'Conceptualizing' the endometrium: Identification of conceptus-derived proteins during early pregnancy in cattle

Biology of Reproduction

Volumn 92, Issue 6, 2015, Pages

  Forde, Niamh ^a   Bazer, Fuller W ^b   Spencer, Thomas E ^c   Lonergan, Pat ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

^b TEXAS A AND M UNIVERSITY   (United States)

^c UNIVERSITY OF MISSOURI   (United States)

Author keywords

Conceptus; Endometrium; Gene expression; Proteomics; Uterine luminal fluid

Indexed keywords

ACONITATE HYDRATASE; ACONITATE HYDRATASE 2; ACTIN RELATED PROTEIN 2-3 COMPLEX; ALPHA ACTININ 1; BETA GALACTOSIDASE; CREATINE KINASE; CREATINE KINASE U TYPE; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE TYPE II ALPHA REGULATORY SUBUNIT; EARLY PREGNANCY FACTOR; ELONGATION FACTOR 2; GALECTIN 3; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN A1; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN A2 B1 ISOFORM A2; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN F; INTERFERON TAU 3; ISOCITRATE DEHYDROGENASE 2; KERATIN TYPE II; KERATIN TYPE II CYTOSKELETAL 75; MESSENGER RNA; PROTEIN; PROTEIN 14 3 3; PROTEIN 14 3 3 GAMMA; PROTEINASE; PSMC4 PROTEIN; RIBONUCLEOPROTEIN; RNA; TAU INTERFERON; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BOVINE; CONCEPTION; CONTROLLED STUDY; CULTURE MEDIUM; ENDOMETRIUM; FIRST TRIMESTER PREGNANCY; HEIFER; IN VITRO STUDY; IN VIVO STUDY; LIQUID CHROMATOGRAPHY; MOLECULAR RECOGNITION; NANO LIQUID CHROMATOGRAPHY TANDEM MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEOMICS; RNA SEQUENCE; TANDEM MASS SPECTROMETRY; UTERINE LUMINAL FLUID; UTERUS FLUID; ANIMAL; BREEDING; FEMALE; FETUS; GENE EXPRESSION PROFILING; METABOLISM; PREGNANCY;

BOS;

ANIMALS; CATTLE; ENDOMETRIUM; FEMALE; FETUS; GENE EXPRESSION PROFILING; PREGNANCY; PREGNANCY, ANIMAL;

EID: 84936929253     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.115.129296     Document Type: Article

References (49)

1. Forde N, Lonergan P. Transcriptomic analysis of the bovine endometrium: what is required to establish uterine receptivity to implantation in cattle? J Reprod Dev 2012; 58:189-195.
2. 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.
3. Carter F, Forde N, Duffy P, Wade M, Fair T, Crowe MA, Evans AC, Kenny DA, Roche JF, Lonergan P. Effect of increasing progesterone concentration from Day 3 of pregnancy on subsequent embryo survival and development in beef heifers. Reprod Fertil Dev 2008; 20:368-375.
4. 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.
5. Satterfield MC, Bazer FW, Spencer TE. Progesterone regulation of preimplantation conceptus growth and galectin 15 (LGALS15) in the ovine uterus. Biol Reprod 2006; 75:289-296.
6. Geisert RD, Fox TC, Morgan GL, Wells ME, Wettemann RP, Zavy MT. Survival of bovine embryos transferred to progesterone-treated asynchronous recipients. J Reprod Fertil 1991; 92:475-482.
7. O'Hara L, Forde N, Carter F, Rizos D, Maillo V, Ealy AD, Kelly AK, Rodriguez P, Isaka N, Evans AC, Lonergan P. Paradoxical effect of supplementary progesterone between Day 3 and Day 7 on corpus luteum function and conceptus development in cattle. Reprod Fertil Dev 2014; 26: 328-336.
8. 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.
9. 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.
10. Bott RC, Ashley RL, Henkes LE, Antoniazzi AQ, Bruemmer JE, Niswender GD, Bazer FW, Spencer TE, Smirnova NP, Anthony RV, Hansen TR. Uterine vein infusion of interferon tau (IFNT) extends luteal life span in ewes. Biol Reprod 2010; 82:725-735.
11. 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.
12. Mansouri-Attia N, Aubert J, Reinaud P, Giraud-Delville C, Taghouti G, Galio L, Everts RE, Degrelle S, Richard C, Hue I, Yang X, Tian XC, et al. Gene expression profiles of bovine caruncular and intercaruncular endometrium at implantation. Physiol Genomics 2009; 39:14-27.
13. 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.
14. Bazer FW, Burghardt RC, Johnson GA, Spencer TE, Wu G. Interferons and progesterone for establishment and maintenance of pregnancy: interactions among novel cell signaling pathways. Reprod Biol 2008; 8: 179-211.
15. 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.
16. Forde N, Duffy GB, McGettigan PA, Browne JA, Mehta JP, Kelly AK, Mansouri-Attia N, Sandra O, Loftus BJ, Crowe MA, Fair T, Roche JF, et al. Evidence for an early endometrial response to pregnancy in cattle: both dependent upon and independent of interferon tau. Physiol Genomics 2012; 44:799-810.
17. Bartol FF, Roberts RM, Bazer FW, Lewis GS, Godkin JD, Thatcher WW. Characterization of proteins produced in vitro by periattachment bovine conceptuses. Biol Reprod 1985; 32:681-693.
18. Godkin JD, Bazer FW, Moffatt J, Sessions F, Roberts RM. Purification and properties of a major, low molecular weight protein released by the trophoblast of sheep blastocysts at day 13-21. J Reprod Fertil 1982; 65: 141-150.
19. Godkin JD, Bazer FW, Lewis GS, Geisert RD, Roberts RM. Synthesis and release of polypeptides by pig conceptuses during the period of blastocyst elongation and attachment. Biol Reprod 1982; 27:977-987.
20. Masters RA, Roberts RM, Lewis GS, Thatcher WW, Bazer FW, Godkin JD. High molecular weight glycoproteins released by expanding, preattachment sheep, pig and cow blastocysts in culture. J Reprod Fertil 1982; 66:571-583.
21. Dorniak P, Bazer FW, Spencer TE. Prostaglandins regulate conceptus elongation and mediate effects of interferon tau on the ovine uterine endometrium. Biol Reprod 2011; 84:1119-1127.
22. Dorniak P, Welsh TH Jr, Bazer FW, Spencer TE. Endometrial HSD11B1 and cortisol regeneration in the ovine uterus: effects of pregnancy, interferon tau, and prostaglandins. Biol Reprod 2011; 86:124.
23. Spencer TE, Forde N, Dorniak P, Hansen TR, Romero JJ, Lonergan P. Conceptus-derived prostaglandins regulate gene expression in the endometrium prior to pregnancy recognition in ruminants. Reproduction 2013; 146:377-387.
24. Forde N, McGettigan PA, Mehta JP, O'Hara L, Mamo S, Bazer FW, Spencer TE, Lonergan P. Proteomic analysis of uterine fluid during the pre-implantation period of pregnancy in cattle. Reproduction 2014; 147: 575-587.
25. Mamo S, Mehta JP, Forde N, McGettigan P, Lonergan P. Conceptusendometrium crosstalk during maternal recognition of pregnancy in cattle. Biol Reprod 2012; 87:6.
26. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010; 26:139-140.
27. Tabb DL. What's driving false discovery rates? J Proteome Res 2008; 7: 45-46.
28. GeneCards. Rehovot, Israel: Weizmann Institute of Science. www.genecards.org. Accessed 20 January 2015.
29. Forde N, Mehta JP, McGettigan PA, Mamo S, Bazer FW, Spencer TE, Lonergan P. Alterations in expression of endometrial genes coding for proteins secreted into the uterine lumen during conceptus elongation in cattle. BMC Genomics 2013; 14:321.
30. Ledgard AM, Lee RS, Peterson AJ. Bovine endometrial legumain and TIMP-2 regulation in response to presence of a conceptus. Mol Reprod Dev 2009; 76:65-74.
31. Song G, Spencer TE, Bazer FW. Cathepsins in the ovine uterus: regulation by pregnancy, progesterone, and interferon tau. Endocrinology 2005; 146: 4825-4833.
32. Simmons RM, Erikson DW, Kim J, Burghardt RC, Bazer FW, Johnson GA, Spencer TE. Insulin-like growth factor binding protein one in the ruminant uterus: potential endometrial marker and regulator of conceptus elongation. Endocrinology 2009; 150:4295-4305.
33. Okumu LA, Fair T, Szekeres-Bartho J, O'Doherty AM, Crowe MA, Roche JF, Lonergan P, Forde N. Endometrial expression of progesterone induced blocking factor and galectins-1,-3,-9 and-3 binding protein in the luteal phase and early pregnancy in cattle. Physiol Genomics 2011; 43: 903-910.
34. Satterfield MC, Song G, Kochan KJ, Riggs PK, Simmons RM, Elsik CG, Adelson DL, Bazer FW, Zhou H, Spencer TE. Discovery of candidate genes and pathways in the endometrium regulating ovine blastocyst growth and conceptus elongation. Physiol Genomics 2009; 39:85-99.
35. Dore JJ, Roberts MP, Godkin JD. Early gestational expression of retinolbinding protein mRNA by the ovine conceptus and endometrium. Mol Reprod Dev 1994; 38:24-29.
36. MacKenzie SH, Roberts MP, Liu KH, Dore JJ, Godkin JD. Bovine endometrial retinol-binding protein secretion, messenger ribonucleic acid expression, and cellular localization during the estrous cycle and early pregnancy. Biol Reprod 1997; 57:1445-1450.
37. Mullen MP, Forde N, Parr MH, Diskin MG, Morris DG, Nally JE, Evans AC, Crowe MA. Alterations in systemic concentrations of progesterone during the early luteal phase affect RBP4 expression in the bovine uterus. Reprod Fertil Dev 2012; 24:715-722.
38. Dorniak P, Bazer FW, Spencer TE. Biological role of interferon tau in endometrial function and conceptus elongation. J Anim Sci 2013; 91(4): 1627-1638.
39. Austin KJ, Ward SK, Teixeira MG, Dean VC, Moore DW, Hansen TR. Ubiquitin cross-reactive protein is released by the bovine uterus in response to interferon during early pregnancy. Biol Reprod 1996; 54: 600-606.
40. Johnson GA, Spencer TE, Hansen TR, Austin KJ, Burghardt RC, Bazer FW. Expression of the interferon tau inducible ubiquitin cross-reactive protein in the ovine uterus. Biol Reprod 1999; 61:312-318.
41. Toyokawa K, Carling SJ, Ott TL. Cellular localization and function of the antiviral protein, ovine Mx1 (oMx1): I. Ovine Mx1 is secreted by endometrial epithelial cells via an 'unconventional' secretory pathway. Am J Reprod Immunol 2007; 57:13-22.
42. Black SG, Arnaud F, Burghardt RC, Satterfield MC, Fleming JA, Long CR, Hanna C, Murphy L, Biek R, Palmarini M, Spencer TE. Viral particles of endogenous betaretroviruses are released in the sheep uterus and infect the conceptus trophectoderm in a transspecies embryo transfer model. J Virol 2010; 84:9078-9085.
43. Ruiz-Gonzalez I, Xu J, Wang X, Burghardt RC, Dunlap K, Bazer FW. Exosomes, endogenous retroviruses and toll-like receptors: pregnancy recognition in ewes. Reproduction 2015; 149(3):281-291.
44. Burns G, Brooks K, Wildung M, Navakanitworakul R, Christenson LK, Spencer TE. Extracellular vesicles in luminal fluid of the ovine uterus. PLoS One 9:e90913.
45. Kropp J, Salih SM, Khatib H. Expression of microRNAs in bovine and human pre-implantation embryo culture media. Front Genet 2014; 5:91.
46. Rosenbluth EM, Shelton DN, Wells LM, Sparks AE, Van Voorhis BJ. Human embryos secrete microRNAs into culture media-a potential biomarker for implantation. Fertil Steril 2014; 101:1493-1500.
47. Lewis SK, Farmer JL, Burghardt RC, Newton GR, Johnson GA, Adelson DL, Bazer FW, Spencer TE. Galectin 15 (LGALS15): a gene uniquely expressed in the uteri of sheep and goats that functions in trophoblast attachment. Biol Reprod 2007; 77:1027-1036.
48. Ishihama Y, Oda Y, Tabata T, Sato T, Nagasu T, Rappsilber J, Mann M. Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics 2005; 4:1265-1272.
49. 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.