Differential activation of spinal microglial and astroglial cells in a mouse model of peripheral neuropathic pain

Amin, 1996, A novel mechanism of action of tetracyclines: effects on nitric oxide synthases, Proc. Natl. Acad. Sci. U.S.A., 93, 14014, 10.1073/pnas.93.24.14014 Aronson, 1980, Pharmacotherapeutics of the newer tetracyclines, J. Am. Vet. Med. Assoc., 176, 1061 Bennett, 1988, A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man, Pain, 33, 87, 10.1016/0304-3959(88)90209-6 Blum, 2004, Clinical potential of minocycline for neurodegenerative disorders, Neurobiol. Dis., 17, 359, 10.1016/j.nbd.2004.07.012 Chaplan, 1994, Quantitative assessment of tactile allodynia in the rat paw, J. Neurosci. Methods, 53, 55, 10.1016/0165-0270(94)90144-9 Chen, 2007, Hyperalgesia in response to traumatic occlusion and GFAP expression in rat correction of parabranchial nucleus: modulation with fluorocitrate, Cell Tissue Res., 329, 231, 10.1007/s00441-007-0409-3 Choi, 1994, Behavioral signs of ongoing pain and cold allodynia in a rat model of neuropathic pain, Pain, 59, 369, 10.1016/0304-3959(94)90023-X Colburn, 1999, The effect of site and type of nerve injury on spinal glial activation and neuropathic pain behavior, Exp. Neurol., 157, 289, 10.1006/exnr.1999.7065 Colovic, 2003, Liquid chromatographic determination of minocycline in brain-to-plasma distribution studies in the rat, Life Sci., 791, 337 Coyle, 1998, Partial peripheral nerve injury leads to activation of astroglia and microglia which parallels the development of allodynic behavior, Glia, 23, 75, 10.1002/(SICI)1098-1136(199805)23:1<75::AID-GLIA7>3.0.CO;2-3 Cui, 2008, A novel role of minocycline: attenuating morphine antinociceptive tolerance by inhibition of p38 MAPK in the activated spinal microglia, Brain Behav. Immun., 22, 114, 10.1016/j.bbi.2007.07.014 DeLeo, 2004, Neuroimmune activation and neuroinflammation in chronic pain and opioid tolerance/hyperalgesia, Neuroscientist., 10, 40, 10.1177/1073858403259950 Dorazil-Dudzik, 2004, The effects of local pentoxifylline and propentofylline treatment on formalin-induced pain and tumor necrosis factor-alpha messenger RNA levels in the inflamed tissue of the rat paw, Anesth. Analg., 98, 1566, 10.1213/01.ANE.0000113235.88534.48 Fehlings, 2005, Current status of clinical trials for acute spinal cord injury, Injury, 36, 113, 10.1016/j.injury.2005.06.022 Garrison, 1991, Staining of glial fibrillary acidic protein (GFAP) in lumbar spinal cord increases following a sciatic nerve constriction injury, Brain Res., 565, 1, 10.1016/0006-8993(91)91729-K Gieseler, 2009, Inhibitory modulation of the mitochondrial permeability transition by minocycline, Biochem Pharmacol., 77, 888, 10.1016/j.bcp.2008.11.003 Griffin, 2007, Complement induction in spinal cord microglia results in anaphylatoxin C5a-mediated pain hypersensitivity, J. Neurosci., 27, 8699, 10.1523/JNEUROSCI.2018-07.2007 Gwak, 2009, Remote astrocytic and microglial activation modulates neuronal hyperexcitability and below-level neuropathic pain after spinal injury in rat, Neuroscience, 161, 895, 10.1016/j.neuroscience.2009.03.055 Hains, 2006, Activated microglia contribute to the maintenance of chronic pain after spinal cord injury, J Neurosci., 26, 4308, 10.1523/JNEUROSCI.0003-06.2006 Haydon, P.G., 2001. GLIA: listening and talking to the synapse. Nat. Rev. Neurosci. 2, 185–193. Review. Jasmin, 1998, The cold plate as a test of nociceptive behaviors: description and application to the study of chronic neuropathic and inflammatory pain models, Pain, 75, 367, 10.1016/S0304-3959(98)00017-7 Jin, 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, 4017, 10.1523/JNEUROSCI.23-10-04017.2003 Lan, 2007, Blocking the glial function suppresses subcutaneous formalin-induced nociceptive behavior in the rat, Neurosci Res., 57, 112, 10.1016/j.neures.2006.09.014 Ledeboer, 2005, Minocycline attenuates mechanical allodynia and proinflammatory cytokine expression in rat models of pain facilitation, Pain, 115, 71, 10.1016/j.pain.2005.02.009 Levin, 2008, Complement activation in the peripheral nervous system following the spinal nerve ligation model of neuropathic pain, Pain, 137, 182, 10.1016/j.pain.2007.11.005 Lin, 2007, Chronic intrathecal infusion of minocycline prevents the development of spinal-nerve ligation-induced pain in rats, Reg Anesth Pain Med., 32, 209 Liu, 2007, Pentoxifylline attenuates the development of hyperalgesia in a rat model of neuropathic pain, Neurosci. Lett., 412, 268, 10.1016/j.neulet.2006.11.022 Lu, 2004, Preincisional intravenous pentoxifylline attenuating perioperative cytokine response, reducing morphine consumption, and improving recovery of bowel function in patients undergoing colorectal cancer surgery, Anesth. Analg., 99, 1465, 10.1213/01.ANE.0000132974.32249.C8 Lundblad, 1995, Pentoxifylline improves survival and reduces tumor necrosis factor, interleukin-6, and endothelin-1 in fulminant intra-abdominal sepsis in rats, Shock, 3, 210, 10.1097/00024382-199503000-00009 Ma, 2002, Partial sciatic nerve ligation induces increase in the phosphorylation of extracellular signal-regulated kinase (ERK) and c-Jun N-terminal kinase (JNK) in astrocytes in the lumbar spinal dorsal horn and the gracile nucleus, Pain, 99, 175, 10.1016/S0304-3959(02)00097-0 Marchand, 2005, Role of the immune system in chronic pain, Nat. Rev. Neurosci., 6, 521, 10.1038/nrn1700 Mika, 2007, Minocycline and pentoxifylline attenuate allodynia and hyperalgesia and potentiate the effects of morphine in rat and mouse models of neuropathic pain, Eur. J. Pharmacol., 560, 142, 10.1016/j.ejphar.2007.01.013 Mika, 2009, Attenuation of morphine tolerance by minocycline and pentoxifylline in naive and neuropathic mice, Brain Behav. Immun., 23, 75, 10.1016/j.bbi.2008.07.005 Milligan, 2003, Spinal glia and proinflammatory cytokines mediate mirror-image neuropathic pain in rats, J. Neurosci., 23, 1026, 10.1523/JNEUROSCI.23-03-01026.2003 Mishra, 2009, Antioxidant potential of Minocycline in Japanese encephalitis virus infection in murine neuroblastoma cells: correlation with membrane fluidity and cell death, Neurochem Int., 54, 464, 10.1016/j.neuint.2009.01.022 Nakagawa, 2007, Intrathecal administration of ATP produces long-lasting allodynia in rats: differential mechanisms in the phase of the induction and maintenance, Neuroscience, 147, 445, 10.1016/j.neuroscience.2007.03.045 Narita, 2006, Direct evidence for spinal cord microglia in the development of a neuropathic pain-like state in mice, J. Neurochem., 97, 1337, 10.1111/j.1471-4159.2006.03808.x Neuner, 1994, Pentoxifylline in vivo down-regulates the release of IL-1 beta, IL-6, IL-8 and tumour necrosis factor-alpha by human peripheral blood mononuclear cells, Immunology, 83, 262 Obata, 2006, Spinal glial activation contributes to postoperative mechanical hypersensitivity in the rat, J. Pain, 7, 816, 10.1016/j.jpain.2006.04.004 Paxinos, 1986 Perry, V.H., Matyszak, M.K., Fearn, S., 1993. Altered antigen expression of microglia in the aged rodent CNS. Glia 7, 60-7. Review. Popovich, 1997, Cellular inflammatory response after spinal cord injury in Sprague–Dawley and Lewis rats, J. Comp. Neurol., 377, 443, 10.1002/(SICI)1096-9861(19970120)377:3<443::AID-CNE10>3.0.CO;2-S Qin, 2006, The lumbar spinal cord glial cells actively modulate subcutaneous formalin induced hyperalgesia in the rat, Neurosci. Res., 55, 442, 10.1016/j.neures.2006.04.017 Raghavendra, 2003, Anti-hyperalgesic and morphine-sparing actions of propentofylline following peripheral nerve injury in rats: mechanistic implications of spinal glia and proinflammatory cytokines, Pain, 104, 655, 10.1016/S0304-3959(03)00138-6 Raghavendra, 2004, Complete Freunds adjuvant-induced peripheral inflammation evokes glial activation and proinflammatory cytokine expression in the CNS, Eur. J. Neurosci., 20, 467, 10.1111/j.1460-9568.2004.03514.x Robinson, 1986, Macrophage heterogeneity in the rat as delineated by two monoclonal. Antibodies MRC OX-41 and MRC OX-42, the latter recognizing complement receptor type 3, Immunology, 57, 239 Rodriguez Parkitna, 2006, Comparison of gene expression profiles in neuropathic and inflammatory pain, J. Physiol. Pharmacol., 57, 401 Schafer, 2000, Complement C1q is dramatically up-regulated in brain microglia in response to transient global cerebral ischemia, J. Immunol., 164, 5446, 10.4049/jimmunol.164.10.5446 Smith, K., Leyden, J.J., 2005. Safety of doxycycline and minocycline: a systematic review. Clin. Ther. 27, 1329–1342. Review. Sommer, 1998, Painful mononeuropathy in C57BL/Wld mice with delayed wallerian degeneration:differential effects of cytokine production and nerve regeneration on thermal and mechanical hypersensitivity, Brain Res., 784, 154, 10.1016/S0006-8993(97)01327-9 Sterling, 2004, Minocycline treatment reduces delayed oligodendrocyte death, attenuates axonal dieback, and improves functional outcome after spinal cord injury, J. Neurosci., 24, 2182, 10.1523/JNEUROSCI.5275-03.2004 Strassburger, 2008, Anti-inflammatory treatment with the p38 mitogen-activated protein kinase inhibitor SB239063 is neuroprotective, decreases the number of activated microglia and facilitates neurogenesis in oxygen-glucose-deprived hippocampal slice cultures, Eur. J. Pharmacol., 592, 55, 10.1016/j.ejphar.2008.06.099 Sweitzer, 2001, Intrathecal interleukin-1 receptor antagonist in combination with soluble tumor necrosis factor receptor exhibits an anti-allodynic action in a rat model of neuropathic pain, Neuroscience, 103, 529, 10.1016/S0306-4522(00)00574-1 Tanga, 2004, Quantitative real-time RT-PCR assessment of spinal microglial and astrocytic activation markers in a rat model of neuropathic pain, Neurochem. Int., 45, 397, 10.1016/j.neuint.2003.06.002 Tawfik, 2007, Modulating glial activation in opioid tolerance and neuropathic pain: a role for glutamate transporters, 341 Temburni, 2001, New functions for glia in the brain, Proc. Natl. Acad. Sci. U. S. A., 98, 3631, 10.1073/pnas.081073198 Tikka, 2001, Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia, J. Neurosci., 21, 2580, 10.1523/JNEUROSCI.21-08-02580.2001 Watkins, 2003, Glia: a novel drug discovery target for clinical pain, Nat. Rev. Drug Discov., 2, 973, 10.1038/nrd1251 Watkins, 2001, Spinal cord glia: new players in pain, Pain, 93, 201, 10.1016/S0304-3959(01)00359-1 Watkins, 2005, Glia: novel counter-regulators of opioid analgesia, Trends Neurosci., 28, 661, 10.1016/j.tins.2005.10.001 Wie, 2009, Pentoxifylline attenuates nociceptive sensitization and cytokine expression in a tibia fracture rat model of complex regional pain syndrome, Eur. J. Pain, 13, 253, 10.1016/j.ejpain.2008.04.014 Willoughby, 2003, Fluorocitrate-mediated astroglial dysfunction causes seizures, J Neurosci. Res., 74, 160, 10.1002/jnr.10743 Wordliczek, 2000, The effect of pentoxifylline on post-injury hyperalgesia in rats and postoperative pain in patients, Life Sci., 66, 1155, 10.1016/S0024-3205(00)00419-7 Xin, 2009, Plasticity in expression of the glutamate transporters GLT-1 and GLAST in spinal dorsal horn glial cells following partial sciatic nerve ligation, Molecular Pain, 26, 5 Xu, 2007, 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, 10.1016/j.expneurol.2006.11.016 Xu, 2007, Sciatic Nerve Ligation-Induced Proliferation of Spinal Cord Astrocytes Is Mediated by kappa Opioid Activation of p38 Mitogen-Activated Protein Kinase, J. Neurosci., 27, 2570, 10.1523/JNEUROSCI.3728-06.2007 Yong, 2004, The promise of minocycline in neurology, Lancet Neurol., 3, 744, 10.1016/S1474-4422(04)00937-8 Yrjänheikki, 1999, A tetracycline. derivative, minocycline, reduces inflammation and protects against focal cerebral ischemia with a wide therapeutic window, Proc. Natl. Acad. Sci. U.S.A., 96, 13496, 10.1073/pnas.96.23.13496 Zabel, 1993, Inhibition of endogenous TNF formation by pentoxifylline, Immunobiology, 187, 447, 10.1016/S0171-2985(11)80356-6 Zhang, 2006, Protective effects of minocycline on 3, 4-methylenedioxymethamphetamine-induced neurotoxicity in serotonergic and dopaminergic neurons of mouse brain, Eur. J. Pharmacol., 544, 1, 10.1016/j.ejphar.2006.05.047 Zimmermann, 1983, Ethical guidelines for investigations of experimental pain in conscious animals, Pain, 16, 109, 10.1016/0304-3959(83)90201-4 Zimmermann, 2001, Pathobiology of neuropathic pain, Eur. J. Pharmacol., 429, 23, 10.1016/S0014-2999(01)01303-6