Filopodia-like Actin Cables Position Nuclei in Association with Perinuclear Actin in Drosophila Nurse Cells

Huelsmann, Sven; Ylänne, Jari; Brown, Nicholas H.

doi:10.1016/j.devcel.2013.08.014

Cited by 72 publications

(125 citation statements)

References 56 publications

(43 reference statements)

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“…This remote action of E-Cad is somewhat reminiscent of another E-Cad function during oogenesis: E-Cad clusters at the nurse cells' PM control the orientation of the filopodia-like actin cables that position nuclei during later stages of oogenesis. In a similar fashion, these E-Cad clusters are interspersed between the membrane-originating tips of filopodia (51).…”

Section: Discussionmentioning

confidence: 85%

Drosophila E-cadherin is required for the maintenance of ring canals anchoring to mechanically withstand tissue growth

Loyer

Kolotuev

Pinot

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Intercellular bridges called "ring canals" (RCs) resulting from incomplete cytokinesis play an essential role in intercellular communication in somatic and germinal tissues. During Drosophila oogenesis, RCs connect the maturing oocyte to nurse cells supporting its growth. Despite numerous genetic screens aimed at identifying genes involved in RC biogenesis and maturation, how RCs anchor to the plasma membrane (PM) throughout development remains unexplained. In this study, we report that the clathrin adaptor protein 1 (AP-1) complex, although dispensable for the biogenesis of RCs, is required for the maintenance of the anchorage of RCs to the PM to withstand the increased membrane tension associated with the exponential tissue growth at the onset of vitellogenesis. Here we unravel the mechanisms by which AP-1 enables the maintenance of RCs' anchoring to the PM during size expansion. We show that AP-1 regulates the localization of the intercellular adhesion molecule E-cadherin and that loss of AP-1 causes the disappearance of the E-cadherin-containing adhesive clusters surrounding the RCs. E-cadherin itself is shown to be required for the maintenance of the RCs' anchorage, a function previously unrecognized because of functional compensation by N-cadherin. Scanning block-face EM combined with transmission EM analyses reveals the presence of interdigitated, actin-and Moesin-positive, microvilli-like structures wrapping the RCs. Thus, by modulating E-cadherin trafficking, we show that the sustained E-cadherin-dependent adhesion organizes the microvilli meshwork and ensures the proper attachment of RCs to the PM, thereby counteracting the increasing membrane tension induced by exponential tissue growth.

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Section: Discussionmentioning

confidence: 85%

Drosophila E-cadherin is required for the maintenance of ring canals anchoring to mechanically withstand tissue growth

Loyer

Kolotuev

Pinot

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…In Drosophila, overall filamin protein structure its actin-crosslinking function are conserved in Cheerio. It plays a key role in ring canal formation during oogenesis (Sokol and Cooley, 1999) and is involved in the positioning of nuclei in ovarian nurse cells (Huelsmann et al, 2013), but the role of Cheerio in muscles had remained elusive.…”

Section: Discussionmentioning

confidence: 99%

“…7B). We also tested whether CryAB colocalized with cher-240 in sarcomeres using the cher CPTI0847 line, which carries a Venus insertion that does not affect cheerio function (Huelsmann et al, 2013). We observed that Venus-tagged Cheerio colocalized at the level of Z-bands with CryAB (Fig.…”

Section: Cryab Interacts With Cheerio In Larval Musclesmentioning

confidence: 99%

“…Cheerio, which makes a link between perinuclear actin and cytoplasmic actin cables, is involved in nuclei positioning in Drosophila nurse cells (Huelsmann et al, 2013). It is also well known that in vertebrate muscles the Cheerio ortholog Filamin C is associated with Z-bands and when mutated leads to myofibrilar myopathies (Goldfarb and Dalakas, 2009).…”

Section: Cryab Is Required For Z-band Patterning and Muscle Integritymentioning

confidence: 99%

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Drosophila small heat shock protein CryAB ensures structural integrity of developing muscles, and proper muscle and heart performance

et al. 2015

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Molecular chaperones, such as the small heat shock proteins (sHsps), maintain normal cellular function by controlling protein homeostasis in stress conditions. However, sHsps are not only activated in response to environmental insults, but also exert developmental and tissuespecific functions that are much less known. Here, we show that during normal development the Drosophila sHsp CryAB [L(2)efl] is specifically expressed in larval body wall muscles and accumulates at the level of Z-bands and around myonuclei. CryAB features a conserved actin-binding domain and, when attenuated, leads to clustering of myonuclei and an altered pattern of sarcomeric actin and the Z-band-associated actin crosslinker Cheerio (filamin). Our data suggest that CryAB and Cheerio form a complex essential for muscle integrity: CryAB colocalizes with Cheerio and, as revealed by mass spectrometry and co-immunoprecipitation experiments, binds to Cheerio, and the muscle-specific attenuation of cheerio leads to CryAB-like sarcomeric phenotypes. Furthermore, muscle-targeted expression of CryAB R120G , which carries a mutation associated with desmin-related myopathy (DRM), results in an altered sarcomeric actin pattern, in affected myofibrillar integrity and in Z-band breaks, leading to reduced muscle performance and to marked cardiac arrhythmia. Taken together, we demonstrate that CryAB ensures myofibrillar integrity in Drosophila muscles during development and propose that it does so by interacting with the actin crosslinker Cheerio. The evidence that a DRM-causing mutation affects CryAB muscle function and leads to DRM-like phenotypes in the fly reveals a conserved stress-independent role of CryAB in maintaining muscle cell cytoarchitecture.

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“…The incomplete transfer of nurse cell cytoplasm and short egg phenotype resembles that of other 'dumpless' mutants, and suggests that mito-nuclear incompatibility also impairs germline functions (Bilder and Haigo, 2012;Frydman and Spradling, 2001;Mahajan-Miklos and Cooley, 1994). Rapid transfer of nurse cell cytoplasm depends on actin polymerization and contraction, and is sensitive to ATP/ADP ratio, perhaps explaining why it is sensitive to mitochondrial dysfunction (Huelsmann et al, 2013). A recent report indicates that compromised function of the muscular ovariole sheath can also affect nurse cell dumping and results in short eggs with reduced ooplasm (Andersen and Horne-Badovinac, 2016).…”

Section: Discussionmentioning

confidence: 99%

Incompatibility between mitochondrial and nuclear genomes during oogenesis results in ovarian failure and embryonic lethality

2017

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Mitochondrial dysfunction can cause female infertility. An important unresolved issue is the extent to which incompatibility between mitochondrial and nuclear genomes contributes to female infertility. It has previously been shown that a mitochondrial haplotype from D. simulans (simw 501) is incompatible with a nuclear genome from the D. melanogaster strain Oregon-R (OreR), resulting in impaired development, which was enhanced at higher temperature. This mitonuclear incompatibility is between alleles of the nuclear-encoded mitochondrial tyrosyl-tRNA synthetase (Aatm) and the mitochondrialencoded tyrosyl-tRNA that it aminoacylates. Here, we show that this mito-nuclear incompatibility causes a severe temperature-sensitive female infertility. The OreR nuclear genome contributed to death of ovarian germline stem cells and reduced egg production, which was further enhanced by the incompatibility with simw 501 mitochondria. Mito-nuclear incompatibility also resulted in aberrant egg morphology and a maternal-effect on embryonic chromosome segregation and survival, which was completely dependent on the temperature and mito-nuclear genotype of the mother. Our findings show that maternal mito-nuclear incompatibility during Drosophila oogenesis has severe consequences for egg production and embryonic survival, with important broader relevance to human female infertility and mitochondrial replacement therapy.

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Filopodia-like Actin Cables Position Nuclei in Association with Perinuclear Actin in Drosophila Nurse Cells

Cited by 72 publications

References 56 publications

Drosophila E-cadherin is required for the maintenance of ring canals anchoring to mechanically withstand tissue growth

Drosophila E-cadherin is required for the maintenance of ring canals anchoring to mechanically withstand tissue growth

Drosophila small heat shock protein CryAB ensures structural integrity of developing muscles, and proper muscle and heart performance

Incompatibility between mitochondrial and nuclear genomes during oogenesis results in ovarian failure and embryonic lethality

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