Paxillin and Ponsin Interact in Nascent Costameres of Muscle Cells

Journal of Molecular Biology

Volumn 369, Issue 3, 2007, Pages 665-682

  Gehmlich, Katja ^a   Pinotsis, Nikos ^b   Hayeß, Katrin ^a   van der Ven, Peter F M ^a   Milting, Hendrik ^c   El Banayosy, Aly ^c   Körfer, Reiner ^c   Wilmanns, Matthias ^b   Ehler, Elisabeth ^d   Fürst, Dieter O ^a  

^a UNIVERSITY OF POTSDAM   (Germany)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c RUHR UNIVERSITY BOCHUM   (Germany)

^d KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

costamere; muscle cells; paxillin; ponsin; src homology 3 domain (SH3)

Indexed keywords

ADAPTOR PROTEIN; HELIX LOOP HELIX PROTEIN; PAXILLIN; PONSIN; PROLINE; PROTEIN SH3; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; DOWN REGULATION; EXTRACELLULAR MATRIX; FLUORESCENCE; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HEART FAILURE; HEART MUSCLE CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; MECHANOTRANSDUCTION; MORPHOLOGY; MUSCLE CELL; MUSCLE DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN STRUCTURE; RAT; TITRIMETRY;

EID: 34248164443     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.03.050     Document Type: Article

References (77)

1. Hynes R.O. Integrins: bidirectional, allosteric signaling machines. Cell 110 (2002) 673-687
2. Horwitz A.R., and Werb Z. Cell-to-cell contact and extracellular matrix- cell adhesion and the extracellular matrix: recent progress and emerging themes. Curr. Opin. Cell Biol. 10 (1998) 563-565
3. Samarel A.M. Costameres, focal adhesions, and cardiomyocyte mechanotransduction. Am. J. Physiol. Heart Circ. Physiol. 289 (2005) H2291-H2301
4. Turner C.E. Paxillin and focal adhesion signalling. Nature Cell Biol. 2 (2000) E231-E236
5. Pardo J.V., Siliciano J.D., and Craig S.W. A vinculin-containing cortical lattice in skeletal muscle: transverse lattice elements ("costameres") mark sites of attachment between myofibrils and sarcolemma. Proc. Natl Acad. Sci. USA 80 (1983) 1008-1012
6. Ervasti J.M. Costameres: the Achilles' heel of Herculean muscle. J. Biol. Chem. 278 (2003) 13591-13594
7. Small J.V., Fürst D.O., and Thornell L.E. The cytoskeletal lattice of muscle cells. Eur. J. Biochem. 208 (1992) 559-572
8. Zamir E., and Geiger B. Molecular complexity and dynamics of cell-matrix adhesions. J. Cell Sci. 114 (2001) 3583-3590
9. Berthier C., and Blaineau S. Supramolecular organization of the subsarcolemmal cytoskeleton of adult skeletal muscle fibers. A review. Biol. Cell 89 (1997) 413-434
10. Lapidos K.A., Kakkar R., and McNally E.M. The dystrophin glycoprotein complex: signaling strength and integrity for the sarcolemma. Circ. Res. 94 (2004) 1023-1031
11. Thompson T.G., Chan Y.M., Hack A.A., Brosius M., Rajala M., Lidov H.G., et al. Filamin 2 (FLN2): a muscle-specific sarcoglycan interacting protein. J. Cell Biol. 148 (2000) 115-126
12. Van der Flier A., Gaspar A.C., Thorsteinsdottir S., Baudoin C., Groeneveld E., Mummery C.L., and Sonnenberg A. Spatial and temporal expression of the beta1D integrin during mouse development. Dev. Dynam. 210 (1997) 472-486
13. Danowski B.A., Imanaka-Yoshida K., Sanger J.M., and Sanger J.W. Costameres are sites of force transmission to the substratum in adult rat cardiomyocytes. J. Cell Biol. 118 (1992) 1411-1420
14. Eble D.M., Strait J.B., Govindarajan G., Lou J., Byron K.L., and Samarel A.M. Endothelin-induced cardiac myocyte hypertrophy: role for focal adhesion kinase. Am. J. Physiol. Heart Circ. Physiol. 278 (2000) H1695-H1707
15. Sharp W.W., Simpson D.G., Borg T.K., Samarel A.M., and Terracio L. Mechanical forces regulate focal adhesion and costamere assembly in cardiac myocytes. Am. J. Physiol. 273 (1997) H546-H556
16. Bendig G., Grimmler M., Huttner I.G., Wessels G., Dahme T., Just S., et al. Integrin-linked kinase, a novel component of the cardiac mechanical stretch sensor, controls contractility in the zebrafish heart. Genes Dev. 20 (2006) 2361-2372
17. Brancaccio M., Fratta L., Notte A., Hirsch E., Poulet R., Guazzone S., et al. Melusin, a muscle-specific integrin beta1-interacting protein, is required to prevent cardiac failure in response to chronic pressure overload. Nature Med. 9 (2003) 68-75
18. Olson T.M., Illenberger S., Kishimoto N.Y., Huttelmaier S., Keating M.T., and Jockusch B.M. Metavinculin mutations alter actin interaction in dilated cardiomyopathy. Circulation 105 (2002) 431-437
19. Hayashi Y.K., Chou F.L., Engvall E., Ogawa M., Matsuda C., Hirabayashi S., et al. Mutations in the integrin alpha7 gene cause congenital myopathy. Nature Genet. 19 (1998) 94-97
20. Schaller M.D. FAK and paxillin: regulators of N-cadherin adhesion and inhibitors of cell migration?. J. Cell Biol. 166 (2004) 157-159
21. Quach N.L., and Rando T.A. Focal adhesion kinase is essential for costamerogenesis in cultured skeletal muscle cells. Dev. Biol. 293 (2006) 38-52
22. Salgia R., Li J.L., Lo S.H., Brunkhorst B., Kansas G.S., Sobhany E.S., et al. Molecular cloning of human paxillin, a focal adhesion protein phosphorylated by P210BCR/ABL. J. Biol. Chem. 270 (1995) 5039-5047
23. Turner C.E. Paxillin. Int. J. Biochem. Cell Biol. 30 (1998) 955-959
24. Tumbarello D.A., Brown M.C., and Turner C.E. The paxillin LD motifs. FEBS Letters 513 (2002) 114-118
25. Turner C.E. Paxillin interactions. J. Cell Sci. 113 (2000) 4139-4140
26. Macias M.J., Wiesner S., and Sudol M. WW and SH3 domains, two different scaffolds to recognize proline-rich ligands. FEBS Letters 513 (2002) 30-37
27. Kioka N., Ueda K., and Amachi T. Vinexin, CAP/ponsin, ArgBP2: a novel adaptor protein family regulating cytoskeletal organization and signal transduction. Cell Struct. Funct. 27 (2002) 1-7
28. Zhang M., Liu J., Cheng A., Deyoung S.M., Chen X., Dold L.H., and Saltiel A.R. CAP interacts with cytoskeletal proteins and regulates adhesion-mediated ERK activation and motility. EMBO J. 25 (2006) 5284-5293
29. Holm L., and Sander C. Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233 (1993) 123-138
30. Massenet C., Chenavas S., Cohen-Addad C., Dagher M.C., Brandolin G., Pebay-Peyroula E., and Fieschi F. Effects of p47phox C terminus phosphorylations on binding interactions with p40phox and p67phox. Structural and functional comparison of p40phox and p67phox SH3 domains. J. Biol. Chem. 280 (2005) 13752-13761
31. Fazi B., Cope M.J., Douangamath A., Ferracuti S., Schirwitz K., Zucconi A., et al. Unusual binding properties of the SH3 domain of the yeast actin-binding protein Abp1: structural and functional analysis. J. Biol. Chem. 277 (2002) 5290-5298
32. Feng S., Kasahara C., Rickles R.J., and Schreiber S.L. Specific interactions outside the proline-rich core of two classes of Src homology 3 ligands. Proc. Natl Acad. Sci. USA 92 (1995) 12408-12415
33. Lim W.A., Richards F.M., and Fox R.O. Structural determinants of peptide-binding orientation and of sequence specificity in SH3 domains. Nature 372 (1994) 375-379
34. Musacchio A., Wilmanns M., and Saraste M. Structure and function of the SH3 domain. Prog. Biophys. Mol. Biol. 61 (1994) 283-297
35. Mandai K., Nakanishi H., Satoh A., Takahashi K., Satoh K., Nishioka H., et al. Ponsin/SH3P12: an l-afadin- and vinculin-binding protein localized at cell-cell and cell-matrix adherens junctions. J. Cell Biol. 144 (1999) 1001-1017
36. Lin W.H., Huang C.J., Liu M.W., Chang H.M., Chen Y.J., Tai T.Y., and Chuang L.M. Cloning, mapping, and characterization of the human sorbin and SH3 domain containing 1 (SORBS1) gene: a protein associated with c-Abl during insulin signaling in the hepatoma cell line Hep3B. Genomics 74 (2001) 12-20
37. Arber S., Hunter J.J., Ross Jr. J., Hongo M., Sansig G., Borg J., et al. MLP-deficient mice exhibit a disruption of cardiac cytoarchitectural organization, dilated cardiomyopathy, and heart failure. Cell 88 (1997) 393-403
38. Flick M.J., and Konieczny S.F. The muscle regulatory and structural protein MLP is a cytoskeletal binding partner of betaI-spectrin. J. Cell Sci. 113 (2000) 1553-1564
39. Zolk O., Caroni P., and Bohm M. Decreased expression of the cardiac LIM domain protein MLP in chronic human heart failure. Circulation 101 (2000) 2674-2677
40. Sudol M. The WW module competes with the SH3 domain?. Trends Biochem. Sci. 21 (1996) 161-163
41. Musacchio A., Saraste M., and Wilmanns M. High-resolution crystal structures of tyrosine kinase SH3 domains complexed with proline-rich peptides. Nature Struct. Biol. 1 (1994) 546-551
42. Viguera A.R., Arrondo J.L., Musacchio A., Saraste M., and Serrano L. Characterization of the interaction of natural proline-rich peptides with five different SH3 domains. Biochemistry 33 (1994) 10925-10933
43. Musi V., Birdsall B., Fernandez-Ballester G., Guerrini R., Salvatori S., Serrano L., and Pastore A. New approaches to high-throughput structure characterization of SH3 complexes: the example of Myosin-3 and Myosin-5 SH3 domains from S. cerevisiae. Protein Sci. 15 (2006) 795-807
44. Mahoney N.M., Janmey P.A., and Almo S.C. Structure of the profilin-poly-l-proline complex involved in morphogenesis and cytoskeletal regulation. Nature Struct. Biol. 4 (1997) 953-960
45. Vaynberg J., Fukuda T., Chen K., Vinogradova O., Velyvis A., Tu Y., et al. Structure of an ultraweak protein-protein complex and its crucial role in regulation of cell morphology and motility. Mol. Cell 17 (2005) 513-523
46. Weng Z., Taylor J.A., Turner C.E., Brugge J.S., and Seidel-Dugan C. Detection of Src homology 3-binding proteins, including paxillin, in normal and v-Src-transformed Balb/c 3T3 cells. J. Biol. Chem. 268 (1993) 14956-14963
47. Hirschy A., Schatzmann F., Ehler E., and Perriard J.C. Establishment of cardiac cytoarchitecture in the developing mouse heart. Dev. Biol. 289 (2006) 430-441
48. Hagel M., George E.L., Kim A., Tamimi R., Opitz S.L., Turner C.E., et al. The adaptor protein paxillin is essential for normal development in the mouse and is a critical transducer of fibronectin signaling. Mol. Cell. Biol. 22 (2002) 901-915
49. Ribon V., Herrera R., Kay B.K., and Saltiel A.R. A role for CAP, a novel, multifunctional Src homology 3 domain-containing protein in formation of actin stress fibers and focal adhesions. J. Biol. Chem. 273 (1998) 4073-4080
50. Ribon V., Printen J.A., Hoffman N.G., Kay B.K., and Saltiel A.R. A novel, multifuntional c-Cbl binding protein in insulin receptor signaling in 3T3-L1 adipocytes. Mol. Cell. Biol. 18 (1998) 872-879
51. Cowan C.A., and Henkemeyer M. The SH2/SH3 adaptor Grb4 transduces B-ephrin reverse signals. Nature 413 (2001) 174-179
52. Lebre A.S., Jamot L., Takahashi J., Spassky N., Leprince C., Ravise N., et al. Ataxin-7 interacts with a Cbl-associated protein that it recruits into neuronal intranuclear inclusions. Hum. Mol. Genet. 10 (2001) 1201-1213
53. Ronty M., Taivainen A., Moza M., Kruh G.D., Ehler E., and Carpen O. Involvement of palladin and alpha-actinin in targeting of the Abl/Arg kinase adaptor ArgBP2 to the actin cytoskeleton. Exp. Cell Res. 310 (2005) 88-98
54. Nunes S.M., Ferralli J., Choi K., Brown-Luedi M., Minet A.D., and Chiquet-Ehrismann R. The intracellular domain of teneurin-1 interacts with MBD1 and CAP/ponsin resulting in subcellular codistribution and translocation to the nuclear matrix. Exp. Cell Res. 305 (2005) 122-132
55. Schröder R., Fürst D.O., Klasen C., Reimann J., Herrmann H., and van der Ven P.F. Association of plectin with Z-discs is a prerequisite for the formation of the intermyofibrillar desmin cytoskeleton. Lab. Invest. 80 (2000) 455-464
56. van der Ven P.F.M., Wiesner S., Salmikangas P., Auerbach D., Himmel M., Kempa S., et al. Indications for a novel muscular dystrophy pathway. gamma-filamin, the muscle-specific filamin isoform, interacts with myotilin. J. Cell Biol. 151 (2000) 235-248
57. Obermann W.M.J., Gautel M., Steiner F., van der Ven P.F.M., Weber K., and Fürst D.O. The structure of the sarcomeric M band: localization of defined domains of myomesin, M-protein, and the 250-kD carboxy-terminal region of titin by immunoelectron microscopy. J. Cell Biol. 134 (1996) 1441-1453
58. Gehmlich K., Geier C., Osterziel K.J., van der Ven P.F.M., and Fürst D.O. Decreased interactions of mutant muscle LIM protein (MLP) with N-RAP and alpha-actinin and their implication for hypertrophic cardiomyopathy. Cell Tissue Res. 317 (2004) 129-136
59. Fürst D.O., Osborn M., Nave R., and Weber K. The organization of titin filaments in the half-sarcomere revealed by monoclonal antibodies in immunoelectron microscopy: a map of ten nonrepetitive epitopes starting at the Z line extends close to the M line. J. Cell Biol. 106 (1988) 1563-1572
60. Lange S., Auerbach D., McLoughlin P., Perriard E., Schafer B.W., Perriard J.C., and Ehler E. Subcellular targeting of metabolic enzymes to titin in heart muscle may be mediated by DRAL/FHL-2. J. Cell Sci. 115 (2002) 4925-4936
61. Pacholsky D., Vakeel P., Himmel M., Löwe T., Stradal T., Rottner K., et al. Xin repeats define a novel actin-binding motif. J. Cell Sci. 117 (2004) 5257-5268
62. Mueller-Dieckmann J. The open-access high-throughput crystallization facility at EMBL Hamburg. Acta Crystallor. sect. D 62 (2006) 1446-1452
63. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Macromol. Crystallog. 276 (1997) 307-326
64. Matthews B.W. Solvent content of protein crystals. J. Mol. Biol. 33 (1968) 491-497
65. Vagin A., and Teplyakov A. MOLREP: an automated program for molecular replacement. J. Appl. Crystallog. 30 (1997) 1022-1025
66. Perrakis A., Harkiolaki M., Wilson K.S., and Lamzin V.S. ARP/wARP and molecular replacement. Acta Crystallog. sect. D 57 (2001) 1445-1450
67. Jones T.A., Zou J.Y., Cowan S.W., and Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A 47 (1991) 110-119
68. Winn M.D., Isupov M.N., and Murshudov G.N. Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallog. sect. D 57 (2001) 122-133
69. Sheldrick G.M., and Schneider T.R. SHELXL: High-resolution refinement. Methods Enzymol. 277 (1997) 319-343
70. Corpet F. Multiple sequence alignment with hierarchical clustering. Nucl. Acids Res. 16 (1988) 10881-10890
71. Kabsch W. A solution for the best rotation to relate two sets of vectors. Acta Crystallog. 32 (1976) 922-923
72. Jones S., and Thornton J.M. Principles of protein-protein interactions. Proc. Natl Acad. Sci. USA 93 (1996) 13-20
73. Wallace A.C., Laskowski R.A., and Thornton J.M. LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng. 8 (1995) 127-134
74. Moss M.L., Kuzmic P., Stuart J.D., Tian G.C., Peranteau A.G., Frye S.V., et al. Inhibition of human steroid 5 alpha reductases type I and II by 6-aza-steroids: structural determinants of one-step vs two-step mechanism. Biochemistry 35 (1996) 3457-3464
75. Schröder R., Pacholsky D., Reimann J., Matten J., Wiche G., Fürst D.O., and van der Ven P.F.M. Primary longitudinal adhesion structures: plectin-containing precursors of costameres in differentiating human skeletal muscle cells. Histochem. Cell Biol. 118 (2002) 301-310
76. Aquila L.A., McCarthy P.M., Smedira N.G., Young J.B., and Moravec C.S. Cytoskeletal structure and recovery in single human cardiac myocytes. J. Heart Lung Transplant. 23 (2004) 954-963
77. Vandenbroere I., Paternotte N., Dumont J.E., Erneux C., and Pirson I. The c-Cbl-associated protein and c-Cbl are two new partners of the SH2-containing inositol polyphosphate 5-phosphatase SHIP2. Biochem. Biophys. Res. Commun. 300 (2003) 494-500