Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
권호 표지
DOI QR코드

DOI QR Code

Germline Modification and Engineering in Avian Species

  • Lee, Hong Jo (Department of Agricultural Biotechnology, College of Agriculture and Life Sciences, and Research Institute of Agriculture and Life Sciences, Seoul National University) ;
  • Lee, Hyung Chul (Department of Cell and Developmental Biology, University College London) ;
  • Han, Jae Yong (Department of Agricultural Biotechnology, College of Agriculture and Life Sciences, and Research Institute of Agriculture and Life Sciences, Seoul National University)
  • Received : 2015.08.21
  • Accepted : 2015.08.27
  • Published : 2015.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

Production of genome-edited animals using germline-competent cells and genetic modification tools has provided opportunities for investigation of biological mechanisms in various organisms. The recently reported programmed genome editing technology that can induce gene modification at a target locus in an efficient and precise manner facilitates establishment of animal models. In this regard, the demand for genome-edited avian species, which are some of the most suitable model animals due to their unique embryonic development, has also increased. Furthermore, germline chimera production through longterm culture of chicken primordial germ cells (PGCs) has facilitated research on production of genome-edited chickens. Thus, use of avian germline modification is promising for development of novel avian models for research of disease control and various biological mechanisms. Here, we discuss recent progress in genome modification technology in avian species and its applications and future strategies.

Keywords

References

  1. Carsience, R.S., Clark, M.E., Verrinder Gibbins, A.M., and Etches, R.J. (1993). Germline chimeric chickens from dispersed donor blastodermal cells and compromised recipient embryos. Development 117, 669-675.
  2. Chang, I.K., Jeong, D.K., Hong, Y.H., Park, T.S., Moon, Y.K., Ohno, T., and Han, J.Y. (1997) Production of germline chimeric chickens by transfer of cultured primordial germ cells. Cell Biol. Int. 21, 495-499. https://doi.org/10.1006/cbir.1997.0173
  3. Cheon, D.J., and Orsulic, S. (2011). Mouse models of cancer. Annu. Rev. Pathol. 6, 95-119. https://doi.org/10.1146/annurev.pathol.3.121806.154244
  4. Choi, J.W., Kim, S., Kim, T.M., Kim, Y.M., Seo, H.W., Park, T.S., Jeong, J.W., Song, G., and Han, J.Y. (2010). Basic fibroblast growth factor activates MEK/ERK cell signaling pathway and stimulates the proliferation of chicken primordial germ cells. PLoS One 5, e12968. https://doi.org/10.1371/journal.pone.0012968
  5. Christian, M., Cermak, T., Doyle, E.L., Schmidt, C., Zhang, F., Hummel, A., Bogdanove, A.J., and Voytas, D.F. (2010). Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 186, 757-761. https://doi.org/10.1534/genetics.110.120717
  6. Cohen, S.N., Chang, A.C., Boyer, H.W., and Helling, R.B. (1973). Construction of biologically functional bacterial plasmids in vitro. Proc. Natl. Acad. Sci. USA 70, 3240-3244. https://doi.org/10.1073/pnas.70.11.3240
  7. Dove, A. (2000). Milking the genome for profit. Nat. Biotechnol. 18, 1045-1048. https://doi.org/10.1038/80231
  8. Evans, M.J., and Kaufman, M.H. (1981). Establishment in culture of pluripotential cells from mouse embryos. Nature 292, 154-156. https://doi.org/10.1038/292154a0
  9. Eyal-Giladi, H., and Kochav, S. (1976). From cleavage to primitive streak formation: a complementary normal table and a new look at the first stages of the development of the chick. I. General morphology. Dev. Biol. 49, 321-337. https://doi.org/10.1016/0012-1606(76)90178-0
  10. Hamburger, V., and Hamilton, H.L. (1992). A series of normal stages in the development of the chick embryo. 1951. Dev. Dyn. 195, 231-272. https://doi.org/10.1002/aja.1001950404
  11. Han, J.Y. (2009). Germ cells and transgenesis in chickens. Comp. Immunol. Microbiol. Infect. Dis. 32, 61-80. https://doi.org/10.1016/j.cimid.2007.11.010
  12. Han, J.Y., Park, T.S., Hong, Y.H., Jeong, D.K., Kim, J.N., Kim, K.D., and Lim, J.M. (2002). Production of germline chimeras by transfer of chicken gonadal primordial germ cells maintained in vitro for an extended period. Theriogenology 58, 1531-1539. https://doi.org/10.1016/S0093-691X(02)01061-0
  13. Han, J.Y., Lee, H.C., and Park, T.S. (2015). Germline-competent stem cells in avian species and its application. Asian J. Androl. 17, 421-426.
  14. Hawkridge, A.M. (2014). The chicken model of spontaneous ovarian cancer. Proteomics Clin. Appl. 8, 689-699. https://doi.org/10.1002/prca.201300135
  15. Jean, C., Aubel, P., Soleihavoup, C., Bouhallier, F., Voisin, S., Lavial, F., and Pain, B. (2013). Pluripotent genes in avian stem cells. Dev. Growth Differ. 55, 41-51. https://doi.org/10.1111/dgd.12021
  16. Kaletta, T., and Hengartner, M.O. (2006). Finding function in novel targets: C. elegans as a model organism. Nat. Rev. Drug Discov. 5, 387-398. https://doi.org/10.1038/nrd2031
  17. Kamihira, M., Ono, K., Esaka, K., Nishijima, K., Kigaku, R., Komatsu, H., Yamashita, T., Kyogoku, K., and Iijima, S. (2005). Highlevel expression of single-chain Fv-Fc fusion protein in serum and egg white of genetically manipulated chickens by using a retroviral vector. J. Virol. 79, 10864-10874. https://doi.org/10.1128/JVI.79.17.10864-10874.2005
  18. Kamihira, M., Kawabe, Y., Shindo, T., Ono, K., Esaka, K., Yamashita, T., Nishijima, K., and Iijima, S. (2009). Production of chimeric monoclonal antibodies by genetically manipulated chickens. J. Biotechnol. 141, 18-25. https://doi.org/10.1016/j.jbiotec.2009.02.022
  19. Kanatsu-Shinohara, M., Ogonuki, N., Inoue, K., Miki, H., Ogura, A., Toyokuni, S., and Shinohara, T. (2003). Long-term proliferation in culture and germline transmission of mouse male germline stem cells. Biol. Reprod. 69, 612-616. https://doi.org/10.1095/biolreprod.103.017012
  20. Kanatsu-Shinohara, M., Morimoto, H., and Shinohara, T. (2012). Enrichment of mouse spermatogonial stem cells by melanoma cell adhesion molecule expression. Biol. Reprod. 87, 139. https://doi.org/10.1095/biolreprod.112.103861
  21. Kim, H., and Kim, J.S. (2014). A guide to genome engineering with programmable nucleases. Nat. Rev. Genet. 15, 321-334. https://doi.org/10.1038/nrg3686
  22. Koo, T., Lee, J., and Kim, J.S. (2015). Measuring and reducing Offtarget activities of programmable nucleases including CRISPRCas9. Mol. Cells 38, 475-481. https://doi.org/10.14348/molcells.2015.0103
  23. Lee, Y.M., Jung, J.G., Kim, J.N., Park, T.S., Kim, T.M., Shin, S.S., Kang, D.K., Lim, J.M., and Han, J.Y. (2006). A testis-mediated germline chimera production based on transfer of chicken testicular cells directly into heterologous testes. Biol. Reprod. 75, 380-386. https://doi.org/10.1095/biolreprod.106.052084
  24. Lee, S.I., Lee, B.R., Hwang, Y.S., Lee, H.C., Rengaraj, D., Song, G., Park, T.S., and Han, J.Y. (2011). MicroRNA-mediated posttranscriptional regulation is required for maintaining undifferentiated properties of blastoderm and primordial germ cells in chickens. Proc. Natl. Acad. Sci. USA 108, 10426-10431. https://doi.org/10.1073/pnas.1106141108
  25. Lieschke, G.J., and Currie, P.D. (2007). Animal models of human disease: zebrafish swim into view. Nat. Rev. Genet. 8, 353-367. https://doi.org/10.1038/nrg2091
  26. Lillico, S.G., Sherman, A., McGrew, M.J., Robertson, C.D., Smith, J., Haslam, C., Barnard, P., Radcliffe, P.A., Mitrophanous, K.A., Elliot, E.A., et al. (2007). Oviduct-specific expression of two therapeutic proteins in transgenic hens. Proc. Natl. Acad. Sci. USA 104, 1771-1776. https://doi.org/10.1073/pnas.0610401104
  27. Lim, J.J., Seol, D.W., Choi, K.H., Shin, D.H., Kim, H.J., Song, S.H., and Lee, D.R. (2014). Spermatogonial stem cell enrichment using simple grafting of testis and in vitro cultivation. Sci. Rep. 4, 5923.
  28. Lyall, J., Irvine, R.M., Sherman, A., McKinley, T.J., Nunez, A., Purdie, A., Outtrim, L., Brown, I.H., Rolleston-Smith, G., Sang, H., et al. (2011). Suppression of avian influenza transmission in genetically modified chickens. Science 331, 223-226. https://doi.org/10.1126/science.1198020
  29. Macdonald, J., Glover, J.D., Taylor, L., Sang, H.M., and McGrew, M.J. (2010). Characterisation and germline transmission of cultured avian primordial germ cells. PLoS One 5, e15518. https://doi.org/10.1371/journal.pone.0015518
  30. Macdonald, J., Taylor, L., Sherman, A., Kawakami, K., Takahashi, Y., Sang, H.M., and McGrew, M.J. (2012). Efficient genetic modification and germ-line transmission of primordial germ cells using piggyBac and Tol2 transposons. Proc. Natl. Acad. Sci. USA 109, E1466-1472. https://doi.org/10.1073/pnas.1118715109
  31. Mali, P., Yang, L., Esvelt, K.M., Aach, J., Guell, M., DiCarlo, J.E., Norville, J.E., and Church, G.M. (2013). RNA-guided human genome engineering via Cas9. Science 339, 823-826. https://doi.org/10.1126/science.1232033
  32. Maruyama, T., Dougan, S.K., Truttmann, M.C., Bilate, A.M., Ingram, J.R., and Ploegh, H.L. (2015). Increasing the efficiency of precise genome editing with CRISPR-Cas9 by inhibition of nonhomologous end joining. Nat. Biotechnol. 33, 538-542. https://doi.org/10.1038/nbt.3190
  33. Matsui, Y., Zsebo, K., and Hogan, B.L. (1992). Derivation of pluripotential embryonic stem cells from murine primordial germ cells in culture. Cell 70, 841-847. https://doi.org/10.1016/0092-8674(92)90317-6
  34. McMahon, M.A., Rahdar, M., and Porteus, M. (2012). Gene editing: not just for translation anymore. Nat. Methods 9, 28-31.
  35. Mizuarai, S., Ono, K., Yamaguchi, K., Nishijima, K., Kamihira, M., and Iijima, S. (2001). Production of transgenic quails with high frequency of germ-line transmission using VSV-G pseudotyped retroviral vector. Biochem. Biophys. Res. Commun. 286, 456-463. https://doi.org/10.1006/bbrc.2001.5422
  36. Musunuru, K. (2013). Genome editing of human pluripotent stem cells to generate human cellular disease models. Dis. Model Mech. 6, 896-904. https://doi.org/10.1242/dmm.012054
  37. Naito, M., Tajima, A., Yasuda, Y., and Kuwana, T. (1994). Production of germline chimeric chickens, with high transmission rate of donor-derived gametes, produced by transfer of primordial germ cells. Mol. Reprod. Dev. 39, 153-161. https://doi.org/10.1002/mrd.1080390206
  38. Nakamura, Y., Usui, F., Ono, T., Takeda, K., Nirasawa, K., Kagami, H., and Tagami, T. (2010). Germline replacement by transfer of primordial germ Cells into partially sterilized embryos in the chicken. Biol. Reprod. 83, 130-137. https://doi.org/10.1095/biolreprod.110.083923
  39. Nieuwkoop, P.D., and Sutasurya, L.A. (1979). Primordial germ cells in the chordates: embryogenesis and phylogenesis. (Cambridge Eng.; New York: Cambridge University Press).
  40. O'Connell, M.R., Oakes, B.L., Sternberg, S.H., East-Seletsky, A., Kaplan, M., and Doudna, J.A. (2014). Programmable RNA recognition and cleavage by CRISPR/Cas9. Nature 516, 263-266. https://doi.org/10.1038/nature13769
  41. Ogura, A., Inoue, K., and Wakayama, T. (2013). Recent advancements in cloning by somatic cell nuclear transfer. Philos. Trans. R Soc. Lond. B Biol. Sci. 368, 20110329.
  42. Ono, T., Matsumoto, T., and Arisawa, Y. (1998). Production of donor-derived offspring by transfer of primordial germ cells in Japanese quail. Exp. Anim. 47, 215-219. https://doi.org/10.1538/expanim.47.215
  43. Pain, B., Clark, M.E., Shen, M., Nakazawa, H., Sakurai, M., Samarut, J., and Etches, R.J. (1996). Long-term in vitro culture and characterisation of avian embryonic stem cells with multiple morphogenetic potentialities. Development 122, 2339-2348.
  44. Park, T.S., and Han, J.Y. (2012). piggyBac transposition into primordial germ cells is an efficient tool for transgenesis in chickens. Proc. Natl. Acad. Sci. USA 109, 9337-9341. https://doi.org/10.1073/pnas.1203823109
  45. Park, T.S., Hong, Y.H., Kwon, S.C., Lim, J.M., and Han, J.Y. (2003a). Birth of germline chimeras by transfer of chicken embryonic germ (EG) cells into recipient embryos. Mol. Reprod. Dev. 65, 389-395. https://doi.org/10.1002/mrd.10304
  46. Park, T.S., Jeong, D.K., Kim, J.N., Song, G.H., Hong, Y.H., Lim, J.M., and Han, J.Y. (2003b). Improved germline transmission in chicken chimeras produced by transplantation of gonadal primordial germ cells into recipient embryos. Biol. Reprod. 68, 1657-1662. https://doi.org/10.1095/biolreprod.102.006825
  47. Park, K.J., Kang, S.J., Kim, T.M., Lee, Y.M., Lee, H.C., Song, G., and Han, J.Y. (2010). Gamma-irradiation depletes endogenous germ cells and increases donor cell distribution in chimeric chickens. In Vitro Cell Dev. Biol. Anim. 46, 828-833. https://doi.org/10.1007/s11626-010-9361-8
  48. Park, T.S., Lee, H.J., Kim, K.H., Kim, J.S., and Han, J.Y. (2014). Targeted gene knockout in chickens mediated by TALENs. Proc. Natl. Acad. Sci. USA 111, 12716-12721. https://doi.org/10.1073/pnas.1410555111
  49. Park, T.S., Lee, H.G., Moon, J.K., Lee, H.J., Yoon, J.W., Yun, B.N., Kang, S.C., Kim, J., Kim, H., Han, J.Y., et al. (2015). Deposition of bioactive human epidermal growth factor in the egg white of transgenic hens using an oviduct-specific minisynthetic promoter. FASEB J. 29, 2386-2396. https://doi.org/10.1096/fj.14-264739
  50. Petitte, J.N., Clark, M.E., Liu, G., Verrinder Gibbins, A.M., and Etches, R.J. (1990). Production of somatic and germline chimeras in the chicken by transfer of early blastodermal cells. Development 108, 185-189.
  51. Petitte, J.N., Liu, G., and Yang, Z. (2004). Avian pluripotent stem cells. Mech. Dev. 121, 1159-1168. https://doi.org/10.1016/j.mod.2004.05.003
  52. Rengaraj, D., Lee, B.R., Lee, S.I., Seo, H.W., and Han, J.Y. (2011). Expression patterns and miRNA regulation of DNA methyltransferases in chicken primordial germ cells. PLoS One 6, e19524. https://doi.org/10.1371/journal.pone.0019524
  53. Rengaraj, D., Lee, S.I., Park, T.S., Lee, H.J., Kim, Y.M., Sohn, Y.A., Jung, M., Noh, S.J., Jung, H., and Han, J.Y. (2014). Small noncoding RNA profiling and the role of piRNA pathway genes in the protection of chicken primordial germ cells. BMC Genomics 15, 757. https://doi.org/10.1186/1471-2164-15-757
  54. Resnick, J.L., Bixler, L.S., Cheng, L., and Donovan, P.J. (1992). Long-term proliferation of mouse primordial germ cells in culture. Nature 359, 550-551. https://doi.org/10.1038/359550a0
  55. Saitou, M., and Yamaji, M. (2012). Primordial germ cells in mice. Cold Spring Harb Perspect Biol 4, a008375.
  56. Salter, D.W., Smith, E.J., Hughes, S.H., Wright, S.E., Fadly, A.M., Witter, R.L., and Crittenden, L.B. (1986). Gene insertion into the chicken germ line by retroviruses. Poult. Sci. 65, 1445-1458. https://doi.org/10.3382/ps.0651445
  57. Schrauwen, E.J., and Fouchier, R.A. (2014). Host adaptation and transmission of influenza A viruses in mammals. Emerg. Microbes Infect. 3, e9. https://doi.org/10.1038/emi.2014.9
  58. Schusser, B., Collarini, E.J., Yi, H., Izquierdo, S.M., Fesler, J., Pedersen, D., Klasing, K.C., Kaspers, B., Harriman, W.D., van de Lavoir, M.C., et al. (2013). Immunoglobulin knockout chickens via efficient homologous recombination in primordial germ cells. Proc. Natl. Acad. Sci. USA 110, 20170-20175. https://doi.org/10.1073/pnas.1317106110
  59. Sijmons, P.C., Dekker, B.M., Schrammeijer, B., Verwoerd, T.C., van den Elzen, P.J., and Hoekema, A. (1990). Production of correctly processed human serum albumin in transgenic plants. Biotechnology 8, 217-221. https://doi.org/10.1038/nbt0390-217
  60. Singh, P., Schimenti, J.C., and Bolcun-Filas, E. (2015). A mouse geneticist's practical guide to CRISPR applications. Genetics 199, 1-15. https://doi.org/10.1534/genetics.114.169771
  61. Stevens, L. (1991). Egg white proteins. Comp. Biochem. Physiol. B 100, 1-9. https://doi.org/10.1016/0300-9629(91)90179-G
  62. Tajima, A., Naito, M., Yasuda, Y., and Kuwana, T. (1993). Production of germ line chimera by transfer of primordial germ cells in the domestic chicken (Gallus domesticus). Theriogenology 40, 509-519. https://doi.org/10.1016/0093-691X(93)90404-S
  63. Tan, W.S., Carlson, D.F., Walton, M.W., Fahrenkrug, S.C., and Hackett, P.B. (2012). Precision editing of large animal genomes. Adv. Genet. 80, 37-97. https://doi.org/10.1016/B978-0-12-404742-6.00002-8
  64. Tsunekawa, N., Naito, M., Sakai, Y., Nishida, T., and Noce, T. (2000). Isolation of chicken vasa homolog gene and tracing the origin of primordial germ cells. Development 127, 2741-2750.
  65. van de Lavoir, M.C., Diamond, J.H., Leighton, P.A., Mather-Love, C., Heyer, B.S., Bradshaw, R., Kerchner, A., Hooi, L.T., Gessaro, T.M., Swanberg, S.E., et al. (2006). Germline transmission of genetically modified primordial germ cells. Nature 441, 766-769. https://doi.org/10.1038/nature04831
  66. Vecchio, G. (2015). A fruit fly in the nanoworld: once again Drosophila contributes to environment and human health. Nanotoxicology 9, 135-137.
  67. Veeramah, K.R., and Hammer, M.F. (2014). The impact of wholegenome sequencing on the reconstruction of human population history. Nat. Rev. Genet. 15, 149-162.
  68. White, J.K., Gerdin, A.K., Karp, N.A., Ryder, E., Buljan, M., Bussell, J.N., Salisbury, J., Clare, S., Ingham, N.J., Podrini, C., et al. (2013a). Genome-wide generation and systematic phenotyping of knockout mice reveals new roles for many genes. Cell 154, 452-464. https://doi.org/10.1016/j.cell.2013.06.022
  69. White, R., Rose, K., and Zon, L. (2013b). Zebrafish cancer: the state of the art and the path forward. Nat. Rev. Cancer 13, 624-636. https://doi.org/10.1038/nrc3589
  70. Wilmut, I., Schnieke, A.E., McWhir, J., Kind, A.J., and Campbell, K.H. (1997). Viable offspring derived from fetal and adult mammalian cells. Nature 385, 810-813. https://doi.org/10.1038/385810a0

Cited by

  1. Avian embryos and related cell lines: A convenient platform for recombinant proteins and vaccine production vol.12, pp.5, 2017, https://doi.org/10.1002/biot.201600598
  2. RNA-Seq analysis on chicken taste sensory organs: An ideal system to study organogenesis vol.7, pp.1, 2017, https://doi.org/10.1038/s41598-017-09299-7
  3. Genome Modification Technologies and Their Applications in Avian Species vol.18, pp.11, 2017, https://doi.org/10.3390/ijms18112245
  4. Primordial germ cell-mediated transgenesis and genome editing in birds vol.9, pp.1, 2018, https://doi.org/10.1186/s40104-018-0234-4
  5. Efficient production of human interferon beta in the white of eggs from ovalbumin gene–targeted hens vol.8, pp.1, 2018, https://doi.org/10.1038/s41598-018-28438-2
  6. culture system vol.59, pp.2, 2018, https://doi.org/10.1080/00071668.2017.1413234
  7. Drug resistance in influenza A virus: the epidemiology and management vol.10, pp.None, 2015, https://doi.org/10.2147/idr.s105473
  8. Beyond the Chicken: Alternative Avian Models for Developmental Physiological Research vol.12, pp.None, 2015, https://doi.org/10.3389/fphys.2021.712633