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Muscle specific stress fibers give rise to sarcomeres and are mechanistically distinct from stress fibers in non-muscle cells

Aidan M. Feinx, Nilay Taneja, Abigail C. Neininger, Mike R. Visetsouk, Benjamin R. Nixon, Annabelle E. Manalo, Jason R. Becker, Scott W. Crawley, David M. Bader, Matthew J. Tyska, Jennifer H. Gutzman, Dylan T. Burnette
doi: https://doi.org/10.1101/235424
Aidan M. Feinx
1Department of Cell and Developmental Biology, Vanderbilt University, Nashville, TN.
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Nilay Taneja
1Department of Cell and Developmental Biology, Vanderbilt University, Nashville, TN.
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Abigail C. Neininger
1Department of Cell and Developmental Biology, Vanderbilt University, Nashville, TN.
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Mike R. Visetsouk
2Department of Biological Sciences, Cell and Molecular Biology, University of Wisconsin Milwaukee, Milwaukee WI.
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Benjamin R. Nixon
3Department of Medicine, Vanderbilt University Medical Center, Nashville, TN.
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Annabelle E. Manalo
1Department of Cell and Developmental Biology, Vanderbilt University, Nashville, TN.
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Jason R. Becker
3Department of Medicine, Vanderbilt University Medical Center, Nashville, TN.
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Scott W. Crawley
4Department of Biological Sciences, The University of Toledo, Toledo, OH.
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David M. Bader
1Department of Cell and Developmental Biology, Vanderbilt University, Nashville, TN.
3Department of Medicine, Vanderbilt University Medical Center, Nashville, TN.
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Matthew J. Tyska
1Department of Cell and Developmental Biology, Vanderbilt University, Nashville, TN.
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Jennifer H. Gutzman
2Department of Biological Sciences, Cell and Molecular Biology, University of Wisconsin Milwaukee, Milwaukee WI.
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Dylan T. Burnette
1Department of Cell and Developmental Biology, Vanderbilt University, Nashville, TN.
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  • For correspondence: dylan.burnette@vanderbilt.edu
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Abstract

The sarcomere is the basic contractile unit within cardiomyocytes driving heart muscle contraction. We sought to test the mechanisms regulating thin (i.e., actin) and thick (i.e., myosin) filament assembly during sarcomere formation. Thus, we developed an assay using human cardiomyocytes to test de novo sarcomere assembly. Using this assay, we report a population of muscle-specific stress fibers are essential sarcomere precursors. We show sarcomeric actin filaments arise directly from these muscle stress fibers. This process requires formin-mediated but not Arp2/3-mediated actin polymerization and nonmuscle myosin IIB but not non-muscle myosin IIA. Furthermore, we show a short species of β cardiac myosin II filaments grows to form ~1.5 long filaments that then “stitch” together to form the stack of filaments at the core of the sarcomere (i.e., A-band). Interestingly, these are different from mechanisms that have previously been reported during stress fiber assembly in non-muscle cells. Thus, we provide a new model of cardiac sarcomere assembly based on distinct mechanisms of stress fiber regulation between non-muscle and muscle cells.

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Posted December 18, 2017.
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Muscle specific stress fibers give rise to sarcomeres and are mechanistically distinct from stress fibers in non-muscle cells
Aidan M. Feinx, Nilay Taneja, Abigail C. Neininger, Mike R. Visetsouk, Benjamin R. Nixon, Annabelle E. Manalo, Jason R. Becker, Scott W. Crawley, David M. Bader, Matthew J. Tyska, Jennifer H. Gutzman, Dylan T. Burnette
bioRxiv 235424; doi: https://doi.org/10.1101/235424
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Muscle specific stress fibers give rise to sarcomeres and are mechanistically distinct from stress fibers in non-muscle cells
Aidan M. Feinx, Nilay Taneja, Abigail C. Neininger, Mike R. Visetsouk, Benjamin R. Nixon, Annabelle E. Manalo, Jason R. Becker, Scott W. Crawley, David M. Bader, Matthew J. Tyska, Jennifer H. Gutzman, Dylan T. Burnette
bioRxiv 235424; doi: https://doi.org/10.1101/235424

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