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 Research

Volumn 1302, Issue , 2009, Pages 85-96

  Tesser Viscaíno, Silvia A ^a,b   Denadai Souza, Alexandre ^c,d   Teixeira, Simone A ^d   Ervolino, Edílson ^c,d   Cruz Rizzolo, Roelf J ^c   Costa, Soraia K ^d   Muscará, Marcelo N ^d   Casatti, Cláudio A ^a,c  

^a UNIVERSITY OF CAMPINAS   (Brazil)

^b PAULISTA UNIVERSITY   (Brazil)

^c SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^d UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Arthritis; Nitric oxide synthase; Spinal trigeminal nucleus; Temporomandibular joint

Indexed keywords

7 NITROINDAZOLE; CARRAGEENAN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; INDUCIBLE NITRIC OXIDE SYNTHASE; MESSENGER RNA; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PROTEIN FOS;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINOCICEPTION; ARTHRITIS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; MALE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TEMPOROMANDIBULAR JOINT; TRIGEMINAL NUCLEUS;

ANIMALS; ARTHRALGIA; ARTHRITIS, EXPERIMENTAL; CARRAGEENAN; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; INDAZOLES; INFLAMMATION MEDIATORS; MALE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; NITRIC OXIDE SYNTHASE TYPE III; NOCICEPTORS; PAIN MEASUREMENT; PAIN THRESHOLD; POSTERIOR HORN CELLS; RATS; RATS, WISTAR; RNA, MESSENGER; TEMPOROMANDIBULAR JOINT DISORDERS; TRIGEMINAL CAUDAL NUCLEUS;

ANIMALIA; RATTUS;

EID: 71849096093     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2009.09.056     Document Type: Article

References (81)

1. Ayers N.A., Kapas L., and Krueger J.M. Circadian variation of nitric oxide synthase activity and cytosolic protein levels in rat brain. Brain Res. 707 (1996) 127-130
2. Bereiter D.A., and Bereiter D.F. Morphine and NMDA receptor antagonism reduce c-fos expression in spinal trigeminal nucleus produced by acute injury to the TMJ region. Pain 85 (2000) 65-77
3. Bereiter D.A., Hirata H., and Hu J.W. Trigeminal subnucleus caudalis: beyond homologies with the spinal dorsal horn. Pain 1 (2000) 221-224
4. Bredt D.S., and Snyder S.H. Nitric oxide: a physiologic messenger molecule. Annu. Rev. Biochem. 63 (1994) 175-195
5. Bredt D.S., Ferris C.D., and Snyder S.H. Nitric oxide synthase regulatory sites. Phosphorylation by cyclic AMP-dependent protein kinase, protein kinase C, and calcium/calmodulin protein kinase; identification of flavin and calmodulin binding sites. J. Biol. Chem. 267 (1992) 10976-10981
6. Broton J.G., Hu J.W., and Sessle B.J. 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
7. Callsen-Cencic P., Hoheisel U., Kaske A., Mense S., and Tenschert S. The controversy about spinal neuronal nitric oxide synthase: under which conditions is it up- or downregulated?. Cell Tissue Res. 295 (1999) 183-194
8. Chiang C.Y., Wang J., Xie Y.F., Zhang S., Hu J.W., Dostrovsky J.O., and Sessle B.J. Astroglial glutamate-glutamine shuttle is involved in central sensitization of nociceptive neurons in rat medullary dorsal horn. J. Neurosci. 27 (2007) 9068-9076
9. Cunha T.M., Verri Jr. W.A., Vivancos G.G., Moreira I.F., Reis S., Parada C.A., Cunha F.Q., and Ferreira S.H. An electronic pressure-meter nociception paw test for mice. Braz. J. Med. Biol. Res. 37 (2004) 401-407
10. Chu Y.C., Guan Y., Skinner J., Raja S.N., Johns R.A., and Tao Y.X. Effect of genetic knockout or pharmacologic inhibition of neuronal nitric oxide synthase on complete Freund's adjuvant-induced persistent pain. Pain 119 (2005) 113-123
11. Denadai-Souza A., Camargo L.D., Ribela M.T., Keeble J.E., Costa S.K., and Muscará M.N. Participation of peripheral tachykinin NK(1) receptors in the carrageenan-induced inflammation of the rat temporomandibular joint. Eur. J. Pain 13 (2009) 812-819
12. Dinerman J.L., Steiner J.P., Dawson T.M., Dawson V., and Snyder S.H. Cyclic nucleotide dependent phosphorylation of neuronal nitric oxide synthase inhibits catalytic activity. Neuropharmacology 11 (1994) 1245-1251
13. Dohrn C.S., Mullett M.A., Price R.H., and Beitz A.J. Distribution of nitric oxide synthase-immunoreactive interneurons in the spinal trigeminal nucleus. J. Comp. Neurol. 346 (1994) 449-460
14. Donaldson K.W. Rheumatoid diseases and the temporomandibular joint: a review. Cranio 13 (1995) 264-269
15. Duarte I.D., and Ferreira S.H. L-NAME causes antinociception by stimulation of the arginine-NO-cGMP pathway. Mediators Inflamm. 9 (2000) 25-30
16. Dubner R., and Ren K. Brainstem mechanisms of persistent pain following injury. J. Orofac. Pain 18 (2004) 299-305
17. Dun N.J., Dun S.L., Wu S.Y., Förstermann U., Schimidt H.H.H.W., and Tseng L.F. Nitric oxide synthase immunoreactivity in the rat, mouse, cat and squirrel monkey spinal cord. Neuroscience 54 (1993) 845-857
18. El-Mlili N., Rodrigo R., Naghizadeh B., Cauli O., and Felipo V. Chronic hyperammonemia reduces the activity of neuronal nitric oxide synthase in cerebellum by altering its localization and increasing its phosphorylation by calcium-calmodulin kinase II. J. Neurochem. 106 (2008) 1440-1449
19. Faria M.S., Muscará M.N., Moreno Junior H., Teixeira S.A., Dias H.B., de Oliveira B., Graeff F.G., and de Nucci G. Acute inhibition of nitric oxide synthesis induces anxiolysis in the plus maze test. Eur. J. Pharmacol. 323 (1997) 37-43
20. Goff J.R., Burkey A.R., Goff D.J., and Jasmin L. Reorganization of the spinal dorsal horn in models of chronic pain: correlation with behaviour. Neuroscience 82 (1998) 559-574
21. Guo W., Wang H., Watanabe M., Shimizu K., Zou S., LaGraize S.C., Wei F., Dubner R., and Ren K. Glial-cytokine-neuronal interactions underlying the mechanisms of persistent pain. J. Neurosci. 27 (2007) 6006-6018
22. Hathaway C.B., Hu J.W., and Bereiter D.A. Distribution of Fos-like immunoreactivity in the caudal brainstem of the rat following noxious chemical stimulation of the temporomandibular joint. J. Comp. Neurol. 356 (1995) 444-456
23. Hayashi Y., Nishio M., Naito Y., Yokokura H., Nimura Y., Hidaka H., and Watanabe Y. Regulation of neuronal nitric-oxide synthase by calmodulin kinases. J. Biol. Chem. 274 (1999) 20597-20602
24. Heneka M.T., and Feinstein D.L. Expression and function of inducible nitric oxide synthase in neurons. J. Neuroimmunol. 114 (2001) 8-18
25. Herb K., Cho S., and Stiles M.A. Temporomandibular joint pain and dysfunction. Curr. Pain Headache Rep. 10 (2006) 408-414
26. Hiki K., Hattori R., Kawai C., and Yui Y. Purification of insoluble nitric oxide synthase from rat cerebellum. J. Biochem. 111 (1992) 556-558
27. Hoheisel U., Unger T., and Mense S. A block of spinal nitric oxide synthesis leads to increased background activity predominantly in nociceptive dorsal horn neurones in the rat. Pain 88 (2000) 249-257
28. Hoheisel U., Unger T., and Mense S. The possible role of the NO-cGMP pathway in nociception: different spinal and supraspinal action of enzyme blockers on rat dorsal horn neurones. Pain 117 (2005) 358-367
29. Ikeda H., Stark J., Fischer H., Wagner M., Drdla R., Jäger T., and Sandkühler J. Synaptic amplifier of inflammatory pain in the spinal dorsal horn. Science 312 (2006) 1659-1662
30. Infante C., Díaz M., Hernández A., Constandil L., and Pelissier T. Expression of nitric oxide synthase isoforms in the dorsal horn of monoarthritic rats: effects of competitive and uncompetitive N-methyl-d-aspartate antagonists. Arthritis Res. Ther. 9 (2007) R53
31. Komeima K., Hayashi Y., Naito Y., and Watanabe Y. Inhibition of neuronal nitric-oxide synthase by calcium/ calmodulin-dependent protein kinase IIalpha through Ser847 phosphorylation in NG108-15 neuronal cells. J. Biol. Chem. 275 (2000) 28139-28143
32. Lam H.H.D., Hanley D.F., Trapp B.D., Saito S., Raja S., Dawon T.M., and Yamaguchi H. Induction of cord neuronal nitric oxide synthase (NOS) after formalin in the rat hind paw. Neurosci. Lett. 210 (1996) 201-204
33. Lam D.K., Sessle B.J., and Hu J.W. Glutamate and capsaicin effects on trigeminal nociception I: Activation and peripheral sensitization of deep craniofacial nociceptive afferents. Brain Res. 1251 (2009) 130-139
34. Lam D.K., Sessle B.J., and Hu J.W. Glutamate and capsaicin effects on trigeminal nociception II: activation and central sensitization in brainstem neurons with deep craniofacial afferent input. Brain Res. 1253 (2009) 48-59
35. Laurindo C., Hernandez A., Constandil L., and Pelissier T. Nitric oxide synthase and soluble guanylate cyclase are involved in spinal cord wind-up activity of monoarthritic, but not of normal rats. Neurosci. Lett. 352 (2003) 64-66
36. Lee J.S., Zhand Y., and Ro J.Y. Involvement of neuronal, inducible and endothelial nitric oxide synthases in capsaicin-induced muscle hypersensitivity. Eur. J. Pain 13 (2009) 924-928
37. Leman S., Viltart O., and Sequeira H. Double immunocytochemistry for the detection of Fos protein in retrogradely identified neurons using cholera toxin B subunit. Brain Res. Brain Res. Protoc. 5 (2000) 298-304
38. Leong S., Liu H., and Yeo J. 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
39. Licinio J., Prolo P., McCann S.M., and Wong M.L. Brain iNOS: current understanding and clinical implications. Mol. Med. Today 5 (1999) 225-232
40. Lorenzetti B.B., and Ferreira S.H. Activation of the arginine-nitric oxide pathway in primary sensory neurons contributes to dipyrone-induced spinal and peripheral analgesia. Inflamm. Res. 45 (1996) 308-311
41. Lundeberg T., Alstergren P., Appelgren A., Appelgren B., Carleson J., Kopp S., and Theodorsson E. A model for experimentally induced temporomandibular joint arthritis in rats: effects of carrageenan on neuropeptide-like immunoreactivity. Neuropeptides 30 (1996) 37-41
42. Maihofner C., Euchenhofer C., Tegeder I., Beck K.F., Pfeilschifter J., and Geisslinger G. Regulation and immunohistochemical localization of nitric oxide synthases and soluble guanylyl cyclase in mouse spinal cord following nociceptive stimulation. Neurosci. Lett. 290 (2000) 71-75
43. Nathan C., and Xie Q.W. Regulation of biosynthesis of nitric oxide. J. Biol. Chem. 269 (1994) 13725-13728
44. Nazli M., Hismiogullari E.S., Thippeswamy T., and Morris R. How central is nitric oxide (NO) to the activation of c-fos in spinal neurones following noxious peripheral stimulation in the rat?. Brain Res. 888 (2001) 172-175
45. Okeson J.P. Management of temporomandibular disorders and occlusion (2007), Mosby-Year Book, St. Louis
46. Pardutz A., Krizbai I., Multon S., Vecsei L., and Schoenen J. Systemic nitroglycerin increases nNOS levels in rat trigeminal nucleus caudalis. Neuroreport 11 (2000) 3071-3075
47. Pelegrini-da-Silva A., Oliveira M.C., Parada C.A., and Tambeli C.H. Nerve growth factor acts with the beta2-adrenoceptor to induce spontaneous nociceptive behavior during temporomandibular joint inflammatory hyperalgesia. Life Sci. 83 (2008) 780-785
48. Piao Z.G., Cho I.H., Park C.K., Hong J.P., Choi S.Y., Lee S.J., Lee S., Park K., Kim J.S., and Oh S.B. Activation of glia and microglial p38 MAPK in medullary dorsal horn contributes to tactile hypersensitivity following trigeminal sensory nerve injury. Pain 121 (2006) 219-231
49. Pozza M., Bettelli C., Magnani F., Mascia M.T., Manzini E., and Calza M. Is neuronal nitric oxide involved in adjuvant-induced joint inflammation?. Eur. J. Pharmacol. 359 (1998) 87-93
50. Prado W.A., Schiavon V.F., and Cunha F.Q. Dual effect of local application of nitric oxide donors in a model of incision pain in rats. Eur. J. Pharmacol. 441 (2002) 57-65
51. Radhakrishnan R., Moore S.A., and Sluka K.A. Unilateral carrageenan injection into muscle or joint induces chronic bilateral hyperalgesia in rats. Pain 104 (2003) 567-577
52. Rameau G.A., Chiu L.Y., and Ziff E.B. NMDA receptor regulation of nNOS phosphorylation and induction of neuron death. Neurobiol. Aging 24 (2003) 1123-1133
53. Rameau G.A., Chiu L.Y., and Ziff E.B. Bidirectional regulation of neuronal nitric-oxide synthase phosphorylation at serine 847 by the N-methyl-d-aspartate receptor. J. Biol. Chem. 279 (2004) 14307-14314
54. Ren K. An improved method for assessing mechanical allodynia in the rat. Physiol. Behav. 67 (1999) 711-716
55. Rodrigues L.L., Oliveira M.C., Pelegrini-da-Silva A., de Arruda Veiga M.C., Parada C.A., and Tambeli C.H. Peripheral sympathetic component of the temporomandibular joint inflammatory pain in rats. J. Pain 7 (2006) 929-936
56. Rogério F., Teixeira S.A., Júnior H.J., Maria C.C., Vieira A.S., de Rezende A.C., Pereira G.A., Muscará M.N., and Langone F. mRNA and protein expression and activities of nitric oxide synthases in the lumbar spinal cord of neonatal rats after sciatic nerve transection and melatonin administration. Neurosci. Lett. 407 (2006) 182-187
57. Sarlani E., and Greenspan J.D. Why look in the brain for answers to temporomandibular disorder pain?. Cells Tissues Organs 180 (2005) 69-75
58. Sessle B.J. 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
59. Song T., Hatano N., Kambe T., Miyamoto Y., Ihara H., Yamamoto H., Sugimoto K., Kume K., Yamaguchi F., Tokuda M., and Watanabe Y. Nitric oxide-mediated modulation of calcium/calmodulin-dependent protein kinase II. Biochem. J. 412 (2008) 223-231
60. Sung Y.J., and Ambron R.T. Pathways that elicit long-term changes in gene expression in nociceptive neurons following nerve injury: contributions to neuropathic pain. Neurol. Res. 26 (2004) 195-203
61. Takeda M., Tanimoto T., Nasu M., Ikeda M., Kadoi J., and 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 116 (2005) 375-385
62. Takeda M., Tanimoto T., Ikeda M., Nasu M., Kadoi J., Shima Y., Ohta H., and Matsumoto S. Temporomandibular joint inflammation potentiates the excitability of trigeminal root ganglion neurons innervating the facial skin in rats. J. Neurophysiol. 93 (2005) 2723-2738
63. Takemura M., Tsujio A., Iwase K., Shimada T., and Shigenaga Y. Central terminals of orofacial primary afferents and NADPH-diaphorase activity in the trigemino-solitary complex of rats. Brain Res. 781 (1998) 77-89
64. Takemura M., Sugiyo S., Moritani M., Kobayashi M., and Yonehara N. Mechanisms of orofacial pain control in the central nervous system. Arch. Histol. Cytol. 69 (2006) 79-100
65. Tao F., Tao Y.X., Mao P., Zhao C., Li D., Liaw W.J., Raja S.N., and Johns R.A. Intact carrageenan-induced thermal hyperalgesia in mice lacking inducible nitric oxide synthase. Neuroscience 120 (2003) 847-854
66. Tao F., Tao Y.X., Zhao C., Dore S., Liaw W.J., Raja S.N., and Johns R.A. Differential roles of neuronal and endothelial nitric oxide synthases during carrageenan-induced inflammatory hyperalgesia. Neuroscience 128 (2004) 421-430
67. Tegeder I., Schmidtko A., Niederberger E., Ruth P., and Geisslinger G. Dual effects of spinally delivered 8-bromo-cyclic guanosine monophosphate (8-bromo-cGMP) in formalin-induced nociception in rats. Neurosc. Lett. 332 (2002) 146-150
68. Teixeira S.A., Castro G.M., Papes F., Martins M.L., Rogério F., Langone F., Santos L.M., Arruda P., de Nucci G., and Muscará M.N. Expression and activity of nitric oxide synthase isoforms in rat brain during the development of experimental allergic encephalomyelitis. Brain Res. Mol. Brain Res. 99 (2002) 17-25
69. Ting E., Roveroni R.C., Ferrari L.F., Lotufo C.M., Veiga M.C., Parada C.A., and Tambeli C.H. Indirect mechanism of histamine-induced nociception in temporomandibular joint of rats. Life Sci. 81 (2007) 765-771
70. Traub R.J., Solodkin A., Meller S.T., and Gebhart G.F. Spinal cord NADPH-diaphorase histochemical staining but not nitric oxide synthase immunoreactivity increases following carrageenan-produced hindpaw inflammation in the rat. Brain Res. 668 (1994) 204-210
71. Uludag O., Tunctan B., Altug S., Zengil H., and Abacioglu N. Twenty-four-hour variation of L-arginine/nitric oxide/cyclic guanosine monophosphate pathway demonstrated by the mouse visceral pain model. Chronobiol. Int. 24 (2007) 413-424
72. Vivancos G.G., Parada C.A., and Ferreira S.H. Opposite nociceptive effects of the arginine/NO/cGMP pathway stimulation in dermal and subcutaneous tissues. Br. J. Pharmacol. 138 (2003) 1351-1357
73. Wangensteen R., Sainz J., Rodriguez-Gomez I., Moreno J.M., Osuna A., and Vargas F. Chronic blockade of neuronal nitric oxide synthase does not affect long-term control of blood pressure in normal, saline-drinking or deoxycorticosterone-treated rats. Exp. Physiol. 88 (2003) 243-250
74. Wu J., Lin Q., Lu Y., Willis W.D., and Westlund K.N. Changes in nitric oxide synthase isoforms in the spinal cord of rat following induction of chronic arthritis. Exp. Brain Res. 118 (1998) 457-465
75. Wu J., Fang L., Lin Q., and Willis W.D. Nitric oxide synthase in spinal cord central sensitization following intradermal injection of capsaicin. Pain 95 (2001) 47-58
76. Yao D., and Sessle B.J. Nitroglycerin facilitates calcitonin gene-related peptide-induced behavior. Neuroreport 19 (2008) 1307-1311
77. Yeo J.F. Does nitric oxide play a role in orofacial pain transmission?. Ann. N.Y. Acad. Sci. 962 (2002) 151-160
78. Yeo J.F., Ling S.F., Tang N., and Ong W.Y. Antinociceptive effect of CNS peroxynitrite scavenger in a mouse model of orofacial pain. Exp. Brain Res. 184 (2008) 435-438
79. Yonehara N., Takemura M., Yoshimura M., Iwase K., Seo H.G., Taniguchi N., and Shigenaga Y. Nitric oxide in the rat spinal cord in Freund's adjuvant-induced hyperalgesia. Jpn. J. Pharmacol. 75 (1997) 327-335
80. Zhou Q., Imbe H., Dubner R., and Ren K. Persistent Fos protein expression after orofacial deep or cutaneous tissue inflammation in rats: implications for persistent orofacial pain. J. Comp. Neurol. 412 (1999) 276-291
81. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16 (1983) 109-110