Perineural expression of high-mobility group box-1 contributes to long-lasting mechanical hypersensitivity via matrix metalloprotease-9 up-regulation in mice with painful peripheral neuropathy

Fang Fang Zhang, Norimitsu Morioka, Sakura Harano, Yoki Nakamura, Keyue Liu, Masahiro Nishibori, Kazue Hisaoka-Nakashima, Yoshihiro Nakata

Research output: Contribution to journalArticle

13 Citations (Scopus)

Abstract

High-mobility group box-1 (HMGB1) has been shown to be critical in the modulation of nociceptive transduction following a peripheral neuropathy. However, the precise role of peripherally expressed HMGB1 in neuropathic pain has yet to be fully elaborated. Following a partial sciatic nerve ligation (PSNL) in mice, a persistent ipsilateral up-regulation of HMGB1 was observed from 3 to 21 days after PSNL, in paralleled with a robust ipsilateral hind paw mechanical hypersensitivity. Increased HMGB1 was detected in both infiltrating macrophages and proliferating Schwann cells in the ipsilateral nerve 14 days following PSNL. Repeated perineural treatment with anti-HMGB1 antibody significantly ameliorated PSNL-induced mechanical hypersensitivity. Several pronociceptive molecules, including matrix metalloprotease-9 (MMP-9), tumor necrosis factor-α, interleukin-1β (IL-1β), and cyclooxygenase-2, were up-regulated in injured sciatic nerve 14 days following PSNL. Repeated perineural treatment with an anti-HMGB1 antibody significantly suppressed expression of MMP-9, but not other pronociceptive molecules. Perineural treatment with a selective MMP-9 inhibitor ameliorated PSNL-induced mechanical hypersensitivity. The current findings demonstrate that the maintenance of the neuropathic state following an injured nerve is dependent on the up-regulation of HMGB1 and MMP-9. Thus, blocking HMGB1 function in sciatic nerve could be a potent therapeutic strategy for the treatment of neuropathic pain. Increased peripheral high-mobility group box-1 (HMGB1) is involved in the modulation of nociceptive transduction following a peripheral neuropathy. Following nerve injury in mice, increased HMGB1 is detected in both infiltrating macrophages and proliferating Schwann cells in the ipsilateral nerve. Repeated perineural treatment with anti-HMGB1 antibody significantly ameliorates nerve injury-induced mechanical hypersensitivity, and suppresses expression of matrix metalloprotease-9 (MMP-9). The findings demonstrate that the maintenance of the neuropathic state following an injury nerve is dependent on the up-regulation of HMGB1 and MMP-9. Increased peripheral high-mobility group box-1 (HMGB1) is involved in the modulation of nociceptive transduction following a peripheral neuropathy. Following nerve injury in mice, increased HMGB1 is detected in both infiltrating macrophages and proliferating Schwann cells in the ipsilateral nerve. Repeated perineural treatment with anti-HMGB1 antibody significantly ameliorates nerve injury-induced mechanical hypersensitivity, and suppresses expression of matrix metalloprotease-9 (MMP-9). The findings demonstrate that the maintenance of the neuropathic state following an injury nerve is dependent on the up-regulation of HMGB1 and MMP-9.

Original languageEnglish
Pages (from-to)837-850
Number of pages14
JournalJournal of Neurochemistry
Volume136
Issue number4
DOIs
Publication statusPublished - Feb 1 2016

Fingerprint

Metalloproteases
Peripheral Nervous System Diseases
Sciatic Nerve
Hypersensitivity
Up-Regulation
Ligation
Macrophages
Schwann Cells
Wounds and Injuries
Antibodies
Cells
Maintenance
Modulation
Neuralgia
Therapeutics
Molecules
Painful Neuropathy
Cyclooxygenase 2
Interleukin-1
Tumor Necrosis Factor-alpha

Keywords

  • Allodynia
  • anti-HMGB1 monoclonal antibody
  • HMGB1
  • MMP-9
  • sciatic nerve

ASJC Scopus subject areas

  • Biochemistry
  • Cellular and Molecular Neuroscience

Cite this

Perineural expression of high-mobility group box-1 contributes to long-lasting mechanical hypersensitivity via matrix metalloprotease-9 up-regulation in mice with painful peripheral neuropathy. / Zhang, Fang Fang; Morioka, Norimitsu; Harano, Sakura; Nakamura, Yoki; Liu, Keyue; Nishibori, Masahiro; Hisaoka-Nakashima, Kazue; Nakata, Yoshihiro.

In: Journal of Neurochemistry, Vol. 136, No. 4, 01.02.2016, p. 837-850.

Research output: Contribution to journalArticle

Zhang, Fang Fang ; Morioka, Norimitsu ; Harano, Sakura ; Nakamura, Yoki ; Liu, Keyue ; Nishibori, Masahiro ; Hisaoka-Nakashima, Kazue ; Nakata, Yoshihiro. / Perineural expression of high-mobility group box-1 contributes to long-lasting mechanical hypersensitivity via matrix metalloprotease-9 up-regulation in mice with painful peripheral neuropathy. In: Journal of Neurochemistry. 2016 ; Vol. 136, No. 4. pp. 837-850.
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AU - Harano, Sakura

AU - Nakamura, Yoki

AU - Liu, Keyue

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AU - Hisaoka-Nakashima, Kazue

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KW - Allodynia

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KW - MMP-9

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