Actin cables and comet tails organize mitochondrial networks in mitosis

Andrew S. Moore, Stephen M. Coscia, Cory L. Simpson, Fabian E. Ortega, Eric C. Wait, John M. Heddleston, Jeffrey J. Nirschl, Christopher J. Obara, Pedro Guedes-Dias, C. Alexander Boecker, Teng-Leong Chew, Julie A. Theriot, Jennifer Lippincott-Schwartz and Erika L. F. Holzbaur ()
Additional contact information
Andrew S. Moore: University of Pennsylvania Perelman School of Medicine
Stephen M. Coscia: University of Pennsylvania Perelman School of Medicine
Cory L. Simpson: University of Pennsylvania Perelman School of Medicine
Fabian E. Ortega: Stanford University
Eric C. Wait: Howard Hughes Medical Institute, Janelia Research Campus
John M. Heddleston: Howard Hughes Medical Institute, Janelia Research Campus
Jeffrey J. Nirschl: University of Pennsylvania Perelman School of Medicine
Christopher J. Obara: Howard Hughes Medical Institute, Janelia Research Campus
Pedro Guedes-Dias: University of Pennsylvania Perelman School of Medicine
C. Alexander Boecker: University of Pennsylvania Perelman School of Medicine
Teng-Leong Chew: Howard Hughes Medical Institute, Janelia Research Campus
Julie A. Theriot: University of Washington
Jennifer Lippincott-Schwartz: Howard Hughes Medical Institute, Janelia Research Campus
Erika L. F. Holzbaur: University of Pennsylvania Perelman School of Medicine

Nature, 2021, vol. 591, issue 7851, 659-664

Abstract: Abstract Symmetric cell division requires the even partitioning of genetic information and cytoplasmic contents between daughter cells. Whereas the mechanisms coordinating the segregation of the genome are well known, the processes that ensure organelle segregation between daughter cells remain less well understood1. Here we identify multiple actin assemblies with distinct but complementary roles in mitochondrial organization and inheritance in mitosis. First, we find a dense meshwork of subcortical actin cables assembled throughout the mitotic cytoplasm. This network scaffolds the endoplasmic reticulum and organizes three-dimensional mitochondrial positioning to ensure the equal segregation of mitochondrial mass at cytokinesis. Second, we identify a dynamic wave of actin filaments reversibly assembling on the surface of mitochondria during mitosis. Mitochondria sampled by this wave are enveloped within actin clouds that can spontaneously break symmetry to form elongated comet tails. Mitochondrial comet tails promote randomly directed bursts of movement that shuffle mitochondrial position within the mother cell to randomize inheritance of healthy and damaged mitochondria between daughter cells. Thus, parallel mechanisms mediated by the actin cytoskeleton ensure both equal and random inheritance of mitochondria in symmetrically dividing cells.

Date: 2021
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DOI: 10.1038/s41586-021-03309-5

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