Microfibrous substrate geometry as a critical trigger for organization, self-renewal, and differentiation of human embryonic stem cells within synthetic 3-dimensional microenvironments

FASEB Journal

Volumn 26, Issue 8, 2012, Pages 3240-3251

  Carlson, Aaron L ^a   Florek, Charles A ^a,b   Kim, Joseph J ^a   Neubauer, Thomas ^a   Moore, Jennifer C ^c,d   Cohen, Rick I ^c,d   Kohn, Joachim ^b,c   Grumet, Martin ^c,d   Moghe, Prabhas V ^a,e  

^a RUTGERS UNIVERSITY   (United States)

^b RUTGERS UNIVERSITY   (United States)

^c RUTGERS UNIVERSITY   (United States)

^d RUTGERS UNIVERSITY   (United States)

^e The State University of New Jersey   (United States)

Author keywords

Fibrous scaffolds; Poly D lysine; Tissue engineering

Indexed keywords

LAMININ; MATRIGEL; POLYLYSINE; SCAFFOLD PROTEIN; SCLEROPROTEIN;

ARTICLE; CELL ADHESION; CELL CONTACT; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL RENEWAL; CELL VIABILITY; COLONY FORMATION; CONTROLLED STUDY; ELECTROSPINNING; EMBRYONIC STEM CELL; FIBER; GEOMETRY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; THREE DIMENSIONAL IMAGING;

BIOPOLYMERS; CELL ADHESION; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL PROLIFERATION; COLLAGEN; DRUG COMBINATIONS; EMBRYONIC STEM CELLS; HUMANS; LAMININ; POLYLYSINE; PROTEOGLYCANS; STEREOISOMERISM; TISSUE SCAFFOLDS; TYROSINE;

EID: 84864762783     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-192732     Document Type: Article

References (52)

1. Thomson, J. A., Itskovitz-Eldor, J., Shapiro, S. S., Waknitz, M. A., Swiergiel, J. J., Marshall, V. S., and Jones, J. M. (1998) Embryonic stem cell lines derived from human blastocysts. Science 282, 1145-1147 (Pubitemid 28516247)
2. Reubinoff, B. E., Pera, M. F., Fong, C.-Y., Trounson, A., and Bongso, A. (2000) Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro. Nat. Biotech. 18, 399-404 (Pubitemid 30217526)
3. Ariff Bongso, C.-Y. F., Kalamegam Gauthaman, (2008) Taking stem cells to the clinic: major challenges. J. Cell. Biochem. 105, 1352-1360
4. McDevitt, T. C., and Palecek, S. P. (2008) Innovation in the culture and derivation of pluripotent human stem cells. Curr. Opin. Biotech. 19, 527-533
5. Yao, S., Chen, S., Clark, J., Hao, E., Beattie, G. M., Hayek, A., and Ding, S. (2006) Long-term self-renewal and directed differentiation of human embryonic stem cells in chemically defined conditions. Proc. Natl. Acad. Sci. U. S. A. 103, 6907-6912
6. Ludwig, T. E., Levenstein, M. E., Jones, J. M., Berggren, W. T., Mitchen, E. R., Frane, J. L., Crandall, L. J., Daigh, C. A., Conard, K. R., Piekarczyk, M. S., Llanas, R. A., and Thomson, J. A. (2006) Derivation of human embryonic stem cells in defined conditions. Nat. Biotech. 24, 185-187 (Pubitemid 43221701)
7. Brafman, D. A., Chang, C. W., Fernandez, A., Willert, K., Varghese, S., and Chien, S. (2010) Long-term human pluripotent stem cell self-renewal on synthetic polymer surfaces. Biomaterials 31, 9135-9144
8. Villa-Diaz, L. G., Nandivada, H., Ding, J., Nogueira-de-Souza, N. C., Krebsbach, P. H., O'Shea, K. S., Lahann, J., and Smith, G. D. (2010) Synthetic polymer coatings for long-term growth of human embryonic stem cells. Nat. Biotech. 28, 581-583
9. Melkoumian, Z., Weber, J. L., Weber, D. M., Fadeev, A. G., Zhou, Y., Dolley-Sonneville, P., Yang, J., Qiu, L., Priest, C. A., Shogbon, C., Martin, A. W., Nelson, J., West, P., Beltzer, J. P., Pal, S., and Brandenberger, R. (2010) Synthetic peptide-acrylate surfaces for long-term self-renewal and cardiomyocyte differentiation of human embryonic stem cells. Nat. Biotech. 28, 606-610
10. Watt, F. M., and Hogan, B. L. M. (2000) Out of Eden: stem cells and their niches. Science 287, 1427-1430 (Pubitemid 30127126)
11. Burdick, J. A., and Vunjak-Novakovic, G. (2008) Engineered microenvironments for controlled stem cell differentiation. Tissue Eng. A 15, 205-219
12. Lee, J., Cuddihy, M. J., and Kotov, N. A. (2008) Three-dimensional cell culture matrices: state of the art. Tissue Eng. B 14, 61
13. Berrier, A. L., and Yamada, K. M. (2007) Cell-matrix adhesion. J. Cell. Physiol. 213, 565-573 (Pubitemid 350058247)
14. Doyle, A. D., Wang, F. W., Matsumoto, K., and Yamada, K. M. (2009) One-dimensional topography underlies three-dimensional fibrillar cell migration. J. Cell Biol. 184, 481-490
15. Ranucci, C. S., Kumar, A., Batra, S. P., and Moghe, P. V. (2000) Control of hepatocyte function on collagen foams: sizing matrix pores toward selective induction of 2-D and 3-D cellular morphogenesis. Biomaterials 21, 783-793 (Pubitemid 30216433)
16. Liu, H., Lin, J., and Roy, K. (2006) Effect of 3D scaffold and dynamic culture condition on the global gene expression profile of mouse embryonic stem cells. Biomaterials 27, 5978-5989 (Pubitemid 44414971)
17. Levenberg, S., Huang, N. F., Lavik, E., Rogers, A. B., Itskovitz-Eldor, J., and Langer, R. (2003) Differentiation of human embryonic stem cells on three-dimensional polymer scaffolds. Proc. Natl. Acad. Sci. U. S. A. 100, 12741-12746 (Pubitemid 37339969)
18. Bahney, C. S., Hsu, C.-W., Yoo, J. U., West, J. L., and Johnstone, B. (2011) A bioresponsive hydrogel tuned to chondrogenesis of human mesenchymal stem cells. FASEB J. 25, 1486-1496
19. Gerecht, S., Burdick, J. A., Ferreira, L. S., Townsend, S. A., Langer, R., and Vunjak-Novakovic, G. (2007) Hyaluronic acid hydrogel for controlled self-renewal and differentiation of human embryonic stem cells. Proc. Natl. Acad. Sci. U. S. A. 104, 11298-11303 (Pubitemid 47175135)
20. Li, Z., Leung, M., Hopper, R., Ellenbogen, R., and Zhang, M. (2010) Feeder-free self-renewal of human embryonic stem cells in 3D porous natural polymer scaffolds. Biomaterials 31, 404-412
21. Gauthaman, K., Venugopal, J. R., Yee, F. C., Peh, G. S. L., Ramakrishna, S., and Bongso, A. (2009) Nanofibrous substrates support colony formation and maintain stemness of human embryonic stem cells. J. Cell. Mol. Med. 13, 3475-3484
22. Ferreira, L. S., Gerecht, S., Fuller, J., Shieh, H. F., Vunjak-Novakovic, G., and Langer, R. (2007) Bioactive hydrogel scaffolds for controllable vascular differentiation of human embryonic stem cells. Biomaterials 28, 2706-2717 (Pubitemid 46420712)
23. Smith, L. A., Liu, X., Hu, J., and Ma, P. X. (2010) The enhancement of human embryonic stem cell osteogenic differentiation with nano-fibrous scaffolding. Biomaterials 31, 5526-5535
24. Yang, F., Cho, S.-W., Son, S. M., Hudson, S. P., Bogatyrev, S., Keung, L., Kohane, D. S., Langer, R., and Anderson, D. G. (2010) Combinatorial extracellular matrices for human embryonic stem cell differentiation in 3D. Biomacromolecules 11, 1909-1914
25. Shahbazi, E., Kiani, S., Gourabi, H., and Baharvand, H. (2011) Electrospun nanofibrillar surfaces promote neuronal differentiation and function from human embryonic stem cells. Tissue Eng. A 17, 3021-3031
26. Ertel, S. I., and Kohn, J. (1994) Evaluation of a series of tyrosine-derived polycarbonates as degradable biomaterials. J. Biomed. Mater. Res. 28, 919-930 (Pubitemid 24237855)
27. Meechaisue, C., Dubin, R., Supaphol, P., Hoven, V. P., and Kohn, J. (2006) Electrospun mat of tyrosine-derived polycarbonate fibers for potential use as tissue scaffolding material. J. Biomater. Sci. Polym. Ed. 17, 1039-1056 (Pubitemid 44559974)
28. Treiser, M. D., Yang, E. H., Gordonov, S., Cohen, D. M., Androulakis, I. P., Kohn, J., Chen, C. S., and Moghe, P. V. (2009) Cytoskeleton-based forecasting of stem cell lineage fates. Proc. Natl. Acad. Sci. U. S. A. 107, 610-615
29. Liu, E., Treiser, M. D., Johnson, P. A., Patel, P., Rege, A., Kohn, J., and Moghe, P. V. (2007) Quantitative biorelevant profiling of material microstructure within 3D porous scaffolds via multiphoton fluorescence microscopy. J. Biomed. Mater. Res. B Appl. Biomater. 82B, 284-297 (Pubitemid 47106232)
30. Ludwig, T. E., Bergendahl, V., Levenstein, M. E., Yu, J., Probasco, M. D., and Thomson, J. A. (2006) Feeder-independent culture of human embryonic stem cells. Nat. Meth. 3, 637-646 (Pubitemid 44123431)
31. Bajpai, R., Lesperance, J., Kim, M., and Terskikh, A. V. (2008) Efficient propagation of single cells accutase-dissociated human embryonic stem cells. Mol. Reprod. Dev. 75, 818-827 (Pubitemid 351438945)
32. Watanabe, K., Ueno, M., Kamiya, D., Nishiyama, A., Matsumura, M., Wataya, T., Takahashi, J. B., Nishikawa, S., Nishikawa, S., Muguruma, K., and Sasai, Y. (2007) A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat. Biotech. 25, 681-686 (Pubitemid 46897207)
33. Nat, R., Nilbratt, M., Narkilahti, S., Winblad, B., Hovatta, O., and Nordberg, A. (2007) Neurogenic neuroepithelial and radial glial cells generated from six human embryonic stem cell lines in serum-free suspension and adherent cultures. Glia 55, 385-399
34. Hu, B.-Y., and Zhang, S.-C. (2010) Directed differentiation of neural-stem cells and subtype-specific neurons from hESCs. In Cellular Programming and Reprogramming Vol. 636, pp. 123-137, Humana Press, New York
35. Chen, Y.-F., Tseng, C.-Y., Wang, H.-W., Kuo, H.-C., Yang, V. W., and Lee, O. K. (2011) Rapid generation of mature hepatocyte-like cells from human induced pluripotent stem cells by an efficient three-step protocol. Hepatology 55, 1193-1203
36. Huang, H., Zhao, X., Chen, L., Xu, C., Yao, X., Lu, Y., Dai, L., and Zhang, M. (2006) Differentiation of human embryonic stem cells into smooth muscle cells in adherent monolayer culture. Biochem. Biophys. Res. Commun. 351, 321-327 (Pubitemid 44666692)
37. Meng, Y., Eshghi, S., Li, Y. J., Schmidt, R., Schaffer, D. V., and Healy, K. E. (2010) Characterization of integrin engagement during defined human embryonic stem cell culture. FASEB J. 24, 1056-1065
38. Braam, S. R., Zeinstra, L., Litjens, S., Ward-van Oostwaard, D., van den Brink, S., van Laake, L., Lebrin, F., Kats, P., Hochstenbach, R., Passier, R., Sonnenberg, A., and Mummery, C. L. (2008) Recombinant vitronectin is a functionally defined substrate that supports human embryonic stem cell self-renewal via αVβ5 integrin. Stem Cells 26, 2257-2265
39. Sands, R. W., and Mooney, D. J. (2007) Polymers to direct cell fate by controlling the microenvironment. Curr. Opin. Biotech. 18, 448-453 (Pubitemid 350116593)
40. Dawson, E., Mapili, G., Erickson, K., Taqvi, S., and Roy, K. (2008) Biomaterials for stem cell differentiation. Adv. Drug Deliv. Rev. 60, 215-228 (Pubitemid 350236400)
41. Stevens, M. M., and George, J. H. (2005) Exploring and engineering the cell surface interface. Science 310, 1135-1138 (Pubitemid 41681731)
42. Cukierman, E., Pankov, R., Stevens, D. R., and Yamada, K. M. (2001) Taking cell-matrix adhesions to the third dimension. Science 294, 1708-1712 (Pubitemid 33104840)
43. Lim, S. H., Liu, X. Y., Song, H., Yarema, K. J., and Mao, H.-Q. (2010) The effect of nanofiber-guided cell alignment on the preferential differentiation of neural stem cells. Biomaterials 31, 9031-9039
44. Tai, B. C. U., Wan, A. C. A., and Ying, J. Y. (2010) Modified polyelectrolyte complex fibrous scaffold as a matrix for 3D cell culture. Biomaterials 31, 5927-5935
45. Lim, S. H., and Mao, H.-Q. (2009) Electrospun scaffolds for stem cell engineering. Adv. Drug Deliv. Rev. 61, 1084-1096
46. Cao, H., Liu, T., and Chew, S. Y. (2009) The application of nanofibrous scaffolds in neural tissue engineering. Adv. Drug Deliv. Rev. 61, 1055-1064
47. Carlberg, B., Axell, M. Z., Nannmark, U., Liu, J., and Kuhn, H. G. (2009) Electrospun polyurethane scaffolds for proliferation and neuronal differentiation of human embryonic stem cells. Biomed. Mater. 4, 045004
48. Mahairaki, V., Lim, S. H., Christopherson, G. T., Xu, L., Nasonkin, I., Yu, C., Mao, H.-Q., and Koliatsos, V. E. (2011) Nanofiber matrices promote the neuronal differentiation of human embryonic stem cell derived-neural precursors in vitro. Tissue Eng. A. 17, 855-863
49. Ouyang, A., Ng, R., and Yang, S. T. (2007) Long-term culturing of undifferentiated embryonic stem cells in conditioned media and three-dimensional fibrous matrices without extracellular matrix coating. Stem Cells 25, 447-454 (Pubitemid 46232800)
50. Gao, S. Y., Lees, J. G., Wong, J. C. Y., Croll, T. I., George, P., Cooper-White, J. J., and Tuch, B. E. (2010) Modeling the adhesion of human embryonic stem cells to poly(lactic-coglycolic acid) surfaces in a 3D environment. J. Biomed. Mater. Res. A. 92A, 683-692
51. Miyazaki, T., Futaki, S., Hasegawa, K., Kawasaki, M., Sanzen, N., Hayashi, M., Kawase, E., Sekiguchi, K., Nakatsuji, N., and Suemori, H. (2008) Recombinant human laminin isoforms can support the undifferentiated growth of human embryonic stem cells. Biochem. Biophys. Res. Commun. 375, 27-32
52. Bourke, S. L., and Kohn, J. (2003) Polymers derived from the amino acid -tyrosine: polycarbonates, polyarylates and copolymers with poly(ethylene glycol). Adv. Drug Deliv. Rev. 55, 447-466 (Pubitemid 36423299)