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Exosomal OTULIN from M2 macrophages promotes the recovery of spinal cord injuries via stimulating Wnt/β-catenin pathway-mediated vascular regeneration

Luo, Zixiang, Peng, Wei, Xu, Yan, Xie, Yong, Liu, Yudong, Lu, Hongbin, Cao, Yong, Hu, Jianzhong·2021·Acta Biomaterialia

Abstract

Vascularization following spinal cord injury (SCI) provides trophic support for rebuilding up and maintaining the homeostasis of neuronal networks, and the promotion of angiogenesis is beneficial for functional recovery after SCI. M2 macrophages have been reported to exhibit powerful pro-angiogenic functions during tissue repair. Exosomes are important paracrine mediators of their parent cells and play critical roles in tissue regeneration. However, the role of M2 macrophage-derived exosomes (M2-Exos) in SCI is still largely unknown. In the present study, we determined that M2-Exos could augment the angiogenic activities of spinal cord microvascular endothelial cells (SCMECs) in vitro. Hydrogel-mediated sustained release of M2-Exos significantly promoted vascular regeneration and functional recovery in mice after SCI. Furthermore, proteomics analysis showed that ubiquitin thioesterase otulin (OTULIN) protein was highly enriched in M2-Exos. Functional assays demonstrated that OTULIN protein was required for the M2-Exos-induced pro-angiogenic effects in SCMECs, as well as positive effects on vascular regeneration, cell proliferation, and functional recovery in the mouse model of SCI. Mechanically, OTULIN from M2-Exos could activate the Wnt/β-catenin signaling by increasing the protein level of β-catenin via inhibiting its ubiquitination and trigger the expression of angiogenesis-related genes that are reported to be the downstream targets of Wnt/β-catenin signaling. Inhibition…

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Research works printed but not linked: 53

  1. Ahuja, 2017, Traumatic spinal cord injury, Nat. Rev. Dis. Prim., 3, 17018, 10.1038/nrdp.2017.18 · DOI · Paper page
  2. Fan, 2018, Microenvironment imbalance of Spinal Cord Injury, Cell Transplant., 27, 853, 10.1177/0963689718755778 · DOI
  3. Segarra, 2018, Endothelial Dab1 signaling orchestrates neuro-glia-vessel communication in the central nervous system, Science, 361, 10.1126/science.aao2861 · DOI
  4. Rauch, 2009, Engineering angiogenesis following spinal cord injury: a coculture of neural progenitor and endothelial cells in a degradable polymer implant leads to an increase in vessel density and formation of the blood-spinal cord barrier, Eur. J. Neurosci., 29, 132, 10.1111/j.1460-9568.2008.06567.x · DOI
  5. Dray, 2009, Quantitative analysis by in vivo imaging of the dynamics of vascular and axonal networks in injured mouse spinal cord, Proc. Natl. Acad. Sci. U. S. A., 106, 9459, 10.1073/pnas.0900222106 · DOI
  6. Facchiano, 2002, Promotion of regeneration of corticospinal tract axons in rats with recombinant vascular endothelial growth factor alone and combined with adenovirus coding for this factor, J. Neurosurg., 97, 161, 10.3171/jns.2002.97.1.0161 · DOI
  7. Widenfalk, 2003, Vascular endothelial growth factor improves functional outcome and decreases secondary degeneration in experimental spinal cord contusion injury, Neuroscience, 120, 951, 10.1016/S0306-4522(03)00399-3 · DOI
  8. Tkach, 2016, Communication by extracellular vesicles: where we are and where we need to go, Cell, 164, 1226, 10.1016/j.cell.2016.01.043 · DOI · Paper page
  9. Ramachandran, 2012, Horizontal transfer of RNAs: exosomes as mediators of intercellular communication, Wiley Interdiscip. Rev. RNA, 3, 286, 10.1002/wrna.115 · DOI
  10. Fruhbeis, 2013, Neurotransmitter-triggered transfer of exosomes mediates oligodendrocyte-neuron communication, PLoS Biol., 11, 10.1371/journal.pbio.1001604 · DOI · Paper page
  11. Chen, 2012, Horizontal transfer of microRNAs: molecular mechanisms and clinical applications, Protein Cell, 3, 28, 10.1007/s13238-012-2003-z · DOI
  12. Kalani, 2014, Exosomes: mediators of neurodegeneration, neuroprotection and therapeutics, Mol. Neurobiol., 49, 590, 10.1007/s12035-013-8544-1 · DOI
  13. He, 2018, Exosome theranostics: biology and translational medicine, Theranostics, 8, 237, 10.7150/thno.21945 · DOI
  14. Chen, 2018, Exosomal DMBT1 from human urine-derived stem cells facilitates diabetic wound repair by promoting angiogenesis, Theranostics, 8, 1607, 10.7150/thno.22958 · DOI
  15. Hu, 2012, Microglia/macrophage polarization dynamics reveal novel mechanism of injury expansion after focal cerebral ischemia, Stroke, 43, 3063, 10.1161/STROKEAHA.112.659656 · DOI
  16. Zhang, 2017, The cystathionine beta-synthase/hydrogen sulfide pathway contributes to microglia-mediated neuroinflammation following cerebral ischemia, Brain. Behav. Immun., 66, 332, 10.1016/j.bbi.2017.07.156 · DOI
  17. David, 2011, Repertoire of microglial and macrophage responses after spinal cord injury, Nat. Rev. Neurosci., 12, 388, 10.1038/nrn3053 · DOI · Paper page
  18. Mosser, 2008, Exploring the full spectrum of macrophage activation, Nat. Rev. Immunol., 8, 958, 10.1038/nri2448 · DOI · Paper page
  19. Zajac, 2013, Angiogenic capacity of M1- and M2-polarized macrophages is determined by the levels of TIMP-1 complexed with their secreted proMMP-9, Blood, 122, 4054, 10.1182/blood-2013-05-501494 · DOI
  20. Welser, 2010, Microglial activation state exerts a biphasic influence on brain endothelial cell proliferation by regulating the balance of TNF and TGF-beta1, J. Neuroinflammation, 7, 89, 10.1186/1742-2094-7-89 · DOI
  21. Fu, 2020, The roles of tumor-associated macrophages in tumor angiogenesis and metastasis, Cell. Immunol., 353, 10.1016/j.cellimm.2020.104119 · DOI
  22. Ying, 2013, Investigation of macrophage polarization using bone marrow derived macrophages, J. Vis. Exp., 10.3791/50323-v · DOI
  23. Ruck, 2014, Isolation of primary murine brain microvascular endothelial cells, J. Vis. Exp., e52204
  24. Thery, 2006, Isolation and characterization of exosomes from cell culture supernatants and biological fluids, Curr. Protoc. Cell Biol. Chapter, 3, 22
  25. Basso, 2006, Basso Mouse Scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains, J. Neurotrauma, 23, 635, 10.1089/neu.2006.23.635 · DOI
  26. Schlag, 2001, Serial recording of sensory, corticomotor, and brainstem-derived motor evoked potentials in the rat, Somatosens Mot. Res., 18, 106, 10.1080/135578501012006219 · DOI
  27. Zhang, 2010, Wnt pathway antagonists and angiogenesis, Protein Cell, 1, 898, 10.1007/s13238-010-0112-0 · DOI
  28. Corada, 2010, The Wnt/beta-catenin pathway modulates vascular remodeling and specification by upregulating Dll4/Notch signaling, Dev. Cell, 18, 938, 10.1016/j.devcel.2010.05.006 · DOI
  29. Milich, 2019, The origin, fate, and contribution of macrophages to spinal cord injury pathology, Acta Neuropathol., 137, 785, 10.1007/s00401-019-01992-3 · DOI
  30. Barile, 2017, Exosomes: Therapy delivery tools and biomarkers of diseases, Pharmacol. Ther., 174, 63, 10.1016/j.pharmthera.2017.02.020 · DOI
  31. Lan, 2019, M2 macrophage-derived exosomes promote cell migration and invasion in colon cancer, Cancer Res., 79, 146, 10.1158/0008-5472.CAN-18-0014 · DOI · Paper page
  32. Dai, 2020, M2 macrophage-derived exosomes carry microRNA-148a to alleviate myocardial ischemia/reperfusion injury via inhibiting TXNIP and the TLR4/NF-kappaB/NLRP3 inflammasome signaling pathway, J. Mol. Cell. Cardiol., 142, 65, 10.1016/j.yjmcc.2020.02.007 · DOI
  33. Yang, 2020, M2 bone marrow-derived macrophage-derived exosomes shuffle microRNA-21 to accelerate immune escape of glioma by modulating PEG3, Cancer Cell Int., 20, 93, 10.1186/s12935-020-1163-9 · DOI
  34. Deng, 2021, M2 macrophage-derived exosomal miR-590-3p attenuates DSS-induced mucosal damage and promotes epithelial repair via the LATS1/YAP/beta-catenin signalling axis, J. Crohns. Colitis, 15, 665, 10.1093/ecco-jcc/jjaa214 · DOI
  35. Draijer, 2019, Distinctive effects of GM-CSF and M-CSF on proliferation and polarization of two major pulmonary macrophage populations, J. Immunol., 202, 2700, 10.4049/jimmunol.1801387 · DOI
  36. Martin, 2011, Chapter 6 - Immunohistology of non-hodgkin lymphoma, 156
  37. Zhou, 2020, Interleukin 37 suppresses M1 macrophage polarization through inhibition of the Notch1 and nuclear factor Kappa B pathways, Front. Cell Dev. Biol., 8, 56, 10.3389/fcell.2020.00056 · DOI
  38. Simeoli, 2017, Exosomal cargo including microRNA regulates sensory neuron to macrophage communication after nerve trauma, Nat. Commun., 8, 1778, 10.1038/s41467-017-01841-5 · DOI
  39. Douglas, 2019, Post-translational modification of OTULIN regulates ubiquitin dynamics and cell death, Cell Rep., 29, 10.1016/j.celrep.2019.11.014 · DOI
  40. Wang, 2020, ABL1-dependent OTULIN phosphorylation promotes genotoxic Wnt/beta-catenin activation to enhance drug resistance in breast cancers, Nat. Commun., 11, 3965, 10.1038/s41467-020-17770-9 · DOI
  41. Rivkin, 2013, The linear ubiquitin-specific deubiquitinase gumby regulates angiogenesis, Nature, 498, 318, 10.1038/nature12296 · DOI
  42. Goritz, 2011, A pericyte origin of spinal cord scar tissue, Science, 333, 238, 10.1126/science.1203165 · DOI · Paper page
  43. Dias, 2018, Fibrotic scarring following lesions to the central nervous system, Matrix Biol., 68-69, 561, 10.1016/j.matbio.2018.02.009 · DOI
  44. Guimaraes-Camboa, 2017, Pericytes of multiple organs do not behave as mesenchymal stem cells in vivo, Cell Stem Cell, 20, 10.1016/j.stem.2016.12.006 · DOI
  45. Xi, 2020, Microenvironment-responsive immunoregulatory electrospun fibers for promoting nerve function recovery, Nat. Commun., 11, 4504, 10.1038/s41467-020-18265-3 · DOI
  46. Hu, 2014, High-resolution three-dimensional visualization of the rat spinal cord microvasculature by synchrotron radiation micro-CT, Med. Phys., 41, 10.1118/1.4894704 · DOI
  47. Jiang, 2020, SRmuCT reveals 3D microstructural alterations of the vascular and neuronal network in a rat model of chronic compressive thoracic spinal cord injury, Aging Dis., 11, 603, 10.14336/AD.2019.0529 · DOI
  48. Hu, 2017, Nondestructive imaging of the internal microstructure of vessels and nerve fibers in rat spinal cord using phase-contrast synchrotron radiation microtomography, J. Synchrotron. Radiat., 24, 482, 10.1107/S1600577517000121 · DOI
  49. Cao, 2015, Three-dimensional imaging of microvasculature in the rat spinal cord following injury, Sci. Rep., 5, 12643, 10.1038/srep12643 · DOI
  50. Rolke, 2006, Quantitative sensory testing: a comprehensive protocol for clinical trials, Eur. J. Pain, 10, 77, 10.1016/j.ejpain.2005.02.003 · DOI
  51. Barrot, 2012, Tests and models of nociception and pain in rodents, Neuroscience, 211, 39, 10.1016/j.neuroscience.2011.12.041 · DOI
  52. Burke, 2017, Neuropathic pain prevalence following spinal cord injury: a systematic review and meta-analysis, Eur. J. Pain, 21, 29, 10.1002/ejp.905 · DOI · Paper page
  53. Widerstrom-Noga, 2017, Neuropathic pain and spinal cord injury: phenotypes and pharmacological management, Drugs, 77, 967, 10.1007/s40265-017-0747-8 · DOI

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Metadata

Authors
Luo, Z., Peng, W., Xu, Y., Xie, Y., Liu, Y., Lu, H., Cao, Y., & Hu, J.
Venue
Acta Biomaterialia
Publisher
Elsevier BV
Published
2021-12
Volume
136
Pages
519-532
ISSN
1742-7061
Cited by
96
References
4
Language
en
Funders
  • Science and Technology Bureau, Changsha (41965)
  • National Natural Science Foundation of China (82030071, 81874004, 81902224)
  • Fundamental Research Funds for Central Universities of the Central South University (2020zzts265)
  • Central South University
  • Natural Science Foundation of Hunan Province (2019JJ50959)
  • Xiangya Hospital, Central South University

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