دورية أكاديمية

Differential Gene Regulation of the Human Blastocyst Trophectoderm and Inner Cell Mass by Progesterone.

التفاصيل البيبلوغرافية
العنوان: Differential Gene Regulation of the Human Blastocyst Trophectoderm and Inner Cell Mass by Progesterone.
المؤلفون: Snow KS; Division of Reproductive Endocrinology and Infertility Department of Obstetrics and Gynecology, Duke University, 5601 Arringdon Park Dr Suite 210, Morrisville, NC, 27560, USA., Raburn DJ; Division of Reproductive Endocrinology and Infertility Department of Obstetrics and Gynecology, Duke University, 5601 Arringdon Park Dr Suite 210, Morrisville, NC, 27560, USA., Price TM; Division of Reproductive Endocrinology and Infertility Department of Obstetrics and Gynecology, Duke University, 5601 Arringdon Park Dr Suite 210, Morrisville, NC, 27560, USA. price067@mc.duke.edu.
المصدر: Reproductive sciences (Thousand Oaks, Calif.) [Reprod Sci] 2024 May; Vol. 31 (5), pp. 1363-1372. Date of Electronic Publication: 2023 Dec 27.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Springer Country of Publication: United States NLM ID: 101291249 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1933-7205 (Electronic) Linking ISSN: 19337191 NLM ISO Abbreviation: Reprod Sci Subsets: MEDLINE
أسماء مطبوعة: Publication: 2020- : [New York] : Springer
Original Publication: Thousand Oaks, Calif. : Sage
مواضيع طبية MeSH: Progesterone*/pharmacology , Blastocyst*/metabolism , Blastocyst*/drug effects , Gene Expression Regulation, Developmental* , Blastocyst Inner Cell Mass*/metabolism, Humans ; Receptors, Progesterone/metabolism ; Receptors, Progesterone/genetics ; Female ; Embryonic Development/drug effects ; Embryonic Development/physiology ; Human Embryonic Stem Cells/metabolism ; Human Embryonic Stem Cells/drug effects
مستخلص: Knowledge of action of progesterone (P4) on the human preimplantation embryo is lacking. The objective of this study was to determine expression of a mitochondrial P4 receptor (PR-M) in the trophectoderm (TE) and the inner cell mass (ICM) of the human blastocyst and to determine P4-induced gene expression during growth from the cleavage to the blastocyst stage. Previously cryopreserved cleavage stage embryos were treated with P4 (10 -6 M) or vehicle until blastocyst development. Cells from the TE and the ICM of dissected euploid embryos underwent RNA-seq analysis, while other embryos were used for analysis of nuclear PR (nPR) and PR-M expression.PR-M expression was confirmed in the TE, the ICM, and a human embryonic stem cell line (HESC). Conversely, nPR expression was absent in the TE and the ICM with low expression in the HESC line. RNA-seq analysis revealed P4 effects greater in the TE with 183 significant pathway changes compared to 27 in the ICM. The TE response included significant upregulation of genes associated with DNA replication, cell cycle phase transition and others, exemplified by a 7.6-fold increase in the cell proliferation gene, F-Box Associated Domain Containing. The majority of ICM pathways were downregulated including chromosome separation, centromere complex assembly and chromatin remodeling at centromere. This study confirms that human blastocysts express PR-M in both the TE and the ICM, but lack expression of nPR. P4-induced gene regulation differs greatly in the two cell fractions with the predominant effect of cell proliferation in the TE and not the ICM.
(© 2023. The Author(s), under exclusive licence to Society for Reproductive Investigation.)
References: Koninckx P, Kennedy S, Barlow D. Endometriotic disease: the role of peritoneal fluid. Hum Reprod Update. 1998;4:741–51. (PMID: 10027629)
Young S, Savaris R, Lessey B, Sharkey A, Balthazar U, Zaino R, Sherwin R, Fritz M. Effect of randomized serum progesterone concentration on secretory endometrial histologic development and gene expression. Hum Reprod. 2017;32(9):1903–14.
Dai Q, Provost MP, Raburn DJ, Price TM. Progesterone increases mitochondria membrane potential in non-human primate oocytes and embryos. Reprod Sci. 2020;27:1206–14. (PMID: 32046426)
Peluso JJ, Pru CA, Liu X, Kelp NC, Pru JK. Progesterone receptor membrane component 1 and 2 regulate granulosa cell mitosis and survival through a NFΚB-dependent mechanism†. Biol Reprod. 2019;100:1571–80. (PMID: 308777636561858)
Guo M, Zhang C, Wang Y, Feng L, Wang Z, Niu W, et al. Progesterone receptor membrane component 1 mediates progesterone-induced suppression of oocyte meiotic prophase i and primordial folliculogenesis. Sci Rep. 2016;6:36869. (PMID: 278489735111101)
Zhu Y, Rice C, Pang Y, P. T. Cloning, expression, and characterization of a membrane progestin receptor and evidence it is an intermediary in meiotic maturation of fish oocytes. PNAS. 2003;100:2231–6. (PMID: 12574519151323)
Josefsberg Ben-Yehoshua L, Lewellyn AL, Thomas P, Maller JL. The role of xenopus membrane progesterone receptor β in mediating the effect of progesterone on oocyte maturation. Mol Endocrinol. 2007;21:664–73. (PMID: 17185392)
Price TM, Dai Q. The role of a mitochondrial progesterone receptor (PR-M) in progesterone action. Semin Reprod Med. 2015;33:185–94. (PMID: 26036900)
Hill KK, Roemer SC, Churchill MEA, Edwards DP. Structural and functional analysis of domains of the progesterone receptor. Mol Cell Endocrinol. 2012;348:418–29. (PMID: 21803119)
Dai Q, Shah AA, Garde RV, Yonish BA, Zhang L, Medvitz NA, et al. A truncated progesterone receptor (PR-M) Localizes to the mitochondrion and controls cellular respiration. Mol Endocrinol. 2013;27:741–53. (PMID: 235189223634113)
Dai Q, Likes C, Luz A, Mao L, Yeh J, Wei Z, et al. A mitochondrial progesterone receptor increase cardia beta-oxidation and remodeling. J Endocr Soc. 2019;3:446–67. (PMID: 307465056364628)
Feng Q, Crochet JR, Dai Q, Leppert PC, Price TM. Expression of a mitochondrial progesterone receptor (PR-M) in leiomyomata and association with increased mitochondrial membrane potential. J Clin Endocrinol Metab. 2014;99:E390–9. (PMID: 244233175393478)
Behera MA, Dai Q, Garde R, Saner C, Jungheim E, Price TM. Progesterone stimulates mitochondrial activity with subsequent inhibition of apoptosis in MCF-10A benign breast epithelial cells. Am J Physiol Endocrinol Metab. 2009;297:E1089–96.
Rienzi L, Gracia C, Maggiulli R, LaBarbera AR, Kaser DJ, Ubaldi FM, Vanderpoel S, Racowsky C. Oocyte, embryo and blastocyst cryopreservation in ART: systematic review and meta-analysis comparing slow-freezing versus vitrification to produce evidence for the development of global guidance. Hum Reprod Update. 2017;23(2):139–55. (PMID: 27827818)
Saner K, Welter B, Zhang F, Hansen E, Dupont B, Wei Y, et al. Cloning and expression of a novel, truncated progesterone receptor. Mol Cell Endocrinol. 2003;200:155–63. (PMID: 12644308)
Li B, Xu L, Lu WY, Xu W, Wang MH, Yang K, et al. A whole-mechanical method to establish human embryonic stem cell line HN4 from discarded embryos. Cytotechnology. 2010;62:509–18. (PMID: 209765542995138)
Chen S, Zhou Y, Chen Y, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018;34:i884–i90. (PMID: 304230866129281)
Kersey PJ, Staines DM, Lawson D, Kulesha E, Derwent P, Humphrey JC, et al. Ensembl Genomes: an integrative resource for genome-scale data from non-vertebrate species. Nucleic Acids Res. 2012;40:D91–7. (PMID: 22067447)
Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29:15–21. (PMID: 23104886)
Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2013;30:923–30. (PMID: 24227677)
Love M, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550. (PMID: 255162814302049)
Huber W, Carey VJ, Gentleman R, Anders S, Carlson M, Carvalho BS, et al. Orchestrating high-throughput genomic analysis with Bioconductor. Nat Methods. 2015;12:115–21. (PMID: 256335034509590)
Team RC. R: A Language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ . Vienna, Austria, 2019.
Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci. 2005;102:15545–50. (PMID: 161995171239896)
Moran TJ, Gray S, Mikosz CA, Conzen SD. The glucocorticoid receptor mediates a survival signal in human mammary epithelial cells. Cancer Res. 2000;60:867–72. (PMID: 10706096)
National Center for Biotechnology Information. Gene Expression Omnibus.  https://ncbi.nlm.nih.gov/bioproject/1046549 .
Gilula NB, Epstein ML, Beers WH. Cell-to-cell communication and ovulation. A study of the cumulus-oocyte complex. J Cell Biol. 1978;78:58–75. (PMID: 670298)
Borland R, Erickson G, Ducibella T. Accumulation of steroids in rabbit preimplantation blastocysts. J Reprod Fertil. 1977;49:219–24. (PMID: 850212)
Swegen A, Grupen CG, Gibb Z, Baker MA, de Ruijter-Villani M, Smith ND, Stout TAE, Aitken RJ. From peptide masses to pregnancy maintenance: a comprehensive proteomic analysis of the early equine embryo secretome, blastocoel fluid, and capsule. Proteomics. 17(17–18). https://doi.org/10.1002/pmic.201600433 .
Hou Q, Gorski J. Estrogen receptor and progesterone receptor genes are expressed differentially in mouse embryos during preimplantation development. Proc Natl Acad Sci USA. 1993;90(20):9460–4.
Aparicio IM, Garcia-Herreros M, O’Shea LC, Hensey C, Lonergan P, Fair T. Expression, regulation, and function of progesterone receptors in bovine cumulus oocyte complexes during in vitro maturation. Biol Reprod. 2011;84:910–21. (PMID: 21228216)
Yan L, Yang M, Guo H, Yang H, Wu J, Li R, et al. Single-cell RNA-Seq profiling of human preimplantation embryos and embryonic stem cells. Nat Struct Mol Biol. 2013;20:1131–9. (PMID: 23934149)
Blakeley P, Fogarty N, del Valle I, Wamaitha S, Hu T, Elder K, et al. Defining the three cell lineages of the human blastocyst by single cell RNA-seq. Development. 2015;142:3151–65. (PMID: 262933004582176)
Akison LK, Robker RL. The critical roles of progesterone receptor (PGR) in ovulation, oocyte developmental competence and oviductal transport in mammalian reproduction. Reprod Domest Anim. 2012;47(Suppl 4):288–96. (PMID: 22827383)
Lopata A. Implantation of the human embryo. Hum Reprod. 1996;11(Suppl 1):175–84. discussion 93-5. (PMID: 8968778)
Stephenson E, Jacquet L, Miere C, Wood V, Kadeva N, Cornwell G, et al. Derivation and propagation of human embryonic stem cell lines from frozen embryos in an animal product–free environment. Nat Protoc. 2012;7:1366–81. (PMID: 22722371)
Hackett CH, Fortier LA. Embryonic stem cells and iPS cells: sources and characteristics. Vet Clin North Am Equine Pract. 2011;27:233–42. (PMID: 218727563479634)
Xu J, Li Y, Xu Y, Ding C, Li T, Zhou C. A simple and effective method for the isolation of inner cell mass samples from human blastocysts for gene expression analysis. In Vitro Cell Dev Biol Anim. 2014;50:232–6. (PMID: 24263978)
Theunissen TW, Jaenisch R. Mechanisms of gene regulation in human embryos and pluripotent stem cells. Development. 2017;144:4496–509. (PMID: 292549925769625)
Acton BM, Jurisicova A, Jurisica I, Casper RF. Alterations in mitochondrial membrane potential during preimplantation stages of mouse and human embryo development. Mol Hum Reprod. 2004;10:23–32. (PMID: 14665703)
Zorova LD, Popkov VA, Plotnikov EY, Silachev DN, Pevzner IB, Jankauskas SS, et al. Mitochondrial membrane potential. Anal Biochem. 2018;552:50–9. (PMID: 28711444)
Leese H, Conaghan J, Martin K, Hardy K. Early human embryo metabolism. BioEssays. 1993;15:259–64. (PMID: 8517855)
Miwa T, Kanda M, Koike M, Iwata N, Tanaka H, Umeda S, et al. Identification of NCCRP1 as an epigenetically regulated tumor suppressor and biomarker for malignant phenotypes of squamous cell carcinoma of the esophagus. Oncol Lett. 2017;14:4822–8. (PMID: 290854865649603)
Kallio H, Tolvanen M, Jänis J, Pan P, Laurila E, Kallioniemi A, et al. Characterization of non-specific cytotoxic cell receptor protein 1: a new member of the lectin-type subfamily of F-box proteins. PLoS One. 2011;6:e27152. (PMID: 220872553210139)
de Salort J, Cuenca M, Terhorst C, Engel P, Romero X. Ly9 (CD229) Cell-Surface Receptor is Crucial for the Development of Spontaneous Autoantibody Production to Nuclear Antigens. Front Immunol. 2013;4:225. (PMID: 239141903728625)
Sintes J, Cuenca M, Romero X, Bastos R, Terhorst C, Angulo A, et al. Cutting edge: Ly9 (CD229), a SLAM family receptor, negatively regulates the development of thymic innate memory-like CD8+ T and invariant NKT cells. J Immunol. 2013;190:21–6. (PMID: 23225888)
de la Fuente MA, Tovar V, Villamor N, Zapater N, Pizcueta P, Campo E, et al. Molecular characterization and expression of a novel human leukocyte cell-surface marker homologous to mouse Ly-9. Blood. 2001;97:3513–20. (PMID: 11369645)
Gruber I, Klein M. Embryo culture media for human IVF: which possibilities exist? J Turk Ger Gynecol Assoc. 2011;12:110–7. (PMID: 245919723939101)
Ghaemi SR, Salehnia M, Valojerdi MR. The effect of progesterone and exogenous gonadotropin on preimplantation mouse embryo development and implantation. Exp Anim. 2008;57:27–34. (PMID: 18256516)
Salehnia M, Zavareh S. The effects of progesterone on oocyte maturation and embryo development. Int J Fertil Steril. 2013;7:74–81. (PMID: 245204673850344)
Zheng P, Si W, Bavister BD, Yang J, Ding C, Ji W. 17Beta-estradiol and progesterone improve in-vitro cytoplasmic maturation of oocytes from unstimulated prepubertal and adult rhesus monkeys. Hum Reprod. 2003;18:2137–44. (PMID: 14507835)
فهرسة مساهمة: Keywords: Blastocyst gene expression; Embryo culture media; P4 supplementation; RNA-seq
المشرفين على المادة: 4G7DS2Q64Y (Progesterone)
0 (Receptors, Progesterone)
تواريخ الأحداث: Date Created: 20231227 Date Completed: 20240513 Latest Revision: 20240925
رمز التحديث: 20240925
DOI: 10.1007/s43032-023-01429-z
PMID: 38151652
قاعدة البيانات: MEDLINE
الوصف
تدمد:1933-7205
DOI:10.1007/s43032-023-01429-z