Three-dimensional differentiation of embryonic stem cells into islet-like insulin-producing clusters

Tissue Engineering - Part A

Volumn 15, Issue 8, 2009, Pages 1941-1952

  Wang, Xiuli ^a,b   Ye, Kaiming ^a  

^a UNIVERSITY OF ARKANSAS   (United States)

^b Tufts University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINES; CELL MEMBRANES; GENE EXPRESSION; GLUCOSE; INSULIN; PEPTIDES; THREE DIMENSIONAL;

3-D ENVIRONMENTS; 3D CULTURE; ADULT MICE; CELL CLUSTERS; CELL THERAPY; EMBRYONIC STEM CELLS; ENDOCRINE CELLS; ES CELLS; GENE EXPRESSION PROFILES; GLUCOSE TRANSPORTERS; GLUCOSE-RESPONSIVE; INSULIN RELEASE; PANCREATIC CELLS; PANCREATIC ISLET; PEPTIDE SYNTHESIS; THREE-DIMENSIONAL (3D); TISSUE STRUCTURE; TWO-DIMENSIONAL;

CELL CULTURE;

ACTIVIN A; C PEPTIDE; CYCLOPAMINE; FIBROBLAST GROWTH FACTOR; GLUCOSE; GLUCOSE TRANSPORTER 2; INSULIN;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL THERAPY; CONTROLLED STUDY; DIABETES MELLITUS; EMBRYONIC STEM CELL; ENDOCRINE CELL; GENE EXPRESSION REGULATION; INSULIN RELEASE; MOUSE; NONHUMAN; PANCREAS CELL; PANCREAS ISLET BETA CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; THREE DIMENSIONAL IMAGING;

ANIMALS; BIOLOGICAL MARKERS; CELL AGGREGATION; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; EMBRYO, MAMMALIAN; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLUCOSE; IMMUNOHISTOCHEMISTRY; INSULIN; INSULIN-SECRETING CELLS; MICE; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STAINING AND LABELING;

EID: 68749116401     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2008.0181     Document Type: Article

References (42)

1. Meier, J.J., Bhushan, A., and Butler, P.C. The potential for stem cell therapy in diabetes. Pediatr Res 59, 65R, 2006.
2. Madsen, O.D., and Serup, P. Towards cell therapy for diabetes. Nat Biotechnol 24, 1481, 2006.
3. Gangaram-Panday, S.T., Faas, M.M., and de Vos, P. Towards stem-cell therapy in the endocrine pancreas. Trends Mol Med 13, 164, 2007.
4. Xu, X., Kahan, B., Forgianni, A., Jing, P., Jacobson, L., Browning, V., Treff, N., and Odorico, J. Endoderm and pancreatic islet lineage differentiation from human embryonic stem cells. Cloning Stem Cells 8, 96, 2006.
5. Segev, FL, Fishman, B., Ziskind, A., Shulman, M., and Itskovitz-Eldor, J. Differentiation of human embryonic stem cells into insulin-producing clusters. Stem Cells 22, 265, 2004.
6. D'Amour, K.A., Bang, A.G., Eliazer, S., Kelly, O.G., Agul-nick, A.D., Smart, N.G., Moorman, M.A., Kroon, E., Carpenter, M.K., and Baetge, E.E. Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells. Nat Biotechnol 24, 1392, 2006.
7. Shim, J.H., Kim, S.E., Woo, D.H., Kim, S.K., Oh, C.H., McKay, R., and Kim, J.H. Directed differentiation of human embryonic stem cells towards a pancreatic cell fate. Diabe-tologia 50, 1228, 2007.
8. Jiang, W., Shi, Y., Zhao, D., Chen, S., Yong, J., Zhang, J., Qing, T., Sun, X., Zhang, P., Ding, M., Li, D., and Deng, H. In vitro derivation of functional insulin-producing cells from human embryonic stem cells. Cell Res 17, 333, 2007.
9. Kania, G., Blyszczuk, P., and Wobus, A.M. The generation of insulin-producing cells from embryonic stem cells - a discussion of controversial findings. Int J Dev Biol 48, 1061, 2004.
10. Rolletschek, A., Kania, G., and Wobus, A.M. Generation of pancreatic insulin-producing cells from embryonic stem cells - 'proof of principle', but questions still unanswered. Diabetologia 49, 2541, 2006.
11. Sipione, S., Eshpeter, A., Lyon, J.G., Korbutt, G.S., and Bleackley, R.C. Insulin expressing cells from differentiated embryonic stem cells are not beta cells. Diabetologia 47, 499, 2004.
12. Hansson, M., Tonning, A., Frandsen, U., Petri, A., Rajagopal, J., Englund, M.C., Heller, R.S., Hakansson, J., Fleckner, J., Skold, H.N., Melton, D., Semb, PL, and Serup, P. Artifactual insulin release from differentiated embryonic stem cells. Diabetes 53, 2603, 2004.
13. Lumelsky, N., Blondel, O., Laeng, P., Velasco, I., Ravin, R., and McKay, R. Differentiation of embryonic stem cells to insulin-secreting structures similar to pancreatic islets. Science 292, 1389, 2001.
14. Rajagopal, J., Anderson, W.J., Kume, S., Martinez, O.I., and Melton, D. A. Insulin staining of ES cell progeny from insulin uptake. Science 299, 363, 2003.
15. Baharvand, F.L., Jafary, FL, Massumi, M., and Ashtiani, S.K. Generation of insulin-secreting cells from human embryonic stem cells. Dev Growth Differ 48, 323, 2006.
16. Brolen, G.K., Heins, N., Edsbagge, J., and Semb, H. Signals from the embryonic mouse pancreas induce differentiation of human embryonic stem cells into insulin-producing beta-cell-like cells. Diabetes 54, 2867, 2005.
17. Mfopou, J.K., Willems, E., Leyns, L., and Bouwens, L. Expression of regulatory genes for pancreas development during murine embryonic stem cell differentiation. Int J Dev Biol 49, 915, 2005.
18. Tarn, P.P., Williams, E.A., and Chan, W.Y. Gastrulation in the mouse embryo: ultrastructural and molecular aspects of germ layer morphogenesis. Microsc Res Tech 26, 301, 1993.
19. Watt, F.M., and Hogan, B.L. Out of Eden: stem cells and their niches. Science 287, 1427, 2000.
20. Czyz, J., and Wobus, A. Embryonic stem cell differentiation: the role of extracellular factors. Differ Res Biol Divers 68, 167, 2001.
21. Grayson, W.L., Ma, T., and Bunnell, B. Human mesenchymal stem cells tissue development in 3D PET matrices. Biotechnol Prog 20, 905, 2004.
22. Schmeichel, K.L., and Bissell, M.J. Modeling tissue-specific signaling and organ function in three dimensions. J Cell Sci 116, 2377, 2003.
23. Levenberg, S., Huang, N.F., Lavik, E., Rogers, A.B., Itskovitz-Eldor, J., and Langer, R. Differentiation of human embryonic stem cells on three-dimensional polymer scaffolds. Proc Natl Acad Sci USA 100, 12741, 2003.
24. Liu, H., and Roy, K. Biomimetic three-dimensional cultures significantly increase hematopoietic differentiation efficacy of embryonic stem cells. Tissue Eng 11, 319, 2005.
25. Mohr, J.C., de Pablo, J.J., and Palecek, S.P. 3-D microwell culture of human embryonic stem cells. Biomaterials 27, 6032, 2006.
26. Falasca, L., Miccheli, A., Sartori, E., Tomassini, A., and Conti Devirgiliis, L. Hepatocytes entrapped in alginate gelbeads and cultured in bioreactor: rapid repolarization and reconstitution of adhesion areas. Cells Tissues Organs 168, 126, 2001.
27. Yim, E.K., and Leong, K.W. Proliferation and differentiation of human embryonic germ cell derivatives in bioactive polymeric fibrous scaffold. J Biomater Sci 16, 1193, 2005.
28. Shi, Y., Hou, L., Tang, F., Jiang, W., Wang, P., Ding, M., and Deng, H. Inducing embryonic stem cells to differentiate into pancreatic beta cells by a novel three-step approach with activin A and all-trans retinoic acid. Stem Cells 23, 656, 2005.
29. Latif, Z.A., Noel, J., and Alejandro, R. A simple method of staining fresh and cultured islets. Transplantation 45, 827, 1988.
30. Artner, I., Blanchi, B., Raum, J.C., Guo, M., Kaneko, T., Cordes, S., Sieweke, M., and Stein, R. MafB is required for islet beta cell maturation. Proc Natl Acad Sci USA 104, 3853, 2007.
31. Bauwens, C.L., Peerani, R., Niebruegge, S., Woodhouse, K.A., Kumacheva, E., Husain, M., and Zandstra, P.W. Control of human embryonic stem cell colony and aggregate size heterogeneity influences differentiation trajectories. Stem Cells 26, 2300, 2008.
32. Metrakos, P., Yuan, S., Qi, S.J., Duguid, W.P., and Rosenberg, L. Collagen gel matrix promotes islet cell proliferation. Transplant Proc 26, 3349, 1994.
33. Yuan, S., Rosenberg, L., Paraskevas, S., Agapitos, D., and Duguid, W.P. Transdifferentiation of human islets to pancreatic ductal cells in collagen matrix culture. Differ Res Biol Divers 61, 67, 1996.
34. Nagata, N., Gu, Y., Hori, H., Balamurugan, A.N., Touma, M., Kawakami, Y., Wang, W., Baba, T.T., Satake, A., Nozawa, M., Tabata, Y., and Inoue, K. Evaluation of insulin secretion of isolated rat islets cultured in extracellular matrix. Cell Transplant 10, 447, 2001.
35. Ravi Kurukulasuriya, J.L. Progress towards glucagon receptor antagonist therapy for type 2 diabetes. Expert Opin Ther Pat 15, 1739, 2005.
36. Sjoholm, A. Effects of nicotinamide on clonal rat insulinoma cell proliferation, polyamine content and insulin secretion. Anticancer Res 13, 1283, 1993.
37. Yang, L., Li, S., Hatch, H., Ahrens, K., Cornelius, J.G., Petersen, B.E., and Peck, A.B. In vitro trans-differentiation of adult hepatic stem cells into pancreatic endocrine hormone-producing cells. Proc Natl Acad Sci USA 99, 8078, 2002.
38. Chen, S.S., Revoltella, R.P., Zimmerberg, J., and Margolis, L. Differentiation of rhesus monkey embryonic stem cells in three-dimensional collagen matrix. Methods Mol Biol 330, 431, 2006.
39. Kang, X., Xie, Y., Powell, H.M., James Lee, L., Belury, M.A., Lannutti, J.J., and Kniss, D.A. Adipogenesis of murine embryonic stem cells in a three-dimensional culture system using electrospun polymer scaffolds. Biomaterials 28, 450, 2007.
40. Baharvand, H., Hashemi, S.M., Kazemi Ashtiani, S., and Farrokhi, A. Differentiation of human embryonic stem cells into hepatocytes in 2D and 3D culture systems in vitro. Int J Dev Biol 50, 645, 2006.
41. Teitelman, G., Alpert, S., Polak, J.M., Martinez, A., and Hanahan, D. Precursor cells of mouse endocrine pancreas coexpress insulin, glucagon and the neuronal proteins ty-rosine hydroxylase and neuropeptide Y, but not pancreatic polypeptide. Development 118, 1031, 1993.
42. Kroon, E., Martinson, L.A., Kadoya, K., Bang, A.G., Kelly, O.G., Eliazer, S., Young, H., Richardson, M., Smart, N.G., Cunningham, J., Agulnick, A.D., D'Amour, K.A., Carpenter, M.K., and Baetge, E.E. Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nat Biotechnol 26, 443, 2008.