Programming pluripotent precursor cells derived from Xenopus embryos to generate specific tissues and organs
Annette Borchers, Tomas Pieler, Annette Borchers, Tomas Pieler
Abstract
Xenopus embryos provide a rich source of pluripotent cells that can be differentiated into functional organs. Since the molecular principles of vertebrate organogenesis appear to be conserved between Xenopus and mammals, this system can provide useful guidelines for the directional manipulation of human embryonic stem cells. Pluripotent Xenopus cells can be easily isolated from the animal pole of blastula stage Xenopus embryos. These so called "animal cap" cells represent prospective ectodermal cells, but give rise to endodermal, mesodermal and neuro-ectodermal derivatives if treated with the appropriate factors. These factors include evolutionary conserved modulators of the key developmental signal transduction pathways that can be supplied either by mRNA microinjection or direct application of recombinant proteins. This relatively simple system has added to our understanding of pancreas, liver, kidney, eye and heart development. In particular, recent studies have used animal cap cells to generate ectopic eyes and hearts, setting the stage for future work aimed at programming pluripotent cells for regenerative medicine.
Figures
References
- Spemann H. Experimentelle Beiträge zu einer Theorie der Entwicklung. Springer; Berlin, Germany: 1936.
- De Robertis E.M. Spemann’s organizer and self-regulation in amphibian embryos. Nat. Rev. Mol. Cell Biol. 2006;7:296–302. doi: 10.1038/nrm1855.
- Nieuwkoop P.D. Pattern Formation in Artificially Activated Ectoderm (Rana Pipiens and Ambystoma Punctatum) Dev. Biol. 1963;7:255–279. doi: 10.1016/0012-1606(63)90122-2.
- Dale L., Slack J.M. Regional specification within the mesoderm of early embryos of Xenopus laevis. Development. 1987;100:279–295.
- Hemmati-Brivanlou A., Melton D.A. A truncated activin receptor inhibits mesoderm induction and formation of axial structures in Xenopus embryos. Nature. 1992;359:609–614. doi: 10.1038/359609a0.
- Lamb T.M., Harland R.M. Fibroblast growth factor is a direct neural inducer, which combined with noggin generates anterior-posterior neural pattern. Development. 1995;121:3627–3636.
- Clements D., Woodland H.R. VegT induces endoderm by a self-limiting mechanism and by changing the competence of cells to respond to TGF-beta signals. Dev. Biol. 2003;258:454–463. doi: 10.1016/S0012-1606(03)00124-6.
- Henry G.L., Melton D.A. Mixer, a homeobox gene required for endoderm development. Science. 1998;281:91–96. doi: 10.1126/science.281.5373.91.
- Horb M.E., Thomsen G.H. A vegetally localized T-box transcription factor in Xenopus eggs specifies mesoderm and endoderm and is essential for embryonic mesoderm formation. Development. 1997;124:1689–1698.
- Asashima M., Ito Y., Chan T., Michiue T., Nakanishi M., Suzuki K., Hitachi K., Okabayashi K., Kondow A., Ariizumi T. In vitro organogenesis from undifferentiated cells in Xenopus. Dev. Dyn. 2009;238:1309–1320. doi: 10.1002/dvdy.21979.
- Fukui Y., Furue M., Myoishi Y., Sato J.D., Okamoto T., Asashima M. Long-term culture of Xenopus presumptive ectoderm in a nutrient-supplemented culture medium. Dev. Growth Differ. 2003;45:499–506. doi: 10.1111/j.1440-169X.2003.00717.x.
- Zaret K.S., Grompe M. Generation and regeneration of cells of the liver and pancreas. Science. 2008;322:1490–1494. doi: 10.1126/science.1161431.
- Moriya N., Komazaki S., Takahashi S., Yokota C., Asashima M. In vitro pancreas formation from Xenopus ectoderm treated with activin and retinoic acid. Dev. Growth Differ. 2000;42:593–602. doi: 10.1046/j.1440-169x.2000.00542.x.
- Chen Y., Jurgens K., Hollemann T., Claussen M., Ramadori G., Pieler T. Cell-autonomous and signal-dependent expression of liver and intestine marker genes in pluripotent precursor cells from Xenopus embryos. Mech. Dev. 2003;120:277–288. doi: 10.1016/S0925-4773(02)00460-4.
- Chen Y., Pan F.C., Brandes N., Afelik S., Solter M., Pieler T. Retinoic acid signaling is essential for pancreas development and promotes endocrine at the expense of exocrine cell differentiation in Xenopus. Dev. Biol. 2004;271:144–160. doi: 10.1016/j.ydbio.2004.03.030.
- Pan F.C., Chen Y., Loeber J., Henningfeld K., Pieler T. I-SceI meganuclease-mediated transgenesis in Xenopus. Dev. Dyn. 2006;235:247–252. doi: 10.1002/dvdy.20608.
- Afelik S., Chen Y., Pieler T. Combined ectopic expression of Pdx1 and Ptf1a/p48 results in the stable conversion of posterior endoderm into endocrine and exocrine pancreatic tissue. Genes Dev. 2006;20:1441–1446. doi: 10.1101/gad.378706.
- Pan F.C., Afelik S., Pieler T. (University of Göttingen, Göttingen, Germany). 2006. Unpublished work.
- Borowiak M., Melton D.A. How to make beta cells? Curr. Opin. Cell Biol. 2009;21:727–732. doi: 10.1016/j.ceb.2009.08.006.
- Mayhew C.N., Wells J.M. Converting human pluripotent stem cells into beta-cells: Recent advances and future challenges. Curr. Opin. Organ. Transplant. 2009;15:54–60.
- Nakanishi M., Hamazaki T.S., Komazaki S., Okochi H., Asashima M. Pancreatic tissue formation from murine embryonic stem cells in vitro. Differentiation. 2007;75:1–11. doi: 10.1111/j.1432-0436.2006.00109.x.
- Brandli A.W. Towards a molecular anatomy of the Xenopus pronephric kidney. Int. J. Dev. Biol. 1999;43:381–395.
- Moriya N., Uchiyama H., Asashima M. Induction of Pronephric Tubules by Activin and Retinoic Acid in Presumptive Ectoderm of Xenopus laevis. Dev. Growth Differ. 1993;35:123–128.
- Heller N., Brandli A.W. Xenopus Pax-2/5/8 orthologues: novel insights into Pax gene evolution and identification of Pax-8 as the earliest marker for otic and pronephric cell lineages. Dev. Genet. 1999;24:208–219. doi: 10.1002/(SICI)1520-6408(1999)24:3/4<208::AID-DVG4>;2-J.
- Osafune K., Nishinakamura R., Komazaki S., Asashima M. In vitro induction of the pronephric duct in Xenopus explants. Dev. Growth Differ. 2002;44:161–167. doi: 10.1046/j.1440-169x.2002.00631.x.
- Eid S.R., Terrettaz A., Nagata K., Brandli A.W. Embryonic expression of Xenopus SGLT-1L, a novel member of the solute carrier family 5 (SLC5), is confined to tubules of the pronephric kidney. Int. J. Dev. Biol. 2002;46:177–184.
- Chan T.C., Ariizumi T., Asashima M. A model system for organ engineering: transplantation of in vitro induced embryonic kidney. Naturwissenschaften. 1999;86:224–227. doi: 10.1007/s001140050602.
- Tetelin S., Jones E.A. Xenopus Wnt11b is identified as a potential pronephric inducer. Dev. Dyn. 239:148–159.
- Afouda B.A., Hoppler S. Xenopus explants as an experimental model system for studying heart development. Trends Cardiovasc. Med. 2009;19:220–226. doi: 10.1016/j.tcm.2010.01.001.
- Warkman A.S., Krieg P.A. Xenopus as a model system for vertebrate heart development. Semin. Cell Dev. Biol. 2007;18:46–53. doi: 10.1016/j.semcdb.2006.11.010.
- Grunz H. Suramin changes the fate of Spemann’s organizer and prevents neural induction in Xenopus laevis. Mech. Dev. 1992;38:133–141. doi: 10.1016/0925-4773(92)90005-5.
- Grunz H. Amphibian embryos as a model system for organ engineering: in vitro induction and rescue of the heart anlage. Int. J. Dev. Biol. 1999;43:361–364.
- Latinkic B.V., Kotecha S., Mohun T.J. Induction of cardiomyocytes by GATA4 in Xenopus ectodermal explants. Development. 2003;130:3865–3876. doi: 10.1242/dev.00599.
- Pandur P., Lasche M., Eisenberg L.M., Kuhl M. Wnt-11 activation of a non-canonical Wnt signalling pathway is required for cardiogenesis. Nature. 2002;418:636–641. doi: 10.1038/nature00921.
- Zhang C., Basta T., Klymkowsky M.W. SOX7 and SOX18 are essential for cardiogenesis in Xenopus. Dev. Dyn. 2005;234:878–891. doi: 10.1002/dvdy.20565.
- Ariizumi T., Komazaki S., Asashima M., Malacinski G.M. Activin treated urodele ectoderm: A model experimental system for cardiogenesis. Int. J. Dev. Biol. 1996;40:715–718.
- Ariizumi T., Kinoshita M., Yokota C., Takano K., Fukuda K., Moriyama N., Malacinski G.M., Asashima M. Amphibian in vitro heart induction: A simple and reliable model for the study of vertebrate cardiac development. Int. J. Dev. Biol. 2003;47:405–410.
- Afouda B.A., Martin J., Liu F., Ciau-Uitz A., Patient R., Hoppler S. GATA transcription factors integrate Wnt signalling during heart development. Development. 2008;135:3185–3190. doi: 10.1242/dev.026443.
- Samuel L.J., Latinkic B.V. Early activation of FGF and nodal pathways mediates cardiac specification independently of Wnt/beta-catenin signaling. PLoS One. 2009;4:e7650. doi: 10.1371/journal.pone.0007650.
- Sedohara A., Komazaki S., Asashima M. In vitro induction and transplantation of eye during early Xenopus development. Dev. Growth Differ. 2003;45:463–471. doi: 10.1111/j.1440-169X.2003.00713.x.
- Lan L., Vitobello A., Bertacchi M., Cremisi F., Vignali R., Andreazzoli M., Demontis G.C., Barsacchi G., Casarosa S. Noggin elicits retinal fate in Xenopus animal cap embryonic stem cells. Stem Cells. 2009;27:2146–2152. doi: 10.1002/stem.167.
- Viczian A.S., Solessio E.C., Lyou Y., Zuber M.E. Generation of functional eyes from pluripotent cells. PLoS Biol. 2009;7:e1000174. doi: 10.1371/journal.pbio.1000174.
- Cartry J., Nichane M., Ribes V., Colas A., Riou J.F., Pieler T., Dolle P., Bellefroid E.J., Umbhauer M. Retinoic acid signalling is required for specification of pronephric cell fate. Dev. Biol. 2006;299:35–51. doi: 10.1016/j.ydbio.2006.06.047.
Source: PubMed