Origin and function of fluctuations in cell behaviour and the emergence of patterns

Seminars in Cell and Developmental Biology

Volumn 20, Issue 7, 2009, Pages 877-884

  Mateus, Ana M ^a,b   Gorfinkiel, Nicole ^a   Arias, Alfonso Martinez ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

Author keywords

Adhesion; Cytoskeleton; Fluctuations; Morphogenesis; Planar cell polarity

Indexed keywords

CADHERIN; INTEGRIN; MYOSIN; WNT PROTEIN;

CAENORHABDITIS ELEGANS; CELL ADHESION; CELL FATE; CELL FUNCTION; CELL HETEROGENEITY; CELL MATURATION; CHLAMYDOMONAS; CYTOSKELETON; DICTYOSTELIUM; DROSOPHILA; ESCHERICHIA COLI; GASTRULATION; GENETIC ANALYSIS; MICROTUBULE; MOLECULAR GENETICS; MORPHOGENESIS; NONHUMAN; POLARIZATION; REVIEW; XENOPUS; ZEBRA FISH;

EID: 70349336677     PISSN: 10849521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.semcdb.2009.07.009     Document Type: Review

References (85)

1. Wolpert L. Principles of development. 3rd ed. (2006), Oxford University Press, Oxford
2. Steinberg M.S., and Takeichi M. Experimental specification of cell sorting, tissue spreading, and specific spatial patterning by quantitative differences in cadherin expression. Proc Natl Acad Sci USA 91 (1994) 206-209
3. Ide H., Yokoyama H., Endo T., Omi M., Tamura K., and Wada N. Pattern formation in dissociated limb bud mesenchyme in vitro and in vivo. Wound Repair Regen 6 (1998) 398-402
4. Edelman G.M. Topobiology (1988), Basic Books Inc., New York
5. Myers D.C., Sepich D.S., and Solnica-Krezel L. Convergence and extension in vertebrate gastrulae: cell movements according to or in search of identity?. Trends Genet 18 (2002) 447-455
6. Keller R., Shook D., and Skoglund P. The forces that shape embryos: physical aspects of convergent extension by cell intercalation. Phys Biol 5 (2008) 15007
7. Leier A. Systems biology (IV) multi-scale and spatial modelling (2006). http://www.itee.uq.edu.au/~comp4006/Systems%2520Biology4.pdf Available from: http://www.itee.uq.edu.au/∼comp4006/Systems%20Biology4.pdf.
8. Goldman R.D., Grin B., Mendez M.G., and Kuczmarski E.R. Intermediate filaments: versatile building blocks of cell structure. Curr Opin Cell Biol 20 (2008) 28-34
9. Pollard T.D., and Borisy G.G. Cellular motility driven by assembly and disassembly of actin filaments. Cell 112 (2003) 453-465
10. Desai A.T., and Mitchison J. Microtubule polymerization dynamics. Annu Rev Cell Dev Biol 13 (1997) 83-117
11. Nedelec F.J., Surrey T., Maggs A.C., and Leibler S. Self-organization of microtubules and motors. Nature 389 (1997) 305-308
12. Surrey T., Nedelec F., Leibler S., and Karsenti E. Physical properties determining self-organization of motors and microtubules. Science 292 (2001) 1167-1171
13. Nedelec F., Surrey T., and Karsenti E. Self-organisation and forces in the microtubule cytoskeleton. Curr Opin Cell Biol 15 (2003) 118-124
14. Backouche F., Haviv L., Groswasser D., and Bernheim-Groswasser A. Active gels: dynamics of patterning and self-organization. Phys Biol 3 (2006) 264-273
15. Bendix P.M., Koenderink G.H., Cuvelier D., Dogic Z., Koeleman B.N., Brieher W.M., et al. A quantitative analysis of contractility in active cytoskeletal protein networks. Biophys J 94 (2008) 3126-3136
16. Pinot M., Chesnel F., Kubiak J.Z., Arnal I., Nedelec F.J., and Gueroui Z. Effects of confinement on the self-organization of microtubules and motors. Curr Biol 19 (2009) 954-960
17. Welch M.D., and Mullins R.D. Cellular control of actin nucleation. Annu Rev Cell Dev Biol 18 (2002) 247-288
18. Salbreux G., Joanny J.F., Prost J., and Pullarkat P. Shape oscillations of non-adhering fibroblast cells. Phys Biol 4 (2007) 268-284
19. Bornens M., Paintrand M., and Celati C. The cortical microfilament system of lymphoblasts displays a periodic oscillatory activity in the absence of microtubules: implications for cell polarity. J Cell Biol 109 (1989) 1071-1083
20. Pletjushkina O.J., Rajfur Z., Pomorski P., Oliver T.N., Vasiliev J.M., and Jacobson K.A. Induction of cortical oscillations in spreading cells by depolymerization of microtubules. Cell Motil Cytoskeleton 48 (2001) 235-244
21. Paluch E., Piel M., Prost J., Bornens M., and Sykes C. Cortical actomyosin breakage triggers shape oscillations in cells and cell fragments. Biophys J 89 (2005) 724-733
22. Turing A.M. The chemical basis of morphogenesis. Phil Trans R Soc London B 237 (1952) 37-72
23. Wedlich-Soldner R., and Li R. Spontaneous cell polarization: undermining determinism. Nat Cell Biol 5 (2003) 267-270
24. Verkhovsky A.B., Svitkina T.M., and Borisy G.G. Self-polarization and directional motility of cytoplasm. Curr Biol 9 (1999) 11-20
25. Thery M., Racine V., Piel M., Pepin A., Dimitrov A., Chen Y., et al. Anisotropy of cell adhesive microenvironment governs cell internal organization and orientation of polarity. Proc Natl Acad Sci USA 103 (2006) 19771-19776
26. Georgiou M., Marinari E., Burden J., and Baum B. Cdc42, Par6, and aPKC regulate Arp2/3-mediated endocytosis to control local adherens junction stability. Curr Biol 18 (2008) 1631-1638
27. Leibfried A., Fricke R., Morgan M.J., Bogdan S., and Bellaiche Y. Drosophila Cip4 and WASp define a branch of the Cdc42-Par6-aPKC pathway regulating E-cadherin endocytosis. Curr Biol 18 (2008) 1639-1648
28. Dawes-Hoang R.E., Parmar K.M., Christiansen A.E., Phelps C.B., Brand A.H., and Wieschaus E.F. folded gastrulation, cell shape change and the control of myosin localization. Development 132 (2005) 4165-4178
29. Friedl P., and Gilmour D. Collective cell migration in morphogenesis, regeneration and cancer. Nat Rev Mol Cell Biol 10 (2009) 445-457
30. Colas J.F., and Schoenwolf G.C. Towards a cellular and molecular understanding of neurulation. Dev Dyn 221 (2001) 117-145
31. Montell D.J. Morphogenetic cell movements: diversity from modular mechanical properties. Science 322 (2008) 1502-1505
32. Siu C.H., Harris T.J., Wang J., and Wong E. Regulation of cell-cell adhesion during Dictyostelium development. Semin Cell Dev Biol 15 (2004) 633-641
33. Haas P., and Gilmour D. Chemokine signaling mediates self-organizing tissue migration in the zebrafish lateral line. Dev Cell 10 (2006) 673-680
34. Martin A.C., Kaschube M., and Wieschaus E.F. Pulsed contractions of an actin-myosin network drive apical constriction. Nature 457 (2009) 495-499
35. Kiehart D.P., Galbraith C.G., Edwards K.A., Rickoll W.L., and Montague R.A. Multiple forces contribute to cell sheet morphogenesis for dorsal closure in Drosophila. J Cell Biol 149 (2000) 471-490
36. Hutson M.S., Tokutake Y., Chang M.S., Bloor J.W., Venakides S., Kiehart D.P., et al. Forces for morphogenesis investigated with laser microsurgery and quantitative modeling. Science 300 (2003) 145-149
37. Solon J., Kaya-Copur A., Colombelli J., and Brunner D. Pulsed forces timed by a ratchet-like mechanism drive directed tissue movement during dorsal closure. Cell 137 (2009) 1331-1342
38. Gorfinkiel N., Blanchard G.B., Adams R.J., and Arias A.M. Mechanical control of global cell behaviour during dorsal closure in Drosophila. Development 136 (2009) 1889-1898
39. 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
40. Kafer J., Hayashi T., Maree A.F., Carthew R.W., and Graner F. Cell adhesion and cortex contractility determine cell patterning in the Drosophila retina. Proc Natl Acad Sci USA 104 (2007) 18549-18554
41. Hilgenfeldt S., Erisken S., and Carthew R.W. Physical modeling of cell geometric order in an epithelial tissue. Proc Natl Acad Sci USA 105 (2008) 907-911
42. Stern C.D. Gastrulation from cells to embryo (2004), Cold Spring Harbour Laboratory Press, New York
43. 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
44. Keller R.E., Danilchik M., Gimlich R., and Shih J. The function and mechanism of convergent extension during gastrulation of Xenopus laevis. J Embryol Exp Morphol 89 Suppl. (1985) 185-209
45. Yin C., Kiskowski M., Pouille P.A., Farge E., and Solnica-Krezel L. Cooperation of polarized cell intercalations drives convergence and extension of presomitic mesoderm during zebrafish gastrulation. J Cell Biol 180 (2008) 221-232
46. Kam Z., Minden J.S., Agard D.A., Sedat J.W., and Leptin M. Drosophila gastrulation: analysis of cell shape changes in living embryos by three-dimensional fluorescence microscopy. Development 112 (1991) 365-370
47. McMahon A., Supatto W., Fraser S.E., and Stathopoulos A. Dynamic analyses of Drosophila gastrulation provide insights into collective cell migration. Science 322 (2008) 1546-1550
48. Butler L.C., Blanchard G.B., Kabla A.J., Lawrence N.J., Welchman D.P., Mahadevan L., et al. Cell shape changes indicate a role for extrinsic tensile forces in Drosophila germ-band extension. Nat Cell Biol (2009)
49. Bertet C., Sulak L., and Lecuit T. Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature 429 (2004) 667-671
50. 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
51. Keller R. Shaping the vertebrate body plan by polarized embryonic cell movements. Science 298 (2002) 1950-1954
52. Solnica-Krezel L. Conserved patterns of cell movements during vertebrate gastrulation. Curr Biol 15 (2005) R213-R228
53. Yang X., Dormann D., Munsterberg A.E., and Weijer C.J. Cell movement patterns during gastrulation in the chick are controlled by positive and negative chemotaxis mediated by FGF4 and FGF8. Dev Cell 3 (2002) 425-437
54. Wilson R., Vogelsang E., and Leptin M. FGF signalling and the mechanism of mesoderm spreading in Drosophila embryos. Development 132 (2005) 491-501
55. Nutt S.L., Dingwell K.S., Holt C.E., and Amaya E. Xenopus Sprouty2 inhibits FGF-mediated gastrulation movements but does not affect mesoderm induction and patterning. Genes Dev 15 (2001) 1152-1166
56. Griffin K., Patient R., and Holder N. Analysis of FGF function in normal and no tail zebrafish embryos reveals separate mechanisms for formation of the trunk and the tail. Development 121 (1995) 2983-2994
57. Symes K., and Mercola M. Embryonic mesoderm cells spread in response to platelet-derived growth factor and signaling by phosphatidylinositol 3-kinase. Proc Natl Acad Sci USA 93 (1996) 9641-9644
58. 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
59. Cho N.K., Keyes L., Johnson E., Heller J., Ryner L., Karim F., et al. Developmental control of blood cell migration by the Drosophila VEGF pathway. Cell 108 (2002) 865-876
60. Duchek P., and Rorth P. Guidance of cell migration by EGF receptor signaling during Drosophila oogenesis. Science 291 (2001) 131-133
61. Zavadil J., and Bottinger E.P. TGF-beta and epithelial-to-mesenchymal transitions. Oncogene 24 (2005) 5764-5774
62. von der Hardt S., Bakkers J., Inbal A., Carvalho L., Solnica-Krezel L., Heisenberg C.P., et al. The Bmp gradient of the zebrafish gastrula guides migrating lateral cells by regulating cell-cell adhesion. Curr Biol 17 (2007) 475-487
63. Wada A., Kato K., Uwo M.F., Yonemura S., and Hayashi S. Specialized extraembryonic cells connect embryonic and extraembryonic epidermis in response to Dpp during dorsal closure in Drosophila. Dev Biol 301 (2007) 340-349
64. Fernandez B.G., Arias A.M., and Jacinto A. Dpp signalling orchestrates dorsal closure by regulating cell shape changes both in the amnioserosa and in the epidermis. Mech Dev 124 (2007) 884-897
65. Pouille P.A., Ahmadi P., Brunet A.C., and Farge E. Mechanical signals trigger Myosin II redistribution and mesoderm invagination in Drosophila embryos. Sci Signal 2 (2009) ra16
66. Eaton S. Planar polarization of Drosophila and vertebrate epithelia. Curr Opin Cell Biol 9 (1997) 860-866
67. Wharton Jr. K.A. Runnin' with the Dvl: proteins that associate with Dsh/Dvl and their significance to Wnt signal transduction. Dev Biol 253 (2003) 1-17
68. Simons M., and Mlodzik M. Planar cell polarity signaling: from fly development to human disease. Annu Rev Genet 42 (2008) 517-540
69. Classen A.K., Anderson K.I., Marois E., and Eaton S. Hexagonal packing of Drosophila wing epithelial cells by the planar cell polarity pathway. Dev Cell 9 (2005) 805-817
70. Ulrich F., Krieg M., Schotz E.M., Link V., Castanon I., Schnabel V., et al. Wnt11 functions in gastrulation by controlling cell cohesion through Rab5c and E-cadherin. Dev Cell 9 (2005) 555-564
71. Wallingford J.B., Rowning B.A., Vogeli K.M., Rothbacher U., Fraser S.E., and Harland R.M. Dishevelled controls cell polarity during Xenopus gastrulation. Nature 405 (2000) 81-85
72. Goto T., and Keller R. The planar cell polarity gene strabismus regulates convergence and extension and neural fold closure in Xenopus. Dev Biol 247 (2002) 165-181
73. Jessen J.R., Topczewski J., Bingham S., Sepich D.S., Marlow F., Chandrasekhar A., et al. Zebrafish trilobite identifies new roles for Strabismus in gastrulation and neuronal movements. Nat Cell Biol 4 (2002) 610-615
74. Gong Y., Mo C., and Fraser S.E. Planar cell polarity signalling controls cell division orientation during zebrafish gastrulation. Nature 430 (2004) 689-693
75. Goldstein B., Takeshita H., Mizumoto K., and Sawa H. Wnt signals can function as positional cues in establishing cell polarity. Dev Cell 10 (2006) 391-396
76. Heisenberg C.P., Tada M., Rauch G.J., Saude L., Concha M.L., Geisler R., et al. Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. Nature 405 (2000) 76-81
77. Nicolis G., and Prigogine I. Self organization in nonequilibrium systems (1977), Wiley, New York
78. Karsenti E. Self-organization in cell biology: a brief history. Nat Rev Mol Cell Biol 9 (2008) 255-262
79. 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
80. Mombach J.C., Glazier J.A., Raphael R.C., and Zajac M. Quantitative comparison between differential adhesion models and cell sorting in the presence and absence of fluctuations. Phys Rev Lett 75 (1995) 2244-2247
81. Arias A.M., and Hayward P. Filtering transcriptional noise during development: concepts and mechanisms. Nat Rev Genet 7 (2006) 34-44
82. Korobkova E., Emonet T., Vilar J.M., Shimizu T.S., and Cluzel P. From molecular noise to behavioural variability in a single bacterium. Nature 428 (2004) 574-578
83. Spudich J.L., and Koshland Jr. D.E. Non-genetic individuality: chance in the single cell. Nature 262 (1976) 467-471
84. Polin M., Tuval I., Drescher K., Gollub J.P., and Goldstein R.E. Chlamydomonas swims with two "gears" in a eukaryotic version of run-and-tumble locomotion. Science 325 (2009) 487-490
85. Samadani A., Mettetal J., and van Oudenaarden A. Cellular asymmetry and individuality in directional sensing. Proc Natl Acad Sci USA 103 (2006) 11549-11554