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Receptor protein tyrosine phosphatase sigma inhibits axon regrowth in the adult injured CNS
Abstract
Recently, receptor protein tyrosine phosphatase-sigma (RPTPsigma) has been shown to inhibit axon regeneration in injured peripheral nerves. Unlike the peripheral nervous system (PNS), central nervous system (CNS) neurons fail to regenerate their axons after injury or in disease. In order to assess the role of RPTPsigma in CNS regeneration, we used the retinocollicular system of adult mice lacking RPTPsigma to evaluate retinal ganglion cell (RGC) axon regrowth after optic nerve lesion. Quantitative analysis demonstrated a significant increase in the number of RGC axons that crossed the glial scar and extended distally in optic nerves from RPTPsigma (-/-) mice compared to wild-type littermate controls. Although we found that RPTPsigma is expressed by adult RGCs in wild-type mice, the retinas and optic nerves of adult RPTPsigma (-/-) mice showed no histological defects. Furthermore, the time-course of RGC death after nerve lesion was not different between knockout and wild-type animals. Thus, enhanced axon regrowth in the absence of RPTPsigma could not be attributed to developmental defects or increased neuronal survival. Finally, we show constitutively elevated activity of mitogen-activated protein kinase (MAPK) and Akt kinase in adult RPTPsigma (-/-) mice retinas, suggesting that these signaling pathways may contribute to promoting RGC axon regrowth following traumatic nerve injury. Our results support a model in which RPTPsigma inhibits axon regeneration in the adult injured CNS.
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“RPTPσ can bind with high affinity to neurocan and aggrecan and strongly inhibits axon outgrowth and regeneration (Sapieha et al., 2005;Shen et al., 2009;Fry et al., 2010;Lang et al., 2015).”
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 Sapieha et al., 2005
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“In the CNS, loss of RPTPs has been reported to promote axon regeneration in the injured optic nerve (Sapieha et al. 2005) and to markedly improve axon extension into the lesion 12 Cite this article as Cold Spring Harb Perspect Biol 2010;2:a001867 penumbra following dorsal column crush injury (Shen…”
BackgroundProteoglycan-Specific Molecular Switch for RPTPσ Clustering and Neuronal Extension
Coles, C. H., Shen, Y., Tenney, A. P., Siebold, C., Sutton, G. C., Lu, W., Gallagher, J. T., Jones, E. Y., Flanagan, J. G., & Aricescu, A. R. (2011) · Science · doi:10.1126/science.1200840 · Cited by 320
Dissecting the Dual Role of the Glial Scar and Scar-Forming Astrocytes in Spinal Cord Injury
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“…leukocyte common antigenrelated (LAR), protein tyrosine phosphatase σ (PTPσ) and nogo receptors 1, 2, and 3 (NgR), CSPGs adhere to and immobilize regenerating axons to function as inhibitory factors (Sapieha et al., 2005; Schwab and Strittmatter, 2014; Lang et al., 2015; Dyck et al., 2018, 2019).”
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Scar-mediated inhibition and CSPG receptors in the CNS
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“Moreover, previous studies indicated enhanced regeneration of injured optic nerve and peripheral nerves in PTPσ knockout mice (Fry et al., 2010; McLean et al., 2002; Sapieha et al., 2005; Thompson et al., 2003).”
ResultExcitotoxic Death of Retinal NeuronsIn VivoOccurs via a Non-Cell-Autonomous Mechanism
Lebrun-Julien, F., Duplan, L., Pernet, V., Osswald, I. K., Sapieha, P. S., Bourgeois, P., Dickson, K. M., Bowie, D., Barker, P. A., & Polo, A. D. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0831-09.2009 · Cited by 191
“Fluorogold-positive retinal ganglion cells were counted in 12 retinal zones: three areas in each eye quadrant located at 0.5, 1.0, and 1.5 mm from the optic nerve head were examined (Sapieha et al., 2005), corresponding to a total area of 0.5 mm 2.”
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Structural genomics of protein phosphatases
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Brown, J. M., Xia, J., Zhuang, B., Cho, K.-S., Rogers, C. J., Gama, C. I., Rawat, M., Tully, S. E., Uetani, N., Mason, D. E., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1121318109 · Cited by 154
Self-citationPromoting optic nerve regeneration
Fischer, D., & Leibinger, M. (2012) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2012.06.005 · Cited by 152
“, 2009) and enhanced axonal regeneration beyond the glial scar in the optic nerve (Sapieha et al., 2005).”
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Mammalian Motoneuron Axon Targeting Requires Receptor Protein Tyrosine Phosphatases σ and δ
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“9% NaCl, which was applied to the superior colliculus as described (58).”
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Protein tyrosine phosphatase variants in human hereditary disorders and disease susceptibilities
Hendriks, W. J. A. J., & Pulido, R. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2013.05.022 · Cited by 117
Gene therapy and transplantation in CNS repair: The visual system
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Molecular mechanisms of scar-sourced axon growth inhibitors
Ohtake, Y., & Li, S. (2014) · Brain Research · doi:10.1016/j.brainres.2014.08.064 · Cited by 105
“Consistently, PTPσ knockout mice exhibited enhanced regeneration of injured optic nerve and peripheral nerves after injury (Fry et al., 2010; McLean et al., 2002; Sapieha et al., 2005; Thompson et al., 2003).”
BackgroundInhibition of p75NTR in glia potentiates TrkA-mediated survival of injured retinal ganglion cells
Lebrun-Julien, F., Morquette, B., Douillette, A., Saragovi, H. U., & Polo, A. D. (2008) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2008.12.005 · Cited by 99
Lost in the jungle: new hurdles for optic nerve axon regeneration
Pernet, V., & Schwab, M. E. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2014.05.002 · Cited by 87
Microenvironmental regulation of oligodendrocyte replacement and remyelination in spinal cord injury
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“…Ashii et al. 2012; Furusho et al. 2012), and lack of RPTP-σ or blockade of LAR has been shown to improve remyelination, axonal growth and functional recovery following SCI (McLean et al. 2002; Thompson et al. 2003; Sapeiha et al. 2005; Shen et al. 2009; Fry et al. 2010; Fisher et al. 2011) (Fig.”
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Silver, D. J., & Silver, J. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.03.016 · Cited by 85
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Advances in the Signaling Pathways Downstream of Glial-Scar Axon Growth Inhibitors
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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
“One of these, receptor protein tyrosine phosphatase sigma (PTP ), has been successfully targeted in experimental studies to promote axon regeneration in the optic nerve (196) and the spinal cord (197, 198).”
BackgroundUetani, N., Bertozzi, K., Chagnon, M. J., Hendriks, W. J. A. J., Tremblay, M. L., & Bouchard, M. (2009) · Journal of Clinical Investigation · doi:10.1172/jci37196 · Cited by 70
Self-citationExploring Optic Nerve Axon Regeneration
Li, H., Sun, Z.-L., Yang, X., Zhu, L., & Feng, D. (2017) · Current Neuropharmacology · doi:10.2174/1570159x14666161227150250 · Cited by 66
“Accordingly, neurons from PTPσ knockout mice displayed reduced sensitivity towards CSPGs in culture [102] and enhanced axonal regeneration beyond the glial scar in the ON [103].”
BackgroundMaintenance of Axo-Oligodendroglial Paranodal Junctions Requires DCC and Netrin-1
Jarjour, A. A., Bull, S.-J., Almasieh, M., Rajasekharan, S., Baker, K. A., Mui, J., Antel, J., Polo, A. D., & Kennedy, T. E. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.3285-08.2008 · Cited by 69
“The needle tip was inserted into the superior (dorsal) hemisphere of the eye, at the level of the pars plana, at a 45° angle through the sclera into the vitreous body as described previously (Sapieha et al., 2005).”
MethodSelf-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
“Deletion of PTP σ activates MAPK and Akt signals in adult mouse retinal cells 70 .”
Receptor protein tyrosine phosphatase sigma regulates synapse structure, function and plasticity
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LAR Receptor Tyrosine Phosphatase Family in Healthy and Diseased Brain
Cornejo, F., Cortés, B. I., Findlay, G. M., & Cancino, G. I. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.659951 · Cited by 54
“The same results were observed when axonal regeneration was evaluated after optic nerve injury, where the number of axons that cross the lesion site was higher in PTPRS deficient mice (Sapieha et al., 2005).”
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“9% NaCl, which was applied to both superior colliculi as described (Sapieha et al., 2005).”
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LAR Receptor Tyrosine Phosphatases and HSPGs Guide Peripheral Sensory Axons to the Skin
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Proteoglycans and axon guidance: a new relationship between old partners
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Dimerization of Protein Tyrosine Phosphatase σ Governs both Ligand Binding and Isoform Specificity
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“Although the role of ligand interactions is currently unclear, it is likely that they influence the biological functions of this phosphatase (6, 15, 33, 42, 44, 46, 49, 56, 60).”
BackgroundStrategies to neutralize RhoA/ROCK pathway after spinal cord injury
Roy, A., Pathak, Z., & Kumar, H. (2021) · Experimental Neurology · doi:10.1016/j.expneurol.2021.113794 · Cited by 39
Diverse functions of protein tyrosine phosphatase σ in the nervous and immune systems
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“Consistently, PTPσ knockout mice exhibited enhanced regeneration of optic nerve and peripheral nerve after injury (McLean et al., 2002; Sapieha et al., 2005; Thompson et al., 2003).”
InfluentialMolecular approaches for spinal cord injury treatment
Martinez, A. B., de Almeida, F. M., Marques, S. A., dos Santos, A. R., Prins, C. A., Cardoso, F. S. D. S., Heringer, L. D. S., & Mendonça, H. R. (2022) · Neural Regeneration Research · doi:10.4103/1673-5374.344830 · Cited by 43
“CSPG signals through different receptors, such as LAR, protein tyrosine phosphatase σ (PTPσ) and NgR 1, 2, and 3 (Sapieha et al., 2005; Schwab and Strittmatter, 2014; Lang et al., 2015; Dyck et al., 2018, 2019).”
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Duan, Y., & Giger, R. J. (2010) · Science Signaling · doi:10.1126/scisignal.3110pe6 · Cited by 34
Mechanisms of PTPσ-Mediated Presynaptic Differentiation
Bomkamp, C., Padmanabhan, N., Karimi, B., Ge, Y., Chao, J. T., Loewen, C. J. R., Siddiqui, T. J., & Craig, A. M. (2019) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2019.00017 · Cited by 32
“This is exemplified by the first discovered and best known pair of synaptic organizing proteins, the postsynaptic neuroligins (Scheiffele et al., 2000) and the presynaptic neurexins (Graf et al., 2004).”
BackgroundNeuroprotection and regeneration in glaucoma.
Levin, L. A. (2005) · PubMed · doi:10.1016/j.ohc.2005.07.001 · Cited by 30
“For example, upregulation of cAMP allows regeneration of spinal cord [54,55] and retinal ganglion cell [56] axons, and mice lacking receptor protein tyrosine phosphatase sigma have increased retinal ganglion cell axon regeneration past a glial scar [57].”
RPTPs in axons, synapses and neurology
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Protein Tyrosine Phosphatase σ in Proteoglycan-Mediated Neural Regeneration Regulation
Chien, P. N., & Ryu, S. E. (2012) · Molecular Neurobiology · doi:10.1007/s12035-012-8346-x · Cited by 26
“However, the similar lesion or injury in PTPσ knockout mice does not show the inhibition, resulting in the regeneration of long distance axons [36–39] (Fig.”
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“It is abundantly expressed in both the developing and mature mammalian nervous systems,(16) acting to inhibit axon growth and slow axon regeneration.(14,17)”
BackgroundNB‐3 signaling mediates the cross‐talk between post‐traumatic spinal axons and scar‐forming cells
Huang, Z., Gao, Y., Sun, Y., Zhang, C., Yin, Y., Shimoda, Y., Watanabe, K., & Liu, Y. (2016) · The EMBO Journal · doi:10.15252/embj.201593460 · Cited by 22
“Loss of PTP r enhances regeneration in sciatic, facial, optic, and corticospinal axons after injury (McLean et al , 2002; Thompson et al , 2003; Sapieha et al , 2005; Shen et al , 2009; Fry et al , 2010), although the mechanism remains unclear.”
Martin, K. R., Narang, P., Xu, Y., Kauffman, A. L., Petit, J. L., Xu, H. E., Meurice, N., & MacKeigan, J. P. (2012) · PLoS ONE · doi:10.1371/journal.pone.0050217 · Cited by 20
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Traffic lights for axon growth: proteoglycans and their neuronal receptors
Shen, Y. (2014) · Neural Regeneration Research · doi:10.4103/1673-5374.128236 · Cited by 19
“…are now increasingly recognized as key regulators of post-injury axonal plasticity (Xie et al., 2001; McLean et al., 2002; Thompson, 2003; Van der Zee et al., 2003; Sapieha et al., 2005; Shen et al., 2009; Fry et al., 2010; Fisher et al., 2011; Takahashi et al., 2012; Gardner and Habecker, 2013).”
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Small Molecules Targeting PTPσ–Trk Interactions Promote Sympathetic Nerve Regeneration
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Integrating virtual and biochemical screening for protein tyrosine phosphatase inhibitor discovery
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“Initially, genetic deletion of PTPσ was found to diminish neuronal sensitivity toward CSPGs and comprehensively enabled regenerative RGC axons to penetrate the glial scar at the lesion sites [120, 130].”
BackgroundAstrogliosis and Axonal Regeneration
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“In contrast, RPTPσ, which closely resembles LAR, has been shown to slow axon regeneration after peripheral nerve injury and to inhibit axon regeneration following facial and optic nerve crush (Thompson et al., 2003; Sapieha et al., 2005).”
BackgroundRodemer, W., Zhang, G., Sinitsa, I., Hu, J., Jin, L., Li, S., & Selzer, M. E. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.00061 · Cited by 9
“For example, following optic nerve crush, PTPσ deletion reportedly improved axon regeneration but did not prevent retinal ganglion cell death (Sapieha et al., 2005).”
BackgroundERG responses to high-frequency flickers require FAT3 signaling in mouse retinal bipolar cells
Avilés, E. C., Wang, S. K., Patel, S., Cordero, S., Shi, S., Lin, L., Kefalov, V. J., Goodrich, L. V., Cepko, C. L., & Xue, Y. (2025) · The Journal of General Physiology · doi:10.1085/jgp.202413642 · Cited by 9
“This might also explain why Ptprs mutants have no obvious changes in retinal lamination (Sapieha et al., 2005).”
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Identification of novel protein tyrosine phosphatase sigma inhibitors promoting neurite extension
Lee, H. S., Ku, B., Park, T. H., Park, H., Choi, J., Chang, K., Kim, C., Ryu, S. E., & Kim, S. J. (2015) · Bioorganic & Medicinal Chemistry Letters · doi:10.1016/j.bmcl.2015.11.026 · Cited by 8
Awakening the stalled axon — Surprises in CSPG gradients
Lee, S. J., Kalinski, A. L., & Twiss, J. L. (2014) · Experimental Neurology · doi:10.1016/j.expneurol.2013.12.025 · Cited by 6
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“The rate of surviving RGCs reported in the present study is in agreement with previous studies [14].”
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“Injury to adult brain neurons often results in cell death as mature neurons lack the capacity for self-repair [1–3].”
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“…these measures cannot rebuild the visual pathway and restore visual functions (Fischer et al., 2004; Gaub et al., 2011; Leon et al., 2000; Lu et al., 2020; Moore et al., 2009; Park et al., 2008; Sapieha et al., 2005; So and Aguayo, 1985; Sun et al., 2011; Yin et al., 2003; You et al., 2016).”
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“It is also noteworthy that, unrelated to TrkC activity, PTPsigma also regulates axonal growth after injury and inhibits axon regeneration (Sapieha et al., 2005; Thompson et al., 2003).”
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“In this regard, a line of experimental evidence indicated the involvement of PTPr in mediating the inhibitory role of CSPG in neural regeneration (Shen et al., 2009; Sapieha et al., 2005; McLean et al., 2002).”
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Self-citationProtein Tyrosine Phosphatase Receptor Type S (PTPRS) Regulates Hematopoietic Stem
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Spinal Cord and Peripheral Nerve Regeneration Current Research and Future Possibilities
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Glypican-1 modulates CSPG inhibition on growing axons
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Metadata
- Authors
- Sapieha, P. S., Duplan, L., Uetani, N., Joly, S., Tremblay, M. L., Kennedy, T. E., & Di Polo, A.
- Affiliations
- Université de Montréal (CA)
- McGill University (CA)
- Montreal Neurological Institute and Hospital (CA)
- Venue
- Molecular and Cellular Neuroscience
- Publisher
- Elsevier BV
- Published
- 2005-04
- Volume
- 28
- Issue
- 4
- Pages
- 625-635
- ISSN
- 1044-7431 (ISSN-L)
- OpenAlex
- W2092811972
- Cited by
- 106
- References
- 76
- Citations by year
- 2025: 3 · 2024: 1 · 2023: 3 · 2022: 4 · 2021: 3 · 2020: 7 · 2019: 3 · 2018: 2 · 2017: 4 · 2016: 5 · 2015: 10 · 2014: 15 · 2013: 6 · 2012: 10
- FWCI
- 1.45
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Molecular and Cellular Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Canadian Institutes of Health Research
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nerve injury and regeneration
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
- Health Sciences › Medicine › Ophthalmology › Glaucoma and retinal disorders
- Keywords
- axon regeneration, optic nerve injury, retinal ganglion cells, glial scar, mitogen-activated protein kinase, Akt kinase, knockout mice
- MeSH terms
- Animals, Axons, Female, Mice, Inbred BALB C, Nerve Regeneration, Neural Inhibition, Retinal Ganglion Cells, Protein Tyrosine Phosphatases, Mice, Knockout, Optic Nerve Injuries, Mice, Receptor-Like Protein Tyrosine Phosphatases, Class 2
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