Systemic minocycline differentially influences changes in spinal microglial markers following formalin-induced nociception

Journal of Neuroimmunology

Volumn 221, Issue 1-2, 2010, Pages 25-31

  Li, Kai ^a   Fu, Kai Yuan ^a   Light, Alan R ^b   Mao, Jianren ^c  

^a PEKING UNIVERSITY SCHOOL AND HOSPITAL OF STOMATOLOGY   (China)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Formalin; MHC class I; Microglia; Minocycline; OX 42; P38 MAPK

Indexed keywords

FORMALDEHYDE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MINOCYCLINE; MITOGEN ACTIVATED PROTEIN KINASE P38; CD1 ANTIGEN; CD1B ANTIGEN; HLA ANTIGEN CLASS 1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL STRUCTURE; CHEMICAL LABELING; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; MALE; MICROGLIA; NOCICEPTION; NONHUMAN; PAIN; PRIORITY JOURNAL; RAT; SPINAL CORD; SYSTEMIC THERAPY; UPREGULATION; ANIMAL; CHEMICALLY INDUCED DISORDER; DISEASE MODEL; DRUG EFFECT; METABOLISM; METHODOLOGY; PAIN ASSESSMENT; PATHOLOGY; SPRAGUE DAWLEY RAT; TIME;

ANIMALS; ANTIGENS, CD1; DISEASE MODELS, ANIMAL; FORMALDEHYDE; HISTOCOMPATIBILITY ANTIGENS CLASS I; MALE; MICROGLIA; MINOCYCLINE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PAIN; PAIN MEASUREMENT; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD; TIME FACTORS; UP-REGULATION;

EID: 77951212436     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2010.02.003     Document Type: Article

References (43)

1. Amin A.R., Attur M.G., Thakker G.D., Patel P.D., Vyas P.R., Patel R.N., Patel I.R., Abramson S.B. A novel mechanism of action of tetracyclines: effects on nitric oxide synthases. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:14014-14019.
2. Bianchi M., Panerai A.E. Formalin injection in the tail facilitates hindpaw withdrawal reflexes induced by thermal stimulation in the rat: effect of paracetamol. Neurosci. Lett. 1997, 237:89-92.
3. Cadet R., Aigouy L., Woda A. Enhanced nociceptive behaviour following conditioning injection of formalin in the perioral area of the rat. Brain Res. 1995, 676:189-195.
4. Cho I.H., Chung Y.M., Park C.K., Park S.H., Li H.Y., Kim D., Piao Z.G., Choi S.Y., Lee S.J., Park K., Kim J.S., Jung S.J., Oh S.B. Systemic administration of minocycline inhibits formalin-induced inflammatory pain in rat. Brain Res. 2006, 1072:208-214.
5. Coderre T.J., Vaccarino A.L., Melzack R. Central nervous system plasticity in the tonic pain response to subcutaneous formalin injection. Brain Res. 1990, 535:155-158.
6. Coyle D.E. Partial peripheral nerve injury leads to activation of astroglia and microglia which parallels the development of allodynic behavior. Glia 1998, 23:75-83.
7. De Leo J.A., Tawfik V.L., LaCroix-Fralish M.L. The tetrapartite synapse: path to CNS sensitization and chronic pain. Pain 2006, 122:17-21.
8. Dubuisson D., Dennis S.G. The formalin test: a quantitative study of the analgesic effects of morphine, meperidine, and brain stem stimulation in rats and cats. Pain 1977, 4:161-174.
9. Fendrick S.E., Miller K.R., Streit W.J. Minocycline does not inhibit microglia proliferation or neuronal regeneration in the facial nucleus following crush injury. Neurosci. Lett. 2005, 385:220-223.
10. Fox C., Dingman A., Derugin N., Wendland M.F., Manabat C., Ji S., Ferriero D.M., Vexler Z.S. Minocycline confers early but transient protection in the immature brain following focal cerebral ischemia-reperfusion. J. Cereb. Blood Flow Metab. 2005, 25:1138-1149.
11. Fu K.Y., Light A.R., Maixner W. Long-lasting inflammation and long-term hyperalgesia after subcutaneous formalin injection into the rat hindpaw. J. Pain 2001, 2:2-11.
12. Fu K.Y., Light A.R., Matsushima G.K., Maixner W. Microglial reactions after subcutaneous formalin injection into the rat hind paw. Brain Res. 1999, 825:59-67.
13. Fu K.Y., Tan Y.H., Sung B., Mao J. Peripheral formalin injection induces unique spinal cord microglial phenotypic changes. Neurosci. Lett. 2009, 449:234-239.
14. Graeber M.B., Streit W.J., Kreutzberg G.W. Axotomy of the rat facial nerve leads to increased CR3 complement receptor expression by activated microglial cells. J. Neurosci. Res. 1988, 21:18-24.
15. Hains B.C., Waxman S.G. Activated microglia contribute to the maintenance of chronic pain after spinal cord injury. J. Neurosci. 2006, 26:4308-4317.
16. Hashizume H., DeLeo J.A., Colburn R.W., Weinstein J.N. Spinal glial activation and cytokine expression after lumbar root injury in the rat. Spine 2000, 25:1206-1217.
17. Honore P., Rogers S.D., Schwei M.J., Salak-Johnson J.L., Luger N.M., Sabino M.C., Clohisy D.R., Mantyh P.W. Murine models of inflammatory, neuropathic and cancer pain each generates a unique set of neurochemical changes in the spinal cord and sensory neurons. Neuroscience 2000, 98:585-598.
18. Hua R., Walz W. Minocycline treatment prevents cavitation in rats after a cortical devascularizing lesion. Brain Res. 2006, 1090:172-181.
19. Hua X.Y., Svensson C.I., Matsui T., Fitzsimmons B., Yaksh T.L., Webb M. Intrathecal minocycline attenuates peripheral inflammation-induced hyperalgesia by inhibiting p38 MAPK in spinal microglia. Eur. J. Neurosci. 2005, 22:2431-2440.
20. Ji R.R., Samad T.A., Jin S.X., Schmoll R., Woolf C.J. p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron 2002, 36:57-68.
21. Ji R.R., Suter M.R. p38 MAPK, microglial signaling, and neuropathic pain. Mol. Pain 2007, 3:33.
22. Jin S.X., Zhuang Z.Y., Woolf C.J., Ji R.R. 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. 2003, 23:4017-4022.
23. Kim S.Y., Bae J.C., Kim J.Y., Lee H.L., Lee K.M., Kim D.S., Cho H.J. Activation of p38 MAP kinase in the rat dorsal root ganglia and spinal cord following peripheral inflammation and nerve injury. Neuroreport 2002, 13:2483-2486.
24. Ledeboer A., Sloane E.M., Milligan E.D., Frank M.G., Mahony J.H., Maier S.F., Watkins L.R. Minocycline attenuates mechanical allodynia and proinflammatory cytokine expression in rat models of pain facilitation. Pain 2005, 115:71-83.
25. Lin C.S., Tsaur M.L., Chen C.C., Wang T.Y., Lin C.F., Lai Y.L., Hsu T.C., Pan Y.Y., Yang C.H., Cheng J.K. Chronic intrathecal infusion of minocycline prevents the development of spinal-nerve ligation-induced pain in rats. Reg. Anesth. Pain Med. 2007, 32:209-216.
26. Lin T., Li K., Zhang F.Y., Zhang Z.K., Light A.R., Fu K.Y. Dissociation of spinal microglia morphological activation and peripheral inflammation in inflammatory pain models. J. Neuroimmunol. 2007, 192:40-48.
27. Marchand F., Tsantoulas C., Singh D., Grist J., Clark A.K., Bradbury E.J., McMahon S.B. Effects of Etanercept and Minocycline in a rat model of spinal cord injury. Eur. J. Pain 2009, 13:673-681.
28. McMahon S.B., Cafferty W.B., Marchand F. Immune and glial cell factors as pain mediators and modulators. Exp. Neurol. 2005, 192:444-462.
29. Moalem G., Tracey D.J. Immune and inflammatory mechanisms in neuropathic pain. Brain Res. Rev. 2006, 51:240-264.
30. Molander C., Hongpaisan J., Svensson M., Aldskogius H. Glial cell reactions in the spinal cord after sensory nerve stimulation are associated with axonal injury. Brain Res. 1997, 747:122-129.
31. Owolabi S.A., Saab C.Y. Fractalkine and minocycline alter neuronal activity in the spinal cord dorsal horn. FEBS Lett. 2006, 580:4306-4310.
32. Piao Z.G., Cho I.H., Park C.K., Hong J.P., Choi S.Y., Lee S.J., Lee S., Park K., Kim J.S., Oh S.B. Activation of glia and microglial p38 MAPK in medullary dorsal horn contributes to tactile hypersensitivity following trigeminal sensory nerve injury. Pain 2006, 121:219-231.
33. Raghavendra V., Tanga F., DeLeo J.A. Inhibition of microglial activation attenuates the development but not existing hypersensitivity in a rat model of neuropathy. J. Pharmacol. Exp. Ther. 2003, 306:624-630.
34. Ravina B.M., Fagan S.C., Hart R.G., Hovinga C.A., Murphy D.D., Dawson T.M., Marler J.R. Neuroprotective agents for clinical trials in Parkinson's disease: a systematic assessment. Neurology 2003, 60:1234-1240.
35. Sharma N.K., Ryals J.M., Liu H., Liu W., Wright D.E. Acidic saline-induced primary and secondary mechanical hyperalgesia in mice. J. Pain 2009, 10:1231-1241.
36. Skyba D.A., King E.W., Sluka K.A. Effects of NMDA and non-NMDA ionotropic glutamate receptor antagonists on the development and maintenance of hyperalgesia induced by repeated intramuscular injection of acidic saline. Pain 2002, 98:69-78.
37. Svensson C.I., Marsala M., Westerlund A., Calcutt N.A., Campana W.M., Freshwater J.D., Catalano R., Feng Y., Protter A.A., Scott B., Yaksh T.L. Activation of p38 mitogen-activated protein kinase in spinal microglia is a critical link in inflammation-induced spinal pain processing. J Neurochem 2003, 86:1534-1544.
38. Svensson C.I., Schafers M., Jones T.L., Powell H., Sorkin L.S. Spinal blockade of TNF blocks spinal nerve ligation-induced increases in spinal P-p38. Neurosci. Lett. 2005, 379:209-213.
39. Tikka T.M., Koistinaho J.E. Minocycline provides neuroprotection against N-methyl-d-aspartate neurotoxicity by inhibiting microglia. J. Immunol. 2001, 166:7527-7533.
40. Tsuda M., Mizokoshi A., Shigemoto-Mogami Y., Koizumi S., Inoue K. Activation of p38 mitogen-activated protein kinase in spinal hyperactive microglia contributes to pain hypersensitivity following peripheral nerve injury. Glia 2004, 45:89-95.
41. Watkins L.R., Hutchinson M.R., Milligan E.D., Maier S.F. "Listening" and "talking" to neurons: implications of immune activation for pain control and increasing the efficacy of opioids. Brain Res. Rev. 2007, 56:148-169.
42. Wiertelak E.P., Furness L.E., Horan R., Martinez J., Maier S.F., Watkins L.R. Subcutaneous formalin produces centrifugal hyperalgesia at a non-injected site via the NMDA-nitric oxide cascade. Brain Res. 1994, 649:19-26.
43. Yong V.W., Wells J., Giuliani F., Casha S., Power C., Metz L.M. The promise of minocycline in neurology. Lancet Neurol. 2004, 3:744-751.