The role of nitric oxide in orofacial pain

Nitric Oxide - Biology and Chemistry

Volumn 26, Issue 1, 2012, Pages 32-37

  Fan, Wenguo ^a   Huang, Fang ^a   Wu, Zhi ^a   Zhu, Xiao ^b   Li, Dongpei ^b   He, Hongwen ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b GUANGDONG MEDICAL UNIVERSITY   (China)

Author keywords

Nitric oxide; Orofacial pain; Review

Indexed keywords

CYCLIC GMP; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUTAMIC ACID; INDUCIBLE NITRIC OXIDE SYNTHASE; N METHYL DEXTRO ASPARTIC ACID; NITRIC OXIDE; NITRIC OXIDE SYNTHASE;

CHRONIC OROFACIAL PAIN; ELECTROACUPUNCTURE; FACE PAIN; GENE EXPRESSION; HUMAN; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MUSCULOSKELETAL PAIN; NERVE CONDUCTION; NEUROMODULATION; NOCICEPTION; OROFACIAL PAIN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SOMATOSENSORY CORTEX; TRIGEMINAL NERVE;

ANIMALS; FACIAL PAIN; HUMANS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NOCICEPTION; TRIGEMINAL NERVE;

EID: 83655172305     PISSN: 10898603     EISSN: 10898611     Source Type: Journal    
DOI: 10.1016/j.niox.2011.11.003     Document Type: Review

References (92)

1. R.M. Palmer, A.G. Ferrige, and S. Moncada Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor Nature 327 1987 524 526 (Pubitemid 17085822)
2. D.E. Baranano, C.D. Ferris, and S.H. Snyder Atypical neural messengers Trends Neurosci. 24 2001 99 106 (Pubitemid 32115440)
3. D. Boehning, and S.H. Snyder Novel neural modulators Annu. Rev. Neurosci. 26 2003 105 131 (Pubitemid 37064930)
4. A. Dhir, and S.K. Kulkarni Nitric oxide and major depression Nitric Oxide 24 2011 125 131
5. Z.D. Luo, and D. Cizkova The role of nitric oxide in nociception Curr. Rev. Pain 4 2000 459 466
6. Y. Cury, G. Picolo, V.P. Gutierrez, and S.H. Ferreira Pain and analgesia: the dual effect of nitric oxide in the nociceptive system Nitric Oxide 25 2011 243 254
7. American Board of Orofacial Pain. < abop.net/index.asp >.
8. J.P. OKESON, Orofacial Pain-Guidelines for Assessment, Diagnosis, and Management, Quintessence Books, Chicago, 1996, pp. 1-3.
9. N.E. Lazarov The mesencephalic trigeminal nucleus in the cat Adv. Anat. Embryol. Cell Biol. 153 2000 iii xiv 1-103
10. E. Marani, and K.G. Usunoff The trigeminal motonucleus in man Arch. Physiol. Biochem. 106 1998 346 354 (Pubitemid 29451062)
11. N.E. Lazarov Comparative analysis of the chemical neuroanatomy of the mammalian trigeminal ganglion and mesencephalic trigeminal nucleus Prog. Neurobiol. 66 2002 19 59 (Pubitemid 34230413)
12. D.A. Bereiter, K.M. Hargreaves, and J.W. Hu Trigeminal mechanisms of nociception: peripheral and brainstem organization A. Basbaum, M.C. Bushnell, Science of Pain vol. 5 2009 Elsevier New York City 435 460
13. B.J. Sessle Acute and chronic craniofacial pain: brainstem mechanisms of nociceptive transmission and neuroplasticity, and their clinical correlates Crit. Rev. Oral Biol. Med. 11 2000 57 91 (Pubitemid 30080932)
14. J. Olszewski On the anatomical and functional organization of the spinal trigeminal nucleus J. Comp. Neurol. 92 1950 401 413
15. J.W. Hu, and B.J. Sessle Comparison of responses of cutaneous nociceptive and nonnociceptive brain stem neurons in trigeminal subnucleus caudalis (medullary dorsal horn) and subnucleus oralis to natural and electrical stimulation of tooth pulp J. Neurophysiol. 52 1984 39 53 (Pubitemid 14095899)
16. J.G. Broton, J.W. Hu, and B.J. Sessle Effects of temporomandibular joint stimulation on nociceptive and nonnociceptive neurons of the cat's trigeminal subnucleus caudalis (medullary dorsal horn) J. Neurophysiol. 59 1988 1575 1589
17. S. Gobel Golgi studies in the substantia gelatinosa neurons in the spinal trigeminal nucleus J. Comp. Neurol. 162 1975 397 415
18. K.D. Phelan, and W.M. Falls An analysis of the cyto- and myeloarchitectonic organization of trigeminal nucleus interpolaris in the rat Somatosens. Mot. Res. 6 1989 333 366 (Pubitemid 19165925)
19. W.M. Falls, B.J. Moore, and M.T. Schneider Fine structural characteristics and synaptic connections of trigeminocerebellar projection neurons in rat trigeminal nucleus oralis Somatosens. Mot. Res. 7 1990 1 18 (Pubitemid 20187052)
20. H. Wang, F. Wei, R. Dubner, and K. Ren Selective distribution and function of primary afferent nociceptive inputs from deep muscle tissue to the brainstem trigeminal transition zone J. Comp. Neurol. 498 2006 390 402 (Pubitemid 44205082)
21. C. Nathan, and Q.W. Xie Nitric oxide synthases: roles, tolls, and controls Cell 78 1994 915 918 (Pubitemid 24292319)
22. D.S. Bredt, and S.H. Snyder Nitric oxide a novel neuronal messenger Neuron 8 1992 3 11
23. Z. Lohinai, A.D. Szekely, P. Benedek, and A. Csillag Nitric oxide synthase containing nerves in the cat and dog dental pulp and gingiva Neurosci. Lett. 227 1997 91 94 (Pubitemid 27245042)
24. D. Kolesar, M. Kolesarova, A. Schreiberova, M. Lackova, and J. Marsala Distribution of NADPH diaphorase-exhibiting primary afferent neurons in the trigeminal ganglion and mesencephalic trigeminal nucleus of the rabbit Cell Mol. Neurobiol. 26 2006 1265 1279 (Pubitemid 44924046)
25. W. Fan, W. Dong, S. Leng, D. Li, S. Cheng, C. Li, H. Qu, and H. He Expression and colocalization of NADPH-diaphorase and heme oxygenase-2 in trigeminal ganglion and mesencephalic trigeminal nucleus of the rat J. Mol. Histol. 39 2008 427 433
26. P. Alm, B. Uvelius, J. Ekstrom, B. Holmqvist, B. Larsson, and K.E. Andersson Nitric oxide synthase-containing neurons in rat parasympathetic, sympathetic and sensory ganglia: a comparative study Histochem. J. 27 1995 819 831
27. I.I. Stoyanova, and N.E. Lazarov Localization of nitric oxide synthase in rat trigeminal primary afferent neurons using NADPH-diaphorase histochemistry J. Mol. Histol. 36 2005 187 193 (Pubitemid 40768428)
28. R. Ramachandran, K.B. Ploug, A. Hay-Schmidt, J. Olesen, I. Jansen-Olesen, and S. Gupta Nitric oxide synthase (NOS) in the trigeminal vascular system and other brain structures related to pain in rats Neurosci. Lett. 484 2010 192 196
29. N. Lazarov, and A. Dandov Distribution of NADPH-diaphorase and nitric oxide synthase in the trigeminal ganglion and mesencephalic trigeminal nucleus of the cat. A histochemical and immunohistochemical study Acta Anat. (Basel) 163 1998 191 200 (Pubitemid 29100770)
30. M. Hou, M. Kanje, J. Longmore, J. Tajti, R. Uddman, and L. Edvinsson 5-HT(1B) and 5-HT(1D) receptors in the human trigeminal ganglion: co-localization with calcitonin gene-related peptide substance P and nitric oxide synthase Brain Res. 909 2001 112 120 (Pubitemid 32710124)
31. M. Hou, R. Uddman, J. Tajti, and L. Edvinsson Nociceptin immunoreactivity and receptor mRNA in the human trigeminal ganglion Brain Res. 964 2003 179 186 (Pubitemid 36165142)
32. E. Borsani, S. Giovannozzi, R. Boninsegna, R. Rezzani, M. Labanca, M. Tschabitscher, and L.F. Rodella Nitroxidergic system in human trigeminal ganglia neurons: a quantitative evaluation Acta Histochem. 112 2010 444 451
33. A.A. Harper, and S.N. Lawson Conduction velocity is related to morphological cell type in rat dorsal root ganglion neurones J. Physiol. 359 1985 31 46 (Pubitemid 15152926)
34. C.S. Dohrn, and A.J. Beitz NMDA receptor mRNA expression in NOS-containing neurons in the spinal trigeminal nucleus of the rat Neurosci. Lett. 175 1994 28 32 (Pubitemid 24215477)
35. W. Fan, F. Huang, W. Dong, Z. Gao, C. Li, X. Zhu, D. Li, and H. He Distribution of heme oxygenase-2 and NADPH-diaphorase in the spinal trigeminal nucleus of the rat J. Mol. Histol. 40 2009 209 215
36. J.F. Yeo, F.R. Tang, and S.K. Leong Ultrastructural study of NADPH-d positive neurons in laminae I and II of the rat caudal spinal trigeminal nucleus Int. J. Neurosci. 91 1997 29 43
37. J.F. Yeo Does nitric oxide play a role in orofacial pain transmission? Ann. N. Y. Acad. Sci. 962 2002 151 160
38. C.S. Dohrn, M.A. Mullett, R.H. Price, and A.J. Beitz Distribution of nitric oxide synthase-immunoreactive interneurons in the spinal trigeminal nucleus J. Comp. Neurol. 346 1994 449 460 (Pubitemid 24258512)
39. J. Wood, and J. Garthwaite Models of the diffusional spread of nitric oxide: implications for neural nitric oxide signalling and its pharmacological properties Neuropharmacology 33 1994 1235 1244 (Pubitemid 24353714)
40. B.M. Gratt, and M. Anbar A pilot study of nitric oxide blood levels in patients with chronic orofacial pain Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 100 2005 441 448 (Pubitemid 41331034)
41. M. Anbar, and B.M. Gratt Role of nitric oxide in the physiopathology of pain J. Pain Symptom Manage. 14 1997 225 254 (Pubitemid 27415740)
42. M. Anbar, and B.M. Gratt The possible role of nitric oxide in the physiopathology of pain associated with temporomandibular joint disorders J. Oral Maxillofac. Surg. 56 1998 872 882 Discussion 883-874
43. S. Suenaga, K. Abeyama, A. Hamasaki, T. Mimura, and T. Noikura Temporomandibular disorders: relationship between joint pain and effusion and nitric oxide concentration in the joint fluid Dentomaxillofac. Radiol. 30 2001 214 218 (Pubitemid 33695633)
44. M.S. Evcil, A. Keles, I. Uzun, B. Demircan, and M. Koseoglu Nitric oxide levels in serum of patients with symptomatic irreversible pulpitis J. Pain Palliat. Care Pharmacother. 20 2006 15 19 (Pubitemid 43855678)
45. M. Takemura, A. Tsujio, K. Iwase, T. Shimada, and Y. Shigenaga Central terminals of orofacial primary afferents and NADPH-diaphorase activity in the trigemino-solitary complex of rats Brain Res. 781 1998 77 89
46. W. Fan, F. Huang, C. Li, H. Qu, Z. Gao, S. Leng, D. Li, and H. He Involvement of NOS/NO in the development of chronic dental inflammatory pain in rats Brain Res. Rev. 59 2009 324 332
47. E. Borsani, R. Albertini, M. Labanca, C. Lonati, R. Rezzani, and L.F. Rodella Peripheral purinergic receptor modulation influences the trigeminal ganglia nitroxidergic system in an experimental murine model of inflammatory orofacial pain J. Neurosci. Res. 88 2010 2715 2726
48. H.S. Jung, H.B. Jeon, I.S. Jeon, B.J. Lee, H.W. Yoo, D.K. Ahn, and D.H. Youn Preventing extracellular diffusion of trigeminal nitric oxide enhances formalin-induced orofacial pain Korean J. Physiol. Pharmacol. 13 2009 379 383
49. J.S. Lee, Y. Zhang, and J.Y. Ro Involvement of neuronal inducible and endothelial nitric oxide synthases in capsaicin-induced muscle hypersensitivity Eur. J. Pain 13 2009 924 928
50. S.A. Tesser-Viscaino, A. Denadai-Souza, S.A. Teixeira, E. Ervolino, R.J. Cruz-Rizzolo, S.K. Costa, M.N. Muscara, and C.A. Casatti Putative antinociceptive action of nitric oxide in the caudal part of the spinal trigeminal nucleus during chronic carrageenan-induced arthritis in the rat temporomandibular joint Brain Res. 1302 2009 85 96
51. L. Rodella, R. Rezzani, G. Corsetti, and R. Bianchi Nitric oxide involvement in the trigeminal hyperalgesia in diabetic rats Brain Res. 865 2000 112 115 (Pubitemid 30256214)
52. N. Yonehara, C. Kudo, and Y. Kamisaki Involvement of NMDA-nitric oxide pathways in the development of tactile hypersensitivity evoked by the loose-ligation of inferior alveolar nerves in rats Brain Res. 963 2003 232 243 (Pubitemid 36126304)
53. A.S. Law, K.R. Baumgardner, S.T. Meller, and G.F. Gebhart Localization and changes in NADPH-diaphorase reactivity and nitric oxide synthase immunoreactivity in rat pulp following tooth preparation J. Dent. Res. 78 1999 1585 1595 (Pubitemid 32501246)
54. N. Kawashima, H. Nakano-Kawanishi, N. Suzuki, M. Takagi, and H. Suda Effect of NOS inhibitor on cytokine and COX2 expression in rat pulpitis J. Dent. Res. 84 2005 762 767
55. T. Yamaza, K.F. Masuda, Y. Tsukiyama, K. Nishijima, R. Murakami, M.A. Kido, K. Koyano, and T. Tanaka NF-kappaB activation and iNOS expression in the synovial membrane of rat temporomandibular joints after induced synovitis J. Dent. Res. 82 2003 183 188 (Pubitemid 41766040)
56. D.R. Pena-dos-Santos, F.P. Severino, S.A. Pereira, D.B. Rodrigues, F.Q. Cunha, S.M. Vieira, M.H. Napimoga, and J.T. Clemente-Napimoga Activation of peripheral kappa/delta opioid receptors mediates 15-deoxy-(Delta12,14)- prostaglandin J2 induced-antinociception in rat temporomandibular joint Neuroscience 163 2009 1211 1219
57. D.K. Ahn, Y.S. Kim, and J.S. Park Central NO is involved in the antinociceptive action of intracisternal antidepressants in freely moving rats Neurosci. Lett. 243 1998 105 108 (Pubitemid 28109422)
58. S.M. le Grand, S. Patumraj, P. Phansuwan-Pujito, and A. Srikiatkhachorn Melatonin inhibits cortical spreading depression-evoked trigeminal nociception Neuroreport 17 2006 1709 1713 (Pubitemid 44621569)
59. J. Olesen, and I. Jansen-Olesen Nitric oxide mechanisms in migraine Pathol. Biol. (Paris) 48 2000 648 657
60. L.L. Thomsen, and J. Olesen Nitric oxide in primary headaches Curr. Opin. Neurol. 14 2001 315 321 (Pubitemid 32510595)
61. L.L. Thomsen Investigations into the role of nitric oxide and the large intracranial arteries in migraine headache Cephalalgia 17 1997 873 895 (Pubitemid 28034353)
62. L.L. Thomsen, J. Brennum, H.K. Iversen, and J. Olesen Effects of nitrogen oxide donor glyceryl trinitrate on pressure pain threshold in humans Ugeskr. Laeger 159 1997 4645 4648
63. P.M. Schlechtweg, J. Roder, M.J. Fischer, W. Neuhuber, and K. Messlinger Increase in NADPH-diaphorase-positive and neuronal NO synthase immunoreactive neurons in the rat spinal trigeminal nucleus following infusion of a NO donor-evidence for a feed-forward process in NO production involved in trigeminal nociception Cephalalgia 29 2009 566 579
64. M. Larsson, and J. Broman Synaptic plasticity and pain: role of ionotropic glutamate receptors Neuroscientist 17 2011 256 273
65. C. Goudet, V. Magnaghi, M. Landry, F. Nagy, R.W.t. Gereau, and J.P. Pin Metabotropic receptors for glutamate and GABA in pain Brain. Res. Rev. 60 2009 43 56
66. H.J. Lee, E.M. Pogatzki-Zahn, and T.J. Brennan The effect of the AMPA/kainate receptor antagonist LY293558 in a rat model of postoperative pain J. Pain 7 2006 768 777 (Pubitemid 44466694)
67. C.H. Kim, J. Lee, J.Y. Lee, and K.W. Roche Metabotropic glutamate receptors: phosphorylation and receptor signaling J. Neurosci. Res. 86 2008 1 10
68. D. Bleakman, A. Alt, and E.S. Nisenbaum Glutamate receptors and pain Semin. Cell Dev. Biol. 17 2006 592 604 (Pubitemid 46389351)
69. S. Leong, H. Liu, and J. Yeo Nitric oxide synthase and glutamate receptor immunoreactivity in the rat spinal trigeminal neurons expressing Fos protein after formalin injection Brain Res. 855 2000 107 115 (Pubitemid 30067700)
70. T. Fujita, Y. Kamisaki, and N. Yonehara Nitric oxide-induced increase of excitatory amino acid levels in the trigeminal nucleus caudalis of the rat with tactile hypersensitivity evoked by the loose-ligation of the inferior alveolar nerves J. Neurochem. 91 2004 558 567 (Pubitemid 39431151)
71. N. Yonehara, K. Amano, and Y. Kamisaki Involvement of the NMDA-nitric oxide pathway in the development of hypersensitivity to tactile stimulation in dental injured rats Jpn. J. Pharmacol. 90 2002 145 155 (Pubitemid 35291301)
72. S.R. Jaffrey, H. Erdjument-Bromage, C.D. Ferris, P. Tempst, and S.H. Snyder Protein S-nitrosylation: a physiological signal for neuronal nitric oxide Nat. Cell Biol. 3 2001 193 197 (Pubitemid 32118373)
73. W. Kummer, S. Behrends, T. Schwarzlmuller, A. Fischer, and D. Koesling Subunits of soluble guanylyl cyclase in rat and guinea-pig sensory ganglia Brain Res. 721 1996 191 195 (Pubitemid 26179853)
74. J.Y. Ro, J. Lee, N.F. Capra, and Y. Zhang Role of soluble guanylate cyclase in the trigeminal subnucleus caudalis in capsaicin-induced muscle hypersensitivity Brain Res. 1184 2007 141 148 (Pubitemid 350160592)
75. J.T. Clemente-Napimoga, A. Pellegrini-da-Silva, V.H. Ferreira, M.H. Napimoga, C.A. Parada, and C.H. Tambeli Gonadal hormones decrease temporomandibular joint kappa-mediated antinociception through a down-regulation in the expression of kappa opioid receptors in the trigeminal ganglia Eur. J. Pharmacol. 617 2009 41 47
76. R.T. Almeida, and I.D. Duarte Nitric oxide/cGMP pathway mediates orofacial antinociception induced by electroacupuncture at the St36 acupoint Brain Res. 1188 2008 54 60 (Pubitemid 50007737)
77. N.C. Favaro-Moreira, K.E. Torres-Chavez, L. Fischer, and C.H. Tambeli Peripheral estradiol induces temporomandibular joint antinociception in rats by activating the nitric oxide/cyclic guanosine monophosphate signaling pathway Neuroscience 164 2009 724 732
78. M. Tal A novel antioxidant alleviates heat hyperalgesia in rats with an experimental painful peripheral neuropathy Neuroreport 7 1996 1382 1384 (Pubitemid 26280996)
79. J.F. Yeo, S.F. Ling, N. Tang, and W.Y. Ong Antinociceptive effect of CNS peroxynitrite scavenger in a mouse model of orofacial pain Exp. Brain Res. 184 2008 435 438 (Pubitemid 50004509)
80. L.R. Watkins, and S.F. Maier Immune regulation of central nervous system functions: from sickness responses to pathological pain J. Intern. Med. 257 2005 139 155 (Pubitemid 40193964)
81. Y.F. Xie, S. Zhang, C.Y. Chiang, J.W. Hu, J.O. Dostrovsky, and B.J. Sessle Involvement of glia in central sensitization in trigeminal subnucleus caudalis (medullary dorsal horn) Brain Behav. Immun. 21 2007 634 641 (Pubitemid 46829766)
82. F. Marchand, M. Perretti, and S.B. McMahon Role of the immune system in chronic pain Nat. Rev. Neurosci. 6 2005 521 532 (Pubitemid 40942819)
83. W. Guo, H. Wang, M. Watanabe, K. Shimizu, S. Zou, S.C. LaGraize, F. Wei, R. Dubner, and K. Ren Glial-cytokine-neuronal interactions underlying the mechanisms of persistent pain J. Neurosci. 27 2007 6006 6018 (Pubitemid 46849761)
84. S.E. Freeman, V.V. Patil, and P.L. Durham Nitric oxide-proton stimulation of trigeminal ganglion neurons increases mitogen-activated protein kinase and phosphatase expression in neurons and satellite glial cells Neuroscience 157 2008 542 555
85. C.V. Vause, and P.L. Durham CGRP stimulation of iNOS and NO release from trigeminal ganglion glial cells involves mitogen-activated protein kinase pathways J. Neurochem. 110 2009 811 821
86. A. Panconesi, M.L. Bartolozzi, and L. Guidi Migraine pain: reflections against vasodilatation J. Headache Pain 10 2009 317 325
87. S. Benemei, P. Nicoletti, J.G. Capone, F. De Cesaris, and P. Geppetti Migraine Handb. Exp. Pharmacol. 2009 75 89
88. J. Li, C.V. Vause, and P.L. Durham Calcitonin gene-related peptide stimulation of nitric oxide synthesis and release from trigeminal ganglion glial cells Brain Res. 1196 2008 22 32
89. S. Koulchitsky, M.J. Fischer, and K. Messlinger Calcitonin gene-related peptide receptor inhibition reduces neuronal activity induced by prolonged increase in nitric oxide in the rat spinal trigeminal nucleus Cephalalgia 29 2009 408 417
90. J. Bellamy, E.J. Bowen, A.F. Russo, and P.L. Durham Nitric oxide regulation of calcitonin gene-related peptide gene expression in rat trigeminal ganglia neurons Eur. J. Neurosci. 23 2006 2057 2066
91. M. Eberhardt, L. Neeb, E.M. Vogel, G. Tiegs, U. Reuter, K. Messlinger, and M.J. Fischer Glyceroltrinitrate facilitates stimulated CGRP release but not gene expression of CGRP or its receptor components in rat trigeminal ganglia Neuropeptides 43 2009 483 489
92. R. Greco, C. Tassorelli, G. Sandrini, P. Di Bella, S. Buscone, and G. Nappi Role of calcitonin gene-related peptide and substance P in different models of pain Cephalalgia 28 2008 114 126