The sensory innervation of junctional and oral sulcular epithelium was investigated by use of anterograde transport of wheat-germ agglutinin-horseradish peroxidase from the trigeminal ganglion. By light microscopy, labeled intra-epithelial nerve fibers were observed forming a dense plexus in the apical two-thirds of the junctional epithelium, with some fibers located near the enamel space. Occasional fibers extended coronally to the sulcus bottom. By electron microscopy, labeled intra-epithelial axon terminals or varicosities were demonstrated to be in close contact with both junctional epithelial cells and neutrophils. These varicosities, which were occasionally surrounded by the cytoplasmic processes of epithelial cells or neutrophils, frequently contained large granular and small clear vesicles. In contrast to the junctional epithelium, the oral sulcular epithelium was sparsely innervated, except for the transition region between the oral sulcular epithelium and the junctional epithelium, where a dense innervation by labeled intraepithelial fibers was found. These fibers extended as far as the stratum spinosum. Electron microscopy revealed mitochondria-filled profiles of varicosities between epithelial cells. This study shows differences in the distribution and ultrastructure of sensory nerves between the junctional and oral sulcular epithelia, and further provides morphological evidence that sensory nerves in the junctional epithelium come into contact not only with epithelial cells but also with neutrophils.
Get full access to this article
View all access options for this article.
References
1.
Adams, J.C. (1981): Heavy Metal Intensification of DAB-based HRP Reaction Product, J Histochem Cytochem29:775.
2.
Aldskogius, H.; Kinnman, E.; and Persson, J. (1986): Labeling of Cutaneous Sensory Nerve Endings with Axonally Transported Horseradish Peroxidase and Wheat Germ Agglutinin-Horseradish Peroxidase Conjugate: A Methodological Study in the Rat, J Neurosci Meth15 :281-294.
3.
Andres, K.H.; Von During, M.; Muszynski, K.; and Schmidt, R.F. (1987): Nerve Fibres and their Terminals of the Dura Mater Encephali of the Rat, Anat Embryol175:289-301.
4.
Ayasaka, N. and Tanaka, T. (1989): A Cytochemical Study of Horseradish Peroxidase Uptake in Rat Junctional Epithelium, J Dent Res68:1503-1507.
5.
Bar-Shavit, Z.; Goldman, R.; Stabinsky, Y.; Gottlieb, P.; Fridkin, M.; Teichberg, V.I.; and Blumberg, S. (1980): Enhancement of Phagocytosis-A Newly Found Activity of Substance P Residing in its N-Terminal Tetrapeptide Sequence, Biochem Biophys Res Commun94:1445-1451.
6.
Byers, M.R. and Holland, G.R. (1977): Trigeminal Nerve Endings in Gingiva, Junctional Epithelium and Periodontal Ligament of Rat Molars as Demonstrated by Autoradiography , Anat Rec188:509-524.
7.
Byers, M.R.; Mecifi, K.B.; and Kimberly, C.L. (1987): Numerous Nerves with Calcitonin Gene-related Peptide-Like Immunoreactivity Innervate Junctional Epithelium of Rats, Brain Res419:311-314.
8.
Cauna, N. (1973): The Free Penicillate Nerve Endings of the Human Hairy Skin, J Anat115:277-288.
9.
Chan, K.Y. and Byers, M.R. (1985a): Sensory Nerve Endings of the Incisive Papilla of Rat Hard Palate Studied by Peroxidase Cytochemical Methods, J Comp Neurol234:192-200.
10.
Chan, K.Y. and Byers, M.R. (1985b): Anterograde Axonal Transport and Intercellular Transfer of WGA-HRP in Trigeminal-innervated Sensory Receptors of Rat Incisive Papilla, J Comp Neurol234:201-217.
11.
Gulbenkian, S.; Merighi, A.; Wharton, J.; Varndell, I.M.; and Polak, J.M. (1986): Ultrastructural Evidence for the Coexistence of Calcitonin Gene-related Peptide and Substance P in Secretory Vesicles of Peripheral Nerves in the Guinea Pig, J Neurocytol15:535-542.
12.
Holland, G.R. (1984): Innervation of Oral Mucosa and Sensory Perception . In: The Structure and Function of Oral Mucosa, J. Meyer, C.A. Squier , and S.J. Gerson, Eds., Oxford: Pergamon Press, pp. 195-217.
13.
Holzer, P. (1988): Local Effector Functions of Capsaicin-sensitive Sensory Nerve Endings: Involvement of Tachykinins, Calcitonin Gene-related Peptide and Other Neuropeptides, Neuroscience24:739-768.
14.
Kimberly, C.L. and Byers, M.R. (1988): Inflammation of Rat Molar Pulp and Periodontium Causes Increased Calcitonin Gene-related Peptide and Axonal Sprouting, Anat Rec222:289-300.
15.
Lange, D. and Schroeder, H.E. (1971): Cytochemistry and Ultrastructure of Gingival Sulcus Cells, Helv Odontol Acta15:65-86.
16.
Levine, J.D.; Lau, W.; Kwiat, G.; and Goetzl, E.J. (1984): Leukotriene B4 Produces Hyperalgesia that is Dependent on Polymorphonuclear Leukocytes, Science225:743-745.
17.
Levine, J.D.; Gooding, J.; Donatoni, P.; Borden, L.; and Goetzl, E.J. (1985): The Role of the Polymorphonuclear Leukocyte in Hyperalgesia, J Neurosci5:3025-3029.
18.
Luzardo-Baptista, M. (1973): Intraepithelial Nerve Fibers in the Human Oral Mucosa. An Electron Microscopic Study, Oral Surg Oral Med Oral Pathol35:372-376.
19.
Lynn, B. and Hunt, S.P. (1984): Afferent C-Fibres: Physiological and Biochemical Correlations, Trends Neurosci7:186-188.
20.
Maeda, T. ; Iwanaga, T. ; Fujita, T. ; Takahashi, Y.; and Kobayashi, S.( 1987): Distribution of Nerve Fibers Immunoreactive to Neurofilament Protein in Rat Molars and Periodontium, Cell Tissue Res249:13-23.
21.
Marfurt, C.F. and Turner, D.F. (1983): Sensory Nerve Endings in the Rat Oro-Facial Region Labeled by the Anterograde and Transganglionic Transport of Horseradish Peroxidase: A New Method for Tracing Peripheral Nerve Fibers, Brain Res261:1-12.
22.
Mesulam, M.-M. (1978): Tetramethyl Benzidine for Horseradish Peroxidase Neurohistochemistry: ANon-carcinogenic Blue Reaction-Product with Superior Sensitivity for Visualizing Neural Afferents and Efferents, J Histochem Cytochem26:106-117.
23.
Munger, B.L. (1965): The Intraepidermal Innervation of the Snout Skin of the Opossum. A Light and Electron Microscope Study, with Observations on the Nature of Merkel's Tastzellen, J Cell Biol26:79-97.
24.
Murray, R.G. and Murray, A. (1967): Fine Structure of Taste Buds of Rabbit Foliate Papillae, J Ultrastruct Res19:327-353.
25.
Olucha, F.; Martinez-Garcia, F.; and Lopez-Garcia, C. (1985): A New Stabilizing Agent for the Tetramethyl Benzidine (TMB) Reaction Product in the Histochemical Detection of Horseradish Peroxidase (HRP), J Neurosci Meth13:131-138.
26.
Robertson, B. and Aldskogius, H. (1982): The Use of Anterogradely Transported Wheat Germ Agglutinin-Horseradish Peroxidase Conjugate to Visualize Cutaneous Sensory Nerve Endings, Brain Res240:327-330.
27.
Robertson, B. and Arvidsson, J. (1985): Transganglionic Transport of Wheat Germ Agglutinin-HRP and Choleragenoid-HRP in Rat Trigeminal Primary Sensory Neurons, Brain Res348:44-51.
28.
Romanowski, A.W.; Squier, C.A.; and Lesch, C.A. (1988): Permeability of Rodent Junctional Epithelium to Exogenous Protein, J Periodont Res23:81-86.
29.
Salt, T.E. and Hill, R.G. (1983): Neurotransmitter Candidates of Somatosensory Primary Afferent Fibres, Neuroscience10:1083-1103.
30.
Schroeder, H.E. (1986): Gingiva. In: Handbook of Microscopic Anatomy, Vol. 5, The Periodontium, A. Oksche and L. Vollrath, Eds., Berlin: Springer-Verlag, pp. 233-323.
31.
Tanaka, T. (1984): Transport Pathway and Uptake of Micro peroxidase in the Junctional Epithelium of Healthy Rat Gingiva, J Periodont Res19:26-39.
32.
Turner, D.F. (1983): The Morphology and Distribution of Merkel Cells in Primate Gingival Mucosa, Anat Rec205:197-205.
33.
Van Dyke, T.E.; Levine, M.J.; and Genco, R.J. (1985): Neutrophil Function and Oral Disease, J Oral Pathol14:95-120.
34.
Yeh, Y. and Byers, M.R. (1983): Fine Structure and Axonal Transport Labeling of Intraepithelial Sensory Nerve Endings in Anterior Hard Palate of the Rat, Somatosens Res1:1-19.
35.
Zahm, D.S. and Munger, B.L. (1985): The Innervation of the Primate Fungiform Papilla. Development, Distribution and Changes Following Selective Ablation, Brain Res Rev9:147-186.
