Spinal microglial motility is independent of neuronal activity and plasticity in adult mice

Molecular Pain

Volumn 6, Issue , 2010, Pages

  Chen, Tao ^a,b   Koga, Kohei ^a   Li, Xiang Yao ^a,b   Zhuo, Min ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b Seoul National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; ADENOSINE TRIPHOSPHATE; CARBACHOL; CHEMOKINE; CYTOKINE; FRACTALKINE; GLUTAMIC ACID; NEUROTRANSMITTER; NORADRENALIN; SEROTONIN; SUBSTANCE P; ACETYLCHOLINE; MORPHINE;

ADULT ANIMAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MOTILITY; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DORSAL ROOT; FEMALE; IN VIVO STUDY; MACROPHAGE; MALE; MICROGLIA; MOUSE; NERVE CELL PLASTICITY; NERVE CONDUCTION; NERVE INJURY; NOCICEPTIVE STIMULATION; NONHUMAN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; SPINAL CORD; SPINAL CORD DORSAL HORN; TISSUE SLICE; ANIMAL; CYTOLOGY; DRUG EFFECT; IN VITRO STUDY; METABOLISM; PHYSIOLOGY; SPINAL ROOT; TRANSGENIC MOUSE;

ACETYLCHOLINE; ADENOSINE TRIPHOSPHATE; ANIMALS; CARBACHOL; FEMALE; GLUTAMIC ACID; MALE; MICE; MICE, TRANSGENIC; MICROGLIA; MORPHINE; NOREPINEPHRINE; SEROTONIN; SPINAL CORD; SPINAL NERVE ROOTS; SUBSTANCE P;

EID: 77950642677     PISSN: 17448069     EISSN: None     Source Type: Journal    
DOI: 10.1186/1744-8069-6-19     Document Type: Article

References (44)

1. Hickey WF. Basic principles of immunological surveillance of the normal central nervous system. Glia 2001, 36:118-124. 10.1002/glia.1101, 11596120.
2. Streit WJ, Mrak RE, Griffin WS. Microglia and neuroinflammation: a pathological perspective. J Neuroinflammation 2004, 1:14. 10.1186/1742-2094-1-14, 509427, 15285801.
3. Nimmerjahn A, Kirchhoff F, Helmchen F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 2005, 308:1314-1318. 10.1126/science.1110647, 15831717.
4. Inoue K, Tsuda M. Microglia and neuropathic pain. Glia 2009, 57:1469-1479. 10.1002/glia.20871, 19306358.
5. Tsuda M, Inoue K, Salter MW. Neuropathic pain and spinal microglia: a big problem from molecules in "small" glia. Trends Neurosci 2005, 28:101-107. 10.1016/j.tins.2004.12.002, 15667933.
6. McMahon SB, Malcangio M. Current challenges in glia-pain biology. Neuron 2009, 64:46-54. 10.1016/j.neuron.2009.09.033, 19840548.
7. Turchan-Cholewo J, Dimayuga FO, Ding Q, Keller JN, Hauser KF, Knapp PE, Bruce-Keller AJ. Cell-specific actions of HIV-Tat and morphine on opioid receptor expression in glia. J Neurosci Res 2008, 86:2100-2110. 10.1002/jnr.21653, 2760290, 18338799.
8. Farber K, Kettenmann H. Physiology of microglial cells. Brain Res Brain Res Rev 2005, 48:133-143. 10.1016/j.brainresrev.2004.12.003, 15850652.
9. Fields RD, Burnstock G. Purinergic signalling in neuron-glia interactions. Nat Rev Neurosci 2006, 7:423-436. 10.1038/nrn1928, 2062484, 16715052.
10. Calvo CF, Cesselin F, Gelman M, Glowinski J. Identification of an opioid peptide secreted by rat embryonic mixed brain cells as a promoter of macrophage migration. Eur J Neurosci 2000, 12:2676-2684. 10.1046/j.1460-9568.2000.00145.x, 10971611.
11. Liu GJ, Nagarajah R, Banati RB, Bennett MR. Glutamate induces directed chemotaxis of microglia. Eur J Neurosci 2009, 29:1108-1118. 10.1111/j.1460-9568.2009.06659.x, 19302147.
12. Wu LJ, Zhuo M. Resting microglial motility is independent of synaptic plasticity in mammalian brain. J Neurophysiol 2008, 99:2026-2032. 10.1152/jn.01210.2007, 18256162.
13. Zhang F, Vadakkan KI, Kim SS, Wu LJ, Shang Y, Zhuo M. Selective activation of microglia in spinal cord but not higher cortical regions following nerve injury in adult mouse. Mol Pain 2008, 4:15. 10.1186/1744-8069-4-15, 2374773, 18423014.
14. Zhuo M. Neuronal mechanism for neuropathic pain. Mol Pain 2007, 3:14. 10.1186/1744-8069-3-14, 1904186, 17553143.
15. Sandkuhler J. Understanding LTP in pain pathways. Mol Pain 2007, 3:9. 10.1186/1744-8069-3-9, 1852298, 17407590.
16. Sandkuhler J, Liu X. Induction of long-term potentiation at spinal synapses by noxious stimulation or nerve injury. Eur J Neurosci 1998, 10:2476-2480. 10.1046/j.1460-9568.1998.00278.x, 9749775.
17. Ji RR, Suter MR. p38 MAPK, microglial signaling, and neuropathic pain. Mol Pain 2007, 3:33. 10.1186/1744-8069-3-33, 2186318, 17974036.
18. Jung S, Aliberti J, Graemmel P, Sunshine MJ, Kreutzberg GW, Sher A, Littman DR. Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol Cell Biol 2000, 20:4106-4114. 10.1128/MCB.20.11.4106-4114.2000, 85780, 10805752.
19. Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, Jung S, Littman DR, Dustin ML, Gan WB. ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 2005, 8:752-758. 10.1038/nn1472, 15895084.
20. Wu LJ, Vadakkan KI, Zhuo M. ATP-induced chemotaxis of microglial processes requires P2Y receptor-activated initiation of outward potassium currents. Glia 2007, 55:810-821. 10.1002/glia.20500, 17357150.
21. Li P, Wilding TJ, Kim SJ, Calejesan AA, Huettner JE, Zhuo M. Kainate-receptor-mediated sensory synaptic transmission in mammalian spinal cord. Nature 1999, 397:161-164. 10.1038/16469, 9923678.
22. Li P, Zhuo M. Substance P and neurokinin A mediate sensory synaptic transmission in young rat dorsal horn neurons. Brain Res Bull 2001, 55:521-531. 10.1016/S0361-9230(01)00553-6, 11543953.
23. Feng YP, Li YQ, Wang W, Wu SX, Chen T, Shigemoto R, Mizuno N. Morphological evidence for GABA/glycine-cocontaining terminals in synaptic contact with neurokinin-1 receptor-expressing neurons in the sacral dorsal commissural nucleus of the rat. Neurosci Lett 2005, 388:144-148. 10.1016/j.neulet.2005.06.022, 16043285.
24. Sawynok J, Reid A. Interactions of descending serotonergic systems with other neurotransmitters in the modulation of nociception. Behav Brain Res 1996, 73:63-68. 10.1016/0166-4328(96)00072-1, 8788479.
25. Watkins LR, Hutchinson MR, Johnston IN, Maier SF. Glia: novel counter-regulators of opioid analgesia. Trends Neurosci 2005, 28:661-669.
26. Lograsso M, Nadeson R, Goodchild CS. The spinal antinociceptive effects of cholinergic drugs in rats: receptor subtype specificity in different nociceptive tests. BMC Pharmacol 2002, 2:20. 10.1186/1471-2210-2-20, 137595, 12441008.
27. Millan MJ. Descending control of pain. Prog Neurobiol 2002, 66:355-474. 10.1016/S0301-0082(02)00009-6, 12034378.
28. Ikeda H, Heinke B, Ruscheweyh R, Sandkuhler J. Synaptic plasticity in spinal lamina I projection neurons that mediate hyperalgesia. Science 2003, 299:1237-1240. 10.1126/science.1080659, 12595694.
29. Ikeda H, Stark J, Fischer H, Wagner M, Drdla R, Jager T, Sandkuhler J. Synaptic amplifier of inflammatory pain in the spinal dorsal horn. Science 2006, 312:1659-1662. 10.1126/science.1127233, 16778058.
30. Watkins LR, Milligan ED, Maier SF. Spinal cord glia: new players in pain. Pain 2001, 93:201-205. 10.1016/S0304-3959(01)00359-1, 11514078.
31. Abbadie C, Lindia JA, Cumiskey AM, Peterson LB, Mudgett JS, Bayne EK, DeMartino JA, MacIntyre DE, Forrest MJ. Impaired neuropathic pain responses in mice lacking the chemokine receptor CCR2. Proc Natl Acad Sci USA 2003, 100:7947-7952. 10.1073/pnas.1331358100, 164693, 12808141.
32. 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 2005, 6:434-438. 10.1016/j.jpain.2005.02.001, 15993821.
33. Tsuda M, Shigemoto-Mogami Y, Koizumi S, Mizokoshi A, Kohsaka S, Salter MW, Inoue K. P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature 2003, 424:778-783. 10.1038/nature01786, 12917686.
34. Boucsein C, Zacharias R, Farber K, Pavlovic S, Hanisch UK, Kettenmann H. Purinergic receptors on microglial cells: functional expression in acute brain slices and modulation of microglial activation in vitro. Eur J Neurosci 2003, 17:2267-2276. 10.1046/j.1460-9568.2003.02663.x, 12814360.
35. Thacker MA, Clark AK, Bishop T, Grist J, Yip PK, Moon LD, Thompson SW, Marchand F, McMahon SB. CCL2 is a key mediator of microglia activation in neuropathic pain states. Eur J Pain 2009, 13:263-272. 10.1016/j.ejpain.2008.04.017, 18554968.
36. White FA, Sun J, Waters SM, Ma C, Ren D, Ripsch M, Steflik J, Cortright DN, Lamotte RH, Miller RJ. Excitatory monocyte chemoattractant protein-1 signaling is up-regulated in sensory neurons after chronic compression of the dorsal root ganglion. Proc Natl Acad Sci USA 2005, 102:14092-14097. 10.1073/pnas.0503496102, 1236537, 16174730.
37. Harrison JK, Jiang Y, Chen S, Xia Y, Maciejewski D, McNamara RK, Streit WJ, Salafranca MN, Adhikari S, Thompson DA, et al. Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia. Proc Natl Acad Sci USA 1998, 95:10896-10901. 10.1073/pnas.95.18.10896, 27992, 9724801.
38. Nishiyori A, Minami M, Ohtani Y, Takami S, Yamamoto J, Kawaguchi N, Kume T, Akaike A, Satoh M. Localization of fractalkine and CX3CR1 mRNAs in rat brain: does fractalkine play a role in signaling from neuron to microglia?. FEBS Lett 1998, 429:167-172. 10.1016/S0014-5793(98)00583-3, 9650583.
39. Verge GM, Milligan ED, Maier SF, Watkins LR, Naeve GS, Foster AC. Fractalkine (CX3CL1) and fractalkine receptor (CX3CR1) distribution in spinal cord and dorsal root ganglia under basal and neuropathic pain conditions. Eur J Neurosci 2004, 20:1150-1160. 10.1111/j.1460-9568.2004.03593.x, 15341587.
40. Coull JA, Beggs S, Boudreau D, Boivin D, Tsuda M, Inoue K, Gravel C, Salter MW, De Koninck Y. BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature 2005, 438:1017-1021. 10.1038/nature04223, 16355225.
41. Milligan ED, Watkins LR. Pathological and protective roles of glia in chronic pain. Nat Rev Neurosci 2009, 10:23-36. 10.1038/nrn2533, 2752436, 19096368.
42. Ozaktay AC, Kallakuri S, Takebayashi T, Cavanaugh JM, Asik I, DeLeo JA, Weinstein JN. Effects of interleukin-1 beta, interleukin-6, and tumor necrosis factor on sensitivity of dorsal root ganglion and peripheral receptive fields in rats. Eur Spine J 2006, 15:1529-1537. 10.1007/s00586-005-0058-8, 16474945.
43. Yoshimura M, Jessell TM. Primary afferent-evoked synaptic responses and slow potential generation in rat substantia gelatinosa neurons in vitro. J Neurophysiol 1989, 62:96-108.
44. Yasaka T, Kato G, Furue H, Rashid MH, Sonohata M, Tamae A, Murata Y, Masuko S, Yoshimura M. Cell-type-specific excitatory and inhibitory circuits involving primary afferents in the substantia gelatinosa of the rat spinal dorsal horn in vitro. J Physiol 2007, 581:603-618. 10.1113/jphysiol.2006.123919, 2075204, 17347278.