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红耳龟的皮肤神经支配:利用免疫荧光技术对鳞片感受器和感觉小体进行新的鉴定与分析及其生态学意义

Cutaneous Innervation in the Red-Eared Slider Turtle: Novel Identification and Analysis of Scale Sensilla and Sensory Corpuscles With Immunofluorescence Insights and Ecological Implications.

作者信息

Rashwan Ahmed M, El-Gendy Samir A A, Ez Elarab Samar M, Seif Manal, El-Mansi Ahmed A, Eldesoqui Mamdouh B, Alsafy Mohamed A M

机构信息

Department of Anatomy and Embryology, Faculty of Veterinary Medicine, Damanhour University, Damanhour, Egypt.

Laboratory of Life Science Frontiers, Center for iPS Cell Research and Application (CiRA), Kyoto University, Kyoto, Japan.

出版信息

J Exp Zool A Ecol Integr Physiol. 2025 Jul 16. doi: 10.1002/jez.70014.

Abstract

The red-eared slider turtle inhabits environments ranging from freshwater to semiterrestrial settings. Understanding the sensory adaptations of this species is crucial, particularly concerning its limb skin, which plays a key role in environmental interaction and survival. This study presents the first detailed identification of scale sensilla and sensory corpuscles in the red-eared slider's limb skin, offering insights into their innervation and distribution. We combined scanning electron microscopy (SEM), light microscopy, and immunofluorescence with ten antibodies to elucidate the sensory architecture and adaptation mechanisms of the turtle's skin. The antibodies include E-cadherin, four neural markers (Nestin, PGP9.5, neuron-specific enolase [NSE], and Synaptophysin), and five additional markers (PDGFRα, CD34, Vimentin, α-SMA, and Tom20) to analyze sensory structures and distribution patterns. SEM revealed scale sensilla resembling artichokes, with concentric layers surrounding a central dome featuring microplicae, grooves, and pores. Light microscopy showed these sensilla as dome-shaped structures elevated above the epidermal surface. Immunofluorescence with E-cadherin highlighted scale sensilla cells, central cells, and dermal papillae, while neural markers confirmed sensory nerves within the scale sensilla, underscoring their sensory role. Three types of sensory corpuscles were identified in the limb skin: Meissner's and Ruffini corpuscles in the dermis, and Pacinian corpuscles in the hypodermis. The four neural markers showed strong expression in sensory nerve fiber endings across all corpuscles, highlighting their roles in detecting pressure, vibration, and tactile stimuli. CD34 and PDGFRα were expressed in perineurial fibroblast-like cells and telocytes within the external capsules and concentric lamellae of Pacinian corpuscles, as well as in the external capsules of Meissner's and Ruffini corpuscles, with telocytes surrounding all three types. Vimentin was found in connective tissue and lamellar cells in all corpuscles, suggesting its role in structural support. α-SMA was strongly expressed in Pacinian corpuscles and minimally in Meissner's and Ruffini corpuscles, indicating its primary role in maintaining structural integrity in Pacinian corpuscles. Tom20 highlighted high mitochondrial activity in the nerve fibers and supporting cells of all corpuscles, with the highest expression in Meissner's corpuscles, reflecting the significant metabolic demands of these sensory structures. This study offers unprecedented insights into the sensory architecture of the red-eared slider turtle's skin. The novel identification and analysis of scale sensilla and sensory corpuscles, combined with 10 antibodies, enhances our understanding of the skin's innervation and its role in environmental adaptation, contributing valuable knowledge to sensory biology and herpetology.

摘要

红耳龟栖息于从淡水到半陆地的环境中。了解该物种的感官适应性至关重要,尤其是其肢体皮肤,它在与环境的相互作用和生存中起着关键作用。本研究首次详细鉴定了红耳龟肢体皮肤中的鳞片感受器和感觉小体,深入了解了它们的神经支配和分布情况。我们将扫描电子显微镜(SEM)、光学显微镜和免疫荧光与十种抗体相结合,以阐明龟皮肤的感觉结构和适应机制。这些抗体包括E-钙黏蛋白、四种神经标记物(巢蛋白、PGP9.5、神经元特异性烯醇化酶[NSE]和突触素)以及另外五种标记物(血小板衍生生长因子受体α[PDGFRα]、CD34、波形蛋白、α-平滑肌肌动蛋白[α-SMA]和Tom20),用于分析感觉结构和分布模式。扫描电子显微镜显示鳞片感受器类似洋蓟,围绕中央圆顶有同心层,中央圆顶具有微褶、凹槽和小孔。光学显微镜显示这些感受器为高于表皮表面的圆顶状结构。用E-钙黏蛋白进行免疫荧光显示了鳞片感受器细胞、中央细胞和真皮乳头,而神经标记物证实了鳞片感受器内的感觉神经,强调了它们的感觉作用。在肢体皮肤中鉴定出三种类型的感觉小体:真皮中的迈斯纳小体和鲁菲尼小体,以及皮下组织中的环层小体。这四种神经标记物在所有小体的感觉神经纤维末梢中均有强烈表达,突出了它们在检测压力、振动和触觉刺激方面的作用。CD34和PDGFRα在环层小体的外囊和同心板层内的神经束膜成纤维样细胞和端细胞中表达,也在迈斯纳小体和鲁菲尼小体的外囊中表达,端细胞围绕着这三种小体。波形蛋白在所有小体的结缔组织和板层细胞中均有发现,表明其在结构支持方面的作用。α-SMA在环层小体中强烈表达,在迈斯纳小体和鲁菲尼小体中表达最少,表明其在维持环层小体结构完整性方面的主要作用。Tom20突出了所有小体的神经纤维和支持细胞中的高线粒体活性,在迈斯纳小体中表达最高,反映了这些感觉结构的显著代谢需求。本研究为红耳龟皮肤的感觉结构提供了前所未有的见解。对鳞片感受器和感觉小体的新鉴定和分析,结合十种抗体,增强了我们对皮肤神经支配及其在环境适应中的作用的理解,为感觉生物学和爬虫学贡献了宝贵的知识。

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