A Testis-Specific Long Non-Coding RNA, lncRNA-Tcam1, Regulates Immune-Related Genes in Mouse Male Germ Cells

Kurihara, Misuzu; Otsuka, Kai; Matsubara, Shin; Shiraishi, Akira; Satake, Honoo; Kimura, Atsushi

doi:10.3389/fendo.2017.00299

Cited by 37 publications

(29 citation statements)

References 74 publications

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“…Total RNA was extracted from isolated follicles, purified, and treated with TURBO DNase as previously described (Matsubara et al, 2017). A total of 500 ng or 150 ng of quality-verified RNA from sieved follicles or further purified follicles, respectively, was subjected to RNA-seq analysis using a HiSeq1500 instrument (Illumina, San Diego, CA) in the rapid mode, as previously described (Kawada et al, 2017; Kurihara et al, 2017). The resultant reads were aligned to the Ciona cDNA library, which was downloaded from the ghost database (http://ghost.zool.kyoto-u.ac.jp/cgi-bin/gb2/gbrowse/kh/).…”

Section: Methodsmentioning

confidence: 99%

The regulation of oocyte maturation and ovulation in the closest sister group of vertebrates

Matsubara

Shiraishi

Osugi

et al. 2019

eLife

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Ascidians are the closest living relatives of vertebrates, and their study is important for understanding the evolutionary processes of oocyte maturation and ovulation. In this study, we first examined the ovulation of Ciona intestinalis Type A by monitoring follicle rupture in vitro, identifying a novel mechanism of neuropeptidergic regulation of oocyte maturation and ovulation. Ciona vasopressin family peptide (CiVP) directly upregulated the phosphorylation of extracellular signal–regulated kinase (CiErk1/2) via its receptor. CiVP ultimately activated a maturation-promoting factor, leading to oocyte maturation via germinal vesicle breakdown. CiErk1/2 also induced expression of matrix metalloproteinase (CiMMP2/9/13) in the oocyte, resulting in collagen degradation in the outer follicular cell layer and liberation of fertile oocytes from the ovary. This is the first demonstration of essential pathways regulating oocyte maturation and ovulation in ascidians and will facilitate investigations of the evolutionary process of peptidergic regulation of oocyte maturation and ovulation throughout the phylum Chordata.

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Section: Methodsmentioning

confidence: 99%

The regulation of oocyte maturation and ovulation in the closest sister group of vertebrates

Matsubara

Shiraishi

Osugi

et al. 2019

eLife

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“…It is exclusively expressed in mouse male germ cells and is assumed to play a crucial role in meiosis. In a recent report, it was found that lncRNA-Tcam1 regulates immune related genes in mouse germ cells [ 132 ]. The induction of lncRNA-tcam1 transcription using the tet-off system in GC-2 cells upregulated six genes, Trim30a, Ifit3, Tgtp2, Ifi47, Oas1g, and Gbp3.…”

Section: Introductionmentioning

confidence: 99%

Long non-coding RNAs (lncRNAs) in spermatogenesis and male infertility

Joshi

Rajender

2020

Reprod Biol Endocrinol

100

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Background Long non-coding RNAs (lncRNAs) have a size of more than 200 bp and are known to regulate a host of crucial cellular processes like proliferation, differentiation and apoptosis by regulating gene expression. While small noncoding RNAs (ncRNAs) such as miRNAs, siRNAs, Piwi-interacting RNAs have been extensively studied in male germ cell development, the role of lncRNAs in spermatogenesis remains largely unknown. Objective In this article, we have reviewed the biology and role of lncRNAs in spermatogenesis along with the tools available for data analysis. Results and conclusions Till date, three microarray and four RNA-seq studies have been undertaken to identify lncRNAs in mouse testes or germ cells. These studies were done on pre-natal, post-natal, adult testis, and different germ cells to identify lncRNAs regulating spermatogenesis. In case of humans, five RNA-seq studies on different germ cell populations, including two on sperm, were undertaken. We compared three studies on human germ cells to identify common lncRNAs and found 15 lncRNAs (LINC00635, LINC00521, LINC00174, LINC00654, LINC00710, LINC00226, LINC00326, LINC00494, LINC00535, LINC00616, LINC00662, LINC00668, LINC00467, LINC00608, and LINC00658) to show consistent differential expression across these studies. Some of the targets of these lncRNAs included CENPB, FAM98B, GOLGA6 family, RPGR, TPM2, GNB5, KCNQ10T1, TAZ, LIN28A, CDKN2B, CDKN2A, CDKN1A, CDKN1B, CDKN1C, EZH2, SUZ12, VEGFA genes. A lone study on human male infertility identified 9879 differentially expressed lncRNAs with three (lnc32058, lnc09522, and lnc98497) of them showing specific and high expression in immotile sperm in comparison to normal motile sperm. A few lncRNAs (Mrhl, Drm, Spga-lncRNAs, NLC1-C, HongrES2, Tsx, LncRNA-tcam1, Tug1, Tesra, AK015322, Gm2044, and LncRNA033862) have been functionally validated for their roles in spermatogenesis. Apart from rodents and humans, studies on sheep and bull have also identified lncRNAs potentially important for spermatogenesis. A number of these non-coding RNAs are strong candidates for further research on their roles in spermatogenesis.

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“…Tslrn1 is highly expressed in mouse primary spermatocytes, and mice with its knockout showed a significant reduction in spermatozoa [20]. Our group identified lncRNA-Tcam1 that is expressed at a high level in spermatocytes and suggested that it regulates immune-related genes for immune response during meiosis [88]. Downregulation of mrhl RNA is required for activation of Wnt signaling and the entry of spermatogonia into meiosis [89].…”

Section: Discussionmentioning

confidence: 99%

A novel testis-specific long noncoding RNA,Tesra, activates thePrss42/Tessp-2gene during mouse spermatogenesis†

Satoh

Takei

Kawamura

et al. 2018

Biology of Reproduction

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The progression of spermatogenesis is precisely controlled by meiotic stage-specific genes, but the molecular mechanism for activation of such genes is still elusive. Here we found a novel testis-specific long noncoding RNA (lncRNA), Tesra , that was specifically expressed in the mouse testis at the Prss/Tessp gene cluster on chromosome 9. Tesra was transcribed downstream of Prss44/Tessp-4 , starting within the gene, as a 4435-nucleotide transcript and developmentally activated at a stage similar to that for Prss/Tessp genes. By in situ hybridization, Tesra was found to be localized in and around germ cells and Leydig cells, being consistent with biochemical data showing its existence in cytoplasmic, nuclear, and extracellular fractions. Based on the finding of more signals in nuclei of pachytene spermatocytes, we explored the possibility that Tesra plays a role in transcriptional activation of Prss/Tessp genes. By a ChIRP assay, the Tesra transcript was found to bind to the Prss42/Tessp-2 promoter region in testicular germ cells, and transient overexpression of Tesra significantly activated endogenous Prss42/Tessp-2 expression and increased Prss42/Tessp-2 promoter activity in a reporter construct. These findings suggest that Tesra activates the Prss42/Tessp-2 gene by binding to the promoter. Finally, we investigated whether Tesra co-functioned with enhancers adjacent to another lncRNA, lncRNA-HSVIII . In the Tet-on system, Tesra transcription significantly increased activity of one enhancer, but Tesra and the enhancer were not interdependent. Collectively, our results proposed a potential function of an lncRNA, Tesra , in transcriptional activation and suggest a novel relationship between an lncRNA and an enhancer.

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A Testis-Specific Long Non-Coding RNA, lncRNA-Tcam1, Regulates Immune-Related Genes in Mouse Male Germ Cells

Cited by 37 publications

References 74 publications

The regulation of oocyte maturation and ovulation in the closest sister group of vertebrates

The regulation of oocyte maturation and ovulation in the closest sister group of vertebrates

Long non-coding RNAs (lncRNAs) in spermatogenesis and male infertility

A novel testis-specific long noncoding RNA,Tesra, activates thePrss42/Tessp-2gene during mouse spermatogenesis†

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