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Targeted up-regulation of Drp1 in dorsal horn attenuates neuropathic pain hypersensitivity by increasing mitochondrial fission

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Zhang, Kun-Long, Li, Shu-Jiao, Pu, Xue-Yin, Wu, Fei-Fei, Liu, Hui, Wang, Rui-Qing, Liu, Bo-Zhi, Li, Ze +5 more·2022·Redox Biology
DOI 10.1016/j.redox.2021.102216PMC PMC8718665
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Abstract

Mitochondria play an essential role in pathophysiology of both inflammatory and neuropathic pain (NP), but the mechanisms are not yet clear. Dynamin-related protein 1 (Drp1) is broadly expressed in the central nervous system and plays a role in the induction of mitochondrial fission process. Spared nerve injury (SNI), due to the dysfunction of the neurons within the spinal dorsal horn (SDH), is the most common NP model. We explored the neuroprotective role of Drp1 within SDH in SNI. SNI mice showed pain behavior and anxiety-like behavior, which was associated with elevation of Drp1, as well as increased density of mitochondria in SDH. Ultrastructural analysis showed SNI induced damaged mitochondria into smaller perimeter and area, tending to be circular. Characteristics of vacuole in the mitochondria further showed SNI induced the increased number of vacuole, widened vac-perimeter and vac-area. Stable overexpression of Drp1 via AAV under the control of the Drp1 promoter by intraspinal injection (Drp1 OE) attenuated abnormal gait and alleviated pain hypersensitivity of SNI mice. Mitochondrial ultrastructure analysis showed that the increased density of mitochondria induced by SNI was recovered by Drp1 OE which, however, did not change mitochondrial morphology and vacuole parameters within SDH. Contrary to Drp1 OE, down-regulation of Drp1 in the SDH by AAV-Drp1 shRNA (Drp1 RNAi) did not alter painful behavior induced by SNI. Ultrastructural analysis showed the treatment by combination of SNI and Drp1 RNAi (SNI + Drp1 RNAi) amplified the damages of mitochondria with the decreased distribution density, increased perimeter and area, as well as larger circularity tending to be more circular. Vacuole data showed SNI + Drp1 RNAi increased vacuole density, perimeter and area within the SDH mitochondria. Our results illustrate that mitochondria within the SDH are sensitive to NP, and targeted mitochondrial Drp1 overexpression attenuates pain hypersensitivity. Drp1 offers a novel therapeutic target for pain treatment.

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Authors
Zhang, K.-L., Li, S.-J., Pu, X.-Y., Wu, F.-F., Liu, H., Wang, R.-Q., Liu, B.-Z., Li, Z., Li, K.-F., Qian, N.-S., Yang, Y.-L., Yuan, H., & Wang, Y.-Y.
Affiliations
  • Xijing Hospital (CN)
  • Air Force Medical University (CN)
  • Yan'an University (CN)
Corresponding author
Yuan, Hua
ORCID
Venue
Redox Biology
Publisher
Elsevier BV
Published
2022-02
Volume
49
Pages
102216
ISSN
2213-2317 (ISSN-L)
DOI
10.1016/j.redox.2021.102216
PMC
PMC8718665
OpenAlex
W4200546049
Cited by
52
References
2
Citations by year
2026: 12 · 2025: 17 · 2024: 16 · 2023: 6 · 2022: 1
FWCI
3.67
Type
journal article
Language
en
Update notices
erratum (2022-04-01)
Open access
Licence
Locations
  • Redox Biology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Topics
  • Health Sciences › Medicine › Physiology › Pain Mechanisms and Treatments
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
  • Health Sciences › Medicine › Anesthesiology and Pain Medicine › Pain Management and Treatment
Keywords
Drp1, mitochondrial fission, neuropathic pain, dorsal horn, spared nerve injury, mitochondrial ultrastructure, neuroprotection, hyperalgesia, anxiety-like behavior, AAV gene delivery
MeSH terms
Animals, Neuralgia, Up-Regulation, Rats, Sprague-Dawley, Dynamins, Mice, Rats, Mitochondrial Dynamics, Spinal Cord Dorsal Horn

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