Characterization and comparative profiling of ovarian microRNAs during ovine anestrus and the breeding season

BMC Genomics, Oct 2014

Background Seasonal estrus is a critical limiting factor of animal fecundity, and it involves changes in both ovarian biology and hormone secretion in different seasons. Previous studies indicate that two classes of small RNAs (miRNAs and piRNAs) play important regulatory roles in ovarian biology. To understand the roles of small RNA-mediated post-transcriptional regulation in ovine seasonal estrus, the variation in expression patterns of ovarian small RNAs during anestrus and the breeding season were analyzed using Solexa sequencing technology. In addition, reproductive hormone levels were determined during ovine anestrus and the breeding season. Results A total of 483 miRNAs (including 97 known, 369 conserved and 17 predicated novel miRNAs), which belong to 183 different miRNA families, were identified in ovaries of Tan sheep and Small Tail Han (STH) sheep. Compared with the three stages of the breeding season, 25 shared significantly differentially expressed (including 19 up- and six down-regulated) miRNAs were identified in ovine anestrus. KEGG Pathway analysis revealed that the target genes for some of the differentially expressed miRNAs were involved in reproductive hormone related pathways (e.g. steroid biosynthesis, androgen and estrogen metabolism and GnRH signaling pathway) as well as follicular/luteal development related pathways. Moreover, the expression of the differentially expressed miRNAs and most of their target genes were negatively correlated in the above pathways. Furthermore, the levels of estrogen, progesterone and LH in ovine anestrus were significantly lower than those in the breeding season. Combining the results of pathway enrichment analysis, expression of target genes and hormone measurement, we suggest that these differentially expressed miRNAs in anestrus might participate in attenuation of ovarian activity by regulating the above pathways. Besides miRNAs, a large and unexpectedly diverse set of piRNAs were also identified. Conclusions The miRNA profiles of ovine ovaries in anestrus were presented for the first time. The identification and characterization of miRNAs that are differentially expressed between ovine anestrus and the breeding season will help understanding of the role of miRNAs in the regulation of seasonal estrus, and provides candidates for determining miRNAs which could be potentially used to regulate ovine seasonal estrus.

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Characterization and comparative profiling of ovarian microRNAs during ovine anestrus and the breeding season

BMC Genomics Characterization and comparative profiling of ovarian microRNAs during ovine anestrus and the breeding season Ran Di 0 Jianning He 0 Shuhui Song 2 Dongmei Tian 2 Qiuyue Liu 0 Xiaojun Liang 1 Qing Ma 1 Min Sun 2 Jiandong Wang 1 Wenming Zhao 2 Guiling Cao 0 Jinxin Wang 0 Zhimin Yang 0 Ying Ge 0 Mingxing Chu 0 0 Key Laboratory of Farm Animal Genetic Resources and Germplasm Innovation of Ministry of Agriculture, Institute of Animal Science, Chinese Academy of Agricultural Sciences , No. 2, Yuanmingyuan West Rd, Beijing , China 1 Research Center of Grass and Livestock, Ningxia Academy of Agriculture and Forestry Sciences , Yinchuan, Ningxia , China 2 Core Genomic Facility, Beijing Institute of Genomics, Chinese Academy of Sciences , Beijing , China Background: Seasonal estrus is a critical limiting factor of animal fecundity, and it involves changes in both ovarian biology and hormone secretion in different seasons. Previous studies indicate that two classes of small RNAs (miRNAs and piRNAs) play important regulatory roles in ovarian biology. To understand the roles of small RNA-mediated post-transcriptional regulation in ovine seasonal estrus, the variation in expression patterns of ovarian small RNAs during anestrus and the breeding season were analyzed using Solexa sequencing technology. In addition, reproductive hormone levels were determined during ovine anestrus and the breeding season. Results: A total of 483 miRNAs (including 97 known, 369 conserved and 17 predicated novel miRNAs), which belong to 183 different miRNA families, were identified in ovaries of Tan sheep and Small Tail Han (STH) sheep. Compared with the three stages of the breeding season, 25 shared significantly differentially expressed (including 19 up- and six down-regulated) miRNAs were identified in ovine anestrus. KEGG Pathway analysis revealed that the target genes for some of the differentially expressed miRNAs were involved in reproductive hormone related pathways (e.g. steroid biosynthesis, androgen and estrogen metabolism and GnRH signaling pathway) as well as follicular/luteal development related pathways. Moreover, the expression of the differentially expressed miRNAs and most of their target genes were negatively correlated in the above pathways. Furthermore, the levels of estrogen, progesterone and LH in ovine anestrus were significantly lower than those in the breeding season. Combining the results of pathway enrichment analysis, expression of target genes and hormone measurement, we suggest that these differentially expressed miRNAs in anestrus might participate in attenuation of ovarian activity by regulating the above pathways. Besides miRNAs, a large and unexpectedly diverse set of piRNAs were also identified. Conclusions: The miRNA profiles of ovine ovaries in anestrus were presented for the first time. The identification and characterization of miRNAs that are differentially expressed between ovine anestrus and the breeding season will help understanding of the role of miRNAs in the regulation of seasonal estrus, and provides candidates for determining miRNAs which could be potentially used to regulate ovine seasonal estrus. Sheep; Seasonal estrus; Anestrus; Ovary; miRNA; piRNA - Background Many kinds of animal, such as sheep, horse, bird and fish, are seasonal breeders. Seasonal breeding is a critical limiting factor of animal fecundity. Most sheep in Northern China are estrous in the short-day season and anestrus in the long-day season [1]. Therefore, ewes cannot mate during anestrus and no lambs can be born for several months. Thus, for the mutton industry, seasonal estrus has been a bottleneck limiting efficient lamb meat supply throughout the year. MicroRNAs (miRNAs) belong to a large family of endogenous non-coding RNAs and have emerged as important post-transcriptional regulators. Many miRNAs have been identified in hircine ovary [2,3], mammary gland [4], testis [5], skin [6], hair [7], or ovine muscle [8]. Recently, genome-wide changes of miRNAs associated with follicular-luteal transition were identified in ovine ovary [9]. Previous studies in mice and pig indicated that miRNAs play critical roles in almost all ovarian biological processes [10-12]. For sheep, the obvious difference of ovarian biology exists between ovine anestrus and the breeding season. However the roles of miRNAs in the regulation of ovine seasonal estrus are unknown. Moreover, to date, only 153 (105 precursors) ovine miRNAs have been identified and listed in the miRBase database (Release 20). The characteristics of miRNA profiles in the ovine anestrus ovary are still unclear. PIWI-interacting RNAs (piRNAs) are a recently discovered class of small non-coding RNA with a typical length between 23 nt and 32 nt [13-15]. They are typically clustered in the genome in a mono-directional or bidirectional manner. They are highly expressed in sperm cells and have also been identified in oocytes and ovaries of Drosophila and mammals (...truncated)


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Ran Di, Jianning He, Shuhui Song, Dongmei Tian, Qiuyue Liu, Xiaojun Liang, Qing Ma, Min Sun, Jiandong Wang, Wenming Zhao, Guiling Cao, Jinxin Wang, Zhimin Yang, Ying Ge, Mingxing Chu. Characterization and comparative profiling of ovarian microRNAs during ovine anestrus and the breeding season, BMC Genomics, 2014, pp. 899, 15, DOI: 10.1186/1471-2164-15-899