Src64 controls a novel actin network required for proper ring canal formation in the <i>Drosophila</i> male germline

Eikenes, Åsmund Husabø; Malerød, Lene; Lie-Jensen, Anette; Wegner, Catherine S.; Brech, Andreas; Liestøl, Knut; Stenmark, Harald; Haglund, Kaisa

doi:10.1242/dev.124370

Cited by 12 publications

(4 citation statements)

References 52 publications

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“…The presence of septins at germline ring canals during oogenesis was not entirely clear; concentrations of Sep2, Pnut, and Sep1 were sometimes observed at female germline ring canals ( Fares et al 1995 ; Adam 1999 ). The double ring localization of septin-GFPs is similar to the localization of phospho-tyrosine immunostaining found at male germline ring canals ( Eikenes et al 2015 ), and is reminiscent of the double septin ring at the bud neck of S. cerevisiae ( Jiménez et al 1998 ; Renz et al 2016 ) and the double ring localization of Hts-RC in this study ( Figure S1 , F and G); thus, double ring localization may be an aspect of germline ring canal structure and a function that warrants further investigation. Although septins are not required for ring canal formation in the female germline, it is conceivable they might have a nonessential role at their outer rims, perhaps by maintaining membrane shape or rigidity ( Tanaka-Takiguchi et al 2009 ; Tooley et al 2009 ; Mostowy et al 2011 ; Gilden et al 2012 ), regulating membrane remodelling ( Sellin et al 2011b ), acting as a lateral diffusion barrier ( Schmidt and Nichols 2004 ; Caudron and Barral 2009 ; Hu et al 2010 ; Kwitny et al 2010 ; Spiliotis and Gladfelter 2012 ; Clay et al 2014 ; Ewers et al 2014 ), or protein scaffolding ( Hanrahan and Snyder 2003 ; Kozubowski et al 2005 ; Kinoshita 2006 ; Hagiwara et al 2011 ; Hall and Russell 2012 ; Feng et al 2015 ).…”

Section: Discussionsupporting

confidence: 72%

Partial Functional Diversification ofDrosophila melanogasterSeptin GenesSep2andSep5

O’Neill

Clark

2016

G3 Genes|Genomes|Genetics

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The septin family of hetero-oligomeric complex-forming proteins can be divided into subgroups, and subgroup members are interchangeable at specific positions in the septin complex. Drosophila melanogaster has five septin genes, including the two SEPT6 subgroup members Sep2 and Sep5. We previously found that Sep2 has a unique function in oogenesis, which is not performed by Sep5. Here, we find that Sep2 is uniquely required for follicle cell encapsulation of female germline cysts, and that Sep2 and Sep5 are redundant for follicle cell proliferation. The five D. melanogaster septins localize similarly in oogenesis, including as rings flanking the germline ring canals. Pnut fails to localize in Sep5; Sep2 double mutant follicle cells, indicating that septin complexes fail to form in the absence of both Sep2 and Sep5. We also find that mutations in septins enhance the mutant phenotype of bazooka, a key component in the establishment of cell polarity, suggesting a link between septin function and cell polarity. Overall, this work suggests that Sep5 has undergone partial loss of ancestral protein function, and demonstrates redundant and unique functions of septins.

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Section: Discussionsupporting

confidence: 72%

Partial Functional Diversification ofDrosophila melanogasterSeptin GenesSep2andSep5

O’Neill

Clark

2016

G3 Genes|Genomes|Genetics

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“…Src64 also might regulate myosin activity or actin dynamics during microfilament ring contraction. Src64 has been implicated in actin regulation in many contexts, including ovarian ring canal growth, male germline ring canal formation, and eye epithelial tumors (Dodson et al, ; Eikenes et al, ; Guarnieri, Dodson, & Simon, ; Lu, Guarnieri, & Simon, ; O'Reilly et al, ; Roulier, Panzer, & Beckendorf, ; Strong et al, ; Turkel et al, ). Src64 is involved in assembling the contractile ring during wound healing in Drosophila (Tsarouhas, Yao, & Samakovlis, ).…”

Section: Discussionmentioning

confidence: 99%

Actomyosin contraction during cellularization is regulated in part by Src64 control of Actin 5C protein levels

Carter

Gadwala

Chougule

et al. 2019

Genesis

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Summary Src64 is required for actomyosin contraction during cellularization of the Drosophila embryonic blastoderm. The mechanism of actomyosin ring constriction is poorly understood even though a number of cytoskeletal regulators have been implicated in the assembly, organization, and contraction of these microfilament rings. How these cytoskeletal processes are regulated during development is even less well understood. To investigate the role of Src64 as an upstream regulator of actomyosin contraction, we conducted a proteomics screen to identify proteins whose expression levels are controlled by src64. Global levels of actin are reduced in src64 mutant embryos. Furthermore, we show that reduction of the actin isoform Actin 5C causes defects in actomyosin contraction during cellularization similar to those caused by src64 mutation, indicating that a relatively high level of Actin 5C is required for normal actomyosin contraction and furrow canal structure. However, reduction of Actin 5C levels only slows down actomyosin ring constriction rather than preventing it, suggesting that src64 acts not only to modulate actin levels, but also to regulate the actomyosin cytoskeleton by other means.

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“…GSCs divide asymmetrically, giving rise to one daughter that remains a GSC and a cystoblast that differentiates. Delayed abscission between the GSC and cystoblast keeps the pair connected well into G2 of the subsequent cell cycle (Ables and Drummond-Barbosa, 2013; Eikenes Å et al, 2015; Hinnant et al, 2017; Mathieu et al, 2013; Matias et al, 2015). Cystoblasts divide four times with incomplete cytokinesis, creating 16-cell cysts.…”

Section: Introductionmentioning

confidence: 99%

β-importins Tnpo-SR and Cadmus and the small GTPase Ran promote ovarian cyst formation inDrosophila

Williams

et al. 2021

Preprint

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Germ cells undergo mitotic expansion via incomplete cytokinesis, forming cysts of undifferentiated cells that remain interconnected prior to meiotic initiation, through mechanisms that are not well-defined. In somatic cells, an actomyosin contractile network controls cleavage furrow formation and abscission and is spatiotemporally regulated by Ras-related nuclear protein (Ran). Here, we identify Ran and β-importins as critical regulators of cyst development in the Drosophila ovary. Depletion of Ran or the β-importins Tnpo-SR and cadmus disrupts oocyte selection and results in egg chambers with variable numbers of germ cells, suggesting abnormal cyst development and cyst fragmentation. We demonstrate that Ran, Tnpo-SR, and Cadmus regulate key cellular processes during cyst formation, including cell cycle dynamics, fusome biogenesis, and ring canal stability, yet do so independently of mitotic spindle assembly. Further, Tnpo-SR and Cadmus control cyclin accumulation and suppress cytokinesis independent of Ran-GTP, suggesting that β-importins sequester protein cargos that normally promote the mitotic-to-meiotic transition. Our data demonstrates that Ran and β-importins are critical for germ cell cyst formation, a role that is likely conserved in other organisms.

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Src64 controls a novel actin network required for proper ring canal formation in the Drosophila male germline

Cited by 12 publications

References 52 publications

Partial Functional Diversification ofDrosophila melanogasterSeptin GenesSep2andSep5

Partial Functional Diversification ofDrosophila melanogasterSeptin GenesSep2andSep5

Actomyosin contraction during cellularization is regulated in part by Src64 control of Actin 5C protein levels

β-importins Tnpo-SR and Cadmus and the small GTPase Ran promote ovarian cyst formation inDrosophila

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