The PR/SET domain Zinc finger protein Prdm4 regulates gene expression in embryonic stem cells but plays a nonessential role in the developing mouse embryo

Molecular and Cellular Biology

Volumn 33, Issue 19, 2013, Pages 3936-3950

  Bogani, Debora ^a   Morgan, Marc A J ^a,c   Nelson, Andrew C ^a   Costello, Ita ^a   McGouran, Joanna F ^b   Kessler, Benedikt M ^b   Robertson, Elizabeth J ^a   Bikoff, Elizabeth K ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; PROTEIN PRDM4; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

ALLELE; AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; COMBINATORIAL CHEMISTRY; CONTROLLED STUDY; DNA BINDING; EMBRYO; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; GENE; GENE EXPRESSION; HIGH THROUGHPUT SEQUENCING; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLURIPOTENT STEM CELL; PRDM4 GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; ZINC FINGER MOTIF;

ANIMALS; BASE SEQUENCE; BINDING SITES; BLOTTING, NORTHERN; BLOTTING, WESTERN; CELLS, CULTURED; CHROMATIN IMMUNOPRECIPITATION; DNA-BINDING PROTEINS; EMBRYO, MAMMALIAN; EMBRYONIC STEM CELLS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MALE; MICE; NODAL PROTEIN; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEIN BINDING; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SELEX APTAMER TECHNIQUE; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION FACTORS; ZINC FINGERS;

EID: 84886786164     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00498-13     Document Type: Article

References (85)

1. Fog CK, Galli GG, Lund AH. 2012. PRDM proteins: important players in differentiation and disease. Bioessays 34:50-60.
2. Fumasoni I, Meani N, Rambaldi D, Scafetta G, Alcalay M, Ciccarelli FD. 2007. Family expansion and gene rearrangements contributed to the functional specialization of PRDM genes in vertebrates. BMC Evol. Biol. 7:187. doi:10.1186/1471-2148-7-187.
3. Hohenauer T, Moore AW. 2012. The Prdm family: expanding roles in stem cells and development. Development 139:2267-2282.
4. Harper J, Mould A, Andrews RM, Bikoff EK, Robertson EJ. 2011. The transcriptional repressor Blimp1/Prdm1 regulates postnatal reprogramming of intestinal enterocytes. Proc. Natl. Acad. Sci. U. S. A. 108:10585- 10590.
5. Mould A, Morgan MA, Li L, Bikoff EK, Robertson EJ. 2012. Blimp1/ Prdm1 governs terminal differentiation of endovascular trophoblast giant cells and defines multipotent progenitors in the developing placenta. Genes Dev. 26:2063-2074.
6. Muncan V, Heijmans J, Krasinski SD, Buller NV, Wildenberg ME, Meisner S, Radonjic M, Stapleton KA, Lamers WH, Biemond I, van den Bergh Weerman MA, O'Carroll D, Hardwick JC, Hommes DW, van den Brink GR. 2011. Blimp1 regulates the transition of neonatal to adult intestinal epithelium. Nat. Commun. 2:452. doi:10.1038/ncomms1463.
7. Ohinata Y, Payer B, O'Carroll D, Ancelin K, Ono Y, Sano M, Barton SC, Obukhanych T, Nussenzweig M, Tarakhovsky A, Saitou M, Surani MA. 2005. Blimp1 is a critical determinant of the germ cell lineage in mice. Nature 436:207-213.
8. Robertson EJ, Charatsi I, Joyner CJ, Koonce CH, Morgan M, Islam A, Paterson C, Lejsek E, Arnold SJ, Kallies A, Nutt SL, Bikoff EK. 2007. Blimp1 regulates development of the posterior forelimb, caudal pharyngeal arches, heart and sensory vibrissae in mice. Development 134:4335-4345.
9. Vincent SD, Dunn NR, Sciammas R, Shapiro-Shalef M, Davis MM, Calame K, Bikoff EK, Robertson EJ. 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.
10. Yamaji M, Seki Y, Kurimoto K, Yabuta Y, Yuasa M, Shigeta M, Yamanaka K, Ohinata Y, Saitou M. 2008. Critical function of Prdm14 for the establishment of the germ cell lineage in mice. Nat. Genet. 40:1016-1022.
11. Seale P, Bjork B, Yang W, Kajimura S, Chin S, Kuang S, Scime A, Devarakonda S, Conroe HM, Erdjument-Bromage H, Tempst P, Rudnicki MA, Beier DR, Spiegelman BM. 2008. PRDM16 controls a brown fat/skeletal muscle switch. Nature 454:961-967.
12. Bjork BC, Turbe-Doan A, Prysak M, Herron BJ, Beier DR. 2010. Prdm16 is required for normal palatogenesis in mice. Hum. Mol. Genet. 19:774-789.
13. Aguilo F, Avagyan S, Labar A, Sevilla A, Lee DF, Kumar P, Lemischka IR, Zhou BY, Snoeck HW. 2011. Prdm16 is a physiologic regulator of hematopoietic stem cells. Blood 117:5057-5066.
14. Goyama S, Yamamoto G, Shimabe M, Sato T, Ichikawa M, Ogawa S, Chiba S, Kurokawa M. 2008. Evi-1 is a critical regulator for hematopoietic stem cells and transformed leukemic cells. Cell Stem Cell 3:207-220.
15. Baudat F, Buard J, Grey C, Fledel-Alon A, Ober C, Przeworski M, Coop G, de Massy B. 2010. PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science 327:836-840.
16. Myers S, Bowden R, Tumian A, Bontrop RE, Freeman C, MacFie TS, McVean G, Donnelly P. 2010. Drive against hotspot motifs in primates implicates the PRDM9 gene in meiotic recombination. Science 327:876-879.
17. Parvanov ED, Petkov PM, Paigen K. 2010. Prdm9 controls activation of mammalian recombination hotspots. Science 327:835. doi:10.1126 /science.1181495.
18. Jenuwein T. 2001. Re-SET-ting heterochromatin by histone methyltransferases. Trends Cell Biol. 11:266-273.
19. Kouzarides T. 2002. Histone methylation in transcriptional control. Curr. Opin. Genet. Dev. 12:198-209.
20. Pinheiro I, Margueron R, Shukeir N, Eisold M, Fritzsch C, Richter FM, Mittler G, Genoud C, Goyama S, Kurokawa M, Son J, Reinberg D, Lachner M, Jenuwein T. 2012. Prdm3 and Prdm16 are H3K9me1 methyltransferases required for mammalian heterochromatin integrity. Cell 150:948-960.
21. Bikoff EK, Morgan MA, Robertson EJ. 2009. An expanding job description for Blimp-1/PRDM1. Curr. Opin. Genet. Dev. 19:379-385.
22. Segurel L, Leffler EM, Przeworski M. 2011. The case of the fickle fingers: how the PRDM9 zinc finger protein specifies meiotic recombination hotspots in humans. PLoS Biol. 9:e1001211. doi:10.1371/journal.pbio .1001211.
23. Galli GG, Honnens de Lichtenberg K, Carrara M, Hans W, Wuelling M, Mentz B, Multhaupt HA, Fog CK, Jensen KT, Rappsilber J, Vortkamp A, Coulton L, Fuchs H, Gailus-Durner V, Hrabe de Angelis M, Calogero RA, Couchman JR, Lund AH. 2012. Prdm5 regulates collagen gene transcription by association with RNA polymerase II in developing bone. PLoS Genet. 8:e1002711. doi:10.1371/journal.pgen.1002711.
24. Ma Z, Swigut T, Valouev A, Rada-Iglesias A, Wysocka J. 2011. Sequence- specific regulator Prdm14 safeguards mouse ESCs from entering extraembryonic endoderm fates. Nat. Struct. Mol. Biol. 18:120-127.
25. Shaffer AL, Lin KI, Kuo TC, Yu X, Hurt EM, Rosenwald A, Giltnane JM, Yang L, Zhao H, Calame K, Staudt LM. 2002. Blimp-1 orchestrates plasma cell differentiation by extinguishing the mature B cell gene expression program. Immunity 17:51-62.
26. Chang DH, Angelin-Duclos C, Calame K. 2000. BLIMP-1: trigger for differentiation of myeloid lineage. Nat. Immunol. 1:169-176.
27. Horsley V, O'Carroll D, Tooze R, Ohinata Y, Saitou M, Obukhanych T, Nussenzweig M, Tarakhovsky A, Fuchs E. 2006. Blimp1 defines a progenitor population that governs cellular input to the sebaceous gland. Cell 126:597-609.
28. Martins G, Calame K. 2008. Regulation and functions of Blimp-1 in T and B lymphocytes. Annu. Rev. Immunol. 26:133-169.
29. Martins GA, Cimmino L, Liao J, Magnusdottir E, Calame K. 2008. Blimp-1 directly represses Il2 and the Il2 activator Fos, attenuating T cell proliferation and survival. J. Exp. Med. 205:1959-1965.
30. Magnusdottir E, Kalachikov S, Mizukoshi K, Savitsky D, Ishida-Yamamoto A, Panteleyev AA, Calame K. 2007. Epidermal terminal differentiation depends on B lymphocyte-induced maturation protein-1. Proc. Natl. Acad. Sci. U. S. A. 104:14988-14993.
31. Doody GM, Care MA, Burgoyne NJ, Bradford JR, Bota M, Bonifer C, Westhead DR, Tooze RM. 2010. An extended set of PRDM1/BLIMP1 target genes links binding motif type to dynamic repression. Nucleic Acids Res. 38:5336-5350.
32. Chittka A, Chao MV. 1999. Identification of a zinc finger protein whose subcellular distribution is regulated by serum and nerve growth factor. Proc. Natl. Acad. Sci. U. S. A. 96:10705-10710.
33. Chittka A, Nitarska J, Grazini U, Richardson WD. 2012. Transcription factor positive regulatory domain 4 (PRDM4) recruits protein arginine methyltransferase 5 (PRMT5) to mediate histone arginine methylation and control neural stem cell proliferation and differentiation. J. Biol. Chem. 287:42995-43006.
34. Kendall SE, Ryczko MC, Mehan M, Verdi JM. 2003. Characterization of NADE, NRIF and SC-1 gene expression during mouse neurogenesis. Brain Res. Dev. Brain Res. 144:151-158.
35. Briknarova K, Atwater DZ, Glicken JM, Maynard SJ, Ness TE. 2011. The PR/SET domain in PRDM4 is preceded by a zinc knuckle. Proteins 79:2341-2345.
36. Chittka A, Arevalo JC, Rodriguez-Guzman M, Perez P, Chao MV, Sendtner M. 2004. The p75NTR-interacting protein SC1 inhibits cell cycle progression by transcriptional repression of cyclin E. J. Cell Biol. 164:985-996.
37. Nagy A, Gertenstein M, Vinterstein K, Behringer R. 2003. Manipulating the mouse embryo: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
38. Kim KC, Geng L, Huang S. 2003. Inactivation of a histone methyltransferase by mutations in human cancers. Cancer Res. 63:7619-7623.
39. Hayashi S, Lewis P, Pevny L, McMahon AP. 2002. Efficient gene modulation in mouse epiblast using a Sox2Cre transgenic mouse strain. Mech. Dev. 119(Suppl 1):S97-S101.
40. Niwa H, Yamamura K, Miyazaki J. 1991. Efficient selection for highexpression transfectants with a novel eukaryotic vector. Gene 108:193-199.
41. Morgan MA, Mould AW, Li L, Robertson EJ, Bikoff EK. 2012. Alternative splicing regulates Prdm1/Blimp-1DNAbinding activities and corepressor interactions. Mol. Cell. Biol. 32:3403-3413.
42. Costello I, Biondi CA, Taylor JM, Bikoff EK, Robertson EJ. 2009. Smad4-dependent pathways control basement membrane deposition and endodermal cell migration at early stages of mouse development. BMC Dev. Biol. 9:54. doi:10.1186/1471-213X-9-54.
43. Schmidt D, Wilson MD, Spyrou C, Brown GD, Hadfield J, Odom DT. 2009. ChIP-seq: using high-throughput sequencing to discover protein-DNA interactions. Methods 48:240-248.
44. Lunter G, Goodson M. 2011. Stampy: a statistical algorithm for sensitive and fast mapping of Illumina sequence reads. Genome Res. 21:936-939.
45. Feng J, Liu T, Qin B, Zhang Y, Liu XS. 2012. Identifying ChIP-seq enrichment using MACS. Nat. Protoc. 7:1728-1740.
46. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, Liu XS. 2008. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9:R137. doi:10.1186/gb-2008 -9-9-r137.
47. Shin H, Liu T, Manrai AK, Liu XS. 2009. CEAS: cis-regulatory element annotation system. Bioinformatics 25:2605-2606.
48. Bailey TL, Elkan C. 1994. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol. 2:28-36.
49. McLean CY, Bristor D, Hiller M, Clarke SL, Schaar BT, Lowe CB, Wenger AM, Bejerano G. 2010. GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol. 28:495-501.
50. Parisi S, Cozzuto L, Tarantino C, Passaro F, Ciriello S, Aloia L, Antonini D, De Simone V, Pastore L, Russo T. 2010. Direct targets of Klf5 transcription factor contribute to the maintenance of mouse embryonic stem cell undifferentiated state. BMC Biol. 8:128. doi:10.1186/1741 -7007-8-128.
51. Huang DW, Sherman BT, Lempicki RA. 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4:44-57.
52. Huang da, W, Sherman BT, Lempicki RA. 2009. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37:1-13.
53. Yabuta Y, Kurimoto K, Ohinata Y, Seki Y, Saitou M. 2006. Gene expression dynamics during germline specification in mice identified by quantitative single-cell gene expression profiling. Biol. Reprod. 75:705-716.
54. Flicek P, Ahmed I, Amode MR, Barrell D, Beal K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fairley S, Fitzgerald S, Gil L, Garcia-Giron C, Gordon L, Hourlier T, Hunt S, Juettemann T, Kahari AK, Keenan S, Komorowska M, Kulesha E, Longden I, Maurel T, McLaren WM, Muffato M, Nag R, Overduin B, Pignatelli M, Pritchard B, Pritchard E, Riat HS, Ritchie GR, Ruffier M, Schuster M, Sheppard D, Sobral D, Taylor K, Thormann A, Trevanion S, White S, Wilder SP, Aken BL, Birney E, Cunningham F, Dunham I, Harrow J, Herrero J, Hubbard TJ, Johnson N, Kinsella R, Parker A, Spudich G, Yates A, Zadissa A, Searle SM. 2013. Ensembl 2013. Nucleic Acids Res. 41:D48-D55.
55. Kunarso G, Chia NY, Jeyakani J, Hwang C, Lu X, Chan YS, Ng HH, Bourque G. 2010. Transposable elements have rewired the core regulatory network of human embryonic stem cells. Nat. Genet. 42:631-634.
56. Zhu Z, Dumas JJ, Lietzke SE, Lambright DG. 2001. A helical turn motif in Mss4 is a critical determinant of Rab binding and nucleotide release. Biochemistry 40:3027-3036.
57. Thaw P, Baxter NJ, Hounslow AM, Price C, Waltho JP, Craven CJ. 2001. Structure of TCTP reveals unexpected relationship with guanine nucleotide-free chaperones. Nat. Struct. Biol. 8:701-704.
58. Lowther WT, Weissbach H, Etienne F, Brot N, Matthews BW. 2002. The mirrored methionine sulfoxide reductases of Neisseria gonorrhoeae pilB. Nat. Struct. Biol. 9:348-352.
59. Shapiro-Shelef M, Lin KI, McHeyzer-Williams LJ, Liao J, McHeyzer-Williams MG, Calame K. 2003. Blimp-1 is required for the formation of immunoglobulin secreting plasma cells and pre-plasma memory B cells. Immunity 19:607-620.
60. Shen MM. 2007. Nodal signaling: developmental roles and regulation. Development 134:1023-1034.
61. Kubo A, Shinozaki K, Shannon JM, Kouskoff V, Kennedy M, Woo S, Fehling HJ, Keller G. 2004. Development of definitive endoderm from embryonic stem cells in culture. Development 131:1651-1662.
62. Ogawa K, Saito A, Matsui H, Suzuki H, Ohtsuka S, Shimosato D, Morishita Y, Watabe T, Niwa H, Miyazono K. 2007. Activin-Nodal signaling is involved in propagation of mouse embryonic stem cells. J. Cell Sci. 120:55-65.
63. Yasunaga M, Tada S, Torikai-Nishikawa S, Nakano Y, Okada M, Jakt LM, Nishikawa S, Chiba T, Era T, Nishikawa S. 2005. Induction and monitoring of definitive and visceral endoderm differentiation of mouse ES cells. Nat. Biotechnol. 23:1542-1550.
64. Vallier L, Mendjan S, Brown S, Chng Z, Teo A, Smithers LE, Trotter MW, Cho CH, Martinez A, Rugg-Gunn P, Brons G, Pedersen RA. 2009. Activin/Nodal signalling maintains pluripotency by controlling Nanog expression. Development 136:1339-1349.
65. Ema M, Mori D, Niwa H, Hasegawa Y, Yamanaka Y, Hitoshi S, Mimura J, Kawabe Y, Hosoya T, Morita M, Shimosato D, Uchida K, Suzuki N, Yanagisawa J, Sogawa K, Rossant J, Yamamoto M, Takahashi S, Fujii-Kuriyama Y. 2008. Kruppel-like factor 5 is essential for blastocyst development and the normal self-renewal of mouse ESCs. Cell Stem Cell 3:555-567.
66. Jiang J, Chan YS, Loh YH, Cai J, Tong GQ, Lim CA, Robson P, Zhong S, Ng HH. 2008. A core Klf circuitry regulates self-renewal of embryonic stem cells. Nat. Cell Biol. 10:353-360.
67. Lee KL, Lim SK, Orlov YL, Yit LY, Yang H, Ang LT, Poellinger L, Lim B. 2011. Graded Nodal/Activin signaling titrates conversion of quantitative phospho-Smad2 levels into qualitative embryonic stem cell fate decisions. PLoS Genet. 7:e1002130. doi:10.1371/journal.pgen.1002130.
68. Skarnes WC, Rosen B, West AP, Koutsourakis M, Bushell W, Iyer V, Mujica AO, Thomas M, Harrow J, Cox T, Jackson D, Severin J, Biggs P, Fu J, Nefedov M, de Jong PJ, Stewart AF, Bradley A. 2011. A conditional knockout resource for the genome-wide study of mouse gene function. Nature 474:337-342.
69. Kinameri E, Inoue T, Aruga J, Imayoshi I, Kageyama R, Shimogori T, Moore AW. 2008. Prdm proto-oncogene transcription factor family expression and interaction with the Notch-Hes pathway in mouse neurogenesis. PLoS One 3:e3859. doi:10.1371/journal.pone.0003859.
70. Moore AW, Jan LY, Jan YN. 2002. hamlet, a binary genetic switch between single-and multiple-dendrite neuron morphology. Science 297: 1355-1358.
71. Baxendale S, Davison C, Muxworthy C, Wolff C, Ingham PW, Roy S. 2004. The B-cell maturation factor Blimp-1 specifies vertebrate slow-twitch muscle fiber identity in response to Hedgehog signaling. Nat. Gen. 36:88-93.
72. Elworthy S, Hargrave M, Knight R, Mebus K, Ingham PW. 2008. Expression of multiple slow myosin heavy chain genes reveals a diversity of zebrafish slow twitch muscle fibres with differing requirements for Hedgehog and Prdm1 activity. Development 135:2115-2126.
73. Hernandez-Lagunas L, Choi IF, Kaji T, Simpson P, Hershey C, Zhou Y, Zon L, Mercola M, Artinger KB. 2005. Zebrafish narrowminded disrupts the transcription factor prdm1 and is required for neural crest and sensory neuron specification. Dev. Biol. 278:347-357.
74. Vincent SD, Mayeuf A, Niro C, Saitou M, Buckingham M. 2012. Non conservation of function for the evolutionarily conserved prdm1 protein in the control of the slow twitch myogenic program in the mouse embryo. Mol. Biol. Evol. 29:3181-3191.
75. Yang XH, Huang S. 1999. PFM1 (PRDM4), a new member of the PRdomain family, maps to a tumor suppressor locus on human chromosome 12q23-q24.1. Genomics 61:319-325.
76. Geng Y, Eaton EN, Picon M, Roberts JM, Lundberg AS, Gifford A, Sardet C, Weinberg RA. 1996. Regulation of cyclin E transcription by E2Fs and retinoblastoma protein. Oncogene 12:1173-1180.
77. Norris DP, Brennan J, Bikoff EK, Robertson EJ. 2002. The Foxh1-dependent autoregulatory enhancer controls the level of Nodal signals in the mouse embryo. Development 129:3455-3468.
78. Vincent SD, Dunn NR, Hayashi S, Norris DP, Robertson EJ. 2003. Cell fate decisions within the mouse organizer are governed by graded Nodal signals. Genes Dev. 17:1646-1662.
79. Brennan J, Norris DP, Robertson EJ. 2002. Nodal activity in the node governs left-right asymmetry. Genes Dev. 16:2339-2344.
80. Norris DP, Robertson EJ. 1999. Asymmetric and node-specific nodal expression patterns are controlled by two distinct cis-acting regulatory elements. Genes Dev. 13:1575-1588.
81. Dahle O, Kumar A, Kuehn MR. 2010. Nodal signaling recruits the histone demethylase Jmjd3 to counteract polycomb-mediated repression at target genes. Sci. Signal. 3:ra48. doi:10.1126/scisignal.2000841.
82. Chen X, Xu H, Yuan P, Fang F, Huss M, Vega VB, Wong E, Orlov YL, Zhang W, Jiang J, Loh YH, Yeo HC, Yeo ZX, Narang V, Govindarajan KR, Leong B, Shahab A, Ruan Y, Bourque G, Sung WK, Clarke ND, Wei CL, Ng HH. 2008. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133:1106-1117.
83. Yamaji M, Ueda J, Hayashi K, Ohta H, Yabuta Y, Kurimoto K, Nakato R, Yamada Y, Shirahige K, Saitou M. 2013. PRDM14 ensures naive pluripotency through dual regulation of signaling and epigenetic pathways in mouse embryonic stem cells. Cell Stem Cell 12:368 -382.
84. Rugg-Gunn PJ, Cox BJ, Ralston A, Rossant J. 2010. Distinct histone modifications in stem cell lines and tissue lineages from the early mouse embryo. Proc. Natl. Acad. Sci. U. S. A. 107:10783-10790.
85. Ross SE, McCord AE, Jung C, Atan D, Mok SI, Hemberg M, Kim TK, Salogiannis J, Hu L, Cohen S, Lin Y, Harrar D, McInnes RR, Greenberg ME. 2012. Bhlhb5 and Prdm8 form a repressor complex involved in neuronal circuit assembly. Neuron 73:292-303.