Persistent and polarized global actin flow is essential for directionality during cell migration

Lawrence Yolland; Mubarik Burki; Stefania Marcotti; Andrei Luchici; Fiona N. Kenny; John Robert Davis; Eduardo Serna-Morales; Jan Müller; Michael Sixt; Andrew  Davidson; Will Wood; Linus J. Schumacher; Robert G. Endres; Mark  Miodownik; Brian M. Stramer

doi:10.1038/s41556-019-0411-5

Persistent and polarized global actin flow is essential for directionality during cell migration

Lawrence Yolland, Mubarik Burki, Stefania Marcotti, Andrei Luchici, Fiona N. Kenny, John Robert Davis, Eduardo Serna-Morales, Jan Müller, Michael Sixt, Andrew Davidson, Will Wood, Linus J. Schumacher, Robert G. Endres, Mark Miodownik, Brian M. Stramer

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Abstract

Cell migration is hypothesized to involve a cycle of behaviours beginning with leading edge extension. However, recent evidence suggests that the leading edge may be dispensable for migration, raising the question of what actually controls cell directionality. Here, we exploit the embryonic migration of Drosophila macrophages to bridge the different temporal scales of the behaviours controlling motility. This approach reveals that edge fluctuations during random motility are not persistent and are weakly correlated with motion. In contrast, flow of the actin network behind the leading edge is highly persistent. Quantification of actin flow structure during migration reveals a stable organization and asymmetry in the cell-wide flowfield that strongly correlates with cell directionality. This organization is regulated by a gradient of actin network compression and destruction, which is controlled by myosin contraction and cofilin-mediated disassembly. It is this stable actin-flow polarity, which integrates rapid fluctuations of the leading edge, that controls inherent cellular persistence.

Original language	English
Pages (from-to)	1370–1381
Number of pages	12
Journal	Nature Cell Biology
Volume	21
Issue number	11
Early online date	4 Nov 2019
DOIs	https://doi.org/10.1038/s41556-019-0411-5
Publication status	Published - Nov 2019

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Persistent and polarized global_YOLLAND_Accepted4November2019_GREEN AAMAccepted author manuscript, 84.6 MB

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Yolland, L., Burki, M., Marcotti, S., Luchici, A., Kenny, F. N., Davis, J. R., Serna-Morales, E., Müller, J., Sixt, M., Davidson, A., Wood, W., Schumacher, L. J., Endres, R. G., Miodownik, M., & Stramer, B. M. (2019). Persistent and polarized global actin flow is essential for directionality during cell migration. Nature Cell Biology, 21(11), 1370–1381. https://doi.org/10.1038/s41556-019-0411-5

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title = "Persistent and polarized global actin flow is essential for directionality during cell migration",

abstract = "Cell migration is hypothesized to involve a cycle of behaviours beginning with leading edge extension. However, recent evidence suggests that the leading edge may be dispensable for migration, raising the question of what actually controls cell directionality. Here, we exploit the embryonic migration of Drosophila macrophages to bridge the different temporal scales of the behaviours controlling motility. This approach reveals that edge fluctuations during random motility are not persistent and are weakly correlated with motion. In contrast, flow of the actin network behind the leading edge is highly persistent. Quantification of actin flow structure during migration reveals a stable organization and asymmetry in the cell-wide flowfield that strongly correlates with cell directionality. This organization is regulated by a gradient of actin network compression and destruction, which is controlled by myosin contraction and cofilin-mediated disassembly. It is this stable actin-flow polarity, which integrates rapid fluctuations of the leading edge, that controls inherent cellular persistence.",

author = "Lawrence Yolland and Mubarik Burki and Stefania Marcotti and Andrei Luchici and Kenny, {Fiona N.} and Davis, {John Robert} and Eduardo Serna-Morales and Jan M{\"u}ller and Michael Sixt and Andrew Davidson and Will Wood and Schumacher, {Linus J.} and Endres, {Robert G.} and Mark Miodownik and Stramer, {Brian M.}",

year = "2019",

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doi = "10.1038/s41556-019-0411-5",

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volume = "21",

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Yolland, L, Burki, M , Marcotti, S, Luchici, A, Kenny, FN , Davis, JR , Serna-Morales, E, Müller, J, Sixt, M, Davidson, A, Wood, W, Schumacher, LJ, Endres, RG, Miodownik, M & Stramer, BM 2019, 'Persistent and polarized global actin flow is essential for directionality during cell migration', Nature Cell Biology, vol. 21, no. 11, pp. 1370–1381. https://doi.org/10.1038/s41556-019-0411-5

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T1 - Persistent and polarized global actin flow is essential for directionality during cell migration

AU - Yolland, Lawrence

AU - Burki, Mubarik

AU - Marcotti, Stefania

AU - Luchici, Andrei

AU - Kenny, Fiona N.

AU - Davis, John Robert

AU - Serna-Morales, Eduardo

AU - Müller, Jan

AU - Sixt, Michael

AU - Davidson, Andrew

AU - Wood, Will

AU - Schumacher, Linus J.

AU - Endres, Robert G.

AU - Miodownik, Mark

AU - Stramer, Brian M.

PY - 2019/11

Y1 - 2019/11

N2 - Cell migration is hypothesized to involve a cycle of behaviours beginning with leading edge extension. However, recent evidence suggests that the leading edge may be dispensable for migration, raising the question of what actually controls cell directionality. Here, we exploit the embryonic migration of Drosophila macrophages to bridge the different temporal scales of the behaviours controlling motility. This approach reveals that edge fluctuations during random motility are not persistent and are weakly correlated with motion. In contrast, flow of the actin network behind the leading edge is highly persistent. Quantification of actin flow structure during migration reveals a stable organization and asymmetry in the cell-wide flowfield that strongly correlates with cell directionality. This organization is regulated by a gradient of actin network compression and destruction, which is controlled by myosin contraction and cofilin-mediated disassembly. It is this stable actin-flow polarity, which integrates rapid fluctuations of the leading edge, that controls inherent cellular persistence.

AB - Cell migration is hypothesized to involve a cycle of behaviours beginning with leading edge extension. However, recent evidence suggests that the leading edge may be dispensable for migration, raising the question of what actually controls cell directionality. Here, we exploit the embryonic migration of Drosophila macrophages to bridge the different temporal scales of the behaviours controlling motility. This approach reveals that edge fluctuations during random motility are not persistent and are weakly correlated with motion. In contrast, flow of the actin network behind the leading edge is highly persistent. Quantification of actin flow structure during migration reveals a stable organization and asymmetry in the cell-wide flowfield that strongly correlates with cell directionality. This organization is regulated by a gradient of actin network compression and destruction, which is controlled by myosin contraction and cofilin-mediated disassembly. It is this stable actin-flow polarity, which integrates rapid fluctuations of the leading edge, that controls inherent cellular persistence.

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JO - Nature Cell Biology

JF - Nature Cell Biology

IS - 11

ER -

Persistent and polarized global actin flow is essential for directionality during cell migration

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