Defining the earliest step of cardiovascular progenitor specification during embryonic stem cell differentiation

Journal of Cell Biology

Volumn 192, Issue 5, 2011, Pages 751-765

  Bondue, Antoine ^a   Tännler, Simon ^a   Chiapparo, Giuseppe ^a   Chabab, Samira ^a   Ramialison, Mirana ^b   Paulissen, Catherine ^a   Beck, Benjamin ^a   Harvey, Richard ^b,c   Blanpain, Cédric ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b VICTOR CHANG CARDIAC RESEARCH INSTITUTE   (Australia)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL ISOLATION; CELL LINEAGE; CONTROLLED STUDY; EMBRYO DEVELOPMENT; HEART MUSCLE CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; STEM CELL; STEM CELL MOBILIZATION; TRANSCRIPTION REGULATION;

EID: 79952374113     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.201007063     Document Type: Article

References (40)

1. Bondue, A., and C. Blanpain. 2010. Mesp1: a key regulator of cardiovascular lineage commitment. Circ. Res. 107:1414-1427. doi:10.1161/CIRCRESAHA.110.227058
2. Bondue, A., G. Lapouge, C. Paulissen, C. Semeraro, M. Iacovino, M. Kyba, and C. Blanpain. 2008. Mesp1 acts as a master regulator of multipotent cardiovascular progenitor specification. Cell Stem Cell. 3:69-84. doi:10.1016/j.stem.2008.06.009
3. Brade, T., S. Gessert, M. Kühl, and P. Pandur. 2007. The amphibian second heart field: Xenopus islet-1 is required for cardiovascular development. Dev. Biol. 311:297-310. doi:10.1016/j.ydbio.2007.08.004 (Pubitemid 350046524)
4. Bu, L., X. Jiang, S. Martin-Puig, L. Caron, S. Zhu, Y. Shao, D.J. Roberts, P.L. Huang, I.J. Domian, and K.R. Chien. 2009. Human ISL1 heart progenitors generate diverse multipotent cardiovascular cell lineages. Nature. 460:113-117. doi:10.1038/nature08191
5. Buckingham, M., and C. Desplan. 2010. Developmental mechanisms, patterning and evolution. Curr. Opin. Genet. Dev. 20:343-345. doi:10.1016/j.gde.2010.06.006
6. Cai, C.L., X. Liang, Y. Shi, P.H. Chu, S.L. Pfaff, J. Chen, and S. Evans. 2003. Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev. Cell. 5:877-889. doi:10.1016/S15345807(03)00363-0 (Pubitemid 37527688)
7. David, R., C. Brenner, J. Stieber, F. Schwarz, S. Brunner, M. Vollmer, E. Mentele, J. Müller-Höcker, S. Kitajima, H. Lickert, et al. 2008. MesP1 drives vertebrate cardiovascular differentiation through Dkk-1-mediated blockade of Wnt-signalling. Nat. Cell Biol. 10:338-345. doi:10.1038/ncb1696 (Pubitemid 351331021)
8. Ema, M., S. Takahashi, and J. Rossant. 2006. Deletion of the selection cassette, but not cis-acting elements, in targeted Flk1-lacZ allele reveals Flk1 expression in multipotent mesodermal progenitors. Blood. 107:111-117. doi:10.1182/blood-2005-05-1970 (Pubitemid 43053531)
9. Han, K., and J.L. Manley. 1993. Functional domains of the Drosophila Engrailed protein. EMBO J. 12:2723-2733. (Pubitemid 23218322)
10. Haraguchi, S., S. Kitajima, A. Takagi, H. Takeda, T. Inoue, and Y. Saga. 2001. Transcriptional regulation of Mesp1 and Mesp2 genes: differential usage of enhancers during development. Mech. Dev. 108:59-69. doi:10.1016/S0925-4773(01) 00478-6 (Pubitemid 32918177)
11. Harel, I., E. Nathan, L. Tirosh-Finkel, H. Zigdon, N. Guimarães-Camboa, S.M. Evans, and E. Tzahor. 2009. Distinct origins and genetic programs of head muscle satellite cells. Dev. Cell. 16:822-832. doi:10.1016/j.devcel.2009.05.007
12. Hidaka, K., M. Shirai, J.K. Lee, T. Wakayama, I. Kodama, M.D. Schneider, and T. Morisaki. 2010. The cellular prion protein identifies bipotential cardiomyogenic progenitors. Circ. Res. 106:111-119. doi:10.1161/CIRCRESAHA.109. 209478
13. Huang, da W., B.T. Sherman, and R.A. Lempicki. 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4:44-57. doi:10.1038/nprot.2008.211
14. Iida, M., T. Heike, M. Yoshimoto, S. Baba, H. Doi, and T. Nakahata. 2005. Identification of cardiac stem cells with FLK1, CD31, and VE-cadherin expression during embryonic stem cell differentiation. FASEB J. 19:371-378. doi:10.1096/fj.041998com (Pubitemid 40316525)
15. Jensen, K.B., and F.M. Watt. 2006. Single-cell expression profiling of human epidermal stem and transit-amplifying cells: Lrig1 is a regulator of stem cell quiescence. Proc. Natl. Acad. Sci. USA. 103:11958-11963. doi:10.1073/pnas.0601886103 (Pubitemid 44215793)
16. Kattman, S.J., T.L. Huber, and G.M. Keller. 2006. Multipotent flk-1+ cardiovascular progenitor cells give rise to the cardiomyocyte, endothelial, and vascular smooth muscle lineages. Dev. Cell. 11:723-732. doi:10.1016/j.devcel. 2006.10.002 (Pubitemid 44644969)
17. Kattman, S.J., E.D. Adler, and G.M. Keller. 2007. Specification of multipotential cardiovascular progenitor cells during embryonic stem cell differentiation and embryonic development. Trends Cardiovasc. Med. 17:240-246. doi:10.1016/j.tcm.2007.08.004 (Pubitemid 47532729)
18. Kitajima, S., A. Takagi, T. Inoue, and Y. Saga. 2000. MesP1 and MesP2 are essential for the development of cardiac mesoderm. Development. 127:3215-3226. (Pubitemid 30649534)
19. Kwon, C., L. Qian, P. Cheng, V. Nigam, J. Arnold, and D. Srivastava. 2009. A regulatory pathway involving Notch1/beta-catenin/Isl1 determines cardiac progenitor cell fate. Nat. Cell Biol. 11:951-957. doi:10.1038/ncb1906
20. Kyba, M., R.C. Perlingeiro, and G.Q. Daley. 2002. HoxB4 confers definitive lymphoid-myeloid engraftment potential on embryonic stem cell and yolk sac hematopoietic progenitors. Cell. 109:29-37. doi:10.1016/S0092-8674(02) 00680-3 (Pubitemid 34327514)
21. Lindsley, R.C., J.G. Gill, T.L. Murphy, E.M. Langer, M. Cai, M. Mashayekhi, W. Wang, N. Niwa, J.M. Nerbonne, M. Kyba, and K.M. Murphy. 2008. Mesp1 coordinately regulates cardiovascular fate restriction and epithelial-mesenchymal transition in differentiating ESCs. Cell Stem Cell. 3:55-68. doi:10.1016/j.stem.2008.04.004
22. Liu, P., N.A. Jenkins, and N.G. Copeland. 2003. A highly efficient recombineering-based method for generating conditional knockout mutations. Genome Res. 13:476-484. doi:10.1101/gr.749203 (Pubitemid 36395405)
23. Ma, Q., B. Zhou, and W.T. Pu. 2008. Reassessment of Isl1 and Nkx2-5 cardiac fate maps using a Gata4-based reporter of Cre activity. Dev. Biol. 323:98-104. doi:10.1016/j.ydbio.2008.08.013
24. Martin-Puig, S., Z. Wang, and K.R. Chien. 2008. Lives of a heart cell: tracing the origins of cardiac progenitors. Cell Stem Cell. 2:320-331. doi:10.1016/j.stem.2008.03.010 (Pubitemid 351455247)
25. McBratney-Owen, B., S. Iseki, S.D. Bamforth, B.R. Olsen, and G.M. Morriss-Kay. 2008. Development and tissue origins of the mammalian cranial base. Dev. Biol. 322:121-132. doi:10.1016/j.ydbio.2008.07.016
26. Meilhac, S.M., M. Esner, R.G. Kelly, J.F. Nicolas, and M.E. Buckingham. 2004. The clonal origin of myocardial cells in different regions of the embryonic mouse heart. Dev. Cell. 6:685-698. doi:10.1016/S15345807(04)001339 (Pubitemid 38579352)
27. Moretti, A., L. Caron, A. Nakano, J.T. Lam, A. Bernshausen, Y. Chen, Y. Qyang, L. Bu, M. Sasaki, S. Martin-Puig, et al. 2006. Multipotent embryonic isl1+ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification. Cell. 127:1151-1165. doi:10.1016/j.cell.2006.10.029 (Pubitemid 44895618)
28. Murry, C.E., and G. Keller. 2008. Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell. 132:661-680. doi:10.1016/j.cell.2008.02.008 (Pubitemid 351260059)
29. Nelson, T.J., R.S. Faustino, A. Chiriac, R. Crespo-Diaz, A. Behfar, and A. Terzic. 2008. CXCR4+/FLK-1+ biomarkers select a cardiopoietic lineage from embryonic stem cells. Stem Cells. 26:1464-1473. doi:10.1634/stemcells.20070808
30. Olson, E.N. 2006. Gene regulatory networks in the evolution and development of the heart. Science. 313:1922-1927. doi:10.1126/science.1132292 (Pubitemid 44497993)
31. Prall, O.W., M.K. Menon, M.J. Solloway, Y. Watanabe, S. Zaffran, F. Bajolle, C. Biben, J.J. McBride, B.R. Robertson, H. Chaulet, et al. 2007. An Nkx2-5/Bmp2/Smad1 negative feedback loop controls heart progenitor specification and proliferation. Cell. 128:947-959. doi:10.1016/j.cell.2007.01.042 (Pubitemid 46341418)
32. Saga, Y., N. Hata, S. Kobayashi, T. Magnuson, M.F. Seldin, and M.M. Taketo. 1996. MesP1: a novel basic helix-loop-helix protein expressed in the nascent mesodermal cells during mouse gastrulation. Development. 122:2769-2778. (Pubitemid 26326509)
33. Saga, Y., S. Miyagawa-Tomita, A. Takagi, S. Kitajima, J. Miyazaki, and T. Inoue. 1999. MesP1 is expressed in the heart precursor cells and required for the formation of a single heart tube. Development. 126:3437-3447. (Pubitemid 29396783)
34. Saga, Y., S. Kitajima, and S. Miyagawa-Tomita. 2000. Mesp1 expression is the earliest sign of cardiovascular development. Trends Cardiovasc. Med. 10:345-352. doi:10.1016/S1050-1738(01)00069-X (Pubitemid 32448044)
35. Stolfi, A., T.B. Gainous, J.J. Young, A. Mori, M. Levine, and L. Christiaen. 2010. Early chordate origins of the vertebrate second heart field. Science. 329:565-568. doi:10.1126/science.1190181
36. Sun, Y., X. Liang, N. Najafi, M. Cass, L. Lin, C.L. Cai, J. Chen, and S.M. Evans. 2007. Islet 1 is expressed in distinct cardiovascular lineages, including pacemaker and coronary vascular cells. Dev. Biol. 304:286-296. doi:10.1016/j.ydbio.2006.12.048 (Pubitemid 46399697)
37. Takakura, N., H. Yoshida, Y. Ogura, H. Kataoka, S. Nishikawa, and S. Nishikawa. 1997. PDGFR alpha expression during mouse embryogenesis: immunolocalization analyzed by whole-mount immunohistostaining using the monoclonal anti-mouse PDGFR alpha antibody APA5. J. Histochem. Cytochem. 45:883-893. (Pubitemid 27248804)
38. Wu, S.M., Y. Fujiwara, S.M. Cibulsky, D.E. Clapham, C.L. Lien, T.M. Schultheiss, and S.H. Orkin. 2006. Developmental origin of a bipotential myocardial and smooth muscle cell precursor in the mammalian heart. Cell. 127:1137-1150. doi:10.1016/j.cell.2006.10.028 (Pubitemid 44914005)
39. Yang, L., M.H. Soonpaa, E.D. Adler, T.K. Roepke, S.J. Kattman, M. Kennedy, E. Henckaerts, K. Bonham, G.W. Abbott, R.M. Linden, et al. 2008. Human cardiovascular progenitor cells develop from a KDR+ embryonic-stem-cell-derived population. Nature. 453:524-528. doi:10.1038/nature06894 (Pubitemid 351733312)
40. Yoshida, T., P. Vivatbutsiri, G. Morriss-Kay, Y. Saga, and S. Iseki. 2008. Cell lineage in mammalian craniofacial mesenchyme. Mech. Dev. 125:797-808. doi:10.1016/j.mod.2008.06.007