The developmental origins and lineage contributions of endocardial endothelium

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1863, Issue 7, 2016, Pages 1937-1947

  Nakano, Atsushi ^b   Nakano, Haruko ^b   Smith, Kelly A ^a   Palpant, Nathan J ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cardiovascular; Directed differentiation; Hematopoiesis; Human pluripotent stem cells, cardiac; Lineage tracing

Indexed keywords

NOTCH RECEPTOR; TRANSCRIPTION FACTOR NKX2.5;

ADHERENS JUNCTION; ANGIOGENESIS; CARDIAC MUSCLE; CARDIAC MUSCLE CELL; CARDIAC STEM CELL; CELL DIFFERENTIATION; CELL FATE; CELL LINEAGE; CELL PLASTICITY; CORONARY ARTERY; EMBRYO DEVELOPMENT; ENDOCARDIUM; ENDODERM; ENDOTHELIUM CELL; FIBROBLAST; GENE EXPRESSION; HEART DEVELOPMENT; HEMANGIOBLAST; HEMATOPOIESIS; HUMAN; MESODERM; MESODERMAL CELL; NONHUMAN; NUCLEAR REPROGRAMMING; PLURIPOTENT STEM CELL; PRIMITIVE STREAK; PRIORITY JOURNAL; PROMOTER REGION; REVIEW; VASCULAR ENDOTHELIUM; VASCULARIZATION; WNT SIGNALING PATHWAY; ANIMAL; CELL PROLIFERATION; EMBRYOLOGY; GENE EXPRESSION REGULATION; INDUCED PLURIPOTENT STEM CELL; METABOLISM; MORPHOGENESIS; PHENOTYPE; PHYSIOLOGY;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; ENDOCARDIUM; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MORPHOGENESIS; PHENOTYPE;

EID: 84957684902     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2016.01.022     Document Type: Review

References (166)

1. Virágh S., Szabó E., Challice C.E. Formation of the primitive myo- and endocardial tubes in the chicken embryo. J. Mol. Cell. Cardiol. 1989, 21:123-137.
2. Sabin F. Studies on the origin of blood vessels and of red blood corpuscles as seen in the living blastoderm of chicks during the second day of incubation. Contrib. Embryol. 1920, 9:214.
3. Sugi Y., Markwald R.R. Formation and early morphogenesis of endocardial endothelial precursor cells and the role of endoderm. Dev. Biol. 1996, 175:66-83.
4. Dzierzak E., Speck N.A. Of lineage and legacy: the development of mammalian hematopoietic stem cells. Nat. Immunol. 2008, 9:129-136.
5. Shivdasani R.A., Mayer E.L., Orkin S.H. Absence of blood formation in mice lacking the t-cell leukaemia oncoprotein tal-1/scl. Nature 1995, 373:432-434.
6. Rönicke V., Risau W., Breier G. Characterization of the endothelium-specific murine vascular endothelial growth factor receptor-2 (flk-1) promoter. Circ. Res. 1996, 79:277-285.
7. Hewett P.W. Identification of tumour-induced changes in endothelial cell surface protein expression: an in vitro model. Int. J. Biochem. Cell Biol. 2001, 33:325-335.
8. Tam P.P., Parameswaran M., Kinder S.J., Weinberger R.P. The allocation of epiblast cells to the embryonic heart and other mesodermal lineages: the role of ingression and tissue movement during gastrulation. Development 1997, 124:1631-1642.
9. Flamme I., Frölich T., Risau W. Molecular mechanisms of vasculogenesis and embryonic angiogenesis. J. Cell. Physiol. 1997, 173:206-210.
10. Russ A.P., Wattler S., Colledge W.H., Aparicio S.A., Carlton M.B., Pearce J.J., Barton S.C., Surani M.A., Ryan K., Nehls M.C., Wilson V., Evans M.J. Eomesodermin is required for mouse trophoblast development and mesoderm formation. Nature 2000, 404:95-99.
11. Costello I., Pimeisl I.M., Dräger S., Bikoff E.K., Robertson E.J., Arnold S.J. The t-box transcription factor eomesodermin acts upstream of mesp1 to specify cardiac mesoderm during mouse gastrulation. Nat. Cell Biol. 2011, 13:1084-1091.
12. Chan S.S., Shi X., Toyama A., Arpke R.W., Dandapat A., Iacovino M., Kang J., Le G., Hagen H.R., Garry D.J., Kyba M. Mesp1 patterns mesoderm into cardiac, hematopoietic, or skeletal myogenic progenitors in a context-dependent manner. Cell Stem Cell 2013, 12:587-601.
13. Saga Y., Hata N., Kobayashi S., Magnuson T., Seldin M.F., Taketo M.M. Mesp1: a novel basic helix-loop-helix protein expressed in the nascent mesodermal cells during mouse gastrulation. Development 1996, 122:2769-2778.
14. Saga Y., Miyagawa-Tomita S., Takagi A., Kitajima S., Miyazaki J., Inoue T. Mesp1 is expressed in the heart precursor cells and required for the formation of a single heart tube. Development 1999, 126:3437-3447.
15. Devine W.P., Wythe J.D., George M., Koshiba-Takeuchi K., Bruneau B.G. Early patterning and specification of cardiac progenitors in gastrulating mesoderm. Elife 2014, 3.
16. Lescroart F., Chabab S., Lin X., Rulands S., Paulissen C., Rodolosse A., Auer H., Achouri Y., Dubois C., Bondue A., Simons B.D., Blanpain C. Early lineage restriction in temporally distinct populations of mesp1 progenitors during mammalian heart development. Nat. Cell Biol. 2014, 16:829-840.
17. Lee R.K., Stainier D.Y., Weinstein B.M., Fishman M.C. Cardiovascular development in the zebrafish. II. Endocardial progenitors are sequestered within the heart field. Development 1994, 120:3361-3366.
18. Keegan B.R., Meyer D., Yelon D. Organization of cardiac chamber progenitors in the zebrafish blastula. Development 2004, 131:3081-3091.
19. Misfeldt A.M., Boyle S.C., Tompkins K.L., Bautch V.L., Labosky P.A., Baldwin H.S. Endocardial cells are a distinct endothelial lineage derived from flk1+ multipotent cardiovascular progenitors. Dev. Biol. 2009, 333:78-89.
20. Kattman S.J., Huber T.L., Keller G.M. Multipotent flk-1+ cardiovascular progenitor cells give rise to the cardiomyocyte, endothelial, and vascular smooth muscle lineages. Dev. Cell 2006, 11:723-732.
21. Ema M., Takahashi S., Rossant J. Deletion of the selection cassette, but not cis-acting elements, in targeted flk1-lacz allele reveals flk1 expression in multipotent mesodermal progenitors. Blood 2006, 107:111-117.
22. Cai C.L., Liang X., Shi Y., Chu P.H., Pfaff S.L., Chen J., Evans S. Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev. Cell 2003, 5:877-889.
23. Verzi M.P., McCulley D.J., De Val S., Dodou E., Black B.L. The right ventricle, outflow tract, and ventricular septum comprise a restricted expression domain within the secondary/anterior heart field. Dev. Biol. 2005, 287:134-145.
24. Moretti A., Caron L., Nakano A., Lam J.T., Bernshausen A., Chen Y., Qyang Y., Bu L., Sasaki M., Martin-Puig S., Sun Y., Evans S.M., Laugwitz K.L., Chien K.R. Multipotent embryonic isl1+ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification. Cell 2006, 127:1151-1165.
25. Nascone N., Mercola M. An inductive role for the endoderm in xenopus cardiogenesis. Development 1995, 121:515-523.
26. Schultheiss T.M., Burch J.B., Lassar A.B. A role for bone morphogenetic proteins in the induction of cardiac myogenesis. Genes Dev. 1997, 11:451-462.
27. Marvin M.J., Di Rocco G., Gardiner A., Bush S.M., Lassar A.B. Inhibition of wnt activity induces heart formation from posterior mesoderm. Genes Dev. 2001, 15:316-327.
28. Schneider V.A., Mercola M. Wnt antagonism initiates cardiogenesis in Xenopus laevis. Genes Dev. 2001, 15:304-315.
29. Madabhushi M., Lacy E. Anterior visceral endoderm directs ventral morphogenesis and placement of head and heart via bmp2 expression. Dev. Cell 2011, 21:907-919.
30. Zhang H., Bradley A. Mice deficient for bmp2 are nonviable and have defects in amnion/chorion and cardiac development. Development 1996, 122:2977-2986.
31. Paffett-Lugassy N., Singh R., Nevis K.R., Guner-Ataman B., O'Loughlin E., Jahangiri L., Harvey R.P., Burns C.G., Burns C.E. Heart field origin of great vessel precursors relies on NKX2-5-mediated vasculogenesis. Nat. Cell Biol. 2013.
32. Stanley E.G., Biben C., Elefanty A., Barnett L., Koentgen F., Robb L., Harvey R.P. Efficient cre-mediated deletion in cardiac progenitor cells conferred by a 3'utr-ires-cre allele of the homeobox gene NKX2-5. Int. J. Dev. Biol. 2002, 46:431-439.
33. Heikinheimo M., Scandrett J.M., Wilson D.B. Localization of transcription factor gata-4 to regions of the mouse embryo involved in cardiac development. Dev. Biol. 1994, 164:361-373.
34. Yamaguchi T.P., Dumont D.J., Conlon R.A., Breitman M.L., Rossant J. Flk-1, an flt-related receptor tyrosine kinase is an early marker for endothelial cell precursors. Development 1993, 118:489-498.
35. Ferdous A., Caprioli A., Iacovino M., Martin C.M., Morris J., Richardson J.A., Latif S., Hammer R.E., Harvey R.P., Olson E.N., Kyba M., Garry D.J. NKX2-5 transactivates the ets-related protein 71 gene and specifies an endothelial/endocardial fate in the developing embryo. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:814-819.
36. Sumanas S., Lin S. Ets1-related protein is a key regulator of vasculogenesis in zebrafish. PLoS Biol. 2006, 4.
37. De Val S., Chi N.C., Meadows S.M., Minovitsky S., Anderson J.P., Harris I.S., Ehlers M.L., Agarwal P., Visel A., Xu S.M., Pennacchio L.A., Dubchak I., Krieg P.A., Stainier D.Y., Black B.L. Combinatorial regulation of endothelial gene expression by ets and forkhead transcription factors. Cell 2008, 135:1053-1064.
38. Palencia-Desai S., Kohli V., Kang J., Chi N.C., Black B.L., Sumanas S. Vascular endothelial and endocardial progenitors differentiate as cardiomyocytes in the absence of etsrp/etv2 function. Development 2011, 138:4721-4732.
39. Wong K.S., Proulx K., Rost M.S., Sumanas S. Identification of vasculature-specific genes by microarray analysis of etsrp/etv2 overexpressing zebrafish embryos. Dev. Dyn. 2009, 238:1836-1850.
40. de la Pompa J.L., Timmerman L.A., Takimoto H., Yoshida H., Elia A.J., Samper E., Potter J., Wakeham A., Marengere L., Langille B.L., Crabtree G.R., Mak T.W. Role of the nf-atc transcription factor in morphogenesis of cardiac valves and septum. Nature 1998, 392:182-186.
41. Ranger A.M., Grusby M.J., Hodge M.R., Gravallese E.M., de la Brousse F.C., Hoey T., Mickanin C., Baldwin H.S., Glimcher L.H. The transcription factor nf-atc is essential for cardiac valve formation. Nature 1998, 392:186-190.
42. Evans S.M., Yelon D., Conlon F.L., Kirby M.L. Myocardial lineage development. Circ. Res. 2010, 107:1428-1444.
43. von Gise A., Pu W.T. Endocardial and epicardial epithelial to mesenchymal transitions in heart development and disease. Circ. Res. 2012, 110:1628-1645.
44. Baldwin H.S. Early embryonic vascular development. Cardiovasc. Res. 1996, 31. (Spec No:E34-45).
45. Brown C.B., Boyer A.S., Runyan R.B., Barnett J.V. Requirement of type iii tgf-beta receptor for endocardial cell transformation in the heart. Science 1999, 283:2080-2082.
46. Harris I.S., Black B.L. Development of the endocardium. Pediatr. Cardiol. 2010, 31:391-399.
47. Barrallo-Gimeno A., Nieto M.A. The snail genes as inducers of cell movement and survival: implications in development and cancer. Development 2005, 132:3151-3161.
48. Moskowitz I.P., Wang J., Peterson M.A., Pu W.T., Mackinnon A.C., Oxburgh L., Chu G.C., Sarkar M., Berul C., Smoot L., Robertson E.J., Schwartz R., Seidman J.G., Seidman C.E. Transcription factor genes smad4 and gata4 cooperatively regulate cardiac valve development. [corrected]. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:4006-4011.
49. Timmerman L.A., Grego-Bessa J., Raya A., Bertrán E., Pérez-Pomares J.M., Díez J., Aranda S., Palomo S., McCormick F., Izpisúa-Belmonte J.C., de la Pompa J.L. Notch promotes epithelial-mesenchymal transition during cardiac development and oncogenic transformation. Genes Dev. 2004, 18:99-115.
50. Shelton E.L., Yutzey K.E. Twist1 function in endocardial cushion cell proliferation, migration, and differentiation during heart valve development. Dev. Biol. 2008, 317:282-295.
51. Akiyama H., Chaboissier M.C., Behringer R.R., Rowitch D.H., Schedl A., Epstein J.A., de Crombrugghe B. Essential role of sox9 in the pathway that controls formation of cardiac valves and septa. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:6502-6507.
52. Ma L., Lu M.F., Schwartz R.J., Martin J.F. Bmp2 is essential for cardiac cushion epithelial-mesenchymal transition and myocardial patterning. Development 2005, 132:5601-5611.
53. Enciso J.M., Gratzinger D., Camenisch T.D., Canosa S., Pinter E., Madri J.A. Elevated glucose inhibits vegf-a-mediated endocardial cushion formation: modulation by pecam-1 and mmp-2. J. Cell Biol. 2003, 160:605-615.
54. Garg V., Muth A.N., Ransom J.F., Schluterman M.K., Barnes R., King I.N., Grossfeld P.D., Srivastava D. Mutations in notch1 cause aortic valve disease. Nature 2005, 437:270-274.
55. Garside V.C., Chang A.C., Karsan A., Hoodless P.A. Co-ordinating notch, bmp, and tgf-β signaling during heart valve development. Cell. Mol. Life Sci. 2013, 70:2899-2917.
56. Wang Y., Wu B., Chamberlain A.A., Lui W., Koirala P., Susztak K., Klein D., Taylor V., Zhou B. Endocardial to myocardial notch-wnt-bmp axis regulates early heart valve development. PLoS One 2013, 8.
57. Kruithof B.P., Krawitz S.A., Gaussin V. Atrioventricular valve development during late embryonic and postnatal stages involves condensation and extracellular matrix remodeling. Dev. Biol. 2007, 302:208-217.
58. Chen H.I., Poduri A., Numi H., Kivela R., Saharinen P., McKay A.S., Raftrey B., Churko J., Tian X., Zhou B., Wu J.C., Alitalo K., Red-Horse K. Vegf-c and aortic cardiomyocytes guide coronary artery stem development. J. Clin. Invest. 2014, 124:4899-4914.
59. Lin C.J., Lin C.Y., Chen C.H., Zhou B., Chang C.P. Partitioning the heart: mechanisms of cardiac septation and valve development. Development 2012, 139:3277-3299.
60. Tian X., Pu W.T., Zhou B. Cellular origin and developmental program of coronary angiogenesis. Circ. Res. 2015, 116:515-530.
61. Dyer L., Pi X., Patterson C. Connecting the coronaries: how the coronary plexus develops and is functionalized. Dev. Biol. 2014, 395:111-119.
62. Wada A.M., Willet S.G., Bader D. Coronary vessel development: A unique form of vasculogenesis. Arterioscler. Thromb. Vasc. Biol. 2003, 23:2138-2145.
63. Lavine K.J., Ornitz D.M. Shared circuitry: developmental signaling Cascades regulate both embryonic and adult coronary vasculature. Circ. Res. 2009, 104:159-169.
64. Riley P.R., Smart N. Vascularizing the heart. Cardiovasc. Res. 2011, 91:260-268.
65. Zhou B., Ma Q., Rajagopal S., Wu S.M., Domian I., Rivera-Feliciano J., Jiang D., von Gise A., Ikeda S., Chien K.R., Pu W.T. Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature 2008, 454:109-113.
66. Cai C.L., Martin J.C., Sun Y., Cui L., Wang L., Ouyang K., Yang L., Bu L., Liang X., Zhang X., Stallcup W.B., Denton C.P., McCulloch A., Chen J., Evans S.M. A myocardial lineage derives from tbx18 epicardial cells. Nature 2008, 454:104-108.
67. Katz T.C., Singh M.K., Degenhardt K., Rivera-Feliciano J., Johnson R.L., Epstein J.A., Tabin C.J. Distinct compartments of the proepicardial organ give rise to coronary vascular endothelial cells. Dev. Cell 2012, 22:639-650.
68. Red-Horse K., Ueno H., Weissman I.L., Krasnow M.A. Coronary arteries form by developmental reprogramming of venous cells. Nature 2010, 464:549-553.
69. Wu B., Zhang Z., Lui W., Chen X., Wang Y., Chamberlain A.A., Moreno-Rodriguez R.A., Markwald R.R., O'Rourke B.P., Sharp D.J., Zheng D., Lenz J., Baldwin H.S., Chang C.P., Zhou B. Endocardial cells form the coronary arteries by angiogenesis through myocardial-endocardial vegf signaling. Cell 2012, 151:1083-1096.
70. Tian X., Hu T., Zhang H., He L., Huang X., Liu Q., Yu W., Yang Z., Yan Y., Yang X., Zhong T.P., Pu W.T., Zhou B. Vessel formation. De novo formation of a distinct coronary vascular population in neonatal heart. Science 2014, 345:90-94.
71. Ma Q., Zhou B., Pu W.T. Reassessment of isl1 and NKX2-5 cardiac fate maps using a gata4-based reporter of cre activity. Dev. Biol. 2008, 323:98-104.
72. Harrison M.R., Bussmann J., Huang Y., Zhao L., Osorio A., Burns C.G., Burns C.E., Sucov H.M., Siekmann A.F., Lien C.L. Chemokine-guided angiogenesis directs coronary vasculature formation in zebrafish. Dev. Cell 2015, 33:442-454.
73. Chen H.I., Sharma B., Akerberg B.N., Numi H.J., Kivelä R., Saharinen P., Aghajanian H., McKay A.S., Bogard P.E., Chang A.H., Jacobs A.H., Epstein J.A., Stankunas K., Alitalo K., Red-Horse K. The sinus venosus contributes to coronary vasculature through vegfc-stimulated angiogenesis. Development 2014, 141:4500-4512.
74. Tian X., Hu T., Zhang H., He L., Huang X., Liu Q., Yu W., Yang Z., Zhang Z., Zhong T.P., Yang X., Yan Y., Baldini A., Sun Y., Lu J., Schwartz R.J., Evans S.M., Gittenberger-de Groot A.C., Red-Horse K., Zhou B. Subepicardial endothelial cells invade the embryonic ventricle wall to form coronary arteries. Cell Res. 2013, 23:1075-1090.
75. Nakano H., Liu X., Arshi A., Nakashima Y., van Handel B., Sasidharan R., Harmon A.W., Shin J.H., Schwartz R.J., Conway S.J., Harvey R.P., Pashmforoush M., Mikkola H.K., Nakano A. Haemogenic endocardium contributes to transient definitive haematopoiesis. Nat. Commun. 2013, 4:1564.
76. Masino A.M., Gallardo T.D., Wilcox C.A., Olson E.N., Williams R.S., Garry D.J. Transcriptional regulation of cardiac progenitor cell populations. Circ. Res. 2004, 95:389-397.
77. Mandal L., Banerjee U., Hartenstein V. Evidence for a fruit fly hemangioblast and similarities between lymph-gland hematopoiesis in fruit fly and mammal aorta-gonadal-mesonephros mesoderm. Nat. Genet. 2004, 36:1019-1023.
78. Han Z., Olson E.N. Hand is a direct target of tinman and gata factors during drosophila cardiogenesis and hematopoiesis. Development 2005, 132:3525-3536.
79. Schoenebeck J.J., Keegan B.R., Yelon D. Vessel and blood specification override cardiac potential in anterior mesoderm. Dev. Cell 2007, 13:254-267.
80. Chen V.C., Stull R., Joo D., Cheng X., Keller G. Notch signaling respecifies the hemangioblast to a cardiac fate. Nat. Biotechnol. 2008, 26:1169-1178.
81. Peterkin T., Gibson A., Patient R. Common genetic control of haemangioblast and cardiac development in zebrafish. Development 2009, 136:1465-1474.
82. Nagel S., Venturini L., Przybylski G.K., Grabarczyk P., Schmidt C.A., Meyer C., Drexler H.G., Macleod R.A., Scherr M. Activation of mir-17-92 by nk-like homeodomain proteins suppresses apoptosis via reduction of e2f1 in t-cell acute lymphoblastic leukemia. Leuk. Lymphoma 2009, 50:101-108.
83. Su X., Della-Valle V., Delabesse E., Azgui Z., Berger R., Merle-Béral H., Bernard O.A., Nguyen-Khac F. Transcriptional activation of the cardiac homeobox gene csx1/NKX2-5 in a b-cell chronic lymphoproliferative disorder. Haematologica 2008, 93:1081-1085.
84. Nagel S., Meyer C., Quentmeier H., Kaufmann M., Drexler H.G., MacLeod R.A. Mef2c is activated by multiple mechanisms in a subset of t-acute lymphoblastic leukemia cell lines. Leukemia 2008, 22:600-607.
85. Nagel S., Scherr M., Kel A., Hornischer K., Crawford G.E., Kaufmann M., Meyer C., Drexler H.G., MacLeod R.A. Activation of tlx3 and NKX2-5 in t(5;14)(q35;q32) t-cell acute lymphoblastic leukemia by remote 3'-bcl11b enhancers and coregulation by pu.1 and hmga1. Cancer Res. 2007, 67:1461-1471.
86. Przybylski G.K., Dik W.A., Grabarczyk P., Wanzeck J., Chudobska P., Jankowski K., von Bergh A., van Dongen J.J., Schmidt C.A., Langerak A.W. The effect of a novel recombination between the homeobox gene NKX2-5 and the trd locus in t-cell acute lymphoblastic leukemia on activation of the NKX2-5 gene. Haematologica 2006, 91:317-321.
87. Dieterlen-Lièvre F. Emergence of haematopoietic stem cells during development. C R Biol. 2007, 330:504-509.
88. Orkin S.H., Zon L.I. Hematopoiesis: an evolving paradigm for stem cell biology. Cell 2008, 132:631-644.
89. Yoshimoto M., Porayette P., Yoder M.C. Overcoming obstacles in the search for the site of hematopoietic stem cell emergence. Cell Stem Cell 2008, 3:583-586.
90. Zovein A.C., Hofmann J.J., Lynch M., French W.J., Turlo K.A., Yang Y., Becker M.S., Zanetta L., Dejana E., Gasson J.C., Tallquist M.D., Iruela-Arispe M.L. Fate tracing reveals the endothelial origin of hematopoietic stem cells. Cell Stem Cell 2008, 3:625-636.
91. Bertrand J.Y., Chi N.C., Santoso B., Teng S., Stainier D.Y., Traver D. Haematopoietic stem cells derive directly from aortic endothelium during development. Nature 2010, 464:108-111.
92. Boisset J.C., van Cappellen W., Andrieu-Soler C., Galjart N., Dzierzak E., Robin C. In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium. Nature 2010, 464:116-120.
93. Kissa K., Herbomel P. Blood stem cells emerge from aortic endothelium by a novel type of cell transition. Nature 2010, 464:112-115.
94. Adamo L., Naveiras O., Wenzel P.L., McKinney-Freeman S., Mack P.J., Gracia-Sancho J., Suchy-Dicey A., Yoshimoto M., Lensch M.W., Yoder M.C., García-Cardeña G., Daley G.Q. Biomechanical forces promote embryonic haematopoiesis. Nature 2009, 459:1131-1135.
95. North T.E., Goessling W., Peeters M., Li P., Ceol C., Lord A.M., Weber G.J., Harris J., Cutting C.C., Huang P., Dzierzak E., Zon L.I. Hematopoietic stem cell development is dependent on blood flow. Cell 2009, 137:736-748.
96. Rasmussen T.L., Kweon J., Diekmann M.A., Belema-Bedada F., Song Q., Bowlin K., Shi X., Ferdous A., Li T., Kyba M., Metzger J.M., Koyano-Nakagawa N., Garry D.J. Er71 directs mesodermal fate decisions during embryogenesis. Development 2011, 138:4801-4812.
97. Schupp M.O., Waas M., Chun C.Z., Ramchandran R. Transcriptional inhibition of etv2 expression is essential for embryonic cardiac development. Dev. Biol. 2014, 393:71-83.
98. Gantz J.A., Palpant N.J., Welikson R.E., Hauschka S.D., Murry C.E., Laflamme M.A. Targeted genomic integration of a selectable floxed dual fluorescence reporter in human embryonic stem cells. PLoS One 2012, 7.
99. Palpant N.J., Pabon L., Rabinowitz J.S., Hadland B.K., Stoick-Cooper C.L., Paige S.L., Bernstein I.D., Moon R.T., Murry C.E. Transmembrane protein 88: a wnt regulatory protein that specifies cardiomyocyte development. Development 2013, 140:3799-3808.
100. Palpant N.J., Hofsteen P., Pabon L., Reinecke H., Murry C.E. Cardiac development in zebrafish and human embryonic stem cells is inhibited by exposure to tobacco cigarettes and e-cigarettes. PLoS One 2015, 10.
101. Palpant N.J., Pabon L., Roberts M., Hadland B., Jones D., Jones C., Moon R.T., Ruzzo W.L., Bernstein I., Zheng Y., Murry C.E. Inhibition of β-catenin signaling respecifies anterior-like endothelium into beating human cardiomyocytes. Development 2015.
102. Szabo L., Morey R., Palpant N.J., Wang P.L., Afari N., Jiang C., Parast M.M., Murry C.E., Laurent L.C., Salzman J. Statistically based splicing detection reveals neural enrichment and tissue-specific induction of circular rna during human fetal development. Genome Biol. 2015, 16:126.
103. Murry C.E., Keller G. Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell 2008, 132:661-680.
104. Lian X., Hsiao C., Wilson G., Zhu K., Hazeltine L.B., Azarin S.M., Raval K.K., Zhang J., Kamp T.J., Palecek S.P. Robust cardiomyocyte differentiation from human pluripotent stem cells via temporal modulation of canonical wnt signaling. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:E1848-E1857.
105. Lian X., Zhang J., Azarin S.M., Zhu K., Hazeltine L.B., Bao X., Hsiao C., Kamp T.J., Palecek S.P. Directed cardiomyocyte differentiation from human pluripotent stem cells by modulating wnt/β-catenin signaling under fully defined conditions. Nat. Protoc. 2013, 8:162-175.
106. White M.P., Rufaihah A.J., Liu L., Ghebremariam Y.T., Ivey K.N., Cooke J.P., Srivastava D. Limited gene expression variation in human embryonic stem cell and induced pluripotent stem cell-derived endothelial cells. Stem Cells 2013, 31:92-103.
107. Rafii S., Kloss C.C., Butler J.M., Ginsberg M., Gars E., Lis R., Zhan Q., Josipovic P., Ding B.S., Xiang J., Elemento O., Zaninovic N., Rosenwaks Z., Sadelain M., Rafii J.A., James D. Human esc-derived hemogenic endothelial cells undergo distinct waves of endothelial to hematopoietic transition. Blood 2013, 121:770-780.
108. Kennedy M., Awong G., Sturgeon C.M., Ditadi A., LaMotte-Mohs R., Zúñiga-Pflücker J.C., Keller G. T lymphocyte potential marks the emergence of definitive hematopoietic progenitors in human pluripotent stem cell differentiation cultures. Cell Rep. 2012, 2:1722-1735.
109. Choi K.D., Vodyanik M.A., Togarrati P.P., Suknuntha K., Kumar A., Samarjeet F., Probasco M.D., Tian S., Stewart R., Thomson J.A., Slukvin I.I. Identification of the hemogenic endothelial progenitor and its direct precursor in human pluripotent stem cell differentiation cultures. Cell Rep. 2012, 2:553-567.
110. Kennedy M., D'Souza S.L., Lynch-Kattman M., Schwantz S., Keller G. Development of the hemangioblast defines the onset of hematopoiesis in human es cell differentiation cultures. Blood 2007, 109:2679-2687.
111. Shiba Y., Fernandes S., Zhu W.Z., Filice D., Muskheli V., Kim J., Palpant N.J., Gantz J., Moyes K.W., Reinecke H., Van Biber B., Dardas T., Mignone J.L., Izawa A., Hanna R., Viswanathan M., Gold J.D., Kotlikoff M.I., Sarvazyan N., Kay M.W., Murry C.E., Laflamme M.A. Human es-cell-derived cardiomyocytes electrically couple and suppress arrhythmias in injured hearts. Nature 2012, 489:322-325.
112. Chong J.J., Yang X., Don C.W., Minami E., Liu Y.W., Weyers J.J., Mahoney W.M., Van Biber B., Cook S.M., Palpant N.J., Gantz J.A., Fugate J.A., Muskheli V., Gough G.M., Vogel K.W., Astley C.A., Hotchkiss C.E., Baldessari A., Pabon L., Reinecke H., Gill E.A., Nelson V., Kiem H.P., Laflamme M.A., Murry C.E. Human embryonic-stem-cell-derived cardiomyocytes regenerate non-human primate hearts. Nature 2014, 510:273-277.
113. Ditadi A., Sturgeon C.M., Tober J., Awong G., Kennedy M., Yzaguirre A.D., Azzola L., Ng E.S., Stanley E.G., French D.L., Cheng X., Gadue P., Speck N.A., Elefanty A.G., Keller G. Human definitive haemogenic endothelium and arterial vascular endothelium represent distinct lineages. Nat. Cell Biol. 2015, 17:580-591.
114. Xu P.F., Houssin N., Ferri-Lagneau K.F., Thisse B., Thisse C. Construction of a vertebrate embryo from two opposing morphogen gradients. Science 2014, 344:87-89.
115. Gadue P., Huber T.L., Paddison P.J., Keller G.M. Wnt and tgf-beta signaling are required for the induction of an in vitro model of primitive streak formation using embryonic stem cells. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:16806-16811.
116. Nostro M.C., Cheng X., Keller G.M., Gadue P. Wnt, activin, and bmp signaling regulate distinct stages in the developmental pathway from embryonic stem cells to blood. Cell Stem Cell 2008, 2:60-71.
117. Mendjan S., Mascetti V.L., Ortmann D., Ortiz M., Karjosukarso D.W., Ng Y., Moreau T., Pedersen R.A. Nanog and cdx2 pattern distinct subtypes of human mesoderm during exit from pluripotency. Cell Stem Cell 2014.
118. Faial T., Bernardo A.S., Mendjan S., Diamanti E., Ortmann D., Gentsch G.E., Mascetti V.L., Trotter M.W., Smith J.C., Pedersen R.A. Brachyury and smad signalling collaboratively orchestrate distinct mesoderm and endoderm gene regulatory networks in differentiating human embryonic stem cells. Development 2015, 142:2121-2135.
119. Paige S.L., Osugi T., Afanasiev O.K., Pabon L., Reinecke H., Murry C.E. Endogenous wnt/beta-catenin signaling is required for cardiac differentiation in human embryonic stem cells. PLoS One 2010, 5.
120. Ueno S., Weidinger G., Osugi T., Kohn A.D., Golob J.L., Pabon L., Reinecke H., Moon R.T., Murry C.E. Biphasic role for wnt/beta-catenin signaling in cardiac specification in zebrafish and embryonic stem cells. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:9685-9690.
121. Wu B., Wang Y., Lui W., Langworthy M., Tompkins K.L., Hatzopoulos A.K., Baldwin H.S., Zhou B. Nfatc1 coordinates valve endocardial cell lineage development required for heart valve formation. Circ. Res. 2011, 109:183-192.
122. Maska E.L., Cserjesi P., Hua L.L., Garstka M.E., Brody H.M., Morikawa Y. A tlx2-cre mouse line uncovers essential roles for hand1 in extraembryonic and lateral mesoderm. Genesis 2010, 48:479-484.
123. Zhang R., Han P., Yang H., Ouyang K., Lee D., Lin Y.F., Ocorr K., Kang G., Chen J., Stainier D.Y., Yelon D., Chi N.C. In vivo cardiac reprogramming contributes to zebrafish heart regeneration. Nature 2013, 498:497-501.
124. Porrello E.R., Mahmoud A.I., Simpson E., Hill J.A., Richardson J.A., Olson E.N., Sadek H.A. Transient regenerative potential of the neonatal mouse heart. Science 2011, 331:1078-1080.
125. Palpant N.J., Metzger J.M. Aesthetic cardiology: adipose-derived stem cells for myocardial repair. Curr. Stem Cell Res. Ther. Jun 2010, 5(2):145-152. (Review).
126. Palpant N.J., Yasuda S., MacDougald O., Metzger J.M. Non-canonical wnt signaling enhances differentiation of sca1+/c-kit+ adipose-derived murine stromal vascular cells into spontaneously beating cardiac myocytes. J. Mol. Cell. Cardiol. 2007, 43:362-370.
127. Murry C.E., Kay M.A., Bartosek T., Hauschka S.D., Schwartz S.M. Muscle differentiation during repair of myocardial necrosis in rats via gene transfer with myod. J. Clin. Invest. 1996, 98:2209-2217.
128. Lattanzi L., Salvatori G., Coletta M., Sonnino C., Cusella de Angelis M.G., gioglio L., CE Murry, Kelly R., Ferrari G., Molinaro M., Crescenzi M., Mavilio F., G. Cossu High efficiency myogenic conversion of human fibroblasts by adenoviral vector-mediated myod gene transfer. An alternative strategy for ex vivo gene therapy of primary myopathies. J. Clin. Invest. 1998, 101:2119-2128.
129. Palpant N.J., Murry C.E. Regenerative medicine: reprogramming the injured heart. Nature 2012, 485:585-586.
130. Murry C.E., Palpant N.J., MacLellan W.R. Cardiopoietry in motion: primed mesenchymal stem cells for ischemic cardiomyopathy. J. Am. Coll. Cardiol. 2013, 61:2339-2340.
131. Palpant N.J., Murry C.E. Proliferation at the heart of preadolescence. Cell 2014, 157:765-767.
132. Wu S.M., Fujiwara Y., Cibulsky S.M., Clapham D.E., Lien C.L., Schultheiss T.M., Orkin S.H. Developmental origin of a bipotential myocardial and smooth muscle cell precursor in the mammalian heart. Cell 2006, 127:1137-1150.
133. Paige S.L., Thomas S., Stoick-Cooper C.L., Wang H., Maves L., Sandstrom R., Pabon L., Reinecke H., Pratt G., Keller G., Moon R.T., Stamatoyannopoulos J., Murry C.E. A temporal chromatin signature in human embryonic stem cells identifies regulators of cardiac development. Cell 2012, 151:221-232.
134. Ieda M., Fu J.D., Delgado-Olguin P., Vedantham V., Hayashi Y., Bruneau B.G., Srivastava D. Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell 2010, 142:375-386.
135. Pang Z.P., Yang N., Vierbuchen T., Ostermeier A., Fuentes D.R., Yang T.Q., Citri A., Sebastiano V., Marro S., Südhof T.C., Wernig M. Induction of human neuronal cells by defined transcription factors. Nature 2011, 476:220-223.
136. Cowan C.A., Atienza J., Melton D.A., Eggan K. Nuclear reprogramming of somatic cells after fusion with human embryonic stem cells. Science 2005, 309:1369-1373.
137. Zhou Q., Brown J., Kanarek A., Rajagopal J., Melton D.A. In vivo reprogramming of adult pancreatic exocrine cells to beta-cells. Nature 2008, 455:627-632.
138. Papapetrou E.P., Tomishima M.J., Chambers S.M., Mica Y., Reed E., Menon J., Tabar V., Mo Q., Studer L., Sadelain M. Stoichiometric and temporal requirements of oct4, sox2, klf4, and c-myc expression for efficient human ipsc induction and differentiation. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:12759-12764.
139. Takeuchi J.K., Bruneau B.G. Directed transdifferentiation of mouse mesoderm to heart tissue by defined factors. Nature 2009, 459:708-711.
140. Szabo E., Rampalli S., Risueño R.M., Schnerch A., Mitchell R., Fiebig-Comyn A., Levadoux-Martin M., Bhatia M. Direct conversion of human fibroblasts to multilineage blood progenitors. Nature 2010, 468:521-526.
141. Anokye-Danso F., Trivedi C.M., Juhr D., Gupta M., Cui Z., Tian Y., Zhang Y., Yang W., Gruber P.J., Epstein J.A., Morrisey E.E. Highly efficient mirna-mediated reprogramming of mouse and human somatic cells to pluripotency. Cell Stem Cell 2011, 8:376-388.
142. Burridge P.W., Keller G., Gold J.D., Wu J.C. Production of de novo cardiomyocytes: human pluripotent stem cell differentiation and direct reprogramming. Cell Stem Cell 2012, 10:16-28.
143. Takahashi K., Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126:663-676.
144. Van Handel B., Montel-Hagen A., Sasidharan R., Nakano H., Ferrari R., Boogerd C.J., Schredelseker J., Wang Y., Hunter S., Org T., Zhou J., Li X., Pellegrini M., Chen J.N., Orkin S.H., Kurdistani S.K., Evans S.M., Nakano A., Mikkola H.K. Scl represses cardiomyogenesis in prospective hemogenic endothelium and endocardium. Cell 2012, 150:590-605.
145. Fioret B.A., Heimfeld J.D., Paik D.T., Hatzopoulos A.K. Endothelial cells contribute to generation of adult ventricular myocytes during cardiac homeostasis. Cell Rep. 2014, 8:229-241.
146. Willems E., Spiering S., Davidovics H., Lanier M., Xia Z., Dawson M., Cashman J., Mercola M. Small-molecule inhibitors of the wnt pathway potently promote cardiomyocytes from human embryonic stem cell-derived mesoderm. Circ. Res. 2011, 109:360-364.
147. Klaus A., Saga Y., Taketo M.M., Tzahor E., Birchmeier W. Distinct roles of wnt/beta-catenin and bmp signaling during early cardiogenesis. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:18531-18536.
148. Kattman S.J., Witty A.D., Gagliardi M., Dubois N.C., Niapour M., Hotta A., Ellis J., Keller G. Stage-specific optimization of activin/nodal and bmp signaling promotes cardiac differentiation of mouse and human pluripotent stem cell lines. Cell Stem Cell 2011, 8:228-240.
149. R. Jain, Li D,M. Gupta, Manderfield LJ, Ifkovits JL, Q.Wang, F. Liu, Y. Liu, A. Poleshko, A. Padmanabhan, Raum JC, Li L, Morrisey EE, Lu MM, Won KJ, Epstein JA, Heart development. Integration of bmp and wnt signaling by hopx specifies commitment of cardiomyoblasts. Science 2015, 348:aaa6071.
150. Moignard V., Woodhouse S., Haghverdi L., Lilly A.J., Tanaka Y., Wilkinson A.C., Buettner F., Macaulay I.C., Jawaid W., Diamanti E., Nishikawa S., Piterman N., Kouskoff V., Theis F.J., Fisher J., Göttgens B. Decoding the regulatory network of early blood development from single-cell gene expression measurements. Nat. Biotechnol. 2015, 33:269-276.
151. Treutlein B., Brownfield D.G., Wu A.R., Neff N.F., Mantalas G.L., Espinoza F.H., Desai T.J., Krasnow M.A., Quake S.R. Reconstructing lineage hierarchies of the distal lung epithelium using single-cell rna-seq. Nature 2014, 509:371-375.
152. Trapnell C., Cacchiarelli D., Grimsby J., Pokharel P., Li S., Morse M., Lennon N.J., Livak K.J., Mikkelsen T.S., Rinn J.L. The dynamics and regulators of cell fate decisions are revealed by pseudotemporal ordering of single cells. Nat. Biotechnol. 2014, 32:381-386.
153. Zhou X., Crow A.L., Hartiala J., Spindler T.J., Ghazalpour A., Barsky L.W., Bennett B.B., Parks B.W., Eskin E., Jain R., Epstein J.A., Lusis A.J., Adams G.B., Allayee H. The genetic landscape of hematopoietic stem cell frequency in mice. Stem Cell Reports 2015.
154. Yutzey K.E., Bader D. Diversification of cardiomyogenic cell lineages during early heart development. Circ. Res. 1995, 77:216-219.
155. Sturgeon C.M., Ditadi A., Awong G., Kennedy M., Keller G. Wnt signaling controls the specification of definitive and primitive hematopoiesis from human pluripotent stem cells. Nat. Biotechnol. 2014, 32:554-561.
156. Little M.H., Takasato M. Generating a self-organizing kidney from pluripotent cells. Curr. Opin. Organ Transplant. 2015, 20:178-186.
157. Takasato M., Little M.H. The origin of the mammalian kidney: implications for recreating the kidney in vitro. Development 2015, 142:1937-1947.
158. Coulombe K.L., Bajpai V.K., Andreadis S.T., Murry C.E. Heart regeneration with engineered myocardial tissue. Annu. Rev. Biomed. Eng. 2014, 16:1-28.
159. Lancaster M.A., Knoblich J.A. Generation of cerebral organoids from human pluripotent stem cells. Nat. Protoc. 2014, 9:2329-2340.
160. Lancaster M.A., Knoblich J.A. Organogenesis in a dish: modeling development and disease using organoid technologies. Science 2014, 345:1247125.
161. Laflamme M.A., Chen K.Y., Naumova A.V., Muskheli V., Fugate J.A., Dupras S.K., Reinecke H., Xu C., Hassanipour M., Police S., O'Sullivan C., Collins L., Chen Y., Minami E., Gill E.A., Ueno S., Yuan C., Gold J., Murry C.E. Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat. Biotechnol. 2007, 25:1015-1024.
162. Burridge P.W., Matsa E., Shukla P., Lin Z.C., Churko J.M., Ebert A.D., Lan F., Diecke S., Huber B., Mordwinkin N.M., Plews J.R., Abilez O.J., Cui B., Gold J.D., Wu J.C. Chemically defined generation of human cardiomyocytes. Nat. Methods 2014, 11:855-860.
163. Witty A.D., Mihic A., Tam R.Y., Fisher S.A., Mikryukov A., Shoichet M.S., Li R.K., Kattman S.J., Keller G. Generation of the epicardial lineage from human pluripotent stem cells. Nat. Biotechnol. 2014, 32:1026-1035.
164. Iyer D., Gambardella L., Bernard W.G., Serrano F., Mascetti V.L., Pedersen R.A., Talasila A., Sinha S. Robust derivation of epicardium and its differentiated smooth muscle cell progeny from human pluripotent stem cells. Development 2015, 142:1528-1541.
165. Kreutziger K.L., Muskheli V., Johnson P., Braun K., Wight T.N., Murry C.E. Developing vasculature and stroma in engineered human myocardium. Tissue Eng. Part A. 2011, 17:1219-1228.
166. Tulloch N.L., Muskheli V., Razumova M.V., Korte F.S., Regnier M., Hauch K.D., Pabon L., Reinecke H., Murry C.E. Growth of engineered human myocardium with mechanical loading and vascular coculture. Circ. Res. 2011, 109:47-59.