Functional compensation for the loss of testis-specific poly(A)-binding protein, PABPC2, during mouse spermatogenesis

Kashiwabara, Shin‐ichi; Tsuruta, Satsuki; Okada, Keitaro; Saegusa, Ayaka; Miyagaki, Yu; Baba, Tadashi

doi:10.1262/jrd.2016-023

Cited by 11 publications

(8 citation statements)

References 36 publications

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“…The recombinant proteins were purified on a Ni-NTA His column (Merck Millipore, Billerica, MA, USA), emulsified with Freund’s complete or incomplete adjuvant (Becton Dickinson, Franklin Lakes, NJ, USA), and injected intradermally into female New Zealand White rabbits (Japan SLC) [25]. Each antiserum was fractionated with ammonium sulfate (0–40% saturation), followed by immunoaffinity chromatography on a Sepharose 4B (GE Healthcare, Piscataway, NJ, USA) column conjugated with the same protein region fused to glutathione S -transferase (GST) [26]. The anti-PAPOLB antibody was prepared as described previously [22].…”

Section: Methodsmentioning

confidence: 99%

Adenylation by testis-specific cytoplasmic poly(A) polymerase, PAPOLB/TPAP, is essential for spermatogenesis

Kashiwabara

Tsuruta

Okada

et al. 2016

Journal of Reproduction and Development

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The testis-specific cytoplasmic poly(A) polymerase PAPOLB/TPAP is essential for spermatogenesis. Although this enzyme is responsible for poly(A) tail extension of a subset of mRNAs in round spermatids, the stability and translational efficiency of these mRNAs are unaffected by the absence of PAPOLB. To clarify the functional importance of this enzyme’s adenylation activity, we produced PAPOLB-null mice expressing a polyadenylation-defective PAPOLB mutant (PAPOLBD114A), in which the catalytic Asp at residue 114 was mutated to Ala. Introducing PAPOLBD114A failed to rescue PAPOLB-null phenotypes, such as reduced expression of haploid-specific mRNAs, spermiogenesis arrest, and male infertility. These results suggest that PAPOLB regulates spermatogenesis through its adenylation activity.

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Section: Methodsmentioning

confidence: 99%

Adenylation by testis-specific cytoplasmic poly(A) polymerase, PAPOLB/TPAP, is essential for spermatogenesis

Kashiwabara

Tsuruta

Okada

et al. 2016

Journal of Reproduction and Development

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“…Other genes involved in the process are well-described, including Boll , Dazl and Tdrd 5/1/6/9 [49–53]. Another gene involved in this functional category is Papbc2, an RNA-binding protein that plays a role in the translational regulation of the mRNAs required in the later stages of spermatogenesis [54]. Its paralog Papbc6 is tagged with “RNA binding” GO, but has no known phenotypical function in the literature.…”

Section: Discussionmentioning

confidence: 99%

An evolutionary approach to recover genes predominantly expressed in the testes of the zebrafish, chicken and mouse

et al. 2019

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Background Previously, we have demonstrated that genes involved in ovarian function are highly conserved throughout evolution. In this study, we aimed to document the conservation of genes involved in spermatogenesis from flies to vertebrates and their expression profiles in vertebrates. Results We retrieved 379 Drosophila melanogaster genes that are functionally involved in male reproduction according to their mutant phenotypes and listed their vertebrate orthologs. 83% of the fly genes have at least one vertebrate ortholog for a total of 625 mouse orthologs. This conservation percentage is almost twice as high as the 42% rate for the whole fly genome and is similar to that previously found for genes preferentially expressed in ovaries. Of the 625 mouse orthologs, we selected 68 mouse genes of interest, 42 of which exhibited a predominant relative expression in testes and 26 were their paralogs. These 68 mouse genes exhibited 144 and 60 orthologs in chicken and zebrafish, respectively, gathered in 28 groups of paralogs. Almost two thirds of the chicken orthologs and half of the zebrafish orthologs exhibited a relative expression ≥50% in testis. Finally, our focus on functional in silico data demonstrated that most of these genes were involved in the germ cell process, primarily in structure elaboration/maintenance and in acid nucleic metabolism. Conclusion Our work confirms that the genes involved in germ cell development are highly conserved across evolution in vertebrates and invertebrates and display a high rate of conservation of preferential testicular expression among vertebrates. Among the genes highlighted in this study, three mouse genes ( Lrrc46, Pabpc6 and Pkd2l1 ) have not previously been described in the testes, neither their zebrafish nor chicken orthologs. The phylogenetic approach developed in this study finally allows considering new testicular genes for further fundamental studies in vertebrates, including model species (mouse and zebrafish). Electronic supplementary material The online version of this article (10.1186/s12862-019-1462-8) contains supplementary material, which is available to authorized users.

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“…All [114] Cytoplasm Nucleus [114,117] Not determined --PABPC1L Testis Ovary Early embryos [119] Cytoplasm [119] Nucleus [75] Male: fertile Female: infertile [119] Failure to produce mature eggs [119] Maternal mRNA translational activation [119] Smaller in size, containing peripheral germinal vesicles, and loosely associated with cumulus cells [76] Chromatin reorganization and transcriptional silencing [76] Defective cumulus expansion [77] Regulating cumulus and granulosa cell functions [77] Disrupted transzonal processes (TZPs) and gap junctions at the preantral stage of folliculogenesis [74] Maintaining oocyte-somatic communication [74] PABPC2 Testis [17] Cytoplasm [17,75] Male: fertile [58] No effect [58] No effect [58] PABPN1 All [114] Cytoplasm Nucleus [114] Not determined --…”

Section: Pabpc1mentioning

confidence: 99%

Revisiting poly(A)‐binding proteins: Multifaceted regulators during gametogenesis and early embryogenesis

Zhao

Fan

2021

BioEssays

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Post-transcriptional regulation faces a distinctive challenge in gametes. Transcription is limited when the germ cells enter the division phase due to condensed chromatin, while gene expression during gamete maturation, fertilization, and early cleavage depends on existing mRNA post-transcriptional coordination. The dynamics of the 3ʹ-poly(A) tail play crucial roles in defining mRNA fate. The 3ʹ-poly(A) tail is covered with poly(A)-binding proteins (PABPs) that help to mediate mRNA metabolism and recent work has shed light on the number and function of germ cell-specific expressed PABPs. There are two structurally different PABP groups distinguished by their cytoplasmic and nuclear localization. Both lack catalytic activity but are coupled with various roles through their interaction with multifunctional partners during mRNA metabolism. Here, we present a synopsis of PABP function during gametogenesis and early embryogenesis and describe both conventional and current models of the functions and regulation of PABPs, with an emphasis on the physiological significance of how germ cell-specific PABPs potentially affect human fertility.

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Functional compensation for the loss of testis-specific poly(A)-binding protein, PABPC2, during mouse spermatogenesis

Cited by 11 publications

References 36 publications

Adenylation by testis-specific cytoplasmic poly(A) polymerase, PAPOLB/TPAP, is essential for spermatogenesis

Adenylation by testis-specific cytoplasmic poly(A) polymerase, PAPOLB/TPAP, is essential for spermatogenesis

An evolutionary approach to recover genes predominantly expressed in the testes of the zebrafish, chicken and mouse

Revisiting poly(A)‐binding proteins: Multifaceted regulators during gametogenesis and early embryogenesis

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