Minocycline, a microglial inhibitor, blocks spinal CCL2-induced heat hyperalgesia and augmentation of glutamatergic transmission in substantia gelatinosa neurons

Journal of Neuroinflammation

Volumn 11, Issue , 2014, Pages

  Huang, Chung Yu ^a   Chen, Ying Ling ^b   Li, Allen H ^c   Lu, Juu Chin ^a   Wang, Hung Li ^a,c,d  

^a CHANG GUNG UNIVERSITY   (Taiwan)

^b CHANG GUNG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Taiwan)

^c CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

^d CHANG GUNG UNIVERSITY   (Taiwan)

Author keywords

CC chemokine ligand 2; Glutamatergic transmission; Heat hyperalgesia; Microglia; Substantia gelatinosa neurons; Tumor necrosis factor

Indexed keywords

GLUTAMIC ACID; MINOCYCLINE; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA INHIBITOR; UNCLASSIFIED DRUG; WP 9QY;

AMPLITUDE MODULATION; ANALGESIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; GABAERGIC TRANSMISSION; GLUTAMATERGIC TRANSMISSION; HOT PLATE TEST; HYPERALGESIA; INHIBITORY POSTSYNAPTIC POTENTIAL; LATENT PERIOD; MALE; MICROGLIA; MINIATURE ENDPLATE POTENTIAL; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; RAT; SPINAL CORD NERVE CELL; SUBSTANTIA GELATINOSA; THERMAL STIMULATION; WITHDRAWAL REFLEX;

ANIMALS; CHEMOKINE CCL2; EXCITATORY AMINO ACID AGENTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMIC ACID; GLYCINE AGENTS; HYPERALGESIA; INHIBITORY POSTSYNAPTIC POTENTIALS; MALE; MINOCYCLINE; NEURONS; PAIN THRESHOLD; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; SODIUM CHANNEL BLOCKERS; STRYCHNINE; SUBSTANTIA GELATINOSA; SYNAPTIC TRANSMISSION; TETRODOTOXIN;

EID: 84892383715     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-11-7     Document Type: Article

References (53)

1. Zhang J, De Koninck Y. Spatial and temporal relationship between monocyte chemoattractant protein-1 expression and spinal glial activation following peripheral nerve injury. J Neurochem 2006, 97:772-783. 10.1111/j.1471-4159.2006.03746.x, 16524371.
2. Dansereau MA, Gosselin RD, Pohl M, Pommier B, Mechighel P, Mauborgne A, Rostene W, Kitabgi P, Beaudet N, Sarret P, Melik-Parsadaniantz S. Spinal CCL2 pronociceptive action is no longer effective in CCR2 receptor antagonist-treated rats. J Neurochem 2008, 106:757-769. 10.1111/j.1471-4159.2008.05429.x, 18419759.
3. Gao YJ, Zhang L, Samad OA, Suter MR, Yasuhiko K, Xu ZZ, Park JY, Lind AL, Ma Q, Ji RR. JNK-induced MCP-1 production in spinal cord astrocytes contributes to central sensitization and neuropathic pain. J Neurosci 2009, 29:4096-4108. 10.1523/JNEUROSCI.3623-08.2009, 2682921, 19339605.
4. Jeon SM, Lee KM, Cho HJ. Expression of monocyte chemoattractant protein-1 in rat dorsal root ganglia and spinal cord in experimental models of neuropathic pain. Brain Res 2009, 1251:103-111.
5. Van Steenwinckel J, Reaux-Le Goazigo A, Pommier B, Mauborgne A, Dansereau MA, Kitabgi P, Sarret P, Pohl M, Melik-Parsadaniantz S. CCL2 released from neuronal synaptic vesicles in the spinal cord is a major mediator of local inflammation and pain after peripheral nerve injury. J Neurosci 2011, 15:5865-5875.
6. Abbadie C, Bhangoo S, De Koninck Y, Malcangio M, Melik-Parsadaniantz S, White FA. Chemokines and pain mechanisms. Brain Res Rev 2009, 60:125-135. 10.1016/j.brainresrev.2008.12.002, 2691997, 19146875.
7. Gao YJ, Ji RR. Chemokines, neuronal-glial interactions, and central processing of neuropathic pain. Pharmacol Ther 2010, 126:56-68. 10.1016/j.pharmthera.2010.01.002, 2839017, 20117131.
8. Jung H, Toth PT, White FA, Miller RJ. Monocyte chemoattractant protein-1 functions as a neuromodulator in dorsal root ganglia neurons. J Neurochem 2008, 104:254-263. 2186066, 17944871.
9. 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.
10. Knerlich-Lukoschus F, Juraschek M, Blomer U, Lucius R, Mehdorn HM, Held-Feindt J. Force-dependent development of neuropathic central pain and time-related CCL2/CCR2 expression after graded spinal cord contusion injuries of the rat. J Neurotrauma 2008, 25:427-448. 10.1089/neu.2007.0431, 18338959.
11. Tanaka T, Minami M, Nakagawa T, Satoh M. Enhanced production of monocyte chemoattractant protein-1 in the dorsal root ganglia in a rat model of neuropathic pain: possible involvement in the development of neuropathic pain. Neurosci Res 2004, 48:463-469. 10.1016/j.neures.2004.01.004, 15041200.
12. 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.
13. Light AR, Perl ER. Spinal termination of functionally identified primary afferent neurons with slowly conducting myelinated fibers. J Comp Neurol 1979, 186:133-150. 10.1002/cne.901860203, 109477.
14. 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.
15. Sugiura Y, Lee CL, Perl ER. Central projections of identified unmyelinated (C) afferent fibers innervating mammalian skin. Science 1986, 234:358-361. 10.1126/science.3764416, 3764416.
16. Furue H, Katafuchi T, Yoshimura M. Sensory processing and functional reorganization of sensory transmission under pathological conditions in the spinal dorsal horn. Neurosci Res 2004, 48:361-368. 10.1016/j.neures.2003.12.005, 15041189.
17. Basbaum AI, Bautista DM, Scherrer G, Julius D. Cellular and molecular mechanisms of pain. Cell 2009, 139:267-284. 10.1016/j.cell.2009.09.028, 2852643, 19837031.
18. Woolf CJ, Salter MW. Neuronal plasticity: increasing the gain in pain. Science 2000, 288:1765-1769. 10.1126/science.288.5472.1765, 10846153.
19. Kuner R. Central mechanisms of pathological pain. Nat Med 2010, 16:1258-1266. 10.1038/nm.2231, 20948531.
20. 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.
21. Svensson CI, Marsala M, Westerlund A, Calcutt NA, Campana WM, Freshwater JD, Catalano R, Feng Y, Protter AA, Scott B, Yaksh TL. 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. 10.1046/j.1471-4159.2003.01969.x, 12950462.
22. Raghavendra V, Tanga FY, DeLeo JA. Complete Freund's adjuvant-induced peripheral inflammation evokes glial activation and proinflammatory cytokine expression in the CNS. Eur J Neurosci 2004, 20:467-473. 10.1111/j.1460-9568.2004.03514.x, 15233755.
23. Inoue K, Tsuda M. Microglia and neuropathic pain. Glia 2009, 57:1469-1479. 10.1002/glia.20871, 19306358.
24. Graeber MB, Christie MJ. Multiple mechanisms of microglia: a gatekeeper's contribution to pain states. Exp Neurol 2012, 234:255-261. 10.1016/j.expneurol.2012.01.007, 22273537.
25. Tsuda M, Beggs S, Salter MW, Inoue K. Microglia and intractable chronic pain. Glia 2013, 61:55-61. 10.1002/glia.22379, 22740331.
26. Raghavendra V, Tanga F, DeLeo JA. 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. 10.1124/jpet.103.052407, 12734393.
27. Hanisch UK. Microglia as a source and target of cytokines. Glia 2002, 40:140-155. 10.1002/glia.10161, 12379902.
28. Jana M, Dasgupta S, Saha RN, Liu X, Pahan K. Induction of tumor necrosis factor-alpha (TNF-alpha) by interleukin-12 p40 monomer and homodimer in microglia and macrophages. J Neurochem 2003, 86:519-528. 1955470, 12871593.
29. Ji RR, Suter MR. p38 MAPK, microglial signaling, and neuropathic pain. Mol Pain 2007, 3:33. 10.1186/1744-8069-3-33, 2186318, 17974036.
30. Kawasaki Y, Zhang L, Cheng JK, Ji RR. Cytokine mechanisms of central sensitization: distinct and overlapping role of interleukin-1β, interleukin-6, and tumor necrosis factor-α in regulating synaptic and neuronal activity in the superficial spinal cord. J Neurosci 2008, 28:5189-5194. 10.1523/JNEUROSCI.3338-07.2008, 2408767, 18480275.
31. Zhang L, Berta T, Xu ZZ, Liu T, Park JY, Ji RR. TNF-alpha contributes to spinal cord synaptic plasticity and inflammatory pain: distinct role of TNF receptor subtypes 1 and 2. Pain 2011, 152:419-427. 10.1016/j.pain.2010.11.014, 3022092, 21159431.
32. Zhang J, Shi XQ, Echeverry S, Mogil JS, De Koninck Y, Rivest S. Expression of CCR2 in both resident and bone marrow-derived microglia plays a critical role in neuropathic pain. J Neurosci 2007, 27:12396-12406. 10.1523/JNEUROSCI.3016-07.2007, 17989304.
33. Chen YL, Li AH, Yeh TH, Chou AH, Wang HL. Nocistatin and nociceptin exert opposite effects on the excitability of central amygdala nucleus-periaqueductal gray projection neurons. Mol Cell Neurosci 2009, 40:76-88. 10.1016/j.mcn.2008.09.003, 18930828.
34. Chen YL, Li AH, Yeh TH, Chou AH, Weng YS, Wang HL. Nocistatin excites rostral agranular insular cortex-periaqueductal gray projection neurons by enhancing transient receptor potential cation conductance via G(αq/11)-PLC-protein kinase C pathway. Neurosci 2010, 168:226-239.
35. Ackley MA, Governo RJM, Cass CE, Young JD, Baldwin SA, King AE. Control of glutamatergic neurotransmission in the rat spinal dorsal horn by the nucleoside transporter ENT1. J Physiol 2003, 548:507-517. 10.1113/jphysiol.2002.038091, 2342870, 12611914.
36. Weng HR, Chen JH, Cata JP. Inhibition of glutamate uptake in the spinal cord induces hyperalgesia and increased responses of spinal dorsal horn neurons to peripheral afferent stimulation. Neurosci 2006, 138:1351-1360.
37. Cherney RJ, Mo R, Meyer DT, Nelson DJ, Lo YC, Yang G, Scherle PA, Mandlekar S, Wasserman ZR, Jezak H, Solomon KA, Tebben AJ, Carter PH, Decicco CP. Discovery of disubstituted cyclohexanes as a new class of CC chemokine receptor 2 antagonists. J Med Chem 2008, 51:721-724. 10.1021/jm701488f, 18232650.
38. Tikka TM, Koistinaho JE. Minocycline provides neuroprotection against N-Methyl-D-aspartate neurotoxicity by inhibiting microglia. J Immunol 2001, 166:7527-7533.
39. Tikka T, Fiebch BL. Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J Neurosci 2001, 21:2580-2588.
40. Ledeboer A, Sloane EM, Milligan ED, Frank MG, Mahony JH, Maier SF, Watkins LR. Minocycline attenuates mechanical allodynia and proinflammatory cytokine expression in rat models of pain facilitation. Pain 2005, 115:71-83. 10.1016/j.pain.2005.02.009, 15836971.
41. Hua XY, Svensson CI, Matsui T, Fitzsimmons B, Yaksh TL, Webb M. Intrathecal minocycline attenuates peripheral inflammation-induced hyperalgesia by inhibiting p38 MAPK in spinal microglia. Eur J Neurosci 2005, 22:2431-2440. 10.1111/j.1460-9568.2005.04451.x, 16307586.
42. Takasaki W, Kajino Y, Kajino K, Murali R, Greene MI. Structure based design and characterization of exocyclic peptidomimetics that inhibit TNF alpha binding to its receptor. Nat Biotechnol 1997, 15:1266-1270. 10.1038/nbt1197-1266, 9359109.
43. Sun JH, Yang B, Donnelly DF, Ma C, LaMotte RH. MCP-1 enhances excitability of nociceptive neurons in chronically compressed dorsal root ganglia. J Neurophysiol 2006, 96:2189-2199. 10.1152/jn.00222.2006, 16775210.
44. Menetski J, Mistry S, Lu M, Mudgett JS, Ransohoff RM, Demartino JA, Macintyre DE, Abbadie C. Mice overexpressing chemokine ligand 2 (CCL2) in astrocytes display enhanced nociceptive responses. Neuroscience 2007, 149:706-714. 10.1016/j.neuroscience.2007.08.014, 17870246.
45. Jeon SM, Lee KM, Park ES, Jeon YH, Cho HJ. Monocyte chemoattractant protein-1 immunoreactivity in sensory ganglia and hindpaw after adjuvant injection. Neuroreport 2008, 19:183-186. 10.1097/WNR.0b013e3282f3c781, 18185105.
46. 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.
47. Jung H, Bhangoo S, Banisadr G, Freitag C, Ren D, White FA, Miller RJ. Visualization of chemokine receptor activation in transgenic mice reveals peripheral activation of CCR2 receptors in states of neuropathic pain. J Neurosci 2009, 29:8051-8062. 10.1523/JNEUROSCI.0485-09.2009, 3097108, 19553445.
48. Miller RJ, Jung H, Bhangoo SK, White FA. Cytokine and chemokine regulation of sensory neuron function. Handb Exp Pharmacol 2009, 194:417-449. 10.1007/978-3-540-79090-7_12, 2746245, 19655114.
49. Kao DJ, Li AH, Chen JC, Luo RS, Chen YL, Lu JC, Wang HL. CC chemokine ligand 2 upregulates the current density and expression of TRPV1 channels and Nav1.8 sodium channels in dorsal root ganglion neurons. J Neuroinflammation 2012, 9:189. 10.1186/1742-2094-9-189, 3458897, 22870919.
50. Santos SF, Rebelo S, Derkach VA, Safronov BV. Excitatory interneurons dominate sensory processing in the spinal substantia gelatinosa of rat. J Physiol 2007, 581:241-254. 10.1113/jphysiol.2006.126912, 2075233, 17331995.
51. Akimoto N, Honda K, Uta D, Beppu K, Ushijima Y, Matsuzaki Y, Nakashima S, Kido MA, Imoto K, Takano Y, Noda M. CCL-1 in the spinal cord contributes to neuropathic pain induced by nerve injury. Cell Death Dis 2013, 4:e679. 10.1038/cddis.2013.198, 3702283, 23788036.
52. Narita M, Yoshida T, Nakajima M, Narita M, Miyatake M, Takagi T, Yajima Y, Suzuki T. Direct evidence for spinal cord microglia in the development of a neuropathic pain-like state in mice. J Neurochem 2006, 97:1337-1348. 10.1111/j.1471-4159.2006.03808.x, 16606373.
53. Peters CM, Eisenach JC. Contribution of the chemokine (C-C motif) ligand 2 (CCL2) to mechanical hypersensitivity after surgical incision in rats. Anesthesiol 2010, 112:1250-1258.