Hierarchical assembly of presynaptic components in defined C. elegans synapses
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The presynaptic regions of axons accumulate synaptic vesicles, active zone proteins and periactive zone proteins. However, the rules for orderly recruitment of presynaptic components are not well understood. We systematically examined molecular mechanisms of presynaptic development in egg-laying synapses of Caenorhabditis elegans, demonstrating that two scaffolding molecules, SYD-1 and SYD-2, have key roles in presynaptic assembly. SYD-2 (liprin-alpha) was previously shown to regulate the size and the shape of active zones. We now show that in syd-1 and syd-2 mutants, synaptic vesicles and numerous other presynaptic proteins fail to accumulate at presynaptic sites. SYD-1 and SYD-2 function cell-autonomously at presynaptic terminals, downstream of synaptic specificity molecule SYG-1. SYD-1 is likely to act upstream of SYD-2 to positively regulate its synaptic assembly activity. These data imply a hierarchical organization of presynaptic assembly, in which transmembrane specificity molecules initiate synaptogenesis by recruiting a few key scaffolding proteins, which in turn assemble other presynaptic components.
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Proteins related to C. elegans SYD-1 are important for the assembly of active zones in invertebrates.
“In addition to these five core active zone proteins, piccolo and bassoon (two large homologous proteins) are associated in vertebrates with active zones (tom Dieck et al., 1998; Wang et al., 1999; Fenster et al., 2000; Limbach et al., 2011), and proteins related to C. elegans SYD-1 are important for the assembly of active zones in invertebrates (Hallam et al., 2002; Patel et al., 2006; Owald et al”
From The Presynaptic Active Zone (2012) · cites this paper as Patel et al., 2006
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References 50 · Cited by 178
- Authors
- Patel, M. R., Lehrman, E. K., Poon, V. Y., Crump, J. G., Zhen, M., Bargmann, C. I., & Shen, K.
- Affiliations
- Stanford University (US)
- University of Southern California (US)
- University of Toronto (CA)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Shen, Kang
- Venue
- Nature Neuroscience
- Published
- 2006-11-19
- Volume
- 9
- Issue
- 12
- Pages
- 1488-1498
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC3917495
- OpenAlex
- W2165554927
- Cited by
- 178
- References
- 50
- Citations by year
- 2026: 2 · 2025: 5 · 2024: 4 · 2023: 7 · 2022: 6 · 2021: 7 · 2020: 10 · 2019: 7 · 2018: 13 · 2017: 6 · 2016: 12 · 2015: 12 · 2014: 8 · 2013: 16 · 2012: 8
- FWCI
- 4.05
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (R01NS048392)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Keywords
- Caenorhabditis elegans, Liprin-α, synaptic specificity, synaptic vesicles, active zone proteins, scaffold proteins, synaptogenesis, hierarchical assembly, presynaptic terminals
- MeSH terms
- Animals, Cytoskeleton, Immunoglobulins, Motor Neurons, Mutation, Nerve Tissue Proteins, Phosphoproteins, Caenorhabditis elegans, Presynaptic Terminals, Caenorhabditis elegans Proteins, Intercellular Signaling Peptides and Proteins
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