{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,13]],"date-time":"2026-10-13T23:03:10Z","timestamp":1791932590648,"version":"4.3.4"},"reference-count":73,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2016,8,11]],"date-time":"2016-08-11T00:00:00Z","timestamp":1470873600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2016,8,11]],"date-time":"2016-08-11T00:00:00Z","timestamp":1470873600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>This study investigates the efficacy of local and intravenous mesenchymal stem cell (MSC) administration to augment neuroregeneration in both a sciatic nerve cut-and-repair and rat hindlimb transplant model. Bone marrow-derived MSCs were harvested and purified from Brown-Norway (BN) rats. Sciatic nerve transections and repairs were performed in three groups of Lewis (LEW) rats: negative controls (n\u2009=\u20094), local MSCs (epineural) injection (n\u2009=\u20094), and systemic MSCs (intravenous) injection (n\u2009=\u20094). Syngeneic (LEW-LEW) (n\u2009=\u20094) and allogeneic (BN-LEW) (n\u2009=\u20094) hindlimb transplants were performed and assessed for neuroregeneration after local or systemic MSC treatment. Rats undergoing sciatic nerve cut-and-repair and treated with either local or systemic injection of MSCs had significant improvement in the speed of recovery of compound muscle action potential amplitudes and axon counts when compared with negative controls. Similarly, rats undergoing allogeneic hindlimb transplants treated with local injection of MSCs exhibited significantly increased axon counts. Similarly, systemic MSC treatment resulted in improved nerve regeneration following allogeneic hindlimb transplants. Systemic administration had a more pronounced effect on electromotor recovery while local injection was more effective at increasing fiber counts, suggesting different targets of action. Local and systemic MSC injections significantly improve the pace and degree of nerve regeneration after nerve injury and hindlimb transplantation.<\/jats:p>","DOI":"10.1038\/srep31306","type":"journal-article","created":{"date-parts":[[2016,8,11]],"date-time":"2016-08-11T09:48:56Z","timestamp":1470908936000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":85,"title":["Mesenchymal Stem Cells Enhance Nerve Regeneration in a Rat Sciatic Nerve Repair and Hindlimb Transplant Model"],"prefix":"10.1038","volume":"6","author":[{"given":"Damon S.","family":"Cooney","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eric G.","family":"Wimmers","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zuhaib","family":"Ibrahim","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Johanna","family":"Grahammer","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joani M.","family":"Christensen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gabriel A.","family":"Brat","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lehao W.","family":"Wu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Karim A.","family":"Sarhane","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joseph","family":"Lopez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christoph","family":"Wallner","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Georg J.","family":"Furtm\u00fcller","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nance","family":"Yuan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"John","family":"Pang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kakali","family":"Sarkar","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"W. P. Andrew","family":"Lee","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gerald","family":"Brandacher","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2016,8,11]]},"reference":[{"key":"BFsrep31306_CR1","doi-asserted-by":"publisher","first-page":"80","DOI":"10.1097\/00006534-197707000-00012","volume":"60","author":"MG Orgel","year":"1977","unstructured":"Orgel, M. G. & Terzis, J. K. Epineurial vs. perineurial repair. Plast. Reconstr. Surg. 60, 80\u201391 (1977).","journal-title":"Plast. Reconstr. Surg."},{"key":"BFsrep31306_CR2","doi-asserted-by":"publisher","first-page":"1771","DOI":"10.1046\/j.0953-816x.2001.01814.x","volume":"14","author":"M Dezawa","year":"2001","unstructured":"Dezawa, M., Takahashi, I., Esaki, M., Takano, M. & Sawada, H. Sciatic nerve regeneration in rats induced by transplantation of in vitro differentiated bone-marrow stromal cells. Eur. J. Neurosci. 14, 1771\u20131776 (2001).","journal-title":"Eur. J. Neurosci."},{"key":"BFsrep31306_CR3","doi-asserted-by":"publisher","first-page":"331","DOI":"10.1097\/SAP.0b013e31826239f0","volume":"69","author":"KS Koh","year":"2012","unstructured":"Koh, K. S. et al. Clinical application of human adipose tissue-derived mesenchymal stem cells in progressive hemifacial atrophy (Parry-Romberg disease) with microfat grafting techniques using 3-dimensional computed tomography and 3-dimensional camera. Ann. Plast. Surg. 69, 331\u2013337 (2012).","journal-title":"Ann. Plast. Surg."},{"key":"BFsrep31306_CR4","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1146\/annurev-bioeng-070909-105309","volume":"12","author":"B Parekkadan","year":"2010","unstructured":"Parekkadan, B. & Milwid, J. M. Mesenchymal stem cells as therapeutics. Annu. Rev. Biomed. Eng. 12, 87\u2013117 (2010).","journal-title":"Annu. Rev. Biomed. Eng."},{"key":"BFsrep31306_CR5","doi-asserted-by":"publisher","first-page":"119","DOI":"10.1016\/j.bbrc.2004.03.192","volume":"318","author":"S Bhagavati","year":"2004","unstructured":"Bhagavati, S. & Xu, W. Isolation and enrichment of skeletal muscle progenitor cells from mouse bone marrow. Biochem. Biophys. Res. Commun. 318, 119\u2013124 (2004).","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"BFsrep31306_CR6","doi-asserted-by":"publisher","first-page":"143","DOI":"10.1126\/science.284.5411.143","volume":"284","author":"MF Pittenger","year":"1999","unstructured":"Pittenger, M. F. et al. Multilineage potential of adult human mesenchymal stem cells. Science 284, 143\u2013147 (1999).","journal-title":"Science"},{"key":"BFsrep31306_CR7","doi-asserted-by":"publisher","first-page":"840","DOI":"10.1002\/glia.20421","volume":"54","author":"J Caddick","year":"2006","unstructured":"Caddick, J., Kingham, P. J., Gardiner, N. J., Wiberg, M. & Terenghi, G. Phenotypic and functional characteristics of mesenchymal stem cells differentiated along a Schwann cell lineage. Glia 54, 840\u2013849 (2006).","journal-title":"Glia"},{"key":"BFsrep31306_CR8","doi-asserted-by":"publisher","first-page":"275","DOI":"10.1016\/S0079-6123(02)37021-3","volume":"137","author":"MB Bunge","year":"2002","unstructured":"Bunge, M. B. Bridging the transected or contused adult rat spinal cord with Schwann cell and olfactory ensheathing glia transplants. Prog. Brain.Res. 137, 275\u2013282 (2002).","journal-title":"Prog. Brain.Res."},{"key":"BFsrep31306_CR9","doi-asserted-by":"publisher","first-page":"262","DOI":"10.1080\/10790268.2008.11760720","volume":"31","author":"MB Bunge","year":"2008","unstructured":"Bunge, M. B. Novel combination strategies to repair the injured mammalian spinal cord. J. Spinal.Cord.Med. 31, 262\u2013269 (2008).","journal-title":"J. Spinal.Cord.Med."},{"key":"BFsrep31306_CR10","doi-asserted-by":"publisher","first-page":"381","DOI":"10.1177\/096368979800700406","volume":"7","author":"GW Plant","year":"1998","unstructured":"Plant, G. W., Chirila, T. V. & Harvey, A. R. Implantation of collagen IV\/poly(2-hydroxyethyl methacrylate) hydrogels containing Schwann cells into the lesioned rat optic tract. Cell.Transplant. 7, 381\u2013391 (1998).","journal-title":"Cell.Transplant."},{"key":"BFsrep31306_CR11","doi-asserted-by":"publisher","first-page":"242","DOI":"10.1016\/j.expneurol.2011.01.013","volume":"228","author":"A Ladak","year":"2011","unstructured":"Ladak, A., Olson, J., Tredget, E. E. & Gordon, T. Differentiation of mesenchymal stem cells to support peripheral nerve regeneration in a rat model. Exp. Neurol. 228, 242\u2013252 (2011).","journal-title":"Exp. Neurol."},{"key":"BFsrep31306_CR12","doi-asserted-by":"publisher","first-page":"509","DOI":"10.1081\/BIO-200039608","volume":"32","author":"P Zhang","year":"2004","unstructured":"Zhang, P. et al. Bone marrow stromal cells differentiated into functional Schwann cells in injured rats sciatic nerve. Artif. Cells.Blood.Substit. Immobil. Biotechnol. 32, 509\u2013518 (2004).","journal-title":"Artif. Cells.Blood.Substit. Immobil. Biotechnol."},{"key":"BFsrep31306_CR13","doi-asserted-by":"publisher","first-page":"537","DOI":"10.1016\/j.expneurol.2010.01.022","volume":"223","author":"S Wakao","year":"2010","unstructured":"Wakao, S. et al. Long-term observation of auto-cell transplantation in non-human primate reveals safety and efficiency of bone marrow stromal cell-derived Schwann cells in peripheral nerve regeneration. Exp. Neurol. 223, 537\u2013547 (2010).","journal-title":"Exp. Neurol."},{"key":"BFsrep31306_CR14","doi-asserted-by":"publisher","first-page":"179","DOI":"10.1177\/000348941212100307","volume":"121","author":"R Salomone","year":"2012","unstructured":"Salomone, R. et al. Assessment of a neurophysiological model of the mandibular branch of the facial nerve in rats by electromyography. Ann. Otol. Rhinol. Laryngol. 121, 179\u2013184 (2012).","journal-title":"Ann. Otol. Rhinol. Laryngol."},{"key":"BFsrep31306_CR15","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1016\/j.brainres.2009.01.056","volume":"1262","author":"J Wang","year":"2009","unstructured":"Wang, J., Ding, F., Gu, Y., Liu, J. & Gu, X. Bone marrow mesenchymal stem cells promote cell proliferation and neurotrophic function of Schwann cells in vitro and in vivo . Brain.Res. 1262, 7\u201315 (2009).","journal-title":"Brain.Res."},{"key":"BFsrep31306_CR16","doi-asserted-by":"publisher","first-page":"1264","DOI":"10.1089\/ten.tea.2011.0491","volume":"18","author":"S Marconi","year":"2012","unstructured":"Marconi, S. et al. Human adipose-derived mesenchymal stem cells systemically injected promote peripheral nerve regeneration in the mouse model of sciatic crush. Tissue.Eng. Part.A 18, 1264\u20131272 (2012).","journal-title":"Tissue.Eng. Part.A"},{"key":"BFsrep31306_CR17","doi-asserted-by":"publisher","first-page":"1357","DOI":"10.3171\/2012.2.JNS111360","volume":"116","author":"DY Yang","year":"2012","unstructured":"Yang, D. Y. et al. Dual regeneration of muscle and nerve by intravenous administration of human amniotic fluid-derived mesenchymal stem cells regulated by stromal cell-derived factor-1alpha in a sciatic nerve injury model. J. Neurosurg. 116, 1357\u20131367 (2012).","journal-title":"J. Neurosurg."},{"key":"BFsrep31306_CR18","doi-asserted-by":"publisher","first-page":"86","DOI":"10.1097\/MOT.0b013e328334f074","volume":"15","author":"SJ Hong","year":"2010","unstructured":"Hong, S. J., Traktuev, D. O. & March, K. L. Therapeutic potential of adipose-derived stem cells in vascular growth and tissue repair. Curr. Opin. Organ. Transplant. 15, 86\u201391 (2010).","journal-title":"Curr. Opin. Organ. Transplant"},{"key":"BFsrep31306_CR19","doi-asserted-by":"publisher","first-page":"241","DOI":"10.1136\/ard.2008.101881","volume":"69","author":"E Gonzalez-Rey","year":"2010","unstructured":"Gonzalez-Rey, E. et al. Human adipose-derived mesenchymal stem cells reduce inflammatory and T cell responses and induce regulatory T cells in vitro in rheumatoid arthritis. Ann. Rheum. Dis. 69, 241\u2013248 (2010).","journal-title":"Ann. Rheum. Dis."},{"key":"BFsrep31306_CR20","doi-asserted-by":"publisher","first-page":"389","DOI":"10.1097\/01.TP.0000045055.63901.A9","volume":"75","author":"WT Tse","year":"2003","unstructured":"Tse, W. T., Pendleton, J. D., Beyer, W. M., Egalka, M. C. & Guinan, E. C. Suppression of allogeneic T-cell proliferation by human marrow stromal cells: implications in transplantation. Transplantation 75, 389\u2013397 (2003).","journal-title":"Transplantation"},{"key":"BFsrep31306_CR21","doi-asserted-by":"publisher","first-page":"150","DOI":"10.1016\/j.cellimm.2009.06.010","volume":"259","author":"KH Yoo","year":"2009","unstructured":"Yoo, K. H. et al. Comparison of immunomodulatory properties of mesenchymal stem cells derived from adult human tissues. Cell. Immunol. 259, 150\u2013156 (2009).","journal-title":"Cell. Immunol."},{"key":"BFsrep31306_CR22","doi-asserted-by":"publisher","first-page":"2770","DOI":"10.1089\/scd.2012.0176","volume":"21","author":"CS Lin","year":"2012","unstructured":"Lin, C. S., Lin, G. & Lue, T. F. Allogeneic and xenogeneic transplantation of adipose-derived stem cells in immunocompetent recipients without immunosuppressants. Stem.Cells.Dev. 21, 2770\u20132778 (2012).","journal-title":"Stem.Cells.Dev."},{"key":"BFsrep31306_CR23","doi-asserted-by":"publisher","first-page":"3358","DOI":"10.1016\/j.transproceed.2007.08.103","volume":"39","author":"B Fang","year":"2007","unstructured":"Fang, B., Song, Y., Liao, L., Zhang, Y. & Zhao, R. C. Favorable response to human adipose tissue-derived mesenchymal stem cells in steroid-refractory acute graft-versus-host disease. Transplant. Proc. 39, 3358\u20133362 (2007).","journal-title":"Transplant. Proc."},{"key":"BFsrep31306_CR24","doi-asserted-by":"publisher","first-page":"814","DOI":"10.1111\/j.1399-3046.2007.00780.x","volume":"11","author":"B Fang","year":"2007","unstructured":"Fang, B. et al. Human adipose tissue-derived mesenchymal stromal cells as salvage therapy for treatment of severe refractory acute graft-vs.-host disease in two children. Pediatr. Transplant. 11, 814\u2013817 (2007).","journal-title":"Pediatr. Transplant."},{"key":"BFsrep31306_CR25","doi-asserted-by":"publisher","first-page":"261","DOI":"10.1007\/s00277-008-0599-0","volume":"88","author":"B Fang","year":"2009","unstructured":"Fang, B. et al. Mesenchymal stem cells for the treatment of refractory pure red cell aplasia after major ABO-incompatible hematopoietic stem cell transplantation. Ann. Hematol. 88, 261\u2013266 (2009).","journal-title":"Ann. Hematol."},{"key":"BFsrep31306_CR26","doi-asserted-by":"publisher","first-page":"1710","DOI":"10.1016\/j.transproceed.2007.02.091","volume":"39","author":"B Fang","year":"2007","unstructured":"Fang, B., Song, Y., Zhao, R. C., Han, Q. & Lin, Q. Using human adipose tissue-derived mesenchymal stem cells as salvage therapy for hepatic graft-versus-host disease resembling acute hepatitis. Transplant. Proc. 39, 1710\u20131713 (2007).","journal-title":"Transplant. Proc."},{"key":"BFsrep31306_CR27","doi-asserted-by":"publisher","first-page":"269","DOI":"10.1007\/s12015-010-9193-7","volume":"7","author":"B Lindroos","year":"2011","unstructured":"Lindroos, B., Suuronen, R. & Miettinen, S. The potential of adipose stem cells in regenerative medicine. Stem.Cell. Rev. 7, 269\u2013291 (2011).","journal-title":"Stem.Cell. Rev."},{"key":"BFsrep31306_CR28","doi-asserted-by":"publisher","first-page":"5340","DOI":"10.1182\/blood-2008-04-154567","volume":"113","author":"BJ Capoccia","year":"2009","unstructured":"Capoccia, B. J. et al. Revascularization of ischemic limbs after transplantation of human bone marrow cells with high aldehyde dehydrogenase activity. Blood 113, 5340\u20135351 (2009).","journal-title":"Blood"},{"key":"BFsrep31306_CR29","doi-asserted-by":"publisher","first-page":"1297","DOI":"10.1089\/scd.2010.0466","volume":"20","author":"JC Ra","year":"2011","unstructured":"Ra, J. C. et al. Safety of intravenous infusion of human adipose tissue-derived mesenchymal stem cells in animals and humans. Stem.Cells.Dev. 20, 1297\u20131308 (2011).","journal-title":"Stem.Cells.Dev."},{"key":"BFsrep31306_CR30","doi-asserted-by":"publisher","first-page":"214","DOI":"10.1016\/j.jss.2010.02.015","volume":"164","author":"AM Abarbanell","year":"2010","unstructured":"Abarbanell, A. M. Mesenchymal stem cells\u2013a new approach to intestinal ischemia\/reperfusion injury? J. Surg. Res. 164, 214\u2013215 (2010).","journal-title":"J. Surg. Res."},{"key":"BFsrep31306_CR31","doi-asserted-by":"publisher","first-page":"234","DOI":"10.1097\/TP.0b013e318298f9fa","volume":"96","author":"M Franquesa","year":"2013","unstructured":"Franquesa, M. et al. Mesenchymal Stem Cells in Solid Organ Transplantation (MiSOT) Fourth Meeting: lessons learned from first clinical trials. Transplantation 96, 234\u2013238 (2013).","journal-title":"Transplantation"},{"key":"BFsrep31306_CR32","doi-asserted-by":"publisher","first-page":"132","DOI":"10.1900\/RDS.2010.7.132","volume":"7","author":"V Sordi","year":"2010","unstructured":"Sordi, V. & Piemonti, L. Mesenchymal stem cells as feeder cells for pancreatic islet transplants. Rev. Diabet. Stud. 7, 132\u2013143 (2010).","journal-title":"Rev. Diabet. Stud."},{"key":"BFsrep31306_CR33","doi-asserted-by":"publisher","first-page":"1579","DOI":"10.1016\/S0140-6736(08)60690-X","volume":"371","author":"K Le Blanc","year":"2008","unstructured":"Le Blanc, K. et al. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet 371, 1579\u20131586 (2008).","journal-title":"Lancet"},{"key":"BFsrep31306_CR34","doi-asserted-by":"publisher","first-page":"1517","DOI":"10.1089\/ten.tea.2010.0460","volume":"17","author":"W Gruenloh","year":"2011","unstructured":"Gruenloh, W. et al. Characterization and in vivo testing of mesenchymal stem cells derived from human embryonic stem cells. Tissue.Eng. Part A 17, 1517\u20131525 (2011).","journal-title":"Tissue.Eng. Part A"},{"key":"BFsrep31306_CR35","doi-asserted-by":"publisher","first-page":"1025","DOI":"10.2217\/rme.15.63","volume":"10","author":"E Carvalho","year":"2015","unstructured":"Carvalho, E., Verma, P., Hourigan, K. & Banerjee, R. Myocardial infarction: stem cell transplantation for cardiac regeneration. Regen. Med. 10, 1025\u20131043 (2015).","journal-title":"Regen. Med."},{"key":"BFsrep31306_CR36","doi-asserted-by":"publisher","first-page":"1815","DOI":"10.1182\/blood-2004-04-1559","volume":"105","author":"S Aggarwal","year":"2005","unstructured":"Aggarwal, S. & Pittenger, M. F. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105, 1815\u20131822 (2005).","journal-title":"Blood"},{"key":"BFsrep31306_CR37","doi-asserted-by":"publisher","first-page":"2020","DOI":"10.1016\/j.arthro.2013.09.074","volume":"29","author":"KL Wong","year":"2013","unstructured":"Wong, K. L. et al. Injectable cultured bone marrow-derived mesenchymal stem cells in varus knees with cartilage defects undergoing high tibial osteotomy: a prospective, randomized controlled clinical trial with 2 years\u2019 follow-up. Arthroscopy 29, 2020\u20132028 (2013).","journal-title":"Arthroscopy"},{"key":"BFsrep31306_CR38","doi-asserted-by":"publisher","first-page":"225","DOI":"10.1007\/s11255-009-9659-1","volume":"43","author":"AV Vanikar","year":"2011","unstructured":"Vanikar, A. V. et al. Effect of co-transplantation of mesenchymal stem cells and hematopoietic stem cells as compared to hematopoietic stem cell transplantation alone in renal transplantation to achieve donor hypo-responsiveness. Int. Urol. Nephrol. 43, 225\u2013232 (2011).","journal-title":"Int. Urol. Nephrol."},{"key":"BFsrep31306_CR39","doi-asserted-by":"publisher","first-page":"85","DOI":"10.1111\/jgh.12029","volume":"28","author":"L Wang","year":"2013","unstructured":"Wang, L. et al. Pilot study of umbilical cord-derived mesenchymal stem cell transfusion in patients with primary biliary cirrhosis. J. Gastroenterol. Hepatol. 28 Suppl 1, 85\u201392 (2013).","journal-title":"J. Gastroenterol. Hepatol."},{"key":"BFsrep31306_CR40","doi-asserted-by":"publisher","first-page":"1308","DOI":"10.1038\/mt.2008.93","volume":"16","author":"G Bauer","year":"2008","unstructured":"Bauer, G. et al. In vivo biosafety model to assess the risk of adverse events from retroviral and lentiviral vectors. Mol. Ther. 16, 1308\u20131315 (2008).","journal-title":"Mol. Ther."},{"key":"BFsrep31306_CR41","doi-asserted-by":"crossref","unstructured":"Lyons, A. B. & Doherty, K. V. Flow cytometric analysis of cell division by dye dilution. Curr. Protoc. Cytom Chapter 9, Unit 9.11 (2004).","DOI":"10.1002\/0471142956.cy0911s27"},{"key":"BFsrep31306_CR42","doi-asserted-by":"publisher","first-page":"915","DOI":"10.1016\/j.bbrc.2007.05.212","volume":"359","author":"S Shimizu","year":"2007","unstructured":"Shimizu, S. et al. Peripheral nerve regeneration by the in vitro differentiated-human bone marrow stromal cells with Schwann cell property. Biochem. Biophys. Res. Commun. 359, 915\u2013920 (2007).","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"BFsrep31306_CR43","doi-asserted-by":"publisher","first-page":"1377","DOI":"10.1016\/j.cell.2007.04.028","volume":"129","author":"Y Takashima","year":"2007","unstructured":"Takashima, Y. et al. Neuroepithelial cells supply an initial transient wave of MSC differentiation. Cell 129, 1377\u20131388 (2007).","journal-title":"Cell"},{"key":"BFsrep31306_CR44","doi-asserted-by":"publisher","first-page":"e84206","DOI":"10.1371\/journal.pone.0084206","volume":"8","author":"Y Sowa","year":"2013","unstructured":"Sowa, Y. et al. Adipose stromal cells contain phenotypically distinct adipogenic progenitors derived from neural crest. PLoS.One 8, e84206 (2013).","journal-title":"PLoS.One"},{"key":"BFsrep31306_CR45","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1093\/jnen\/64.1.37","volume":"64","author":"T Kamada","year":"2005","unstructured":"Kamada, T. et al. Transplantation of bone marrow stromal cell-derived Schwann cells promotes axonal regeneration and functional recovery after complete transection of adult rat spinal cord. J. Neuropathol. Exp. Neurol. 64, 37\u201345 (2005).","journal-title":"J. Neuropathol. Exp. Neurol."},{"key":"BFsrep31306_CR46","doi-asserted-by":"publisher","first-page":"192","DOI":"10.1016\/j.brainres.2009.07.087","volume":"1295","author":"T Furuya","year":"2009","unstructured":"Furuya, T. et al. Treatment of rat spinal cord injury with a Rho-kinase inhibitor and bone marrow stromal cell transplantation. Brain.Res. 1295, 192\u2013202 (2009).","journal-title":"Brain.Res."},{"key":"BFsrep31306_CR47","doi-asserted-by":"publisher","first-page":"e0147184","DOI":"10.1371\/journal.pone.0147184","volume":"11","author":"Y Xu","year":"2016","unstructured":"Xu, Y. et al. A Silk Fibroin\/Collagen Nerve Scaffold Seeded with a Co-Culture of Schwann Cells and Adipose-Derived Stem Cells for Sciatic Nerve Regeneration. PLoS. One 11, e0147184 (2016).","journal-title":"PLoS. One"},{"key":"BFsrep31306_CR48","doi-asserted-by":"publisher","first-page":"973","DOI":"10.1097\/NEN.0b013e3181eff6dc","volume":"69","author":"D Matsuse","year":"2010","unstructured":"Matsuse, D. et al. Human umbilical cord-derived mesenchymal stromal cells differentiate into functional Schwann cells that sustain peripheral nerve regeneration. J. Neuropathol. Exp. Neurol. 69, 973\u2013985 (2010).","journal-title":"J. Neuropathol. Exp. Neurol."},{"key":"BFsrep31306_CR49","doi-asserted-by":"publisher","first-page":"1392","DOI":"10.1002\/jnr.23002","volume":"90","author":"K Tomita","year":"2012","unstructured":"Tomita, K., Madura, T., Mantovani, C. & Terenghi, G. Differentiated adipose-derived stem cells promote myelination and enhance functional recovery in a rat model of chronic denervation. J. Neurosci. Res. 90, 1392\u20131402 (2012).","journal-title":"J. Neurosci. Res."},{"key":"BFsrep31306_CR50","doi-asserted-by":"publisher","first-page":"1016","DOI":"10.1002\/jcb.22204","volume":"107","author":"Y Amoh","year":"2009","unstructured":"Amoh, Y. et al. Human hair follicle pluripotent stem (hfPS) cells promote regeneration of peripheral-nerve injury: an advantageous alternative to ES and iPS cells. J. Cell. Biochem. 107, 1016\u20131020 (2009).","journal-title":"J. Cell. Biochem."},{"key":"BFsrep31306_CR51","doi-asserted-by":"publisher","first-page":"828","DOI":"10.4103\/1673-5374.131599","volume":"9","author":"Y Ni","year":"2014","unstructured":"Ni, Y. et al. miR-21 promotes the differentiation of hair follicle-derived neural crest stem cells into Schwann cells. Neural.Regen. Res. 9, 828\u2013836 (2014).","journal-title":"Neural.Regen. Res"},{"key":"BFsrep31306_CR52","doi-asserted-by":"publisher","first-page":"E2011","DOI":"10.1002\/hed.24371","volume":"38","author":"A Batioglu-Karaaltin","year":"2016","unstructured":"Batioglu-Karaaltin, A. et al. Human olfactory stem cells for injured facial nerve reconstruction in a rat model. Head.Neck 38 Suppl 1, E2011\u201320 (2016).","journal-title":"Head.Neck"},{"key":"BFsrep31306_CR53","doi-asserted-by":"publisher","first-page":"281","DOI":"10.1515\/revneuro-2014-0065","volume":"26","author":"D Duan","year":"2015","unstructured":"Duan, D. & Lu, M. Olfactory mucosa: a rich source of cell therapy for central nervous system repair. Rev. Neurosci. 26, 281\u2013293 (2015).","journal-title":"Rev. Neurosci."},{"key":"BFsrep31306_CR54","first-page":"417","volume":"111","author":"F Dammann","year":"2014","unstructured":"Dammann, F. et al. Diagnostic imaging modalities in head and neck disease. Dtsch. Arztebl. Int. 111, 417\u2013423 (2014).","journal-title":"Dtsch. Arztebl. Int."},{"key":"BFsrep31306_CR55","doi-asserted-by":"publisher","first-page":"91","DOI":"10.1016\/j.jneumeth.2008.05.020","volume":"173","author":"A Bozkurt","year":"2008","unstructured":"Bozkurt, A. et al. CatWalk gait analysis in assessment of functional recovery after sciatic nerve injury. J. Neurosci. Methods 173, 91\u201398 (2008).","journal-title":"J. Neurosci. Methods"},{"key":"BFsrep31306_CR56","doi-asserted-by":"publisher","first-page":"351e","DOI":"10.1097\/PRS.0000000000000892","volume":"135","author":"JT Shores","year":"2015","unstructured":"Shores, J. T., Brandacher, G. & Lee, W. P. Hand and upper extremity transplantation: an update of outcomes in the worldwide experience. Plast. Reconstr. Surg. 135, 351e\u201360e (2015).","journal-title":"Plast. Reconstr. Surg."},{"key":"BFsrep31306_CR57","doi-asserted-by":"publisher","first-page":"627","DOI":"10.1097\/TP.0b013e318184ca6a","volume":"86","author":"B Swearingen","year":"2008","unstructured":"Swearingen, B. et al. Science of composite tissue allotransplantation. Transplantation 86, 627\u2013635 (2008).","journal-title":"Transplantation"},{"key":"BFsrep31306_CR58","doi-asserted-by":"publisher","first-page":"2451","DOI":"10.1056\/NEJMoa072828","volume":"357","author":"JM Dubernard","year":"2007","unstructured":"Dubernard, J. M. et al. Outcomes 18 months after the first human partial face transplantation. N. Engl. J. Med. 357, 2451\u20132460 (2007).","journal-title":"N. Engl. J. Med."},{"key":"BFsrep31306_CR59","doi-asserted-by":"publisher","first-page":"34","DOI":"10.1186\/scrt34","volume":"1","author":"BA Bunnell","year":"2010","unstructured":"Bunnell, B. A., Betancourt, A. M. & Sullivan, D. E. New concepts on the immune modulation mediated by mesenchymal stem cells. Stem. Cell. Res. Ther. 1, 34 (2010).","journal-title":"Stem. Cell. Res. Ther."},{"key":"BFsrep31306_CR60","doi-asserted-by":"publisher","first-page":"939","DOI":"10.1038\/mt.2009.62","volume":"17","author":"DJ Prockop","year":"2009","unstructured":"Prockop, D. J. Repair of tissues by adult stem\/progenitor cells (MSCs): controversies, myths, and changing paradigms. Mol. Ther. 17, 939\u2013946 (2009).","journal-title":"Mol. Ther."},{"key":"BFsrep31306_CR61","doi-asserted-by":"crossref","first-page":"585","DOI":"10.1002\/stem.269","volume":"28","author":"HK Salem","year":"2010","unstructured":"Salem, H. K. & Thiemermann, C. Mesenchymal stromal cells: current understanding and clinical status. Stem.Cells 28, 585\u2013596 (2010).","journal-title":"Stem.Cells"},{"key":"BFsrep31306_CR62","doi-asserted-by":"publisher","first-page":"1855","DOI":"10.4049\/jimmunol.179.3.1855","volume":"179","author":"N Gupta","year":"2007","unstructured":"Gupta, N. et al. Intrapulmonary delivery of bone marrow-derived mesenchymal stem cells improves survival and attenuates endotoxin-induced acute lung injury in mice. J. Immunol. 179, 1855\u20131863 (2007).","journal-title":"J. Immunol."},{"key":"BFsrep31306_CR63","doi-asserted-by":"publisher","first-page":"569","DOI":"10.1517\/14712598.8.5.569","volume":"8","author":"SS Iyer","year":"2008","unstructured":"Iyer, S. S. & Rojas, M. Anti-inflammatory effects of mesenchymal stem cells: novel concept for future therapies. Expert. Opin. Biol. Ther. 8, 569\u2013581 (2008).","journal-title":"Expert. Opin. Biol. Ther."},{"key":"BFsrep31306_CR64","doi-asserted-by":"publisher","first-page":"4120","DOI":"10.1182\/blood-2004-02-0586","volume":"105","author":"XX Jiang","year":"2005","unstructured":"Jiang, X. X. et al. Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood 105, 4120\u20134126 (2005).","journal-title":"Blood"},{"key":"BFsrep31306_CR65","doi-asserted-by":"publisher","first-page":"e269","DOI":"10.1371\/journal.pmed.0040269","volume":"4","author":"SH Mei","year":"2007","unstructured":"Mei, S. H. et al. Prevention of LPS-induced acute lung injury in mice by mesenchymal stem cells overexpressing angiopoietin 1. PLoS. Med. 4, e269 (2007).","journal-title":"PLoS. Med."},{"key":"BFsrep31306_CR66","doi-asserted-by":"publisher","first-page":"8407","DOI":"10.1073\/pnas.1432929100","volume":"100","author":"LA Ortiz","year":"2003","unstructured":"Ortiz, L. A. et al. Mesenchymal stem cell engraftment in lung is enhanced in response to bleomycin exposure and ameliorates its fibrotic effects. Proc. Natl. Acad. Sci. USA 100, 8407\u20138411 (2003).","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"BFsrep31306_CR67","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1165\/rcmb.2004-0330OC","volume":"33","author":"M Rojas","year":"2005","unstructured":"Rojas, M. et al. Bone marrow-derived mesenchymal stem cells in repair of the injured lung. Am. J. Respir. Cell.Mol. Biol. 33, 145\u2013152 (2005).","journal-title":"Am. J. Respir. Cell.Mol. Biol."},{"key":"BFsrep31306_CR68","doi-asserted-by":"publisher","first-page":"120","DOI":"10.1002\/glia.20025","volume":"47","author":"E Udina","year":"2004","unstructured":"Udina, E. et al. FK506 enhances regeneration of axons across long peripheral nerve gaps repaired with collagen guides seeded with allogeneic Schwann cells. Glia 47, 120\u2013129 (2004).","journal-title":"Glia"},{"key":"BFsrep31306_CR69","doi-asserted-by":"publisher","first-page":"602","DOI":"10.3171\/jns.2006.105.4.602","volume":"105","author":"C Auba","year":"2006","unstructured":"Auba, C., Hontanilla, B., Arcocha, J. & Gorria, O. Peripheral nerve regeneration through allografts compared with autografts in FK506-treated monkeys. J. Neurosurg. 105, 602\u2013609 (2006).","journal-title":"J. Neurosurg."},{"key":"BFsrep31306_CR70","doi-asserted-by":"publisher","first-page":"1832","DOI":"10.1097\/01.PRS.0000091167.27303.18","volume":"112","author":"RK Yang","year":"2003","unstructured":"Yang, R. K. et al. Dose-dependent effects of FK506 on neuroregeneration in a rat model. Plast. Reconstr. Surg. 112, 1832\u20131840 (2003).","journal-title":"Plast. Reconstr. Surg."},{"key":"BFsrep31306_CR71","doi-asserted-by":"publisher","first-page":"537","DOI":"10.1089\/neu.2006.23.537","volume":"23","author":"FP Hamers","year":"2006","unstructured":"Hamers, F. P., Koopmans, G. C. & Joosten, E. A. CatWalk-assisted gait analysis in the assessment of spinal cord injury. J. Neurotrauma 23, 537\u2013548 (2006).","journal-title":"J. Neurotrauma"},{"key":"BFsrep31306_CR72","doi-asserted-by":"publisher","first-page":"385","DOI":"10.1002\/mus.22303","volume":"45","author":"P Devesa","year":"2012","unstructured":"Devesa, P. et al. Growth hormone treatment enhances the functional recovery of sciatic nerves after transection and repair. Muscle.Nerve 45, 385\u2013392 (2012).","journal-title":"Muscle.Nerve"},{"key":"BFsrep31306_CR73","doi-asserted-by":"publisher","first-page":"238","DOI":"10.1179\/1743132812Y.0000000003","volume":"34","author":"B Caner","year":"2012","unstructured":"Caner, B. et al. Intraperitoneal administration of CDP-choline or a combination of cytidine plus choline improves nerve regeneration and functional recovery in a rat model of sciatic nerve injury. Neurol. Res. 34, 238\u2013245 (2012).","journal-title":"Neurol. Res."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/srep31306.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/srep31306","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/srep31306.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,1,5]],"date-time":"2023-01-05T05:19:06Z","timestamp":1672895946000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/srep31306"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016,8,11]]},"references-count":73,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2016,8,25]]}},"alternative-id":["BFsrep31306"],"URL":"https:\/\/doi.org\/10.1038\/srep31306","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2016,8,11]]},"assertion":[{"value":"12 January 2016","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"18 July 2016","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"11 August 2016","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing financial interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"31306"}}