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Functional regeneration after laser axotomy
Abstract
Understanding how nerves regenerate is an important step towards developing treatments for human neurological disease, but investigation has so far been limited to complex organisms (mouse and zebrafish) in the absence of precision techniques for severing axons (axotomy). Here we use femtosecond laser surgery for axotomy in the roundworm Caenorhabditis elegans and show that these axons functionally regenerate after the operation. Application of this precise surgical technique should enable nerve regeneration to be studied in vivo in its most evolutionarily simple form.
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“In contrast, forward locomotion in these mutants or D-ablated worms is described either as wild type (Walthall et al., 1993; Yanik et al., 2004), or nearly wild type with a reduction in amplitude (McIntire et al., 1993b).”
From Gait Modulation in C. elegans: An Integrated Neuromechanical Model (2012) · cites this paper as Yanik et al., 2004
In the citing paper
“The function of D-class neurons can be knocked out through mutation of genes required in the GABA pathway (McIntire et al., 1993b), by targeted killing of D-class neurons (Walthall et al., 1993) and by laser axotomy (Yanik et al., 2004), yielding essentially the same so-called shrinker phenotype (Hodgkin, 1983) in all cases: When touched on the head, wild type worms will back up, whereas worms who”
From Gait Modulation in C. elegans: An Integrated Neuromechanical Model (2012) · cites this paper as Yanik et al., 2004
In the citing paper
“In fact, in every case where forward locomotion of GABA pathway defective worms was reported (McIntire et al., 1993b; Walthall et al., 1993; Yanik et al., 2004), the assay was performed on agar.”
From Gait Modulation in C. elegans: An Integrated Neuromechanical Model (2012) · cites this paper as Yanik et al., 2004
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“axonal stumps into growth cone-like structures in response to laser axotomy [68].”
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“…and biophotonics, where it enables precise surgery on cells and within transparent tissues (Vogel et al. 1990; Juhasz et al. 1999; Koenig et al. 1999; Tirlapur & Koenig 2002; Yanik et al. 2004; Vogel et al. 2005; Chung & Mazur 2009; Palanker et al. 2010; Stevenson et al. 2010; Hoy et al. 2014).”
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Self-citationA Self-Regulating Feed-Forward Circuit Controlling C. elegans Egg-Laying Behavior
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“To determine the effect of the nerve-ring input on HSN activity, we severed the HSN axons using femtosecond laser ablation [11, 32, 33].”
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“Yanik et al [15] used femtosecond laser surgery to cut individual axons in the roundworm C.”
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“showed that motor neuron axons regrow after being cut (Yanik et al., 2004), pioneering C.”
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“…to focally photoablate individual fluorescently labeled dendrites, axons, and/or glial processes in mammals, as has been done in invertebrate axons (119), and then test for resting tension in different regions (CGM, OCL, gyral WM blades), orientations (radial vs. tangential), species,…”
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“high cell viability and causing no nonspecific intracellular ablation.(56) For our experiments, we expected a laser induced photodam-”
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“A model for PNS axon regeneration in Caenorhabditis elegans has been described (Yanik et al., 2004), but no paradigms are available yet to study regenerating CNS axons in worms or flies.”
BackgroundAxonal regeneration proceeds through specific axonal fusion in transected C. elegans neurons
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“RESULTS Different neuronal types have different capacities for adult-stage axon regeneration Yanik et al. discovered functional regeneration of axons of the DA/DB motoneurons after adult-stage axotomy (Yanik et al., 2004).”
BackgroundInfluentialNotch Signaling Inhibits Axon Regeneration
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“Two-Photon Laser Axotomy of the First Branchpoint Eliminates High-Frequency Bursts To test the role of the first node of Ranvier more directly and within the same cell, two-photon laser axotomy was applied to cut targeted locations of visualized axons with micrometerprecise spatial control (Mejia-Gervacio et al., 2007…”
Digital holographic microscopy for quantitative cell dynamic evaluation during laser microsurgery
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“Recently, laser scissors have been utilized to study the process of injury and regeneration in the nervous system [14].”
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Neuro-optical microfluidic platform to study injury and regeneration of single axons
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“As observed previously [2,3,9,12,13], severed processes display substantial regeneration from the soma-proximal side, with the severed stump regenerating a structure that first extends multiple spike-like filopodia and then directs further axonal extension (see Movie S1 for a typical depiction of wild type (WT) regene…”
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Microfluidic Chips for In Vivo Imaging of Cellular Responses to Neural Injury in Drosophila Larvae
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“elegans axons can regrow along the distal stump, and can sometimes re-fuse with the distal stump [15,16,19].”
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Nanomedicine in Ophthalmology: The New Frontier
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The Genetics of Axon Guidance and Axon Regeneration in Caenorhabditis elegans
Chisholm, A. D., Hutter, H., Jin, Y., & Wadsworth, W. G. (2016) · Genetics · doi:10.1534/genetics.115.186262 · Cited by 96
“Both cholinergic and GABAergic motor neurons exhibit comparable regenerative responses; the axonal regrowth, although errorprone, can restore behavioral function (Yanik et al. 2004).”
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“Although this has not yet been used to ablate neuronal cells of zebrafish, it has been successful in studying neuronal regeneration in Caenorhabditis elegans [184].”
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Self-citationFemtosecond Laser Micromachining
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“above are observed, but even here cell level regeneration is observed as axons are capable of regrowth after injury (Yanik et al. 2004; Yanik et al. 2006; Chen et al. 2011).”
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“Regeneration of pLL axons qualitatively resembled axon regeneration described in invertebrates [59] and in some other vertebrate axons [60,61].”
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“This laser axotomy approach differs from a previous technique that used a regenerative optical amplifier to provide pulse powers of 10–40 nJ and oil immersion, high NA short working distance objectives to break down the optical transparency and cause rapid heating and vaporization at the focal spot [49].”
MethodAn all-optical approach for probing microscopic flows in living embryos.
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“Thanks to the relatively low scattering of near infrared light in tissue, this technique can be used to perform 3D-confined dissections in thicker specimens, permitting useful applications in neuroscience (6) and developmental biology (7).”
MethodExploring Living Multicellular Organisms, Organs, and Tissues Using Microfluidic Systems
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The growth factor SVH-1 regulates axon regeneration in C. elegans via the JNK MAPK cascade
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“Perforation of membranes, cutting for filaments and destruction of cell organelles were possible in living tissue without sideeffects [10].”
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“For some relevant phenotypes, such as axonal regeneration after microsurgery [78] or maintenance of motorneuron synapses, subcellular observations are required.”
BackgroundTwo-photon axotomy and time-lapse confocal imaging in live zebrafish embryos
O'Brien, G. S., Rieger, S., Martin, S. M., Cavanaugh, A. M., Portera-Cailliau, C., & Sagasti, A. (2009) · Journal of Visualized Experiments · doi:10.3791/1129 · Cited by 75
Metadata
- Authors
- Yanik, M. F., Cinar, H., Cinar, H. N., Chisholm, A. D., Jin, Y., & Ben-Yakar, A.
- Affiliations
- Stanford University (US)
- University of California, Santa Cruz (US)
- Howard Hughes Medical Institute (US)
- Venue
- Nature
- Published
- 2004-12-15
- Volume
- 432
- Issue
- 7019
- Pages
- 822-822
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2076188357
- Cited by
- 598
- References
- 0
- Citations by year
- 2026: 6 · 2025: 14 · 2024: 15 · 2023: 21 · 2022: 15 · 2021: 30 · 2020: 38 · 2019: 23 · 2018: 20 · 2017: 25 · 2016: 37 · 2015: 21 · 2014: 24 · 2013: 35 · 2012: 45
- FWCI
- 7.85
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nerve injury and regeneration
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Planarian Biology and Electrostimulation
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Keywords
- nerve regeneration, axotomy, Caenorhabditis elegans, functional regeneration
- MeSH terms
- Animals, Axons, Larva, Locomotion, Motor Neurons, Nerve Regeneration, Neurosurgery, Caenorhabditis elegans, Axotomy, Laser Therapy
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