Microtubule organization in presynaptic boutons relies on the formin DAAM

Migh, Ede; Götz, Torsten; Földi, István; Szikora, Szilárd; Gombos, Rita; Darula, Zsuzsanna; Medzihradszky, Katalin F.; Maléth, József; Hegyi, Péter; Sigrist, Stephan J.; Mihály, József

doi:10.1242/dev.158519

Cited by 24 publications

(22 citation statements)

References 61 publications

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“…For proteomic analysis, the gel was stained with Coomassie Brilliant Blue then destained with the mix of 40% ethanol and 10% acetic acid. The 50-65 kDa region of the soluble and insoluble sample were subjected to in-gel digestion as described in Migh et al [48]. Briefly, protein disulfide bridges were reduced with dithiothreitol (30 min, 56°C) then the resulting sulfhydryl groups were capped using iodoacetamide (30 min, RT, in the dark) following digestion with sequencing grade side chain protected trypsin (4h, 37°C).…”

Section: Methodsmentioning

confidence: 99%

Sperm-Leucylaminopeptidases are required for male fertility as structural components of mitochondrial paracrystalline material in Drosophila melanogaster sperm

et al. 2019

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Drosophila melanogaster sperm reach an extraordinary long size, 1.8 mm, by the end of spermatogenesis. The mitochondrial derivatives run along the entire flagellum and provide structural rigidity for flagellar movement, but its precise function and organization is incompletely understood. The two mitochondrial derivatives differentiate and by the end of spermatogenesis the minor one reduces its size and the major one accumulates paracrystalline material inside it. The molecular constituents and precise function of the paracrystalline material have not yet been revealed. Here we purified the paracrystalline material from mature sperm and identified by mass spectrometry Sperm-Leucylaminopeptidase (S-Lap) family members as important constituents of it. To study the function of S-Lap proteins we show the characterization of classical mutants and RNAi lines affecting of the S-Lap genes and the analysis of their mutant phenotypes. We show that the male sterile phenotype of the S-Lap mutants is caused by defects in paracrystalline material accumulation and abnormal structure of the elongated major mitochondrial derivatives. Our work shows that S-Lap proteins localize and accumulate in the paracrystalline material of the major mitochondrial derivative. Therefore, we propose that S-Lap proteins are important constituents of the paracrystalline material of Drosophila melanogaster sperm.

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Section: Methodsmentioning

confidence: 99%

Sperm-Leucylaminopeptidases are required for male fertility as structural components of mitochondrial paracrystalline material in Drosophila melanogaster sperm

et al. 2019

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“…These findings suggest a model where increased stabilization of MTs is associated with increased NMJ expansion. Additional factors that are associated with MT stability, such as the formins Diaphanous (Pawson, Eaton, & Davis, ) and DAAM (Bartolini & Gundersen, ; Migh et al, ), have also been found to promote NMJ expansion.…”

Section: Introductionmentioning

confidence: 99%

dTACC restricts bouton addition and regulates microtubule organization at the Drosophila neuromuscular junction

et al. 2019

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Regulation of the synaptic cytoskeleton is essential to proper neuronal development and wiring. Perturbations in neuronal microtubules (MTs) are associated with numerous pathologies, yet it remains unclear how changes in MTs may be coupled to synapse morphogenesis. Studies have identified many MT regulators that promote synapse growth. However, less is known about the factors that restrict growth, despite the potential links of synaptic overgrowth to severe neurological conditions. Here, we report that dTACC, which is implicated in MT assembly and stability, prevents synapse overgrowth at the Drosophila neuromuscular junction by restricting addition of new boutons throughout larval development. dTACC localizes to the axonal MT lattice and is required to maintain tubulin levels and the integrity of higher‐order MT structures in motor axon terminals. While previous reports have demonstrated the roles of MT‐stabilizing proteins in promoting synapse growth, our findings suggest that in certain contexts, MT stabilization may correlate with restricted growth.

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“…Few studies, however, have explored these possibilities using modern imaging approaches. Presynaptic MAP-associated stable MT loops, EB1-labeled dynamic pioneer MTs, and DAAM-dependent stable MT regulation of SV release and AZ morphology have been described at the Drosophila neuromuscular junction (19)(20)(21).…”

Section: Introductionmentioning

confidence: 99%

Activity-dependent nucleation of dynamic microtubules at presynaptic boutons is required for neurotransmission

Kumar

Blockus

et al. 2019

Preprint

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Highlights:• Excitatory boutons are hotspots for neuronal activity-induced γ-tubulin dependent MT nucleation• The augmin complex is required for the correct polarity of presynaptic de novo nucleated MTs • Presynaptic MT nucleation promotes SV motility and exocytosis at sites of release In Brief: Our results demonstrate that excitatory en passant boutons are hotspots for neuronal activity-induced γ-tubulin-and augmin-dependent oriented MT nucleation, and that the resulting presynaptic de novo nucleated MTs promote inter-bouton SV motility which is rate-limiting for neurotransmitter release. 2 SUMMARY Control of microtubule (MT) dynamics is critical for neuronal function. Whether MT nucleation is regulated at presynaptic boutons and influences overall presynaptic activity remains unknown. By visualizing MT dynamics at individual excitatory en passant boutons in axons of hippocampal neurons we found that MTs preferentially grow from presynaptic boutons as a result of g-tubulin and augmin-dependent nucleation. MT nucleation at boutons is promoted by neuronal activity, functionally coupled to synaptic vesicle (SV) transport, and required for neurotransmission. Hence, en passant boutons act as hotspots for activitydependent MT nucleation, which is required for neurotransmission by providing the tracks for a rate-limiting supply of SVs to sites of neurotransmitter release.

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Microtubule organization in presynaptic boutons relies on the formin DAAM

Cited by 24 publications

References 61 publications

Sperm-Leucylaminopeptidases are required for male fertility as structural components of mitochondrial paracrystalline material in Drosophila melanogaster sperm

Sperm-Leucylaminopeptidases are required for male fertility as structural components of mitochondrial paracrystalline material in Drosophila melanogaster sperm

dTACC restricts bouton addition and regulates microtubule organization at the Drosophila neuromuscular junction

Activity-dependent nucleation of dynamic microtubules at presynaptic boutons is required for neurotransmission

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