Sigma-1 receptor-mediated increase in spinal p38 MAPK phosphorylation leads to the induction of mechanical allodynia in mice and neuropathic rats

Experimental Neurology

Volumn 247, Issue , 2013, Pages 383-391

  Moon, Ji Young ^a   Roh, Dae Hyun ^b   Yoon, Seo Yeon ^c   Kang, Suk Yun ^a   Choi, Sheu Ran ^a   Kwon, Soon Gu ^a   Choi, Hoon Seong ^a   Han, Ho Jae ^a   Beitz, Alvin J ^d   Lee, Jang Hern ^a  

^a Seoul National University   (South Korea)

^b Kyung Hee University   (South Korea)

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

^d UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Mechanical allodynia; Neuropathic pain; P38 MAPK; Sigma 1 receptor

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE P38; SIGMA 1 OPIATE RECEPTOR;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; MALE; MOLECULAR PATHOLOGY; NEUROPATHIC PAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; RAT; RECEPTOR UPREGULATION; WESTERN BLOTTING;

MECHANICAL ALLODYNIA; NEUROPATHIC PAIN; P38 MAPK; SIGMA-1 RECEPTOR;

ANALYSIS OF VARIANCE; ANIMALS; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; ETHYLENEDIAMINES; HYPERALGESIA; IMIDAZOLES; MALE; MICE; MICE, INBRED ICR; MORPHOLINES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PAIN MEASUREMENT; PAIN THRESHOLD; PHOSPHORYLATION; PYRIDINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, SIGMA; SCIATICA; SPINAL CORD;

EID: 84881372529     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2013.01.004     Document Type: Article

References (51)

1. Alonso G., Phan V., Guillemain I., Saunier M., Legrand A., Anoal M., Maurice T. Immunocytochemical localization of the sigma(1) receptor in the adult rat central nervous system. Neuroscience 2000, 97:155-170.
2. Aydar E., Palmer C.P., Klyachko V.A., Jackson M.B. The sigma receptor as a ligand-regulated auxiliary potassium channel subunit. Neuron 2002, 34:399-410.
3. Barone F.C., Irving E.A., Ray A.M., Lee J.C., Kassis S., Kumar S., Badger A.M., Legos J.J., Erhardt J.A., Ohlstein E.H., Hunter A.J., Harrison D.C., Philpott K., Smith B.R., Adams J.L., Parsons A.A. Inhibition of p38 mitogen-activated protein kinase provides neuroprotection in cerebral focal ischemia. Med. Res. Rev. 2001, 21:129-145.
4. Bennett G.J., Xie Y.K. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 1988, 33:87-107.
5. Boyle D.L., Jones T.L., Hammaker D., Svensson C.I., Rosengren S., Albani S., Sorkin L., Firestein G.S. Regulation of peripheral inflammation by spinal p38 MAP kinase in rats. PLoS Med. 2006, 3:e338.
6. Cendan C.M., Pujalte J.M., Portillo-Salido E., Montoliu L., Baeyens J.M. Formalin-induced pain is reduced in sigma(1) receptor knockout mice. Eur. J. Pharmacol. 2005, 511:73-74.
7. Chen M., Sun H.Y., Li S.J., Das M., Kong J.M., Gao T.M. Nitric oxide as an upstream signal of p38 mediates hypoxia/reoxygenation-induced neuronal death. Neurosignals 2009, 17:162-168.
8. Cheng H.T., Dauch J.R., Oh S.S., Hayes J.M., Hong Y., Feldman E.L. p38 mediates mechanical allodynia in a mouse model of type 2 diabetes. Mol. Pain 2010, 6:28.
9. Crown E.D., Gwak Y.S., Ye Z., Johnson K.M., Hulsebosch C.E. Activation of p38 MAP kinase is involved in central neuropathic pain following spinal cord injury. Exp. Neurol. 2008, 213:257-267.
10. de la Puente B., Nadal X., Portillo-Salido E., Sanchez-Arroyos R., Ovalle S., Palacios G., Muro A., Romero L., Entrena J.M., Baeyens J.M., Lopez-Garcia J.A., Maldonado R., Zamanillo D., Vela J.M. Sigma-1 receptors regulate activity-induced spinal sensitization and neuropathic pain after peripheral nerve injury. Pain 2009, 145:294-303.
11. Duman E.N., Kesim M., Kadioglu M., Ulku C., Kalyoncu N.I., Yaris E. Effect of gender on antinociceptive effect of paroxetine in hot plate test in mice. Prog. Neuropsychopharmacol. Biol. Psychiatry 2006, 30:292-296.
12. Fitzsimmons B.L., Zattoni M., Svensson C.I., Steinauer J., Hua X.Y., Yaksh T.L. Role of spinal p38alpha and beta MAPK in inflammatory hyperalgesia and spinal COX-2 expression. NeuroReport 2010, 21:313-317.
13. Gao Y.J., Ji R.R. Chemokines, neuronal-glial interactions, and central processing of neuropathic pain. Pharmacol. Ther. 2010, 126:56-68.
14. Gosselin R.D., Suter M.R., Ji R.R., Decosterd I. Glial cells and chronic pain. Neuroscientist 2010, 16:519-531.
15. Guitart X., Codony X., Monroy X. Sigma receptors: biology and therapeutic potential. Psychopharmacology 2004, 174:301-319.
16. Gwak Y.S., Unabia G.C., Hulsebosch C.E. Activation of p-38alpha MAPK contributes to neuronal hyperexcitability in caudal regions remote from spinal cord injury. Exp. Neurol. 2009, 220:154-161.
17. Hama A.T., Broadhead A., Lorrain D.S., Sagen J. The antinociceptive effect of the asthma drug ibudilast in rat models of peripheral and central neuropathic pain. J. Neurotrauma 2012, 29:600-610.
18. Hargreaves K., Dubner R., Brown F., Flores C., Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 1988, 32:77-88.
19. Hayashi T., Su T.P. Sigma-1 receptor chaperones at the ER-mitochondrion interface regulate Ca(2+) signaling and cell survival. Cell 2007, 131:596-610.
20. Hylden J.L., Wilcox G.L. Intrathecal morphine in mice: a new technique. Eur. J. Pharmacol. 1980, 67:313-316.
21. Ikeda H., Kiritoshi T., Murase K. Contribution of microglia and astrocytes to the central sensitization, inflammatory and neuropathic pain in the juvenile rat. Mol. Pain 2012, 8:43.
22. Ji R.R., Suter M.R. p38 MAPK, microglial signaling, and neuropathic pain. Mol. Pain 2007, 3:33.
23. Jin S.X., Zhuang Z.Y., Woolf C.J., Ji R.R. 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. 2003, 23:4017-4022.
24. Kim H.W., Kwon Y.B., Roh D.H., Yoon S.Y., Han H.J., Kim K.W., Beitz A.J., Lee J.H. Intrathecal treatment with sigma1 receptor antagonists reduces formalin-induced phosphorylation of NMDA receptor subunit 1 and the second phase of formalin test in mice. Br. J. Pharmacol. 2006, 148:490-498.
25. Kumar S., Boehm J., Lee J.C. p38 MAP kinases: key signalling molecules as therapeutic targets for inflammatory diseases. Nat. Rev. Drug Discov. 2003, 2:717-726.
26. Latremoliere A., Woolf C.J. Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J. Pain 2009, 10:895-926.
27. Lee S.A., Park J.K., Kang E.K., Bae H.R., Bae K.W., Park H.T. Calmodulin-dependent activation of p38 and p42/44 mitogen-activated protein kinases contributes to c-fos expression by calcium in PC12 cells: modulation by nitric oxide. Mol. Brain Res. 2000, 75:16-24.
28. Lee K.M., Jeon S.M., Cho H.J. Tumor necrosis factor receptor 1 induces interleukin-6 upregulation through NF-kappaB in a rat neuropathic pain model. Eur. J. Pain 2009, 13:794-806.
29. Liu W., Wang C.H., Cui Y., Mo L.Q., Zhi J.L., Sun S.N., Wang Y.L., Yu H.M., Zhao C.M., Feng J.Q. Inhibition of neuronal nitric oxide synthase antagonizes morphine antinociceptive tolerance by decreasing activation of p38 MAPK in the spinal microglia. Neurosci. Lett. 2006, 410:174-177.
30. Matsuyoshi H., Takimoto K., Yunoki T., Erickson V.L., Tyagi P., Hirao Y., Wanaka A., Yoshimura N. Distinct cellular distributions of Kv4 pore-forming and auxiliary subunits in rat dorsal root ganglion neurons. Life Sci. 2012, 91:258-263.
31. Mestre C., Pelissier T., Fialip J., Wilcox G., Eschalier A. A method to perform direct transcutaneous intrathecal injection in rats. J. Pharmacol. Toxicol. Methods 1994, 32:197-200.
32. Nishimura T., Ishima T., Iyo M., Hashimoto K. Potentiation of nerve growth factor-induced neurite outgrowth by fluvoxamine: role of sigma-1 receptors, IP3 receptors and cellular signaling pathways. PLoS One 2008, 3:e2558.
33. Ohsawa M., Hayashi S.S., Kamei J. Effect of acute topical application of +-pentazocine on the mechanical allodynia in diabetic mice. Eur. J. Pharmacol. 2010, 641:49-53.
34. Ossipov M.H., Bian D., Malan T.P., Lai J., Porreca F. Lack of involvement of capsaicin-sensitive primary afferents in nerve-ligation injury induced tactile allodynia in rats. Pain 1999, 79:127-133.
35. Osuka K., Watanabe Y., Usuda N., Atsuzawa K., Aoshima C., Yamauchi K., Takayasu M., Yoshida J. Phosphorylation of neuronal nitric oxide synthase at Ser847 in the nucleus intermediolateralis after spinal cord injury in mice. Neuroscience 2007, 145:241-247.
36. Pande M., Hur J., Hong Y., Backus C., Hayes J.M., Oh S.S., Kretzler M., Feldman E.L. Transcriptional profiling of diabetic neuropathy in the BKS db/db mouse: a model of type 2 diabetes. Diabetes 2011, 60:1981-1989.
37. Roh D.H., Kim H.W., Yoon S.Y., Seo H.S., Kwon Y.B., Han H.J., Beitz A.J., Lee J.H. 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 2008, 12:552-563.
38. Roh D.H., Kim H.W., Yoon S.Y., Seo H.S., Kwon Y.B., Kim K.W., Han H.J., Beitz A.J., Lee J.H. Intrathecal administration of sigma-1 receptor agonists facilitates nociception: involvement of a protein kinase C-dependent pathway. J. Neurosci. Res. 2008, 86:3644-3654.
39. Roh D.H., Kim H.W., Yoon S.Y., Seo H.S., Kwon Y.B., Kim K.W., Han H.J., Beitz A.J., Na H.S., Lee J.H. 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 2008, 109:879-889.
40. Roh D.H., Choi S.R., Yoon S.Y., Kang S.Y., Moon J.Y., Kwon S.G., Han H.J., Beitz A.J., Lee J.H. Spinal neuronal NOS activation mediates sigma-1 receptor-induced mechanical and thermal hypersensitivity in mice: involvement of PKC-dependent GluN1 phosphorylation. Br. J. Pharmacol. 2011, 163:1707-1720.
41. Romero L., Zamanillo D., Nadal X., Sanchez-Arroyos R., Rivera-Arconada I., Dordal A., Montero A., Muro A., Bura A., Segales C., Laloya M., Hernandez E., Portillo-Salido E., Escriche M., Codony X., Encina G., Burgueno J., Merlos M., Baeyens J.M., Giraldo J., Lopez-Garcia J.A., Maldonado R., Plata-Salaman C.R., Vela J.M. Pharmacological properties of S1RA, a new sigma-1 receptor antagonist that inhibits neuropathic pain and activity-induced spinal sensitization. Br. J. Pharmacol. 2012, 166:2289-2306.
42. Sorkin L., Svensson C.I., Jones-Cordero T.L., Hefferan M.P., Campana W.M. Spinal p38 mitogen-activated protein kinase mediates allodynia induced by first-degree burn in the rat. J. Neurosci. Res. 2009, 87:948-955.
43. Su T.P., Hayashi T., Maurice T., Buch S., Ruoho A.E. The sigma-1 receptor chaperone as an inter-organelle signaling modulator. Trends Pharmacol. Sci. 2010, 31:557-566.
44. Svensson C.I., Fitzsimmons B., Azizi S., Powell H.C., Hua X.Y., Yaksh T.L. Spinal p38beta isoform mediates tissue injury-induced hyperalgesia and spinal sensitization. J. Neurochem. 2005, 92:1508-1520.
45. Trang T., Beggs S., Wan X., Salter M.W. P2X4-receptor-mediated synthesis and release of brain-derived neurotrophic factor in microglia is dependent on calcium and p38-mitogen-activated protein kinase activation. J. Neurosci. 2009, 29:3518-3528.
46. Ueda H. Molecular mechanisms of neuropathic pain-phenotypic switch and initiation mechanisms. Pharmacol. Ther. 2006, 109:57-77.
47. Ueda H., Inoue M., Yoshida A., Mizuno K., Yamamoto H., Maruo J., Matsuno K., Mita S. Metabotropic neurosteroid/sigma-receptor involved in stimulation of nociceptor endings of mice. J. Pharmacol. Exp. Ther. 2001, 298:703-710.
48. Wen Y.R., Suter M.R., Ji R.R., Yeh G.C., Wu Y.S., Wang K.C., Kohno T., Sun W.Z., Wang C.C. Activation of p38 mitogen-activated protein kinase in spinal microglia contributes to incision-induced mechanical allodynia. Anesthesiology 2009, 110:155-165.
49. Wu H.E., Sun H.S., Cheng C.W., Tseng L.F. p38 mitogen-activated protein kinase inhibitor SB203580 reverses the antianalgesia induced by dextro-morphine or morphine in the mouse spinal cord. Eur. J. Pharmacol. 2006, 550:91-94.
50. Xu L., Huang Y., Yu X., Yue J., Yang N., Zuo P. The influence of p38 mitogen-activated protein kinase inhibitor on synthesis of inflammatory cytokine tumor necrosis factor alpha in spinal cord of rats with chronic constriction injury. Anesth. Analg. 2007, 105:1838-1844. (table of contents).
51. Zhang H., Yoon S.Y., Zhang H., Dougherty P.M. Evidence that spinal astrocytes but not microglia contribute to the pathogenesis of paclitaxel-induced painful neuropathy. J. Pain 2012, 13:293-303.