SMAD7 directly converts human embryonic stem cells to telencephalic fate by a default mechanism

Stem Cells

Volumn 31, Issue 1, 2013, Pages 35-47

  Ozair, Mohammad Zeeshan ^a   Noggle, Scott ^a   Warmflash, Aryeh ^a   Krzyspiak, Joanna Ela ^a   Brivanlou, Ali H ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Human embryonic stem cells; MEK; Neural differentiation; Neural induction; TGF

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; SMAD7 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ARTICLE; CELL FATE; DOWN REGULATION; EMBRYONIC STEM CELL; GENE EXPRESSION; HUMAN; HUMAN CELL; NERVE CELL; NERVOUS TISSUE; NONHUMAN; TELENCEPHALON;

BRAIN; CELL LINE; EMBRYONIC STEM CELLS; FIBROBLAST GROWTH FACTORS; HUMANS; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASES; NEUROGENESIS; PLURIPOTENT STEM CELLS; SMAD7 PROTEIN; TELENCEPHALON; TRANSFORMING GROWTH FACTOR BETA;

AMPHIBIA;

EID: 84871535695     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1246     Document Type: Article

References (64)

1. Spemann H, Mangold H. Induction of embryonic primordia by implantation of organizers from a different species. 1923. Int J Dev Biol 2001;45:13-38. (Pubitemid 33730577)
2. Hemmati-Brivanlou A, Melton DA. A truncated activin receptor inhibits mesoderm induction and formation of axial structures in Xenopus embryos. Nature 1992;359:609-614.
3. Hemmati-Brivanlou A, Melton DA. Inhibition of activin receptor signaling promotes neuralization in Xenopus. Cell 1994;77:273-281. (Pubitemid 24138624)
4. Munoz-Sanjuan I, Brivanlou AH. Neural induction, the default model and embryonic stem cells. Nat Rev Neurosci 2002;3:271-280. (Pubitemid 135706606)
5. Poorgholi Belverdi M, Krause C, Guzman A et al. Comprehensive analysis of TGF-beta and BMP receptor interactomes. Eur J Cell Biol 2012;91:287-293.
6. Taylor IW, Wrana JL. SnapShot: The TGFbeta pathway interactome. Cell 2008;133:378 e1.
7. Xu RH, Peck RM, Li DS et al. Basic FGF and suppression of BMP signaling sustain undifferentiated proliferation of human ES cells. Nat Methods 2005;2:185-190. (Pubitemid 41122125)
8. Yu P, Pan G, Yu J et al. FGF2 sustains NANOG and switches the outcome of BMP4-induced human embryonic stem cell differentiation. Cell Stem Cell 2011;8:326-334.
9. Liu A, Niswander LA. Bone morphogenetic protein signalling and vertebrate nervous system development. Nat Rev Neurosci 2005;6:945-954. (Pubitemid 41753088)
10. Levine AJ, Brivanlou AH. Proposal of a model of mammalian neural induction. Dev Biol 2007;308:247-256. (Pubitemid 47223107)
11. Stern CD. Neural induction: 10 years on since the 'default model'. Curr Opin Cell Biol 2006;18:692-697. (Pubitemid 44692471)
12. Camus A, Perea-Gomez A, Moreau A et al. Absence of Nodal signaling promotes precocious neural differentiation in the mouse embryo. Dev Biol 2006;295:743-755. (Pubitemid 43927707)
13. Bachiller D, Klingensmith J, Kemp C et al. The organizer factors Chordin and Noggin are required for mouse forebrain development. Nature 2000;403:658-661. (Pubitemid 30104006)
14. Chambers SM, Fasano CA, Papapetrou EP et al. Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat Biotechnol 2009;27:275-280.
15. Li W, Sun W, Zhang Y et al. Rapid induction and long-term self-renewal of primitive neural precursors from human embryonic stem cells by small molecule inhibitors. Proc Natl Acad Sci USA 2011;108:8299-8304.
16. Smith JR, Vallier L, Lupo G et al. Inhibition of Activin/Nodal signaling promotes specification of human embryonic stem cells into neuroectoderm. Dev Biol 2008;313:107-117. (Pubitemid 350298306)
17. Watanabe K, Kamiya D, Nishiyama A et al. Directed differentiation of telencephalic precursors from embryonic stem cells. Nat Neurosci 2005;8:288-296. (Pubitemid 40300185)
18. Pankratz MT, Li XJ, Lavaute TM et al. Directed neural differentiation of human embryonic stem cells via an obligated primitive anterior stage. Stem Cells 2007;25:1511-1520. (Pubitemid 47106020)
19. Ying QL, Stavridis M, Griffiths D et al. Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat Biotechnol 2003;21:183-186. (Pubitemid 36188218)
20. Casellas R, Brivanlou AH. Xenopus Smad7 inhibits both the activin and BMP pathways and acts as a neural inducer. Dev Biol 1998;198:1-12. (Pubitemid 28272698)
21. Yan X, Z Liu, Y Chen. Regulation of TGF-beta signaling by Smad7. Acta Biochim Biophys Sin 2009;41:263-272.
22. Pogoda HM, Meyer D. Zebrafish Smad7 is regulated by Smad3 and BMP signals. Dev Dyn 2002;224:334-349. (Pubitemid 34700952)
23. Zwijsen A, van Rooijen MA, Goumans MJ et al. Expression of the inhibitory Smad7 in early mouse development and upregulation during embryonic vasculogenesis. Dev Dyn 2000;218:663-670. (Pubitemid 30604918)
24. Zhang L, Huang H, Zhou F et al. RNF12 controls embryonic stem cell fate and morphogenesis in zebrafish embryos by targeting Smad7 for degradation. Mol Cell 2012;46:650-661.
25. Chen Q, Chen H, Zheng D et al. Smad7 is required for the development and function of the heart. J Biol Chem 2009;284:292-300.
26. Li R, Rosendahl A, Brodin G et al. Deletion of exon I of SMAD7 in mice results in altered B cell responses. J Immunol 2006;176:6777-6784. (Pubitemid 43787860)
27. Tojo M, Takebe A, Takahashi S et al. Smad7-deficient mice show growth retardation with reduced viability. J Biochem 2012;151:621-631.
28. Weng Q, Chen Y, Wang H et al. Dual-mode modulation of Smad signaling by Smad-interacting protein Sip1 is required for myelination in the central nervous system. Neuron 2012;73:713-728.
29. Chng Z, Teo A, Pedersen RA et al. SIP1 mediates cell-fate decisions between neuroectoderm and mesendoderm in human pluripotent stem cells. Cell Stem Cell 2010;6:59-70.
30. Greber B, Coulon P, Zhang M et al. FGF signalling inhibits neural induction in human embryonic stem cells. EMBO J 2011;30:4874-4884.
31. Vallier L, Alexander M, Pedersen RA. Activin/Nodal and FGF pathways cooperate to maintain pluripotency of human embryonic stem cells. J Cell Sci 2005;118:4495-4509. (Pubitemid 41556347)
32. James D, Levine AJ, Besser D et al. TGFbeta/activin/nodal signaling is necessary for the maintenance of pluripotency in human embryonic stem cells. Development 2005;132:1273-1282. (Pubitemid 40528787)
33. Rosa A, Spagnoli FM, Brivanlou AH. The miR-430/427/302 family controls mesendodermal fate specification via species-specific target selection. Dev Cell 2009;16:517-527.
34. Watanabe K, Ueno M, Kamiya D et al. A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat Biotechnol 2007;25:681-686. (Pubitemid 46897207)
35. Lacoste A, Berenshteyn F, Brivanlou AH. An efficient and reversible transposable system for gene delivery and lineage-specific differentiation in human embryonic stem cells. Cell Stem Cell 2009;5:332-342.
36. James D, Noggle SA, Swigut T et al. Contribution of human embryonic stem cells to mouse blastocysts. Dev Biol 2006;295:90-102. (Pubitemid 44041334)
37. Suarez-Farinas M, Noggle S, Heke M et al. Comparing independent microarray studies: The case of human embryonic stem cells. BMC Genomics 2005;6:99.
38. Kamiya D, Banno S, Sasai N et al. Intrinsic transition of embryonic stemcell differentiation into neural progenitors. Nature 2011;470:503-509.
39. Hanna JH, Saha K, Jaenisch R. Pluripotency and cellular reprogramming: Facts, hypotheses, unresolved issues. Cell 2010;143:508-525.
40. Vallier L, Mendjan S, Brown S et al. Activin/Nodal signalling maintains pluripotency by controlling Nanog expression. Development 2009;136:1339-1349.
41. Boyer LA, Lee TI, Cole MF et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 2005;122:947-956. (Pubitemid 41345211)
42. Rosa A, Brivanlou AH. A regulatory circuitry comprised of miR-302 and the transcription factors OCT4 and NR2F2 regulates human embryonic stem cell differentiation. EMBO J 2011;30:237-248.
43. Wang Z, Oron E, Nelson B et al. Distinct lineage specification roles for NANOG, OCT4, and SOX2 in human embryonic stem cells. Cell Stem Cell 2012;10:440-454.
44. Tamplin OJ, Kinzel D, Cox BJ et al. Microarray analysis of Foxa2 mutant mouse embryos reveals novel gene expression and inductive roles for the gastrula organizer and its derivatives. BMC Genomics 2008;9:511.
45. Goulding MD, Chalepakis G, Deutsch U et al. Pax-3, a novel murine DNA binding protein expressed during early neurogenesis. EMBO J 1991;10:1135-1147. (Pubitemid 21905575)
46. Chen G, Gulbranson DR, Yu P et al. Thermal stability of FGF protein is a determinant factor in regulating self-renewal, differentiation and reprogramming in human pluripotent stem cells. Stem Cells 2012;30:623-630.
47. LaVaute TM, Yoo YD, Pankratz MT et al. Regulation of neural specification from human embryonic stem cells by BMP and FGF. Stem Cells 2009;27:1741-1749.
48. Stavridis MP, Lunn JS, Collins BJ et al. A discrete period of FGF-induced Erk1/2 signalling is required for vertebrate neural specification. Development 2007;134:2889-2894. (Pubitemid 47386901)
49. Kunath T, Saba-El-Leil MK, Almousailleakh M et al. FGF stimulation of the Erk1/2 signalling cascade triggers transition of pluripotent embryonic stem cells from self-renewal to lineage commitment. Development 2007;134:2895-2902. (Pubitemid 47386902)
50. Sterneckert J, Stehling M, Bernemann C et al. Neural induction intermediates exhibit distinct roles of Fgf signaling. Stem Cells 2010;28:1772-1781.
51. Greber B, Wu G, Bernemann C et al. Conserved and divergent roles of FGF signaling in mouse epiblast stem cells and human embryonic stem cells. Cell Stem Cell 2010;6:215-226.
52. Patani R, Compston A, Puddifoot CA et al. Activin/Nodal inhibition alone accelerates highly efficient neural conversion from human embryonic stem cells and imposes a caudal positional identity. PLoS One 2009;4:e7327.
53. Varelas X, Samavarchi-Tehrani P, Narimatsu M et al. The Crumbs complex couples cell density sensing to Hippo-dependent control of the TGF-beta-SMAD pathway. Dev Cell 2010;19:831-844.
54. Han G, Li AG, Liang YY et al. Smad7-induced beta-catenin degradation alters epidermal appendage development. Dev Cell 2006;11:301-312. (Pubitemid 44283940)
55. Menendez L, Yatskievych TA, Antin PB et al. Wnt signaling and a Smad pathway blockade direct the differentiation of human pluripotent stem cells to multipotent neural crest cells. Proc Natl Acad Sci USA 2011;108:19240-19245.
56. Sato N, Meijer L, Skaltsounis L et al. Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat Med 2004;10:55-63. (Pubitemid 38524699)
57. Eiraku M, Watanabe K, Matsuo-Takasaki M et al. Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals. Cell Stem Cell 2008;3:519-532.
58. Fasano CA, Chambers SM, Lee G et al. Efficient derivation of functional floor plate tissue from human embryonic stem cells. Cell Stem Cell 2010;6:336-347.
59. Stern CD. Neural induction: Old problem, new findings, yet more questions. Development 2005;132:2007-2021. (Pubitemid 40744462)
60. Najm FJ, Zaremba A, Caprariello AV et al. Rapid and robust generation of functional oligodendrocyte progenitor cells from epiblast stem cells. Nat Methods 2011;8:957-962.
61. Greber B, Lehrach H, Adjaye J. Control of early fate decisions in human ES cells by distinct states of TGFbeta pathway activity. Stem Cells Dev 2008;17:1065-1077.
62. Kim H, Lee G, Ganat Y et al. miR-371-3 expression predicts neural differentiation propensity in human pluripotent stem cells. Cell Stem Cell 2011;8:695-706.
63. Chang C, Harland RM. Neural induction requires continued suppression of both Smad1 and Smad2 signals during gastrulation. Development 2007;134:3861-3872. (Pubitemid 350187345)
64. Ying QL, Wray J, Nichols J et al. The ground state of embryonic stem cell self-renewal. Nature 2008;453:519-523. (Pubitemid 351733324)