ATP-dependent chromatin remodeling complex SWI/SNF in cardiogenesis and cardiac progenitor cell development

Abstract

The recent identification of cardiac progenitor cells (CPCs) provides a new paradigm for studying and treating heart disease. To realize the full potential of CPCs for therapeutic purposes, it is essential to understand the genetic and epigenetic mechanisms guiding CPC differentiation into cardiomyocytes, smooth muscle, or endothelial cells. ATP-dependent chromatin remodelers mediate one critical epigenetic mechanism. These large multiprotein complexes open up chromatin to modulate transcription factor access to DNA. SWI/SNF, one of the major types of chromatin remodelers, plays a key role in various aspects of development (de la Serna et al., 2006; Wu et al., 2009), including heart development and disease (Lickert et al., 2004; Wang et al., 2004; Huang et al., 2008; Stankunas et al., 2008; Hang et al., 2010). In this review, we describe the specific function of various SWI/SNF components in cardiogenesis and cardiac progenitor cell (CPC) self-renewal and differentiation. We envision that a detailed understanding of the SWI/SNF in heart development and CPC formation and differentiation will generate novel insights into epigenetic mechanisms that govern CPC differentiation and may have significant implications in understanding and treating heart disease.

Keywords

ATP-dependent chromatin remodeling / SWI/SNF / cardiogenesis and cardiac progenitor cell

References

[1] Abu-Issa R, Smyth G, Smoak I, Yamamura K, Meyers E N (2002). Fgf8 is required for pharyngeal arch and cardiovascular development in the mouse. Development, 129(19): 4613–4625

[2] Arceci R J, King A A, Simon M C, Orkin S H, Wilson D B (1993). Mouse GATA-4: a retinoic acid-inducible GATA-binding transcription factor expressed in endodermally derived tissues and heart. Mol Cell Biol, 13(4): 2235–2246

[3] Bajpai R, Chen D A, Rada-Iglesias A, Zhang J, Xiong Y Q, Helms J, Chang C P, Zhao Y M, Swigut T, Wysocka J (2010). CHD7 cooperates with PBAF to control multipotent neural crest formation. Nature, 463, 958–962

[4] Bannister A J, Zegerman P, Partridge J F, Miska E A, Thomas J O, Allshire R C, Kouzarides T (2001). Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature, 410(6824): 120–124

[5] Berger S L (2007). The complex language of chromatin regulation during transcription. Nature, 447(7143): 407–412

[6] Bernstein B E, Kamal M, Lindblad-Toh K, Bekiranov S, Bailey D K, Huebert D J, McMahon S, Karlsson E K, Kulbokas E J 3rd, Gingeras T R, Schreiber S L, Lander E S (2005). Genomic maps and comparative analysis of histone modifications in human and mouse. Cell, 120(2): 169–181

[7] Boyer L A, Latek R R, Peterson C L (2004). The SANT domain: a unique histone-tail-binding module? Nat Rev Mol Cell Biol, 5(2): 158–163

[8] Brand T (2003). Heart development: molecular insights into cardiac specification and early morphogenesis. Dev Biol, 258(1): 1–19

[9] Bruneau B G (2010). Chromatin remodeling in heart development. Curr Opin Genet Dev, 20(5):505–11

[10] Bruneau B G, Logan M, Davis N, Levi T, Tabin C J, Seidman J G, Seidman C E (1999). Chamber-specific cardiac expression of Tbx5 and heart defects in Holt-Oram syndrome. Dev Biol, 211(1): 100–108

[11] Buckingham M, Meilhac S, Zaffran S (2005). Building the mammalian heart from two sources of myocardial cells. Nat Rev Genet, 6(11): 826–837

[12] Bultman S, Gebuhr T, Yee D, La Mantia C, Nicholson J, Gilliam A, Randazzo F, Metzger D, Chambon P, Crabtree G, Magnuson T (2000). A Brg1 null mutation in the mouse reveals functional differences among mammalian SWI/SNF complexes. Mol Cell, 6(6): 1287–1295

[13] Cai C L, Liang X, Shi Y, Chu P H, Pfaff S L, Chen J, Evans S (2003a). Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev Cell, 5(6): 877–889

[14] Cai S, Han H, Kohwi-Shigematsu T (2003b). Tissue-specific nuclear architecture and gene expression regulated by SATB1. Nature Genetics, 34: 42–51

[15] Chen H, Shi S, Acosta L, Li W, Lu J, Bao S, Chen Z, Yang Z, Schneider M D, Chien K R, Conway S J, Yoder M C, Haneline L S, Franco D, Shou W (2004). BMP10 is essential for maintaining cardiac growth during murine cardiogenesis. Development, 131(9): 2219–2231

[16] Chi T H, Wan M, Lee P P, Akashi K, Metzger D, Chambon P, Wilson C B, Crabtree G R (2003). Sequential roles of Brg, the ATPase subunit of BAF chromatin remodeling complexes, in thymocyte development. Immunity, 19(2): 169–182

[17] Christoffels V M, Hoogaars W M, Tessari A, Clout D E, Moorman A F, Campione M (2004). T-box transcription factor Tbx2 represses differentiation and formation of the cardiac chambers. Dev Dyn, 229(4): 763–770

[18] Cirillo L A, Lin F R, Cuesta I, Friedman D, Jarnik M, Zaret K S (2002). Opening of compacted chromatin by early developmental transcription factors HNF3 (FoxA) and GATA-4. Mol Cell, 9(2): 279–289

[19] de la Serna I L, Ohkawa Y, Imbalzano A N (2006). Chromatin remodelling in mammalian differentiation: lessons from ATP-dependent remodellers. Nat Rev Genet, 7(6): 461–473

[20] Dodou E, Verzi M P, Anderson J P, Xu S M, Black B L (2004). Mef2c is a direct transcriptional target of ISL1 and GATA factors in the anterior heart field during mouse embryonic development. Development, 131(16): 3931–3942

[21] Fischle W, Wang Y, Allis C D (2003). Histone and chromatin cross-talk. Curr Opin Cell Biol, 15(2): 172–183

[22] Francastel C, Schübeler D, Martin D I, Groudine M (2000). Nuclear compartmentalization and gene activity. Nat Rev Mol Cell Biol, 1(2): 137–143

[23] Frank D U, Fotheringham L K, Brewer J A, Muglia L J, Tristani-Firouzi M, Capecchi M R, Moon A M (2002). An Fgf8 mouse mutant phenocopies human 22q11 deletion syndrome. Development, 129(19): 4591–4603

[24] Gao X, Tate P, Hu P, Tjian R, Skarnes W C, Wang Z (2008). ES cell pluripotency and germ-layer formation require the SWI/SNF chromatin remodeling component BAF250a. Proc Natl Acad Sci USA, 105(18): 6656–6661

[25] Gassmann M, Casagranda F, Orioli D, Simon H, Lai C, Klein R, Lemke G (1995). Aberrant neural and cardiac development in mice lacking the ErbB4 neuregulin receptor. Nature, 378:390–394

[26] Gottlieb P D, Pierce S A, Sims III R J, Yamagishi H, Weihe E K, Harriss J V, Maika S D, Kuziel W A, King H L, Olson E N, Nakagawa O, Srivastava D (2002). Bop encodes a muscle-restricted protein containing MYND and SET domains and is essential for cardiac differentiation and morphogenesis. Nature Genetics 31: 25–32

[27] Grego-Bessa J, Luna-Zurita L, del Monte G, Bolós V, Melgar P, Arandilla A, Garratt A N, Zang H, Mukouyama Y S, Chen H, Shou W, Ballestar E, Esteller M, Rojas A, Pérez-Pomares J M, de la Pompa J L (2007). Notch signaling is essential for ventricular chamber development. Dev Cell, 12(3): 415–429

[28] Habets P E, Moorman A F, Clout D E, van Roon M A, Lingbeek M, van Lohuizen M, Campione M, Christoffels V M (2002). Cooperative action of Tbx2 and Nkx2.5 inhibits ANF expression in the atrioventricular canal: implications for cardiac chamber formation. Genes Dev, 16(10): 1234–1246

[29] Han P, Hang C T, Yang J, Chang C P (2011). Chromatin remodeling in cardiovascular development and physiology. Circ Res, 108(3): 378–396

[30] Hang C T, Yang J, Han P, Cheng H L, Shang C, Ashley E, Zhou B, Chang C P (2010). Chromatin regulation by Brg1 underlies heart muscle development and disease. Nature, 466: 62–67

[31] Harrelson Z, Kelly R G, Goldin S N, Gibson-Brown J J, Bollag R J, Silver L M, Papaioannou V E (2004). Tbx2 is essential for patterning the atrioventricular canal and for morphogenesis of the outflow tract during heart development. Development, 131(20): 5041–5052

[32] Hassan A H, Prochasson P, Neely K E, Galasinski S C, Chandy M, Carrozza M J, Workman J L (2002). Function and selectivity of bromodomains in anchoring chromatin-modifying complexes to promoter nucleosomes. Cell, 111(3): 369–379

[33] Hiroi Y, Kudoh S, Monzen K, Ikeda Y, Yazaki Y, Nagai R, Komuro I (2001). Tbx5 associates with Nkx2-5 and synergistically promotes cardiomyocyte differentiation. Nature Genetics, 28: 276–280

[34] Hu T, Yamagishi H, Maeda J, McAnally J, Yamagishi C, Srivastava D (2004). Tbx1 regulates fibroblast growth factors in the anterior heart field through a reinforcing autoregulatory loop involving forkhead transcription factors. Development, 131(21): 5491–5502

[35] Huang X, Gao X, Diaz-Trelles R, Ruiz-Lozano P, Wang Z (2008). Coronary development is regulated by ATP-dependent SWI/SNF chromatin remodeling component BAF180. Dev Biol, 319(2): 258–266

[36] Jiang C, Pugh B F (2009). Nucleosome positioning and gene regulation: advances through genomics. Nat Rev Genet, 10(3): 161–172

[37] Kelly R G, Brown N A, Buckingham M E (2001). The arterial pole of the mouse heart forms from Fgf10-expressing cells in pharyngeal mesoderm. Dev Cell, 1(3): 435–440

[38] Kelly R G, Buckingham M E (2002). The anterior heart-forming field: voyage to the arterial pole of the heart. Trends Genet, 18(4): 210–216

[39] Kitagawa H, Fujiki R, Yoshimura K, Mezaki Y, Uematsu Y, Matsui D, Ogawa S, Unno K, Okubo M, Tokita A, Nakagawa T, Ito T, Ishimi Y, Nagasawa H, Matsumoto T, Yanagisawa J, Kato S (2003). The chromatin-remodeling complex WINAC targets a nuclear receptor to promoters and is impaired in Williams syndrome. Cell, 113(7): 905–917

[40] Konev A Y, Tribus M, Park S Y, Podhraski V, Lim C Y, Emelyanov A V, Vershilova E, Pirrotta V, Kadonaga J T, Lusser A, Fyodorov D V (2007). CHD1 motor protein is required for deposition of histone variant H3.3 into chromatin in vivo. Science, 317(5841): 1087–1090

[41] Kraus F, Haenig B, Kispert A (2001). Cloning and expression analysis of the mouse T-box gene tbx20. Mech Dev, 100(1): 87–91

[42] Kuramochi Y, Guo X, Sawyer D B (2006). Neuregulin activates erbB2-dependent src/FAK signaling and cytoskeletal remodeling in isolated adult rat cardiac myocytes. J Mol Cell Cardiol, 41(2): 228–235

[43] Kwon H, Imbalzano A, Khavari P, Kingston R, Green M (1994). Nucleosome disruption and enhancement of activator binding by a human SW1/SNF complex. Nature, 370(6489): 477–481

[44] Lachner M, O’Carroll D, Rea S, Mechtler K, Jenuwein T (2001). Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature, 410(6824): 116–120

[45] Lee J H, Hart S R, Skalnik D G (2004). Histone deacetylase activity is required for embryonic stem cell differentiation. Genesis, 38(1): 32–38

[46] Lee K F, Simon H, Chen H, Bates B, Hung MC, Hauser C (1995). Requirement for neuregulin receptor erbB2 in neural and cardiac development. Nature, 23;378(6555):394–398

[47] Lessard J, Wu J I, Ranish J A, Wan M, Winslow M M, Staahl B T, Wu H, Aebersold R, Graef I A, Crabtree G R (2007). An essential switch in subunit composition of a chromatin remodeling complex during neural development. Neuron, 55(2): 201–215

[48] Liberatore C M, Searcy-Schrick R D, Yutzey K E (2000). Ventricular expression of tbx5 inhibits normal heart chamber development. Dev Biol, 223(1): 169–180

[49] Lickert H, Takeuchi J K, Von Both I, Walls J R, McAuliffe F, Adamson S L, Henkelman R M, Wrana J L, Rossant J, Bruneau B G (2004). Baf60c is essential for function of BAF chromatin remodelling complexes in heart development. Nature, 432(7013): 107–112

[50] Lodén M, van Steensel B (2005). Whole-genome views of chromatin structure. Chromosome Res, 13(3): 289–298

[51] Lomvardas S, Thanos D (2001). Nucleosome sliding via TBP DNA binding in vivo. Cell, 106(6): 685–696

[52] Lou X, Deshwar A R, Crump J G, Scott I C (2011). Smarcd3b and Gata5 promote a cardiac progenitor fate in the zebrafish embryo. Development, 138(15): 3113–3123

[53] Luger K, Mäder A W, Richmond R K, Sargent D F, Richmond T J (1997). Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature, 389(6648): 251–260

[54] Maeda J, Yamagishi H, McAnally J, Yamagishi C, Srivastava D (2006). Tbx1 is regulated by forkhead proteins in the secondary heart field. Dev Dyn, 235(3): 701–710

[55] Martens J H, O’Sullivan R J, Braunschweig U, Opravil S, Radolf M, Steinlein P, Jenuwein T (2005). The profile of repeat-associated histone lysine methylation states in the mouse epigenome. EMBO J, 24(4): 800–812

[56] Meyer D, Birchmeier C (1995). Multiple essential functions of neuregulin in development. Nature 378: 386–390

[57] Mizuguchi G, Shen X, Landry J, Wu W H, Sen S, Wu C (2004). ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science, 303(5656): 343–348

[58] Moorman A, Lamers W (1999). Development of the conduction system of the vertebrate heart. Heart development, 151: 195–207

[59] Moorman A F, Christoffels V M (2003). Cardiac chamber formation: development, genes, and evolution. Physiol Rev, 83(4): 1223–1267

[60] Morrison A J, Shen X (2009). Chromatin remodelling beyond transcription: the INO80 and SWR1 complexes. Nat Rev Mol Cell Biol, 10(6): 373–384

[61] Nie Z, Xue Y, Yang D, Zhou S, Deroo B J, Archer T K, Wang W (2000). A specificity and targeting subunit of a human SWI/SNF family-related chromatin-remodeling complex. Mol Cell Biol, 20(23): 8879–8888

[62] Oyake T, Itoh K, Motohashi H, Hayashi N, Hoshino H, Nishizawa M, Yamamoto M, Igarashi K (1996). Bach proteins belong to a novel family of BTB-basic leucine zipper transcription factors that interact with MafK and regulate transcription through the NF-E2 site. Mol Cell Biol, 16(11): 6083–6095

[63] Park E J, Ogden L A, Talbot A, Evans S, Cai C L, Black B L, Frank D U, Moon A M (2006). Required, tissue-specific roles for Fgf8 in outflow tract formation and remodeling. Development, 133(12): 2419–2433

[64] Phan D, Rasmussen T L, Nakagawa O, McAnally J, Gottlieb P D, Tucker P W, Richardson J A, Bassel-Duby R, Olson E N (2005). BOP, a regulator of right ventricular heart development, is a direct transcriptional target of MEF2C in the developing heart. Development, 132(11): 2669–2678

[65] Polach K J, Widom J (1996). A model for the cooperative binding of eukaryotic regulatory proteins to nucleosomal target sites. J Mol Biol, 258(5): 800–812

[66] Poot R A, Bozhenok L, van den Berg D L, Steffensen S, Ferreira F, Grimaldi M, Gilbert N, Ferreira J, Varga-Weisz P D (2004). The Williams syndrome transcription factor interacts with PCNA to target chromatin remodelling by ISWI to replication foci. Nat Cell Biol, 6(12): 1236–1244

[67] Saha A, Wittmeyer J, Cairns B R (2006). Chromatin remodelling: the industrial revolution of DNA around histones. Nat Rev Mol Cell Biol, 7(6): 437–447

[68] Schneider M D, Gaussin V, Lyons K M (2003). Tempting fate: BMP signals for cardiac morphogenesis. Cytokine Growth Factor Rev, 14(1): 1–4

[69] Simone C, Forcales S V, Hill D A, Imbalzano A N, Latella L, Puri P L (2004). p38 pathway targets SWI-SNF chromatin-remodeling complex to muscle-specific loci. Nature Genetics 36: 738–743

[70] Singh M K, Christoffels V M, Dias J M, Trowe M O, Petry M, Schuster-Gossler K, Bürger A, Ericson J, Kispert A (2005). Tbx20 is essential for cardiac chamber differentiation and repression of Tbx2. Development, 132(12): 2697–2707

[71] Stankunas K, Hang C T, Tsun Z Y, Chen H, Lee N V, Wu J I, Shang C, Bayle J H, Shou W, Iruela-Arispe M L, Chang C P (2008). Endocardial Brg1 represses ADAMTS1 to maintain the microenvironment for myocardial morphogenesis. Dev Cell, 14(2): 298–311

[72] Stennard F A, Costa M W, Lai D, Biben C, Furtado M B, Solloway M J, McCulley D J, Leimena C, Preis J I, Dunwoodie S L, Elliott D E, Prall O W, Black B L, Fatkin D, Harvey R P (2005). Murine T-box transcription factor Tbx20 acts as a repressor during heart development, and is essential for adult heart integrity, function and adaptation. Development, 132(10): 2451–2462

[73] Takeuchi J K, Bruneau B G (2009). Directed transdifferentiation of mouse mesoderm to heart tissue by defined factors. Nature, 459(7247): 708–711

[74] von Both I, Silvestri C, Erdemir T, Lickert H, Walls J R, Henkelman R M, Rossant J, Harvey R P, Attisano L, Wrana J L (2004). Foxh1 is essential for development of the anterior heart field. Dev Cell, 7(3): 331–345

[75] Wang W, Côté J, Xue Y, Zhou S, Khavari P A, Biggar S R, Muchardt C, Kalpana G V, Goff S P, Yaniv M, Workman J L, Crabtree G R (1996a). Purification and biochemical heterogeneity of the mammalian SWI-SNF complex. EMBO J, 15(19): 5370–5382

[76] Wang W, Xue Y, Zhou S, Kuo A, Cairns B R, Crabtree G R (1996b). Diversity and specialization of mammalian SWI/SNF complexes. Genes Dev, 10(17): 2117–2130

[77] Wang Z, Zhai W, Richardson J A, Olson E N, Meneses J J, Firpo M T, Kang C, Skarnes W C, Tjian R (2004). Polybromo protein BAF180 functions in mammalian cardiac chamber maturation. Genes Dev, 18(24): 3106–3116

[78] Wu J I, Lessard J, Crabtree G R (2009). Understanding the words of chromatin regulation. Cell, 136(2): 200–206

[79] Wu J I, Lessard J, Olave I A, Qiu Z, Ghosh A, Graef I A, Crabtree G R (2007). Regulation of dendritic development by neuron-specific chromatin remodeling complexes. Neuron, 56(1): 94–108

[80] Xue Y, Canman J C, Lee C S, Nie Z, Yang D, Moreno G T, Young M K, Salmon E D, Wang W (2000). The human SWI/SNF-B chromatin-remodeling complex is related to yeast rsc and localizes at kinetochores of mitotic chromosomes. Proc Natl Acad Sci USA, 97(24): 13015–13020

[81] Yan Z, Cui K, Murray D M, Ling C, Xue Y, Gerstein A, Parsons R, Zhao K, Wang W (2005). PBAF chromatin-remodeling complex requires a novel specificity subunit, BAF200, to regulate expression of selective interferon-responsive genes. Genes Dev, 19(14): 1662–1667

[82] Yoshimura K, Kitagawa H, Fujiki R, Tanabe M, Takezawa S, Takada I, Yamaoka I, Yonezawa M, Kondo T, Furutani Y, Yagi H, Yoshinaga S, Masuda T, Fukuda T, Yamamoto Y, Ebihara K, Li D Y, Matsuoka R, Takeuchi J K, Matsumoto T, Kato S (2009). Distinct function of 2 chromatin remodeling complexes that share a common subunit, Williams syndrome transcription factor (WSTF). Proc Natl Acad Sci USA, 106(23): 9280–9285

[83] Zhao K, Wang W, Rando O J, Xue Y, Swiderek K, Kuo A, Crabtree G R (1998). Rapid and phosphoinositol-dependent binding of the SWI/SNF-like BAF complex to chromatin after T lymphocyte receptor signaling. Cell, 95(5): 625–636

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