Impairment of preimplantation porcine embryo development by histone demethylase KDM5B knockdown through disturbance of bivalent H3K4me3-H3K27me3 modifications

Biology of Reproduction

Volumn 92, Issue 3, 2015, Pages

  Huang, Jiaojiao ^a,b   Zhang, Hongyong ^a,b   Wang, Xianlong ^a   Dobbs, Kyle B ^c,d   Yao, Jing ^a   Qin, Guosong ^a   Whitworth, Kristin ^c   Walters, Eric M ^c   Prather, Randall S ^c   Zhao, Jianguo ^a  

^a INSTITUTE OF ZOOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c UNIVERSITY OF MISSOURI   (United States)

^d NORTHEASTERN UNIVERSITY   (United States)

Author keywords

Embryonic development; H3K4me3; Histone demethylase; KDM5B; Pig

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; HISTONE DEMETHYLASE; HISTONE DEMETHYLASE KDM5B; HISTONE DEMETHYLASE KDM6A; HISTONE H3; HOX PROTEIN; HOXA13 PROTEIN; HOXA2 PROTEIN; HOXA3 PROTEIN; HOXA7 PROTEIN; HOXB4 PROTEIN; HOXB7 PROTEIN; HOXC8 PROTEIN; HOXD13 PROTEIN; HOXD8 PROTEIN; MORPHOLINO OLIGONUCLEOTIDE; OCTAMER TRANSCRIPTION FACTOR 4; TET1 PROTEIN; TET2 PROTEIN; TET3 PROTEIN; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; DNA BINDING PROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; BLASTOCYST; CONTROLLED STUDY; DNA METHYLATION; EMBRYO; EMBRYO DEVELOPMENT; GENE SILENCING; GENE TRANSLOCATION; HISTONE MODIFICATION; HOX GENE; NIDATION; NONHUMAN; PORCINE EMBRYO; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; EMBRYO CULTURE; EMBRYOLOGY; FEMALE; GENE DELETION; GENETICS; HOMEOBOX; METHYLATION; MOLECULAR GENETICS; PHYSIOLOGY; PIG;

MURINAE; SUIDAE; SUS;

AMINO ACID SEQUENCE; ANIMALS; DNA-BINDING PROTEINS; EMBRYO CULTURE TECHNIQUES; EMBRYONIC DEVELOPMENT; FEMALE; GENE DELETION; GENE KNOCKDOWN TECHNIQUES; GENES, HOMEOBOX; HISTONE DEMETHYLASES; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; METHYLATION; MOLECULAR SEQUENCE DATA; SWINE;

EID: 84928323123     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.114.122762     Document Type: Article

References (57)

1. Albert M, Schmitz SU, Kooistra SM, Malatesta M, Morales Torres C, Rekling JC, Johansen JV, Abarrategui I, Helin K. The histone demethylase Jarid1b ensures faithful mouse development by protecting developmental genes from aberrant H3K4me3. PLoS Genet 2013; 9:e1003461.
2. Dean W, Santos F, Reik W. Epigenetic reprogramming in early mammalian development and following somatic nuclear transfer. Semin Cell Dev Biol 2003; 14:93-100.
3. Dyban AP, Dyban PA. Theoretical and applied aspects of epigenetic reprogramming in mammalian development [in Russian]. Genetika 2006; 42:1615-1620.
4. Li E. Chromatin modification and epigenetic reprogramming in mammalian development. Nat Rev Genet 2002; 3:662-673.
5. Reik W, Dean W, Walter J. Epigenetic reprogramming in mammalian development. Science 2001; 293:1089-1093.
6. Santos F, Peters AH, Otte AP, Reik W, Dean W. Dynamic chromatin modifications characterise the first cell cycle in mouse embryos. Dev Biol 2005; 280:225-236.
7. Sasaki H, Matsui Y. Epigenetic events in mammalian germ-cell development: reprogramming and beyond. Nat Rev Genet 2008; 9: 129-140.
8. Surani MA, Hayashi K, Hajkova P. Genetic and epigenetic regulators of pluripotency. Cell 2007; 128:747-762.
9. Pacheco-Trigon S, Hennequet-Antier C, Oudin JF, Piumi F, Renard JP, Duranthon V. Molecular characterization of genomic activities at the onset of zygotic transcription in mammals. Biol Reprod 2002; 67:1907-1918.
10. Hamatani T, Carter MG, Sharov AA, Ko MS. Dynamics of global gene expression changes during mouse preimplantation development. Dev Cell 2004; 6:117-131.
11. Turner BM. Cellular memory and the histone code. Cell 2002; 111: 285-291.
12. Xu Y, Fang F. Histone methylation and transcriptional regulation in cardiovascular disease. Cardiovasc Hematol Disord Drug Targets 2014; 14:89-97.
13. An W. Histone acetylation and methylation: combinatorial players for transcriptional regulation. Subcell Biochem 2007; 41:351-369.
14. Miller JL, Grant PA. The role of DNA methylation and histone modifications in transcriptional regulation in humans. Subcell Biochem 2013; 61:289-317.
15. Huang C, Xu M, Zhu B. Epigenetic inheritance mediated by histone lysine methylation: maintaining transcriptional states without the precise restoration of marks?. Philos Trans R Soc Lond B Biol Sci 2013; 368: 20110332.
16. Rivera C, Gurard-Levin ZA, Almouzni G, Loyola A. Histone lysine methylation and chromatin replication. Biochim Biophys Acta 2014; 1839:1433-1439.
17. Blackledge NP, Klose RJ. Histone lysine methylation: an epigenetic modification? Epigenomics 2010; 2:151-161.
18. Ostrup O, Reiner AH, Alestrom P, Collas P. The specific alteration of histone methylation profiles by DZNep during early zebrafish development. Biochim Biophys Acta 2014; 1839:1307-1315.
19. Aday AW, Zhu LJ, Lakshmanan A, Wang J, Lawson ND. Identification of cis regulatory features in the embryonic zebrafish genome through largescale profiling of H3K4me1 and H3K4me3 binding sites. Dev Biol 2011; 357:450-462.
20. Bi Y, Lv Z, Wang Y, Hai T, Huo R, Zhou Z, Zhou Q, Sha J. WDR82, a key epigenetics-related factor, plays a crucial role in normal early embryonic development in mice. Biol Reprod 2011; 84:756-764.
21. Dahl JA, Reiner AH, Klungland A, Wakayama T, Collas P. Histone H3 lysine 27 methylation asymmetry on developmentally-regulated promoters distinguish the first two lineages in mouse preimplantation embryos. PLoS One 2010; 5:e9150.
22. Gao Y, Hyttel P, Hall VJ. Regulation of H3K27me3 and H3K4me3 during early porcine embryonic development. Mol Reprod Dev 2010; 77: 540-549.
23. Gao Y, Hyttel P, Hall VJ. Dynamic changes in epigenetic marks and gene expression during porcine epiblast specification. Cell Reprogram 2011; 13:345-360.
24. Gan Q, Yoshida T, McDonald OG, Owens GK. Concise review: epigenetic mechanisms contribute to pluripotency and cell lineage determination of embryonic stem cells. Stem Cells 2007; 25:2-9.
25. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, Jaenisch R, Wagschal A, et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 2006; 125:315-326.
26. Azuara V, Perry P, Sauer S, Spivakov M, Jorgensen HF, John RM, Gouti M, Casanova M, Warnes G, Merkenschlager M, Fisher AG. Chromatin signatures of pluripotent cell lines. Nat Cell Biol 2006; 8:532-538.
27. Stock JK, Giadrossi S, Casanova M, Brookes E, Vidal M, Koseki H, Brockdorff N, Fisher AG, Pombo A. Ring1-mediated ubiquitination of H2A restrains poised RNA polymerase II at bivalent genes in mouse ES cells. Nat Cell Biol 2007; 9:1428-1435.
28. Dey BK, Stalker L, Schnerch A, Bhatia M, Taylor-Papidimitriou J, Wynder C. The histone demethylase KDM5b/JARID1b plays a role in cell fate decisions by blocking terminal differentiation. Mol Cell Biol 2008; 28:5312-5327.
29. Zhang Y, Yang H, Guo X, Rong N, Song Y, Xu Y, Lan W, Zhang X, Liu M, Xu Y, Cao C. The PHD1 finger of KDM5B recognizes unmodified H3K4 during the demethylation of histone H3K4me2/3 by KDM5B. Protein Cell 2014; 5:837-850.
30. Christensen J, Agger K, Cloos PA, Pasini D, Rose S, Sennels L, Rappsilber J, Hansen KH, Salcini AE, Helin K. RBP2 belongs to a family of demethylases, specific for tri-and dimethylated lysine 4 on histone 3. Cell 2007; 128:1063-1076.
31. Yamane K, Tateishi K, Klose RJ, Fang J, Fabrizio LA, Erdjument-Bromage H, Taylor-Papadimitriou J, Tempst P, Zhang Y. PLU-1 is an H3K4 demethylase involved in transcriptional repression and breast cancer cell proliferation. Mol Cell 2007; 25:801-812.
32. Roesch A, Vultur A, Bogeski I, Wang H, Zimmermann KM, Speicher D, Korbel C, Laschke MW, Gimotty PA, Philipp SE, Krause E, Patzold S, et al. Overcoming intrinsic multidrug resistance in melanoma by blocking the mitochondrial respiratory chain of slow-cycling JARID1B(high) cells. Cancer Cell 2013; 23:811-825.
33. Barrett A, Madsen B, Copier J, Lu PJ, Cooper L, Scibetta AG, Burchell J, Taylor-Papadimitriou J. PLU-1 nuclear protein, which is upregulated in breast cancer, shows restricted expression in normal human adult tissues: a new cancer/testis antigen? Int J Cancer 2002; 101:581-588.
34. Lu PJ, Sundquist K, Baeckstrom D, Poulsom R, Hanby A, Meier-Ewert S, Jones T, Mitchell M, Pitha-Rowe P, Freemont P, Taylor-Papadimitriou J. A novel gene (PLU-1) containing highly conserved putative DNA/chromatin binding motifs is specifically up-regulated in breast cancer. J Biol Chem 1999; 274:15633-15645.
35. + breast cancer cells. Int J Oncol 2011; 38:1267-1277.
36. Kidder BL, Hu G, Yu ZX, Liu C, Zhao K. Extended self-renewal and accelerated reprogramming in the absence of Kdm5b. Mol Cell Biol 2013; 33:4793-4810.
37. Zou MR, Cao J, Liu Z, Huh SJ, Polyak K, Yan Q. Histone demethylase jumonji AT-rich interactive domain 1B (JARID1B) controls mammary gland development by regulating key developmental and lineage specification genes. J Biol Chem 2014; 289:17620-17633.
38. Yoshioka K, Suzuki C, Tanaka A, Anas IM, Iwamura S. Birth of piglets derived from porcine zygotes cultured in a chemically defined medium. Biol Reprod 2002; 66:112-119.
39. Lai L, Prather RS. A method for producing cloned pigs by using somatic cells as donors. Methods Mol Biol 2004; 254:149-164.
40. Zhang D, Ma W, Li YH, Hou Y, Li SW, Meng XQ, Sun XF, Sun QY, Wang WH. Intra-oocyte localization of MAD2 and its relationship with kinetochores, microtubules, and chromosomes in rat oocytes during meiosis. Biol Reprod 2004; 71:740-748.
41. Rasmussen PB, Staller P. The KDM5 family of histone demethylases as targets in oncology drug discovery. Epigenomics 2014; 6:277-286.
42. Benevolenskaya EV. Histone H3K4 demethylases are essential in development and differentiation. Biochem Cell Biol 2007; 85:435-443.
43. Zou MR, Cao J, Liu Z, Huh SJ, Polyak K, Yan Q. Histone demethylase jumonji AT-rich interactive domain 1B (JARID1B) controls mammary gland development by regulating key developmental and lineage specification genes. J Biol Chem 2014; 289:17620-17633.
44. Shi Y, Lan F, Matson C, Mulligan P, Whetstine JR, Cole PA, Casero RA. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 2004; 119:941-953.
45. Li Q, Lian S, Dai Z, Xiang Q, Dai X. BGDB: a database of bivalent genes. Database (Oxford) 2013; 2013:bat057.
46. Agger K, Cloos PA, Christensen J, Pasini D, Rose S, Rappsilber J, Issaeva I, Canaani E, Salcini AE, Helin K. UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature 2007; 449:731-734.
47. Cao R, Wang H, He J, Erdjument-Bromage H, Tempst P, Zhang Y. Role of hPHF1 in H3K27 methylation and Hox gene silencing. Mol Cell Biol 2008; 28:1862-1872.
48. Wu X, Gong Y, Yue J, Qiang B, Yuan J, Peng X. Cooperation between EZH2, NSPc1-mediated histone H2A ubiquitination and Dnmt1 in HOX gene silencing. Nucleic Acids Res 2008; 36:3590-3599.
49. Yu BD, Hess JL, Horning SE, Brown GA, Korsmeyer SJ. Altered Hox expression and segmental identity in Mll-mutant mice. Nature 1995; 378: 505-508.
50. Hong S, Cho YW, Yu LR, Yu H, Veenstra TD, Ge K. Identification of JmjC domain-containing UTX and JMJD3 as histone H3 lysine 27 demethylases. Proc Natl Acad Sci U S A 2007; 104:18439-18444.
51. Swigut T, Wysocka J. H3K27 demethylases, at long last. Cell 2007; 131: 29-32.
52. Lee MG, Villa R, Trojer P, Norman J, Yan KP, Reinberg D, Di Croce L, Shiekhattar R. Demethylation of H3K27 regulates polycomb recruitment and H2A ubiquitination. Science 2007; 318:447-450.
53. Lan F, Bayliss PE, Rinn JL, Whetstine JR, Wang JK, Chen S, Iwase S, Alpatov R, Issaeva I, Canaani E, Roberts TM, Chang HY, et al. A histone H3 lysine 27 demethylase regulates animal posterior development. Nature 2007; 449:689-694.
54. Pan G, Tian S, Nie J, Yang C, Ruotti V, Wei H, Jonsdottir GA, Stewart R, Thomson JA. Whole-genome analysis of histone H3 lysine 4 and lysine 27 methylation in human embryonic stem cells. Cell Stem Cell 2007; 1: 299-312.
55. Zhao XD, Han X, Chew JL, Liu J, Chiu KP, Choo A, Orlov YL, Sung WK, Shahab A, Kuznetsov VA, Bourque G, Oh S, et al. Whole-genome mapping of histone H3 Lys4 and 27 trimethylations reveals distinct genomic compartments in human embryonic stem cells. Cell Stem Cell 2007; 1:286-298.
56. Sui X, Price C, Li Z, Chen J. Crosstalk between DNA and histones: Tet's new role in embryonic stem cells. Curr Genomics 2012; 13:603-608.
57. Lee K, Hamm J, Whitworth K, Spate L, Park KW, Murphy CN, Prather RS. Dynamics of TET family expression in porcine preimplantation embryos is related to zygotic genome activation and required for the maintenance of NANOG. Dev Biol 2014; 386:86-95.