Turing's next steps: The mechanochemical basis of morphogenesis

Nature Reviews Molecular Cell Biology

Volumn 12, Issue 6, 2011, Pages 400-406

  Howard, Jonathon ^a   Grill, Stephan W ^a,b   Bois, Justin S ^c  

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

^b MAX PLANCK INSTITUT FÜR PHYSIK KOMPLEXER SYSTEME   (Germany)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; MOLECULAR MOTOR; MORPHOGEN; MYOSIN;

CELL SHAPE; CHEMICAL REACTION; DIFFUSION; EMBRYO DEVELOPMENT; FRICTION; MECHANOTRANSDUCTION; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SPATIAL ORIENTATION; STRESS; TISSUE TYPES; VISCOELASTICITY;

ANIMALS; CELL DIFFERENTIATION; DIFFUSION; MODELS, BIOLOGICAL; MOLECULAR MOTOR PROTEINS; MORPHOGENESIS; SIGNAL TRANSDUCTION;

EID: 79957474426     PISSN: 14710072     EISSN: 14710080     Source Type: Journal    
DOI: 10.1038/nrm3120     Document Type: Review

References (57)

1. Turing, A. M. The chemical basis of morphogenesis. Proc. R. Soc. Lond. B Biol. Sci. 237, 37-72 (1952).
2. Gierer, A. & Meinhardt, H. A theory of biological pattern formation. Kybernetik 12, 30-39 (1972).
3. Wolpert, L. Positional information and the spatial pattern of cellular differentiation. J. Theor. Biol. 25, 1-47 (1969).
4. Frohnhěr, H. N. C. & Nslein-Volhard, C. Organization of the anterior pattern in the Drosophila embryo by the maternal gene bicoid. Nature 324, 120-125 (1986).
5. Kondo, S. & Miura, T. Reaction-diffusion model as a framework for understanding biological pattern formation. Science 329, 1616-1620 (2010).
6. Huxley, A. F. & Niedergerke, R. Structural changes in muscle during contraction. Interference microscopy of living cells. Nature 173, 971-976 (1954).
7. Huxley, H. E. & Hanson, J. Changes in the cross-striations of muscle during contraction and stretch and their structural interpretion. Nature 173, 973-976 (1954).
8. Gibbons, I. R. & Rowe, A. J. Dynein: A protein with adenosine triphosphatase activity from cilia. Science 149, 424-426 (1965).
9. Brady, S. T. A novel brain ATPase with properties expected for the fast axonal transport motor. Nature 317, 73-75 (1985). (Pubitemid 15016692)
10. Vale, R. D., Reese, T. S. & Sheetz, M. P. Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility. Cell 42, 39-50 (1985). (Pubitemid 16237554)
11. Crick, F. Diffusion in embryogenesis. Nature 225, 420-422 (1970).
12. Howard, J. Mechanics of Motor Proteins and the Cytoskeleton (Sinauer Associates, Sunderland, Massachusetts, 2001).
13. Luby-Phelps, K. Cytoarchitecture and physical properties of cytoplasm: Volume, viscosity, diffusion, intracellular surface area. Int. Rev. Cytol. 192, 189-221 (2000). (Pubitemid 29501953)
14. Helenius, J., Brouhard, G., Kalaidzidis, Y., Diez, S. & Howard, J. The depolymerizing kinesin MCAK uses lattice diffusion to rapidly target microtubule ends. Nature 441, 115-119 (2006).
15. Gutzeit, H. O. & Koppa, R. Time-lapse film analysis of cytoplasmic streaming during late oogenesis of Drosophila. J. Embryol. Exp. Morphol. 67, 101-111 (1982). (Pubitemid 12177043)
16. Goldstein, R. E., Tuval, I. & van de Meent, J.-W. Microfluidics of cytoplasmic streaming and its implications for intracellular transport. Proc. Natl Acad. Sci. USA 105, 3663-3667 (2008). (Pubitemid 351723454)
17. Short, M. B. et al. Flows driven by flagella of multicellular organisms enhance long-range molecular transport. Proc. Natl Acad. Sci. USA 103, 8315-8319 (2006). (Pubitemid 43838452)
18. Baas, P. W., Deitch, J. S., Black, M. M. & Banker, G. A. Polarity orientation of microtubules in hippocampal neurons: Uniformity in the axon and nonuniformity in the dendrite. Proc. Natl Acad. Sci. USA 85, 8335-8339 (1988).
19. Snider, J. et al. Intracellular actin-based transport: How far you go depends on how often you switch. Proc. Natl Acad. Sci. USA 101, 13204-13209 (2004). (Pubitemid 39209643)
20. Zimyanin, V. L. et al. In vivo imaging of oskar mRNA transport reveals the mechanism of posterior localization. Cell 134, 843-853 (2008).
21. Wilhelm, C. Out-of-equilibrium microrheology inside living cells. Phys. Rev. Lett. 101, 028101 (2008).
22. Engler, A. J., Sen, S., Sweeney, H. L. & Discher, D. E. Matrix elasticity directs stem cell lineage specification. Cell 126, 677-689 (2006). (Pubitemid 44233625)
23. Mayer, M., Depken, M., Bois, J. S., Jicher, F. & Grill, S. W. Anisotropies in cortical tension reveal the physical basis of polarizing cortical flows. Nature 467, 617-621 (2010).
24. Rauzi, M., Lenne, P.-F. & Lecuit, T. Planar polarized actomyosin contractile flows control epithelial junction remodelling. Nature 468, 1110-1114 (2010).
25. Zerzour, R., Kroeger, J. & Geitmann, A. Polar growth in pollen tubes is associated with spatially confined dynamic changes in cell mechanical properties. Dev. Biol. 334, 437-446 (2009).
26. Howard, J. Mechanical signaling in networks of motor and cytoskeletal proteins. Annu. Rev. Biophys. 38, 217-234 (2009).
27. Vogel, V. & Sheetz, M. Local force and geometry sensing regulate cell functions. Nature Rev. Mol. Cell Biol. 7, 265-275 (2006).
28. Brown, G. C. & Kholodenko, B. N. Spatial gradients of cellular phospho-proteins. FEBS Lett. 457, 452-454 (1999). (Pubitemid 29414741)
29. Wartlick, O., Kicheva, A. & Gonzěz-Gait, M. Morphogen gradient formation. Cold Spring Harb. Perspect. Biol. 1, a001255 (2009).
30. Kalab, P., Weis, K. & Heald, R. Visualization of a Ran-GTP gradient in interphase and mitotic Xenopus egg extracts. Science 295, 2452-2456 (2002). (Pubitemid 34270259)
31. Caudron, M., Bunt, G., Bastiaens, P. & Karsenti, E. Spatial coordination of spindle assembly by chromosome-mediated signaling gradients. Science 309, 1373-1376 (2005). (Pubitemid 41209364)
32. Kicheva, A. et al. Kinetics of morphogen gradient formation. Science 315, 521-525 (2007). (Pubitemid 46175757)
33. Belenkaya, T. Y. et al. Drosophila Dpp morphogen movement is independent of dynamin-mediated endocytosis but regulated by the glypican members of heparan sulfate proteoglycans. Cell 119, 231-244 (2004). (Pubitemid 39360905)
34. Yu, S. R. et al. Fgf8 morphogen gradient forms by a source-sink mechanism with freely diffusing molecules. Nature 461, 533-536 (2009).
35. Driever, W. & Nslein-Volhard, C. A gradient of bicoid protein in Drosophila embryos. Cell 54, 83-93 (1988).
36. Gregor, T., Bialek, W., de Ruyter van Steveninck, R. R., Tank, D. W. & Wieschaus, E. F. Diffusion and scaling during early embryonic pattern formation. Proc. Natl Acad. Sci. USA 102, 18403-18407 (2005). (Pubitemid 43011238)
37. Gregor, T., Wieschaus, E. F., McGregor, A. P., Bialek, W. & Tank, D. W. Stability and nuclear dynamics of the bicoid morphogen gradient. Cell 130, 141-152 (2007). (Pubitemid 47031319)
38. Spirov, A. et al. Formation of the bicoid morphogen gradient: An mRNA gradient dictates the protein gradient. Development 136, 605-614 (2009).
39. Abu-Arish, A., Porcher, A., Czerwonka, A., Dostatni, N. & Fradin, C. High mobility of Bicoid captured by fluorescence correlation spectroscopy: Implication for the rapid establishment of its gradient. Biophys. J. 99, L33-L35 (2010).
40. Meinhardt, H. The Algorithmic Beauty of Sea Shells (Springer, Berlin; London, 2009).
41. Nakamasu, A., Takahashi, G., Kanbe, A. & Kondo, S. Interactions between zebrafish pigment cells responsible for the generation of Turing patterns. Proc. Natl Acad. Sci. USA 106, 8429-8434 (2009).
42. Naoz, M., Manor, U., Sakaguchi, H., Kachar, B. & Gov, N. S. Protein localization by actin treadmilling and molecular motors regulates stereocilia shape and treadmilling rate. Biophys. J. 95, 5706-5718 (2008).
43. Manor, U. et al. Regulation of stereocilia length by myosin XVa and whirlin depends on the actin-regulatory protein Eps8. Curr. Biol. 21, 167-172 (2011).
44. Varga, V. et al. Yeast Kinesin-8 depolymerizes microtubules in a length-dependent manner. Nature Cell Biol. 8, 957-962 (2006). (Pubitemid 44314726)
45. Varga, V., Leduc, C., Bormuth, V., Diez, S. & Howard, J. Kinesin-8 motors act cooperatively to mediate length-dependent microtubule depolymerization. Cell 138, 1174-1183 (2009).
46. Howard, J. & Hyman, A. A. Microtubule polymerases and depolymerases. Curr. Opin. Cell Biol. 19, 31-35 (2007). (Pubitemid 46138038)
47. Mayr, M. et al. The human kinesin Kif18A is a motile microtubule depolymerase essential for chromosome congression. Curr. Biol. 17, 488-498 (2007). (Pubitemid 46401386)
48. Stumpff, J., Vondassow, G., Wagenbach, M., Asbury, C. & Wordeman, L. The Kinesin-8 motor Kif18A suppresses kinetochore movements to control mitotic chromosome alignment. Dev. Cell 14, 252-262 (2008). (Pubitemid 351189173)
49. Wargacki, M. M., Tay, J. C., Muller, E. G., Asbury, C. L. & Davis, T. N. Kip3, the yeast Kinesin-8, is required for clustering of kinetochores at metaphase. Cell Cycle 9, 2581-2588 (2010).
50. Salbreux, G., Prost, J. & Joanny, J.-F. Hydrodynamics of cellular cortical flows and the formation of contractile rings. Phys. Rev. Lett. 103, 058102 (2009).
51. Bois, J., Jülicher, F. & Grill, S. Pattern formation in active fluids. Phys. Rev. Lett. 106, 028103 (2011).
52. 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 7, 413-424 (2004). (Pubitemid 39232976)
53. David, D. J. V., Tishkina, A. & Harris, T. J. C. The PAR complex regulates pulsed actomyosin contractions during amnioserosa apical constriction in Drosophila. Development 137, 1645-1655 (2010).
54. Riedel-Kruse, I. H., Hilfinger, A., Howard, J. & Jülicher, F. How molecular motors shape the flagellar beat. HFSP J. 1, 192 (2007).
55. Aigouy, B. et al. Cell flow reorients the axis of planar polarity in the wing epithelium of Drosophila. Cell 142, 773-786 (2010).
56. Hamant, O. et al. Developmental patterning by mechanical signals in Arabidopsis. Science 322, 1650-1655 (2008).
57. Schneider, M. E., Dosé, A. C., Salles, F. T., Chang, W. et al. A new compartment at stereocilia tips defined by spatial and temporal patterns of myosin IIIa expression. J. Neurosci. 26, 10243-10252 (2006). (Pubitemid 44527418)