دورية أكاديمية

Biosensor capability of the endometrium is mediated in part, by altered miRNA cargo from conceptus-derived extracellular vesicles.

التفاصيل البيبلوغرافية
العنوان: Biosensor capability of the endometrium is mediated in part, by altered miRNA cargo from conceptus-derived extracellular vesicles.
المؤلفون: De Bem THC; Discovery and Translational Sciences Department, Leeds Institute of Cardiovascular and Metabolic Medicine, School of Medicine, University of Leeds, Leeds, UK.; Departamento de Medicina Veterinária, Faculdade de Zootecnia e Engenharia de Alimentos, Universidade de São Paulo, Pirassununga, Brazil., Bridi A; Departamento de Medicina Veterinária, Faculdade de Zootecnia e Engenharia de Alimentos, Universidade de São Paulo, Pirassununga, Brazil., Tinning H; Discovery and Translational Sciences Department, Leeds Institute of Cardiovascular and Metabolic Medicine, School of Medicine, University of Leeds, Leeds, UK., Sampaio RV; Departamento de Medicina Veterinária, Faculdade de Zootecnia e Engenharia de Alimentos, Universidade de São Paulo, Pirassununga, Brazil., Malo-Estepa I; Discovery and Translational Sciences Department, Leeds Institute of Cardiovascular and Metabolic Medicine, School of Medicine, University of Leeds, Leeds, UK., Wang D; LeedsOmics, University of Leeds, Leeds, UK.; National Heart and Lung Institute, Imperial College London, London, UK., Vasconcelos EJR; LeedsOmics, University of Leeds, Leeds, UK., Nociti RP; Departamento de Medicina Veterinária, Faculdade de Zootecnia e Engenharia de Alimentos, Universidade de São Paulo, Pirassununga, Brazil., de Ávila ACFCM; Departamento de Medicina Veterinária, Faculdade de Zootecnia e Engenharia de Alimentos, Universidade de São Paulo, Pirassununga, Brazil., Rodrigues Sangalli J; Departamento de Medicina Veterinária, Faculdade de Zootecnia e Engenharia de Alimentos, Universidade de São Paulo, Pirassununga, Brazil., Motta IG; Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, Pirassununga, Brazil., Arantes Ataíde G Jr; Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, Pirassununga, Brazil., da Silva JCB; Departamento de Medicina Veterinária, Faculdade de Zootecnia e Engenharia de Alimentos, Universidade de São Paulo, Pirassununga, Brazil., Fumie Watanabe Y; Vitrogen - Biotecnologia em Reprodução Animal, Cravinhos, Brazil., Gonella-Diaza A; North Florida Research and Education Center, Institute of Food and Agricultural Sciences, University of Florida, Gainesville, Florida, USA., da Silveira JC; Departamento de Medicina Veterinária, Faculdade de Zootecnia e Engenharia de Alimentos, Universidade de São Paulo, Pirassununga, Brazil., Pugliesi G; Department of Animal Reproduction, School of Veterinary Medicine and Animal Science, University of São Paulo, Pirassununga, Brazil., Vieira Meirelles F; Departamento de Medicina Veterinária, Faculdade de Zootecnia e Engenharia de Alimentos, Universidade de São Paulo, Pirassununga, Brazil., Forde N; Discovery and Translational Sciences Department, Leeds Institute of Cardiovascular and Metabolic Medicine, School of Medicine, University of Leeds, Leeds, UK.; LeedsOmics, University of Leeds, Leeds, UK.
المصدر: FASEB journal : official publication of the Federation of American Societies for Experimental Biology [FASEB J] 2024 May 31; Vol. 38 (10), pp. e23639.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Federation of American Societies for Experimental Biology Country of Publication: United States NLM ID: 8804484 Publication Model: Print Cited Medium: Internet ISSN: 1530-6860 (Electronic) Linking ISSN: 08926638 NLM ISO Abbreviation: FASEB J Subsets: MEDLINE
أسماء مطبوعة: Publication: 2020- : [Bethesda, Md.] : Hoboken, NJ : Federation of American Societies for Experimental Biology ; Wiley
Original Publication: [Bethesda, Md.] : The Federation, [c1987-
مواضيع طبية MeSH: Endometrium*/metabolism , Endometrium*/cytology , Extracellular Vesicles*/metabolism , MicroRNAs*/metabolism , MicroRNAs*/genetics, Female ; Animals ; Cattle ; Pregnancy ; Biosensing Techniques/methods ; Embryo Implantation/physiology ; Embryo, Mammalian/metabolism
مستخلص: We tested the hypothesis that the biosensor capability of the endometrium is mediated in part, by the effect of different cargo contained in the extracellular vesicles secreted by the conceptus during the peri-implantation period of pregnancy. We transferred Bos taurus taurus embryos of different origin, in vivo (high developmental potential (IV)), in vitro (intermediate developmental potential (IVF)), or cloned (low developmental potential (NT)), into Bos taurus indicus recipients. Extracellular vesicles (EVs) recovered from Day 16 conceptus-conditioned medium were characterized and their microRNA (miRNA) cargo sequenced alongside RNA sequencing of their respective endometria. There were substantial differences in the endometrial response to in vivo versus in vitro and in vivo versus cloned conceptuses (1153 and 334DEGs respectively) with limited differences between in vitro Vs cloned conceptuses (36 DEGs). The miRNA cargo contained in conceptus-derived EVs was similar between all three groups (426 miRNA in common). Only 8 miRNAs were different between in vivo and cloned conceptuses, while only 6 miRNAs were different between in vivo and in vitro-derived conceptuses. Treatment of endometrial epithelial cells with mimic or inhibitors for miR-128 and miR-1298 changed the proteomic content of target cells (96 and 85, respectively) of which mRNAs are altered in the endometrium in vivo (PLXDC2, COPG1, HSPA12A, MCM5, TBL1XR1, and TTF). In conclusion, we have determined that the biosensor capability of the endometrium is mediated in part, by its response to different EVs miRNA cargo produced by the conceptus during the peri-implantation period of pregnancy.
(© 2024 The Authors. The FASEB Journal published by Wiley Periodicals LLC on behalf of Federation of American Societies for Experimental Biology.)
References: Wiltbank MC, Baez GM, Garcia‐Guerra A, et al. Pivotal periods for pregnancy loss during the first trimester of gestation in lactating dairy cows. Theriogenology. 2016;86:239‐253.
Hansen TR, Sinedino LDP, Spencer TE. Paracrine and endocrine actions of interferon tau (IFNT). Reproduction. 2017;154:F45‐F59.
Mamo S, Mehta JP, Forde N, McGettigan P, Lonergan P. Conceptus‐endometrium crosstalk during maternal recognition of pregnancy in cattle. Biol Reprod. 2012;87:1‐9.
Forde N, Bazer FW, Spencer TE, Lonergan P. ‘Conceptualizing’ the endometrium: identification of conceptus‐derived proteins during early pregnancy in cattle. Biol Reprod. 2015;92:1‐13.
Mansouri‐Attia N, Sandra O, Aubert J, et al. Endometrium as an early sensor of in vitro embryo manipulation technologies. Proc Natl Acad Sci. 2009;106:5687‐5692.
Bauersachs S, Ulbrich SE, Zakhartchenko V, et al. The endometrium responds differently to cloned versus fertilized embryos. Proc Natl Acad Sci. 2009;106:5681‐5686.
Macklon NS, Brosens JJ. The human endometrium as a sensor of embryo quality. Biol Reprod. 2014;91:1‐8.
Forde N, Lonergan P. Interferon‐tau and fertility in ruminants. Reproduction. 2017;154:F33‐F43.
Godkin JD, Bazer FW, Thatcher WW, Roberts RM. Proteins released by cultured day 15‐16 conceptuses prolong luteal maintenance when introduced into the uterine lumen of cyclic ewes. Reproduction. 1984;71:57‐64.
Thatcher WW, Bartol FF, Knickerbocker JJ, et al. Maternal recognition of pregnancy in cattle. J Dairy Sci. 1984;67:2797‐2811.
Tinning H, Taylor A, Wang D, et al. The role of CAPG in molecular communication between the embryo and the uterine endometrium: is its function conserved in species with different implantation strategies? FASEB J. 2020;34:11015‐11029.
Bauersachs S, Ulbrich SE, Reichenbach HD, et al. Comparison of the effects of early pregnancy with human interferon, alpha 2 (IFNA2), on gene expression in bovine endometrium. Biol Reprod. 2012;86:1‐15.
Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol. 2013;200:373‐383.
Desrochers LM, Bordeleau F, Reinhart‐King CA, Cerione RA, Antonyak MA. Microvesicles provide a mechanism for intercellular communication by embryonic stem cells during embryo implantation. Nat Commun. 2016;7:11958.
Black SG, Arnaud F, Palmarini M, Spencer TE. Endogenous retroviruses in trophoblast differentiation and placental development. Am J Reprod Immunol. 2010;64:255‐264.
Burns G, Brooks K, Wildung M, Navakanitworakul R, Christenson LK, Spencer TE. Extracellular vesicles in luminal fluid of the ovine uterus. PLoS One. 2014;9:e90913.
Machtinger R, Laurent LC, Baccarelli AA. Extracellular vesicles: roles in gamete maturation, fertilization and embryo implantation. Hum Reprod Update. 2015;22:182‐193.
Kropp J, Salih SM, Khatib H. Expression of microRNAs in bovine and human pre‐implantation embryo culture media. Front Genet. 2014;5:91.
Rosenbluth EM, Shelton DN, Wells LM, Sparks AET, van Voorhis BJ. Human embryos secrete microRNAs into culture media—a potential biomarker for implantation. Fertil Steril. 2014;101:1493‐1500.
Bridi A, Andrade GM, del Collado M, et al. Small extracellular vesicles derived from in vivo‐ or in vitro‐produced bovine blastocysts have different miRNAs profiles—implications for embryo‐maternal recognition. Mol Reprod Dev. 2021;88:628‐643.
Parrish JJ, Susko‐Parrish J, Winer MA, First NL. Capacitation of bovine sperm by heparin. Biol Reprod. 1988;38:1171‐1180.
De Bem THC, Da Silveira JC, Sampaio RV, et al. Low levels of exosomal‐miRNAs in maternal blood are associated with early pregnancy loss in cloned cattle. Sci Rep. 2017;7:14319.
De Bem THC, Chiaratti MR, Rochetti R, et al. Viable calves produced by somatic cell nuclear transfer using meiotic‐blocked oocytes. Cell Reprogram. 2011;13:419‐429.
De Bem THC, Adona P, Bressan F, et al. The influence of morphology, follicle size and Bcl‐2 and Bax transcripts on the developmental competence of bovine oocytes. Reprod Domest Anim. 2014;49:576‐583.
Crescitelli R, Lässer C, Szabó TG, et al. Distinct RNA profiles in subpopulations of extracellular vesicles: apoptotic bodies, microvesicles and exosomes. J Extracell Vesicles. 2013;2:20677.
Martin M. Cutadapt removes adapter sequences from high‐throughput sequencing reads. EMBnet J. 2011;17:10‐12.
Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory‐efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009;10:1‐10.
Kitts PA, Church DM, Thibaud‐Nissen F, et al. Assembly: a resource for assembled genomes at NCBI. Nucleic Acids Res. 2016;44:D73‐D80.
Li H, Handsaker B, Wysoker A, et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009;25:2078‐2079.
Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014;30:923‐930.
Kozomara A, Birgaoanu M, Griffiths‐Jones S. miRBase: from microRNA sequences to function. Nucleic Acids Res. 2019;47:D155‐D162.
Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA‐seq data with DESeq2. Genome Biol. 2014;15:1‐21.
Dobin A, Davis CA, Schlesinger F, et al. STAR: ultrafast universal RNA‐seq aligner. Bioinformatics. 2013;29:15‐21.
Liao Y, Smyth GK, Shi W. The R package Rsubread is easier, faster, cheaper and better for alignment and quantification of RNA sequencing reads. Nucleic Acids Res. 2019;47:e47.
Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26:139‐140.
Yu G, Wang LG, Han Y, He QY. clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS. 2012;16:284‐287.
Luo W, Brouwer C. Pathview: an R/Bioconductor package for pathway‐based data integration and visualization. Bioinformatics. 2013;29:1830‐1831.
Wickham H. ggplot2. Springer International Publishing; 2016.
Kolde R. pheatmap: Pretty Heatmaps. R Packag. 2019.
Hume L, Edge JC, Tinning H, et al. MicroRNAs emerging coordinate with placental mammals alter pathways in endometrial epithelia important for endometrial function. iScience. 2023;26:106339.
Sandra O, Constant F, Vitorino CA, et al. Maternal organism and embryo biosensoring: insights from ruminants. J Reprod Immunol. 2015;108:105‐113.
Tinning H, Edge JC, De Bem THC, et al. Review: endometrial function in pregnancy establishment in cattle. Animal. 2023;17:100751.
Forde N, Carter F, Fair T, et al. Progesterone‐regulated changes in endometrial gene expression contribute to advanced conceptus development in cattle. Biol Reprod. 2009;81:784‐794.
Forde N, Mehta JP, Minten M, et al. Effects of low progesterone on the endometrial transcriptome in cattle. Biol Reprod. 2012;87:1‐11.
Forde N, Beltman ME, Duffy GB, et al. Changes in the endometrial transcriptome during the bovine estrous cycle: effect of low circulating progesterone and consequences for conceptus elongation. Biol Reprod. 2011;84:266‐278.
Forde N, Mehta JP, McGettigan PA, et al. Alterations in expression of endometrial genes coding for proteins secreted into the uterine lumen during conceptus elongation in cattle. BMC Genomics. 2013;14:1‐13.
Théry C, Witwer KW, Aikawa E, et al. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines. J Extracell Vesicles. 2018;7:1535750.
Chaney HL, Grose LF, LaBarbara JM, et al. Galectin‐1 induces gene and protein expression related to maternal‐conceptus immune tolerance in bovine endometrium. Biol Reprod. 2022;106:487‐502.
O'Neil EV, Burns GW, Spencer TE. Extracellular vesicles: novel regulators of conceptus‐uterine interactions? Theriogenology. 2020;150:106‐112.
Nakamura K, Kusama K, Ideta A, Imakawa K, Hori M. IFNT‐independent effects of intrauterine extracellular vesicles (EVs) in cattle. Reproduction. 2020;159:503‐511.
Nakamira K, Kusama K, Hori M, et al. Global analyses and potential effects of extracellular vesicles on the establishment of conceptus implantation during the peri‐implantation period. J Reprod Dev. 2023;69:2023‐2044.
Guzewska MM, Myszczynski K, Heifetz Y, Kaczmarek MM. Embryonic signals mediate extracellular vesicle biogenesis and trafficking at the embryo–maternal interface. Cell Commun Signal. 2023;21:210.
Guzewska MM, Witek KJ, Karnas E, et al. miR‐125b‐5p impacts extracellular vesicle biogenesis, trafficking, and EV subpopulation release in the porcine trophoblast by regulating ESCRT‐dependent pathway. FASEB J. 2023;37:e23054.
Burns GW, Brooks KE, Spencer TE. Extracellular vesicles originate from the conceptus and uterus during early pregnancy in sheep. Biol Reprod. 2016;94:56‐61.
Ruiz‐González I, Minten M, Wang X, Dunlap KA, Bazer FW. Involvement of TLR7 and TLR8 in conceptus development and establishment of pregnancy in sheep. Reproduction. 2015;149:305‐316.
Hamdi M, Cañon‐Beltrán K, Mazzarella R, et al. Characterization and profiling analysis of bovine oviduct and uterine extracellular vesicles and their miRNA cargo through the estrous cycle. FASEB J. 2021;35:e22000.
Forde N, Maillo V, O'Gaora P, et al. Sexually dimorphic gene expression in bovine conceptuses at the initiation of implantation. Biol Reprod. 2016;95:92‐101.
Bazer FW, Burghardt RC, Johnson GA, Spencer TE, Wu G. Mechanisms for the establishment and maintenance of pregnancy: synergies from scientific collaborations. Biol Reprod. 2018;99:225‐241.
Bermejo‐Alvarez P, Ramos‐Ibeas P, Gutierrez‐Adan A. Solving the “X” in embryos and stem cells. Stem Cells Dev. 2012;21:1215‐1224.
Hansen PJ, Dobbs KB, Denicol AC, Siqueira LGB. Sex and the preimplantation embryo: implications of sexual dimorphism in the preimplantation period for maternal programming of embryonic development. Cell Tissue Res. 2016;363:237‐247.
Heneweer C. Adhesiveness of human uterine epithelial RL95‐2 cells to trophoblast: rho protein regulation. Mol Hum Reprod. 2002;8:1014‐1022.
Garrido‐Gómez T, Dominguez F, Quiñonero A, et al. Annexin A2 is critical for embryo adhesiveness to the human endometrium by RhoA activation through F‐Actin regulation. FASEB J. 2012;26:3715‐3727.
Grewal S, Carver J, Ridley AJ, Mardon HJ. Human endometrial stromal cell rho GTPases have opposing roles in regulating focal adhesion turnover and embryo invasion in Vitro1. Biol Reprod. 2010;83:75‐82.
Davila J, Laws MJ, Kannan A, et al. Rac1 regulates endometrial secretory function to control placental development. PLoS Genet. 2015;11:e1005458.
Zhang D, Yu Y, Ding C, Zhang R, Duan T, Zhou Q. Decreased B7‐H3 promotes unexplained recurrent miscarriage via RhoA/ROCK2 signaling pathway and regulates the secretion of decidual NK cells. Biol Reprod. 2023;108:504‐518.
Fromm B, Høye E, Domanska D, et al. MirGeneDB 2.1: toward a complete sampling of all major animal phyla. Nucleic Acids Res. 2022;50:D204‐D210.
Bazer FW, Song G, Kim J, et al. Uterine biology in pigs and sheep. J Anim Sci Biotechnol. 2012;3:1‐21.
معلومات مُعتمدة: BB/R017522/1 UKRI | Biotechnology and Biological Sciences Research Council (BBSRC); 2016/22790-1 Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP); 2017/50438-3 Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP); 2018/14137-1 Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)
فهرسة مساهمة: Keywords: endometrium; extracellular vesicles; microRNA
تواريخ الأحداث: Date Created: 20240514 Date Completed: 20240514 Latest Revision: 20240514
رمز التحديث: 20240515
DOI: 10.1096/fj.202302423RR
PMID: 38742798
قاعدة البيانات: MEDLINE
الوصف
تدمد:1530-6860
DOI:10.1096/fj.202302423RR