Protein 4.1R regulates cell adhesion, spreading, migration and motility of mouse keratinocytes by modulating surface expression of β1 integrin

Journal of Cell Science

Volumn 124, Issue 14, 2011, Pages 2478-2487

  Chen, Lixiang ^a   Hughes, Richard A ^a   Baines, Anthony J ^b   Conboy, John ^c   Mohandas, Narla ^a   An, Xiuli ^a,d  

^a NEW YORK BLOOD CENTER   (United States)

^b UNIVERSITY OF KENT   (United Kingdom)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^d PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

Author keywords

1 integrin; 4.1R; Cell motility; Keratinocyte

Indexed keywords

ACTIN; ADAPTOR PROTEIN; BETA1 INTEGRIN; FIBRONECTIN; FOCAL ADHESION KINASE; PROTEIN 4.1R; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL CULTURE; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CELL SURFACE; CONTROLLED STUDY; EPIDERMIS; FOCAL ADHESION; IN VITRO STUDY; IN VIVO STUDY; KERATINOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; SKIN; STRESS FIBER; WOUND HEALING;

ACTINS; ANIMALS; ANTIGENS, CD29; CELL ADHESION; CELL MOVEMENT; CYTOSKELETAL PROTEINS; KERATINOCYTES; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; PAXILLIN; PROTEIN ISOFORMS; TALIN; VINCULIN;

MUS;

EID: 79960421243     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.078170     Document Type: Article

References (43)

1. An, X. L., Takakuwa, Y., Manno, S., Han, B. G., Gascard, P. and Mohandas, N. (2001). Structural and functional characterization of protein 4.1R-phosphatidylserine interaction: potential role in 4.1R sorting within cells. J. Biol. Chem. 276, 35778-35785.
2. Binda, A. V., Kabbani, N., Lin, R. and Levenson, R. (2002). D2 and D3 dopamine receptor cell surface localization mediated by interaction with protein 4.1N. Mol. Pharmacol. 62, 507-513.
3. Blanpain, C. and Fuchs, E. (2009). Epidermal homeostasis: a balancing act of stem cells in the skin. Nat. Rev. Mol. Cell Biol. 10, 207-217.
4. Calderwood, D. A., Zent, R., Grant, R., Rees, D. J., Hynes, R. O. and Ginsberg, M. H. (1999). The Talin head domain binds to integrin beta subunit cytoplasmic tails and regulates integrin activation. J. Biol. Chem. 274, 28071-28074.
5. Chishti, A. H., Kim, A. C., Marfatia, S. M., Lutchman, M., Hanspal, M., Jindal, H., Liu, S. C., Low, P. S., Rouleau, G. A., Mohandas, N. et al. (1998). The FERM domain: a unique module involved in the linkage of cytoplasmic proteins to the membrane. Trends Biochem. Sci. 23, 281-282.
6. Danen, E. H., van Rheenen, J., Franken, W., Huveneers, S., Sonneveld, P., Jalink, K. and Sonnenberg, A. (2005). Integrins control motile strategy through a Rho-cofilin pathway. J. Cell Biol. 169, 515-526.
7. Diakowski, W., Grzybek, M. and Sikorski, A. F. (2006). Protein 4.1, a component of the erythrocyte membrane skeleton and its related homologue proteins forming the protein 4.1/FERM superfamily. Folia Histochem. Cytobiol. 44, 231-248.
8. Fuchs, E. (1990). Epidermal differentiation. Curr. Opin. Cell Biol. 2, 1028-1035.
9. Fuchs, E. (1994). Epidermal differentiation and keratin gene expression. Princess Takamatsu Symp. 24, 290-302.
10. Fuchs, E. and Raghavan, S. (2002). Getting under the skin of epidermal morphogenesis. Nat. Rev. Genet. 3, 199-209.
11. Galbraith, C. G., Yamada, K. M. and Galbraith, J. A. (2007). Polymerizing actin fibers position integrins primed to probe for adhesion sites. Science 315, 992-995.
12. Geiger, B. and Bershadsky, A. (2001). Assembly and mechanosensory function of focal contacts. Curr. Opin. Cell Biol. 13, 584-592.
13. Has, C., Herz, C., Zimina, E., Qu, H. Y., He, Y., Zhang, Z. G., Wen, T. T., Gache, Y., Aumailley, M. and Bruckner-Tuderman, L. (2009). Kindlin-1 Is required for RhoGTPase-mediated lamellipodia formation in keratinocytes. Am. J. Pathol. 175, 1442-1452.
14. Herz, C., Aumailley, M., Schulte, C., Schlotzer-Schrehardt, U., Bruckner-Tuderman, L. and Has, C. (2006). Kindlin-1 is a phosphoprotein involved in regulation of polarity, proliferation, and motility of epidermal keratinocytes. J. Biol. Chem. 281, 36082-36090.
15. Huang, S. C., Jagadeeswaran, R., Liu, E. S. and Benz, E. J., Jr (2004). Protein 4.1R, a microtubule-associated protein involved in microtubule aster assembly in mammalian mitotic extract. J. Biol. Chem. 279, 34595-34602.
16. Hubbard, T., Barker, D., Birney, E., Cameron, G., Chen, Y., Clark, L., Cox, T., Cuff, J., Curwen, V., Down, T. et al. (2002). The Ensembl genome database project. Nucleic Acids Res. 30, 38-41.
17. Kang, Q., Wang, T., Zhang, H., Mohandas, N. and An, X. (2009a). A Golgi-associated protein 4.1B variant is required for assimilation of proteins in the membrane. J. Cell Sci. 122, 1091-1099.
18. Kang, Q., Yu, Y., Pei, X., Hughes, R., Heck, S., Zhang, X., Guo, X., Halverson, G., Mohandas, N. and An, X. (2009b). Cytoskeletal protein 4.1R negatively regulates Tcell activation by inhibiting the phosphorylation of LAT. Blood 113, 6128-6137.
19. Kaverina, I., Krylyshkina, O. and Small, J. V. (2002). Regulation of substrate adhesion dynamics during cell motility. Int. J. Biochem. Cell Biol. 34, 746-761.
20. Kirfel, G. and Herzog, V. (2004). Migration of epidermal keratinocytes: mechanisms, regulation, and biological significance. Protoplasma 223, 67-78.
21. Krauss, S. W., Spence, J. R., Bahmanyar, S., Barth, A. I., Go, M. M., Czerwinski, D. and Meyer, A. J. (2008). Downregulation of protein 4.1R, a mature centriole protein, disrupts centrosomes, alters cell cycle progression, and perturbs mitotic spindles and anaphase. Mol. Cell. Biol. 28, 2283-2294.
22. Lu, D., Yan, H., Othman, T. and Rivkees, S. A. (2004a). Cytoskeletal protein 4.1G is a binding partner of the metabotropic glutamate receptor subtype 1 alpha. J. Neurosci. Res. 78, 49-55.
23. Lu, D., Yan, H., Othman, T., Turner, C. P., Woolf, T. and Rivkees, S. A. (2004b). Cytoskeletal protein 4.1G binds to the third intracellular loop of the A1 adenosine receptor and inhibits receptor action. Biochem. J. 377, 51-59.
24. Marfatia, S. M., Leu, R. A., Branton, D. and Chishti, A. H. (1995). Identification of the protein 4.1 binding interface on glycophorin C and p55, a homologue of the Drosophila discs-large tumor suppressor protein. J. Biol. Chem. 270, 715-719.
25. Martin, P. (1997). Wound healing-aiming for perfect skin regeneration. Science 276, 75-81.
26. Maximov, A., Tang, T. S. and Bezprozvanny, I. (2003). Association of the type 1 inositol (1,4,5)-trisphosphate receptor with 4.1N protein in neurons. Mol. Cell. Neurosci. 22, 271-283.
27. McCarty, J. H., Cook, A. A. and Hynes, R. O. (2005). An interaction between {alpha}v{beta}8 integrin and Band 4.1B via a highly conserved region of the Band 4.1 C-terminal domain. Proc. Natl. Acad. Sci. USA 102, 13479-13483.
28. Morgenstern, J. P. and Land, H. (1990). Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res. 18, 3587-3596.
29. Nunomura, W., Takakuwa, Y., Tokimitsu, R., Krauss, S. W., Kawashima, M. and Mohandas, N. (1997). Regulation of CD44-protein 4.1 interaction by Ca2+ and calmodulin. Implications for modulation of CD44-ankyrin interaction. J. Biol. Chem. 272, 30322-30328.
30. Perez-Ferreiro, C. M., Luque, C. M. and Correas, I. (2001). 4.1R proteins associate with interphase microtubules in human T cells: a 4.1R constitutive region is involved in tubulin binding. J. Biol. Chem. 276, 44785-44791.
31. Pollard, T. D. and Borisy, G. G. (2003). Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453-465.
32. Raja, S. K., Garcia, M. S. and Isseroff, R. R. (2007). Wound re-epithelialization: modulating keratinocyte migration in wound healing. Front. Biosci. 12, 2849-2868.
33. Rheinwald, J. G. and Green, H. (1975). Serial cultivation of strains of human epidermal keratinocytes: the formation of keratinizing colonies from single cells. Cell 6, 331-343.
34. Rheinwald, J. G. and Green, H. (1977). Epidermal growth factor and the multiplication of cultured human epidermal keratinocytes. Nature 265, 421-424.
35. Saito, M., Sugai, M., Katsushima, Y., Yanagisawa, T., Sukegawa, J. and Nakahata, N. (2005). Increase in cell-surface localization of parathyroid hormone receptor by cytoskeletal protein 4.1G. Biochem. J. 392, 75-81.
36. Salomao, M., Zhang, X., Yang, Y., Lee, S., Hartwig, J. H., Chasis, J. A., Mohandas, N. and An, X. (2008). Protein 4.1R-dependent multiprotein complex: new insights into the structural organization of the red blood cell membrane. Proc. Natl. Acad. Sci. USA 105, 8026-8031.
37. Shi, Z. T., Afzal, V., Coller, B., Patel, D., Chasis, J. A., Parra, M., Lee, G., Paszty, C., Stevens, M., Walensky, L. et al. (1999). Protein 4.1R-deficient mice are viable but have erythroid membrane skeleton abnormalities. J. Clin. Invest. 103, 331-340.
38. Stagg, M. A., Carter, E., Sohrabi, N., Siedlecka, U., Soppa, G. K., Mead, F., Mohandas, N., Taylor-Harris, P., Baines, A., Bennett, P. et al. (2008). Cytoskeletal protein 4.1R affects repolarization and regulates calcium handling in the heart. Circ. Res. 103, 855-863.
39. Sun, C. X., Robb, V. A. and Gutmann, D. H. (2002). Protein 4.1 tumor suppressors: getting a FERM grip on growth regulation. J. Cell Sci. 115, 3991-4000.
40. Tang, P., Cao, C., Xu, M. and Zhang, L. (2007). Cytoskeletal protein radixin activates integrin alpha(M)beta(2) by binding to its cytoplasmic tail. FEBS Lett. 581, 1103-1108.
41. Taylor-Harris, P. M., Keating, L. A., Maggs, A. M., Phillips, G. W., Birks, E. J., Franklin, R. C., Yacoub, M. H., Baines, A. J. and Pinder, J. C. (2005). Cardiac muscle cell cytoskeletal protein 4.1: analysis of transcripts and subcellular locationrelevance to membrane integrity, microstructure, and possible role in heart failure. Mamm. Genome 16, 137-151.
42. Watt, F. M. (2002). Role of integrins in regulating epidermal adhesion, growth and differentiation. EMBO J. 21, 3919-3926.
43. Yang, S., Guo, X., Debnath, G., Mohandas, N. and An, X. (2009). Protein 4.1R links E-cadherin/beta-catenin complex to the cytoskeleton through its direct interaction with beta-catenin and modulates adherens junction integrity. Biochim. Biophys. Acta 1788, 1458-1465.