Activity-triggered tetrapartite neuron-glial interactions following peripheral injury

Current Opinion in Pharmacology

Volumn 26, Issue , 2016, Pages 16-25

  Ren, Ke ^a,b   Dubner, Ronald ^a,b  

^a UNIVERSITY OF MARYLAND DENTAL SCHOOL   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CCR7; CONNEXIN 43; FRACTALKINE; GLIAL FIBRILLARY ACIDIC PROTEIN; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 10; INTERLEUKIN 17 RECEPTOR; INTERLEUKIN 18; INTERLEUKIN 18 RECEPTOR; INTERLEUKIN 1BETA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN S100B; PURINERGIC P2Y12 RECEPTOR; VESICULAR GLUTAMATE TRANSPORTER 1;

ANTINOCICEPTION; ARTICLE; CELL ACTIVATION; CELL ACTIVITY; CELL INTERACTION; CELL MOTILITY; CHRONIC PAIN; DOWN REGULATION; GLIA CELL; HUMAN; INTRACELLULAR SIGNALING; NERVE CELL; NERVE CELL EXCITABILITY; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; ANIMAL; GLIA; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; CHRONIC PAIN; HUMANS; NEUROGLIA; NEURONS; NEUROPROTECTION; PERIPHERAL NERVE INJURIES;

EID: 84943328434     PISSN: 14714892     EISSN: 14714973     Source Type: Journal    
DOI: 10.1016/j.coph.2015.09.006     Document Type: Review

References (92)

1. R.R. Ji, Z.Z. Xu, and Y.J. Gao Emerging targets in neuroinflammation-driven chronic pain Nat Rev Drug Discov 13 2014 533 548
2. D.N. Xanthos, and J. Sandkühler Neurogenic neuroinflammation: inflammatory CNS reactions in response to neuronal activity Nat Rev Neurosci 15 2014 43 53
3. A. Aguzzi, B.A. Barres, and M.L. Bennett Microglia: scapegoat, saboteur, or something else? Science 339 2013 156 161
4. A.J. Svahn, T.S. Becker, and M.B. Graeber Emergent properties of microglia Brain Pathol 24 2014 665 670
5. S.B. McMahon, and M. Malcangio Current challenges in glia-pain biology Neuron 64 2009 46 54
6. Y. Shi, B.B. Gelman, J.G. Lisinicchia, and S.J. Tang Chronic-pain-associated astrocytic reaction in the spinal cord dorsal horn of human immunodeficiency virus-infected patients J Neurosci 32 2012 10833 10840
7. M.F. Bjurstrom, S.E. Giron, and C.A. Griffis Cerebrospinal fluid cytokines and neurotrophic factors in human chronic pain populations: a comprehensive review Pain Pract 2014 10.1111/papr.12252 [Epub ahead of print]
8. M.L. Loggia, D.B. Chonde, O. Akeju, G. Arabasz, C. Catana, R.R. Edwards, E. Hill, S. Hsu, D. Izquierdo-Garcia, R.R. Ji, and et al. Evidence for brain glial activation in chronic pain patients Brain 138 2015 604 615
9. V. Papadopoulos, M. Baraldi, T.R. Guilarte, T.B. Knudsen, J.J. Lacapère, P. Lindemann, M.D. Norenberg, D. Nutt, A. Weizman, M.R. Zhang, and et al. Translocator protein (18kDa): new nomenclature for the peripheral-type benzodiazepine receptor based on its structure and molecular function Trends Pharmacol Sci 27 2006 402 409
10. H. Hernstadt, S. Wang, G. Lim, and J. Mao Spinal translocator protein (TSPO) modulates pain behavior in rats with CFA-induced monoarthritis Brain Res 1286 2009 42 52
11. X.H. Wei, X. Wei, F.Y. Chen, Y. Zang, W.J. Xin, R.P. Pang, Y. Chen, J. Wang, Y.Y. Li, K.F. Shen, and et al. The upregulation of translocator protein (18 kDa) promotes recovery from neuropathic pain in rats J Neurosci 33 2013 1540 1551
12. S. Biesmans, P.D. Acton, C. Cotto, X. Langlois, L. Ver Donck, J.A. Bouwknecht, S.A. Aelvoet, N. Hellings, T.F. Meert, and R. Nuydens Effect of stress and peripheral immune activation on astrocyte activation in transgenic bioluminescent Gfap-luc mice Glia 63 2015 1126 1137
13. R.B. Banati, A. Cagnin, D.J. Brooks, R.N. Gunn, R. Myers, T. Jones, R. Birch, and P. Anand Long-term trans-synaptic glial responses in the human thalamus after peripheral nerve injury Neuroreport 12 2001 3439 3442
14. H. Kettenmann, U.K. Hanisch, M. Noda, and A. Verkhratsky Physiology of microglia Physiol Rev 91 2011 461 553
15. U.B. Eyo, and L.J. Wu Bidirectional microglia-neuron communication in the healthy brain Neural Plast 2013 2013 456857
16. M.W. Salter, and S. Beggs Sublime microglia: expanding roles for the guardians of the CNS Cell 158 2014 15 24
17. Y.R. Wen, M.R. Suter, Y. Kawasaki, J. Huang, M. Pertin, T. Kohno, C.B. Berde, I. Decosterd, and R.R. Ji 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 2007 312 321
18. M. Okubo, A. Castro, W. Guo, S. Zou, K. Ren, F. Wei, A. Keller, and R. Dubner Transition to persistent orofacial pain after nerve injury involves supraspinal serotonin mechanisms J Neurosci 33 2013 5152 5161
19. A.M. Taylor, A. Castonguay, A.J. Taylor, N.P. Murphy, A. Ghogha, C. Cook, L. Xue, M.C. Olmstead, Y. De Koninck, C.J. Evans, and et al. Microglia disrupt mesolimbic reward circuitry in chronic pain J Neurosci 35 2015 8442 8450
20. K. Baalman, M.A. Marin, T.S. Ho, M. Godoy, L. Cherian, C. Robertson, and M.N. Rasband Axon initial segment-associated microglia J Neurosci 35 2015 2283 2292
21. M.È. Tremblay, R.L. Lowery, and A.K. Majewska Microglial interactions with synapses are modulated by visual experience PLoS Biol 8 2010 e1000527
22. U.B. Eyo, N. Gu, S. De, H. Dong, J.R. Richardson, and L.J. Wu Modulation of microglial process convergence toward neuronal dendrites by extracellular calcium J Neurosci 35 2015 2417 2422
23. H. Wake, A.J. Moorhouse, S. Jinno, S. Kohsaka, and J. Nabekura Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals J Neurosci 29 2009 3974 3980
24. S. Beggs, and M.W. Salter The known knowns of microglia-neuronal signalling in neuropathic pain Neurosci Lett 557 2013 37 42
25. P. Barragán-Iglesias, J.B. Pineda-Farias, C. Cervantes-Durán, M. Bravo-Hernández, H.I. Rocha-González, J. Murbartián, and V. Granados-Soto Role of spinal P2Y6 and P2Y11 receptors in neuropathic pain in rats: possible involvement of glial cells Mol Pain 10 2014 29
26. G. Magni, and S. Ceruti The purinergic system and glial cells: emerging costars in nociception Biomed Res Int 2014 2014 495789
27. Y.L. Ying, X.H. Wei, X.B. Xu, S.Z. She, L.J. Zhou, J. Lv, D. Li, B. Zheng, and X.G. Liu Over-expression of P2X7 receptors in spinal glial cells contributes to the development of chronic postsurgical pain induced by skin/muscle incision and retraction (SMIR) in rats Exp Neurol 261 2014 836 843
28. Y. Yang, H. Li, T.T. Li, H. Luo, X.Y. Gu, N. Lü, R.R. Ji, and Y.Q. Zhang Delayed activation of spinal microglia contributes to the maintenance of bone cancer pain in female Wistar rats via P2X7 receptor and IL-18 J Neurosci 35 2015 7950 7963
29. J. Lee, Y.E. Chun, K.S. Han, J. Lee, D.H. Woo, and C.J. Lee Ca(2+) entry is required for mechanical stimulation-induced ATP release from astrocyte Exp Neurobiol 24 2015 17 23
30. E. Tatsumi, H. Yamanaka, K. Kobayashi, H. Yagi, M. Sakagami, and K. Noguchi RhoA/ROCK pathway mediates p38 MAPK activation and morphological changes downstream of P2Y12/13 receptors in spinal microglia in neuropathic pain Glia 63 2015 216 228
31. J.K. Harrison, Y. Jiang, S. Chen, Y. Xia, D. Maciejewski, R.K. McNamara, W.J. Streit, M.N. Salafranca, S. Adhikari, D.A. Thompson, and et al. Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia Proc Natl Acad Sci USA 95 1998 10896 10901
32. K. Kierdorf, and M. Prinz Factors regulating microglia activation Front Cell Neurosci 7 2013 44
33. M. Kiyomoto, M. Shinoda, A. Okada-Ogawa, N. Noma, K. Shibuta, Y. Tsuboi, B.J. Sessle, Y. Imamura, and K. Iwata Fractalkine signaling in microglia contributes to ectopic orofacial pain following trapezius muscle inflammation J Neurosci 33 2013 7667 7680
34. A.K. Clark, and M. Malcangio Fractalkine/CX3CR1 signaling during neuropathic pain Front Cell Neurosci 8 2014 121
35. R.C. Paolicelli, K. Bisht, and M.È. Tremblay Fractalkine regulation of microglial physiology and consequences on the brain and behavior Front Cell Neurosci 8 2014 129
36. G.M. Verge, E.D. Milligan, S.F. Maier, L.R. Watkins, G.S. Naeve, and A.C. Foster Fractalkine (CX3CL1) and fractalkine receptor (CX3CR1) distribution in spinal cord and dorsal root ganglia under basal and neuropathic pain conditions Eur J Neurosci 20 2004 1150 1160
37. E.A. Old, S. Nadkarni, J. Grist, C. Gentry, S. Bevan, K.W. Kim, A.J. Mogg, M. Perretti, and M. Malcangio Monocytes expressing CX3CR1 orchestrate the development of vincristine-induced pain J Clin Investig 124 2014 2023 2036
38. A.K. Clark, D. Gruber-Schoffnegger, R. Drdla-Schutting, K.J. Gerhold, M. Malcangio, and J. Sandkühler Selective activation of microglia facilitates synaptic strength J Neurosci 35 2015 4552 4570
39. T. Chen, K. Koga, X.Y. Li, and M. Zhuo Spinal microglial motility is independent of neuronal activity and plasticity in adult mice Mol Pain 6 2010 19
40. Y. Ren, X.M. Leng, B. Yang, and X. Zhang Aberrant CD200/CD200R1 expression contributes to painful synovium hyperplasia in a patient with primary hypertrophic osteoarthropathy Rheumatol Int 33 2013 2509 2512
41. C.Y. Chiang, B.J. Sessle, and J.O. Dostrovsky Role of astrocytes in pain Neurochem Res 37 2012 2419 2431
42. R.R. Hansen, and M. Malcangio Astrocytes - multitaskers in chronic pain Eur J Pharmacol 716 2013 120 128
43. R.R. Ji, T. Berta, and M. Nedergaard Glia and pain: is chronic pain a gliopathy? Pain 154 Suppl. 1 2013 S10 S28
44. R.B. Griggs, R.R. Donahue, J. Morgenweck, P.M. Grace, A. Sutton, L.R. Watkins, and B.K. Taylor Pioglitazone rapidly reduces neuropathic pain through astrocyte and non-genomic PPARγ mechanisms Pain 156 2015 469 482
45. H. Wang, W. Guo, K. Yang, F. Wei, R. Dubner, and K. Ren Contribution of primary afferent input to trigeminal astroglial hyperactivity cytokine induction and NMDA receptor phosphorylation Open Pain J 2010 2010 144 152
46. S.A. Shankarappa, J.H. Tsui, K.N. Kim, G. Reznor, J.C. Dohlman, R. Langer, and D.S. Kohane Prolonged nerve blockade delays the onset of neuropathic pain Proc Natl Acad Sci USA 109 2012 17555 17560
47. F. Wei, W. Guo, S. Zou, K. Ren, and R. Dubner Supraspinal glial-neuronal interactions contribute to descending pain facilitation J Neurosci 28 2008 10482 10495
48. G. Chen, C.K. Park, R.G. Xie, T. Berta, M. Nedergaard, and R.R. Ji Connexin-43 induces chemokine release from spinal cord astrocytes to maintain late-phase neuropathic pain in mice Brain 137 2014 2193 2209
49. C.R. Robinson, H. Zhang, and P.M. Dougherty Astrocytes, but not microglia, are activated in oxaliplatin and bortezomib-induced peripheral neuropathy in the rat Neuroscience 274 2014 308 317
50. G. Tenorio, A. Kulkarni, and B.J. Kerr Resident glial cell activation in response to perispinal inflammation leads to acute changes in nociceptive sensitivity: implications for the generation of neuropathic pain Pain 154 2013 71 81
51. H.C. Pan, Y.C. Chou, and S.H. Sun P2X7 R-mediated Ca(2+)-independent d-serine release via pannexin-1 of the P2X7 R-pannexin-1 complex in astrocytes Glia 63 2015 877 893
52. 2+ signalling: an unexpected complexity Nat Rev Neurosci 15 2014 327 335
53. S.R. Bond, and C.C. Naus The pannexins: past and present Front Physiol 5 2014 58
54. D. Bravo, P. Ibarra, J. Retamal, T. Pelissier, C. Laurido, A. Hernandez, and L. Constandil Pannexin 1: a novel participant in neuropathic pain signaling in the rat spinal cord Pain 155 2014 2108-2015
55. B. Sung, G. Lim, and J. Mao Altered expression and uptake activity of spinal glutamate transporters after nerve injury contribute to the pathogenesis of neuropathic pain in rats J Neurosci 23 2003 2899 2910
56. K.J. Nicholson, T.M. Gilliland, and B.A. Winkelstein Upregulation of GLT-1 by treatment with ceftriaxone alleviates radicular pain by reducing spinal astrocyte activation and neuronal hyperexcitability J Neurosci Res 92 2014 116 129
57. H. Nie, and H.R. Weng Impaired glial glutamate uptake induces extrasynaptic glutamate spillover in the spinal sensory synapses of neuropathic rats J Neurophysiol 103 2010 2570 2580
58. C. Karus, M.A. Mondragão, D. Ziemens, and C.R. Rose Astrocytes restrict discharge duration and neuronal sodium loads during recurrent network activity Glia 63 2015 936 957
59. S. Kirischuk, V. Parpura, and A. Verkhratsky Sodium dynamics: another key to astroglial excitability? Trends Neurosci 35 2012 497 506
60. L.E. Spataro, E.M. Sloane, E.D. Milligan, J. Wieseler-Frank, D. Schoeniger, B.M. Jekich, R.M. Barrientos, S.F. Maier, and L.R. Watkins Spinal gap junctions: potential involvement in pain facilitation J Pain 5 2004 392 405
61. H. Wang, Y. Cao, C.Y. Chiang, J.O. Dostrovsky, and B.J. Sessle The gap junction blocker carbenoxolone attenuates nociceptive behavior and medullary dorsal horn central sensitization induced by partial infraorbital nerve transection in rats Pain 155 2014 429 435
62. Q. Xu, Y.K. Cheong, F. Yang, V. Tiwari, J. Li, J. Liu, S.N. Raja, W. Li, and Y. Guan Intrathecal carbenoxolone inhibits neuropathic pain and spinal wide-dynamic range neuronal activity in rats after an L5 spinal nerve injury Neurosci Lett 563 2014 45 50
63. C.R. Robinson, and P.M. Dougherty Spinal astrocyte gap junction and glutamate transporter expression contributes to a rat model of bortezomib-induced peripheral neuropathy Neuroscience 285 2015 1 10
64. M. Rovegno, P.A. Soto, P.J. Sáez, C.C. Naus, J.C. Sáez, and R. von Bernhardi Connexin43 hemichannels mediate secondary cellular damage spread from the trauma zone to distal zones in astrocyte monolayers Glia 63 2015 1185 1199
65. V. Abudara, L. Roux, G. Dallérac, I. Matias, J. Dulong, J.P. Mothet, N. Rouach, and C. Giaume Activated microglia impairs neuroglial interaction by opening Cx43 hemichannels in hippocampal astrocytes Glia 63 2015 795 811
66. J.A. De Leo, V.L. Tawfik, and M.L. LaCroix-Fralish The tetrapartite synapse: path to CNS sensitization and chronic pain Pain 122 2006 17 21
67. K. Ren, and R. Dubner Interactions between the immune and nervous systems in pain Nat Med 16 2010 1267 1276
68. P.M. Grace, M.R. Hutchinson, S.F. Maier, and L.R. Watkins Pathological pain and the neuroimmune interface Nat Rev Immunol 14 2014 217 231
69. A.K. Clark, E.A. Old, and M. Malcangio Neuropathic pain and cytokines: current perspectives J Pain Res 21 2013 803 814
70. M.V. Sofroniew Multiple roles for astrocytes as effectors of cytokines and inflammatory mediators Neuroscientist 20 2014 160 172
71. W. Guo, K. Miyoshi, R. Dubner, M. Gu, M. Li, J. Liu, J. Yang, S. Zou, K. Ren, K. Noguchi, and et al. Spinal 5-HT3 receptors mediate descending facilitation and contribute to behavioral hypersensitivity via a reciprocal neuron-glial signaling cascade Mol Pain 10 2014 35
72. S. Imai, D. Ikegami, A. Yamashita, T. Shimizu, M. Narita, K. Niikura, M. Furuya, Y. Kobayashi, K. Miyashita, D. Okutsu, and et al. Epigenetic transcriptional activation of monocyte chemotactic protein 3 contributes to long-lasting neuropathic pain Brain 136 2013 828 843
73. X. Meng, Y. Zhang, L. Lao, R. Saito, A. Li, C.M. Bäckman, B.M. Berman, K. Ren, P.K. Wei, and R.X. Zhang Spinal interleukin-17 promotes thermal hyperalgesia and NMDA NR1 phosphorylation in an inflammatory pain rat model Pain 154 2013 294 305
74. W. Guo, H. Wang, M. Watanabe, K. Shimizu, S. Zou, S.C. LaGraize, F. Wei, R. Dubner, and K. Ren Glial-cytokine-neuronal interactions underlying the mechanisms of persistent pain J Neurosci 27 2007 6006 6018
75. K.A. Won, M.J. Kim, K.Y. Yang, J.S. Park, M.K. Lee, M.K. Park, Y.C. Bae, and D.K. Ahn The glial-neuronal GRK2 pathway participates in the development of trigeminal neuropathic pain in rats J Pain 15 2014 250 261
76. X. Yan, and H.R. Weng Endogenous interleukin-1β in neuropathic rats enhances glutamate release from the primary afferents in the spinal dorsal horn through coupling with presynaptic N-methyl-d-aspartic acid receptors J Biol Chem 288 2013 30544 30557
77. X. Yan, R. Yadav, M. Gao, and H.R. Weng Interleukin-1 beta enhances endocytosis of glial glutamate transporters in the spinal dorsal horn through activating protein kinase C Glia 62 2014 1093 1109
78. X. Yan, E. Jiang, and H.R. Weng Activation of toll like receptor 4 attenuates GABA synthesis and postsynaptic GABA receptor activities in the spinal dorsal horn via releasing interleukin-1 beta J Neuroinflammation 12 2015 4
79. E.D. Milligan, and L.R. Watkins Pathological and protective roles of glia in chronic pain Nat Rev Neurosci 10 2009 23 36
80. V. Tiwari, Y. Guan, and S.N. Raja Modulating the delicate glial-neuronal interactions in neuropathic pain: promises and potential caveats Neurosci Biobehav Rev 45 2014 19 27
81. A.J. Kwilasz, P.M. Grace, P. Serbedzija, S.F. Maier, and L.R. Watkins The therapeutic potential of interleukin-10 in neuroimmune diseases Neuropharmacology 96 2015 55 69
82. N. Villacampa, B. Almolda, A. Vilella, I.L. Campbell, B. González, and B. Castellano Astrocyte-targeted production of IL-10 induces changes in microglial reactivity and reduces motor neuron death after facial nerve axotomy Glia 63 2015 1166 1184
83. K. Janes, E. Esposito, T. Doyle, S. Cuzzocrea, D.K. Tosh, K.A. Jacobson, and D. Salvemini A3 adenosine receptor agonist prevents the development of paclitaxel-induced neuropathic pain by modulating spinal glial-restricted redox-dependent signaling pathways Pain 155 2014 2560 2567
84. S. Gritsch, J. Lu, S. Thilemann, S. Wörtge, W. Möbius, J. Bruttger, K. Karram, T. Ruhwedel, M. Blanfeld, D. Vardeh, and et al. Oligodendrocyte ablation triggers central pain independently of innate or adaptive immune responses in mice Nat Commun 5 2014 5472
85. M. Leinders, L. Knaepen, M. De Kock, C. Sommer, E. Hermans, and R. Deumens Up-regulation of spinal microglial Iba-1 expression persists after resolution of neuropathic pain hypersensitivity Neurosci Lett 554 2013 146 150
86. V.R. Ducourneau, T. Dolique, S. Hachem-Delaunay, L.S. Miraucourt, A. Amadio, L. Blaszczyk, F. Jacquot, J. Ly, L. Devoize, S.H. Oliet, R. Dallel, and et al. Cancer pain is not necessarily correlated with spinal overexpression of reactive glia markers Pain 155 2014 275 291
87. E. Alfonso Romero-Sandoval, and S. Sweitzer Nonneuronal central mechanisms of pain: glia and immune response Prog Mol Biol Transl Sci 131 2015 325 358
88. R.P. Landry, V.L. Jacobs, E.A. Romero-Sandoval, and J.A. De Leo Propentofylline, a CNS glial modulator does not decrease pain in post-herpetic neuralgia patients: in vitro evidence for differential responses in human and rodent microglia and macrophages Exp Neurol 234 2012 340 350
89. V. Martinez, B. Szekely, J. Lemarié, F. Martin, M. Gentili, S. Ben Ammar, J.F. Lepeintre, C. Garreau de Loubresse, M. Chauvin, and D. Bouhassira The efficacy of a glial inhibitor, minocycline, for preventing persistent pain after lumbar discectomy: a randomized, double-blind, controlled study Pain 234 2013 1197 1203
90. P. Vanelderen, J. Van Zundert, T. Kozicz, M. Puylaert, P. De Vooght, R. Mestrum, R. Heylen, E. Roubos, and K. Vissers Effect of minocycline on lumbar radicular neuropathic pain: a randomized, placebo-controlled, double-blind clinical trial with amitriptyline as a comparator Anesthesiology 122 2015 399 406
91. J. Kalliomäki, N. Attal, B. Jonzon, F.W. Bach, K. Huizar, S. Ratcliffe, B. Eriksson, M. Janecki, A. Danilov, D. Bouhassira, and et al. A randomized, double-blind, placebo-controlled trial of a chemokine receptor 2 (CCR2) antagonist in posttraumatic neuralgia Pain 154 2013 761 767
92. L.R. Watkins, M.R. Hutchinson, and K.W. Johnson Commentary on Landry et al.: "Propentofylline, a CNS glial modulator, does not decrease pain in post-herpetic neuralgia patients: in vitro evidence for differential responses in human and rodent microglia and macrophages" Exp Neurol 234 2012 351 353