Conserved roles of mouse DUX and human DUX4 in activating cleavage-stage genes and MERVL/HERVL retrotransposons

Nature Genetics

Volumn 49, Issue 6, 2017, Pages 925-934

  Hendrickson, Peter G ^a   Doráis, Jessie A ^a,b   Grow, Edward J ^a   Whiddon, Jennifer L ^c   Lim, Jong Won ^c   Wike, Candice L ^a   Weaver, Bradley D ^a   Pflueger, Christian ^a   Emery, Benjamin R ^b   Wilcox, Aaron L ^b   Nix, David A ^a   Peterson, C Matthew ^b   Tapscott, Stephen J ^c   Carrell, Douglas T ^b   Cairns, Bradley R ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c USA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR DUX4; TRANSCRIPTOME; UNCLASSIFIED DRUG; CHROMATIN; DUX4 PROTEIN, HUMAN; DUX4 PROTEIN, MOUSE; HOMEODOMAIN PROTEIN; RETROPOSON;

2 CELL EMBRYO LIKE CELL; ALTERNATIVE RNA SPLICING; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BINDING AFFINITY; CELLS BY BODY ANATOMY; GENE ACTIVATION; GENE EXPRESSION; HUMAN; MERVL HERVL GENE; MOUSE; MOUSE EMBRYONIC STEM CELL; NONHUMAN; OOCYTE CLEAVAGE; OOCYTE DEVELOPMENT; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; RETROPOSON; TRANSCRIPTION REGULATION; ADULT; ANIMAL; BLASTOCYST; CHROMATIN; FEMALE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; OOCYTE; PHYSIOLOGY; TRANSGENIC MOUSE;

ADULT; ALTERNATIVE SPLICING; ANIMALS; BLASTOCYST; CHROMATIN; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; HUMANS; MICE, TRANSGENIC; OOCYTES; RETROELEMENTS; TRANSCRIPTOME;

EID: 85018449904     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.3844     Document Type: Article

References (51)

1. Liu, L. et al. Telomere lengthening early in development. Nat. Cell Biol. 9, 1436-1441 (2007).
2. Matoba, S. et al. Embryonic development following somatic cell nuclear transfer impeded by persisting histone methylation. Cell 159, 884-895 (2014).
3. Chung, Y.G. et al. Histone demethylase expression enhances human somatic cell nuclear transfer efficiency and promotes derivation of pluripotent stem cells. Cell Stem Cell 17, 758-766 (2015).
4. Zalzman, M. et al. Zscan4 regulates telomere elongation and genomic stability in ES cells. Nature 464, 858-863 (2010).
5. Kalmbach, K., Robinson, L.G. Jr., Wang, F., Liu, L. & Keefe, D. Telomere length reprogramming in embryos and stem cells. BioMed Res. Int. 2014, 925121 (2014).
6. Macfarlan, T.S. et al. Endogenous retroviruses and neighboring genes are coordinately repressed by LSD1/KDM1A. Genes Dev. 25, 594-607 (2011).
7. Gifford, W.D., Pfaff, S.L. & Macfarlan, T.S. Transposable elements as genetic regulatory substrates in early development. Trends Cell Biol. 23, 218-226 (2013).
8. Macfarlan, T.S. et al. Embryonic stem cell potency fluctuates with endogenous retrovirus activity. Nature 487, 57-63 (2012).
9. Ishiuchi, T. et al. Early embryonic-like cells are induced by downregulating replication-dependent chromatin assembly. Nat. Struct. Mol. Biol. 22, 662-671 (2015).
10. Eckersley-Maslin, M.A. et al. MERVL/Zscan4 network activation results in transient genome-wide DNA demethylation of mESCs. Cell Rep. 17, 179-192 (2016).
11. Choi, Y.J. et al. Deficiency of microRNA miR-34a expands cell fate potential in pluripotent stem cells. Science 355, eaag1927 (2017).
12. Geng, L.N. et al. DUX4 activates germline genes, retroelements, and immune mediators: implications for facioscapulohumeral dystrophy. Dev. Cell 22, 38-51 (2012).
13. Young, J.M. et al. DUX4 binding to retroelements creates promoters that are active in FSHD muscle and testis. PLoS Genet. 9, e1003947 (2013).
14. Gertz, J. et al. Transposase mediated construction of RNA-seq libraries. Genome Res. 22, 134-141 (2012).
15. Xue, Z. et al. Genetic programs in human and mouse early embryos revealed by single-cell RNA sequencing. Nature 500, 593-597 (2013).
16. Yan, L. et al. Single-cell RNA-Seq profiling of human preimplantation embryos and embryonic stem cells. Nat. Struct. Mol. Biol. 20, 1131-1139 (2013).
17. Leidenroth, A. & Hewitt, J.E. A family history of DUX4: phylogenetic analysis of DUXA, B, C and Duxbl reveals the ancestral DUX gene. BMC Evol. Biol. 10, 364 (2010).
18. Holland, P.W.H., Booth, H.A.F. & Bruford, E.A. Classification and nomenclature of all human homeobox genes. BMC Biol. 5, 47 (2007).
19. Burglin, T.R. & Affolter, M. Homeodomain proteins: an update. Chromosoma 125, 497-521 (2016).
20. Dunwell, T.L. & Holland, P.W.H. Diversity of human and mouse homeobox gene expression in development and adult tissues. BMC Dev. Biol. 16, 40 (2016).
21. Madissoon, E. et al. Characterization and target genes of nine human PRD-like homeobox domain genes expressed exclusively in early embryos. Sci. Rep. 6, 28995 (2016).
22. Tohonen, V. et al. Novel PRD-like homeodomain transcription factors and retrotransposon elements in early human development. Nat. Commun. 6, 8207 (2015).
23. Jouhilahti, E.-M. et al. The human PRD-like homeobox gene LEUTX has a central role in embryo genome activation. Development 143, 3459-3469 (2016).
24. Ko, M.S.H. in Mammalian Preimplantation Development 120, 103-124 (Elsevier, 2016).
25. Goke, J. et al. Dynamic transcription of distinct classes of endogenous retroviral elements marks specific populations of early human embryonic cells. Cell Stem Cell 16, 135-141 (2015).
26. McLean, C.Y. et al. GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol. 28, 495-501 (2010).
27. Deng, Q., Ramskold, D., Reinius, B. & Sandberg, R. Single-cell RNA-seq reveals dynamic, random monoallelic gene expression in mammalian cells. Science 343, 193-196 (2014).
28. Leidenroth, A. et al. Evolution of DUX gene macrosatellites in placental mammals. Chromosoma 121, 489-497 (2012).
29. Clapp, J. et al. Evolutionary conservation of a coding function for D4Z4, the tandem DNA repeat mutated in facioscapulohumeral muscular dystrophy. Am. J. Hum. Genet. 81, 264-279 (2007).
30. Eidahl, J.O. et al. Mouse Dux is myotoxic and shares partial functional homology with its human paralog DUX4. Hum. Mol. Genet. 25, 4577-4589 (2016).
31. Schoorlemmer, J., Perez-Palacios, R., Climent, M., Guallar, D. & Muniesa, P. Regulation of mouse retroelement MuERV-L/MERVL expression by REX1 and epigenetic control of stem cell potency. Front. Oncol. 4, 14 (2014).
32. Kigami, D., Minami, N., Takayama, H. & Imai, H. MuERV-L is one of the earliest transcribed genes in mouse one-cell embryos. Biol. Reprod. 68, 651-654 (2003).
33. Ribet, D. et al. Murine endogenous retrovirus MuERV-L is the progenitor of the "orphan" epsilon viruslike particles of the early mouse embryo. J. Virol. 82, 1622-1625 (2008).
34. Buenrostro, J.D., Giresi, P.G., Zaba, L.C., Chang, H.Y. & Greenleaf, W.J. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 10, 1213-1218 (2013).
35. Wu, J. et al. The landscape of accessible chromatin in mammalian preimplantation embryos. Nature 534, 652-657 (2016).
36. Zhou, L.-Q. & Dean, J. Reprogramming the genome to totipotency in mouse embryos. Trends Cell Biol. 25, 82-91 (2015).
37. Ishiuchi, T. & Torres-Padilla, M.-E. Towards an understanding of the regulatory mechanisms of totipotency. Curr. Opin. Genet. Dev. 23, 512-518 (2013).
38. Harrison, M.M., Li, X.-Y., Kaplan, T., Botchan, M.R. & Eisen, M.B. Zelda binding in the early Drosophila melanogaster embryo marks regions subsequently activated at the maternal-to-zygotic transition. PLoS Genet. 7, e1002266 (2011).
39. Sun, Y. et al. Zelda overcomes the high intrinsic nucleosome barrier at enhancers during Drosophila zygotic genome activation. Genome Res. 25, 1703-1714 (2015).
40. Iwafuchi-Doi, M. & Zaret, K.S. Pioneer transcription factors in cell reprogramming. Genes Dev. 28, 2679-2692 (2014).
41. Morgani, S.M. & Brickman, J.M. The molecular underpinnings of totipotency. Phil. Trans. R. Soc. Lond. B 369, 20130549 (2014).
42. De Paepe, C., Krivega, M., Cauffman, G., Geens, M. & Van de Velde, H. Totipotency and lineage segregation in the human embryo. Mol. Hum. Reprod. 20, 599-618 (2014).
43. Borsos, M. & Torres-Padilla, M.-E. Building up the nucleus: nuclear organization in the establishment of totipotency and pluripotency during mammalian development. Genes Dev. 30, 611-621 (2016).
44. Yasuda, T. et al. Recurrent DUX4 fusions in B cell acute lymphoblastic leukemia of adolescents and young adults. Nat. Genet. 48, 569-574 (2016).
45. Zhang, J. et al. Deregulation of DUX4 and ERG in acute lymphoblastic leukemia. Nat. Genet. 48, 1481-1489 (2016).
46. Patro, R., Mount, S.M. & Kingsford, C. Sailfish enables alignment-free isoform quantification from RNA-seq reads using lightweight algorithms. Nat. Biotechnol. 32, 462-464 (2014).
47. Niakan, K.K. & Eggan, K. Analysis of human embryos from zygote to blastocyst reveals distinct gene expression patterns relative to the mouse. Dev. Biol. 375, 454-464 (2012).
48. Bailey, T.L. et al. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 37 (Suppl. 2), W202-W208 (2009).
49. Buenrostro, J.D., Giresi, P.G., Zaba, L.C., Chang, H.Y. & Greenleaf, W.J. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 10, 1213-1218 (2013).
50. Ramirez, F., Dundar, F., Diehl, S., Gruning, B.A. & Manke, T. deepTools: a flexible platform for exploring deep-sequencing data. Nucleic Acids Res. 42, W187-W191 (2014).
51. Yu, G., Wang, L.G. & He, Q.Y. ChIPseeker: an R/Bioconductor package for ChIP peak annotation, comparison and visualization. Bioinformatics 31, 2382-2383 (2015).