Michael Morgan , Vida Nazemian , Jenny Thai , Irene Lin , Susan Northfield , Jason J. Ivanusic
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We found that: 1) TrkB is expressed in myelinated medium diameter neurons that innervate the knee joint and bone in naïve animals; 2) peripheral application of BDNF increases the sensitivity of Aδ, but not C knee joint and bone afferent neurons, in response to mechanical stimulation, in naïve animals; 3) BDNF expression increases in synovial tissue in early MIA-induced OA, when pathology is confined to the joint, and in the subchondral bone in late MIA-induced OA, when there is additional damage to the surrounding bone; and 4) TrkB inhibition reverses MIA-induced changes in the sensitivity of Aδ but not C knee joint afferent neurons early in MIA-induced OA, and Aδ but not C bone afferent neurons late in MIA-induced OA. Our findings suggest that BDNF/TrkB signaling may have a role to play in the pathogenesis of OA pain, through effects on knee joint afferent neurons early in disease when there is inflammation confined to the joint, and bone afferent neurons late in disease when there is involvement of damage to subchondral bone. Targeted manipulation of BDNF/TrkB signaling may provide therapeutic benefit for the management of OA pain.</div></div>","PeriodicalId":9301,"journal":{"name":"Bone","volume":"189 ","pages":"Article 117260"},"PeriodicalIF":3.5000,"publicationDate":"2024-09-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"BDNF sensitizes bone and joint afferent neurons at different stages of MIA-induced osteoarthritis\",\"authors\":\"Michael Morgan , Vida Nazemian , Jenny Thai , Irene Lin , Susan Northfield , Jason J. Ivanusic\",\"doi\":\"10.1016/j.bone.2024.117260\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<div><div>There is emerging evidence that Brain Derived Neurotrophic Factor (BDNF), and one of its receptors TrkB, play important roles in the pathogenesis of osteoarthritis (OA) pain. Whilst these studies clearly highlight the potential for targeting BDNF/TrkB signaling to treat OA pain, the mechanism for how BDNF/TrkB signaling contributes to OA pain remains unclear. In this study, we used an animal model of mono-iodoacetate (MIA)-induced OA, in combination with electrophysiology, behavioral testing, Western blot analysis, and retrograde tracing and immunohistochemistry, to identify roles for BDNF/TrkB signaling in the pathogenesis of OA pain. We found that: 1) TrkB is expressed in myelinated medium diameter neurons that innervate the knee joint and bone in naïve animals; 2) peripheral application of BDNF increases the sensitivity of Aδ, but not C knee joint and bone afferent neurons, in response to mechanical stimulation, in naïve animals; 3) BDNF expression increases in synovial tissue in early MIA-induced OA, when pathology is confined to the joint, and in the subchondral bone in late MIA-induced OA, when there is additional damage to the surrounding bone; and 4) TrkB inhibition reverses MIA-induced changes in the sensitivity of Aδ but not C knee joint afferent neurons early in MIA-induced OA, and Aδ but not C bone afferent neurons late in MIA-induced OA. Our findings suggest that BDNF/TrkB signaling may have a role to play in the pathogenesis of OA pain, through effects on knee joint afferent neurons early in disease when there is inflammation confined to the joint, and bone afferent neurons late in disease when there is involvement of damage to subchondral bone. Targeted manipulation of BDNF/TrkB signaling may provide therapeutic benefit for the management of OA pain.</div></div>\",\"PeriodicalId\":9301,\"journal\":{\"name\":\"Bone\",\"volume\":\"189 \",\"pages\":\"Article 117260\"},\"PeriodicalIF\":3.5000,\"publicationDate\":\"2024-09-17\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Bone\",\"FirstCategoryId\":\"3\",\"ListUrlMain\":\"https://www.sciencedirect.com/science/article/pii/S8756328224002497\",\"RegionNum\":2,\"RegionCategory\":\"医学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q2\",\"JCRName\":\"ENDOCRINOLOGY & METABOLISM\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Bone","FirstCategoryId":"3","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S8756328224002497","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"ENDOCRINOLOGY & METABOLISM","Score":null,"Total":0}
引用次数: 0
摘要
越来越多的证据表明,脑源性神经营养因子(BDNF)及其受体之一TrkB在骨关节炎(OA)疼痛的发病机制中发挥着重要作用。虽然这些研究明确强调了靶向 BDNF/TrkB 信号转导治疗 OA 疼痛的潜力,但 BDNF/TrkB 信号转导如何导致 OA 疼痛的机制仍不清楚。在这项研究中,我们利用单碘醋酸(MIA)诱导的 OA 动物模型,结合电生理学、行为测试、Western 印迹分析、逆行追踪和免疫组织化学,确定了 BDNF/TrkB 信号在 OA 疼痛发病机制中的作用。我们发现1)TrkB表达于神经支配膝关节和骨的髓鞘中径神经元中;2)在外周应用BDNF可增加膝关节和骨传入神经元Aδ对机械刺激的敏感性,但不能增加C传入神经元对机械刺激的敏感性;3)在 MIA 引起的 OA 早期,滑膜组织中的 BDNF 表达增加,此时病变仅限于关节;在 MIA 引起的 OA 晚期,软骨下骨中的 BDNF 表达增加,此时周围骨质受到额外损伤;4)TrkB抑制可逆转MIA诱导的Aδ膝关节传入神经元(而非C膝关节传入神经元)在MIA诱导的OA早期的敏感性变化,以及Aδ骨传入神经元(而非C骨传入神经元)在MIA诱导的OA晚期的敏感性变化。我们的研究结果表明,当炎症局限于关节时,BDNF/TrkB 信号通过影响膝关节传入神经元,而当软骨下骨受损时,BDNF/TrkB 信号通过影响疾病晚期的骨传入神经元,可能在 OA 疼痛的发病机制中发挥作用。对 BDNF/TrkB 信号的靶向操作可能会为治疗 OA 疼痛带来疗效。
BDNF sensitizes bone and joint afferent neurons at different stages of MIA-induced osteoarthritis
There is emerging evidence that Brain Derived Neurotrophic Factor (BDNF), and one of its receptors TrkB, play important roles in the pathogenesis of osteoarthritis (OA) pain. Whilst these studies clearly highlight the potential for targeting BDNF/TrkB signaling to treat OA pain, the mechanism for how BDNF/TrkB signaling contributes to OA pain remains unclear. In this study, we used an animal model of mono-iodoacetate (MIA)-induced OA, in combination with electrophysiology, behavioral testing, Western blot analysis, and retrograde tracing and immunohistochemistry, to identify roles for BDNF/TrkB signaling in the pathogenesis of OA pain. We found that: 1) TrkB is expressed in myelinated medium diameter neurons that innervate the knee joint and bone in naïve animals; 2) peripheral application of BDNF increases the sensitivity of Aδ, but not C knee joint and bone afferent neurons, in response to mechanical stimulation, in naïve animals; 3) BDNF expression increases in synovial tissue in early MIA-induced OA, when pathology is confined to the joint, and in the subchondral bone in late MIA-induced OA, when there is additional damage to the surrounding bone; and 4) TrkB inhibition reverses MIA-induced changes in the sensitivity of Aδ but not C knee joint afferent neurons early in MIA-induced OA, and Aδ but not C bone afferent neurons late in MIA-induced OA. Our findings suggest that BDNF/TrkB signaling may have a role to play in the pathogenesis of OA pain, through effects on knee joint afferent neurons early in disease when there is inflammation confined to the joint, and bone afferent neurons late in disease when there is involvement of damage to subchondral bone. Targeted manipulation of BDNF/TrkB signaling may provide therapeutic benefit for the management of OA pain.
期刊介绍:
BONE is an interdisciplinary forum for the rapid publication of original articles and reviews on basic, translational, and clinical aspects of bone and mineral metabolism. The Journal also encourages submissions related to interactions of bone with other organ systems, including cartilage, endocrine, muscle, fat, neural, vascular, gastrointestinal, hematopoietic, and immune systems. Particular attention is placed on the application of experimental studies to clinical practice.