Archives of Oral Biology
Volume 46, Issue 8 , Pages 729-743 , August 2001

Neuropeptide expression in the ferret trigeminal ganglion following ligation of the inferior alveolar nerve

  • C Elcock

      Affiliations

    • Corresponding Author InformationCorresponding author. Department of Child Dental Health, School of Clinical Dentistry, Claremont Crescent, Sheffield, S10 2TA, UK. Tel.: +44-0114-2717849/7885/7891; fax: +44-0114-2717843
  • ,
  • F.M Boissonade
  • ,
  • P.P Robinson

,Accepted 13 February 2001.

References 

  1. Aldskogius H, Arvidsson J. Nerve cell degeneration and death in trigeminal ganglion of adult rat following peripheral nerve injury. J. Neurocytol. 1978;7:229–250
  2. Aldskogius H, Risling M. Preferential loss of unmyelinated L7 dorsal root axons following sciatic nerve resection in kittens. Brain Res. 1983;289:358–361
  3. Ambalavanar R, Morris R. The distribution of binding by isolectin I-B4 from Griffonia simplicifolia in the trigeminal ganglion and brainstem trigeminal nuclei in the rat. Neuroscience. 1992;47:421–429
  4. Arvidsson U, Ulfhake B, Cullheim S, Bergstrand A, Theodorsson E, Hökfelt T. Distribution of 125I-Galanin binding sites, immunoreactive galanin, and its coexistence with 5-hydroxytryptamine in the cat spinal cord: biochemical, histochemical, and experimental studies at the light and electron microscopic level. J. Compar. Neurol. 1991;308:115–138
  5. Atkinson ME, Shehab SAS. Peripheral axotomy of the rat mandibular trigeminal nerve leads to an increase in VIP and decrease of other primary afferent neuropeptides in the spinal trigeminal nucleus. Regul. Peptides. 1986;16:69–82
  6. Baranowski AP, Priestley JV, McMahon S. Substance P in cutaneous primary sensory neurons — A comparison of models of nerve injury that allow varying degrees of regeneration. Neuroscience. 1993;55:1025–1036
  7. Basbaum AI, Fields HL. Endogenous pain control systems: brainstem spinal pathways and endorphin circuitry. Annu. Rev. Neurosci. 1984;7:309–332
  8. Bird EV, Boissonade FMB, Robinson PP. Neuropeptide expression in the inferior alveolar nerve following transection injury. J. Dental Res. 1998;77:107
  9. Bongenhielm U, Boissonade FM, Westermark A, Robinson PP, Fried K. Sympathetic nerve sprouting fails to occur in the trigeminal ganglion after peripheral nerve injury in the rat. Pain. 2000;82(3):283–288
  10. Bongenhielm U, Nosrat CA, Nosrat I, Eriksson J, Fjell J, Fried K. Expression of sodium channel SNS/PN3 and ankyrin(G) mRNAs in the trigeminal ganglion after inferior alveolar nerve injury in the rat. Exp. Neurol. 2000;164(2):384–395
  11. Bongenhielm U, Robinson PP. Spontaneous and mechanically evoked afferent activity originating from myelinated fibres in ferret inferior alveolar nerve neuromas. Pain. 1996;67:399–406
  12. Bongenhielm U, Robinson PP. Afferent activity from myelinated inferior alveolar nerve fibres in ferrets after constriction or section and regeneration. Pain. 1998;74:123–132
  13. Budai D, Fields HL. Endogenous opioid peptides acting at mu-opioid receptors in the dorsal horn contribute to midbrain modulation of spinal nociceptive neurons. J. Neurophysiol. 1998;79(2):677–687
  14. Cavanaugh MV. Quantitative effects of the peripheral innervation on nerve and spinal ganglion cells. J. Compar. Neurol. 1951;94:181–219
  15. Cooper BY, Sessle BJ. Anatomy, physiology and pathophysiology of trigeminal system paresthesias and dysesthesias. In:  LaBanc JP,  Gregg JM editor. Oral and Maxillofacial Clinics of North America. Trigeminal Nerve Injury: Diagnosis and Management. 4 (2):1992;p. 297–322
  16. Devor M. The pathophysiology of damaged nerves. In:  Wall PD,  Melzack R editor. Textbook of Pain, Chpt. 4. Churchill Livingstone; 1994;p. 79–100
  17. Doughty SE, Atkinson ME, Shehab SA. A quantitative study of neuropeptide immunoreactive cell bodies of primary afferent neurones following rat sciatic nerve peripheral axotomy. Regul. Peptides. 1991;35:59–72
  18. Elcock, C., Boissonade, F.M., Robinson, P.P., 2001. Changes in neuropeptide expression in the trigeminal ganglion following inferior alveolar nerve section in the ferret. Neuroscience 102(3), 655–667.
  19. Fields HL. Sources of variability in the sensation of pain. Pain. 1988;33:195–200
  20. Fried K, Erdelyi G. Inferior alveolar nerve regeneration and incisor pulpal reinnervation following intramandibular neurotomy in the cat. Brain Res. 1982;244:259–268
  21. Fried K, Hildebrand C. Axon number and size distribution in the developing feline inferior alveolar nerve. J. Neurol. Sci. 1982;53:169–180
  22. Fristad I, Heyeraas KJ, Hals Kvinnsland I. Neuropeptide Y expression in trigeminal ganglion and mandibular division of the trigeminal nerve after inferior alveolar nerve axotomy in young rats. Exp. Neurol. 1996;142:276–286
  23. Fristad I, Jacobsen EB, Hals Kvinnsland I. Coexpression of vasoactive intestinal polypeptide and substance P in reinnervating pulpal nerves and in trigeminal ganglion neurones after axotomy of the inferior alveolar nerve axotomy in the rat. Arch. Oral Biol. 1998;43:183–189
  24. Gregg JM. Studies of traumatic neuralgia in the maxillofacial region: symptom complexes and response to microsurgery. J. Oral Maxillofacial Surg. 1990;48(2):135–140
  25. Gregg JM. Studies of traumatic neuralgia in the maxillofacial region: surgical pathology and neural mechanisms. J. Oral Maxillofacial Surg. 1990;48(3):228–237
  26. Hökfelt T, Weisenfeld-Hallin Z, Villar M, Melander T. Increase of galanin-like immunoreactivity in rat dorsal root ganglion after peripheral axotomy. Neurosci. Lett. 1987;83:217–220
  27. Hökfelt T, Zhang X, Wiesenfeld-Hallin Z. Messenger plasticity in primary sensory neurones following axotomy and its functional implications. Trends Neurosci. 1994;17:22–30
  28. Holland GR. Fibre numbers and sizes in the inferior alveolar nerve of the cat. J. Anat. (Lond.). 1978;127(2):343–352
  29. Holland GR, Robinson PP. Cell counts in the trigeminal ganglion of the cat after inferior alveolar nerve injuries. J. Anat. 1990;171:179–186
  30. Holland GR, Robinson PP. Peripheral nerve damage and repair. In:  Harris M,  Edgar M,  Meghji S editor. Clinical Oral Science, Chpt. 22. Oxford: Wright; 1998;p. 274–289
  31. Hua X, Boublik JH, Spicer MA, Rivier JE, Brown MR, Yaksh TL. The antinociceptive effects of spinally administered neuropeptide Y in the rat; Systematic studies on structure–activity relationship. J. Pharmacol. Exp. Ther. 1991;258:243–248
  32. Hunt SP, Rossi J. Peptide- and non-peptide-containing unmyelinated primary afferents: the parallel processing of nociceptive information. Phil. Trans. R. Soc. Lond. B. 1985;308:283–289
  33. Jessell TM, Iversen LL, Cuello AC. Capsaicin-induced depletion of substance P from primary sensory neurones. Brain Res. 1978;152:183–188
  34. Jessell T, Tsunoo A, Kanazawa I, Otsuka M. Substance P: depletion in the dorsal horn of the rat spinal cord after section of the peripheral processes of primary sensory neurones. Brain Res. 1979;168:247–259
  35. Kashiba H, Senba E, Ueda Y, Tohyama M. Co-localised but target-unrelated expression of vasoactive intestinal polypeptide and galanin in rat dorsal root ganglion neurons after peripheral nerve crush injury. Brain Res. 1992;582:47–57
  36. Kipp DP, Goldstein BH, Weiss WW. Dysaesthesia after mandibular third molar surgery: a retrospective study. J. Am. Dental Assoc. 1980;100:185–192
  37. Lawson SN, Waddell PJ. Soma neurofilament immunoreactivity is related to cell size and fibre conduction velocity in rat primary sensory neurons. J. Physiol. 1991;435:41–63
  38. Lee Y, Kawai Y, Shiosaka S, Takami K, Kiyama H, Hillyard CJ, et al.  Coexistence of calcitonin gene-related peptide and substance P-like peptide in single cells of the trigeminal ganglion of the rat: immunohistochemical analysis. Brain Res. 1985;330:194–196
  39. Lee Y, Takami K, Kawai Y, Girgis S, Hillyard CJ, MacIntyre I, et al.  Distribution of calcitonin gene-related peptide in the rat peripheral nervous system with reference to its coexistence with substance P. Neuroscience. 1985;15:1227–1237
  40. Lisney SJW. Regeneration of unmyelinated axons after injury of mammalian peripheral nerve. Q. J. Exp. Physiol. 1989;74(6):757–784
  41. Long A, Bongenhielm U, Boissonade FMB, Fried K, Robinson PP. Neuropeptide immunoreactivity in ligature-induced neuromas of the inferior alveolar nerve in the ferret. Brain Res. 1998;791:263–270
  42. Molander C, Wang HF, Riverio-Melián C, Grant G. Early decline and late restoration of spinal cord binding and transganglionic transport of isolectin B4 from Griffonia simplicifolia I after peripheral nerve transection or crush. Restor. Neurol. Neurosci. 1996;10:123–133
  43. Munglani R, Hudspith MJ, Hunt SP. The therapeutic potential of neuropeptide Y. Analgesic, anxiolytic and antihypertensive. Drugs. 1996;52(3):371–389
  44. Noguchi K, De León M, Nahin RL, Senba E, Ruda MA. Quantification of axotomy-induced alteration of neuropeptide mRNAs in dorsal root ganglion neurons with special reference to neuropeptide Y mRNA and the effects of neonatal capsaicin treatment. J. Neurosci. 1993;35:54–66
  45. Plenderleith MB, Cameron AA, Key B, Snow PJ. The plant lectin soybean agglutinin binds to the soma, axon and central terminals of a subpopulation of small diameter primary sensory neurons in the rat and cat. Neuroscience. 1989;31(3):683–695
  46. Plenderleith MB, Snow PJ. The effect of peripheral nerve section on lectin binding in the superficial dorsal horn of the rat spinal cord. Brain Res. 1990;507:146–150
  47. Post C, Alari L, Hökfelt T. Intrathecal galanin increases the latency in the tail-flick and hot-plate test in mouse. Acta. Physiol. Scand. 1988;132:583–584
  48. Ranson SW. Retrograde degeneration in the spinal nerves. J. Compar. Neurol. 1906;16:265–293
  49. Ranson SW. Alterations in the spinal ganglion cells following neurotomy. J. Compar. Neurol. 1909;19:125–153
  50. Rood JP. Lingual split technique. Damage to inferior alveolar and lingual nerves during removal of impacted mandibular third molars. Br. Dental J. 1983;154:402–403
  51. Rydh-Rinder M, Holmberg K, Elfvin L-G, Wiesenfeld-Hallin Z, Hökfelt T. Effects of peripheral axotomy on neuropeptides and nitric oxide synthase in dorsal root ganglia and spinal cord of the guinea pig: an immunohistochemical study. Brain Res. 1996;707:180–188
  52. Salt TE, Hill RH. Neurotransmitter candidates of somatosensory primary afferent fibres. Neuroscience. 1983;10(4):1083–1103
  53. Shehab SAS, Atkinson ME. Vasoactive intestinal polypeptide increases in areas of the dorsal horn of the spinal cord from which other neuropeptides are depleted following peripheral axotomy. Exp. Brain Res. 1986;62:422–430
  54. Silverman JD, Kruger L. Selective neuronal glycoconjugate expression in sensory and autonomic ganglia: a relation of lectin reactivity to peptide and enzyme markers. J. Neurocytol. 1990;19:789–801
  55. Skofitsch G, Jacobowitz DM. Calcitonin gene-related peptide coexists with substance P in capsaicin sensitive neurons and sensory ganglia of the rat. Peptides. 1985;6:747–754
  56. Skofitsch G, Jacobowitz DM. Galanin-like immunoreactivity in capsaicin sensitive sensory neurons and ganglia. Brain Res. Bull. 1985;15:191–195
  57. Streit WJ, Schulte BA, Balentine JD, Spicer SS. Histochemical localisation of galactose-containing glycoconjugates in sensory neurons and their processes in the central and peripheral nervous system of the rat. J. Histochem. Cytochem. 1985;33(10):1042–1052
  58. Streit WJ, Schulte BA, Balentine JD, Spicer SS. Evidence for glycoconjugate in nociceptive primary sensory neurons and its origin from the golgi complex. Brain Res. 1986;377:1–17
  59. Sunderland S. In: Nerve Injuries and their Repair, A Critical Appraisal. Chpt. 33, Nerve Injury and Sensory Function. London: Churchill Livingstone; 1991;p. 305–331
  60. Tal M, Devor M. Ectopic discharge in injured nerves: comparison of trigeminal and somatic afferents. Brain Res. 1992;579:148–151
  61. Tong Y-G, Wang HF, Ju G, Grant G, Hökfelt T, Zhang X. Increased uptake and transport of cholera-toxin B-subunit in dorsal root ganglion neurons after peripheral axotomy: possible implications for sensory sprouting. J. Compar. Neurol. 1999;404:143–158
  62. Van Gool AV, Ten Bosch JJ, Boering G. Clinical consequences of complaints and complications after removal of the mandibular third molar. Int. J. Oral Surg. 1977;6:29–37
  63. Villar MJ, Cortés R, Theodorsson E, Wiesenfeld-Hallin Z, Schalling Z, Fahrenkrug J, et al.  Neuropeptide expression in dorsal root ganglion cells and spinal cord after peripheral nerve injury with special reference to galanin. Neuroscience. 1989;33:587–604
  64. Villar MJ, Wiesenfeld-Hallin Z, Xu XJ, Theodorsson E, Emson PC, Hökfelt T. Further studies on Galanin-, Substance P-, and CGRP-like immunoreactivities in primary sensory neurons and spinal cord: Effect of dorsal rhizotomies and sciatic nerve lesions. Exp. Neurol. 1991;122:29–39
  65. Wakisaka S, Kajander KC, Bennett GJ. Increased neuropeptide Y (NPY)-like immunoreactivity in rat sensory neurons following peripheral axotomy. Neurosci. Lett. 1991;124:200–203
  66. Wakisaka, S., Takikita, S., Sasaski, Y., Kato, J., Tabata, M.J., Kurisu, K., 1993. Cell size-specific appearance of neuropeptide Y in the trigeminal ganglion following peripheral axotomy of different branches of the mandibular nerve of the rat. Brain Res. 347–350.
  67. Wall PD, Gutnick M. Ongoing activity in peripheral nerves: The physiology and pharmacology of impulses originating in a neuroma. Exp. Neurol. 1974;43:580–593
  68. Wang H, Rivero-Melián C, Robertson B, Grant G. Transganglionic transport and binding of the isolectin B4 from Griffonia simplicifolia I in rat primary sensory neurons. Neuroscience. 1994;62:539–551
  69. Watkins LR, Mayer DJ. Organization of endogenous opiate and nonopiate pain control systems. Science. 1982;216:1185–1192
  70. Wiesenfeld-Hallin Z, Villar MJ, Hökfelt T. The effects of intrathecal galanin and C-fiber stimulation on the flexor reflex in the rat. Brain Res. 1989;486:205–213
  71. Xu JY, Fujimoto JM, Tseng LF. Involvement of supraspinal epsilon and mu opioid receptors in inhibition of the tail-flick response induced by etorphine in the mouse. J. Pharmacol. Exp. Ther. 1992;263(1):246–252
  72. Yaksh TL, Malmberg AB. Central pharmacology of nociceptive transmission. In:  Wall PD,  Melzack R editor. Textbook of Pain, Chpt. 9. Churchill Livingstone; 1994;p. 165–200
  73. Yanagisawa Y-M, Yagi N, Otsuka M, Yanaihara C, Yanaihara N. Inhibitory effects of galanin on the isolated spinal cord of the newborn rat. Neurosci. Lett. 1986;70(2):278–282
  74. Zhang Q, Ji R-R, Lindsay R, Hökfelt T. Effect of growth factors on substance P mRNA expression in axotomised dorsal root ganglia. NeuroReport. 1995;6:1309–1312
  75. Zhang X, Ji R-R, Arvidsson J, Lundberg JM, Bartfai T, Bedecs K, et al.  Expression of peptides, nitric oxide synthase and NPY receptor in trigeminal and nodose ganglia after nerve lesions. Exp. Brain Res. 1996;111:393–404
  76. Zhang X, Ju G, Elde R, Hökfelt T. Effect of peripheral nerve cut on neuropeptides in dorsal root ganglia and the spinal cord of monkey with special reference to galanin. J. Neurocytol. 1993;22:281–342
  77. Zhang X, Shi T, Holmberg K, Landry M, Huang W, Xiao H, et al.  Expression and regulation of neuropeptide Y Y2 receptor in sensory autonomic ganglion. Proc. Natl. Acad. Sci. 1997;94:729–734

PII: S0003-9969(01)00029-2

doi: 10.1016/S0003-9969(01)00029-2

Archives of Oral Biology
Volume 46, Issue 8 , Pages 729-743 , August 2001