Zic1 transcription factor in bone: Neural developmental protein regulates mechanotransduction in osteocytes

FASEB Journal

Volumn 24, Issue 8, 2010, Pages 2893-2903

  Kalogeropoulos, Michail ^a   Varanasi, Satya S ^a   Olstad, Ole K ^c   Sanderson, Paul ^d   Gautvik, Vigdis T ^e   Reppe, Sjur ^e   Francis, Roger M ^b   Gautvik, Kaare M ^c,e,f   Birch, Mark A ^a   Datta, Harish K ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

^c ULLEVÅL UNIVERSITY HOSPITAL   (Norway)

^d NEWCASTLE UPON TYNE HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

^e Lovisenberg Deacon Hospital   (Norway)

^f UNIVERSITY OF OSLO   (Norway)

Author keywords

Fluid flow; Mechanical stress; Mechanosensors; Shear stress

Indexed keywords

LYMPHOID ENHANCER FACTOR 1; PROTEIN; PROTEIN PATCHED 1; PROTEIN ZIC; T CELL FACTOR PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GLI1; TRANSCRIPTION FACTOR GLI3; TRANSCRIPTION FACTOR ZIC1; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

ADULT; AGED; ANIMAL CELL; ARTICLE; BONE; BONE BIOPSY; CELL LINE; CELL TYPE; CEREBELLUM; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOSOL; DATA ANALYSIS SOFTWARE; FLOW RATE; GENE EXPRESSION; GENE REGULATORY NETWORK; GENE SILENCING; HUMAN; HUMAN TISSUE; ILIAC CREST; IN VITRO STUDY; LUMBAR SPINE; MALE; MECHANICAL STRESS; MECHANOTRANSDUCTION; MEDIATOR; NONHUMAN; NUCLEUS ACCUMBENS; OSCILLATORY POTENTIAL; OSTEOBLAST; OSTEOCYTE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RECEPTOR UPREGULATION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSCRIPTOMICS;

ANIMALS; BONE AND BONES; CELL LINE; CILIA; GENE EXPRESSION PROFILING; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MECHANOTRANSDUCTION, CELLULAR; MICE; NERVE TISSUE PROTEINS; OSTEOCYTES; RATS; STRESS, MECHANICAL; TRANSCRIPTION FACTORS;

MURINAE; RATTUS;

EID: 77955827746     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-148908     Document Type: Article

References (50)

1. Rubin, C. T., and Lanyon, L. E. (1984) Regulation of bone formation by applied dynamic loads. J. Bone Joint Surg. Am. 66, 397-402
2. Rubin, C. T., and Lanyon, L. E. (1985) Regulation of bone mass by mechanical strain magnitude. Calcif. Tissue Int. 37, 411-417
3. Lanyon, L. E. (1993) Osteocytes, strain detection, bone modelling and remodeling. Calcif. Tissue Int. 53, S102-S107
4. Huiskes, R., Ruimerman, R., van Lenthe, G. H., and Janssen, J. D. (2000) Effects of mechanical forces on maintenance and adaptation of form in trabecular bone. Nature 405, 704-706
5. Turner, C. H., and Pavalko, F. M., (1998) Mechanotransduction and functional response of the skeleton to physical stress: the mechanisms and mechanics of bone adaptation. J. Orthop. Sci. 3, 346-355
6. Skerry, T. M., Bitensky, L., Chayen, J., and Lanyon, L. E. (1989) Early strain-related changes in enzyme activity in osteocytes following bone loading in vivo. J. Bone Miner. Res. 4, 783-788
7. Bonewald, L. F. (2006) Mechanosensation and transduction in osteocytes. Bonekey Osteovision 3, 7-15
8. Bonewald, L. (2006) Osteocytes as multifunctional cells. J. Musculoskelet. Neuronal Interact. 6, 331-333
9. Bonewald, L. F., and Johnson, M. L. (2008) Osteocytes, mechanosensing and Wnt signaling. Bone 42, 606-615
10. Han, Y., Cowin, S. C., Schaffler, M. B., and Weinbaum, S. (2004) Mechanotransduction and strain amplification in osteocyte cell processes. Proc. Natl. Acad. Sci. U. S. A. 10, 16689-16694
11. Noble, B. S. (2008) The osteocyte lineage. Arch. Biochem. Biophys. 473, 106-111
12. Tatsumi, S., Ishii, K., Amizuka, N., Li, M., Kobayashi, T., Kohno, K., Ito, M., Takeshita, S., and Ikeda, K. (2007) Targeted ablation of osteocytes induces osteoporosis with defective mechanotransduction. Cell Metab. 5, 464-475
13. Datta, H. K., Varanasi, S. S., Olstad, O. K., Gautvik, V., Sanderson, P., Francis, R. M., Reppe, S., and Gautvik, K. M. (2009) Global transcriptome analysis of human trabecular bone reveals skeletal site-related variation in critical signalling. 31st Annual Meeting of the American Society for Bone and Mineral Research, Denver, CO (abstr SU0078)
14. Mannion, A. F., Adams, M. A., and Dolan, P. (2000) Sudden and unexpected loading generates high forces on the lumbar spine. Spine 25, 842-852
15. Aruga, J., Yokota, N., Hashimoto, M., Furuichi, T., Fukuda, M., and Mikoshiba, K. (1994) A novel zinc finger protein, Zic, is involved in neurogenesis, especially in the cell lineage of cerebellar granule cells. J. Neurochem. 63, 1880-1890
16. Aruga, J., (2004) The role of Zic genes in neural development. Mol. Cell. Neurosci. 26, 205-221
17. Aruga, J., Nagai, T., Tokuyama, T., Hayashizaki, Y., Okazaki, Y., Chapman, V. M., and Mikoshiba, K., (1996) The mouse Zic gene family: homologues of the Drosophila pair-rule gene odd-paired. J. Biol. Chem. 271, 1043-1047
18. Aruga, J., Minowa, O., Yaginuma, H., Kuno, J., Nagai, T., Noda, T., and Mikoshiba, K. (1998) Mouse Zic1 is involved in cerebellar development. J. Neurosci. 18, 284-293
19. Inoue, T., Ota, M., Mikoshiba, K., and Aruga, J., (2007) Zic2 and Zic3 synergistically control neurulation and segmentation of paraxial mesoderm in mouse embryo. Dev. Biol. 306, 669-684
20. Grinberg, I., Northrup, H., Ardinger, H., Prasad, C., Dobyns, W. B., and Millen, K. J. (2004) Heterozygous deletion of the linked genes ZIC1 and ZIC4 is involved in Dandy-Walker malformation. Nat. Genet. 36, 1053-1055
21. Al-oanzi, Z. H., Tuck, S. P., Raj, N., Harrop, J. S., Summers, G. D., Cook, D. B., Francis, R. M., and Datta, H. K. (2006) Assessment of vitamin D status in male osteoporosis. Clin. Chem. 52, 248-254
22. Reppe, S., Stilgren, L., Abrahamsen, B., Olstad, O. K., Cero, F., Brixen, K., Nissen-Meyer, L. S., and Gautvik, K. M. (2007) Abnormal muscle and hematopoietic gene expression may be important for clinical morbidity in primary hyperparathyroidism. Am. J. Physiol. Endocrinol. Metab. 292, E1465-E1473
23. Sprowson, A. P., McCaskie, A. W., and Birch, M. A. (2008) ASARM-truncated MEPE and AC-100 enhance osteogenesis by promoting osteoprogenitor adhesion. J. Orthop. Res. 26, 1256-1262
24. Kraiss, L., Weyrich, A., Alto, N., Dixon, D., Ennis, T., Modur, V., Mcintyre, T., Prescott, S., and Zimmerman, G. (2000) Fluid flow activates a regulator of translation, p70/p85 S6 kinase, in human endothelial cells. Am. J. Physiol. Heart Circ. Physiol. 278, H1537-H1544
25. Pazour, G. J., Dickert, B. L., Vucica, Y., Seeley, E. S., Rosenbaum, J.L., Witman, G. B., and Cole, D. G. (2000) Chlamydomonas IFT88 and its mouse homologue, polycystic kidney disease gene Tg737, are required for assembly of cilia and flagella. J. Cell Biol. 151, 709-718
26. Huangfu, D., and Anderson, K. V. (2006) Review: Signaling from Smo to Ci/Gli: conservation and divergence of Hedgehog pathways from Drosophila to vertebrates. Development 133, 3-14
27. Rohatgi, R., Milenkovic, L., and Scott, M. P. (2007) Patched1 regulates hedgehog signaling at the primary cilium. Science 317, 372-376
28. Wang, B., Fallon, J. F., and Beachy, P. A. (2000) Hedgehog-regulated processing of Gli3 produces an anterior/posterior repressor gradient in the developing vertebrate limb. Cell 100, 423-434
29. Koyabu, Y., Nakata, K., Mizugishi, K., Aruga, J., and Mikoshiba, K. (2001) Physical and functional interactions between Zic and Gli proteins. J. Biol. Chem. 276, 6889-6892
30. Dai, P., Akimaru, H., Tanaka, Y., Maekawa, T., Nakafuku, M., and Ishii, S. (1999) Sonic Hedgehog-induced activation of the Gli1 promoter is mediated by GLI3. J. Biol. Chem. 274, 8143-8152
31. Koyama, E., Young, B., Nagayama, M., Shibukawa, Y., Enomoto-Iwamoto, M., Iwamoto, M., Maeda, Y., Lanske, B., Song, B., Serra, R., and Pacifici, M. (2007) Conditional Kif3a ablation causes abnormal hedgehog signaling topography, growth plate dysfunction and ectopic cartilage and bone formation in mouse cranial base synchondroses. Development 134, 2159-2169
32. Zhang, Q., Murcia, N. S., Chittenden, L. R., Richards, W. G., Michaud, E. J., Woychik, R. P., and Yoder, B. K. (2003) Loss of the Tg737 protein results in skeletal patterning defects. Dev. Dyn. 227, 78-90
33. Haycraft, C. J., Banizs, B., Aydin-Son, Y., Zhang, Q., Michaud, E. J., and Yoder, B. K. (2005) Gli2 and Gli3 localize to cilia and require the intraflagellar transport protein polaris for processing and function. PLoS Genet. 1, e53
34. Kamel, M. A., Holladay, B. R., and Johnson, M. L. (2006) Potential interaction of prostaglandin and Wnt signaling pathways mediating bone cell responses to fluid flow. J. Bone Miner. Res. 21, S92 (abstr. F166)
35. Merzdorf, C. S., and Sive, H. L. (2006) The zic1 gene is an activator of Wnt signaling. Int. J. Dev. Biol. 50, 611-617
36. Xiao, Z., Zhang, S., Magenheimer, B. S., Luo, J., and Quarles, L. D. (2008) Polycystin-1 regulates skeletogenesis through stimulation of the osteoblast-specific transcription factor RUNX2-II. J. Biol. Chem. 283, 12624-12634
37. Gaur, T., Lengner, C. J., Hovhannisyan, H., Bhat, R. A., Bodine, P. V., Komm, B. S., Javed, A., van Wijnen, A. J., Stein, J. L., Stein, G. S., and Lian, J. B. (2005) Canonical WNT signaling promotes osteogenesis by directly stimulating Runx2 gene expression. J. Biol. Chem. 280, 33132-33140
38. Xiao, Z., Zhang, S., Mahlios, J., Zhou, G., Magenheimer, B. S., Guo, D., Dallas, S. L., Maser, R., Calvet, J. P., Bonewald, L., and Quarles, L. D. (2006) Cilia-like structures and polycystin-1 in osteoblasts/osteocytes and associated abnormalities in skeletogenesis and Runx2 expression. J. Biol. Chem. 281, 30884-30895
39. Malone, A. M., Anderson, C. T., Tummala, P., Kwon, R. Y., Johnston, T. R., Stearns, T., and Jacobs, C. R., (2007) Primary cilia mediate mechanosensing in bone cells by a calcium-independent mechanism. Proc. Natl. Acad. Sci. U. S. A. 104, 13325-13330
40. Zhang, K., Barragan-Adjemian, C., Ye, L., Kotha, S., Dallas, M., Lu, Y., Zhao, S., Harris, M., Harris, S. E., Feng, J. Q., and Bonewald, L. F. (2006) E11/gp38 selective expression in osteocytes: regulation by mechanical strain and role in dendrite elongation. Mol. Cell. Biol. 26, 4539-4552
41. Zhao, S., Zhang, Y. K., Harris, S., Ahuja, S. S., and Bonewald, L. F. (2002) MLO-Y4 osteocyte-like cells support osteoclast formation and activation. J. Bone Miner. Res. 17, 2068-2079
42. Taylor, A. F., Saunders, M. M., Shingle, D. L., Cimbala, J. M., Zhou, Z., and Donahue, H. J. (2007) Mechanically stimulated osteocytes regulate osteoblastic activity via gap junctions. Am. J. Physiol. Cell Physiol. 292, C545-C552
43. Vezeridis, P. S., Semeins, C. M., Qian, C., and Klein-Nulend, J. (2006) Osteocytes subjected to pulsating fluid flow regulate osteoblast proliferation and differentiation. Biochem. Biophys. Res. Commun. 348, 1082-1088
44. You, L., Temiyasathit, S., and Jacobs, C. (2008) Osteocytes as mechanosensors in the inhibition of bone resorption due to mechanical loading. Bone 42, 172-179
45. Robling, G., Niziolek, P. J., Baldridge, L. A., Condon, K. W., Allen, M. R., Alam, I., Mantila, S. M., Gluhak-Heinrich, J., Bellido, T. M., and Harris, S. E., and Turner, C. H. (2008) Mechanical stimulation of bone in vivo reduces osteocyte expression of Sost/sclerostin. J. Biol. Chem. 283, 5866-5875
46. Paic, F., Igwe, J. C., Nori, R., Kronenberg, M. S., Franceschetti, T., Harrington, P., Kuo, L., Shin, D. G., Rowe, D. W., Harris, S. E., and Kalajzic, I. (2009) Identification of differentially expressed genes between osteoblasts and osteocytes. Bone 45, 682-692
47. Skeletal site-related variation in human bone transcriptome and signaling. Received June 18, 2009 from ArrayExpress accession E-MEXP-2219, http://www.ebi.ac.uk/aerep/login
48. Yang, W., Harris, M. A., Heinrich, J. G., Guo, D., Bonewald, L. F., and Harris. S.E. (2009) Gene expression signatures of a fibroblastoid preosteoblast and cuboidal osteoblast cell model compared to the MLO-Y4 osteocyte cell model. Bone 44, 32-45
49. Yang, W., Lu, Y., Kalajzic, I., Guo, D., Harris, M. A., Gluhak-Heinrich, J., Kotha, S, Bonewald, L. F., Feng, J. Q., Rowe, D. W., Turner, C. H., Robling, A. G., and Harris, S. E. (2005) Dentin matrix protein 1 gene cis-regulation: use in osteocytes to characterize local responses to mechanical loading in vitro and in vivo. J. Biol. Chem. 280, 20680-20690
50. Collins, T. J. (2007) ImageJ for microscopy. BioTechniques 43(1 Suppl.), 25-30