Journal of Traditional Chinese Medicine ›› 2023, Vol. 43 ›› Issue (4): 686-694.DOI: 10.19852/j.cnki.jtcm.2023.04.005
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Analgesic efficacy of median nerve stimulation in mice with chemotherapy-induced peripheral neuropathy via modulation of brain-derived neurotrophic factor expression
Dong-Wook Kang1, Jae-Gyun Choi1, Hee Ju Song1, Jaehyuk Kim1, Miae Lee1, Taehee Kim1, Suk-Yun Kang2, Yeonhee Ryu2, Hwa Seung Yoo3, Jin Sun Lee4, Jin Bong Park5, Sang Do Lee1(
), Hyun-Woo Kim1()
- 1 Department of Physiology and Medical Science, College of Medicine and Brain Research Institute, Chungnam National University, Daejeon 35015, Republic of Korea
2 KM Fundamental Research Division Korea Institute of Oriental Medicine, Daejeon 34054, Republic of Korea
3 East-West Cancer Center, Dunsan Korean Medicine Hospital of Daejeon University, Daejeon 35234, Republic of Korea
4 Department of Surgery, Chungnam National University Hospital, Daejeon 35015, Republic of Korea
5 Laboratory of Veterinary Pharmacology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, 1 Gwanak-ro, Gwanak-gu, Seoul 08826, Republic of Korea
-
Received:2021-12-16Accepted:2022-08-03Online:2023-08-15Published:2023-07-03 -
Contact:Hyun-Woo Kim, Department of Physiology and Medical Science, College of Medicine and Brain Research Institute, Chungnam National University, Daejeon 35015, Republic of Korea. kim0827@cnu.ac.kr. Telephone: +82-42-580-8220; +82-42-580-8217
Sang Do Lee, Department of Physiology and Medical Science, College of Medicine, Chungnam National University, Daejeon 35015, Republic of Korea. sdlee@cnu.ac.kr -
Supported by:“Korea Health Technology R & D Project through the Korea Health Industry Development Institute, funded by the Ministry of Health and Welfare, Republic of Korea(HI15C0007);“Chungnam National University, and Basic Science Research Program through the National Research Foundation of Korea(2021R1F1A1062509);Study on the Angiotensin Converting Enzyme Inhibitor (ACEi)-related Pain Mechanism by Mediating Substance P, Bradykinin and Angiotensin II Activities(2021R1A6A3A01086598);Study on the Role and Interaction Mechanisms of BDNF and APE1/Ref-1 in Animal Models of Chronic Pain Accompanied with Depression
Cite this article
Dong-Wook Kang, Jae-Gyun Choi, Hee Ju Song, Jaehyuk Kim, Miae Lee, Taehee Kim, Suk-Yun Kang, Yeonhee Ryu, Hwa Seung Yoo, Jin Sun Lee, Jin Bong Park, Sang Do Lee, Hyun-Woo Kim. Analgesic efficacy of median nerve stimulation in mice with chemotherapy-induced peripheral neuropathy via modulation of brain-derived neurotrophic factor expression[J]. Journal of Traditional Chinese Medicine, 2023, 43(4): 686-694.
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Table 1 Changes in body weight after DTX injection (g)
| Group | n | Pre BW | Day 2 BW | Day 4 BW | Day 6 BW | Day 12 BW | Day 20 BW | Day 22 BW |
|---|---|---|---|---|---|---|---|---|
| Vehicle DTX | 5 7 | 30.7±0.5 30.0±1.1 | 31.2±0.5 31.9±0.8 | 32.4±0.5 33.2±0.8 | 33.0±0.6 33.4±0.9 | 35.1±0.8 36.2±1.1 | 36.6±1.0 36.3±1.2 | 36.2±0.9 37.7±1.3 |
Table 1 Changes in body weight after DTX injection (g)
| Group | n | Pre BW | Day 2 BW | Day 4 BW | Day 6 BW | Day 12 BW | Day 20 BW | Day 22 BW |
|---|---|---|---|---|---|---|---|---|
| Vehicle DTX | 5 7 | 30.7±0.5 30.0±1.1 | 31.2±0.5 31.9±0.8 | 32.4±0.5 33.2±0.8 | 33.0±0.6 33.4±0.9 | 35.1±0.8 36.2±1.1 | 36.6±1.0 36.3±1.2 | 36.2±0.9 37.7±1.3 |
Table 2 Changes in pain response after DTX injection (%)
| Group | n | Pre PWF | Day 2 PWF | Day 4 PWF | Day 6 PWF | Day 12 PWF | Day 20 PWF | Day 22 PWF |
|---|---|---|---|---|---|---|---|---|
| Vehicle DTX | 5 7 | 9.0±1.9 11.4±2.1 | 9.0±1.9 43.6±8.8a | 10.0±1.6 62.1±6.3a | 9.0±2.9 65.7±3.0a | 11.0±3.7 66.4±4.0a | 10.0±1.6 62.1±5.0a | 11.0±4.0 33.6±5.1b |
Table 2 Changes in pain response after DTX injection (%)
| Group | n | Pre PWF | Day 2 PWF | Day 4 PWF | Day 6 PWF | Day 12 PWF | Day 20 PWF | Day 22 PWF |
|---|---|---|---|---|---|---|---|---|
| Vehicle DTX | 5 7 | 9.0±1.9 11.4±2.1 | 9.0±1.9 43.6±8.8a | 10.0±1.6 62.1±6.3a | 9.0±2.9 65.7±3.0a | 11.0±3.7 66.4±4.0a | 10.0±1.6 62.1±5.0a | 11.0±4.0 33.6±5.1b |
Figure 1 Effect of intraperitoneal administration of ANA-12 on DTX-induced mechanical allodynia Multiple injections of DTX induced mechanical hypersensitivity, and this pain response was significantly attenuated by intraperitoneal administration of ANA-12, the specific TrkB receptor antagonist. DTX group: CIPN model mice without treatment (n = 7); DTX + ANA-12 group: CIPN model mice treated with ANA-12 (1 mg/kg) (n = 8). DTX: docetaxel; ANA-12: N-[2-[(2-oxoazepan-3-yl) carbamoyl] phenyl]-1-benzothiophene-2-carboxamide; CIPN: chemotherapy-induced peripheral neuropathy. aP < 0.01, bP < 0.001 and cP < 0.05 compared with DTX group. Differences among groups analyzed by two-way analysis of variance.
Figure 1 Effect of intraperitoneal administration of ANA-12 on DTX-induced mechanical allodynia Multiple injections of DTX induced mechanical hypersensitivity, and this pain response was significantly attenuated by intraperitoneal administration of ANA-12, the specific TrkB receptor antagonist. DTX group: CIPN model mice without treatment (n = 7); DTX + ANA-12 group: CIPN model mice treated with ANA-12 (1 mg/kg) (n = 8). DTX: docetaxel; ANA-12: N-[2-[(2-oxoazepan-3-yl) carbamoyl] phenyl]-1-benzothiophene-2-carboxamide; CIPN: chemotherapy-induced peripheral neuropathy. aP < 0.01, bP < 0.001 and cP < 0.05 compared with DTX group. Differences among groups analyzed by two-way analysis of variance.
Table 3 Restoration of normal motor function over time after anesthesia (s)
| Group | n | Pre RT | 0 min RT | 20 min RT | 40 min RT | 60 min RT | 80 min RT | 100 min RT |
|---|---|---|---|---|---|---|---|---|
| Vehicle Avertin | 5 5 | 116.6±2.4 120.0±0.0 | 118.6±1.0 19.0±9.9a | 120.0±0.0 0.0±0.0a | 119.6±0.4 0.0±0.0a | 120.0±0.0 15.8±4.9a | 119.4±0.6 56.4±7.4a | 120.0±0.0 117.6±2.4 |
Table 3 Restoration of normal motor function over time after anesthesia (s)
| Group | n | Pre RT | 0 min RT | 20 min RT | 40 min RT | 60 min RT | 80 min RT | 100 min RT |
|---|---|---|---|---|---|---|---|---|
| Vehicle Avertin | 5 5 | 116.6±2.4 120.0±0.0 | 118.6±1.0 19.0±9.9a | 120.0±0.0 0.0±0.0a | 119.6±0.4 0.0±0.0a | 120.0±0.0 15.8±4.9a | 119.4±0.6 56.4±7.4a | 120.0±0.0 117.6±2.4 |
Figure 2 Effect of repeated LFMNS on DTX-induced mechanical allodynia A: changes in body weight during the experiment period. There was no significant weight loss during the experimental period; B: changes in pain response during the experimental period. Multiple injections of DTX induced mechanical hypersensitivity, and this pain response was significantly attenuated by repeated LFMNS at the wrist area. Vehicle group: 5% DMSO injected mice (n = 5); DTX group: CIPN model mice without treatment (n = 10); DTX + LFMNS group: CIPN model mice treated with LFMNS (n = 10); DTX + LFMNS + Dulo. group: CIPN model mice treated with LFMNS combined with Duloxetine (10 mg/kg) (n = 10). DTX: docetaxel; LFMNS: low-frequency median nerve stimulation; Dulo: duloxetine; DMSO: dimethyl sulfate solution; CIPN: chemotherapy-induced peripheral neuropathy. aP < 0.01, bP < 0.001 DTX + LFMNS group vs DTX group; cP < 0.01, dP < 0.001 DTX + LFMNS + Dulo. group vs DTX group; eP < 0.05 DTX + LFMNS group vs DTX + LFMNS + Dulo. group. Differences among groups analyzed by two-way analysis of variance.
Figure 2 Effect of repeated LFMNS on DTX-induced mechanical allodynia A: changes in body weight during the experiment period. There was no significant weight loss during the experimental period; B: changes in pain response during the experimental period. Multiple injections of DTX induced mechanical hypersensitivity, and this pain response was significantly attenuated by repeated LFMNS at the wrist area. Vehicle group: 5% DMSO injected mice (n = 5); DTX group: CIPN model mice without treatment (n = 10); DTX + LFMNS group: CIPN model mice treated with LFMNS (n = 10); DTX + LFMNS + Dulo. group: CIPN model mice treated with LFMNS combined with Duloxetine (10 mg/kg) (n = 10). DTX: docetaxel; LFMNS: low-frequency median nerve stimulation; Dulo: duloxetine; DMSO: dimethyl sulfate solution; CIPN: chemotherapy-induced peripheral neuropathy. aP < 0.01, bP < 0.001 DTX + LFMNS group vs DTX group; cP < 0.01, dP < 0.001 DTX + LFMNS + Dulo. group vs DTX group; eP < 0.05 DTX + LFMNS group vs DTX + LFMNS + Dulo. group. Differences among groups analyzed by two-way analysis of variance.
Figure 3 Expression change of BDNF protein and mRNA in lumbar 4-5 segment DRG DRG samples were collected 5 d after the first treatment of LFMNS. A: changes in pain response during the experimental period. LFMNS treated groups have shown significant analgesic effects in the pain response test. Vehicle group: 5% DMSO injected mice (n = 5); DTX group: CIPN model mice without treatment (n = 7); DTX + LFMNS group: CIPN model mice treated with LFMNS (n = 8); DTX + LFMNS + Dulo. group: CIPN model mice treated with LFMNS combined with Duloxetine (10 mg/kg) (n = 8). aP < 0.01 DTX + LFMNS group vs DTX group, bP < 0.01 DTX + LFMNS + Dulo. group vs DTX group. Differences among groups analyzed by two-way analysis of variance. B-C: changes in the molecular expression of DRG neurons. DTX injected mice showed a significantly enhanced BDNF protein expression in DRG neurons and repeated LFMNS were suppressed this increment (B1/B2/B3: G1; B4/B5/B6: G2; B7/B8/B9: G3; B10/B11/B12: G4, × 100). G1: Vehicle group; G2: DTX group; G3: DTX + LFMNS group; G4: DTX + LFMNS + Dulo. group. Vehicle group: 5% DMSO injected mice (n = 5); DTX group: CIPN model mice without treatment (n = 6); DTX + LFMNS group: CIPN model mice treated with LFMNS (n = 6); DTX + LFMNS + Dulo. group: CIPN model mice treated with LFMNS combined with Duloxetine (10 mg/kg) (n = 6). D: changes in the BDNF mRNA expression of DRG. DTX-injected mice showed significantly enhanced BDNF mRNA expression in DRG, and repeated LFMNS suppressed this increment. G1: Vehicle group; G2: DTX group; G3: DTX + LFMNS group; G4: DTX + LFMNS + Dulo. group. Vehicle group: 5% DMSO injected mice (n = 5); DTX group: CIPN model mice without treatment (n = 7); DTX + LFMNS group: CIPN model mice treated with LFMNS (n = 7); DTX + LFMNS + Dulo. group: CIPN model mice treated with LFMNS combined with Duloxetine (10 mg/kg) (n = 7). B1/B4/B7/B10: expressed NeuN in the DRG; B2/B5/B8/B11: expressed BDNF in the DRG; B3/B6/B9/B12: merged images of NeuN and BDNF. DTX: docetaxel; LFMNS: low-frequency median nerve stimulation; Dulo.: duloxetine; DMSO: dimethyl sulfate solution; CIPN: chemotherapy-induced peripheral neuropathy; DRG: dorsal root ganglion; BDNF: brain-derived neurotrophic factor. cP < 0.01 and dP < 0.001 compared with DTX group. eP > 0.05, no significant difference DTX + LFMNS group vs DTX + LFMNS + Dulo. group. Differences among groups analyzed by one-way analysis of variance.
Figure 3 Expression change of BDNF protein and mRNA in lumbar 4-5 segment DRG DRG samples were collected 5 d after the first treatment of LFMNS. A: changes in pain response during the experimental period. LFMNS treated groups have shown significant analgesic effects in the pain response test. Vehicle group: 5% DMSO injected mice (n = 5); DTX group: CIPN model mice without treatment (n = 7); DTX + LFMNS group: CIPN model mice treated with LFMNS (n = 8); DTX + LFMNS + Dulo. group: CIPN model mice treated with LFMNS combined with Duloxetine (10 mg/kg) (n = 8). aP < 0.01 DTX + LFMNS group vs DTX group, bP < 0.01 DTX + LFMNS + Dulo. group vs DTX group. Differences among groups analyzed by two-way analysis of variance. B-C: changes in the molecular expression of DRG neurons. DTX injected mice showed a significantly enhanced BDNF protein expression in DRG neurons and repeated LFMNS were suppressed this increment (B1/B2/B3: G1; B4/B5/B6: G2; B7/B8/B9: G3; B10/B11/B12: G4, × 100). G1: Vehicle group; G2: DTX group; G3: DTX + LFMNS group; G4: DTX + LFMNS + Dulo. group. Vehicle group: 5% DMSO injected mice (n = 5); DTX group: CIPN model mice without treatment (n = 6); DTX + LFMNS group: CIPN model mice treated with LFMNS (n = 6); DTX + LFMNS + Dulo. group: CIPN model mice treated with LFMNS combined with Duloxetine (10 mg/kg) (n = 6). D: changes in the BDNF mRNA expression of DRG. DTX-injected mice showed significantly enhanced BDNF mRNA expression in DRG, and repeated LFMNS suppressed this increment. G1: Vehicle group; G2: DTX group; G3: DTX + LFMNS group; G4: DTX + LFMNS + Dulo. group. Vehicle group: 5% DMSO injected mice (n = 5); DTX group: CIPN model mice without treatment (n = 7); DTX + LFMNS group: CIPN model mice treated with LFMNS (n = 7); DTX + LFMNS + Dulo. group: CIPN model mice treated with LFMNS combined with Duloxetine (10 mg/kg) (n = 7). B1/B4/B7/B10: expressed NeuN in the DRG; B2/B5/B8/B11: expressed BDNF in the DRG; B3/B6/B9/B12: merged images of NeuN and BDNF. DTX: docetaxel; LFMNS: low-frequency median nerve stimulation; Dulo.: duloxetine; DMSO: dimethyl sulfate solution; CIPN: chemotherapy-induced peripheral neuropathy; DRG: dorsal root ganglion; BDNF: brain-derived neurotrophic factor. cP < 0.01 and dP < 0.001 compared with DTX group. eP > 0.05, no significant difference DTX + LFMNS group vs DTX + LFMNS + Dulo. group. Differences among groups analyzed by one-way analysis of variance.
Figure 4 Expression change of BDNF protein and mRNA in lumbar 4-5 segment spinal cord dorsal area Lumbar spinal cord samples were collected 5 d after the first treatment of LFMNS. A-B: changes in the molecular expression of spinal cord after treatment. DTX injected mice showed a significantly enhanced BDNF protein expression in the Lumbar spinal cord dorsal area, and repeated LFMNS have suppressed this increment. G1: Vehicle group; G2: DTX group; G3: DTX + LFMNS group; G4: DTX + LFMNS + Dulo. group. Vehicle group: 5% DMSO injected mice (n = 3); DTX group: CIPN model mice without treatment (n = 3); DTX + LFMNS group: CIPN model mice treated with LFMNS (n = 3); DTX + LFMNS + Dulo. group: CIPN model mice treated with LFMNS combined with Duloxetine (10 mg/kg) (n = 3). C: changes in the BDNF mRNA expression of spinal cord. There are no changes observed in spinal cord expressions of BDNF mRNA. G1: Vehicle group; G2: DTX group; G3: DTX + LFMNS group; G4: DTX + LFMNS + Dulo. group. Vehicle group: 5% DMSO injected mice (n = 5); DTX group: CIPN model mice without treatment (n = 7); DTX + LFMNS group: CIPN model mice treated with LFMNS (n = 7); DTX + LFMNS + Dulo. group: CIPN model mice treated with LFMNS combined with Duloxetine (10 mg/kg) (n = 7). DTX: docetaxel; LFMNS: low-frequency median nerve stimulation; Dulo.: duloxetine; DMSO: dimethyl sulfate solution; CIPN: chemotherapy-induced peripheral neuropathy; BDNF: brain-derived neurotrophic factor. aP < 0.05, bP < 0.01, compared with DTX group. Differences among groups analyzed by one-way analysis of variance.
Figure 4 Expression change of BDNF protein and mRNA in lumbar 4-5 segment spinal cord dorsal area Lumbar spinal cord samples were collected 5 d after the first treatment of LFMNS. A-B: changes in the molecular expression of spinal cord after treatment. DTX injected mice showed a significantly enhanced BDNF protein expression in the Lumbar spinal cord dorsal area, and repeated LFMNS have suppressed this increment. G1: Vehicle group; G2: DTX group; G3: DTX + LFMNS group; G4: DTX + LFMNS + Dulo. group. Vehicle group: 5% DMSO injected mice (n = 3); DTX group: CIPN model mice without treatment (n = 3); DTX + LFMNS group: CIPN model mice treated with LFMNS (n = 3); DTX + LFMNS + Dulo. group: CIPN model mice treated with LFMNS combined with Duloxetine (10 mg/kg) (n = 3). C: changes in the BDNF mRNA expression of spinal cord. There are no changes observed in spinal cord expressions of BDNF mRNA. G1: Vehicle group; G2: DTX group; G3: DTX + LFMNS group; G4: DTX + LFMNS + Dulo. group. Vehicle group: 5% DMSO injected mice (n = 5); DTX group: CIPN model mice without treatment (n = 7); DTX + LFMNS group: CIPN model mice treated with LFMNS (n = 7); DTX + LFMNS + Dulo. group: CIPN model mice treated with LFMNS combined with Duloxetine (10 mg/kg) (n = 7). DTX: docetaxel; LFMNS: low-frequency median nerve stimulation; Dulo.: duloxetine; DMSO: dimethyl sulfate solution; CIPN: chemotherapy-induced peripheral neuropathy; BDNF: brain-derived neurotrophic factor. aP < 0.05, bP < 0.01, compared with DTX group. Differences among groups analyzed by one-way analysis of variance.
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