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海马体的蛋白质组学与脂质组学整合分析以揭示癫痫的代谢图谱

Integrated Proteomics and Lipidomics Analysis of Hippocampus to Reveal the Metabolic Landscape of Epilepsy.

作者信息

Chen Yinyu, Nie Qianyun, Song Tao, Zou Xing, Li Qifu, Zhang Peng

机构信息

Key Laboratory of Tropical Translational Medicine of Ministry of Education & the First Affiliated Hospital, Hainan Medical University, Xueyuan Road 3#, Longhuaqu, Haikou 571199, Hainan, China.

Department of Pathology, School of Basic Medicine and Life Sciences, Hainan Medical University, Xueyuan Road 3#, Longhuaqu, Haikou 571199 Hainan, China.

出版信息

ACS Omega. 2025 Feb 25;10(9):9351-9367. doi: 10.1021/acsomega.4c10085. eCollection 2025 Mar 11.

DOI:10.1021/acsomega.4c10085
PMID:40092809
原文链接:https://pmc.ncbi.nlm.nih.gov/articles/PMC11904687/
Abstract

Epilepsy encompasses a spectrum of chronic brain disorders characterized by transient central nervous system dysfunctions induced by recurrent, aberrant, synchronized neuronal discharges. Hippocampal sclerosis (HS) is identified as the predominant pathological alteration in epilepsy, particularly in temporal lobe epilepsy. This study investigates the metabolic profiles of epileptic hippocampal tissues using proteomics and lipidomics techniques. An epilepsy model was established in Sprague-Dawley (SD) rats via intraperitoneal injection of pentylenetetrazole (PTZ), with hippocampal tissue samples subsequently extracted for histopathological examination. Proteomics analysis was conducted using isobaric tags for relative and absolute quantitation (iTRAQ) combined with liquid chromatography-tandem mass spectrometry (LC-MS/MS), while lipidomics analysis employed ultrahigh-performance liquid chromatography quadrupole time-of-flight mass spectrometry (UHPLC Q-TOF/MS). Proteomic analysis identified 144 proteins with significant differential expression in acute epileptic hippocampal tissue and 83 proteins in chronic epileptic hippocampal tissue. Key proteins, including neurofilament heavy (Nefh), vimentin (Vim), gelsolin (Gsn), NAD-dependent protein deacetylase (Sirt2), 2',3'-cyclic-nucleotide 3'-phosphodiesterase (Cnp), myocyte enhancer factor 2D (Mef2d), and Cathepsin D (Ctsd), were pivotal in epileptic hippocampal tissue injury and validated through parallel reaction monitoring (PRM). Concurrently, lipid metabolomics analysis identified 32 metabolites with significant differential expression in acute epileptic hippocampal tissue and 61 metabolites in chronic epileptic hippocampal tissue. Bioinformatics analysis indicated that glycerophospholipid (GP) metabolism, glycosylphosphatidylinositol (GPI)-anchor biosynthesis, and glycerolipid (GL) metabolism were crucial in epileptic hippocampal tissue injury. Integrated proteomics and lipidomics analysis revealed key protein-lipid interactions in acute and chronic epilepsy and identified critical pathways such as sphingolipid signaling, autophagy, and calcium signaling. These findings provide deeper insights into the pathophysiological mechanisms of epileptic hippocampal tissue damage, potentially unveiling novel therapeutic avenues for clinicians.

摘要

癫痫是一系列慢性脑部疾病的统称，其特征是由反复出现的、异常的、同步的神经元放电引起短暂的中枢神经系统功能障碍。海马硬化（HS）被认为是癫痫，尤其是颞叶癫痫的主要病理改变。本研究使用蛋白质组学和脂质组学技术研究癫痫海马组织的代谢谱。通过腹腔注射戊四氮（PTZ）在Sprague-Dawley（SD）大鼠中建立癫痫模型，随后提取海马组织样本进行组织病理学检查。蛋白质组学分析使用用于相对和绝对定量的等压标签（iTRAQ）结合液相色谱-串联质谱（LC-MS/MS）进行，而脂质组学分析采用超高效液相色谱四极杆飞行时间质谱（UHPLC Q-TOF/MS）。蛋白质组学分析在急性癫痫海马组织中鉴定出144种具有显著差异表达的蛋白质，在慢性癫痫海马组织中鉴定出83种蛋白质。关键蛋白质，包括神经丝重链（Nefh）、波形蛋白（Vim）、凝溶胶蛋白（Gsn）、NAD依赖性蛋白脱乙酰酶（Sirt2）、2',3'-环核苷酸3'-磷酸二酯酶（Cnp）、肌细胞增强因子2D（Mef2d）和组织蛋白酶D（Ctsd），在癫痫海马组织损伤中起关键作用，并通过平行反应监测（PRM）得到验证。同时，脂质代谢组学分析在急性癫痫海马组织中鉴定出32种具有显著差异表达的代谢物，在慢性癫痫海马组织中鉴定出61种代谢物。生物信息学分析表明，甘油磷脂（GP）代谢、糖基磷脂酰肌醇（GPI）-锚生物合成和甘油脂（GL）代谢在癫痫海马组织损伤中至关重要。综合蛋白质组学和脂质组学分析揭示了急性和慢性癫痫中的关键蛋白质-脂质相互作用，并确定了鞘脂信号传导、自噬和钙信号传导等关键途径。这些发现为癫痫海马组织损伤的病理生理机制提供了更深入的见解，可能为临床医生揭示新的治疗途径。

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Front Vet Sci. 2023 Dec 21;10:1258244. doi: 10.3389/fvets.2023.1258244. eCollection 2023.
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Expression of Cytoskeletal Proteins (GFAP, Vimentin), Proapoptotic Protein (Caspase-3) and Protective Protein (S100) in the Epileptic Focus in Adults and Children with Drug-Resistant Temporal Lobe Epilepsy Associated with Focal Cortical Dysplasia.在药物难治性颞叶癫痫伴局灶性皮质发育不良的成人和儿童癫痫灶中细胞骨架蛋白（GFAP、Vimentin）、促凋亡蛋白（Caspase-3）和保护蛋白（S100）的表达。
Int J Mol Sci. 2023 Sep 23;24(19):14490. doi: 10.3390/ijms241914490.
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BDNF as potential biomarker of epilepsy severity and psychiatric comorbidity: pitfalls in the clinical population.
BDNF 作为癫痫严重程度和精神共病的潜在生物标志物：临床人群中的陷阱。
Epilepsy Res. 2023 Sep;195:107200. doi: 10.1016/j.eplepsyres.2023.107200. Epub 2023 Aug 2.
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Ginsenoside Rg1 improved learning and memory ability and reduces neuronal apoptosis in epileptic rats through ERK/CREB/BDNF signal pathway.人参皂苷 Rg1 通过 ERK/CREB/BDNF 信号通路改善癫痫大鼠的学习记忆能力并减少神经元凋亡。
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Astrocyte-derived SerpinA3N promotes neuroinflammation and epileptic seizures by activating the NF-κB signaling pathway in mice with temporal lobe epilepsy.星形胶质细胞衍生的丝氨酸蛋白酶抑制剂 A3N 通过激活小胶质细胞 NF-κB 信号通路促进颞叶癫痫小鼠神经炎症和癫痫发作。
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