Intra‑cerebral implantation of a variety of collagenous scaffolds with nervous embryonic cells

Drobnik,Jacek; Pietrucha,Krystyna; Janczar,Karolina; Polis,Lech; Polis,Bartosz; Safandowska,Marta; Szymański,Jacek

doi:10.3892/etm.2019.8116

Intra‑cerebral implantation of a variety of collagenous scaffolds with nervous embryonic cells

Authors:
- Jacek Drobnik
- Krystyna Pietrucha
- Karolina Janczar
- Lech Polis
- Bartosz Polis
- Marta Safandowska
- Jacek Szymański
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Affiliations: Laboratory of Connective Tissue Metabolism, Department of Pathophysiology, Medical University of Lodz, 90‑136 Lodz, Poland, Department of Material and Commodity Sciences and Textile Metrology, Lodz University of Technology, 90‑924 Lodz, Poland, Department of Pathomorphology, Medical University of Lodz, 92‑213 Lodz, Poland, Department of Neurosurgery, Polish Mothers' Memorial Hospital‑Research Institute, 93‑338 Lodz, Poland, Central Scientific Laboratory, Medical University of Lodz, 92‑215 Lodz, Poland
Published online on: October 21, 2019 https://doi.org/10.3892/etm.2019.8116
Pages: 4758-4764
Copyright: © Drobnik et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Collagenous scaffolds provide good conditions for embryonic nerve cell growth. The aim of the current study was to assess the brains reaction to the implantation of 3D sponge‑shaped scaffolds. These scaffolds consisted of collagen (Col) and Col with chondroitin sulphate, which is modified by carbodiimide, or Col crosslinked with dialdehyde cellulose. The current study also evaluated the expression of integrins α2 and β1 in embryonic nerve cells. Embryonic nerve cells were isolated from the brains of rat embryos. Acellular scaffolds, or scaffolds populated with embryonic nerve cells, were implanted into the rats brain. The fibers of all the implanted scaffolds remained intact and served as a template for cell infiltration. The implants induced minimal to moderate inflammatory responses and minimal glial scar formations. Immunohistochemical studies did not indicate any microtubule‑associated protein 2 or glial fibrillary acidic protein‑positive cells inside the scaffolds. Acellular and cell‑populated scaffolds yielded similar responses in the brain. The expression of integrin α2 and β1 was observed in embryonic nervous cells. TC‑I15, the integrin α2β1 inhibitor, was not demonstrated to modify cell entrapment within the collagenous scaffolds. All applied scaffolds were well tolerated by the tissue and were indicated to support blood vessel formation. Therefore, all tested biomaterials are recommended for further studies. Additional chemical modifications of the material are suggested to protect the seeded cells from apoptosis after implantation into the brain.

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1	Chwalek K, Tang-Schomer MD, Omenetto FG and Kaplan DL: In vitro bioengineered model of cortical brain tissue. Nat Protoc. 10:1362–1373. 2015. View Article : Google Scholar : PubMed/NCBI
2	Huang KF, Hsu WC, Chiu WT and Wang JY: Functional improvement and neurogenesis after collagen-GAG matrix implantation into surgical brain trauma. Biomaterials. 33:2067–2075. 2012. View Article : Google Scholar : PubMed/NCBI
3	Teng YD, Lavik EB, Qu X, Park KI, Ourednik J, Zurakowski D, Langer R and Snyder EY: Functional recovery following traumatic spinal cord injury mediated by unique polymer scaffold seeded with neural stem cells. Proc Natl Acad Sci USA. 99:3024–3029. 2002. View Article : Google Scholar : PubMed/NCBI
4	Kowalska-Ludwicka K, Cala J, Grobelski B, Sygut D, Jesionek-Kupnicka D, Kolodziejczyk M, Bielecki S and Pasieka Z: Modified bacterial cellulose tubes for regeneration of damaged peripheral nerves. Arch Med Sci. 9:527–534. 2013. View Article : Google Scholar : PubMed/NCBI
5	Huang KF, Hsu WC, Hsiao JK, Chen GS and Wang JY: Collagen-Glycosaminoglycan Matrix implantation promotes angiogenesis following surgical brain trauma. BioMed Res Int. 2014:6724092014. View Article : Google Scholar : PubMed/NCBI
6	Bandtlow CE and Zimmerman DR: Proteoglycans in the developing brain: New conceptual insights for old proteins. Physiol Rev. 80:1267–1290. 2000. View Article : Google Scholar : PubMed/NCBI
7	Drobnik J, Pietrucha K, Piera L, Szymański J and Szczepanowska A: Collagenous scaffolds supplemented with hyaluronic acid and chondroitin sulfate used for wound fibroblast and embryonic nerve cell culture. Adv Clin Exp Med. 26:223–230. 2017. View Article : Google Scholar : PubMed/NCBI
8	Pietrucha K, Szymański J and Drobnik J: The behavior of embryonic neural cells within the 3D micro-structured collagen-based scaffolds. IFMBE Proceedings. 45:549–552. 2015. View Article : Google Scholar
9	Sirko S, von Holst A, Wizenmann A, Gotz M and Faissner A: Chondroitin sulphate glycosaminoglycans control proliferation, radial glia cell differentiation and neurogenesis in neural stem/progenitor cells. Development. 134:2727–2738. 2007. View Article : Google Scholar : PubMed/NCBI
10	Li YY, Choy TH, Ho FC and Chan PB: Scaffold composition affects cytoskeleton organization cell-matrix interaction and the cellular fate of human mesenchymal stem cells upon chondrogenic differentiation. Biomaterials. 52:208–220. 2015. View Article : Google Scholar : PubMed/NCBI
11	Milner R and Campbel IL: The integrin family of cell adhesion molecules has multiple functions within CNS. J Neurosci Res. 69:286–291. 2002. View Article : Google Scholar : PubMed/NCBI
12	Pietrucha K, Zychowicz M, Podobinska M and Buzanska L: Functional properties of different collagen scaffolds to create a biomimetic niche for neurally committed human induced pluripotent stem cells (iPSC). Folia Neuropathol. 55:110–123. 2017. View Article : Google Scholar : PubMed/NCBI
13	Pietrucha K: Physicochemical properties of 3D collagen-CS scaffolds for potential use in neural tissue engineering. Int J Biol Macromol. 80:732–739. 2015. View Article : Google Scholar : PubMed/NCBI
14	Pietrucha K: Development of collagen cross-linked with dialdehyde cellulose as a potential 3D scaffold for neural tissue engineering. IFMBE Proceeding. 45:349–352. 2015. View Article : Google Scholar
15	Pietrucha K and Safandowska M: Dialdehyde cellulose-crosslinked collagen and its physicochemical properties. Process Biochem. 50:2105–2111. 2015. View Article : Google Scholar
16	Pietrucha K, Marzec E and Kudzin M: Pore structure and dielectric behaviour of the 3D collagen-DAC scaffolds designed for nerve tissue repair. Int J Biol Macromol. 92:1298–1306. 2016. View Article : Google Scholar : PubMed/NCBI
17	Rauch U: Extracellular matrix components associated with remodeling process in brain. Cell Mol Life Sci. 61:2031–2045. 2004. View Article : Google Scholar : PubMed/NCBI
18	Jurga M, Dainiak MB, Sarnowska A, Jablonska A, Thripathi A, Plieva FM, Savina IN, Strojek L, Jungvid H, Kumar A, et al: The performance of laminin-containing cryogel scaffolds in neural tissue regeneration. Biomaterials. 32:3423–3434. 2011. View Article : Google Scholar : PubMed/NCBI
19	Vaysse L, Beduer A, Sol JC, Vieu C and Loubinoux I: Micropatterned bioimplant with guided neuronal cells to promote tissue reconstruction and improve functional recovery after primary motor cortex insult. Biomaterials. 58:46–53. 2015. View Article : Google Scholar : PubMed/NCBI
20	Ju R, Wen Y, Gou R, Wang Y and Xu Q: The experimental therapy on brain ischemia by improvement of local angiogenesis with tissue engineering in the mouse. Cell Transplant. 23 (Suppl 1):S83–S95. 2014. View Article : Google Scholar : PubMed/NCBI
21	Yu S, Yao S, Wen Y, Wang Y, Wang H and Xu Q: Angiogenic microspheres promote neural regeneration and motor function recovery after spinal cord injury in rats. Sci Rep. 6:334282016. View Article : Google Scholar : PubMed/NCBI
22	Tapon-Bretaudière J, Drouet B, Matou S, Mourão PA, Bros A, Letourner D and Fischer AM: Modulation of vascular human endothelial rat smooth muscle cell growth by a fucosylated chondroitin sulphate from echinoderm. Thromb Haemost. 84:332–337. 2000. View Article : Google Scholar : PubMed/NCBI
23	Deguchi K, Tsuru K, Hayashi T, Takaishi M, Nagahara M, Nagotani S, Sehara Y, Jin G, Zhang H, Hayakawa S, et al: Implantation of the new porous gelatin-siloxane hybrid into brain lesions as a potential scaffod for tissue regeneration. J Cereb Blood Flow Metab. 26:1263–1273. 2006. View Article : Google Scholar : PubMed/NCBI
24	Summitomo S, Muramatsu R, Fujii S and Yamashita T: Vascular endothelial cells promote cortical neurite outgrowth via an integrin β3-dependent mechanism. Biochem Biophys Res Commun. 450:593–597. 2014. View Article : Google Scholar : PubMed/NCBI
25	Emgard M, Hallin U, Karlsson J, Bahr BA, Brundin P and Blomgren K: Both apoptosis and necrosis occur early after intracerebral grafting of ventral mesencephalic tissue: A role for protease activation. J Neurochem. 86:1223–1232. 2003. View Article : Google Scholar : PubMed/NCBI
26	Sortwell CE, Pitzer MR and Collier TJ: Time course of apoptotic cell death within mesencephalic cell suspension grafts: Implications for improving grafted dopamine neuron survival. Exp Neurol. 165:268–277. 2000. View Article : Google Scholar : PubMed/NCBI
27	Marchionini DM, Collier TJ, Pitzer MR and Sortwell CE: Reassessment of caspase inhibition to augment grafted dopamine neuron survival. Cell Transplant. 13:273–282. 2004. View Article : Google Scholar : PubMed/NCBI
28	Lanfer B, Hermann A, Kirsh M, Freudenberg U, Reuner U, Werner C and Storch A: Directed growth of adult human white matter stem cell-derived neurons on aligned fibrillar collagen. Tissue Eng Part A. 16:1103–1113. 2010. View Article : Google Scholar : PubMed/NCBI
29	Yoshinaga T, Hashimoto E, Ukai W, Ishii T, Shirasaka T, Kigawa Y, Tateno M, Kaneta H, Watanabe K, Igarashi T, et al: Effects of atelocollagen on neural stem cell function and its migrating capacity into brain in psychiatric disease model. J Neural Transm (Vienna). 120:1491–1498. 2013. View Article : Google Scholar : PubMed/NCBI