Electroacupuncture alleviates type 2 diabetes mellitus by promoting plasma-derived exosomal circular RNA of enhancer of zeste homolog 1 expression

doi:10.19852/j.cnki.jtcm.2025.06.005

Journal of Traditional Chinese Medicine ›› 2025, Vol. 45 ›› Issue (6): 1228-1237.DOI: 10.19852/j.cnki.jtcm.2025.06.005

• Original Articles • Previous Articles Next Articles

Electroacupuncture alleviates type 2 diabetes mellitus by promoting plasma-derived exosomal circular RNA of enhancer of zeste homolog 1 expression

SHOU Yin¹, JIANG Juntao², HU Jianlin³, JI Wei⁴, CHEN Chunyan⁵, HU Li⁶(), MA Yuhang⁷, ZHANG Bimeng¹()

1 Department of Acupuncture-Moxibustion, Shanghai General Hospital, Shanghai Jiaotong University School of Medicine, Shanghai 200000, China
2 Department of Urology, Shanghai General Hospital, Shanghai Jiaotong University School of Medicine, Shanghai 200000, China
3 Department of Reproduction, Shanghai General Hospital, Shanghai Jiaotong University School of Medicine, Shanghai 200000, China
4 Department of Traditional Chinese Orthopedics, Xiangshan TCM Hospital, Shanghai, China
5 Shanghai Research Institute of Qigong, Taiji Health Center, Shanghai University of Traditional Chinese Medicine, Shanghai 200000, China
6 Acumox and Tuina Research Section, College of Acumox and Tuina, Shanghai University of Traditional Chinese Medicine, Shanghai 200000, China
7 Department of Endorcinolgy and Metabolism, Shanghai General Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200000, China

Received:2024-11-12 Accepted:2025-05-07 Online:2025-12-15 Published:2025-11-24
Contact: HU Li, Acumox and Tuina Research Section, College of Acumox and Tuina, Shanghai University of Traditional Chinese Medicine, Shanghai 200000, China. huli6862292006@163.com, Telephone: +86-21-37798133
Prof. ZHANG Bimeng, Department of Acupuncture-Moxibustion, Shanghai General Hospital, Shanghai Jiaotong University School of Medicine, Shanghai 200000, China. acusci2007@126.com
About author:SHOU Yin and HU Jianlin are co-first authors and contributed equally to this work
Supported by:
Science and Technology Committee of Songjiang District, Shanghai(2024SJKJGG001);project: Mechanistic Study on the Therapeutic Effect of Electroacupuncture in Diabetic Osteoporosis via Exosomal circular RNA of Enhancer of Zeste Homolog 1-Regulated miR-128/ Transient Receptor Potential Vanilloid 1 Axis-Mediated Ferroptosis in Osteoclasts; the Shanghai Municipal Health Bureau [grant number: 2020LP010];Project: a Randomized Controlled Study of Traditional Chinese Acupuncture Combined with Rehabilitation Training for the Treatment of Intensive Care Unit-Acquired Weakness; the Science and Technology Commission of Shanghai Municipality (grant number: 20511101204);Project: Traditional Chinese Medicine Data Collection and Governance for Early Screening and Stratified Diagnosis and Treatment of Pancreatic Cancer; the Shanghai University of Traditional Chinese Medicine (grant number: 2021LK100);Project: the Role of Sestrin 2/mechanistic Target of Rapamycin-Mediated Autophagy in Age-Related Skeletal Muscle Atrophy and the Effects of Acupuncture;Shanghai General Hospital(grant number: 202220);Project: Research on the Construction of Talent Evaluation System by the Southern Outpatient Party Branch; and Shanghai Municipal Commission of Health and Family Planning [grant number: ZY(2021-2023)-0208];Project: Special Program of the Integrated Chinese and Western Medicine Innovation Research Institute

Abstract

Abstract:

OBJECTIVE: To investigate the effect of electroacupuncture (EA) on regulatory functions of one specific exosomal circRNA of Enhancer of Zeste Homolog (CircEZH) and its potential mechanisms of action in type 2 diabetes (T2DM).

METHODS: Mice were fed a high-fat diet (HFD) and intraperitoneally injected with streptozotocin to create the T2DM model and then were used for two experiments involving the following groups: experiment 1 (control group, T2DM group, T2DM+EA group, 10 mice per group) and experiment 2 [control group, T2DM group, T2DM+ CircEZH1-siRNA (20 nmol/20 g) group, 10 mice per group]. Exosomal size, distribution, and morphology were evaluated via transmission electron microscopy and nanoparticle tracking analysis. The expression of CircEZH1 and CircEZH2 in exosomes was assessed by quantitative real-time polymerase chain reaction. Insulin expression was assessed by enzyme-linked immunosorbent assay, immunofluorescence, and western blotting. The effects of exosomal CircEZH1 knockout and overexpression in Min6 cells were assessed by cell counting kit-8 and flow cytometry. Meanwhile, the effect of CircEZH1 knockout on insulin sensitivity was assessed by glucose tolerance test (GTT) and insulin tolerance test (ITT) in vivo.

RESULTS: EA treatment significantly reduced the serum insulin level and cell apoptosis in pancreatic tissue in a T2DM model. EA treatment markedly upregulated CircEZH1 expression in the exosomes of T2DM mice. Further study showed that CircEZH1 overexpression resulted in increased Min6 cell viability and decreased Min6 cell apoptosis when compared with the levels in an overexpression control group. In Min6 cells with CircEZH1 knockout, the opposite trends were identified. CircEZH1-knockout Min6 cells also showed reduced insulin expression. In vivo, CircEZH1-knockout T2DM mice displayed damaged insulin sensitivity, which was demonstrated by elevated levels of fasting blood glucose and decreased glucose tolerance in the GTT and insulin sensitivity in the ITT.

CONCLUSIONS: EA can affect CircEZH1 expression specifically in the exosomes in β cells in the pancreatic islets to improve T2DM. Exosomal CircEZH1 is a potential therapeutic candidate to treat T2DM.

Key words: diabetes mellitus, type 2, electroacupuncture, diet, high-fat, exosomal CircEZH1

SHOU Yin, JIANG Juntao, HU Jianlin, JI Wei, CHEN Chunyan, HU Li, MA Yuhang, ZHANG Bimeng. Electroacupuncture alleviates type 2 diabetes mellitus by promoting plasma-derived exosomal circular RNA of enhancer of zeste homolog 1 expression[J]. Journal of Traditional Chinese Medicine, 2025, 45(6): 1228-1237.

Figures/Tables 7

Figure 1 Evaluation of the quality of exosomes A: size distribution of plasma exosomes assessed using NTA; A1: Control; A2: T2DM; A3: T2DM + EA; B: morphological appearance of plasma exosomes under a transmission electron microscope (Control); B1: Control-1; B2: Control-2; B3: Control-3; C: morphological appearance of plasma exosomes under a transmission electron microscope (T2DM); C1:T2DM-1; C2:T2DM-2; C3:T2DM-3; D: morphological appearance of plasma exosomes under a transmission electron microscope (T2DM + EA); D1: T2DM + EA-1; D1: T2DM + EA-1; D1: T2DM + EA-1. NTA: nanoparticle tracking analysis; T2DM: type 2 diabetes; EA: electroacupuncture. Control (low-fat diet), T2DM (HFD + STZ 50 mg/kg), and T2DM + EA (T2DM mice treated with electroacupuncture at ST36 and BL20 for 4 weeks). Briefly, for the mice in the T2DM model + EA group, the acupuncture Zusanli (ST36) and Pishu (BL20) points (frequency 2 Hz, intensity 1-3 mA, intermittent waveform, serial length 30 s, increasing once every 5 min, lasting for 15 min) were stimulated once every 2 d, 3 times a week, for 4 weeks (12 times in total). Before EA treatment, T2DM mice were under 2% isoflurane anesthesia.

Figure 2 EA treatment reduced the insulin level and cell apoptosis in pancreatic tissue of T2DM A: serum insulin level detected using ELISA; B: immunofluorescence analysis of insulin and c-caspase 3 expression in pancreatic tissue; C: immunofluorescence analysis of insulin and c-caspase 3 expression in pancreatic tissue; D: immunofluorescence analysis of insulin and c-caspase 3 expression in pancreatic tissue; B1, C1, D1: merge-1; B2, C2, D2: merge-2; B3, C3, D3: merge-3; B4, C4, D4: insulin-1; B5, C5, D5: insulin-2; B6, C6, D6: insulin-3; B7, C7, D7: c-caspase3-1; B8, C8, D8: c-caspase3-2; B9, C9, D9: c-caspase3-3; B10, C10, D10: DAPI-1; B11, C11, D11: DAPI-2; B12, C12, D12: DAPI-3; D1: merge-1; D2: merge-2; D3: merge-3; D4: insulin-1; D5: insulin-2; D6: insulin-3; D7: c-caspase3-1; D8: c-caspase3-2; D9: c-caspase3-3; D10: DAPI-1; D11: DAPI-2; D12: DAPI-3. Control (low-fat diet), T2DM (HFD + STZ), and T2DM + CircEZH1-siRNA (T2DM mice administered CircEZH1-siRNA, 20 nmol/20 g). Briefly, for the mice in the T2DM model + EA group, the acupuncture Zusanli (ST36) and Pishu (BL20) points (frequency 2 Hz, intensity 1-3 mA, intermittent waveform, serial length 30 s, increasing once every 5 min, lasting for 15 min) were stimulated once every 2 d, 3 times a week, for 4 weeks (12 times in total). Before EA treatment, T2DM mice were under 2% isoflurane anesthesia. T2DM: type 2 diabetes, EA: electroacupuncture; ELISA: enzyme-linked immunosorbent assay; DAPI: 4′,6-diamidino-2-phenylindole; ANOVA: analysis of variance. The statistical analyses included one-way ANOVA and t-tests to compare differences among treatment groups. Error bars represent the mean?± standard deviation (n = 3). Compared with the ctrl group, aP < 0.001; compared with T2DM group, bP < 0.05.

Table 1 CircEZH1 and CircEZH2 expression in plasma exosomes detected using qPCR ($\bar{x}$± s)

Group	n	circEZH1/GAPDH relative expression	circEZH2/GAPDH relative expression
Ctrl-exo	3	1.00±0.43	1.00±0.21
T2DM-exo	3	0.06±0.01^a	0.79±0.14
T2DM+EA-exo	3	0.42±0.17^b	1.02±0.15

Table 2 CircEZH1 expression affected Min6 cell viability and apoptosis ($\bar{x}$ ± s)

Group	n	Cell viability of Min6 (%)					Apoptosis (%)
Group	n	0 h	24 h	48 h	72 h	96 h	Apoptosis (%)
OE-NC	5	100.00±3.44	225.81±16.15	410.09±2.04	627.22±25.83	793.71±35.24	6.51±0.36
CircEZH1-OE	5	100.00±1.43	253.32±4.71	523.34±25.23^a	765.49±49.01^c	1012.72±28.5^a	1.73±0.04^a
siRNA-NC	5	100.00±7.33	210.23±9.41	397.33±15.98	613.46±46.85	765.41±53.34	6.57±0.14
CircEZH1-siRNA	5	100.00±6.61	226.26±8.45	267.43±7.94^b	491.17±62.66^d	658.6±55.82^e	9.81±0.28^c

Figure 3 Effect of CircEZH1 expression on the insulin level in Min6 cells A: insulin level in Min6 cell supernatant detected using ELISA. Control (low-fat diet), T2DM (HFD + STZ 50 mg/kg), and T2DM + EA (T2DM mice treated with electroacupuncture at ST36 and BL20 for 4 weeks); B: representative band of insulin protein in in Min6 cells detected using Western blotting; C: relative protein levels of insulin results. Control (scramble siRNA or empty vector), CircEZH1 overexpression, CircEZH1 knockdown (CircEZH1 siRNA) and NC (Min6 cell without CircEZH1overexpression). HFD: high-fat diet; STZ: streptozotocin; T2DM: type 2 diabetes mellitus; EA: electroacupuncture; ST36: Zusanli acupoint; BL20: Pishu acupoint; siRNA: Small interfering RNA; CircEZH1: Circular RNA enhancer of zeste homolog 1. Briefly, for the mice in the T2DM model + EA group, the acupuncture Zusanli (ST36) and Pishu (BL20) points (frequency 2 Hz, intensity 1-3 mA, intermittent waveform, serial length 30 s, increasing once every 5 min, lasting for 15 min) were stimulated once every 2 d, 3 times a week, for 4 weeks (12 times in total). Before EA treatment, T2DM mice were under 2% isoflurane anesthesia. OE-NC: Min6 cell without CircEZH1overexpression; CircEZH1: circular RNA of Enhancer of Zeste Homolog 1; ELISA: enzyme-linked immunosorbent assay; ANOVA: analysis of variance. Error bars represent the mean?±?standard deviation (n = 3). Compared with OE-NC group, aP < 0.05, bP < 0.001; compared with siRNA-NC group, cP < 0.0.05. The statistical analyses included one-way ANOVA and t-tests to compare differences among treatment groups.

Table 3 CircEZH1 deletion alters glucose tolerance ($\bar{x}$ ± s)

Group	n	Blood Glucose (mg/dL)					Fasting glucose (mg/dL)	Summed GTT (AUC)
Group	n	0 min	30 min	60 min	90 min	120 min	Fasting glucose (mg/dL)	Summed GTT (AUC)
Ctrl	5	107±11	107±11	21681±1252	104±9	93±11	107±11	21681±1252
T2DM	5	222±22^a	222±22^a	39166±2498^a	284±50^a	196±14^a	222±22^a	39166±2498^a
T2DM+CircEZH1-siRNA	5	251±5^a	251±5^ab	47590±3093^ab	319±22^a	234±16^a	251±5^ac	47590±3093^ab

Table 4 CircEZH1 deletion promotes insulin resistance ($\bar{x}$ ± s)

Group	n	Blood Glucose (mg/dL)					Fasting glucose (mg/dL)	Summed GTT (AUC)
Group	n	0 min	30 min	60 min	90 min	120 min	Fasting glucose (mg/dL)	Summed GTT (AUC)
Ctrl	5	147±18	96±21	78±23	81±22	87±18	147±18	11161±2352
T2DM	5	219±18^a	125±14^c	107±15^c	111±16^c	126±25^f	219±18^a	15466±1500^f
T2DM+CircEZH1-siRNA	5	276±12^ab	169±9^ab	140±17^ad	138±4^ae	156±14^ae	276±12^ab	19910±655^ad

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