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The RPMI-1640 vitamin mixture promotes bovine blastocyst development in vitro and downregulates gene expression of TXNIP with epigenetic modification of associated histones

Part of: Advancing the DOHaD Agenda in Africa

Published online by Cambridge University Press:  02 August 2017

S. Ikeda ,
M. Sugimoto  and
S. Kume
S. Ikeda*
Affiliation:
Laboratory of Animal Physiology and Functional Anatomy, Graduate School of Agriculture, Kyoto University, Kyoto, Japan
M. Sugimoto
Affiliation:
Laboratory of Animal Physiology and Functional Anatomy, Graduate School of Agriculture, Kyoto University, Kyoto, Japan
S. Kume
Affiliation:
Laboratory of Animal Physiology and Functional Anatomy, Graduate School of Agriculture, Kyoto University, Kyoto, Japan
*
*Address for correspondence: S. Ikeda, PhD, Laboratory of Animal Physiology and Functional Anatomy, Graduate School of Agriculture, Kyoto University, Kyoto 606-8502, Japan. (Email ikedash@kais.kyoto-u.ac.jp)
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Abstract

Diverse environmental conditions surrounding preimplantation embryos, including available nutrients, affect their metabolism and development in both short- and long-term manner. Thioredoxin-interacting protein (TXNIP) is a possible marker for preimplantation stress that is implicated in in vitro fertilization- (IVF) induced long-term DOHaD effects. B vitamins, as participants in one-carbon metabolism, may affect preimplantation embryos by epigenetic alterations of metabolically and developmentally important genes. In vitro-produced bovine embryos were cultured with or without Roswell Park Memorial Institute 1640 vitamin mixture, containing B vitamins and B vitamin-like substances, from day 3 after IVF and we evaluated blastocyst development and TXNIP messenger RNA (mRNA) expression in the blastocysts by reverse transcription-quantitative polymerase chain reaction. The degree of trimethylation of histone H3 lysine 27 (H3K27me3) at TXNIP promoter was examined semi-quantitatively by chromatin immunoprecipitation polymerase chain reaction. Total H3K27me3 were also compared between the groups by Western blot analysis. The vitamin treatment significantly increased the rates of blastocyst development (P<0.05) and their hatching (P<0.001) from the zona pellucida by day 8. The mRNA expression of TXNIP was lower (P<0.01) in blastocysts in the vitamin-mixture-treated group concomitant with higher (P<0.05) level of H3K27me3 of its promoter compared with the control group. The total H3K27me3 in the vitamin-mixture-treated group was also higher (P<0.01) than that in the control group. The epigenetic control of genes related to important metabolic processes during the periconceptional period by nutritional conditions in utero and/or in vitro may have possible implication for the developmental programming during this period that may impact the welfare and production traits of farm animals.

Keywords

B vitaminblastocystepigeneticsprogrammingTXNIP
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 9 , Issue 1: Themed Issue: DOHaD AFRICA , February 2018 , pp. 87 - 94
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Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2017 

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References

1. Sun, C, Velazquez, MA, Fleming, TP. DOHaD and the periconceptional period, a critical window in time. In The Epigenome and Developmental Origins of Health and Disease (ed. Rosenfeld CS), 2015; pp 33–47. Academic Press: Cambridge.Google Scholar
2. Cantone, I, Fisher, AG. Epigenetic programming and reprogramming during development. Nat Struct Mol Biol. 2013; 20, 282–289.CrossRefGoogle ScholarPubMed
3. Hatanaka, Y, Inoue, K, Oikawa, M, et al. Histone chaperone CAF-1 mediates repressive histone modifications to protect preimplantation mouse embryos from endogenous retrotransposons. Proc Natl Acad Sci USA. 2015; 112, 14641–14646.CrossRefGoogle ScholarPubMed
4. Nishiyama, A, Matsui, M, Iwata, S, et al. Identification of thioredoxin-binding protein-2/vitamin D(3) up-regulated protein 1 as a negative regulator of thioredoxin function and expression. J Biol Chem. 1999; 274, 21645–21650.CrossRefGoogle ScholarPubMed
5. Chong, CR, Chan, WP, Nguyen, TH, et al. Thioredoxin-interacting protein: pathophysiology and emerging pharmacotherapeutics in cardiovascular disease and diabetes. Cardiovasc Drugs Ther. 2014; 28, 347–360.CrossRefGoogle Scholar
6. Spindel, ON, World, C, Berk, BC. Thioredoxin interacting protein: redox dependent and independent regulatory mechanisms. Antioxid Redox Signal. 2012; 16, 587–596.CrossRefGoogle ScholarPubMed
7. Feuer, SK, Liu, X, Donjacour, A, et al. Use of a mouse in vitro fertilization model to understand the developmental origins of health and disease hypothesis. Endocrinology. 2014; 155, 1956–1969.CrossRefGoogle ScholarPubMed
8. Yu, M, Geiger, B, Deeb, N, Rothschild, MF. Investigation of TXNIP (thioredoxin-interacting protein) and TRX (thioredoxin) genes for growth-related traits in pigs. Mamm Genome. 2007; 18, 197–209.CrossRefGoogle ScholarPubMed
9. Toufeer, M, Bonnefont, CM, Foulon, E, et al. Gene expression profiling of dendritic cells reveals important mechanisms associated with predisposition to Staphylococcus infections. PLoS One. 2011; 6, e22147.CrossRefGoogle ScholarPubMed
10. Kerro Dego, O, Oliver, SP, Almeida, RA. Host-pathogen gene expression profiles during infection of primary bovine mammary epithelial cells with Escherichia coli strains associated with acute or persistent bovine mastitis. Vet Microbiol. 2012; 155, 291–297.CrossRefGoogle ScholarPubMed
11. Ikeda, S, Sugimoto, M, Kume, S. Importance of methionine metabolism in morula-to-blastocyst transition in bovine preimplantation embryos. J Reprod Dev. 2012; 58, 91–97.CrossRefGoogle ScholarPubMed
12. Ikeda, S, Namekawa, T, Sugimoto, M, Kume, S. Expression of methylation pathway enzymes in bovine oocytes and preimplantation embryos. J Exp Zool A Ecol Genet Physiol. 2010; 313, 129–136.CrossRefGoogle ScholarPubMed
13. Kwong, WY, Adamiak, SJ, Gwynn, A, Singh, R, Sinclair, KD. Endogenous folates and single-carbon metabolism in the ovarian follicle, oocyte and pre-implantation embryo. Reproduction. 2010; 139, 705–715.CrossRefGoogle ScholarPubMed
14. Zhang, B, Denomme, MM, White, CR, et al. Both the folate cycle and betaine-homocysteine methyltransferase contribute methyl groups for DNA methylation in mouse blastocysts. FASEB J. 2015; 29, 1069–1079.CrossRefGoogle ScholarPubMed
15. Shojaei Saadi, HA, Gagne, D, Fournier, E, et al. Responses of bovine early embryos to S-adenosyl methionine supplementation in culture. Epigenomics. 2016; 8, 1039–1060.CrossRefGoogle ScholarPubMed
16. Ducker, GS, Rabinowitz, JD. One-carbon metabolism in health and disease. Cell Metab. 2016; 25, 27–42.CrossRefGoogle ScholarPubMed
17. Mentch, SJ, Locasale, JW. One-carbon metabolism and epigenetics: understanding the specificity. Ann N Y Acad Sci. 2016; 1363, 91–98.CrossRefGoogle ScholarPubMed
18. Xu, J, Sinclair, KD. One-carbon metabolism and epigenetic regulation of embryo development. Reprod Fertil Dev. 2015; 27, 667–676.CrossRefGoogle ScholarPubMed
19. Moore, GE, Gerner, RE, Franklin, HA. Culture of normal human leukocytes. JAMA. 1967; 199, 519–524.CrossRefGoogle ScholarPubMed
20. Takahashi, Y, First, NL. In vitro development of bovine one-cell embryos: influence of glucose, lactate, pyruvate, amino acids and vitamins. Theriogenology. 1992; 37, 963–978.CrossRefGoogle ScholarPubMed
21. Rosenkrans, CF Jr, First, NL. Effect of free amino acids and vitamins on cleavage and developmental rate of bovine zygotes in vitro. J Anim Sci. 1994; 72, 434–437.CrossRefGoogle ScholarPubMed
22. Kudo, M, Ikeda, S, Sugimoto, M, Kume, S. Methionine-dependent histone methylation at developmentally important gene loci in mouse preimplantation embryos. J Nutr Biochem. 2015; 26, 1664–1669.CrossRefGoogle ScholarPubMed
23. Goossens, K, Van Poucke, M, Van Soom, A, et al. Selection of reference genes for quantitative real-time PCR in bovine preimplantation embryos. BMC Dev Biol. 2005; 5, 27.CrossRefGoogle ScholarPubMed
24. Kimura, H. Histone modifications for human epigenome analysis. J Hum Genet. 2013; 58, 439–445.CrossRefGoogle ScholarPubMed
25. Hublitz, P, Albert, M, Peters, AH. Mechanisms of transcriptional repression by histone lysine methylation. Int J Dev Biol. 2009; 53, 335–354.CrossRefGoogle ScholarPubMed
26. Holm, P, Booth, PJ, Schmidt, MH, Greve, T, Callesen, H. High bovine blastocyst development in a static in vitro production system using SOFaa medium supplemented with sodium citrate and myo-inositol with or without serum-proteins. Theriogenology. 1999; 52, 683–700.CrossRefGoogle ScholarPubMed
27. Kane, MT, Bavister, BD. Vitamin requirements for development of eight-cell hamster embryos to hatching blastocysts in vitro. Biol Reprod. 1988; 39, 1137–1143.CrossRefGoogle ScholarPubMed
28. Kane, MT. The effects of water-soluble vitamins on the expansion of rabbit blastocysts in vitro. J Exp Zool. 1988; 245, 220–223.CrossRefGoogle ScholarPubMed
29. Norman, RJ. 2015 RANZCOG Arthur Wilson Memorial Oration ‘From little things, big things grow: the importance of periconception medicine’. Aust N Z J Obstet Gynaecol. 2015; 55, 535–540.CrossRefGoogle Scholar
30. Gluckman, PD, Hanson, MA. Living with the past: evolution, development, and patterns of disease. Science. 2004; 305, 1733–1736.CrossRefGoogle ScholarPubMed
31. Rubio-Ruiz, ME, Peredo-Escarcega, AE, Cano-Martinez, A, Guarner-Lans, V. An evolutionary perspective of nutrition and inflammation as mechanisms of cardiovascular disease. Int J Evol Biol. 2015; 2015, 179791.CrossRefGoogle ScholarPubMed
32. Fernandez-Real, JM, Ricart, W. Insulin resistance and inflammation in an evolutionary perspective: the contribution of cytokine genotype/phenotype to thriftiness. Diabetologia. 1999; 42, 1367–1374.CrossRefGoogle Scholar
33. Shalev, A. Minireview: thioredoxin-interacting protein: regulation and function in the pancreatic beta-cell. Mol Endocrinol. 2014; 28, 1211–1220.CrossRefGoogle ScholarPubMed
34. Pang, YW, Sun, YQ, Sun, WJ, et al. Melatonin inhibits paraquat-induced cell death in bovine preimplantation embryos. J Pineal Res. 2016; 60, 155–166.CrossRefGoogle ScholarPubMed
35. De Marinis, Y, Cai, M, Bompada, P, et al. Epigenetic regulation of the thioredoxin-interacting protein (TXNIP) gene by hyperglycemia in kidney. Kidney Int. 2016; 89, 342–353.CrossRefGoogle ScholarPubMed
36. Friso, S, Udali, S, De Santis, D, Choi, SW. One-carbon metabolism and epigenetics. Mol Aspects Med. 2017; 54, 28–36.Google Scholar
37. Bai, H, Sakurai, T, Fujiwara, H, et al. Functions of interferon tau as an immunological regulator for establishment of pregnancy. Reprod Med Biol. 2012; 11, 109–116.CrossRefGoogle ScholarPubMed
38. Kubisch, HM, Sirisathien, S, Bosch, P, et al. Effects of developmental stage, embryonic interferon-tau secretion and recipient synchrony on pregnancy rate after transfer of in vitro produced bovine blastocysts. Reprod Domest Anim. 2004; 39, 120–124.CrossRefGoogle ScholarPubMed
39. Rodina, TM, Cooke, FN, Hansen, PJ, Ealy, AD. Oxygen tension and medium type actions on blastocyst development and interferon-tau secretion in cattle. Anim Reprod Sci. 2009; 111, 173–188.CrossRefGoogle ScholarPubMed
40. Ikeda, S. Nutriepigenetics in livestock early embryos – roles of one-carbon metabolism in early embryonic development. Proc Jpn Soc Anim Nutr Metab. 2016; 60, 1–11.Google Scholar
41. Sinclair, KD, Rutherford, KM, Wallace, JM, et al. Epigenetics and developmental programming of welfare and production traits in farm animals. Reprod Fertil Dev. 2016; 28, 1443–1478.Google Scholar
42. Triantaphyllopoulos, KA, Ikonomopoulos, I, Bannister, AJ. Epigenetics and inheritance of phenotype variation in livestock. Epigenetics Chromatin. 2016; 9, 31.CrossRefGoogle ScholarPubMed
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