Skip to main content
Top
Published in: Journal of Assisted Reproduction and Genetics 11/2016

01-11-2016 | Embryo Biology

Differential expression pattern of Twist1 in mouse preimplantation embryos suggests its multiple roles during early development

Authors: Berna Sozen, Suray Pehlivanoglu, Necdet Demir

Published in: Journal of Assisted Reproduction and Genetics | Issue 11/2016

Login to get access

Abstract

Purpose

The purpose of the present study is to understand Twist-related protein 1 (Twist1) spatiotemporal expression patterns and functions during early embryo development.

Methods

We performed whole-mount double immunofluorescence staining and reverse transcription (RT)-PCR analysis of the Twist1 protein and gene throughout the preimplantation development in mice.

Results

We determined that after compaction, the expression of Twist1 becomes developmentally differentiated and targeted in the inner cells of embryos. In blastocysts at E4.5, uniform staining of the inner cell mass was apparent, and it had been gradually translocated to the nucleus of hatched embryonic cells at E4.75. Furthermore, the effect of potential regulators of Twist on its expression level during blastocyst development was also sought. Accordingly, Twist1 expression appeared to be upregulated in both mRNA and protein level following culture of embryos in the presence of high glucose.

Conclusions

Our study revealed the dynamic Twist localization within the early stage of embryo. The results are discussed in terms of potential roles of Twist1 in the processes of lineage segregation, hatching, and implantation in post-compaction embryos and in blastocysts.
Literature
1.
go back to reference Sozen B, Can A, Demir N. Cell fate regulation during preimplantation development: a view of adhesion-linked molecular interactions. Dev Biol. 2014;395:73–83.CrossRefPubMed Sozen B, Can A, Demir N. Cell fate regulation during preimplantation development: a view of adhesion-linked molecular interactions. Dev Biol. 2014;395:73–83.CrossRefPubMed
3.
go back to reference Seshagiri PB, Sen Roy S, Sireesha G, Rao RP. Cellular and molecular regulation of mammalian blastocyst hatching. J Reprod Immunol. 2009;83:79–84.CrossRefPubMed Seshagiri PB, Sen Roy S, Sireesha G, Rao RP. Cellular and molecular regulation of mammalian blastocyst hatching. J Reprod Immunol. 2009;83:79–84.CrossRefPubMed
4.
go back to reference Kane MT, Morgan PM, Coonan C. Peptide growth factors and preimplantation development. Hum Reprod Update. 1997;3:137–57.CrossRefPubMed Kane MT, Morgan PM, Coonan C. Peptide growth factors and preimplantation development. Hum Reprod Update. 1997;3:137–57.CrossRefPubMed
5.
go back to reference Sargent IL, Martin KL, Barlow DH. The use of recombinant growth factors to promote human embryo development in serum-free medium. Hum Reprod. 1998;13 Suppl 4:239–48.CrossRefPubMed Sargent IL, Martin KL, Barlow DH. The use of recombinant growth factors to promote human embryo development in serum-free medium. Hum Reprod. 1998;13 Suppl 4:239–48.CrossRefPubMed
6.
go back to reference Seshagiri PB, Mishra A, Ramesh G, Rao RP. Regulation of peri-attachment embryo development in the golden hamster: role of growth factors. J Reprod Immunol. 2002;53:203–13.CrossRefPubMed Seshagiri PB, Mishra A, Ramesh G, Rao RP. Regulation of peri-attachment embryo development in the golden hamster: role of growth factors. J Reprod Immunol. 2002;53:203–13.CrossRefPubMed
7.
go back to reference Simon C, Gimeno MJ, Mercader A, Frances A, Garcia Velasco J, Remohi J, et al. Cytokines-adhesion molecules-invasive proteinases. The missing paracrine/autocrine link in embryonic implantation? Mol Hum Reprod. 1996;2:405–24.CrossRefPubMed Simon C, Gimeno MJ, Mercader A, Frances A, Garcia Velasco J, Remohi J, et al. Cytokines-adhesion molecules-invasive proteinases. The missing paracrine/autocrine link in embryonic implantation? Mol Hum Reprod. 1996;2:405–24.CrossRefPubMed
9.
go back to reference Simpson P. Maternal-zygotic gene interactions during formation of the dorsoventral pattern in Drosophila embryos. Genetics. 1983;105:615–32.PubMedPubMedCentral Simpson P. Maternal-zygotic gene interactions during formation of the dorsoventral pattern in Drosophila embryos. Genetics. 1983;105:615–32.PubMedPubMedCentral
10.
go back to reference Li Y, Wang W, Yang R, Wang T, Su T, Weng D, Tao T, Li W, Ma D, Wang S. Correlation of TWIST2 up-regulation and epithelial-mesenchymal transition during tumorigenesis and progression of cervical carcinoma. Gynecol Oncol. 2012b 124; 112-118. Li Y, Wang W, Yang R, Wang T, Su T, Weng D, Tao T, Li W, Ma D, Wang S. Correlation of TWIST2 up-regulation and epithelial-mesenchymal transition during tumorigenesis and progression of cervical carcinoma. Gynecol Oncol. 2012b 124; 112-118.
11.
go back to reference Soo K, O’Rourke MP, Khoo PL, Steiner KA, Wong N, Behringer RR, et al. Twist function is required for the morphogenesis of the cephalic neural tube and the differentiation of the cranial neural crest cells in the mouse embryo. Dev Biol. 2002;247:251–70.CrossRefPubMed Soo K, O’Rourke MP, Khoo PL, Steiner KA, Wong N, Behringer RR, et al. Twist function is required for the morphogenesis of the cephalic neural tube and the differentiation of the cranial neural crest cells in the mouse embryo. Dev Biol. 2002;247:251–70.CrossRefPubMed
12.
go back to reference Vincentz JW, Barnes RM, Rodgers R, Firulli BA, Conway SJ, Firulli AB. An absence of Twist1 results in aberrant cardiac neural crest morphogenesis. Dev Biol. 2008;320:131–9.CrossRefPubMedPubMedCentral Vincentz JW, Barnes RM, Rodgers R, Firulli BA, Conway SJ, Firulli AB. An absence of Twist1 results in aberrant cardiac neural crest morphogenesis. Dev Biol. 2008;320:131–9.CrossRefPubMedPubMedCentral
13.
14.
go back to reference Li C, Ren Y, et al. Twist overexpression promoted epithelial-to-mesenchymal transition of human peritoneal mesothelial cells under high glucose. Nephrol Dial Transplant. 2012;27(11):4119–24.CrossRefPubMed Li C, Ren Y, et al. Twist overexpression promoted epithelial-to-mesenchymal transition of human peritoneal mesothelial cells under high glucose. Nephrol Dial Transplant. 2012;27(11):4119–24.CrossRefPubMed
15.
go back to reference Lo HW, Hsu SC, et al. Epidermal growth factor receptor cooperates with signal transducer and activator of transcription 3 to induce epithelial-mesenchymal transition in cancer cells via up-regulation of TWIST gene expression. Cancer Res. 2007;67(19):9066–76.CrossRefPubMedPubMedCentral Lo HW, Hsu SC, et al. Epidermal growth factor receptor cooperates with signal transducer and activator of transcription 3 to induce epithelial-mesenchymal transition in cancer cells via up-regulation of TWIST gene expression. Cancer Res. 2007;67(19):9066–76.CrossRefPubMedPubMedCentral
16.
go back to reference Margetts PJ. Twist: a new player in the epithelial-mesenchymal transition of the peritoneal mesothelial cells. Nephrol Dial Transplant. 2012;27(11):3978–81.CrossRefPubMed Margetts PJ. Twist: a new player in the epithelial-mesenchymal transition of the peritoneal mesothelial cells. Nephrol Dial Transplant. 2012;27(11):3978–81.CrossRefPubMed
17.
go back to reference Ozturk S, Yaba-Ucar A, Sozen B, Mutlu D, Demir N. Superovulation alters embryonic poly(A)-binding protein (Epab) and poly(A)-binding protein, cytoplasmic 1 (Pabpc1) gene expression in mouse oocytes and early embryos. Reprod Fertil Dev. 2014;28(3):375–83.CrossRef Ozturk S, Yaba-Ucar A, Sozen B, Mutlu D, Demir N. Superovulation alters embryonic poly(A)-binding protein (Epab) and poly(A)-binding protein, cytoplasmic 1 (Pabpc1) gene expression in mouse oocytes and early embryos. Reprod Fertil Dev. 2014;28(3):375–83.CrossRef
18.
go back to reference Sozen B, Ozturk S, Yaba A, Demir N. The p38 MAPK signalling pathway is required for glucose metabolism, lineage specification and embryo survival during mouse preimplantation development. Mech Dev. 2015;138 Pt(3):375–98.CrossRef Sozen B, Ozturk S, Yaba A, Demir N. The p38 MAPK signalling pathway is required for glucose metabolism, lineage specification and embryo survival during mouse preimplantation development. Mech Dev. 2015;138 Pt(3):375–98.CrossRef
20.
go back to reference Brunet T, Bouclet A, Ahmadi P, Mitrossilis D, Driquez B, Brunet AC, et al. Evolutionary conservation of early mesoderm specification by mechanotransduction in Bilateria. Nat Commun. 2013;4:2821.CrossRefPubMedPubMedCentral Brunet T, Bouclet A, Ahmadi P, Mitrossilis D, Driquez B, Brunet AC, et al. Evolutionary conservation of early mesoderm specification by mechanotransduction in Bilateria. Nat Commun. 2013;4:2821.CrossRefPubMedPubMedCentral
21.
go back to reference Kang Y, Massague J. Epithelial-mesenchymal transitions: twist in development and metastasis. Cell. 2004;118:277–9.CrossRefPubMed Kang Y, Massague J. Epithelial-mesenchymal transitions: twist in development and metastasis. Cell. 2004;118:277–9.CrossRefPubMed
22.
go back to reference Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, et al. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell. 2004;117:927–39.CrossRefPubMed Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, et al. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell. 2004;117:927–39.CrossRefPubMed
23.
go back to reference Vestweber D, Gossler A, Boller K, Kemler R. Expression and distribution of cell adhesion molecule uvomorulin in mouse preimplantation embryos. Dev Biol. 1987;124:451–6.CrossRefPubMed Vestweber D, Gossler A, Boller K, Kemler R. Expression and distribution of cell adhesion molecule uvomorulin in mouse preimplantation embryos. Dev Biol. 1987;124:451–6.CrossRefPubMed
24.
go back to reference Fuchtbauer EM. Expression of M-twist during postimplantation development of the mouse. Dev Dyn. 1995;204:316–22.CrossRefPubMed Fuchtbauer EM. Expression of M-twist during postimplantation development of the mouse. Dev Dyn. 1995;204:316–22.CrossRefPubMed
25.
go back to reference Wolf C, Thisse C, Stoetzel C, Thisse B, Gerlinger P, Perrin-Schmitt F. The M-twist gene of Mus is expressed in subsets of mesodermal cells and is closely related to the Xenopus X-twi and the Drosophila twist genes. Dev Biol. 1991;143:363–73.CrossRefPubMed Wolf C, Thisse C, Stoetzel C, Thisse B, Gerlinger P, Perrin-Schmitt F. The M-twist gene of Mus is expressed in subsets of mesodermal cells and is closely related to the Xenopus X-twi and the Drosophila twist genes. Dev Biol. 1991;143:363–73.CrossRefPubMed
26.
go back to reference Yamanaka Y, Lanner F, Rossant J. FGF signal-dependent segregation of primitive endoderm and epiblast in the mouse blastocyst. Development. 2010;137:715–24.CrossRefPubMed Yamanaka Y, Lanner F, Rossant J. FGF signal-dependent segregation of primitive endoderm and epiblast in the mouse blastocyst. Development. 2010;137:715–24.CrossRefPubMed
27.
go back to reference Gasperowicz M, Natale DR. Establishing three blastocyst lineages—then what? Biol Reprod. 2011;84:621–30.CrossRefPubMed Gasperowicz M, Natale DR. Establishing three blastocyst lineages—then what? Biol Reprod. 2011;84:621–30.CrossRefPubMed
28.
go back to reference O’Rourke MP, Soo K, Behringer RR, Hui CC, Tam PP. Twist plays an essential role in FGF and SHH signal transduction during mouse limb development. Dev Biol. 2002;248:143–56.CrossRefPubMed O’Rourke MP, Soo K, Behringer RR, Hui CC, Tam PP. Twist plays an essential role in FGF and SHH signal transduction during mouse limb development. Dev Biol. 2002;248:143–56.CrossRefPubMed
29.
go back to reference Zuniga A, Quillet R, Perrin-Schmitt F, Zeller R. Mouse Twist is required for fibroblast growth factor-mediated epithelial-mesenchymal signalling and cell survival during limb morphogenesis. Mech Dev. 2002;114:51–9.CrossRefPubMed Zuniga A, Quillet R, Perrin-Schmitt F, Zeller R. Mouse Twist is required for fibroblast growth factor-mediated epithelial-mesenchymal signalling and cell survival during limb morphogenesis. Mech Dev. 2002;114:51–9.CrossRefPubMed
30.
go back to reference Dadi TD, Li MW, Lloyd KC. Decreased growth factor expression through RNA interference inhibits development of mouse preimplantation embryos. Comp Med. 2009;59:331–8.PubMedPubMedCentral Dadi TD, Li MW, Lloyd KC. Decreased growth factor expression through RNA interference inhibits development of mouse preimplantation embryos. Comp Med. 2009;59:331–8.PubMedPubMedCentral
31.
go back to reference Martin KL, Barlow DH, Sargent IL. Heparin-binding epidermal growth factor significantly improves human blastocyst development and hatching in serum-free medium. Hum Reprod. 1998;13:1645–52.CrossRefPubMed Martin KL, Barlow DH, Sargent IL. Heparin-binding epidermal growth factor significantly improves human blastocyst development and hatching in serum-free medium. Hum Reprod. 1998;13:1645–52.CrossRefPubMed
32.
33.
go back to reference Gardner DK, Leese HJ. The role of glucose and pyruvate transport in regulating nutrient utilization by preimplantation mouse embryos. Development. 1988;104:423–9.PubMed Gardner DK, Leese HJ. The role of glucose and pyruvate transport in regulating nutrient utilization by preimplantation mouse embryos. Development. 1988;104:423–9.PubMed
34.
go back to reference Gardner DK, Pool TB, Lane M. Embryo nutrition and energy metabolism and its relationship to embryo growth, differentiation, and viability. Semin Reprod Med. 2000;18:205–18.CrossRefPubMed Gardner DK, Pool TB, Lane M. Embryo nutrition and energy metabolism and its relationship to embryo growth, differentiation, and viability. Semin Reprod Med. 2000;18:205–18.CrossRefPubMed
35.
go back to reference Pantaleon M, Scott J, Kaye PL. Nutrient sensing by the early mouse embryo: hexosamine biosynthesis and glucose signaling during preimplantation development. Biol Reprod. 2008;78:595–600.CrossRefPubMed Pantaleon M, Scott J, Kaye PL. Nutrient sensing by the early mouse embryo: hexosamine biosynthesis and glucose signaling during preimplantation development. Biol Reprod. 2008;78:595–600.CrossRefPubMed
Metadata
Title
Differential expression pattern of Twist1 in mouse preimplantation embryos suggests its multiple roles during early development
Authors
Berna Sozen
Suray Pehlivanoglu
Necdet Demir
Publication date
01-11-2016
Publisher
Springer US
Published in
Journal of Assisted Reproduction and Genetics / Issue 11/2016
Print ISSN: 1058-0468
Electronic ISSN: 1573-7330
DOI
https://doi.org/10.1007/s10815-016-0794-1

Other articles of this Issue 11/2016

Journal of Assisted Reproduction and Genetics 11/2016 Go to the issue