TALEN-mediated gene disruption on y chromosome reveals critical role of EIF2S3Y in mouse spermatogenesis

Stem Cells and Development

Volumn 24, Issue 10, 2015, Pages 1164-1170

  Matsubara, Yohei ^a   Kato, Tomoko ^b   Kashimada, Kenichi ^a   Tanaka, Hiromitsu ^c   Zhi, Zhou ^d   Ichinose, Shizuko ^e   Mizutani, Shuki ^a   Morio, Tomohiro ^a   Chiba, Tomoki ^a   Ito, Yoshiaki ^a   Saga, Yumiko ^d   Takada, Shuji ^b   Asahara, Hiroshi ^a,b,f  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^b NATIONAL RESEARCH INSTITUTE FOR CHILD HEALTH AND DEVELOPMENT   (Japan)

^c NAGASAKI INTERNATIONAL UNIVERSITY   (Japan)

^d NATIONAL INSTITUTE OF GENETICS   (Japan)

^e TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^f SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION ACTIVATOR LIKE EFFECTOR NUCLEASE; ENDONUCLEASE; INITIATION FACTOR 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AZOOSPERMIA; CELL DIFFERENTIATION; FRAMESHIFT MUTATION; GENE DISRUPTION; GENE FUNCTION; GENE MUTATION; GENOTYPE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPERMATOGENESIS; SPERMATOGONIUM; STEM CELL; Y CHROMOSOME; ANIMAL; CYTOLOGY; GENE TARGETING; GENETICS; KNOCKOUT MOUSE; TESTIS;

MUS;

ANIMALS; ENDONUCLEASES; EUKARYOTIC INITIATION FACTOR-2; GENE TARGETING; MALE; MICE; MICE, KNOCKOUT; SPERMATOGENESIS; SPERMATOGONIA; TESTIS; Y CHROMOSOME;

EID: 84928886508     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2014.0466     Document Type: Article

References (34)

1. Lahn BT and DC Page. (1997). Functional coherence of the human Y chromosome. Science 278:675-680.
2. Skaletsky H, T Kuroda-Kawaguchi, PJ Minx, HS Cordum, L Hillier, LG Brown, S Repping, T Pyntikova, J Ali, et al. (2003). The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423:825-837.
3. Toure A, EJ Clemente, P Ellis, SK Mahadevaiah, OA Ojarikre, PA Ball, L Reynard, KL Loveland, PS Burgoyne and NA Affara. (2005). Identification of novel Y chromosome encoded transcripts by testis transcriptome analysis of mice with deletions of the Y chromosome long arm. Genome Biol 6:R102.
4. Burgoyne PS and MJ Mitchell. (2007). The roles of mouse Y chromosome genes in spermatogenesis. In: The Y Chromosome and Male Germ Cell Biology in Health and Diseases. Lau YF, Chan WY, eds. World Scientific, Singapore, pp 1-25.
5. Burgoyne PS, ER Levy and A McLaren. (1986). Sperma-togenic failure in male mice lacking H-Y antigen. Nature 320:170-172.
6. Sutcliffe MJ and PS Burgoyne. (1989). Analysis of the testes of H-Y negative XOSxrb mice suggests that the spermatogenesis gene (Spy) acts during the differentiation of the A spermatogonia. Development 107:373-380.
7. Mazeyrat S, N Saut, CA Sargent, S Grimmond, G Long-epied, IE Ehrmann, PS Ellis, A Greenfield, NA Affara and MJ Mitchell. (1998). The mouse Y chromosome interval necessary for spermatogonial proliferation is gene dense with syntenic homology to the human AZFa region. Hum Mol Genet 7:1713-1724.
8. Mazeyrat S, N Saut, V Grigoriev, SK Mahadevaiah, OA Ojarikre, A Rattigan, C Bishop, EM Eicher, MJ Mitchell and PS Burgoyne. (2001). A Y-encoded subunit of the translation initiation factor Eif2 is essential for mouse spermatogenesis. Nat Genet 29:49-53.
9. Sung YH, IJ Baek, DH Kim, J Jeon, J Lee, K Lee, D Jeong, JS Kim and HW Lee. (2013). Knockout mice created by TALEN-mediated gene targeting. Nat Biotechnol 31: 23-24.
10. Davies B, G Davies, C Preece, R Puliyadi, D Szumska and S Bhattacharya. (2013). Site specific mutation of the Zic2 locus by microinjection of TALEN mRNA in mouse CD1, C3H and C57BL/6J oocytes. PLoS One 8:e60216.
11. Qiu Z, M Liu, Z Chen, Y Shao, H Pan, G Wei, C Yu, L Zhang, X Li, et al. (2013). High-efficiency and heritable gene targeting in mouse by transcription activator-like effector nucleases. Nucleic Acids Res 41:e120.
12. Takada S, T Sato, Y Ito, S Yamashita, T Kato, M Kawa-sumi, M Kanai-Azuma, A Igarashi, T Kato, M Tamano and H Asahara. (2013). Targeted gene deletion of miRNAs in mice by TALEN system. PLoS One 8:e76004.
13. Christian M, T Cermak, EL Doyle, C Schmidt, F Zhang, A Hummel, AJ Bogdanove and DF Voytas. (2010). Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 186:757-761.
14. Wang H, YC Hu, S Markoulaki, GG Welstead, AW Cheng, CS Shivalila, T Pyntikova, DB Dadon, DF Voytas, et al. (2013). TALEN-mediated editing of the mouse Y chromosome. Nat Biotechnol 31:530-532.
15. Kato T, K Miyata, M Sonobe, S Yamashita, M Tamano, K Miura, Y Kanai, S Miyamoto, T Sakuma, et al. (2013). Production of Sry knockout mouse using TALEN via oo-cyte injection. Sci Rep 3:3136.
16. Hasegawa K and Y Saga. (2012). Retinoic acid signaling in Sertoli cells regulates organization of the blood-testis barrier through cyclical changes in gene expression. Development 139:4347-4355.
17. Chiarini-Garcia H and LD Russell. (2002). Characterization of mouse spermatogonia by transmission electron microscopy. Reproduction 123:567-577.
18. Buageaw A, M Sukhwani, A Ben-Yehudah, J Ehmcke, VY Rawe, C Pholpramool, KE Orwig and S Schlatt. (2005). GDNF family receptor alpha1 phenotype of spermatogonial stem cells in immature mouse testes. Biol Reprod 73:1011-1016.
19. Suzuki H, A Sada, S Yoshida and Y Saga. (2009). The heterogeneity of spermatogonia is revealed by their topology and expression of marker proteins including the germ cell-specific proteins Nanos2 and Nanos3. Dev Biol 336: 222-231.
20. Tanaka H, LA Pereira, M Nozaki, J Tsuchida, K Sawada, H Mori and Y Nishimune. (1997). A germ cell-specific nuclear antigen recognized by a monoclonal antibody raised against mouse testicular germ cells. Int J Androl 20:361-366.
21. Tokuhiro K, M Hirose, Y Miyagawa, A Tsujimura, S Irie, A Isotani, M Okabe, Y Toyama, C Ito, et al. (2008). Meichroacidin containing the membrane occupation and recognition nexus motif is essential for spermatozoa morphogenesis. J Biol Chem 283:19039-19048.
22. Pereira LA, H Tanaka, Y Nagata, K Sawada, H Mori, LM Chimelli and Y Nishimune. (1998). Characterization and expression of a stage specific antigen by monoclonal antibody TRA 54 in testicular germ cells. Int J Androl 21: 34-40.
23. de Rooij DG. (1998). Stem cells in the testis. Int J Exp Pathol 79:67-80.
24. de Rooij DG and LD Russell. (2000). All you wanted to know about spermatogonia but were afraid to ask. J Androl 21:776-798.
25. Raverdeau M, A Gely-Pernot, B Feret, C Dennefeld, G Benoit, I Davidson, P Chambon, M Mark and NB Ghyse-linck. (2012). Retinoic acid induces Sertoli cell paracrine signals for spermatogonia differentiation but cell autonomously drives spermatocyte meiosis. Proc Natl Acad Sci USA 109:16582-16587.
26. Huang Z, B Rivas and AI Agoulnik. (2013). NOTCH1 gain of function in germ cells causes failure of spermatogenesis in male mice. PLoS One 8:e71213.
27. Sugimoto R, Y Nabeshima and S Yoshida. (2012). Retinoic acid metabolism links the periodical differentiation of germ cells with the cycle of Sertoli cells in mouse seminiferous epithelium. Mech Dev 128:610-624.
28. Chakraborty P, FW Buaas, M Sharma, E Snyder, DG de Rooij and RE Braun. (2014). LIN28A marks the sper-matogonial progenitor population and regulates its cyclic expansion. Stem Cells 32:860-873.
29. Sutcliffe MJ and PS Burgoyne. (1989). Analysis of the testes of H-Y negative XOSxrb mice suggests that the spermatogenesis gene (Spy) acts during the differentiation of the A spermatogonia. Development 107:373-380.
30. Gebauer F and MW Hentze. (2004). Molecular mechanisms of translational control. Nat Rev Mol Cell Biol 5: 827-835.
31. Gaspar NJ, TG Kinzy, BJ Scherer, M Humbelin, JW Her-shey and WC Merrick. (1994). Translation initiation factor eIF-2. Cloning and expression of the human cDNA encoding the gamma-subunit. J Biol Chem 269:3415-3422.
32. Naranda T, I Sirangelo, BJ Fabbri and JW Hershey. (1995). Mutations in the NKXD consensus element indicate that GTP binds to the gamma-subunit of translation initiation factor eIF2. FEBS Lett 372:249-252.
33. Erickson FL and EM Hannig. (1996). Ligand interactions with eukaryotic translation initiation factor 2: role of the gamma-subunit. EMBO J 15:6311-6320.
34. Ehrmann IE, PS Ellis, S Mazeyrat, S Duthie, N Brockdorff, MG Mattei, MA Gavin, NA Affara, GM Brown, et al. (1998). Characterization of genes encoding translation initiation factor eIF-2gamma in mouse and human: sex chromosome localization, escape from X-inactivation and evolution. Hum Mol Genet 7:1725-1737.