Skip to main content
Top
Published in: Molecular Pain 1/2013

Open Access 01-12-2013 | Research

Brain-derived neurotrophic factor enhances the excitability of small-diameter trigeminal ganglion neurons projecting to the trigeminal nucleus interpolaris/caudalis transition zone following masseter muscle inflammation

Authors: Mamoru Takeda, Masayuki Takahashi, Junichi Kitagawa, Takuya Kanazawa, Masanori Nasu, Shigeji Matsumoto

Published in: Molecular Pain | Issue 1/2013

Login to get access

Abstract

Background

The trigeminal subnuclei interpolaris/caudalis transition zones (Vi/Vc) play an important role in orofacial deep pain, however, the role of primary afferent projections to the Vi/Vc remains to be determined. This study investigated the functional significance of hyperalgesia to the brain-derived neurotrophic factor (BDNF)-tyrosine kinase B (trkB) signaling system in trigeminal ganglion (TRG) neurons projecting to the Vi/Vc transition zone following masseter muscle (MM) inflammation.

Results

The escape threshold from mechanical stimulation applied to skin above the inflamed MM was significantly lower than in naïve rats. Fluorogold (FG) labeling was used to identify the TRG neurons innervating the MM, while microbeads (MB) were used to label neurons projecting to the Vi/Vc region. FG/MB-labeled TRG neurons were immunoreactive (IR) for BDNF and trkB. The mean number of BDNF/trkB-IR small/medium-diameter TRG neurons was significantly higher in inflamed rats than in naïve rats. In whole-cell current-clamp experiments, the majority of dissociated small-diameter TRG neurons showed a depolarization response to BDNF that was associated with spike discharge, and the concentration of BDNF that evoked a depolarizing response was significantly lower in the inflamed rats. In addition, the relative number of BDNF-induced spikes during current injection was significantly higher in inflamed rats. The BDNF-induced changes in TRG neuron excitability was abolished by tyrosine kinase inhibitor, K252a.

Conclusion

The present study provided evidence that BDNF enhances the excitability of the small-diameter TRG neurons projecting onto the Vi/Vc following MM inflammation. These findings suggest that ganglionic BDNF-trkB signaling is a therapeutic target for the treatment of trigeminal inflammatory hyperalgesia.
Appendix
Available only for authorised users
Literature
1.
go back to reference Bereiter DA, Bereiter DF: Morphine and NMDA receptor antagonism reduce c-fos expression in spinal trigeminal nucleus produced by acute injury to TMJ region. Pain 2000, 85: 65–77. 10.1016/S0304-3959(99)00246-8CrossRefPubMed Bereiter DA, Bereiter DF: Morphine and NMDA receptor antagonism reduce c-fos expression in spinal trigeminal nucleus produced by acute injury to TMJ region. Pain 2000, 85: 65–77. 10.1016/S0304-3959(99)00246-8CrossRefPubMed
2.
go back to reference Sessle BJ: Acute and chronic craniofacial pain: brainstem mechanisms of nociceptive transmission and neuroplasticity and their clinical correlates. Crit Rev Oral Biol Med 2000, 11: 57–91. 10.1177/10454411000110010401CrossRefPubMed Sessle BJ: Acute and chronic craniofacial pain: brainstem mechanisms of nociceptive transmission and neuroplasticity and their clinical correlates. Crit Rev Oral Biol Med 2000, 11: 57–91. 10.1177/10454411000110010401CrossRefPubMed
3.
go back to reference Bereiter DA, Shen S, Benetti AP: Sex differences in amino acid release from rostral trigeminal subnucleus caudalis after acute injury to the TMJ region. Pain 2002, 98: 89–99. 10.1016/S0304-3959(01)00476-6CrossRefPubMed Bereiter DA, Shen S, Benetti AP: Sex differences in amino acid release from rostral trigeminal subnucleus caudalis after acute injury to the TMJ region. Pain 2002, 98: 89–99. 10.1016/S0304-3959(01)00476-6CrossRefPubMed
4.
go back to reference Imbe H, Dubner R, Ren K: Masseteric inflammation-induced Fos protein expression in the trigeminal interpolaris/caudalis transition zone: contribution of somatosensory-vagal-adrenal integration. Brain Res 1999, 845: 165–175. 10.1016/S0006-8993(99)01913-7CrossRefPubMed Imbe H, Dubner R, Ren K: Masseteric inflammation-induced Fos protein expression in the trigeminal interpolaris/caudalis transition zone: contribution of somatosensory-vagal-adrenal integration. Brain Res 1999, 845: 165–175. 10.1016/S0006-8993(99)01913-7CrossRefPubMed
5.
go back to reference Sugiyo S, Takemura M, Dubner R, Ren K: Trigeminal transition zone/rostral ventral medial medulla connections and facilitation of orofacial hyperalgesia after masseter muscle inflammation in rats. J Comp Neurol 2005, 493: 510–523. 10.1002/cne.20797CrossRefPubMed Sugiyo S, Takemura M, Dubner R, Ren K: Trigeminal transition zone/rostral ventral medial medulla connections and facilitation of orofacial hyperalgesia after masseter muscle inflammation in rats. J Comp Neurol 2005, 493: 510–523. 10.1002/cne.20797CrossRefPubMed
6.
7.
go back to reference Wang H, Wei F, Dubner R, Ren K: Selective distribution and function of primary afferent nociceptive inputs from deep muscle tissue to the brain stem trigeminal transition zone. J Comp Neurol 2006, 498: 390–402. 10.1002/cne.21062CrossRefPubMed Wang H, Wei F, Dubner R, Ren K: Selective distribution and function of primary afferent nociceptive inputs from deep muscle tissue to the brain stem trigeminal transition zone. J Comp Neurol 2006, 498: 390–402. 10.1002/cne.21062CrossRefPubMed
8.
go back to reference Amir R, Devor M: Chemically mediated cross-excitation in rat dorsal root ganglia. J Neurosci 1996, 16: 4733–4741.PubMed Amir R, Devor M: Chemically mediated cross-excitation in rat dorsal root ganglia. J Neurosci 1996, 16: 4733–4741.PubMed
9.
go back to reference Matsuka Y, Neubert JK, Maidment NT, Spigelman I: Concurrent release of ATP and substance P within guinea pig trigeminal ganglia in vivo. Brain Res 2001, 915: 248–255. 10.1016/S0006-8993(01)02888-8CrossRefPubMed Matsuka Y, Neubert JK, Maidment NT, Spigelman I: Concurrent release of ATP and substance P within guinea pig trigeminal ganglia in vivo. Brain Res 2001, 915: 248–255. 10.1016/S0006-8993(01)02888-8CrossRefPubMed
10.
go back to reference Takeda M, Tanimoto T, Ikeda M, Nasu M, Kadoi J, Shima Y, Ohta H, Matsumoto S: Temporomandibular joint inflammation potentiates the excitability of trigeminal root ganglion neurons innervating the facial skin in rats. J Neurophysiol 2005, 93: 2723–2738. 10.1152/jn.00631.2004CrossRefPubMed Takeda M, Tanimoto T, Ikeda M, Nasu M, Kadoi J, Shima Y, Ohta H, Matsumoto S: Temporomandibular joint inflammation potentiates the excitability of trigeminal root ganglion neurons innervating the facial skin in rats. J Neurophysiol 2005, 93: 2723–2738. 10.1152/jn.00631.2004CrossRefPubMed
11.
go back to reference Takeda M, Tanimoto T, Nasu M, Ikeda M, Kadoi J, Matsumoto S: Activation of NK1 receptor of trigeminal root ganglion via substance P paracrine mechanism contributes to the mechanical allodynia in the temporomandibular joint inflammation in rats. Pain 2005., 116: Takeda M, Tanimoto T, Nasu M, Ikeda M, Kadoi J, Matsumoto S: Activation of NK1 receptor of trigeminal root ganglion via substance P paracrine mechanism contributes to the mechanical allodynia in the temporomandibular joint inflammation in rats. Pain 2005., 116:
12.
go back to reference Takeda M, Takahashi M, Hara N, Matsumoto S: Glial cell line-derived Neurotrophic factor modulates the excitability of nociceptive trigeminal ganglion neurons via a paracrine mechanism following inflammation. Brain Behav Immun 2013, 28: 100–107. 375–385CrossRefPubMed Takeda M, Takahashi M, Hara N, Matsumoto S: Glial cell line-derived Neurotrophic factor modulates the excitability of nociceptive trigeminal ganglion neurons via a paracrine mechanism following inflammation. Brain Behav Immun 2013, 28: 100–107. 375–385CrossRefPubMed
13.
go back to reference Takeda M, Takahashi M, Matsumoto S: Contribution of activation of satellite glia in sensory ganglia to pathological pain. Neurosci Biobehav Rev 2009, 33: 784–792. 10.1016/j.neubiorev.2008.12.005CrossRefPubMed Takeda M, Takahashi M, Matsumoto S: Contribution of activation of satellite glia in sensory ganglia to pathological pain. Neurosci Biobehav Rev 2009, 33: 784–792. 10.1016/j.neubiorev.2008.12.005CrossRefPubMed
14.
go back to reference Takeda M, Takahashi M, Matsumoto S: Suppression of neurokinin-1 receptor in trigeminal ganglia attenuates central sensitization following inflammation. J Peripher Nev Syst 2012, 17: 169–181. 10.1111/j.1529-8027.2012.00404.xCrossRef Takeda M, Takahashi M, Matsumoto S: Suppression of neurokinin-1 receptor in trigeminal ganglia attenuates central sensitization following inflammation. J Peripher Nev Syst 2012, 17: 169–181. 10.1111/j.1529-8027.2012.00404.xCrossRef
15.
go back to reference Pezet S, Malcangio M, McMahorn SB: BDNF: a neuromodulator in nociceptive pathways ? Brain Res Rev 2002, 40: 240–249. 10.1016/S0165-0173(02)00206-0CrossRefPubMed Pezet S, Malcangio M, McMahorn SB: BDNF: a neuromodulator in nociceptive pathways ? Brain Res Rev 2002, 40: 240–249. 10.1016/S0165-0173(02)00206-0CrossRefPubMed
16.
go back to reference Matayoshi S, Jiang N, Katafuchi T, Koga K, Furue H, Yasaka T, Nakatsuka T, Zhou XF, Kawasaki Y, Tanaka N, Yoshimura M: Actions of brain-derived Neurotrophic factor on spinal nociceptive transmission during inflammation in the rat. J Physiol 2005, 569: 685–695. 10.1113/jphysiol.2005.095331PubMedCentralCrossRefPubMed Matayoshi S, Jiang N, Katafuchi T, Koga K, Furue H, Yasaka T, Nakatsuka T, Zhou XF, Kawasaki Y, Tanaka N, Yoshimura M: Actions of brain-derived Neurotrophic factor on spinal nociceptive transmission during inflammation in the rat. J Physiol 2005, 569: 685–695. 10.1113/jphysiol.2005.095331PubMedCentralCrossRefPubMed
17.
go back to reference Obata K, Noguchi K: BDNF in sensory neurons and chronic pain. Neurosci Res 2006, 55: 1–10. 10.1016/j.neures.2006.01.005CrossRefPubMed Obata K, Noguchi K: BDNF in sensory neurons and chronic pain. Neurosci Res 2006, 55: 1–10. 10.1016/j.neures.2006.01.005CrossRefPubMed
18.
go back to reference Ren K, Dubner R: Pain facilitation and activity-dependent plasticity in pain modulatory circuitry: role of BDNF-trkB signaling and NMDA receptors. Mol Neurobiol 2007, 35: 224–235. 10.1007/s12035-007-0028-8CrossRefPubMed Ren K, Dubner R: Pain facilitation and activity-dependent plasticity in pain modulatory circuitry: role of BDNF-trkB signaling and NMDA receptors. Mol Neurobiol 2007, 35: 224–235. 10.1007/s12035-007-0028-8CrossRefPubMed
19.
go back to reference Zhou XF, Rush RA: Endogenous brain-derived Neurotrophic factor is anterogradely transported primary sensory neurons. Neuroscience 1996, 74: 945–953.CrossRefPubMed Zhou XF, Rush RA: Endogenous brain-derived Neurotrophic factor is anterogradely transported primary sensory neurons. Neuroscience 1996, 74: 945–953.CrossRefPubMed
20.
go back to reference Thompson SW, Bennett DL, Ker BJ, Bradbury EJ, McMahon SB: Brain-derived Neurotrophic factor is an endogenous modulator of nociceptive responses in the spinal cord. Proc Natl Acad Sci USA 1999, 96: 7714–7718. 10.1073/pnas.96.14.7714PubMedCentralCrossRefPubMed Thompson SW, Bennett DL, Ker BJ, Bradbury EJ, McMahon SB: Brain-derived Neurotrophic factor is an endogenous modulator of nociceptive responses in the spinal cord. Proc Natl Acad Sci USA 1999, 96: 7714–7718. 10.1073/pnas.96.14.7714PubMedCentralCrossRefPubMed
21.
go back to reference Wetmore C, Olson L: Neuronal and nonneuronal expression of neurotrophins and their receptor in sensory and sympathetic ganglia suggest new intracellular trophic interactions. J Comp Neurol 1995, 353: 143–159. 10.1002/cne.903530113CrossRefPubMed Wetmore C, Olson L: Neuronal and nonneuronal expression of neurotrophins and their receptor in sensory and sympathetic ganglia suggest new intracellular trophic interactions. J Comp Neurol 1995, 353: 143–159. 10.1002/cne.903530113CrossRefPubMed
22.
go back to reference Buldyrev T, Tanner NM, Hsieh HY, Dodd EG, Nguyen LT, Balkowiec A: Calcitonin gene-related peptide enhances release of native brain derived neurotorophic factor from trigeminal ganglion neurons. J Neurochem 2006, 99: 1338–1350. 10.1111/j.1471-4159.2006.04161.xPubMedCentralCrossRefPubMed Buldyrev T, Tanner NM, Hsieh HY, Dodd EG, Nguyen LT, Balkowiec A: Calcitonin gene-related peptide enhances release of native brain derived neurotorophic factor from trigeminal ganglion neurons. J Neurochem 2006, 99: 1338–1350. 10.1111/j.1471-4159.2006.04161.xPubMedCentralCrossRefPubMed
23.
go back to reference Behnia A, Zhang L, Charles M, Gold MS: Changes in trkB-like immunoreactivity in rat trigeminal ganglion after tooth injury. J Endo 2003, 29: 135–140. 10.1097/00004770-200302000-00012CrossRef Behnia A, Zhang L, Charles M, Gold MS: Changes in trkB-like immunoreactivity in rat trigeminal ganglion after tooth injury. J Endo 2003, 29: 135–140. 10.1097/00004770-200302000-00012CrossRef
24.
go back to reference Tarsa L, Balkowiec-Iskra E, Kratochvil FJ 3rd, Jenkins VK, McLean A, Brown A, Smith JA, Baumgartner JC, Balkowiec A: Tooth pulp inflammation increases brain-derived Neurotrophic factor expression in rodent trigeminal ganglion neurons. Neuroscience 2010, 167: 1205–1215. 10.1016/j.neuroscience.2010.03.002PubMedCentralCrossRefPubMed Tarsa L, Balkowiec-Iskra E, Kratochvil FJ 3rd, Jenkins VK, McLean A, Brown A, Smith JA, Baumgartner JC, Balkowiec A: Tooth pulp inflammation increases brain-derived Neurotrophic factor expression in rodent trigeminal ganglion neurons. Neuroscience 2010, 167: 1205–1215. 10.1016/j.neuroscience.2010.03.002PubMedCentralCrossRefPubMed
25.
go back to reference Zimmermann M: Ethical guidelines for investigations of experimental pain in conscious animals. Pain 1983, 16: 109–110. 10.1016/0304-3959(83)90201-4CrossRefPubMed Zimmermann M: Ethical guidelines for investigations of experimental pain in conscious animals. Pain 1983, 16: 109–110. 10.1016/0304-3959(83)90201-4CrossRefPubMed
26.
go back to reference Takeda M, Tanimoto T, Ito M, Nasu M, Matsumoto S: Role of capsaicin-sensitive primary afferent inputs from the masseter muscle in the C 1 spinal neurons responding to tooth-pulp stimulation in rats. Exp Brain Res 2005, 160: 107–117. 10.1007/s00221-004-1990-2CrossRefPubMed Takeda M, Tanimoto T, Ito M, Nasu M, Matsumoto S: Role of capsaicin-sensitive primary afferent inputs from the masseter muscle in the C 1 spinal neurons responding to tooth-pulp stimulation in rats. Exp Brain Res 2005, 160: 107–117. 10.1007/s00221-004-1990-2CrossRefPubMed
27.
go back to reference Takeda M, Kadoi J, Takahashi M, Nasy M, Matsumoto S: Somatostatin inhibits the excitability of rat small-diameter trigeminal ganglion neurons that innervate nasal mucosa and project to upper cervical dorsal horn via activation of Somatostatin 2a receptor. Neuroscience 2007, 148: 744–756. 10.1016/j.neuroscience.2007.06.048CrossRefPubMed Takeda M, Kadoi J, Takahashi M, Nasy M, Matsumoto S: Somatostatin inhibits the excitability of rat small-diameter trigeminal ganglion neurons that innervate nasal mucosa and project to upper cervical dorsal horn via activation of Somatostatin 2a receptor. Neuroscience 2007, 148: 744–756. 10.1016/j.neuroscience.2007.06.048CrossRefPubMed
28.
go back to reference Phillips JK, Goodchild AK, Dubey R, Sesiashvili E, Takeda M, Chalmers PM, Pilowsky PM, Lipski J: Differential expression of catecholamine biosynthetic enzymes in the rat ventrolateral medulla. J Comp Neurol 2001, 431: 20–34.CrossRef Phillips JK, Goodchild AK, Dubey R, Sesiashvili E, Takeda M, Chalmers PM, Pilowsky PM, Lipski J: Differential expression of catecholamine biosynthetic enzymes in the rat ventrolateral medulla. J Comp Neurol 2001, 431: 20–34.CrossRef
29.
go back to reference Paxinos G, Watson C: The Rat brain in stereotaxic coordinates, compact. 6th edition. Sydney: Academic; 2009. Paxinos G, Watson C: The Rat brain in stereotaxic coordinates, compact. 6th edition. Sydney: Academic; 2009.
30.
go back to reference Takeda M, Tanimoto T, Ikeda M, Nasu M, Kadoi J, Yoshida S, Matsumoto S: Enhanced excitability of rat trigeminal root ganglion neurons via decrease in a-type potassium currents following temporomandibular joint inflammation. Neuroscience 2006, 138: 621–630. 10.1016/j.neuroscience.2005.11.024CrossRefPubMed Takeda M, Tanimoto T, Ikeda M, Nasu M, Kadoi J, Yoshida S, Matsumoto S: Enhanced excitability of rat trigeminal root ganglion neurons via decrease in a-type potassium currents following temporomandibular joint inflammation. Neuroscience 2006, 138: 621–630. 10.1016/j.neuroscience.2005.11.024CrossRefPubMed
31.
go back to reference Greg JM, Dixon AD: Somatotopic organization of the trigeminal ganglion in the rat. Arch Oral Biol 1993, 18: 487–498.CrossRef Greg JM, Dixon AD: Somatotopic organization of the trigeminal ganglion in the rat. Arch Oral Biol 1993, 18: 487–498.CrossRef
32.
go back to reference Zhang YH, Chi XX, Nicol GD: Brain derived Neurotrophic factor enhances the excitability of rat sensory neurons through activation of the p75 neurotrophin receptor and the sphingomyelin pathway. J Physiol 2008, 586: 3113–3127. 10.1113/jphysiol.2008.152439PubMedCentralCrossRefPubMed Zhang YH, Chi XX, Nicol GD: Brain derived Neurotrophic factor enhances the excitability of rat sensory neurons through activation of the p75 neurotrophin receptor and the sphingomyelin pathway. J Physiol 2008, 586: 3113–3127. 10.1113/jphysiol.2008.152439PubMedCentralCrossRefPubMed
33.
go back to reference Drake-Baumann R: Rapid modulation of inhibitory synaptic currents in cerebellar purkinje cells by BDNF. Synapse 2005, 57: 183–190. 10.1002/syn.20170CrossRefPubMed Drake-Baumann R: Rapid modulation of inhibitory synaptic currents in cerebellar purkinje cells by BDNF. Synapse 2005, 57: 183–190. 10.1002/syn.20170CrossRefPubMed
34.
go back to reference Waddell PJ, Lawson SN: Electrophysiological properties of subpopulations of rat dorsal root ganglion neurons in vitro. Neuroscience 1990, 1036: 811–822.CrossRef Waddell PJ, Lawson SN: Electrophysiological properties of subpopulations of rat dorsal root ganglion neurons in vitro. Neuroscience 1990, 1036: 811–822.CrossRef
35.
go back to reference Ritter AM, Mendell LM: Somal membrane properties of physiologically identified sensory neurons in the rat: effects of nerve growth factor. J Neurophysiol 1992, 68: 2033–2041.PubMed Ritter AM, Mendell LM: Somal membrane properties of physiologically identified sensory neurons in the rat: effects of nerve growth factor. J Neurophysiol 1992, 68: 2033–2041.PubMed
36.
go back to reference Moore BA, Stewart TMR, Hill C, Vanner SJ: TNBS ileitis evokes hyperexcitability and changes in ionic membrane properties of nociceptive DRG neurons. Am J Physiol Gastrointest Liver Physiol 2002, 282: G1045-G1051.CrossRefPubMed Moore BA, Stewart TMR, Hill C, Vanner SJ: TNBS ileitis evokes hyperexcitability and changes in ionic membrane properties of nociceptive DRG neurons. Am J Physiol Gastrointest Liver Physiol 2002, 282: G1045-G1051.CrossRefPubMed
37.
go back to reference Wang H, Guo W, Yang K, Wei F, Dubner R, Ren K: Contribution of primary afferent input to trigeminal astroglial hyperactivity, cytokine induction and NMDA receptor phosphorylation. Open Pain J 2010, 3: 144–152.CrossRef Wang H, Guo W, Yang K, Wei F, Dubner R, Ren K: Contribution of primary afferent input to trigeminal astroglial hyperactivity, cytokine induction and NMDA receptor phosphorylation. Open Pain J 2010, 3: 144–152.CrossRef
38.
go back to reference Michael GJ, Averill S, Nitkunan A, Rattray M, Bennett DL, Yan Q, Priestley JV: Nerve growth factor treatment increases brain-derived Neurotrophic factor selectively in trkA-expressing dorsal root ganglion cells and in their central termination within the spinal cord. J Neurosci 1997, 17: 8476–8490.PubMed Michael GJ, Averill S, Nitkunan A, Rattray M, Bennett DL, Yan Q, Priestley JV: Nerve growth factor treatment increases brain-derived Neurotrophic factor selectively in trkA-expressing dorsal root ganglion cells and in their central termination within the spinal cord. J Neurosci 1997, 17: 8476–8490.PubMed
39.
go back to reference Li WP, Xian C, Rush RA, Zhou XF: Upregulation of brain-derived Neurotrophic factor and Neuropeptide Y in the dorsal ascending sensory pathway following sciatic nerve injury in rat. Neurosci Lett 1999, 260: 49–52. 10.1016/S0304-3940(98)00958-6CrossRefPubMed Li WP, Xian C, Rush RA, Zhou XF: Upregulation of brain-derived Neurotrophic factor and Neuropeptide Y in the dorsal ascending sensory pathway following sciatic nerve injury in rat. Neurosci Lett 1999, 260: 49–52. 10.1016/S0304-3940(98)00958-6CrossRefPubMed
40.
go back to reference Kafitz KW, Rose CR, Thoenen H, Konnerth A: Neurotrophin-evoked rapid excitation through trkB receptor. Nature 1999, 401: 918–921. 10.1038/44847CrossRefPubMed Kafitz KW, Rose CR, Thoenen H, Konnerth A: Neurotrophin-evoked rapid excitation through trkB receptor. Nature 1999, 401: 918–921. 10.1038/44847CrossRefPubMed
41.
go back to reference Mannion RJ, Costigan M, Decosterd I, Amaya F, Ma QP, Holstege JC, Ji RR, Acheson A, Lindsay RM, Wilkinson GA, Woolf CJ: Neurotrophins: peripherally and centrally acting modulators of tactile stimulus induced inflammatory pain hypersensitivity. Proc Natl Acad Sci USA 1999, 96: 9385–9390. 10.1073/pnas.96.16.9385PubMedCentralCrossRefPubMed Mannion RJ, Costigan M, Decosterd I, Amaya F, Ma QP, Holstege JC, Ji RR, Acheson A, Lindsay RM, Wilkinson GA, Woolf CJ: Neurotrophins: peripherally and centrally acting modulators of tactile stimulus induced inflammatory pain hypersensitivity. Proc Natl Acad Sci USA 1999, 96: 9385–9390. 10.1073/pnas.96.16.9385PubMedCentralCrossRefPubMed
42.
go back to reference Lever IJ, Bradbury EJ, Cunningham JR, Adelson DW, Jones MG, Mc Mahon SB, Marvizon JC, Malcangio M: Brain-derived Neurotrophic factor is released in the dorsal horn by distinctive patterns of afferent fiber stimulation. J Neurosci 2001, 21: 4469–4477.PubMed Lever IJ, Bradbury EJ, Cunningham JR, Adelson DW, Jones MG, Mc Mahon SB, Marvizon JC, Malcangio M: Brain-derived Neurotrophic factor is released in the dorsal horn by distinctive patterns of afferent fiber stimulation. J Neurosci 2001, 21: 4469–4477.PubMed
43.
go back to reference Gunjigake KK, Got T, Nakano K, Konoo T, Kobayashi S, Yamaguchi K: Correlation between the appearance of neuropeptides in the rat trigeminal ganglion and reinnervation of healing root socket tooth extraction. Acta Histochem 2006, 39: 69–77.CrossRef Gunjigake KK, Got T, Nakano K, Konoo T, Kobayashi S, Yamaguchi K: Correlation between the appearance of neuropeptides in the rat trigeminal ganglion and reinnervation of healing root socket tooth extraction. Acta Histochem 2006, 39: 69–77.CrossRef
44.
go back to reference Ichikawa H, Yabuuchi T, Jin HW, Terayama R, Yamaai T, Deguchi T, Kamioka H, Takani-Yamamoto T, Sugimoto T: Brain-derived Neurotrophic factor-immunoreactive primary sensory neurons in the trigeminal ganglion and trigeminal sensory nucleus. Brain Res 2006, 1081: 113–118. 10.1016/j.brainres.2006.01.027CrossRefPubMed Ichikawa H, Yabuuchi T, Jin HW, Terayama R, Yamaai T, Deguchi T, Kamioka H, Takani-Yamamoto T, Sugimoto T: Brain-derived Neurotrophic factor-immunoreactive primary sensory neurons in the trigeminal ganglion and trigeminal sensory nucleus. Brain Res 2006, 1081: 113–118. 10.1016/j.brainres.2006.01.027CrossRefPubMed
45.
go back to reference Lee SL, Kim JK, Kim DS, Cho HJ: Expression of mRNAs encoding full-length and truncated TrkB receptors in rat dorsal root ganglia and spinal cord following peripheral inflammation. Neuroreport 1999, 9: 2847–2851.CrossRef Lee SL, Kim JK, Kim DS, Cho HJ: Expression of mRNAs encoding full-length and truncated TrkB receptors in rat dorsal root ganglia and spinal cord following peripheral inflammation. Neuroreport 1999, 9: 2847–2851.CrossRef
46.
go back to reference Cho HJ, Kim SY, Park MJ, Kin DS, Kim JK, Chu MY: Expression of mRNA for brain-derived Neurotrophic factor in the dorsal root ganglion following peripheral inflammation. Brain Res 1997, 749: 358–362. 10.1016/S0006-8993(97)00048-6CrossRefPubMed Cho HJ, Kim SY, Park MJ, Kin DS, Kim JK, Chu MY: Expression of mRNA for brain-derived Neurotrophic factor in the dorsal root ganglion following peripheral inflammation. Brain Res 1997, 749: 358–362. 10.1016/S0006-8993(97)00048-6CrossRefPubMed
47.
go back to reference Watkins LR, Maier SF: Beyond neurons: evidence that immune and glial cells contribute to pathological pain states. Physiol Rev 2001, 82: 981–1011.CrossRef Watkins LR, Maier SF: Beyond neurons: evidence that immune and glial cells contribute to pathological pain states. Physiol Rev 2001, 82: 981–1011.CrossRef
48.
go back to reference Balkowiec-Iskra E, Vermehren-Schmadeick A, Balkowiec A: Tumor necrosis factor -α increases brain-deribed Neurotrophic factor expression in trigeminal ganglion neurons in an activity-dependent manner. Neuroscience 2011, 180: 322–333.PubMedCentralCrossRefPubMed Balkowiec-Iskra E, Vermehren-Schmadeick A, Balkowiec A: Tumor necrosis factor -α increases brain-deribed Neurotrophic factor expression in trigeminal ganglion neurons in an activity-dependent manner. Neuroscience 2011, 180: 322–333.PubMedCentralCrossRefPubMed
49.
go back to reference Lin YT, Ro LS, Wang HL, Chen JC: Upregulation of dorsal root ganglia BDNF and trkB receptor in inflammatory pain: an in vivo and in vitro study. J Neuroinflammation 2011, 8: 126. 10.1186/1742-2094-8-126PubMedCentralCrossRefPubMed Lin YT, Ro LS, Wang HL, Chen JC: Upregulation of dorsal root ganglia BDNF and trkB receptor in inflammatory pain: an in vivo and in vitro study. J Neuroinflammation 2011, 8: 126. 10.1186/1742-2094-8-126PubMedCentralCrossRefPubMed
50.
go back to reference Balkowiec A, Katz DM: Activity-dependent release of endogenous brain-deribed Neurotrophic factor from primary sensory neurons detected by Elisa in situ . J Neurosci 2000, 20: 7417–7423.PubMed Balkowiec A, Katz DM: Activity-dependent release of endogenous brain-deribed Neurotrophic factor from primary sensory neurons detected by Elisa in situ . J Neurosci 2000, 20: 7417–7423.PubMed
51.
go back to reference Trueta C, De-Miguel FF: Extrasynaptic exocytosis and its mechanism: a source of molecules mediating volume transmission in the nervous system. Front Physiol 2012, 3: 319.PubMedCentralPubMed Trueta C, De-Miguel FF: Extrasynaptic exocytosis and its mechanism: a source of molecules mediating volume transmission in the nervous system. Front Physiol 2012, 3: 319.PubMedCentralPubMed
52.
go back to reference Rose CR, Blum R, Kafitz KW, Kovalchuk Y: Konnerth: from modulator to mediator: rapid effects of BDNF on ion channels. Bioassays 2004, 26: 1185–1194. 10.1002/bies.20118CrossRef Rose CR, Blum R, Kafitz KW, Kovalchuk Y: Konnerth: from modulator to mediator: rapid effects of BDNF on ion channels. Bioassays 2004, 26: 1185–1194. 10.1002/bies.20118CrossRef
53.
go back to reference Takeda M, Kitagawa J, Takahashi M, Iwata K, Mastsumoto S: Glial cell line-derived Neurotrophic factor acutely modulates the excitability of rat small-diameter trigeminal ganglion neurons innervating facial skin. Brain Behav Immun 2010, 24: 72–82. 10.1016/j.bbi.2009.08.002CrossRefPubMed Takeda M, Kitagawa J, Takahashi M, Iwata K, Mastsumoto S: Glial cell line-derived Neurotrophic factor acutely modulates the excitability of rat small-diameter trigeminal ganglion neurons innervating facial skin. Brain Behav Immun 2010, 24: 72–82. 10.1016/j.bbi.2009.08.002CrossRefPubMed
54.
go back to reference Chao MV: Neurotrophins and their receptors: a convergence point for many signaling pathways. Nat Neurosci 2003, 4: 299–309.CrossRef Chao MV: Neurotrophins and their receptors: a convergence point for many signaling pathways. Nat Neurosci 2003, 4: 299–309.CrossRef
55.
go back to reference Cao XH, Byum HS, Chen SR, Cai YQ, Pan HL: Reduction in voltage-gated K + channel activity in primary sensory neurons in painful diabetic neuropathy: role of brain derived Neurotrophic factor. J Neurochemistry 2010, 114: 1460–1475. Cao XH, Byum HS, Chen SR, Cai YQ, Pan HL: Reduction in voltage-gated K + channel activity in primary sensory neurons in painful diabetic neuropathy: role of brain derived Neurotrophic factor. J Neurochemistry 2010, 114: 1460–1475.
56.
go back to reference Hille B: Potassium channels and chloride channels. In Ion channels of excitable membranes. 3rd edition. Edited by: Hille B. Sunderland, Massachusetts: Sinauer Associates; 2001:134–167. Hille B: Potassium channels and chloride channels. In Ion channels of excitable membranes. 3rd edition. Edited by: Hille B. Sunderland, Massachusetts: Sinauer Associates; 2001:134–167.
57.
go back to reference Takeda M, Kitagawa J, Takahashi M, Mastsumoto S: Activation of interleukin-1β receptor suppresses the voltage-gated potassium currents in the small-diameter trigeminal ganglion neurons following peripheral inflammation. Pain 2008, 139: 594–602. 10.1016/j.pain.2008.06.015CrossRefPubMed Takeda M, Kitagawa J, Takahashi M, Mastsumoto S: Activation of interleukin-1β receptor suppresses the voltage-gated potassium currents in the small-diameter trigeminal ganglion neurons following peripheral inflammation. Pain 2008, 139: 594–602. 10.1016/j.pain.2008.06.015CrossRefPubMed
58.
go back to reference Yossoufian M, Walmsley B: Brain-derived Neurotrophic factor modulates cell excitability in the mouse medial nucleus of trapezoid body. Eur J Neurosci 2007, 25: 1647–1652. 10.1111/j.1460-9568.2007.05428.xCrossRef Yossoufian M, Walmsley B: Brain-derived Neurotrophic factor modulates cell excitability in the mouse medial nucleus of trapezoid body. Eur J Neurosci 2007, 25: 1647–1652. 10.1111/j.1460-9568.2007.05428.xCrossRef
59.
go back to reference Guo W, Robbins MT, We F, Zou S, Dubner R, Ren K: Supraspinal brain-derived Neurotrophic factor signaling: a novel mechanism for descending pain facilitation. J Neurosci 2006, 26: 126–137. 10.1523/JNEUROSCI.3686-05.2006CrossRefPubMed Guo W, Robbins MT, We F, Zou S, Dubner R, Ren K: Supraspinal brain-derived Neurotrophic factor signaling: a novel mechanism for descending pain facilitation. J Neurosci 2006, 26: 126–137. 10.1523/JNEUROSCI.3686-05.2006CrossRefPubMed
60.
go back to reference Devor M, Wall PD: Cross-excitation in dorsal root ganglia of nerve-injured and intact rats. J Neurophysiol 1990, 64: 1733–1746.PubMed Devor M, Wall PD: Cross-excitation in dorsal root ganglia of nerve-injured and intact rats. J Neurophysiol 1990, 64: 1733–1746.PubMed
61.
go back to reference Utzschneider D, Kocsis J, Devor M: Mutual excitation among dorsal root ganglion neurons in the rat. Neurosci Lett 1992, 146: 53–56. 10.1016/0304-3940(92)90170-CCrossRefPubMed Utzschneider D, Kocsis J, Devor M: Mutual excitation among dorsal root ganglion neurons in the rat. Neurosci Lett 1992, 146: 53–56. 10.1016/0304-3940(92)90170-CCrossRefPubMed
62.
go back to reference Oh EJ, Weinreich D: Chemical communication between vagal afferent somata in nodose ganglia of the rat and guinea pig in vitro. J Neurophysiol 2001, 2001(87):2801–2807. Oh EJ, Weinreich D: Chemical communication between vagal afferent somata in nodose ganglia of the rat and guinea pig in vitro. J Neurophysiol 2001, 2001(87):2801–2807.
Metadata
Title
Brain-derived neurotrophic factor enhances the excitability of small-diameter trigeminal ganglion neurons projecting to the trigeminal nucleus interpolaris/caudalis transition zone following masseter muscle inflammation
Authors
Mamoru Takeda
Masayuki Takahashi
Junichi Kitagawa
Takuya Kanazawa
Masanori Nasu
Shigeji Matsumoto
Publication date
01-12-2013
Publisher
BioMed Central
Published in
Molecular Pain / Issue 1/2013
Electronic ISSN: 1744-8069
DOI
https://doi.org/10.1186/1744-8069-9-49

Other articles of this Issue 1/2013

Molecular Pain 1/2013 Go to the issue