Nascent polypeptide-associated complex as tissue-specific cofactor during germinal cell differentiation in Drosophila testes

Kogan, Galina L.; Akulenko, Natalia; Abramov, Yu. A.; Fefelova, Elena; Гвоздев, В. А.

doi:10.1134/s0026893317040112

Cited by 11 publications

(37 citation statements)

References 29 publications

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“…These genes are represented by two distinct closely related, but non-adjacent pairs and an additional pair outside these two pairs, as paralogs of the ubiquitously expressed bicaudal (bic) gene encoding β-subunit of NAC protein [30] as well as in Flybase. β NACtes are paralogs of the ubiquitously expressed bicaudal (bic) gene encoding β-subunit of NAC protein [7]. The specific expression of these genes in testis spermatocytes, but not in somatic testes cells, has been demonstrated [7].…”

Section: Resultsmentioning

confidence: 99%

“…β NACtes are paralogs of the ubiquitously expressed bicaudal (bic) gene encoding β-subunit of NAC protein [7]. The specific expression of these genes in testis spermatocytes, but not in somatic testes cells, has been demonstrated [7]. The gene CG4415 product carries α-NAC domain and was shown to be expressed in embryonic gonad (Fisher et al, 2012, Flybase).…”

Section: Resultsmentioning

confidence: 99%

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Detection of the germline specific NAC protein paralog enriched by intrinsically disordered regions inDrosophila melanogaster

Kogan

Mikhaleva

et al. 2021

Preprint

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Nascent polypeptide associated complex (NAC) consisting of α- and β-subunits is an essential conserved ubiquitously expressed ribosome-associated protein in eukaryotes. NAC is considered as a chaperone and co-translational regulator of nascent protein sorting providing homeostasis of cellular proteins. Here we discovered the germinal cell specific NAC (gNAC) homologue, which differs from the ubiquitously expressed NAC by the presence of expanded intrinsically disordered regions (IDRs) at the N- and C-ends of the α- and β-subunits, respectively. We propose this evolutionary acquisition of long IDRs drive gNAC to endow both the specific conformational plasticity for binding client proteins and novel functions regulated by post-transcriptional modifications (PTM). At the same time, we demonstrated that the well-known lethal effect of the loss of ubiquitous NAC-β is suppressed by ectopic expression of its germinal paralog indicating the absence of strict functional differences between the ubiquitous and germline NAC-β subunit paralogs for protein homeostasis.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Detection of the germline specific NAC protein paralog enriched by intrinsically disordered regions inDrosophila melanogaster

Kogan

Mikhaleva

et al. 2021

Preprint

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“…βNACtes6 is one of six βNACtes paralogs in Drosophila that are located in the middle of the arm of the X chromosome (five in cytogenetic region 12E and one in 13D). The names of these βNAC paralogs include the suffix testis (tes) because they were previously shown to be highly expressed in the D. melanogaster male germline during spermatogenesis where they associate with ribosomes (Kogan et al 2017). However, examination of RNA-Seq data from the modENCODE project indicated that there is a pulse of expression of all six of these paralogs in wandering larval 3 rd instar imaginal discs, explaining how knockdown of a gene named for its testis expression could impair growth of wing tissue (Graveley et al 2011).…”

Section: Resultsmentioning

confidence: 99%

An RNAi Screen for Genes Required for Growth ofDrosophilaWing Tissue

Rotelli

Bolling

Killion

et al. 2019

G3 Genes|Genomes|Genetics

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Cell division and tissue growth must be coordinated with development. Defects in these processes are the basis for a number of diseases, including developmental malformations and cancer. We have conducted an unbiased RNAi screen for genes that are required for growth in the Drosophila wing, using GAL4-inducible short hairpin RNA (shRNA) fly strains made by the Drosophila RNAi Screening Center. shRNA expression down the center of the larval wing disc using dpp-GAL4, and the central region of the adult wing was then scored for tissue growth and wing hair morphology. Out of 4,753 shRNA crosses that survived to adulthood, 18 had impaired wing growth. FlyBase and the new Alliance of Genome Resources knowledgebases were used to determine the known or predicted functions of these genes and the association of their human orthologs with disease. The function of eight of the genes identified has not been previously defined in Drosophila. The genes identified included those with known or predicted functions in cell cycle, chromosome segregation, morphogenesis, metabolism, steroid processing, transcription, and translation. All but one of the genes are similar to those in humans, and many are associated with disease. Knockdown of lin-52, a subunit of the Myb-MuvB transcription factor, or βNACtes6, a gene involved in protein folding and trafficking, resulted in a switch from cell proliferation to an endoreplication growth program through which wing tissue grew by an increase in cell size (hypertrophy). It is anticipated that further analysis of the genes that we have identified will reveal new mechanisms that regulate tissue growth during development.

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“…Another fraction of the testes, 38.8% (n = 19), exhibited a mosaic phenotype characterized by the presence of small germ cell clusters along with the cysts of spermatogonial cells and spermatocytes (not shown). We found that the level of Piwi, marker of GSCs, returned to wild-type and the marker of spermatocytes βNACtes [52] was restored to the wild-type level indicating the maintenance of the spermatocyte population in the "rescued" testes ( Figure 3E). In the wild-type testes the expected number of spectrosomes does not exceed 30.…”

Section: Ectopic Expression Of β-Integrin Rescued Early Stages Of Spementioning

confidence: 89%

The Drosophila RNA Helicase Belle (DDX3) Non-Autonomously Suppresses Germline Tumorigenesis Via Regulation of a Specific mRNA Set

Kotov

Godneeva

Olenkina

et al. 2020

Cells

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DDX3 subfamily DEAD-box RNA helicases are essential developmental regulators of RNA metabolism in eukaryotes. belle, the single DDX3 ortholog in Drosophila, is required for fly viability, fertility, and germline stem cell maintenance. Belle is involved both in translational activation and repression of target mRNAs in different tissues; however, direct targets of Belle in the testes are essentially unknown. Here we showed that belle RNAi knockdown in testis cyst cells caused a disruption of adhesion between germ and cyst cells and generation of tumor-like clusters of stem-like germ cells. Ectopic expression of β-integrin in cyst cells rescued early stages of spermatogenesis in belle knockdown testes, indicating that integrin adhesion complexes are required for the interaction between somatic and germ cells in a cyst. To address Belle functions in spermatogenesis in detail we performed cross-linking immunoprecipitation and sequencing (CLIP-seq) analysis and identified multiple mRNAs that interacted with Belle in the testes. The set of Belle targets includes transcripts of proteins that are essential for preventing the tumor-like clusters of germ cells and for sustaining spermatogenesis. By our hypothesis, failures in the translation of a number of mRNA targets additively contribute to developmental defects observed in the testes with belle knockdowns both in cyst cells and in the germline.

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Nascent polypeptide-associated complex as tissue-specific cofactor during germinal cell differentiation in Drosophila testes

Cited by 11 publications

References 29 publications

Detection of the germline specific NAC protein paralog enriched by intrinsically disordered regions inDrosophila melanogaster

Detection of the germline specific NAC protein paralog enriched by intrinsically disordered regions inDrosophila melanogaster

An RNAi Screen for Genes Required for Growth ofDrosophilaWing Tissue

The Drosophila RNA Helicase Belle (DDX3) Non-Autonomously Suppresses Germline Tumorigenesis Via Regulation of a Specific mRNA Set

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