{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,22]],"date-time":"2026-09-22T19:36:30Z","timestamp":1790105790086,"version":"4.0.1"},"reference-count":57,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2022,12,30]],"date-time":"2022-12-30T00:00:00Z","timestamp":1672358400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000002","name":"NIH","doi-asserted-by":"publisher","award":["R01HD038082"],"award-info":[{"award-number":["R01HD038082"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"NIH","doi-asserted-by":"publisher","award":["R01HD088571"],"award-info":[{"award-number":["R01HD088571"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"NIH","doi-asserted-by":"publisher","award":["R01HD080224"],"award-info":[{"award-number":["R01HD080224"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"NIH","doi-asserted-by":"publisher","award":["T32 GM108556"],"award-info":[{"award-number":["T32 GM108556"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"NIH","doi-asserted-by":"publisher","award":["R01HD038082"],"award-info":[{"award-number":["R01HD038082"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"NIH","doi-asserted-by":"publisher","award":["R01HD088571"],"award-info":[{"award-number":["R01HD088571"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"NIH","doi-asserted-by":"publisher","award":["R01HD080224"],"award-info":[{"award-number":["R01HD080224"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"NIH","doi-asserted-by":"publisher","award":["T32 GM108556"],"award-info":[{"award-number":["T32 GM108556"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"NIH","doi-asserted-by":"publisher","award":["R01HD038082"],"award-info":[{"award-number":["R01HD038082"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"NIH","doi-asserted-by":"publisher","award":["R01HD088571"],"award-info":[{"award-number":["R01HD088571"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"NIH","doi-asserted-by":"publisher","award":["R01HD080224"],"award-info":[{"award-number":["R01HD080224"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"NIH","doi-asserted-by":"publisher","award":["T32 GM108556"],"award-info":[{"award-number":["T32 GM108556"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"name":"NIH","award":["R01HD038082"],"award-info":[{"award-number":["R01HD038082"]}]},{"name":"NIH","award":["R01HD088571"],"award-info":[{"award-number":["R01HD088571"]}]},{"name":"NIH","award":["R01HD080224"],"award-info":[{"award-number":["R01HD080224"]}]},{"name":"NIH","award":["T32 GM108556"],"award-info":[{"award-number":["T32 GM108556"]}]},{"name":"UMass Faculty Research Grant\/Endowment Healey Grant","award":["R01HD038082"],"award-info":[{"award-number":["R01HD038082"]}]},{"name":"UMass Faculty Research Grant\/Endowment Healey Grant","award":["R01HD088571"],"award-info":[{"award-number":["R01HD088571"]}]},{"name":"UMass Faculty Research Grant\/Endowment Healey Grant","award":["R01HD080224"],"award-info":[{"award-number":["R01HD080224"]}]},{"name":"UMass Faculty Research Grant\/Endowment Healey Grant","award":["T32 GM108556"],"award-info":[{"award-number":["T32 GM108556"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>The sperm energy restriction and recovery (SER) treatment developed in our laboratory was shown to improve fertilization and blastocyst development following in vitro fertilization (IVF) in mice. Here, we investigated the effects of SER on early embryogenesis. Developmental events observed during the first cell cycle indicated that progression through the pronuclear stages of SER-generated embryos is advanced in comparison with control-generated embryos. These findings prompted further analysis of potential effects of SER on pronuclear chromatin dynamics, focusing on the key H3K4me3 and H3K27ac histone modifications. Nearly all the SER-generated embryos displayed H3K4me3 in the male pronuclei at 12 h post-insemination (HPI), while a subset of the control-generated embryos did not. Additionally, SER-generated embryos displayed a more homogenous intensity of H3K27ac at 8 and 12 HPI compared to control embryos. These changes in histone modifications during the first cell cycle were accompanied by differences in gene expression at the two-cell stage; both of these changes in early embryos could potentially play a role in the improved developmental outcomes of these embryos later in development. Our results indicate that sperm incubation conditions have an impact on early embryo development and can be useful for the improvement of assisted reproductive technology outcomes.<\/jats:p>","DOI":"10.3390\/ijms24010640","type":"journal-article","created":{"date-parts":[[2022,12,30]],"date-time":"2022-12-30T03:31:17Z","timestamp":1672371077000},"page":"640","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":7,"title":["Sperm Energy Restriction and Recovery (SER) Alters Epigenetic Marks during the First Cell Cycle of Development in Mice"],"prefix":"10.3390","volume":"24","author":[{"given":"Darya A.","family":"Tourzani","sequence":"first","affiliation":[{"name":"Department of Veterinary and Animal Sciences, Integrated Sciences Building, University of Massachusetts, Amherst, MA 01003, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qiangzong","family":"Yin","sequence":"additional","affiliation":[{"name":"Department of Biochemistry and Molecular Biotechnology, University of Massachusetts Chan Medical School, Worcester, MA 01605, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Erica A.","family":"Jackson","sequence":"additional","affiliation":[{"name":"Department of Veterinary and Animal Sciences, Integrated Sciences Building, University of Massachusetts, Amherst, MA 01003, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Oliver J.","family":"Rando","sequence":"additional","affiliation":[{"name":"Department of Biochemistry and Molecular Biotechnology, University of Massachusetts Chan Medical School, Worcester, MA 01605, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pablo E.","family":"Visconti","sequence":"additional","affiliation":[{"name":"Department of Veterinary and Animal Sciences, Integrated Sciences Building, University of Massachusetts, Amherst, MA 01003, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5468-2700","authenticated-orcid":false,"given":"Maria G.","family":"Gervasi","sequence":"additional","affiliation":[{"name":"Department of Veterinary and Animal Sciences, Integrated Sciences Building, University of Massachusetts, Amherst, MA 01003, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,12,30]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"797","DOI":"10.1042\/BST20170493","article-title":"Regulation of the meiotic divisions of mammalian oocytes and eggs","volume":"46","author":"Sanders","year":"2018","journal-title":"Biochem. Soc. Trans."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"992","DOI":"10.1095\/biolreprod.104.036244","article-title":"Transgenic RNA interference reveals role for mouse sperm phospholipase Czeta in triggering Ca2+ oscillations during fertilization","volume":"72","author":"Knott","year":"2005","journal-title":"Biol. Reprod."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"3533","DOI":"10.1242\/dev.129.15.3533","article-title":"PLC zeta: A sperm-specific trigger of Ca2+ oscillations in eggs and embryo development","volume":"129","author":"Saunders","year":"2002","journal-title":"Development"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1016\/j.ydbio.2007.12.012","article-title":"The roles of Ca2+, downstream protein kinases, and oscillatory signaling in regulating fertilization and the activation of development","volume":"315","author":"Ducibella","year":"2008","journal-title":"Dev. Biol."},{"key":"ref_5","first-page":"1","article-title":"Paternal contributions to the mammalian zygote: Fertilization after sperm\u2014Egg fusion","volume":"195","author":"Sutovsky","year":"2000","journal-title":"Int. Rev. Cytol."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Scheffler, K., Uraji, J., Jentoft, I., Cavazza, T., Monnich, E., Mogessie, B., and Schuh, M. (2021). Two mechanisms drive pronuclear migration in mouse zygotes. Nat. Commun., 12.","DOI":"10.1038\/s41467-021-21020-x"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1016\/S0074-7696(08)60544-6","article-title":"Fertilization of mammalian eggs in vitro","volume":"12","author":"Austin","year":"1961","journal-title":"Int. Rev. Cytol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"200","DOI":"10.1002\/rmb2.12032","article-title":"Potential of zygotes to produce live births can be identified by the size of the male and female pronuclei just before their membranes break down","volume":"16","author":"Otsuki","year":"2017","journal-title":"Reprod. Med. Biol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"919","DOI":"10.1016\/j.mam.2013.01.003","article-title":"The maternal to zygotic transition in mammals","volume":"34","author":"Li","year":"2013","journal-title":"Mol. Aspects Med."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"E6780","DOI":"10.1073\/pnas.1804309115","article-title":"Minor zygotic gene activation is essential for mouse preimplantation development","volume":"115","author":"Abe","year":"2018","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"296","DOI":"10.1006\/dbio.1996.8466","article-title":"Regulation of transcriptional activity during the first and second cell cycles in the preimplantation mouse embryo","volume":"181","author":"Aoki","year":"1997","journal-title":"Dev. Biol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1016\/j.stem.2021.11.012","article-title":"Human embryonic genome activation initiates at the one-cell stage","volume":"29","author":"Asami","year":"2021","journal-title":"Cell Stem Cell"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"436","DOI":"10.1038\/s41580-018-0008-z","article-title":"Dynamics of the epigenetic landscape during the maternal-to-zygotic transition","volume":"19","author":"Reik","year":"2018","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Gamarra, N., and Narlikar, G.J. (2021). Collaboration through chromatin: Motors of transcription and chromatin structure. J. Mol. Biol., 433.","DOI":"10.1016\/j.jmb.2021.166876"},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Marcho, C., Cui, W., and Mager, J. (2015). Epigenetic dynamics during preimplantation development. Reproduction, 150.","DOI":"10.1530\/REP-15-0180"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"662","DOI":"10.1038\/nrg887","article-title":"Chromatin modification and epigenetic reprogramming in mammalian development","volume":"3","author":"Li","year":"2002","journal-title":"Nat. Rev. Genet."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"4615","DOI":"10.1242\/dev.124.22.4615","article-title":"Differential H4 acetylation of paternal and maternal chromatin precedes DNA replication and differential transcriptional activity in pronuclei of 1-cell mouse embryos","volume":"124","author":"Adenot","year":"1997","journal-title":"Development"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"823","DOI":"10.1016\/j.cell.2007.05.009","article-title":"High-resolution profiling of histone methylations in the human genome","volume":"129","author":"Barski","year":"2007","journal-title":"Cell"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1099","DOI":"10.4238\/2012.April.27.9","article-title":"Differences in H3K4 trimethylation in in vivo and in vitro fertilization mouse preimplantation embryos","volume":"11","author":"Wu","year":"2012","journal-title":"Genet. Mol. Res."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1659","DOI":"10.1016\/j.theriogenology.2006.01.038","article-title":"In vitro development of domestic cat embryos following intra-cytoplasmic sperm injection with testicular spermatozoa","volume":"66","author":"Comizzoli","year":"2006","journal-title":"Theriogenology"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"551","DOI":"10.1007\/s10815-018-1136-2","article-title":"The mutual benefits of research in wild animal species and human-assisted reproduction","volume":"35","author":"Comizzoli","year":"2018","journal-title":"J. Assist. Reprod. Genet."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1016\/S1472-6483(10)60769-9","article-title":"High rate of biological loss in assisted reproduction: It is in the seed, not in the soil","volume":"14","author":"Patrizio","year":"2007","journal-title":"Reprod. Biomed. Online"},{"key":"ref_23","unstructured":"Centers for Disease Control and Prevention (2021). Assisted Reproductive Technology Fertility Clinic and National Summary Report, US Department of Health and Human Services."},{"key":"ref_24","unstructured":"European IVF Monitoring Consortium (EIM), for the European Society of Human Reproduction and Embryology (ESHRE) (2022). ART in Europe, 2018: Results generated from European registries by ESHRE. Hum. Reprod. Open, 2022."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Navarrete, F.A., Aguila, L., Martin-Hidalgo, D., Tourzani, D.A., Luque, G.M., Ardestani, G., Garcia-Vazquez, F.A., Levin, L.R., Buck, J., and Darszon, A. (2019). Transient Sperm Starvation Improves the Outcome of Assisted Reproductive Technologies. Front. Cell Dev. Biol., 7.","DOI":"10.3389\/fcell.2019.00262"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Sanchez-Cardenas, C., Romarowski, A., Orta, G., De la Vega-Beltran, J.L., Martin-Hidalgo, D., Hernandez-Cruz, A., Visconti, P.E., and Darszon, A. (2021). Starvation induces an increase in intracellular calcium and potentiates the progesterone-induced mouse sperm acrosome reaction. FASEB J., 35.","DOI":"10.1096\/fj.202100122R"},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Yang, F., Gracia Gervasi, M., Orta, G., Tourzani, D.A., De la Vega-Beltran, J.L., Ruthel, G., Darszon, A., Visconti, P.E., and Wang, P.J. (2022). C2CD6 regulates targeting and organization of the CatSper calcium channel complex in sperm flagella. Development, 149.","DOI":"10.1242\/dev.199988"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"2860","DOI":"10.1016\/j.cell.2021.04.013","article-title":"Parental genome unification is highly error-prone in mammalian embryos","volume":"184","author":"Cavazza","year":"2021","journal-title":"Cell"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"548","DOI":"10.1038\/nature19360","article-title":"Broad histone H3K4me3 domains in mouse oocytes modulate maternal-to-zygotic transition","volume":"537","author":"Dahl","year":"2016","journal-title":"Nature"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"535","DOI":"10.1093\/humupd\/dmy017","article-title":"The contribution of human sperm proteins to the development and epigenome of the preimplantation embryo","volume":"24","author":"Castillo","year":"2018","journal-title":"Hum. Reprod. Update"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Sharma, U. (2019). Paternal Contributions to Offspring Health: Role of Sperm Small RNAs in Intergenerational Transmission of Epigenetic Information. Front. Cell Dev. Biol., 7.","DOI":"10.3389\/fcell.2019.00215"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1016\/j.molcel.2019.04.014","article-title":"Maintenance of CTCF- and Transcription Factor-Mediated Interactions from the Gametes to the Early Mouse Embryo","volume":"75","author":"Jung","year":"2019","journal-title":"Mol. Cell"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1126\/science.aar7462","article-title":"Dual-spindle formation in zygotes keeps parental genomes apart in early mammalian embryos","volume":"361","author":"Reichmann","year":"2018","journal-title":"Science"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1530\/rep.0.1250133","article-title":"Effect of sperm preparation method on in vitro fertilization in pigs","volume":"125","author":"Matas","year":"2003","journal-title":"Reproduction"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Tesarik, J. (2022). Control of Maternal-to-Zygotic Transition in Human Embryos and Other Animal Species (Especially Mouse): Similarities and Differences. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23158562"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"625","DOI":"10.1530\/rep.0.1250625","article-title":"Remodelling the paternal chromatin at fertilization in mammals","volume":"125","author":"McLay","year":"2003","journal-title":"Reproduction"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1523","DOI":"10.15252\/embj.201490648","article-title":"The first murine zygotic transcription is promiscuous and uncoupled from splicing and 3\u2019 processing","volume":"34","author":"Abe","year":"2015","journal-title":"EMBO J."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1016\/0012-1606(91)90298-H","article-title":"Regulation of gene expression in preimplantation mouse embryos: Effects of the zygotic clock and the first mitosis on promoter and enhancer activities","volume":"147","author":"Wiekowski","year":"1991","journal-title":"Dev. Biol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1131","DOI":"10.1002\/j.1460-2075.1993.tb05754.x","article-title":"Analysis of gene expression in mouse preimplantation embryos demonstrates that the primary role of enhancers is to relieve repression of promoters","volume":"12","author":"Majumder","year":"1993","journal-title":"EMBO J."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1262\/jrd.2017-058","article-title":"Regulation of zygotic gene activation by chromatin structure and epigenetic factors","volume":"63","author":"Funaya","year":"2017","journal-title":"J. Reprod. Dev."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1016\/j.ydbio.2005.01.025","article-title":"Dynamic chromatin modifications characterise the first cell cycle in mouse embryos","volume":"280","author":"Santos","year":"2005","journal-title":"Dev. Biol."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Igolkina, A.A., Zinkevich, A., Karandasheva, K.O., Popov, A.A., Selifanova, M.V., Nikolaeva, D., Tkachev, V., Penzar, D., Nikitin, D.M., and Buzdin, A. (2019). H3K4me3, H3K9ac, H3K27ac, H3K27me3 and H3K9me3 Histone Tags Suggest Distinct Regulatory Evolution of Open and Condensed Chromatin Landmarks. Cells, 8.","DOI":"10.3390\/cells8091034"},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Lepikhov, K., and Walter, J. (2004). Differential dynamics of histone H3 methylation at positions K4 and K9 in the mouse zygote. BMC Dev. Biol., 4.","DOI":"10.1186\/1471-213X-4-12"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"553","DOI":"10.1038\/nature19361","article-title":"Allelic reprogramming of the histone modification H3K4me3 in early mammalian development","volume":"537","author":"Zhang","year":"2016","journal-title":"Nature"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"575","DOI":"10.1017\/S0967199417000405","article-title":"Acetylation and methylation profiles of H3K27 in porcine embryos cultured in vitro","volume":"25","author":"Marinho","year":"2017","journal-title":"Zygote"},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Kang, M.H., You, S.Y., Hong, K., and Kim, J.H. (2020). DMSO impairs the transcriptional program for maternal-to-embryonic transition by altering histone acetylation. Biomaterials, 230.","DOI":"10.1016\/j.biomaterials.2019.119604"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1262\/jrd.2017-127","article-title":"Ubiquitin-proteasome system modulates zygotic genome activation in early mouse embryos and influences full-term development","volume":"64","author":"Higuchi","year":"2018","journal-title":"J. Reprod. Dev."},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Navarrete, F.A., Alvau, A., Lee, H.C., Levin, L.R., Buck, J., Leon, P.M., Santi, C.M., Krapf, D., Mager, J., and Fissore, R.A. (2016). Transient exposure to calcium ionophore enables in vitro fertilization in sterile mouse models. Sci. Rep., 6.","DOI":"10.1038\/srep33589"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"470","DOI":"10.1016\/j.devcel.2018.06.024","article-title":"Small RNAs Gained during Epididymal Transit of Sperm Are Essential for Embryonic Development in Mice","volume":"46","author":"Conine","year":"2018","journal-title":"Dev. Cell"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1126\/science.aad6780","article-title":"Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals","volume":"351","author":"Sharma","year":"2016","journal-title":"Science"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1366","DOI":"10.1016\/j.celrep.2017.01.034","article-title":"Chromatin States in Mouse Sperm Correlate with Embryonic and Adult Regulatory Landscapes","volume":"18","author":"Jung","year":"2017","journal-title":"Cell. Rep."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"708","DOI":"10.1038\/s41587-020-0497-0","article-title":"Single-cell RNA counting at allele and isoform resolution using Smart-seq3","volume":"38","author":"Ziegenhain","year":"2020","journal-title":"Nat. Biotechnol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"491","DOI":"10.1101\/gr.209601.116","article-title":"UMI-tools: Modeling sequencing errors in Unique Molecular Identifiers to improve quantification accuracy","volume":"27","author":"Smith","year":"2017","journal-title":"Genome Res."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1093\/bioinformatics\/bts635","article-title":"STAR: Ultrafast universal RNA-seq aligner","volume":"29","author":"Dobin","year":"2013","journal-title":"Bioinformatics"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"923","DOI":"10.1093\/bioinformatics\/btt656","article-title":"featureCounts: An efficient general purpose program for assigning sequence reads to genomic features","volume":"30","author":"Liao","year":"2014","journal-title":"Bioinformatics"},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Zhang, Y., Parmigiani, G., and Johnson, W.E. (2020). ComBat-seq: Batch effect adjustment for RNA-seq count data. NAR Genom. Bioinform., 2.","DOI":"10.1093\/nargab\/lqaa078"},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"Love, M.I., Huber, W., and Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol., 15.","DOI":"10.1186\/s13059-014-0550-8"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/1\/640\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T01:56:12Z","timestamp":1760147772000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/1\/640"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,12,30]]},"references-count":57,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2023,1]]}},"alternative-id":["ijms24010640"],"URL":"https:\/\/doi.org\/10.3390\/ijms24010640","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,12,30]]}}}