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Article(id=1207416370262810947, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1207416365246419268, articleNumber=null, orderNo=null, doi=10.11855/j.issn.0577-7402.2022.09.0886, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1638979200000, receivedDateStr=2021-12-09, revisedDate=null, revisedDateStr=null, acceptedDate=1647273600000, acceptedDateStr=2022-03-15, onlineDate=1765800095382, onlineDateStr=2025-12-15, pubDate=1664294400000, pubDateStr=2022-09-28, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1765800095382, onlineIssueDateStr=2025-12-15, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1765800095382, creator=13701087609, updateTime=1765800095382, updator=13701087609, issue=Issue{id=1207416365246419268, tenantId=1146029695717560320, journalId=1189873630562394117, year='2022', volume='47', issue='9', pageStart='851', pageEnd='956', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=0, createTime=1765800094186, creator=13701087609, updateTime=1765800167087, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1207416671069904914, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1207416365246419268, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1207416671069904915, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1207416365246419268, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=886, endPage=892, ext={EN=ArticleExt(id=1207416370770321739, articleId=1207416370262810947, tenantId=1146029695717560320, journalId=1189873630562394117, language=EN, title=Effect and mechanism of HMB on ICU acquired weakness associated with ARDS, columnId=1190310110212751762, journalTitle=Medical Journal of Chinese People’s Liberation Army, columnName=Basic Research, runingTitle=null, highlight=null, articleAbstract=

Objective To explore the role and mechanism of β-hydroxy-β-methyl butyric acid (HMB) in intensive care unit-acquired weakness (ICU-AW) associated with acute respiratory distress syndrome (ARDS). Methods Forty SPF grade male C57BL/6 mice were randomly divided into control group, sham operation group, model group, and HMB group, with 10 mice in each group. Model group and HMB group were treated with 3 μg/g lipopolysaccharide (LPS) by intratracheal injection to prepare the ICU-AW model associated with ARDS. Sham operation group received the same amount of sterile water. No procedures for control group. On the second day of modeling, mice in HMB group were given 340 mg/(kg·d) HMB by intragastric administration,and mice in the other three groups were given an equal volume of normal saline for continuous intragastric administration for two weeks. Additional 20 mice were randomized into the ARQ-092 group and Akt inhibitor control group, with 10 mice in each group.On the second day of modeling, both groups were given Akt inhibitor (ARQ-092 group) or an equivalent volume of the carrier (Akt inhibitor control group) orally for 10 hours after HMB intragastric administration for 12 days. We evaluated the grasping force of forelimb muscles and measured the sarcopenia index (SI). HE staining was used to observe the pathological changes in lung and muscle tissues. The mRNA expressions of Akt, FoxO3a, Atrogin1, and MuRF1 in mouse gastrocnemius were tested by qRT-PCR, and the expression levels of Akt/FoxO3a pathway related proteins in mouse gastrocnemius was further detected by Western blotting. Results Compared with the model group, the grasping force and SI of forelimb muscle in HMB group were significantly higher(P<0.05). HE staining revealed regular lung tissue structure in control group and sham operation group. Alveolar septa in model group were thickened and fractured, with structural disorder and inflammatory cell infiltration. The injury degree of lung tissue in HMB group was lighter compared with the model group. We observed normal phenotypes of the muscle tracts of gastrocnemius in control group and sham operation group. In model group, we detected muscle fiber atrophy and decreased quantity, muscle bundle structure destruction, and decreased cross-sectional area. The injury degree of the gastrocnemius muscle in HMB group was mild. In addition, compared with model group, the mRNA expressions of Akt and FoxO3a in the gastrocnemius of HMB group were significantly increased (P<0.05), and the phosphorylation levels of Akt and FoxO3a protein were also increased (P<0.05), the levels of Atrogin1 and MuRF1 mRNA and protein expressions decreased (P<0.05). Conclusion HMB can play a protective role in ICU-AW by regulating the Akt-FoxO3A-MurF1/Atrogin1 signaling pathway, which may be valuable for ICU-AW prevention and treatment. The Akt inhibitor ARQ-092 reversed the protective effect of HMB.

, correspAuthors=Jian Feng, Fu-Xiang Li, authorNote=null, correspAuthorsNote=
* Li Fu-Xiang, E-mail: ;
Feng Jian, E-mail:
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目的 探讨β-羟基-β-甲基丁酸(HMB)在小鼠急性呼吸窘迫综合征(ARDS)相关ICU获得性衰弱(ICU-AW)中的作用及其机制。方法 将40只SPF级雄性C57BL/6小鼠随机分为对照组、假手术组、模型组及HMB组，每组10只。模型组及HMB组小鼠在气管内注入3 μg/g脂多糖(LPS)，制备ARDS相关ICU-AW模型，假手术组注入等量无菌水，对照组不予操作。造模第2天，HMB组给予340 mg/(kg·d) HMB灌胃，其余3组给予等体积生理盐水，连续灌胃2周。另取与HMB组相同处理的小鼠20只，随机分为ARQ-092组与Akt抑制剂对照组，每组10只。从造模第2天开始，每天在HMB灌胃10 h后口服Akt抑制剂(ARQ-092组)或等体积载体(Akt抑制剂对照组)，持续给药12 d。测量各组小鼠前肢肌肉抓力、肌肉减少指数(SI)；HE染色观察肺组织及肌肉组织病理变化；qRT-PCR检测小鼠腓肠肌中Akt、FoxO3a、Atrogin1及MuRF1的mRNA表达水平；Western blotting检测小鼠腓肠肌中Akt/FoxO3a通路相关蛋白表达水平。结果 HMB组小鼠的前肢肌肉抓力及SI均明显高于模型组(P<0.05)。HE染色结果显示，对照组及假手术组肺组织结构正常；模型组肺泡间隔可见明显增厚、断裂，结构紊乱，炎性细胞浸润；HMB组肺组织损伤程度较模型组轻。对照组及假手术组小鼠的腓肠肌肌束结构正常；模型组出现肌纤维萎缩、数量减少，肌束结构破坏，横截面积减少；HMB组小鼠腓肠肌损伤程度较轻。与模型组比较，HMB组小鼠腓肠肌中Akt及FoxO3a mRNA表达水平均明显升高(P<0.05)，Akt及FoxO3a蛋白磷酸化水平也明显升高(P<0.05)，而Atrogin1及MuRF1的mRNA及蛋白表达水平均明显降低(P<0.05)。结论 HMB可通过调控Akt-FoxO3a-MuRF1/Atrogin1信号通路在ICU-AW中发挥保护作用，可能对ICU-AW的防治具有重要价值，而Akt抑制剂ARQ-092能够逆转HMB的此种保护作用。

, correspAuthors=冯健, 李福祥, authorNote=null, correspAuthorsNote=
李福祥，E-mail：;
冯健，E-mail：
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潘晓佳，硕士研究生，主要从事重症医学方面的研究

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潘晓佳，硕士研究生，主要从事重症医学方面的研究

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潘晓佳，硕士研究生，主要从事重症医学方面的研究

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HMB. β-羟基-β-甲基丁酸

, figureFileSmall=h3T7UBqTiNuIrItBr7RnYQ==, figureFileBig=HQnSniL+L+SZAgNaHJ/Nyg==, tableContent=null), ArticleFig(id=1207416377409905370, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1207416370262810947, language=EN, label=Fig. 2, caption=Comparison of grasping force (A) and SI (B) of mice in each group (n=10), figureFileSmall=R/21IYgCH6FSQT5OR3MIDQ==, figureFileBig=ryxxCXLFu/ihA5oqBICFsQ==, tableContent=null), ArticleFig(id=1207416378605282018, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1207416370262810947, language=CN, label=图2, caption=各组小鼠抓力值(A)及SI(B)比较(n=10)

SI. 肌肉减少指数；HMB. β-羟基-β-甲基丁酸；与假手术组比较，(1)P<0.05；与模型组比较，(2)P<0.05

, figureFileSmall=R/21IYgCH6FSQT5OR3MIDQ==, figureFileBig=ryxxCXLFu/ihA5oqBICFsQ==, tableContent=null), ArticleFig(id=1207416378680779496, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1207416370262810947, language=EN, label=Fig. 3, caption=Effects of HMB intervention on mRNA and protein expression of Akt-FoxO3a-MuRF1/Atrogin1 signaling pathway, figureFileSmall=78EcuqcCMxrCGS70mz3SOg==, figureFileBig=jgncNiB5DNnCvDeP+sWM1w==, tableContent=null), ArticleFig(id=1207416378773054192, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1207416370262810947, language=CN, label=图3, caption=HMB干预对Akt-FoxO3a-MuRF1/Atrogin1信号通路mRNA及蛋白表达的影响

HMB. β-羟基-β-甲基丁酸；A. qRT-PCR；B. Western blotting；C. 蛋白相对表达量；与假手术组比较，(1)P<0.05；与模型组比较，(2)P<0.05

, figureFileSmall=78EcuqcCMxrCGS70mz3SOg==, figureFileBig=jgncNiB5DNnCvDeP+sWM1w==, tableContent=null), ArticleFig(id=1207416378882106104, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1207416370262810947, language=EN, label=Fig. 4, caption=Effect of Akt inhibitor ARQ-092 on HMB protection, figureFileSmall=BrMg/M1AKGHrLb1cgKYByQ==, figureFileBig=gECoh7+y4Zr2bSJ4O8Nhew==, tableContent=null), ArticleFig(id=1207416378982769406, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1207416370262810947, language=CN, label=图4, caption=Akt抑制剂ARQ-092对HMB保护作用的影响

HMB. β-羟基-β-甲基丁酸；A. 小鼠抓力值(n=10)；B. 小鼠SI (n=10)；C. 腓肠肌组织病理图(HE)；D. qRT-PCR；E. Western blotting；F. 蛋白相对表达量；与ARQ-092组比较，(1)P<0.05

, figureFileSmall=BrMg/M1AKGHrLb1cgKYByQ==, figureFileBig=gECoh7+y4Zr2bSJ4O8Nhew==, tableContent=null), ArticleFig(id=1207416379079238406, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1207416370262810947, language=EN, label=Tab. 1, caption=

Primer sequences of genes

, figureFileSmall=null, figureFileBig=null, tableContent=
基因引物序列(5'-3')
Akt正义：TCAGGATGTGGATCAGCGAGAGTC
反义：AGGCAGCGGATGATAAAGGTGTTG
FoxO3a正义：CTGGGGGAACCTGTCCTATG
反义：TCATTCTGAACGCGCATGAAG
Atrogin1正义：ACGGGAACTTCTCCAGACTCTCTAC
反义：CTGCTGCCAGTGTAGAATGGTCTC
MuRF1正义：CCTGATGGAAACGCTATGGAGAACC
反义：GGATTCGCAGCCTGGAAGATGTC
GAPDH正义：TTGTGATGGGTGTGAACCACGAGA
反义：CATGAGCCCTTCCACAATGCCAAA
), ArticleFig(id=1207416379192484619, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1207416370262810947, language=CN, label=表1, caption=

基因引物序列

, figureFileSmall=null, figureFileBig=null, tableContent=
基因引物序列(5'-3')
Akt正义：TCAGGATGTGGATCAGCGAGAGTC
反义：AGGCAGCGGATGATAAAGGTGTTG
FoxO3a正义：CTGGGGGAACCTGTCCTATG
反义：TCATTCTGAACGCGCATGAAG
Atrogin1正义：ACGGGAACTTCTCCAGACTCTCTAC
反义：CTGCTGCCAGTGTAGAATGGTCTC
MuRF1正义：CCTGATGGAAACGCTATGGAGAACC
反义：GGATTCGCAGCCTGGAAGATGTC
GAPDH正义：TTGTGATGGGTGTGAACCACGAGA
反义：CATGAGCCCTTCCACAATGCCAAA
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HMB在小鼠急性呼吸窘迫综合征相关ICU获得性衰弱中的作用及其机制
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潘晓佳 1, 2 , 徐朝霞 2 , 林宁 3 , 林正霄 1, 2 , 赵磊 2 , 冯健 2, * , 李福祥 1, 2, *
解放军医学杂志 | 基础研究 2022,47(9): 886-892
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解放军医学杂志 | 基础研究 2022, 47(9): 886-892
HMB在小鼠急性呼吸窘迫综合征相关ICU获得性衰弱中的作用及其机制
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潘晓佳1, 2, 徐朝霞2, 林宁3, 林正霄1, 2, 赵磊2, 冯健2, * , 李福祥1, 2, *
作者信息
  • 1西南交通大学医学院，四川成都 610031
  • 2西部战区总医院重症医学科，四川成都 610083
  • 3西部战区总医院营养科，四川成都 610083

    • 潘晓佳，硕士研究生，主要从事重症医学方面的研究

通讯作者:

李福祥，E-mail：;
冯健，E-mail：
Effect and mechanism of HMB on ICU acquired weakness associated with ARDS
Xiao-Jia Pan1, 2, Chao-Xia Xu2, Ning Lin3, Zheng-Xiao Lin1, 2, Lei Zhao2, Jian Feng2, * , Fu-Xiang Li1, 2, *
Affiliations
  • 1School of Medicine, Southwest Jiaotong University, Chengdu, Sichuan 610031, China
  • 2Department of Intensive Care Medicine, General Hospital of Western Theater Command, Chengdu, Sichuan 610083, China
  • 3Department of Nutrition, General Hospital of Western Theater Command, Chengdu, Sichuan 610083, China
出版时间: 2022-09-28 doi: 10.11855/j.issn.0577-7402.2022.09.0886
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摘要
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目的 探讨β-羟基-β-甲基丁酸(HMB)在小鼠急性呼吸窘迫综合征(ARDS)相关ICU获得性衰弱(ICU-AW)中的作用及其机制。方法 将40只SPF级雄性C57BL/6小鼠随机分为对照组、假手术组、模型组及HMB组，每组10只。模型组及HMB组小鼠在气管内注入3 μg/g脂多糖(LPS)，制备ARDS相关ICU-AW模型，假手术组注入等量无菌水，对照组不予操作。造模第2天，HMB组给予340 mg/(kg·d) HMB灌胃，其余3组给予等体积生理盐水，连续灌胃2周。另取与HMB组相同处理的小鼠20只，随机分为ARQ-092组与Akt抑制剂对照组，每组10只。从造模第2天开始，每天在HMB灌胃10 h后口服Akt抑制剂(ARQ-092组)或等体积载体(Akt抑制剂对照组)，持续给药12 d。测量各组小鼠前肢肌肉抓力、肌肉减少指数(SI)；HE染色观察肺组织及肌肉组织病理变化；qRT-PCR检测小鼠腓肠肌中Akt、FoxO3a、Atrogin1及MuRF1的mRNA表达水平；Western blotting检测小鼠腓肠肌中Akt/FoxO3a通路相关蛋白表达水平。结果 HMB组小鼠的前肢肌肉抓力及SI均明显高于模型组(P<0.05)。HE染色结果显示，对照组及假手术组肺组织结构正常；模型组肺泡间隔可见明显增厚、断裂，结构紊乱，炎性细胞浸润；HMB组肺组织损伤程度较模型组轻。对照组及假手术组小鼠的腓肠肌肌束结构正常；模型组出现肌纤维萎缩、数量减少，肌束结构破坏，横截面积减少；HMB组小鼠腓肠肌损伤程度较轻。与模型组比较，HMB组小鼠腓肠肌中Akt及FoxO3a mRNA表达水平均明显升高(P<0.05)，Akt及FoxO3a蛋白磷酸化水平也明显升高(P<0.05)，而Atrogin1及MuRF1的mRNA及蛋白表达水平均明显降低(P<0.05)。结论 HMB可通过调控Akt-FoxO3a-MuRF1/Atrogin1信号通路在ICU-AW中发挥保护作用，可能对ICU-AW的防治具有重要价值，而Akt抑制剂ARQ-092能够逆转HMB的此种保护作用。

重症监护室获得性衰弱  /  急性呼吸窘迫综合征  /  肌肉萎缩  /  β-羟基-β-甲基丁酸  /  Akt/FoxO3a通路

Objective To explore the role and mechanism of β-hydroxy-β-methyl butyric acid (HMB) in intensive care unit-acquired weakness (ICU-AW) associated with acute respiratory distress syndrome (ARDS). Methods Forty SPF grade male C57BL/6 mice were randomly divided into control group, sham operation group, model group, and HMB group, with 10 mice in each group. Model group and HMB group were treated with 3 μg/g lipopolysaccharide (LPS) by intratracheal injection to prepare the ICU-AW model associated with ARDS. Sham operation group received the same amount of sterile water. No procedures for control group. On the second day of modeling, mice in HMB group were given 340 mg/(kg·d) HMB by intragastric administration,and mice in the other three groups were given an equal volume of normal saline for continuous intragastric administration for two weeks. Additional 20 mice were randomized into the ARQ-092 group and Akt inhibitor control group, with 10 mice in each group.On the second day of modeling, both groups were given Akt inhibitor (ARQ-092 group) or an equivalent volume of the carrier (Akt inhibitor control group) orally for 10 hours after HMB intragastric administration for 12 days. We evaluated the grasping force of forelimb muscles and measured the sarcopenia index (SI). HE staining was used to observe the pathological changes in lung and muscle tissues. The mRNA expressions of Akt, FoxO3a, Atrogin1, and MuRF1 in mouse gastrocnemius were tested by qRT-PCR, and the expression levels of Akt/FoxO3a pathway related proteins in mouse gastrocnemius was further detected by Western blotting. Results Compared with the model group, the grasping force and SI of forelimb muscle in HMB group were significantly higher(P<0.05). HE staining revealed regular lung tissue structure in control group and sham operation group. Alveolar septa in model group were thickened and fractured, with structural disorder and inflammatory cell infiltration. The injury degree of lung tissue in HMB group was lighter compared with the model group. We observed normal phenotypes of the muscle tracts of gastrocnemius in control group and sham operation group. In model group, we detected muscle fiber atrophy and decreased quantity, muscle bundle structure destruction, and decreased cross-sectional area. The injury degree of the gastrocnemius muscle in HMB group was mild. In addition, compared with model group, the mRNA expressions of Akt and FoxO3a in the gastrocnemius of HMB group were significantly increased (P<0.05), and the phosphorylation levels of Akt and FoxO3a protein were also increased (P<0.05), the levels of Atrogin1 and MuRF1 mRNA and protein expressions decreased (P<0.05). Conclusion HMB can play a protective role in ICU-AW by regulating the Akt-FoxO3A-MurF1/Atrogin1 signaling pathway, which may be valuable for ICU-AW prevention and treatment. The Akt inhibitor ARQ-092 reversed the protective effect of HMB.

ICU-acquired weakness  /  acute respiratry distress syndrme  /  muscular atrophy  /  β-hydroxy-β-methylbutyric acid  /  Akt/FoxO3a pathway
潘晓佳, 徐朝霞, 林宁, 林正霄, 赵磊, 冯健, 李福祥. HMB在小鼠急性呼吸窘迫综合征相关ICU获得性衰弱中的作用及其机制. 解放军医学杂志, 2022 , 47 (9) : 886 -892 . DOI: 10.11855/j.issn.0577-7402.2022.09.0886
Xiao-Jia Pan, Chao-Xia Xu, Ning Lin, Zheng-Xiao Lin, Lei Zhao, Jian Feng, Fu-Xiang Li. Effect and mechanism of HMB on ICU acquired weakness associated with ARDS[J]. Medical Journal of Chinese People’s Liberation Army, 2022 , 47 (9) : 886 -892 . DOI: 10.11855/j.issn.0577-7402.2022.09.0886
正文
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ICU获得性衰弱(ICU-acquired weakness，ICU-AW)是危重症患者常见的获得性神经肌肉功能障碍，中后期患者的病死率及致残率居高不下[1-2]。但目前尚无有效的干预措施能持续地预防危重症患者的肌肉损失，主要原因在于其发病机制不完全清楚。既往研究表明，E3泛素连接酶的肌环指蛋白1(muscle ring finger protein l，MuRF1)及肌萎缩盒F蛋白(atrogun 1/muscle atrophy F-box，Atrogin1/MAFbx)与肌肉蛋白质的降解密切相关，在ICU-AW发病过程中发挥重要作用[3]。另有研究表明，叉头框蛋白O(forkhead box O，FoxO)能够通过磷酸化与非磷酸化的转化调控MuRF1及Atrogin1的表达[4-6]。在FoxO蛋白家族成员中，FoxO3a缺失较少受到其他因素的补偿，表明FoxO3a是萎缩程序的关键因素。而蛋白激酶B(protein kinase B，Akt/PKB)对FoxO3a的表达及磷酸化/非磷酸化转化过程具有调控作用[7]，当FoxO被Akt磷酸化后，会向细胞质中转位，从而失去对肌萎缩基因的调控作用；非磷酸化的FoxO位于细胞核中，可通过促进肌萎缩基因MuRF1及Atrogin1等的表达，加剧肌萎缩[8]。上述研究提示，Akt-FoxO3a-MuRF1/Atrogin1信号通路在骨骼肌蛋白降解途径中发挥着重要作用，但其在ICU-AW中的作用机制尚不完全清楚。β-羟基-β-甲基丁酸(β-hydroxy-β-methylbutyrate，HMB)是一种安全有效的营养补充剂，也是必需支链氨基酸亮氨酸的代谢物[9]。有文献报道，HMB可用于增强骨骼肌的质量及强度，在老年人及癌症相关的恶病质患者中，补充HMB可以减少骨骼肌萎缩[10-11]，但其具体的作用机制以及是否通过Akt-FoxO3a-MuRF1/Atrogin1这一经典信号通路发挥作用尚不清楚。因此，深入研究HMB改善骨骼肌萎缩的机制对ICU-AW的防治具有重要意义。本研究观察了HMB对急性呼吸窘迫综合征(acute respiratory distress syndrome，ARDS)相关的ICU-AW小鼠骨骼肌形态学及功能的影响，并探讨了其作用机制，以期为ICU-AW的防治提供新思路。
1 材料与方法
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1.1 实验动物
8~10周龄SPF级雄性C57BL/6小鼠60只，体重(27.2±1.3) g，购自成都达硕实验动物有限公司[动物许可证号：SCXK(川)2020-030]。动物SPF级常规饲养，室温维持在20~25 ℃，12 h光照与黑暗交替，给予常规饲料自由饮食，正式实验开始前适应性饲养2周。本研究获得西部战区总医院实验动物伦理委员会批准(批准号：2020ky025)，实验过程符合国家及单位有关实验动物的管理及使用规定。
1.2 主要试剂
HMB购于上海麦克林生物科技股份有限公司，大肠埃希菌(O55：B5L2880)脂多糖(LPS)购于美国Sigma公司，全蛋白提取试剂盒、BCA蛋白浓度测定试剂盒均购于北京索莱宝科技有限公司，抗体MuRF1、Atrogin1及山羊抗兔二抗均购于英国Abcam公司，抗体β-tubulin、Akt、p-Akt、FoxO3a、p-FoxO3a均购于美国Cell Signaling公司，qRT-PCR引物购于四川生工科技有限公司。
1.3 研究方法
1.3.1 动物分组及模型建立
选取40只小鼠，采用随机数字表法分为对照组、假手术组、模型组及HMB组，每组10只。按照Files等[12]的方法于小鼠气管内滴注LPS，建立ARDS相关ICU-AW模型，动物术前称重、编号，禁食12 h，自由饮水。于小鼠腹腔注射1%戊巴比妥钠(50 mg/kg)，待麻醉生效后将动物仰卧固定于操作台上，颈部正中切开5~8 mm，钝性分离皮下组织，暴露气管。用微型注射器由气管向肺分向注射，模型组及HMB组小鼠气管内注入3 μg/g LPS，1 min内注射完毕；假手术组给予等体积生理盐水，注射后立即将动物直立并旋转，使药物均匀分布于两肺。缝合皮肤，待小鼠苏醒后放回饲养笼。自模型建立第2天开始，HMB组以340 mg/(kg·d) HMB灌胃[13]，其余3组给予等体积生理盐水，连续给药2周。另取与HMB组相同处理的小鼠20只，随机分为ARQ-092组与Akt抑制剂对照组，每组10只。在0.01 mol/L磷酸载体(pH值7.25)中配制ARQ-092，从造模后第2天开始，ARQ-092组在HMB灌胃10 h后口服100 mg/kg ARQ-092[14-15]，1次/d，持续12 d，Akt抑制剂对照组给予等体积磷酸载体。
1.3.2 肌肉力量评估
造模开始至第16天，每天用无创爪抓力测试仪测量小鼠前肢肌肉抓力[16-17]。将小鼠的前肢放在爪抓力测试仪金属板上，逐渐向后拉，当小鼠爪子松开时会收缩肢体，此时，金属板连接着的力传感器可测量当前产生卸力的量程，此数据为小鼠当次的抓力值，连续测量5次，结果取平均值[18]。
1.3.3 肌肉减少指数(sarcopenia index，SI)检测
造模第16天后处死小鼠，称量各组小鼠体重并记录。采用戊巴比妥钠麻醉小鼠，分离腓肠肌并剔除肌腱等结缔组织，取出腓肠肌后浸入生理盐水，洗去附着的血液，称量前用滤纸吸除多余的生理盐水及组织液，称量骨骼肌质量，计算小鼠腓肠肌质量(mg)与体重(g)的比值，即SI。
1.3.4 肺组织及肌肉组织病理学检查
取造模48 h小鼠的肺组织及干预完成后小鼠的腓肠肌，迅速放入4%多聚甲醛溶液中固定48 h，脱水，常规石蜡包埋，4 μm厚度切片，按照HE染色试剂盒操作说明书步骤进行HE染色，并在光学显微镜下观察、拍照。
1.3.5 qRT-PCR检测相关基因mRNA的表达
采用qRT-PCR检测腓肠肌中Akt、FoxO3a、MuRF1及Atrogin1 mRNA的表达水平，引物序列见表1。采用Trizol法提取腓肠肌组织标本中的总RNA，离心、洗涤、再溶解，测定总RNA纯度及浓度。一步法qRT-PCR反应条件：反转录反应42 ℃ 5 min，95 ℃10 s；PCR反应95 ℃ 15 s，63 ℃ 1 min，共40个循环。每孔为总体积25 μl含RNA的反应液，每组2~3个复孔。以GAPDH作为内参照，采用2–ΔΔCt法计算各组目的基因的相对表达量。
1.3.6 Western blotting检测腓肠肌中Akt、p-Akt、FoxO3a、p-FoxO3a、MuRF1及Atrogin1蛋白相对表达量
裂解腓肠肌组织，提取总蛋白，采用BCA法进行蛋白定量，经SDS-PAGE电泳、转膜、封闭后，加入相应的一抗Akt(1:1000)、p-Akt(1:1000)、FoxO3a(1:1000)、p-FoxO3a(1:1000)、Atrogin1(1:1000)、MuRF1(1:1000)、α-Tubulin (1:2000)，4 ℃孵育过夜，TBST漂洗3次后加入相应的辣根过氧化物酶标记二抗(1:2000)孵育1 h，TBST漂洗3次，每次10 min。洗膜后DAB显色，采用凝胶图像分析系统拍照，以α-tubulin为内参照，对目的基因条带灰度值进行统计分析。
1.4 统计学处理
使用GraphPad Prism V5及SPSS 20.0软件进行制图及数据分析。计量资料以$\bar{x}±s$表示，符合正态分布且方差齐时，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LSD-t检验；两组间比较采用t检验；方差不齐时采用秩和检验。P<0.05为差异有统计学意义。
2 结果
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2.1 各组小鼠肺组织及腓肠肌组织形态比较
利用气管内滴注LPS建立ARDS相关ICU-AW小鼠模型，造模48 h的肺组织HE染色结果显示，对照组及假手术组小鼠肺泡结构完整，无损伤表现；模型组及HMB组出现肺间质水肿，中性粒细胞浸润，肺泡间隔增宽、结构紊乱，表明气管内滴注LPS的小鼠有明显的ARDS病理表现(图1A)。HMB干预2周后腓肠肌HE染色结果显示，对照组及假手术组小鼠肌束结构完整，肌纤维排列紧密，大小形态正常，未见细胞碎裂、溶解，两组间无明显差异；与对照组及假手术组比较，模型组出现肌肉萎缩及不同程度的肌束结构破坏，可见细胞数量减少，肌纤维排列更为疏松，横截面积减少；与模型组比较，HMB组小鼠腓肠肌损伤程度减轻(图1B)。
2.2 HMB对ARDS相关ICU-AW小鼠骨骼肌力量及SI的影响
各组小鼠造模前抓力值比较差异无统计学意义(P>0.05)；第2、3、4天，与对照组比较，假手术组小鼠抓力值降低(P<0.05)；第1~16天，与对照组及假手术组比较，模型组小鼠抓力值均降低(P<0.05)；第3~16天，与模型组比较，HMB组小鼠抓力值均升高(P<0.05，图2A)。与对照组比较，假手术组小鼠SI无明显变化(P>0.05)，模型组小鼠SI则明显降低(P<0.05)；与模型组比较，HMB组小鼠SI明显升高(P<0.05)，但模型组与对照组及假手术组比较，差异均无统计学意义(P>0.05，图2B)。
2.3 HMB对ARDS相关ICU-AW小鼠Akt-FoxO3a-MuRF1/Atrogin1信号通路的影响
qRT-PCR检测结果显示，对照组及假手术组小鼠腓肠肌组织中Akt、FoxO3a、MuRF1及Atrogin1的mRNA表达水平比较差异均无统计学意义(P>0.05)；与假手术组比较，模型组小鼠腓肠肌组织中Akt和FoxO3a的mRNA表达水平明显降低(0.35±0.09 vs.1.10±0.12；0.32±0.08 vs. 1.04±0.12，P<0.05)，Atrogin1的mRNA表达水平明显升高(1.55±0.23 vs.0.99±0.24，P<0.05)，MuRF1的升高趋势更明显(2.79±0.27 vs. 1.12±0.14，P<0.05，图3A)；而HMB干预则逆转了这一趋势。Western blotting结果与qRT-PCR结果趋势一致(图3B、C)。
2.4 Akt抑制剂ARQ-092对HMB保护作用的影响
造模第5~16天，ARQ-092组抓力值及SI均低于Akt抑制剂对照组(P<0.05，图4A、B)。腓肠肌组织HE染色结果显示，ARQ-092组较Akt抑制剂对照组的细胞数量减少，肌纤维横截面积缩小，排列疏松(图4C)。qRT-PCR结果显示，与Akt抑制剂对照组比较，ARQ-092组Akt及FoxO3a的mRNA表达水平均明显降低(0.35±0.07 vs. 0.97±0.18；0.50±0.10 vs. 1.08±0.15，P<0.05)；Atrogin1及MuRF1的mRNA表达水平均明显升高(1.49±0.18 vs. 1.00±0.08；2.81±0.26 vs. 1.39±0.27，P<0.05，图4D)。Western blotting结果与qRT-PCR结果趋势一致(图4E、F)。
3 讨论
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大量研究表明，脓毒症是ICU-AW发生发展的主要危险因素，肺部感染相关ICU-AW是导致患者病死率及长期罹病率较高的重要因素[19]。ICU-AW的病死率居高不下，严重威胁患者健康，并给家庭及社会造成沉重的经济负担，关于ICU-AW的研究已成为近年来研究的热点。为深入探讨ICU-AW的发病机制，本研究采用Files等[12]的方法建立ARDS相关ICU-AW小鼠模型，该模型成功复制人类ICU-AW相关肌肉萎缩的一些关键特征，包括严重的骨骼肌萎缩、与ARDS相关的无力、与肌肉功能下降相关的肌肉收缩蛋白的优先丧失、ARDS消退后的肌肉无力持续存在等，提示该ARDS相关ICU-AW小鼠模型可作为本研究的理想动物模型，为下一步研究ICU-AW的发病机制及治疗措施创造了有利条件。
HMB是必需氨基酸亮氨酸的一种内源性代谢物，目前已在人类及动物模型中对HMB开展了深入研究。在动物模型中，HMB可有效减轻脓毒症引起的膈肌无力及地塞米松诱导的肌肉萎缩[20-21]；在临床人群中，HMB已被证实可减轻癌症恶病质、慢性阻塞性肺疾病(chronic obstructive pulmonary disease，COPD)、获得性免疫缺陷综合征、肝硬化及肌肉减少症患者或虚弱老年人的肌肉萎缩[22-24]。本研究结果显示，经HMB治疗后，ARDS相关ICU-AW小鼠的骨骼肌抓力值明显升高，表明HMB具有保护骨骼肌功能的作用。另外，本研究还发现，HMB能明显增加ICU-AW小鼠的腓肠肌质量并升高SI。小鼠腓肠肌组织病理切片显示，与模型组比较，HMB组肌束中由肌膜围绕的肌纤维排列更加规则有序，肌纤维及肌束的横截面积增加，炎性细胞浸润少，损伤程度更轻，证实HMB治疗能减轻ICU-AW小鼠的骨骼肌萎缩，并提高骨骼肌的力量，保护ICU-AW小鼠的骨骼肌，这与上述研究结果一致。
既往研究表明，蛋白质降解与合成失衡是ICU-AW骨骼肌萎缩的主要机制之一[25]。当蛋白质降解率超过合成时会导致肌肉萎缩，其中蛋白质降解主要与泛素-蛋白酶体途径的激活有关[8]。泛素-蛋白酶体系统中的两种主要标志物Atrogin1及MuRF1的过表达可以促进肌肉蛋白质分解及肌肉萎缩，进而参与ICU-AW的发生发展。因此，深入研究Atrogin1及MuRF1的调控机制，对骨骼肌蛋白降解及ICU-AW的防治具有重要意义。FoxO3a是骨骼肌蛋白水解途径中的重要分子，且能够通过诱导自噬相关基因表达参与骨骼肌功能的调控[26]，因而受到研究者关注。FoxO3a具有磷酸化及非磷酸化两种状态，非磷酸化的FoxO3a能够上调骨骼肌中的Atrogin1及MuRF1表达，从而加速蛋白降解，引起骨骼肌萎缩，而FoxO3a磷酸化与非磷酸化状态的转化受Akt调控，活化的Akt能够促进FoxO3a由非磷酸化转为磷酸化状态，从而通过阻止Atrogin1及MuRF1表达来减轻骨骼肌萎缩[6, 27-28]。由此可见，Akt-FoxO3a-MuRF1/Atrogin1信号通路在骨骼肌蛋白降解过程中具有重要作用。本研究采用qRT-PCR及Western blotting评估mRNA及蛋白表达，结果显示模型组小鼠腓肠肌组织中Akt及FoxO3a的mRNA表达水平明显下降，磷酸化水平明显降低，MuRF1及Atrogin1的表达明显增加，提示ICU-AW小鼠骨骼肌分解代谢水平升高。HMB干预使Akt及FoxO3a的mRNA表达水平及磷酸化水平均有提高，明显降低MuRF1及Atrogin1的表达，表明HMB可能通过激活Akt/FoxO3a信号通路，促进Akt及FoxO3a的磷酸化，进而抑制MuRF1/Atrogin1介导的骨骼肌分解代谢途径发挥保护作用。本研究为进一步验证这一猜想，采用Akt抑制剂ARQ-092进行干预，结果表明ARQ-092能够逆转HMB对ICU-AW小鼠的保护作用。
综上所述，本研究提示HMB可能通过调控Akt-FoxO3a-MuRF1/Atrogin1信号通路在ICU-AW中发挥保护作用，对ICU-AW的防治具有重要价值。本研究的不足之处在于仅在ARDS相关ICU-AW的蛋白质降解方面进行了观察验证，初步探索了HMB治疗ARDS相关ICU-AW的机制，但缺乏对蛋白质合成、自噬以及细胞凋亡三者之间信号通路的探究，需要后续深入研究予以验证。
基金
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  • 四川省干部保健科研课题(川干研2022-1303)
  • 西部战区总医院军事医学科研项目(2019LH05)
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2022年第47卷第9期
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doi: 10.11855/j.issn.0577-7402.2022.09.0886
  • 接收时间：2021-12-09
  • 首发时间：2025-12-15
  • 出版时间：2022-09-28
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  • 收稿日期：2021-12-09
  • 录用日期：2022-03-15
基金
Sichuan Province Cadre Health Research Project(川干研2022-1303)
四川省干部保健科研课题(川干研2022-1303)
General Hospital of Western Theater Command Military Medical Research Project of China(2019LH05)
西部战区总医院军事医学科研项目(2019LH05)
作者信息
    1西南交通大学医学院，四川成都 610031
    2西部战区总医院重症医学科，四川成都 610083
    3西部战区总医院营养科，四川成都 610083

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species		 占总种数比例
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鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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