Spinal translocator protein alleviates chronic neuropathic pain behavior and modulates spinal astrocyte-neuronal function in rats with L5 spinal nerve ligation model

Pain

Volumn 157, Issue 1, 2016, Pages 103-116

  Liu, Xiaoming ^a   Liu, Hongjun ^a   Xu, Shuangshuang ^a   Tang, Zongxiang ^b   Xia, Weiliang ^c   Cheng, Zhuqiang ^a   Li, Weiyan ^a   Jin, Yi ^a  

^a JINLING HOSPITAL   (China)

^b NANJING UNIVERSITY OF CHINESE MEDICINE   (China)

^c SHANGHAI JIAO TONG UNIVERSITY   (China)

Author keywords

Astrocyte; Chemokine; Chronic neuropathic pain; Neuronal glial interaction; Translocator protein

Indexed keywords

4' CHLORODIAZEPAM; ANALGESIC AGENT; CARRIER PROTEIN; CHEMOKINE RECEPTOR CXCR2; CXCL1 CHEMOKINE; N SEC BUTYL 1 (2 CHLOROPHENYL) N METHYL 3 ISOQUINOLINECARBOXAMIDE; STRESS ACTIVATED PROTEIN KINASE 1; TRANSLOCATOR PROTEIN; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID A RECEPTOR; 4'-CHLORODIAZEPAM; BENZODIAZEPINE DERIVATIVE; ISOQUINOLINE DERIVATIVE; TSPO PROTEIN, RAT;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; CHRONIC PAIN; CONTROLLED STUDY; DOSE RESPONSE; ENZYME ACTIVATION; ENZYME LINKED IMMUNOSORBENT ASSAY; IN VITRO STUDY; IN VIVO STUDY; LENTIVIRINAE; MALE; NERVE CELL; NEUROMODULATION; NEUROPATHIC PAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SPINAL CORD DORSAL HORN; SPINAL NERVE LIGATION INJURY; UPREGULATION; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; WESTERN BLOTTING; ANIMAL; COMPLICATION; DRUG EFFECTS; GENETICS; INJURIES; METABOLISM; NEURALGIA; PERIPHERAL NERVE INJURY; SPINAL NERVE;

ANIMALS; ASTROCYTES; BENZODIAZEPINONES; CARRIER PROTEINS; CHEMOKINE CXCL1; CHRONIC PAIN; ISOQUINOLINES; MAP KINASE SIGNALING SYSTEM; NEURALGIA; NEURONS; PERIPHERAL NERVE INJURIES; RATS; RECEPTORS, GABA-A; SPINAL NERVES; UP-REGULATION;

EID: 84953722389     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1097/j.pain.0000000000000339     Document Type: Article

References (40)

1. Chang JL, Peng HY, Wu HC, Lu HT, Pan SF, Chen MJ, Lin TB. Acute neurosteroids inhibits the spinal reflex potentiation via GABAergic neurotransmission. Am J Physiol Renal Physiol 2010; 299: F43-8
2. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 1994; 53: 55-63
3. Chelli B, Pini S, Abelli M, Cardini A, Lari L, Muti M, Gesi C, Cassano GB, Lucacchini A, Martini C. Platelet 18 kDa translocator protein density is reduced in depressed patients with adult separation anxiety. Eur Neuropsychopharmacol 2008; 18: 249-54
4. Chen MK, Guilarte TR. Translocator protein 18kDa (TSPO): molecular sensor of brain injury and repair. Pharmacol Ther 2008; 118: 1-17
5. DalBóS, Nardi GM, Ferrara P, Ribeiro-do-Valle RM, Farges RC. Antinociceptive effects of peripheral benzodiazepine receptors. Pharmacology 2004; 70: 188-94
6. Fan J, Rone MB, Papadopoulos V. Translocator protein 2 is involved in cholesterol redistribution during erythropoiesis. J Biol Chem 2009; 284: 30484-97
7. Gao YJ, Ji RR. C-Fos and pERK, which is a better marker for neuronal activation and central sensitization after noxious stimulation and tissue injury?. Open Pain J 2009; 2: 11-7
8. Gao YJ, Ji RR. Chemokines, neuronal-glial interactions, and central processing of neuropathic pain. Pharmacol Ther 2010; 126: 56-68
9. Gao YJ, Xu ZZ, Liu YC, Wen YR, Decosterd I, Ji RR. The c-Jun N-Terminal kinase 1 (JNK1) in spinal astrocytes is required for the maintenance of bilateral mechanical allodynia under a persistent inflammatory pain condition. PAIN 2010: 148: 309-19
10. 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: 4096-108
11. Giatti S, Pesaresi M, Cavaletti G, Bianchi R, Carozzi V, Lombardi R, Maschi O, Lauria G, Garcia-Segura LM, Caruso D, Melcangi RC. Neuroprotective effects of a ligand of translocator protein-18 kDa (Ro5-4864) in experimental diabetic neuropathy. Neuroscience 2009; 164: 520-9
12. Gilron I, Watson CP, Cahill CM, Moulin DE. Neuropathic pain: a practical guide for the clinician. CMAJ 2006; 175: 265-75
13. Girard C, Liu S, Cadepond F, Adams D, Lacroix C, Verleye M, Gillardin JM, Baulieu EE, Schumacher M, Schweizer-Groyer G. Etifoxine improves peripheral nerve regeneration and functional recovery. Proc Natl Acad Sci U S A 2008; 105: 20505-10
14. Gosselin RD, Varela C, Banisadr G, Mechighel P, Rostene W, Kitabgi P, Melik-Parsadaniantz S. Constitutive expression of CCR2 chemokine receptor and inhibition by MCP-1/CCL2 of GABA-induced currents in spinal cord neurones. J Neurochem 2005; 95: 1023-34
15. Hernstadt H, Wang S, Lim G, Mao J. Spinal translocator protein (TSPO) modulates pain behavior in rats with CFA-induced monoarthritis. Brain Res 2009; 1286: 42-52
16. Ji RR, Baba H, Brenner GJ, Woolf CJ. Nociceptive-specific activation of ERK in spinal neurons contributes to pain hypersensitivity. Nat Neurosci 1999; 2: 1114-9
17. Ji RR, Strichartz G. Cell signaling and the genesis of neuropathic pain. Sci STKE 2004; 2004: reE14
18. JordàEG, Jiménez A, Verdaguer E, Canudas AM, Folch J, Sureda FX, Camins A, Pallàs M. Evidence in favour of a role for peripheral-Type benzodiazepine receptor ligands in amplification of neuronal apoptosis. Apoptosis 2005; 10: 91-104
19. Karchewski LA, Bloechlinger S, Woolf CJ. Axonal injury-dependent induction of the peripheral benzodiazepine receptor in small-diameter adult rat primary sensory neurons. Eur J Neurosci 2004; 20: 671-83
20. Karim F, Wang CC, Gereau RWt. Metabotropic glutamate receptor subtypes 1 and 5 are activators of extracellular signal-regulated kinase signaling required for inflammatory pain in mice. J Neurosci 2001; 21: 3771-9
21. 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
22. Kim HN, Lee SJ, Koh JY. The neurosteroids, allopregnanolone and progesterone, induce autophagy in cultured astrocytes. Neurochem Int 2012; 60: 125-33
23. Korkhov VM, Sachse C, Short JM, Tate CG. Three-dimensional structure of TspO by electron cryomicroscopy of helical crystals. Structure 2010; 18: 677-87
24. Labombarda F, González S, Lima A, Roig P, Guennoun R, Schumacher M, De Nicola AF. Progesterone attenuates astro- and microgliosis and enhances oligodendrocyte differentiation following spinal cord injury. Exp Neurol 2011; 231: 135-46
25. Lacapere JJ, Papadopoulos V. Peripheral-Type benzodiazepine receptor: structure and function of a cholesterol-binding protein in steroid and bile acid biosynthesis. Steroids 2003; 68: 569-85
26. Lacroix-Fralish ML, Tawfik VL, Nutile-McMenemy N, Harris BT, Deleo JA. Differential regulation of neuregulin 1 expression by progesterone in astrocytes and neurons. Neuron Glia Biol 2006; 2: 227-34
27. Liu X, Li W, Dai L, Zhang T, Xia W, Liu H, Ma K, Xu J, Jin Y. Early repeated administration of progesterone improves the recovery of neuropathic pain and modulates spinal 18kDa-Translocator protein (TSPO) expression. J Steroid Biochem Mol Biol 2014; 143: 130-40
28. Mika J, Osikowicz M, Rojewska E, Korostynski M, Wawrzczak-Bargiela A, Przewlocki R, Przewlocka B. Differential activation of spinal microglial and astroglial cells in a mouse model of peripheral neuropathic pain. Eur J Pharmacol 2009; 623: 65-72
29. Miller RJ, Rostene W, Apartis E, Banisadr G, Biber K, Milligan ED, White FA, Zhang J. Chemokine action in the nervous system. J Neurosci 2008; 28: 11792-5
30. Miyoshi K, Obata K, Kondo T, Okamura H, Noguchi K. Interleukin-18- mediated microglia/astrocyte interaction in the spinal cord enhances neuropathic pain processing after nerve injury. JNeurosci 2008; 28: 12775-87
31. Papadopoulos V, Baraldi M, Guilarte TR, Knudsen TB, Lacapère JJ, Lindemann P, Norenberg MD, Nutt D, Weizman A, Zhang MR, Gavish M. Translocator protein (18kDa): new nomenclature for the peripheral-Type benzodiazepine receptor based on its structure and molecular function. Trends Pharmacol Sci 2006; 27: 402-9
32. Papadopoulos V, Liu J, Culty M. Is there a mitochondrial signaling complex facilitating cholesterol import?. Mol Cell Endocrinol 2007; 266: 59-64
33. Parker MA, Bazan HE, Marcheselli V, Rodriguez de Turco EB, Bazan NG. Platelet-Activating factor induces permeability transition and cytochrome c release in isolated brain mitochondria. J Neurosci Res 2002; 69: 39-50
34. Shimizu T, Kaji A, Murayama C, Magata F, Shirasuna K, Wakamiya K, Okuda K, Miyamoto A. Effects of interleukin-8 on estradiol and progesterone production by bovine granulosa cells from large folliclesand progesterone production by luteinizing granulosa cells in culture. Cytokine 2012; 57: 175-81
35. Veiga S, Azcoitia I, Garcia-Segura LM. Ro5-4864, a peripheral benzodiazepine receptor ligand, reduces reactive gliosis and protects hippocampal hilar neurons from kainic acid excitotoxicity. J Neurosci Res 2005; 80: 129-37
36. Vowinckel E, Reutens D, Becher B, Verge G, Evans A, Owens T, Antel JP. PK11195 binding to the peripheral benzodiazepine receptor as a marker of microglia activation in multiple sclerosis and experimental autoimmune encephalomyelitis. J Neurosci Res 1997; 50: 345-53
37. Wei XH, Wei X, Chen FY, Zang Y, Xin WJ, Pang RP, Chen Y, Wang J, Li YY, Shen KF, Zhou LJ, Liu XG. The upregulation of translocator protein (18 kDa) promotes recovery from neuropathic pain in rats. J Neurosci 2013; 33: 1540-51
38. White FA, Jung H, Miller RJ. Chemokines and the pathophysiology of neuropathic pain. Proc Natl Acad Sci U S A 2007; 104: 20151-8
39. Yasuno F, Ota M, Kosaka J, Ito H, Higuchi M, Doronbekov TK, Nozaki S, Fujimura Y, Koeda M, Asada T, Suhara T. Increased binding of peripheral benzodiazepine receptor in Alzheimer's disease measured by positron emission tomography with [11C]DAA1106. Biol Psychiatry 2008; 64: 835-41
40. Zhang ZJ, Cao DL, Zhang X, Ji RR, Gao YJ. Chemokine contribution to neuropathic pain: respective induction of CXCL1 and CXCR2 in spinal cord astrocytes and neurons. PAIN 2013; 154: 2185-97