Activin promotes differentiation of cultured mouse trophoblast stem cells towards a labyrinth cell fate

Developmental Biology

Volumn 335, Issue 1, 2009, Pages 120-131

  Natale, David R C ^a   Hemberger, Myriam ^b   Hughes, Martha ^a   Cross, James C ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b BABRAHAM INSTITUTE   (United Kingdom)

Author keywords

Activin; Labyrinth; Mouse; Nodal; Placenta; TGF ; Trophoblast; Trophoblast stem cell

Indexed keywords

ACTIVIN; ACTIVIN RECEPTOR; FIBROBLAST GROWTH FACTOR 4; PROTEIN NODAL; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL FATE; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; FEMALE; GIANT CELL; INNER EAR; MALE; MOUSE; NONHUMAN; PLACENTA; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYNCYTIOTROPHOBLAST; TROPHOBLAST;

EID: 70349786406     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2009.08.022     Document Type: Article

References (55)

1. Anson-Cartwright L., Dawson K., Holmyard D., Fisher S.J., Lazzarini R.A., and Cross J.C. The glial cells missing-1 protein is essential for branching morphogenesis in the chorioallantoic placenta. Nat. Genet. 25 (2000) 311-314
2. Basyuk E., Cross J.C., Corbin J., Nakayama H., Hunter P., Nait-Oumesmar B., and Lazzarini R.A. Murine Gcm1 gene is expressed in a subset of placental trophoblast cells. Dev. Dyn. 214 (1999) 303-311
3. Ben-Haim N., Lu C., Guzman-Ayala M., Pescatore L., Mesnard D., Bischofberger M., Naef F., Robertson E.J., and Constam D.B. The nodal precursor acting via activin receptors induces mesoderm by maintaining a source of its convertases and BMP4. Dev. Cell. 11 (2006) 313-323
4. Chang H., Brown C.W., and Matzuk M.M. Genetic analysis of the mammalian transforming growth factor-beta superfamily. Endocr. Rev. 23 (2002) 787-823
5. Church G.M., and Gilbert W. Genomic sequencing. Proc. Natl. Acad. Sci. U. S. A 81 (1984) 1991-1995
6. Conlon F.L., Lyons K.M., Takaesu N., Barth K.S., Kispert A., Herrmann B., and Robertson E.J. A primary requirement for nodal in the formation and maintenance of the primitive streak in the mouse. Development 120 (1994) 1919-1928
7. Cross J.C., Nakano H., Natale D.R., Simmons D.G., and Watson E.D. Branching morphogenesis during development of placental villi. Differentiation 74 (2006) 393-401
8. de Caestecker M. The transforming growth factor-beta superfamily of receptors. Cytokine Growth Factor Rev. 15 (2004) 1-11
9. Derynck R., and Zhang Y.E. Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 425 (2003) 577-584
10. Dickson M.C., Martin J.S., Cousins F.M., Kulkarni A.B., Karlsson S., and Akhurst R.J. Defective haematopoiesis and vasculogenesis in transforming growth factor-beta 1 knock out mice. Development 121 (1995) 1845-1854
11. Dono R., Scalera L., Pacifico F., Acampora D., Persico M.G., and Simeone A. The murine cripto gene: expression during mesoderm induction and early heart morphogenesis. Development 118 (1993) 1157-1168
12. Dupressoir A., Marceau G., Vernochet C., Benit L., Kanellopoulos C., Sapin V., and Heidmann T. Syncytin-A and syncytin-B, two fusogenic placenta-specific murine envelope genes of retroviral origin conserved in Muridae. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 725-730
13. Erlebacher A., Price K.A., and Glimcher L.H. Maintenance of mouse trophoblast stem cell proliferation by TGF-beta/activin. Dev. Biol. 275 (2004) 158-169
14. Feldman B., Poueymirou W., Papaioannou V.E., DeChiara T.M., and Goldfarb M. Requirement of FGF-4 for postimplantation mouse development. Science 267 (1995) 246-249
15. Gardner R.L., and Johnson M.H. Investigation of early mammalian development using interspecific chimaeras between rat and mouse. Nat. New Biol. 246 (1973) 86-89
16. Gardner R.L., Papaioannou V.E., and Barton S.C. Origin of the ectoplacental cone and secondary giant cells in mouse blastocysts reconstituted from isolated trophoblast and inner cell mass. J. Embryol. Exp. Morphol. 30 (1973) 561-572
17. Goldin S.N., and Papaioannou V.E. Paracrine action of FGF4 during periimplantation development maintains trophectoderm and primitive endoderm. Genesis 36 (2003) 40-47
18. Gotoh N., Manova K., Tanaka S., Murohashi M., Hadari Y., Lee A., Hamada Y., Hiroe T., Ito M., Kurihara T., Nakazato H., Shibuya M., Lax I., Lacy E., and Schlessinger J. The docking protein FRS2alpha is an essential component of multiple fibroblast growth factor responses during early mouse development. Mol. Cell Biol. 25 (2005) 4105-4116
19. Goumans M.J., and Mummery C. Functional analysis of the TGFbeta receptor/Smad pathway through gene ablation in mice. Int. J. Dev. Biol. 44 (2000) 253-265
20. Gritsman K., Zhang J., Cheng S., Heckscher E., Talbot W.S., and Schier A.F. The EGF-CFC protein one-eyed pinhead is essential for nodal signaling. Cell 97 (1999) 121-132
21. Gu Z., Nomura M., Simpson B.B., Lei H., Feijen A., van den Eijnden-van Raaij J., Donahoe P.K., and Li E. The type I activin receptor ActRIB is required for egg cylinder organization and gastrulation in the mouse. Genes Dev. 12 (1998) 844-857
22. Guzman-Ayala M., Ben-Haim N., Beck S., and Constam D.B. Nodal protein processing and fibroblast growth factor 4 synergize to maintain a trophoblast stem cell microenvironment. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 15656-15660
23. Hogan B. Manipulating the Mouse Embryo : A Laboratory Manual (1994), Cold Spring Harbor Laboratory Press, Plainview, N.Y
24. Hughes M., Dobric N., Scott I.C., Su L., Starovic M., St-Pierre B., Egan S.E., Kingdom J.C., and Cross J.C. The Hand1, Stra13 and Gcm1 transcription factors override FGF signaling to promote terminal differentiation of trophoblast stem cells. Dev. Biol. 271 (2004) 26-37
25. Iannaccone P.M., Zhou X., Khokha M., Boucher D., and Kuehn M.R. Insertional mutation of a gene involved in growth regulation of the early mouse embryo. Dev. Dyn. 194 (1992) 198-208
26. Jones R.L., Stoikos C., Findlay J.K., and Salamonsen L.A. TGF-beta superfamily expression and actions in the endometrium and placenta. Reproduction 132 (2006) 217-232
27. Kim J., Wu H.H., Lander A.D., Lyons K.M., Matzuk M.M., and Calof A.L. GDF11 controls the timing of progenitor cell competence in developing retina. Science 308 (2005) 1927-1930
28. Kitisin K., Saha T., Blake T., Golestaneh N., Deng M., Kim C., Tang Y., Shetty K., Mishra B., and Mishra L. Tgf-beta signaling in development. Sci STKE. 2007 (2007) cm1
29. Kumar A., Novoselov V., Celeste A.J., Wolfman N.M., ten Dijke P., and Kuehn M.R. Nodal signaling uses activin and transforming growth factor-beta receptor-regulated Smads. J. Biol. Chem. 276 (2001) 656-661
30. Laping N.J., Grygielko E., Mathur A., Butter S., Bomberger J., Tweed C., Martin W., Fornwald J., Lehr R., Harling J., Gaster L., Callahan J.F., and Olson B.A. Inhibition of transforming growth factor (TGF)-beta1-induced extracellular matrix with a novel inhibitor of the TGF-beta type I receptor kinase activity: SB-431542. Mol. Pharmacol. 62 (2002) 58-64
31. Larsson J., Goumans M.J., Sjostrand L.J., van Rooijen M.A., Ward D., Leveen P., Xu X., ten Dijke P., Mummery C.L., and Karlsson S. Abnormal angiogenesis but intact hematopoietic potential in TGF-beta type I receptor-deficient mice. EMBO J. 20 (2001) 1663-1673
32. Lau A.L., Kumar T.R., Nishimori K., Bonadio J., and Matzuk M.M. Activin betaC and betaE genes are not essential for mouse liver growth, differentiation, and regeneration. Mol. Cell Biol. 20 (2000) 6127-6137
33. Liem Jr. K.F., Tremml G., and Jessell T.M. A role for the roof plate and its resident TGFbeta-related proteins in neuronal patterning in the dorsal spinal cord. Cell 91 (1997) 127-138
34. Ma G.T., Soloveva V., Tzeng S.J., Lowe L.A., Pfendler K.C., Iannaccone P.M., Kuehn M.R., and Linzer D.I. Nodal regulates trophoblast differentiation and placental development. Dev. Biol. 236 (2001) 124-135
35. Ma L., Cantrup R., Varrault A., Colak D., Klenin N., Gotz M., McFarlane S., Journot L., and Schuurmans C. Zac1 functions through TGFbetaII to negatively regulate cell number in the developing retina. Neural. Develop. 2 (2007) 11
36. Mariano J.M., Montuenga L.M., Prentice M.A., Cuttitta F., and Jakowlew S.B. Concurrent and distinct transcription and translation of transforming growth factor-beta type I and type II receptors in rodent embryogenesis. Int. J. Dev. Biol. 42 (1998) 1125-1136
37. Matzuk M.M., Kumar T.R., Vassalli A., Bickenbach J.R., Roop D.R., Jaenisch R., and Bradley A. Functional analysis of activins during mammalian development. Nature 374 (1995) 354-356
38. Muntener M., and Hsu Y.C. Development of trophoblast and placenta of the mouse. A reinvestigation with regard to the in vitro culture of mouse trophoblast and placenta. Acta Anat. (Basel) 98 (1977) 241-252
39. Natale D.R., Starovic M., and Cross J.C. Phenotypic analysis of the mouse placenta. Methods Mol. Med. 121 (2006) 275-293
40. Ogawa K., Saito A., Matsui H., Suzuki H., Ohtsuka S., Shimosato D., Morishita Y., Watabe T., Niwa H., and Miyazono K. Activin-Nodal signaling is involved in propagation of mouse embryonic stem cells. J. Cell Sci. 120 (2007) 55-65
41. Oshima M., Oshima H., and Taketo M.M. TGF-beta receptor type II deficiency results in defects of yolk sac hematopoiesis and vasculogenesis. Dev. Biol. 179 (1996) 297-302
42. Roelen B.A., Lin H.Y., Knezevic V., Freund E., and Mummery C.L. Expression of TGF-beta s and their receptors during implantation and organogenesis of the mouse embryo. Dev. Biol. 166 (1994) 716-728
43. Shen M.M., Wang H., and Leder P. A differential display strategy identifies Cryptic, a novel EGF-related gene expressed in the axial and lateral mesoderm during mouse gastrulation. Development 124 (1997) 429-442
44. Shi Y., and Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113 (2003) 685-700
45. Simmons D.G., and Cross J.C. Determinants of trophoblast lineage and cell subtype specification in the mouse placenta. Dev. Biol. 284 (2005) 12-24
46. Simmons D.G., Fortier A.L., and Cross J.C. Diverse subtypes and developmental origins of trophoblast giant cells in the mouse placenta. Dev. Biol. 304 (2007) 567-578
47. Simmons D.G., Natale D.R., Begay V., Hughes M., Leutz A., and Cross J.C. Early patterning of the chorion leads to the trilaminar trophoblast cell structure in the placental labyrinth. Development 135 (2008) 2083-2091
48. Slager H.G., Lawson K.A., van den Eijnden-van Raaij A.J., de Laat S.W., and Mummery C.L. Differential localization of TGF-beta 2 in mouse preimplantation and early postimplantation development. Dev. Biol. 145 (1991) 205-218
49. Song J., Oh S.P., Schrewe H., Nomura M., Lei H., Okano M., Gridley T., and Li E. The type II activin receptors are essential for egg cylinder growth, gastrulation, and rostral head development in mice. Dev. Biol. 213 (1999) 157-169
50. Tamada H., McMaster M.T., Flanders K.C., Andrews G.K., and Dey S.K. Cell type-specific expression of transforming growth factor-β1 in the mouse uterus during the periimplantation period. Mol. Endocrinol. 4 (1990) 965-972
51. Tanaka S., Kunath T., Hadjantonakis A.K., Nagy A., and Rossant J. Promotion of trophoblast stem cell proliferation by FGF4. Science 282 (1998) 2072-2075
52. Uy G.D., Downs K.M., and Gardner R.L. Inhibition of trophoblast stem cell potential in chorionic ectoderm coincides with occlusion of the ectoplacental cavity in the mouse. Development 129 (2002) 3913-3924
53. Vassalli A., Matzuk M.M., Gardner H.A., Lee K.F., and Jaenisch R. Activin/inhibin beta B subunit gene disruption leads to defects in eyelid development and female reproduction. Genes Dev. 8 (1994) 414-427
54. Watabe T., Nishihara A., Mishima K., Yamashita J., Shimizu K., Miyazawa K., Nishikawa S., and Miyazono K. TGF-beta receptor kinase inhibitor enhances growth and integrity of embryonic stem cell-derived endothelial cells. J. Cell Biol. 163 (2003) 1303-1311
55. Yeo C., and Whitman M. Nodal signals to Smads through Cripto-dependent and Cripto-independent mechanisms. Mol. Cell 7 (2001) 949-957