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Establishment of rat embryonic stem-like cells from the morula using a combination of feeder layers

Published online by Cambridge University Press:  01 August 2009

Chiaki Sano ,
Asako Matsumoto ,
Eimei Sato ,
Emiko Fukui ,
Midori Yoshizawa  and
Hiromichi Matsumoto
Chiaki Sano
Affiliation:
Laboratory of Animal Breeding and Reproduction, Division of Animal Science, Faculty of Agriculture, Utsunomiya University, Utsunomiya, Tochigi 321–8505, Japan.
Asako Matsumoto
Affiliation:
Laboratory of Animal Reproduction, Graduate School of Agricultural Science, Tohoku University, Sendai, Miyagi 981–8555, Japan.
Eimei Sato
Affiliation:
Laboratory of Animal Reproduction, Graduate School of Agricultural Science, Tohoku University, Sendai, Miyagi 981–8555, Japan.
Emiko Fukui
Affiliation:
Laboratory of Animal Breeding and Reproduction, Division of Animal Science, Faculty of Agriculture, Utsunomiya University, Utsunomiya, Tochigi 321–8505, Japan.
Midori Yoshizawa
Affiliation:
Laboratory of Animal Breeding and Reproduction, Division of Animal Science, Faculty of Agriculture, Utsunomiya University, Utsunomiya, Tochigi 321–8505, Japan.
Hiromichi Matsumoto*
Affiliation:
Laboratory of Animal Breeding and Reproduction, Division of Animal Science, Faculty of Agriculture, Utsunomiya University, 350 Minemachi, Utsunomiya, Tochigi 321–8505, Japan.
*
All correspondence to: Hiromichi Matsumoto. Laboratory of Animal Breeding and Reproduction, Division of Animal Science, Faculty of Agriculture, Utsunomiya University, 350 Minemachi, Utsunomiya, Tochigi 321–8505, Japan. Telephone: +81 28 649 5432. Fax: +81 28 649 5431. e-mail: matsu@cc.utsunomiya-u.ac.jp
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Summary

Embryonic stem (ES) cells are characterized by pluripotency, in particular the ability to form a germline on injection into blastocysts. Despite numerous attempts, ES cell lines derived from rat embryos have not yet been established. The reason for this is unclear, although certain intrinsic biological differences among species and/or strains have been reported. Herein, using Wistar-Imamichi rats, specific characteristics of preimplantation embryos are described. At the blastocyst stage, Oct4 (also called Pou5f1) was expressed in both the inner cell mass (ICM) and the trophectoderm (TE), whereas expression of Cdx2 was localized to the TE. In contrast, at an earlier stage, expression of Oct4 was detected in all the nuclei in the morula. These stages were examined using a combination of feeder layers (rat embryonic fibroblast [REF] for primary outgrowth and SIM mouse embryo-derived thioguanine- and ouabain-resistant [STO] cells for passaging) to establish rat ES-like cell lines. The rat ES-like cell lines obtained from the morula maintained expression of Oct4 over long-term culture, whereas cell lines derived from blastocysts lost pluripotency during early passage. The morula-derived ES-like cell lines showed Oct4 expression in a long-term culture, even after cryogenic preservation, thawing and EGFP transfection. These results indicate that rat ES-like cell lines with long-term Oct4 expression can be established from the morula of Wistar-Imamichi rats using a combination of feeder layers.

Keywords

Cdx2ES-like cellsMorulaOct4Rat
Type
Research Article
Information
Zygote , Volume 17 , Issue 3 , August 2009 , pp. 229 - 237
Copyright
Copyright © Cambridge University Press 2009

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References

Bradley, A., Evans, M., Kaufman, M.H. & Robertson, E. (1984). Formation of germ-line chimaeras from embryo-derived teratocarcinoma cell lines. Nature 309, 255–6.CrossRefGoogle ScholarPubMed
Brenin, D., Look, J., Bader, M., Hubner, N., Levan, G. & Iannaccone, P. (1997). Rat embryonic stem cells: a progress report. Transplant. Proc. 29, 1761–5.CrossRefGoogle ScholarPubMed
Buehr, M., Nichols, J., Stenhouse, F., Mountford, P., Greenhalgh, C.J., Kantachuvesiri, S., Brooker, G., Mullins, J. & Smith, A.G. (2003). Rapid loss of Oct-4 and pluripotency in cultured rodent blastocysts and derivative cell lines. Biol. Reprod. 68, 222–9.CrossRefGoogle ScholarPubMed
Cauffman, G., Van de Velde, H., Liebaers, I. & Van Steirteghem, A. (2005). Oct-4 mRNA and protein expression during human preimplantation development. Mol. Hum. Reprod. 11, 173–81.CrossRefGoogle ScholarPubMed
Cauffman, G., Liebaers, I., Van Steirteghem, A. & Van de Velde, H. (2006). POU5F1 isoforms show different expression patterns in human embryonic stem cells and preimplantation embryos. Stem Cells 24, 2685–91.CrossRefGoogle ScholarPubMed
Demers, S.P., Yoo, J.G., Lian, L., Therrien, J. & Smith, L.C. (2007). Rat embryonic stem-like (ES-like) cells can contribute to extraembryonic tissues in vivo. Cloning Stem Cells 9, 512–22.CrossRefGoogle ScholarPubMed
Fandrich, F., Lin, X., Chai, G.X., Schulze, M., Ganten, D., Bader, M., Holle, J., Huang, D.S., Parwaresch, R., Zavazava, N. & Binas, B. (2002). Preimplantation-stage stem cells induce long-term allogeneic graft acceptance without supplementary host conditioning. Nat. Med. 8, 171–8.CrossRefGoogle ScholarPubMed
Hogan, B., Beddington, R., Costantini, F. & Lacy, E. (1994). Manipulating the Mouse Embryo. Cold Spring Harbor Laboratory, NY: Cold Spring Harbor Laboratory Press.Google Scholar
Iannaccone, P.M., Taborn, G.U., Garton, R.L., Caplice, M.D. & Brenin, D.R. (1994). Pluripotent embryonic stem cells from the rat are capable of producing chimeras. Dev. Biol. 163, 288–92.CrossRefGoogle ScholarPubMed
Kageyama, S., Fukui, E. & Yoshizawa, M. (2004). Detection of nucleolar organizer regions on chromosomes by flourescence in situ hybridization with human 28S rRNA gene and cloning of 28S rRNA gene in Sika deer. Anim. Sci. J. 75, 111–6.CrossRefGoogle Scholar
Kirchhof, N., Carnwath, J.W., Lemme, E., Anastassiadis, K., Scholer, H. & Niemann, H. (2000). Expression pattern of Oct-4 in preimplantation embryos of different species. Biol. Reprod. 63, 1698–705.CrossRefGoogle ScholarPubMed
Knezevic, V., Poljak, M., Bradamante, Z., Serman, D., Levak-Svajger, B. & Svajger, A. (2005). Yolk sac carcinoma derived from the rat epiblast as a renal isograft. Coll. Antropol. 29, 189–97.Google ScholarPubMed
Li, P., Tong, C., Mehrian-Shai, R., Jia, L., Wu, N., Yan, Y., Maxson, R.E., Schulze, E.N., Song, H., Hsieh, C.L., Pera, M.F., & Ying, Q.L. (2008). Germline competent embryonic stem cells derived from rat blastocysts. Cell 135, 1299–310.CrossRefGoogle ScholarPubMed
Mannello, F. & Tonti, G.A. (2007). Concise review: no breakthroughs for human mesenchymal and embryonic stem cell culture: conditioned medium, feeder layer, or feeder-free; medium with fetal calf serum, human serum, or enriched plasma; serum-free, serum replacement nonconditioned medium, or ad hoc formula? All that glitters is not gold! Stem Cells 25, 1603–9.CrossRefGoogle Scholar
Matsumoto, H. & Sugawara, S. (1998). Effect of phosphate on the second cleavage division of the rat embryo. Hum. Reprod. 13, 398–402.CrossRefGoogle ScholarPubMed
Matsumoto, H., Shoji, N., Sugawara, S., Umezu, M. & Sato, E. (1998a). Microscopic analysis of enzyme activity, mitochondrial distribution and hydrogen peroxide in two-cell rat embryos. J. Reprod. Fertil. 113, 231–8.CrossRefGoogle ScholarPubMed
Matsumoto, H., Shoji, N., Umezu, M. & Sato, E. (1998b). Microtubule and microfilament dynamics in rat embryos during the two-cell block in vitro. J. Exp. Zool. 281, 149–53.3.0.CO;2-O>CrossRefGoogle ScholarPubMed
Matsumoto, H., Jiang, J.Y., Mitani, D. & Sato, E. (2002a). Distribution and gene expression of cytoskeletal proteins in two-cell rat embryos and developmental arrest. J. Exp. Zool. 293, 641–8.CrossRefGoogle ScholarPubMed
Matsumoto, H., Ma, W.G., Daikoku, T., Zhao, X., Paria, B.C., Das, S.K., Trzaskos, J.M. & Dey, S.K. (2002b). Cyclooxygenase-2 differentially directs uterine angiogenesis during implantation in mice. J. Biol. Chem. 277, 29260–7.CrossRefGoogle ScholarPubMed
Matsumoto, H., Daikoku, T., Wang, H., Sato, E. & Dey, S.K. (2004). Differential expression of ezrin/radixin/moesin (ERM) and ERM-associated adhesion molecules in the blastocyst and uterus suggests their functions during implantation. Biol. Reprod. 70, 729–36.CrossRefGoogle ScholarPubMed
Nichols, J., Smith, A. & Buehr, M. (1998a). Rat and mouse epiblasts differ in their capacity to generate extraembryonic endoderm. Reprod. Fertil. Dev. 10, 517–25.CrossRefGoogle ScholarPubMed
Nichols, J., Zevnik, B., Anastassiadis, K., Niwa, H., Klewe-Nebenius, D., Chambers, I., Scholer, H. & Smith, A. (1998b). Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95, 379–91.CrossRefGoogle ScholarPubMed
Okabe, M., Ikawa, M., Kominami, K., Nakanishi, T. & Nishimune, Y. (1997). ‘Green mice’ as a source of ubiquitous green cells. FEBS Lett. 407, 313–9.CrossRefGoogle ScholarPubMed
Prelle, K., Vassiliev, I.M., Vassilieva, S.G., Wolf, E. & Wobus, A.M. (1999). Establishment of pluripotent cell lines from vertebrate species—present status and future prospects. Cells Tissues Organs 165, 220–36.CrossRefGoogle ScholarPubMed
Ruhnke, M., Ungefroren, H., Zehle, G., Bader, M., Kremer, B. & Fandrich, F. (2003). Long-term culture and differentiation of rat embryonic stem cell-like cells into neuronal, glial, endothelial, and hepatic lineages. Stem Cells 21, 428–36.CrossRefGoogle ScholarPubMed
Scholer, H.R., Hatzopoulos, A.K., Balling, R., Suzuki, N. & Gruss, P. (1989). A family of octamer-specific proteins present during mouse embryogenesis: evidence for germline-specific expression of an Oct factor. EMBO J. 8, 2543–50.CrossRefGoogle ScholarPubMed
Schulze, M., Ungefroren, H., Bader, M. & Fandrich, F. (2006). Derivation, maintenance, and characterization of rat embryonic stem cells in vitro. Methods Mol. Biol. 329, 45–58.Google ScholarPubMed
Shinozawa, T., Sugawara, A., Matsumoto, A., Han, Y.J., Tomioka, I., Inai, K., Sasada, H., Kobayashi, E., Matsumoto, H. & Sato, E. (2006). Development of rat tetraploid and chimeric embryos aggregated with diploid cells. Zygote 14, 287–97.CrossRefGoogle ScholarPubMed
Sobis, H., Verstuyf, A. & Vandeputte, M. (1993). Visceral yolk sac-derived tumors. Int. J. Dev. Biol. 37, 155–68.Google ScholarPubMed
Strumpf, D., Mao, C.A., Yamanaka, Y., Ralston, A., Chawengsaksophak, K., Beck, F. & Rossant, J. (2005). Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 132, 2093–102.CrossRefGoogle ScholarPubMed
Tesar, P.J. (2005). Derivation of germ-line-competent embryonic stem cell lines from preblastocyst mouse embryos. Proc. Natl. Acad. Sci. USA 102, 8239–44.CrossRefGoogle ScholarPubMed
Ulloa Ulloa, C.M., Yoshizawa, M., Komoriya, E., Mitsui, A., Nagai, T. & Kikuchi, K. (2008). The blastocyst production rate and incidence of chromosomal abnormalities by developmental stage in in vitro produced porcine embryos. J. Reprod. Dev. 54, 22–9.CrossRefGoogle Scholar
van Eijk, M.J., van Rooijen, M.A., Modina, S., Scesi, L., Folkers, G., van Tol, H.T., Bevers, M.M., Fisher, S.R., Lewin, H.A., Rakacolli, D., Galli, C., de Vaureix, C., Trounson, A.O., Mummery, C.L. & Gandolfi, F. (1999). Molecular cloning, genetic mapping, and developmental expression of bovine POU5F1. Biol. Reprod. 60, 1093–103.CrossRefGoogle ScholarPubMed
Vassilieva, S., Guan, K., Pich, U. & Wobus, A.M. (2000). Establishment of SSEA-1- and Oct-4-expressing rat embryonic stem-like cell lines and effects of cytokines of the IL-6 family on clonal growth. Exp. Cell Res. 258, 361–73.CrossRefGoogle ScholarPubMed