{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,16]],"date-time":"2026-10-16T22:50:34Z","timestamp":1792191034068,"version":"4.4.0"},"reference-count":45,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2017,10,2]],"date-time":"2017-10-02T00:00:00Z","timestamp":1506902400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2017,10,2]],"date-time":"2017-10-02T00:00:00Z","timestamp":1506902400000},"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 activation of T helper cells requires antigens to be exposed on the surface of antigen presenting cells (APCs) via MHC class II (MHC-II) molecules. Expression of MHC-II is generally limited to professional APCs, but other cell types can express MHC-II under inflammatory conditions. However, the importance of these conditional APCs is unknown. We and others have previously shown that Schwann cells are potentially conditional APCs, but the functional relevance of MHC-II expression by Schwann cells has not been studied <jats:italic>in vivo<\/jats:italic>. Here, we conditionally deleted the MHC-II \u03b2-chain from myelinating Schwann cells in mice and investigated how this influenced post-traumatic intraneural inflammation and neuropathic pain using the chronic constriction injury (CCI) model. We demonstrate that deletion of MHC-II in myelinating Schwann cells reduces thermal hyperalgesia and, to a lesser extent, also diminishes mechanical allodynia in CCI in female mice. This was accompanied by a reduction of intraneural CD4+ T cells and greater preservation of preferentially large-caliber axons. Activation of T helper cells by MHC-II on Schwann cells thus promotes post-traumatic axonal loss and neuropathic pain. Hence, we provide experimental evidence that Schwann cells gain antigen-presenting function <jats:italic>in vivo<\/jats:italic> and modulate local immune responses and diseases in the peripheral nerves.<\/jats:p>","DOI":"10.1038\/s41598-017-12744-2","type":"journal-article","created":{"date-parts":[[2017,9,26]],"date-time":"2017-09-26T10:59:31Z","timestamp":1506423571000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":79,"title":["Schwann cells promote post-traumatic nerve inflammation and neuropathic pain through MHC class II"],"prefix":"10.1038","volume":"7","author":[{"given":"Maike","family":"Hartlehnert","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Angelika","family":"Derksen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tim","family":"Hagenacker","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David","family":"Kindermann","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria","family":"Sch\u00e4fers","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mathias","family":"Pawlak","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bernd C.","family":"Kieseier","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4341-4719","authenticated-orcid":false,"given":"Gerd","family":"Meyer zu Horste","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2017,10,2]]},"reference":[{"key":"12744_CR1","doi-asserted-by":"publisher","first-page":"823","DOI":"10.1038\/nri3084","volume":"11","author":"J Neefjes","year":"2011","unstructured":"Neefjes, J., Jongsma, M. L., Paul, P. & Bakke, O. Towards a systems understanding of MHC class I and MHC class II antigen presentation. Nat Rev Immunol \n                           11, 823\u2013836, https:\/\/doi.org\/10.1038\/nri3084 (2011).","journal-title":"Nat Rev Immunol"},{"key":"12744_CR2","doi-asserted-by":"publisher","first-page":"975","DOI":"10.1146\/annurev.immunol.22.012703.104538","volume":"23","author":"ES Trombetta","year":"2005","unstructured":"Trombetta, E. S. & Mellman, I. Cell biology of antigen processing in vitro and in vivo. Annu Rev Immunol \n                           23, 975\u20131028 (2005).","journal-title":"Annu Rev Immunol"},{"key":"12744_CR3","doi-asserted-by":"publisher","DOI":"10.1186\/1756-8722-6-61","volume":"6","author":"J Mai","year":"2013","unstructured":"Mai, J., Virtue, A., Shen, J., Wang, H. & Yang, X. F. An evolving new paradigm: endothelial cells\u2013conditional innate immune cells. Journal of hematology & oncology \n                           6, 61, https:\/\/doi.org\/10.1186\/1756-8722-6-61 (2013).","journal-title":"Journal of hematology & oncology"},{"key":"12744_CR4","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2172-5-5","volume":"5","author":"AL Rothermel","year":"2004","unstructured":"Rothermel, A. L. et al. Endothelial cells present antigens in vivo. BMC immunology \n                           5, 5, https:\/\/doi.org\/10.1186\/1471-2172-5-5 (2004).","journal-title":"BMC immunology"},{"key":"12744_CR5","doi-asserted-by":"publisher","first-page":"132","DOI":"10.1016\/S0165-5728(03)00093-6","volume":"138","author":"H Wiendl","year":"2003","unstructured":"Wiendl, H. et al. Antigen processing and presentation in human muscle: cathepsin S is critical for MHC class II expression and upregulated in inflammatory myopathies. J Neuroimmunol \n                           138, 132\u2013143 (2003).","journal-title":"J Neuroimmunol"},{"key":"12744_CR6","doi-asserted-by":"publisher","first-page":"1321","DOI":"10.1038\/sj.gt.3302293","volume":"11","author":"B Cao","year":"2004","unstructured":"Cao, B., Bruder, J., Kovesdi, I. & Huard, J. Muscle stem cells can act as antigen-presenting cells: implication for gene therapy. Gene therapy \n                           11, 1321\u20131330, https:\/\/doi.org\/10.1038\/sj.gt.3302293 (2004).","journal-title":"Gene therapy"},{"key":"12744_CR7","doi-asserted-by":"publisher","first-page":"719","DOI":"10.1038\/nri3754","volume":"14","author":"T Kambayashi","year":"2014","unstructured":"Kambayashi, T. & Laufer, T. M. Atypical MHC class II-expressing antigen-presenting cells: can anything replace a dendritic cell? Nat Rev Immunol \n                           14, 719\u2013730, https:\/\/doi.org\/10.1038\/nri3754 (2014).","journal-title":"Nat Rev Immunol"},{"key":"12744_CR8","doi-asserted-by":"publisher","DOI":"10.1186\/1742-2094-9-119","volume":"9","author":"H Liu","year":"2012","unstructured":"Liu, H. et al. Immunodominant fragments of myelin basic protein initiate T cell-dependent pain. J Neuroinflammation \n                           9, 119, https:\/\/doi.org\/10.1186\/1742-2094-9-119 (2012).","journal-title":"J Neuroinflammation"},{"key":"12744_CR9","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1002\/mus.20893","volume":"37","author":"G Meyer zu Horste","year":"2008","unstructured":"Meyer zu Horste, G., Hu, W., Hartung, H. P., Lehmann, H. C. & Kieseier, B. C. The immunocompetence of Schwann cells. Muscle Nerve \n                           37, 3\u201313 (2008).","journal-title":"Muscle Nerve"},{"key":"12744_CR10","doi-asserted-by":"publisher","first-page":"80","DOI":"10.1002\/glia.20903","volume":"58","author":"G Meyer Zu Horste","year":"2010","unstructured":"Meyer Zu Horste, G. et al. Expression of antigen processing and presenting molecules by Schwann cells in inflammatory neuropathies. Glia \n                           58, 80\u201392, https:\/\/doi.org\/10.1002\/glia.20903 (2010).","journal-title":"Glia"},{"key":"12744_CR11","doi-asserted-by":"publisher","first-page":"483","DOI":"10.1016\/j.nbd.2009.11.006","volume":"37","author":"G Meyer zu Horste","year":"2010","unstructured":"Meyer zu Horste, G. et al. Mouse Schwann cells activate MHC class I and II restricted T-cell responses, but require external peptide processing for MHC class II presentation. Neurobiol Dis \n                           37, 483\u2013490, https:\/\/doi.org\/10.1016\/j.nbd.2009.11.006 (2010).","journal-title":"Neurobiol Dis"},{"key":"12744_CR12","doi-asserted-by":"publisher","first-page":"68","DOI":"10.1016\/j.jns.2013.01.018","volume":"333","author":"PJ Armati","year":"2013","unstructured":"Armati, P. J. & Mathey, E. K. An update on Schwann cell biology\u2013immunomodulation, neural regulation and other surprises. J Neurol Sci \n                           333, 68\u201372, https:\/\/doi.org\/10.1016\/j.jns.2013.01.018 (2013).","journal-title":"J Neurol Sci"},{"key":"12744_CR13","doi-asserted-by":"publisher","first-page":"1630","DOI":"10.1212\/01.wnl.0000282763.29778.59","volume":"70","author":"RD Treede","year":"2008","unstructured":"Treede, R. D. et al. Neuropathic pain: redefinition and a grading system for clinical and research purposes. Neurology \n                           70, 1630\u20131635, https:\/\/doi.org\/10.1212\/01.wnl.0000282763.29778.59 (2008).","journal-title":"Neurology"},{"key":"12744_CR14","doi-asserted-by":"publisher","first-page":"924","DOI":"10.1016\/S1474-4422(14)70102-4","volume":"13","author":"TS Jensen","year":"2014","unstructured":"Jensen, T. S. & Finnerup, N. B. Allodynia and hyperalgesia in neuropathic pain: clinical manifestations and mechanisms. Lancet Neurol \n                           13, 924\u2013935, https:\/\/doi.org\/10.1016\/S1474-4422(14)70102-4 (2014).","journal-title":"Lancet Neurol"},{"key":"12744_CR15","doi-asserted-by":"publisher","first-page":"380","DOI":"10.1016\/j.pain.2007.08.013","volume":"136","author":"D Bouhassira","year":"2008","unstructured":"Bouhassira, D., Lanteri-Minet, M., Attal, N., Laurent, B. & Touboul, C. Prevalence of chronic pain with neuropathic characteristics in the general population. Pain \n                           136, 380\u2013387, https:\/\/doi.org\/10.1016\/j.pain.2007.08.013 (2008).","journal-title":"Pain"},{"key":"12744_CR16","doi-asserted-by":"publisher","first-page":"281","DOI":"10.1016\/j.jpain.2005.11.008","volume":"7","author":"N Torrance","year":"2006","unstructured":"Torrance, N., Smith, B. H., Bennett, M. I. & Lee, A. J. The epidemiology of chronic pain of predominantly neuropathic origin. Results from a general population survey. J Pain \n                           7, 281\u2013289, https:\/\/doi.org\/10.1016\/j.jpain.2005.11.008 (2006).","journal-title":"J Pain"},{"key":"12744_CR17","doi-asserted-by":"publisher","first-page":"1361","DOI":"10.1038\/nn1992","volume":"10","author":"J Scholz","year":"2007","unstructured":"Scholz, J. & Woolf, C. J. The neuropathic pain triad: neurons, immune cells and glia. Nat Neurosci \n                           10, 1361\u20131368, https:\/\/doi.org\/10.1038\/nn1992 (2007).","journal-title":"Nat Neurosci"},{"key":"12744_CR18","doi-asserted-by":"publisher","first-page":"199","DOI":"10.1083\/jcb.200109021","volume":"156","author":"ML Feltri","year":"2002","unstructured":"Feltri, M. L. et al. Conditional disruption of beta 1 integrin in Schwann cells impedes interactions with axons. J Cell Biol \n                           156, 199\u2013209 (2002).","journal-title":"J Cell Biol"},{"key":"12744_CR19","doi-asserted-by":"publisher","first-page":"152","DOI":"10.1002\/gene.10056","volume":"32","author":"K Hashimoto","year":"2002","unstructured":"Hashimoto, K., Joshi, S. K. & Koni, P. A. A conditional null allele of the major histocompatibility IA-beta chain gene. 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Pain \n                           33, 87\u2013107 (1988).","journal-title":"Pain"},{"key":"12744_CR22","doi-asserted-by":"publisher","first-page":"4332","DOI":"10.1172\/JCI58675","volume":"121","author":"CH Ma","year":"2011","unstructured":"Ma, C. H. et al. Accelerating axonal growth promotes motor recovery after peripheral nerve injury in mice. J Clin Invest \n                           121, 4332\u20134347, https:\/\/doi.org\/10.1172\/JCI58675 (2011).","journal-title":"J Clin Invest"},{"key":"12744_CR23","doi-asserted-by":"publisher","first-page":"428","DOI":"10.1111\/j.1750-3639.2010.00466.x","volume":"21","author":"L Schirmer","year":"2011","unstructured":"Schirmer, L., Antel, J. P., Bruck, W. & Stadelmann, C. Axonal loss and neurofilament phosphorylation changes accompany lesion development and clinical progression in multiple sclerosis. Brain Pathol \n                           21, 428\u2013440, https:\/\/doi.org\/10.1111\/j.1750-3639.2010.00466.x (2011).","journal-title":"Brain Pathol"},{"key":"12744_CR24","doi-asserted-by":"publisher","first-page":"167","DOI":"10.1111\/j.1533-2500.2010.00367.x","volume":"10","author":"R Vallejo","year":"2010","unstructured":"Vallejo, R., Tilley, D. M., Vogel, L. & Benyamin, R. The role of glia and the immune system in the development and maintenance of neuropathic pain. Pain Pract \n                           10, 167\u2013184, https:\/\/doi.org\/10.1111\/j.1533-2500.2010.00367.x (2010).","journal-title":"Pain Pract"},{"key":"12744_CR25","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0021223","volume":"6","author":"G Meyer Zu Horste","year":"2011","unstructured":"Meyer Zu Horste, G. et al. Quinpramine Ameliorates Rat Experimental Autoimmune Neuritis and Redistributes MHC Class II Molecules. PloS one \n                           6, e21223 (2011).","journal-title":"PloS one"},{"key":"12744_CR26","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1038\/nature12240","volume":"498","author":"MR Hepworth","year":"2013","unstructured":"Hepworth, M. R. et al. Innate lymphoid cells regulate CD4+ T-cell responses to intestinal commensal bacteria. Nature \n                           498, 113\u2013117, https:\/\/doi.org\/10.1038\/nature12240 (2013).","journal-title":"Nature"},{"key":"12744_CR27","doi-asserted-by":"publisher","first-page":"6503","DOI":"10.4049\/jimmunol.176.11.6503","volume":"176","author":"M Shimoda","year":"2006","unstructured":"Shimoda, M. et al. Conditional ablation of MHC-II suggests an indirect role for MHC-II in regulatory CD4 T cell maintenance. J Immunol \n                           176, 6503\u20136511 (2006).","journal-title":"J Immunol"},{"key":"12744_CR28","doi-asserted-by":"publisher","first-page":"879","DOI":"10.1038\/nn.4316","volume":"19","author":"Y Poitelon","year":"2016","unstructured":"Poitelon, Y. et al. YAP and TAZ control peripheral myelination and the expression of laminin receptors in Schwann cells. Nat Neurosci \n                           19, 879\u2013887, https:\/\/doi.org\/10.1038\/nn.4316 (2016).","journal-title":"Nat Neurosci"},{"key":"12744_CR29","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1084\/jem.20130720","volume":"211","author":"E Porrello","year":"2014","unstructured":"Porrello, E. et al. Jab1 regulates Schwann cell proliferation and axonal sorting through p27. J Exp Med \n                           211, 29\u201343, https:\/\/doi.org\/10.1084\/jem.20130720 (2014).","journal-title":"J Exp Med"},{"key":"12744_CR30","doi-asserted-by":"publisher","first-page":"5590","DOI":"10.1523\/JNEUROSCI.3342-12.2013","volume":"33","author":"S Orita","year":"2013","unstructured":"Orita, S. et al. Schwann cell LRP1 regulates remak bundle ultrastructure and axonal interactions to prevent neuropathic pain. J Neurosci \n                           33, 5590\u20135602, https:\/\/doi.org\/10.1523\/JNEUROSCI.3342-12.2013 (2013).","journal-title":"J Neurosci"},{"key":"12744_CR31","doi-asserted-by":"publisher","first-page":"503","DOI":"10.1146\/annurev-cellbio-100913-013101","volume":"30","author":"KA Nave","year":"2014","unstructured":"Nave, K. A. & Werner, H. B. Myelination of the nervous system: mechanisms and functions. 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Pain \n                           124, 13\u201317, https:\/\/doi.org\/10.1016\/j.pain.2006.06.020 (2006).","journal-title":"Pain"},{"key":"12744_CR36","doi-asserted-by":"publisher","DOI":"10.3389\/fnbeh.2014.00040","volume":"8","author":"L Nicotra","year":"2014","unstructured":"Nicotra, L., Tuke, J., Grace, P. M., Rolan, P. E. & Hutchinson, M. R. Sex differences in mechanical allodynia: how can it be preclinically quantified and analyzed? Front Behav Neurosci \n                           8, 40, https:\/\/doi.org\/10.3389\/fnbeh.2014.00040 (2014).","journal-title":"Front Behav Neurosci"},{"key":"12744_CR37","doi-asserted-by":"publisher","first-page":"681","DOI":"10.1016\/j.neuron.2005.08.017","volume":"47","author":"C Taveggia","year":"2005","unstructured":"Taveggia, C. et al. Neuregulin-1 type III determines the ensheathment fate of axons. Neuron \n                           47, 681\u2013694 (2005).","journal-title":"Neuron"},{"key":"12744_CR38","doi-asserted-by":"publisher","first-page":"700","DOI":"10.1126\/science.1095862","volume":"304","author":"GV Michailov","year":"2004","unstructured":"Michailov, G. V. et al. Axonal neuregulin-1 regulates myelin sheath thickness. Science \n                           304, 700\u2013703, https:\/\/doi.org\/10.1126\/science.1095862 (2004).","journal-title":"Science"},{"key":"12744_CR39","doi-asserted-by":"publisher","first-page":"48","DOI":"10.1038\/nn.3281","volume":"16","author":"RM Stassart","year":"2013","unstructured":"Stassart, R. M. et al. A role for Schwann cell-derived neuregulin-1 in remyelination. 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J Neurosci \n                           26, 10299\u201310304, https:\/\/doi.org\/10.1523\/JNEUROSCI.3135-06.2006 (2006).","journal-title":"J Neurosci"},{"key":"12744_CR42","doi-asserted-by":"publisher","unstructured":"Austin, P. J., Wu, A. & Moalem-Taylor, G. Chronic constriction of the sciatic nerve and pain hypersensitivity testing in rats. Journal of visualized experiments: JoVE, https:\/\/doi.org\/10.3791\/3393 (2012).","DOI":"10.3791\/3393"},{"key":"12744_CR43","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1016\/S0091-3057(02)00961-9","volume":"74","author":"AK Baker","year":"2002","unstructured":"Baker, A. K., Hoffmann, V. L. & Meert, T. F. Dextromethorphan and ketamine potentiate the antinociceptive effects of mu- but not delta- or kappa-opioid agonists in a mouse model of acute pain. Pharmacol Biochem Behav \n                           74, 73\u201386 (2002).","journal-title":"Pharmacol Biochem Behav"},{"key":"12744_CR44","doi-asserted-by":"publisher","first-page":"66","DOI":"10.4097\/kjae.2012.62.1.66","volume":"62","author":"BY Hwang","year":"2012","unstructured":"Hwang, B. Y., Kim, E. S., Kim, C. H., Kwon, J. Y. & Kim, H. K. Gender differences in paclitaxel-induced neuropathic pain behavior and analgesic response in rats. Korean J Anesthesiol \n                           62, 66\u201372, https:\/\/doi.org\/10.4097\/kjae.2012.62.1.66 (2012).","journal-title":"Korean J Anesthesiol"},{"key":"12744_CR45","doi-asserted-by":"publisher","first-page":"61","DOI":"10.1002\/ana.21026","volume":"61","author":"G Meyer zu Horste","year":"2007","unstructured":"Meyer zu Horste, G. et al. Antiprogesterone therapy uncouples axonal loss from demyelination in a transgenic rat model of CMT1A neuropathy. Ann Neurol \n                           61, 61\u201372 (2007).","journal-title":"Ann Neurol"}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-017-12744-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-017-12744-2","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-017-12744-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,23]],"date-time":"2022-12-23T11:28:37Z","timestamp":1671794917000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-017-12744-2"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,10,2]]},"references-count":45,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2017,12]]}},"alternative-id":["12744"],"URL":"https:\/\/doi.org\/10.1038\/s41598-017-12744-2","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,10,2]]},"assertion":[{"value":"11 November 2016","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"15 September 2017","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"2 October 2017","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare that they have no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing Interests"}}],"article-number":"12518"}}