3D matrix microenvironment for targeted differentiation of embryonic stem cells into neural and glial lineages

Biomaterials

Volumn 34, Issue 25, 2013, Pages 5995-6007

  Kothapalli, Chandrasekhar R ^a   Kamm, Roger D ^b  

^a Cleveland State University   (United States)

^b Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

Dopaminergic neurons; Embryonic stem cells; Gel modulus; Motor neurons; Retinoic acid; Sonic hedgehog

Indexed keywords

DOPAMINERGIC NEURONS; EMBRYONIC STEM CELLS; MOTOR NEURONS; RETINOIC ACIDS; SONIC HEDGEHOGS;

BRAIN; COLLAGEN; MOLECULES; NEURODEGENERATIVE DISEASES; OPTIMIZATION; REPAIR; STEM CELLS; STIFFNESS MATRIX; THREE DIMENSIONAL COMPUTER GRAPHICS;

NEURONS;

BETA1 INTEGRIN; COLLAGEN TYPE 1; FIBROBLAST GROWTH FACTOR 8; MATRIGEL; MOLECULAR SCAFFOLD; OCTAMER TRANSCRIPTION FACTOR 4; RETINOIC ACID; SONIC HEDGEHOG PROTEIN;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ARTICLE; ASTROCYTE; CELL COMPOSITION; CELL DIFFERENTIATION; CELL LINEAGE; CELL MIGRATION; CELL REGENERATION; CELL SURVIVAL; CELL TYPE; CONTROLLED STUDY; CYTOARCHITECTURE; DOPAMINERGIC NERVE CELL; EMBRYO; EMBRYOID BODY; EMBRYONIC STEM CELL; EXTRACELLULAR MATRIX; GLIA CELL; HYDROGEL; INTRACELLULAR SIGNALING; MICROENVIRONMENT; MOLECULE; MOTONEURON; MOUSE; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; REGENERATIVE MEDICINE; RIGIDITY; SPINAL MUSCULAR ATROPHY; STEM CELL TRANSPLANTATION; TISSUE ENGINEERING;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; DOPAMINERGIC NEURONS; EMBRYONIC STEM CELLS; HEDGEHOG PROTEINS; MICE; MOTOR NEURONS; NEUROGLIA; NEURONS; TISSUE SCAFFOLDS; TRETINOIN;

ERINACEIDAE; MURINAE;

EID: 84878580558     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2013.04.042     Document Type: Article

References (71)

1. McKay R. Stem cells in the central nervous system. Science 1997, 276:66-71.
2. Schwab M.E. Repairing the injured spinal cord. Science 2002, 295:1029-1031.
3. Cavallucci V., D'Amelio M. Matter of life and death: the pharmacological approaches targeting apoptosis in brain diseases. Curr Pharm Des 2011, 17:215-229.
4. Yiu G., He Z. Glial inhibition of CNS axon regeneration. Nat Rev Neurosci 2006, 7:617-627.
5. McKeon R.J., Schreiber R.C., Rudge J.S., Silver J. Reduction of neurite outgrowth in a model of glial scarring following CNS injury is correlated with the expression of inhibitory molecules on reactive astrocytes. JNeurosci 1991, 11:3398-3411.
6. Popovic N., Brundin P. Therapeutic potential of controlled drug delivery systems in neurodegenerative diseases. Int J Pharm 2006, 314:120-126.
7. Lim S.T., Airavaara M., Harvey B.K. Viral vectors for neurotrophic factor delivery: a gene therapy approach for neurodegenerative diseases of the CNS. Pharmacol Res 2010, 61:14-26.
8. Einstein O., Ben-Hur T. The changing face of neural stem cell therapy in neurologic diseases. Arch Neurol 2008, 65:452-456.
9. Ben-Hur T. Reconstructing neural circuits using transplanted neural stem cells in the injured spinal cord. JClin Invest 2010, 120:3096-3098.
10. Björklund A., Lindvall O. Cell replacement therapies for central nervous system disorders. Nat Neurosci 2000, 3:537-544.
11. Quinn S., Walters W., Vescovi A., Whittemore S. Lineage restriction of neuroepithelial precursor cells from fetal human spinal cord. JNeurosci Res 1999, 57:590-602.
12. Amit M., Carpenter M.K., Inokuma M.S., Chiu C.P., Harris C.P., Waknitz M.A., et al. Clonally derived human embryonic stem cell lines maintain pluripotency and proliferative potential for prolonged periods of culture. Dev Biol 2000, 227:271-278.
13. Bradley A., Evans M., Kaufman M.H., Robertson E. Formation of germ-line chimaeras from embryo-derived teratocarcinoma cell lines. Nature 1984, 309:255-256.
14. Wiles M.V. Embryonic stem cell differentiation invitro. Methods Enzymol 1993, 225:900-918.
15. Shakesheff K., Cannizzaro S., Langer R. Creating biomimetic microenvironments with synthetic polymer-peptide hybrid molecules. JBiomater Sci Polym Ed 1998, 9:507-518.
16. Willerth S.M. Neural tissue engineering using embryonic and induced pluripotent stem cells. Stem Cell Res Ther 2011, 2:17.
17. Kuai X.L., Gagliardi C., Flaat M., Bunnell B.A. Differentiation of nonhuman primate embryonic stem cells along neural lineages. Differentiation 2009, 77:229-238.
18. Schuldiner M., Yanuka O., Itskovitz-Eldor J., Melton D.A., Benvenisty N. Effects of eight growth factors on the differentiation of cells derived from human embryonic stem cells. Proc Natl Acad Sci USA 2000, 97:11307-11312.
19. Schuldiner M., Eiges R., Eden A., Yanuka O., Itskovitz-Eldor J., Goldstein R.S., et al. Induced neuronal differentiation of human embryonic stem cells. Brain Res 2001, 913:201-205.
20. Willerth S.M., Sakiyama-Elbert S.E. Kientic analysis of neurotrophin-3 mediated differentiation of embryonic stem cells into neurons. Tissue Eng Part A 2009, 15:307-318.
21. Pacherník J., Bryja V., Esner M., Kubala L., Dvorák P., Hampl A. Neural differentiation of pluripotent mouse embryonal carcinoma cells by retinoic acid: inhibitory effect of serum. Physiol Res 2005, 54:115-122.
22. Pacherník J., Esner M., Bryja V., Dvorák P., Hampl A. Neural differentiation of mouse embryonic stem cells grown in monolayer. Reprod Nutr Dev 2002, 42:317-326.
23. Mondragon-Teran P., Lye G.J., Veraitch F.S. Lowering oxygen tension enhances the differentiation of mouse embryonic stem cells into neuronal cells. Biotechnol Prog 2009, 25:1480-1488.
24. O'Shea K.S. Neuronal differentiation of mouse embryonic stem cells: lineage selection and forced differentiation paradigms. Blood Cells Mol Dis 2001, 27:705-712.
25. Zhang S.C., Wernig M., Duncan I.D., Brüstle O., Thomson J.A. Invitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat Biotechnol 2001, 19:1129-1133.
26. Bouhon I.A., Kato H., Chandran S., Allen N.D. Neural differentiation of mouse embryonic stem cells in chemically defined medium. Brain Res Bull 2005, 68:62-75.
27. Lorincz M.T. Optimized neuronal differentiation of murine embryonic stem cells: role of cell density. Methods Mol Biol 2006, 330:55-69.
28. Gratsch T.E., O'Shea K.S. Noggin and neurogenesis in embryonic stem cells. FASEB J 1998, 12:974.
29. Kawasaki H., Mizuseki K., Nishikawa S., Kaneko S., Kuwana Y., Nakanishi S., et al. Induction of midbrain dopaminergic neurons from ES cells by stromal cell-derived inducing activity. Neuron 2000, 28:31-40.
30. Chen E.Y., Wang Y.C., Mintz A., Richards A., Chen C.S., Lu D., et al. Activatedcharcoal composite biomaterial promotes human embryonic stem cell differentiation toward neuronal lineage. JBiomed Mater Res A 2012, 100:2006-2017.
31. Lam H.J., Patel S., Wang A., Chu J., Li S. Invitro regulation of neural differentiation and axon growth by growth factors and bioactive nanofibers. Tissue Eng Part A 2010, 16:2641-2648.
32. Levenberg S., Burdick J.A., Kraehenbuehl T., Langer R. Neurotrophin-induced differentiation of human embryonic stem cells on three-dimensional polymeric scaffolds. Tissue Eng 2005, 11:506-512.
33. Flaim C.J., Chien S., Bhatia S.N. An extracellular matrix microarray for probing cellular differentiation. Nat Methods 2005, 2:119-125.
34. Murray P., Edgar D. The topographical regulation of embryonic stem cell differentiation. Philos Trans R Soc Lond B Biol Sci 2004, 359:1009-1020.
35. Arnaoutova I., Geoge J., Kleinman H.K., Benton G. Basement membrane matrix (BME) has multiple uses with stem cells. Stem Cell Rev 2012, 8:163-169.
36. Holmes T.C., de Lacalle S., Su X., Liu G., Rich A., Zhang S. Extensive neurite outgrowth and active synapse formation on self-assembling peptide scaffolds. Proc Natl Acad Sci USA 2000, 97:6728-6733.
37. Hammond N.A., Kamm R.D. Elastic deformation and failure in protein filament bundles: atomistic simulations and coarse-grained modeling. Biomaterials 2008, 29:3152-3160.
38. Yamamura N., Sudo R., Ikeda M., Tanishita K. Effects of the mechanical properties of collagen gel on the invitro formation of microvessel networks by endothelial cells. Tissue Eng 2007, 13:1443-1453.
39. Wan C.R., Chung S., Kamm R.D. Differentiation of embryonic stem cells into cardiomyocytes in a compliant microfluidic system. Ann Biomed Eng 2011, 39:1840-1847.
40. Bain G., Kitchens D., Yao M., Huettner J.E., Gottlieb D.I. Embryonic stem cells express neuronal properties invitro. Dev Biol 1995, 168:342-357.
41. Chen M.S., Almeida E.A.C., Huovila A.-P.J., Takahashi Y., Shaw L.M., Mercurio A.M., et al. Evidence that distinct states of the integrin α6β1 interact with laminin and an ADAM. JCell Biol 1999, 144:549-561.
42. Hammond N.A., Kamm R.D. Mechanical characterization of self-assembling peptide hydrogels by microindentation. JBiomed Mater Res A 2013, in press.
43. Matei G.A., Thoreson E.L., Pratt J.R., Newell D.B., Burnham N.A. Precision and accuracy of thermal calibration of atomic force microscopy cantilevers. Rev Sci Instrum 2006, 77.
44. Sneddon I.N. The relation between load and penetration in the axisymmetric boussinesq problem for a punch of arbitrary profile. Int J Eng Sci 1965, 3:47-57.
45. Okada Y., Shimazaki T., Sobue G., Okano H. Retinoic-acid-concentration-dependent acquisition of neural cell identity during invitro differentiation of mouse embryonic stem cells. Dev Biol 2004, 275:124-142.
46. Ma W., Tavakoli T., Derby E., Serebryakova Y., Rao M.S., Mattson M.P. Cell-extracellular matrix interactions regulate neural differentiation of human embryonic stem cells. BMC Dev Biol 2008, 8:90.
47. Zhang J.Q., Yu X.B., Ma B.F., Yu W.H., Zhang A.X., Huang G., et al. Neural differentiation of embryonic stem cells induced by conditioned medium from neural stem cell. Neuroreport 2006, 17:981-986.
48. Uemura M., Refaat M.M., Shinoyama M., Hayashi H., Hashimoto N., Takahashi J. Matrigel supports survival and neuronal differentiation of grafted embryonic stem cell-derived neural precursor cells. JNeurosci Res 2010, 88:542-551.
49. Chen S.S., Revoltella R.P., Papini S., Michelini M., Fitzgerald W., Zimmerberg J., et al. Multilineage differentiation of rhesus monkey embryonic stem cells in three-dimensional culture systems. Stem Cells 2003, 21:281-295.
50. Ma W., Fitzgerald W., Liu Q.Y., O'Shaughnessy T.J., Maric D., Lin H.J., et al. CNS stem and progenitor cell differentiation into functional neuronal circuits in three-dimensional collagen gels. Exp Neurol 2004, 190:276-288.
51. Willerth S.M., Arendas K.J., Gottlieb D.I., Sakiyama-Elbert S.E. Optimization of fibrin scaffolds for differentiation of murine embryonic stem cells into neural lineage cells. Biomaterials 2006, 27:5990-6003.
52. Battista S., Guarnieri D., Borselli C., Zeppetelli S., Borzacchiello A., Mayol L., et al. The effect of matrix composition of 3D constructs on embryonic stem cell differentiation. Biomaterials 2005, 26:6194-6207.
53. Soofi S.S., Last J.A., Liliensiek S.J., Nealey P.F., Murphy C.J. The elastic modulus of Matrigel (TM) as determined by atomic force microscopy. JStruct Biol 2009, 167:216-219.
54. Leipzig N.D., Shoichet M.S. The effect of substrate stiffness on adult neural stem cell behavior. Biomaterials 2009, 30:6867-6878.
55. Glaser T., Brüstle O. Retinoic acid induction of ES-cell-derived neurons: the radial glia connection. Trends Neurosci 2005, 28:397-400.
56. Finley M.F., Devata S., Huettner J.E. BMP-4 inhibits neural differentiation of murine embryonic stem cells. JNeurobiol 1999, 40:271-287.
57. Smukler S.R., Runciman S.B., Xu S., van der Kooy D. Embryonic stem cells assume a primitive neural stem cell fate in the absence of extrinsic influences. JCell Biol 2006, 172:79-90.
58. Lin T., Chao C., Saito S.I., Mazur S.J., Murphy M.E., Appella E., et al. p53 induces differentiation of mouse embryonic stem cells by suppressing Nanog expression. Nat Cell Biol 2005, 7:165-171.
59. Maden M. Retinoic acid in the development, regeneration and maintenance of the nervous system. Nat Rev Neurosci 2007, 8:755-765.
60. Bain G., Ray W.J., Yao M., Gottlieb D.I. From embryonal carcinoma cells to neurons: the P19 pathway. Bio Essays 1994, 16:343-348.
61. Edward M.K., McBurney M.W. The concentration of retinoic acid determines the differentiated cell types formed by a teratocarcinoma cell line. Dev Biol 1983, 98:187-191.
62. Clagett-Dame M., McNeill E.M., Muley P.D. Role of all-trans retinoic acid in neurite outgrowth and axonal elongation. JNeurobiol 2006, 66:739-756.
63. Mey J., McCaffery P. Retinoic acid signaling in the nervous system of adult vertebrates. Neuroscientist 2004, 10:409-421.
64. Flanagan L.A., Rabaza L.M., Derzic S., Schwartz P.H., Monuki E.S. Regulation of human neural precursor cells by laminin and integrins. JNeurosci Res 2006, 83:845-856.
65. Czyz J., Wobus A.M. Embryonic stem cell differentiation: the role of extracellular factors. Differentiation 2001, 68:167-174.
66. Lee S.H., Lumelsky N., Studer L., Auerbach J.M., McKay R.D. Efficient generation of midbrain and hindbrain neurons from mouse embryonic stem cells. Nat Biotechnol 2000, 18:675-679.
67. Perrier A.L., Tabar V., Barberi T., Rubio M.E., Bruses J., Topf N., et al. Derivation of midbrain dopamine neurons from human embryonic stem cells. Proc Natl Acad Sci USA 2004, 101:12543-12548.
68. Wu C.Y., Whye D., Mason R.W., Wang W. Efficient differentiation of mouse embryonic stem cells into motor neurons. JVis Exp 2012, 64:e3813.
69. Wichterle H., Peljto M. Differentiation of mouse embryonic stem cells to spinal motor neurons. Curr Protoc Stem Cell Biol 2008, Chapter 1, Unit 1, H.1.1-1H.1.9.
70. Shin S., Dalton S., Stice S.L. Human motor neuron differentiation from human embryonic stem cells. Stem Cells Dev 2005, 14:266-269.
71. Cho M.S., Lee Y.E., Kim J.Y., Chung S., Cho Y.H., Kim D.S., et al. Highly efficient and large-scale generation of functional dopamine neurons from human embryonic stem cells. Proc Natl Acad Sci USA 2008, 105:3392-3397.