Asymmetric mode of Ca 2+-S100A4 interaction with nonmuscle myosin IIA generates nanomolar affinity required for filament remodeling

Structure

Volumn 20, Issue 4, 2012, Pages 654-666

  Elliott, Paul R ^a   Irvine, Andrew F ^b   Jung, Hyun Suk ^c   Tozawa, Kaeko ^a   Pastok, Martyna W ^a   Picone, Remigio ^d,e,f   Badyal, Sandip K ^b   Basran, Jaswir ^b   Rudland, Philip S ^a   Barraclough, Roger ^a   Lian, Lu Yun ^a   Bagshaw, Clive R ^b,g   Kriajevska, Marina ^b   Barsukov, Igor L ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b UNIVERSITY OF LEICESTER   (United Kingdom)

^c Korea Basic Science Institute (KBSI)   (South Korea)

^d MRC Laboratory for Molecular Cell Biology   (United Kingdom)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

^f LONDON CENTRE FOR NANOTECHNOLOGY   (United Kingdom)

^g UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CALVASCULIN; DIMER; MYOSIN HEAVY CHAIN; MYOSIN IIA; NONMUSCLE MYOSIN IIA; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ARTICLE; BINDING AFFINITY; BINDING SITE; CELL MIGRATION; CELL MOTILITY; CELL SHAPE; CELL SPREADING; HUMAN; HUMAN CELL; MUTATIONAL ANALYSIS; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; STOICHIOMETRY; STRESS FIBER; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; BINDING SITES; CALCIUM; CELL LINE, TUMOR; CELL MOVEMENT; CYTOSKELETON; EPITHELIAL CELLS; HUMANS; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NONMUSCLE MYOSIN TYPE IIA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; POINT MUTATION; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; S100 PROTEINS; THERMODYNAMICS;

EID: 84859379161     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2012.02.002     Document Type: Article

References (45)

1. N.S. Ambartsumian, M.S. Grigorian, I.F. Larsen, O. Karlstrøm, N. Sidenius, J. Rygaard, G. Georgiev, and E. Lukanidin Metastasis of mammary carcinomas in GRS/A hybrid mice transgenic for the mts1 gene Oncogene 13 1996 1621 1630
2. H. Andersen, J. Mejlvang, S. Mahmood, I. Gromova, P. Gromov, E. Lukanidin, M. Kriajevska, J.K. Mellon, and E. Tulchinsky Immediate and delayed effects of E-cadherin inhibition on gene regulation and cell motility in human epidermoid carcinoma cells Mol. Cell. Biol. 25 2005 9138 9150
3. S.J. Atkinson, and M. Stewart Molecular interactions in myosin assembly. Role of the 28-residue charge repeat in the rod J. Mol. Biol. 226 1992 7 13
4. 2+-dependent interaction between S100A4 and tail fragments of nonmuscle myosin heavy chain IIA J. Mol. Biol. 405 2011 1004 1026
5. S. Bhattacharya, E. Large, C.W. Heizmann, B.A. Hemmings, and W.J. Chazin Structure of the Ca2+/S100B/NDR kinase peptide complex: insights into S100 target specificity and activation of the kinase Biochemistry 42 2003 14416 14426
6. S.A. Burgess, M.L. Walker, K. Thirumurugan, J. Trinick, and P.J. Knight Use of negative stain and single-particle image processing to explore dynamic properties of flexible macromolecules J. Struct. Biol. 147 2004 247 258
7. T.H. Charpentier, L.E. Thompson, M.A. Liriano, K.M. Varney, P.T. Wilder, E. Pozharski, E.A. Toth, and D.J. Weber The effects of CapZ peptide (TRTK-12) binding to S100B-Ca2+ as examined by NMR and X-ray crystallography J. Mol. Biol. 396 2010 1227 1243
8. K. Clark, J. Middelbeek, M.V. Dorovkov, C.G. Figdor, A.G. Ryazanov, E. Lasonder, and F.N. van Leeuwen The alpha-kinases TRPM6 and TRPM7, but not eEF-2 kinase, phosphorylate the assembly domain of myosin IIA, IIB and IIC FEBS Lett. 582 2008 2993 2997
9. B.R. Davies, M.P. Davies, F.E. Gibbs, R. Barraclough, and P.S. Rudland Induction of the metastatic phenotype by transfection of a benign rat mammary epithelial cell line with the gene for p9Ka, a rat calcium-binding protein, but not with the oncogene EJ-ras-1 Oncogene 8 1993 999 1008
10. M.P. Davies, P.S. Rudland, L. Robertson, E.W. Parry, P. Jolicoeur, and R. Barraclough Expression of the calcium-binding protein S100A4 (p9Ka) in MMTV-neu transgenic mice induces metastasis of mammary tumours Oncogene 13 1996 1631 1637
11. N.G. Dulyaninova, K.M. Hite, W.D. Zencheck, D.A. Scudiero, S.C. Almo, R.H. Shoemaker, and A.R. Bresnick Cysteine 81 is critical for the interaction of S100A4 and myosin-IIA Biochemistry 50 2011 7218 7227
12. H.L. Ford, D.L. Silver, B. Kachar, J.R. Sellers, and S.B. Zain Effect of Mts1 on the structure and activity of nonmuscle myosin II Biochemistry 36 1997 16321 16327
13. S.C. Garrett, K.M. Varney, D.J. Weber, and A.R. Bresnick S100A4, a mediator of metastasis J. Biol. Chem. 281 2006 677 680
14. 2+-binding kinetics of metastasis-associated protein, S100A4 FEBS Lett. 582 2008 1651 1656
15. R.P. House, M. Pozzuto, P. Patel, N.G. Dulyaninova, Z.H. Li, W.D. Zencheck, M.I. Vitolo, D.J. Weber, and A.R. Bresnick Two functional S100A4 monomers are necessary for regulating nonmuscle myosin-IIA and HCT116 cell invasion Biochemistry 50 2011 6920 6932
16. T.M. Ismail, D.G. Fernig, P.S. Rudland, C.J. Terry, G. Wang, and R. Barraclough The basic C-terminal amino acids of calcium-binding protein S100A4 promote metastasis Carcinogenesis 29 2008 2259 2266
17. T.M. Ismail, S. Zhang, D.G. Fernig, S. Gross, M.L. Martin-Fernandez, V. See, K. Tozawa, C.J. Tynan, G. Wang, and M.C. Wilkinson Self-association of calcium-binding protein S100A4 and metastasis J. Biol. Chem. 285 2010 914 922
18. W.P. Jencks On the attribution and additivity of binding energies Proc. Natl. Acad. Sci. USA 78 1981 4046 4050
19. H.S. Jung, S. Komatsu, M. Ikebe, and R. Craig Head-head and head-tail interaction: a general mechanism for switching off myosin II activity in cells Mol. Biol. Cell 19 2008 3234 3242
20. E.J. Kim, and D.M. Helfman Characterization of the metastasis-associated protein, S100A4. Roles of calcium binding and dimerization in cellular localization and interaction with myosin J. Biol. Chem. 278 2003 30063 30073
21. B. Kiss, A. Duelli, L. Radnai, K.A. Kékesi, G. Katona, and L. Nyitray Crystal structure of S100A4-myosin IIA tail fragment complex reveals an asymmetric target binding mechanism in the S100 protein family Proc. Natl. Acad. Sci. USA 2012 in press
22. M. Kriajevska, S. Tarabykina, I. Bronstein, N. Maitland, M. Lomonosov, K. Hansen, G. Georgiev, and E. Lukanidin Metastasis-associated Mts1 (S100A4) protein modulates protein kinase C phosphorylation of the heavy chain of nonmuscle myosin J. Biol. Chem. 273 1998 9852 9856
23. M. Kriajevska, I.B. Bronstein, D.J. Scott, S. Tarabykina, M. Fischer-Larsen, O. Issinger, and E. Lukanidin Metastasis-associated protein Mts1 (S100A4) inhibits CK2-mediated phosphorylation and self-assembly of the heavy chain of nonmuscle myosin Biochim. Biophys. Acta 1498 2000 252 263
24. Y.T. Lee, Y.N. Dimitrova, G. Schneider, W.B. Ridenour, S. Bhattacharya, S.E. Soss, R.M. Caprioli, A. Filipek, and W.J. Chazin Structure of the S100A6 complex with a fragment from the C-terminal domain of Siah-1 interacting protein: a novel mode for S100 protein target recognition Biochemistry 47 2008 10921 10932
25. Z.H. Li, A. Spektor, O. Varlamova, and A.R. Bresnick Mts1 regulates the assembly of nonmuscle myosin-IIA Biochemistry 42 2003 14258 14266
26. Z.H. Li, N.G. Dulyaninova, R.P. House, S.C. Almo, and A.R. Bresnick S100A4 regulates macrophage chemotaxis Mol. Biol. Cell 21 2010 2598 2610
27. V.N. Malashkevich, K.M. Varney, S.C. Garrett, P.T. Wilder, D. Knight, T.H. Charpentier, U.A. Ramagopal, S.C. Almo, D.J. Weber, and A.R. Bresnick Structure of Ca2+-bound S100A4 and its interaction with peptides derived from nonmuscle myosin-IIA Biochemistry 47 2008 5111 5126
28. A.D. McLachlan, and J. Karn Periodic charge distributions in the myosin rod amino acid sequence match cross-bridge spacings in muscle Nature 299 1982 226 231
29. E.F. Pettersen, T.D. Goddard, C.C. Huang, G.S. Couch, D.M. Greenblatt, E.C. Meng, and T.E. Ferrin UCSF Chimera - a visualization system for exploratory research and analysis J. Comput. Chem. 25 2004 1605 1612
30. R. Picone, X. Ren, K.D. Ivanovitch, J.D. Clarke, R.A. McKendry, and B. Baum A polarised population of dynamic microtubules mediates homeostatic length control in animal cells PLoS Biol. 8 2010 e1000542
31. S. Réty, J. Sopkova, M. Renouard, D. Osterloh, V. Gerke, S. Tabaries, F. Russo-Marie, and A. Lewit-Bentley The crystal structure of a complex of p11 with the annexin II N-terminal peptide Nat. Struct. Biol. 6 1999 89 95
32. A. Rezvanpour, L. Santamaria-Kisiel, and G.S. Shaw The S100A10-annexin A2 complex provides a novel asymmetric platform for membrane repair J. Biol. Chem. 286 2011 40174 40183
33. D. Ricketson, C.A. Johnston, and K.E. Prehoda Multiple tail domain interactions stabilize nonmuscle myosin II bipolar filaments Proc. Natl. Acad. Sci. USA 107 2010 20964 20969
34. R.R. Rustandi, D.M. Baldisseri, and D.J. Weber Structure of the negative regulatory domain of p53 bound to S100B(betabeta) Nat. Struct. Biol. 7 2000 570 574
35. L. Santamaria-Kisiel, A.C. Rintala-Dempsey, and G.S. Shaw Calcium-dependent and -independent interactions of the S100 protein family Biochem. J. 396 2006 201 214
36. S. Tarabykina, T.R.L. Griffiths, E. Tulchinsky, J.K. Mellon, I.B. Bronstein, and M. Kriajevska Metastasis-associated protein S100A4: spotlight on its role in cell migration Curr. Cancer Drug Targets 7 2007 217 228
37. M. Théry Micropatterning as a tool to decipher cell morphogenesis and functions J. Cell Sci. 123 2010 4201 4213
38. K.M. Vallely, R.R. Rustandi, K.C. Ellis, O. Varlamova, A.R. Bresnick, and D.J. Weber Solution structure of human Mts1 (S100A4) as determined by NMR spectroscopy Biochemistry 41 2002 12670 12680
39. M. Vicente-Manzanares, J. Zareno, L. Whitmore, C.K. Choi, and A.F. Horwitz Regulation of protrusion, adhesion dynamics, and polarity by myosins IIA and IIB in migrating cells J. Cell Biol. 176 2007 573 580
40. M. Vicente-Manzanares, M.A. Koach, L. Whitmore, M.L. Lamers, and A.F. Horwitz Segregation and activation of myosin IIB creates a rear in migrating cells J. Cell Biol. 183 2008 543 554
41. M. Vicente-Manzanares, X. Ma, R.S. Adelstein, and A.R. Horwitz Non-muscle myosin II takes centre stage in cell adhesion and migration Nat. Rev. Mol. Cell Biol. 10 2009 778 790
42. N.T. Wright, B.L. Prosser, K.M. Varney, D.B. Zimmer, M.F. Schneider, and D.J. Weber S100A1 and calmodulin compete for the same binding site on ryanodine receptor J. Biol. Chem. 283 2008 26676 26683
43. N.T. Wright, B.R. Cannon, P.T. Wilder, M.T. Morgan, K.M. Varney, D.B. Zimmer, and D.J. Weber Solution structure of S100A1 bound to the CapZ peptide (TRTK12) J. Mol. Biol. 386 2009 1265 1277
44. P.J. Wyatt Light scattering and the absolute characterization of macromolecules Anal. Chim. Acta 272 1993 1 40
45. S. Zhang, G. Wang, D. Liu, Z. Bao, D.G. Fernig, P.S. Rudland, and R. Barraclough The C-terminal region of S100A4 is important for its metastasis-inducing properties Oncogene 24 2005 4401 4411