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Effects of acupuncture at Baihui (GV 20) and Zusanli (ST 36) on peripheral serum expression of MicroRNA 124, laminin and integrin β1 in rats with cerebral ischemia reperfusion injury

  • Acupuncture Research
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Abstract

Objective

To explore the effects of acupuncture at Baihui (GV 20) and Zusanli (ST 36) on the peripheral serum expression of microRNA 124 (miRNA 124), laminin and integrin β1 in rats with cerebral ischemia reperfusion injury (CIRI).

Methods

Seventy-two healthy male Sprague-Dawley rats were randomized into a model group, an acupuncture group, and a sham-operated group using a random digits table, with 24 rats per group. Each group was further randomly divided into 1-, 3-, 5-, and 7-day subgroups based on the reperfusion time according to a random digits table, with 6 rats in each subgroup. In the model and acupuncture groups, CIRI was induced using the thread occlusion method. Electroacupuncture stimulation was applied daily to GV 20 and left ST 36 for 20 min at the indicated time points after successful operations. Serum was sampled for detecting laminin and integrin β1 protein via enzyme-linked immunosorbent assay, and serum miRNA 124 was examined using quantitative polymerase chain reaction.

Results

The serum level of miRNA 124 in the cerebral ischemia rats increased significantly, and the peak expression of miRNA 124 in both the model and acupuncture groups occurred at 3 days. The expression of miRNA 124 in the acupuncture group was higher than in the model group at the same time point (5.96±0.01 vs. 3.11±0.04, P <0.05). Laminin expression in serum from the cerebral ischemia group was higher than that in the sham-operated group. Compared with the model group, the level of laminin in the serum of the acupuncture group was significantly lower at each time point, especially at the 3-day, and 7-day time points (589.12±3.57 vs. 793.05±5.28, and 600.53±3.05 vs. 899.06±5.74, P <0.05). The level of integrin β1 in the serum from the acupuncture group was lower than that in the model group particularly at the 3-day and 7-day time points (208.66±0.95 vs. 280.83±1.77, and 212.36±0.95 vs. 316.77±2.42, P <0.05). Additionally, the model group and the acupuncture group showed dual peaks of integrin β1 and laminin expression at 3-day and 7-day.

Conclusions

Acupuncture at GV 20 and ST 36 in rats alleviated CIRI and was associated with upregulated expression of miRNA 124 and with downregulated expression of integrin β1 and laminin in peripheral serum. These changes may represent one of the mechanisms underlying acupuncture’s attenuation of CIRI.

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References

  1. Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Blaha MJ, et al. Heart disease and stroke statistics–2014 update: a report from the American Heart Association. Circulation 2014;129(3):e28–e292.

    Article  PubMed  Google Scholar 

  2. Chen X, Ba Y, Ma L, Cai X, Yin Y, Wang K, et al. Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res 2008;18:997–1006.

    Article  PubMed  CAS  Google Scholar 

  3. Mishima T, Mizuguchi Y, Kawahigashi Y, Takizawa T, Takizawa T. RT-PCR-based analysis of microRNA (miR-1 and -124) expression in mouse CNS. Brain Res 2007;1131:37–43.

    Article  PubMed  CAS  Google Scholar 

  4. Liu X, Li F, Zhao S, Luo Y, Kang J, Zhao H, et al. MicroRNA-124-mediated regulation of inhibitory member of apoptosis-stimulating protein of p53 family in experimental stroke. Stroke 2013;44:1973–1980.

    Article  PubMed  CAS  Google Scholar 

  5. Akerblom M, Sachdeva R, Barde I, Verp S, Gentner B, Trono D, et al. MicroRNA-124 is a subventricular zone neuronal fate determinant. J Neurosci 2012;32:8879–8889.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Liu FJ, Lim KY, Kaur P, Sepramaniam S, Armugam A, Wong PT, et al. MicroRNAs involved in regulating spontaneous recovery in embolic stroke model. PLoS One 2013;8(6):e66393.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  7. Chen LF, Fang JQ, Wu YY, Ma RJ, Xu SY, Shen LH, et al. Motor dysfunction in stroke of subacute stage treated with acupuncture: multi-central randomized controlled study. Chin Acupunct Moxibust (Chin) 2014;34:313–318.

    Google Scholar 

  8. Dong QJ, Yang ZX. Systematic review of resuscitation needling technique for wind stroke. Chin Acupunct Moxibust (Chin) 2013;33:475–480.

    CAS  Google Scholar 

  9. Tang X, Tang CL, Xu FM, Xie HW, Li LM, Song YE. Effect of scalp acupuncture combined with body acupuncture on limb function in subacute stroke patients. Acupunct Res (Chin) 2012;37:488–492.

    Google Scholar 

  10. Zhao YL, Li WC, Huang J, Fu ZL, Tan LQ, Tang ZA, et al. Effects of jingjin acupuncture on fine activity of hemiplegic hand in recovery period of stroke. Chin Acupunct Moxibust (Chin) 2014;34:120–124.

    Google Scholar 

  11. Chen SH, Sun H, Xu H, Zhang YM, Gao Y, Li S. Effects of acupuncture of Baihui (GV 20) and Zusanli (ST 36) on the expreβsion of cerebral IL-1ß and TNF-a proteins in cerebral ischemia reperfusion injury rats. Acupunct Res (Chin) 2012;37:470–475.

    CAS  Google Scholar 

  12. Chen SH, Sun H, Xu H, Zhang YM, Wang FM, Gao Y. Effects of acupuncture of Baihui (GV 20) and Zusanli (ST 36) on the expression of interleukin-6 in bilateral rats’ brain after cerebral ischemia reperfusion injury. J Clin Acupunct Moxibust (Chin) 2014;30(1):42–46.

    CAS  Google Scholar 

  13. Longa EZ, Weinstein PR, Carlson S, Cummins R. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 1989;20:84–91.

    Article  PubMed  CAS  Google Scholar 

  14. Bederson JB, Pitts LH, Tsuji M, Nishimura MC, Davis RL, Bartkowski H. Rat middle cerebral artery occlusion: evaluation of the model and development of a neurologic examination. Stroke 1986;17:472–476.

    Article  PubMed  CAS  Google Scholar 

  15. Li ZR, ed. Experimental acupuncturology. Beijing: China Press of Traditional Chinese Medicine; 2007:255.

  16. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods 2001;25:402–408.

    Article  PubMed  CAS  Google Scholar 

  17. Liu S, Agalliu D, Yu C, Fisher M. The role of pericytes in blood-brain barrier function and stroke. Curr Pharm Des 2012;18:3653–3662.

    Article  PubMed  CAS  Google Scholar 

  18. Richardson RM, Singh A, Sun D, Fillmore HL, Dietrich DW, Bullock MR. Stem cell biology intraumatic brain injury: effects of injury and strategies for repair. J Neurosurg 2010;12:1125–1138.

    Article  Google Scholar 

  19. Plate KH. Mechanisms of angiogenesis in the brain. J Neuropathol Exp Neurol 1999;58:313–320.

    Article  PubMed  CAS  Google Scholar 

  20. Arenillas JF, Sobrino T, Castillo J, Dávalos A. The role of angiogenesis in damage and recovery from ischemic stroke. Curr Treat Options Cardiovasc Med 2007;9:205–212.

    Article  PubMed  Google Scholar 

  21. Zhang YM, Xu H, Sun H, Chen SH, Wang FM. Electroacupuncture treatment improves neurological function associated with regulation of tight junction proteins in rats with cerebral ischemia reperfusion injury. Evid Based Complement Alternat Med 2014;2014:989340.

  22. Xu H, Zhang Y, Sun H, Chen S, Wang F. Effects of acupuncture at GV20 and ST36 on the expression of matrix metalloproteinase 2, aquaporin 4, and aquaporin 9 in rats subjected to cerebral ischemia/reperfusion injury. PLoS One 2014;9(5):e97488.

    Google Scholar 

  23. Nam MH, Ahn KS, Choi SH. Acupuncture stimulation induces neurogenesis in adult brain. Int Rev Neurobiol 2013;111:67–90.

    Article  PubMed  Google Scholar 

  24. Cheng LC, Pastrana E, Tavazoie M, Doetsch F. Mir-124 regulates adult neurogenesis in the subventricular zone stem cell niche. Nat Neurosci 2009;12:399–408.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  25. Akerblom M, Sachdeva R, Barde I, Verp S, Gentner B, Trono D, et al. MicroRNA-124 is a subventricular zone neuronal fate determinant. J Neurosci 2012;32:8879–8889.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Cheng LC, Pastrana E, Tavazoie M, Doetsch F. miR-124 regulates adult neurogenesis in the subventricular zone stem cell niche. Nat Neurosci 2009;12:399–408.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  27. Sun Y, Gui H, Li Q, Luo ZM, Zheng MJ, Duan JL, et al. MicroRNA-124 protects neurons against apoptosis in cerebral ischemic stroke. CNS Neurosci Ther 2013;19:813–819.

    Article  PubMed  CAS  Google Scholar 

  28. Gao FB. Context-dependent functions of specific microRNAs in neuronal development. Neural Dev 2010;5:25.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Sun Y, Gui H, Li Q, Luo ZM, Zheng MJ, Duan JL, et al. MicroRNA-124 protects neurons against apoptosis in cerebral ischemic stroke. CNS Neurosci Ther 2013;19:813–819.

    Article  PubMed  CAS  Google Scholar 

  30. Jeyaseelan K, Lim KY, Armugam A. MicroRNA expression in the blood and brain of rats subjected to transient focal ischemia by middle cerebral artery occlusion. Stroke 2008;39:959–966.

    Article  PubMed  CAS  Google Scholar 

  31. Weng H, Shen C, Hirokawa G, Ji X, Takahashi R, Shimada K, et al. Plasma miR-124 as a biomarker for cerebral infarction. Biomed Res 2011;32:135–141.

    Article  PubMed  CAS  Google Scholar 

  32. Laterza OF, Lim L, Garrett-Engele PW, Vlasakova K, Muniappa N, Tanaka WK, et al. Plasma microRNAs as sensitive and specific biomarkers of tissue injury. Clin Chem 2009;55:1977–1983.

    Article  PubMed  CAS  Google Scholar 

  33. Liu Y, Wang Y, Liao W, Niu X, Hu B, Deng ZF. Dynamic change and significance of miR-124 expression in subependymal zone after ischemic brain injury in rats. Chin J Minim Invasive Neurosurg (Chin) 2013;18:417–419.

    CAS  Google Scholar 

  34. Persidsky Y, Ramirez SH, Haorah J, Kanmogne GD. Blood-brain barrier: structural components and function under physiologic and pathologic conditions. J Neuroimm Pharmacol 2006;1:223–236.

    Article  Google Scholar 

  35. Guillemin GJ, Brew BJ. Microglia, macrophages, perivascular macrophages, and pericytes: a review of function and identification. J Leukoc Biol 2004;75:388–397.

    Article  PubMed  CAS  Google Scholar 

  36. Hawkins BT, Davis TP. The blood-brain barrier/neurovascular unit in health and disease. Pharmacol Rev 2005;57:173–185.

    Article  PubMed  CAS  Google Scholar 

  37. Abbott NJ, Ronnback L, Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 2006;7:41–53.

    Article  PubMed  CAS  Google Scholar 

  38. Yurchenco PD, Patton BL. Developmental and pathogenic mechanisms of basement membrane assembly. Curr Pharm Des 2009;15:1277–1294.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  39. Willis CL, Camire RB, Brule SA, Ray DE. Partial recovery of the damaged rat blood–brain barrier is mediated by adherens junction complexes, extracellular matrix remodeling and macrophage infiltration following focal astrocyte loss. Neuroscience 2013;250:773–785.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  40. Form DM, Pratt BM, Madri JA. Endothelial cell proliferation during angiogenesis. In vitro modulation by basement membrane components. Lab Invest 1986;55:521–530.

    PubMed  CAS  Google Scholar 

  41. Al-Jamal R, Harrison DJ. Beta1 integrin in tissue remodelling and repair: from phenomena to concepts. Pharmacol Ther 2008;120:81–101.

    Article  PubMed  CAS  Google Scholar 

  42. Milner R, Campbell IL. Developmental regulation of beta1 integrins during angiogenesis in the central nervous system. Mol Cell Neurosci 2002;20:616–626.

    Article  PubMed  CAS  Google Scholar 

  43. Carlson TR, Hu H, Braren R, Kim YH, Wang RA. Cellautonomous requirement for beta1 integrin in endothelial cell adhesion, migration and survival during angiogenesis in mice. Development 2008;135:2193–2202.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  44. Milner R, Hung S, Wang X, Berg GI, Spatz M, del Zoppo GJ. Responses of endothelial cell and astrocyte matrixintegrin receptors to ischemia mimic those observed in the neurovascular unit. Stroke 2008;39:191–197.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Lathia JD, Chigurupati S, Thundyil J, Selvaraj PK, Mughal MR, Woodruff TM, et al. Pivotal role for beta-1 integrin in neurovascular remodelling after ischemic stroke. Exp Neurol 2010;221:107–114.

    Article  PubMed  CAS  Google Scholar 

  46. Xu H, Sun H, Chen SH, Zhang YM, Piao YL, Gao Y. Effects of acupuncture at Baihui (DU 20) and Zusanli (ST 36) on the expression of heat shock protein 70 and tumor necrosis factor α in the peripheral serum of cerebral ischemiareperfusion-injured rats. Chin J Integr Med 2014;20:369–374.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Traditional Chinese Medicine, Peking Union Medical College Hospital, Peking Union Medical College, Chinese Academy of Medical Sciences, Beijing, 100730, China

    Su-hui Chen  (陈素辉), Hua Sun  (孙 华), Ya-min Zhang  (张亚敏), Hong Xu  (徐 虹), Yang Yang  (杨 杨) & Fu-ming Wang  (王富明)

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  1. Su-hui Chen  (陈素辉)
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  2. Hua Sun  (孙 华)
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  3. Ya-min Zhang  (张亚敏)
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  4. Hong Xu  (徐 虹)
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  5. Yang Yang  (杨 杨)
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  6. Fu-ming Wang  (王富明)
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Corresponding author

Correspondence to Hua Sun  (孙 华).

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Supported by the National Natural Science Foundation of China (No. 81273850)

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Chen, Sh., Sun, H., Zhang, Ym. et al. Effects of acupuncture at Baihui (GV 20) and Zusanli (ST 36) on peripheral serum expression of MicroRNA 124, laminin and integrin β1 in rats with cerebral ischemia reperfusion injury. Chin. J. Integr. Med. 22, 49–55 (2016). https://doi.org/10.1007/s11655-015-2112-7

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  • DOI: https://doi.org/10.1007/s11655-015-2112-7

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