Generating high-purity cardiac and endothelial derivatives from patterned mesoderm using human pluripotent stem cells

Nature Protocols

Volumn 12, Issue 1, 2017, Pages 15-31

  Palpant, Nathan J ^a   Pabon, Lil ^b   Friedman, Clayton E ^a,b   Roberts, Meredith ^b   Hadland, Brandon ^b   Zaunbrecher, Rebecca J ^b   Bernstein, Irwin ^b   Zheng, Ying ^b   Murry, Charles E ^b  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN A; BONE MORPHOGENETIC PROTEIN 4;

ARTICLE; CARDIAC MUSCLE CELL; CELL CULTURE; CELL DIFFERENTIATION; CELL POLARITY; CELL POPULATION; COLONY FORMING UNIT; ENDOTHELIUM CELL; FLOW CYTOMETRY; HUMAN; INDUCED PLURIPOTENT STEM CELL; LIMIT OF QUANTITATION; MESODERM; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REPRODUCIBILITY; CARDIAC MUSCLE; CELL CULTURE TECHNIQUE; CELL LINE; CELL LINEAGE; CYTOLOGY; PLURIPOTENT STEM CELL; PROCEDURES;

CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL LINE; CELL LINEAGE; ENDOTHELIAL CELLS; HUMANS; MESODERM; MYOCARDIUM; PLURIPOTENT STEM CELLS;

EID: 85000786709     PISSN: 17542189     EISSN: 17502799     Source Type: Journal    
DOI: 10.1038/nprot.2016.153     Document Type: Article

References (49)

1. Murry, C.E. & Keller, G. Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell 132, 661-680 (2008).
2. Xu, P.F., Houssin, N., Ferri-Lagneau, K.F., Thisse, B. & Thisse, C. Construction of a vertebrate embryo from two opposing morphogen gradients. Science 344, 87-89 (2014).
3. Kattman, S.J. et al. Stage-specific optimization of activin/nodal and BMP signaling promotes cardiac differentiation of mouse and human pluripotent stem cell lines. Cell Stem Cell 8, 228-240 (2011).
4. 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 2, 60-71 (2008).
5. Sumi, T., Tsuneyoshi, N., Nakatsuji, N. & Suemori, H. Defining early lineage specification of human embryonic stem cells by the orchestrated balance of canonical Wnt/beta-catenin, Activin/Nodal and BMP signaling. Development 135, 2969-2979 (2008).
6. Palpant, N.J. et al. Inhibition of β-catenin signaling respecifies anterior-like endothelium into beating human cardiomyocytes. Development 142, 3198-209 (2015).
7. Palpant, N.J. et al. Transmembrane protein 88: a Wnt regulatory protein that specifies cardiomyocyte development. Development 140, 3799-3808 (2013).
8. Wamstad, J.A. et al. Dynamic and coordinated epigenetic regulation of developmental transitions in the cardiac lineage. Cell 151, 206-220 (2012).
9. Willems, E. et al. Small-molecule inhibitors of the Wnt pathway potently promote cardiomyocytes from human embryonic stem cell-derived mesoderm. Circ. Res. 109, 360-364 (2011).
10. Mendjan, S. et al. NANOG and CDX2 pattern distinct subtypes of human mesoderm during exit from pluripotency. Cell Stem Cell 15, 310-325 (2014).
11. Faial, T. et al. Brachyury and SMAD signalling collaboratively orchestrate distinct mesoderm and endoderm gene regulatory networks in differentiating human embryonic stem cells. Development 142, 2121-2135 (2015).
12. Yutzey, K.E. & Bader, D. Diversification of cardiomyogenic cell lineages during early heart development. Circ. Res. 77, 216-219 (1995).
13. Van Handel, B. et al. Scl represses cardiomyogenesis in prospective hemogenic endothelium and endocardium. Cell 150, 590-605 (2012).
14. Rafii, S. et al. Human ESC-derived hemogenic endothelial cells undergo distinct waves of endothelial to hematopoietic transition. Blood 121, 770-780 (2013).
15. Nourse, M.B. et al. VEGF induces differentiation of functional endothelium from human embryonic stem cells: implications for tissue engineering. Arterioscler. Thromb. Vasc. Biol. 30, 80-89 (2010).
16. Orlova, V.V. et al. Generation, expansion and functional analysis of endothelial cells and pericytes derived from human pluripotent stem cells. Nat. Protoc. 9, 1514-1531 (2014).
17. Levenberg, S., Ferreira, L.S., Chen-Konak, L., Kraehenbuehl, T.P. & Langer, R. Isolation, differentiation and characterization of vascular cells derived from human embryonic stem cells. Nat. Protoc. 5, 1115-1126 (2010).
18. 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 109, 2679-2687 (2007).
19. White, M.P. et al. Limited gene expression variation in human embryonic stem cell and induced pluripotent stem cell-derived endothelial cells. Stem Cells 31, 92-103 (2013).
20. Misfeldt, A.M. et al. Endocardial cells are a distinct endothelial lineage derived from Flk1+ multipotent cardiovascular progenitors. Dev. Biol. 333, 78-89 (2009).
21. Peterkin, T., Gibson, A. & Patient, R. Common genetic control of haemangioblast and cardiac development in zebrafish. Development 136, 1465-1474 (2009).
22. de la Pompa, J.L. et al. Role of the NF-ATc transcription factor in morphogenesis of cardiac valves and septum. Nature 392, 182-186 (1998).
23. Ranger, A.M. et al. The transcription factor NF-ATc is essential for cardiac valve formation. Nature 392, 186-190 (1998).
24. Morikawa, Y. & Cserjesi, P. Extra-embryonic vasculature development is regulated by the transcription factor HAND1. Development 131, 2195-2204 (2004).
25. Barnes, R.M., Firulli, B.A., Conway, S.J., Vincentz, J.W. & Firulli, A.B. Analysis of the Hand1 cell lineage reveals novel contributions to cardiovascular, neural crest, extra-embryonic, and lateral mesoderm derivatives. Dev. Dyn. 239, 3086-3097 (2010).
26. Burridge, P.W. et al. Chemically defined generation of human cardiomyocytes. Nat. Methods 11, 855-860 (2014).
27. Lian, X. et al. Directed cardiomyocyte differentiation from human pluripotent stem cells by modulating Wnt/β-catenin signaling under fully defined conditions. Nat. Protoc. 8, 162-175 (2013).
28. Lian, X. et al. Robust cardiomyocyte differentiation from human pluripotent stem cells via temporal modulation of canonical Wnt signaling. Proc. Natl. Acad. Sci. USA 109, E1848-E1857 (2012).
29. Kempf, H., Kropp, C., Olmer, R., Martin, U. & Zweigerdt, R. Cardiac differentiation of human pluripotent stem cells in scalable suspension culture. Nat. Protoc. 10, 1345-1361 (2015).
30. Ditadi, A. et al. Human definitive haemogenic endothelium and arterial vascular endothelium represent distinct lineages. Nat. Cell Biol. 17, 580-591 (2015).
31. Witty, A.D. et al. Generation of the epicardial lineage from human pluripotent stem cells. Nat. Biotechnol. 32, 1026-1035 (2014).
32. Zhang, J. et al. Extracellular matrix promotes highly efficient cardiac differentiation of human pluripotent stem cells: the matrix sandwich method. Circ. Res. 111, 1125-1136 (2012).
33. Paige, S.L. et al. Endogenous Wnt/beta-catenin signaling is required for cardiac differentiation in human embryonic stem cells. PLoS One 5, e11134 (2010).
34. Ueno, S. et al. Biphasic role for Wnt/beta-catenin signaling in cardiac specification in zebrafish and embryonic stem cells. Proc. Natl. Acad. Sci. USA 104, 9685-9690 (2007).
35. Mummery, C.L. et al. Differentiation of human embryonic stem cells and induced pluripotent stem cells to cardiomyocytes: a methods overview. Circ. Res. 111, 344-358 (2012).
36. Lian, X., Zhang, J., Zhu, K., Kamp, T.J. & Palecek, S.P. Insulin inhibits cardiac mesoderm, not mesendoderm, formation during cardiac differentiation of human pluripotent stem cells and modulation of canonical Wnt signaling can rescue this inhibition. Stem Cells 31, 447-457 (2013).
37. Dubois, N.C. et al. SIRPA is a specific cell-surface marker for isolating cardiomyocytes derived from human pluripotent stem cells. Nat. Biotechnol. 29, 1011-1018 (2011).
38. Gantz, J.A. et al. Targeted genomic integration of a selectable floxed dual fluorescence reporter in human embryonic stem cells. PLoS One 7, e46971 (2012).
39. Ovchinnikov, D.A. et al. Isolation of contractile cardiomyocytes from human pluripotent stem-cell-derived cardiomyogenic cultures using a human NCX1-EGFP reporter. Stem Cells Dev. 24, 11-20 (2015).
40. Elliott, D.A. et al. NKX2-5(eGFP/w) hESCs for isolation of human cardiac progenitors and cardiomyocytes. Nat. Methods 8, 1037-1040 (2011).
41. Tohyama, S. et al. Distinct metabolic flow enables large-scale purification of mouse and human pluripotent stem cell-derived cardiomyocytes. Cell Stem Cell 12, 127-137 (2013).
42. Ciau-Uitz, A., Pinheiro, P., Gupta, R., Enver, T. & Patient, R. Tel1/ETV6 specifies blood stem cells through the agency of VEGF signaling. Dev. Cell 18, 569-578 (2010).
43. Ciau-Uitz, A., Pinheiro, P., Kirmizitas, A., Zuo, J. & Patient, R. VEGFA-dependent and -independent pathways synergise to drive Scl expression and initiate programming of the blood stem cell lineage in Xenopus. Development 140, 2632-2642 (2013).
44. Kennedy, M. et al. T lymphocyte potential marks the emergence of definitive hematopoietic progenitors in human pluripotent stem cell differentiation cultures. Cell Rep. 2, 1722-1735 (2012).
45. Choi, K.D. et al. Identification of the hemogenic endothelial progenitor and its direct precursor in human pluripotent stem cell differentiation cultures. Cell Rep. 2, 553-567 (2012).
46. Nakano, A., Nakano, H., Smith, K. & Palpant, N.J. The developmental origins and lineage contributions of endocardial endothelium. Biochim. Biophys. Acta 1863, 1937-1947 (2016).
47. Nakano, H. et al. Haemogenic endocardium contributes to transient definitive haematopoiesis. Nat. Commun. 4, 1564 (2013).
48. 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. 32, 554-561 (2014).
49. Zheng, Y. et al. In vitro microvessels for the study of angiogenesis and thrombosis. Proc. Natl. Acad. Sci. USA 109, 9342-9347 (2012).