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Transmembrane voltage potential is an essential cellular parameter for the detection and control of tumor development in a Xenopus model

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Chernet, Brook T., Levin, Michael·2013·Disease Models & Mechanisms
DOI 10.1242/dmm.010835PMC PMC3634644
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Abstract

Summary: Understanding mechanisms that orchestrate cell behavior into appropriately patterned tissues and organs within the organism is an essential element of preventing, detecting and treating cancer. Bioelectric signals (resting transmembrane voltage potential gradients in all cells) underlie an important and broadly conserved set of control mechanisms that regulate pattern formation. We tested the role of transmembrane potential in tumorigenesis mediated by canonical oncogenes in Xenopus laevis. Depolarized membrane potential (Vmem) was a characteristic of induced tumor-like structures (ITLSs) generated by overexpression of Gli1, KrasG12D, Xrel3 or p53Trp248. This bioelectric signature was also present in precursor ITLS sites. Vmem is a bioelectric marker that reveals ITLSs before they become histologically and morphologically apparent. Moreover, voltage was functionally important: overexpression of hyperpolarizing ion transporters caused a return to normal Vmem and significantly reduced ITLS formation in vivo. To characterize the molecular mechanism by which Vmem change regulates ITLS phenotypes, we performed a suppression screen. Vmem hyperpolarization was transduced into downstream events via Vmem-regulated activity of SLC5A8, a sodium-butyrate exchanger previously implicated in human cancer. These data indicate that butyrate, a histone deacetylase (HDAC) inhibitor, might be responsible for transcriptional events that mediate suppression of ITLSs by hyperpolarization. Vmem is a convenient cellular parameter by which tumors induced by human oncogenes can be detected in vivo and represents a new diagnostic modality. Moreover, control of resting membrane potential is functionally involved in the process by which oncogene-bearing cells depart from normal morphogenesis programs to form tumors. Modulation of Vmem levels is a novel and promising strategy for tumor normalization.

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Authors
Chernet, B. T., & Levin, M.
Affiliations
Tufts University (US)
Corresponding author
Levin, Michael
ORCID
Levin, Michael
Venue
Disease Models & Mechanisms
Publisher
The Company of Biologists
Published
2013-01-01
Volume
6
Issue
3
Pages
595-607
ISSN
  • 1754-8403 (ISSN-L)
  • 1754-8411
DOI
10.1242/dmm.010835
PMC
PMC3634644
OpenAlex
W2100967971
Cited by
148
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0
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FWCI
17.71
Type
journal article
Language
en
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  • Disease Models & Mechanisms (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
  • PubMed Central (publishedVersion, cc-by-nc-sa)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • HighWire Press Open Archive (submittedVersion)
Funders
National Institute of Arthritis and Musculoskeletal and Skin Diseases (AR061988, R01AR061988, AR055993, R01AR055993)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant and Biological Electrophysiology Studies
  • 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
Keywords
bioelectric signals, tumor detection, Xenopus laevis, Gli1, KRAS G12D, membrane depolarization, hyperpolarization, ion transporters, SLC5A8, butyrate, histone deacetylase inhibition, morphogenesis
MeSH terms
Animals, Butyrates, Cell Transformation, Neoplastic, Disease Models, Animal, Embryo, Nonmammalian, Genetic Testing, Humans, Membrane Potentials, Models, Biological, Oncogenes, Suppression, Genetic, Xenopus laevis, Tumor Suppressor Proteins, Xenopus Proteins, Mutant Proteins

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 ›

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