σ1 receptors activate astrocytes via p38 MAPK phosphorylation leading to the development of mechanical allodynia in a mouse model of neuropathic pain

British Journal of Pharmacology

Volumn 171, Issue 24, 2014, Pages 5881-5897

  Moon, J Y ^a   Roh, D H ^b   Yoon, S Y ^c   Choi, S R ^a   Kwon, S G ^a   Choi, H S ^a   Kang, S Y ^d   Han, H J ^a   Beitz, A J ^e   Oh, S B ^a,f   Lee, J H ^a  

^a Seoul National University   (South Korea)

^b Kyung Hee University   (South Korea)

^c Korea Institute of Science and Technology   (South Korea)

^d Korea Institute of Oriental Medicine (KIOM)   (South Korea)

^e UNIVERSITY OF MINNESOTA   (United States)

^f Seoul National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; FLUOROCITRIC ACID; GLIAL FIBRILLARY ACIDIC PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; N [2 (3,4 DICHLOROPHENYL)ETHYL] 2 DIMETHYLAMINO N METHYLETHYLAMINE; SIGMA 1 OPIATE RECEPTOR; SIGMA OPIATE RECEPTOR; SIGMA-1 RECEPTOR;

ALLODYNIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; CELL ACTIVATION; CELL ACTIVITY; CELLULAR DISTRIBUTION; CHRONIC CONSTRICTION INJURY; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; DRUG POTENTIATION; ENZYME PHOSPHORYLATION; LOW DRUG DOSE; MALE; MOUSE; NEUROPATHIC PAIN; NONHUMAN; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS REGULATION; RECEPTOR BLOCKING; SPINAL CORD DORSAL HORN; ANIMAL; DISEASE MODEL; HYPERALGESIA; INJURIES; METABOLISM; NEURALGIA; PHOSPHORYLATION; SCIATIC NERVE;

ANIMALS; ASTROCYTES; DISEASE MODELS, ANIMAL; HYPERALGESIA; MICE; NEURALGIA; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; RECEPTORS, SIGMA; SCIATIC NERVE;

EID: 84919399854     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12893     Document Type: Article

References (65)

1. Agulhon C, Petravicz J, McMullen AB, Sweger EJ, Minton SK, Taves SR, et al. (2008). What is the role of astrocyte calcium in neurophysiology? Neuron 59: 932-946.
2. Alexander SP, Benson HE, Faccenda E, Pawson AJ, Sharman JL, McGrath JC, et al. (2013a). The Concise Guide to PHARMACOLOGY 2013/14: Overview. Br J Pharmacol 170: 1 449 -1 458.
3. Alexander SP, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013b). The Concise Guide to PHARMACOLOGY 2013/14: Ligand-gated ion channels. Br J Pharmacol 170: 1582-1606
4. Alexander SP, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013c). The Concise Guide to PHARMACOLOGY 2013/14: Enzymes. Br J Pharmacol 170: 1797-1867.
5. Alonso G, Phan V, Guillemain I, Saunier M, Legrand A, Anoal M, et al. (2000). Immunocytochemical localization of the sigma-1 receptor in the adult rat central nervous system. Neuroscience 97: 155-170.
6. Barone FC, Irving EA, Ray AM, Lee JC, Kassis S, Kumar S, et al. (2001). Inhibition of p38 mitogen-activated protein kinase provides neuroprotection in cerebral focal ischemia. Med Res Rev 21: 129-145.
7. Ben Achour S, Pont-Lezica L, Bechade C, Pascual O, (2010). Is astrocyte calcium signaling relevant for synaptic plasticity? Neuron Glia Biol 6: 147-155.
8. Bennett GJ, Xie YK, (1988). A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33: 87-107.
9. Carlsson A, Ohsawa M, Hallberg M, Nyberg F, Kamei J, (2010). Substance P(1-7) induces antihyperalgesia in diabetic mice through a mechanism involving the naloxone-sensitive sigma receptors. Eur J Pharmacol 626: 250-255.
10. Dunn KW, Kamocka MM, McDonald JH, (2011). A practical guide to evaluating colocalization in biological microscopy. Am J Physiol Cell Physiol 300: C723-C742.
11. Francardo V, Bez F, Wieloch T, Nissbrandt H, Ruscher K, Cenci MA, (2014). Pharmacological stimulation of sigma-1 receptors has neurorestorative effects in experimental parkinsonism. Brain 137: 1998-2014.
12. Gao YJ, Ji RR, (2010a). Light touch induces ERK activation in superficial dorsal horn neurons after inflammation: involvement of spinal astrocytes and JNK signaling in touch-evoked central sensitization and mechanical allodynia. J Neurochem 115: 505-514.
13. Gao YJ, Ji RR, (2010b). Targeting astrocyte signaling for chronic pain. Neurother 7: 482-493.
14. Gao YJ, Zhang L, Samad OA, Suter MR, Yasuhiko K, Xu ZZ, et al. (2009). JNK-induced MCP-1 production in spinal cord astrocytes contributes to central sensitization and neuropathic pain. J Neurosci 29: 4096-4108.
15. Gao YJ, Zhang L, Ji RR, (2010c). Spinal injection of TNF-alpha-activated astrocytes produces persistent pain symptom mechanical allodynia by releasing monocyte chemoattractant protein-1. Glia 58: 1871-1880.
16. Gekker G, Hu S, Sheng WS, Rock RB, Lokensgard JR, Peterson PK, (2006). Cocaine-induced HIV-1 expression in microglia involves sigma-1 receptors and transforming growth factor-beta1. Int Immunopharmacol 6: 1029-1033.
17. Gosselin RD, Suter MR, Ji RR, Decosterd I, (2010). Glial cells and chronic pain. Neuroscientist 16: 519-531.
18. Guitart X, Codony X, Monroy X, (2004). Sigma receptors: biology and therapeutic potential. Psychopharmacology (Berl) 174: 301-319.
19. Guo W, Wang H, Watanabe M, Shimizu K, Zou S, LaGraize SC, et al. (2007). Glial-cytokine-neuronal interactions underlying the mechanisms of persistent pain. J Neurosci 27: 6006-6018.
20. Halassa MM, Fellin T, Haydon PG, (2007). The tripartite synapse: roles for gliotransmission in health and disease. Trends Mol Med 13: 54-63.
21. 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.
22. Hayashi T, Su TP, (2001). Regulating ankyrin dynamics: roles of sigma-1 receptors. Proc Natl Acad Sci U S A 98: 491-496.
23. Hellewell SB, Bruce A, Feinstein G, Orringer J, Williams W, Bowen WD, (1994). Rat liver and kidney contain high densities of sigma 1 and sigma 2 receptors: characterization by ligand binding and photoaffinity labeling. Eur J Pharmacol 268: 9-18.
24. Hylden JL, Wilcox GL, (1980). Intrathecal morphine in mice: a new technique. Eur J Pharmacol 67: 313-316.
25. Ikeda H, Kiritoshi T, Murase K, (2012). Contribution of microglia and astrocytes to the central sensitization, inflammatory and neuropathic pain in the juvenile rat. Mol Pain 8: 43.
26. Ji XT, Qian NS, Zhang T, Li JM, Li XK, Wang P, et al. (2013). Spinal astrocytic activation contributes to mechanical allodynia in a rat chemotherapy-induced neuropathic pain model. PLoS ONE 8: e60733.
27. Kang SY, Kim CY, Roh DH, Yoon SY, Park JH, Lee HJ, et al. (2011). Chemical stimulation of the ST36 acupoint reduces both formalin-induced nociceptive behaviors and spinal astrocyte activation via spinal alpha-2 adrenoceptors. Brain Res Bull 86: 412-421.
28. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, (2010). Animal research: Reporting in vivo experiments: the ARRIVE guidelines. Br J Pharmacol 160: 1577-1579.
29. Kumar S, Boehm J, Lee JC, (2003). p38 MAP kinases: key signalling molecules as therapeutic targets for inflammatory diseases. Nat Rev Drug Discov 2: 717-726.
30. Latremoliere A, Woolf CJ, (2009). Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J Pain 10: 895-926.
31. Lee SH, Park J, Che Y, Han PL, Lee JK, (2000). Constitutive activity and differential localization of p38alpha and p38beta MAPKs in adult mouse brain. J Neurosci Res 60: 623-631.
32. Mancuso R, Olivan S, Rando A, Casas C, Osta R, Navarro X, (2012). Sigma-1R agonist improves motor function and motoneuron survival in ALS mice. Neurother 9: 814-826.
33. Mavlyutov TA, Epstein ML, Andersen KA, Ziskind-Conhaim L, Ruoho AE, (2010). The sigma-1 receptor is enriched in postsynaptic sites of C-terminals in mouse motoneurons. An anatomical and behavioral study. Neuroscience 167: 247-255.
34. McGrath J, Drummond G, McLachlan E, Kilkenny C, Wainwright C, (2010). Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160: 1573-1576.
35. Miyano K, Morioka N, Sugimoto T, Shiraishi S, Uezono Y, Nakata Y, (2010). Activation of the neurokinin-1 receptor in rat spinal astrocytes induces Ca2+ release from IP3-sensitive Ca2+ stores and extracellular Ca2+ influx through TRPC3. Neurochem Int 57: 923-934.
36. Monnet FP, (2005). Sigma-1 receptor as regulator of neuronal intracellular Ca2+: clinical and therapeutic relevance. Biol Cell 97: 873-883.
37. Moon JY, Roh DH, Yoon SY, Kang SY, Choi SR, Kwon SG, et al. (2013). Sigma-1 receptor-mediated increase in spinal p38 MAPK phosphorylation leads to the induction of mechanical allodynia in mice and neuropathic rats. Exp Neurol 247: 383-391.
38. Narita M, Yoshida T, Nakajima M, Narita M, Miyatake M, Takagi T, et al. (2006). Direct evidence for spinal cord microglia in the development of a neuropathic pain-like state in mice. J Neurochem 97: 1337-1348.
39. Nieto FR, Cendan CM, Sanchez-Fernandez C, Cobos EJ, Entrena JM, Tejada MA, et al. (2012). Role of sigma-1 receptors in paclitaxel-induced neuropathic pain in mice. J Pain 13: 1107-1121.
40. Ossipov MH, Bian D, Malan TP Jr, Lai J, Porreca F, (1999). Lack of involvement of capsaicin-sensitive primary afferents in nerve-ligation injury induced tactile allodynia in rats. Pain 79: 127-133.
41. Palacios G, Muro A, Vela JM, Molina-Holgado E, Guitart X, Ovalle S, et al. (2003). Immunohistochemical localization of the sigma1-receptor in oligodendrocytes in the rat central nervous system. Brain Res 961: 92-99.
42. de la Puente B, Nadal X, Portillo-Salido E, Sanchez-Arroyos R, Ovalle S, Palacios G, et al. (2009). Sigma-1 receptors regulate activity-induced spinal sensitization and neuropathic pain after peripheral nerve injury. Pain 145: 294-303.
43. Pawson AJ, Sharman JL, Benson HE, Faccenda E, Alexander SP, Buneman OP, et al.; NC-IUPHAR (2014). The IUPHAR/BPS Guide to PHARMACOLOGY: an expert-driven knowledgebase of drug targets and their ligands. Nucl Acids Res 42 (Database Issue): D1098-D1106.
44. Roh DH, Kim HW, Yoon SY, Seo HS, Kwon YB, Han HJ, et al. (2008a). Depletion of capsaicin-sensitive afferents prevents lamina-dependent increases in spinal N-methyl-D-aspartate receptor subunit 1 expression and phosphorylation associated with thermal hyperalgesia in neuropathic rats. Eur J Pain 12: 552-563.
45. Roh DH, Kim HW, Yoon SY, Seo HS, Kwon YB, Kim KW, et al. (2008b). Intrathecal administration of sigma-1 receptor agonists facilitates nociception: involvement of a protein kinase C-dependent pathway. J Neurosci Res 86: 3644-3654.
46. Roh DH, Kim HW, Yoon SY, Seo HS, Kwon YB, Kim KW, et al. (2008c). Intrathecal injection of the sigma-1 receptor antagonist BD1047 blocks both mechanical allodynia and increases in spinal NR1 expression during the induction phase of rodent neuropathic pain. Anesthesiology 109: 879-889.
47. Roh DH, Yoon SY, Seo HS, Kang SY, Moon JY, Song S, et al. (2010). Sigma-1 receptor-induced increase in murine spinal NR1 phosphorylation is mediated by the PKCalpha and epsilon, but not the PKCzeta, isoforms. Neurosci Lett 477: 95-99.
48. Roh DH, Choi SR, Yoon SY, Kang SY, Moon JY, Kwon SG, et al. (2011). Spinal neuronal NOS activation mediates sigma-1 receptor-induced mechanical and thermal hypersensitivity in mice: involvement of PKC-dependent GluN1 phosphorylation. Br J Pharmacol 163: 1707-1720.
49. Ruscher K, Shamloo M, Rickhag M, Ladunga I, Soriano L, Gisselsson L, et al. (2011). The sigma-1 receptor enhances brain plasticity and functional recovery after experimental stroke. Brain 134: 732-746.
50. Su TP, Hayashi T, Vaupel DB, (2009). When the endogenous hallucinogenic trace amine N,N-dimethyltryptamine meets the sigma-1 receptor. Sci Signal 2: pe12.
51. Su TP, Hayashi T, Maurice T, Buch S, Ruoho AE, (2010). The sigma-1 receptor chaperone as an inter-organelle signaling modulator. Trends Pharmacol Sci 31: 557-566.
52. Svensson CI, Fitzsimmons B, Azizi S, Powell HC, Hua XY, Yaksh TL, (2005). Spinal p38beta isoform mediates tissue injury-induced hyperalgesia and spinal sensitization. J Neurochem 92: 1508-1520.
53. Terayama R, Omura S, Fujisawa N, Yamaai T, Ichikawa H, Sugimoto T, (2008). Activation of microglia and p38 mitogen-activated protein kinase in the dorsal column nucleus contributes to tactile allodynia following peripheral nerve injury. Neuroscience 153: 1245-1255.
54. Tsuda M, Mizokoshi A, Shigemoto-Mogami Y, Koizumi S, Inoue K, (2004). Activation of p38 mitogen-activated protein kinase in spinal hyperactive microglia contributes to pain hypersensitivity following peripheral nerve injury. Glia 45: 89-95.
55. Ueda H, (2006). Molecular mechanisms of neuropathic pain-phenotypic switch and initiation mechanisms. Pharmacol Ther 109: 57-77.
56. Wang S, Song L, Tan Y, Ma Y, Tian Y, Jin X, et al. (2012). A functional relationship between trigeminal astroglial activation and NR1 expression in a rat model of temporomandibular joint inflammation. Pain Med 13: 1590-1600.
57. Wen YR, Suter MR, Ji RR, Yeh GC, Wu YS, Wang KC, et al. (2009). Activation of p38 mitogen-activated protein kinase in spinal microglia contributes to incision-induced mechanical allodynia. Anesthesiology 110: 155-165.
58. Xu M, Bruchas MR, Ippolito DL, Gendron L, Chavkin C, (2007). Sciatic nerve ligation-induced proliferation of spinal cord astrocytes is mediated by kappa opioid activation of p38 mitogen-activated protein kinase. J Neurosci 27: 2570-2581.
59. Zhang GH, Lv MM, Wang S, Chen L, Qian NS, Tang Y, et al. (2011a). Spinal astrocytic activation is involved in a virally-induced rat model of neuropathic pain. PLoS ONE 6: e23059.
60. Zhang H, Nei H, Dougherty PM, (2010). A p38 mitogen-activated protein kinase-dependent mechanism of disinhibition in spinal synaptic transmission induced by tumor necrosis factor-alpha. J Neurosci 30: 12844-12855.
61. Zhang H, Yoon SY, Zhang H, Dougherty PM, (2012). Evidence that spinal astrocytes but not microglia contribute to the pathogenesis of Paclitaxel-induced painful neuropathy. J Pain 13: 293-303.
62. Zhang RX, Li A, Liu B, Wang L, Ren K, Zhang H, et al. (2008a). IL-1ra alleviates inflammatory hyperalgesia through preventing phosphorylation of NMDA receptor NR-1 subunit in rats. Pain 135: 232-239.
63. Zhang RX, Liu B, Li A, Wang L, Ren K, Qiao JT, et al. (2008b). Interleukin 1beta facilitates bone cancer pain in rats by enhancing NMDA receptor NR-1 subunit phosphorylation. Neuroscience 154: 1533-1538.
64. Zhang X, Wang J, Zhou Q, Xu Y, Pu S, Wu J, et al. (2011b). Brain-derived neurotrophic factor-activated astrocytes produce mechanical allodynia in neuropathic pain. Neuroscience 199: 452-460.
65. Zhao J, Ha Y, Liou GI, Gonsalvez GB, Smith SB, Bollinger KE, (2014). Sigma receptor ligand, (+)-pentazocine, suppresses inflammatory responses of retinal microglia. Invest Ophthalmol Vis Sci 55: 3375-3384.