定量蛋白质组学分析皮质酮对急性创伤性脑损伤的神经保护作用

doi:10.3877/cma.j.issn.2095-9141.2025.01.003

中华神经创伤外科电子杂志 ›› 2025, Vol. 11 ›› Issue (01) : 17 -25. doi: 10.3877/cma.j.issn.2095-9141.2025.01.003

基础研究

定量蛋白质组学分析皮质酮对急性创伤性脑损伤的神经保护作用

吕一帆¹, 张斌², 茆翔³, 刘佰运¹, 高国一¹, 牛非¹^,^†(

)

^1. 100070 北京市神经外科研究所中枢神经系统损伤研究北京市重点实验室和首都医科大学附属北京天坛医院神经外科
^2. 100070 北京，首都医科大学附属北京天坛医院重症医学科
^3. 230022 合肥，安徽医科大学第一附属医院神经外科

收稿日期:2024-08-16 出版日期:2025-02-15
通信作者: 牛非
基金资助:
国家自然科学基金(81771327)北京市卫生健康委员会2022年预算项目(11000022T000000423832)北京市神经外科研究所科研培育基金

Protein profiling indentified neuroprotection effect after corticosterone intervention in rats with traumatic brain injury

Yifan Lyu¹, Bin Zhang², Xiang Mao³, Baiyun Liu¹, Guoyi Gao¹, Fei Niu¹^,^†()

^1. Key Laboratory of Central Nervous System Injury，Beijing Neurosurgical Institute，and Neurosurgery Center，Beijing Tiantan Hospital，Capital Medical University，Beijing 100070，China
^2. Department of Critical Care Medicine，Beijing Tiantan Hospital，Capital Medical University，Beijing 100070，China
^3. Department of Neurosurgery，the First Affiliated Hospital of Anhui Medical University，Hefei 230022，China

Received:2024-08-16 Published:2025-02-15
Corresponding author: Fei Niu

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引用本文：

吕一帆, 张斌, 茆翔, 刘佰运, 高国一, 牛非. 定量蛋白质组学分析皮质酮对急性创伤性脑损伤的神经保护作用[J/OL]. 中华神经创伤外科电子杂志, 2025, 11(01): 17-25.

Yifan Lyu, Bin Zhang, Xiang Mao, Baiyun Liu, Guoyi Gao, Fei Niu. Protein profiling indentified neuroprotection effect after corticosterone intervention in rats with traumatic brain injury[J/OL]. Chinese Journal of Neurotraumatic Surgery(Electronic Edition), 2025, 11(01): 17-25.

目的

通过定量蛋白质组学探讨皮质酮（CORT）对急性创伤性脑损伤（TBI）的神经保护作用。

方法

选取15只SD雄性大鼠，随机分为假手术组、TBI模型组和CORT治疗组，每组5只。使用控制性皮质撞击（CCI）建立大鼠TBI模型（TBI模型组），假手术组与TBI模型组操作步骤相同，仅不打击皮质；CORT治疗组在打击后1 h内腹腔注射CORT（0.3 mg/kg），给药1次/d，连续给药2 d。TBI 48 h后，通过超高效液相色谱和同位素标记相对与绝对定量（iTRAQ）蛋白质质谱分析TBI模型组和CORT治疗组大鼠海马组织之间的差异蛋白。采用OmicStudio工具、基因本体（GO）数据库、通路分析软件（IPA）、Cytoscape软件分别就差异蛋白表达情况的火山图、细胞组分、生物进程、分子功能、经典富集通路以及蛋白质之间的相互作用进行绘制和分析。

结果

蛋白质质谱数据显示，共鉴定出3134种蛋白质，其中CORT治疗组和TBI模型组有71种差异表达的蛋白质。火山图结果显示，与TBI模型组相比，CORT治疗组上调的差异蛋白有28种［差异倍数（FC）≥1.5］，下调的差异蛋白有32种（FC≤0.65）。生物信息学分析（GO和IPA富集经典通路）结果显示，富集的经典通路包括肝脏X受体（LXR）/类视黄醇X受体（RXR）激活通路［-log₁₀（P值）=6.96］、法尼醇X受体（FXR）/RXR激活通路［-log₁₀（P值）=6.84］，急性期反应信号通路［-log₁₀（P值）=5.81］等。差异蛋白质之间相互作用节点排在前5位的蛋白质包括α-1-抗蛋白酶、血清转铁蛋白、血纤维蛋白溶酶原、补体C3、细胞色素C等。

结论

CORT对TBI神经保护作用的机制可能涉及调节凝血障碍、促进铁稳态平衡、减少脂质过氧化、对急性期的反应以及抗凋亡等作用。

关键词: 创伤性脑损伤, 生物标志物, 蛋白质组学, 皮质酮, iTRAQ, 神经保护

Objective

To explore the neuroprotective effect of corticosterone （CORT） on acute traumatic brain injury （TBI） through quantitative proteomics.

Methods

Fifteen male Sprague-Dawley（SD） rats were selected and randomly divided into a sham operation group，a TBI model group，and a CORT treatment group，with 5 rats in each group. A rat TBI model was established using controlled cortical impact （CCI）. The operation steps of the sham operation group were the same as those of the TBI model group，except that the cortex was not impacted. The CORT treatment group was intraperitoneally injected with CORT （0.3 mg/kg） within 1 h after impact，once a day for 2 consecutive days. At 48 h after TBI，ultra-high performance liquid chromatography and isobaric tags for relative and absolute quantitation（iTRAQ） protein mass spectrometry were used to analyze the differential proteins in the hippocampal tissues between the TBI model group and the CORT treatment group. OmicStudio tools，the Gene Ontology （GO） database，Ingenuity Pathway Analysis （IPA） software，and Cytoscape software were used to plot and analyze the volcano plot of differential protein expression，cellular components，biological processes and molecular functions，canonical enrichment pathways，and the interactions between proteins，respectively.

Results

The results of protein mass spectrometry data showed that a total of 3134 proteins were identified，and there were 71 differentially expressed proteins between the CORT treatment group and the TBI model group. The results of the volcano plot showed that，compared with the TBI model group，there were 28 up-regulated differential proteins ［fold change （FC）≥1.5） and 32 down-regulated differential proteins （FC≤0.65） in the CORT treatment group. The results of bioinformatics analysis （GO and IPA enrichment of canonical pathways） showed that the enriched canonical pathways included liver X receptor/retinoid X receptor （RXR） activation ［-log₁₀（P）=6.96］，farnesoid X receptor/RXR activation ［-log₁₀（P）=6.84］，acute phase response signaling pathway ［-log₁₀（P）=5.81］，etc.. The top 5 proteins in the interaction nodes among the differential proteins included α-1-antichymotrypsin，serum transferrin，plasminogen，complement C3，cytochrome C，etc..

Conclusion

The mechanism of the neuroprotective effect of CORT on TBI may involve regulating coagulation disorders，promoting iron homeostasis，reducing lipid peroxidation，the response to the acute phase，and anti-apoptosis.

Key words: Traumatic brain injury, Biomarkers, Proteomics, Corticosterone, iTRAQ, Neuroprotection

图1 各组大鼠TBI 48 h的脑组织图片 A：假手术组；B：TBI模型组；C：CORT治疗组；TBI：创伤性脑损伤；CORT：皮质酮

Fig.1 Pictures of brain tissue in rats with brain injury at 48 h in each group

表1 CORT治疗组和TBI模型组间具有倍数变化的差异表达蛋白

Tab.1 Differentially expressed proteins with fold changes between CORT treatment group and TBI model group

编号	蛋白名称	基因名	CORT/TBI（差异倍数≤0.65与≥1.5）	P值
P54311	Guanine nucleotide-binding protein G（I）/G（S）/G（T） subunit beta-1	Gnb1	0.046	0.007
P24090	Alpha-2-HS-glycoprotein	Ahsg	0.063	0.042
P68255	14-3-3 protein theta	Ywhaq	0.104	0.003
P62747	Rho-related GTP-binding protein RhoB	Rhob	0.119	0.009
P00787	Cathepsin B	Ctsb	0.134	0.014
P09606	Glutamine synthetase	Glul	0.143	0.022
Q01177	Plasminogen	Plg	0.167	0.001
Q05962	ADP/ATP translocase 1	Slc25a4	0.167	0.034
P12346	Serotransferrin	Tf	0.185	＜0.001
P62898	Cytochrome c， somatic	Cycs	0.192	0.007
P29117	Peptidyl-prolyl cis-trans isomerase F， mitochondrial	Ppif	0.207	0.022
P46101	Dipeptidyl aminopeptidase-like protein 6	Dpp6	0.286	＜0.001
B0BNE5	S-formylglutathione hydrolase	Esd	0.288	0.019
P20059	Hemopexin	Hpx	0.302	0.016
Q8CFN2	Cell division control protein 42 homolog	Cdc42	0.331	0.040
P04276	Vitamin D-binding protein	Gc	0.350	＜0.001
P01946	Hemoglobin subunit alpha-1/2	Hba1	0.363	＜0.001
Q6P6R2	Dihydrolipoyl dehydrogenase， mitochondrial	Dld	0.373	0.005
P18266	Glycogen synthase kinase-3 beta	Gsk3b	0.413	0.012
P07150	Annexin A1	Anxa1	0.425	0.001
P01026	Complement C3	C3	0.440	＜0.001
Q9QYF3	Unconventional myin-Va	Myo5a	0.466	0.003
Q8CHM7	2-hydroxyacyl-CoA lyase 1	Hacl1	0.492	0.026
P63102	14-3-3 protein zeta/delta	Ywhaz	0.496	0.037
Q6UPE1	Electron transfer flavoprotein-ubiquinone oxidoreductase， mitochondrial	Etfdh	0.515	0.001
P06687	Sodium/potassium-transporting ATPase subunit alpha-3	Atp1a3	0.540	0.019
P04636	Malate dehydrogenase， mitochondrial	Mdh2	0.550	0.013
Q08602	Geranylgeranyl transferase type-2 subunit alpha	Rabggta	0.570	0.012
P17475	Alpha-1-antiproteinase	Serpina1	0.586	0.010
Q62915	REVERSED Peripheral plasma membrane protein CASK	Cask	0.586	0.042
Q63041	Alpha-1-macroglobulin	A1m	0.614	0.020
O35180	Endophilin-A3	Sh3gl3	0.631	0.032
P34926	Microtubule-associated protein 1A	Map1a	1.514	0.033
Q62824	Exocyst complex component 4	Exoc4	1.514	0.036
P61265	Syntaxin-1B	Stx1b	1.514	0.037
O55166	Vacuolar protein sorting-associated protein 52 homolog	Vps52	1.556	0.028
P09527	Ras-related protein Rab-7a	Rab7a	1.629	0.032
P07335	Creatine kinase B-type	Ckb	1.675	0.043
A1L1I3	Numb-like protein	Numbl	1.706	0.016
O35550	Rab GTPase-binding effector protein 1	Rabep1	1.706	0.044
P29457	Serpin H1	Serpinh1	1.738	0.028
P35281	Ras-related protein Rab-10	Rab10	1.754	0.045
Q63560	Microtubule-associated protein 6	Map6	1.770	0.004
Q5U300	Ubiquitin-like modifier-activating enzyme 1	Uba1	1.770	0.020
P10888	Cytochrome c oxidase subunit 4 isoform 1， mitochondrial	Cox4i1	1.836	0.034
Q924S5	Lon protease homolog， mitochondrial	Lonp1	1.888	0.047
P11915	Non-specific lipid-transfer protein	Scp2	1.959	0.016
Q9ERH3	WD repeat-containing protein 7	Wdr7	1.995	0.009
P16086	Spectrin alpha chain， non-erythrocytic 1	Sptan1	2.032	＜0.001
Q62936	Disks large homolog 3	Dlg3	2.051	0.005
Q9QWN8	Spectrin beta chain， non-erythrocytic 2	Sptbn2	2.089	0.003
P11507	Sarcoplasmic/endoplasmic reticulum calcium ATPase 2	Atp2a2	2.228	0.035
Q60587	Trifunctional enzyme subunit beta， mitochondrial	Hadhb	2.333	0.009
P60881	Synaptomal-associated protein 25	Snap25	2.399	0.045
P18886	Carnitine O-palmitoyltransferase 2， mitochondrial	Cpt2	2.443	0.007
Q04400	Adenylate cyclase type 5	Adcy5	2.729	0.009
Q80WF4	Transmembrane protein 132A	Tmem132a	2.780	0.007
Q6IFW6	Keratin， type I cytkeletal 10	Krt10	2.884	0.015
O08719	Ena/VASP-like protein	Evl	2.992	0.040
Q5EGZ1	Angiotensin-converting enzyme 2	Ace2	6.138	0.037

表1 CORT治疗组和TBI模型组间具有倍数变化的差异表达蛋白

Tab.1 Differentially expressed proteins with fold changes between CORT treatment group and TBI model group

编号	蛋白名称	基因名	CORT/TBI（差异倍数≤0.65与≥1.5）	P值
P54311	Guanine nucleotide-binding protein G（I）/G（S）/G（T） subunit beta-1	Gnb1	0.046	0.007
P24090	Alpha-2-HS-glycoprotein	Ahsg	0.063	0.042
P68255	14-3-3 protein theta	Ywhaq	0.104	0.003
P62747	Rho-related GTP-binding protein RhoB	Rhob	0.119	0.009
P00787	Cathepsin B	Ctsb	0.134	0.014
P09606	Glutamine synthetase	Glul	0.143	0.022
Q01177	Plasminogen	Plg	0.167	0.001
Q05962	ADP/ATP translocase 1	Slc25a4	0.167	0.034
P12346	Serotransferrin	Tf	0.185	＜0.001
P62898	Cytochrome c， somatic	Cycs	0.192	0.007
P29117	Peptidyl-prolyl cis-trans isomerase F， mitochondrial	Ppif	0.207	0.022
P46101	Dipeptidyl aminopeptidase-like protein 6	Dpp6	0.286	＜0.001
B0BNE5	S-formylglutathione hydrolase	Esd	0.288	0.019
P20059	Hemopexin	Hpx	0.302	0.016
Q8CFN2	Cell division control protein 42 homolog	Cdc42	0.331	0.040
P04276	Vitamin D-binding protein	Gc	0.350	＜0.001
P01946	Hemoglobin subunit alpha-1/2	Hba1	0.363	＜0.001
Q6P6R2	Dihydrolipoyl dehydrogenase， mitochondrial	Dld	0.373	0.005
P18266	Glycogen synthase kinase-3 beta	Gsk3b	0.413	0.012
P07150	Annexin A1	Anxa1	0.425	0.001
P01026	Complement C3	C3	0.440	＜0.001
Q9QYF3	Unconventional myin-Va	Myo5a	0.466	0.003
Q8CHM7	2-hydroxyacyl-CoA lyase 1	Hacl1	0.492	0.026
P63102	14-3-3 protein zeta/delta	Ywhaz	0.496	0.037
Q6UPE1	Electron transfer flavoprotein-ubiquinone oxidoreductase， mitochondrial	Etfdh	0.515	0.001
P06687	Sodium/potassium-transporting ATPase subunit alpha-3	Atp1a3	0.540	0.019
P04636	Malate dehydrogenase， mitochondrial	Mdh2	0.550	0.013
Q08602	Geranylgeranyl transferase type-2 subunit alpha	Rabggta	0.570	0.012
P17475	Alpha-1-antiproteinase	Serpina1	0.586	0.010
Q62915	REVERSED Peripheral plasma membrane protein CASK	Cask	0.586	0.042
Q63041	Alpha-1-macroglobulin	A1m	0.614	0.020
O35180	Endophilin-A3	Sh3gl3	0.631	0.032
P34926	Microtubule-associated protein 1A	Map1a	1.514	0.033
Q62824	Exocyst complex component 4	Exoc4	1.514	0.036
P61265	Syntaxin-1B	Stx1b	1.514	0.037
O55166	Vacuolar protein sorting-associated protein 52 homolog	Vps52	1.556	0.028
P09527	Ras-related protein Rab-7a	Rab7a	1.629	0.032
P07335	Creatine kinase B-type	Ckb	1.675	0.043
A1L1I3	Numb-like protein	Numbl	1.706	0.016
O35550	Rab GTPase-binding effector protein 1	Rabep1	1.706	0.044
P29457	Serpin H1	Serpinh1	1.738	0.028
P35281	Ras-related protein Rab-10	Rab10	1.754	0.045
Q63560	Microtubule-associated protein 6	Map6	1.770	0.004
Q5U300	Ubiquitin-like modifier-activating enzyme 1	Uba1	1.770	0.020
P10888	Cytochrome c oxidase subunit 4 isoform 1， mitochondrial	Cox4i1	1.836	0.034
Q924S5	Lon protease homolog， mitochondrial	Lonp1	1.888	0.047
P11915	Non-specific lipid-transfer protein	Scp2	1.959	0.016
Q9ERH3	WD repeat-containing protein 7	Wdr7	1.995	0.009
P16086	Spectrin alpha chain， non-erythrocytic 1	Sptan1	2.032	＜0.001
Q62936	Disks large homolog 3	Dlg3	2.051	0.005
Q9QWN8	Spectrin beta chain， non-erythrocytic 2	Sptbn2	2.089	0.003
P11507	Sarcoplasmic/endoplasmic reticulum calcium ATPase 2	Atp2a2	2.228	0.035
Q60587	Trifunctional enzyme subunit beta， mitochondrial	Hadhb	2.333	0.009
P60881	Synaptomal-associated protein 25	Snap25	2.399	0.045
P18886	Carnitine O-palmitoyltransferase 2， mitochondrial	Cpt2	2.443	0.007
Q04400	Adenylate cyclase type 5	Adcy5	2.729	0.009
Q80WF4	Transmembrane protein 132A	Tmem132a	2.780	0.007
Q6IFW6	Keratin， type I cytkeletal 10	Krt10	2.884	0.015
O08719	Ena/VASP-like protein	Evl	2.992	0.040
Q5EGZ1	Angiotensin-converting enzyme 2	Ace2	6.138	0.037

图2 CORT治疗组与TBI模型组间差异蛋白表达情况的火山图蓝色代表下调的差异蛋白（FC≤0.65），红色代表上调的差异蛋白（FC≥1.5），灰色代表FC＞0.65且＜1.5的差异蛋白；TBI：创伤性脑损伤；CORT：皮质酮；FC：差异倍数

Fig.2 Volcano diagram of differential protein expression between CORT treatment group and TBI model group

图3 CORT治疗组与TBI模型组间差异表达蛋白的基因本体功能分类

Fig.3 Gene functional classification of differentially expressed proteins between CORT treatment group and TBI model group

图4 CORT治疗组与TBI模型组差异蛋白的通路富集分析结果

Fig.4 Pathway enrichment analysis of differentially expressed proteins between CORT treatment group and TBI model group

图5 CORT治疗组与TBI模型组间前10节点蛋白的蛋白质之间的相互作用绿色代表下调的差异蛋白（FC≤0.65）；红色代表上调的差异蛋白（FC≥1.5）；长方形表示富集的经典通路；连接线显示多种蛋白质之间或蛋白质与通路之间的相互作用；TBI：创伤性脑损伤；CORT：皮质酮；FC：差异倍数

Fig.5 Protein-protein interactions with top 10 node proteins between CORT treatment group and TBI model group

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Protein profiling indentified neuroprotection effect after corticosterone intervention in rats with traumatic brain injury

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Protein profiling indentified neuroprotection effect after corticosterone intervention in rats with traumatic brain injury