All-trans retinoic acid and basic fibroblast growth factor synergistically direct pluripotent human embryonic stem cells to extraembryonic lineages

Stem Cell Research

Volumn 10, Issue 2, 2013, Pages 228-240

  Jagtap, Smita ^a   Meganathan, Kesavan ^a   Wagh, Vilas ^a   Natarajan, Karthick ^a   Hescheler, Jürgen ^a   Sachinidis, Agapios ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; RETINOIC ACID; TRANSCRIPTOME;

ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; CELL STRUCTURE; CGA GENE; CONTROLLED STUDY; DDAH2 GENE; DOWN REGULATION; ECTODERM; EMBRYONIC STEM CELL; EPIGENETICS; GENE; GENE EXPRESSION; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; IGFBP3 GENE; KRT7 GENE; NANOG GENE; PLURIPOTENT STEM CELL; POU5F1 GENE; PRIORITY JOURNAL; PROMOTER REGION; SIGNAL TRANSDUCTION; TDGF1 GENE; UPREGULATION;

ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL LINE; CELL LINEAGE; CELL SHAPE; CLUSTER ANALYSIS; DRUG SYNERGISM; ECTODERM; EMBRYONIC STEM CELLS; EXTRAEMBRYONIC MEMBRANES; FIBROBLAST GROWTH FACTOR 2; GENE EXPRESSION REGULATION; HUMANS; MICE; PLURIPOTENT STEM CELLS; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSCRIPTION FACTORS; TRANSCRIPTOME; TRETINOIN; TROPHOBLASTS;

EID: 84872346048     PISSN: 18735061     EISSN: 18767753     Source Type: Journal    
DOI: 10.1016/j.scr.2012.12.002     Document Type: Article

References (76)

1. Amit M., Shariki C., Margulets V., Itskovitz-Eldor J. Feeder layer- and serum-free culture of human embryonic stem cells. Biol. Reprod. 2004, 70:837-845.
2. Ayling L.J., Whitley G.S.J., Aplin J.D., Cartwright J.E. Dimethylarginine dimethylaminohydrolase (DDAH) regulates trophoblast invasion and motility through effects on nitric oxide. Hum. Reprod. 2006, 21:2530-2537.
3. Baharvand H., Mehrjardi N.Z., Hatami M., Kiani S., Rao M., Haghighi M.M. Neural differentiation from human embryonic stem cells in a defined adherent culture condition. Int. J. Dev. Biol. 2007, 51:371-378.
4. Beck S., Le Good J.A., Guzman M., Ben Haim N., Roy K., Beermann F., Constam D.B. Extraembryonic proteases regulate Nodal signalling during gastrulation. Nat. Cell Biol. 2002, 4:981-985.
5. Bel-Vialar S., Itasaki N., Krumlauf R. Initiating Hox gene expression: in the early chick neural tube differential sensitivity to FGF and RA signaling subdivides the HoxB genes in two distinct groups. Development 2002, 129:5103-5115.
6. Cai L.H., Ye Z.H., Zhou B.Y., Mali P., Zhou C.Q., Cheng L.Z. Promoting human embryonic stem cell renewal or differentiation by modulating Wnt signal and culture conditions. Cell Res. 2007, 17:62-72.
7. Collins M.D., Eckhoff C., Weiss R., Resnick E., Nau H., Scott W.J. Differential teratogenesis of all-trans-retinoic acid administered on gestational day 9.5 to SWV and C57BL/6N mice: emphasis on limb dysmorphology. Birth Defects Res. A Clin. Mol. Teratol. 2006, 76:96-106.
8. Das P., Ezashi T., Schulz L.C., Westfall S.D., Livingston K.A., Roberts R.M. Effects of FGF2 and oxygen in the BMP4-driven differentiation of trophoblast from human embryonic stem cells. Stem Cell Res. 2007, 1:61-74.
9. Dennis G., Sherman B.T., Hosack D.A., Yang J., Gao W., Lane H.C., Lempicki R.A. DAVID: database for annotation, visualization, and integrated discovery. Genome Biol. 2003, 4.
10. Dhara S.K., Stice S.L. Neural differentiation of human embryonic stem cells. J. Cell. Biochem. 2008, 105:633-640.
11. Dickson B.J. Molecular mechanisms of axon guidance. Science 2002, 298:1959-1964.
12. Ding J.X., Yang L., Yan Y.T., Chen A., Desai N., Wynshaw-Boris A., Shen M.M. Cripto is required for correct orientation of the anterior-posterior axis in the mouse embryo. Nature 1998, 395:702-707.
13. Dono R., Texido G., Dussel R., Ehmke H., Zeller R. Impaired cerebral cortex development and blood pressure regulation in FGF-2-deficient mice. EMBO J. 1998, 17:4213-4225.
14. Dravid G., Ye Z., Hammond H., Chen G., Pyle A., Donovan P., Yu X., Cheng L. Defining the role of Wnt/beta-catenin signaling in the survival, proliferation, and self-renewal of human embryonic stem cells. Stem Cell. 2005, 23:1489-1501.
15. Dvorak P., Dvorakova D., Koskova S., Vodinska M., Najvirtova M., Krekac D., Hampl A. Expression and potential role of fibroblast growth factor 2 and its receptors in human embryonic stem cells. Stem Cells 2005, 23:1200-1211.
16. Eiselleova L., Matulka K., Kriz V., Kunova M., Schmidtova Z., Neradil J., Tichy B., Dvorakova D., Pospisilova S., Hampl A., Dvorak P. A complex role for FGF-2 in self-renewal, survival, and adhesion of human embryonic stem cells. Stem Cells 2009, 27:1847-1857.
17. Erlebacher A., Price K.A., Glimcher L.H. Maintenance of mouse trophoblast stem cell proliferation by TGF-beta/activin. Dev. Biol. 2004, 275:158-169.
18. Ferri A.L.M., Lin W., Mavromatakis Y.E., Wang J.C., Sasaki H., Whitsett J.A., Ang S.L. Foxa1 and Foxa2 regulate multiple phases of midbrain dopaminergic neuron development in a dosage-dependent manner. Development 2007, 134:2761-2769.
19. Fujikura J., Yamato E., Yonemura S., Hosoda K., Masui S., Nakao K., Miyazaki J., Niwa H. Differentiation of embryonic stem cells is induced by GATA factors. Genes Dev. 2002, 16:784-789.
20. Goldfarb M. Functions of fibroblast growth factors in vertebrate development. Cytokine Growth Factor Rev. 1996, 7:311-325.
21. Golos T.G., Pollastrini L.M., Gerami-Naini B. Human embryonic stem cells as a model for trophoblast differentiation. Semin. Reprod. Med. 2006, 24:314-321.
22. Greber B., Lehrach H., Adjaye J. Fibroblast growth factor 2 modulates transforming growth factor beta signaling in mouse embryonic fibroblasts and human ESCs (hESCs) to support hESC self-renewal. Stem Cells 2007, 25:455-464.
23. Haimovici F., Anderson D.J. Effects of growth-factors and growth factor-extracellular matrix interactions on mouse trophoblast outgrowth in-vitro. Biol. Reprod. 1993, 49:124-130.
24. Hay D.C., Sutherland L., Clark J., Burdon T. Oct-4 knockdown induces similar patterns of endoderm and trophoblast differentiation markers in human and mouse embryonic stem cells. Stem Cells 2004, 22:225-235.
25. Hayashi K., Kobayashi T., Umino T., Goitsuka R., Matsui Y., Kitamura D. SMAD1 signaling is critical for initial commitment of germ cell lineage from mouse epiblast. Mech. Dev. 2002, 118:99-109.
26. Hemberger M. Genetic-epigenetic intersection in trophoblast differentiation implications for extraembryonic tissue function. Epigenetics 2010, 5:24-29.
27. Hendrickx A.G., Hummler H. Teratogenicity of all-trans retinoic acid during early embryonic development in the cynomolgus monkey (Macaca fascicularis). Teratology 1992, 45:65-74.
28. Home P., Ray S., Dutta D., Bronshteyn I., Larson M., Paul S. GATA3 is selectively expressed in the trophectoderm of peri-implantation embryo and directly regulates Cdx2 gene expression. J. Biol. Chem. 2009, 284:28729-28737.
29. Hu B.Y., Weick J.P., Yu J.Y., Ma L.X., Zhang X.Q., Thomson J.A., Zhang S.C. Neural differentiation of human induced pluripotent stem cells follows developmental principles but with variable potency. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:4335-4340.
30. Hyslop L., Stojkovic M., Armstrong L., Walter T., Stojkovic P., Przyborski S., Herbert M., Murdoch A., Strachan T., Lako M. Downregulation of NANOG induces differentiation of human embryonic stem cells to extraembryonic lineages. Stem Cells 2005, 23:1035-1043.
31. Ishida W., Hamamoto T., Kusanagi K., Yagi K., Kawabata M., Takehara K., Sampath T.K., Kato M., Miyazono K. Smad6 is a Smad1/5-induced SMAD inhibitor - characterization of bone morphogenetic protein-responsive element in the mouse Smad6 PROMOTER. J. Biol. Chem. 2000, 275:6075-6079.
32. Jagtap S., Meganathan K., Gaspar J., Wagh V., Winkler J., Hescheler J., Sachinidis A. Cytosine arabinoside induces ectoderm and inhibits mesoderm expression in human embryonic stem cells during multilineage differentiation. Br. J. Pharmacol. 2011, 162:1743-1756.
33. 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.
34. Jetten A.M., Jetten M.E.R., Sherman M.I. Analyses of cell-surface and secreted proteins of primary cultures of mouse extra-embryonic membranes. Dev. Biol. 1979, 70:89-104.
35. Johannesson M., Stahlberg A., Ameri J., Sand F.W., Norrman K., Semb H. FGF4 and retinoic acid direct differentiation of hESCs into PDX1-expressing foregut endoderm in a time- and concentration-dependent manner. PLoS One 2009, 4.
36. Kitisin K., Saha T., Blake T., Golestaneh N., Deng M., Kim C., Tang Y., Shetty K., Mishra B., Mishra L. Tgf-Beta signaling in development. Sci. STKE 2007, cm1.
37. Klug S., Kraft J.C., Wildi E., Merker H.J., Persaud T.V.N., Nau H., Neubert D. Influence of 13-cis and all-trans retinoic acid on rat embryonic-development in vitro - correlation with isomerization and drug transfer to the embryo. Arch. Toxicol. 1989, 63:185-192.
38. Kuckenberg P., Kubaczka C., Schorle H. The role of transcription factor Tcfap2c/TFAP2C in trophectoderm development. Reprod. BioMed. Online 2012, 25:12-20.
39. Levenstein M.E., Ludwig T.E., Xu R.H., Llanas R.A., VanDenHeuvel-Kramer K., Manning D., Thomson J.A. Basic fibroblast growth factor support of human embryonic stem cell self-renewal. Stem Cells 2006, 24:568-574.
40. Li X.J., Du Z.W., Zarnowska E.D., Pankratz M., Hansen L.O., Pearce R.A., Zhang S.C. Specification of motoneurons from human embryonic stem cells. Nat. Biotechnol. 2005, 23:215-221.
41. Ludwig T.E., Bergendahl V., Levenstein M.E., Yu J.Y., Probasco M.D., Thomson J.A. Feeder-independent culture of human embryonic stem cells (vol 3, pg 637, 2006). Nat. Methods 2006, 3:867.
42. Maden M. Retinoic acid in the development, regeneration and maintenance of the nervous system. Nat. Rev. Neurosci. 2007, 8:755-765.
43. Matin M.M., Walsh J.R., Gokhale P.J., Draper J.S., Bahrami A.R., Morton I., Moore H.D., Andrews P.W. Specific knockdown of Oct4 and beta 2-microglobulin expression by RNA interference in human embryonic stem cells and embryonic carcinoma cells. Stem Cells 2004, 22:659-668.
44. Metallo C.M., Ji L., De Pablo J.J., Palecek S.P. Retinoic acid and bone morphogenetic protein signaling synergize to efficiently direct epithelial differentiation of human embryonic stem cells. Stem Cells 2008, 26:372-380.
45. Morris S.M., Tallquist M.D., Rock C.O., Cooper J.A. Dual roles for the Dab2 adaptor protein in embryonic development and kidney transport. EMBO J. 2002, 21:1555-1564.
46. MorrissKay G.M., Sokolova N. Embryonic development and pattern formation. FASEB J. 1996, 10:961-968.
47. Olivera-Martinez I., Storey K.G. Wnt signals provide a timing mechanism for the FGF-retinoid differentiation switch during vertebrate body axis extension. Development 2007, 134:2125-2135.
48. Pankratz M.T., Li X.J., LaVaute T.M., Lyons E.A., Chen X., Zhang S.C. Directed neural differentiation of human embryonic stem cells via an obligated primitive anterior stage. Stem Cells 2007, 25:1511-1520.
49. Pera M.F., Andrade J., Houssami S., Reubinoff B., Trounson A., Stanley E.G., Ward-van Oostwaard D., Mummery C. Regulation of human embryonic stem cell differentiation by BMP-2 and its antagonist noggin. J. Cell Sci. 2004, 117:1269-1280.
50. Pfarrer C., Weise S., Berisha B., Schams D., Leiser R., Hoffmann B., Schuler G. Fibroblast growth factor (FGF)-1, FGF2, FGF7 and FGF receptors are uniformly expressed in trophoblast giant cells during restricted trophoblast invasion in cows. Placenta 2006, 27:758-770.
51. Potta S.P., Liang H., Pfannkuche K., Winkler J., Chen S., Doss M.X., Obernier K., Kamisetti N., Schulz H., Hubner N., Hescheler J., Sachinidis A. Functional characterization and transcriptome analysis of embryonic stem cell-derived contractile smooth muscle cells. Hypertension 2009, 53:196-204.
52. Ralston A., Cox B.J., Nishioka N., Sasaki H., Chea E., Rugg-Gunn P., Guo G.J., Robson P., Draper J.S., Rossant J. Gata3 regulates trophoblast development downstream of Tead4 and in parallel to Cdx2. Development 2010, 137:395-403.
53. Rhinn M., Dolle P. Retinoic acid signalling during development. Development 2012, 139:843-858.
54. Rodriguez T.A., Srinivas S., Clements M.P., Smith J.C., Beddington R.S.P. Induction and migration of the anterior visceral endoderm is regulated by the extra-embryonic ectoderm. Development 2005, 132:2513-2520.
55. Rossant Janet Development of the extraembryonic lineages. Semin. Dev. Biol. 1995, 6:237-247.
56. Russ A.P., Wattler S., Colledge W.H., Aparicio S.A.J.R., Carlton M.B.L., Pearce J.J., Barton S.C., Surani M.A., Ryan K., Nehls M.C., Wilson V., Evans M.J. Eomesodermin is required for mouse trophoblast development and mesoderm formation. Nature 2000, 404:95-99.
57. Savage M.P., Hart C.E., Riley B.B., Sasse J., Olwin B.B., Fallon J.F. Distribution of Fgf-2 suggests it has a role in chick limb bud growth. Dev. Dyn. 1993, 198:159-170.
58. Schulz L.C., Ezashi T., Das P., Westfall S.D., Livingston K.A., Roberts R.M. Human embryonic stem cells as models for trophoblast differentiation. Placenta 2008, 29(Suppl. A):S10-S16.
59. Shi Y.G., Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 2003, 113:685-700.
60. Shim J.H., Kim S.E., Woo D.H., Kim S.K., Oh C.H., Mckay R., Kim J.H. Directed differentiation of human embryonic stem cells towards a pancreatic cell fate. Diabetologia 2007, 50:1228-1238.
61. Shiotsugu J., Katsuyama Y., Arima K., Baxter A., Koide T., Song J., Chandraratna R.A.S., Blumberg B. Multiple points of interaction between retinoic acid and FGF signaling during embryonic axis formation. Development 2004, 131:2653-2667.
62. Storey K.G., Goriely A., Sargent C.M., Brown J.M., Burns H.D., Abud H.M., Heath J.K. Early posterior neural tissue is induced by FGF in the chick embryo. Development 1998, 125:473-484.
63. Takase M., Imamura T., Sampath T.K., Takeda K., Ichijo H., Miyazono K., Kawabata M. Induction of Smad6 mRNA by bone morphogenetic proteins. Biochem. Biophys. Res. Commun. 1998, 244:26-29.
64. Tanaka S., Kunath T., Hadjantonakis A.K., Nagy A., Rossant J. Promotion of trophoblast stem cell proliferation by FGF4. Science 1998, 282:2072-2075.
65. 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.
66. Tomikawa J., Fukatsu K., Tanaka S., Shiota K. DNA methylation-dependent epigenetic regulation of dimethylarginine dimethylaminohydrolase 2 gene in trophoblast cell lineage. J. Biol. Chem. 2006, 281:12163-12169.
67. Tremblay K.D., Dunn N.R., Robertson E.J. Mouse embryos lacking Smad1 signals display defects in extra-embryonic tissues and germ cell formation. Development 2001, 128:3609-3621.
68. Vallier L., Alexander M., Pedersen R.A. Activin/Nodal and FGF pathways cooperate to maintain pluripotency of human embryonic stem cells. J. Cell Sci. 2005, 118:4495-4509.
69. Wigle J., Eisenstat D.D. Homeobox genes in vertebrate forebrain development and disease. Clin. Genet. 2008, 73:212-226.
70. Wu Z., Zhang W., Chen G., Cheng L., Liao J., Jia N., Gao Y., Dai H., Yuan J., Cheng L., Xiao L. Combinatorial signals of activin/nodal and bone morphogenic protein regulate the early lineage segregation of human embryonic stem cells. J. Biol. Chem. 2008, 283:24991-25002.
71. Xu R.H., Chen X., Li D.S., Li R., Addicks G.C., Glennon C., Zwaka T.P., Thomson J.A. BMP4 initiates human embryonic stem cell differentiation to trophoblast. Nat. Biotechnol. 2002, 20:1261-1264.
72. Yan J.L., Tanaka S., Oda M., Makino T., Ohgane J., Shiota K. Retinoic acid promotes differentiation of trophoblast stem cells to a giant cell fate. Dev. Biol. 2001, 235:422-432.
73. Yang D.H., Smith E.R., Roland I.H., Sheng Z.J., He J.Q., Martin W.D., Hamilton T.C., Lambeth J.D., Xu X.X. Disabled-2 is essential for endodermal cell positioning and structure formation during mouse embryogenesis. Dev. Biol. 2002, 251:27-44.
74. Yashiro K., Zhao X.L., Uehara M., Yamashita K., Nishijima M., Nishino J., Saijoh Y., Sakai Y., Hamada H. Regulation of retinoic acid distribution is required for proximodistal patterning and outgrowth of the developing mouse limb. Dev. Cell 2004, 6:411-422.
75. Yu P.Z., Pan G.J., Yu J.Y., Thomson J.A. FGF2 sustains NANOG and switches the outcome of BMP4-induced human embryonic stem cell differentiation. Cell Stem Cell 2011, 8:326-334.
76. Zhuang Y., Gudas L.J. Overexpression of COUP-TF1 in murine embryonic stem cells reduces retinoic acid-associated growth arrest and increases extraembryonic endoderm gene expression. Differentiation 2008, 76:760-771.