Journal of Traditional Chinese Medicine ›› 2024, Vol. 44 ›› Issue (4): 734-744.DOI: 10.19852/j.cnki.jtcm.20240610.004
• Original articles • Previous Articles Next Articles
Electroacupuncture ameliorates blood-brain barrier disruption after ischemic stroke through histone acetylation regulation at the matrix metalloproteinase 9 and tissue inhibitor of metalloproteinase 2 genes
CHEN Yonglin, OUYANG Ling, MENG Lingling, WU Bufan, PENG Rou, LIU Sitong, HOU Dan, WANG Yaling, JING Xinyue, LU Shengfeng(
), FU Shuping()
- Key Laboratory of Acupuncture and Medicine Research of Ministry of Education, Nanjing University of Chinese Medicine, Nanjing 210023, China
-
Received:2023-02-22Accepted:2023-07-20Online:2024-08-15Published:2024-06-10 -
Contact:Prof. FU Shuping, Key Laboratory of Acupuncture and Medicine Research of Ministry of Education, Nanjing University of Chinese Medicine, Nanjing, 210023, China.shupingfu@njucm.edu.cn ; Prof. LU Shengfeng, Key Laboratory of Acupuncture and Medicine Research of Ministry of Education, Nanjing University of Chinese Medicine, Nanjing, 210023, China.lushengfeng@njucm.edu.cn Telephone: +86-18761894980 -
Supported by:National Natural Science Foundation of China: the Role of Intestinal Flora-Treg/γδT Cell-IL-17 Signaling in the Neuroprotective Effect of Electroacupuncture on Ischemic Brain Injury(81774403);Natural Science Foundation of the Jiangsu Province of China: Study on the Mechanism of Acupuncture Anti-stroke Immune Inflammatory Response Based on Intestinal Treg/γδT Cell-IL-17 Signaling Pathway(BK20171492);Postgraduate Scientific Research Innovation Practice Project of the Jiangsu Province of China: a Study based on the Butyric Acid-HDAC-Foxp3 Pathway to Explore the Regulatory Effect of Acupuncture on Intestinal Treg in Rats with Stroke(KYCX21_1715);a Study on the Anti-brain Injury of Electroacupuncture Based on Intestinal Microbiota-Treg/γδT Cell-IL-17 Pathway(KYCX21_1716);Key University Science Research Project of Jiangsu Province: the Role of Preactivation of the Treg Immune Response in the Mechanism of Anti-stroke Neuroinflammatory Response in Acupuncture Pretreatment(22KJA360003)
Cite this article
CHEN Yonglin, OUYANG Ling, MENG Lingling, WU Bufan, PENG Rou, LIU Sitong, HOU Dan, WANG Yaling, JING Xinyue, LU Shengfeng, FU Shuping. Electroacupuncture ameliorates blood-brain barrier disruption after ischemic stroke through histone acetylation regulation at the matrix metalloproteinase 9 and tissue inhibitor of metalloproteinase 2 genes[J]. Journal of Traditional Chinese Medicine, 2024, 44(4): 734-744.
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Figure 1 EA treatment reduced cerebral damage after I/R injury in rats A: the experimental timeline; B: Longa neurologic score 1 d after ischemia, n = 11; C: Longa neurologic score 3 d after ischemia, n = 7; D: representative photograph of Evans blue extravasation in the brains of rats 24 h after I/R injury. The blue area shows penetrating Evans blue, signifying BBB destruction; E: quantitative analysis of Evans blue penetration in each group 1 d after ischemic stroke, n = 7; F: Evans blue exudation 3 d after ischemia, n = 4. Sham group: sham operated; MCAO group: MCAO operated; MEA group: MCAO rats received 3 d of EA treatment; HATi group: MCAO rats received 3 d of EA treatment and a single 4 mg/kg intraperitoneal injection of HATi. I/R: ischemia/reperfusion; MCAO: middle cerebral artery occlusion; EA: electroacupuncture; HATi: histone acetyltransferase inhibitor; EB: Evans blue; RT-qPCR: real-time quantitative polymerase chain reaction; ChIP: chromatin immunoprecipitation; BBB: blood-brain barrier. Data were analyzed by one-way analysis of variance and are represented as the mean ± standard deviation. aP < 0.05 vs the sham group, bP < 0.05 the MCAO group vs the MEA group, cP < 0.05 the MEA group vs the HATi group.
Figure 1 EA treatment reduced cerebral damage after I/R injury in rats A: the experimental timeline; B: Longa neurologic score 1 d after ischemia, n = 11; C: Longa neurologic score 3 d after ischemia, n = 7; D: representative photograph of Evans blue extravasation in the brains of rats 24 h after I/R injury. The blue area shows penetrating Evans blue, signifying BBB destruction; E: quantitative analysis of Evans blue penetration in each group 1 d after ischemic stroke, n = 7; F: Evans blue exudation 3 d after ischemia, n = 4. Sham group: sham operated; MCAO group: MCAO operated; MEA group: MCAO rats received 3 d of EA treatment; HATi group: MCAO rats received 3 d of EA treatment and a single 4 mg/kg intraperitoneal injection of HATi. I/R: ischemia/reperfusion; MCAO: middle cerebral artery occlusion; EA: electroacupuncture; HATi: histone acetyltransferase inhibitor; EB: Evans blue; RT-qPCR: real-time quantitative polymerase chain reaction; ChIP: chromatin immunoprecipitation; BBB: blood-brain barrier. Data were analyzed by one-way analysis of variance and are represented as the mean ± standard deviation. aP < 0.05 vs the sham group, bP < 0.05 the MCAO group vs the MEA group, cP < 0.05 the MEA group vs the HATi group.
Figure 2 EA treatment regulated the expression of MMP-9 and TIMP-1/2 after MCAO A: RT-qPCR shows the relative mRNA levels of MMP-9 in ischemic brain tissues 24 h after I/R injury, n = 4; B: RT-qPCR shows the relative mRNA levels of TIMP-1 in ischemic brain tissues 24 h after ischemia/reperfusion injury, n = 4; C: RT-qPCR shows the relative mRNA levels of TIMP-2 in ischemic brain tissues 24 h after I/R injury, n = 4. Sham group: sham operated; MCAO group: MCAO operated; MEA group: MCAO rats received 3 d of EA treatment; HATi group: MCAO rats received 3 d of EA treatment and a single 4 mg/kg intraperitoneal injection of HATi. MMP-9: matrix metalloproteinase 9; TIMP-1/2: tissue inhibitor of metalloproteinase 1/2; MCAO: middle cerebral artery occlusion; EA: electroacupuncture; HATi: histone acetyltransferase inhibitor; RT-qPCR: real-time quantitative polymerase chain reaction. Data were analyzed by one-way analysis of variance and are represented as the mean ± standard deviation. aP < 0.05, vs the sham group; bP < 0.05, the MCAO group vs the MEA group; cP < 0.05, the MEA group vs the HATi group.
Figure 2 EA treatment regulated the expression of MMP-9 and TIMP-1/2 after MCAO A: RT-qPCR shows the relative mRNA levels of MMP-9 in ischemic brain tissues 24 h after I/R injury, n = 4; B: RT-qPCR shows the relative mRNA levels of TIMP-1 in ischemic brain tissues 24 h after ischemia/reperfusion injury, n = 4; C: RT-qPCR shows the relative mRNA levels of TIMP-2 in ischemic brain tissues 24 h after I/R injury, n = 4. Sham group: sham operated; MCAO group: MCAO operated; MEA group: MCAO rats received 3 d of EA treatment; HATi group: MCAO rats received 3 d of EA treatment and a single 4 mg/kg intraperitoneal injection of HATi. MMP-9: matrix metalloproteinase 9; TIMP-1/2: tissue inhibitor of metalloproteinase 1/2; MCAO: middle cerebral artery occlusion; EA: electroacupuncture; HATi: histone acetyltransferase inhibitor; RT-qPCR: real-time quantitative polymerase chain reaction. Data were analyzed by one-way analysis of variance and are represented as the mean ± standard deviation. aP < 0.05, vs the sham group; bP < 0.05, the MCAO group vs the MEA group; cP < 0.05, the MEA group vs the HATi group.
Figure 3 EA treatment regulated H3K9ace occupancy at target gene promoters A: ChIP analysis of the enrichment of acetylated H3K9 on promoters of MMP-9 －21 bp - －177 bp region, n = 3 or 4; B: ChIP analysis of the enrichment of acetylated H3K9 on promoters of MMP-9 －678 bp - －886 bp region, n = 3 or 4; C: ChIP analysis of the enrichment of acetylated H3K9 on promoters of TIMP-1 －271 bp - －549 bp region, n = 3 or 4; D: ChIP analysis of the enrichment of acetylated H3K9 on promoters of TIMP-1 －580 bp - －822 bp region, n = 3 or 4. E: ChIP analysis of the enrichment of acetylated H3K9 on promoters of TIMP-2 －248 bp - －425 bp region, n = 3 or 4. F: ChIP analysis of the enrichment of acetylated H3K9 on promoters of TIMP-2 －34 bp - －150 bp region, n = 3 or 4. Sham group: sham operated; MCAO group: MCAO operated; MEA group: MCAO rats received 3 d of EA treatment; HATi group: MCAO rats received 3 d of EA treatment and a single 4 mg/kg intraperitoneal injection of HATi. MCAO: middle cerebral artery occlusion; EA: electroacupuncture; HATi: histone acetyltransferase inhibitor; H3K9ace: histone H3 lysine 9 acetylation; MMP-9: matrix metalloproteinase 9; TIMP-1: tissue inhibitor of metalloproteinase 1; TIMP-2: tissue inhibitor of metalloproteinase 2; ChIP: chromatin immunoprecipitation. Data were analyzed by one-way analysis of variance and are represented as the mean ± standard deviation. aP < 0.05 vs the sham group, bP < 0.05 the MCAO group vs the MEA group, cP < 0.05 the MEA group vs the HATi group.
Figure 3 EA treatment regulated H3K9ace occupancy at target gene promoters A: ChIP analysis of the enrichment of acetylated H3K9 on promoters of MMP-9 －21 bp - －177 bp region, n = 3 or 4; B: ChIP analysis of the enrichment of acetylated H3K9 on promoters of MMP-9 －678 bp - －886 bp region, n = 3 or 4; C: ChIP analysis of the enrichment of acetylated H3K9 on promoters of TIMP-1 －271 bp - －549 bp region, n = 3 or 4; D: ChIP analysis of the enrichment of acetylated H3K9 on promoters of TIMP-1 －580 bp - －822 bp region, n = 3 or 4. E: ChIP analysis of the enrichment of acetylated H3K9 on promoters of TIMP-2 －248 bp - －425 bp region, n = 3 or 4. F: ChIP analysis of the enrichment of acetylated H3K9 on promoters of TIMP-2 －34 bp - －150 bp region, n = 3 or 4. Sham group: sham operated; MCAO group: MCAO operated; MEA group: MCAO rats received 3 d of EA treatment; HATi group: MCAO rats received 3 d of EA treatment and a single 4 mg/kg intraperitoneal injection of HATi. MCAO: middle cerebral artery occlusion; EA: electroacupuncture; HATi: histone acetyltransferase inhibitor; H3K9ace: histone H3 lysine 9 acetylation; MMP-9: matrix metalloproteinase 9; TIMP-1: tissue inhibitor of metalloproteinase 1; TIMP-2: tissue inhibitor of metalloproteinase 2; ChIP: chromatin immunoprecipitation. Data were analyzed by one-way analysis of variance and are represented as the mean ± standard deviation. aP < 0.05 vs the sham group, bP < 0.05 the MCAO group vs the MEA group, cP < 0.05 the MEA group vs the HATi group.
Figure 4 EA treatment regulated H3K27ace occupancy at target gene promoters A: ChIP analysis of the enrichment of acetylated H3K27 on promoters of MMP-9 －21 bp - －177 bp region, n = 3 or 4; B: ChIP analysis of the enrichment of acetylated H3K27 on promoters of MMP-9 －678 bp - －886 bp region, n = 3 or 4; C: ChIP analysis of the enrichment of acetylated H3K27 on promoters of TIMP-1 －271 bp - －549 bp region, n = 3 or 4; D: ChIP analysis of the enrichment of acetylated H3K27 on promoters of TIMP-1 －580 bp - －822 bp region, n = 3 or 4; E: ChIP analysis of the enrichment of acetylated H3K27 on promoters of TIMP-2 －248 bp - －425 bp region, n = 3 or 4. F: ChIP analysis of the enrichment of acetylated H3K27 on promoters of TIMP-2 －34 bp - －150 bp region, n = 3 or 4. Sham group: sham operated; MCAO group: MCAO operated; MEA group: MCAO rats received 3 d of EA treatment; HATi group: MCAO rats received 3 d of EA treatment and a single 4 mg/kg intraperitoneal injection of HATi. MCAO: middle cerebral artery occlusion; EA: electroacupuncture; HATi: histone acetyltransferase inhibitor; H3K27ace: histone H3 lysine 27 acetylation; MMP-9: matrix metalloproteinase 9; TIMP-1: tissue inhibitor of metalloproteinase 1; TIMP-2: tissue inhibitor of metalloproteinase 2; ChIP: chromatin immunoprecipitation. Data were analyzed by one-way analysis of variance and are represented as the mean ± standard deviation. aP < 0.05 vs the sham group, bP < 0.05 the MCAO group vs the MEA group, cP < 0.05 the MEA group vs the HATi group.
Figure 4 EA treatment regulated H3K27ace occupancy at target gene promoters A: ChIP analysis of the enrichment of acetylated H3K27 on promoters of MMP-9 －21 bp - －177 bp region, n = 3 or 4; B: ChIP analysis of the enrichment of acetylated H3K27 on promoters of MMP-9 －678 bp - －886 bp region, n = 3 or 4; C: ChIP analysis of the enrichment of acetylated H3K27 on promoters of TIMP-1 －271 bp - －549 bp region, n = 3 or 4; D: ChIP analysis of the enrichment of acetylated H3K27 on promoters of TIMP-1 －580 bp - －822 bp region, n = 3 or 4; E: ChIP analysis of the enrichment of acetylated H3K27 on promoters of TIMP-2 －248 bp - －425 bp region, n = 3 or 4. F: ChIP analysis of the enrichment of acetylated H3K27 on promoters of TIMP-2 －34 bp - －150 bp region, n = 3 or 4. Sham group: sham operated; MCAO group: MCAO operated; MEA group: MCAO rats received 3 d of EA treatment; HATi group: MCAO rats received 3 d of EA treatment and a single 4 mg/kg intraperitoneal injection of HATi. MCAO: middle cerebral artery occlusion; EA: electroacupuncture; HATi: histone acetyltransferase inhibitor; H3K27ace: histone H3 lysine 27 acetylation; MMP-9: matrix metalloproteinase 9; TIMP-1: tissue inhibitor of metalloproteinase 1; TIMP-2: tissue inhibitor of metalloproteinase 2; ChIP: chromatin immunoprecipitation. Data were analyzed by one-way analysis of variance and are represented as the mean ± standard deviation. aP < 0.05 vs the sham group, bP < 0.05 the MCAO group vs the MEA group, cP < 0.05 the MEA group vs the HATi group.
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