Mammalian oocyte development depends on the temporally controlled translation of maternal transcripts, particularly in the coordination of meiotic and early embryonic development when transcription has ceased. The translation of mRNA is regulated by various RNA-binding proteins. We show that the absence of cytoplasmic polyadenylation element-binding protein 3 (CPEB3) negatively affects female reproductive fitness. CPEB3-depleted oocytes undergo meiosis normally but experience early embryonic arrest due to a disrupted transcriptome, leading to aberrant protein expression and the subsequent failure of embryonic transcription initiation. We found that CPEB3 stabilizes a subset of mRNAs with a significantly longer 3'UTR that is enriched in its distal region with cytoplasmic polyadenylation elements. Overall, our results suggest that CPEB3 is an important maternal factor that regulates the stability and translation of a subclass of mRNAs that are essential for the initiation of embryonic transcription and thus for embryonic development.

Department of Animal Sciences Genetics Institute University of Florida Gainesville FL 32610 USA

Laboratory of Biochemistry and Molecular Biology of Germ Cells IAPG CAS Rumburska 89 277 21 Libechov Czech Republic

Life Sciences Institute Zhejiang University Hangzhou 310058 China

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Walker M.H., Tobler K.J. StatPearls. StatPearls Publishing; Treasure Island, FL, USA: 2022. [(accessed on 19 December 2022)]. Female Infertility. Available online: http://www.ncbi.nlm.nih.gov/books/NBK556033/

Mtango N.R., Potireddy S., Latham K.E. Oocyte Quality and Maternal Control of Development. Int. Rev. Cell Mol. Biol. 2008;268:223–290. doi: 10.1016/S1937-6448(08)00807-1. PubMed DOI

Pellestor F., Andréo B., Arnal F., Humeau C., Demaille J. Maternal Aging and Chromosomal Abnormalities: New Data Drawn from in Vitro Unfertilized Human Oocytes. Hum. Genet. 2003;112:195–203. doi: 10.1007/s00439-002-0852-x. PubMed DOI

De Vantéry C., Stutz A., Vassalli J.D., Schorderet-Slatkine S. Acquisition of Meiotic Competence in Growing Mouse Oocytes Is Controlled at Both Translational and Posttranslational Levels. Dev. Biol. 1997;187:43–54. doi: 10.1006/DBIO.1997.8599. PubMed DOI

Navot D., Bergh R.A., Williams M.A., Garrisi G.J., Guzman I., Sandler B., Grunfeld L. Poor Oocyte Quality Rather than Implantation Failure as a Cause of Age-Related Decline in Female Fertility. Lancet. 1991;337:1375–1377. doi: 10.1016/0140-6736(91)93060-M. PubMed DOI

De La Fuente R., Viveiros M.M., Burns K.H., Adashi E.Y., Matzuk M.M., Eppig J.J. Major Chromatin Remodeling in the Germinal Vesicle (GV) of Mammalian Oocytes Is Dispensable for Global Transcriptional Silencing but Required for Centromeric Heterochromatin Function. Dev. Biol. 2004;275:447–458. doi: 10.1016/j.ydbio.2004.08.028. PubMed DOI

Clarke H.J. Post-Transcriptional Control of Gene Expression During Mouse Oogenesis. Results Probl. Cell Differ. 2012;55:1–21. doi: 10.1007/978-3-642-30406-4_1. PubMed DOI

Hake L.E., Richter J.D. Translational Regulation of Maternal MRNA. Biochim. Biophys. Acta-Rev. Cancer. 1997;1332:M31–M38. doi: 10.1016/S0304-419X(96)00039-X. PubMed DOI

De Moor C.H., Meijer H., Lissenden S. Mechanisms of Translational Control by the 3′ UTR in Development and Differentiation. Semin. Cell Dev. Biol. 2005;16:49–58. doi: 10.1016/J.SEMCDB.2004.11.007. PubMed DOI

Susor A., Jansova D., Cerna R., Danylevska A., Anger M., Toralova T., Malik R., Supolikova J., Cook M.S., Oh J.S., et al. Temporal and Spatial Regulation of Translation in the Mammalian Oocyte via the MTOR-EIF4F Pathway. Nat. Commun. 2015;6:6078. doi: 10.1038/ncomms7078. PubMed DOI PMC

Richter J.D. Cytoplasmic Polyadenylation in Development and Beyond. Microbiol. Mol. Biol. Rev. 1999;63:446–456. doi: 10.1128/MMBR.63.2.446-456.1999. PubMed DOI PMC

Sha Q.Q., Zhang J., Fan H.Y. A Story of Birth and Death: MRNA Translation and Clearance at the Onset of Maternal-to-Zygotic Transition in Mammals. Biol. Reprod. 2019;101:579–590. doi: 10.1093/BIOLRE/IOZ012. PubMed DOI

Dominguez D., Freese P., Alexis M.S., Su A., Hochman M., Palden T., Bazile C., Lambert N.J., Van Nostrand E.L., Pratt G.A., et al. Sequence, Structure, and Context Preferences of Human RNA Binding Proteins. Mol. Cell. 2018;70:854–867. doi: 10.1016/J.MOLCEL.2018.05.001. PubMed DOI PMC

Hentze M.W., Castello A., Schwarzl T., Preiss T. A Brave New World of RNA-Binding Proteins. Nat. Rev. Mol. Cell Biol. 2018;19:327–341. doi: 10.1038/nrm.2017.130. PubMed DOI

Susor A., Jansova D., Anger M., Kubelka M. Translation in the Mammalian Oocyte in Space and Time. Cell Tissue Res. 2016;363:69–84. doi: 10.1007/s00441-015-2269-6. PubMed DOI

Morgan M., Much C., Digiacomo M., Azzi C., Ivanova I., Vitsios D.M., Pistolic J., Collier P., Moreira P., Benes V., et al. mRNA 3′ Uridylation and Poly(A) Tail Length Sculpt the Mammalian Maternal Transcriptome. Nature. 2017;548:347–351. doi: 10.1038/nature23318. PubMed DOI PMC

Vassalli J.D., Huarte J., Belin D., Gubler P., Vassalli A., O’Connell M.L., Parton L.A., Rickles R.J., Strickland S. Regulated Polyadenylation Controls MRNA Translation during Meiotic Maturation of Mouse Oocytes. Genes Dev. 1989;3:2163–2171. doi: 10.1101/gad.3.12b.2163. PubMed DOI

Stebbins-Boaz B., Hake L.E., Richterl J.D. CPEB Controls the Cytoplasmic Polyadenylation of Cyclin, Cdk2 and c-Mos MRNAs and Is Necessary for Oocyte Maturation in Xenopus. EMBO J. 1996;15:2582–2592. doi: 10.1002/j.1460-2075.1996.tb00616.x. PubMed DOI PMC

Reyes J.M., Ross P.J. Cytoplasmic Polyadenylation in Mammalian Oocyte Maturation. Wiley Interdiscip. Rev. RNA. 2016;7:71–89. doi: 10.1002/WRNA.1316. PubMed DOI

Wickens M. In the Beginning Is the End: Regulation of Poly(A) Addition and Removal during Early Development. Trends Biochem. Sci. 1990;15:320–324. doi: 10.1016/0968-0004(90)90022-4. PubMed DOI

Burns D.M., Richter J.D. CPEB Regulation of Human Cellular Senescence, Energy Metabolism, and P53 MRNA Translation. Genes Dev. 2008;22:3449–3460. doi: 10.1101/gad.1697808. PubMed DOI PMC

Mcgrew L.L., Dworkin-Rastl E., Dworkin M.B., Richter J.D. Poly(A) Elongation during Xenopus Oocyte Maturation Is Required for Translational Recruitment and Is Mediated by a Short Sequence Element. Genes Dev. 1989;3:803–815. doi: 10.1101/gad.3.6.803. PubMed DOI

Yang F., Wang W., Cetinbas M., Sadreyev R.I., Blower M.D. Genome-Wide Analysis Identifies Cis-Acting Elements Regulating MRNA Polyadenylation and Translation during Vertebrate Oocyte Maturation. RNA. 2020;26:324–344. doi: 10.1261/rna.073247.119. PubMed DOI PMC

Kim J.H., Richter J.D. Opposing Polymerase-Deadenylase Activities Regulate Cytoplasmic Polyadenylation. Mol. Cell. 2006;24:173–183. doi: 10.1016/J.MOLCEL.2006.08.016. PubMed DOI

Mendez R., Richter J.D. Translational Control by CPEB: A Means to the End. Nat. Rev. Mol. Cell Biol. 2001;2:521–529. doi: 10.1038/35080081. PubMed DOI

Tay J., Hodgman R., Richter J.D. The Control of Cyclin B1 MRNA Translation during Mouse Oocyte Maturation. Dev. Biol. 2000;221:1–9. doi: 10.1006/dbio.2000.9669. PubMed DOI

Komrskova P., Susor A., Malik R., Prochazkova B., Liskova L., Supolikova J., Hladky S., Kubelka M. Aurora Kinase A Is Not Involved in CPEB1 Phosphorylation and Cyclin B1 MRNA Polyadenylation during Meiotic Maturation of Porcine Oocytes. PLoS ONE. 2014;9:101222. doi: 10.1371/JOURNAL.PONE.0101222. PubMed DOI PMC

Theis M., Si K., Kandel E.R. Two Previously Undescribed Members of the Mouse CPEB Family of Genes and Their Inducible Expression in the Principal Cell Layers of the Hippocampus. Proc. Natl. Acad. Sci. USA. 2003;100:9602. doi: 10.1073/PNAS.1133424100. PubMed DOI PMC

Jansova D., Tetkova A., Koncicka M., Kubelka M., Susor A. Localization of RNA and Translation in the Mammalian Oocyte and Embryo. PLoS ONE. 2018;13:e0192544. doi: 10.1371/journal.pone.0192544. PubMed DOI PMC

Cao L.R., Jiang J.C., Fan H.Y. Positive Feedback Stimulation of Ccnb1 and Mos MRNA Translation by MAPK Cascade during Mouse Oocyte Maturation. Front. Cell Dev. Biol. 2020;8:609430. doi: 10.3389/fcell.2020.609430. PubMed DOI PMC

Chen J., Melton C., Suh N., Oh J.S., Horner K., Xie F., Sette C., Blelloch R., Conti M. Genome-Wide Analysis of Translation Reveals a Critical Role for Deleted in Azoospermia-like (Dazl) at the Oocyte-to-Zygote Transition. Genes Dev. 2011;25:755–766. doi: 10.1101/GAD.2028911. PubMed DOI PMC

Setoyama D., Yamashita M., Sagata N. Mechanism of Degradation of CPEB during Xenopus Oocyte Maturation. Proc. Natl. Acad. Sci. USA. 2007;104:18001–18006. doi: 10.1073/pnas.0706952104. PubMed DOI PMC

Prochazkova B., Komrskova P., Kubelka M. Molecular Sciences CPEB2 Is Necessary for Proper Porcine Meiotic Maturation and Embryonic Development. Int. J. Mol. Sci. 2018;19:3138. doi: 10.3390/ijms19103138. PubMed DOI PMC

Belloc E., Piqué M., Méndez R. Sequential Waves of Polyadenylation and Deadenylation Define a Translation Circuit That Drives Meiotic Progression. Biochem. Soc. Trans. 2008;36:665–670. doi: 10.1042/BST0360665. PubMed DOI

Belloc E., Méndez R. A Deadenylation Negative Feedback Mechanism Governs Meiotic Metaphase Arrest. Nature. 2008;452:1017–1021. doi: 10.1038/nature06809. PubMed DOI

Igea A., Méndez R. Meiosis Requires a Translational Positive Loop Where CPEB1 Ensues Its Replacement by CPEB4. EMBO J. 2010;29:2182–2193. doi: 10.1038/EMBOJ.2010.111. PubMed DOI PMC

Tsai L.Y., Chang Y.W., Lin P.Y., Chou H.J., Liu T.J., Lee P.T., Huang W.H., Tsou Y.L., Huang Y.S. CPEB4 Knockout Mice Exhibit Normal Hippocampus-Related Synaptic Plasticity and Memory. PLoS ONE. 2013;8:84978. doi: 10.1371/JOURNAL.PONE.0084978. PubMed DOI PMC

Wang J., Wu H., Wang X., Zhao X., Sun L., Cheng Y., Jiang X., Li J., Zhang G. CPEB3, an RNA-Binding Protein, Modulates the Behavior of Endometriosis-Derived Stromal Cells via Regulating CXCL12. DNA Cell Biol. 2022;41:606–616. doi: 10.1089/dna.2021.1017. PubMed DOI

Wang Y., Chen C.Z., Fu X.H., Liu J.B., Peng Y.X., Wang Y.J., Han D.X., Zhang Z., Yuan B., Gao Y., et al. CPEB3 Regulates the Proliferation and Apoptosis of Bovine Cumulus Cells. Anim. Sci. J. 2020;91:e13416. doi: 10.1111/ASJ.13416. PubMed DOI

E F., Zhang H., Yin W., Wang C., Liu Y., Li Y., Wang L., Wu Y., Zhang R., Zou C., et al. CPEB3 Deficiency in Mice Affect Ovarian Follicle Development and Causes Premature Ovarian Insufficiency. Cell Death Dis. 2021;13:21. doi: 10.1038/S41419-021-04374-4. PubMed DOI PMC

Boroviak T., Stirparo G.G., Dietmann S., Hernando-Herraez I., Mohammed H., Reik W., Smith A., Sasaki E., Nichols J., Bertone P. Single Cell Transcriptome Analysis of Human, Marmoset and Mouse Embryos Reveals Common and Divergent Features of Preimplantation Development. Development. 2018;145:dev167833. doi: 10.1242/DEV.167833. PubMed DOI PMC

Potireddy S., Vassena R., Patel B.G., Latham K.E. Analysis of Polysomal MRNA Populations of Mouse Oocytes and Zygotes: Dynamic Changes in Maternal MRNA Utilization and Function. Dev. Biol. 2006;298:155–166. doi: 10.1016/J.YDBIO.2006.06.024. PubMed DOI

Tetkova A., Hancova M. Mouse Oocyte Isolation, Cultivation and RNA Microinjection. Bio-Protocol. 2016;6:e1729. doi: 10.21769/bioprotoc.1729. DOI

Masek T., del Llano E., Gahurova L., Kubelka M., Susor A., Roucova K., Lin C.-J., Bruce A.W., Pospisek M. Identifying the Translatome of Mouse NEBD-Stage Oocytes via SSP-Profiling; A Novel Polysome Fractionation Method. Int. J. Mol. Sci. 2020;21:1254. doi: 10.3390/ijms21041254. PubMed DOI PMC

Iyyappan R., Aleshkina D., Ming H., Dvoran M., Kakavand K., Anso Va D.J., Ar Del Llano E., Gahuro V.A.L., Br Uce A.W., Masek T., et al. The Translational Oscillation in Oocyte and Early Embryo Development. Nucleic Acids Res. 2023;51:12076–12091. doi: 10.1093/NAR/GKAD996. PubMed DOI PMC

Sallés F.J., Strickland S. Analysis of Poly(A) Tail Lengths by PCR: The PAT Assay. Methods Mol. Biol. 1999;118:441–448. doi: 10.1385/1-59259-676-2:441. PubMed DOI

Šušor A., Jelínková L., Karabínová P., Torner H., Tomek W., Kovářová H., Kubelka M. Regulation of Cap-Dependent Translation Initiation in the Early Stage Porcine Parthenotes. Mol. Reprod. Dev. 2008;75:1716–1725. doi: 10.1002/mrd.20913. PubMed DOI

Sha Q.Q., Dai X.X., Dang Y., Tang F., Liu J., Zhang Y.L., Fan H.Y. A MAPK Cascade Couples Maternal MRNA Translation and Degradation to Meiotic Cell Cycle Progression in Mouse Oocytes. Development. 2017;144:452–463. doi: 10.1242/dev.144410. PubMed DOI

Lu W.H., Chao H.W., Lin P.Y., Lin S.H., Liu T.H., Chen H.W., Huang Y.S. CPEB3-Dowregulated Nr3c1 MRNA Translation Confers Resilience to Developing Posttraumatic Stress Disorder-like Behavior in Fear-Conditioned Mice. Neuropsychopharmacology. 2021;46:1669–1679. doi: 10.1038/S41386-021-01017-2. PubMed DOI PMC

Huang Y.S., Kan M.C., Lin C.L., Richter J.D. CPEB3 and CPEB4 in Neurons: Analysis of RNA-Binding Specificity and Translational Control of AMPA Receptor GluR2 MRNA. EMBO J. 2006;25:4865–4876. doi: 10.1038/SJ.EMBOJ.7601322. PubMed DOI PMC

Hervás R., del Carmen Fernández-Ramírez M., Galera-Prat A., Suzuki M., Nagai Y., Bruix M., Menéndez M., Laurents D.V., Carrión-Vázquez M. Divergent CPEB Prion-like Domains Reveal Different Assembly Mechanisms for a Generic Amyloid-like Fold. BMC Biol. 2021;19:43. doi: 10.1186/S12915-021-00967-9. PubMed DOI PMC

Fioriti L., Myers C., Huang Y.Y., Li X., Stephan J.S., Trifilieff P., Colnaghi L., Kosmidis S., Drisaldi B., Pavlopoulos E., et al. The Persistence of Hippocampal-Based Memory Requires Protein Synthesis Mediated by the Prion-like Protein CPEB3. Neuron. 2015;86:1433–1448. doi: 10.1016/J.NEURON.2015.05.021. PubMed DOI

Stephan J.S., Fioriti L., Lamba N., Colnaghi L., Karl K., Derkatch I.L., Kandel E.R. The CPEB3 Protein Is a Functional Prion That Interacts with the Actin Cytoskeleton. Cell Rep. 2015;11:1772–1785. doi: 10.1016/J.CELREP.2015.04.060. PubMed DOI

Kageyama S.I., Liu H., Nagata M., Aoki F. The Role of ETS Transcription Factors in Transcription and Development of Mouse Preimplantation Embryos. Biochem. Biophys. Res. Commun. 2006;344:675–679. doi: 10.1016/J.BBRC.2006.03.192. PubMed DOI

Inoue K., Oikawa M., Kamimura S., Ogonuki N., Nakamura T., Nakano T., Abe K., Ogura A. Trichostatin A Specifically Improves the Aberrant Expression of Transcription Factor Genes in Embryos Produced by Somatic Cell Nuclear Transfer. Sci. Rep. 2015;5:10127. doi: 10.1038/SREP10127. PubMed DOI PMC

Zhao Z.H., Meng T.G., Li A., Schatten H., Wang Z.B., Sun Q.Y. RNA-Seq Transcriptome Reveals Different Molecular Responses during Human and Mouse Oocyte Maturation and Fertilization. BMC Genom. 2020;21:475. doi: 10.1186/s12864-020-06885-4. PubMed DOI PMC

Luong X.G., Daldello E.M., Rajkovic G., Yang C.R., Conti M. Genome-Wide Analysis Reveals a Switch in the Translational Program upon Oocyte Meiotic Resumption. Nucleic Acids Res. 2020;48:3257–3276. doi: 10.1093/NAR/GKAA010. PubMed DOI PMC

Pavlopoulos E., Trifilieff P., Chevaleyre V., Fioriti L., Zairis S., Pagano A., Malleret G., Kandel E.R. Neuralized1 Activates CPEB3: A Novel Function of Ubiquitination in Synaptic Plasticity and Memory Storage. Cell. 2011;147:1369–1383. doi: 10.1016/J.CELL.2011.09.056. PubMed DOI PMC

Qu W., Jin H., Chen B.P., Liu J., Li R., Guo W., Tian H. CPEB3 Regulates Neuron-Specific Alternative Splicing and Involves Neurogenesis Gene Expression. Aging (Albany N. Y.) 2020;13:2330–2347. doi: 10.18632/AGING.202259. PubMed DOI PMC

Falco G., Lee S.L., Stanghellini I., Bassey U.C., Hamatani T., Ko M.S.H. Zscan4: A Novel Gene Expressed Exclusively in Late 2-Cell Embryos and Embryonic Stem Cells. Dev. Biol. 2007;307:539–550. doi: 10.1016/J.YDBIO.2007.05.003. PubMed DOI PMC

Ishiguro K.I., Monti M., Akiyama T., Kimura H., Chikazawa-Nohtomi N., Sakota M., Sato S., Redi C.A., Ko S.B.H., Ko M.S.H. Zscan4 Is Expressed Specifically during Late Meiotic Prophase in Both Spermatogenesis and Oogenesis. In Vitro Cell. Dev. Biol. Anim. 2017;53:167–178. doi: 10.1007/S11626-016-0096-Z. PubMed DOI PMC

Smith R., Susor A., Ming H., Tait J., Conti M., Jiang Z., Lin C.-J. The H3.3 Chaperone Hira Complex Orchestrates Oocyte Developmental Competence. Development. 2022;149:dev200044. doi: 10.1242/DEV.200044. PubMed DOI PMC

Davis J.N., McGhee L., Meyers S. The ETO (MTG8) Gene Family. Gene. 2003;303:1–10. doi: 10.1016/S0378-1119(02)01172-1. PubMed DOI

Willcockson M.A., Healton S.E., Weiss C.N., Bartholdy B.A., Botbol Y., Mishra L.N., Sidhwani D.S., Wilson T.J., Pinto H.B., Maron M.I., et al. H1 Histones Control the Epigenetic Landscape by Local Chromatin Compaction. Nature. 2021;589:293–298. doi: 10.1038/S41586-020-3032-Z. PubMed DOI PMC

Wu J., Huang B., Chen H., Yin Q., Liu Y., Xiang Y., Zhang B., Liu B., Wang Q., Xia W., et al. The Landscape of Accessible Chromatin in Mammalian Preimplantation Embryos. Nature. 2016;534:652–657. doi: 10.1038/NATURE18606. PubMed DOI

Chari S., Wilky H., Govindan J., Amodeo A.A. Histone Concentration Regulates the Cell Cycle and Transcription in Early Development. Development. 2019;146:dev177402. doi: 10.1242/dev.177402. PubMed DOI PMC

Pirngruber J., Johnsen S.A. Induced G1 Cell-Cycle Arrest Controls Replication-Dependent Histone MRNA 3′ End Processing through P21, NPAT and CDK9. Oncogene. 2010;29:2853–2863. doi: 10.1038/onc.2010.42. PubMed DOI

Lyons S.M., Cunningham C.H., Welch J.D., Groh B., Guo A.Y., Wei B., Whitfield M.L., Xiong Y., Marzluff W.F. A Subset of Replication-Dependent Histone MRNAs Are Expressed as Polyadenylated RNAs in Terminally Differentiated Tissues. Nucleic Acids Res. 2016;44:9190–9205. doi: 10.1093/NAR/GKW620. PubMed DOI PMC

Alizadeh Z., Kageyama S.I., Aoki F. Degradation of Maternal MRNA in Mouse Embryos: Selective Degradation of Specific MRNAs after Fertilization. Mol. Reprod. Dev. 2005;72:281–290. doi: 10.1002/MRD.20340. PubMed DOI

Yu C., Ji S.Y., Sha Q.Q., Dang Y., Zhou J.J., Zhang Y.L., Liu Y., Wang Z.W., Hu B., Sun Q.Y., et al. BTG4 Is a Meiotic Cell Cycle–Coupled Maternal-Zygotic-Transition Licensing Factor in Oocytes. Nat. Struct. Mol. Biol. 2016;23:387–394. doi: 10.1038/nsmb.3204. PubMed DOI

Hosoda N., Funakoshi Y., Hirasawa M., Yamagishi R., Asano Y., Miyagawa R., Ogami K., Tsujimoto M., Hoshino S.I. Anti-Proliferative Protein Tob Negatively Regulates CPEB3 Target by Recruiting Caf1 Deadenylase. EMBO J. 2011;30:13111323. doi: 10.1038/EMBOJ.2011.37. PubMed DOI PMC

Jiang J.C., Zhang H., Cao L.R., Dai X.X., Zhao L.W., Liu H.B., Fan H.Y. Oocyte Meiosis-Coupled Poly(A) Polymerase α Phosphorylation and Activation Trigger Maternal MRNA Translation in Mice. Nucleic Acids Res. 2021;49:5867–5880. doi: 10.1093/NAR/GKAB431. PubMed DOI PMC

Zhang H., Lee J.Y., Tian B. Biased Alternative Polyadenylation in Human Tissues. Genome Biol. 2005;6:R100. doi: 10.1186/GB-2005-6-12-R100. PubMed DOI PMC

Liu D., Brockman J.M., Dass B., Hutchins L.N., Singh P., McCarrey J.R., MacDonald C.C., Graber J.H. Systematic Variation in MRNA 3’-Processing Signals during Mouse Spermatogenesis. Nucleic Acids Res. 2007;35:234–246. doi: 10.1093/NAR/GKL919. PubMed DOI PMC

Zhang Y., Shen L., Shi Q., Zhao G., Wang F. Comprehensive Analysis of APA Events and Their Association with Tumor Microenvironment in Lung Adenocarcinoma. Front. Genet. 2021;12:645360. doi: 10.3389/fgene.2021.645360. PubMed DOI PMC

Liu Y., Zhao H., Shao F., Zhang Y., Nie H., Zhang J., Li C., Hou Z., Chen Z.J., Wang J., et al. Remodeling of Maternal MRNA through Poly(A) Tail Orchestrates Human Oocyte-to-Embryo Transition. Nat. Struct. Mol. Biol. 2023;30:200–215. doi: 10.1038/S41594-022-00908-2. PubMed DOI PMC

Aoki F., Hara K.T., Schultz R.M. Acquisition of Transcriptional Competence in the 1-Cell Mouse Embryo: Requirement for Recruitment of Maternal MRNAs. Mol. Reprod. Dev. 2003;64:270–274. doi: 10.1002/MRD.10227. PubMed DOI

Absence of CDK12 in oocyte leads to female infertility

Spatiotemporal dynamics and selectivity of mRNA translation during mouse pre-implantation development