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Oosit olgunlaşması ve embriyo gelişimi sırasında PATL2 transkript düzeylerinin zamansal düzenlenmesi: Bir silico analizi

Year 2025, Volume: 8 Issue: 3, 263 - 270, 22.10.2025
https://doi.org/10.53446/actamednicomedia.1634724

Abstract

Amaç: Kadın kısırlığı üreme sisteminin nispeten sık görülen bir bozukluğudur ve moleküler etiyolojisi ve ilişkili hücresel mekanizmaları henüz açıklanamamıştır. PATL2'deki belirli mutasyonların, oosit olgunlaşmasının durması ve oosit meiotik eksikliği ile karakterize edilen kadın kısırlığına yol açtığı belirlenmiştir. PATL2, oosit olgunlaşmasında translasyonel baskılayıcı olarak işlev gören bir RNA bağlayıcı protein kodlar; bu nedenle, PATL2 ekspresyonunun uygun zamansal kontrolünün normal oosit olgunlaşması için elzem olduğu ileri sürülmüştür.
Yöntem: Bu çalışmada, R programlama dilini kullanarak, farelerde oosit olgunlaşması ve embriyo gelişimi sırasında PATL2 transkript seviyelerinin zamansal düzenlenmesini analiz etmek için transkriptomik verileri kullanılmıştır.
Bulgular: Fare oositlerinde PATL2 geninin mRNA ekspresyonunun primordial folikül aşamasından birincil folikül aşamasına kadar arttığı ve ekspresyonunun birincil ve ikincil folikül aşamalarında yüksek kaldığı, ardından antral folikül aşamalarında (üçüncül folikül aşaması) azaldığı gösterilmiştir. Ayrıca, farelerde PATL2 ekspresyonunun metafaz 2 (MII) aşamasındaki oositlerde germinal vezikül (GV) aşamasındaki oositlere kıyasla daha düşük olduğu ve PATL2 transkript seviyelerinin embriyo gelişimi sırasında bile değiştiği bulunmuştur.
Sonuç: Mevcut çalışmadaki veriler, oosit büyümesi sırasında PATL2 ekspresyonunun transkripsiyon seviyesinde zamansal olarak düzenlendiğini ve protein seviyesinde gerçekleştirilen önceki araştırmaları desteklediğini göstermektedir. PATL2'nin oosit matürasyon durması ve dişi kısırlığındaki önemi ve tanımlanan PATL2 patojenik varyantlarının sayısı göz önüne alındığında, oositlerde transkripsiyonel seviyede PATL2 regülasyonunun daha iyi bir mekanistik anlayışı klinik öneme sahip olabilir ve yeni tedavi stratejilerinin geliştirilmesine rehberlik edebilir.

References

  • Maddirevula S, Coskun S, Alhassan S, Elnour A, Alsaif HS, Ibrahim N, et al. Female Infertility Caused by Mutations in the Oocyte-Specific Translational Repressor PATL2. Am J Hum Genet. 2017;101(4):603-608. doi: 10.1016/j.ajhg. 2017.08.009.
  • Chen B, Zhang Z, Sun X, Kuang Y, Mao X, Wang X, et al. Biallelic Mutations in PATL2 Cause Female Infertility Characterized by Oocyte Maturation Arrest. Am J Hum Genet. 2017;101(4):609-615. doi: 10.1016/j.ajhg.2017.08. 018.
  • Christou-Kent M, Kherraf ZE, Amiri-Yekta A, Le Blévec E, Karaouzène T, Conne B, et al. PATL2 is a key actor of oocyte maturation whose invalidation causes infertility in women and mice. EMBO Mol Med. 2018;10(5):e8515. doi: 10.15252/emmm.201708515.
  • Huang L, Tong X, Wang F, Luo L, Jin R, Fu Y, et al. Novel mutations in PATL2 cause female infertility with oocyte germinal vesicle arrest. Hum Reprod. 2018;33(6):1183-1190. doi: 10.1093/humrep/dey100.
  • Christou-Kent M, Ray PF, Arnoult C. Échec de maturation ovocytaire - Un rôle essentiel pour la protéine PATL2 dans l’ovogenèse [Oocyte maturation failure: an essential role for the protein PATL2 in human oogenesis]. Med Sci (Paris). 2018;34(12):1042-1045. French. doi: 10.1051/ medsci/2018287.
  • Wu L, Chen H, Li D, Song D, Chen B, Yan Z, et al. Novel mutations in PATL2: expanding the mutational spectrum and corresponding phenotypic variability associated with female infertility. J Hum Genet. 2019;64(5):379-385. doi: 10.1038/s10038-019-0568-6.
  • Liu Z, Zhu L, Wang J, Luo G, Xi Q, Zhou X, et al. Novel homozygous mutations in PATL2 lead to female infertility with oocyte maturation arrest. J Assist Reprod Genet. 2020;37(4):841-847. doi: 10.1007/s10815-020-01698-6.
  • Cao Q, Zhao C, Wang C, Cai L, Xia M, Zhang X, et al. The Recurrent Mutation in PATL2 Inhibits Its Degradation Thus Causing Female Infertility Characterized by Oocyte Maturation Defect Through Regulation of the Mos-MAPK Pathway. Front Cell Dev Biol. 2021;9:628649. doi: 10.3389/ fcell.2021.628649.
  • Sang Q, Zhou Z, Mu J, Wang L. Genetic factors as potential molecular markers of human oocyte and embryo quality. J Assist Reprod Genet. 2021;38(5):993-1002. doi: 10.1007/s10815-021-02196-z.
  • Peng SL, Wu QF, Xie Q, Tan J, Shu KY. PATL2 regulated the apoptosis of ovarian granulosa cells in patients with PCOS. Gynecol Endocrinol. 2021;37(7):629-634. doi: 10.1080/ 09513590.2021.1928066.
  • Huang L, Wang Y, Lu F, Jin Q, Song G, Ji J, et al. Novel mutations in NLRP5 and PATL2 cause female infertility characterized by primarily oocyte maturation abnormality and consequent early embryonic arrest. J Assist Reprod Genet. 2022;39(3):711-718. doi: 10.1007/s10815-022-02412-4.
  • Huo M, Zhang Y, Shi S, Shi H, Liu Y, Zhang L, et al. Gene Spectrum and Clinical Traits of Nine Patients With Oocyte Maturation Arrest. Front Genet. 2022;13:772143. doi: 10.3389/fgene.2022.772143.
  • Xue N, Wang Y, Xu X, Jiang X, Li C, Wang J, et al. Establishment of pluripotent stem cell line induced by PATL2 heterozygous mutation in patients with oocyte maturation defect-4. Stem Cell Res. 2022;61:102776. doi: 10.1016/j.scr.2022.102776.
  • Loeuillet C, Dhellemmes M, Cazin C, Kherraf ZE, Fourati Ben Mustapha S, Zouari R, et al. A recurrent ZP1 variant is responsible for oocyte maturation defect with degenerated oocytes in infertile females. Clin Genet. 2022;102(1):22-29. doi: 10.1111/cge.14144.
  • Capalbo A, Buonaiuto S, Figliuzzi M, Damaggio G, Girardi L, Caroselli S, et al. Maternal exome analysis for the diagnosis of oocyte maturation defects and early embryonic developmental arrest. Reprod Biomed Online. 2022;45(3):508-518. doi: 10.1016/j.rbmo.2022.05.009.
  • Lei Q, Li J, Zhou X, Zhang W. [Oocyte maturation arrest due to compound heterozygous variants of the PATL2 gene in a case]. Zhonghua Yi Xue Yi Chuan Xue Za Zhi. 2022;39(7):759-762. Chinese. doi: 10.3760/cma.j. cn511374-20210316-00234.
  • Sun L, Tong K, Liu W, Tian Y, Yang S, Zhou D, et al. Identification and characterization of a novel homozygous splice site variant of PATL2 causing female infertility due to oocyte germinal vesicle arrest. Front Genet. 2022;13:967288. doi: 10.3389/fgene.2022.967288.
  • Zhu L, Yang Q, Jin H, Zhou J, Wang M, Yang L, et al. Oocyte phenotype, genetic diagnosis, and clinical outcome in case of patients with oocyte maturation arrest. Front Endocrinol (Lausanne). 2022;13:1016563. doi: 10.3389/ fendo.2022.1016563.
  • Campos G, Sciorio R, Esteves SC. Total fertilization failure after ICSI: insights into pathophysiology, diagnosis, and management through artificial oocyte activation. Hum Reprod Update. 2023;29(4):369-394. doi: 10.1093/ humupd/dmad007. PMID: 36977357.
  • Torra-Massana M, Rodríguez A, Vassena R. Exonic genetic variants associated with unexpected fertilization failure and zygotic arrest after ICSI: a systematic review. Zygote. 2023;31(4):316-341. doi: 10.1017/S096719942300014X.
  • Zhang Z, Liu R, Zhou H, Li Q, Qu R, Wang W, et al. PATL2 regulates mRNA homeostasis in oocytes by interacting with EIF4E and CPEB1. Development. 2023;150(12): dev201572. doi: 10.1242/dev.201572.
  • Zhou H, Cai YL, Luo Q, Zou L, Yin YX, Chen Y, et al. High carrier frequency of pathogenic PATL2 gene mutations predicted in population: a bioinformatics-based approach. Front Genet. 2023 May;14:1097951. doi: 10.3389/ fgene.2023.1097951.
  • Lv XJ, Guo J, Lin G. Novel mutations in TRIP13 lead to female infertility with oocyte maturation arrest. Yi Chuan. 2023;45(6):514-525. doi: 10.16288/j.yczz.23-022.
  • Ye Z, Li D, Niu X, Yang A, Pan Z, Yu R, et al. Identification novel mutations and phenotypic spectrum expanding in PATL2 in infertile women with IVF/ICSI failure. J Assist Reprod Genet. 2024;41(5):1233-1243. doi: 10.1007/ s10815-024-03071-3.
  • Hu HY, Zhang GH, Deng WF, Wei TY, Feng ZK, et al. Novel PATL2 variants cause female infertility with oocyte maturation defect. J Assist Reprod Genet. 2024. doi: 10.1007/s10815-024-03150-5.
  • Wan LB, Pan H, Hannenhalli S, Cheng Y, Ma J, Fedoriw A, et al. Maternal depletion of CTCF reveals multiple functions during oocyte and preimplantation embryo development. Development. 2008;135(16):2729-38. doi: 10.1242/ dev.024539.
  • Mitchell LE. Maternal effect genes: Update and review of evidence for a link with birth defects. HGG Adv. 2021;3(1):100067. doi: 10.1016/j.xhgg.2021.100067.
  • Musfee FI, Oluwafemi OO, Agopian AJ, Hakonarson H, Goldmuntz E, Mitchell LE. Maternal effect genes as risk factors for congenital heart defects. HGG Adv. 2022;3(2):100098. doi: 10.1016/j.xhgg.2022.100098.
  • Pan H, O'brien MJ, Wigglesworth K, Eppig JJ, Schultz RM. Transcript profiling during mouse oocyte development and the effect of gonadotropin priming and development in vitro. Dev Biol. 2005;286(2):493-506. doi: 10.1016/j.ydbio. 2005.08.023.
  • Pan H, Ma P, Zhu W, Schultz RM. Age-associated increase in aneuploidy and changes in gene expression in mouse eggs. Dev Biol. 2008;316(2):397-407. doi: 10.1016/j.ydbio. 2008.01.048.
  • Barrett T, Wilhite SE, Ledoux P, Evangelista C, Kim IF, Tomashevsky M, et al. NCBI GEO: archive for functional genomics data sets--update. Nucleic Acids Res. 2013;41(Database issue):D991-5. doi: 10.1093/nar/ gks1193.
  • Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002;30(1):207-10. doi: 10.1093/nar/30.1.207.
  • R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2022. URL https://www.R-project.org/.
  • Wickham H, Bryan J. _readxl: Read Excel Files_. R package version 1.4.2, 2023. <https://CRAN.R-project.org /package=readxl>.
  • Wickham H, Averick M, Bryan J, Chang W, McGowan LD, François R, et al. “Welcome to the tidyverse.” J of Open Source Software_, 2019;4(43):1686. doi:10.21105/joss. 01686 <https://doi.org/10.21105/joss.01686>.
  • Kassambara A. _ggpubr: 'ggplot2' Based Publication Ready Plots_. R package version 0.6.0. 2023. <https://CRAN.R-project.org/package=ggpubr>.
  • Xie Y. knitr: A General-Purpose Package for Dynamic Report Generation in R. R package version 1.42. 2023.
  • Allaire J, Xie Y, Dervieux C, McPherson J, Luraschi J, Ushey K, et al. _rmarkdown: Dynamic Documents for R_. R package version 2.21. 2023. <https://github.com/rstudio /rmarkdown>.
  • Berkel C, Cacan E. Lower expression of NINJ1 (Ninjurin 1), a mediator of plasma membrane rupture, is associated with advanced disease and worse prognosis in serous ovarian cancer. Immunol Res. 2023;71(1):15-28. doi: 10.1007/s12026-022-09323-7.
  • Berkel C. Retrospective analysis of transcriptomic differences between triple-negative breast cancer (TNBC) and non-TNBC. Eur J of Bio, 2024;83(1):19-27.
  • Royston P. Remark AS R94: A remark on Algorithm AS 181: The WW test for normality. Appl Stat, 1995;44:547–551. doi:10.2307/2986146.
  • Nakamura Y, Tanaka KJ, Miyauchi M, Huang L, Tsujimoto M, Matsumoto K. Translational repression by the oocyte-specific protein P100 in Xenopus. Dev Biol. 2010;344(1):272-83. doi: 10.1016/j.ydbio.2010.05.006.
  • Berkel C. Inducers and Inhibitors of Pyroptotic Death of Granulosa Cells in Models of Premature Ovarian Insufficiency and Polycystic Ovary Syndrome. Reprod Sci. 2024 ;31(10):2972-2992. doi: 10.1007/s43032-024-01643-3.

Temporal regulation of PATL2 transcript levels during oocyte maturation and embryo development: An in silico analysis

Year 2025, Volume: 8 Issue: 3, 263 - 270, 22.10.2025
https://doi.org/10.53446/actamednicomedia.1634724

Abstract

Objective: Female infertility is a relatively frequent disorder of the reproductive system, and its molecular etiology and associated cellular mechanisms remain unexplained. Certain mutations in PATL2 gene have been identified to cause female infertility, characterized by oocyte maturation arrest and oocyte meiotic deficiency. PATL2 encodes an RNA-binding protein functioning as a translational repressor in oocyte maturation; therefore, proper temporal control of PATL2 expression was suggested to be essential for normal oocyte maturation.
Methods: Transcriptomics data was used to analyze temporal regulation of PATL2 transcript levels during oocyte maturation and embryo development in mice, using R programming language.
Results: Based on in silico analysis, mRNA expression of the PATL2 gene in mouse oocytes was found to increase from the primordial follicle stage to the primary follicle stage (p ≤ 0.05). Its expression was reported to stay high in the primary and secondary follicle stages, then to decrease in the antral follicle stages (tertiary follicle stages). Besides, PATL2 expression was shown to be lower in metaphase 2 (MII)-stage oocytes compared to germinal vesicle (GV)-stage oocytes in mice (p ≤ 0.05). Moreover, it was observed that PATL2 transcript levels even change during embryo development.
Conclusion: Data in the present study points to the temporal regulation of PATL2 expression at the transcription level during oocyte growth, supporting previous research performed at the protein level. Considering the importance of PATL2 in oocyte maturation arrest and female sterility, and also the number of PATL2 pathogenic variants previously identified, a better mechanistic understanding of PATL2 regulation at the transcriptional level in oocytes might have clinical significance and guide the development of novel treatment strategies.

Ethical Statement

Not applicable.

Supporting Institution

None

References

  • Maddirevula S, Coskun S, Alhassan S, Elnour A, Alsaif HS, Ibrahim N, et al. Female Infertility Caused by Mutations in the Oocyte-Specific Translational Repressor PATL2. Am J Hum Genet. 2017;101(4):603-608. doi: 10.1016/j.ajhg. 2017.08.009.
  • Chen B, Zhang Z, Sun X, Kuang Y, Mao X, Wang X, et al. Biallelic Mutations in PATL2 Cause Female Infertility Characterized by Oocyte Maturation Arrest. Am J Hum Genet. 2017;101(4):609-615. doi: 10.1016/j.ajhg.2017.08. 018.
  • Christou-Kent M, Kherraf ZE, Amiri-Yekta A, Le Blévec E, Karaouzène T, Conne B, et al. PATL2 is a key actor of oocyte maturation whose invalidation causes infertility in women and mice. EMBO Mol Med. 2018;10(5):e8515. doi: 10.15252/emmm.201708515.
  • Huang L, Tong X, Wang F, Luo L, Jin R, Fu Y, et al. Novel mutations in PATL2 cause female infertility with oocyte germinal vesicle arrest. Hum Reprod. 2018;33(6):1183-1190. doi: 10.1093/humrep/dey100.
  • Christou-Kent M, Ray PF, Arnoult C. Échec de maturation ovocytaire - Un rôle essentiel pour la protéine PATL2 dans l’ovogenèse [Oocyte maturation failure: an essential role for the protein PATL2 in human oogenesis]. Med Sci (Paris). 2018;34(12):1042-1045. French. doi: 10.1051/ medsci/2018287.
  • Wu L, Chen H, Li D, Song D, Chen B, Yan Z, et al. Novel mutations in PATL2: expanding the mutational spectrum and corresponding phenotypic variability associated with female infertility. J Hum Genet. 2019;64(5):379-385. doi: 10.1038/s10038-019-0568-6.
  • Liu Z, Zhu L, Wang J, Luo G, Xi Q, Zhou X, et al. Novel homozygous mutations in PATL2 lead to female infertility with oocyte maturation arrest. J Assist Reprod Genet. 2020;37(4):841-847. doi: 10.1007/s10815-020-01698-6.
  • Cao Q, Zhao C, Wang C, Cai L, Xia M, Zhang X, et al. The Recurrent Mutation in PATL2 Inhibits Its Degradation Thus Causing Female Infertility Characterized by Oocyte Maturation Defect Through Regulation of the Mos-MAPK Pathway. Front Cell Dev Biol. 2021;9:628649. doi: 10.3389/ fcell.2021.628649.
  • Sang Q, Zhou Z, Mu J, Wang L. Genetic factors as potential molecular markers of human oocyte and embryo quality. J Assist Reprod Genet. 2021;38(5):993-1002. doi: 10.1007/s10815-021-02196-z.
  • Peng SL, Wu QF, Xie Q, Tan J, Shu KY. PATL2 regulated the apoptosis of ovarian granulosa cells in patients with PCOS. Gynecol Endocrinol. 2021;37(7):629-634. doi: 10.1080/ 09513590.2021.1928066.
  • Huang L, Wang Y, Lu F, Jin Q, Song G, Ji J, et al. Novel mutations in NLRP5 and PATL2 cause female infertility characterized by primarily oocyte maturation abnormality and consequent early embryonic arrest. J Assist Reprod Genet. 2022;39(3):711-718. doi: 10.1007/s10815-022-02412-4.
  • Huo M, Zhang Y, Shi S, Shi H, Liu Y, Zhang L, et al. Gene Spectrum and Clinical Traits of Nine Patients With Oocyte Maturation Arrest. Front Genet. 2022;13:772143. doi: 10.3389/fgene.2022.772143.
  • Xue N, Wang Y, Xu X, Jiang X, Li C, Wang J, et al. Establishment of pluripotent stem cell line induced by PATL2 heterozygous mutation in patients with oocyte maturation defect-4. Stem Cell Res. 2022;61:102776. doi: 10.1016/j.scr.2022.102776.
  • Loeuillet C, Dhellemmes M, Cazin C, Kherraf ZE, Fourati Ben Mustapha S, Zouari R, et al. A recurrent ZP1 variant is responsible for oocyte maturation defect with degenerated oocytes in infertile females. Clin Genet. 2022;102(1):22-29. doi: 10.1111/cge.14144.
  • Capalbo A, Buonaiuto S, Figliuzzi M, Damaggio G, Girardi L, Caroselli S, et al. Maternal exome analysis for the diagnosis of oocyte maturation defects and early embryonic developmental arrest. Reprod Biomed Online. 2022;45(3):508-518. doi: 10.1016/j.rbmo.2022.05.009.
  • Lei Q, Li J, Zhou X, Zhang W. [Oocyte maturation arrest due to compound heterozygous variants of the PATL2 gene in a case]. Zhonghua Yi Xue Yi Chuan Xue Za Zhi. 2022;39(7):759-762. Chinese. doi: 10.3760/cma.j. cn511374-20210316-00234.
  • Sun L, Tong K, Liu W, Tian Y, Yang S, Zhou D, et al. Identification and characterization of a novel homozygous splice site variant of PATL2 causing female infertility due to oocyte germinal vesicle arrest. Front Genet. 2022;13:967288. doi: 10.3389/fgene.2022.967288.
  • Zhu L, Yang Q, Jin H, Zhou J, Wang M, Yang L, et al. Oocyte phenotype, genetic diagnosis, and clinical outcome in case of patients with oocyte maturation arrest. Front Endocrinol (Lausanne). 2022;13:1016563. doi: 10.3389/ fendo.2022.1016563.
  • Campos G, Sciorio R, Esteves SC. Total fertilization failure after ICSI: insights into pathophysiology, diagnosis, and management through artificial oocyte activation. Hum Reprod Update. 2023;29(4):369-394. doi: 10.1093/ humupd/dmad007. PMID: 36977357.
  • Torra-Massana M, Rodríguez A, Vassena R. Exonic genetic variants associated with unexpected fertilization failure and zygotic arrest after ICSI: a systematic review. Zygote. 2023;31(4):316-341. doi: 10.1017/S096719942300014X.
  • Zhang Z, Liu R, Zhou H, Li Q, Qu R, Wang W, et al. PATL2 regulates mRNA homeostasis in oocytes by interacting with EIF4E and CPEB1. Development. 2023;150(12): dev201572. doi: 10.1242/dev.201572.
  • Zhou H, Cai YL, Luo Q, Zou L, Yin YX, Chen Y, et al. High carrier frequency of pathogenic PATL2 gene mutations predicted in population: a bioinformatics-based approach. Front Genet. 2023 May;14:1097951. doi: 10.3389/ fgene.2023.1097951.
  • Lv XJ, Guo J, Lin G. Novel mutations in TRIP13 lead to female infertility with oocyte maturation arrest. Yi Chuan. 2023;45(6):514-525. doi: 10.16288/j.yczz.23-022.
  • Ye Z, Li D, Niu X, Yang A, Pan Z, Yu R, et al. Identification novel mutations and phenotypic spectrum expanding in PATL2 in infertile women with IVF/ICSI failure. J Assist Reprod Genet. 2024;41(5):1233-1243. doi: 10.1007/ s10815-024-03071-3.
  • Hu HY, Zhang GH, Deng WF, Wei TY, Feng ZK, et al. Novel PATL2 variants cause female infertility with oocyte maturation defect. J Assist Reprod Genet. 2024. doi: 10.1007/s10815-024-03150-5.
  • Wan LB, Pan H, Hannenhalli S, Cheng Y, Ma J, Fedoriw A, et al. Maternal depletion of CTCF reveals multiple functions during oocyte and preimplantation embryo development. Development. 2008;135(16):2729-38. doi: 10.1242/ dev.024539.
  • Mitchell LE. Maternal effect genes: Update and review of evidence for a link with birth defects. HGG Adv. 2021;3(1):100067. doi: 10.1016/j.xhgg.2021.100067.
  • Musfee FI, Oluwafemi OO, Agopian AJ, Hakonarson H, Goldmuntz E, Mitchell LE. Maternal effect genes as risk factors for congenital heart defects. HGG Adv. 2022;3(2):100098. doi: 10.1016/j.xhgg.2022.100098.
  • Pan H, O'brien MJ, Wigglesworth K, Eppig JJ, Schultz RM. Transcript profiling during mouse oocyte development and the effect of gonadotropin priming and development in vitro. Dev Biol. 2005;286(2):493-506. doi: 10.1016/j.ydbio. 2005.08.023.
  • Pan H, Ma P, Zhu W, Schultz RM. Age-associated increase in aneuploidy and changes in gene expression in mouse eggs. Dev Biol. 2008;316(2):397-407. doi: 10.1016/j.ydbio. 2008.01.048.
  • Barrett T, Wilhite SE, Ledoux P, Evangelista C, Kim IF, Tomashevsky M, et al. NCBI GEO: archive for functional genomics data sets--update. Nucleic Acids Res. 2013;41(Database issue):D991-5. doi: 10.1093/nar/ gks1193.
  • Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002;30(1):207-10. doi: 10.1093/nar/30.1.207.
  • R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2022. URL https://www.R-project.org/.
  • Wickham H, Bryan J. _readxl: Read Excel Files_. R package version 1.4.2, 2023. <https://CRAN.R-project.org /package=readxl>.
  • Wickham H, Averick M, Bryan J, Chang W, McGowan LD, François R, et al. “Welcome to the tidyverse.” J of Open Source Software_, 2019;4(43):1686. doi:10.21105/joss. 01686 <https://doi.org/10.21105/joss.01686>.
  • Kassambara A. _ggpubr: 'ggplot2' Based Publication Ready Plots_. R package version 0.6.0. 2023. <https://CRAN.R-project.org/package=ggpubr>.
  • Xie Y. knitr: A General-Purpose Package for Dynamic Report Generation in R. R package version 1.42. 2023.
  • Allaire J, Xie Y, Dervieux C, McPherson J, Luraschi J, Ushey K, et al. _rmarkdown: Dynamic Documents for R_. R package version 2.21. 2023. <https://github.com/rstudio /rmarkdown>.
  • Berkel C, Cacan E. Lower expression of NINJ1 (Ninjurin 1), a mediator of plasma membrane rupture, is associated with advanced disease and worse prognosis in serous ovarian cancer. Immunol Res. 2023;71(1):15-28. doi: 10.1007/s12026-022-09323-7.
  • Berkel C. Retrospective analysis of transcriptomic differences between triple-negative breast cancer (TNBC) and non-TNBC. Eur J of Bio, 2024;83(1):19-27.
  • Royston P. Remark AS R94: A remark on Algorithm AS 181: The WW test for normality. Appl Stat, 1995;44:547–551. doi:10.2307/2986146.
  • Nakamura Y, Tanaka KJ, Miyauchi M, Huang L, Tsujimoto M, Matsumoto K. Translational repression by the oocyte-specific protein P100 in Xenopus. Dev Biol. 2010;344(1):272-83. doi: 10.1016/j.ydbio.2010.05.006.
  • Berkel C. Inducers and Inhibitors of Pyroptotic Death of Granulosa Cells in Models of Premature Ovarian Insufficiency and Polycystic Ovary Syndrome. Reprod Sci. 2024 ;31(10):2972-2992. doi: 10.1007/s43032-024-01643-3.
There are 43 citations in total.

Details

Primary Language English
Subjects Bioinformatics and Computational Biology (Other), Obstetrics and Gynaecology
Journal Section Research Articles
Authors

Çağlar Berkel 0000-0003-4787-5157

Publication Date October 22, 2025
Submission Date February 6, 2025
Acceptance Date July 18, 2025
Published in Issue Year 2025 Volume: 8 Issue: 3

Cite

AMA Berkel Ç. Temporal regulation of PATL2 transcript levels during oocyte maturation and embryo development: An in silico analysis. Acta Medica Nicomedia. October 2025;8(3):263-270. doi:10.53446/actamednicomedia.1634724

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