Complex genome-wide transcription dynamics orchestrated by Blimp1 for the specification of the germ cell lineage in mice

Genes and Development

Volumn 22, Issue 12, 2008, Pages 1617-1635

  Kurimoto, Kazuki ^a   Yabuta, Yukihiro ^a   Ohinata, Yasuhide ^a   Shigeta, Mayo ^a   Yamanaka, Kaori ^a   Saitou, Mitinori ^a,b  

^a RIKEN KOBE INSTITUTE   (Japan)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

Blimp1 Prdm1; Cell fate specification; Genome wide gene expression profiling; Primordial germ cells; Single cell analysis

Indexed keywords

B LYMPHOCYTE INDUCED MATURATION PROTEIN 1;

ANIMAL CELL; ARTICLE; CELL FATE; CONTROLLED STUDY; ECTODERM; GENE REGULATORY NETWORK; GENETIC DAMAGE; GENETIC TRANSCRIPTION; GERM CELL; MESODERM; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; BODY PATTERNING; CELL LINEAGE; CLUSTER ANALYSIS; EMBRYO, MAMMALIAN; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, DEVELOPMENTAL; GENOME; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, BIOLOGICAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

MUS;

EID: 45349107280     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1649908     Document Type: Article

References (63)

1. Ancelin, K., Lange, U.C., Hajkova, P., Schneider, R., Bannister, A.J., Kouzarides, T., and Surani, M.A. 2006. Blimp1 associates with Prmt5 and directs histone arginine methylation in mouse germ cells. Nat. Cell Biol. 8: 623-630.
2. Avilion, A.A., Nicolis, S.K., Pevny, L.H., Perez, L., Vivian, N., and Lovell-Badge, R. 2003. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes & Dev. 17: 126-140.
3. Bortvin, A., Eggan, K., Skaletsky, H., Akutsu, H., Berry, D.L., Yanagimachi, R., Page, D.C., and Jaenisch, R. 2003. Incomplete reactivation of Oct4-related genes in mouse embryos cloned from somatic nuclei. Development 130: 1673-1680.
4. Bostick, M., Kim, J.K., Esteve, P.O., Clark, A., Pradhan, S., and Jacobsen, S.E. 2007. UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science 317: 1760-1764.
5. Buehr, M., McLaren, A., Bartley, A., and Darling, S. 1993. Proliferation and migration of primordial germ cells in We/We mouse embryos. Dev. Dyn. 198: 182-189.
6. Chang, H. and Matzuk, M.M. 2001. Smad5 is required for mouse primordial germ cell development. Mech. Dev. 104: 61-67.
7. Chiquoine, A.D. 1954. The identification, origin and migration of the primordial germ cells in the mouse embryo. Anat. Rec. 118: 135-146.
8. Chu, G.C., Dunn, N.R., Anderson, D.C., Oxburgh, L., and Robertson, E.J. 2004. Differential requirements for Smad4 in TGFβ-dependent patterning of the early mouse embryo. Development 131: 3501-3512.
9. Ciruna, B. and Rossant, J. 2001. FGF signaling regulates mesoderm cell fate specification and morphogenetic movement at the primitive streak. Dev. Cell 1: 37-49.
10. Eisen, M.B., Spellman, P.T., Brown, P.O., and Botstein, D. 1998. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. 95: 14863-14868.
11. Extavour, C.G. and Akam, M. 2003. Mechanisms of germ cell specification across the metazoans: Epigenesis and preformation. Development 130: 5869-5884.
12. Ginsburg, M., Snow, M.H., and McLaren, A. 1990. Primordial germ cells in the mouse embryo during gastrulation. Development 110: 521-528.
13. Gyory, I., Wu, J., Fejer, G., Seto, E., and Wright, K.L. 2004. PRDIBF1 recruits the histone H3 methyltransferase G9a in transcriptional silencing. Nat. Immunol. 5: 299-308.
14. Hacohen, N., Kramer, S., Sutherland, D., Hiromi, Y., and Krasnow, M.A. 1998. sprouty encodes a novel antagonist of FGF signaling that patterns apical branching of the Drosophila airways. Cell 92: 253-263.
15. Hayashi, K., Kobayashi, T., Umino, T., Goitsuka, R., Matsui, Y., and Kitamura, D. 2002. SMAD1 signaling is critical for initial commitment of germ cell lineage from mouse epiblast. Mech. Dev. 118: 99-109.
16. Hayashi, K., de Sousa Lopes, S.M., and Surani, M.A. 2007. Germ cell specification in mice. Science 316: 394-396.
17. Horsley, V., O'Carroll, D., Tooze, R., Ohinata, Y., Saitou, M., Obukhanych, T., Nussenzweig, M., Tarakhovsky, A., and Fuchs, E. 2006. Blimp1 defines a progenitor population that governs cellular input to the sebaceous gland. Cell 126: 597-609.
18. Hosack, D.A., Dennis Jr., G., Sherman, B.T., Lane, H.C., and Lempicki, R.A. 2003. Identifying biological themes within lists of genes with EASE. Genome Biol. 4: R70. doi: 10.1186/gb-2003-4-10-r70.
19. Kallies, A., Hasbold, J., Tarlinton, D.M., Dietrich, W., Corcoran, L.M., Hodgkin, P.D., and Nutt, S.L. 2004. Plasma cell ontogeny defined by quantitative changes in blimp-1 expression. J. Exp. Med. 200: 967-977.
20. Kuo, T.C. and Calame, K.L. 2004. 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: 5556-5563.
21. Kurimoto, K., Yabuta, Y., Ohinata, Y., Ono, Y., Uno, K.D., Yamada, R.G., Ueda, H.R., and Saitou, M. 2006. An improved single-cell cDNA amplification method for efficient high-density oligonucleotide microarray analysis. Nucleic Acids Res. 34: e42. doi: 10.1093/nar/gkl050.
22. Kurimoto, K., Yabuta, Y., Ohinata, Y., and Saitou, M. 2007. Global single-cell cDNA amplification to provide a template for representative high-density oligonucleotide microarray analysis. Nat. Protoc. 2: 739-752.
23. Lawson, K.A. and Hage, W.J. 1994. Clonal analysis of the origin of primordial germ cells in the mouse. Ciba Found. Symp. 182: 68-84.
24. Lawson, K.A., Dunn, N.R., Roelen, B.A., Zeinstra, L.M., Davis, A.M., Wright, C.V., Korving, J.P., and Hogan, B.L. 1999. Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes & Dev. 13: 424-436.
25. Lee, J.M., Dedhar, S., Kalluri, R., and Thompson, E.W. 2006. The epithelial-mesenchymal transition: New insights in signaling, development, and disease. J. Cell Biol. 172: 973-981.
26. Lin, Y., Wong, K., and Calame, K. 1997. Repression of c-myc transcription by Blimp-1, an inducer of terminal B cell differentiation. Science 276: 596-599.
27. Lin, K.I., Angelin-Duclos, C., Kuo, T.C., and Calame, K. 2002. Blimp-1-dependent repression of Pax-5 is required for differentiation of B cells to immunoglobulin M-secreting plasma cells. Mol. Cell. Biol. 22: 4771-4780.
28. Magnusdottir, E., Kalachikov, S., Mizukoshi, K., Savitsky, D., Ishida-Yamamoto, A., Panteleyev, A.A., and Calame, K. 2007. Epidermal terminal differentiation depends on B lymphocyte-induced maturation protein-1. Proc. Natl. Acad. Sci. 104: 14988-14993.
29. Maruyama, M., Ichisaka, T., Nakagawa, M., and Yamanaka, S. 2005. Differential roles for Sox15 and Sox2 in transcriptional control in mouse embryonic stem cells. J. Biol. Chem. 280: 24371-24379.
30. Mintz, B. and Russell, E.S. 1957. Gene-induced embryological modifications of primordial germ cells in the mouse. J. Exp. Zool. 134: 207-237.
31. Nagai, T., Ibata, K., Park, E.S., Kubota, M., Mikoshiba, K., and Miyawaki, A. 2002. A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat. Biotechnol. 20: 87-90.
32. Nishikawa, S., Kusakabe, M., Yoshinaga, K., Ogawa, M., Hayashi, S., Kunisada, T., Era, T., and Sakakura, T. 1991. In utero manipulation of coat color formation by a monoclonal anti-c-kit antibody: Two distinct waves of c-kit-dependency during melanocyte development. EMBO J. 10: 2111-2118.
33. Ohinata, Y., Payer, B., O'Carroll, D., Ancelin, K., Ono, Y., Sano, M., Barton, S.C., Obukhanych, T., Nussenzweig, M., Tarakhovsky, A., et al. 2005. Blimp1 is a critical determinant of the germ cell lineage in mice. Nature 436: 207-213.
34. Peinado, H., Olmeda, D., and Cano, A. 2007. Snail, Zeb and bHLH factors in tumour progression: An alliance against the epithelial phenotype? Nat. Rev. Cancer 7: 415-428.
35. Piskurich, J.F., Lin, K.I., Lin, Y., Wang, Y., Ting, J.P., and Calame, K. 2000. BLIMP-I mediates extinction of major histocompatibility class II transactivator expression in plasma cells. Nat. Immunol. 1: 526-532.
36. R Development Core Team. 2005. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
37. Ren, B., Chee, K.J., Kim, T.H., and Maniatis, T. 1999. PRDIBF1/Blimp-1 repression is mediated by corepressors of the Groucho family of proteins. Genes & Dev. 13: 125-137.
38. Robertson, E.J., Charatsi, I., Joyner, C.J., Koonce, C.H., Morgan, M., Islam, A., Paterson, C., Lejsek, E., Arnold, S.J., Kallies, A., et al. 2007. Blimp1 regulates development of the posterior forelimb, caudal pharyngeal arches, heart and sensory vibrissae in mice. Development 134: 4335-4345.
39. Saeed, A.I., Sharov, V., White, J., Li, J., Liang, W., Bhagabati, N., Braisted, J., Klapa, M., Currier, T., Thiagarajan, M., et al. 2003. TM4: A free, open-source system for microarray data management and analysis. Biotechniques 34: 374-378.
40. Saitou, M., Barton, S.C., and Surani, M.A. 2002. A molecular programme for the specification of germ cell fate in mice. Nature 418: 293-300.
41. Saitou, M., Payer, B., O'Carroll, D., Ohinata, Y., and Surani, M.A. 2005. Blimp1 and the emergence of the germ line during development in the mouse. Cell Cycle 4: 1736-1740.
42. Sato, M., Kimura, T., Kurokawa, K., Fujita, Y., Abe, K., Masuhara, M., Yasunaga, T., Ryo, A., Yamamoto, M., and Nakano, T. 2002. Identification of PGC7, a new gene expressed specifically in preimplantation embryos and germ cells. Mech. Dev. 113: 91-94.
43. Sciammas, R. and Davis, M.M. 2004. Modular nature of Blimp-1 in the regulation of gene expression during B cell maturation. J. Immunol. 172: 5427-5440.
44. Seki, Y., Hayashi, K., Itoh, K., Mizugaki, M., Saitou, M., and Matsui, Y. 2005. Extensive and orderly reprogramming of genome-wide chromatin modifications associated with specification and early development of germ cells in mice. Dev. Biol. 278: 440-458.
45. Seki, Y., Yamaji, M., Yabuta, Y., Sano, M., Shigeta, M., Matsui, Y., Saga, Y., Tachibana, M., Shinkai, Y., and Saitou, M. 2007. Cellular dynamics associated with the genome-wide epigenetic reprogramming in migrating primordial germ cells in mice. Development 134: 2627-2638.
46. Seydoux, G. and Braun, R.E. 2006. Pathway to totipotency: Lessons from germ cells. Cell 127: 891-904.
47. Shaffer, A.L., Lin, K.I., Kuo, T.C., Yu, X., Hurt, E.M., Rosenwald, A., Giltnane, J.M., Yang, L., Zhao, H., Calame, K., et al. 2002. Blimp-1 orchestrates plasma cell differentiation by extinguishing the mature B cell gene expression program. Immunity 17: 51-62.
48. Sharif, J., Muto, M., Takebayashi, S., Suetake, I., Iwamatsu, A., Endo, T.A., Shinga, J., Mizutani-Koseki, Y., Toyoda, T., Okamura, K., et al. 2007. The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature 450: 908-912.
49. Takahashi, K. and Yamanaka, S. 2006. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676.
50. Tam, P.P. and Snow, M.H. 1981. Proliferation and migration of primordial germ cells during compensatory growth in mouse embryos. J. Embryol. Exp. Morphol. 64: 133-147.
51. Tanaka, S.S. and Matsui, Y. 2002. Developmentally regulated expression of mil-1 and mil-2, mouse interferon-induced transmembrane protein like genes, during formation and differentiation of primordial germ cells. Mech. Dev. 119 (Suppl. 1): S261-S267.
52. Tanaka, S.S., Yamaguchi, Y.L., Tsoi, B., Lickert, H., and Tam, P.P. 2005. IFITM/Mil/fragilis family proteins IFITM1 and IFITM3 play distinct roles in mouse primordial germ cell homing and repulsion. Dev. Cell 9: 745-756.
53. Tremblay, K.D., Dunn, N.R., and Robertson, E.J. 2001. Mouse embryos lacking Smad1 signals display defects in extra-embryonic tissues and germ cell formation. Development 128: 3609-3621.
54. Tsuda, M., Sasaoka, Y., Kiso, M., Abe, K., Haraguchi, S., Kobayashi, S., and Saga, Y. 2003. Conserved role of nanos proteins in germ cell development. Science 301: 1239-1241.
55. Turner Jr., C.A., Mack, D.H., and Davis, M.M. 1994. Blimp-1, a novel zinc finger-containing protein that can drive the maturation of B lymphocytes into immunoglobulin-secreting cells. Cell 77: 297-306.
56. Vincent, S.D., Dunn, N.R., Sciammas, R., Shapiro-Shalef, M., Davis, M.M., Calame, K., Bikoff, E.K., and Robertson, E.J. 2005. 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: 1315-1325.
57. Wood, H.B. and Episkopou, V. 1999. Comparative expression of the mouse Sox1, Sox2 and Sox3 genes from pre-gastrulation to early somite stages. Mech. Dev. 86: 197-201.
58. Yabuta, Y., Kurimoto, K., Ohinata, Y., Seki, Y., and Saitou, M. 2006. Gene expression dynamics during germline specification in mice identified by quantitative single-cell gene expression profiling. Biol. Reprod. 75: 705-716.
59. Yeung, K.Y. and Ruzzo, W.L. 2001. Principal component analysis for clustering gene expression data. Bioinformatics 17: 763-774.
60. Ying, Y. and Zhao, G.Q. 2001. Cooperation of endoderm-derived BMP2 and extraembryonic ectoderm-derived BMP4 in primordial germ cell generation in the mouse. Dev. Biol. 232: 484-492.
61. Ying, Y., Liu, X.M., Marble, A., Lawson, K.A., and Zhao, G.Q. 2000. Requirement of Bmp8b for the generation of primordial germ cells in the mouse. Mol. Endocrinol. 14: 1053-1063.
62. Youngren, K.K., Coveney, D., Peng, X., Bhattacharya, C., Schmidt, L.S., Nickerson, M.L., Lamb, B.T., Deng, J.M., Behringer, R.R., Capel, B., et al. 2005. The Ter mutation in the dead end gene causes germ cell loss and testicular germ cell tumours. Nature 435: 360-364.
63. Yu, J., Angelin-Duclos, C., Greenwood, J., Liao, J., and Calame, K. 2000. Transcriptional repression by blimp-1 (PRDI-BF1) involves recruitment of histone deacetylase. Mol. Cell. Biol. 20: 2592-2603.