Molecular bioelectricity: How endogenous voltage potentials control cell behavior and instruct pattern regulation in vivo

Molecular Biology of the Cell

Volumn 25, Issue 24, 2014, Pages 3835-3850

  Levin, Michael ^a  

^a TUFTS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ION CHANNEL; VOLTAGE GATED CALCIUM CHANNEL;

ANATOMICAL CONCEPTS; APOPTOSIS; ARTICLE; BIOENERGY; CELL DEDIFFERENTIATION; CELL DIFFERENTIATION; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; CELL SHAPE; CELL TYPE; ELECTRIC POTENTIAL; ELECTRICAL SYNAPSE; EYE DEVELOPMENT; GAP JUNCTION; GENE EXPRESSION; HUMAN; IN VIVO STUDY; LIMB REGENERATION; MEMBRANE STEADY POTENTIAL; MOLECULAR GENETICS; NONHUMAN; SECOND MESSENGER; SIGNAL TRANSDUCTION; SOMATIC CELL; STEM CELL; ANIMAL; BIOLOGICAL MODEL; CELL COMMUNICATION; ELECTROPHYSIOLOGY; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORK; GENETICS; MORPHOGENESIS;

ANIMALS; BODY PATTERNING; CELL COMMUNICATION; CELL PHYSIOLOGICAL PHENOMENA; ELECTROPHYSIOLOGICAL PHENOMENA; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORKS; HUMANS; MODELS, GENETIC; SIGNAL TRANSDUCTION;

EID: 84913555653     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E13-12-0708     Document Type: Article

References (338)

1. Adamatzky A, Costello B, Bull L, Holley J (2011). Towards arithmetic circuits in sub-excitable chemical media. Israel J Chem 51, 56-66.
2. Adams DS (2008). A new tool for tissue engineers: ions as regulators of morphogenesis during development and regeneration. Tissue Eng Part A 14, 1461-1468.
3. Adams DS, Levin M (2006a). Inverse drug screens: a rapid and inexpensive method for implicating molecular targets. Genesis 44, 530-540.
4. Adams DS, Levin M (2006b). Strategies and techniques for investigation of biophysical signals in patterning. In: Analysis of Growth Factor Signaling in Embryos, ed. M Whitman and AK Sater, Oxford, UK: Taylor and Francis, 177-262.
5. Adams DS, Levin M (2012a). General principles for measuring resting membrane potential and ion concentration using fluorescent bioelectricity reporters. Cold Spring Harb Protoc 2012, 385-397.
6. Adams DS, Levin M (2012b). Measuring resting membrane potential using the fluorescent voltage reporters DiBAC4(3) and CC2-DMPE. Cold Spring Harb Protoc 2012, 459-464.
7. Adams DS, Levin M (2013). Endogenous voltage gradients as mediators of cell-cell communication: strategies for investigating bioelectrical signals during pattern formation. Cell Tissue Res 352, 95-122.
8. 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.
9. Adams DS, Robinson KR, Fukumoto T, Yuan S, Albertson RC, Yelick P, Kuo L, McSweeney M, Levin M (2006). Early, H+-V-ATPase-dependent proton flux is necessary for consistent left-right patterning of non-mammalian vertebrates. Development 133, 1657-1671.
10. Adams DS, Tseng AS, Levin M (2013). Light-activation of the Archaerhodopsin H(+)-pump reverses age-dependent loss of vertebrate regeneration: sparking system-level controls in vivo. Biol Open 2, 306-313.
11. Akemann W, Mutoh H, Perron A, Kyung Park Y, Iwamoto Y, Knopfel T (2012). Imaging neural circuit dynamics with a voltage-sensitive fluorescent protein. J Neurophys 108, 2323-2337.
12. Albrecht-Buehler G (1985). Is cytoplasm intelligent too? Cell Muscle Motil 6, 1-21.
13. Alves H, Dechering K, Van Blitterswijk C, De Boer J (2011). High-throughput assay for the identification of compounds regulating osteogenic differentiation of human mesenchymal stromal cells. PLoS One 6, e26678.
14. Anava S, Saad Y, Ayali A (2013). The role of gap junction proteins in the development of neural network functional topology. Insect Mol Biol 2, 457-472.
15. Anderson JD (1951). Galvanotaxis of slime mold. J Gen Physiol 35, 1-16.
16. Aprea J, Calegari F (2012). Bioelectric state and cell cycle control of mammalian neural stem cells. Stem Cells Int 2012, 816049.
17. Arcangeli A, Bianchi L, Becchetti A, Faravelli L, Coronnello M, Mini E, Olivotto M, Wanke E (1995). A novel inward-rectifying K+ current with a cell-cycle dependence governs the resting potential of mammalian neuroblastoma cells. J Physiol 489, 455-471.
18. Arcangeli A, Carla M, Bene M, Becchetti A, Wanke E, Olivotto M (1993). Polar/apolar compounds induce leukemia cell differentiation by modulating cell-surface potential. Proc Natl Acad Sci USA 90, 5858-5862.
19. Arcangeli A, Crociani O, Lastraioli E, Masi A, Pillozzi S, Becchetti A (2009). Targeting ion channels in cancer: a novel frontier in antineoplastic therapy. Curr Med Chem 16, 66-93.
20. Arcangeli A, Pillozzi S, Becchetti A (2012). Targeting ion channels in leukemias: a new challenge for treatment. Curr Med Chem 19, 683-696.
21. Aryasomayajula A, Derix J, Perike S, Gerlach G, Funk RH (2010). DC microelectrode array for investigating the intracellular ion changes. Biosens Bioelectron 26, 1268-1272.
22. Aur D (2012). From neuroelectrodynamics to thinking machines. Cogn Comput 4, 4-12.
23. Aw S, Adams DS, Qiu D, Levin M (2008). H,K-ATPase protein localization and Kir4.1 function reveal concordance of three axes during early determination of left-right asymmetry. Mech Dev 125, 353-372.
24. Aw S, Koster J, Pearson W, Nichols C, Shi NQ, Carneiro K, Levin M (2010). The ATP-sensitive K(+)-channel (K(ATP)) controls early left-right patterning in Xenopus and chick embryos. Dev Biol 346, 39-53.
25. Aw S, Levin M (2009). Is left-right asymmetry a form of planar cell polarity? Development 136, 355-366.
26. Baglioni S, Cantini G, Poli G, Francalanci M, Squecco R, Di Franco A, Borgogni E, Frontera S, Nesi G, Liotta F, et al. (2012). Functional differences in visceral and subcutaneous fat pads originate from differences in the adipose stem cell. PLoS One 7, e36569.
27. Barel O, Shalev SA, Ofir R, Cohen A, Zlotogora J, Shorer Z, Mazor G, Finer G, Khateeb S, Zilberberg N, et al. (2008). Maternally inherited Birk Barel mental retardation dysmorphism syndrome caused by a mutation in the genomically imprinted potassium channel KCNK9. Am J Hum Genet 83, 193-199.
28. Bartel DP, Sheng M, Lau LF, Greenberg ME (1989). Growth factors and membrane depolarization activate distinct programs of early response gene expression: dissociation of fos and jun induction. Genes Dev 3, 304-313.
29. Barth LG, Barth LJ (1974a). Ionic regulation of embryonic induction and cell differentiation in Rana pipiens. Dev Biol 39, 1-22.
30. Barth LJ, Barth LG (1974b). Effect of the potassium ion on induction of notochord from gastrula ectoderm of Rana pipiens. Biol Bull 146, 313-325.
31. Bauer R, Lehmann C, Fuss B, Eckardt F, Hoch M (2002). The Drosophila gap junction channel gene innexin 2 controls foregut development in response to Wingless signalling. J Cell Sci 115, 1859-1867.
32. Bauer R, Lehmann C, Martini J, Eckardt F, Hoch M (2004). Gap junction channel protein innexin 2 is essential for epithelial morphogenesis in the Drosophila embryo. Mol Biol Cell 15, 2992-3004.
33. 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.
34. Beane WS, Morokuma J, Lemire JM, Levin M (2013). Bioelectric signaling regulates head and organ size during planarian regeneration. Development 140, 313-322.
35. Becchetti A (2011). Ion channels and transporters in cancer. 1. Ion channels and cell proliferation in cancer. Am J Physiol Cell Physiol 301, C255-265.
36. Beloussov LV (2008). Mechanically based generative laws of morphogenesis. Phys Biol 5, 015009.
37. Beloussov L (2011). Mechanoelectrical and photon-generating devices in cells and organisms: from molecular machines to macroscopic fields. J Phys Conf Ser 329, 012008.
38. Beloussov LV, Grabovsky VI (2006). Morphomechanics: goals, basic experiments and models. Int J Dev Biol 50, 81-92.
39. Bendahhou S, Donaldson MR, Plaster NM, Tristani-Firouzi M, Fu YH, Ptacek LJ (2003). Defective potassium channel Kir2.1 trafficking underlies Andersen-Tawil syndrome. J Biol Chem 278, 51779-51785.
40. Bennett ES, Smith BA, Harper JM (2004). Voltage-gated Na+ channels confer invasive properties on human prostate cancer cells. Pflugers Arch 447, 908-914.
41. Bentrup F, Sandan T, Jaffe L (1967). Induction of polarity in Fucus eggs by potassium ion gradients. Protoplasma 64, 254.
42. Ben-Zvi D, Shilo BZ, Barkai N (2011). Scaling of morphogen gradients. Curr Opin Genet Dev 21, 704-710.
43. 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.
44. Birmingham K, Gradinaru V, Anikeeva P, Grill WM, Pikov V, McLaughlin B, Pasricha P, Weber D, Ludwig K, Famm K (2014). Bioelectronic medicines: a research roadmap. Nat Rev Drug Discov 13, 399-400.
45. Blackiston D, Adams DS, Lemire JM, Lobikin M, Levin M (2011). Transmembrane potential of GlyCl-expressing instructor cells induces a neoplastic-like conversion of melanocytes via a serotonergic pathway. Dis Models Mech 4, 67-85.
46. Blackiston D, Anderson GM, Rahman N, Bieck C, Levin M (2015). A novel method for inducing nerve growth via modulation of host resting potential. Neurotherapeutics (in press).
47. Boettiger A, Ermentrout B, Oster G (2009). The neural origins of shell structure and pattern in aquatic mollusks. Proc Natl Acad Sci USA 106, 6837-6842.
48. Boettiger AN, Oster G (2009). Emergent complexity in simple neural systems. Commun Integr Biol 2, 467-470.
49. Borgens RB (1986). The role of natural and applied electric fields in neuronal regeneration and development. Prog Clin Biol Res 210, 239-250.
50. Borgens RB, Blight AR, McGinnis ME (1987). Behavioral recovery induced by applied electric fields after spinal cord hemisection in guinea pig. Science 238, 366-369.
51. 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.
52. Borgens RB, Blight AR, Murphy DJ (1986). Axonal regeneration in spinal cord injury: a perspective and new technique. J Comp Neurol 250, 157-167.
53. Borgens R, Robinson K, Vanable J, McGinnis M (1989). Electric Fields in Vertebrate Repair, New York: Alan R. Liss.
54. Borgens RB, Shi R (1995). Uncoupling histogenesis from morphogenesis in the vertebrate embryo by collapse of the transneural tube potential. Dev Dyn 203, 456-467.
55. Borthwick KJ, Kandemir N, Topaloglu R, Kornak U, Bakkaloglu A, Yordam N, Ozen S, Mocan H, Shah GN, Sly WS, et al. (2003). A phenocopy of CAII deficiency: a novel genetic explanation for inherited infantile osteopetrosis with distal renal tubular acidosis. J Med Genet 40, 115-121.
56. Britz-Cunningham S, Shah M, Zuppan C, Fletcher W (1995). Mutations of the connexin-43 gap-junction gene in patients with heart malformations and defects of laterality. N Engl J Med 332, 1323-1329.
57. Burr HS (1941). Changes in the field properties of mice with transplanted tumors. Yale J Biol Med 13, 783-788.
58. Burr HS, Northrop FSC (1935). The electro-dynamic theory of life. Q Rev Biol 10, 322-333.
59. Burr HS, Smith GM, Strong LC (1940). Electrometric studies of tumors in mice induced by the external application of benzpyrene. Yale J Biol Med 12, 711-717.
60. Bustamante JO, Hanover JA, Liepins A (1995). The ion channel behavior of the nuclear pore complex. J Membr Biol 146, 239-251.
61. Campetelli A, Bonazzi D, Minc N (2012). Electrochemical regulation of cell polarity and the cytoskeleton. Cytoskeleton (Hoboken) 69, 601-612.
62. 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, 3081-3093.
63. Cao L, Wei D, Reid B, Zhao S, Pu J, Pan T, Yamoah E, Zhao M (2013). Endogenous electric currents might guide rostral migration of neuroblasts. EMBO Rep 14, 184-190 .
64. Casimiro MC, Knollmann BC, Yamoah EN, Nie L, Vary JC Jr, Sirenko SG, Greene AE, Grinberg A, Huang SP, Ebert SN, Pfeifer K (2004). Targeted point mutagenesis of mouse Kcnq1: phenotypic analysis of mice with point mutations that cause Romano-Ward syndrome in humans. Genomics 84, 555-564.
65. Certal AC, Almeida RB, Carvalho LM, Wong E, Moreno N, Michard E, Carneiro J, Rodriguez-Leon J, Wu HM, Cheung AY, 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, 614-634.
66. Chakravarty S, Rizvi SI (2011). Circadian modulation of sodium-potassium ATPase and sodium - proton exchanger in human erythrocytes: in vitro effect of melatonin. Cell Mol Biol 57, 80-86.
67. Chan JD, Agbedanu PN, Zamanian M, Gruba SM, Haynes CL, Day TA, Marchant JS (2014). "Death and axes": unexpected ca(2+) entry phenologs predict new anti-schistosomal agents. PLoS Pathog 10, e1003942.
68. Chen PS, Garfinkel A, Weiss JN, Karagueuzian HS (1997). Spirals, chaos, and new mechanisms of wave propagation. Pacing Clin Electrophysiol 20, 414-421.
69. Chernet BT, Levin M (2013a). Transmembrane voltage potential is an essential cellular parameter for the detection and control of tumor development in a Xenopus model. Dis Models Mech 6, 595-607.
70. Chernet B, Levin M (2013b). Endogenous voltage potentials and the microenvironment: bioelectric signals that reveal, induce and normalize cancer. J Exp Clin Oncol, doi:10.4172/2324-9110.S1-002.
71. Chernet BT, Levin M (2014). Transmembrane voltage potential of somatic cells controls oncogene-mediated tumorigenesis at long-range. Oncotarget 5, 3287-3306.
72. Chifflet S, Hernandez JA, Grasso S, Cirillo A (2003). Nonspecific depolarization of the plasma membrane potential induces cytoskeletal modifications of bovine corneal endothelial cells in culture. Exp Cell Res 282, 1-13.
73. Chinnery HR, Pearlman E, McMenamin PG (2008). Cutting edge: membrane nanotubes in vivo: a feature of MHC class II +cells in the mouse cornea. J Immunol 180, 5779-5783.
74. Chopra SS, Stroud DM, Watanabe H, Bennett JS, Burns CG, Wells KS, Yang T, Zhong TP, Roden DM (2010). Voltage-gated sodium channels are required for heart development in zebrafish. Circ Res 106, 1342-1350.
75. Chouabe C, Neyroud N, Guicheney P, Lazdunski M, Romey G, Barhanin J (1997). Properties of KvLQT1 K +channel mutations in Romano-Ward and Jervell and Lange-Nielsen inherited cardiac arrhythmias. EMBO J 16, 5472-5479.
76. Chow RL, Altmann CR, Lang RA, Hemmati-Brivanlou A (1999). Pax6 induces ectopic eyes in a vertebrate. Dev Suppl 126, 4213-4222.
77. Cifra M, Fields JZ, Farhadi A (2011). Electromagnetic cellular interactions. Prog Biophys Mol Biol 105, 223-246.
78. Civitelli R (2008). Cell-cell communication in the osteoblast/osteocyte lineage. Arch Biochem Biophys 473, 188-192.
79. Cone CD Jr (1970). Variation of the transmembrane potential level as a basic mechanism of mitosis control. Oncology 24, 438-470.
80. Cone CD (1971). Unified theory on the basic mechanism of normal mitotic control and oncogenesis. J Theor Biol 30, 151-181.
81. Cone CD (1974). The role of the surface electrical transmembrane potential in normal and malignant mitogenesis. Ann NY Acad Sci 238, 420-435.
82. Cone CD, Cone CM (1976). Induction of mitosis in mature neurons in central nervous system by sustained depolarization. Science 192, 155-158.
83. Cone CD, Tongier M (1971). Control of somatic cell mitosis by simulated changes in the transmembrane potential level. Oncology 25, 168-182.
84. Cone CD, Tongier M (1973). Contact inhibition of division: involvement of the electrical transmembrane potential. J Cell Physiol 82, 373-386.
85. Culiat CT, Stubbs LJ, Woychik RP, Russell LB, Johnson DK, Rinchik EM (1995). Deficiency of the beta 3 subunit of the type A gamma-aminobutyric acid receptor causes cleft palate in mice. Nat Genet 11, 344-346.
86. Dahal GR, Rawson J, Gassaway B, Kwok B, Tong Y, Ptacek LJ, Bates E (2012). An inwardly rectifying K+ channel is required for patterning. Development 139, 3653-3664.
87. Davidson LA (2012). Epithelial machines that shape the embryo. Trends Cell Biol 22, 82-87.
88. Davie JR (2003). Inhibition of histone deacetylase activity by butyrate. J Nutr 133, 2485S-2493S.
89. Davy A, Bush JO, Soriano P (2006). Inhibition of gap junction communication at ectopic Eph/ephrin boundaries underlies craniofrontonasal syndrome. PLoS Biol 4, e315.
90. Debeer P, Van Esch H, Huysmans C, Pijkels E, De Smet L, Van de Ven W, Devriendt K, Fryns JP (2005). Novel GJA1 mutations in patients with oculo-dento-digital dysplasia (ODDD). Eur J Med Genet 48, 377-387.
91. Ding F, Zhang G, Liu L, Jiang L, Wang R, Zheng Y, Wang G, Xie M, Duan Y (2012). Involvement of cationic channels in proliferation and migration of human mesenchymal stem cells. Tissue Cell 44, 358-364.
92. Dolmetsch RE, Xu K, Lewis RS (1998). Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392, 933-936.
93. Du Y, Du Z, Zheng H, Wang D, Li S, Yan Y, Li Y (2013). GABA exists as a negative regulator of cell proliferation in spermaogonial stem cells. Cell Mol Biol Lett 18, 149-162.
94. Dubach JM, Balaconis MK, Clark HA (2011a). Fluorescent nanoparticles for the measurement of ion concentration in biological systems. J Vis Exp, DOI:10.3791/2896.
95. Dubach JM, Lim E, Zhang N, Francis KP, Clark H (2011b). In vivo sodium concentration continuously monitored with fluorescent sensors. Integr Biol (Camb) 3, 142-148.
96. Ewart JL, Cohen MF, Meyer RA, Huang GY, Wessels A, Gourdie RG, Chin AJ, Park SM, Lazatin BO, Villabon S, et al. (1997). Heart and neural tube defects in transgenic mice overexpressing the Cx43 gap junction gene. Development 124, 1281-1292.
97. Famm K, Litt B, Tracey KJ, Boyden ES, Slaoui M (2013). Drug discovery: a jump-start for electroceuticals. Nature 496, 159-161.
98. Farhadi A, Forsyth C, Banan A, Shaikh M, Engen P, Fields JZ, Keshavarzian A (2007). Evidence for non-chemical, non-electrical intercellular signaling in intestinal epithelial cells. Bioelectrochemistry 71, 142-148.
99. Felder CC, MacArthur L, Ma AL, Gusovsky F, Kohn EC (1993). Tumor-suppressor function of muscarinic acetylcholine receptors is associated with activation of receptor-operated calcium influx. Proc Natl Acad Sci USA 90, 1706-1710.
100. Fels D (2009). Cellular communication through light. PLoS One 4, e5086.
101. Fenton FH, Evans SJ, Hastings HM (1999). Memory in an excitable medium: a mechanism for spiral wave breakup in the low-excitability limit. Phys Rev Lett 83, 3964-3967.
102. Fraser SP, Diss JK, Chioni AM, Mycielska ME, Pan H, Yamaci RF, Pani F, Siwy Z, Krasowska M, Grzywna Z, et al. (2005). Voltage-gated sodium channel expression and potentiation of human breast cancer metastasis. Clin Cancer Res 11, 5381-5389.
103. Fukumoto T, Blakely R, Levin M (2005a). Serotonin transporter function is an early step in left-right patterning in chick and frog embryos. Dev Neurosci 27, 349-363.
104. Fukumoto T, Kema IP, Levin M (2005b). Serotonin signaling is a very early step in patterning of the left-right axis in chick and frog embryos. Curr Biol 15, 794-803.
105. Funk RH, Monsees T, Ozkucur N (2009). Electromagnetic effects-from cell biology to medicine. Prog Histochem Cytochem 43, 177-264.
106. Gabriel LA, Sachdeva R, Marcotty A, Rockwood EJ, Traboulsi EI (2011). Oculodentodigital dysplasia: new ocular findings and a novel connexin 43 mutation. Arch Ophthalmol 129, 781-784.
107. Geard N, Willadsen K (2009). Dynamical approaches to modeling developmental gene regulatory networks. Birth Defects Res C Embryo Today 87, 131-142.
108. Gershenson C (2012). Guiding the self-organization of random Boolean networks. Theory Biosci 131, 181-191.
109. Gloyn AL, Pearson ER, Antcliff JF, Proks P, Bruining GJ, Slingerland AS, Howard N, Srinivasan S, Silva JM, Molnes J, et al. (2004). Activating mutations in the gene encoding the ATP-sensitive potassium-channel subunit Kir6.2 and permanent neonatal diabetes. N Engl J Med 350, 1838-1849.
110. Gorgcki J, Gorgcka FN (2007). Chemical wave based programming in reaction-diffusion systems. Int J Unconv Comput 3, 259-270.
111. Greer PL, Greenberg ME (2008). From synapse to nucleus: calcium-dependent gene transcription in the control of synapse development and function. Neuron 59, 846-860.
112. 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, 2419-2425.
113. Harrington DB, Becker RO (1973). Electrical stimulation of RNA and protein synthesis in the frog erythrocyte. Exp Cell Res 76, 95-98.
114. Hatten ME, Liem RK, Mason CA (1986). Weaver mouse cerebellar granule neurons fail to migrate on wild-type astroglial processes in vitro. J Neurosci 6, 2676-2683.
115. He XB, Yi SH, Rhee YH, Kim H, Han YM, Lee SH, Lee H, Park CH, Lee YS, Richardson E, et al. (2011). Prolonged membrane depolarization enhances midbrain dopamine neuron differentiation via epigenetic histone modifications. Stem Cells 29, 1861-1873.
116. Hermle T, Saltukoglu D, Grunewald J, Walz G, Simons M (2010). Regulation of Frizzled-dependent planar polarity signaling by a V-ATPase subunit. Curr Biol 20, 1269-1276.
117. Higashimori H, Sontheimer H (2007). Role of Kir4.1 channels in growth control of glia. Glia 55, 1668-1679.
118. Higuchi H, Iwasa A, Yoshida H, Miki N (1990). Long lasting increase in neuropeptide Y gene expression in rat adrenal gland with reserpine treatment: positive regulation of transsynaptic activation and membrane depolarization. Mol Pharmacol 38, 614-623.
119. Hinard V, Belin D, Konig S, Bader CR, Bernheim L (2008). Initiation of human myoblast differentiation via dephosphorylation of Kir2.1 K+ channels at tyrosine 242. Development 135, 859-867.
120. Homanics GE, DeLorey TM, Firestone LL, Quinlan JJ, Handforth A, Harrison NL, Krasowski MD, Rick CE, Korpi ER, Makela R, et al. (1997). Mice devoid of gamma-aminobutyrate type A receptor beta3 subunit have epilepsy, cleft palate, and hypersensitive behavior. Proc Natl Acad Sci USA 94, 4143-4148.
121. Hoptak-Solga AD, Nielsen S, Jain I, Thummel R, Hyde DR, Iovine MK (2008). Connexin43 (GJA1) is required in the population of dividing cells during fin regeneration. Dev Biol 317, 541-548.
122. Hotary KB, Robinson KR (1992). Evidence of a role for endogenous electrical fields in chick embryo development. Development 114, 985-996.
123. House CD, Vaske CJ, Schwartz AM, Obias V, Frank B, Luu T, Sarvazyan N, Irby R, Strausberg RL, Hales TG, et al. (2010). Voltage-gated Na+ channel SCN5A is a key regulator of a gene transcriptional network that controls colon cancer invasion. Cancer Res 70, 6957-6967.
124. Hronik-Tupaj M, Kaplan DL (2012). A review of the responses of two- and three-dimensional engineered tissues to electric fields. Tissue Eng Part B Rev 18, 167-180.
125. Huang S, Eichler G, Bar-Yam Y, Ingber DE (2005). Cell fates as high-dimensional attractor states of a complex gene regulatory network. Phys Rev Lett 94, 128701.
126. Hyman L, Bellamy A (1922). Studies on the correlation between metabolic gradients, electrical gradients, and galvanotaxis I. Biol Bull 43, 313-347.
127. Inaba M, Yamanaka H, Kondo S (2012). Pigment pattern formation by contact-dependent depolarization. Science 335, 677.
128. Iovine MK, Higgins EP, Hindes A, Coblitz B, Johnson SL (2005). Mutations in connexin43 (GJA1) perturb bone growth in zebrafish fins. Dev Biol 278, 208-219.
129. Iwashita M, Watanabe M, Ishii M, Chen T, Johnson SL, Kurachi Y, Okada N, Kondo S (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.
130. Jaffe LF (1966). Electrical currents through the developing fucus egg. Proc Natl Acad Sci USA 56, 1102-1109.
131. Jaffe LF (1968). Localization in the developing Fucus egg and the general role of localizing currents. Adv Morphog 7, 295-328.
132. Jaffe L (1982). Developmental currents, voltages, and gradients. In: Developmental Order: its origin and regulation, ed. S Subtelny, New York: Alan R. Liss, 183-215.
133. Jaffe LF, Nuccitelli R (1977). Electrical controls of development. Annu Rev Biophys Bioeng 6, 445-476.
134. Jaffe LF, Poo MM (1979). Neurites grow faster towards the cathode than the anode in a steady field. J Exp Zool 209, 115-128.
135. Jia X, Yang J, Song W, Li P, Wang X, Guan C, Yang L, Huang Y, Gong X, Liu M, et al. (2013). Involvement of large conductance Ca(2+)-activated K (+) channel in laminar shear stress-induced inhibition of vascular smooth muscle cell proliferation. Pflugers Arch 465, 221-232.
136. Jiang P, Rushing S, Kong CW, Fu J, Lieu DK, Chan C, Deng W, Li R (2009). Electrophysiological properties of human induced pluripotent stem cells. Am J Physiol Cell Physiol 298, C486-C495.
137. Justet C, Evans F, Vasilskis E, Hernandez JA, Chifflet S (2013). ENaC contribution to epithelial wound healing is independent of the healing mode and of any increased expression in the channel. Cell Tissue Res 353, 53-64.
138. Kawakami Y, Raya A, Raya RM, Rodriguez-Esteban C, Belmonte JC (2005). Retinoic acid signalling links left-right asymmetric patterning and bilaterally symmetric somitogenesis in the zebrafish embryo. Nature 435, 165-171.
139. Knopfel T, Lin MZ, Levskaya A, Tian L, Lin JY, Boyden ES (2010). Toward the second generation of optogenetic tools. J Neurosci 30, 14998-15004.
140. Konig S, Beguet A, Bader CR, Bernheim L (2006). The calcineurin pathway links hyperpolarization (Kir2.1)-induced Ca2+ signals to human myoblast differentiation and fusion. Development 133, 3107-3114.
141. Kujawski S, Lin W, Kitte F, Bormel M, Fuchs S, Arulmozhivarman G, Vogt S, Theil D, Zhang Y, Antos CL (2014). Calcineurin regulates coordinated outgrowth of zebrafish regenerating fins. Dev Cell 28, 573-587.
142. Kumai M, Nishii K, Nakamura K, Takeda N, Suzuki M, Shibata Y (2000). Loss of connexin45 causes a cushion defect in early cardiogenesis. Development 127, 3501-3512.
143. Kurtz I, Schrank AR (1955). Bioelectrical properties of intact and regenerating earthworms Eisenia foetida. Physiol Zool 28, 322-330.
144. Lallet-Daher H, Wiel C, Gitenay D, Navaratnam N, Augert A, Le Calve B, Verbeke S, Carling D, Aubert S, Vindrieux D, et al. (2013). Potassium channel KCNA1 modulates oncogene-induced senescence and transformation. Cancer Res 73, 5253-5265.
145. Lan J-Y, Williams C, Levin M, Black LDIII (2014). Depolarization of cellular resting membrane potential promotes neonatal cardiomyocyte proliferation in vitro. Cell Mol Bioeng 7, 1-14.
146. Lang F, Foller M, Lang KS, Lang PA, Ritter M, Gulbins E, Vereninov A, Huber SM (2005). Ion channels in cell proliferation and apoptotic cell death. J Membr Biol 205, 147-157.
147. Lang F, Stournaras C (2014). Ion channels in cancer: future perspectives and clinical potential. Philos Trans R Soc Lond B Biol Sci 369, 20130108.
148. Lange C, Prenninger S, Knuckles P, Taylor V, Levin M, Calegari F (2011). The H(+) vacuolar ATPase maintains neural stem cells in the developing mouse cortex. Stem Cells Dev 20, 843-850.
149. Langlois VS, Martyniuk CJ (2013). Genome wide analysis of Silurana (Xenopus) tropicalis development reveals dynamic expression using network enrichment analysis. Mech Dev 130, 304-322.
150. Lauritzen I, Zanzouri M, Honore E, Duprat F, Ehrengruber MU, Lazdunski M, Patel AJ (2003). K+-dependent cerebellar granule neuron apoptosis. Role of task leak K +channels. J Biol Chem 278, 32068-32076.
151. Lechleiter J, Girard S, Peralta E, Clapham D (1991). Spiral calcium wave propagation and annihilation in Xenopus laevis oocytes. Science 252, 123-126.
152. Lee MP, Hu RJ, Johnson LA, Feinberg AP (1997). Human KVLQT1 gene shows tissue-specific imprinting and encompasses Beckwith-Wiedemann syndrome chromosomal rearrangements. Nat Genet 15, 181-185.
153. 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.
154. Levin M (2007). Large-scale biophysics: ion flows and regeneration. Trends Cell Biol 17, 262-271.
155. Levin M (2012a). Molecular bioelectricity in developmental biology: new tools and recent discoveries: control of cell behavior and pattern formation by transmembrane potential gradients. BioEssays 34, 205-217.
156. Levin M (2012b). Morphogenetic fields in embryogenesis, regeneration, and cancer: non-local control of complex patterning. Bio Systems 109, 243-261.
157. Levin M (2013). Reprogramming cells and tissue patterning via bioelectrical pathways: molecular mechanisms and biomedical opportunities. Wiley Interdiscip Rev Syst Biol Med 5, 657-676.
158. Levin M (2014). Endogenous bioelectrical networks store non-genetic patterning information during development and regeneration. J Physiol 592, 2295-2305.
159. Levin M, Buznikov GA, Lauder JM (2006). Of minds and embryos: left-right asymmetry and the serotonergic controls of pre-neural morphogenesis. Dev Neurosci 28, 171-185.
160. Levin M, Palmer AR (2007). Left-right patterning from the inside out: widespread evidence for intracellular control. Bioessays 29, 271-287.
161. Levin M, Stevenson CG (2012). Regulation of cell behavior and tissue patterning by bioelectrical signals: challenges and opportunities for biomedical engineering. Annu Rev Biomed Eng 14, 295-323.
162. Levin M, Thorlin T, Robinson KR, Nogi T, Mercola M (2002). Asymmetries in H+/K+-ATPase and cell membrane potentials comprise a very early step in left-right patterning. Cell 111, 77-89.
163. Li F, Yin J, Yue T, Liu L, Zhang H (2010). The chloride intracellular channel 5 (CLIC5) involved in C2C12 myoblasts proliferation and differentiation. Cell Biol Int 34, 379-384.
164. Liebau S, Propper C, Bockers T, Lehmann-Horn F, Storch A, Grissmer S, Wittekindt OH (2006). Selective blockage of Kv1.3 and Kv3.1 channels increases neural progenitor cell proliferation. J Neurochem 99, 426-437.
165. Liebau S, Tischendorf M, Ansorge D, Linta L, Stockmann M, Weidgang C, Iacovino M, Boeckers T, von Wichert G, Kyba M, et al. (2011). An inducible expression system of the calcium-activated potassium channel 4 to study the differential impact on embryonic stem cells. Stem Cells Int 2011 456815.
166. Liesi P, Stewart RR, Wright JM (2000). Involvement of GIRK2 in postnatal development of the weaver cerebellum. J Neurosci Res 60, 164-173.
167. Liu X, Tonegawa S (2010). Optogenetics 3.0. Cell 141, 22-24.
168. Lobikin M, Chernet B, Lobo D, Levin M (2012a). Resting potential, oncogene-induced tumorigenesis, and metastasis: the bioelectric basis of cancer in vivo. Phys Biol 9, 065002.
169. Lobikin M, Wang G, Xu J, Hsieh YW, Chuang CF, Lemire JM, Levin M (2012b). Early, nonciliary role for microtubule proteins in left-right patterning is conserved across kingdoms. Proc Natl Acad Sci USA 109, 12586-12591.
170. Lobo D, Beane WS, Levin M (2012). Modeling planarian regeneration: a primer for reverse-engineering the worm. PLoS Comput Biol 8, e1002481.
171. Lotvall J, Valadi H (2007). Cell to cell signalling via exosomes through esRNA. Cell Adh Migr 1, 156-158.
172. Lund E (1947). Bioelectric Fields and Growth, Austin: University of Texas Press.
173. MacFarlane SN, Sontheimer H (2000). Changes in ion channel expression accompany cell cycle progression of spinal cord astrocytes. Glia 30, 39-48.
174. Marder E (2009). Electrical synapses: rectification demystified. Curr Biol 19, R34-35.
175. Marsh G, Beams HW (1947). Electrical control of growth polarity in regenerating Dugesia-Tigrina. Fed Proc 6, 163-164.
176. Marsh G, Beams HW (1949). Electrical control of axial polarity in a regenerating annelid. Anat Rec 105, 513-514.
177. Marsh G, Beams HW (1950). Electrical control of growth axis in a regenerating annelid. Anat Rec 108, 512.
178. Marsh G, Beams HW (1952). Electrical control of morphogenesis in regenerating Dugesia Tigrina.1. Relation of axial polarity to field strength. J Cell Comp Physiol 39, 191.
179. Marsh G, Beams H (1957). Electrical control of morphogenesis in regenerating Dugesia tigrina. J Cell Comp Physiol 39, 191-211.
180. Marshall WF (2011). Origins of cellular geometry. BMC Biol 9, 57.
181. Martino JJ, Wall BA, Mastrantoni E, Wilimczyk BJ, La Cava SN, Degenhardt K, White E, Chen S (2013). Metabotropic glutamate receptor 1 (Grm1) is an oncogene in epithelial cells. Oncogene 32, 4366-4376.
182. Mazzanti M, Bustamante JO, Oberleithner H (2001). Electrical dimension of the nuclear envelope. Physiol Rev 81, 1-19.
183. McCaig CD, Rajnicek AM, Song B, Zhao M (2005). Controlling cell behavior electrically: current views and future potential. Physiol Rev 85, 943-978.
184. Mello de Queiroz F, Ponte CG, Bonomo A, Vianna-Jorge R, Suarez-Kurtz G (2008). Study of membrane potential in T lymphocytes subpopulations using flow cytometry. BMC Immunol 9, 63.
185. 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, 1609-1622.
186. Miki T, Iwanaga T, Nagashima K, Ihara Y, Seino S (2001). Roles of ATP-sensitive K +channels in cell survival and differentiation in the endocrine pancreas. Diabetes 50(Suppl 1), S48-S51.
187. Minc N, Chang F (2010). Electrical control of cell polarization in the fission yeast Schizosaccharomyces pombe. Curr Biol 20, 710-716.
188. Monteiro J, Aires R, Becker JD, Jacinto A, Certal AC, Rodriguez-Leon J (2014). V-ATPase proton pumping activity is required for adult zebrafish appendage regeneration. PLoS One 9, e92594.
189. Morokuma J, Blackiston D, Adams DS, Seebohm G, Trimmer B, Levin M (2008a). Modulation of potassium channel function confers a hyperproliferative invasive phenotype on embryonic stem cells. Proc Natl Acad Sci USA 105, 16608-16613.
190. Morokuma J, Blackiston D, Levin M (2008b). KCNQ1 and KCNE1 K+ channel components are involved in early left-right patterning in Xenopus laevis embryos. Cell Physiol Biochem 21, 357-372.
191. Muller C, Maeso I, Wittbrodt J, Martinez-Morales JR (2013). The medaka mutation tintachina sheds light on the evolution of V-ATPase B subunits in vertebrates. Sci Rep 3, 3217.
192. Muller P, Rogers KW, Jordan BM, Lee JS, Robson D, Ramanathan S, Schier AF (2012). Differential diffusivity of Nodal and Lefty underlies a reaction-diffusion patterning system. Science 336, 721-724.
193. Murata Y, Iwasaki H, Sasaki M, Inaba K, Okamura Y (2005). Phosphoinositide phosphatase activity coupled to an intrinsic voltage sensor. Nature 435,1239-1243.
194. Mutoh H, Perron A, Akemann W, Iwamoto Y, Knopfel T (2011). Optogenetic monitoring of membrane potentials. Exp Physiol 96, 13-18.
195. Nakanishi S, Okazawa M (2006). Membrane potential-regulated Ca2+ signalling in development and maturation of mammalian cerebellar granule cells. J Physiol 575, 389-395.
196. Nelson CM (2009). Geometric control of tissue morphogenesis. Biochim Biophys Acta 1793, 903-910.
197. Ng SY, Chin CH, Lau YT, Luo J, Wong CK, Bian ZX, Tsang SY (2010). Role of voltage-gated potassium channels in the fate determination of embryonic stem cells. J Cell Physiol 224, 165-177.
198. Niehrs C (2010). On growth and form: a Cartesian coordinate system of Wnt and BMP signaling specifies bilaterian body axes. Development 137, 845-857.
199. Nilius B, Schwarz G, Droogmans G (1993). Control of intracellular calcium by membrane potential in human melanoma cells. Am J Physiol 265, C1501-1510.
200. Nishii K, Kumai M, Shibata Y (2001). Regulation of the epithelial-mesenchymal transformation through gap junction channels in heart development. Trends Cardiovasc Med 11, 213-218.
201. Nishimoto S, Vu AT, Naselaris T, Benjamini Y, Yu B, Gallant JL (2011). Reconstructing visual experiences from brain activity evoked by natural movies. Curr Biol 21, 1641-1646.
202. Nishiyama M, von Schimmelmann MJ, Togashi K, Findley WM, Hong K (2008). Membrane potential shifts caused by diffusible guidance signals direct growth-cone turning. Nat Neurosci 11, 762-771.
203. Nogi T, Levin M (2005). Characterization of innexin gene expression and functional roles of gap-junctional communication in planarian regeneration. Dev Biol 287, 314-335.
204. Nogi T, Zhang D, Chan JD, Marchant JS (2009). A novel biological activity of praziquantel requiring voltage-operated ca channel Beta subunits: subversion of flatworm regenerative polarity. PLoS Negl Trop Dis 3, e464.
205. Novák B, Bentrup FW (1972). An electrophysiological study of regeneration in Acetabularia mediterranea. Planta 108, 227-244.
206. Novak B, Sirnoval C (1975). Inhibition of regeneration of Acetabularia mediterranea enucleated posterior stalk segments by electrical isolation. Plant Sci Lett 5, 183-188.
207. Nuccitelli R, Robinson K, Jaffe L (1986). On electrical currents in development. Bioessays 5, 292-294.
208. Nuckels RJ, Ng A, Darland T, Gross JM (2009). The vacuolar-ATPase complex regulates retinoblast proliferation and survival, photoreceptor morphogenesis, and pigmentation in the zebrafish eye. Invest Ophthalmol Vis Sci 50, 893-905.
209. 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, 9609-9618.
210. O'Connell KM, Tamkun MM (2005). Targeting of voltage-gated potassium channel isoforms to distinct cell surface microdomains. J Cell Sci 118, 2155-2166.
211. Okamura Y, Dixon JE (2011). Voltage-sensing phosphatase: its molecular relationship with PTEN. Physiology (Bethesda) 26, 6-13.
212. Olivotto M, Arcangeli A, Carla M, Wanke E (1996). Electric fields at the plasma membrane level: a neglected element in the mechanisms of cell signalling. Bioessays 18, 495-504.
213. O'Neill JS, Reddy AB (2011). Circadian clocks in human red blood cells. Nature 469, 498-503.
214. 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, 206-219.
215. Oviedo NJ, Morokuma J, Walentek P, Kema IP, Gu MB, Ahn JM, Hwang JS, Gojobori T, Levin M (2010). Long-range neural and gap junction protein-mediated cues control polarity during planarian regeneration. Dev Biol 339, 188-199.
216. Oviedo NJ, Nicolas CL, Adams DS, Levin M (2008). Live imaging of planarian membrane potential using DiBAC4(3). CSH Protoc 2008, pdb prot5055.
217. Ozkucur N, Epperlein HH, Funk RH (2010). Ion imaging during axolotl tail regeneration in vivo. Dev Dyn 239, 2048-2057.
218. 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.
219. 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.
220. Palacios-Prado N, Bukauskas FF (2009). Heterotypic gap junction channels as voltage-sensitive valves for intercellular signaling. Proc Natl Acad Sci USA 106, 14855-14860.
221. Pan L, Borgens RB (2010). Perpendicular organization of sympathetic neurons within a required physiological voltage. Exp Neurol 222, 161-164.
222. Pan L, Borgens RB (2012). Strict perpendicular orientation of neural crest-derived neurons in vitro is dependent on an extracellular gradient of voltage. J Neurosci Res 90, 1335-1346.
223. Park JY, Helm JF, Zheng W, Ly QP, Hodul PJ, Centeno BA, Malafa MP (2008). Silencing of the candidate tumor suppressor gene solute carrier family 5 member 8 (SLC5A8) in human pancreatic cancer. Pancreas 36, e32-39.
224. Patel N, Poo MM (1982). Orientation of neurite growth by extracellular electric fields. J Neurosci 2, 483-496.
225. Patil N, Cox DR, Bhat D, Faham M, Myers RM, Peterson AS (1995). A potassium channel mutation in weaver mice implicates membrane excitability in granule cell differentiation. Nat Genet 11, 126-129.
226. Paul SM, Palladino MJ, Beitel GJ (2007). A pump-independent function of the Na,K-ATPase is required for epithelial junction function and tracheal tube-size control. Development 134, 147-155.
227. Pei L, Wiser O, Slavin A, Mu D, Powers S, Jan LY, Hoey T (2003). Oncogenic potential of TASK3 (Kcnk9) depends on K+ channel function. Proc Natl Acad Sci USA 100, 7803-7807.
228. Perathoner S, Daane JM, Henrion U, Seebohm G, Higdon CW, Johnson SL, Nusslein-Volhard C, Harris MP (2014). Bioelectric signaling regulates size in zebrafish fins. PLoS Genet 10, e1004080.
229. Pereda AE, Curti S, Hoge G, Cachope R, Flores CE, Rash JE (2013). Gap junction-mediated electrical transmission: regulatory mechanisms and plasticity. Biochim Biophys Acta 1828, 134-146.
230. Pillozzi S, Brizzi MF, Balzi M, Crociani O, Cherubini A, Guasti L, Bartolozzi B, Becchetti A, Wanke E (2002). HERG potassium channels are constitutively expressed in primary human acute myeloid leukemias and regulate cell proliferation of normal and leukemic hemopoietic progenitors. Leukemia 16, 1791-1798.
231. Pizzuti A, Flex E, Mingarelli R, Salpietro C, Zelante L, Dallapiccola B (2004). A homozygous GJA1 gene mutation causes a Hallermann-Streiff/ODDD spectrum phenotype. Hum Mutat 23, 286.
232. Podda MV, Piacentini R, Barbati SA, Mastrodonato A, Puzzo D, D'Ascenzo M, Leone L, Grassi C (2013). Role of cyclic nucleotide-gated channels in the modulation of mouse hippocampal neurogenesis. PLoS One 8, e73246.
233. Priel A, Ramos AJ, Tuszynski JA, Cantiello HF (2006). A biopolymer transistor: electrical amplification by microtubules. Biophys J 90, 4639-4643.
234. Pullar CE (2011). The Physiology of Bioelectricity in Development, Tissue Regeneration, and Cancer, Boca Raton, FL: CRC Press.
235. Pullar CE, Isseroff RR (2005). Cyclic AMP mediates keratinocyte directional migration in an electric field. J Cell Sci 118, 2023-2034.
236. Rakic P, Sidman RL (1973a). Sequence of developmental abnormalities leading to granule cell deficit in cerebellar cortex of weaver mutant mice. J Comp Neurol 152, 103-132.
237. Rakic P, Sidman RL (1973b). Weaver mutant mouse cerebellum: defective neuronal migration secondary to abnormality of Bergmann glia. Proc Natl Acad Sci USA 70, 240-244.
238. Raya A, Kawakami Y, Rodriguez-Esteban C, Ibanes M, Rasskin-Gutman D, Rodriguez-Leon J, Buscher D, Feijo JA, Izpisua Belmonte JC (2004). Notch activity acts as a sensor for extracellular calcium during vertebrate left-right determination. Nature 427, 121-128.
239. Reaume AG, De Sousa PA, Kilkarni S, Langille BL, Zhu D, Davies TC, Juneja SC, Kidder GM, Rossant J (1995). Cardiac malformation in neonatal mice lacking connexin43. Science 267, 1831-1834.
240. Reddien PW, Sanchez Alvarado A (2004). Fundamentals of planarian regeneration. Annu Rev Cell Dev Biol 20, 725-757.
241. Reid B, Graue-Hernandez EO, Mannis MJ, Zhao M (2011a). Modulating endogenous electric currents in human corneal wounds - a novel approach of bioelectric stimulation without electrodes. Cornea 30, 338-343.
242. Reid B, Nuccitelli R, Zhao M (2007). Non-invasive measurement of bioelectric currents with a vibrating probe. Nat Protoc 2, 661-669.
243. Reid B, Vieira AC, Cao L, Mannis MJ, Schwab IR, Zhao M (2011b). Specific ion fluxes generate cornea wound electric currents. Commun Integr Biol 4, 462-465.
244. Rigas S, Debrosses G, Haralampidis K, Vicente-Agullo F, Feldmann KA, Grabov A, Dolan L, Hatzopoulos P (2001). TRH1 encodes a potassium transporter required for tip growth in Arabidopsis root hairs. Plant Cell 13, 139-151.
245. Ring H, Mendu SK, Shirazi-Fard S, Birnir B, Hallbook F (2012). GABA maintains the proliferation of progenitors in the developing chick ciliary marginal zone and non-pigmented ciliary epithelium. PLoS One 7, e36874.
246. Rivas A, Francis HW (2005). Inner ear abnormalities in a Kcnq1 (Kvlqt1) knockout mouse: a model of Jervell and Lange-Nielsen syndrome. Otol Neurotol 26, 415-424.
247. Rock JR, Futtner CR, Harfe BD (2008). The transmembrane protein TMEM16A is required for normal development of the murine trachea. Dev Biol 321, 141-149.
248. Roepke TK, Purtell K, King EC, La Perle KM, Lerner DJ, Abbott GW (2010). Targeted deletion of Kcne2 causes gastritis cystica profunda and gastric neoplasia. PLoS One 5, e11451.
249. Root CM, Velazquez-Ulloa NA, Monsalve GC, Minakova E, Spitzer NC (2008). Embryonically expressed GABA and glutamate drive electrical activity regulating neurotransmitter specification. J Neurosci 28, 4777-4784.
250. Rouzaire-Dubois B, Gerard V, Dubois JM (1993). Involvement of K+ channels in the quercetin-induced inhibition of neuroblastoma cell growth. Pflugers Arch 423, 202-205.
251. Rubenstein M, Sai Y, Chuong CM, Shen WM (2009). Regenerative patterning in Swarm Robots: mutual benefits of research in robotics and stem cell biology. Int J Dev Biol 53, 869-881.
252. Saito T, Schlegel R, Andresson T, Yuge L, Yamamoto M, Yamasaki H (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 NIH3T3 cells. Oncogene 17, 1673-1680.
253. Salo E, Abril JF, Adell T, Cebria F, Eckelt K, Fernandez-Taboada E, Handberg-Thorsager M, Iglesias M, Molina MD, Rodriguez-Esteban G (2009). Planarian regeneration: achievements and future directions after 20 years of research. Int J Dev Biol 53, 1317-1327.
254. Savy C, Martin-Martinelli E, Simon A, Duyckaerts C, Verney C, Adelbrecht C, Raisman-Vozari R, Nguyen-Legros J (1999). Altered development of dopaminergic cells in the retina of weaver mice. J Comp Neurol 412, 656-668.
255. Scemes E, Suadicani SO, Dahl G, Spray DC (2007). Connexin and pannexin mediated cell-cell communication. Neuron Glia Biol 3, 199-208.
256. Schiffmann Y (1991). An hypothesis: phosphorylation fields as the source of positional information and cell differentiation-(cAMP, ATP) as the universal morphogenetic Turing couple. Prog Biophys Mol Biol 56, 79-105.
257. Schiffmann Y (1997). Self-organization in biology and development. Prog Biophys Mol Biol 68, 145-205.
258. Schonecker S, Kraushaar U, Dufer M, Sahr A, Hardtner C, Guenther E, Walther R, Lendeckel U, Barthlen W, Krippeit-Drews P, et al. (2014). Long-term culture and functionality of pancreatic islets monitored using microelectrode arrays. Integr Biol (Camb) 6, 540-544.
259. Schwab A (2001). Function and spatial distribution of ion channels and transporters in cell migration. Am J Physiol Renal Physiol 280, F739-747.
260. Schwab A, Gabriel K, Finsterwalder F, Folprecht G, Greger R, Kramer A, Oberleithner H (1995). Polarized ion transport during migration of transformed Madin-Darby canine kidney cells. Pflugers Arch 430, 802-807.
261. Sekulic DL, Sataric BM, Tuszynski JA, Sataric MV (2011). Nonlinear ionic pulses along microtubules. Eur Phys J E Soft Matter 34, 1-11.
262. Sharmeen S, Skrtic M, Sukhai MA, Hurren R, Gronda M, Wang X, Fonseca SB, Sun H, Wood TE, Ward R, et al. (2010). The antiparasitic agent ivermectin induces chloride-dependent membrane hyperpolarization and cell death in leukemia cells. Blood 116, 3593-3603.
263. Shen JX, Qin D, Wang H, Wu C, Shi FD, Wu J (2013). Roles of nicotinic acetylcholine receptors in stem cell survival/apoptosis, proliferation and differentiation. Curr Mol Med 13, 1455-1464.
264. Shen B, Xiang Z, Miller B, Louie G, Wang W, Noel JP, Gage FH, Wang L (2011). Genetically encoding unnatural amino acids in neural stem cells and optically reporting voltage-sensitive domain changes in differentiated neurons. Stem Cells 9, 1231-1240.
265. Sheth R, Marcon L, Bastida MF, Junco M, Quintana L, Dahn R, Kmita M, Sharpe J, Ros MA (2012). Hox genes regulate digit patterning by controlling the wavelength of a Turing-type mechanism. Science 338, 1476-1480.
266. 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.
267. Shu X, Cheng K, Patel N, Chen F, Joseph E, Tsai HJ, Chen JN (2003). Na,KATPase is essential for embryonic heart development in the zebrafish. Development 130, 6165-6173.
268. Simons M, Gault WJ, Gotthardt D, Rohatgi R, Klein TJ, Shao Y, Lee HJ, Wu AL, Fang Y, Satlin LM, et al. (2009). Electrochemical cues regulate assembly of the Frizzled/Dishevelled complex at the plasma membrane during planar epithelial polarization. Nat Cell Biol 11, 286-294.
269. Sims K Jr, Eble DM, Iovine MK (2009). Connexin43 regulates joint location in zebrafish fins. Dev Biol 327, 410-418.
270. Sinha G (2013). Charged by GSK investment, battery of electroceuticals advance. Nat Med 19, 654.
271. Sirnes S, Bruun J, Kolberg M, Kjenseth A, Lind GE, Svindland A, Brech A, Nesbakken A, Lothe RA, Leithe E, et al. (2012). Connexin43 acts as a colorectal cancer tumor suppressor and predicts disease outcome. Int J Cancer. 131, 570-581.
272. 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: Methods and New Frontiers in Neuroscience, ed. AC Michael, Boca Raton, FL: CRC Press, 373-405.
273. Song B, Gu Y, Pu J, Reid B, Zhao Z, Zhao M (2007). Application of direct current electric fields to cells and tissues in vitro and modulation of wound electric field in vivo. Nat Protoc 2, 1479-1489.
274. Song Z, He CD, Liu J, Sun C, Lu P, Li L, Gao L, Zhang Y, Xu Y, Shan L, et al. (2012). Blocking glutamate-mediated signalling inhibits human melanoma growth and migration. Exp Dermatol 21, 926-931.
275. Speyer CL, Smith JS, Banda M, DeVries JA, Mekani T, Gorski DH (2012). Metabotropic glutamate receptor-1: a potential therapeutic target for the treatment of breast cancer. Breast Cancer Res Treat 132, 565-573.
276. Steinberg BE, Touret N, Vargas-Caballero M, Grinstein S (2007). In situ measurement of the electrical potential across the phagosomal membrane using FRET and its contribution to the proton-motive force. Proc Natl Acad Sci USA 104, 9523-9528.
277. Stern C (1982). Experimental reversal of polarity in chick embryo epiblast sheets in vitro. Exp Cell Res 140, 468-471.
278. Stillwell EF, Cone CM, Cone CD (1973). Stimulation of DNA synthesis in CNS neurones by sustained depolarisation. Nat New Biol 246, 110-111.
279. Stroh A, Tsai HC, Ping Wang L, Zhang F, Kressel J, Aravanis A, Santhanam N, Deisseroth K, Konnerth A, Schneider MB (2010). Tracking stem cell differentiation in the setting of automated optogenetic stimulation. Stem Cells 29, 78-88.
280. Stuhmer W, Alves F, Hartung F, Zientkowska M, Pardo LA (2006). Potassium channels as tumour markers. FEBS Lett 580, 2850-2852.
281. Stump RF, Robinson KR (1983). Xenopus neural crest cell migration in an applied electrical field. J Cell Biol 97, 1226-1233.
282. Sun Y, Dong Z, Jin T, Ang KH, Huang M, Haston KM, Peng J, Zhong TP, Finkbeiner S, Weiss WA, et al. (2013). Imaging-based chemical screening reveals activity-dependent neural differentiation of pluripotent stem cells. Elife 2, e00508.
283. Sun Y, Wang C, Dai J (2010). Biophotons as neural communication signals demonstrated by in situ biophoton autography. Photochem Photobiol Sci 9, 315-322.
284. Sundelacruz S, Levin M, Kaplan DL (2008). Membrane potential controls adipogenic and osteogenic differentiation of mesenchymal stem cells. PLoS One 3, e3737.
285. Sundelacruz S, Levin M, Kaplan DL (2013). Depolarization alters phenotype, maintains plasticity of predifferentiated mesenchymal stem cells. Tiss Eng. Part A 19, 1889-1908.
286. Sutor B, Hagerty T (2005). Involvement of gap junctions in the development of the neocortex. Biochim Biophys Acta 1719, 59-68.
287. Swapna I, Borodinsky LN (2012). Interplay between electrical activity and bone morphogenetic protein signaling regulates spinal neuron differentiation. Proc Natl Acad Sci USA 109, 4016336-16341.
288. Takagi H, Kaneko K (2005). Dynamical systems basis of metamorphosis: diversity and plasticity of cellular states in reaction diffusion network. J Theor Biol 234, 173-186.
289. 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, 10034-10037.
290. Teng GQ, Zhao X, Lees-Miller JP, Quinn FR, Li P, Rancourt DE, London B, Cross JC, Duff HJ (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, 1483-1491.
291. Than BL, Goos JA, Sarver AL, O'Sullivan MG, Rod A, Starr TK, Fijneman RJ, Meijer GA, Zhao L, Zhang Y, et al. (2013). The role of KCNQ1 in mouse and human gastrointestinal cancers. Oncogene 33, 3861-3868.
292. Toko K, Iiyama S, Tanaka C, Hayashi K, Yamafuji K (1987). Relation of growth process to spatial patterns of electric potential and enzyme activity in bean roots. Biophys Chem 27, 39-58.
293. Tong Y, Wei J, Zhang S, Strong JA, Dlouhy SR, Hodes ME, Ghetti B, Yu L (1996). The weaver mutation changes the ion selectivity of the affected inwardly rectifying potassium channel GIRK2. FEBS Lett 390, 63-68.
294. Tong X, Yin L, Giardina C (2004). Butyrate suppresses Cox-2 activation in colon cancer cells through HDAC inhibition. Biochem Biophys Res Commun 317, 463-471.
295. Tseng AS, Beane WS, Lemire JM, Masi A, Levin M (2010). Induction of vertebrate regeneration by a transient sodium current. J Neurosci 30, 13192-13200.
296. Tseng AS, Carneiro K, Lemire JM, Levin M (2011). HDAC activity is required during Xenopus tail regeneration. PLoS One 6, e26382.
297. Tseng A, Levin M (2013). Cracking the bioelectric code: Probing endogenous ionic controls of pattern formation. Commun Integr Biol 6, 1-8.
298. Tsutsui H, Karasawa S, Okamura Y, Miyawaki A (2008). Improving membrane voltage measurements using FRET with new fluorescent proteins. Nat Methods 5, 683-685.
299. Tyner KM, Kopelman R, Philbert MA (2007). "Nanosized voltmeter" enables cellular-wide electric field mapping. Biophys J 93, 1163-1174.
300. Uzman JA, Patil S, Uzgare AR, Sater AK (1998). The role of intracellular alkalinization in the establishment of anterior neural fate in Xenopus. Dev Biol 193, 10-20.
301. Uzun S, Gokce S, Wagner K (2005). Cystic fibrosis transmembrane conductance regulator gene mutations in infertile males with congenital bilateral absence of the vas deferens. Tohoku J Exp Med 207, 279-285.
302. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO (2007). Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9, 654-659.
303. Vandenberg LN, Lemire JM, Levin M (2012). Serotonin has early, cilia-independent roles in Xenopus left-right patterning. Dis Models Mech 6, 261-268.
304. 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.
305. Vandenberg LN, Morrie RD, Seebohm G, Lemire JM, Levin M (2013). Rab GTPases are required for early orientation of the left-right axis in Xenopus. Mech Dev 130, 254-271.
306. van Vliet P, de Boer TP, van der Heyden MA, El Tamer MK, Sluijter JP, Doevendans PA, Goumans MJ (2010). Hyperpolarization induces differentiation in human cardiomyocyte progenitor cells. Stem Cell Rev 6, 178-185.
307. Veale EL, Hassan M, Walsh Y, Al-Moubarak E, Mathie A (2014). Recovery of current through mutated TASK3 potassium channels underlying Birk Barel syndrome. Mol Pharmacol 85, 397-407.
308. Vieira AC, Reid B, Cao L, Mannis MJ, Schwab IR, Zhao M (2011). Ionic components of electric current at rat corneal wounds. PLoS One 6, e17411.
309. Volta A (1800). On the electricity excited by the mere contact of conducting substances of different kinds. Abstracts Philos Trans R Soc Lond 1, 27-29.
310. von Dassow M, Davidson LA (2011). Physics and the canalization of morphogenesis: a grand challenge in organismal biology. Phys Biol 8, 045002.
311. Wahlgren J, De LKT, Brisslert M, Vaziri Sani F, Telemo E, Sunnerhagen P, Valadi H (2012). Plasma exosomes can deliver exogenous short interfering RNA to monocytes and lymphocytes. Nucleic Acids Res 40, e130.
312. Wang L, Zhou P, Craig RW, Lu L (1999). Protection from cell death by mcl-1 is mediated by membrane hyperpolarization induced by K(+) channel activation. J Membr Biol 172, 113-120.
313. Wang SJ, Weng CH, Xu HW, Zhao CJ, Yin ZQ (2014). Effect of optogenetic stimulus on the proliferation and cell cycle progression of neural stem cells. J Membr Biol 247, 493-500.
314. Wang Z (2004). Roles of K +channels in regulating tumour cell proliferation and apoptosis. Pflugers Arch 448, 274-286.
315. Watanabe M, Iwashita M, Ishii M, Kurachi Y, Kawakami A, Kondo S, Okada N (2006). Spot pattern of leopard Danio is caused by mutation in the zebrafish connexin41.8 gene. EMBO Rep 7, 893-897.
316. Wee EL, Zimmerman EF (1985). GABA uptake in embryonic palate mesenchymal cells of two mouse strains. Neurochem Res 10, 1673-1688.
317. Weksberg R, Nishikawa J, Caluseriu O, Fei YL, Shuman C, Wei C, Steele L, Cameron J, Smith A, Ambus I, et al. (2001). Tumor development in the Beckwith-Wiedemann syndrome is associated with a variety of constitutional molecular 11p15 alterations including imprinting defects of KCNQ1OT1. Hum Mol Genet 10, 2989-3000.
318. Wilschanski M, Dupuis A, Ellis L, Jarvi K, Zielenski J, Tullis E, Martin S, Corey M, Tsui LC, Durie P (2006). Mutations in the cystic fibrosis transmembrane regulator gene and in vivo transepithelial potentials. Am J Respir Crit Care Med 174, 787-794.
319. Wittig D, Wang X, Walter C, Gerdes HH, Funk RH, Roehlecke C (2012). Multi-level communication of human retinal pigment epithelial cells via tunneling nanotubes. PLoS One 7, e33195.
320. Wonderlin WF, Strobl JS (1996). Potassium channels, proliferation and G1 progression. J Membr Biol 154, 91-107.
321. Woodruff RI (2005). Calmodulin transit via gap junctions is reduced in the absence of an electric field. J Insect Physiol 51, 843-852.
322. Xie C, Jiang XH, Zhang JT, Sun TT, Dong JD, Sanders AJ, Diao RY, Wang Y, Fok KL, Tsang LL, et al. (2013). CFTR suppresses tumor progression through miR-193b targeting urokinase plasminogen activator (uPA) in prostate cancer. Oncogene 32, e1-72282-2291, 2291.
323. Yamashita M (2011). Fluctuations in nuclear envelope's potential mediate synchronization of early neural activity. Biochem Biophys Res Commun 406, 107-111.
324. Yamashita M (2013). Electric axon guidance in embryonic retina: galvanotropism revisited. Biochem Biophys Res Commun 431, 280-283.
325. Yan X, Han J, Zhang Z, Wang J, Cheng Q, Gao K, Ni Y, Wang Y (2009). Lung cancer A549 cells migrate directionally in DC electric fields with polarized and activated EGFRs. Bioelectromagnetics 30, 29-35.
326. Yang M, Brackenbury WJ (2013). Membrane potential and cancer progression. Front Physiol 4, 185.
327. Yasuda T, Adams DJ (2010). Physiological roles of ion channels in adult neural stem cells and their progeny. J Neurochem 114, 946-959.
328. You MH, Song MS, Lee SK, Ryu PD, Lee SY, Kim DY (2012). Voltage-gated K(+) channels in adipogenic differentiation of bone marrow-derived human mesenchymal stem cells. Acta Pharmacol Sin 34, 129-136.
329. Yu K, Ruan DY, Ge SY (2002). Three electrophysiological phenotypes of cultured human umbilical vein endothelial cells. Gen Physiol Biophys 21, 315-326.
330. Yun Z, Zhengtao D, Jiachang Y, Fangqiong T, Qun W (2007). Using cadmium telluride quantum dots as a proton flux sensor and applying to detect H9 avian influenza virus. Anal Biochem 364, 122-127.
331. Zhang D, Chan JD, Nogi T, Marchant JS (2011). Opposing roles of voltagegated Ca2+ channels in neuronal control of regenerative patterning. J Neurosci 31, 15983-15995.
332. Zhang J, Chan YC, Ho JC, Siu CW, Lian Q, Tse HF (2012). Regulation of cell proliferation of human induced pluripotent stem cell-derived mesenchymal stem cells via Ether a go-go 1 (hEAG1) potassium channel. Am J Physiol Cell Physiol 303, C115-C125.
333. Zhang JT, Jiang XH, Xie C, Cheng H, Da Dong J, Wang Y, Fok KL, Zhang XH, Sun TT, Tsang LL, et al. (2013). Downregulation of CFTR promotes epithelial-to-mesenchymal transition and is associated with poor prognosis of breast cancer. Biochim Biophys Acta 1833, 2961-2969.
334. Zhao M (2009). Electrical fields in wound healing-an overriding signal that directs cell migration. Semin Cell Dev Biol 20, 674-682.
335. Zhao M, Chalmers L, Cao L, Vieira AC, Mannis M, Reid B (2012). Electrical signaling in control of ocular cell behaviors. Progr Retin Eye Res 31, 65-88.
336. Zhao M, McCaig CD, Agius-Fernandez A, Forrester JV, Araki-Sasaki K (1997). Human corneal epithelial cells reorient and migrate cathodally in a small applied electric field. Curr Eye Res 16, 973-984.
337. Zoidl G, Dermietzel R (2010). Gap junctions in inherited human disease. Pflugers Arch 460, 451-466.
338. Zykov VS (1990). Spiral waves in two-dimensional excitable media. Ann NY Acad Sci 591, 75-85.