Zasp regulates integrin activation

Journal of Cell Science

Volumn 125, Issue 23, 2012, Pages 5647-5657

  Bouaouina, Mohamed ^a   Jani, Klodiana ^b   Long, Jenny Y ^a   Czerniecki, Stefan ^c   Morse, Elizabeth M ^a   Ellis, Stephanie J ^c   Tanentzapf, Guy ^c   Schöck, Frieder ^a,b   Calderwood, David A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Adhesion receptor; Extracellular matrix; Integrin activation; Muscle attachment; PDZ domain protein; Zasp

Indexed keywords

INTEGRIN; MEMBRANE PROTEIN; PDZ MOTIF CONTAINING PROTEIN; TALIN; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 5;

ANIMAL CELL; ARTICLE; BINDING KINETICS; CARDIOMYOPATHY; CHO CELL; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; MUSCLE CONTRACTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FUNCTION; TISSUE CULTURE;

ANIMALS; CARRIER PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; EXTRACELLULAR MATRIX; HUMANS; INTEGRIN ALPHA5BETA1; INTEGRINS; MUSCLE, SKELETAL; MYOCARDIUM; TALIN;

EID: 84874716470     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.103291     Document Type: Article

References (58)

1. Arimura, T., Hayashi, T., Terada, H., Lee, S. Y., Zhou, Q., Takahashi, M., Ueda, K., Nouchi, T., Hohda, S., Shibutani, M. et al. (2004). A Cypher/ZASP mutation associated with dilated cardiomyopathy alters the binding affinity to protein kinase C. J. Biol. Chem. 279, 6746-6752.
2. Bai, J., Binari, R., Ni, J. Q., Vijayakanthan, M., Li, H. S. and Perrimon, N. (2008). RNA interference screening in Drosophila primary cells for genes involved in muscle assembly and maintenance. Development 135, 1439-1449.
3. Barrett, J. S., Yu, J., Kapil, R., Padovani, P., Brown, F., Ebling, W. F., Corjay, M. H., Reilly, T. M., Bozarth, J. M., Mousa, S. A. et al. (1999). Disposition and exposure of the fibrinogen receptor antagonist XV459 on alphaIIBbeta3 binding sites in the guinea pig. Biopharm. Drug Dispos. 20, 309-318.
4. Bouaouina, M. and Calderwood, D. A. (2011). Kindlins. Curr. Biol. 21, R99-R101.
5. Bouaouina, M., Lad, Y. and Calderwood, D. A. (2008). The N-terminal domains of talin cooperate with the phosphotyrosine binding-like domain to activate beta1 and beta3 integrins. J. Biol. Chem. 283, 6118-6125.
6. Bouaouina, M., Harburger, D. S. and Calderwood, D. A. (2012). Talin and signaling through integrins. Methods Mol. Biol. 757, 325-347.
7. Brower, D. L., Wilcox, M., Piovant, M., Smith, R. J. and Reger, L. A. (1984). Related cell-surface antigens expressed with positional specificity in Drosophila imaginal discs. Proc. Natl. Acad. Sci. USA 81, 7485-7489.
8. Brown, P. J. and Juliano, R. L. (1985). Selective inhibition of fibronectin-mediated cell adhesion by monoclonal antibodies to a cell-surface glycoprotein. Science 228, 1448-1451.
9. Brown, N. H., Gregory, S. L., Rickoll, W. L., Fessler, L. I., Prout, M., White, R. A. and Fristrom, J. W. (2002). Talin is essential for integrin function in Drosophila. Dev. Cell 3, 569-579.
10. Calderwood, D. A. (2004). Integrin activation. J. Cell Sci. 117, 657-666.
11. Cheng, H., Kimura, K., Peter, A. K., Cui, L., Ouyang, K., Shen, T., Liu, Y., Gu, Y., Dalton, N. D., Evans, S. M. et al. (2010). Loss of enigma homolog protein results in dilated cardiomyopathy. Circ. Res. 107, 348-356.
12. Chu, P. H., Bardwell, W. M., Gu, Y., Ross, J., Jr and Chen, J. (2000). FHL2 (SLIM3) is not essential for cardiac development and function. Mol. Cell. Biol. 20, 7460-7462.
13. Czuchra, A., Meyer, H., Legate, K. R., Brakebusch, C. and Fässler, R. (2006). Genetic analysis of beta1 integrin "activation motifs"in mice. J. Cell Biol. 174, 889-899.
14. Ellis, S. J., Pines, M., Fairchild, M. J. and Tanentzapf, G. (2011). In vivo functional analysis reveals specific roles for the integrin-binding sites of talin. J. Cell Sci. 124, 1844-1856.
15. Faulkner, G., Pallavicini, A., Formentin, E., Comelli, A., Ievolella, C., Trevisan, S., Bortoletto, G., Scannapieco, P., Salamon, M., Mouly, V. et al. (1999). ZASP: a new Z-band alternatively spliced PDZ-motif protein. J. Cell Biol. 146, 465-475.
16. Fogerty, F. J., Fessler, L. I., Bunch, T. A., Yaron, Y., Parker, C. G., Nelson, R. E., Brower, D. L., Gullberg, D. and Fessler, J. H. (1994). Tiggrin, a novel Drosophila extracellular matrix protein that functions as a ligand for Drosophila alpha PS2 beta PS integrins. Development 120, 1747-1758.
17. Goult, B. T., Bouaouina, M., Harburger, D. S., Bate, N., Patel, B., Anthis, N. J., Campbell, I. D., Calderwood, D. A., Barsukov, I. L., Roberts, G. C. et al. (2009). The structure of the N-terminus of kindlin-1: a domain important for alphaiibbeta3 integrin activation. J. Mol. Biol. 394, 944-956.
18. Han, J., Lim, C. J., Watanabe, N., Soriani, A., Ratnikov, B., Calderwood, D. A., Puzon-McLaughlin, W., Lafuente, E. M., Boussiotis, V. A., Shattil, S. J. et al. (2006). Reconstructing and deconstructing agonist-induced activation of integrin alphaIIbbeta3. Curr. Biol. 16, 1796-1806.
19. Harburger, D. S. and Calderwood, D. A. (2009). Integrin signalling at a glance. J. Cell Sci. 122, 159-163.
20. Harburger, D. S., Bouaouina, M. and Calderwood, D. A. (2009). Kindlin-1 and -2 directly bind the C-terminal region of beta integrin cytoplasmic tails and exert integrin-specific activation effects. J. Biol. Chem. 284, 11485-11497.
21. Heckmann, D., Meyer, A., Marinelli, L., Zahn, G., Stragies, R. and Kessler, H. (2007). Probing integrin selectivity: rational design of highly active and selectiveligands for the alpha5beta1 and alphavbeta3 integrin receptor. Angew. Chem. Int. Ed. Engl. 46, 3571-3574.
22. Huang, C., Zhou, Q., Liang, P., Hollander, M. S., Sheikh, F., Li, X., Greaser, M., Shelton, G. D., Evans, S. and Chen, J. (2003). Characterization and in vivo functional analysis of splice variants of cypher. J. Biol. Chem. 278, 7360-7365.
23. Jani, K. and Schöck, F. (2007). Zasp is required for the assembly of functional integrin adhesion sites. J. Cell Biol. 179, 1583-1597.
24. Katzemich, A., Long, J. Y., Jani, K., Lee, B. R. and Schöck, F. (2011). Muscle typespecific expression of Zasp52 isoforms in Drosophila. Gene Expr. Patterns 11, 484-490.
25. Kendall, T., Mukai, L., Jannuzi, A. L. and Bunch, T. A. (2011). Identification of integrin beta subunit mutations that alter affinity for extracellular matrix ligand. J. Biol. Chem. 286, 30981-30993.
26. Kim, C., Ye, F., Hu, X. and Ginsberg, M. H. (2012). Talin activates integrins by altering the topology of the b transmembrane domain. J. Cell Biol. 197, 605-611.
27. Lad, Y., Harburger, D. S. and Calderwood, D. A. (2007). Integrin cytoskeletal interactions. Methods Enzymol. 426, 69-84.
28. Lee, H. S., Lim, C. J., Puzon-McLaughlin, W., Shattil, S. J. and Ginsberg, M. H. (2009). RIAM activates integrins by linking talin to ras GTPase membrane-targeting sequences. J. Biol. Chem. 284, 5119-5127.
29. Loughran, G., Healy, N. C., Kiely, P. A., Huigsloot, M., Kedersha, N. L. and O'Connor, R. (2005). Mystique is a new insulin-like growth factor-I-regulated PDZLIM domain protein that promotes cell attachment and migration and suppresses Anchorage-independent growth. Mol. Biol. Cell 16, 1811-1822.
30. Luo, B. H., Carman, C. V. and Springer, T. A. (2007). Structural basis of integrin regulation and signaling. Annu. Rev. Immunol. 25, 619-647.
31. Ma, Y. Q., Qin, J., Wu, C. and Plow, E. F. (2008). Kindlin-2 (Mig-2): a co-activator of beta3 integrins. J. Cell Biol. 181, 439-446.
32. Manevich-Mendelson, E., Grabovsky, V., Feigelson, S. W., Cinamon, G., Gore, Y., Goverse, G., Monkley, S. J., Margalit, R., Melamed, D., Mebius, R. E. et al. (2010). Talin1 is required for integrin-dependent B lymphocyte homing to lymph nodes and the bone marrow but not for follicular B-cell maturation in the spleen. Blood 116, 5907-5918.
33. Martin-Bermudo, M. D., Dunin-Borkowski, O. M. and Brown, N. H. (1998). Modulation of integrin activity is vital for morphogenesis. J. Cell Biol. 141, 1073-1081.
34. Meves, A., Stremmel, C., Gottschalk, K. and Fässler, R. (2009). The Kindlin protein family: new members to the club of focal adhesion proteins. Trends Cell Biol. 19, 504-513.
35. Millon-Frémillon, A., Bouvard, D., Grichine, A., Manet-Dupé, S., Block, M. R. and Albiges-Rizo, C. (2008). Cell adaptive response to extracellular matrix density is controlled by ICAP-1-dependent beta1-integrin affinity. J. Cell Biol. 180, 427-441.
36. Montanez, E., Ussar, S., Schifferer, M., Bösl, M., Zent, R., Moser, M. and Fässler, R. (2008). Kindlin-2 controls bidirectional signaling of integrins. Genes Dev. 22, 1325-1330.
37. Moser, M., Nieswandt, B., Ussar, S., Pozgajova, M. and Fässler, R. (2008). Kindlin-3 is essential for integrin activation and platelet aggregation. Nat. Med. 14, 325-330.
38. Moser, M., Bauer, M., Schmid, S., Ruppert, R., Schmidt, S., Sixt, M., Wang, H. V., Sperandio, M. and Fässler, R. (2009a). Kindlin-3 is required for beta2 integrinmediated leukocyte adhesion to endothelial cells. Nat. Med. 15, 300-305.
39. Moser, M., Legate, K. R., Zent, R. and Fässler, R. (2009b). The tail of integrins, talin, and kindlins. Science 324, 895-899.
40. O'Toole, T. E., Katagiri, Y., Faull, R. J., Peter, K., Tamura, R., Quaranta, V., Loftus, J. C., Shattil, S. J. and Ginsberg, M. H. (1994). Integrin cytoplasmic domains mediate inside-out signal transduction. J. Cell Biol. 124, 1047-1059.
41. Pines, M., Fairchild, M. J. and Tanentzapf, G. (2011). Distinct regulatory mechanisms control integrin adhesive processes during tissue morphogenesis. Dev. Dyn. 240, 36-51.
42. Samson, T., Smyth, N., Janetzky, S., Wendler, O., Mü ller, J. M., Schü le, R., von der Mark, H., von der Mark, K. and Wixler, V. (2004). The LIM-only proteins FHL2 and FHL3 interact with alpha- and beta-subunits of the muscle alpha7beta1 integrin receptor. J. Biol. Chem. 279, 28641-28652.
43. Shattil, S. J., Kim, C. and Ginsberg, M. H. (2010). The final steps of integrin activation: the end game. Nat. Rev. Mol. Cell Biol. 11, 288-300.
44. Sheikh, F., Bang, M. L., Lange, S. and Chen, J. (2007). "Z"eroing in on the role of Cypher in striated muscle function, signaling, and human disease. Trends Cardiovasc. Med. 17, 258-262.
45. Sparrow, J. C. and Schöck, F. (2009). The initial steps of myofibril assembly: integrins pave the way. Nat. Rev. Mol. Cell Biol. 10, 293-298.
46. Tadokoro, S., Shattil, S. J., Eto, K., Tai, V., Liddington, R. C., de Pereda, J. M., Ginsberg, M. H. and Calderwood, D. A. (2003). Talin binding to integrin beta tails: a final common step in integrin activation. Science 302, 103-106.
47. Tanentzapf, G. and Brown, N. H. (2006). An interaction between integrin and the talin FERM domain mediates integrin activation but not linkage to the cytoskeleton. Nat. Cell Biol. 8, 601-606.
48. Tanentzapf, G., Martin-Bermudo, M. D., Hicks, M. S. and Brown, N. H. (2006). Multiple factors contribute to integrin-talin interactions in vivo. J. Cell Sci. 119, 1632-1644.
49. Te Velthuis, A. J., Isogai, T., Gerrits, L. and Bagowski, C. P. (2007). Insights into the molecular evolution of the PDZ/LIM family and identification of a novel conserved protein motif. PLoS ONE 2, e189.
50. Ussar, S., Moser, M., Widmaier, M., Rognoni, E., Harrer, C., Genzel-Boroviczeny, O. and Fässler, R. (2008). Loss of Kindlin-1 causes skin atrophy and lethal neonatal intestinal epithelial dysfunction. PLoS Genet. 4, e1000289.
51. van der Meer, D. L., Marques, I. J., Leito, J. T., Besser, J., Bakkers, J., Schoonheere, E. and Bagowski, C. P. (2006). Zebrafish cypher is important for somite formation and heart development. Dev. Biol. 299, 356-372.
52. Vatta, M., Mohapatra, B., Jimenez, S., Sanchez, X., Faulkner, G., Perles, Z., Sinagra, G., Lin, J. H., Vu, T. M., Zhou, Q. et al. (2003). Mutations in Cypher/ ZASP in patients with dilated cardiomyopathy and left ventricular non-compaction. J. Am. Coll. Cardiol. 42, 2014-2027.
53. Wixler, V., Geerts, D., Laplantine, E., Westhoff, D., Smyth, N., Aumailley, M., Sonnenberg, A. and Paulsson, M. (2000). The LIM-only protein DRAL/FHL2 binds to the cytoplasmic domain of several alpha and beta integrin chains and is recruited to adhesion complexes. J. Biol. Chem. 275, 33669-33678.
54. Ye, F. and Petrich, B. G. (2011). Kindlin: helper, co-activator, or booster of talin in integrin activation? Curr. Opin. Hematol. 18, 356-360.
55. Ye, F., Hu, G., Taylor, D., Ratnikov, B., Bobkov, A. A., McLean, M. A., Sligar, S. G., Taylor, K. A. and Ginsberg, M. H. (2010). Recreation of the terminal events in physiological integrin activation. J. Cell Biol. 188, 157-173.
56. Yuan, L., Fairchild, M. J., Perkins, A. D. and Tanentzapf, G. (2010). Analysis of integrin turnover in fly myotendinous junctions. J. Cell Sci. 123, 939-946.
57. Zhou, Q., Ruiz-Lozano, P., Martone, M. E. and Chen, J. (1999). Cypher, a striated muscle-restricted PDZ and LIM domain-containing protein, binds to alpha-actinin-2 and protein kinase C. J. Biol. Chem. 274, 19807-19813.
58. Zhou, Q., Chu, P. H., Huang, C., Cheng, C. F., Martone, M. E., Knoll, G., Shelton, G. D., Evans, S. and Chen, J. (2001). Ablation of Cypher, a PDZ-LIM domain Z-line protein, causes a severe form of congenital myopathy. J. Cell Biol. 155, 605-612.