Pluripotency factors regulate definitive endoderm specification through eomesodermin

Genes and Development

Volumn 25, Issue 3, 2011, Pages 238-250

  Teo, Adrian Kee Keong ^a,b   Arnold, Sebastian J ^c   Trotter, Matthew W B ^a   Brown, Stephanie ^a   Ang, Lay Teng ^a   Chng, Zhenzhi ^a,b   Robertson, Elizabeth J ^d   Dunn, N Ray ^b   Vallier, Ludovic ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b INSTITUTE OF MEDICAL BIOLOGY   (Singapore)

^c UNIVERSITY OF FREIBURG   (Germany)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Activin Nodal signaling; Definitive endoderm; Eomes; Human embryonic stem cells; Nanog; Pluripotency factors

Indexed keywords

EOMESODERMIN; OCTAMER TRANSCRIPTION FACTOR 4; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; ECTODERM; EMBRYO; EMBRYONIC STEM CELL; ENDODERM; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION INITIATION;

ACTIVINS; ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL LINE; ENDODERM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; HOMEODOMAIN PROTEINS; HUMANS; MICE; NODAL PROTEIN; OCTAMER TRANSCRIPTION FACTOR-3; PLURIPOTENT STEM CELLS; SOXB1 TRANSCRIPTION FACTORS; T-BOX DOMAIN PROTEINS;

MAMMALIA;

EID: 79551592864     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.607311     Document Type: Article

References (45)

1. Arnold SJ, Robertson EJ. 2009. Making a commitment: Cell lineage allocation and axis patterning in the early mouse embryo. Nat Rev Mol Cell Biol 10: 91-103.
2. Arnold SJ, Hofmann UK, Bikoff EK, Robertson EJ. 2008. Pivotal roles for eomesodermin during axis formation, epithelium-to- mesenchyme transition and endoderm specification in the mouse. Development 135: 501-511.
3. Avilion AA, Nicolis SK, Pevny LH, Perez L, Vivian N, Lovell- Badge R. 2003. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev 17: 126-140.
4. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, Zucker JP, Guenther MG, Kumar RM, Murray HL, Jenner RG, et al. 2005. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122: 947-956.
5. Brons IG, Smithers LE, Trotter MW, Rugg-Gunn P, Sun B, Chuva de Sousa Lopes SM, Howlett SK, Clarkson A, Ahrlund-Richter L, Pedersen RA, et al. 2007. Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 448: 191-195.
6. Chew JL, Loh YH, Zhang W, Chen X, Tam WL, Yeap LS, Li P, Ang YS, Lim B, Robson P, et al. 2005. Reciprocal transcriptional regulation of Pou5f1 and Sox2 via the Oct4/Sox2 complex in embryonic stem cells. Mol Cell Biol 25: 6031-6046. (Pubitemid 40946556)
7. Chng Z, Teo A, Pedersen RA, Vallier L. 2010. SIP1 mediates cell-fate decisions between neuroectoderm and mesendoderm in human pluripotent stem cells. Cell Stem Cell 6: 59-70.
8. Conlon FL, Fairclough L, Price BM, Casey ES, Smith JC. 2001. Determinants of T box protein specificity. Development 128: 3749-3758.
9. D'Amour KA, Agulnick AD, Eliazer S, Kelly OG, Kroon E, Baetge EE. 2005. Efficient differentiation of human embryonic stem cells to definitive endoderm. Nat Biotechnol 23: 1534-1541. (Pubitemid 41752931)
10. Davis S, Miura S, Hill C, Mishina Y, Klingensmith J. 2004. BMP receptor IA is required in the mammalian embryo for endodermal morphogenesis and ectodermal patterning. Dev Biol 270: 47-63.
11. Downs KM. 2008. Systematic localization of Oct-3/4 to the gastrulating mouse conceptus suggests manifold roles in mammalian development. Dev Dyn 237: 464-475.
12. Dufort D, Schwartz L, Harpal K, Rossant J. 1998. The transcription factor HNF3b is required in visceral endoderm for normal primitive streak morphogenesis. Development 125: 3015-3025.
13. Greber B, Wu G, Bernemann C, Joo JY, Han DW, Ko K, Tapia N, Sabour D, Sterneckert J, Tesar P, et al. 2010. Conserved and divergent roles of FGF signaling in mouse epiblast stem cells and human embryonic stem cells. Cell Stem Cell 6: 215-226.
14. Hall J, Guo G, Wray J, Eyres I, Nichols J, Grotewold L, Morfopoulou S, Humphreys P, Mansfield W, Walker R, et al. 2009. Oct4 and LIF/Stat3 additively induce Kruppel factors to sustain embryonic stem cell self-renewal. Cell Stem Cell 5: 597-609.
15. Hart AH, Hartley L, Sourris K, Stadler ES, Li R, Stanley EG, Tam PP, Elefanty AG, Robb L. 2002. Mixl1 is required for axial mesendoderm morphogenesis and patterning in the murine embryo. Development 129: 3597-3608.
16. Hart AH, Hartley L, Ibrahim M, Robb L. 2004. Identification, cloning and expression analysis of the pluripotency promoting Nanog genes in mouse and human. Dev Dyn 230: 187-198.
17. Inman GJ, Nicolas FJ, Callahan JF, Harling JD, Gaster LM, Reith AD, Laping NJ, Hill CS. 2002. SB-431542 is a potent and specific inhibitor of transforming growth factor-β superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol Pharmacol 62: 65-74.
18. Izumi N, Era T, Akimaru H, Yasunaga M, Nishikawa S. 2007. Dissecting the molecular hierarchy for mesendoderm differentiation through a combination of embryonic stem cell culture and RNA interference. Stem Cells 25: 1664-1674.
19. Kanai-Azuma M, Kanai Y, Gad JM, Tajima Y, Taya C, Kurohmaru M, Sanai Y, Yonekawa H, Yazaki K, Tam PP, et al. 2002. Depletion of definitive gut endoderm in Sox17-null mutant mice. Development 129: 2367-2379.
20. Lim CY, Tam WL, Zhang J, Ang HS, Jia H, Lipovich L, Ng HH, Wei CL, Sung WK, Robson P, et al. 2008. Sall4 regulates distinct transcription circuitries in different blastocyst-derived stem cell lineages. Cell Stem Cell 3: 543-554.
21. Loh YH, Wu Q, Chew JL, Vega VB, Zhang W, Chen X, Bourque G, George J, Leong B, Liu J, et al. 2006. The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet 38: 431-440.
22. Lunde K, Belting HG, Driever W. 2004. Zebrafish pou5f1/pou2, homolog of mammalian Oct4, functions in the endoderm specification cascade. Curr Biol 14: 48-55.
23. Martello G, Zacchigna L, Inui M, Montagner M, Adorno M, Mamidi A, Morsut L, Soligo S, Tran U, Dupont S, et al. 2007. MicroRNA control of Nodal signalling. Nature 449: 183-188.
24. Mesnard D, Guzman-Ayala M, Constam DB. 2006. Nodal specifies embryonic visceral endoderm and sustains pluripotent cells in the epiblast before overt axial patterning. Development 133: 2497-2505.
25. Morkel M, Huelsken J, Wakamiya M, Ding J, van de Wetering M, Clevers H, Taketo MM, Behringer RR, Shen MM, Birchmeier W. 2003. b-Catenin regulates Cripto- and Wnt3- dependent gene expression programs in mouse axis and mesoderm formation. Development 130: 6283-6294.
26. Nagy A, Gertsenstein M, Vintersten K, Behringer R. 2003. Manipulating the mouse embryo: A laboratory manual (3rd ed.). Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
27. Niwa H, Miyazaki J, Smith AG. 2000. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet 24: 372-376.
28. Niwa H, Ogawa K, Shimosato D, Adachi K. 2009. A parallel circuit of LIF signalling pathways maintains pluripotency of mouse ES cells. Nature 460: 118-122.
29. Picozzi P, Wang F, Cronk K, Ryan K. 2009. Eomesodermin requires transforming growth factor-b/activin signaling and binds Smad2 to activate mesodermal genes. J Biol Chem 284: 2397-2408.
30. Reubinoff BE, Pera MF, Fong CY, Trounson A, Bongso A. 2000. Embryonic stem cell lines from human blastocysts: Somatic differentiation in vitro. Nat Biotechnol 18: 399-404.
31. Rivera-Perez JA, Mallo M, Gendron-Maguire M, Gridley T, Behringer RR. 1995. Goosecoid is not an essential component of the mouse gastrula organizer but is required for craniofacial and rib development. Development 121: 3005-3012.
32. Rosa A, Spagnoli FM, Brivanlou AH. 2009. The miR-430/427/ 302 family controls mesendodermal fate specification via species-specific target selection. Dev Cell 16: 517-527.
33. Russ AP, Wattler S, Colledge WH, Aparicio SA, Carlton MB, Pearce JJ, Barton SC, Surani MA, Ryan K, Nehls MC, et al. 2000. Eomesodermin is required for mouse trophoblast development and mesoderm formation. Nature 404: 95-99.
34. Tesar PJ, Chenoweth JG, Brook FA, Davies TJ, Evans EP, Mack DL, Gardner RL, McKay RD. 2007. New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 448: 196-199.
35. Thiery JP, Sleeman JP. 2006. Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 7: 131-142.
36. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. 1998. Embryonic stem cell lines derived from human blastocysts. Science 282: 1145-1147.
37. Touboul T, Hannan NR, Corbineau S, Martinez A, Martinet C, Branchereau S, Mainot S, Strick-Marchand H, Pedersen R, Di Santo J, et al. 2010. Generation of functional hepatocytes from human embryonic stem cells under chemically defined conditions that recapitulate liver development. Hepatology 51: 1754-1765.
38. Vallier L, Reynolds D, Pedersen RA. 2004. Nodal inhibits differentiation of human embryonic stem cells along the neuroectodermal default pathway. Dev Biol 275: 403-421.
39. Vallier L, Alexander M, Pedersen RA. 2005. Activin/Nodal and FGF pathways cooperate to maintain pluripotency of human embryonic stem cells. J Cell Sci 118: 4495-4509.
40. Vallier L, Mendjan S, Brown S, Chng Z, Teo A, Smithers LE, Trotter MW, Cho CH, Martinez A, Rugg-Gunn P, et al. 2009a. Activin/Nodal signalling maintains pluripotency by controlling Nanog expression. Development 136: 1339-1349.
41. Vallier L, Touboul T, Brown S, Cho C, Bilican B, Alexander M, Cedervall J, Chandran S, Ahrlund-Richter L, Weber A, et al. 2009b. Signaling pathways controlling pluripotency and early cell fate decisions of human induced pluripotent stem cells. Stem Cells 27: 2655-2666.
42. Vallier L, Touboul T, Chng Z, Brimpari M, Hannan N, Millan E, Smithers LE, Trotter M, Rugg-Gunn P, Weber A, et al. 2009c. Early cell fate decisions of human embryonic stem cells and mouse epiblast stemcells are controlled by the same signalling pathways. PLoS ONE 4: e6082. doi: 10.1371/journal.pone.0006082.
43. Vincent SD, Dunn NR, Hayashi S, Norris DP, Robertson EJ. 2003. Cell fate decisions within the mouse organizer are governed by graded Nodal signals. Genes Dev 17: 1646-1662.
44. Xanthos JB, Kofron M, Wylie C, Heasman J. 2001. Maternal VegT is the initiator of a molecular network specifying endoderm in Xenopus laevis. Development 128: 167-180.
45. Xu RH, Sampsell-Barron TL, Gu F, Root S, Peck RM, Pan G, Yu J, Antosiewicz-Bourget J, Tian S, Stewart R, et al. 2008. NANOG is a direct target of TGFb/activin-mediated SMAD signaling in human ESCs. Cell Stem Cell 3: 196-206.