The upregulation of translocator protein (18 kDa) promotes recovery from neuropathic pain in rats

Journal of Neuroscience

Volumn 33, Issue 4, 2013, Pages 1540-1551

  Wei, Xu Hong ^a   Wei, Xiao ^a   Chen, Feng Ying ^b   Zang, Ying ^a   Xin, Wen Jun ^a   Pang, Rui Ping ^a   Chen, Yuan ^a   Wang, Jun ^a   Li, Yong Yong ^a   Shen, Kai Feng ^a   Zhou, Li Jun ^a   Liu, Xian Guo ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b SUN YAT SEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

4' CHLORODIAZEPAM; AMINOGLUTETHIMIDE DERIVATIVE; CARRIER PROTEIN; TOLL LIKE RECEPTOR 4; TRANSLOCATOR PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ALLODYNIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BEHAVIOR; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; HYPERALGESIA; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; MALE; MICROGLIA; NEUROPATHIC PAIN; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL NERVE; UPREGULATION; WESTERN BLOTTING;

ANIMALS; ASTROCYTES; BLOTTING, WESTERN; CARRIER PROTEINS; CELLS, CULTURED; COCULTURE TECHNIQUES; ENZYME-LINKED IMMUNOSORBENT ASSAY; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; MALE; NEURALGIA; NEUROGLIA; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; SPINAL NERVES; UP-REGULATION;

EID: 84872694582     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0324-12.2013     Document Type: Article

References (71)

1. Agnello D., Carvelli L, Muzio V, Villa P, Bottazzi B, Polentarutti N, Mennini T, Mantovani A., Ghezzi P. (2000). Increased peripheral benzodiazepine binding sites and pentraxin 3 expression in the spinal cord during EAE: relation to inflammatory cytokines and modulation by dexamethasone and rolipram. J Neuroimmunol 109:105-111. Medline
2. Akira S., Uematsu S, Takeuchi O. (2006). Pathogen recognition and innate immunity. Cell 124:783-801. CrossRef Medline
3. Aouad M., Charlet A, Rodeau JL, Poisbeau P. (2009). Reduction and prevention of vincristine-induced neuropathic pain symptoms by the nonbenzodiazepine anxiolytic etifoxine are mediated by 3alpha-reduced neurosteroids. Pain 147:54-59 CrossRef Medline
4. Basbaum AI. (1999). Distinct neurochemical features of acute and persistent pain. Proc Natl Acad Sci U S A 96:7739-7743. CrossRef Medline
5. Basile AS., Skolnick P. (1986). Subcellular localization of "peripheral-type" binding sites for benzodiazepines in rat brain. J Neurochem 46:305-308. CrossRef Medline
6. Bettoni I., Comelli F, Rossini C, Granucci F, Giagnoni G, Peri F, Costa B (2008) 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 56:1312-1319. CrossRef Medline
7. Blanco AM., Guerri C. (2007). Ethanol intake enhances inflammatory mediators in brain: role of glial cells and TLR4/IL-1RI receptors. Front Biosci 12:2616-2630. CrossRef Medline
8. Bordet T., Buisson B, Michaud M, Drouot C, Galéa P, Delaage P, Akentieva NP, Evers AS, Covey DF, Ostuni MA, Lacaperè JJ, Massaad C, Schumacher M, Steidl EM, Maux D, Delaage M, Henderson CE, Pruss RM (2007) Identification and characterization of cholest-4-en-3-one, oxime (TRO19622), a novel drug candidate for amyotrophic lateral sclerosis. J Pharmacol Exp Ther 322: 709-720. CrossRef Medline
9. Bordet T., Buisson B, Michaud M, Abitbol JL, Marchand F, Grist J, Andriambeloson E, Malcangio M, Pruss RM. (2008). Specific antinociceptive activity of cholest-4-en-3-one, oxime (TRO19622) in experimental models of painful diabetic and chemotherapy-induced neuropathy. J Pharmacol Exp Ther 326:623-632. CrossRef Medline
10. Buchanan PJ., Ernst RK, Elborn JS, Schock B. (2009). Role of CFTR, Pseudomonas aeruginosa and Toll-like receptors in cystic fibrosis lung inflammation. Biochem Soc Trans 37:863-867. CrossRef Medline
11. Chaplan SR., Bach FW, Pogrel JW, Chung JM, Yaksh TL. (1994). Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53:55-63. CrossRef Medline
12. Charalampopoulos I., Alexaki VI, Tsatsanis C, Minas V, Dermitzaki E, Lasaridis I, Vardouli L, Stournaras C, Margioris AN, Castanas E, Gravanis A (2006) Neurosteroids as endogenous inhibitors of neuronal cell apoptosis in aging. Ann N Y Acad Sci 1088:139-152. CrossRef Medline
13. Charlet A., Lasbennes F, Darbon P, Poisbeau P. (2008). Fast non-genomic effects of progesterone-derived neurosteroids on nociceptive thresholds and pain symptoms. Pain 139:603-609. CrossRef Medline
14. Chen X., Pang RP, Shen KF, Zimmermann M, Xin WJ, Li YY, Liu XG. (2011). TNF-alpha enhances the currents of voltage gated sodium channels in uninjured dorsal root ganglion neurons following motor nerve injury. Exp Neurol 227:279-286. CrossRef Medline
15. Clark AK., D'Aquisto F, Gentry C, Marchand F, McMahon SB, Malcangio M (2006) Rapid co-release of interleukin 1beta and caspase 1 in spinal cord inflammation. J Neurochem 99:868-880. CrossRef Medline
16. Cosentino M., Marino F, Cattaneo S, Di Grazia L, Francioli C, Fietta AM, Lecchini S., Frigo G. (2000). Diazepam-binding inhibitor-derived peptides induce intracellular calcium changes and modulate human neutrophil function. J Leukoc Biol 67:637-643. Medline
17. Culty M., Li H, Boujrad N, Amri H, Vidic B, Bernassau JM, Reversat JL, Papadopoulos V. (1999). In vitro studies on the role of the peripheraltype benzodiazepine receptor in steroidogenesis. J Steroid Biochem Mol Biol 69:123-130. CrossRef Medline
18. Cummins TR., Sheets PL, Waxman SG. (2007). The roles of sodium channels in nociception: implications for mechanisms of pain. Pain 131:243-257. CrossRef Medline
19. DalB ó S, Nardi GM, Ferrara P, Ribeiro-do-Valle RM, Farges RC. (2004). Antinociceptive effects of peripheral benzodiazepine receptors. Pharmacology 70:188-194. CrossRef Medline
20. Denkers EY., Butcher BA, Del Rio L, Kim L. (2004). Manipulation of mitogen-activated protein kinase/nuclear factor-kappaB-signaling cascades during intracellular Toxoplasma gondii infection. Immunol Rev 201:191-205. CrossRef Medline
21. Eschenfelder S., Häbler HJ, JänigW. (2000). Dorsal root section elicits signs of neuropathic pain rather than reversing them in rats with L5 spinal nerve injury. Pain 87:213-219. CrossRef Medline
22. Eser D., Baghai TC, Schüle C, Nothdurfter C, Rupprecht R. (2008). Neuroactive steroids as endogenous modulators of anxiety. Curr Pharm Des 14: 3525-3533. CrossRef Medline
23. French JF., Matlib MA. (1988). Identification of a high-affinity peripheraltype benzodiazepine binding site in rat aortic smooth muscle membranes. J Pharmacol Exp Ther 247:23-28. Medline
24. Garnier M., Boujrad N, Oke BO, Brown AS, Riond J, Ferrara P, Shoyab M, Suarez-Quian CA, Papadopoulos V. (1993). Diazepam binding inhibitor is a paracrine/autocrine regulator of Leydig cell proliferation and steroidogenesis: action via peripheral-type benzodiazepine receptor and independent mechanisms. Endocrinology 132:444-458. CrossRef Medline
25. Giatti S., Pesaresi M, Cavaletti G, Bianchi R, Carozzi V, Lombardi R, Maschi O, Lauria G, Garcia-Segura LM, Caruso D, Melcangi RC. (2009). Neuroprotective effects of a ligand of translocator protein-18 kDa (Ro5-4864) in experimental diabetic neuropathy. Neuroscience 164:520-529. CrossRef Medline
26. Hardwick M., Fertikh D, Culty M, Li H, Vidic B, Papadopoulos V. (1999). Peripheral-type benzodiazepine receptor (PBR) in human breast cancer: correlation of breast cancer cell aggressive phenotype with PBR expression, nuclear localization, and PBR-mediated cell proliferation and nuclear transport of cholesterol. Cancer Res 59:831-842. Medline
27. Hargreaves K., Dubner R, Brown F, Flores C, Joris J. (1988). A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32:77-88. CrossRef Medline
28. Hernstadt H., Wang S, Lim G, Mao J. (2009). Spinal translocator protein (TSPO) modulates pain behavior in rats with CFA-induced monoarthritis. Brain Res 1286:42-52. CrossRef Medline
29. Hoeger-Bement MK, Sluka KA. (2003). Phosphorylation of CREB and mechanical hyperalgesia is reversed by blockade of the cAMP pathway in a time-dependent manner after repeated intramuscular acid injections. J Neurosci 23:5437-5445. Medline
30. Hsieh HL., Wang HH, Wu CY, Jou MJ, Yen MH, Parker P, Yang CM. (2007). BK-induced COX-2 expression via PKC-delta-dependent activation of p42/p44 MAPK and NF-kappaB in astrocytes. Cell Signal 19:330-340. CrossRef Medline
31. Janeway CA Jr, Medzhitov R. (2002). Innate immune recognition. Annu Rev Immunol 20:197-216. CrossRef Medline
32. Jiang C., Cui K, Wang J, He Y. (2011). Microglia and cyclooxygenase-2: possible therapeutic targets of progesterone for stroke. Int Immunopharmacol 11:1925-1931. CrossRef Medline
33. Jin SX., Zhuang ZY, Woolf CJ, Ji RR. (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 23:4017-4022. Medline
34. Kawasaki Y., Zhang L, Cheng JK, Ji RR. (2008). 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 28:5189-5194. Medline
35. Kim SH., Chung JM. (1992). An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 50:355-363. CrossRef Medline
36. Malayev A., Gibbs TT, FarbDH. (2002). Inhibition of theNMDAresponse by pregnenolone sulphate reveals subtype selective modulation of NMDA receptors by sulphated steroids. Br J Pharmacol 135:901-909. CrossRef Medline
37. Marino F., Cattaneo S, Cosentino M, Rasini E, Di Grazia L, Fietta AM, Lecchini S, Frigo G. (2001). Diazepam stimulates migration and phagocytosis of human neutrophils: possible contribution of peripheral-type benzodiazepine receptors and intracellular calcium. Pharmacology 63: 42-49. CrossRef Medline
38. Niederberger E., Geisslinger G. (2008). Proteomics in neuropathic pain research. Anesthesiology 108:314-323. CrossRef Medline
39. Nothdurfter C., Baghai TC, Schüle C, Rupprecht R. (2012). Translocator protein (18 kDa) (TSPO) as a therapeutic target for anxiety and neurologic disorders. Eur Arch Psychiatry Clin Neurosci 262 Suppl 2:S10-S112. CrossRef Medline
40. O'Beirne GB, Woods MJ, WilliamsDC. (1990). Two subcellular locations for peripheral-type benzodiazepine acceptors in rat liver. Eur J Biochem 188: 131-138. CrossRef Medline
41. Oh YJ., Francis JW, Markelonis GJ, Oh TH. (1992). Interleukin-1-beta and tumor necrosis factor-alpha increase peripheral-type benzodiazepine binding sites in cultured polygonal astrocytes. J Neurochem 58:2131-2138. CrossRef Medline
42. Oke BO., Suarez-Quian CA, Riond J, Ferrara P, Papadopoulos V. (1992). Cell surface localization of the peripheral-type benzodiazepine receptor (PBR) in adrenal cortex. Mol Cell Endocrinol 87: R1-R6. CrossRef Medline
43. Papadopoulos V., Baraldi M, Guilarte TR, Knudsen TB, Lacapère JJ, Lindemann P, Norenberg MD, Nutt D, Weizman A, Zhang MR, Gavish M (2006) Translocator protein (18kDa): new nomenclature for the peripheral-type benzodiazepine receptor based on its structure and molecular function. Trends Pharmacol Sci 27:402-409. CrossRef Medline
44. Rey C., Mauduit C, Naureils O, Benahmed M, Louisot P, Gasnier F. (2000). Upregul ation of mitochondrial peripheral benzodiazepine receptor expression by tumor necrosis factor alpha in testicular leydig cells. Possible involvement in cell survival. Biochem Pharmacol 60:1639-1646. Medline
45. Ringkamp M., Grethel EJ, Choi Y, Meyer RA, Raja SN. (1999). Mechanical hyperalgesia after spinal nerve ligation in rat is not reversed by intraplantar or systemic administration of adrenergic antagonists. Pain 79:135-141. Medline
46. Romero-Sandoval A, Chai N, Nutile-McMenemy N, Deleo JA. (2008a). A comparison of spinal Iba1 and GFAP expression in rodent models of acute and chronic pain. Brain Res 1219:116-126. CrossRef Medline
47. Romero-Sandoval A, Nutile-McMenemy N, DeLeo JA. (2008b). Spinal microglial and perivascular cell cannabinoid receptor type 2 activation reduces behavioral hypersensitivity without tolerance after peripheral nerve injury. Anesthesiology 108:722-734. CrossRef Medline
48. Ruff MR., Pert CB, Weber RJ, Wahl LM, Wahl SM, Paul SM. (1985). Benzodiazepine receptor-mediated chemotaxis of human monocytes. Science 229:1281-1283. CrossRef Medline
49. Rupprecht R., Papadopoulos V, Rammes G, Baghai TC, Fan J, Akula N, Groyer G., Adams D, Schumacher M. (2010). Translocator protein (18 kDa) (TSPO) as a therapeutic target for neurological and psychiatric disorders. Nat Rev Drug Discov 9:971-988. CrossRef Medline
50. Sakai M., Fonseca ES, Dagli ML, Palermo-Neto J. (2006). Diazepam effects on Ehrlich tumor growth and macrophage activity in mice. Life Sci 78:1777-1783. CrossRef Medline
51. Schüle C, Eser D, Baghai TC, Nothdurfter C, Kessler JS, Rupprecht R. (2011). Neuroactive steroids in affective disorders: target for novel antidepressant or anxiolytic drugs? Neuroscience 191:55-77. CrossRef Medline
52. Scuteri A., Galimberti A, Maggioni D, Ravasi M, Pasini S, Nicolini G, Bossi M, Miloso M., Cavaletti G, Tredici G. (2009). Role of MAPKs in platinuminduced neuronal apoptosis. Neurotoxicology 30:312-319. CrossRef Medline
53. Shoshan-Barmatz V, Ben-Hail D. (2012). VDAC, a multi-functional mitochondrial protein as a pharmacological target. Mitochondrion 12:24-34. CrossRef Medline
54. Siniscalco D., Fuccio C, Giordano C, Ferraraccio F, Palazzo E, Luongo L, Rossi F, Roth KA, Maione S, de Novellis V. (2007). Role of reactive oxygen species and spinal cord apoptotic genes in the development of neuropathic pain. Pharmacol Res 55:158-166. CrossRef Medline
55. Srinivasan S., Stevens M, Wiley JW. (2000). Diabetic peripheral neuropathy: evidence for apoptosis and associated mitochondrial dysfunction. Diabetes 49:1932-1938. CrossRef Medline
56. Tegeder I., Niederberger E, Schmidt R, Kunz S, Gühring H, Ritzeler O, Michaelis M, Geisslinger G. (2004). Specific Inhibition of IkappaB kinase reduces hyperalgesia in inflammatory and neuropathic pain models in rats. J Neurosci 24:1637-1645. CrossRef Medline
57. Tsuda M., Inoue K, Salter MW. (2005). Neuropathic pain and spinal microglia: a big problem from molecules in "small" glia. Trends Neurosci 28: 101-107. CrossRef Medline
58. Veiga S., Azcoitia I, Garcia-Segura LM. (2005). Ro5-4864, a peripheral benzodiazepine receptor ligand, reduces reactive gliosis and protects hippocampal hilar neurons from kainic acid excitotoxicity. J Neurosci Res 80:129-137. CrossRef Medline
59. Villalba M., Hott M, Martin C, Aguila B, Valdivia S, Quezada C, Zambrano A, Concha MI., Otth C. (2012). Herpes simplex virus type 1 induces simultaneous activation of Toll-like receptors 2 and 4 and expression of the endogenous ligand serum amyloidAin astrocytes. Med Microbiol Immunol 201:371-379. CrossRef Medline
60. Vowinckel E., Reutens D, Becher B, Verge G, Evans A, Owens T, Antel JP (1997) PK11195 binding to the peripheral benzodiazepine receptor as a marker of microglia activation in multiple sclerosis and experimental autoimmune encephalomyelitis. J Neurosci Res 50:345-353. CrossRef Medline
61. Warf BC., Fok-Seang J, Miller RH. (1991). Evidence for the ventral origin of oligodendrocyte precursors in the rat spinal cord. J Neurosci 11: 2477-2488. Medline
62. Watkins LR., Maier SF. (2003). Glia: a novel drug discovery target for clinical pain. Nat Rev Drug Discov 2:973-985. CrossRef Medline
63. Wei XH., Zang Y, WuCY, Xu JT, Xin WJ, Liu XG. (2007). Peri-sciatic administration of recombinant rat TNF-alpha induces mechanical allodynia via upregulation of TNF-alpha in dorsal root ganglia and in spinal dorsal horn: the role of NF-kappa B pathway. Exp Neurol 205:471-484. CrossRef Medline
64. Yasuno F., Ota M, Kosaka J, Ito H, Higuchi M, Doronbekov TK, Nozaki S, Fujimura Y., Koeda M, Asada T, Suhara T. (2008). Increased binding of peripheral benzodiazepine receptor in Alzheimer's disease measured by positron emission tomography with [11C]DAA1106. Biol Psychiatry 64: 835-841. Medline
65. Zang Y., He XH, Xin WJ, Pang RP, Wei XH, Zhou LJ, Li YY, Liu XG. (2010). Inhibition of NF-kappaB prevents mechanical allodynia induced by spinal ventral root transection and suppresses the re-expression of Nav1.3 in DRG neurons in vivo and in vitro. Brain Res 1363:151-158. CrossRef Medline
66. Zhang X., Neufeld AH. (2007). Signal transduction pathways for epidermal growth factor stimulated cyclooxygenase-2 induction in astrocytes. Exp Eye Res 85:280-288. CrossRef Medline
67. Zhao P., Waxman SG, Hains BC. (2007). Extracellular signal-regulated kinase-regulated microglia-neuron signaling by prostaglandin E2 contributes to pain after spinal cord injury. J Neurosci 27:2357-2368. CrossRef Medline
68. Zhou LJ., Yang T, Wei X, Liu Y, Xin WJ, Chen Y, Pang RP, Zang Y, Li YY, Liu XG. (2011). Brain-derived neurotrophic factor contributes to spinal long-term potentiation and mechanical hypersensitivity by activation of spinal microglia in rat. Brain Behav Immun 25:322-334. CrossRef Medline
69. Zhuang ZY., Gerner P, Woolf CJ, Ji RR. (2005). ERK is sequentially activated in neurons, microglia, and astrocytes by spinal nerve ligation and contributes to mechanical allodynia in this neuropathic pain model. Pain 114: 149-159. CrossRef Medline
70. Zhuang ZY., Wen YR, Zhang DR, Borsello T, Bonny C, Strichartz GR, Decosterd I., Ji RR. (2006). A peptide c-Jun N-terminal kinase (JNK) inhibitor blocks mechanical allodynia after spinal nerve ligation: respective roles of JNK activation in primary sensory neurons and spinal astrocytes for neuropathic pain development and maintenance. J Neurosci 26:3551-3560. CrossRef Medline
71. ZimmermannM. (1983). Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16:109-110. CrossRef Medline