Bioinformatics analysis of gene sets enrichment between bovine embryonic cleavage ‎and development blastocysts using DNA microarray data

Document Type : Research Paper

Authors

1 Ph.D. Candidate, Department of Animal Sciences, Islamic Azad University, Science and Research Branch, Tehran, Iran

2 Assistant Professor, Department of Animal Sciences, Islamic Azad University, Science and Research Branch, Tehran, Iran

3 Associate Professor, Department of Animal Sciences, Faculty of Agriculture, Yasouj University, Yasouj, Iran

4 Professor, Department of Animal Sciences, Islamic Azad University, Science and Research Branch, Tehran, Iran

5 Assistant Professor, Department of Animal Sciences, Islamic Azad University, Qods City Branch, Tehran, Iran

Abstract

In order to understand the causes of bovine embryo mortality and viability, it is necessary to identify different pathways between the embryonic fission and the blastocyst. The enriched sets of genes from a bovine embryonic cell to a 16-cell and blastocyst stage were examined. The raw DNA microarray data was downloaded from the GEO database. Then differentially expressed probes were enriched with the online software agriGO v2 by means of singular enrichment analysis (SEA). The results of this study showed that a total of 5 genes with increased expression, including KPNA7, RGS2, TESC, MLLT11, BMP15 and 5 genes with decreased expression, including KRT8, CLDN6, PLAC8, FN1, KRT18 had the highest differentially expressed pattern (P ≤0.05). In addition, 39 gene sets in various molecular metabolic pathways, including NADP metabolism, tRNA, ATP, phospholipid catabolism, apoptosis and cell growth, glycolysis, mitosis; 13 gene sets on the path of molecular functions, including manganese ion, RRNA, cytochrome C oxidation activities, translation primers, ATP and ATPase activity and at the level of the cellular components of 12 gene sets on the path of the cytoplasmic cavesicle membrane, endoplasmic reticulum membrane, microtubules and Spindles and plasma membrane showed the highest enrichment (P ≤0.05). As a result, the gene sets enriched with blastocysts indicate the beginning of cell differentiation and the transition from the blastocyst state to the implantation process. Ultimately, at this stage, gene sets are expressed, the interaction of which is likely to result in the survival or analysis of the embryo.

Keywords


  1. Aaltonen, J., Laitinen, M. P., Vuojolainen, K., Jaatinen, R., Horelli-Kuitunen, N., Seppä, L., Louhio, H., Tuuri, T., Sjöberg, J., Bützow, R., Hovata, O., Dale, L., & Ritvos, O. (1999). Human growth differentiation factor 9 (GDF-9) and its novel homolog GDF-9B are expressed in oocytes during early folliculogenesis. The Journal of Clinical Endocrinology and Metabolism, 84(8), 2744-2750.
  2. Abramow-Newerly, M., Roy, A. A., Nunn, C., & Chidiac, P. (2006). RGS proteins have a signalling complex: interactions between RGS proteins and GPCRs, effectors, and auxiliary proteins. Cellular Signalling, 18(5), 579-591.
  3. Adjaye, J., Herwig, R., Brink, T. C., Herrmann, D., Greber, B., Sudheer, S., Groth, D., Carnwath, J. W., Lehrach, H., & Niemann, H. (2007). Conserved molecular portraits of bovine and human blastocysts as a consequence of the transition from maternal to embryonic control of gene expression. Physiological Genomics, 31(2), 315-327.
  4. Bauersachs, S., Ulbrich, S. E., Zakhartchenko, V., Minten, M., Reichenbach, M., Reichenbach, H. D., Blum, H., Spencer, T. E., & Wolf, E. (2009). The endometrium responds differently to cloned versus fertilized embryos. Proceedings of the National Academy of Sciences of the United States of America, 106(14), 5681-5686.
  5. Bazer, F. W., Roberts, R. M., & Thatcher, W. W. (1979). Actions of hormones on the uterus and effect on conceptus development. Journal of Animal Science, 49 Suppl 2, 35-45.
  6. Beiki H., Nejati A. J., Pakdel A., Masoudi A. N., Hu Z. and Reecy J. M. 2016, Large-scale gene co-expression network as a source of functional annotation for cattle genes. BMC Genomics, 201617:846.
  7. Bermejo-Alvarez, P., Rizos, D., Rath, D., Lonergan, P., & Gutierrez-Adan, A. (2010). Sex determines the expression level of one third of the actively expressed genes in bovine blastocysts. Proceedings of the National Academy of Sciences of the United States of America, 107(8), 3394-3399.
  8. Boni, R., Tosti, E., Roviello, S., & Dale, B. (1999). Intercellular communication in in vivo- and in vitro-produced bovine embryos. Biology of Reproduction, 61(4), 1050-1055.
  9. Brunet-Simon, A., Henrion, G., Renard, J. P., & Duranthon, V. (2001). Onset of zygotic transcription and maternal transcript legacy in the rabbit embryo. Molecular Reproduction and Development, 58(2), 127-136.
  10. Burt D. W. (1992). Evolutionary grouping of the transforming growth factor-beta superfamily. Biochemical and Biophysical Research Communications, 184(2), 590-595.
  11. Chou, C. C., Sun, Y. J., Meng, M., & Hsiao, C. D. (2000). The crystal structure of phosphoglucose isomerase/autocrine motility factor/neuroleukin complexed with its carbohydrate phosphate inhibitors suggests its substrate/receptor recognition. The Journal of Biological Chemistry, 275(30), 23154-23160.
  12. Clemente, M., Lopez-Vidriero, I., O'Gaora, P., Mehta, J. P., Forde, N., Gutierrez-Adan, A., Lonergan, P., & Rizos, D. (2011). Transcriptome changes at the initiation of elongation in the bovine conceptus. Biology of Reproduction, 85(2), 285-295.
  13. Co, N. N., Tsang, W. P., Tsang, T. Y., Yeung, C. L., Yau, P. L., Kong, S. K., & Kwok, T. T. (2010). AF1q enhancement of gamma irradiation-induced apoptosis by up-regulation of BAD expression via NF-kappaB in human squamous carcinoma A431 cells. Oncology Reports, 24(2), 547-554.
  14. Diskin, M. G., & Morris, D. G. (2008). Embryonic and early foetal losses in cattle and other ruminants. Reproduction in Domestic Animals = Zuchthygiene, 43 Suppl 2, 260-267.
  15. Dorji, Ohkubo, Y., Miyoshi, K., & Yoshida, M. (2012). Gene expression profile differences in embryos derived from prepubertal and adult Japanese Black cattle during in vitro development. Reproduction, Fertility, and Development, 24(2), 370-381.
  16. Dube, J. L., Wang, P., Elvin, J., Lyons, K. M., Celeste, A. J., & Matzuk, M. M. (1998). The bone morphogenetic protein 15 gene is X-linked and expressed in oocytes. Molecular Endocrinology (Baltimore, Md.), 12(12), 1809-1817.
  17. Duranthon, V., & Renard, J. P. (2001). The developmental competence of mammalian oocytes: a convenient but biologically fuzzy concept. Theriogenology, 55(6), 1277-1289.
  18. Fleming, T. P., Butler, L., Lei, X., Collins, J., Javed, Q., Sheth, B., Stoddart, N., Wild, A., & Hay, M. (1994). Molecular maturation of cell adhesion systems during mouse early development. Histochemistry, 101(1), 1-7.
  19. Frank, D., Fortino, W., Clark, L., Musalo, R., Wang, W., Saxena, A., Li, C. M., Reik, W., Ludwig, T., & Tycko, B. (2002). Placental overgrowth in mice lacking the imprinted gene Ipl. Proceedings of the National Academy of Sciences of the United States of America, 99(11), 7490-7495.
  20. Furuse, M., Sasaki, H., & Tsukita, S. (1999). Manner of interaction of heterogeneous claudin species within and between tight junction strands. The Journal of Cell Biology, 147(4), 891-903.
  21. Gad, A., Besenfelder, U., Rings, F., Ghanem, N., Salilew-Wondim, D., Hossain, M. M., Tesfaye, D., Lonergan, P., Becker, A., Cinar, U., Schellander, K., Havlicek, V., & Hölker, M. (2011). 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. Human Reproduction (Oxford, England), 26(7), 1693-1707.
  22. Gossler, A. (1992). Early Embryonic Development of Animals. (pp.151-201) Springer, Berlin.
  23. Guo, M., Rupe, M. A., Dieter, J. A., Zou, J., Spielbauer, D., Duncan, K. E., Howard, R. J., Hou, Z., & Simmons, C. R. (2010). Cell Number Regulator1 affects plant and organ size in maize: implications for crop yield enhancement and heterosis. The Plant Cell, 22(4), 1057–1073.
  24. Heyman, Y., Chavatte-Palmer, P., LeBourhis, D., Camous, S., Vignon, X., & Renard, J. P. (2002). Frequency and occurrence of late-gestation losses from cattle cloned embryos. Biology of Reproduction, 66(1), 6-13.
  25. Huang, d., Sherman, B. T., & Lempicki, R. A. (2009). Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Research, 37(1), 1-13.
  26. Huang, W., Yandell, B. S., & Khatib, H. (2010). Transcriptomic profiling of bovine IVF embryos revealed candidate genes and pathways involved in early embryonic development. BMC Genomics, 11, 23.
  27. Inai, T., Kamimura, T., Hirose, E., Iida, H., & Shibata, Y. (2010). The protoplasmic or exoplasmic face association of tight junction particles cannot predict paracellular permeability or heterotypic claudin compatibility. European Journal of Cell Biology, 89(7), 547-556.
  28. Jeffery, C. J., Bahnson, B. J., Chien, W., Ringe, D., & Petsko, G. A. (2000). Crystal structure of rabbit phosphoglucose isomerase, a glycolytic enzyme that moonlights as neuroleukin, autocrine motility factor, and differentiation mediator. Biochemistry, 39(5), 955-964.
  29. Jimenez-Preitner, M., Berney, X., & Thorens, B. (2012). Plac8 is required for white adipocyte differentiation in vitro and cell number control in vivo. PloS one, 7(11), e48767.
  30. Johnson, M. H., & Ziomek, C. A. (1981). The foundation of two distinct cell lineages within the mouse morula. Cell, 24(1), 71-80.
  31. Jones, R. L., Stoikos, C., Findlay, J. K., & Salamonsen, L. A. (2006). TGF-beta superfamily expression and actions in the endometrium and placenta. Reproduction (Cambridge, England), 132(2), 217-232.
  32. Kues, W. A., Sudheer, S., Herrmann, D., Carnwath, J. W., Havlicek, V., Besenfelder, U., Lehrach, H., Adjaye, J., & Niemann, H. (2008). Genome-wide expression profiling reveals distinct clusters of transcriptional regulation during bovine preimplantation development in vivo. Proceedings of the National Academy of Sciences of the United States of America, 105(50), 19768-19773.
  33. Levay, K., & Slepak, V. Z. (2010). Up- or downregulation of tescalcin in HL-60 cells is associated with their differentiation to either granulocytic or macrophage-like lineage. Experimental Cell Research, 316(7), 1254-1262.
  34. MacLean, J. A., 2nd, Chakrabarty, A., Xie, S., Bixby, J. A., Roberts, R. M., & Green, J. A. (2003). Family of Kunitz proteins from trophoblast: expression of the trophoblast Kunitz domain proteins (TKDP) in cattle and sheep. Molecular Reproduction and Development, 65(1), 30-40.
  35. Mansouri-Attia, N., Sandra, O., Aubert, J., Degrelle, S., Everts, R. E., Giraud-Delville, C., Heyman, Y., Galio, L., Hue, I., Yang, X., Tian, X. C., Lewin, H. A., & Renard, J. P. (2009). Endometrium as an early sensor of in vitro embryo manipulation technologies. Proceedings of the National Academy of Sciences of the United States of America, 106(14), 5687-5692.
  36. Michibata, H., Chiba, H., Wakimoto, K., Seishima, M., Kawasaki, S., Okubo, K., Mitsui, H., Torii, H., & Imai, Y. (2004). Identification and characterization of a novel component of the cornified envelope, cornifelin. Biochemical and Biophysical Research Communications, 318(4), 803-813.
  37. Mitko, K., Ulbrich, S. E., Wenigerkind, H., Sinowatz, F., Blum, H., Wolf, E., & Bauersachs, S. (2008). Dynamic changes in messenger RNA profiles of bovine endometrium during the oestrous cycle. Reproduction (Cambridge, England), 135(2), 225-240.
  38. Moroianu, J., Blobel, G., & Radu, A. (1996). The binding site of karyopherin alpha for karyopherin beta overlaps with a nuclear localization sequence. Proceedings of the National Academy of Sciences of the United States of America, 93(13), 6572-6576.
  39. Niemann, H., & Elsaesser, F. (1986). Evidence for estrogen-dependent blastocyst formation in the pig. Biology of Reproduction, 35(1), 10-16.
  40. Ogawa, Y., Sun, B. K., & Lee, J. T. (2008). Intersection of the RNA interference and X-inactivation pathways. Science (New York, N.Y.), 320(5881), 1336-1341.
  41. Pankov, R., & Yamada, K. M. (2002). Fibronectin at a glance. Journal of Cell Science, 115(Pt 20), 3861-3863.
  42. Paria, B. C., Sengupta, J., & Manchanda, S. K. (1984). Role of embryonic oestrogen in rabbit blastocyst development and metabolism. Journal of Reproduction and Fertility, 70(2), 429-436.
  43. Park, J., Schlederer, M., Schreiber, M., Ice, R., Merkel, O., Bilban, M., Hofbauer, S., Kim, S., Addison, J., Zou, J., Ji, C., Bunting, S. T., Wang, Z., Shoham, M., Huang, G., Bago-Horvath, Z., Gibson, L. F., Rojanasakul, Y., Remick, S., Ivanov, A., … Tse, W. (2015). AF1q is a novel TCF7 co-factor which activates CD44 and promotes breast cancer metastasis. Oncotarget, 6(24), 20697–20710.
  44. Roberts, R. M., Chen, Y., Ezashi, T., & Walker, A. M. (2008). Interferons and the maternal-conceptus dialog in mammals. Seminars In Cell & Developmental Biology, 19(2), 170-177.
  45. Salas, M., John, R., Saxena, A., Barton, S., Frank, D., Fitzpatrick, G., Higgins, M. J., & Tycko, B. (2004). Placental growth retardation due to loss of imprinting of Phlda2. Mechanisms of Development, 121(10), 1199-1210.
  46. Steinert, P. M., & Roop, D. R. (1988). Molecular and cellular biology of intermediate filaments. Annual Review of Biochemistry, 57, 593-625.
  47. Stewart M. (1990). Intermediate filaments: structure, assembly and molecular interactions. Current Opinion in Cell Biology, 2(1), 91-100.
  48. Sun, Y. J., Chou, C. C., Chen, W. S., Wu, R. T., Meng, M., & Hsiao, C. D. (1999). The crystal structure of a multifunctional protein: phosphoglucose isomerase/autocrine motility factor/neuroleukin. Proceedings of the National Academy of Sciences of the United States of America, 96(10), 5412-5417.
  49. Ukarapong, S., Bao, Y., Perera, E. M., & Berkovitz, G. D. (2012). Megakaryocyte development is normal in mice with targeted disruption of Tescalcin. Experimental Cell Research, 318(5), 662–669.
  50. Van Itallie, C. M., & Anderson, J. M. (2013). Claudin interactions in and out of the tight junction. Tissue Barriers, 1(3), e25247.
  51. Wang, L., Srinivasan, S., Theiss, A. L., Merlin, D., & Sitaraman, S. V. (2007). Interleukin-6 induces keratin expression in intestinal epithelial cells: potential role of keratin-8 in interleukin-6-induced barrier function alterations. The Journal of Biological Chemistry, 282(11), 8219-8227.
  52. Weber, R. J., Pedersen, R. A., Wianny, F., Evans, M. J., & Zernicka-Goetz, M. (1999). Polarity of the mouse embryo is anticipated before implantation. Development (Cambridge, England), 126(24), 5591-5598.
  53. Wei, C. J., Xu, X., & Lo, C. W. (2004). Connexins and cell signaling in development and disease. Annual Review of Cell and Developmental Biology, 20, 811-838.
  54. Xie, D., Chen, C. C., Ptaszek, L. M., Xiao, S., Cao, X., Fang, F., Ng, H. H., Lewin, H. A., Cowan, C., & Zhong, S. (2010). Rewirable gene regulatory networks in the preimplantation embryonic development of three mammalian species. Genome Research, 20(6), 804-815.
  55. Yamazaki, Y., Tokumasu, R., Kimura, H., & Tsukita, S. (2011). Role of claudin species-specific dynamics in reconstitution and remodeling of the zonula occludens. Molecular Biology of the Cell, 22(9), 1495-1504.
  56. Ye, B., Li, L., Xu, H., Chen, Y., & Li, F. (2019). Opposing roles of TCF7/LEF1 and TCF7L2 in cyclin D2 and Bmp4 expression and cardiomyocyte cell cycle control during late heart development. Laboratory Investigation; A Journal of Technical Methods and Pathology, 99(6), 807-818.