Mutations in the paxillin-binding site of Integrin-linked kinase (ILK) destabilize the pseudokinase domain and cause embryonic lethality in mice

Journal of Biological Chemistry

Volumn 288, Issue 26, 2013, Pages 18863-18871

  Moik, Daniel ^a   Bod̈ttcher, Anika ^a   Makhina, Tatiana ^a   Grashoff, Carsten ^a   Bulus, Nada ^b   Zent, Roy ^b,c   Fässler, Reinhard ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b VANDERBILT UNIVERSITY   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMICAL ANALYSIS; DEVELOPMENTAL DELAY; EMBRYONIC LETHALITY; EXTRACELLULAR MATRICES; GLYCINE RESIDUES; GROWTH FACTOR RECEPTORS; INTEGRIN-LINKED KINASE; PROTEIN STABILITY;

ADHESION; AMINO ACIDS; BINDING SITES; CELL CULTURE; DEFECTS; ENZYMES; MAMMALS;

CELL SIGNALING;

ALPHA PARVIN; INTEGRIN LINKED KINASE; MEMBRANE PROTEIN; PAXILLIN; PHOSPHOTRANSFERASE; PSEUDOKINASE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL ADHESION; CELL SPREADING; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; EMBRYO; EMBRYO DEATH; EMBRYO DEVELOPMENT; ENZYME STABILITY; EXTRACELLULAR MATRIX; FEMALE; FIBROBLAST; GENE MUTATION; GERM LINE; IN VITRO STUDY; MIGRATION INHIBITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION;

CELL ADHESION; CELL MIGRATION; DEVELOPMENT; EMBRYONIC DEVELOPMENT; INTEGRIN-LINKED KINASE; PARVIN; PAXILLIN; PINCH; PROTEIN STABILITY; VASCULOGENESIS;

AMINO ACID MOTIFS; ANIMALS; BINDING SITES; CELL ADHESION; CELL MOVEMENT; EMBRYO, MAMMALIAN; FLOW CYTOMETRY; FOCAL ADHESIONS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, LETHAL; MICE; MICROFILAMENT PROTEINS; MUTATION; PAXILLIN; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; TIME FACTORS;

MUS;

EID: 84879561516     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.470476     Document Type: Article

References (41)

1. Wickström, S. A., Radovanac, K., and Fässler, R. (2011) Genetic analyses of integrin signaling. Cold Spring Harb. Perspect. Biol. 3, a005116
2. Lange, A., Wickström, S. A., Jakobson, M., Zent, R., Sainio, K., and Fässler, R. (2009) Integrin-linked kinase is an adaptor with essential functions during mouse development. Nature 461, 1002-1006
3. Widmaier, M., Rognoni, E., Radovanac, K., Azimifar, S. B., and Fässler, R. (2012) Integrin-linked kinase at a glance. J. Cell Sci. 125, 1839-1843
4. Chiswell, B. P., Zhang, R., Murphy, J. W., Boggon, T. J., and Calderwood, D. A. (2008) The structural basis of integrin-linked kinase-PINCH interactions. Proc. Natl. Acad. Sci. U.S.A. 105, 20677-20682
5. Fukuda, K., Gupta, S., Chen, K., Wu, C., and Qin, J. (2009) The pseudoactive site of ILK is essential for its binding to α-Parvin and localization to focal adhesions. Mol. Cell 36, 819-830
6. Stanchi, F., Grashoff, C., Nguemeni Yonga, C. F., Grall, D., Fässler, R., and Van Obberghen-Schilling, E. (2009) Molecular dissection of the ILK-PINCH-parvin triad reveals a fundamental role for the ILK kinase domain in the late stages of focal-adhesion maturation. J. Cell Sci. 122, 1800-1811
7. Fukuda, T., Chen, K., Shi, X., and Wu, C. (2003) PINCH-1 is an obligate partner of integrin-linked kinase (ILK) functioning in cell shape modulation, motility, and survival. J. Biol. Chem. 278, 51324-51333 (Pubitemid 38020371)
8. Zhang, Y., Chen, K., Tu, Y., Velyvis, A., Yang, Y., Qin, J., and Wu, C. (2002) Assembly of the PINCH-ILK-CH-ILKBP complex precedes and is essential for localization of each component to cell-matrix adhesion sites. J. Cell Sci. 115, 4777-4786 (Pubitemid 36054631)
9. Montanez, E., Wickström, S. A., Altstätter, J., Chu, H., and Fässler, R. (2009) α-parvin controls vascular mural cell recruitment to vessel wall by regulating RhoA/ROCK signalling. EMBO J. 28, 3132-3144
10. Boulter, E., Grall, D., Cagnol, S., and Van Obberghen-Schilling, E. (2006) Regulation of cell-matrix adhesion dynamics and Rac-1 by integrin linked kinase. FASEB J. 20, 1489-1491
11. Tu, Y., Li, F., and Wu, C. (1998) Nck-2, a novel Src homology2/3- containing adaptor protein that interacts with the LIM-only protein PINCH and components of growth factor receptor kinase-signaling pathways. Mol. Biol. Cell 9, 3367-3382 (Pubitemid 28551035)
12. Azimifar, S. B., Böttcher, R. T., Zanivan, S., Grashoff, C., Krüger, M., Legate, K. R., Mann, M., and Fässler, R. (2012) Induction of membrane circular dorsal ruffles requires co-signalling of integrin-ILK-complex and EGF receptor. J. Cell Sci. 125, 435-448
13. Sakai, T., Li, S., Docheva, D., Grashoff, C., Sakai, K., Kostka, G., Braun, A., Pfeifer, A., Yurchenco, P. D., and Fässler, R. (2003) Integrin-linked kinase (ILK) is required for polarizing the epiblast, cell adhesion, and controlling actin accumulation. Genes Dev. 17, 926-940 (Pubitemid 36397379)
14. Lorenz, K., Grashoff, C., Torka, R., Sakai, T., Langbein, L., Bloch, W., Aumailley, M., and Fässler, R. (2007) Integrin-linked kinase is required for epidermal and hair follicle morphogenesis. J. Cell Biol. 177, 501-513 (Pubitemid 46718278)
15. Wickström, S. A., Lange, A., Hess, M. W., Polleux, J., Spatz, J. P., Krüger, M., Pfaller, K., Lambacher, A., Bloch, W., Mann, M., Huber, L. A., and Fässler, R. (2010) Integrin-linked kinase controls microtubule dynamics required for plasma membrane targeting of caveolae. Dev. Cell 19, 574-588
16. Friedrich, E. B., Liu, E., Sinha, S., Cook, S., Milstone, D. S., MacRae, C. A., Mariotti, M., Kuhlencordt, P. J., Force, T., Rosenzweig, A., St-Arnaud, R., Dedhar, S., and Gerszten, R. E. (2004) Integrin-linked kinase regulates endothelial cell survival and vascular development. Mol. Cell. Biol. 24, 8134-8144 (Pubitemid 39167462)
17. Deakin, N. O., and Turner, C. E. (2008) Paxillin comes of age. J. Cell Sci. 121, 2435-2444
18. Hagel, M., George, E. L., Kim, A., Tamimi, R., Opitz, S. L., Turner, C. E., Imamoto, A., and Thomas, S. M. (2002) The adaptor protein paxillin is essential for normal development in the mouse and is a critical transducer of fibronectin signaling. Mol. Cell. Biol. 22, 901-915 (Pubitemid 34053067)
19. Wade, R., Bohl, J., and Vande Pol, S. (2002) Paxillin null embryonic stem cells are impaired in cell spreading and tyrosine phosphorylation of focal adhesion kinase. Oncogene 21, 96-107 (Pubitemid 34076382)
20. Nikolopoulos, S. N., and Turner, C. E. (2001) Integrin-linked kinase (ILK) binding to paxillin LD1 motif regulates ILK localization to focal adhesions. J. Biol. Chem. 276, 23499-23505
21. Nikolopoulos, S. N., and Turner, C. E. (2002) Molecular dissection of actopaxin-integrin-linked kinase-Paxillin interactions and their role in subcellular localization. J. Biol. Chem. 277, 1568-1575 (Pubitemid 34968915)
22. Stiegler, A. L., Draheim, K. M., Li, X., Chayen, N. E., Calderwood, D. A., and Boggon, T. J. (2012) Structural Basis for Paxillin Binding and Focal Adhesion Targeting of β-Parvin. J. Biol. Chem. 287, 32566-32577
23. Lorenz, S., Vakonakis, I., Lowe, E. D., Campbell, I. D., Noble, M. E., and Hoellerer, M. K. (2008) Structural analysis of the interactions between paxillin LD motifs and α-parvin. Structure 16, 1521-1531
24. Wang, X., Fukuda, K., Byeon, I. J., Velyvis, A., Wu, C., Gronenborn, A., and Qin, J. (2008) The structure of α-parvin CH2-paxillin LD1 complex reveals a novel modular recognition for focal adhesion assembly. J. Biol. Chem. 283, 21113-21119
25. Gao, G., Prutzman, K. C., King, M. L., Scheswohl, D. M., DeRose, E. F., London, R. E., Schaller, M. D., and Campbell, S. L. (2004) NMR solution structure of the focal adhesion targeting domain of focal adhesion kinase in complex with a paxillin LD peptide: evidence for a two-site binding model. J. Biol. Chem. 279, 8441-8451 (Pubitemid 38294737)
26. Fässler, R., and Meyer, M. (1995) Consequences of lack of β1 integrin gene expression in mice. Genes Dev. 9, 1896-1908
27. Betz, U. A., Vosshenrich, C. A., Rajewsky, K., and Müller, W. (1996) Bypass of lethality with mosaic mice generated by Cre-loxP-mediated recombination. Curr. Biol. 6, 1307-1316 (Pubitemid 27004916)
28. Jat, P. S., and Sharp, P. A. (1986) Large T antigens of simian virus 40 and polyomavirus efficiently establish primary fibroblasts. J. Virol. 59, 746-750 (Pubitemid 16011141)
29. Li, M. Z., and Elledge, S. J. (2007) Harnessing homologous recombination in vitro to generate recombinant DNA via SLIC. Nat. Methods 4, 251-256 (Pubitemid 46358876)
30. Mátés, L., Chuah, M. K., Belay, E., Jerchow, B., Manoj, N., Acosta-Sanchez, A., Grzela, D. P., Schmitt, A., Becker, K., Matrai, J., Ma, L., Samara-Kuko, E., Gysemans, C., Pryputniewicz, D., Miskey, C., Fletcher, B., Vanden-Driessche, T., Ivics, Z., and Izsvák, Z. (2009) Molecular evolution of a novel hyperactive Sleeping Beauty transposase enables robust stable gene transfer in vertebrates. Nat. Genet. 41, 753-761
31. Moik, D. V., Janbandhu, V. C., and Fässler, R. (2011) Loss of migfilin expression has no overt consequences on murine development and homeostasis. J. Cell Sci. 124, 414-421
32. Schneider, C. A., Rasband, W. S., and Eliceiri, K. W. (2012) NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675
33. Chen, D., Roberts, R., Pohl, M., Nigam, S., Kreidberg, J., Wang, Z., Heino, J., Ivaska, J., Coffa, S., Harris, R. C., Pozzi, A., and Zent, R. (2004) Differential expression of collagen- and laminin-binding integrins mediates ureteric bud and inner medullary collecting duct cell tubulogenesis. Am. J. Physiol. Renal Physiol. 287, F602-611 (Pubitemid 39280493)
34. Meyer, M., Müller, A. K., Yang, J., Moik, D., Ponzio, G., Ornitz, D. M., Grose, R., and Werner, S. (2012) FGF receptors 1 and 2 are key regulators of keratinocyte migration in vitro and in wounded skin. J. Cell Sci. 125, 5690-5701
35. Theiler, K. (1989) The House Mouse: Atlas of Embryonic Development, pp. 26-112 Springer-Verlag, New York
36. Schmidt, A., Brixius, K., and Bloch, W. (2007) Endothelial precursor cell migration during vasculogenesis. Circ. Res. 101, 125-136 (Pubitemid 47196580)
37. Aoyagi, Y., Fujita, N., and Tsuruo, T. (2005) Stabilization of integrin-linked kinase by binding to Hsp90. Biochem. Biophys. Res. Commun. 331, 1061-1068 (Pubitemid 40692468)
38. Dickson, M. C., Martin, J. S., Cousins, F. M., Kulkarni, A. B., Karlsson, S., and Akhurst, R. J. (1995) Defective haematopoiesis and vasculogenesis in transforming growth factor-β 1 knock out mice. Development 121, 1845-1854
39. Martin, J. S., Dickson, M. C., Cousins, F. M., Kulkarni, A. B., Karlsson, S., and Akhurst, R. J. (1995) Analysis of homozygous TGF β1 null mouse embryos demonstrates defects in yolk sac vasculogenesis and hematopoiesis. Ann. N.Y. Acad. Sci. 752, 300-308
40. Oshima, M., Oshima, H., and Taketo, M. M. (1996) TGF-β receptor type II deficiency results in defects of yolk sac hematopoiesis and vasculogenesis. Dev. Biol. 179, 297-302 (Pubitemid 26363265)
41. Radovanac, K., Morgner, J., Schulz, J. N., Blumbach, K., Patterson, C., Geiger, T., Mann, M., Krieg, T., Eckes, B., Fässler, R., and Wickström, S. A. (2013) Stabilization of integrin-linked kinase by the Hsp90-CHIP axis impacts cellular force generation, migration and the fibrotic response. EMBO J. 32, 1409-1424