Maternal program of apoptosis activated shortly after midblastula transition by overexpression of S-adenosylmethionine decarboxylase in Xenopus early embryos

Koichiro Shiokawa, Masatake Kai, Takayasu Higo, Chikara Kaito, Jun'ichi Yokoska, Yukuto Yasuhiko, Eri Kajita, Michiyo Nagano, Yoichi Yamada, Mikihito Shibata, Tomoyasu Muto, Jun Shinga, Hiroshi Hara, Eiji Takayama, Hiroshi Fukamachi, Yoshio Yaoita, Kazuei Igarashi

Research output: Contribution to journalReview article

7 Citations (Scopus)

Abstract

When we studied polyamine metabolism in Xenopus embryos, we cloned the cDNA for Xenopus S-adenosylmethionine decarboxylase (SAMDC), which converts SAM (S-adenosylmethionine), the methyl donor, into decarboxylated SAM (dcSAM), the aminopropyl donor, and microinjected its in vitro transcribed mRNA into Xenopus fertilized eggs. We found here that the mRNA injection induces a SAM deficient state in early embryos due to over-function of the overexpressed SAMDC, which in turn induces inhibition of protein synthesis. Such embryos developed quite normally until blastula stage, but stopped development at the early gastrula stage, due to induction of massive cell dissociation and cell autolysis, irrespective of the dosage and stage of the mRNA injection. We found that the dissociated cells were TUNEL-positive, contained fragmented nuclei with ladder-forming DNA, and furthermore, rescued completely by coinjection of Bcl-2 mRNA. Thus, overexpression of SAMDC in Xenopus embryos appeared to switch on apoptotic program, probably via inhibition of protein synthesis. Here, we briefly review our results together with those reported from other laboratories. After discussing the general importance of this newly discovered apoptotic program, we propose that the maternal program of apoptosis serves as a surveillance mechanism to eliminate metabolically severely-damaged cells and functions as a 'fail-safe' mechanism for normal development in Xenopus embryos. Copyright (C) 2000 Elsevier Science Inc.

Original languageEnglish
Pages (from-to)149-155
Number of pages7
JournalComparative Biochemistry and Physiology - B Biochemistry and Molecular Biology
Volume126
Issue number2
DOIs
Publication statusPublished - Jan 1 2000
Externally publishedYes

Fingerprint

Adenosylmethionine Decarboxylase
Xenopus
Embryonic Structures
Mothers
Apoptosis
S-Adenosylmethionine
Messenger RNA
Ladders
Polyamines
Blastula
Gastrula
Autolysis
Injections
Metabolism
Zygote
In Situ Nick-End Labeling
Proteins
Complementary DNA
Cells
Switches

Keywords

  • Bcl-2
  • Cell autonomous dissociation
  • Early embryogenesis
  • Maternal apoptotic program
  • Midblastula transition
  • Overexpression of SAMDC
  • Polyamines
  • S-adenosylmethionine decarboxylase cDNA
  • Surveillance mechanism
  • Xenopus embryos

ASJC Scopus subject areas

  • Biochemistry
  • Physiology
  • Molecular Biology

Cite this

Maternal program of apoptosis activated shortly after midblastula transition by overexpression of S-adenosylmethionine decarboxylase in Xenopus early embryos. / Shiokawa, Koichiro; Kai, Masatake; Higo, Takayasu; Kaito, Chikara; Yokoska, Jun'ichi; Yasuhiko, Yukuto; Kajita, Eri; Nagano, Michiyo; Yamada, Yoichi; Shibata, Mikihito; Muto, Tomoyasu; Shinga, Jun; Hara, Hiroshi; Takayama, Eiji; Fukamachi, Hiroshi; Yaoita, Yoshio; Igarashi, Kazuei.

In: Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology, Vol. 126, No. 2, 01.01.2000, p. 149-155.

Research output: Contribution to journalReview article

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', Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology, vol. 126, no. 2, pp. 149-155. https://doi.org/10.1016/S0305-0491(00)00193-0
Shiokawa, Koichiro ; Kai, Masatake ; Higo, Takayasu ; Kaito, Chikara ; Yokoska, Jun'ichi ; Yasuhiko, Yukuto ; Kajita, Eri ; Nagano, Michiyo ; Yamada, Yoichi ; Shibata, Mikihito ; Muto, Tomoyasu ; Shinga, Jun ; Hara, Hiroshi ; Takayama, Eiji ; Fukamachi, Hiroshi ; Yaoita, Yoshio ; Igarashi, Kazuei. / Maternal program of apoptosis activated shortly after midblastula transition by overexpression of S-adenosylmethionine decarboxylase in Xenopus early embryos. In: Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology. 2000 ; Vol. 126, No. 2. pp. 149-155.
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AU - Shiokawa, Koichiro

AU - Kai, Masatake

AU - Higo, Takayasu

AU - Kaito, Chikara

AU - Yokoska, Jun'ichi

AU - Yasuhiko, Yukuto

AU - Kajita, Eri

AU - Nagano, Michiyo

AU - Yamada, Yoichi

AU - Shibata, Mikihito

AU - Muto, Tomoyasu

AU - Shinga, Jun

AU - Hara, Hiroshi

AU - Takayama, Eiji

AU - Fukamachi, Hiroshi

AU - Yaoita, Yoshio

AU - Igarashi, Kazuei

PY - 2000/1/1

Y1 - 2000/1/1

N2 - When we studied polyamine metabolism in Xenopus embryos, we cloned the cDNA for Xenopus S-adenosylmethionine decarboxylase (SAMDC), which converts SAM (S-adenosylmethionine), the methyl donor, into decarboxylated SAM (dcSAM), the aminopropyl donor, and microinjected its in vitro transcribed mRNA into Xenopus fertilized eggs. We found here that the mRNA injection induces a SAM deficient state in early embryos due to over-function of the overexpressed SAMDC, which in turn induces inhibition of protein synthesis. Such embryos developed quite normally until blastula stage, but stopped development at the early gastrula stage, due to induction of massive cell dissociation and cell autolysis, irrespective of the dosage and stage of the mRNA injection. We found that the dissociated cells were TUNEL-positive, contained fragmented nuclei with ladder-forming DNA, and furthermore, rescued completely by coinjection of Bcl-2 mRNA. Thus, overexpression of SAMDC in Xenopus embryos appeared to switch on apoptotic program, probably via inhibition of protein synthesis. Here, we briefly review our results together with those reported from other laboratories. After discussing the general importance of this newly discovered apoptotic program, we propose that the maternal program of apoptosis serves as a surveillance mechanism to eliminate metabolically severely-damaged cells and functions as a 'fail-safe' mechanism for normal development in Xenopus embryos. Copyright (C) 2000 Elsevier Science Inc.

AB - When we studied polyamine metabolism in Xenopus embryos, we cloned the cDNA for Xenopus S-adenosylmethionine decarboxylase (SAMDC), which converts SAM (S-adenosylmethionine), the methyl donor, into decarboxylated SAM (dcSAM), the aminopropyl donor, and microinjected its in vitro transcribed mRNA into Xenopus fertilized eggs. We found here that the mRNA injection induces a SAM deficient state in early embryos due to over-function of the overexpressed SAMDC, which in turn induces inhibition of protein synthesis. Such embryos developed quite normally until blastula stage, but stopped development at the early gastrula stage, due to induction of massive cell dissociation and cell autolysis, irrespective of the dosage and stage of the mRNA injection. We found that the dissociated cells were TUNEL-positive, contained fragmented nuclei with ladder-forming DNA, and furthermore, rescued completely by coinjection of Bcl-2 mRNA. Thus, overexpression of SAMDC in Xenopus embryos appeared to switch on apoptotic program, probably via inhibition of protein synthesis. Here, we briefly review our results together with those reported from other laboratories. After discussing the general importance of this newly discovered apoptotic program, we propose that the maternal program of apoptosis serves as a surveillance mechanism to eliminate metabolically severely-damaged cells and functions as a 'fail-safe' mechanism for normal development in Xenopus embryos. Copyright (C) 2000 Elsevier Science Inc.

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KW - Midblastula transition

KW - Overexpression of SAMDC

KW - Polyamines

KW - S-adenosylmethionine decarboxylase cDNA

KW - Surveillance mechanism

KW - Xenopus embryos

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