Spermiogenesis and Male Fertility Require the Function of Suppressor of Hairy-Wing in Somatic Cyst Cells of Drosophila

Tingting Duan; Pamela K Geyer

doi:10.1534/genetics.118.301088

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Spermiogenesis and Male Fertility Require the Function of Suppressor of Hairy-Wing in Somatic Cyst Cells of Drosophila

Journal article

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Peer reviewed

Spermiogenesis and Male Fertility Require the Function of Suppressor of Hairy-Wing in Somatic Cyst Cells of Drosophila

Tingting Duan and Pamela K Geyer

Genetics (Austin), Vol.209(3), pp.757-772

07/2018

DOI: 10.1534/genetics.118.301088

PMCID: PMC6028245

PMID: 29739818

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Abstract

Suppressor of Hairy-wing [Su(Hw)] protein is an example of a multivalent transcription factor. Although best known for its role in establishing the chromatin insulator of the retrotransposon, Su(Hw) functions as an activator and repressor at non- genomic sites. It remains unclear how the different regulatory activities of Su(Hw) are utilized during development. Motivated from observations of spatially restricted expression of Su(Hw) in the testis, we investigated the role of Su(Hw) in spermatogenesis to advance an understanding of its developmental contributions as an insulator, repressor, and activator protein. We discovered that Su(Hw) is required for sustained male fertility. Although dynamics of Su(Hw) expression coincide with changes in nuclear architecture and activation of coregulated testis-specific gene clusters, we show that loss of Su(Hw) does not disrupt meiotic chromosome pairing or transcription of testis-specific genes, suggesting that Su(Hw) has minor architectural or insulator functions in the testis. Instead, Su(Hw) has a prominent role as a repressor of neuronal genes, consistent with suggestions that Su(Hw) is a functional homolog of mammalian REST, a repressor of neuronal genes in non-neuronal tissues. We show that Su(Hw) regulates transcription in both germline and somatic cells. Surprisingly, the essential spermatogenesis function of Su(Hw) resides in somatic cyst cells, implying context-specific consequences due to loss of this transcription factor. Together, our studies highlight that Su(Hw) has a major developmental function as a transcriptional repressor, with the effect of its loss dependent upon the cell-specific factors.

Animals

Drosophila - physiology

Drosophila Proteins - genetics

Drosophila Proteins - metabolism

Fertility - genetics

Gene Expression Regulation, Developmental

Gene Regulatory Networks

Male

Organ Specificity

Repressor Proteins - genetics

Repressor Proteins - metabolism

Spermatogenesis

Testis - growth & development

Testis - metabolism

Transcription, Genetic

Details

Title: Subtitle: Spermiogenesis and Male Fertility Require the Function of Suppressor of Hairy-Wing in Somatic Cyst Cells of Drosophila
Creators: Tingting Duan - University of Iowa
Pamela K Geyer - University of Iowa
Resource Type: Journal article
Publication Details: Genetics (Austin), Vol.209(3), pp.757-772
DOI: 10.1534/genetics.118.301088
PMID: 29739818
PMCID: PMC6028245
NLM abbreviation: Genetics
ISSN: 0016-6731
eISSN: 1943-2631
Grant note: R01 GM042539 / NIGMS NIH HHS P30 CA086862 / NCI NIH HHS
Language: English
Date published: 07/2018
Academic Unit: Obstetrics and Gynecology; Biochemistry and Molecular Biology
Record Identifier: 9984288729202771

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