A comparative study of human and porcine–derived decellularised nerve matrices

doi:10.12336/biomatertransl.2023.03.006

Biomaterials Translational ›› 2023, Vol. 4 ›› Issue (3): 180-195.doi: 10.12336/biomatertransl.2023.03.006

A comparative study of human and porcine–derived decellularised nerve matrices

Rui Li¹^,², Shuai Qiu³, Weihong Yang²^,⁴, Zilong Rao¹, Jiaxin Chen¹, Yuexiong Yang⁴, Qingtang Zhu³^,^*(), Xiaolin Liu³, Ying Bai¹^,^*(), Daping Quan¹^,^*()

1 Guangdong Engineering Technology Research Centre for Functional Biomaterials, School of Materials Science and Engineering, Sun Yat–sen University, Guangzhou, Guangdong Province, China
2 Key Laboratory for Polymeric Composite & Functional Materials of Ministry of Education, School of Chemistry, Sun Yat–sen University, Guangzhou, Guangdong Province, China
3 Guangdong Engineering Technology Research Centre for Peripheral Nerve Tissue, Department of Orthopaedic and Microsurgery, The First Affiliated Hospital of Sun Yat–sen University, Guangzhou, Guangdong Province, China
4 Guangzhou Zhongda Medical Equipment Co., Ltd., Guangzhou, Guangdong Province, China

Received:2022-11-17 Revised:2022-12-06 Accepted:2023-03-08 Online:2023-09-28 Published:2023-09-28
Contact: *Qingtang Zhu, Zhuqingt@mail.sysu.edu.cn; Ying Bai, baiy28@mail.sysu.edu.cn; Daping Quan, cesqdp@mail.sysu.edu.cn.

Abstract

Abstract:

Decellularised extracellular matrix (dECM) biomaterials originating from allogeneic and xenogeneic tissues have been broadly studied in the field of regenerative medicine and have already been used in clinical treatments. Allogeneic dECMs are considered more compatible, but they have the drawback of extremely limited human tissue sources. Their availability is also restricted by the health and age of the donors. To investigate the viability of xenogeneic tissues as a substitute for human tissues, we fabricated both porcine decellularised nerve matrix (pDNM) and human decellularised nerve matrix for a comprehensive comparison. Photomicrographs showed that both dECM scaffolds retained the ECM microstructures of native human nerve tissues. Proteomic analysis demonstrated that the protein compositions of both dECMs were also very similar to each other. Their functional ECM contents effectively promoted the proliferation, migration, and maturation of primary human Schwann cells in vitro. However, pDNM contained a few antigens that induced severe host immune responses in humanised mice. Interestingly, after removing the α–galactosidase antigen, the immune responses were highly alleviated and the pre–treated pDNM maintained a human decellularised nerve matrix–like pro–regenerative phenotype. Therefore, we believe that an α–galactosidase–free pDNM may serve as a viable substitute for human decellularised nerve matrix in future clinical applications.

Key words: allogeneic, decellularised nerve matrix, immune response, xenogeneic, α–Gal

Cite this article

Figures/Tables 11

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.

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.

References 53

1.	Krishtul, S.; Baruch, L.; Machluf, M. Processed tissue-derived extracellular matrices: tailored platforms empowering diverse therapeutic applications. Adv Funct Mater. 2020, 30, 1900386.
2.	Garreta, E.; Oria, R.; Tarantino, C.; Pla-Roca, M.; Prado, P.; Fernández-Avilés, F.; Campistol, J. M.; Samitier, J.; Montserrat, N. Tissue engineering by decellularization and 3D bioprinting. Mater Today. 2017, 20, 166-178. doi: 10.1016/j.mattod.2016.12.005 URL
3.	Hussey, G. S.; Dziki, J. L.; Badylak, S. F. Extracellular matrix-based materials for regenerative medicine. Nat Rev Mater. 2018, 3, 159-173. doi: 10.1038/s41578-018-0023-x
4.	Li, T.; Javed, R.; Ao, Q. Xenogeneic decellularized extracellular matrix-based biomaterials for peripheral nerve repair and regeneration. Curr Neuropharmacol. 2021, 19, 2152-2163. doi: 10.2174/1570159X18666201111103815 URL
5.	Zouhair, S.; Sasso, E. D.; Tuladhar, S. R.; Fidalgo, C.; Vedovelli, L.; Filippi, A.; Borile, G.; Bagno, A.; Marchesan, M.; Giorgio, R.; Gregori, D.; Wolkers, W. F.; Romanato, F.; Korossis, S.; Gerosa, G.; Iop, L. A comprehensive comparison of bovine and porcine decellularized pericardia: new insights for surgical applications. Biomolecules. 2020, 10, 371. doi: 10.3390/biom10030371 URL
6.	Capella-Monsonís, H.; De Pieri, A.; Peixoto, R.; Korntner, S.; Zeugolis, D. I. Extracellular matrix-based biomaterials as adipose-derived stem cell delivery vehicles in wound healing: a comparative study between a collagen scaffold and two xenografts. Stem Cell Res Ther. 2020, 11, 510. doi: 10.1186/s13287-020-02021-x
7.	Bowers, S. L.; Banerjee, I.; Baudino, T. A. The extracellular matrix: at the center of it all. J Mol Cell Cardiol. 2010, 48, 474-482. doi: 10.1016/j.yjmcc.2009.08.024 URL
8.	Keane, T. J.; Londono, R.; Turner, N. J.; Badylak, S. F. Consequences of ineffective decellularization of biologic scaffolds on the host response. Biomaterials. 2012, 33, 1771-1781. doi: 10.1016/j.biomaterials.2011.10.054 URL
9.	Badylak, S. F. Xenogeneic extracellular matrix as a scaffold for tissue reconstruction. Transpl Immunol. 2004, 12, 367-377. doi: 10.1016/j.trim.2003.12.016 URL
10.	Badylak, S. F.; Gilbert, T. W. Immune response to biologic scaffold materials. Semin Immunol. 2008, 20, 109-116. doi: 10.1016/j.smim.2007.11.003 URL
11.	Kasper, M.; Deister, C.; Beck, F.; Schmidt, C. E. Bench-to-bedside lessons learned: commercialization of an acellular nerve graft. Adv Healthc Mater. 2020, 9, e2000174.
12.	Yang, L. M.; Liu, X. L.; Zhu, Q. T.; Zhang, Y.; Xi, T. F.; Hu, J.; He, C. F.; Jiang, L. Human peripheral nerve-derived scaffold for tissue-engineered nerve grafts: histology and biocompatibility analysis. J Biomed Mater Res B Appl Biomater. 2011, 96, 25-33.
13.	Colwell, A. S.; Longaker, M. T.; Lorenz, H. P. Mammalian fetal organ regeneration. Adv Biochem Eng Biotechnol. 2005, 93, 83-100.
14.	Sicari, B. M.; Johnson, S. A.; Siu, B. F.; Crapo, P. M.; Daly, K. A.; Jiang, H.; Medberry, C. J.; Tottey, S.; Turner, N. J.; Badylak, S. F. The effect of source animal age upon the in vivo remodeling characteristics of an extracellular matrix scaffold. Biomaterials. 2012, 33, 5524-5533. doi: 10.1016/j.biomaterials.2012.04.017 URL
15.	Badylak, S. F. The extracellular matrix as a biologic scaffold material. Biomaterials. 2007, 28, 3587-3593. doi: 10.1016/j.biomaterials.2007.04.043 URL
16.	Seif-Naraghi, S. B.; Singelyn, J. M.; Salvatore, M. A.; Osborn, K. G.; Wang, J. J.; Sampat, U.; Kwan, O. L.; Strachan, G. M.; Wong, J.; Schup-Magoffin, P. J.; Braden, R. L.; Bartels, K.; DeQuach, J. A.; Preul, M.; Kinsey, A. M.; DeMaria, A. N.; Dib, N.; Christman, K. L. Safety and efficacy of an injectable extracellular matrix hydrogel for treating myocardial infarction. Sci Transl Med. 2013, 5, 173ra125.
17.	Chen, S.; Du, Z.; Zou, J.; Qiu, S.; Rao, Z.; Liu, S.; Sun, X.; Xu, Y.; Zhu, Q.; Liu, X.; Mao, H. Q.; Bai, Y.; Quan, D. Promoting neurite growth and schwann cell migration by the harnessing decellularized nerve matrix onto nanofibrous guidance. ACS Appl Mater Interfaces. 2019, 11, 17167-17176. doi: 10.1021/acsami.9b01066 URL
18.	Zheng, C.; Yang, Z.; Chen, S.; Zhang, F.; Rao, Z.; Zhao, C.; Quan, D.; Bai, Y.; Shen, J. Nanofibrous nerve guidance conduits decorated with decellularized matrix hydrogel facilitate peripheral nerve injury repair. Theranostics. 2021, 11, 2917-2931. doi: 10.7150/thno.50825 URL
19.	Deng, R.; Luo, Z.; Rao, Z.; Lin, Z.; Chen, S.; Zhou, J.; Zhu, Q.; Liu, X.; Bai, Y.; Quan, D. Decellularized extracellular matrix containing electrospun fibers for nerve regeneration: a comparison between core-shell structured and preblended composites. Adv Fiber Mater. 2022, 4, 503-519. doi: 10.1007/s42765-021-00124-5
20.	Xu, Y.; Zhou, J.; Liu, C.; Zhang, S.; Gao, F.; Guo, W.; Sun, X.; Zhang, C.; Li, H.; Rao, Z.; Qiu, S.; Zhu, Q.; Liu, X.; Guo, X.; Shao, Z.; Bai, Y.; Zhang, X.; Quan, D. Understanding the role of tissue-specific decellularized spinal cord matrix hydrogel for neural stem/progenitor cell microenvironment reconstruction and spinal cord injury. Biomaterials. 2021, 268, 120596. doi: 10.1016/j.biomaterials.2020.120596 URL
21.	Lin, T.; Liu, S.; Chen, S.; Qiu, S.; Rao, Z.; Liu, J.; Zhu, S.; Yan, L.; Mao, H.; Zhu, Q.; Quan, D.; Liu, X. Hydrogel derived from porcine decellularized nerve tissue as a promising biomaterial for repairing peripheral nerve defects. Acta Biomater. 2018, 73, 326-338. doi: 10.1016/j.actbio.2018.04.001 URL
22.	Rao, Z.; Lin, T.; Qiu, S.; Zhou, J.; Liu, S.; Chen, S.; Wang, T.; Liu, X.; Zhu, Q.; Bai, Y.; Quan, D. Decellularized nerve matrix hydrogel scaffolds with longitudinally oriented and size-tunable microchannels for peripheral nerve regeneration. Mater Sci Eng C Mater Biol Appl. 2021, 120, 111791. doi: 10.1016/j.msec.2020.111791 URL
23.	Keane, T. J.; Badylak, S. F. The host response to allogeneic and xenogeneic biological scaffold materials. J Tissue Eng Regen Med. 2015, 9, 504-511. doi: 10.1002/term.1874 URL
24.	Brown, B. N.; Londono, R.; Tottey, S.; Zhang, L.; Kukla, K. A.; Wolf, M. T.; Daly, K. A.; Reing, J. E.; Badylak, S. F. Macrophage phenotype as a predictor of constructive remodeling following the implantation of biologically derived surgical mesh materials. Acta Biomater. 2012, 8, 978-987. doi: 10.1016/j.actbio.2011.11.031 URL
25.	Brown, B. N.; Valentin, J. E.; Stewart-Akers, A. M.; McCabe, G. P.; Badylak, S. F. Macrophage phenotype and remodeling outcomes in response to biologic scaffolds with and without a cellular component. Biomaterials. 2009, 30, 1482-1491. doi: 10.1016/j.biomaterials.2008.11.040 URL
26.	Galili, U. Interaction of the natural anti-Gal antibody with alpha-galactosyl epitopes: a major obstacle for xenotransplantation in humans. Immunol Today. 1993, 14, 480-482. doi: 10.1016/0167-5699(93)90261-I URL
27.	Mestas, J.; Hughes, C. C. Of mice and not men: differences between mouse and human immunology. J Immunol. 2004, 172, 2731-2738. doi: 10.4049/jimmunol.172.5.2731 URL
28.	Qiu, S.; Rao, Z.; He, F.; Wang, T.; Xu, Y.; Du, Z.; Yao, Z.; Lin, T.; Yan, L.; Quan, D.; Zhu, Q.; Liu, X. Decellularized nerve matrix hydrogel and glial-derived neurotrophic factor modifications assisted nerve repair with decellularized nerve matrix scaffolds. J Tissue Eng Regen Med. 2020, 14, 931-943. doi: 10.1002/term.v14.7 URL
29.	Devaud, Y. R.; Avilla-Royo, E.; Trachsel, C.; Grossmann, J.; Martin, I.; Lutolf, M. P.; Ehrbar, M. Label-free quantification proteomics for the identification of mesenchymal stromal cell matrisome inside 3D poly(ethylene glycol) hydrogels. Adv Healthc Mater. 2018, 7, e1800534.
30.	UniProt, Consortium. UniProt: the universal protein knowledgebase in 2021. Nucleic Acids Res. 2021, 49, D480-D489. doi: 10.1093/nar/gkaa1100 URL
31.	Morfeld, P. Controlling the false discovery rate in many SMR analyses. J Occup Environ Med. 2016, 58, e21-22. doi: 10.1097/JOM.0000000000000599 URL
32.	Naba, A.; Clauser, K. R.; Ding, H.; Whittaker, C. A.; Carr, S. A.; Hynes, R. O. The extracellular matrix: Tools and insights for the “omics” era. Matrix Biol. 2016, 49, 10-24. doi: 10.1016/j.matbio.2015.06.003 URL
33.	Schneider, C. A.; Rasband, W. S.; Eliceiri, K. W. NIH image to ImageJ: 25 years of image analysis. Nat Methods. 2012, 9, 671-675.
34.	Bubner, B.; Baldwin, I. T. Use of real-time PCR for determining copy number and zygosity in transgenic plants. Plant Cell Rep. 2004, 23, 263-271. doi: 10.1007/s00299-004-0859-y URL
35.	Stone, K. R.; Ayala, G.; Goldstein, J.; Hurst, R.; Walgenbach, A.; Galili, U. Porcine cartilage transplants in the cynomolgus monkey. III. Transplantation of alpha-galactosidase-treated porcine cartilage. Transplantation. 1998, 65, 1577-1583. doi: 10.1097/00007890-199806270-00007 URL
36.	Percie du Sert, N.; Hurst, V.; Ahluwalia, A.; Alam, S.; Avey, M. T.; Baker, M.; Browne, W. J.; Clark, A.; Cuthill, I. C.; Dirnagl, U.; Emerson, M.; Garner, P.; Holgate, S. T.; Howells, D. W.; Karp, N. A.; Lazic, S. E.; Lidster, K.; MacCallum, C. J.; Macleod, M.; Pearl, E. J.; Petersen, O. H.; Rawle, F.; Reynolds, P.; Rooney, K.; Sena, E. S.; Silberberg, S. D.; Steckler, T.; Würbel, H. The ARRIVE guidelines 2.0: Updated guidelines for reporting animal research. PLoS Biol. 2020, 18, e3000410. doi: 10.1371/journal.pbio.3000410 URL
37.	Lan, P.; Tonomura, N.; Shimizu, A.; Wang, S.; Yang, Y. G. Reconstitution of a functional human immune system in immunodeficient mice through combined human fetal thymus/liver and CD34⁺ cell transplantation. Blood. 2006, 108, 487-492.
38.	Khan, S.; Kaihara, K. A. Single-cell RNA-sequencing of peripheral blood mononuclear cells with ddSEQ. Methods Mol Biol. 2019, 1979, 155-176.
39.	Wang, R. M.; Johnson, T. D.; He, J.; Rong, Z.; Wong, M.; Nigam, V.; Behfar, A.; Xu, Y.; Christman, K. L. Humanized mouse model for assessing the human immune response to xenogeneic and allogeneic decellularized biomaterials. Biomaterials. 2017, 129, 98-110. doi: 10.1016/j.biomaterials.2017.03.016 URL
40.	Crapo, P. M.; Medberry, C. J.; Reing, J. E.; Tottey, S.; van der Merwe, Y.; Jones, K. E.; Badylak, S. F. Biologic scaffolds composed of central nervous system extracellular matrix. Biomaterials. 2012, 33, 3539-3547. doi: 10.1016/j.biomaterials.2012.01.044 URL
41.	Behan, B. L.; DeWitt, D. G.; Bogdanowicz, D. R.; Koppes, A. N.; Bale, S. S.; Thompson, D. M. Single-walled carbon nanotubes alter Schwann cell behavior differentially within 2D and 3D environments. J Biomed Mater Res A. 2011, 96, 46-57.
42.	Aamodt, J. M.; Grainger, D. W. Extracellular matrix-based biomaterial scaffolds and the host response. Biomaterials. 2016, 86, 68-82. doi: 10.1016/j.biomaterials.2016.02.003 URL
43.	Walsh, N. C.; Kenney, L. L.; Jangalwe, S.; Aryee, K. E.; Greiner, D. L.; Brehm, M. A.; Shultz, L. D. Humanized mouse models of clinical disease. Annu Rev Pathol. 2017, 12, 187-215. doi: 10.1146/pathmechdis.2017.12.issue-1 URL
44.	Kočí, Z.; Výborný, K.; Dubišová, J.; Vacková, I.; Jäger, A.; Lunov, O.; Jiráková, K.; Kubinová, Š. Extracellular matrix hydrogel derived from human umbilical cord as a scaffold for neural tissue repair and its comparison with extracellular matrix from porcine tissues. Tissue Eng Part C Methods. 2017, 23, 333-345. doi: 10.1089/ten.tec.2017.0089 URL
45.	Tan, Q. W.; Zhang, Y.; Luo, J. C.; Zhang, D.; Xiong, B. J.; Yang, J. Q.; Xie, H. Q.; Lv, Q. Hydrogel derived from decellularized porcine adipose tissue as a promising biomaterial for soft tissue augmentation. J Biomed Mater Res A. 2017, 105, 1756-1764. doi: 10.1002/jbm.a.v105.6 URL
46.	Bikhet, M.; Morsi, M.; Hara, H.; Rhodes, L. A.; Carlo, W. F.; Cleveland, D.; Cooper, D. K. C.; Iwase, H. The immune system in infants: Relevance to xenotransplantation. Pediatr Transplant. 2020, 24, e13795. doi: 10.1111/petr.v24.7 URL
47.	Yan, L.; Guo, Y.; Qi, J.; Zhu, Q.; Gu, L.; Zheng, C.; Lin, T.; Lu, Y.; Zeng, Z.; Yu, S.; Zhu, S.; Zhou, X.; Zhang, X.; Du, Y.; Yao, Z.; Lu, Y.; Liu, X. Iodine and freeze-drying enhanced high-resolution MicroCT imaging for reconstructing 3D intraneural topography of human peripheral nerve fascicles. J Neurosci Methods. 2017, 287, 58-67. doi: 10.1016/j.jneumeth.2017.06.009 URL
48.	Spang, M. T.; Christman, K. L. Extracellular matrix hydrogel therapies: in vivo applications and development. Acta Biomater. 2018, 68, 1-14. doi: 10.1016/j.actbio.2017.12.019 URL
49.	Bi, H.; Ye, K.; Jin, S. Proteomic analysis of decellularized pancreatic matrix identifies collagen V as a critical regulator for islet organogenesis from human pluripotent stem cells. Biomaterials. 2020, 233, 119673. doi: 10.1016/j.biomaterials.2019.119673 URL
50.	Choudhury, D.; Yee, M.; Sheng, Z. L. J.; Amirul, A.; Naing, M. W. Decellularization systems and devices: State-of-the-art. Acta Biomater. 2020, 115, 51-59. doi: 10.1016/j.actbio.2020.07.060 URL
51.	Xing, H.; Lee, H.; Luo, L.; Kyriakides, T. R. Extracellular matrix-derived biomaterials in engineering cell function. Biotechnol Adv. 2020, 42, 107421. doi: 10.1016/j.biotechadv.2019.107421 URL
52.	Yue, Y.; Xu, W.; Kan, Y.; Zhao, H. Y.; Zhou, Y.; Song, X.; Wu, J.; Xiong, J.; Goswami, D.; Yang, M.; Lamriben, L.; Xu, M.; Zhang, Q.; Luo, Y.; Guo, J.; Mao, S.; Jiao, D.; Nguyen, T. D.; Li, Z.; Layer, J. V.; Li, M.; Paragas, V.; Youd, M. E.; Sun, Z.; Ding, Y.; Wang, W.; Dou, H.; Song, L.; Wang, X.; Le, L.; Fang, X.; George, H.; Anand, R.; Wang, S. Y.; Westlin, W. F.; Güell, M.; Markmann, J.; Qin, W.; Gao, Y.; Wei, H. J.; Church, G. M.; Yang, L. Extensive germline genome engineering in pigs. Nat Biomed Eng. 2021, 5, 134-143. doi: 10.1038/s41551-020-00613-9
53.	Niu, D.; Wei, H. J.; Lin, L.; George, H.; Wang, T.; Lee, I. H.; Zhao, H. Y.; Wang, Y.; Kan, Y.; Shrock, E.; Lesha, E.; Wang, G.; Luo, Y.; Qing, Y.; Jiao, D.; Zhao, H.; Zhou, X.; Wang, S.; Wei, H.; Güell, M.; Church, G. M.; Yang, L. Inactivation of porcine endogenous retrovirus in pigs using CRISPR-Cas9. Science. 2017, 357, 1303-1307. doi: 10.1126/science.aan4187 URL

A comparative study of human and porcine–derived decellularised nerve matrices

RichHTML

PDF

Knowledge

share this article

Abstract

Cite this article

Figures/Tables 11

References 53

Related Articles 0

Recommended Articles

Metrics

Comments

Journal Info

For Authors

For Reviewers

Archives