Neurite Sprouting and Synapse Deterioration in the Aging Caenorhabditis elegans Nervous System
Open accessAbstract
Caenorhabditis elegans is a powerful model for analysis of the conserved mechanisms that modulate healthy aging. In the aging nematode nervous system, neuronal death and/or detectable loss of processes are not readily apparent, but because dendrite restructuring and loss of synaptic integrity are hypothesized to contribute to human brain decline and dysfunction, we combined fluorescence microscopy and electron microscopy (EM) to screen at high resolution for nervous system changes. We report two major components of morphological change in the aging C. elegans nervous system: (1) accumulation of novel outgrowths from specific neurons, and (2) physical decline in synaptic integrity. Novel outgrowth phenotypes, including branching from the main dendrite or new growth from somata, appear at a high frequency in some aging neurons, but not all. Mitochondria are often associated with age-associated branch sites. Lowered insulin signaling confers some maintenance of ALM and PLM neuron structural integrity into old age, and both DAF-16/FOXO and heat shock factor transcription factor HSF-1 exert neuroprotective functions. hsf-1 can act cell autonomously in this capacity. EM evaluation in synapse-rich regions reveals a striking decline in synaptic vesicle numbers and a diminution of presynaptic density size. Interestingly, old animals that maintain locomotory prowess exhibit less synaptic decline than same-age decrepit animals, suggesting that synaptic integrity correlates with locomotory healthspan. Our data reveal similarities between the aging C. elegans nervous system and mammalian brain, suggesting conserved neuronal responses to age. Dissection of neuronal aging mechanisms in C. elegans may thus influence the development of brain healthspan-extending therapies.
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Neurite outgrowth and synapse formation in C. elegans continue through larval development, the L4 stage, and adulthood, and ectopic neurite sprouting continues with aging.
“Outgrowth of neurites and establishment of synapses in C. elegans occurs throughout larval development and continues through the L4 larval stage and into adulthood, and ectopic neurite sprouting continues as the nervous system ages45,46.”
From Whole-animal connectomes of both Caenorhabditis elegans sexes (2019) · cites this paper as [46]
The Results section, “C. elegans touch receptor neurons exhibit new neurite outgrowth with age” (page unavailable), reports new branches that become more frequent in aging adults, supporting the ectopic-sprouting portion. Our copy does not establish that neurite outgrowth and synapse formation continue throughout larval development, through L4, and into adulthood; its aging-synapse findings concern deterioration rather than new synapse formation. (LLM, conf=0.86)
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- Authors
- Toth, M. L., Melentijevic, I., Shah, L., Bhatia, A., Lu, K., Talwar, A., Naji, H., Ibanez-Ventoso, C., Ghose, P., Jevince, A., Xue, J., Herndon, L. A., Bhanot, G., Rongo, C., Hall, D. H., & Driscoll, M.
- Affiliations
- Rutgers, The State University of New Jersey (US)
- Albert Einstein College of Medicine (US)
- Corresponding author
- Driscoll, M.
- Venue
- Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2012-06-27
- Volume
- 32
- Issue
- 26
- Pages
- 8778-8790
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3427745
- OpenAlex
- W2058446462
- Cited by
- 205
- References
- 68
- Citations by year
- 2026: 10 · 2025: 14 · 2024: 29 · 2023: 9 · 2022: 14 · 2021: 13 · 2020: 15 · 2019: 15 · 2018: 12 · 2017: 15 · 2016: 17 · 2015: 11 · 2014: 16 · 2013: 10 · 2012: 4
- FWCI
- 4.25
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Neuroscience (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Rutgers University Community Repository (Rutgers University) (submittedVersion)
- ANU Open Research (Australian National University) (submittedVersion)
- Funders
- New Jersey Commission on Spinal Cord Research
- National Institutes of Health (HD071593, R24OD010943)
- Intellectual and Developmental Disabilities Research Center
- National Institute on Aging (R01AG024882, AG024882, R21AG041498)
- National Institute of General Medical Sciences (R01GM101972, T32GM008339)
- National Institute of Neurological Disorders and Stroke (R01NS034435, NS034435)
- National Center for Research Resources
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD071593, P30HD071593)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- neuronal aging, Caenorhabditis elegans, neurite outgrowth, dendritic branching, synaptic integrity, synaptic vesicles, presynaptic density, insulin signaling, DAF-16/FOXO, HSF1, heat shock transcription factor, mitochondrial accumulation, locomotion, healthspan, neuroprotection, brain aging
- MeSH terms
- Age Factors, Aging, Animals, Mitochondria, Mutation, Nervous System, Neurons, Receptor, Insulin, Synapses, Touch, Transcription Factors, Signal Transduction, Neurites, Caenorhabditis elegans, Caenorhabditis elegans Proteins, Animals, Genetically Modified, Microscopy, Electron, Transmission, Green Fluorescent Proteins, Forkhead Transcription Factors
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