Substratum-induced differentiation of human pluripotent stem cells reveals the coactivator YAP is a potent regulator of neuronal specification

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 38, 2014, Pages 13805-13810

  Musah, Samira ^a,e   Wrighton, Paul J ^a   Zaltsman, Yefim ^a   Zhong, Xiaofen ^b   Zorn, Stefan ^c   Parlato, Matthew B ^c   Hsiao, Cheston ^c   Palecek, Sean P ^c   Chang, Qiang ^a,b   Murphy, William L ^c,d   Kiessling, Laura L ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c Wisconsin Electric Machines and Power Electronics Consortium   (United States)

^d University of Wisconsin Health   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Biomaterials; Glycosaminoglycans; Mechanotransduction; Neuronal differentiation; YAP TAZ

Indexed keywords

ACTIN; PHOSPHOPROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; YAP1 (YES-ASSOCIATED) PROTEIN, HUMAN;

CELL CULTURE; CELL DIFFERENTIATION; CHEMISTRY; CULTURE TECHNIQUE; CYTOLOGY; EXTRACELLULAR MATRIX; HUMAN; METABOLISM; NERVE CELL; PLURIPOTENT STEM CELL; PROCEDURES; TIME;

ACTINS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELLS, CULTURED; EXTRACELLULAR MATRIX; HUMANS; NEURONS; PHOSPHOPROTEINS; PLURIPOTENT STEM CELLS; TIME FACTORS;

EID: 84907222899     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1415330111     Document Type: Article

References (49)

1. Thomson JA, et al (1998) Embryonic stem cell lines derived from human blastocysts. Science 282 (5391):1145-1147.
2. Takahashi K, et al (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131(5):861-872.
3. Chowdhury F, et al (2010) Material properties of the cell dictate stress-induced spreading and differentiation in embryonic stem cells. Nat Mater 9(1):82-88.
4. Chowdhury F, et al (2010) Soft substrates promote homogeneous self-renewal of embryonic stem cells via downregulating cell-matrix tractions. PLoS ONE 5(12):e15655.
5. Engler AJ, Sen S, Sweeney H.L., Discher D.E. (2006) Matrix elasticity directs stem cell lineage specification. Cell 126(4):677-689.
6. Holst J, et al (2010) Substrate elasticity provides mechanical signals for the expansion of hemopoietic stem and progenitor cells. Nat Biotechnol 28(10):1123-1128.
7. Mammoto T, Ingber D.E. (2010) Mechanical control of tissue and organ development. Development 137(9):1407-1420.
8. Moore SW, Sheetz M.P. (2011) Biophysics of substrate interaction: Influence on neural motility, differentiation, and repair. Dev Neurobiol 71(11):1090-1101.
9. Yang C, Tibbitt MW, Basta L, Anseth K.S. (2014) Mechanical memory and dosing influence stem cell fate. Nat Mater 13(6):645-652.
10. Li J, Han D, Zhao Y-P (2014) Kinetic behaviour of the cells touching substrate: The interfacial stiffness guides cell spreading. Sci Rep 4:3910.
11. Murphy WL, McDevitt TC, Engler A.J. (2014) Materials as stem cell regulators. Nat Mater 13(6):547-557.
12. Neirinckx V, Coste C, Rogister B., Wislet-Gendebien S (2013) Concise review: Adult mesenchymal stem cells, adult neural crest stem cells, and therapy of neurological pathologies: a state of play. Stem Cells Transl Med 2(4):284-296.
13. Krabbe C, Zimmer J, Meyer M. (2005) Neural trans differentiation of mesenchymal stem cells - A critical review. APMIS 113(11-12):831-844.
14. Lu P, Blesch A, Tuszynski M.H. (2004) Induction of bone marrow stromal cells to neurons: Differentiation, trans differentiation, or artifact? J Neurosci Res 77(2):174-191.
15. Musah S, et al (2012) Glycosaminoglycan-binding hydrogels enable mechanical control of human pluripotent stem cell self-renewal. ACS Nano 6(11):10168-10177.
16. Dupont S, et al (2011) Role of YAP/TAZ in mechanotransduction. Nature 474 (7350): 179-183.
17. Lian I, et al (2010) The role of YAP transcription coactivator in regulating stem cell self-renewal and differentiation. Genes Dev 24(11):1106-1118.
18. Roztocil T, Matter-Sadzinski L, Alliod C., Ballivet M, Matter J.M. (1997) NeuroM, a neural helix-loop-helix transcription factor, defines a new transition stage in neu-rogenesis. Development 124(17):3263-3272.
19. Cao X, Pfaff SL, Gage F.H. (2008) YAP regulates neural progenitor cell number via the TEA domain transcription factor. Genes Dev 22(23):3320-3334.
20. Zhang H, Deo M, Thompson R.C., Uhler MD, Turner D.L. (2012) Negative regulation of Yap during neuronal differentiation. Dev Biol 361(1):103-115.
21. Sun Y, et al (2014) Hippo/YAP-mediated rigidity-dependent motor neuron differentiation of human pluripotent stem cells. Nat Mater 13(6):599-604.
22. Gauvin R, Parenteau-Bareil R, Dokmeci M.R., Merryman WD, Khademhosseini A. (2012) Hydrogels and microtechnologies for engineering the cellular microenvironment. Nanobiotechnol 4(3):235-246.
23. Klim JR, Li L, Wrighton P.J., Piekarczyk MS, Kiessling L.L. (2010) A defined glycosami-noglycan-binding substratum for human pluripotent stem cells. Nat Methods 7(12): 989-994.
24. Ludwig TE, et al (2006) Derivation of human embryonic stem cells in defined conditions. Nat Biotechnol 24(2):185-187.
25. Watanabe K, et al (2007) A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat Biotechnol 25(6):681-686.
26. Wang N, Butler JP, Ingber D.E. (1993) Mechanotransduction across the cell surface and through the cytoskeleton. Science 260 (5111):1124-1127.
27. Derda R, et al (2010) High-throughput discovery of synthetic surfaces that support proliferation of pluripotent cells. J Am Chem Soc 132(4):1289-1295.
28. Du ZW, Hu BY, Ayala M, Sauer B., Zhang S.C. (2009) Cre recombination-mediated cassette exchange for building versatile transgenic human embryonic stem cells lines. Stem Cells 27(5):1032-1041.
29. Maxwell DJ, Belle MD, Cheunsuang O, Stewart A., Morris R. (2007) Morphology of inhibitory and excitatory interneurons in superficial laminae of the rat dorsal horn. J Physiol 584(Pt 2):521-533.
30. Liu H, Zhang S.C. (2011) Specification of neuronal and glial subtypes from human pluripotent stem cells. Cell Mol Life Sci 68(24):3995-4008.
31. Johnson MA, Weick JP, Pearce R.A., Zhang S-C (2007) Functional neural development from human embryonic stem cells: Accelerated synaptic activity via astrocyte co-culture. J Neurosci 27(12):3069-3077.
32. Discher DE, Mooney DJ, Zandstra P.W. (2009) Growth factors, matrices, and forces combine and control stem cells. Science 324 (5935):1673-1677.
33. Spector I, Shochet NR, Kashman Y, Groweiss A. (1983) Latrunculins: Novel marine toxins that disrupt microfilament organization in cultured cells. Science 219 (4584):493-495.
34. Guo X, Zhao B. (2013) Integration of mechanical and chemical signals by YAP and TAZ transcription coactivators. Cell Biosci 3(1):33.
35. Fairbanks BD, et al (2009) A versatile synthetic extracellular matrix mimic via thiol-norbornene photo polymerization. Adv Mater 21(48):5005-5010.
36. Lin YT, et al (2012) YAP regulates neuronal differentiation through Sonic hedgehog signaling pathway. Exp Cell Res 318(15):1877-1888.
37. Fernandez-L A, et al. (2009) YAP1 is amplified and up-regulated in hedgehog-associated medulloblastomas and mediates Sonic hedgehog-driven neural precursor proliferation. Genes Dev 23(23):2729-2741.
38. Alarcón C., et al (2009) Nuclear CDKs drive Smad transcriptional activation and turnover in BMP and TGF-beta pathways. Cell 139(4):757-769.
39. Neely MD, et al (2012) DMH1, a highly selective small molecule BMP inhibitor promotes neurogenesis of hiPSCs: Comparison of PAX6 and SOX1 expression during neural induction. ACS Chem Neurosci 3(6):482-491.
40. Surmacz B, et al (2012) Directing differentiation of human embryonic stem cells toward anterior neural ectoderm using small molecules. Stem Cells 30(9):1875-1884.
41. Chambers SM, et al (2009) Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat Biotechnol 27(3):275-280.
42. LaVaute TM, et al (2009) Regulation of neural specification from human embryonic stem cells by BMP and FGF. Stem Cells 27(8):1741-1749.
43. Shimada T, et al (2012) A simplified method to generate serotonergic neurons from mouse embryonic stem and induced pluripotent stem cells. J Neurochem 122(1):81-93.
44. Chambers SM, et al (2012) Combined small-molecule inhibition accelerates developmental timing and converts human pluripotent stem cells into nociceptors. Nat Biotechnol 30(7):715-720.
45. Ma L, et al (2012) Human embryonic stem cell-derived GABA neurons correct locomotion deficits in quinolinic acid-lesioned mice. Cell Stem Cell 10(4):455-464.
46. Liu H, Zhang S.C. (2011) Specification of neuronal and glial subtypes from human pluripotent stem cells. Cell Mol Life Sci 68(24):3995-4008.
47. Zhang Y, et al (2013) Rapid single-step induction of functional neurons from human pluripotent stem cells. Neuron 78(5):785-798.
48. Zhao B, Tumaneng K, Guan K.L. (2011) The Hippo pathway in organ size control, tissue regeneration and stem cell self-renewal. Nat Cell Biol 13(8):877-883.
49. Boggiano JC, Fehon R.G. (2012) Growth control by committee: intercellular junctions, cell polarity, and the cytoskeleton regulate Hippo signaling. Dev Cell 22(4):695-702.