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Cardiomyocyte nuclearity and ploidy: when is double trouble?

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Abstract

Considerable effort has gone into investigating mechanisms that underlie the developmental transition in which mammalian cardiomyocytes (CMs) switch from being able to proliferate during development, to essentially having lost that ability at maturity. This problem is interesting not only for scientific curiosity, but also for its clinical relevance because controlling the ability of mature CMs to replicate would provide a much-needed approach for restoring cardiac function in damaged hearts. In this review, we focus on the propensity of mature mammalian CMs to be multinucleated and polyploid, and the extent to which this may be necessary for normal physiology yet possibly disadvantageous in some circumstances. In this context, we explore whether the concept of the myonuclear domain (MND) in multinucleated skeletal muscle fibers might apply to cardiomyocytes, and whether cardio-MND size might be related to the transition of CMs to become multinuclear. Nuclei in CMs are almost certainly integrators of not only biochemical, but also—because of their central location within the myofibrils—mechanical information, and this multimodal, integrative function in adult CMs—involving molecules that have been extensively studied along with newly identified possibilities—could influence both gene expression as well as replication of the genome and the nuclei themselves.

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Notes

  1. We have chosen to use “nuclearity” to refer to the number of nuclei in a cell, paralleling its definition in chemistry. Note that “nucleation” has been used more commonly in the cell biology literature to refer to the number of nuclei in a cell and also the process of increasing the number of nuclei in a cell, while it has different meanings in chemistry and biochemistry. In this review, we retain the limited use of “binucleation” to refer to the process of increasing the number of nuclei in a cell from one to two. Furthermore, to avoid confusion with the class of blood cells termed “mononuclear,” the commonly used, related terms “mononucleated” (instead of mononuclear), “binucleated,” “tetranucleated” and “multinucleated” are used to describe cells with one nucleus, two nuclei, four nuclei, or more than one nucleus, respectively.

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Acknowledgements

We thank: Mark Bauer in Florida State University’s College of Medicine for assistance with artistic development and graphic design of Fig. 1; Karissa Dieseldorff Jones and Jennifer M. Le Patourel for expert assistance with obtaining and imaging isolated cardiomyocytes (Fig. 2) using the microscopy facilities of Florida State University’s Biological Science Imaging Resource in the Department of Biological Science; Drs. Jonathan Bensley and M. Jane Black for permission to plot in Fig. 3 their original data from Table 1 in Bensley et al. (2016) that was published under a Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0); and Dr. Jerome Irianto, Jamie R. Johnston, Karissa Dieseldorff Jones and Jennifer M. Le Patourel for helpful discussions. Supported by U.S. National Institutes of Health National Heart, Lung and Blood Institute Grant No. R01 HL128683 to JRP.

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Correspondence to P. Bryant Chase.

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Landim-Vieira, M., Schipper, J.M., Pinto, J.R. et al. Cardiomyocyte nuclearity and ploidy: when is double trouble?. J Muscle Res Cell Motil 41, 329–340 (2020). https://doi.org/10.1007/s10974-019-09545-7

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  • DOI: https://doi.org/10.1007/s10974-019-09545-7

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