314
Views
8
CrossRef citations to date
0
Altmetric
Research Articles

Extracellular vesicles from human umbilical cord mesenchymal stem cells reduce lipopolysaccharide-induced spinal cord injury neuronal apoptosis by mediating miR-29b-3p/PTEN

, , , , , , , , , & show all
Pages 634-649 | Received 01 Dec 2021, Accepted 28 Mar 2022, Published online: 22 May 2022

References

  • Anjum A, Yazid MD, Fauzi Daud M, Idris J, Ng AMH, Selvi Naicker A, Ismail OHR, Athi Kumar RK, Lokanathan Y. Spinal cord injury: pathophysiology, multimolecular interactions, and underlying recovery mechanisms. Int J Mol Sci. 2020;21(20):7533.doi:10.3390/ijms21207533.
  • Ahuja CS, Nori S, Tetreault L, Wilson J, Kwon B, Harrop J, Choi D, Fehlings MG. Traumatic spinal cord injury-repair and regeneration. Neurosurgery. 2017;80(3S):S9–S22.doi:10.1093/neuros/nyw080.
  • Eckert MJ, Martin MJ. Trauma: spinal Cord Injury. Surg Clin North Am. 2017;97(5):1031–1045.doi:10.1016/j.suc.2017.06.008.
  • Ambrozaitis KV, Kontautas E, Spakauskasand B, Vaitkaitis D. [Pathophysiology of acute spinal cord injury]. Medicina (Kaunas). 2006;42(3):255–261.
  • Fan B, Wei Z, Yao X et al. Microenvironment imbalance of spinal cord injury. Cell Transplant. 2018;27:853–866.
  • Liang B, Liang JM, Ding JN, Xu J, Xuand JG, Chai YM. Dimethyloxaloylglycine-stimulated human bone marrow mesenchymal stem cell-derived exosomes enhance bone regeneration through angiogenesis by targeting the AKT/mTOR pathway. Stem Cell Res Ther. 2019;10(1):335.doi:10.1186/s13287-019-1410-y.
  • Fong CY, Subramanian A, Biswas A, Gauthaman K, Srikanth P, Hande MP, Bongso A. Derivation efficiency, cell proliferation, freeze-thaw survival, stem-cell properties and differentiation of human Wharton’s jelly stem cells. Reprod Biomed Online. 2010;21(3):391–401.doi:10.1016/j.rbmo.2010.04.010.
  • Guo ZY, Sun X, Xu XL, Zhao Q, Pengand J, Wang Y. Human umbilical cord mesenchymal stem cells promote peripheral nerve repair via paracrine mechanisms. Neural Regen Res. 2015;10(4):651–658.doi:10.4103/1673-5374.155442.
  • Kern S, Eichler H, Stoeve J, Kluterand H, Bieback K. Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells. 2006;24(5):1294–1301.doi:10.1634/stemcells.2005-0342.
  • Li Z, Qin H, Feng Z, Liu W, Zhou Y, Yang L, Zhao W, Li Y. Human umbilical cord mesenchymal stem cell-loaded amniotic membrane for the repair of radial nerve injury. Neural Regen Res. 2013;8(36):3441–3448.doi:10.3969/j.1673-5374.2013.36.010.
  • Ma J, Zhao Y, Sun L, Sun X, Zhao X, Sun X, Qian H, Xu W, Zhu W. Exosomes derived from akt -modified human umbilical cord mesenchymal stem cells improve cardiac regeneration and promote angiogenesis via activating platelet-derived growth factor D. Stem Cells Transl Med. 2017;6(1):51–59.doi:10.5966/sctm.2016-0038.
  • Hu SL, Luo HS, Li JT, Xia Y-Z, Li L, Zhang L-J, Meng H, Cui G-Y, Chen Z, Wu N, Lin J-K, Zhu G, Feng H. Functional recovery in acute traumatic spinal cord injury after transplantation of human umbilical cord mesenchymal stem cells. Crit Care Med. 2010;38(11):2181–2189.doi:10.1097/CCM.0b013e3181f17c0e.
  • Li X, Tan J, Xiao Z, Zhao Y, Han S, Liu D, Yin W, Li J, Li J, Wanggou S, Chen B, Ren C, Jiang X, Dai J. Transplantation of hUC-MSCs seeded collagen scaffolds reduces scar formation and promotes functional recovery in canines with chronic spinal cord injury. Sci Rep. 2017;7(1):43559.doi:10.1038/srep43559.
  • Dutta D, Khan N, Wu J, Jay SM. Extracellular Vesicles as an Emerging Frontier in Spinal Cord Injury Pathobiology and Therapy. Trends Neurosci. 2021;44(6):492–506.
  • Khan NZ, Cao T, He J, Ritzel RM, Li Y, Henry RJ, Colson C, Stoica BA, Faden AI, Wu J. Spinal cord injury alters microRNA and CD81+ exosome levels in plasma extracellular nanoparticles with neuroinflammatory potential. Brain Behav Immun. 2021;92:165–183.doi:10.1016/j.bbi.2020.12.007.
  • de Rivero Vaccari JP, Brand F 3rd, Adamczak S, Lee SW, Perez‐Barcena J, Wang MY, … Keane RW. Exosome-mediated inflammasome signaling after central nervous system injury. J Neurochem. 2016;136 Suppl 1:39–48.doi:10.1111/jnc.13036.
  • Osier N, Motamedi V, Edwards K et al. Exosomes in acquired neurological disorders: new insights into pathophysiology and treatment. Mol Neurobiol. 2018;55(12):9280–9293. doi:10.1007/s12035-018-1054-4.
  • Zhou X, Chu X, Yuan H et al. Mesenchymal stem cell derived EVs mediate neuroprotection after spinal cord injury in rats via the microRNA-21-5p/FasL gene axis. Biomed Pharmacother. 2019;115:108818.
  • Yu T, Zhao C, Hou S, Zhou W, Wangand B, Chen Y. Exosomes secreted from miRNA-29b-modified mesenchymal stem cells repaired spinal cord injury in rats. Braz J Med Biol Res. 2019;52(12):e8735.doi:10.1590/1414-431x20198735.
  • Chandran R, Mehtaand SL, Vemuganti R. Non-coding RNAs and neuroprotection after acute CNS injuries. Neurochem Int. 2017;111:12–22.doi:10.1016/j.neuint.2017.01.015.
  • Liu NK, Xu XM. MicroRNA in central nervous system trauma and degenerative disorders. Physiol Genomics. 2011;43(10):571–580.doi:10.1152/physiolgenomics.00168.2010.
  • Chen L, Li Q, Wang J, Jin S, Zheng H, Lin J, He F, Zhang H, Ma S, Mei J, Yu J. MiR-29b-3p promotes chondrocyte apoptosis and facilitates the occurrence and development of osteoarthritis by targeting PGRN. J Cell Mol Med. 2017;21(12):3347–3359.doi:10.1111/jcmm.13237.
  • Khanna S, Rink C, Ghoorkhanian R, Gnyawali S, Heige M, Wijesinghe DS, Chalfant CE, Chan YC, Banerjee J, Huang Y et al. Loss of miR-29b following acute ischemic stroke contributes to neural cell death and infarct size. J Cereb Blood Flow Metab. 2013;33(8):1197–206.
  • Liu D, Wangand J, Liu M. Long noncoding RNA TUG1 promotes proliferation and inhibits apoptosis in multiple myeloma by inhibiting miR-29b-3p. Biosci Rep. 2019;39(3):BSR20182489.
  • Kole AJ, Swahari V, Hammond SM, Deshmukh M. miR-29b is activated during neuronal maturation and targets BH3-only genes to restrict apoptosis. Genes Dev. 2011;25(2):125–30.
  • Hobert JA, Embacher R, Mester JL, Frazier TW 2ndandC. Eng. Biochemical screening and PTEN mutation analysis in individuals with autism spectrum disorders and macrocephaly. Eur J Hum Genet. 2014;22(2):273–276.doi:10.1038/ejhg.2013.114.
  • Marchese M, Conti V, Valvo G, Moro F, Muratori F, Tancredi R, Santorelli FM, Guerrini R, Sicca F. Autism-epilepsy phenotype with macrocephaly suggests PTEN, but not GLIALCAM, genetic screening. BMC Med Genet. 2014;15(1):26.doi:10.1186/1471-2350-15-26.
  • Cao Y, Jiang C, Linand H, Chen Z. Silencing of long noncoding RNA growth arrest-specific 5 alleviates neuronal cell apoptosis and inflammatory responses through sponging microRNA-93 to repress PTEN expression in spinal cord injury. Front Cell Neurosci. 2021;15:646788.doi:10.3389/fncel.2021.646788.
  • He S, Wang Z, Li Y, Dong J, Xiang D, Ren L, Guo L, Shu J. MicroRNA-92a-3p enhances functional recovery and suppresses apoptosis after spinal cord injury via targeting phosphatase and tensin homolog. Biosci Rep. 2020;40(5). doi:10.1042/BSR20192743.
  • Li K, Liu J, Song L et al. Effect of electroacupuncture treatment at dazhui (GV14) and mingmen (GV4) modulates the PI3K/AKT/mTOR signaling pathway in rats after spinal cord injury. Neural Plast. 2020;2020:5474608.
  • Zhang M, Wang L, Huangand S, He X. Exosomes with high level of miR-181c from bone marrow-derived mesenchymal stem cells inhibit inflammation and apoptosis to alleviate spinal cord injury. J Mol Histol. 2021;52(2):301–311.doi:10.1007/s10735-020-09950-0.
  • Vernava AM, Goldberg SM. 3rdandS.M. Goldberg. Is the Kock pouch still a viable option? Int J Colorectal Dis. 1988;3(2):135–138.doi:10.1007/BF01645320.
  • Walker CL, Wu X, Liuand NK, Xu XM. Bisperoxovanadium mediates neuronal protection through inhibition of PTEN and activation of PI3K/AKT-mTOR signaling after traumatic spinal injuries. J Neurotrauma. 2019;36(18):2676–2687.doi:10.1089/neu.2018.6294.
  • Cai W, Wen H, Zhou Q, Wu L, Chen Y, Zhou H, Jin M. 14-Deoxy-11,12-didehydroandrographolide inhibits apoptosis in influenza A(H5N1) virus-infected human lung epithelial cells via the caspase-9-dependent intrinsic apoptotic pathway which contributes to its antiviral activity. Antiviral Res. 2020;181:104885.doi:10.1016/j.antiviral.2020.104885.
  • Dias MS. Traumatic brain and spinal cord injury. Pediatr Clin North Am. 2004;51(2):271–303.doi:10.1016/S0031-3955(03)00211-6.
  • Wang C, Wang Q, Lou Y, Xu J, Feng Z, Chen Y, Tang Q, Zheng G, Zhang Z, Wu Y, Tian N, Zhou Y, Xu H, Zhang X. Salidroside attenuates neuroinflammation and improves functional recovery after spinal cord injury through microglia polarization regulation. J Cell Mol Med. 2018;22(2):1148–1166.doi:10.1111/jcmm.13368.
  • Liu XJ, Zheng XP, Zhang R, Guoand YL, Wang JH. Combinatorial effects of miR-20a and miR-29b on neuronal apoptosis induced by spinal cord injury. Int J Clin Exp Pathol. 2015;8(4):3811–3818.
  • Yang Y, Cheng T, Xie P et al. PMEPA1 interference activates PTEN/PI3K/AKT, thereby inhibiting the proliferation, invasion and migration of pancreatic cancer cells and enhancing the sensitivity to gemcitabine and cisplatin. Drug Dev Res. 2021;83(1):64–74.
  • Chen Y, Wei Z, Liu J, Xie H, Wang B, Wu J, Zhu Z, Fan Y. Long noncoding RNA ZFAS1 aggravates spinal cord injury by binding with miR-1953 and regulating the PTEN/PI3K/AKT pathway. Neurochem Int. 2021;147:104977.doi:10.1016/j.neuint.2021.104977.
  • Lu Y, Zhou Y, Zhang R, Wen L, Wu K, Li Y, Yao Y, Duan R, Jia Y. Bone mesenchymal stem cell-derived extracellular vesicles promote recovery following spinal cord injury via improvement of the integrity of the blood-spinal cord barrier. Front Neurosci. 2019;13:209.doi:10.3389/fnins.2019.00209.
  • Porter AG, Janicke RU. Emerging roles of caspase-3 in apoptosis. Cell Death Differ. 1999;6(2):99–104.doi:10.1038/sj.cdd.4400476.
  • Zhao M, Zhang J, Huang W, Dong J, Guo J, U KP, Weng Z, Liu S, Chan HC, Feng H, Jiang X. CFTR promotes malignant glioma development via up-regulation of Akt/Bcl2-mediated anti-apoptosis pathway. J Cell Mol Med. 2020;24(13):7301–7312.doi:10.1111/jcmm.15300.
  • Baradaran Rahimi V, Rakhshandeh H, Raucci F, Buono B, Shirazinia R, Samzadeh Kermani A, Maione F, Mascolo N, Askari VR. Anti-Inflammatory and anti-oxidant activity of Portulaca oleracea extract on LPS-Induced rat lung injury. Molecules. 2019;24(1):139.doi:10.3390/molecules24010139.
  • Quertainmont R, Cantinieaux D, Botman O, Sid S, Schoenenand J, Franzen R, Rameshwar P. Mesenchymal stem cell graft improves recovery after spinal cord injury in adult rats through neurotrophic and pro-angiogenic actions. PLoS One. 2012;7(6):e39500.doi:10.1371/journal.pone.0039500.
  • Liu W, Rong Y, Wang J, Zhou Z, Ge X, Ji C, Jiang D, Gong F, Li L, Chen J, Zhao S, Kong F, Gu C, Fan J, Cai W. Exosome-shuttled miR-216a-5p from hypoxic preconditioned mesenchymal stem cells repair traumatic spinal cord injury by shifting microglial M1/M2 polarization. J Neuroinflammation. 2020;17(1):47.doi:10.1186/s12974-020-1726-7.
  • Zhang J, Li S, Li L, Li M, Guo C, Yao J, Mi S. Exosome and exosomal microRNA: trafficking, sorting, and function. Genomics Proteomics Bioinformatics. 2015;13(1):17–24.doi:10.1016/j.gpb.2015.02.001.
  • Bai G, Jiang L, Meng P, Li J, Han C, Wang Y, Wang Q. LncRNA neat1 promotes regeneration after spinal cord injury by targeting miR-29b. J Mol Neurosci. 2021;71(6):1174–1184.doi:10.1007/s12031-020-01740-3.
  • Xiao X, Li W, Rong D, Xu Z, Zhang Z, Ye H, Xie L, Wu Y, Zhang Y, Wang X. Human umbilical cord mesenchymal stem cells-derived extracellular vesicles facilitate the repair of spinal cord injury via the miR-29b-3p/PTEN/Akt/mTOR axis. Cell Death Discov. 2021;7(1):212.doi:10.1038/s41420-021-00572-3.
  • Kang J, Zhang C, Zhi Z, Wang Y, Liu J, Wu F, Xu G. Stem-like cells of various origins showed therapeutic effect to improve the recovery of spinal cord injury. Artif Cells Nanomed Biotechnol. 2020;48(1):627–638.doi:10.1080/21691401.2020.1725031.
  • Young W. Spinal cord regeneration. Cell Transplant. 2014;23(4–5):573–611.doi:10.3727/096368914X678427.
  • Chen J, Zhang C, Li S, Li Z, Laiand X, Xia Q, Wang K. Exosomes derived from nerve stem cells loaded with FTY720 promote the recovery after spinal cord injury in rats by PTEN/AKT signal pathway. J Immunol Res. 2021;2021:8100298.doi:10.1155/2021/8100298.
  • Guan C, Luan L, Liand J, Yang L. MiR-212-3p improves rat functional recovery and inhibits neurocyte apoptosis in spinal cord injury models via PTEN downregulation-mediated activation of AKT/mTOR pathway. Brain Res. 2021;1768:147576.doi:10.1016/j.brainres.2021.147576.
  • Chen J, Wang Z, Zheng Z, Chen Y, Khor S, Shi K, He Z, Wang Q, Zhao Y, Zhang H, Li X, Li J, Yin J, Wang X, Xiao J. Neuron and microglia/macrophage-derived FGF10 activate neuronal FGFR2/PI3K/Akt signaling and inhibit microglia/macrophages TLR4/NF-kappaB-dependent neuroinflammation to improve functional recovery after spinal cord injury. Cell Death Dis. 2017;8(10):e3090.doi:10.1038/cddis.2017.490.
  • Yin H, Shen L, Xuand C, Liu J. Lentivirus-Mediated overexpression of miR-29a promotes axonal regeneration and functional recovery in experimental spinal cord injury via PI3K/Akt/mTOR pathway. Neurochem Res. 2018;43(11):2038–2046.doi:10.1007/s11064-018-2625-5.
  • Li Y, Guo Y, Fan Y, Tian H, Liand K, Mei X. Melatonin enhances autophagy and reduces apoptosis to promote locomotor recovery in spinal cord injury via the PI3K/AKT/mTOR signaling pathway. Neurochem Res. 2019;44(8):2007–2019.doi:10.1007/s11064-019-02838-w.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.