Aging <i>Drosophila melanogaster</i> display altered pre‐ and postsynaptic ultrastructure at adult neuromuscular junctions

Wagner, Nicole; Laugks, Ulrike; Heckmann, Manfred; Asan, Esther; Neuser, Kirsa

doi:10.1002/cne.23798

Cited by 21 publications

(42 citation statements)

References 74 publications

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“…Similar results were observed at neuromuscular junctions of aged fruit flies [46]. The authors found that, with progression of age, the number of BRP-labeled spots, which indicate active zones, per bouton increased up to an age of 42 days and that this increase is accompanied by an increase in bouton volume.…”

Section: Discussionsupporting

confidence: 76%

Age-associated increase of the active zone protein Bruchpilot within the honeybee mushroom body

et al. 2017

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In honeybees, age-associated structural modifications can be observed in the mushroom bodies. Prominent examples are the synaptic complexes (microglomeruli, MG) in the mushroom body calyces, which were shown to alter their size and density with age. It is not known whether the amount of intracellular synaptic proteins in the MG is altered as well. The presynaptic protein Bruchpilot (BRP) is localized at active zones and is involved in regulating the probability of neurotransmitter release in the fruit fly, Drosophila melanogaster. Here, we explored the localization of the honeybee BRP (Apis mellifera BRP, AmBRP) in the bee brain and examined age-related changes in the AmBRP abundance in the central bee brain and in microglomeruli of the mushroom body calyces. We report predominant AmBRP localization near the membrane of presynaptic boutons within the mushroom body MG. The relative amount of AmBRP was increased in the central brain of two-week old bees whereas the amount of Synapsin, another presynaptic protein involved in the regulation of neurotransmitter release, shows an increase during the first two weeks followed by a decrease. In addition, we demonstrate an age-associated modulation of AmBRP located near the membrane of presynaptic boutons within MG located in mushroom body calyces where sensory input is conveyed to mushroom body intrinsic neurons.We discuss that the observed age-associated AmBRP modulation might be related to maturation processes or to homeostatic mechanisms that might help to maintain synaptic functionality in old animals.

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Section: Discussionsupporting

confidence: 76%

Age-associated increase of the active zone protein Bruchpilot within the honeybee mushroom body

et al. 2017

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“…The intensity of Dlg immunolabeling was not affected by aging (see also Beramendi et al, 2007) or dormancy (Figures 4D,E, Supplementary Figure S1C). The synaptic boutons as measured in HRP labeled specimens increase in size with age and often merged under normal conditions (see also Beramendi et al, 2007; Wagner et al, 2015), but not under diapause conditions (Figure 4G). The number and length of axon branches of the NMJ were not affected by aging or diapause (Figures 4H,I), although we discovered that the branch number was higher in flies sampled just after eclosion, and that this number remained in flies taken to diapause conditions after eclosion (Figure 4H).…”

Section: Resultsmentioning

confidence: 74%

“…We selected the second and third ventral longitudinal muscle (VLM) of the abdominal body wall for analysis since this has been investigated during aging previously (Hebbar et al, 2006; Wagner et al, 2015). NMJs from flies exposed to 8 weeks of dormancy were compared to ones from newly hatched flies and flies kept at 25°C and 12L:12D for 1 or 8 weeks after immunolabeling with antisera to HRP, discs large ( Dlg ) and the synapse protein bruchpilot ( Brp ).…”

Section: Resultsmentioning

confidence: 99%

“…However, in contrast to mammals, the brain of Drosophila does not display obvious histological signs of neurodegeneration or apoptosis with increasing age, unless genetically manipulated or exposed to oxidative stress (see Chan and Bonini, 2000; White et al, 2010; Mohan et al, 2014). Only more subtle signs of aging have been revealed in the fly: central neurons do display some ultrastructural changes (Martín-Peña et al, 2006) and certain structural and molecular features were shown to be affected in axon terminations of motor neurons (Beramendi et al, 2007; Wagner et al, 2015). On the other hand, many behaviors, including learning and memory, are known to deteriorate over the lifespan (Grotewiel et al, 2005; Tonoki and Davis, 2012; Yamazaki et al, 2014) suggesting that aging induces deleterious effects on neurons and neuronal circuits in the Drosophila brain.…”

Section: Introductionmentioning

confidence: 99%

“…We recorded rhythmic activity and sleep patterns, complex walking behavior, and simple reflex climbing behavior (negative geotaxis), all known to change with age (Gargano et al, 2005; Koh et al, 2006; Umezaki et al, 2012; Ismail et al, 2015). In the peripheral nervous system it has been shown that the morphology of the axon terminations of motor neurons changes with age (Beramendi et al, 2007; Wagner et al, 2015). Hence, we analyzed expression of proteins in and morphology of the axon terminations of abdominal motor neurons in our experimental flies.…”

Section: Introductionmentioning

confidence: 99%

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Behavioral Senescence and Aging-Related Changes in Motor Neurons and Brain Neuromodulator Levels Are Ameliorated by Lifespan-Extending Reproductive Dormancy in Drosophila

Liao

Broughton

Nässel

2017

Front. Cell. Neurosci.

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The lifespan of Drosophila melanogaster can be extended substantially by inducing reproductive dormancy (also known as diapause) by lowered temperature and short days. This increase of longevity is accompanied by lowered metabolism and increased stress tolerance. We ask here whether behavioral senescence is ameliorated during adult dormancy. To study this we kept flies for seven or more weeks in normal rearing conditions or in diapause conditions and compared to 1-week-old flies in different behavioral assays of sleep, negative geotaxis and exploratory walking. We found that the senescence of geotaxis and locomotor behavior seen under normal rearing conditions was negligible in flies kept in dormancy. The normal senescence of rhythmic activity and sleep patterns during the daytime was also reduced by adult dormancy. Investigating the morphology of specific neuromuscular junctions (NMJs), we found that changes normally seen with aging do not take place in dormant flies. To monitor age-associated changes in neuronal circuits regulating activity rhythms, sleep and walking behavior we applied antisera to tyrosine hydroxylase (TH), serotonin and several neuropeptides to examine changes in expression levels and neuron morphology. In most neuron types the levels of stored neuromodulators decreased during normal aging, but not in diapause treated flies. No signs of neurodegeneration were seen in either condition. Our data suggest that age-related changes in motor neurons could be the cause of part of the behavioral senescence and that this is ameliorated by reproductive diapause. Earlier studies established a link between age-associated decreases in neuromodulator levels and behavioral decline that could be rescued by overexpression of neuromodulator. Thus, it is likely that the retained levels of neuromodulators in dormant flies alleviate behavioral senescence.

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Ultrastructural comparison of theDrosophilalarval and adult ventral abdominal neuromuscular junction

Wagner

2017

Journal of Morphology

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Drosophila melanogaster has recently emerged as model system for studying synaptic transmission and plasticity during adulthood, aging and neurodegeneration. However, still little is known about the basic neuronal mechanisms of synaptic function in the adult fly. Per se, adult Drosophila neuromuscular junctions should be highly suited for studying these aspects as they allow for genetic manipulations in combination with ultrastructural and electrophysiological analyses. Although different neuromuscular junctions of the adult fly have been described during the last years, a direct ultrastructural comparison with their larval counterpart is lacking. The present study was designed to close this gap by providing a detailed ultrastructural comparison of the larval and the adult neuromuscular junction of the ventrolongitudinal muscle. Assessment of several parameters revealed similarities but also major differences in the ultrastructural organisation of the two model neuromuscular junctions. While basic morphological parameters are retained from the larval into the adult stage, the analysis discovered major differences of potential functional relevance in the adult: The electron-dense membrane apposition of the presynaptic and postsynaptic membrane is shorter, the subsynaptic reticulum is less elaborated and the number of synaptic vesicles at a certain distance of the presynaptic membrane is higher.

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Aging Drosophila melanogaster display altered pre‐ and postsynaptic ultrastructure at adult neuromuscular junctions

Cited by 21 publications

References 74 publications

Age-associated increase of the active zone protein Bruchpilot within the honeybee mushroom body

Age-associated increase of the active zone protein Bruchpilot within the honeybee mushroom body

Behavioral Senescence and Aging-Related Changes in Motor Neurons and Brain Neuromodulator Levels Are Ameliorated by Lifespan-Extending Reproductive Dormancy in Drosophila

Ultrastructural comparison of theDrosophilalarval and adult ventral abdominal neuromuscular junction

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