A dynamic cell adhesion surface regulates tissue architecture in growth plate cartilage

Development (Cambridge)

Volumn 141, Issue 10, 2014, Pages 2085-2095

  Romereim, Sarah M ^a,b   Conoan, Nicholas H ^a   Chen, Baojiang ^a   Dudley, Andrew T ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Adhesion; Chondrogenesis; Mouse; Polarity

Indexed keywords

BETA CATENIN; CADHERIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARTILAGE CELL; CELL ADHESION; CELL FUNCTION; CELL MIGRATION; CELL POLARITY; CELL SHAPE; CELL SPREADING; CELL SURFACE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DAUGHTER CELL; ELECTRON MICROSCOPY; EXTRACELLULAR CALCIUM; GROWTH PLATE; IMMUNOFLUORESCENCE; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ADHESION; CHONDROGENESIS; MOUSE; POLARITY;

ANIMALS; ANIMALS, NEWBORN; CARTILAGE; CELL ADHESION; CELL DIVISION; CELL MEMBRANE; CELL POLARITY; CELL SHAPE; CELLS, CULTURED; CHONDROCYTES; FEMALE; GROWTH PLATE; MALE; MICE; MICE, TRANSGENIC;

EID: 84900017099     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.105452     Document Type: Article

References (63)

1. Ahrens, M. J. and Dudley, A. T. (2011). Chemical pretreatment of growth plate cartilage increases immunofluorescence sensitivity. J. Histochem. Cytochem. 59, 408-418.
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. Besson, S. and Debregeas, G. (2007). Statics and dynamics of adhesion between two soap bubbles. Eur. Phys. J. E. Soft Matter 24, 109-117.
5. Brodland, G. W. (2003). New information from cell aggregate compression tests and its implications for theories of cell sorting. Biorheology 40, 273-277.
6. Campos-Xavier, A. B., Martinet, D., Bateman, J., Belluoccio, D., Rowley, L., Tan, T. Y., Baxova, A., Gustavson, K.-H., Borochowitz, Z. U., Innes, A. M. et al. (2009). Mutations in the heparan-sulfate proteoglycan glypican 6 (GPC6) impair endochondral ossification and cause recessive omodysplasia. Am. J. Hum. Genet. 84, 760-770.
7. Chakraborty, P. K., Lee, W.-K., Molitor, M., Wolff, N. A. and Thevenod, F. (2010). Cadmium induces Wnt signaling to upregulate proliferation and survival genes in sub-confluent kidney proximal tubule cells. Mol. Cancer 9, 102.
8. 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.
9. Contreras, R. G., Miller, J. H., Zamora, M., Gonzalez-Mariscal, L. and Cereijido, M. (1992). Interaction of calcium with plasma membrane of epithelial (MDCK) cells during junction formation. Am. J. Physiol. 263, C313-C318.
10. Dodds, G. S. (1930). Row formation and other types of arrangement of cartilage cells in endochondral ossification. Anat. Rec. 46, 385-399.
11. Duguay, D., Foty, R. A. and Steinberg, M. S. (2003). Cadherin-mediated cell adhesion and tissue segregation: qualitative and quantitative determinants. Dev. Biol. 253, 309-323.
12. Dzamba, B. J., Jakab, K. R., Marsden, M., Schwartz, M. A. and DeSimone, D. W. (2009). Cadherin adhesion, tissue tension, and noncanonical Wnt signaling regulate fibronectin matrix organization. Dev. Cell. 16, 421-432.
13. Eswarakumar, V. P., Monsonego-Ornan, E., Pines, M., Antonopoulou, I., Morriss-Kay, G. M. and Lonai, P. (2002). The IIIc alternative of Fgfr2 is a positive regulator of bone formation. Development 129, 3783-3793.
14. Feil, R., Wagner, J., Metzger, D. and Chambon, P. (1997). Regulation of Cre recombinase activity by mutated estrogen receptor ligand-binding domains. Biochem. Biophys. Res. Commun. 237, 752-757.
15. Foty, R. A. and Steinberg, M. S. (2004). Cadherin-mediated cell-cell adhesion and tissue segregation in relation to malignancy. Int. J. Dev. Biol. 48, 397-409.
16. Foty, R. A. and Steinberg, M. S. (2005). The differential adhesion hypothesis: a direct evaluation. Dev. Biol. 278, 255-263.
17. Gao, B., Song, H., Bishop, K., Elliot, G., Garrett, L., English, M. A., Andre, P., Robinson, J., Sood, R., Minami, Y. et al. (2011). Wnt signaling gradients establish planar cell polarity by inducing Vangl2 phosphorylation through Ror2. Dev. Cell 20, 163-176.
18. Gemp, I. M., Carthew, R. W. and Hilgenfeldt, S. (2011). Cadherin-dependent cell morphology in an epithelium: constructing a quantitative dynamical model. PLoS Comput. Biol. 7, e1002115.
19. Graner, F. (1993). Can surface adhesion drive cell-rearrangement? Part I: biological cell-sorting. J. Theor. Biol. 164, 455-476.
20. Harris, A. K. (1976). Is Cell sorting caused by differences in the work of intercellular adhesion? A critique of the Steinberg hypothesis. J. Theor. Biol. 61, 267-285.
21. Hayashi, T. and Carthew, R. W. (2004). Surface mechanics mediate pattern formation in the developing retina. Nature 431, 647-652.
22. Hunziker, E. B. (1994). Mechanism of longitudinal bone growth and its regulation by growth plate chondrocytes. Microsc. Res. Tech. 28, 505-519.
23. Hunziker, E. B. and Schenk, R. K. (1989). Physiological mechanisms adopted by chondrocytes in regulating longitudinal bone growth in rats. J. Physiol. 414, 55-71.
24. Karsenty, G. and Wagner, E. F. (2002). Reaching a genetic and molecular understanding of skeletal development. Dev. Cell 2, 389-406.
25. Keller, R., Davidson, L., Edlund, A., Elul, T., Ezin, M., Shook, D. and Skoglund, P. (2000). Mechanisms of convergence and extension by cell intercalation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355, 897-922.
26. Kim, S. A., Tai, C.-Y., Mok, L.-P., Mosser, E. A. and Schuman, E. M. (2011). Calcium-dependent dynamics of cadherin interactions at cell-cell junctions. Proc. Natl. Acad. Sci. U.S.A. 108, 9857-9862.
27. King, K. B. and Kimura, J. H. (2003). The establishment and characterization of an immortal cell line with a stable chondrocytic phenotype. J. Cell Biochem. 89, 992-1004.
28. Kovacs, E. M., Goodwin, M., Ali, R. G., Paterson, A. D. and Yap, A. S. (2002). Cadherin-directed actin assembly: E-cadherin physically associates with the Arp2/3 complex to direct actin assembly in nascent adhesive contacts. Curr. Biol. 12, 379-382.
29. Koyama, E., Young, B., Nagayama, M., Shibukawa, Y., Enomoto-Iwamoto, M., Iwamoto, M., Maeda, Y., Lanske, B., Song, B., Serra, R. et al. (2007). Conditional Kif3a ablation causes abnormal hedgehog signaling topography, growth plate dysfunction, and excessive bone and cartilage formation during mouse skeletogenesis. Development 134, 2159-2169.
30. Kraft, B., Berger, C. D., Wallkamm, V., Steinbeisser, H. and Wedlich, D. (2012). Wnt-11 and Fz7 reduce cell adhesion in convergent extension by sequestration of PAPC and C-cadherin. J. Cell Biol. 198, 695-709.
31. Kronenberg, H. M. (2003). Developmental regulation of the growth plate. Nature 423, 332-336.
32. Li, Y. and Dudley, A. T. (2009). Noncanonical frizzled signaling regulates cell polarity of growth plate chondrocytes. Development 136, 1083-1092.
33. Li, Y., Ahrens, M. J., Wu, A., Liu, J. and Dudley, A. T. (2011). Calcium/calmodulin- dependent protein kinase II activity regulates the proliferative potential of growth plate chondrocytes. Development 138, 359-370.
34. Liu, Z., Tan, J. L., Cohen, D. M., Yang, M. T., Sniadecki, N. J., Ruiz, S. A., Nelson, C. M. and Chen, C. S. (2010). Mechanical tugging force regulates the size of cell-cell junctions. Proc. Natl. Acad. Sci. U.S.A. 107, 9944-9949.
35. Manning, M. L., Foty, R. A., Steinberg, M. S. and Schoetz, E.-M. (2010). Coaction of intercellular adhesion and cortical tension specifies tissue surface tension. Proc. Natl. Acad. Sci. U.S.A. 107, 12517-12522.
36. Maruthamuthu, V., Sabass, B., Schwarz, U. S. and Gardel, M. L. (2011). Cell- ECM traction force modulates endogenous tension at cell-cell contacts. Proc. Natl. Acad. Sci. U.S.A. 108, 4708-4713.
37. McBratney-Owen, B., Iseki, S., Bamforth, S. D., Olsen, B. R. and Morriss-Kay, G. M. (2008). Development and tissue origins of the mammalian cranial base. Dev. Biol. 322, 121-132.
38. Mukhopadhyay, K., Lefebvre, V., Zhou, G., Garofalo, S., Kimura, J. H. and de Crombrugghe, B. (1995). Use of a new rat chondrosarcoma cell line to delineate a 119-base pair chondrocyte-specific enhancer element and to define active promoter segments in the mouse pro-alpha 1(II) collagen gene. J. Biol. Chem. 270, 27711-27719.
39. Muzumdar, M. D., Tasic, B., Miyamichi, K., Li, L. and Luo, L. (2007). A global double-fluorescent Cre reporter mouse. Genesis 45, 593-605.
40. Nagayama, M., Iwamoto, M., Hargett, A., Kamiya, N., Tamamura, Y., Young, B., Morrison, T., Takeuchi, H., Pacifici, M., Enomoto-Iwamoto, M. et al. (2008). Wnt/beta-catenin signaling regulates cranial base development and growth. J. Dent. Res. 87, 244-249.
41. Nakamura, E., Nguyen, M.-T. and Mackem, S. (2006). Kinetics of tamoxifen- regulated Cre activity in mice using a cartilage-specific CreER(T) to assay temporal activity windows along the proximodistal limb skeleton. Dev. Dyn. 235, 2603-2612.
42. Peng, Y. and Axelrod, J. D. (2012). Asymmetric protein localization in planar cell polarity: mechanisms, puzzles, and challenges. Curr. Top. Dev. Biol. 101, 33-53.
43. Prozialeck, W. C. and Lamar, P. C. (1999). Interaction of cadmium (Cd(2+)) with a 13-residue polypeptide analog of a putative calcium-binding motif of E-cadherin. Biochim. Biophys. Acta 1451, 93-100.
44. Prozialeck, W. C. and Niewenhuis, R. J. (1991). Cadmium (Cd2+) disrupts Ca(2+)-dependent cell-cell junctions and alters the pattern of E-cadherin immunofluorescence in LLC-PK1 cells. Biochem. Biophys. Res. Commun. 181, 1118-1124.
45. Prozialeck, W. C., Lamar, P. C. and Lynch, S. M. (2003). Cadmium alters the localization of N-cadherin, E-cadherin, and beta-catenin in the proximal tubule epithelium. Toxicol. Appl. Pharmacol. 189, 180-195.
46. Randall, R. M., Shao, Y. Y., Wang, L. and Ballock, R. T. (2012). Activation of Wnt Planar Cell Polarity (PCP) signaling promotes growth plate column formation in vitro. J. Orthop. Res. 30, 1906-1914.
47. Romereim, S. M. and Dudley, A. T. (2011). Cell polarity: the missing link in skeletal morphogenesis? Organogenesis 7, 217-228.
48. Shum, L., Wang, X., Kane, A. A. and Nuckolls, G. H. (2003). BMP4 promotes chondrocyte proliferation and hypertrophy in the endochondral cranial base. Int. J. Dev. Biol. 47, 423-431.
49. Singh, J. and Mlodzik, M. (2012). Planar cell polarity signaling: coordination of cellular orientation across tissues. Wiley Interdiscip. Rev. Dev. Biol. 1, 479-499.
50. Thery, M., Pepin, A., Dressaire, E., Chen, Y. and Bornens, M. (2006a). Cell distribution of stress fibres in response to the geometry of the adhesive environment. Cell Motil. Cytoskeleton 63, 341-355.
51. Thery, M., Racine, V., Piel, M., Pepin, A., Dimitrov, A., Chen, Y., Sibarita, J.-B. and Bornens, M. (2006b). Anisotropy of cell adhesive microenvironment governs cell internal organization and orientation of polarity. Proc. Natl. Acad. Sci. U.S.A. 103, 19771-19776.
52. Thompson, J., Wong, L., Lau, P. S. and Bannigan, J. (2008). Adherens junction breakdown in the periderm following cadmium administration in the chick embryo: distribution of cadherins and associated molecules. Reprod. Toxicol. 25, 39-46.
53. Topczewski, J., Sepich, D. S., Myers, D. C., Walker, C., Amores, A., Lele, Z., Hammerschmidt, M., Postlethwait, J. and Solnica-Krezel, L. (2001). The zebrafish glypican knypek controls cell polarity during gastrulation movements of convergent extension. Dev. Cell 1, 251-264.
54. Troyanovsky, R. B., Laur, O. and Troyanovsky, S. M. (2007). Stable and unstable cadherin dimers: mechanisms of formation and roles in cell adhesion. Mol. Biol. Cell 18, 4343-4352.
55. Volk, T. and Geiger, B. (1986). A-CAM: a 135-kD receptor of intercellular adherens junctions. II. Antibody-mediated modulation of junction formation. J. Cell Biol. 103, 1451-1464.
56. Wallingford, J. B., Fraser, S. E. and Harland, R. M. (2002). Convergent extension: the molecular control of polarized cell movement during embryonic development. Dev. Cell 2, 695-706.
57. 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.
58. Wilson, E. B. (1900). The Cell in Development and Inheritance. Norwood, MA: The Macmillan Company, Norwood Press.
59. Wilson, R., Diseberg, A. F., Gordon, L., Zivkovic, S., Tatarczuch, L., Mackie, E. J., Gorman, J. J. and Bateman, J. F. (2010). Comprehensive profiling of cartilage extracellular matrix formation and maturation using sequential extraction and label- free quantitative proteomics. Mol. Cell. Proteomics 9, 1296-1313.
60. Yang, Y. (2009). Growth and patterning in the limb: signaling gradients make the decision. Sci. Signal. 2, p e3.
61. 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.
62. Yin, C., Ciruna, B. and Solnica-Krezel, L. (2009). Convergence and extension movements during vertebrate gastrulation. Curr. Top. Dev. Biol. 89, 163-192.
63. Young, B., Minugh-Purvis, N., Shimo, T., St-Jacques, B., Iwamoto, M., Enomoto-Iwamoto, M., Koyama, E. and Pacifici, M. (2006). Indian and sonic hedgehogs regulate synchondrosis growth plate and cranial base development and function. Dev. Biol. 299, 272-282.