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

Lobikin, Maria; Chernet, Brook; Lobo, Daniel; Levin, Michael

doi:10.1088/1478-3975/9/6/065002

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

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

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

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

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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.

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Depolarization (caused by lowering the Cl− concentration in the extracellular medium, which caused Cl− efflux) was found to be directly responsible for malignant proliferation.
“Depolarization (caused by lowering the Cl− concentration in the extracellular medium, which caused Cl− efflux) was found to be directly responsible for malignant proliferation.”
From Membrane potential and cancer progression (2013) · cites this paper as Lobikin et al., 2012
Results §3.1 reports that chloride efflux depolarized GlyCl-expressing cells in Xenopus embryos and that melanocytes subsequently proliferated more and showed cancer-like behavior. The paper calls this a “neoplastic-like” phenotype, not established malignant proliferation; it also says the effect was non-cell-autonomous—the depolarized cells signaled to melanocytes rather than being the proliferating cells themselves. Page numbers are unavailable in our copy. (LLM, conf=0.84)
Experimental — accuracy not yet measured
In vivo evidence shows that membrane depolarization itself, regardless of the types of ions and ion channel/transporter proteins, is able to bring cancerous transformation (i.e., increased proliferation, change in morphology and abnormal angiogenesis) in Xenopus laevis embryos.
“More recently, in vivo evidence shows that membrane depolarization itself, regardless of the types of ions and ion channel/transporter proteins, is able to bring cancerous transformation (i.e., increased proliferation, change in morphology and abnormal angiogenesis) in Xenopus laevis embryos (Lobikin et al., 2012).”
From Membrane potential and cancer progression (2013) · cites this paper as Lobikin et al., 2012
Vm modulates important cellular activities, such as proliferation and differentiation.
“changes in Vm, representing the long-term, slowly changing bioelectric gradient in non-excitable cells (Lobikin et al., 2012), have been shown to control critical cell functions including proliferation, migration, and differentiation (Binggeli and Weinstein, 1986; Schwab et al., 2007; Blackiston et al., 2009; Sundelacruz et al., 2009).”
From Membrane potential and cancer progression (2013) · cites this paper as Lobikin et al., 2012
Cancer cells possess a relatively more depolarized resting membrane potential compared to non-cancer cells.
“Indeed, cancer cells are known to possess a relatively more depolarized resting membrane potential compared to non-cancer cells [28,29,30,31].”
From Permeabilizing Cell Membranes with Electric Fields (2021) · cites this paper as [28]
Cancer cells have a relatively depolarized resting Vm compared to non-cancer cells, observed in various cellular types of the brain.
“Further evidence of the relatively depolarized resting Vm of cancer cells in comparison to that of non-cancer cells has been observed in various cellular types of the brain (summarized in Table S4) [81,82,83].”
From Permeabilizing Cell Membranes with Electric Fields (2021) · cites this paper as [28]

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Membrane potential and cancer progression
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A biophysical approach to cancer dynamics: Quantum chaos and energy turbulence
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Harnessing the Membrane Potential to Combat Cancer Progression
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Biophysical control of plasticity and patterning in regeneration and cancer
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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

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

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