Running the gauntlet: challenges to genome integrity in spermiogenesis

ABSTRACTSpecies’ continuity depends on gametogenesis to produce the only cell types that can transmit genetic information across generations. Spermiogenesis, which encompasses post-meiotic, haploid stages of male gametogenesis, is a process that leads to the formation of sperm cells well-known for t...

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Main Authors: Maiko Kitaoka, Yukiko M. Yamashita
Format: Article
Language:English
Published: Taylor & Francis Group 2024-12-01
Series:Nucleus
Subjects:
Online Access:https://www.tandfonline.com/doi/10.1080/19491034.2024.2339220
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author Maiko Kitaoka
Yukiko M. Yamashita
author_facet Maiko Kitaoka
Yukiko M. Yamashita
author_sort Maiko Kitaoka
collection DOAJ
description ABSTRACTSpecies’ continuity depends on gametogenesis to produce the only cell types that can transmit genetic information across generations. Spermiogenesis, which encompasses post-meiotic, haploid stages of male gametogenesis, is a process that leads to the formation of sperm cells well-known for their motility. Spermiogenesis faces three major challenges. First, after two rounds of meiotic divisions, the genome lacks repair templates (no sister chromatids, no homologous chromosomes), making it incredibly vulnerable to any genomic insults over an extended time (typically days-weeks). Second, the sperm genome becomes transcriptionally silent, making it difficult to respond to new perturbations as spermiogenesis progresses. Third, the histone-to-protamine transition, which is essential to package the sperm genome, counterintuitively involves DNA break formation. How spermiogenesis handles these challenges remains poorly understood. In this review, we discuss each challenge and their intersection with the biology of protamines. Finally, we discuss the implication of protamines in the process of evolution.
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spelling doaj.art-00dc7ae8835f4c7fa15e2cd8fabda8482024-04-10T03:29:04ZengTaylor & Francis GroupNucleus1949-10341949-10422024-12-0115110.1080/19491034.2024.2339220Running the gauntlet: challenges to genome integrity in spermiogenesisMaiko Kitaoka0Yukiko M. Yamashita1Whitehead Institute for Biomedical Research and Howard Hughes Medical Institute, Cambridge, MA, USAWhitehead Institute for Biomedical Research and Howard Hughes Medical Institute, Cambridge, MA, USAABSTRACTSpecies’ continuity depends on gametogenesis to produce the only cell types that can transmit genetic information across generations. Spermiogenesis, which encompasses post-meiotic, haploid stages of male gametogenesis, is a process that leads to the formation of sperm cells well-known for their motility. Spermiogenesis faces three major challenges. First, after two rounds of meiotic divisions, the genome lacks repair templates (no sister chromatids, no homologous chromosomes), making it incredibly vulnerable to any genomic insults over an extended time (typically days-weeks). Second, the sperm genome becomes transcriptionally silent, making it difficult to respond to new perturbations as spermiogenesis progresses. Third, the histone-to-protamine transition, which is essential to package the sperm genome, counterintuitively involves DNA break formation. How spermiogenesis handles these challenges remains poorly understood. In this review, we discuss each challenge and their intersection with the biology of protamines. Finally, we discuss the implication of protamines in the process of evolution.https://www.tandfonline.com/doi/10.1080/19491034.2024.2339220DNA damageDouble stranded breaks (DSB)genome integrityprotaminesSpermiogenesis
spellingShingle Maiko Kitaoka
Yukiko M. Yamashita
Running the gauntlet: challenges to genome integrity in spermiogenesis
Nucleus
DNA damage
Double stranded breaks (DSB)
genome integrity
protamines
Spermiogenesis
title Running the gauntlet: challenges to genome integrity in spermiogenesis
title_full Running the gauntlet: challenges to genome integrity in spermiogenesis
title_fullStr Running the gauntlet: challenges to genome integrity in spermiogenesis
title_full_unstemmed Running the gauntlet: challenges to genome integrity in spermiogenesis
title_short Running the gauntlet: challenges to genome integrity in spermiogenesis
title_sort running the gauntlet challenges to genome integrity in spermiogenesis
topic DNA damage
Double stranded breaks (DSB)
genome integrity
protamines
Spermiogenesis
url https://www.tandfonline.com/doi/10.1080/19491034.2024.2339220
work_keys_str_mv AT maikokitaoka runningthegauntletchallengestogenomeintegrityinspermiogenesis
AT yukikomyamashita runningthegauntletchallengestogenomeintegrityinspermiogenesis