Abbreviations:A1BG (alpha-1-B glycoprotein), ACN (acetonitrile), AGC (automatic gain control), AHSG (alpha 2-HS glycoprotein), AI (artificial insemination), ALPL (alkaline phosphatase, liver/bone/kidney), ART (assistant reproductive technology), BCAM (basal cell adhesion molecule), BSA (bovine serum albumin), BSG (basigin), C5 (complement C5), C9 (complement C9), C areas (caruncular areas), CAPN2 (calpain 2), CHP1 (calcineurin-like EF-hand protein 1), CID (collision-induced dissociation), CLDN4 (claudin 4), COL6A1 (collagen type VI alpha 1 chain), COL6A2 (collagen type VI alpha 2 chain), CSTB (cathepsin B), DEPs (differentially expressed proteins), DTT (dithiothreitol), EDTA (ethylenediaminetetraacetic acid), EMB (embigin), EMILIN1 (elastin microfibril interfacer 1), ESI (electrospray ionization), FA (formic acid), FBS (fetal bovine serum), FC (fold change), FDR (false discovery rate), FITC (fluorescein isothiocyanate labeled), FKBP1A (FK506 binding protein 1A), FN1 (fibronectin 1), GE (glandular epithelium), GO (Gene Ontology), GOT2 (glutamic-oxaloacetic transaminase 2), GSEA (Gene Set Enrichment Analysis), HE (hematoxylin-eosin), HPLC (high-performance liquid chromatography), HSP90AB1 (heat shock protein 90 alpha family class B member 1), HSPA8 (heat shock protein family A (Hsp70) member 8), IAM (iodoacetamide), IC areas (intercaruncular areas), IDH2 (isocitrate dehydrogenase (NADP(+)) 2), IFN-τ (interferon τ), ISG15 (interferon-stimulated gene-15), ITGA9 (integrin subunit alpha 9), IVF (in vitro fertilization), IVO (in vivo), LC (liquid chromatography), LC-ESI-MS/MS (liquid chromatography–electrospray ionization–tandem mass spectroscopy), LE (luminal epithelium), LTQ (linear ion trap), MCT1 (monocarboxylate transporter 1), MCTs (monocarboxylate transporters), MS (mass spectrometry), myo (myometrium), NME1 (nometastatic gene 23-H1), P/S (penicillin and streptomycin), PBS (phosphate-buffered saline), PC (PathwayConnector), PGF2α (prostaglandin F2α), PLG (plasminogen), PMSF (phenylmethanesulfonyl fluoride), PTK7 (protein tyrosine kinase 7), ROS (reactive oxygen species), RPSA (40S ribosomal protein SA), S (stroma), SCNT (somatic cell nuclear transfer), SLC2A1 (solute carrier family 2 member 1), TCA (trichloroacetic acid), TGFBI (transforming growth factor beta induced), v (blood vessels), XICs (extracted ion currents)
- Martal J.L.
- Chêne N.M.
- Huynh L.P.
- L’Haridon R.M.
- Reinaud P.B.
- Guillomot M.W.
- Charlier M.A.
- Charpigny S.Y.
- Choi Y.
- Johnson G.A.
- Burghardt R.C.
- Berghman L.R.
- Joyce M.M.
- Taylor K.M.
- David Stewart M.
- Bazer F.W.
- Spencer T.E.
- Oliveira J.F.
- Henkes L.E.
- Ashley R.L.
- Purcell S.H.
- Smirnova N.P.
- Veeramachaneni D.N.R.
- Anthony R.V.
- Hansen T.R.
Identifying differentially abundant membrane and secreted proteins between the conceptus and endometrium
Screening differentially abundant membrane proteins and their interacting secreted partners
- Szklarczyk D.
- Gable A.L.
- Lyon D.
- Junge A.
- Wyder S.
- Huerta-Cepas J.
- Simonovic M.
- Doncheva N.T.
- Morris J.H.
- Bork P.
- Jensen L.J.
- von Mering C.
Screening differentially abundant secreted proteins and their interacting membrane partners
Construction of a repository of the potential ligand–receptor pathway cascade
The key pathways and processes at the maternal–fetal interface
The receptive response of the endometrium to the embryonic lactate signal
Glutathione (GSH)-based cell redox homeostasis is the target of lactate-induced histone lactylation
- Song G.
- Bailey D.W.
- Dunlap K.A.
- Burghardt R.C.
- Spencer T.E.
- Bazer F.W.
- Johnson G.A.
- Muramatsu H.
- Sumitomo M.
- Morinaga S.
- Kajikawa K.
- Kobayashi I.
- Nishikawa G.
- Kato Y.
- Watanabe M.
- Zennami K.
- Kanao K.
- Nakamura K.
- Suzuki S.
- Yoshikawa K.
Animals and treatment
LC-ESI-MS/MS analysis with a linear ion trap-orbitrap (LTQ-orbitrap) collision induced dissociation (CID)
Analyses of differentially abundant proteins
Annotations of differentially abundant membrane and secreted proteins
Construction of membrane-secreted partner interactions
- Szklarczyk D.
- Gable A.L.
- Lyon D.
- Junge A.
- Wyder S.
- Huerta-Cepas J.
- Simonovic M.
- Doncheva N.T.
- Morris J.H.
- Bork P.
- Jensen L.J.
- von Mering C.
- Mootha V.K.
- Lindgren C.M.
- Eriksson K.-F.
- Subramanian A.
- Sihag S.
- Lehar J.
- Puigserver P.
- Carlsson E.
- Ridderstråle M.
- Laurila E.
- Houstis N.
- Daly M.J.
- Patterson N.
- Mesirov J.P.
- Golub T.R.
- et al.
Conflict of interest
- Supplemental Table S1
- Supplemental Table S2
- Supplemental Table S3
- Supplemental Figures S1–S6
- Roadmap to embryo implantation: Clues from mouse models.Nat. Rev. Genet. 2006; 7: 185-199
- Uterine receptivity to implantation of blastocysts in mammals.Front. Biosci. (Schol. Ed.). 2011; 3: 745-767
- Mechanisms of implantation: Strategies for successful pregnancy.Nat. Med. 2012; 18: 1754-1767
- Estimates of human fertility and pregnancy loss.Fertil. Steril. 1996; 65: 503-509
- Implantation and the survival of early pregnancy.N. Engl. J. Med. 2001; 345: 1400-1408
- Human implantation: The last barrier in assisted reproduction technologies?.Reprod. Biomed. Online. 2006; 13: 887-904
- Physiological and molecular determinants of embryo implantation.Mol. Aspects Med. 2013; 34: 939-980
- The use of ruminant models in biomedical perinatal research.Theriogenology. 2012; 78: 1763-1773
- Animal models of implantation.Reproduction. 2004; 128: 679-695
- IFN-tau: A novel subtype I IFN1. Structural characteristics, non-ubiquitous expression, structure-function relationships, a pregnancy hormonal embryonic signal and cross-species therapeutic potentialities.Biochimie. 1998; 80: 755-777
- Mediators of maternal recognition of pregnancy in mammals.Exp. Biol. Med. 1992; 199: 373-384
- Implantation mechanisms: Insights from the sheep.Reproduction. 2004; 128: 657-668
- Pregnancy recognition and conceptus implantation in domestic ruminants: Roles of progesterone, interferons and endogenous retroviruses.Reprod. Fertil. Dev. 2007; 19: 65
- Interferon regulatory factor-two restricts expression of interferon-stimulated genes to the endometrial stroma and glandular epithelium of the ovine uterus.Biol. Reprod. 2001; 65: 1038-1049
- Expression of interferon receptor subunits, IFNAR1 and IFNAR2, in the ovine uterus.Biol. Reprod. 2002; 67: 847-853
- A microarray analysis for genes regulated by interferon-τ in ovine luminal epithelial cells.Reproduction. 2007; 134: 123-135
- Expression of interferon (IFN)-stimulated genes in extrauterine tissues during early pregnancy in sheep is the consequence of endocrine IFN-τ release from the uterine vein.Endocrinology. 2008; 149: 1252-1259
- Endometrial HSD11B1 and cortisol regeneration in the ovine uterus: Effects of pregnancy, interferon tau, and prostaglandins.Biol. Reprod. 2012; 86: 124
- Identification and characterization of glycosylation-dependent cell adhesion molecule 1-like protein expression in the ovine uterus.Biol. Reprod. 1999; 60: 241-250
- The endometrium responds differently to cloned versus fertilized embryos.Proc. Natl. Acad. Sci. U. S. A. 2009; 106: 5681-5686
- Endometrium as an early sensor of in vitro embryo manipulation technologies.Proc. Natl. Acad. Sci. U. S. A. 2009; 106: 5687-5692
- Fine-tuned adaptation of embryo–endometrium pairs at implantation revealed by transcriptome analyses in Bos taurus.PLoS Biol. 2019; 17: 1-20
- Comparative analysis of dynamic proteomic profiles between in vivo and in vitro produced mouse embryos during postimplantation period.J. Proteome Res. 2013; 12: 3843-3856
- Characterization of global loss of imprinting in fetal overgrowth syndrome induced by assisted reproduction.Proc. Natl. Acad. Sci. U. S. A. 2015; 112: 4618-4623
- Impaired imprinted X chromosome inactivation is responsible for the skewed sex ratio following in vitro fertilization.Proc. Natl. Acad. Sci. U. S. A. 2016; 113: 3197-3202
- Protein synthesis by day 16 bovine conceptuses during the time of maternal recognition of pregnancy.Int. J. Mol. Sci. 2020; 21: 2870
- Comparative analysis of proteomic profiles between endometrial caruncular and intercaruncular areas in ewes during the peri-implantation period.J. Anim. Sci. Biotechnol. 2013; 4: 39
- Analysis of the uterine lumen in fertility-classified heifers: I. Glucose, prostaglandins, and lipids.Biol. Reprod. 2020; 102: 456-474
- Analysis of the uterine lumen in fertility-classified heifers: II. Proteins and metabolites†.Biol. Reprod. 2020; 102: 571-587
- A draft network of ligand–receptor-mediated multicellular signalling in human.Nat. Commun. 2015; 6: 7866
- Analysis of single-cell RNA-seq identifies cell-cell communication associated with tumor characteristics.Cell Rep. 2018; 25: 1458-1468.e4
- Single-cell reconstruction of the early maternal–fetal interface in humans.Nature. 2018; 563: 347-353
- Conceptus signals for establishment and maintenance of pregnancy.Anim. Reprod. Sci. 2004; 82–83: 537-550
- αv β3 integrin may participate in conceptus attachment by regulating morphologic changes in the endometrium during peri-implantation in ovine.Reprod. Domest. Anim. 2011; 46: 840-847
- Gastrin-releasing peptide (GRP) in the ovine uterus: Regulation by interferon tau and progesterone.Biol. Reprod. 2008; 79: 376-386
- Interferon tau: A novel pregnancy recognition signal.Am. J. Reprod. Immunol. 1997; 37: 412-420
- The proteome of IVF-induced aberrant embryo-maternal crosstalk by implantation stage in ewes.J. Anim. Sci. Biotechnol. 2020; 11: 7
- New histological observations on the placenta of the sheep.Am. J. Anat. 1950; 87: 391-457
- Uterine protein secretions: Relationship to development of the conceptus.J. Anim. Sci. 1975; 41: 1376-1382
- Comparative analysis between endometrial proteomes of pregnant and non-pregnant ewes during the peri-implantation period.J. Anim. Sci. Biotechnol. 2015; 6: 1-14
- Human endometrium: An active site of cytokine production and action.Endocr. Rev. 1991; 12: 272-290
- Force measurements of the α5β1 integrin–fibronectin interaction.Biophys. J. 2003; 84: 1252-1262
- Collagen VI is a basement membrane component that regulates epithelial cell-fibronectin interactions.Matrix Biol. 2011; 30: 195-206
- TRPM7/RPSA complex regulates pancreatic cancer cell migration.Front. Cell Dev. Biol. 2020; 8: 549
- STRING v11: Protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets.Nucleic Acids Res. 2019; 47: D607-D613
- Adhesion molecules in endometrial epithelium: Tissue integrity and embryo implantation.J. Anat. 2009; 215: 3-13
- The formation and function of oviduct fluid.Reproduction. 1988; 82: 843-856
- Analysis of the uterine epithelial and conceptus transcriptome and luminal fluid proteome during the peri-implantation period of pregnancy in sheep.Biol. Reprod. 2016; 95: 88
- Development of a culture medium (BECM-3) for porcine embryos: Effects of bovine serum albumin and fetal bovine serum on embryo development.Biol. Reprod. 1996; 55: 1069-1074
- Models for study of human embryo implantation: Choice of cell lines?.Biol. Reprod. 2010; 82: 235-245
- Apposition to endometrial epithelial cells activates mouse blastocysts for implantation.Mol. Hum. Reprod. 2017; 23: 617-627
- Investigating the role of CD44 and hyaluronate in embryo-epithelial interaction using an in vitro model.Mol. Hum. Reprod. 2019; 25: 265-273
- PathwayConnector: Finding complementary pathways to enhance functional analysis.Bioinformatics. 2019; 35: 889-891
- A glucosephosphate isomerase (GPI) null mutation in Mus musculus: Evidence that anaerobic glycolysis is the predominant energy delivering pathway in early post-implantation embryos.Comp. Biochem. Physiol. Part B Comp. Biochem. 1992; 101: 309-314
- Genetic evidence that glycolysis is necessary for gastrulation in the mouse.Dev. Dyn. 1996; 207: 300-308
- Steroids regulate SLC2A1 and SLC2A3 to deliver glucose into trophectoderm for metabolism via glycolysis.Endocrinology. 2020; 161: 1-19
- Conceptus metabolomic profiling reveals stage-specific phenotypes leading up to pregnancy recognition in cattle†.Biol. Reprod. 2021; 104: 1022-1033
- Parallels between embryo and cancer cell metabolism.Biochem. Soc. Trans. 2013; 41: 664-669
- Lactate production by the mammalian blastocyst: Manipulating the microenvironment for uterine implantation and invasion?.Bioessays. 2015; 37: 364-371
- Nucleolar stress regulation of endometrial receptivity in mouse models and human cell lines.Cell Death Dis. 2019; 10: 831
- ATP mediates the interaction between human blastocyst and endometrium.Cell Prolif. 2019; 53e12737
- Inhibition of lactate transport and glycolysis in Ehrlich ascites tumor cells by bioflavonoids.Biochemistry. 1979; 18: 3506-3511
- Monocarboxylate transporters in cancer.Mol. Metab. 2020; 33: 48-66
- Metabolic regulation of gene expression by histone lactylation.Nature. 2019; 574: 575-580
- Nutrient concentrations in murine follicular fluid and the female reproductive tract.Theriogenology. 2005; 64: 992-1006
- Lactate produced during labor modulates uterine inflammation via GPR81 (HCA1).Am. J. Obstet. Gynecol. 2017; 216: 60.e1-60.e17
- Silencing of the JNK pathway maintains progesterone receptor activity in decidualizing human endometrial stromal cells exposed to oxidative stress signals.FASEB J. 2010; 24: 1541-1551
- Retinoic acid stimulation of VEGF secretion from human endometrial stromal cells is mediated by production of reactive oxygen species.J. Physiol. 2011; 589: 863-875
- The Nrf2 regulatory network provides an interface between redox and intermediary metabolism.Trends Biochem. Sci. 2014; 39: 199-218
- Life and death responses to trophinin-mediated adhesion during blastocyst implantation.Cell Cycle. 2011; 10: 574-575
- Antioxidative signalling pathways regulate the level of reactive oxygen species at the endometrial–extraembryonic membranes interface during early pregnancy.Int. J. Biochem. Cell Biol. 2012; 44: 1511-1518
- Different enzymatic antioxidative pathways operate within the sheep caruncular and intercaruncular endometrium throughout the estrous cycle and early pregnancy.Theriogenology. 2017; 99: 111-118
- Redox state, antioxidative activity and lipid peroxidation in erythrocytes and plasma of chronic ambulatory peritoneal dialysis patients.Clin. Chim. Acta. 1995; 234: 127-136
- Antimelanogenic and antioxidant properties of gallic acid.Biol. Pharm. Bull. 2007; 30: 1052-1055
- Dynamic proteomic profiles of in vivo- and in vitro-produced mouse postimplantation extraembryonic tissues and placentas.Biol. Reprod. 2014; 91: 1-16
- Changes in gene expression during the early to mid-luteal (receptive phase) transition in human endometrium detected by high-density microarray screening.Mol. Hum. Reprod. 2002; 8: 871-879
- Transcriptomic changes during the pre-receptive to receptive transition in human endometrium detected by RNA-Seq.J. Clin. Endocrinol. Metab. 2014; 99: E2744-E2753
- Pregnancy-induced changes in metabolome and proteome in ovine uterine flushings.Biol. Reprod. 2017; 97: 273-287
- Conceptus-endometrium crosstalk during maternal recognition of pregnancy in cattle.Biol. Reprod. 2012; 87: 1-9
- Proteomic analysis of pregnancy-related proteins from pig uterus endometrium during pregnancy.Proteome Sci. 2011; 9: 41
- Calpain 2 activity increases at the time of implantation in rat uterine luminal epithelial cells and administration of calpain inhibitor significantly reduces implantation sites.Histochem. Cell Biol. 2014; 141: 423-430
- Adhesion molecules and implantation.J. Reprod. Immunol. 2002; 55: 101-112
- NME1 at the human maternal-fetal interface downregulates titin expression and invasiveness of trophoblast cells via MAPK pathway in early pregnancy.Reproduction. 2010; 139: 799-808
- NME1 suppression promotes growth, adhesion and implantation of endometrial stromal cells via Akt and MAPK/Erk1/2 signal pathways in the endometriotic milieu.Hum. Reprod. 2013; 28: 2822-2831
- Expression of cystatin C in the rat endometrium during the peri-implantation period.Biochem. Biophys. Res. Commun. 2006; 349: 236-244
- Cathepsin B, cathepsin L, and cystatin C in the porcine uterus and placenta: Potential roles in endometrial/placental remodeling and in fluid-phase transport of proteins secreted by uterine epithelia across placental areolae.Biol. Reprod. 2010; 82: 854-864
- Embryonic regulation of integrins 3, 4, and 1 in human endometrial epithelial cells in vitro.J. Clin. Endocrinol. Metab. 1997; 82: 2607-2616
- Epithelial membrane protein-2 regulates surface expression of αvβ3 integrin in the endometrium.Dev. Biol. 2005; 287: 336-345
- Quantification of fibronectin 1 (FN1) splice variants, including two novel ones, and analysis of integrins as candidate FN1 receptors in bovine preimplantation embryos.BMC Dev. Biol. 2009; 9: 1-16
- Defects in mesoderm, neural tube and vascular development in mouse embryos lacking fibronectin.Development. 1993; 119: 1079-1091
- Inhibition of histone methyltransferase EZH2 suppresses endometriotic vesicle development in a rat model of endometriosis.Reprod. Sci. 2020; 27: 1812-1820
- Histone lactylation drives oncogenesis by facilitating m6A reader protein YTHDF2 expression in ocular melanoma.Genome Biol. 2021; 22: 85
- Targeting lactate dehydrogenase-a promotes docetaxel-induced cytotoxicity predominantly in castration-resistant prostate cancer cells.Oncol. Rep. 2019; 42: 224-230
- Oxamate is an alternative substrate for pyruvate carboxylase from Rhizobium etli.Biochemistry. 2013; 52: 2888-2894
- Dynamic epigenomic landscapes during early lineage specification in mouse embryos.Nat. Genet. 2018; 50: 96-105
- Flux through hepatic pyruvate carboxylase and phosphoenolpyruvate carboxykinase detected by hyperpolarized 13C magnetic resonance.Proc. Natl. Acad. Sci. U. S. A. 2011; 108: 19084-19089
- Metabolism of hyperpolarized [1-13C]pyruvate through alternate pathways in rat liver.NMR Biomed. 2016; 29: 466-474
- Controlling the false discovery rate: A practical and powerful approach to multiple testing.J. R. Stat. Soc. Ser. B. 1995; 57: 289-300
- Proteomic profile of uterine luminal fluid from early pregnant ewes.J. Proteome Res. 2010; 9: 3878-3885
- MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification.Nat. Biotechnol. 2008; 26: 1367-1372
- Stable isotope labeling by amino acids in cell culture (SILAC) and proteome quantitation of mouse embryonic stem cells to a depth of 5,111 proteins.Mol. Cell. Proteomics. 2008; 7: 672-683
- Probability-based pattern recognition and statistical framework for randomization: Modeling tandem mass spectrum/peptide sequence false match frequencies.Bioinformatics. 2007; 23: 2210-2217
- Database searching and accounting of multiplexed precursor and product ion spectra from the data independent analysis of simple and complex peptide mixtures.Proteomics. 2009; 9: 1696-1719
- Quantitative proteomic analysis of single pancreatic islets.Proc. Natl. Acad. Sci. U. S. A. 2009; 106: 18902-18907
- Manipulating the Mouse Embryo: A Laboratory Manual, Fourth Edition.Cold Spring Harbor Laboratory Press, New York, United States2014
- The role of the osteopontin-integrin αvβ3 interaction at implantation: Functional analysis using three different in vitro models.Hum. Reprod. 2014; 29: 739-749
- miR-133b reverses the hydrosalpinx-induced impairment of embryo attachment through down-regulation of SGK1.J. Clin. Endocrinol. Metab. 2016; 101: 1478-1489
- Blastocyst-induced ATP release from luminal epithelial cells initiates decidualization through the P2Y2 receptor in mice.Sci. Signal. 2020; 13eaba3396
- DAVID Bioinformatics Resources: Expanded annotation database and novel algorithms to better extract biology from large gene lists.Nucleic Acids Res. 2007; 35: W169-W175
- Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources.Nat. Protoc. 2009; 4: 44-57
- ggplot2: Elegant Graphics for Data Analysis.Springer-Verlag, New York, NY2016
- Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles.Proc. Natl. Acad. Sci. U. S. A. 2005; 102: 15545-15550
- PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes.Nat. Genet. 2003; 34: 267-273
- cyto-Hubba: A cytoscape plug-in for hub object analysis in network biology.Genome Informatics. 2009; 5: 2-3
- Performance and its limits in rigid body protein-protein docking.Structure. 2020; 28: 1071-1081.e3
- New additions to the ClusPro server motivated by CAPRI.Proteins. 2017; 85: 435-444
- The ClusPro web server for protein–protein docking.Nat. Protoc. 2017; 12: 255-278
- How good is automated protein docking?.Proteins. 2013; 81: 2159-2166
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