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Ecdysteroid-Induced Programmed Cell Death Is Essential for Sex-Specific Wing Degeneration of the Wingless-Female Winter Moth

The winter moth, Nyssiodes lefuarius, has a unique life history in that adults appear during early spring after a long pupal diapause from summer to winter. The moth exhibits striking sexual dimorphism in wing form; males have functional wings of normal size, whereas females lack wings. We previousl...

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Autores principales: Niitsu, Shuhei, Toga, Kouhei, Tomizuka, Shigekazu, Maekawa, Kiyoto, Machida, Ryuichiro, Kamito, Takehiko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3928446/
https://www.ncbi.nlm.nih.gov/pubmed/24558499
http://dx.doi.org/10.1371/journal.pone.0089435
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author Niitsu, Shuhei
Toga, Kouhei
Tomizuka, Shigekazu
Maekawa, Kiyoto
Machida, Ryuichiro
Kamito, Takehiko
author_facet Niitsu, Shuhei
Toga, Kouhei
Tomizuka, Shigekazu
Maekawa, Kiyoto
Machida, Ryuichiro
Kamito, Takehiko
author_sort Niitsu, Shuhei
collection PubMed
description The winter moth, Nyssiodes lefuarius, has a unique life history in that adults appear during early spring after a long pupal diapause from summer to winter. The moth exhibits striking sexual dimorphism in wing form; males have functional wings of normal size, whereas females lack wings. We previously found that cell death of the pupal epithelium of females appears to display condensed chromatin within phagocytes. To provide additional detailed data for interpreting the role of cell death, we performed light microscopy, transmission electron microscopy, and TUNEL assay. We consequently detected two modes of cell death, i.e., dying cells showed both DNA fragmentation derived from epithelial nuclei and autophagic vacuole formation. To elucidate the switching mechanism of sex-specific wing degeneration in females of N. lefuarius, we tested the effects of the steroid hormone 20-hydroxyecdysone (20E) on pupal diapause termination and wing morphogenesis in both sexes. When 20E (5.4 µg) was injected into both sexes within 2 days of pupation, wing degeneration started 4 days after 20E injection in females, whereas wing morphogenesis and scale formation started 6 days after 20E injection in males. We discuss two important findings: (1) degeneration of the pupal wing epithelium of females was not only due to apoptosis and phagocytotic activation but also to autophagy and epithelial cell shrinkage; and (2) 20E terminated the summer diapause of pupae, and triggered selective programmed cell death only of the female-pupal wing epithelium in the wingless female winter moth.
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spelling pubmed-39284462014-02-20 Ecdysteroid-Induced Programmed Cell Death Is Essential for Sex-Specific Wing Degeneration of the Wingless-Female Winter Moth Niitsu, Shuhei Toga, Kouhei Tomizuka, Shigekazu Maekawa, Kiyoto Machida, Ryuichiro Kamito, Takehiko PLoS One Research Article The winter moth, Nyssiodes lefuarius, has a unique life history in that adults appear during early spring after a long pupal diapause from summer to winter. The moth exhibits striking sexual dimorphism in wing form; males have functional wings of normal size, whereas females lack wings. We previously found that cell death of the pupal epithelium of females appears to display condensed chromatin within phagocytes. To provide additional detailed data for interpreting the role of cell death, we performed light microscopy, transmission electron microscopy, and TUNEL assay. We consequently detected two modes of cell death, i.e., dying cells showed both DNA fragmentation derived from epithelial nuclei and autophagic vacuole formation. To elucidate the switching mechanism of sex-specific wing degeneration in females of N. lefuarius, we tested the effects of the steroid hormone 20-hydroxyecdysone (20E) on pupal diapause termination and wing morphogenesis in both sexes. When 20E (5.4 µg) was injected into both sexes within 2 days of pupation, wing degeneration started 4 days after 20E injection in females, whereas wing morphogenesis and scale formation started 6 days after 20E injection in males. We discuss two important findings: (1) degeneration of the pupal wing epithelium of females was not only due to apoptosis and phagocytotic activation but also to autophagy and epithelial cell shrinkage; and (2) 20E terminated the summer diapause of pupae, and triggered selective programmed cell death only of the female-pupal wing epithelium in the wingless female winter moth. Public Library of Science 2014-02-18 /pmc/articles/PMC3928446/ /pubmed/24558499 http://dx.doi.org/10.1371/journal.pone.0089435 Text en © 2014 Niitsu et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Niitsu, Shuhei
Toga, Kouhei
Tomizuka, Shigekazu
Maekawa, Kiyoto
Machida, Ryuichiro
Kamito, Takehiko
Ecdysteroid-Induced Programmed Cell Death Is Essential for Sex-Specific Wing Degeneration of the Wingless-Female Winter Moth
title Ecdysteroid-Induced Programmed Cell Death Is Essential for Sex-Specific Wing Degeneration of the Wingless-Female Winter Moth
title_full Ecdysteroid-Induced Programmed Cell Death Is Essential for Sex-Specific Wing Degeneration of the Wingless-Female Winter Moth
title_fullStr Ecdysteroid-Induced Programmed Cell Death Is Essential for Sex-Specific Wing Degeneration of the Wingless-Female Winter Moth
title_full_unstemmed Ecdysteroid-Induced Programmed Cell Death Is Essential for Sex-Specific Wing Degeneration of the Wingless-Female Winter Moth
title_short Ecdysteroid-Induced Programmed Cell Death Is Essential for Sex-Specific Wing Degeneration of the Wingless-Female Winter Moth
title_sort ecdysteroid-induced programmed cell death is essential for sex-specific wing degeneration of the wingless-female winter moth
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3928446/
https://www.ncbi.nlm.nih.gov/pubmed/24558499
http://dx.doi.org/10.1371/journal.pone.0089435
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