Development and Reproduction (한국발생생물학회지:발생과생식)

The Korean Society of Developmental Biology (한국발생생물학회)
권호 표지
DOI QR코드

DOI QR Code

A Maternal Transcription Factor, Junction Mediating and Regulatory Protein is Required for Preimplantation Development in the Mouse

  • Lin, Zi-Li (College of Animal Sciences, Jilin University) ;
  • Li, Ying-Hua (Department of Animal Sciences, Yanbian University) ;
  • Jin, Yong- Xun (College of Animal Sciences, Jilin University) ;
  • Kim, Nam-Hyung (College of Animal Sciences, Jilin University)
  • Received : 2019.07.02
  • Accepted : 2019.08.29
  • Published : 2019.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

Junction-mediating and regulatory protein (JMY) is a regulator of both transcription and actin filament assembly. The actin-regulatory activity of JMY is based on a cluster of three actin-binding Wiskott-Aldrich syndrome protein homology 2 (WH2) domains that nucleate actin filaments directly and promote nucleation of the Arp2/3 complex. In addition to these activities, we examined the activity of JMY generation in early embryo of mice carrying mutations in the JMY gene by CRISPR/Cas9 mediated genome engineering. We demonstrated that JMY protein shuttled expression between the cytoplasm and the nucleus. Knockout of exon 2, CA (central domain and Arp2/3-binding acidic domain) and NLS-2 (nuclear localization signal domain) on the JMY gene by CRISPR/Cas9 system was effective and markedly impeded embryonic development. Additionally, it impaired transcription and zygotic genome activation (ZGA)-related genes. These results suggest that JMY acts as a transcription factor, which is essential for the early embryonic development in mice.

Keywords

References

  1. Bultman SJ, Gebuhr TC, Pan H, Svoboda P, Schultz RM, Magnuson (2006) Maternal BRG1 regulates zygotic genome activation in the mouse. Genes Dev 20:1744-1754. https://doi.org/10.1101/gad.1435106
  2. Ceglia I, Lee KW, Cahill ME, Graves SM, Dietz D, Surmeier DJ, Nestler EJ, Nairn AC, Greengard P, Kim Y. (2017) WAVE1 in neurons expressing the D1 dopamine receptor regulates cellular and behavioral actions of cocaine. Proc Natl Acad Sci 114:1395-1400. https://doi.org/10.1073/pnas.1621185114
  3. Cho SW, Lee J, Carroll D, Kim JS, Lee J (2013) Heritable gene knockout in Caenorhabditis elegans by direct injection of Cas9-sgRNA ribonucleoproteins. Genetics 195:1177-1180. https://doi.org/10.1534/genetics.113.155853
  4. Coutts AS, Boulahbel H, Graham A, La Thangue NB (2007) Mdm2 targets the p53 transcription cofactor JMY for degradation. EMBO Rep 8:84-90. https://doi.org/10.1038/sj.embor.7400855
  5. Coutts AS, Pires IM, Weston L, Buffa FM, Milani M, Li JL, Harris AL, Hammond EM, La Thangu NB (2011) Hypoxia-driven cell motility reflects the interplay between JMY and HIF-$1{\alpha}$. Oncogene 30:4835-4842. https://doi.org/10.1038/onc.2011.188
  6. Coutts AS, Weston L, La Thangue NB (2009) A transcription co-factor integrates cell adhesion and motility with the p53 response. Proc Natl Acad Sci 106:19872-19877. https://doi.org/10.1073/pnas.0906785106
  7. Firat-Karalar EN, Hsiue PP, Welch MD (2011) The actin nucleation factor JMY is a negative regulator of neuritogenesis. Mol Biol Cell 22:4563-4574. https://doi.org/10.1091/mbc.e11-06-0585
  8. Fujii W, Kawasaki K, Sugiura K, Naito K (2013) Efficient generation of large-scale genome-modified mice using gRNA and CAS9 endonuclease. Nucleic Acids Res 41:e187. https://doi.org/10.1093/nar/gkt772
  9. Guo X, Zhang T, Hu Z, Zhang Y, Shi Z, Wang Q, Cui Y, Wang F, Zhao H, Chen Y (2014) Efficient RNA/Cas9-mediated genome editing in Xenopus tropicalis. Development 141:707-714. https://doi.org/10.1242/dev.099853
  10. Hai T, Teng F, Guo R, Li W, Zhou Q (2014) One-step generation of knockout pigs by zygote injection of CRISPR/Cas system. Cell Res 24:372-375. https://doi.org/10.1038/cr.2014.11
  11. Hoeng JC, Dawson SC, House SA, Sagolla MS, Pham JK, Mancuso JJ, Lowe J, Cande WZ (2007) High-resolution crystal structure and in vivo function of a Kinesin-2 homologue in Giardia intestinalis (2007) Highresolution crystal structure and in vivo function of a kinesin-2 homologue in Giardia intestinalis. Mol Biol Cell 19:3124-3137. https://doi.org/10.1091/mbc.E07-11-1156
  12. Ito H, Morishita R, Shinoda T, Iwamoto I, Sudo K, Okamoto K, Nagata K (2010) Dysbindin-1, WAVE2 and Abi-1 form a complex that regulates dendritic spine formation. Mol Psychiatry 15:976-986. https://doi.org/10.1038/mp.2010.69
  13. Jao LE, Wente SR, Chen W (2013) Efficient multiplex biallelic zebrafish genome editing using a CRISPR nuclease system. Proc Natl Acad Sci 110:13904-13909. https://doi.org/10.1073/pnas.1308335110
  14. Lin Z, Xu YN, Namgoong S, Kim NH (2014) JMY functions as actin nucleation-promoting factor and mediator for p53-mediated DNA damage in porcine oocytes. PLOS ONE 9:e109385. https://doi.org/10.1371/journal.pone.0109385
  15. Lin ZL, Cui XS, Namgoong S, Kim NH (2015) Junctionmediating and regulatory protein (JMY) is essential for early porcine embryonic development. J Reprod Dev 61:361-367. https://doi.org/10.1262/jrd.2015-021
  16. Niu Y, Shen B, Cui Y, Chen Y, Wang J, Wang L, Kang Y, Zhao X, Si W, Li W, Xiang AP, Zhou J, Guo X, Bi Y, Si C, Hu B, Dong G, Wang H, Zhou Z, Li T, Tan T, Pu X, Wang F, Ji S, Zhou Q, Huang X, Ji W, Sha J (2014) Generation of gene-modified cynomolgus monkey via Cas9/RNA-mediated gene targeting in one-cell embryos. Cell 156:836-843. https://doi.org/10.1016/j.cell.2014.01.027
  17. Pinyol R, Haeckel A, Ritter A, Qualmann B, Kessels MM (2007). Regulation of N-WASP and the Arp2/3 complex by Abp1 controls neuronal morphology. PLOS ONE 2:e400. https://doi.org/10.1371/journal.pone.0000400
  18. Schultz RM (1993) Regulation of zygotic gene activation in the mouse. Bioessays 15:531-538. https://doi.org/10.1002/bies.950150806
  19. Shikama N, Lee CW, France S, Delavaine L, Lyon J, Krstic-Demonacos M, La Thangue NB (1999) A novel cofactor for p300 that regulates the p53 response. Mol Cell 4:365-376. https://doi.org/10.1016/S1097-2765(00)80338-X
  20. Sun SC, Xu YN, Li YH, Lee SE, Jin YX, Cui XS, Kim NH (2011) WAVE2 regulates meiotic spindle stability, peripheral positioning and polar body emission in mouse oocytes. Cell Cycle 10:1853-1860. https://doi.org/10.4161/cc.10.11.15796
  21. Wang H, Hu YC, Markoulaki S, Welstead GG, Cheng AW, Shivalila CS, Pyntikova T, Dadon DB, Voytas DF, Bogdanove AJ, Page DC, Jaenisch R (2013) TALENmediated editing of the mouse Y chromosome. Nat Biotechnol 31:530-532. https://doi.org/10.1038/nbt.2595
  22. Yi K, Unruh JR, Deng M, Slaughter BD, Rubinstein B, Li R (2011) Dynamic maintenance of asymmetric meiotic spindle position through Arp2/3-complex-driven cytoplasmic streaming in mouse oocytes. Nat Cell Biol 13:1252-1258. https://doi.org/10.1038/ncb2320
  23. Zeng F, Schultz RM (2005) RNA transcript profiling during zygotic gene activation in the preimplantation mouse embryo. Dev Biol 283:40-57. https://doi.org/10.1016/j.ydbio.2005.03.038
  24. Zuchero JB, Coutts AS, Quinlan ME, Thangue NB, Mullins RD (2009) p53-cofactor JMY is a multifunctional actin nucleation factor. Nat Cell Biol 11:451-459. https://doi.org/10.1038/ncb1852
  25. Zuo E, Cai Y, Li K, Wei Y, Wang BA, Sun Y, Liu Z, Liu J, Hu X, Wei W, Huo X, Shi L, Tang C, Liang D, Wang Y, Nie YH, Zhang CC, Yao X, Wang X, Zhou C, Ying W, Wang Q, Chen RC, Shen Q, Xu GL, Li J, Sun Q, Xiong ZQ, Yang H (2017) One-step generation of complete gene knockout mice and monkeys by CRISPR/Cas9-mediated gene editing with multiple sgRNAs. Cell Res 27:933-945. https://doi.org/10.1038/cr.2017.81