Mena/VASP and αiI-Spectrin complexes regulate cytoplasmic actin networks in cardiomyocytes and protect from conduction abnormalities and dilated cardiomyopathy

Cell Communication and Signaling

Volumn 11, Issue 1, 2013, Pages

  Benz, Peter M ^a,b   Merkel, Carla J ^a,c   Offner, Kristin ^a   Abeßer, Marco ^a   Ullrich, Melanie ^a   Fischer, Tobias ^a   Bayer, Barbara ^d   Wagner, Helga ^d   Gambaryan, Stepan ^a,e   Ursitti, Jeanine A ^f   Adham, Ibrahim M ^g   Linke, Wolfgang A ^h   Feller, Stephan M ^i,j   Fleming, Ingrid ^b   Renné, Thomas ^k,l   Frantz, Stefan ^d   Unger, Andreas ^h   Schuh, Kai ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b GOETHE UNIVERSITY   (Germany)

^c UNIVERSITY OF BONN   (Germany)

^d UNIVERSITY HOSPITAL WÜRZBURG   (Germany)

^e SECHENOV INSTITUTE OF EVOLUTIONARY PHYSIOLOGY AND BIOCHEMISTRY   (Russian Federation)

^f UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^g UNIVERSITY OF GÖTTINGEN   (Germany)

^h RUHR UNIVERSITY BOCHUM   (Germany)

ⁱ UNIVERSITY OF OXFORD   (United Kingdom)

^j MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^k KAROLINSKA INSTITUTE   (Sweden)

^l UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

more..

Author keywords

Actin; Dilated cardiomyopathy; Heart; Mena VASP; Spectrin

Indexed keywords

ACTIN; ALPHAII SPECTRIN; BETA ACTIN; CYTOPLASMIC ACTIN; CYTOSKELETON PROTEIN; FODRIN; MENA PROTEIN; UNCLASSIFIED DRUG; VASODILATOR STIMULATED PHOSPHOPROTEIN; ACTIN BINDING PROTEIN; CELL ADHESION MOLECULE; ENAH PROTEIN, MOUSE; PHOSPHOPROTEIN; SPECTRIN; VASODILATOR-STIMULATED PHOSPHOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONGESTIVE CARDIOMYOPATHY; CONTROLLED STUDY; FEMALE; HEART MUSCLE CELL; HEART MUSCLE CONDUCTION DISTURBANCE; HEART MUSCLE FIBROSIS; HEART PROTECTION; HEART VENTRICLE HYPERTROPHY; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SARCOMERE; THIN FILAMENT; WILD TYPE; ANIMAL; CHEMISTRY; CYTOPLASM; GENETICS; HEART MUSCLE CONDUCTION SYSTEM; METABOLISM; SRC HOMOLOGY DOMAIN; TRANSGENIC MOUSE;

MUS;

ACTINS; ANIMALS; CARDIOMYOPATHY, DILATED; CELL ADHESION MOLECULES; CYTOPLASM; CYTOSKELETAL PROTEINS; HEART CONDUCTION SYSTEM; MALE; MICE; MICE, TRANSGENIC; MICROFILAMENT PROTEINS; MYOCYTES, CARDIAC; PHOSPHOPROTEINS; SPECTRIN; SRC HOMOLOGY DOMAINS;

EID: 84881271838     PISSN: None     EISSN: 1478811X     Source Type: Journal    
DOI: 10.1186/1478-811X-11-56     Document Type: Article

References (41)

1. The actin gene family: function follows isoform. Perrin BJ, Ervasti JM, Cytoskeleton (Hoboken) 2010 67 630 634 10.1002/cm.20475
2. Diverse roles of the actin cytoskeleton in striated muscle. Kee AJ, Gunning PW, Hardeman EC, J Muscle Res Cell Motil 2009 30 187 197 10.1007/s10974-009-9193-x 19997772
3. Molecular genetics and genomics of heart failure. Liew CC, Dzau VJ, Nat Rev Genet 2004 5 811 825 10.1038/nrg1470 15520791
4. The transitional junction: a new functional subcellular domain at the intercalated disc. Bennett PM, Maggs AM, Baines AJ, Pinder JC, Mol Biol Cell 2006 17 2091 2100 10.1091/mbc.E05-12-1109 16481394
5. Hypertrophic stimulation increases beta-actin dynamics in adult feline cardiomyocytes. Balasubramanian S, Mani SK, Kasiganesan H, Baicu CC, Kuppuswamy D, PLoS One 2010 5 11470 10.1371/journal.pone.0011470 20635003
6. ENA/VASP proteins: multifunctional regulators of actin cytoskeleton dynamics. Sechi AS, Wehland J, Front Biosci 2004 9 1294 1310 10.2741/1324 14977545
7. Distribution, cellular localization, and postnatal development of VASP and Mena expression in mouse tissues. Gambaryan S, Hauser W, Kobsar A, Glazova M, Walter U, Histochem Cell Biol 2001 116 535 543 10.1007/s00418-001-0353-3 11810195
8. VASP is a processive actin polymerase that requires monomeric actin for barbed end association. Hansen SD, Mullins RD, J Cell Biol 2010 191 571 584 10.1083/jcb.201003014 21041447
9. Ena/VASP proteins enhance actin polymerization in the presence of barbed end capping proteins. Barzik M, Kotova TI, Higgs HN, Hazelwood L, Hanein D, Gertler FB, Schafer DA, J Biol Chem 2005 280 28653 28662 10.1074/jbc.M503957200 15939738
10. Cytoskeleton assembly at endothelial cell-cell contacts is regulated by alphaII-spectrin-VASP complexes. Benz PM, Blume C, Moebius J, Oschatz C, Schuh K, Sickmann A, Walter U, Feller SM, Renne T, J Cell Biol 2008 180 205 219 10.1083/jcb.200709181 18195108
11. Differential VASP phosphorylation controls remodeling of the actin cytoskeleton. Benz PM, Blume C, Seifert S, Wilhelm S, Waschke J, Schuh K, Gertler F, Munzel T, Renne T, J Cell Sci 2009 122 3954 3965 10.1242/jcs.044537 19825941
12. Ena/VASP proteins can regulate distinct modes of actin organization at cadherin-adhesive contacts. Scott JA, Shewan AM, den Elzen NR, Loureiro JJ, Gertler FB, Yap AS, Mol Biol Cell 2006 17 1085 1095 16371509
13. Ena/VASP Is Required for neuritogenesis in the developing cortex. Kwiatkowski AV, Rubinson DA, Dent EW, van Veen EJ, Leslie JD, Zhang J, Mebane LM, Philippar U, Pinheiro EM, Burds AA, et al. Neuron 2007 56 441 455 10.1016/j.neuron.2007.09.008 17988629
14. Mena is required for neurulation and commissure formation. Lanier LM, Gates MA, Witke W, Menzies AS, Wehman AM, Macklis JD, Kwiatkowski D, Soriano P, Gertler FB, Neuron 1999 22 313 325 10.1016/S0896-6273(00)81092-2 10069337
15. The vasodilator-stimulated phosphoprotein (VASP) is involved in cGMP- and cAMP-mediated inhibition of agonist-induced platelet aggregation, but is dispensable for smooth muscle function. Aszodi A, Pfeifer A, Ahmad M, Glauner M, Zhou XH, Ny L, Andersson KE, Kehrel B, Offermanns S, Fassler R, Embo J 1999 18 37 48 10.1093/emboj/18.1.37 9878048
16. Megakaryocyte hyperplasia and enhanced agonist-induced platelet activation in vasodilator-stimulated phosphoprotein knockout mice. Hauser W, Knobeloch KP, Eigenthaler M, Gambaryan S, Krenn V, Geiger J, Glazova M, Rohde E, Horak I, Walter U, Zimmer M, Proc Natl Acad Sci U S A 1999 96 8120 8125 10.1073/pnas.96.14.8120 10393958
17. Mutations in Drosophila enabled and rescue by human vasodilator- stimulated phosphoprotein (VASP) indicate important functional roles for Ena/VASP homology domain 1 (EVH1) and EVH2 domains. Ahern-Djamali SM, Comer AR, Bachmann C, Kastenmeier AS, Reddy SK, Beckerle MC, Walter U, Hoffmann FM, Mol Biol Cell 1998 9 2157 2171 10.1091/mbc.9.8.2157 9693373
18. Mena and vasodilator-stimulated phosphoprotein are required for multiple actin-dependent processes that shape the vertebrate nervous system. Menzies AS, Aszodi A, Williams SE, Pfeifer A, Wehman AM, Goh KL, Mason CA, Fassler R, Gertler FB, J Neurosci 2004 24 8029 8038 10.1523/JNEUROSCI.1057-04.2004 15371503
19. The spectrin-associated cytoskeleton in mammalian heart. Baines AJ, Pinder JC, Front Biosci 2005 10 3020 3033 10.2741/1759 15970557
20. Membrane domains based on ankyrin and spectrin associated with cell-cell interactions. Bennett V, Healy J, Cold Spring Harb Perspect Biol 2009 1 003012 10.1101/cshperspect.a003012 20457566
21. Spectrin and ankyrin-based pathways: metazoan inventions for integrating cells into tissues. Bennett V, Baines AJ, Physiol Rev 2001 81 1353 1392 11427698
22. Not just a plasma membrane protein: in cardiac muscle cells alpha-II spectrin also shows a close association with myofibrils. Bennett PM, Baines AJ, Lecomte MC, Maggs AM, Pinder JC, J Muscle Res Cell Motil 2004 25 119 126 15360127
23. Cell organization, growth, and neural and cardiac development require alphaII-spectrin. Stankewich MC, Cianci CD, Stabach PR, Ji L, Nath A, Morrow JS, J Cell Sci 2011 124 3956 3966 10.1242/jcs.080374 22159418
24. A rapid protein expression and purification system using Chinese hamster ovary cells expressing retrovirus receptor. Suzuki J, Fukuda M, Kawata S, Maruoka M, Kubo Y, Takeya T, Shishido T, J Biotechnol 2006 126 463 474 10.1016/j.jbiotec.2006.04.039 16766074
25. Mena, a relative of VASP and Drosophila Enabled, is implicated in the control of microfilament dynamics. Gertler FB, Niebuhr K, Reinhard M, Wehland J, Soriano P, Cell 1996 87 227 239 10.1016/S0092-8674(00)81341-0 8861907
26. Gene trap: knockout on the fast lane. Ullrich M, Schuh K, Methods Mol Biol 2009 561 145 159 10.1007/978-1-60327-019-9-10 19504070
27. Mice deficient in the serine/threonine protein kinase VRK1 are infertile due to a progressive loss of spermatogonia. Wiebe MS, Nichols RJ, Molitor TP, Lindgren JK, Traktman P, Biol Reprod 2010 82 182 193 10.1095/biolreprod.109. 079095 19696012
28. Efficiency assessment of the gene trap approach. Voss AK, Thomas T, Gruss P, Dev Dyn 1998 212 171 180 10.1002/(SICI)1097-0177(199806)212:2<171::AID- AJA3>3.0.CO;2-E 9626493
29. Regulation of cardiac hypertrophy by intracellular signalling pathways. Heineke J, Molkentin JD, Nat Rev Mol Cell Biol 2006 7 589 600 16936699
30. Role of an alternatively spliced form of alphaII-spectrin in localization of connexin 43 in cardiomyocytes and regulation by stress-activated protein kinase. Ursitti JA, Petrich BG, Lee PC, Resneck WG, Ye X, Yang J, Randall WR, Bloch RJ, Wang Y, J Mol Cell Cardiol 2007 42 572 581 10.1016/j.yjmcc.2006.11.018 17276456
31. A syntaxin 1, Galpha(o), and N-type calcium channel complex at a presynaptic nerve terminal: analysis by quantitative immunocolocalization. Li Q, Lau A, Morris TJ, Guo L, Fordyce CB, Stanley EF, J Neurosci 2004 24 4070 4081 10.1523/JNEUROSCI.0346-04.2004 15102922
32. SH3 domain ligand binding: What's the consensus and where's the specificity? Saksela K, Permi P, FEBS Lett 2012 586 2609 2614 10.1016/j.febslet.2012.04.042 22710157
33. Regulation of VASP phosphorylation in cardiac myocytes: differential regulation by cyclic nucleotides and modulation of protein expression in diabetic and hypertrophic heart. Sartoretto JL, Jin BY, Bauer M, Gertler FB, Liao R, Michel T, Am J Physiol Heart Circ Physiol 2009 297 1697 H1710 10.1152/ajpheart.00595.2009 19734360
34. Mammalian enabled (Mena) is a critical regulator of cardiac function. Aguilar F, Belmonte SL, Ram R, Noujaim SF, Dunaevsky O, Protack TL, Jalife J, Massey TH, Gertler FB, Blaxall BC, Am J Physiol Heart Circ Physiol 2011 300 1841 H1852 10.1152/ajpheart.01127.2010 21335464
35. Disruption of cardiac Ena-VASP protein localization in intercalated disks causes dilated cardiomyopathy. Eigenthaler M, Engelhardt S, Schinke B, Kobsar A, Schmitteckert E, Gambaryan S, Engelhardt CM, Krenn V, Eliava M, Jarchau T, et al. Am J Physiol Heart Circ Physiol 2003 285 2471 H2481 12933343
36. Ena/VASP: towards resolving a pointed controversy at the barbed end. Bear JE, Gertler FB, J Cell Sci 2009 122 1947 1953 10.1242/jcs.038125 19494122
37. The effect of divalent cations on the interaction between calf spleen profilin and different actins. Larsson H, Lindberg U, Biochim Biophys Acta 1988 953 95 105 3342244
38. Connexins: a myriad of functions extending beyond assembly of gap junction channels. Dbouk HA, Mroue RM, El-Sabban ME, Talhouk RS, Cell Commun Signal 2009 7 4 10.1186/1478-811X-7-4 19284610
39. Cytochalasin B affects the gap and tight junctions of mouse hepatocytes in vivo. Rassat J, Robenek H, Themann H, J Submicrosc Cytol 1982 14 427 439 6891002
40. Zonula occludens-1 alters connexin43 gap junction size and organization by influencing channel accretion. Hunter AW, Barker RJ, Zhu C, Gourdie RG, Mol Biol Cell 2005 16 5686 5698 10.1091/mbc.E05-08-0737 16195341
41. BLAT-the BLAST-like alignment tool. Kent WJ, Genome Res 2002 12 656 664 11932250