Skip to main content
SpringerLink
Log in

The Use of Electroporation in Developmental Biology

  • Reference work entry
  • First Online:
Handbook of Electroporation

Abstract

During the formation of a complex organism, cells divide, die, migrate, and differentiate. Biologists have established tools to observe those phenomena but also to change their course, which subsequently enables to infer causal relationships between various events occurring in different cell groups. More precisely, present approaches mostly rely on modifications of gene expression. For instance, cells are labeled with fluorescent proteins and tracked within the embryo, molecular signals are switched on and off to perturb regulatory pathways. Importantly, in all those experiments, the exogenous genetic material must be delivered at the right place and with the appropriate timing: requirements that can both be fulfilled by electroporation. After 15 years of constant refinement, this technique has now superseded methods like viral infection, microinjection, and lipofection. Applications encompass a large number of model organisms, targeted anatomical structures, and molecular biology techniques.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 1,799.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 1,999.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abud HE, Lock P, Heath JK (2004) Efficient gene transfer into the epithelial cell layer of embryonic mouse intestine using low-voltage electroporation. Gastroenterology 126:1779–1787

    Article  Google Scholar 

  • Akamatsu W, Okano HJ, Osumi N, Inoue T, Nakamura S, Sakakibara SI, Miura M, Matsuo N, Darnell RB, Okano H (1999) Mammalian ELAV-like neuronal RNA-binding proteins HuB and HuC promote neuronal development in both the central and the peripheral nervous systems. Proc Natl Acad Sci U S A 96:9885–9890

    Article  Google Scholar 

  • Alie TM, Vrljicak PJ, Myburgh DB, Gupta IR (2007) Microinjection and electroporation of embryonic kidney explants: an improved method. Kidney Int 72:121–125

    Article  Google Scholar 

  • Ando T, Fujiwara H (2013) Electroporation-mediated somatic transgenesis for rapid functional analysis in insects. Development 140:454–458

    Article  Google Scholar 

  • Atkins RL, Wang D, Burke RD (2000) Localized electroporation: a method for targeting expression of genes in avian embryos. BioTechniques 28:94–100

    Google Scholar 

  • Bansal T, Lenhart J, Kim T, Duan C, Maharbiz MM (2009) Patterned delivery and expression of gene constructs into zebrafish embryos using microfabricated interfaces. Biomed Microdevices 11:633–641

    Article  Google Scholar 

  • Barembaum M, Bronner-Fraser M (2007) Spalt4 mediates invagination and otic placode gene expression in cranial ectoderm. Development 134:3805–3814

    Article  Google Scholar 

  • Barker M, Billups B, Hamann M (2009) Focal macromolecule delivery in neuronal tissue using simultaneous pressure ejection and local electroporation. J Neurosci Methods 177:273–284

    Article  Google Scholar 

  • Bartkowska K, Paquin A, Gauthier AS, Kaplan DR, Miller FD (2007) Trk signaling regulates neural precursor cell proliferation and differentiation during cortical development. Development 134:4369–4380

    Article  Google Scholar 

  • Bhattacharyya S, Kulesa PM, Fraser SE (2008) Vital labeling of embryonic cells using fluorescent dyes and proteins. In: Bronner-Fraser M (ed) Avian embryology, 2nd edn. Academic, London, pp 187–210

    Chapter  Google Scholar 

  • Bobick BE, Alexander PG, Tuan RS (2014) High efficiency transfection of embryonic limb mesenchyme with plasmid DNA using square wave pulse electroporation and sucrose buffer. BioTechniques 56:85–89

    Article  Google Scholar 

  • Bosch TCG, Augustin R, Gellner K, Khalturin K, Lohmann JU (2002) In vivo electroporation for genetic manipulations of whole hydra polyps. Differentiation 70:140–147

    Article  Google Scholar 

  • Brown CY, Eom DS, Amarnath S, Agarwala S (2012) A simple technique for early in vivo electroporation of E1 chick embryos. Dev Dyn 241:545–552

    Article  Google Scholar 

  • Bullmann T, Arendt T, Frey U, Hanashima C (2015) A transportable, inexpensive electroporator for in utero electroporation. Develop Growth Differ 57:369–377

    Article  Google Scholar 

  • Buono RJ, Linser PJ (1992) Transient expression of RSVCAT in transgenic zebrafish made by electroporation. Mol Mar Biol Biotechnol 1:271–275

    Google Scholar 

  • Calegari F, Haubensak W, Yang D, Huttner WB, Buchholz F (2002) Tissue-specific RNA interference in postimplantation mouse embryos with endoribonuclease-prepared short interfering RNA. Proc Natl Acad Sci U S A 99:14236–14240

    Article  Google Scholar 

  • Cerda GA, Thomas JE, Allende ML, Karlstrom RO, Palma V (2006) Electroporation of DNA, RNA, and morpholinos into zebrafish embryos. Methods 39:207–211

    Article  Google Scholar 

  • Chabot S, Rosazza C, Golzio M, Zumbusch A, Teissié J, Rols MP (2013) Nucleic acids electro-transfer: from bench to bedside. Curr Drug Metab 14:300–308

    Article  Google Scholar 

  • Chernet BT, Levin M (2012) A versatile protocol for mRNA electroporation of Xenopus laevis embryos. Cold Spring Harb Protocol:447–452

    Google Scholar 

  • Chudakov DM, Matz MV, Lukyanov S, Lukyanov KA (2010) Fluorescent proteins and their applications in imaging living cells and tissues. Physiol Rev 90:1103–1163

    Article  Google Scholar 

  • Corbo JC, Levine M, Zeller RW (1997) Characterization of a notochord-specific enhancer from the Brachyury promoter region of the ascidian, Ciona intestinalis. Development 124:589–602

    Google Scholar 

  • Couly GF, Coltey PM, Le Douarin NM (1993) The triple origin of skull in higher vertebrates: a study in quail-chick chimeras. Development 117:409–429

    Google Scholar 

  • Cui C, Lansford R, Filla MB, Little CD, Cheuvront TJ, Rongish BJ (2006) Electroporation and EGFP labeling of gastrulating quail embryos. Dev Dyn 235:2802–2810

    Article  Google Scholar 

  • dal Maschio M, Ghezzi D, Bony G, Alabastri A, Deidda G, Brondi M, Sato SS, Zaccaria RP, Fabrizio ED, Ratto GM, Cancedda L (2012) High-performance and site-directed in utero electroporation by a triple-electrode probe. Nat Commun 3:960

    Article  Google Scholar 

  • Danielian PS, Muccino D, Rowitch DH, Michael SK, McMahon AP (1998) Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Curr Biol 8:1323–1326

    Article  Google Scholar 

  • Davidson BP, Tsang TE, Khoo PL, Gad JM, Tam PPL (2003) Introduction of cell markers into germ layer tissues of the mouse gastrula by whole embryo electroporation. Genesis 35:57–62

    Article  Google Scholar 

  • De la Rossa A, Jabaudon D (2015) In vivo rapid gene delivery into postmitotic neocortical neurons using iontoporation. Nat Protoc 10:25–32

    Article  Google Scholar 

  • deCastro M, Saijoh Y, Schoenwolf JC (2006) Optimized cationic lipid-based gene delivery reagents for use in developing vertebrate embryos. Dev Dyn 235:2210–2219

    Article  Google Scholar 

  • Donovan SL, Dyer MA (2006) Preparation and square wave electroporation of retinal explant cultures. Nat Protoc 1:2710–2718

    Article  Google Scholar 

  • Driver EC, Kelley MW (2010) Transfection of mouse cochlear explants by electroporation. Curr Protocol Neurosci. Chapter 4:Unit 4.34.1–10

    Google Scholar 

  • Echeverri K, Tanaka EM (2003) Electroporation as a tool to study in vivo spinal cord regeneration. Dev Dyn 226:418–425

    Article  Google Scholar 

  • Echeverri K, Tanaka EM (2005) Proximodistal patterning during limb regeneration. Dev Biol 279:391–401

    Article  Google Scholar 

  • Eichele G, Tickle C, Alberts BM (1985) Studies on mechanism of retinoid-induced pattern duplications in the early chick limb bud: temporal and spatial aspects. J Cell Biol 101:1913–1920

    Article  Google Scholar 

  • Eide FF, Eisenberg SR, Sanders TA (2000) Electroporation-mediated gene transfer in free-swimming embryonic Xenopus laevis. FEBS Lett 496:29–32

    Article  Google Scholar 

  • Falk J, Drinjakovic J, Leung KM, Dwivedy A, Regan AG, Piper M, Holt CE (2007) Electroporation of cDNA/morpholinos to targeted areas of embryonic CNS in Xenopus. BMC Dev Biol 7:107

    Article  Google Scholar 

  • Fox MB, Esveld DC, Valero A, Luttge R, Mastwijk HC, Bartels PV, van den Berg A, Boom RM (2006) Electroporation of cells in microfluidic device: a review. Anal Bioanal Chem 385:474–485

    Article  Google Scholar 

  • Fukuchi-Shimogori T, Grove EA (2001) Neocortex patterning by the secreted signaling molecule FGF8. Science 294:1071–1074

    Article  Google Scholar 

  • Fukuda K, Sakamoto N, Narita T, Saitoh K, Kameda T, Iba H, Yasugi S (2000) Application of efficient and specific gene transfer systems and organ culture techniques for the elucidation of mechanisms of epithelial-mesenchymal interaction in the developing gut. Develop Growth Differ 42:207–211

    Article  Google Scholar 

  • Geetha-Loganathan P, Nimmagadda S, Hafez I, Fu K, Cullis PR, Richman JM (2011) Development of high-concentration lipoplexes for in vivo gene function studies in vertebrate embryos. Dev Dyn 240:2108–2119

    Article  Google Scholar 

  • Geng T, Lu C (2013) Microfluidic electroporation for cellular analysis and delivery. Lab Chip 13:3830–3821

    Article  Google Scholar 

  • Gilbert SF (2013) Developmental biology, 10th edn. Sinauer, Sunderland

    Google Scholar 

  • Giroux SJD, Alves-Leiva C, Lécluse Y, Martin P, Albagl O, Godin I (2007) Gene transfer to pre-hematopoietic and committed hematopoietic precursors in the early mouse yolk sac: a comparative study between in situ electroporation and retroviral transduction. BMC Dev Biol 7:79

    Article  Google Scholar 

  • Golzio M, Teissie J, Rols MP (2002) Direct visualization at the single-cell level of electrically mediated gene delivery. Proc Natl Acad Sci U S A 99:1292–1297

    Article  Google Scholar 

  • Grabarek JB, Plusa B, Glover DM, Zernicka-Goetz M (2002) Efficient delivery of dsRNA into zona-enclosed mouse oocytes and preimplantation embryos by electroporation. Genesis 32:269–276

    Article  Google Scholar 

  • Haas K, Sin WC, Javaherian A, Li Z, Cline HT (2001) Single-cell electroporation for gene transfer in vivo. Neuron 29:583–591

    Article  Google Scholar 

  • Haas K, Jensen K, Sin WC, Foa L, Cline HT (2002) Targeted electroporation in Xenopus tadpoles in vivo-from single cells to the entire brain. Differentiation 70:148–154

    Article  Google Scholar 

  • Harrison RL, Byrne BJ, Tung L (1998) Electroporation-mediated gene transfer in cardiac tissue. FEBS Lett 435:1–5

    Article  Google Scholar 

  • Hashimoto-Torii K, Motoyama J, Hui CC, Kuroiwa A, Nakafuku M, Shimamura K (2003) Differential activities of sonic hedgehog mediated by Gli transcription factors define distinct neuronal subtypes in the dorsal thalamus. Mech Dev 120:1097–1111

    Article  Google Scholar 

  • Hatakeyama J, Shimamura K (2008) Method for electroporation for the early chick embryo. Develop Growth Differ 5:449–452

    Article  Google Scholar 

  • Hendricks M, Jesuthasan S (2007) Electroporation-based methods for in vivo, whole mount and primary culture analysis of zebrafish brain development. Neural Dev 2:6

    Article  Google Scholar 

  • Huang KS, Lin YC, Su KC, Chen HY (2007) An electroporation microchip system for the transfection of zebrafish embryos using quantum dots and GFP genes for evaluation. Biomed Microdevices 9:761–768

    Article  Google Scholar 

  • Huang Y, Wilkie R, Wilson V (2015) Methods for precisely localized transfer of cells or DNA into early postimplantation mouse embryos. J Vis Exp 106:53295

    Google Scholar 

  • Iba H (2000) Gene transfer into chicken embryos by retrovirus vectors. Develop Growth Differ 42:213–218

    Article  Google Scholar 

  • Iimura T, Pourquié O (2008) Manipulation and electroporation of the avian segmental plate and somites in vitro. In: Bronner-Fraser M (ed) Avian embryology, 2nd edn. Academic, London, pp 257–270

    Chapter  Google Scholar 

  • Inoue K (1992) Expression of reporter genes introduced by microinjection and electroporation in fish embryos and fry. Mol Mar Biol Biotechnol 1:266–270

    Google Scholar 

  • Itasaki N, Bel-Vialar S, Krumlauf R (1999) ‘Shocking’ developments in chick embryology: electroporation and in ovo gene expression. Nat Cell Biol 1:E203–E207

    Article  Google Scholar 

  • Jaenisch R (1988) Transgenic animals. Science 240:1468–1474

    Article  Google Scholar 

  • Kaestner L, Scholz A, Lipp P (2015) Conceptual and technical aspects of transfection and gene delivery. Bioorg Med Chem Lett 25:1171–1176

    Article  Google Scholar 

  • Kamdar KP, Wagner TN, Finnerly V (1995) Electroporation of Drosophila embryos. In: Nickoloff JA (ed) Animal cell electroporation and electrofusion protocols. Humana Press, Totowa, pp 239–243

    Chapter  Google Scholar 

  • Katahira T, Nakamura H (2003) Gene silencing in chick embryos with a vector-based small interfering RNA system. Develop Growth Differ 45:361–367

    Article  Google Scholar 

  • Kera SA, Agerwala SM, Horne JH (2010) The temporal resolution of in vivo electroporation in zebrafish: a method for time-resolved loss of function. Zebrafish 7:97–108

    Article  Google Scholar 

  • Kos R, Tucker RP, Hall R, Duong TD, Erickson CA (2003) Methods for introducing morpholinos into the chicken embryo. Dev Dyn 226:470–477

    Article  Google Scholar 

  • Kretzschmar K, Watt FM (2012) Lineage tracing. Cell 148:33–45

    Article  Google Scholar 

  • Krull CE (2004) A primer on using in ovo electroporation to analyze gene function. Dev Dyn 229:433–439

    Article  Google Scholar 

  • Kumar A, Godwin JW, Gates PB, Garza-Garcia AA, Brockes JP (2007) Molecular basis for the nerve dependence of limb regeneration in an adult vertebrate. Science 318:772–777

    Article  Google Scholar 

  • Le Douarin N, Dieterlen-Lièvre F, Creuzet S, Teillet MA (2008) Quail–chick transplantations. In: Bronner-Fraser M (ed) Avian embryology, 2nd edn. Academic, London, pp 19–58

    Chapter  Google Scholar 

  • Lee JM, Takahashi M, Mon H, Koga K, Kawaguchi Y, Kusakabe T (2005) Efficient gene transfer into silkworm larval tissues by a combination of sonoporation and lipofection. Cell Biol Int 29:976–979

    Article  Google Scholar 

  • Lee JM, Kim JY, Cho KW, Lee MJ, Cho SW, Kwak S, Cai J, Jung HS (2008) Wnt11/Fgfr1b cross-talk modulates the fate of cells in palate development. Dev Biol 314:341–350

    Article  Google Scholar 

  • Leopold RA, Hughes KJ, DeVault JD (1996) Using electroporation and a slot cuvette to deliver plasmid DNA to insect embryos. Genet Anal: Biomol Eng 12:197–200

    Article  Google Scholar 

  • Lin G, Chen Y, Slack JMW (2007) Regeneration of neural crest derivatives in the Xenopus tadpole tail. BMC Dev Biol 7:56

    Article  Google Scholar 

  • Matsuda T, Cepko CL (2007) Controlled expression of transgenes introduced by in vivo electroporation. Proc Natl Acad Sci U S A 104:1027–1032

    Article  Google Scholar 

  • Mazari E, Laniel J, Dubois G, Griffon S, Marty F, Perea-Gomez A, Gosse C (2010) Mouse embryo electroporation and culture in devices made by soft lithography. In: Verpoorte S, Andersson-Svahn H, Emnéus J, Pamme N (eds) Proceedings of the 14th international conference on miniaturized systems for chemistry and life sciences. CBMS, San Diego, pp 312–314

    Google Scholar 

  • Mazari E, Mantelet M, Iranzo J, Perea-Gomez A, Gosse C (2011) Localized electroporation of mouse embryo using dielectric guides. In: Digest of the technical papers of the 16th international conference on solid-state sensors, actuators, and microsystems. IEEE, Piscataway, pp 1172–1175

    Google Scholar 

  • Mazari E, Zhao X, Migeotte I, Collignon J, Gosse C, Perea-Gomez A (2014) A microdevice to locally electroporate embryos with high efficiency and reduced cell damage. Development 141:1–11

    Article  Google Scholar 

  • Mellitzer G, Hallonet M, Chen L, Ang SL (2002) Spatial and temporal ‘knock down’ of gene expression by electroporation of double-stranded RNA and morpholinos into early postimplantation mouse embryos. Mech Dev 118:57–63

    Article  Google Scholar 

  • Momose T, Tonegawa A, Takeuchi J, Ogawa H, Umesono K, Yasuda K (1999) Efficient targeting of gene expression in chick embryos by microelectroporation. Develop Growth Differ 41:335–344

    Article  Google Scholar 

  • Moto K, Salam SEA, Sakurai S, Iwami M (1999) Gene transfer into insect brain and cell-specific expression of Bombyxin gene. Dev Genes Evol 209:447–450

    Article  Google Scholar 

  • Müller F, Lele Z, Varadi L, Menczel L, Orban L (1993) Efficient transient expression system based on square pulse electroporation and in vivo luciferase assay of fertilized fish eggs. FEBS Lett 324:27–32

    Article  Google Scholar 

  • Murakami Y, Motohashi K, Yano K, Ikebukuro K, Yokoyama K, Tamiya E, Karube I (1994) Micromachined electroporation system for transgenic fish. J Biotechnol 34:35–42

    Article  Google Scholar 

  • Muramatsu T, Mizutani Y, Okumura J (1996) Live detection of the firefly luciferase gene expression by bioluminescence in incubating chicken embryos. Amin Sci Technol (Jpn) 67:906–909

    Google Scholar 

  • Muramatsu T, Mizutani Y, Ohmori Y, Okumura J (1997) Comparison of three nonviral transfection methods for foreign gene expression in early chicken embryos in ovo. Biochem Biophys Res Commun 230:376–380

    Article  Google Scholar 

  • Nakamura H (2009) Electroporation and sonoporation in developmental biology. Springer, Tokyo

    Book  Google Scholar 

  • Nakamura H, Funahashi J (2013) Electroporation: past, present and future. Develop Growth Differ 55:15–19

    Article  Google Scholar 

  • Oberg KC, Pira CU, Revelli JP, Ratz B, Aguilar-Cordova E, Eichele G (2002) Efficient ectopic gene expression targeting chick mesoderm. Dev Dyn 224:291–302

    Article  Google Scholar 

  • Odani N, Ito K, Nakamura H (2008) Electroporation as an efficient method of gene transfer. Develop Growth Differ 50:443–448

    Article  Google Scholar 

  • Ogura T (2002) In vivo electroporation: a new frontier for gene delivery and embryology. Differentiation 70:163–171

    Article  Google Scholar 

  • Ohta S, Suzuki K, Tachibana K, Yamada G (2003) Microbubble-enhanced sonoporation: efficient gene transduction technique for chick embryos. Genesis 37:91–101

    Article  Google Scholar 

  • Olofsson J, Nolkrantz K, Ryttsén F, Lambie BA, Weber SG, Orwar O (2003) Single-cell electroporation. Curr Opin Biotechnol 14:29–34

    Article  Google Scholar 

  • Olofsson J, Levin M, Strömberg A, Weber SG, Ryttsén F, Orwar O (2007) Scanning electroporation of selected areas of adherent cell cultures. Anal Chem 79:4410–4418

    Article  Google Scholar 

  • Paganin-Gioanni A, Bellard E, Escoffre JM, Rols MP, Teissié J, Golzio M (2011) Direct visualization at the single-cell level of siRNA electrotransfer into cancer cells. Proc Natl Acad Sci U S A 108:10443–10447

    Article  Google Scholar 

  • Pekarik V, Bourikas D, Miglino N, Joset P, Preiswerk S, Stoeckli ET (2003) Screening for gene function in chicken embryo using RNAi and electroporation. Nat Biotechnol 21:93–96

    Article  Google Scholar 

  • Peng H, Wu Y, Zhang Y (2012) Efficient delivery of DNA and morpholinos into mouse preimplantation embryos by electroporation. PLoS One 7:e43748

    Article  Google Scholar 

  • Powers DA, Hereford L, Cole T, Chen TT, Lin CM, Kight K, Creech K, Dunham R (1992) Electroporation: a method for transferring genes into the gametes of zebrafish (Brachydanio rerio), channel catfish (Ictalurus punctatus), and common carp (Cyprinus carpio). Mol Mar Biol Biotechnol 1:301–308

    Google Scholar 

  • Pu H, Young AP (1990) Glucocorticoid-inducible expression of a glutamine synthetase-CAT-encoding fusion plasmid after transfection of intact chicken retinal explant cultures. Gene 89:259–263

    Article  Google Scholar 

  • Quinlan GA, Khoo PL, Wong N, Trainor PA, Tam PPL (2008) Cell grafting and labeling in postimplantation mouse embryos. In: Sharpe P, Mason I (eds) Molecular embryology: methods and protocols, 2nd edn. Humana Press, New-York, pp 47–70

    Google Scholar 

  • Saito T (2006) In vivo electroporation in the embryonic mouse central nervous system. Nat Protoc 1:1552–1558

    Article  Google Scholar 

  • Saito T, Nakatsuji N (2001) Efficient gene transfer into the embryonic mouse brain using in vivo electroporation. Dev Biol 240:237–246

    Article  Google Scholar 

  • Sakai D, Trainor PA (2014) Gene transfer techniques in whole embryo cultured post-implantation mouse embryos. In: Lewandoski M (ed) Mouse molecular embryology. Humana Press, New-York, pp 227–234

    Chapter  Google Scholar 

  • Sasagawa S, Takabatake T, Takabatake Y, Muramatsu T, Takeshima K (2002) Improved mRNA electroporation method for Xenopus neurula embryos. Genesis 33:81–85

    Article  Google Scholar 

  • Sasaki H, Yoshida K, Hozumi A, Sasakura Y (2014) CRISPR/Cas9-mediated gene knockout in the ascidian Ciona intestinalis. Develop Growth Differ 56:499–510

    Article  Google Scholar 

  • Sato M, Ohtsuka M, Watanabe S, Gurumurthy CB (2016) Nucleic acids delivery methods for genome editing in zygotes and embryos: the old, the new, and the old-new. Biol Direct 11:16

    Article  Google Scholar 

  • Sauka-Spengler T, Barembaum M (2008) Gain- and loss-of-function approaches in the chick embryo. In: Bronner-Fraser M (ed) Avian embryology, 2nd edn. Academic, London, pp 237–256

    Chapter  Google Scholar 

  • Scaal M, Gros J, Lesbros C, Marcelle C (2004) In ovo electroporation of avian somites. Dev Dyn 229:643–650

    Article  Google Scholar 

  • Semple-Rowland SL, Berry J (2014) Use of lentiviral vectors to deliver and express bicistronic transgenes in developing chicken embryos. Methods 66:466–473

    Article  Google Scholar 

  • Shaner NC, Campbell RE, Steinbach PA, Giepmans BNG, Palmer AE, Tsien RY (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp red fluorescent protein. Nat Biotechnol 22:1567–1572

    Article  Google Scholar 

  • Sharpe P, Mason I (2008) Molecular embryology: methods and protocols, 2nd edn. Humana Press, New-York

    Google Scholar 

  • Shin MK, Levorse JM, Ingram RS, Tilghman SM (1999) The temporal requirement for endothelin receptor-B signalling during neural crest development. Nature 402:496–501

    Article  Google Scholar 

  • Simkin JE, McKeown SJ, Newgreen DF (2009) Focal electroporation in ovo. Dev Dyn 238:3152–3155

    Article  Google Scholar 

  • Simkin JE, Zhang D, Ighaniyan S, Newgreen DF (2014) Parameters affecting efficiency of in ovo electroporation of the avian neural tube and crest. Dev Dyn 243:1440–1447

    Article  Google Scholar 

  • Skachkov I, Luan Y, van der Steen AFW, de Jong N, Kooiman K (2014) Targeted microbubble mediated sonoporation of endothelial cells in vivo. IEEE Trans Ultrason Ferroelectr Freq Control 61:1661–1667

    Article  Google Scholar 

  • Slack JMW (2006) Essential developmental biology, 2nd edn. Blackwell, Malden

    Google Scholar 

  • Smith KM, Gee L, Bode HR (2000) HyAlx, an aristaless-related gene, is involved in tentacle formation in hydra. Development 127:4743–4752

    Google Scholar 

  • Soares ML, Haraguchi S, Torres-Padilla ME, Kalmar T, Carpenter L, Bell G, Morrison A, Ring CJA, Clarke NJ, Glover DM, Zernicka-Goetz M (2005) Functional studies of signaling pathways in peri-implantation development of the mouse embryo by RNAi. BMC Dev Biol 5:28

    Article  Google Scholar 

  • Soares ML, Torres-Padilla ME, Zernicka-Goetz M (2008) Bone morphogenetic protein 4 signaling regulates development of the anterior visceral endoderm in the mouse embryo. Develop Growth Differ 50:615–621

    Article  Google Scholar 

  • Spemann H, Mangold H (1924) Über die Induktion von Embryonalanlagen durch Implantation artfremder Organisatoren. W Roux’ Arch f Entw d Organis u mikrosk Anat 100:599–638. Translated and reprinted as: Spemann H, Mangold H (2001) Induction of embryonic primordia by implantation of organizers from different species. Int J Dev Biol 45:13–38

    Google Scholar 

  • Stark DA, Kulesa PM (2007) An in vivo comparison of photoactivatable fluorescent proteins in an avian embryo model. Dev Dyn 236:1583–1594

    Article  Google Scholar 

  • Stern CD, Fraser SE (2001) Tracing the lineage of tracing cell lineages. Nat Cell Biol 3:E216–E218

    Article  Google Scholar 

  • Stern CD, Ireland GW, Herrick SE, Gherardi E, Gray J, Perryman M, Stoker M (1990) Epithelial scatter factor and development of the chick embryonic axis. Development 110:1271–1284

    Google Scholar 

  • Stolfi A, Gandhi S, Salek F, Christiaen L (2014) Tissue-specific genome editing in Ciona embryos by CRISPR/Cas9. Development 141:4115–4120

    Article  Google Scholar 

  • Streit A, Tambalo M, Chen J, Grocott T, Anwar M, Sosinsky A, Stern CD (2013) Experimental approaches for gene regulatory network construction: the chick as a model system. Genesis 51:296–310

    Article  Google Scholar 

  • Svingen T, Wilhelm D, Combes AN, Hosking B, Harley VR, Sinclair AH, Koopman P (2009) Ex vivo magnetofection: a novel strategy for the study of gene function in mouse organogenesis. Dev Dyn 238:956–964

    Article  Google Scholar 

  • Swartz M, Eberhart J, Mastick GS, Krull CE (2001) Sparking new frontiers: using in vivo electroporation for genetic manipulations. Dev Biol 233:13–21

    Article  Google Scholar 

  • Tabata H, Nakajima K (2001) Efficient in utero gene transfer system to the developing mouse brain using electroporation: visualization of neuronal migration in the developing cortex. Neuroscience 103:865–872

    Article  Google Scholar 

  • Takahashi M, Nomura T, Osumi N (2008a) Transferring genes into cultured mammalian embryos by electroporation. Develop Growth Differ 50:485–497

    Article  Google Scholar 

  • Takahashi Y, Watanabe T, Nakagawa S, Kawakami K, Sato Y (2008b) Transposon-mediated stable integration and tetracycline-inducible expression of electroporated transgenes in chicken embryos. In: Bronner-Fraser M (ed) Avian embryology, 2nd edn. Academic, London, pp 271–280

    Chapter  Google Scholar 

  • Tanaka SS, Yamaguchi YL, Jones VJ, Tam PPL (2014) Analyzing gene function in whole mouse embryo and fetal organ in vitro. In: Lewandoski M (ed) Mouse molecular embryology. Humana Press, New-York, pp 367–393

    Chapter  Google Scholar 

  • Tawk M, Tuil D, Torrente Y, Vriz S, Paulin D (2002) High-efficiency gene transfer into adult fish: a new tool to study fin regeneration. Genesis 32:27–31

    Article  Google Scholar 

  • Tawk M, Bianco IS, Clarke JDW (2009) Focal electroporation in zebrafish embryos and larvae. In: Lieschke GJ, Oates AC, Kawakami K (eds) Zebrafish: methods and protocols. Humana Press, Dordrecht, pp 145–151

    Chapter  Google Scholar 

  • Teh C, Chong SW, Korzh V (2003) DNA delivery into anterior neural tube of zebrafish embryos by electroporation. BioTechniques 35:950–954

    Google Scholar 

  • Thomas JL (2003) Electroporation, an alternative to biolistics for transfection of Bombyx mori embryos and larval tissues. J Insect Sci 3:17

    Article  Google Scholar 

  • Thomas JL, Bardou J, L’hoste S, Mauchamp B, Chavancy G (2001) A helium burst biolistic device adapted to penetrate fragile insect tissues. J Insect Sci 1:9

    Article  Google Scholar 

  • Tsunekawa Y, Terhune RK, Fujita I, Shitamukai A, Suetsugu T, Matsuzaki F (2016) Developing a de novo targeted knock-in method based on in utero electroporation into the mammalian brain. Development 143:3216–3222

    Article  Google Scholar 

  • Véron N, Qu Z, Kipen PAS, Hirst CE, Marcelle C (2015) CRISPR mediated somatic cell genome engineering in the chicken. Dev Biol 407:68–74

    Article  Google Scholar 

  • Voiculescu O, Papanayotou C, Stern CD (2008) Spatially and temporally controlled electroporation of early chick embryos. Nat Protoc 3:419–426

    Article  Google Scholar 

  • Wang S, Lee LJ (2013) Micro-/nanofluidics cell electroporation. Biomicrofluidics 7:011301

    Article  Google Scholar 

  • Zhao X, Mazari E, Suárez-Boomgaard D, Migeotte I, Perea-Gomez A, Gosse C (2014) Finite element model simulations to assist the design of microdevices dedicated to the localized electroporation of mouse embryos. ECS Trans 64:7–14

    Article  Google Scholar 

Download references

Acknowledgments

This book chapter was written in the context of collaborative research projects funded by the grants “ElectroMice” (CNRS PI: Physique Chimie Biologie 2008), “ElectroTagMam” (Cnano IdF 2011), “ElectroDev” (PHC Tournesol 2014), and “RhoGTPases and collective migration” (FNRS MIS 2013).

Author information

Authors and Affiliations

  1. Laboratoire de Photonique et de Nanostructures, LPN-CNRS, Route de Nozay, 91460, Marcoussis, France

    Charlie Gosse & Xuan Zhao

  2. Institut de Recherche Interdisciplinaire en Biologie Humaine et Moléculaire, Université Libre de Bruxelles, Campus Erasme, ULB CP602, route de Lennik 808, 1070, Bruxelles, Belgium

    I. Migeotte & Diana Suárez-Boomgaard

  3. Biologie du Développement et Reproduction, UMR 1198 INRA, ENVA, Université Paris-Saclay, 78352, Cedex, Jouy-en-Josas, France

    Isabelle Hue

  4. Physiopathologie et Pharmacotoxicologie Placentaire Humaine, INSERM UMR-S1139, Université Paris Descartes, Sorbonne Paris Cité, 4 avenue de l’Observatoire, 75006, Paris, France

    Séverine Degrelle

  5. Institut de Biologie Valrose, CNRS UMR7277, Inserm U1091, Université Nice Sophia Antipolis, Parc Valrose, 06108, Cedex 2, Nice, France

    Aitana Perea-Gomez

  6. Center for International Research on MicroMechatronics, Institute of Industrial Science, The University of Tokyo, 4-6-1 Komaba, Meguro-ku, Tokyo, 153-8505, Japan

    E. Mazari

Authors
  1. Charlie Gosse
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xuan Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. I. Migeotte
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Diana Suárez-Boomgaard
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Isabelle Hue
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Séverine Degrelle
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Aitana Perea-Gomez
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. E. Mazari
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Charlie Gosse .

Editor information

Editors and Affiliations

  1. Faculty of Electrical Engineering, University of Ljubljana, Ljubljana, Slovenia

    Damijan Miklavčič

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this entry

Cite this entry

Gosse, C. et al. (2017). The Use of Electroporation in Developmental Biology. In: Miklavčič, D. (eds) Handbook of Electroporation. Springer, Cham. https://doi.org/10.1007/978-3-319-32886-7_139

Download citation

Publish with us

Policies and ethics

Societies and partnerships

Search

Navigation