The transcriptome signature of the receptive bovine uterus determined at early gestation

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Binelli, Mario ^a   Scolari, Saara C ^a   Pugliesi, Guilherme ^a   Van Hoeck, Veerle ^a   Gonella Diaza, Angela M ^a   Andrade, Sónia C S ^a   Gasparin, Gustavo R ^b   Coutinho, Luiz L ^b  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b Laboratório de Genética Animal Departamento de Zootecnia ESALQUSP   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

PROGESTERONE; TRANSCRIPTOME;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEEF CATTLE; BLOOD SAMPLING; CONTROLLED STUDY; CORPUS LUTEUM; ESTRUS; FEMALE; GENE EXPRESSION REGULATION; GENE MAPPING; GENETIC TRANSCRIPTION; GENOME ANALYSIS; GESTATION PERIOD; MICROSOME; NONHUMAN; PREGNANCY OUTCOME; PROGESTERONE BLOOD LEVEL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RNA SEQUENCE; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; TAURINE CATTLE; UPREGULATION; UTERUS; UTERUS BIOPSY; ANIMAL; BOVINE; GENE EXPRESSION PROFILING; GENETICS; PHYSIOLOGY; PREGNANCY;

BOS; BOS TAURUS; BOVINAE;

ANIMALS; CATTLE; FEMALE; GENE EXPRESSION PROFILING; PREGNANCY; PREGNANCY OUTCOME; REAL-TIME POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, RNA; UTERUS;

EID: 84928910655     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0122874     Document Type: Article

References (44)

1. Santos JEP, Thatcher WW, Chebel RC, Cerri R LA, Galvão KN. The effect of embryonic death rates in cattle on the efficacy of estrus synchronization programs. Anim Reprod Sci. 2014; 82: 513-535.
2. Grimard B, Freret S, Chevallier A, Pinto A, Ponsart C, Humblot P. Genetic and environmental factors influencing first service conception rate and late embryonic/foetal mortality in low fertility dairy herds. Anim Reprod Sci. 2006; 91: 31-44. PMID: 16310097
3. Berg DK, van Leeuwen J, Beaumont S, Berg M, Pfeffer PL. Embryo loss in cattle between Days 7 and 16 of pregnancy. Therio. 2010; 73: 250-260.
4. Spencer TE, Bazer FW. Uterine and placental factors regulating conceptus growth in domestic animals. Journal of Anim Science. 2004; 82: 4-13.
5. Forde N, Spencer TE, Bazer FW, Song G, Roche JF, Lonergan P. Effect of pregnancy and progesterone concentration on expression of genes encoding for transporters or secreted proteins in the bovine endometrium. Phys Gen. 2010; 41: 53-62. PMID: 22081757
6. Kim JY, Burghardt RC, Wu G, Johnson GA, Spencer TE, Bazer FW. Select nutrients in the ovine uterine lumen. VII. Effects of arginine, leucine, glutamine, and glucose on trophectoderm cell signaling, proliferation, and migration. Biol Reprod. 2011; 84: 62-69. doi: 10.1095/biolreprod.110.085738 PMID: 20844282
7. Clemente M, de La Fuente J, Fair T, Al Naib A, Gutierrez-Adan A, Roche JF et al. Progesterone and conceptus elongation in cattle: a direct effect on the embryo or an indirect effect via the endometrium? Repr. 2009; 138: 507-517.
8. Forde N, Beltman ME, Duffy GB, Duffy P, Mehta JP, O'Gaora P et al. 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. doi: 10.1095/biolreprod.110.085910 PMID: 20881316
9. Kaloglu C, Onarlioglu B. Extracellular matrix remodelling in rat endometrium during early pregnancy: the role of fibronectin and laminin. Tissue Cell. 2010; 42: 301-306. doi: 10.1016/j.tice.2010.07.004 PMID: 20810141
10. Forde N, Carter F, Spencer TE, Bazer FW, Sandra O, Mansouri Attia M, et al. Conceptus-induced changes in the endometrial transcriptome: how soon does the cow know she is pregnant? Biol Reprod. 2011; 85: 144-156. doi: 10.1095/biolreprod.110.090019 PMID: 21349821
11. Beltman ME, Forde N, Lonergan P, Crowe MA. Altered endometrial immune gene expression in beef heifers with retarded embryos. Reprod Fertil Dev. 2013; 25: 966-970. doi: 10.1071/RD12232 PMID: 23034328
12. Rashid NA, Lalitkumar S, Lalitkumar PG, Gemzell-Danielsson K. Endometrial receptivity and human embryo implantation. Am J Reprod Immunol. 2011; 66: 23-30. doi: 10.1111/j.1600-0897.2011.01048.x PMID: 21726335
13. Revel A. Defective endometrial receptivity. Fertil Steril. 2012; 97:1028-1032. doi: 10.1016/j.fertnstert. 2012.03.039 PMID: 22542142
14. Fatemi HM, Popovic-Todorovic B. Implantation in assisted reproduction: a look at endometrial receptivity. Reprod Biomed Online. 2013; 27: 530-538. doi: 10.1016/j.rbmo.2013.05.018 PMID: 23933035
15. Garrido-Gomez T, Ruiz-Alonso M, Blesa D, Diaz-Gimeno P, Vilella F Somón C. Profiling the gene signature of endometrial receptivity: clinical results. Fertil Steril. 2013; 99: 1078-1085. doi: 10.1016/j. fertnstert.2012.12.005 PMID: 23312228
16. Diaz-Gimeno P, Horcajadas JA, Martinez-Conejero JA, Esteban FJ, Alama P, Pellicer A et al. A genomic diagnostic tool for human endometrial receptivity based on the transcriptomic signature. Fertil Steril. 2011; 95: 50-60. doi: 10.1016/j.fertnstert.2010.04.063 PMID: 20619403
17. Ruiz-Alonso M, Blesa D, Díaz-Gimeno P, Gómez E, Fernández-Sánchez M, Carranza F et al. The endometrial receptivity array for diagnosis and personalized embryo transfer as a treatment for patients with repeated implantation failure. Fertil Steril. 2013; 100: 818-824. doi: 10.1016/j.fertnstert.2013.05. 004 PMID: 23756099
18. Salilew-Wondim D, Hölker M, Rings F, Ghanem N, Ulas-Cinar M, Peippo J, et al. Bovine pretransfer endometrium and embryo transcriptome fingerprints as predictors of pregnancy success after embryo transfer. Phys Gen. 2010; 42: 201-218.
19. 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. PMID: 22738902
20. Minten MA, Bilby TR, Bruno RG, Allen CC, Madsen CA, Wang Z, et al. Effects of fertility on gene expression and function of the bovine endometrium. PLoSOne. 2013. August 5. doi: 10.1371/journal. pone.0069444
21. Bauersachs S, Ulbrich SE, Gross K, Schmidt SE, Meyer HH, Wenigerkind H, et al. Embryo-induced transcriptome changes in bovine endometrium reveal species- specific and common molecular markers of uterine receptivity. Repr. 2006; 132: 319-331.
22. Pugliesi G, Scolari SC, Mesquita FS, Maturana Filho M, Araújo ER, Cardoso D, et al. Impact of probing the reproductive tract during early pregnancy on fertility of beef cows. Repr Dom Anim. 2014; 49: 35-39.
23. Mesquita FS, Pugliesi G, Scolari SC, França MR, Ramos RS, Oliveira M, et al. Manipulation of the periovulatory sex steroidal milieu affects endometrial but not luteal gene expression in early diestrus Nelore cows. Therio. 2014; 81: 861-869.
24. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nature Methods. 2012; 9: 357-359. doi: 10.1038/nmeth.1923 PMID: 22388286
25. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-Seq data with DESeq2. Genome Biol. 2014; 15: 550. PMID: 25516281
26. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 2004; 5: 80. PMID: 15461798
27. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. JRSS Series B. 1995; 289-300.
28. Dennis JR, Sherman G, Hosack BT, Yang DA, Gao J. DAVID: database for annotation, visualization, and integrated discovery. Genome Biol. 2003; 4: 3.
29. Baumann CG, Morris DG, Sreenan JM, Leese HJ. The quiet embryo hypothesis: molecular characteristics favoring viability. Mol Reprod Dev. 2007; 74: 1345-1353. PMID: 17342740
30. Ulbrich SE, Frohlich T, Schulke K, Englberger E, Waldschmitt N, Arnold GJ, et al. Evidence for estro-gen-dependent uterine serpin (SERPINA14) expression during estrus in the bovine endometrial glandular epithelium and lumen. Biol Reprod. 2009; 8: 795-805.
31. Binelli M, Pugliesi G, Van Hoeck V, Sponchiado M, Ramos RS, Oliveira M, et al. The role of proestrus on fertility and postovulatory uterine function in the cow. Anim Reprod. 2014; 11: 246-253.
32. Groothuis PG, Dassen HH, Romano A, Punyadeera C. Estrogen and the endometrium: lessons learned from gene expression profiling in rodents and human. Hum Reprod Update. 2007; 13: 405-417. PMID: 17584823
33. Brenner CA, Adler RR, Rappolee DA, Pedersen RA, Werb Z. Genes for extracellular-matrix-degrading metalloproteinases and their inhibitor, TIMP, are expressed during early mammalian development. Genes Dev. 1989; 3: 848-859. PMID: 2744464
34. Nissi R, Talvensaari-Mattila A, Kotila V, Niinimäki M, Järvelä I, Turpeenniemi-Hujane T. Circulating matrix metalloproteinase MMP-9 and MMP-2/TIMP-2 complex are associated with spontaneous early pregnancy failure. Reprod Biol Endocrinol. 2013; 11: 2. doi: 10.1186/1477-7827-11-2 PMID: 23320481
35. Favaro RR, Salgado RM, Covarrubias AC, Bruni F, Lima C, Fortes ZB, et al. Long-term type 1 diabetes impairs decidualization and extracellular matrix remodeling during early embryonic development in mice. Placenta. 2013; 34: 1128-1135. doi: 10.1016/j.placenta.2013.09.012 PMID: 24125804
36. Giudice LC. Potential biochemical markers of uterine receptivity. Hum Reprod. 1999; 14: 3-16. PMID: 10690796
37. Llobat L, Marco-Jiménez F, Peñaranda DS, Thieme R, Navarrete A, Vincente JS, et al. mRNA expression in rabbit blastocyst and endometrial tissue of candidate gene involved in gestational losses. Reprod Domest Anim. 2012; 47: 281-287. doi: 10.1111/rda.12073 PMID: 23279519
38. Murphy CR. The cytoskeleton of uterine epithelial cells: a new player in uterine receptivity and the plasma membrane transformation. Hum Reprod Update. 1995; 1: 567-580. PMID: 9079397
39. Forde N, Duffy GB, McGettigan PA, Browne JA, Mehta JP, Kelly AK, 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. doi: 10.1152/physiolgenomics.00067.2012 PMID: 22759920
40. Walker CG, Littlejohn MD, Mitchell MD, Roche JR, Meier S. Endometrial gene expression during early pregnancy differs between fertile and subfertile dairy cow strains. Physiol Genomics. 2012; 44: 47-58. doi: 10.1152/physiolgenomics.00254.2010 PMID: 22045914
41. Robert C. Microarray analysis of gene expression during early development: a cautionary overview. Reproduction. 2010; 140: 787-801. doi: 10.1530/REP-10-0191 PMID: 20833752
42. Walker CG, Littlejohn MD, Meier S, Roche JR, Mitchell MD. DNA methylation is correlated with gene expression during early pregnancy in Bos taurus. Physiological Genomics. 2013; 45: 276-286. doi: 10. 1152/physiolgenomics.00145.2012 PMID: 23386203
43. Cakmak H, Taylor HS. Implantation failure: molecular mechanisms and clinical treatment. Hum Reprod Update. 2011; 17: 242-253. doi: 10.1093/humupd/dmq037 PMID: 20729534
44. Ilesanmi AO, Hawkins DA, Lessey BA. Immunohistochemical markers of uterine receptivity in the human endometrium. Microsc Res Tech. 1993; 25: 208-222. PMID: 8400422