1932

Abstract

Living systems exhibit remarkable abilities to self-assemble, regenerate, and remodel complex shapes. How cellular networks construct and repair specific anatomical outcomes is an open question at the heart of the next-generation science of bioengineering. Developmental bioelectricity is an exciting emerging discipline that exploits endogenous bioelectric signaling among many cell types to regulate pattern formation. We provide a brief overview of this field, review recent data in which bioelectricity is used to control patterning in a range of model systems, and describe the molecular tools being used to probe the role of bioelectrics in the dynamic control of complex anatomy. We suggest that quantitative strategies recently developed to infer semantic content and information processing from ionic activity in the brain might provide important clues to cracking the bioelectric code. Gaining control of the mechanisms by which large-scale shape is regulated in vivo will drive transformative advances in bioengineering, regenerative medicine, and synthetic morphology, and could be used to therapeutically address birth defects, traumatic injury, and cancer.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-bioeng-071114-040647
2017-06-21
2024-04-17
Loading full text...

Full text loading...

/deliver/fulltext/bioeng/19/1/annurev-bioeng-071114-040647.html?itemId=/content/journals/10.1146/annurev-bioeng-071114-040647&mimeType=html&fmt=ahah

Literature Cited

  1. Gentile L, Cebria F, Bartscherer K. 1.  2011. The planarian flatworm: an in vivo model for stem cell biology and nervous system regeneration. Dis. Models Mech. 4:12–19 [Google Scholar]
  2. Illingworth CM. 2.  1974. Trapped fingers and amputated finger tips in children. J. Pediatr. Surg. 9:853–58 [Google Scholar]
  3. Bubenik AB, Pavlansky R. 3.  1965. Trophic responses to trauma in growing antlers. J. Exp. Zool. 159:289–302 [Google Scholar]
  4. French V. 4.  1980. Positional information around the segments of the cockroach leg. J. Embryol. Exp. Morphol. 59:281–313 [Google Scholar]
  5. Farinella-Ferruzza N. 5.  1956. The transformation of a tail into a limb after xenoplastic transformation. Experientia 15:304–5 [Google Scholar]
  6. Vandenberg LN, Adams DS, Levin M. 6.  2012. Normalized shape and location of perturbed craniofacial structures in the Xenopus tadpole reveal an innate ability to achieve correct morphology. Dev. Dyn. 241:863–78 [Google Scholar]
  7. Mintz B, Illmensee K. 7.  1975. Normal genetically mosaic mice produced from malignant teratocarcinoma cells. PNAS 72:3585–89 [Google Scholar]
  8. Rose SM, Wallingford HM. 8.  1948. Transformation of renal tumors of frogs to normal tissues in regenerating limbs of salamanders. Science 107:457 [Google Scholar]
  9. Doursat R, Sayama H, Michel O. 9.  2013. A review of morphogenetic engineering. Nat Comput 12:517–35 [Google Scholar]
  10. Slack J. 10.  2014. Establishment of spatial pattern. Wiley Interdiscip. Rev. Dev. Biol. 3:379–88 [Google Scholar]
  11. Miller CJ, Davidson LA. 11.  2013. The interplay between cell signalling and mechanics in developmental processes. Nat. Rev. Genet. 14:733–44 [Google Scholar]
  12. Levin M. 12.  2014. Molecular bioelectricity: how endogenous voltage potentials control cell behavior and instruct pattern regulation in vivo. Mol. Biol. Cell 25:3835–50 [Google Scholar]
  13. Bates E. 13.  2015. Ion channels in development and cancer. Annu. Rev. Cell Dev. Biol. 31:231–47 [Google Scholar]
  14. Roux W. 14.  1892. Über die morphologische Polarisation von Eiern und Embryonen durch den electrischen Strom. Sitzungsber. Acad. Wiss. Wien Math. Naturwiss. 101:27–228 [Google Scholar]
  15. Hotary KB, Robinson KR. 15.  1992. Evidence of a role for endogenous electrical fields in chick embryo development. Development 114:985–96 [Google Scholar]
  16. Pullar CE. 16.  2011. The Physiology of Bioelectricity in Development, Tissue Regeneration, and Cancer Boca Raton: CRC
  17. Reid B, Zhao M. 17.  2014. The electrical response to injury: molecular mechanisms and wound healing. Adv. Wound Care 3:184–201 [Google Scholar]
  18. Adams DS. 18.  2008. A new tool for tissue engineers: ions as regulators of morphogenesis during development and regeneration. Tissue Eng 14:1461–68 [Google Scholar]
  19. Funk RH. 19.  2015. Endogenous electric fields as guiding cue for cell migration. Front. Physiol. 6:143 [Google Scholar]
  20. Levin M. 20.  2014. Endogenous bioelectrical networks store non-genetic patterning information during development and regeneration. J. Physiol. 592:2295–305 [Google Scholar]
  21. Binggeli R, Weinstein R. 21.  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 [Google Scholar]
  22. Palacios-Prado N, Bukauskas FF. 22.  2009. Heterotypic gap junction channels as voltage-sensitive valves for intercellular signaling. PNAS 106:14855–60 [Google Scholar]
  23. Mathews J, Levin M. 23.  2016. Gap junctional signaling in pattern regulation: physiological network connectivity instructs growth and form. Dev. Neurobiol. In press. https://doi.org/10.1002/dneu.22405 [Crossref]
  24. Blackiston DJ, McLaughlin KA, Levin M. 24.  2009. Bioelectric controls of cell proliferation: ion channels, membrane voltage and the cell cycle. Cell Cycle 8:3519–28 [Google Scholar]
  25. Certal AC, Almeida RB, Carvalho LM, Wong E, Moreno N. 25.  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 [Google Scholar]
  26. Aprea J, Calegari F. 26.  2012. Bioelectric state and cell cycle control of mammalian neural stem cells. Stem. Cells Int. 2012:816049 [Google Scholar]
  27. Volkov A, Waite AJ, Wooten JD, Markin VS. 27.  2012. Circadian rhythms in biologically closed electrical circuits of plants. Plant Signal. Behav. 7:282–84 [Google Scholar]
  28. Jiang P, Rushing SN, Kong CW, Fu J, Lieu DK. 28.  et al. 2010. Electrophysiological properties of human induced pluripotent stem cells. Am. J. Physiol. Cell Physiol. 298:C486–95 [Google Scholar]
  29. Sundelacruz S, Levin M, Kaplan DL. 29.  2008. Membrane potential controls adipogenic and osteogenic differentiation of mesenchymal stem cells. PLOS ONE 3:e3737 [Google Scholar]
  30. Meade JC, Li C, Moate ME, Davis-Hayman SR, Lushbaugh WB, Finley RW. 30.  1997. Molecular characterization of a sarcoplasmic-endoplasmic reticulum Ca+2 ATPase gene from Trichomonas vaginalis. . J. Eukaryot. Microbiol. 44:480–86 [Google Scholar]
  31. Greer PL, Greenberg ME. 31.  2008. From synapse to nucleus: calcium-dependent gene transcription in the control of synapse development and function. Neuron 59:846–60 [Google Scholar]
  32. Nishiyama M, von Schimmelmann MJ, Togashi K, Findley WM, Hong K. 32.  2008. Membrane potential shifts caused by diffusible guidance signals direct growth-cone turning. Nat. Neurosci. 11:762–71 [Google Scholar]
  33. Pai VP, Aw S, Shomrat T, Lemire JM, Levin M. 33.  2012. Transmembrane voltage potential controls embryonic eye patterning in Xenopus laevis. . Development 139:313–23 [Google Scholar]
  34. Beane WS, Morokuma J, Adams DS, Levin M. 34.  2011. A chemical genetics approach reveals H,K-ATPase-mediated membrane voltage is required for planarian head regeneration. Chem. Biol. 18:77–89 [Google Scholar]
  35. Zhang D, Chan JD, Nogi T, Marchant JS. 35.  2011. Opposing roles of voltage-gated Ca2+ channels in neuronal control of regenerative patterning. J. Neurosci. 31:15983–95 [Google Scholar]
  36. Fukumoto T, Kema IP, Levin M. 36.  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 [Google Scholar]
  37. Lobikin M, Chernet B, Lobo D, Levin M. 37.  2012. Resting potential, oncogene-induced tumorigenesis, and metastasis: the bioelectric basis of cancer in vivo. Phys. Biol. 9:065002 [Google Scholar]
  38. Blackiston DJ, Anderson GM, Rahman N, Bieck C, Levin M. 38.  2015. A novel method for inducing nerve growth via modulation of host resting potential: gap junction–mediated and serotonergic signaling mechanisms. Neurotherapeutics 12:170–84 [Google Scholar]
  39. Chernet BT, Levin M. 39.  2013. 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 [Google Scholar]
  40. Ganapathy V, Thangaraju M, Gopal E, Martin PM, Itagaki S. 40.  et al. 2008. Sodium-coupled monocarboxylate transporters in normal tissues and in cancer. AAPS J 10:193–99 [Google Scholar]
  41. Okamura Y, Dixon JE. 41.  2011. Voltage-sensing phosphatase: its molecular relationship with PTEN. Physiology 26:6–13 [Google Scholar]
  42. Zhou Y, Wong CO, Cho KJ, van der Hoeven D, Liang H. 42.  et al. 2015. Signal transduction. Membrane potential modulates plasma membrane phospholipid dynamics and K-ras signaling. Science 349:873–76 [Google Scholar]
  43. Wheeler DG, Cooper E. 43.  2001. Depolarization strongly induces human cytomegalovirus major immediate-early promoter/enhancer activity in neurons. J. Biol. Chem. 276:31978–85 [Google Scholar]
  44. Pai VP, Martyniuk CJ, Echeverri K, Sundelacruz S, Kaplan DL, Levin M. 44.  2016. Genome-wide analysis reveals conserved transcriptional responses downstream of resting potential change in Xenopus embryos, axolotl regeneration, and human mesenchymal cell differentiation. Regeneration 3:3–25 [Google Scholar]
  45. Zanzouri M, Lauritzen I, Duprat F, Mazzuca M, Lesage F. 45.  et al. 2006. Membrane potential–regulated transcription of the resting K+ conductance TASK-3 via the calcineurin pathway. J. Biol. Chem. 281:28910–18 [Google Scholar]
  46. Burr HS. 46.  1941. Changes in the field properties of mice with transplanted tumors. Yale J. Biol. Med. 13:783–88 [Google Scholar]
  47. Qiu C, Shivacharan RS, Zhang M, Durand DM. 47.  2015. Can neural activity propagate by endogenous electrical field?. J. Neurosci. 35:15800–11 [Google Scholar]
  48. Cortese B, Palama IE, D'Amone S, Gigli G. 48.  2014. Influence of electrotaxis on cell behaviour. Integr. Biol. 6:817–30 [Google Scholar]
  49. Wang X, Veruki ML, Bukoreshtliev NV, Hartveit E, Gerdes HH. 49.  2010. Animal cells connected by nanotubes can be electrically coupled through interposed gap-junction channels. PNAS 107:17194–99 [Google Scholar]
  50. Wahlgren J, Karlson TDL, Brisslert M, Vaziri Sani F, Telemo E. 50.  et al. 2012. Plasma exosomes can deliver exogenous short interfering RNA to monocytes and lymphocytes. Nucleic Acids Res 40:e130 [Google Scholar]
  51. Adams DS, Levin M. 51.  2013. Endogenous voltage gradients as mediators of cell–cell communication: strategies for investigating bioelectrical signals during pattern formation. Cell Tissue Res 352:95–122 [Google Scholar]
  52. Adams DS, Levin M. 52.  2006. Inverse drug screens: a rapid and inexpensive method for implicating molecular targets. Genesis 44:530–40 [Google Scholar]
  53. Levin M, Thorlin T, Robinson KR, Nogi T, Mercola M. 53.  2002. Asymmetries in H+/K+-ATPase and cell membrane potentials comprise a very early step in left–right patterning. Cell 111:77–89 [Google Scholar]
  54. Adams DS, Masi A, Levin M. 54.  2007. H+ pump–dependent changes in membrane voltage are an early mechanism necessary and sufficient to induce Xenopus tail regeneration. Development 134:1323–35 [Google Scholar]
  55. Gupta PB, Onder TT, Jiang G, Tao K, Kuperwasser C. 55.  et al. 2009. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 138:645–59 [Google Scholar]
  56. Sun Y, Dong Z, Jin T, Ang KH, Huang M. 56.  et al. 2013. Imaging-based chemical screening reveals activity-dependent neural differentiation of pluripotent stem cells. eLife 2:e00508 [Google Scholar]
  57. Treger JS, Priest MF, Bezanilla F. 57.  2015. Single-molecule fluorimetry and gating currents inspire an improved optical voltage indicator. eLife 4:e10482 [Google Scholar]
  58. Tyner KM, Kopelman R, Philbert MA. 58.  2007. “Nanosized voltmeter” enables cellular-wide electric field mapping. Biophys. J. 93:1163–74 [Google Scholar]
  59. Smith PJS, Sanger RS, Messerli MA. 59.  2007. Principles, development and applications of self-referencing electrochemical microelectrodes to the determination of fluxes at cell membranes. Methods and New Frontiers in Neuroscience AC Michael 373–405 Boca Raton: CRC [Google Scholar]
  60. Salmanzadeh A, Sano MB, Shafiee H, Stremler MA, Davalos RV. 60.  2012. Isolation of rare cancer cells from blood cells using dielectrophoresis. IEEE Eng. Med. Biol. Soc. Conf 2012590–93 [Google Scholar]
  61. Schonecker S, Kraushaar U, Dufer M, Sahr A, Hardtner C. 61.  et al. 2014. Long-term culture and functionality of pancreatic islets monitored using microelectrode arrays. Integr. Biol. 6:540–44 [Google Scholar]
  62. Modi S, Krishnan Y. 62.  2011. A method to map spatiotemporal pH changes inside living cells using a pH-triggered DNA nanoswitch. Methods Mol. Biol. 749:61–77 [Google Scholar]
  63. Mello de Queiroz F, Ponte CG, Bonomo A, Vianna-Jorge R, Suarez-Kurtz G. 63.  2008. Study of membrane potential in T lymphocytes subpopulations using flow cytometry. BMC Immunol 9:63 [Google Scholar]
  64. Newton JC, Knisley SB, Zhou X, Pollard AE, Ideker RE. 64.  1999. Review of mechanisms by which electrical stimulation alters the transmembrane potential. J. Cardiovasc. Electrophysiol. 10:234–43 [Google Scholar]
  65. Baigent S, Stark J, Warner A. 65.  2001. Convergent dynamics of two cells coupled by a nonlinear gap junction. Nonlinear Anal 47:257–68 [Google Scholar]
  66. Hassan AM, El-Shenawee M. 66.  2010. Modeling biopotential signals and current densities of multiple breast cancerous cells. IEEE Trans. Biomed. Eng 572099–106 [Google Scholar]
  67. Cervera J, Alcaraz A, Mafe S. 67.  2016. Bioelectrical signals and ion channels in the modeling of multicellular patterns and cancer biophysics. Sci. Rep. 6:20403 [Google Scholar]
  68. Cervera J, Manzanares JA, Mafe S. 68.  2015. Electrical coupling in ensembles of nonexcitable cells: Modeling the spatial map of single cell potentials. J. Phys. Chem. B 119:2968–78 [Google Scholar]
  69. Law R, Levin M. 69.  2015. Bioelectric memory: modeling resting potential bistability in amphibian embryos and mammalian cells. Theor. Biol. Med. Model 1222 [Google Scholar]
  70. Pietak A, Levin M. 70.  2016. Exploring instructive physiological signaling with the bioelectric tissue simulation engine (BETSE). Front. Bioeng. Biotechnol. 4:55 [Google Scholar]
  71. Erson EZ, Cavusoglu MC. 71.  2012. Design of a framework for modeling, integration and simulation of physiological models. Comput. Methods Progr. Biomed. 107:524–37 [Google Scholar]
  72. Cheney N, Clune J, Lipson H. 72.  2014. Evolved electrophysiological soft robots. Proceedings of the 14th International Conference on the Synthesis and Simulation of Living Systems (ALIFE 14) H Sayama, J Rieffel, S Risi, F Doursat, H Lipson 222–29 Cambridge, MA: MIT Press [Google Scholar]
  73. De A, Chakravarthy VS, Levin M. 73.  2016. A computational model of planarian regeneration. Int. J. Parallel Emerg. Distrib. Syst. In press
  74. Tseng AS, Beane WS, Lemire JM, Masi A, Levin M. 74.  2010. Induction of vertebrate regeneration by a transient sodium current. J. Neurosci. 30:13192–200 [Google Scholar]
  75. Blackiston D, Adams DS, Lemire JM, Lobikin M, Levin M. 75.  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 [Google Scholar]
  76. Pai VP, Lemire JM, Pare JF, Lin G, Chen Y, Levin M. 76.  2015. Endogenous gradients of resting potential instructively pattern embryonic neural tissue via notch signaling and regulation of proliferation. J. Neurosci. 35:4366–85 [Google Scholar]
  77. Vardy E, Robinson JE, Li C, Olsen RH, DiBerto JF. 77.  et al. 2015. A new DREADD facilitates the multiplexed chemogenetic interrogation of behavior. Neuron 86:936–46 [Google Scholar]
  78. Lin JY. 78.  2011. A user's guide to channelrhodopsin variants: features, limitations and future developments. Exp. Physiol. 96:19–25 [Google Scholar]
  79. Wheeler MA, Smith CJ, Ottolini M, Barker BS, Purohit AM. 79.  et al. 2016. Genetically targeted magnetic control of the nervous system. Nat. Neurosci. 19:756–61 [Google Scholar]
  80. Long X, Ye J, Zhao D, Zhang S-J. 80.  2015. Magnetogenetics: remote non-invasive magnetic activation of neuronal activity with a magnetoreceptor. Sci. Bull. 60:2107–19 [Google Scholar]
  81. Bernstein JG, Garrity PA, Boyden ES. 81.  2012. Optogenetics and thermogenetics: technologies for controlling the activity of targeted cells within intact neural circuits. Curr. Opin. Neurobiol. 22:61–71 [Google Scholar]
  82. Ibsen S, Tong A, Schutt C, Esener S, Chalasani SH. 82.  2015. Sonogenetics is a non-invasive approach to activating neurons in Caenorhabditis elegans. Nat. Commun. 6:8264 [Google Scholar]
  83. Adams DS, Lemire JM, Kramer RH, Levin M. 83.  2014. Optogenetics in developmental biology: using light to control ion flux-dependent signals in Xenopus embryos. Int. J. Dev. Biol. 58:851–61 [Google Scholar]
  84. Wang SJ, Weng CH, Xu HW, Zhao CJ, Yin ZQ. 84.  2014. Effect of optogenetic stimulus on the proliferation and cell cycle progression of neural stem cells. J. Membr. Biol. 247:493–500 [Google Scholar]
  85. Stroh A, Tsai HC, Wang LP, Zhang F, Kressel J. 85.  et al. 2010. Tracking stem cell differentiation in the setting of automated optogenetic stimulation. Stem Cells 29:78–88 [Google Scholar]
  86. Chernet BT, Adams DS, Lobikin M, Levin M. 86.  2016. Use of genetically encoded, light-gated ion translocators to control tumorigenesis. Oncotarget 7:19575–88 [Google Scholar]
  87. Adams DS, Tseng AS, Levin M. 87.  2013. Light-activation of the Archaerhodopsin H+-pump reverses age-dependent loss of vertebrate regeneration: sparking system-level controls in vivo. Biol. Open 2:306–13 [Google Scholar]
  88. Pashaie R, Baumgartner R, Richner TJ, Brodnick SK, Azimipour M. 88.  et al. 2015. Closed-loop optogenetic brain interface. IEEE Trans. Biomed. Eng 622327–37 [Google Scholar]
  89. Golding A, Guay JA, Herrera-Rincon C, Levin M, Kaplan DL. 89.  2016. A tunable silk hydrogel device for studying limb regeneration in adult Xenopus laevis. PLOS ONE 11:e0155618 [Google Scholar]
  90. Zhang Y, Levin M. 90.  2009. Particle tracking model of electrophoretic morphogen movement reveals stochastic dynamics of embryonic gradient. Dev. Dyn. 238:1923–35 [Google Scholar]
  91. Chernet B, Levin M. 91.  2013. Endogenous voltage potentials and the microenvironment: bioelectric signals that reveal, induce and normalize cancer. J. Clin. Exp. Oncol. Suppl 1:S1–002 [Google Scholar]
  92. Tai G, Reid B, Cao L, Zhao M. 92.  2009. Electrotaxis and wound healing: experimental methods to study electric fields as a directional signal for cell migration. Methods Mol. Biol. 571:77–97 [Google Scholar]
  93. Cao L, Wei D, Reid B, Zhao S, Pu J. 93.  et al. 2013. Endogenous electric currents might guide rostral migration of neuroblasts. EMBO Rep 14:184–90 [Google Scholar]
  94. Yamashita M. 94.  2013. Electric axon guidance in embryonic retina: galvanotropism revisited. Biochem. Biophys. Res. Commun. 431:280–83 [Google Scholar]
  95. Pan L, Borgens RB. 95.  2012. Strict perpendicular orientation of neural crest–derived neurons in vitro is dependent on an extracellular gradient of voltage. J. Neurosci. Res. 90:1335–46 [Google Scholar]
  96. Lalli M, Asthagiri A. 96.  2015. Collective migration exhibits greater sensitivity but slower dynamics of alignment to applied electric fields. Cell. Mol. Bioeng. 8:247 [Google Scholar]
  97. Minc N, Chang F. 97.  2010. Electrical control of cell polarization in the fission yeast Schizosaccharomyces pombe. Curr. Biol. 20:710–16 [Google Scholar]
  98. Shi R, Borgens RB. 98.  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 [Google Scholar]
  99. Herrera-Rincon C, Torets C, Sanchez-Jimenez A, Avendaño C, Panetsos F. 99.  2012. Chronic electrical stimulation of transected peripheral nerves preserves anatomy and function in the primary somatosensory cortex. Eur. J. Neurosci. 36:3679–90 [Google Scholar]
  100. Langlois VS, Martyniuk CJ. 100.  2013. Genome wide analysis of Silurana (Xenopus) tropicalis development reveals dynamic expression using network enrichment analysis. Mech. Dev. 130:304–22 [Google Scholar]
  101. House CD, Vaske CJ, Schwartz AM, Obias V, Frank B. 101.  et al. 2010. Voltage-gated Na+ channel SCN5A is a key regulator of a gene transcriptional network that controls colon cancer invasion. Cancer Res 70:6957–67 [Google Scholar]
  102. Kawakami Y, Raya A, Raya RM, Rodríguez-Esteban C, Belmonte JC. 102.  2005. Retinoic acid signalling links left–right asymmetric patterning and bilaterally symmetric somitogenesis in the zebrafish embryo. Nature 435:165–71 [Google Scholar]
  103. Perathoner S, Daane JM, Henrion U, Seebohm G, Higdon CW. 103.  et al. 2014. Bioelectric signaling regulates size in zebrafish fins. PLOS Genet 10:e1004080 [Google Scholar]
  104. Monteiro J, Aires R, Becker JD, Jacinto A, Certal AC, Rodríguez-León J. 104.  2014. V-ATPase proton pumping activity is required for adult zebrafish appendage regeneration. PLOS ONE 9:e92594 [Google Scholar]
  105. Nuckels RJ, Ng A, Darland T, Gross JM. 105.  2009. The vacuolar–ATPase complex regulates retinoblast proliferation and survival, photoreceptor morphogenesis, and pigmentation in the zebrafish eye. Investig. Ophthalmol. Vis. Sci. 50:893–905 [Google Scholar]
  106. Sims K Jr, Eble DM, Iovine MK. 106.  2009. Connexin43 regulates joint location in zebrafish fins. Dev. Biol. 327:410–18 [Google Scholar]
  107. Néant I, Mellström B, Gonzalez P, Naranjo JR, Moreau M, Leclerc C. 107.  2015. Kcnip1 a Ca2+-dependent transcriptional repressor regulates the size of the neural plate in Xenopus. . Biochim. Biophys. Acta 1853:2077–85 [Google Scholar]
  108. Panakova D, Werdich AA, Macrae CA. 108.  2010. Wnt11 patterns a myocardial electrical gradient through regulation of the L-type Ca2+ channel. Nature 466:874–78 [Google Scholar]
  109. Adams DS, Uzel SG, Akagi J, Wlodkowic D, Andreeva V. 109.  et al. 2016. Bioelectric signalling via potassium channels: a mechanism for craniofacial dysmorphogenesis in KCNJ2-associated Andersen–Tawil Syndrome. J. Physiol. 594:3245–70 [Google Scholar]
  110. Vandenberg LN, Morrie RD, Adams DS. 110.  2011. V-ATPase-dependent ectodermal voltage and pH regionalization are required for craniofacial morphogenesis. Dev. Dyn. 240:1889–904 [Google Scholar]
  111. Dahal GR, Rawson J, Gassaway B, Kwok B, Tong Y. 111.  et al. 2012. An inwardly rectifying K+ channel is required for patterning. Development 139:3653–64 [Google Scholar]
  112. Michard E, Alves F, Feijo JA. 112.  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 [Google Scholar]
  113. Feijo JA, Michard E, Dias P. 113.  2008. Tobacco pollen tubes as cellular models for ion dynamics: improved spatial and temporal resolution of extracellular flux and free cytosolic concentration of calcium and protons using pHluorin and YC3.1 CaMeleon. Sex Plant Reprod 21:169–81 [Google Scholar]
  114. Rajnicek AM, Gow NA, McCaig CD. 114.  1992. Electric field–induced orientation of rat hippocampal neurones in vitro. Exp. Physiol. 77:229–32 [Google Scholar]
  115. Rajnicek AM, McCaig CD, Gow NA. 115.  1994. Electric fields induce curved growth of Enterobacter cloacae, Escherichia coli, and Bacillus subtilis cells: implications for mechanisms of galvanotropism and bacterial growth. J. Bacteriol. 176:702–13 [Google Scholar]
  116. Kucerova R, Walczysko P, Reid B, Ou J, Leiper LJ. 116.  et al. 2011. The role of electrical signals in murine corneal wound re-epithelialization. J. Cell. Physiol. 226:1544–53 [Google Scholar]
  117. Martin-Granados C, McCaig CD. 117.  2014. Harnessing the electric spark of life to cure skin wounds. Adv. Wound Care 3:127–38 [Google Scholar]
  118. Chifflet S, Hernandez JA, Grasso S. 118.  2005. A possible role for membrane depolarization in epithelial wound healing. Am. J. Physiol. Cell Physiol. 288:C1420–30 [Google Scholar]
  119. Minuk GY, Zhang M, Gong Y, Minuk L, Dienes H. 119.  et al. 2007. Decreased hepatocyte membrane potential differences and GABAA-β3 expression in human hepatocellular carcinoma. Hepatology 45:735–45 [Google Scholar]
  120. Sabin K, Santos-Ferreira T, Essig J, Rudasill S, Echeverri K. 120.  2015. Dynamic membrane depolarization is an early regulator of ependymoglial cell response to spinal cord injury in axolotl. Dev. Biol. 408:14–25 [Google Scholar]
  121. Diaz Quiroz JF, Tsai E, Coyle M, Sehm T, Echeverri K. 121.  2014. Precise control of miR-125b levels is required to create a regeneration-permissive environment after spinal cord injury: a cross-species comparison between salamander and rat. Dis. Models Mech. 7:601–11 [Google Scholar]
  122. Zhang Z, Chen J, He Y, Zhan X, Zhao R. 122.  et al. 2014. miR-125b inhibits hepatitis B virus expression in vitro through targeting of the SCNN1A gene. Arch. Virol. 159:3335–43 [Google Scholar]
  123. Tseng A, Levin M. 123.  2013. Cracking the bioelectric code: probing endogenous ionic controls of pattern formation. Commun. Integr. Biol. 6:1–8 [Google Scholar]
  124. Marsh G, Beams HW. 124.  1949. Electrical control of axial polarity in a regenerating annelid. Anat. Rec. 105:513–14 [Google Scholar]
  125. Blackiston DJ, Levin M. 125.  2013. Ectopic eyes outside the head in Xenopus tadpoles provide sensory data for light-mediated learning. J. Exp. Biol. 216:1031–40 [Google Scholar]
  126. Thompson DM, Koppes AN, Hardy JG, Schmidt CE. 126.  2014. Electrical stimuli in the central nervous system microenvironment. Annu. Rev. Biomed. Eng 16397–430 [Google Scholar]
  127. Levin M. 127.  2007. Large-scale biophysics: ion flows and regeneration. Trends Cell Biol 17:262–71 [Google Scholar]
  128. Levin M, Stevenson CG. 128.  2012. Regulation of cell behavior and tissue patterning by bioelectrical signals: challenges and opportunities for biomedical engineering. Annu. Rev. Biomed. Eng 14295–323 [Google Scholar]
  129. Oviedo NJ, Morokuma J, Walentek P, Kema IP, Gu MB. 129.  et al. 2010. Long-range neural and gap junction protein–mediated cues control polarity during planarian regeneration. Dev. Biol. 339:188–99 [Google Scholar]
  130. Sullivan KG, Emmons-Bell M, Levin M. 130.  2016. Physiological inputs regulate species-specific anatomy during embryogenesis and regeneration. Commun. Integr. Biol. 9:e1192733 [Google Scholar]
  131. Levin M, Buznikov GA, Lauder JM. 131.  2006. Of minds and embryos: left–right asymmetry and the serotonergic controls of pre-neural morphogenesis. Dev. Neurosci. 28:171–85 [Google Scholar]
  132. Chan JD, Agbedanu PN, Zamanian M, Gruba SM, Haynes CL. 132.  et al. 2014. ‘Death and axes’: unexpected Ca2+ entry phenologs predict new anti-schistosomal agents. PLOS Pathog 10:e1003942 [Google Scholar]
  133. Miller RP, Becker BA. 133.  1975. Teratogenicity of oral diazepam and diphenylhydantoin in mice. Toxicol. Appl. Pharmacol. 32:53–61 [Google Scholar]
  134. Borodinsky LN, Belgacem YH, Swapna I, Visina O, Balashova OA. 134.  et al. 2015. Spatiotemporal integration of developmental cues in neural development. Dev. Neurobiol. 75:349–59 [Google Scholar]
  135. Aon MA, Cortassa S. 135.  1989. The regulation of plant-cell growth—a bio- electromechanochemical model. J. Theor. Biol. 138:429–56 [Google Scholar]
  136. Justet C, Evans F, Vasilskis E, Hernandez JA, Chifflet S. 136.  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 [Google Scholar]
  137. Nogi T, Levin M. 137.  2005. Characterization of innexin gene expression and functional roles of gap-junctional communication in planarian regeneration. Dev. Biol. 287:314–35 [Google Scholar]
  138. Emmons-Bell M, Durant F, Hammelman J, Bessonov N, Volpert V. 138.  et al. 2015. Gap junctional blockade stochastically induces different species-specific head anatomies in genetically wild-type Girardia dorotocephala flatworms. Int. J. Mol. Sci. 16:27865–96 [Google Scholar]
  139. Chernet BT, Levin M. 139.  2014. Transmembrane voltage potential of somatic cells controls oncogene-mediated tumorigenesis at long-range. Oncotarget 5:3287–306 [Google Scholar]
  140. Fraser SP, Diss JK, Chioni AM, Mycielska ME, Pan H. 140.  et al. 2005. Voltage-gated sodium channel expression and potentiation of human breast cancer metastasis. Clin. Cancer Res. 11:5381–89 [Google Scholar]
  141. Arcangeli A, Pillozzi S, Becchetti A. 141.  2012. Targeting ion channels in leukemias: a new challenge for treatment. Curr. Med. Chem 19683–96 [Google Scholar]
  142. Yang M, Brackenbury WJ. 142.  2013. Membrane potential and cancer progression. Front. Physiol. 4:185 [Google Scholar]
  143. Olivotto M, Arcangeli A, Carla M, Wanke E. 143.  1996. Electric fields at the plasma membrane level: a neglected element in the mechanisms of cell signalling. BioEssays 18:495–504 [Google Scholar]
  144. Than BL, Goos JA, Sarver AL, O'Sullivan MG, Rod A. 144.  et al. 2013. The role of KCNQ1 in mouse and human gastrointestinal cancers. Oncogene 33:3861–68 [Google Scholar]
  145. Newmark PA. 145.  2005. Opening a new can of worms: a large-scale RNAi screen in planarians. Dev. Cell 8:623–24 [Google Scholar]
  146. Mullins MC, Hammerschmidt M, Haffter P, Nüsslein-Volhard C. 146.  1994. Large-scale mutagenesis in the zebrafish: in search of genes controlling development in a vertebrate. Curr. Biol. 4:189–202 [Google Scholar]
  147. Adamatzky A, Costello B, Bull L, Holley J. 147.  2011. Towards arithmetic circuits in sub-excitable chemical media. Isr. J. Chem. 51:56–66 [Google Scholar]
  148. Leonetti M, Marcq P, Nuebler J, Homble F. 148.  2005. Cotransport-induced instability of membrane voltage in tip-growing cells. Phys. Rev. Lett. 95:208105 [Google Scholar]
  149. Zaika O, Palygin O, Tomilin V, Mamenko M, Staruschenko A, Pochynyuk O. 149.  2015. Insulin and IGF-1 activate Kir4.1/5.1 channels in cortical collecting duct principal cells to control basolateral membrane voltage. Am. J. Physiol. Renal Physiol. 310:F311–21 [Google Scholar]
  150. Swapna I, Borodinsky LN. 150.  2012. Interplay between electrical activity and bone morphogenetic protein signaling regulates spinal neuron differentiation. PNAS 109:16336–41 [Google Scholar]
  151. Jindal GA, Goyal Y, Burdine RD, Rauen KA, Shvartsman SY. 151.  2015. RASopathies: unraveling mechanisms with animal models. Dis. Models Mech. 8:769–72 [Google Scholar]
  152. Belgacem YH, Borodinsky LN. 152.  2015. Inversion of Sonic hedgehog action on its canonical pathway by electrical activity. PNAS 112:4140–45 [Google Scholar]
  153. Andrikopoulos P, Fraser SP, Patterson L, Ahmad Z, Burcu H. 153.  et al. 2011. Angiogenic functions of voltage-gated Na+ channels in human endothelial cells: modulation of vascular endothelial growth factor (VEGF) signaling. J. Biol. Chem. 286:16846–60 [Google Scholar]
  154. Zhang R, Qian F, Rajagopalan L, Pereira FA, Brownell WE, Anvari B. 154.  2007. Prestin modulates mechanics and electromechanical force of the plasma membrane. Biophys. J. 93:L7–9 [Google Scholar]
  155. Ghosh K, Ingber DE. 155.  2007. Micromechanical control of cell and tissue development: implications for tissue engineering. Adv. Drug Deliv. Rev. 59:1306–18 [Google Scholar]
  156. Joshi SD, von Dassow M, Davidson LA. 156.  2010. Experimental control of excitable embryonic tissues: Three stimuli induce rapid epithelial contraction. Exp. Cell Res. 316:103–14 [Google Scholar]
  157. Brownell WE, Qian F, Anvari B. 157.  2010. Cell membrane tethers generate mechanical force in response to electrical stimulation. Biophys. J. 99:845–52 [Google Scholar]
  158. Callies C, Fels J, Liashkovich I, Kliche K, Jeggle P. 158.  et al. 2011. Membrane potential depolarization decreases the stiffness of vascular endothelial cells. J. Cell Sci. 124:1936–42 [Google Scholar]
  159. Warren EA, Payne CK. 159.  2015. Cellular binding of nanoparticles disrupts the membrane potential. RSC Adv 5:13660–66 [Google Scholar]
  160. Hechavarria D, Dewilde A, Braunhut S, Levin M, Kaplan DL. 160.  2010. BioDome regenerative sleeve for biochemical and biophysical stimulation of tissue regeneration. Med. Eng. Phys 321065–73 [Google Scholar]
  161. Ruckh TT, Mehta AA, Dubach JM, Clark HA. 161.  2013. Polymer-free optode nanosensors for dynamic, reversible, and ratiometric sodium imaging in the physiological range. Sci. Rep. 3:3366 [Google Scholar]
  162. Knöpfel T, Lin MZ, Levskaya A, Tian L, Lin JY, Boyden ES. 162.  2010. Toward the second generation of optogenetic tools. J. Neurosci. 30:14998–5004 [Google Scholar]
  163. Robinson KR, Messerli MA. 163.  1996. Electric embryos: the embryonic epithelium as a generator of developmental information. Nerve Growth and Guidance CD McCaig 131–50 London: Portland [Google Scholar]
  164. Bovetti S, Fellin T. 164.  2015. Optical dissection of brain circuits with patterned illumination through the phase modulation of light. J. Neurosci. Methods 241:66–77 [Google Scholar]
  165. Seeger-Armbruster S, Bosch-Bouju C, Little ST, Smither RA, Hughes SM. 165.  et al. 2015. Patterned, but not tonic, optogenetic stimulation in motor thalamus improves reaching in acute drug–induced Parkinsonian rats. J. Neurosci. 35:1211–16 [Google Scholar]
  166. Birmingham K, Gradinaru V, Anikeeva P, Grill WM, Pikov V. 166.  et al. 2014. Bioelectronic medicines: a research roadmap. Nat. Rev. Drug Discov. 13:399–400 [Google Scholar]
  167. Brunet T, Arendt D. 167.  2016. From damage response to action potentials: early evolution of neural and contractile modules in stem eukaryotes. Philos. Trans. R. Soc. Lond. B 371:20150043 [Google Scholar]
  168. Cervera J, Alcaraz A, Mafe S. 168.  2014. Membrane potential bistability in nonexcitable cells as described by inward and outward voltage-gated ion channels. J. Phys. Chem. B 118:12444–50 [Google Scholar]
  169. Gallaher J, Bier M, Siegenbeek van Heukelom J. 169.  2009. The role of chloride transport in the control of the membrane potential in skeletal muscle—theory and experiment. Biophys. Chem. 143:18–25 [Google Scholar]
  170. Cang C, Aranda K, Ren D. 170.  2014. A non-inactivating high-voltage-activated two-pore Na+ channel that supports ultra-long action potentials and membrane bistability. Nat. Commun. 5:5015 [Google Scholar]
  171. Bull L, Budd A, Stone C, Uroukov I, de Lacy Costello B, Adamatzky A. 171.  2008. Towards unconventional computing through simulated evolution: control of nonlinear media by a learning classifier system. Artif. Life 14:203–22 [Google Scholar]
  172. Hsu H, Huang E, Yang XC, Karschin A, Labarca C. 172.  et al. 1993. Slow and incomplete inactivations of voltage-gated channels dominate encoding in synthetic neurons. Biophys. J. 65:1196–206 [Google Scholar]
  173. McNamara HM, Zhang H, Werley CA, Cohen AE. 173.  2016. Optically controlled oscillators in an engineered bioelectric tissue. Phys. Rev. X 6:031001 [Google Scholar]
  174. Quian Quiroga R, Panzeri S. 174.  2009. Extracting information from neuronal populations: information theory and decoding approaches. Nat. Rev. Neurosci. 10:173–85 [Google Scholar]
  175. Schultz SR, Ince RAA, Panzeri S. 175.  2014. Applications of information theory to analysis of neural data. arXiv1501.01860 [q-bio]
  176. Stoianov I, Genovesio A, Pezzulo G. 176.  2015. Prefrontal goal codes emerge as latent states in probabilistic value learning. J. Cogn. Neurosci. 28:140–57 [Google Scholar]
  177. Olshausen BA, Field DJ. 177.  1997. Sparse coding with an overcomplete basis set: a strategy employed by V1?. Vis. Res. 37:3311–25 [Google Scholar]
  178. Johnson A, Fenton AA, Kentros C, Redish AD. 178.  2009. Looking for cognition in the structure within the noise. Trends Cogn. Sci. 13:55–64 [Google Scholar]
  179. Pfeiffer BE, Foster DJ. 179.  2013. Hippocampal place-cell sequences depict future paths to remembered goals. Nature 497:74–79 [Google Scholar]
  180. Pezzulo G, van der Meer MAA, Lansink CS, Pennartz CMA. 180.  2014. Internally generated sequences in learning and executing goal-directed behavior. Trends Cogn. Sci. 18:647–57 [Google Scholar]
  181. Diba K, Buzsáki G. 181.  2007. Forward and reverse hippocampal place-cell sequences during ripples. Nat. Neurosci. 10:1241–42 [Google Scholar]
  182. Ramirez S, Liu X, Lin P-A, Suh J, Pignatelli M. 182.  et al. 2013. Creating a false memory in the hippocampus. Science 341:387–91 [Google Scholar]
  183. Nishimoto S, Vu AT, Naselaris T, Benjamini Y, Yu B, Gallant JL. 183.  2011. Reconstructing visual experiences from brain activity evoked by natural movies. Curr. Biol. 21:1641–46 [Google Scholar]
  184. Huth AG, de Heer WA, Griffiths TL, Theunissen FE, Gallant JL. 184.  2016. Natural speech reveals the semantic maps that tile human cerebral cortex. Nature 532:453–58 [Google Scholar]
  185. Cunningham JP, Yu BM. 185.  2014. Dimensionality reduction for large-scale neural recordings. Nat. Neurosci. 17:1500–9 [Google Scholar]
  186. Verschure P, Pennartz CMA, Pezzulo G. 186.  2014. The why, what, where, when and how of goal-directed choice: neuronal and computational principles. Philos. Trans. R. Soc. Lond. B 369:20130483 [Google Scholar]
  187. Tononi G. 187.  2008. Consciousness as integrated information: a provisional manifesto. Biol. Bull. 215:216–42 [Google Scholar]
  188. Friston K. 188.  2010. The free-energy principle: a unified brain theory?. Nat. Rev. Neurosci. 11:127–38 [Google Scholar]
  189. Pezzulo G, Rigoli F, Friston K. 189.  2015. Active Inference, homeostatic regulation and adaptive behavioural control. Prog. Neurobiol. 134:17–35 [Google Scholar]
  190. Gold JI, Shadlen MN. 190.  2007. The neural basis of decision making. Annu. Rev. Neurosci. 30:535–74 [Google Scholar]
  191. Lisman J. 191.  2015. The challenge of understanding the brain: where we stand in 2015. Neuron 86:864–82 [Google Scholar]
  192. Yoon G, Quitania L, Kramer JH, Fu YH, Miller BL, Ptacek LJ. 192.  2006. Andersen–Tawil syndrome: definition of a neurocognitive phenotype. Neurology 66:1703–10 [Google Scholar]
  193. Fukumoto T, Blakely R, Levin M. 193.  2005. Serotonin transporter function is an early step in left–right patterning in chick and frog embryos. Dev. Neurosci. 27:349–63 [Google Scholar]
  194. Gallaher J, Bier M, van Heukelom JS. 194.  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 [Google Scholar]
  195. Bissiere S, Zelikowsky M, Ponnusamy R, Jacobs NS, Blair HT, Fanselow MS. 195.  2011. Electrical synapses control hippocampal contributions to fear learning and memory. Science 331:87–91 [Google Scholar]
  196. Turner CH, Robling AG, Duncan RL, Burr DB. 196.  2002. Do bone cells behave like a neuronal network?. Calcif. Tissue Int. 70:435–42 [Google Scholar]
  197. Chakravarthy SV, Ghosh J. 197.  1997. On Hebbian-like adaptation in heart muscle: a proposal for ‘cardiac memory’. Biol. Cybern. 76:207–15 [Google Scholar]
  198. Regot S, Macia J, Conde N, Furukawa K, Kjellén J. 198.  et al. 2011. Distributed biological computation with multicellular engineered networks. Nature 469:207–11 [Google Scholar]
  199. Baluska F, Levin M. 199.  2016. On having no head: cognition throughout biological systems. Front. Psychol. 7:902 [Google Scholar]
  200. Bakkum DJ, Chao ZC, Potter SM. 200.  2008. Spatio-temporal electrical stimuli shape behavior of an embodied cortical network in a goal-directed learning task. J. Neural Eng. 5:310–23 [Google Scholar]
  201. Dranias MR, Ju H, Rajaram E, VanDongen AM. 201.  2013. Short-term memory in networks of dissociated cortical neurons. J. Neurosci. 33:1940–53 [Google Scholar]
  202. DeMarse TB, Dockendorf KP. 202.  2005. Adaptive flight control with living neuronal networks on microelectrode arrays. Proceedings of the IEEE Joint Conference on Neural Networks1548–51 Piscataway, NJ: IEEE [Google Scholar]
  203. Chao ZC, Bakkum DJ, Potter SM. 203.  2008. Shaping embodied neural networks for adaptive goal-directed behavior. PLOS Comput. Biol. 4:e1000042 [Google Scholar]
  204. Hunter PJ, Crampin EJ, Nielsen PM. 204.  2008. Bioinformatics, multiscale modeling and the IUPS Physiome Project. Brief. Bioinform. 9:333–43 [Google Scholar]
  205. Ishiguro K, Ando T, Watanabe O, Goto H. 205.  2010. Novel application of low pH-dependent fluorescent dyes to examine colitis. BMC Gastroenterol 10:4 [Google Scholar]
  206. Reid B, Graue-Hernandez EO, Mannis MJ, Zhao M. 206.  2011. Modulating endogenous electric currents in human corneal wounds—a novel approach of bioelectric stimulation without electrodes. Cornea 30:338–43 [Google Scholar]
  207. Sebastian A, Iqbal SA, Colthurst J, Volk SW, Bayat A. 207.  2015. Electrical stimulation enhances epidermal proliferation in human cutaneous wounds by modulating p53–SIVA1 interaction. J. Investig. Dermatol. 135:1166–74 [Google Scholar]
  208. Bates EA. 208.  2013. A potential molecular target for morphological defects of fetal alcohol syndrome: Kir2.1. Curr. Opin. Genet. Dev. 23:324–29 [Google Scholar]
  209. Rouabhia M, Park HJ, Zhang Z. 209.  2016. Electrically activated primary human fibroblasts improve in vitro and in vivo skin regeneration. J. Cell. Physiol. 231:1814–21 [Google Scholar]
  210. Spugnini EP, Citro G, Fais S. 210.  2010. Proton pump inhibitors as anti vacuolar-ATPases drugs: a novel anticancer strategy [sic]. J. Exp. Clin. Cancer Res. 29:44 [Google Scholar]
  211. Aur D. 211.  2012. From neuroelectrodynamics to thinking machines. Cogn. Comput. 4:4–12 [Google Scholar]
  212. Rubenstein M, Sai Y, Chuong CM, Shen WM. 212.  2009. Regenerative patterning in swarm robots: mutual benefits of research in robotics and stem cell biology. Int. J. Dev. Biol. 53:869–81 [Google Scholar]
  213. Montague PR, Dolan RJ, Friston KJ, Dayan P. 213.  2012. Computational psychiatry. Trends Cogn. Sci. 16:72–80 [Google Scholar]
  214. Liu X, Ramirez S, Tonegawa S. 214.  2014. Inception of a false memory by optogenetic manipulation of a hippocampal memory engram. Philos. Trans. R. Soc. Lond. B 369:20130142 [Google Scholar]
/content/journals/10.1146/annurev-bioeng-071114-040647
Loading
/content/journals/10.1146/annurev-bioeng-071114-040647
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error