A nuclear F-actin scaffold stabilizes ribonucleoprotein droplets against gravity in large cells

Actin is abundant in the nuclei of oocytes but its role has been unclear. Feric and Brangwynne find that actin forms a network that prevents the sedimentation of RNA and protein bodies caused by gravitational forces. The size of a typical eukaryotic cell is of the order of ∼10 μm. However, some cell...

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Vydáno v:Nature cell biology Ročník 15; číslo 10; s. 1253 - 1259
Hlavní autoři: Feric, Marina, Brangwynne, Clifford P.
Médium: Journal Article
Jazyk:angličtina
Vydáno: London Nature Publishing Group UK 01.10.2013
Nature Publishing Group
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ISSN:1465-7392, 1476-4679, 1476-4679
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Abstract Actin is abundant in the nuclei of oocytes but its role has been unclear. Feric and Brangwynne find that actin forms a network that prevents the sedimentation of RNA and protein bodies caused by gravitational forces. The size of a typical eukaryotic cell is of the order of ∼10 μm. However, some cell types grow to very large sizes, including oocytes (immature eggs) of organisms from humans to starfish. For example, oocytes of the frog Xenopus laevis grow to a diameter ≥1 mm. They have a correspondingly large nucleus (germinal vesicle) of ∼450 μm in diameter, which is similar to smaller somatic nuclei, but contains a significantly higher concentration of actin. The form and structure of this nuclear actin remain controversial, and its potential mechanical role within these large nuclei is unknown. Here, we use a microrheology and quantitative imaging approach to show that germinal vesicles contain an elastic F-actin scaffold that mechanically stabilizes these large nuclei against gravitational forces, which are usually considered negligible within cells. We find that on actin disruption, ribonucleoprotein droplets, including nucleoli and histone locus bodies, undergo gravitational sedimentation and fusion. We develop a model that reveals how gravity becomes an increasingly potent force as cells and their nuclei grow larger than ∼10 μm, explaining the requirement for a stabilizing nuclear F-actin scaffold in large Xenopus oocytes. All life forms are subject to gravity, and our results may have broad implications for cell growth and size control.
AbstractList The size of a typical eukaryotic cell is of the order of ∼10 μm. However, some cell types grow to very large sizes, including oocytes (immature eggs) of organisms from humans to starfish. For example, oocytes of the frog Xenopus laevis grow to a diameter ≥1 mm. They have a correspondingly large nucleus (germinal vesicle) of ∼450 μm in diameter, which is similar to smaller somatic nuclei, but contains a significantly higher concentration of actin. The form and structure of this nuclear actin remain controversial, and its potential mechanical role within these large nuclei is unknown. Here, we use a microrheology and quantitative imaging approach to show that germinal vesicles contain an elastic F-actin scaffold that mechanically stabilizes these large nuclei against gravitational forces, which are usually considered negligible within cells. We find that on actin disruption, ribonucleoprotein droplets, including nucleoli and histone locus bodies, undergo gravitational sedimentation and fusion. We develop a model that reveals how gravity becomes an increasingly potent force as cells and their nuclei grow larger than ∼10 μm, explaining the requirement for a stabilizing nuclear F-actin scaffold in large Xenopus oocytes. All life forms are subject to gravity, and our results may have broad implications for cell growth and size control.
The size of a typical eukaryotic cell is of the order of ∼10 μm. However, some cell types grow to very large sizes, including oocytes (immature eggs) of organisms from humans to starfish. For example, oocytes of the frog Xenopus laevis grow to a diameter ≥1 mm. They have a correspondingly large nucleus (germinal vesicle) of ∼450 μm in diameter, which is similar to smaller somatic nuclei, but contains a significantly higher concentration of actin. The form and structure of this nuclear actin remain controversial, and its potential mechanical role within these large nuclei is unknown. Here, we use a microrheology and quantitative imaging approach to show that germinal vesicles contain an elastic F-actin scaffold that mechanically stabilizes these large nuclei against gravitational forces, which are usually considered negligible within cells. We find that on actin disruption, ribonucleoprotein droplets, including nucleoli and histone locus bodies, undergo gravitational sedimentation and fusion. We develop a model that reveals how gravity becomes an increasingly potent force as cells and their nuclei grow larger than ∼10 μm, explaining the requirement for a stabilizing nuclear F-actin scaffold in large Xenopus oocytes. All life forms are subject to gravity, and our results may have broad implications for cell growth and size control.The size of a typical eukaryotic cell is of the order of ∼10 μm. However, some cell types grow to very large sizes, including oocytes (immature eggs) of organisms from humans to starfish. For example, oocytes of the frog Xenopus laevis grow to a diameter ≥1 mm. They have a correspondingly large nucleus (germinal vesicle) of ∼450 μm in diameter, which is similar to smaller somatic nuclei, but contains a significantly higher concentration of actin. The form and structure of this nuclear actin remain controversial, and its potential mechanical role within these large nuclei is unknown. Here, we use a microrheology and quantitative imaging approach to show that germinal vesicles contain an elastic F-actin scaffold that mechanically stabilizes these large nuclei against gravitational forces, which are usually considered negligible within cells. We find that on actin disruption, ribonucleoprotein droplets, including nucleoli and histone locus bodies, undergo gravitational sedimentation and fusion. We develop a model that reveals how gravity becomes an increasingly potent force as cells and their nuclei grow larger than ∼10 μm, explaining the requirement for a stabilizing nuclear F-actin scaffold in large Xenopus oocytes. All life forms are subject to gravity, and our results may have broad implications for cell growth and size control.
Actin is abundant in the nuclei of oocytes but its role has been unclear. Feric and Brangwynne find that actin forms a network that prevents the sedimentation of RNA and protein bodies caused by gravitational forces. The size of a typical eukaryotic cell is of the order of ∼10 μm. However, some cell types grow to very large sizes, including oocytes (immature eggs) of organisms from humans to starfish. For example, oocytes of the frog Xenopus laevis grow to a diameter ≥1 mm. They have a correspondingly large nucleus (germinal vesicle) of ∼450 μm in diameter, which is similar to smaller somatic nuclei, but contains a significantly higher concentration of actin. The form and structure of this nuclear actin remain controversial, and its potential mechanical role within these large nuclei is unknown. Here, we use a microrheology and quantitative imaging approach to show that germinal vesicles contain an elastic F-actin scaffold that mechanically stabilizes these large nuclei against gravitational forces, which are usually considered negligible within cells. We find that on actin disruption, ribonucleoprotein droplets, including nucleoli and histone locus bodies, undergo gravitational sedimentation and fusion. We develop a model that reveals how gravity becomes an increasingly potent force as cells and their nuclei grow larger than ∼10 μm, explaining the requirement for a stabilizing nuclear F-actin scaffold in large Xenopus oocytes. All life forms are subject to gravity, and our results may have broad implications for cell growth and size control.
The size of a typical eukaryotic cell is of the order of ~10 µm. However, some cell types grow to very large sizes, including oocytes (immature eggs) of organisms from humans to starfish. For example, oocytes of the frog Xenopus laevis grow to a diameter [greater than or equal to] 1 mm. They have a correspondingly large nucleus (germinal vesicle) of ~450 µm in diameter, which is similar to smaller somatic nuclei, but contains a significantly higher concentration of actin. The form and structure of this nuclear actin remain controversial, and its potential mechanical role within these large nuclei is unknown. Here, we use a microrheology and quantitative imaging approach to show that germinal vesicles contain an elastic F-actin scaffold that mechanically stabilizes these large nuclei against gravitational forces, which are usually considered negligible within cells. We find that on actin disruption, ribonucleoprotein droplets, including nucleoli and histone locus bodies, undergo gravitational sedimentation and fusion. We develop a model that reveals how gravity becomes an increasingly potent force as cells and their nuclei grow larger than ~10 µm, explaining the requirement for a stabilizing nuclear F-actin scaffold in large Xenopus oocytes. All life forms are subject to gravity, and our results may have broad implications for cell growth and size control.
The size of a typical eukaryotic cell is of the order of 10μm. However, some cell types grow to very large sizes, including oocytes (immature eggs) of organisms from humans to starfish. For example, oocytes of the frog Xenopus laevis grow to a diameter ≥1mm. They have a correspondingly large nucleus (germinal vesicle) of 450μm in diameter, which is similar to smaller somatic nuclei, but contains a significantly higher concentration of actin. The form and structure of this nuclear actin remain controversial, and its potential mechanical role within these large nuclei is unknown. Here, we use a microrheology and quantitative imaging approach to show that germinal vesicles contain an elastic F-actin scaffold that mechanically stabilizes these large nuclei against gravitational forces, which are usually considered negligible within cells. We find that on actin disruption, ribonucleoprotein droplets, including nucleoli and histone locus bodies, undergo gravitational sedimentation and fusion. We develop a model that reveals how gravity becomes an increasingly potent force as cells and their nuclei grow larger than 10μm, explaining the requirement for a stabilizing nuclear F-actin scaffold in large Xenopus oocytes. All life forms are subject to gravity, and our results may have broad implications for cell growth and size control.
Audience Academic
Author Brangwynne, Clifford P.
Feric, Marina
Author_xml – sequence: 1
  givenname: Marina
  surname: Feric
  fullname: Feric, Marina
  organization: Department of Chemical and Biological Engineering, Princeton University
– sequence: 2
  givenname: Clifford P.
  surname: Brangwynne
  fullname: Brangwynne, Clifford P.
  email: cbrangwy@princeton.edu
  organization: Department of Chemical and Biological Engineering, Princeton University
BackLink https://www.ncbi.nlm.nih.gov/pubmed/23995731$$D View this record in MEDLINE/PubMed
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Snippet Actin is abundant in the nuclei of oocytes but its role has been unclear. Feric and Brangwynne find that actin forms a network that prevents the sedimentation...
The size of a typical eukaryotic cell is of the order of ∼10 μm. However, some cell types grow to very large sizes, including oocytes (immature eggs) of...
The size of a typical eukaryotic cell is of the order of ~10 µm. However, some cell types grow to very large sizes, including oocytes (immature eggs) of...
The size of a typical eukaryotic cell is of the order of 10μm. However, some cell types grow to very large sizes, including oocytes (immature eggs) of...
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StartPage 1253
SubjectTerms 631/136/2434/1706
631/80/128/1276
Actin
Actins - metabolism
Amphibians
Animals
Brownian motion
Cancer Research
Cell Biology
Cell Nucleus - metabolism
Cell Size
Cells
Developmental Biology
Eggs
Female
Gravitation
Humans
letter
Life Sciences
Microscopy, Confocal
Models, Biological
Nuclear Matrix - metabolism
Oocytes - cytology
Oocytes - growth & development
Oocytes - metabolism
Physiological aspects
Ribonucleoproteins
Ribonucleoproteins - metabolism
Stem Cells
Xenopus - metabolism
Title A nuclear F-actin scaffold stabilizes ribonucleoprotein droplets against gravity in large cells
URI https://link.springer.com/article/10.1038/ncb2830
https://www.ncbi.nlm.nih.gov/pubmed/23995731
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Volume 15
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