Activation of toll like receptor 4 attenuates GABA synthesis and postsynaptic GABA receptor activities in the spinal dorsal horn via releasing interleukin-1 beta

Journal of Neuroinflammation

Volumn 12, Issue 1, 2015, Pages

  Yan, Xisheng ^a,b,c   Jiang, Enshe ^b,d   Weng, Han Rong ^a,b  

^a UNIVERSITY OF GEORGIA   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c TONGREN HOSPITAL OF WUHAN UNIVERSITY   (China)

^d HENAN UNIVERSITY   (China)

Author keywords

Cytokines; GLT 1; Neuroinflammation; Nociception

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; GLUTAMATE TRANSPORTER; GLUTAMIC ACID; GLUTAMINE; INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; PROTEIN KINASE C; TOLL LIKE RECEPTOR 4; AMINO ACID RECEPTOR AFFECTING AGENT; ENZYME INHIBITOR; GABAERGIC RECEPTOR AFFECTING AGENT; GLIAL FIBRILLARY ACIDIC PROTEIN; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; MINOCYCLINE;

4 AMINOBUTYRIC ACID METABOLISM; ADULT; AMINO ACID DEFICIENCY; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME ACTIVATION; GABAERGIC SYSTEM; GABAERGIC TRANSMISSION; GLIA CELL; INHIBITORY POSTSYNAPTIC POTENTIAL; MALE; NERVE CELL PLASTICITY; NERVE FUNCTION; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PAIN; RAT; RECEPTOR UPREGULATION; SPINAL CORD DORSAL HORN; YOUNG ADULT; ANIMAL; CYTOLOGY; DRUG EFFECTS; GENETICS; METABOLISM; PHYSIOLOGY; SPRAGUE DAWLEY RAT; TRANSGENIC RAT;

AMINO ACID TRANSPORT SYSTEM X-AG; ANIMALS; ASTROCYTES; ENZYME INHIBITORS; EXCITATORY AMINO ACID AGENTS; GABA AGENTS; GAMMA-AMINOBUTYRIC ACID; GLIAL FIBRILLARY ACIDIC PROTEIN; INHIBITORY POSTSYNAPTIC POTENTIALS; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; INTERLEUKIN-1BETA; LIPOPOLYSACCHARIDES; MALE; MINOCYCLINE; RATS; RATS, SPRAGUE-DAWLEY; RATS, TRANSGENIC; RECEPTORS, GABA; SPINAL CORD DORSAL HORN; TOLL-LIKE RECEPTOR 4;

EID: 84924901925     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/s12974-014-0222-3     Document Type: Article

References (77)

1. Lehnardt S, Lachance C, Patrizi S, Lefebvre S, Follett PL, Jensen FE, et al. The toll-like receptor TLR4 is necessary for lipopolysaccharide-induced oligodendrocyte injury in the CNS. J Neurosci. 2002;22:2478-86.
2. Olson JK, Miller SD. Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs. J Immunol. 2004;173:3916-24.
3. Bettoni I, Comelli F, Rossini C, Granucci F, Giagnoni G, Peri F, et al. Glial TLR4 receptor as new target to treat neuropathic pain: efficacy of a new receptor antagonist in a model of peripheral nerve injury in mice. Glia. 2008;56:1312-9.
4. Tanga FY, Nutile-McMenemy N, DeLeo JA. The CNS role of Toll-like receptor 4 in innate neuroimmunity and painful neuropathy. Proc Natl Acad Sci U S A. 2005;102:5856-61.
5. Wu FX, Bian JJ, Miao XR, Huang SD, Xu XW, Gong DJ, et al. Intrathecal siRNA against Toll-like receptor 4 reduces nociception in a rat model of neuropathic pain. Int J Med Sci. 2010;7:251-9.
6. Li X, Wang XW, Feng XM, Zhou WJ, Wang YQ, Mao-Ying QL. Stage-dependent anti-allodynic effects of intrathecal Toll-like receptor 4 antagonists in a rat model of cancer induced bone pain. J Physiol Sci. 2013;63:203-9.
7. Sorge RE, LaCroix-Fralish ML, Tuttle AH, Sotocinal SG, Austin JS, Ritchie J, et al. Spinal cord Toll-like receptor 4 mediates inflammatory and neuropathic hypersensitivity in male but not female mice. J Neurosci. 2011;31:15450-4.
8. Hutchinson MR, Zhang Y, Shridhar M, Evans JH, Buchanan MM, Zhao TX, et al. Evidence that opioids may have toll-like receptor 4 and MD-2 effects. Brain Behav Immun. 2010;24:83-95.
9. Basbaum AI, Bautista DM, Scherrer G, Julius D. Cellular and molecular mechanisms of pain. Cell. 2009;139:267-84.
10. Tsantoulas C, McMahon SB. Opening paths to novel analgesics: the role of potassium channels in chronic pain. Trends Neurosci. 2014;37:146-58.
11. Woolf CJ. Central sensitization: implications for the diagnosis and treatment of pain. Pain. 2011;152:S2-15.
12. Bardoni R, Takazawa T, Tong CK, Choudhury P, Scherrer G, Macdermott AB. Pre- and postsynaptic inhibitory control in the spinal cord dorsal horn. Ann N Y Acad Sci. 2013;1279:90-6.
13. Yaksh TL. Behavioral and autonomic correlates of the tactile evoked allodynia produced by a spinal glycine inhibition:effects of modulatory receptor systems and excitatory amino acid antagonists. Pain. 1989;37:111-23.
14. Coull JAM, Boudreau D, Bachand K, Prescott SA, Nault F, Sik A, et al. Trans-synaptic shift in anion gradient in spinal lamina I neurons as a mechanism of neuropathic pain. Nature. 2003;424:938-42.
15. Moore KA, Kohno T, Karchewski LA, Scholz J, Baba H, Woolf CJ. Partial peripheral nerve injury promotes a selective loss of GABAergic inhibition in the superficial dorsal horn of the spinal cord. J Neurosci. 2002;22:6724-31.
16. Bak LK, Schousboe A, Waagepetersen HS. The glutamate/GABA-glutamine cycle: aspects of transport, neurotransmitter homeostasis and ammonia transfer. J Neurochem. 2006;98:641-53.
17. Mathews GC, Diamond JS. Neuronal glutamate uptake contributes to GABA synthesis and inhibitory synaptic strength. J Neurosci. 2003;23:2040-8.
18. Liang SL, Carlson GC, Coulter DA. Dynamic regulation of synaptic GABA release by the glutamate-glutamine cycle in hippocampal area CA1. J Neurosci. 2006;26:8537-48.
19. Ortinski PI, Dong J, Mungenast A, Yue C, Takano H, Watson DJ, et al. Selective induction of astrocytic gliosis generates deficits in neuronal inhibition. Nat Neurosci. 2010;13:584-91.
20. Jiang E, Yan X, Weng HR. Glial glutamate transporter and glutamine synthetase regulate GABAergic synaptic strength in the spinal dorsal horn. J Neurochem. 2012;121:526-36.
21. Weng HR, Chen JH, Pan ZZ, Nie H. Glial glutamate transporter 1 regulates the spatial and temporal coding of glutamatergic synaptic transmission in spinal lamina II neurons. Neuroscience. 2007;149:898-907.
22. Yang K, Fujita T, Kumamoto E. Adenosine inhibits GABAergic and glycinergic transmission in adult rat substantia gelatinosa neurons. J Neurophysiol. 2004;92:2867-77.
23. 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.
24. Nie H, Weng HR. Glutamate transporters prevent excessive activation of NMDA receptors and extrasynaptic glutamate spillover in the spinal dorsal horn. J Neurophysiol. 2009;101:2041-51.
25. Yan X, Yadav R, Gao M, Weng HR. Interleukin-1 beta enhances endocytosis of glial glutamate transporters in the spinal dorsal horn through activating protein kinase C. Glia. 2014;62:1093-109.
26. Pascual O, Ben Achour S, Rostaing P, Triller A, Bessis A. Microglia activation triggers astrocyte-mediated modulation of excitatory neurotransmission. Proc Natl Acad Sci U S A. 2012;109:E197-205.
27. Clark AK, Staniland AA, Marchand F, Kaan TK, McMahon SB, Malcangio M. P2X7-dependent release of interleukin-1beta and nociception in the spinal cord following lipopolysaccharide. J Neurosci. 2010;30:573-82.
28. Nikodemova M, Watters JJ, Jackson SJ, Yang SK, Duncan ID. Minocycline down-regulates MHC II expression in microglia and macrophages through inhibition of IRF-1 and protein kinase C (PKC)alpha/betaII. J Biol Chem. 2007;282:15208-16.
29. Zink MC, Uhrlaub J, DeWitt J, Voelker T, Bullock B, Mankowski J, et al. Neuroprotective and anti-human immunodeficiency virus activity of minocycline. JAMA. 2005;293:2003-11.
30. Pang T, Wang J, Benicky J, Saavedra JM. Minocycline ameliorates LPS-induced inflammation in human monocytes by novel mechanisms including LOX-1, Nur77 and LITAF inhibition. Biochim Biophys Acta. 2012;1820:503-10.
31. Gruber-Schoffnegger D, Drdla-Schutting R, Honigsperger C, Wunderbaldinger G, Gassner M, Sandkuhler J. Induction of thermal hyperalgesia and synaptic long-term potentiation in the spinal cord lamina I by TNF-alpha and IL-1beta is mediated by glial cells. J Neurosci. 2013;33:6540-51.
32. Cho IH, Lee MJ, Jang M, Gwak NG, Lee KY, Jung HS. Minocycline markedly reduces acute visceral nociception via inhibiting neuronal ERK phosphorylation. Mol Pain. 2012;8:13.
33. Zhang RX, Li A, Liu B, Wang L, Ren K, Zhang H, et al. IL-1ra alleviates inflammatory hyperalgesia through preventing phosphorylation of NMDA receptor NR-1 subunit in rats. Pain. 2008;135:232-9.
34. Kawasaki Y, Zhang L, Cheng JK, Ji RR. Cytokine mechanisms of central sensitization: distinct and overlapping role of interleukin-1beta, interleukin-6, and tumor necrosis factor-alpha in regulating synaptic and neuronal activity in the superficial spinal cord. J Neurosci. 2008;28:5189-94.
35. Kohno T, Wang H, Amaya F, Brenner GJ, Cheng JK, Ji RR, et al. Bradykinin enhances AMPA and NMDA receptor activity in spinal cord dorsal horn neurons by activating multiple kinases to produce pain hypersensitivity. J Neurosci. 2008;28:4533-40.
36. Juge N, Gray JA, Omote H, Miyaji T, Inoue T, Hara C, et al. Metabolic control of vesicular glutamate transport and release. Neuron. 2010;68:99-112.
37. Zhou Q, Petersen CC, Nicoll RA. Effects of reduced vesicular filling on synaptic transmission in rat hippocampal neurones. J Physiol. 2000;525(Pt 1):195-206.
38. Zucker RS. Short-term synaptic plasticity. Annu Rev Neurosci. 1989;12:13-31.
39. Manabe T, Wyllie DJ, Perkel DJ, Nicoll RA. Modulation of synaptic transmission and long-term potentiation: effects on paired pulse facilitation and EPSC variance in the CA1 region of the hippocampus. J Neurophysiol. 1993;70:1451-9.
40. Foster TC, McNaughton BL. Long-term enhancement of CA1 synaptic transmission is due to increased quantal size, not quantal content. Hippocampus. 1991;1:79-91.
41. Xu H, Wu LJ, Wang H, Zhang X, Vadakkan KI, Kim SS, et al. Presynaptic and postsynaptic amplifications of neuropathic pain in the anterior cingulate cortex. J Neurosci. 2008;28:7445-53.
42. Ingram RA, Fitzgerald M, Baccei ML. Developmental changes in the fidelity and short-term plasticity of GABAergic synapses in the neonatal rat dorsal horn. J Neurophysiol. 2008;99:3144-50.
43. Levy LM, Warr O, Attwell D. Stoichiometry of the glial glutamate transporter GLT-1 expressed inducibly in a Chinese hamster ovary cell line selected for low endogenous Na+-dependent glutamate uptake. J Neurosci. 1998;18:9620-8.
44. Wadiche JI, Arriza JL, Amara SG, Kavanaugh MP. Kinetics of a human glutamate transporter. Neuron. 1995;14:1019-27.
45. Tegeder I, Adolph J, Schmidt H, Woolf CJ, Geisslinger G, Lotsch J. Reduced hyperalgesia in homozygous carriers of a GTP cyclohydrolase 1 haplotype. Eur J Pain. 2008;12:1069-77.
46. Zhang HJ, Xin WJ, Dougherty PM. Synaptically evoked glutamate transporter currents in spinal dorsal horn astrocytes. Molecular Pain. 2009;5:36.
47. Adolph O, Koster S, Rath M, Georgieff M, Weigt HU, Engele J, et al. Rapid increase of glial glutamate uptake via blockade of the protein kinase A pathway. GLIA. 2007;55:1699-707.
48. Bergles DE, Jahr CE. Synaptic activation of glutamate transporters in hippocampal astrocytes. Neuron. 1997;19:1297-308.
49. Fang H, Huang Y, Zuo Z. The different responses of rat glutamate transporter type 2 and its mutant (tyrosine 403 to histidine) activity to volatile anesthetics and activation of protein kinase C. Brain Res. 2002;953:255-64.
50. Wadiche JI, Jahr CE. Multivesicular release at climbing fiber-Purkinje cell synapses. Neuron. 2001;32:301-13.
51. Nicotra L, Loram LC, Watkins LR, Hutchinson MR. Toll-like receptors in chronic pain. Exp Neurol. 2012;234:316-29.
52. Ren K, Dubner R. Interactions between the immune and nervous systems in pain. Nat Med. 2010;16:1267-76.
53. Grace PM, Hutchinson MR, Maier SF, Watkins LR. Pathological pain and the neuroimmune interface. Nat Rev Immunol. 2014;14:217-31.
54. Cao L, Tanga FY, Deleo JA. The contributing role of CD14 in toll-like receptor 4 dependent neuropathic pain. Neuroscience. 2009;158:896-903.
55. Hutchinson MR, Zhang Y, Brown K, Coats BD, Shridhar M, Sholar PW, et al. Non-stereoselective reversal of neuropathic pain by naloxone and naltrexone: involvement of toll-like receptor 4 (TLR4). Eur J Neurosci. 2008;28:20-9.
56. Christianson CA, Dumlao DS, Stokes JA, Dennis EA, Svensson CI, Corr M, et al. Spinal TLR4 mediates the transition to a persistent mechanical hypersensitivity after the resolution of inflammation in serum-transferred arthritis. Pain. 2011;152:2881-91.
57. Saito O, Svensson CI, Buczynski MW, Wegner K, Hua XY, Codeluppi S, et al. Spinal glial TLR4-mediated nociception and production of prostaglandin E(2) and TNF. Br J Pharmacol. 2010;160:1754-64.
58. Yoon SY, Patel D, Dougherty PM. Minocycline blocks lipopolysaccharide induced hyperalgesia by suppression of microglia but not astrocytes. Neuroscience. 2012;221:214-24.
59. Yan X, Weng HR. Endogenous interleukin-1b in neuropathic rats enhances glutamate release from the primary afferents in the spinal dorsal horn through coupling with presynaptic NMDA receptors. J Biol Chem. 2013;288:30544-57.
60. Danbolt NC. Glutamate uptake. Prog Neurobiol. 2001;65:1-105.
61. Milligan ED, Watkins LR. Pathological and protective roles of glia in chronic pain. Nat Rev Neurosci. 2009;10:23-36.
62. Tanaka K, Watase K, Manabe T, Yamada K, Watanabe M, Takahashi K, et al. Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science. 1997;276:1699-702.
63. Doyle T, Chen Z, Muscoli C, Bryant L, Esposito E, Cuzzocrea S, et al. Targeting the overproduction of peroxynitrite for the prevention and reversal of paclitaxel-induced neuropathic pain. J Neurosci. 2012;32:6149-60.
64. Nie H, Weng HR. Impaired glial glutamate uptake induces extrasynaptic glutamate spillover in the spinal sensory synapses of neuropathic rats. J Neurophysiol. 2010;103:2570-80.
65. Nie H, Zhang H, Weng HR. Minocycline prevents impaired glial glutamate uptake in the spinal sensory synapses of neuropathic rats. Neuroscience. 2010;170:901-12.
66. Sung B, Lim G, Mao J. Altered expression and uptake activity of spinal glutamate transporters after nerve injury contribute to the pathogenesis of neuropathic pain in rats. J Neurosci. 2003;23:2899-910.
67. 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. Neuroscience. 2006;138:1351-60.
68. Liaw WJ, Stephens Jr RL, Binns BC, Chu Y, Sepkuty JP, Johns RA, et al. Spinal glutamate uptake is critical for maintaining normal sensory transmission in rat spinal cord. Pain. 2005;115:60-70.
69. Sung B, Wang S, Zhou B, Lim G, Yang L, Zeng Q, et al. Altered spinal arachidonic acid turnover after peripheral nerve injury regulates regional glutamate concentration and neuropathic pain behaviors in rats. Pain. 2007;131:121-31.
70. Tawfik VL, Regan MR, Haenggeli C, Lacroix-Fralish ML, Nutile-McMenemy N, Perez N, et al. Propentofylline-induced astrocyte modulation leads to alterations in glial glutamate promoter activation following spinal nerve transection. Neuroscience. 2008;152:1086-92.
71. Gao M, Yan X, Weng HR. Inhibition of glycogen synthase kinase 3beta activity with lithium prevents and attenuates paclitaxel-induced neuropathic pain. Neuroscience. 2013;254:301-11.
72. Weng HR, Gao M, Maixner DW. Glycogen synthase kinase 3 beta regulates glial glutamate transporter protein expression in the spinal dorsal horn in rats with neuropathic pain. Exp Neurol. 2014;252:18-27.
73. Stiller CO, Cui JG, O'Connor WT, Brodin E, Meyerson BA, Linderoth B. Release of y-aminobutyric acid in the dorsal horn and suppression of tactile alloydynia by spinal cord stimulation in mononeuropathic rats. Neurosurgery. 1996;39:367-74.
74. Malan TP, Mata HP, Porreca F. Spinal GABA A and GABA B receptor pharmacology in a model of neuropathic pain. Anesthesiology. 2002;96:1161-7.
75. Hugel S, Schlichter R. Convergent control of synaptic GABA release from rat dorsal horn neurones by adenosine and GABA autoreceptors. J Physiol. 2003;551:479-89.
76. Takeda D, Nakatsuka T, Papke R, Gu JG. Modulation of inhibitory synaptic activity by a non-alpha4beta2, non-alpha7 subtype of nicotinic receptors in the substantia gelatinosa of adult rat spinal cord. Pain. 2003;101:13-23.
77. Zhang HM, Chen SR, Matsui M, Gautam D, Wess J, Pan HL. Opposing functions of spinal M2, M3, and M4 receptor subtypes in regulation of GABAergic inputs to dorsal horn neurons revealed by muscarinic receptor knockout mice. Mol Pharmacol. 2006;69:1048-55.