Thyroid hormone receptor beta is critical for intestinal remodeling during Xenopus tropicalis metamorphosis

Shibata, Yuki; Tanizaki, Yuta; Shi, Yun‐Bo

doi:10.1186/s13578-020-00411-5

Cited by 32 publications

(21 citation statements)

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“…ChIP-Seq identification of candidate TR target genes during intestinal remodeling. We and others have recently shown that knocking out of either TRα or TRβ delays intestinal remodeling during natural and/or T3 induced metamorphosis 11,[13][14][15]18 . RNA-Seq analysis of the intestine of premetamorphic wild-type and TRα −/− tadpoles treated with or without T3 for 18 h revealed that most of the T3 regulated genes were dependent on TRα, suggesting that TRα plays a dominant role early during T3induced intestinal remodeling 19 .…”

Section: Resultsmentioning

confidence: 95%

“…In addition to epithelial transformation, the connective tissue and muscles also remodel extensively, accompanied by shortening of the intestine 5,9 . More recently, we and others have used genome-editing tools such as TALEN and CRISPR/Cas enzymes 10 to study the role of endogenous TR genes during metamorphosis [11][12][13][14][15][16][17][18] . These studies revealed an important role of endogenous TRs during intestinal remodeling.…”

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Thyroid hormone receptor α controls larval intestinal epithelial cell death by regulating the CDK1 pathway

et al. 2022

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Thyroid hormone (T3) regulates adult intestine development through T3 receptors (TRs). It is difficult to study TR function during postembryonic intestinal maturation in mammals due to maternal influence. We chose intestinal remodeling during Xenopus tropicalis metamorphosis as a model to study TR function in adult organ development. By using ChIP (chromatin immunoprecipitation)-Seq, we identified over 3000 TR-bound genes in the intestine of premetamorphic wild type or TRα (the major TR expressed during premetamorphosis)-knockout tadpoles. Surprisingly, cell cycle-related GO (gene ontology) terms and biological pathways were highly enriched among TR target genes even though the first major event during intestinal metamorphosis is larval epithelial cell death, and TRα knockout drastically reduced this enrichment. More importantly, treatment of tadpoles with cell cycle inhibitors blocked T3-induced intestinal remodeling, especially larval epithelial cell death, suggesting that TRα-dependent activation of cell cycle is important for T3-induced apoptosis during intestinal remodeling.

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Section: Resultsmentioning

confidence: 95%

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Thyroid hormone receptor α controls larval intestinal epithelial cell death by regulating the CDK1 pathway

et al. 2022

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“…5 ) that promote transcription of genes that drive metamorphosis ( Kulkarni and Buchholz, 2014 ; Sachs and Buchholz, 2019 ). For example, CS can induce expression of TRs to increase cellular sensitivity to the hormone signal ( Bonett et al, 2010 ; Kikuyama et al, 1993 ; Niki et al, 1981 ; Suzuki and Kikuyama, 1983 ), especially TR beta which is necessary for proper completion of metamorphosis ( Nakajima et al, 2019 ; Shibata et al, 2020a , 2020b ). The actions of CSs were synergistic with low or subthreshold doses of TH, producing strong induction of TR expression ( Bonett et al, 2010 ).…”

Section: Stress Hormones and Developmental Plasticitymentioning

confidence: 99%

Stress hormones mediate developmental plasticity in vertebrates with complex life cycles

Denver

2021

Neurobiology of Stress

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The environment experienced by developing organisms can shape the timing and character of developmental processes, generating different phenotypes from the same genotype, each with different probabilities of survival and performance as adults. Chordates have two basic modes of development, indirect and direct. Species with indirect development, which includes most fishes and amphibians, have a complex life cycle with a free-swimming larva that is typically a growth stage, followed by a metamorphosis into the adult form. Species with direct development, which is an evolutionarily derived developmental mode, develop directly from embryo to the juvenile without an intervening larval stage. Among the best studied species with complex life cycles are the amphibians, especially the anurans (frogs and toads). Amphibian tadpoles are exposed to diverse biotic and abiotic factors in their developmental habitat. They have extensive capacity for developmental plasticity, which can lead to the expression of different, adaptive morphologies as tadpoles (polyphenism), variation in the timing of and size at metamorphosis, and carry-over effects on the phenotype of the juvenile/adult. The neuroendocrine stress axis plays a pivotal role in mediating environmental effects on amphibian development. Before initiating metamorphosis, if tadpoles are exposed to predators they upregulate production of the stress hormone corticosterone (CORT), which acts directly on the tail to cause it to grow, thereby increasing escape performance. When tadpoles reach a minimum body size to initiate metamorphosis they can vary the timing of transformation in relation to growth opportunity or mortality risk in the larval habitat. They do this by modulating the production of thyroid hormone (TH), the primary inducer of metamorphosis, and CORT, which synergizes with TH to promote tissue transformation. Hypophysiotropic neurons that release the stress neurohormone corticotropin-releasing factor (CRF) are activated in response to environmental stress (e.g., pond drying, food restriction, etc.), and CRF accelerates metamorphosis by directly inducing secretion of pituitary thyrotropin and corticotropin, thereby increasing secretion of TH and CORT. Although activation of the neuroendocrine stress axis promotes immediate survival in a deteriorating larval habitat, costs may be incurred such as reduced tadpole growth and size at metamorphosis. Small size at transformation can impair performance of the adult, reducing probability of survival in the terrestrial habitat, or fecundity. Furthermore, elevations in CORT in the tadpole caused by environmental stressors cause long term, stable changes in neuroendocrine function, behavior and physiology of the adult, which can affect fitness. Comparative studies show that the roles of stress hormones in developmental plasticity are conserved across vertebrate taxa including humans.

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“…Interestingly, we have shown previously that high levels of PRMT1 mRNA are expressed in an evolutionally conserved manner during the formation of the adult intestine in vertebrates, including intestinal maturation in mouse around 2–3 weeks after birth and intestinal remodeling during Xenopus laevis metamorphosis [ 31 ]. Importantly, intestinal remodeling during amphibian metamorphosis involves de novo development of adult stem cells in a T3-dependent process and that T3 signaling in the larval intestine is both necessary and sufficient for the formation of the adult stem cells through the dedifferentiation of some larval epithelial cells [ 32 – 40 ]. Furthermore, transgenic and knockdown studies in Xenopus have revealed a critical role of PRMT1 as a TR coactivator for amphibian metamorphosis and in the development of the adult stem cells [ 31 ].…”

Section: Introductionmentioning

confidence: 99%

Protein arginine methyltransferase 1 regulates cell proliferation and differentiation in adult mouse adult intestine

et al. 2021

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Background Adult stem cells play an essential role in adult organ physiology and tissue repair and regeneration. While much has been learnt about the property and function of various adult stem cells, the mechanisms of their development remain poorly understood in mammals. Earlier studies suggest that the formation of adult mouse intestinal stem cells takes place during the first few weeks after birth, the postembryonic period when plasma thyroid hormone (T3) levels are high. Furthermore, deficiency in T3 signaling leads to defects in adult mouse intestine, including reduced cell proliferation in the intestinal crypts, where stem cells reside. Our earlier studies have shown that protein arginine methyltransferase 1 (PRMT1), a T3 receptor coactivator, is highly expressed during intestinal maturation in mouse. Methods We have analyzed the expression of PRMT1 by immunohistochemistry and studied the effect of tissue-specific knockout of PRMT1 in the intestinal epithelium. Results We show that PRMT1 is expressed highly in the proliferating transit amplifying cells and crypt base stem cells. By using a conditional knockout mouse line, we have demonstrated that the expression of PRMT1 in the intestinal epithelium is critical for the development of the adult mouse intestine. Specific removal of PRMT1 in the intestinal epithelium results in, surprisingly, more elongated adult intestinal crypts with increased cell proliferation. In addition, epithelial cell migration along the crypt-villus axis and cell death on the villus are also increased. Furthermore, there are increased Goblet cells and reduced Paneth cells in the crypt while the number of crypt base stem cells remains unchanged. Conclusions Our finding that PRMT1 knockout increases cell proliferation is surprising considering the role of PRMT1 in T3-signaling and the importance of T3 for intestinal development, and suggests that PRMT1 likely regulates pathways in addition to T3-signaling to affect intestinal development and/or homeostasis, thus affecting cell proliferating and epithelial turn over in the adult.

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Thyroid hormone receptor beta is critical for intestinal remodeling during Xenopus tropicalis metamorphosis

Cited by 32 publications

References 76 publications

Thyroid hormone receptor α controls larval intestinal epithelial cell death by regulating the CDK1 pathway

Thyroid hormone receptor α controls larval intestinal epithelial cell death by regulating the CDK1 pathway

Stress hormones mediate developmental plasticity in vertebrates with complex life cycles

Protein arginine methyltransferase 1 regulates cell proliferation and differentiation in adult mouse adult intestine

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