Long noncoding RNA expression profile changes associated with dietary energy in the sheep testis during sexual maturation

Abstract

Spermatogenesis can be affected by nutrition, which operates through normal physiological processes by changing the testicular mass and hormone levels profoundly. However, little is known regarding how testis development is regulated by long noncoding RNA (lncRNA). In this study, we investigated the effects of high-grain (HG) feeding on testis development during sexual maturation mediated by lncRNA. The HG diet group showed an increase in growth hormone (GH), insulin-like growth factor-1 (IGF-1) and testosterone (T) levels, and in the number of sperm in the seminiferous tubules compared with the hay-fed group (p < 0.05). Moreover, we found 59 differentially expressed (DE) lncRNAs and 229 DE mRNAs in sheep testis between the two groups. qRT-PCR results of 20 randomly selected DE lncRNAs and mRNAs were also consistent with the RNA-seq data. Through functional enrichment analysis and lncRNA-mRNA interaction network analysis, we screened several lncRNAs that may be enriched for male reproduction such as spermatogenesis, sperm motility, steroid hormones, MAPK and ErbB signaling pathways. This study provides a first insight into the development of the testis with HG feeding in sheep and shows that these changes are associated with alterations in lncRNA expression.In the current intensive sheep production system in China, most rams are fed high-energy diets after sexual maturation, in order to maximize their body weight gain. High-energy diets with adequate protein, vitamins, and minerals may also hasten testis development and spermatogenesis 1 . However, the process of spermatogenesis is complicated and involves strict developmental regulations at both the transcriptional and the post-transcriptional level 2 . It is difficult to have a thorough understanding of the effects of nutrition on spermatogenesis. Among the regulators of spermatogenesis, recent years researchers have shifted their focus to post-transcriptional control mediated by noncoding RNAs (ncRNAs), which has emerged as an important regulator of spermatogenesis. The ncRNAs such as microRNA (miRNA) 3,4 , PIWI-interacting RNA (piRNA) 5,6 , small interfering RNA (siRNA) 7 and lncRNA 8-10 are known to play regulatory role in male germ cell development. Evidence revealed that the reductions in spermatozoal quality induced by under-nutrition were mediated by changes in expression of miRNAs and piRNAs 11 . A recent study also found miRNAs were involved in sheep abnormal reproductive morphology, apoptosis and male infertility response to under-nutrition 12 . Despite the findings, the understanding of how ncRNAs associated with effects of nutrition on spermatogenesis in the adult testis remains limited.The lncRNAs are one of the most abundant ncRNA families which are more than 200 nucleotides in length. Studies have demonstrated lncRNAs as a new regulatory molecule are involved in mammalian development 13,14 . Recently, many lncRNAs have been identified in specific developmental stages of testes and spermatogenesis in mouse, rat and human models. They are predicte...

Assembly and validation of conserved long non-coding RNAs in the ruminant transcriptome

“…Although most of the lncRNAs (n = 4972, 64% of the 7809 lncRNAs with average TPM > 1 in at least one tissue) have idiosyncratic ‘mixed expression’ profiles (see Methods), 1339 lncRNAs (17%) are nevertheless detected at an average TPM > 1 in all 13 tissues (Table S19). Many are enriched in specific tissues, with 904 (12%) lncRNAs exhibiting a testes-specific expression pattern, consistent with a previous study identifying numerous lncRNAs involved in ovine testicular development and spermatogenesis [71].…”

Changes in long non-coding RNA expression profiles related to the antagonistic effects of Escherichia coli F17 on lamb spleens

“…we found that the expression level of lncRNAs was lower than mRNAs in lamb spleens (Fig. 4 ), which was in agreement with the results from sheep testicular tissues 9 , and the average lengths of lncRNAs and mRNAs in sheep were longer than those in pigs (1,713 bp and 1,983 bp, respectively) 20 . We searched for all the coding genes within the 100-kb flanking regions of the lncRNAs and identified intersecting genes that were significantly co-expressed with the lncRNAs as indicated by Pearson correlation calculations 23 .…”

Comparative Transcriptome Profiling of mRNA and lncRNA Related to Tail Adipose Tissues of Sheep

“…We identified 9,082 lncRNAs from tail fat of LFTS, STHS, and TS, and most of them belong to intergenic lncRNAs. LncRNAs from tail fats are relatively abundant compared with these from other tissues, such as 6,924 and 5,602 lncRNAs from muscle and blood samples of Hu sheep, respectively ( Zhang et al, 2017 ; Feng et al, 2018 ). The tail fat lncRNAs also share several typical characters with other mammalian lncRNAs.…”