Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Differential expression of microRNAs in porcine placentas on Days 30 and 90 of gestation

Lijie Su A , Shuhong Zhao A , Mengjin Zhu A and Mei Yu A B
+ Author Affiliations
- Author Affiliations

A Key Lab of Agricultural Animal Genetics, Breeding and Reproduction of Ministry of Education, Huazhong (Central China) Agricultural University, Wuhan, 430070, Hubei, PR China.

B Corresponding author. Email: yumei@mail.hzau.edu.cn

Reproduction, Fertility and Development 22(8) 1175-1182 https://doi.org/10.1071/RD10046
Submitted: 9 March 2010  Accepted: 7 April 2010   Published: 1 October 2010

Abstract

The porcine placenta is classified as a non-invasive epitheliochorial type. To meet the increasing demands for nutrients by the rapidly growing conceptus and/or fetus, the placental microscopic folds undergo significant morphological and biochemical changes during two periods critical for conceptus and/or fetus, namely Days 30–40 and after Day 90 of gestation. MicroRNAs (miRNAs) are a class of small non-coding RNAs that can modulate gene activity by inhibiting the translation or regulation of mRNA degradation. In the present study, we identified 17 differentially expressed miRNAs in porcine placenta on Days 30 and 90 of gestation using a locked nucleic acid (LNA) microRNA array. Stem–loop real-time reverse transcription–polymerase chain reaction confirmed the differential expression of eight selected miRNAs (miR-24, miR-125b, miR-92b, miR-106a, miR-17, let-7i, miR-27a and miR-20). Analysis of targets and the pathways in which these miRNAs are involved revealed that the differentially expressed miRNAs target many genes that are important in various processes, including cell growth, trophoblast differentiation, angiogenesis and formation and maintenance of adherens junctions. The results of the present study suggest potential roles for these differentially expressed miRNAs in porcine placental growth and function.

Additional keywords: epitheliochorial placenta, microarray, miRNAs, pig, target gene.


Acknowledgements

This research was supported by the National High Science and Technology Foundation of China ‘863’ (2007AA10Z148), National Natural Science Foundation of China (30771537), the Program for New Century Excellent Talents in University (NCET-08–0784) and Excellent Youth Foundation of Hubei Scientific Committee (2008CDB106). The authors thank Dr Quanyong Zhou, Yi Li and Xue Bai for sample collection and preparation.


References

Bartel, D. P. (2004). MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 116, 281–297.
CrossRef | PubMed |

Biensen, N. J. , Wilson, M. E. , and Ford, S. P. (1998). The impact of either a Meishan or Yorkshire uterus on Meishan or Yorkshire fetal and placental development to Days 70, 90 and 110 of gestation. J. Anim. Sci. 76, 2169–2176.
PubMed |

Bolstad, B. M. , Irizarry, R. A. , Astrand, M. , and Speed, T. P. (2003). A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19, 185–193.
CrossRef | PubMed |

Boyle, K. , and Robb, L. (2008). The role of SOCS3 in modulating leukaemia inhibitory factor signalling during murine placental development. J. Reprod. Immunol. 77, 1–6.
CrossRef | PubMed |

Burghardt, R. C. , Burghardt, J. R. , Spencer, T. E. , Bayless, K. J. , and Johnson, G. A. (2009). Enhanced focal adhesion assembly reflects increased mechanosensation and mechanotransduction at maternal–conceptus interface and uterine wall during ovine pregnancy. Reproduction 137, 567–582.
CrossRef | PubMed |

Chen, C. F. , Ridzon, D. A. , Broomer, A. J. , Lao, K. Q. , Livak, K. J. , and Guegler, K. J. (2005). Real-time quantification of microRNAs by stem–loop RT-PCR. Nucleic Acids Res. 33, e179.
CrossRef | PubMed |

de Hoon, M. J. L. , Imoto, S. , Nolan, J. , and Miyano, S. (2004). Open source clustering software. Bioinformatics 20, 1453–1454.
CrossRef | PubMed |

Distl, O. (2007). Mechanisms of regulation of litter size in pigs on the genome level. Reprod. Domest. Anim. 42, 10–16.
CrossRef | PubMed |

Ford, S. P. , Vonnahme, K. A. , and Wilson, M. E. (2002). Uterine capacity in the pig reflects a combination of uterine environment and conceptus genotype effects. J. Anim. Sci. 80, E66–E73.


Geisert, R. D. , and Schmitt, R. A. M. (2002). Early embryonic survival in the pig: can it be improved? J. Anim. Sci. 80, E54–E65.


Hu, W. , Feng, Z. , Teresky, A. K. , and Levine, A. J. (2007). p53 regulates maternal reproduction through LIF. Nature 450, 721–724.
CrossRef | PubMed |

Hu, Y. , Li, P. , Hao, S. , Liu, L. , Zhao, J. , and Hou, Y. (2009). Differential expression of microRNAs in the placentae of Chinese patients with severe pre-eclampsia. Clin. Chem. Lab. Med. 47, 923–929.
CrossRef | PubMed |

Hui, A. B. , Lenarduzzi, M. , Krushel, T. , Waldron, L. , Pintilie, M. , Gullane, P. , Cummings, B. , and Liu, F. F. (2010). Comprehensive microRNA profiling for head and neck squamous cell carcinomas. Clin. Cancer Res. 16, 1129–1139.
CrossRef | PubMed |

Ishikawa, T. , Tamai, Y. , Zorn, A. M. , Yoshida, H. , Seldin, M. F. , Nishikawa, S. , and Taketo, M. M. (2001). Mouse Wnt receptor gene Fzd5 is essential for yolksac and placental angiogenesis. Development 128, 25–33.
PubMed |

Jeays-Ward, K. , Hoyle, C. , Brennan, J. , Dandonneau, M. , Alldus, G. , Capel, B. , and Swain, A. (2003). Endothelial and steroidogenic cell migration are regulated by WNT4 in the developing mammalian gonad. Development 130, 3663–3670.
CrossRef | PubMed |

Kaufmann P., and Burton G. (1999). Anatomy and genesis of the placenta. In ‘The Physiology of Reproduction’. (Eds J. D. Knobil and N. Y. Neill.) pp. 441–484. (Raven Press: New York.)

Kim, J. , Cho, I. S. , Hong, J. S. , Choi, Y. K. , Kim, H. , and Lee, Y. S. (2008). Identification and characterization of new microRNAs from pig. Mamm. Genome 19, 570–580.
CrossRef | PubMed |

Knight, J. W. , Bazer, F. W. , Thatcher, W. W. , Franke, D. E. , and Wallace, H. D. (1977). Conceptus development in intact and unilaterally hysterectomized–ovariectomized gilts: interrelations among hormonal status, placental development, fetal fluids, and fetal growth. J. Anim. Sci. 44, 620–637.
PubMed |

Lal, A. , Navarro, F. , Maher, C. A. , Maliszewski, L. E. , Gorospe, M. , Hide, W. , and Lieberman, J. (2009). MiR-24 inhibits cell proliferation by targeting E2F2, MYC, and other cell-cycle genes via binding to ‘seedless’ 3′UTR microRNA recognition elements. Mol. Cell 35, 610–625.
CrossRef | PubMed |

Le, M. T. , Teh, C. , Shyh-Chang, N. , Xie, H. , Zhou, B. , and Lim, B. (2009). MicroRNA-125b is a novel negative regulator of p53. Genes Dev. 23, 862–876.
CrossRef | PubMed |

Leach, L. , Lammiman, M. J. , Babawale, M. O. , Hobson, S. A. , Bromilou, B. , Lovat, S. , and Simmonds, M. J. (2000). Molecular organization of tight and adherens junctions in the human placental vascular tree. Placenta 21, 547–557.
CrossRef | PubMed |

Lee, E. J. , Gusev, Y. , Jiang, J. , Nuovo, G. J. , Lerner, M. R. , Frankel, W. L. , Morgan, D. L. , Postier, R. G. , Brackett, D. J. , and Schmittgen, T. D. (2007). Expression profiling identifies microRNA signature in pancreatic cancer. Int. J. Cancer 120, 1046–1054.
CrossRef | PubMed |

Leiser, R. , and Kaufmann, P. (1994). Placental structure: in a comparative aspect. Exp. Clin. Endocrinol. 102, 122–134.
CrossRef | PubMed |

Leiser, R. , Pfarrer, C. , Abd-Elnaeim, M. , and Dantzer, V. (1998). Feto–maternal anchorage in epitheliochorial and endotheliochorial placental types studied by histology and microvascular corrosion casts. Placenta 19, 21–39.
CrossRef | PubMed |

Liu, T. , Tang, H. , Lang, Y. , Liu, M. , and Li, X. (2009). MicroRNA-27a functions as an oncogene in gastric adenocarcinoma by targeting prohibitin. Cancer Lett. 273, 233–242.
CrossRef | PubMed |

Livak, K. J. , and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2–Ct method. Methods 25, 402–408.
CrossRef | PubMed |

Luo, S. S. , Ishibashi, O. , Ishikawa, G. , Matsubara, S. , and Takizawa, T. (2009). Human villous trophoblasts express and secrete placenta-specific microRNAs into maternal circulation via exosomes. Biol. Reprod. 81, 717–729.
CrossRef | PubMed |

MacPhee, D. J. , Mostachfi, H. , Han, R. , Lye, S. J. , Post, M. , and Caniggia, I. (2001). Focal adhesion kinase is a key mediator of human trophoblast development. Lab. Invest. 81, 1469–1483.
PubMed |

Mishra, P. J. , Song, B. , Wang, Y. , Humeniuk, R. , Banerjee, D. , Merlino, G. , Ju, J. , and Bertino, J. R. (2009). MiR-24 tumor suppressor activity is regulated independent of p53 and through a target site polymorphism. PLoS One 4, e8445.
CrossRef | PubMed |

Moussad, E. E. , Rageh, M. A. , Wilson, A. K. , Geisert, R. D. , and Brigstock, D. R. (2002). Temporal and spatial expression of connective tissue growth factor (CCN2; CTGF) and transforming growth factor beta type 1 (TGF-beta1) at the utero–placental interface during early pregnancy in the pig. Mol. Pathol. 55, 186–192.
CrossRef | PubMed |

Muñoz, G. , Ovilo, C. , Estellé, J. , Silió, L. , Fernández, A. , and Rodriguez, C. (2007). Association with litter size of new polymorphisms on ESR1 and ESR2 genes in a Chinese–European pig line. Genet. Sel. Evol. 39, 195–206.
CrossRef | PubMed |

Pineles, B. L. , Romero, R. , Montenegro, D. , Tarca, A. L. , Han, Y. M. , Kim, Y. M. , Draghici, S. , Espinoza, J. , Kusanovic, J. P. , Mittal, P. , Hassan, S. S. , and Kim, C. J. (2007). Distinct subsets of microRNAs are expressed differentially in the human placentas of patients with preeclampsia. Am. J. Obstet. Gynecol. 196, 261.e1–261.e6.
CrossRef |

Pope W. F. (1994). Embryonic mortality in swine. In ‘Embryonic Mortality in Domestic Species’. (Eds M. T. Zavy and R. D. Geisert.) pp. 53–78. (CRC Press: Boca Raton.)

Pope, W. F. , and First, N. L. (1985). Factors affecting the survival of pig embryos. Theriogenology 23, 91–105.
CrossRef |

Reynolds, L. P. , and Redmer, D. A. (1995). Utero–placental vascular development and placental function. J. Anim. Sci. 73, 1839–1851.
PubMed |

Rothschild M. F. (1998). Identification of quantitative trait loci and interesting candidate genes in the pig: progress and prospects. In ‘Proceedings of the 6th World Congress on Genetics Applied to Livestock Production’. pp. 403–409. (Armidale, NSW.)

Roy, H. , Bhardwaj, S. , and Ylä-Herttuala, S. (2006). Biology of vascular endothelial growth factors. FEBS Lett. 580, 2879–2887.
CrossRef | PubMed |

Sengupta, S. , Nie, J. , Wagner, R. J. , Yang, C. , Stewart, R. , and Thomson, J. A. (2009). MicroRNA 92b controls the G1/S checkpoint gene p57 in human embryonic stem cells. Stem Cells 27, 1524–1528.
CrossRef | PubMed |

Takahashi, Y. , Takahashi, M. , Carpino, N. , Jou, S. T. , Chao, J. R. , Tanaka, S. , Shigeyoshi, Y. , Parganas, E. , and Ihle, J. N. (2008). Leukemia inhibitory factor regulates trophoblast giant cell differentiation via janus kinase 1-signal transducer and activator of transcription 3-suppressor of cytokine signaling 3 pathway. Mol. Endocrinol. 22, 1673–1681.
CrossRef | PubMed |

Tan, P. K. , Downey, T. J. , Spitznagel, E. L., Jr , Xu, P. , Fu, D. , Dimitrov, D. S. , Lempicki, R. A. , Raaka, B. M. , and Cam, M. C. (2003). Evaluation of gene expression measurements from commercial microarray platforms. Nucleic Acids Res. 31, 5676–5684.
CrossRef | PubMed |

Vallet, J. L. , and Freking, B. A. (2007). Differences in placental structure during gestation associated with large and small pig fetuses. J. Anim. Sci. 85, 3267–3275.
CrossRef | PubMed |

Vonnahme, K. A. , Wilson, M. E. , and Ford, S. P. (2001). Relationship between placental vascular endothelial growth factor expression and placental/endometrial vascularity in the pig. Biol. Reprod. 64, 1821–1825.
CrossRef | PubMed |

Wernersson, R. , Schierup, M. H. , Jorgensen, F. G. , Yang, H. , and Bolund, L. (2005). Pigs in sequence space: a 0.66X coverage pig genome survey based on shotgun sequencing. BMC Genomics 6, 70.
CrossRef | PubMed |

Wigmore, P. M. C. , and Strickland, N. C. (1985). Placental growth in the pig. Anat. Embryol. (Berl.) 173, 263–268.
CrossRef | PubMed |

Ye, W. , Lv, Q. , Wong, C. K. , Li, G. , Yang, B. B. , and Zhang, Y. (2008). The effect of central loops in miRNA : MRE duplexes on the efficiency of miRNA-mediated gene regulation. PLoS One 3, e1719.
CrossRef | PubMed |

Zerlin, M. , Julius, M. A. , and Kitajewski, J. (2008). Wnt/Frizzled signaling in angiogenesis. Angiogenesis 11, 63–69.
CrossRef | PubMed |

Zhang, X. , Gaspard, J. P. , and Chung, D. C. (2001). Regulation of vascularendothelial growth factor by the Wnt and K-ras pathways in colonic neoplasia. Cancer Res. 61, 6050–6054.
PubMed |

Zhou, Q. Y. , Fang, M. D. , Huang, T. H. , Li, C. C. , Yu, M. , and Zhao, S. H. (2009). Detection of differentially expressed genes between Erhualian and Large White placentas on Day 75 and 90 of gestation. BMC Genomics 10, 337.
CrossRef | PubMed |

Zhu, X. M. , Han, T. , Sargent, I. L. , Yin, G. W. , and Yao, Y. Q. (2009). Differential expression profile of microRNAs in human placentas from preeclamptic pregnancies vs normal pregnancies. Am. J. Obstet. Gynecol. 200, 661.e1–661.e7.
CrossRef |



Rent Article (via Deepdyve) Export Citation Cited By (21)