P2X4R + microglia drive neuropathic pain

Nature Neuroscience

Volumn 15, Issue 8, 2012, Pages 1068-1073

  Beggs, Simon ^a,b,c   Trang, Tuan ^a,b,d   Salter, Michael W ^a,b,c,d  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; FIBRONECTIN; MITOGEN ACTIVATED PROTEIN KINASE; MONOCYTE CHEMOTACTIC PROTEIN 1; PURINERGIC P2X4 RECEPTOR;

ALLODYNIA; CELL PROLIFERATION; CEREBROSPINAL FLUID; HOMEOSTASIS; HUMAN; HYPERALGESIA; HYPERSENSITIVITY; IMMUNOCOMPETENT CELL; IN VIVO STUDY; INFECTION; INFLAMMATORY PAIN; INJURY; MICROGLIA; NERVE INJURY; NERVOUS SYSTEM INFLAMMATION; NEUROPATHIC PAIN; NEUROPROTECTION; NOCICEPTIVE STIMULATION; NONHUMAN; PAIN; PERIPHERAL NERVE; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW;

ANIMALS; BIOLOGICAL MARKERS; HUMANS; MICROGLIA; NEURALGIA; PERIPHERAL NERVES; PHENOTYPE; RATS; RECEPTORS, PURINERGIC P2X4;

EID: 84864487226     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3155     Document Type: Review

References (50)

1. Hanisch, U.-K. & Kettenmann, H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat. Neurosci. 10, 1387-1394 (2007).
2. Tsuda, M. et al. P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature 424, 778-783 (2003).
3. Ulmann, L. et al. Up-regulation of P2X4 receptors in spinal microglia after peripheral nerve injury mediates BDNF release and neuropathic pain. J. Neurosci. 28, 11263-11268 (2008).
4. Trang, T., Beggs, S., Wan, X. & Salter, M.W. P2X4-receptor-mediated synthesis and release of brain-derived neurotrophic factor in microglia is dependent on calcium and p38-mitogen-activated protein kinase activation. J. Neurosci. 29, 3518-3528 (2009).
5. Nissl, F. Ueber einige Beziehungen zur Nervenzellenerkrankungen und gliosen Erscheinungen bei verschiedenen Psychosen. Arch. Psychiatr. 32, 656-676 (1899).
6. Cammermeyer, J. Juxtavascular karyokinesis and microglia cell proliferation during retrograde reaction in the mouse facial nucleus. Ergeb. Anat. Entwicklungsgesch. 38, 1-22 (1965).
7. Gehrmann, J., Monaco, S. & Kreutzberg, G.W. Spinal cord microglial cells and DRG satellite cells rapidly respond to transection of the rat sciatic nerve. Restor. Neurol. Neurosci. 2, 181-198 (1991).
8. Eriksson, N.P. et al. A quantitative analysis of the microglial cell reaction in central primary sensory projection territories following peripheral nerve injury in the adult rat. Exp. Brain Res. 96, 19-27 (1993).
9. Graeber, M.B., Tetzlaff, W., Streit, W.J. & Kreutzberg, G.W. Microglial cells but not astrocytes undergo mitosis following rat facial nerve axotomy. Neurosci. Lett. 85, 317-321 (1988).
10. Svensson, M., Eriksson, P., Persson, J., Liu, L. & Aldskogius, H. Functional properties of microglia following peripheral nerve injury. Neuropathol. Appl. Neurobiol. 20, 185-187 (1994).
11. Kreutzberg, G.W. Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 19, 312-318 (1996).
12. Liu, L., Persson, J.K., Svensson, M. & Aldskogius, H. Glial cell responses, complement, and clusterin in the central nervous system following dorsal root transection. Glia 23, 221-238 (1998).
13. Rezaie, P. & Male, D. Mesoglia & microglia-a historical review of the concept of mononuclear phagocytes within the central nervous system. J. Hist. Neurosci. 11, 325-374 (2002).
14. Penfield, W. Cytology & Cellular Pathology of the Nervous System (Hafner, 1965).
15. Clark, A.K., Gentry, C., Bradbury, E.J., McMahon, S.B. & Malcangio, M. Role of spinal microglia in rat models of peripheral nerve injury and inflammation. Eur. J. Pain 11, 223-230 (2007).
16. Honore, P. et al. Murine models of inflammatory, neuropathic and cancer pain each generates a unique set of neurochemical changes in the spinal cord and sensory neurons. Neuroscience 98, 585-598 (2000).
17. Lin, T. et al. Dissociation of spinal microglia morphological activation and peripheral inflammation in inflammatory pain models. J. Neuroimmunol. 192, 40-48 (2007).
18. Tsuda, M. et al. Behavioral phenotypes of mice lacking purinergic P2X4 receptors in acute and chronic pain assays. Mol. Pain 5, 28 (2009).
19. Zhang, J. et al. Expression of CCR2 in both resident and bone marrow-derived microglia plays a critical role in neuropathic pain. J. Neurosci. 27, 12396-12406 (2007).
20. Abbadie, C. et al. Chemokines and pain mechanisms. Brain Res. Rev. 60, 125-134 (2009).
21. Toyomitsu, E. et al. CCL2 promotes P2X4 receptor trafficking to the cell surface of microglia. Purinergic Signal. 8, 301-310 (2012).
22. Biber, K. et al. Neuronal CCL21 up-regulates microglia P2X4 expression and initiates neuropathic pain development. EMBO J. 30, 1864-1873 (2011).
23. de Jong, E.K. et al. Vesicle-mediated transport and release of CCL21 in endangered neurons: a possible explanation for microglia activation remote from a primary lesion. J. Neurosci. 25, 7548-7557 (2005).
24. de Jong, E.K. et al. Expression, transport, and axonal sorting of neuronal CCL21 in large dense-core vesicles. FASEB J. 22, 4136-4145 (2008).
25. Tsuda, M. et al. IFN-γ receptor signaling mediates spinal microglia activation driving neuropathic pain. Proc. Natl. Acad. Sci. USA 106, 8032-8037 (2009).
26. Tsuda, M. et al. Fibronectin/integrin system is involved in P2X4 receptor upregulation in the spinal cord and neuropathic pain after nerve injury. Glia 56, 579-585 (2008).
27. Nasu-Tada, K., Koizumi, S., Tsuda, M., Kunifusa, E. & Inoue, K. Possible involvement of increase in spinal fibronectin following peripheral nerve injury in upregulation of microglial P2X4, a key molecule for mechanical allodynia. Glia 53, 769-775 (2006).
28. Tsuda, M., Toyomitsu, E., Kometani, M., Tozaki-Saitoh, H. & Inoue, K. Mechanisms underlying fibronectin-induced up-regulation of P2X4R expression in microglia: distinct roles of PI3K-Akt and MEK-ERK signalling pathways. J. Cell. Mol. Med. 13, 3251-3259 (2009).
29. Tsuda, M. et al. Lyn tyrosine kinase is required for P2X4 receptor upregulation and neuropathic pain after peripheral nerve injury. Glia 56, 50-58 (2008).
30. Yuan, H. et al. Role of mast cell activation in inducing microglial cells to release neurotrophin. J. Neurosci. Res. 88, 1348-1354 (2010).
31. Coull, J.A.M. et al. Trans-synaptic shift in anion gradient in spinal lamina I neurons as a mechanism of neuropathic pain. Nature 424, 938-942 (2003).
32. Prescott, S.A., Sejnowski, T.J. & De Koninck, Y. Reduction of anion reversal potential subverts the inhibitory control of firing rate in spinal lamina I neurons: towards a biophysical basis for neuropathic pain. Mol. Pain 2, 32 (2006).
33. Knabl, J. et al. Reversal of pathological pain through specific spinal GABAA receptor subtypes. Nature 451, 330-334 (2008).
34. Coull, J.A.M. et al. BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature 438, 1017-1021 (2005).
35. Keller, A.F., Beggs, S., Salter, M.W. & De Koninck, Y. Transformation of the output of spinal lamina I neurons after nerve injury and microglia stimulation underlying neuropathic pain. Mol. Pain 3, 27 (2007).
36. Jahr, C.E. & Jessell, T.M. ATP excites a subpopulation of rat dorsal horn neurones. Nature 304, 730-733 (1983).
37. + wave propagation in dorsal spinal cord astrocytes. J. Neurosci. 20, 2800-2808 (2000).
38. Foley, J.C., McIver, S.R. & Haydon, P.G. Gliotransmission modulates baseline mechanical nociception. Mol. Pain 7, 93 (2011).
39. Salter, M.W., De Koninck, Y. & Henry, J.L. Physiological roles for adenosine and ATP in synaptic transmission in the spinal dorsal horn. Prog. Neurobiol. 41, 125-156 (1993).
40. Suter, M.R., Berta, T., Gao, Y.-J., Decosterd, I. & Ji, R.-R. Large A-fiber activity is required for microglial proliferation and p38 MAPK activation in the spinal cord: different effects of resiniferatoxin and bupivacaine on spinal microglial changes after spared nerve injury. Mol. Pain 5, 53 (2009).
41. Tozaki-Saitoh, H. et al. P2Y12 receptors in spinal microglia are required for neuropathic pain after peripheral nerve injury. J. Neurosci. 28, 4949-4956 (2008).
42. Kettenmann, H., Hanisch, U.-K., Noda, M. & Verkhratsky, A. Physiology of microglia. Physiol. Rev. 91, 461-553 (2011).
43. Rivest, S. Regulation of innate immune responses in the brain. Nat. Rev. Immunol. 9, 429-439 (2009).
44. Milligan, E.D. & Watkins, L.R. Pathological and protective roles of glia in chronic pain. Nat. Rev. Neurosci. 10, 23-36 (2009).
45. Landry, R.P., Jacobs, V.L., Romero-Sandoval, E.A. & Deleo, J.A. 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, 340-350 (2012).
46. Watkins, L.R., Hutchinson, M.R. & Johnson, K.W. 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, 351-353 (2012).
47. Sorge, R.E. et al. Spinal cord Toll-like receptor 4 mediates inflammatory and neuropathic hypersensitivity in male but not female mice. J. Neurosci. 31, 15450-15454 (2011).
48. Beggs, S., Currie, G., Salter, M.W., Fitzgerald, M. & Walker, S.M. Priming of adult pain responses by neonatal pain experience: maintenance by central neuroimmune activity. Brain 135, 404-417 (2012).
49. Suleman, S., Beggs, S., Mogil, J.S. & Salter, M.W. Genetic correlation of microglial activation-associated proteins and pain-related behaviours across 12 inbred mouse strains. Proc. 12th World Congress on Pain. (IASP Press, 2008).
50. Asiedu, M., Ossipov, M.H., Kaila, K. & Price, T.J. Acetazolamide and midazolam act synergistically to inhibit neuropathic pain. Pain 148, 302-308 (2010).