Different localizations of growth-associated protein (GAP-43) in mechanoreceptors and free nerve endings of adult rat periodontal ligament, dental pulp and skin

Archives of Histology and Cytology

Volumn 59, Issue 3, 1996, Pages 291-304

  Maeda, Takeyasu ^a,b   Byers, Margaret R ^b  

^a NIIGATA UNIVERSITY   (Japan)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH ASSOCIATED PROTEIN; NERVE GROWTH FACTOR RECEPTOR;

ADOLESCENT; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; MECHANORECEPTOR; MICROSCOPY; NERVE ENDING; NONHUMAN; PERIODONTAL LIGAMENT; PROTEIN EXPRESSION; RAT; SCHWANN CELL; SKIN; TISSUE DISTRIBUTION; TOOTH PULP;

EID: 0029762083     PISSN: 09149465     EISSN: None     Source Type: Journal    
DOI: 10.1679/aohc.59.291     Document Type: Article

References (65)

1. ANDRES, K. H. and M. VON DURING: Morphology of cutaneous receptors. In: (ed. by) A. IGGO: Handbook of sensory physiology. Vol. II. Somatosensory system. Springer, Berlin-Heiderberg-New York, 1973 (p. 3-28).
2. BEERTSEN, W., V. EVERTS and A. VAN DEN HOOF: Fine structure and possible function of cells containing leptomeric organelles in the periodontal ligament of the rat incisor. Arch. Oral Biol. 1099-1100 (1974).
3. BENOWITZ, L. I. and A. ROUTTENBERG: A membrane phosphoprotein associated with neural development, axonal regeneration, phospholipid metabolism, and synaptic plasticity. Trends Neurosci. 10: 527-532 (1987).
4. BENOWITZ, L. I., P. J. APOSTOLIDES, N. PERRONE-BIZZOZERO, S. P. FINKLESTEIN and H. ZWIERS: Anatomical distribution of the growth-associated protein GAP-43/B-50 in the adult rat brain. J. Neurosci. 8: 339-352 (1988).
5. BENOWITZ, L. I., N. I. PERRONNE, F. E. FINKLESTEIN and E. D. BIRD: Localization of the growth-associated phosphoprotein GAP-43 (B-50, F1) in the human cerebral cortex. J. Neurosci. 9: 990-995 (1989).
6. BIEMESDERFER, D., B. MONGER, J. BINCK, J. and R. DUBNER: The pilo-Ruffini complex: A non-sinus hair and associated slowly-adapting mechanoreceptor in primate skin. Brain Res. 142: 197-222 (1978).
7. BYERS, M. R.: Dental sensory receptors. Int. Rev. Neurobiol. 25: 39-94 (1984).
8. _: Sensory innervation of periodontal ligament of rat molars consists of unencapsulated Ruffini-like mechanoreceptors and free nerve endings. J. Comp. Neurol. 231: 500-518 (1985).
9. _: Segregation of NGF receptor in sensory receptors, nerves, and local cells of teeth and periodontium demonstrated by EM immunocytochemistry. J. Neurocytol. 19: 765-777 (1990).
10. BYERS, M. R. and W. K. DONG: 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: 117-217 (1989).
11. BYERS, M. R., M. V. O. NÄRHI and K. B. MECIFI: Acute and chronic reactions of dental sensory nerve fibers in hydrodynamic stimulation or injury. Anat. Rec. 221: 872-883 (1988).
12. CAUNA, N.: The distribution of cholinesterase in the cutaneous receptor organs, especially touch corpuscles of the human finger. J. Histochem. Cytochem. 8: 367-375 (1960).
13. CHAMBERS, M. R., K. H. ANDRES, M. VON DÜRING and A. IGGO: Structure and function of the slowly adapting type II mechanoreceptor in hair skin. Quart. J. Exp. Physiol. 57: 417-445 (1972).
14. CURTIS, R.: Growth-associated protein-43 (GAP-43) is expressed by glial cells of the central and peripheral nervous system. Ann. New York Acad. Sci. 679: 407-411 (1993).
15. CURTIS, R., H. J. S. STEWART, S. M. HALL, G. P. WILKIN, R. MIRSKY and K. R. JESSEN: GAP-43 is expressed by nonmyelin-forming Schwann cells of the peripheral nervous system. J. Cell Biol. 116: 1155-1464 (1992).
16. DE LA MONTE, S. M., H. J. FEDEROFF, S. C. NG, E. GEABCZYK and M. C. FISHMAN: GAP-43 gene expression during development: persistence in a distinctive set of neurons. Devel. Brain Res. 46: 161-168 (1989).
17. FRANK, R. M. and J. NALBANDIAN: Innervation and dentin-pulp sensitivity. In: (ed. by) A OKSCHE and L. VOLLRATH: Handbook of microscopic anatomy. Vol. V/6: Teeth. Springer-Verlag, Berlin-Heiderberg-New York. 1989 (p. 265-286).
18. FRIED, K. and M. RISLING: Growth-associated protein (GAP-43)-like immunoreactivity in primary and permanent tooth pulp nerve fibers of the cat. Brain Res. 572: 19-26 (1992).
19. GOLDING, J. P. and D. A. TONGE: Expression of GAP-43 in normal and regenerating nerves in the frog. Neuroscience 52: 415-426 (1992).
20. GORDEN-WEEKS, P. R.: The cytoskeleton of isolated, neuronal growth cones. Neuroscience 13: 119-136 (1989).
21. GREENBERG, M. M., C. LEITAO, J. TROGADIS and J. K. STEVENS: Irregular geometries in normal unmyelinated axons: a 30 serial EM analysis. J. Neurocytol. 19: 978-988 (1990).
22. HALL, S. M., A. P. KENT, R. CURTIS and D. ROBERTSON: Electron microscopic immunocytochemistry of GAP-43 within proximal and chronically denervated distal stumps of transected peripheral nerve. J. Neurocytol. 21: 820-831 (1992).
23. HEYERAAS, K. J., I. KVINNSLAND, M. R. BYERS and E. B. JACOBSEN: Nerve fibers immunoreactive to protein gene product 9.5, calcitonin gene-related peptide, substance P, and neuropeptide Y in the dental pulp, peri odontal ligament, and gingiva in cats. Acta Odontol. Scand. 51: 207-221 (1993).
24. IDE, C.: Histochemical study of lamellar cell development of Meissner corpuscles. Arch. Histol. Jap. 45: 83-97 (1982).
25. IDE, C. and T. SAITO: Electron microscopic cytochemistry of cholinesterase activity of mouse digital corpuscle. Acta Histochem. Cytochem. 13: 218-226 (1980a).
26. _: Electron microscopic histochemistry of cholinesterase activity of Vater-Pacini corpuscles. Acta Histochem. Cytochem. 13: 298-305 (1980b).
27. IWANAGA, T., T. FUJITA, Y. TAKAHASHI and T. NAKAJIMA: Meissner's and Pacinian corpuscles as studied by immunohistochemistry for S-100 protein, neuron-specific enolase and neurofilament protein. Neurosci. Lett. 31: 117-121 (1982).
28. JACOBSON, R. D., I. VIRAG and H. P. SKENE: A protein associated with axon growth, GAP-43, is widely distributed and developmentally regulated in rat CNS. J. Neurosci. 6: 1843-1855 (1986).
29. KANNARI, K., O. SATO, T. MAEDA, T. IWANAGA and T. FUJITA: A possible mechanism of mechanoreception in Ruffini endings in the periodontal ligament of hamster incisors. J. Comp. Neurol. 313: 368-376 (1991).
30. KHAYAT, B. G., M. R. BYERS, P. E. TAYLOR, K. B. MECIFI and C. L. KIMBERLY: Responses of nerve fibers to pulpal inflammation and periapical lesions in rat molars demonstrated by CGRP immunocytochemistry. J. Endodont. 14: 577-587 (1988).
31. KIMBERLY, C. L. and M. R. BYERS: Inflammation of rat molar pulp and periodontium causes increased calcitonin gene-related peptide and axonal sprouting. Anat. Rec. 222: 289-300 (1988).
32. KVINNSLAND, I. and K. J. HEYERAAS: Effect of traumatic occlusion on CGRP and SP immunoreactive nerve fiber morphology in rat molar pulp and periodontium. Histochemistry 97: 111-120 (1992).
33. KVINNSLAND, I. and S. KVINNSLAND: Changes of CGRP-immunoreactive nerve fibers during experimental tooth movement in rats. Eur. J. Orthod. 12: 320-329 (1990).
34. KVINNSLAND, I., K. J. HEYERAAS and M. R. BYERS: Effects of dental trauma on pulpal and periodontal nerve morphology. Proc. Finn. Dent. Soc. 88 (Suppl.): 125-132 (1992).
35. MAEDA, T., T. IWANAGA, Y. TAKAHASHI, T. FUJITA and S. KOBAYASHI: Distribution of nerve fibers immunoreactive to neurofilament protein in rat molars and periodontium. Cell Tiss. Res. 249: 13-23 (1987).
36. MAEDA, T., O. SATO, S. KOBAYASHI, T. IWANAGA and T. FUJITA: 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 (1989).
37. MAEDA, T., K. KANNARI, O. SATO, S. KOBAYASHI, T. IWANAGA and T. FUJITA: Cholinesterase activity in terminal Schwann cells associated with Ruffini endings in the periodontal ligament of rat incisors. Anat. Rec. 228: 339-344 (1990).
38. MAEDA, T., O. SATO, T. IWANAGA and Y. TAKANO: Im munocytochemical localization of nerve growth factor receptor (NGFR) in human teeth. Proc. Finn. Dent. Res. 88 (Suppl.): 557-562 (1992).
39. MCINTOSH, H., D. PARKINSON, K. MEIRI, N. DAW and M. WILLARD: A GAP-like protein in cat visual cortex. Visual Neurosci. 2: 583-591 (1989).
40. MEIRI, K. F. and P. R. GORDEN-WEEK: GAP-43 in growth cones is associated with areas of membrane that are tightly bound to substrate and is a component of a membrane skeleton subcellular fraction. J. Neurosci. 10: 256-266 (1990).
41. MUNGER, B. and C. IDE: The structure and function of cutaneous sensoty receptors. Arch. Histol. Cytol. 51: 1-34 (1988).
42. NAKAKURA-OHSHIMA, K., T. MAEDA, H. OHSHIMA, T. NODA and Y. TAKANO: 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 (1995).
43. PLANTINGA, L. C., J. VERHAAGEN, P. M. EDWARDS, E. M. HOL, P. R. BAR and W. H. GISPEN: The expression of B-50/GAP-43 in Schwann cells in upregulated in degenerating peripheral nerve stumps following nerve injury. Brain Res. 602: 69-76 (1993).
44. SAITO, I., K. ISHII, K. HANADA, O. SATO and T. MAEDA: 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 (1991).
45. SAITO, I., K. KANADA and T. MAEDA: Alteration of nerve growth factor-receptor expression in the periodontal ligament of the rat during experimental tooth movement. Arch. Oral Biol. 38: 923-929 (1993).
46. SATO, O.: Responses of pulpal nerves to cavity preparation in rat molars: An immunohistochemical study using neurofilament protein (NFP) antiserum. Arch. Histol. Cytol. 52: 433-446 (1989).
47. SATO, O., T. MAEDA, S. KOBAYASHI, T. IWANAGA, T. FUJITA and Y. TAKAHASHI: Innervation of periodontal ligament and dental pulp in the rat incisor: An immunohistochemical investigation of neurofilament protein and glia-specific S-100 protein. Cell Tiss. Res. 251: 13-21 (1988).
48. SATO, O., T. MAEDA, T. IWANAGA and S. KOBAYASHI: 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 (1989).
49. SATO, O., T. MAEDA, K. KANNARI, T. IWANAGA and T. FUJITA: Immunohistochemical demonstration of nerve growth factor receptor in human teeth. Biomed. Res. 11: 353-358 (1990).
50. SCHROEDER, H. E.: Periodontal ligament: In: (ed. by) A. OKSCHE and L. VOLLRATH: Handbook of microscopic anatomy. Vol. V/5, The periodontium. Springer-Verlag, Berlin-Heiderberg-New York, 1986 (p. 170-233).
51. SHARKEY, K. A., P. J. COGGINS, W. TETZLAFF, H. ZWIERS, M. A. BISBY and J. S. DAVIDSON: Distribution of growth-associated protein, B-50 (GAP-43) in the mammalian enteric nervous system Neuroscience 38: 13-20 (1990).
52. SKENE J. H. P.: Axonal growth-associated proteins. Ann. Rev. Neurosci. 12: 127-156 (1989).
53. SKENE, J. H. P. and I. VILAG: Posttranslational membrane attachment and dynamic fatty acylation of a neuronal growth cone protein, GAP-43. J. Cell Biol. 108: 613-624 (1989).
54. SKENE, J. H. P. and F. M. WILLARD: Changes in the axonally transported proteins during axon regeneration in toad retinal ganglion cells. J. Cell Biol. 89: 96-103 (1981).
55. SODEK, J.: A comparison of the rates of synthesis and turnover of collagen and non-collagen proteins in adult rat periodontal tissues and skin using a microassay. Arch. Oral Biol. 22: 655-665 (1977).
56. SODEYAMA, T., T. MAEDA, Y. TAKANO and K. HARA: Responses of periodontal nerve terminals to experimentaly induced occlusal trauma in rat molars: An immunohistochemical study using PGP 9.5 antibody. J. Periodont. 31: 235-248 (1996).
57. STEWART, H. J. S., T. COWEN, R. CURTIS, G. P. WILKIN, R. MIRSKY and K. R. JESSEN: GAP-43 immunoreactivity is widespread in the autonomic neurons and sensory neurons of the cat. Neuroscience 47: 673-684 (1992).
58. TAYLOR, P. E., M. R. BYERS and P. E. REDD: Sprouting of CGRP nerve fibers in response to dentin injury in rat molars. Brain Res. 461: 371-376 (1988).
59. TETZLAFF, W., H. ZWIERS, K. LEDERIS, L. CASSAR and M. A. BISBY: 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 (1989).
60. VAN LOOKEREN CAMPAGNE, M., A. B. OBSTREICHER, P. M. P. VAN BERGEN, E. HENEGOUWEN and W. H. GISPEN: Ultrastructural immunocytochemical localization of B-50/GAP-43, a protein kinase C substrate, in isolated presynaptic nerve terminals and neuronal growth cones. J. Neurocytol. 18: 479-489 (1989).
61. VERHAAGEN, J., A. B. OBSTREICHER, P. M. EDWARDS, H. VELDMAN, F. G. I. JENNEKENS and W. H. GISPEN: Light and electron microscopical study of phosphoprotein B-50 following denervation and reinnervation of the rat soleus muscle. J. Neurosci. 8: 1759-1766 (1986).
62. VERHAAGEN, J., C. O. M. VAN HOOF, P. M. EDWARDS, P. N. E. DE GRAAN, A. B. OESTREICHER, P. SCHOTMAN, F. G. I. JENNEKENS and W. H. GISPEN: The kinase C substrate protein B-50 and axonal regeneration. Brain Res. Bull. 17: 737-741 (1986).
63. WINKELMANN, R. N.: Nerve endings in normal and pathologic skin. Charles C. Thomas, Springfield, Illinois, 1960 (p. 81-86).
64. WOOLF, C. J., M. L. REYNOLDS, M. S. CHONG, P. EMSON, N. IRWIN and L. I. BENOWITZ: Denervationof the motor endoplate results in the rapid expression by terminal Schwann cells of the growth-associated protein GAP-43. J. Neurosci. 12: 3999-4010 (1992).
65. YAMAURA, Y.: Immunohistochemical investigations on the nerve fibers of the dental pulp after the cavity preparation. Jap. J. Conserv. Dent. 30: 824-838 (1987).