Early developing pig embryos mediate their own environment in the maternal tract

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Almiñana, Carmen ^a   Heath, Paul R ^b   Wilkinson, Stephen ^a   Sanchez Osorio, Jonatan ^c   Cuello, Cristina ^c   Parrilla, Inmaculada ^c   Gil, Maria A ^c   Vazquez, Jose L ^c   Vazquez, Juan Maria ^c   Roca, Jordi ^c   Martinez, Emilio A ^c   Fazeli, Alireza ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c UNIVERSITY OF MURCIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; MESSENGER RNA; ORGANIC ANION TRANSPORTER 1; PROTEIN RDX; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 2; UNCLASSIFIED DRUG; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; ARTIFICIAL INSEMINATION; BLASTOCYST; COMPUTER ANALYSIS; CONTROLLED STUDY; DOWN REGULATION; EMBRYO DEVELOPMENT; EXPERIMENTAL MODEL; FEMALE; FEMALE GENITAL SYSTEM; FETOPLACENTAL UNIT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; IMMUNE SYSTEM; IMMUNOMODULATION; IN VIVO STUDY; LAPAROSCOPIC INSEMINATION; MALE; MATHEMATICAL MODEL; MICROARRAY ANALYSIS; NONHUMAN; OOCYTE; OVIDUCT; PORCINE EMBRYO; SWINE; UTERUS HORN; ANIMAL; ANIMAL EMBRYO; DNA MICROARRAY; GENETICS; METABOLISM; PHYSIOLOGY; PREGNANCY; PRENATAL DEVELOPMENT; SIGNAL TRANSDUCTION; UTERUS;

SUIDAE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BLASTOCYST; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; FEMALE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PREGNANCY; SIGNAL TRANSDUCTION; SWINE; TOLL-LIKE RECEPTOR 4; UTERUS;

EID: 84859097237     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0033625     Document Type: Article

References (60)

1. Haouzi D, Assou S, Mahmoud K, Tondeur S, Reme T, et al. (2009) Gene expression profile of human endometrial receptivity: comparison between natural and stimulated cycles for the same patients. Hum Reprod 24: 1436-1445.
2. Fazeli A, (2008) Maternal communication with gametes and embryos. Theriogenology 70: 1182-1187.
3. Pope W, (1994) Embryonic mortality in swine; In: Geisert Rd ZM, editors. Boca Raton CRS Press pp. 53-77.
4. Simon C, Moreno C, Remohi J, Pellicer A, (1998) Molecular interactions between embryo and uterus in the adhesion phase of human implantation. Hum Reprod 13 (Suppl 3): 219-232; discussion 233-216.
5. Wolf E, Arnold GJ, Bauersachs S, Beier HM, Blum H, et al. (2003) Embryo-maternal communication in bovine- strategies for deciphering a complex cross-talk. Reprod Domest Anim 38: 276-289.
6. Gluckman PDaHMA, (2006) The developmental origins of health and disease: an overview. In: Gluckman P, Hanson Me, editors. Developmental Origins of Health and Disease. Developmental Origins of Health and Disease Cambridge, UK, Cambridge University Press Cambridge University Press.
7. Baker DJ, (1998) Mothers, babies and Health in later life Edinburgh Churchill Livingstone.
8. Fleming TP, Kwong WY, Porter R, Ursell E, Fesenko I, et al. (2004) The embryo and its future. Biol Reprod 71: 1046-1054.
9. Vickers MH, Krechowec SO, Breier BH, (2007) Is later obesity programmed in utero? Curr Drug Targets 8: 923-934.
10. Lee KF, Yao YQ, Kwok KL, Xu JS, Yeung WS, (2002) Early developing embryos affect the gene expression patterns in the mouse oviduct. Biochem Biophys Res Commun 292: 564-570.
11. Klein C, Scoggin KE, Ealy AD, Troedsson MH, (2010) Transcriptional profiling of equine endometrium during the time of maternal recognition of pregnancy. Biol Reprod 83: 102-113.
12. Spencer TE, Johnson GA, Bazer FW, Burghardt RC, Palmarini M, (2007) Pregnancy recognition and conceptus implantation in domestic ruminants: roles of progesterone, interferons and endogenous retroviruses. Reprod Fertil Dev 19: 65-78.
13. Yoshinaga K, Adams CE, (1966) Delayed implantation in the spayed, progesterone treated adult mouse. J Reprod Fertil 12: 593-595.
14. Dey SK, (1996) Implantation Lippincott-Raven, Philadelphia Adashi, E.Y.,et al (Eds).
15. Lee KF, Kwok KL, Yeung WS, (2000) Suppression subtractive hybridization identifies genes expressed in oviduct during mouse preimplantation period. Biochem Biophys Res Commun 277: 680-685.
16. Bauersachs S, Ulbrich SE, Gross K, Schmidt SE, Meyer HH, et al. (2006) Embryo-induced transcriptome changes in bovine endometrium reveal species-specific and common molecular markers of uterine receptivity. Reproduction 132: 319-331.
17. Klein C, Bauersachs S, Ulbrich SE, Einspanier R, Meyer HH, et al. (2006) Monozygotic twin model reveals novel embryo-induced transcriptome changes of bovine endometrium in the preattachment period. Biol Reprod 74: 253-264.
18. Walker CG, Meier S, Littlejohn MD, Lehnert K, Roche JR, et al. (2010) Modulation of the maternal immune system by the pre-implantation embryo. BMC Genomics 11: 474.
19. Chang HS, Cheng WT, Wu HK, Choo KB, (2000) Identification of genes expressed in the epithelium of porcine oviduct containing early embryos at various stages of development. Mol Reprod Dev 56: 331-335.
20. Ka H, Seo H, Kim M, Choi Y, Lee CK, (2009) Identification of differentially expressed genes in the uterine endometrium on day 13of the estrous cycle and pregnancy in pigs. Mol Reprod Dev 76: 75-84.
21. Ostrup E, Bauersachs S, Blum H, Wolf E, Hyttel P, (2010) Differential endometrial gene expression in pregnant and nonpregnant sows. Biol Reprod 83: 277-285.
22. Horcajadas JA, Riesewijk A, Martin J, Cervero A, Mosselman S, et al. (2004) Global gene expression profiling of human endometrial receptivity. J Reprod Immunol 63: 41-49.
23. Roberts RM, Ealy AD, Alexenko AP, Han CS, Ezashi T, (1999) Trophoblast interferons. Placenta 20: 259-264.
24. Spencer TE, Bazer FW, (1995) Temporal and spatial alterations in uterine estrogen receptor and progesterone receptor gene expression during the estrous cycle and early pregnancy in the ewe. Biol Reprod 53: 1527-1543.
25. Spencer TE, Bazer FW, (2004) Conceptus signals for establishment and maintenance of pregnancy. Reprod Biol Endocrinol 2: 49.
26. Hendriks BS, Hua F, Chabot JR, (2008) Analysis of mechanistic pathway models in drug discovery: p38 pathway. Biotechnol Prog 24: 96-109.
27. Wilkinson SJ, Benson N, Kell DB, (2008) Proximate parameter tuning for biochemical networks with uncertain kinetic parameters. Mol Biosyst 4: 74-97.
28. An GC, Faeder JR, (2009) Detailed qualitative dynamic knowledge representation using a BioNetGen model of TLR-4 signaling and preconditioning. Math Biosci 217: 53-63.
29. Soede NM, Noordhuizen JP, Kemp B, (1992) The duration of ovulation in pigs, studied by transrectal ultrasonography, is not related to early embryonic diversity. Theriogenology 38: 653-666.
30. Bolarin A, Vazquez JM, Parrilla I, Vazquez JL, Martinez EA, et al. (2009) Validation of trans-rectal ultrasonography for counting preovulatory follicles in weaned sows. Anim Reprod Sci 113: 137-142.
31. Johnson LA, Pursel VG, (1975) Effect of age of boars on testicular lipids and fatty acids. J Anim Sci 40: 108-113.
32. Hernandez M, Roca J, Calvete JJ, Sanz L, Muino-Blanco T, et al. (2007) Cryosurvival and in vitro fertilizing capacity postthaw is improved when boar spermatozoa are frozen in the presence of seminal plasma from good freezer boars. J Androl 28: 689-697.
33. Tsai S, Mir B, Martin AC, Estrada JL, Bischoff SR, et al. (2006) Detection of transcriptional difference of porcine imprinted genes using different microarray platforms. BMC Genomics 7: 328.
34. Wolfinger RD, Gibson G, Wolfinger ED, Bennett L, Hamadeh H, et al. (2001) Assessing gene significance from cDNA microarray expression data via mixed models. J Comput Biol 8: 625-637.
35. Kanehisa M, Goto S, Hattori M, Aoki-Kinoshita KF, Itoh M, et al. (2006) From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res 34: D354-357.
36. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
37. Matsumoto H, Daikoku T, Wang H, Sato E, Dey SK, (2004) Differential expression of ezrin/radixin/moesin (ERM) and ERM-associated adhesion molecules in the blastocyst and uterus suggests their functions during implantation. Biol Reprod 70: 729-736.
38. Martin JC, Jasper MJ, Valbuena D, Meseguer M, Remohi J, et al. (2000) Increased adhesiveness in cultured endometrial-derived cells is related to the absence of moesin expression. Biol Reprod 63: 1370-1376.
39. Patel P, Weerasekera N, Hitchins M, Boyd CA, Johnston DG, et al. (2003) Semi quantitative expression analysis of MDR3, FIC1, BSEP, OATP-A, OATP-C,OATP-D, OATP-E and NTCP gene transcripts in 1st and 3rd trimester human placenta. Placenta 24: 39-44.
40. Loubiere LS, Vasilopoulou E, Bulmer JN, Taylor PM, Stieger B, et al. (2010) Expression of thyroid hormone transporters in the human placenta and changes associated with intrauterine growth restriction. Placenta 31: 295-304.
41. Ross JW, Ashworth MD, Mathew D, Reagan P, Ritchey JW, et al. (2010) Activation of the transcription factor, nuclear factor kappa-B, during the estrous cycle and early pregnancy in the pig. Reprod Biol Endocrinol 8: 39.
42. Koga K, Mor G, (2010) Toll-like receptors at the maternal-fetal interface in normal pregnancy and pregnancy disorders. Am J Reprod Immunol 63: 587-600.
43. Riesewijk A, Martin J, van Os R, Horcajadas JA, Polman J, et al. (2003) Gene expression profiling of human endometrial receptivity on days LH+3versus LH+7 by microarray technology. Mol Hum Reprod 9: 253-264.
44. Klein C, Troedsson MH, (2011) Transcriptional profiling of equine conceptuses reveals new aspects of embryo-maternal communication in the horse. Biol Reprod 84: 872-885.
45. Reese J, Das SK, Paria BC, Lim H, Song H, et al. (2001) Global gene expression analysis to identify molecular markers of uterine receptivity and embryo implantation. J Biol Chem 276: 44137-44145.
46. Kell DB, (2004) Metabolomics and systems biology: making sense of the soup. Current Opinion in Microbiology 7: 296-307.
47. Wilkinson DJ, (2009) Stochastic modelling for quantitative description of heterogeneous biological systems. Nat Rev Genet 10: 122-133.
48. Oda K, Kitano H, (2006) A comprehensive map of the toll-like receptor signaling network. Mol Syst Biol 2: 2006 0015.
49. Faeder JBML, Hlavacek WS, (2008) Rule-based modeling of biochemical systems with BioNetGen. Methods in Molecular Biology: Systems Biology Totowa, NJ Humana Press.
50. Aboussahoud W, Bruce C, Elliott S, Fazeli A, (2010) Activation of Toll-like receptor 5 decreases the attachment of human trophoblast cells to endometrial cells in vitro. Hum Reprod 25: 2217-2228.
51. Geisert RD, Zavy MT, Moffatt RJ, Blair RM, Yellin T, (1990) Embryonic steroids and the establishment of pregnancy in pigs. J Reprod Fertil Suppl 40: 293-305.
52. Ziecik AJ, (2002) Old, new and the newest concepts of inhibition of luteolysis during early pregnancy in pig. Domest Anim Endocrinol 23: 265-275.
53. Fujiwara H, Araki Y, Toshimori K, (2009) Is the zona pellucida an intrinsic source of signals activating maternal recognition of the developing mammalian embryo? J Reprod Immunol 81: 1-8.
54. Denker HW, (2000) Structural dynamics and function of early embryonic coats. Cells Tissues Organs 166: 180-207.
55. Dumont JN, Brummett AR, (1985) Egg envelopes in vertebrates. Dev Biol (N Y 1985) 1: 235-288.
56. Rath D, Topfer-Petersen E, Michelmann HW, Schwartz P, von Witzendorff D, et al. (2006) Structural, biochemical and functional aspects of sperm-oocyte interactions in pigs. Soc Reprod Fertil Suppl 62: 317-330.
57. Michelmann HW, Rath D, Topfer-Petersen E, Schwartz P, (2007) Structural and functional events on the porcine zona pellucida during maturation, fertilization and embryonic development: a scanning electron microscopy analysis. Reprod Domest Anim 42: 594-602.
58. Herrler A, Beier HM, (2000) Early embryonic coats: morphology, function, practical applications. An overview. Cells Tissues Organs 166: 233-246.
59. Telford NA, Watson AJ, Schultz GA, (1990) Transition from maternal to embryonic control in early mammalian development: a comparison of several species. Mol Reprod Dev 26: 90-100.
60. Wakuda K, Takakura K, Nakanishi K, Kita N, Shi H, et al. (1999) Embryo-dependent induction of embryo receptivity in the mouse endometrium. J Reprod Fertil 115: 315-324.