Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-22T14:55:30.680Z Has data issue: false hasContentIssue false

Identification and characterization of POU class V family genes in Japanese red bellied newt, Cynops pyrrhogaster

Published online by Cambridge University Press:  15 August 2019

Shun Hasegawa
Affiliation:
Department of Life Science, Faculty of Science, Rikkyo University, Tokyo 171-8501, Japan
Isseki Nakao
Affiliation:
Department of Life Science, Faculty of Science, Rikkyo University, Tokyo 171-8501, Japan
Yuki Ootani
Affiliation:
Department of Life Science, Faculty of Science, Rikkyo University, Tokyo 171-8501, Japan
Ami Ogawa
Affiliation:
Department of Life Science, Faculty of Science, Rikkyo University, Tokyo 171-8501, Japan
Miku Takano
Affiliation:
Department of Life Science, Faculty of Science, Rikkyo University, Tokyo 171-8501, Japan
Tsutomu Kinoshita*
Affiliation:
Department of Life Science, Faculty of Science, Rikkyo University, Tokyo 171-8501, Japan
*
Address for correspondence: Tsutomu Kinoshita. Department of Life Science, Faculty of Science, Rikkyo University, 3-34-1 Nishi-Ikebukuro, Toshima-ku, Tokyo 171-8501, Japan. Tel: +81 3-3985-2388. Fax: +81 3-3985-3386. E-mail: [email protected]

Summary

Mammalian Pou5f1 encodes the POU family class V (POU-V) transcription factor which is essential for the pluripotency of embryonic cells and germ cells. In vertebrates, various POU-V family genes have been identified and classified into the POU5F1 family or its paralogous POU5F3 family. In this study, we cloned two cDNAs named CpPou5f1 and CpPou5f3, which encode POU-V family proteins of the Japanese red bellied newt Cynops pyrrhogaster. In the predicted amino acid sequence encoded by CpPou5f1, the typical MAGH sequence at the N-terminus and deletion of arginine at the fifth position of POU-homeodomain were recognized, but not in the sequence encoded by CpPou5f3. Phylogenetic analysis using Clustal Omega software indicated that CpPou5f1 and CpPou5f3 are classified into the clade of the POU5F1 and POU5F3 families, respectively. In a real-time polymerase chain reaction (RT-PCR) analysis, the marked gene expression of CpPou5f1 was observed during oogenesis and early development up to the tail-bud stage, whereas weak gene expression of CpPou5f3 was detected only in the early stages of oogenesis and gastrula. In adult organs, CpPou5f1 was expressed only in the ovary, while gene expression of CpPou5f3 was recognized in various organs. A regeneration experiment using larval forelimb revealed that transient gene expression of CpPou5f1 occurred at the time of wound healing, followed by gene activation of CpPou5f3 during the period of blastema formation. These results suggest that CpPou5f1 and CpPou5f3 might play different roles in embryogenesis and limb regeneration.

Type
Research Article
Copyright
© Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bachvarova, RF, Masi, T, Drum, M, Parker, N, Mason, K, Patient, R and Johnson, AD (2004) Gene expression in the axolotl germ line: Axdazl, Axvh, Axoct-4, and Axkit. Dev Dyn 231, 871–80.CrossRefGoogle ScholarPubMed
Brockes, JP (1997) Amphibian limb regeneration: rebuilding a complex structure. Science 276, 81–7.CrossRefGoogle ScholarPubMed
Burgess, S, Reim, G, Chen, W, Hopkins, N and Brand, M (2002) The zebrafish spiel-ohne-grenzen (spg) gene encodes the POU-domain protein Pou2 related to mammalian Oct4 and is essential for formation of the midbrain and hindbrain, and for pre-gastrula morphogenesis. Development 129, 905–16.Google ScholarPubMed
Casco-Robles, MM, Yamada, S, Miura, T and Chiba, C (2010) Simple and efficient transgenesis with I-SceI meganuclease in the newt, Cynops pyrrhogaster . Dev Dyn 239, 3275–84.CrossRefGoogle ScholarPubMed
Chaar, ZY and Tsilfidis, C (2006) Newt opportunities for understanding the dedifferentiation process. Sci World J 6(Suppl 1), 5564.CrossRefGoogle ScholarPubMed
Eguchi, G, Eguchi, Y, Nakamura, K, Yadav, MC, Millan, JL and Tsonis, PA (2011) Regenerative capacity in newts is not altered by repeated regeneration and ageing. Nat Commun 2, 384.CrossRefGoogle Scholar
Frank, D and Harland, RM (1992) Localized expression of a Xenopus POU gene depends on cell-autonomous transcriptional activation and induction-dependent inactivation. Development 115, 439–48.Google ScholarPubMed
Frankenberg, S and Renfree, MB (2013) On the origin of POU5F1. BMC Biol 11, 56.CrossRefGoogle ScholarPubMed
Frankenberg, S, Pask, A and Renfree, MB (2010) The evolution of class V POU domain transcription factors in vertebrates and their characterization in a marsupial. Dev Biol 337, 162–70.CrossRefGoogle Scholar
Frankenberg, SR, Frank, D, Harland, R, Johnson, AD, Nichols, J, Niwa, H, Schöler, HR, Tanaka, E, Wylie, C and Brickman, JM (2014) The POU-er of gene nomenclature. Development 141, 2921–3.CrossRefGoogle ScholarPubMed
Gold, DA, Gates, RD and Jacobs, DK (2014) The early expansion and evolutionary dynamics of POU class genes. Mol Biol Evol 31, 3136–47.CrossRefGoogle ScholarPubMed
Gurdon, JB (1977) Methods for nuclear transplantation in amphibia. Methods Cell Biol 16, 125–39.CrossRefGoogle ScholarPubMed
Hinkley, CS, Martin, JF, Leibham, D and Perry, M (1992) Sequential expression of multiple POU proteins during amphibian early development. Mol Cell Biol 12, 638–49.CrossRefGoogle ScholarPubMed
Kehler, J, Tolkunova, E, Koschorz, B, Pesce, M, Gentile, L, Boiani, M, Lomeli, H, Nagy, A, McLaughlin, KJ, Schöler, HR and Tomilin, A (2004) Oct4 is required for primordial germ cell survival. EMBO Rep 5, 1078–83.CrossRefGoogle ScholarPubMed
Knapp, D, Schulz, H, Rascon, CA, Volkmer, M, Scholz, J, Nacu, E, Le, M, Novozhilov, S, Tazaki, A, Protze, S, Jacob, T, Hubner, N, Habermann, B and Tanaka, EM (2013) Comparative transcriptional profiling of the axolotl limb identifies a tripartite regeneration-specific gene program. PLoS One 8, e61352.CrossRefGoogle ScholarPubMed
Kragl, M, Knapp, D, Nacu, E, Khattak, S, Schnapp, E, Epperlein, HH and Tanaka, EM (2008) Novel insights into the flexibility of cell and positional identity during urodele limb regeneration. Cold Spring Harbor Symp Quant Biol 73, 583–92.CrossRefGoogle ScholarPubMed
Maki, N, Martinson, J, Nishimura, O, Tarui, H, Meller, J, Tsonis, PA and Agata, K (2010) Expression profiles during dedifferentiation in newt lens regeneration revealed by expressed sequence tags. Mol Vis 16, 72–8.Google ScholarPubMed
Morrison, GM and Brickman, JM (2006) Conserved roles for Oct4 homologues in maintaining multipotency during early vertebrate development. Development 133, 2011–22.CrossRefGoogle ScholarPubMed
Nichols, J, Zevnik, B, Anastassiadis, K, Niwa, H, Klewe-Nebenius, D, Chambers, I, Schöler, H and Smith, A (1998) Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95, 379–91.CrossRefGoogle ScholarPubMed
Niwa, H, Miyazaki, J and Smith, AG (2000) Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet 24, 372–6.CrossRefGoogle ScholarPubMed
Okada, Y and Ichikawa, M (1947) Normal table of Triturus pyrrhogaster . Appl J Exp Morphol 3, 16.Google Scholar
Okamoto, K, Okazawa, H, Okuda, A, Sakai, M, Muramatsu, M and Hamada, H (1990) A novel octamer binding transcription factor is differentially expressed in mouse embryonic cells. Cell 60, 461–72.CrossRefGoogle ScholarPubMed
Rosner, MH, Vigano, MA, Ozato, K, Timmons, PM, Poirier, F, Rigby, PW and Staudt, LM (1990) A POU-domain transcription factor in early stem cells and germ cells of the mammalian embryo. Nature 345, 686–92.CrossRefGoogle ScholarPubMed
Sanchez Alvarado, A and Tsonis, PA (2006) Bridging the regeneration gap: genetic insights from diverse animal models. Nat Rev Genet 7, 873–84.CrossRefGoogle ScholarPubMed
Scheer, U, Trendelenburg, MF and Franke, WW (1976) Regulation of transcription of genes of ribosomal RNA during amphibian oogenesis. A biochemical and morphological study. J Cell Biol 69, 465–89.CrossRefGoogle ScholarPubMed
Schöler, HR, Hatzopoulos, AK, Balling, R, Suzuki, N and 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
Schöler, HR, Dressler, GR, Balling, R, Rohdewohld, H and Gruss, P (1990) Oct-4: a germline-specific transcription factor mapping to the mouse t-complex. EMBO J 9, 2185–95.CrossRefGoogle ScholarPubMed
Simon, A and Tanaka, EM (2013) Limb regeneration. Wiley interdisciplinary reviews. Dev Biol 2, 291300.Google Scholar
Takahashi, K and Yamanaka, S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663–76.CrossRefGoogle ScholarPubMed
Takahashi, K, Tanabe, K, Ohnuki, M, Narita, M, Ichisaka, T, Tomoda, K and Yamanaka, S (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861–72.CrossRefGoogle ScholarPubMed
Takeda, H, Matsuzaki, T, Oki, T, Miyagawa, T and Amanuma, H (1994) A novel POU domain gene, zebrafish pou2: expression and roles of two alternatively spliced twin products in early development. Genes Dev 8, 4559.CrossRefGoogle ScholarPubMed
Tapia, N, Reinhardt, P, Duemmler, A, Wu, G, Arauzo-Bravo, MJ, Esch, D, Greber, B, Cojocaru, V, Rascon, CA, Tazaki, A, Kump, K, Voss, R, Tanaka, EM and Schöler, HR (2012) Reprogramming to pluripotency is an ancient trait of vertebrate Oct4 and Pou2 proteins. Nat Commun 3, 1279.CrossRefGoogle ScholarPubMed
Vivien, C, Scerbo, P, Girardot, F, Le Blay, K, Demeneix, BA and Coen, L (2012) Non-viral expression of mouse Oct4, Sox2, and Klf4 transcription factors efficiently reprograms tadpole muscle fibers in vivo . J Biol Chem 287, 7427–35.CrossRefGoogle ScholarPubMed
Watanabe, M, Yasuoka, Y, Mawaribuchi, S, Kuretani, A, Ito, M, Kondo, M, Ochi, H, Ogino, H, Fukui, A, Taira, M and Kinoshita, T (2017) Conservatism and variability of gene expression profiles among homeologous transcription factors in Xenopus laevis . Dev Biol 426, 301–24.CrossRefGoogle ScholarPubMed
Whitfield, T, Heasman, J and Wylie, C (1993) XLPOU-60, a Xenopus POU-domain mRNA, is oocyte-specific from very early stages of oogenesis, and localised to presumptive mesoderm and ectoderm in the blastula. Dev Biol 155, 361–70.CrossRefGoogle ScholarPubMed
Whitfield, TT, Heasman, J and Wylie, CC (1995) Early embryonic expression of XLPOU-60, a Xenopus POU-domain protein. Dev Biol 169, 759–69.CrossRefGoogle ScholarPubMed
Yeom, YI, Fuhrmann, G, Ovitt, CE, Brehm, A, Ohbo, K, Gross, M, Hubner, K and Schöler, HR (1996) Germline regulatory element of Oct-4 specific for the totipotent cycle of embryonal cells. Development 122, 881–94.Google ScholarPubMed