Chromatin States in Mouse Sperm Correlate with Embryonic and Adult Regulatory Landscapes

Cell Reports

Volumn 18, Issue 6, 2017, Pages 1366-1382

  Jung, Yoon Hee ^a   Sauria, Michael E G ^b   Lyu, Xiaowen ^a   Cheema, Manjinder S ^d   Ausio, Juan ^d   Taylor, James ^b,c   Corces, Victor G ^a  

^a EMORY UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Johns Hopkins University   (United States)

^d UNIVERSITY OF VICTORIA   (Canada)

Author keywords

chromatin; CTCF; pluripotency; stem cell; TAD; transcription

Indexed keywords

COHESIN; TRANSCRIPTION FACTOR CTCF; CELL CYCLE PROTEIN; NONHISTONE PROTEIN; PROTEIN BINDING;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COMPARTMENTALIZATION; CHROMATIN STRUCTURE; EMBRYO; EMBRYONIC STEM CELL; HISTONE MODIFICATION; MOUSE; NONHUMAN; NUCLEOSOME; PROMOTER REGION; PROTEIN FOLDING; SPERM; SPERMATID; ANIMAL; BINDING SITE; CHROMATIN; GENETICS; GENOME; GERM CELL; MALE; METABOLISM; SPERMATOZOON;

ANIMALS; BINDING SITES; CELL CYCLE PROTEINS; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; EMBRYONIC STEM CELLS; GENOME; GERM CELLS; MALE; MICE; NUCLEOSOMES; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; SPERMATIDS; SPERMATOZOA;

EID: 85011854047     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2017.01.034     Document Type: Article

References (38)

1. Balhorn, R., Gledhill, B.L., Wyrobek, A.J., Mouse sperm chromatin proteins: quantitative isolation and partial characterization. Biochemistry 16 (1977), 4074–4080.
2. Bannister, A.J., Schneider, R., Myers, F.A., Thorne, A.W., Crane-Robinson, C., Kouzarides, T., Spatial distribution of di- and tri-methyl lysine 36 of histone H3 at active genes. J. Biol. Chem. 280 (2005), 17732–17736.
3. Battulin, N., Fishman, V.S., Mazur, A.M., Pomaznoy, M., Khabarova, A.A., Afonnikov, D.A., Prokhortchouk, E.B., Serov, O.L., Comparison of the three-dimensional organization of sperm and fibroblast genomes using the Hi-C approach. Genome Biol., 16, 2015, 77.
4. Bošković, A., Bender, A., Gall, L., Ziegler-Birling, C., Beaujean, N., Torres-Padilla, M.E., Analysis of active chromatin modifications in early mammalian embryos reveals uncoupling of H2A.Z acetylation and H3K36 trimethylation from embryonic genome activation. Epigenetics 7 (2012), 747–757.
5. Brykczynska, U., Hisano, M., Erkek, S., Ramos, L., Oakeley, E.J., Roloff, T.C., Beisel, C., Schübeler, D., Stadler, M.B., Peters, A.H., Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa. Nat. Struct. Mol. Biol. 17 (2010), 679–687.
6. Carone, B.R., Hung, J.H., Hainer, S.J., Chou, M.T., Carone, D.M., Weng, Z., Fazzio, T.G., Rando, O.J., High-resolution mapping of chromatin packaging in mouse embryonic stem cells and sperm. Dev. Cell 30 (2014), 11–22.
7. Chen, K., Xi, Y., Pan, X., Li, Z., Kaestner, K., Tyler, J., Dent, S., He, X., Li, W., DANPOS: dynamic analysis of nucleosome position and occupancy by sequencing. Genome Res. 23 (2013), 341–351.
8. Corces, M.R., Buenrostro, J.D., Wu, B., Greenside, P.G., Chan, S.M., Koenig, J.L., Snyder, M.P., Pritchard, J.K., Kundaje, A., Greenleaf, W.J., et al. Lineage-specific and single-cell chromatin accessibility charts human hematopoiesis and leukemia evolution. Nat. Genet. 48 (2016), 1193–1203.
9. Darrow, E.M., Huntley, M.H., Dudchenko, O., Stamenova, E.K., Durand, N.C., Sun, Z., Huang, S.C., Sanborn, A.L., Machol, I., Shamim, M., et al. Deletion of DXZ4 on the human inactive X chromosome alters higher-order genome architecture. Proc. Natl. Acad. Sci. USA 113 (2016), E4504–E4512.
10. Dowen, J.M., Fan, Z.P., Hnisz, D., Ren, G., Abraham, B.J., Zhang, L.N., Weintraub, A.S., Schuijers, J., Lee, T.I., Zhao, K., Young, R.A., Control of cell identity genes occurs in insulated neighborhoods in mammalian chromosomes. Cell 159 (2014), 374–387.
11. Erkek, S., Hisano, M., Liang, C.Y., Gill, M., Murr, R., Dieker, J., Schübeler, D., van der Vlag, J., Stadler, M.B., Peters, A.H., Molecular determinants of nucleosome retention at CpG-rich sequences in mouse spermatozoa. Nat. Struct. Mol. Biol. 20 (2013), 868–875.
12. Grunewald, S., Paasch, U., Glander, H.J., Anderegg, U., Mature human spermatozoa do not transcribe novel RNA. Andrologia 37 (2005), 69–71.
13. Guo, Y., Xu, Q., Canzio, D., Shou, J., Li, J., Gorkin, D.U., Jung, I., Wu, H., Zhai, Y., Tang, Y., et al. CRISPR inversion of CTCF sites alters genome topology and enhancer/promoter function. Cell 162 (2015), 900–910.
14. Hackett, J.A., Surani, M.A., Beyond DNA: programming and inheritance of parental methylomes. Cell 153 (2013), 737–739.
15. Hammoud, S.S., Nix, D.A., Zhang, H., Purwar, J., Carrell, D.T., Cairns, B.R., Distinctive chromatin in human sperm packages genes for embryo development. Nature 460 (2009), 473–478.
16. Hammoud, S.S., Low, D.H.P., Yi, C., Carrell, D.T., Guccione, E., Cairns, B.R., Chromatin and transcription transitions of mammalian adult germline stem cells and spermatogenesis. Cell Stem Cell 15 (2014), 239–253.
17. Heard, E., Martienssen, R.A., Transgenerational epigenetic inheritance: myths and mechanisms. Cell 157 (2014), 95–109.
18. Henikoff, S., Greally, J.M., Epigenetics, cellular memory and gene regulation. Curr. Biol. 26 (2016), R644–R648.
19. Kagey, M.H., Newman, J.J., Bilodeau, S., Zhan, Y., Orlando, D.A., van Berkum, N.L., Ebmeier, C.C., Goossens, J., Rahl, P.B., Levine, S.S., et al. Mediator and cohesin connect gene expression and chromatin architecture. Nature 467 (2010), 430–435.
20. Lieberman-Aiden, E., van Berkum, N.L., Williams, L., Imakaev, M., Ragoczy, T., Telling, A., Amit, I., Lajoie, B.R., Sabo, P.J., Dorschner, M.O., et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326 (2009), 289–293.
21. Lim, J.P., Brunet, A., Bridging the transgenerational gap with epigenetic memory. Trends Genet. 29 (2013), 176–186.
22. Liu, T., Use model-based analysis of ChIP-Seq (MACS) to analyze short reads generated by sequencing protein-DNA interactions in embryonic stem cells. Methods Mol. Biol. 1150 (2014), 81–95.
23. Maza, I., Caspi, I., Zviran, A., Chomsky, E., Rais, Y., Viukov, S., Geula, S., Buenrostro, J.D., Weinberger, L., Krupalnik, V., et al. Transient acquisition of pluripotency during somatic cell transdifferentiation with iPSC reprogramming factors. Nat. Biotechnol. 33 (2015), 769–774.
24. Mikkelsen, T.S., Ku, M., Jaffe, D.B., Issac, B., Lieberman, E., Giannoukos, G., Alvarez, P., Brockman, W., Kim, T.K., Koche, R.P., et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448 (2007), 553–560.
25. Nitzsche, A., Paszkowski-Rogacz, M., Matarese, F., Janssen-Megens, E.M., Hubner, N.C., Schulz, H., de Vries, I., Ding, L., Huebner, N., Mann, M., et al. RAD21 cooperates with pluripotency transcription factors in the maintenance of embryonic stem cell identity. PLoS One, 6, 2011, e19470.
26. Oakberg, E.F., Duration of spermatogenesis in the mouse. Nature 180 (1957), 1137–1138.
27. Ong, C.T., Corces, V.G., CTCF: an architectural protein bridging genome topology and function. Nat. Rev. Genet. 15 (2014), 234–246.
28. Pugacheva, E.M., Rivero-Hinojosa, S., Espinoza, C.A., Méndez-Catalá, C.F., Kang, S., Suzuki, T., Kosaka-Suzuki, N., Robinson, S., Nagarajan, V., Ye, Z., et al. Comparative analyses of CTCF and BORIS occupancies uncover two distinct classes of CTCF binding genomic regions. Genome Biol., 16, 2015, 161.
29. Rando, O.J., Intergenerational transfer of epigenetic information in sperm. Cold Spring Harb. Perspect. Med., 6, 2016, a022988.
30. Rao, S.S., Huntley, M.H., Durand, N.C., Stamenova, E.K., Bochkov, I.D., Robinson, J.T., Sanborn, A.L., Machol, I., Omer, A.D., Lander, E.S., Aiden, E.L., A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159 (2014), 1665–1680.
31. Samans, B., Yang, Y., Krebs, S., Sarode, G.V., Blum, H., Reichenbach, M., Wolf, E., Steger, K., Dansranjavin, T., Schagdarsurengin, U., Uniformity of nucleosome preservation pattern in mammalian sperm and its connection to repetitive DNA elements. Dev. Cell 30 (2014), 23–35.
32. Schep, A.N., Buenrostro, J.D., Denny, S.K., Schwartz, K., Sherlock, G., Greenleaf, W.J., Structured nucleosome fingerprints enable high-resolution mapping of chromatin architecture within regulatory regions. Genome Res. 25 (2015), 1757–1770.
33. Selvaraj, S., R Dixon, J., Bansal, V., Ren, B., Whole-genome haplotype reconstruction using proximity-ligation and shotgun sequencing. Nat. Biotechnol. 31 (2013), 1111–1118.
34. Sharma, U., Conine, C.C., Shea, J.M., Boskovic, A., Derr, A.G., Bing, X.Y., Belleannee, C., Kucukural, A., Serra, R.W., Sun, F., et al. Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals. Science 351 (2016), 391–396.
35. Shen, Y., Yue, F., McCleary, D.F., Ye, Z., Edsall, L., Kuan, S., Wagner, U., Dixon, J., Lee, L., Lobanenkov, V.V., Ren, B., A map of the cis-regulatory sequences in the mouse genome. Nature 488 (2012), 116–120.
36. Soumillon, M., Necsulea, A., Weier, M., Brawand, D., Zhang, X., Gu, H., Barthès, P., Kokkinaki, M., Nef, S., Gnirke, A., et al. Cellular source and mechanisms of high transcriptome complexity in the mammalian testis. Cell Rep. 3 (2013), 2179–2190.
37. Van Holde, K.E., Chromatin. 1989, Springer.
38. Whyte, W.A., Orlando, D.A., Hnisz, D., Abraham, B.J., Lin, C.Y., Kagey, M.H., Rahl, P.B., Lee, T.I., Young, R.A., Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell 153 (2013), 307–319.