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Article(id=1198602002860179850, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1198601997155922872, articleNumber=null, orderNo=null, doi=10.11855/j.issn.0577-7402.0371.2023.0831, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1678464000000, receivedDateStr=2023-03-11, revisedDate=null, revisedDateStr=null, acceptedDate=1687795200000, acceptedDateStr=2023-06-27, onlineDate=1763698586430, onlineDateStr=2025-11-21, pubDate=1719504000000, pubDateStr=2024-06-28, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1763698586430, onlineIssueDateStr=2025-11-21, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1763698586430, creator=13701087609, updateTime=1763698586430, updator=13701087609, issue=Issue{id=1198601997155922872, tenantId=1146029695717560320, journalId=1189873630562394117, year='2024', volume='49', issue='6', pageStart='611', pageEnd='732', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=0, createTime=1763698585070, creator=13701087609, updateTime=1763698770557, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1198602775211901122, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1198601997155922872, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1198602775211901123, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1198601997155922872, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=694, endPage=700, ext={EN=ArticleExt(id=1198602003933921680, articleId=1198602002860179850, tenantId=1146029695717560320, journalId=1189873630562394117, language=EN, title=Mitigative effect and mechanism of nootkatone on depression-like behavior in mild blast traumatic brain injury rat, columnId=1190310110212751762, journalTitle=Medical Journal of Chinese People’s Liberation Army, columnName=Basic Research, runingTitle=null, highlight=null, articleAbstract=

Objective To investigate the mechanism of nootkatone (NKT) in mitigating depression-like behavior caused by blast traumatic brain injury (TBI). Methods The rat bTBI depression-like model was established by simulating the shock wave parameters of blast overpressure (BOP of 60 kPa, 90 kPa, and 120 kPa) with a biological shock wave tube. After 14 days of exposure, we evaluated the depression-like behavior of rats using the tail suspension test and forced swimming test. We identified that the BOP (120 kPa) condition caused the most noticeable depressive behavior and used this condition for subsequent experiments. Thirty male SD rats were randomly divided into sham operation group, bTBI group (BOP of 120 kPa), and bTBI+NKT group [at 1 d after exposure to BOP of 120 kPa, giving NKT 10 mg/(kg·d) orally for 14 days], 10 in each group. After 14 days of exposure, the depression-like behavior of rats was evaluated by tail suspension test and forced swimming test. The expression levels of protein kinase A (PKA), phosphorylated cyclic adenosine monophosphate effector binding protein (pCREB), and brain-derived neurotrophic factor (BDNF) in the hippocampus of rat were determined by Western blotting. Immunohistochemistry was used to detect the generation of proliferating cell nuclear antigen (PCNA)-labeled neurons in the hippocampal dentate gyrus (DG). Results BOP of 90 kPa can cause depression-like in rats and BOP of 120 kPa can cause the most noticeable depressive behavior (P<0.05). Therefore, we selected the BOP exposure of 120 kPa for subsequent experiments. After 14 days of BOP exposure, compared with sham operation group, the immobility time of tad suspension test in bTBI group was prolonged (P<0.05), the latency of for ced swimming test was shortened, the immobility time was prolonged (P<0.05), the expression levels of PKA, pCREB and BDNF protein in hippocampus were lowered (P<0.05), and the number of PCNA-labeled neurons in hippocampal DG area was reduced (P<0.05); compared with the bTBI group, the immobility time of tail suspension test in bTBI+NKT group was shortened (P<0.05), the latency of forced swimming test was prolonged, the immobility time was shortened (P<0.05), the expression levels of PKA, pCREB and BDNF protein in hippocampus were increased (P<0.05), and the number of PCNA-labeled neurons in hippocampal DG area was increased (P<0.05). Conclusions Early treatment with NKT can improve depression-like behavior in mild bTBI rats. The mechanism may be related to the up-regulation of the PKA-CREB-BDNF signaling pathway and increased expression levels of pCREB and BDNF in the hippocampus, which results in increased neuron numbers in the DG region of the hippocampus.

, correspAuthors=Jun-Hong Gao, authorNote=null, correspAuthorsNote=
E-mail:
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目的 探究诺卡酮(NKT)对轻度脑爆震伤(bTBI)大鼠抑郁样行为的缓解作用及其机制。方法 采用生物激波管分别模拟爆炸超压(BOP)为60 kPa、90 kPa和120 kPa的冲击波建立大鼠bTBI抑郁样模型。BOP暴露后14 d，采用悬尾实验及强迫游泳实验对大鼠抑郁样行为进行评估，选取抑郁样行为最为明显的BOP(120 kPa)进行后续实验。30只大鼠随机分为假手术组、bTBI组(120 kPa BOP暴露)、bTBI+NKT组[120 kPa BOP暴露后第1天开始，经口给药给予NKT 10 mg/(kg·d)，共14 d]，每组10只。BOP暴露后14 d，采用悬尾实验及强迫游泳实验对大鼠抑郁样行为进行评估；采用Western blotting检测海马组织中蛋白激酶A(PKA)、磷酸化环磷腺苷效应元件结合蛋白(pCREB)及脑源性神经营养因子(BDNF)的表达水平；免疫组化检测海马齿状回区(DG)增殖细胞核抗原(PCNA)标记的神经发生情况。结果 90 kPa的BOP暴露即可引起大鼠抑郁样行为，而120 kPa组大鼠BOP暴露后产生的抑郁样行为更明显(P<0.05)，据此选取120 kPa的BOP暴露进行后续实验。BOP暴露后14 d，与假手术组比较，bTBI组大鼠悬尾实验不动时间延长(P<0.05)，强迫游泳实验潜伏期缩短，不动时间延长(P<0.05)，海马组织中PKA、pCREB和BDNF蛋白表达水平降低(P<0.05)，海马DG区PCNA阳性神经元数量减少(P<0.05)；与bTBI组比较，bTBI+NKT组大鼠悬尾实验不动时间缩短(P<0.05)，强迫游泳实验潜伏期延长，不动时间缩短(P<0.05)，海马组织中PKA、pCREB和BDNF蛋白表达水平升高(P<0.05)，海马DG区PCNA阳性神经元数量增加(P<0.05)。结论 早期给予NKT治疗可缓解轻度bTBI大鼠的抑郁样行为，其机制可能与NKT通过激活海马PKA/CREB/BDNF信号通路，使pCREB和BDNF表达水平上调，进而促进海马DG区神经发生有关。

, correspAuthors=高俊宏, authorNote=null, correspAuthorsNote=
高俊宏，E-mail：
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范小琳，医学硕士，工程师，主要从事武器装备生物效应的评估研究

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范小琳，医学硕士，工程师，主要从事武器装备生物效应的评估研究

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范小琳，医学硕士，工程师，主要从事武器装备生物效应的评估研究

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BOP. 爆炸超压；A. 悬尾实验的不动时间；B. 强迫游泳实验的潜伏期；C. 强迫游泳实验的不动时间；与假手术组比较，(1)P<0.05；与60 kPa组比较，(2)P<0.05；与90 kPa组比较，(3)P<0.05

, figureFileSmall=IG8x8hDJDL0ij3SglMhv+w==, figureFileBig=3chUq87WCK8e5HUTMhbRaw==, tableContent=null), ArticleFig(id=1198602013492740850, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198602002860179850, language=EN, label=Fig.2, caption=Effects of nootkatone on depression-like behavior in bTBI rat models (n=10), figureFileSmall=R8/Qap/qOiEJDKrPdm4SWQ==, figureFileBig=aHamLBPrVwD7dwGXH0L5qw==, tableContent=null), ArticleFig(id=1198602013605987065, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198602002860179850, language=CN, label=图2, caption=诺卡酮对bTBI大鼠抑郁样行为的影响(n=10)

bTBI. 脑爆震伤；NKT. 诺卡酮；A. 悬尾实验的不动时间；B. 强迫游泳实验的潜伏期；C. 强迫游泳实验的不动时间；与假手术组比较，(1)P<0.05；与bTBI组比较，(2)P<0.05

, figureFileSmall=R8/Qap/qOiEJDKrPdm4SWQ==, figureFileBig=aHamLBPrVwD7dwGXH0L5qw==, tableContent=null), ArticleFig(id=1198602013756982017, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198602002860179850, language=EN, label=Fig.3, caption=Effects of nootkatone on PKA, pCREB/CREB and BDNF expression in rat hippocampus (n=4), figureFileSmall=9148dj61rntskJR4ZtAZcw==, figureFileBig=q50wAezO9sXm3Wew5myF/w==, tableContent=null), ArticleFig(id=1198602013870228231, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198602002860179850, language=CN, label=图3, caption=诺卡酮对bTBI大鼠海马区PKA、pCREB/CREB和BDNF蛋白表达的影响(n=4)

bTBI. 脑爆震伤；NKT. 诺卡酮；PKA. 蛋白激酶A；pCREB. 磷酸化环磷腺苷效应元件结合蛋白；BDNF. 脑源性神经营养因子；与假手术组比较，(1)P<0.05；与bTBI组比较，(2)P<0.05

, figureFileSmall=9148dj61rntskJR4ZtAZcw==, figureFileBig=q50wAezO9sXm3Wew5myF/w==, tableContent=null), ArticleFig(id=1198602014008640271, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198602002860179850, language=EN, label=Fig.4, caption=Effects of nootkatone on neurogenesis in DG region of hippocampus of bTBI rats (n=6), figureFileSmall=SbGsy2HTin+FR5T7gLRYoA==, figureFileBig=rjdKJCvnxSspHTQNF6ESWw==, tableContent=null), ArticleFig(id=1198602014113497879, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198602002860179850, language=CN, label=图4, caption=诺卡酮对bTBI大鼠海马DG区神经发生的影响(n=6)

bTBI. 脑爆震伤；NKT. 诺卡酮；DG. 齿状回区；PCNA. 增殖细胞核抗原；A. 海马DG区PCNA阳性细胞染色图；B. 海马DG区PCNA阳性细胞定量分析；与假手术组比较，(1)P<0.05；与bTBI组比较，(2)P<0.05

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诺卡酮对轻度脑爆震伤大鼠抑郁样行为的缓解作用及其机制
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范小琳 , 王鸿 , 王琪 , 李存治 , 卢青 , 李亮 , 马宁 , 高俊宏 *
解放军医学杂志 | 基础研究 2024,49(6): 694-700
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解放军医学杂志 | 基础研究 2024, 49(6): 694-700
诺卡酮对轻度脑爆震伤大鼠抑郁样行为的缓解作用及其机制
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范小琳, 王鸿, 王琪, 李存治, 卢青, 李亮, 马宁, 高俊宏*
作者信息
  • 兵器工业卫生研究所，陕西西安 710065

    • 范小琳，医学硕士，工程师，主要从事武器装备生物效应的评估研究

通讯作者:

高俊宏，E-mail：
Mitigative effect and mechanism of nootkatone on depression-like behavior in mild blast traumatic brain injury rat
Xiao-Lin Fan, Hong Wang, Qi Wang, Cun-Zhi Li, Qing Lu, Liang Li, Ning Ma, Jun-Hong Gao*
Affiliations
  • Institute for Hygiene of Ordnance Industry, Xi'an, Shaanxi 710065, China
出版时间: 2024-06-28 doi: 10.11855/j.issn.0577-7402.0371.2023.0831
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摘要
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目的 探究诺卡酮(NKT)对轻度脑爆震伤(bTBI)大鼠抑郁样行为的缓解作用及其机制。方法 采用生物激波管分别模拟爆炸超压(BOP)为60 kPa、90 kPa和120 kPa的冲击波建立大鼠bTBI抑郁样模型。BOP暴露后14 d，采用悬尾实验及强迫游泳实验对大鼠抑郁样行为进行评估，选取抑郁样行为最为明显的BOP(120 kPa)进行后续实验。30只大鼠随机分为假手术组、bTBI组(120 kPa BOP暴露)、bTBI+NKT组[120 kPa BOP暴露后第1天开始，经口给药给予NKT 10 mg/(kg·d)，共14 d]，每组10只。BOP暴露后14 d，采用悬尾实验及强迫游泳实验对大鼠抑郁样行为进行评估；采用Western blotting检测海马组织中蛋白激酶A(PKA)、磷酸化环磷腺苷效应元件结合蛋白(pCREB)及脑源性神经营养因子(BDNF)的表达水平；免疫组化检测海马齿状回区(DG)增殖细胞核抗原(PCNA)标记的神经发生情况。结果 90 kPa的BOP暴露即可引起大鼠抑郁样行为，而120 kPa组大鼠BOP暴露后产生的抑郁样行为更明显(P<0.05)，据此选取120 kPa的BOP暴露进行后续实验。BOP暴露后14 d，与假手术组比较，bTBI组大鼠悬尾实验不动时间延长(P<0.05)，强迫游泳实验潜伏期缩短，不动时间延长(P<0.05)，海马组织中PKA、pCREB和BDNF蛋白表达水平降低(P<0.05)，海马DG区PCNA阳性神经元数量减少(P<0.05)；与bTBI组比较，bTBI+NKT组大鼠悬尾实验不动时间缩短(P<0.05)，强迫游泳实验潜伏期延长，不动时间缩短(P<0.05)，海马组织中PKA、pCREB和BDNF蛋白表达水平升高(P<0.05)，海马DG区PCNA阳性神经元数量增加(P<0.05)。结论 早期给予NKT治疗可缓解轻度bTBI大鼠的抑郁样行为，其机制可能与NKT通过激活海马PKA/CREB/BDNF信号通路，使pCREB和BDNF表达水平上调，进而促进海马DG区神经发生有关。

脑爆震伤  /  抑郁  /  PKA/CREB/BDNF通路  /  海马  /  爆炸冲击波

Objective To investigate the mechanism of nootkatone (NKT) in mitigating depression-like behavior caused by blast traumatic brain injury (TBI). Methods The rat bTBI depression-like model was established by simulating the shock wave parameters of blast overpressure (BOP of 60 kPa, 90 kPa, and 120 kPa) with a biological shock wave tube. After 14 days of exposure, we evaluated the depression-like behavior of rats using the tail suspension test and forced swimming test. We identified that the BOP (120 kPa) condition caused the most noticeable depressive behavior and used this condition for subsequent experiments. Thirty male SD rats were randomly divided into sham operation group, bTBI group (BOP of 120 kPa), and bTBI+NKT group [at 1 d after exposure to BOP of 120 kPa, giving NKT 10 mg/(kg·d) orally for 14 days], 10 in each group. After 14 days of exposure, the depression-like behavior of rats was evaluated by tail suspension test and forced swimming test. The expression levels of protein kinase A (PKA), phosphorylated cyclic adenosine monophosphate effector binding protein (pCREB), and brain-derived neurotrophic factor (BDNF) in the hippocampus of rat were determined by Western blotting. Immunohistochemistry was used to detect the generation of proliferating cell nuclear antigen (PCNA)-labeled neurons in the hippocampal dentate gyrus (DG). Results BOP of 90 kPa can cause depression-like in rats and BOP of 120 kPa can cause the most noticeable depressive behavior (P<0.05). Therefore, we selected the BOP exposure of 120 kPa for subsequent experiments. After 14 days of BOP exposure, compared with sham operation group, the immobility time of tad suspension test in bTBI group was prolonged (P<0.05), the latency of for ced swimming test was shortened, the immobility time was prolonged (P<0.05), the expression levels of PKA, pCREB and BDNF protein in hippocampus were lowered (P<0.05), and the number of PCNA-labeled neurons in hippocampal DG area was reduced (P<0.05); compared with the bTBI group, the immobility time of tail suspension test in bTBI+NKT group was shortened (P<0.05), the latency of forced swimming test was prolonged, the immobility time was shortened (P<0.05), the expression levels of PKA, pCREB and BDNF protein in hippocampus were increased (P<0.05), and the number of PCNA-labeled neurons in hippocampal DG area was increased (P<0.05). Conclusions Early treatment with NKT can improve depression-like behavior in mild bTBI rats. The mechanism may be related to the up-regulation of the PKA-CREB-BDNF signaling pathway and increased expression levels of pCREB and BDNF in the hippocampus, which results in increased neuron numbers in the DG region of the hippocampus.

blast traumatic brain injury  /  depression  /  PKA/CREB/BDNF signaling pathway  /  hippocampal  /  blast shock wave
范小琳, 王鸿, 王琪, 李存治, 卢青, 李亮, 马宁, 高俊宏. 诺卡酮对轻度脑爆震伤大鼠抑郁样行为的缓解作用及其机制. 解放军医学杂志, 2024 , 49 (6) : 694 -700 . DOI: 10.11855/j.issn.0577-7402.0371.2023.0831
Xiao-Lin Fan, Hong Wang, Qi Wang, Cun-Zhi Li, Qing Lu, Liang Li, Ning Ma, Jun-Hong Gao. Mitigative effect and mechanism of nootkatone on depression-like behavior in mild blast traumatic brain injury rat[J]. Medical Journal of Chinese People’s Liberation Army, 2024 , 49 (6) : 694 -700 . DOI: 10.11855/j.issn.0577-7402.0371.2023.0831
正文
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脑爆震伤(blast traumatic brain injury，bTBI)是指由爆炸瞬间产生的复杂压力波直接作用造成的颅脑损伤[1]。随着全球恐怖袭击和局部冲突事件的频发，创伤性脑损伤(traumatic brain injury，TBI)病例数不断增加，且已经成为士兵的一种标志性损伤。在伊拉克和阿富汗战争期间(2001-2011)，约417 503名美国武装部队成员在服役期间至少遭受过一次脑外伤，其中近2/3涉及爆炸事件，遭受爆炸的人员中约83.3%被诊断为轻微的、不复杂的bTBI或脑震荡[2-4]。许多在全球反恐战争中遭受过轻度bTBI的士兵在回国后会出现慢性精神障碍，如抑郁和认知障碍等[2,5-6]。然而，导致轻度bTBI后抑郁和认知障碍的机制尚不清楚。近年来，神经再生在抗抑郁机制中的作用受到关注。研究发现，TBI后，神经发生下脑室下区(subventricular zone，SVZ)和海马齿状回区(dentate gyrus，DG)，且神经发生持续时间分别至少为2周或4周[7]。也有研究发现，抑郁与海马体的神经发生呈负相关[8-12]。目前大多数抗抑郁药物的作用机制均涉及海马DG区神经发生的激活[13]。多项研究发现，神经发生与脑源性神经营养因子(brain-derived neurotrophic factor，BDNF)密切相关[9-10,14]。BDNF的表达涉及磷酸化环磷酸腺苷反应元件结合蛋白(phosphrylated cyclic adenosine monophosphate response element binding，pCREB)，而pCREB也参与了抑郁和抗抑郁类反应[15-16]。研究表明，pCREB在TBI后海马神经发生中发挥着重要作用[17-18]。本课题组前期研究利用实弹爆炸成功建立轻度bTBI大鼠模型，评估了爆炸超压(blast overpressure，BOP)暴露后大鼠的抑郁样行为，并对海马组织中环磷酸腺苷(cAMP)/蛋白激酶A(PKA)/环磷腺苷效应元件结合蛋白(CREB)/BDNF信号通路进行检测；结果表明，单次BOP暴露后，大鼠出现抑郁样行为，同时海马组织中cAMP/PKA/CREB/BDNF信号通路被抑制[19]，提示轻度bTBI致抑郁样行为可能与cAMP/PKA/CREB/BDNF信号通路相关蛋白表达水平的下调有关。诺卡酮(nootkatone，NKT)是一种天然存在的倍半萜烯类中草药提取物，具有多种药理特性，如益智、杀菌、抗氧化和抗过敏等[20]。研究发现，NKT能显著改善阿尔茨海默病小鼠的神经行为表现[21]，其在脂多糖诱导的神经炎症中可激活PKA/CREB信号通路发挥抗炎作用[22]。王凯新等[23]发现，在不可预知应激模型中，NKT可激活海马PKA/CREB/BDNF信号通路，促进DG区神经再生，从而缓解小鼠的抑郁症状。由此推测，NKT可能对bTBI造成的抑郁样行为具有治疗作用，其机制可能与海马PKA/CREB/BDNF信号通路的激活和神经发生相关。本研究探讨NKT改善轻度bTBI大鼠抑郁样行为的作用机制，以期为新型抗抑郁药的开发提供理论依据。
1 材料与方法
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1.1 实验动物
雄性10周龄SD大鼠[体重(200~240) g]70只，购自北京斯贝福生物技术有限公司[实验动物生产许可证号：SCXK(京)2019-0010]。所有大鼠均给予充足的食物和水，每笼5只，环境为12 h/12 h光暗循环，室内温度(22~26) ℃、湿度40%~60%。本研究通过兵器工业卫生研究所实验动物伦理委员会批准(批件号IACUC202107)，实验过程符合国家和单位有关实验动物的管理和使用规定。
1.2 实验试剂
NKT(批号：HY-N2195，纯度97%以上)购自美国Med Chem ExPress公司，溶解于0.5%羧甲基纤维素钠溶液中；细胞核和细胞质蛋白提取试剂盒、BCA蛋白测定试剂盒、DAB辣根过氧化物酶显色试剂盒等购自上海酶联生物科技有限公司；兔源Anti-PKA、Anti-CREB、Anti-pCREB、Anti-BDNF和Anti-GAPDH抗体购自美国CST公司；增殖细胞核抗原(proliferating cell nuclear antigen，PCNA)细胞增殖检测试剂盒购自生工生物工程(上海)股份有限公司。
1.3 bTBI模型制备
取40只SD大鼠，分为60 kPa组、90 kPa组、120 kPa组与假手术组，每组10只。60 kPa组、90 kPa组、120 kPa组根据文献[24]的方法采用生物激波管构建bTBI模型，压力峰值分别为60 kPa、90 kPa和120 kPa。造模前，腹腔注射氯胺酮与甲苯噻嗪合剂[10:1 (100 mg/10 mg/kg)] 0.1 ml/100 g麻醉大鼠，采用俯卧位测试，并用防冲击海绵裹住躯干(防止躯干冲击伤)，暴露头部朝向冲击波发射口，然后施加一次BOP。假手术组大鼠仅接受麻醉和噪声暴露，不接受冲击波暴露，即将大鼠放置在生物激波管旁边。作为质量控制措施，本研究使用的压力传感器为PCB压电型(Depew，NY，113B28)。所有数据在2.0 MHz频率下采样记录，单次采集时间为200 ms。
1.4 NKT干预
采用3种不同压力(60、90和120 kPa)建模后，选取大鼠抑郁样行为最为明显的压力(120 kPa)用于NKT干预研究。取30只SD大鼠分为假手术组、bTBI组、bTBI+NKT组，每组10只。NTK干预剂量参考文献[25]，准确称取0.1 g NKT粉末加入100 ml 0.5%羧甲基纤维素钠溶液中混匀，终浓度为1 mg/ml。暴露结束后第1天起，bTBI+NKT组以10 mg/(kg·d)的剂量连续经口给药14 d，假手术组和bTBI组连续经口给予等体积的0.5%羧甲基纤维素钠溶液14 d。
1.5 大鼠行为学检测
悬尾实验和强迫游泳实验是评估实验动物抑郁样行为的常用方法[26-27]。BOP暴露后14 d，利用悬尾实验和强迫游泳实验进行大鼠行为学检测。
悬尾实验：用胶带将松紧带固定在大鼠尾部(距尾尖约1 cm处)，并将松紧带钩在水平杆上，使大鼠处于倒挂状态，采用盲法观察并记录6 min内大鼠的累积不动时间。
强迫游泳实验：将大鼠放置在含水[温度：(25±1) ℃；深度：15 cm]的塑料圆柱体(高：30 cm；直径：20 cm)中测试6 min游泳，采用盲法观察并记录大鼠前2 min内首次出现静止不动的时间，即潜伏期，后4 min内大鼠的累积不动时间(大鼠在水中停止挣扎，身体保持漂浮状态或有轻微的肢体活动，头部露出水面，被认定为不动行为)。
1.6 Western blotting检测大鼠海马组织PKA、CREB、pCREB和BDNF蛋白表达水平
BOP暴露后14 d，深度麻醉下颈椎脱位处死大鼠，分离海马组织。用含有蛋白酶和磷酸酶抑制剂的RIPA缓冲液提取总蛋白。用BCA试剂测定蛋白总浓度，将蛋白浓度归一化后，取30 μg蛋白样品经聚丙烯酰胺凝胶电泳转移到PVDF膜(Millipore，IPVH00010，USA)上，用5%脱脂奶粉室温封闭2 h；加入兔抗PKA(1:2000)、CREB(1:2000)、pCREB(1:2000)、BDNF(1:2000)和GAPDH(1:4000)一抗4 ℃孵育过夜；次日用TBST洗膜，加入辣根过氧化物酶标记的羊抗兔二抗(1:5000)室温孵育2 h；TBST洗膜后，用增强型化学发光检测试剂观察抗体反应条带。应用Tanon 5200凝胶成像系统获得图像，Image-pro Plus 6.0软件进行半定量分析。
1.7 免疫组化检测大鼠海马DG区PCNA阳性细胞
BOP暴露后14 d，深度麻醉下颈椎脱位处死大鼠，取全脑组织于4%多聚甲醛溶液中室温固定48 h后，进行组织脱水、石蜡包埋。将石蜡包埋的脑组织做冠状切片，切片厚度为5 μm，置于60 ℃恒温烤箱2 h，脱蜡、复水后，用3%过氧化氢甲醇阻断内源性过氧化物酶5 min，再用10%山羊血清37 ℃孵育30 min；加入兔抗PCNA(1:500，用5% BSA稀释) 4 ℃孵育过夜；次日PBS冲洗5 min，与生物素化兔抗山羊IgG在37 ℃孵育30 min，再次PBS冲洗5 min；去除PBS后，加入DAB，梯度脱水(75%乙醇5 min，85%乙醇5 min，95%乙醇5 min，100%乙醇5 min)；二甲苯中浸泡15 min，吸水纸吸去多余液体；封片后，使用Leica DM500相机拍片，使用Image-pro Plus 6.0软件进行分析。每只大鼠选用3张切片。
1.8 统计学处理
采用SPSS 20.0软件进行统计分析。应用Shapiro-Wilk检验各组数据的正态分布情况，所有数据均符合正态分布并以$\bar{x}±s$表示。多组间比较采用单因素方差分析(one-way ANOVA)，进一步两两比较采用Turkey法。P<0.05为差异有统计学意义。
2 结果
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2.1 不同BOP暴露对大鼠抑郁样行为的影响
悬尾实验结果显示，BOP暴露后14 d，假手术组、60 kPa组、90 kPa组和120 kPa组大鼠不动时间分别为(182.2±24.4) s、(181.9±30.2) s、(210.7±25.6) s和(225.3±35.0) s。120 kPa组不动时间长于假手术组和60 kPa组，差异有统计学意义(P<0.05，图1A)。
强迫游泳实验结果显示，BOP暴露后14 d，假手术组、60 kPa组、90 kPa组和120 kPa组大鼠强迫游泳潜伏期分别为(96.8±12.6) s、(92.8±10.5) s、(68.6±15.3) s和(51.0±10.1) s，不动时间分别为(78.7±23.9) s、(86.8±11.3) s、(102.6±14.6) s和(103.9±16.7) s。与假手术组比较，90 kPa组和120 kPa组强迫游泳潜伏期缩短(P<0.05)，不动时间延长(P<0.05)；与60 kPa组比较，90 kPa组和120 kPa组强迫游泳潜伏期缩短(P<0.05)，不动时间延长(P<0.05)；与90 kPa组比较，120 kPa组强迫游泳潜伏期缩短(P<0.05，图1B、C)。
以上结果表明，90 kPa的BOP暴露即可引起大鼠的抑郁样行为，且120 kPa组大鼠BOP暴露后产生的抑郁样行为更明显，据此选取120 kPa的BOP暴露进行后续实验。
2.2 NKT对bTBI大鼠抑郁样行为的影响
悬尾实验结果显示，NKT干预对bTBI大鼠不动时间具有明显影响(F=11.50，P<0.05)。与假手术组比较，bTBI组(120 kPa)大鼠不动时间延长(P<0.05)；与bTBI组(120 kPa)相比，bTBI+NKT组大鼠不动时间缩短(P<0.05，图2A)。
强迫游泳实验结果显示，NKT干预对bTBI大鼠的潜伏期和不动时间具有明显影响(F=20.32，P<0.05；F=6.37，P<0.05)。与假手术组比较，bTBI组(120 kPa)大鼠潜伏期缩短，不动时间延长(P<0.05)；与bTBI组(120 kPa)比较，bTBI+NKT组大鼠潜伏期延长，不动时间缩短(P<0.05，图2B、C)。
2.3 NKT对bTBI大鼠海马组织中PKA/CREB/BDNF信号通路相关蛋白表达的影响
Western blotting检测结果显示，压力峰值为120 kPa的BOP暴露后14 d，NKT对bTBI大鼠海马组织中PKA、pCREB及BDNF蛋白表达水平有影响(F=43.49，P<0.05；F=4.38，P<0.05；F=58.66，P<0.05)。与假手术组比较，bTBI组海马组织中PKA、pCREB/CREB及BDNF蛋白表达水平降低(P<0.05)；与bTBI组比较，bTBI+NKT组海马组织中PKA、pCREB/CREB及BDNF蛋白表达水平升高(P<0.05，图3)。
2.4 NKT对bTBI大鼠海马DG区神经发生的影响
压力峰值为120 kPa的BOP暴露后14 d，NKT对PCNA阳性神经元数量有影响(F=22.63，P<0.05)。与假手术组比较，bTBI组海马DG区PCNA阳性神经元(黄色)数量减少(P<0.05)；与bTBI组比较，bTBI+NKT组海马DG区PCNA阳性神经元数量增多(P<0.05，图4)。
3 讨论
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本研究结果显示，NKT早期治疗可显著改善轻度bTBI大鼠的抑郁样行为。悬尾实验及强迫游泳实验结果显示，bTBI组大鼠不动时间延长，潜伏期缩短，而NKT治疗可减轻bTBI大鼠的抑郁样行为。表明在抑郁症状发生前予以NKT，或许能预防轻度bTBI后急性期抑郁样行为的发生。
研究发现，NKT的抗炎作用可通过下调PI3K/Akt、NF-κB和p38 MAPK并上调PKA/CREB信号通路介导[20]。cAMP/PKA/CREB是一条重要的抗炎信号通路，cAMP通过激活位点Thr197诱导下游蛋白PKA的激活，PKA通过激活位点Ser133激活CREB，激活的CREB通过核易位从细胞质进入细胞核，诱导细胞因子的表达[28]。目前，大多数抗抑郁药物都依赖于PKA/CREB/BDNF通路，进而调节下游突触的传递[29]，其中BDNF是神经系统营养因子家族中重要的一员，广泛分布于哺乳动物中枢神经系统中，且大脑皮层和海马中含量最为丰富[30]。BDNF与其特异性受体结合后能激活下游多条信号通路，进而发挥多种生物学功能。大量研究表明，BDNF及其下游通路不仅在神经元生长、发育、分化及轴突、树突发育中发挥重要作用[31]，而且与抑郁症[32]等多种神经及精神疾病的发生发展有关。pCREB也是海马神经发生的相关因素，在小鼠TBI模型中，海马组织中pCREB表达水平下降[33]。Seno等[34]通过激光诱导BOP建立小鼠bTBI模型，在损伤后28 d发现小鼠出现明显的抑郁样行为，同时海马组织中pCREB、BDNF表达水平明显下降，而给予5-羟色胺重吸收抑制剂治疗能明显上调海马组织中pCREB、BDNF的表达水平并促进海马DG区神经发生的增加，最终改善bTBI小鼠的抑郁样行为。本研究结果显示，NKT连续干预14 d后，bTBI大鼠海马组织中PKA/CREB/BDNF信号通路相关蛋白表达发生变化，bTBI组大鼠海马组织中PKA、pCREB、BDNF蛋白表达水平较假手术组明显下降，而bTBI+NKT组上述蛋白表达水平较bTBI组明显升高。表明早期给予NKT治疗能明显上调bTBI大鼠海马组织中BDNF、pCREB的表达水平。
神经发生是新神经元从神经干细胞或前体细胞分化出来的一种生理现象，主要发生在胚胎期和胎儿期。新神经元随着个体的发育而减少，但即使在成熟后，海马和SV2中的神经发生仍然存在。近年来，神经发生在抗抑郁机制中的作用受到关注。有研究发现，慢性抗抑郁药物的行为改善效应可能是通过刺激海马神经发生介导的[9,35]。因此，本研究观察了NKT治疗14 d后海马DG区的神经发生标志物PCNA的表达情况，进一步探索轻度bTBI抑郁样行为恢复的潜在机制。结果显示，BOP暴露后14 d，bTBI+NKT组海马DG区PCNA阳性神经元数量较bTBI组明显增多。表明早期NKT治疗可激活海马DG区的神经发生。
本研究具有一定局限性：(1)基于激波管模拟的爆炸环境，毁伤元较单一，难以完全复现实弹爆炸建立的bTBI模型；(2)仅观察了NKT干预bTBI大鼠损伤后的抑郁症状和cAMP/PKA/CREB/BDNF信号通路相关蛋白的变化，仅能推测NKT干预对bTBI致抑郁样行为的变化可能与cAMP/PKA/CREB/BDNF信号通路相关蛋白表达水平的上调有关，未来应进一步对cAMP/PKA/CREB/BDNF信号通路进行人为阻断并观察NKT对bTBI大鼠损伤后抑郁症状的影响。
综上所述，本研究结果表明，早期给予NKT治疗可改善轻度bTBI大鼠的抑郁样行为，其机制可能与NKT通过激活海马PKA/CREB/BDNF信号通路，使pCREB和BDNF表达水平上调，进而促进海马DG区神经发生有关。
基金
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  • 陕西省自然科学基金项目(2023-JC-QN-0983)
  • 陕西省自然科学基金项目(2023-JC-YB-684)
文献
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doi: 10.11855/j.issn.0577-7402.0371.2023.0831
  • 接收时间：2023-03-11
  • 首发时间：2025-11-21
  • 出版时间：2024-06-28
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  • 收稿日期：2023-03-11
  • 录用日期：2023-06-27
基金
Natural Science Foundation of Shaanxi Province(2023-JC-QN-0983)
陕西省自然科学基金项目(2023-JC-QN-0983)
Natural Science Foundation of Shaanxi Province(2023-JC-YB-684)
陕西省自然科学基金项目(2023-JC-YB-684)
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    兵器工业卫生研究所，陕西西安 710065

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