{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,20]],"date-time":"2026-09-20T15:13:45Z","timestamp":1789917225297,"version":"4.0.1"},"reference-count":55,"publisher":"National Academy of Sciences","issue":"34","content-domain":{"domain":["www.pnas.org"],"crossmark-restriction":true},"short-container-title":["Proc. Natl. Acad. Sci. U.S.A."],"published-print":{"date-parts":[[2016,8,23]]},"abstract":"<jats:title>Significance<\/jats:title>\n                  <jats:p>Debilitating heart conditions, dilated cardiomyopathy (DCM) and hypertrophic cardiomyopathy (HCM), are often due to inherited or acquired mutations in genes that encode specific components of adhesion complexes. In muscle tissue, some of these adhesion complexes have specialized structures, called intercalated discs, which are important for contraction and coordinated movement. Here we provide molecular insights into the cytoskeletal protein metavinculin, which is necessary for the proper development and maintenance of heart tissue and is mutated in human DCM and HCM. We show that the binding of lipid causes metavinculin to dimerize and involves a specific metavinculin amino acid associated with severe DCM\/HCM. Collectively, our studies provide insight into how such metavinculin mutations in components of adhesion complexes lead to cardiomyopathies.<\/jats:p>","DOI":"10.1073\/pnas.1600702113","type":"journal-article","created":{"date-parts":[[2016,8,8]],"date-time":"2016-08-08T23:03:32Z","timestamp":1470697412000},"page":"9539-9544","update-policy":"https:\/\/doi.org\/10.1073\/pnas.cm10313","source":"Crossref","is-referenced-by-count":24,"title":["Differential lipid binding of vinculin isoforms promotes quasi-equivalent dimerization"],"prefix":"10.1073","volume":"113","author":[{"given":"Krishna","family":"Chinthalapudi","sequence":"first","affiliation":[{"name":"Cell Adhesion Laboratory, Department of Cancer Biology, The Scripps Research Institute, Jupiter, FL 33458;"},{"name":"Department of Immunology and Microbial Sciences, The Scripps Research Institute, Jupiter, FL 33458;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Erumbi S.","family":"Rangarajan","sequence":"additional","affiliation":[{"name":"Cell Adhesion Laboratory, Department of Cancer Biology, The Scripps Research Institute, Jupiter, FL 33458;"},{"name":"Department of Immunology and Microbial Sciences, The Scripps Research Institute, Jupiter, FL 33458;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David T.","family":"Brown","sequence":"additional","affiliation":[{"name":"Department of Biochemistry, University of Mississippi Medical Center, Jackson, MS 39216"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tina","family":"Izard","sequence":"additional","affiliation":[{"name":"Cell Adhesion Laboratory, Department of Cancer Biology, The Scripps Research Institute, Jupiter, FL 33458;"},{"name":"Department of Immunology and Microbial Sciences, The Scripps Research Institute, Jupiter, FL 33458;"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"341","published-online":{"date-parts":[[2016,8,8]]},"reference":[{"key":"e_1_3_4_1_2","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1242\/dev.125.2.327","article-title":"Vinculin knockout results in heart and brain defects during embryonic development","volume":"125","author":"Xu W","year":"1998","unstructured":"W Xu, H Baribault, ED Adamson, Vinculin knockout results in heart and brain defects during embryonic development. Development 125, 327\u2013337 (1998).","journal-title":"Development"},{"key":"e_1_3_4_2_2","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1002\/cm.970220206","article-title":"Overexpression of vinculin suppresses cell motility in BALB\/c 3T3 cells","volume":"22","author":"Rodr\u00edguez Fern\u00e1ndez JL","year":"1992","unstructured":"JL Rodr\u00edguez Fern\u00e1ndez, B Geiger, D Salomon, A Ben-Ze\u2019ev, Overexpression of vinculin suppresses cell motility in BALB\/c 3T3 cells. Cell Motil Cytoskeleton 22, 127\u2013134 (1992).","journal-title":"Cell Motil Cytoskeleton"},{"key":"e_1_3_4_3_2","doi-asserted-by":"crossref","first-page":"9161","DOI":"10.1073\/pnas.92.20.9161","article-title":"Targeted disruption of vinculin genes in F9 and embryonic stem cells changes cell morphology, adhesion, and locomotion","volume":"92","author":"Coll JL","year":"1995","unstructured":"JL Coll, , Targeted disruption of vinculin genes in F9 and embryonic stem cells changes cell morphology, adhesion, and locomotion. Proc Natl Acad Sci USA 92, 9161\u20139165 (1995).","journal-title":"Proc Natl Acad Sci USA"},{"key":"e_1_3_4_4_2","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1083\/jcb.107.2.545","article-title":"Immunolocalization of meta-vinculin in human smooth and cardiac muscles","volume":"107","author":"Belkin AM","year":"1988","unstructured":"AM Belkin, OI Ornatsky, MA Glukhova, VE Koteliansky, Immunolocalization of meta-vinculin in human smooth and cardiac muscles. J Cell Biol 107, 545\u2013553 (1988).","journal-title":"J Cell Biol"},{"key":"e_1_3_4_5_2","doi-asserted-by":"crossref","first-page":"6631","DOI":"10.1016\/S0021-9258(18)68688-0","article-title":"Diversity of vinculin\/meta-vinculin in human tissues and cultivated cells. Expression of muscle specific variants of vinculin in human aorta smooth muscle cells","volume":"263","author":"Belkin AM","year":"1988","unstructured":"AM Belkin, OI Ornatsky, AE Kabakov, MA Glukhova, VE Koteliansky, Diversity of vinculin\/meta-vinculin in human tissues and cultivated cells. Expression of muscle specific variants of vinculin in human aorta smooth muscle cells. J Biol Chem 263, 6631\u20136635 (1988).","journal-title":"J Biol Chem"},{"key":"e_1_3_4_6_2","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1016\/S0014-5793(98)00723-6","article-title":"Differential actin organization by vinculin isoforms: Implications for cell type-specific microfilament anchorage","volume":"431","author":"R\u00fcdiger M","year":"1998","unstructured":"M R\u00fcdiger, N Korneeva, C Schwienbacher, EE Weiss, BM Jockusch, Differential actin organization by vinculin isoforms: Implications for cell type-specific microfilament anchorage. FEBS Lett 431, 49\u201354 (1998).","journal-title":"FEBS Lett"},{"key":"e_1_3_4_7_2","doi-asserted-by":"crossref","first-page":"767","DOI":"10.1111\/j.1432-1033.1992.tb16692.x","article-title":"An additional exon in the human vinculin gene specifically encodes meta-vinculin-specific difference peptide. Cross-species comparison reveals variable and conserved motifs in the meta-vinculin insert","volume":"204","author":"Koteliansky VE","year":"1992","unstructured":"VE Koteliansky, , An additional exon in the human vinculin gene specifically encodes meta-vinculin-specific difference peptide. Cross-species comparison reveals variable and conserved motifs in the meta-vinculin insert. Eur J Biochem 204, 767\u2013772 (1992).","journal-title":"Eur J Biochem"},{"key":"e_1_3_4_8_2","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1161\/01.CIR.95.1.17","article-title":"Dilated cardiomyopathy associated with deficiency of the cytoskeletal protein metavinculin","volume":"95","author":"Maeda M","year":"1997","unstructured":"M Maeda, E Holder, B Lowes, S Valent, RD Bies, Dilated cardiomyopathy associated with deficiency of the cytoskeletal protein metavinculin. Circulation 95, 17\u201320 (1997).","journal-title":"Circulation"},{"key":"e_1_3_4_9_2","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1161\/hc0402.102930","article-title":"Metavinculin mutations alter actin interaction in dilated cardiomyopathy","volume":"105","author":"Olson TM","year":"2002","unstructured":"TM Olson, , Metavinculin mutations alter actin interaction in dilated cardiomyopathy. Circulation 105, 431\u2013437 (2002).","journal-title":"Circulation"},{"key":"e_1_3_4_10_2","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1016\/j.ymgme.2005.08.006","article-title":"Identification of a metavinculin missense mutation, R975W, associated with both hypertrophic and dilated cardiomyopathy","volume":"87","author":"Vasile VC","year":"2006","unstructured":"VC Vasile, , Identification of a metavinculin missense mutation, R975W, associated with both hypertrophic and dilated cardiomyopathy. Mol Genet Metab 87, 169\u2013174 (2006).","journal-title":"Mol Genet Metab"},{"key":"e_1_3_4_11_2","doi-asserted-by":"crossref","first-page":"1033","DOI":"10.1016\/S0002-9440(10)63364-0","article-title":"Heterozygous inactivation of the vinculin gene predisposes to stress-induced cardiomyopathy","volume":"165","author":"Zemljic-Harpf AE","year":"2004","unstructured":"AE Zemljic-Harpf, , Heterozygous inactivation of the vinculin gene predisposes to stress-induced cardiomyopathy. Am J Pathol 165, 1033\u20131044 (2004).","journal-title":"Am J Pathol"},{"key":"e_1_3_4_12_2","doi-asserted-by":"crossref","first-page":"1189","DOI":"10.1016\/j.str.2004.05.009","article-title":"Crystal structure of human vinculin","volume":"12","author":"Borgon RA","year":"2004","unstructured":"RA Borgon, C Vonrhein, G Bricogne, PR Bois, T Izard, Crystal structure of human vinculin. Structure 12, 1189\u20131197 (2004).","journal-title":"Structure"},{"key":"e_1_3_4_13_2","doi-asserted-by":"crossref","first-page":"e10679","DOI":"10.1371\/journal.pone.0010679","article-title":"A helix replacement mechanism directs metavinculin functions","volume":"5","author":"Rangarajan ES","year":"2010","unstructured":"ES Rangarajan, JH Lee, SD Yogesha, T Izard, A helix replacement mechanism directs metavinculin functions. PLoS One 5, e10679 (2010).","journal-title":"PLoS One"},{"key":"e_1_3_4_14_2","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1038\/nature02281","article-title":"Vinculin activation by talin through helical bundle conversion","volume":"427","author":"Izard T","year":"2004","unstructured":"T Izard, , Vinculin activation by talin through helical bundle conversion. Nature 427, 171\u2013175 (2004).","journal-title":"Nature"},{"key":"e_1_3_4_15_2","doi-asserted-by":"crossref","first-page":"27667","DOI":"10.1074\/jbc.M403076200","article-title":"Structural basis for amplifying vinculin activation by talin","volume":"279","author":"Izard T","year":"2004","unstructured":"T Izard, C Vonrhein, Structural basis for amplifying vinculin activation by talin. J Biol Chem 279, 27667\u201327678 (2004).","journal-title":"J Biol Chem"},{"key":"e_1_3_4_16_2","doi-asserted-by":"crossref","first-page":"6112","DOI":"10.1128\/MCB.25.14.6112-6122.2005","article-title":"Structural dynamics of \u03b1-actinin-vinculin interactions","volume":"25","author":"Bois PR","year":"2005","unstructured":"PR Bois, RA Borgon, C Vonrhein, T Izard, Structural dynamics of \u03b1-actinin-vinculin interactions. Mol Cell Biol 25, 6112\u20136122 (2005).","journal-title":"Mol Cell Biol"},{"key":"e_1_3_4_17_2","doi-asserted-by":"crossref","first-page":"7228","DOI":"10.1074\/jbc.M510397200","article-title":"The vinculin binding sites of talin and \u03b1-actinin are sufficient to activate vinculin","volume":"281","author":"Bois PR","year":"2006","unstructured":"PR Bois, BP O\u2019Hara, D Nietlispach, J Kirkpatrick, T Izard, The vinculin binding sites of talin and \u03b1-actinin are sufficient to activate vinculin. J Biol Chem 281, 7228\u20137236 (2006).","journal-title":"J Biol Chem"},{"key":"e_1_3_4_18_2","doi-asserted-by":"crossref","first-page":"744","DOI":"10.1038\/308744a0","article-title":"An interaction between vinculin and talin","volume":"308","author":"Burridge K","year":"1984","unstructured":"K Burridge, P Mangeat, An interaction between vinculin and talin. Nature 308, 744\u2013746 (1984).","journal-title":"Nature"},{"key":"e_1_3_4_19_2","doi-asserted-by":"crossref","first-page":"554","DOI":"10.1016\/0006-291X(87)90564-X","article-title":"Specific interaction of vinculin with \u03b1-actinin","volume":"146","author":"Wachsstock DH","year":"1987","unstructured":"DH Wachsstock, JA Wilkins, S Lin, Specific interaction of vinculin with \u03b1-actinin. Biochem Biophys Res Commun 146, 554\u2013560 (1987).","journal-title":"Biochem Biophys Res Commun"},{"key":"e_1_3_4_20_2","doi-asserted-by":"crossref","first-page":"847","DOI":"10.1083\/jcb.142.3.847","article-title":"\u03b1-Catenin-vinculin interaction functions to organize the apical junctional complex in epithelial cells","volume":"142","author":"Watabe-Uchida M","year":"1998","unstructured":"M Watabe-Uchida, , \u03b1-Catenin-vinculin interaction functions to organize the apical junctional complex in epithelial cells. J Cell Biol 142, 847\u2013857 (1998).","journal-title":"J Cell Biol"},{"key":"e_1_3_4_21_2","doi-asserted-by":"crossref","first-page":"567","DOI":"10.1242\/jcs.056432","article-title":"Vinculin regulates cell-surface E-cadherin expression by binding to \u03b2-catenin","volume":"123","author":"Peng X","year":"2010","unstructured":"X Peng, LE Cuff, CD Lawton, KA DeMali, Vinculin regulates cell-surface E-cadherin expression by binding to \u03b2-catenin. J Cell Sci 123, 567\u2013577 (2010).","journal-title":"J Cell Sci"},{"key":"e_1_3_4_22_2","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/0092-8674(82)90377-4","article-title":"High-affinity interaction of vinculin with actin filaments in vitro","volume":"28","author":"Wilkins JA","year":"1982","unstructured":"JA Wilkins, S Lin, High-affinity interaction of vinculin with actin filaments in vitro. Cell 28, 83\u201390 (1982).","journal-title":"Cell"},{"key":"e_1_3_4_23_2","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1038\/373261a0","article-title":"F-actin binding site masked by the intramolecular association of vinculin head and tail domains","volume":"373","author":"Johnson RP","year":"1995","unstructured":"RP Johnson, SW Craig, F-actin binding site masked by the intramolecular association of vinculin head and tail domains. Nature 373, 261\u2013264 (1995).","journal-title":"Nature"},{"key":"e_1_3_4_24_2","doi-asserted-by":"crossref","first-page":"476","DOI":"10.1126\/science.3099391","article-title":"The cytoskeletal protein vinculin contains transformation-sensitive, covalently bound lipid","volume":"235","author":"Burn P","year":"1987","unstructured":"P Burn, MM Burger, The cytoskeletal protein vinculin contains transformation-sensitive, covalently bound lipid. Science 235, 476\u2013479 (1987).","journal-title":"Science"},{"key":"e_1_3_4_25_2","doi-asserted-by":"crossref","first-page":"1136","DOI":"10.1111\/j.1432-1033.1997.01136.x","article-title":"Characterization of two F-actin-binding and oligomerization sites in the cell-contact protein vinculin","volume":"247","author":"H\u00fcttelmaier S","year":"1997","unstructured":"S H\u00fcttelmaier, P Bubeck, M R\u00fcdiger, BM Jockusch, Characterization of two F-actin-binding and oligomerization sites in the cell-contact protein vinculin. Eur J Biochem 247, 1136\u20131142 (1997).","journal-title":"Eur J Biochem"},{"key":"e_1_3_4_26_2","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1016\/S0960-9822(98)70199-X","article-title":"The interaction of the cell-contact proteins VASP and vinculin is regulated by phosphatidylinositol-4,5-bisphosphate","volume":"8","author":"H\u00fcttelmaier S","year":"1998","unstructured":"S H\u00fcttelmaier, , The interaction of the cell-contact proteins VASP and vinculin is regulated by phosphatidylinositol-4,5-bisphosphate. Curr Biol 8, 479\u2013488 (1998).","journal-title":"Curr Biol"},{"key":"e_1_3_4_27_2","doi-asserted-by":"crossref","first-page":"753","DOI":"10.1042\/bj3180753","article-title":"The focal-adhesion vasodilator-stimulated phosphoprotein (VASP) binds to the proline-rich domain in vinculin","volume":"318","author":"Brindle NP","year":"1996","unstructured":"NP Brindle, MR Holt, JE Davies, CJ Price, DR Critchley, The focal-adhesion vasodilator-stimulated phosphoprotein (VASP) binds to the proline-rich domain in vinculin. Biochem J 318, 753\u2013757 (1996).","journal-title":"Biochem J"},{"key":"e_1_3_4_28_2","doi-asserted-by":"crossref","first-page":"565","DOI":"10.1016\/j.tibs.2004.09.001","article-title":"Vinculin: A dynamic regulator of cell adhesion","volume":"29","author":"Demali KA","year":"2004","unstructured":"KA Demali, Vinculin: A dynamic regulator of cell adhesion. Trends Biochem Sci 29, 565\u2013567 (2004).","journal-title":"Trends Biochem Sci"},{"key":"e_1_3_4_29_2","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1002\/pro.2041","article-title":"Crystal structure of vinculin in complex with vinculin binding site 50 (VBS50), the integrin binding site 2 (IBS2) of talin","volume":"21","author":"Yogesha SD","year":"2012","unstructured":"SD Yogesha, ES Rangarajan, C Vonrhein, G Bricogne, T Izard, Crystal structure of vinculin in complex with vinculin binding site 50 (VBS50), the integrin binding site 2 (IBS2) of talin. Protein Sci 21, 583\u2013588 (2012).","journal-title":"Protein Sci"},{"key":"e_1_3_4_30_2","doi-asserted-by":"crossref","first-page":"1471","DOI":"10.1002\/pro.671","article-title":"Intermolecular versus intramolecular interactions of the vinculin binding site 33 of talin","volume":"20","author":"Yogesha SD","year":"2011","unstructured":"SD Yogesha, A Sharff, G Bricogne, T Izard, Intermolecular versus intramolecular interactions of the vinculin binding site 33 of talin. Protein Sci 20, 1471\u20131476 (2011).","journal-title":"Protein Sci"},{"key":"e_1_3_4_31_2","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1083\/jcb.200605091","article-title":"Shigella applies molecular mimicry to subvert vinculin and invade host cells","volume":"175","author":"Izard T","year":"2006","unstructured":"T Izard, G Tran Van Nhieu, PR Bois, Shigella applies molecular mimicry to subvert vinculin and invade host cells. J Cell Biol 175, 465\u2013475 (2006).","journal-title":"J Cell Biol"},{"key":"e_1_3_4_32_2","doi-asserted-by":"crossref","first-page":"23214","DOI":"10.1074\/jbc.M110.184283","article-title":"Novel vinculin binding site of the IpaA invasin of Shigella","volume":"286","author":"Park H","year":"2011","unstructured":"H Park, C Valencia-Gallardo, A Sharff, G Tran Van Nhieu, T Izard, Novel vinculin binding site of the IpaA invasin of Shigella. J Biol Chem 286, 23214\u201323221 (2011).","journal-title":"J Biol Chem"},{"key":"e_1_3_4_33_2","doi-asserted-by":"crossref","first-page":"4588","DOI":"10.1038\/sj.emboj.7601863","article-title":"Vinculin binding in its closed conformation by a helix addition mechanism","volume":"26","author":"Nhieu GT","year":"2007","unstructured":"GT Nhieu, T Izard, Vinculin binding in its closed conformation by a helix addition mechanism. EMBO J 26, 4588\u20134596 (2007).","journal-title":"EMBO J"},{"key":"e_1_3_4_34_2","doi-asserted-by":"crossref","first-page":"531","DOI":"10.1038\/381531a0","article-title":"Regulation of vinculin binding to talin and actin by phosphatidyl-inositol-4-5-bisphosphate","volume":"381","author":"Gilmore AP","year":"1996","unstructured":"AP Gilmore, K Burridge, Regulation of vinculin binding to talin and actin by phosphatidyl-inositol-4-5-bisphosphate. Nature 381, 531\u2013535 (1996).","journal-title":"Nature"},{"key":"e_1_3_4_35_2","doi-asserted-by":"crossref","first-page":"827","DOI":"10.1042\/bj3140827","article-title":"Acidic phospholipids inhibit the intramolecular association between the N- and C-terminal regions of vinculin, exposing actin-binding and protein kinase C phosphorylation sites","volume":"314","author":"Weekes J","year":"1996","unstructured":"J Weekes, ST Barry, DR Critchley, Acidic phospholipids inhibit the intramolecular association between the N- and C-terminal regions of vinculin, exposing actin-binding and protein kinase C phosphorylation sites. Biochem J 314, 827\u2013832 (1996).","journal-title":"Biochem J"},{"key":"e_1_3_4_36_2","doi-asserted-by":"crossref","first-page":"603","DOI":"10.1016\/S0092-8674(00)81549-4","article-title":"Crystal structure of the vinculin tail suggests a pathway for activation","volume":"99","author":"Bakolitsa C","year":"1999","unstructured":"C Bakolitsa, JM de Pereda, CR Bagshaw, DR Critchley, RC Liddington, Crystal structure of the vinculin tail suggests a pathway for activation. Cell 99, 603\u2013613 (1999).","journal-title":"Cell"},{"key":"e_1_3_4_37_2","doi-asserted-by":"crossref","first-page":"638","DOI":"10.1126\/science.1162912","article-title":"Stretching single talin rod molecules activates vinculin binding","volume":"323","author":"del Rio A","year":"2009","unstructured":"A del Rio, , Stretching single talin rod molecules activates vinculin binding. Science 323, 638\u2013641 (2009).","journal-title":"Science"},{"key":"e_1_3_4_38_2","doi-asserted-by":"crossref","first-page":"643","DOI":"10.1083\/jcb.201404128","article-title":"Lipid binding promotes oligomerization and focal adhesion activity of vinculin","volume":"207","author":"Chinthalapudi K","year":"2014","unstructured":"K Chinthalapudi, , Lipid binding promotes oligomerization and focal adhesion activity of vinculin. J Cell Biol 207, 643\u2013656 (2014).","journal-title":"J Cell Biol"},{"key":"e_1_3_4_39_2","doi-asserted-by":"crossref","first-page":"45103","DOI":"10.1074\/jbc.M111.244293","article-title":"The vinculin C-terminal hairpin mediates F-actin bundle formation, focal adhesion, and cell mechanical properties","volume":"286","author":"Shen K","year":"2011","unstructured":"K Shen, , The vinculin C-terminal hairpin mediates F-actin bundle formation, focal adhesion, and cell mechanical properties. J Biol Chem 286, 45103\u201345115 (2011).","journal-title":"J Biol Chem"},{"key":"e_1_3_4_40_2","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1074\/jbc.275.1.95","article-title":"Actin activates a cryptic dimerization potential of the vinculin tail domain","volume":"275","author":"Johnson RP","year":"2000","unstructured":"RP Johnson, SW Craig, Actin activates a cryptic dimerization potential of the vinculin tail domain. J Biol Chem 275, 95\u2013105 (2000).","journal-title":"J Biol Chem"},{"key":"e_1_3_4_41_2","doi-asserted-by":"crossref","first-page":"31533","DOI":"10.1074\/jbc.M314245200","article-title":"Comparative biochemical analysis suggests that vinculin and metavinculin cooperate in muscular adhesion sites","volume":"279","author":"Witt S","year":"2004","unstructured":"S Witt, A Zieseniss, U Fock, BM Jockusch, S Illenberger, Comparative biochemical analysis suggests that vinculin and metavinculin cooperate in muscular adhesion sites. J Biol Chem 279, 31533\u201331543 (2004).","journal-title":"J Biol Chem"},{"key":"e_1_3_4_42_2","doi-asserted-by":"crossref","first-page":"2758","DOI":"10.1021\/acs.biochem.5b00015","article-title":"Lipid-directed vinculin dimerization","volume":"54","author":"Chinthalapudi K","year":"2015","unstructured":"K Chinthalapudi, DN Patil, ES Rangarajan, C Rader, T Izard, Lipid-directed vinculin dimerization. Biochemistry 54, 2758\u20132768 (2015).","journal-title":"Biochemistry"},{"key":"e_1_3_4_43_2","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1101\/SQB.1962.027.001.005","article-title":"Physical principles in the construction of regular viruses","volume":"27","author":"Caspar DL","year":"1962","unstructured":"DL Caspar, A Klug, Physical principles in the construction of regular viruses. Cold Spring Harb Symp Quant Biol 27, 1\u201324 (1962).","journal-title":"Cold Spring Harb Symp Quant Biol"},{"key":"e_1_3_4_44_2","doi-asserted-by":"crossref","first-page":"1240","DOI":"10.1073\/pnas.96.4.1240","article-title":"Principles of quasi-equivalence and Euclidean geometry govern the assembly of cubic and dodecahedral cores of pyruvate dehydrogenase complexes","volume":"96","author":"Izard T","year":"1999","unstructured":"T Izard, , Principles of quasi-equivalence and Euclidean geometry govern the assembly of cubic and dodecahedral cores of pyruvate dehydrogenase complexes. Proc Natl Acad Sci USA 96, 1240\u20131245 (1999).","journal-title":"Proc Natl Acad Sci USA"},{"key":"e_1_3_4_45_2","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1016\/j.molcel.2005.11.020","article-title":"Three-dimensional structure of vinculin bound to actin filaments","volume":"21","author":"Janssen ME","year":"2006","unstructured":"ME Janssen, , Three-dimensional structure of vinculin bound to actin filaments. Mol Cell 21, 271\u2013281 (2006).","journal-title":"Mol Cell"},{"key":"e_1_3_4_46_2","doi-asserted-by":"crossref","first-page":"2548","DOI":"10.1074\/jbc.R115.686493","article-title":"Mechanisms and functions of vinculin interactions with phospholipids at cell adhesion sites","volume":"291","author":"Izard T","year":"2016","unstructured":"T Izard, DT Brown, Mechanisms and functions of vinculin interactions with phospholipids at cell adhesion sites. J Biol Chem 291, 2548\u20132555 (2016).","journal-title":"J Biol Chem"},{"key":"e_1_3_4_47_2","doi-asserted-by":"crossref","first-page":"7223","DOI":"10.1074\/jbc.M807842200","article-title":"Lipid binding to the tail domain of vinculin: Specificity and the role of the N and C termini","volume":"284","author":"Palmer SM","year":"2009","unstructured":"SM Palmer, MP Playford, SW Craig, MD Schaller, SL Campbell, Lipid binding to the tail domain of vinculin: Specificity and the role of the N and C termini. J Biol Chem 284, 7223\u20137231 (2009).","journal-title":"J Biol Chem"},{"key":"e_1_3_4_48_2","doi-asserted-by":"crossref","first-page":"695","DOI":"10.1083\/jcb.200204153","article-title":"The relationship between force and focal complex development","volume":"159","author":"Galbraith CG","year":"2002","unstructured":"CG Galbraith, KM Yamada, MP Sheetz, The relationship between force and focal complex development. J Cell Biol 159, 695\u2013705 (2002).","journal-title":"J Cell Biol"},{"key":"e_1_3_4_49_2","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1083\/jcb.200302001","article-title":"Talin1 is critical for force-dependent reinforcement of initial integrin-cytoskeleton bonds but not tyrosine kinase activation","volume":"163","author":"Giannone G","year":"2003","unstructured":"G Giannone, G Jiang, DH Sutton, DR Critchley, MP Sheetz, Talin1 is critical for force-dependent reinforcement of initial integrin-cytoskeleton bonds but not tyrosine kinase activation. J Cell Biol 163, 409\u2013419 (2003).","journal-title":"J Cell Biol"},{"key":"e_1_3_4_50_2","doi-asserted-by":"crossref","first-page":"4605","DOI":"10.1242\/jcs.00792","article-title":"Early molecular events in the assembly of matrix adhesions at the leading edge of migrating cells","volume":"116","author":"Zaidel-Bar R","year":"2003","unstructured":"R Zaidel-Bar, C Ballestrem, Z Kam, B Geiger, Early molecular events in the assembly of matrix adhesions at the leading edge of migrating cells. J Cell Sci 116, 4605\u20134613 (2003).","journal-title":"J Cell Sci"},{"key":"e_1_3_4_51_2","doi-asserted-by":"crossref","first-page":"34043","DOI":"10.18632\/oncotarget.5868","article-title":"Vinculin-cell membrane interactions","volume":"6","author":"Brown DT","year":"2015","unstructured":"DT Brown, T Izard, Vinculin-cell membrane interactions. Oncotarget 6, 34043\u201334044 (2015).","journal-title":"Oncotarget"},{"key":"e_1_3_4_52_2","first-page":"292fs26","article-title":"Cardiac aging: Send in the vinculin reinforcements","volume":"7","author":"DeLeon-Pennell KY","year":"2015","unstructured":"KY DeLeon-Pennell, ML Lindsey, Cardiac aging: Send in the vinculin reinforcements. Sci Transl Med 7, 292fs26 (2015).","journal-title":"Sci Transl Med"},{"key":"e_1_3_4_53_2","doi-asserted-by":"crossref","first-page":"292ra99","DOI":"10.1126\/scitranslmed.aaa5843","article-title":"Vinculin network-mediated cytoskeletal remodeling regulates contractile function in the aging heart","volume":"7","author":"Kaushik G","year":"2015","unstructured":"G Kaushik, , Vinculin network-mediated cytoskeletal remodeling regulates contractile function in the aging heart. Sci Transl Med 7, 292ra99 (2015).","journal-title":"Sci Transl Med"},{"key":"e_1_3_4_54_2","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1107\/S0907444911007773","article-title":"Data processing and analysis with the autoPROC toolbox","volume":"67","author":"Vonrhein C","year":"2011","unstructured":"C Vonrhein, , Data processing and analysis with the autoPROC toolbox. Acta Crystallogr D Biol Crystallogr 67, 293\u2013302 (2011).","journal-title":"Acta Crystallogr D Biol Crystallogr"},{"key":"e_1_3_4_55_2","volume-title":"BUSTER version 2.9","author":"Bricogne G","year":"2011","unstructured":"G Bricogne, BUSTER version 2.9 (Global Phasing, Cambridge, UK, 2011)."}],"container-title":["Proceedings of the National Academy of Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/pnas.org\/doi\/pdf\/10.1073\/pnas.1600702113","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,6,7]],"date-time":"2022-06-07T10:32:40Z","timestamp":1654597960000},"score":1,"resource":{"primary":{"URL":"https:\/\/pnas.org\/doi\/full\/10.1073\/pnas.1600702113"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016,8,8]]},"references-count":55,"journal-issue":{"issue":"34","published-print":{"date-parts":[[2016,8,23]]}},"alternative-id":["10.1073\/pnas.1600702113"],"URL":"https:\/\/doi.org\/10.1073\/pnas.1600702113","relation":{},"ISSN":["0027-8424","1091-6490"],"issn-type":[{"value":"0027-8424","type":"print"},{"value":"1091-6490","type":"electronic"}],"subject":[],"published":{"date-parts":[[2016,8,8]]},"assertion":[{"value":"2016-08-08","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}