Nuclear Scaling Is Coordinated among Individual Nuclei in Multinucleated Muscle Fibers

Stefanie E. Windner, Angelika Manhart, Amelia Brown, Alexander Mogilner, Mary K. Baylies

Research output: Contribution to journalArticle

Abstract

Optimal cell performance depends on cell size and the appropriate relative size, i.e., scaling, of the nucleus. How nuclear scaling is regulated and contributes to cell function is poorly understood, especially in skeletal muscle fibers, which are among the largest cells, containing hundreds of nuclei. Here, we present a Drosophila in vivo system to analyze nuclear scaling in whole multinucleated muscle fibers, genetically manipulate individual components, and assess muscle function. Despite precise global coordination, we find that individual nuclei within a myofiber establish different local scaling relationships by adjusting their size and synthetic activity in correlation with positional or spatial cues. While myonuclei exhibit compensatory potential, even minor changes in global nuclear size scaling correlate with reduced muscle function. Our study provides the first comprehensive approach to unraveling the intrinsic regulation of size in multinucleated muscle fibers. These insights to muscle cell biology will accelerate the development of interventions for muscle diseases. Muscle fibers are large multinucleated cells with remarkable size plasticity. Windner et al. investigate the relationship between muscle cell size and nuclear content. They show that cells contain a heterogeneous population of nuclei and explore mechanisms of nuclear coordination, as well as the functional consequences of scaling perturbations.

Original languageEnglish (US)
Pages (from-to)48-62.e3
JournalDevelopmental Cell
Volume49
Issue number1
DOIs
StatePublished - Apr 8 2019

Fingerprint

Muscle
Muscles
Fibers
Cell Size
Muscle Cells
Muscle Development
Skeletal Muscle Fibers
Drosophila
Cues
Cell Biology
Cytology
Plasticity
Population
Cells

Keywords

  • cell size
  • Drosophila
  • Fibrillarin
  • nuclear positioning
  • nuclear scaling
  • nuclear synthetic activity
  • nucleolus
  • polyploidy
  • skeletal muscle
  • syncytial organization

ASJC Scopus subject areas

  • Molecular Biology
  • Biochemistry, Genetics and Molecular Biology(all)
  • Developmental Biology
  • Cell Biology

Cite this

Nuclear Scaling Is Coordinated among Individual Nuclei in Multinucleated Muscle Fibers. / Windner, Stefanie E.; Manhart, Angelika; Brown, Amelia; Mogilner, Alexander; Baylies, Mary K.

In: Developmental Cell, Vol. 49, No. 1, 08.04.2019, p. 48-62.e3.

Research output: Contribution to journalArticle

Windner, Stefanie E. ; Manhart, Angelika ; Brown, Amelia ; Mogilner, Alexander ; Baylies, Mary K. / Nuclear Scaling Is Coordinated among Individual Nuclei in Multinucleated Muscle Fibers. In: Developmental Cell. 2019 ; Vol. 49, No. 1. pp. 48-62.e3.
@article{7aae78abc79d4e37b91f7a416a498cef,
title = "Nuclear Scaling Is Coordinated among Individual Nuclei in Multinucleated Muscle Fibers",
abstract = "Optimal cell performance depends on cell size and the appropriate relative size, i.e., scaling, of the nucleus. How nuclear scaling is regulated and contributes to cell function is poorly understood, especially in skeletal muscle fibers, which are among the largest cells, containing hundreds of nuclei. Here, we present a Drosophila in vivo system to analyze nuclear scaling in whole multinucleated muscle fibers, genetically manipulate individual components, and assess muscle function. Despite precise global coordination, we find that individual nuclei within a myofiber establish different local scaling relationships by adjusting their size and synthetic activity in correlation with positional or spatial cues. While myonuclei exhibit compensatory potential, even minor changes in global nuclear size scaling correlate with reduced muscle function. Our study provides the first comprehensive approach to unraveling the intrinsic regulation of size in multinucleated muscle fibers. These insights to muscle cell biology will accelerate the development of interventions for muscle diseases. Muscle fibers are large multinucleated cells with remarkable size plasticity. Windner et al. investigate the relationship between muscle cell size and nuclear content. They show that cells contain a heterogeneous population of nuclei and explore mechanisms of nuclear coordination, as well as the functional consequences of scaling perturbations.",
keywords = "cell size, Drosophila, Fibrillarin, nuclear positioning, nuclear scaling, nuclear synthetic activity, nucleolus, polyploidy, skeletal muscle, syncytial organization",
author = "Windner, {Stefanie E.} and Angelika Manhart and Amelia Brown and Alexander Mogilner and Baylies, {Mary K.}",
year = "2019",
month = "4",
day = "8",
doi = "10.1016/j.devcel.2019.02.020",
language = "English (US)",
volume = "49",
pages = "48--62.e3",
journal = "Developmental Cell",
issn = "1534-5807",
publisher = "Cell Press",
number = "1",

}

TY - JOUR

T1 - Nuclear Scaling Is Coordinated among Individual Nuclei in Multinucleated Muscle Fibers

AU - Windner, Stefanie E.

AU - Manhart, Angelika

AU - Brown, Amelia

AU - Mogilner, Alexander

AU - Baylies, Mary K.

PY - 2019/4/8

Y1 - 2019/4/8

N2 - Optimal cell performance depends on cell size and the appropriate relative size, i.e., scaling, of the nucleus. How nuclear scaling is regulated and contributes to cell function is poorly understood, especially in skeletal muscle fibers, which are among the largest cells, containing hundreds of nuclei. Here, we present a Drosophila in vivo system to analyze nuclear scaling in whole multinucleated muscle fibers, genetically manipulate individual components, and assess muscle function. Despite precise global coordination, we find that individual nuclei within a myofiber establish different local scaling relationships by adjusting their size and synthetic activity in correlation with positional or spatial cues. While myonuclei exhibit compensatory potential, even minor changes in global nuclear size scaling correlate with reduced muscle function. Our study provides the first comprehensive approach to unraveling the intrinsic regulation of size in multinucleated muscle fibers. These insights to muscle cell biology will accelerate the development of interventions for muscle diseases. Muscle fibers are large multinucleated cells with remarkable size plasticity. Windner et al. investigate the relationship between muscle cell size and nuclear content. They show that cells contain a heterogeneous population of nuclei and explore mechanisms of nuclear coordination, as well as the functional consequences of scaling perturbations.

AB - Optimal cell performance depends on cell size and the appropriate relative size, i.e., scaling, of the nucleus. How nuclear scaling is regulated and contributes to cell function is poorly understood, especially in skeletal muscle fibers, which are among the largest cells, containing hundreds of nuclei. Here, we present a Drosophila in vivo system to analyze nuclear scaling in whole multinucleated muscle fibers, genetically manipulate individual components, and assess muscle function. Despite precise global coordination, we find that individual nuclei within a myofiber establish different local scaling relationships by adjusting their size and synthetic activity in correlation with positional or spatial cues. While myonuclei exhibit compensatory potential, even minor changes in global nuclear size scaling correlate with reduced muscle function. Our study provides the first comprehensive approach to unraveling the intrinsic regulation of size in multinucleated muscle fibers. These insights to muscle cell biology will accelerate the development of interventions for muscle diseases. Muscle fibers are large multinucleated cells with remarkable size plasticity. Windner et al. investigate the relationship between muscle cell size and nuclear content. They show that cells contain a heterogeneous population of nuclei and explore mechanisms of nuclear coordination, as well as the functional consequences of scaling perturbations.

KW - cell size

KW - Drosophila

KW - Fibrillarin

KW - nuclear positioning

KW - nuclear scaling

KW - nuclear synthetic activity

KW - nucleolus

KW - polyploidy

KW - skeletal muscle

KW - syncytial organization

UR - http://www.scopus.com/inward/record.url?scp=85063322351&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85063322351&partnerID=8YFLogxK

U2 - 10.1016/j.devcel.2019.02.020

DO - 10.1016/j.devcel.2019.02.020

M3 - Article

C2 - 30905770

AN - SCOPUS:85063322351

VL - 49

SP - 48-62.e3

JO - Developmental Cell

JF - Developmental Cell

SN - 1534-5807

IS - 1

ER -