Integrin activation promotes axon growth on inhibitory chondroitin sulfate proteoglycans by enhancing integrin signaling
Open accessAbstract
Chondroitin sulfate proteoglycans (CSPGs) are upregulated after CNS lesions, where they inhibit axon regeneration. In order for axon growth and regeneration to occur, surface integrin receptors must interact with surrounding extracellular matrix molecules. We have explored the hypothesis that CSPGs inhibit regeneration by inactivating integrins and that forcing integrins into an active state might overcome this inhibition. Using cultured rat sensory neurons, we show that the CSPG aggrecan inhibits laminin-mediated axon growth by impairing integrin signaling via decreasing phosphorylated FAK (pFAK) and pSrc levels, without affecting surface integrin levels. Forcing integrin activation and signaling by manganese or an activating antibody TS2/16 reversed the inhibitory effect of aggrecan on mixed aggrecan/laminin surfaces, and enhanced axon growth from cultured rat sensory neurons (manganese) and human embryonic stem cell-derived motoneurons (TS2/16). The inhibitory effect of Nogo-A can also be reversed by integrin activation. These results suggest that inhibition by CSPGs can act via inactivation of integrins, and that activation of integrins is a potential method for improving axon regeneration after injury.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
β1-integrins interact with CSPGs.
“Previous studies revealed an interaction between β1-integrins and CSPGs (Tan et al., 2011;Wu et al., 2002).”
From The hyaluronan and proteoglycan link proteins: Organizers of the brain extracellular matrix and key molecules for neuronal function and plasticity (2015) · cites this paper as Tan et al., 2011
A potential mechanism of CSPG-mediated repulsion may be through control of integrins.
“A potential mechanism of CSPG-mediated repulsion may be through control of integrins.”
From The hyaluronan and proteoglycan link proteins: Organizers of the brain extracellular matrix and key molecules for neuronal function and plasticity (2015) · cites this paper as Tan et al., 2011
CSPGs, especially their GAG moieties, may inhibit growth by blocking the growth-promoting activity of integrins.
“Specifically, CSPGs, and particularly their GAG moieties, may act by i) binding to a specific receptor; ii) blocking the growth-promoting activity of integrins; iii) presenting growth-inhibitory proteins.”
From The hyaluronan and proteoglycan link proteins: Organizers of the brain extracellular matrix and key molecules for neuronal function and plasticity (2015) · cites this paper as Tan et al., 2011
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Hynes (2002) · doi:10.1016/s0092-8674(02)00971-6 · Cited by 8,606 · see citing works
Regeneration beyond the glial scar
Silver, J., & Miller, J. H. (2004) · Nature reviews. Neuroscience · doi:10.1038/nrn1326 · Cited by 3,090 · see citing works
Integrin-regulated FAK–Src signaling in normal and cancer cells
Mitra, S. K., & Schlaepfer, D. D. (2006) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2006.08.011 · Cited by 1,591 · see citing works
Focal adhesion kinase: the first ten years
Parsons, J. T. (2003) · Journal of Cell Science · doi:10.1242/jcs.00373 · Cited by 1,364 · see citing works
Kindlin-3 is essential for integrin activation and platelet aggregation
Moser, M., Nieswandt, B., Ussar, S., Požgajová, M., & Fässler, R. (2008) · Nature Medicine · doi:10.1038/nm1722 · Cited by 700 · see citing works
PTPσ Is a Receptor for Chondroitin Sulfate Proteoglycan, an Inhibitor of Neural Regeneration
Shen, Y., Tenney, A. P., Busch, S. A., Horn, K. P., Cuascut, F. X., Liu, K., He, Z., Silver, J., & Flanagan, J. G. (2009) · Science · doi:10.1126/science.1178310 · Cited by 682 · see citing works
Kindlin-2 controls bidirectional signaling of integrinsPreprint
Montañez, E., Ussar, S., Schifferer, M., Bösl, M. R., Zent, R., Moser, M., & Fässler, R. (2008) · Genes & Development · doi:10.1101/gad.469408 · Cited by 452 · see citing works
Monnier, P. P., Sierra, A., Schwab, J. M., Henke‐Fahle, S., & Mueller, B. K. (2003) · Molecular and Cellular Neuroscience · doi:10.1016/s1044-7431(02)00035-0 · Cited by 400 · see citing works
Tang, X., Davies, J. E., & Davies, S. J. A. (2002) · Journal of Neuroscience Research · doi:10.1002/jnr.10523 · Cited by 387 · see citing works
The cell biology of neuronal navigation
Song, H., & Poo, M. (2001) · Nature Cell Biology · doi:10.1038/35060164 · Cited by 379 · see citing works
Koprivica, V., Cho, K., Park, J. B., Yiu, G. C., Atwal, J. K., Gore, B. B., Kim, J. A., Lin, E., Tessier‐Lavigne, M., Chen, D. F., et al. (2005) · Science · doi:10.1126/science.1115462 · Cited by 363 · see citing works
Regulation of Integrin α5β1-Fibronectin Interactions by Divalent Cations
Mould, A. P., Akiyama, S. K., & Humphries, M. J. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.44.26270 · Cited by 328 · see citing works
Sivasankaran, R., Pei, J., Wang, K., Zhang, Y. P., Shields, C. B., Xu, X., & He, Z. (2004) · Nature Neuroscience · doi:10.1038/nn1193 · Cited by 315 · see citing works
Bazzoni, G., Shih, D.-T., Buck, C. A., & Hemler, M. E. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.43.25570 · Cited by 276 · see citing works
Nieswandt, B., Moser, M., Pleines, I., Varga-Szabó, D., Monkley, S., Critchley, D. R., & Fässler, R. (2007) · The Journal of Experimental Medicine · doi:10.1084/jem.20071827 · Cited by 273 · see citing works
Semaphorin function in neural plasticity and disease
Pasterkamp, R. J., & Giger, R. J. (2009) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2009.06.001 · Cited by 227 · see citing works
Suppression of Rho-kinase activity promotes axonal growth on inhibitory CNS substrates
Borisoff, J., Chan, C. C. M., Hiebert, G. W., Oschipok, L. W., Robertson, G. S., Zamboni, R. J., Steeves, J. D., & Tetzlaff, W. (2003) · Molecular and Cellular Neuroscience · doi:10.1016/s1044-7431(02)00032-5 · Cited by 210 · see citing works
Structural basis for the inhibition of activin signalling by follistatin
Harrington, A. E., Morris-Triggs, S. A., Ruotolo, B. T., Robinson, C. V., Ohnuma, S., & Hyvönen, M. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7601000 · Cited by 166 · see citing works
α9 Integrin Promotes Neurite Outgrowth on Tenascin-C and Enhances Sensory Axon Regeneration
Andrews, M. R., Czvitkovich, S., Dassie, E., Vogelaar, C. F., Faissner, A., Blits, B., Gage, F. H., ffrench‐Constant, C., & Fawcett, J. W. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0759-09.2009 · Cited by 161 · see citing works
Self-citationMould, A. P., Askari, J. A., Aota, S., Yamada, K. M., Irie, A., Takada, Y., Mardon, H. J., & Humphries, M. J. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.28.17283 · Cited by 157 · see citing works
Regulation of Neurite Outgrowth by Integrin Activation
Ivins, J. K., Yurchenco, P. D., & Lander, A. D. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-17-06551.2000 · Cited by 152 · see citing works
Role of integrins in the peripheral nervous system
Previtali, S. C., Feltri, M. L., Archelos, J. J., Quattrini, A., Wrabetz, L. G., & Hartung, H. P. (2001) · Progress in Neurobiology · doi:10.1016/s0301-0082(00)00045-9 · Cited by 141 · see citing works
Hu, F., & Strittmatter, S. M. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1068-07.2008 · Cited by 137 · see citing works
White matter inhibitors in CNS axon regeneration failure
Xie, F., & Zheng, B. (2007) · Experimental Neurology · doi:10.1016/j.expneurol.2007.07.005 · Cited by 104 · see citing works
Schwann cell migration is integrin-dependent and inhibited by astrocyte-produced aggrecan
Afshari, F. T., Kwok, J. C., White, L., & Fawcett, J. W. (2010) · Glia · doi:10.1002/glia.20970 · Cited by 103 · see citing works
Self-citationOn the existence of a cartilage‐like proteoglycan and link proteins in the central nervous system
Asher, R. A., Scheibe, R. J., Keiser, H. D., & Bignami, A. (1995) · Glia · doi:10.1002/glia.440130406 · Cited by 100 · see citing works
Neurotrophins support regenerative axon assembly over CSPGs by an ECM-integrin-independent mechanism
Zhou, F., Walzer, M., Wu, Y.-H., Zhou, J., Dedhar, S., & Snider, W. D. (2006) · Journal of Cell Science · doi:10.1242/jcs.03016 · Cited by 98 · see citing works
Bazzoni, G., Ma, L., Blue, M., & Hemler, M. E. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.12.6670 · Cited by 92 · see citing works
Patani, R., Compston, A., Puddifoot, C. A., Wyllie, D. J. A., Hardingham, G. E., Allen, N. D., & Chandran, S. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007327 · Cited by 84 · see citing works
Self-citationReichardt, L. F., Bixby, J. L., Hall, D. E., Ignatius, M. J., Neugebauer, K. M., & Tomaselli, K. J. (1989) · Developmental Neuroscience · doi:10.1159/000111910 · Cited by 71 · see citing works
Integrin signaling is integral to regeneration
Lemons, M. L., & Condic, M. L. (2007) · Experimental Neurology · doi:10.1016/j.expneurol.2007.05.027 · Cited by 65 · see citing works
Lemons, M. L., & CONDIC, M. (2006) · Experimental Neurology · doi:10.1016/j.expneurol.2006.06.008 · Cited by 47 · see citing works
Manganese induces neurite outgrowth in PC12 cells via upregulation of αv integrins
Lein, P. J., Gallagher, P. J., Amodeo, J., Howie, H. L., & Roth, J. A. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02943-7 · Cited by 46 · see citing works
ADP-ribosylation of integrin α7 modulates the binding of integrin α7β1 to laminin
Zhao, Z., Gruszczynska‐Biegala, J., & Żółkiewska, A. (2004) · Biochemical Journal · doi:10.1042/bj20040590 · Cited by 41 · see citing works
Classification of ‘activation’ antibodies against integrin β1 chain
Tsuchida, J., Ueki, S., Saito, Y., & Takagi, J. (1997) · FEBS Letters · doi:10.1016/s0014-5793(97)01206-4 · Cited by 37 · see citing works
Chan, C. C. M., Roberts, C. R., Steeves, J. D., & Tetzlaff, W. (2007) · Journal of Neuroscience Research · doi:10.1002/jnr.21522 · Cited by 37 · see citing works
Li, H., Domowicz, M. S., Hennig, A. K., & Schwartz, N. B. (1996) · Molecular Brain Research · doi:10.1016/0169-328x(95)00269-x · Cited by 32 · see citing works
The receptor tyrosine phosphatase CRYP? affects growth cone morphology
Mueller, B. K., Ledig, M. M., & Wahl, S. (2000) · Journal of Neurobiology · doi:10.1002/1097-4695(200008)44:2 · Cited by 12 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The Biology of Regeneration Failure and Success After Spinal Cord Injury
Tran, A. P., Warren, P. M., & Silver, J. (2018) · Physiological Reviews · doi:10.1152/physrev.00017.2017 · Cited by 883 · see citing works
Moving beyond the glial scar for spinal cord repair
Bradbury, E. J., & Burnside, E. R. (2019) · Nature Communications · doi:10.1038/s41467-019-11707-7 · Cited by 748 · see citing works
The roles of perineuronal nets and the perinodal extracellular matrix in neuronal function
Fawcett, J. W., Oohashi, T., & Pizzorusso, T. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-019-0196-3 · Cited by 589 · see citing works
Self-citationPathophysiology of the brain extracellular matrix: a new target for remyelination
Lau, L. W., Cua, R., Keough, M. B., Haylock-Jacobs, S., & Yong, V. W. (2013) · Nature reviews. Neuroscience · doi:10.1038/nrn3550 · Cited by 549 · see citing works
Extracellular matrix and perineuronal nets in CNS repair
Kwok, J. C. F., Dick, G., Wang, D., & Fawcett, J. W. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20974 · Cited by 395 · see citing works
Self-citationNogo limits neural plasticity and recovery from injury
Schwab, M. E., & Strittmatter, S. M. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.02.011 · Cited by 379 · see citing works
Contrasting the Glial Response to Axon Injury in the Central and Peripheral Nervous Systems
Lutz, A. B., & Barres, B. A. (2014) · Developmental Cell · doi:10.1016/j.devcel.2013.12.002 · Cited by 229 · see citing works
Dyck, S. M., & Karimi‐Abdolrezaee, S. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2015.04.006 · Cited by 189 · see citing works
Scar-mediated inhibition and CSPG receptors in the CNS
Sharma, K., Selzer, M. E., & Li, S. (2012) · Experimental Neurology · doi:10.1016/j.expneurol.2012.07.009 · Cited by 189 · see citing works
Extracellular matrix abnormalities in schizophrenia
Berretta, S. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.08.010 · Cited by 179 · see citing works
Burnside, E. R., & Bradbury, E. J. (2013) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12114 · Cited by 153 · see citing works
Orlando, C., Ster, J., Gerber, U., Fawcett, J. W., & Raineteau, O. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.2406-12.2012 · Cited by 153 · see citing works
Self-citationAngiogenesis in the ischemic core: A potential treatment target?
Kanazawa, M., Takahashi, T., Ishikawa, M., Onodera, O., Shimohata, T., & del Zoppo, G. J. (2019) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x19834158 · Cited by 152 · see citing works
The Struggle to Make CNS Axons Regenerate: Why Has It Been so Difficult?
Fawcett, J. W. (2019) · Neurochemical Research · doi:10.1007/s11064-019-02844-y · Cited by 137 · see citing works
Self-citationCan injured adult CNS axons regenerate by recapitulating development?
Hilton, B. J., & Bradke, F. (2017) · Development · doi:10.1242/dev.148312 · Cited by 134 · see citing works
Oohashi, T., Edamatsu, M., Bekku, Y., & Carulli, D. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2015.09.010 · Cited by 131 · see citing works
Gardiner, N. J. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20950 · Cited by 129 · see citing works
Extracellular matrix and traumatic brain injury
George, N., & Geller, H. M. (2018) · Journal of Neuroscience Research · doi:10.1002/jnr.24151 · Cited by 128 · see citing works
An Extracellular Perspective on CNS Maturation: Perineuronal Nets and the Control of Plasticity
Carulli, D., & Verhaagen, J. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22052434 · Cited by 123 · see citing works
Chondroitin sulphate proteoglycans: Key modulators of spinal cord and brain plasticity
Bartus, K., James, N. D., Bosch, K. D., & Bradbury, E. J. (2011) · Experimental Neurology · doi:10.1016/j.expneurol.2011.08.008 · Cited by 117 · see citing works
“GAG-ing with the neuron”: The role of glycosaminoglycan patterning in the central nervous system
Smith, P. D., Coulson‐Thomas, V. J., Foscarin, S., Kwok, J. C. F., & Fawcett, J. W. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2015.08.004 · Cited by 112 · see citing works
Self-citationMyers, J. P., & Gómez, T. M. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2381-11.2011 · Cited by 111 · see citing works
Integrins promote axonal regeneration after injury of the nervous system
Nieuwenhuis, B., Haenzi, B., Andrews, M. R., Verhaagen, J., & Fawcett, J. W. (2018) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12398 · Cited by 104 · see citing works
Self-citationMolecular mechanisms of scar-sourced axon growth inhibitors
Ohtake, Y., & Li, S. (2014) · Brain Research · doi:10.1016/j.brainres.2014.08.064 · Cited by 102 · see citing works
Miller, G. M., & Hsieh‐Wilson, L. C. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2015.08.015 · Cited by 98 · see citing works
Extracellular matrix control of dendritic spine and synapse structure and plasticity in adulthood
Levy, A. D., Omar, M. H., & Koleske, A. J. (2014) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2014.00116 · Cited by 96 · see citing works
N-Glycosylation in Regulation of the Nervous System
Scott, H. A., & Panin, V. M. (2014) · Advances in neurobiology · doi:10.1007/978-1-4939-1154-7_17 · Cited by 90 · see citing works
Cheah, M., Andrews, M. R., Chew, D. J., Moloney, E. B., Verhaagen, J., Fässler, R., & Fawcett, J. W. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.0901-16.2016 · Cited by 89 · see citing works
Self-citationLei, W., Xing, S., Deng, C.-Y., Ju, X.-C., Jiang, X., & Luo, Z. (2012) · Cell Research · doi:10.1038/cr.2012.40 · Cited by 86 · see citing works
ARF6 Directs Axon Transport and Traffic of Integrins and Regulates Axon Growth in Adult DRG Neurons
Eva, R., Crisp, S. J., Marland, J. R. K., Norman, J. C., Kanamarlapudi, V., ffrench‐Constant, C., & Fawcett, J. W. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.1409-12.2012 · Cited by 85 · see citing works
Self-citationHayani, H., Song, I., & Dityatev, A. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00149 · Cited by 84 · see citing works
Dyck, S. M., Alizadeh, A., Santhosh, K. T., Proulx, E. H., Wu, C., & Karimi‐Abdolrezaee, S. (2015) · Stem Cells · doi:10.1002/stem.1979 · Cited by 84 · see citing works
Contributions of chondroitin sulfate proteoglycans to neurodevelopment, injury, and cancer
Silver, D. J., & Silver, J. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.03.016 · Cited by 84 · see citing works
Nakamura, F., Ohshima, T., & Goshima, Y. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.00188 · Cited by 81 · see citing works
Nogo-A Represses Anatomical and Synaptic Plasticity in the Central Nervous System
Kempf, A., & Schwab, M. E. (2013) · Physiology · doi:10.1152/physiol.00052.2012 · Cited by 76 · see citing works
Where no synapses go: gatekeepers of circuit remodeling and synaptic strength
Mironova, Y. A., & Giger, R. J. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.04.003 · Cited by 75 · see citing works
Biomaterials for revascularization and immunomodulation after spinal cord injury
Haggerty, A. E., Maldonado-Lasunción, I., & Oudega, M. (2018) · Biomedical Materials · doi:10.1088/1748-605x/aaa9d8 · Cited by 61 · see citing works
Advances in the Signaling Pathways Downstream of Glial-Scar Axon Growth Inhibitors
Sami, A., Selzer, M. E., & Li, S. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.00174 · Cited by 74 · see citing works
Role of CSPG receptor LAR phosphatase in restricting axon regeneration after CNS injury
Xu, B., Park, D., Ohtake, Y., Li, H., Hayat, U., Liu, J., Selzer, M. E., Longo, F. M., & Li, S. (2014) · Neurobiology of Disease · doi:10.1016/j.nbd.2014.08.030 · Cited by 73 · see citing works
Molecular and Cellular Mechanisms of Axonal Regeneration After Spinal Cord Injury
van Niekerk, E. A., Tuszynski, M. H., Lu, P., & Dulin, J. N. (2016) · Molecular & Cellular Proteomics · doi:10.1074/mcp.r115.053751 · Cited by 72 · see citing works
Astroglial-Derived Periostin Promotes Axonal Regeneration after Spinal Cord Injury
Shih, C., Lacagnina, M., Leuer-Bisciotti, K., & Pröschel, C. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.2947-13.2014 · Cited by 70 · see citing works
Sensory axon regeneration: rebuilding functional connections in the spinal cord
Smith, G. M., Falone, A. E., & Frank, E. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.10.006 · Cited by 69 · see citing works
Selective rab11 transport and the intrinsic regenerative ability of CNS axons
Koseki, H., Donegà, M., Lam, B., Petrova, V., van Erp, S., Yeo, G. S. H., Kwok, J. C. F., ffrench‐Constant, C., Eva, R., & Fawcett, J. W. (2017) · eLife · doi:10.7554/elife.26956 · Cited by 67 · see citing works
Self-citationFlexible Roles for Proteoglycan Sulfation and Receptor Signaling
Yu, P., Pearson, C. S., & Geller, H. M. (2018) · Trends in Neurosciences · doi:10.1016/j.tins.2017.10.005 · Cited by 67 · see citing works
Howell, M. D., & Gottschall, P. E. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.05.034 · Cited by 66 · see citing works
Integrin signalling and traffic during axon growth and regeneration
Eva, R., & Fawcett, J. W. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.03.018 · Cited by 65 · see citing works
Self-citationCheng, Y., Yin, Y., Zhang, A., Bernstein, A. M., Kawaguchi, R., Gao, K., Potter, K., Gilbert, H.-Y., Ao, Y., Ou, J., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-31960-7 · Cited by 64 · see citing works
β1 Integrin-Focal Adhesion Kinase (FAK) Signaling Modulates Retinal Ganglion Cell (RGC) Survival
Santos, A. R. C., Corredor, R. G., Obeso, B. A., Trakhtenberg, E. F., Wang, Y., Ponmattam, J., Dvoriantchikova, G., Ivanov, D., Shestopalov, V. I., Goldberg, J. L., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0048332 · Cited by 64 · see citing works
Tan, C. L., Andrews, M. R., Kwok, J. C. F., Heintz, T. G., Gumy, L. F., Fässler, R., & Fawcett, J. W. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.5472-11.2012 · Cited by 63 · see citing works
Self-citationTwo PTP receptors mediate CSPG inhibition by convergent and divergent signaling pathways in neurons
Ohtake, Y., Wong, D., Abdul-Muneer, P. M., Selzer, M. E., & Li, S. (2016) · Scientific Reports · doi:10.1038/srep37152 · Cited by 59 · see citing works
Vecino, E., Heller, J. P., Veiga‐Crespo, P., Martin, K. R. G., & Fawcett, J. W. (2015) · PLoS ONE · doi:10.1371/journal.pone.0125250 · Cited by 59 · see citing works
Self-citationDefective Mitochondrial Dynamics Underlie Manganese-Induced Neurotoxicity
Morcillo, P., Cordero, H., Ijomone, O. M., Ayodele, A. J., Bornhorst, J., Gunther-Cummins, L., Macaluso, F., Bowman, A. B., & Aschner, M. (2021) · Molecular Neurobiology · doi:10.1007/s12035-021-02341-w · Cited by 55 · see citing works
A Molecular Mechanism Regulating the Timing of Corticogeniculate Innervation
Brooks, J. M., Su, J., Levy, C., Wang, J. S., Seabrook, T. A., Guido, W., & Fox, M. A. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.09.041 · Cited by 55 · see citing works
Lerch, J. K., Martinez‐Ondaro, Y., Bixby, J. L., & Lemmon, V. (2014) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2014.02.002 · Cited by 50 · see citing works
Vimentin phosphorylation by Cdc2 in Schwann cell controls axon growth via β1‐integrin activation
Chang, I. A., Oh, M., Kim, M. H., Park, S., Kim, B. G., & Namgung, U. (2012) · The FASEB Journal · doi:10.1096/fj.11-199018 · Cited by 50 · see citing works
Kilinc, D., Blasiak, A., O’Mahony, J. J., & Lee, G. U. (2014) · Scientific Reports · doi:10.1038/srep07128 · Cited by 46 · see citing works
Yu, P., Jin, J., Tilve, S. M., Huang, Z., Zhou, L., & Geller, H. M. (2018) · Neural Regeneration Research · doi:10.4103/1673-5374.226398 · Cited by 46 · see citing works
Integrin Activation: Implications for Axon Regeneration
Cheah, M., & Andrews, M. R. (2018) · Cells · doi:10.3390/cells7030020 · Cited by 45 · see citing works
The Synaptic Extracellular Matrix: Long-Lived, Stable, and Still Remarkably Dynamic
Dankovich, T. M., & Rizzoli, S. O. (2022) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2022.854956 · Cited by 44 · see citing works
The roles of neuronal and glial precursors in overcoming chondroitin sulfate proteoglycan inhibition
Ketschek, A., Haas, C., Gallo, G., & Fischer, I. (2012) · Experimental Neurology · doi:10.1016/j.expneurol.2012.03.017 · Cited by 44 · see citing works
Theotokis, P., Lourbopoulos, A. I., Touloumi, O., Lagoudaki, R., Kofidou, E., Nousiopoulou, E., Poulatsidou, K.-N., Kesidou, E., Tascos, N., Spandou, E., et al. (2012) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e31826caebe · Cited by 44 · see citing works
Achieving CNS axon regeneration by manipulating convergent neuro-immune signaling
Gensel, J. C., Kigerl, K. A., Mandrekar-Colucci, S., Gaudet, A. D., & Popovich, P. G. (2012) · Cell and Tissue Research · doi:10.1007/s00441-012-1425-5 · Cited by 43 · see citing works
The challenges of long-distance axon regeneration in the injured CNS
Chew, D. J., Fawcett, J. W., & Andrews, M. R. (2012) · Progress in brain research · doi:10.1016/b978-0-444-59544-7.00013-5 · Cited by 43 · see citing works
Self-citationAxonal Localization of Integrins in the CNS Is Neuronal Type and Age Dependent
Andrews, M. R., Soleman, S., Cheah, M., Tumbarello, D. A., Mason, M. R. J., Moloney, E. B., Verhaagen, J., Bensadoun, J., Schneider, B. L., Aebischer, P., et al. (2016) · eNeuro · doi:10.1523/eneuro.0029-16.2016 · Cited by 42 · see citing works
Self-citationPetrova, V., & Eva, R. (2018) · Developmental Neurobiology · doi:10.1002/dneu.22608 · Cited by 41 · see citing works
Diverse functions of protein tyrosine phosphatase σ in the nervous and immune systems
Ohtake, Y., Saito, A., & Li, S. (2018) · Experimental Neurology · doi:10.1016/j.expneurol.2018.01.014 · Cited by 37 · see citing works
Zhang, Y., Chopp, M., Liu, X., Kassis, H., Wang, X., Li, C., An, G., & Zhang, Z. G. (2015) · Developmental Neurobiology · doi:10.1002/dneu.22292 · Cited by 35 · see citing works
DeVault, L., Li, T., Izabel, S., Thompson-Peer, K. L., Jan, L. Y., & Yn, J. (2018) · Genes & Development · doi:10.1101/gad.308270.117 · Cited by 35 · see citing works
Regulation of the E/I-balance by the neural matrisome
Mueller-Buehl, C., Wegrzyn, D., Bauch, J., & Faissner, A. (2023) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2023.1102334 · Cited by 32 · see citing works
Enhancing RPE Cell-Based Therapy Outcomes for AMD: The Role of Bruch's Membrane
Heller, J. P., & Martin, K. R. G. (2014) · Translational Vision Science & Technology · doi:10.1167/tvst.3.4.4 · Cited by 32 · see citing works
The diverse roles and multiple forms of focal adhesion kinase in brain
Armendariz, B. G., Masdeu, M., Soriano, E., Ureña, J. M., & Burgaya, F. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12737 · Cited by 32 · see citing works
Chondroitin sulfate proteoglycans from salmon nasal cartilage inhibit angiogenesis
Kobayashi, T., Kakizaki, I., Nozaka, H., & Nakamura, T. (2016) · Biochemistry and Biophysics Reports · doi:10.1016/j.bbrep.2016.11.009 · Cited by 32 · see citing works
Shida, M., Mikami, T., Tamura, J.-I., & Kitagawa, H. (2019) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2019.06.004 · Cited by 31 · see citing works
The Role of Perineuronal Nets in Physiology and Disease: Insights from Recent Studies
Auer, S., Schicht, M., Hoffmann, L., Budday, S., Frischknecht, R., Blümcke, I., & Paulsen, F. P. (2025) · Cells · doi:10.3390/cells14050321 · Cited by 30 · see citing works
β1-Integrin cytoskeletal signaling regulates sensory neuron response to matrix dimensionality
Ribeiro, A., Balasubramanian, S., Hughes, D. N., Vargo, S., Powell, E. M., & Leach, J. B. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.05.057 · Cited by 29 · see citing works
Guijarro-Belmar, A., Viskontas, M., Wei, Y., Bo, X., Shewan, D. A., & Huang, W. L. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.0374-19.2019 · Cited by 27 · see citing works
Integrin-α9β1 as a Novel Therapeutic Target for Refractory Diseases: Recent Progress and Insights
Xu, S., Zhang, T., Cao, Z., Zhong, W., Zhang, C., Li, H., & Song, J. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.638400 · Cited by 27 · see citing works
Kinesin KIF4A transports integrin β1 in developing axons of cortical neurons
Heintz, T. G., Heller, J. P., Zhao, R., Cáceres, A., Eva, R., & Fawcett, J. W. (2014) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2014.09.003 · Cited by 27 · see citing works
Self-citationPeptides and Astroglia Improve the Regenerative Capacity of Alginate Gels in the Injured Spinal Cord
Schackel, T., Kumar, P., Günther, M. I., Liu, S., Brunner, M., Sandner, B., Puttagunta, R., Müller, R., Weidner, N., & Blesch, A. (2018) · Tissue Engineering Part A · doi:10.1089/ten.tea.2018.0082 · Cited by 27 · see citing works
Secretion of a mammalian chondroitinase ABC aids glial integration at PNS/CNS boundaries
Warren, P. M., Andrews, M. R., Smith, M., Bartus, K., Bradbury, E., Verhaagen, J., Fawcett, J., & Kwok, J. C. F. (2020) · Scientific Reports · doi:10.1038/s41598-020-67526-0 · Cited by 21 · see citing works
Self-citationMungenast, L., Nieminen, R., Gaiser, C., Faia-Torres, A. B., Rühe, J., & Suter‐Dick, L. (2023) · Biomaterials and Biosystems · doi:10.1016/j.bbiosy.2023.100081 · Cited by 26 · see citing works
Full length talin stimulates integrin activation and axon regeneration
Tan, C. L., Kwok, J. C. F., Heller, J. P., Zhao, R., Eva, R., & Fawcett, J. W. (2015) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2015.03.011 · Cited by 25 · see citing works
Self-citationGlycosylation in Axonal Guidance
Mutalik, S. P., & Gupton, S. L. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22105143 · Cited by 25 · see citing works
Global Analysis of Neuronal Phosphoproteome Regulation by Chondroitin Sulfate Proteoglycans
Yu, P., Pisitkun, T., Wang, G., Wang, R., Katagiri, Y., Guček, M., Knepper, M. A., & Geller, H. M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0059285 · Cited by 25 · see citing works
Zhou, H., Li, X., Li, F., Liu, C., Liang, Z., Liu, S., Zhang, B., Wang, T., Chu, T., Lu, L., et al. (2014) · Brain Research · doi:10.1016/j.brainres.2014.08.048 · Cited by 24 · see citing works
Integrin Signaling in the Central Nervous System in Animals and Human Brain Diseases
Ikeshima-Kataoka, H., Sugimoto, C., & Tsubokawa, T. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23031435 · Cited by 24 · see citing works
Day, P., Alves, N., Daniell, E., Dasgupta, D., Ogborne, R., Steeper, A., Raza, M., Ellis, C., Fawcett, J. W., Keynes, R. J., et al. (2020) · PLoS ONE · doi:10.1371/journal.pone.0221851 · Cited by 23 · see citing works
Self-citationRetinal inputs signal astrocytes to recruit interneurons into visual thalamus
Su, J., Charalambakis, N., Sabbagh, U., Somaiya, R. D., Monavarfeshani, A., Guido, W., & Fox, M. A. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1913053117 · Cited by 23 · see citing works
da Costa, G., Ribeiro, F. F., Sebastião, A. M., Muir, E. M., & Vaz, S. H. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.1003145 · Cited by 22 · see citing works
Bidirectional remodeling of β1-integrin adhesions during chemotropic regulation of nerve growth
Carlstrom, L. P., Hines, J. H., Henle, S. J., & Henley, J. R. (2011) · BMC Biology · doi:10.1186/1741-7007-9-82 · Cited by 22 · see citing works
Bäumer, B. E., Kurz, A., Borrie, S. C., Sickinger, S., Dours-Zimmermann, M. T., Zimmermann, D. R., & Bandtlow, C. E. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.3094-13.2014 · Cited by 22 · see citing works
Intrinsic Mechanisms Regulating Axon Regeneration
Eva, R., Andrews, M. R., Franssen, E. H. P., & Fawcett, J. W. (2012) · International review of neurobiology · doi:10.1016/b978-0-12-407178-0.00004-1 · Cited by 22 · see citing works
Self-citationSakai, Y., Tsunekawa, M., Ohta, K., Shimizu, T., Pastuhov, S. I., Hanafusa, H., Hisamoto, N., & Matsumoto, K. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.2456-20.2021 · Cited by 22 · see citing works
The Extracellular Matrix in the Nervous System: The Good and the Bad Aspects
Vecino, E., & Kwok, J. C. F. (2016) · InTech eBooks · doi:10.5772/62527 · Cited by 21 · see citing works
Self-citationYao, M., Sun, H., Yuan, Q., Li, N., Li, H., Tang, Y., Leung, G., & Wu, W. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.10.035 · Cited by 20 · see citing works
Loers, G., Liao, Y., Hu, C., Xue, W., Shen, H., Zhao, W., & Schachner, M. (2019) · Scientific Reports · doi:10.1038/s41598-018-37685-2 · Cited by 20 · see citing works
Schweitzer, B., Singh, J., Fejtova, A., Groc, L., Heine, M., & Frischknecht, R. (2017) · Scientific Reports · doi:10.1038/s41598-017-07003-3 · Cited by 19 · see citing works
Clutching at Guidance Cues: The Integrin–FAK Axis Steers Axon Outgrowth
Davis-Lunn, M., Goult, B. T., & Andrews, M. R. (2023) · Biology · doi:10.3390/biology12070954 · Cited by 18 · see citing works
Wang, Y., Zhang, X., Tian, J., Shan, J., Hu, Y., Zhai, Y., & Guo, J. (2019) · The FASEB Journal · doi:10.1096/fj.201801949rr · Cited by 18 · see citing works
Regulation of Intracellular Structural Tension by Talin in the Axon Growth and Regeneration
Dingyu, W., Fanjie, M., Zhengzheng, D., Baosheng, H., Chao, Y., Yi, P., Wu, H., Guo, J., & Hu, G. (2015) · Molecular Neurobiology · doi:10.1007/s12035-015-9394-9 · Cited by 16 · see citing works
- Authors
- Tan, C. L., Kwok, J. C. F., Patani, R., ffrench-Constant, C., Chandran, S., & Fawcett, J. W.
- Affiliations
- University of Cambridge (GB)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2011-04-27
- Volume
- 31
- Issue
- 17
- Pages
- 6289-6295
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3116378
- OpenAlex
- W2068815747
- Cited by
- 160
- References
- 38
- Citations by year
- 2026: 3 · 2025: 8 · 2024: 1 · 2023: 5 · 2022: 7 · 2021: 12 · 2020: 10 · 2019: 10 · 2018: 16 · 2017: 7 · 2016: 8 · 2015: 13 · 2014: 19 · 2013: 12 · 2012: 19
- FWCI
- 7.94
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, other-oa)
- UCL Discovery (University College London) (submittedVersion)
- UEA Digital Repository (University of East Anglia) (submittedVersion)
- Funders
- Wellcome Trust
- British Heart Foundation (SP/10/003/28287)
- Motor Neurone Disease Association
- European Commission
- Henry Smith Charity
- John and Lucille Van Geest Foundation
- Medical Research Council
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nerve injury and regeneration
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Proteoglycans and glycosaminoglycans research
- Health Sciences › Medicine › Immunology and Allergy › Cell Adhesion Molecules Research
- Keywords
- integrin activation, chondroitin sulfate proteoglycans, axon regeneration, aggrecan, laminin, focal adhesion kinase, Src kinase, Nogo-A, sensory neurons, motor neurons, extracellular matrix, central nervous system injury, integrin signaling
- MeSH terms
- Animals, Antibodies, Axons, Cells, Cultured, Dose-Response Relationship, Drug, Drug Interactions, Ganglia, Spinal, Gene Expression Regulation, Humans, Male, Manganese, Neural Inhibition, Neurons, Chondroitin Sulfate Proteoglycans, Time Factors, Signal Transduction, Integrins, Rats, Sprague-Dawley, Chondroitin ABC Lyase, Lamins, Rats, Aggrecans
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
