Evolution of insect proteomes: insights into synapse organization and synaptic vesicle life cycle

Yanay, Chava; Morpurgo, Noa; Linial, Michal

doi:10.1186/gb-2008-9-2-r27

Cited by 18 publications

(26 citation statements)

References 114 publications

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“…Hdc , actin , sesB , neurexinI , synaptotagmin1 ) ( Fig. 2b,c ) are involved in memory formation and olfaction in invertebrates via different mechanisms: dendrite pruning ( Hdc ), dendritic spine formation and elimination ( actin ), energy metabolism during neurotransmission ( sesB ), cell adhesion and signaling at the presynaptic terminal ( neurexinI ) and neurotransmitter release ( synaptotagmin1 ) 14 15 39 40 41 42 43 44 45 46 . The fact that learning induces long-term downregulation of these genes (as indicated by their increased expression when Dnmts are inhibited and by previous studies 12 13 14 ) suggests that memories may be stabilized, or normalized, by reducing synaptic remodeling.…”

Section: Discussionmentioning

confidence: 99%

Dnmts and Tet target memory-associated genes after appetitive olfactory training in honey bees

Biergans

Galizia

Reinhard

et al. 2015

Sci Rep

144

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DNA methylation and demethylation are epigenetic mechanisms involved in memory formation. In honey bees DNA methyltransferase (Dnmt) function is necessary for long-term memory to be stimulus specific (i.e. to reduce generalization). So far, however, it remains elusive which genes are targeted and what the time-course of DNA methylation is during memory formation. Here, we analyse how DNA methylation affects memory retention, gene expression, and differential methylation in stimulus-specific olfactory long-term memory formation. Out of 30 memory-associated genes investigated here, 9 were upregulated following Dnmt inhibition in trained bees. These included Dnmt3 suggesting a negative feedback loop for DNA methylation. Within these genes also the DNA methylation pattern changed during the first 24 hours after training. Interestingly, this was accompanied by sequential activation of the DNA methylation machinery (i.e. Dnmts and Tet). In sum, memory formation involves a temporally complex epigenetic regulation of memory-associated genes that facilitates stimulus specific long-term memory in the honey bee.

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Section: Discussionmentioning

confidence: 99%

Dnmts and Tet target memory-associated genes after appetitive olfactory training in honey bees

Biergans

Galizia

Reinhard

et al. 2015

Sci Rep

144

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“…The identification of the iTRAPs and their key role in ensuring the accurate retrieval of both sybII and synaptotagmin-1 during neuronal activity have revealed a hitherto unappreciated level of complexity in cargo selection and packing into SVs. The iTRAPS have appeared relatively late in evolution, with no close functionally-related homologs present in invertebrate species (Janz et al, 1998 ; Abraham et al, 2006 ; Yanay et al, 2008 ). This is in stark contrast to the monomeric adaptors, which are evolutionarily conserved from C. elegans and Drosophila through to higher order mammalian species.…”

Section: The Itraps—implications For Neuronal Functionmentioning

confidence: 99%

The iTRAPs: Guardians of Synaptic Vesicle Cargo Retrieval During Endocytosis

Gordon

Cousin

2016

Front. Synaptic Neurosci.

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The reformation of synaptic vesicles (SVs) during endocytosis is essential for the maintenance of neurotransmission in central nerve terminals. Newly formed SVs must be generated with the correct protein cargo in the correct stoichiometry to be functional for exocytosis. Classical clathrin adaptor protein complexes play a key role in sorting and clustering synaptic vesicle cargo in this regard. However it is becoming increasingly apparent that additional “fail-safe” mechanisms exist to ensure the accurate retrieval of essential cargo molecules. For example, the monomeric adaptor proteins AP180/CALM and stonin-2 are required for the efficient retrieval of synaptobrevin II (sybII) and synaptotagmin-1 respectively. Furthermore, recent studies have revealed that sybII and synaptotagmin-1 interact with other SV cargoes to ensure a high fidelity of retrieval. These cargoes are synaptophysin (for sybII) and SV2A (for synaptotagmin-1). In this review, we summarize current knowledge regarding the retrieval mechanisms for both sybII and synaptotagmin-1 during endocytosis. We also define and set criteria for a new functional group of SV molecules that facilitate the retrieval of their interaction partners. We have termed these molecules intrinsic trafficking partners (iTRAPs) and we discuss how the function of this group impacts on presynaptic performance in both health and disease.

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“…Drosophila melanogaster (dm) does not have orthologs of Bassoon or Piccolo, despite the fact that the majority of proteins that contribute to human presynaptic architecture are well conserved in insects [13]. Another coiled-coil protein-Bruchpilot-has been suggested to take on some of Bassoon's functions at the fly AZ along with the fly ortholog of RIM1, dmRIM (comparatively, a much larger protein showing regions of homology with mammalian Piccolo [14,15]).…”

mentioning

confidence: 99%

An evolutionarily conserved mechanism for presynaptic trapping

Fernandez

Torres

Zamorano

2010

Cell. Mol. Life Sci.

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Presynaptic differentiation takes place over three interrelated acts involving the biogenesis and trafficking of molecular complexes of active zone material, the "trapping" or stabilization of active zone sites, and the subsequent development of mature synapses. Although the identities of proteins involved with establishing presynaptic specializations have been increasingly delineated, the exact functional mechanisms by which the active zone is assembled remain poorly understood. Here, we discuss a theoretical model for how the trapping stage of presynaptic differentiation might occur in developing neurons. We suggest that subsets of active zone proteins containing polyglutamine domains undergo concentration-dependent prion-like conversions as they accumulate at the plasma membrane. This conversion might serve to aggregate the proteins into a singular structure, which is then able to recruit scaffolding agents necessary for regulated synaptic transmission. A brief informatics analysis in support of this 'Q' assembly hypothesis--across commonly used models of synaptogenesis--is presented.

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Evolution of insect proteomes: insights into synapse organization and synaptic vesicle life cycle

Cited by 18 publications

References 114 publications

Dnmts and Tet target memory-associated genes after appetitive olfactory training in honey bees

Dnmts and Tet target memory-associated genes after appetitive olfactory training in honey bees

The iTRAPs: Guardians of Synaptic Vesicle Cargo Retrieval During Endocytosis

An evolutionarily conserved mechanism for presynaptic trapping

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