Microfluidic devices to study the effect of electric fields on C. elegans and Danio rerio

Abstract Electrotaxis or galvanotaxis is the movement of unicellular and multicellular organisms toward a desired direction under exposure to direct or alternating current electric fields. The mechanisms underpinning how electrical stimulus evokes taxis response are not fully understood in animal models due to their complexities. Caenorhabditis elegans (C. elegans) and Danio rerio (D. rerio) have been used as model organisms to understand basic biological processes in electrotaxis due to their simple sensory and motor systems. However, their small size and continuous movement have limited the development of effective experimental techniques to study electrotaxis. Thus, microfluidics has been adopted to study the electrosensation of C. elegans and D. rerio and to develop various electric-based application devices. In this chapter, we provide an up-to-date review on the developed techniques to interrogate and use the electrosensation of C. elegans and D. rerio for the development of various manipulation and drug-screening tools. The content of this chapter can be useful to worm and fish biologists for understanding the advanced screening technologies and to microfluidic engineers for improving their devices.

[1]  Min Zhao,et al.  Controlling cell behavior electrically: current views and future potential. , 2005, Physiological reviews.

[2]  M. Ladanyi,et al.  Human synovial sarcoma proto-oncogene Syt is essential for early embryonic development through the regulation of cell migration , 2009, Laboratory Investigation.

[3]  Min Zhao,et al.  Guided Migration of Neural Stem Cells Derived from Human Embryonic Stem Cells by an Electric Field , 2012, Stem cells.

[4]  I. Chin-Sang,et al.  C. elegans chemotaxis assay. , 2013, Journal of visualized experiments : JoVE.

[5]  D. MacEwan,et al.  Influx of extracellular Ca2+ is necessary for electrotaxis in Dictyostelium , 2006, Journal of Cell Science.

[6]  Guido Dehnhardt,et al.  Electroreception in the Guiana dolphin (Sotalia guianensis) , 2012, Proceedings of the Royal Society B: Biological Sciences.

[7]  Aravinthan D. T. Samuel,et al.  Neural Circuits Mediate Electrosensory Behavior in Caenorhabditis elegans , 2007, The Journal of Neuroscience.

[8]  J. Pettigrew,et al.  Electroreception in monotremes. , 1999, The Journal of experimental biology.

[9]  P. Rezai,et al.  Behavior of Caenorhabditis elegans in alternating electric field and its application to their localization and control , 2010 .

[10]  Pak Kin Wong,et al.  Advances in Wound-Healing Assays for Probing Collective Cell Migration , 2012, Journal of laboratory automation.

[11]  Amir Reza Peimani,et al.  A microfluidic device for partial immobilization, chemical exposure and behavioural screening of zebrafish larvae. , 2017, Lab on a chip.

[12]  P. Rezai,et al.  Effect of pulse direct current signals on electrotactic movement of nematodes Caenorhabditis elegans and Caenorhabditis briggsae. , 2011, Biomicrofluidics.

[13]  Pouya Rezai,et al.  Electrotaxis of Caenorhabditis elegans in a microfluidic environment. , 2010, Lab on a chip.

[14]  Fadi A. Issa,et al.  Neural circuit activity in freely behaving zebrafish (Danio rerio) , 2011, Journal of Experimental Biology.

[15]  Pouya Rezai,et al.  Electrical sorting of Caenorhabditis elegans. , 2012, Lab on a chip.

[16]  U. Ko,et al.  A sorting strategy for C. elegans based on size-dependent motility and electrotaxis in a micro-structured channel. , 2012, Lab on a Chip.

[17]  Kailiang Jia,et al.  Modulating Behavior in C. elegans Using Electroshock and Antiepileptic Drugs , 2016, PloS one.

[18]  Luke P. Lee,et al.  A Novel Long-term, Multi-Channel and Non-invasive Electrophysiology Platform for Zebrafish , 2016, Scientific Reports.

[19]  Roy J. Lycke,et al.  Microfluidics-enabled method to identify modes of Caenorhabditis elegans paralysis in four anthelmintics. , 2013, Biomicrofluidics.

[20]  Liang Huang,et al.  On-demand dielectrophoretic immobilization and high-resolution imaging of C. elegans in microfluids , 2018 .

[21]  Khaled Youssef,et al.  Electric egg-laying: a new approach for regulating C. elegans egg-laying behaviour in a microchannel using electric field. , 2021, Lab on a chip.

[22]  P. Selvaganapathy,et al.  An automated microfluidic system for screening Caenorhabditis elegans behaviors using electrotaxis. , 2016, Biomicrofluidics.

[23]  Zhaoyang Feng,et al.  Light-sensitive neurons and channels mediate phototaxis in C. elegans , 2008, Nature Neuroscience.

[24]  Y. Seo,et al.  Pulsed Electromagnetic Fields Increase Pigmentation through the p-ERK/p-p38 Pathway in Zebrafish (Danio rerio) , 2018, International journal of molecular sciences.

[25]  Guido Dehnhardt,et al.  Passive electroreception in aquatic mammals , 2013, Journal of Comparative Physiology A.

[26]  M. Bissonnette,et al.  Corrigendum: TET-catalyzed 5-hydroxymethylcytosine regulates gene expression in differentiating colonocytes and colon cancer , 2016, Scientific Reports.

[27]  P. Bayat,et al.  Microfluidic Devices and Their Applications , 2017 .

[28]  Xiaobin Zheng,et al.  Lamin-B1 contributes to the proper timing of epicardial cell migration and function during embryonic heart development , 2016, Molecular biology of the cell.

[29]  Bifeng Liu,et al.  A microfluidic microfilter chip driven by electrotaxis and fluid flow for size-dependent C. elegans sorting with high purity and efficiency , 2018 .

[30]  Jaehoon Jung,et al.  Microfluidic Device to Measure the Speed of C. elegans Using the Resistance Change of the Flexible Electrode , 2016, Micromachines.

[31]  Pouya Rezai,et al.  Microfluidic devices for embryonic and larval zebrafish studies. , 2019, Briefings in functional genomics.

[32]  Khaled Youssef,et al.  Miniaturized Sensors and Actuators for Biological Studies on Small Model Organisms of Disease , 2018 .

[33]  P. Rezai,et al.  A microfluidic phenotype analysis system reveals function of sensory and dopaminergic neuron signaling in C. elegans electrotactic swimming behavior , 2013, Worm.

[34]  Daniel Robert,et al.  Detection and Learning of Floral Electric Fields by Bumblebees , 2013, Science.

[35]  Santosh Pandey,et al.  A microfluidic platform for high-sensitivity, real-time drug screening on C. elegans and parasitic nematodes. , 2011, Lab on a chip.

[36]  Shih-Wei Peng,et al.  Electrotaxis of lung cancer cells in ordered three-dimensional scaffolds. , 2012, Biomicrofluidics.

[37]  J. Spieth,et al.  Overview of gene structure in C. elegans. , 2014, WormBook : the online review of C. elegans biology.

[38]  N C Sukul,et al.  Influence of potential difference and current on the electrotaxis of Caenorhaditis elegans. , 1978, Journal of nematology.

[39]  Edmund R. Hunt,et al.  Static electric field detection and behavioural avoidance in cockroaches , 2008, Journal of Experimental Biology.

[40]  N. Chronis,et al.  Probing the physiology of ASH neuron in Caenorhabditis elegans using electric current stimulation. , 2011, Applied physics letters.

[41]  P. Cormie,et al.  Embryonic zebrafish neuronal growth is not affected by an applied electric field in vitro , 2007, Neuroscience Letters.

[42]  L. Carnell,et al.  C. elegans Demonstrates Distinct Behaviors within a Fixed and Uniform Electric Field , 2016, PloS one.

[43]  R. L. Russell,et al.  Normal and mutant thermotaxis in the nematode Caenorhabditis elegans. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[44]  M. Messerli,et al.  The involvement of Ca2+ and integrins in directional responses of zebrafish keratocytes to electric fields , 2009, Journal of cellular physiology.

[45]  Benoit Ladoux,et al.  Running Worms: C. elegans Self-Sorting by Electrotaxis , 2011, PloS one.

[46]  William R. Schafer Mechanosensory molecules and circuits in C. elegans , 2014, Pflügers Archiv - European Journal of Physiology.

[47]  Khaled Youssef,et al.  Parallel-Channel Electrotaxis and Neuron Screening of Caenorhabditis elegans , 2020, Micromachines.

[48]  Khaled Youssef,et al.  Phenotypic chemical and mutant screening of zebrafish larvae using an on-demand response to electric stimulation. , 2019, Integrative biology : quantitative biosciences from nano to macro.

[49]  C. Link C. elegans models of age-associated neurodegenerative diseases: Lessons from transgenic worm models of Alzheimer’s disease , 2006, Experimental Gerontology.

[50]  Elena M. Vayndorf,et al.  Behavioral Phenotyping and Pathological Indicators of Parkinson's Disease in C. elegans Models , 2017, Front. Genet..

[51]  Sun Min Kim,et al.  Effectively controlled microfluidic trap for spatiotemporal analysis of the electrotaxis of Caenorhabditis elegans , 2018, Electrophoresis.

[52]  Bifeng Liu,et al.  Highly efficient microfluidic sorting device for synchronizing developmental stages of C. elegans based on deflecting electrotaxis. , 2015, Lab on a chip.

[53]  G. Silverman,et al.  C. elegans in high-throughput drug discovery. , 2014, Advanced drug delivery reviews.

[54]  P. Rezai,et al.  Multi-phenotypic and bi-directional behavioral screening of zebrafish larvae. , 2020, Integrative biology : quantitative biosciences from nano to macro.

[55]  Muniesh Muthaiyan Shanmugam,et al.  Galvanotaxis of Caenorhabditis elegans: current understanding and its application in improving research , 2017 .

[56]  Amir Reza Peimani,et al.  A microfluidic device to study electrotaxis and dopaminergic system of zebrafish larvae. , 2018, Biomicrofluidics.

[57]  Khaled Youssef,et al.  Studying Parkinson's disease using Caenorhabditis elegans models in microfluidic devices. , 2019, Integrative biology : quantitative biosciences from nano to macro.

[58]  Ji-Yen Cheng,et al.  In vitro electrical-stimulated wound-healing chip for studying electric field-assisted wound-healing process. , 2012, Biomicrofluidics.

[59]  Mei Zhen,et al.  A hybrid microfluidic device for on-demand orientation and multidirectional imaging of C. elegans organs and neurons. , 2016, Biomicrofluidics.

[60]  Yung-Shin Sun,et al.  Studying Electrotaxis in Microfluidic Devices , 2017, Sensors.

[61]  Khaled Youssef,et al.  Semi-mobile C. elegans electrotaxis assay for movement screening and neural monitoring of Parkinson’s disease models , 2020 .

[62]  H. Chuang,et al.  Exercise in an electrotactic flow chamber ameliorates age-related degeneration in Caenorhabditis elegans , 2016, Scientific Reports.

[63]  Han-Sheng Chuang,et al.  Dielectrophoresis of Caenorhabditis elegans. , 2011, Lab on a chip.