دورية أكاديمية
Dynamics of transcription is affected by oxygen tension and developmental speed during in vitro production of bovine embryos.
العنوان: | Dynamics of transcription is affected by oxygen tension and developmental speed during in vitro production of bovine embryos. |
---|---|
المؤلفون: | de Lima CB; Centre de Recherche en Reproduction, Développement et Santé Intergénérationnelle (CRDSI), Département des Sciences Animales, Université Laval, Quebec, Quebec, Canada.; Laboratory of Embryonic Metabolism and Epigenetic, Center of Natural and Human Science, Federal University of ABC, Santo Andre, SP, Brazil., do Amaral DT; Center of Natural and Human Science, Federal University of ABC, Santo Andre, SP, Brazil., Ispada J; Laboratory of Embryonic Metabolism and Epigenetic, Center of Natural and Human Science, Federal University of ABC, Santo Andre, SP, Brazil., Dos Santos ÉC; Laboratory of Embryonic Metabolism and Epigenetic, Center of Natural and Human Science, Federal University of ABC, Santo Andre, SP, Brazil., Fontes PK; Laboratory of Embryonic Metabolism and Epigenetic, Center of Natural and Human Science, Federal University of ABC, Santo Andre, SP, Brazil., Nogueira MFG; Department of Biological Sciences, School of Sciences and Languages, São Paulo State University, Campus Assis, Assis, SP, Brazil., Milazzotto MP; Laboratory of Embryonic Metabolism and Epigenetic, Center of Natural and Human Science, Federal University of ABC, Santo Andre, SP, Brazil. |
المصدر: | Reproduction in domestic animals = Zuchthygiene [Reprod Domest Anim] 2024 May; Vol. 59 (5), pp. e14620. |
نوع المنشور: | Journal Article |
اللغة: | English |
بيانات الدورية: | Publisher: Paul Parey Scientific Publishers Country of Publication: Germany NLM ID: 9015668 Publication Model: Print Cited Medium: Internet ISSN: 1439-0531 (Electronic) Linking ISSN: 09366768 NLM ISO Abbreviation: Reprod Domest Anim Subsets: MEDLINE |
أسماء مطبوعة: | Original Publication: Berlin ; Hamburg : Paul Parey Scientific Publishers, c1990- |
مواضيع طبية MeSH: | Oxygen*/metabolism , Embryonic Development* , Gene Expression Regulation, Developmental* , Embryo Culture Techniques*/veterinary , Blastocyst*/metabolism, Animals ; Cattle/embryology ; Transcription, Genetic ; Fertilization in Vitro/veterinary ; Female |
مستخلص: | This study examines the impact of oxygen tension and embryo kinetics on gene transcription dynamics in pathways crucial for embryonic preimplantation development, including lipid metabolism, carbohydrate transport and metabolism, mitochondrial function, stress response, apoptosis and transcription regulation. Bovine embryos were generated in vitro and allocated into two groups based on oxygen tension (20% or 5%) at 18 h post insemination (hpi). At 40 hpi, embryos were categorized into Fast (≥4 cells) or Slow (2 cells) groups, resulting in four experimental groups: FCL20, FCL5, SCL20 and SCL5. Embryo collection also occurred at 72 hpi (16-cell stage; groups FMO20, FMO5, SMO20 and SMO5) and at 168 hpi (expanded blastocyst (BL) stage; groups FBL20, FBL5, SBL20 and SBL5). Pools of three embryos per group were analysed in four replicates using inventoried TaqMan assays specific for Bos taurus, targeting 93 genes. Gene expression patterns were analysed using the K-means algorithm, revealing three main clusters: genes with low relative abundance at the cleavage (CL) and 16-cell morula (MO) stages but increased at the BL stage (cluster 1); genes with higher abundances at CL but decreasing at MO and BL (cluster 2); and genes with low levels at CL, higher levels at MO and decreased levels at BL (cluster 3). Within each cluster, genes related to epigenetic mechanisms, cell differentiation events and glucose metabolism were particularly influenced by differences in developmental kinetics and oxygen tension. Fast-developing embryos, particularly those cultured under low oxygen tension, exhibited transcript dynamics more closely resembling that reported in vivo-produced embryos. (© 2024 Wiley‐VCH GmbH. Published by John Wiley & Sons Ltd.) |
References: | Akella, N. M., Ciraku, L., & Reginato, M. J. (2019). Fueling the fire: Emerging role of the hexosamine biosynthetic pathway in cancer. BMC Biology, 17(1), 52. https://doi.org/10.1186/s12915‐019‐0671‐3. Alves, G. P., Cordeiro, F. B., Bruna de Lima, C., Annes, K., Cristina dos Santos, É., Ispada, J., Fontes, P. K., Nogueira, M. F. G., Nichi, M., & Milazzotto, M. P. (2019). Follicular environment as a predictive tool for embryo development and kinetics in cattle. Reproduction, Fertility and Development, 31(3), 451–461. https://doi.org/10.1071/RD18143. Amin, A., Gad, A., Salilew‐Wondim, D., Prastowo, S., Held, E., Hoelker, M., Rings, F., Tholen, E., Neuhoff, C., Looft, C., Schellander, K., & Tesfaye, D. (2014). Bovine embryo survival under oxidative‐stress conditions is associated with activity of the NRF2‐mediated oxidative‐stress‐response pathway: NRF2‐mediated oxidative stress response activity in embryos. Molecular Reproduction and Development, 81(6), 497–513. https://doi.org/10.1002/mrd.22316. Bogliotti, Y. S., Chung, N., Paulson, E. E., Chitwood, J., Halstead, M., Kern, C., Schultz, R. M., & Ross, P. J. (2020). Transcript profiling of bovine embryos implicates specific transcription factors in the maternal‐to‐embryo transition. Biology of Reproduction, 102(3), 671–679. https://doi.org/10.1093/biolre/ioz209. Carrocera, S., Caamaño, J. N., Trigal, B., Martín, D., & Díez, C. (2016). Developmental kinetics of in vitro–produced bovine embryos: An aid for making decisions. Theriogenology, 85(5), 822–827. https://doi.org/10.1016/j.theriogenology.2015.10.028. Catalá, M. G., Izquierdo, D., Rodríguez‐Prado, M., Hammami, S., & Paramio, M.‐T. (2012). Effect of oocyte quality on blastocyst development after in vitro fertilization (IVF) and intracytoplasmic sperm injection (ICSI) in a sheep model. Fertility and Sterility, 97(4), 1004–1008. https://doi.org/10.1016/j.fertnstert.2011.12.043. de Lima, C. B., dos Santos, É. C., Ispada, J., Fontes, P. K., Nogueira, M. F. G., dos Santos, C. M. D., & Milazzotto, M. P. (2020). The dynamics between in vitro culture and metabolism: Embryonic adaptation to environmental changes. Scientific Reports, 10(1), 15672. https://doi.org/10.1038/s41598‐020‐72221‐1. Dobrzyn, P., Dobrzyn, A., Miyazaki, M., Cohen, P., Asilmaz, E., Hardie, D. G., Friedman, J. M., & Ntambi, J. M. (2004). Stearoyl‐CoA desaturase 1 deficiency increases fatty acid oxidation by activating AMP‐activated protein kinase in liver. Proceedings of the National Academy of Sciences of the United States of America, 101(17), 6409–6414. https://doi.org/10.1073/pnas.0401627101. Dobrzyn, P., Sampath, H., Dobrzyn, A., Miyazaki, M., & Ntambi, J. M. (2008). Loss of stearoyl‐CoA desaturase 1 inhibits fatty acid oxidation and increases glucose utilization in the heart. American Journal of Physiology: Endocrinology and Metabolism, 294(2), E357–E364. https://doi.org/10.1152/ajpendo.00471.2007. Feng, Z., & Levine, A. J. (2010). The regulation of energy metabolism and the IGF‐1/mTOR pathways by the p53 protein. Trends in Cell Biology, 20(7), 427–434. https://doi.org/10.1016/j.tcb.2010.03.004. Fontes, P. K., Castilho, A. C. S., Razza, E. M., & Nogueira, M. F. G. (2020). Bona fide gene expression analysis of samples from the bovine reproductive system by microfluidic platform. Analytical Biochemistry, 596, 113641. https://doi.org/10.1016/j.ab.2020.113641. Goll, M. G., & Bestor, T. H. (2005). Eukaryotic cytosine methyltransferases. Annual Review of Biochemistry, 74(1), 481–514. https://doi.org/10.1146/annurev.biochem.74.010904.153721. Graf, A., Krebs, S., Zakhartchenko, V., Schwalb, B., Blum, H., & Wolf, E. (2014). Fine mapping of genome activation in bovine embryos by RNA sequencing. Proceedings of the National Academy of Sciences of the United States of America, 111(11), 4139–4144. https://doi.org/10.1073/pnas.1321569111. Gu, Z. (2022). Complex heatmap visualization. iMeta, 1(3), e43. Guerin, P. (2001). Oxidative stress and protection against reactive oxygen species in the pre‐implantation embryo and its surroundings. Human Reproduction Update, 7(2), 175–189. https://doi.org/10.1093/humupd/7.2.175. Halkidi, M., Vazirgiannis, M., & Batistakis, Y. (2000). Quality scheme assessment in the clustering process. Proceedings of PKDD, 1910, 265–276. Hardy, M. L. M., Day, M. L., & Morris, M. B. (2021). Redox regulation and oxidative stress in mammalian oocytes and embryos developed in vivo and in vitro. International Journal of Environmental Research and Public Health, 18(21), 11374. https://doi.org/10.3390/ijerph182111374. Heard, E., Clerc, P., & Avner, P. (1997). X‐Chromosome inactivation in mammals. Annual Review of Genetics, 31(1), 571–610. https://doi.org/10.1146/annurev.genet.31.1.571. Herbemont, C., Labrosse, J., Bennani‐Smires, B., Cedrin‐Durnerin, I., Peigne, M., Sermondade, N., Sarandi, S., Vivot, A., Vicaut, E., Talib, Z., Grynberg, M., & Sifer, C. (2021). Impact of oxygen tension according to embryo stage of development: A prospective randomized study. Scientific Reports, 11(1), 22313. https://doi.org/10.1038/s41598‐021‐01488‐9. Ispada, J., da Fonseca Junior, A. M., de Lima, C. B., dos Santos, E. C., Fontes, P. K., Nogueira, M. F. G., da Silva, V. L., Almeida, F. N., Leite, S. C., Chitwood, J. L., Ross, P. J., & Milazzotto, M. P. (2020). Tricarboxylic acid cycle metabolites as mediators of DNA methylation reprogramming in bovine preimplantation embryos. International Journal of Molecular Sciences, 21(18), 6868. https://doi.org/10.3390/ijms21186868. Ispada, J., de Lima, C. B., Sirard, M.‐A., Fontes, P. K., Nogueira, M. F. G., Annes, K., & Milazzotto, M. P. (2018). Genome‐wide screening of DNA methylation in bovine blastocysts with different kinetics of development. Epigenetics & Chromatin, 11(1), 1. https://doi.org/10.1186/s13072‐017‐0171‐z. Juan, C. A., Pérez de la Lastra, J. M., Plou, F. J., & Pérez‐Lebeña, E. (2021). The chemistry of reactive oxygen species (ROS) revisited: Outlining their role in biological macromolecules (DNA, lipids and proteins) and induced pathologies. International Journal of Molecular Sciences, 22, 4642. https://doi.org/10.3390/ijms22094642. Kassambara, A., & Mundt, F. (2020). Package ‘factoextra’. Extract and visualize the results of multivariate data analyses. 76(2). Khan, D. R., Dubé, D., Gall, L., Peynot, N., Ruffini, S., Laffont, L., Le Bourhis, D., Degrelle, S., Jouneau, A., & Duranthon, V. (2012). Expression of pluripotency master regulators during two key developmental transitions: EGA and early lineage specification in the bovine embryo. PLoS One, 7(3), e34110. https://doi.org/10.1371/journal.pone.0034110. Krisher, R. L. (2004). The effect of oocyte quality on development. Journal of Animal Science, 82(E‐Suppl), E14–E23. https://doi.org/10.2527/2004.8213_supplE14x. Lee, M. T., Bonneau, A. R., Takacs, C. M., Bazzini, A. A., DiVito, K. R., Fleming, E. S., & Giraldez, A. J. (2013). Nanog, Pou5f1 and SoxB1 activate zygotic gene expression during the maternal‐to‐zygotic transition. Nature, 503(7476), 360–364. Leite, R. F., Annes, K., Ispada, J., de Lima, C. B., dos Santos, É. C., Fontes, P. K., Nogueira, M. F. G., & Milazzotto, M. P. (2017). Oxidative stress alters the profile of transcription factors related to early development on in vitro produced embryos. Oxidative Medicine and Cellular Longevity, 2017, 1–14. https://doi.org/10.1155/2017/1502489. Li, W., Daya, S., & Gunby, J. (2004). Faster embryo growth rate in vitro increases probability of pregnancy in assisted reproduction cycles. International Congress Series, 1271, 143–146. https://doi.org/10.1016/j.ics.2004.05.122. Liemburg‐Apers, D. C., Willems, P. H. G. M., Koopman, W. J. H., & Grefte, S. (2015). Interactions between mitochondrial reactive oxygen species and cellular glucose metabolism. Archives of Toxicology, 89(8), 1209–1226. https://doi.org/10.1007/s00204‐015‐1520‐y. Luna, M., Copperman, A. B., Duke, M., Ezcurra, D., Sandler, B., & Barritt, J. (2008). Human blastocyst morphological quality is significantly improved in embryos classified as fast on day 3 (≥10 cells), bringing into question current embryological dogma. Fertility and Sterility, 89(2), 358–363. https://doi.org/10.1016/j.fertnstert.2007.03.030. Maechler, M. (2023). Cluster: “Finding groups in data”: Cluster analysis extended Rousseeuw et al. R package version 2.1. 0. 2015. Memili, E., & First, N. L. (1999). Control of gene expression at the onset of bovine embryonic development. Biology of Reproduction, 61(5), 1198–1207. https://doi.org/10.1095/biolreprod61.5.1198. Milazzotto, M. P., Goissis, M. D., Chitwood, J. L., Annes, K., Soares, C. A., Ispada, J., Assumpção, M. E. O. Á., & Ross, P. J. (2016). Early cleavages influence the molecular and the metabolic pattern of individually cultured bovine blastocysts: Morphokinetic and transcriptome pattern in embryos. Molecular Reproduction and Development, 83(4), 324–336. https://doi.org/10.1002/mrd.22619. Milazzotto, M. P., Noonan, M. J., & de Almeida Monteiro Melo Ferraz, M. (2022). Mining RNAseq data reveals dynamic metaboloepigenetic profiles in human, mouse and bovine pre‐implantation embryos. iScience, 25(3), 103904. https://doi.org/10.1016/j.isci.2022.103904. Obeidat, Y., Catandi, G., Carnevale, E., Chicco, A. J., DeMann, A., Field, S., & Chen, T. (2019). A multi‐sensor system for measuring bovine embryo metabolism. Biosensors and Bioelectronics, 126, 615–623. https://doi.org/10.1016/j.bios.2018.09.071. Okano, M., Bell, D. W., Haber, D. A., & Li, E. (1999). DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell, 99(3), 247–257. https://doi.org/10.1016/S0092‐8674(00)81656‐6. Pantaleon, M., Harvey, M. B., Pascoe, W. S., James, D. E., & Kaye, P. L. (1997). Glucose transporter GLUT3: Ontogeny, targeting, and role in the mouse blastocyst. Proceedings of the National Academy of Sciences of the United States of America, 94(8), 3795–3800. https://doi.org/10.1073/pnas.94.8.3795. Pantaleon, M., Scott, J., & Kaye, P. L. (2008). Nutrient sensing by the early mouse embryo: Hexosamine biosynthesis and glucose signaling during preimplantation development. Biology of Reproduction, 78(4), 595–600. https://doi.org/10.1095/biolreprod.107.062877. Parrish, J. J., Susko‐Parrish, J., Winer, M. A., & First, N. L. (1988). Capacitation of bovine sperm by heparin. Biology of Reproduction, 38(5), 1171–1180. https://doi.org/10.1095/biolreprod38.5.1171. Parrish, J. J., Susko‐Parrish, J. L., Leibfried‐Rutledge, M. L., Critser, E. S., Eyestone, W. H., & First, N. L. (1986). Bovine in vitro fertilization with frozen‐thawed semen. Theriogenology, 25(4), 591–600. https://doi.org/10.1016/0093‐691X(86)90143‐3. Perry, A. C., Asami, M., Lam, B. Y., & Yeo, G. S. (2023). The initiation of mammalian embryonic transcription: To begin at the beginning. Trends in Cell Biology, 33(5), 365–373. Rousseeuw, P. J. (1987). Silhouettes: A graphical aid to the interpretation and validation of cluster analysis. Journal of Computational and Applied Mathematics, 20, 53–65. https://doi.org/10.1016/0377‐0427(87)90125‐7. Salilew‐Wondim, D., Tesfaye, D., Rings, F., Held‐Hoelker, E., Miskel, D., Sirard, M.‐A., Tholen, E., Schellander, K., & Hoelker, M. (2021). The global gene expression outline of the bovine blastocyst: Reflector of environmental conditions and predictor of developmental capacity. BMC Genomics, 22(1), 408. https://doi.org/10.1186/s12864‐021‐07693‐0. Silva, T., Santos, E. C., Annes, K., Soares, C. A., Leite, R. F., Lima, C. B., & Milazzotto, M. P. (2016). Morphokinetic‐related response to stress in individually cultured bovine embryos. Theriogenology, 86(5), 1308–1317. https://doi.org/10.1016/j.theriogenology.2016.04.072. Soto‐Moreno, E. J., Balboula, A., Spinka, C., & Rivera, R. M. (2021). Serum supplementation during bovine embryo culture affects their development and proliferation through macroautophagy and endoplasmic reticulum stress regulation. PLoS One, 16(12), e0260123. https://doi.org/10.1371/journal.pone.0260123. Trigal, B., Gómez, E., Caamaño, J. N., Muñoz, M., Moreno, J., Carrocera, S., Martín, D., & Diez, C. (2012). In vitro and in vivo quality of bovine embryos in vitro produced with sex‐sorted sperm. Theriogenology, 78(7), 1465–1475. https://doi.org/10.1016/j.theriogenology.2012.06.018. Wang, X., Xiao, Y., Zhou, Y., & Wang, H. (2023). Development speed of sibling embryo positively reflects live birth rate after fresh day 3 embryo transfer. Scientific Reports, 13(1), 6402. https://doi.org/10.1038/s41598‐023‐33573‐6. Wei, Q., Zhong, L., Zhang, S., Mu, H., Xiang, J., Yue, L., Dai, Y., & Han, J. (2017). Bovine lineage specification revealed by single‐cell gene expression analysis from zygote to blastocyst. Biology of Reproduction, 97(1), 5–17. https://doi.org/10.1093/biolre/iox071. Winata, C. L., & Korzh, V. (2018). The translational regulation of maternal mRNA s in time and space. FEBS Letters, 592(17), 3007–3023. https://doi.org/10.1002/1873‐3468.13183. Yagi, M., Kabata, M., Tanaka, A., Ukai, T., Ohta, S., Nakabayashi, K., Shimizu, M., Hata, K., Meissner, A., Yamamoto, T., & Yamada, Y. (2020). Identification of distinct loci for de novo DNA methylation by DNMT3A and DNMT3B during mammalian development. Nature Communications, 11(1), 3199. https://doi.org/10.1038/s41467‐020‐16989‐w. Yuan, Y. Q., Van Soom, A., Coopman, F. O. J., Mintiens, K., Boerjan, M. L., Van Zeveren, A., de Kruif, A., & Peelman, L. J. (2003). Influence of oxygen tension on apoptosis and hatching in bovine embryos cultured in vitro. Theriogenology, 59(7), 1585–1596. https://doi.org/10.1016/S0093‐691X(02)01204‐9. |
معلومات مُعتمدة: | Coordenação de Aperfeiçoamento de Pessoal de Nível Superior; 2015/03381-0 Fundação de Amparo à Pesquisa do Estado de São Paulo; 2017/18384-0 Fundação de Amparo à Pesquisa do Estado de São Paulo |
فهرسة مساهمة: | Keywords: bovine; development; embryo; oxygen tension |
المشرفين على المادة: | S88TT14065 (Oxygen) |
تواريخ الأحداث: | Date Created: 20240527 Date Completed: 20240527 Latest Revision: 20240527 |
رمز التحديث: | 20240527 |
DOI: | 10.1111/rda.14620 |
PMID: | 38798166 |
قاعدة البيانات: | MEDLINE |
تدمد: | 1439-0531 |
---|---|
DOI: | 10.1111/rda.14620 |