Sex affects immunolabeling for histone 3 K27me3 in the trophectoderm of the bovine blastocyst but not labeling for histone 3 K18ac


Autoři: Luciano de R. Carvalheira aff001;  Paula Tríbulo aff001;  Álan M. Borges aff002;  Peter J. Hansen aff001
Působiště autorů: Department of Animal Sciences, D.H. Barron Reproductive and Perinatal Biology Research Program, and Genetics Institute, University of Florida, Gainesville, Florida, United States of America aff001;  Departamento de Clínica e Cirurgia Veterinárias, Escola de Veterinária, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil aff002
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0223570

Souhrn

The mammalian embryo displays sexual dimorphism in the preimplantation period. Moreover, competence of the embryo to develop is dependent on the sire from which the embryo is derived and can be modified by embryokines produced by the endometrium such as colony stimulating factor 2 (CSF2). The preimplantation period is characterized by large changes in epigenetic modifications of DNA and histones. It is possible, therefore, that effects of sex, sire, and embryo regulatory molecules are mediated by changes in epigenetic modifications. Here it was tested whether global levels of two histone modifications in the trophectoderm of the bovine blastocyst were affected by sex, sire, and CSF2. It was found that amounts of immunolabeled H3K27me3 were greater (P = 0.030) for male embryos than female embryos. Additionally, labeling for H3K27me3 and H3K18ac depended upon the bull from which embryos were derived. Although CSF2 reduced the proportion of embryos developing to the blastocyst, there was no effect of CSF2 on labeling for H3K27me3 or H3K18ac. Results indicate that the blastocyst trophoctoderm can be modified epigenetically by embryo sex and paternal inheritance through alterations in histone epigenetic marks.

Klíčová slova:

DNA methylation – Embryos – Epigenetics – Histones – Oocytes – Sperm – Blastocysts – Histone modification


Zdroje

1. Kobayashi S, Isotani A, Mise N, Yamamoto M, Fujihara Y, Kaseda K, Nakanishi T, Ikawa M, Hamada H, Abe K, Okabe M. Comparison of gene expression in male and female mouse blastocysts revealed imprinting of the X-linked gene, Rhox5/Pem, at preimplantation stages. Curr Biol. 2006; 16:166–172. doi: 10.1016/j.cub.2005.11.071 16431368

2. Bermejo-Alvarez P, Rizos D, Rath D, Lonergan P, Gutierrez-Adan A. Sex determines the expression level of one third of the actively expressed genes in bovine blastocysts. Proc Natl Acad Sci USA 2010; 107:3394–3399. https://doi.org/10.1073/pnas.0913843107. 20133684

3. Denicol AC, Leão BC, Dobbs KB, Mingoti GZ, Hansen PJ. Influence of sex on basal and dickkopf-1 regulated gene expression in the bovine morula. PLoS One 2015;10:e0133587. doi: 10.1371/journal.pone.0133587 26196299

4. Lowe R, Gemma C, Rakyan VK, Holland ML. Sexually dimorphic gene expression emerges with embryonic genome activation and is dynamic throughout development. BMC Genomics 2015; 16:295. doi: 10.1186/s12864-015-1506-4 25888192

5. Petropoulos S, Edsgärd D, Reinius B, Deng Q, Panula SP, Codeluppi S, Plaza Reyes A, Linnarsson S, Sandberg R, Lanner F. Single-cell RNA-seq reveals lineage and x chromosome dynamics in human preimplantation embryos. Cell. 2016;165:1012–1026. doi: 10.1016/j.cell.2016.03.023 27062923

6. Heras S, De Coninck DI, Van Poucke M, Goossens K, Bogado Pascottini O, Van Nieuwerburgh F, Deforce D, De Sutter P, Leroy JL, Gutierrez-Adan A, Peelman L, Van Soom A. Suboptimal culture conditions induce more deviations in gene expression in male than female bovine blastocysts. BMC Genomics. 2016;17:72. doi: 10.1186/s12864-016-2393-z 26801242

7. Bermejo-Alvarez P, Rizos D, Rath D, Lonergan P, Gutierrez-Adan A. Epigenetic differences between male and female bovine blastocysts produced in vitro. Physiol Genomics 2008; 32:264–272. doi: 10.1152/physiolgenomics.00234.2007 17986520

8. Gross N, Kropp J, Khatib H. Sexual dimorphism of miRNAs secreted by bovine In vitro-produced embryos. Front Genet 2017;8:39. doi: 10.3389/fgene.2017.00039 28421107

9. Siqueira LG, Hansen PJ. Sex differences in response of the bovine embryo to colony-stimulating factor 2. Reproduction 2016;152:645–654. doi: 10.1530/REP-16-0336 27601717

10. Pérez-Crespo M, Ramírez MA, Fernández-González R, Rizos D, Lonergan P, Pintado B, Gutiérrez-Adán A. Differential sensitivity of male and female mouse embryos to oxidative induced heat-stress is mediated by glucose-6-phosphate dehydrogenase gene expression. Mol Reprod Dev 2005;72:502–10. doi: 10.1002/mrd.20366 16149081

11. Kimura K, Spate LD, Green MP, Roberts RM. Effects of D-glucose concentration, D-fructose, and inhibitors of enzymes of the pentose phosphate pathway on the development and sex ratio of bovine blastocysts. Mol Reprod Dev 2005;72:201–207. doi: 10.1002/mrd.20342 15968626

12. Hansen PJ, Dobbs KB, Denicol AC, Siqueira LGB. Sex and the preimplantation embryo: implications of sexual dimorphism in the preimplantation period for maternal programming of embryonic development. Cell Tissue Res 2016;363:237–247. doi: 10.1007/s00441-015-2287-4 26391275

13. Pérez-Cerezales S, Ramos-Ibeas P, Rizos D, Lonergan P, Bermejo-Alvarez P, Gutiérrez-Adán A. Early sex-dependent differences in response to environmental stress. Reproduction 2018;155:R39–R51. doi: 10.1530/REP-17-0466 29030490

14. Engel N. Sex differences in early embryogenesis: inter-chromosomal regulation sets the stage for sex-biased gene networks: The dialogue between the sex chromosomes and autosomes imposes sexual identity soon after fertilization. Bioessays 2018;40:e1800073. doi: 10.1002/bies.201800073 29943439

15. Dobbs KB, Rodriguez M, Sudano MJ, Ortega MS, Hansen PJ. Dynamics of DNA methylation during early development of the preimplantation bovine embryo. PloS One 2013;8:e66230. doi: 10.1371/journal.pone.0066230 23799080

16. Jiang Z, Lin J, Dong H, Zheng X, Marjani SL, Duan J, Ouyang Z, Chen J, Tian XC. DNA methylomes of bovine gametes and in vivo produced preimplantation embryos. Biol Reprod 2018; 99:949–959. doi: 10.1093/biolre/ioy138 29912291

17. Wu X, Li Y, Xue L, Wang L, Yue Y, Li K, Bou S, Li GP, Yu H. Multiple histone site epigenetic modifications in nuclear transfer and in vitro fertilized bovine embryos. Zygote 2011; 19:31–45. doi: 10.1017/S0967199410000328 20609268

18. Ross PJ, Ragina NP, Rodriguez RM, Iager AE, Siripattarapravat K, Lopez-Corrales N, Cibelli JB. Polycomb gene expression and histone H3 lysine 27 trimethylation changes during bovine preimplantation development. Reproduction 2008;136:777–785. doi: 10.1530/REP-08-0045 18784248

19. Bernstein BE, Meissner A, Lander ES. The mammalian epigenome. Cell 2007;128:669–681. doi: 10.1016/j.cell.2007.01.033 17320505

20. Dobbs KB, Gagné D, Fournier E, Dufort I, Robert C, Block J, Sirard MA, Bonilla L, Ealy AD, Loureiro B, Hansen PJ. Sexual dimorphism in developmental programming of the bovine preimplantation embryo caused by colony-stimulating factor 2. Biol Reprod 2014;91:80. doi: 10.1095/biolreprod.114.121087 25078682

21. Cochran SD, Cole JB, Null DJ, Hansen PJ. Single nucleotide polymorphisms in candidate genes associated with fertilizing ability of sperm and subsequent embryonic development in cattle. Biol Reprod 2013;89:69. doi: 10.1095/biolreprod.113.111260 23904513

22. Kropp J, Carrillo JA, Namous H, Daniels A, Salih SM, Song J, Khatib H. Male fertility status is associated with DNA methylation signatures in sperm and transcriptomic profiles of bovine preimplantation embryos. BMC Genomics 2017;18:280. doi: 10.1186/s12864-017-3673-y 28381255

23. Ortega MS, Wohlgemuth S, Tribulo P, Siqueira LG, Cole JB, Hansen PJ. A single nucleotide polymorphism in COQ9 affects mitochondrial and ovarian function and fertility in Holstein cows. Biol Reprod 2017;96:652–663. doi: 10.1093/biolre/iox004 28339599

24. Canovas S, Cibelli JB, Ross PJ. Jumonji domain-containing protein 3 regulates histone 3 lysine 27 methylation during bovine preimplantation development. Proc Natl Acad Sci USA 2012;109:2400–2405. doi: 10.1073/pnas.1119112109 22308433

25. Liu X, Wang C, Liu W, Li J, Li C, Kou X, Chen J, Zhao Y, Gao H, Wang H, Zhang Y, Gao Y, Gao S. Distinct features of H3K4me3 and H3K27me3 chromatin domains in pre-implantation embryos. Nature 2016;537):558–562. doi: 10.1038/nature19362 27626379

26. Oliveira CS, Saraiva NZ, de Souza MM, Tetzner TA, de Lima MR, Garcia JM. Effects of histone hyperacetylation on the preimplantation development of male and female bovine embryos. Reprod Fertil Dev 2010;22:1041–1048. doi: 10.1071/RD09238 20591338

27. Sandhu A, Mohapatra SK, Agrawal H, Singh MK, Palta P, Singla SK, Chauhan MS, Manik RS. Effect of sex of embryo on developmental competence, epigenetic status, and gene expression in buffalo (Bubalus bubalis) embryos produced by hand-made cloning. Cell Reprogram 2016;18:356–365. doi: 10.1089/cell.2015.0077 27696910

28. Ortega MS, Moraes JGN, Patterson DJ, Smith MF, Behura SK, Poock S, Spencer TE. Influences of sire conception rate on pregnancy establishment in dairy cattle. Biol Reprod 2018; 99:1244–1254. doi: 10.1093/biolre/ioy141 29931362

29. Driver AM, Huang W, Gajic S, Monson RL, Rosa GJ, Khatib H. Short communication: Effects of the progesterone receptor variants on fertility traits in cattle. J Dairy Sci 2009;92:4082–4085. doi: 10.3168/jds.2009-2013 19620692

30. Khatib H, Huang W, Mikheil D, Schutzkus V, Monson RL. Effects of signal transducer and activator of transcription (STAT) genes STAT1 and STAT3 genotypic combinations on fertilization and embryonic survival rates in Holstein cattle. J Dairy Sci 2009;92:6186–6191. doi: 10.3168/jds.2009-2439 19923622

31. Kutchy NA, Menezes ESB, Chiappetta A, Tan W, Wills RW, Kaya A, Topper E, Moura AA, Perkins AD, Memili E. Acetylation and methylation of sperm histone 3 lysine 27 (H3K27ac and H3K27me3) are associated with bull fertility. Andrologia 2018;50.e12915. doi: 10.1111/and.12915 29057498

32. Shojaei Saadi HA, Fournier É, Vigneault C, Blondin P, Bailey J, Robert C. Genome-wide analysis of sperm DNA methylation from monozygotic twin bulls. Reprod Fertil Dev 2017;29:838–843. doi: 10.1071/RD15384 26751019

33. McLay DW, Clarke HJ.Remodelling the paternal chromatin at fertilization in mammals. Reproduction 2003; 125:625–633; http://dx.doi.org/10.1530/rep.0.1250625; 12713425

34. Norman HD, Hutchison JL, Miller RH. Use of sexed semen and its effect on conception rate, calf sex, dystocia, and stillbirth of Holsteins in the United States. J Dairy Sci 2010; 93:3880–3890. doi: 10.3168/jds.2009-2781 20655457

35. Siqueira LG, Tribulo P, Chen Z, Denicol AC, Ortega MS, Negrón-Pérez VM, Kannampuzha-Francis J, Pohler KG, Rivera RM, Hansen PJ. Colony-stimulating factor 2 acts from days 5 to 7 of development to modify programming of the bovine conceptus at day 86 of gestation. Biol Reprod 2017;96:743–757. doi: 10.1093/biolre/iox018 28379294

36. Ozawa M, Sakatani M, Dobbs KB, Kannampuzha-Francis J, Hansen PJ. Regulation of gene expression in the bovine blastocyst by colony stimulating factor 2. BMC Res Notes. 2016;9:250. doi: 10.1186/s13104-016-2038-y 27130208

37. Dobbs KB, Khan FA, Sakatani M, Moss JI, Ozawa M, Ealy AD, Hansen PJ. Regulation of pluripotency of inner cell mass and growth and differentiation of trophectoderm of the bovine embryo by colony stimulating factor 2. Biol Reprod 2013;89:141. doi: 10.1095/biolreprod.113.113183 24198123

38. Loureiro B, Oliveira LJ, Favoreto MG, Hansen P J Colony-stimulating factor 2 inhibits induction of apoptosis in the bovine preimplantation embryo. Am J Reprod Immunol 2011;, 65: 578–588. doi: 10.1111/j.1600-0897.2010.00953.x 21223422


Článek vyšel v časopise

PLOS One


2019 Číslo 10

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…


Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Léčba bolesti v ordinaci praktického lékaře
nový kurz
Autoři: MUDr. PhDr. Zdeňka Nováková, Ph.D.

Revmatoidní artritida: včas a k cíli
Autoři: MUDr. Heřman Mann

Jistoty a nástrahy antikoagulační léčby aneb kardiolog - neurolog - farmakolog - nefrolog - právník diskutují
Autoři: doc. MUDr. Štěpán Havránek, Ph.D., prof. MUDr. Roman Herzig, Ph.D., doc. MUDr. Karel Urbánek, Ph.D., prim. MUDr. Jan Vachek, MUDr. et Mgr. Jolana Těšínová, Ph.D.

Léčba akutní pooperační bolesti
Autoři: doc. MUDr. Jiří Málek, CSc.

Nové antipsychotikum kariprazin v léčbě schizofrenie
Autoři: prof. MUDr. Cyril Höschl, DrSc., FRCPsych.

Všechny kurzy
Kurzy Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Nemáte účet?  Registrujte se

Zapomenuté heslo

Zadejte e-mailovou adresu se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se