Circadian Rhythm of Osteocalcin in the Maxillomandibular Complex

Abstract

The human body displays central circadian rhythms of activity. Recent findings suggest that peripheral tissues, such as bone, possess their own circadian clocks. Studies have shown that osteocalcin protein levels oscillate over a 24-hour period, yet the specific skeletal sites involved and its transcriptional profile remain unknown. The current study aimed to test the hypothesis that peripheral circadian mechanisms regulate transcription driven by the osteocalcin promoter. Transgenic mice harboring the human osteocalcin promoter linked to a luciferase reporter gene were used. Mice of both genders and various ages were analyzed non-invasively at sequential times throughout 24-hour periods. Statistical analyses of luminescent signal intensity of osteogenic activity from multiple skeletal sites indicated a periodicity of ~ 24 hrs. The maxillomandibular complex displayed the most robust oscillatory pattern. These findings have implications for dental treatments in orthodontics and maxillofacial surgery, as well as for the mechanisms underlying bone remodeling in the maxillomandibular complex.

Get full access to this article

View all access options for this article.

References

Ando H, Yanagihara H, Hayashi Y, Obi Y, Tsuruoka S, Takamura T, et al. (2005). Rhythmic messenger ribonucleic acid expression of clock genes and adipocytokines in mouse visceral adipose tissue. Endocrinology 146:5631–5636.

Balsalobre A, Damiola F, Schibler U (1998). A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell 93:929–937.

Bollen AM, Martin MD, Leroux BG, Eyre DR (1995). Circadian variation in urinary excretion of bone collagen cross-links. J Bone Miner Res 10:1885–1890.

Caillot-Augusseau A, Lafage-Proust MH, Margaillan P, Vergely N, Faure S, Paillet S, et al. (2000). Weight gain reverses bone turnover and restores circadian variation of bone resorption in anorexic patients. Clin Endocrinol (Oxf) 52:113–121.

Clemens TL, Tang H, Maeda S, Kesterson RA, Demayo F, Pike JW, et al. (1997). Analysis of osteocalcin expression in transgenic mice reveals a species difference in vitamin D regulation of mouse and human osteocalcin genes. J Bone Miner Res 12:1570–1576.

Contag CH, Spilman SD, Contag PR, Oshiro M, Eames B, Dennery P, et al. (1997). Visualizing gene expression in living mammals using a bioluminescent reporter. Photochem Photobiol 66:523–531.

Foster H, Small DJ, Fox JG (1983). The mouse in biomedical research. Vol. III. Normative biology, immunology, and husbandry. Boston: Academic Press, Inc.

Fu L, Patel MS, Bradley A, Wagner EF, Karsenty G (2005). The molecular clock mediates leptin-regulated bone formation. Cell 122: 803–815.

Griffin EA Jr, Staknis D, Weitz CJ (1999). Light-independent role of CRY1 and CRY2 in the mammalian circadian clock. Science 286: 768–771.

10.

Gundberg CM, Markowitz ME, Mizruchi M, Rosen JF (1985). Osteocalcin in human serum: a circadian rhythm. J Clin Endocrinol Metab 60: 736–739.

11.

Heshmati HM, Riggs BL, Burritt MF, McAlister CA, Wollan PC, Khosla S (1998). Effects of the circadian variation in serum cortisol on markers of bone turnover and calcium homeostasis in normal postmenopausal women. J Clin Endocrinol Metab 83:751–756.

12.

Igarashi K, Miyoshi K, Shinoda H, Saeki S, Mitani H (1998). Diurnal variation in tooth movement in response to orthodontic force in rats. Am J Orthod Dentofacial Orthop 114:8–14.

13.

Ilizarov GA, Devyatov AA, Kamerin VK (1980). Plastic reconstruction of longitudinal bone defects by means of compression and subsequent distraction. Acta Chir Plast 22:32–41.

14.

Iris B, Zilberman Y, Zeira E, Galun E, Honigman A, Turgeman G, et al. (2003). Molecular imaging of the skeleton: quantitative real-time bioluminescence monitoring gene expression in bone repair and development. J Bone Miner Res 18:570–578.

15.

Levi F, Schibler U (2007). Circadian rhythms: mechanisms and therapeutic implications. Annu Rev Pharmacol Toxicol 47:593–628.

16.

Lou X, Chen Y, Luo S, Chen G (2000). [Circadian rhythm changes of the levels of endogenous insulin in growing rat condylar cartilage after functional mandibular protrusion]. Hua Xi Kou Qiang Yi Xue Za Zhi 18:252–254 (article in Chinese).

17.

Lowrey PL, Takahashi JS (2004). Mammalian circadian biology: elucidating genome-wide levels of temporal organization. Annu Rev Genomics Hum Genet 5:407–441.

18.

Miyoshi K, Igarashi K, Saeki S, Shinoda H, Mitani H (2001). Tooth movement and changes in periodontal tissue in response to orthodontic force in rats vary depending on the time of day the force is applied. Eur J Orthod 23:329–338.

19.

Panda S, Antoch MP, Miller BH, Su AI, Schook AB, Straume M, et al. (2002). Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109:307–320.

20.

Patel MS, Elefteriou F (2007). The new field of neuroskeletal biology. Calcif Tissue Int 80:337–347; erratum in Calcif Tissue Int 81:247, 2008.

21.

Ptitsyn AA, Zvonic S, Conrad SA, Scott LK, Mynatt RL, Gimble JM (2006). Circadian clocks are resounding in peripheral tissues. PLoS Comput Biol 2:e16.

22.

Shao P, Ohtsuka-Isoya M, Shinoda H (2003). Circadian rhythms in serum bone markers and their relation to the effect of etidronate in rats. Chronobiol Int 20:325–336.

23.

Shearman LP, Sriram S, Weaver DR, Maywood ES, Chaves I, Zheng B, et al. (2000). Interacting molecular loops in the mammalian circadian clock. Science 288:1013–1019.

24.

Simmons DJ, Yang C, Gundberg CM, Kidder L, Cornelissen G, Thomas M, et al. (1990). Calcitonin: chronotherapeutic effect on osteopenia in the ovariectomized rat. Prog Clin Biol Res 341(A):517–527.

25.

Sokoll LJ, Booth SL, Davidson KW, Dallal GE, Sadowski JA (1998). Diurnal variation in total and undercarboxylated osteocalcin: influence of increased dietary phylloquinone. Calcif Tissue Int 62: 447–452.

26.

Srivastava AK, Bhattacharyya S, Li X, Mohan S, Baylink DJ (2001). Circadian and longitudinal variation of serum C-telopeptide, osteocalcin, and skeletal alkaline phosphatase in C3H/HeJ mice. Bone 29:361–367.

27.

Storch KF, Lipan O, Leykin I, Viswanathan N, Davis FC, Wong WH, et al. (2002). Extensive and divergent circadian gene expression in liver and heart. Nature 417:78–83.

28.

Thompson JF, Hayes LS, Lloyd DB (1991). Modulation of firefly luciferase stability and impact on studies of gene regulation. Gene 103:171–177.

29.

Yamada S, Saeki S, Takahashi I, Igarashi K, Shinoda H, Mitani H (2002). Diurnal variation in the response of the mandible to orthopedic force. J Dent Res 81:711–715.

30.

Ye L, Li J, Chen Y, Luo S (2001). [Changes of osteocalcin in serum of young SD rats after functional protrusion]. Hua Xi Kou Qiang Yi Xue Za Zhi 19:322–324 (article in Chinese).

31.

Zheng X, Tian W, Long J (2003). [An experimental study on circadian rhythm of the proliferative index of mandibular osteoblast in goats]. Hua Xi Kou Qiang Yi Xue Za Zhi 21:10–12, 27 (article in Chinese).

32.

Zvonic S, Ptitsyn AA, Conrad SA, Scott LK, Floyd ZE, Kilroy G, et al. (2006). Characterization of peripheral circadian clocks in adipose tissues. Diabetes 55:962–970.

33.

Zvonic S, Ptitsyn AA, Kilroy G, Wu X, Conrad SA, Scott LK, et al. (2007). Circadian oscillation of gene expression in murine calvarial bone. J Bone Miner Res 22:357–365.

34.

Zylka MJ, Shearman LP, Weaver DR, Reppert SM (1998). Three period homologs in mammals: differential light responses in the suprachiasmatic circadian clock and oscillating transcripts outside of brain. Neuron 20:1103–1110.

Supplementary Material

Please find the following supplemental material available below.

For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.

For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.

0.00 MB

0.65 MB