Cited by 166Planarian Biology and ElectrostimulationDevelopmental Biology and Gene RegulationCancer Cells and Metastasis

The DOI matches its Crossref record; 188 of the 189 references it cites were found in a registry or an index, and 1 are not checked yet.

Resting potential, oncogene-induced tumorigenesis, and metastasis: the bioelectric basis of cancer in vivo

Open access

Lobikin, Maria, Chernet, Brook, Lobo, Daniel, Levin, Michael·2012·Physical Biology

DOI 10.1088/1478-3975/9/6/065002PMC PMC3528107

Open this paper in CoChat — free account

Abstract

Cancer may result from localized failure of instructive cues that normally orchestrate cell behaviors toward the patterning needs of the organism. Steady-state gradients of transmembrane voltage (V(mem)) in non-neural cells are instructive, epigenetic signals that regulate pattern formation during embryogenesis and morphostatic repair. Here, we review molecular data on the role of bioelectric cues in cancer and present new findings in the Xenopus laevis model on how the microenvironment's biophysical properties contribute to cancer in vivo. First, we investigated the melanoma-like phenotype arising from serotonergic signaling by 'instructor' cells-a cell population that is able to induce a metastatic phenotype in normal melanocytes. We show that when these instructor cells are depolarized, blood vessel patterning is disrupted in addition to the metastatic phenotype induced in melanocytes. Surprisingly, very few instructor cells need to be depolarized for the hyperpigmentation phenotype to occur; we present a model of antagonistic signaling by serotonin receptors that explains the unusual all-or-none nature of this effect. In addition to the body-wide depolarization-induced metastatic phenotype, we investigated the bioelectrical properties of tumor-like structures induced by canonical oncogenes and cancer-causing compounds. Exposure to carcinogen 4-nitroquinoline 1-oxide (4NQO) induces localized tumors, but has a broad (and variable) effect on the bioelectric properties of the whole body. Tumors induced by oncogenes show aberrantly high sodium content, representing a non-invasive diagnostic modality. Importantly, depolarized transmembrane potential is not only a marker of cancer but is functionally instructive: susceptibility to oncogene-induced tumorigenesis is significantly reduced by forced prior expression of hyperpolarizing ion channels. Importantly, the same effect can be achieved by pharmacological manipulation of endogenous chloride channels, suggesting a strategy for cancer suppression that does not require gene therapy. Together, these data extend our understanding of the recently demonstrated role of transmembrane potential in tumor formation and metastatic cell behavior. V(mem) is an important non-genetic biophysical aspect of the microenvironment that regulates the balance between normally patterned growth and carcinogenesis.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1088/1478-3975/9/6/065002

Cites

188 of 189 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

1 retracted

Retracted: Overexpression HERG K+ channel gene mediates cell‐growth signals on activation of oncoproteins SP1 and NF‐κB and inactivation of tumor suppressor Nkx3.1
Lin, H., Xiao, J., Luo, X., Wang, H., Gao, H., Yang, B., & Wang, Z. (2007) · Journal of Cellular Physiology · doi:10.1002/jcp.21015 · Cited by 33
Retracted
Hallmarks of Cancer: The Next Generation
Hanahan, D., & Weinberg, R. A. (2011) · Cell · doi:10.1016/j.cell.2011.02.013 · Cited by 66,590
Normal Table of Xenopus Laevis (Daudin)
Nieuwkoop, P. D., & Faber, J. (1958) · Copeia · doi:10.2307/1439568 · Cited by 4,542
A review of central 5-HT receptors and their function
Barnes, N. M., & Sharp, T. (1999) · Neuropharmacology · doi:10.1016/s0028-3908(99)00010-6 · Cited by 3,211
Normal table of Xenopus laevis (Daudin)
Gurdon, J. B. (1995) · Trends in Genetics · doi:10.1016/s0168-9525(00)89129-5 · Cited by 2,888
Putting tumours in context
Bissell, M. J., & Radisky, D. (2001) · Nature Reviews Cancer · doi:10.1038/35094059 · Cited by 2,180
Vascular Channel Formation by Human Melanoma Cells in Vivo and in Vitro: Vasculogenic Mimicry
Maniotis, A. J., Folberg, R., Hess, A. R., Seftor, E. A., Gardner, L. M. G., Pe’er, J., Trent, J. M., Meltzer, P. S., & Hendrix, M. J. C. (1999) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)65173-5 · Cited by 2,049
Why don't we get more cancer? A proposed role of the microenvironment in restraining cancer progression
Bissell, M. J., & Hines, W. C. (2011) · Nature Medicine · doi:10.1038/nm.2328 · Cited by 1,584
Early development of Xenopus laevis : a laboratory manual
Sive, H. L., Grainger, R. M., & Harland, R. M. (2000) · Medical Entomology and Zoology · Cited by 1,222
Electrical signals control wound healing through phosphatidylinositol-3-OH kinase-γ and PTEN
Zhao, M., Song, B., Pu, J., Wada, T., Reid, B., Tai, G., Wang, F., Guo, A., Walczysko, P., Gu, Y., et al. (2006) · Nature · doi:10.1038/nature04925 · Cited by 1,172
Controlling Cell Behavior Electrically: Current Views and Future Potential
McCaig, C., Rajnicek, A. M., Song, B., & Zhao, M. (2005) · Physiological Reviews · doi:10.1152/physrev.00020.2004 · Cited by 1,098
Vasculogenic mimicry and tumour-cell plasticity: lessons from melanoma
Hendrix, M. J. C., Seftor, E. A., Hess, A. R., & Seftor, R. E. B. (2003) · Nature reviews. Cancer · doi:10.1038/nrc1092 · Cited by 846
A positive-feedback-based bistable ‘memory module’ that governs a cell fate decision.
Xiong, W., & Ferrell, J. E. (2003) · Nature · doi:10.1038/nature02089 · Cited by 741
Activation of the transcription factor Gli1 and the Sonic hedgehog signalling pathway in skin tumours
Dahmane, N., Lee, J. D., Robins, P., Heller, P., & Altaba, A. R. I. (1997) · Nature · doi:10.1038/39918 · Cited by 639
Cancer attractors: A systems view of tumors from a gene network dynamics and developmental perspective
Huang, S., Ernberg, I. T., & Kauffman, S. A. (2009) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2009.07.003 · Cited by 572
Context, tissue plasticity, and cancer
Bissell, M. J., & LaBarge, M. A. (2005) · Cancer Cell · doi:10.1016/j.ccr.2004.12.013 · Cited by 517
Cancer cell-derived microvesicles induce transformation by transferring tissue transglutaminase and fibronectin to recipient cells
Antonyak, M. A., Li, B., Boroughs, L. K., Johnson, J. L., Druso, J. E., Bryant, K. L., Holowka, D. A., & Cerione, R. A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1017667108 · Cited by 514
Role of membrane potential in the regulation of cell proliferation and differentiation
Sundelacruz, S., Levin, M., & Kaplan, D. L. (2009) · Stem Cell Reviews and Reports · doi:10.1007/s12015-009-9080-2 · Cited by 489
Voltage-Gated Sodium Channel Expression and Potentiation of Human Breast Cancer Metastasis
Fraser, S. P., Diss, J. K. J., Chioni, A.-M., Mycielska, M. E., Pan, H., Yamaci, R. F., Pani, F., Siwy, Z., Krasowska, M., Grzywna, Z., et al. (2005) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-05-0327 · Cited by 481
Serotonylation of small GTPases is a signal transduction pathway that triggers platelet α-granule release
Walther, D. J., Peter, J.-U., Winter, S., Höltje, M., Paulmann, N., Grohmann, M., Vowinckel, J., Alamo-Bethencourt, V., Wilhelm, C. S., Ahnert-Hilger, G., et al. (2003) · Cell · doi:10.1016/s0092-8674(03)01014-6 · Cited by 475
Reprogramming metastatic tumour cells with embryonic microenvironments
Hendrix, M. J. C., Seftor, E. A., Seftor, R. E. B., Kasemeier‐Kulesa, J. C., Kulesa, P. M., & Postovit, L.-M. M. (2007) · Nature reviews. Cancer · doi:10.1038/nrc2108 · Cited by 475
Bioelectric controls of cell proliferation: Ion channels, membrane voltage and the cell cycle
Blackiston, D. J., McLaughlin, K. A., & Levin, M. (2009) · Cell Cycle · doi:10.4161/cc.8.21.9888 · Cited by 468
Ion channels and the hallmarks of cancer
Prevarskaya, N., Skryma, R., & Shuba, Y. (2010) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2010.01.005 · Cited by 448
Oncogenic potential of EAG K+ channels
Pardo, L. A., del Camino, D., Sánchez, A., Alves, F., Brüggemann, A., Beckh, S., & Stühmer, W. (1999) · The EMBO Journal · doi:10.1093/emboj/18.20.5540 · Cited by 446
Intracellular Serotonin Modulates Insulin Secretion from Pancreatic β-Cells by Protein Serotonylation
Paulmann, N., Grohmann, M., Voigt, J.-P., Bert, B., Vowinckel, J., Bader, M., Skelin, M., Jevšek, M., Fink, H., Rupnik, M., et al. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000229 · Cited by 404
Asymmetries in H+/K+-ATPase and Cell Membrane Potentials Comprise a Very Early Step in Left-Right Patterning
Levin, M. G., Thorlin, T., Robinson, K. R., Nogi, T., & Mercola, M. A. (2002) · Cell · doi:10.1016/s0092-8674(02)00939-x · Cited by 397
GLI transcription factors: Mediators of oncogenic Hedgehog signalling
Kasper, M., Regl, G., Frischauf, A., & Aberger, F. (2006) · European Journal of Cancer · doi:10.1016/j.ejca.2005.08.039 · Cited by 378
Increased sodium ion influx is necessary to initiate rat hepatocyte proliferation
Koch, K. S., & Leffert, H. L. (1979) · Cell · doi:10.1016/0092-8674(79)90364-7 · Cited by 373
Neurotransmitters as early signals for central nervous system development
Nguyen, L., Rigo, J., Rocher, V., Belachew, S. M., Malgrange, B., Rogister, B., Leprince, P., & Moonen, G. (2001) · Cell and Tissue Research · doi:10.1007/s004410000343 · Cited by 371
Bistability in cell signaling: How to make continuous processes discontinuous, and reversible processes irreversible
Ferrell, J. E., & Xiong, W. (2001) · Chaos An Interdisciplinary Journal of Nonlinear Science · doi:10.1063/1.1349894 · Cited by 366
The tissue organization field theory of cancer: A testable replacement for the somatic mutation theory
Soto, A. M., & Sonnenschein, C. (2011) · BioEssays · doi:10.1002/bies.201100025 · Cited by 353
Stimulated platelets use serotonin to enhance their retention of procoagulant proteins on the cell surface
Dale, G. L., Friese, P., Batár, P., Hamilton, S. F., Reed, G. L., Jackson, K. W., Clemetson, K. J., & Alberio, L. (2002) · Nature · doi:10.1038/415175a · Cited by 338
Electrical dimensions in cell science
McCaig, C., Song, B., & Rajnicek, A. M. (2009) · Journal of Cell Science · doi:10.1242/jcs.023564 · Cited by 325
Bioelectrical impedance phase angle in clinical practice: implications for prognosis in advanced colorectal cancer
Gupta, D., Lammersfeld, C. A., Burrows, J., Dahlk, S., Vashi, P. G., Grutsch, J. F., Hoffman, S., & Lis, C. G. (2004) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/80.6.1634 · Cited by 322
The somatic mutation theory of cancer: growing problems with the paradigm?
Soto, A. M., & Sonnenschein, C. (2004) · BioEssays · doi:10.1002/bies.20087 · Cited by 306
Apoptosis-induced compensatory proliferation. The Cell is dead. Long live the Cell!
Fan, Y., & Bergmann, A. (2008) · Trends in Cell Biology · doi:10.1016/j.tcb.2008.08.001 · Cited by 304
A causal role for ERG in neoplastic transformation of prostate epithelium
Klezovitch, O., Risk, M. C., Coleman, I. M., Lucas, J. M., Null, M., True, L. D., Nelson, P. S., & Vasioukhin, V. I. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0711711105 · Cited by 302
Skin Cancer Identification Using Multifrequency Electrical Impedance—A Potential Screening Tool
Åberg, P., Nicander, I., Hansson, J., Geladi, P. L. M., Holmgren, U., & Ollmar, S. (2004) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2004.836523 · Cited by 301
Can cancer be reversed by engineering the tumor microenvironment?
Ingber, D. E. (2008) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2008.03.016 · Cited by 297
Voltage-Gated Potassium Channels in Cell Proliferation
Pardo, L. A. (2004) · Physiology · doi:10.1152/physiol.00011.2004 · Cited by 297
The fate of human malignant melanoma cells transplanted into zebrafish embryos: Assessment of migration and cell division in the absence of tumor formation
Lee, L. M. J., Seftor, E. A., Bonde, G., Cornell, R. A., & Hendrix, M. J. C. (2005) · Developmental Dynamics · doi:10.1002/dvdy.20471 · Cited by 296
High incidence of spontaneous and chemically induced liver tumors in mice deficient for connexin32
Temme, A., Buchmann, A., Gabriel, H., Nelles, E., Schwarz, M., & Willecke, K. (1997) · Current Biology · doi:10.1016/s0960-9822(06)00302-2 · Cited by 287
Targeting Ion Channels in Cancer: A Novel Frontier in Antineoplastic Therapy
Arcangeli, A., Crociani, O., Lastraioli, E., Masi, A., Pillozzi, S., & Becchetti, A. (2008) · Current Medicinal Chemistry · doi:10.2174/092986709787002835 · Cited by 284
Roles of K + channels in regulating tumour cell proliferation and apoptosis
Wang, Z. (2004) · Pfl�gers Archiv European Journal of Physiology · doi:10.1007/s00424-004-1258-5 · Cited by 280
Serotonin and serotonin-like substances as regulators of early embryogenesis and morphogenesis
Buznikov, G. A., Lambert, H. W., & Lauder, J. M. (2001) · Cell and Tissue Research · doi:10.1007/s004410100408 · Cited by 274
H+ pump-dependent changes in membrane voltage are an early mechanism necessary and sufficient to induce Xenopus tail regeneration
Adams, D. S., Masi, A., & Levin, M. G. (2007) · Development · doi:10.1242/dev.02812 · Cited by 268
Early, H+-V-ATPase-dependent proton flux is necessary for consistent left-right patterning of non-mammalian vertebrates
Adams, D. S., Robinson, K. R., Fukumoto, T., Yuan, S., Albertson, R. C., Yelick, P. C., Kuo, L. E. Y., McSweeney, M., & Levin, M. G. (2006) · Development · doi:10.1242/dev.02341 · Cited by 267
Genomic amplification and oncogenic properties of the KCNK9 potassium channel gene
Mu, D., Chen, L., Zhang, X., See, L.-H., Koch, C. M., Yen, C., Tong, J. J., Spiegel, L. A., Nguyen, K. C. Q., Servoss, A., et al. (2003) · Cancer Cell · doi:10.1016/s1535-6108(03)00054-0 · Cited by 263
Untitled work
(1998) · PubMed · Cited by 262
Untitled work
(1980) · PubMed · Cited by 257
A new role for an old molecule: serotonin as a mitogen
Fanburg, B. L., & Lee, S. L. (1997) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.1997.272.5.l795 · Cited by 255
Voltage-Gated Na+ Channel SCN5A Is a Key Regulator of a Gene Transcriptional Network That Controls Colon Cancer Invasion
House, C. D., Vaske, C. J., Schwartz, A. M., Obias, V., Frank, B. C., Luu, T. V., Sarvazyan, N. A., Irby, R., Strausberg, R. L., Hales, T. G., et al. (2010) · Cancer Research · doi:10.1158/0008-5472.can-10-1169 · Cited by 254
Bioelectric Fields and Growth
LUND, E. J. (1947) · Soil Science · doi:10.1097/00010694-194709000-00010 · Cited by 249
Membrane Potential Controls Adipogenic and Osteogenic Differentiation of Mesenchymal Stem Cells
Sundelacruz, S., Levin, M., & Kaplan, D. L. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003737 · Cited by 249
Serotonin Signaling Is a Very Early Step in Patterning of the Left-Right Axis in Chick and Frog Embryos
Fukumoto, T., Kema, I. P., & Levin, M. G. (2005) · Current Biology · doi:10.1016/j.cub.2005.03.044 · Cited by 249
Molecular bioelectricity in developmental biology: New tools and recent discoveries
Levin, M. G. (2012) · BioEssays · doi:10.1002/bies.201100136 · Cited by 248
Reprogramming metastatic melanoma cells to assume a neural crest cell-like phenotype in an embryonic microenvironment
Kulesa, P. M., Kasemeier‐Kulesa, J. C., Teddy, J. M., Margaryan, N. V., Seftor, E. A., Seftor, R. E. B., & Hendrix, M. J. C. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506977103 · Cited by 245
Membrane potentials and sodium channels: Hypotheses for growth regulation and cancer formation based on changes in sodium channels and gap junctions
Binggeli, R., & Weinstein, R. C. (1986) · Journal of Theoretical Biology · doi:10.1016/s0022-5193(86)80209-0 · Cited by 239
A novel inward‐rectifying K+ current with a cell‐cycle dependence governs the resting potential of mammalian neuroblastoma cells.
Arcangeli, A., Bianchi, L. K., Becchetti, A., Faravelli, L., Coronnello, M., Mini, E., Olivotto, M., & Wanke, E. (1995) · The Journal of Physiology · doi:10.1113/jphysiol.1995.sp021065 · Cited by 239
Functional activity of serotoninergic and melatoninergic systems expressed in the skin
Slominski, A. T., Pisarchik, A. V., Zbytek, B., Tobin, D. J., Kauser, S., & Wortsman, J. (2003) · Journal of Cellular Physiology · doi:10.1002/jcp.10287 · Cited by 234
Untitled work
(2002) · PubMed · Cited by 228
Bioelectric mechanisms in regeneration: Unique aspects and future perspectives
Levin, M. G. (2009) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2009.04.013 · Cited by 222
Cancer as a dynamic developmental disorder.
Rubin, H. (1985) · PubMed · Cited by 217
herg1 Gene and HERG1 Protein Are Overexpressed in Colorectal Cancers and Regulate Cell Invasion of Tumor Cells
Lastraioli, E., Guasti, L., Crociani, O., Polvani, S., Hofmann, G., Witchel, H. J., Bencini, L., Calistri, M., Messerini, L., Scatizzi, M., et al. (2004) · Cancer Research · doi:10.1158/0008-5472.can-03-2360 · Cited by 213
Stimulation of malignant growth in rodents by antidepressant drugs at clinically relevant doses.
Brandes, L. J., Arron, R. J., Bogdanovic, R. P., TONG, J. J., Zaborniak, C. L., Hogg, G. R., Warrington, R. C., Fang, W., & LaBella, F. S. (1992) · PubMed · Cited by 211
Ivermectin, an Unconventional Agonist of the Glycine Receptor Chloride Channel
Shan, Q., Haddrill, J. L., & Lynch, J. W. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m011264200 · Cited by 211
Induction of Mitosis in Mature Neurons in Central Nervous System by Sustained Depolarization
Cone, C. D., & Cone, C. M. (1976) · Science · doi:10.1126/science.56781 · Cited by 208
Digitalis-Induced Signaling by Na+/K+-ATPase in Human Breast Cancer Cells
Kometiani, P., Liu, L., & Askari, A. (2005) · Molecular Pharmacology · doi:10.1124/mol.104.007302 · Cited by 208
Gap Junctions Are Involved in the Early Generation of Left–Right Asymmetry
Levin, M. G., & Mercola, M. A. (1998) · Developmental Biology · doi:10.1006/dbio.1998.9024 · Cited by 204
Vesicular monoamine transporters: Structure‐function, pharmacology, and medicinal chemistry
Wimalasena, K. (2010) · Medicinal Research Reviews · doi:10.1002/med.20187 · Cited by 199
Induction of Vertebrate Regeneration by a Transient Sodium Current
Tseng, A.-S. K., Beane, W. S., Lemire, J. M., Masi, A., & Levin, M. G. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3315-10.2010 · Cited by 199
SLC5A8 (SMCT1)-mediated transport of butyrate forms the basis for the tumor suppressive function of the transporter
Gupta, N., Martin, P. M., Prasad, P. D., & Ganapathy, V. (2005) · Life Sciences · doi:10.1016/j.lfs.2005.10.028 · Cited by 196
A Chemical Genetics Approach Reveals H,K-ATPase-Mediated Membrane Voltage Is Required for Planarian Head Regeneration
Beane, W. S., Morokuma, J., Adams, D. S., & Levin, M. G. (2011) · Chemistry & Biology · doi:10.1016/j.chembiol.2010.11.012 · Cited by 195
Increased pH and tumorigenicity of fibroblasts expressing a yeast proton pump
Perona, R., & Serrano, R. (1988) · Nature · doi:10.1038/334438a0 · Cited by 194
Transmembrane voltage potential controls embryonic eye patterning in Xenopus laevis
Pai, V. P., Aw, S. S., Shomrat, T., Lemire, J. M., & Levin, M. G. (2011) · Development · doi:10.1242/dev.073759 · Cited by 191
Ion channels and transporters in cancer. 1. Ion channels and cell proliferation in cancer
Becchetti, A. (2011) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00047.2011 · Cited by 187
Heat shock-inducible Cre/Lox approaches to induce diverse types of tumors and hyperplasia in transgenic zebrafish
Le, X., Langenau, D. M., Keefe, M. D., Kutok, J. L., Neuberg, D. S., & Zon, L. I. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0611302104 · Cited by 186
5-Hydroxytryptamine 2B receptor regulates cell-cycle progression: Cross-talk with tyrosine kinase pathways
Nebigil, C. G., Launay, J., Hickel, P., Tournois, C., & Maroteaux, L. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.050282397 · Cited by 184
Ivermectin in human medicine
Ottesen, E. A., & Campbell, W. C. (1994) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/34.2.195 · Cited by 181
Membrane potential bistability is controlled by the hyperpolarization‐activated current IH in rat cerebellar Purkinje neurons in vitro
Williams, S. R., Christensen, S. R., Stuart, G. J., & Häusser, M. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2001.013136 · Cited by 181
Membrane transduction mechanisms
Cone, R. A., & Dowling, J. E. (1979) · Raven Press eBooks · Cited by 175
MONOVALENT ION FLUXES AND THE CONTROL OF CELL PROLIFERATION IN CULTURED FIBROBLASTS
Rozengurt, E., & Mendoza, S. A. (1980) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1980.tb15977.x · Cited by 175
Endogenous voltage gradients as mediators of cell-cell communication: strategies for investigating bioelectrical signals during pattern formation
Adams, D. S., & Levin, M. G. (2012) · Cell and Tissue Research · doi:10.1007/s00441-012-1329-4 · Cited by 173
Oncogenic potential of TASK3 ( Kcnk9 ) depends on K + channel function
Pei, L., Wiser, O., Slavin, A., Mu, D., Powers, S., Jan, L. Y., & Hoey, T. C. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1232448100 · Cited by 172
Ether a go-go Potassium Channels as Human Cervical Cancer Markers
Farias, L. M. B., Ocaña, D. B., Díaz, L., Larrea, F., Avila-Chávez, E., Cadena, A., Hinojosa, L. M., Lara, G., Villanueva, L. A., Vargas, C., et al. (2004) · Cancer Research · doi:10.1158/0008-5472.can-04-1204 · Cited by 164
Serotonin and fluoxetine modulate bone cell function in vitro
Gustafsson, B. I., Thommesen, L., Stunes, A. K., Tømmerås, K. A., Westbroek, I., Waldum, H. L., Slørdahl, K., Tamburstuen, M. V., Reseland, J. E., & Syversen, U. (2006) · Journal of Cellular Biochemistry · doi:10.1002/jcb.20734 · Cited by 157
A potential novel marker for human prostate cancer: voltage-gated sodium channel expression in vivo
Diss, J. K. J., Stewart, D., Pani, F., Foster, C. S., Walker, M. M., Patel, A. S., & Djamgoz, M. B. A. (2005) · Prostate Cancer and Prostatic Diseases · doi:10.1038/sj.pcan.4500796 · Cited by 156
Altered serotonin physiology in human breast cancers favors paradoxical growth and cell survival
Pai, V. P., Marshall, A. M., Hernandez, L. L., Buckley, A. R., & Horseman, N. D. (2009) · Breast Cancer Research · doi:10.1186/bcr2448 · Cited by 155
Expression of serotonin receptors and role of serotonin in human prostate cancer tissue and cell lines
Dizeyi, N., Bjartell, A. S., Nilsson, E., Hansson, J., Gadaleanu, V., Cross, N. A., & Abrahamsson, P. (2004) · The Prostate · doi:10.1002/pros.10374 · Cited by 154
EGF receptor signalling is essential for electric-field-directed migration of breast cancer cells
Pu, J., McCaig, C., Cao, L., Zhao, Z., Segall, J. E., & Zhao, M. (2007) · Journal of Cell Science · doi:10.1242/jcs.002774 · Cited by 149
Endothelium-derived factors as paracrine mediators of prostate cancer progression
Pirtskhalaishvili, G., & Nelson, J. B. (2000) · The Prostate · doi:10.1002/1097-0045(20000615)44:1 · Cited by 145
Blockade of central 5-hydroxytryptamine receptors by methiothepin
Monachon, M. A., Burkard, W. P., Jalfre, M., & Haefely, W. E. (1972) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/bf00501854 · Cited by 143
Serotonin stimulates mitogen-activated protein kinase activity through the formation of superoxide anion
Lee, S.-L., Wang, W., Finlay, G. A., & Fanburg, B. L. (1999) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.1999.277.2.l282 · Cited by 141
Mammary gland homeostasis employs serotonergic regulation of epithelial tight junctions
Stull, M. A., Pai, V. P., Vomachka, A. J., Marshall, A. M., Jacob, G. A., & Horseman, N. D. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0708136104 · Cited by 139
Of Minds and Embryos: Left-Right Asymmetry and the Serotonergic Controls of Pre-Neural Morphogenesis
Levin, M. G., Buznikov, G. A., & Lauder, J. M. (2006) · Developmental Neuroscience · doi:10.1159/000091915 · Cited by 137
Neuroendocrine activity of the melanocyte
Slominski, A. T. (2009) · Experimental Dermatology · doi:10.1111/j.1600-0625.2009.00892.x · Cited by 128
Molecular pharmacology of voltage-gated sodium channel expression in metastatic disease: Clinical potential of neonatal Nav1.5 in breast cancer
Onkal, R., & Djamgoz, M. B. A. (2009) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2009.08.040 · Cited by 127
Transmembrane potential of GlyCl-expressing instructor cells induces a neoplastic-like conversion of melanocytes via a serotonergic pathway
Blackiston, D. J., Adams, D. S., Lemire, J. M., Lobikin, M., & Levin, M. G. (2010) · Disease Models & Mechanisms · doi:10.1242/dmm.005561 · Cited by 127
The dominance of the microenvironment in breast and ovarian cancer
Roskelley, C. D., & Bissell, M. J. (2002) · Seminars in Cancer Biology · doi:10.1006/scbi.2001.0417 · Cited by 126
Morphogens, morphostats, microarchitecture and malignancy
Potter, J. D. (2007) · Nature reviews. Cancer · doi:10.1038/nrc2146 · Cited by 125
Cancer and the Theory of Organisers
Waddington, C. H. (1935) · Nature · doi:10.1038/135606a0 · Cited by 124
Expression and Role of hERG Channels in Cancer Cells
Arcangeli, A. (2005) · Novartis Foundation Symposia · doi:10.1002/047002142x.ch17 · Cited by 123
THE ROLE OF THE SURFACE ELECTRICAL TRANSMEMBRANE POTENTIAL IN NORMAL AND MALIGNANT MITOGENESIS
Cone, C. D. (1974) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1974.tb26808.x · Cited by 120
Modulation of potassium channel function confers a hyperproliferative invasive phenotype on embryonic stem cells
Morokuma, J., Blackiston, D. J., Adams, D. S., Seebohm, G., Trimmer, B. A., & Levin, M. G. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0808328105 · Cited by 118
Measuring Resting Membrane Potential Using the Fluorescent Voltage Reporters DiBAC4(3) and CC2-DMPEPreprint
Adams, D. S., & Levin, M. G. (2012) · Cold Spring Harbor Protocols · doi:10.1101/pdb.prot067702 · Cited by 117
An Emerging Role for Voltage-Gated Na+ Channels in Cellular Migration: Regulation of Central Nervous System Development and Potentiation of Invasive Cancers
Brackenbury, W. J., Djamgoz, M. B. A., & Isom, L. L. (2008) · The Neuroscientist · doi:10.1177/1073858408320293 · Cited by 116
P53 activity is essential for normal development in Xenopus
Wallingford, J. B., Seufert, D. W., Virta, V. C., & Vize, P. D. (1997) · Current Biology · doi:10.1016/s0960-9822(06)00333-2 · Cited by 110
Identification of Ether à Go-Go and Calcium-Activated Potassium Channels in Human Melanoma Cells
Meyer, R., Schönherr, R., Gavrilova-Ruch, O., Wohlrab, W., & Heinemann, S. H. (1999) · The Journal of Membrane Biology · doi:10.1007/s002329900563 · Cited by 109
Activity‐dependent regulation of voltage‐gated Na+ channel expression in Mat‐LyLu rat prostate cancer cell line
Brackenbury, W. J., & Djamgoz, M. B. A. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2006.106906 · Cited by 107
ClC3 Is a Critical Regulator of the Cell Cycle in Normal and Malignant Glial Cells
Habela, C. W., Olsen, M. L., & Sontheimer, H. W. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1897-08.2008 · Cited by 107
Reprogramming multipotent tumor cells with the embryonic neural crest microenvironment
Kasemeier‐Kulesa, J. C., Teddy, J. M., Postovit, L.-M. M., Seftor, E. A., Seftor, R. E. B., Hendrix, M. J. C., & Kulesa, P. M. (2008) · Developmental Dynamics · doi:10.1002/dvdy.21613 · Cited by 107
Beyond the Oncogene Paradigm: Understanding Complexity in Cancerogenesis
Bizzarri, M., Cucina, A., Conti, F., & D’Anselmi, F. (2008) · Acta Biotheoretica · doi:10.1007/s10441-008-9047-8 · Cited by 105
Molecular diversity and function of voltage-gated (Kv) potassium channels in epithelial cells
O’Grady, S. M., & Lee, S. Y. (2005) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2005.04.002 · Cited by 105
Untitled work
(1983) · PubMed · Cited by 99
Serotonin-transporter mediated efflux: A pharmacological analysis of amphetamines and non-amphetamines
Hilber, B., Scholze, P., Dorostkar, M. M., Sandtner, W., Holy, M., Boehm, S., Singer, E. A., & Sitte, H. H. (2005) · Neuropharmacology · doi:10.1016/j.neuropharm.2005.08.008 · Cited by 99
Biphasic Regulation of Mammary Epithelial Resistance by Serotonin through Activation of Multiple Pathways
Pai, V. P., & Horseman, N. D. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m802476200 · Cited by 94
Neuronal characteristics of small-cell lung cancer
Onganer, P. U., Seckl, M. J., & Djamgoz, M. B. A. (2005) · British Journal of Cancer · doi:10.1038/sj.bjc.6602857 · Cited by 94
Electrical Impedance Scanning for the Early Detection of Breast Cancer in Young Women: Preliminary Results of a Multicenter Prospective Clinical Trial
Stojadinovic, A., Nissan, A., Gallimidi, Z., Lenington, S., Logan, W. W., Zuley, M. L., Yeshaya, A., Shimonov, M., Melloul, M., Fields, S. I., et al. (2005) · Journal of Clinical Oncology · doi:10.1200/jco.2005.06.155 · Cited by 93
PACα- an optogenetic tool for in vivo manipulation of cellular cAMP levels, neurotransmitter release, and behavior in Caenorhabditis elegans
Weissenberger, S., Schultheis, C., Liewald, J. F., Erbguth, K., Nagel, G., & GOTTSCHALK, A. R. (2010) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2010.07148.x · Cited by 92
The Wisdom of the Body: Future Techniques and Approaches to Morphogenetic Fields in Regenerative Medicine, Developmental Biology and Cancer
Levin, M. G. (2011) · Regenerative Medicine · doi:10.2217/rme.11.69 · Cited by 92
The Role of Serotonin and Neurotransmitters During Craniofacial Development
Moiseiwitsch, J. (2000) · Critical Reviews in Oral Biology & Medicine · doi:10.1177/10454411000110020601 · Cited by 91
Small-cell Lung Cancer (Human): Potentiation of Endocytic Membrane Activity by Voltage-gated Na+ Channel Expression in Vitro
Onganer, P. U., & Djamgoz, M. B. A. (2005) · The Journal of Membrane Biology · doi:10.1007/s00232-005-0747-6 · Cited by 89
H,K-ATPase protein localization and Kir4.1 function reveal concordance of three axes during early determination of left–right asymmetry
Aw, S. S., Adams, D. S., Qiu, D., & Levin, M. G. (2007) · Mechanisms of Development · doi:10.1016/j.mod.2007.10.011 · Cited by 88
General Principles for Measuring Resting Membrane Potential and Ion Concentration Using Fluorescent Bioelectricity Reporters
Adams, D. S., & Levin, M. (2012) · Cold Spring Harbor Protocols · doi:10.1101/pdb.top067710 · Cited by 88
Self-citation
The serotonin transporter (SLC6A4) is present in B‐cell clones of diverse malignant origin: probing a potential antitumor target for psychotropics
Meredith, E. J., Holder, M. J., Chamba, A., Challa, A., Lee, A. D., Bunce, C. M., Drayson, M. T., Pilkington, G. J., Blakely, R., Dyer, M. J. S., et al. (2005) · The FASEB Journal · doi:10.1096/fj.04-3477fje · Cited by 83
Watch thy neighbor: cancer is a communal affair
Weaver, V. M., & Gilbert, P. M. (2004) · Journal of Cell Science · doi:10.1242/jcs.01137 · Cited by 82
Targeting K+ channels for cancer therapy.
Conti, M. (2004) · PubMed · Cited by 79
The H + Vacuolar ATPase Maintains Neural Stem Cells in the Developing Mouse Cortex
Lange, C. M., Prenninger, S., Knuckles, P., Taylor, V., Levin, M. G., & Calegari, F. (2010) · Stem Cells and Development · doi:10.1089/scd.2010.0484 · Cited by 78
An Improved Ivermectin-activated Chloride Channel Receptor for Inhibiting Electrical Activity in Defined Neuronal Populations
Lynagh, T., & Lynch, J. W. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.107789 · Cited by 77
Targeted Deletion of Kcne2 Causes Gastritis Cystica Profunda and Gastric Neoplasia
Roepke, T. K., Purtell, K., King, E. C., Perle, K. M. D. L., Lerner, D. J., & Abbott, G. W. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011451 · Cited by 75
Control of development by ionic currents.
Lf, J. (1979) · PubMed · Cited by 70
Can gap junctions deliver?
Brink, P. R., Valiūnas, V., Gordon, C. R., Rosen, M. R., & Cohen, I. S. (2011) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2011.09.025 · Cited by 69
Altered expression of KCNK9 in colorectal cancers
Kim, C. J., Cho, Y. G., Jeong, S. W., Kim, Y. S., Kim, S. Y., Nam, S. W., Lee, S. H., Yoo, N. J., Lee, J. Y., & Park, W. S. (2004) · Apmis · doi:10.1111/j.1600-0463.2004.apm1120905.x · Cited by 68
Histone deacetylase activity is necessary for left-right patterning during vertebrate development
Carneiro, K., Donnet, C., Rejtar, T., Karger, B. L., Barisone, G. A., Dı́az, E., Kortagere, S., Lemire, J. M., & Levin, M. G. (2011) · BMC Developmental Biology · doi:10.1186/1471-213x-11-29 · Cited by 68
IONIC EVENTS AT THE MEMBRANE INITIATE RAT LIVER REGENERATION*
Leffert, H. L., & Koch, K. S. (1980) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1980.tb15979.x · Cited by 67
A Systems Biology Approach to Cancer: Fractals, Attractors, and Nonlinear Dynamics
Dinicola, S., D’Anselmi, F., Pasqualato, A., Proietti, S., Lisi, E., Cucina, A., & Bizzarri, M. (2011) · OMICS A Journal of Integrative Biology · doi:10.1089/omi.2010.0091 · Cited by 66
Volume-regulated chloride conductance in the LNCaP human prostate cancer cell line
Шуба, Я. М., Prevarskaya, N. B., Lemonnier, L., Coppenolle, F. V., Kostyuk, P. G., Mauroy, B., & Skryma, R. N. (2000) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.2000.279.4.c1144 · Cited by 66
Serotonin‐like immunoreactivity in Merkel cells and their afferent neurons in touch domes from the hairy skin of rats
English, K. B., Wang, Z.-Z., Stayner, N., Stensaas, L. J., Martin, H. A., & Tuckett, R. P. (1992) · The Anatomical Record · doi:10.1002/ar.1092320112 · Cited by 63
Transducing Bioelectric Signals into Epigenetic Pathways During Tadpole Tail Regeneration
Tseng, A.-S. K., & Levin, M. G. (2012) · The Anatomical Record · doi:10.1002/ar.22495 · Cited by 61
Untitled work
(1978) · PubMed · Cited by 58
Inwardly rectifying K+ channels and volume-regulated anion channels in multidrug-resistant small cell lung cancer cells.
Jirsch, J. D., Deeley, R. G., Cole, S. P. C., Stewart, A. J., & Fedida, D. (1993) · PubMed · Cited by 58
New Advances in the Chemistry and Biology of Organized Growth: (Section of Pathology).
Needham, J. (1936) · PubMed · Cited by 58
ß‐adrenergic receptor agonists delay while antagonists accelerate epithelial wound healing: Evidence of an endogenous adrenergic network within the corneal epithelium
Pullar, C. E., Zhao, M., Song, B., Pu, J., Reid, B., Ghoghawala, S. Y., McCaig, C., & Isseroff, R. R. (2007) · Journal of Cellular Physiology · doi:10.1002/jcp.20934 · Cited by 56
Element concentration changes in mitotically active and postmitotic enterocytes. An x-ray microanalysis study.
Cameron, I. L., Smith, N. K. R., & Pool, T. B. (1979) · The Journal of Cell Biology · doi:10.1083/jcb.80.2.444 · Cited by 55
Fluoxetine induces preventive and complex effects against colon cancer development in epithelial and stromal areas in rats
Kannen, V., Marini, T., Turatti, A., de Carvalho, M. C., Brandão, M. L., Jabor, V. A. P., Bonato, P. S., Ferreira, F. R., Zanette, D. L., Silva, W. A., et al. (2011) · Toxicology Letters · doi:10.1016/j.toxlet.2011.04.024 · Cited by 54
The significance of biological heterogeneity
Rubin, H. (1990) · Cancer Metastasis Review · doi:10.1007/bf00047585 · Cited by 53
Impact of serotonin on tumour growth
Vicaut, É., Laemmel, E., & Stucker, O. (2000) · Annals of Medicine · doi:10.3109/07853890008998826 · Cited by 53
Inverse drug screens: a rapid and inexpensive method for implicating molecular targets
Adams, D. S., & Levin, M. G. (2006) · genesis · doi:10.1002/dvg.20246 · Cited by 52
New Advances in the Chemistry and Biology of Organized Growth
Needham, J. (1936) · Proceedings of the Royal Society of Medicine · doi:10.1177/003591573602901209 · Cited by 51
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
Saito, T., Schlegel, R., Andresson, T., Yuge, L., Yamamoto, M., & Yamasaki, H. (1998) · Oncogene · doi:10.1038/sj.onc.1202092 · Cited by 48
Flux Coupling in the Human Serotonin Transporter
Adams, S. V., & DeFelice, L. J. (2002) · Biophysical Journal · doi:10.1016/s0006-3495(02)75328-9 · Cited by 48
Physiological roles of ion channels in adult neural stem cells and their progeny
Yasuda, T., & Adams, D. J. (2010) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2010.06822.x · Cited by 48
Heterooligomeric assembly of inward-rectifier K + channels from subunits of different subfamilies: K ir 2.1 (IRK1) and K ir 4.1 (BIR10)
Fakler, B., Bond, C. T., Adelman, J. P., & Ruppersberg, J. P. (1996) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s004240050251 · Cited by 46
Morphostats: a missing concept in cancer biology.
Potter, J. D. (2001) · PubMed · Cited by 46
Expression of genes coding melatonin and serotonin receptors in rodent skin
Slominski, A. T., Pisarchik, A. V., & Wortsman, J. (2004) · Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression · doi:10.1016/j.bbaexp.2004.09.002 · Cited by 45
Embryonic Morphogenetic Field Induces Phenotypic Reversion in Cancer Cells. Review Article
Bizzarri, M., Cucina, A., Biava, P. M., Proietti, S., D’Anselmi, F., Dinicola, S., Pasqualato, A., & Lisi, E. (2011) · Current Pharmaceutical Biotechnology · doi:10.2174/138920111794295701 · Cited by 45
A Unique Role for Heat Shock Protein 70 and Its Binding Partner Tissue Transglutaminase in Cancer Cell Migration
Boroughs, L. K., Antonyak, M. A., Johnson, J. L., & Cerione, R. A. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.242438 · Cited by 44
Transformation of renal tumors of frogs to normal tissues in regenerating limbs of salamanders.
Sm, R., & Hm, W. (1948) · PubMed · Cited by 44
Plausibility of stromal initiation of epithelial cancers without a mutation in the epithelium: a computer simulation of morphostats
Baker, S. G., Soto, A. M., Sonnenschein, C., Cappuccio, A., Potter, J. D., & Kramer, B. S. (2009) · BMC Cancer · doi:10.1186/1471-2407-9-89 · Cited by 43
Overexpression of a Novel XenopusRel mRNA Gene Induces Tumors in Early Embryos
Yang, S., Lockwood, A., Hollett, P. D., Ford, R., & Kao, K. R. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.22.13746 · Cited by 36
Bio-Electric Correlates of Methylcolanthrene-Induced Tumors in Mice.
Burr, H. S., Lc, S., & Smith, G. M. (1938) · PubMed · Cited by 35
Cellular concentration of magnesium and other ions in relation to protein synthesis, cell proliferation and cancer.
Cameron, I. L., & Smith, N. K. R. (1989) · PubMed · Cited by 33
Changes in the Field Properties of Mice with Transplanted Tumors.
Burr, H. S. (1941) · PubMed · Cited by 33
A Serotonin-like Immunoreactivity is Present in Human Cutaneous Melanocytes
Johansson, O., Liu, P., Liang, Y., Gangi, S., Bondesson, L., Nordlind, K., Olsson, M. J., Löntz, W., & Verhofstad, A. A. J. (1998) · Journal of Investigative Dermatology · doi:10.1046/j.1523-1747.1998.00460.x · Cited by 32
Circadian variations in biologically closed electrochemical circuits in Aloe vera and Mimosa pudica
Volkov, A. G., Baker, K. D., Foster, J. C., Clemmons, J. I., Jovanov, E., & Markin, V. S. (2011) · Bioelectrochemistry · doi:10.1016/j.bioelechem.2011.01.004 · Cited by 32
Important role of serotonin in the antitumor effects of recombinant human tumor necrosis factor-alpha in mice.
Manda, T., Nishigaki, F., Mori, J., & Shimomura, K. (1988) · PubMed · Cited by 29
A flk‐1 promoter/enhancer reporter transgenic Xenopus laevis generated using the Sleeping Beauty transposon system: An in vivo model for vascular studies
Doherty, J. R., Hamlet, M. R. J., Kuliyev, E., & Mead, P. E. (2007) · Developmental Dynamics · doi:10.1002/dvdy.21321 · Cited by 28
Upregulation of colonic ion channels in APC Min/+ mice
Ousingsawat, J., Spitzner, M., Schreiber, R., & Kunzelmann, K. (2008) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-008-0451-3 · Cited by 26
Energy dispersive x-ray microanalysis of the concentration of elements in relation to cell reproduction in normal and in cancer cells.
Cameron, I. L., & Nk, S. (1980) · PubMed · Cited by 26
First order phase transition and hysteresis in a cell’s maintenance of the membrane potential—An essential role for the inward potassium rectifiers
Gallaher, J. A., Bier, M., & van Heukelom, J. S. (2010) · Biosystems · doi:10.1016/j.biosystems.2010.05.007 · Cited by 24
An X‐ray microanalysis survey of the concentration of elements in the cytoplasm of different mammalian cell types
Cameron, I. L., Pool, T. B., & Smith, N. K. R. (1979) · Journal of Cellular Physiology · doi:10.1002/jcp.1041010315 · Cited by 24
A causal role for ERG in neoplastic transformation of prostate epithelium
Dehm, S. M. (2008) · Urologic Oncology Seminars and Original Investigations · doi:10.1016/j.urolonc.2008.09.004 · Cited by 24
The role of natural and applied electric fields in neuronal regeneration and development.
Borgens, R. B. (1986) · PubMed · Cited by 24
The National Academy of Sciences: Abstracts of Papers Presented at 1948 Meeting
(1948) · Science · doi:10.1126/science.107.2784.457 · Cited by 22
Biologic Organization and the Cancer Problem.
Burr, H. S. (1940) · PubMed · Cited by 21
Circadian rhythms in electrical circuits of Clivia miniata
Volkov, A. G., Wooten, J. D., Waite, A. J., Brown, C. R., & Markin, V. S. (2011) · Journal of Plant Physiology · doi:10.1016/j.jplph.2011.03.012 · Cited by 20
Embryogenesis and carcinogenesis: order and disorder.
Tsonis, P. A. (1987) · PubMed · Cited by 20
Tissue transglutaminase and its role in human cancer progression.
Li, B., Cerione, R., & Antonyak, M. A. (2011) · Advances in Enzymology and Related Subjects · doi:10.1002/9781118105771.ch6 · Cited by 19
Cancer-related aspects of regeneration research: a review.
Donaldson, D. J., & Jm, M. (1975) · PubMed · Cited by 17
Response to “The tissue organization field theory of cancer: A testable replacement for the somatic mutation theory” DOI: 10.1002/bies.201100025
Vaux, D. L. (2011) · BioEssays · doi:10.1002/bies.201100063 · Cited by 15
Circadian rhythms in biologically closed electrical circuits of plants
Volkov, A. G., Waite, A. J., Wooten, J. D., & Markin, V. S. (2012) · Plant Signaling & Behavior · doi:10.4161/psb.18798 · Cited by 15
Characterization of a serotonin receptor endogenous to frog melanophores
Potenza, M. N., & Lerner, M. R. (1994) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/bf00178200 · Cited by 14
Bistable dynamics of cardiac cell models coupled by dynamic gap junctions linked to Cardiac Memory
Sachdeva, G., Kalyanasundaram, K., Krishnan, J., & Chakravarthy, V. S. (2009) · Biological Cybernetics · doi:10.1007/s00422-009-0352-3 · Cited by 11
Regeneration and cancer.
WOLSKY, A. A. (1978) · PubMed · Cited by 10
AMPHIBIAN TISSUE REGENERATION - A MODEL FOR CANCER REGULATION (REVIEW)
DELRIOTSONIS, K., & Tsonis, P. A. (1992) · International Journal of Oncology · doi:10.3892/ijo.1.2.161 · Cited by 9
A Versatile Protocol for mRNA Electroporation of Xenopus laevis EmbryosPreprint
Chernet, B. T., & Levin, M. G. (2012) · Cold Spring Harbor Protocols · doi:10.1101/pdb.prot067694 · Cited by 9
Cell cycle-fluctuations in concentration of various elements in cytoplasm and in nucleus/chromatin of Physarum polycephalum.
Jeter, J. R., Cameron, I. L., Nk, S., Wl, S., & Jj, W. (1982) · PubMed · Cited by 6
Transplantation of chemically induced gastric cancer in Wistar rats.
Hirose, M., Takahashi, M., Hananouchi, M., Tatematsu, M., & Kinoshita, H. (1976) · PubMed · Cited by 4
Acquisition and maintenance of endocrine functions at high altitudes.
Cr, M., & Price, D. W. (1948) · PubMed · Cited by 1

Research works printed but not linked: 36

Adams D S, 2012, Cell Tissue Res.
Adams D S, 2012, Cold Spring Harb. Protoc.
Adams D S, 2012, Cold Spring Harb. Protoc.
Bianchi L, 1998, Cancer Res., 58, 815
10.1016/S1535-6108(04)00375-7 · DOI
Borgens R B, 1986, Prog. Clin. Biol. Res., 210, 239
Brandes L J, 1992, Cancer Res., 52, 3796
Burr H S, 1940, Yale J. Biol. Med., 12, 277
Burr H S, 1941, Yale J. Biol. Med., 13, 783
Burr H S, 1938, Yale J. Biol. Med., 10, 539
Cameron I L, 1980, Scan. Electron Microsc., Pt2, 463
Cameron I L, 1989, Magnesium, 8, 31
Cameron I L, 1980, Cancer Res., 40, 1493
Chernet B T, 2012, Cold Spring Harb. Protoc., 4, 447
Conti M, 2004, J. Exp. Ther. Oncol., 4, 161
Del Rio-Tsonis K, 1992, Int. J. Oncol., 1, 161
Donaldson D J, 1975, Growth, 39, 475
Fanburg B, 1997, Am. J. Physiol., 272, L795
Hirose M, 1976, Gann, 67, 365
Jeter J R, 1982, Cytobios, 35, 47
Jirsch J, 1993, Cancer Res., 53, 4156
Lee S L, 1999, Am. J. Physiol., 277, L282
Levin M, 2011, Bioessays
Manda T, 1988, Cancer Res., 48, 4250
Needham J, 1963, Chemical Embryology
Potter J D, 2001, Cancer Epidemiol. Biomarkers Prev., 10, 161
Rowlatt C, 1994, New Frontiers in Cancer Causation., 45
Rubin H, 1985, Cancer Res., 45, 2935
Seilern-Aspang F, 1965, Relation Between Regeneration and Tumor Growth, Regeneration in Animals and Related Problems, 452
Smith N R, 1978, Cancer Res., 38, 1952
Sonnenschein C, 1999, The Society of Cells : Cancer Control of Cell Proliferation
Sparks R L, 1983, Cancer Res., 43, 73
Tseng A-S, 2012, Anat. Rec.
Tsonis P A, 1987, Anticancer Res., 7, 617
Wang H, 2002, Cancer Res., 62, 4843
Wolsky A, 1978, Growth., 42, 425

Sorted by citations

Membrane potential and cancer progression
Yang, M., & Brackenbury, W. J. (2013) · Frontiers in Physiology · doi:10.3389/fphys.2013.00185 · Cited by 614
Ion Channels in Cancer: Are Cancer Hallmarks Oncochannelopathies?
Prevarskaya, N. B., Skryma, R. N., & Шуба, Я. М. (2018) · Physiological Reviews · doi:10.1152/physrev.00044.2016 · Cited by 505
Molecular bioelectricity: how endogenous voltage potentials control cell behavior and instruct pattern regulation in vivo
Levin, M. G. (2014) · Molecular Biology of the Cell · doi:10.1091/mbc.e13-12-0708 · Cited by 410
The Computational Boundary of a “Self”: Developmental Bioelectricity Drives Multicellularity and Scale-Free Cognition
Levin, M. G. (2019) · Frontiers in Psychology · doi:10.3389/fpsyg.2019.02688 · Cited by 334
Endogenous Bioelectric Signaling Networks: Exploiting Voltage Gradients for Control of Growth and Form
Levin, M. G., Pezzulo, G., & Finkelstein, J. M. (2017) · Annual Review of Biomedical Engineering · doi:10.1146/annurev-bioeng-071114-040647 · Cited by 294

See all 166

Authors: Lobikin, M., Chernet, B., Lobo, D., & Levin, M.
Affiliations: Tufts University (US)
Corresponding author: Lobikin, Maria
Chernet, Brook
Lobo, Daniel
Levin, Michael
ORCID: Lobo, Daniel
Levin, Michael
Venue: Physical Biology
Publisher: IOP Publishing
Published: 2012-11-29
Volume: 9
Issue: 6
Pages: 065002
ISSN: 1478-3967 (ISSN-L)
1478-3975
DOI: 10.1088/1478-3975/9/6/065002
PMC: PMC3528107
OpenAlex: W2100068438
Cited by: 166
References: 189
Citations by year: 2026: 6 · 2025: 15 · 2024: 11 · 2023: 11 · 2022: 12 · 2021: 14 · 2020: 10 · 2019: 13 · 2018: 12 · 2017: 17 · 2016: 13 · 2015: 14 · 2014: 11 · 2013: 6 · 2012: 1
FWCI: 4.11
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Physical Biology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Maryland Shared Open Access Repository (USMAI Consortium) (submittedVersion)
Digital Repository at the University of Maryland (University of Maryland College Park)
Funders: National Institutes of Health
National Institute of Arthritis and Musculoskeletal and Skin Diseases (AR061988, R01AR061988, AR055993, R01AR055993)
National Center for Research Resources (P41RR001395)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Planarian Biology and Electrostimulation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
Keywords: resting membrane potential, bioelectricity, metastasis, transmembrane voltage, serotonin signaling, melanocytes, depolarization, hyperpigmentation, 4-nitroquinoline 1-oxide, chloride channels, tumor microenvironment, Xenopus laevis, cancer diagnosis, tumor suppression
MeSH terms: Animals, Blood Vessels, Carcinogens, Cell Transformation, Neoplastic, Humans, Melanocytes, Melanoma, Membrane Potentials, Neoplasm Metastasis, Oncogenes, Receptors, Serotonin, Serotonin, Sodium, Xenopus laevis, 4-Nitroquinoline-1-oxide, Signal Transduction, Body Patterning, Tumor Microenvironment

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Resting potential, oncogene-induced tumorigenesis, and metastasis: the bioelectric basis of cancer in vivo

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks