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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Forward locomotion in D-class mutants or D-ablated worms is described either as wild type or nearly wild type with a reduction in amplitude.
“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
Knocking out D-class neuron function yields essentially the same shrinker phenotype in all cases: when touched on the head, worms contract muscles along both sides of their bodies.
“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 every case where forward locomotion of GABA pathway defective worms was reported, the assay was performed on agar.
“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
Cites
The structure of the nervous system of the nematode <i>Caenorhabditis elegans</i>
White, J. G., Southgate, E., Thomson, J. N., & Brenner, S. (1986) · Philosophical Transactions of the Royal Society of London. B, Biological Sciences · doi:10.1098/rstb.1986.0056 · Cited by 5,589 · see citing works
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Femtosecond laser micromachining in transparent materials
Gattass, R. R., & Mazur, E. (2008) · Nature Photonics · doi:10.1038/nphoton.2008.47 · Cited by 3,267 · see citing works
Ultrafast lasers—reliable tools for advanced materials processing
Sugioka, K., & Cheng, Y. (2014) · Light: Science & Applications · doi:10.1038/lsa.2014.30 · Cited by 1,545 · see citing works
Thermo‐plasmonics: using metallic nanostructures as nano‐sources of heat
Baffou, G., & Quidant, R. (2013) · Laser & Photonics Review · doi:10.1002/lpor.201200003 · Cited by 1,318 · see citing works
Mechanisms of femtosecond laser nanosurgery of cells and tissues
Vogel, A., Noack, J., Hüttman, G., & Paltauf, G. (2005) · Applied Physics B · doi:10.1007/s00340-005-2036-6 · Cited by 1,410 · see citing works
Finding function in novel targets: C. elegans as a model organism
Kaletta, T., & Hengartner, M. O. (2006) · Nature Reviews Drug Discovery · doi:10.1038/nrd2031 · Cited by 1,091 · see citing works
Principles of two-photon excitation microscopy and its applications to neuroscience
Svoboda, K., & Yasuda, R. (2006) · Neuron · doi:10.1016/j.neuron.2006.05.019 · Cited by 1,027 · see citing works
Ablation-cooled material removal with ultrafast bursts of pulses
Kerse, C., Kalaycıoğlu, H., Elahi, P., Çetin, B., Kesim, D. K., Akçaalan, Ö., Yavaş, S., Aşık, M. D., Oktem, B., Hoogland, H., et al. (2016) · Nature · doi:10.1038/nature18619 · Cited by 860 · see citing works
Serial time-encoded amplified imaging for real-time observation of fast dynamic phenomena
Goda, K., Tsia, K., & Jalali, B. (2009) · Nature · doi:10.1038/nature07980 · Cited by 753 · see citing works
In situ wavefront correction and its application to micromanipulation
Čižmár, T., Mazilu, M., & Dholakia, K. (2010) · Nature Photonics · doi:10.1038/nphoton.2010.85 · Cited by 455 · see citing works
Rotational manipulation of single cells and organisms using acoustic waves
Ahmed, D., Ozcelik, A., Bojanala, N., Nama, N., Upadhyay, A., Chen, Y.-C., Hanna-Rose, W., & Huang, T. (2016) · Nature Communications · doi:10.1038/ncomms11085 · Cited by 481 · see citing works
Neuronal Intrinsic Mechanisms of Axon Regeneration
Liu, K., Tedeschi, A., Park, K. K., & He, Z. (2011) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-061010-113723 · Cited by 458 · see citing works
Axon Regeneration Requires A Conserved MAP Kinase Pathway
Hammarlund, M., Nix, P., Hauth, L., Jorgensen, E., & Bastiani, M. (2009) · Science · doi:10.1126/science.1165527 · Cited by 453 · see citing works
Wallerian Degeneration, Wld<sup>S</sup>, and Nmnat
Coleman, M. P., & Freeman, M. R. (2010) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-060909-153248 · Cited by 473 · see citing works
“…the focus of this work is exploring mechanisms of regeneration of the proximal stump (Guo et al. 2008; Hammarlund et al. 2007, 2009; Wu et al. 2007; Yanik et al. 2004), we can glean some information regarding degeneration of the distal fragment, which beads, degenerates, and disappears in a manner…”
BackgroundSahu, T. A., Ratre, Y. K., Chauhan, S., Bhaskar, L. V., Nair, M. P., & Verma, H. K. (2021) · Journal of Drug Delivery Science and Technology · doi:10.1016/j.jddst.2021.102487 · Cited by 509 · see citing works
Adult neurogenesis and brain regeneration in zebrafish
Kızıl, Ç., Kaslin, J., Kroehne, V., & Brand, M. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20918 · Cited by 346 · see citing works
“Recent advancements in nanosurgery methods, which reduce the traumaticity and increase the precision of the injury, seems promising (Yanik et al., 2004; Steinmayer et al., 2010; Samara et al., 2010) and will probably serve as better tools to alleviate degenerative effects of physical lesions in the future.”
BackgroundHigh-throughput in vivo vertebrate screening
Pardo-Martín, C., Chang, T.-Y., Koo, B. K., Gilleland, C., Wasserman, S., & Yanik, M. (2010) · Nature Methods · doi:10.1038/nmeth.1481 · Cited by 341 · see citing works
Self-citationRegulation of axonal regeneration after mammalian spinal cord injury
Zheng, B., & Tuszynski, M. H. (2023) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-022-00562-y · Cited by 328 · see citing works
Coherent Anti-Stokes Raman Scattering Imaging of Axonal Myelin in Live Spinal Tissues
Wang, H., Fu, Y., Zickmund, P., Shi, R., & Cheng, J. (2005) · Biophysical Journal · doi:10.1529/biophysj.105.061911 · Cited by 317 · see citing works
Rohde, C., Zeng, F., Gonzalez-Rubio, R., Angel, M., & Yanik, M. (2007) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.0706513104 · Cited by 316 · see citing works
Self-citationGhosh-Roy, A., Wu, Z.-L., Goncharov, A., Jin, Y.-S., & Chisholm, A. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.5464-09.2010 · Cited by 304 · see citing works
“This distinction between central and peripheral axon regeneration reflects differences both in glial microenvironment (Yiu and He, 2006) and in intrinsic growth abilities (Filbin, 2003).”
BackgroundSelf-citationFacilitation of axon regeneration by enhancing mitochondrial transport and rescuing energy deficits
Zhou, B., Yu, P., Lin, M.-Y., Sun, T., Chen, Y., & Sheng, Z. (2016) · The Journal of Cell Biology · doi:10.1083/jcb.201605101 · Cited by 321 · see citing works
Surgical applications of femtosecond lasers
Chung, S. H., & Mazur, E. (2009) · Journal of Biophotonics · doi:10.1002/jbio.200910053 · Cited by 265 · see citing works
“elegans described post-surgery functional regeneration of motor axons [120, 121].”
BackgroundAxon pruning: An essential step underlying the developmental plasticity of neuronal connections
Low, L. K., & Cheng, H.-J. (2006) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2006.1883 · Cited by 258 · see citing works
“Interestingly, a recent report has demonstrated that axon regeneration can be modelled to some extent in C. elegans (Yanik et al. 2004).”
BackgroundA microfabricated array of clamps for immobilizing and imaging C. elegans
Hulme, S. E., Shevkoplyas, S. S., Apfeld, J., Fontana, W., & Whitesides, G. M. (2007) · Lab on a Chip · doi:10.1039/b707861g · Cited by 216 · see citing works
Nanotechnology, nanomedicine and nanosurgery.
Freitas, R. (2005) · International Journal of Surgery · doi:10.1016/j.ijsu.2005.10.007 · Cited by 233 · see citing works
Wu, Z.-L., Ghosh-Roy, A., Yanik, M., Zhang, J. Z., Jin, Y.-S., & Chisholm, A. (2007) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.0707001104 · Cited by 231
Self-citationClark, D., Biron, D., Sengupta, P., & Samuel, A. D. T. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.1137-06.2006 · Cited by 226 · see citing works
“elegans using tightly focused femtosecond laser pulses (Yanik et al., 2004; Chung et al., 2006).”
BackgroundMethodAxons break in animals lacking β-spectrin
Hammarlund, M., Jorgensen, E., & Bastiani, M. (2007) · Journal of Cell Biology · doi:10.1083/jcb.200611117 · Cited by 216 · see citing works
“elegans neurons that have been artifi cially severed also fail to regrow normally, demonstrating that abnormal regrowth is a property of regenerating neurons rather than of spectrin mutants (Yanik et al., 2004).”
BackgroundFemtosecond laser nanoaxotomy lab-on-a-chip for in vivo nerve regeneration studies
Guo, S. X., Bourgeois, F., Chokshi, T., Durr, N., Hilliard, M., Chronis, N., & Ben-Yakar, A. (2008) · Nature Methods · doi:10.1038/nmeth.1203 · Cited by 215 · see citing works
Self-citationMitochondria localize to injured axons to support regeneration
Han, S., Baig, H. S., & Hammarlund, M. (2016) · Neuron · doi:10.1016/j.neuron.2016.11.025 · Cited by 210 · see citing works
Liu, Y., Lai, P., Ma, C., Xu, X., Grabar, A., & Wang, L.-H. V. (2015) · Nature Communications · doi:10.1038/ncomms6904 · Cited by 208
Axon regeneration requires coordinate activation of p38 and JNK MAPK pathways
Nix, P., Hisamoto, N., Matsumoto, K., & Bastiani, M. (2011) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1104830108 · Cited by 200 · see citing works
Axon Regeneration Pathways Identified by Systematic Genetic Screening in C. elegans
Chen, L., Wang, Z., Ghosh‐Roy, A., Hubert, T., Yan, D., O'Rourke, S., Bowerman, B. A., Wu, Z., Jin, Y., & Chisholm, A. D. (2011) · Neuron · doi:10.1016/j.neuron.2011.07.009 · Cited by 196 · see citing works
“Axons labeled with GFP transgenes can be severed precisely with ultrafast laser irradiation (Yanik et al., 2004).”
Self-citationUltrafast laser direct writing and nanostructuring in transparent materials
Beresna, M., Gecevičius, M., & Kazansky, P. G. (2014) · Advances in Optics and Photonics · doi:10.1364/aop.6.000293 · Cited by 224 · see citing works
Traveling waves in developing cerebellar cortex mediated by asymmetrical Purkinje cell connectivity
Watt, A. J., Cuntz, H., Mori, M., Nusser, Z., Sjöström, P. J., & Häusser, M. (2009) · Nature Neuroscience · doi:10.1038/nn.2285 · Cited by 194 · see citing works
Jain, K. (2008) · Humana Press · doi:10.1007/978-1-61779-983-9 · Cited by 179
Pulse energy dependence of subcellular dissection by femtosecond laser pulses.
Heisterkamp, A., Maxwell, I., Mazur, E., Underwood, J. M., Nickerson, J., Kumar, S., & Ingber, D. (2005) · Optics Express · doi:10.1364/opex.13.003690 · Cited by 178 · see citing works
Future impact of nanotechnology on medicine and dentistry
Patil, M., Mehta, D., & Guvva, S. (2008) · Journal of Indian Society of Periodontology · doi:10.4103/0972-124x.44088 · Cited by 176 · see citing works
Recent progress in ultrafast lasers based on 2D materials as a saturable absorber
Ma, C., Wang, C., Gao, B., Adams, J., Wu, G., & Zhang, H. (2019) · Applied Physics Reviews · doi:10.1063/1.5099188 · Cited by 215 · see citing works
Breckwoldt, M. O., Pfister, F., Bradley, P. M., Marinković, P., Williams, P. R., Brill, M. S., Plomer, B., Schmalz, A., Clair, D. K. S., Naumann, R., et al. (2014) · Nature Medicine · doi:10.1038/nm.3520 · Cited by 178 · see citing works
Hydrogen Peroxide Promotes Injury-Induced Peripheral Sensory Axon Regeneration in the Zebrafish Skin
Rieger, S., & Sagasti, A. (2011) · PLoS Biology · doi:10.1371/journal.pbio.1000621 · Cited by 173 · see citing works
“elegans and zebrafish have utilized laser axotomy to precisely damage single axons in the peripheral nervous system, making it possible to assess the influence of nonneuronal tissues on axonal regeneration [9,10].”
BackgroundUltrafast Laser Applications in Manufacturing Processes: A State of the Art Review
Lei, S., Zhao, X., Yu, X., Hu, A., Vukelić, S., Jun, M. B., Joe, H.-E., Yao, Y. L., & Shin, Y. C. (2019) · Journal of manufacturing science and engineering · doi:10.1115/msec2019-2968 · Cited by 45 · see citing works
“Ampli fi ed pulse trains at few kHz repetition rate with pulse energies above the damage threshold are used for bubble formation [297 – 301], which plays a key role in the surgery process.”
Spontaneous Age-Related Neurite Branching in Caenorhabditis elegans
Tank, E. M. H., Rodgers, K. E., & Kenyon, C. J. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.6606-10.2011 · Cited by 176 · see citing works
“Neuronal regeneration and age-dependent branch formation When neurons in young C. elegans are cut, they can regenerate (Yanik et al., 2004).”
BackgroundGait Modulation in C. elegans: An Integrated Neuromechanical Model
Boyle, J. H., Berri, S., & Cohen, N. (2012) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2012.00010 · Cited by 163 · see citing works
“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.”
BackgroundInfluentialBrukman, N. G., Uygur, B., Podbilewicz, B., & Chernomordik, L. (2019) · The Journal of Cell Biology · doi:10.1083/jcb.201901017 · Cited by 195 · see citing works
“A system to cut axons using laser microsurgery (axotomy) was implemented in C. elegans (Yanik et al., 2004) and was used in a breakthrough experiment which determined that EFF-1 fuses cut axons in the PLM mechanosensory neuron (Ghosh-Roy and Chisholm, 2010).”
MethodZeng, F., Rohde, C., & Yanik, M. (2008) · Lab on a Chip · doi:10.1039/b804808h · Cited by 161
Self-citationInsulin/IGF1 Signaling Inhibits Age-Dependent Axon Regeneration
Byrne, A. B., Walradt, T. J., Gardner, K. E., Hubbert, A., Reinke, V., & Hammarlund, M. (2014) · Neuron · doi:10.1016/j.neuron.2013.11.019 · Cited by 158 · see citing works
CO 2 and compressive immobilization of C. elegans on-chip
Chokshi, T. V., Ben‐Yakar, A., & Chronis, N. (2008) · Lab on a Chip · doi:10.1039/b807345g · Cited by 136 · see citing works
Self-citationHulme, S. E., & Whitesides, G. M. (2011) · Angewandte Chemie International Edition · doi:10.1002/anie.201005461 · Cited by 137 · see citing works
Targeted transfection of stem cells with sub-20 femtosecond laser pulses.
Uchugonova, A., König, K., Bueckle, R., Isemann, A., & Tempea, G. (2008) · Optics Express · doi:10.1364/oe.16.009357 · Cited by 140
Ben-Yakar, A., Chronis, N., & Lu, H. (2009) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2009.10.010 · Cited by 138 · see citing works
“Microfluidics for nerve regeneration studies Ultrafast laser nanosurgery has emerged as a new neurosurgical tool that is capable of precisely ablating neuronal tissue in living organisms in a minimally invasive fashion [29,30].”
BackgroundSelf-citationIn-Vitro Approaches for Studying Blast-Induced Traumatic Brain Injury
Chen, Y. C., Smith, D. H., & Meaney, D. F. (2009) · Journal of Neurotrauma · doi:10.1089/neu.2008.0645 · Cited by 128 · see citing works
“Certainly, the laser-induced shock-wave pulse can be controlled to create nanosurgical procedures capable of in-vivo transection of individual nerve fibers within the roundworm Caenorhabditis elegans (Yanik et al., 2004).”
Miniaturized probe for femtosecond laser microsurgery and two-photon imaging
Hoy, C. L., Durr, N. J., Chen, P., Piyawattanametha, W., Ra, H., Solgaard, O., & Ben‐Yakar, A. (2008) · Optics Express · doi:10.1364/oe.16.009996 · Cited by 126 · see citing works
Self-citationThe DLK signalling pathway—a double‐edged sword in neural development and regeneration
Tedeschi, A., & Bradke, F. (2013) · EMBO Reports · doi:10.1038/embor.2013.64 · Cited by 133 · see citing works
“axonal stumps into growth cone-like structures in response to laser axotomy [68].”
Liang, X., Linz, N., Freidank, S., Paltauf, G., & Vogel, A. (2022) · Journal of Fluid Mechanics · doi:10.1017/jfm.2022.202 · Cited by 143 · see citing works
“…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).”
BackgroundTibbitt, M., Kloxin, A. M., Dyamenahalli, K., & Anseth, K. (2010) · Soft Matter · doi:10.1039/c0sm00174k · Cited by 123 · see citing works
Samara, C., Rohde, C., Gilleland, C., Norton, S., Haggarty, S., & Yanik, M. (2010) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1005372107 · Cited by 121 · see citing works
Self-citationA Self-Regulating Feed-Forward Circuit Controlling C. elegans Egg-Laying Behavior
Zhang, M., Chung, S., Fang-Yen, C. M., Craig, C., Kerr, R. A., Suzuki, H., Samuel, A. D. T., Mazur, E., & Schafer, W. R. (2008) · Current Biology · doi:10.1016/j.cub.2008.08.047 · Cited by 103 · see citing works
“To determine the effect of the nerve-ring input on HSN activity, we severed the HSN axons using femtosecond laser ablation [11, 32, 33].”
MethodEvolutionary loss of animal regeneration: pattern and process.
Bely, A. E. (2010) · Integrative and Comparative Biology · doi:10.1093/icb/icq118 · Cited by 119 · see citing works
“As an example, it is widely known that the nematode model organism Caenorhabditis elegans cannot regenerate at the ‘‘structure’’ level, such as after a transverse body amputation (although this speci es is capable of axonal regeneration; Yanik et al. 2004).”
BackgroundGold-Nanoparticle-Enhanced Cancer Photothermal Therapy
Li, J., & Gu, M. (2009) · IEEE Journal of Selected Topics in Quantum Electronics · doi:10.1109/jstqe.2009.2030340 · Cited by 118 · see citing works
“2) Selecting ultrafast pulsed lasers, particularly femtosecond laser, instead of CW laser: Femtosecond laser microsurgery (FLMS) has emerged as a superior technique for ablation of cells and subcellular structures [63], [ 64 ].”
MethodNanomedicine: Techniques, Potentials, and Ethical Implications
Ebbesen, M., & Jensen, T. G. (2006) · Journal of Biomedicine and Biotechnology · doi:10.1155/jbb/2006/51516 · Cited by 117 · see citing works
“Yanik et al [15] used femtosecond laser surgery to cut individual axons in the roundworm C.”
BackgroundLaser Microsurgery in Caenorhabditis elegans
Fang-Yen, C., Gabel, C. V., Samuel, A. D. T., Bargmann, C., & Avery, L. (2012) · Methods in Cell Biology · doi:10.1016/b978-0-12-394620-1.00006-0 · Cited by 116 · see citing works
“showed that motor neuron axons regrow after being cut (Yanik et al., 2004), pioneering C.”
A 2020 view of tension-based cortical morphogenesis
Essen, D. C. V. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2016830117 · Cited by 124 · see citing works
“…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,…”
Leary, S., Liu, C., & Apuzzo, M. (2006) · Neurosurgery · doi:10.1227/01.neu.0000217016.79256.16 · Cited by 113 · see citing works
Torgersen, J., Ovsianikov, A., Mironov, V. A., Pucher, N., Qin, X., Li, Z., Cicha, K., Machacek, T., Liska, R., Jantsch, V., et al. (2012) · Journal of Biomedical Optics · doi:10.1117/1.jbo.17.10.105008 · Cited by 137 · see citing works
“high cell viability and causing no nonspecific intracellular ablation.(56) For our experiments, we expected a laser induced photodam-”
BackgroundPiqué, A., Auyeung, R. C. Y., Kim, H., Charipar, N. A., & Mathews, S. A. (2016) · Journal of Physics D Applied Physics · doi:10.1088/0022-3727/49/22/223001 · Cited by 119 · see citing works
Axonal Injury and Regeneration in the Adult Brain of Drosophila
Ayaz, D., Leyssen, M., Koch, M., Yan, J.-K., Srahna, M., Sheeba, V., Fogle, K. J., Holmes, T. C., & Hassan, B. A. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0101-08.2008 · Cited by 103
“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
Neumann, B., Nguyen, K. C. Q., Hall, D. H., Ben-Yakar, A., & Hilliard, M. A. (2011) · Developmental Dynamics · doi:10.1002/dvdy.22606 · Cited by 101 · see citing works
“The development of laser-based surgery to transect individual axons in C. elegans (Yanik et al., 2004), has enabled this organism to become a crucial genetic model system to study axonal regeneration at the cellular and molecular level (Ghosh-Roy and Chisholm, 2010).”
BackgroundInfluentialSelf-citationCanty, A. J., Huang, L., Jackson, J., Little, G. E., Knott, G. W., Maco, B., & Paola, V. D. (2013) · Nature Communications · doi:10.1038/ncomms3038 · Cited by 99 · see citing works
Gabel, C. V., Antoine, F., Chuang, C., Samuel, A. D. T., & Chang, C. (2008) · Development · doi:10.1242/dev.013995 · Cited by 97 · see citing works
“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
Bejjani, R. E., & Hammarlund, M. (2012) · Neuron · doi:10.1016/j.neuron.2011.11.017 · Cited by 96 · see citing works
“Neuron 73, 268–278, January 26, 2012 ª2012 Elsevier Inc. 269 40 A ** B as the neurons regenerate (Yanik et al., 2004).”
BackgroundInfluentialFirst node of Ranvier facilitates high-frequency burst encoding.
Kole, M. (2011) · Neuron · doi:10.1016/j.neuron.2011.06.024 · Cited by 96 · see citing works
“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
Yu, L.-F., Mohanty, S., Zhang, J., Genc, S., Kim, M. K., Berns, M., & Chen, Z.-P. (2009) · Optics Express · doi:10.1364/oe.17.012031 · Cited by 96
“Recently, laser scissors have been utilized to study the process of injury and regeneration in the nervous system [14].”
MethodMcKinnon, D. D., Brown, T. E., Kyburz, K. A., Kiyotake, E. A., & Anseth, K. S. (2014) · Biomacromolecules · doi:10.1021/bm500731b · Cited by 105 · see citing works
Crossing the threshold of ultrafast laser writing in bulk silicon
Chanal, M., Fedorov, V. Y., Chambonneau, M., Clady, R. G. C. R., Tzortzakis, S., & Grojo, D. (2017) · Nature Communications · doi:10.1038/s41467-017-00907-8 · Cited by 109 · see citing works
Neuro-optical microfluidic platform to study injury and regeneration of single axons
Kim, Y. T., Karthikeyan, K., Chirvi, S., & Davé, D. P. (2009) · Lab on a Chip · doi:10.1039/b903720a · Cited by 86 · see citing works
Pinan-Lucarré, B., Gabel, C. V., Reina, C. P., Hulme, S. E., Shevkoplyas, S., Slone, R. D., Xue, J., Qiao, Y., Weisberg, S., Roodhouse, K., et al. (2012) · PLoS Biology · doi:10.1371/journal.pbio.1001331 · Cited by 90 · see citing works
“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…”
BackgroundWorm chips: microtools for C. elegans biology.
Chronis, N. (2010) · Lab on a Chip · doi:10.1039/b919983g · Cited by 88 · see citing works
Coşkun, A., Şencan, I., Su, T.-W., & Ozcan, A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0015955 · Cited by 87 · see citing works
“is an essential need for all these fields to enable high-throughput screening of this model organism. While several high-throughput imaging platforms have been successfully demonstrated so far”
BackgroundJiang, K., Zhang, P.-L., Song, S., Sun, T.-Z., Chen, Y., Shi, H.-C., Yan, H., Lu, Q.-H., & Chen, G. (2024) · Materials Science in Semiconductor Processing · doi:10.1016/j.mssp.2024.108559 · Cited by 87
Microfluidic Chips for In Vivo Imaging of Cellular Responses to Neural Injury in Drosophila Larvae
Ghannad‐Rezaie, M., Wang, X., Mishra, B., Collins, C. A., & Chronis, N. (2012) · PLoS ONE · doi:10.1371/journal.pone.0029869 · Cited by 91 · see citing works
“elegans axons can regrow along the distal stump, and can sometimes re-fuse with the distal stump [15,16,19].”
BackgroundSpinal cord regeneration: where fish, frogs and salamanders lead the way, can we follow?
Quiroz, J. D. D., & Echeverri, K. (2013) · Biochemical Journal · doi:10.1042/bj20121807 · Cited by 85 · see citing works
Nanomedicine in Ophthalmology: The New Frontier
Zarbin, M. A., Montemagno, C. D., Leary, J. F., & Ritch, R. H. (2010) · American Journal of Ophthalmology · doi:10.1016/j.ajo.2010.03.019 · Cited by 83 · see citing works
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 94 · see citing works
“Both cholinergic and GABAergic motor neurons exhibit comparable regenerative responses; the axonal regrowth, although errorprone, can restore behavioral function (Yanik et al. 2004).”
BackgroundInfluentialSelf-citationFleisch, V. C., Fraser, B., & Allison, W. T. (2010) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2010.10.012 · Cited by 92 · see citing works
“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].”
MethodPlasma-mediated ablation: an optical tool for submicrometer surgery on neuronal and vascular systems
Tsai, P. S., Blinder, P., Migliori, B. J., Neev, J., Jin, Y., Squier, J. A., & Kleinfeld, D. (2009) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2009.02.003 · Cited by 89 · see citing works
Self-citationFemtosecond Laser Micromachining
Cerami, L. R., Mazur, E., Nolte, S., & Schaffer, C. B. (2013) · Springer eBooks · doi:10.1007/978-3-319-00017-6_12 · Cited by 53 · see citing works
Mechanisms of Laser-Induced Dissection and Transport of Histologic Specimens
Vogel, A., Lorenz, K., Horneffer, V., Hüttmann, G., von Smolinski, D., & Gebert, A. (2007) · Biophysical Journal · doi:10.1529/biophysj.106.102277 · Cited by 78 · see citing works
Kilinc, D., Peyrin, J., Soubeyre, V., Magnifico, S., Saïas, L., Viovy, J., & Brugg, B. (2010) · Neurotoxicity Research · doi:10.1007/s12640-010-9152-8 · Cited by 82 · see citing works
Femtosecond laser nanoaxotomy properties and their effect on axonal recovery in C. elegans.
Bourgeois, F., & Ben-Yakar, A. (2007) · Optics Express · doi:10.1364/oe.16.005963 · Cited by 81 · see citing works
Self-citationTaming Ultrafast Laser Filaments for Optimized Semiconductor–Metal Welding
Chambonneau, M., Li, Q.-F., Fedorov, V., Blothe, M., Schaarschmidt, K., Lorenz, M., Tzortzakis, S., & Nolte, S. (2020) · Laser & Photonics reviews · doi:10.1002/lpor.202000433 · Cited by 77
Lai, A. G., & Aboobaker, A. A. (2017) · Developmental Biology · doi:10.1016/j.ydbio.2017.10.010 · Cited by 84 · see citing works
“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).”
BackgroundVillegas, R., Martin, S. M., O'Donnell, K. C., Carrillo, S. A., Sagasti, A., & Allende, M. (2012) · Neural Development · doi:10.1186/1749-8104-7-19 · Cited by 77
“Regeneration of pLL axons qualitatively resembled axon regeneration described in invertebrates [59] and in some other vertebrate axons [60,61].”
BackgroundTurney, S. G., & Lichtman, J. W. (2012) · PLoS Biology · doi:10.1371/journal.pbio.1001352 · Cited by 83 · see citing works
“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.
Supatto, W., Fraser, S., & Vermot, J. (2008) · Biophysical Journal · doi:10.1529/biophysj.108.137786 · Cited by 77
“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
Sivagnanam, V., & Gijs, M. A. M. (2013) · Chemical Reviews · doi:10.1021/cr200432q · Cited by 72 · see citing works
The growth factor SVH-1 regulates axon regeneration in C. elegans via the JNK MAPK cascade
Li, C., Hisamoto, N., Nix, P., Kanao, S., Mizuno, T., Bastiani, M., & Matsumoto, K. (2012) · Nature Neuroscience · doi:10.1038/nn.3052 · Cited by 76
New concepts in laser medicine: Towards a laser surgery with cellular precision
Hüttmann, G., Yao, C., & Endl, E. (2005) · doi:10.1016/j.mla.2005.03.010 · Cited by 76
“Perforation of membranes, cutting for filaments and destruction of cell organelles were possible in living tissue without sideeffects [10].”
BackgroundTeschendorf, D., & Link, C. D. (2009) · Molecular Neurodegeneration · doi:10.1186/1750-1326-4-38 · Cited by 74 · see citing works
“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
- 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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