Cited by 185Nerve injury and regenerationSpinal Cord Injury ResearchProteoglycans and glycosaminoglycans research

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Increased chondroitin sulfate proteoglycan expression in denervated brainstem targets following spinal cord injury creates a barrier to axonal regeneration overcome by chondroitinase ABC and neurotrophin-3.

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Massey, James M., Amps, Jeremy, Viapiano, Mariano S., Matthews, Russell T., Wagoner, Michelle R., Whitaker, Christopher M., Alilain, Warren, Yonkof, Alicia L., Khalyfa, Abdelnaby, Cooper, Nigel G.F., Silver, Jerry, Onifer, Stephen M.·2008·Experimental Neurology

DOI 10.1016/j.expneurol.2007.03.029PMC PMC2270474

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Abstract

Increased chondroitin sulfate proteoglycan (CSPG) expression in the vicinity of a spinal cord injury (SCI) is a primary participant in axonal regeneration failure. However, the presence of similar increases of CSPG expression in denervated synaptic targets well away from the primary lesion and the subsequent impact on regenerating axons attempting to approach deafferented neurons have not been studied. Constitutively expressed CSPGs within the extracellular matrix and perineuronal nets of the adult rat dorsal column nuclei (DCN) were characterized using real-time PCR, Western blot analysis and immunohistochemistry. We show for the first time that by 2 days and through 3 weeks following SCI, the levels of NG2, neurocan and brevican associated with reactive glia throughout the DCN were dramatically increased throughout the DCN despite being well beyond areas of trauma-induced blood brain barrier breakdown. Importantly, regenerating axons from adult sensory neurons microtransplanted 2 weeks following SCI between the injury site and the DCN were able to regenerate rapidly within white matter (as shown previously by Davies et al. [Davies, S.J., Goucher, D.R., Doller, C., Silver, J., 1999. Robust regeneration of adult sensory axons in degenerating white matter of the adult rat spinal cord. J. Neurosci. 19, 5810-5822]) but were unable to enter the denervated DCN. Application of chondroitinase ABC or neurotrophin-3-expressing lentivirus in the DCN partially overcame this inhibition. When the treatments were combined, entrance by regenerating axons into the DCN was significantly augmented. These results demonstrate both an additional challenge and potential treatment strategy for successful functional pathway reconstruction after SCI.

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See all 185

Authors: Massey, J. M., Amps, J., Viapiano, M. S., Matthews, R. T., Wagoner, M. R., Whitaker, C. M., Alilain, W., Yonkof, A. L., Khalyfa, A., Cooper, N. G. F., Silver, J., & Onifer, S. M.
Affiliations: University of Louisville (US)
Case Western Reserve University (US)
Yale University (US)
Corresponding author: Onifer, Stephen M.
ORCID: Viapiano, Mariano S.
Matthews, Russell T.
Alilain, Warren
Khalyfa, Abdelnaby
Cooper, Nigel G.F.
Silver, Jerry
Onifer, Stephen M.
Venue: Experimental Neurology
Publisher: Elsevier BV
Published: 2008-02
Volume: 209
Issue: 2
Pages: 426-445
ISSN: 0014-4886 (ISSN-L)
DOI: 10.1016/j.expneurol.2007.03.029
PMC: PMC2270474
OpenAlex: W1998297893
Cited by: 185
References: 114
Citations by year: 2026: 7 · 2025: 3 · 2024: 4 · 2023: 8 · 2022: 7 · 2021: 10 · 2020: 6 · 2019: 8 · 2018: 9 · 2017: 3 · 2016: 5 · 2015: 7 · 2014: 15 · 2013: 15 · 2012: 15
FWCI: 5.29
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Experimental Neurology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health (NS25713, NS40411, RR15576, RR16481)
Office of Experimental Program to Stimulate Competitive Research (EPS-9874764)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nerve injury and regeneration
Health Sciences › Medicine › Clinical Neurology › Spinal Cord Injury Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Proteoglycans and glycosaminoglycans research
Keywords: chondroitin sulfate proteoglycans, spinal cord injury, axon regeneration, denervation, dorsal column nuclei, chondroitinase ABC, neurotrophin-3, NG2, neurocan, brevican, perineuronal nets, sensory neurons, white matter, reactive glia
MeSH terms: Chondroitin Sulfate Proteoglycan 4, Animals, Antigens, Brain Stem, Cholera Toxin, Disease Models, Animal, Extracellular Matrix, Ganglia, Spinal, Gene Expression Regulation, Genetic Vectors, Male, Nerve Tissue Proteins, Chondroitin Sulfate Proteoglycans, Proteoglycans, Random Allocation, Spinal Cord Injuries, Time Factors, Genetic Therapy, Rats, Sprague-Dawley, Cell Transplantation, Chondroitin ABC Lyase, Neurotrophin 3, Rats

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Increased chondroitin sulfate proteoglycan expression in denervated brainstem targets following spinal cord injury creates a barrier to axonal regeneration overcome by chondroitinase ABC and neurotrophin-3.

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