Advertisement

Biological Theory

, Volume 9, Issue 2, pp 194–208 | Cite as

The Work Surfaces of Morphogenesis: The Role of the Morphogenetic Field

  • Sheena E. B. TylerEmail author
Long Article

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.

Keywords

Bauplan Bioelectromagnetic information Cancer Regeneration Form Morphogenetic field 

Notes

Acknowledgments

I would like to thank Barbara Verrall for helpful comments on the manuscript, and Luke Tyler for assistance with proof reading.

Supplementary material

Supplementary material 1 (MOV 13339 kb)

13752_2014_177_MOESM2_ESM.pdf (937 kb)
Supplementary material 2 (PDF 937 kb)

References

  1. Aaron RK, Ciombor DM, Simon BJ (2004) Treatment of nonunions with electric and electromagnetic fields. Clin Orthop Relat Res 419:21–29Google Scholar
  2. Abel R, Macho GA (2011) Ontogenetic changes in the internal and external morphology of the ilium in modern humans. J Anat 218:324–335Google Scholar
  3. Abu-Issa R, Kirby ML (2008) Patterning of the heart field in the chick. Dev Biol 319:223–233Google Scholar
  4. 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 134:1323–1335Google Scholar
  5. Allman GJ (1864) Report on the present state of our knowledge of the reproductive system in the Hydroida. Rep Br Assoc Advmt Sci 33:351–426Google Scholar
  6. Arcangeli A, Crociani O, Lastraioli E et al (2009) Targeting ion channels in cancer: a novel frontier in antineoplastic therapy. Curr Med Chem 16:66–93Google Scholar
  7. Astigiano S, Damonte P, Fossati S et al (2005) Fate of embryonal carcinoma cells injected into postimplantation mouse embryos. Differentiation 73:484–490Google Scholar
  8. Aufderheide KJ, Frankel J, Williams NE (1980) Formation and positioning of surface-related structures in protozoa. Microbiol Rev 44:252–302Google Scholar
  9. Ayala FJ (1983) Microevolution and macroevolution. In: Bendall DS (ed) Evolution from molecules to men. Cambridge University Press, Cambridge, pp 387–402Google Scholar
  10. Barth LG, Barth LJ (1974) Ionic regulation of embryonic induction and cell differentiation in Rana pipiens. Dev Biol 39:1–22Google Scholar
  11. Becker RO, Sparado JA (1972) Electrical stimulation of partial limb regeneration in mammals. Bull NY Acad Med 48:627–641Google Scholar
  12. 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 70:1079–1083Google Scholar
  13. Beloussov LV (1997) Life of Alexander G. Gurwitsch and his relevant contribution to the theory of morphogenetic fields. Int J Dev Biol 41:771–779Google Scholar
  14. Beloussov LV, Grabovsky VI (2006) Morphomechanics: goals, basic experiments and models. Int J Dev Biol 50:81–92Google Scholar
  15. Beloussov LV, Volodyaev IV (2013) From molecular machines to macroscopic fields: an accent to characteristic times. Eur J Biophys 1:6–15Google Scholar
  16. Bizzarri M, Cucina A, Biava PM et al (2011) Embryonic morphogenetic field induces phenotypic reversion in cancer cells. Curr Pharm Biotechnol 12:243–253Google Scholar
  17. Borgens RB, Rouleau MF, DeLanney LE (1983) A steady efflux of ionic current predicts hind limb development in the axolotl. J Exp Zool 228:491–503Google Scholar
  18. 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 74:4528–4532Google Scholar
  19. Borgens RB, McGinnis ME, Vanable JW Jr et al (1984) Stump currents in regenerating salamanders and newts. J Exp Zool 231:249–256Google Scholar
  20. 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 296:634–653Google Scholar
  21. 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 16:639–657Google Scholar
  22. Boveri T (1901) Die Polarität von Ovocyte, Ei und Larve des Strongylocentrotus lividus. Zool Jahrb 14:630–653Google Scholar
  23. Boveri T (1910) Die Potenzen der Ascaris-Blastomeren bei abgeänderter Furchung. Festschrift zur sechzichsten Geburtstag Richard Hertwig 3:131–214Google Scholar
  24. 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 28:585–593Google Scholar
  25. Brockes JP (1998) Regeneration and cancer. Biochim Biophys Acta 1377:M1–M11Google Scholar
  26. Burr HS (1941) Changes in the field properties of mice with transplanted tumors. Yale J Biol Med 13:783–788Google Scholar
  27. Burr HS (1947) Field theory in biology. Sci Monogr 64:217–225Google Scholar
  28. Burr HS, Sinnott EW (1944) Electrical correlates of form in cucurbit fruits. Am J Bot 31:249–253Google Scholar
  29. Chang WH, Chen LT, Sun JS et al (2004) Effect of pulse-burst electromagnetic field stimulation on osteoblast cell activities. Bioelectromagnetics 25:457–465Google Scholar
  30. Chiang M, Robinson KR, Vanable JW Jr (1992) Electrical fields in the vicinity of epithelial wounds in the isolated bovine eye. Exp Eye Res 54:999–1003Google Scholar
  31. Child CM (1941) Patterns and problems of development. University of Chicago Press, ChicagoGoogle Scholar
  32. Cone CD (1974) The role of the surface electrical transmembrane potential in normal and malignant mitogenesis. Ann NY Acad Sci 238:420–435Google Scholar
  33. Cone CD, Cone CM (1976) Induction of mitosis in mature neurons in central nervous system by sustained depolarization. Science 192:155–158Google Scholar
  34. De Robertis EM, Morita EA, Cho KWY (1991) Gradient fields and homeobox genes. Development 112:669–678Google Scholar
  35. 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 61:104–113Google Scholar
  36. 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):183–184Google Scholar
  37. Driesch H (1892b) Entwicklungsmechanische Studien VI. Uber einige allgemeine Fragen der theoretichen Morphologie. Z wiss Zool 55:1–62Google Scholar
  38. Driesch H (1894) Analytische Theorie der organischen Entwicklung. Engelmann, LeipzigGoogle Scholar
  39. Driesch H (1908) The science and philosophy of the organism, vol 1. Adam and Charles Black, LondonGoogle Scholar
  40. Farge E (2013) Mechano-sensing in embryonic biochemical and morphologic patterning: evolutionary perspectives in the emergence of primary organisms. Biol Theory 8:232–244Google Scholar
  41. Frankel J (1989) Pattern formation: ciliate studies and models. Oxford University Press, OxfordGoogle Scholar
  42. Frankel J (1991) The patterning of ciliates. J Protozool 38:519–525Google Scholar
  43. Frankel J (1992) Positional information in cells and organisms. Trends Cell Biol 2:256–260Google Scholar
  44. Frankel J (2008) What do genic mutations tell us about the structural patterning of a complex single-celled organism? Eukaryot Cell 7:1617–1639Google Scholar
  45. Franklin S, Vondriska TM (2011) Genomes, proteomes, and the Central Dogma. Circ Cardiovasc Genet 4:576. doi: 10.1161/CIRCGENETICS.110.957795 Google Scholar
  46. 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 15:794–803Google Scholar
  47. Funk RH, Monsees T, Ozkucur N (2009) Electromagnetic effects—from cell biology to medicine. Prog Histochem Cytochem 43:177–264Google Scholar
  48. Gilbert SF, Opitz JM, Raff RA (1996) Resynthesizing evolutionary and developmental biology. Dev Biol 173:357–372Google Scholar
  49. Goodwin BC (1985) The causes of morphogenesis. BioEssays 3:32–36Google Scholar
  50. Goodwin BC (1988) Problems and prospects in morphogenesis. Experientia 44:633–637Google Scholar
  51. Goodwin BC (2000) The life of form. Emergent patterns of morphological transformation. Acad Sci Paris, Sci de la vie/Life Sci 323:15–21Google Scholar
  52. Goodwin BC, Cohen MH (1969) A phase-shift model for the spatial and temporal organization of developing systems. J Theor Biol 25:49–107Google Scholar
  53. Goodwin BC, Trainor LEH (1980) A field description of the cleavage process in morphogenesis. J Theor Biol 85:757–770Google Scholar
  54. Goodwin BC, Trainor LEH (1985) Tip and whorl morphogenesis in Acetabularia by calcium-regulated strain fields. J Theor Biol 117:79–105Google Scholar
  55. Gordon R (1999) The hierarchical genome and differentiation waves, vol 1. World Scientific Publishing, LondonGoogle Scholar
  56. Gordon R, Parkinson J (2005) Potential roles for diatomists in nanotechnology. J Nanosci Nanotechnol 5:35–40Google Scholar
  57. Gould SJ (1980) Is a new general theory of evolution emerging? Paleobiology 6:119–130Google Scholar
  58. Graw J (2010) Eye development. Curr Top Dev Biol 90:343–387Google Scholar
  59. Gurwitsch AG (1910) Über Determinierung, Normierung und Zufall in der Ontogenese. Arch Entw Mech 30:133–193Google Scholar
  60. Gurwitsch AG (1912) Die Vererbung als Verwirklichungsvorgang. Biol Zbl 22:458–486Google Scholar
  61. Gurwitsch AG (1922) Über den Begriff des embryonalen Feldes. Arch Entw Mech 51:388–415Google Scholar
  62. Gurwitsch AG (1944) A biological field theory. Sovietskaye Nauka, MoscowGoogle Scholar
  63. Harold FM (1995) From morphogenes to morphogenesis. Microbiology 141:2765–2778Google Scholar
  64. Harold FM (2005) Molecules into cells: specifying spatial architecture. Microbiol Mol Biol Rev 69:544–564Google Scholar
  65. Harrison RG (1918) Experiments on the development of the forelimb of Amblystoma, a self-differentiating equipotential system. J Exp Zool 25:413–461Google Scholar
  66. Hendrix MJ, Seftor EA, Seftor RE et al (2007) Reprogramming metastatic tumour cells with embryonic microenvironments. Nat Rev Cancer 7:246–255Google Scholar
  67. 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 5:508–521Google Scholar
  68. Holtfreter J (1945) Neuralization and epidermization of gastrula ectoderm. J Exp Zool 98:161–209Google Scholar
  69. Horder TJ, Weindling PJ (1983) In: Horder TJ, Witkowski JA, Wylie CC (eds) A history of embryology. Cambridge University Press, Cambridge, pp 183–242Google Scholar
  70. Huxley J, De Beer GR (1934) The elements of experimental embryology. Cambridge University Press, CambridgeGoogle Scholar
  71. Jaeger J, Reinitz J (2006) On the dynamic nature of positional information. BioEssays 28:1102–1111Google Scholar
  72. Jaffe L (1981) The role of ionic currents in establishing developmental pattern. Philos Trans R Soc Lond B 295:553–566Google Scholar
  73. Jaffe LF (1986) Calcium and morphogenetic fields. Ciba Found Symp 122:271–288Google Scholar
  74. Jaimovich E, Carrasco MA (2002) IP3 dependent Ca2+ signals in muscle cells are involved in regulation of gene expression. Biol Res 35:195–202Google Scholar
  75. Jerka-Dziadosz M, Beisson J (1990) Genetic approaches to ciliate pattern formation: from self-assembly to morphogenesis. Trends Genet 6:41–45Google Scholar
  76. Kalthoff K (1996) Analysis of biological development. McGraw-Hill, New YorkGoogle Scholar
  77. Kurtz I, Shrank AR (1955) Bioelectrical properties of intact and regenerating earthworms Eisenia fetida. Physiol Zool 28:322–330Google Scholar
  78. 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 Google Scholar
  79. Lakirev AV, Belousov LV (1986) Computer modeling of gastrulation and neurulation in amphibian embryos based on mechanical tension fields. Ontogenez 17(6):636–647Google Scholar
  80. Lang F, Foller M, Lang KS et al (2005) Ion channels in cell proliferation and apoptotic cell death. J Membr Biol 205:147–157Google Scholar
  81. Lee M, Vasioukhin V (2008) Cell polarity and cancer–cell and tissue polarity as a noncanonical tumor suppressor. J Cell Sci 121:1141–1150Google Scholar
  82. Levin M (2003) Bioelectromagnetics in morphogenesis. Bioelectromagnetics 24:295–315Google Scholar
  83. Levin M (2009) Bioelectric mechanisms in regeneration: unique aspects and future perspectives. Semin Cell Dev Biol 20:543–556Google Scholar
  84. Levin M (2012) Molecular bioelectricity in developmental biology: new tools and recent discoveries. BioEssays 34:205–217Google Scholar
  85. Lord EM, Sanders LC (1992) Roles for the extracellular matrix in plant development and pollination. Dev Biol 153:16–28Google Scholar
  86. Løvtrup S, Løvtrup M (1988) The morphogenesis of molluscan shells: a mathematical account using biological parameters. J Morphol 197:53–62Google Scholar
  87. 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 34:470–493Google Scholar
  88. Lund EJ (1931) Electric correlation between living cells in cortex and wood in the Douglas fir. Plant Physiol 6:631–652Google Scholar
  89. Lund EJ (1947) Bioelectric fields and growth. University of Texas Press, AustinGoogle Scholar
  90. Marsh G, Beams HW (1957) Electrical control of morphogenesis in regenerating Dugesia tigrina. J Cell Comp Physiol 39:191–211Google Scholar
  91. 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 25:16–21Google Scholar
  92. Martinez-Frias ML, Frias JL, Opitz JM (1998) Errors of morphogenesis and developmental field theory. Am J Med Genet. 76(4):291–296Google Scholar
  93. McCaig CD, Rajnicek AM, Song B et al (2005) Controlling cell behavior electrically: current views and future potential. Physiol Rev 85:943–978Google Scholar
  94. McCaig CD, Song B, Rajnicek AM (2009) Electrical dimensions in cell science. J Cell Sci 122:4267–4276Google Scholar
  95. McGinnis W, Krumlauf R (1992) Homeobox genes and axial patterning. Cell 68:283–302Google Scholar
  96. McLachlan JC (1999) The use of models and metaphors in developmental biology. Endeavour 23:51–55Google Scholar
  97. Messerli MA, Graham DM (2011) Extracellular electrical fields direct wound healing and regeneration. Biol Bull 221:79–92Google Scholar
  98. Metcalf MEM, Borgens RB (1994) Weak applied voltages interfere with amphibian morphogenesis and pattern. J Exp Zool 268:322–338Google Scholar
  99. Morgan TH (1934) Embryology and genetics. Columbia University Press, New YorkGoogle Scholar
  100. 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 255–282Google Scholar
  101. Murray JD, Oster GF (1984) Cell traction models for generating pattern and form in morphogenesis. J Math Biol 19:265–279Google Scholar
  102. Nanney DL (1966) Cortical integration in Tetrahymena: an exercise in cytogeometry. J Exp Zool 161:307–318Google Scholar
  103. Needham J (1936) New advances in the chemistry and biology of organized growth. J Proc R Soc Med 29:1577–1626Google Scholar
  104. Needham J (1942) Biochemistry and morphogenesis. Cambridge University Press, CambridgeGoogle Scholar
  105. Newman SA, Linde-Medina M (2013) Physical determinants in the emergence and inheritance of multicellular form. Biol Theory 8:274–285Google Scholar
  106. Nick P, Furuya M (1992) Induction and fixation of polarity: early steps in plant morphogenesis. Dev Growth Differ 34:115–125Google Scholar
  107. Niehrs C (2004) Regionally specific induction by the Spemann Mangold organizer. Nat Rev Genet 5:425–434Google Scholar
  108. Niehrs C (2010) On growth and form: a Cartesian coordinate system of Wnt and BMP signaling specifies bilaterian body axes. Development 137:845–857Google Scholar
  109. Nieuwkoop PD (1973) The organization center of the amphibian embryo: its origin, spatial organization, and morphogenetic action. Adv Morphogenet 10:1–39Google Scholar
  110. Nieuwkoop PD (1977) Origin and establishment of embryonic polar axes in amphibian development. Curr Top Dev Biol 11:115–132Google Scholar
  111. 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 127:4373–4381Google Scholar
  112. 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 23–46Google Scholar
  113. Nuccitelli R (1988) Physiological electric fields can influence cell motility, growth and polarity. Adv Cell Biol 2:213–232Google Scholar
  114. Nuccitelli R (2003) A role for endogenous electric fields in wound healing. Curr Top Dev Biol 58:1–26Google Scholar
  115. 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 19:645–655Google Scholar
  116. O’Shea PS (1988) Physical fields and cellular organization: field dependent mechanisms of morphogenesis. Experientia 44:684–694Google Scholar
  117. Ochi H, Westerfield M (2007) Signaling networks that regulate muscle development: lessons from zebrafish. Dev Growth Differ 49:1–11Google Scholar
  118. Opitz JM (1985) The developmental field concept. Am J Med Genet 21:1–11Google Scholar
  119. Opitz JM (1993) Blastogenesis and the “primary field” in human development. Birth Defects Orig Artic Ser 29:3–37Google Scholar
  120. Oppenheimer JM (1966) The growth and development of developmental biology. In: Locke M (ed) Major problems in developmental biology. Academic Press, New York, pp 1–27Google Scholar
  121. 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 165–255Google Scholar
  122. Pai VP, Aw S, Shomrat T, Lemire JM, Levin M (2012) Transmembrane voltage potential controls embryonic eye patterning in Xenopus laevis. Development 139:313–323Google Scholar
  123. Papageorgiou S (2006) Pulling forces acting on Hox gene clusters cause expression collinearity. Int J Dev Biol 50:301–308Google Scholar
  124. Phillips A (2012) Structural optimisation: biomechanics of the femur. Proc ICE—Eng Comput Mech 165:147–154Google Scholar
  125. Pilla AA (2002) Low-intensity electromagnetic and mechanical modulation of bone growth and repair: are they equivalent? J Orthop Sci 7(3):420–428Google Scholar
  126. Poo M, Robinson KR (1977) Electrophoresis of concanavalin A receptors along embryonic muscle cell membrane. Nature 265:602–605Google Scholar
  127. Potter JD (2007) Morphogens, morphostats, microarchitecture and malignancy. Nat Rev Cancer 7:464–474Google Scholar
  128. Raff RA, Kaufmann TC (1983) Embryos, genes and evolution. Macmillan, LondonGoogle Scholar
  129. 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):367Google Scholar
  130. Raup DM (1962) Computer as aid in describing form in gastropod shells. Science 138:150–152Google Scholar
  131. Rehm WS (1938) Bud regeneration and electrical polarities in Phaseolus multiflorus. Plant Physiol 13:81–101Google Scholar
  132. Reid DT, Peichel CL (2010) Perspectives on the genetic architecture of divergence in body shape in sticklebacks. Integr Comp Biol 50:1057–1066Google Scholar
  133. Reissis D, Abel RL (2012) Development of fetal trabecular micro-architecture in the humerus and femur. J Anat 220:496–503Google Scholar
  134. 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 1–25Google Scholar
  135. 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 219–252Google Scholar
  136. Runnström J (1914) Analytische Studien uber die Seeigelenentwicklung. I W Roux Arch Entw Mech Org 40:526–564Google Scholar
  137. Sachs T (1991) Cell polarity and tissue patterning in plants. Development Suppl 1:83–93Google Scholar
  138. 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 40:7–20Google Scholar
  139. Schock F, Perrimon N (2002) Molecular mechanisms of morphogenesis. Cell and Dev Biol 18:463–493Google Scholar
  140. Schwartz JH (2013) Emergence of shape. Biol Theory 8:209–210Google Scholar
  141. Settleman J (2001) Rac ‘n Rho: the music that shapes the embryo. Dev Cell 1:321–331Google Scholar
  142. 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 Google Scholar
  143. 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 2:3–10Google Scholar
  144. 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 202:101–114Google Scholar
  145. 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 100:7865–7870Google Scholar
  146. Sinnott EW (1960) Plant morphogenesis. McGraw-Hill, New YorkGoogle Scholar
  147. Sinnott EW, Bloch R (1944) Visible expression of cytoplasmic pattern in the differentiation of xylem strands. Proc Natl Acad Sci USA 30:388–392Google Scholar
  148. Sonnenschein C, Soto AM (1999) The society of cells: cancer and control of cell proliferation. Springer, New YorkGoogle Scholar
  149. Sonnenschein C, Soto AM (2000) Somatic mutation theory of carcinogenesis: why it should be dropped and replaced. Mol Carcinog 29:205–211Google Scholar
  150. Sonnenschein C, Soto AM (2008) Theories of carcinogenesis: an emerging perspective. Semin Cancer Biol 18:372–377Google Scholar
  151. Stumpf HF (1967) Über den Verlauf eines Schuppenorientierenden Gefalles bei Galleria mellonella. Wilhelm Roux Arch Entw Mech Org 158:315–330Google Scholar
  152. Sundelacruz S, Levin M, Kaplan DL (2008) Membrane potential controls adipogenic and osteogenic differentiation of mesenchymal stem cells. PLoS One 3:e3737Google Scholar
  153. Thomas JB (1939) Electric control of polarity in plants. PhD thesis, Wageningen University, Wageningen, The NetherlandsGoogle Scholar
  154. Thomas GH, Kiehart DP (1994) Beta spectrin has a restricted tissue and sub-cellular distribution during Drosophila embryogenesis. Development 120:2039–2050Google Scholar
  155. Thompson DA (1942) On growth and form. The University Press, CambridgeGoogle Scholar
  156. Thorpe TA (2012) History of plant tissue culture. Methods Mol Biol 877:9–27Google Scholar
  157. Tsikolia N (2006) The role and limits of a gradient based explanation of morphogenesis: a theoretical consideration. Int J Dev Biol 50:333–340Google Scholar
  158. Tucker JB (1981) Cytoskeletal coordination and intercellular signalling during metazoan embryogenesis. J Embryol Exp Morphol 65:1–25Google Scholar
  159. Tyler SEB, Kimber SJ (2006) The dynamic nature of mollusc egg surface architecture and its relation to the microtubule network. Int J Dev Biol 50:405–412Google Scholar
  160. Tyler SEB, Butler RD, Kimber SJ (1998) Morphological evidence for a morphogenetic field in gastropod mollusc eggs. Int J Dev Biol 42:79–85Google Scholar
  161. Tyner KM, Kopelman R, Philbert MA (2007) “Nanosized voltmeter” enables cellular-wide electric field mapping. Biophys J 93:1163–1174Google Scholar
  162. Vandenberg LN, Morrie RD, Adams DS (2011) V-ATPase-dependent ectodermal voltage and pH regionalization are required for craniofacial morphogenesis. Dev Dyn 240:1889–1904Google Scholar
  163. Viczian AS, Solessio EC, Lyou Y et al (2009) Generation of functional eyes from pluripotent cells. PLoS Biol 7:e1000174Google Scholar
  164. Vöchting H (1877) Ueber Theilbarkeit im Pflanzenreich und die Wirkung innerer und äusserer Krafte auf Organbildung an Pflanzentheilen. Arch gesamte Physiol Mensch Tiere 15:153–190Google Scholar
  165. Vöchting H (1878) Über Organbildung im Pflanzenreich. Cohen, BonnGoogle Scholar
  166. 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 312:90–102Google Scholar
  167. Waddington CH (1935) Cancer and the theory of organisers. Nature 135:606–608Google Scholar
  168. Waddington CH (1956) Principles of embryology. Allen and Unwin, LondonGoogle Scholar
  169. Wallace R (2007) Neural membrane microdomains as computational systems: toward molecular modelling in the study of neural disease. Biosystems 87:20–30Google Scholar
  170. Wallis J (1659) Tractatus duo, priore de Cycloide. OxfordGoogle Scholar
  171. Wardlaw CW (1968) Morphogenesis in plants. Methuen, LondonGoogle Scholar
  172. Wardlaw CW (1970) Cellular differentiation in plants and other essays. Manchester University Press, ManchesterGoogle Scholar
  173. 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
  174. Weiss PA (1939) Principles of development: a text in experimental embryology. Holt, New YorkGoogle Scholar
  175. Willier BH, Oppenheimer JM (1974) Foundations of experimental embryology. Hafner Press, New YorkGoogle Scholar
  176. 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 468:1056–1065Google Scholar
  177. Wolpert L (1969) Positional information and the spatial pattern of cellular differentiation. J Theor Biol 25:1–47Google Scholar
  178. Wolpert L (1977) The development of pattern and form in animals. Carolina Biological, BurlingtonGoogle Scholar
  179. 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 347–361Google Scholar
  180. Woodruff RI, Telfer WH (1973) Electrical properties of ovarian cells linked by intercellular bridges. Ann NY Acad Sci 238:408–419Google Scholar
  181. Woodruff RI, Telfer WH (1980) Electrophoresis of proteins in intercellular bridges. Nature 286:84–86Google Scholar
  182. Zhao M (2009) Electrical fields in wound healing—an overriding signal that directs cell migration. Semin Cell Dev Biol 20:674–682Google Scholar
  183. Zhao M, Forrester JV, McCaig CD (1999a) A small physiological field orients cell division. Proc Natl Acad Sci USA 96:4942–4946Google Scholar
  184. 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 10:1259–1276Google Scholar

Copyright information

© Konrad Lorenz Institute for Evolution and Cognition Research 2014

Authors and Affiliations

  1. 1.John Ray Research Field StationCheshireUK

Personalised recommendations