{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,27]],"date-time":"2026-09-27T05:41:34Z","timestamp":1790487694233,"version":"4.1.0"},"reference-count":51,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2017,10,3]],"date-time":"2017-10-03T00:00:00Z","timestamp":1506988800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2017,10,3]],"date-time":"2017-10-03T00:00:00Z","timestamp":1506988800000},"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>The current gold standard treatment for peripheral nerve injury is nerve grafting but this has disadvantages such as donor site morbidity. New techniques focus on replacing these grafts with nerve conduits enhanced with growth factors and\/or various cell types such as mesenchymal stem cells (MSCs). Dental-MSCs (D-MSCs) including stem cells obtained from apical papilla (SCAP), dental pulp stem cells (DPSC), and periodontal ligament stem cells (PDLSC) are potential sources of MSCs for nerve repair. Here we present the characterization of various D-MSCs from the same human donors for peripheral nerve regeneration. SCAP, DPSC and PDLSC expressed <jats:italic>BDNF<\/jats:italic>, <jats:italic>GDNF<\/jats:italic>, <jats:italic>NGF<\/jats:italic>, <jats:italic>NTF3<\/jats:italic>, <jats:italic>ANGPT1<\/jats:italic> and <jats:italic>VEGFA<\/jats:italic> growth factor transcripts. Conditioned media from D-MSCs enhanced neurite outgrowth in an <jats:italic>in vitro<\/jats:italic> assay. Application of neutralizing antibodies showed that brain derived neurotrophic factor plays an important mechanistic role by which the D-MSCs stimulate neurite outgrowth. SCAP, DPSC and PDLSC were used to treat a 10 mm nerve gap defect in a rat sciatic nerve injury model. All the stem cell types significantly enhanced axon regeneration after two weeks and showed neuroprotective effects on the dorsal root ganglia neurons. Overall the results suggested SCAP to be the optimal dental stem cell type for peripheral nerve repair.<\/jats:p>","DOI":"10.1038\/s41598-017-12969-1","type":"journal-article","created":{"date-parts":[[2017,9,27]],"date-time":"2017-09-27T10:17:24Z","timestamp":1506507444000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":128,"title":["The neurotrophic effects of different human dental mesenchymal stem cells"],"prefix":"10.1038","volume":"7","author":[{"given":"Mallappa K.","family":"Kolar","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vinay N.","family":"Itte","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2596-5936","authenticated-orcid":false,"given":"Paul J.","family":"Kingham","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lev N.","family":"Novikov","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mikael","family":"Wiberg","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1594-1738","authenticated-orcid":false,"given":"Peyman","family":"Kelk","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2017,10,3]]},"reference":[{"key":"12969_CR1","doi-asserted-by":"publisher","unstructured":"Isaacs, J. Treatment of acute peripheral nerve injuries: current concepts. J Hand Surg Am \n                           35, 491\u2013497 quiz 498, https:\/\/doi.org\/10.1016\/j.jhsa.2009.12.009 (2010).","DOI":"10.1016\/j.jhsa.2009.12.009"},{"key":"12969_CR2","first-page":"303","volume":"11","author":"M Wiberg","year":"2003","unstructured":"Wiberg, M. & Terenghi, G. Will it be possible to produce peripheral nerves? Surg Technol Int \n                           11, 303\u2013310 (2003).","journal-title":"Surg Technol Int"},{"key":"12969_CR3","doi-asserted-by":"publisher","first-page":"1503","DOI":"10.1016\/j.bjps.2008.06.041","volume":"62","author":"M Aberg","year":"2009","unstructured":"Aberg, M. et al. Clinical evaluation of a resorbable wrap-around implant as an alternative to nerve repair: a prospective, assessor-blinded, randomised clinical study of sensory, motor and functional recovery after peripheral nerve repair. J Plast Reconstr Aesthet Surg \n                           62, 1503\u20131509, https:\/\/doi.org\/10.1016\/j.bjps.2008.06.041 (2009).","journal-title":"J Plast Reconstr Aesthet Surg"},{"key":"12969_CR4","doi-asserted-by":"publisher","first-page":"116","DOI":"10.1089\/ten.teb.2011.0498","volume":"18","author":"JH Bell","year":"2012","unstructured":"Bell, J. H. & Haycock, J. W. Next generation nerve guides: materials, fabrication, growth factors, and cell delivery. Tissue Eng Part B Rev \n                           18, 116\u2013128, https:\/\/doi.org\/10.1089\/ten.TEB.2011.0498 (2012).","journal-title":"Tissue Eng Part B Rev"},{"key":"12969_CR5","doi-asserted-by":"publisher","first-page":"202","DOI":"10.1098\/rsif.2011.0438","volume":"9","author":"W Daly","year":"2012","unstructured":"Daly, W., Yao, L., Zeugolis, D., Windebank, A. & Pandit, A. A biomaterials approach to peripheral nerve regeneration: bridging the peripheral nerve gap and enhancing functional recovery. J R Soc Interface \n                           9, 202\u2013221, https:\/\/doi.org\/10.1098\/rsif.2011.0438 (2012).","journal-title":"J R Soc Interface"},{"key":"12969_CR6","doi-asserted-by":"publisher","first-page":"40","DOI":"10.1089\/ten.teb.2011.0240","volume":"18","author":"AR Nectow","year":"2012","unstructured":"Nectow, A. R., Marra, K. G. & Kaplan, D. L. Biomaterials for the development of peripheral nerve guidance conduits. Tissue Eng Part B Rev \n                           18, 40\u201350, https:\/\/doi.org\/10.1089\/ten.TEB.2011.0240 (2012).","journal-title":"Tissue Eng Part B Rev"},{"key":"12969_CR7","doi-asserted-by":"publisher","first-page":"741","DOI":"10.1089\/scd.2013.0396","volume":"23","author":"PJ Kingham","year":"2014","unstructured":"Kingham, P. J., Kolar, M. K., Novikova, L. N., Novikov, L. N. & Wiberg, M. Stimulating the neurotrophic and angiogenic properties of human adipose-derived stem cells enhances nerve repair. 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Fibrin conduit supplemented with human mesenchymal stem cells and immunosuppressive treatment enhances regeneration after peripheral nerve injury. Neurosci Lett \n                           516, 171\u2013176, https:\/\/doi.org\/10.1016\/j.neulet.2012.03.041 (2012).","journal-title":"Neurosci Lett"},{"key":"12969_CR10","doi-asserted-by":"publisher","first-page":"31","DOI":"10.1159\/000368188","volume":"200","author":"S Wakao","year":"2014","unstructured":"Wakao, S., Matsuse, D. & Dezawa, M. Mesenchymal Stem Cells as a Source of Schwann Cells: Their Anticipated Use in Peripheral Nerve Regeneration. Cells Tissues Organs \n                           200, 31\u201341 (2014).","journal-title":"Cells Tissues Organs"},{"key":"12969_CR11","doi-asserted-by":"publisher","first-page":"399","DOI":"10.4252\/wjsc.v7.i2.399","volume":"7","author":"MT Saito","year":"2015","unstructured":"Saito, M. T., Silverio, K. G., Casati, M. Z., Sallum, E. A. & Nociti, F. H. Jr Tooth-derived stem cells: Update and perspectives. World J Stem Cells \n                           7, 399\u2013407, https:\/\/doi.org\/10.4252\/wjsc.v7.i2.399 (2015).","journal-title":"World J Stem Cells"},{"key":"12969_CR12","doi-asserted-by":"publisher","first-page":"307","DOI":"10.4103\/1305-7456.137631","volume":"8","author":"D Ponnaiyan","year":"2014","unstructured":"Ponnaiyan, D. & Jegadeesan, V. Comparison of phenotype and differentiation marker gene expression profiles in human dental pulp and bone marrow mesenchymal stem cells. Eur J Dent \n                           8, 307\u2013313, https:\/\/doi.org\/10.4103\/1305-7456.137631 (2014).","journal-title":"Eur J Dent"},{"key":"12969_CR13","doi-asserted-by":"publisher","first-page":"371","DOI":"10.1007\/s00774-014-0601-y","volume":"33","author":"OG Davies","year":"2015","unstructured":"Davies, O. G., Cooper, P. R., Shelton, R. M., Smith, A. J. & Scheven, B. A. A comparison of the in vitro mineralisation and dentinogenic potential of mesenchymal stem cells derived from adipose tissue, bone marrow and dental pulp. J Bone Miner Metab \n                           33, 371\u2013382, https:\/\/doi.org\/10.1007\/s00774-014-0601-y (2015).","journal-title":"J Bone Miner Metab"},{"key":"12969_CR14","doi-asserted-by":"publisher","first-page":"792","DOI":"10.1177\/0022034509340867","volume":"88","author":"GT Huang","year":"2009","unstructured":"Huang, G. T., Gronthos, S. & Shi, S. Mesenchymal stem cells derived from dental tissues vs. those from other sources: their biology and role in regenerative medicine. J Dent Res \n                           88, 792\u2013806, https:\/\/doi.org\/10.1177\/0022034509340867 (2009).","journal-title":"J Dent Res"},{"key":"12969_CR15","doi-asserted-by":"publisher","first-page":"1634","DOI":"10.1096\/fj.13-243980","volume":"28","author":"W Martens","year":"2014","unstructured":"Martens, W. et al. Human dental pulp stem cells can differentiate into Schwann cells and promote and guide neurite outgrowth in an aligned tissue-engineered collagen construct in vitro. FASEB J \n                           28, 1634\u20131643, https:\/\/doi.org\/10.1096\/fj.13-243980 (2014).","journal-title":"FASEB J"},{"key":"12969_CR16","doi-asserted-by":"publisher","first-page":"4554","DOI":"10.1002\/jbm.a.35119","volume":"102","author":"MH Beigi","year":"2014","unstructured":"Beigi, M. H. et al. In vivo integration of poly(epsilon-caprolactone)\/gelatin nanofibrous nerve guide seeded with teeth derived stem cells for peripheral nerve regeneration. J Biomed Mater Res A \n                           102, 4554\u20134567, https:\/\/doi.org\/10.1002\/jbm.a.35119 (2014).","journal-title":"J Biomed Mater Res A"},{"key":"12969_CR17","doi-asserted-by":"publisher","first-page":"2827","DOI":"10.3969\/j.issn.1673-5374.2013.30.005","volume":"8","author":"B Li","year":"2013","unstructured":"Li, B. et al. Human periodontal ligament stem cells repair mental nerve injury. Neural Regen Res \n                           8, 2827\u20132837, https:\/\/doi.org\/10.3969\/j.issn.1673-5374.2013.30.005 (2013).","journal-title":"Neural Regen Res"},{"key":"12969_CR18","doi-asserted-by":"publisher","DOI":"10.1155\/2016\/8102478","volume":"2016","author":"M Ahmed Nel","year":"2016","unstructured":"Ahmed Nel, M., Murakami, M., Hirose, Y. & Nakashima, M. Therapeutic Potential of Dental Pulp Stem Cell Secretome for Alzheimer\u2019s Disease Treatment: An In Vitro Study. Stem Cells Int \n                           2016, 8102478, https:\/\/doi.org\/10.1155\/2016\/8102478 (2016).","journal-title":"Stem Cells Int"},{"key":"12969_CR19","first-page":"21","volume":"6","author":"A Esmaeili","year":"2014","unstructured":"Esmaeili, A., Alifarja, S., Nourbakhsh, N. & Talebi, A. Messenger RNA Expression Patterns of Neurotrophins during Transdifferentiation of Stem Cells from Human-Exfoliated Deciduous Teeth into Neural-like Cells. Avicenna J Med Biotechnol \n                           6, 21\u201326 (2014).","journal-title":"Avicenna J Med Biotechnol"},{"key":"12969_CR20","doi-asserted-by":"publisher","first-page":"3089","DOI":"10.1089\/ten.tea.2013.0347","volume":"20","author":"JF de Almeida","year":"2014","unstructured":"de Almeida, J. F., Chen, P., Henry, M. A. & Diogenes, A. Stem cells of the apical papilla regulate trigeminal neurite outgrowth and targeting through a BDNF-dependent mechanism. Tissue Eng Part A \n                           20, 3089\u20133100, https:\/\/doi.org\/10.1089\/ten.TEA.2013.0347 (2014).","journal-title":"Tissue Eng Part A"},{"key":"12969_CR21","doi-asserted-by":"publisher","DOI":"10.1002\/14651858.CD004345.pub2","volume":"7","author":"P Coulthard","year":"2014","unstructured":"Coulthard, P. et al. Surgical techniques for the removal of mandibular wisdom teeth. Cochrane Database Syst Rev \n                           7, CD004345, https:\/\/doi.org\/10.1002\/14651858.CD004345.pub2 (2014).","journal-title":"Cochrane Database Syst Rev"},{"key":"12969_CR22","doi-asserted-by":"publisher","first-page":"551","DOI":"10.1038\/nature13536","volume":"513","author":"N Kaukua","year":"2014","unstructured":"Kaukua, N. et al. Glial origin of mesenchymal stem cells in a tooth model system. Nature \n                           513, 551\u2013554, https:\/\/doi.org\/10.1038\/nature13536 (2014).","journal-title":"Nature"},{"key":"12969_CR23","doi-asserted-by":"publisher","first-page":"200","DOI":"10.1002\/bdrc.20012","volume":"72","author":"I Miletich","year":"2004","unstructured":"Miletich, I. & Sharpe, P. T. Neural crest contribution to mammalian tooth formation. Birth Defects Res C Embryo Today \n                           72, 200\u2013212, https:\/\/doi.org\/10.1002\/bdrc.20012 (2004).","journal-title":"Birth Defects Res C Embryo Today"},{"key":"12969_CR24","doi-asserted-by":"publisher","first-page":"6541","DOI":"10.1073\/pnas.1137104100","volume":"100","author":"TA Mitsiadis","year":"2003","unstructured":"Mitsiadis, T. A., Cheraud, Y., Sharpe, P. & Fontaine-Perus, J. Development of teeth in chick embryos after mouse neural crest transplantations. Proc Natl Acad Sci USA \n                           100, 6541\u20136545, https:\/\/doi.org\/10.1073\/pnas.1137104100 (2003).","journal-title":"Proc Natl Acad Sci USA"},{"key":"12969_CR25","doi-asserted-by":"publisher","first-page":"80","DOI":"10.1172\/JCI59251","volume":"122","author":"K Sakai","year":"2012","unstructured":"Sakai, K. et al. Human dental pulp-derived stem cells promote locomotor recovery after complete transection of the rat spinal cord by multiple neuro-regenerative mechanisms. J Clin Invest \n                           122, 80\u201390, https:\/\/doi.org\/10.1172\/JCI59251 (2012).","journal-title":"J Clin Invest"},{"key":"12969_CR26","doi-asserted-by":"publisher","first-page":"415","DOI":"10.1002\/jcp.22050","volume":"223","author":"G Ding","year":"2010","unstructured":"Ding, G. et al. Effect of cryopreservation on biological and immunological properties of stem cells from apical papilla. J Cell Physiol \n                           223, 415\u2013422, https:\/\/doi.org\/10.1002\/jcp.22050 (2010).","journal-title":"J Cell Physiol"},{"key":"12969_CR27","doi-asserted-by":"publisher","first-page":"315","DOI":"10.1080\/14653240600855905","volume":"8","author":"M Dominici","year":"2006","unstructured":"Dominici, M. et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. 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Stem Cells Transl Med \n                           3, 375\u2013386, https:\/\/doi.org\/10.5966\/sctm.2013-0074 (2014).","journal-title":"Stem Cells Transl Med"},{"key":"12969_CR32","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0109305","volume":"9","author":"B Mead","year":"2014","unstructured":"Mead, B., Logan, A., Berry, M., Leadbeater, W. & Scheven, B. A. Paracrine-mediated neuroprotection and neuritogenesis of axotomised retinal ganglion cells by human dental pulp stem cells: comparison with human bone marrow and adipose-derived mesenchymal stem cells. PLoS One \n                           9, e109305, https:\/\/doi.org\/10.1371\/journal.pone.0109305 (2014).","journal-title":"PLoS One"},{"key":"12969_CR33","doi-asserted-by":"publisher","unstructured":"Yamamoto, T. et al. Trophic Effects of Dental Pulp Stem Cells on Schwann Cells in Peripheral Nerve Regeneration. Cell Transplant, doi:https:\/\/doi.org\/10.3727\/096368915X688074 (2015).","DOI":"10.3727\/096368915X688074"},{"key":"12969_CR34","doi-asserted-by":"publisher","first-page":"515","DOI":"10.1016\/j.neuroscience.2011.09.064","volume":"199","author":"AJ Reid","year":"2011","unstructured":"Reid, A. J. et al. Nerve repair with adipose-derived stem cells protects dorsal root ganglia neurons from apoptosis. Neuroscience \n                           199, 515\u2013522, https:\/\/doi.org\/10.1016\/j.neuroscience.2011.09.064 (2011).","journal-title":"Neuroscience"},{"key":"12969_CR35","doi-asserted-by":"publisher","first-page":"54","DOI":"10.1016\/j.expneurol.2005.10.029","volume":"198","author":"L Crigler","year":"2006","unstructured":"Crigler, L., Robey, R. C., Asawachaicharn, A., Gaupp, D. & Phinney, D. G. Human mesenchymal stem cell subpopulations express a variety of neuro-regulatory molecules and promote neuronal cell survival and neuritogenesis. 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Neurosurg Focus \n                           26, E3, https:\/\/doi.org\/10.3171\/FOC.2009.26.2.E3 (2009).","journal-title":"Neurosurg Focus"},{"key":"12969_CR40","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 \n                           14, 1771\u20131776 (2001).","journal-title":"Eur J Neurosci"},{"key":"12969_CR41","doi-asserted-by":"publisher","first-page":"267","DOI":"10.1016\/j.expneurol.2007.06.029","volume":"207","author":"PJ Kingham","year":"2007","unstructured":"Kingham, P. J. et al. Adipose-derived stem cells differentiate into a Schwann cell phenotype and promote neurite outgrowth in vitro. 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