Cytoskeletal symmetry breaking and chirality: From reconstituted systems to animal development

Symmetry

Volumn 7, Issue 4, 2015, Pages 2062-2107

  Pohl, Christian ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

Actin; C. elegans; Cell division; Chirality; Drosophila; Embryogenesis; Microtubules; Myosin; Polarity; Spindle; Symmetry breaking

Indexed keywords

EID: 84952837122     PISSN: None     EISSN: 20738994     Source Type: Journal    
DOI: 10.3390/sym7042062     Document Type: Review

References (310)

1. Li, R.; Bowerman, B. Symmetry breaking in biology. Cold Spring Harb. Perspect. Biol. 2010, 2, doi:10.1101/cshperspect.a003475.
2. Wodarz, A. Establishing cell polarity in development. Nat. Cell Biol. 2002, 4, E39-E44.
3. Meinhardt, H. Models for the generation and interpretation of gradients. Cold Spring Harb. Perspect. Biol. 2009, 1, doi:10.1101/cshperspect.a001362.
4. Meinhardt, H. Models of biological pattern formation: From elementary steps to the organization of embryonic axes. Curr. Top. Dev. Biol. 2008, 81, 1-63.
5. Nance, J.; Zallen, J.A. Elaborating polarity: PAR proteins and the cytoskeleton. Development 2011, 138, 799-809.
6. Howell, A.S.; Savage, N.S.; Johnson, S.A.; Bose, I.; Wagner, A.W.; Zyla, T.R.; Nijhout, H.F.; Reed, M.C.; Goryachev, A.B.; Lew, D.J. Singularity in polarization: Rewiring yeast cells to make two buds. Cell 2009, 139, 731-743.
7. Li, R.; Gundersen, G.G. Beyond polymer polarity: How the cytoskeleton builds a polarized cell. Nat. Rev. Mol. Cell Biol. 2008, 9, 860-873.
8. Cowan, C.R.; Hyman, A.A. Acto-myosin reorganization and PAR polarity in C. elegans. Development 2007, 134, 1035-1043.
9. Van Amerongen, R.; Nusse, R. Towards an integrated view of Wnt signaling in development. Development 2009, 136, 3205-3214.
10. Greenwald, I. Notch and the awesome power of genetics. Genetics 2012, 191, 655-669.
11. Wedlich-Söldner, R.; Altschuler, S.; Wu, L.; Li, R. Spontaneous cell polarization through actomyosin-based delivery of the Cdc42 GTPase. Science 2003, 299, 1231-1235.
12. Bi, E.; Park, H.O. Cell polarization and cytokinesis in budding yeast. Genetics 2012, 191, 347-387.
13. Mayer, M.; Depken, M.; Bois, J.S.; Jülicher, F.; Grill, S.W. Anisotropies in cortical tension reveal the physical basis of polarizing cortical flows. Nature 2010, 467, 617-621.
14. Munro, E.; Nance, J.; Priess, J.R. Cortical flows powered by asymmetrical contraction transport PAR proteins to establish and maintain anterior-posterior polarity in the early C. elegans embryo. Dev. Cell 2004, 7, 413-424.
15. Jenkins, N.; Saam, J.R.; Mango, S.E. CYK-4/GAP provides a localized cue to initiate anteroposterior polarity upon fertilization. Science 2006, 313, 1298-1301.
16. Goehring, N.W.; Trong, P.K.; Bois, J.S.; Chowdhury, D.; Nicola, E.M.; Hyman, A.A.; Grill, S.W. Polarization of PAR proteins by advective triggering of a pattern-forming system. Science 2011, 334, 1137-1141.
17. Paré, A.C.; Vichas, A.; Fincher, C.T.; Mirman, Z.; Farrell, D.L.; Mainieri, A.; Zallen, J.A. A positional Toll receptor code directs convergent extension in Drosophila. Nature 2014, 515, 523-527.
18. Ruprecht, V.; Wieser, S.; Callan-Jones, A.; Smutny, M.; Morita, H.; Sako, K.; Barone, V.; Ritsch-Marte, M.; Sixt, M.; Voituriez, R.; et al. Cortical contractility triggers a stochastic switch to fast amoeboid cell motility. Cell 2015, 160, 673-685.
19. Hashimoto, M.; Shinohara, K.; Wang, J.; Ikeuchi, S.; Yoshiba, S.; Meno, C.; Nonaka, S.; Takada, S.; Hatta, K.; Wynshaw-Boris, A.; et al. Planar polarization of node cells determines the rotational axis of node cilia. Nat. Cell Biol. 2010, 12, 170-176.
20. Borovina, A.; Superina, S.; Voskas, D.; Ciruna, B. Vangl2 directs the posterior tilting and asymmetric localization of motile primary cilia. Nat. Cell Biol. 2010, 12, 407-412.
21. Van der Gucht, J.; Sykes, C. Physical model of cellular symmetry breaking. Cold Spring Harb. Perspect. Biol. 2009, 1, doi:10.1101/cshperspect.a001909.
22. Lancaster, M.A.; Knoblich, J.A. Organogenesis in a dish: Modeling development and disease using organoid technologies. Science 2014, 345, doi:10.1126/science.1247125.
23. Turing, A.M. The chemical basis of morphogenesis. Philosoph. Trans. R. Soc. Lond. 1952, 237, 37-72.
24. Ladewig, J.; Koch, P.; Brüstle, O. Leveling Waddington: The emergence of direct programming and the loss of cell fate hierarchies. Nat. Rev. Mol. Cell Biol. 2013, 14, 225-236.
25. Fievet, B.T.; Rodriguez, J.; Naganathan, S.; Lee, C.; Zeiser, E.; Ishidate, T.; Shirayama, M.; Grill, S.; Ahringer, J. Systematic genetic interaction screens uncover cell polarity regulators and functional redundancy. Nat. Cell Biol. 2013, 15, 103-112.
26. Motegi, F.; Seydoux, G. The PAR network: Redundancy and robustness in a symmetry-breaking system. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2013, 368, doi:10.1098/rstb.2013.0010.
27. Mitchison, T.; Kirschner, M. Dynamic instability of microtubule growth. Nature 1984, 312, 237-242.
28. Mitchison, T.; Kirschner, M. Microtubule assembly nucleated by isolated centrosomes. Nature 1984, 312, 232-237.
29. Kirschner, M.; Mitchison, T. Beyond self-assembly: From microtubules to morphogenesis. Cell 1986, 45, 329-342.
30. Padinhateeri, R.; Kolomeisky, A.B.; Lacoste, D. Random hydrolysis controls the dynamic instability of microtubules. Biophys. J. 2012, 102, 1274-1283.
31. Bayley, P.M.; Schilstra, M.J.; Martin, S.R. A simple formulation of microtubule dynamics: Quantitative implications of the dynamic instability of microtubule populations in vivo and in vitro. J. Cell Sci. 1989, 93, 241-254.
32. Dogterom, M.; Leibler, S. Physical aspects of the growth and regulation of microtubule structures. Phys. Rev. Lett. 1993, 70, 1347-1350.
33. Flyvbjerg, H.; Holy, T.E.; Leibler, S. Stochastic dynamics of microtubules: A model for caps and catastrophes. Phys. Rev. Lett. 1994, 73, 2372-2375.
34. Margolin, G.; Gregoretti, I.V.; Goodson, H.V.; Alber, M.S. Analysis of a mesoscopic stochastic model of microtubule dynamic instability. Phys. Rev. E Stat. Nonliner Soft Matter Phys. 2006, 74, doi:10.1103/PhysRevE.74.041920.
35. Zong, C.; Lu, T.; Shen, T.; Wolynes, P.G. Nonequilibrium self-assembly of linear fibers: Microscopic treatment of growth, decay, catastrophe and rescue. Phys. Biol. 2006, 3, 83-92.
36. Antal, T.; Krapivsky, P.L.; Redner, S.; Mailman, M.; Chakraborty, B. Dynamics of an idealized model of microtubule growth and catastrophe. Phys. Rev. E Stat. Nonliner Soft Matter Phys. 2007, 76, doi:10.1103/PhysRevE.76.041907.
37. Ranjith, P.; Lacoste, D.; Mallick, K.; Joanny, J.F. Nonequilibrium self-assembly of a filament coupled to ATP/GTP hydrolysis. Biophys. J. 2009, 96, 2146-2159.
38. Kueh, H.Y.; Mitchison, T.J. Structural plasticity in actin and tubulin polymer dynamics. Science 2009, 325, 960-963.
39. Wang, H.W.; Nogales, E. Nucleotide-dependent bending flexibility of tubulin regulates microtubule assembly. Nature 2005, 435, 911-915.
40. Brouhard, G.J.; Rice, L.M. The contribution of αβ-tubulin curvature to microtubule dynamics. J. Cell Biol. 2014, 207, 323-334.
41. Zhang, R.; Alushin, G.M.; Brown, A.; Nogales, E. Mechanistic origin of microtubule dynamic instability and its modulation by EB proteins. Cell 2015, 162, 849-859.
42. Carlier, M.F.; Melki, R.; Pantaloni, D.; Hill, T.L.; Chen, Y. Synchronous oscillations in microtubule polymerization. Proc. Natl. Acad. Sci. USA 1987, 84, 5257-5261.
43. Pirollet, F.; Job, D.; Margolis, R.L.; Garel, J.R. An oscillatory mode for microtubule assembly. EMBO J. 1987, 6, 3247-3252.
44. Tabony, J.; Job, D. Spatial structures in microtubular solutions requiring a sustained energy source. Nature 1990, 346, 448-451.
45. Mandelkow, E.; Mandelkow, E.M.; Hotani, H.; Hess, B.; Müller, S.C. Spatial patterns from oscillating microtubules. Science 1989, 246, 1291-1293.
46. Buxbaum, R.E.; Dennerll, T.; Weiss, S.; Heidemann, S.R. F-actin and microtubule suspensions as indeterminate fluids. Science 1987, 235, 1511-1514.
47. Tabony, J.; Job, D. Gravitational symmetry breaking in microtubular dissipative structures. Proc. Natl. Acad. Sci. USA 1992, 89, 6948-6952.
48. Papaseit, C.; Pochon, N.; Tabony, J. Microtubule self-organization is gravity-dependent. Proc. Natl. Acad. Sci. USA 2000, 97, 8364-8368.
49. Tuszynski, J.A.; Sataric, M.V.; Portet, S.; Dixon, J.M. Gravitational symmetry breaking leads to a polar liquid crystal phase of microtubules in vitro. J. Biol. Phys. 2005, 31, 477-486.
50. Yokota, H.; Neff, A.W.; Malacinski, G.M. Early development of Xenopus embryos is affected by simulated gravity. Adv. Space Res. 1994, 14, 249-255.
51. Nouri, C.; Tuszynski, J.A.; Wiebe, M.W.; Gordon, R. Simulation of the effects of microtubules in the cortical rotation of amphibian embryos in normal and zero gravity. Biosystems 2012, 109, 444-449.
52. Tabony, J.; Rigotti, N.; Glade, N.; Cortès, S. Effect of weightlessness on colloidal particle transport and segregation in self-organising microtubule preparations. Biophys. Chem. 2007, 127, 172-180.
53. Reber, S.B.; Baumgart, J.; Widlund, P.O.; Pozniakovsky, A.; Howard, J.; Hyman, A.A.; Jülicher, F. XMAP215 activity sets spindle length by controlling the total mass of spindle microtubules. Nat. Cell Biol. 2013, 15, 1116-1122.
54. Brugués, J.; Needleman, D. Physical basis of spindle self-organization. Proc. Natl. Acad. Sci. USA 2014, 111, 18496-18500.
55. Schliwa, M.; Woehlke, G. Molecular motors. Switching on kinesin. Nature 2001, 411, 424-425.
56. Nédélec, F.J.; Surrey, T.; Maggs, A.C.; Leibler, S. Self-organization of microtubules and motors. Nature 1997, 389, 305-308.
57. Surrey, T.; Nedelec, F.; Leibler, S.; Karsenti, E. Physical properties determining self-organization of motors and microtubules. Science 2001, 292, 1167-1171.
58. Nogales, E. An electron microscopy journey in the study of microtubule structure and dynamics. Protein Sci. 2015, doi:10.1002/pro.2808.
59. Millecamps, S.; Julien, J.P. Axonal transport deficits and neurodegenerative disease. Nat. Rev. Neurosci. 2013, 14, 161-176.
60. Sanchez, T.; Chen, D.T.; DeCamp, S.J.; Heymann, M.; Dogic, Z. Spontaneous motion in hierarchically assembled active matter. Nature 2012, 491, 431-434.
61. Keber, F.C.; Loiseau, E.; Sanchez, T.; de Camp, S.J.; Giomi, L.; Bowick, M.J.; Marchetti, M.C.; Dogic, Z.; Bausch, A.R. Topology and dynamics of active nematic vesicles. Science 2014, 345, 1135-1139.
62. Sumino, Y.; Nagai, K.H.; Shitaka, Y.; Tanaka, D.; Yoshikawa, K.; Chaté, H.; Oiwa, K. Large-scale vortex lattice emerging from collectively moving microtubules. Nature 2012, 483, 448-452.
63. Serbus, L.R.; Cha, B.J.; Theurkauf, W.E.; Saxton, W.M. Dynein and the actin cytoskeleton control kinesin-driven cytoplasmic streaming in Drosophila oocytes. Development 2005, 132, 3743-3752.
64. Wasteneys, G.O.; Ambrose, J.C. Spatial organization of plant cortical microtubules: Close encounters of the 2D kind. Trends Cell Biol. 2009, 19, 62-71.
65. Sanchez, T.; Welch, D.; Nicastro, D.; Dogic, Z. Cilia-like beating of active microtubule bundles. Science 2011, 333, 456-459.
66. Dotti, C.G.; Banker, G.A. Experimentally induced alteration in the polarity of developing neurons. Nature 1987, 330, 254-256.
67. Forscher, P.; Smith, S.J. Actions of cytochalasins on the organization of actin filaments and microtubules in a neuronal growth cone. J. Cell Biol. 1988, 107, 1505-1516.
68. Andersen, S.S.; Bi, G.Q. Axon formation: A molecular model for the generation of neuronal polarity. Bioessays 2000, 22, 172-179.
69. Bradke, F.; Dotti, C.G. The role of local actin instability in axon formation. Science 1999, 283, 1931-1934.
70. Schaefer, A.W.; Schoonderwoert, V.T.; Ji, L.; Mederios, N.; Danuser, G.; Forscher, P. Coordination of actin filament and microtubule dynamics during neurite outgrowth. Dev. Cell 2008, 15, 146-162.
71. Burnette, D.T.; Ji, L.; Schaefer, A.W.; Medeiros, N.A.; Danuser, G.; Forscher, P. Myosin II activity facilitates microtubule bundling in the neuronal growth cone neck. Dev. Cell 2008, 15, 163-169.
72. Witte, H.; Neukirchen, D.; Bradke, F. Microtubule stabilization specifies initial neuronal polarization. J. Cell Biol. 2008, 180, 619-632.
73. Seetapun, D.; Odde, D.J. Cell-length-dependent microtubule accumulation during polarization. Curr. Biol. 2010, 20, 979-988.
74. Goldstein, B.; Macara, I.G. The PAR proteins: Fundamental players in animal cell polarization. Dev. Cell 2007, 13, 609-622.
75. Kemphues, K. PARsing embryonic polarity. Cell 2000, 101, 345-348.
76. Shi, S.H.; Jan, L.Y.; Jan, Y.N. Hippocampal neuronal polarity specified by spatially localized mPar3/mPar6 and PI 3-kinase activity. Cell 2003, 112, 63-75.
77. Chen, S.; Chen, J.; Shi, H.; Wei, M.; Castaneda-Castellanos, D.R.; Bultje, R.S.; Pei, X.; Kriegstein, A.R.; Zhang, M.; Shi, S.H. Regulation of microtubule stability and organization by mammalian Par3 in specifying neuronal polarity. Dev. Cell 2013, 24, 26-40.
78. Hu, C.K.; Coughlin, M.; Field, C.M.; Mitchison, T.J. Cell polarization during monopolar cytokinesis. J. Cell Biol. 2008, 181, 195-202.
79. Rankin, K.E.; Wordeman, L. Long astral microtubules uncouple mitotic spindles from the cytokinetic furrow. J. Cell Biol. 2010, 190, 35-43.
80. Motegi, F.; Zonies, S.; Hao, Y.; Cuenca, A.A.; Griffin, E.; Seydoux, G. Microtubules induce self-organization of polarized PAR domains in Caenorhabditis elegans zygotes. Nat. Cell Biol. 2011, 13, 1361-1367.
81. Insolera, R.; Chen, S.; Shi, S.H. Par proteins and neuronal polarity. Dev. Neurobiol. 2011, 71, 483-494.
82. Salbreux, G.; Charras, G.; Paluch, E. Actin cortex mechanics and cellular morphogenesis. Trends Cell Biol. 2012, 22, 536-545.
83. Heisenberg, C.P.; Bellaïche, Y. Forces in tissue morphogenesis and patterning. Cell 2013, 23, 948-962.
84. Murrell, M.; Oakes, P.W.; Lenz, M.; Gardel, M.L. Forcing cells into shape: The mechanics of actomyosin contractility. Nat. Rev. Mol. Cell Biol. 2015, 16, 486-498.
85. Goehring, N.W.; Grill, S.W. Cell polarity: Mechanochemical patterning. Trends Cell Biol. 2013, 23, 72-80.
86. Grill, S.W. Growing up is stressful: Biophysical laws of morphogenesis. Curr. Opin. Genet. Dev. 2011, 21, 647-652.
87. Gardel, M.L.; Shin, J.H.; MacKintosh, F.C.; Mahadevan, L.; Matsudaira, P.; Weitz, D.A. Elastic behavior of cross-linked and bundled actin networks. Science 2004, 304, 1301-1305.
88. Salbreux, G.; Prost, J.; Joanny, J.F. Hydrodynamics of cellular cortical flows and the formation of contractile rings. Phys. Rev. Lett. 2009, 103, doi:10.1103/PhysRevLett.103.058102.
89. Dalhaimer, P.; Discher, D.E.; Lubensky, T.C. Crosslinked actin networks show liquid crystal elastomer behaviour, including soft-mode elasticity. Nat. Phys. 2007, 3, 354-360.
90. Wagner, B.; Tharmann, R.; Haase, I.; Fischer, M.; Bausch, A.R. Cytoskeletal polymer networks: The molecule structure of cross-linkers determines macroscopic properties. Proc. Natl. Acad. Sci. USA 2006, 103, 13974-13978.
91. Vogel, S.K.; Schwille, P. Minimal systems to study membrane-cytoskeleton interactions. Curr. Opin. Biotechnol. 2012, 23, 758-765.
92. Vogel, S.K.; Heinemann, F.; Chwastek, G.; Schwille, P. The design of MACs (minimal actin cortices). Cytoskeleton 2013, 70, 706-717.
93. Schaller, V.; Weber, C.; Semmrich, C.; Frey, E.; Bausch, A.R. Polar patterns of driven filaments. Nature 2010, 467, 73-77.
94. Charras, G.T.; Yarrow, J.C.; Horton, M.A.; Mahadevan, L.; Mitchison, T.J. Non-equilibration of hydrostatic pressure in blebbing cells. Nature 2005, 435, 365-369.
95. Sedzinski, J.; Biro, M.; Oswald, A.; Tinevez, J.Y.; Salbreux, G.; Paluch, E. Polar actomyosin contractility destabilizes the position of the cytokinetic furrow. Nature 2011, 476, 462-466.
96. Purvanov, V.; Holst, M.; Khan, J.; Baarlink, C.; Grosse, R. G-protein-coupled receptor signaling and polarized actin dynamics drive cell-in-cell invasion. Elife 2014, 3, doi: 10.7554/eLife.02786.
97. Yam, P.T.; Wilson, C.A.; Ji, L.; Hebert, B.; Barnhart, E.L.; Dye, N.A.; Wiseman, P.W.; Danuser, G.; Theriot, J.A. Actin-myosin network reorganization breaks symmetry at the cell rear to spontaneously initiate polarized cell motility. J. Cell Biol. 2007, 178, 1207-1221.
98. Barnhart, E.; Lee, K.C.; Allen, G.M.; Theriot, J.A.; Mogilner, A. Balance between cell-substrate adhesion and myosin contraction determines the frequency of motility initiation in fish keratocytes. Proc. Natl. Acad. Sci. USA 2015, 112, 5045-5050.
99. Vogel, S.K.; Petrasek, Z.; Heinemann, F.; Schwille, P. Myosin motors fragment and compact membrane-bound actin filaments. Elife 2013, 2, doi:10.7554/eLife.00116.
100. Carvalho, K.; Tsai, F.C.; Lees, E.; Voituriez, R.; Koenderink, G.H.; Sykes, C. Cell-sized liposomes reveal how actomyosin cortical tension drives shape change. Proc. Natl. Acad. Sci. USA 2013, 110, 16456-16461.
101. Carvalho, K.; Lemière, J.; Faqir, F.; Manzi, J.; Blanchoin, L.; Plastino, J.; Betz, T.; Sykes, C. Actin polymerization or myosin contraction: Two ways to build up cortical tension for symmetry breaking. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2013, 368, doi:10.1098/rstb.2013.0005.
102. Van Oudenaarden, A.; Theriot, J.A. Cooperative symmetry-breaking by actin polymerization in a model for cell motility. Nat. Cell Biol. 1999, 1, 493-499.
103. Van der Gucht, J.; Paluch, E.; Plastino, J.; Sykes, C. Stress release drives symmetry breaking for actin-based movement. Proc. Natl. Acad. Sci. USA 2005, 102, 7847-7852.
104. Sekimoto, K.; Prost, J.; Jülicher, F.; Boukellal, H.; Bernheim-Grosswasser, A. Role of tensile stress in actin gels and a symmetry-breaking instability. Eur. Phys. J. E Soft Matter 2004, 13, 247-259.
105. Abu Shah, E.; Keren, K. Symmetry breaking in reconstituted actin cortices. Elife 2014, 3, doi:10.7554/eLife.01433.
106. John, K.; Peyla, P.; Kassner, K.; Prost, J.; Misbah, C. Nonlinear study of symmetry breaking in actin gels: Implications for cellular motility. Phys. Rev. Lett. 2008, 100, doi:10.1103/PhysRevLett.100.068101.
107. Lewis, O.L.; Guy, R.D.; Allard, J.F. Actin-myosin spatial patterns from a simplified isotropic viscoelastic model. Biophys. J. 2014, 107, 863-870.
108. Pinot, M.; Steiner, V.; Dehapiot, B.; Yoo, B.K.; Chesnel, F.; Blanchoin, L.; Kervrann, C.; Gueroui, Z. Confinement induces actin flow in a meiotic cytoplasm. Proc. Natl. Acad. Sci. USA 2012, 109, 11705-11710.
109. Cunningham, C.C. Actin polymerization and intracellular solvent flow in cell surface blebbing. J. Cell Biol. 1995, 129, 1589-1599.
110. Mills, J.C.; Stone, N.; Erhardt, J.; Pittman, R.N. Apoptotic membrane blebbing is regulated by myosin light chain phosphorylation. J. Cell Biol. 1998, 140, 627-636.
111. Miyoshi, H.; Umeshita, K.; Sakon, M.; Imajoh-Ohmi, S.; Fujitani, K.; Gotoh, M.; Oiki, E.; Kambayashi, J.; Monden, M. Calpain activation in plasma membrane bleb formation during tert-butyl hydroperoxide-induced rat hepatocyte injury. Gastroenterology 1996, 110, 1897-1904.
112. Sahai, E.; Marshall, C.J. Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signaling and extracellular proteolysis. Nat. Cell Biol. 2003, 5, 711-719.
113. Paluch, E.; Sykes, C.; Prost, J.; Bornens, M. Dynamic modes of the cortical actomyosin gel during cell locomotion and division. Trends Cell Biol. 2006, 16, 5-10.
114. Yoshida, K.; Soldati, T. Dissection of amoeboid movement into two mechanically distinct modes. J. Cell Sci. 2006, 119, 3833-3844.
115. Lämmermann, T.; Sixt, M. Mechanical modes of "amoeboid" cell migration. Curr. Opin. Cell Biol. 2009, 21, 636-644.
116. Renkawitz, J.; Schumann, K.; Weber, M.; Lämmermann, T.; Pflicke, H.; Piel, M.; Polleux, J.; Spatz, J.P.; Sixt, M. Adaptive force transmission in amoeboid cell migration. Nat. Cell Biol. 2009, 11, 1438-1443.
117. Bergert, M.; Erzberger, A.; Desai, R.A.; Aspalter, I.M.; Oates, A.C.; Charras, G.; Salbreux, G.; Paluch, E.K. Force transmission during adhesion-independent migration. Nat. Cell Biol. 2015, 17, 524-529.
118. Florey, O.; Krajcovic, M.; Sun, Q.; Overholtzer, M. Entosis. Curr. Biol. 2010, 20, R88-R89.
119. Sun, Q.; Luo, T.; Ren, Y.; Florey, O.; Shirasawa, S.; Sasazuki, T.; Robinson, D.N.; Overholtzer, M. Competition between human cells by entosis. Cell Res. 2014, 24, 1299-1310.
120. Cramer, L.P. Forming the cell rear first: Breaking cell symmetry to trigger directed cell migration. Nat. Cell Biol. 2010, 12, 628-632.
121. Cramer, L.P. Mechanism of cell rear retraction in migrating cells. Curr. Opin. Cell Biol. 2013, 25, 591-599.
122. Mseka, T.; Bamburg, J.R.; Cramer, L.P. ADF/cofilin family proteins control formation of oriented actinfilament bundles in the cell body to trigger fibroblast polarization. J. Cell Sci. 2007, 120, 4332-4344.
123. Verkhovsky, A.B.; Svitkina, T.M.; Borisy, G.G. Selfpolarization and directional motility of cytoplasm. Curr. Biol. 1999, 9, 11-20.
124. Chi, Q.; Yin, T.; Gregersen, H.; Deng, X.; Fan, Y.; Zhao, J.; Liao, D.; Wang, G. Rear actomyosin contractility-driven directional cell migration in three-dimensional matrices: A mechano-chemical coupling mechanism. J. R. Soc. Interface 2014, 11, doi:10.1098/rsif.2013.1072.
125. Fournier, M.F.; Sauser, R.; Ambrosi, D.; Meister, J.-J.; Verkhovsky, A.B. Force transmission in migrating cells. J. Cell Biol. 2010, 188, 287-297.
126. Nagel, O.; Guven, C.; Theves, M.; Driscoll, M.; Losert, W.; Beta, C. Geometry-driven polarity in motile amoeboid cells. PLoS ONE 2014, 9, doi:10.1371/journal.pone.0113382.
127. Liu, Y.J.; le Berre, M.; Lautenschlaeger, F.; Maiuri, P.; Callan-Jones, A.; Heuzé, M.; Takaki, T.; Voituriez, R.; Piel, M. Confinement and low adhesion induce fast amoeboid migration of slow mesenchymal cells. Cell 2015, 160, 659-672.
128. Inagaki, N.; Toriyama, M.; Sakumura, Y. Systems biology of symmetry breaking during neuronal polarity formation. Dev. Neurobiol. 2011, 71, 584-593.
129. Fivaz, M.; Bandara, S.; Inoue, T.; Meyer, T. Robust neuronal symmetry breaking by Ras-triggered local positive feedback. Curr. Biol. 2008, 18, 44-50.
130. Oinuma, I.; Katoh, H.; Negishi, M. R-Ras controls axon specification upstream of glycogen synthase kinase-3β through integrin-linked kinase. J. Biol. Chem. 2007, 282, 303-318.
131. Iwasawa, N.; Negishi, M.; Oinuma, I. R-Ras controls axon branching through afadin in cortical neurons. Mol. Biol. Cell 2012, 23, 2793-2804.
132. Mitchison, T.; Kirschner, M. Cytoskeletal dynamics and nerve growth. Neuron 1988, 1, 761-772.
133. Shimada, T.; Toriyama, M.; Uemura, K.; Kamiguchi, H.; Sugiura, T.; Watanabe, N.; Inagaki, N. Shootin1 interacts with actin retrograde flow and L1-CAM to promote axon outgrowth. J. Cell Biol. 2008, 181, 817-829.
134. Neukirchen, D.; Bradke, F. Neuronal polarization and the cytoskeleton. Semin. Cell Dev. Biol. 2011, 22, 825-833.
135. Bendezú, F.O.; Vincenzetti, V.; Vavylonis, D.; Wyss, R.; Vogel, H.; Martin, S.G. Spontaneous Cdc42 polarization independent of GDI-mediated extraction and actin-based trafficking. PLoS Biol. 2015, 13, doi:10.1371/journal.pbio.1002097.
136. Wedlich-Söldner, R.; Wai, S.C.; Schmidt, T.; Li, R. Robust cell polarity is a dynamic state established by coupling transport and GTPase signaling. J. Cell Biol. 2004, 166, 889-900.
137. Irazoqui, J.E.; Gladfelter, A.S.; Lew, D.J. Scaffold-mediated symmetry breaking by Cdc42p. Nat. Cell Biol. 2003, 5, 1062-1070.
138. Freisinger, T.; Klünder, B.; Johnson, J.; Müller, N.; Pichler, G.; Beck, G.; Costanzo, M.; Boone, C.; Cerione, R.A.; Frey, E.; Wedlich-Söldner, R. Establishment of a robust single axis of cell polarity by coupling multiple positive feedback loops. Nat. Commun. 2013, 4, doi:10.1038/ncomms2795.
139. Fairn, G.D.; Hermansson, M.; Somerharju, P.; Grinstein, S. Phosphatidylserine is polarized and required for proper Cdc42 localization and for development of cell polarity. Nat. Cell Biol. 2011, 13, 1424-1430.
140. Haupt, A.; Campetelli, A.; Bonazzi, D.; Piel, M.; Chang, F.; Minc, N. Electrochemical regulation of budding yeast polarity. PLoS Biol. 2014, 12, doi:10.1371/journal.pbio.1002029.
141. Blackmond, G. The origin of biological homochirality. Cold Spring Harb. Perspect. Biol. 2010, 2, 2787-2884.
142. Holmes, K.C.; Popp, D.; Gebhard, W.; Kabsch, W. Atomic model of the actin filament. Nature 1990, 347, 44-49.
143. Sase, I.; Miyata, H.; Ishiwata, S.; Kinosita, K., Jr. Axial rotation of sliding actin filaments revealed by single-fluorophore imaging. Proc. Natl. Acad. Sci. USA 1997, 94, 5646-5650.
144. Beausang, J.F.; Schroeder, H.W., III; Nelson, P.C.; Goldman, Y.E. Twirling of actin by myosins II and V observed via polarized TIRF in a modified gliding assay. Biophys. J. 2008, 95, 5820-5831.
145. Nishizaka, T.; Yagi, T.; Tanaka, Y.; Ishiwata, S. Right-handed rotation of an actin filament in an in vitro motile system. Nature 1993, 361, 269-271.
146. Vilfan, A. Twirling motion of actin filaments in gliding assays with nonprocessive Myosin motors. Biophys. J. 2009, 97, 1130-1137.
147. Sun, Y.; Schroeder, H.W., III; Beausang, J.F.; Homma, K.; Ikebe, M.; Goldman, Y.E. Myosin VI walks "wiggly" on actin with large and variable tilting. Mol. Cell 2007, 28, 954-964.
148. Heacock, A.M.; Agranoff, B.W. Clockwise growth of neurites from retinal explants. Science 1977, 198, 64-66.
149. Schwartz, M.; Agranoff, B.W. Outgrowth and maintenance of neurites from cultured goldfish retinal ganglion cells. Brain Res. 1981, 206, 331-343.
150. Romijn, H.J.; Mud, M.T.; Wolters, P.S.; Corner, M.A. Neurite formation in dissociated cerebral cortex in vitro: Evidence for clockwise outgrowth and autotopic contacts. Brain Res. 1980, 192, 575-580.
151. Tamada, A.; Kawase, S.; Murakami, F.; Kamiguchi, H. Autonomous right-screw rotation of growth cone filopodia drives neurite turning. J. Cell Biol. 2010, 188, 429-441.
152. Yamanaka, H.; Kondo, S. Rotating pigment cells exhibit an intrinsic chirality. Genes Cells 2015, 20, 29-35.
153. Tanner, K.; Mori, H.; Mroue, R.; Bruni-Cardoso, A.; Bissell, M.J. Coherent angular motion in the establishment of multicellular architecture of glandular tissues. Proc. Natl. Acad. Sci. USA 2012, 109, 1973-1978.
154. Xu, J.; van Keymeulen, A.; Wakida, N.M.; Carlton, P.; Berns, M.W.; Bourne, H.R. Polarity reveals intrinsic cell chirality. Proc. Natl. Acad. Sci. USA 2007, 104, 9296-9300.
155. Wan, L.Q.; Ronaldson, K.; Park, M.; Taylor, G.; Zhang, Y.; Gimble, J.M.; Vunjak-Novakovic, G. Micropatterned mammalian cells exhibit phenotype-specific left-right asymmetry. Proc. Natl. Acad. Sci. USA 2011, 108, 12295-12300.
156. Wan, L.Q.; Ronaldson, K.; Guirguis, M.; Vunjak-Novakovic, G. Micropatterning of cells reveals chiral morphogenesis. Stem Cell Res. Ther. 2013, 4, 24.
157. Chen, T.H.; Hsu, J.J.; Zhao, X.; Guo, C.; Wong, M.N.; Huang, Y.; Li, Z.; Garfinkel, A.; Ho, C.M.; Tintut, Y.; et al. Left-right symmetry breaking in tissue morphogenesis via cytoskeletal mechanics. Circ. Res. 2012, 110, 551-559.
158. Rørth, P. Fellow travellers: Emergent properties of collective cell migration. EMBO Rep. 2012, 13, 984-991.
159. Doxzen, K.; Vedula, S.R.K.; Leong, M.C.; Hirata, H.; Gov, N.; Kabla, A.J.; Ladoux, B.; Lim, C.T. Guidance of collective cell migration by substrate geometry. Integr. Biol. 2013, 5, 1026-1035.
160. Rappel, W.-J.; Nicol, A.; Sarkissian, A.; Levine, H.; Loomis, W.F. Self-organized vortex state in two-dimensional Dictyostelium dynamics. Phys. Rev. Lett. 1999, 83, 1247-1250.
161. Leong, F.Y. Physical explanation of coupled cell-cell rotational behavior and interfacial morphology: A particle dynamics model. Biophys. J. 2013, 105, 2301-2311.
162. Tee, Y.H.; Shemesh, T.; Thiagarajan, V.; Hariadi, R.F.; Anderson, K.L.; Page, C.; Volkmann, N.; Hanein, D.; Sivaramakrishnan, S.; Kozlov, M.M.; et al. Cellular chirality arising from the self-organization of the actin cytoskeleton. Nat. Cell Biol. 2015, 17, 445-457.
163. Ambravaneswaran, V.; Wong, I.Y.; Aranyosi, A.J.; Toner, M.; Irimia, D. Directional decisions during neutrophil chemotaxis inside bifurcating channels. Integr. Biol. 2010, 2, 639-647.
164. Pohl, C. Left-right patterning in the C. elegans embryo: Unique mechanisms and common principles. Commun. Integr. Biol. 2011, 4, 1-7.
165. Wood, W.B. Evidence from reversal of handedness in C. elegans embryos for early cell interactions determining cell fates. Nature 1991, 349, 536-538.
166. McManus, C. Reversed bodies, reversed brains and (some) reversed behaviors: Of zebrafish and men. Dev. Cell 2005, 8, 796-797.
167. Sutherland, M.J.; Ware, S.M. Disorders of left-right asymmetry: Heterotaxy and situs inversus. Am. J. Med. Genet. C Semin. Med. Genet. 2009, 151, 307-317.
168. Yost, H.J. Coordinating the development of bilateral symmetry and left-right asymmetry. Semin. Cell Dev. Biol. 2009, 20, 455.
169. Brown, N.; Wolpert, L. The development of handedness in left/right asymmetry. Development 1990, 109, 1-9.
170. Weisblat, D.A. Asymmetric cell divisions in the early embryo of the leech Helobdella robusta. Prog. Mol. Subcell Biol. 2007, 45, 79-95.
171. Crampton, H. Reversal of cleavage in a sinistral gastropod. Ann. N. Y. Acad. Sci. 1894, 8, 167-170.
172. Kuroda, R.; Endo, B.; Abe, M.; Shimizu, M. Chiral blastomere arrangement dictates zygotic left-right asymmetry pathway in snails. Nature 2009, 462, 790-794.
173. Poole, R.J.; Hobert, O. Early embryonic programming of neuronal left/right asymmetry in C. elegans. Curr. Biol. 2006, 16, 2279-2292.
174. Freeman, G.; Lundelius, J.W. Evolutionary implications of the mode of D quadrant specification in coelomates with spiral cleavage. J. Evol. Biol. 1992, 5, 205-247.
175. Lyons, D.C.; Weisblat, D.A. D quadrant specification in the leech Helobdella: Actomyosin contractility controls the unequal cleavage of the CD blastomere. Dev. Biol. 2009, 334, 46-58.
176. Ren, X.; Weisblat, D.A. Asymmetrization of first cleavage by transient disassembly of one spindle pole aster in the leech Helobdella robusta. Dev. Biol. 2006, 292, 103-115.
177. Luetjens, C.M. Multiple, alternative cleavage patterns precede uniform larval morphology during normal development of Dreissena polymorpha (Mollusca, Lamellibranchia). Wilhelm Roux Arch. Dev. Biol. 1995, 205, 138-149.
178. Luetjens, C.M.; Dorresteijn, A.W.C. The site of fertilisation determines dorsoventral polarity but not chirality in the zebra mussel embryo. Zygote 1998, 6, 125-135.
179. Boycott, A.E.; Diver, C.; Garstang, S.L.; Hardy, A.C.; Turner, F.M. The inheritance of sinistrality in Lymnaea peregra. Phil. Trans. R. Soc. Lond. B 1930, 219, 51-131.
180. Sturtevant, A.H. Inheritance of direction of coiling in Lymnaea. Science 1923, 58, 269-270.
181. Freeman, G.; Lundelius, J.W. The developmental genetics of dextrality and sinistrality in the gastropod Lymnaea peregra. Wilhelm Roux Arch. Dev. Biol. 1982, 191, 69-83.
182. Hosoiri, Y.; Harada, Y.; Kuroda, R. Construction of a backcross progeny collection of dextral and sinistral individuals of a freshwater gastropod, Lymnaea stagnalis. Dev. Genes Evol. 2003, 213, 193-198.
183. Shibazaki, Y.; Shimizu, M.; Kuroda, R. Body handedness is directed by genetically determined cytoskeletal dynamics in the early embryo. Curr. Biol. 2004, 14, 1462-1467.
184. Meshcheryakov, V.N.; Beloussov, L.V. Asymmetrical rotations of blastomeres in early cleavage of gastropoda. Wilhelm Roux Arch. Dev. Biol. 1975, 177, 193-203.
185. Grande, C.; Patel, N.H. Nodal signalling is involved in left-right asymmetry in snails. Nature 2009, 457, 1007-1011.
186. Fürthauer, S.; Strempel, M.; Grill, S.W.; Jülicher, F. Active chiral fluids. Eur. Phys. J. E Soft Matter 2012, 35, 89.
187. Naganathan, S.R.; Fürthauer, S.; Nishikawa, M.; Jülicher, F.; Grill, S.W. Active torque generation by the actomyosin cell cortex drives left-right symmetry breaking. Elife 2014, 3, doi:10.7554/eLife.04165.
188. Schonegg, S.; Hyman, A.A.; Wood, W.B. Timing and mechanism of the initial cue establishing handed left-right asymmetry in Caenorhabditis elegans embryos. Genesis 2014, 52, 572-580.
189. Bergmann, D.C.; Lee, M.; Robertson, B.; Tsou, M.F.; Rose, L.S.; Wood, W.B. Embryonic handedness choice in C. elegans involves the Galpha protein GPA-16. Development 2003, 130, 5731-5740.
190. Wood, W.B.; Bergmann, D.; Florance, A. Maternal effect of low temperature on handedness determination in C. elegans embryos. Dev. Genet. 1996, 19, 222-230.
191. Pohl, C.; Bao, Z. Chiral forces organize left-right patterning in C. elegans by uncoupling midline and anteroposterior axis. Dev. Cell 2010, 19, 402-412.
192. Singh, D.; Pohl, C. A function for the midbody remnant in embryonic patterning. Commun. Integr. Biol. 2014, 7, doi:10.4161/cib.28533.
193. Singh, D.; Pohl, C. Coupling of rotational cortical flow, asymmetric midbody positioning, and spindle rotation mediates dorsoventral axis formation in C. elegans. Dev. Cell 2014, 28, 253-267.
194. Pinheiro, D.; Bellaïche, Y. Making the most of the midbody remnant: Specification of the dorsal-ventral axis. Dev. Cell 2014, 28, 219-220.
195. Hutter, H.; Schnabel, R. glp-1 and inductions establishing embryonic axes in C. elegans. Development 1994, 120, 2051-2064.
196. Hutter, H.; Schnabel, R. Establishment of left-right asymmetry in the Caenorhabditis elegans embryo: A multistep process involving a series of inductive events. Development 1995, 121, 3417-3424.
197. Pohl, C.; Tiongson, M.; Moore, J.L.; Santella, A.; Bao, Z. Actomyosin-based self-organization of cell internalization during C. elegans gastrulation. BMC Biol. 2012, 10, doi:10.1186/1741-7007-10-94.
198. Gros, J.; Feistel, K.; Viebahn, C.; Blum, M.; Tabin, C.J. Cell movements at Hensen's node establish left/right asymmetric gene expression in the chick. Science 2009, 324, 941-944.
199. Taniguchi, K.; Maeda, R.; Ando, T.; Okumura, T.; Nakazawa, N.; Hatori, R.; Nakamura, M.; Hozumi, S.; Fujiwara, H.; Matsuno, K. Chirality in planar cell shape contributes to left-right asymmetric epithelial morphogenesis. Science 2011, 333, 339-341.
200. Bischoff, M.; Schnabel, R. A posterior centre establishes and maintains polarity of the Caenorhabditis elegans embryo by a Wnt-dependent relay mechanism. PLoS Biol. 2006, 4, doi:10.1371/journal.pbio.0040396.
201. Bischoff, M.; Schnabel, R. Global cell sorting is mediated by local cell-cell interactions in the C. elegans embryo. Dev. Biol. 2006, 294, 432-444.
202. Schnabel, R.; Bischoff, M.; Hintze, A.; Schulz, A.K.; Hejnol, A.; Meinhardt, H.; Hutter, H. Global cell sorting in the C. elegans embryo defines a new mechanism for pattern formation. Dev. Biol. 2006, 294, 418-431.
203. Schulze, J.; Houthoofd, W.; Uenk, J.; Vangestel, S.; Schierenberg, E. Plectus-A stepping stone in embryonic cell lineage evolution of nematodes. Evodevo 2012, 3, doi:10.1186/2041-9139-3-13.
204. Schulze, J.; Schierenberg, E. Evolution of embryonic development in nematodes. Evodevo 2011, 2, doi:10.1186/2041-9139-2-18.
205. Coutelis, J.B.; González-Morales, N.; Géminard, C.; Noselli, S. Diversity and convergence in the mechanisms establishing L/R asymmetry in metazoa. EMBO Rep. 2014, 15, 926-937.
206. Hozumi, S.; Maeda, R.; Taniguchi, K.; Kanai, M.; Shirakabe, S.; Sasamura, T.; Spéder, P.; Noselli, S.; Aigaki, T.; Murakami, R.; et al. An unconventional myosin in Drosophila reverses the default handedness in visceral organs. Nature 2006, 440, 798-802.
207. Spéder, P.; Adám, G.; Noselli, S. Type ID unconventional myosin controls left-right asymmetry in Drosophila. Nature 2006, 440, 803-807.
208. Géminard, C.; González-Morales, N.; Coutelis, J.B.; Noselli, S. The myosin ID pathway and left-right asymmetry in Drosophila. Genesis 2014, 52, 471-480.
209. Kim, S.V.; Flavell, R.A. Myosin I: From yeast to human. Cell Mol. Life Sci. 2008, 65, 2128-2137.
210. Pyrpassopoulos, S.; Feeser, E.; Mazerik, J.N.; Tyska, M.J.; Ostap, E.M. Membrane-bound Myo1c powers asymmetric motility of actin filaments. Curr. Biol. 2012, 22, 1688-1692.
211. Okumura, T.; Sasamura, T.; Inatomi, M.; Hozumi, S.; Nakamura, M.; Hatori, R.; Taniguchi, K.; Nakazawa, N.; Suzuki, E.; Maeda, R.; et al. Class I myosins have overlapping and specialized functions in left-right asymmetric development in Drosophila. Genetics 2015, 199, 1183-1199.
212. Petzoldt, A.G.; Coutelis, J.B.; Géminard, C.; Spéder, P.; Suzanne, M.; Cerezo, D.; Noselli, S. DE-Cadherin regulates unconventional Myosin ID and Myosin IC in Drosophila left-right asymmetry establishment. Development 2012, 139, 1874-1884.
213. Brembeck, F.H.; Rosário, M.; Birchmeier, W. Balancing cell adhesion and Wnt signaling, the key role of beta-catenin. Curr. Opin. Genet. Dev. 2006, 16, 51-59.
214. González-Morales, N.; Géminard, C.; Lebreton, G.; Cerezo, D.; Coutelis, J.-B.; Noselli, S. The atypical cadherin dachsous controls left-right asymmetry in Drosophila. Dev. Cell 2015, 33, 675-689.
215. Marcinkevicius, E.; Zallen, J.A. Regulation of cytoskeletal organization and junctional remodeling by the atypical cadherin Fat. Development 2013, 140, 433-443.
216. Hatori, R.; Ando, T.; Sasamura, T.; Nakazawa, N.; Nakamura, M.; Taniguchi, K.; Hozumi, S.; Kikuta, J.; Ishii, M.; Matsuno, K. Left-right asymmetry is formed in individual cells by intrinsic cell chirality. Mech. Dev. 2014, 133, 146-162.
217. Kuroda, J.; Nakamura, M.; Yoshida, M.; Yamamoto, H.; Maeda, T.; Taniguchi, K.; Nakazawa, N.; Hatori, R.; Ishio, A.; Ozaki, A.; et al. Canonical Wnt signaling in the visceral muscle is required for left-right asymmetric development of the Drosophila midgut. Mech. Dev. 2012, 128, 625-639.
218. Coutelis, J.B.; Géminard, C.; Spéder, P.; Suzanne, M.; Petzoldt, A.G.; Noselli, S. Drosophila left/right asymmetry establishment is controlled by the Hox gene abdominal-B. Dev. Cell 2013, 24, 89-97.
219. Haigo, S.L.; Bilder, D. Global tissue revolutions in a morphogenetic movement controlling elongation. Science 2011, 331, 1071-1074.
220. Viktorinová, I.; Dahmann, C. Microtubule polarity predicts direction of egg chamber rotation in Drosophila. Curr. Biol. 2013, 23, 1472-1477.
221. Cetera, M.; Ramirez-San Juan, G.R.; Oakes, P.W.; Lewellyn, L.; Fairchild, M.J.; Tanentzapf, G.; Gardel, M.L.; Horne-Badovinac, S. Epithelial rotation promotes the global alignment of contractile actin bundles during Drosophila egg chamber elongation. Nat. Commun. 2014, 5, doi:10.1038/ncomms6511.
222. Wang, H.; Lacoche, S.; Huang, L.; Xue, B.; Muthuswamy, S.K. Rotational motion during three-dimensional morphogenesis of mammary epithelial acini relates to laminin matrix assembly. Proc. Natl. Acad. Sci. USA 2013, 110, 163-168.
223. Thitamadee, S.; Tuchihara, K.; Hashimoto, T. Microtubule basis for left-handed helical growth in Arabidopsis. Nature 2002, 417, 193-196.
224. Buschmann, H.; Fabri, C.O.; Hauptmann, M.; Hutzler, P.; Laux, T.; Lloyd, C.W.; Schäffner, A.R. Helical growth of the Arabidopsis mutant tortifolia1 reveals a plant-specific microtubule-associated protein. Curr. Biol. 2004, 14, 1515-1521.
225. Lobikin, M.; Wang, G.; Xu, J.; Hsieh, Y.W.; Chuang, C.F.; Lemire, J.M.; Levin, M. Early, nonciliary role for microtubule proteins in left-right patterning is conserved across kingdoms. Proc. Natl. Acad. Sci. USA 2012, 109, 12586-12591.
226. Chang, C.; Hsieh, Y.W.; Lesch, B.J.; Bargmann, C.I.; Chuang, C.F. Microtubule-based localization of a synaptic calcium-signaling complex is required for left-right neuronal asymmetry in C. elegans. Development 2011, 138, 3509-3518.
227. Buschmann, H.; Hauptmann, M.; Niessing, D.; Lloyd, C.W.; Schäffner, A.R. Helical growth of the Arabidopsis mutant tortifolia2 does not depend on cell division patterns but involves handed twisting of isolated cells. Plant Cell 2009, 21, 2090-2106.
228. Hoson, T.; Matsumoto, S.; Soga, K.; Wakabayashi, K. Cortical microtubules are responsible for gravity resistance in plants. Plant Signal Behav. 2010, 5, 752-754.
229. Oda, Y.; Fukuda, H. Initiation of cell wall pattern by a Rho-and microtubule-driven symmetry breaking. Science 2012, 337, 1333-1336.
230. Afzelius, B. A human syndrome caused by immotile cilia. Science 1976, 193, 317-319.
231. Wagner, M.K.; Yost, H.J. Left-right development: The roles of nodal cilia. Curr. Biol. 2000, 10, R149-R151.
232. Lee, J.D.; Anderson, K.V. Morphogenesis of the node and notochord: The cellular basis for the establishment and maintenance of left-right asymmetry in the mouse. Dev. Dyn. 2008, 237, 3464-3476.
233. Babu, D.; Roy, S. Left-right asymmetry: Cilia stir up new surprises in the node. Open Biol. 2013, 3, doi:10.1098/rsob.130052.
234. Komatsu, Y.; Mishina, Y. Establishment of left-right asymmetry in vertebrate development: The node in mouse embryos. Cell Mol. Life Sci. 2013, 70, 4659-4666.
235. Supp, D.M.; Witte, D.P.; Potter, S.S.; Brueckner, M. Mutation of an axonemal dynein affects left-right asymmetry in inversus viscerum mice. Nature 1997, 389, 963-966.
236. Nonaka, S.; Tanaka, Y.; Okada, Y.; Takeda, S.; Harada, A.; Kanai, Y.; Kido, M.; Hirokawa, N. Randomization of left-right asymmetry due to loss of nodal cilia generating leftward flow of extraembryonic fluid in mice lacking KIF3B motor protein. Cell 1998, 95, 829-837.
237. Okada, Y.; Nonaka, S.; Tanaka, Y.; Saijoh, Y.; Hamada, H.; Hirokawa, N. Abnormal nodal flow precedes situs inversus in iv and inv mice. Mol. Cell 1999, 4, 459-468.
238. Supp, D.M.; Brueckner, M.; Kuehn, M.R.; Witte, D.P.; Lowe, L.A.; McGrath, J.; Corrales, J.; Potter, S.S. Targeted deletion of the ATP binding domain of left-right dynein confirms its role in specifying development of left-right asymmetries. Development 1999, 126, 5495-5504.
239. Essner, J.J.; Amack, J.D.; Nyholm, M.K.; Harris, E.B.; Yost, H.J. Kupffer's vesicle is a ciliated organ of asymmetry in the zebrafish embryo that initiates left-right development of the brain, heart and gut. Development 2005, 132, 1247-1260.
240. Schweickert, A.; Weber, T.; Beyer, T.; Vick, P.; Bogusch, S.; Feistel, K.; Blum, M. Cilia-driven leftward flow determines laterality in Xenopus. Curr. Biol. 2007, 17, 60-66.
241. Nonaka, S.; Shiratori, H.; Saijoh, Y.; Hamada, H. Determination of left-right patterning of the mouse embryo by artificial nodal flow. Nature 2002, 418, 96-99.
242. Levin, M.; Johnson, R.L.; Sterna, C.D.; Kuehn, M.; Tabin, C. A molecular pathway determining left-right asymmetry in chick embryogenesis. Cell 1995, 82, 803-814.
243. Meno, C.; Saijoh, Y.; Fujii, H.; Ikeda, M.; Yokoyama, T.; Yokoyama, M.; Toyoda, Y.; Hamada, H. Left-right asymmetric expression of the TGF beta-family member lefty in mouse embryos. Nature 1996, 381, 151-155.
244. Collignon, J.; Varlet, I.; Robertson, E.J. Relationship between asymmetric nodal expression and the direction of embryonic turning. Nature 1996, 381, 155-158.
245. Lowe, L.A.; Supp, D.M.; Sampath, K.; Yokoyama, T.; Wright, C.V.E.; Potter, S.S.; Overbeek, P.; Kuehn, M.R. Conserved left-right asymmetry of nodal expression and alterations in murine situs inversus. Nature 1996, 381, 158-161.
246. Tanaka, Y.; Okada, Y.; Hirokawa, N. FGF-induced vesicular release of Sonic hedgehog and retinoic acid in leftward nodal flow is critical for left-right determination. Nature 2005, 435, 172-177.
247. Shinohara, K.; Kawasumi, A.; Takamatsu, A.; Yoshiba, S.; Botilde, Y.; Motoyama, N.; Reith, W.; Durand, B.; Shiratori, H.; Hamada, H. Two rotating cilia in the node cavity are sufficient to break left-right symmetry in the mouse embryo. Nat. Commun. 2012, 3, 622.
248. McGrath, J.; Somlo, S.; Makova, S.; Tian, X.; Brueckner, M. Two populations of node monocilia initiate left-right asymmetry in the mouse. Cell 2003, 114, 61-73.
249. Noël, E.S.; Verhoeven, M.; Lagendijk, A.K.; Tessadori, F.; Smith, K.; Choorapoikayil, S.; Hertog, D.J.; Bakkers, J. A Nodal-independent and tissue-intrinsic mechanism controls heart-looping chirality. Nat. Commun. 2013, 4, doi:10.1038/ncomms3754.
250. 3 ciliopathy. Genesis 2014, 52, 600-613.
251. Wang, G.; Manning, M.L.; Amack, J.D. Regional cell shape changes control form and function of Kupffer's vesicle in the zebrafish embryo. Dev. Biol. 2012, 370, 52-62.
252. Itasaki, N.; Nakamura, H.; Sumida, H.; Yasuda, M. Actin bundles on the right side in the caudal part of the heart tube play a role in dextro-looping in the embryonic chick heart. Anat. Embryol. 1991, 183, 29-39.
253. Blum, M.; Schweickert, A.; Vick, P.; Wright, C.V.; Danilchik, M.V. Symmetry breakage in the vertebrate embryo: When does it happen and how does it work? Dev. Biol. 2014, 393, 109-123.
254. Danilchik, M.V.; Brown, E.E.; Riegert, K. Intrinsic chiral properties of the Xenopus egg cortex: An early indicator of left-right asymmetry? Development 2006, 133, 4517-4526.
255. Bray, D.; White, J.G. Cortical flow in animal cells. Science 1988, 239, 883-888.
256. Lewis, W.H. The role of a superficial plasmagel layer in changes of form, locomotion and division of cells in tissue culture. Arch. Exp. Zellforsch. 1939, 23, 1-7.
257. Strome, S. Asymmetric movements of cytoplasmic components in Caenorhabditis elegans zygotes. J. Embryol. Exp. Morphol. 1986, 97, 15-29.
258. Hird, S.N.; White, J.G. Cortical and cytoplasmic flow polarity in early embryonic cells of Caenorhabditis elegans. J. Cell Biol. 1993, 121, 1343-1355.
259. Hird, S. Cortical actin movements during the first cell cycle of the Caenorhabditis elegans embryo. J. Cell Sci. 1996, 109, 525-533.
260. Goldstein, B.; Hird, S.N. Specification of the anteroposterior axis in Caenorhabditis elegans. Development 1996, 122, 1467-1474.
261. Sadler, P.L.; Shakes, D.C. Anucleate Caenorhabditis elegans sperm can crawl, fertilize oocytes and direct anterior-posterior polarization of the 1-cell embryo. Development 2000, 127, 355-366.
262. Nance, J.; Priess, J.R. Cell polarity and gastrulation in C. elegans. Development 2002, 129, 387-397.
263. Lee, J.Y.; Goldstein, B. Mechanisms of cell positioning during C. elegans gastrulation. Development 2003, 130, 307-320.
264. Nance, J.; Munro, E.M.; Priess, J.R. C. elegans PAR-3 and PAR-6 are required for apicobasal asymmetries associated with cell adhesion and gastrulation. Development 2003, 130, 5339-5350.
265. Lee, J.Y.; Marston, D.J.; Walston, T.; Hardin, J.; Halberstadt, A.; Goldstein, B. Wnt/frizzled signaling controls C. elegans gastrulation by activating actomyosin contractility. Curr. Biol. 2006, 16, 1986-1997.
266. Rohrschneider, M.R.; Nance, J. Polarity and cell fate specification in the control of Caenorhabditis elegans gastrulation. Dev. Dyn. 2009, 238, 789-796.
267. Roh-Johnson, M.; Shemer, G.; Higgins, C.D.; McClellan, J.H.; Werts, A.D.; Tulu, U.S.; Gao, L.; Betzig, E.; Kiehart, D.P.; Goldstein, B. Triggering a cell shape change by exploiting preexisting actomyosin contractions. Science 2012, 335, 1232-1235.
268. Wang, X.; Zhou, F.; Lv, S.; Yi, P.; Zhu, Z.; Yang, Y.; Feng, G.; Li, W.; Ou, G. Transmembrane protein MIG-13 links the Wnt signaling and Hox genes to the cell polarity in neuronal migration. Proc. Natl. Acad. Sci. USA 2013, 110, 11175-11180.
269. Witze, E.S.; Litman, E.S.; Argast, G.M.; Moon, R.T.; Ahn, N.G. Wnt5a control of cell polarity and directional movement by polarized redistribution of adhesion receptors. Science 2008, 320, 365-369.
270. Gon, H.; Fumoto, K.; Ku, Y.; Matsumoto, S.; Kikuchi, A. Wnt5a signaling promotes apical and basolateral polarization of single epithelial cells. Mol. Biol. Cell 2013, 24, 3764-3774.
271. Cui, C.; Chatterjee, B.; Lozito, T.P.; Zhang, Z.; Francis, R.J.; Yagi, H.; Swanhart, L.M.; Sanker, S.; Francis, D.; Yu, Q.; et al. Wdpcp, a PCP protein required for ciliogenesis, regulates directional cell migration and cell polarity by direct modulation of the actin cytoskeleton. PLoS Biol. 2013, 11, doi:10.1371/journal.pbio.1001720.
272. Dickinson, D.J.; Nelson, W.J.; Weis, W.I. A polarized epithelium organized by β-and a-catenin predates cadherin and metazoan origins. Science 2011, 331, 1336-1339.
273. St Johnston, D.; Ahringer, J. Cell polarity in eggs and epithelia: Parallels and diversity. Cell 2010, 141, 757-774.
274. Roth, S.; Lynch, J.A. Symmetry breaking during Drosophila oogenesis. Cold Spring Harb. Perspect. Biol. 2009, 1, doi:10.1101/cshperspect.a001891.
275. Doerflinger, H.; Benton, R.; Torres, I.L.; Zwart, M.F.; St Johnston, D. Drosophila anterior-posterior polarity requires actin-dependent PAR-1 recruitment to the oocyte posterior. Curr. Biol. 2006, 16, 1090-1095.
276. Leibfried, A.; Müller, S.; Ephrussi, A. A Cdc42-regulated actin cytoskeleton mediates Drosophila oocyte polarization. Development 2013, 140, 362-371.
277. Kiehart, D.P.; Lutz, M.S.; Chan, D.; Ketchum, A.S.; Laymon, R.A.; Nguyen, B.; Goldstein, L.S. Identification of the gene for fly non-muscle myosin heavy chain: Drosophila myosin heavy chains are encoded by a gene family. EMBO J. 1989, 8, 913-922.
278. Young, P.E.; Richman, A.M.; Ketchum, A.S.; Kiehart, D.P. Morphogenesis in Drosophila requires nonmuscle myosin heavy chain function. Genes Dev. 1993, 7, 29-41.
279. Blankenship, J.T.; Wieschaus, E. Two new roles for the Drosophila AP patterning system in early morphogenesis. Development 2001, 128, 5129-5138.
280. Zallen, J.A.; Wieschaus, E. Patterned gene expression directs bipolar planar polarity in Drosophila. Dev. Cell 2004, 6, 343-355.
281. Dawes-Hoang, R.E.; Parmar, K.M.; Christiansen, A.E.; Phelps, C.B.; Brand, A.H.; Wieschaus, E.F. Folded gastrulation, cell shape change and the control of myosin localization. Development 2005, 132, 4165-4178.
282. Bertet, C.; Sulak, L.; Lecuit, T. Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature 2004, 429, 667-671.
283. Rauzi, M.; Verant, P.; Lecuit, T.; Lenne, P.F. Nature and anisotropy of cortical forces orienting Drosophila tissue morphogenesis. Nat. Cell Biol. 2008, 10, 1401-1410.
284. Fernandez-Gonzalez, R.; Simoes Sde, M.; Röper, J.C.; Eaton, S.; Zallen, J.A. Myosin II dynamics are regulated by tension in intercalating cells. Dev. Cell 2009, 17, 736-743.
285. Martin, A.C.; Kaschube, M.; Wieschaus, E.F. Pulsed contractions of an actin-myosin network drive apical constriction. Nature 2009, 457, 495-499.
286. Rauzi, M.; Lenne, P.F.; Lecuit, T. Planar polarized actomyosin contractile flows control epithelial junction remodelling. Nature 2010, 468, 1110-1114.
287. Simões Sde, M.; Mainieri, A.; Zallen, J.A. Rho GTPase and Shroom direct planar polarized actomyosin contractility during convergent extension. J. Cell Biol. 2014, 204, 575-589.
288. Kasza, K.E.; Farrell, D.L.; Zallen, J.A. Spatiotemporal control of epithelial remodeling by regulated myosin phosphorylation. Proc. Natl. Acad. Sci. USA 2014, 111, 11732-11737.
289. He, B.; Doubrovinski, K.; Polyakov, O.; Wieschaus, E. Apical constriction drives tissue-scale hydrodynamic flow to mediate cell elongation. Nature 2014, 508, 392-396.
290. Munjal, A.; Philippe, J.M.; Munro, E.; Lecuit, T. A self-organized biomechanical network drives shape changes during tissue morphogenesis. Nature 2015, doi:10.1038/nature14603.
291. Behrndt, M.; Salbreux, G.; Campinho, P.; Hauschild, R.; Oswald, F.; Roensch, J.; Grill, S.W.; Heisenberg, C.P. Forces driving epithelial spreading in zebrafish gastrulation. Science 2012, 338, 257-260.
292. Yi, K.; Rubinstein, B.; Li, R. Symmetry breaking and polarity establishment during mouse oocyte maturation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2013, 368, doi:10.1098/rstb.2013.0002.
293. Lepage, S.E.; Bruce, A.E.E. Zebrafish epiboly: Mechanics and mechanisms. Int. J. Dev. Biol. 2010, 54, 1213-1228.
294. Lucas, E.P.; Khanal, I.; Gaspar, P.; Fletcher, G.C.; Polesello, C.; Tapon, N.; Thompson, B.J. The Hippo pathway polarizes the actin cytoskeleton during collective migration of Drosophila border cells. J. Cell Biol. 2013, 201, 875-885.
295. Goldstein, B. Cell contacts orient some cell division axes in the Caenorhabditis elegans embryo. J. Cell Biol. 1995, 129, 1071-1080.
296. Thorpe, C.J.; Schlesinger, A.; Carter, J.C.; Bowerman, B. Wnt signaling polarizes an early C. elegans blastomere to distinguish endoderm from mesoderm. Cell 1997, 90, 695-705.
297. Schlesinger, A.; Shelton, C.A.; Maloof, J.N.; Meneghini, M.; Bowerman, B. Wnt pathway components orient a mitotic spindle in the early Caenorhabditis elegans embryo without requiring gene transcription in the responding cell. Genes Dev. 1999, 13, 2028-2038.
298. Bei, Y.; Hogan, J.; Berkowitz, L.A.; Soto, M.; Rocheleau, C.E.; Pang, K.M.; Collins, J.; Mello, C.C. SRC-1 and Wnt signaling act together to specify endoderm and to control cleavage orientation in early C. elegans embryos. Dev. Cell 2002, 3, 113-125.
299. Goldstein, B.; Takeshita, H.; Mizumoto, K.; Sawa, H. Wnt signals can function as positional cues in establishing cell polarity. Dev. Cell 2006, 10, 391-396.
300. Arata, Y.; Lee, J.Y.; Goldstein, B.; Sawa, H. Extracellular control of PAR protein localization during asymmetric cell division in the C. elegans embryo. Development 2010, 137, 3337-3345.
301. Habib, S.J.; Chen, B.C.; Tsai, F.C.; Anastassiadis, K.; Meyer, T.; Betzig, E.; Nusse, R. A localized Wnt signal orients asymmetric stem cell division in vitro. Science 2013, 339, 1445-1448.
302. Sugioka, K.; Mizumoto, K.; Sawa, H. Wnt regulates spindle asymmetry to generate asymmetric nuclear β-catenin in C. elegans. Cell 2011, 146, 942-954.
303. Knoblich, J.A. Asymmetric cell division: Recent developments and their implications for tumour biology. Nat. Rev. Mol. Cell Biol. 2010, 11, 849-860.
304. Pelletier, L.; Yamashita, Y.M. Centrosome asymmetry and inheritance during animal development. Curr. Opin. Cell Biol. 2012, 24, 541-546.
305. Lu, M.S.; Johnston, C.A. Molecular pathways regulating mitotic spindle orientation in animal cells. Development 2013, 140, 1843-1856.
306. O'Donnell, L.; O'Bryan, M.K. Microtubules and spermatogenesis. Semin. Cell Dev. Biol. 2014, 30, 45-54.
307. Segalen, M.; Bellaïche, Y. Cell division orientation and planar cell polarity pathways. Semin. Cell Dev. Biol. 2009, 20, 972-977.
308. Goodrich, L.V.; Strutt, D. Principles of planar polarity in animal development. Development 2011, 138, 1877-1892.
309. Matis, M.; Axelrod, J.D. Regulation of PCP by the Fat signaling pathway. Genes Dev. 2013, 27, 2207-2220.
310. Guirao, B.; Meunier, A.; Mortaud, S.; Aguilar, A.; Corsi, J.M.; Strehl, L.; Hirota, Y.; Desoeuvre, A.; Boutin, C.; Han, Y.G.; et al. Coupling between hydrodynamic forces and planar cell polarity orients mammalian motile cilia. Nat. Cell Biol. 2010, 12, 341-350.