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Rhythmic dentinogenesis in the rabbit incisor: Circadian, ultradian, and infradian periods

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Summary

We have identified a variety of biological rhythms involved in the apposition and mineralization of dentin in the rabbit incisor.

Animals were injected during the day or night with lead acetate at 2-week intervals—to provide biological time markers in forming dentin—and transverse undecalcified sections of the lower incisors were prepared for electron microprobe analysis. The positions of the lead markers were identified, and the continuous distribution of calcium and sulfur was measured at 1 µm intervals between the markers. In thin sections stained with hematoxylin after decalcification, the widths of a series of structural increments (bands) were measured with an ocular micrometer.

Fourier analysis of the data revealed spectra of structural and compositional rhythms with a range of periodicities which extended from a matter of hours [ultradian (<24 h)] to days [infradian (>24 h) and circadian (approximately 24 h)].

The structural and compositional rhythms appeared to be independent to the extent that they did not necessarily have the same periods, or amplitudes. Nor were there simple phase relationships between all of the rhythms. At some times, Ca and S fluctuations are inversely proportional (180° out of phase), but in other cases they are directly proportional or out of phase by varying degrees other than 180°. The analyses thus suggest that calcium and sulfur deposition (representing mineral and glycosaminoglycan deposition, respectively) are not simply inversely proportional, and that the hematoxylin-stained structural increments did not solely reflect differences in the distribution of the mineral components in dentin.

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References

  1. Okada, M.: Studies in the periodic pattern of hard tissues in animal body, pp. 26–31. Shanghai Evening Post, Medical Edition of September, 1943

  2. Okada, M., Mimura, T.: Zur physiologie und pharmakologie der hartgewebe. I. Eine vitalfarbungsmethode mit bleisalzen und ihre anwendung bei den untersuchunger uber die rhythmische streifenbildung der harten zahngewebe. Proc. Jap. Pharm. Soc. 12th Mtg., Jpn. J. Med. Sci. IV. Pharmacology,11:167–170, 1938

    Google Scholar 

  3. Okada, M. Mimura, T.: Zur physiologie und pharmakologie der hartgewebe III. Uber die genese der rhythmischen streifenbildung der harten zahngewebe. Proc. Jap. Pharm. Soc. 14th Mtg., Jpn. J. Med. Sci. IV. Pharmacology,13:92–95, 1940

    Google Scholar 

  4. Okada, M., Mimura, T.: Zur physiologie und pharmakologie der hartegewebe. VII. Uber den zeitlichen verlauf der schwangerschaft und entbindung geseher von der streifenfigur im dentin des mutterlisches kaninchens. Proc. Jap. Pharm. Soc. 15th Mtg., Jpn. J. Med. Sci. IV. Pharmacology,14:7–10, 1941

    Google Scholar 

  5. Okada, M., Mimura, T.: Zur physiologie und pharmakologie der hartgeweve. VIII. Uber den zeitlichen verlauf der mobilisierung des subkutanen bleidepots. Proc. Jap. Pharm. Soc. 16 Mtg., Jpn. J. Med. Sci. IV. Pharmacology,15:9–11, 1942

    Google Scholar 

  6. Okada, M., Mimura, T., Fuse, S.: Zur physiologie und pharmakologie der hartegewebe. VI. Eine methode der pharmakologischen untersuchung durch die anwendung von streifenfiguren in kaninchendentin. Proc. Jap. Pharmacol. Soc. 14th Mtg., Jpn. J. Med. Sci. IV. Pharmacology,13:99–101, 1940

    Google Scholar 

  7. Okada, M., Mimura, T., Ishida, T., Matsumoto, S.: Comparison of tissue deposition of various Ca preparations using rabbit dentin as an indicator, Proc. Jpn. Acad.35:42–46, 1939

    Google Scholar 

  8. Okada, M., Mimura, T., Ishida, T., Matsumoto, S.: The hematoxylin stainability of decalcified dentin and the calcification, Proc. Jpn. Acad.35:47–52, 1939

    Google Scholar 

  9. Schour, I., Hoffman, M.M.: Studies in tooth development. II. The rate of apposition of enamel and dentin in man and other mammals, J. Dent. Res.18:161–175, 1939

    Google Scholar 

  10. Schour, I., Hoffman, M.M.: Studies in tooth development. I. The 16 µm calcification rhythm in the enamel and dentin from fish to man, J. Dent. Res.18:91–102, 1939

    Google Scholar 

  11. Hoffman, M.M., Schour, I.: Quantitative studies on the development of the rat molar. I. The growth pattern of the primary and secondary dentin from birth to 500 days of age, Anat. Rec.78:233–252, 1940

    Article  Google Scholar 

  12. Yilmaz, S., Newman, H.N., Poole, D.F.G.: Diurnal periodicity of v. Ebner growth lines in pig dentin, Arch. Oral Biol.22:511–513, 1977

    Article  CAS  PubMed  Google Scholar 

  13. Kraus, B.S., Jordan, E.S.: The Human Dentition Before Birth. Henry Kimpton, London, 1965

    Google Scholar 

  14. Newman, H.N., Poole, D.F.G.: Observations with SEM and TEM on the structure of human surface enamel, Arch. Oral Biol.19:1135–1143, 1974

    Article  CAS  PubMed  Google Scholar 

  15. Simmons, D.J.: Circadian mitotic rhythm in epiphyseal cartilage, Nature202:646–648, 1964

    Google Scholar 

  16. Simmons, D.J.: Daily rhythm in S35 incorporation into epiphyseal cartilage in mice, Experientia24:363–371, 1968

    Article  CAS  PubMed  Google Scholar 

  17. Hansson, L.I., Stenstrom, A., Thorngren, K.G.: Diurnal variation of longitudinal bone growth in the rabbit, Acta Orthop. Scand.45(4):499–507, 1974

    Article  CAS  PubMed  Google Scholar 

  18. Simmons, D.J., Nichols, G.: Diurnal periodicity in the metabolic activity of bone turnover, Am. J. Physiol.210:411–418, 1966

    CAS  PubMed  Google Scholar 

  19. Simmons, D.J., Whiteside, L.A., Whitson, S.W.: Biorhythmic profiles in the rat skeleton, Metab. Bone Dis. Rel. Res.2:49–64, 1979

    Article  Google Scholar 

  20. Rasmussen, H., Bordier, P.: The Physiology and Cellular Basis of Metabolic Bone Disease. Williams & Wilkins, Baltimore, 1974

    Google Scholar 

  21. Schneider, B.J.: Lead acetate as a vital marker for the analysis of bone growth, Am. J. Phys. Anthrop.29(2):197–200, 1968.

    Article  CAS  PubMed  Google Scholar 

  22. Osmansky, C.P., Yaeger, J.A.: Microradiography of rat incisor dentin during the development of the response to injected fluoride, Anat. Rec.148:467–483, 1964

    Article  Google Scholar 

  23. Tappen, N.C., Simmons, D.J.: Correspondence of silver nitrate staining patterns in decalcified bone with the micro-radiographic image, Anat. Rec.182:267–274, 1975

    Article  CAS  PubMed  Google Scholar 

  24. Dolman, J.W.: A method for the extraction of environmental and geophysical information from growth records in invertebrates and stromatolites. In G.D. Rosenberg, S.K. Runcorn (eds.): Growth Rhythms and The History of the Earth's Rotation, pp. 191–222. John Wiley & Son, London, 1975

    Google Scholar 

  25. Rosenberg, G.D., Jones, C.B.: Approaches to chemical periodicities in molluscs and stromatolites. In G.D. Rosenberg, S.K. Runcorn, (eds.): Growth Rhythms and the History of the Earth's Rotation, pp. 223–242. John Wiley, London, 1975

    Google Scholar 

  26. Shimshoni, M.: On Fisher's test of significance in harmonic analysis, Geophys. J.R. Astr. Soc.23:373–377, 1971

    Google Scholar 

  27. Rosenberg, G.D., Ashton, M., Hewitt, R., Simmons, D.: Growth rhythms: evaluation by a significance test in harmonic analysis. In: Skeletal growth. D. Rhoads and R. Lutz, eds. Plenum (In Press)

  28. Rosenberg, G.D., Simmons, D.J.: Rhythmic dentinogenesis in the rabbit incisor. 2. Allometric aspects. Calcif. Tissue Int. (this volume)

  29. Jowsey, J.: Metabolic Diseases of Bone. W.B. Saunders Co., Philadelphia, 1977

    Google Scholar 

  30. Kumazai, A., Sakai, T.: Effect of Pb acetate on serum Ca and P in rats, Arch. Int. Pharmacodyn. Ther.160:248–252, 1966

    Google Scholar 

  31. Kato, Y., Takimoto, S., Ogura, H.: Mechanisms of induction of hypercalcemia and hyperphosphatemia by Pb acetate in rat, Calcif. Tissue Res.24:41–46, 1977

    Article  CAS  PubMed  Google Scholar 

  32. Rosenberg, G.D., Simmons, D.J., Halberg, F., Nelson, W., Burstein, A.: Skeletal effects of methylprednisolone sodium succinate administration on an every day or alternate day chronopharmacologic dose schedule, Chronobiologia (in press)

  33. Lucas, H.F., Jr., Stanford, J.E.: Excretion and retention of Pb-210 in rats. Ann. Rpt. Radiol. Phys. Div., Argonne Natl. Lab. ANL 7360: 105–110, July 1966–June 1967

  34. Wergedal, J.E., Baylink, D.J.: Electron microprobe measurements of bone mineralization rate in vivo, Am. J. Physiol.226(2):345–352, 1974

    CAS  PubMed  Google Scholar 

  35. de Bernard, B., Stagni, N., Colautti, I., Vittur, F., Bonucci, E.: Glycosaminoglycans and endochondral calcification, Clin. Orthop.126:285–291, 1977

    PubMed  Google Scholar 

  36. Nicholson, W.A.P., Ashton, B.A., Hohling, H.J., Quint, P., Schrieber, J., Ashton, I.K., Boyde, A.: Electron microprobe investigation into the process of hard tissue formation, Cell Tissue Res.177:331–345, 1977

    Article  CAS  PubMed  Google Scholar 

  37. Johnson, A.R.: Sr, Ca, Mg and P content of rat incisors as determined by electron microprobe analysis, J. Dent. Res.51:115–121, 1972

    CAS  PubMed  Google Scholar 

  38. Weatherell, J.A., Robinson, C.: The inorganic composition of teeth. In I. Zipkin (ed.): Biological Mineralization, pp. 43–74. John Wiley, New York, 1973

    Google Scholar 

  39. Weatherell, J.A., Robinson, C., Hallsworth, A.S.: Variation in the chemical composition of human enamel, J. Dent. Res.53:180–192, 1974

    CAS  PubMed  Google Scholar 

  40. Dirlich, G., Zulley, J., Schulz, H.: The temporal pattern of the REM sleep rhythm, pp. 483–493. Proc. XII Internat. Conf. Chronobiol., Milan, II Ponte, 1977

  41. Globus, G.G., Phoebus, E.C., Humphries, J., Boyd, R., Sharp, R.: Ultradian rhythms in human telemetered gross motor activity, Aerospace Med.44:882–887, 1973

    CAS  PubMed  Google Scholar 

  42. Weitzman, E.D.: Temporal patterns of neuro-endocrine secretion in man: Relationship to the 24-hour sleep waking cycle. In F. Halberg (ed.): Chronobiological Aspects of Endocrinology, pp. 169–184. F.K. Schauttauer, New York, 1974

    Google Scholar 

  43. Takahashi, Y., Kipnis, D.M., Daughaday, W.H.: Growth hormone secretion during sleep, J. Clin. Invest.47:2079–2090, 1968

    CAS  PubMed  Google Scholar 

  44. Yen, S.S.C., Vandenberg, G., Tsai, C.C., Parker, D.C.: Ultradian fluctuations of gonadotropins. In M. Ferin, F. Halberg, R.M. Richart, R.L.V. Wiele (eds.): Biorhythms and Human Reproduction, pp. 203–218. John Wiley, New York, 1974

    Google Scholar 

  45. Weeke, J.: Circadian variation of the serum thyrotropin level in normal subjects, Scand. J. Clin. Lab Invest.31:337–342, 1973

    CAS  PubMed  Google Scholar 

  46. O'Connor, J.F., Wu, G.Y., Gallagher, T.F., Hillman, L.: The 24-hour plasma thyroxin profile in normal man, J. Clin. Endocrinol. Metab.39:765–771, 1974

    PubMed  Google Scholar 

  47. Berson, S.A., Yallow, R.A.: Radioimmunoassay of ACTH in plasma, J. Clin. Invest.74:2725–2754, 1968

    Google Scholar 

  48. Gallagher, T.F., Yoshida, K., Roffwerg, H., Fukushima, D.K., Weitzman, E.D., Hellman, L.: ACTH and cortisol secretory pattern in man, J. Clin. Endocrinol. Metab.36:1058–1068, 1973

    CAS  PubMed  Google Scholar 

  49. Rosenfeld, R.S., Hellman, L., Roffwerg, H.D., Weitzman, E.D., Fukushima, D.K., Gallagher, T.F.: Dehydroisoandrosterone is secreted episodically and synchronously with cortisol by normal man, J. Clin. Endocrinol. Metab.33:87–92, 1971

    Article  CAS  PubMed  Google Scholar 

  50. Delbridge, L., Everitt, A.V.: The effect of hypophysectomy and age on the stabilization of labile cross-links in collagen, Exp. Gerontol.7:413–315, 1972

    Article  CAS  PubMed  Google Scholar 

  51. Henneman, D.H.: Effect of estrogen on in vivo and in vitro collagen biosynthesis and maturation in old and young female guinea pigs, Endocrinology83(4):678–690, 1968

    CAS  PubMed  Google Scholar 

  52. Henneman, D.H.: Effect of estradiol-17 on collagen biosynthesis, degradation, and re-utilization in vivo, Biochem. Biophys. Res. Commun.44(2):326–332, 1971

    Article  CAS  PubMed  Google Scholar 

  53. Whitson, S.W.: Estrogen-induced osteoid formation in the osteon of mature female rabbits; an electron microscope study, Anat. Rec.173(4):417–436, 1972

    Article  CAS  PubMed  Google Scholar 

  54. Rudman, D., Freiden, D., Patterson, J.H., Gibbas, D.L.: Diurnal variation in the responsiveness of human subjects to human growth hormone, J. Clin. Invest.52(4):912–918, 1973

    Article  CAS  PubMed  Google Scholar 

  55. Krieger, D., Albin, J., Paget, S., Glick, S.M.: Failure of suppression of nocturnal growth hormone rise by actue corticosteroid administration, Horm. Metab.4(6):463–466, 1972

    Article  CAS  Google Scholar 

  56. Ness, A.R.: The response of the rabbit mandibular incisor to experimental shortening and to the prevention of its eruption, Proc. R. Soc. Biol.146:129–154, 1956

    Article  CAS  Google Scholar 

  57. Schour, I., Medab, H.: The effect of experimental removal of the clinical portion of the upper incisor of the rat upon the rate of eruption and tooth morphology, J. Dent. Res.30:521–530, 1951

    Google Scholar 

  58. Ullman, G.A., Meyer, J., Schneider, B.J.: Experimental studies on the interrelations of condylar growth and alveolar bone formation. III. Response to relief of occlusion in aged rats, Angle Orthodontist39:83–92, 1969

    CAS  PubMed  Google Scholar 

  59. Michaeli, Y., Weinrub, M.W.: Role of attrition and occlusal contact in the physiology of the rat incisor. II. Diurnal rhythm in eruption and attrition, J. Dent. Res.47:486–491, 1968

    CAS  PubMed  Google Scholar 

  60. Horton, B.J., Turley, S.D., West, C.E.: Diurnal variation in the feeding pattern of rabbits, Life Sci.15:1895–1907, 1974

    Article  Google Scholar 

  61. Grewe, M., Felts, W.J.L.: Influence of occlusion on the cellular activity of mouse mandibular incisors, J. Dent. Res.47:65–69, 1968

    Google Scholar 

  62. Mantell, P.A.: The circadian rhythm of mitotic activity in the incisor pulp and the cornea ofRattus norvegicus, Arch. Oral Biol.18:403–407, 1973

    Article  CAS  PubMed  Google Scholar 

  63. Roberts, W.E.: Cell kinetic nature and diurnal periodicity of the rat periodontal ligament, Arch. Oral Biol.20:465–471, 1975

    Article  CAS  PubMed  Google Scholar 

  64. Miani, A., Miani, C.: Circadian advancement rhythm of the calcification front in dog dentin, Panminerva Med.14:127–136, 1972

    CAS  Google Scholar 

  65. Talmage, R.V., Roycroft, J.H., Anderson, J.J.B.: Daily fluctuations in plasma calcium, phosphate, and their radionuclide concentration in the rat, Calcif. Tissue Res.17:91–102, 1975

    CAS  PubMed  Google Scholar 

  66. Phillippens, K.M.H., von Mayersbach, H., Scheving, L.E.: Effects of the scheduling of meal feeding at different phases of the circadian system in rats, J. Nutr.107(2):176–193, 1977

    Google Scholar 

  67. Rosenberg, G.D., Runcorn, S.K. (eds.): Growth Rhythms and the History of the Earth's Rotation. John Wiley, London, 1975

    Google Scholar 

  68. Lutz, R., Rhoads, D.: Anaerobiosis and a theory of growth line formation, Science198:1222–1227, 1977

    PubMed  CAS  Google Scholar 

  69. Schmidt, W.J., Keil, A.: Polarizing Microscopy of Dental Tissues. Pergamon Press, Oxford, 1971

    Google Scholar 

  70. Moss, Melvin L.: Studies on dentin. I. Mantle dentin, Acta Anat. (Basel)87:481–507, 1974

    CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Geology, Indiana University/Purdue University, 46202, Indianapolis, Indiana, USA

    G. D. Rosenberg

  2. Department of Surgery, Division of Orthopedic Surgery, Washington University School of Medicine, 63110, St. Louis, Missouri, USA

    D. J. Simmons

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  1. G. D. Rosenberg
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Rosenberg, G.D., Simmons, D.J. Rhythmic dentinogenesis in the rabbit incisor: Circadian, ultradian, and infradian periods. Calcif Tissue Int 32, 29–44 (1980). https://doi.org/10.1007/BF02408519

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