Skip to main content Accessibility help
×
Home

Clarifying tetrapod embryogenesis, a physicist's point of view

  • V. Fleury (a1)

Abstract

The origin of tetrapods is a complex question that webs together genetic, paleontological, developmental and physical facts. Basically, the development of embryos is described by a complex mix of mechanical movements and biochemical inductions of genetic origin. It is difficult to sort out in this scientific question what are the fundamental features imposed by conservation laws of physics, and by force equilibria, and what can be ascribed to successive, very specific, stop-and-go inductions of genetic nature. A posteriori, evolution selects the parameters of this process as found in the observed species. Whether there is a general law to animal formation seems out of the question. However, several concepts developed in biology, like the concept of “organizer” seem questionable from a physics point of view, since the entire deformation and force field should be the “organizer” of development, and one can hardly ascribe such a role to a single small area of the embryo body. In the same spirit, the concept of “positional information” encapsulated in concentration of chemicals seems questionable since the deformation and force fields in embryonic tissues are tensors. Finally, the concept of a development organized in space along three orthogonal (“Cartesian”) axes associated to chemical gradients seems also questionable, since early embryo development is driven by complex vortex fields, with hyperbolic trajectories which span the entire embryo. Such hyperbolic trajectories are best understood by a description in terms of dipolar components of the morphogenetic forces, whose projections along orthogonal axe have no specific meaning except as a mathematical tool. I review here the present state of description of several aspects of tetrapods morphogenesis and evolution, from the point of view of physics. It is getting clear that several basic features of tetrapods body are a direct consequences of fundamental laws of physics. Several lines of work reviewed here show that the topology of the tetrapods may be directly related to the structure of the earliest movements in embryos. The bio-mechanical approach leads to important consequences for the constraints on evolution of the craniates. Such consequences have received a controversial welcome in the last decade, although they may encapsulate the true origin of craniates, esp. simians, and eventually homo.

Copyright

Corresponding author

References

Hide All
[1] Prince, V.E., Dev. Biol. 249, 1 (2002)
[2] Davidson, E.H., Erwin, D.H., Science 311, 796 (2006)
[3] Hinman, V.F., Davidson, E.H., PNAS 104, 19404 (2007)
[4] McPherron, A.C., Lawler, A.M., Lee, S.-J., Nature genetics 22, 260 (1999)
[5] A.S. Romer, Vertebrate Paleontology (The University of Chicago Press, Chicago, 1966)
[6] Krings, M., Stone, A., Schmitz, R., Krainitzki, H., Stoneking, M., Pääbo, S., Cell 90, 19 (1997)
[7] N. Eldredge, S.J. Gould, Punctuated equilibria, an alternative to phyletic gradualism In Models in Paleobiology, edited by T.J.M. Schopf (Freeman Cooper, San Francisco, 1972), pp. 82–115, reprinted in N. Eldredge, Time frames (Princeton Univ. Press., Princeton, 1985)
[8] R. Dawkins, The Blind Watchmaker (W.W. Norton & Company, Inc., New York, 1996)
[9] M. Dennet, Darwin's Dangerous Idea: Evolution and the Meanings of Life (Simon and Schuster, 1995)
[10] D'Arcy Wentworth Thomson, On growth and Form (Cambridge University press, Cambridge, 1917)
[11] Gaunt, S.J., Int. J. Develop. Biol. 44, 109 (2000)
[12] C. Darwin, On the origin of species (London, Murray, 1859)
[13] C. Darwin, On the origin of species (London, Murray, 1859), Chap. XIII, all further quotations of Darwin's work will appear in the text as (ibid., 1859), Chap. X
[14] Cretekos, C.J., Wang, Y., Green, E.D., Comparative Sequencing Program, NISC, Martin, J.F., Rasweiler IV, J.J., Behringer, R.R., Genes and Development 22, 141 (2008)
[15] L'origine de l'Humanité, edited by Y. Coppens, P. Picq (Fayard, Paris, 2000)
[16] Fleury, V., Revue des Questions Scientifiques 177, 235 (2006)
[17] Bellus, G.A., Hefferon, T.W., de Luna, R.O., Hecht, J.T., Horton, W.A., Machado, M., Kaitila, I., McIntosh, I., Francomano, C.A., Am. J. Hum. Genet. 56, 368 (1995)
[18] R.J. Ferry Jr., M. Shim, topic Gigantism and Acromegaly e-medicine, July 2007, http://www.emedicine.com/ped/topic2634.htm
[19] H. Lodish, A.B. Lawrence, S. Zipursky, P. Matsudaira, D. Baltimore, J. Darnell, Molecular Cell Biology (W.H. Freeman and Company, New York, 2000), Chap. 14
[20] Dearden, P.K., Wilson, M.J., Sablan, L., Osborne, P.W., Havler, M., McNaughton, E., Kimura, K., Milshina, N.V., Hasselmann, M., Gempe, T., Schioett, M., Brown, S.J., Elsik, C.G., Holland, P.W.H., Kadowaki, T., Beye, M., Genome Research 16, 1376 (2006), doi:10.1101/gr.5108606
[21] Sanchez, L., Thieffry, D., J. Theor. Biol. 224, 517 (2003)
[22] A central concept in developmental biology is that of a morphogen, a substance that specifies cell identity as a function of its concentration. A continuous gradient of morphogen concentration can elicit a set of unique cellular responses at a finite number of threshold concentrations: above the threshold, one response is elicited; below it, cells respond differently. In reference [19], Chap. 14
[23] Farge, E., Current biology 13, 1365 (2003)
[24] Honoré, E., Maingret, F., Lazdunski, M., A.J. Patel EMBO J. 21, 12 (2002)
[25] Papageorgiou, S., Int. J. Dev. Biol. 50, 301 (2006)
[26] W.J. Gehring, The Homeobox as a key for understanding the principles of the genetic control of development, Hox Gene Expression, edited by Dr. S. Papageorgiou (Landes Bioscience and Springer Science + Business Media, 2007), Chap. 1
[27] Struhl, G., Nature 292, 635 (1981)
[28] P.H. Lawrence, The making of a fly (Blackwell publishing, Oxford, 1992)
[29] L.I. Held Jr., Imaginal Discs, Developmental and Cell Biology Series (Cambridge University Press, Cambridge, 2005)
[30] French, V., Bryant, P.J., Bryant, S.V., Science 193, 969 (1976)
[31] Poslethwait, J.H., Schneiderman, H., Dev. Biol. 25, 606 (1971)
[32] Serrano, N., O'Farrell, P.H., Curr. Biol. 7, R186 (1997)
[33] Williams, J.A., Padock, S.W., Caroll, S.B., Development 117, 571 (1993), see also the interactive fly website: http://www.sdbonline.org/fly/aimain/1aahome.htm
[34] Branching in Nature, edited by V. Fleury, M. Leonetti, J.-F. Gouyet (EDP Sciences, les Ulis, 2000)
[35] T. Vicsek, Fractal Growth phenomena (World Scientific, Singapore, 2000)
[36] P. Pelcé, Theory of growth and form in condensed matter Physics (Lavoisier, Paris, 2008)
[37] V. Fleury, T. Watanabe, C.R. Acad. Sci., série biologies 327, 663 (2004)
[38] Dumais, J., Shaw, S.L., Steele, C.R., Long, S.R., Ray, P.M., Int. J. Dev. Biol. 50, 209 (2006)
[39] McGinnis, W., Garber, R.L., Wirz, J., Kuroiwa, A., Gehring, W., Cell 37, 403 (1984)
[40] Duboule, D., Development, Supplement 120, 135 (1994)
[41] Duboule, D., Dollé, P., EMBO J. 8, 1497 (1989)
[42] Condie, B.G., Capecchi, M.R., Development 119, 579 (1993)
[43] Charite, J., Cell 8, 589 (1994)
[44] Zakany, J., Duboule, D., Curr. Opin. Gen. Devel. 17, 359 (2007)
[45] Spitz, F., Gonzalez, F., Duboule, D., Cell 113, 405 (2003)
[46] Burke, A.C., Nowicki, J.L., Am. Zool. 41, 687 (2001)
[47] Coates, M., Cohn, M., Biol. Essays 20, 371 (1998)
[48] Cohn, M.J., Tickle, C., Nature 399, 474 (1999) ; Cohn, M., Patel, K., Krumlauf, R., Wilkinson, D.G., Clarke, J.D.W., Tickle, C., Nature 387, 97 (1997)
[49] Rallis, R.C., Buono, J.D., Logan, M.P.O., Development 132, 1961 (2005)
[50] Schwabe, J.W.R., Rodriguez-Esteban, C., Izpisua-Belmonte, J.C., Trends Gen. 14, 229 (1998)
[51] Cohn, M.J., Izpisúa-Belmonte, J.C., Abud, H., Heath, J.K., Tickle, C., Cell 80, 739 (1995)
[52] Sekine, K., Ohuchi, H., Fujiwara, M., Yamasaki, M., Yoshizawa, T., Sato, T., Yagishita, N., Matsui, D., Koga, Y., Itoh, N., Kato, S., Nature genetics 21, 138 (1999)
[53] Boulet, A.M., Moon, A.M., Arenkiel, B.R., Capecchi, M.R., Dev. Biol. 273, 361 (2004)
[54] Chapman, D.L., Garvey, N., Hancock, S., Alexiou, M., Agulnik, S.I., Thomas, J., Bollag, R.J., Silver, L.M., Papaioannou, V.E., Dev. Dyn. 206, 379 (2000)
[55] Gibson-Brown, J.J., Agulnik, S.I., Chapman, D.L., Alexiou, M., Garvey, N., Silver, L.M., Papaioannou, V.E., Mech. Dev. 56, 93 (1996)
[56] Rallis, C., Bruneau, B.G., Buono, J.D., Seidman, C.E., Seidman, J.G., Nissim, S., Tabin, C.J., Logan, M.P.O., Development 130, 2741 (2003)
[57] Minguillon, C., Buono, J.D., Logan, M.P., Dev. Cell 8, 75 (2005)
[58] Khan, P., Linkhart, B., Simon, H.-G., Dev. Biol. 250, 383 (2002)
[59] Takeuchi, J.K., Koshiba-Takeuchi, K., Matsumoto, K., Vogel-Höpker, A., Naitoh-Matsuo, M., Ogura, K., Takahashi, N., Yasuda, K., Ogura, T., Nature 398, 810 (1999)
[60] Zákány, J., Duboule, D., Cell Tissue Res. 296, 19 (1999)
[61] Riddle, R.D., Johnson, R.L., Laufer, E., Tabin, C., Cell 75, 1401 (1993)
[62] McGlinn, E., Tabin, C.J., Curr. Opin. Gen. Devel. 16, 426 (2006)
[63] Brian, D., Harfe, P., Scherz, J., Nissim, S., Tian, H., McMahon, A.P., Tabin, C. J., Cell 118, 20 (2004)
[64] J.W. Saunders, M.T. Gasseling, Ectoderm-mesenchymal interactions in the origin of wing symmetry, in Epithelial-Mesenchymal Interactions, edited by R.E. Billingham, R. Fleichmajer (Williams and Wilkins, 1968), pp. 78–97
[65] Mikiko, T., Cohn, M.J., Ashby, P., Davey, M., Martin, P., Tickle, C., Development 127, 4011 (2000)
[66] Richardson, M.K., Carl, T.F., Hanken, J., Elinson, R.P., Cope, C., Bagley, P., J. Anat. 192, 379 (1998)
[67] Oster, G.F., Murray, J.D., Maini, P.K., J. Embr. Exp. Morph. 89, 93 (1985)
[68] N.H. Shubin, P. Alberch, A morphogenetic approach to the origin and basic organization of the tetrapod limb, in Evolutionary Biology, edited by M.K. Hecht, B. Wallace, G.I. Prance (Plenum Press, New York, 1986), pp. 319–387
[69] Rushikesh, S., Bastida, M.F., Ros, M., Dev. Biol. 310, 430 (2007)
[70] Dubrulle, J., Pourquié, O., Curr. Opin. Gen. Dev. 12, 519 (2002)
[71] Chiang, C., Litingtung, Y., Harris, M.P., Simandl, B.K., Li, Y., Beachy, P.A., Fallon, J.F., Dev. Biol. 236, 421 (2001)
[72] Chourrout, D., Delsuc, F., Chourrout, P., Edvardsen, R.B., Rentzsch, F., Renfer, E., Jensen, M.F., Zhu, B., de Jong, P., Steele, R.E., Technau, U., Nature 442, 684 (2006)
[73] Duboule, D., Science 266, 575 (1994)
[74] Shraiman, B.I., PNAS 102, 8 (2005)
[75] Cohn, M.J., Nature 406, 953 (2000)
[76] Niswander, L., Int. J. Dev. Biol. 46, 877 (2002)
[77] Kawakami, Y., Capdevila, J., Büscher, D., Itoh, T., Rodriguez-Esteban, N.J., Izpisúa-Belmonte, J.C., Cell 104, 891 (2004)
[78] Rancourt, D.E., Tsuzuki, T., Capecchi, M.R., Genes Dev. 9, 108 (1995)
[79] Agarwal, P., Wylie, J.N., Arkhito, O., Li, C., Deng, C., Grosschedle, R., Bruneau, B.G., Development 130, 623 (2003)
[80] Popperl, H., Rikhof, H., Chang, H., Haffter, P., Kimmel, C.B., Moens, C.B., Mol. Cell 6, 255 (2000)
[81] Cohn, M.J., Patel, K., Krumlauf, R., Wlkinson, D.G., Clarke, J.D., Tickle, C., Nature 387, 97 (1997)
[82] E. Mooney, Lower Limb Embryology Review (2006), emedicine; http://www.emedicine.com/plastic/topic215-htm
[83] K. Kardong, Vertebrates: Comparative anatomy, function, evolution, 2nd edn. (Mc Graw Hill, 1998)
[84] Morris, S.C., Proc. Natl. Acad. Sci. USA 97, 4426 (2000)
[85] D. Shu, X.-L. Zhang, S.C. Morris Nature (1996)
[86] S.C. Morris, The Crucible of Creation: The Burgess Shale and the Rise of Animals (Oxford University Press, New York, 1998)
[87] Shu, D.-G., Luo, H.-L., Morris, S.C., Zhang, X.-L., Hu, S.-X., Chen, L., Han, J., Zhu, M., Li, Y., Chen, L.-Z., Nature 402, 42 (1999)
[88] Ritchie, A., Zool. J. Linnean Soc. 47, 69 (1967)
[89] Thacker, C.E., Mol. Phyl. Evol. 26, 354 (2003)
[90] Miller, P.J., J. Fish Biology 5, 353 (2006)
[91] Daeschler, E.B., Shubin, N.H., Jenkins Jr, F.A.., Nature 440, 757 (2006)
[92] D. Ahn, R.K. Ho, Dev. Biol. (2008), in press
[93] Tabin, C., Development 116, 289 (1992)
[94] J.A. Clarck, M.I. Coates, Bull. Mus. Nat. d'Hist. Nat., Paris, 4e série, 17, Section C, 357 (1995)
[95] Langevin, H.M., Kirsten N. Storch, M.J. Cipolla, S.L. White, T.R. Buttolph, D.J. Taatjes, Histochem. Cell Biol. 125, 487 (2006)
[96] Meier, S., Packard, D., Dev. Biol. 102, 309 (1984)
[97] One finds many molecular stainings of the chorio-amniotic fold in the data base GEISHA (Neuropillin, Fgfr2, etc.), http://geisha.arizona.edu/geisha
[98] Davis, M.C., Dahn, R.D., Shubin, N.H., Nature 447, 473 (2007)
[99] Sanger, T.J., Jeremy, J., Gibson-Brown, J., Evolution 58, 2103 (2004)
[100] Rage, J.C., Escuillié, F., C.R. Acad. Sci. Paris Earth Sci. 330, 513 (2000)
[101] Amasaki, H., Ishikawa, H., Daigo, M., Anat. Anz. 169, 145 (1989)
[102] Falzoni, P., Boldorini, R., Zilioli, M., Sorrentino, G., Z. Minerva Ped. 47, 489 (1995)
[104] J.S. Rackoff, The origin of the tetrapod limb and the ancestry of vertebrates, in The Terrestrial Environment and the Origin of Land Vertebrates, edited by A.L. Pachen (Academic Press, London, 1980)
[105] Logan, M., Tabin, C.J., Science 283, 1736 (1999)
[106] DeLaurier, A., Schweitzer, R., Logan, M., Dev. Biol. 299, 22 (2006)
[107] Rodriguez-Esteban, C., Tsukui, T., Yonei, S., Magallon, J., Tamura, K., Belmonte, J.C.I., Nature 398, 814 (1999)
[108] Liao, X., Collins, M.D., Dev. Dyn. 237, 1553 (2008)
[109] Gerhardt, J.C., Danilchik, M., Doniach, T., Roberts, S., Rowning, B., Stewart, R., Development 107, 37 (1989)
[110] Nouri, C., Luppes, R., Veldman, A.E.P., Tuszynski, J.A., Gordon, R., Phys. Biol. 5, 1 (2008)
[111] S. Gilbert, Developmental Biology (Sinauer Press, Mass, 2000)
[112] H. Driesch, The potency of the first two cleavage cells in echinoderm development, Experimental production of partial and double formations, in: Foundations of Experimental Embryology, edited by B.H. Willier, J.M. Oppenheimer (Hafner, New York, 1892)
[113] L. Chabry, Embryologie normale et tératologique des Ascidies, edited by F. Alcan (Paris, 1887)
[114] Gastrulation, edited by C. Stern (Cold Spring Harbor Laboratory Press, New York, 2004)
[115] Lane, M.C., Sheets, M.D., Dev. Biol. 296, 12 (2006)
[116] Kimura, W., Yasugi, S., Stern, C.D., Fukuda, K., Dev. Biol. 289, 283 (2006)
[117] Joubin, K., Stern, C.D., Cell 98, 559 (1999)
[118] Spemann, O., Mangold, H., Entwicklungsmech. Org. 100, 599 (1924); Translated into English by V. Hamburger, in: Foundations of Experimental Embryology, edited by B.H. Willier, J.M. Oppenheimer (Prentice Hall International, Englewood Cliffs, NJ, 1924)
[119] Fleury, V., Al-Kilani, A., Unbekandt, M., Nguyen, T.-H., Organogenesis 3, 49 (2007)
[120] Keller, R., Science 298, 1950 (2002)
[121] Cui, C., Yang, X., Chuai, M., Glazier, J.A., Weijer, C.J., Dev. Biol. 284, 37 (2005)
[122] Keller, R., Shih, J., Sater, A., Dev. Dyn. 193, 199 (1992)
[123] Keller, R., Davidson, L., Edlund, A., Elul, T., Ezin, M., Shook, D., Skoglund, P., Philos. Trans. R. Soc. Lond. Biol. Sci. 355, 897 (2000)
[124] Stern, C.D., Voiculescu, O., Bertocchini, F., Skromne, I., Keller, R.E., Nature 306, 318 (2007)
[125] Rivier, N., Miri, M.F., Oguey, C., Colloids and Surfaces 1, 39 (2005)
[126] Odin, C., Guilbert, T., Al-Kilani, A., Boryskina, O.P., Fleury, V., Le Grand, Y., Opt. Expr. 16, 16151 (2008)
[127] Wojciak-Stothard, B., Ridley, A.J., J. Cell Biol. 161, 429 (2003)
[128] S. Munevar, Mechanics of Fibroblast Migration: a Dissertation, UMMass Medical school (printed by scholarship@UMMS 2003), and references therein
[129] Wetzel, R., Arch. Entw. Mech. Org. 119, 188 (1929)
[130] Callebaut, M., Van Nueten, E., Bortier, H., Harrisson, F., J. Morphology 255, 315 (2003)
[131] Fleury, V., Organogenesis 2, 6 (2005)
[132] Yang, X., Dormann, D., Münsterberg, A.E., Weijer, C.J., Dev. Cell 3, 425 (2002)
[133] Painter, J., Maini, O.K., Bull. Math. Biol. 62, 501 (2000)
[134] Chapman, S.C., Schubert, F.R., Schoenwolf, G.C., Lumsden, A., Dev. Biol. 245, 187 (2002)
[135] Patel, N.H., Science 266, 581 (1994)
[136] Bertocchini, F., Stern, C.D., Dev. Cell 3, 735 (2002)
[137] Graner, F., Glazier, J.A., Phys. Rev. Lett. 69, 2013 (1992)
[138] Chuai, M., Weijer, C.J., Curr. Top. Dev. Biol. 81, 135 (2008)
[139] Special issue of International Journal of developmental dynamics “Developmental Morphodynamics” 50, (2006)
[140] Jacobson, A.G., Gordon, R., J. Exp. Zool. 197, 2 (1976)
[141] LeNoble, F., Moyon, D., Pardanaud, L., Yuan, L., Djonov, V., Mattheijssen, R., Bréant, C., Fleury, V., Eichmann, A., Development 131, 361 (2004)
[142] Unbekandt, M., Moral, P.M.D., Sala, F., Bellusci, S., Warburton, D., Fleury, V., Mech. Dev. 125, 314 (2008)
[143] Malek, A.M., Gibbons, G.H., Dzau, V.J., Izumo, S., J. Clin. Invest. 92, 2013 (1993)
[144] Muratore, C.S., Nguyen, H.T., Ziegler, M.M., Wilson, J.M., J. Pediatr. Surg. 35, 906 (2000)
[145] Théry, M., Jiménez-Dalmaroni, A., Racine, V., Bornens, M., Jülicher, F., Nature 447, 7143 (2007)
[146] Roy, P., Rajfur, Z., Pomorski, P., Jacobson, K., Nat. Cell Biol. 4, E91 (2002)
[147] Tschumperlin, D.J., Dai, G., Maly, I.V., Kikuchi, T., Laiho, L., Mc Vittie, A.K., Haley, K.J., Lilly, C.M., So, P.T., Lauffenburger, D.A. et al., Nature 429, 83 (2004)
[148] Al-Kilani, A., Lorthois, S., Nguyen, T.-H., Le Noble, F., Cornelissen, A., Unbekandt, M., Boryskina, O., Leroy, L., Fleury, V., Phys. Rev. E 77, 1 (2008)
[149] Lo, C.-M., Wang, H.-B., Dembo, M., Wang, Y.-L., Biophys. J. 79, 144 (2000)
[150] Lazopoulos, K.A., Stamenovic, D., J. Biomech. 41, 1289 (2008)
[151] Nguyen, T.-H., Eichmann, A., Lenoble, F., Fleury, V., Phys. Rev. E 73, 061907 (2006)
[152] Forgacs, G., Foty, R.A., Shafrir, Y., Steinberg, M.S., Biophys. J. 74, 2227 (1998)
[153] Aderogba, K., J. of Eng. Math. 10, 143 (1976), and references therein
[154] E. Guyon, J.-P. Hulin, L. Petit, C.M. Mitescu, Physical Hydrodynamics (Oxford University press, Oxford, 2001)
[155] Schwarz, U.S., Safran, S.A., Phys. Rev. Lett. 88, 048102 (2002)
[156] R. Keller, L. Davidson, Cell movements of gastrulation. Gastrulation from Cells to Embryos, edited by C. Stern (Cold Spring Harbor Press, Cold Spring Harbor, New York, 2004)
[157] Niehrs, C., Steinbeisser, H., De Robertis, E.M., Science 263, 817 (1994)
[158] Zamir, E.A., Czirók, A., Cui, C., Little, C.D., Rongish, B.J., Proc. Natl. Acad. Sci. USA 103, 52 (2006)
[159] Chuai, M. , Zeng, W., Yang, X., Boychenko, V., Glazier, J.A., Weijer, C.J., Dev. Biol. 296, 137 (2006)
[160] Lee, C.-H., Gumbiner, B.M., Dev. Biol. 171, 363 (1995)
[161] Sakiyama, J.-I., Yamagishi, A., Kuroiwa, A., Development 130, 1225 (2003)
[162] Mikawa, T., Poh, A., Kelly, K., Ishii, Y., Reese, D., Developmental dynamics 229, 422 (2004)
[163] Verkhovski, A.B., Svitkina, T.M., Borisy, G.G., Curr. Biol. 9, 11 (1999) (in this remarkable piece of work, the authors show that it suffices to gently push a cell on one side to generate a massive directional motion of the cell, this means that cells react to a presure gradient by a directional move oriented by the gradient)
[164] Skromme, I., Stern, C., Development 128, 2915 (2001)
[165] Chapman, D.L., Garvey, N., Hancock, S., Alexiou, M., Agulnik, S.I., Thomas, J., Bollag, R.J., Silver, L.M., Papaioannou, V.E., Dev. Dyn. 206, 379 (1996)
[166] Montero, J.-A., Heisenberg, C.-P., Trends Cell Biol. 14, 620 (2004)
[167] Adelmann, H.B., Q. Rev. Biol. 11, 284 (1936)
[168] Saha, M., Servetnick, M., Grainger, R., Curr. Opin. Genet. Dev. 2, 582 (1992)
[169] Marlow, F., Zwartkruis, F., Malicki, J., Neuhauss, S.C.F., Abbas, L., Weaver, M., Driever, W., Solnica-Krezel, L., Dev. Biol. 203, 382 (1998)
[170] Stopak, D., Wessels, N.K., Harris, A.K., Proc. Nat. Acad. Sci. USA 82, 2804 (1985)
[171] Krenn, V., Wachtler, F., Anat. Embryol. 181, 453 (1990)
[172] Kardon, G., Development 125, 4019 (1998)
[173] Boryskina, O.P., Fleury, V., abstract of the VII Kharkiv Young Scientist conference, Ukraine National Academy of Science, Institute of radiophysics and Electronics, 2008; O.P. Boryskina, Y. Le Grand, C. Odin, V. Fleury, J. the European Microwave Association 4, 255 (2008)
[174] Damon, B.J., Mezentseva, V., Kumaratilake, J.S., Forgacs, G., Newman, S.A., Dev. Biol. 321, 319 (2008)
[175] Pourquié, O., Ann. Rev. Cell Dev. Biol. 17, 311 (2001)
[176] A.G. Jacobson, Somites and head mesoderm arise from somitomeres, in The origin and fate of somites, edited by E.J. Sanders (IOS Press, Amsterdam, 2001)
[177] Lipton, B.H., Jacobson, A.G., Dev. Biol. 38, 91 (1974)
[178] Meier, S., Jacobson, A.G., J. Exp. Zool. 219, 217 (1982)
[179] P.L. Gould, Analysis of Plates and Shells (Prentice Hall, 1999)
[180] Kücken, M., Forensic Science International 171, 85 (2007)
[181] Garcia-Garcia, M.J., Eggenschwiler, J.T., Caspary, T., Alcorn, H.L., Wyler, M.R., Huangfu, D., Rakeman, A.S., Lee, J.D., Feinberg, E.H., Timmer, J.R., Anderson, K.V., Proc. Natl. Acad. Sci. USA 102, 5913 (2005)
[182] Shariff, K., Leonard, A.A., Annu. Rev. Fluid. Mech. 24, 235 (1992)
[183] Mae-Wan, H., Haffegee, J., Newton, R., Yu-ming, Z., Bolton, J.S., Ross, S., Bioelectrochem. Bioenerg. 41, 81 (1996)
[184] Freeman, J.W., Silver, F.H., Conn. Tiss. Res. 456, 107 (2005)
[185] Wilson, W., Driessen, N.J.B., van Donkelaar, R.C.C., Ito, K., OsteoArthritis and Cartilage 14, 1196 (2006)
[186] Karsenty, G., Wagner, E.F., Dev. Cell 2, 389 (2002), and references therein
[187] Amprino, R., Ant. Embr. 172, 1 (1985)
[188] Meier, S., J. Embryol. Exp. Morph. 55, 291 (1980)
[189] M.A. England, Aspects of somite formation in the early chick embryo, in Somites in developing embryos, edited by R. Bellairs, D.A. Ede, J.W. Walsh (Plenum Press, New York, 1986)
[190] Dambricourt-Malassé, A., C.R. Palevol. 5, 109 (2006)
[191] Dambricourt-Malassé, A., Deshayes, M.-J., F. Cahiers d'anthropologie et de biométrie humaine 23, 1 (2005)

Keywords

Related content

Powered by UNSILO

Clarifying tetrapod embryogenesis, a physicist's point of view

  • V. Fleury (a1)

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.