The MAGUK-family protein CASK is targeted to nuclei of the basal epidermis and controls keratinocyte proliferation

Journal of Cell Science

Volumn 121, Issue 16, 2008, Pages 2705-2717

  Ojeh, Nkemcho ^a   Pekovic, Vanja ^a   Jahoda, Colin ^a   Määttä, Arto ^a  

^a DURHAM UNIVERSITY   (United Kingdom)

Author keywords

CASK; Keratinocytes; Nucleus; Proliferation; Wound healing

Indexed keywords

KERATINOCYTE GROWTH FACTOR; MEMBRANE ASSOCIATED GUANYLATE CYCLASE KINASE; MYC PROTEIN; PROTEIN KINASE (CALCIUM,CALMODULIN); PROTEIN SERINE THREONINE KINASE; TRANSFORMING GROWTH FACTOR ALPHA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL CYCLE S PHASE; CELL DIFFERENTIATION; CELL MEMBRANE; CELL MIGRATION; CELL NUCLEUS; CELL PROLIFERATION; CELL SPREADING; CONTROLLED STUDY; DOWN REGULATION; EPIDERMIS; EPIDERMIS CELL; EXTRACELLULAR MATRIX; GROWTH REGULATION; HAIR FOLLICLE; HUMAN; HUMAN CELL; KERATINOCYTE; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; RECEPTOR UPREGULATION; RNA INTERFERENCE; SKIN GRAFT; TISSUE CULTURE; UPREGULATION; WOUND HEALING;

ANIMALS; ANIMALS, NEWBORN; BASEMENT MEMBRANE; CELL DIFFERENTIATION; CELL MOVEMENT; CELL NUCLEUS; CELL PROLIFERATION; CELLS, CULTURED; EPIDERMIS; GUANYLATE KINASE; HAIR FOLLICLE; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KERATINOCYTES; MICE; MICE, INBRED C57BL; MULTIGENE FAMILY; PROTEIN TRANSPORT; WOUND HEALING;

RODENTIA;

EID: 52649086911     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.025643     Document Type: Article

References (50)

1. Alexander, C. M., Reichsman, F., Hinkes, M. T., Lincecum, J., Becker, K. A., Cumberledge, S. and Bernfield, M. (2000). Syndecan-1 is required for Wnt-1-induced mammary tumorigenesis in mice. Nat. Genet. 25, 329-332.
2. Arnold, I. and Watt, F. M. (2001). c-Myc activation in transgenic mouse epidermis results in mobilization of stem cells and differentiation of their progeny. Curr. Biol. 11, 558-568.
3. Atasoy, D., Schoch, S., Ho, A., Nadasy, K. A., Liu, X., Zhang, W., Mukherjee, K., Nosyreva, E. D., Fernandez-Chacon, R., Missler, M. et al. (2007). Deletion of CASK in mice is lethal and impairs synaptic function. Proc. Natl. Acad. Sci. USA 104, 2525-2530.
4. Baeg, G. H., Lin, X., Khare, N., Baumgartner, S. and Perrimon, N. (2001). Heparan sulfate proteoglycans are critical for the organization of the extracellular distribution of Wingless. Development 128, 87-94.
5. Benezra, M., Greenberg, R. S. and Masur, S. K. (2007). Localization of ZO-1 in the nucleolus of corneal fibroblasts. Invest. Ophthalmol. Vis. Sci. 48, 2043-2049.
6. Blanpain, C., Lowry, W. E., Pasolli, H. A. and Fuchs, E. (2006). Canonical notch signaling functions as a commitment switch in the epidermal lineage. Genes Dev. 20, 3022-3035.
7. Chellappan, S. P., Hiebert, S., Mudryj, M., Horowitz, J. M. and Nevins, J. R. (1991). The E2F transcription factor is a cellular target for the RB protein. Cell 65, 1053-1061.
8. Cohen, A. R., Woods, D. F., Marfatia, S. M., Walther, Z., Chishti, A. H. and Anderson, J. M. (1998). Human CASK/LIN-2 binds syndecan-2 and protein 4.1 and localizes to the basolateral membrane of epithelial cells. J. Cell Biol. 142, 129-138.
9. Dyer, J. A., Kill, I. R., Pugh, G., Quinlan, R. A., Lane, E. B. and Hutchison, C. J. (1997). Cell cycle changes in A-type lamin associations detected in human dermal fibroblasts using monoclonal antibodies. Chromosome Res. 5, 383-394.
10. Elenius, K., Vainio, S., Laato, M., Sahnivirta, M., Thesleff, I. and Jalkanen, M. (1991). Induced expression of syndecan in healing wounds. J. Cell Biol. 114, 585-595.
11. Elenius, V., Gotte, M., Reizes, O., Elenius, K. and Bernfield, M. (2004). Inhibition by the soluble syndecan-1 ectodomains delays wound repair in mice overexpressing syndecan-1. J. Biol. Chem. 279, 41928-41935.
12. Frye, M. and Watt, F. M. (2006). The RNA methyltransferase Misu (NSun2) mediates Myc-induced proliferation and is upregulated in tumors. Curr. Biol. 16, 971-981.
13. Funke, L., Dakoji, S. and Bredt, D. S. (2005). Membrane-associated guanylate kinases regulate adhesion and plasticity at cell junctions. Annu. Rev. Biochem. 74, 219-245.
14. Gardner, K. L., Sanford, J. L., Mays, T. A. and Rafael-Fortney, J. A. (2006). CASK localizes to nuclei in developing skeletal muscle and motor neuron culture models and is agrin-independent. J. Cell Physiol. 206, 196-202.
15. Geng, Y. and Weinberg, R. A. (1993). Transforming growth factor beta effects on expression of G1 cyclins and cyclin-dependent protein kinases. Proc. Natl. Acad. Sci. USA 90, 10315-10319.
16. Grootjans, J. J., Zimmermann, P., Reekmans, G., Smets, A., Degeest, G., Durr, J. and David, G. (1997). Syntenin, a PDZ protein that binds syndecan cytoplasmic domains. Proc. Natl. Acad. Sci USA 94, 13683-13688.
17. Guimond, S., Maccarana, M., Olwin, B. B., Lindahl, U. and Rapraeger, A. C. (1993). Activating and inhibitory heparin sequences for FGF-2 (basic FGF). Distinct requirements for FGF-1, FGF-2, and FGF-4. J. Biol. Chem. 268, 23906-23914.
18. Hata, Y., Butz, S. and Sudhof, T. C. (1996). CASK: a novel dlg/ PSD95 homolog with an N-terminal calmodulin-dependent protein kinase domain identified by interaction with neurexins. J. Neurosci. 16, 2488-2494.
19. Hennings, H., Michael, D., Cheng, C., Steinert, P., Holbrook, K. and Yuspa, S. H. (1980). Calcium regulation of growth and differentiation of mouse epidermal cells in culture. Cell 19, 245-254.
20. Hsueh, Y. P. (2006). The role of the MAGUK protein CASK in neural development and synaptic function. Curr. Med. Chem. 13, 1915-1927.
21. Hsueh, Y. P. and Sheng, M. (1999). Regulated expression and subcellular localization of syndecan heparan sulfate proteoglycans and the syndecan-binding protein CASK/LIN-2 during rat brain development. J. Neurosci. 19, 7415-7425.
22. Hsueh, Y. P., Yang, F. C., Kharazia, V., Naisbitt, S., Cohen, A. R., Weinberg, R. J. and Sheng, M. (1998). Direct interaction of CASK/ LIN-2 and syndecan heparan sulfate proteoglycan and their overlapping distribution in neuronal synapses. J. Cell Biol. 142, 139-151.
23. Hsueh, Y. P., Wang, T. F., Yang, F. C. and Sheng, M. (2000). Nuclear translocation and transcription regulation by the membrane-associated guanylate kinase CASK/LIN-2. Nature 404, 298-302.
24. Kurose, A., Tanaka, T., Huang, X., Traganos, F. and Darynkiewicz, Z. (2006). Synchronization in the cell cycle by inhibitors of DNA replication induces histone H2AX phosphorylation: an indication of DNA damage. Cell Prolif. 39, 231-240.
25. Laverty, H. G. and Wilson, J. B. (1998). Marine CASK is disrupted in a sex-linked cleft palate mouse mutant. Genomics 53, 29-41.
26. Lee, S., Fan, S., Makarova, O., Straight, S. and Margolis, B. (2002). A novel and conserved protein-protein interaction domain of mammalian Liu-2/CASK binds and recruits SAP97 to the lateral surface of epithelia. Mol. Cell. Biol. 22, 1778-1791.
27. Lehtonen, S., Ryan, J. J., Kudlicka, K., Iino, N., Zhou, H. and Farquhar, M. G. (2005). Cell junction-associated proteins IQGAP1, MAGI-2, CASK, spectrins, and alpha-actinin are components of the nephrin multiprotein complex. Proc. Natl. Acad. Sci. USA 102, 9814-9819.
28. Long, H. A., Boczonadi, V., McInroy, L., Goldberg, M. and Maatta, A. (2006). Periplakin-dependent re-organisation of keratin cytoskeleton and loss of collective migration in keratin-8-downregulated epithelial sheets. J. Cell Sci. 119, 5147-5159.
29. Long B. M. and Sahnivirta, M. (2002). Heparin/Heparan sulfate domains in binding and signaling of fibroblast growth factor 8b. J. Biol. Chem. 277, 32616-32623.
30. Lyon, M., Rushton, G. and Gallagher, J. T. (1997). The interaction of the transforming growth factor-betas with heparin/heparan sulfate is isoform-specific. J. Biol. Chem. 272, 18000-18006.
31. Martinez-Estrada, O. M., Villa, A., Breviario, F., Orsenigo, F., Dejana, E. and Bazzoni, G. (2001). Association of junctional adhesion molecule with calcium/calmodulin-dependent serine protein kinase (CASK/ LIN-2) in human epithelial caco-2 cells. J. Biol. Chem. 276, 9291-9296.
32. Mortier, E., Wuytens, G., Leenaerts, I., Hannes, F., Heung, M. Y., Degeest, G., David, G. and Zimmermann, P. (2005). Nuclear speckles and nucleoli targeting by PIP2-PDZ domain interactions. EMBO J. 24, 2556-2565.
33. Munger, K., Pietenpol, J. A., Pittelkow, M. R., Holt, J. T. and Moses, H. L. (1992). Transforming growth factor beta 1 regulation of c-myc expression, pRB phosphorylation, and cell cycle progression in keratinocytes. Cell Growth Differ. 3, 291-298.
34. Nix, S. L., Chishti, A. H., Anderson, J. M. and Walther, Z. (2000). hCASK and hDlg associate in epithelia, and their src homology 3 and guanylate kinase domains participate in both intramolecular and intermolecular interactions. J. Biol. Chem. 275, 41192-41200.
35. Ojeh, N. O., Frame, J. D. and Navsaria, H. A. (2001). In vitro characterization of an artificial dermal scaffold. Tissue Eng. 7, 457-472.
36. Ojeh, N., Hiilesvuo, K., Warri, A., Salmivirta, M., Henttinen, T. and Maatta, A. (2008). Ectopic expression of syndecan-1 in basal epidermis affects keratinocyte proliferation and wound re-epithelialization. J. Invest. Dermatol. 128, 26-34.
37. Pekovic, V., Harborth, J., Broers, J. L., Ramaekers, F. C., van Engelen, B., Lammens, M., von Zglinicki, T., Foisner, R., Hutchison, C. and Markiewicz, E. (2007). Nucleoplasmic LAP2alpha-lamin A complexes are required to maintain a proliferative state in human fibroblasts. J. Cell Biol. 176, 163-172.
38. Rapraeger, A. C., Krufka, A. and Olwin, B. B. (1991). Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation. Science 252, 1705-1708.
39. Rider, C. C. (2006). Heparin/heparan sulphate binding in the TGF-beta cytokine superfamily. Biochem. Soc. Trans. 34, 458-460.
40. Roberts, S., Calautti, E., Vanderweil, S., Nguyen, H. O., Foley, A., Baden, H. P. and Viel, A. (2007). Changes in localization of human discs large (hDlg) during keratinocyte differentiation is associated with expression of alternatively spliced hDlg variants. Exp. Cell Res. 313, 2521-2530.
41. Smola, H., Stark, H. J., Thiekotter, G., Mirancea, N., Krieg, T. and Fusenig, N. E. (1998). Dynamics of basement membrane formation by keratinocyte-fibroblast interactions in organotypic skin culture. Exp. Cell Res. 239, 399-410.
42. Stepp, M. A., Gibson, H. E., Gala, P. H., Iglesia, D. D., Pajoohesh-Ganji, A., Pal-Ghosh, S., Brown, M., Aquino, C., Schwartz, A. M., Goldberger, O. et al. (2002). Defects in keratinocyte activation during wound healing in the syndecan-1-deficient mouse. J. Cell Sci. 115, 4517-4531.
43. Stepp, M. A., Liu, Y., Pal-Ghosh, S., Jurjus, R. A., Tadvalkar, G., Sekaran, A., Losicco, K., Jiang, L., Larsen, M., Li, L. et al. (2007). Reduced migration, altered matrix and enhanced TGFbeta1 signaling are signatures of mouse keratinocytes lacking Sdc1. J. Cell Sci. 120, 2851-2863.
44. Tsuda, M., Kamimura, K., Nakato, H., Archer, M., Staatz, W., Fox, B., Humphrey, M., Olson, S., Futch, T., Kaluza, V. et al. (1999). The cell-surface proteoglycan Dally regulates Wingless signalling in Drosophila. Nature 400, 276-280.
45. Waikel, R. L., Kawachi, Y., Waikel, P. A., Wang, X. J. and Roop, D. R. (2001). Deregulated expression of c-Myc depletes epidermal stem cells. Nat. Genet. 28, 165-168.
46. Wang, T. F., Ding, C. N., Wang, G. S., Luo, S. C., Lin, Y. L., Ruan, Y., Hevner, R., Rubenstein, J. L. and Hsueh, Y. P. (2004). Identification of Tbr-1/CASK complex target genes in neurons. J. Neurochem. 91, 1483-1492.
47. Waseem, A., Dogan, B., Tidman, N., Alam, Y., Purkis, P., Jackson, S., Lalli, A., Machesney, M. and Leigh, I. M. (1999). Keratin 15 expression in stratified epithelia: downregulation in activated keratinocytes. J. Invest. Dermatol. 112, 362-369.
48. Watt, F. M., Lo, Celso, C. and Silva-Vargas, V. (2006). Epidermal stem cells: an update. Curr. Opin. Genet. Dev. 16, 518-524.
49. Werner, S., Krieg, T. and Smola, H. (2007). Keratinocyte-fibroblast interactions in wound healing. J. Invest. Dermatol. 127, 998-1008.
50. Zanet, J., Pibre, S., Jacquet, C., Ramirez, A., de Alboran, I. M. and Gandarillas, A. (2005). Endogenous Myc controls mammalian epidermal cell size, hyperproliferation, endoreplication and stem cell amplification. J. Cell Sci. 118, 1693-1704.