Sigma-1 receptor expression in sensory neurons and the effect of painful peripheral nerve injury

Molecular Pain

Volumn 9, Issue 1, 2013, Pages

  Bangaru, Madhavi L ^a   Weihrauch, Dorothee ^a   Tang, Qing Bo ^a   Zoga, Vasiliki ^a   Hogan, Quinn ^b   Wu, Hsiang en ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b CLEMENT J ZABLOCKI VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Dorsal root ganglion; Endoplasmic reticulum; Neuropathic pain; Peripheral nerve injury; Sensory neuron; Sigma 1 receptor

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; ISOLECTIN B4; NEUROFILAMENT 200; NEUROFILAMENT PROTEIN; SIGMA 1 OPIATE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL SIZE; CELL SUBPOPULATION; CONTROLLED STUDY; CYTOPLASM; DOWN REGULATION; ENDOPLASMIC RETICULUM; GLIA CELL; IMMUNOHISTOCHEMISTRY; NEUROPATHIC PAIN; NONHUMAN; PATHOGENESIS; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; SATELLITE CELL; SENSORY NERVE CELL; SPINAL GANGLION;

ANIMALS; CALCITONIN GENE-RELATED PEPTIDE; ENDOPLASMIC RETICULUM; GANGLIA, SPINAL; GENE EXPRESSION REGULATION; MALE; NEUROFILAMENT PROTEINS; PERIPHERAL NERVE INJURIES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, SIGMA; SATELLITE CELLS, PERINEURONAL; SENSORY RECEPTOR CELLS;

EID: 84883610229     PISSN: None     EISSN: 17448069     Source Type: Journal    
DOI: 10.1186/1744-8069-9-47     Document Type: Article

References (79)

1. Hayashi T, Su TP. Sigma-1 receptor chaperones at the ER-mitochondrion interface regulate Ca(2+) signaling and cell survival. Cell 2007, 131:596-610. 10.1016/j.cell.2007.08.036, 17981125.
2. Matsumoto RR. σ Receptors: historical perspective and background. Sigma Receptors 2007, 1-23. New York, NY: Springer, Matsumoto RR, Bowen WD, Su T-P, 1.
3. Palacios G, Muro A, Verdu E, Pumarola M, Vela JM. Immunohistochemical localization of the sigma1 receptor in Schwann cells of rat sciatic nerve. Brain Res 2004, 1007:65-70. 10.1016/j.brainres.2004.02.013, 15064136.
4. Palacios G, Muro A, Vela JM, Molina-Holgado E, Guitart X, Ovalle S, Zamanillo D. Immunohistochemical localization of the sigma1-receptor in oligodendrocytes in the rat central nervous system. Brain Res 2003, 961:92-99. 10.1016/S0006-8993(02)03892-1, 12535781.
5. 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. 10.1016/S0306-4522(00)00014-2, 10771347.
6. Tchedre KT, Huang RQ, Dibas A, Krishnamoorthy RR, Dillon GH, Yorio T. Sigma-1 receptor regulation of voltage-gated calcium channels involves a direct interaction between sigma-1 receptors and the voltage-gated L-type calcium channel. Invest Ophthalmol Vis Sci 2008, 49:4993-5002. 10.1167/iovs.08-1867, 18641291.
7. Hayashi T, Tsai SY, Mori T, Fujimoto M, Su TP. Targeting ligand-operated chaperone sigma-1 receptors in the treatment of neuropsychiatric disorders. Expert Opin Ther Targets 2011, 15:557-577. 3076924, 21375464.
8. Maurice T, Su TP. The pharmacology of sigma-1 receptors. Pharmacol Ther 2009, 124:195-206. 10.1016/j.pharmthera.2009.07.001, 2785038, 19619582.
9. Tagashira H, Zhang C, Lu YM, Hasegawa H, Kanai H, Han F, Fukunaga K. Stimulation of sigma(1)-receptor restores abnormal mitochondrial Ca(2+) mobilization and ATP production following cardiac hypertrophy. Biochim Biophys Acta 1830, 2013:3082-3094.
10. Megalizzi V, Le Mercier M, Decaestecker C. Sigma receptors and their ligands in cancer biology: overview and new perspectives for cancer therapy. Med Res Rev 2012, 32:410-427. 10.1002/med.20218, 20687157.
11. Hayashi T, Justinova Z, Hayashi E, Cormaci G, Mori T, Tsai SY, Barnes C, Goldberg SR, Su TP. Regulation of sigma-1 receptors and endoplasmic reticulum chaperones in the brain of methamphetamine self-administering rats. J Pharmacol Exp Ther 2010, 332:1054-1063. 10.1124/jpet.109.159244, 2835445, 19940104.
12. Hiranita T, Soto PL, Tanda G, Katz JL. Reinforcing effects of sigma-receptor agonists in rats trained to self-administer cocaine. J Pharmacol Exp Ther 2010, 332:515-524. 10.1124/jpet.109.159236, 2812106, 19892920.
13. Villard V, Espallergues J, Keller E, Alkam T, Nitta A, Yamada K, Nabeshima T, Vamvakides A, Maurice T. Antiamnesic and neuroprotective effects of the aminotetrahydrofuran derivative ANAVEX1-41 against amyloid beta(25-35)-induced toxicity in mice. Neuropsychopharmacology 2009, 34:1552-1566. 10.1038/npp.2008.212, 19052542.
14. Yao H, Yang Y, Kim KJ, Bethel-Brown C, Gong N, Funa K, Gendelman HE, Su TP, Wang JQ, Buch S. Molecular mechanisms involving sigma receptor-mediated induction of MCP-1: implication for increased monocyte transmigration. Blood 2010, 115:4951-4962. 10.1182/blood-2010-01-266221, 2890169, 20354174.
15. Ajmo CT, Vernon DO, Collier L, Pennypacker KR, Cuevas J. Sigma receptor activation reduces infarct size at 24 hours after permanent middle cerebral artery occlusion in rats. Curr Neurovasc Res 2006, 3:89-98. 10.2174/156720206776875849, 16719792.
16. Cuevas J, Behensky A, Deng W, Katnik C. Afobazole modulates neuronal response to ischemia and acidosis via activation of sigma-1 receptors. J Pharmacol Exp Ther 2011, 339:152-160. 10.1124/jpet.111.182774, 21715562.
17. Tseng LF, Hogan QH, Wu HE. (+)-Morphine attenuates the (-)-morphine-produced tail-flick inhibition via the sigma-1 receptor in the mouse spinal cord. Life Sci 2011, 89:875-877. 10.1016/j.lfs.2011.09.018, 3220751, 21989208.
18. Terashvili M, Wu HE, Moore RM, Harder DR, Tseng LF. (+)-Morphine and (-)-morphine stereoselectively attenuate the (-)-morphine-produced tail-flick inhibition via the naloxone-sensitive sigma receptor in the ventral periaqueductal gray of the rat. Eur J Pharmacol 2007, 571:1-7. 10.1016/j.ejphar.2007.05.033, 3718891, 17597599.
19. Wu HE, Hong JS, Tseng LF. Stereoselective action of (+)-morphine over (-)-morphine in attenuating the (-)-morphine-produced antinociception via the naloxone-sensitive sigma receptor in the mouse. Eur J Pharmacol 2007, 571:145-151. 10.1016/j.ejphar.2007.06.012, 2080825, 17617400.
20. Chien CC, Pasternak GW. Selective antagonism of opioid analgesia by a sigma system. J Pharmacol Exp Ther 1994, 271:1583-1590.
21. Chien CC, Pasternak GW. Sigma antagonists potentiate opioid analgesia in rats. Neurosci Lett 1995, 190:137-139. 10.1016/0304-3940(95)11504-P, 7644123.
22. Mei J, Pasternak GW. Sigma1 receptor modulation of opioid analgesia in the mouse. J Pharmacol Exp Ther 2002, 300:1070-1074. 10.1124/jpet.300.3.1070, 11861817.
23. Mei J, Pasternak GW. Modulation of brainstem opiate analgesia in the rat by sigma 1 receptors: a microinjection study. J Pharmacol Exp Ther 2007, 322:1278-1285. 10.1124/jpet.107.121137, 17545312.
24. Kim HW, Kwon YB, Roh DH, Yoon SY, Han HJ, Kim KW, Beitz AJ, Lee JH. 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. 1751783, 16682960.
25. Roh DH, Kim HW, Yoon SY, Seo HS, Kwon YB, Kim KW, Han HJ, Beitz AJ, Na HS, Lee JH. 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. 10.1097/ALN.0b013e3181895a83, 18946301.
26. Romero L, Zamanillo D, Nadal X, Sanchez-Arroyos R, Rivera-Arconada I, Dordal A, Montero A, Muro A, Bura A, Segales C, et al. 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. 10.1111/j.1476-5381.2012.01942.x, 3448894, 22404321.
27. Roh DH, Kim HW, Yoon SY, Seo HS, Kwon YB, Kim KW, Han HJ, Beitz AJ, Lee JH. Intrathecal administration of sigma-1 receptor agonists facilitates nociception: Involvement of a protein kinase C-dependent pathway. J Neurosci Res 2008, 86:3644-3654. 10.1002/jnr.21802, 18655205.
28. Roh DH, Choi SR, Yoon SY, Kang SY, Moon JY, Kwon SG, Han HJ, Beitz AJ, Lee JH. Spinal nNOS activation mediates sigma-1 receptor-induced mechanical and thermal hypersensitivity in mice: involvement of PKC-dependent NR1 phosphorylation. Br J Pharmacol 2011, 163:1707-1720. 10.1111/j.1476-5381.2011.01316.x, 3166697, 21391983.
29. Yoon SY, Roh DH, Seo HS, Kang SY, Han HJ, Beitz AJ, Lee JH. Intrathecal injection of the neurosteroid, DHEAS, produces mechanical allodynia in mice: involvement of spinal sigma-1 and GABA receptors. Br J Pharmacol 2009, 157:666-673. 10.1111/j.1476-5381.2009.00197.x, 2707978, 19422393.
30. Zimmermann M. Pathobiology of neuropathic pain. Eur J Pharmacol 2001, 429:23-37. 10.1016/S0014-2999(01)01303-6, 11698024.
31. von Hehn CA, Baron R, Woolf CJ. Deconstructing the neuropathic pain phenotype to reveal neural mechanisms. Neuron 2012, 73:638-652. 10.1016/j.neuron.2012.02.008, 3319438, 22365541.
32. Cai YQ, Chen SR, Pan HL. Upregulation of nuclear factor of activated T-cells by nerve injury contributes to development of neuropathic pain. J Pharmacol Exp Ther 2013, 345:161-168. 10.1124/jpet.112.202192, 23386250.
33. Inquimbert P, Bartels K, Babaniyi OB, Barrett LB, Tegeder I, Scholz J. Peripheral nerve injury produces a sustained shift in the balance between glutamate release and uptake in the dorsal horn of the spinal cord. Pain 2012, 153:2422-2431. 10.1016/j.pain.2012.08.011, 23021150.
34. Takeuchi Y, Yamasaki M, Nagumo Y, Imoto K, Watanabe M, Miyata M. Rewiring of afferent fibers in the somatosensory thalamus of mice caused by peripheral sensory nerve transection. J Neurosci 2012, 32:6917-6930. 10.1523/JNEUROSCI.5008-11.2012, 22593060.
35. Rigaud M, Gemes G, Weyker PD, Cruikshank JM, Kawano T, Wu HE, Hogan QH. Axotomy depletes intracellular calcium stores in primary sensory neurons. Anesthesiology 2009, 111:381-392. 10.1097/ALN.0b013e3181ae6212, 2891519, 19602958.
36. Hogan QH, McCallum JB, Sarantopoulos C, Aason M, Mynlieff M, Kwok WM, Bosnjak ZJ. Painful neuropathy decreases membrane calcium current in mammalian primary afferent neurons. Pain 2000, 86:43-53. 10.1016/S0304-3959(99)00313-9, 10779659.
37. McCallum JB, Kwok WM, Sapunar D, Fuchs A, Hogan QH. Painful peripheral nerve injury decreases calcium current in axotomized sensory neurons. Anesthesiology 2006, 105:160-168. 10.1097/00000542-200607000-00026, 3725035, 16810008.
38. Hayashi T, Maurice T, Su TP. Ca(2+) signaling via sigma(1)-receptors: novel regulatory mechanism affecting intracellular Ca(2+) concentration. J Pharmacol Exp Ther 2000, 293:788-798.
39. Zhang H, Cuevas J. Sigma receptors inhibit high-voltage-activated calcium channels in rat sympathetic and parasympathetic neurons. J Neurophysiol 2002, 87:2867-2879.
40. Hayashi T, Su TP. Sigma-1 receptor ligands: potential in the treatment of neuropsychiatric disorders. CNS Drugs 2004, 18:269-284. 10.2165/00023210-200418050-00001, 15089113.
41. Maurice T, Gregoire C, Espallergues J. Neuro(active)steroids actions at the neuromodulatory sigma1 (sigma1) receptor: biochemical and physiological evidences, consequences in neuroprotection. Pharmacol Biochem Behav 2006, 84:581-597. 10.1016/j.pbb.2006.07.009, 16945406.
42. Schaeffer V, Meyer L, Patte-Mensah C, Eckert A, Mensah-Nyagan AG. Sciatic nerve injury induces apoptosis of dorsal root ganglion satellite glial cells and selectively modifies neurosteroidogenesis in sensory neurons. Glia 2010, 58:169-180. 10.1002/glia.20910, 19565659.
43. Hayashi T, Su TP. Regulating ankyrin dynamics: Roles of sigma-1 receptors. Proc Natl Acad Sci USA 2001, 98:491-496. 10.1073/pnas.98.2.491, 14614, 11149946.
44. Weick M, Cherkas PS, Hartig W, Pannicke T, Uckermann O, Bringmann A, Tal M, Reichenbach A, Hanani M. P2 receptors in satellite glial cells in trigeminal ganglia of mice. Neuroscience 2003, 120:969-977. 10.1016/S0306-4522(03)00388-9, 12927203.
45. Gemes G, Bangaru ML, Wu HE, Tang Q, Weihrauch D, Koopmeiners AS, Cruikshank JM, Kwok WM, Hogan QH. Store-operated Ca2+ entry in sensory neurons: functional role and the effect of painful nerve injury. J Neurosci 2011, 31:3536-3549. 10.1523/JNEUROSCI.5053-10.2011, 3565463, 21389210.
46. Hanani M. Satellite glial cells in sensory ganglia: from form to function. Brain Res Brain Res Rev 2005, 48:457-476. 10.1016/j.brainresrev.2004.09.001, 15914252.
47. Hayashi T, Su TP. Sigma-1 receptors at galactosylceramide-enriched lipid microdomains regulate oligodendrocyte differentiation. Proc Natl Acad Sci USA 2004, 101:14949-14954. 10.1073/pnas.0402890101, 522002, 15466698.
48. Xing J, Lu J, Li J. Acid-sensing ion channel subtype 3 function and immunolabelling increases in skeletal muscle sensory neurons following femoral artery occlusion. J Physiol 2012, 590:1261-1272. 3381829, 22183722.
49. Zoga V, Kawano T, Liang MY, Bienengraeber M, Weihrauch D, McCallum B, Gemes G, Hogan Q, Sarantopoulos C. KATP channel subunits in rat dorsal root ganglia: alterations by painful axotomy. Mol Pain 2010, 6:6. 10.1186/1744-8069-6-6, 2825500, 20102598.
50. Monnet FP, Debonnel G, Junien JL, De Montigny C. N-methyl-D-aspartate-induced neuronal activation is selectively modulated by sigma receptors. Eur J Pharmacol 1990, 179:441-445. 10.1016/0014-2999(90)90186-A, 2163857.
51. Son JS, Kwon YB. Sigma-1 Receptor Antagonist BD1047 Reduces Allodynia and Spinal ERK Phosphorylation Following Chronic Compression of Dorsal Root Ganglion in Rats. Korean J Physiol Pharmacol 2010, 14:359-364. 10.4196/kjpp.2010.14.6.359, 3034114, 21311675.
52. Hammond DL, Ackerman L, Holdsworth R, Elzey B. Effects of spinal nerve ligation on immunohistochemically identified neurons in the L4 and L5 dorsal root ganglia of the rat. J Comp Neurol 2004, 475:575-589. 10.1002/cne.20209, 15236238.
53. Aanonsen LM, Seybold VS. Phencyclidine and sigma receptors in rat spinal cord: binding characterization and quantitative autoradiography. Synapse 1989, 4:1-10. 10.1002/syn.890040102, 2549651.
54. McCann DJ, Su TP. Haloperidol competitively inhibits the binding of (+)-[3H]SKF-10,047 to sigma sites. Eur J Pharmacol 1990, 180:361-364. 10.1016/0014-2999(90)90322-W, 2163868.
55. Gundlach AL, Largent BL, Snyder SH. Autoradiographic localization of sigma receptor binding sites in guinea pig and rat central nervous system with (+)3H-3-(3-hydroxyphenyl)-N-(1-propyl)piperidine. J Neurosci 1986, 6:1757-1770.
56. Su TP, Hayashi T, Maurice T, Buch S, Ruoho AE. The sigma-1 receptor chaperone as an inter-organelle signaling modulator. Trends Pharmacol Sci 2010, 31:557-566. 10.1016/j.tips.2010.08.007, 2993063, 20869780.
57. Kourrich S, Su TP, Fujimoto M, Bonci A. The sigma-1 receptor: roles in neuronal plasticity and disease. Trends Neurosci 2012, 35:762-771. 10.1016/j.tins.2012.09.007, 23102998.
58. Fukuoka T, Tokunaga A, Kondo E, Miki K, Tachibana T, Noguchi K. Change in mRNAs for neuropeptides and the GABA(A) receptor in dorsal root ganglion neurons in a rat experimental neuropathic pain model. Pain 1998, 78:13-26. 10.1016/S0304-3959(98)00111-0, 9822208.
59. Fukuoka T, Tokunaga A, Kondo E, Noguchi K. The role of neighboring intact dorsal root ganglion neurons in a rat neuropathic pain model. Proceedings of the 9th world congress on pain 2000, 137-146. Seattle, WA: IASP Press, Dever M, Rowbotham MC, Weisenfeld-Hallin Z, 1.
60. Murinson BB, Griffin JW. C-fiber structure varies with location in peripheral nerve. J Neuropathol Exp Neurol 2004, 63:246-254.
61. Wu G, Ringkamp M, Hartke TV, Murinson BB, Campbell JN, Griffin JW, Meyer RA. Early onset of spontaneous activity in uninjured C-fiber nociceptors after injury to neighboring nerve fibers. J Neurosci 2001, 21:RC140.
62. Ossipov MH, Porreca F. Neuropathic pain: basic mechansim (animal). 2009, 833-855. Oxford, UK: Elsevier, Basbaum AI, Bushnell MC, first, Science of Pain.
63. Cendan CM, Pujalte JM, Portillo-Salido E, Montoliu L, Baeyens JM. Formalin-induced pain is reduced in sigma(1) receptor knockout mice. Eur J Pharmacol 2005, 511:73-74. 10.1016/j.ejphar.2005.01.036, 15777781.
64. Entrena JM, Cobos EJ, Nieto FR, Cendan CM, Gris G, Del Pozo E, Zamanillo D, Baeyens JM. Sigma-1 receptors are essential for capsaicin-induced mechanical hypersensitivity: studies with selective sigma-1 ligands and sigma-1 knockout mice. Pain 2009, 143:252-261. 10.1016/j.pain.2009.03.011, 19375855.
65. de la Puente B, Nadal X, Portillo-Salido E, Sanchez-Arroyos R, Ovalle S, Palacios G, Muro A, Romero L, Entrena JM, Baeyens JM, et al. Sigma-1 receptors regulate activity-induced spinal sensitization and neuropathic pain after peripheral nerve injury. Pain 2009, 145:294-303. 10.1016/j.pain.2009.05.013, 19505761.
66. Kibaly C, Meyer L, Patte-Mensah C, Mensah-Nyagan AG. Biochemical and functional evidence for the control of pain mechanisms by dehydroepiandrosterone endogenously synthesized in the spinal cord. Faseb J 2008, 22:93-104.
67. Penas C, Pascual-Font A, Mancuso R, Fores J, Casas C, Navarro X. Sigma receptor agonist 2-(4-morpholinethyl)1 phenylcyclohexanecarboxylate (Pre084) increases GDNF and BiP expression and promotes neuroprotection after root avulsion injury. J Neurotrauma 2011, 28:831-840. 10.1089/neu.2010.1674, 21332255.
68. Ruscher K, Shamloo M, Rickhag M, Ladunga I, Soriano L, Gisselsson L, Toresson H, Ruslim-Litrus L, Oksenberg D, Urfer R, et al. The sigma-1 receptor enhances brain plasticity and functional recovery after experimental stroke. Brain 2011, 134:732-746. 10.1093/brain/awq367, 21278085.
69. Hall AK, Landis SC. Division and migration of satellite glia in the embryonic rat superior cervical ganglion. J Neurocytol 1992, 21:635-647. 10.1007/BF01191725, 1403009.
70. Shen YC, Wang YH, Chou YC, Liou KT, Yen JC, Wang WY, Liao JF. Dimemorfan protects rats against ischemic stroke through activation of sigma-1 receptor-mediated mechanisms by decreasing glutamate accumulation. J Neurochem 2008, 104:558-572.
71. Behensky AA, Cortes-Salva M, Seminerio MJ, Matsumoto RR, Antilla JC, Cuevas J. In vitro evaluation of guanidine analogs as sigma receptor ligands for potential anti-stroke therapeutics. J Pharmacol Exp Ther 2013, 344:155-166. 10.1124/jpet.112.199513, 23065135.
72. Moon JY, Roh DH, Yoon SY, Kang SY, Choi SR, Kwon SG, Choi HS, Han HJ, Beitz AJ, Lee JH. Sigma-1 receptor-mediated increase in spinal p38 MAPK phosphorylation leads to the induction of mechanical allodynia in mice and neuropathic rats. Exp Neurol 2013, 247:383-391.
73. Kim SH, Chung JM. An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 1992, 50:355-363. 10.1016/0304-3959(92)90041-9, 1333581.
74. Hogan Q, Sapunar D, Modric-Jednacak K, McCallum JB. Detection of neuropathic pain in a rat model of peripheral nerve injury. Anesthesiology 2004, 101:476-487. 10.1097/00000542-200408000-00030, 15277932.
75. Wu HE, Gemes G, Zoga V, Kawano T, Hogan QH. Learned avoidance from noxious mechanical simulation but not threshold semmes weinstein filament stimulation after nerve injury in rats. J Pain 2010, 11:280-286. 10.1016/j.jpain.2009.07.011, 2891524, 19945356.
76. Bangaru ML, Park F, Hudmon A, McCallum JB, Hogan QH. Quantification of gene expression after painful nerve injury: validation of optimal reference genes. J Mol Neurosci 2012, 46:497-504. 10.1007/s12031-011-9628-x, 3273664, 21863315.
77. Hayashi T, Lewis A, Hayashi E, Betenbaugh MJ, Su TP. Antigen retrieval to improve the immunocytochemistry detection of sigma-1 receptors and ER chaperones. Histochem Cell Biol 2011, 135:627-637. 10.1007/s00418-011-0811-5, 3155709, 21573736.
78. Stemkowski PL, Smith PA. Long-term IL-1beta exposure causes subpopulation-dependent alterations in rat dorsal root ganglion neuron excitability. J Neurophysiol 2012, 107:1586-1597. 10.1152/jn.00587.2011, 22170966.
79. Obata K, Katsura H, Mizushima T, Sakurai J, Kobayashi K, Yamanaka H, Dai Y, Fukuoka T, Noguchi K. Roles of extracellular signal-regulated protein kinases 5 in spinal microglia and primary sensory neurons for neuropathic pain. J Neurochem 2007, 102:1569-1584. 10.1111/j.1471-4159.2007.04656.x, 17509087.