How the environment affects early embryonic development
Marc-André Sirard A *
+ Author Affiliations
- Author Affiliations
A Faculté des Sciences de l’Agriculture et de l’Alimentation, Département des Sciences Animales, Centre de Recherche en Reproduction, Développement et Santé Intergénérationnelle (CRDSI), Université Laval, Québec, QC G1V 0A6, Canada.
* Correspondence to: Marc-Andre.Sirard@fsaa.ulaval.ca
Reproduction, Fertility and Development 34(2) 203-213 https://doi.org/10.1071/RD21266
Published online: 15 October 2021
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing on behalf of the IETS
Abstract
In the field of animal reproduction, the environment associated with gametes and embryos refers to the parents’ condition as well as conditions surrounding gametes and embryos in vivo or in vitro. This environment is now known to influence not only the functionality of the early embryo but potentially the future phenotype of the offspring. Using transcriptomic and epigenetic molecular analysis, and the bovine model, recent research has shown that both the female and the male metabolic status, for example age, can affect gene expression and gene programming in the embryo. Evidence demonstrates that milking cows, which are losing weight at the time of conception, generates compromised embryos and offspring with a unique metabolic signature. A similar phenomenon has been associated with different culture conditions and the IVF procedure. The general common consequence of these situations is an embryo behaving on ‘economy’ mode where translation, cell division and ATP production is reduced, potentially to adapt to the perceived future environment. Few epidemiological studies have been done in bovines to assess if these changes result in a different phenotype and more studies are required to associate specific molecular changes in embryos with visible consequences later in life.
Keywords: bovine, DNA, embryo, epigenetic, gametes, methylation, spermatozoa.
References
Anckaert, E, and Fair, T (2015). DNA methylation reprogramming during oogenesis and interference by reproductive technologies: studies in mouse and bovine models. Reproduction, Fertility and Development 27, 739–754.| DNA methylation reprogramming during oogenesis and interference by reproductive technologies: studies in mouse and bovine models.Crossref | GoogleScholarGoogle Scholar |
Bonilla, L, Block, J, Denicol, AC, and Hansen, PJ (2014). Consequences of transfer of an in vitro-produced embryo for the dam and resultant calf. Journal of Dairy Science 97, 229–239.
| Consequences of transfer of an in vitro-produced embryo for the dam and resultant calf.Crossref | GoogleScholarGoogle Scholar | 24210495PubMed |
Cagnone, G, and Sirard, M-A (2014). The impact of exposure to serum lipids during in vitro culture on the transcriptome of bovine blastocysts. Theriogenology 81, 712–722.e3.
| The impact of exposure to serum lipids during in vitro culture on the transcriptome of bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 24439163PubMed |
Cagnone, G, and Sirard, M-A (2016). The embryonic stress response to in vitro culture: insight from genomic analysis. Reproduction 152, R247–R261.
| The embryonic stress response to in vitro culture: insight from genomic analysis.Crossref | GoogleScholarGoogle Scholar | 27601713PubMed |
Cagnone, GLM, Dufort, I, Vigneault, C, and Sirard, M-A (2012). Differential gene expression profile in bovine blastocysts resulting from hyperglycemia exposure during early cleavage stages. Biology of Reproduction 86, 50.
| Differential gene expression profile in bovine blastocysts resulting from hyperglycemia exposure during early cleavage stages.Crossref | GoogleScholarGoogle Scholar |
Cardoso, MC, and Leonhardt, H (1999). DNA methyltransferase is actively retained in the cytoplasm during early development. Journal of Cell Biology 147, 25–32.
| DNA methyltransferase is actively retained in the cytoplasm during early development.Crossref | GoogleScholarGoogle Scholar |
Chaput, C, and Sirard, MA (2020). Embryonic response to high beta-hydroxybutyrate (BHB) levels in postpartum dairy cows. Domestic Animal Endocrinology 72, 106431.
| Embryonic response to high beta-hydroxybutyrate (BHB) levels in postpartum dairy cows.Crossref | GoogleScholarGoogle Scholar | 32325411PubMed |
Chen, Q, Yan, W, and Duan, E (2016). Epigenetic inheritance of acquired traits through sperm RNAs and sperm RNA modifications. Nature Reviews Genetics 17, 733–743.
| Epigenetic inheritance of acquired traits through sperm RNAs and sperm RNA modifications.Crossref | GoogleScholarGoogle Scholar | 27694809PubMed |
Daigneault, BW, Rajput, SK, and Smith, GW (2020). Simple workflow for genome and methylation analyses of ejaculated bovine spermatozoa with low sperm input. BioTechniques 68, 155–158.
| Simple workflow for genome and methylation analyses of ejaculated bovine spermatozoa with low sperm input.Crossref | GoogleScholarGoogle Scholar | 31937114PubMed |
Dance, A, Thundathil, J, Blondin, P, and Kastelic, J (2016). Enhanced early-life nutrition of Holstein bulls increases sperm production potential without decreasing postpubertal semen quality. Theriogenology 86, 687–694.e2.
| Enhanced early-life nutrition of Holstein bulls increases sperm production potential without decreasing postpubertal semen quality.Crossref | GoogleScholarGoogle Scholar | 27114168PubMed |
de Montera, B, Fournier, E, Shojaei Saadi, HA, Gagné, D, Laflamme, I, Blondin, P, Sirard, M-A, and Robert, C (2013). Combined methylation mapping of 5mC and 5hmC during early embryonic stages in bovine. BMC Genomics 14, 406.
| Combined methylation mapping of 5mC and 5hmC during early embryonic stages in bovine.Crossref | GoogleScholarGoogle Scholar | 23773395PubMed |
Denomme, MM, White, CR, Gillio-Meina, C, Macdonald, WA, Deroo, BJ, Kidder, GM, and Mann, MRW (2012). Compromised fertility disrupts Peg1 but not Snrpn and Peg3 imprinted methylation acquisition in mouse oocytes. Frontiers in Genetics 3, 129.
| Compromised fertility disrupts Peg1 but not Snrpn and Peg3 imprinted methylation acquisition in mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 22798963PubMed |
Dong, W, Yang, J, Zhang, Y, Liu, S, Ning, C, Ding, X, Wang, W, Zhang, Y, Zhang, Q, and Jiang, L (2021). Integrative analysis of genome-wide DNA methylation and gene expression profiles reveals important epigenetic genes related to milk production traits in dairy cattle. Journal of Animal Breeding and Genetics , .
| Integrative analysis of genome-wide DNA methylation and gene expression profiles reveals important epigenetic genes related to milk production traits in dairy cattle.Crossref | GoogleScholarGoogle Scholar | 33620112PubMed |
Evans, ACO, Mossa, F, Walsh, SW, Scheetz, D, Jimenez-Krassel, F, Ireland, JLH, Smith, GW, and Ireland, JJ (2012). Effects of maternal environment during gestation on ovarian folliculogenesis and consequences for fertility in bovine offspring. Reproduction in Domestic Animals 47, 31–37.
| Effects of maternal environment during gestation on ovarian folliculogenesis and consequences for fertility in bovine offspring.Crossref | GoogleScholarGoogle Scholar |
Farhadova, S, Gomez-Velazquez, M, and Feil, R (2019). Stability and lability of parental methylation imprints in development and disease. Genes 10, 999.
| Stability and lability of parental methylation imprints in development and disease.Crossref | GoogleScholarGoogle Scholar |
Farin, CE, Farin, PW, and Piedrahita, JA (2004). Development of fetuses from in vitro-produced and cloned bovine embryos. Journal of Animal Science 82, E53–E62.
| Development of fetuses from in vitro-produced and cloned bovine embryos.Crossref | GoogleScholarGoogle Scholar | 15471815PubMed |
Feuer, SK, Liu, X, Donjacour, A, Lin, W, Simbulan, RK, Giritharan, G, Piane, LD, Kolahi, K, Ameri, K, Maltepe, E, and Rinaudo, PF (2014). Use of a mouse in vitro fertilization model to understand the developmental origins of health and disease hypothesis. Endocrinology 155, 1956–1969.
| Use of a mouse in vitro fertilization model to understand the developmental origins of health and disease hypothesis.Crossref | GoogleScholarGoogle Scholar | 24684304PubMed |
Fosslie, M, Manaf, A, Lerdrup, M, Hansen, K, Gilfillan, GD, and Dahl, JA (2020). Going low to reach high: small-scale ChIP-seq maps new terrain. Wiley Interdisciplinary Reviews: Systems Biology and Medicine 12, e1465.
| Going low to reach high: small-scale ChIP-seq maps new terrain.Crossref | GoogleScholarGoogle Scholar | 31478357PubMed |
Gad, A, Hoelker, M, Besenfelder, U, Havlicek, V, Cinar, U, Rings, F, Held, E, Dufort, I, Sirard, M-A, Schellander, K, and Tesfaye, D (2012). Molecular mechanisms and pathways involved in bovine embryonic genome activation and their regulation by alternative in vivo and in vitro culture conditions. Biology of Reproduction 87, 100.
| Molecular mechanisms and pathways involved in bovine embryonic genome activation and their regulation by alternative in vivo and in vitro culture conditions.Crossref | GoogleScholarGoogle Scholar | 22811576PubMed |
Gahurova, L, Tomizawa, S-I, Smallwood, SA, Stewart-Morgan, KR, Saadeh, H, Kim, J, Andrews, SR, Chen, T, and Kelsey, G (2017). Transcription and chromatin determinants of de novo DNA methylation timing in oocytes. Epigenetics & Chromatin 10, 25.
| Transcription and chromatin determinants of de novo DNA methylation timing in oocytes.Crossref | GoogleScholarGoogle Scholar |
Ganesan, A (2018). Epigenetics: the first 25 centuries. Philosophical Transactions of the Royal Society B: Biological Sciences 373, 20170067.
| Epigenetics: the first 25 centuries.Crossref | GoogleScholarGoogle Scholar |
Girard, A, Dufort, I, and Sirard, M-A (2015). The effect of energy balance on the transcriptome of bovine granulosa cells at 60 days postpartum. Theriogenology 84, 1350–1361.e6.
| The effect of energy balance on the transcriptome of bovine granulosa cells at 60 days postpartum.Crossref | GoogleScholarGoogle Scholar | 26316219PubMed |
Hammoud, SS, Low, DHP, Yi, C, Lee, CL, Oatley, JM, Payne, CJ, Carrell, DT, Guccione, E, and Cairns, BR (2015). Transcription and imprinting dynamics in developing postnatal male germline stem cells. Genes & Development 29, 2312–2324.
| Transcription and imprinting dynamics in developing postnatal male germline stem cells.Crossref | GoogleScholarGoogle Scholar |
Hill, PWS, Leitch, HG, Requena, CE, Sun, Z, Amouroux, R, Roman-Trufero, M, Borkowska, M, Terragni, J, Vaisvila, R, Linnett, S, Bagci, H, Dharmalingham, G, Haberle, V, Lenhard, B, Zheng, Y, Pradhan, S, and Hajkova, P (2018). Epigenetic reprogramming enables the transition from primordial germ cell to gonocyte. Nature 555, 392–396.
| Epigenetic reprogramming enables the transition from primordial germ cell to gonocyte.Crossref | GoogleScholarGoogle Scholar | 29513657PubMed |
Hosseini, SM, Dufort, I, Caballero, J, Moulavi, F, Ghanaei, HR, and Sirard, MA (2015). Transcriptome profiling of bovine inner cell mass and trophectoderm derived from in vivo generated blastocysts. BMC Developmental Biology 15, 49.
| Transcriptome profiling of bovine inner cell mass and trophectoderm derived from in vivo generated blastocysts.Crossref | GoogleScholarGoogle Scholar | 26681441PubMed |
Huypens, P, Sass, S, Wu, M, Dyckhoff, D, Tschöp, M, Theis, F, Marschall, S, Hrabě de Angelis, M, and Beckers, J (2016). Epigenetic germline inheritance of diet-induced obesity and insulin resistance. Nature Genetics 48, 497–499.
| Epigenetic germline inheritance of diet-induced obesity and insulin resistance.Crossref | GoogleScholarGoogle Scholar | 26974008PubMed |
Jablonka, E, and Lamb, MJ (2002). The changing concept of epigenetics. Annals of the New York Academy of Sciences 981, 82–96.
| The changing concept of epigenetics.Crossref | GoogleScholarGoogle Scholar | 12547675PubMed |
Jung, YH, Sauria, MEG, Lyu, X, Cheema, MS, Ausio, J, Taylor, J, and Corces, VG (2017). Chromatin states in mouse sperm correlate with embryonic and adult regulatory landscapes. Cell Reports 18, 1366–1382.
| Chromatin states in mouse sperm correlate with embryonic and adult regulatory landscapes.Crossref | GoogleScholarGoogle Scholar | 28178516PubMed |
Kastelic, JP (2014). Understanding and evaluating bovine testes. Theriogenology 81, 18–23.
| Understanding and evaluating bovine testes.Crossref | GoogleScholarGoogle Scholar | 24274406PubMed |
Kindsfather, AJ, Czekalski, MA, Pressimone, CA, Erisman, MP, and Mann, MRW (2019). Perturbations in imprinted methylation from assisted reproductive technologies but not advanced maternal age in mouse preimplantation embryos. Clinical Epigenetics 11, 162.
| Perturbations in imprinted methylation from assisted reproductive technologies but not advanced maternal age in mouse preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 31767035PubMed |
Labrecque, R, Lodde, V, Dieci, C, Tessaro, I, Luciano, AM, and Sirard, MA (2015). Chromatin remodelling and histone mRNA accumulation in bovine germinal vesicle oocytes. Molecular Reproduction and Development 82, 450–462.
| Chromatin remodelling and histone mRNA accumulation in bovine germinal vesicle oocytes.Crossref | GoogleScholarGoogle Scholar | 25940597PubMed |
Lafontaine, S, Labrecque, R, Palomino, JM, Blondin, P, and Sirard, M-A (2020). Specific imprinted genes demethylation in association with oocyte donor’s age and culture conditions in bovine embryos assessed at day 7 and 12 post insemination. Theriogenology 158, 321–330.
| Specific imprinted genes demethylation in association with oocyte donor’s age and culture conditions in bovine embryos assessed at day 7 and 12 post insemination.Crossref | GoogleScholarGoogle Scholar | 33010654PubMed |
Lambert, S, Blondin, P, Vigneault, C, Labrecque, R, Dufort, I, and Sirard, M-A (2018). Spermatozoa DNA methylation patterns differ due to peripubertal age in bulls. Theriogenology 106, 21–29.
| Spermatozoa DNA methylation patterns differ due to peripubertal age in bulls.Crossref | GoogleScholarGoogle Scholar | 29031946PubMed |
Landry, DA, Bellefleur, A-M, Labrecque, R, Grand, F-X, Vigneault, C, Blondin, P, and Sirard, M-A (2016). Effect of cow age on the in vitro developmental competence of oocytes obtained after FSH stimulation and coasting treatments. Theriogenology 86, 1240–1246.
| Effect of cow age on the in vitro developmental competence of oocytes obtained after FSH stimulation and coasting treatments.Crossref | GoogleScholarGoogle Scholar | 27215669PubMed |
Ling, Y-H, Zheng, Q, Li, Y-S, Sui, M-H, Wu, H, Zhang, Y-H, Chu, M-X, Ma, Y-H, Fang, F-G, and Xu, L-N (2019). Identification of lncRNAs by RNA sequencing analysis during in vivo pre-implantation developmental transformation in the goat. Frontiers in Genetics 10, 1040.
| Identification of lncRNAs by RNA sequencing analysis during in vivo pre-implantation developmental transformation in the goat.Crossref | GoogleScholarGoogle Scholar | 31708972PubMed |
Lodde, V, Luciano, AM, Franciosi, F, Labrecque, R, and Sirard, MA (2017). Accumulation of chromatin remodelling enzyme and histone transcripts in bovine oocytes. Results and Problems in Cell Differentiation 63, 223–255.
| Accumulation of chromatin remodelling enzyme and histone transcripts in bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 28779321PubMed |
Market-Velker, BA, Zhang, L, Magri, LS, Bonvissuto, AC, and Mann, MRW (2010). Dual effects of superovulation: loss of maternal and paternal imprinted methylation in a dose-dependent manner. Human Molecular Genetics 19, 36–51.
| Dual effects of superovulation: loss of maternal and paternal imprinted methylation in a dose-dependent manner.Crossref | GoogleScholarGoogle Scholar | 19805400PubMed |
McGraw, S, Vigneault, C, and Sirard, M-A (2007). Temporal expression of factors involved in chromatin remodeling and in gene regulation during early bovine in vitro embryo development. Reproduction 133, 597–608.
| Temporal expression of factors involved in chromatin remodeling and in gene regulation during early bovine in vitro embryo development.Crossref | GoogleScholarGoogle Scholar | 17379654PubMed |
Mellisho, EA, Briones, MA, Velásquez, AE, Cabezas, J, Castro, FO, and Rodríguez-Álvarez, L (2019). Extracellular vesicles secreted during blastulation show viability of bovine embryos. Reproduction 158, 477–492.
| Extracellular vesicles secreted during blastulation show viability of bovine embryos.Crossref | GoogleScholarGoogle Scholar | 31600718PubMed |
Milazzotto, MP, de Lima, CB, da Fonseca, AM, Dos Santos, EC, and Ispada, J (2020). Erasing gametes to write blastocysts: metabolism as the new player in epigenetic reprogramming. Animal Reproduction 17, e20200015.
| Erasing gametes to write blastocysts: metabolism as the new player in epigenetic reprogramming.Crossref | GoogleScholarGoogle Scholar | 33029209PubMed |
Mondou, E, Dufort, I, Gohin, M, Fournier, E, and Sirard, M-A (2012). Analysis of microRNAs and their precursors in bovine early embryonic development. Molecular Human Reproduction 18, 425–434.
| Analysis of microRNAs and their precursors in bovine early embryonic development.Crossref | GoogleScholarGoogle Scholar | 22491901PubMed |
Morin-Doré, L, Blondin, P, Vigneault, C, Grand, F-X, Labrecque, R, and Sirard, M-A (2017). Transcriptomic evaluation of bovine blastocysts obtained from peri-pubertal oocyte donors. Theriogenology 93, 111–123.
| Transcriptomic evaluation of bovine blastocysts obtained from peri-pubertal oocyte donors.Crossref | GoogleScholarGoogle Scholar | 28257859PubMed |
Morin-Doré, L, Blondin, P, Vigneault, C, Grand, F-X, Labrecque, R, and Sirard, M-A (2020). DNA methylation status of bovine blastocysts obtained from peripubertal oocyte donors. Molecular Reproduction and Development 87, 910–924.
| DNA methylation status of bovine blastocysts obtained from peripubertal oocyte donors.Crossref | GoogleScholarGoogle Scholar | 32677283PubMed |
Nagaraj, R, Sharpley, MS, Chi, F, Braas, D, Zhou, Y, Kim, R, Clark, AT, and Banerjee, U (2017). Nuclear localization of mitochondrial TCA cycle enzymes as a critical step in mammalian zygotic genome activation. Cell 168, 210–223.e11.
| Nuclear localization of mitochondrial TCA cycle enzymes as a critical step in mammalian zygotic genome activation.Crossref | GoogleScholarGoogle Scholar | 28086092PubMed |
O’Doherty, AM, O’Shea, LC, and Fair, T (2012). Bovine DNA methylation imprints are established in an oocyte size-specific manner, which are coordinated with the expression of the DNMT3 family proteins. Biology of Reproduction 86, 67.
| Bovine DNA methylation imprints are established in an oocyte size-specific manner, which are coordinated with the expression of the DNMT3 family proteins.Crossref | GoogleScholarGoogle Scholar | 22088914PubMed |
Orozco-Lucero, E, Dufort, I, Robert, C, and Sirard, M-A (2014). Rapidly cleaving bovine two-cell embryos have better developmental potential and a distinctive mRNA pattern. Molecular Reproduction and Development 81, 31–41.
| Rapidly cleaving bovine two-cell embryos have better developmental potential and a distinctive mRNA pattern.Crossref | GoogleScholarGoogle Scholar | 24285591PubMed |
Parlee, SD, and MacDougald, OA (2014). Maternal nutrition and risk of obesity in offspring: the Trojan horse of developmental plasticity. Biochimica et Biophysica Acta (BBA) – Molecular Basis of Disease 1842, 495–506.
| Maternal nutrition and risk of obesity in offspring: the Trojan horse of developmental plasticity.Crossref | GoogleScholarGoogle Scholar |
Pericuesta, E, Gutiérrez-Arroyo, JL, Sánchez-Calabuig, MJ, and Gutiérrez-Adán, A (2021). Postnatal catch-up growth programs telomere dynamics and glucose intolerance in low birth weight mice. International Journal of Molecular Sciences 22, 3657.
| Postnatal catch-up growth programs telomere dynamics and glucose intolerance in low birth weight mice.Crossref | GoogleScholarGoogle Scholar | 33915805PubMed |
Perrier, J-P, Kenny, DA, Chaulot-Talmon, A, Byrne, CJ, Sellem, E, Jouneau, L, Aubert-Frambourg, A, Schibler, L, Jammes, H, Lonergan, P, Fair, S, and Kiefer, H (2020). Accelerating onset of puberty through modification of early life nutrition induces modest but persistent changes in bull sperm DNA methylation profiles post-puberty. Frontiers in Genetics 11, 945.
| Accelerating onset of puberty through modification of early life nutrition induces modest but persistent changes in bull sperm DNA methylation profiles post-puberty.Crossref | GoogleScholarGoogle Scholar | 33005172PubMed |
Ribel-Madsen, R, Fraga, MF, Jacobsen, S, Bork-Jensen, J, Lara, E, Calvanese, V, Fernandez, AF, Friedrichsen, M, Vind, BF, Højlund, K, Beck-Nielsen, H, Esteller, M, Vaag, A, and Poulsen, P (2012). Genome-wide analysis of DNA methylation differences in muscle and fat from monozygotic twins discordant for type 2 diabetes. PLoS ONE 7, e51302.
| Genome-wide analysis of DNA methylation differences in muscle and fat from monozygotic twins discordant for type 2 diabetes.Crossref | GoogleScholarGoogle Scholar | 23251491PubMed |
Salilew-Wondim, D, Fournier, E, Hoelker, M, Saeed-Zidane, M, Tholen, E, Looft, C, Neuhoff, C, Besenfelder, U, Havlicek, V, Rings, F, Gagné, D, Sirard, M-A, Robert, C, Shojaei Saadi, HA, Gad, A, Schellander, K, and Tesfaye, D (2015). Genome-wide DNA methylation patterns of bovine blastocysts developed in vivo from embryos completed different stages of development in vitro. PLoS ONE 10, e0140467.
| Genome-wide DNA methylation patterns of bovine blastocysts developed in vivo from embryos completed different stages of development in vitro.Crossref | GoogleScholarGoogle Scholar | 26536655PubMed |
Salilew-Wondim, D, Gebremedhn, S, Hoelker, M, Tholen, E, Hailay, T, and Tesfaye, D (2020). The role of microRNAs in mammalian fertility: from gametogenesis to embryo implantation. International Journal of Molecular Sciences 21, 585.
| The role of microRNAs in mammalian fertility: from gametogenesis to embryo implantation.Crossref | GoogleScholarGoogle Scholar |
Sampaio, RV, Sangalli, JR, De Bem, THC, Ambrizi, DR, Del Collado, M, Bridi, A, de Ávila, ACFCM, Macabelli, CH, de Jesus Oliveira, L, da Silveira, JC, Chiaratti, MR, Perecin, F, Bressan, FF, Smith, LC, Ross, PJ, and Meirelles, FV (2020). Catalytic inhibition of H3K9me2 writers disturbs epigenetic marks during bovine nuclear reprogramming. Scientific Reports 10, 11493.
| Catalytic inhibition of H3K9me2 writers disturbs epigenetic marks during bovine nuclear reprogramming.Crossref | GoogleScholarGoogle Scholar | 32661262PubMed |
Seah, MKY, and Messerschmidt, DM (2018). From germline to soma: epigenetic dynamics in the mouse preimplantation embryo. Current Topics in Developmental Biology 128, 203–235.
| From germline to soma: epigenetic dynamics in the mouse preimplantation embryo.Crossref | GoogleScholarGoogle Scholar | 29477164PubMed |
Simon, L, Liu, L, Murphy, K, Ge, S, Hotaling, J, Aston, KI, Emery, B, and Carrell, DT (2014). Comparative analysis of three sperm DNA damage assays and sperm nuclear protein content in couples undergoing assisted reproduction treatment. Human Reproduction 29, 904–917.
| Comparative analysis of three sperm DNA damage assays and sperm nuclear protein content in couples undergoing assisted reproduction treatment.Crossref | GoogleScholarGoogle Scholar | 24619433PubMed |
Siqueira, LGB, Dikmen, S, Ortega, MS, and Hansen, PJ (2017). Postnatal phenotype of dairy cows is altered by in vitro embryo production using reverse X-sorted semen. Journal of Dairy Science 100, 5899–5908.
| Postnatal phenotype of dairy cows is altered by in vitro embryo production using reverse X-sorted semen.Crossref | GoogleScholarGoogle Scholar | 28456408PubMed |
Sirard, M-A (2019). Distribution and dynamics of mitochondrial DNA methylation in oocytes, embryos and granulosa cells. Scientific Reports 9, 11937.
| Distribution and dynamics of mitochondrial DNA methylation in oocytes, embryos and granulosa cells.Crossref | GoogleScholarGoogle Scholar | 31417147PubMed |
Svoboda, P (2017). Long and small noncoding RNAs during oocyte-to-embryo transition in mammals. Biochemical Society Transactions 45, 1117–1124.
| Long and small noncoding RNAs during oocyte-to-embryo transition in mammals.Crossref | GoogleScholarGoogle Scholar | 28939692PubMed |
Takeda, K, Kobayashi, E, Nishino, K, Imai, A, Adachi, H, Hoshino, Y, Iwao, K, Akagi, S, Kaneda, M, and Watanabe, S (2019). Age-related changes in DNA methylation levels at CpG sites in bull spermatozoa and in vitro fertilization-derived blastocyst-stage embryos revealed by combined bisulfite restriction analysis. The Journal of Reproduction and Development 65, 305–312.
| Age-related changes in DNA methylation levels at CpG sites in bull spermatozoa and in vitro fertilization-derived blastocyst-stage embryos revealed by combined bisulfite restriction analysis.Crossref | GoogleScholarGoogle Scholar | 31061296PubMed |
Takeda, K, Kobayashi, E, Ogata, K, Imai, A, Sato, S, Adachi, H, Hoshino, Y, Nishino, K, Inoue, M, Kaneda, M, and Watanabe, S (2021). Differentially methylated CpG sites related to fertility in Japanese Black bull spermatozoa: epigenetic biomarker candidates to predict sire conception rate. The Journal of Reproduction and Development 67, 99–107.
| Differentially methylated CpG sites related to fertility in Japanese Black bull spermatozoa: epigenetic biomarker candidates to predict sire conception rate.Crossref | GoogleScholarGoogle Scholar | 33441501PubMed |
Tesfaye, D, Hailay, T, Salilew-Wondim, D, Hoelker, M, Bitseha, S, and Gebremedhn, S (2020). Extracellular vesicle mediated molecular signaling in ovarian follicle: implication for oocyte developmental competence. Theriogenology 150, 70–74.
| Extracellular vesicle mediated molecular signaling in ovarian follicle: implication for oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar | 32088041PubMed |
Torres-Flores, U, and Hernández-Hernández, A (2020). The interplay between replacement and retention of histones in the sperm genome. Frontiers in Genetics 11, 780.
| The interplay between replacement and retention of histones in the sperm genome.Crossref | GoogleScholarGoogle Scholar | 32765595PubMed |
Tremblay, R, Dufort, I, and Sirard, M-A (2018). Metabolic stress induces modifications in the epigenetic program of preimplantation bovine embryos. Molecular Reproduction and Development 85, 117–127.
| Metabolic stress induces modifications in the epigenetic program of preimplantation bovine embryos.Crossref | GoogleScholarGoogle Scholar | 29240275PubMed |
Triantaphyllopoulos, KA, Ikonomopoulos, I, and Bannister, AJ (2016). Epigenetics and inheritance of phenotype variation in livestock. Epigenetics & Chromatin 9, 31–31.
| Epigenetics and inheritance of phenotype variation in livestock.Crossref | GoogleScholarGoogle Scholar |
Veenendaal, M, Painter, R, de Rooij, S, Bossuyt, P, van der Post, J, Gluckman, P, Hanson, M, and Roseboom, T (2013). Transgenerational effects of prenatal exposure to the 1944–45 Dutch famine. BJOG: An International Journal of Obstetrics & Gynaecology 120, 548–554.
| Transgenerational effects of prenatal exposure to the 1944–45 Dutch famine.Crossref | GoogleScholarGoogle Scholar |
Wang, L, Zhang, J, Duan, J, Gao, X, Zhu, W, Lu, X, Yang, L, Zhang, J, Li, G, Ci, W, Li, W, Zhou, Q, Aluru, N, Tang, F, He, C, Huang, X, and Liu, J (2014). Programming and inheritance of parental DNA methylomes in mammals. Cell 157, 979–991.
| Programming and inheritance of parental DNA methylomes in mammals.Crossref | GoogleScholarGoogle Scholar | 24813617PubMed |
Wang, L, Hand, JM, Fu, L, Smith, GW, and Yao, J (2019). DNA methylation and miRNA-1296 act in concert to mediate spatiotemporal expression of KPNA7 during bovine oocyte and early embryonic development. BMC Developmental Biology 19, 23.
| DNA methylation and miRNA-1296 act in concert to mediate spatiotemporal expression of KPNA7 during bovine oocyte and early embryonic development.Crossref | GoogleScholarGoogle Scholar | 31787077PubMed |
Wu, C, and Sirard, M-A (2020). Parental effects on epigenetic programming in gametes and embryos of dairy cows. Frontiers in Genetics 11, 557846.
| Parental effects on epigenetic programming in gametes and embryos of dairy cows.Crossref | GoogleScholarGoogle Scholar | 33173533PubMed |
Wu, C, Blondin, P, Vigneault, C, Labrecque, R, and Sirard, M-A (2020a). The age of the bull influences the transcriptome and epigenome of blastocysts produced by IVF. Theriogenology 144, 122–131.
| The age of the bull influences the transcriptome and epigenome of blastocysts produced by IVF.Crossref | GoogleScholarGoogle Scholar | 31951983PubMed |
Wu, C, Blondin, P, Vigneault, C, Labrecque, R, and Sirard, M-A (2020b). Sperm miRNAs-potential mediators of bull age and early embryo development. BMC Genomics 21, 798.
| Sperm miRNAs-potential mediators of bull age and early embryo development.Crossref | GoogleScholarGoogle Scholar | 33198638PubMed |
Zhang, Y, Chaput, C, Fournier, E, Prunier, J, and Sirard, MA (2021). Comparing the whole genome methylation landscape of dairy calf blood cells revealed intergenerational inheritance of the maternal metabolism. Epigenetics 2, 1–10.
| Comparing the whole genome methylation landscape of dairy calf blood cells revealed intergenerational inheritance of the maternal metabolism.Crossref | GoogleScholarGoogle Scholar |
