Schwann cell transient receptor potential ankyrin 1 (TRPA1) ortholog in zebrafish larvae mediates chemotherapy-induced peripheral neuropathy

IF 6.8 2区 医学 Q1 PHARMACOLOGY & PHARMACY British Journal of Pharmacology Pub Date : 2024-09-05 DOI:10.1111/bph.17318
Elisa Bellantoni, Matilde Marini, Martina Chieca, Chiara Gabellini, Erica Lucia Crapanzano, Daniel Souza Monteiro de Araujo, Daniele Nosi, Lorenzo Roschi, Lorenzo Landini, Gaetano De Siena, Pasquale Pensieri, Alessandra Mastricci, Irene Scuffi, Pierangelo Geppetti, Romina Nassini, Francesco De Logu
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Abstract

Background and Purpose

The oxidant sensor transient receptor potential ankyrin 1 (TRPA1) channel expressed by Schwann cells (SCs) has recently been implicated in several models of neuropathic pain in rodents. Here we investigate whether the pro-algesic function of Schwann cell TRPA1 is not limited to mammals by exploring the role of TRPA1 in a model of chemotherapy-induced peripheral neuropathy (CIPN) in zebrafish larvae.

Experimental Approach

We used zebrafish larvae and a mouse model to test oxaliplatin-evoked nociceptive behaviours. We also performed a TRPA1 selective silencing in Schwann cells both in zebrafish larvae and mice to study their contribution in oxaliplatin-induced CIPN model.

Key Results

We found that zebrafish larvae and zebrafish TRPA1 (zTRPA1)-transfected HEK293T cells respond to reactive oxygen species (ROS) with nociceptive behaviours and intracellular calcium increases, respectively. TRPA1 was found to be co-expressed with the Schwann cell marker, SOX10, in zebrafish larvae. Oxaliplatin caused nociceptive behaviours in zebrafish larvae that were attenuated by a TRPA1 antagonist and a ROS scavenger. Oxaliplatin failed to produce mechanical allodynia in mice with Schwann cell TRPA1 selective silencing (Plp1+-Trpa1 mice). Comparable results were observed in zebrafish larvae where TRPA1 selective silencing in Schwann cells, using the specific Schwann cell promoter myelin basic protein (MBP), attenuated oxaliplatin-evoked nociceptive behaviours.

Conclusion and Implications

These results indicate that the contribution of the oxidative stress/Schwann cell/TRPA1 pro-allodynic pathway to neuropathic pain models seems to be conserved across the animal kingdom.

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斑马鱼幼体中的许旺细胞瞬时受体电位蛋白1(TRPA1)同源物介导化疗引起的周围神经病变
背景和目的:最近,许旺细胞(SC)表达的氧化剂传感器瞬时受体电位蛋白1(TRPA1)通道与啮齿类动物的几种神经病理性疼痛模型有关。在此,我们通过探索 TRPA1 在斑马鱼幼体化疗诱导周围神经病变(CIPN)模型中的作用,研究许旺细胞 TRPA1 的促痛觉功能是否不仅限于哺乳动物:实验方法:我们使用斑马鱼幼体和小鼠模型来测试奥沙利铂诱发的痛觉行为。我们还在斑马鱼幼体和小鼠的许旺细胞中进行了 TRPA1 选择性沉默,以研究它们在奥沙利铂诱导的 CIPN 模型中的贡献:我们发现斑马鱼幼体和斑马鱼TRPA1(zTRPA1)转染的HEK293T细胞对活性氧(ROS)的反应分别是痛觉行为和细胞内钙增加。研究发现,在斑马鱼幼体中,TRPA1与许旺细胞标记物SOX10共同表达。奥沙利铂在斑马鱼幼体中引起痛觉行为,TRPA1拮抗剂和ROS清除剂可减轻这种行为。在许旺细胞 TRPA1 选择性沉默的小鼠(Plp1+-Trpa1 小鼠)中,奥沙利铂不能产生机械异感。在斑马鱼幼体中也观察到了类似的结果,使用特定的许旺细胞启动子髓鞘碱性蛋白(MBP)选择性沉默许旺细胞中的TRPA1,可减轻奥沙利铂诱发的痛觉行为:这些结果表明,氧化应激/许旺细胞/TRPA1 促变态反应途径对神经病理性疼痛模型的作用似乎在整个动物界都是一致的。
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来源期刊
CiteScore
15.40
自引率
12.30%
发文量
270
审稿时长
2.0 months
期刊介绍: The British Journal of Pharmacology (BJP) is a biomedical science journal offering comprehensive international coverage of experimental and translational pharmacology. It publishes original research, authoritative reviews, mini reviews, systematic reviews, meta-analyses, databases, letters to the Editor, and commentaries. Review articles, databases, systematic reviews, and meta-analyses are typically commissioned, but unsolicited contributions are also considered, either as standalone papers or part of themed issues. In addition to basic science research, BJP features translational pharmacology research, including proof-of-concept and early mechanistic studies in humans. While it generally does not publish first-in-man phase I studies or phase IIb, III, or IV studies, exceptions may be made under certain circumstances, particularly if results are combined with preclinical studies.
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