Suppression of the SOX2 neural effector gene by PRDM1 promotes human germ cell fate in embryonic stem cells

Stem Cell Reports

Volumn 2, Issue 2, 2014, Pages 189-204

  Lin, I Ying ^a,b   Chiu, Feng Lan ^c   Yeang, Chen Hsiang ^d   Chen, Hsin Fu ^e,f   Chuang, Ching Yu ^c   Yang, Shii Yi ^a   Hou, Pei Shan ^c   Sintupisut, Nardnisa ^d   Ho, Hong Nerng ^e,f   Kuo, Hung Chih ^a,c   Lin, Kuo I ^a,b  

^a GENOMICS RESEARCH CENTER   (Taiwan)

^b NATIONAL YANG MING UNIVERSITY   (Taiwan)

^c INSTITUTE OF CELLULAR AND ORGANISMIC BIOLOGY   (Taiwan)

^d INSTITUTE OF STATISTICAL SCIENCE   (Taiwan)

^e NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^f NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; BONE MORPHOGENETIC PROTEIN 4; TRANSCRIPTION FACTOR SOX2; WNT3A PROTEIN; PRDM1 PROTEIN, HUMAN; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR SOX;

ARTICLE; CELL DIFFERENTIATION; CELL FATE; CELL LINEAGE; CONTROLLED STUDY; EMBRYONIC STEM CELL; GENE; GERM CELL; GONAD; HUMAN; HUMAN CELL; IN VITRO STUDY; NEURAL EFFECTOR GENE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSCRIPTOMICS; UPREGULATION; BIOLOGICAL MODEL; CYTOLOGY; EMBRYOLOGY; FETUS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM;

MUS;

BONE MORPHOGENETIC PROTEIN 4; CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; FETUS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GERM CELLS; GONADS; HUMANS; MODELS, BIOLOGICAL; REPRESSOR PROTEINS; SOXB1 TRANSCRIPTION FACTORS; WNT3A PROTEIN;

EID: 84893755859     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2013.12.009     Document Type: Article

References (44)

1. K. Ancelin, U.C. Lange, P. Hajkova, R. Schneider, A.J. Bannister, T. Kouzarides, and M.A. Surani Blimp1 associates with Prmt5 and directs histone arginine methylation in mouse germ cells Nat. Cell Biol. 8 2006 623 630
2. C. Angelin-Duclos, G. Cattoretti, K.I. Lin, and K. Calame Commitment of B lymphocytes to a plasma cell fate is associated with Blimp-1 expression in vivo J. Immunol. 165 2000 5462 5471
3. E.K. Bikoff, M.A. Morgan, and E.J. Robertson An expanding job description for Blimp-1/PRDM1 Curr. Opin. Genet. Dev. 19 2009 379 385
4. D.H. Castrillon, B.J. Quade, T.Y. Wang, C. Quigley, and C.P. Crum The human VASA gene is specifically expressed in the germ cell lineage Proc. Natl. Acad. Sci. USA 97 2000 9585 9590
5. D.H. Chang, G. Cattoretti, and K.L. Calame The dynamic expression pattern of B lymphocyte induced maturation protein-1 (Blimp-1) during mouse embryonic development Mech. Dev. 117 2002 305 309
6. H.F. Chen, H.C. Kuo, C.L. Chien, C.T. Shun, Y.L. Yao, P.L. Ip, C.Y. Chuang, C.C. Wang, Y.S. Yang, and H.N. Ho Derivation, characterization and differentiation of human embryonic stem cells: comparing serum-containing versus serum-free media and evidence of germ cell differentiation Hum. Reprod. 22 2007 567 577
7. L.F. Chu, M.A. Surani, R. Jaenisch, and T.P. Zwaka Blimp1 expression predicts embryonic stem cell development in vitro Curr. Biol. 21 2011 1759 1765
8. C.Y. Chuang, K.I. Lin, M. Hsiao, L. Stone, H.F. Chen, Y.H. Huang, S.P. Lin, H.N. Ho, and H.C. Kuo Meiotic competent human germ cell-like cells derived from human embryonic stem cells induced by BMP4/WNT3A signaling and OCT4/EpCAM (epithelial cell adhesion molecule) selection J. Biol. Chem. 287 2012 14389 14401
9. A.T. Clark Establishment and differentiation of human embryonic stem cell derived germ cells Soc. Reprod. Fertil. Suppl. 63 2007 77 86
10. J. de Jong, H. Stoop, A.J. Gillis, R.J. van Gurp, G.J. van de Geijn, Md. Boer, R. Hersmus, P.T. Saunders, R.A. Anderson, J.W. Oosterhuis, and L.H. Looijenga Differential expression of SOX17 and SOX2 in germ cells and stem cells has biological and clinical implications J. Pathol. 215 2008 21 30
11. B.T. Phillips, M.M. McGuire, J.M. Barringer, H. Valli, B.P. Hermann, C.R. Simerly, A. Rajkovic, T. Miki, and K.E. Orwig et al. Direct Differentiation of Human Pluripotent Stem Cells into Haploid Spermatogenic Cells Cell reports 2 2012 440 446
12. B. Freeman The active migration of germ cells in the embryos of mice and men is a myth Reproduction 125 2003 635 643
13. T.L. Gaskell, A. Esnal, L.L. Robinson, R.A. Anderson, and P.T. Saunders Immunohistochemical profiling of germ cells within the human fetal testis: identification of three subpopulations Biol. Reprod. 71 2004 2012 2021
14. N. Geijsen, M. Horoschak, K. Kim, J. Gribnau, K. Eggan, and G.Q. Daley Derivation of embryonic germ cells and male gametes from embryonic stem cells Nature 427 2004 148 154
15. V. Graham, J. Khudyakov, P. Ellis, and L. Pevny SOX2 functions to maintain neural progenitor identity Neuron 39 2003 749 765
16. P. Hajkova, S. Erhardt, N. Lane, T. Haaf, O. El-Maarri, W. Reik, J. Walter, and M.A. Surani Epigenetic reprogramming in mouse primordial germ cells Mech. Dev. 117 2002 15 23
17. A. Hemmati-Brivanlou, and D. Melton Vertebrate embryonic cells will become nerve cells unless told otherwise Cell 88 1997 13 17
18. P.S. Hou, C.Y. Chuang, C.F. Kao, S.J. Chou, L. Stone, H.N. Ho, C.L. Chien, and H.C. Kuo LHX2 regulates the neural differentiation of human embryonic stem cells via transcriptional modulation of PAX6 and CER1 Nucleic Acids Res. 41 2013 7753 7770
19. B. Houmard, C. Small, L. Yang, T. Naluai-Cecchini, E. Cheng, T. Hassold, and M. Griswold Global gene expression in the human fetal testis and ovary Biol. Reprod. 81 2009 438 443
20. H.P. Huang, P.H. Chen, W.L. Hwu, C.Y. Chuang, Y.H. Chien, L. Stone, C.L. Chien, L.T. Li, S.C. Chiang, and H.F. Chen et al. Human Pompe disease-induced pluripotent stem cells for pathogenesis modeling, drug testing and disease marker identification Hum. Mol. Genet. 20 2011 4851 4864
21. K. Hübner, G. Fuhrmann, L.K. Christenson, J. Kehler, R. Reinbold, R. De La Fuente, J. Wood, J.F. Strauss 3rd, M. Boiani, and H.R. Schöler Derivation of oocytes from mouse embryonic stem cells Science 300 2003 1251 1256
22. V.T. Julaton, and R.A. Reijo Pera NANOS3 function in human germ cell development Hum. Mol. Genet. 20 2011 2238 2250
23. K. Kee, J.M. Gonsalves, A.T. Clark, and R.A. Pera Bone morphogenetic proteins induce germ cell differentiation from human embryonic stem cells Stem Cells Dev. 15 2006 831 837
24. K. Kee, V.T. Angeles, M. Flores, H.N. Nguyen, and R.A. Reijo Pera Human DAZL, DAZ and BOULE genes modulate primordial germ-cell and haploid gamete formation Nature 462 2009 222 225
25. J. Kehler, E. Tolkunova, B. Koschorz, M. Pesce, L. Gentile, M. Boiani, H. Lomelí, A. Nagy, K.J. McLaughlin, H.R. Schöler, and A. Tomilin Oct4 is required for primordial germ cell survival EMBO Rep. 5 2004 1078 1083
26. T.C. Kuo, and K.L. Calame B lymphocyte-induced maturation protein (Blimp)-1, IFN regulatory factor (IRF)-1, and IRF-2 can bind to the same regulatory sites J. Immunol. 173 2004 5556 5563
27. K. Kurimoto, Y. Yabuta, Y. Ohinata, M. Shigeta, K. Yamanaka, and M. Saitou Complex genome-wide transcription dynamics orchestrated by Blimp1 for the specification of the germ cell lineage in mice Genes Dev. 22 2008 1617 1635
28. P.B. Moens, and B. Spyropoulos Immunocytology of chiasmata and chromosomal disjunction at mouse meiosis Chromosoma 104 1995 175 182
29. T. Ng, F. Yu, and S. Roy A homologue of the vertebrate SET domain and zinc finger protein Blimp-1 regulates terminal differentiation of the tracheal system in the Drosophila embryo Dev. Genes Evol. 216 2006 243 252
30. Y. Ohinata, B. Payer, D. O'Carroll, K. Ancelin, Y. Ono, M. Sano, S.C. Barton, T. Obukhanych, M. Nussenzweig, and A. Tarakhovsky et al. Blimp1 is a critical determinant of the germ cell lineage in mice Nature 436 2005 207 213
31. Y. Ohinata, H. Ohta, M. Shigeta, K. Yamanaka, T. Wakayama, and M. Saitou A signaling principle for the specification of the germ cell lineage in mice Cell 137 2009 571 584
32. T.S. Park, Z. Galic, A.E. Conway, A. Lindgren, B.J. van Handel, M. Magnusson, L. Richter, M.A. Teitell, H.K. Mikkola, and W.E. Lowry et al. Derivation of primordial germ cells from human embryonic and induced pluripotent stem cells is significantly improved by coculture with human fetal gonadal cells Stem Cells 27 2009 783 795
33. R.M. Perrett, L. Turnpenny, J.J. Eckert, M. O'Shea, S.B. Sonne, I.T. Cameron, D.I. Wilson, E. Rajpert-De Meyts, and N.A. Hanley The early human germ cell lineage does not express SOX2 during in vivo development or upon in vitro culture Biol. Reprod. 78 2008 852 858
34. M. Saitou Germ cell specification in mice Curr. Opin. Genet. Dev. 19 2009 386 395
35. M. Saitou, S.C. Barton, and M.A. Surani A molecular programme for the specification of germ cell fate in mice Nature 418 2002 293 300
36. A.L. Shaffer, K.I. Lin, T.C. Kuo, X. Yu, E.M. Hurt, A. Rosenwald, J.M. Giltnane, L. Yang, H. Zhao, K. Calame, and L.M. Staudt Blimp-1 orchestrates plasma cell differentiation by extinguishing the mature B cell gene expression program Immunity 17 2002 51 62
37. A.I. Su, T. Wiltshire, S. Batalov, H. Lapp, K.A. Ching, D. Block, J. Zhang, R. Soden, M. Hayakawa, and G. Kreiman et al. A gene atlas of the mouse and human protein-encoding transcriptomes Proc. Natl. Acad. Sci. USA 101 2004 6062 6067
38. S.T. Su, H.Y. Ying, Y.K. Chiu, F.R. Lin, M.Y. Chen, and K.I. Lin Involvement of histone demethylase LSD1 in Blimp-1-mediated gene repression during plasma cell differentiation Mol. Cell. Biol. 29 2009 1421 1431
39. M.A. Surani Germ cells: the eternal link between generations C. R. Biol. 330 2007 474 478
40. S.S. Tanaka, Y.L. Yamaguchi, B. Tsoi, H. Lickert, and P.P. Tam IFITM/Mil/fragilis family proteins IFITM1 and IFITM3 play distinct roles in mouse primordial germ cell homing and repulsion Dev. Cell 9 2005 745 756
41. S.D. Vincent, N.R. Dunn, R. Sciammas, M. Shapiro-Shalef, M.M. Davis, K. Calame, E.K. Bikoff, and E.J. Robertson The zinc finger transcriptional repressor Blimp1/Prdm1 is dispensable for early axis formation but is required for specification of primordial germ cells in the mouse Development 132 2005 1315 1325
42. Z. Wang, E. Oron, B. Nelson, S. Razis, and N. Ivanova Distinct lineage specification roles for NANOG, OCT4, and SOX2 in human embryonic stem cells Cell Stem Cell 10 2012 440 454
43. Y. Yabuta, K. Kurimoto, Y. Ohinata, Y. Seki, and M. Saitou Gene expression dynamics during germline specification in mice identified by quantitative single-cell gene expression profiling Biol. Reprod. 75 2006 705 716
44. X. Zhang, C.T. Huang, J. Chen, M.T. Pankratz, J. Xi, J. Li, Y. Yang, T.M. Lavaute, X.J. Li, and M. Ayala et al. Pax6 is a human neuroectoderm cell fate determinant Cell Stem Cell 7 2010 90 100