Characterization of epigenetic changes in Rana [Lithobates] catesbeiana tissues during natural and induced thyroid hormone-dependent metamorphosis using mass spectrometry

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2024

Authors

Kuecks-Winger, Haley Noah

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Abstract

Thyroid hormone (TH) signaling is critical for proper development, growth and metabolism in all vertebrates. Amphibian metamorphosis is a TH-dependent developmental process that requires coordinated physical and biochemical changes to facilitate the transition from a tadpole to a frog. Metamorphosis involves extensive tissue-specific changes in the gene expression of differentiated tissues. Rana catesbeiana (American bullfrog) metamorphosis can be precociously induced by treatment with exogenous TH. However, metamorphosis is temperature-dependent and does not proceed at 5°C even in the presence of TH. Remarkably, a subsequent shift to permissive temperatures (24°C) results in an accelerated metamorphosis, implying that TH establishes a molecular memory at 5°C. Previous studies suggest that epigenetic processes, including histone variant incorporation and post-translational modifications, are involved in TH-signalling during natural metamorphosis and during temperature-modulated, TH-induced metamorphosis. Herein, we use mass spectrometry to characterize the histone composition of R. catesbeiana blood, liver, and tailfin during natural and temperature-modulated induced metamorphosis. The natural metamorphosis model identified tissue- and developmental stage-specific changes in histone abundance and PTMs. The temperature-modulated TH-induced metamorphic model demonstrated temperature- and tissue-specific changes in the abundance and PTMs of histones and other chromatin-binding proteins. To our knowledge, this represents the first unbiased analysis of the chromatin-associated proteins during amphibian metamorphosis. The findings presented herein expand our understanding of putative epigenetic factors involved in regulating TH-dependent development, which has broad relevance to all vertebrate species due to the conserved nature of TH action.

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