Three Testis-Specific Paralogous Serine Proteases Play Different Roles in Murine Spermatogenesis and Are Involved in Germ Cell Survival During Meiosis1

Yoneda, Ryoma; Takahashi, Takayuki; Matsui, Hitoshi; Takano, Naoharu; Hasebe, Yuko; Ogiwara, Katsueki; Kimura, Atsushi

doi:10.1095/biolreprod.112.106328

Cited by 27 publications

(51 citation statements)

References 70 publications

(88 reference statements)

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“…Germ cells were isolated from the mouse testis as previously described [5]. The germ cells were further fractionated into nuclear, membrane, and cytoplasmic subfractions as previously described [8].…”

Section: Isolation Of Germ Cells and Their Fractionation Into Nuclearmentioning

confidence: 99%

“…Western blot analysis was conducted as previously described [5]. The antibody against Prss41/Tessp-1 5 was generated before [7].…”

Section: Western Blot Analysismentioning

confidence: 99%

“…Organ culture of mouse testis fragments was performed as previously described [5], but this time we harvested 7-day-old testes and cultured for 14 days. A part of cultured testis fragments were fixed with Bouin's solution for 18 h at 4°C, and paraffin sections were made to be stained with hematoxylin.…”

Section: Organ Culture Of Testis Fragments With the Prss41/tessp-1 Anmentioning

confidence: 99%

“…We have focused on serine proteases, which are the largest family among the four protease families in mammals [3], during meiosis in murine spermatogenesis. We cloned four testis-specific serine proteases from the mouse testis, and three of them, namely, Prss42/Tessp-2, Prss43/Tessp-3, and Prss44/Tessp-4, are encoded by genes that consist of a cluster at chromosome 9 [4,5]. Although the three genes are paralogs that have similar primary structures, their functions seem to be different.…”

Section: Introductionmentioning

confidence: 99%

“…Although the three genes are paralogs that have similar primary structures, their functions seem to be different. Especially, Prss42/Tessp-2 and Prss43/Tessp-3 are necessary for the progression of meiosis in secondary and primary spermatocytes, respectively, during in vitro spermatogenesis [5].…”

Section: Introductionmentioning

confidence: 99%

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A testis-specific serine protease, Prss41/Tessp-1, is necessary for the progression of meiosis during murine in vitro spermatogenesis

Yoneda

Kimura

2013

Biochemical and Biophysical Research Communications

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The function of protease during male meiosis has not been well studied. We previously cloned and characterized four testis-specific serine proteases in the mouse testis. One of the proteases, Prss41/Tessp-1, was expressed in the germ and Sertoli cell. This time, to examine the involvement of Prss41/Tessp-1 in spermatogenesis, we conducted the organ culture of testis fragments in the presence of the anti-Prss41/Tessp-1 antibody. Because in the Sertoli cell, the Prss41/Tessp-1 protein was mostly associated with the membrane of intracellular organelles by glycosylphosphatidylinositol, the antibody was expected to affect Prss41/Tessp-1 at the plasma membrane of spermatogonia. By adding the antibody, the number of germ cells was decreased in some seminiferous tubules. The marker genes expression strongly suggested that meiosis was arrested at spermatogonia, and the number of apoptotic germ cells increased by terminal deoxynucleotidyl transferase dUTP nick end labeling assay. These data indicated that Prss41/Tessp-1 was necessary for the progression of meiosis at the stage of spermatogonia during in vitro spermatogenesis. Together with our previous study, the current results suggest that the Prss/Tessp proteases are important for the progression of meiosis at each stage.

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Section: Isolation Of Germ Cells and Their Fractionation Into Nuclearmentioning

confidence: 99%

“…Western blot analysis was conducted as previously described [5]. The antibody against Prss41/Tessp-1 5 was generated before [7].…”

Section: Western Blot Analysismentioning

confidence: 99%

Section: Organ Culture Of Testis Fragments With the Prss41/tessp-1 Anmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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A testis-specific serine protease, Prss41/Tessp-1, is necessary for the progression of meiosis during murine in vitro spermatogenesis

Yoneda

Kimura

2013

Biochemical and Biophysical Research Communications

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Male fertility in Mus musculus requires the activity of TRYX5 in sperm migration into the oviduct

Zhang

Cui

et al. 2020

Journal Cellular Physiology

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Nowadays, abnormal loss of serine proteases appears very frequently in male patients with unexplained sterility. In fact, many testis-specific serine proteases, the largest family among the four protease families implicated in murine spermatogenesis, are indispensable for reproduction. In the present study, we demonstrate that the previously uncharacterized testis-specific serine protease TRYX5 (1700074P13Rik) is required for male fertility in mice. Tryx5 −/− male mice are sterile, yet they have normal spermatogenesis and normal sperm parameters. In vivo fertilization experiments showed that the fertilization rate of Tryx5 −/− sperm was almost zero. Sperm counting and analysis of paraffin sections of oviducts revealed that Tryx5 −/− sperm were unable to migrate into the oviduct, which is likely the cause of the observed infertility of the Tryx5 −/− male mice. Importantly, we also found that there was almost no mature ADAM3 present in Tryx5 −/− sperm and almost no ADAM3 precursor in Tryx5 −/− elongated spermatids of S13-16 stage, even though testes of Tryx5 −/− and wild type mice had the same amount of the total precursor ADAM3. Collectively, our results demonstrate that Tryx5 is essential for male fertility in mice and suggest that TRYX5 functions in the stability or localization of ADAM3 precursor in elongated spermatids S13-16 stage, thereby regulating the ability of sperm to migrate from the uterus into the ampulla of the oviduct, the site of fertilization. K E Y W O R D Sknockout mouse, male infertility, sperm migration, Tryx5

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A genomic region transcribed into a long noncoding RNA interacts with the Prss42/Tessp‐2 promoter in spermatocytes during mouse spermatogenesis, and its flanking sequences can function as enhancers

Yoneda

Satoh

Yoshida

et al. 2016

Molecular Reproduction Devel

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SUMMARYSpermatogenesis is precisely regulated by many meiotic stage-specific genes, but their regulatory mechanisms are not fully understood. The Prss/Tessp gene cluster is located on the mouse chromosome 9F2-F3, and the three genes, Prss42/Tessp-2, Prss43/Tessp-3, and Prss44/Tessp-4 on the cluster, are specifically activated in pachytene spermatocytes during meiosis. To elucidate a mechanism of their activation, we searched for DNase I hypersensitive sites (HSs) and long noncoding RNAs (lncRNAs) at the Prss/Tessp locus. We found eight DNase I HSs, three of which were testicular germ cell-specific at or close to the Prss42/Tessp-2 promoter, and a testis-specific lncRNA, lncRNA-HSVIII, which was transcribed from 3' to the Prss42/Tessp-2 gene. By in situ hybridization, lncRNA-HSVIII was localized in nuclei of most pachytene spermatocytes and in cytosols of pachytene spermatocytes at stage X and spermatids. Chromosome conformation capture assay showed that the chromatin at lncRNA-HSVIII specifically interacted with the Prss42/Tessp-2 promoter in primary and secondary spermatocytes. By reporter gene assay, a 5.8-kb genome sequence, encompassing the entire lncRNA-HSVIII sequence and its flanking regions, significantly increased Prss42/Tessp-2 promoter activity, but transfection of this construct did not change the lncRNA-HSVIII expression, which indicated that the increased promoter activity was likely to be dependent on enhancer activity. Indeed, we found that both upstream and downstream regions of the lncRNA-HSVIII sequence significantly increased Prss42/Tessp-2 promoter activity. Our data indicate the direct interaction of a genomic region at lncRNA-HSVIII with the Prss42/Tessp-2 promoter in spermatocytes and suggest that adjacent sequences to the lncRNA function as enhancers for the Prss42/Tessp-2 gene.4

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Three Testis-Specific Paralogous Serine Proteases Play Different Roles in Murine Spermatogenesis and Are Involved in Germ Cell Survival During Meiosis1

Cited by 27 publications

References 70 publications

A testis-specific serine protease, Prss41/Tessp-1, is necessary for the progression of meiosis during murine in vitro spermatogenesis

A testis-specific serine protease, Prss41/Tessp-1, is necessary for the progression of meiosis during murine in vitro spermatogenesis

Male fertility in Mus musculus requires the activity of TRYX5 in sperm migration into the oviduct

A genomic region transcribed into a long noncoding RNA interacts with the Prss42/Tessp‐2 promoter in spermatocytes during mouse spermatogenesis, and its flanking sequences can function as enhancers

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