Regeneration of periodontal Ruffini endings in adults and neonates

Microscopy Research and Technique

Volumn 60, Issue 5, 2003, Pages 516-527

  Wakisaka, Satoshi ^a   Atsumi, Yukako ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

Development; Neonatal injury; Periodontal Ruffini endings; Regeneration

Indexed keywords

CELLS; CYTOLOGY; NEURONS; TISSUE REGENERATION;

CELL-BE; CELL/B.E; CELL/BE; DEVELOPMENT; INFERIOR ALVEOLAR NERVES; MECHANORECEPTORS; NEONATAL INJURY; PERIODONTAL RUFFINI ENDING; REGENERATION; SCHWANN CELLS;

RATS;

CELL MIGRATION; CELLULAR DISTRIBUTION; INCISOR; INFERIOR ALVEOLAR NERVE; LAMELLAR BODY; MECHANORECEPTOR; MOLECULAR MECHANICS; NERVE ENDING; NEWBORN; NONHUMAN; PERIODONTICS; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RAT; REGENERATION; REVIEW; RUFFINI ENDING; SCHWANN CELL; TISSUE REGENERATION;

EID: 0037376454     PISSN: 1059910X     EISSN: None     Source Type: Journal    
DOI: 10.1002/jemt.10292     Document Type: Review

References (112)

1. Andressen C, Blümcke I, Celio MR. 1993. Calcium-binding proteins: selective markers of nerve cells. Cell Tissue Res 271:181-208.
2. Arvidsson J, Ygge J, Grant G. 1986. Cell loss in lumbar dorsal root ganglia and transganglionic degeneration after sciatic nerve resection in the rat. Brain Res 373:15-21.
3. Asahito T, Ohshima H, Hanada K, Wakisaka S, Maeda T. 1999. Postnatal expression of calretinin-immunoreactivity in periodontal Ruffini endings in the rat incisor: A comparison with protein gene product 9.5 (PGP 9.5)-immunoreactivity. Arch Histol Cytol 62:57-69.
4. Atsumi Y, Hayashi S, Nakakura-Ohshima K, Maeda T, Kurisu K, Wakisaka S. 1999a. Heterogeneous localizations of Trk B among individual periodontal Ruffini endings in the rat incisor. Arch Histol Cytol 62:435-440.
5. Atsumi Y, Matsumoto K, Sakuda M, Maeda T, Kurisu K, Wakisaka S. 1999b. Altered distribution of Schwann cells in the periodontal ligament of the rat incisor following resection of the inferior alveolar nerve: an immunohistochemical study on S-100 proteins. Brain Res 849:187-195.
6. Atsumi Y, Imai T, Matsumoto K, Sakuda M, Maeda T, Kurisu K, Wakisaka S. 2000a. Effects of different types of injury to the inferior alveolar nerve on the behavior of Schwann cells during the regeneration of periodontal nerve fibers of rat incisor. Arch Histol Cytol 63:43-54.
7. Atsumi Y, Ajima H, Maeda T, Kurisu K, Wakisaka S. 2000b. Delayed expression of calbindin D28k during regeneration of the periodontal Ruffini endings of the rat incisor following injury to the inferior alveolar nerve. Cells Tissues Organs 167:285-289.
8. Atsumi Y, Imai T, Matsumoto K, Sakuda M, Kurisu K, Wakisaka S. 2000c. Effects of neonatal injury of the inferior alveolar nerve on the development and regeneration of periodontal nerve fibers in the rat incisor. Brain Res 871:201-209.
9. Beertsen W, Everts V, van den Hooff A. 1974. Fine structure and possible function of cells containing leptomergic organelles in the periodontal ligament of the rat incisor. Arch Oral Biol 19:1099-1100.
10. Benowitz LI, Routtenberg A. 1987. A membrane phosphoprotein associated with neural development, axonal regeneration, phospholipid metabolism, and synaptic plasticity. Trends Neurosci 10:527-532.
11. Benowitz LI, Apostolides PJ, Perrone-Bizzozero N, Finklestein SP, Zwiers H. 1988. Anatomical distribution of the growth-associated protein GAP-43/B-50 in the adult rat brain. J Neurosci 8:339-352.
12. Biemesderfer D, Munger BL, Dubner R. 1978. The pilo-Ruffini complex: a non-sinus hair and associated slowly-adapting mechanoreceptor in primate facial skin. Brain Res 142:197-222.
13. Bothwell M. 1991. Keeping track of neurotrophin receptors. Cell 65: 915-918.
14. Bothwell M. 1995. Functional interactions of neurotrophins and neurotrophin receptors. Ann Rev Neurosci 18:223-253.
15. Byers MR. 1985. Sensory innervation of periodontal ligament of rat molars consists of unencapsulated Ruffini-like mechanoreceptors and free nerve endings. J Comp Neurol 231:500-518.
16. Byers MR. 1990. Segregation of NGF receptor in sensory receptors, nerves and local cells of teeth and periodontium demonstrated by EM immunocytochemistry. J Neurocytol 19:765-775.
17. Byers MR, Dong WK. 1989. Comparison of trigeminal receptor location and structure in the periodontal ligament of different types of teeth from the rat, cat, and monkey. J Comp Neurol 279:117-127.
18. Byers MR, Maeda T. 1997. Periodontal innervation: regional specializations, ultrastructure, cytochemistry and tissue interactions. Acta Med Dent Helv 2:116-133.
19. Byers MR, O'Connor TA, Martin RF, Dong WK. 1986. Mesencephalic trigeminal sensory neurons of cat: axon pathways and structure of mechanoreceptive endings in periodontal ligament. J Comp Neurol 250:181-191.
20. Carr PA, Nagy JI. 1993. Emerging relationships between cytochemical properties and sensory modality transmission in primary sensory neurons. Brain Res Bull 30:209-219.
21. Carr PA, Yamamoto T, Karmy G, Baimbridge KG, Nagy JI. 1989. Analysis of parvalbumin and calbindin D28k-immunoreactive neurons in dorsal root ganglia of rat in relation to their cytochrome oxidase and carbonic anhydrase content. Neuroscience 33:363-371.
22. Carr PA, Yamamoto T, Karmy G, Nagy JI. 1991. Cytochemical relationships and central terminations of a unique population of primary afferent neurons in rat. Brain Res Bull 26:825-843.
23. Celio MR. 1990. Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35:375-475.
24. Chambers MR, Andres KH, von Düring M, Iggo A. 1972. The structure and function of the slowly adapting type II mechanoreceptor in hairy skin. Q J Exp Physiol 57:417-445.
25. Curtis R. 1993. Growth-associated protein-43 (GAP-43) is expressed by glial cells of the central and peripheral nervous system. Ann NY Acad Sci 679:407-411.
26. Curtis R, Stewart HJ, Hall SM, Wilkin GP, Mirsky R, Jessen KR. 1992. GAP-43 is expressed by nonmyelin-forming Schwann cells of the peripheral nervous system. J Cell Biol 116:1455-1464.
27. Curtis R, Green D, Lindsay RM, Wilkin GP. 1993. Up-regulation of GAP-43 and growth of axons in rat spinal cord after compression injury. J Neurocytol 22:51-64.
28. Del Valle ME, Vazquez E, Represa J, Malinovsky L, Vega JA. 1994. Immunohistochemical localization of calcium-binding proteins in the human cutaneous sensory corpuscles. Neurosci Lett 168:247-250.
29. Duc C, Barakat-Walter I, Droz B. 1994. Innervation of putative rapidly adapting mechanoreceptors by calbindin- and calretinin-immunoreactive primary sensory neurons in the rat. Eur J Neurosci 6:264-271.
30. Everts V, Beertsen W, van den Hooff A. 1977. Fine structure of an end organ in the periodontal ligament of the mouse incisor. Anat Rec 189:73-89.
31. Fundin BT, Silos Santiago I, Ernfors P, Fagan AM, Aldskogius H, DeChiara TM, Phillips HS, Barbacid M, Yancopoulos GD, Rice FL. 1997. Differential dependency of cutaneous mechanoreceptors on neurotrophins, trk receptors, and P75 LNGFR. Dev Biol 190:94-116.
32. Ghosh A, Greenberg ME. 1995. Calcium signaling in neurons: molecular mechanisms and cellular consequences. Science 268:239-247.
33. Gordon-Weeks PR. 1987. The cytoskeletons of isolated, neuronal growth cones. Neuroscience 21:977-989.
34. Gottschaldt KM, Fruhstorfer H, Schmidt W, Kraft I. 1982. Thermosensitivity and its possible fine-structural basis in mechanoreceptors in the beak skin of geese. J Comp Neurol 205:219-245.
35. Hayashi S, Nakakura-Ohshima K, Ohshima H, Noda T, Honma S, Wakisaka, S, Maeda T. 2000. The development of terminal Schwann cells associated with periodontal Ruffini endings in the rat incisor ligament. Brain Res 858:167-171.
36. Hietanen-Peltola M, Pelto-Huikko M, Rechardt L, Emson P, Hökfelt T. 1992a. Calbindin D-28k-immunoreactivity in rat muscle spindle; a light and electron microscopic study. Brain Res 579:327-332.
37. Hietanen-Peltola M, Pelto-Huikko M, Rechardt L, Hökfelt T. 1992b. Calbindin D-28k-immunoreactivity in rat muscle spindles during postnatal maturation and after denervation. Histochem J 24:673-678.
38. Himes BT, Tessler A. 1989. Death of some dorsal root ganglion neurons and plasticity of others following sciatic nerve section in adult and neonatal rats. J Comp Neurol 284:215-230.
39. Hiroshima K, Maeda T, Hanada K, Wakisaka S. 1998. Calretinin-like immunoreactivity in the regenerating periodontal Ruffini endings of the rat incisor following injury to the inferior alveolar nerve. Brain Res 807:218-221.
40. Hua X-Y, Boublik JH, Spicer MA, Rivier JE, Brown MR, Yaksh TL. 1991. The antinociceptive effects of spinally administered neuropeptide Y in the rat: systematic studies on structure-activity relationship. J Pharmacol Exp Ther 258:243-248.
41. Ichikawa H, Jacobowitz DM, Sugimoto T. 1993. Calretinin-immunoreactive neurons in the trigeminal and dorsal root ganglia of the rat. Brain Res 617:96-102.
42. Ichikawa H, Deguchi T, Nakago T, Jacobowitz DM, Sugimoto T. 1994. Parvalbumin, calretinin and carbonic anhydrase in the trigeminal and spinal primary neurons of the rat. Brain Res 655:241-245.
43. Ichikawa H, Xiao C, He Y-F, Sugimoto T. 1996. Parvalbumin-immunoreactive nerve endings in the periodontal ligaments of rat teeth. Arch Oral Biol 41:1087-1090.
44. Ichikawa H, Jacobowitz DM, Sugimoto T. 1997a. S100 protein-immunoreactive primary sensory neurons in the trigeminal and dorsal root ganglia of the rat. Brain Res 748:253-257.
45. Ichikawa H, Jacobowitz DM, Sugimoto T. 1997b. Coexpression of calretinin and parvalbumin in Ruffini-like endings in the rat incisor periodontal ligament. Brain Res 770:294-297.
46. Jacobson RD, Virag I, Skene JH. 1986. A protein associated with axon growth, GAP-43, is widely distributed and developmentally regulated in rat CNS. J Neurosci 6:1843-1855.
47. Kannari K. 1990. Sensory receptors in the periodontal ligament of hamster incisors with special reference to the distribution, ultrastructure and three-dimensional reconstruction of Ruffini endings. Arch Histol Cytol 53:559-573.
48. Kannari K, Sato O, Maeda T, Iwanaga T, Fujita T. 1991. A possible mechanism of mechanoreception in Ruffini endings in the periodontal ligament of hamster incisors. J Comp Neurol 313:368-376.
49. Kato J, Wakisaka S, Kurisu K. 1996. Immunohistochemical changes in the distribution of nerve fibers in the periodontal ligament during an experimental tooth movement of the rat molar. Acta Anat 157:53-62.
50. Kobayashi H, Ochi K, Saito I, Hanada K, Maeda T. 1998. Alterations in ultrastructural localization of growth-associated protein-43 (GAP-43) in periodontal Ruffini endings of rat molars during experimental tooth movement. J Dent Res 77:503-517.
51. Kvinnsland I, Heyeraas KJ. 1992. Effect of traumatic occlusion on CGRP and SP immunoreactive nerve fibre morphology in rat molar pulp and periodontium. Histochemistry 97:111-120.
52. Kvinnsland I, Kvinnsland S. 1990. Changes of CGRP-immunoreactive nerve fibers during experimental tooth movement in rat. Eur J Orthodont 12:320-329.
53. Lundberg JM, Terenius L, Hökfelt T, Martling CR, Tatemoto K, Mutt V, Polak J, Bloom S, Goldstein M. 1982. Neuropeptide Y (NPY)-like immunoreactivity in peripheral noradrenergic neurons and effects of NPY on sympathetic function. Acta Physiol Scand 116:477-480.
54. Maeda T. 1987. Sensory innervation of the periodontal ligament in the incisor and molar of the monkey, Macaca fuscata. An immunohistochemical study for neurofilament protein and glia-specific S-100 protein. Arch Histol Jpn 50:437-454.
55. Maeda T, Byers MR. 1996. Different localizations of growth-associated protein (GAP-43) in mechanoreceptors and free nerve endings of adult rat periodontal ligament, dental pulp and skin. Arch Histol Cytol 59:291-304.
56. Maeda T, Sato O, Kobayashi S, Iwanaga T, Fujita T. 1989. The ultrastructure of Ruffini endings in the periodontal ligament of rat incisors with special reference to the terminal Schwann cells (K-cells). Anat Rec 223:95-103.
57. Maeda T, Kannari K, Sato O, Iwanaga T. 1990a. Nerve terminals in human periodontal ligament as demonstrated by immunohistochemistry for neurofilament protein (NFP) and S-100 protein. Arch Histol Cytol 53:259-265.
58. Maeda T, Kannari K, Sato O, Kobayashi S, Iwanaga T, Fujita T. 1990b. Cholinesterase activity in terminal Schwann cells associated with Ruffini endings in the periodontal ligament of rat incisors. Anat Rec 228:339-344.
59. Maeda T, Ochi K, Nakakura-Ohshima K, Youn SH, Wakisaka S. 1999. The Ruffini endings as the primary mechanoreceptor in the periodontal ligament: its morphology, cytochemical features, regeneration, and development. Crit Rev Oral Biol Med 10:307-327.
60. Meakin SO, Shooter EM. 1992. The nerve growth factor family of receptors. Trends Neurosci 15:323-331.
61. Mehta A, Reynolds ML, Woolf CJ. 1993. Partial denervation of the medial gastrocnemius muscle results in growth-associated protein-43 immunoreactivity in sprouting axons and Schwann cells. Neuroscience 57:433-442.
62. Mirsky R, Jessen KR. 1996. Schwann cell development, differentiation and myelination. Curr Opin Neurobiol 6:89-96.
63. Mirsky R, Jessen KR. 1999. The neurobiology of Schwann cells. Brain Pathol 9:293-311.
64. Munger BL, Ide C. 1988. The structure and function of cutaneous sensory receptors. Arch Histol Cytol 51:1-34.
65. Nakakura-Ohshima K, Maeda T, Sato O, Takano Y. 1993. Postnatal development of periodontal innervation in rat incisors: an immunohistochemical study using protein gene product 9.5 antibody. Arch Histol Cytol 56:385-398.
66. Nakakura-Ohshima K, Maeda T, Ohshima H, Noda T, Takano Y. 1995. Postnatal development of periodontal Ruffini endings in rat incisors: an immunoelectron microscopic study using protein gene product 9.5 (PGP 9.5) antibody. J Comp Neurol 362:551-564.,
67. Ochi K, Wakisaka S, Youn SH, Hanada K, Maeda T. 1997a. Immunohistochemical localization of calbindin D28k in the periodontal Ruffini endings of rat incisors. Neurosci Lett 228:195-198.
68. Ochi K, Wakisaka S, Youn SH, Hanada K, Maeda T. 1997b. Calretinin-like immunoreactivity in the Ruffini endings, slowly adapting mechanoreceptors, of the periodontal ligament of the rat incisor. Brain Res 769:183-187.
69. Plantinga LC, Verhaagen J, Gispen WH. 1993. The expression of B-50/GAP-43 in Schwann cells. Ann NY Acad Sci 679:412-417.
70. Renehan WE, Munger BL. 1986. Degeneration and regeneration of peripheral nerve in the rat trigeminal system. II. Response to nerve lesions. J Comp Neurol 249:429-459.
71. Reynolds ML, Woolf CJ. 1992. Terminal Schwann cells elaborate extensive processes following denervation of the motor endplate. J Neurocytol 21:50-66.
72. Saito I, Ishii K, Hanada K, Sato O, Maeda T. 1991. Responses of calcitonin gene-related peptide-immunopositive nerve fibres in the periodontal ligament of rat molars to experimental tooth movement. Arch Oral Biol 36:689-692.
73. Saito I, Hanada K, Maeda T. 1993. Alteration of nerve growth factor-receptor expression in the periodontal ligament of the rat during experimental tooth movement. Arch Oral Biol 38:923-929.
74. Sasaki Y, Wakisaka S, Kurisu K. 1994. Effects of peripheral axotomy of the inferior alveolar nerve on the levels of neuropeptide Y in rat trigeminal primary afferent neurons. Brain Res 664:108-114.
75. Sasamura T. 1986. Degeneration and regeneration of Ruffini corpuscles in the joint capsule. J Jpn Orthop Assoc 60:1157-1166.
76. Sato O, Maeda T, Kobayashi S, Iwanaga T, Fujita TY, Takahashi Y. 1988. Innervation of periodontal ligament and dental pulp in the rat incisor: an immunohistochemical investigation of neurofilament protein and glia-specific S-100 protein. Cell Tissue Res 251:13-21.
77. Sato O, Maeda T, Iwanaga T, Kobayashi S. 1989. Innervation of the incisors and periodontal ligament in several rodents: an immunohistochemical study of neurofilament protein and glia-specific S-100 protein. Acta Anat 134:94-99.
78. Sato O, Maeda T, Kannari K, Kawahara I, Iwanaga T, Takano Y. 1992. Innervation of the periodontal ligament in the dog with special reference to the morphology of Ruffini endings. Arch Histol Cytol 55:21-30.
79. Scherer SS, Xu YT, Roling D, Wrabetz L, Feltri ML, Kamholz J. 1994. Expression of growth-associated protein-43 kD in Schwann cells is regulated by axon-Schwann cell interactions and cAMP. J Neurosci Res 38:575-589.
80. Schmalbruch H. 1987. Loss of sensory neurons after sciatic nerve section in the rat. Anat Rec 219:323-329.
81. Schroeder HE. 1986. Periodontal ligament. In: Oksche A, Vollrath L, editors. Handbook of microscopic anatomy, vol. V/5: the periodontium. Berlin: Springer-Verlag; p 170-233.
82. Sharkey KA, Coggins PJ, Tetzlaff W, Zwiers H, Bisby MA, Davision JS. 1990. Distribution of growth-associated protein, B-50 (GAP-43) in the mammalian enteric nervous system. Neuroscience 38:13-20.
83. Shore RC, Berkovitz BK. 1987. Model to explain differential movement of periodontal fibroblasts. Arch Oral Biol 23:507-509.
84. Skene JH. 1989. Axonal growth-associated proteins. Ann Rev Neurosci 12:127-156.
85. Skene JH, Willard M. 1981. Axonally transported proteins associated with axon growth in rabbit central and peripheral nervous systems. J Cell Biol 89:96-103.
86. Snider WD, Elliott JL, Yan Q. 1992. Axotomy-induced neuronal death during development. J Neurobiol 23:1231-1246.
87. Sodeyama T, Maeda T, Takano Y, Hara K. 1996. Responses of periodontal nerve terminals to experimentally induced occlusal trauma in rat molars: an immunohistochemical study using PGP 9.5 antibody. J Periodont Res 31:235-248.
88. Sommervaille T, Reynolds ML, Woolf CJ. 1991. Time-dependent differences in the increase in GAP-43 expression in dorsal root ganglion cells after peripheral axotomy. Neuroscience 45:213-220.
89. Spencer PS, Schaumburg HH. 1973. An ultrastructural study of the inner core of the Pacinian corpuscle. J Neurocytol 2:217-235.
90. Stewart HJ, Cowen T, Curtis R, Wilkin GP, Mirsky R, Jessen KR. 1992. GAP-43 immunoreactivity is widespread in the autonomic neurons and sensory neurons of the rat. Neuroscience 47:673-684.
91. ++-ATPases in Meissner's corpuscle of the Mongolian gerbil. Arch Histol Cytol 55:375-379.
92. Tachibana T, Nawa T, Mizuhira V, Yoshida Y. 1992. Ultrastructural localization of calcium in mechanoreceptors of the oral mucosa. J Neurocytol 21:745-753.
93. Tachibana T, Iida S, Nawa T. 1995. Type-VI collagen as a major component in the interstitial matrix of cutaneous mechanoreceptors. Arch Histol Cytol 58:507-515.
94. Tetzlaff W, Zwiers H, Lederis K, Cassar L, Bisby MA. 1989. Axonal transport and localization of B-50/GAP-43-like immunoreactivity in regenerating sciatic and facial nerves of the rat. J Neurosci 9:1303-1313.
95. Verhaagen J, van Hooff CO, Edwards PM, De Graan PN, Oestreicher AB, Schotman P, Jennekens FG, Gispen WH. 1986. The kinase C substrate protein B-50 and axonal regeneration. Brain Res Bull 17:737-741.
96. Verhaagen J, Oesteicher AB, Edwards PM, Veldman H, Jennekens FG, Gispen WH. 1988. Light- and electron-microscopical study of phosphoprotein B-50 following denervation and reinnervation of the rat soleus muscle. J Neurosci 8:1759-1766.
97. Wakisaka S, Kajander KC, Bennett GJ. 1991. Increased neuropeptide Y (NPY)-like immunoreactivity in rat sensory neurons following peripheral axotomy. Neurosci Lett 124:200-203.
98. Wakisaka S, Kajander KC, Bennett GJ. 1992. Effects of peripheral nerve injuries and tissue inflammation on the levels of neuropeptide Y-like immunoreactivity in rat primary afferent neurons. Brain Res 598:349-352.
99. Wakisaka S, Takikita S, Sasaki Y, Kato J, Tabata MJ, 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 620:347-350.
100. Wakisaka S, Sasaki Y, Kurisu K. 1995. Temporal analysis of neuropeptide Y expression in the rat trigeminal ganglion following peripheral axotomy of the inferior alveolar nerve. Neurosci Lett 188:49-52.
101. Wakisaka S, Youn SH, Kato J, Takemura M, Kurisu K. 1996a. Neuropeptide Y-immunoreactive primary afferents in the dental pulp and periodontal ligament following nerve injury to the inferior alveolar nerve in the rat. Brain Res 712:11-18.
102. Wakisaka S, Youn SH, Maeda T, Kurisu K. 1996b. Immunoelectron microscopic study on neuropeptide Y in the periodontal ligament of the incisor following peripheral nerve injury to the inferior alveolar nerve in the rat. Brain Res 729:259-263.
103. Wakisaka S, Youn SH, Miyawaki Y, Kurisu K. 1996c. The effects of peripheral nerve injury of the masseteric nerve on the levels of calcium binding proteins and neuropeptide Y, and their correlation in the mesencephalic trigeminal nucleus of the rat. Brain Res 735: 249-256.
104. Wakisaka S, Youn SH, Maeda T, Kurisu K. 1996d. Neuropeptide Y-like immunoreactive primary afferents in the periodontal tissues following dental injury in the rat. Regul Peptides 63:163-169.
105. Wakisaka S, Atsumi Y, Youn SH, Maeda T. 2000. Morphological and cytochemical characteristics of periodontal Ruffini ending under normal and regeneration processes. Arch Histol Cytol 63:91-113.
106. White DM. 1998. Contribution of neurotrophin-3 to the neuropeptide Y-induced increase in neurite outgrowth of rat dorsal root ganglion cells. Neuroscience 86:257-263.
107. White DM, Mansfield K. 1996. Vasoactive intestinal polypeptide and neuropeptide Y act indirectly to increase neurite outgrowth of dissociated dorsal root ganglion cells. Neuroscience 73:881-887.
108. Woolf CJ, Reynolds ML, Molander C, O'Brien C, Lindsay RM, Benowitz LI. 1990. The growth-associated protein GAP-43 appears in dorsal root ganglion cells and in the dorsal horn of the rat spinal cord following peripheral nerve injury. Neuroscience 34:465-478.
109. Woolf CJ, Reynolds ML, Chong MS, Emson P, Irwin N, Benowitz LI. 1992. Denervation of the motor endplate results in the rapid expression by terminal Schwann cells of the growth-associated protein GAP-43. J Neurosci 12:3999-4010.
110. Youn SH, Sakuda M, Kurisu K, Wakisaka S. 1997. Regeneration of periodontal primary afferents of the rat incisor following injury of the inferior alveolar nerve with special reference to neuropeptide Y-like immunoreactive primary afferents. Brain Res 752:161-169.
111. Youn SH, Maeda T, Kurisu K, Wakisaka S. 1998. Growth-associated protein-43 (GAP-43) in the regenerating periodontal Ruffini endings of the rat incisor following injury to the inferior alveolar nerve. Brain Res 787:41-48.
112. Zuniga JR. 1999. Trigeminal ganglion cell response to mental nerve transection and repair in the rat. J Oral Maxillofac Surg 57:427-437.