Kindlin binds migfilin tandem LIM domains and regulates migfilin focal adhesion localization and recruitment dynamics

Journal of Biological Chemistry

Volumn 288, Issue 49, 2013, Pages 35569-35580

  Brahme, Nina N ^a   Harburger, David S ^a   Kemp O'Brien, Karl ^b   Stewart, Rachel ^a   Raghavan, Srikala ^a,c   Parsons, Maddy ^b   Calderwood, David A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c Institute for Stem Cell Biology and Regenerative Medicine   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION;

FOCAL ADHESIONS; IN-CONTROL; INTEGRINS; LIM DOMAIN; SUBCELLULAR LOCALIZATIONS;

BINS;

ACTIN; FOCAL ADHESION KINASE; KINDLIN 1 PROTEIN; KINDLIN 2 PROTEIN; KINDLIN PROTEIN; LIM PROTEIN; MIGFILIN PROTEIN; UNCLASSIFIED DRUG; CELL ADHESION MOLECULE; CYTOSKELETON PROTEIN; FBLIM1 PROTEIN, MOUSE; FERMT1 PROTEIN, HUMAN; KINDLIN-2 PROTEIN, MOUSE; MEMBRANE PROTEIN; MUSCLE PROTEIN; PROTEIN BINDING; TUMOR PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL ADHESION; CELL KINETICS; CELL MIGRATION; CELL MOTILITY; CELL SPREADING; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME LOCALIZATION; ENZYME REGULATION; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; FLUORESCENCE RESONANCE ENERGY TRANSFER; FOCAL ADHESION; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN TARGETING; REGULATORY MECHANISM; STRESS FIBER; 3T3 CELL LINE; ANIMAL; CELL CULTURE; DEFICIENCY; GENE INACTIVATION; GENETICS; HUMAN; KERATINOCYTE; METABOLISM; MOUSE; PROTEIN TERTIARY STRUCTURE;

ANIMALS; CELL ADHESION MOLECULES; CELLS, CULTURED; CYTOSKELETAL PROTEINS; FLUORESCENCE RESONANCE ENERGY TRANSFER; FOCAL ADHESIONS; GENE KNOCKOUT TECHNIQUES; HUMANS; KERATINOCYTES; MEMBRANE PROTEINS; MICE; MUSCLE PROTEINS; NEOPLASM PROTEINS; NIH 3T3 CELLS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

EID: 84894328272     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.483016     Document Type: Article

References (57)

1. Rodgers, A. J., and Wilce, M. C. (2000) Structure of the - complex of ATP synthase. Nat. Struct. Biol. 7, 1051-1054
2. Pebay-Peyroula, E., Dahout-Gonzalez, C., Kahn, R., Trézé guet, V., Lauquin, G. J., and Brandolin, G. (2003) Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside. Nature 426, 39-44
3. Trentham, D. R., Eccleston, J. F., and Bagshaw, C. R (1976) Kinetic analysis of ATPase mechanisms. Q. Rev. Biophys. 9, 217-281
4. Miller, D. L., and Westheimer, F.H(1966) The hydrolysis of -phenylpropyl di- and triphosphates. J. Am. Chem. Soc. 88, 1507-1511
5. Schwarzl, S. M (2006) Understanding the ATP Hydrolysis Mechanism in Myosin Using Computer Simulation Techniques, Ph.D. thesis, Ruprecht- Karls University of Heidelberg
6. Brooks, B. R., Bruccoleri, R. E., Olafson, B. D., States, D. J., Swaminathan, S., and Karplus, M. (1983) CHARMM: A program for macromolecular energy, minimization, and dynamics calculations. J. Comput. Chem. 4, 187-217
7. Boyer, P. D (2003) Nobel Lectures, Chemistry, 1996-2000, p. 120, World Scientific Publishing, Singapore
8. Kull, F. J., Sablin, E. P., Lau, R., Fletterick, R. J., and Vale, R.D(1996) Crystal structure of the kinesin motor domain reveals a structural similarity to myosin. Nature 380, 550-555
9. Vale, R. D. (1996) Switches, latches, and amplifiers. Common themes of G proteins and molecular motors. J. Cell Biol. 135, 291-302
10. Howard, J., Hudspeth, A. J., and Vale, R. D. (1989) Movement of microtubules by single kinesin molecules. Nature 342, 154-158
11. Block, S. M., Goldstein, L. S., and Schnapp, B. J. (1990) Bead movement by single kinesin molecules studied with optical tweezers. Nature 348, 348-352
12. Finer, J. T., Simmons, R. M., and Spudich, J. A. (1994) Single myosin molecule mechanics. Piconewton forces and nanometre steps. Nature 368, 113-119
13. Li, G., and Cui, Q. (2004) Mechanochemical coupling in myosin. A theoretical analysis with molecular dynamics and combined QM/MM reaction path calculations. J. Phys. Chem. B 108, 3342-3357
14. Yu, H., Ma, L., Yang, Y., and Cui, Q. (2007) Mechanochemical coupling in the myosin motor domain. I. Insights from equilibrium active-site simulations. PLoS Comput. Biol. 3, e21
15. Hayashi, S., Ueno, H., Shaikh, A. R., Umemura, M., Kamiya, M., Ito, Y., Ikeguchi, M., Komoriya, Y., Iino, R., and Noji, H. (2012) Molecular mechanism of ATP hydrolysis in F1-ATPase revealed by molecular simulations and single-molecule observations. J. Am. Chem. Soc. 134, 8447-8454
16. Grigorenko B. L., Rogov, A. V., Topol, I. A., Burt, S. K., Martinez, H. M., and Nemukhin, A. V. (2007) Mechanism of the myosin catalyzed hydrolysis of ATP as rationalized by molecular modeling. Proc. Natl. Acad. Sci. U.S.A. 104, 7057-7061
17. Grigorenko, B. L., Kaliman, I. A., and Nemukhin, A. V. (2011) Minimum energy reaction profiles for ATP hydrolysis in myosin. J. Mol. Graph. Model. 31, 1-4
18. McGrath, M. J., Kuo, I.-F., Hayashi, S., and Takada, S. (2013) Adenosine triphosphate hydrolysis mechanism in kinesin studied by combined quantum- mechanical/molecular-mechanical metadynamics simulations. J. Am. Chem. Soc. 135, 8908-8919
19. Akola, J., and Jones, R. O. (2003) ATP hydrolysis in water: A density functional study. J. Phys. Chem. B 107, 11774-11783
20. Lymn, R. W., and Taylor, E. W. (1971) Mechanism of adenosine triphosphate hydrolysis by actomyosin. Biochemistry 10, 4617-4624
21. Rayment, I., Holden, H. M., Whittaker, M., Yohn, C. B., Lorenz, M., Holmes, K. C., Milligan, R. A. (1993) Structure of the actin-myosin complex and its implications for muscle contraction. Science 261, 58-65
22. Kuhner, S., and Fischer, S. (2011) Structural mechanism of the ATP-induced dissociation of rigor myosin from actin. Proc. Natl. Acad. Sci. U.S.A. 108, 7793-7798
23. Koppole, S., Smith, J. C., and Fischer, S. (2007) The structural coupling between ATPase activation and recovery stroke in the myosin II motor. Structure 15, 825-837
24. Yang, Y., Yu, H., and Cui, Q. (2008) Extensive conformational transitions are required to turn on ATP hydrolysis in myosin. J. Mol. Biol. 381, 1407-1420
25. Schwarzl, S. M., Smith, J. C., and Fischer, S. (2006) Insights into the chemomechanical coupling of the myosin motor from simulation of its ATPase mechanism. Biochemistry 45, 5830-5847
26. Smith, C. A., and Rayment, I. (1996) X-ray structure of the magnesium(II)-ADP-vanadate complex of the Dictyostelium discoideum myosin motor domain to 1.9 Å resolution. Biochemistry 35, 5404-5417
27. Schwarzl, S. M., Huang, D., Smith, J. C., and Fischer, S. (2005) Nonuniform charge scaling (NUCS). A practical approximation of solvent electrostatic screening in proteins. J. Comput. Chem. 26, 1359-1371
28. Becke, A. D. (1993) Density-functional thermochemistry. III. The role of exact exchange. J. Chem. Phys. 98, 5648-5652
29. Lee, C., Yang, W., and Parr, R. G. (1988) Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density. Phys. Rev. B 37, 785-789
30. Neria, E., Fischer, S., and Karplus, M. (1996) Simulation of activation free energies in molecular systems. J. Chem. Phys. 105, 1902-1921
31. MacKerell, A. D., Jr., Bashford, D., Bellott, M., Dunbrack, R. L., Jr., Evanseck, J. D., Field, M. J., Fischer, S., Gao, J., Guo, H., Ha, S., Joseph- McCarthy, D., Kuchnir, L., Kuczera, K., Lau, F. T. K., Mattos, C., Michnick, S., Ngo, T., Nguyen, D. T., Prodhom, B., Reiher, W. E., III, Roux, B., Schlenkrich, M., Smith, J. C., Stote, R., Straub, J., Watanabe, M., Wiorkiewicz- Kuczera, J., Yin, D., and Karplus, M. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 102, 3586-3616
32. Field, M. J., Bash, P. A., and Karplus, M. (1990) A combined quantummechanical and molecular mechanical potential for molecular-dynamics simulations. J. Comput. Chem. 11, 700-733
33. Gao, J. (1996) Methods and applications of combined quantum mechanical and molecular mechanical potentials. in Reviews in Computational Chemistry, Vol. 7 (Lipkowitz, K. B., and Boyd, D. B., eds) pp. 119-185, John Wiley & Sons, Inc., Hoboken, NJ
34. Roux, B., and Karplus, M. (1991) Ion transport in a model gramicidin channel. Structure and thermodynamics. Biophys. J. 59, 961-981
35. Van Belle, D., Couplet, I., Prevost, M., and Wodak, S. J. (1987) Calculations of electrostatic properties in proteins. Analysis of contributions from induced protein dipoles. J. Mol. Biol. 198, 721-735
36. Lybrand, T. P., and Kollman, P. A. (1985) Water-water and water-ion potential functions including terms for many body effects. J. Phys. Chem. 83, 2923-2933
37. Guo, H., Gresh, N., Roques, B. P., and Salahub, D. R. (2000) Many-body effects in systems of peptide hydrogen-bonded networks and their contributions to ligand binding. A comparison of the performances of DFT and polarizable molecular mechanics. J. Phys. Chem. B 104, 9746-9754
38. Ahlrichs, R., Bar, M., Haser, M., Horn, H., and Kolmel, C. (1989) Electronic structure calculations on workstation computers: The program system turbomole. Chem. Phys. Lett. 162, 165-169
39. Brooks, B. R., Brooks, C. L., 3rd, Mackerell, A. D., Jr., Nilsson, L., Petrella, R. J., Roux, B., Won, Y., Archontis, G., Bartels, C., Boresch, S., Caflisch, A., Caves, L., Cui, Q., Dinner, A. R., Feig, M., Fischer, S., Gao, J., Hodoscek, M., Im, W., Kuczera, K., Lazaridis, T., Ma, J., Ovchinnikov, V., Paci, E., Pastor, R. W., Post, C. B., Pu, J. Z., Schaefer, M., Tidor, B., Venable, R. M., Woodcock, H. L., Wu, X., Yang, W., York, D. M., and Karplus, M. (2009) CHARMM. The biomolecular simulation program. J. Comput. Chem. 30, 1545-1614
40. Fischer, S., and Karplus, M. (1992) Conjugate peak refinement: An algorithm for finding reaction paths and accurate transition states in systems with many degrees of freedom. Chem. Phys. Lett. 194, 252-261
41. Furch, M., Fujita-Becker, S., Geeves, M. A., Holmes, K. C., and Manstein, D. J. (1999) Role of the salt-bridge between switch-1 and switch-2 of Dictyostelium myosin. J. Mol. Biol. 290, 797-809
42. Onishi, H., Kojima, S., Katoh, K., Fujiwara, K., Martinez, H. M., and Morales, M. F. (1998) Functional transitions in myosin. Formation of a critical salt-bridge and transmission of effect to the sensitive tryptophan. Proc. Natl. Acad. Sci. U.S.A. 95, 6653-6658
43. Li, X.-D., Rhodes, T. E., Ikebe, R., Kambara, T., White, H. D., and Ikebe, M. (1998) Effects of mutations in the -phosphate binding site of myosin on its motor function. J. Biol. Chem. 273, 27404-27411
44. Shimada, T., Sasaki, N., Ohkura, R., and Sutoh, K. (1997) Alanine scanning mutagenesis of the switch I region in the ATPase site of Dictyostelium discoideum myosin II. Biochemistry 36, 14037-14043
45. Scheffzek, K., Ahmadian, M. R., Kabsch, W., Wiesmuller, L., Lautwein, A., Schmitz, F., and Wittinghofer, A. (1997) The Ras-RasGAP complex. Structural basis for GTPase activation and its loss in oncogenic Ras mutants. Science 277, 333-338
46. Bowler, M. W., Montgomery, M. G., Leslie, A. G., and Walker, J. E. (2007) Ground state structure of F1-ATPase from bovine heart mitochondria at 1.9 Å resolution. J. Biol. Chem. 282, 14238-14242
47. Rayment, I., Rypniewski, W. R., Schmidt-Base, K., Smith, R., Tomchick, D. R., Benning, M. M., Winkelmann, D. A., Wesenberg, G., and Holden, H. M. (1993) Three-dimensional structure of myosin subfragment-1. A molecular motor. Science 261, 50-58
48. Levy, H. M., and Koshland, D. E., Jr. (1958) Evidence for an intermediate in the hydrolysis of ATP by muscle proteins. J. Am. Chem. Soc. 80, 3164-3165
49. Levy, H. M., and Koshland, D. E., Jr. (1959) Mechanism of hydrolysis of adenosine triphosphate by muscle proteins and its relation to muscular contraction. J. Biol. Chem. 234, 1102-1107
50. Levy, H. M., Sharon, N., Lindemann, E., and Koshland, D. E., Jr. (1960) Properties of the active site in myosin hydrolysis of adenosine triphosphate as indicated by the O18-exchange reaction. J. Biol. Chem. 235, 2628-2632
51. Dempsey, M. E., Boyer, P. D., and Benson, E. S. (1963) Characteristics of an orthophosphate oxygen exchange catalyzed by myosin, actomyosin, and muscle fibers. J. Biol. Chem. 238, 2708-2715
52. Swanson, J. R., and Yount, R. (1966) The properties of heavy meromyosin and myosin catalyzed "medium" and "intermediate" 18O-phosphate exchange. Biochem. Z. 345, 395-409
53. Bagshaw, C. R., Trentham, D. R., Wolcott, R. G., and Boyer, P. D. (1975) Oxygen exchange in the -phosphoryl group of protein-bound ATP during Mg2-dependent adenosine triphosphatase activity of myosin. Proc. Natl. Acad. Sci. U.S.A. 72, 2592-2596
54. Webb, M. R., and Trentham, D. R. (1981) The mechanism of ATP hydrolysis catalyzed by myosin and actomyosin, using rapid reaction techniques to study oxygen exchange. J. Biol. Chem. 256, 10910-10916
55. Shukla, K. K., and Levy, H. M. (1977) Mechanism of oxygen exchange in actin-activated hydrolysis of adenosine triphosphate by myosin subfragment 1. Biochemistry 16, 132-136
56. Sleep, J. A., and Boyer, P. D. (1978) Effect of actin concentration on the intermediate oxygen exchange of myosin. Relation to the refractory state and the mechanism of exchange. Biochemistry 17, 5417-5422
57. Málnási-Csizmadia, A., Pearson, D. S., Kovács, M., Woolley, R. J., Geeves, M. A., and Bagshaw, C. R. (2001) Kinetic resolution of a conformational transition and the ATP hydrolysis step using relaxation methods with a Dictyostelium myosin II mutant containing a single tryptophan residue. Biochemistry 40, 12727-12737