Neuroregenerative effects of olfactory ensheathing cells transplanted in a multi-layered conductive nanofibrous conduit in peripheral nerve repair in rats

Journal of Biomedical Science

Masoud Soleimani¹  Mohammad Vaseei⁶  Masumeh Dodel³  Hana Hanaee-Ahvaz⁷  Abbas Shafiee⁴  Saeed Oraee-Yazdani⁵  Mahboubeh Kabiri² 

[1] Department of Hematology, Faculty of Medical Science, Tarbiat Modares University, Tehran, Iran;Department of Nanotechnology and Tissue Engineering, Stem Cell Technology Research Center, Tehran, Iran;Department of Textile engineering, Amirkabir University of Technology, Tehran, Iran, Stem Cell Technology Research Center, Tehran, Iran;Experimental Dermatology Group, UQ Centre for Clinical Research, The University of Queensland, Herston, Queensland, Australia;Functional Neurosurgery Research Center, Department of Neurosurgery, Shohada Tajrish Hospital, Shahid Beheshti University of Medical Sciences, Tehran, Iran;Pathology Department, Shariati Hospital, Tehran University of Medical Sciences, Tehran, Iran;Department of Stem Cell Biology, Stem Cell Technology Research Center, Tehran, Iran

关键词: Carbon nanotube;    Nanofibrous conduit;    Conductive;    Composite scaffold;    Olfactory Ensheathing Cells;    Nerve tissue engineering;   

Others  :  1213948
DOI  :  10.1186/s12929-015-0144-0

 received in 2015-03-13, accepted in 2015-05-01,  发布年份 2015

【 摘 要 】

Background

The purpose of this study was to evaluate the efficacy of a multi-layered conductive nanofibrous hollow conduit in combination with olfactory ensheathing cells (OEC) to promote peripheral nerve regeneration. We aimed to harness both the topographical and electrical cues of the aligned conductive nanofibrous single-walled carbon nanotube/ poly (_L-lactic acid) (SWCNT/PLLA) scaffolds along with the neurotrophic features of OEC in a nerve tissue engineered approach.

Results

We demonstrated that SWCNT/PLLA composite scaffolds support the adhesion, growth, survival and proliferation of OEC. Using microsurgical techniques, the tissue engineered nerve conduits were interposed into an 8 mm gap in sciatic nerve defects in rats. Functional recovery was evaluated using sciatic functional index (SFI) fortnightly after the surgery. Histological analyses including immunohistochemistry for S100 and NF markers along with toluidine blue staining (nerve thickness) and TEM imaging (myelin sheath thickness) of the sections from middle and distal parts of nerve grafts showed an increased regeneration in cell/scaffold group compared with cell-free scaffold and silicone groups. Neural regeneration in cell/scaffold group was very closely similar to autograft group, as deduced from SFI scores and histological assessments.

Conclusions

Our results indicated that the tissue engineered construct made of rolled sheet of SWCNT/PLLA nanofibrous scaffolds and OEC could promote axonal outgrowth and peripheral nerve regeneration suggesting them as a promising alternative in nerve tissue engineering.

【 授权许可】

   
2015 Kabiri et al.; licensee BioMed Central.

【 图 表 】

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【 参考文献 】

• [1]Evans GR. Peripheral nerve injury: a review and approach to tissue engineered constructs. Anat Rec. 2001; 263(4):396-404.
• [2]Noble J, Munro CA, Prasad VS, Midha R. Analysis of upper and lower extremity peripheral nerve injuries in a population of patients with multiple injuries. J Trauma. 1998; 45(1):116-22.
• [3]Siemionow M, Brzezicki G. Chapter 8: Current techniques and concepts in peripheral nerve repair. Int Rev Neurobiol. 2009; 87:141-72.
• [4]Spivey EC, Khaing ZZ, Shear JB, Schmidt CE. The fundamental role of subcellular topography in peripheral nerve repair therapies. Biomaterials. 2012; 33(17):4264-76.
• [5]Schmidt CE, Leach JB. Neural tissue engineering: strategies for repair and regeneration. Annu Rev Biomed Eng. 2003; 5(1):293-347.
• [6]Gu X, Ding F, Yang Y, Liu J. Construction of tissue engineered nerve grafts and their application in peripheral nerve regeneration. Prog Neurobiol. 2011; 93(2):204-30.
• [7]Jenq CB, Coggeshall RE. Nerve regeneration through holey silicone tubes. Brain Res. 1985; 361(1-2):233-41.
• [8]Oudega M, Gautier SE, Chapon P, Fragoso M, Bates ML, Parel JM et al.. Axonal regeneration into Schwann cell grafts within resorbable poly (< i > α -hydroxyacid) guidance channels in the adult rat spinal cord. Biomaterials. 2001; 22(10):1125-36.
• [9]Ramon-Cueto A, Valverde F. Olfactory bulb ensheathing glia: a unique cell type with axonal growth-promoting properties. Glia. 1995; 14(3):163-73.
• [10]Verdú E, Navarro X, Gudiño-Cabrera G, Rodríguez FJ, Ceballos D, Valero A et al.. Olfactory bulb ensheathing cells enhance peripheral nerve regeneration. Neuroreport. 1999; 10(5):1097-101.
• [11]Franklin R, Gilson J, Franceschini I, Barnett S. Schwann cell‐like myelination following transplantation of an olfactory bulb‐ensheathing cell line into areas of demyelination in the adult CNS. Glia. 1996; 17(3):217-24.
• [12]Chen L, Huang H, Xi H, Zhang F, Liu Y, Chen D et al.. A Prospective Randomized Double-Blind Clinical Trial Using a Combination of Olfactory Ensheathing Cells and Schwann Cells for the Treatment of Chronic Complete Spinal Cord Injuries. Cell Transplant. 2014; 23 Supplement 1:S35-44.
• [13]Wiliams RR, Bunge M. Schwann cell transplantation: a repair strategy for spinal cord injury? Prog Brain Res. 2011; 201:295-312.
• [14]Boyd JG, Doucette R, Kawaja MD. Defining the role of olfactory ensheathing cells in facilitating axon remyelination following damage to the spinal cord. FASEB J. 2005; 19(7):694-703.
• [15]Rao Y, Zhu W, Du Z, Jia C, Du T, Zhao Q et al.. Effectiveness of olfactory ensheathing cell transplantation for treatment of spinal cord injury. Genet Mol Res. 2014; 13(2):4124-9.
• [16]Yazdani SO, Pedram M, Hafizi M, Kabiri M, Soleimani M, Dehghan M-M et al.. A comparison between neurally induced bone marrow derived mesenchymal stem cells and olfactory ensheathing glial cells to repair spinal cord injuries in rat. Tissue and Cell. 2012; 44(4):205-13.
• [17]Cao L, Zhu YL, Su Z, Lv B, Huang Z, Mu L et al.. Olfactory ensheathing cells promote migration of Schwann cells by secreted nerve growth factor. Glia. 2007; 55(9):897-904.
• [18]Guérout N, Duclos C, Drouot L, Abramovici O, Bon‐Mardion N, Lacoume Y et al.. Transplantation of olfactory ensheathing cells promotes axonal regeneration and functional recovery of peripheral nerve lesion in rats. Muscle Nerve. 2011; 43(4):543-51.
• [19]Radtke C, Aizer AA, Agulian SK, Lankford KL, Vogt PM, Kocsis JD. Transplantation of olfactory ensheathing cells enhances peripheral nerve regeneration after microsurgical nerve repair. Brain Res. 2009; 1254:10-7.
• [20]Tan C, Ng M, Ohnmar H, Lokanathan Y, Nur-Hidayah H, Roohi S et al.. Sciatic nerve repair with tissue engineered nerve: Olfactory ensheathing cells seeded poly (lactic-co-glygolic acid) conduit in an animal model. Indian J Orthop. 2013; 47(6):547.
• [21]Potter W, Kalil RE, Kao WJ. Biomimetic material systems for neural progenitor cell-based therapy. Front Biosci. 2008; 13:806-21.
• [22]Chew SY, Wen Y, Dzenis Y, Leong KW. The role of electrospinning in the emerging field of nanomedicine. Curr Pharm Des. 2006; 12(36):4751-70.
• [23]Fan L, Feng C, Zhao W, Qian L, Wang Y, Li Y. Directional neurite outgrowth on superaligned carbon nanotube yarn patterned substrate. Nano Lett. 2012; 12(7):3668-73.
• [24]Schmidt C, Shastri V, Vacanti J, Langer R. Stimulation of neurite outgrowth using an electrically conducting polymer. Proc Natl Acad Sci U S A. 1997; 94(17):8948.
• [25]Zhang Z, Rouabhia M, Wang Z, Roberge C, Shi G, Roche P et al.. Electrically conductive biodegradable polymer composite for nerve regeneration: electricity-stimulated neurite outgrowth and axon regeneration. Artif Organs. 2007; 31(1):13-22.
• [26]Chronakis IS, Grapenson S, Jakob A. Conductive polypyrrole nanofibers via electrospinning: electrical and morphological properties. Polymer. 2006; 47(5):1597-603.
• [27]Voge CM, Kariolis M, MacDonald RA, Stegemann JP. Directional conductivity in SWNT-collagen-fibrin composite biomaterials through strain-induced matrix alignment. J Biomed Mater Res A. 2008; 86(1):269-77.
• [28]MacDonald RA, Voge CM, Kariolis M, Stegemann JP. Carbon nanotubes increase the electrical conductivity of fibroblast-seeded collagen hydrogels. Acta Biomater. 2008; 4(6):1583-92.
• [29]Salehi M, Pasbakhsh P, Soleimani M, Abbasi M, Hasanzadeh G, Modaresi MH et al.. Repair of spinal cord injury by co-transplantation of embryonic stem cell-derived motor neuron and olfactory ensheathing cell. Iran Biomed J. 2009; 13(3):125-35.
• [30]Bain JR, Mackinnon SE, Hunter DA. Functional evaluation of complete sciatic, peroneal, and posterior tibial nerve lesions in the rat. Plast Reconstr Surg. 1989; 83(1):129-38.
• [31]Kabiri M, Soleimani M, Shabani I, Futrega K, Ghaemi N, Ahvaz HH et al.. Neural differentiation of mouse embryonic stem cells on conductive nanofiber scaffolds. Biotechnol Lett. 2012; 34(7):1357-65.
• [32]Chang CJ, Hsu S, Lin F, Chang H, Chang CS. Low‐intensity‐ultrasound–accelerated nerve regeneration using cell‐seeded poly (D, L‐lactic acid‐co‐glycolic acid) conduits: An in vivo and in vitro study. J Biomed Mater Res B Appl Biomater. 2005; 75(1):99-107.
• [33]Lee JY, Bashur CA, Goldstein AS, Schmidt CE. Polypyrrole-coated electrospun PLGA nanofibers for neural tissue applications. Biomaterials. 2009; 30(26):4325-35.
• [34]Li M, Guo Y, Wei Y, MacDiarmid AG, Lelkes PI. Electrospinning polyaniline-contained gelatin nanofibers for tissue engineering applications. Biomaterials. 2006; 27(13):2705-15.
• [35]Murugan R, Ramakrishna S. Design strategies of tissue engineering scaffolds with controlled fiber orientation. Tissue Eng. 2007; 13(8):1845-66.
• [36]Bryan DJ, Tang JB, Doherty SA, Hile DD, Trantolo DJ, Wise DL et al.. Enhanced peripheral nerve regeneration through a poled bioresorbable poly (lactic-co-glycolic acid) guidance channel. J Neural Eng. 2004; 1:91.
• [37]Al-Majed AA, Neumann CM, Brushart TM, Gordon T. Brief electrical stimulation promotes the speed and accuracy of motor axonal regeneration. J Neurosci. 2000; 20(7):2602-8.
• [38]Seil JT, Webster TJ. Electrically active nanomaterials as improved neural tissue regeneration scaffolds. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2010; 2(6):635-47.
• [39]Nguyen QT, Sanes JR, Lichtman JW. Pre-existing pathways promote precise projection patterns. Nat Neurosci. 2002; 5(9):861-7.
• [40]Lin YL, Jen JC, Hsu S, Chiu IM. Sciatic nerve repair by microgrooved nerve conduits made of chitosan-gold nanocomposites. Surg Neurol. 2008; 70:S9-18.
• [41]You H, Wei L, Liu Y, Oudega M, Jiao SS, Feng SN et al.. Olfactory ensheathing cells enhance Schwann cell-mediated anatomical and functional repair after sciatic nerve injury in adult rats. Exp Neurol. 2011; 229(1):158-67.
• [42]Buti M, Verdu E, Labrador RO, Vilches JJ, Forés J, Navarro X. Influence of physical parameters of nerve chambers on peripheral nerve regeneration and reinnervation. Exp Neurol. 1996; 137(1):26-33.
• [43]Jones LL, Sajed D, Tuszynski MH. Axonal regeneration through regions of chondroitin sulfate proteoglycan deposition after spinal cord injury: a balance of permissiveness and inhibition. J Neurosci. 2003; 23(28):9276-88.
• [44]Wewetzer K, Verdú E, Angelov DN, Navarro X. Olfactory ensheathing glia and Schwann cells: two of a kind? Cell Tissue Res. 2002; 309(3):337-45.
• [45]He B-R, Xie S-T, Wu M-M, Hao D-J, Yang H. Phagocytic removal of neuronal debris by olfactory ensheathing cells enhances neuronal survival and neurite outgrowth via p38MAPK activity. Mol Neurobiol. 2014; 49(3):1501-12.