Serum response factor: Master regulator of the actin cytoskeleton and contractile apparatus

American Journal of Physiology - Cell Physiology

Volumn 292, Issue 1, 2007, Pages

  Miano, Joseph M ^a   Long, Xiaochun ^a   Fujiwara, Keigi ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

CArG box; Knockout; Myocardin; Smooth muscle

Indexed keywords

ACTIN; SERUM RESPONSE FACTOR;

ACTIN FILAMENT; BINDING SITE; CELL GROWTH; CELL MIGRATION; CELL PROLIFERATION; CYTOSKELETON; EUKARYOTE; GENE INACTIVATION; GENETIC ANALYSIS; GENOMICS; HUMAN; HUMAN CELL; MUSCLE CONTRACTION; MUSCLE FIBER CONTRACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW;

ACTINS; ANIMALS; BASE SEQUENCE; BINDING SITES; CYTOSKELETON; GENE EXPRESSION REGULATION; GENOMICS; HUMANS; MUSCLE CONTRACTION; SERUM RESPONSE FACTOR;

MUS; PROTISTA;

EID: 33846301667     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00386.2006     Document Type: Review

References (126)

1. Alberti S, Krause SM, Kretz O, Philippar U, Lemberger T, Casanova E, Wiebel FF, Schwarz H, Frotscher M, Schutz G, Nordheim A. Neuronal migration in the murine rostral migratory stream requires serum response factor. Proc Natl Acad Sci USA 102: 6148-6153, 2005.
2. Arsenian S, Weinhold B, Oelgeschlager M, Ruther U, Nordheim A. Serum response factor is essential for mesoderm formation during mouse embryogenesis. EMBO J 17: 6289-6299, 1998.
3. Balza RO Jr, and Misra RP. Role of the serum response factor in regulating contractile apparatus gene expression and sarcomeric integrity in cardiomyocytes. J Biol Chem 281: 6498-6510, 2006.
4. Bamburg JR, McGough A, Ono S. Putting a new twist on actin: ADF/cofilins modulate actin dynamics. Trends Cell Biol 9: 364-370, 1999.
5. Barron MR, Belaguli NS, Zhang SX, Trinh M, Iyer D, Merlo X, Lough JW, Parmacek MS, Bruneau BG, Schwartz RJ. Serum response factor, an enriched cardiac mesoderm obligatory factor, is a downstream gene target for Tbx genes. J Biol Chem 280: 11816-11828, 2005.
6. Belaguli NS, Schildmeyer LA, Schwartz RJ. Organization and myogenic restricted expression of the murine serum response factor gene: a role for autoregulation. J Biol Chem 272: 18222-18231, 1997.
7. Bond-Matthews B, Davidson N. Transcription from each of the Drosophila act5C leader exons is driven by a separate functional promoter. Gene 62: 289-300, 1988.
8. Boxer LM, Prywes R, Roeder RG, Kedes L. The sarcomeric actin CArG-binding factor is indistinguishable from the c-fos serum response factor. Mol Cell Biol 9: 515-522, 1989.
9. Brakebusch C, Fässler R. β1 integrin function in vivo: adhesion, migration and more. Cancer Metast Rev 24: 403-411, 2005.
10. Brancaccio M, Fratta L, Notte A, Hirsch E, Poulet R, Guazzone S, De Acetis M, Vecchione C, Marino G, Altruda F, Silengo L, Tarone G, Lembo G. Melusin, a muscle-specific integrin 1-interacting protein, is required to prevent cardiac failure in response to chronic pressure overload. Nat Med 9: 68-75, 2003.
11. Buchwalter G, Gross C, Wasylyk B. Ets ternary complex transcription factors. Gene 324: 1-14, 2004.
12. Calderwood DA. Talin controls integrin activation. Biochem Soc Trans 32: 434-437, 2004.
13. Casero MC, Sastre L. Characterization of a functional serum response element in the Actin403 gene promoter from the crustacean Artemia franciscana. Eur J Biochem 268: 2587-2592, 2001.
14. Chai J, Baatar D, Tarnawski A. Serum response factor promotes re-epithelialization and muscular structure restoration during gastric ulcer healing. Gastroenterology 126: 1809-1818, 2004.
15. Chai J, Jones MK, Tarnawski AS. Serum response factor is a critical requirement for VEGF signaling in endothelial cells and VEGF-induced angiogenesis. FASEB J 18: 1264-1266, 2004.
16. Chang DF, Belaguli NS, Iyer D, Roberts WB, Wu SP, Dong XR, Marx JG, Shannon-Moore M, Beckerle MC, Majesky MW, Schwartz RJ. Cysteine-rich LIM-only proteins, CRP1 and CRP2 are potent smooth muscle differentiation cofactors. Dev Cell 4: 107-118, 2003.
17. Chang F, Peter M. Yeasts make their mark. Nat Cell Biol 5: 294-299, 2003.
18. Chang VK, Fitch MJ, Donato JJ, Christensen TW, Merchant AM, Tye BK. Mcm1 binds replication origins. J Biol Chem 278: 6093-6100, 2003.
19. Chen J, Kitchen CM, Streb JW, Miano JM. Myocardin: a component of a molecular switch for smooth muscle differentiation. J Mol Cell Cardiol 34: 1345-1356, 2002.
20. Critchley DR. Cytoskeletal proteins talin and vinculin in integrin-mediated adhesion. Biochem Soc Trans 32: 831-836, 2004.
21. Dos Remedios CG, Chhabra D, Kekic M, Dedova IV, Tsubakihara M, Berry DA, Nosworthy NJ. Actin binding proteins: regulation of cytoskeletal microfilaments. Physiol Rev 83: 433-473, 2003.
22. Drake JA, Bird C, Nemesh J, Thomas DJ, Newton-Cheh C, Reymond A, Excoffier L, Attar H, Antonarakis SE, Dermitzakis ET, Hirschhorn JN. Conserved noncoding sequences are selectively constrained and not mutation cold spots. Nat Genet 38: 223-227, 2006.
23. Elble R, Tye BK. Both activation and repression of a-mating-type-specific genes in yeast require transcription factor Mcm1. Proc Natl Acad Sci USA 88: 10966-10970, 1991.
24. Escalante R, Iranfar N, Sastre L, Loomis WF. Identification of genes dependent on the MADS box transcription factor SrfA in Dictyostelium discoideum development. Eukaryot Cell 3: 564-566, 2004.
25. Escalante R, Sastre L. A serum response factor homolog is required for spore differentiation in Dictyostelium. Development 125: 3801-3808, 1998.
26. Escalante R, Vicente JJ, Moreno N, Sastre L. The MADS-box gene srfA is expressed in a complex pattern under the control of alternative promoters and is essential for different aspects of Dictyostelium development. Dev Biol 235: 314-329, 2001.
27. Escalante R, Yamada Y, Cotter D, Sastre L, Sameshima M. The MADS-box transcription factor SrfA is required for actin cytoskeleton organization and spore coat stability during Dictyostelium sporulation. Mech Dev 121: 51-56, 2004.
28. Etkin A, Alarcón JM, Weisberg SP, Touzani K, Huang YY, Nordheim A, Kandel ER. A role in learning for SRF: deletion in the adult forebrain disrupts LTD and the formation of an immediate memory of a novel context. Neuron 50: 127-143, 2006.
29. Feng Y, Walsh CA. The many faces of filamin A: a versatile molecular scaffold for cell motility and signalling. Nat Cell Biol 6: 1034-1038, 2004.
30. Fraser AG, Kamath RS, Zipperlen P, Martinez-Campos M, Sohrmann M, Ahringer J. Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 408: 325-330, 2000.
31. Fritz KE, Jarmolych J, Daoud AS. Association of DNA synthesis and apparent dedifferentiation of aortic smooth muscle cells in vitro. Exp Mol Pathol 12: 354-362, 1970.
32. Gauthier-Rouvière C, Cavadore JC, Blanchard JM, Lamb N, Fernandez A. p67SRF is constitutive nuclear protein implicated in the modulation of genes required throughout the G1 period. Cell Regul 2: 575-588, 1991.
33. Gauthier-Rouvière C, Fernandez A, Lamb NJC. ras-induced c-fos expression and proliferation in living rat fibroblasts involves C-kinase activation and the serum response element pathway. EMBO J 9: 171-180, 1990.
34. Gelman IH. The role of SSeCKS/Gravin/AKAP12 scaffolding proteins in the spatiotemporal control of signaling pathways in oncogenesis and development. Front Biosci 7: 1782-1797, 2002.
35. Geneste O, Copeland JW, Treisman R. LIM kinase and diaphenous cooperate to regulate serum response factor and actin dynamics. J Cell Biol 157: 831-838, 2002.
36. Gerthoffer WT. Actin cytoskeletal dynamics in smooth muscle contraction. Can J Physiol Pharmacol 83: 851-856, 2005.
37. Gimona M, Kaverina I, Resch GP, Vignal E, Burgstaller G. Calponin repeats regulate actin filament stability and formation of podosomes in smooth muscle cells. Mol Biol Cell 14: 2482-2491, 2003.
38. Gineitis D, Treisman R. Differential usage of signal transduction pathways defines two types of serum response factor target gene. J Biol Chem 276: 24531-24539, 2001.
39. Guillemin K, Groppe J, Dücker K, Treisman R, Hafen E, Affolter M, Krasnow MA. The pruned gene encodes the Drosophila serum response factor and regulates cytoplasmic outgrowth during terminal branching of the tracheal system. Development 122: 1353-1362, 1996.
40. Han Z, Li X, Wu J, Olson EN. A myocardin-related transcription factor regulates activity of serum response factor in Drosophila. Proc Natl Acad Sci USA 101: 12567-12572, 2004.
41. Hendrix JA, Wamhoff BR, McDonald OG, Sinha S, Yoshida T, Owens GK. 5′ CArG degeneracy in smooth muscle α-actin is required for injury-induced gene suppression in vivo. J Clin Invest 115: 418-427, 2005.
42. Higgs HN, Pollard TD. Regulation of actin filament network formation through ARP2/3 complex: activation by a diverse array of proteins. Annu Rev Biochem 70: 649-676, 2001.
43. Hill CS, Wynne J, Treisman R. The Rho family GTPases RhoA, Rac1, and cdc42Hs regulate transcriptional activation by SRF. Cell 81: 1159-1170, 1995.
44. Hofmann WA, Stojiljkovic L, Fuchsova B, Vargas GM, Mavrommatis E, Philimonenko V, Kysela K, Goodrich JA, Lessard JL, Hope TJ, Hozak P, de Lanerolle P. Actin is part of pre-initiation complexes and is necessary for transcription by RNA polymerase II. Nat Cell Biol 6: 1094-1101, 2004.
45. Hyder SM, Nawaz Z, Chiappetta C, Yokoyama K, Stancel GM. The protooncogene c-jun contains an unusual estrogen-inducible enhancer within the coding sequence. J Biol Chem 270: 8506-8513, 1995.
46. Hynes RO. Integrins: bidirectional, allosteric signaling machines. Cell 110: 673-687, 2002.
47. Johansen FE, Prywes R. Serum response factor: transcriptional regulation of genes induced by growth factors and differentiation. Biochim Biophys Acta 1242: 1-10, 1995.
48. Kaplan-Albuquerque N, Garat C, Desseva C, Jones PL, Nemenoff RA. Platelet-derived growth factor-BB-mediated activation of Akt suppresses smooth muscle-specific gene expression through inhibition of mitogen-activated protein kinase and redistribution of serum response factor. J Biol Chem 278: 39830-39838, 2003.
49. Kaplan-Albuquerque N, Van P, V, Weiser-Evans MC, Nemenoff RA. Depletion of serum response factor by RNA interference mimics the mitogenic effects of platelet derived growth factor-BB in vascular smooth muscle cells. Circ Res 97: 427-433, 2005.
50. Karakozova M, Kozak M, Wong CC, Bailey AO, Yates JR, III, Mogilner A, Zebroski H, Kashina A. Arginylation of beta-actin regulates actin cytoskeleton and cell motility. Science 313: 192-196, 2006.
51. Khachigian LM, Collins T. Inducible expression of Egr-1-dependent genes: a paradigm of transcriptional activation in vascular endothelium. Circ Res 81: 457-461, 1997.
52. Khachigian LM, Lindner V, Williams AJ, Collins T. Egr-1-induced endothelial cell gene expression: A common theme in vascular injury. Science 271: 1427-1431, 1996.
53. Khromov AS, Wang H, Choudhury N, McDuffie M, Herring BP, Nakamoto R, Owens GK, Somlyo AP, Somlyo AV. Smooth muscle of telokin-deficient mice exhibits increased sensitivity to Ca2+ and decreased cGMP-induced relaxation. Proc Natl Acad Sci USA 103: 2440-2445, 2006.
54. Kim JH, Johansen FE, Robertson N, Catino JJ, Prywes R, Kumar CC. Suppression of Ras transformation by serum response factor. J Biol Chem 269: 13740-13743, 1994.
55. Knöll B, Kretz O, Fiedler C, Alberti S, Schütz G, Frotscher M, Nordheim A. Serum response factor controls neuronal circuit assembly in the hippocampus. Nat Neurosci 9: 195-204, 2006.
56. Kovar DR, Harris ES, Mahaffy R, Higgs HN, Pollard TD. Control of the assembly of ATP- and ADP-actin by formins and profilin. Cell 124: 423-435, 2006.
57. Kumar MS, Owens GK. Combinatorial control of smooth muscle-specific gene expression. Arterioscler Thromb Vasc Biol 23: 737-747, 2003.
58. Kuwahara K, Barrientos T, Pipes GC, Li S, Olson EN. Muscle-specific signaling mechanism that links actin dynamics to serum response factor. Mol Cell Biol 25: 3173-3181, 2005.
59. Lee TC, Chow KL, Fang P, Schwartz RJ. Activation of skeletal α-actin gene transcription: the cooperative formation of serum response factor-binding complexes over positive cis-acting promoter serum response elements displaces a negative-acting nuclear factor enriched in replicating myoblasts and nonmyogenic cells. Mol Cell Biol 11: 5090-5100, 1991.
60. Leung S, Miyamoto NG. Point mutational analysis of the human c-fos serum response factor binding site. Nucleic Acids Res 14: 1177-1195, 1989.
61. Li S, Czubryt MP, McAnally J, Bassel-Duby R, Richardson JA, Wiebel FF, Nordheim A, Olson EN. Requirement for serum response factor for skeletal muscle growth and maturation revealed by tissue-specific gene deletion in mice. Proc Natl Acad Sci USA 102: 1082-1087, 2005.
62. Li S, Guan JL, Chien S. Biochemistry and biomechanics of cell motility. Annu Rev Biomed Eng 7: 105-150, 2005.
63. Li S, Wang DZ, Richardson JA, Olson EN. The serum response factor coactivator myocardin is required for vascular smooth muscle development. Proc Natl Acad Sci USA 100: 9366-9370, 2003.
64. Liu HW, Halayko AJ, Fernandes DJ, Harmon GS, McCauley JA, Kocieniewski P, McConville J, Fu Y, Forsythe SM, Kogut P, Bellam S, Dowell M, Churchill J, Lesso H, Kassiri K, Mitchell RW, Hershenson MB, Camoretti-Mercado B, Solway J. The RhoA/Rho kinase pathway regulates nuclear localization of serum response factor. Am J Respir Cell Mol Biol 29: 39-47, 2003.
65. Mack CP, Hinson JS. Regulation of smooth muscle differentiation by the myocardin family of serum response factor co-factors. J Thromb Haemost 3: 1976-1984, 2005.
66. Mejillano MR, Kojima S, Applewhite DA, Gertler FB, Svitkina TM, Borisy GG. Lamellipodial versus filopodial mode of the actin nanomachinery: pivotal role of the filament barbed end. Cell 118: 363-373, 2004.
67. Messenguy F, Dubois E. Role of MADS box proteins and their cofactors in combinatorial control of gene expression and cell development. Gene 316: 1-21, 2003.
68. Miano JM. Serum response factor: toggling between disparate programs of gene expression. J Mol Cell Cardiol 35: 577-593, 2003.
69. Miano JM, Carlson MJ, Spencer JA, Misra RP. Serum response factor-dependent regulation of the smooth muscle calponin gene. J Biol Chem 275: 9814-9822, 2000.
70. Miano JM, Ramanan N, Georger MA, de Mesy-Bentley KL, Emerson RL, Balza RO Jr, Xiao Q, Weiler H, Ginty DD, Misra RP. Restricted inactivation of serum response factor to the cardiovascular system. Proc Natl Acad Sci USA 101: 17132-17137, 2004.
71. Miano JM, Tota RR, Vlasic N, Danishefsky KJ, Stemerman MB. Early proto-oncogene expression in rat aortic smooth muscle cells following endothelial removal. Am J Pathol 137: 761-765, 1990.
72. Miano JM, Vlasic N, Tota RR, Stemerman MB. Localization of Fos and Jun proteins in rat aortic smooth muscle cells after vascular injury. Am J Pathol 142: 715-724, 1993.
73. Michie KA, Löwe J. Dynamic filaments of the bacterial cytoskeleton. Annu Rev Biochem 75: 467-492, 2006.
74. Minty A, Kedes L. Upstream regions of the human cardiac actin gene that modulate its transcription in muscle cells: presence of an evolutionarily conserved repeated motif. Mol Cell Biol 6: 2125-2136, 1986.
75. Miralles F, Posern G, Zaromytidou AI, Treisman R. Actin dynamics control SRF activity by regulation of its coactivator MAL. Cell 113: 329-342, 2003.
76. Monkley SJ, Zhou XH, Kinston SJ, Giblett SM, Hemmings L, Priddle H, Brown JE, Pritchard CA, Critchley DR, Fässler R. Disruption of the talin gene arrests mouse development at the gastrulation stage. Dev Dyn 219: 560-574, 2000.
77. Montagne J, Groppe J, Guillemin K, Krasnow MA, Gehring WJ, Affolter M. The Drosophila serum response factor gene is required for the formation of intervein tissue of the wing and is allelic to blistered. Development 122: 2589-2597, 1996.
78. Niu Z, Yu W, Zhang SX, Barron M, Belaguli NS, Schneider MD, Parmacek M, Nordheim A, Schwartz RJ. Conditional mutagenesis of the murine serum response factor gene blocks cardiogenesis and the transcription of downstream gene targets. J Biol Chem 280: 32531-32538, 2005.
79. Norman C, Runswick M, Pollock R, Treisman R. Isolation and properties of cDNA clones encoding SRF, a transcription factor that binds to the c-fos serum response element. Cell 55: 989-1003, 1988.
80. Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev 84: 767-801, 2004.
81. Parlakian A, Charvet C, Escoubet B, Mericskay M, Molkentin JD, Gary-Bobo G, De Windt LJ, Ludosky MA, Paulin D, Daegelen D, Tuil D, Li Z. Temporally controlled onset of dilated cardiomyopathy through disruption of the SRF gene in adult heart. Circulation 112: 2930-2939, 2005.
82. Parlakian A, Tuil D, Hamard G, Tavernier G, Hentzen D, Concordet JP, Paulin D, Li Z, Daegelen D. Targeted inactivation of serum response factor in the developing heart results in myocardial defects and embryonic lethality. Mol Cell Biol 24: 5281-5289, 2004.
83. Philippar U, Schratt G, Dieterich C, Müller JM, Galgóczy P, Engel FB, Keating MT, Gertler F, Schüle R, Vingron M, Nordheim A. The SRF target gene Fhl2 antagonizes RhoA/MAL-dependent activation of SRF. Mol Cell 16: 867-880, 2004.
84. Pipes GCT, Creemers EE, Olson EN. The myocardin family of transcriptional coactivators: versatile regulators of cell growth, migration, and myogenesis. Genes Dev 20: 1545-1556, 2006.
85. Pollard TD, Blanchoin L, Mullins RD. Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. Annu Rev Biophys Biomol Struct 29: 545-576, 2000.
86. Poser S, Impey S, Trinh K, Xia Z, Storm DR. SRF-dependent gene expression is required for PI3-kinase-regulated cell proliferation. EMBO J 19: 4955-4966, 2000.
87. Ramanan N, Shen Y, Sarsfield S, Lemberger T, Schütz G, Linden DJ, Ginty DD. SRF mediates activity-induced gene expression and synaptic plasticity but not neuronal viability. Nat Neurosci 8: 767, 2005.
88. Ramaswamy S, Ross KN, Lander ES, Golub TR. A molecular signature of metastasis in primary solid tumors. Nat Genet 33: 49-54, 2003.
89. Reinhard M, Jarchau T, Walter U. Actin-based motility: stop and go with Ena/VASP proteins. Trends Biochem Sci 26: 243-249, 2001.
90. Roberts RG. Dystrophins and dystrobrevins. Genome Biol 2: 3006.1-3006.7, 2001.
91. Roch F, Baonza A, Martin-Blanco E, and Garcia-Bellido A. Genetic interactions and cell behavior in blistered mutants during proliferation and differentiation of the Drosophila wing. Development 125: 1823-1832, 1998.
92. Rybakin V, Clemen CS. Coronin proteins as multifunctional regulators of the cytoskeleton and membrane trafficking. BioEssays 27: 625-632, 2005.
93. Schratt G, Philippar U, Berger J, Schwarz H, Heidenreich O, Nordheim A. Serum response factor is crucial for actin cytoskeletal organization and focal adhesion assembly in embryonic stem cells. J Cell Biol 156: 737-750, 2002.
94. Schratt G, Weinhold B, Lundberg AS, Schuck S, Berger J, Schwarz H, Weinberg RA, Rüther U, Nordheim A. Serum response factor is required for immediate-early gene activation yet is dispensable for proliferation of embryonic stem cells. Mol Cell Biol 21: 2933-2943, 2001.
95. Selvaraj A, Prywes R. Megakaryoblastic leukemia-1/2, a transcriptional co-activator of serum response factor, is required for skeletal myogenic differentiation. J Biol Chem 278: 41977-41987, 2003.
96. Selvaraj A, Prywes R. Expression profiling of serum inducible genes identifies a subset of SRF target genes that are MKL dependent (Abstract). BMC Mol Biol 5: 13, 2004.
97. Shawlot W, Deng JM, Fohn LE, Behringer RR. Restricted β-galactosidase expression of a hygromycin-lacZ gene targeted to the β-actin locus and embryonic lethality of β-actin mutant mice. Transgenic Res 7: 95-103, 1998.
98. Shibanuma M, Iwabuchi Y, Nose K. Possible involvement of Hic-5, a focal adheion protein, in the differentiation of C2C12 myoblasts. Cell Struct Funct 27: 21-27, 2002.
99. Shore P, Sharrocks AD. The MADS-box family of transcription factors. Eur J Biochem 229: 1-13, 1995.
100. Small JV, Resch GP. The comings and goings of actin: coupling protrusion and retraction in cell motility. Curr Opin Cell Biol 17: 517-523, 2005.
101. Somogyi K, Rørth P. Evidence for tension-based regulation of Drosophila MAL and SRF during invasive cell migration. Dev Cell 7: 85-93, 2004.
102. Sotiropoulos A, Gineitis D, Copeland J, Treisman R. Signal-regulated activation of serum response factor is mediated by changes in actin dynamics. Cell 98: 159-169, 1999.
103. Soulez M, Gauthier-Rouvière C, Chafey P, Hentzen D, Vandromme M, Lautredou N, Lamb N, Kahn A, Tuil D. Growth and differentiation of C2 myogenic cells are dependent on serum response factor. Mol Cell Biol 16: 6065-6074, 1996.
104. Streb JW, Miano JM. AKAP12α: an atypical serum response factor-dependent target gene. J Biol Chem 280: 4125-4134, 2005.
105. Sun HQ, Yamamoto M, Mejillano M, Yin HL. Gelsolin, a multifunctional actin regulatory protein. J Biol Chem 274: 33179-33182, 1999.
106. Sun Q, Chen G, Streb JW, Long X, Yang Y, Stoeckert CJ Jr, and Miano JM. Defining the mammalian CArGome. Genome Res 16: 197-207, 2006.
107. Sutherland JD, Witke W. Molecular genetic approaches to understanding the actin cytoskeleton. Curr Opin Cell Biol 11: 142-151, 1999.
108. Treisman R. Identification of a protein-binding site that mediates transcriptional response of the c-fos gene to serum factors. Cell 46: 567-574, 1986.
109. Verheyen EM, Cooley L. Profilin mutations disrupt multiple actin-dependent processes during Drosophila development. Development 120: 717-728, 1994.
110. Wang DZ, Chang PS, Wang Z, Sutherland L, Richardson JA, Small E, Krieg PA, Olson EN. Activation of cardiac gene expression by myocardin, a transcriptional cofactor for serum response factor. Cell 105: 851-862, 2001.
111. Wang DZ, Olson EN. Control of smooth muscle development by the myocardin family of transcriptional coactivators. Curr Opin Genet Dev 14: 558-566, 2004.
112. Wang DZ, Li S, Hockemeyer D, Sutherland L, Wang Z, Schratt G, Richardson JA, Nordheim A, Olson EN. Potentiation of serum response factor activity by a family of myocardin-related transcription factors. Proc Natl Acad Sci USA 99: 14855-14860, 2002.
113. Wang Z, Wang DZ, Hockemeyer D, McNally J, Nordheim A, Olson EN. Myocardin and ternary complex factors compete for SRF to control smooth muscle gene expression. Nature 428: 185-189, 2004.
114. Wear MA, Cooper JA. Capping protein: new insights into mechanism and regulation. Trends Biochem Sci 29: 418-428, 2004.
115. Wechsler-Reya RJ, Elliott KJ, Prendergast GC. A role for the putative tumor suppressor Bin1 in muscle cell differentiation. Mol Cell Biol 18: 566-575, 1998.
116. Wei L, Wang L, Carson JA, Agan JE, Imanaka-Yoshida K, Schwartz RJ. β1 integrin and organized actin filaments facilitate cardiomyocyte- specific RhoA-dependent activation of the skeletal α-actin promoter. FASEB J 15: 785-796, 2001.
117. Witke W. The role of profilin complexes in cell motility and other cellular processes. Trends Cell Biol 14: 461-469, 2004.
118. Woods A, Couchman JR. Syndecan-4 and focal adhesion function. Curr Opin Cell Biol 13: 578-583, 2001.
119. Wynne J, Treisman R. SRF and MCM1 have related but distinct DNA binding specificities. Nucleic Acids Res 20: 3297-3303, 1992.
120. Yang N, Higuchi O, Ohashi K, Nagata K, Wada A, Kangawa K, Nishida E, Mizuno K. Cofilin phosphorylation by LIM-kinase 1 and its role in Rac-mediated actin reorganization. Nature 393: 809-812, 1998.
121. Yoshida T, Kawai-Kowase K, Owens GK. Forced expression of myocardin is not sufficient for induction of smooth muscle differentiation in multipotential cells. Arterioscler Thromb Vasc Biol 24: 1596-1601, 2004.
122. Zaromytidou AI, Miralles F, Treisman R. MAL and ternary complex factor use different mechanisms to contact a common surface on the serum response factor DNA-binding domain. Mol Cell Biol 26: 4134-4148, 2006.
123. Zemljic-Harpf AE, Ponrartana S, Avalos RT, Jordan MC, Roos KP, Dalton ND, Phan VQ, Adamson ED, Ross RS. Heterozygous inactivation of the vinculin gene predisposes to stress-induced cardiomyopathy. Am J Pathol 165: 1033-1044, 2004.
124. Zhang SX, Gras EG, Wycuff DR, Marriot SJ, Kadeer N, Yu W, Olson EN, Garry DJ, Parmacek MS, Schwartz RJ. Identification of direct serum response factor gene targets during DMSO induced P19 cardiac cell differentiation. J Biol Chem 280: 19115-19126, 2005.
125. Zhang X, Azhar G, Chai J, Sheridan P, Nagano K, Brown T, Yang J, Khrapko K, Borras AM, Lawitts J, Misra RP, Wei JY. Cardiomyopathy in transgenic mice with cardiac-specific overexpression of serum response factor. Am J Physiol Heart Circ Physiol 280: H1782-H1792, 2001.
126. Zhang X, Chai J, Azhar G, Sheridan P, Borras AM, Furr MC, Khrapko K, Lawitts J, Misra RP, Wei JY. Early postnatal cardiac changes and premature death in transgenic mice overexpressing a mutant form of serum response factor. J Biol Chem 276: 40033-40040, 2001.