Transcriptome changes in the porcine endometrium during the preattachment phas

Biology of Reproduction

Volumn 89, Issue 6, 2013, Pages

  Samborski, Anastazia ^a   Graf, Alexander ^a   Krebs, Stefan ^a   Kessler, Barbara ^a   Reichenbach, Myriam ^b   Reichenbach, Horst Dieter ^b   Ulbrich, Susanne E ^c,d   Bauersachs, Stefan ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b Landwirtschaftskammer Weser Ems   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d ETH ZURICH   (Switzerland)

Author keywords

Endometrium; Gene expression; Genomics; Illumina GAIIx; Implantation; Pig; Pregnancy; Sus scrofa; Swine; Uterus

Indexed keywords

CALGRANULIN B; EPIDERMAL GROWTH FACTOR RECEPTOR; FIBROBLAST GROWTH FACTOR 9; G PROTEIN COUPLED RECEPTOR; HYPOCALCIN; INTEGRIN; INTERLEUKIN 24; METALLOPROTEINASE; PHOSPHOLIPASE A2; PROSTAGLANDIN E2; PROSTAGLANDIN F; PROSTAGLANDIN F2 ALPHA; PROTEIN KINASE; PROTEIN KINASE ZAP 70; PROTEINASE; T LYMPHOCYTE RECEPTOR; TRANSCRIPTOME; UROPLAKIN 1B; UROPLAKIN 3;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN PRESENTATION; APOPTOSIS; ARTICLE; BIOINFORMATICS; BONE MARROW CELL; CELL CYCLE; CELL DEATH; CELL DIFFERENTIATION; CELL DIVISION; CELL MATURATION; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CHROMOSOME SEGREGATION; CONTROLLED STUDY; ENDOMETRIUM; EPITHELIUM CELL; ESTRUS CYCLE; EXPERIMENTAL PIG; EXTRACELLULAR MATRIX; FEMALE; FIRST TRIMESTER PREGNANCY; FOCAL ADHESION; GENE EXPRESSION; IMMUNE RESPONSE; INNATE IMMUNITY; ION TRANSPORT; MITOSIS; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROTEIN DEGRADATION; RECOGNITION; RNA SEQUENCE; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; UPREGULATION;

ENDOMETRIUM; GENE EXPRESSION; GENOMICS; ILLUMINA GAIIX; IMPLANTATION; PIG; PREGNANCY; SUS SCROFA; SWINE; UTERUS;

ANIMALS; EMBRYO IMPLANTATION; ENDOMETRIUM; FEMALE; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORKS; GESTATIONAL AGE; MOLECULAR SEQUENCE ANNOTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PREGNANCY; SEQUENCE ANALYSIS, RNA; SWINE; TRANSCRIPTOME;

EID: 84895545646     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.113.112177     Document Type: Article

References (86)

1. Geisert RD, Zavy MT, Moffatt RJ, Blair RM, Yellin T. Embryonic steroids and the establishment of pregnancy in pigs. J Reprod Fertil Suppl 1990; 40:293-305.
2. Geisert RD, Brookbank JW, Roberts RM, Bazer FW. Establishment of pregnancy in the pig: II. Cellular remodeling of the porcine blastocyst during elongation on day 12 of pregnancy. Biol Reprod 1982; 27: 941-955.
3. Stroband HW, Van der Lende T. Embryonic and uterine development during early pregnancy in pigs. J Reprod Fertil Suppl 1990; 40:261-277.
4. Yelich JV, Pomp D, Geisert RD. Ontogeny of elongation and gene expression in the early developing porcine conceptus. Biol Reprod 1997; 57:1256-1265.
5. Flint AP, Burton RD, Gadsby JE, Saunders PT, Heap RB. Blastocyst estrogen synthesis and the maternal recognition of pregnancy. Ciba Found Symp 1978; 64:209-238.
6. Guthrie HD, Rexroad CE Jr. Progesterone secretion and prostaglandin F release in vitro by endometrial and luteal tissue of cyclic pigs. J Reprod Fertil 1980; 60:157-163.
7. Gadsby JE, Lovdal JA, Britt JH, Fitz TA. Prostaglandin F2 alpha receptor concentrations in corpora lutea of cycling, pregnant, and pseudopregnant pigs. Biol Reprod 1993; 49:604-608.
8. Ford SP, Christenson RK, Ford JJ. Uterine blood flow and uterine arterial, venous and luminal concentrations of estrogens on days 11, 13 and 15 after estrus in pregnant and non-pregnant sows. J Reprod Fertil 1982; 64: 185-190.
9. Bazer FW, Thatcher WW. Theory of maternal recognition of pregnancy in swine based on estrogen controlled endocrine versus exocrine secretion of prostaglandin F2alpha by the uterine endometrium. Prostaglandins 1977; 14:397-400.
10. Ziecik AJ, Waclawik A, Kaczmarek MM, Blitek A, Jalali BM, Andronowska A. Mechanisms for the establishment of pregnancy in the pig. Reprod Domest Anim 2011; 46(suppl 3):31-41.
11. Waclawik A. Novel insights into the mechanisms of pregnancy establishment: regulation of prostaglandin synthesis and signaling in the pig. Reproduction 2011; 142:389-399.
12. Kennedy TG, Gillio-Meina C, Phang SH. Prostaglandins and the initiation of blastocyst implantation and decidualization. Reproduction 2007; 134: 635-643.
13. Weems CW, Weems YS, Randel RD. Prostaglandins and reproduction in female farm animals. Vet J 2006; 171:206-228.
14. østrup E, Bauersachs S, Blum H, Wolf E, Hyttel P. Differential endometrial gene expression in pregnant and nonpregnant sows. Biol Reprod 2010; 83:277-285.
15. Samborski A, Graf A, Krebs S, Kessler B, Bauersachs S. Deep sequencing of the porcine endometrial transcriptome on day 14 of pregnancy. Biol Reprod 2013; 88:84.
16. Giardine B, Riemer C, Hardison RC, Burhans R, Elnitski L, Shah P, Zhang Y, Blankenberg D, Albert I, Taylor J, Miller W, Kent WJ, et al. Galaxy: a platform for interactive large-scale genome analysis. Genome Res 2005; 15:1451-1455.
17. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010; 26:139-140.
18. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 2003; 4:P3.
19. Bindea G, Mlecnik B, Hackl H, Charoentong P, Tosolini M, Kirilovsky A, Fridman WH, Pages F, Trajanoski Z, Galon J. ClueGO: a Cytoscape plugin to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics 2009; 25:1091-1093.
20. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP. 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.
21. Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, Sturn A, Snuffin M, et al. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 2003; 34:374-378.
22. Streyl D, Kenngott R, Herbach N, Wanke R, Blum H, Sinowatz F, Wolf E, Zerbe H, Bauersachs S. Gene expression profiling of bovine peripartal placentomes: detection of molecular pathways potentially involved in release of fetal membranes. Reproduction 2012; 143:85-105.
23. Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP. Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper-Excel-based tool using pair-wise correlations. Biotechnol Lett 2004; 26:509-515.
24. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001; 25:402-408.
25. The Human Protein Atlas. Stockholm: School of Biotechnology, AlbaNova University Center, Royal Institute of Technology (KTH); 2005. http://www.proteinatlas.org. Accessed February 1, 2013.
26. Merkl M, Ulbrich SE, Otzdorff C, Herbach N, Wanke R, Wolf E, Handler J, Bauersachs S. Microarray analysis of equine endometrium at days 8 and 12 of pregnancy. Biol Reprod 2010; 83:874-886.
27. Anderson LL. Growth, protein content and distribution of early pig embryos. Anat Rec 1978; 190:143-153.
28. Kayser JP, Kim JG, Cerny RL, Vallet JL. Global characterization of porcine intrauterine proteins during early pregnancy. Reproduction 2006; 131:379-388.
29. Sukjumlong S, Kaeoket K, Dalin AM, Persson E. Immunohistochemical studies on estrogen receptor alpha (ER alpha) and the proliferative marker Ki-67 in the sow uterus at different stages of the estrous cycle. Reprod Domest Anim 2003; 38:5-12.
30. Sukjumlong S, Persson E, Kaeoket K, Dalin AM. Immunohistochemical studies on estrogen receptor alpha (ERalpha) and the proliferative marker Ki-67 in the sow uterus at estrus and early pregnancy. Reprod Domest Anim 2004; 39:361-369.
31. Badinga L, Michel FJ, Simmen RC. Uterine-associated serine protease inhibitors stimulate deoxyribonucleic acid synthesis in porcine endometrial glandular epithelial cells of pregnancy. Biol Reprod 1999; 61: 380-387.
32. Ka H, Al-Ramadan S, Erikson DW, Johnson GA, Burghardt RC, Spencer TE, Jaeger LA, Bazer FW. Regulation of expression of fibroblast growth factor 7 in the pig uterus by progesterone and estradiol. Biol Reprod 2007; 77:172-180.
33. Chen C, Spencer TE, Bazer FW. Expression of hepatocyte growth factor and its receptor c-met in the ovine uterus. Biol Reprod 2000; 62: 1844-1850.
34. Negami AI, Sasaki H, Kawakami Y, Kamitani N, Kotsuji F, Tominaga T, Nakamura T. Serum human hepatocyte growth factor in human menstrual cycle and pregnancy: a novel serum marker of regeneration and reconstruction of human endometrium. Horm Res 1995; 44(suppl 2): 42-46.
35. Zhang X. Hepatocyte growth factor system in the mouse uterus: variation across the estrous cycle and regulation by 17-beta-estradiol and progesterone. Biol Reprod 2010; 82:1037-1048.
36. Ross JW, Ashworth MD, White FJ, Johnson GA, Ayoubi PJ, DeSilva U, Whitworth KM, Prather RS, Geisert RD. Premature estrogen exposure alters endometrial gene expression to disrupt pregnancy in the pig. Endocrinology 2007; 148:4761-4773.
37. Dimova T, Mihaylova A, Spassova P, Georgieva R. Establishment of the porcine epitheliochorial placenta is associated with endometrial T-cell recruitment. Am J Reprod Immunol 2007; 57:250-261.
38. Engelhardt H, Croy BA, King GJ. Conceptus influences the distribution of uterine leukocytes during early porcine pregnancy. Biol Reprod 2002; 66: 1875-1880.
39. Bischof RJ, Brandon MR, Lee CS. Cellular immune responses in the pig uterus during pregnancy. J Reprod Immunol 1995; 29:161-178.
40. Bauersachs S, Wolf E. Immune aspects of embryo-maternal cross-talk in the bovine uterus. J Reprod Immunol 2013; 97:20-26.
41. Murphy SP, Tayade C, Ashkar AA, Hatta K, Zhang J, Croy BA. Interferon gamma in successful pregnancies. Biol Reprod 2009; 80:848-859.
42. Bazer FW, Spencer TE, Johnson GA, Burghardt RC, Wu G. Comparative aspects of implantation. Reproduction 2009; 138:195-209.
43. Thomson AJ, Greer MR, Young A, Boswell F, Telfer JF, Cameron IT, Norman JE, Campbell S. Expression of intercellular adhesion molecules ICAM-1 and ICAM-2 in human endometrium: regulation by interferongamma. Mol Hum Reprod 1999; 5:64-70.
44. Nagamatsu T, Barrier BF, Schust DJ. The regulation of T-cell cytokine production by ICOS-B7H2 interactions at the human fetomaternal interface. Immunol Cell Biol 2011; 89:417-425.
45. Heikkinen J, Mottonen M, Alanen A, Lassila O. Phenotypic characterization of regulatory T cells in the human decidua. Clin Exp Immunol 2004; 136:373-378.
46. Wing K, Yamaguchi T, Sakaguchi S. Cell-autonomous and -nonautonomous roles of CTLA-4 in immune regulation. Trends Immunol 2011; 32:428-433.
47. Fuchs E, Weber K. Intermediate filaments: structure, dynamics, function, and disease. Annu Rev Biochem 1994; 63:345-382.
48. Moll R, Levy R, Czernobilsky B, Hohlweg-Majert P, Dallenbach-Hellweg G, Franke WW. Cytokeratins of normal epithelia and some neoplasms of the female genital tract. Lab Invest 1983; 49:599-610.
49. Guillomot M. Changes in extracellular matrix components and cytokeratins in the endometrium during goat implantation. Placenta 1999; 20: 339-345.
50. Liffers ST, Maghnouj A, Munding JB, Jackstadt R, Herbrand U, Schulenborg T, Marcus K, Klein-Scory S, Schmiegel W, Schwarte-Waldhoff I, Meyer HE, Stuhler K, et al. Keratin 23, a novel DPC4/Smad4 target gene which binds 14-3-3epsilon. BMC Cancer 2011; 11:137.
51. Moll R, Divo M, Langbein L. The human keratins: biology and pathology. Histochem Cell Biol 2008; 129:705-733.
52. Kreft ME, Romih R, Sterle M. Antigenic and ultrastructural markers associated with urothelial cytodifferentiation in primary explant outgrowths of mouse bladder. Cell Biol Int 2002; 26:63-74.
53. 2+-dependent vesicle binding: implications for cornified cell envelope formation in stratified squamous epithelia. J Biol Chem 2004; 279: 22773-22780.
54. Nielsen HL, Ronnov-Jessen L, Villadsen R, Petersen OW. Identification of EPSTI1, a novel gene induced by epithelial-stromal interaction in human breast cancer. Genomics 2002; 79:703-710.
55. Klein C, Bauersachs S, Ulbrich SE, Einspanier R, Meyer HH, Schmidt SE, Reichenbach HD, Vermehren M, Sinowatz F, Blum H, Wolf E. Monozygotic twin model reveals novel embryo-induced transcriptome changes of bovine endometrium in the preattachment period. Biol Reprod 2006; 74:253-264.
56. Bauersachs S, Ulbrich SE, Gross K, Schmidt SE, Meyer HH, Wenigerkind H, Vermehren M, Sinowatz F, Blum H, Wolf E. Embryo-induced transcriptome changes in bovine endometrium reveal species-specific and common molecular markers of uterine receptivity. Reproduction 2006; 132:319-331.
57. Olson GE, Winfrey VP, Matrisian PE, NagDas SK, Hoffman LH. Blastocyst-dependent upregulation of metalloproteinase/disintegrin MDC9 expression in rabbit endometrium. Cell Tissue Res 1998; 293:489-498.
58. Mishra B, Koshi K, Kizaki K, Ushizawa K, Takahashi T, Hosoe M, Sato T, Ito A, Hashizume K. Expression of ADAMTS1 mRNA in bovine endometrium and placenta during gestation. Domest Anim Endocrinol 2013; 45:43-48.
59. Zhu H, Leung PC, MacCalman CD. Expression of ADAMTS-5/implantin in human decidual stromal cells: regulatory effects of cytokines. Hum Reprod 2007; 22:63-74.
60. Devarajan P, Mookhtiar K, Van Wart H, Berliner N. Structure and expression of the cDNA encoding human neutrophil collagenase. Blood 1991; 77:2731-2738.
61. Kaeoket K, Persson E, Dalin AM. Influence of pre-ovulatory insemination and early pregnancy on the infiltration by cells of the immune system in the sow endometrium. Anim Reprod Sci 2003; 75:55-71.
62. Shapiro SD, Kobayashi DK, Ley TJ. Cloning and characterization of a unique elastolytic metalloproteinase produced by human alveolar macrophages. J Biol Chem 1993; 268:23824-23829.
63. Erlebacher A. Immunology of the maternal-fetal interface. Annu Rev Immunol 2013; 31:387-411.
64. Ulbrich SE, Meyer SU, Zitta K, Hiendleder S, Sinowatz F, Bauersachs S, Buttner M, Frohlich T, Arnold GJ, Reichenbach HD, Wolf E, Meyer HH. Bovine endometrial metallopeptidases MMP14 and MMP2 and the metallopeptidase inhibitor TIMP2 participate in maternal preparation of pregnancy. Mol Cell Endocrinol 2011; 332:48-57.
65. Thathiah A, Carson DD. MT1-MMP mediates MUC1 shedding independent of TACE/ADAM17. Biochem J 2004; 382:363-373.
66. Tapia A, Gangi LM, Zegers-Hochschild F, Balmaceda J, Pommer R, Trejo L, Pacheco IM, Salvatierra AM, Henriquez S, Quezada M, Vargas M, Rios M, et al. Differences in the endometrial transcript profile during the receptive period between women who were refractory to implantation and those who achieved pregnancy. Hum Reprod 2008; 23:340-351.
67. Nishiura R, Noda N, Minoura H, Toyoda N, Imanaka-Yoshida K, Sakakura T, Yoshida T. Expression of matrix metalloproteinase-3 in mouse endometrial stromal cells during early pregnancy: regulation by interleukin-1alpha and tenascin-C. Gynecol Endocrinol 2005; 21:111-118.
68. Mitko K, Ulbrich SE, Wenigerkind H, Sinowatz F, Blum H, Wolf E, Bauersachs S. Dynamic changes in messenger RNA profiles of bovine endometrium during the estrous cycle. Reproduction 2008; 135:225-240.
69. Forde N, Mehta JP, Minten M, Crowe MA, Roche JF, Spencer TE, Lonergan P. Effects of low progesterone on the endometrial transcriptome in cattle. Biol Reprod 2012; 87:124.
70. Fujiwara H, Imai K, Inoue T, Maeda M, Fujii S. Membrane-bound cell surface peptidases in reproductive organs. Endocr J 1999; 46:11-25.
71. Tsujimoto M, Hattori A. The oxytocinase subfamily of M1 aminopeptidases. Biochim Biophys Acta 2005; 1751:9-18.
72. Rodriguez-Martinez H, Soede NM, Flowers WL. Control of pig reproduction IX. Leicestershire, United Kingdom: Context Products Ltd.; 2013:301-311.
73. Ashworth MD, Ross JW, Hu J, White FJ, Stein DR, Desilva U, Johnson GA, Spencer TE, Geisert RD. Expression of porcine endometrial prostaglandin synthase during the estrous cycle and early pregnancy, and following endocrine disruption of pregnancy. Biol Reprod 2006; 74: 1007-1015.
74. Blitek A, Waclawik A, Kaczmarek MM, Stadejek T, Pejsak Z, Ziecik AJ. Expression of cyclooxygenase-1 and -2 in the porcine endometrium during the estrous cycle and early pregnancy. Reprod Domest Anim 2006; 41: 251-257.
75. Waclawik A, Jabbour HN, Blitek A, Ziecik AJ. Estradiol-17beta, prostaglandin E2 (PGE2), and the PGE2 receptor are involved in PGE2 positive feedback loop in the porcine endometrium. Endocrinology 2009; 150:3823-3832.
76. Tai HH, Ensor CM, Tong M, Zhou H, Yan F. Prostaglandin catabolizing enzymes. Prostaglandins Other Lipid Mediat 2002; 68-69:483-493.
77. Parent M, Madore E, MacLaren LA, Fortier MA. 15-Hydroxyprostaglandin dehydrogenase in the bovine endometrium during the estrous cycle and early pregnancy. Reproduction 2006; 131:573-582.
78. Schuster VL. Prostaglandin transport. Prostaglandins Other Lipid Mediat 2002; 68-69:633-647.
79. Zhou SF, Wang LL, Di YM, Xue CC, Duan W, Li CG, Li Y. Substrates and inhibitors of human multidrug resistance associated proteins and the implications in drug development. Curr Med Chem 2008; 15:1981-2039.
80. Franczak A, Ciereszko R, Kotwica G. Oxytocin (OT) action in uterine tissues of cyclic and early pregnant gilts: OT receptors concentration, prostaglandin F2alpha secretion, and phosphoinositide hydrolysis. Anim Reprod Sci 2005; 88:325-339.
81. Kelder T, van Iersel MP, Hanspers K, Kutmon M, Conklin BR, Evelo C, Pico AR. WikiPathways: building research communities on biological pathways. Nucl Acids Res 2012; 40:D1301-D1307.
82. Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M. KEGG for integration and interpretation of large-scale molecular datasets. Nucleic Acids Res 2012; 40:D109-D114.
83. Online Mendelian Inheritance in Man Database (OMIM). Baltimore, MD: Johns Hopkins University; 2013. http://omim.org/entry/600522. Accessed July 2013.
84. Ababneh M, Ababneh H, Shidaifat F. Expression of cytosolic phospholipase A2 in equine endometrium during the estrous cycle and early pregnancy. Reprod Domest Anim 2011; 46:268-274.
85. Lindbom J, Ljungman AG, Tagesson C. Interferon gamma-induced gene expression of the novel secretory phospholipase A2 type IID in human monocyte-derived macrophages is inhibited by lipopolysaccharide. Inflammation 2005; 29:108-117.
86. Miki Y, Yamamoto K, Taketomi Y, Sato H, Shimo K, Kobayashi T, Ishikawa Y, Ishii T, Nakanishi H, Ikeda K, Taguchi R, Kabashima K, et al. Lymphoid tissue phospholipase A2 group IID resolves contact hypersensitivity by driving antiinflammatory lipid mediators. J Exp Med 2013; 210: 1217-1234.