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Paternal high-fat diet altered H3K36me3 pattern of pre-implantation embryos

Published online by Cambridge University Press:  29 November 2023

Bin Meng
Affiliation:
Laboratory Animal Center, Xi’an Jiaotong University Health Science Centre, Xi’an, Shaanxi, China The Assisted Reproduction Center, Northwest Women’s and Children’s Hospital, Xi’an, China
Jiahui He
Affiliation:
Cancer Center, Renmin Hospital of Wuhan University, Wuhan, Hubei Province, China
Wenbin Cao
Affiliation:
Laboratory Animal Center, Xi’an Jiaotong University Health Science Centre, Xi’an, Shaanxi, China Key Laboratory of Environment and Genes Related to Diseases, Ministry of Education of China, Xi’an, China
Yanru Zhang
Affiliation:
Laboratory Animal Center, Xi’an Jiaotong University Health Science Centre, Xi’an, Shaanxi, China Key Laboratory of Environment and Genes Related to Diseases, Ministry of Education of China, Xi’an, China
Jia Qi
Affiliation:
Laboratory Animal Center, Xi’an Jiaotong University Health Science Centre, Xi’an, Shaanxi, China Key Laboratory of Environment and Genes Related to Diseases, Ministry of Education of China, Xi’an, China
Shiwei Luo
Affiliation:
Laboratory Animal Center, Xi’an Jiaotong University Health Science Centre, Xi’an, Shaanxi, China
Chong Shen
Affiliation:
Laboratory Animal Center, Xi’an Jiaotong University Health Science Centre, Xi’an, Shaanxi, China
Juan Zhao
Affiliation:
Laboratory Animal Center, Xi’an Jiaotong University Health Science Centre, Xi’an, Shaanxi, China Department of Hematology, The First Affiliated Hospital of Xi’an Jiaotong University, Xi’an, Shaanxi, China
Ying Xue
Affiliation:
Laboratory Animal Center, Xi’an Jiaotong University Health Science Centre, Xi’an, Shaanxi, China
Pengxiang Qu
Affiliation:
Laboratory Animal Center, Xi’an Jiaotong University Health Science Centre, Xi’an, Shaanxi, China Key Laboratory of Environment and Genes Related to Diseases, Ministry of Education of China, Xi’an, China
Enqi Liu*
Affiliation:
Laboratory Animal Center, Xi’an Jiaotong University Health Science Centre, Xi’an, Shaanxi, China Key Laboratory of Environment and Genes Related to Diseases, Ministry of Education of China, Xi’an, China
*
Corresponding author: Enqi Liu; Email: liuenqi@xjtu.edu.cn

Summary

The global transition towards diets high in calories has contributed to 2.1 billion people becoming overweight, or obese, which damages male reproduction and harms offspring. Recently, more and more studies have shown that paternal exposure to stress closely affects the health of offspring in an intergenerational and transgenerational way. SET Domain Containing 2 (SETD2), a key epigenetic gene, is highly conserved among species, is a crucial methyltransferase for converting histone 3 lysine 36 dimethylation (H3K36me2) into histone 3 lysine 36 trimethylation (H3K36me3), and plays an important regulator in the response to stress. In this study, we compared patterns of SETD2 expression and the H3K36me3 pattern in pre-implantation embryos derived from normal or obese mice induced by high diet. The results showed that SETD2 mRNA was significantly higher in the high-fat diet (HFD) group than the control diet (CD) group at the 2-cell, 4-cell, 8-cell, and 16-cell stages, and at the morula and blastocyst stages. The relative levels of H3K36me3 in the HFD group at the 2-cell, 4-cell, 8-cell, 16-cell, morula stage, and blastocyst stage were significantly higher than in the CD group. These results indicated that dietary changes in parental generation (F0) male mice fed a HFD were traceable in SETD2/H3K36me3 in embryos, and that a paternal high-fat diet brings about adverse effects for offspring that might be related to SETD2/H3K36me3, which throws new light on the effect of paternal obesity on offspring from an epigenetic perspective.

Type
Research Article
Copyright
© The Author(s), 2023. Published by Cambridge University Press

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References

Bhadsavle, S. S. and Golding, M. C. (2022). Paternal epigenetic influences on placental health and their impacts on offspring development and disease. Frontiers in Genetics, 13, 1068408. doi: 10.3389/fgene.2022.1068408 CrossRefGoogle ScholarPubMed
Biagioni, E. M., May, L. E. and Broskey, N. T. (2021). The impact of advanced maternal age on pregnancy and offspring health: A mechanistic role for placental angiogenic growth mediators. Placenta, 106, 1521. doi: 10.1016/j.placenta.2021.01.024 CrossRefGoogle Scholar
Binder, N. K., Hannan, N. J. and Gardner, D. K. (2012). Paternal diet-induced obesity retards early mouse embryo development, mitochondrial activity and pregnancy health. PLOS ONE, 7(12), e52304. doi: 10.1371/journal.pone.0052304 CrossRefGoogle ScholarPubMed
Broughton, D. E. and Moley, K. H. (2017). Obesity and female infertility: Potential mediators of obesity’s impact. Fertility and Sterility, 107(4), 840847. doi: 10.1016/j.fertnstert.2017.01.017 CrossRefGoogle ScholarPubMed
Chen, K., Liu, J., Liu, S., Xia, M., Zhang, X., Han, D., Jiang, Y., Wang, C. and Cao, X. (2017). Methyltransferase SETD2-mediated methylation of STAT1 is critical for interferon antiviral activity. Cell, 170(3), 492506.e14. doi: 10.1016/j.cell.2017.06.042 CrossRefGoogle ScholarPubMed
Chew, N. W. S., Ng, C. H., Tan, D. J. H., Kong, G., Lin, C., Chin, Y. H., Lim, W. H., Huang, D. Q., Quek, J., Fu, C. E., Xiao, J., Syn, N., Foo, R., Khoo, C. M., Wang, J. W., Dimitriadis, G. K., Young, D. Y., Siddiqui, M. S., Lam, C. S. P., Wang, Y., et al. (2023). The global burden of metabolic disease: Data from 2000 to 2019. Cell Metabolism, 35(3), 414428.e3. doi: 10.1016/j.cmet.2023.02.003 CrossRefGoogle ScholarPubMed
Choufani, S., Turinsky, A. L., Melamed, N., Greenblatt, E., Brudno, M., Bérard, A., Fraser, W. D., Weksberg, R., Trasler, J., Monnier, P. and 3D cohort study group. (2019). Impact of assisted reproduction, infertility, sex and paternal factors on the placental DNA methylome. Human Molecular Genetics, 28(3), 372385. doi: 10.1093/hmg/ddy321 CrossRefGoogle ScholarPubMed
de Castro Barbosa, T., Ingerslev, L. R., Alm, P. S., Versteyhe, S., Massart, J., Rasmussen, M., Donkin, I., Sjögren, R., Mudry, J. M., Vetterli, L., Gupta, S., Krook, A., Zierath, J. R. and Barrès, R. (2016). High-fat diet reprograms the epigenome of rat spermatozoa and transgenerationally affects metabolism of the offspring. Molecular Metabolism, 5(3), 184197. doi: 10.1016/j.molmet.2015.12.002 CrossRefGoogle ScholarPubMed
Deng, M., Chen, B., Liu, Z., Cai, Y., Wan, Y., Zhou, J. and Wang, F. (2020). Exchanges of histone methylation and variants during mouse zygotic genome activation. Zygote, 28(1), 5158. doi: 10.1017/S0967199419000649 CrossRefGoogle ScholarPubMed
Deshpande, S. S., Nemani, H., Pothani, S. and Balasinor, N. H. (2019). Altered endocrine, cytokine signaling and oxidative stress: A plausible reason for differential changes in testicular cells in diet-induced and genetically inherited – Obesity in adult rats. Reproductive Biology, 19(3), 303308. doi: 10.1016/j.repbio.2019.06.005 CrossRefGoogle ScholarPubMed
Fontelles, C. C., da Cruz, R. S., Gonsiewski, A. K., Barin, E., Tekmen, V., Jin, L., Cruz, M. I., Loudig, O., Warri, A. and de Assis, S. (2021). Systemic alterations play a dominant role in epigenetic predisposition to breast cancer in offspring of obese fathers and is transmitted to a second generation. Scientific Reports, 11(1), 7317. doi: 10.1038/s41598-021-86548-w CrossRefGoogle ScholarPubMed
Godschalk, R., Remels, A., Hoogendoorn, C., van Benthem, J., Luijten, M., Duale, N., Brunborg, G., Olsen, A. K., Bouwman, F. G., Munnia, A., Peluso, M., Mariman, E. and van Schooten, F. J. (2018). Paternal exposure to environmental chemical stress affects male offspring’s hepatic mitochondria. Toxicological Sciences, 162(1), 241250. doi: 10.1093/toxsci/kfx246 CrossRefGoogle ScholarPubMed
Hu, M., Sun, X. J., Zhang, Y. L., Kuang, Y., Hu, C. Q., Wu, W. L., Shen, S. H., Du, T. T., Li, H., He, F., Xiao, H. S., Wang, Z. G., Liu, T. X., Lu, H., Huang, Q. H., Chen, S. J. and Chen, Z. (2010). Histone H3 lysine 36 methyltransferase Hypb/Setd2 is required for embryonic vascular remodeling. Proceedings of the National Academy of Sciences of the United States of America, 107(7), 29562961. doi: 10.1073/pnas.0915033107 CrossRefGoogle ScholarPubMed
Jawaid, A., Jehle, K. L. and Mansuy, I. M. (2021). Impact of parental exposure on offspring health in humans. Trends in Genetics, 37(4), 373388. doi: 10.1016/j.tig.2020.10.006 CrossRefGoogle ScholarPubMed
Kaltsas, A., Moustakli, E., Zikopoulos, A., Georgiou, I., Dimitriadis, F., Symeonidis, E. N., Markou, E., Michaelidis, T. M., Tien, D. M. B., Giannakis, I., Ioannidou, E. M., Papatsoris, A., Tsounapi, P., Takenaka, A., Sofikitis, N. and Zachariou, A. (2023). Impact of advanced paternal age on fertility and risks of genetic disorders in offspring. Genes, 14(2). doi: 10.3390/genes14020486 CrossRefGoogle ScholarPubMed
King, S. E. and Skinner, M. K. (2020). Epigenetic transgenerational inheritance of obesity susceptibility. Trends in Endocrinology and Metabolism, 31(7), 478494. doi: 10.1016/j.tem.2020.02.009 CrossRefGoogle ScholarPubMed
Li, C., Diao, F., Qiu, D., Jiang, M., Li, X., Han, L., Li, L., Hou, X., Ge, J., Ou, X., Liu, J. and Wang, Q. (2018). Histone methyltransferase SETD2 is required for meiotic maturation in mouse oocyte. Journal of Cellular Physiology, 234(1), 661668. doi: 10.1002/jcp.26836 CrossRefGoogle ScholarPubMed
Li, C., Huang, Z. and Gu, L. (2020). SETD2 reduction adversely affects the development of mouse early embryos. Journal of Cellular Biochemistry, 121(1), 797803. doi: 10.1002/jcb.29325 CrossRefGoogle ScholarPubMed
Liu, D. J., Zhang, F., Chen, Y., Jin, Y., Zhang, Y. L., Chen, S. B., Xie, Y. Y., Huang, Q. H., Zhao, W. L., Wang, L., Xu, P. F., Chen, Z., Chen, S. J., Li, B., Zhang, A. and Sun, X. J. (2020). setd2 knockout zebrafish is viable and fertile: Differential and developmental stress-related requirements for Setd2 and histone H3K36 trimethylation in different vertebrate animals. Cell Discovery, 6, 72. doi: 10.1038/s41421-020-00203-8 CrossRefGoogle ScholarPubMed
Mitchell, M., Strick, R., Strissel, P. L., Dittrich, R., McPherson, N. O., Lane, M., Pliushch, G., Potabattula, R., Haaf, T. and El Hajj, N. (2017). Gene expression and epigenetic aberrations in F1-placentas fathered by obese males. Molecular Reproduction and Development, 84(4), 316328. doi: 10.1002/mrd.22784 CrossRefGoogle ScholarPubMed
Molenaar, T. M. and van Leeuwen, F. (2022). SETD2: From chromatin modifier to multipronged regulator of the genome and beyond. Cellular and Molecular Life Sciences, 79(6), 346. doi: 10.1007/s00018-022-04352-9 CrossRefGoogle ScholarPubMed
Ohhata, T., Matsumoto, M., Leeb, M., Shibata, S., Sakai, S., Kitagawa, K., Niida, H., Kitagawa, M. and Wutz, A. (2015). Histone H3 lysine 36 trimethylation is established over the Xist promoter by antisense Tsix transcription and contributes to repressing Xist expression. Molecular and Cellular Biology, 35(22), 39093920. doi: 10.1128/MCB.00561-15 CrossRefGoogle ScholarPubMed
Öst, A., Lempradl, A., Casas, E., Weigert, M., Tiko, T., Deniz, M., Pantano, L., Boenisch, U., Itskov, P. M., Stoeckius, M., Ruf, M., Rajewsky, N., Reuter, G., Iovino, N., Ribeiro, C., Alenius, M., Heyne, S., Vavouri, T. and Pospisilik, J. A. (2014). Paternal diet defines offspring chromatin state and intergenerational obesity. Cell, 159(6), 13521364. doi: 10.1016/j.cell.2014.11.005 CrossRefGoogle ScholarPubMed
Park, J. H., Yoo, Y., Cho, M., Lim, J., Lindroth, A. M. and Park, Y. J. (2018). Diet-induced obesity leads to metabolic dysregulation in offspring via endoplasmic reticulum stress in a sex-specific manner. International Journal of Obesity, 42(2), 244251. doi: 10.1038/ijo.2017.203 CrossRefGoogle Scholar
Pascoal, G. F. L., Geraldi, M. V., Maróstica, M. R. Jr. and Ong, T. P. (2022). Effect of paternal diet on spermatogenesis and offspring health: Focus on epigenetics and interventions with food bioactive compounds. Nutrients, 14(10). doi: 10.3390/nu14102150 CrossRefGoogle ScholarPubMed
Pepin, A. S., Lafleur, C., Lambrot, R., Dumeaux, V. and Kimmins, S. (2022). Sperm histone H3 lysine 4 tri-methylation serves as a metabolic sensor of paternal obesity and is associated with the inheritance of metabolic dysfunction. Molecular Metabolism, 59, 101463. doi: 10.1016/j.molmet.2022.101463 CrossRefGoogle ScholarPubMed
Qin, H., Qu, P., Hu, H., Cao, W., Liu, H., Zhang, Y., Zhao, J., Nazira, F. and Liu, E. (2021). Sperm-borne small RNAs improve the developmental competence of pre-implantation cloned embryos in rabbit. Zygote, 29(5), 331336. doi: 10.1017/S0967199420000805 CrossRefGoogle ScholarPubMed
Qu, P., Luo, S., Du, Y., Zhang, Y., Song, X., Yuan, X., Lin, Z., Li, Y. and Liu, E. (2020). Extracellular vesicles and melatonin benefit embryonic develop by regulating reactive oxygen species and 5-methylcytosine. Journal of Pineal Research, 68(3), e12635. doi: 10.1111/jpi.12635 CrossRefGoogle ScholarPubMed
Rodríguez-González, G. L., Vega, C. C., Boeck, L., Vázquez, M., Bautista, C. J., Reyes-Castro, L. A., Saldaña, O., Lovera, D., Nathanielsz, P. W. and Zambrano, E. (2015). Maternal obesity and overnutrition increase oxidative stress in male rat offspring reproductive system and decrease fertility. International Journal of Obesity, 39(4), 549556. doi: 10.1038/ijo.2014.209 CrossRefGoogle ScholarPubMed
Sertorio, M. N., César, H., de Souza, E. A., Mennitti, L. V., Santamarina, A. B., De Souza Mesquita, L. M., Jucá, A., Casagrande, B. P., Estadella, D., Aguiar, O. Jr. and Pisani, L. P. (2022). Parental high-fat high-sugar diet intake programming inflammatory and oxidative parameters of reproductive health in male offspring. Frontiers in Cell and Developmental Biology, 10, 867127. doi: 10.3389/fcell.2022.867127 CrossRefGoogle ScholarPubMed
Shao, W., Ning, W., Liu, C., Zou, Y., Yao, Y., Kang, J. and Cao, Z. (2022). Histone methyltransferase SETD2 is required for porcine early embryonic development. Animals (Basel), 12(17). doi: 10.3390/ani12172226 Google ScholarPubMed
Terashima, M., Barbour, S., Ren, J., Yu, W., Han, Y. and Muegge, K. (2015). Effect of high fat diet on paternal sperm histone distribution and male offspring liver gene expression. Epigenetics, 10(9), 861871. doi: 10.1080/15592294.2015.1075691 CrossRefGoogle ScholarPubMed
Tilman, D. and Clark, M. (2014). Global diets link environmental sustainability and human health. Nature, 515(7528), 518522. doi: 10.1038/nature13959 CrossRefGoogle ScholarPubMed
Wei, J., Antony, J., Meng, F., MacLean, P., Rhind, R., Laible, G. and Oback, B. (2017). KDM4B-mediated reduction of H3K9me3 and H3K36me3 levels improves somatic cell reprogramming into pluripotency. Scientific Reports, 7(1), 7514. doi: 10.1038/s41598-017-06569-2 CrossRefGoogle ScholarPubMed
Wen, X., Han, Z., Liu, S. J., Hao, X., Zhang, X. J., Wang, X. Y., Zhou, C. J., Ma, Y. Z. and Liang, C. G. (2020). Phycocyanin improves reproductive ability in obese female mice by restoring ovary and oocyte quality. Frontiers in Cell and Developmental Biology, 8, 595373. doi: 10.3389/fcell.2020.595373 CrossRefGoogle ScholarPubMed
Xu, Q., Xiang, Y., Wang, Q., Wang, L., Brind’Amour, J., Bogutz, A. B., Zhang, Y., Zhang, B., Yu, G., Xia, W., Du, Z., Huang, C., Ma, J., Zheng, H., Li, Y., Liu, C., Walker, C. L., Jonasch, E., Lefebvre, L.,... Xie, W. (2019). SETD2 regulates the maternal epigenome, genomic imprinting and embryonic development. Nature Genetics, 51(5), 844856. doi: 10.1038/s41588-019-0398-7 CrossRefGoogle ScholarPubMed
Zhang, T., Cooper, S. and Brockdorff, N. (2015). The interplay of histone modifications – Writers that read. EMBO Reports, 16(11), 14671481. doi: 10.15252/embr.201540945 CrossRefGoogle ScholarPubMed
Zhang, Y., Zhang, H., Wu, W., Wang, D., Lv, Y., Zhao, D., Wang, L., Liu, Y. and Zhang, K. (2023). Clinical and genetic features of luscan-lumish syndrome associated with a novel de novo variant of SETD2 gene: Case report and literature review. Frontiers in Genetics, 14, 1081391. doi: 10.3389/fgene.2023.1081391 CrossRefGoogle ScholarPubMed
Zhu, Q., Yang, Q., Lu, X., Wang, H., Tong, L., Li, Z., Liu, G., Bao, Y., Xu, X., Gu, L., Yuan, J., Liu, X. and Zhu, W. G. (2021). SETD2-mediated H3K14 trimethylation promotes ATR activation and stalled replication fork restart in response to DNA replication stress. Proceedings of the National Academy of Sciences of the United States of America, 118(23). doi: 10.1073/pnas.2011278118 CrossRefGoogle Scholar
Zuo, X., Rong, B., Li, L., Lv, R., Lan, F. and Tong, M. H. (2018). The histone methyltransferase SETD2 is required for expression of acrosin-binding protein 1 and protamines and essential for spermiogenesis in mice. Journal of Biological Chemistry, 293(24), 91889197. doi: 10.1074/jbc.RA118.002851 CrossRefGoogle ScholarPubMed