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Effects of S-adenosylmethionine decarboxylase, polyamines, amino acids, and weak bases (amines and ammonia) on development and ribosomal RNA synthesis in Xenopus embryos

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Abstract

We have been studying control mechanisms of gene expression in early embryogenesis in a South African clawed toad Xenopus laevis, especially during the period of midblastula transition (MBT), or the transition from the phase of active cell division (cleavage stage) to the phase of extensive morphogenesis (post-blastular stages). We first found that ribosomal RNA synthesis is initiated shortly after MBT in Xenopus embryos and those weak bases, such as amines and ammonium ion, selectively inhibit the initiation and subsequent activation of rRNA synthesis. We then found that rapidly labeled heterogeneous mRNA-like RNA is synthesized in embryos at pre-MBT stage. We then performed cloning and expression studies of several genes, such as those for activin receptors, follistatin and aldolases, and then reached the studies of S-adenosylmethionine decarboxylase (SAMDC), a key enzyme in polyamine metabolism. Here, we cloned a Xenopus SAMDC cDNA and performed experiments to overexpress the in vitro-synthesized SAMDC mRNA in Xenopus early embryos, and found that the maternally preset program of apoptosis occurs in cleavage stage embryos, which is executed when embryos reach the stage of MBT. In the present article, we first summarize results on SAMDC and the maternal program of apoptosis, and then describe our studies on small-molecular-weight substances like polyamines, amino acids, and amines in Xenopus embryos. Finally, we summarize our studies on weak bases, especially on ammonium ion, as the specific inhibitor of ribosomal RNA synthesis in Xenopus embryonic cells.

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Abbreviations

MBT:

Midblastula transition

pre-MBT:

pre-Midblastula transition

SAMDC:

S-adenosylmethionine decarboxylase

rDNA:

Ribosomal DNA

ODC:

Ornithine decarboxylase

SAM:

S-adenosylmethionine

dcSAM:

Decarboxylated SAM

ORF:

Open reading frame

EGBG:

Ethylglyoxal bis-(guanylhydrazone)

GVBD:

Germinal vesicle breakdown

tRNA:

Transfer RNA

References

  • Anderson JA, Lewellyn AL, Maller JL (1997) Ionizing radiation induces apoptosis and elevates cyclin A1-Cdk2 activity before but not after the midblastula transition in Xenopus. Mol Biol Cell 8:1195–2206

    CAS  PubMed  Google Scholar 

  • Brown DD, Caston JD (1962) Biochemistry of amphibian development. I. Ribosome and protein synthesis in early development of Rana pipiens. Dev Biol 5:412–434

    Article  CAS  PubMed  Google Scholar 

  • Brown DD, Littna E (1964) RNA synthesis during the development of Xenopus laevis, the African clawed toad. J Mol Biol 8:669–687

    Article  CAS  PubMed  Google Scholar 

  • Dawid IB (1966) Deoxyribonucleic acid in amphibian eggs. J Mol Biol 12:581–599

    Article  Google Scholar 

  • Gurdon JB, Brown DD (1965) Cytoplasmic regulation of RNA synthesis and nucleolar formation in developing embryos of Xenopus laevis. J Mol Biol 12:27–35

    Article  CAS  PubMed  Google Scholar 

  • Heasman J (2006) Patterning the early Xenopus embryo. Development 133:1205–1217

    Article  CAS  PubMed  Google Scholar 

  • Kai M, Higo T, Yokoska J, Kaito C, Kajita E, Fukamachi H, Takayama E, Igarashi K, Shiokawa K (2000) Overexpression of S-adenosylmethionine decarboxylase (SAMDC) activates the maternal program of apoptosis shortly after MBT in Xenopus embryos. Int J Dev Biol 44:507–510

    CAS  PubMed  Google Scholar 

  • Kai M, Kaito C, Fukamachi H, Higo T, Takayama E, Hara H, Ohya Y, Igarashi K, Shiokawa K (2003) Overexpression of S-adenosylmethionine decarboxylase (SAMDC) in Xenopus embryos activates maternal program of apoptosis as a “fail-safe” mechanism of early embryogenesis. Cell Res 13:147–158

    Article  CAS  PubMed  Google Scholar 

  • Kaito C, Kai M, Higo T, Takayama E, Fukamachi H, Sekimizu K, Shiokawa K (2001) Activation of the maternally preset program of apoptosis by microinjection of 5-aza-2′-deoxycytidine and 5-methyl-2′-deoxycytidine-5′-triphosphate in Xenopus laevis embryos. Develop Growth Differ 43:383–390

    Article  CAS  Google Scholar 

  • Kajita E, Wakiyama M, Miura K-I, Mizumoto K, Oka T, Komuro I, Miyata T, Yatsuki H, Hori K, Shiokawa K (2000) Isolation and characterization of Xenopus laevis aldolase B cDNA and expression patterns of aldolase A, B and C genes in adult tissues, oocytes and embryos of Xenopus laevis. Biochim Biophys Acta 1493:101–118

    CAS  PubMed  Google Scholar 

  • Kondo M, Tashiro K, Fujii G, Asano M, Miyoshi R, Yamada R, Muramatsu M, Shiokawa K (1991) Actibin receptor mRNA is expressed early in Xenopus embryogenesis and the level of the expression affects in the body axis formation. Biochem Biophys Res Commun 181:684–690

    Article  CAS  PubMed  Google Scholar 

  • Laskey RA, Gerhart JC, Knowland JS (1973) Inhibitor of ribosomal RNA synthesis in neurula cells by extracts from blastulae of Xenopus laevis. Dev Biol 33:241–248

    Article  CAS  PubMed  Google Scholar 

  • Minoura I, Nakamura H, Tashiro K, Shiokawa K (1995) Stimulation of circus movement by activin, bFGF and TGF-beta 2 in isolated animal cap cells of Xenopus laevis. Mech Dev 49:65–69

    Article  CAS  PubMed  Google Scholar 

  • Nakakura N, Miura T, Yamana K, Ito A, Shiokawa K (1987) Synthesis of heterogeneous mRNA-like RNA and low-molecular-weight RNA before the midblastula transition in embryos of Xenopus laevis. Dev Biol 123:421–429

    Article  CAS  PubMed  Google Scholar 

  • Newport J, Kirschner M (1982) A major developmental transition in early Xenopus embryos: I. Characterization and timing of cellular changes at the midblastula stage. Cell 30:675–686

    Article  CAS  PubMed  Google Scholar 

  • Osborne HB, Duval C, Ghoda L, Omilli F, Bassez T, Coffino P (1991) Expression and post-translational regulation of ornithine decarboxylase during early Xenopus development. Eur J Biochem 202:575–581

    Article  CAS  PubMed  Google Scholar 

  • Pajunen A, Crozat A, Jaenne OA, Ihalainen R, Laitinen PH, Stanley B, Madhubala R, Pegg AE (1988) Structure and regulation of mammalian S-adenosylmethionine decarboxylase. J Biol Chem 263:17040–17049

    CAS  PubMed  Google Scholar 

  • Rosander U, Holm I, Grahn B, Lovtrup-Rein H, Mattsson M, Heby O (1995) Down-regulation of ornithine decarboxylase by an increased degradation of the enzyme during gastrulation of Xenopus laevis. Biochim Biophys Acta 1264:121–128

    PubMed  Google Scholar 

  • Shibata M, Shinga J, Yasuhiko Y, Kai M, Miura K-I, Shimogori T, Kashiwagi K, Igarashi K, Shiokawa K (1998) Overexpression of S-adenosylmethionine decarboxylase (SAMDC) in early Xenopus embryos induces cell dissociation and inhibits transition from the blastula to gastrula stage. Int J Dev Biol 42:675–686

    CAS  PubMed  Google Scholar 

  • Shinga J, Kashiwagi K, Tashiro K, Igarashi K, Shiokawa K (1996) Maternal and zygotic expression of mRNA for S-adenosylmethionine decarboxylase and its relevance to the unique polyamine composition in Xenopus oocytes and embryos. Biochim Biophys Acta 1308:31–40

    PubMed  Google Scholar 

  • Shiokawa K, Yamana K (1965) Demonstration of “polyphosphate” and its possible role in RNA synthesis during early development of Rana japonica embryos. Exp Cell Res 38:180–186

    Article  CAS  PubMed  Google Scholar 

  • Shiokawa K, Yamana K (1966) Effects of 6-azauridine on development and RNA synthesis of Xenopus laevis embryos. Mem Fac Sci Kyushu Univ Ser E (Biol) 4:107–122

    Google Scholar 

  • Shiokawa K, Yamana K (1967a) Pattern of RNA synthesis in isolated cells of Xenopus laevis embryos. Dev Biol 16:368–388

    Article  CAS  PubMed  Google Scholar 

  • Shiokawa K, Yamana K (1967b) Inhibitor of ribosomal RNA synthesis in Xenopus laevis embryos. Dev Biol 16:389–406

    Article  CAS  PubMed  Google Scholar 

  • Shiokawa K, Nada O, Yamana K (1967) RNA synthesis in isolated cells from Xenopus laevis embryos. Nature 213:1027–1028

    Article  CAS  Google Scholar 

  • Shiokawa K, Misumi Y, Yasuda Y, Nishio Y, Kurata S, Sameshima M, Yamana K (1979) Synthesis and transport of various RNA species in developing embryos of Xenopus laevis. Dev Biol 68:503–514

    Article  CAS  PubMed  Google Scholar 

  • Shiokawa K, Misumi Y, Yamana K (1981a) Demonstration of rRNA synthesis in pre-gastrular embryos of Xenopus laevis. Dev Growth Differ 23:579–587

    Article  CAS  Google Scholar 

  • Shiokawa K, Tashiro K, Misumi Y, Yamana K (1981b) Non-coordinated synthesis of RNA’s in pre-gastrular embryos of Xenopus laevis. Develop Growth Differ 23:589–597

    Article  CAS  Google Scholar 

  • Shiokawa K, Kawazoe Y, Yamana K (1985) Demonstration that inhibitor of rRNA synthesis in “charcoal-extracts” of Xenopus embryos is artifactually produced ammonium perchlorate. Dev Biol 112:258–260

    Article  CAS  Google Scholar 

  • Shiokawa K, Kawazoe Y, Nomura H, Miura T, Nakakura N, Horiuchi T, Yamana K (1986a) Ammonium ion as a possible regulator of the commencement of rRNA synthesis in Xenopus laevis embryogenesis. Dev Biol 115:380–391

    Article  CAS  PubMed  Google Scholar 

  • Shiokawa K, Kawazoe Y, Tashiro K, Yamana K (1986b) Effects of various ammonium salts, amines, polyamines, and alpha-methylornithine on rRNA synthesis in neurula cells of Xenopus laevis and Xenopus borealis. Cell Differ 18:101–108

    Article  CAS  PubMed  Google Scholar 

  • Shiokawa K, Tashiro K, Atsuchi T, Kawazoe Y (1986c) Alteration of the pool of free amino acids during oogenesis, oocyte maturation and embryogenesis of Xenopus laevis and Xenopus borealis. Zool Sci 3:793–799

    CAS  Google Scholar 

  • Shiokawa K, Fu Y, Kawazoe Y, Yamana K (1987) Mode of action of ammonia and amine on rRNA synthesis in Xenopus laevis embryonic cells. Development 100:513–523

    CAS  PubMed  Google Scholar 

  • Shiokawa K, Misumi Y, Tashiro K, Nakakura N, Yamana K, Oh-uchida M (1989) Changes in the patterns of RNA synthesis in early embryogenesis of Xenopus laevis. Cell Differ Dev 28:17–26

    Article  CAS  PubMed  Google Scholar 

  • Shiokawa K, Kurashima R, Shinga J (1994) Temporal control of gene expression from endogenous and exogenously-introduced DNAs in early embryogenesis of Xenopus laevis. Int J Dev Biol 38:249–255

    CAS  PubMed  Google Scholar 

  • Shiokawa K, Kai M, Higo T, Kaito C, Yokoska J, Yasuhiko Y, Kajita E, Nagano M, Yamada Y, Shibata M, Muto T, Shinga J, Hara H, Takayama E, Fukamachi H, Yaoita Y, Igarashi K (2000) Maternal program of apoptosis activated shortly after midblastula transition by overexpression of S-adenosylmethionine decarboxylase in Xenopus early embryos. Comp Biochem Physiol B 126:149–155

    Article  CAS  PubMed  Google Scholar 

  • Shiokawa K, Takayama E, Higo T, Kuroyanagi S, Kaito C, Hara H, Kajitani M, Sekimizu K, Tadakuma T, Miura K-I, Igarashi K, Yaoita Y (2005) Occurrence of pre-MBT synthesis of caspase-8 mRNA and activation of caspase-8 prior to execution of SAMDC (S-adenosylmethionine decarboxylase)-induced, but not p53-induced, apoptosis in Xenopus late blastulae. Biochem Biophys Res Commun 336:682–691

    Article  CAS  PubMed  Google Scholar 

  • Shiokawa K, Aso M, Kondo T, Uchiyama H, Kuroyanagi S, Takai J, Takahashi S, Kajitani M, Kaito C, Sekimizu K, Takayama E, Igarashi K, Hara H (2008) Gene expression in pre-MBT embryos and activation of maternally-inherited program of apoptosis to be executed at around MBT as a fail-safe mechanism in Xenopus early embryogenesis. Gene Regul Syst Biol 2:213–231

    Google Scholar 

  • Takayama E, Higo T, Kai M, Fukasawa M, Nakajima K, Tadakuma T, Hara H, Igarashi K, Yaoita Y, Shiokawa K (2004) Involvement of caspase-9 in execution of the maternal program of apoptosis in Xenopus late blastulae overexpressed with S-adenosylmethionine decarboxylase. Biochem Biophys Res Commun 325:1367–1375

    Article  CAS  PubMed  Google Scholar 

  • Yang J, Tan C, Darken RS, Wilson PA, Klein PS (2002) β-Catenin/Tcf regulated transcription prior to the midblastula transition. Development 129:5743–5752

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors thank Drs. Masayuki Kajitani and Senji Takahashi, Department of Biosciences Teikyo University, for their supports in our research. The works reported about apoptosis were partially supported by Taisho Pharmaceutical Company, and the works on the regulation of ribosomal RNA synthesis was partially supported by the Ministry of Education of Japan, Anna Fuller Memorial Fund for Cancer Research (USA), and Jane Coffin Memorial Fund for Cancer Research (USA).

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Authors and Affiliations

  1. Department of Judo Therapy, Faculty of Medical Technology, Teikyo University, 1-1 Toyosatodai, Utsunomiya, Tochigi, 320-8551, Japan

    Koichiro Shiokawa & Taro Kariya

  2. Department of Biosciences, School of Science and Engineering, Teikyo University, 1-1 Toyosatodai, Utsunomiya, Tochigi, 320-8551, Japan

    Koichiro Shiokawa, Mai Aso, Takeshi Kondo, Jun-Ichi Takai, Junki Yoshida, Takamichi Mishina, Kota Fuchimukai, Tsukasa Ogasawara & Taro Kariya

  3. Molecular Gene Technics, Genetic Resources Technology, Kyushu University, Hakozaki 6-10-1, Fukuoka, 812-8581, Japan

    Kosuke Tashiro

  4. Graduate School of Pharmaceutical Sciences, Chiba University, 1-8-1 Inohana, Chuo-ku, Chiba, 263-8522, Japan

    Kazuei Igarashi

Authors
  1. Koichiro Shiokawa
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  2. Mai Aso
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  8. Tsukasa Ogasawara
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  9. Taro Kariya
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  10. Kosuke Tashiro
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  11. Kazuei Igarashi
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Corresponding author

Correspondence to Koichiro Shiokawa.

Additional information

This review is dedicated to the late Prof. Nello Bagni to whom the first and the last author owe very much in their academic activities in polyamine researches.

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Shiokawa, K., Aso, M., Kondo, T. et al. Effects of S-adenosylmethionine decarboxylase, polyamines, amino acids, and weak bases (amines and ammonia) on development and ribosomal RNA synthesis in Xenopus embryos. Amino Acids 38, 439–449 (2010). https://doi.org/10.1007/s00726-009-0403-z

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