Tracking circadian rhythms of bone mineral deposition in murine calvarial organ cultures

Journal of Bone and Mineral Research

Volumn 28, Issue 8, 2013, Pages 1846-1854

  McElderry, John David P ^a   Zhao, Guisheng ^a   Khmaladze, Alexander ^a   Wilson, Christopher G ^a   Franceschi, Renny T ^a   Morris, Michael D ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

apatite; circadian rhythm; crystallinity; mineralization; ossification; raman spectroscopy

Indexed keywords

LUCIFERASE; MINERAL; PER1 PROTEIN;

ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; BONE MINERALIZATION; CALVARIA; CHEMICAL REACTION KINETICS; CIRCADIAN RHYTHM; CONTROLLED STUDY; EX VIVO STUDY; MOUSE; NEWBORN; NONHUMAN; ORGAN CULTURE; PROTEIN EXPRESSION; RAMAN SPECTROMETRY; TRANSGENE;

EID: 84881263084     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.1924     Document Type: Article

References (47)

1. Kwon I, Choe HK, Son GH, Kim K., Mammalian molecular clocks. Exp Neurobiol. 2011; 20 (1): 18-28.
2. Reppert SM, Weaver DR., Coordination of circadian timing in mammals. Nature. 2002; 418 (6901): 935-41.
3. Balsalobre A, Brown SA, Marcacci L, Tronche F, Kellendonk C, Reichardt HM, Schutz G, Schibler U., Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science. 2000; 289 (5488): 2344-7.
4. Maywood ES, O'Neill JS, Chesham JE, Hastings MH., Minireview: The circadian clockwork of the suprachiasmatic nuclei-analysis of a cellular oscillator that drives endocrine rhythms. Endocrinology. 2007; 148 (12): 5624-34.
5. Schibler U, Sassone-Corsi P., A web of circadian pacemakers. Cell. 2002; 111 (7): 919-22.
6. Mohawk JA, Green CB, Takahashi JS., Central and peripheral circadian clocks in mammals. Annu Rev Neurosci. 2012; 35: 445-62.
7. Lee C, Etchegaray JP, Cagampang FR, Loudon AS, Reppert SM., Posttranslational mechanisms regulate the mammalian circadian clock. Cell. 2001; 107 (7): 855-67.
8. Kume K, Zylka MJ, Sriram S, Shearman LP, Weaver DR, Jin X, Maywood ES, Hastings MH, Reppert SM., mCRY1 and mCRY2 are essential components of the negative limb of the circadian clock feedback loop. Cell. 1999; 98 (2): 193-205.
9. Duong HA, Robles MS, Knutti D, Weitz CJ., A molecular mechanism for circadian clock negative feedback. Science. 2011; 332 (6036): 1436-9.
10. Maronde E, Schilling AF, Seitz S, Schinke T, Schmutz I, van der Horst G, Amling M, Albrecht U., The clock genes Period 2 and Cryptochrome 2 differentially balance bone formation. PLOS One. 2010; 5 (7): e11527.
11. Zvonic S, Ptitsyn AA, Kilroy G, Wu X, Conrad SA, Scott LK, Guilak F, Pelled G, Gazit D, Gimble JM., Circadian oscillation of gene expression in murine calvarial bone. J Bone Miner Res. 2007; 22 (3): 357-65.
12. Gafni Y, Ptitsyn AA, Zilberman Y, Pelled G, Gimble JM, Gazit D., Circadian rhythm of osteocalcin in the maxillomandibular complex. J Dent Res. 2009; 88 (1): 45-50.
13. Fu L, Patel MS, Bradley A, Wagner EF, Karsenty G., The molecular clock mediates leptin-regulated bone formation. Cell. 2005; 122 (5): 803-15.
14. Yamazaki S, Numano R, Abe M, Hida A, Takahashi R, Ueda M, Block GD, Sakaki Y, Menaker M, Tei H., Resetting central and peripheral circadian oscillators in transgenic rats. Science. 2000; 288 (5466): 682-5.
15. Lamia KA, Storch KF, Weitz CJ., Physiological significance of a peripheral tissue circadian clock. Proc Natl Acad Sci U S A. 2008; 105 (39): 15172-7.
16. Storch KF, Paz C, Signorovitch J, Raviola E, Pawlyk B, Li T, Weitz CJ., Intrinsic circadian clock of the mammalian retina: importance for retinal processing of visual information. Cell. 2007; 130 (4): 730-41.
17. Zvonic S, Ptitsyn AA, Conrad SA, Scott LK, Floyd ZE, Kilroy G, Wu X, Goh BC, Mynatt RL, Gimble JM., Characterization of peripheral circadian clocks in adipose tissues. Diabetes. 2006; 55 (4): 962-70.
18. Duffield GE, Best JD, Meurers BH, Bittner A, Loros JJ, Dunlap JC., Circadian programs of transcriptional activation, signaling, and protein turnover revealed by microarray analysis of mammalian cells. Curr Biol. 2002; 12 (7): 551-7.
19. Balsalobre A, Damiola F, Schibler U., A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell. 1998; 93 (6): 929-37.
20. Edery I., A master CLOCK hard at work brings rhythm to the transcriptome. Genes Dev. 2011; 25 (22): 2321-6.
21. Zhang EE, Kay SA., Clocks not winding down: unravelling circadian networks. Nat Rev Mol Cell Biol. 2010; 11 (11): 764-76.
22. Mengatto CM, Mussano F, Honda Y, Colwell CS, Nishimura I., Circadian rhythm and cartilage extracellular matrix genes in osseointegration: a genome-wide screening of implant failure by vitamin D deficiency. PLOS One. 2011; 6 (1): e15848.
23. Hanyu R, Hayata T, Nagao M, Saita Y, Hemmi H, Notomi T, Nakamoto T, Schipani E, Knonenbery H, Kaneko K, Kurosawa H, Ezura Y, Noda M., Per-1 is a specific clock gene regulated by parathyroid hormone (PTH) signaling in osteoblasts and is functional for the transcriptional events induced by PTH. J Cell Biochem. 2011; 112 (2): 433-8.
24. Gundberg CM, Markowitz ME, Mizruchi M, Rosen JF., Osteocalcin in human serum: a circadian rhythm. J Clin Endocrinol Metab. 1985; 60 (4): 736-9.
25. Hunter GK, Hauschka PV, Poole AR, Rosenberg LC, Goldberg HA, Nucleation and inhibition of hydroxyapatite formation by mineralized tissue proteins. Biochem J. 1996; 317 (Pt 1): 59-64.
26. Gorski JP., Biomineralization of bone: a fresh view of the roles of non-collagenous proteins. Front Biosci. 2012; 17: 2598-621.
27. Colfen H, Biomineralization: a crystal-clear view. Nat Mater. 2010; 9: 960-1.
28. Nudelman F, Pieterse K, George A, Bomans PHH, Friedrich H, Brylka LJ, Hilbers PAJ., With Gd, Sommerdijk NAJM. The role of collagen in bone apatite formation in the presence of hydroxyapatite nucleation inhibitors. Nat Mater. 2010; 9: 1004-9.
29. Crane NJ, Popescu V, Morris MD, Steenhuis P, Ignelzi JMA., Raman spectroscopic evidence for octacalcium phosphate and other transient mineral species deposited during intramembranous mineralization. Bone. 2006; 39 (3): 434-42.
30. Weiner S., Transient precursor strategy in mineral formation of bone. Bone. 2006; 39 (3): 431-3.
31. Grynpas MD, Omelon S., Transient precursor strategy or very small biological apatite crystals?. Bone. 2007; 41 (2): 162-4.
32. Wilsbacher LD, Yamazaki S, Herzog ED, Song EJ, Radcliffe LA, Abe M, Block G, Spitznagel E, Menaker M, Takahashi JS., Photic and circadian expression of luciferase in mPeriod1-luc transgenic mice in vivo. Proc Natl Acad Sci U S A. 2002; 99 (1): 489-94.
33. Wang D, Christensen K, Chawla K, Xiao G, Krebsbach PH, Franceschi RT., Isolation and characterization of MC3T3-E1 preosteoblast subclones with distinct in vitro and in vivo differentiation/mineralization potential. J Bone Miner Res. 1999; 14 (6): 893-03.
34. Li Y, Ge C, Franceschi RT., Differentiation-dependent association of phosphorylated extracellular signal-regulated kinase with the chromatin of osteoblast-related genes. J Bone Miner Res. 2010; 25 (1): 154-63.
35. Press WH, Teukolsky SA, Vetterling WT, Flannery BP., Numerical recipes in C. 2nd ed. New York: Cambridge University Press; 1992.
36. McElderry J-DP, Kole MR, Morris MD., Repeated freeze-thawing of bone tissue affects Raman bone quality measurements. J Biomed Optics. 2011; 16 (7): 071407.
37. Relogio A, Westermark PO, Wallach T, Schellenberg K, Kramer A, Herzel H., Tuning the mammalian circadian clock: robust synergy of two loops. PLoS Comput Biol. 2011; 7 (12): e1002309.
38. Lowrey PL, Takahashi JS., Mammalian circadian biology: elucidating genome-wide levels of temporal organization. Annu Rev Genomics Hum Genet. 2004; 5: 407-1.
39. Koike N, Yoo SH, Huang HC, Kumar V, Lee C, Kim TK, Takahashi JS., Transcriptional architecture and chromatin landscape of the core circadian clock in mammals. Science. 2012; 338 (6105): 349-54.
40. Kazanci M, Fratzl P, Klaushofer K, Paschalis EP., Complementary information on in vitro conversion of amorphous (precursor) calcium phosphate to hydroxyapatite from Raman microspectroscopy and wide-angle X-ray scattering. Calcif Tissue Int. 2006; 79 (5): 354-9.
41. Gorski JP., Is all bone the same? Distinctive distributions and properties of non-collagenous matrix proteins in lamellar vs. woven bone imply the existence of different underlying osteogenic mechanisms. Crit Rev Oral Biol Med. 1998; 9 (2): 201-23.
42. Bonucci E., Bone mineralization. Front Biosci. 2012; 17: 100-28.
43. Baig AA, Fox JL, Young RA, Wang Z, Hsu J, Higuchi WI, Chhettry A, Zhuang H, Otsuka M., Relationships among carbonated apatite solubility, crystallite size, and microstrain parameters. Calcif Tissue Int. 1999; 64 (5): 437-49.
44. Camacho NP, Hou L, Toledano TR, Ilg WA, Brayton CF, Raggio CL, Root L, Boskey AL., The material basis for reduced mechanical properties in oim mice bones. J Bone Miner Res. 1999; 14 (2): 264-72.
45. Wojtowicz A, Dziedzic-Goclawska A, Kaminski A, Stachowicz W, Wojtowicz K, Marks SC Jr, Yamauchi M., Alteration of mineral crystallinity and collagen cross-linking of bones in osteopetrotic toothless (tl/tl) rats and their improvement after treatment with colony stimulating factor-1. Bone. 1997; 20 (2): 127-32.
46. Luchavova M, Zikan V, Michalska D, Raska I Jr, Kubena AA, Stepan JJ., The effect of timing of teriparatide treatment on the circadian rhythm of bone turnover in postmenopausal osteoporosis. Eur J Endocrinol. 2011; 164 (4): 643-8.
47. Shao P, Ohtsuka-Isoya M, Shinoda H., Circadian rhythms in serum bone markers and their relation to the effect of etidronate in rats. Chronobiol Int. 2003; 20 (2): 325-36.