The G-protein-coupled receptor APJ is expressed in the second heart field and regulates Cerberus-Baf60c axis in embryonic stem cell cardiomyogenesis

Cardiovascular Research

Volumn 100, Issue 1, 2013, Pages 95-104

  D'Aniello, Cristina ^a   Fiorenzano, Alessandro ^a   Iaconis, Salvatore ^a   Liguori, Giovanna L ^a   Andolfi, Gennaro ^a   Cobellis, Gilda ^b   Fico, Annalisa ^a   Minchiotti, Gabriella ^a  

^a INSTITUTE OF GENETICS AND BIOPHYSICS ADRIANO BUZZATI TRAVERSO   (Italy)

^b SECOND UNIVERSITY OF NAPLES   (Italy)

Author keywords

Epigenetic; G protein coupled receptors; Myocardial progenitors; Second heart field; Stem cells

Indexed keywords

APELIN RECEPTOR; BRM ASSOCIATED FACTOR SUBUNIT BAF60C; CERBERUS PROTEIN; MYOSIN HEAVY CHAIN ALPHA; PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CARDIOMYOGENESIS; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EMBRYONIC STEM CELL; FLUORESCENCE; HEART DEVELOPMENT; IN SITU HYBRIDIZATION; IN VIVO STUDY; MESODERM; MOUSE; MUSCLE DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION;

EPIGENETIC; G-PROTEIN-COUPLED RECEPTORS; MYOCARDIAL PROGENITORS; SECOND HEART FIELD; STEM CELLS;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CHROMOSOMAL PROTEINS, NON-HISTONE; CYCLIN-DEPENDENT KINASE INHIBITOR P57; EMBRYONIC STEM CELLS; HEART; MICE; MUSCLE PROTEINS; MYOCYTES, CARDIAC; NODAL PROTEIN; PROTEINS; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; SMAD2 PROTEIN;

EID: 84887874942     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvt166     Document Type: Article

References (38)

1. Noseda M, Peterkin T, Simoes F.C., Patient R., Schneider MD. Cardiopoietic factors: extracellular signals for cardiac lineage commitment. Circ Res 2011; 108: 129-152.
2. Vincent SD, Buckingham ME. How to make a heart: the origin and regulation of cardiac progenitor cells. Curr Top Dev Biol 2010; 90: 1-41.
3. Kelly RG. The second heart field. Curr Top Dev Biol 2012; 100: 33-65.
4. Bruneau BG. Chromatin remodelinginheart development. Curr Opin Genet Dev 2010; 20: 505-511.
5. Wamstad JA, Alexander JM, Truty R.M., Shrikumar A., Li F, Eilertson KE et al. Dynamic and coordinated epigenetic regulation of developmental transitions in the cardiac lineage. Cell 2012; 151: 206-220.
6. Ho L, Crabtree GR. Chromatin remodelling during development. Nature 2010; 463: 474-484.
7. Takeuchi JK, Bruneau BG. Directed transdifferentiation of mouse mesoderm to heart tissue by defined factors. Nature 2009; 459: 708-11.
8. Inui M, Fukui A, Ito Y., Asashima M. Xapelin and Xmsr are required for cardiovascular development in Xenopus laevis. Dev Biol 2006; 298: 188-200.
9. Scott IC, Masri B, D'Amico LA, Jin SW, Jungblut B, Wehman AM et al. The G proteincoupled receptor agtrl1b regulates early development of myocardial progenitors. Dev Cell 2007; 12: 403-413.
10. Zeng XX, Wilm TP, Sepich D.S., Solnica-Krezel L. Apelin and its receptor control heart field formation during zebrafish gastrulation. Dev Cell 2007; 12: 391-402.
11. Scimia MC, Hurtado C, Ray S., Metzler S, Wei K, Wang J et al. APJ acts asadual receptor in cardiac hypertrophy. Nature 2012; 488: 394-398.
12. Paskaradevan S, Scott IC. The Aplnr GPCR regulates myocardial progenitor development via a novel cell-non-autonomous, Galpha(i/o) protein-independent pathway. Biol Open 2012; 1: 275-285.
13. Vodyanik MA, Yu J, Zhang X., Tian S, Stewart R, Thomson JA et al. A mesoderm-derived precursor for mesenchymal stem and endothelial cells. Cell Stem Cell 2010; 7: 718-729.
14. Yu QC, Hirst CE, Costa M, Ng E.S., Schiesser JV, Gertow K et al. APELIN promotes hem-atopoiesis from human embryonic stem cells. Blood 2012; 119: 6243-6254.
15. D'Aniello C., Lonardo E, Iaconis S., Guardiola O, Liguoro AM, Liguori GL et al. G proteincoupled receptor APJ and its ligand apelin act downstream of Cripto to specify embryonic stem cells toward the cardiac lineage through extracellular signal-regulated kinase/p70S6 kinase signaling pathway. Circ Res 2009; 105: 231-238.
16. Parisi S, D'Andrea D, Lago CT, Adamson E.D., Persico MG, Minchiotti G. Nodal-dependent Cripto signaling promotes cardiomyogenesis and redirects the neural fate of embryonic stem cells. J Cell Biol 2003; 163: 303-314.
17. Albini S, Coutinho P, Malecova B., Giordani L, Savchenko A, Forcales SV et al. Epigenetic reprogrammingofhuman embryonic stem cells into skeletal muscle cells and generation of contractile myospheres. Cell Reports 2013; 3: 661-670.
18. Saint-Geniez M., Masri B, Malecaze F., Knibiehler B, Audigier Y. Expression of the murine msr/apj receptor and its ligand apelin is upregulated during formation of the retinal vessels. Mech Dev 2002; 110: 183-186.
19. Kidoya H, Ueno M, Yamada Y., Mochizuki N, Nakata M, Yano T et al. Spatial and temporal role of the apelin/APJ system in the caliber size regulation of blood vessels during angiogenesis. EMBO J 2008; 27: 522-534.
20. Eyries M, Siegfried G, Ciumas M., Montagne K, Agrapart M, Lebrin F et al. Hypoxia-induced apelin expression regulates endothelial cell proliferation and regenerative angiogenesis. Circ Res 2008; 103: 432-440.
21. Kelly RG, Brown NA, Buckingham ME. The arterial pole of the mouse heart forms from Fgf10-expressing cells in pharyngeal mesoderm. Dev Cell 2001; 1: 435-440.
22. Bondue A, Lapouge G, Paulissen C., Semeraro C, Iacovino M, Kyba M et al. Mesp1 actsasa master regulator of multipotent cardiovascular progenitor specification. Cell Stem Cell 2008; 3: 69-84.
23. Yu Y, Arora A, Min W., Roifman CM, Grunebaum E. EdU incorporation is an alternative non-radioactive assayto[(3)H]thymidine uptake forin vitro measurement of mice T-cell proliferations. J Immunol Methods 2009; 350: 29-35.
24. Hang CT, Yang J, Han P., Cheng HL, Shang C, Ashley E et al. Chromatin regulationby Brg1 underlies heart muscle development and disease. Nature 2010; 466: 62-67.
25. Romito A, Lonardo E, Roma G., Minchiotti G, Ballabio A, Cobellis G. Lack of sik1 in mouse embryonic stem cells impairs cardiomyogenesis by down-regulating the cyclin-dependent kinase inhibitor p57kip2. PLoS One 2010; 5:e9029.
26. Mercola M, Ruiz-Lozano P, Schneider MD. Cardiac muscle regeneration: lessons from development. Genes Dev 2011; 25: 299-309.
27. Foley AC, Korol O, Timmer A.M., Mercola M. Multiple functions of Cerberus cooperate to induce heart downstream of Nodal. Dev Biol 2007; 303: 57-65.
28. Kitamura R, Takahashi T, Nakajima N., Isodono K, Asada S, Ueno H et al. Stage-specific role of endogenous Smad2 activation in cardiomyogenesis of embryonic stem cells. Circ Res 2007; 101: 78-87.
29. Lickert H, Takeuchi JK, von Both I, Walls JR, McAuliffe F, Adamson SL et al. Baf60c is essential for function of BAF chromatin remodelling complexes in heart development. Nature 2004; 432: 107-112.
30. Bondue A, Tannler S, Chiapparo G., Chabab S, Ramialison M, Paulissen C et al. Defining the earliest step of cardiovascular progenitor specification during embryonic stem cell differentiation. J Cell Biol 2011; 192: 751-765.
31. Lindsley RC, Gill JG, Murphy T.L., Langer EM, Cai M, Mashayekhi M et al. Mesp1 coordi-nately regulates cardiovascular fate restriction and epithelial-mesenchymal transition in differentiating ESCs. Cell Stem Cell 2008; 3: 55-68.
32. Wu SM. Mesp1 at the heart of mesoderm lineage specification. Cell Stem Cell 2008; 3: 1-2.
33. Lickert H, Takeuchi JK, Von Both I, Walls JR, McAuliffe F, Adamson SL et al. Baf60c is essential for function of BAF chromatin remodelling complexes in heart development. Nature 2004; 432: 107-112.
34. Ho L, Jothi R, Ronan J.L., Cui K., Zhao K, Crabtree GR. An embryonic stem cell chromatin remodeling complex, esBAF, is an essential component of the core pluripotency tran-scriptional network. Proc Natl Acad Sci USA 2009; 106: 5187-5191.
35. Ishida J, Hashimoto T, Hashimoto Y., Nishiwaki S, Iguchi T, Harada S et al. Regulatory roles for APJ, a seven-transmembrane receptor related to angiotensin-type 1 receptor in blood pressure in vivo. J Biol Chem 2004; 279: 26274-26279.
36. Charo DN, Ho M, Fajardo G., Kawana M, Kundu RK, Sheikh AY et al. Endogenous regulation of cardiovascular function by apelin-APJ. Am J Physiol Heart Circ Physiol 2009; 297:H1904-H1913.
37. Roberts EM, Newson MJ, Pope G.R., Landgraf R., Lolait SJ, O'Carroll AM. Abnormal fluid homeostasis in apelin receptor knockout mice. J Endocrinol 2009; 202: 453-462.
38. Kuba K, Zhang L, Imai Y., Arab S, Chen M, Maekawa Y et al. Impaired heart contractility in Apelin gene-deficient mice associated with aging and pressure overload. Circ Res 2007; 101:e32-e42.