The mystery of how [form] was all, and is, brought about is still with us–unsolved!
—Wardlaw (1970)
Abstract
How biological form is generated remains one of the most fascinating but elusive challenges for science. Moreover, it is widely documented in contemporary literature that development is tightly coordinated. The idea that such development is governed by a coordinating field of force, the morphogenetic field, and its position in embryology research paradigms, is traced in this article. Empirical evidences for field phenomena are described, ranging from bioelectromagnetic effects, morphology, transplantation, regeneration, and other data. Applications of medical potential including treatment of cancer, birth defects, and wound healing are highlighted. The article hypothesizes that distinct morphological forms may have distinct field parameters. Experimentally tractable field parameters may thus provide an exciting research program for probing morphogenesis and phylogenetic diversity.
Similar content being viewed by others
Notes
The organizer is in turn thought to be induced by a signal secreted by the Nieuwkoop center, with similar signaling centres discovered in the zebrafish, chick, and sea urchin (reviewed by Vonica and Gumbiner 2007). Inducers released by the organizer have now been identified which encode antagonists of bone morphogenetic protein, Nodal or Wnt growth factors. The field parameters may be characterized by the different expression domains of these growth factors and their antagonists, which create signaling gradients, which in turn are implicated in patterning the early embryo in a combinatorial fashion (Niehrs 2004).
File S1 in Online Resource 1 is a higher resolution of the Z-series from Tyler and Kimber (2006) web material at http://www.ijdb.ehu.es/data/05/052007st/S4.mov.
The file shows morphological evidence for a field system in Crepidula mollusc eggs. It is a confocal imaging Z-series of microtubules stained with FITC-anti-α tubulin antibody. All optical sections of 5 μm interval; 16-cell stage leading to 20-cell formation. Progressing through the Z-series reveals interconnection of microtubular network and orientation of spindles and asters with reference to one another throughout the whole embryo; 72 sections.
References
Aaron RK, Ciombor DM, Simon BJ (2004) Treatment of nonunions with electric and electromagnetic fields. Clin Orthop Relat Res 419:21–29
Abel R, Macho GA (2011) Ontogenetic changes in the internal and external morphology of the ilium in modern humans. J Anat 218:324–335
Abu-Issa R, Kirby ML (2008) Patterning of the heart field in the chick. Dev Biol 319:223–233
Adams DS, Masi A, Levin M (2007) H+ pump-dependent changes in membrane voltage are an early mechanism necessary and sufficient to induce Xenopus tail regeneration. Development 134:1323–1335
Allman GJ (1864) Report on the present state of our knowledge of the reproductive system in the Hydroida. Rep Br Assoc Advmt Sci 33:351–426
Arcangeli A, Crociani O, Lastraioli E et al (2009) Targeting ion channels in cancer: a novel frontier in antineoplastic therapy. Curr Med Chem 16:66–93
Astigiano S, Damonte P, Fossati S et al (2005) Fate of embryonal carcinoma cells injected into postimplantation mouse embryos. Differentiation 73:484–490
Aufderheide KJ, Frankel J, Williams NE (1980) Formation and positioning of surface-related structures in protozoa. Microbiol Rev 44:252–302
Ayala FJ (1983) Microevolution and macroevolution. In: Bendall DS (ed) Evolution from molecules to men. Cambridge University Press, Cambridge, pp 387–402
Barth LG, Barth LJ (1974) Ionic regulation of embryonic induction and cell differentiation in Rana pipiens. Dev Biol 39:1–22
Becker RO, Sparado JA (1972) Electrical stimulation of partial limb regeneration in mammals. Bull NY Acad Med 48:627–641
Behrens HM, Weisenseel MH, Sievers A (1982) Rapid changes in the pattern of electric current around the root tip of Lepidium sativum L. following gravistimulation. Plant Physiol 70:1079–1083
Beloussov LV (1997) Life of Alexander G. Gurwitsch and his relevant contribution to the theory of morphogenetic fields. Int J Dev Biol 41:771–779
Beloussov LV, Grabovsky VI (2006) Morphomechanics: goals, basic experiments and models. Int J Dev Biol 50:81–92
Beloussov LV, Volodyaev IV (2013) From molecular machines to macroscopic fields: an accent to characteristic times. Eur J Biophys 1:6–15
Bizzarri M, Cucina A, Biava PM et al (2011) Embryonic morphogenetic field induces phenotypic reversion in cancer cells. Curr Pharm Biotechnol 12:243–253
Borgens RB, Rouleau MF, DeLanney LE (1983) A steady efflux of ionic current predicts hind limb development in the axolotl. J Exp Zool 228:491–503
Borgens RB, Vanable JW Jr, Jaffe LF (1977) Bioelectricity and regeneration: large currents leave the stumps of regenerating newt limbs. Proc Natl Acad Sci USA 74:4528–4532
Borgens RB, McGinnis ME, Vanable JW Jr et al (1984) Stump currents in regenerating salamanders and newts. J Exp Zool 231:249–256
Borgens RB, Blight AR, McGinnis ME (1990) Functional recovery after spinal cord hemisection in guinea pigs: the effects of applied electric fields. J Comp Neurol 296:634–653
Borgens RB, Toombs JP, Breur G et al (1999) An imposed oscillating electrical field improves the recovery of function in neurologically complete paraplegic dogs. J Neurotrauma 16:639–657
Boveri T (1901) Die Polarität von Ovocyte, Ei und Larve des Strongylocentrotus lividus. Zool Jahrb 14:630–653
Boveri T (1910) Die Potenzen der Ascaris-Blastomeren bei abgeänderter Furchung. Festschrift zur sechzichsten Geburtstag Richard Hertwig 3:131–214
Brière C, Goodwin BC (1990) Effects of calcium input/output on the stability of a system for calcium regulated viscoelastic strain fields. J Math Biol 28:585–593
Brockes JP (1998) Regeneration and cancer. Biochim Biophys Acta 1377:M1–M11
Burr HS (1941) Changes in the field properties of mice with transplanted tumors. Yale J Biol Med 13:783–788
Burr HS (1947) Field theory in biology. Sci Monogr 64:217–225
Burr HS, Sinnott EW (1944) Electrical correlates of form in cucurbit fruits. Am J Bot 31:249–253
Chang WH, Chen LT, Sun JS et al (2004) Effect of pulse-burst electromagnetic field stimulation on osteoblast cell activities. Bioelectromagnetics 25:457–465
Chiang M, Robinson KR, Vanable JW Jr (1992) Electrical fields in the vicinity of epithelial wounds in the isolated bovine eye. Exp Eye Res 54:999–1003
Child CM (1941) Patterns and problems of development. University of Chicago Press, Chicago
Cone CD (1974) The role of the surface electrical transmembrane potential in normal and malignant mitogenesis. Ann NY Acad Sci 238:420–435
Cone CD, Cone CM (1976) Induction of mitosis in mature neurons in central nervous system by sustained depolarization. Science 192:155–158
De Robertis EM, Morita EA, Cho KWY (1991) Gradient fields and homeobox genes. Development 112:669–678
Dohmen MRV, Van Der Mey JCA (1977) Local surface differentiations at the vegetal pole of the eggs of Nassarius reticulatus, Buccinum undatum, and Crepidula fornicata (Gastropoda, Prosobranchia). Dev Biol 61:104–113
Driesch H (1892a) Entwicklungsmechanische Studien. I. Der Werth der beiden ersten Furschungszellen in der Echinodermenentwicklung. Experimentelle Erzeutung von Theil- und Doppelbildungen. Z wiss Zool 53(160–178):183–184
Driesch H (1892b) Entwicklungsmechanische Studien VI. Uber einige allgemeine Fragen der theoretichen Morphologie. Z wiss Zool 55:1–62
Driesch H (1894) Analytische Theorie der organischen Entwicklung. Engelmann, Leipzig
Driesch H (1908) The science and philosophy of the organism, vol 1. Adam and Charles Black, London
Farge E (2013) Mechano-sensing in embryonic biochemical and morphologic patterning: evolutionary perspectives in the emergence of primary organisms. Biol Theory 8:232–244
Frankel J (1989) Pattern formation: ciliate studies and models. Oxford University Press, Oxford
Frankel J (1991) The patterning of ciliates. J Protozool 38:519–525
Frankel J (1992) Positional information in cells and organisms. Trends Cell Biol 2:256–260
Frankel J (2008) What do genic mutations tell us about the structural patterning of a complex single-celled organism? Eukaryot Cell 7:1617–1639
Franklin S, Vondriska TM (2011) Genomes, proteomes, and the Central Dogma. Circ Cardiovasc Genet 4:576. doi:10.1161/CIRCGENETICS.110.957795
Fukumoto T, Kema IP, Levin M (2005) Serotonin signaling is a very early step in patterning of the left-right axis in chick and frog embryos. Curr Biol 15:794–803
Funk RH, Monsees T, Ozkucur N (2009) Electromagnetic effects—from cell biology to medicine. Prog Histochem Cytochem 43:177–264
Gilbert SF, Opitz JM, Raff RA (1996) Resynthesizing evolutionary and developmental biology. Dev Biol 173:357–372
Goodwin BC (1985) The causes of morphogenesis. BioEssays 3:32–36
Goodwin BC (1988) Problems and prospects in morphogenesis. Experientia 44:633–637
Goodwin BC (2000) The life of form. Emergent patterns of morphological transformation. Acad Sci Paris, Sci de la vie/Life Sci 323:15–21
Goodwin BC, Cohen MH (1969) A phase-shift model for the spatial and temporal organization of developing systems. J Theor Biol 25:49–107
Goodwin BC, Trainor LEH (1980) A field description of the cleavage process in morphogenesis. J Theor Biol 85:757–770
Goodwin BC, Trainor LEH (1985) Tip and whorl morphogenesis in Acetabularia by calcium-regulated strain fields. J Theor Biol 117:79–105
Gordon R (1999) The hierarchical genome and differentiation waves, vol 1. World Scientific Publishing, London
Gordon R, Parkinson J (2005) Potential roles for diatomists in nanotechnology. J Nanosci Nanotechnol 5:35–40
Gould SJ (1980) Is a new general theory of evolution emerging? Paleobiology 6:119–130
Graw J (2010) Eye development. Curr Top Dev Biol 90:343–387
Gurwitsch AG (1910) Über Determinierung, Normierung und Zufall in der Ontogenese. Arch Entw Mech 30:133–193
Gurwitsch AG (1912) Die Vererbung als Verwirklichungsvorgang. Biol Zbl 22:458–486
Gurwitsch AG (1922) Über den Begriff des embryonalen Feldes. Arch Entw Mech 51:388–415
Gurwitsch AG (1944) A biological field theory. Sovietskaye Nauka, Moscow
Harold FM (1995) From morphogenes to morphogenesis. Microbiology 141:2765–2778
Harold FM (2005) Molecules into cells: specifying spatial architecture. Microbiol Mol Biol Rev 69:544–564
Harrison RG (1918) Experiments on the development of the forelimb of Amblystoma, a self-differentiating equipotential system. J Exp Zool 25:413–461
Hendrix MJ, Seftor EA, Seftor RE et al (2007) Reprogramming metastatic tumour cells with embryonic microenvironments. Nat Rev Cancer 7:246–255
Hinman VF, O’Brien EK, Richards GS et al (2003) Expression of anterior Hox genes during larval development of the gastropod Haliotis asinina. Evol Dev 5:508–521
Holtfreter J (1945) Neuralization and epidermization of gastrula ectoderm. J Exp Zool 98:161–209
Horder TJ, Weindling PJ (1983) In: Horder TJ, Witkowski JA, Wylie CC (eds) A history of embryology. Cambridge University Press, Cambridge, pp 183–242
Huxley J, De Beer GR (1934) The elements of experimental embryology. Cambridge University Press, Cambridge
Jaeger J, Reinitz J (2006) On the dynamic nature of positional information. BioEssays 28:1102–1111
Jaffe L (1981) The role of ionic currents in establishing developmental pattern. Philos Trans R Soc Lond B 295:553–566
Jaffe LF (1986) Calcium and morphogenetic fields. Ciba Found Symp 122:271–288
Jaimovich E, Carrasco MA (2002) IP3 dependent Ca2+ signals in muscle cells are involved in regulation of gene expression. Biol Res 35:195–202
Jerka-Dziadosz M, Beisson J (1990) Genetic approaches to ciliate pattern formation: from self-assembly to morphogenesis. Trends Genet 6:41–45
Kalthoff K (1996) Analysis of biological development. McGraw-Hill, New York
Kurtz I, Shrank AR (1955) Bioelectrical properties of intact and regenerating earthworms Eisenia fetida. Physiol Zool 28:322–330
Lage K, Mollgard K, Greenway S et al (2010) Dissecting spatiotemporal protein networks driving human heart development and related disorders. Mol Syst Biol 6:381. doi:10.1038/msb.2010.36
Lakirev AV, Belousov LV (1986) Computer modeling of gastrulation and neurulation in amphibian embryos based on mechanical tension fields. Ontogenez 17(6):636–647
Lang F, Foller M, Lang KS et al (2005) Ion channels in cell proliferation and apoptotic cell death. J Membr Biol 205:147–157
Lee M, Vasioukhin V (2008) Cell polarity and cancer–cell and tissue polarity as a noncanonical tumor suppressor. J Cell Sci 121:1141–1150
Levin M (2003) Bioelectromagnetics in morphogenesis. Bioelectromagnetics 24:295–315
Levin M (2009) Bioelectric mechanisms in regeneration: unique aspects and future perspectives. Semin Cell Dev Biol 20:543–556
Levin M (2012) Molecular bioelectricity in developmental biology: new tools and recent discoveries. BioEssays 34:205–217
Lord EM, Sanders LC (1992) Roles for the extracellular matrix in plant development and pollination. Dev Biol 153:16–28
Løvtrup S, Løvtrup M (1988) The morphogenesis of molluscan shells: a mathematical account using biological parameters. J Morphol 197:53–62
Lund EJ (1921) Experimental control of organic polarity by the electric current. I. Effects of the electric current on regenerating internodes of Obelia commissuralis. J Exp Zool 34:470–493
Lund EJ (1931) Electric correlation between living cells in cortex and wood in the Douglas fir. Plant Physiol 6:631–652
Lund EJ (1947) Bioelectric fields and growth. University of Texas Press, Austin
Marsh G, Beams HW (1957) Electrical control of morphogenesis in regenerating Dugesia tigrina. J Cell Comp Physiol 39:191–211
Martens JR, O’Connell K, Tamkun M (2004) Targeting of ion channels to membrane microdomains: localization of KV channels to lipid rafts. Trends Pharmacol Sci 25:16–21
Martinez-Frias ML, Frias JL, Opitz JM (1998) Errors of morphogenesis and developmental field theory. Am J Med Genet. 76(4):291–296
McCaig CD, Rajnicek AM, Song B et al (2005) Controlling cell behavior electrically: current views and future potential. Physiol Rev 85:943–978
McCaig CD, Song B, Rajnicek AM (2009) Electrical dimensions in cell science. J Cell Sci 122:4267–4276
McGinnis W, Krumlauf R (1992) Homeobox genes and axial patterning. Cell 68:283–302
McLachlan JC (1999) The use of models and metaphors in developmental biology. Endeavour 23:51–55
Messerli MA, Graham DM (2011) Extracellular electrical fields direct wound healing and regeneration. Biol Bull 221:79–92
Metcalf MEM, Borgens RB (1994) Weak applied voltages interfere with amphibian morphogenesis and pattern. J Exp Zool 268:322–338
Morgan TH (1934) Embryology and genetics. Columbia University Press, New York
Morozova N, Shubin M (2013) The geometry of morphogenesis and the morphogenetic field concept. In: Capasso V, Gromov M, Harel-Belan A et al (eds) Pattern formation in morphogenesis: problems and mathematical issues. Springer, Berlin, pp 255–282
Murray JD, Oster GF (1984) Cell traction models for generating pattern and form in morphogenesis. J Math Biol 19:265–279
Nanney DL (1966) Cortical integration in Tetrahymena: an exercise in cytogeometry. J Exp Zool 161:307–318
Needham J (1936) New advances in the chemistry and biology of organized growth. J Proc R Soc Med 29:1577–1626
Needham J (1942) Biochemistry and morphogenesis. Cambridge University Press, Cambridge
Newman SA, Linde-Medina M (2013) Physical determinants in the emergence and inheritance of multicellular form. Biol Theory 8:274–285
Nick P, Furuya M (1992) Induction and fixation of polarity: early steps in plant morphogenesis. Dev Growth Differ 34:115–125
Niehrs C (2004) Regionally specific induction by the Spemann Mangold organizer. Nat Rev Genet 5:425–434
Niehrs C (2010) On growth and form: a Cartesian coordinate system of Wnt and BMP signaling specifies bilaterian body axes. Development 137:845–857
Nieuwkoop PD (1973) The organization center of the amphibian embryo: its origin, spatial organization, and morphogenetic action. Adv Morphogenet 10:1–39
Nieuwkoop PD (1977) Origin and establishment of embryonic polar axes in amphibian development. Curr Top Dev Biol 11:115–132
Niwa N, Inoue Y, Nozawa A et al (2000) Correlation of diversity of leg morphology in Gryllus bimaculatus (cricket) with divergence in DPP expression pattern during leg development. Development 127:4373–4381
Nuccitelli R (1984) The involvement of transcellular ion currents and electric fields in pattern formation. In: Malacinski GM, Brant SV (eds) Pattern formation: a primer in developmental biology. Macmillan, New York, pp 23–46
Nuccitelli R (1988) Physiological electric fields can influence cell motility, growth and polarity. Adv Cell Biol 2:213–232
Nuccitelli R (2003) A role for endogenous electric fields in wound healing. Curr Top Dev Biol 58:1–26
Nuccitelli R, Nuccitelli P, Changyi L et al (2011) The electric field near human skin wounds declines with age and provides a non-invasive indicator of wound healing. Wound Repair Regen 19:645–655
O’Shea PS (1988) Physical fields and cellular organization: field dependent mechanisms of morphogenesis. Experientia 44:684–694
Ochi H, Westerfield M (2007) Signaling networks that regulate muscle development: lessons from zebrafish. Dev Growth Differ 49:1–11
Opitz JM (1985) The developmental field concept. Am J Med Genet 21:1–11
Opitz JM (1993) Blastogenesis and the “primary field” in human development. Birth Defects Orig Artic Ser 29:3–37
Oppenheimer JM (1966) The growth and development of developmental biology. In: Locke M (ed) Major problems in developmental biology. Academic Press, New York, pp 1–27
Oster GF, Odell G, Alberch P (1980) Mechanics, morphogenesis and evolution. In: Oster G (ed) Mathematical problems in the life sciences. American Mathematical Society, Providence, pp 165–255
Pai VP, Aw S, Shomrat T, Lemire JM, Levin M (2012) Transmembrane voltage potential controls embryonic eye patterning in Xenopus laevis. Development 139:313–323
Papageorgiou S (2006) Pulling forces acting on Hox gene clusters cause expression collinearity. Int J Dev Biol 50:301–308
Phillips A (2012) Structural optimisation: biomechanics of the femur. Proc ICE—Eng Comput Mech 165:147–154
Pilla AA (2002) Low-intensity electromagnetic and mechanical modulation of bone growth and repair: are they equivalent? J Orthop Sci 7(3):420–428
Poo M, Robinson KR (1977) Electrophoresis of concanavalin A receptors along embryonic muscle cell membrane. Nature 265:602–605
Potter JD (2007) Morphogens, morphostats, microarchitecture and malignancy. Nat Rev Cancer 7:464–474
Raff RA, Kaufmann TC (1983) Embryos, genes and evolution. Macmillan, London
Ramadan A, Elsaidy M, Zyada R (2008) Effect of low-intensity direct current on the healing of chronic wounds: a literature review. J Wound Care 17:292–296. Erratum 17(8):367
Raup DM (1962) Computer as aid in describing form in gastropod shells. Science 138:150–152
Rehm WS (1938) Bud regeneration and electrical polarities in Phaseolus multiflorus. Plant Physiol 13:81–101
Reid DT, Peichel CL (2010) Perspectives on the genetic architecture of divergence in body shape in sticklebacks. Integr Comp Biol 50:1057–1066
Reissis D, Abel RL (2012) Development of fetal trabecular micro-architecture in the humerus and femur. J Anat 220:496–503
Robinson KR (1989) Endogenous and applied electrical currents: their measurement and application. In: Borgens RB, Robinson KR, Vanable JW Jr et al (eds) Electric fields in vertebrate repair: natural and applied voltages in vertebrate regeneration and healing. Liss, New York, pp 1–25
Rosene HF, Lund EJ (1953) Bioelectric fields and correlation in plants. In: Loomis WE (ed) Growth and differentiation in plants. Iowa State College Press, Ames, pp 219–252
Runnström J (1914) Analytische Studien uber die Seeigelenentwicklung. I W Roux Arch Entw Mech Org 40:526–564
Sachs T (1991) Cell polarity and tissue patterning in plants. Development Suppl 1:83–93
Sander K (1996) On the causation of animal morphogenesis: concepts of German-speaking authors from Theodor Schwann (1839) to Richard Goldschmidt (1927). Int J Dev Biol 40:7–20
Schock F, Perrimon N (2002) Molecular mechanisms of morphogenesis. Cell and Dev Biol 18:463–493
Schwartz JH (2013) Emergence of shape. Biol Theory 8:209–210
Settleman J (2001) Rac ‘n Rho: the music that shapes the embryo. Dev Cell 1:321–331
Shapiro S (2012) A review of oscillating field stimulation to treat human spinal cord injury. World Neurosurg. doi:10.1016/j.wneu.2012.11.039
Shapiro S, Borgens R, Pascuzzi R et al (2005) Oscillating field stimulation for complete spinal cord injury in humans: a phase 1 trial. J Neurosurg Spine 2:3–10
Shi R, Borgens RB (1995) Three-dimensional gradients of voltage during development of the nervous system as invisible coordinates for the establishment of embryonic pattern. Dev Dyn 202:101–114
Shih YL, Le T, Rothfield L (2003) Division site selection in Escherichia coli involves dynamic redistribution of Min proteins within coiled structures that extend between the two cell poles. Proc Natl Acad Sci USA 100:7865–7870
Sinnott EW (1960) Plant morphogenesis. McGraw-Hill, New York
Sinnott EW, Bloch R (1944) Visible expression of cytoplasmic pattern in the differentiation of xylem strands. Proc Natl Acad Sci USA 30:388–392
Sonnenschein C, Soto AM (1999) The society of cells: cancer and control of cell proliferation. Springer, New York
Sonnenschein C, Soto AM (2000) Somatic mutation theory of carcinogenesis: why it should be dropped and replaced. Mol Carcinog 29:205–211
Sonnenschein C, Soto AM (2008) Theories of carcinogenesis: an emerging perspective. Semin Cancer Biol 18:372–377
Stumpf HF (1967) Über den Verlauf eines Schuppenorientierenden Gefalles bei Galleria mellonella. Wilhelm Roux Arch Entw Mech Org 158:315–330
Sundelacruz S, Levin M, Kaplan DL (2008) Membrane potential controls adipogenic and osteogenic differentiation of mesenchymal stem cells. PLoS One 3:e3737
Thomas JB (1939) Electric control of polarity in plants. PhD thesis, Wageningen University, Wageningen, The Netherlands
Thomas GH, Kiehart DP (1994) Beta spectrin has a restricted tissue and sub-cellular distribution during Drosophila embryogenesis. Development 120:2039–2050
Thompson DA (1942) On growth and form. The University Press, Cambridge
Thorpe TA (2012) History of plant tissue culture. Methods Mol Biol 877:9–27
Tsikolia N (2006) The role and limits of a gradient based explanation of morphogenesis: a theoretical consideration. Int J Dev Biol 50:333–340
Tucker JB (1981) Cytoskeletal coordination and intercellular signalling during metazoan embryogenesis. J Embryol Exp Morphol 65:1–25
Tyler SEB, Kimber SJ (2006) The dynamic nature of mollusc egg surface architecture and its relation to the microtubule network. Int J Dev Biol 50:405–412
Tyler SEB, Butler RD, Kimber SJ (1998) Morphological evidence for a morphogenetic field in gastropod mollusc eggs. Int J Dev Biol 42:79–85
Tyner KM, Kopelman R, Philbert MA (2007) “Nanosized voltmeter” enables cellular-wide electric field mapping. Biophys J 93:1163–1174
Vandenberg LN, Morrie RD, Adams DS (2011) V-ATPase-dependent ectodermal voltage and pH regionalization are required for craniofacial morphogenesis. Dev Dyn 240:1889–1904
Viczian AS, Solessio EC, Lyou Y et al (2009) Generation of functional eyes from pluripotent cells. PLoS Biol 7:e1000174
Vöchting H (1877) Ueber Theilbarkeit im Pflanzenreich und die Wirkung innerer und äusserer Krafte auf Organbildung an Pflanzentheilen. Arch gesamte Physiol Mensch Tiere 15:153–190
Vöchting H (1878) Über Organbildung im Pflanzenreich. Cohen, Bonn
Vonica A, Gumbiner BM (2007) The Xenopus Nieuwkoop center and Spemann-Mangold organizer share molecular components and a requirement for maternal Wnt activity. Dev Biol 312:90–102
Waddington CH (1935) Cancer and the theory of organisers. Nature 135:606–608
Waddington CH (1956) Principles of embryology. Allen and Unwin, London
Wallace R (2007) Neural membrane microdomains as computational systems: toward molecular modelling in the study of neural disease. Biosystems 87:20–30
Wallis J (1659) Tractatus duo, priore de Cycloide. Oxford
Wardlaw CW (1968) Morphogenesis in plants. Methuen, London
Wardlaw CW (1970) Cellular differentiation in plants and other essays. Manchester University Press, Manchester
Webb SE, Millar AL (2011) Visualization of Ca2+ signaling during embryonic skeletal muscle formation in vertebrates. Cold Spring Harb Perspect Biol 3(2). doi: 10.1101/cshperspect.a004325
Weiss PA (1939) Principles of development: a text in experimental embryology. Holt, New York
Willier BH, Oppenheimer JM (1974) Foundations of experimental embryology. Hafner Press, New York
Wolff J (1870) Über die innere Architectur der Knochen und ihre Bedeutung für die Frage vom Knochenwachsthum. Virchows Arch Pathol Anat Physiol 50:389–450. Translated and abridged by Heller MO, Taylor WR, Aslanidis N et al. In: Wolff J (2010) On the inner architecture of bones and its importance for bone growth. Clin Orthop Relat Res 468:1056–1065
Wolpert L (1969) Positional information and the spatial pattern of cellular differentiation. J Theor Biol 25:1–47
Wolpert L (1977) The development of pattern and form in animals. Carolina Biological, Burlington
Wolpert L (1986) Gradients, position and pattern: a history. In: Horder TJ, Witkowski JA, Wylie CC (eds) A history of embryology. Cambridge University Press, Cambridge, pp 347–361
Woodruff RI, Telfer WH (1973) Electrical properties of ovarian cells linked by intercellular bridges. Ann NY Acad Sci 238:408–419
Woodruff RI, Telfer WH (1980) Electrophoresis of proteins in intercellular bridges. Nature 286:84–86
Zhao M (2009) Electrical fields in wound healing—an overriding signal that directs cell migration. Semin Cell Dev Biol 20:674–682
Zhao M, Forrester JV, McCaig CD (1999a) A small physiological field orients cell division. Proc Natl Acad Sci USA 96:4942–4946
Zhao M, Dick A, Forrester JV et al (1999b) Electric field-directed cell motility involves up-regulated expression and asymmetric redistribution of the epidermal growth factor receptors and is enhanced by fibronectin and laminin. Mol Biol Cell 10:1259–1276
Acknowledgments
I would like to thank Barbara Verrall for helpful comments on the manuscript, and Luke Tyler for assistance with proof reading.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary material 1 (MOV 13339 kb)
Rights and permissions
About this article
Cite this article
Tyler, S.E.B. The Work Surfaces of Morphogenesis: The Role of the Morphogenetic Field. Biol Theory 9, 194–208 (2014). https://doi.org/10.1007/s13752-014-0177-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13752-014-0177-8