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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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“In contrast, many sensory neurons in the head and tail of the animal do not show significant re-growth [49, 52, 53].”
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“elegans neurons display a robust regeneration response following precise severing of single, stereotyped axons using a high-powered laser (57, 58).”
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“Among the several existing immobilization techniques, the traditional methods include the use of anesthetics [1, 2] or gluing worms to substrates [7] to ensure complete immobilization during surgery and imaging.”
BackgroundMethodSelf-citationLaser fabrication of functional micro-supercapacitors
Wang, Y., Zhao, Y., & Qu, L. (2020) · Journal of Energy Chemistry · doi:10.1016/j.jechem.2020.12.002 · Cited by 69
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Ex vivo characterization of sub-10-fs pulses
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“Axons of touch cells (and many other neuronal types), after being severed using a pulsed laser beam, are capable of spontaneous regrowth [51].”
BackgroundNerve Regeneration in Caenorhabditis elegans After Femtosecond Laser Axotomy
Yanik, M., Cinar, H., Cinar, H. N., Gibby, A., Chisholm, A., Jin, Y.-S., & Ben-Yakar, A. (2006) · IEEE Journal of Selected Topics in Quantum Electronics · doi:10.1109/jstqe.2006.879579 · Cited by 51
“Recently, for axotomy of subcellular neuronal processes in vivo, we have performed femtosecond laser nanosurgery using a homemade microscope with two-photon imaging capability [3].”
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Ben-Yakar, A., & Bourgeois, F. (2009) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2009.01.008 · Cited by 48
“It has been successfully applied to severe axons [10] and dendrites of neurons [11], blood vessels [12], and membranes of embryos (chorion) [13], whose dimensions may vary from microns to as small as a couple of hundred nanometers.”
Self-citationLocation-dependent photogeneration of calcium waves in HeLa cells
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Self-citationAxotomy-induced HIF-serotonin signalling axis promotes axon regeneration in C. elegans
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Molecular Control of Axon Growth
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“elegans, single axons labeled by Green Fluorescent Protein (GFP) can be severed by laser axotomy, and this technique was recently used to test 654 mutant lines for inhibition or potentiation of axon regeneration (Chen et al., 2011; Yanik et al., 2004).”
BackgroundMethodInfluentialMicrofluidic platforms for the study of neuronal injury in vitro
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Self-citationPhotostimulation of astrocytes with femtosecond laser pulses.
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Genetic dissection of axon regeneration
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“They found that the GABAergic motor neuron axons are capable of functional regeneration post laser axotomy [2].”
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Magidson, V., Loncarek, J., Hergert, P. J., Rieder, C., & Khodjakov, A. (2007) · Methods in Cell Biology · doi:10.1016/s0091-679x(06)82007-8 · Cited by 42
“For example, near infrared femtosecond lasers have much better penetration depth and thus are indispensable for in-tissue ablations (Chung et al., 2006; Yanik et al., 2004).”
BackgroundInfluentialAxon regeneration in C. elegans: Worming our way to mechanisms of axon regeneration
Byrne, A. B., & Hammarlund, M. (2016) · Experimental Neurology · doi:10.1016/j.expneurol.2016.08.015 · Cited by 46
“Not only do the axons regenerate, the regenerated axons are able to restore functional connections with the musculature (Yanik et al., 2004; El Bejjani and Hammarlund, 2012).”
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“Although, functional regeneration in a D-type GABAergic motor neuron was reported earlier (16), no study to date has addressed the functional aspect of regeneration in touch neurons.”
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Sarntinoranont, M., Lee, S., Hong, Y., King, M., Subhash, G., Kwon, J., & Moore, D. F. (2012) · Journal of Neurotrauma · doi:10.1089/neu.2011.1772 · Cited by 39
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Fabrication and Applications of Heterostructure Materials for Broadband Ultrafast Photonics
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“Technological development of femtosecond laser axotomy in C. elegans opened the door to identifying novel factors in axon injury response (Yanik et al. 2004).”
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Self-citationPeculiarities in light scattering by spherical particles with radial anisotropy.
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“The nematode Caenorhabditis elegans has been successfully used as a model system to study the mechanisms of axon regeneration (Yanik et al. 2004; Hammarlund et al. 2007; O’Brien & Sagasti 2009).”
MethodThe Caenorhabditis elegans interneuron ALA is (also) a high-threshold mechanosensor
Sanders, J., Nagy, S., Fetterman, G. C., Wright, C. S., Treinin, M., & Biron, D. (2013) · BMC Neuroscience · doi:10.1186/1471-2202-14-156 · Cited by 34
“Ablations and axotomy were performed on L4 larvae, immobilized with 10 μM levamisole on a 2% agarose pad, using a Ti:sapphire femtosecond laser, as previously described [61-63].”
MethodAxon regeneration mechanisms: insights from C. elegans
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“discovered functional regeneration of axons of the DA/DB motoneurons after adult-stage axotomy (Yanik et al., 2004).”
BackgroundMicrofluidics: streamlining discovery in worm biology
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“To examine the effect of ets-1 on axon regeneration, we assayed regrowth after laser axot-omy in γ -aminobutyric acid (GABA)-releasing D-type motor neurons, which extend their axons from the ventral to the dorsal nerve cord (Fig 2A) [4,6].”
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In vivo Imaging of Mitochondrial Transport in Single-Axon Regeneration of Zebrafish Mauthner Cells
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“We initially applied in vivo laser axotomy (Yanik et al., 2004; O’Brien et al., 2009; Byrne et al., 2011; O’Donnell et al., 2013) to precisely sever a single M axon.”
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Axonal fusion: An alternative and efficient mechanism of nerve repair
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Neuronal functions of FOXO/DAF-16
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“Adult neurons can be severed using laser axotomy, which allows for accurate and reproducible cutting of single neurons in vivo, followed by a stereotyped regenerative response [53].”
BackgroundAxon Regeneration in C. elegans
Hammarlund, M., & Jin, Y.-S. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.04.001 · Cited by 31
“The GABA neurons were the first neurons analyzed by laser axotomy [1].”
BackgroundMethodSelf-citationCanty, A. J., Ruivo, L. M. T.-G., Nesarajah, C., Song, S., Jackson, J., Little, G. E., & Paola, V. D. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0254-13.2013 · Cited by 33
“Laser-mediated axotomy in the living mouse brain We have used short pulses of high-energy femtosecond lasers (Yanik et al., 2004; O’Brien et al., 2009; Ylera et al., 2009; Allegra Mascaro et al., 2010; Farrar et al., 2012; Canty et al., 2013) directed through the viewing window to induce discrete…”
MethodBaumgart, J., Kuetemeyer, K., Bintig, W., Ngezahayo, A., Ertmer, W., Lubatschowski, H., & Heisterkamp, A. (2009) · Journal of Biomedical Optics · doi:10.1117/1.3253382 · Cited by 31
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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