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Publications

Bioelectricity

Durant, F., Morokuma, J., Fields, C., Williams, K., Adams, D. S., and Levin, M., (2017), Long-Term, Stochastic Editing of Regenerative Anatomy via Targeting Endogenous Bioelectric Gradients, Biophysical Journal, 112: 2231-2243
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Mathews, J., and Levin, M., (2017), Gap Junctional Signaling in Pattern Regulation: physiological network connectivity instructs growth and form, Developmental Neurobiology, 77(5): 643-673
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Levin, M., Pezzulo, G., and Finkelstein, J. M., (2017), Endogenous Bioelectric Signaling Networks: Exploiting Voltage Gradients for Control of Growth and Form, Annual Review of Biomedical Engineering, vol. 19, in press
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Thurber, A. E., Nelson, M., Frost C. L., Levin, M., Brackenbury W. J., and Kaplan D. L., (2017), IK channel activation increases tumor growth and induces differential behavioral responses in two breast epithelial cell lines, Oncotarget, in press
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Lobo, D., Lobikin, M., and Levin, M., (2017), Discovering novel phenotypes with automatically inferred dynamic models: partial melanocyte conversion in Xenopus, Nature Scientific Reports, 7: 41339
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Pezzulo, G., and Levin, M., (2016), Top-down Models in biology: Explanation and control of complex living systems above the molecular level, Journal of the Royal Society Interface, in press

Herrera-Rincon, C., Guay, J., and Levin, M., (2016), Bioelectrical coordination of cell activity toward anatomical target states: an engineering perspective on regeneration, in Regenerative Engineering and Developmental Biology: Principles and Applications, David Gardiner ed., CRC Press, Florida, in press

Pietak, A., and Levin, M., (2016), Exploring Instructive Physiological Signaling with the Bioelectric Tissue Simulation Engine (BETSE), Frontiers in Bioengineering and Biotechnology, 4(55): doi 10.3389/fbioe.2016.00055
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Sullivan, K. G., Emmons-Bell, M., and Levin, M., (2016), Physiological Inputs Regulate Species-Specific Anatomy During Embryogenesis And Regeneration, Communicative and Integrative Biology, 9:4, e1192733
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Durant, F., Lobo, D., Hammelman, J., and Levin, M., (2016), Physiological controls of large-scale patterning in planarian regeneration: a molecular and computational perspective on growth and form, Regeneration, 3(2): 78-102
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Chernet, B. T., Adams, D. S., Lobikin, M., and Levin, M., (2016), Use of genetically encoded, light-gated ion translocators to control tumorigenesis, Oncotarget, 7(15): 19575-19588
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D. S. Adams, S. G. M. Uzel, J. Akagi, D. Wlodkowic, V. Andreeva, P. C. Yelick, A. Devitt-Lee, J-F. Pare, and Michael Levin, (2016), Bioelectric signaling via potassium channels: a mechanism for craniofacial dysmorphogenesis in KCNJ2-associated Andersen-Tawil Syndrome, Journal of Physiology, 12: 3245-3270
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Li, C., Levin, M., and Kaplan, D., (2016), Bioelectric modulation of macrophage polarization, Scientific Reports, 6:21044, doi:10.1038/srep21044
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Sundelacruz, S., Levin M., and Kaplan, D. L., (2015), Comparison of the depolarization response of human mesenchymal stem cells from different donors, Science Reports, 5: 18279 (doi: 10.1038/srep18279)
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Emmons-Bell, M., Durant, F., Hammelman, J., Bessonov, N., Volpert, V., Morokuma, J., Pinet, K., Adams, D. S., Pietak, A., Lobo, D., and Levin, M., (2015), Gap junctional blockade stochastically induces different species-specific head anatomies in genetically wild-type Girardia dorotocephala flatworms, International Journal of Molecular Sciences, 16: 27865–27896
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Pezzulo, G., and Levin, M., (2015), Re-membering the body: applications of computational neuroscience to the top-down control of regeneration of limbs and other complex organs, Integrative Biology, 7: 1487-1517
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Lobikin, M., Lobo, D., Blackiston, D. J., Martyniuk, C. J., Tkachenko, E., and Levin, M., (2015), Serotonergic regulation of melanocyte conversion: A bioelectrically regulated network for stochastic all-or-none hyperpigmentation, Science Signaling, 8(397): ra99
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Law, R., and Levin, M., (2015), Bioelectric memory: modeling resting potential bistability in amphibian embryos and mammalian cells, Theoretical Biology and Medical Modelling, 12: (1): 22
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Pai, V. P., Martyniuk, C. J., Echeverri, K., Sundelacruz, S., Kaplan, D. L., and Levin, M., (2015), Genome-wide analysis reveals conserved transcriptional responses downstream of resting potential change in Xenopus embryos, axolotl regeneration, and human mesenchymal cell differentiation, Regeneration, 3(1): 3-25
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Schatzberg, D., Lawtn, M., Hadyniak S. E., Ross E. J., Carney T., Beane W. S., Levin, M., and Bradham, C. A., (2015), H+/K+-ATPase activity is required for biomineralization in sea urchin embryos, Developmental Biology, 406(2): 259-270
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Pai, V. P., Lemire J. M., Chen Y., Lin G., and Levin M., (2015), Local and long-range endogenous resting potential gradients antagonistically regulate apoptosis and proliferation in the embryonic CNS, International Journal of Developmental Biology, 59: 327-340 (2015)
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Lobikin, M., Pare, J-F., Kaplan, D. L., and Levin, M., (2015), Selective Depolarization Of Transmembrane Potential Alters Muscle Patterning And Muscle Cell Localization In Embryonic Xenopus Laevis, International Journal of Developmental Biology, 59: 303-311 (2015)
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Pai, V., Lemire, J. M., Pare, J-F., Lin, G., Chen, Y., and Levin, M., (2015), Endogenous gradients of resting potential instructively pattern embryonic neural tissue via Notch signaling and regulation of proliferation, Journal of Neuroscience, 35(10): 4366-4385
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Blackiston, D., Anderson, G. M., Rahman, N., Bieck, C., and Levin, M., (2015), A novel method for inducing nerve growth via modulation of host resting potential, Neurotherapeutics, 12: 170-184
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Chernet, B. T., Fields, C., and Levin, M., (2014), Long-range gap junctional signaling controls oncogene-mediated tumorigenesis in Xenopus laevis embryos, Frontiers in Physiology, 5(519) 1-15, doi: 10.3389/fphys.2014.00519
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Levin, M., (2014), Molecular bioelectricity: how endogenous voltage potentials control cell behavior and instruct pattern regulation in vivo, Molecular Biology of the Cell, 25: 3835-3850
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Özkucur, N., Quinn, K. P., Pang, J. C., Du, C., Georgakoudi, I., Miller, E., Levin, M., and Kaplan, D. L., (2015), Membrane potential depolarization causes alterations in neuron arrangement and connectivity in cocultures, Brain and Behavior, 5(1): 24-38
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Adams, D.S., Lemire, J. M., Kramer, R. H., and Levin, M., (2014), Optogenetics in developmental biology: using light to control ion flux-dependent signals in Xenopus embryos, International Journal of Developmental Biology, 58: 851-861
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Lan J. Y., Williams C., Levin M., and Black L.D. III, (2014), Depolarization of Cellular Resting Membrane Potential Promotes Neonatal Cardiomyocyte Proliferation In Vitro, Cellular and Molecular Bioengineering, doi: 10.1007/s12195-014-0346-7
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Mustard, J., and Levin, M., (2014), Bioelectrical mechanisms for programming growth and form: taming physiological networks for soft body robotics, Soft Robotics, 1(3): 169-191
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Chernet, B., and Levin, M., (2014), Transmembrane voltage potential of somatic cells controls oncogene-mediated tumorigenesis at long-range, Oncotarget, 5(10): 3287-3306
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Hernandez-Diaz S., and Levin, M., (2014), Alteration of bioelectrically-controlled processes in the embryo: a teratogenic mechanism for anticonvulsants, Reproductive Toxicology, 47: 111-114
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Levin, M., (2014), Endogenous bioelectrical networks store non-genetic patterning information during development and regeneration, Journal of Physiology, 592(11): 2295–2305.
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Pai, V., and Levin, M., (2014), Bioelectric Controls of Stem Cell Function, in Stem Cells, edited by F. Calegari and C. Waskow, CRC Press, Chapter 5, p. 106-145
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Lobikin, M., and Levin, M., (2014), Endogenous bioelectric cues as morphogenetic signals in vivo, chapter 15 in The Fields of Cells, edited by D. Fels and M. Cifra, p. 283-302
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Sundelacruz S, Li C, Choi YJ, Levin M, Kaplan DL., (2013), Bioelectric modulation of wound healing in a 3D in vitro model of tissue-engineered bone, Biomaterials, 34(28): 6695-705
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Sundelacruz S, Levin M, Kaplan DL., (2013), Depolarization Alters Phenotype, Maintains Plasticity of Predifferentiated Mesenchymal Stem Cells, Tissue Engineering Part A, 19 (17-18): 1889-908
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Chernet, B., and Levin, M., (2013), Endogenous voltage potentials and the microenvironment: bioelectric signals that reveal, induce, and normalize cancer, Journal of Clinical and Experimental Oncology, S1: doi:10.4172/2324-9110.S1-002

Levin, M., (2013), Reprogramming cells and tissue patterning via bioelectrical pathways: molecular mechanisms and biomedical opportunities, WIREs Systems Biology and Medicine, 5(6): 657-676
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Chernet, B. T., and Levin, M., (2013), Transmembrane voltage potential is an essential cellular parameter for the detection and control of tumor development, Disease Models and Mechanisms, 6: 595-607
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Beane, W. S., Morokuma, J., Lemire, J. M., and Levin, M., (2013), Bioelectric signaling regulates head and organ size during planarian regeneration, Development, 140:313-322
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Tseng, A-S., and Levin, M., (2013), Cracking the bioelectric code: probing endogenous ionic controls of pattern formation, Communicative and Integrative Biology, 6(1):1-8
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Adams, D. S., Tseng, A-S. and M. Levin, (2013), Light-activation of the Archaerhodopsin H+ pump reverses age-dependent loss of vertebrate regeneration: sparking system-level controls in vivo, Biology Open, 2(3): 306-313
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Pai, V. P., Vandenberg, L. N,, Blackiston, D. J., and Levin, M., (2012), Neurally-derived tissues in Xenopus laevis embryos exhibit a consistent bioelectrical left-right asymmetry, Stem Cells International, Vol. 2012, Article ID 353491, 16 pages, doi:10.1155/2012/353491
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Lobikin, M., Chernet, B., Lobo, D., and Levin, M., (2012), Resting potential, oncogene-induced tumorigenesis, and metastasis: the bioelectric basis of cancer in vivo, Physical Biology, 9: 065002 [cover]
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Tseng, A-S., and M. Levin, (2012), Transducing bioelectrical signals into epigenetic pathways during tadpole tail regeneration, Anatomical Record, 295:1541-1551
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Adams, D. S., and Levin, M., (2012), Endogenous Voltage Gradients as Mediators of Cell-Cell Communication: Strategies for Investigating Bioelectrical Signals During Pattern Formation, Cell and Tissue Research, (2013) 352:95-122 [cover]
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Levin, M., and Stevenson, C., (2012), Regulation of Cell Behavior and Tissue Patterning by Bioelectrical Signals: challenges and opportunities for biomedical engineering, Annual Reviews in Biomedical Engineering, 14: 295-323
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Adams, D. S., and M. Levin, (2012), General principles for measuring resting membrane potential and ion concentration using fluorescent bioelectricity reporters, CSHL Protocols, doi: 10.1101/pdb.top067710 [cover]
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Adams, D. S., and M. Levin, (2012), Measuring resting membrane potential using the fluorescent voltage reporters DiBAC4(3) and CC2-DMPE, CSHL Protocols, doi: 10.1101/pdb.prot067702
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Levin, M., (2012), Molecular bioelectricity in developmental biology: new tools and recent discoveries, BioEssays, 34(3): 205-217 [cover]
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Pai, V., Aw, S., Shomrat, T., Lemire, J. M., and Levin, M., (2012), Transmembrane voltage potential controls embryonic eye patterning in Xenopus laevis. Development, 139: 313-323
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Blackiston, D., Adams, D. S., Lemire, J. M., Lobikin, M., and Levin, M., (2011), Transmembrane potential of GlyCl-expressing instructor cells induces a neoplastic-like conversion of melanocytes via a serotonergic pathway. Disease Models and Mechanisms, 4: 67-85
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Beane, W. S., Morokuma, J., Adams, D. S., and Levin, M., (2011), A chemical genetics approach reveals H,K-ATPase-mediated membrane voltage is required for planarian head regeneration. Cell Chemistry and Biology, 18: 77-89
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Lange, C., Silvia, P., Knuckles, P., Taylor, V., Levin, M., Calegari, F., (2011), The H+ V-ATPase maintains neural stem cells in the developing mouse cortex. Stem Cells and Development, 20(5): 1-8
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Levin, M. (2011), Endogenous bioelectrical signals in development, regeneration, and neoplasm, in Topical Talks: The Biomedical & Life Sciences Collection, Henry Stewart Talks Ltd, London.
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Levin, M. (2011), Left-Right Asymmetry in Embryonic Development: How epigenetic, biophysical forces and gene activity interplay to determine a major embryonic axis, in Topical Talks: The Biomedical & Life Sciences Collection, Henry Stewart Talks Ltd, London.
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Levin, M., (2011), Endogenous Bioelectric Signals as Morphogenetic Controls of Development, Regeneration, and Neoplasm, in The Physiology of Bioelectricity in Development, Tissue Regeneration, and Cancer, C. Pullar ed., CRC Press.
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Levin, M., (2011), The wisdom of the body: future techniques and approaches to morphogenetic fields in regenerative medicine, developmental biology, and cancer. Regenerative Medicine, 6(6): 667-673
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Aw, S., Koster, J., Pearson, W., Nicols, C., Shi, N. Q., Carneiro, K., and Levin, M., (2010), The ATP-sensitive K+-channel (KATP) controls early left-right patterning in Xenopus and chick embryos. Developmental Biology, 346: 39-53
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Tseng, A-S., Beane, W. S., Lemire, J. M., Masi, A., and M. Levin, (2010), Induction of vertebrate regeneration by a transient sodium current, Journal of Neuroscience, 30(39): 13192-13200
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Zhang, Y., and M. Levin, (2009), Particle tracking model of electrophoretic morphogen movement reveals stochastic dynamics of embryonic gradient, Developmental Dynamics, 238(8): 1923-1935
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Levin, M. (2009), Bioelectric mechanisms in regeneration: Unique aspects and future perspectives. Seminars in Cell and Developmental Biology, 20: 543-556
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Levin, M., Sundelacruz, S., Levin M., Kaplan, D. L., (2009), Role of membrane potential in the regulation of cell proliferation and differentiation, Stem Cell Reviews, 5(3): 231-46
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Blackiston, D. J., K. McLaughlin, and Levin, M., (2009), Bioelectric controls of cell proliferation: ion channels, membrane voltage, and the cell cycle, Cell Cycle, 8(21): 3527-3536
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Morokuma, J., Blackiston, D., and Levin, M., (2008), KCNQ1 and KCNE1 K+ channel components are involved in early left-right patterning in Xenopus embryos, Cellular Physiology and Biophysics, 21: 345-360
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Morokuma, J., Blackiston, D., Adams, D. S., Trimmer, B., and Levin, M., (2008), Modulation of potassium channel confers a hyper-proliferative, invasive phenotype on embryonic stem cells, Proceedings of the National Academy of Science, 105(43): 16608-16613
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Sundelacruz, S., M. Levin, and D. L. Kaplan, (2008), Membrane potential controls adipogenic and osteogenic differentiation of mesenchymal stem cells, PLoS One, 3(11): e3737, 1-15
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Oviedo, N. J., Nicolas, C. L., Adams, D. S., and Levin, M., (2008), Live imaging of planarian membrane potential using DiBAC4(3). Cold Spring Harbor Protocols, doi:10.1101/pdb.prot5055
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Adams, D. S., Masi, A., and Levin, M. (2007), H+ Pump-dependent changes in membrane voltage are an early mechanism necessary and sufficient to induce tail regeneration. Development, 134: 1323-1335
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Aw, S., Adams, D. S., Qiu, D., and Levin, M., (2007), H,K-ATPase protein Localization and Kir4.1 function reveal concordance of 3 axes during early determination of left-right asymmetry, Mechanisms of Development, 125: 353-372
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Levin, M., (2007), Large-Scale Biophysics: Ion Flows and Regeneration. Trends in Cell Biology, 17(6): 262-271
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Hibino, T., I. Yuichiro, Levin, M., and Nishino, A., (2006), Ion flow regulates left-right asymmetry in sea urchin development. Development, Genes and Evolution, 216(5): 265-76
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Shimeld, S. M., and Levin, M., (2006), Evidence for the regulation of left-right asymmetry in Ciona intestinalis by ion flux. Developmental Dynamics, 235(6): 1543-1553
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Adams DS, Robinson KR, Fukumoto T, Yuan S, Yelick P, Kuo L, McSweeney M, Levin M., (2006), The V-ATPase generates asymmetric H+ flux required for correct LR asymmetry in chick and frog embryos. Development, 133: 1657-1671
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Esser, A. T., Smith, K. C., Weaver, J. C., and Levin, M., (2006), A Mathematical Model of Morphogen Electrophoresis through Gap Junctions. Developmental Dynamics, 235: 2144-2159
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Adams, D. S., and Levin, M., (2006), Inverse Drug Screens: a rapid and inexpensive method for implicating molecular targets. Genesis, 44: 530-540
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Adams, D., and Levin, M., (2006), Strategies and techniques for investigation of biophysical signals in patterning, in Analysis of Growth Factor signaling in Embryos, M. Whitman and A. K. Sater eds., pp. 177-214, Methods in Signal Transduction Series, CRC Press

M. Levin, (2003), Electromagnetic fields in morphogenesis. Bioelectromagnetics, 24: 295-315
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M. Levin, (2003), Motor protein control of ion flux is an early step in embryonic Left-Right asymmetry. BioEssays, 25(10): 1002-1010
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Levin, Michael, T. Thorlin, K. Robinson, T. Nogi, and M. Mercola, (2002), H+/K+-ATPase activity comprises an early step of left-right asymmetry during development. Cell, 111: 77-89
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J. Rutenberg, S. M. Cheng, and M. Levin, (2002), Early embryonic expression of ion channels and pumps in chick and Xenopus embryogenesis. Developmental Dynamics, 225(4): 469-484
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S. M. Cheng, I. Chen, and M. Levin, (2002), Katp channel activity is required for hatching in Xenopus. Developmental Dynamics, 225(4): 588-591
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Levin, Michael, (1999), Endogenous electromagnetic fields and radiations in regeneration, development, and neoplasm, Proceedings of the First World Congress on the Effects of Electricity and Magnetism in the Natural World, Madeira, Portugal

Levin, Michael, and Susan G. Ernst, (1997), DC magnetic field effects on early sea urchin development. Bioelectromagnetics, 18(3): 255-263
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Levin, Michael, and Ernst, Susan G., (1995), AC magnetic field effects on early sea urchin development. Bioelectromagnetics, 16: 231-240
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Levin, Michael, Current and potential applications of bioelectromagnetics in medicine, (1993), ISSEEM Journal, 4(1): 77-87
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