Publications

Aging as a loss of morphostatic information: a developmental bioelectricity perspective
Pio-Lopez, L., Levin, M. (2024)
Ageing Research Reviews, 2024, 97:102310, doi:10.1016/j.arr.2024.102310

Electroceuticals: emerging applications beyond the nervous system and excitable tissues
Balasubramanian, S., Weston, D., Levin, M., Davidian, D. C. C. (2024)
Cell Press, 2109 doi.org/10.1016/j.tips.2024.03.001

Charging Ahead: Examining the future therapeutic potential of electroceuticals
Balasubramanian, S., Weston, D., Levin, M., Davidian, D. C. C. (2024)
Advanced Therapeutics, 2024, 2300344

Programmable delivery of fluoxetine via wearable bioelectronics for wound healing in vivo
Li, H., Yang, H.-Y., Asefifeyzabadi, N., Baniya, P., Medina Lopez, A., Gallegos, A., Zhu, K., Hsieh, H.-C., Nguyen, T., Hernandez, C., Zlobina, K., Recendez, C., Tebyani, M., Carrión, H., Selberg, J., Luo, L., Alhamo, M. A., Soulika, A. M., Levin, M., Norouzi, N., Gomez, M., Zhao, M., Teodorescu, M., Isseroff, R. R., Rolandi, M. (2024)
Advanced Materials Technology, 9(7):2301115

Future Medicine: from molecular pathways to the collective intelligence of the body
Lagasse, E., and Levin, M. (2023)
Trends in Molecular Medicine, 29(9): 687-710

Morphoceuticals: Perspectives for discovery of drugs targeting anatomical control mechanisms in regenerative medicine, cancer and aging
Pio-Lopez, L., and Levin, M. (2023)
Drug Discovery Today, 28(6): 103585

Cellular Signaling Pathways as Plastic, Proto-cognitive Systems: Implications for Biomedicine
Mathews, J., Chang, J., Devlin, L., and Levin, M. (2023)
Patterns, 4(5): 100737

Synthetic morphology with agential materials
Davies, J., and Levin, M. (2023)
Nature Reviews Bioengineering, 1(1): 46-59

Ion Channel Drugs Suppress Cancer Phenotype in NG108-15 and U87 Cells: Toward Novel Electroceuticals for Glioblastoma
Mathews, J., Kuchling, F., Baez-Nieto, D., Diberardinis, M., Pan, J. Q., and Levin, M. (2022)
Cancers, 14(6): 1499

Acute multidrug delivery via a wearable bioreactor facilitates long-term limb regeneration and functional recovery in adult Xenopus laevis
Murugan, N. J., Vigran, H. J., Miller, K., Golding, A., Pham, Q. L., Sperry, M., Rasmussen-Ivey, C., Kane, A. W., Kaplan, D. L., and Levin, M. (2022)
Science Advances, 8(4): abj2164

When left does not seem right: epigenetic and bioelectric differences between left- and right-sided breast cancer
Masuelli, S., Sebastian, R., Campoy, E., Branham, M. T., Marzese, D. M., Matthew, S., DeBlas, G., Rodolfo, A., Levin, M., and Roque, M. (2022)
Molecular Medicine, 28(1): 15

Potassium channel-driven bioelectric signalling regulates metastasis in triple-negative breast cancer
Payne, S. L., Ram, P., Srinivasan, D. H., Le, T. T., Levin, M., and Oudin, M. J. (2021)
EBioMedicine, 75: 103767

Bioelectrical approaches to cancer as a problem of the scaling of the cellular self
Levin, M. (2021)
Progress in Biophysics and Molecular Biology, 165: 102-113

Inducing Vertebrate Limb Regeneration: A Review of Past Advances and Future Outlook
Davidian, D., and Levin, M. (2021)
in K. D. Poss and D. T. Fox (Ed.), Regeneration, CSH Press: Boca Raton, FL,  doi:10.1101/cshperspect.a040782

A cellular platform for the development of synthetic living machines
Blackiston, D., Lederer, E., Kriegman, S., Garnier, S., Bongard, J., and Levin, M. (2021)
Science Robotics, 6(52): eabf1571

Learning and synaptic plasticity in 3D bioengineered neural tissues
Cairns, D. M., Rusk, W., Levin, M., Rouleau, N., and Kaplan, D. (2021)
Neuroscience Letters, 750: 135799

Bioelectric Signaling: Reprogrammable Circuits Underlying Embryogenesis, Regeneration, and Cancer
Levin, M. (2021)
Cell, 184(8): 1971-1989

Gene Regulatory Networks Exhibit Several Kinds of Memory: Quantification of Memory in Biological and Random Transcriptional Networks
Biswas, S., Manicka, S., Hoel, E., and Levin, M. (2021)
iScience, 24(3): 102131

Bistability of Somatic Pattern Memories: Stochastic Outcomes in Bioelectric Circuits Underlying Regeneration
Pezzulo, G., Lapalme, J., Durant, F., and Levin, M. (2021)
Philosophical Proceedings of the Royal Society B, 376(1821): 20190765

Machine Learning-Driven Bioelectronics for Closed-Loop Control of Cells
Selberg, J., Jafari, M., Mathews, J., Jia, M., Pansodtee, P., Dechiraju, H., Wu, C., Cordero, S., Flora, A., Yonas, N., Jannetty, S., Diberardinis, M., Teodorescu, M., Levin, M., Gomez, M., and Rolandi, M. (2020)
Advanced Intelligent Systems, 2(12): 2000140

HCN2 Channel-induced Rescue of Brain Teratogenesis via local and long-range bioelectric repair
Pai, V., Cervera, J., Mafé, S., Willocq, V., Lederer, E., and Levin, M. (2020)
Frontiers in Cellular Neuroscience, 14: 136

A 3D tissue model of traumatic brain injury with excitotoxicity that is inhibited by chronic exposure to gabapentinoids
Rouleau, N., Bonzanni, M., Erndt-Marino, J., Sievert, K., Ramirez, C., Rusk, W., Levin, M., and Kaplan, D. (2020)
Biomolecules, 10(8): 1196

von Willebrand factor D and EGF domains is an evolutionarily conserved and required feature of blastemas capable of multitissue appendage regeneration
Leigh, N. D., Sessa, S., Dragalzew, A. C., Payzin‐Dogru, D., Sousa, J. F., Aggouras, A. N., Johnson, K., Dunlap, G. S., Haas, B. J., Levin, M., Schneider, I., Whited, J. L. (2020)
Evolution & Development, 22(4): 297-311

Sertraline induces DNA damage and cellular toxicity in Drosophila that can be ameliorated by antioxidants
Jajoo, A., Donlon, C., Shnayder, S., Levin, M., and McVey, M. (2020)
Scientific Reports, 10: 4512

An in vivo brain–bacteria interface: the developing brain as a key regulator of innate immunity
Herrera-Rincon, C., Paré, J-F., Martyniuk, C. J., Jannetty, S. K., Harrison C., Fischer, A., Dinis, A., Keshari, V., Novak, R., and Levin, M. (2020)
NPJ Regenerative Medicine, 5: 2

A Meta-Analysis of Bioelectric Data in Cancer, Embryogenesis, and Regeneration
Srivastava, P., Kane, A., Harrison, C., and Levin, M. (2020)
Bioelectricity, 3(1): 42-67

A scalable pipeline for designing reconfigurable organisms
Kriegman, S., Blackiston, D., Levin, M., and Bongard, J. (2020)
Proceedings of the National Academy of Sciences of the United States, 117(4): 1853-1859

Assessment of Enrichment of Human Mesenchymal Stem Cells Based on Plasma and Mitochondrial Membrane Potentials
Kamaldinov, T., Erndt-Marino, J., Levin, M., Kaplan, D. L., and Hahn, M. S. (2020)
Bioelectricity, 2(1): 21-32

Endogenous Bioelectrics in Development, Cancer, and Regeneration: Drugs and Bioelectronic Devices as Electroceuticals for Regenerative Medicine
Levin, M., Selberg, J., and Rolandi, M. (2019)
iScience, 22: 519–533

Interdisciplinary Approach Needed to Crack Morphogenesis
Finkelstein J., McLaughlin K., Levin M. (2019)
The Scientist, December 2019

L-type voltage-gated Ca2+ channel CaV1.2 regulates chondrogenesis during limb development
Atsuta, Y., Tomizwa, R. R., Levin, M., and Tabin, C. J. (2019)
Proceedings of the National Academy of Sciences of the United States, 116(43): 21592-21601

Hyperosmolar potassium inhibits myofibroblast conversion and reduces scar tissue formation
Grasman, J., Williams, M., Razis, C., Bonzanni, M., Golding, A., Cairns, D. M., Levin, M., and Kaplan, D. L. (2019)
ACS Biomaterials Science & Engineering, 5(10): 5327-5336

Bioelectric control of metastasis in solid tumors
Payne, S. L., Levin, M., and Oudin, M. J.,(2019)
Bioelectricity, 1(3): 114-130

A flow through device for simultaneous dielectrophoretic cell trapping and AC electroporation
Punjiya, M., Nehad, H. R., Mathews, J., Levin, M., and Sonkusale, S. (2019)
Scientific Reports, 9: 11988

Bioelectrical controls of morphogenesis: from ancient mechanisms of cell coordination to biomedical opportunities
Whited, J., and Levin, M. (2019)
Current Opinion in Genetics & Development, 57: 61-69

EDEn – Electroceutical Design Environment: An Ion Channel Database with Small Molecule Modulators
Churchill, C. D. M., Winter, P., Tuszynski, J. A., and Levin, M. (2019)
iScience, 11: 42-56

Membrane potential depolarization alters calcium flux and phosphate signaling during osteogenic differentiation of human mesenchymal stem cells
Sundelacruz, S., Moody, A. T., Levin, M., and Kaplan, D. (2019)
Bioelectricity, 1(1): 56-66

Brief Local Application of Progesterone via a Wearable Bioreactor Induces Long-Term Regenerative Response in Adult Xenopus Hindlimb
Herrera-Rincon, C., Golding, A. S., Moran, K. M., Harrison, C., Martyniuk, C. J., Guay, J. A., Zaltsman, J., Carabello, H., Kaplan, D. L., and Levin, M. (2018)
Cell Reports, 25(6): 1593-1609

Ivermectin promotes peripheral nerve regeneration during wound healing
Cairns, D. M., Giordano, J. E., Conte, S., Levin, M., and Kaplan, D. L. (2018)
ACS Omega, 3(10): 12392-12402

Cross-limb Communication During Xenopus Hind-limb Regenerative Response: Non-Local Bioelectric Injury Signals
Busse, S. M., McMillen, P. T., and Levin, M. (2018)
Development, 145(19): dev164210

HCN2 Rescues brain defects by enforcing endogenous voltage pre-patterns
Pai, V. P., Pietak, A., Willocq, V., Ye, B., Shi, N-Q., and Levin, M. (2018)
Nature Communications, 9(1): 998

Niclosamide rescues microcephaly in a humanized in vivo model of Zika infection using human induced neural stem cells
Cairns, D. M., Boorgu, D. S. S. K., Levin, M., and Kaplan, D. L. (2018)
Biology Open, 7(1): bio031807

Booting up the organism during development: pre-behavioral functions of the vertebrate brain in guiding body morphogenesis
Herrera-Rincon, C., and Levin, M. (2018)
Communicative & Integrative Biology, 11(1): e1433440

Cancer as a Disorder of Patterning Information: computational and biophysical perspectives on the cancer problem
Moore, D., Walker, S., and Levin, M. (2017)
Convergent Science Physical Oncology, 3(4): 043001

Using optogenetics in vivo to stimulate regeneration
Adams, D. S., Tseng. A-S., and Levin, M. (2017)
In K. Appasani (Ed.), Optogenetics: From Neuronal Function to Mapping and Disease Biology, Cambridge University Press: Cambridge, UK, p. 66-76

Ion channel and neurotransmitter modulators as electroceutical approaches to the control of cancer
Tuszynski, J., Tilli, T. M., and Levin, M. (2017)
Current Pharmaceutical Design, 23(32): 4827-4841

Bioelectric regulation of innate immune system function in regenerating and intact Xenopus laevis
Paré, J-F., Martyniuk, C. J., and Levin, M. (2017)
NPJ Regenerative Medicine, 2: 15

Serotonergic stimulation induces nerve growth and promotes visual learning via posterior eye grafts in a vertebrate model of induced sensory plasticity
Blackiston, D., Vien, K., and Levin, M. (2017)
NPJ Regenerative Medicine, 2: 8

Discovering novel phenotypes with automatically inferred dynamic models: partial melanocyte conversion in Xenopus
Lobo, D., Lobikin, M., and Levin, M. (2017)
Scientific Reports, 7: 41339

Endogenous Bioelectric Signaling Networks: Exploiting Voltage Gradients for Control of Growth and Form
Levin, M., Pezzulo, G., and Finkelstein, J. M. (2017)
Annual Review of Biomedical Engineering, 19: 353-87

Bioelectrical coordination of cell activity toward anatomical target states: an engineering perspective on regeneration
Herrera-Rincon, C., Guay, J., and Levin, M. (2016)
Chapter 4 in D. Gardiner (Ed.), Regenerative Engineering and Developmental Biology: Principles and Applications, CRC Press: Boca Raton, FL, p. 55-112

A Tunable Silk Hydrogel Device for Studying Limb Regeneration in Adult Xenopus laevis
Golding, A., Guay, J. A., Herrera-Rincon, C., Levin, M., and Kaplan, D. L. (2016)
PLoS One, 11(6): e0155618

Computational discovery and in vivo validation of hnf4 as a regulatory gene in planarian re-generation
Lobo, D., Morokuma, J., and Levin, M. (2016)
Bioinformatics, 32(17): 2681-2685

Bioelectric signaling via potassium channels: a mechanism for craniofacial dysmorphogenesis in KCNJ2-associated Andersen-Tawil Syndrome
Adams, D. S., Uzel, S. G. M., Akagi, J., Wlodkowic, D., Andreeva, V., Yelick, P. C., Devitt-Lee, A., Paré, J-F., and  Levin, M. (2016)
Journal of Physiology, 594(12): 3245-3270

Use of genetically encoded, light-gated ion translocators to control tumorigenesis
Chernet, B. T., Adams, D. S., Lobikin, M., and Levin, M. (2016)
Oncotarget, 7(15): 19575-19588

Bioelectric modulation of macrophage polarization
Li, C., Levin, M., and Kaplan, D. (2016)
Scientific Reports, 6: 21044

Comparison of the depolarization response of human mesenchymal stem cells from different donors
Sundelacruz, S., Levin M., and Kaplan, D. L. (2015)
Scientific Reports, 5: 18279

Gap junctional blockade stochastically induces different species-specific head anatomies in genetically wild-type Girardia dorotocephala flatworms
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)
International Journal of Molecular Sciences, 16(11): 27865–27896

Serotonergic regulation of melanocyte conversion: A bioelectrically regulated network for stochastic all-or-none hyperpigmentation
Lobikin, M., Lobo, D., Blackiston, D. J., Martyniuk, C. J., Tkachenko, E., and Levin, M. (2015)
Science Signaling, 8(397): ra99

Molecular bioelectricity: how endogenous voltage potentials control cell behavior and
instruct pattern regulation in vivo
Levin, M. (2014)
Molecular Biology of the Cell, 25(24): 3835-3850

Membrane potential depolarization causes alterations in neuron arrangement and connectivity in cocultures
Özkucur, N., Quinn, K. P., Pang, J. C., Du, C., Georgakoudi, I., Miller, E., Levin, M., and Kaplan, D. L. (2015)
Brain and Behavior, 5(1): 24-38

Endogenous gradients of resting potential instructively pattern embryonic neural tissue via Notch signaling and regulation of proliferation
Pai, V., Lemire, J. M., Paré, J-F., Lin, G., Chen, Y., and Levin, M. (2015)
Journal of Neuroscience, 35(10): 4366-4385

Inferring regulatory networks from experimental morphological phenotypes: a computational method reverse-engineers planarian regeneration
Lobo, D., and Levin, M. (2015)
PLoS Computational Biology, 11(6): e1004295

A novel method for inducing nerve growth via modulation of host resting potential
Blackiston, D., Anderson, G. M., Rahman, N., Bieck, C., and Levin, M. (2015)
Neurotherapeutics, 12(1): 170-184

Transmembrane voltage potential of somatic cells controls oncogene-mediated tumorigenesis at long-range
Chernet, B., and Levin, M. (2014)
Oncotarget, 5(10): 3287-3306

Depolarization Alters Phenotype, Maintains Plasticity of Predifferentiated Mesenchymal Stem Cells
Sundelacruz, S., Levin, M., and Kaplan, D. L. (2013)
Tissue Engineering Part A, 19(17-18): 1889-1908

Transmembrane voltage potential is an essential cellular parameter for the detection and control of tumor development
Chernet, B. T., and Levin, M. (2013)
Disease Models & Mechanisms, 6(3): 595-607

Transmembrane voltage potential controls embryonic eye patterning in Xenopus laevis
Pai, V., Aw, S., Shomrat, T., Lemire, J. M., and Levin, M. (2012)
Development, 139(2): 313-323

The wisdom of the body: future techniques and approaches to morphogenetic fields in regenerative medicine, developmental biology, and cancer
Levin, M. (2011)
Regenerative Medicine, 6(6): 667-673

Patterned femtosecond-laser ablation of Xenopus laevis melanocytes for studies of cell migration, wound repair, and developmental processes
Mondia, J. P., Adams, D. S., Orendorff, R. D., Levin, M., and Omenetto, F. (2011)
Biomedical Optics Express, 2(8): 2383-2391

Long-distance signals are required for morphogenesis of the regenerating Xenopus tadpole tail
Mondia, J. P., Levin, M., Omenetto, F. G., Orendorff, R. D., Branch, M. R., and Adams, D. S. (2011)
PLoS One, 6(9): e24953

The H+ Vacuolar ATPase Maintains Neural Stem Cells in the Developing Mouse Cortex
Lange, C., Prenninger, S., Knuckles, P., Taylor V., Levin, M., and Calegari, F. (2011)
Stem Cells and Development, 20(5): 1-8

A second-generation device for automated training and quantitative behavior analyses of molecularly-tractable model organisms
Blackiston, D., Shomrat, T., Nicolas, C. L., Granata, C., and Levin, M. (2010)
PLoS One, 5(12): e14370

Induction of vertebrate regeneration by a transient sodium current
Tseng, A-S., Beane, W. S., Lemire, J. M., Masi, A., and Levin, M. (2010)
Journal of Neuroscience, 30(39): 13192-13200

Long-range Neural and Gap Junction Protein-mediated Cues Control Polarity During Planarian Regeneration
Oviedo, N. J., Morokuma, J., Walentek, P., Kema, I. P., Gu, M. B., Ahn, J. M., Hwang, J. S., Gojobori, T. and Levin, M. (2010)
Developmental Biology, 339(1): 188-199

Bioelectric controls of cell proliferation: ion channels, membrane voltage, and the cell cycle
Blackiston, D. J., K. McLaughlin, and Levin, M. (2009)
Cell Cycle, 8(21): 3519-3528

Bioelectric mechanisms in regeneration: Unique aspects and future perspectives
Levin, M. (2009)
Seminars in Cell and Developmental Biology, 20(5): 543-556

Errors of Geometry: regeneration in a broader perspective
Levin, M. (2009)
Seminars in Cell and Developmental Biology, 20(6): 643-645

Role of membrane potential in the regulation of cell proliferation and differentiation
Levin, M., Sundelacruz, S., Levin M., and Kaplan, D. L. (2009)
Stem Cell Reviews, 5(3): 231-246

Tail regeneration in Xenopus laevis as a model for understanding tissue repair
Tseng, A-S., and Levin, M. (2008)
Journal of Dental Research, 87(9): 806-816

Modulation of potassium channel confers a hyper-proliferative invasive phenotype on embryonic stem cells
Morokuma, J., Blackiston, D., Adams, D. S., Seebohm, G., Trimmer, B., and Levin, M. (2008)
Proceedings of the National Academy of Science, 105(43): 16608-16613

Membrane potential controls adipogenic and osteogenic differentiation of mesenchymal stem cell
Sundelacruz, S., Levin, M., and Kaplan, D. L. (2008)
PLoS One, 3(11): e3737

Apoptosis is required during early stages of tail regeneration in Xenopus laevis
Tseng, A-S., Adams, D. S., Qiu, D., Koustubhan, P., and Levin, M. (2007)
Developmental Biology, 301(1): 62-69

H+ Pump-dependent changes in membrane voltage are an early mechanism necessary and sufficient to induce Xenopus tail regeneration
Adams, D. S., Masi, A., and Levin, M. (2007)
Development, 134(7): 1323-1335

smedxin-11 is a Planarian Stem Cell Gap Junction Gene Required for Regeneration and Homeostasis
Oviedo, N. J., and Levin, M. (2007)
Development, 134(17): 3121-3131

Inverse Drug Screens: a rapid and inexpensive method for implicating molecular targets
Adams, D. S., and Levin, M. (2006)
Genesis, 44(11): 530-540