Switch enhancers interpret TGF-β and hippo signaling to control cell fate in human embryonic stem cells

Cell Reports

Volumn 5, Issue 6, 2013, Pages 1611-1624

  Beyer, Tobias A ^a   Weiss, Alexander ^a   Khomchuk, Yuliya ^a   Huang, Kui ^a   Ogunjimi, Abiodun A ^a   Varelas, Xaralabos ^a   Wrana, Jeffrey L ^a,b  

^a MOUNT SINAI HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN FOXH1; PROTEIN TAZ; PROTEIN TEAD; PROTEIN YAP; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ARTICLE; CELL DIFFERENTIATION; CELL DISRUPTION; CELL FATE; CELL MATURATION; COMPLEX FORMATION; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; GENE EXPRESSION REGULATION; GENE REPRESSION; GENE SWITCHING; HUMAN; HUMAN CELL; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEOMICS; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GERM LAYERS; HUMANS; OCTAMER TRANSCRIPTION FACTOR-3; PLURIPOTENT STEM CELLS; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA;

EID: 84891012505     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.11.021     Document Type: Article

References (40)

1. Akopian V., Andrews P.W., Beil S., Benvenisty N., Brehm J., Christie M., Ford A., Fox V., Gokhale P.J., Healy L., et al. Comparison of defined culture systems for feeder cell free propagation of human embryonic stem cells. InVitro Cell. Dev. Biol. Anim. 2010, 46:247-258. International Stem Cell Initiative Consortium.
2. Beyer T.A., Narimatsu M., Weiss A., David L., Wrana J.L. The TGFβ superfamily in stem cell biology and early mammalian embryonic development. Biochim. Biophys. Acta 2013, 1830:2268-2279.
3. Boyer L.A., Lee T.I., Cole M.F., Johnstone S.E., Levine S.S., Zucker J.P., Guenther M.G., Kumar R.M., Murray H.L., Jenner R.G., et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 2005, 122:947-956.
4. Brown S., Teo A., Pauklin S., Hannan N., Cho C.H., Lim B., Vardy L., Dunn N.R., Trotter M., Pedersen R., Vallier L. Activin/Nodal signaling controls divergent transcriptional networks in human embryonic stem cells and in endoderm progenitors. Stem Cells 2011, 29:1176-1185.
5. D'Amour K.A., Agulnick A.D., Eliazer S., Kelly O.G., Kroon E., Baetge E.E. Efficient differentiation of human embryonic stem cells to definitive endoderm. Nat. Biotechnol. 2005, 23:1534-1541.
6. Fujii M., Toyoda T., Nakanishi H., Yatabe Y., Sato A., Matsudaira Y., Ito H., Murakami H., Kondo Y., Kondo E., et al. TGF-β synergizes with defects in the Hippo pathway to stimulate human malignant mesothelioma growth. J.Exp. Med. 2012, 209:479-494.
7. 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.
8. Hanna J.H., Saha K., Jaenisch R. Pluripotency and cellular reprogramming: facts, hypotheses, unresolved issues. Cell 2010, 143:508-525.
9. Hoodless P.A., Pye M., Chazaud C., Labbé E., Attisano L., Rossant J., Wrana J.L. FoxH1 (Fast) functions to specify the anterior primitive streak in the mouse. Genes Dev. 2001, 15:1257-1271.
10. Hu G., Wade P.A. NuRD and pluripotency: a complex balancing act. Cell Stem Cell 2012, 10:497-503.
11. James D., Levine A.J., Besser D., Hemmati-Brivanlou A. TGFbeta/activin/nodal signaling is necessary for the maintenance of pluripotency in human embryonic stem cells. Development 2005, 132:1273-1282.
12. Kim S.W., Yoon S.J., Chuong E., Oyolu C., Wills A.E., Gupta R., Baker J. Chromatin and transcriptional signatures for Nodal signaling during endoderm formation in hESCs. Dev. Biol. 2011, 357:492-504.
13. Koontz L.M., Liu-Chittenden Y., Yin F., Zheng Y., Yu J., Huang B., Chen Q., Wu S., Pan D. The Hippo effector Yorkie controls normal tissue growth by antagonizing scalloped-mediated default repression. Dev. Cell 2013, 25:388-401.
14. Kunarso G., Chia N.Y., Jeyakani J., Hwang C., Lu X., Chan Y.S., Ng H.H., Bourque G. Transposable elements have rewired the core regulatory network of human embryonic stem cells. Nat. Genet. 2010, 42:631-634.
15. Labbé E., Silvestri C., Hoodless P.A., Wrana J.L., Attisano L. Smad2 and Smad3 positively and negatively regulate TGF beta-dependent transcription through the forkhead DNA-binding protein FAST2. Mol. Cell 1998, 2:109-120.
16. Lian I., Kim J., Okazawa H., Zhao J., Zhao B., Yu J., Chinnaiyan A., Israel M.A., Goldstein L.S., Abujarour R., et al. The role of YAP transcription coactivator in regulating stem cell self-renewal and differentiation. Genes Dev. 2010, 24:1106-1118.
17. Liang J., Wan M., Zhang Y., Gu P., Xin H., Jung S.Y., Qin J., Wong J., Cooney A.J., Liu D., Songyang Z. Nanog and Oct4 associate with unique transcriptional repression complexes in embryonic stem cells. Nat. Cell Biol. 2008, 10:731-739.
18. Massagué J., Seoane J., Wotton D. Smad transcription factors. Genes Dev. 2005, 19:2783-2810.
19. McLean C.Y., Bristor D., Hiller M., Clarke S.L., Schaar B.T., Lowe C.B., Wenger A.M., Bejerano G. GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol. 2010, 28:495-501.
20. Mellacheruvu D., Wright Z., Couzens A.L., Lambert J.P., St-Denis N.A., Li T., Miteva Y.V., Hauri S., Sardiu M.E., Low T.Y., et al. The CRAPome: a contaminant repository for affinity purification-mass spectrometry data. Nat. Methods 2013, 10:730-736.
21. Mullen A.C., Orlando D.A., Newman J.J., Lovén J., Kumar R.M., Bilodeau S., Reddy J., Guenther M.G., DeKoter R.P., Young R.A. Mastertranscription factors determine cell-type-specific responses to TGF-β signaling. Cell 2011, 147:565-576.
22. Niwa H., Miyazaki J., Smith A.G. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat. Genet. 2000, 24:372-376.
23. Ogunjimi A.A., Zeqiraj E., Ceccarelli D.F., Sicheri F., Wrana J.L., David L. Structural basis for specificity of TGFβ family receptor small molecule inhibitors. Cell. Signal. 2012, 24:476-483.
24. Oh H., Slattery M., Ma L., Crofts A., White K.P., Mann R.S., Irvine K.D. Genome-wide association of Yorkie with chromatin and chromatin-remodeling complexes. Cell Rep. 2013, 3:309-318.
25. Reynolds N., Latos P., Hynes-Allen A., Loos R., Leaford D., O'Shaughnessy A., Mosaku O., Signolet J., Brennecke P., Kalkan T., et al. NuRD suppresses pluripotency gene expression to promote transcriptional heterogeneity and lineage commitment. Cell Stem Cell 2012, 10:583-594.
26. Silvestri C., Narimatsu M., von Both I., Liu Y., Tan N.B., Izzi L., McCaffery P., Wrana J.L., Attisano L. Genome-wide identification of Smad/Foxh1 targets reveals a role for Foxh1 in retinoic acid regulation and forebrain development. Dev. Cell 2008, 14:411-423.
27. Tam P.P., Loebel D.A. Gene function in mouse embryogenesis: get set for gastrulation. Nat. Rev. Genet. 2007, 8:368-381.
28. Tamm C., Böwer N., Annerén C. Regulation of mouse embryonic stem cell self-renewal by a Yes-YAP-TEAD2 signaling pathway downstream of LIF. J.Cell Sci. 2011, 124:1136-1144.
29. Teo A.K., Arnold S.J., Trotter M.W., Brown S., Ang L.T., Chng Z., Robertson E.J., Dunn N.R., Vallier L. Pluripotency factors regulate definitive endoderm specification through eomesodermin. Genes Dev. 2011, 25:238-250.
30. Thomson J.A., Itskovitz-Eldor J., Shapiro S.S., Waknitz M.A., Swiergiel J.J., Marshall V.S., Jones J.M. Embryonic stem cell lines derived from human blastocysts. Science 1998, 282:1145-1147.
31. Varelas X., Wrana J.L. Coordinating developmental signaling: novel roles for the Hippo pathway. Trends Cell Biol. 2012, 22:88-96.
32. Varelas X., Sakuma R., Samavarchi-Tehrani P., Peerani R., Rao B.M., Dembowy J., Yaffe M.B., Zandstra P.W., Wrana J.L. TAZ controls Smad nucleocytoplasmic shuttling and regulates human embryonic stem-cell self-renewal. Nat. Cell Biol. 2008, 10:837-848.
33. Varelas X., Samavarchi-Tehrani P., Narimatsu M., Weiss A., Cockburn K., Larsen B.G., Rossant J., Wrana J.L. The Crumbs complex couples cell density sensing to Hippo-dependent control of the TGF-β-SMAD pathway. Dev. Cell 2010, 19:831-844.
34. Wang Z., Oron E., Nelson B., Razis S., Ivanova N. Distinct lineage specification roles for NANOG, OCT4, and SOX2 in human embryonic stem cells. Cell Stem Cell 2012, 10:440-454.
35. Weiss A., Attisano L. The TGFbeta superfamily signaling pathway. Wiley Interdiscip. Rev. Dev. Biol. 2013, 2:47-63.
36. Xu C., Inokuma M.S., Denham J., Golds K., Kundu P., Gold J.D., Carpenter M.K. Feeder-free growth of undifferentiated human embryonic stem cells. Nat. Biotechnol. 2001, 19:971-974.
37. Xu R.H., Sampsell-Barron T.L., Gu F., Root S., Peck R.M., Pan G., Yu J., Antosiewicz-Bourget J., Tian S., Stewart R., Thomson J.A. NANOG is a direct target of TGFbeta/activin-mediated SMAD signaling in human ESCs. Cell Stem Cell 2008, 3:196-206.
38. Yamamoto M., Meno C., Sakai Y., Shiratori H., Mochida K., Ikawa Y., Saijoh Y., Hamada H. The transcription factor FoxH1 (FAST) mediates Nodal signaling during anterior-posterior patterning and node formation in the mouse. Genes Dev. 2001, 15:1242-1256.
39. Young R.A. Control of the embryonic stem cell state. Cell 2011, 144:940-954.
40. Zhao B., Ye X., Yu J., Li L., Li W., Li S., Yu J., Lin J.D., Wang C.Y., Chinnaiyan A.M., et al. TEAD mediates YAP-dependent gene induction and growth control. Genes Dev. 2008, 22:1962-1971.