Journal of Dental Anesthesia and Pain Medicine

The Korean Dental Society of Anesthsiology (대한치과마취과학회)
권호 표지
DOI QR코드

DOI QR Code

Role of neuron and non-neuronal cell communication in persistent orofacial pain

  • Iwata, Koichi (Department of Physiology, Nihon University School of Dentistry) ;
  • Shinoda, Masamichi (Department of Physiology, Nihon University School of Dentistry)
  • Received : 2019.03.04
  • Accepted : 2019.04.07
  • Published : 2019.04.30
Download PDF
⟨ Previous Next ⟩

Abstract

It is well known that trigeminal nerve injury causes hyperexcitability in trigeminal ganglion neurons, which become sensitized. Long after trigeminal nerve damage, trigeminal spinal subnucleus caudalis and upper cervical spinal cord (C1/C2) nociceptive neurons become hyperactive and are sensitized, resulting in persistent orofacial pain. Communication between neurons and non-neuronal cells is believed to be involved in these mechanisms. In this article, the authors highlight several lines of evidence that neuron-glial cell and neuron macrophage communication have essential roles in persistent orofacial pain mechanisms associated with trigeminal nerve injury and/or orofacial inflammation.

Keywords

References

  1. Sessle BJ. The neurobiology of facial and dental pain: present knowledge, future directions. J Dent Res 1987; 66: 962-81. https://doi.org/10.1177/00220345870660052201
  2. Dubner R, Bennett GJ. Spinal and trigeminal mechanisms of nociception. Annu Rev Neurosci 1983; 6: 381-418. https://doi.org/10.1146/annurev.ne.06.030183.002121
  3. Bereiter DA, Hirata H, Hu JW. Trigeminal subnucleus caudalis: beyond homologies with the spinal dorsal horn. Pain 2000; 88: 221-4. https://doi.org/10.1016/S0304-3959(00)00434-6
  4. Herculano-Houzel S. The glia/neuron ratio: how it varies uniformly across brain structures and species and what that means for brain physiology and evolution. Glia 2014; 62: 1377-91. https://doi.org/10.1002/glia.22683
  5. Zhang ZJ, Jiang BC, Gao YJ. Chemokines in neuron-glial cell interaction and pathogenesis of neuropathic pain. Cell Mol Life Sci 2017; 74: 3275-91. https://doi.org/10.1007/s00018-017-2513-1
  6. Tsuboi Y, Takeda M, Tanimoto T, Ikeda M, Matsumoto S, Kitagawa J, et al. Alteration of the second branch of the trigeminal nerve activity following inferior alveolar nerve transection in rats. Pain 2004; 111: 323-34. https://doi.org/10.1016/j.pain.2004.07.014
  7. Batbold D, Shinoda M, Honda K, Furukawa A, Koizumi M, Akasaka R, et al. Macrophages in trigeminal ganglion contribute to ectopic mechanical hypersensitivity following inferior alveolar nerve injury in rats. J Neuroinflammation 2017; 14: 249. https://doi.org/10.1186/s12974-017-1022-3
  8. Pannese E. The satellite cells of the sensory ganglia. Adv Anat Embryol Cell Biol 1981; 65: 1-111. https://doi.org/10.1007/978-3-642-67750-2_1
  9. Li L, Zhou XF. Pericellular Griffonia simplicifolia I isolectin B4-binding ring structures in the dorsal root ganglia following peripheral nerve injury in rats. J Comp Neurol 2001; 439: 259-74. https://doi.org/10.1002/cne.1349
  10. Xie W, Strong JA, Meij JT, Zhang JM, Yu L. Neuropathic pain: early spontaneous afferent activity is the trigger. Pain 2005; 116: 243-56. https://doi.org/10.1016/j.pain.2005.04.017
  11. Xie W, Strong JA, Zhang JM. Early blockade of injured primary sensory afferents reduces glial cell activation in two rat neuropathic pain models. Neuroscience 2009; 160: 847-57. https://doi.org/10.1016/j.neuroscience.2009.03.016
  12. Kushnir R, Cherkas PS, Hanani M. Peripheral inflammation upregulates P2X receptor expression in satellite glial cells of mouse trigeminal ganglia: a calcium imaging study. Neuropharmacology 2011; 61: 739-46. https://doi.org/10.1016/j.neuropharm.2011.05.019
  13. Chessell IP, Hatcher JP, Bountra C, Michel AD, Hughes JP, Green P, et al. Disruption of the P2X7 purinoceptor gene abolishes chronic inflammatory and neuropathic pain. Pain 2005; 114: 386-96. https://doi.org/10.1016/j.pain.2005.01.002
  14. Gu Y, Chen Y, Zhang X, Li GW, Wang C, Huang LY. Neuronal soma-satellite glial cell interactions in sensory ganglia and the participation of purinergic receptors. Neuron Glia Biol 2010; 6: 53-62. https://doi.org/10.1017/S1740925X10000116
  15. Chen Y, Zhang X, Wang C, Li G, Gu Y, Huang LY. Activation of P2X7 receptors in glial satellite cells reduces pain through downregulation of P2X3 receptors in nociceptive neurons. Proc Natl Acad Sci U S A 2008; 105: 16773-8. https://doi.org/10.1073/pnas.0801793105
  16. Ceruti S, Fumagalli M, Villa G, Verderio C, Abbracchio MP. Purinoceptor-mediated calcium signaling in primary neuron-glia trigeminal cultures. Cell Calcium 2008; 43: 576-90. https://doi.org/10.1016/j.ceca.2007.10.003
  17. Xu JT, Xin WJ, Zang Y, Wu CY, Liu XG. The role of tumor necrosis factor-alpha in the neuropathic pain induced by Lumbar 5 ventral root transection in rat. Pain 2006; 123: 306-21. https://doi.org/10.1016/j.pain.2006.03.011
  18. Takeda M, Tanimoto T, Kadoi J, Nasu M, Takahashi M, Kitagawa J, et al. Enhanced excitability of nociceptive trigeminal ganglion neurons by satellite glial cytokine following peripheral inflammation. Pain 2007; 129: 155-66. https://doi.org/10.1016/j.pain.2006.10.007
  19. Takeda M, Takahashi M, Matsumoto S. Contribution of activated interleukin receptors in trigeminal ganglion neurons to hyperalgesia via satellite glial interleukin-1beta paracrine mechanism. Brain Behav Immun 2008; 22: 1016-23. https://doi.org/10.1016/j.bbi.2008.03.004
  20. Hensellek S, Brell P, Schaible HG, Brauer R, Segond von Banchet G. The cytokine TNFalpha increases the proportion of DRG neurones expressing the TRPV1 receptor via the TNFR1 receptor and ERK activation. Mol Cell Neurosci 2007; 36: 381-91. https://doi.org/10.1016/j.mcn.2007.07.010
  21. Chen X, Pang RP, Shen KF, Zimmermann M, Xin WJ, Li YY, et al. TNF-alpha enhances the currents of voltage gated sodium channels in uninjured dorsal root ganglion neurons following motor nerve injury. Exp Neurol 2011; 227: 279-86. https://doi.org/10.1016/j.expneurol.2010.11.017
  22. He XH, Zang Y, Chen X, Pang RP, Xu JT, Zhou X, et al. TNF-alpha contributes to up-regulation of Nav1.3 and Nav1.8 in DRG neurons following motor fiber injury. Pain 2010; 151: 266-79. https://doi.org/10.1016/j.pain.2010.06.005
  23. Jin X, Gereau RWt. Acute p38-mediated modulation of tetrodotoxin-resistant sodium channels in mouse sensory neurons by tumor necrosis factor-alpha. J Neurosci 2006; 26: 246-55. https://doi.org/10.1523/JNEUROSCI.3858-05.2006
  24. Donegan M, Kernisant M, Cua C, Jasmin L, Ohara PT. Satellite glial cell proliferation in the trigeminal ganglia after chronic constriction injury of the infraorbital nerve. Glia 2013; 61: 2000-8. https://doi.org/10.1002/glia.22571
  25. Komori T, Morikawa Y, Inada T, Hisaoka T, Senba E. Site-specific subtypes of macrophages recruited after peripheral nerve injury. Neuroreport 2011; 22: 911-7. https://doi.org/10.1097/WNR.0b013e32834cd76a
  26. Lu X, Richardson PM. Responses of macrophages in rat dorsal root ganglia following peripheral nerve injury. J Neurocytol 1993; 22: 334-41. https://doi.org/10.1007/BF01195557
  27. Harvey LD, Yin Y, Attarwala IY, Begum G, Deng J, Yan HQ, et al. Administration of DHA Reduces Endoplasmic Reticulum Stress-Associated Inflammation and Alters Microglial or Macrophage Activation in Traumatic Brain Injury. ASN Neuro 2015; 7.
  28. Abbadie C, Lindia JA, Cumiskey AM, Peterson LB, Mudgett JS, Bayne EK, et al. Impaired neuropathic pain responses in mice lacking the chemokine receptor CCR2. Proc Natl Acad Sci U S A 2003; 100: 7947-52. https://doi.org/10.1073/pnas.1331358100
  29. Kwon MJ, Shin HY, Cui Y, Kim H, Thi AH, Choi JY, et al. CCL2 Mediates Neuron-Macrophage Interactions to Drive Proregenerative Macrophage Activation Following Preconditioning Injury. J Neurosci 2015; 35: 15934-47. https://doi.org/10.1523/JNEUROSCI.1924-15.2015
  30. Kim D, You B, Lim H, Lee SJ. Toll-like receptor 2 contributes to chemokine gene expression and macrophage infiltration in the dorsal root ganglia after peripheral nerve injury. Mol Pain 2011; 7: 74.
  31. Raghavendra V, Tanga F, Rutkowski MD, DeLeo JA. Anti-hyperalgesic and morphine-sparing actions of propentofylline following peripheral nerve injury in rats: mechanistic implications of spinal glia and proinflammatory cytokines. Pain 2003; 104: 655-64. https://doi.org/10.1016/S0304-3959(03)00138-6
  32. Wagner R, Myers RR. Endoneurial injection of TNF-alpha produces neuropathic pain behaviors. Neuroreport 1996; 7: 2897-901. https://doi.org/10.1097/00001756-199611250-00018
  33. Wang CL, Lu CY, Pi CC, Zhuang YJ, Chu CL, Liu WH, et al. Extracellular polysaccharides produced by Ganoderma formosanum stimulate macrophage activation via multiple pattern-recognition receptors. BMC Complement Altern Med 2012; 12: 119. https://doi.org/10.1186/1472-6882-12-S1-P119
  34. Fu C, Yin Z, Yu D, Yang Z. Substance P and calcitonin gene-related peptide expression in dorsal root ganglia in sciatic nerve injury rats. Neural Regen Res 2013; 8: 3124-30.
  35. Sun J, Ramnath RD, Zhi L, Tamizhselvi R, Bhatia M. Substance P enhances NF-kappaB transactivation and chemokine response in murine macrophages via ERK1/2 and p38 MAPK signaling pathways. Am J Physiol Cell Physiol 2008; 294: C1586-96. https://doi.org/10.1152/ajpcell.00129.2008
  36. Matsumoto K, Nakajima T, Sakai H, Kato S, Sagara A, Arakawa K, et al. Increased expression of 5-HT3 and NK 1 receptors in 5-fluorouracil-induced mucositis in mouse jejunum. Dig Dis Sci 2013; 58: 3440-51. https://doi.org/10.1007/s10620-013-2709-7
  37. Bardelli C, Gunella G, Varsaldi F, Balbo P, Del Boca E, Bernardone IS, et al. Expression of functional NK1 receptors in human alveolar macrophages: superoxide anion production, cytokine release and involvement of NF-kappaB pathway. Br J Pharmacol 2005; 145: 385-96. https://doi.org/10.1038/sj.bjp.0706198
  38. Noma N, Tsuboi Y, Kondo M, Matsumoto M, Sessle BJ, Kitagawa J, et al. Organization of pERK-immunoreactive cells in trigeminal spinal nucleus caudalis and upper cervical cord following capsaicin injection into oral and craniofacial regions in rats. J Comp Neurol 2008; 507: 1428-40. https://doi.org/10.1002/cne.21620
  39. Iwata K, Imai T, Tsuboi Y, Tashiro A, Ogawa A, Morimoto T, et al. Alteration of medullary dorsal horn neuronal activity following inferior alveolar nerve transection in rats. J Neurophysiol 2001; 86: 2868-77. https://doi.org/10.1152/jn.2001.86.6.2868
  40. 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. https://doi.org/10.1038/16040
  41. Suzuki I, Tsuboi Y, Shinoda M, Shibuta K, Honda K, Katagiri A, et al. Involvement of ERK phosphorylation of trigeminal spinal subnucleus caudalis neurons in thermal hypersensitivity in rats with infraorbital nerve injury. PLoS One 2013; 8: e57278. https://doi.org/10.1371/journal.pone.0057278
  42. Okada-Ogawa A, Suzuki I, Sessle BJ, Chiang CY, Salter MW, Dostrovsky JO, et al. Astroglia in medullary dorsal horn (trigeminal spinal subnucleus caudalis) are involved in trigeminal neuropathic pain mechanisms. J Neurosci 2009; 29: 11161-71. https://doi.org/10.1523/JNEUROSCI.3365-09.2009
  43. Shibuta K, Suzuki I, Shinoda M, Tsuboi Y, Honda K, Shimizu N, et al. Organization of hyperactive microglial cells in trigeminal spinal subnucleus caudalis and upper cervical spinal cord associated with orofacial neuropathic pain. Brain Res 2012; 1451: 74-86. https://doi.org/10.1016/j.brainres.2012.02.023
  44. Chiang CY, Dostrovsky JO, Iwata K, Sessle BJ. Role of glia in orofacial pain. Neuroscientist 2011; 17: 303-20. https://doi.org/10.1177/1073858410386801
  45. Inoue K. A state-of-the-art perspective on microgliopathic pain. Open Biol 2018; 8.
  46. Rothhammer V, Borucki DM, Tjon EC, Takenaka MC, Chao CC, Ardura-Fabregat A, et al. Microglial control of astrocytes in response to microbial metabolites. Nature 2018; 557: 724-8. https://doi.org/10.1038/s41586-018-0119-x

Cited by

  1. Pathophysiological mechanisms of persistent orofacial pain vol.62, pp.2, 2019, https://doi.org/10.2334/josnusd.19-0373
  2. Morphological and Functional Changes of Corneal Nerves and Their Contribution to Peripheral and Central Sensory Abnormalities vol.14, 2019, https://doi.org/10.3389/fncel.2020.610342
  3. Role of macrophage-mediated Toll-like receptor 4–interleukin-1R signaling in ectopic tongue pain associated with tooth pulp inflammation vol.17, pp.1, 2019, https://doi.org/10.1186/s12974-020-01995-y
  4. Sensory Neuron TLR4 mediates the development of nerve-injury induced mechanical hypersensitivity in female mice vol.97, 2019, https://doi.org/10.1016/j.bbi.2021.06.011