Rapid and selective removal of larval erythrocytes from systemic circulation during metamorphosis of the bullfrog, <i>Rana catesbeiana</i>

Hasebe, Takashi; Oshima, Hiroyuki; Kawamura, Kazushi; Kikuyama, Sakaé

doi:10.1046/j.1440-169x.1999.00461.x

Cited by 20 publications

(11 citation statements)

References 18 publications

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“…Previous work has shown that larval erythrocytes containing larval globins are replaced by adult erythrocytes expressing adult globins during natural and TH-induced metamorphosis (Weber, 1996;Hasebe et al, 1999). A decrease in larval ␤-globin mRNA during natural metamorphosis has been reported previously (Banville and Williams, 1985).…”

Section: Discussionmentioning

confidence: 82%

Distinctive gene profiles occur at key points during natural metamorphosis in the Xenopus laevis tadpole tail

Veldhoen

Crump

Werry

et al. 2002

Developmental Dynamics

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Thyroid hormones (THs) are essential for tadpole metamorphosis into a juvenile frog; however, a complex interplay between additional hormones and signaling events also contributes to this dramatic developmental phase. A major mechanism of TH action is the nuclear receptor-mediated regulation of gene transcription of responsive genes. By using the precocious metamorphic model, several genes have been identified as TH responsive in the regressing tail. Many of these genes also exhibit altered expression during natural metamorphosis. Although identification of these genes provides insight into the mechanism whereby TH acts, complex interplay between TH and other hormones and the developmental stage-dependency of tissue responses contribute to the timing and coordination of metamorphic events. We investigated the temporal gene expression profile in Xenopus laevis tadpole tails from premetamorphosis through metamorphic climax by using a combination of a novel frog cDNA array containing 420 genes and quantitative real-time PCR. Seventy-nine genes were identified whose steady-state mRNA expression levels were altered in the tadpole tail during natural metamorphosis, of which 34 have previously been identified to be TH responsive in frogs or mammals. Of these genes, 75 clustered into 13 groups that displayed distinct developmental expression profiles. The levels of 28 transcripts were altered during premetamorphosis, 31 during prometamorphosis, and 43 with the onset of tail regression. This work establishes an important baseline for determining the mechanisms whereby tissues undergo differing metamorphic fates.

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Section: Discussionmentioning

confidence: 82%

Distinctive gene profiles occur at key points during natural metamorphosis in the Xenopus laevis tadpole tail

Veldhoen

Crump

Werry

et al. 2002

Developmental Dynamics

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“…In this model, however, it is difficult to explain how the mature, larval RBCs circulating in metamorphosing tadpoles are selectively removed from the circulation. Because selective apoptosis of mature, larval RBCs in the spleen was demonstrated in vivo at the metamorphosis climax, and in recipient adults treated with T 3 in RBC-transfer experiments (Tamori and Wakahara, 2000), it can be concluded the larval-adult conversion of RBCs in X. laevis is conducted by replacement of RBC populations, which is similar to the mechanism known in general transformation in anuran metamorphosis, selective removal of mature, larval specific cells (Hasebe et al, 1999;Izutsu et al, 1996;Nishikawa and Hayashi, 1995;Ohmura and Wakahara, 1998;Yoshizato, 1992).…”

Section: Selective Removal Of Larval Rbcs During Metamorphosismentioning

confidence: 72%

“…Recently, Hasebe et al (1999) demonstrated that the larval RBCs were selectively removed from the systemic circulation at the time of the metamorphic climax in R. catesbeiana, by means of in vitro fluorescence labeling of RBCs and injection of the labeled cells into animals at various metamorphic stages. The labeled larval RBCs were ingested by hepatic and splenic macrophages, indicating that macrophages are involved in the splenic elimination of larval cells.…”

Section: Selective Removal Of Larval Rbcs During Metamorphosismentioning

confidence: 99%

Mechanisms of Egg Activation and Polyspermy Block in Amphibians and Comparative Aspects with Fertilization in Other Vertebrates

Iwao¹

2000

Zoological Science

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“…Surprisingly, approximately 10% of total RBCs are still larval-type at 3 weeks after the completion of metamorphosis, and it takes another 5 months to complete Hb switching [57] This delayed removal of larval cells may be related to the fact that postmetamorphic X. laevis froglets remain aquatic. Larval RBCs, but not co-existing adult RBCs, are selectively sequestered from the systemic circulation by macrophages in the liver and spleen during metamorphic climax [56]. Interestingly, in R. catesbeiana during the metamorphic climax, circulating adult RBCs, but not larval RBCs, contain fragmented genome (DNA ladder) that is typical to apoptotic cells, suggesting that some of the adult RBCs undergo apoptosis just when they appear as in the mature adult frog [55, 58] and that larval RBCs do not undergo typical apoptosis at least in the circulating blood [55].…”

Section: Apoptosis In Larva-specific and Larval-to-adult Remodeling Omentioning

confidence: 99%

Apoptosis in amphibian organs during metamorphosis

2009

Self Cite

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During amphibian metamorphosis, the larval tissues/organs rapidly degenerate to adapt from the aquatic to the terrestrial life. At the cellular level, a large quantity of apoptosis occurs in a spatiotemporally-regulated fashion in different organs to ensure timely removal of larval organs/tissues and the development of adult ones for the survival of the individuals. Thus, amphibian metamorphosis provides us a good opportunity to understand the mechanisms regulating apoptosis. To investigate this process at the molecular level, a number of thyroid hormone (TH) response genes have been isolated from several organs of Xenopus laevis tadpoles and their expression and functional analyses are now in progress using modern molecular and genetic technologies. In this review, we will first summarize when and where apoptosis occurs in typical larva-specific and larval-to-adult remodeling amphibian organs to highlight that the timing of apoptosis is different in different tissues/organs, even though all are induced by the same circulating TH. Next, to discuss how TH spatiotemporally regulates the apoptosis, we will focus on apoptosis of the X. laevis small intestine, one of the best characterized remodeling organs. Functional studies of TH response genes using transgenic frogs and culture techniques have shown that apoptosis of larval epithelial cells can be induced by TH either cell-autonomously or indirectly through interactions with extracellular matrix (ECM) components of the underlying basal lamina. Here, we propose that multiple intra- and extracellular apoptotic pathways are coordinately controlled by TH to ensure massive but well-organized apoptosis, which is essential for the proper progression of amphibian metamorphosis.

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Rapid and selective removal of larval erythrocytes from systemic circulation during metamorphosis of the bullfrog, Rana catesbeiana

Cited by 20 publications

References 18 publications

Distinctive gene profiles occur at key points during natural metamorphosis in the Xenopus laevis tadpole tail

Distinctive gene profiles occur at key points during natural metamorphosis in the Xenopus laevis tadpole tail

Mechanisms of Egg Activation and Polyspermy Block in Amphibians and Comparative Aspects with Fertilization in Other Vertebrates

Apoptosis in amphibian organs during metamorphosis

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