Matatia Peri R, Christian Elena, Sokol Caroline L
Division of Rheumatology, Allergy & Immunology, Center for Immunology & Inflammatory Diseases, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts, USA.
Department of Immunology, Harvard Medical School, Boston, Massachusetts, USA.
Immunol Rev. 2024 Sep;326(1):83-101. doi: 10.1111/imr.13375. Epub 2024 Aug 2.
Food allergy is classically characterized by an inappropriate type-2 immune response to allergenic food antigens. However, how allergens are detected and how that detection leads to the initiation of allergic immunity is poorly understood. In addition to the gastrointestinal tract, the barrier epithelium of the skin may also act as a site of food allergen sensitization. These barrier epithelia are densely innervated by sensory neurons, which respond to diverse physical environmental stimuli. Recent findings suggest that sensory neurons can directly detect a broad array of immunogens, including allergens, triggering sensory responses and the release of neuropeptides that influence immune cell function. Reciprocally, immune mediators modulate the activation or responsiveness of sensory neurons, forming neuroimmune feedback loops that may impact allergic immune responses. By utilizing cutaneous allergen exposure as a model, this review explores the pivotal role of sensory neurons in allergen detection and their dynamic bidirectional communication with the immune system, which ultimately orchestrates the type-2 immune response. Furthermore, it sheds light on how peripheral signals are integrated within the central nervous system to coordinate hallmark features of allergic reactions. Drawing from this emerging evidence, we propose that atopy arises from a dysregulated neuroimmune circuit.
食物过敏的经典特征是对过敏性食物抗原产生不适当的2型免疫反应。然而,目前人们对过敏原是如何被检测到的,以及这种检测如何引发过敏免疫反应的了解还很少。除了胃肠道,皮肤的屏障上皮也可能是食物过敏原致敏的部位。这些屏障上皮由感觉神经元密集支配,感觉神经元对各种物理环境刺激作出反应。最近的研究结果表明,感觉神经元可以直接检测包括过敏原在内的多种免疫原,触发感觉反应并释放影响免疫细胞功能的神经肽。相反,免疫介质调节感觉神经元的激活或反应性,形成可能影响过敏免疫反应的神经免疫反馈回路。通过将皮肤过敏原暴露作为模型,本综述探讨了感觉神经元在过敏原检测中的关键作用,以及它们与免疫系统的动态双向通信,这最终协调了2型免疫反应。此外,它还阐明了外周信号是如何在中枢神经系统中整合以协调过敏反应的标志性特征的。基于这一最新证据,我们提出特应性是由失调的神经免疫回路引起的。