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Intra-cellular Calcium Release Dynamics Due to Nanosecond Electric Pulsing

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Ultrashort Electric Pulse Effects in Biology and Medicine

Part of the book series: Series in BioEngineering ((SERBIOENG))

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Abstract

Permeabilization of cell membranous structures by nanosecond electric field pulses triggers a transient rise of cytosolic calcium with multifarious downstream effects. Electroporation of intracellular membranes (such as those of the Endoplasmic Reticulum) are likely responsible for the calcium release. This is an important application of pulsed electric fields, since calcium is known as a ubiquitous second messenger molecule that regulates several responses in cell signaling, including enzyme activation, gene transcription, neurotransmitter release, secretion, muscle contraction etc. In this chapter, a model based analysis of the dynamical calcium release in response to an external electric pulse is discussed. The results obtained are shown to match experimental data fairly well.

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References

  • Atri A, Amundson J, Clapham D, Sneyd J (1993) A single-pool model for intracellular calcium oscillations and waves in the Xenopus laevis oocyte. Biophys J 65:1727–1739

    Article  Google Scholar 

  • Barritt GJ (1999) Receptor-activated Ca2+ inflow in animal cells: a variety of pathways tailored to meet different intracellular Ca2+ signalling requirements. Biochem J 337:153–169

    Article  Google Scholar 

  • Beebe SJ, Fox PM, Rec LJ, Willis LK, Schoenbach KH (2003) Nanosecond, high intensity pulsed electric fields induce apoptosis in human cells. FASEB J 17:1493–1495

    Article  Google Scholar 

  • Beebe SJ, Blackmore PF, White J, Joshi RP, Schoenbach KH (2004) Nanosecond pulsed electric fields modulate cell function through intracellular signal transduction mechanisms. Physiol Meas 25:1077–1093

    Article  Google Scholar 

  • Bernardi P, Petronilli V (1996) The permeability transition pore as a mitochondrial calcium release channel: a critical appraisal. J Bioenerg Biomembr 28:131–138

    Article  Google Scholar 

  • Berridge M, Bootman MD, Lipp P (1998) Calcium—a life and death signal. Nature 395:645–648

    Article  Google Scholar 

  • Berridge MJ, Bootman MD, Roderick HL (2003) Calcium signalling: dynamics, homeostasis and remodeling. Nat Rev Mol Cell Biol 4:517–529

    Article  Google Scholar 

  • Bootman MD, Berridge MJ, Roderick HL (2002) Calcium signaling: more messengers, more channels, more complexity. Curr Biol 12:R563–R565

    Article  Google Scholar 

  • Bugrim AE, Zhabotinsky AM, Epstein IR (1997) Calcium waves in a model with a random spatially discrete distribution of Ca2+ release sites. Biophys J 73:2897–2906

    Article  Google Scholar 

  • Bugrim A, Fontanilla R, Eutenier BB, Keizer J, Nuccitelli R (2003) Sperm initiate a Ca2+ wave in frog eggs that is more similar to Ca2+ waves initiated by IP3 than by Ca2+. Biophys J 84:1580–1590

    Article  Google Scholar 

  • Catterall WA (2000) Structure and regulation of voltage-gated Ca2+ channels. Annu Rev Cell Dev Biol 16:521–555

    Article  Google Scholar 

  • Cherepanov DA, Feniouk BA, Junge W, Mulkidjanian AY (2003) Low dielectric permittivity of water at the membrane interface: effect on the energy coupling mechanism in biological membranes. Biophys J 85:1307–1316

    Article  Google Scholar 

  • De Young GW, Keizer J (1992) A single-pool inositol 1,4,5-trisphosphate-receptor-based model for agonist-stimulated oscillations in Ca2+ concentration. Proc Natl Acad Sci U S A 8920:9895–9899

    Article  Google Scholar 

  • Deng J, Schoenbach KH, Buescher ES, Hair PS, Fox PM, Beebe SJ (2003) The effects of intense submicrosecond electrical pulses on cells. Biophysical J 84:2709–2714

    Article  Google Scholar 

  • Falcke M (2003) On the role of stochastic channel behavior in intracellular Ca2+ dynamics. Biophys J 84:42–56

    Article  Google Scholar 

  • Falcke MB, Lechleiter JD, Hudson JL (1999) Spiral breakup and defect dynamics in a model for intracellular Ca2+ dynamics. Physica D 129:236–252

    Article  Google Scholar 

  • Falcke M, Tsimring L, Levine H (2000) Stochastic spreading of intracellular Ca2+ release. Phys Rev E 62:2636–2643

    Article  Google Scholar 

  • Haak LL, Song L, Molinski TF, Pessah IN, Cheng H, Russell JT (2001) Sparks and puffs in oligodendrocyte progenitors: cross talk between ryanodine receptors and inositol trisphosphate receptors. J Neurosci 21:3860–3870

    Article  Google Scholar 

  • Hu Q, Viswanadham S, Joshi RP, Schoenbach KH, Beebe SJ, Blackmore PF (2005) Simulations of transient membrane behavior in cells subjected to a high-intensity ultrashort electric pulse. Phys Rev E.71:031914/1–9

    Google Scholar 

  • Ichas F, Mazat JP (1998) From calcium signaling to cell death: two conformations for the mitochondrial permeability transition pore. Switching from low- to high-conductance state. Biochim Biophys Acta 1366:33–50

    Article  Google Scholar 

  • Jafri MS, Keizer J (1995) On the roles of Ca2+ diffusion, Ca2+ buffers, and the endoplasmic reticulum in IP3-induced Ca2+ waves. Biophys J 69:2139–2153

    Article  Google Scholar 

  • Joshi RP, Hu Q, Schoenbach KH (2004) Modeling studies of cell response to ultrashort, high-intensity electric fields—implications for intracellular manipulation. IEEE Trans Plasma Sci 32:1677–1686

    Article  Google Scholar 

  • Joshi RP, Nguyen A, Sridhara V, Hu Q, Nuccitelli R, Schoenbach KH (2007) Simulations of intra-cellular calcium release dynamics in response to a high-intensity, ultra-short electric pulse. Phys Rev E 75:041920/1–10

    Google Scholar 

  • Keizer J, Smith GD (1998) Spark-to-wave transition: saltatory transmission of calcium waves in cardiac myocytes. Biophys Chem 72:87–100

    Article  Google Scholar 

  • Keizer J, Smith GD, Ponce-Dawson S, Pearson JE (1998) Saltatory propagation of Ca2+ waves by Ca2+ sparks. Biophys J 75:595–600

    Article  Google Scholar 

  • Li YX, Rinzel J (1994) Equations for InsP3 receptor-mediated [Ca2+]i oscillations derived from a detailed kinetic model: a Hodgkin-Huxley like formalism. J Theor Biol 166:461–473

    Article  Google Scholar 

  • Mak D, McBride S, Raghuram V, Yue Y, Joseph S, Fosken J (2000) Single-channel properties in endoplasmic reticulum membrane of recombinant type 3 inositol trisphosphate receptor. J Gen Physiol 115:241–256

    Article  Google Scholar 

  • Marchant JS, Parker I (2001) Role of elementary Ca(2+) puffs in generating repetitive Ca(2+) oscillations. EMBO J 20:65–76

    Article  Google Scholar 

  • Parsegian VA (1969) Energy of an ion crossing a low dielectric membrane: solutions to four relevant electrostatic problems. Nature 221:844–846

    Article  Google Scholar 

  • Partridge LD, Muller TH, Swandulla D (1994) Calcium-activated non-selective channels in the nervous system. Brain Res Rev 19:319–325

    Article  Google Scholar 

  • Putney JW (2005) Capacitative calcium entry: sensing the calcium stores. J Cell Biol 169:381–382

    Article  Google Scholar 

  • Roberts-Crowley ML, Mitra-Ganguli T, Liu L, Rittenhouse AR (2009) Regulation of voltage-gated Ca2+ channels by lipids. Cell Calcium 45:589–601

    Article  Google Scholar 

  • Semenov I, Xiao S, Pakomov AG (2013) Primary pathways of intracellular Ca2+ mobilization by nanosecond pulsed electric field. Biochim Biophys Acta 1828:981–989

    Article  Google Scholar 

  • Shuai JW, Jung P (2002) Optimal intracellular calcium signaling. Phys Rev Lett 88:68102/1–4

    Google Scholar 

  • Shuai JW, Jung P (2003) Optimal ion channel clustering for intracellular calcium signaling. Proc Natl Acad Sci 100:506–510

    Article  Google Scholar 

  • Sneyd J, Falcke M (2005) Models of the inositol trisphosphate receptor. Progress Biophys Mol Biol 89:207–245

    Article  Google Scholar 

  • Sridhara V, Joshi RP, Schoenbach KH (2006) Microscopic calculations of local lipid membrane permittivities and diffusion coefficients for application to electroporation analyses. Biochem Biophys Res Comm 348:643–648

    Article  Google Scholar 

  • Sun Y, Vernier PT, Behrend M, Wang J, Thu MM, Gundersen MA, Marcu L (2006) Fluorescence microscopy imaging of electroperturbation in mammalian cells. J Biomed Opt 11:024010/1–10

    Google Scholar 

  • Swillens S, Champeil P, Combettes L, Dupont G (1998) From calcium blips to calcium puffs: theoretical analysis of the requirements for interchannel communication. J Physiol (Lond) 509:67–80

    Article  Google Scholar 

  • Tarek M (2005) Membrane electroporation: a molecular dynamics simulation. Biophys J 88:4045–4053

    Article  Google Scholar 

  • Vasilkoski Z, Esser AT, Gowrishankar TR, Weaver JC (2006) Membrane electroporation: the absolute rate equation and nanosecond time scale pore creation. Phys Rev E 74:21904/1–12

    Google Scholar 

  • Vernier PT, Sun Y, Marcu L, Salemi S, Craft CM, Gundersen MA (2003) Calcium bursts induced by nanosecond electric pulses. Biochem Biophys Res Commun 310:286–295

    Article  Google Scholar 

  • Wagner J, Li YX, Pearson J, Keizer J (1998) Simulation of the fertilization Ca2+ wave in Xenopus laevis eggs. Biophys J 75:2088–2097

    Article  Google Scholar 

  • Wagner J, Fall CP, Hong F, Sims CE, Allbritton NL, Fontanilla RA, Moraru II, Loew LM, Nuccitelli R (2004) A wave of IP3 production accompanies the fertilization Ca2+ wave in the egg of the frog, Xenopus laevis: theoretical and experimental support. Cell Calcium 35:433–447

    Article  Google Scholar 

  • White JA, Blackmore PF, Schoenbach KH, Beebe SJ (2004) Stimulation of capacitive calcium entry in HL-60 cells by nanosecond pulsed electric fields. J Biol Chem 279:22964–22972

    Article  Google Scholar 

  • Zimmermann U, Neil GA (1996) Electromanipulation of Cells. CRC Press, Boca Raton, FL

    Google Scholar 

  • Zwanzig RW (1961) Lectures in theoretical physics. Interscience, New York

    MATH  Google Scholar 

Download references

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Correspondence to Ravi Joshi .

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Joshi, R. (2021). Intra-cellular Calcium Release Dynamics Due to Nanosecond Electric Pulsing. In: Ultrashort Electric Pulse Effects in Biology and Medicine. Series in BioEngineering. Springer, Singapore. https://doi.org/10.1007/978-981-10-5113-5_6

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  • DOI: https://doi.org/10.1007/978-981-10-5113-5_6

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