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Evidence for hormonal control of heart regenerative capacity during endothermy acquisition

by Bigley, Rachel B. , Cutie, Stephen , Szweda, Luke I. , Hirose, Kentaro , Scanlan, Thomas S. , Reeder, DeeAnn M. , Yartsev, Michael M. , Wolfgang, Michael J. , Smith, Megan , Schmid, Tobias , Maden, Malcom , Payumo, Alexander Y. , Huang, Guo N. , Wilson, Emily , Muroy, Sandra E. , Olgin, Jeffrey E. , Flamant, Frederic , Wang, Jiajia , Field, Kenneth A. , Gillett, Ellen , Zhang, Hao , Guyot, Romain , Lunn, Dominic , Hoang, Alison , Yu, Hongyao , Buffenstein, Rochelle , Grützner, Frank , Hu, Guang

in Adults / Animals / Body temperature / Body Temperature Regulation / Cardiomyocytes / Cell Cycle Checkpoints / Cell Proliferation / Correlation / Danio rerio / Diploids / Diploidy / Engineering Sciences / Heart / Heart - physiology / Hormones / Inactivation / Mammals / Metabolic rate / Metabolism / Mice / Myocytes, Cardiac - classification / Myocytes, Cardiac - physiology / Ontogeny / Phylogeny / Polyploidy / Receptors, Thyroid Hormone - genetics / Receptors, Thyroid Hormone - physiology / Regeneration - drug effects / Regeneration - genetics / Regeneration - physiology / Signal Transduction / Thyroid / Thyroid gland / Thyroid hormones / Thyroid Hormones - pharmacology / Thyroid Hormones - physiology / Thyroxine / Tradeoffs / Vertebrates / Zebrafish

2019

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2019

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2019

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Journal Article

Evidence for hormonal control of heart regenerative capacity during endothermy acquisition

Bigley, Rachel B.,

Cutie, Stephen,

Szweda, Luke I.,

Hirose, Kentaro,

Scanlan, Thomas S.,

Reeder, DeeAnn M.,

Yartsev, Michael M.,

Wolfgang, Michael J.,

Smith, Megan,

Schmid, Tobias,

Maden, Malcom,

Payumo, Alexander Y.,

Huang, Guo N.,

Wilson, Emily,

Muroy, Sandra E.,

Olgin, Jeffrey E.,

Flamant, Frederic,

Wang, Jiajia,

Field, Kenneth A.,

Gillett, Ellen,

Zhang, Hao,

Guyot, Romain,

Lunn, Dominic,

Hoang, Alison,

Yu, Hongyao,

Buffenstein, Rochelle,

Grützner, Frank,

Hu, Guang

2019

Overview

Tissue regenerative potential displays striking divergence across phylogeny and ontogeny, but the underlying mechanisms remain enigmatic. Loss of mammalian cardiac regenerative potential correlates with cardiomyocyte cell-cycle arrest and polyploidization as well as the development of postnatal endothermy. We reveal that diploid cardiomyocyte abundance across 41 species conforms to Kleiber’s law—the ¾-power law scaling of metabolism with bodyweight—and inversely correlates with standard metabolic rate, body temperature, and serum thyroxine level. Inactivation of thyroid hormone signaling reduces mouse cardiomyocyte polyploidization, delays cell-cycle exit, and retains cardiac regenerative potential in adults. Conversely, exogenous thyroid hormones inhibit zebrafish heart regeneration. Thus, our findings suggest that loss of heart regenerative capacity in adult mammals is triggered by increasing thyroid hormones and may be a trade-off for the acquisition of endothermy.

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Publisher

American Association for the Advancement of Science,The American Association for the Advancement of Science,American Association for the Advancement of Science (AAAS)

Subject

Adults

/ Animals

/ Body temperature

/ Body Temperature Regulation

/ Cardiomyocytes

/ Cell Cycle Checkpoints