Cytoskeletal Disruption After Electroporation and Its Significance to Pulsed Electric Field Therapies

Overview

Journal Cancers (Basel)

Publisher MDPI

Specialty Oncology

Date 2020 May 6

PMID 32366043

Citations 21

Authors

Philip M Graybill

Rafael V Davalos

Affiliations

Soon will be listed here.

Abstract

Pulsed electric fields (PEFs) have become clinically important through the success of Irreversible Electroporation (IRE), Electrochemotherapy (ECT), and nanosecond PEFs (nsPEFs) for the treatment of tumors. PEFs increase the permeability of cell membranes, a phenomenon known as electroporation. In addition to well-known membrane effects, PEFs can cause profound cytoskeletal disruption. In this review, we summarize the current understanding of cytoskeletal disruption after PEFs. Compiling available studies, we describe PEF-induced cytoskeletal disruption and possible mechanisms of disruption. Additionally, we consider how cytoskeletal alterations contribute to cell-cell and cell-substrate disruption. We conclude with a discussion of cytoskeletal disruption-induced anti-vascular effects of PEFs and consider how a better understanding of cytoskeletal disruption after PEFs may lead to more effective therapies.

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References

Pakhomov A, Xiao S, Pakhomova O, Semenov I, Kuipers M, Ibey B . Disassembly of actin structures by nanosecond pulsed electric field is a downstream effect of cell swelling. Bioelectrochemistry. 2014; 100:88-95. PMC: 4105330. DOI: 10.1016/j.bioelechem.2014.01.004. View

Tolstykh G, Thompson G, Beier H, Steelman Z, Ibey B . nsPEF-induced PIP depletion, PLC activity and actin cytoskeletal cortex remodeling are responsible for post-exposure cellular swelling and blebbing. Biochem Biophys Rep. 2017; 9:36-41. PMC: 5614542. DOI: 10.1016/j.bbrep.2016.11.005. View

Lira R, Dimova R, Riske K . Giant unilamellar vesicles formed by hybrid films of agarose and lipids display altered mechanical properties. Biophys J. 2014; 107(7):1609-19. PMC: 4190656. DOI: 10.1016/j.bpj.2014.08.009. View

Thompson G, Roth C, Dalzell D, Kuipers M, Ibey B . Calcium influx affects intracellular transport and membrane repair following nanosecond pulsed electric field exposure. J Biomed Opt. 2014; 19(5):055005. DOI: 10.1117/1.JBO.19.5.055005. View

Kato Y, Miyakawa T, Tanokura M . Overview of the mechanism of cytoskeletal motors based on structure. Biophys Rev. 2017; 10(2):571-581. PMC: 5899727. DOI: 10.1007/s12551-017-0368-1. View

Sowers A . The long-lived fusogenic state induced in erythrocyte ghosts by electric pulses is not laterally mobile. Biophys J. 1987; 52(6):1015-20. PMC: 1330100. DOI: 10.1016/S0006-3495(87)83294-0. View

Alieva I, Zemskov E, Smurova K, Kaverina I, Verin A . The leading role of microtubules in endothelial barrier dysfunction: disassembly of peripheral microtubules leaves behind the cytoskeletal reorganization. J Cell Biochem. 2013; 114(10):2258-72. PMC: 3901434. DOI: 10.1002/jcb.24575. View

Chen X, Swanson R, Kolb J, Nuccitelli R, Schoenbach K . Histopathology of normal skin and melanomas after nanosecond pulsed electric field treatment. Melanoma Res. 2009; 19(6):361-71. PMC: 3137734. DOI: 10.1097/CMR.0b013e32832f1558. View

Scheffer H, Nielsen K, de Jong M, van Tilborg A, Vieveen J, Bouwman A . Irreversible electroporation for nonthermal tumor ablation in the clinical setting: a systematic review of safety and efficacy. J Vasc Interv Radiol. 2014; 25(7):997-1011. DOI: 10.1016/j.jvir.2014.01.028. View

10.

Nesin V, Pakhomov A . Inhibition of voltage-gated Na(+) current by nanosecond pulsed electric field (nsPEF) is not mediated by Na(+) influx or Ca(2+) signaling. Bioelectromagnetics. 2012; 33(6):443-51. PMC: 3330144. DOI: 10.1002/bem.21703. View

11.

Batista Napotnik T, Wu Y, Gundersen M, Miklavcic D, Vernier P . Nanosecond electric pulses cause mitochondrial membrane permeabilization in Jurkat cells. Bioelectromagnetics. 2011; 33(3):257-64. DOI: 10.1002/bem.20707. View

12.

Henson J . Relationships between the actin cytoskeleton and cell volume regulation. Microsc Res Tech. 1999; 47(2):155-62. DOI: 10.1002/(SICI)1097-0029(19991015)47:2<155::AID-JEMT7>3.0.CO;2-T. View

13.

Tsai F, Kuo G, Chang S, Tsai P . Ca2+ signaling in cytoskeletal reorganization, cell migration, and cancer metastasis. Biomed Res Int. 2015; 2015:409245. PMC: 4421034. DOI: 10.1155/2015/409245. View

14.

Bazzoni G, Dejana E . Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis. Physiol Rev. 2004; 84(3):869-901. DOI: 10.1152/physrev.00035.2003. View

15.

OBrien E, Salmon E, Erickson H . How calcium causes microtubule depolymerization. Cell Motil Cytoskeleton. 1997; 36(2):125-35. DOI: 10.1002/(SICI)1097-0169(1997)36:2<125::AID-CM3>3.0.CO;2-8. View

16.

Bennett W, Sapay N, Tieleman D . Atomistic simulations of pore formation and closure in lipid bilayers. Biophys J. 2014; 106(1):210-9. PMC: 3907245. DOI: 10.1016/j.bpj.2013.11.4486. View

17.

Stacey M, Fox P, Buescher S, Kolb J . Nanosecond pulsed electric field induced cytoskeleton, nuclear membrane and telomere damage adversely impact cell survival. Bioelectrochemistry. 2011; 82(2):131-4. DOI: 10.1016/j.bioelechem.2011.06.002. View

18.

Levine Z, Vernier P . Life cycle of an electropore: field-dependent and field-independent steps in pore creation and annihilation. J Membr Biol. 2010; 236(1):27-36. DOI: 10.1007/s00232-010-9277-y. View

19.

Mostowy S, Cossart P . Septins: the fourth component of the cytoskeleton. Nat Rev Mol Cell Biol. 2012; 13(3):183-94. DOI: 10.1038/nrm3284. View

20.

Chopinet L, Rols M . Nanosecond electric pulses: a mini-review of the present state of the art. Bioelectrochemistry. 2014; 103:2-6. DOI: 10.1016/j.bioelechem.2014.07.008. View