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Sonoporation in Developmental Biology

  • Sho Ohta
  • Kentaro Suzuki
  • Shinichi Miyagawa
  • Yukiko Ogino
  • Mylah Villacorte
  • Yoshihiro Wada
  • Gen Yamada

Recent, molecular biology techniques have accomplished a large contribution to developmental biology. Especially, gene transduction techniques are indispensable to study the roles of regulatory genes underlying embryogenesis.

Replication-competent retroviruses, transfection with lipofection and an in ovo electroporation have been established as gene transduction techniques for embryos. (Yamada et al., 1997; Muramatsu et al., 1998; Fukuda et al., 2000; Iba, 2000; Nakamura et al., 2000). Particularly, in ovo electroporation for chick embryos has been recognized as a powerful method to efficiently induce exogenous genes into target cells or tissues, and it has been widely utilized to investigate their functions during embryonic development. Because the electric current tend to affect mainly the epithelial cells of the embryo, in ovo electroporation is suitable for the studies of neurogenesis and neuronal differentiation. In fact, large number of information relating to neuronal development has been brought from the studies using in ovo electroporation (Okafuji et al., 1999; Nakamura and Funahashi, 2001).

Keywords

Chick Embryo Primitive Streak Gene Transduction Ultrasound Exposure High Ultrasound Intensity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Bachiller, D., Klingensmith, J., Kemp, C., Belo, J. A., Anderson, R. M., May, S. R., McMahon, J. A., McMahon, A. P., Harland, R. M., Rossant, J., De Robertis, E. M. (2000). The organizer factors Chordin and Noggin are required for mouse forebrain development. Nature 403, 658–61.CrossRefGoogle Scholar
  2. Bao, S., Thrall, B. D., Miller, D. L. (1997). Transfection of a reporter plasmid into cultured cells by sonoporation in vitro. Ultrasound Med Biol 23, 953–959.CrossRefGoogle Scholar
  3. Brunet, L. J., McMahon, J. A., McMahon, A. P., Harland, R. M. (1998). Noggin, cartilage mor phogenesis, and joint formation in the mammalian skeleton. Science 280, 1455–7.CrossRefGoogle Scholar
  4. Catala, M., Teillet, M. A., Le Douarin, N. M. (1995). Organization and development of the tail bud analyzed with the quail-chick chimaera system. Mech Dev 51, 51–65.CrossRefGoogle Scholar
  5. Chuai, M., Zeng, W., Yang, X., Boychenko, V., Glazier, J. A., Weijer, C. J. (2006). Cell movement during chick primitive streak formation. Dev Biol 296, 137–49.CrossRefGoogle Scholar
  6. 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. Dev Growth Differ 42, 207–11. Review.CrossRefGoogle Scholar
  7. Haraguchi, R., Suzuki, K., Murakami, R., Sakai, M., Kamikawa, M., Kengaku, M., Sekine, K., Kawano, H., Kato, S., Ueno, N., Yamada, G. (2000). Molecular analysis of external genitalia formation: the role of fibroblast growth factor (Fgf) genes during genital tubercle formation. Development 127, 2471–9.Google Scholar
  8. Iba, H. (2000) Gene transfer into chicken embryos by retrovirus vectors. Dev Growth Differ 42, 213–8. Review.CrossRefGoogle Scholar
  9. Kim, H. J., Greenleaf, J. F., Kinnick, R. R., Bronk, J. T., Bolander, M. E. (1996) Ultrasound-mediated transfection of mammalian cells. Hum Gene Ther 7, 1339–46.CrossRefGoogle Scholar
  10. Koch, S., Pohl, P., Cobet, U., Rainov, N. G. (2000) Ultrasound enhancement of liposome-mediated cell transfection is caused by cavitation effects. Ultrasound Med Biol 26, 897–903.CrossRefGoogle Scholar
  11. Komatsu, Y., Scott, G., Nagy, A., Kaartinen, V., Mishina, Y. (2007). BMP type I receptor ALK2 is essential for proper patterning at late gastrulation during mouse embryogenesis. Dev Dyn 236, 512–7.CrossRefGoogle Scholar
  12. Lawson, A., Schoenwolf, G. C. (2001). Cell populations and morphogenetic movements underly ing formation of the avian primitive streak and organizer. Genesis 29, 188–95.CrossRefGoogle Scholar
  13. Liem, K. F., Jr., Tremml, G., Roelink, H., Jessell, T. M. (1995). Dorsal differentiation of neural plate cells induced by BMP-mediated signals from epidermal ectoderm. Cell 82, 969–79.CrossRefGoogle Scholar
  14. Liu, J. P., Jessell, T. M. (1998). A role for rhoB in the delamination of neural crest cells from the dorsal neural tube. Development 125, 5055–67.Google Scholar
  15. McMahon, J. A., Takada, S., Zimmerman, L. B., Fan, C. M., Harland, R. M., McMahon, A. P. (1998). Noggin-mediated antagonism of BMP signaling is required for growth and patterning of the neural tube and somite. Genes Dev 12, 1438–52.CrossRefGoogle Scholar
  16. Mishina, Y., Suzuki, A., Ueno, N., Behringer, R. R. (1995). Bmpr encodes a type I bone morpho-genetic protein receptor that is essential for gastrulation during mouse embryogenesis. Genes Dev 9, 3027–37.CrossRefGoogle Scholar
  17. Muramatsu, T., Nakamura, A., Park, H. M. (1998) In vivo electroporation: a powerful and con venient means of nonviral gene transfer to tissues of living animals. Int J Mol Med 1, 55–62. Review.Google Scholar
  18. Nakamura, H., Funahashi, J. (2001) Introduction of DNA into chick embryos by in ovo electro poration. Methods 24, 43–8.CrossRefGoogle Scholar
  19. Nakamura, H., Watanabe, Y., Funahashi, J. (2000) Misexpression of genes in brain vesicles by in ovo electroporation. Dev Growth Differ 42, 199–201. Review.CrossRefGoogle Scholar
  20. Newman, C. M., Lawrie, A., Brisken, A. F., Cumberland, D. C. (2001) Ultrasound gene therapy: on the road from concept to reality. Echocardiography 18, 339–47.CrossRefGoogle Scholar
  21. Ohta, S., Suzuki, K., Tachibana, K., Yamada, G. (2003) Microbubble-enhanced sonoporation: efficient gene transduction technique for chick embryos. Genesis 37, 91–101.CrossRefGoogle Scholar
  22. Ohta, K., Lupo, G., Kuriyama, S., Keynes, R., Holt, C. E., Harris, W. A., Tanaka, H., Ohnuma, S. (2004). Tsukushi functions as an organizer inducer by inhibition of BMP activity in coopera tion with chordin. Dev Cell 7, 347–58.CrossRefGoogle Scholar
  23. Ohta, S., Ogino, Y., Suzuki, K., Kaminura, M., Tachibana, K., Tamada, G. (2007a) Sonoporation: an efficient technique for the introduction of genes into chick embryos: Gene Transfer (eds. T. Friedmann and J. Rossi), pp. 711–16. Cold Spring Harbor Laboratory Press, New York, USA.Google Scholar
  24. Ohta S., Suzuki K., Tachibana K., Tanaka H., Yamada G. (2007b) Cessation of gastrulation is mediated by suppression of epithelial-mesenchymal transition at the ventral ectodermal ridge. Development 134, 4315–24.CrossRefGoogle Scholar
  25. Okafuji, T., Funahashi J., Nakamura H. (1999) Roles of Pax-2 in initiation of the chick tectal development. Brain Res Dev Brain Res 116, 41–9.CrossRefGoogle Scholar
  26. Sakai, D., Tanaka, Y., Endo, Y., Osumi, N., Okamoto, H., Wakamatsu, Y. (2005). Regulation of Slug transcription in embryonic ectoderm by beta-catenin-Lef/Tcf and BMP-Smad signaling. Dev Growth Differ 47, 471–82.CrossRefGoogle Scholar
  27. Schoenwolf, G. C. (1981). Morphogenetic processes involved in the remodeling of the tail region of the chick embryo. Anat Embryol (Berl) 162, 183–97.CrossRefGoogle Scholar
  28. Shook, D., Keller, R. (2003). Mechanisms, mechanics and function of epithelial-Mesenchymal transitions in early development. Mech Dev 120, 1351–83.CrossRefGoogle Scholar
  29. Suzuki, K., Bachiller, D., Chen, Y. P., Kamikawa, M., Ogi, H., Haraguchi, R., Ogino, Y., Minami, Y., Mishina, Y., Ahn, K., Crenshaw, EB III, Yamada, G. (2003). Regulation of outgrowth and apoptosis for the terminal appendage: external genitalia development by con certed actions of BMP signaling [corrected]. Development 130, 6209–20.CrossRefGoogle Scholar
  30. Tachibana, K., Tachibana, S. (1995) Albumin microbubble echo-contrast material as an enhancer for ultrasound accelerated thrombolysis. Circulation 92,1148–50.Google Scholar
  31. Tachibana, K., Tachibana, S. (2001) The use of ultrasound for drug delivery. Echocardiography 18, 323–8.CrossRefGoogle Scholar
  32. Tam, P. P., Beddington, R. S. (1987). The formation of mesodermal tissues in the mouse embryo during gastrulation and early organogenesis. Development 99, 109–26.Google Scholar
  33. Taniyama, Y., Tachibana, K., Hiraoka, K., Namba, T., Yamasaki, K., Hashiya, N., Aoki, M., Ogihara, T., Yasufumi, K., Morishita, R. (2002) Local delivery of plasmid DNA into rat carotid artery using ultrasound. Circulation 105:1233–39.CrossRefGoogle Scholar
  34. Wasan, E. K., Reimer, D. L., Bally, M. B. (1996) Plasmid DNA is protected against ultrasonic cavitation-induced damage when complexed to cationic liposomes. J Pharm Sci 85, 427–33.CrossRefGoogle Scholar
  35. Wilson, V., Beddington, R. S. (1996). Cell fate and morphogenetic movement in the late mouse primitive streak. Mech Dev 55, 79–89.CrossRefGoogle Scholar
  36. Xu, Z., Raghavan, M., Hall, T. L., Chang, C. W., Mycek, M. A., Fowlkes, J. B., Cain, C. A. (2007) High speed imaging of bubble clouds generated in pulsed ultrasound cavitational therapy — histotripsy. IEEE Trans Ultrason Ferroelectr Freq Control 54, 2091–101.CrossRefGoogle Scholar
  37. Yamada, G., Nakamura, S., Haraguchi, R., Sakai, M., Terashi, T., Sakisaka, S., Toyoda, T., Ogino, Y., Hatanaka, H., Kaneda, Y. (1997) An efficient liposome-mediated gene transfer into the branchial arch, neural tube and the heart of chick embryos: a strategy to elucidate the organogenesis. Cell Mol Biol (Noisy-le-grand) 43, 1165–9.Google Scholar

Copyright information

© Springer 2009

Authors and Affiliations

  • Sho Ohta
    • 2
  • Kentaro Suzuki
    • 1
  • Shinichi Miyagawa
    • 1
  • Yukiko Ogino
    • 1
  • Mylah Villacorte
    • 1
  • Yoshihiro Wada
    • 3
  • Gen Yamada
    • 1
  1. 1.Center for Animal Resources and Development (CARD), Graduate School of Medical and Pharmaceutical SciencesKumamoto UniversityKumamotoJapan
  2. 2., Department of Neurobiology and AnatomyUniversity of Utah, School of MedicineSalt Lake CityUSA
  3. 3.Department of Urology, Graduate School of Medical SciencesKumamoto UniversityKumamotoJapan

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