Mouse Dazl and its novel splice variant functions in translational repression of target mRNAs in embryonic stem cells

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1829, Issue 5, 2013, Pages 425-435

  Xu, Xingbo ^a   Tan, Xiaoying ^a   Lin, Qiong ^b   Schmidt, Bernhard ^a   Engel, Wolfgang ^a   Pantakani, D V Krishna ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

Dazl; ESCs; RNA binding protein; Splice variant; Translation repression

Indexed keywords

CALRETICULIN; DELETED IN AZOOSPERMIA LIKE PROTEIN; KRUPPEL LIKE FACTOR 4; MESSENGER RNA; OCTAMER TRANSCRIPTION FACTOR 4; RNA BINDING PROTEIN; TRANSCRIPTION FACTOR SOX2; TUBULIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; AGAR GEL ELECTROPHORESIS; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; DOWN REGULATION; EMBRYONIC STEM CELL; EXON; FEMALE; GERM CELL; IMMUNOPRECIPITATION; LUNG; MALE; MOUSE; NONHUMAN; OVARY; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA TRANSLATION; SPERMATOGENESIS; TESTIS; WESTERN BLOTTING;

ALTERNATIVE SPLICING; ANIMALS; CYTOPLASM; DEAD-BOX RNA HELICASES; DOWN-REGULATION; EMBRYONIC STEM CELLS; FEMALE; GERM CELLS; MALE; MICE; MICE, MUTANT STRAINS; OCTAMER TRANSCRIPTION FACTOR-3; OVARY; PLURIPOTENT STEM CELLS; PROTEIN BIOSYNTHESIS; PROTEIN ISOFORMS; RNA, MESSENGER; RNA-BINDING PROTEINS; SOXB1 TRANSCRIPTION FACTORS;

VERTEBRATA;

EID: 84876057018     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2012.12.010     Document Type: Article

References (54)

1. Haag E.S. Rolling back to BOULE. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:6983-6985.
2. Peng J.X., Xie J.L., Zhou L., Hong Y.H., Gui J.F. Evolutionary conservation of Dazl genomic organization and its continuous and dynamic distribution throughout germline development in gynogenetic gibel carp. J. Exp. Zool. B Mol. Dev. Evol. 2009, 312:855-871.
3. Reijo R., Lee T.Y., Salo P., Alagappan R., Brown L.G., Rosenberg M., Rozen S., Jaffe T., Straus D., Hovatta O., et al. Diverse spermatogenic defects in humans caused by Y chromosome deletions encompassing a novel RNA-binding protein gene. Nat. Genet. 1995, 10:383-393.
4. Saxena R., Brown L.G., Hawkins T., Alagappan R.K., Skaletsky H., Reeve M.P., Reijo R., Rozen S., Dinulos M.B., Disteche C.M., Page D.C. The DAZ gene cluster on the human Y chromosome arose from an autosomal gene that was transposed, repeatedly amplified and pruned. Nat. Genet. 1996, 14:292-299.
5. Reynolds N., Cooke H.J. Role of the DAZ genes in male fertility. Reprod. Biomed. Online 2005, 10:72-80.
6. Eberhart C.G., Maines J.Z., Wasserman S.A. Meiotic cell cycle requirement for a fly homologue of human Deleted in Azoospermia. Nature 1996, 381:783-785.
7. Houston D.W., King M.L. A critical role for Xdazl, a germ plasm-localized RNA, in the differentiation of primordial germ cells in Xenopus. Development 2000, 127:447-456.
8. Karashima T., Sugimoto A., Yamamoto M. Caenorhabditis elegans homologue of the human azoospermia factor DAZ is required for oogenesis but not for spermatogenesis. Development 2000, 127:1069-1079.
9. Ruggiu M., Speed R., Taggart M., McKay S.J., Kilanowski F., Saunders P., Dorin J., Cooke H.J. The mouse Dazla gene encodes a cytoplasmic protein essential for gametogenesis. Nature 1997, 389:73-77.
10. Reijo R.A., Dorfman D.M., Slee R., Renshaw A.A., Loughlin K.R., Cooke H., Page D.C. DAZ family proteins exist throughout male germ cell development and transit from nucleus to cytoplasm at meiosis in humans and mice. Biol. Reprod. 2000, 63:1490-1496.
11. Lin Y., Page D.C. Dazl deficiency leads to embryonic arrest of germ cell development in XY C57BL/6 mice. Dev. Biol. 2005, 288:309-316.
12. Saunders P.T., Turner J.M., Ruggiu M., Taggart M., Burgoyne P.S., Elliott D., Cooke H.J. Absence of mDazl produces a final block on germ cell development at meiosis. Reproduction 2003, 126:589-597.
13. Tung J.Y., Rosen M.P., Nelson L.M., Turek P.J., Witte J.S., Cramer D.W., Cedars M.I., Pera R.A. Variants in Deleted in AZoospermia-Like (DAZL) are correlated with reproductive parameters in men and women. Hum. Genet. 2006, 118:730-740.
14. Tung J.Y., Rosen M.P., Nelson L.M., Turek P.J., Witte J.S., Cramer D.W., Cedars M.I., Reijo-Pera R.A. Novel missense mutations of the Deleted-in-AZoospermia-Like (DAZL) gene in infertile women and men. Reprod. Biol. Endocrinol. 2006, 4:40.
15. Schrans-Stassen B.H., Saunders P.T., Cooke H.J., de Rooij D.G. Nature of the spermatogenic arrest in Dazl-/- mice. Biol. Reprod. 2001, 65:771-776.
16. Haston K.M., Tung J.Y., Reijo Pera R.A. Dazl functions in maintenance of pluripotency and genetic and epigenetic programs of differentiation in mouse primordial germ cells in vivo and in vitro. PLoS One 2009, 4:e5654.
17. Cauffman G., Van de Velde H., Liebaers I., Van Steirteghem A. DAZL expression in human oocytes, preimplantation embryos and embryonic stem cells. Mol. Hum. Reprod. 2005, 11:405-411.
18. Moore F.L., Jaruzelska J., Dorfman D.M., Reijo-Pera R.A. Identification of a novel gene, DZIP (DAZ-interacting protein), that encodes a protein that interacts with DAZ (deleted in azoospermia) and is expressed in embryonic stem cells and germ cells. Genomics 2004, 83:834-843.
19. Xu X., Pantakani D.V., Luhrig S., Tan X., Khromov T., Nolte J., Dressel R., Zechner U., Engel W. Stage-specific germ-cell marker genes are expressed in all mouse pluripotent cell types and emerge early during induced pluripotency. PLoS One 2011, 6:e22413.
20. Yu Z., Ji P., Cao J., Zhu S., Li Y., Zheng L., Chen X., Feng L. Dazl promotes germ cell differentiation from embryonic stem cells. J. Mol. Cell. Biol. 2009, 1:93-103.
21. Chen J., Melton C., Suh N., Oh J.S., Horner K., Xie F., Sette C., Blelloch R., Conti M. Genome-wide analysis of translation reveals a critical role for deleted in azoospermia-like (Dazl) at the oocyte-to-zygote transition. Genes Dev. 2011, 25:755-766.
22. Collier B., Gorgoni B., Loveridge C., Cooke H.J., Gray N.K. The DAZL family proteins are PABP-binding proteins that regulate translation in germ cells. EMBO J. 2005, 24:2656-2666.
23. Jiao X., Trifillis P., Kiledjian M. Identification of target messenger RNA substrates for the murine deleted in azoospermia-like RNA-binding protein. Biol. Reprod. 2002, 66:475-485.
24. Reynolds N., Collier B., Bingham V., Gray N.K., Cooke H.J. Translation of the synaptonemal complex component Sycp3 is enhanced in vivo by the germ cell specific regulator Dazl. RNA 2007, 13:974-981.
25. Reynolds N., Collier B., Maratou K., Bingham V., Speed R.M., Taggart M., Semple C.A., Gray N.K., Cooke H.J. Dazl binds in vivo to specific transcripts and can regulate the pre-meiotic translation of Mvh in germ cells. Hum. Mol. Genet. 2005, 14:3899-3909.
26. Zeng M., Deng W., Wang X., Qiu W., Liu Y., Sun H., Tao D., Zhang S., Ma Y. DAZL binds to the transcripts of several Tssk genes in germ cells. BMB Rep. 2008, 41:300-304.
27. Matlin A.J., Clark F., Smith C.W. Understanding alternative splicing: towards a cellular code. Nat. Rev. Mol. Cell Biol. 2005, 6:386-398.
28. Stamm S., Ben-Ari S., Rafalska I., Tang Y., Zhang Z., Toiber D., Thanaraj T.A., Soreq H. Function of alternative splicing. Gene 2005, 344:1-20.
29. Coulombre J.L., Russel E.S. Analysis of the pleiotropism at the W-locus in the mouse; the effect of W and W substitution upon postnatal development of germ cells. J. Exp. Zool. 1954, 126:277-296.
30. Lyon M.F., Hawkes S.G. X-linked gene for testicular feminization in the mouse. Nature 1970, 227:1217-1219.
31. Moutier R. New mutation causing sterility restricted to the male in rats and mice. The Laboratory Animal in the Study of Reproduction 1976, 115-117.
32. Bennett W.I., Gall A.M., Southard J.L., Sidman R.L. Abnormal spermiogenesis in quaking, a myelin-deficient mutant mouse. Biol. Reprod. 1971, 5:30-58.
33. Zimmermann S., Steding G., Emmen J.M., Brinkmann A.O., Nayernia K., Holstein A.F., Engel W., Adham I.M. Targeted disruption of the Insl3 gene causes bilateral cryptorchidism. Mol. Endocrinol. 1999, 13:681-691.
34. Lee J.H., Schutte D., Wulf G., Fuzesi L., Radzun H.J., Schweyer S., Engel W., Nayernia K. Stem-cell protein Piwil2 is widely expressed in tumors and inhibits apoptosis through activation of Stat3/Bcl-XL pathway. Hum. Mol. Genet. 2006, 15:201-211.
35. Khromov T., Pantakani D.V., Nolte J., Wolf M., Dressel R., Engel W., Zechner U. Global and gene-specific histone modification profiles of mouse multipotent adult germline stem cells. Mol. Hum. Reprod. 2011, 17:166-174.
36. Smorag L., Zheng Y., Nolte J., Zechner U., Engel W., Pantakani D.V. MicroRNA signature in various cell types of mouse spermatogenesis: Evidence for stage-specifically expressed miRNA-221, -203, and -34b-5p mediated spermatogenesis regulation. Biol. Cell 2012, 104:677-692.
37. Meyer S., Nolte J., Opitz L., Salinas-Riester G., Engel W. Pluripotent embryonic stem cells and multipotent adult germline stem cells reveal similar transcriptomes including pluripotency-related genes. Mol. Hum. Reprod. 2010, 16:846-855.
38. Townley-Tilson W.H., Pendergrass S.A., Marzluff W.F., Whitfield M.L. Genome-wide analysis of mRNAs bound to the histone stem-loop binding protein. RNA 2006, 12:1853-1867.
39. Schulz C., Lytovchenko O., Melin J., Chacinska A., Guiard B., Neumann P., Ficner R., Jahn O., Schmidt B., Rehling P. Tim50's presequence receptor domain is essential for signal driven transport across the TIM23 complex. J. Cell Biol. 2011, 195:643-656.
40. Crimmins D.L., Mische S.M., Denslow N.D. Chemical cleavage of proteins in solution. Curr. Protoc. Protein Sci. 2005, 14. (Chapter 11, Unit 11).
41. Lee K.H., Lee S., Kim B., Chang S., Kim S.W., Paick J.S., Rhee K. Dazl can bind to dynein motor complex and may play a role in transport of specific mRNAs. EMBO J. 2006, 25:4263-4270.
42. Williamson M.P. The structure and function of proline-rich regions in proteins. Biochem. J. 1994, 297(Pt 2):249-260.
43. Tsui S., Dai T., Roettger S., Schempp W., Salido E.C., Yen P.H. Identification of two novel proteins that interact with germ-cell-specific RNA-binding proteins DAZ and DAZL1. Genomics 2000, 65:266-273.
44. Gorgoni B., Gray N.K. The roles of cytoplasmic poly(A)-binding proteins in regulating gene expression: a developmental perspective. Brief. Funct. Genomics Proteomic 2004, 3:125-141.
45. Kim B., Cooke H.J., Rhee K. DAZL is essential for stress granule formation implicated in germ cell survival upon heat stress. Development 2012, 139:568-578.
46. Maines J.Z., Wasserman S.A. Post-transcriptional regulation of the meiotic Cdc25 protein Twine by the Dazl orthologue Boule. Nat. Cell Biol. 1999, 1:171-174.
47. Maegawa S., Yamashita M., Yasuda K., Inoue K. Zebrafish DAZ-like protein controls translation via the sequence 'GUUC'. Genes Cells 2002, 7:971-984.
48. Tsui S., Dai T., Warren S.T., Salido E.C., Yen P.H. Association of the mouse infertility factor DAZL1 with actively translating polyribosomes. Biol. Reprod. 2000, 62:1655-1660.
49. Zeng M., Lu Y., Liao X., Li D., Sun H., Liang S., Zhang S., Ma Y., Yang Z. DAZL binds to 3[U+02B9]UTR of Tex19.1 mRNAs and regulates Tex19.1 expression. Mol. Biol. Rep. 2009, 36:2399-2403.
50. Morton S., Yang H.T., Moleleki N., Campbell D.G., Cohen P., Rousseau S. Phosphorylation of the ARE-binding protein DAZAP1 by ERK2 induces its dissociation from DAZ. Biochem. J. 2006, 399:265-273.
51. Brook M., Smith J.W., Gray N.K. The DAZL and PABP families: RNA-binding proteins with interrelated roles in translational control in oocytes. Reproduction 2009, 137:595-617.
52. Gill M.E., Hu Y.C., Lin Y., Page D.C. Licensing of gametogenesis, dependent on RNA binding protein DAZL, as a gateway to sexual differentiation of fetal germ cells. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:7443-7448.
53. Fox M., Urano J., Reijo Pera R.A. Identification and characterization of RNA sequences to which human PUMILIO-2 (PUM2) and deleted in Azoospermia-like (DAZL) bind. Genomics 2005, 85:92-105.
54. Venables J.P., Ruggiu M., Cooke H.J. The RNA-binding specificity of the mouse Dazl protein. Nucleic Acids Res. 2001, 29:2479-2483.