Interleukin-1 receptor antagonist ameliorates the pain hypersensitivity, spinal inflammation and oxidative stress induced by systemic lipopolysaccharide in neonatal rats.


Journal

Neurochemistry international
ISSN: 1872-9754
Titre abrégé: Neurochem Int
Pays: England
ID NLM: 8006959

Informations de publication

Date de publication:
05 2020
Historique:
received: 15 09 2019
revised: 05 01 2020
accepted: 13 01 2020
pubmed: 29 1 2020
medline: 26 1 2021
entrez: 29 1 2020
Statut: ppublish

Résumé

Perinatal inflammation-induced reduction in pain threshold may alter pain sensitivity to hyperalgesia or allodynia which may persist into adulthood. In this study, we investigated the anti-inflammatory protective effect of interleukin-1 receptor antagonist (IL-1ra), an anti-inflammatory cytokine, on systemic lipopolysaccharide (LPS)-induced spinal cord inflammation and oxidative stress, thermal hyperalgesia, and mechanical allodynia in neonatal rats. Intraperitoneal (i.p.) injection of LPS (2 mg/kg) or sterile saline was performed in postnatal day 5 (P5) rat pups, and IL-1ra (100 mg/kg) or saline was administered (i.p.) 5 min after LPS injection. Pain reflex behavior, spinal cord inflammation and oxidative stress were examined 24 h after LPS administration. Systemic LPS exposure led to a reduction of tactile threshold in the von Frey filament tests (mechanical allodynia) and pain response latency in the tail-flick test (thermal hyperalgesia) of P6 neonatal rats. Spinal cord inflammation was indicated by the increased numbers of activated glial cells including microglia (Iba1+) and astrocytes (GFAP+), and elevated levels of pro-inflammatory cytokine interleukin-1β (IL-1β), cyclooxygenase-2 (COX-2), and prostaglandin E2 (PGE2) 24 h after LPS treatment. LPS treatment induced spinal oxidative stress as evidenced by the increase in thiobarbituric acid reactive substances (TBARS) content in the spinal cord. LPS exposure also led to a significant increase in oligodendrocyte lineage population (Olig2+) and mature oligodendrocyte cells (APC+) in the neonatal rat spinal cord. IL-1ra treatment significantly reduced LPS-induced effects including hyperalgesia, allodynia, the increased number of activated microglia, astrocytes and oligodendrocytes, and elevated levels of IL-1β, COX-2, PGE2, and lipid peroxidation (TBARS) in the neonatal rat spinal cord. These data suggest that IL-1ra provides a protective effect against the development of pain hypersensitivity, spinal cord inflammation and oxidative stress in the neonatal rats following LPS exposure, which may be associated with the blockade of LPS-induced pro-inflammatory cytokine IL-1β.

Identifiants

pubmed: 31987865
pii: S0197-0186(19)30517-0
doi: 10.1016/j.neuint.2020.104686
pmc: PMC7078012
mid: NIHMS1557955
pii:
doi:

Substances chimiques

Interleukin 1 Receptor Antagonist Protein 0
Lipopolysaccharides 0
Receptors, Interleukin-1 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

104686

Subventions

Organisme : NIGMS NIH HHS
ID : P20 GM121334
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS080844
Pays : United States

Informations de copyright

Copyright © 2020. Published by Elsevier Ltd.

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Auteurs

Cheng-Ta Hsieh (CT)

School of Medicine, Fu Jen Catholic University, New Taipei City, 24205, Taiwan; Division of Neurosurgery, Department of Surgery, Cathay General Hospital, Taipei, 10630, Taiwan; Department of Chemistry, Fu Jen Catholic University, New Taipei City, 24205, Taiwan; Graduate Institute of Biomedical and Pharmaceutical Science, Fu Jen Catholic University, New Taipei City, 24205, Taiwan.

Yih-Jing Lee (YJ)

School of Medicine, Fu Jen Catholic University, New Taipei City, 24205, Taiwan.

Jonathan W Lee (JW)

Department of Pediatrics, Division of Newborn Medicine, University of Mississippi Medical Center, Jackson, MS, 39216, USA.

Silu Lu (S)

Department of Pediatrics, Division of Newborn Medicine, University of Mississippi Medical Center, Jackson, MS, 39216, USA; Department of Neurology, University of Mississippi Medical Center, Jackson, MS, 39216, USA.

Michelle A Tucci (MA)

Department of Anesthesiology, University of Mississippi Medical Center, Jackson, MS, 39216, USA.

Xiaoli Dai (X)

Department of Anesthesiology, University of Mississippi Medical Center, Jackson, MS, 39216, USA.

Norma Beatriz Ojeda (NB)

Department of Pediatrics, Division of Newborn Medicine, University of Mississippi Medical Center, Jackson, MS, 39216, USA.

Hyun Joon Lee (HJ)

Department of Neurology, University of Mississippi Medical Center, Jackson, MS, 39216, USA; Research Services, G.V. (Sonny) Montgomery Veterans Administration Medical Center, Jackson, MS, 39216, USA.

Lir-Wan Fan (LW)

Department of Pediatrics, Division of Newborn Medicine, University of Mississippi Medical Center, Jackson, MS, 39216, USA.

Lu-Tai Tien (LT)

School of Medicine, Fu Jen Catholic University, New Taipei City, 24205, Taiwan. Electronic address: 068154@mail.fju.edu.tw.

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