Biomaterials Translational ›› 2023, Vol. 4 ›› Issue (3): 180-195.doi: 10.12336/biomatertransl.2023.03.006
• RESEARCH ARTICLE • Previous Articles
Rui Li1,2, Shuai Qiu3, Weihong Yang2,4, Zilong Rao1, Jiaxin Chen1, Yuexiong Yang4, Qingtang Zhu3,*(), Xiaolin Liu3, Ying Bai1,*(
), Daping Quan1,*(
)
Received:
2022-11-17
Revised:
2022-12-06
Accepted:
2023-03-08
Online:
2023-09-28
Published:
2023-09-28
Contact:
*Qingtang Zhu, Li, R.; Qiu, S.; Yang, W.; Rao, Z.; Chen, J.; Yang, Y.; Zhu, Q.; Liu, X.; Bai, Y.; Quan. D. A comparative study of human and porcine-derived decellularised nerve matrices. Biomater Transl. 2023, 4(3), 180-195.
Gene | Primer sequence | Product size (bp) |
---|---|---|
MAP–2 | Forward: 5'–CTT CAC GCA CAC CAG GCA CTC–3' | 102 |
Reverse: 5'–CCT TCT TCT CAC TCG GCA CCA AG–3' | ||
GAP43 | Forward: 5'–TCC ACT GAT AAC TCG CCG TCC TC–3' | 94 |
Reverse: 5'–CAG CAG CAG TGA CAG CAG CAG–3' | ||
MBP | Forward: 5'–CGA GGA CGG AGA TGA GGA GTA GTC–3' | 197 |
Reverse: 5'–CAG CTC AGC GAC GCA GAG TG–3' | ||
MPZ | Forward: 5'–TGG TGC TGT TGC TGC TGC TG–3' | 185 |
Reverse: 5'–GGT GCT TCT GCT GTG GTC CAG–3' | ||
GFAP | Forward: 5'–GCT GCG GCT CGA TCA ACT CAC–3' | 169 |
Reverse: 5'–GGT GGC TTC ATC TGC TTC CTG TC–3' | ||
S100β | Forward: 5'–ACA ATG ATG GAG ACG GCG AAT GTG–3' | 80 |
Reverse: 5'–GAA CTC GTG GCA GGC AGT AGT AAC–3' | ||
β–Actin | Forward: 5'–GCA AGT GCT TCT AGG CGG ACT G–3' | 195 |
Reverse: 5'–CTG CTG TCA CCT TCA CCG TTC C–3' |
Table 1. Primer sequences used for quantitative polymerase chain reaction
Gene | Primer sequence | Product size (bp) |
---|---|---|
MAP–2 | Forward: 5'–CTT CAC GCA CAC CAG GCA CTC–3' | 102 |
Reverse: 5'–CCT TCT TCT CAC TCG GCA CCA AG–3' | ||
GAP43 | Forward: 5'–TCC ACT GAT AAC TCG CCG TCC TC–3' | 94 |
Reverse: 5'–CAG CAG CAG TGA CAG CAG CAG–3' | ||
MBP | Forward: 5'–CGA GGA CGG AGA TGA GGA GTA GTC–3' | 197 |
Reverse: 5'–CAG CTC AGC GAC GCA GAG TG–3' | ||
MPZ | Forward: 5'–TGG TGC TGT TGC TGC TGC TG–3' | 185 |
Reverse: 5'–GGT GCT TCT GCT GTG GTC CAG–3' | ||
GFAP | Forward: 5'–GCT GCG GCT CGA TCA ACT CAC–3' | 169 |
Reverse: 5'–GGT GGC TTC ATC TGC TTC CTG TC–3' | ||
S100β | Forward: 5'–ACA ATG ATG GAG ACG GCG AAT GTG–3' | 80 |
Reverse: 5'–GAA CTC GTG GCA GGC AGT AGT AAC–3' | ||
β–Actin | Forward: 5'–GCA AGT GCT TCT AGG CGG ACT G–3' | 195 |
Reverse: 5'–CTG CTG TCA CCT TCA CCG TTC C–3' |
Figure 1. Structural and histological characterisations of the hDNM and pDNM scaffolds. Representative SEM micrographs of the hDNM (A) and pDNM (B) at lower magnification. Representative SEM micrographs of the hDNM (C) and pDNM (D) at higher magnification. Scale bars: 1 mm in A1, B1; 100 μm in A2, B2; 20 μm in A3, B3; 10 μm in A4, B4, C1, C2, D1, D2; and 1 μm in C3, D3. (E) Representative micrographs of hDNM and pDNM cross–sections after H&E staining. Scale bars: 500 μm. (F) DNA content quantified in the fresh tissues, hDNM, pDNM, hDNM–gel and pDNM–gel. Data are expressed as mean ± SD (n = 4). ***P < 0.001. H&E: haematoxylin–eosin; hDNM: human decellularised nerve matrix; n.s: not significant; pDNM: porcine decellularised nerve matrix; SEM: scanning electron microscopy.
Figure 2. Proteomic analysis of hDNM and pDNM. (A) Unsupervised hierarchical clustering between the hDNM and pDNM using Pearson’s correlation. (B) Volcano plot showing the differentially–expressed proteins between the hDNM and pDNM. (C) Heatmap and cluster dendrogram of protein abundances in the hDNM and pDNM. FC: fold change; hDNM: human decellularised nerve matrix; pDNM: porcine decellularised nerve matrix.
Classification | pDNM | hDNM | |
---|---|---|---|
Core matrisome | ECM glycoproteins | LAMB3, MXRA5, EDIL3, SLIT1, VWA3A, EMILIN3 | EMILIN2, CTGF, LAMA1, SRPX |
Collagens | None | COL6A6 | |
Proteoglycans | None | None | |
ECM–associated proteins | ECM–related proteins | ELFN2, FREM2, C1QL4, PLXNA2, PLXNA4, ANXA9 | GPC5, FCN1, PLXNA3 |
ECM regulators | ADAMTS14, TIMP3, CTSG, MMP12, MEP1A, ADAMTS7, ADAMTS5 | FAM20C, ADAMTS21, ADAMTS15, ADAMTSL3 | |
Secreted factors | WNT3A, BMP3, INHBA, MSTN, S100A4, NFSF15, FGF14, S100A13, ANGPTL7, HHIP, BRINP2, GDF3, FGF9 | MEGF11, IL4, GDF5, INHBB |
Table 2. Specific dECM proteins identified only in the pDNM or hDNM
Classification | pDNM | hDNM | |
---|---|---|---|
Core matrisome | ECM glycoproteins | LAMB3, MXRA5, EDIL3, SLIT1, VWA3A, EMILIN3 | EMILIN2, CTGF, LAMA1, SRPX |
Collagens | None | COL6A6 | |
Proteoglycans | None | None | |
ECM–associated proteins | ECM–related proteins | ELFN2, FREM2, C1QL4, PLXNA2, PLXNA4, ANXA9 | GPC5, FCN1, PLXNA3 |
ECM regulators | ADAMTS14, TIMP3, CTSG, MMP12, MEP1A, ADAMTS7, ADAMTS5 | FAM20C, ADAMTS21, ADAMTS15, ADAMTSL3 | |
Secreted factors | WNT3A, BMP3, INHBA, MSTN, S100A4, NFSF15, FGF14, S100A13, ANGPTL7, HHIP, BRINP2, GDF3, FGF9 | MEGF11, IL4, GDF5, INHBB |
Figure 3. Matrisome analysis of the proteomic composition in pDNM and hDNM. (A) Venn diagram showing the number of ECM proteins detected in hDNM and pDNM. (B, C) Percentages of the ECM proteins and their corresponding matrisome subcategories identified in pDNM (B) and hDNM (C). (D) Heatmap representing significant distinctions in the co–expressed ECM proteins between pDNM and hDNM. The relative abundance of the 35 shared proteins identified in pDNM was higher than that in hDNM. (E) Volcano plot of the differentially expressed ECM proteins in pDNM compared to hDNM. The red and blue dots indicate the significantly up– and down–regulated ECM proteins, respectively (n = 3 for both pDNM and hDNM). ECM: extracellular matrix, hDNM: human decellularised nerve matrix; pDNM: porcine decellularised nerve matrix.
Figure 4. Bioactivities of both hDNM–gel and pDNM–gel in regulating the behaviours of cultured HSCs. (A) Representative fluorescence micrographs of the cultured HSCs on hDNM–gel and pDNM–gel after 48 hours of incubation and live/dead staining, compared to the control (no hydrogel). Scale bars: 100 μm. (B) Representative fluorescence confocal micrographs of HSCs cultured for 48 hours and immunostained with EdU (green), S100 (red), and DAPI (blue). Scale bars: 100 μm. (C) Number of proliferating (EdU+/S100+) HSCs in B. (D) Wound healing characterisation showing the wound gaps at 0 and 24 hours in the control, hDNM–gel, and pDNM–gel groups. Scale bars: 100 μm. (E) HSC migration based on the wound healing experiments in D (n = 3). (F) MAP–2, GAP43, MBP, MPZ, GFAP, and S100β mRNA expression of the HSCs cultured on hDNM–gel and pDNM–gel were significantly upregulated compared to the control group (n = 5). β–actin was used as the reference. Data are shown as the mean ± SD. *P < 0.05, **P < 0.01, ***P < 0.001. DAPI: 6–diamidino–2–phenylindole–dihydrochloride; dECM: decellularised extracellular matrix; EdU: 5–ethynyl–2′–deoxyuridine; GAP43: growth–associated protein 43; GFAP: glial fibrillary acidic protein; hDNM–gel: human decellularised nerve matrix hydrogel; HSCs: human Schwann cells; MAP–2: microtubule–associated protein–2; MBP: myelin basic protein; MPZ: myelin protein zero; n.s, not significant; pDNM–gel: porcine decellularised nerve matrix hydrogel.
Figure 5. Detection of the immunogenic contents (α–Gal, MHC–1, and endotoxin) in hDNM and pDNM. (A, B) Western blot results and quantification of α–Gal antigen in hDNM, pDNM, and pDNM pre–treated with α–galactosidase (pDNM–enzymolysis). (C) Immunofluorescence staining and BF micrographs showing the presence of α–Gal antigen (green) within the hDNM, pDNM, and pDNM–enzymolysis samples. Scale bars: 100 μm. (D) Quantification of the immunoreactivity of α–Gal antigens. (E) Quantification of α–Gal content in raw porcine nerve tissues, pDNM, and pDNM after α–Gal treatment. (F) Western blot image and (G) quantification of the MHC–1 content in hDNM and pDNM. (H) Quantification of the endotoxin content in hDNM and pDNM. Data are presented as mean ± SD (n = 3). **P < 0.01, ***P < 0.001. α–Gal: α–galactosidase; BF: bright field; hDNM: human decellularised nerve matrix; MHC–1: major histocompatibility complex 1; n.s.: not significant; pDNM: porcine decellularised nerve matrix.
Figure 6. Host immune responses to subcutaneously injected hDNM, pDNM, and pDNM–enzymolysis in a humanised mouse model. Hu–mice received the same volume of sterile saline as the control. (A) H&E staining of the subcutaneous tissues sectioned from the Hu–mice in each group. Scale bars: 200 μm. (B) The total number of infiltrating cells in the dotted box in A based on H&E histological staining. (C) Flow cytometry results showing the human immune cells after treatment. (D, E) Quantitative analysis of the density of human leukocytes (hCD45+) (D) and the density of human B cells (hCD45+ hCD19+) (E) based on flow cytometric assessments. Data are presented as mean ± SD (n = 3). *P < 0.05, **P < 0.01, ***P < 0.001. H&E: haematoxylin–eosin; hDNM: human decellularised nerve matrix; n.s: not significant; pDNM: porcine decellularised nerve matrix.
Figure 7. Evaluation of T cell repopulation and their subtypes after injection of hDNM, pDNM, or pDNM–enzymolysis into humanised mice, analysed using flow cytometry. (A) T cells (hCD45+hCD3+) and their subtypes, including T helper cells (hCD3+hCD4+) and cytotoxic T cells (hCD3+hCD8+). (B) The density of total human T cells after introducing the dECMs into Hu–mice. (C) The percentage of the T helper cells (hCD3+hCD4+). (D) The percentage of cytotoxic T cells (hCD3+hCD8+). (E) The ratios of T helper cells/cytotoxic T cells. The data are expressed as mean ± SD (n = 3). *P < 0.05, **P < 0.01, ***P < 0.001. hDNM: human decellularised nerve matrix; n.s: not significant; pDNM: porcine decellularised nerve matrix.
Additional Figure 1. A flow chart of the in vivo study. DNM: decellularised nerve matrix; NPG: NOD–Prkdcscid Il2rgnull; PBMC: peripheral blood mononuclear cell.
Additional Figure 2. Scanning electron micrographs showing cross–sectional views of a native human nerve and a native porcine nerve. Scale bars: 1 mm.
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