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A Post-Synaptic Scaffold at the Origin of the Animal Kingdom
Open accessAbstract
BACKGROUND: The evolution of complex sub-cellular structures such as the synapse requires the assembly of multiple proteins, each conferring added functionality to the integrated structure. Tracking the early evolution of synapses has not been possible without genomic information from the earliest branching animals. As the closest extant relatives to the Eumetazoa, Porifera (sponges) represent a pivotal group for understanding the evolution of nervous systems, because sponges lack neurons with clearly recognizable synapses, in contrast to eumetazoan animals. METHODOLOGY/PRINCIPAL FINDINGS: We show that the genome of the demosponge Amphimedon queenslandica possesses a nearly complete set of post-synaptic protein homologs whose conserved interaction motifs suggest assembly into a complex structure. In the critical synaptic scaffold gene, dlg, residues that make hydrogen bonds and van der Waals interactions with the PDZ ligand are 100% conserved between sponge and human, as is the motif organization of the scaffolds. Expression in Amphimedon of multiple post-synaptic gene homologs in larval flask cells further supports the existence of an assembled structure. Among the few post-synaptic genes absent from Amphimedon, but present in Eumetazoa, are receptor genes including the entire ionotropic glutamate receptor family. CONCLUSIONS/SIGNIFICANCE: Highly conserved protein interaction motifs and co-expression in sponges of multiple proteins whose homologs interact in eumetazoan synapses indicate that a complex protein scaffold was present at the origin of animals, perhaps predating nervous systems. A relatively small number of crucial innovations to this pre-existing structure may represent the founding changes that led to a post-synaptic element.
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“An “ancestral complexity” of cnidarians in terms of synaptic proteins is therefore apparent [28,32].”
From Back to the Basics: Cnidarians Start to Fire (2017) · cites this paper as [28]
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“most of the structural components of the post-synaptic density (PSD) are present in the sponge Amphimedon [22,28], and some have clear homologs in choanoflagellates and other unicellular holozoans [29,30]”
From Back to the Basics: Cnidarians Start to Fire (2017) · cites this paper as [28]
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Metadata
- Authors
- Sakarya, O., Armstrong, K. A., Adamska, M., Adamski, M., Wang, I.-F., Tidor, B., Degnan, B. M., Oakley, T. H., & Kosik, K. S.
- Affiliations
- University of California, Santa Barbara (US)
- MIT Computer Science and Artificial Intelligence Laboratory (US)
- The University of Queensland (AU)
- Corresponding author
- Kosik, Kenneth S.
- ORCID
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2007-06-06
- Volume
- 2
- Issue
- 6
- Pages
- e506
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC1876816
- OpenAlex
- W2079236594
- Cited by
- 291
- References
- 52
- Citations by year
- 2026: 2 · 2025: 5 · 2024: 6 · 2023: 2 · 2022: 3 · 2021: 8 · 2020: 13 · 2019: 15 · 2018: 8 · 2017: 16 · 2016: 21 · 2015: 28 · 2014: 20 · 2013: 12 · 2012: 18
- FWCI
- 24.18
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
- Funders
- U.S. Department of Energy
- Joint Genome Institute
- Topics
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- sponge genome, Amphimedon queenslandica, PDZ domain, protein interaction motifs, ionotropic glutamate receptors, Eumetazoa, protein complex formation
- MeSH terms
- Animals, Humans, Nerve Tissue Proteins, Porifera, Synapses, Genome, Evolution, Molecular
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