol 2,259-69 (2006)
15. Brandow AM, Farley RA, Panepinto JA: Neuropathic pain in patients with sickle cell disease. Pediatr Blood Cancer (2013)
16. Teixeira MJ, Paiva WS, Assis MS, Fonoff ET, Bor-Seng-Shu E, Cecon AD: Neuropathic pain in patients with spinal cord injury: report of 213 patients. Arq Neuropsiquiatr 71,600-3 (2013)
17. Geber C, Breimhorst M, Burbach B, Egenolf C, Baier B, Fechir M, Koerber J, Treede RD, Vogt T, Birklein F: Pain in chemotherapy-induced neuropathy - More than neuropathic? Pain (2013)
18. Jones RC, Backonja MM: Review of neuropathic pain screening and assessment tools. Curr Pain Headache Rep 17,363 (2013)
19. Jongen JL, Hans G, Benzon HT, Huygen F, Hartrick CT: Neuropathic Pain and Pharmacological Treatment. Pain Pract (2013)
20. Magrinelli F, Zanette G, Tamburin S: Neuropathic pain: diagnosis and treatment. Pract Neurol 13,292-307 (2013)
21. Nakipoglu-Yuzer GF, Atci N, Ozgirgin N: Neuropathic pain in spinal cord injury. Pain Physician 16,259-64 (2013)
22. Clark MR: Chronic Pain Perspectives: Targeting systemic inflammation in patients with obesity-related pain: How best to prevent acute pain from becoming chronic? J Fam Pract 62,S3-9 (2013)
23. Pritzlaff S, Carinci AJ, Christo PJ: Chronic Pain Perspectives: Targeting systemic inflammation in patients with obesity-related pain: Neurogenic thoracic outlet syndrome: An often overlooked but treatable condition. J Fam Pract 62,S16-21 (2013)
24. Nardi N, Campillo-Gimenez B, Pong S, Branchu P, Ecoffey C, Wodey E: Chronic pain after cesarean: Impact and risk factors associated. Ann Fr Anesth Reanim (2013)
25. Liou JT, Liu FC, Mao CC, Lai YS, Day YJ: Inflammation confers dual effects on nociceptive processing in chronic neuropathic pain model. Anesthesiology 114,660-72 (2011)
26. Fredberg U, Stengaard-Pedersen K: Chronic tendinopathy tissue pathology, pain mechanisms, and etiology with a special focus on inflammation. Scand J Med Sci Sports 18,3-15 (2008)
27. Tal M: A Role for Inflammation in Chronic Pain. Curr Rev Pain 3,440-446 (1999)
28. Edwards T: Inflammation, pain, and chronic disease: an integrative approach to treatment and prevention. Altern Ther Health Med 11,20-7; quiz 28, 75 (2005)
29. Kaufmann T, Bloch C, Schmidt W, Jonas L: Chronic inflammation and pain inside the mandibular jaw and a 10-year forgotten amalgam filling in an alveolar cavity of an extracted molar tooth. Ultrastruct Pathol 29,405-13 (2005)
30. Ludwig M, Vidal A, Diemer T, Pabst W, Failing K, Weidner W: Chronic prostatitis/chronic pelvic pain pyndrome): seminal markers of inflammation. World J Urol 21,82-5 (2003)
31. Ellis A, Bennett DL: Neuroinflammation and the generation of neuropathic pain. Br J Anaesth 111,26-37 (2013)
32. Attal N: Management of neuropathic cancer pain. Ann Oncol 21,1134-5 (2010)
33. Yeng LT: Pharmacological treatment of neuropathic pain. Drugs Today (Barc) 45 Suppl C,7-12 (2009)
34. Bickel A: Therapeutic strategies for neuropathic pain. MMW Fortschr Med 151,40-4; quiz 45 (2009)
35. Marquez JO: Neuropathic pain. Arq Neuropsiquiatr 67,1166-7; author reply 1167 (2009)
36. Information from your family doctor. Diabetic peripheral neuropathic pain. Am Fam Physician 82,159 (2010)
37. Fischer TZ, Waxman SG: Neuropathic pain in diabetes - evidence for a central mechanism. Nat Rev Neurol 6,462-6 (2010)
38. Ou GK, Wang RX, Li JJ, Cao H, Lian QQ, Li J: Effect of M8046 on expression of COX-2/PGE2 in spinal cord and DRG in rats with neuropathic pain. Zhongguo Ying Yong Sheng Li Xue Za Zhi 29,97-100, 105 (2013)
39. Ma W, St-Jacques B, Duarte PC: Targeting pain mediators induced by injured nerve-derived COX2 and PGE2 to treat neuropathic pain. Expert Opin Ther Targets 16,527-40 (2012)
40. Ma W, Quirion R: Does COX2-dependent PGE2 play a role in neuropathic pain? Neurosci Lett 437,165-9 (2008)
41. Westlund KN, Zhang L, Ma F, Oz HS: Chronic inflammation and pain in a tumor necrosis factor receptor (TNFR) (p55/p75-/-) dual deficient murine model. Transl Res 160,84-94 (2012)
42. Okamoto K, Martin DP, Schmelzer JD, Mitsui Y, Low PA: Pro- and anti-inflammatory cytokine gene expression in rat sciatic nerve chronic constriction injury model of neuropathic pain. Exp Neurol 169,386-91 (2001)
43. Luo Y, Zou Y, Yang L, Liu J, Liu S: Transplantation of NSCs with OECs alleviates neuropathic pain associated with NGF downregulation in rats following spinal cord injury. Neurosci Lett 549,103-8 (2013)
44. Cirillo G, Cavaliere C, Bianco MR, De Simone A, Colangelo AM, Sellitti S: Intrathecal NGF administration reduces reactive astrocytosis and changes neurotrophin receptors expression pattern in a rat model of neuropathic pain. Cell Mol Neurobiol 30,51-62 (2010)
45. Kiguchi N, Kobayashi Y, Kishioka S: Chemokines and cytokines in neuroinflammation leading to neuropathic pain. Curr Opin Pharmacol 12,55-61 (2012)
46. Myers RR, Campana WM, Shubayev VI: The role of neuroinflammation in neuropathic pain: mechanisms and therapeutic targets. Drug Discov Today 11,8-20 (2006)
47. Araque A, Navarrete M: Glial cells in neuronal network function. Philos Trans R Soc Lond B Biol Sci 365,2375-81 (2010)
48. Lopez-Bayghen E, Ortega A: Glial cells and synaptic activity: translational control of metabolic coupling. Rev Neurol 50,607-15 (2010)
49. Sills RC, Garman RH: Gene expression, biomarkers, and glial cells in nervous system diseases. Toxicol Pathol 39,97-8 (2011)
50. Zawadzka M, Rivers LE, Fancy SP, Zhao C, Tripathi R, Jamen F, Young K, Goncharevich A, Pohl H, Rizzi M, Rowitch DH, Kessaris N, Suter U, Richardson WD, Franklin RJ: CNS-resident glial progenitor/stem cells produce Schwann cells as well as oligodendrocytes during repair of CNS demyelination. Cell Stem Cell 6,578-90 (2010)
51. Deitmer JW, Steinhauser C: Synaptic processes-The role of glial cells. Preface. Brain Res Rev 63,1 (2010)
52. Pfrieger FW: Role of glial cells in the formation and maintenance of synapses. Brain Res Rev 63,39-46 (2010)
53. Gosselin RD, Suter MR, Ji RR, Decosterd I: Glial cells and chronic pain. Neuroscientist 16,519-31 (2010)
54. Jasmin L, Vit JP, Bhargava A, Ohara PT: Can satellite glial cells be therapeutic targets for pain control? Neuron Glia Biol 6,63-71 (2010)
55. Colburn RW, Rickman AJ, DeLeo JA: The effect of site and type of nerve injury on spinal glial activation and neuropathic pain behavior. Exp Neurol 157,289-304 (1999)
56. Colburn RW, DeLeo JA, Rickman AJ, Yeager MP, Kwon P, Hickey WF: Dissociation of microglial activation and neuropathic pain behaviors following peripheral nerve injury in the rat. J Neuroimmunol 79,163-75 (1997)
57. Coyle DE: Partial peripheral nerve injury leads to activation of astroglia and microglia which parallels the development of allodynic behavior. Glia 23,75-83 (1998)
58. Ledeboer A, Hutchinson MR, Watkins LR, Johnson KW: Ibudilast (AV-411). A new class therapeutic candidate for neuropathic pain and opioid withdrawal syndromes. Expert Opin Investig Drugs 16,935-50 (2007)
59. Chang L, Cooper MS, Clark VP: Imaging biomarkers and the role of neuroinflammation in neuropathic pain. J Neuroimmune Pharmacol 8,448-51 (2013)
60. Chang RC, Chiu K, Ho YS, So KF: Modulation of neuroimmune responses on glia in the central nervous system: implication in therapeutic intervention against neuroinflammation. Cell Mol Immunol 6,317-26 (2009)
61. Kielian T, Esen N: Effects of neuroinflammation on glia-glia gap junctional intercellular communication: a perspective. Neurochem Int 45,429-36 (2004)
62. Foresti ML, Arisi GM, Shapiro LA: Role of glia in epilepsy-associated neuropathology, neuroinflammation and neurogenesis. Brain Res Rev 66,115-22 (2011)
63. Skaper SD, Facci L, Giusti P: Mast cells, glia and neuroinflammation: partners in crime? Immunology (2013)
64. Whalley K: Neuroimmunology: Targeting microglia. Nat Rev Neurosci 14,741 (2013)
65. Li Y, Du XF, Du JL: Physiological properties and functions of microglia. Sheng Li Xue Bao 65,471-82 (2013)
66. Tsuda M, Masuda T, Kitano J, Shimoyama H, Tozaki-Saitoh H, Inoue K: IFN-gamma receptor signaling mediates spinal microglia activation driving neuropathic pain. Proc Natl Acad Sci U S A 106,8032-7 (2009)
67. Aldskogius H, Kozlova EN: Microglia and neuropathic pain. CNS Neurol Disord Drug Targets 12,768-72 (2013)
68. Tsuda M, Tozaki-Saitoh H, Inoue K: Purinergic system, microglia and neuropathic pain. Curr Opin Pharmacol 12,74-9 (2012)
69. Inoue K, Tsuda M: Purinergic systems, neuropathic pain and the role of microglia. Exp Neurol 234,293-301 (2012)
70. Biber K, Tsuda M, Tozaki-Saitoh H, Tsukamoto K, Toyomitsu E: Neuronal CCL21 up-regulates microglia P2X4 expression and initiates neuropathic pain development. EMBO J 30,1864-73 (2011)
71. Thacker MA, Clark AK, Bishop T, Grist J, Yip PK, Moon LD: CCL2 is a key mediator of microglia activation in neuropathic pain states. Eur J Pain 13,263-72 (2009)
72. Xu JT, Xin WJ, Wei XH, Wu CY: p38 activation in uninjured primary afferent neurons and in spinal microglia contributes to the development of neuropathic pain induced by selective motor fiber injury. Exp Neurol 204,355-65 (2007)
73. Lindia JA, McGowan E, Jochnowitz N, Abbadie C: Induction of CX3CL1 expression in astrocytes and CX3CR1 in microglia in the spinal cord of a rat model of neuropathic pain. J Pain 6,434-8 (2005)
74. Zhuang ZY, Kawasaki Y, Tan PH, Wen YR: 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 21,642-51 (2007)
75. Coull JA, Beggs S, Boudreau D, Boivin D, Tsuda M, Inoue K: BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature 438,1017-21 (2005)
76. Inoue K, Tsuda M: P2X4 receptors of microglia in neuropathic pain. CNS Neurol Disord Drug Targets 11,699-704 (2012)
77. Beggs S, Trang T, Salter MW: P2X4R+ microglia drive neuropathic pain. Nat Neurosci 15,1068-73 (2012)
78. Kobayashi K, Takahashi E, Miyagawa Y: Induction of the P2X7 receptor in spinal microglia in a neuropathic pain model. Neurosci Lett 504,57-61 (2011)
79. Ulmann L, Hatcher JP, Hughes JP, Chaumont S, Green PJ, Conquet F, Buell GN: Up-regulation of P2X4 receptors in spinal microglia after peripheral nerve injury mediates BDNF release and neuropathic pain. J Neurosci 28,11263-8 (2008)
80. Kobayashi K, Yamanaka H, Yanamoto F: Multiple P2Y subtypes in spinal microglia are involved in neuropathic pain after peripheral nerve injury. Glia 60,1529-39 (2012)
81. He WJ, Cui J, Du L, Zhao YD, Burnstock G: Spinal P2X(7) receptor mediates microglia activation-induced neuropathic pain in the sciatic nerve injury rat model. Behav Brain Res 226,163-70 (2012)
82. Honore P, Donnelly-Roberts D, Namovic MT, Hsieh G, Zhu CZ: A-740003 [N-(1-{[(cyanoimino)(5-quinolinylamino)methyl]amino}-2,2-dimethylpropyl)-2- (3,4-dimethoxyphenyl)acetamide], a novel and selective P2X7 receptor antagonist, dose-dependently reduces neuropathic pain in the rat. J Pharmacol Exp Ther 319,1376-85 (2006)
83. Watson AJ, Frank MG: Astrocytes do the "shuttle". Sleep 36,1413-4 (2013)
84. Garrison CJ, Dougherty PM, Kajander KC, Carlton SM: Staining of glial fibrillary acidic protein (GFAP) in lumbar spinal cord increases following a sciatic nerve constriction injury. Brain Res 565,1-7 (1991)
85. Didier M, Harandi M, Aguera M, Bancel B, Tardy M: Differential immunocytochemical staining for glial fibrillary acidic (GFA) protein, S-100 protein and glutamine synthetase in the rat subcommissural organ, nonspecialized ventricular ependyma and adjacent neuropil. Cell Tissue Res 245,343-51 (1986)
86. Ikeda H, Kiritoshi T, Murase K: Contribution of microglia and astrocytes to the central sensitization, inflammatory and neuropathic pain in the juvenile rat. Mol Pain 8,43 (2012)
87. Zhuang ZY, Wen YR, Zhang DR, Borsello T, Bonny C: A peptide c-Jun N-terminal kinase (JNK) inhibitor blocks mechanical allodynia after spinal nerve ligation: respective roles of JNK activation in primary sensory neurons and spinal astrocytes for neuropathic pain development and maintenance. J Neurosci 26,3551-60 (2006)
88. Zhuang ZY, Gerner P, Woolf CJ, Ji RR: ERK is sequentially activated in neurons, microglia, and astrocytes by spinal nerve ligation and contributes to mechanical allodynia in this neuropathic pain model. Pain 114,149-59 (2005)
89. Hofstetter C, Boockvar J: Generation of neural stem cells: a team approach. Neurosurgery 67,N22-3 (2010)
90. Hofstetter CP, Boockvar JA: Neural stem cells: targeting glioma in 3-dimensions. Neurosurgery 66,N15 (2010)
91. Davies JE, Proschel C, Zhang N, Noble M: Transplanted astrocytes derived from BMP- or CNTF-treated glial-restricted precursors have opposite effects on recovery and allodynia after spinal cord injury. J Biol 7,24 (2008)
92. Davies JE, Huang C, Proschel C, Noble M: Astrocytes derived from glial-restricted precursors promote spinal cord repair. J Biol 5,7 (2006)
93. Gao YJ, Zhang L, Samad OA, Suter MR, Yasuhiko K, Xu ZZ: JNK-induced MCP-1 production in spinal cord astrocytes contributes to central sensitization and neuropathic pain. J Neurosci 29,4096-108 (2009)
94. Mirzaei V, Manaheji H, Maghsoudi N and Zaringhalam J: Comparison of changes in mRNA expression of spinal glutamate transporters following induction of two neuropathic pain models. Spinal Cord 48,791-7 (2010)
95. Sung B, Lim G, Mao J: Altered expression and uptake activity of spinal glutamate transporters after nerve injury contribute to the pathogenesis of neuropathic pain in rats. J Neurosci 23,2899-910 (2003)
96. Jacobs VL, De Leo JA: Increased glutamate uptake in astrocytes via propentofylline results in increased tumor cell apoptosis using the CNS-1 glioma model. J Neurooncol 114,33-42 (2013)
97. Norsted Gregory E, Delaney A, Abdelmoaty S, Bas DB, Codeluppi S: Pentoxifylline and propentofylline prevent proliferation and activation of the mammalian target of rapamycin and mitogen activated protein kinase in cultured spinal astrocytes. J Neurosci Res 91,300-12 (2013)
98. Vinken M, Vanhaecke T, Papeleu P, Snykers S: Connexins and their channels in cell growth and cell death. Cell Signal 18,592-600 (2006)
99. Chen MJ, Kress B, Han X, Moll K, Peng W: Astrocytic CX43 hemichannels and gap junctions play a crucial role in development of chronic neuropathic pain following spinal cord injury. Glia 60,1660-70 (2012)
100. Roh DH, Yoon SY, Seo HS, Kang SY, Han HJ: Intrathecal injection of carbenoxolone, a gap junction decoupler, attenuates the induction of below-level neuropathic pain after spinal cord injury in rats. Exp Neurol 224,123-32 (2010)
101. Zhang ZJ, Dong YL, Lu Y, Cao S: Chemokine CCL2 and its receptor CCR2 in the medullary dorsal horn are involved in trigeminal neuropathic pain. J Neuroinflammation 9,136 (2012)
102. Kingwell K: Pain: MAPK inhibitor shows promise in clinical trial for neuropathic pain. Nat Rev Neurol 7,360 (2011)
103. Wu J, Xu Y, Pu S, Jiang W, Du D: p38/MAPK inhibitor modulates the expression of dorsal horn GABA(B) receptors in the spinal nerve ligation model of neuropathic pain. Neuroimmunomodulation 18,150-5 (2011)
104. Ji RR, Suter MR: p38 MAPK, microglial signaling, and neuropathic pain. Mol Pain 3,33 (2007)
105. Ma W, Quirion R: The ERK/MAPK pathway, as a target for the treatment of neuropathic pain. Expert Opin Ther Targets 9,699-713 (2005)
106. Jarvis MF, Honore P, Shieh CC, Chapman M: A-803467, a potent and selective Nav1.8 sodium channel blocker, attenuates neuropathic and inflammatory pain in the rat. Proc Natl Acad Sci U S A 104,8520-5 (2007)
107. Lai J, Gold MS, Kim CS, Bian D, Ossipov MH: Inhibition of neuropathic pain by decreased expression of the tetrodotoxin-resistant sodium channel, NaV1.8. Pain 95,143-52 (2002)
108. Armero P, Muriel C, Lopez M, Santos J, Gonzalez-Sarmiento R: Analysis of TRPV1 gene polymorphisms in Spanish patients with neuropathic pain. Med Clin (Barc) 139,1-4 (2012)
109. Christoph T, Grunweller A, Mika J, Schafer MK: Silencing of vanilloid receptor TRPV1 by RNAi reduces neuropathic and visceral pain in vivo. Biochem Biophys Res Commun 350,238-43 (2006)
110. Urano H, Ara T, Fujinami Y, Hiraoka BY: Aberrant TRPV1 expression in heat hyperalgesia associated with trigeminal neuropathic pain. Int J Med Sci 9,690-7 (2012)
111. Finnerup NB, Sindrup SH, Jensen TS: The evidence for pharmacological treatment of neuropathic pain. Pain 150,573-81 (2010)
112. Cvijanovic M, Simic S, Banic Horvat S, Jovin Z: Contemporary treatment neuropathic pain. Med Pregl 64,443-7 (2011)
113. Smith HS, Argoff CE: Pharmacological treatment of diabetic neuropathic pain. Drugs 71,557-89 (2011)
114. Jefferies K: Treatment of neuropathic pain. Semin Neurol 30,425-32 (2010)
115. Vranken JH: Elucidation of pathophysiology and treatment of neuropathic pain. Cent Nerv Syst Agents Med Chem 12,304-14 (2012)
116. Garg G, Adams JD: Treatment of neuropathic pain with plant medicines. Chin J Integr Med 18,565-70 (2012)
117. Cho DC, Cheong JH, Yang MS, Hwang SJ, Kim JM, Kim CH: The effect of minocycline on motor neuron recovery and neuropathic pain in a rat model of spinal cord injury. J Korean Neurosurg Soc 49,83-91 (2011)
118. Guasti L, Richardson D, Jhaveri M, Eldeeb K, Barrett D: Minocycline treatment inhibits microglial activation and alters spinal levels of endocannabinoids in a rat model of neuropathic pain. Mol Pain 5,35 (2009)
119. Padi SS, Kulkarni SK: Minocycline prevents the development of neuropathic pain, but not acute pain: possible anti-inflammatory and antioxidant mechanisms. Eur J Pharmacol 601,79-87 (2008)