A microparticle approach to morphogen delivery within pluripotent stem cell aggregates

Biomaterials

Volumn 34, Issue 30, 2013, Pages 7227-7235

  Bratt Leal, Andrés M ^a   Nguyen, Anh H ^a   Hammersmith, Katy A ^a   Singh, Ankur ^b   McDevitt, Todd C ^a  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Bone morphogenic protein; Differentiation; Embryoid body; Embryonic stem cells; Mesoderm; Microparticle

Indexed keywords

BONE MORPHOGENIC PROTEIN; EMBRYOID BODY; EMBRYONIC STEM CELLS; MESODERM; MICRO PARTICLES;

BIOLOGICAL MATERIALS; BIOMATERIALS; DIFFERENTIATION (CALCULUS); GENE EXPRESSION; STEM CELLS; THREE DIMENSIONAL;

AGGREGATES;

BONE MORPHOGENETIC PROTEIN 4; GELATIN; NOGGIN;

ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL FATE; CELL LINEAGE; CONTROLLED STUDY; ECTODERM; FLOW CYTOMETRY; GENE EXPRESSION; HUMAN; HUMAN CELL; MESODERM; PLURIPOTENT STEM CELL; PRIORITY JOURNAL;

BONE MORPHOGENIC PROTEIN; DIFFERENTIATION; EMBRYOID BODY; EMBRYONIC STEM CELLS; MESODERM; MICROPARTICLE;

ANIMALS; BONE MORPHOGENETIC PROTEIN 4; CELL AGGREGATION; CELL DIFFERENTIATION; COCULTURE TECHNIQUES; EMBRYOID BODIES; GELATIN; MESODERM; MICE; MICROSPHERES; PLURIPOTENT STEM CELLS; SPHEROIDS, CELLULAR;

EID: 84880508868     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2013.05.079     Document Type: Article

References (32)

1. Doetschman T.C., Eistetter H., Katz M., Schmidt W., Kemler R. The invitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. JEmbryol Exp Morphol 1985, 87:27-45.
2. Bratt-Leal A.M., Carpenedo R.L., Ungrin M.D., Zandstra P.W., McDevitt T.C. Incorporation of biomaterials in multicellular aggregates modulates pluripotent stem cell differentiation. Biomaterials 2011, 32:48-56.
3. Keller G.M. Invitro differentiation of embryonic stem cells. Curr Opin Cell Biol 1995, 7:862-869.
4. 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 1995, 9:2105-2116.
5. Czyz J., Wobus A. Embryonic stem cell differentiation: the role of extracellular factors. Differentiation 2001, 68:167-174.
6. Chambers S.M., Fasano C.A., Papapetrou E.P., Tomishima M., Sadelain M., Studer L. Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat Biotechnol 2009, 27:275-280.
7. Lee H., Shamy G.A., Elkabetz Y., Schofield C.M., Harrsion N.L., Panagiotakos G., et al. Directed differentiation and transplantation of human embryonic stem cell-derived motoneurons. Stem Cells 2007, 25:1931-1939.
8. Carpenedo R.L., Bratt-Leal A.M., Marklein R.A., Seaman S.A., Bowen N.J., McDonald J.F., et al. Homogeneous and organized differentiation within embryoid bodies induced by microsphere-mediated delivery of small molecules. Biomaterials 2009, 30:2507-2515.
9. Sachlos E., Auguste D.T. Embryoid body morphology influences diffusive transport of inductive biochemicals: a strategy for stem cell differentiation. Biomaterials 2008, 29:4471-4480.
10. Van Winkle A.P., Gates I.D., Kallos M.S. Mass transfer limitations in embryoid bodies during human embryonic stem cell differentiation. Cells Tissues Organs 2012, 196:34-47.
11. Jing D., Parikh A., Tzanakakis E.S. Cardiac cell generation from encapsulated embryonic stem cells in static and scalable culture systems. Cell Transplant 2010, 19:1397-1412.
12. Carpenedo R.L., Sargent C.Y., McDevitt T.C. Rotary suspension culture enhances the efficiency, yield and homogeneity of embryoid body differentiation. Stem Cells 2007, 25(9):2224-2234.
13. Ungrin M.D., Joshi C., Nica A., Bauwens C., Zandstra P.W. Reproducible, ultra high-throughput formation of multicellular organization from single cell suspension-derived human embryonic stem cell aggregates. PLoS ONE 2008, 3:e1565.
14. Nguyen D., Sa S., Pegan J.D., Rich B., Xiang G., McCloskey K.E., et al. Tunable shrink-induced honeycomb microwell arrays for uniform embryoid bodies. Lab Chip 2009, 9:3338-3344.
15. Fehling H.J., Lacaud G., Kubo A., Kennedy M., Robertson S., Keller G., et al. Tracking mesoderm induction and its specification to the hemangioblast during embryonic stem cell differentiation. Development 2003, 130:4217-4227.
16. Rahman N., Purpura K.A., Wylie R.G., Zandstra P.W., Shoichet M.S. The use of vascular endothelial growth factor functionalized agarose to guide pluripotent stem cell aggregates toward blood progenitor cells. Biomaterials 2010, 31:8262-8270.
17. Pfaffl M.W. Anew mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29:e45.
18. Purpura K.A., Bratt-Leal A.M., Hammersmith K.A., McDevitt T.C., Zandstra P.W. Systematic engineering of 3D pluripotent stem cell niches to guide blood development. Biomaterials 2012, 33:1271-1280.
19. Yang L., Soonpaa M.H., Adler E.D., Roepke T.K., Kattman S.J., Kennedy M., et al. Human cardiovascular progenitor cells develop from a KDR+ embryonic-stem-cell-derived population. Nature 2008, 453:524-528.
20. Pick M., Azzola L., Mossman A., Stanley E.G., Elefanty A.G. Differentiation of human embryonic stem cells in serum-free medium reveals distinct roles for bone morphogenetic protein 4, vascular endothelial growth factor, stem cell factor, and fibroblast growth factor 2 in hematopoiesis. Stem Cells 2007, 25:2206-2214.
21. Pearson S., Sroczynska P., Lacaud G., Kouskoff V. The stepwise specification of embryonic stem cells to hematopoietic fate is driven by sequential exposure to Bmp4, activin A, bFGF and VEGF. Development 2008, 135:1525-1535.
22. Purpura K.A., Morin J., Zandstra P.W. Analysis of the temporal and concentration-dependent effects of BMP-4, VEGF, and TPO on development of embryonic stem cell-derived mesoderm and blood progenitors in a defined, serum-free media. Exp Hematol 2008, 36:1186-1198.
23. Bratt-Leal A.M., Kepple K.L., Carpenedo R.L., Cooke M.T., McDevitt T.C. Magnetic manipulation and spatial patterning of multi-cellular stem cell aggregates. Integr Biol (Camb) 2011, 3:1224-1232.
24. Kraushaar D.C., Rai S., Condac E., Nairn A., Zhang S., Yamaguchi Y., et al. Heparan sulfate facilitates FGF and BMP signaling to drive mesoderm differentiation of mouse embryonic stem cells. JBiol Chem 2012, 287:22691-22700.
25. Khan S.A., Nelson M.S., Pan C., Gaffney P.M., Gupta P. Endogenous heparan sulfate and heparin modulate bone morphogenetic protein-4 signaling and activity. Am J Physiol Cell Physiol 2008, 294:C1387-C1397.
26. Impellitteri N.A., Toepke M.W., Lan Levengood S.K., Murphy W.L. Specific VEGF sequestering and release using peptide-functionalized hydrogel microspheres. Biomaterials 2012, 33:3475-3484.
27. Hudalla G.A., Kouris N.A., Koepsel J.T., Ogle B.M., Murphy W.L. Harnessing endogenous growth factor activity modulates stem cell behavior. Integr Biol (Camb) 2011, 3:832-842.
28. Benoit D.S., Anseth K.S. Heparin functionalized PEG gels that modulate protein adsorption for hMSC adhesion and differentiation. Acta Biomater 2005, 1:461-470.
29. Nair R., Ngangan A.V., Kemp M.L., McDevitt T.C. Gene expression signatures of extracellular matrix and growth factors during embryonic stem cell differentiation. PLoS ONE 2012, 7:e42580.
30. Petersen D.R., Gustavsen C., Lindskog S.R., Magnuson M.A., Zaret K.S., Serup P. Engineering artificial signaling centers to polarize embryoid body differentiation. Stem Cells Dev 2012, 21:647-653.
31. Sharon N., Mor I., Golan-lev T., Fainsod A., Benvenisty N. Molecular and functional characterizations of gastrula organizer cells derived from human embryonic stem cells. Stem Cells 2011, 29:600-608.
32. ten Berge D., Koole W., Fuerer C., Fish M., Eroglu E., Nusse R. Wnt signaling mediates self-organization and axis formation in embryoid bodies. Cell Stem Cell 2008, 3:508-518.