Allele-specific enhancer interaction at the Peg3 imprinted domain


Autoři: Joomyeong Kim aff001;  Wesley D. Frey aff001;  Kaustubh Sharma aff001;  Subash Ghimire aff001;  Ryoichi Teruyama aff001;  Lisa Stubbs aff002
Působiště autorů: Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana, United States of America aff001;  Cell and Developmental Biology, Institute for Genomic Biology, University of Illinois, Urbana, Illinois, United States of America aff002
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0224287

Souhrn

The parental allele specificity of mammalian imprinted genes has been evolutionarily well conserved, although its functional constraints and associated mechanisms are not fully understood. In the current study, we generated a mouse mutant with switched active alleles driving the switch from paternal-to-maternal expression for Peg3 and the maternal-to-paternal expression for Zim1. The expression levels of Peg3 and Zim1, but not the spatial expression patterns, within the brain showed clear differences between wild type and mutant animals. We identified putative enhancers localized upstream of Peg3 that displayed allele-biased DNA methylation, and that also participate in allele-biased chromosomal conformations with regional promoters. Most importantly, these data suggest for the first time that long-distance enhancers may contribute to allelic expression within imprinted domains through allele-biased interactions with regional promoters.

Klíčová slova:

DNA isolation – DNA methylation – Genomic imprinting – Hypothalamus – Immunostaining – Mammalian genomics – Polymerase chain reaction – BAC cloning


Zdroje

1. Bartolomei MS, Ferguson-Smith AC. Mammalian genomic imprinting. Cold Spring Harb Perspect Biol. 2011;3(7).

2. Barlow DP, Bartolomei MS. Genomic imprinting in mammals. Cold Spring Harb Perspect Biol. 2014;6(2).

3. Renfree MB, Suzuki S, Kaneko-Ishino T. The origin and evolution of genomic imprinting and viviparity in mammals. Philos Trans R Soc Lond B Biol Sci. 2013;368:20120151. doi: 10.1098/rstb.2012.0151 23166401

4. Keverne EB. Importance of the matriline for genomic imprinting, brain development and behaviour. Philos Trans R Soc Lond B Biol Sci. 2013;368:20110327. doi: 10.1098/rstb.2011.0327 23166391

5. Ivanova E, Kelsey G. Imprinted genes and hypothalamic function. J Mol Endocrinol. 2011;47:R67–74. doi: 10.1530/JME-11-0065 21798993

6. Feil R, Berger F. Convergent evolution of genomic imprinting in plants and mammals. Trends Genet. 2007;23:192–199. doi: 10.1016/j.tig.2007.02.004 17316885

7. Kuroiwa Y, Kaneko-Ishino T, Kagitani F, Kohda T, Li LL, Tada M et al. Peg3 imprinted gene on proximal chromosome 7 encodes for a zinc finger protein. Nat Genet. 1996;12:186–190. doi: 10.1038/ng0296-186 8563758

8. Relaix F, Weng X, Marazzi G, Yang E, Copeland N, Jenkins N et al. Pw1, A novel zinc finger gene implicated in the myogenic and neuronal lineages. Dev Biol. 1996;77:383–396.

9. Kim J, Ashworth L, Branscomb E, Stubbs L. The human homolog of a mouse-imprinted gene, Peg3, maps to a zinc finger gene-rich region of human chromosome 19q13.4. Genome Res. 1997;7:532–540. doi: 10.1101/gr.7.5.532 9149948

10. He H, Kim J. Regulation and function of the Peg3 imprinted domain. Genomic and Informatics. 2014;12:105–113.

11. Kim J, Ekram MB, Kim H, Faisal M, Frey WD et al. Imprinting control region (ICR) of the Peg3 domain. Hum Mol Genet. 2012;21:2677–2687. doi: 10.1093/hmg/dds092 22394678

12. He H, Perera BP, Ye A, Kim J. Parental and sexual conflicts over the Peg3 imprinted domain. Sci Rep. 2016;6:38136. doi: 10.1038/srep38136 27901122

13. Perera BP, Kim J. Alternative promoters of Peg3 with maternal specificity. Sci Rep. 2016;6:24438. doi: 10.1038/srep24438 27075691

14. Bretz CL, Kim J. Transcription-driven DNA methylation setting on the mouse Peg3 locus. Epigenetics. 2017;12:945–952. doi: 10.1080/15592294.2017.1377869 28925797

15. Thiaville MM, Kim H, Frey WD, Kim J. Identification of an evolutionarily conserved cis-regulatory element controlling the Peg3 imprinted domain. PLoS One. 2013;8:e75417. doi: 10.1371/journal.pone.0075417 24040411

16. Kim J, Ye A. Phylogenetic and Epigenetic Footprinting of the Putative Enhancers of the Peg3 Domain. PLoS One. 2016;11:e0154216. doi: 10.1371/journal.pone.0154216 27104590

17. Bakshi A, Bretz CL, Cain TL, Kim J. Intergenic DNA hypomethylated regions as putative regulators of imprinted domains. Epigenomics. 2018;10:445–461. doi: 10.2217/epi-2017-0125 29569934

18. Bretz CL, Frey WD, Teruyama R, Kim J. Allele and dosage specificity of the Peg3 imprinted domain. PLoS One. 2018;13:e0197069. doi: 10.1371/journal.pone.0197069 29734399

19. Li L, Keverne EB, Aparicio SA, Ishino F, Barton SC, Tada M et al. Regulation of maternal behavior and offspring growth by paternally expressed Peg3. Science. 1999;284:330–333. doi: 10.1126/science.284.5412.330 10195900

20. Curley JP, Pinnock SB, Dickson SL, Thresher R, Miyoshi N, Surani MA et al. Increased body fat in mice with a targeted mutation of the paternally expressed imprinted gene Peg3. FASEB J. 2005;19:1302–1304 doi: 10.1096/fj.04-3216fje 15928196

21. Kim J, Frey WD, He H, Kim H, Ekram MB, Bakshi A et al. Peg3 mutational effects on reproduction and placenta-specific gene families. PLoS One. 2013;8:e83359. doi: 10.1371/journal.pone.0083359 24391757

22. Frey WD, Kim J. Tissue-Specific Contributions of Paternally Expressed Gene 3 in Lactation and Maternal Care of Mus musculus. PLoS One. 2015;10:e0144459. doi: 10.1371/journal.pone.0144459 26640945

23. Kim J, Lu X, Stubbs L, Zim1, a maternally expressed mouse Kruppel-type zinc-finger gene located in proximal chromosome 7. Hum Mol Genet. 1999;8:847–854. doi: 10.1093/hmg/8.5.847 10196374

24. Perera BP, Teruyama R. Kim J. Yy1 gene dosage effect and bi-allelic expression of Peg3. PLoS One. 2015;10:e0119493. doi: 10.1371/journal.pone.0119493 25774914

25. Clark SJ, Harrison J, Paul CL, Frommer M. High sensitivity mapping of methylated cytosines. Nucleic Acids Res. 1994;22:2990–2997. doi: 10.1093/nar/22.15.2990 8065911

26. Xiong Z, Laird PW. COBRA: a sensitive and quantitative DNA methylation assay. Nucleic Acids Res. 1997;25:2532–2534. doi: 10.1093/nar/25.12.2532 9171110

27. Dekker J. The three ‘C’s of chromosome conformation capture: controls, controls, control. Nat Methods. 2006;3:17–21. doi: 10.1038/nmeth823 16369547

28. Miele A, Gheldof N, Tabuchi TM, Dostie J, Dekker J. Mapping chromatin interactions by chromosome conformation capture. Curr Protoc Mol Biol. 2006;Chapter 21:Unit 21.11. doi: 10.1002/0471142727.mb2111s74 18265379

29. Xu J, Carter AC, Gendrel AV, Attia M, Loftus J, Greenleaf WJ, Tibshirani R, Heard E, Chang HY. Landscape of monoallelic DNA accessibility in mouse embryonic stem cells and neural progenitor cells. Nat Genet. 2017;49:377–386. doi: 10.1038/ng.3769 28112738

30. Chess A. Monoallelic Gene Expression in Mammals. Annu Rev Genet. 2016;50:317–327. doi: 10.1146/annurev-genet-120215-035120 27893959

31. Zwemer LM, Zak A, Thompson BR, Kirby A, Daly MJ, Chess A, Gimelbrant AA. Autosomal monoallelic expression in the mouse. Genome Biol. 2012;13:R10. doi: 10.1186/gb-2012-13-2-r10 22348269

32. Winer J, Jung CK, Shackel I, Williams PM. Development and validation of real-time quantitative reverse transcriptase–polymerase chain reaction for monitoring gene expression in cardiac myocytes in vitro. Anal Biochem. 1999;270:41–49. doi: 10.1006/abio.1999.4085 10328763


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2019 Číslo 10