Abstract

In understanding how a radially symmetrical actin cytoskeleton spontaneously evolves into a chiral system, here we construct a torsional clutch-filament model for one radial fiber. The model analysis indicates that when actin filaments in growth tend to actively drive the radial fiber to only rotate counter-clockwise, certain amount of passive elastic energy also builds up within the radial fiber upon filament growth, the release of which tends to drive it to rotate clockwise. The competition between these two sources would eventually determine the cellular swirling direction, which can be counter-clockwise or clockwise. The model prediction is in consistency with recent experimental findings. This work provides understanding into how the cellular chirality can be modulated by varied molecular components associated with the cytoskeleton.

References

1.
Levin
,
M.
,
2005
, “
Left-Right Asymmetry in Embryonic Development: A Comprehensive Review
,”
Mech. Dev.
,
122
(
1
), pp.
3
25
. 10.1016/j.mod.2004.08.006
2.
Roychoudhuri
,
R.
,
Putcha
,
V.
, and
Moller
,
H.
,
2006
, “
Cancer and Laterality: A Study of the Five Major Paired Organs (UK)
,”
Cancer Causes Control
,
17
(
5
), pp.
655
662
. 10.1007/s10552-005-0615-9
3.
Paulozzi
,
L. J.
, and
Lary
,
J. M.
,
1999
, “
Laterality Patterns in Infants With External Birth Defects
,”
Teratology
,
60
(
5
), pp.
265
271
. 10.1002/(SICI)1096-9926(199911)60:5<265::AID-TERA7>3.0.CO;2-H
4.
Naganathan
,
S. R.
,
Middelkoop
,
T. C.
,
Furthauer
,
S.
, and
Grill
,
S. W.
,
2016
, “
Actomyosin-Driven Left-Right Asymmetry: From Molecular Torques to Chiral Self Organization
,”
Curr. Opin. Cell Biol.
,
38
, pp.
24
30
. 10.1016/j.ceb.2016.01.004
5.
Heacock
,
A. M.
, and
Agranoff
,
B. W.
,
1977
, “
Clockwise Growth of Neurites From Retinal Explants
,”
Science
,
198
(
4312
), pp.
64
66
. 10.1126/science.897684
6.
Tamada
,
A.
,
Kawase
,
S.
,
Murakami
,
F.
, and
Kamiguchi
,
H.
,
2010
, “
Autonomous Right-Screw Rotation of Growth Cone Filopodia Drives Neurite Turning
,”
J. Cell Biol.
,
188
(
3
), pp.
429
441
. 10.1083/jcb.200906043
7.
Wan
,
L. Q.
,
Ronaldson
,
K.
,
Park
,
M.
,
Taylor
,
G.
,
Zhang
,
Y.
,
Gimble
,
J. M.
, and
Vunjak-Novakovic
,
G.
,
2011
, “
Micropatterned Mammalian Cells Exhibit Phenotype-Specific Left-Right Asymmetry
,”
Proc. Natl. Acad. Sci. USA
,
108
(
30
), pp.
12295
12300
. 10.1073/pnas.1103834108
8.
Worley
,
K. E.
,
Shieh
,
D.
, and
Wan
,
L. Q.
,
2015
, “
Inhibition of Cell-Cell Adhesion Impairs Directional Epithelial Migration on Micropatterned Surfaces
,”
Integr. Biol.
,
7
(
5
), pp.
580
590
. 10.1039/c5ib00073d
9.
Tee
,
Y. H.
,
Shemesh
,
T.
,
Thiagarajan
,
V.
,
Hariadi
,
R. F.
,
Anderson
,
K. L.
,
Page
,
C.
,
Volkmann
,
N.
,
Hanein
,
D.
,
Sivaramakrishnan
,
S.
,
Kozlov
,
M. M.
, and
Bershadsky
,
A. D.
,
2015
, “
Cellular Chirality Arising From the Self-Organization of the Actin Cytoskeleton
,”
Nat. Cell Biol.
,
17
(
4
), pp.
445
457
. 10.1038/ncb3137
10.
Lebreton
,
G.
,
Geminard
,
C.
,
Lapraz
,
F.
,
Pyrpassopoulos
,
S.
,
Cerezo
,
D.
,
Speder
,
P.
,
Ostap
,
E. M.
, and
Noselli
,
S.
,
2018
, “
Molecular to Organismal Chirality is Induced by the Conserved Myosin 1D
,”
Science
,
362
(
6417
), pp.
949
952
. 10.1126/science.aat8642
11.
Jalal
,
S.
,
Shi
,
S. D.
,
Acharya
,
V.
,
Huang
,
R. Y. J.
,
Viasnoff
,
V.
,
Bershadsky
,
A. D.
, and
Tee
,
Y. H.
,
2019
, “
Actin Cytoskeleton Self-Organization in Single Epithelial Cells and Fibroblasts Under Isotropic Confinement
,”
J. Cell Sci.
,
132
(
5
), p.
14
. 10.1242/jcs.220780
12.
Inaki
,
M.
,
Liu
,
J. Y.
, and
Matsuno
,
K.
,
2016
, “
Cell Chirality: Its Origin and Roles in Left-Right Asymmetric Development
,”
Philos. Trans. R. Soc. B Biol. Sci.
,
371
(
1710
), p.
9
. 10.1098/rstb.2015.0403
13.
Inaki
,
M.
,
Sasamura
,
T.
, and
Matsuno
,
K.
,
2018
, “
Cell Chirality Drives Left-Right Asymmetric Morphogenesis
,”
Front. Cell. Dev. Biol.
,
6
, p.
9
. 10.3389/fcell.2018.00034
14.
Shemesh
,
T.
,
Otomo
,
T.
,
Rosen
,
M. K.
,
Bershadsky
,
A. D.
, and
Kozlov
,
M. M.
,
2005
, “
A Novel Mechanism of Actin Filament Processive Capping by Formin: Solution of the Rotation Paradox
,”
J. Cell Biol.
,
170
(
6
), pp.
889
893
. 10.1083/jcb.200504156
15.
Mitchison
,
T.
, and
Kirschner
,
M.
,
1988
, “
Cytoskeletal Dynamics and Nerve Growth
,”
Neuron
,
1
(
9
), pp.
761
772
. 10.1016/0896-6273(88)90124-9
16.
Chan
,
C. E.
, and
Odde
,
D. J.
,
2008
, “
Traction Dynamics of Filopodia on Compliant Substrates
,”
Science
,
322
(
5908
), pp.
1687
1691
. 10.1126/science.1163595
17.
Elosegui-Artola
,
A.
,
Oria
,
R.
,
Chen
,
Y. F.
,
Kosmalska
,
A.
,
Perez-Gonzalez
,
C.
,
Castro
,
N.
,
Zhu
,
C.
,
Trepat
,
X.
, and
Roca-Cusachs
,
P.
,
2016
, “
Mechanical Regulation of a Molecular Clutch Defines Force Transmission and Transduction in Response to Matrix Rigidity
,”
Nat. Cell Biol.
,
18
(
5
), pp.
540
548
. 10.1038/ncb3336
18.
Paul
,
A. S.
, and
Pollard
,
T. D.
,
2009
, “
Review of the Mechanism of Processive Actin Filament Elongation by Formins
,”
Cell Motil. Cytoskeleton
,
66
(
8
), pp.
606
617
. 10.1002/cm.20379
19.
Breitsprecher
,
D.
, and
Goode
,
B. L.
,
2013
, “
Formins at a Glance
,”
J. Cell Sci.
,
126
(
1
), pp.
1
7
. 10.1242/jcs.107250
20.
Ma
,
R.
, and
Berro
,
J.
,
2018
, “
Structural Organization and Energy Storage in Crosslinked Actin Assemblies
,”
PLoS Comput. Biol.
,
14
(
5
), p.
25
. 10.1371/journal.pcbi.1006150
21.
Burnette
,
D. T.
,
Manley
,
S.
,
Sengupta
,
P.
,
Sougrat
,
R.
,
Davidson
,
M. W.
,
Kachar
,
B.
, and
Lippincott-Schwartz
,
J.
,
2011
, “
A Role for Actin Arcs in the Leading-Edge Advance of Migrating Cells
,”
Nat. Cell Biol.
,
13
(
4
), pp.
371
381
. 10.1038/ncb2205
22.
Hotulainen
,
P.
, and
Lappalainen
,
P.
,
2006
, “
Stress Fibers are Generated by Two Distinct Actin Assembly Mechanisms in Motile Cells
,”
J. Cell Biol.
,
173
(
3
), pp.
383
394
. 10.1083/jcb.200511093
23.
Bell
,
G. I.
,
1978
, “
Models for Specific Adhesion of Cells to Cells
,”
Science
,
200
(
4342
), pp.
618
627
. 10.1126/science.347575
24.
Holmes
,
K. C.
,
Popp
,
D.
,
Gebhard
,
W.
, and
Kabsch
,
W.
,
1990
, “
Atomic Model of the Actin Filament
,”
Nature
,
347
(
6288
), pp.
44
49
. 10.1038/347044a0
25.
Kabsch
,
W.
,
Mannherz
,
H. G.
,
Suck
,
D.
,
Pai
,
E. F.
, and
Holmes
,
K. C.
,
1990
, “
Atomic-Structure of the Actin-Dnase-I Complex
,”
Nature
,
347
(
6288
), pp.
37
44
. 10.1038/347037a0
26.
Yu
,
M.
,
Le
,
S. M.
,
Efremov
,
A. K.
,
Zeng
,
X. J.
,
Bershadsky
,
A.
, and
Yan
,
J.
,
2018
, “
Effects of Mechanical Stimuli on Profilin- and Formin-Mediated Actin Polymerization
,”
Nano Lett.
,
18
(
8
), pp.
5239
5247
. 10.1021/acs.nanolett.8b02211
27.
Gillespie
,
D. T.
,
1976
, “
General Method for Numerically Simulating Stochastic Time Evolution of Coupled Chemical Reactions
,”
J. Comput. Phys.
,
22
(
4
), pp.
403
434
. 10.1016/0021-9991(76)90041-3
28.
Gillespie
,
D. T.
,
1977
, “
Exact Stochastic Simulation of Coupled Chemical Reactions
,”
J. Phys. Chem.
,
81
(
25
), pp.
2340
2361
. 10.1021/j100540a008
29.
Evans
,
E. A.
, and
Calderwood
,
D. A.
,
2007
, “
Forces and Bond Dynamics in Cell Adhesion
,”
Science
,
316
(
5828
), pp.
1148
1153
. 10.1126/science.1137592
30.
Harada
,
R.
,
Sugita
,
Y.
, and
Feig
,
M.
,
2012
, “
Protein Crowding Affects Hydration Structure and Dynamics
,”
J. Am. Chem. Soc.
,
134
(
10
), pp.
4842
4849
. 10.1021/ja211115q
31.
Michaelis
,
L.
, and
Menten
,
M. L.
,
1913
, “
The Kinetics of the Inversion Effect
,”
Biochem. Z.
,
49
, pp.
333
369
.
32.
Higashida
,
C.
,
Suetsugu
,
S.
,
Tsuji
,
T.
,
Monypenny
,
J.
,
Narumiya
,
S.
, and
Watanabe
,
N.
,
2008
, “
G-actin Regulates Rapid Induction of Actin Nucleation by mDia1 to Restore Cellular Actin Polymers
,”
J. Cell Sci.
,
121
(
20
), pp.
3403
3412
. 10.1242/jcs.030940
33.
Chen
,
B.
,
2013
, “
Self-Regulation of Motor Force Through Chemomechanical Coupling in Skeletal Muscle Contraction
,”
ASME J. Appl. Mech.
,
80
(
5
), p.
051013
. 10.1115/1.4023680
34.
Chen
,
B.
,
2014
, “
Probing the Effect of Random Adhesion Energy on Receptor-Mediated Endocytosis With a Semistochastic Model
,”
ASME J. Appl. Mech.
,
81
(
8
), p.
081013
. 10.1115/1.4027739
35.
Chen
,
X. F.
, and
Chen
,
B.
,
2014
, “
Probing the Instability of a Cluster of Slip Bonds Upon Cyclic Loads With a Coupled Finite Element Analysis and Monte Carlo Method
,”
ASME J. Appl. Mech.
,
81
(
11
), p.
111002
. 10.1115/1.4028437
36.
Chen
,
X. F.
, and
Chen
,
B.
,
2016
, “
Simplified Analysis for the Association of a Constrained Receptor to an Oscillating Ligand
,”
ASME J. Appl. Mech.
,
83
(
9
), p.
091006
. 10.1115/1.4033891
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