Biology and Physics of Cell Shape Changes in Development

Current Biology

Volumn 19, Issue 17, 2009, Pages

  Paluch, Ewa ^a,b   Heisenberg, Carl Philipp ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^b INTERNATIONAL INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; ANIMAL EMBRYO; BIOMECHANICS; CELL ADHESION; CELL GROWTH; CELL MOTION; CELL SHAPE; CYTOLOGY; DROSOPHILA; EMBRYO DEVELOPMENT; MORPHOGENESIS; PHYSIOLOGY; PRENATAL DEVELOPMENT; REVIEW; ZEBRA FISH;

ANIMALS; BIOMECHANICS; BODY PATTERNING; CELL ADHESION; CELL GROWTH PROCESSES; CELL MOVEMENT; CELL SHAPE; DROSOPHILA; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; ZEBRAFISH;

EID: 69949150648     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2009.07.029     Document Type: Review

References (117)

1. Thompson D.A.W. On Growth and Form (1917), Cambridge University Press
2. Ingber D.E. The riddle of morphogenesis: a question of solution chemistry or molecular cell engineering?. Cell 75 (1993) 1249-1252
3. Bereiter-Hahn J. Mechanics of crawling cells. Med. Eng. Phys. 27 (2005) 743-753
4. Eggert U.S., Mitchison T.J., and Field C.M. Animal cytokinesis: from parts list to mechanisms. Annu. Rev. Biochem. 75 (2006) 543-566
5. Paluch E., Sykes C., Prost J., and Bornens M. Dynamic modes of the cortical actomyosin gel during cell locomotion and division. Trends Cell Biol. 16 (2006) 5-10
6. Lammermann T., Bader B.L., Monkley S.J., Worbs T., Wedlich-Soldner R., Hirsch K., Keller M., Forster R., Critchley D.R., Fassler R., et al. Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature 453 (2008) 51-55
7. Vicente-Manzanares M., Zareno J., Whitmore L., Choi C.K., and Horwitz A.F. Regulation of protrusion, adhesion dynamics, and polarity by myosins IIA and IIB in migrating cells. J. Cell Biol. 176 (2007) 573-580
8. Martin A.C., Kaschube M., and Wieschaus E.F. Pulsed contractions of an actin-myosin network drive apical constriction. Nature 457 (2009) 495-499
9. Borisy G.G., and Svitkina T.M. Actin machinery: pushing the envelope. Curr. Opin. Cell Biol. 12 (2000) 104-112
10. Rafelski S.M., and Theriot J.A. Crawling toward a unified model of cell mobility: spatial and temporal regulation of actin dynamics. Annu. Rev. Biochem. 73 (2004) 209-239
11. Mitchison T.J., Charras G.T., and Mahadevan L. Implications of a poroelastic cytoplasm for the dynamics of animal cell shape. Semin. Cell Dev. Biol. 19 (2008) 215-223
12. Sheetz M.P., Sable J.E., and Döbereiner H.G. Continuous membrane-cytoskeleton adhesion requires continuous accommodation to lipid and cytoskeleton dynamics. Annu. Rev. Biophys. Biomol. Struct. 35 (2006) 417-434
13. Keren K., Pincus Z., Allen G.M., Barnhart E.L., Marriott G., Mogilner A., and Theriot J.A. Mechanism of shape determination in motile cells. Nature 453 (2008) 475-480
14. Effler J.C., Kee Y.S., Berk J.M., Tran M.N., Iglesias P.A., and Robinson D.N. Mitosis-specific mechanosensing and contractile-protein redistribution control cell shape. Curr. Biol. 16 (2006) 1962-1967
15. Ingber D.E. Tensegrity I. Cell structure and hierarchical systems biology. J. Cell Sci. 116 (2003) 1157-1173
16. Thery M., and Bornens M. Cell shape and cell division. Curr. Opin. Cell Biol. 18 (2006) 648-657
17. Blaser H., Reichman-Fried M., Castanon I., Dumstrei K., Marlow F.L., Kawakami K., Solnica-Krezel L., Heisenberg C.P., and Raz E. Migration of zebrafish primordial germ cells: a role for myosin contraction and cytoplasmic flow. Dev Cell 11 (2006) 613-627
18. Kunwar P.S., Siekhaus D.E., and Lehmann R. In vivo migration: a germ cell perspective. Annu. Rev. Cell. Dev. Biol. 22 (2006) 237-265
19. Fraser S.E., and Harland R.M. The molecular metamorphosis of experimental embryology. Cell 100 (2000) 41-55
20. Scott M.P. Development: the natural history of genes. Cell 100 (2000) 27-40
21. Montell D.J. Morphogenetic cell movements: diversity from modular mechanical properties. Science 322 (2008) 1502-1505
22. Lecuit T., and Lenne P.F. Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nat. Rev. Mol. Cell. Biol. 8 (2007) 633-644
23. Farhadifar R., Roper J.C., Aigouy B., Eaton S., and Julicher F. The influence of cell mechanics, cell-cell interactions, and proliferation on epithelial packing. Curr. Biol. 17 (2007) 2095-2104
24. Hutson M.S., Tokutake Y., Chang M.S., Bloor J.W., Venakides S., Kiehart D.P., and Edwards G.S. Forces for morphogenesis investigated with laser microsurgery and quantitative modeling. Science 300 (2003) 145-149
25. Rauzi M., Verant P., Lecuit T., and Lenne P.F. Nature and anisotropy of cortical forces orienting Drosophila tissue morphogenesis. Nat. Cell. Biol. 10 (2008) 1401-1410
26. Toyama Y., Peralta X.G., Wells A.R., Kiehart D.P., and Edwards G.S. Apoptotic force and tissue dynamics during Drosophila embryogenesis. Science 321 (2008) 1683-1686
27. Davidson L., von Dassow M., and Zhou J. Multi-scale mechanics from molecules to morphogenesis. Int. J. Biochem. Cell Biol. (2009) 10.1016/j.biocel.2009.04.015
28. Yeung A., and Evans E. Cortical shell-liquid core model for passive flow of liquid-like spherical cells into micropipets. Biophys J. 56 (1989) 139-149
29. Hochmuth R.M. Micropipette aspiration of living cells. J. Biomech. 33 (2000) 15-22
30. Dai J., Ting-Beall H.P., Hochmuth R.M., Sheetz M.P., and Titus M.A. Myosin I contributes to the generation of resting cortical tension. Biophys. J. 77 (1999) 1168-1176
31. Lomakina E.B., Spillmann C.M., King M.R., and Waugh R.E. Rheological analysis and measurement of neutrophil indentation. Biophys. J. 87 (2004) 4246-4258
32. Krieg M., Arboleda-Estudillo Y., Puech P.H., Kafer J., Graner F., Muller D.J., and Heisenberg C.P. Tensile forces govern germ-layer organization in zebrafish. Nat. Cell. Biol. 10 (2008) 429-436
33. Liu X.H., and Wang X. The deformation of an adherent leukocyte under steady shear flow: a numerical study. J. Biomech. 37 (2004) 1079-1085
34. Caille N., Thoumine O., Tardy Y., and Meister J.J. Contribution of the nucleus to the mechanical properties of endothelial cells. J. Biomech. 35 (2002) 177-187
35. Riveline D., Zamir E., Balaban N.Q., Schwarz U.S., Ishizaki T., Narumiya S., Kam Z., Geiger B., and Bershadsky A.D. Focal contacts as mechanosensors: externally applied local mechanical force induces growth of focal contacts by an mDia1-dependent and ROCK-independent mechanism. J. Cell Biol. 153 (2001) 1175-1186
36. Brodland W.G., and Chen H.H. The mechanics of cell sorting and envelopment. J. Biomech. 33 (2000) 845-851
37. Janmey P.A., and McCulloch C.A. Cell mechanics: integrating cell responses to mechanical stimuli. Annu. Rev. Biomed. Eng. 9 (2007) 1-34
38. Tabdanov E., Borghi N., Brochard-Wyart F., Dufour S., and Thiery J.P. Role of E-cadherin in membrane-cortex interaction probed by nanotube extrusion. Biophys. J. 96 (2009) 2457-2465
39. Balaban N.Q., Schwarz U.S., Riveline D., Goichberg P., Tzur G., Sabanay I., Mahalu D., Safran S., Bershadsky A., Addadi L., et al. Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates. Nat. Cell Biol. 3 (2001) 466-472
40. Wang N., and Ingber D.E. Control of cytoskeletal mechanics by extracellular matrix, cell shape, and mechanical tension. Biophys. J. 66 (1994) 2181-2189
41. Oates A.C., Gorfinkiel N., Gonzalez-Gaitan M., and Heisenberg C.P. Quantitative approaches in developmental biology. Nat. Rev. Genet. 10 (2009) 517-530
42. Steinberg M.S. Reconstruction of tissues by dissociated cells. Some morphogenetic tissue movements and the sorting out of embryonic cells may have a common explanation. Science 141 (1963) 401-408
43. Foty R.A., Pfleger C.M., Forgacs G., and Steinberg M.S. Surface tensions of embryonic tissues predict their mutual envelopment behavior. Development 122 (1996) 1611-1620
44. Foty R.A., and Steinberg M.S. The differential adhesion hypothesis: a direct evaluation. Dev. Biol. 278 (2005) 255-263
45. Bertet C., Sulak L., and Lecuit T. Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature 429 (2004) 667-671
46. Blankenship J.T., Backovic S.T., Sanny J.S., Weitz O., and Zallen J.A. Multicellular rosette formation links planar cell polarity to tissue morphogenesis. Dev. Cell 11 (2006) 459-470
47. Wei Y., and Mikawa T. Formation of the avian primitive streak from spatially restricted blastoderm: evidence for polarized cell division in the elongating streak. Development 127 (2000) 87-96
48. da Silva S.M., and Vincent J.P. Oriented cell divisions in the extending germband of Drosophila. Development 134 (2007) 3049-3054
49. Gong Y., Mo C., and Fraser S.E. Planar cell polarity signalling controls cell division orientation during zebrafish gastrulation. Nature 430 (2004) 689-693
50. Ridley A.J., Schwartz M.A., Burridge K., Firtel R.A., Ginsberg M.H., Borisy G., Parsons J.T., and Horwitz A.R. Cell migration: integrating signals from front to back. Science 302 (2003) 1704-1709
51. Paluch E., and Charras G.T. Blebs lead the way: how to migrate without lamellipodia. Nat. Rev. Mol. Cell Biol. 9 (2008) 730-736
52. Lauffenburger D.A., and Horwitz A.F. Cell migration: a physically integrated molecular process. Cell 84 (1996) 359-369
53. Mitchison T.J., and Cramer L.P. Actin-based cell motility and cell locomotion. Cell 84 (1996) 371-379
54. Giannone G., Dubin-Thaler B.J., Rossier O., Cai Y., Chaga O., Jiang G., Beaver W., Dobereiner H.G., Freund Y., Borisy G., et al. Lamellipodial actin mechanically links myosin activity with adhesion-site formation. Cell 128 (2007) 561-575
55. Palecek S.P., Loftus J.C., Ginsberg M.H., Lauffenburger D.A., and Horwitz A.F. Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. Nature 385 (1997) 537-540
56. Bellion A., Baudoin J.-P., Alvarez C., Bornens M., and Metin C. Nucleokinesis in tangentially migrating neurons comprises two alternating phases: forward migration of the Golgi/centrosome associated with centrosome splitting and myosin contraction at the rear. J. Neurosci. 25 (2005) 5691-5699
57. Pollard T.D., and Borisy G.G. Cellular motility driven by assembly and disassembly of actin filaments. Cell 112 (2003) 453-465
58. Kunwar P.S., Sano H., Renault A.D., Barbosa V., Fuse N., and Lehmann R. Tre1 GPCR initiates germ cell transepithelial migration by regulating Drosophila melanogaster E-cadherin. J. Cell. Biol. 183 (2008) 157-168
59. Friedl P., and Gilmour D. Collective cell migration in morphogenesis, regeneration and cancer. Nat. Rev. Mol. Cell Biol. 10 (2009) 445-457
60. Melani M., Simpson K.J., Brugge J.S., and Montell D. Regulation of cell adhesion and collective cell migration by hindsight and its human homolog RREB1. Curr. Biol. 18 (2008) 532-537
61. McDonald J.A., Khodyakova A., Aranjuez G., Dudley C., and Montell D.J. PAR-1 kinase regulates epithelial detachment and directional protrusion of migrating border cells. Curr. Biol. 18 (2008) 1659-1667
62. Niewiadomska P., Godt D., and Tepass U. DE-Cadherin is required for intercellular motility during Drosophila oogenesis. J. Cell Biol. 144 (1999) 533-547
63. Chen X., and Gumbiner B.M. Paraxial protocadherin mediates cell sorting and tissue morphogenesis by regulating C-cadherin adhesion activity. J. Cell Biol. 174 (2006) 301-313
64. Zhong Y., Brieher W.M., and Gumbiner B.M. Analysis of C-cadherin regulation during tissue morphogenesis with an activating antibody. J. Cell Biol. 144 (1999) 351-359
65. Wacker S., Grimm K., Joos T., and Winklbauer R. Development and control of tissue separation at gastrulation in Xenopus. Dev. Biol. 224 (2000) 428-439
66. Medina A., Swain R.K., Kuerner K.M., and Steinbeisser H. Xenopus paraxial protocadherin has signaling functions and is involved in tissue separation. EMBO J. 23 (2004) 3249-3258
67. Unterseher F., Hefele J.A., Giehl K., De Robertis E.M., Wedlich D., and Schambony A. Paraxial protocadherin coordinates cell polarity during convergent extension via Rho A and JNK. EMBO J. 23 (2004) 3259-3269
68. Nandadasa S., Tao Q., Menon N.R., Heasman J., and Wylie C. N- and E-cadherins in Xenopus are specifically required in the neural and non-neural ectoderm, respectively, for F-actin assembly and morphogenetic movements. Development 136 (2009) 1327-1338
69. Marsden M., and DeSimone D.W. Integrin-ECM interactions regulate cadherin-dependent cell adhesion and are required for convergent extension in Xenopus. Curr. Biol. 13 (2003) 1182-1191
70. Dzamba B.J., Jakab K.R., Marsden M., Schwartz M.A., and DeSimone D.W. Cadherin adhesion, tissue tension, and noncanonical Wnt signaling regulate fibronectin matrix organization. Dev. Cell 16 (2009) 421-432
71. Davidson L.A., Marsden M., Keller R., and Desimone D.W. Integrin alpha5beta1 and fibronectin regulate polarized cell protrusions required for Xenopus convergence and extension. Curr. Biol. 16 (2006) 833-844
72. Somogyi K., and Rorth P. Evidence for tension-based regulation of Drosophila MAL and SRF during invasive cell migration. Dev. Cell 7 (2004) 85-93
73. Lecaudey V., Cakan-Akdogan G., Norton W.H., and Gilmour D. Dynamic Fgf signaling couples morphogenesis and migration in the zebrafish lateral line primordium. Development 135 (2008) 2695-2705
74. Aman A., and Piotrowski T. Wnt/beta-catenin and Fgf signaling control collective cell migration by restricting chemokine receptor expression. Dev. Cell 15 (2008) 749-761
75. Nechiporuk A., and Raible D.W. FGF-dependent mechanosensory organ patterning in zebrafish. Science 320 (2008) 1774-1777
76. Bianco A., Poukkula M., Cliffe A., Mathieu J., Luque C.M., Fulga T.A., and Rorth P. Two distinct modes of guidance signalling during collective migration of border cells. Nature 448 (2007) 362-365
77. McDonald J.A., Pinheiro E.M., and Montell D.J. PVF1, a PDGF/VEGF homolog, is sufficient to guide border cells and interacts genetically with Taiman. Development 130 (2003) 3469-3478
78. Montero J.A., Kilian B., Chan J., Bayliss P.E., and Heisenberg C.P. Phosphoinositide 3-kinase is required for process outgrowth and cell polarization of gastrulating mesendodermal cells. Curr. Biol. 13 (2003) 1279-1289
79. Nagel M., Tahinci E., Symes K., and Winklbauer R. Guidance of mesoderm cell migration in the Xenopus gastrula requires PDGF signaling. Development 131 (2004) 2727-2736
80. Yang X., Chrisman H., and Weijer C.J. PDGF signalling controls the migration of mesoderm cells during chick gastrulation by regulating N-cadherin expression. Development 135 (2008) 3521-3530
81. Simons M., and Mlodzik M. Planar cell polarity signaling: from fly development to human disease. Annu. Rev. Genet. 42 (2008) 517-540
82. Tada M., and Kai M. Noncanonical Wnt/PCP signaling during vertebrate gastrulation. Zebrafish 6 (2009) 29-40
83. Bastock R., and Strutt D. The planar polarity pathway promotes coordinated cell migration during Drosophila oogenesis. Development 134 (2007) 3055-3064
84. Marlow F., Topczewski J., Sepich D., and Solnica-Krezel L. Zebrafish rho kinase 2 acts downstream of wnt11 to mediate cell polarity and effective convergence and extension movements. Curr. Biol. 12 (2002) 876-884
85. Ulrich F., Krieg M., Schotz E.M., Link V., Castanon I., Schnabel V., Taubenberger A., Mueller D., Puech P.H., and Heisenberg C.P. Wnt11 functions in gastrulation by controlling cell cohesion through Rab5c and E-cadherin. Dev. Cell 9 (2005) 555-564
86. Wodarz A., Stewart D.B., Nelson W.J., and Nusse R. Wingless signaling modulates cadherin-mediated cell adhesion in Drosophila imaginal disc cells. J. Cell. Sci. 119 (2006) 2425-2434
87. Winter C.G., Wang B., Ballew A., Royou A., Karess R., Axelrod J.D., and Luo L. Drosophila Rho-associated kinase (Drok) links Frizzled-mediated planar cell polarity signaling to the actin cytoskeleton. Cell 105 (2001) 81-91
88. Silver D.L., and Montell D.J. Paracrine signaling through the JAK/STAT pathway activates invasive behavior of ovarian epithelial cells in Drosophila. Cell 107 (2001) 831-841
89. Beccari S., Teixeira L., and Rorth P. The JAK/STAT pathway is required for border cell migration during Drosophila oogenesis. Mech. Dev. 111 (2002) 115-123
90. Yamashita S., Miyagi C., Carmany-Rampey A., Shimizu T., Fujii R., Schier A.F., and Hirano T. Stat3 controls cell movements during zebrafish gastrulation. Dev. Cell 2 (2002) 363-375
91. Miyagi C., Yamashita S., Ohba Y., Yoshizaki H., Matsuda M., and Hirano T. STAT3 noncell-autonomously controls planar cell polarity during zebrafish convergence and extension. J. Cell Biol. 166 (2004) 975-981
92. Leptin M. Gastrulation in Drosophila: the logic and the cellular mechanisms. EMBO J. 18 (1999) 3187-3192
93. Jacinto A., Woolner S., and Martin P. Dynamic analysis of dorsal closure in Drosophila: from genetics to cell biology. Dev. Cell 3 (2002) 9-19
94. Solon J., Kaya A., Colombelli J., and Brunner D. Pulsed forces timed by a ratchet-like mechanism drive directed tissue movement during dorsal closure. Cell 137 (2009) 1183-1185
95. Keller R. Shaping the vertebrate body plan by polarized embryonic cell movements. Science 298 (2002) 1950-1954
96. Rolo A., Skoglund P., and Keller R. Morphogenetic movements driving neural tube closure in Xenopus require myosin IIB. Dev. Biol. 327 (2009) 327-338
97. Skoglund P., Rolo A., Chen X., Gumbiner B.M., and Keller R. Convergence and extension at gastrulation require a myosin IIB-dependent cortical actin network. Development 135 (2008) 2435-2444
98. Blanchard G.B., Kabla A.J., Schultz N.L., Butler L.C., Sanson B., Gorfinkiel N., Mahadevan L., and Adams R.J. Tissue tectonics: morphogenetic strain rates, cell shape change and intercalation. Nat. Methods 6 (2009) 458-464
99. Gorfinkiel N., Blanchard G.B., Adams R.J., and Martinez-Arias A. Mechanical control of global cell behaviour during dorsal closure in Drosophila. Development 136 (2009) 1889-1898
100. Butler L.C., Blanchard G.B., Kabla A.J., Lawrence N.J., Welchman D.P., Mahadevan L., Adams R.J., and Sanson B. Cell shape changes indicate a role for extrinsic tensile forces in Drosophila germ-band extension. Nat. Cell Biol. 11 (2009) 859-864
101. Riedel-Kruse I.H., Muller C., and Oates A.C. Synchrony dynamics during initiation, failure, and rescue of the segmentation clock. Science 317 (2007) 1911-1915
102. Reichman-Fried M., Minina S., and Raz E. Autonomous modes of behavior in primordial germ cell migration. Dev. Cell 6 (2004) 589-596
103. Thorpe J.L., Doitsidou M., Ho S.Y., Raz E., and Farber S.A. Germ cell migration in zebrafish is dependent on HMGCoA reductase activity and prenylation. Dev. Cell 6 (2004) 295-302
104. Haas P., and Gilmour D. Chemokine signaling mediates self-organizing tissue migration in the zebrafish lateral line. Dev. Cell 10 (2006) 673-680
105. Paluch E., and Heisenberg C.-P. Chaos begets order: asynchronous cell contractions drive epithelial morphogenesis. Dev. Cell 16 (2009) 4-6
106. Helenius J., Heisenberg C.P., Gaub H.E., and Muller D.J. Single-cell force spectroscopy. J. Cell Sci. 121 (2008) 1785-1791
107. Evans E., Ritchie K., and Merkel R. Sensitive force technique to probe molecular adhesion and structural linkages at biological interfaces. Biophys. J. 68 (1995) 2580-2587
108. Sung K.-L.P., Sung L.A., Crimmins M., Burakoff S.J., and Chien S. Determination of junction avidity of cytolytic T cell and target cell. Science 234 (1986) 1405-1408
109. Chu Y.S., Thomas W.A., Eder O., Pincet F., Perez E., Thiery J.P., and Dufour S. Force measurements in E-cadherin-mediated cell doublets reveal rapid adhesion strengthened by actin cytoskeleton remodeling through Rac and Cdc42. J. Cell. Biol. 167 (2004) 1183-1194
110. Benoit M., Gabriel D., Gerisch G., and Gaub H.E. Discrete interactions in cell adhesion measured by single-molecule force spectroscopy. Nat. Cell Biol. 2 (2000) 313-317
111. Kucik D.F. Measurement of adhesion under flow conditions. Curr. Protoc. Cell Biol. (2009) Chapter 9, Unit 9.6
112. Puech P.H., Taubenberger A., Ulrich F., Krieg M., Muller D.J., and Heisenberg C.P. Measuring cell adhesion forces of primary gastrulating cells from zebrafish using atomic force microscopy. J. Cell Sci. 118 (2005) 4199-4206
113. Litvinov R.I., Shuman H., Bennett J.S., and Weisel J.W. Binding strength and activation state of single fibrinogen-integrin pairs on living cells. Proc. Natl. Acad. Sci. USA 99 (2002) 7426-7431
114. Evans E., and Yeung A. Apparent viscosity and cortical tension of blood granulocytes determined by micropipet aspiration. Biophys. J. 56 (1989) 151-160
115. Wu H.W., T,K, and Moy V.T. Mechanical properties of L929 cells measured by atomic force microscopy: effects of anticytoskeletal drugs and membrane crosslinking. Scanning 20 (1998) 389-397
116. Thoumine O., and Ott A. Time scale dependent viscoelastic and contractile regimes in fobroblasts probed by microplate manipulation. J. Cell Sci. 110 (1997) 2109-2116
117. Guck J., Ananthakrishnan R., Mahmood H., Moon T.J., Cunningham C.C., and Kas J. The optical stretcher: a novel laser tool to micromanipulate cells. Biophys. J. 81 (2001) 767-784