Animal Bioscience

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
권호 표지
DOI QR코드

DOI QR Code

Comparison of primordial germ cell differences at different developmental time points in chickens

  • Wei Gong (Joint International Research Laboratory of Agriculture and Agri-Product Safety of Ministry of Education of China, Yangzhou University) ;
  • Yichen Zou (Joint International Research Laboratory of Agriculture and Agri-Product Safety of Ministry of Education of China, Yangzhou University) ;
  • Xin Liu (Joint International Research Laboratory of Agriculture and Agri-Product Safety of Ministry of Education of China, Yangzhou University) ;
  • Yingjie Niu (Joint International Research Laboratory of Agriculture and Agri-Product Safety of Ministry of Education of China, Yangzhou University) ;
  • Kai Jin (Joint International Research Laboratory of Agriculture and Agri-Product Safety of Ministry of Education of China, Yangzhou University) ;
  • Bichun Li (Joint International Research Laboratory of Agriculture and Agri-Product Safety of Ministry of Education of China, Yangzhou University) ;
  • Qisheng Zuo (Joint International Research Laboratory of Agriculture and Agri-Product Safety of Ministry of Education of China, Yangzhou University)
  • Received : 2024.04.29
  • Accepted : 2024.07.08
  • Published : 2024.11.01
Download PDF
⟨ Previous Next ⟩

Abstract

Objective: Recently, the application in the field of germplasm resource conservation has become an important application of primordial germ cells (PGCs). However, due to the lack of deep understanding of the biological characteristics of PGCs at different time points, there is no systematic scheme for the selection of PGCs at which time points in practical application, which affects the practical application effect of PGCs. This study aims to clarify the differences in PGCs during development. Methods: Here, migration experiment, EdU proliferation assay and cell apoptosis assay were conducted to compare the differences in the migration ability, the proliferation ability and the recovery efficiency among female and male PGCs at E3.5, E4.5, and E5.5, which were explained by the following transcriptome sequencing analysis. Results: We found that there were larger differences between female and male PGCs at different embryonic ages, while smaller differences between female and male PGCs at the same embryonic age. Further comparison showed that the cell migration ability of female and male PGCs decreased gradually during development, so female and male PGCs at E3.5 are more suitable for in vitro allotransplantation. At the same time, the proliferation ability of PGCs gradually decreased during development, and cell adhesion and extracellular matrix communication were weakened, indicating that female and male PGCs of E3.5 are more suitable for in vitro long-term culture cell line establishment. Interestingly, female and male PGCs at E5.5 showed strong DNA damage repair ability, thus more suitable for in vitro long-term cryopreservation. Conclusion: This study provides a theoretical basis for systematically selecting PGCs at suitable developmental time points as cell materials for efficient utilization by analyzing the characteristics of female and male PGCs at different developmental time points based on transcriptome.

Keywords

Acknowledgement

We thank the Poultry Institute of the Chinese Academy of Agricultural Sciences Experimental Poultry Farm for providing experimental materials.

References

  1. Nakamura Y, Usui F, Miyahara D, et al. Efficient system for preservation and regeneration of genetic resources in chicken: concurrent storage of primordial germ cells and live animals from early embryos of a rare indigenous fowl (Gifujidori). Reprod Fertil Dev 2010;22:1237-46. https://doi.org/10.1071/RD10056 
  2. Saito T, Goto-Kazeto R, Arai K, Yamaha E. Xenogenesis in teleost fish through generation of germ-line chimeras by single primordial germ cell transplantation. Biol Reprod 2008;78:159-66. https://doi.org/10.1095/biolreprod.107.060038
  3. Chuma S, Kanatsu-Shinohara M, Inoue K, et al. Spermatogenesis from epiblast and primordial germ cells following transplantation into postnatal mouse testis. Development 2005;132:117-22. https://doi.org/10.1242/dev.01555 
  4. Asaoka M, Sakamaki Y, Fukumoto T, et al. Offspring production from cryopreserved primordial germ cells in Drosophila. Commun Biol 2021;4:1159. https://doi.org/10.1038/s42003-021-02692-z 
  5. Naito M, Matsubara Y, Harumi T, et al. Differentiation of donor primordial germ cells into functional gametes in the gonads of mixed-sex germline chimaeric chickens produced by transfer of primordial germ cells isolated from embryonic blood. Reproduction 1999;117:291-8. https://doi.org/10.1530/jrf.0.1170291 
  6. Nakamura Y, Yamamoto Y, Usui F, et al. Migration and proliferation of primordial germ cells in the early chicken embryo. Poult Sci 2007;86:2182-93. https://doi.org/10.1093/ps/86.10.2182 
  7. Liu C, Chang IK, Khazanehdari KA, et al. Uniparental chicken offsprings derived from oogenesis of chicken primordial germ cells (ZZ. Biol Reprod 2017;96:686-93. https://doi.org/10.1095/biolreprod.116.144253 
  8. Woodcock ME, Gheyas AA, Mason AS, et al. Reviving rare chicken breeds using genetically engineered sterility in surrogate host birds. Proc Natl Acad Sci USA 2019;116:20930-7. https://doi.org/10.1073/pnas.1906316116 
  9. Zhao ZH, Meng TG, Li A, Schatten H, Wang Z-B, Sun Q-Y. RNA-Seq transcriptome reveals different molecular responses during human and mouse oocyte maturation and fertilization. BMC Genomics 2020;21:475. https://doi.org/10.1186/s12864-020-06885-4 
  10. Ge Q, Feng F, Liu L, et al. RNA-Seq analysis of the pathogenesis of STZ-induced male diabetic mouse liver. J Diabetes Complications 2020;34:107444. https://doi.org/10.1016/j.jdiacomp.2019.107444 
  11. Ding Y, Zhao J, Xu X, et al. Inhibition of autophagy maintains ESC pluripotency and inhibits primordial germ cell formation in chickens. Stem Cells Int 2023;2023:4956871. https://doi.org/10.1155/2023/4956871 
  12. Gong W, Zhao J, Yao Z, et al. The establishment and optimization of a chicken primordial germ cell induction model using small-molecule compounds. Animals 2024;14:302. https://doi.org/10.3390/ani14020302 
  13. Zuo Q, Jin K, Wang M, Zhang Y, Chen G, Li B. BMP4 activates the Wnt-Lin28A-Blimp1 -Wnt pathway to promote primordial germ cells formation via altering H3K4me2. J Cell Sci 2020;134:jcs249375. https://doi.org/10.1242/jcs.249375 
  14. Chen C, Zhou S, Lian Z, et al. Tle4z1 facilitate the male Sexual differentiation of chicken embryos. Front Physiol 2022;13:856980. https://doi.org/10.3389/fphys.2022.856980 
  15. Ge C, Zhang C, Ye J, Tang X, Wu Y. Ginsenosides promote proliferation of chicken primordial germ cells via PKC-involved activation of NF-kappaB. Cell Biol Int 2007;31:1251-6. https://doi.org/10.1016/j.cellbi.2007.05.001 
  16. Zuo Q, Zhou J, Wang M, Zhang Y, Chen G, Li B. Study on the function and mechanism of Lin28B in the formation of chicken primordial germ cells. Animals 2020;11:43. https://doi.org/10.3390/ani11010043 
  17. Meng L, Wang S, Jiang H, et al. Oct4 dependent chromatin activation is required for chicken primordial germ cell migration. Stem Cell Rev Rep 2022;18:2535-46. https://doi.org/10.1007/s12015-022-10371-7 
  18. Rao X, Huang X, Zhou Z, Lin X. An improvement of the 2ˆ(-delta delta CT) method for quantitative real-time polymerase chain reaction data analysis. Biostat Bioinforma Biomath 2013;3:71-85. 
  19. Chen S, Zhou Y, Chen Y, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 2018;34:i884-90. https://doi.org/10.1093/bioinformatics/bty560 
  20. Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nat Methods 2015;12:357-60. https://doi.org/10.1038/nmeth.3317 
  21. The Gene Ontology Consortium. The gene ontology resource: 20 years and still going strong. Nucleic Acids Res 2019;47:D330-8. https://doi.org/10.1093/nar/gky1055 
  22. Kanehisa M, Araki M, Goto S, et al. KEGG for linking genomes to life and the environment. Nucleic Acids Res 2008;36(Suppl 1):D480-4. https://doi.org/10.1093/nar/gkm882 
  23. Niu YJ, Ren W, Liu G, et al. Clonally derived chicken primordial germ cell lines maintain biological characteristics and proliferative potential in long-term culture. Theriogenology 2024;215:67-77. https://doi.org/10.1016/j.theriogenology.2023.11.023 
  24. Saraswathibhatla A, Indana D, Chaudhuri O. Cell-extracellular matrix mechanotransduction in 3D. Nat Rev Mol Cell Biol 2023;24:495-516. https://doi.org/10.1038/s41580-023-00583-1 
  25. Mishra YG, Manavathi B. Focal adhesion dynamics in cellular function and disease. Cell Signal 2021;85:110046. https://doi.org/10.1016/j.cellsig.2021.110046 
  26. Arseni L, Lombardi A, Orioli D. From structure to phenotype: impact of collagen alterations on human health. Int J Mol Sci 2018;19:1407. https://doi.org/10.3390/ijms19051407 
  27. Paavolainen O, Peuhu E. Integrin-mediated adhesion and mechanosensing in the mammary gland. Semin Cell Dev Biol 2021;114:113-25. https://doi.org/10.1016/j.semcdb.2020.10.010 
  28. Han JY, Park TS, Hong YH, et al. Production of germline chimeras by transfer of chicken gonadal primordial germ cells maintained in vitro for an extended period. Theriogenology 2002;58:1531-9. https://doi.org/10.1016/S0093-691X(02)01061-0 
  29. Park TS, Jeong DK, Kim JN, et al. Improved germline transmission in chicken chimeras produced by transplantation of gonadal primordial germ cells into recipient embryos. Biol Reprod 2003;68:1657-62. https://doi.org/10.1095/biolreprod.102.006825 
  30. Xie L, Lu Z, Chen D, et al. Derivation of chicken primordial germ cells using an indirect co-culture system. Theriogenology 2019;123:83-9. https://doi.org/10.1016/j.theriogenology.2018.09.017 
  31. Song Y, Duraisamy S, Ali J, et al. Characteristics of long-term cultures of avian primordial germ cells and gonocytes. Biol Reprod 2014;90:15. https://doi.org/10.1095/biolreprod.113.113381 
  32. Naito M, Harumi T, Kuwana T. Long-term culture of chicken primordial germ cells isolated from embryonic blood and production of germline chimaeric chickens. Anim Reprod Sci 2015;153:50-61. https://doi.org/10.1016/j.anireprosci.2014.12.003 
  33. Tonus C, Cloquette K, Ectors F, et al. Long term-cultured and cryopreserved primordial germ cells from various chicken breeds retain high proliferative potential and gonadal colonisation competency. Reprod Fertil Dev 2016;28:628-39. https:// doi.org/10.1071/RD14194 
  34. Altgilbers S, Klein S, Dierks C, Weigend S, Kues WA. Cultivation and characterization of primordial germ cells from blue layer hybrids (Araucana crossbreeds) and generation of germline chimeric chickens. Sci Rep 2021;11:12923. https://doi.org/10.1038/s41598-021-91490-y 
  35. Xu X, Cowley S, Flaim CJ, James W, Seymour L, Cui Z. The roles of apoptotic pathways in the low recovery rate after cryopreservation of dissociated human embryonic stem cells. Biotechnol Prog 2010;26:827-37. https://doi.org/10.1002/btpr.368 
  36. Kim JH, Choi JI, Che YH, et al. Enhancing viability of human embryonic stem cells during cryopreservation via RGDREP-mediated activation of FAK/AKT/FoxO3a signaling pathway. Tissue Eng Regen Med 2023;20:1133-43. https://doi.org/10.1007/s13770-023-00568-3 
  37. Vanhulle VP, Neyrinck AM, Pycke JM, Horsmans Y, Delzenne NM. Role of apoptotic signaling pathway in metabolic disturbances occurring in liver tissue after cryopreservation: study on rat precision-cut liver slices. Life Sci 2006;78:1570-7. https://doi.org/10.1016/j.lfs.2005.07.036 
  38. Jung SE, Oh HJ, Ahn JS, Kim YH, Kim BJ, Ryu BY. Antioxidant or apoptosis inhibitor supplementation in culture media improves post-thaw recovery of murine spermatogonial stem cells. Antioxidants 2021;10:754. https://doi.org/10.3390/antiox10050754 
  39. Shu WH, Yang SH, Wei M, et al. Effects of sericin on oxidative stress and PI3K/AKT/mTOR signal pathway in cryopreserved mice ovarian tissue. Cryobiology 2023;111:16-25. https://doi.org/10.1016/j.cryobiol.2023.03.003