Molecular bioelectricity in developmental biology: New tools and recent discoveries: Control of cell behavior and pattern formation by transmembrane potential gradients

BioEssays

Volumn 34, Issue 3, 2012, Pages 205-217

  Levin, Michael ^a  

^a TUFTS UNIVERSITY   (United States)

Author keywords

Bioelectricity; Ion channels; Membrane voltage; Prepattern

Indexed keywords

ION; ION CHANNEL; MESSENGER RNA; PROTEIN;

ARTICLE; BIOELECTRIC SIGNAL; CELL DIFFERENTIATION; CELL FUNCTION; CELL INTERACTION; CELL MIGRATION; CELL PROLIFERATION; CRANIOFACIAL DEVELOPMENT; DEVELOPMENTAL BIOLOGY; ELECTRIC POTENTIAL; EMBRYO DEVELOPMENT; FLUORESCENCE; GENE EXPRESSION; HUMAN; ION TRANSPORT; MEMBRANE POTENTIAL; MOLECULAR BIOELECTRICITY; MOLECULAR BIOLOGY; MOLECULAR DYNAMICS; NEOPLASM; NONHUMAN; REGENERATIVE MEDICINE; SIGNAL TRANSDUCTION; TISSUE GROWTH; TISSUE REGENERATION;

ANIMALS; BODY PATTERNING; CELL DIFFERENTIATION; CELL MEMBRANE; CELL POLARITY; DEVELOPMENTAL BIOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; ION CHANNELS; MEMBRANE POTENTIALS; REGENERATION; RNA, MESSENGER; SIGNAL TRANSDUCTION; SURFACE PROPERTIES;

EID: 84857050462     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201100136     Document Type: Article

References (111)

1. Nuccitelli R. 2003. A role for endogenous electric fields in wound healing. Curr Top Dev Biol 58: 1- 26.
2. Zhao M. 2009. Electrical fields in wound healing - an overriding signal that directs cell migration. Semin Cell Dev Biol 20: 674- 82.
3. McCaig CD, Song B, Rajnicek AM. 2009. Electrical dimensions in cell science. J Cell Sci 122: 4267- 76.
4. Robinson K, Messerli M. 1996. Electric embryos: the embryonic epithelium as a generator of developmental information. In McCaig C, ed; Nerve Growth and Guidance. Portland: Portland Press. p. 131- 41.
5. Jenkins LS, Duerstock BS, Borgens RB. 1996. Reduction of the current of injury leaving the amputation inhibits limb regeneration in the red spotted newt. Dev Biol 178: 251- 62.
6. Hotary KB, Robinson KR. 1992. Evidence of a role for endogenous electrical fields in chick embryo development. Development 114: 985- 96.
7. 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- 14.
8. Woodruff R, Telfer W. 1980. Electrophoresis of proteins in intercellular bridges. Nature 286: 84- 6.
9. Borgens RB, Shi R. 1995. Uncoupling histogenesis from morphogenesis in the vertebrate embryo by collapse of the transneural tube potential. Dev Dyn 203: 456- 67.
10. Blackiston DJ, McLaughlin KA, Levin M. 2009. Bioelectric controls of cell proliferation: ion channels, membrane voltage and the cell cycle. Cell Cycle 8: 3519- 28.
11. Cone CD, Cone CM. 1976. Induction of mitosis in mature neurons in central nervous system by sustained depolarization. Science 192: 155- 8.
12. Levin M. 2009. Bioelectric mechanisms in regeneration: unique aspects and future perspectives. Semin Cell Dev Biol 20: 543- 56.
13. Vandenberg LN, Morrie RD, Adams DS. 2011. V-ATPase-dependent ectodermal voltage and pH regionalization are required for craniofacial morphogenesis. Dev Dyn 240: 1889- 904.
14. Tantama M, Hung YP, Yellen G. 2011. Imaging intracellular pH in live cells with a genetically encoded red fluorescent protein sensor. J Am Chem Soc 133: 10034- 7.
15. Tseng AS, Beane WS, Lemire JM, Masi A, et al. 2010. Induction of vertebrate regeneration by a transient sodium current. J Neurosci 30: 13192- 200.
16. Smith PJS, Sanger RS, Messerli MA. 2007. Principles, development and applications of self-referencing electrochemical microelectrodes to the determination of fluxes at cell membranes. In: Michael AC, ed; Methods and New Frontiers in Neuroscience. Boca Raton, FL: CRC Press. Ch. 18, p. 373- 405.
17. Reid B, Nuccitelli R, Zhao M. 2007. Non-invasive measurement of bioelectric currents with a vibrating probe. Nat Protoc 2: 661- 9.
18. Adams DS, Levin M. 2006. Inverse drug screens: a rapid and inexpensive method for implicating molecular targets. Genesis 44: 530- 40.
19. Blackiston D, Adams DS, Lemire JM, Lobikin M, et al. 2011. Transmembrane potential of GlyCl-expressing instructor cells induces a neoplastic-like conversion of melanocytes via a serotonergic pathway. Dis Model Mech 4: 67- 85.
20. Morokuma J, Blackiston D, Adams DS, Seebohm G, et al. 2008. Modulation of potassium channel function confers a hyperproliferative invasive phenotype on embryonic stem cells. Proc Natl Acad Sci USA 105: 16608- 13.
21. 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.
22. Yao L, McCaig CD, Zhao M. 2009. Electrical signals polarize neuronal organelles, direct neuron migration, and orient cell division. Hippocampus 19: 855- 68.
23. Pan L, Borgens RB. 2010. Perpendicular organization of sympathetic neurons within a required physiological voltage. Exp Neurol 222: 161- 4.
24. Nishiyama M, von Schimmelmann MJ, Togashi K, Findley WM, et al. 2008. Membrane potential shifts caused by diffusible guidance signals direct growth-cone turning. Nat Neurosci 11: 762- 71.
25. Ozkucur N, Perike S, Sharma P, Funk RH. 2011. Persistent directional cell migration requires ion transport proteins as direction sensors and membrane potential differences in order to maintain directedness. BMC Cell Biol 12: 4.
26. Cao L, Pu J, Zhao M. 2011. GSK-3beta is essential for physiological electric field-directed Golgi polarization and optimal electrotaxis. Cell Mol Life Sci 68: 3081- 93.
27. Zhao M, Song B, Pu J, Wada T, et al. 2006. Electrical signals control wound healing through phosphatidylinositol-3-OH kinase-gamma and PTEN. Nature 442: 457- 60.
28. Sundelacruz S, Levin M, Kaplan DL. 2008. Membrane potential controls adipogenic and osteogenic differentiation of mesenchymal stem cells. PLoS ONE 3: e3737.
29. Ng SY, Chin CH, Lau YT, Luo J, et al. 2010. Role of voltage-gated potassium channels in the fate determination of embryonic stem cells. J Cell Physiol 224: 165- 77.
30. + channels at tyrosine 242. Development 135: 859- 67.
31. Li F, Yin J, Yue T, Liu L, et al. 2010. The chloride intracellular channel 5 (CLIC5) involved in C2C12 myoblasts proliferation and differentiation. Cell Biol Int 34: 379- 84.
32. Root CM, Velazquez-Ulloa NA, Monsalve GC, Minakova E, et al. 2008. Embryonically expressed GABA and glutamate drive electrical activity regulating neurotransmitter specification. J Neurosci 28: 4777- 84.
33. Yasuda T, Adams DJ. 2010. Physiological roles of ion channels in adult neural stem cells and their progeny. J Neurochem 114: 946- 59.
34. Lange C, Prenninger S, Knuckles P, Taylor V, et al. 2011. The H(+) vacuolar ATPase maintains neural stem cells in the developing mouse cortex. Stem Cells Dev 20: 843- 50.
35. van Vliet P, de Boer TP, van der Heyden MA, El Tamer MK, et al. 2010. Hyperpolarization induces differentiation in human cardiomyocyte progenitor cells. Stem Cell Rev 6: 178- 85.
36. Park JY, Helm JF, Zheng W, Ly QP, et al. 2008. Silencing of the candidate tumor suppressor gene solute carrier family 5 member 8 (SLC5A8) in human pancreatic cancer. Pancreas 36: e32- 9.
37. + channel SCN5A is a key regulator of a gene transcriptional network that controls colon cancer invasion. Cancer Res 70: 6957- 67.
38. Jaffe LF. 1966. Electrical currents through the developing fucus egg. Proc Natl Acad Sci USA 56: 1102- 9.
39. Minc N, Chang F. 2010. Electrical control of cell polarization in the fission yeast Schizosaccharomyces pombe. Curr Biol 20: 710- 6.
40. Michard E, Alves F, Feijo JA. 2009. The role of ion fluxes in polarized cell growth and morphogenesis: the pollen tube as an experimental paradigm. Int J Dev Biol 53: 1609- 22.
41. Certal AC, Almeida RB, Carvalho LM, Wong E, et al. 2008. Exclusion of a proton ATPase from the apical membrane is associated with cell polarity and tip growth in Nicotiana tabacum pollen tubes. Plant Cell 20: 614- 34.
42. Levin M. 2007. Large-scale biophysics: ion flows and regeneration. Trends Cell Biol 17: 262- 71.
43. Lacroix J, Halaszovich CR, Schreiber DN, Leitner MG, et al. 2011. Controlling the activity of a phosphatase and tensin homolog (PTEN) by membrane potential. J Biol Chem 286: 17945- 53.
44. Child CM. 1941. Patterns and Problems of Development. Chicago, IL: The University of Chicago press. ix, p. 811.
45. Beane WS, Morokuma J, Adams DS, Levin M. 2011. A chemical genetics approach reveals H, K-ATPase-mediated membrane voltage is required for planarian head regeneration. Chem Biol 18: 77- 89.
46. + pump-dependent changes in membrane voltage are an early mechanism necessary and sufficient to induce Xenopus tail regeneration. Development 134: 1323- 35.
47. Esser AT, Smith KC, Weaver JC, Levin M. 2006. Mathematical model of morphogen electrophoresis through gap junctions. Dev Dyn 235: 2144- 59.
48. Wang X, Veruki ML, Bukoreshtliev NV, Hartveit E, et al. 2010. Animal cells connected by nanotubes can be electrically coupled through interposed gap-junction channels. Proc Natl Acad Sci USA 107: 17194- 9.
49. Pai VP, Aw S, Shomrat T, Lemire JM, et al. 2012. Transmembrane voltage potential conrols embryonic eye patterning in Xenopus laevis. Development 139: 313- 23.
50. Aw S, Levin M. 2009. Is left-right asymmetry a form of planar cell polarity? Development 136: 355- 66.
51. Burr HS, Sinnott EW. 1944. Electrical correlates of form in cucurbit fruits. Am J Bot 31: 249- 53.
52. Burr HS, Hovland CI. 1937. Bio-electric correlates of development in amblystoma. Yale J Biol Med 9: 540- 9.
53. Yamashita M. 2011. Fluctuations in nuclear envelope's potential mediate synchronization of early neural activity. Biochem Biophys Res Commun 406: 107- 11.
54. Tyner KM, Kopelman R, Philbert MA. 2007. " Nanosized voltmeter" enables cellular-wide electric field mapping. Biophys J 93: 1163- 74.
55. O'Connell KM, Rolig AS, Whitesell JD, Tamkun MM. 2006. Kv2.1 potassium channels are retained within dynamic cell surface microdomains that are defined by a perimeter fence. J Neurosci 26: 9609- 18.
56. O'Connell KM, Tamkun MM. 2005. Targeting of voltage-gated potassium channel isoforms to distinct cell surface microdomains. J Cell Sci 118: 2155- 66.
57. Wallace R. 2007. Neural membrane microdomains as computational systems: toward molecular modeling in the study of neural disease. Biosystems 87: 20- 30.
58. Bonchev D, Thomas S, Apte A, Kier LB. 2010. Cellular automata modelling of biomolecular networks dynamics. SAR QSAR Environ Res 21: 77- 102.
59. Brock A, Chang H, Huang S. 2009. Non-genetic heterogeneity - a mutation-independent driving force for the somatic evolution of tumours. Nat Rev Genet 10: 336- 42.
60. Yu K, Ruan DY, Ge SY. 2002. Three electrophysiological phenotypes of cultured human umbilical vein endothelial cells. Gen Physiol Biophys 21: 315- 26.
61. Akemann W, Lundby A, Mutoh H, Knopfel T. 2009. Effect of voltage sensitive fluorescent proteins on neuronal excitability. Biophys J 96: 3959- 76.
62. Mennerick S, Chisari M, Shu HJ, Taylor A, et al. 2010. Diverse voltage-sensitive dyes modulate GABAA receptor function. J Neurosci 30: 2871- 9.
63. Adams DS, Levin M. 2006. Strategies and techniques for investigation of biophysical signals in patterning. In: Whitman M, Sater AK, eds; Analysis of Growth Factor Signaling in Embryos. Boca Raton, FL: CRC press. p. 177- 262.
64. Gallaher J, Bier M, van Heukelom JS. 2010. First order phase transition and hysteresis in a cell's maintenance of the membrane potential - an essential role for the inward potassium rectifiers. Biosystems 101: 149- 55.
65. Sachdeva G, Kalyanasundaram K, Krishnan J, Chakravarthy VS. 2010. Bistable dynamics of cardiac cell models coupled by dynamic gap junctions linked to cardiac memory. Biol Cybern 102: 109- 21.
66. Xiong W, Ferrell JE, Jr. 2003. A positive-feedback-based bistable 'memory module' that governs a cell fate decision. Nature 426: 460- 5.
67. Levin M. 2006. Is the early left-right axis like a plant, a kidney, or a neuron? The integration of physiological signals in embryonic asymmetry. Birth Defects Res C Embryo Today 78: 191- 223.
68. Fischbarg J, Diecke FP. 2005. A mathematical model of electrolyte and fluid transport across corneal endothelium. J Membr Biol 203: 41- 56.
69. Hechavarria D, Dewilde A, Braunhut S, Levin M, et al. 2010. BioDome regenerative sleeve for biochemical and biophysical stimulation of tissue regeneration. Med Eng Phys 32: 1065- 73.
70. Reid B, Graue-Hernandez EO, Mannis MJ, Zhao M. 2011. Modulating endogenous electric currents in human corneal wounds-a novel approach of bioelectric stimulation without electrodes. Cornea 30: 338- 43.
71. Skinner JE, Molnar M, Vybiral T, Mitra M. 1992. Application of chaos theory to biology and medicine. Integr Physiol Behav Sci 27: 39- 53.
72. Turner CH, Robling AG, Duncan RL, Burr DB. 2002. Do bone cells behave like a neuronal network? Calcif Tissue Int 70: 435- 42.
73. Caporale N, Kolstad KD, Lee T, Tochitsky I, et al. 2011. LiGluR restores visual responses in rodent models of inherited blindness. Mol Ther 19: 1212- 9.
74. Roberts A, Stirling CA. 1971. Properties and propagation of a cardiac-like impulse in skin of young tadpoles. Zeitschrift Fur Vergleichende Physiologie 71: 295- 310.
75. +-V-ATPase-dependent proton flux is necessary for consistent left-right patterning of non-mammalian vertebrates. Development 133: 1657- 71.
76. Oviedo NJ, Nicolas CL, Adams DS, Levin M. 2008. Live imaging of planarian membrane potential using DiBAC4(3). CSH Protoc pdb prot5055.
77. Ozkucur N, Epperlein HH, Funk RH. 2010. Ion imaging during axolotl tail regeneration in vivo. Dev Dyn 239: 2048- 57.
78. Tsutsui H, Karasawa S, Okamura Y, Miyawaki A. 2008. Improving membrane voltage measurements using FRET with new fluorescent proteins. Nat Methods 5: 683- 5.
79. Mutoh H, Perron A, Akemann W, Iwamoto Y, et al. 2011. Optogenetic monitoring of membrane potentials. Exp Physiol 96: 13- 8.
80. Akemann W, Mutoh H, Perron A, Rossier J, et al. 2010. Imaging brain electric signals with genetically targeted voltage-sensitive fluorescent proteins. Nat Methods 7: 643- 9.
81. Murata Y, Iwasaki H, Sasaki M, Inaba K, et al. 2005. Phosphoinositide phosphatase activity coupled to an intrinsic voltage sensor. Nature 435: 1239- 43.
82. Mutoh H, Perron A, Dimitrov D, Iwamoto Y, et al. 2009. Spectrally-resolved response properties of the three most advanced FRET based fluorescent protein voltage probes. PLoS ONE 4: e4555.
83. Schiffmann Y. 2011. Turing-Child field underlies spatial periodicity in Drosophila and planarians. Prog Biophys Mol Biol 105: 258- 69.
84. Zhang Y, Levin M. 2009. Particle tracking model of electrophoretic morphogen movement reveals stochastic dynamics of embryonic gradient. Dev Dyn 238: 1923- 35.
85. Garny A, Nickerson DP, Cooper J, Weber dos Santos R, et al. 2008. CellML and associated tools and techniques. Philos Transact A Math Phys Eng Sci 366: 3017- 43.
86. Schultheis C, Liewald JF, Bamberg E, Nagel G, et al. 2011. Optogenetic long-term manipulation of behavior and animal development. PLoS ONE 6: e18766.
87. Arrenberg AB, Stainier DY, Baier H, Huisken J. 2010. Optogenetic control of cardiac function. Science 330: 971- 4.
88. Wyart C, Del Bene F, Warp E, Scott EK, et al. 2009. Optogenetic dissection of a behavioural module in the vertebrate spinal cord. Nature 461: 407- 10.
89. Arrenberg AB, Del Bene F, Baier H. 2009. Optical control of zebrafish behavior with halorhodopsin. Proc Natl Acad Sci USA 106: 17968- 73.
90. Tomita H, Sugano E, Fukazawa Y, Isago H, et al. 2009. Visual properties of transgenic rats harboring the channelrhodopsin-2 gene regulated by the thy-1.2 promoter. PLoS ONE 4: e7679.
91. Fortin DL, Dunn TW, Kramer RH. 2011. Engineering light-regulated ion channels. Cold Spring Harb Protoc 2011: 579- 85.
92. Fortin DL, Banghart MR, Dunn TW, Borges K, et al. 2008. Photochemical control of endogenous ion channels and cellular excitability. Nat Methods 5: 331- 8.
93. Onkal R, Djamgoz MB. 2009. Molecular pharmacology of voltage-gated sodium channel expression in metastatic disease: clinical potential of neonatal Nav1.5 in breast cancer. Eur J Pharmacol 625: 206- 19.
94. Pardo LA, del Camino D, Sanchez A, Alves F, et al. 1999. Oncogenic potential of EAG K(+) channels. EMBO J 18: 5540- 7.
95. + channel function. Proc Natl Acad Sci USA 100: 7803- 7.
96. Saito T, Schlegel R, Andresson T, Yuge L, et al. 1998. Induction of cell transformation by mutated 16K vacuolar H+-ATPase (ductin) is accompanied by down-regulation of gap junctional intercellular communication and translocation of connexin 43 in NIH3T3cells. Oncogene 17: 1673- 80.
97. Gupta N, Martin PM, Prasad PD, Ganapathy V. 2006. SLC5A8 (SMCT1)-mediated transport of butyrate forms the basis for the tumor suppressive function of the transporter. Life Sci 78: 2419- 25.
98. Roepke TK, Purtell K, King EC, La Perle KM, et al. 2010. Targeted deletion of Kcne2 causes gastritis cystica profunda and gastric neoplasia. PLoS ONE 5: e11451.
99. Dinicola S, D'Anselmi F, Pasqualato A, Proietti S, et al. 2011. A systems biology approach to cancer: fractals, attractors, and nonlinear dynamics. OMICS 15: 93- 104.
100. Potter JD. 2007. Morphogens, morphostats, microarchitecture and malignancy. Nat Rev Cancer 7: 464- 74.
101. Rock JR, Futtner CR, Harfe BD. 2008. The transmembrane protein TMEM16A is required for normal development of the murine trachea. Dev Biol 321: 141- 9.
102. Iwashita M, Watanabe M, Ishii M, Chen T, et al. 2006. Pigment pattern in jaguar/obelix zebrafish is caused by a Kir7.1 mutation: Implications for the regulation of melanosome movement. PLoS Genet 2: e197.
103. Teng GQ, Zhao X, Lees-Miller JP, Quinn FR, et al. 2008. Homozygous missense N629D hERG (KCNH2) potassium channel mutation causes developmental defects in the right ventricle and its outflow tract and embryonic lethality. Circ Res 103: 1483- 91.
104. Watanabe M, Iwashita M, Ishii M, Kurachi Y, et al. 2006. Spot pattern of leopard Danio is caused by mutation in the zebrafish connexin41.8 gene. EMBO Rep 7: 893- 7.
105. Hoptak-Solga AD, Nielsen S, Jain I, Thummel R, et al. 2008. Connexin43 (GJA1) is required in the population of dividing cells during fin regeneration. Dev Biol 317: 541- 8.
106. Iovine MK, Higgins EP, Hindes A, Coblitz B, et al. 2005. Mutations in connexin43 (GJA1) perturb bone growth in zebrafish fins. Dev Biol 278: 208- 19.
107. Bendahhou S, Donaldson MR, Plaster NM, Tristani-Firouzi M, et al. 2003. Defective potassium channel Kir2.1 trafficking underlies Andersen-Tawil syndrome. J Biol Chem 278: 51779- 85.
108. Binggeli R, Weinstein R. 1986. Membrane potentials and sodium channels: hypotheses for growth regulation and cancer formation based on changes in sodium channels and gap junctions. J Theor Biol 123: 377- 401.
109. Stillwell EF, Cone CM, Cone CD. 1973. Stimulation of DNA synthesis in CNS neurones by sustained depolarisation. Nat New Biol 246: 110- 1.
110. + channel components are involved in early left-right patterning in Xenopus laevis embryos. Cell Physiol Biochem 21: 357- 72.
111. Barrett T, Troup DB, Wilhite SE, Ledoux P, et al. 2011. NCBI GEO: archive for functional genomics data sets - 10 years on. Nucleic Acids Res 39: D1005- 10.