The developmental origin of primordial germ cells and the transmission of the donor-derived gametes in mixed-sex germline chimeras to the offspring in the chicken

Kono, Hiroshi; Tagami, Takahiro; Matsubara, Yuko; Harumi, Takashi; Hanada, Hirofumi; Maruyama, K.; Sakurai, Michiharu; Kuwana, Takashi; Naito, Mitsuru

doi:10.1002/(sici)1098-2795(199712)48:4<501::aid-mrd11>3.0.co;2-w

Cited by 101 publications

(60 citation statements)

References 34 publications

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“…In avian species, PGCs, the predecessor of spermatozoa and ova, originate from the central zone of the area pellucida (Ginsburg and Eyal-Giladi, 1987;Kagami et al, 1997). At the primitive streak stage, PGCs are located at the extra embryonic region, called the germinal crescent (England and Matsumura, 1993).…”

Section: Conservation Of Avian Genetic Resources Through Germline Chimentioning

confidence: 99%

Conservation of Avian Genetic Resources

Tajima

2013

J. Poult. Sci.

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Conservation of avian genetic resources is important, as 13.0% (1,313/10,064) of known avian species are currently categorized as endangered by the International Union for Conservation of Nature and Natural Resources (IUCN, 2012). Development of an integrated system for conservation of avian genetics is necessary; however, germplasm conservation systems developed for mammals cannot be applied directly to avians, primarily due to the unique anatomical and physiological characteristics of the avian egg. Thus an alternative strategy for conservation of oviparous species of animals must be developed. Recent technological developments for producing germline chimeras by the transfer of primordial germ cells into recipient embryos has enabled the conservation and retrieval of chicken genetic resources in their complete form. Furthermore, the possibility of propagating endangered wild birds through interspecies germline chimeras has been proposed.In the present review, the current status of avian genetic resource conservation is presented with a focus on the following 4 topics: 1) semen cryopreservation, 2) germline chimeras, 3) somatic nuclear transfer, and 4) other related technologies.

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Section: Conservation Of Avian Genetic Resources Through Germline Chimentioning

confidence: 99%

Conservation of Avian Genetic Resources

Tajima

2013

J. Poult. Sci.

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“…In the chicken, segregation of PGCs from somatic cells occurs during the early stages of blastoderm formation (1)(2)(3). These cells accumulate in the germinal crescent region anterior to the forming head at day 1 of incubation [stage 4 Hamburger and Hamilton (HH)] and subsequently migrate via the circulatory system to the forming gonads on day 3 of incubation (stage 15 HH) (4).…”

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confidence: 99%

Efficient genetic modification and germ-line transmission of primordial germ cells using piggyBac and Tol2 transposons

Macdonald

Taylor

Sherman

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

151

125

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The derivation of germ-line competent avian primordial germ cells establishes a cell-based model system for the investigation of germ cell differentiation and the production of genetically modified animals. Current methods to modify primordial germ cells using DNA or retroviral vectors are inefficient and prone to epigenetic silencing. Here, we validate the use of transposable elements for the genetic manipulation of primordial germ cells. We demonstrate that chicken primordial germ cells can be modified in vitro using transposable elements. Both piggyBac and Tol2 transposons efficiently transpose primordial germ cells. Tol2 transposon integration sites were spread throughout both the macro-and microchromosomes of the chicken genome and were more prevalent in gene transcriptional units and intronic regions, consistent with transposon integrations observed in other species. We determined that the presence of insulator elements was not required for reporter gene expression from the integrated transposon. We further demonstrate that a gene-trap cassette carried in the Tol2 transposon can trap and mutate endogenous transcripts in primordial germ cells. Finally, we observed that modified primordial germ cells form functional gametes as demonstrated by the generation of transgenic offspring that correctly expressed a reporter gene carried in the transposon. Transposable elements are therefore efficient vectors for the genetic manipulation of primordial germ cells and the chicken genome.poultry | transgenesis | transposition P rimordial germ cells (PGCs) are specified in the early embryo and are the lineage-restricted stem cells for the germ cell population. In the chicken, segregation of PGCs from somatic cells occurs during the early stages of blastoderm formation (1-3). These cells accumulate in the germinal crescent region anterior to the forming head at day 1 of incubation [stage 4 Hamburger and Hamilton (HH)] and subsequently migrate via the circulatory system to the forming gonads on day 3 of incubation (stage 15 HH) (4). Chicken PGCs can be isolated from embryonic blood at this developmental stage and propagated indefinitely in culture (5). When returned to the circulatory system of an equivalent stage host embryo, the cultured PGCs migrated to and populated the forming embryonic gonad. Breeding from the resulting germline chimeras demonstrated that the cultured PGCs formed functional gametes by production of offspring derived from these cells. Germ-line transmission of cultured PGCs has now been demonstrated for three different chicken breeds (5-7).This in vitro system for the long-term propagation of chicken PGCs is the basis of a unique stem cell model for both the investigation of germ cell differentiation and the generation of genetically modified chickens. Thus far, chicken PGCs have proved highly resistant to genetic modification. Stable transfection of PGCs has been achieved by electroporation of plasmid DNA, at a frequency of ∼1 in 10 6 , but expression from integrated reporter constructs depended on t...

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“…Therefore, our culture condition could be effective only in male PGC-LCs culture. Kagami et al (1995Kagami et al ( , 1997 were demonstrated that genetically male and female PGCs derived from blastoderm could differentiate into functional gametes in the mixed-sex chimeric chicken gonads. Meanwhile, female cPGCs derived from St. 15 embryonic blood could not differentiate into functional spermatozoa in the male chimeric chicken testis; a frequency of W-bearing spermatozoa in the ejaculated semen was 0.2% .…”

Section: Discussionmentioning

confidence: 99%

Culture Conditions for Maintain Propagation, Long-term Survival and Germline Transmission of Chicken Primordial Germ Cell-Like Cells

et al. 2014

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Transplantation of primordial germ cells (PGCs), which are the progenitor cells of gametes, is a powerful tool for generation of transgenic chickens. However, the frequencies of transgene integration into the genome of purified PGCs still remain low. An in vitro culture system enabling chicken PGCs to propagate efficiently would be useful for efficient transgenesis of PGCs. In the present study, we optimized the culture conditions for chicken PGCs to enhance the proliferation and evaluated the germline transmission of cultured PGCs that proliferated for long periods of time. PGC-like cells (PGC-LCs), that have remarkably similar morphological characteristics to intact PGCs, could be derived by cultivation of blood containing PGCs obtained from 2.5-day-old chicken embryos according to the protocol of van de Lavoir et al. (2006). We determined which feeder cells and which growth factors were required to improve proliferation of PGC-LCs. Male PGC-LCs survival and proliferation were enhanced during culture in the basic medium containing either basic fibroblast growth factor (bFGF) alone or both bFGF and stem cell factor (SCF) on a feeder of buffalo rat liver (BRL) cells. Male PGC-LCs could be propagated in defined culture condition for extended periods. These cells expressed the germline-specific protein Vasa and undifferentiated cell marker stage-specific embryonic antigen-1 (SSEA-1) and pluripotency genes Nanog and PouV. Furthermore, Male PGC-LCs cultured for 225 d could migrate toward and colonize within recipient gonads and transmit to the next generation following transplantation. We succeeded in produce 3 offspring originating from long-term cultured PGC-LCs from a germline chimeric rooster (6%). The present study represents valuable steps toward defining a culture condition enabling PGCLCs to propagate efficiently for long periods in vitro with maintenance of their commitment to the germline.

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The developmental origin of primordial germ cells and the transmission of the donor-derived gametes in mixed-sex germline chimeras to the offspring in the chicken

Cited by 101 publications

References 34 publications

Conservation of Avian Genetic Resources

Conservation of Avian Genetic Resources

Efficient genetic modification and germ-line transmission of primordial germ cells using piggyBac and Tol2 transposons

Culture Conditions for Maintain Propagation, Long-term Survival and Germline Transmission of Chicken Primordial Germ Cell-Like Cells

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