Gene Expression Profiles of Bovine Caruncular and Intercaruncular
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Gene expression profiles of bovine caruncular and intercaruncular endometrium at implantation Nadera Mansouri-Atiia, Julie Aubert, Pierrette Reinaud, Corinne Giraud-Delville, Geraldine Taghouti, Laurent Galio, Robin, E. Everts, Severine Degrelle, Christophe Richard, Isabelle Hue, et al. To cite this version: Nadera Mansouri-Atiia, Julie Aubert, Pierrette Reinaud, Corinne Giraud-Delville, Geraldine Taghouti, et al.. Gene expression profiles of bovine caruncular and intercaruncular endometrium at implantation. Physiological Genomics, American Physiological Society, 2009, 39 (1), pp.14-27. 10.1152/physiolge- nomics.90404.2008. hal-01197513 HAL Id: hal-01197513 https://hal.archives-ouvertes.fr/hal-01197513 Submitted on 31 May 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Nadéra Mansouri-Attia, Julie Aubert, Pierrette Reinaud, Corinne Giraud-Delville, Géraldine Taghouti, Laurent Galio, Robin E. Everts, Séverine Degrelle, Christophe Richard, Isabelle Hue, Xiangzhong Yang, X. Cindy Tian, Harris A. Lewin, Jean-Paul Renard and Olivier Sandra Physiol Genomics 39:14-27, 2009. First published Jul 21, 2009; doi:10.1152/physiolgenomics.90404.2008 You might find this additional information useful... Supplemental material for this article can be found at: http://physiolgenomics.physiology.org/cgi/content/full/90404.2008/DC1 This article cites 89 articles, 46 of which you can access free at: http://physiolgenomics.physiology.org/cgi/content/full/39/1/14#BIBL Updated information and services including high-resolution figures, can be found at: http://physiolgenomics.physiology.org/cgi/content/full/39/1/14 Downloaded from Additional material and information about Physiological Genomics can be found at: http://www.the-aps.org/publications/pg This information is current as of September 9, 2010 . physiolgenomics.physiology.org on September 9, 2010 Physiological Genomics publishes results of a wide variety of studies from human and from informative model systems with techniques linking genes and pathways to physiology, from prokaryotes to eukaryotes. It is published quarterly in January, April, July, and October by the American Physiological Society, 9650 Rockville Pike, Bethesda MD 20814-3991. Copyright © 2009 by the American Physiological Society. ISSN: 1094-8341, ESSN: 1531-2267. Visit our website at http://www.the-aps.org/. Physiol Genomics 39: 14–27, 2009. First published July 21, 2009; doi:10.1152/physiolgenomics.90404.2008. CALL FOR PAPERS Comparative Genomics Gene expression profiles of bovine caruncular and intercaruncular endometrium at implantation Nade´ra Mansouri-Attia,1 Julie Aubert,2 Pierrette Reinaud,1 Corinne Giraud-Delville,1 Ge´raldine Taghouti,1 Laurent Galio,3 Robin E. Everts,4 Se´verine Degrelle,1 Christophe Richard,5 Isabelle Hue,1 Xiangzhong Yang,6 X. Cindy Tian,6 Harris A. Lewin,4 Jean-Paul Renard,1 and Olivier Sandra1 1Institut National de la Recherche Agronomique, Unite´Mixte de Recherche (UMR) 1198 Biologie du De´veloppement et Reproduction, Jouy-en-Josas; Ecole Nationale Ve´te´rinaire d’Alfort, Maisons Alfort; 2AgroParisTech, UMR 518 Mathe´matiques et Informatiques Applique´es; Institut National de la Recherche Agronomique, UMR 518 Mathe´matiques et Informatiques Applique´es, Paris; 3Institut National de la Recherche Agronomique, UR1196, Unite´Ge´nomique et Physiologie de la Lactation, Jouy-en-Josas, France; 4Department of Animal Sciences, University of Illinois at Urbana-Champaign, Downloaded from Urbana, Illinois; 5Institut National de la Recherche Agronomique, UE1298 Unite´Commune d’Expe´rimentation Animale de Bressonvilliers, Leudeville, France; and 6Center for Regenerative Biology, Department of Animal Sciences, Storrs, Connecticut Submitted 19 December 2008; accepted in final form 16 July 2009 Mansouri-Attia N, Aubert J, Reinaud P, Giraud-Delville C, Tag- the conceptus (embryo and embryonic annexes) and the ma- physiolgenomics.physiology.org houti G, Galio L, Everts RE, Degrelle S, Richard C, Hue I, Yang X, ternal environment (85). The success of implantation relies on Tian XC, Lewin HA, Renard JP, Sandra O. Gene expression profiles several essential steps including the adjustment of the uterine of bovine caruncular and intercaruncular endometrium at implantation. environment to support the development of the conceptus and Physiol Genomics 39: 14–27, 2009. First published July 21, 2009; the profound remodeling of the endometrium structure neces- doi:10.1152/physiolgenomics.90404.2008.—At implantation the endo- sary for the apposition, adhesion, and invasion phases (36). In metrium undergoes modifications necessary for its physical interactions contrast to human and rodents, the invasion of the maternal with the trophoblast as well as the development of the conceptus. We aim tissue by the fetal tissue is very limited in ruminants (71) and to identify endometrial factors and pathways essential for a successful leads to a synepitheliochorial placentation (86). Since the implantation in the caruncular (C) and the intercaruncular (IC) areas in trophoblast appears to be intrinsically invasive in mammals cattle. Using a 13,257-element bovine oligonucleotide array, we estab- (11), apposition, adhesion, and invasion processes are thought lished expression profiles at day 20 of the estrous cycle or pregnancy to be controlled by the endometrium (83). In mammalian (implantation), revealing 446 and 1,295 differentially expressed genes species presenting an invasive implantation, decidua re- on September 9, 2010 (DEG) in C and IC areas, respectively (false discovery rate ϭ 0.08). The strains the invasion of the embryo in a spatiotemporal impact of the conceptus was higher on the immune response function in manner (20). The expression and the regulation of some C but more prominent on the regulation of metabolism function in IC. factors involved in the apposition, adhesion, and invasion The C vs. IC direct comparison revealed 1,177 and 453 DEG in cyclic aspects of implantation have been reported in ruminants (62, and pregnant animals respectively (false discovery rate ϭ 0.05), with a 79), but, overall, the comparative cascade of molecular major impact of the conceptus on metabolism and cell adhesion. We mechanisms remains largely unknown. selected 15 genes including C11ORF34, CXCL12, CXCR4, PLAC8, The sequence of events occurring during implantation in- SCARA5, and NPY and confirmed their differential expression by quan- volves a variety of maternal and embryonic factors (80). titative RT-PCR. The cellular localization was analyzed by in situ Uterine factors include enzymes, cytokines, growth factors, hybridization and, upon pregnancy, showed gene-specific patterns of cell ions, hormones, glucose, transport proteins, and adhesion mol- distribution, including a high level of expression in the luminal epithe- ecules (collectively termed histotroph) that have been shown to lium for C11ORF34 and MX1. Using primary cultures of bovine endo- metrial cells, we identified PTN, PLAC8, and CXCL12 as interferon- be mainly synthesized by the endometrial glands (65). In (IFNT) target genes and MSX1 and CXCR7 as IFNT-regulated genes, ruminants, these glands are specifically localized in large whereas C11ORF34 was not an IFNT-regulated gene. Our transcriptomic endometrial areas [intercaruncular zones (IC)] while small data provide novel molecular insights accounting for the biological aglandular caruncular areas of stromal origin [caruncles (C)] functions related to the C or IC endometrial areas and may contribute to are scattered over the endometrium surface. The endometrial the identification of potential biomarkers for normal and perturbed early glands of the IC areas have been shown to be crucial for the pregnancy. development of the conceptus (33). The C areas are present in transcriptome; interferon-tau; pregnancy; cattle the cyclic endometrium, and they fuse with the fetal cotyledons to give rise to placentomes in the pregnant animals (3). There- fore, given the structural differences and biological functions IN MAMMALS, the establishment and maintenance of pregnancy associated to the C and IC areas, these two distinct endometrial require a subtle and tightly regulated communication between zones have to be analyzed separately for a more comprehensive understanding of the implantation process in ruminants. Address for reprint requests and other correspondence: O. Sandra, INRA, UMR Uterine receptivity to implantation has been shown to be 1198 INRA-ENVA, Biologie du De´veloppement et Reproduction, Domaine de dependent on P4, whereas interferon- (IFNT) has been iden- Vilvert, F-78352 Jouy-en-Josas, France (e-mail: [email protected]). tified as the major signal of pregnancy recognition in ruminants 14 1094-8341/09 $8.00 Copyright © 2009 the American Physiological Society GENE PROFILING OF BOVINE ENDOMETRIUM AT IMPLANTATION 15 (74). This type I IFN is exclusively produced by the mononu- Mini kit; Qiagen, Courtaboeuf, France). Quality and integrity of total clear trophectoderm cells of the elongating conceptus during extracted and purified