Connective Tissue Biology
Full Access
Effect of surgical sympathectomy on bone remodeling at rat incisor and molar root sockets
H. S. Sandhu,
M. S. Herskovits,
I. J. Singh,
H. S. Sandhu
Division of Oral Biology, Faculty of Dentistry, The University of Western Ontario, London, Canada N6A 5C1
Search for more papers by this authorM. S. Herskovits
Department of Anatomy, New York College of Osteopathic Medicine, Old Westbury, NY 11568
Search for more papers by this authorI. J. Singh
Department of Anatomy, New York University Dental Center, New York, NY 10010
Search for more papers by this authorH. S. Sandhu,
M. S. Herskovits,
I. J. Singh,
H. S. Sandhu
Division of Oral Biology, Faculty of Dentistry, The University of Western Ontario, London, Canada N6A 5C1
Search for more papers by this authorM. S. Herskovits
Department of Anatomy, New York College of Osteopathic Medicine, Old Westbury, NY 11568
Search for more papers by this authorI. J. Singh
Department of Anatomy, New York University Dental Center, New York, NY 10010
Search for more papers by this authorAbstract
Sympathectomy was carried out in 4-week-old Sprague-Dawley rats by unilateral surgical removal of the superior cervical ganglion. Sham-treated rats served as controls. All rats were injected with tetracycline hydrochloride at surgery as well as 36 hr prior to sacrifice. Rats were killed at 7, 14, or 21 days following sympathectomy. Mandibular periosteal and endosteal surfaces were analyzed by fluorochrome morphometry. Osteoclasts were identified by acid phosphatase staining, and incisor and molar root sockets were analyzed morphometrically. Following sympathectomy, periosteal and endosteal apposition as well as the rate of mineralization were significantly lower. At the same time, a significant increase in the number of osteoclasts per socket as well as in active and inactive bone resorption surfaces was also seen. All parameters, however, returned to normal values 2–3 weeks after sympathectomy. The data provide the first direct quantitative evidence that sympathetic neurons modulate bone resorption and bone remodeling in vivo.
Literature Cited
- Arsenault, A. L., and F. P. Ottensmeyer (1983) Quantitative spatial distribution of calcium, phosphorous and sulfur in calcifying epiphysis by high resolution electron spectroscopic imaging. Proc. Natl. Acad. Sci. USA, 80: 1322–1326.
- Asher, M. A., and C. B. Sledge (1968) Hyperoxia and in vitro bone resorption. Clin. Orthop., 61: 48–51.
- Basle, M. F., A., Rebel, and J. C. Reinier (1983) Bone tissue in reflex sympathetic dystrophy syndrome–Sudeck's atrophy: Structural and ultrastructural studies. Metab. Bone Dis. Rel. Res., 4: 305–311.
- Baylink, D., M., Stauffer, and J. Wergedal (1970) Formation, mineralization and resorption of bone in vitamin D deficient rats. J. Clin. Invest., 49: 1122–1134.
- Brighton, C. T., and R. B. Heppenstall (1971) Oxygen tension of healing fractures in the rabbit. J. Bone Joint Surg., 54A: 323–332.
- Brighton, C. T., R. D., Ray, L. W. Soble, and K. E. Kuettner (1969) In vitro epiphyseal plate growth in various oxygen tensions. J. Bone Joint Surg., 51A: 1383–1396.
- Brooks, M. (1972) Blood supply of developing bone and its possible bearing on malformations of the limb and face in congenital haemangiomatous disorders. Proc. R. Soc. Med., 65: 597–599.
- Chambers, T. J., P. M. J., McSheehy, B. M. Thomson, and K. Fuller (1985) The effect of calcium-regulating hormones and prostaglandins on bone resorption by osteoclasts disaggregated from neonatal rabbit bones. Endocrinology, 116: 234–239.
- Chiego, D. J., R. M., Klein, J. K. Avery, and I. M. Gruhl (1986) Denervation-induced changes in cell proliferation in the rat molar after wounding. Anat. Rec., 214: 348–352.
- Duncan, C. P., and S. S. Shim (1977) The autonomic nerve supply of bone. J. Bone Joint Surg., 59B: 323–330.
- Evans, R. A., C. R., Dunsten, and D. J. Baylink (1979) Histochemical identifications of osteoclasts in undecalcified sections of human bone. Miner. Electrolyte Metab., 2: 179–185.
- Fell, W. A. (1949) The effect of sympathectomy on the size of Haversian canals of the cat. J. Anat., 83: 67–68.
- Frost, H. M. (1973a) Bone Remodeling and Its Relation to Metabolic Bone Disease. Charles C. Thomas, Springfield, IL.
- Frost, H. M. (1973b) The origin and nature of transients in human bone remodeling dynamics. In: Clinical Aspects of Metabolic Bone Disease. B. Frame, A. M. Parfitt, and H. Duncan, eds. Excerpta Medica, New York.
- Frost, H. M. (1983) Bone histomorphometry: Choice of marking agent and labeling schedule. In: Bone Histomorphometry: Techniques and Interpretation. R. R. Recker, ed. CRC Press, Boca Raton FL, pp. 37–52.
- Goldhaber, P. (1966) Remodelling of bone in tissue culture. J. Dent. Res., 45: 490–499.
- Gray, D. H., and D. L. Hamblen (1976) The effects of hyperoxia upon bone in organ culture. Clin. Orthop., 119: 225–230.
- Gray, D. H., J. M., Katz, and K. S. Speak (1978) The effects of varying oxygen tension upon bone resorption in vitro. J. Bone Joint Surg. 60B: 575–578.
- Gray, D. H., J. M., Katz, and K. S. Speak (1980) The effect of varying oxygen tension on hydroxyproline synthesis in mouse calvaria in vitro. Clin. Orthop., 146: 276–281.
- Herskovits, M. S., and I. J. Singh (1984) Effect of guanethidine-induced sympathectomy on osteoblastic activity in the rat femur evaluated by 3H-proline autoradiography. Acta Anat., 120: 151–155.
- Herskovits, M. S., and I. J. Singh (1986) Autoradiography of 3H-proline uptake by fibroblasts of the periodontal ligament and odontoblasts of the rat incisor after guanethidine-induced sympathectomy. Arch. Oral Biol., 31: 415–417.
- Hohmann, E. L., and A. H. Tashjian, Jr. (1984) Functional receptors for vasoactive intestinal peptide on human osteosarcoma cells. Endocrinology 114: 1321–1327.
- Hohmann, E. L., L. Levine, and A. H. Tashjian, Jr. (1983) Vasoactive intestinal peptide stimulates bone resorption via a cyclic adenosine 3′, 5′ monophosphate-dependant mechanism. Endocrinology, 112: 1233–1239.
- Hohmann, E. L., R. P., Elde, J. A. Rysavy, S. Einzig, and R. L. Gebhard (1986) Innervation of periosteum and bone by sympathetic vasoactive peptides containing nerve fibres. Science, 232: 868–871.
- Holtrop, M. E., and L. G. Raisz (1979) Comparison of the effects of 1,25(OH)2D3, prostaglandin E2 and osteoclast-activating factor with parathyroid hormone on the ultrastucture of osteoclasts in cultured long bones of fetal rats. Calcif. Tissue Int., 29: 201–205.
- Holtrop, M. E., G. J., King, K. A. Cox, and B. Reit (1979) Time-related changes in the ultrastructure of osteoclasts after injection of parathyroid hormone in young rats. Calcif. Tissue Int., 27: 129–135.
- Horton, J. E., J. J., Oppenheim, S. E. Mergenhagen, and L. G. Raisz (1974) Macrophage-lymphocyte energy in the production of osteoclasts activity factor. J. Immunol., 113: 1278–1287.
- Jaworski, Z. F. G., B., Duck, and G. Sekaly (1981) Kinetics of osteoclasts and their nuclei in evolving secondary Haversian system. J. Anat., 133: 397–405.
- Klein, D. C., and L. G. Raisz (1970) Prostaglandins: Stimulation of bone resorption in tissue culture. Endocrinology, 86: 1436–1440.
- Klein, R. M., D. J., Chiego, and J. K. Avery (1981) Effects of guanethidine-induced sympathectomy on cell proliferation in the progenitive compartments of neonatal mouse incisor. Arch. Oral Biol., 26: 319–325.
- Liu, C. C., and D. J. Baylink (1984) Differential response in alveolar bone osteoclasts residing at two different bone sites. Calcif. Tissue Int., 36: 397–405.
- Liu, C. C., J. I., Rader, H. Gruber, and D. J. Baylink (1982) Acute reduction in osteoclast number during bone repletion. Metab. Bone Dis. Relat. Res., 4: 201–209.
- Luben, R. A., G. L., Wong, and C. Cohn (1976) Effects of parahormone and calcitonin on citrate and hyaluranate metabolism in cultured bone. Endocrinology, 98: 413–419.
- Luben, R. A., G. L., Wong, and C. Cohn (1977) Parathormone-stimulated resorption of devitalized bone by cultured osteoclast-type bone cells. Nature, 265: 629–630.
- Melcher, A. H., and G. M. Hodge (1968) In vitro culture of an organ containing mixed epithelial and connective tissues on a chemically defined medium. Nature, 219: 301–302.
- Mescher, A. L., and S. E. Munaim (1986) Changes in the extracellular matrix and glycosaminoglycan synthesis during the initiation of regeneration in adult newt limb. Anat. Rec., 214: 424–431.
- Miller, M. L., and R. S. McCuskey (1973) Innervation of bone marrow in the rabbit. Scand. J. Haematol., 10: 17–23.
- Retzlaff, E., F., Mitchell, J. Upledger, J. Vredeveoogd, and J. Walsh (1981) Light and scanning microscopy of nerve fibres within the parietal bones of primates. Anat. Rec., 199: 201A.
- Roberts, W. E. (1975) Cell population dynamics of periodontal ligament stimulated with parathyroid extract. Am. J. Anat., 143: 363–370.
- Saffar, J. L., and R. Baron (1977) A quantitative study of osteoclastic bone resorption during experimental periodontal disease in Golden Hamster. J. Periodont. Res., 12: 387–394.
- Sandhu, H. S., and S. S. Jande (1982) Effects of beta-aminopropionitrile on formation and mineralization of rat bone matrix. Calcif. Tissue Int., 34: 80–85.
- Scheven, B. A., W. M., Elizabeth, E. W. Kawileranag-DeHaas, A. Wessenaar, and P. J. Nijweide (1986) Differentiation kinetics of osteoclasts in the periosteum of embryonic bones in vivo and in vitro. Anat. Rec., 214: 418–423.
- Singh, I. J., R. M., Klein, and M. Herskovits (1981) Autoradiographic assessment of 3H-proline uptake by osteoblasts following guanethidine-induced sympathectomy in the rat. Cell Tissue Res., 216: 215–220.
- Singh, I. J., M. S., Herskovits, D. J. Chiego, Jr., and R. M., Klein (1982) Modulation of osteoblastic activity by sensory and autonomic innervation of bone. In: Factors and Mechanisms Influencing Bone Growth. A. D. Dixon and B. G. Sarnat, eds. Alan R. Liss, New York, pp. 534–551.
- Tashjian, A. H., E. F., Voelkel, P. Goldhaber, and L. Levine (1973) Prostaglandins, bone resorption and hypercalcaemia. Prostaglandins, 3: 515–524.
- Thompson, E. R., D. J., Baylink, and J. E. Wergedal (1975) Increase in number and size of osteoclasts in response to calcium or phosphate deficiency in rat. Endocrinology, 97: 283–289.
- Vignery, A., and R. Baron (1978) Effects of parathyroid hormone on the osteoclastic pool, bone resorption and formation in rat alveolar bone. Calcif. Tissue Res., 26: 23–28.
- Vignery, A., and R. Baron (1980) Dynamic histomorphometry of alveolar bone remodeling in the adult rat. Anat. Rec., 196: 191–200.
- Warshawsky, H., D., Goltzman, M. P. Rouleau, and J. J. M. Bergeron (1980) Direct in vivo demonstration by autoradiography of specific binding sites for calcitonin in skeletal and renal tissues of the rat. J. Cell Biol., 85: 682–694.
- Webber, R. H., J. R., Dedice, J. R. Ferguson, and J. P. Powell (1970) Bone marrow response to stimulation of the sympathetic trunks in rats. Acta Anat., 77: 92–97.
- Westen, H., K. F., Muck, and L. Post (1981) Enzyme histochemistry on bone marrow sections after embedding in methacrylate at low temperature. Histochemistry, 70: 95–105.
