Citation: Mathews, J.; Kuchling, F.;
Baez-Nieto, D.; Diberardinis, M.; Pan,
J.Q.; Levin, M. Ion Channel Drugs
Suppress Cancer Phenotype in
NG108-15 and U87 Cells: Toward
Novel Electroceuticals for
Glioblastoma. Cancers 2022, 14, 1499.
https://doi.org/10.3390/
cancers14061499
Academic Editors: Diane S. Lidke,
Jennifer M. Gillette and
Alessandra Cambi
Received: 29 January 2022
Accepted: 9 March 2022
Published: 15 March 2022
Publisher’s Note: MDPI stays neutral
with regard to jurisdictional claims in
published maps and institutional affil-
iations.
Copyright: © 2022 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
cancers
Article
Ion Channel Drugs Suppress Cancer Phenotype in NG108-15
and U87 Cells: Toward Novel Electroceuticals for Glioblastoma
Juanita Mathews
1
, Franz Kuchling
1
, David Baez-Nieto
2
, Miranda Diberardinis
1
, Jen Q. Pan
2
and Michael Levin
1,3,
*
1
Allen Discovery Center at Tufts University, Medford, MA 02155, USA; juanita.mathews@tufts.edu (J.M.);
franz.kuchling@tufts.edu (F.K.); midiberardinis@comcast.net (M.D.)
2
Stanley Center of Psychiatric Research, Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA;
dbaez@broadinstitute.org (D.B.-N.); jpan@broadinstitute.org (J.Q.P.)
3
Wyss Institute for Biologically Inspired Engineering, Harvard University, Boston, MA 02115, USA
* Correspondence: michael.levin@tufts.edu; Tel.: +1-(617)-627-6161
Simple Summary: Glioblastoma is a rapidly progressing brain cancer that is very difficult to treat.
Given that many aspects of cell and tissue behavior are controlled by electric signaling, we sought to
test whether drugs that target ion channel proteins might be effective at controlling the spread and
functionality of glioblastoma cells in culture. Testing aspects of cell growth and physiology, we show
that several novel combinations of ion channel drugs, which are already approved in human patients
for other purposes, are highly effective against two types of glioblastoma cells. This facilitates the
development of new strategies to address cancer by repurposing the large class of ion channel drugs
against cancer.
Abstract: Glioblastoma is a lethal brain cancer that commonly recurs after tumor resection and
chemotherapy treatment. Depolarized resting membrane potentials and an acidic intertumoral
extracellular pH have been associated with a proliferative state and drug resistance, suggesting
that forced hyperpolarization and disruption of proton pumps in the plasma membrane could
be a successful strategy for targeting glioblastoma overgrowth. We screened 47 compounds and
compound combinations, most of which were ion-modulating, at different concentrations in the
NG108-15 rodent neuroblastoma/glioma cell line. A subset of these were tested in the U87 human
glioblastoma cell line. A FUCCI cell cycle reporter was stably integrated into both cell lines to
monitor proliferation and cell cycle response. Immunocytochemistry, electrophysiology, and a panel
of physiological dyes reporting voltage, calcium, and pH were used to characterize responses. The
most effective treatments on proliferation in U87 cells were combinations of NS1643 and pantoprazole;
retigabine and pantoprazole; and pantoprazole or NS1643 with temozolomide. Marker analysis
and physiological dye signatures suggest that exposure to bioelectric drugs significantly reduces
proliferation, makes the cells senescent, and promotes differentiation. These results, along with
the observed low toxicity in human neurons, show the high efficacy of electroceuticals utilizing
combinations of repurposed FDA approved drugs.
Keywords: cancer; glioblastoma; NG108-15; U89; ion channel; blockers; openers
1. Introduction
Glioblastoma (GBM) is a cancer of the brain that has a high mortality rate and a short
median survivability time of around 14 to 15 months [1]. Prognosis is particularly poor
for glioblastoma patients due to the failure of standard interventions in preventing tumor
re-growth. Currently, the standard treatment for GBM is resection of the main tumor
followed by radiation and temozolomide (TMZ) administration [2]. However, reoccurrence
of GBM is common (90%) and usually arises from the area immediately next to the resected
area [3,4]. Thus, the invasiveness and hypermigratory nature of these residual cancer cells
Cancers 2022, 14, 1499. https://doi.org/10.3390/cancers14061499 https://www.mdpi.com/journal/cancers