Generation of vascular endothelial and smooth muscle cells from human pluripotent stem cells

Nature Cell Biology

Volumn 17, Issue 8, 2015, Pages 994-1003

  Patsch, Christoph ^a   Challet Meylan, Ludivine ^b   Thoma, Eva C ^a   Urich, Eduard ^a   Heckel, Tobias ^a   O'Sullivan, John F ^c   Grainger, Stephanie J ^d,e   Kapp, Friedrich G ^f   Sun, Lin ^c   Christensen, Klaus ^a   Xia, Yulei ^b   Florido, Mary H C ^b   He, Wei ^a   Pan, Wei ^a   Prummer, Michael ^a   Warren, Curtis R ^b   Jakob Roetne, Roland ^a   Certa, Ulrich ^a   Jagasia, Ravi ^a   Freskgard, Per Ola ^a   Adatto, Isaac ^c   Kling, Dorothee ^a   Huang, Paul ^c   Zon, Leonard I ^b,f   Chaikof, Elliot L ^d,e   Gerszten, Robert E ^c   Graf, Martin ^a   Iacone, Roberto ^a   Cowan, Chad A ^b,c,f   more..

^a F HOFFMANN LA ROCHE LTD   (Switzerland)

^b Harvard University   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e HARVARD UNIVERSITY   (United States)

^f BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1BETA; TRANSCRIPTION FACTOR SOX17; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN; VASCULOTROPIN A; BIOLOGICAL MARKER; BONE MORPHOGENETIC PROTEIN 4; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; PLATELET DERIVED GROWTH FACTOR B; PLATELET-DERIVED GROWTH FACTOR BB; PROTEIN KINASE INHIBITOR;

ARTICLE; CALCIUM TRANSPORT; CELL ADHESION; CELL DENSITY; CELL DIFFERENTIATION; CELL RENEWAL; CONTROLLED STUDY; ENDOTHELIUM CELL; GENE EXPRESSION; LEUKOCYTE ADHERENCE; MESODERM; METABOLOMICS; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMOOTH MUSCLE FIBER; UPREGULATION; VASCULAR ENDOTHELIUM; ANGIOGENESIS; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINE; CELL LINEAGE; COCULTURE; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; HUMAN; METABOLISM; NONOBESE DIABETIC MOUSE; PHENOTYPE; PHYSIOLOGY; PROCEDURES; SCID MOUSE; TIME; TRANSPLANTATION; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULAR SMOOTH MUSCLE; WNT SIGNALING PATHWAY;

ANIMALS; BIOMARKERS; BONE MORPHOGENETIC PROTEIN 4; CELL DIFFERENTIATION; CELL LINE; CELL LINEAGE; COCULTURE TECHNIQUES; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIAL CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLYCOGEN SYNTHASE KINASE 3; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; METABOLOMICS; MICE, INBRED NOD; MICE, SCID; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NEOVASCULARIZATION, PHYSIOLOGIC; PHENOTYPE; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-SIS; TIME FACTORS; TRANSCRIPTION, GENETIC; TRANSFECTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; WNT SIGNALING PATHWAY;

EID: 84938743523     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3205     Document Type: Article

References (55)

1. Thomson, J. A. et al. Embryonic stem cell lines derived from human blastocysts. Science 282, 1145-1147 (1998
2. Takahashi, K. et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861-872 (2007
3. Yu, J. et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 318, 1917-1920 (2007
4. Grskovic, M., Javaherian, A., Strulovici, B. & Daley, G. Q. Induced pluripotent stem cells-opportunities for disease modelling and drug discovery. Nat. Rev. Drug Discov. 10, 915-929 (2011
5. Tiscornia, G., Vivas, E. L. & Belmonte, J. C. Diseases in a dish: modeling human genetic disorders using induced pluripotent cells. Nat. Med. 17, 1570-1576 (2011
6. Zhu, H., Lensch, M. W., Cahan, P. & Daley, G. Q. Investigating monogenic and complex diseases with pluripotent stem cells. Nat. Rev. Genet. 12, 266-275 (2011
7. James, D. et al. Expansion and maintenance of human embryonic stem cell-derived endothelial cells by TGFbeta inhibition is Id1 dependent. Nat. Biotechnol. 28, 161-166 (2010
8. Levenberg, S., Golub, J. S., Amit, M., Itskovitz-Eldor, J. & Langer, R. Endothelial cells derived from human embryonic stem cells. Proc. Natl Acad. Sci. USA 99, 4391-4396 (2002
9. Kane, N. M. et al. Derivation of endothelial cells from human embryonic stem cells by directed differentiation: analysis of microRNA and angiogenesis in vitro and in vivo. Arterioscler. Thromb. Vasc. Biol. 30, 1389-1397 (2010
10. Vodyanik, M. A., Bork, J. A., Thomson, J. A. & Slukvin, II Human embryonic stem cell-derived CD34C cells: efficient production in the coculture with OP9 stromal cells and analysis of lymphohematopoietic potential. Blood 105, 617-626 (2005
11. Li, Z. et al. Comparison of reporter gene and iron particle labeling for tracking fate of human embryonic stem cells and differentiated endothelial cells in living subjects. Stem Cells 26, 864-873 (2008
12. Wang, H. et al. Gene expression profile signatures indicate a role for Wnt signaling in endothelial commitment from embryonic stem cells. Circ. Res. 98, 1331-1339 (2006
13. Levenberg, S., Zoldan, J., Basevitch, Y. & Langer, R. Endothelial potential of human embryonic stem cells. Blood 110, 806-814 (2007
14. Kelly, M. A. & Hirschi, K. K. Signaling hierarchy regulating human endothelial cell development. Arterioscler. Thromb. Vasc. Biol. 29, 718-724 (2009
15. Wang, Z. Z. et al. Endothelial cells derived from human embryonic stem cells form durable blood vessels in vivo. Nat. Biotechnol. 25, 317-318 (2007
16. 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
17. Inman, G. et al. SB-431542 is a potent and specific inhibitor of transforming growth factor-superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol. Pharmacol. 62, 65-74 (2002
18. Orlova, V. V. et al. Functionality of endothelial cells and pericytes from human pluripotent stem cells demonstrated in cultured vascular plexus and zebrafish xenografts. Arterioscler. Thromb. Vasc. Biol. 34, 177-186 (2014
19. Yamashita, J. et al. Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors. Nature 408, 92-96 (2000
20. Tam, P. P. & Loebel, D. A. Gene function in mouse embryogenesis: get set for gastrulation. Nat. Rev. Genet. 8, 368-381 (2007
21. Huelsken, J. et al. Requirement for beta-catenin in anterior-posterior axis formation in mice. J. Cell Biol. 148, 567-578 (2000
22. Liu, Y., Festing, M. H., Hester, M., Thompson, J. C. & Weinstein, M. Generation of novel conditional and hypomorphic alleles of the Smad2 gene. Genesis 40, 118-123 (2004
23. Woll, P. S. et al. Wnt signaling promotes hematoendothelial cell development from human embryonic stem cells. Blood 111, 122-131 (2008
24. Brade, T., Manner, J. & Kuhl, M. The role of Wnt signalling in cardiac development and tissue remodelling in the mature heart. Cardiovasc. Res. 72, 198-209 (2006
25. Park, C. et al. A hierarchical order of factors in the generation of FLK1-And SCLexpressing hematopoietic and endothelial progenitors from embryonic stem cells. Development 131, 2749-2762 (2004
26. Tada, S. et al. Characterization of mesendoderm: a diverging point of the definitive endoderm and mesoderm in embryonic stem cell differentiation culture. Development 132, 4363-4374 (2005
27. 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
28. Bone, H. K., Nelson, A. S., Goldring, C. E., Tosh, D. & Welham, M. J. A novel chemically directed route for the generation of definitive endoderm from human embryonic stem cells based on inhibition of GSK-3. J. Cell Sci. 124, 1992-2000 (2011
29. Sato, N., Meijer, L., Skaltsounis, L., Greengard, P. & Brivanlou, A. H. Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat. Med. 10, 55-63 (2004
30. Fabian, M. A. et al. A small molecule-kinase interaction map for clinical kinase inhibitors. Nat. Biotechnol. 23, 329-336 (2005
31. Soker, S., Takashima, S., Miao, H. Q., Neufeld, G. & Klagsbrun, M. Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 92, 735-745 (1998
32. DeAlmeida, V. I. et al. The soluble wnt receptor Frizzled8CRD-hFc inhibits the growth of teratocarcinomas in vivo. Cancer Res. 67, 5371-5379 (2007
33. Winnier, G., Blessing, M., Labosky, P. A. & Hogan, B. L. Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev. 9, 2105-2116 (1995
34. Watanabe, K. et al. A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat. Biotechnol. 25, 681-686 (2007
35. Yamamizu, K., Kawasaki, K., Katayama, S., Watabe, T. & Yamashita, J. K. Enhancement of vascular progenitor potential by protein kinase A through dual induction of Flk-1 and Neuropilin-1. Blood 114, 3707-3716 (2009
36. Englund, M. C. et al. The establishment of 20 different human embryonic stem cell lines and subclones; a report on derivation, culture, characterisation and banking. In Vitro Cell. Dev. Biol. Anim. 46, 217-230 (2010
37. Burridge, P. W. et al. A universal system for highly efficient cardiac differentiation of human induced pluripotent stem cells that eliminates interline variability. PLoS ONE 6, e18293 (2011
38. Chan, M. C. et al. Molecular basis for antagonism between PDGF and the TGFbeta family of signalling pathways by control of miR-24 expression. EMBO J. 29, 559-573 (2010
39. Owens, G. K., Kumar, M. S. & Wamhoff, B. R. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol. Rev. 84, 767-801 (2004
40. Cheung, C., Bernardo, A. S., Trotter, M. W., Pedersen, R. A. & Sinha, S. Generation of human vascular smooth muscle subtypes provides insight into embryological origin-dependent disease susceptibility. Nat. Biotechnol. 30, 165-173 (2012
41. Engert, S., Liao, W. P., Burtscher, I. & Lickert, H. Sox17-2A-iCre: a knock-in mouse line expressing Cre recombinase in endoderm and vascular endothelial cells. Genesis 47, 603-610 (2009
42. Atienza, J. M. et al. Dynamic and label-free cell-based assays using the real-Time cell electronic sensing system. Assay Drug Dev. Technol. 4, 597-607 (2006
43. Solly, K., Wang, X., Xu, X., Strulovici, B. & Zheng, W. Application of real-Time cell electronic sensing (RT-CES) technology to cell-based assays. Assay Drug Dev. Technol. 2, 363-372 (2004
44. Rabiet, M. J. et al. Thrombin-induced increase in endothelial permeability is associated with changes in cell-To-cell junction organization. Arterioscler. Thromb. Vasc. Biol. 16, 488-496 (1996
45. Galkina, E. & Ley, K. Vascular adhesion molecules in atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 27, 2292-2301 (2007
46. Lusis, A. J. Atherosclerosis. Nature 407, 233-241 (2000
47. Rasmussen, L. M., Wolf, Y. G. & Ruoslahti, E. Vascular smooth muscle cells from injured rat aortas display elevated matrix production associated with transforming growth factor-beta activity. Am. J. Pathol. 147, 1041-1048 (1995
48. Grainger, S. J., Carrion, B., Ceccarelli, J. & Putnam, A. J. Stromal cell identity influences the in vivo functionality of engineered capillary networks formed by co-delivery of endothelial cells and stromal cells. Tissue Eng. Part A 19, 1209-1222 (2013
49. Cowan, C. A. et al. Derivation of embryonic stem-cell lines from human blastocysts. N. Engl. J. Med. 350, 1353-1356 (2004
50. Warren, L. et al. Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell 7, 618-630 (2010
51. Challet Meylan, L., Patsch, C. & Thoma, E. C. Endothelial cells differentiation from hPSCs. Nat. Protoc. Exch. http: //dx.doi.org/10.1038/protex.2015.055 (2015
52. Thoma, E. C., Challet Meylan, L. & Patsch, C. Vascular smooth muscle cells differentiation from hPSCs. Nat. Protoc. Exch. http: //dx.doi.org/10.1038/protex. 2015.056 (2015
53. Gotlieb, A. I. & Spector, W. Migration into an in vitro experimental wound: a comparison of porcine aortic endothelial and smooth muscle cells and the effect of culture irradiation. Am. J. Pathol. 103, 271-282 (1981
54. Collins, S. J., Gallo, R. C. & Gallagher, R. E. Continuous growth and differentiation of human myeloid leukaemic cells in suspension culture. Nature 270, 347-349 (1977
55. Wang, T. J. et al. Metabolite profiles and the risk of developing diabetes. Nat. Med. 17, 448-453 (2011