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Journal of Bone and Mineral Metabolism
Published in: Journal of Bone and Mineral Metabolism 3/2012

01-05-2012 | Review Article

A fluorescence spotlight on the clockwork development and metabolism of bone

Authors: Tadahiro Iimura, Ayako Nakane, Mayu Sugiyama, Hiroki Sato, Yuji Makino, Takashi Watanabe, Yuzo Takagi, Rika Numano, Akira Yamaguchi

Published in: Journal of Bone and Mineral Metabolism | Issue 3/2012

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Abstract

Biological phenomena that exhibit periodic activity are often referred as biorhythms or biological clocks. Among these, circadian rhythms, cyclic patterns reflecting a 24-h cycle, are the most obvious in many physiological activities including bone growth and metabolism. In the late 1990s, several clock genes were isolated and their primary structures and functions were identified. The feedback loop model of transcriptional factors was proposed to work as a circadian core oscillator not only in the suprachiasmatic nuclei of the anterior hypothalamus, which is recognized as the mammalian central clock, but also in various peripheral tissues including cartilage and bone. Looking back to embryonic development, the fundamental architecture of skeletal patterning is regulated by ultradian clocks that are defined as biorhythms that cycle more than once every 24 h. As post-genomic approaches, transcriptome analysis by micro-array and bioimaging assays to detect luminescent and fluorescent signals have been exploited to uncover a more comprehensive set of genes and spatio-temporal regulation of the clockwork machinery in animal models. In this review paper, we provide an overview of topics related to these molecular clocks in skeletal biology and medicine, and discuss how fluorescence imaging approaches can contribute to widening our views of this realm of biomedical science.
Literature
1.
2.
3.
Iimura T, Pourquie O (2007) Hox genes in time and space during vertebrate body formation. Dev Growth Differ 49:265–275PubMedCrossRef
4.
Iimura T, Denans N, Pourquie O (2009) Establishment of Hox vertebral identities in the embryonic spine precursors. Curr Top Dev Biol 88:201–234PubMedCrossRef
5.
Jouve C, Iimura T, Pourquie O (2002) Onset of the segmentation clock in the chick embryo: evidence for oscillations in the somite precursors in the primitive streak. Development 129:1107–1117PubMed
6.
Iimura T, Pourquie O (2006) Collinear activation of Hoxb genes during gastrulation is linked to mesoderm cell ingression. Nature 442:568–571PubMedCrossRef
7.
Iimura T, Himeno A, Nakane A, Yamaguchi A (2010) Hox genes, a molecular constraint for the development and evolution of the vertebrate body plan. J Oral Biosci 52:155–163CrossRef
8.
Dequeant ML, Pourquie O (2008) Segmental patterning of the vertebrate embryonic axis. Nat Rev Genet 9:370–382PubMedCrossRef
9.
Yang X, Dormann D, Munsterberg AE, Weijer CJ (2002) Cell movement patterns during gastrulation in the chick are controlled by positive and negative chemotaxis mediated by FGF4 and FGF8. Dev Cell 3:425–437PubMedCrossRef
10.
Iimura T, Yang X, Weijer CJ, Pourquie O (2007) Dual mode of paraxial mesoderm formation during chick gastrulation. Proc Natl Acad Sci USA 104:2744–2749PubMedCrossRef
11.
Freitas C, Rodrigues S, Charrier JB, Teillet MA, Palmeirim I (2001) Evidence for medial/lateral specification and positional information within the presomitic mesoderm. Development 128:5139–5147PubMed
12.
Benazeraf B, Francois P, Baker RE, Denans N, Little CD, Pourquie O (2010) A random cell motility gradient downstream of FGF controls elongation of an amniote embryo. Nature 466:248–252PubMedCrossRef
13.
Palmeirim I, Henrique D, Ish-Horowicz D, Pourquie O (1997) Avian hairy gene expression identifies a molecular clock linked to vertebrate segmentation and somitogenesis. Cell 91:639–648PubMedCrossRef
14.
Niwa Y, Masamizu Y, Liu T, Nakayama R, Deng CX, Kageyama R (2007) The initiation and propagation of Hes7 oscillation are cooperatively regulated by Fgf and notch signaling in the somite segmentation clock. Dev Cell 13:298–304PubMedCrossRef
15.
Dequeant ML, Glynn E, Gaudenz K, Wahl M, Chen J, Mushegian A, Pourquie O (2006) A complex oscillating network of signaling genes underlies the mouse segmentation clock. Science 314:1595–1598PubMedCrossRef
16.
Dale JK et al (2006) Oscillations of the snail genes in the presomitic mesoderm coordinate segmental patterning and morphogenesis in vertebrate somitogenesis. Dev Cell 10:355–366PubMedCrossRef
17.
Aulehla A, Herrmann BG (2004) Segmentation in vertebrates: clock and gradient finally joined. Genes Dev 18:2060–2067PubMedCrossRef
18.
Aulehla A, Wehrle C, Brand-Saberi B, Kemler R, Gossler A, Kanzler B, Herrmann BG (2003) Wnt3a plays a major role in the segmentation clock controlling somitogenesis. Dev Cell 4:395–406PubMedCrossRef
19.
Bessho Y, Hirata H, Masamizu Y, Kageyama R (2003) Periodic repression by the bHLH factor Hes7 is an essential mechanism for the somite segmentation clock. Genes Dev 17:1451–1456PubMedCrossRef
20.
Dale JK, Maroto M, Dequeant ML, Malapert P, McGrew M, Pourquie O (2003) Periodic notch inhibition by lunatic fringe underlies the chick segmentation clock. Nature 421:275–278PubMedCrossRef
21.
Lewis J (2003) Autoinhibition with transcriptional delay: a simple mechanism for the zebrafish somitogenesis oscillator. Curr Biol 13:1398–1408PubMedCrossRef
22.
Aulehla A, Wiegraebe W, Baubet V, Wahl MB, Deng C, Taketo M, Lewandoski M, Pourquie O (2008) A beta-catenin gradient links the clock and wavefront systems in mouse embryo segmentation. Nat Cell Biol 10:186–193PubMedCrossRef
23.
Cornier AS et al (2008) Mutations in the MESP2 gene cause spondylothoracic dysostosis/Jarcho–Levin syndrome. Am J Hum Genet 82:1334–1341PubMedCrossRef
24.
Haraguchi S, Kitajima S, Takagi A, Takeda H, Inoue T, Saga Y (2001) Transcriptional regulation of Mesp1 and Mesp2 genes: differential usage of enhancers during development. Mech Dev 108:59–69PubMedCrossRef
25.
Kitajima S, Takagi A, Inoue T, Saga Y (2000) MesP1 and MesP2 are essential for the development of cardiac mesoderm. Development 127:3215–3226PubMed
26.
Morimoto M, Kiso M, Sasaki N, Saga Y (2006) Cooperative Mesp activity is required for normal somitogenesis along the anterior-posterior axis. Dev Biol 300:687–698PubMedCrossRef
27.
Morimoto M, Sasaki N, Oginuma M, Kiso M, Igarashi K, Aizaki K, Kanno J, Saga Y (2007) The negative regulation of Mesp2 by mouse Ripply2 is required to establish the rostro-caudal patterning within a somite. Development 134:1561–1569PubMedCrossRef
28.
Morimoto M, Takahashi Y, Endo M, Saga Y (2005) The Mesp2 transcription factor establishes segmental borders by suppressing Notch activity. Nature 435:354–359PubMedCrossRef
29.
Nakajima Y, Morimoto M, Takahashi Y, Koseki H, Saga Y (2006) Identification of Epha4 enhancer required for segmental expression and the regulation by Mesp2. Development 133:2517–2525PubMedCrossRef
30.
Nomura-Kitabayashi A, Takahashi Y, Kitajima S, Inoue T, Takeda H, Saga Y (2002) Hypomorphic Mesp allele distinguishes establishment of rostrocaudal polarity and segment border formation in somitogenesis. Development 129:2473–2481PubMed
31.
Oginuma M, Hirata T, Saga Y (2008) Identification of presomitic mesoderm (PSM)-specific Mesp1 enhancer and generation of a PSM-specific Mesp1/Mesp2-null mouse using BAC-based rescue technology. Mech Dev 125:432–440PubMedCrossRef
32.
Oginuma M, Niwa Y, Chapman DL, Saga Y (2008) Mesp2 and Tbx6 cooperatively create periodic patterns coupled with the clock machinery during mouse somitogenesis. Development 135:2555–2562PubMedCrossRef
33.
Oginuma M, Takahashi Y, Kitajima S, Kiso M, Kanno J, Kimura A, Saga Y (2010) The oscillation of Notch activation, but not its boundary, is required for somite border formation and rostral-caudal patterning within a somite. Development 137:1515–1522PubMedCrossRef
34.
Saga Y (1998) Genetic rescue of segmentation defect in MesP2-deficient mice by MesP1 gene replacement. Mech Dev 75:53–66PubMedCrossRef
35.
Saga Y, Hata N, Koseki H, Taketo MM (1997) Mesp2: a novel mouse gene expressed in the presegmented mesoderm and essential for segmentation initiation. Genes Dev 11:1827–1839PubMedCrossRef
36.
Sasaki N, Kiso M, Kitagawa M, Saga Y (2011) The repression of Notch signaling occurs via the destabilization of mastermind-like 1 by Mesp2 and is essential for somitogenesis. Development 138:55–64PubMedCrossRef
37.
Takahashi J, Ohbayashi A, Oginuma M, Saito D, Mochizuki A, Saga Y, Takada S (2011) Analysis of Ripply1/2-deficient mouse embryos reveals a mechanism underlying the rostro-caudal patterning within a somite. Dev Biol 342:134–145CrossRef
38.
Takahashi Y, Hiraoka S, Kitajima S, Inoue T, Kanno J, Saga Y (2005) Differential contributions of Mesp1 and Mesp2 to the epithelialization and rostro-caudal patterning of somites. Development 132:787–796PubMedCrossRef
39.
Takahashi Y, Inoue T, Gossler A, Saga Y (2003) Feedback loops comprising Dll1, Dll3 and Mesp2, and differential involvement of Psen1 are essential for rostrocaudal patterning of somites. Development 130:4259–4268PubMedCrossRef
40.
Takahashi Y, Koizumi K, Takagi A, Kitajima S, Inoue T, Koseki H, Saga Y (2000) Mesp2 initiates somite segmentation through the Notch signalling pathway. Nat Genet 25:390–396PubMedCrossRef
41.
Takahashi Y, Takagi A, Hiraoka S, Koseki H, Kanno J, Rawls A, Saga Y (2007) Transcription factors Mesp2 and Paraxis have critical roles in axial musculoskeletal formation. Dev Dyn 236:1484–1494PubMedCrossRef
42.
Takahashi Y, Yasuhiko Y, Kitajima S, Kanno J, Saga Y (2007) Appropriate suppression of Notch signaling by Mesp factors is essential for stripe pattern formation leading to segment boundary formation. Dev Biol 304:593–603PubMedCrossRef
43.
Yasuhiko Y, Haraguchi S, Kitajima S, Takahashi Y, Kanno J, Saga Y (2006) Tbx6-mediated Notch signaling controls somite-specific Mesp2 expression. Proc Natl Acad Sci USA 103:3651–3656PubMedCrossRef
44.
Yasuhiko Y, Kitajima S, Takahashi Y, Oginuma M, Kagiwada H, Kanno J, Saga Y (2008) Functional importance of evolutionally conserved Tbx6 binding sites in the presomitic mesoderm-specific enhancer of Mesp2. Development 135:3511–3519PubMedCrossRef
45.
Bessho Y, Miyoshi G, Sakata R, Kageyama R (2001) Hes7: a bHLH-type repressor gene regulated by Notch and expressed in the presomitic mesoderm. Genes Cells 6:175–185PubMedCrossRef
46.
Bessho Y, Sakata R, Komatsu S, Shiota K, Yamada S, Kageyama R (2001) Dynamic expression and essential functions of Hes7 in somite segmentation. Genes Dev 15:2642–2647PubMedCrossRef
47.
Hirata H, Bessho Y, Kokubu H, Masamizu Y, Yamada S, Lewis J, Kageyama R (2004) Instability of Hes7 protein is crucial for the somite segmentation clock. Nat Genet 36:750–754PubMedCrossRef
48.
Takashima Y, Ohtsuka T, Gonzalez A, Miyachi H, Kageyama R (2011) Intronic delay is essential for oscillatory expression in the segmentation clock. Proc Natl Acad Sci USA 108:3300–3305PubMedCrossRef
49.
Turnpenny PD et al (2007) Abnormal vertebral segmentation and the notch signaling pathway in man. Dev Dyn 236:1456–1474PubMedCrossRef
50.
Giampietro PF et al (2009) Progress in the understanding of the genetic etiology of vertebral segmentation disorders in humans. Ann N Y Acad Sci 1151:38–67PubMedCrossRef
51.
Dunwoodie SL (2009) The role of Notch in patterning the human vertebral column. Curr Opin Genet Dev 19:329–337PubMedCrossRef
52.
Pascoal S, Carvalho CR, Rodriguez-Leon J, Delfini MC, Duprez D, Thorsteinsdottir S, Palmeirim I (2007) A molecular clock operates during chick autopod proximal-distal outgrowth. J Mol Biol 368:303–309PubMedCrossRef
53.
Shimojo H, Ohtsuka T, Kageyama R (2008) Oscillations in notch signaling regulate maintenance of neural progenitors. Neuron 58:52–64PubMedCrossRef
54.
Hirata H, Yoshiura S, Ohtsuka T, Bessho Y, Harada T, Yoshikawa K, Kageyama R (2002) Oscillatory expression of the bHLH factor Hes1 regulated by a negative feedback loop. Science 298:840–843PubMedCrossRef
55.
Masamizu Y, Ohtsuka T, Takashima Y, Nagahara H, Takenaka Y, Yoshikawa K, Okamura H, Kageyama R (2006) Real-time imaging of the somite segmentation clock: revelation of unstable oscillators in the individual presomitic mesoderm cells. Proc Natl Acad Sci USA 103:1313–1318PubMedCrossRef
56.
Burke AC, Nelson CE, Morgan BA, Tabin C (1995) Hox genes and the evolution of vertebrate axial morphology. Development 121:333–346PubMed
57.
Dolle P, Izpisua-Belmonte JC, Falkenstein H, Renucci A, Duboule D (1989) Coordinate expression of the murine Hox-5 complex homoeobox-containing genes during limb pattern formation. Nature 342:767–772PubMedCrossRef
58.
Gaunt SJ, Sharpe PT, Duboule D (1988) Spatially restricted domains of homeogene transcripts in mouse embryos: relation to a segmented body plan. Development 104:169–179
59.
Graham A, Papalopulu N, Krumlauf R (1989) The murine and Drosophila homeobox gene complexes have common features of organization and expression. Cell 57:367–378PubMedCrossRef
60.
Kmita M, Duboule D (2003) Organizing axes in time and space; 25 years of colinear tinkering. Science 301:331–333PubMedCrossRef
61.
62.
63.
64.
Deschamps J (2004) Developmental biology. Hox genes in the limb: a play in two acts. Science 304:1610–1611PubMedCrossRef
65.
Deschamps J (2007) Ancestral and recently recruited global control of the Hox genes in development. Curr Opin Genet Dev 17:422–427PubMedCrossRef
66.
Deschamps J, van den Akker E, Forlani S, De Graaff W, Oosterveen T, Roelen B, Roelfsema J (1999) Initiation, establishment and maintenance of Hox gene expression patterns in the mouse. Int J Dev Biol 43:635–650PubMed
67.
Deschamps J, van Nes J (2005) Developmental regulation of the Hox genes during axial morphogenesis in the mouse. Development 132:2931–2942PubMedCrossRef
68.
Young T, Deschamps J (2009) Hox, Cdx, and anteroposterior patterning in the mouse embryo. Curr Top Dev Biol 88:235–255PubMedCrossRef
69.
Di-Poi N, Montoya-Burgos JI, Miller H, Pourquie O, Milinkovitch MC, Duboule D (2010) Changes in Hox genes’ structure and function during the evolution of the squamate body plan. Nature 464:99–103PubMedCrossRef
70.
Soshnikova N, Duboule D (2009) Epigenetic temporal control of mouse Hox genes in vivo. Science 324:1320–1323PubMedCrossRef
71.
Tschopp P, Duboule D (2011) A regulatory ‘landscape effect’ over the HoxD cluster. Dev Biol 351:288–296PubMedCrossRef
72.
Young T et al (2009) Cdx and Hox genes differentially regulate posterior axial growth in mammalian embryos. Dev Cell 17:516–526PubMedCrossRef
73.
Iimura T, Pourquie O (2008) Manipulation and electroporation of the avian segmental plate and somites in vitro. Methods Cell Biol 87:257–270PubMedCrossRef
74.
75.
Panda S et al (2002) Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109:307–320PubMedCrossRef
76.
Storch KF, Lipan O, Leykin I, Viswanathan N, Davis FC, Wong WH, Weitz CJ (2002) Extensive and divergent circadian gene expression in liver and heart. Nature 417:78–83PubMedCrossRef
77.
Young ME, Razeghi P, Taegtmeyer H (2001) Clock genes in the heart: characterization and attenuation with hypertrophy. Circ Res 88:1142–1150PubMedCrossRef
78.
Shimba S et al (2005) Brain and muscle Arnt-like protein-1 (BMAL1), a component of the molecular clock, regulates adipogenesis. Proc Natl Acad Sci USA 102:12071–12076PubMedCrossRef
79.
Muhlbauer E, Wolgast S, Finckh U, Peschke D, Peschke E (2004) Indication of circadian oscillations in the rat pancreas. FEBS Lett 564:91–96PubMedCrossRef
80.
Yoo SH et al (2004) PERIOD2:LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc Natl Acad Sci USA 101:5339–5346PubMedCrossRef
81.
Tei H, Okamura H, Shigeyoshi Y, Fukuhara C, Ozawa R, Hirose M, Sakaki Y (1997) Circadian oscillation of a mammalian homologue of the Drosophila period gene. Nature 389:512–516PubMedCrossRef
82.
Sun ZS, Albrecht U, Zhuchenko O, Bailey J, Eichele G, Lee CC (1997) RIGUI, a putative mammalian ortholog of the Drosophila period gene. Cell 90:1003–1011PubMedCrossRef
83.
Albrecht U, Sun ZS, Eichele G, Lee CC (1997) A differential response of two putative mammalian circadian regulators, mper1 and mper2, to light. Cell 91:1055–1064PubMedCrossRef
84.
Shearman LP, Zylka MJ, Weaver DR, Kolakowski LF Jr, Reppert SM (1997) Two period homologs: circadian expression and photic regulation in the suprachiasmatic nuclei. Neuron 19:1261–1269PubMedCrossRef
85.
Yamazaki S et al (2000) Resetting central and peripheral circadian oscillators in transgenic rats. Science 288:682–685PubMedCrossRef
86.
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 20:1103–1110PubMedCrossRef
87.
Ando H, Yanagihara H, Hayashi Y, Obi Y, Tsuruoka S, Takamura T, Kaneko S, Fujimura A (2005) Rhythmic messenger ribonucleic acid expression of clock genes and adipocytokines in mouse visceral adipose tissue. Endocrinology 146:5631–5636PubMedCrossRef
88.
Ptitsyn AA, Zvonic S, Conrad SA, Scott LK, Mynatt RL, Gimble JM (2006) Circadian clocks are resounding in peripheral tissues. PLoS Comput Biol 2:e16PubMedCrossRef
89.
Zvonic S et al (2006) Characterization of peripheral circadian clocks in adipose tissues. Diabetes 55:962–970PubMedCrossRef
90.
Balsalobre A, Damiola F, Schibler U (1998) A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell 93:929–937PubMedCrossRef
91.
Ueda HR, Hayashi S, Chen W, Sano M, Machida M, Shigeyoshi Y, Iino M, Hashimoto S (2005) System-level identification of transcriptional circuits underlying mammalian circadian clocks. Nat Genet 37:187–192PubMedCrossRef
92.
Fu L, Lee CC (2003) The circadian clock: pacemaker and tumour suppressor. Nat Rev Cancer 3:350–361PubMedCrossRef
93.
94.
95.
Honma S, Kawamoto T, Takagi Y, Fujimoto K, Sato F, Noshiro M, Kato Y, Honma K (2002) Dec1 and Dec2 are regulators of the mammalian molecular clock. Nature 419:841–844PubMedCrossRef
96.
Akashi M, Takumi T (2005) The orphan nuclear receptor RORalpha regulates circadian transcription of the mammalian core-clock Bmal1. Nat Struct Mol Biol 12:441–448PubMedCrossRef
97.
Hirota T, Fukada Y (2004) Resetting mechanism of central and peripheral circadian clocks in mammals. Zoolog Sci 21:359–368PubMedCrossRef
98.
Matsuo T, Yamaguchi S, Mitsui S, Emi A, Shimoda F, Okamura H (2003) Control mechanism of the circadian clock for timing of cell division in vivo. Science 302:255–259PubMedCrossRef
99.
Miller BH et al (2007) Circadian and CLOCK-controlled regulation of the mouse transcriptome and cell proliferation. Proc Natl Acad Sci USA 104:3342–3347PubMedCrossRef
100.
Hansson LI, Stenstrom A, Thorngren KG (1974) Diurnal variation of longitudinal bone growth in the rabbit. Acta Orthop Scand 45:499–507PubMedCrossRef
101.
102.
Simmons DJ, Nichols G Jr (1966) Diurnal periodicity in the metabolic activity of bone tissue. Am J Physiol 210:411–418PubMed
103.
Walker KV, Kember NF (1972) Cell kinetics of growth cartilage in the rat tibia I. Measurements in young male rats. Cell Tissue Kinet 5:401–408PubMed
104.
Stutzmann J, Petrovic A (1978) Persistence in organ-culture of a growth-rate circadian-rhythm. Chronobiologia 5:183–184
105.
Simmons DJ (1974) Chronobiology of endochondral ossification. Chronobiologia 1:97–109PubMed
106.
Saeki S (1995) Diurnal Rhythms in the colagen-synthetic activities of cartilage cells and osteoblasts in the rat mandibular condyle. Jpn J Oral Biol 37:70–79CrossRef
107.
Russell JE, Simmons DJ, Huber B, Roos BA (1983) Meal timing as a Zeitgeber for skeletal deoxyribonucleic acid and collagen synthesis rhythms. Endocrinology 113:2035–2042PubMedCrossRef
108.
Nickla DL, Rada JA, Wallman J (1999) Isolated chick sclera shows a circadian rhythm in proteoglycan synthesis perhaps associated with the rhythm in ocular elongation. J Comp Physiol A 185:81–90PubMedCrossRef
109.
Simmons DJ, Arsenis C, Whitson SW, Kahn SE, Boskey AL, Gollub N (1983) Mineralization of rat epiphyseal cartilage: a circadian rhythm. Miner Electrolyte Metab 9:28–37PubMed
110.
Farnum CE, Wilsman NJ (1989) Condensation of hypertrophic chondrocytes at the chondro-osseous junction of growth plate cartilage in Yucatan swine: relationship to long bone growth. Am J Anat 186:346–358PubMedCrossRef
111.
Shen M, Kawamoto T, Yan W, Nakamasu K, Tamagami M, Koyano Y, Noshiro M, Kato Y (1997) Molecular characterization of the novel basic helix-loop-helix protein DEC1 expressed in differentiated human embryo chondrocytes. Biochem Biophys Res Commun 236:294–298PubMedCrossRef
112.
Fujimoto K et al (2001) Molecular cloning and characterization of DEC2, a new member of basic helix-loop-helix proteins. Biochem Biophys Res Commun 280:164–171PubMedCrossRef
113.
Li Y, Song X, Ma Y, Liu J, Yang D, Yan B (2004) DNA binding, but not interaction with Bmal1, is responsible for DEC1-mediated transcription regulation of the circadian gene mPer1. Biochem J 382:895–904PubMedCrossRef
114.
Hamaguchi H et al (2004) Expression of the gene for Dec2, a basic helix-loop-helix transcription factor, is regulated by a molecular clock system. Biochem J 382:43–50PubMedCrossRef
115.
Hinoi E, Ueshima T, Hojo H, Iemata M, Takarada T, Yoneda Y (2006) Up-regulation of per mRNA expression by parathyroid hormone through a protein kinase A-CREB-dependent mechanism in chondrocytes. J Biol Chem 281:23632–23642PubMedCrossRef
116.
Hanyu R et al (2011) 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 112:433–438PubMedCrossRef
117.
Russell JE, Walker WV, Fenster RJ, Simmons DJ (1985) In vitro evaluation of circadian patterns of bone collagen formation. Proc Soc Exp Biol Med 180:375–381PubMed
118.
Russell JE, Grazman B, Simmons DJ (1984) Mineralization in rat metaphyseal bone exhibits a circadian stage dependency. Proc Soc Exp Biol Med 176:342–345PubMed
119.
Muhlbauer RC, Fleisch H (1995) The diurnal rhythm of bone resorption in the rat Effect of feeding habits and pharmacological inhibitors. J Clin Invest 95:1933–1940PubMedCrossRef
120.
Fu L, Patel MS, Bradley A, Wagner EF, Karsenty G (2005) The molecular clock mediates leptin-regulated bone formation. Cell 122:803–815PubMedCrossRef
121.
Akhtar RA et al (2002) Circadian cycling of the mouse liver transcriptome, as revealed by cDNA microarray, is driven by the suprachiasmatic nucleus. Curr Biol 12:540–550PubMedCrossRef
122.
Zvonic S et al (2007) Circadian oscillation of gene expression in murine calvarial bone. J Bone Miner Res 22:357–365PubMedCrossRef
123.
Gafni Y, Ptitsyn AA, Zilberman Y, Pelled G, Gimble JM, Gazit D (2009) Circadian rhythm of osteocalcin in the maxillomandibular complex. J Dent Res 88:45–50PubMedCrossRef
124.
Iris B et al (2003) Molecular imaging of the skeleton: quantitative real-time bioluminescence monitoring gene expression in bone repair and development. J Bone Miner Res 18:570–578PubMedCrossRef
125.
126.
Patel MS, Elefteriou F (2007) The new field of neuroskeletal biology. Calcif Tissue Int 80:337–347PubMedCrossRef
127.
Joseph F, Chan BY, Durham BH, Ahmad AM, Vinjamuri S, Gallagher JA, Vora JP, Fraser WD (2007) The circadian rhythm of osteoprotegerin and its association with parathyroid hormone secretion. J Clin Endocrinol Metab 92:3230–3238PubMedCrossRef
128.
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 20:325–336PubMedCrossRef
129.
Rejnmark L, Lauridsen AL, Vestergaard P, Heickendorff L, Andreasen F, Mosekilde L (2002) Diurnal rhythm of plasma 1, 25-dihydroxyvitamin D and vitamin D-binding protein in postmenopausal women: relationship to plasma parathyroid hormone and calcium and phosphate metabolism. Eur J Endocrinol 146:635–642PubMedCrossRef
130.
Qvist P, Christgau S, Pedersen BJ, Schlemmer A, Christiansen C (2002) Circadian variation in the serum concentration of C-terminal telopeptide of type I collagen (serum CTx): effects of gender, age, menopausal status, posture, daylight, serum cortisol, and fasting. Bone 31:57–61PubMedCrossRef
131.
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 29:361–367PubMedCrossRef
132.
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 83:751–756PubMedCrossRef
133.
Aoshima H, Kushida K, Takahashi M, Ohishi T, Hoshino H, Suzuki M, Inoue T (1998) Circadian variation of urinary type I collagen crosslinked C-telopeptide and free and peptide-bound forms of pyridinium crosslinks. Bone 22:73–78PubMedCrossRef
134.
Bollen AM, Martin MD, Leroux BG, Eyre DR (1995) Circadian variation in urinary excretion of bone collagen cross-links. J Bone Miner Res 10:1885–1890PubMedCrossRef
135.
Nielsen HK, Laurberg P, Brixen K, Mosekilde L (1991) Relations between diurnal variations in serum osteocalcin, cortisol, parathyroid hormone, and ionized calcium in normal individuals. Acta Endocrinol (Copenh) 124:391–398
136.
Gundberg CM, Markowitz ME, Mizruchi M, Rosen JF (1985) Osteocalcin in human serum: a circadian rhythm. J Clin Endocrinol Metab 60:736–739PubMedCrossRef
137.
Luchavova M, Zikan V, Michalska D, Raska I, Kubena A, Stepan JJ (2011) The effect of timing of teriparatide treatment on the circadian rhythm of bone turnover in postmenopausal osteoporosis. Eur J Endocrinol 164:643–648PubMedCrossRef
138.
Iimura T, Sugiyama M, Watanabe T, Nakane A, Makino Y, Yamaguchi A (2011) Lighting up skeletal biology by fluorescent imaging. J Oral Biosci (In press)
139.
Iimura T, Sugiyama M, Makino Y, Nakane A, Watanabe T, Yamaguchi A (2011) Illumination of vertebrate development by fluorescence live imaging. Cytom Res 21:57–63
140.
Hughes AT, Guilding C, Lennox L, Samuels RE, McMahon DG, Piggins HD (2008) Live imaging of altered period1 expression in the suprachiasmatic nuclei of Vipr2−/− mice. J Neurochem 106:1646–1657PubMedCrossRef
141.
Ohta H, Yamazaki S, McMahon DG (2005) Constant light desynchronizes mammalian clock neurons. Nat Neurosci 8:267–269PubMedCrossRef
142.
Numano R et al (2006) Constitutive expression of the Period1 gene impairs behavioral and molecular circadian rhythms. Proc Natl Acad Sci USA 103:3716–3721PubMedCrossRef
143.
Kamioka H, Honjo T, Takano-Yamamoto T (2001) A three-dimensional distribution of osteocyte processes revealed by the combination of confocal laser scanning microscopy and differential interference contrast microscopy. Bone 28:145–149PubMedCrossRef
144.
Sugawara Y, Kamioka H, Honjo T, Tezuka K, Takano-Yamamoto T (2005) Three-dimensional reconstruction of chick calvarial osteocytes and their cell processes using confocal microscopy. Bone 36:877–883PubMedCrossRef
145.
Xie Y et al (2009) Detection of functional haematopoietic stem cell niche using real-time imaging. Nature 457:97–101PubMedCrossRef
146.
Ishii M, Egen JG, Klauschen F, Meier-Schellersheim M, Saeki Y, Vacher J, Proia RL, Germain RN (2009) Sphingosine-1-phosphate mobilizes osteoclast precursors and regulates bone homeostasis. Nature 458:524–528PubMedCrossRef
Metadata
Title
A fluorescence spotlight on the clockwork development and metabolism of bone
Authors
Tadahiro Iimura
Ayako Nakane
Mayu Sugiyama
Hiroki Sato
Yuji Makino
Takashi Watanabe
Yuzo Takagi
Rika Numano
Akira Yamaguchi
Publication date
01-05-2012
Publisher
Springer Japan
Published in
Journal of Bone and Mineral Metabolism / Issue 3/2012
Print ISSN: 0914-8779
Electronic ISSN: 1435-5604
DOI
https://doi.org/10.1007/s00774-011-0295-3

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