大鼠脊髓损伤后降钙素基因相关肽及神经元钙超载的变化及相关性分析

doi:10.3877/cma.j.issn.2095-9141.2024.04.002

中华神经创伤外科电子杂志 ›› 2024, Vol. 10 ›› Issue (04) : 198 -205. doi: 10.3877/cma.j.issn.2095-9141.2024.04.002

基础研究

大鼠脊髓损伤后降钙素基因相关肽及神经元钙超载的变化及相关性分析

薛文¹, 刘卓², 贾卫华¹, 张小义¹, 刘进¹, 王爱国¹, 冯志刚¹, 杨鑫¹, 田祺¹, 段虎斌¹^,^†(

)

1.033000 山西吕梁，吕梁市人民医院（山西医科大学附属吕梁医院）神经外科
2.510000 广州，广东三九脑科医院神经外一科

收稿日期:2024-02-03 出版日期:2024-08-15
通信作者: 段虎斌
基金资助:
国家自然科学基金（30600637）吕梁市重点研发项目（社会发展）（2019SHFZ63）吕梁市引进高层次科技人才重点研发项目（2023RC08）

Changes and prognosis of calcitonin gene-related peptide and neuronal calcium overload after spinal cord injury in rats

Wen Xue¹, Zhuo Liu², Weihua Jia¹, Xiaoyi Zhang¹, Jin Liu¹, Aiguo Wang¹, Zhigang Feng¹, Xin Yang¹, Qi Tian¹, Hubin Duan¹^,^†()

1.Department of Neurosurgery, Lvliang People’s Hospital (Lvliang Hospital of Shanxi Medical University), Lvliang 033000, China
2.Department of Neurosurgery,Guangdong Sanjiu Brain Hospital,Guangzhou 510000,China

Received:2024-02-03 Published:2024-08-15
Corresponding author: Hubin Duan

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引用本文：

薛文, 刘卓, 贾卫华, 张小义, 刘进, 王爱国, 冯志刚, 杨鑫, 田祺, 段虎斌. 大鼠脊髓损伤后降钙素基因相关肽及神经元钙超载的变化及相关性分析[J]. 中华神经创伤外科电子杂志, 2024, 10(04): 198-205.

Wen Xue, Zhuo Liu, Weihua Jia, Xiaoyi Zhang, Jin Liu, Aiguo Wang, Zhigang Feng, Xin Yang, Qi Tian, Hubin Duan. Changes and prognosis of calcitonin gene-related peptide and neuronal calcium overload after spinal cord injury in rats[J]. Chinese Journal of Neurotraumatic Surgery(Electronic Edition), 2024, 10(04): 198-205.

目的

研究脊髓损伤（SCI）后神经元内钙离子（Ca²⁺）浓度及血浆中降钙素基因相关肽（CGRP）浓度的变化，及其与SCI 严重程度之间的关系。

方法

100 只雄性Wistar 大鼠按照随机数字表法以3∶1分为实验组（75只）和对照组（25只），实验组采用Feeney法按自由落体致伤原理制成不同损伤程度的SCI大鼠病理模型，并按照损伤严重程度分为轻度组（25只）、中度组（25只）和重度组（25只），对照组仅行手术操作，不进行打击损伤。在建模后0.5、6、12、24、48、72 h，每组分别取10只大鼠予以眼内眦取血，采用放射免疫分析法测定血浆中CGRP浓度；并分别于各时间点取3只大鼠（伤后72 h的3只大鼠从眼内眦取血的10只大鼠中随机选取）予以断颈处死，取出脊髓（T9～11），分离神经元并进行纯度检测，通过激光扫描共聚焦荧光显微镜测定神经元内Ca²⁺浓度。

结果

实验组大鼠的神经元内Ca²⁺荧光像素值在损伤后持续升高，24 h时达到最高，之后逐渐下降，各时间点的Ca²⁺荧光像素值均明显高于对照组，且重度组＞中度组＞轻度组，差异均有统计学意义（P＜0.05）。实验组大鼠血浆中CGRP 浓度在损伤后0.5 h 快速上升，显著高于对照组，差异有统计学意义（P＜0.05）；损伤后6 h开始降低，48 h逐渐升高，且损伤后6、12、24、48 h的血浆中CGRP 浓度均低于对照组，差异有统计学意义（P＜0.05）。实验组中，3组大鼠损伤后0.5 h血浆中CGRP 浓度比较，差异无统计学意义（P＞0.05）；损伤后12、24、48 h 血浆中CGRP 浓度比较，重度组＜中度组＜轻度组，差异有统计学意义（P＜0.05）。相关性分析显示，中度组和重度组的Ca²⁺浓度和CGRP 浓度呈负相关（中度组：r=-0.513，P＜0.001；重度组：r=-0.391，P=0.013）。

结论

SCI早期会出现神经元内钙超载和CGRP 浓度异常，且二者呈负相关，可能与原发损伤信号的传导及继发性级联反应二次损伤密切相关，SCI发生后及早维持神经元内Ca²⁺浓度和血浆中CGRP浓度的稳态，有利于SCI患者的治疗并改善预后。

关键词: 神经损伤与修复, 脊髓损伤, 钙超载, 降钙素基因相关肽

Objective

To study the changes in the concentrations of calcium ion (Ca²⁺)in neurons and calcitonin-gene-related peptide (CGRP) in plasma and their relationship with the severity of spinal cord injury (SCI).

Methods

A total of 100 male Wistar rats were randomly divided into experimental group(75 rats)and control group (25 rats)in a ratio of 3∶1 according to the random number table method.The experimental group was made into pathological models of SCI rats with light, medium and heavy injuries according to the principle of free fall injury by Feeney method, and divided into mild group(25 rats), moderate group (25 rats) and severe group (25 rats) according to the severity of injuries. The control group only underwent surgery, and did not cause SCI. At each time period (0.5, 6, 12, 24, 48 and 72 h) after the establishment of the model, 10 rats in each group were randomly selected to take blood from the eye canthus, and the CGRP concentration in plasma was determined by radioimmunoassay,among which 3 rats were randomly selected (including 3 rats randomly selected from 10 rats with blood taken from the canthus at 72 h after modeling)to be killed by neck-breaking,and the spinal cord (T9-11)was taken out, and the neurons were isolated and the purity was detected, the intracellular Ca²⁺concentration of neurons was measured by laser scanning confocal microscopy.

Results

The intracellular Ca²⁺ fluorescence pixel values of the experimental group rats rapidly increased after injury, reaching the highest value at 24 h and gradually decreased thereafter.Ca²⁺fluorescence pixel values at each time point were significantly higher than those of the control group, with severe group＞moderate group＞mild group,and the differences were statistically significant (P＜0.05).The concentration of CGRP in the plasma of the experimental group rats rapidly increased at 0.5 h after injury,significantly higher than that of the control group, and the difference was statistically significant (P＜0.05); The concentration of CGRP in the plasma began to decrease at 6 h after injury and gradually increased at 48 h, the concentrations of CGRP in the plasma at 6, 12, 24, and 48 h after injury were all lower than those in the control group, and the differences were statistically significant (P＜0.05). In the experimental group, there was no statistically significant difference in the concentration of CGRP in the plasma of the three groups of rats at 0.5 h after injury (P＞0.05); The plasma concentration of CGRP was compared at 12, 24, and 48 h after injury, with the severe grouP＜moderate grouP＜mild group, and the differences were statistically significant (P＜0.05).Correlation analysis showed a negative correlation between Ca²⁺concentration and CGRP concentration in the moderate and severe groups (moderate group: r=-0.513,P＜0.001; severe group: r=-0.391, P=0.013).

Conclusion

In the early stage of SCI, there may be intracellular calcium overload and abnormal CGRP concentration in neurons, which are negatively correlated and may be closely related to the transmission of primary injury signals and secondary cascade reactions. Maintaining the steady state of intracellular Ca²⁺ concentration and CGRP concentration in plasma as soon as possible after SCI is beneficial for the treatment and improvement of prognosis of SCI patients.

Key words: Nerve injury and repair, Spinal cord injury, Calcium overload, Calcitonin-generelated peptide

图1 脊髓损伤建模装置示意图

Fig.1 Schematic diagram of spinal cord injury modeling device

图2 脊髓神经元荧光鉴定染色图

Fig.2 Fluorescence identification staining of spinal cord neurons

图3 2组大鼠脊髓神经元纯度检验（10×） A：对照组；B：实验组

Fig.3 Purity test of spinal cord neurons in two groups of rats(10×)

图4 各组大鼠脊髓损伤后24 h Ca²⁺荧光离子成像 A：对照组；B：轻度组；C：中度组；D：重度组

Fig.4 Ca²⁺fluorescence ion imaging 24 h after spinal cord injury in each group of rats

表1 实验组和对照组大鼠SCI后不同时间的Ca²⁺荧光像素值比较

Tab.1 Comparison of Ca²⁺fluorescence pixel values between experimental group and control group at different time

组别	只数	0.5 h（ $\bar{x}$ ±s）	6 h（ $\bar{x}$ ±s）	12 h[M（Q₁，Q₃）]	24 h[M（Q₁，Q₃）]	48 h（ $\bar{x}$ ±s）	72 h[M（Q₁，Q₃）]
对照组	10	86.56±7.74	85.37±5.84	88.59（84.00，89.89）	85.89（81.78，87.70）	85.80±4.25	85.81（78.90，88.83）
轻度组	10	95.51±4.83^a	106.13±8.55^a	113.14（111.77，114.63）^a	160.64（153.73，162.83）^a	135.69±4.55^a	116.37（110.11，125.16）^a
中度组	10	101.68±6.28^ab	110.70±1.84^ab	122.59（121.17，123.83）^ab	177.50（171.76，181.61）^ab	146.22±4.32^ab	137.43（131.88，139.49）^ab
重度组	10	103.51±5.06^abc	121.04±4.39^abc	132.38（129.23，136.76）^abc	194.01（186.82，203.19）^abc	159.34±4.20^abc	142.43（140.53，151.11）^abc
F/H值		15.225	64.817	157.024	497.836	511.836	93.155
P值		＜0.001	＜0.001	＜0.001	＜0.001	＜0.001	＜0.001

表1 实验组和对照组大鼠SCI后不同时间的Ca²⁺荧光像素值比较

Tab.1 Comparison of Ca²⁺fluorescence pixel values between experimental group and control group at different time

组别	只数	0.5 h（ $\bar{x}$ ±s）	6 h（ $\bar{x}$ ±s）	12 h[M（Q₁，Q₃）]	24 h[M（Q₁，Q₃）]	48 h（ $\bar{x}$ ±s）	72 h[M（Q₁，Q₃）]
对照组	10	86.56±7.74	85.37±5.84	88.59（84.00，89.89）	85.89（81.78，87.70）	85.80±4.25	85.81（78.90，88.83）
轻度组	10	95.51±4.83^a	106.13±8.55^a	113.14（111.77，114.63）^a	160.64（153.73，162.83）^a	135.69±4.55^a	116.37（110.11，125.16）^a
中度组	10	101.68±6.28^ab	110.70±1.84^ab	122.59（121.17，123.83）^ab	177.50（171.76，181.61）^ab	146.22±4.32^ab	137.43（131.88，139.49）^ab
重度组	10	103.51±5.06^abc	121.04±4.39^abc	132.38（129.23，136.76）^abc	194.01（186.82，203.19）^abc	159.34±4.20^abc	142.43（140.53，151.11）^abc
F/H值		15.225	64.817	157.024	497.836	511.836	93.155
P值		＜0.001	＜0.001	＜0.001	＜0.001	＜0.001	＜0.001

表2 实验组与对照组大鼠SCI后不同时间的CGRP浓度比较（µg/mL）

Tab.2 Comparison of CGRP concentration between experimental group and control group at different time (µg/mL)

组别	只数	0.5 h（ $\bar{x}$ ±s）	6 h（ $\bar{x}$ ±s）	12 h[M（Q₁，Q₃）]	24 h（ $\bar{x}$ ±s）	48 h（ $\bar{x}$ ±s）	72 h（ $\bar{x}$ ±s）
对照组	10	3.22±0.35	3.03±0.29	3.43（3.11，3.81）	3.14±0.32	3.18±0.46	3.25±0.38
轻度组	10	6.55±0.29^a	2.67±0.60	2.33（1.97，2.73）^a	1.80±0.21^a	2.67±0.35^a	3.68±0.72
中度组	10	6.73±0.63^a	2.96±0.33	1.47（1.34，1.61）^ab	1.21±0.23^ab	1.88±0.19^ab	3.06±0.64
重度组	10	6.08±0.37^a	1.48±0.23^abc	1.12（1.05，1.32）^abc	0.65±0.10^abc	1.48±0.40^abc	1.94±0.62^abc
F/H值		129.109	31.014	128.067	195.703	39.607	13.407
P值		＜0.001	0.013	＜0.001	＜0.001	＜0.001	＜0.001

表2 实验组与对照组大鼠SCI后不同时间的CGRP浓度比较（µg/mL）

Tab.2 Comparison of CGRP concentration between experimental group and control group at different time (µg/mL)

组别	只数	0.5 h（ $\bar{x}$ ±s）	6 h（ $\bar{x}$ ±s）	12 h[M（Q₁，Q₃）]	24 h（ $\bar{x}$ ±s）	48 h（ $\bar{x}$ ±s）	72 h（ $\bar{x}$ ±s）
对照组	10	3.22±0.35	3.03±0.29	3.43（3.11，3.81）	3.14±0.32	3.18±0.46	3.25±0.38
轻度组	10	6.55±0.29^a	2.67±0.60	2.33（1.97，2.73）^a	1.80±0.21^a	2.67±0.35^a	3.68±0.72
中度组	10	6.73±0.63^a	2.96±0.33	1.47（1.34，1.61）^ab	1.21±0.23^ab	1.88±0.19^ab	3.06±0.64
重度组	10	6.08±0.37^a	1.48±0.23^abc	1.12（1.05，1.32）^abc	0.65±0.10^abc	1.48±0.40^abc	1.94±0.62^abc
F/H值		129.109	31.014	128.067	195.703	39.607	13.407
P值		＜0.001	0.013	＜0.001	＜0.001	＜0.001	＜0.001

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Changes and prognosis of calcitonin gene-related peptide and neuronal calcium overload after spinal cord injury in rats

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Changes and prognosis of calcitonin gene-related peptide and neuronal calcium overload after spinal cord injury in rats