DNA methylation-mediated transcription factors regulate piwil1 expression during chicken spermatogenesis

Journal of Reproduction and Development

Volumn 62, Issue 4, 2016, Pages 367-372

  Qiu, Lingling ^a   Xu, Lu ^a   Chang, Guobin ^a   Guo, Qixin ^a   Liu, Xiangping ^b   Bi, Yulin ^a   Zhang, Yu ^a   Wang, Hongzhi ^b   Wang, Kehua ^b   Lu, Wei ^a   Ren, Lichen ^a   Zhu, Pengfei ^a   Wu, Yun ^a   Zhang, Yang ^a   Xu, Qi ^a   Chen, Guo Hong ^a  

^a YANGZHOU UNIVERSITY   (China)

^b INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

Chicken; DNA methylation; Piwil1; Spermatogenesis

Indexed keywords

ARGONAUTE PROTEIN; TRANSCRIPTION FACTOR SOX;

ANIMAL; BINDING SITE; CELL LINE; CHICKEN; CPG ISLAND; DNA METHYLATION; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; PROMOTER REGION; SPERMATOGENESIS; SPERMATOZOON;

ANIMALS; ARGONAUTE PROTEINS; BINDING SITES; CELL LINE; CHICKENS; CPG ISLANDS; DNA METHYLATION; GENE EXPRESSION REGULATION; MALE; PROMOTER REGIONS, GENETIC; SOXB1 TRANSCRIPTION FACTORS; SPERMATOGENESIS; SPERMATOZOA;

EID: 84983458696     PISSN: 09168818     EISSN: 13484400     Source Type: Journal    
DOI: 10.1262/jrd.2016-003     Document Type: Article

References (28)

1. Loveland KL, Hogarth C, Mendis S, Efthymiadis A, Ly J, Itman C, Meachem S, Brown CW, Jans DA. Drivers of germ cell maturation. Ann N Y Acad Sci 2005; 1061: 173–182.
2. Tanaka H, Baba T. Gene expression in spermiogenesis. Cell Mol Life Sci 2005; 62: 344–354.
3. Cox DN, Chao A, Lin H. piwi encodes a nucleoplasmic factor whose activity modulates the number and division rate of germline stem cells. Development 2000; 127: 503–514.
4. Kuramochi-Miyagawa S, Kimura T, Ijiri TW, Isobe T, Asada N, Fujita Y, Ikawa M, Iwai N, Okabe M, Deng W, Lin H, Matsuda Y, Nakano T. Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 2004; 131: 839–849.
5. Hou Y, Yuan J, Zhou X, Fu X, Cheng H, Zhou R. DNA demethylation and USF regulate the meiosis-specific expression of the mouse Miwi. PLoS Genet 2012; 8: e1002716.
6. Deng W, Lin H. miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell 2002; 2: 819–830.
7. Houwing S, Berezikov E, Ketting RF. Zili is required for germ cell differentiation and meiosis in zebrafish. EMBO J 2008; 27: 2702–2711.
8. Kuramochi-Miyagawa S, Watanabe T, Gotoh K, Totoki Y, Toyoda A, Ikawa M, Asada N, Kojima K, Yamaguchi Y, Ijiri TW, Hata K, Li E, Matsuda Y, Kimura T, Okabe M, Sakaki Y, Sasaki H, Nakano T. DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev 2008; 22: 908–917.
9. Gunawardane LS, Saito K, Nishida KM, Miyoshi K, Kawamura Y, Nagami T, Siomi H, Siomi MC. A slicer-mediated mechanism for repeat-associated siRNA 5′ end formation in Drosophila. Science 2007; 315: 1587–1590.
10. Kim TH, Yun TW, Rengaraj D, Lee SI, Lim SM, Seo HW, Park TS, Han JY. Conserved functional characteristics of the PIWI family members in chicken germ cell lineage. Theriogenology 2012; 78: 1948–1959.
11. Hamburger V, Hamilton HL. A series of normal stages in the development of the chick embryo. J Morphol 1951; 88: 49–92.
12. Yu F, Ding LJ, Sun GB, Sun PX, He XH, Ni LG, Li BC. Transgenic sperm produced by electrotransfection and allogeneic transplantation of chicken fetal spermatogonial stem cells. Mol Reprod Dev 2010; 77: 340–347.
13. Li B, Wang XY, Tian Z, Xiao XJ, Xu Q, Wei CX, Y F, Sun HC, Chen GH. Directional differentiation of chicken spermatogonial stem cells in vitro. Cytotherapy 2010; 12: 326–331.
14. Mays-Hoopes LL, Bolen J, Riggs AD, Singer-Sam J. Preparation of spermatogonia, spermatocytes, and round spermatids for analysis of gene expression using fluorescence-activated cell sorting. Biol Reprod 1995; 53: 1003–1011.
15. Mozdziak PE, Angerman-Stewart J, Rushton B, Pardue SL, Petitte JN. Isolation of chicken primordial germ cells using fluorescence-activated cell sorting. Poult Sci 2005; 84: 594–600.
16. Riesco MF, Martínez-Pastor F, Chereguini O, Robles V. Evaluation of zebrafish (Danio rerio) PGCs viability and DNA damage using different cryopreservation protocols. Theriogenology 2012; 77: 122–130.e2.
17. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 1983; 65: 55–63.
18. Connolly MA, Clausen PA, Lazar JG. Purification of RNA from animal cells using trizol. CSH Protoc 2006; 2006: 10–15.
19. Gu Y, Li Q, Pan Z, Li M, Luo H, Xie Z. Molecular cloning, gene expression and methylation status analysis of PIWIL1 in cattle-yaks and the parental generation. Anim Reprod Sci 2013; 140: 131–137.
20. Sohn YA, Lee SI, Choi HJ, Kim HJ, Kim KH, Park TS, Han JY. The CCAAT element in the CIWI promoter regulates transcriptional initiation in chicken primordial germ cells. Mol Reprod Dev 2014; 81: 871–882.
21. Chang G, Chen R, Xu L, Ma T, Wang H, Chen J, Zhang Y, Li Z, Wan F, Guo X, Xu Q, Zhao W, Chen G. DNA methylation and NF-Y regulate Piwil1 expression during chicken spermatogenesis. Anim Reprod Sci 2015; 162: 95–103.
22. Li XZ, Roy CK, Dong X, Bolcun-Filas E, Wang J, Han BW, Xu J, Moore MJ, Schimenti JC, Weng Z, Zamore PD. An ancient transcription factor initiates the burst of piRNA production during early meiosis in mouse testes. Mol Cell 2013; 50: 67–81.
23. Pereira L, Yi F, Merrill BJ. Repression of Nanog gene transcription by Tcf3 limits embryonic stem cell self-renewal. Mol Cell Biol 2006; 26: 7479–7491.
24. Cole MF, Johnstone SE, Newman JJ, Kagey MH, Young RA. Tcf3 is an integral component of the core regulatory circuitry of embryonic stem cells. Genes Dev 2008; 22: 746–755.
25. Yi F, Pereira L, Hoffman JA, Shy BR, Yuen CM, Liu DR, Merrill BJ. Opposing effects of Tcf3 and Tcf1 control Wnt stimulation of embryonic stem cell self-renewal. Nat Cell Biol 2011; 13: 762–770.
26. Virbasius CA, Virbasius JV, Scarpulla RC. NRF-1, an activator involved in nuclear-mitochondrial interactions, utilizes a new DNA-binding domain conserved in a family of developmental regulators. Genes Dev 1993; 7(12A): 2431–2445.
27. Blesa JR, Prieto-Ruiz JA, Abraham BA, Harrison BL, Hegde AA, Hernández-Yago J. NRF-1 is the major transcription factor regulating the expression of the human TOMM34 gene. Biochem Cell Biol 2008; 86: 46–56.
28. Efiok BJ, Chiorini JA, Safer B. A key transcription factor for eukaryotic initiation factor-2 alpha is strongly homologous to developmental transcription factors and may link metabolic genes to cellular growth and development. J Biol Chem 1994; 269: 18921–18930.