{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,29]],"date-time":"2026-10-29T23:51:30Z","timestamp":1793317890603,"version":"4.5.0"},"reference-count":55,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2018,7,23]],"date-time":"2018-07-23T00:00:00Z","timestamp":1532304000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2018,7,23]],"date-time":"2018-07-23T00:00:00Z","timestamp":1532304000000},"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>Cathepsin S (CTSS) activity is elevated in Sj\u00f6gren\u2019s Syndrome (SS) patient tears. Here we tested whether protease inhibition and cystatin C (Cys C) levels are reduced in SS tears, which could lead to enhanced CTSS-driven degradation of tear proteins. CTSS activity against Cys C, LF and sIgA was tested in SS or healthy control tears. Tears from 156 female subjects (33, SS; 33, rheumatoid arthritis; 31, other autoimmune diseases; 35, non-autoimmune dry eye (DE); 24, healthy controls) were analyzed for CTSS activity and Cys C, LF, and sIgA levels. Cys C and LF showed enhanced degradation in SS tears supplemented with recombinant CTSS, but not supplemented healthy control tears. CTSS activity was significantly increased, while Cys C, LF and sIgA levels were significantly decreased, in SS tears compared to other groups. While tear CTSS activity remained the strongest discriminator of SS in autoimmune populations, combining LF and CTSS improved discrimination of SS beyond CTSS in DE patients. Reductions in Cys C and other endogenous proteases may enhance CTSS activity in SS tears. Tear CTSS activity is reconfirmed as a putative biomarker of SS in an independent patient cohort while combined LF and CTSS measurements may distinguish SS from DE patients.<\/jats:p>","DOI":"10.1038\/s41598-018-29411-9","type":"journal-article","created":{"date-parts":[[2018,7,17]],"date-time":"2018-07-17T09:37:36Z","timestamp":1531820256000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":65,"title":["Increased Cathepsin S activity associated with decreased protease inhibitory capacity contributes to altered tear proteins in Sj\u00f6gren\u2019s Syndrome patients"],"prefix":"10.1038","volume":"8","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-7399-4358","authenticated-orcid":false,"given":"Maria C.","family":"Edman","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Srikanth R.","family":"Janga","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhen","family":"Meng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mercy","family":"Bechtold","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alexander F.","family":"Chen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chongiin","family":"Kim","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Luke","family":"Naman","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Arunava","family":"Sarma","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Neha","family":"Teekappanavar","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alice Y.","family":"Kim","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sara","family":"Madrigal","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Simranjit","family":"Singh","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elizabeth","family":"Ortiz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stratos","family":"Christianakis","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniel G.","family":"Arkfeld","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wendy J.","family":"Mack","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Martin","family":"Heur","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"William","family":"Stohl","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8195-5703","authenticated-orcid":false,"given":"Sarah F.","family":"Hamm-Alvarez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2018,7,23]]},"reference":[{"key":"29411_CR1","doi-asserted-by":"publisher","unstructured":"Brito-Zeron, P., Ramos-Casals, M. & group, E.-S. t. f. Advances in the understanding and treatment of systemic complications in Sjogren\u2019s syndrome. Current opinion in rheumatology 26, 520\u2013527, https:\/\/doi.org\/10.1097\/BOR.0000000000000096 (2014).","DOI":"10.1097\/BOR.0000000000000096"},{"key":"29411_CR2","doi-asserted-by":"publisher","first-page":"43","DOI":"10.2147\/OPTH.S80043","volume":"10","author":"KA Beckman","year":"2016","unstructured":"Beckman, K. A., Luchs, J. & Milner, M. S. Making the diagnosis of Sjogren\u2019s syndrome in patients with dry eye. Clin Ophthalmol 10, 43\u201353, https:\/\/doi.org\/10.2147\/OPTH.S80043 (2016).","journal-title":"Clin Ophthalmol"},{"key":"29411_CR3","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1586\/1744666X.2016.1109449","volume":"12","author":"P Brito-Zeron","year":"2016","unstructured":"Brito-Zeron, P. et al. Early diagnosis of primary Sjogren\u2019s syndrome: EULAR-SS task force clinical recommendations. Expert review of clinical immunology 12, 137\u2013156, https:\/\/doi.org\/10.1586\/1744666X.2016.1109449 (2016).","journal-title":"Expert review of clinical immunology"},{"key":"29411_CR4","doi-asserted-by":"publisher","first-page":"5019","DOI":"10.1167\/iovs.09-4523","volume":"51","author":"X Li","year":"2010","unstructured":"Li, X. et al. Increased expression of cathepsins and obesity-induced proinflammatory cytokines in lacrimal glands of male NOD mouse. Invest Ophthalmol Vis Sci 51, 5019\u20135029, https:\/\/doi.org\/10.1167\/iovs.09-4523 (2010).","journal-title":"Invest Ophthalmol Vis Sci"},{"key":"29411_CR5","doi-asserted-by":"publisher","first-page":"1872","DOI":"10.1002\/art.38633","volume":"66","author":"SF Hamm-Alvarez","year":"2014","unstructured":"Hamm-Alvarez, S. F. et al. Tear cathepsin S as a candidate biomarker for Sjogren\u2019s syndrome. Arthritis Rheumatol 66, 1872\u20131881, https:\/\/doi.org\/10.1002\/art.38633 (2014).","journal-title":"Arthritis Rheumatol"},{"key":"29411_CR6","doi-asserted-by":"publisher","first-page":"945","DOI":"10.4049\/jimmunol.0900921","volume":"183","author":"CM Costantino","year":"2009","unstructured":"Costantino, C. M., Ploegh, H. L. & Hafler, D. A. Cathepsin S regulates class II MHC processing in human CD4+ HLA-DR+ T cells. J Immunol 183, 945\u2013952, https:\/\/doi.org\/10.4049\/jimmunol.0900921 (2009).","journal-title":"J Immunol"},{"key":"29411_CR7","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1016\/S1074-7613(00)80249-6","volume":"4","author":"RJ Riese","year":"1996","unstructured":"Riese, R. J. et al. Essential role for cathepsin S in MHC class II-associated invariant chain processing and peptide loading. Immunity 4, 357\u2013366 (1996).","journal-title":"Immunity"},{"key":"29411_CR8","doi-asserted-by":"publisher","first-page":"2560","DOI":"10.1016\/j.bbagen.2014.03.017","volume":"1840","author":"M Fonovic","year":"2014","unstructured":"Fonovic, M. & Turk, B. Cysteine cathepsins and extracellular matrix degradation. Biochim Biophys Acta 1840, 2560\u20132570, https:\/\/doi.org\/10.1016\/j.bbagen.2014.03.017 (2014).","journal-title":"Biochim Biophys Acta"},{"key":"29411_CR9","doi-asserted-by":"publisher","first-page":"e99702","DOI":"10.1371\/journal.pone.0099702","volume":"9","author":"SB Elmariah","year":"2014","unstructured":"Elmariah, S. B., Reddy, V. B. & Lerner, E. A. Cathepsin S signals via PAR2 and generates a novel tethered ligand receptor agonist. PloS one 9, e99702, https:\/\/doi.org\/10.1371\/journal.pone.0099702 (2014).","journal-title":"PloS one"},{"key":"29411_CR10","doi-asserted-by":"publisher","first-page":"1577","DOI":"10.1681\/ASN.2015101162","volume":"27","author":"DJ Nikolic-Paterson","year":"2016","unstructured":"Nikolic-Paterson, D. J. Cathepsin S-Dependent Protease-Activated Receptor-2 Activation: A New Mechanism of Endothelial Dysfunction. Journal of the American Society of Nephrology: JASN 27, 1577\u20131579, https:\/\/doi.org\/10.1681\/ASN.2015101162 (2016).","journal-title":"Journal of the American Society of Nephrology: JASN"},{"key":"29411_CR11","doi-asserted-by":"publisher","first-page":"27215","DOI":"10.1074\/jbc.M114.599712","volume":"289","author":"P Zhao","year":"2014","unstructured":"Zhao, P. et al. Cathepsin S causes inflammatory pain via biased agonism of PAR2 and TRPV4. The Journal of biological chemistry 289, 27215\u201327234, https:\/\/doi.org\/10.1074\/jbc.M114.599712 (2014).","journal-title":"The Journal of biological chemistry"},{"key":"29411_CR12","doi-asserted-by":"publisher","first-page":"1169","DOI":"10.1038\/jid.2011.404","volume":"132","author":"N Kim","year":"2012","unstructured":"Kim, N. et al. Overexpression of cathepsin S induces chronic atopic dermatitis in mice. J Invest Dermatol 132, 1169\u20131176, https:\/\/doi.org\/10.1038\/jid.2011.404 (2012).","journal-title":"J Invest Dermatol"},{"key":"29411_CR13","doi-asserted-by":"crossref","unstructured":"Kirschke, H. In Handbook of Proteolytic Enzymes (ed. Guy Salvesen) 1824\u20131830 (Academic Press, 2013).","DOI":"10.1016\/B978-0-12-382219-2.00412-9"},{"key":"29411_CR14","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.exer.2017.05.006","volume":"161","author":"SC Regmi","year":"2017","unstructured":"Regmi, S. C. et al. Degradation of proteoglycan 4\/lubricin by cathepsin S: Potential mechanism for diminished ocular surface lubrication in Sjogren\u2019s syndrome. Exp Eye Res 161, 1\u20139, https:\/\/doi.org\/10.1016\/j.exer.2017.05.006 (2017).","journal-title":"Exp Eye Res"},{"key":"29411_CR15","doi-asserted-by":"publisher","first-page":"213","DOI":"10.1016\/0014-5793(91)80804-C","volume":"285","author":"V Turk","year":"1991","unstructured":"Turk, V. & Bode, W. The cystatins: protein inhibitors of cysteine proteinases. FEBS letters 285, 213\u2013219 (1991).","journal-title":"FEBS letters"},{"key":"29411_CR16","doi-asserted-by":"publisher","first-page":"1191","DOI":"10.1172\/JCI7709","volume":"104","author":"GP Shi","year":"1999","unstructured":"Shi, G. P. et al. Cystatin C deficiency in human atherosclerosis and aortic aneurysms. The Journal of clinical investigation 104, 1191\u20131197, https:\/\/doi.org\/10.1172\/JCI7709 (1999).","journal-title":"The Journal of clinical investigation"},{"key":"29411_CR17","doi-asserted-by":"publisher","first-page":"332","DOI":"10.1136\/mp.52.6.332","volume":"52","author":"CG Huh","year":"1999","unstructured":"Huh, C. G. et al. Decreased metastatic spread in mice homozygous for a null allele of the cystatin C protease inhibitor gene. Mol Pathol 52, 332\u2013340 (1999).","journal-title":"Mol Pathol"},{"key":"29411_CR18","doi-asserted-by":"publisher","first-page":"591","DOI":"10.1111\/j.1365-2362.2010.02305.x","volume":"40","author":"E Kolwijck","year":"2010","unstructured":"Kolwijck, E. et al. The balance between extracellular cathepsins and cystatin C is of importance for ovarian cancer. Eur J Clin Invest 40, 591\u2013599, https:\/\/doi.org\/10.1111\/j.1365-2362.2010.02305.x (2010).","journal-title":"Eur J Clin Invest"},{"key":"29411_CR19","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1016\/j.biochi.2008.07.007","volume":"91","author":"JL Flanagan","year":"2009","unstructured":"Flanagan, J. L. & Willcox, M. D. Role of lactoferrin in the tear film. Biochimie 91, 35\u201343, https:\/\/doi.org\/10.1016\/j.biochi.2008.07.007 (2009).","journal-title":"Biochimie"},{"key":"29411_CR20","first-page":"193","volume":"3","author":"A Kijlstra","year":"1990","unstructured":"Kijlstra, A. The role of lactoferrin in the nonspecific immune response on the ocular surface. Reg Immunol 3, 193\u2013197 (1990).","journal-title":"Reg Immunol"},{"key":"29411_CR21","doi-asserted-by":"publisher","first-page":"2322","DOI":"10.1167\/iovs.07-0691","volume":"49","author":"E Knop","year":"2008","unstructured":"Knop, E., Knop, N. & Claus, P. Local production of secretory IgA in the eye-associated lymphoid tissue (EALT) of the normal human ocular surface. Invest Ophthalmol Vis Sci 49, 2322\u20132329, https:\/\/doi.org\/10.1167\/iovs.07-0691 (2008).","journal-title":"Invest Ophthalmol Vis Sci"},{"key":"29411_CR22","doi-asserted-by":"publisher","first-page":"1224","DOI":"10.2353\/ajpath.2007.070388","volume":"171","author":"ME Doyle","year":"2007","unstructured":"Doyle, M. E. et al. Autoimmune dacryoadenitis of NOD\/LtJ mice and its subsequent effects on tear protein composition. Am J Pathol 171, 1224\u20131236, https:\/\/doi.org\/10.2353\/ajpath.2007.070388 (2007).","journal-title":"Am J Pathol"},{"key":"29411_CR23","doi-asserted-by":"publisher","first-page":"1245","DOI":"10.1086\/423821","volume":"190","author":"MP Rogan","year":"2004","unstructured":"Rogan, M. P. et al. Loss of microbicidal activity and increased formation of biofilm due to decreased lactoferrin activity in patients with cystic fibrosis. J Infect Dis 190, 1245\u20131253, https:\/\/doi.org\/10.1086\/423821 (2004).","journal-title":"J Infect Dis"},{"key":"29411_CR24","doi-asserted-by":"publisher","first-page":"5088","DOI":"10.1039\/c2an35821b","volume":"137","author":"AK Denisin","year":"2012","unstructured":"Denisin, A. K., Karns, K. & Herr, A. E. Post-collection processing of Schirmer strip-collected human tear fluid impacts protein content. The Analyst 137, 5088\u20135096, https:\/\/doi.org\/10.1039\/c2an35821b (2012).","journal-title":"The Analyst"},{"key":"29411_CR25","doi-asserted-by":"publisher","first-page":"201","DOI":"10.1016\/j.jaut.2011.01.003","volume":"36","author":"M Baugh","year":"2011","unstructured":"Baugh, M. et al. Therapeutic dosing of an orally active, selective cathepsin S inhibitor suppresses disease in models of autoimmunity. Journal of autoimmunity 36, 201\u2013209, https:\/\/doi.org\/10.1016\/j.jaut.2011.01.003 (2011).","journal-title":"Journal of autoimmunity"},{"key":"29411_CR26","doi-asserted-by":"publisher","first-page":"452","DOI":"10.1136\/annrheumdis-2013-203717","volume":"74","author":"KV Rupanagudi","year":"2015","unstructured":"Rupanagudi, K. V. et al. Cathepsin S inhibition suppresses systemic lupus erythematosus and lupus nephritis because cathepsin S is essential for MHC class II-mediated CD4 T cell and B cell priming. Annals of the rheumatic diseases 74, 452\u2013463, https:\/\/doi.org\/10.1136\/annrheumdis-2013-203717 (2015).","journal-title":"Annals of the rheumatic diseases"},{"key":"29411_CR27","doi-asserted-by":"publisher","first-page":"361","DOI":"10.1172\/JCI0214682","volume":"110","author":"K Saegusa","year":"2002","unstructured":"Saegusa, K. et al. Cathepsin S inhibitor prevents autoantigen presentation and autoimmunity. The Journal of clinical investigation 110, 361\u2013369, https:\/\/doi.org\/10.1172\/JCI14682 (2002).","journal-title":"The Journal of clinical investigation"},{"key":"29411_CR28","doi-asserted-by":"publisher","first-page":"1334","DOI":"10.1111\/bcp.12470","volume":"78","author":"CD Payne","year":"2014","unstructured":"Payne, C. D. et al. Pharmacokinetics and pharmacodynamics of the cathepsin S inhibitor, LY3000328, in healthy subjects. British journal of clinical pharmacology 78, 1334\u20131342, https:\/\/doi.org\/10.1111\/bcp.12470 (2014).","journal-title":"British journal of clinical pharmacology"},{"key":"29411_CR29","doi-asserted-by":"publisher","first-page":"806","DOI":"10.3389\/fimmu.2017.00806","volume":"8","author":"M Theron","year":"2017","unstructured":"Theron, M. et al. Pharmacodynamic Monitoring of RO5459072, a Small Molecule Inhibitor of Cathepsin S. Frontiers in immunology 8, 806, https:\/\/doi.org\/10.3389\/fimmu.2017.00806 (2017).","journal-title":"Frontiers in immunology"},{"key":"29411_CR30","doi-asserted-by":"publisher","first-page":"130","DOI":"10.1016\/j.ab.2012.08.011","volume":"430","author":"JM Cox","year":"2012","unstructured":"Cox, J. M. et al. Determination of cathepsin S abundance and activity in human plasma and implications for clinical investigation. Anal Biochem 430, 130\u2013137, https:\/\/doi.org\/10.1016\/j.ab.2012.08.011 (2012).","journal-title":"Anal Biochem"},{"key":"29411_CR31","doi-asserted-by":"publisher","first-page":"2421","DOI":"10.1111\/j.1582-4934.2010.01229.x","volume":"15","author":"D Haves-Zburof","year":"2011","unstructured":"Haves-Zburof, D. et al. Cathepsins and their endogenous inhibitors cystatins: expression and modulation in multiple sclerosis. Journal of cellular and molecular medicine 15, 2421\u20132429, https:\/\/doi.org\/10.1111\/j.1582-4934.2010.01229.x (2011).","journal-title":"Journal of cellular and molecular medicine"},{"key":"29411_CR32","doi-asserted-by":"publisher","first-page":"83","DOI":"10.1016\/S0009-8981(00)00298-9","volume":"300","author":"N Cimerman","year":"2000","unstructured":"Cimerman, N., Brguljan, P. M., Krasovec, M., Suskovic, S. & Kos, J. Serum cystatin C, a potent inhibitor of cysteine proteinases, is elevated in asthmatic patients. Clinica chimica acta; international journal of clinical chemistry 300, 83\u201395 (2000).","journal-title":"Clinica chimica acta; international journal of clinical chemistry"},{"key":"29411_CR33","doi-asserted-by":"publisher","first-page":"269","DOI":"10.1016\/j.jconrel.2013.07.016","volume":"171","author":"M Shah","year":"2013","unstructured":"Shah, M. et al. A rapamycin-binding protein polymer nanoparticle shows potent therapeutic activity in suppressing autoimmune dacryoadenitis in a mouse model of Sjogren\u2019s syndrome. Journal of controlled release: official journal of the Controlled Release Society 171, 269\u2013279, https:\/\/doi.org\/10.1016\/j.jconrel.2013.07.016 (2013).","journal-title":"Journal of controlled release: official journal of the Controlled Release Society"},{"key":"29411_CR34","doi-asserted-by":"publisher","first-page":"372","DOI":"10.1167\/iovs.16-19159","volume":"58","author":"M Shah","year":"2017","unstructured":"Shah, M. et al. Rapamycin Eye Drops Suppress Lacrimal Gland Inflammation In a Murine Model of Sjogren\u2019s Syndrome. Invest Ophthalmol Vis Sci 58, 372\u2013385, https:\/\/doi.org\/10.1167\/iovs.16-19159 (2017).","journal-title":"Invest Ophthalmol Vis Sci"},{"key":"29411_CR35","doi-asserted-by":"publisher","first-page":"8454","DOI":"10.1128\/MCB.00821-07","volume":"27","author":"RA Dean","year":"2007","unstructured":"Dean, R. A. et al. Identification of candidate angiogenic inhibitors processed by matrix metalloproteinase 2 (MMP-2) in cell-based proteomic screens: disruption of vascular endothelial growth factor (VEGF)\/heparin affin regulatory peptide (pleiotrophin) and VEGF\/Connective tissue growth factor angiogenic inhibitory complexes by MMP-2 proteolysis. Molecular and cellular biology 27, 8454\u20138465, https:\/\/doi.org\/10.1128\/MCB.00821-07 (2007).","journal-title":"Molecular and cellular biology"},{"key":"29411_CR36","doi-asserted-by":"publisher","first-page":"211","DOI":"10.1016\/0014-5793(91)80295-E","volume":"280","author":"B Lenarcic","year":"1991","unstructured":"Lenarcic, B., Krasovec, M., Ritonja, A., Olafsson, I. & Turk, V. Inactivation of human cystatin C and kininogen by human cathepsin D. FEBS letters 280, 211\u2013215 (1991).","journal-title":"FEBS letters"},{"key":"29411_CR37","doi-asserted-by":"publisher","first-page":"442","DOI":"10.1038\/icb.2014.121","volume":"93","author":"Y Xu","year":"2015","unstructured":"Xu, Y., Ding, Y., Li, X. & Wu, X. Cystatin C is a disease-associated protein subject to multiple regulation. Immunology and cell biology 93, 442\u2013451, https:\/\/doi.org\/10.1038\/icb.2014.121 (2015).","journal-title":"Immunology and cell biology"},{"key":"29411_CR38","doi-asserted-by":"publisher","first-page":"1912","DOI":"10.1084\/jem.166.6.1912","volume":"166","author":"AH Warfel","year":"1987","unstructured":"Warfel, A. H., Zucker-Franklin, D., Frangione, B. & Ghiso, J. Constitutive secretion of cystatin C (gamma-trace) by monocytes and macrophages and its downregulation after stimulation. J Exp Med 166, 1912\u20131917 (1987).","journal-title":"J Exp Med"},{"key":"29411_CR39","doi-asserted-by":"crossref","unstructured":"Merz, G. S. et al. Human cystatin C forms an inactive dimer during intracellular trafficking in transfected CHO cells. Journal of cellular physiology 173, 423\u2013432, doi:10.1002\/(SICI)1097-4652(199712)173:3<423::AID-JCP15>3.0.CO;2-C (1997).","DOI":"10.1002\/(SICI)1097-4652(199712)173:3<423::AID-JCP15>3.0.CO;2-C"},{"key":"29411_CR40","doi-asserted-by":"publisher","first-page":"3126","DOI":"10.1002\/art.30500","volume":"63","author":"V Bahamondes","year":"2011","unstructured":"Bahamondes, V. et al. Changes in Rab3D expression and distribution in the acini of Sjogren\u2019s syndrome patients are associated with loss of cell polarity and secretory dysfunction. Arthritis Rheum 63, 3126\u20133135, https:\/\/doi.org\/10.1002\/art.30500 (2011).","journal-title":"Arthritis Rheum"},{"key":"29411_CR41","doi-asserted-by":"publisher","first-page":"e43688","DOI":"10.1371\/journal.pone.0043688","volume":"7","author":"M Kamoi","year":"2012","unstructured":"Kamoi, M. et al. Accumulation of secretory vesicles in the lacrimal gland epithelia is related to non-Sjogren\u2019s type dry eye in visual display terminal users. PloS one 7, e43688, https:\/\/doi.org\/10.1371\/journal.pone.0043688 (2012).","journal-title":"PloS one"},{"key":"29411_CR42","doi-asserted-by":"publisher","first-page":"30","DOI":"10.1016\/S0002-9394(14)75074-3","volume":"90","author":"TE Gillette","year":"1980","unstructured":"Gillette, T. E. & Allansmith, M. R. Lactoferrin in human ocular tissues. Am J Ophthalmol 90, 30\u201337 (1980).","journal-title":"Am J Ophthalmol"},{"key":"29411_CR43","doi-asserted-by":"publisher","first-page":"321","DOI":"10.1136\/bjo.68.5.321","volume":"68","author":"IA Mackie","year":"1984","unstructured":"Mackie, I. A. & Seal, D. V. Diagnostic implications of tear protein profiles. Br J Ophthalmol 68, 321\u2013324 (1984).","journal-title":"Br J Ophthalmol"},{"key":"29411_CR44","first-page":"1247","volume":"19","author":"P Versura","year":"2013","unstructured":"Versura, P., Bavelloni, A., Grillini, M., Fresina, M. & Campos, E. C. Diagnostic performance of a tear protein panel in early dry eye. Molecular vision 19, 1247\u20131257 (2013).","journal-title":"Molecular vision"},{"key":"29411_CR45","doi-asserted-by":"publisher","first-page":"1396","DOI":"10.1038\/eye.2010.7","volume":"24","author":"P Versura","year":"2010","unstructured":"Versura, P. et al. Tear proteomics in evaporative dry eye disease. Eye (Lond) 24, 1396\u20131402, https:\/\/doi.org\/10.1038\/eye.2010.7 (2010).","journal-title":"Eye (Lond)"},{"key":"29411_CR46","doi-asserted-by":"crossref","first-page":"224","DOI":"10.1080\/15027732.1986.12461416","volume":"61","author":"PT Janssen","year":"1986","unstructured":"Janssen, P. T. & van Bijsterveld, O. P. Tear fluid proteins in Sjogren\u2019s syndrome. Scand J Rheumatol Suppl 61, 224\u2013227 (1986).","journal-title":"Scand J Rheumatol Suppl"},{"key":"29411_CR47","doi-asserted-by":"publisher","first-page":"284","DOI":"10.1177\/112067219600600311","volume":"6","author":"S Da Dalt","year":"1996","unstructured":"Da Dalt, S., Moncada, A., Priori, R., Valesini, G. & Pivetti-Pezzi, P. The lactoferrin tear test in the diagnosis of Sjogren\u2019s syndrome. Eur J Ophthalmol 6, 284\u2013286 (1996).","journal-title":"Eur J Ophthalmol"},{"key":"29411_CR48","doi-asserted-by":"publisher","first-page":"6","DOI":"10.1186\/s40662-014-0006-y","volume":"1","author":"S D\u2019Souza","year":"2014","unstructured":"D\u2019Souza, S. & Tong, L. Practical issues concerning tear protein assays in dry eye. Eye Vis (Lond) 1, 6, https:\/\/doi.org\/10.1186\/s40662-014-0006-y (2014).","journal-title":"Eye Vis (Lond)"},{"key":"29411_CR49","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1046\/j.1365-3083.1999.00490.x","volume":"49","author":"MG Humphreys-Beher","year":"1999","unstructured":"Humphreys-Beher, M. G., Brayer, J., Yamachika, S., Peck, A. B. & Jonsson, R. An alternative perspective to the immune response in autoimmune exocrinopathy: induction of functional quiescence rather than destructive autoaggression. Scand J Immunol 49, 7\u201310 (1999).","journal-title":"Scand J Immunol"},{"key":"29411_CR50","doi-asserted-by":"publisher","first-page":"693","DOI":"10.1097\/ICO.0000000000000435","volume":"34","author":"V Pastori","year":"2015","unstructured":"Pastori, V., Tavazzi, S. & Lecchi, M. Lactoferrin-loaded contact lenses: eye protection against oxidative stress. Cornea 34, 693\u2013697, https:\/\/doi.org\/10.1097\/ICO.0000000000000435 (2015).","journal-title":"Cornea"},{"key":"29411_CR51","doi-asserted-by":"publisher","first-page":"818","DOI":"10.1093\/rheumatology\/kex495","volume":"57","author":"JF van Nimwegen","year":"2018","unstructured":"van Nimwegen, J. F. et al. Validation of the ACR-EULAR criteria for primary Sjogren\u2019s syndrome in a Dutch prospective diagnostic cohort. Rheumatology (Oxford, England) 57, 818\u2013825, https:\/\/doi.org\/10.1093\/rheumatology\/kex495 (2018).","journal-title":"Rheumatology (Oxford, England)"},{"key":"29411_CR52","doi-asserted-by":"publisher","first-page":"223","DOI":"10.1016\/j.exer.2009.10.008","volume":"90","author":"K Schenke-Layland","year":"2010","unstructured":"Schenke-Layland, K. et al. Lymphocytic infiltration leads to degradation of lacrimal gland extracellular matrix structures in NOD mice exhibiting a Sjogren\u2019s syndrome-like exocrinopathy. Exp Eye Res 90, 223\u2013237, https:\/\/doi.org\/10.1016\/j.exer.2009.10.008 (2010).","journal-title":"Exp Eye Res"},{"issue":"Pt 13","key":"29411_CR53","doi-asserted-by":"crossref","first-page":"1841","DOI":"10.1242\/jcs.111.13.1841","volume":"111","author":"PM Vilalta","year":"1998","unstructured":"Vilalta, P. M., Zhang, L. & Hamm-Alvarez, S. F. A novel taxol-induced vimentin phosphorylation and stabilization revealed by studies on stable microtubules and vimentin intermediate filaments. Journal of cell science 111(Pt 13), 1841\u20131852 (1998).","journal-title":"Journal of cell science"},{"key":"29411_CR54","doi-asserted-by":"publisher","first-page":"C942","DOI":"10.1152\/ajpcell.00275.2015","volume":"310","author":"Z Meng","year":"2016","unstructured":"Meng, Z. et al. Imbalanced Rab3D versus Rab27 increases cathepsin S secretion from lacrimal acini in a mouse model of Sjogren\u2019s Syndrome. Am J Physiol Cell Physiol 310, C942\u2013954, https:\/\/doi.org\/10.1152\/ajpcell.00275.2015 (2016).","journal-title":"Am J Physiol Cell Physiol"},{"key":"29411_CR55","doi-asserted-by":"publisher","first-page":"319","DOI":"10.1016\/j.exer.2009.03.020","volume":"89","author":"K Wu","year":"2009","unstructured":"Wu, K. et al. Altered expression of genes functioning in lipid homeostasis is associated with lipid deposition in NOD mouse lacrimal gland. Exp Eye Res 89, 319\u2013332, https:\/\/doi.org\/10.1016\/j.exer.2009.03.020 (2009).","journal-title":"Exp Eye Res"}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-018-29411-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-018-29411-9","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-018-29411-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,7,5]],"date-time":"2025-07-05T21:15:55Z","timestamp":1751750155000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-018-29411-9"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,7,23]]},"references-count":55,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2018,12]]}},"alternative-id":["29411"],"URL":"https:\/\/doi.org\/10.1038\/s41598-018-29411-9","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,7,23]]},"assertion":[{"value":"16 March 2018","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"11 July 2018","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"23 July 2018","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing Interests"}}],"article-number":"11044"}}