RNA sequencing reveals novel gene clusters in bovine conceptuses associated with maternal recognition of pregnancy and implantation

Biology of Reproduction

Volumn 85, Issue 6, 2011, Pages 1143-1151

  Mamo, Solomon ^a   Mehta, Jai P ^a   McGettigan, Paul ^a   Fair, Trudee ^a   Spencer, Thomas E ^b,c   Bazer, Fuller W ^b   Lonergan, Patrick ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

^b TEXAS A AND M UNIVERSITY   (United States)

^c WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Blastocyst; Bovine; Conceptus; Embryo; Implantation; Maternal recognition of pregnancy; RNA sequencing

Indexed keywords

TRANSCRIPTOME;

ANALYSIS OF VARIANCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; COW; EMBRYO; GENE CLUSTER; GENE EXPRESSION; IMPLANTATION; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; REGULATORY MECHANISM; RNA PROCESSING; RNA SEQUENCE;

ANIMALS; CATTLE; EMBRYO IMPLANTATION; EMBRYO, MAMMALIAN; FEMALE; GENE EXPRESSION PROFILING; MULTIGENE FAMILY; PREGNANCY; SEQUENCE ANALYSIS, RNA; TRANSCRIPTOME;

BOS; BOVINAE;

EID: 84855379268     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.111.092643     Document Type: Article

References (63)

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, Xie S, Mathialagan N. Maternal recognition of pregnancy. Biol Reprod 1996; 54:294-302.
3. 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.
4. Diskin MG, Morris DG. Embryonic and early foetal losses in cattle and other ruminants. Reprod Domest Anim 2008; 43(suppl 2):260-267.
5. Washburn SP, Silvia WJ, Brown CH, McDaniel BT, McAllister AJ. Trends in reproductive performance in Southeastern Holstein and Jersey DHI herds. J Dairy Sci 2002; 85:244-251.
6. Racowsky C. High rates of embryonic loss, yet high incidence of multiple births in human ART: is this paradoxical? Theriogenology 2002; 57:87- 96.
7. 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.
8. 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.
9. 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.
10. 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.
11. 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.
12. Chen Q, Zhang Y, Lu J, Wang Q, Wang S, Cao Y, Wang H, Duan E. Embryo-uterine cross-talk during implantation: the role of Wnt signaling. Mol Hum Reprod 2009; 15:215-221.
13. 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.
14. 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.
15. Ushizawa K, Herath CB, Kaneyama K, Shiojima S, Hirasawa A, Takahashi T, Imai K, Ochiai K, Tokunaga T, Tsunoda Y, Tsujimoto G, Hashizume K. cDNA microarray analysis of bovine embryo gene expression profiles during the pre-implantation period. Reprod Biol Endocrinol 2004; 2:77.
16. Clemente M, Lopez-Vidiero 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.
17. Wang Z, Gerstein M, Snyder M. RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 2009; 10:57-63.
18. Werner T. Next generation sequencing in functional genomics. Brief Bioinform 2010; 11:499-511.
19. Carter F, Rings F, Mamo S, Holker M, Kuzmany A, Besenfelder U, Havlicek V, Mehta JP, Tesfaye D, Schellander K, Lonergan P. Effect of elevated circulating progesterone concentration on bovine blastocyst development and global transcriptome following endoscopic transfer of in vitro produced embryos to the bovine oviduct. Biol Reprod 2010; 83:707- 719.
20. 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.
21. 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.
22. Eck SH, Benet-Pages A, Flisikowski K, Meitinger T, Fries R, Strom TM. Whole genome sequencing of a single Bos taurus animal for single nucleotide polymorphism discovery. Genome Biol 2009; 10:R82.
23. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 2008; 5:621-628.
24. Matsumura H, Yoshida K, Luo S, Kimura E, Fujibe T, Albertyn Z, Barrero RA, Kruger DH, Kahl G, Schroth GP, Terauchi R. High-throughput SuperSAGE for digital gene expression analysis of multiple samples using next generation sequencing. PLoS One; 5:e12010.
25. Mizuno H, Kawahara Y, Sakai H, Kanamori H, Wakimoto H, Yamagata H, Oono Y, Wu J, Ikawa H, Itoh T, Matsumoto T. Massive parallel sequencing of mRNA in identification of unannotated salinity stressinducible transcripts in rice (Oryza sativa L.). BMC Genomics 2010; 11:683.
26. Kurimoto K, Yabuta Y, Ohinata Y, Saitou M. Global single-cell cDNA amplification to provide a template for representative high-density oligonucleotide microarray analysis. Nat Protoc 2007; 2:739-752.
27. Sturn A, Quackenbush J, Trajanoski Z. Genesis: cluster analysis of microarray data. Bioinformatics 2002; 18:207-208.
28. Tamayo P, Slonim D, Mesirov J, Zhu Q, Kitareewan S, Dmitrovsky E, Lander ES, Golub TR. Interpreting patterns of gene expression with selforganizing maps: methods and application to hematopoietic differentiation. Proc Natl Acad Sci U S A 1999; 96:2907-2912.
29. Eisen MB, Spellman PT, Brown PO, Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 1998; 95:14863-14868.
30. Watson AJ, Westhusin ME, De Sousa PA, Betts DH, Barcroft LC. Gene expression regulating blastocyst formation. Theriogenology 1999; 51:117- 133.
31. Dilek FH, Topak N, Aktepe F, Sahin O, Turel KS, Sahin DA, Dilek ON. E-cadherin, beta-catenin adhesion complex and relation to matrilysin expression in pT3 rectosigmoid cancers. Pathol Res Pract 2008; 204:809- 815.
32. Blomberg L, Hashizume K, Viebahn C. Blastocyst elongation, trophoblastic differentiation, and embryonic pattern formation. Reproduction 2008; 135:181-195.
33. Zimin AV, Delcher AL, Florea L, Kelley DR, Schatz MC, Puiu D, Hanrahan F, Pertea G, Van Tassell CP, Sonstegard TS, Marcais G, Roberts M, et al. A whole-genome assembly of the domestic cow, Bos taurus. Genome Biol 2009; 10:R42.
34. Red-Horse K, Zhou Y, Genbacev O, Prakobphol A, Foulk R, McMaster M, Fisher SJ. Trophoblast differentiation during embryo implantation and formation of the maternal-fetal interface. J Clin Invest 2004; 114:744-754.
35. Gonzalez MA, Tachibana KE, Adams DJ, van der Weyden L, Hemberger M, Coleman N, Bradley A, Laskey RA. Geminin is essential to prevent endoreduplication and to form pluripotent cells during mammalian development. Genes Dev 2006; 20:1880-1884.
36. Bazer FW, Wu G, Spencer TE, Johnson GA, Burghardt RC, Bayless K. Novel pathways for implantation and establishment and maintenance of pregnancy in mammals. Mol Hum Reprod 2010; 16:135-152.
37. Vogelstein B, Lane D, Levine AJ. Surfing the p53 network. Nature 2000; 408:307-310.
38. Hu W, Feng Z, Teresky AK, Levine AJ. p53 regulates maternal reproduction through LIF. Nature 2007; 450:721-724.
39. Kang HJ, Feng Z, Sun Y, Atwal G, Murphy ME, Rebbeck TR, Rosenwaks Z, Levine AJ, Hu W. Single-nucleotide polymorphisms in the p53 pathway regulate fertility in humans. Proc Natl Acad Sci U S A 2009; 106:9761-9766.
40. Su HL, Li SS. Molecular features of human ubiquitin-like SUMO genes and their encoded proteins. Gene 2002; 296:65-73.
41. Roberts RM, Cross JC, Leaman DW. Interferons as hormones of pregnancy. Endocr Rev 1992; 13:432-452.
42. Spencer TE, Johnson GA, Bazer FW, Burghardt RC. Fetal-maternal interactions during the establishment of pregnancy in ruminants. Soc Reprod Fertil Suppl 2007; 64:379-396.
43. Roberts RM, Chen Y, Ezashi T, Walker AM. Interferons and the maternalconceptus dialog in mammals. Semin Cell Dev Biol 2008; 19:170-177.
44. Chen Y, Antoniou E, Liu Z, Hearne LB, Roberts RM. A microarray analysis for genes regulated by interferon-tau in ovine luminal epithelial cells. Reproduction 2007; 134:123-135.
45. Gray CA, Abbey CA, Beremand PD, Choi Y, Farmer JL, Adelson DL, Thomas TL, Bazer FW, Spencer TE. Identification of endometrial genes regulated by early pregnancy, progesterone, and interferon tau in the ovine uterus. Biol Reprod 2006; 74:383-394.
46. 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.
47. Arosh JA, Banu SK, Kimmins S, Chapdelaine P, Maclaren LA, Fortier MA. Effect of interferon-tau on prostaglandin biosynthesis, transport, and signaling at the time of maternal recognition of pregnancy in cattle: evidence of polycrine actions of prostaglandin E2. Endocrinology 2004; 145:5280-5293.
48. Emond V, MacLaren LA, Kimmins S, Arosh JA, Fortier MA, Lambert RD. Expression of cyclooxygenase-2 and granulocyte-macrophage colony-stimulating factor in the endometrial epithelium of the cow is up-regulated during early pregnancy and in response to intrauterine infusions of interferon-tau. Biol Reprod 2004; 70:54-64.
49. Ezashi T, Das P, Gupta R, Walker A, Roberts RM. The role of homeobox protein distal-less 3 and its interaction with ETS2 in regulating bovine interferon-tau gene expression-synergistic transcriptional activation with ETS2. Biol Reprod 2008; 79:115-124.
50. Zhao B, Cai J, Boulton M. Expression of placenta growth factor is regulated by both VEGF and hyperglycaemia via VEGFR-2. Microvasc Res 2004; 68:239-246.
51. Mesnard D, Constam DB. Imaging proprotein convertase activities and their regulation in the implanting mouse blastocyst. J Cell Biol 2010; 191:129-139.
52. Hynes RO. Integrins: versatility, modulation, and signaling in cell adhesion. Cell 1992; 69:11-25.
53. Bazer FW, Spencer TE, Johnson GA, Burghardt RC, Wu G. Comparative aspects of implantation. Reproduction 2009; 138:195-209.
54. Wang J, Armant DR. Integrin-mediated adhesion and signaling during blastocyst implantation. Cells Tissues Organs 2002; 172:190-201.
55. MacIntyre DM, Lim HC, Ryan K, Kimmins S, Small JA, MacLaren LA. Implantation-associated changes in bovine uterine expression of integrins and extracellular matrix. Biol Reprod 2002; 66:1430-1436.
56. Fisher S, Gearhart JD, Oster-Granite ML. Expression of the amyloid precursor protein gene in mouse oocytes and embryos. Proc Natl Acad Sci U S A 1991; 88:1779-1782.
57. Porayette P, Gallego MJ, Kaltcheva MM, Meethal SV, Atwood CS. Amyloid-beta precursor protein expression and modulation in human embryonic stem cells: a novel role for human chorionic gonadotropin. Biochem Biophys Res Commun 2007; 364:522-527.
58. 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.
59. Sasser RG, Ruder CA, Ivani KA, Butler JE, Hamilton WC. Detection of pregnancy by radioimmunoassay of a novel pregnancy-specific protein in serum of cows and a profile of serum concentrations during gestation. Biol Reprod 1986; 35:936-942.
60. 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.
61. Gad A, Besenfelder U, Rings F, Ghanem N, Salilew-Wondim D, Hossain MM, Tesfaye D, Lonergan P, Becker A, Cinar U, Schellander K, Havlicek V, et al. Effect of reproductive tract environment following controlled ovarian hyperstimulation treatment on embryo development and global transcriptome profile of blastocysts: implications for animal breeding and human assisted reproduction. Hum Reprod 2011; 26:1693-1707.
62. Stroud B. IETS Statistics and Data Retrieval Committee Report. The year 2009 worldwide statistics of embryo transfer in domestic farm animals. Embryo Transfer Newsletter 2010; 28:11-21.
63. Harhay GP, Smith TP, Alexander LJ, Haudenschild CD, Keele JW, Matukumalli LK, Schroeder SG, Van Tassell CP, Gresham CR, Bridges SM, Burgess SC, Sonstegard TS. An atlas of bovine gene expression reveals novel distinctive tissue characteristics and evidence for improving genome annotation. Genome Biol 2010; 11:R102.