Conceptus-endometrium crosstalk during maternal recognition of pregnancy in cattle

Biology of Reproduction

Volumn 87, Issue 1, 2012, Pages 6-

  Mamo, Solomon ^a   Mehta, Jai P ^a   Forde, Niamh ^a   McGettigan, Paul ^a   Lonergan, Pat ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

Conceptus; Crosstalk; Endometrium; Maternal recognition; Pregnancy

Indexed keywords

INTERLEUKIN 12P35; INTERLEUKIN 23P19; MESSENGER RNA; SOMATOMEDIN BINDING PROTEIN 3; TRANSCRIPTOME; LIGAND;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CATTLE; CELLULAR DISTRIBUTION; CONCEPTION; CONTROLLED STUDY; ENDOMETRIUM; FEMALE; MOLECULAR INTERACTION; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RNA SEQUENCE; SEQUENCE ANALYSIS; ANIMAL; BREEDING; COMPUTER PROGRAM; FETUS; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; STATISTICS; TISSUE DISTRIBUTION;

BOS; BOVINAE;

ANIMALS; CATTLE; ENDOMETRIUM; FEMALE; FETUS; GENE EXPRESSION PROFILING; LIGANDS; PREGNANCY; PREGNANCY, ANIMAL; RECEPTOR CROSS-TALK; RNA, MESSENGER; SOFTWARE; TISSUE DISTRIBUTION; TRANSCRIPTOME;

EID: 84863888585     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.112.099945     Document Type: Article

References (68)

1. Bazer FW, Spencer TE, Johnson GA, Burghardt RC. Uterine receptivity to implantation of blastocysts in mammals. Front Biosci (Schol Ed) 2011; 3: 745-767.
2. Roberts RM, Chen Y, Ezashi T, Walker AM. Interferons and the maternalconceptus dialog in mammals. Semin Cell Dev Biol 2008; 19:170-177.
3. Roberts RM, Xie S, Mathialagan N. Maternal recognition of pregnancy. Biol Reprod 1996; 54:294-302.
4. Lonergan P. Embryonic loss in cattle: a cow or embryo-induced phenomenon? Proceedings of the Annual Meeting of the European Embryo Transfer Association, Poznan, Poland, 11-12 September 2009; 119-125.
5. Betteridge KJ, Eaglesome MD, Randall GC, Mitchell D. Collection, description and transfer of embryos from cattle 10-16 days after oestrus. J Reprod Fertil 1980; 59:205-216.
6. Northey DL, French LR. Effect of embryo removal and intrauterine infusion of embryonic homogenates on the lifespan of the bovine corpus luteum. J Anim Sci 1980; 50:298-302.
7. Forde N, Carter F, Spencer TE, Bazer FW, Sandra O, Mansouri-Attia N, Okumu LA, McGettigan PA, Mehta JP, McBride R, O'Gaora P, Roche JF, et al. Conceptus-induced changes in the endometrial transcriptome: how soon does the cow know she is pregnant? Biol Reprod 2011; 85:144-156.
8. Brandao DO, Maddox-Hyttel P, Lovendahl P, Rumpf R, Stringfellow D, Callesen H. Post hatching development: a novel system for extended in vitro culture of bovine embryos. Biol Reprod 2004; 71:2048-2055.
9. Vejlsted M, Du Y, Vajta G, Maddox-Hyttel P. Post-hatching development of the porcine and bovine embryo-defining criteria for expected development in vivo and in vitro. Theriogenology 2006; 65:153-165.
10. Allison Gray C, Bartol FF, Taylor KM, Wiley AA, Ramsey WS, Ott TL, Bazer FW, Spencer TE. Ovine uterine gland knock-out model: effects of gland ablation on the estrous cycle. Biol Reprod 2000; 62:448-456.
11. Gray CA, Burghardt RC, Johnson GA, Bazer FW, Spencer TE. Evidence that absence of endometrial gland secretions in uterine gland knockout ewes compromises conceptus survival and elongation. Reproduction 2002; 124:289-300.
12. Heyman Y, Chavatte-Palmer P, LeBourhis D, Camous S, Vignon X, Renard JP. Frequency and occurrence of late-gestation losses from cattle cloned embryos. Biol Reprod 2002; 66:6-13.
13. Mansouri-Attia N, Sandra O, Aubert J, Degrelle S, Everts RE, Giraud-Delville C, Heyman Y, Galio L, Hue I, Yang X, Tian XC, Lewin HA, et al. Endometrium as an early sensor of in vitro embryo manipulation technologies. Proc Natl Acad Sci U S A 2009; 106:5687-5692.
14. Bauersachs S, Ulbrich SE, Zakhartchenko V, Minten M, Reichenbach M, Reichenbach HD, Blum H, Spencer TE, Wolf E. The endometrium responds differently to cloned versus fertilized embryos. Proc Natl Acad Sci U S A 2009; 106:5681-5686.
15. Forde N, Carter F, Fair T, Crowe MA, Evans AC, Spencer TE, Bazer FW, McBride R, Boland MP, O'Gaora P, Lonergan P, Roche JF. Progesteroneregulated changes in endometrial gene expression contribute to advanced conceptus development in cattle. Biol Reprod 2009; 81:784-794.
16. Forde N, Beltman ME, Duffy GB, Duffy P, Mehta JP, O'Gaora P, Roche JF, Lonergan P, Crowe MA. 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.
17. Bauersachs S, Ulbrich SE, Reichenbach HD, Reichenbach M, Buttner M, Meyer HH, Spencer TE, Minten M, Sax G, Winter G, Wolf E. Comparison of the effects of early pregnancy with human interferon, alpha 2 (IFNA2), on gene expression in bovine endometrium. Biol Reprod 2012; 86:46, 1-15.
18. Kues WA, Sudheer S, Herrmann D, Carnwath JW, Havlicek V, Besenfelder U, Lehrach H, Adjaye J, Niemann H. Genome-wide expression profiling reveals distinct clusters of transcriptional regulation during bovine preimplantation development in vivo. Proc Natl Acad Sci U S A 2008; 105:19768-19773.
19. Misirlioglu M, Page GP, Sagirkaya H, Kaya A, Parrish JJ, First NL, Memili E. Dynamics of global transcriptome in bovine matured oocytes and preimplantation embryos. Proc Natl Acad Sci U S A 2006; 103: 18905-18910.
20. Diskin MG, Morris DG. Embryonic and early foetal losses in cattle and other ruminants. Reprod Domest Anim 2008; 43(suppl 2):260-267.
21. Mamo S, Mehta JP, McGettigan P, Fair T, Spencer TE, Bazer FW, Lonergan P. RNA sequencing reveals novel gene clusters in bovine conceptuses associated with maternal recognition of pregnancy and implantation. Biol Reprod 2011; 85:1143-1151.
22. Mamo S, Carter F, Lonergan P, Leal CL, Al Naib A, McGettigan P, Mehta JP, Evans AC, Fair T. Sequential analysis of global gene expression profiles in immature and in vitro matured bovine oocytes: potential molecular markers of oocyte maturation. BMC Genomics 2011; 12:151.
23. Levin JZ, Yassour M, Adiconis X, Nusbaum C, Thompson DA, Friedman N, Gnirke A, Regev A. Comprehensive comparative analysis of strandspecific RNA sequencing methods. Nat Methods 2010; 7:709-715.
24. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 2003; 13:2498-2504.
25. Gao J, Ade AS, Tarcea VG, Weymouth TE, Mirel BR, Jagadish HV, States DJ. Integrating and annotating the interactome using the MiMI plugin for cytoscape. Bioinformatics 2009; 25:137-138.
26. Ouyang Z, Song M, Guth R, Ha TJ, Larouche M, Goldowitz D. Conserved and differential gene interactions in dynamical biological systems. Bioinformatics 2011; 27:2851-2858.
27. Spencer TE, Bazer FW. Conceptus signals for establishment and maintenance of pregnancy. Reprod Biol Endocrinol 2004; 2:49.
28. Kramer KK, Duffy JY, Klemann SW, Bixby JA, Low BG, Pope WF, Roberts RM. Selective cloning of cDNA for secretory proteins of early embryos. Identification of a transiently expressed Kunitz domain protein from preimplantation sheep trophoblast. J Biol Chem 1994; 269: 7255-7261.
29. MacLean JA, 2nd, Chakrabarty A, Xie S, Bixby JA, Roberts RM, Green JA. Family of Kunitz proteins from trophoblast: expression of the trophoblast Kunitz domain proteins (TKDP) in cattle and sheep. Mol Reprod Dev 2003; 65:30-40.
30. Larson JH, Kumar CG, Everts RE, Green CA, Everts-van der Wind A, Band MR, Lewin HA. Discovery of eight novel divergent homologs expressed in cattle placenta. Physiol Genomics 2006; 25:405-413.
31. Telugu BP, Walker AM, Green JA. Characterization of the bovine pregnancy-associated glycoprotein gene family-analysis of gene sequences, regulatory regions within the promoter and expression of selected genes. BMC Genomics 2009; 10:185.
32. Green JA, Xie S, Quan X, Bao B, Gan X, Mathialagan N, Beckers JF, Roberts RM. Pregnancy-associated bovine and ovine glycoproteins exhibit spatially and temporally distinct expression patterns during pregnancy. Biol Reprod 2000; 62:1624-1631.
33. Roberts RM, Cross JC, Leaman DW. Interferons as hormones of pregnancy. Endocr Rev 1992; 13:432-452.
34. Spencer TE, Johnson GA, Bazer FW, Burghardt RC, Palmarini M. Pregnancy recognition and conceptus implantation in domestic ruminants: roles of progesterone, interferons and endogenous retroviruses. Reprod Fertil Dev 2007; 19:65-78.
35. Clemente M, Lopez-Vidriero I, O'Gaora P, Mehta JP, Forde N, Gutierrez-Adan A, Lonergan P, Rizos D. Transcriptome changes at the initiation of elongation in the bovine conceptus. Biol Reprod 2011; 85:285-295.
36. Skaug B, Chen ZJ. Emerging role of ISG15 in antiviral immunity. Cell 2010; 143:187-190.
37. Yang L, Wang XL, Wan PC, Zhang LY, Wu Y, Tang DW, Zeng SM. Upregulation of expression of interferon-stimulated gene 15 in the bovine corpus luteum during early pregnancy. J Dairy Sci 2010; 93:1000-1011.
38. Andersen JB, Hassel BA. The interferon regulated ubiquitin-like protein, ISG15, in tumorigenesis: friend or foe? Cytokine Growth Factor Rev 2006; 17:411-421.
39. Han H, Austin KJ, Rempel LA, Hansen TR. Low blood ISG15 mRNA and progesterone levels are predictive of non-pregnant dairy cows. J Endocrinol 2006; 191:505-512.
40. Rempel LA, Francis BR, Austin KJ, Hansen TR. Isolation and sequence of an interferon-tau-inducible, pregnancy- and bovine interferon-stimulated gene product 15 (ISG15)-specific, bovine ubiquitin-activating E1-like (UBE1L) enzyme. Biol Reprod 2005; 72:365-372.
41. Green JC, Okamura CS, Poock SE, Lucy MC. Measurement of interferontau (IFN-tau) stimulated gene expression in blood leukocytes for pregnancy diagnosis within 18-20d after insemination in dairy cattle. Anim Reprod Sci 2010; 121:24-33.
42. Li Q, Zhang M, Kumar S, Zhu LJ, Chen D, Bagchi MK, Bagchi IC. Identification and implantation stage-specific expression of an interferonalpha-regulated gene in human and rat endometrium. Endocrinology 2001; 142:2390-2400.
43. Fensterl V, Sen GC. The ISG56/IFIT1 gene family. J Interferon Cytokine Res 2011; 31:71-78.
44. Bonnevie-Nielsen V, Field LL, Lu S, Zheng DJ, Li M, Martensen PM, Nielsen TB, Beck-Nielsen H, Lau YL, Pociot F. Variation in antiviral 20,50-oligoadenylate synthetase (2050AS) enzyme activity is controlled by a single-nucleotide polymorphism at a splice-acceptor site in the OAS1 gene. Am J Hum Genet 2005; 76:623-633.
45. Seo JY, Yaneva R, Hinson ER, Cresswell P. Human cytomegalovirus directly induces the antiviral protein viperin to enhance infectivity. Science 2011; 332:1093-1097.
46. Fitzgerald KA. The interferon inducible gene: Viperin. J Interferon Cytokine Res 2011; 31:131-135.
47. Spencer TE, Bazer FW. Uterine and placental factors regulating conceptus growth in domestic animals. J Anim Sci 2004; 82E(suppl):E4-E13.
48. Spencer TE, Sandra O, Wolf E. Genes involved in conceptus-endometrial interactions in ruminants: insights from reductionism and thoughts on holistic approaches. Reproduction 2008; 135:165-179.
49. Tanimura K, Nakago S, Murakoshi H, Takekida S, Moriyama T, Matsuo H, Hashimoto K, Maruo T. Changes in the expression and cytological localization of betacellulin and its receptors (ErbB-1 and ErbB-4) in the trophoblasts in human placenta over the course of pregnancy. Eur J Endocrinol 2004; 151:93-101.
50. Naldini L, Tamagnone L, Vigna E, Sachs M, Hartmann G, Birchmeier W, Daikuhara Y, Tsubouchi H, Blasi F, Comoglio PM. Extracellular proteolytic cleavage by urokinase is required for activation of hepatocyte growth factor/scatter factor. EMBO J 1992; 11:4825-4833.
51. Ueki I, Ooi GT, Tremblay ML, Hurst KR, Bach LA, Boisclair YR. Inactivation of the acid labile subunit gene in mice results in mildretardation of postnatal growth despite profound disruptions in the circulating insulin-like growth factor system. Proc Natl Acad Sci U S A 2000; 97:6868-6873.
52. Lee SJ, McPherron AC. Regulation of myostatin activity and muscle growth. Proc Natl Acad Sci U S A 2001; 98:9306-9311.
53. Bazer FW, Wu G, Johnson GA, Kim J, Song G. Uterine histotroph and conceptus development: select nutrients and secreted phosphoprotein 1 affect mechanistic target of rapamycin cell signaling in ewes. Biol Reprod 2011; 85:1094-1107.
54. Haga A, Tanaka N, Funasaka T, Hashimoto K, Nakamura KT, Watanabe H, Raz A, Nagase H. The autocrine motility factor (AMF) and AMFreceptor combination needs sugar chain recognition ability and interaction using the C-terminal region of AMF. J Mol Biol 2006; 358:741-753.
55. Purwana IN, Kanasaki H, Mijiddorj T, Oride A, Miyazaki K. Induction of dual-specificity phosphatase 1 (DUSP1) by pulsatile gonadotropinreleasing hormone stimulation: role for gonadotropin subunit expression in mouse pituitary LbetaT2 cells. Biol Reprod 2011; 84:996-1004.
56. Berry C, Touyz R, Dominiczak AF, Webb RC, Johns DG. Angiotensin receptors: signaling, vascular pathophysiology, and interactions with ceramide. Am J Physiol Heart Circ Physiol 2001; 281:H2337-H2365.
57. Moestrup SK, Schousboe I, Jacobsen C, Leheste JR, Christensen EI, Willnow TE. Beta2-glycoprotein-I (apolipoprotein H) and beta2-glycoprotein-I-phospholipid complex harbor a recognition site for the endocytic receptor megalin. J Clin Invest 1998; 102:902-909.
58. Nolte MA, Arens R, van Os R, van Oosterwijk M, Hooibrink B, van Lier RA, van Oers MH. Immune activation modulates hematopoiesis through interactions between CD27 and CD70. Nat Immunol 2005; 6:412-418.
59. Koch JM, Ramadoss J, Magness RR. Proteomic profile of uterine luminal fluid from early pregnant ewes. J Proteome Res 2010; 9:3878-3885.
60. Riley SC, Findlay JK, Salamonsen LA. Endothelin-1 and endothelin receptors are present in the sheep uterus and conceptus at implantation. J Endocrinol 1995; 147:235-244.
61. Peterson AJ, Ledgard AM, Hodgkinson SC. The proteolysis of insulin-like growth factor binding proteins in ovine uterine luminal fluid. Reprod Fertil Dev 1998; 10:309-314.
62. Munoz M, Corrales FJ, Caamano JN, Diez C, Trigal B, Mora MI, Martin D, Carrocera S, Gomez E. Proteome of the early embryo-maternal dialogue in the cattle uterus. J Proteome Res 2012; 11:751-766.
63. Roy SC, Ghosh J. Dynamic in vivo changes in the activities of gelatinases, matrix metalloproteinases (MMPs), and tissue inhibitor of metalloproteinases (TIMPs) in buffalo (Bubalus bubalis) uterine luminal fluid during estrous cycle and early pregnancy. Mol Reprod Dev 2010; 77:944-953.
64. Adams KL, Bazer FW, Roberts RM. Progesterone-induced secretion of a retinol-binding protein in the pig uterus. J Reprod Fertil 1981; 62:39-47.
65. Kayser JP, Kim JG, Cerny RL, Vallet JL. Global characterization of porcine intrauterine proteins during early pregnancy. Reproduction 2006; 131:379-388.
66. Brigstock DR, Kim GY, Steffen CL. Pig uterine luminal fluid contains the developmentally regulated neurotrophic factor, pleiotrophin. J Endocrinol 1996; 148:103-111.
67. Casado-Vela J, Rodriguez-Suarez E, Iloro I, Ametzazurra A, Alkorta N, Garcia-Velasco JA, Matorras R, Prieto B, Gonzalez S, Nagore D, Simon L, Elortza F. Comprehensive proteomic analysis of human endometrial fluid aspirate. J Proteome Res 2009; 8:4622-4632.
68. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 2008; 5:621-628.