The HSPG syndecan is a core organizer of cholinergic synapses

Zhou, Xin J.; Vachon, Camille; Cizeron, Mélissa; Romatif, Océane; Bülow, Hannes E.; Jospin, Maëlle; Bessereau, Jean-Louis

doi:10.1083/jcb.202011144

Cited by 24 publications

(36 citation statements)

References 93 publications

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“…There were no additional decrease in ACR-16::RFP and UNC-29::RFP in the lin-2;frm-3 double mutants (Figure 4B, D). Together, our results demonstrate that LIN-2 and FRM-3 act in the same genetic pathway regulating the synaptic abundance of ionotropic AChRs in body wall muscles, consistent with results reported in a recent study (Zhou et al, 2021) .…”

Section: Resultssupporting

confidence: 92%

CASK and FARP localize two classes of post-synaptic ACh receptors thereby promoting cholinergic transmission

Liu

Qian

et al. 2022

Preprint

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Synaptic proteins are immobilized at synapses via interactions with scaffolding proteins. Scaffolding proteins for glutamatergic and GABAergic synapses have been extensively studied; however, far less is known about how scaffolds shape the function of cholinergic synapses. Here we analyze the role of two C. elegans post-synaptic scaffolding proteins (LIN-2/CASK and FRM-3/FARP) at cholinergic neuromuscular junctions. Constitutive knockouts or muscle specific inactivation of lin-2 and frm-3 dramatically reduced spontaneous and evoked post-synaptic currents. These synaptic defects resulted from decreased abundance of post-synaptic ionotropic acetylcholine receptors (AChRs) and decreased presynaptic ACh release. Thus, our findings show that post-synaptic LIN-2/FRM-3 complexes coordinately control pre- and post-synaptic function, thereby promoting cholinergic synaptic transmission.

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Section: Resultssupporting

confidence: 92%

CASK and FARP localize two classes of post-synaptic ACh receptors thereby promoting cholinergic transmission

Liu

Qian

et al. 2022

Preprint

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“…The plasmids constructed for this study are described in Table S5. Plasmids used to create single copy insertion alleles by the miniMos method(Frøkjær-Jensen et al 2014) are described in previous studies (Zhou et al 2020, 2021) and the newly generated alleles are listed in Table S5. All constructs were verified by Sanger sequencing from GATC Company.…”

Section: Methodsmentioning

confidence: 99%

“…The plasmids constructed for this study are described in Table S5. Plasmids used to create single copy insertion alleles by the miniMos method(Frøkjaer-Jensen et al 2014) are described in previous studies (Zhou et al 2020(Zhou et al , 2021 and the newly generated alleles are listed in Table S5. or TOMM20 fused to fluorescent proteins, 50 ng/μl pCFJ601 (Mos1 transposase), 10 ng/μl pMA122 (negative selective marker Phsp16.2::peel-1), and 2.5 ng/μl pCFJ90 (Pmyo-2::mCherry).…”

Section: Plasmids and Generation Of Single-copy Insertion Allelesmentioning

confidence: 99%

DAF-2/insulin IGF-1 receptor regulates motility during ageing by integrating opposite signaling from muscle and neuronal tissues

Roy

Molin

Solyga

et al. 2021

Preprint

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During ageing, preservation of locomotion is generally considered an indicator of sustained good health, in elderlies and in animal models. In C. elegans, mutants of the insulin receptor DAF-2 represent a paradigm of healthy ageing, as their increased lifespan is accompanied by a delay in age-related loss of mobility. However, these animals are less mobile than wild-type animals in early adulthood. Here we investigated the DAF-2-dependent relationship between longevity and mobility using an auxin-inducible degron to trigger tissue-specific degradation of endogenous DAF-2. As previously reported, inactivation of DAF-2 in neurons or intestine was sufficient to extend the lifespan of worms, whereas depletion in epidermis, germline or muscle was not. However, neither intestinal nor neuronal depletion of DAF-2 prevented the age-related loss of mobility. In 1-day-old adults, DAF-2 depletion in neurons reduced mobility, while muscle depletion had no effect. By contrast, DAF-2 depletion in the muscle of middle-age animals improved their mobility. The combination of neuronal and muscle effects thus mimics the global locomotor phenotype of daf-2 mutants. Yet, we observed that neuronal or muscle DAF-2 depletion both preserved the mitochondria network in ageing muscle. Overall, these results show that the mobility pattern of daf-2 mutants is determined by the sequential and opposing impact of neurons and muscle tissues and can be dissociated from the regulation of the lifespan. This work also provides the characterization of a versatile tool to analyze the tissue-specific contribution of insulin-like signaling in integrated phenotypes at the whole organism level.

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“…In addition, the mechanism allowing the dual function of MADD-4S at cholinergic versus GABAergic synapses remains to be understood, but probably involves dimerization with the long isoform MADD-4L. Finally, both MADD-4 isoforms promote the synaptic localization of the heparan sulfate glycoprotein syndecan/SDN-1, a key-component of cholinergic NMJs ( Zhou et al, 2021 ). The specific role of the TSP-1 domains in these various molecular interactions remains to be determined.…”

Section: Key Synaptic Roles For the Tsp-1 Ccp And Cub Structural Doma...mentioning

confidence: 99%

Synapse Formation and Function Across Species: Ancient Roles for CCP, CUB, and TSP-1 Structural Domains

et al. 2022

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The appearance of synapses was a crucial step in the creation of the variety of nervous systems that are found in the animal kingdom. With increased complexity of the organisms came a greater number of synaptic proteins. In this review we describe synaptic proteins that contain the structural domains CUB, CCP, or TSP-1. These domains are found in invertebrates and vertebrates, and CUB and CCP domains were initially described in proteins belonging to the complement system of innate immunity. Interestingly, they are found in synapses of the nematode C. elegans, which does not have a complement system, suggesting an ancient function. Comparison of the roles of CUB-, CCP-, and TSP-1 containing synaptic proteins in various species shows that in more complex nervous systems, these structural domains are combined with other domains and that there is partial conservation of their function. These three domains are thus basic building blocks of the synaptic architecture. Further studies of structural domains characteristic of synaptic proteins in invertebrates such as C. elegans and comparison of their role in mammals will help identify other conserved synaptic molecular building blocks. Furthermore, this type of functional comparison across species will also identify structural domains added during evolution in correlation with increased complexity, shedding light on mechanisms underlying cognition and brain diseases.

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The HSPG syndecan is a core organizer of cholinergic synapses

Cited by 24 publications

References 93 publications

CASK and FARP localize two classes of post-synaptic ACh receptors thereby promoting cholinergic transmission

CASK and FARP localize two classes of post-synaptic ACh receptors thereby promoting cholinergic transmission

DAF-2/insulin IGF-1 receptor regulates motility during ageing by integrating opposite signaling from muscle and neuronal tissues

Synapse Formation and Function Across Species: Ancient Roles for CCP, CUB, and TSP-1 Structural Domains

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