Calcium/calmodulin-dependent protein kinase II activity regulates the proliferative potential of growth plate chondrocytes

Development

Volumn 138, Issue 2, 2011, Pages 359-370

  Li, Yuwei ^a   Ahrens, Molly J ^a   Wu, Amy ^a   Liu, Jennifer ^a   Dudley, Andrew T ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Adult stem cells; CamkII; Cartilage; Chick; Chondrocyte maturation; Growth plate; Kinase; Mouse; Transit amplification

Indexed keywords

BETA CATENIN; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; FRIZZLED PROTEIN; PARATHYROID HORMONE RELATED PROTEIN; TRANSCRIPTION FACTOR RUNX2; WNT PROTEIN;

ANIMAL CELL; ARTICLE; CARTILAGE CELL; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; GROWTH PLATE; GROWTH REGULATION; HYPERTROPHY; IMMUNOFLUORESCENCE; IN SITU HYBRIDIZATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STEM CELL; WESTERN BLOTTING;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASE SEQUENCE; BETA CATENIN; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CELL ENLARGEMENT; CELL PROLIFERATION; CHICK EMBRYO; CHONDROCYTES; CORE BINDING FACTOR ALPHA 1 SUBUNIT; DNA PRIMERS; FRIZZLED RECEPTORS; GROWTH PLATE; MICE; MICE, MUTANT STRAINS; MODELS, BIOLOGICAL; PARATHYROID HORMONE-RELATED PROTEIN; SIGNAL TRANSDUCTION;

EID: 78751509038     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.052324     Document Type: Article

References (58)

1. Abad, V., Meyers, J. L., Weise, M., Gafni, R. I., Barnes, K. M., Nilsson, O., Bacher, J. D. and Baron, J. (2002). The role of the resting zone in growth plate chondrogenesis. Endocrinology 143, 1851-1857.
2. Ahrens, M. J., Li, Y., Jiang, H. and Dudley, A. T. (2009). Convergent extension movements in growth plate chondrocytes require gpi-anchored cell surface proteins. Development 136, 3463-3474.
3. Aszodi, A., Hunziker, E. B., Brakebusch, C. and Fassler, R. (2003). Beta1 integrins regulate chondrocyte rotation, G1 progression, and cytokinesis. Genes Dev. 17, 2465-2479.
4. Brault, V., Moore, R., Kutsch, S., Ishibashi, M., Rowitch, D. H., McMahon, A. P., Sommer, L., Boussadia, O. and Kemler, R. (2001). Inactivation of the betacatenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 128, 1253-1264.
5. Breur, G. J., VanEnkevort, B. A., Farnum, C. E. and Wilsman, N. J. (1991). Linear relationship between the volume of hypertrophic chondrocytes and the rate of longitudinal bone growth in growth plates. J. Orthop. Res. 9, 348-359.
6. Breur, G. J., Turgai, J., Vanenkevort, B. A., Farnum, C. E. and Wilsman, N. J. (1994). Stereological and serial section analysis of chondrocytic enlargement in the proximal tibial growth plate of the rat. Anat. Rec. 239, 255-268.
7. Chen, L., Adar, R., Yang, X., Monsonego, E. O., Li, C., Hauschka, P. V., Yayon, A. and Deng, C. X. (1999). Gly369Cys mutation in mouse FGFR3 causes achondroplasia by affecting both chondrogenesis and osteogenesis. J. Clin. Invest. 104, 1517-1525.
8. de Haan, G., Dontje, B. and Nijhof, W. (1996). Concepts of hemopoietic cell amplification. Synergy, redundancy and pleiotropy of cytokines affecting the regulation of erythropoiesis. Leuk. Lymphoma 22, 385-394.
9. De Luca, F., Barnes, K. M., Uyeda, J. A., De-Levi, S., Abad, V., Palese, T., Mericq, V. and Baron, J. (2001). Regulation of growth plate chondrogenesis by bone morphogenetic protein-2. Endocrinology 142, 430-436.
10. Dodds, G. (1930). Row formation and other types of arrangement of cartilage cells in endochondral ossification. Anat. Rec. 46, 385-399.
11. Dong, Y.-F., Soung, D. Y., Schwarz, E. M., O'Keefe, R. J. and Drissi, H. (2006). Wnt induction of chondrocyte hypertrophy through the Runx2 transcription factor. J. Cell. Physiol. 208, 77-86.
12. Fagerholm, A. E., Habrant, D. and Koskinen, A. M. (2010). Calyculins and related marine natural products as serine-threonine protein phosphatase PP1 and PP2A inhibitors and total syntheses of calyculin A, B, and C. Mar. Drugs 8, 122-172.
13. Franceschi, R. T., Xiao, G., Jiang, D., Gopalakrishnan, R., Yang, S. and Reith, E. (2003). Multiple signaling pathways converge on the Cbfa1/Runx2 transcription factor to regulate osteoblast differentiation. Connect. Tissue Res. 44 Suppl. 1, 109-116.
14. Guo, J., Chung, U. I., Yang, D., Karsenty, G., Bringhurst, F. R. and Kronenberg, H. M. (2006). PTH/PTHrP receptor delays chondrocyte hypertrophy via both Runx2-dependent and -independent pathways. Dev. Biol. 292, 116-128.
15. Guo, X., Mak, K. K., Taketo, M. M. and Yang, Y. (2009). The Wnt/beta-catenin pathway interacts differentially with PTHrP signaling to control chondrocyte hypertrophy and final maturation. PLoS ONE 4, e6067.
16. Hartmann, C. and Tabin, C. J. (2000). Dual roles of Wnt signaling during chondrogenesis in the chick limb. Development 127, 3141-3159.
17. Hill, T. P., Spater, D., Taketo, M. M., Birchmeier, W. and Hartmann, C. (2005). Canonical Wnt/beta-catenin signaling prevents osteoblasts from differentiating into chondrocytes. Dev. Cell 8, 727-738.
18. Hughes, S. H. (2004). The RCAS vector system. Folia Biol. (Praha) 50, 107-119.
19. Hunziker, E. B. (1994). Mechanism of longitudinal bone growth and its regulation by growth plate chondrocytes. Microsc. Res. Tech. 28, 505-519.
20. Hunziker, E. B., Schenk, R. K. and Cruz-Orive, L. M. (1987). Quantitation of chondrocyte performance in growth-plate cartilage during longitudinal bone growth. J. Bone Joint Surg. Am. 69, 162-173.
21. Insco, M. L., Leon, A., Tam, C. H., McKearin, D. M. and Fuller, M. T. (2009). Accumulation of a differentiation regulator specifies transit amplifying division number in an adult stem cell lineage. Proc. Natl. Acad. Sci. USA 106, 22311-22316.
22. Ishida, A. and Fujisawa, H. (1995). Stabilization of calmodulin-dependent protein kinase II through the autoinhibitory domain. J. Biol. Chem. 270, 2163-2170.
23. Ishida, A., Kameshita, I., Okuno, S., Kitani, T. and Fujisawa, H. (1995). A novel highly specific and potent inhibitor of calmodulin-dependent protein kinase II. Biochem. Biophys. Res. Commun. 212, 806-812.
24. Ishida, A., Kameshita, I. and Fujisawa, H. (1998a). A novel protein phosphatase that dephosphorylates and regulates Ca2+/calmodulin-dependent protein kinase II. J. Biol. Chem. 273, 1904-1910.
25. Ishida, A., Okuno, S., Kitani, T., Kameshita, I. and Fujisawa, H. (1998b). Regulation of multifunctional Ca2+/calmodulin-dependent protein kinases by Ca2+/calmodulin-dependent protein kinase phosphatase. Biochem. Biophys. Res. Commun. 253, 159-163.
26. Ishihara, H., Martin, B. L., Brautigan, D. L., Karaki, H., Ozaki, H., Kato, Y., Fusetani, N., Watabe, S., Hashimoto, K., Uemura, D. et al. (1989). Calyculin A and okadaic acid: inhibitors of protein phosphatase activity. Biochem. Biophys. Res. Commun. 159, 871-877.
27. Izergina, N., Balmer, J., Bello, B. and Reichert, H. (2009). Postembryonic development of transit amplifying neuroblast lineages in the Drosophila brain. Neural Dev. 4, 44.
28. Kameshita, I., Ishida, A. and Fujisawa, H. (1999). Phosphorylation and activation of Ca2+/calmodulin-dependent protein kinase phosphatase by Ca2+/calmodulin-dependent protein kinase II. FEBS Lett. 456, 249-252.
29. Kitagawa, Y., Hirano, T. and Kawaguchi, S. Y. (2009). Prediction and validation of a mechanism to control the threshold for inhibitory synaptic plasticity. Mol. Syst. Biol. 5, 280.
30. Kozhemyakina, E., Cohen, T., Yao, T.-P. and Lassar, A. B. (2009). Parathyroid hormone-related peptide represses chondrocyte hypertrophy through a protein phosphatase 2A/histone deacetylase 4/MEF2 pathway. Mol. Cell. Biol. 29, 5751-5762.
31. Kronenberg, H. M. (2003). Developmental regulation of the growth plate. Nature 423, 332-336.
32. Kuhl, M., Sheldahl, L. C., Malbon, C. C. and Moon, R. T. (2000a). Ca(2+)/calmodulin-dependent protein kinase II is stimulated by Wnt and Frizzled homologs and promotes ventral cell fates in Xenopus. J. Biol. Chem. 275, 12701-12711.
33. Kuhl, M., Sheldahl, L. C., Park, M., Miller, J. R. and Moon, R. T. (2000b). The Wnt/Ca2+ pathway: a new vertebrate Wnt signaling pathway takes shape. Trends Genet. 16, 279-283.
34. Kuhl, M., Geis, K., Sheldahl, L. C., Pukrop, T., Moon, R. T. and Wedlich, D. (2001). Antagonistic regulation of convergent extension movements in Xenopus by Wnt/beta-catenin and Wnt/Ca2+ signaling. Mech. Dev. 106, 61-76.
35. Lanske, B., Karaplis, A. C., Lee, K., Luz, A., Vortkamp, A., Pirro, A., Karperien, M., Defize, L. H., Ho, C., Mulligan, R. C. et al. (1996). PTH/PTHrP receptor in early development and Indian hedgehog-regulated bone growth. Science 273, 663-666.
36. Legeai-Mallet, L., Benoist-Lasselin, C., Delezoide, A. L., Munnich, A. and Bonaventure, J. (1998). Fibroblast growth factor receptor 3 mutations promote apoptosis but do not alter chondrocyte proliferation in thanatophoric dysplasia. J. Biol. Chem. 273, 13007-13014.
37. Li, T. F., Dong, Y., Ionescu, A. M., Rosier, R. N., Zuscik, M. J., Schwarz, E. M., O'Keefe, R. J. and Drissi, H. (2004). Parathyroid hormone-related peptide (PTHrP) inhibits Runx2 expression through the PKA signaling pathway. Exp. Cell Res. 299, 128-136.
38. Li, Y. and Dudley, A. T. (2009). Noncanonical frizzled signaling regulates cell polarity in growth plate chondroctyes. Development 136, 1083-1092.
39. Lisman, J. E. and Zhabotinsky, A. M. (2001). A model of synaptic memory: a CaMKII/PP1 switch that potentiates transmission by organizing an AMPA receptor anchoring assembly. Neuron 31, 191-201.
40. Logan, M. and Tabin, C. (1998). Targeted gene misexpression in chick limb buds using avian replication-competent retroviruses. Methods 14, 407-420.
41. Lyons, K. M., Jones, C. M. and Hogan, B. L. (1991). The DVR gene family in embryonic development. Trends Genet. 7, 408-412.
42. Mak, K. K., Chen, M. H., Day, T. F., Chuang, P. T. and Yang, Y. (2006). Wnt/betacatenin signaling interacts differentially with Ihh signaling in controlling endochondral bone and synovial joint formation. Development 133, 3695-3707.
43. Mancilla, E. E., De Luca, F., Uyeda, J. A., Czerwiec, F. S. and Baron, J. (1998). Effects of fibroblast growth factor-2 on longitudinal bone growth. Endocrinology 139, 2900-2904.
44. Ovchinnikov, D. A., Deng, J. M., Ogunrinu, G. and Behringer, R. R. (2000). Col2a1-directed expression of Cre recombinase in differentiating chondrocytes in transgenic mice. Genesis 26, 145-146.
45. Papkoff, J., Rubinfeld, B., Schryver, B. and Polakis, P. (1996). Wnt-1 regulates free pools of catenins and stabilizes APC-catenin complexes. Mol. Cell. Biol. 16, 2128-2134.
46. Pi, H. J. and Lisman, J. E. (2008). Coupled phosphatase and kinase switches produce the tristability required for long-term potentiation and long-term depression. J. Neurosci. 28, 13132-13138
47. Robison, A. J., Bartlett, R. K., Bass, M. A. and Colbran, R. J. (2005). Differential modulation of Ca2+/calmodulin-dependent protein kinase II activity by regulated interactions with N-methyl-D-aspartate receptor NR2B subunits and alphaactinin. J. Biol. Chem. 280, 39316-39323.
48. Rubinfeld, B., Robbins, P., El-Gamil, M., Albert, I., Porfiri, E. and Polakis, P. (1997). Stabilization of beta-catenin by genetic defects in melanoma cell lines. Science 275, 1790-1792.
49. Sato, S., Kimura, A., Ozdemir, J., Asou, Y., Miyazaki, M., Jinno, T., Ae, K., Liu, X., Osaki, M., Takeuchi, Y. et al. (2008). The distinct role of the Runx proteins in chondrocyte differentiation and intervertebral disc degeneration: Findings in murine models and in human disease. Arthritis Rheum. 58, 2764-2775.
50. Schulz, C., Kiger, A. A., Tazuke, S. I., Yamashita, Y. M., Pantalena-Filho, L. C., Jones, D. L., Wood, C. G. and Fuller, M. T. (2004). A misexpression screen reveals effects of bag-of-marbles and TGF beta class signaling on the Drosophila male germ-line stem cell lineage. Genetics 167, 707-723.
51. Sumi, M., Kiuchi, K., Ishikawa, T., Ishii, A., Hagiwara, M., Nagatsu, T. and Hidaka, H. (1991). The newly synthesized selective Ca2+/calmodulin dependent protein kinase II inhibitor KN-93 reduces dopamine contents in PC12h cells. Biochem. Biophys. Res. Commun. 181, 968-975.
52. Swarthout, J. T., D'Alonzo, R. C., Selvamurugan, N. and Partridge, N. C. (2002). Parathyroid hormone-dependent signaling pathways regulating genes in bone cells. Gene 282, 1-17.
53. Taschner, M. J., Rafigh, M., Lampert, F., Schnaiter, S. and Hartmann, C. (2008). Ca2+/Calmodulin-dependent kinase II signaling causes skeletal overgrowth and premature chondrocyte maturation. Dev. Biol. 317, 132-146.
54. Vortkamp, A., Lee, K., Lanske, B., Segre, G. V., Kronenberg, H. M. and Tabin, C. J. (1996). Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science 273, 613-622.
55. Wang, Z., Palmer, G. and Griffith, L. C. (1998). Regulation of Drosophila Ca2+/calmodulin-dependent protein kinase II by autophosphorylation analyzed by site-directed mutagenesis. J. Neurochem. 71, 378-387.
56. Wilsman, N. J., Farnum, C. E., Green, E. M., Lieferman, E. M. and Clayton, M. K. (1996). Cell cycle analysis of proliferative zone chondrocytes in growth plates elongating at different rates. J. Orthop. Res. 14, 562-572.
57. Yang, Y., Topol, L., Lee, H. and Wu, J. (2003). Wnt5a and Wnt5b exhibit distinct activities in coordinating chondrocyte proliferation and differentiation. Development 130, 1003-1015.
58. Yoon, B. S. and Lyons, K. M. (2004). Multiple functions of BMPs in chondrogenesis. J. Cell. Biochem. 93, 93-103.