Magnetic Field Promotes Migration of Schwann Cells with Chondroitinase ABC (ChABC)-Loaded Superparamagnetic Nanoparticles Across Astrocyte Boundary in vitro

References

• Wang X, Peng C, Zhang S, et al. Polysialic-acid-based micelles promote neural regeneration in spinal cord injury therapy. Nano Lett. 2019;19(2):829–838. doi:10.1021/acs.nanolett.8b0402030605619
   PubMed Web of Science ®Google Scholar
• Tran AP, Warren PM, Silver J. The biology of regeneration failure and success after spinal cord injury. Physiol Rev. 2018;98(2):881–917. doi:10.1152/physrev.00017.201729513146
   PubMed Web of Science ®Google Scholar
• Huang L, Xia B, Liu Z, Cao Q, Huang J, Luo Z. Superparamagnetic iron oxide nanoparticle-mediated forces enhance the migration of schwann cells across the astrocyte-schwann cell boundary in vitro. Front Cell Neurosci. 2017;11:83.28400720
   PubMed Web of Science ®Google Scholar
• Arthur-Farraj PJ, Latouche M, Wilton DK, et al. c-Jun reprograms Schwann cells of injured nerves to generate a repair cell essential for regeneration. Neuron. 2012;75(4):633–647. doi:10.1016/j.neuron.2012.06.02122920255
   PubMed Web of Science ®Google Scholar
• Huang J, Hu X, Lu L, Ye Z, Zhang Q, Luo Z. Electrical regulation of Schwann cells using conductive polypyrrole/chitosan polymers. J Biomed Mater Res A. 2009;9999A(1):NA–NA. doi:10.1002/jbm.a.32511
   Google Scholar
• Papastefanaki F, Chen J, Lavdas AA, Thomaidou D, Schachner M, Matsas R. Grafts of Schwann cells engineered to express PSA-NCAM promote functional recovery after spinal cord injury. Brain. 2007;130(8):2159–2174. doi:10.1093/brain/awm15517626035
   PubMedGoogle Scholar
• Houle JD, Tom VJ, Mayes D, Wagoner G, Phillips N, Silver J. Combining an autologous peripheral nervous system “bridge” and matrix modification by chondroitinase allows robust, functional regeneration beyond a hemisection lesion of the adult rat spinal cord. J Neurosci. 2006;26(28):7405–7415. doi:10.1523/JNEUROSCI.1166-06.200616837588
   PubMed Web of Science ®Google Scholar
• Dezawa M, Adachi-Usami E. Role of Schwann cells in retinal ganglion cell axon regeneration. Prog Retin Eye Res. 2000;19(2):171–204. doi:10.1016/S1350-9462(99)00010-510674707
   PubMed Web of Science ®Google Scholar
• Liu Z, Zhu S, Liu L, et al. A magnetically responsive nanocomposite scaffold combined with Schwann cells promotes sciatic nerve regeneration upon exposure to magnetic field. Int J Nanomedicine. 2017;12:7815–7832. doi:10.2147/IJN29123395
   PubMed Web of Science ®Google Scholar
• Bunge MB. Novel combination strategies to repair the injured mammalian spinal cord. J Spinal Cord Med. 2016;31(3):262–269. doi:10.1080/10790268.2008.11760720
   Google Scholar
• Kanno H, Pearse DD, Ozawa H, Itoi E, Bunge MB. Schwann cell transplantation for spinal cord injury repair: its significant therapeutic potential and prospectus. Rev Neurosci. 2015;26(2):121–128. doi:10.1515/revneuro-2014-006825581750
   PubMed Web of Science ®Google Scholar
• Tetzlaff W, Okon EB, Karimi-Abdolrezaee S, et al. A systematic review of cellular transplantation therapies for spinal cord injury. J Neurotrauma. 2011;28(8):1611–1682. doi:10.1089/neu.2009.117720146557
   PubMed Web of Science ®Google Scholar
• Fortun J, Hill CE, Bunge MB. Combinatorial strategies with Schwann cell transplantation to improve repair of the injured spinal cord. Neurosci Lett. 2009;456(3):124–132. doi:10.1016/j.neulet.2008.08.09219429147
   PubMed Web of Science ®Google Scholar
• Chaudhry N, Bachelin C, Zujovic V, et al. Myelin-associated glycoprotein inhibits schwann cell migration and induces their death. J Neurosci. 2017;37(24):5885–5899. doi:10.1523/JNEUROSCI.1822-16.201728522736
   PubMed Web of Science ®Google Scholar
• Grimpe B, Pressman Y, Bunge MB, Silver J. The role of proteoglycans in Schwann cell/astrocyte interactions and in regeneration failure at PNS/CNS interfaces. Mol Cell Neurosci. 2005;28(1):18–29. doi:10.1016/j.mcn.2004.06.01015607938
   PubMed Web of Science ®Google Scholar
• Lakatos A, Barnett SC, Franklin RJM. Olfactory ensheathing cells induce less host astrocyte response and chondroitin sulphate proteoglycan expression than schwann cells following transplantation into adult CNS white matter. Exp Neurol. 2003;184(1):237–246. doi:10.1016/S0014-4886(03)00270-X14637095
   PubMed Web of Science ®Google Scholar
• Wiliams RR, Bunge MB. Schwann cell transplantation: a repair strategy for spinal cord injury? Prog Brain Res. 2012;201:295–312.23186720
   PubMed Web of Science ®Google Scholar
• Koh CH, Pronin S, Hughes M. Chondroitinase ABC for neurological recovery after acute brain injury: systematic review and meta-analyses of preclinical studies. Brain Injury. 2018;32(6):715–729. doi:10.1080/02699052.2018.143866529436856
   PubMed Web of Science ®Google Scholar
• Takeuchi K, Yoshioka N, Higa Onaga S, et al. Chondroitin sulphate N-acetylgalactosaminyl-transferase-1 inhibits recovery from neural injury. Nat Commun. 2013;4(1). doi:10.1038/ncomms3740.
   Google Scholar
• Zhao R, Muir EM, Alves JN, et al. Lentiviral vectors express chondroitinase ABC in cortical projections and promote sprouting of injured corticospinal axons. J Neurosci Meth. 2011;201(1):228–238. doi:10.1016/j.jneumeth.2011.08.003
   PubMed Web of Science ®Google Scholar
• Chen M, Zheng B. Axon plasticity in the mammalian central nervous system after injury. Trends Neurosci. 2014;37(10):583–593. doi:10.1016/j.tins.2014.08.00825218468
   PubMed Web of Science ®Google Scholar
• Muir EM, Fyfe I, Gardiner S, et al. Modification of N-glycosylation sites allows secretion of bacterial chondroitinase ABC from mammalian cells. J Biotechnol. 2010;145(2):103–110. doi:10.1016/j.jbiotec.2009.11.00219900493
   PubMed Web of Science ®Google Scholar
• Buss A. Gradual loss of myelin and formation of an astrocytic scar during Wallerian degeneration in the human spinal cord. Brain. 2004;127(1):34–44. doi:10.1093/brain/awh00114534158
   PubMedGoogle Scholar
• Iwashita Y, Fawcett JW, Crang AJ, Franklin RJM, Blakemore WF. Schwann cells transplanted into normal and X-irradiated adult white matter do not migrate extensively and show poor long-term survival. Exp Neurol. 2000;164(2):292–302. doi:10.1006/exnr.2000.744010915568
   PubMed Web of Science ®Google Scholar
• Amani H, Mostafavi E, Arzaghi H, et al. Three-dimensional graphene foams: synthesis, properties, biocompatibility, biodegradability, and applications in tissue engineering. Acs Biomater Sci Eng. 2019;5(1):193–214. doi:10.1021/acsbiomaterials.8b00658
   PubMed Web of Science ®Google Scholar
• Zhang X, Wu F, Men K, et al. Modified Fe3O4 magnetic nanoparticle delivery of CpG inhibits tumor growth and spontaneous pulmonary metastases to enhance immunotherapy. Nanoscale Res Lett. 2018;13(1). doi:10.1186/s11671-018-2661-8.
   Google Scholar
• Zhao X, Cui H, Chen W, et al. Morphology, structure and function characterization of PEI modified magnetic nanoparticles gene delivery system. PLoS One. 2014;9(6):e98919. doi:10.1371/journal.pone.009891924911360
   PubMed Web of Science ®Google Scholar
• Krötz F, Wit CD, Sohn H, et al. Magnetofection—A highly efficient tool for antisense oligonucleotide delivery in vitro and in vivo. Mol Ther. 2003;7(5):700–710. doi:10.1016/S1525-0016(03)00065-012718913
   PubMed Web of Science ®Google Scholar
• Lopez-Verrilli MA, Picou F, Court FA. Schwann cell-derived exosomes enhance axonal regeneration in the peripheral nervous system. Glia. 2013;61(11):1795–1806. doi:10.1002/glia.2255824038411
   PubMed Web of Science ®Google Scholar
• Afshari FT, Fawcett JW. Astrocyte-Schwann-cell coculture systems. Methods Mol Biol. 2012;814:381–391.22144320
   PubMedGoogle Scholar
• Xia B, Huang L, Zhu L, et al. Manipulation of Schwann cell migration across the astrocyte boundary by polysialyltransferase-loaded superparamagnetic nanoparticles under magnetic field. Int J Nanomed. 2016;11:6727–6741. doi:10.2147/IJN.S122358
   PubMed Web of Science ®Google Scholar
• Liu T, Xu J, Chan BP, Chew SY. Sustained release of neurotrophin-3 and chondroitinase ABC from electrospun collagen nanofiber scaffold for spinal cord injury repair. J Biomed Mater Res A. 2012;100A(1):236–242. doi:10.1002/jbm.a.v100a.1
   Web of Science ®Google Scholar
• Kanno H, Pressman Y, Moody A, et al. Combination of engineered Schwann cell grafts to secrete neurotrophin and chondroitinase promotes axonal regeneration and locomotion after spinal cord injury. J Neurosci. 2014;34(5):1838–1855. doi:10.1523/JNEUROSCI.2661-13.201424478364
   PubMed Web of Science ®Google Scholar
• Moon LDF, Asher RA, Rhodes KE, Fawcett JW. Relationship between sprouting axons, proteoglycans and glial cells following unilateral nigrostriatal axotomy in the adult rat. Neuroscience. 2002;109(1):101–117. doi:10.1016/S0306-4522(01)00457-211784703
   PubMed Web of Science ®Google Scholar
• Afshari FT, Kwok JC, Fawcett JW. Analysis of Schwann-astrocyte interactions using in vitro assays. J Visualized Exp. 2011;(47):2214.
   PubMed Web of Science ®Google Scholar
• Cao L, Zhu YL, Su Z, et al. Olfactory ensheathing cells promote migration of Schwann cells by secreted nerve growth factor. Glia. 2007;55(9):897–904. doi:10.1002/glia.2051117405147
   PubMed Web of Science ®Google Scholar
• O’Neill P, Lindsay SL, Pantiru A, et al. Sulfatase-mediated manipulation of the astrocyte-Schwann cell interface. Glia. 2017;65(1):19–33. doi:10.1002/glia.2304727535874
   PubMed Web of Science ®Google Scholar
• Ma T, Wang Y, Qi F, et al. The effect of synthetic oxygen carrier-enriched fibrin hydrogel on Schwann cells under hypoxia condition in vitro. Biomaterials. 2013;34(38):10016–10027. doi:10.1016/j.biomaterials.2013.09.04724095255
   PubMed Web of Science ®Google Scholar
• Okada S, Hara M, Kobayakawa K, Matsumoto Y, Nakashima Y. Astrocyte reactivity and astrogliosis after spinal cord injury. Neurosci Res. 2018;126:39–43. doi:10.1016/j.neures.2017.10.00429054466
   PubMed Web of Science ®Google Scholar
• Silver J, Miller JH. Regeneration beyond the glial scar. Nat Rev Neurosci. 2004;5(2):146–156. doi:10.1038/nrn132614735117
   PubMed Web of Science ®Google Scholar
• Prabha G, Raj V. Preparation and characterization of chitosan-Polyethylene glycol-polyvinylpyrrolidone-coated superparamagnetic iron oxide nanoparticles as carrier system: drug loading and in vitro drug release study. J Biomed Mat Res Part B. 2016;104(4):808–816. doi:10.1002/jbm.b.v104.4
   PubMed Web of Science ®Google Scholar
• Cicha I, Scheffler L, Ebenau A, Lyer S, Alexiou C, Goppelt-Struebe M. Mitoxantrone-loaded superparamagnetic iron oxide nanoparticles as drug carriers for cancer therapy: uptake and toxicity in primary human tubular epithelial cells. Nanotoxicology. 2015;10(5):557–566. doi:10.3109/17435390.2015.109536426468004
   PubMed Web of Science ®Google Scholar
• Bilyy R, Unterweger H, Weigel B, et al. Inert coats of magnetic nanoparticles prevent formation of occlusive intravascular co-aggregates with neutrophil extracellular traps. Front Immunol. 2018;9. doi:10.3389/fimmu.2018.02266.
   Web of Science ®Google Scholar
• Amani H, Kazerooni H, Hassanpoor H, Akbarzadeh A, Pazoki-Toroudi H. Tailoring synthetic polymeric biomaterials towards nerve tissue engineering: a review. Artif Cells Nanomed Biotechnol. 2019;47(1):3524–3539. doi:10.1080/21691401.2019.163972331437011
   PubMed Web of Science ®Google Scholar
• Amani H, Arzaghi H, Bayandori M, et al. controlling cell behavior through the design of biomaterial surfaces: a focus on surface modification techniques. Adv Mater Interfaces. 2019;6(13):1900572. doi:10.1002/admi.v6.13
   Web of Science ®Google Scholar
• Mykhaylyk O, Sobisch T, Almstätter I, et al. Silica-iron oxide magnetic nanoparticles modified for gene delivery: a search for optimum and quantitative criteria. Pharm Res-Dordr. 2012;29(5):1344–1365. doi:10.1007/s11095-011-0661-9
   PubMed Web of Science ®Google Scholar
• Su L, Zhang B, Huang Y, Zhang H, Xu Q, Tan J. Superparamagnetic iron oxide nanoparticles modified with dimyristoylphosphatidylcholine and their distribution in the brain after injection in the rat substantia nigra. Mat Sci Eng. 2017;81:400–406. doi:10.1016/j.msec.2017.08.049
   Google Scholar
• Lozano O, Mejia J, Tabarrant T, et al. Quantification of nanoparticles in aqueous food matrices using particle-induced X-ray emission. Anal Bioanal Chem. 2012;403(10):2835–2841. doi:10.1007/s00216-012-5895-922411536
   PubMed Web of Science ®Google Scholar
• Lozano O, Mejia J, Masereel B, Toussaint O, Lison D, Lucas S. Development of a PIXE analysis method for the determination of the biopersistence of SiC and TiC nanoparticles in rat lungs. Nanotoxicology. 2011;6(3):263–271. doi:10.3109/17435390.2011.57230121504370
   PubMed Web of Science ®Google Scholar
• Wang J, Xiang B, Deng J, et al. Externally applied static magnetic field enhances cardiac retention and functional benefit of magnetically iron-labeled adipose-derived stem cells in infarcted hearts. Stem Cell Transl Med. 2016;5(10):1380–1393. doi:10.5966/sctm.2015-0220
   PubMed Web of Science ®Google Scholar
• Muthana M, Scott SD, Farrow N, et al. A novel magnetic approach to enhance the efficacy of cell-based gene therapies. Gene Ther. 2008;15(12):902–910. doi:10.1038/gt.2008.5718418420
   PubMed Web of Science ®Google Scholar
• Pu A, Stephenson EL, Yong VW. The extracellular matrix: focus on oligodendrocyte biology and targeting CSPGs for remyelination therapies. Glia. 2018;66(9):1809–1825. doi:10.1002/glia.v66.929603376
   PubMed Web of Science ®Google Scholar
• Zou JL, Sun JH, Qiu S, et al. Spatial distribution affects the role of CSPGs in nerve regeneration via the actin filament-mediated pathway. Exp Neurol. 2018;307:37–44. doi:10.1016/j.expneurol.2018.05.02329852179
   PubMed Web of Science ®Google Scholar
• Raspa A, Bolla E, Cuscona C, Gelain F. Feasible stabilization of chondroitinase abc enables reduced astrogliosis in a chronic model of spinal cord injury. CNS Neurosci Ther. 2019;25(1):86–100. doi:10.1111/cns.2019.25.issue-129855151
   PubMed Web of Science ®Google Scholar
• Quraishe S, Forbes LH, Andrews MR. The extracellular environment of the CNS: influence on plasticity, sprouting, and axonal regeneration after spinal cord injury. Neural Plast. 2018;2018:2952386. doi:10.1155/2018/295238629849554
   PubMed Web of Science ®Google Scholar