Skip to main content
Top

Open Access 08-07-2024 | Metastasis | REVIEW

Electrical excitability of cancer cells—CELEX model updated

Author: Mustafa B. A. Djamgoz

Published in: Cancer and Metastasis Reviews

Login to get access

Abstract

The normal functioning of every cell in the body depends on its bioelectric properties and many diseases are caused by genetic and/or epigenetic dysregulation of the underlying ion channels. Metastasis, the main cause of death from cancer, is a complex multi-stage process in which cells break away from a primary tumour, invade the surrounding tissues, enter the circulation by encountering a blood vessel and spread around the body, ultimately lodging in distant organs and reproliferating to form secondary tumours leading to devastating organ failure. Such cellular behaviours are well known to involve ion channels. The CELEX model offers a novel insight to metastasis where it is the electrical excitation of the cancer cells that is responsible for their aggressive and invasive behaviour. In turn, the hyperexcitability is underpinned by concomitant upregulation of functional voltage-gated sodium channels and downregulation of voltage-gated potassium channels. Here, we update the in vitro and in vivo evidence in favour of the CELEX model for carcinomas. The results are unequivocal for the sodium channel. The potassium channel arm is also broadly supported by existing evidence although these data are complicated by the impact of the channels on the membrane potential and consequent secondary effects. Finally, consistent with the CELEX model, we show (i) that carcinomas are indeed electrically excitable and capable of generating action potentials and (ii) that combination of a sodium channel inhibitor and a potassium channel opener can produce a strong, additive anti-invasive effect. We discuss the possible clinical implications of the CELEX model in managing cancer.
Literature
4.
go back to reference Sundelacruz, S., Levin, M., & Kaplan, D. L. (2008). Membrane potential controls adipogenic and osteogenic differentiation of mesenchymal stem cells. PLoS ONE,3, e3737.CrossRefPubMedPubMedCentral Sundelacruz, S., Levin, M., & Kaplan, D. L. (2008). Membrane potential controls adipogenic and osteogenic differentiation of mesenchymal stem cells. PLoS ONE,3, e3737.CrossRefPubMedPubMedCentral
5.
go back to reference van Vliet, P., De Boer, T. P., van der Heyden, M. A., El Tamer, M. K., Sluijter, J. P., Doevendans, P. A., & Goumans, M. (2010). Hyperpolarization induces differentiation in human cardiomyocyte progenitor cells. Stem Cell Reviews and Reports,6(2), 178–185.CrossRefPubMed van Vliet, P., De Boer, T. P., van der Heyden, M. A., El Tamer, M. K., Sluijter, J. P., Doevendans, P. A., & Goumans, M. (2010). Hyperpolarization induces differentiation in human cardiomyocyte progenitor cells. Stem Cell Reviews and Reports,6(2), 178–185.CrossRefPubMed
9.
go back to reference Djamgoz, M. B. A. (2011). Bioelectricity of cancer: Voltage-gated ion channels and direct-current electric fields. In C. Pullar (Ed.), The Physiology of Bioelectricity in Development, Tissue Regeneration, and Cancer (pp. 269–294). Taylor & Francis. Djamgoz, M. B. A. (2011). Bioelectricity of cancer: Voltage-gated ion channels and direct-current electric fields. In C. Pullar (Ed.), The Physiology of Bioelectricity in Development, Tissue Regeneration, and Cancer (pp. 269–294). Taylor & Francis.
11.
go back to reference Fraser, S. P., Diss, J. K., Chioni, A. M., Mycielska, M. E., Pan, H., Yamaci, R. F., Pani, F., Siwy, Z., Krasowska, M., Grzywna, Z., Brackenbury, W. J., Theodorou, D., Koyutürk, M., Kaya, H., Battaloglu, E., De Bella, M. T., Slade, M. J., Tolhurst, R., Palmieri, C., … Djamgoz, M. B. A. (2005). Voltage-gated sodium channel expression and potentiation of human breast cancer metastasis. Clinical Cancer Research,11, 5381–5389. https://doi.org/10.1158/1078-0432.CCR-05-0327 Fraser, S. P., Diss, J. K., Chioni, A. M., Mycielska, M. E., Pan, H., Yamaci, R. F., Pani, F., Siwy, Z., Krasowska, M., Grzywna, Z., Brackenbury, W. J., Theodorou, D., Koyutürk, M., Kaya, H., Battaloglu, E., De Bella, M. T., Slade, M. J., Tolhurst, R., Palmieri, C., … Djamgoz, M. B. A. (2005). Voltage-gated sodium channel expression and potentiation of human breast cancer metastasis. Clinical Cancer Research,11, 5381–5389. https://​doi.​org/​10.​1158/​1078-0432.​CCR-05-0327
12.
go back to reference Grimes, J. A., Fraser, S. P., Stephens, G. J., Downing, J. E. G., Laniado, M. E., Foster, C. S., Abel, P. D., & Djamgoz, M. B. A. (1995). Differential expression of voltage-activated Na+ currents in two prostatic tumour cell lines: Contribution to invasiveness in vitro. FEBS Letters,369, 290–294.CrossRefPubMed Grimes, J. A., Fraser, S. P., Stephens, G. J., Downing, J. E. G., Laniado, M. E., Foster, C. S., Abel, P. D., & Djamgoz, M. B. A. (1995). Differential expression of voltage-activated Na+ currents in two prostatic tumour cell lines: Contribution to invasiveness in vitro. FEBS Letters,369, 290–294.CrossRefPubMed
13.
go back to reference Roger, S., Rollin, J., Barascu, A., Besson, P., Raynal, P. I., Iochmann, S., Lei, M., Bougnoux, P., Gruel, Y., & Le Guennec, J. Y. (2007). Voltage-gated sodium channels potentiate the invasive capacities of human non-small-cell lung cancer cell lines. International Journal of Biochemistry & Cell Biology,39, 774–786.CrossRef Roger, S., Rollin, J., Barascu, A., Besson, P., Raynal, P. I., Iochmann, S., Lei, M., Bougnoux, P., Gruel, Y., & Le Guennec, J. Y. (2007). Voltage-gated sodium channels potentiate the invasive capacities of human non-small-cell lung cancer cell lines. International Journal of Biochemistry & Cell Biology,39, 774–786.CrossRef
14.
go back to reference Laniado, M. E., Lalani, E. N., Fraser, S. P., Grimes, J. A., Bhangal, G., Djamgoz, M. B. A., & Abel, P. D. (1997). Expression and functional analysis of voltage-activated Na+ channels in human prostate cancer cell lines and their contribution to invasion in vitro. American Journal of Pathology,150(4), 1213–1221.PubMedPubMedCentral Laniado, M. E., Lalani, E. N., Fraser, S. P., Grimes, J. A., Bhangal, G., Djamgoz, M. B. A., & Abel, P. D. (1997). Expression and functional analysis of voltage-activated Na+ channels in human prostate cancer cell lines and their contribution to invasion in vitro. American Journal of Pathology,150(4), 1213–1221.PubMedPubMedCentral
17.
go back to reference Fraser, S. P., Salvador, V., Manning, E. A., Mizal, J., Altun, S., Raza, M., Berridge, R. J., & Djamgoz, M. B. A. (2003). Contribution of functional voltage-gated Na+ channel expression to cell behaviors involved in the metastatic cascade in rat prostate cancer: I. Lateral motility. J Cell Physiol,195, 479–487. https://doi.org/10.1002/jcp.10312CrossRefPubMed Fraser, S. P., Salvador, V., Manning, E. A., Mizal, J., Altun, S., Raza, M., Berridge, R. J., & Djamgoz, M. B. A. (2003). Contribution of functional voltage-gated Na+ channel expression to cell behaviors involved in the metastatic cascade in rat prostate cancer: I. Lateral motility. J Cell Physiol,195, 479–487. https://​doi.​org/​10.​1002/​jcp.​10312CrossRefPubMed
19.
go back to reference Grimes, J. A., Djamgoz, M. B. A., Downing, J. E. G., Laniado, M. E., Foster, C. S., & Abel, P. D. (1993). Differences in expression of voltage gated ion channels between low and highly metastatic Dunning prostate cancer cell lines in vitro. Urological Research,21, P72. Grimes, J. A., Djamgoz, M. B. A., Downing, J. E. G., Laniado, M. E., Foster, C. S., & Abel, P. D. (1993). Differences in expression of voltage gated ion channels between low and highly metastatic Dunning prostate cancer cell lines in vitro. Urological Research,21, P72.
23.
go back to reference Diss, J. K. J., Fraser, S. P., & Djamgoz, M. B. A. (2004). Voltage-gated Na+ channels: Multiplicity of expression, plasticity, functional implications and pathophyiological aspects. European Biophysics Journal,33, 180–193.CrossRefPubMed Diss, J. K. J., Fraser, S. P., & Djamgoz, M. B. A. (2004). Voltage-gated Na+ channels: Multiplicity of expression, plasticity, functional implications and pathophyiological aspects. European Biophysics Journal,33, 180–193.CrossRefPubMed
29.
go back to reference Onkal, R., Mattis, J. H., Fraser, S. P., Diss, J. K., Shao, D., Okuse, K., & Djamgoz, M. B. A. (2008). Alternative splicing of Nav1.5: An electrophysiological comparison of “neonatal” and “adult” isoforms and critical involvement of a lysine residue. Journal of Cellular Physiology,216(3), 716–726. https://doi.org/10.1002/jcp.21451CrossRefPubMed Onkal, R., Mattis, J. H., Fraser, S. P., Diss, J. K., Shao, D., Okuse, K., & Djamgoz, M. B. A. (2008). Alternative splicing of Nav1.5: An electrophysiological comparison of “neonatal” and “adult” isoforms and critical involvement of a lysine residue. Journal of Cellular Physiology,216(3), 716–726. https://​doi.​org/​10.​1002/​jcp.​21451CrossRefPubMed
34.
go back to reference Bugan, I., Kucuk, S., Karagoz, Z., Fraser, S. P., Kaya, H., Dodson, A., Foster, C. S., Altun, S., & Djamgoz, M. B. A. (2019). Anti-metastatic effect of ranolazine in an in vivo rat model of prostate cancer, and expression of voltage-gated sodium channel protein in human prostate. Prostate Cancer and Prostatic Diseases,22(4), 569–579. https://doi.org/10.1038/s41391-019-0128-3CrossRefPubMed Bugan, I., Kucuk, S., Karagoz, Z., Fraser, S. P., Kaya, H., Dodson, A., Foster, C. S., Altun, S., & Djamgoz, M. B. A. (2019). Anti-metastatic effect of ranolazine in an in vivo rat model of prostate cancer, and expression of voltage-gated sodium channel protein in human prostate. Prostate Cancer and Prostatic Diseases,22(4), 569–579. https://​doi.​org/​10.​1038/​s41391-019-0128-3CrossRefPubMed
44.
go back to reference Fraser, S. P., Grimes, J. A., & Djamgoz, M. B. A. (2000). Effects of voltage-gated ion channel modulators on rat prostatic cancer cell proliferation: Comparison of strongly and weakly metastatic cell lines. The Prostate,44, 61–76.CrossRefPubMed Fraser, S. P., Grimes, J. A., & Djamgoz, M. B. A. (2000). Effects of voltage-gated ion channel modulators on rat prostatic cancer cell proliferation: Comparison of strongly and weakly metastatic cell lines. The Prostate,44, 61–76.CrossRefPubMed
49.
go back to reference Abdul, M., & Hoosein, N. (2006). Reduced Kv1.3 potassium channel expression in human prostate cancer. The Journal of Membrane Biology,214, 99–102.CrossRefPubMed Abdul, M., & Hoosein, N. (2006). Reduced Kv1.3 potassium channel expression in human prostate cancer. The Journal of Membrane Biology,214, 99–102.CrossRefPubMed
50.
52.
go back to reference Arvind, S., Arivazhagan, A., Santosh, V., & Chandramouli, B. A. (2012). Differential expression of a novel voltage gated potassium channel – Kv1.5 in astrocytomas and its impact on prognosis in glioblastoma. British Journal of Neurosurgery,26, 16–20.CrossRefPubMed Arvind, S., Arivazhagan, A., Santosh, V., & Chandramouli, B. A. (2012). Differential expression of a novel voltage gated potassium channel – Kv1.5 in astrocytomas and its impact on prognosis in glioblastoma. British Journal of Neurosurgery,26, 16–20.CrossRefPubMed
56.
go back to reference Hemmerlein, B., Weseloh, R. M., de Queiroz, F. M., Knotgen, H., Sanchez, A., Rubio, M. E., Martin, S., Schliephacke, T., Jenke, M., Heinz Joachim, R., Stühmer, W., & Pardo, L. A. (2006). Overexpression of Eag1 potassium channels in clinical tumours. Molecular Cancer, 5, 41. Hemmerlein, B., Weseloh, R. M., de Queiroz, F. M., Knotgen, H., Sanchez, A., Rubio, M. E., Martin, S., Schliephacke, T., Jenke, M., Heinz Joachim, R., Stühmer, W., & Pardo, L. A. (2006). Overexpression of Eag1 potassium channels in clinical tumours. Molecular Cancer, 5, 41.
57.
go back to reference Liu, Z., Zhang, J., Gao, Y., Pei, L., Zhou, J., Gu, L., Zhang, L., Zhu, B., Hattori, N., Ji, J., Yuasa, Y., Kim, W., Ushijima, T., Shi, H., & Deng, D. (2014). Large-scale characterization of DNA methylation changes in human gastric carcinomas with and without metastasis. Clinical Cancer Research,20, 4598–4612.CrossRefPubMedPubMedCentral Liu, Z., Zhang, J., Gao, Y., Pei, L., Zhou, J., Gu, L., Zhang, L., Zhu, B., Hattori, N., Ji, J., Yuasa, Y., Kim, W., Ushijima, T., Shi, H., & Deng, D. (2014). Large-scale characterization of DNA methylation changes in human gastric carcinomas with and without metastasis. Clinical Cancer Research,20, 4598–4612.CrossRefPubMedPubMedCentral
59.
go back to reference Ouadid-Ahidouch, H., & Ahidouch, A. (2008). K+ channel expression in human breast cancer cells: Involvement in cell cycle regulation and carcinogenesis. Journal of Membrane Biology,221, 1–6.CrossRefPubMed Ouadid-Ahidouch, H., & Ahidouch, A. (2008). K+ channel expression in human breast cancer cells: Involvement in cell cycle regulation and carcinogenesis. Journal of Membrane Biology,221, 1–6.CrossRefPubMed
60.
go back to reference Hammadi, M., Chopin, V., Matifat, F., Dhennin-Duthille, I., Chasseraud, M., Sevestre, H., & Ouadid-Ahidouch, H. (2012). Human ether a-gogo K+ channel 1 (hEag1) regulates MDA-MB-231 breast cancer cell migration through Orai1-dependent calcium entry. Journal of Cellular Physiology,227, 3837–3846.CrossRefPubMed Hammadi, M., Chopin, V., Matifat, F., Dhennin-Duthille, I., Chasseraud, M., Sevestre, H., & Ouadid-Ahidouch, H. (2012). Human ether a-gogo K+ channel 1 (hEag1) regulates MDA-MB-231 breast cancer cell migration through Orai1-dependent calcium entry. Journal of Cellular Physiology,227, 3837–3846.CrossRefPubMed
62.
go back to reference Martínez, R., Stühmer, W., Martin, S., Schell, J., Reichmann, A., Rohde, V., & Pardo, L. (2015). Analysis of the expression of Kv10.1 potassium channel in patients with brain metastases and glioblastoma multiforme: Impact on survival. BMC Cancer, 15, 839. https://doi.org/10.1186/s12885-015-1848-y Martínez, R., Stühmer, W., Martin, S., Schell, J., Reichmann, A., Rohde, V., & Pardo, L. (2015). Analysis of the expression of Kv10.1 potassium channel in patients with brain metastases and glioblastoma multiforme: Impact on survival. BMC Cancer, 15, 839. https://​doi.​org/​10.​1186/​s12885-015-1848-y
63.
go back to reference Xia, J., Huang, N., Huang, H., Sun, L., Dong, S., Su, J., Zhang, J., Wang, L., Lin, L., Shi, M., Bin, J., Liao, Y., Li, N., & Liao, W. (2016). Voltage-gated sodium channel Nav1.7 promotes gastric cancer progression through MACC1-mediated upregulation of NHE1. Int J Cancer,139, 2553–2569. https://doi.org/10.1002/ijc.30381CrossRefPubMed Xia, J., Huang, N., Huang, H., Sun, L., Dong, S., Su, J., Zhang, J., Wang, L., Lin, L., Shi, M., Bin, J., Liao, Y., Li, N., & Liao, W. (2016). Voltage-gated sodium channel Nav1.7 promotes gastric cancer progression through MACC1-mediated upregulation of NHE1. Int J Cancer,139, 2553–2569. https://​doi.​org/​10.​1002/​ijc.​30381CrossRefPubMed
64.
go back to reference Becchetti, A., Crescioli, S., Zanieri, F., Petroni, G., Mercatelli, R., Coppola, S., Gasparoli, L., D’Amico, M., Pillozzi, S., Crociani, O., Stefanini, M., Fiore, A., Carraresi, L., Morello, V., Manoli, S., Brizzi, M. F., Ricci, D., Rinaldi, M., Masi, A., … Arcangeli, A. (2017). The conformational state of Herg1 channels determines integrin association, downstream signaling, and cancer progression. Science Signaling,10(473), eaaf3236. https://doi.org/10.1126/scisignal.aaf3236 Becchetti, A., Crescioli, S., Zanieri, F., Petroni, G., Mercatelli, R., Coppola, S., Gasparoli, L., D’Amico, M., Pillozzi, S., Crociani, O., Stefanini, M., Fiore, A., Carraresi, L., Morello, V., Manoli, S., Brizzi, M. F., Ricci, D., Rinaldi, M., Masi, A., … Arcangeli, A. (2017). The conformational state of Herg1 channels determines integrin association, downstream signaling, and cancer progression. Science Signaling,10(473), eaaf3236. https://​doi.​org/​10.​1126/​scisignal.​aaf3236
66.
go back to reference Breuer, E. K., Fukushiro-Lopes, D., Dalheim, A., Burnette, M., Zartman, J., Kaja, S., Wells, C., Campo, L., Curtis, K. J., Romero-Moreno, R., Littlepage, L. E., Niebur, G. L., Hoskins, K., Nishimura, M. I., & Gentile, S. (2019). Potassium channel activity controls breast cancer metastasis by affecting β-catenin signaling. Cell Death & Disease,10(3), 180. https://doi.org/10.1038/s41419-019-1429-0CrossRef Breuer, E. K., Fukushiro-Lopes, D., Dalheim, A., Burnette, M., Zartman, J., Kaja, S., Wells, C., Campo, L., Curtis, K. J., Romero-Moreno, R., Littlepage, L. E., Niebur, G. L., Hoskins, K., Nishimura, M. I., & Gentile, S. (2019). Potassium channel activity controls breast cancer metastasis by affecting β-catenin signaling. Cell Death & Disease,10(3), 180. https://​doi.​org/​10.​1038/​s41419-019-1429-0CrossRef
67.
go back to reference Eskandari, N., Senyuk, V., Moore, J., Kalik, Z., Luan, Q., Papautsky, I., Moshiri, A., Bocchetta, M., Salami, S. A., Oryan, S., & Gentile, S. (2021). Molecular activation of the Kv11.1 channel reprograms EMT in colon cancer by inhibiting TGFβ signaling via activation of calcineurin. Cancers (Basel),13(23), 6025. https://doi.org/10.3390/cancers13236025CrossRefPubMed Eskandari, N., Senyuk, V., Moore, J., Kalik, Z., Luan, Q., Papautsky, I., Moshiri, A., Bocchetta, M., Salami, S. A., Oryan, S., & Gentile, S. (2021). Molecular activation of the Kv11.1 channel reprograms EMT in colon cancer by inhibiting TGFβ signaling via activation of calcineurin. Cancers (Basel),13(23), 6025. https://​doi.​org/​10.​3390/​cancers13236025CrossRefPubMed
70.
go back to reference Blandino, J. K., Viglione, M. P., Bradley, W. A., Oie, H. K., & Kim, Y. I. (1995). Voltage-dependent sodium channels in human small-cell lung cancer cells: Role in action potentials and inhibition by Lambert-Eaton syndrome IgG. Journal of Membrane Biology,143(2), 153–163. https://doi.org/10.1007/BF00234661CrossRefPubMed Blandino, J. K., Viglione, M. P., Bradley, W. A., Oie, H. K., & Kim, Y. I. (1995). Voltage-dependent sodium channels in human small-cell lung cancer cells: Role in action potentials and inhibition by Lambert-Eaton syndrome IgG. Journal of Membrane Biology,143(2), 153–163. https://​doi.​org/​10.​1007/​BF00234661CrossRefPubMed
74.
go back to reference Cabello, M., Ge, H., Aracil, C., Moschou, D., Estrela, P., Manuel Quero, J., Pascu, S. I., & Rocha, P. R. F. (2019). Extracellular electrophysiology in the prostate cancer cell model PC-3. Sensors (Basel), 19(1),139. https://doi.org/10.3390/s19010139 Cabello, M., Ge, H., Aracil, C., Moschou, D., Estrela, P., Manuel Quero, J., Pascu, S. I., & Rocha, P. R. F. (2019). Extracellular electrophysiology in the prostate cancer cell model PC-3. Sensors (Basel), 19(1),139. https://​doi.​org/​10.​3390/​s19010139
75.
go back to reference Elinder, F., & Arhem, P. (1994). Effects of gadolinium on ion channels in the myelinated axon of Xenopus laevis: Four sites of action. Biophysical Journal,67(1), 71–83.CrossRefPubMedPubMedCentral Elinder, F., & Arhem, P. (1994). Effects of gadolinium on ion channels in the myelinated axon of Xenopus laevis: Four sites of action. Biophysical Journal,67(1), 71–83.CrossRefPubMedPubMedCentral
76.
go back to reference Diss, J. K. J., Stewart, D., Pani, F., Foster, C. S., Walker, M. M., Patel, A., & Djamgoz, M. B. A. (2005). A potential novel marker for human prostate cancer progression: Voltage-gated Na+ channel expression in vivo. Prostate Cancer and Prostatic Diseases,8, 266–273.CrossRefPubMed Diss, J. K. J., Stewart, D., Pani, F., Foster, C. S., Walker, M. M., Patel, A., & Djamgoz, M. B. A. (2005). A potential novel marker for human prostate cancer progression: Voltage-gated Na+ channel expression in vivo. Prostate Cancer and Prostatic Diseases,8, 266–273.CrossRefPubMed
82.
go back to reference Chen, S. H., Zhang, B. Y., Zhou, B., Zhu, C. Z., Sun, L. Q., & Feng, Y. J. (2019). Perineural invasion of cancer: A complex crosstalk between cells and molecules in the perineural niche. American Journal of Cancer Research,9(1), 1–21.PubMedPubMedCentral Chen, S. H., Zhang, B. Y., Zhou, B., Zhu, C. Z., Sun, L. Q., & Feng, Y. J. (2019). Perineural invasion of cancer: A complex crosstalk between cells and molecules in the perineural niche. American Journal of Cancer Research,9(1), 1–21.PubMedPubMedCentral
87.
go back to reference Hayakawa, Y., Sakitani, K., Konishi, M., Asfaha, S., Niikura, R., Tomita, H., Renz, B. W., Tailor, Y., Macchini, M., Middelhoff, M., Jiang, Z., Tanaka, T., Dubeykovskaya, Z. A., Kim, W., Chen, X., Urbanska, A. M., Nagar, K., Westphalen, C. B., Quante, M., … Wang, T. C. (2017). Nerve growth factor promotes gastric tumorigenesis through aberrant cholinergic signaling. Cancer Cell,31(1), 21–34. https://doi.org/10.1016/j.ccell.2016.11.005CrossRefPubMed Hayakawa, Y., Sakitani, K., Konishi, M., Asfaha, S., Niikura, R., Tomita, H., Renz, B. W., Tailor, Y., Macchini, M., Middelhoff, M., Jiang, Z., Tanaka, T., Dubeykovskaya, Z. A., Kim, W., Chen, X., Urbanska, A. M., Nagar, K., Westphalen, C. B., Quante, M., … Wang, T. C. (2017). Nerve growth factor promotes gastric tumorigenesis through aberrant cholinergic signaling. Cancer Cell,31(1), 21–34. https://​doi.​org/​10.​1016/​j.​ccell.​2016.​11.​005CrossRefPubMed
90.
go back to reference Brisson, L., Driffort, V., Benoist, L., Poet, M., Counillon, L., Antelmi, E., Rubino, R., Besson, P., Labbal, F., Chevalier, S., Reshkin, S. J., Gore, J., & Roger, S. (2013). Nav1.5 Na⁺ channels allosterically regulate the NHE-1 exchanger and promote the activity of breast cancer cell invadopodia. Journal of Cell Science,126(Pt 21), 4835–4842. https://doi.org/10.1242/jcs.123901CrossRefPubMed Brisson, L., Driffort, V., Benoist, L., Poet, M., Counillon, L., Antelmi, E., Rubino, R., Besson, P., Labbal, F., Chevalier, S., Reshkin, S. J., Gore, J., & Roger, S. (2013). Nav1.5 Na⁺ channels allosterically regulate the NHE-1 exchanger and promote the activity of breast cancer cell invadopodia. Journal of Cell Science,126(Pt 21), 4835–4842. https://​doi.​org/​10.​1242/​jcs.​123901CrossRefPubMed
96.
98.
go back to reference Cuzick, J., Holland, R., Barth, V., Davies, R., Faupel, M., Fentiman, I., Frischbier, H. J., LaMarque, J. L., Merson, M., Sacchini, V., Vanel, D., & Veronesi, U. (1998). Electropotential measurements as a new diagnostic modality for breast cancer. Lancet,352, 359–363.CrossRefPubMed Cuzick, J., Holland, R., Barth, V., Davies, R., Faupel, M., Fentiman, I., Frischbier, H. J., LaMarque, J. L., Merson, M., Sacchini, V., Vanel, D., & Veronesi, U. (1998). Electropotential measurements as a new diagnostic modality for breast cancer. Lancet,352, 359–363.CrossRefPubMed
99.
go back to reference Wu, J., Wang, P., Tang, Y., Liu, H., Wang, H., Zhang, W., Zhang, Y., Chen, L., Xu, Z., & Yao, X. (2019). Technical Note: A new method to rapidly identify benign and malignant breast lumps through bioelectrical impedance spectroscopy. Medical Physics,46(5), 2522–2525. https://doi.org/10.1002/mp.13474CrossRefPubMed Wu, J., Wang, P., Tang, Y., Liu, H., Wang, H., Zhang, W., Zhang, Y., Chen, L., Xu, Z., & Yao, X. (2019). Technical Note: A new method to rapidly identify benign and malignant breast lumps through bioelectrical impedance spectroscopy. Medical Physics,46(5), 2522–2525. https://​doi.​org/​10.​1002/​mp.​13474CrossRefPubMed
100.
go back to reference Cunnea, P., Gorgy, T., Petkos, K., Gowers, S. A. N., Lu, H., Morera, C., Wu, W., Lawton, P., Nixon, K., Leong, C. L., Sorbi, F., Domenici, L., Paterson, A., Curry, E., Gabra, H., Boutelle, M. G., Drakakis, E. M., & Fotopoulou, C. (2018). Clinical value of bioelectrical properties of cancerous tissue in advanced epithelial ovarian cancer patients. Science and Reports,8(1), 14695. https://doi.org/10.1038/s41598-018-32720-8CrossRef Cunnea, P., Gorgy, T., Petkos, K., Gowers, S. A. N., Lu, H., Morera, C., Wu, W., Lawton, P., Nixon, K., Leong, C. L., Sorbi, F., Domenici, L., Paterson, A., Curry, E., Gabra, H., Boutelle, M. G., Drakakis, E. M., & Fotopoulou, C. (2018). Clinical value of bioelectrical properties of cancerous tissue in advanced epithelial ovarian cancer patients. Science and Reports,8(1), 14695. https://​doi.​org/​10.​1038/​s41598-018-32720-8CrossRef
103.
go back to reference Evans, S. W., Shi, D. Q., Chavarha, M., Plitt, M. H., Taxidis, J., Madruga, B., Fan, J. L., Hwang, F. J., van Keulen, S. C., Suomivuori, C. M., Pang, M. M., Su, S., Lee, S., Hao, Y. A., Zhang, G., Jiang, D., Pradhan, L., Roth, R. H., Liu, Y., … Lin, M. Z. (2023). A positively tuned voltage indicator for extended electrical recordings in the brain. Nature Methods,20(7), 1104–1113. https://doi.org/10.1038/s41592-023-01913-zCrossRefPubMedPubMedCentral Evans, S. W., Shi, D. Q., Chavarha, M., Plitt, M. H., Taxidis, J., Madruga, B., Fan, J. L., Hwang, F. J., van Keulen, S. C., Suomivuori, C. M., Pang, M. M., Su, S., Lee, S., Hao, Y. A., Zhang, G., Jiang, D., Pradhan, L., Roth, R. H., Liu, Y., … Lin, M. Z. (2023). A positively tuned voltage indicator for extended electrical recordings in the brain. Nature Methods,20(7), 1104–1113. https://​doi.​org/​10.​1038/​s41592-023-01913-zCrossRefPubMedPubMedCentral
112.
go back to reference Langman, L., & Burr, H. S. (1947). Electrometric studies in women with malignancy of cervix uteri. Science,105, 209–210.CrossRefPubMed Langman, L., & Burr, H. S. (1947). Electrometric studies in women with malignancy of cervix uteri. Science,105, 209–210.CrossRefPubMed
113.
go back to reference Oertel, H. (1937). An additional note on the innervation of tumours. Canadian Medical Association Journal,36, 401–403.PubMedPubMedCentral Oertel, H. (1937). An additional note on the innervation of tumours. Canadian Medical Association Journal,36, 401–403.PubMedPubMedCentral
Metadata
Title
Electrical excitability of cancer cells—CELEX model updated
Author
Mustafa B. A. Djamgoz
Publication date
08-07-2024
Publisher
Springer US
Keyword
Metastasis
Published in
Cancer and Metastasis Reviews
Print ISSN: 0167-7659
Electronic ISSN: 1573-7233
DOI
https://doi.org/10.1007/s10555-024-10195-6