Rat vibrissa dermal papilla cells promote healing of spinal cord injury following transplantation

Li,Meiying; Mei,Xianglin; Lv,Shuang; Zhang,Zechuan; Xu,Jinying; Sun,Dongjie; Xu,Jiayi; He,Xia; Chi,Guangfan; Li,Yulin

doi:10.3892/etm.2018.5916

Rat vibrissa dermal papilla cells promote healing of spinal cord injury following transplantation

Authors:
- Meiying Li
- Xianglin Mei
- Shuang Lv
- Zechuan Zhang
- Jinying Xu
- Dongjie Sun
- Jiayi Xu
- Xia He
- Guangfan Chi
- Yulin Li
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Affiliations: Key Laboratory of Pathobiology, Ministry of Education, Jilin University, Changchun, Jilin 130021, P.R. China, Department of Pathology, The Second Hospital of Jilin University, Changchun, Jilin 130041, P.R. China, Clinical Medical College, Jilin University, Changchun, Jilin 130021, P.R. China
Published online on: February 28, 2018 https://doi.org/10.3892/etm.2018.5916
Pages: 3929-3939
Copyright: © Li et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Bone marrow mesenchymal stem cell (BMSC) transplantation is effective for repairing spinal cord injuries (SCIs); however, there are limitations of clinical BMSC applications. Previously, we reported that dermal papilla cells (DPCs) secrete brain‑derived neurotrophic factor and glial cell line‑derived neurotrophic factor more actively than BMSCs. To analyze the therapeutic function of DPCs in SCI, primary DPCs and BMSCs were cultured from the same green fluorescence protein-transgenic rat. The cells were suspended in rat‑tail collagen I and transplanted separately into completely transected spinal cord lesion sites. Grafted‑cell survival was examined with a small animal in vivo imaging detection system, and lesion sites were examined histochemically. In vivo imaging revealed enhanced lesion filling and survival with DPC grafts compared with BMSC grafts on days 14 and 21 post‑transplantation. Hematoxylin and eosin staining demonstrated that lesion area sizes in the two groups were not markedly different. In the DPC transplant group, more axons formed within the lesion sites. CD31‑positive vessel‑like structures were more abundant in lesion sites near the grafted cells in the DPC group. The results of the present study suggest that DPCs may be a valuable alternative source of stem cells for autologous cell therapy for the treatment of SCI.

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1	Nakamura M and Okano H: Cell transplantation therapies for spinal cord injury focusing on induced pluripotent stem cells. Cell Res. 23:70–80. 2013. View Article : Google Scholar : PubMed/NCBI
2	Tang L, Lu X, Zhu R, Qian T, Tao Y, Li K, Zheng J, Zhao P, Li S, Wang X and Li L: Adipose-derived stem cells expressing the neurogenin-2 promote functional recovery after spinal cord injury in rat. Cell Mol Neurobiol. 36:657–667. 2016. View Article : Google Scholar : PubMed/NCBI
3	Mothe AJ and Tator CH: Advances in stem cell therapy for spinal cord injury. J Clin Invest. 122:3824–3834. 2012. View Article : Google Scholar : PubMed/NCBI
4	Yokota K, Kobayakawa K, Kubota K, Miyawaki A, Okano H, Ohkawa Y, Iwamoto Y and Okada S: Engrafted neural stem/progenitor cells promote functional recovery through synapse reorganization with spared host neurons after spinal cord injury. Stem Cell Reports. 5:264–277. 2015. View Article : Google Scholar : PubMed/NCBI
5	Wang YX, Sun JJ, Zhang M, Hou XH, Hong J, Zhou YJ and Zhang ZY: Propofol injection combined with bone marrow mesenchymal stem cell transplantation better improves electrophysiological function in the hindlimb of rats with spinal cord injury than monotherapy. Neural Regen Res. 10:636–643. 2015. View Article : Google Scholar : PubMed/NCBI
6	Sabapathy V, Tharion G and Kumar S: Cell therapy augments functional recovery subsequent to spinal cord injury under experimental conditions. Stem Cells Int. 2015:1321722015. View Article : Google Scholar : PubMed/NCBI
7	Neirinckx V, Cantinieaux D, Coste C, Rogister B, Franzen R and Wislet-Gendebien S: Concise review: Spinal cord injuries: How could adult mesenchymal and neural crest stem cells take up the challenge? Stem Cells. 32:829–843. 2014. View Article : Google Scholar : PubMed/NCBI
8	Ritfeld GJ, Patel A, Chou A, Novosat TL, Castillo DG, Roos RA and Oudega M: The role of brain-derived neurotrophic factor in bone marrow stromal cell-mediated spinal cord repair. Cell Transplant. 24:2209–2220. 2015. View Article : Google Scholar : PubMed/NCBI
9	Cantinieaux D, Quertainmont R, Blacher S, Rossi L, Wanet T, Noël A, Brook G, Schoenen J and Franzen R: Conditioned medium from bone marrow-derived mesenchymal stem cells improves recovery after spinal cord injury in rats: An original strategy to avoid cell transplantation. PLoS One. 8:e695152013. View Article : Google Scholar : PubMed/NCBI
10	Wang X, Zou X, Zhao J, Wu X, E L, Feng L, Wang D, Zhang G, Xing H and Liu H: Site-specific characteristics of bone marrow mesenchymal stromal cells modify the effect of aging on the skeleton. Rejuvenation Res. 2016 Mar 15;(Epub ahead of print). View Article : Google Scholar
11	Li M, Liu JY, Wang S, Xu H, Cui L, Lv S, Xu J, Liu S, Chi G and Li Y: Multipotent neural crest stem cell-like cells from rat vibrissa dermal papilla induce neuronal differentiation of PC12 cells. Biomed Res Int. 2014:1862392014.
12	Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 25:402–408. 2001. View Article : Google Scholar : PubMed/NCBI
13	Medalha CC, Jin Y, Yamagami T, Haas C and Fischer I: Transplanting neural progenitors into a complete transection model of spinal cord injury. J Neurosci Res. 92:607–618. 2014. View Article : Google Scholar : PubMed/NCBI
14	Molina AE, Cristante AF, de Barros TE Sr, Molina MS and Molina TP: A computerized system for the application of Basso, Beattie and Bresnahan scale in Wistar rats. Acta Ortop Bras. 23:179–183. 2015. View Article : Google Scholar : PubMed/NCBI
15	Nakano N, Nakai Y, Seo TB, Homma T, Yamada Y, Ohta M, Suzuki Y, Nakatani T, Fukushima M, Hayashibe M and Ide C: Effects of bone marrow stromal cell transplantation through CSF on the subacute and chronic spinal cord injury in rats. PLoS One. 8:e734942013. View Article : Google Scholar : PubMed/NCBI
16	Dasari VR, Veeravalli KK and Dinh DH: Mesenchymal stem cells in the treatment of spinal cord injuries: A review. World J Stem Cells. 6:120–133. 2014. View Article : Google Scholar : PubMed/NCBI
17	Klar AS, Zimoch J and Biedermann T: Skin tissue engineering: Application of adipose-derived stem cells. Biomed Res Int. 2017:97470102017. View Article : Google Scholar : PubMed/NCBI
18	Li C, Wei G, Gu Q, Wen G, Qi B, Xu L and Tao S: Donor age and cell passage affect osteogenic ability of rat bone marrow mesenchymal stem cells. Cell Biochem Biophys. 72:543–549. 2015. View Article : Google Scholar : PubMed/NCBI
19	Hoffman RM: The hair follicle as a gene therapy target. Nat Biotechnol. 18:20–21. 2000. View Article : Google Scholar : PubMed/NCBI
20	Driskell RR, Clavel C, Rendl M and Watt FM: Hair follicle dermal papilla cells at a glance. J Cell Sci. 124:1179–1182. 2011. View Article : Google Scholar : PubMed/NCBI
21	Tyor WR, Avgeropoulos N, Ohlandt G and Hogan EL: Treatment of spinal cord impact injury in the rat with transforming growth factor-beta. J Neurol Sci. 200:33–41. 2002. View Article : Google Scholar : PubMed/NCBI
22	Walker MJ, Walker CL, Zhang YP, Shields LB, Shields CB and Xu XM: A novel vertebral stabilization method for producing contusive spinal cord injury. J Vis Exp. 5:e501492015.
23	Kim M, Park SR and Choi BH: Biomaterial scaffolds used for the regeneration of spinal cord injury (SCI). Histol Histopathol. 29:1395–1408. 2014.PubMed/NCBI
24	Assunção-Silva RC, Gomes ED, Sousa N, Silva NA and Salgado AJ: Hydrogels and cell based therapies in spinal cord injury regeneration. Stem Cells Int. 2015:9480402015. View Article : Google Scholar : PubMed/NCBI
25	Lu P, Wang Y, Graham L, McHale K, Gao M, Wu D, Brock J, Blesch A, Rosenzweig ES, Havton LA, et al: Long-distance growth and connectivity of neural stem cells after severe spinal cord injury. Cell. 150:1264–1273. 2012. View Article : Google Scholar : PubMed/NCBI
26	Nectow AR, Marra KG and Kaplan DL: Biomaterials for the development of peripheral nerve guidance conduits. Tissue Eng Part B Rev. 18:40–50. 2012. View Article : Google Scholar : PubMed/NCBI
27	Watanabe K, Nakamura M, Okano H and Toyama Y: Establishment of three-dimensional culture of neural stem/progenitor cells in collagen Type-1 Gel. Restor Neurol Neurosci. 25:109–117. 2007.PubMed/NCBI
28	Boehler RM, Kuo R, Shin S, Goodman AG, Pilecki MA, Gower RM, Leonard JN and Shea LD: Lentivirus delivery of IL-10 to promote and sustain macrophage polarization towards an anti-inflammatory phenotype. Biotechnol Bioeng. 111:1210–1221. 2014. View Article : Google Scholar : PubMed/NCBI
29	Zhang F, Wang H, Wang X, Jiang G, Liu H, Zhang G, Wang H, Fang R, Bu X, Cai S and Du J: TGF-β induces M2-like macrophage polarization via SNAIL-mediated suppression of a pro-inflammatory phenotype. Oncotarget. 7:52294–52306. 2016.PubMed/NCBI
30	Liu F, Uchugonova A, Kimura H, Zhang C, Zhao M, Zhang L, Koenig K, Duong J, Aki R, Saito N, et al: The bulge area is the major hair follicle source of nestin-expressing pluripotent stem cells which can repair the spinal cord compared to the dermal papilla. Cell Cycle. 10:830–839. 2011. View Article : Google Scholar : PubMed/NCBI