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Click chemistry extracellular vesicle/peptide/chemokine nanocarriers for treating central nervous system injuries

Ruan, Huitong, Li, Yongfang, Wang, Cheng, Jiang, Yixu, Han, Yulong, Li, Yiwei, Zheng, Dandan, Ye, Jing, Chen, Gang, Yang, Guo-yuan, Deng, Lianfu, Guo, Ming, Zhang, Xingcai, Tang, Yaohui, Cui, Wenguo·2023·Acta Pharmaceutica Sinica B
DOI 10.1016/j.apsb.2022.06.007PMC PMC10213615
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Graphical abstract Graphical abstract Click chemistry extracellular vesicle/peptide/chemokine nanomissiles repair central nervous systems (CNS) injuries by targeting blood vessels, recruiting neural stem cells (NSCs) and inducing their differentiation into neurons.
Graphical abstract Graphical abstract Click chemistry extracellular vesicle/peptide/chemokine nanomissiles repair central nervous systems (CNS) injuries by targeting blood vessels, recruiting neural stem cells (NSCs) and inducing their differentiation into neurons.CC BY-NC-ND · PubMed Central
Figure 1 Schematic illustration of DA7R-SDF-1-EV nanomissile (Dual-EV) treatment on ischemic stroke. BV2 cells were treated with IL-4 to induce M2 polarization, then the M2 microglia-derived EVs (M2-EVs) were isolated for further modification. First, the DBCO group was modified on the surface of EVs and azide groups were introduced into DA7R peptide and the SDF-1 chemokine. Then the Dual-EVs nanomissile was engineered via copper-free click chemistry. After intravenous administration, the Dual-EV could target injured vascular endothelial cells in stroke lesions and accumulate in the lesion site via the VEGFR2-mediated effect. Then NSCs were recruited from the lateral ventricle to the ischemic region via the function of SDF-1. Finally, the Dual-EV induced the NSCs to differentiate into neurons to achieve neurogenesis after stroke.
Figure 1 Schematic illustration of DA7R-SDF-1-EV nanomissile (Dual-EV) treatment on ischemic stroke. BV2 cells were treated with IL-4 to induce M2 polarization, then the M2 microglia-derived EVs (M2-EVs) were isolated for further modification. First, the DBCO group was modified on the surface of EVs and azide groups were introduced into DA7R peptide and the SDF-1 chemokine. Then the Dual-EVs nanomissile was engineered via copper-free click chemistry. After intravenous administration, the Dual-EV could target injured vascular endothelial cells in stroke lesions and accumulate in the lesion site via the VEGFR2-mediated effect. Then NSCs were recruited from the lateral ventricle to the ischemic region via the function of SDF-1. Finally, the Dual-EV induced the NSCs to differentiate into neurons to achieve neurogenesis after stroke.CC BY-NC-ND · PubMed Central
Figure 2 Isolation, modification, and characterization of Dual-EV. (A) BV2 microglia were induced with 20 ng/mL IL-4 for 48 h or not, and then double immunostaining with IBA1 (microglial marker)/CD206 (M2 marker), or IBA1/ARG (M2 marker). Scale bar = 50 μm. (B) Western blotting assay to detect the expression of CD206 and ARG in BV2 cells induced with/without IL-4. (C) Schematic design of dual-modification of DA7R and SDF-1 on the surface of M2-EVs by copper-free click chemistry method. (D) Fluorescence images of Dual-EV. EVs were stained with Dil-red, DA7R was labeled with FITC and SDF-1 was marked with Cy5.5. Scale bar = 0.5 μm. Size distribution was detected by NTA and TEM images of unmodified EVs (E) and Dual-EV (F). Scale bar = 100 nm. (G) Western blot assay of EVs markers, TSG101 and CD63, from EVs and Dual-EV. The cell lysis was set as a negative control.
Figure 2 Isolation, modification, and characterization of Dual-EV. (A) BV2 microglia were induced with 20 ng/mL IL-4 for 48 h or not, and then double immunostaining with IBA1 (microglial marker)/CD206 (M2 marker), or IBA1/ARG (M2 marker). Scale bar = 50 μm. (B) Western blotting assay to detect the expression of CD206 and ARG in BV2 cells induced with/without IL-4. (C) Schematic design of dual-modification of DA7R and SDF-1 on the surface of M2-EVs by copper-free click chemistry method. (D) Fluorescence images of Dual-EV. EVs were stained with Dil-red, DA7R was labeled with FITC and SDF-1 was marked with Cy5.5. Scale bar = 0.5 μm. Size distribution was detected by NTA and TEM images of unmodified EVs (E) and Dual-EV (F). Scale bar = 100 nm. (G) Western blot assay of EVs markers, TSG101 and CD63, from EVs and Dual-EV. The cell lysis was set as a negative control.CC BY-NC-ND · PubMed Central
Figure 3 Effect of M2-EV on NSC differentiation. (A) Representative fluorescent images of NSCs treated with blank medium, M0-EV, M2-EV or Dual-M2-EV for 7 days. M2-EVs promote NSC to differentiate into Tuj 1+ neurons (B) and suppress GFAP+ astrocyte formation (C). Data are presented as mean ± SD, n = 3; ∗∗∗P < 0.001. Scale bar = 100 μm.
Figure 3 Effect of M2-EV on NSC differentiation. (A) Representative fluorescent images of NSCs treated with blank medium, M0-EV, M2-EV or Dual-M2-EV for 7 days. M2-EVs promote NSC to differentiate into Tuj 1+ neurons (B) and suppress GFAP+ astrocyte formation (C). Data are presented as mean ± SD, n = 3; ∗∗∗P < 0.001. Scale bar = 100 μm.CC BY-NC-ND · PubMed Central
Figure 4 Mechamisms of Dual-M2-EV on NSC neuronal differentiation. (A) The heatmap of differentially expressed miRNA in Dual-M2-EV compared with Dual-M0-EV. (B) The network of miRNA-mRNA. The gray circle represented the miRNA, and the green circle meant the target mRNA. (C) Quantitative analysis and representative images by flow cytometry of NSC-differentiated Tuj 1+ cells induced by selected miRNAs. Data are presented as mean ± SD, ∗P < 0.05, ∗∗P < 0.01, ∗∗∗P < 0.001, ns meant non-significance.
Figure 4 Mechamisms of Dual-M2-EV on NSC neuronal differentiation. (A) The heatmap of differentially expressed miRNA in Dual-M2-EV compared with Dual-M0-EV. (B) The network of miRNA-mRNA. The gray circle represented the miRNA, and the green circle meant the target mRNA. (C) Quantitative analysis and representative images by flow cytometry of NSC-differentiated Tuj 1+ cells induced by selected miRNAs. Data are presented as mean ± SD, ∗P < 0.05, ∗∗P < 0.01, ∗∗∗P < 0.001, ns meant non-significance.CC BY-NC-ND · PubMed Central
Figure 5 Internalization of different EVs by HUVECs and its recruitment effect on NSCs. (A) Representative confocal fluorescent images of HUVECs treated with 0.25 μmol/L EVs, DA7R-EV, or Dual-EV for 4 h. Scale bar = 10 μm. (B) Quantitative analysis using flow cytometry to quantify EVs internalized by HUVECs in the overlaid type. (C) Schematic illustration of NSC Transwell migration assay. (D) NSCs were seeded on the Transwell and were treated with blank medium, unmodified EVs, SDF-1-EV and Dual-EV for 48 h. The DAPI-stained NSCs represented these migrated on the lower side of Transwell membrane. Scale bar = 200 μm. (E) percentage of NSCs migration calculated by ImageJ software. Date are represented as mean ± SD for three random division. ∗∗∗P < 0.001. Scale bar = 200 μm.
Figure 5 Internalization of different EVs by HUVECs and its recruitment effect on NSCs. (A) Representative confocal fluorescent images of HUVECs treated with 0.25 μmol/L EVs, DA7R-EV, or Dual-EV for 4 h. Scale bar = 10 μm. (B) Quantitative analysis using flow cytometry to quantify EVs internalized by HUVECs in the overlaid type. (C) Schematic illustration of NSC Transwell migration assay. (D) NSCs were seeded on the Transwell and were treated with blank medium, unmodified EVs, SDF-1-EV and Dual-EV for 48 h. The DAPI-stained NSCs represented these migrated on the lower side of Transwell membrane. Scale bar = 200 μm. (E) percentage of NSCs migration calculated by ImageJ software. Date are represented as mean ± SD for three random division. ∗∗∗P < 0.001. Scale bar = 200 μm.CC BY-NC-ND · PubMed Central
Figure 6 Ischemic brain-targeting ability of Dual-EV in vivo. (A) a photo of a brain harvested from tMCAO mice illustrated the lesion region (left hemisphere: ipsilateral region, right hemisphere: contralateral region). (B) Representative ex vivo IVIS images of brains harvested from model mice which respectively received free EVs, DA7R-EV and Dual-EV labeled with Cy5.5 2 h after administration. (D) Semi-quantitative analysis of fluorescent intensity in the ischemic brain. (E) The ratio of fluorescent signals in the ipsilateral to the contralateral area. Representative images (C) and statistical analysis (F) of different Dil-red-labeled EVs (red) co-localized with CD31-positive vascular endothelial cells (green) in the ischemic region 2 h after administration. Data are presented as mean ± SD, n = 3, ∗P < 0.05, ∗∗∗P < 0.001. Scale bar = 25 μm.
Figure 6 Ischemic brain-targeting ability of Dual-EV in vivo. (A) a photo of a brain harvested from tMCAO mice illustrated the lesion region (left hemisphere: ipsilateral region, right hemisphere: contralateral region). (B) Representative ex vivo IVIS images of brains harvested from model mice which respectively received free EVs, DA7R-EV and Dual-EV labeled with Cy5.5 2 h after administration. (D) Semi-quantitative analysis of fluorescent intensity in the ischemic brain. (E) The ratio of fluorescent signals in the ipsilateral to the contralateral area. Representative images (C) and statistical analysis (F) of different Dil-red-labeled EVs (red) co-localized with CD31-positive vascular endothelial cells (green) in the ischemic region 2 h after administration. Data are presented as mean ± SD, n = 3, ∗P < 0.05, ∗∗∗P < 0.001. Scale bar = 25 μm.CC BY-NC-ND · PubMed Central
Figure 7 Treatment of Dual-EV decreased brain atrophy volumes and improved neurobiological recovery induced by an ischemic stroke. (A) Schematic illustration of ischemic stroke treatment. (B) Brain sections stained with cresyl violet treated with Sham, PBS, EV, DA7R-EV, or Dual-EV on Days 1, 3, 5 and 7 at a dosage of 20 μg EV/day after tMCAO. The dashed line indicated the infarct area, was first drafted along the outer edge of the contralateral hemisphere, then flipped vertically to the ischemic hemisphere. (C) Infarct volumes of brains in each group (n = 4–5). (D) Neuroscores evaluation on Days 1, 3, 7 and 14 post-reperfusion. (E) mNSS of model mice in Day 14, (F) Rotarod test (G) Hanging-wire test. n = 8, data are presented as mean ± SD, ∗P < 0.05, ∗∗P < 0.01, ∗∗∗P < 0.001.
Figure 7 Treatment of Dual-EV decreased brain atrophy volumes and improved neurobiological recovery induced by an ischemic stroke. (A) Schematic illustration of ischemic stroke treatment. (B) Brain sections stained with cresyl violet treated with Sham, PBS, EV, DA7R-EV, or Dual-EV on Days 1, 3, 5 and 7 at a dosage of 20 μg EV/day after tMCAO. The dashed line indicated the infarct area, was first drafted along the outer edge of the contralateral hemisphere, then flipped vertically to the ischemic hemisphere. (C) Infarct volumes of brains in each group (n = 4–5). (D) Neuroscores evaluation on Days 1, 3, 7 and 14 post-reperfusion. (E) mNSS of model mice in Day 14, (F) Rotarod test (G) Hanging-wire test. n = 8, data are presented as mean ± SD, ∗P < 0.05, ∗∗P < 0.01, ∗∗∗P < 0.001.CC BY-NC-ND · PubMed Central
Figure 8 Treatment of Dual-EV enhance neurogenesis in tMCAO mice. Representative fluorescent images of (A) NPCs (Nestin-positive cells, green); (B) Migrating immature neurons (DCX-positive cells, green) in groups treated with PBS, EVs, DA7R-EV or Dual-EV on Day 14 post-stroke in the SVZ (top) or striatum (bottom) region of ischemic mice brains. DAPI (blue): cell nuclei. Scale bar = 50 μm. (C) Relative integrated density (IntDen) of Nestin-positive cells in SVZ region. Data are presented as the ratio of average IntDen of PBS group. Quantitative analysis of DCX+ cells in the SVZ (D) and striatum (E) regions of the ipsilateral ventricle. (F) DCX cells migration distance. Data are presented as mean ± SD, n = 3; ∗P < 0.05, ∗∗P < 0.01, ∗∗∗P < 0.001.
Figure 8 Treatment of Dual-EV enhance neurogenesis in tMCAO mice. Representative fluorescent images of (A) NPCs (Nestin-positive cells, green); (B) Migrating immature neurons (DCX-positive cells, green) in groups treated with PBS, EVs, DA7R-EV or Dual-EV on Day 14 post-stroke in the SVZ (top) or striatum (bottom) region of ischemic mice brains. DAPI (blue): cell nuclei. Scale bar = 50 μm. (C) Relative integrated density (IntDen) of Nestin-positive cells in SVZ region. Data are presented as the ratio of average IntDen of PBS group. Quantitative analysis of DCX+ cells in the SVZ (D) and striatum (E) regions of the ipsilateral ventricle. (F) DCX cells migration distance. Data are presented as mean ± SD, n = 3; ∗P < 0.05, ∗∗P < 0.01, ∗∗∗P < 0.001.CC BY-NC-ND · PubMed Central

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Metadata

Authors
Ruan, H., Li, Y., Wang, C., Jiang, Y., Han, Y., Li, Y., Zheng, D., Ye, J., Chen, G., Yang, G.-Y., Deng, L., Guo, M., Zhang, X., Tang, Y., & Cui, W.
ORCID
Venue
Acta Pharmaceutica Sinica B
Publisher
Elsevier BV
Published
2023-05
Volume
13
Issue
5
Pages
2202-2218
ISSN
2211-3835
DOI
10.1016/j.apsb.2022.06.007
PMC
PMC10213615
Cited by
95
References
6
Language
en
Licence
Funders
  • National Key Research and Development Program of China (2019YFA0112000)
  • China Postdoctoral Science Foundation (2019M661546)
  • Shanghai Municipal Education Commission
  • Natural Science Foundation of Zhejiang Province (LQ21H300009)
  • Shanghai Jiao Tong University (ZH2018ZDA04)
  • National Postdoctoral Program for Innovative Talents (BX20200212)
  • National Natural Science Foundation of China (81801170, 81930051, 82003658)

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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

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