Persistent Fos protein expression after orofacial deep or cutaneous tissue inflammation in rats: Implications for persistent orofacial pain

Journal of Comparative Neurology

Volumn 412, Issue 2, 1999, Pages 276-291

  Zhou, Qiqi ^a   Imbe, Hiroki ^a   Dubner, Ronald ^a   Ren, Ke ^a,b  

^a UNIVERSITY OF MARYLAND DENTAL SCHOOL   (United States)

^b Department of OCBS ^*  (United States)

Author keywords

Freund's adjuvant; Medullary dorsal horn; Paratrigeminal nucleus; Perioral skin; Temporomandibular joint

Indexed keywords

ONCOPROTEIN;

ANIMAL EXPERIMENT; ARTICLE; FACE PAIN; MALE; NOCICEPTIVE STIMULATION; NONHUMAN; PERIORAL DERMATITIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; SKIN INFLAMMATION; TRIGEMINAL NERVE;

ANIMALS; FACIAL PAIN; FREUND'S ADJUVANT; FUNCTIONAL LATERALITY; GENE EXPRESSION REGULATION; GENES, FOS; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MALE; MOUTH; MYCOBACTERIUM TUBERCULOSIS; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; SKIN; TEMPOROMANDIBULAR JOINT; TRIGEMINAL NUCLEI;

EID: 0033588931     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19990920)412:2<276::AID-CNE7>3.0.CO;2-9     Document Type: Article

References (100)

1. Abbadie C, Besson J-M. 1992. C-fos expression in rat lumbar spinal cord during the development of adjuvant-induced arthritis. Neuroscience 48:985-993.
2. Allen GV, Pronych SP. 1997. Trigeminal autonomic pathways involved in nociception-induced reflex cardiovascular responses. Brain Res 754:269-278.
3. Armstrong CL, Hopkins DA. 1998. Neurochemical organization of paratrigeminal nucleus projections to the dorsal vagal complex in the rat. Brain Res 785:49-57.
4. Arvidsson J. 1982. Somatotopic organization of vibrissae afferents in the trigeminal sensory nuclei of the rat studied by transganglionic transport of HRP. J Comp Neurol 211:84-92.
5. Arvidsson J, Pfaller K, Gmeiner S. 1992. The ganglionic origins and central projections of primary sensory neurons innervating the upper and lower lips in the rat. Somatosens Mot Res 9:199-209.
6. Bellavance LL, Beitz AJ. 1996. Altered c-fos expression in the parabrachial nucleus in a rodent model of CFA-induced peripheral inflammation. J Comp Neurol 366:431-447.
7. Bereiter DA. 1993. Microinjections of glutamate within trigeminal subnucleus interpolaris alters adrenal and autonomic function in the cat. Brain Res 622:155-162.
8. Bereiter DA, Hathaway CB, Benetti AP. 1994. Caudal portions of the spinal trigeminal complex are necessary for autonomie responses and display Fos-like immunoreactivity after corneal stimulation in the cat. Brain Res 657:73-82.
9. Bereiter DA, Bereiter DF, Hathaway CB. 1996. The NMDA receptor antagonist MK-801 reduces Fos-like immunoreactivity in central trigeminal neurons and blocks select endocrine and autonomie responses to corneal stimulation in the rat. Pain 64:179-189.
10. Broton JG, Hu JW, Sessle BJ. 1988. Effects of temporomandibular joint stimulation on nociceptive and nonnociceptive neurons of the cat's trigeminal subnucleus caudalis (medullary dorsal horn). J Neurophysiol 59:1575-1589.
11. Bullitt E. 1990. Expression of C-fos like protein as a marker for neuronal activity following noxious stimulation in the rat. J Comp Neurol 296:517-530.
12. Bullitt E, Lee CL, Light AR, Willcockson H. 1992. The effect of stimulus duration on noxious stimulus induced c-fos expression in the rodent spinal cord. Brain Res 580:172-179.
13. Burstein R, Yamamura H, Malick A, Strassman AM. 1998. Chemical stimulation of the intracranial dura induces enhanced responses to facial stimulation in brain stem trigeminal neurons. J Neurophysiol 79:964-982.
14. Capra NF. 1987. Localization and central projections of primary afferent neurons that innervate the temporomandibular joint in cats. Somatosens Res 4:201-213.
15. Capra NF, Dessem D. 1992. Central connections of trigeminal primary afferent neurons: topographical and functional considerations. Cr Rev Oral Biol Med 4:1-52.
16. Carstens E, Saxe I, Ralph R. 1995. Brainstem neurons expressing c-Fos immunoreactivity following irritant chemical stimulation of the rat's tongue. Neuroscience 69:939-953.
17. Chan-Palay V. 1978. The paratrigeminal nucleus. I. Neurons and synaptic organization. J Neurocytol 7:405-418.
18. Coggeshall RE, Lekan HA. 1996. Methods for determining numbers of cells and synapses: a case for more uniform standards of review. J Comp Neurol 364:6-15.
19. Coimbra F, Coimbra A. 1994. Dental noxious input reaches the subnucleus caudalis of the trigeminal complex in the rat, as shown by c-fos expression upon thermal or mechanical stimulation. Neurosci Lett 173:201-204.
20. Coderre TJ, Katz J, Vaccarino AL, Melzack R. 1993. Contribution of central neuroplasticity to pathological pain: review of clinical and experimental evidence. Pain 52:259-285.
21. Desclin JC. 1974. Histological evidence supporting the inferior olive as the major source of cerebellar climbing fibers in the rat. Brain Res 77:365-388.
22. Dubner R. 1991a. Basic mechanisms of pain associated with deep tissues. Can J Physiol Pharmacol 69:607-609.
23. Dubner R. 1991b. Neuronal plasticity and pain following peripheral tissue inflammation or nerve injury. In: Bond MR, Charlton JE, Woolf CJ, editors. Proceedings of the VIth World Congress on pain. Amsterdam: Elsevier. p 264-276.
24. Erickson JT, Millhorn DE. 1991. Fos-like protein is induced in neurons of the medulla oblongata after stimulation of the carotid sinus nerve in awake and anesthetized rats. Brain Res 567:11-24.
25. Feil K, Herbert H. 1995. Topographic organization of spinal and trigeminal somatosensory pathways to the rat parabrachial and Kölliker-Fuse nuclei. J Comp Neurol 353:506-528.
26. Fields HL, Basbaum AI. 1978. Brainstem control of spinal pain transmission neurons. Annu Rev Physiol 40:217-248.
27. Gartner LP, Hiatt JL, Provenza DV. 1976. Development of the squamosomandibular articulation in the Mongolian gerbil (Meriones unguiculatus). Acta Anat 96:404-417.
28. Gebhart GF, Ossipov MH. 1986. Characterization of inhibition of the spinal nociceptive tail-flick reflex in the rat from the medullary lateral reticular nucleus. J Neurosci 6:701-713.
29. Greene EC. 1955. Anatomy of the rat. New York: Hafner.
30. Haas DA, Nakanishi O, MacMillan RE, Jordan RC, Hu JW. 1992. Development of an orofacial model of acute inflammation in the rat. Arch Oral Biol 37:417-422.
31. Hammond DL, Presley R, Gogas KR, Basbaum AI. 1992. Morphine or U-50,488 suppresses Fos protein-like immunoreactivity in the spinal cord and nucleus tractus solitarii evoked by a noxious visceral stimulus in the rat. J Comp Neurol 315:244-253.
32. Harada M, Takeuchi M, Fukao T, Katagiri KA. 1971. A simple method for the quantitative extraction of dye extravasated into skin. J Pharm Pharmc 23:218-219.
33. Hargreaves K, Dubner R, Brown F, Flores C, Joris J. 1988. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32:77-88.
34. Hathaway CB, Hu JW, Bereiter DA. 1995. Distribution of Fos-like immunoreactivity in the caudal brainstem of the rat following noxious chemical stimulation of the temporomandibular joint. J Comp Neurol 356:444-456.
35. Hockfield S, Gobel S. 1982. An anatomical demonstration of projections to the medullary dorsal horn (trigeminal nucleus caudalis) from rostral trigeminal nuclei and the contralateral caudal medulla. Brain Res 252:203-211.
36. Hu JW, Sessle B, Raboisson P, Dallel R, Woda A. 1992. Stimulation of craniofacial muscle afferents induces prolonged facilitatory effects in trigeminal nociceptive brain-stem neurones. Pain 48:53-60.
37. Hunt SP, Pini A, Evan G. 1987. Induction of c-fos-like protein in spinal cord neurons following sensory stimulation. Nature 328:632-634.
38. Hylden JLK, Nahin RL, Traub RJ, Dubner R. 1989. Expansion of receptive fields of spinal lamina I projection neurons in rats with unilateral adjuvant-induced inflammation: the contribution of dorsal horn mechanisms. Pain 37:229-243.
39. Iadarola MJ, Brady LS, Draisci G, Dubner R. 1988. Enhancement of dynorphin gene expression in spinal cord following experimental inflammation: stimulus specificity, behavioral parameters and opioid receptor binding. Pain 35:313-326.
40. Imbe H, Ren K. 1999. Orofacial deep and cutaneous tissue inflammation differentially upregulates preprodynorphin mRNA in the trigeminal and paratrigeminal nuclei of the rat. Mol Brain Res 67:87-97.
41. Jacquin MF, Semba K, Rhoades RW, Egger MD. 1982. Trigeminal primary afferents project bilaterally to dorsal horn and ipsilaterally to cerebellum, reticular formation, and cuneate, solitary, supratrigeminal and vagal nuclei. Brain Res 246:285-291.
42. Jacquin MF, Semba K, Egger MD, Rhoades RW. 1983. Organization of HRP labeled trigeminal mandibular primary afferent neurons in the rat. J Comp Neurol 215:397-420.
43. Jacquin MF, Chiaia NL, Rhoades RW. 1990. Trigeminal projections to contralateral dorsal horn: central extent, peripheral origins, and plasticity. Somatosens Motor Res 7:153-183.
44. Jones SL, Blair RW. 1995. Noxious heat-evoked Fos-like immunoreactivity in the rat medulla, with emphasis on the catecholamine cell groups. J Comp Neurol 354:410-422.
45. Kajander KC, Madsen AM, Iadarola, Draisci MJG, Wakisaka S. 1996. Fos-like immunoreactivity increases in the lumbar spinal cord following a chronic constriction injury to the sciatic nerve of rat. Neurosci Lett 206:9-12.
46. Klineberg I. 1971. Structure and function of temporomandibular joint innervation. Ann R Coll Surg Engl 49:268-288.
47. Kruger L, Saporta S, Swanson LW. 1995. Photographic atlas of the rat brain. Cambridge: University Press.
48. Kuroda R, Yorimae A, Yamada Y, Nakatani J, Takatsuji K. 1995. c-fos expression after formalin injection into the face in the cat. Stereotact Funct Neurosurg 65:152-156.
49. Lanteri-Minet M, Weil-Fugazza J, dePommery J, Menetrey D. 1994. Hinbrain structures involved in pain processing as revealed by the expression of c-Fos and other immediate early gene proteins. Neuroscience 58:287-298.
50. Lima D, Esteves F, Coimbra A. 1994. C-fos activation by noxious input of spinal neurons projecting to the nucleus of the tractus solitarius in the rat. In: Gebhart GF, Hammond DL, Jensen TS, editors. Proceedings of the 7th World Congress on pain, progress in pain research and management. Vol 2. Seattle: IASP Press. p 423-434.
51. Lu J, Hathaway CB, Bereiter DA. 1993. Adrenalectomy enhances Fos-like immunoreactivity within the spinal trigeminal nucleus induced by noxious thermal stimulation of the cornea. Neuroscience 54:809-818.
52. Ma QP, Woolf CJ. 1996. Basal and touch-evoked fos-like immunoreactivity during experimental inflammation in the rat. Pain 67:307-316.
53. Marfurt CF, Rajchert DM. 1991. Trigeminal primary afferent projections to "non-trigeminal" areas of the rat central nervous system. J Comp Neurol 303:489-511.
54. Menétrey D, Gannon A, Levine JD, Basbaum AI. 1989. Expression of c-fos protein in interneurons and projection neurons of the rat spinal cord in response to noxious somatic, articular, and visceral stimulation. J Comp Neurol 285:177-195.
55. Miki K, Dubner R, Ren K. 1999. Selective antagonism of inflammatory hyperexcitability in a subpopulation of MDH nociceptive neurons by an NMDA receptor antagonist and a sodium channel blocker. IASP abstract, The IXth World Congress on Pain (in press).
56. Millan MJ, Czonkowski A, Morris B, Stein C, Arendt R, Huber A, Höllt V, Herz A. 1988. Inflammation of the hind limb as a model of unilateral, localized pain: influence on multiple opioid systems in the spinal cord of the rat. Pain 35:299-312.
57. Mitsikostas DD, Sanchez del Rio M, Waeber C, Moskowitz MA, Cutrer FM. 1998. The NMDA receptor antagonist MK-801 reduces capsaicin-induced c-fos expression within rat trigeminal nucleus caudalis. Pain 76:239-248.
58. Molander C, Xu Q, Rivero-Melian C, Grant G. 1989. Cytoarchitectonic organization of the spinal cord in the rat: II. The cervical and upper thoracic cord. J Comp Neurol 289:375-385.
59. Mönnikes H, Lauer G, Bauer C, Tebbe J, Zittel TT, Arnold R. 1997. Pathways of Fos expression in locus ceruleus, dorsal vagal complex, and PVN in response to intestinal lipid. Am J Physiol 273:R2059-R2071.
60. Munglani, R, Hunt SP. 1995. Molecular biology of pain. Br J Anaesth 75:186-192.
61. Noble HW. 1973. Comparative functional anatomy of temporomandibular joint. Oral Sci Rev 2:3-28.
62. Noguchi K, Kowalski K, Traub RJ, Solodkin A, Iadarola MJ, Ruda MA. 1991. Colocalization of dynorphin and Fos proteins in spinal cord neurons following inflammation induced hyperalgesia. Mol Brain Res 10:227-233.
63. Paxinos G, Watson C. 1986. The rat brain in stereotaxic coordinates. 2nd ed. New York: Academic.
64. Pfaller K, Arvidsson J. 1988. Central distribution of trigeminal and upper cervical primary afferents in the rat studied by anterograde transport of horseradish peroxidase conjugated to wheat germ agglutinin. J Comp Neurol 268:91-108.
65. Phelan KD, Falls WM. 1989. The interstitial system of the spinal trigeminal tract in the rat: Anatomical evidence for morphological and functional heterogeneity. Somatos Mot Res 6:367-399.
66. Presley RW, Menétrey D, Levine JD, Basbaum AI. 1990. Systemic morphine suppresses noxious stimulus-evoked Fos protein-like immunore-activity in the rat spinal cord. J Neurosci 10:323-335.
67. Randich A, Maixner W. 1984. Interactions between cardiovascular and pain regulatory systems. Neurosci Biobehav Rev 8:343-367.
68. Ren K, Dubner R. 1996a. An inflammation/hyperalgesia model for the study of orofacial pain. J Dent Res 75:217.
69. Ren K, Dubner R. 1996b. Enhanced descending modulation of nociception in rats with persistent hindpaw inflammation. J Neurophysiol 76:3025-3037.
70. Ren K, Ruda MA. 1996. Descending modulation of Fos-expression after persistent peripheral inflammation. NeuroReport 7:2186-2190.
71. Ren K, Randich A, Gebhart GF. 1990. Modulation of spinal nociceptive transmission from nuclei tractus solitarii: a relay for effects of vagal afferent stimulation. J Neurophysiol 63:971-986.
72. Ren K, Hylden JLK, Williams GM, Ruda MA, Dubner R. 1992. The effects of a non-competitive NMDA receptor antagonist, MK-801, on behavioral hyperalgesia and dorsal horn neuronal activity in rats with unilateral inflammation. Pain 50:331-344.
73. Ruigrok TJ, Cella F. 1995. Precerebellar nuclei and red nucleus. In: Paxinos G, editor. The rat nervous system, second ed. Sydney: Academic Press. p 277-308.
74. Sagar SM, Sharp FR, Curran T. 1988. Expression of c-fos protein in brain: metabolic mapping at the cellular level. Science 240:1328-1331.
75. Saper CB. 1996. Any way you cut it: a new journal policy for the use of unbiased counting methods. J Comp Neurol 364:5.
76. Sessle BJ, Hu JW. 1991. Mechanisms of pain arising from articular tissues. Can J Physiol Pharmacol 69:617-626.
77. Stein C, Millan MJ, Herz A. 1988. Unilateral inflammation of the hindpaw in rats as a model of prolonged noxious stimulation: alterations in behavior and nociceptive thresholds. Pharmacol Biochem Behav 31:445-451.
78. Strassman AM, Vos BP. 1993. Somatotopic and laminar organization of Fos-like immunoreactivity in the medullary and upper cervical dorsal horn induced by noxious facial stimulation in the rat. J Comp Neurol 331:495-516.
79. Sugimoto T, Hara T, Shirai H, Abe T, Ichikawa H, Sato T. 1994. c-Fos induction in the subnucleus cudalis following noxious mechanical stimulation of the oral mucous membrane. Exp Neurol 129:251-256.
80. Sugimoto T, Fujiyoshi Y, Xiao C, He Y-F, Ichikawa H. 1997. Central projection of calcitonin gene-related peptide (CGRP)- and substance P (SP)-immunoreactive trigeminal primary neurons in the rat. J Comp Neurol 378:425-442.
81. Takemura M, Sugimoto T, Sakai A. 1987. Topographic organization of central terminal region of different sensory branches of the rat mandibular nerve. Exp Neurol 96:540-557.
82. Teppema LJ, Veening JG, Kranenburg A, Dahan A, Berkenbosch A, Olievier C. 1997. Expression of c-fos in the rat brainstem after exposure to hypoxia and to normoxic and hyperoxic hypercapnia. J Comp Neurol 388:169-190.
83. Tölle TR, Castro-Lopes JM, Coimbra A, Zieglgänsberger W. 1990. Opiates modify induction of c-fos proto-oncogene in the spinal cord of the rat following noxious stimulation. Neurosci Lett 111:46-51.
84. 1-, μ-, or κ-opioid receptors are involved inthe tail-flick inhibition induced by β-endorphin from nucleus raphe obscurus in the pentobarbital-anesthetized rat. Eur J Pharmacol 277:251-256.
85. Uemura N, Hisano S, Fukui Y. 1997. Induction of Fos-like immunoreactivity in the lower brainstem and the spinal cord of the rat by intraperitoneal administration of an endogenous satiety substance, 2-buten-4-olide. Neurosci Lett 227:131-134.
86. Vos BP, Strassman AM. 1995. Fos expression in the medullary dorsal horn of the rat after chronic constriction injury to the infraorbital nerve. J Comp Neurol 357:362-375.
87. Wall PD, Woolf CJ. 1984. Muscle but not cutaneous C-afferent input produces prolonged increases in the excitability of the flexion reflex in the rat. J Physiol (Lond) 356:443-458.
88. Wakisaka S, Sasaki Y, Ichikawa H, Matsuo S. 1992. Increase in c-fos-like immunoreactivity in the trigeminal nucleus complex after dental treatment. Proc Finn Dent Soc 88 (Suppl 1):551-555.
89. Williams S, Evan GI, Hunt SP. 1990. Changing patterns of c-fos induction in spinal neurons following thermal cutaneous stimulation in the rat. Neuroscience 36:73-82.
90. Williams S, Evan G, Hunt SP. 1991. C-fos induction in the spinal cord after peripheral nerve lesion. Eur J Neurosci 3:887-894.
91. Woolf CJ. 1983. Evidence for a central component of post-injury pain hypersensitivity. Nature 306:686-688.
92. Woolf CJ, Thompson SWM. 1991. The induction and maintenance of central sensitization is dependent on N-methyl-D-aspartic acid receptor activation: implications for the treatment of post-injury pain hypersensitivity states. Pain 44:93-299.
93. Woolf CJ, Wall PD. 1986. Relative effectiveness of C primary afferent fibers of different origins in evoking a prolonged facilitation of the flexor reflex in the rat. J Neurosci 6:1433-1442.
94. Wu Y-P, Ling E-A. 1998. Induction of Fos-like immunoreactivity in the hypothalamic, medullary and thoracic spinal cord neurons following middle cerebral artery occlusion in rats. Neurosci Res 30:145-153.
95. Yamahiro T, Nakagawa K, Satoh K, Moriyama H, Takada K. 1997. c-fos expression in the trigeminal sensory complex and pontine parabrachial areas following experimental tooth movement. NeuroReport 8:2351-2353.
96. Yamahiro T, Satoh K, Nakagawa K, Moriyama H, Yagi T, Takada K. 1998. Expression of Fos in the rat forebrain following experimental tooth movement. J Dent Res 77:1920-1925.
97. Yu X-M, Sessle BJ, Hu JW. 1993. Differential effects of cutaneous and deep application of inflammatory irritant on mechanoreceptive field properties of trigeminal brain stem nociceptive neurons. J Neurophysiol 70:1704-1707.
98. Yu X-M, Sessle BJ, Vernon H, Hu JW. 1995. Effects of inflammatory irritant application to the rat temporomandibular joint on jaw and neck muscle activity. Pain 60:143-149.
99. Zhou Q-Q, Dubner R, Ren K. 1997a. Orofacial inflammation and trigeminal Fos protein expression in the rat. J Dent Res 76:1261.
100. Zhou Q-Q, Imbe H, Dubner R, Ren K. 1997b. Persistent Fos protein expression after orofacial deep or cutaneous tissue inflammation. Soc Neurosci Abstr 23:1809.