Control of Autoimmune Myocarditis and Multiorgan Inflammation by Glucocorticoid-Induced TNF Receptor Family-Related Proteinhigh, Foxp3-Expressing CD25+ and CD25− Regulatory T Cells
Open accessAbstract
Anomalies of naturally occurring CD4+ regulatory T cells (Treg) cause severe autoimmune/inflammatory diseases in humans and rodents. The transcription factor Foxp3 is currently the most specific marker for natural CD4+ Treg, but it would be useful if other Treg markers, particularly cell surface molecules, could be elucidated. We demonstrate in this study that the vast majority of Foxp3-expressing CD4+ T cells (whether CD25+ or CD25−) show constitutive high-level expression of glucocorticoid-induced TNFR family-related gene/protein (GITR). Transfer of T cell or thymocyte suspensions depleted of GITRhigh cells produces in BALB/c nude mice a wider spectrum and more severe forms of autoimmune diseases than does transfer of similar cell suspensions depleted of CD25+CD4+ T cells only. Notably, mice that receive cells depleted of GITRhigh populations develop severe multiorgan inflammation that includes fatal autoimmune myocarditis resembling giant cell myocarditis in humans, accompanying high-titer anti-myosin autoantibodies. Similar transfer of GITRhigh-depleted cells from prediabetic NOD mice to NOD-SCID mice accelerates the development of diabetes and induces skeletal muscle myositis and other autoimmune/inflammatory diseases. We conclude that GITRhigh, Foxp3-expressing natural Treg, containing both CD25+ and CD25− cell populations, contribute to preventing a variety of autoimmune/inflammatory diseases, and depletion of these cells allows the activation of even weak or rare autoreactive T cells yielding widespread severe autoimmune disease. Diseases induced in this way include many which have been suspected of an autoimmune etiology in humans without much evidence. GITRhigh, Foxp3-expressing natural Treg represent a potential target for the treatment and prevention of these diseases.
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A decreased number of circulating regulatory T cells were found in patients with myocarditis, and adoptive transfer of CD4+ T cells with regulatory T-cell depletion induced fatal myocarditis in mice.
“a decreased number of circulating regulatory T cells were found in patients with myocarditis, and adoptive transfer of CD4 + T cells with regulatory T-cell depletion induced fatal myocarditis in mice”
From Autoimmune Myocarditis, Old Dogs and New Tricks. (2024) · cites this paper as [84]
The section ‘Development of fatal autoimmune myocarditis and other autoimmune diseases in BALB/c nude mice transferred with GITR low T cells’ (page unavailable) reports fatal myocarditis after transfer of T cells depleted of GITR-high regulatory cells; the Discussion says CD4+ T cells could subsequently transfer the disease. The paper does not report a decreased number of circulating regulatory T cells in patients with myocarditis. Its Discussion instead says the relevance of the animal findings to human myocarditis remains to be determined. (LLM, conf=0.88)
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Faridar, A., Thome, A. D., Zhao, W., Thonhoff, J. R., Beers, D. R., Pascual, B., Masdeu, J. C., & Appel, S. H. (2020) · Brain Communications · doi:10.1093/braincomms/fcaa112 · Cited by 105 · see citing works
“Tregs with lower CD25 expression is previously reported in certain cases of autoimmunity and might have a partial suppressor activity rather than a fully active Tregs (Liu et al., 2006; Ono et al., 2006; Bonelli et al., 2009; Coleman et al., 2012; Prado et al., 2013).”
BackgroundClinical presentation and diagnosis of myocarditis
Caforio, A. L. P., Marcolongo, R., Basso, C., & Iliceto, S. (2015) · Heart · doi:10.1136/heartjnl-2014-306363 · Cited by 103 · see citing works
Liao, G., Nayak, S., Regueiro, J. R., Berger, S. B., Detre, C., Ros, X. R., Malefyt, R. D. W., Chatila, T. A., Herzog, R. W., & Terhorst, C. (2010) · International Immunology · doi:10.1093/intimm/dxq001 · Cited by 100 · see citing works
Altara, R., Mallat, Z., Booz, G. W., & Zouein, F. A. (2016) · Journal of Immunology Research · doi:10.1155/2016/4396368 · Cited by 96 · see citing works
Detection of T cell responses to a ubiquitous cellular protein in autoimmune disease
Ito, Y., Hashimoto, M., Hirota, K., Ohkura, N., Morikawa, H., Nishikawa, H., Tanaka, A., Furu, M., Ito, H., Fujii, T., et al. (2014) · Science · doi:10.1126/science.1259077 · Cited by 94 · see citing works
Self-citationRegulatory T cells in systemic lupus erythematosus: past, present and future
Horwitz, D. A. (2008) · Arthritis Research & Therapy · doi:10.1186/ar2511 · Cited by 92 · see citing works
Regulatory T Cells, Transforming Growth Factor–β, and Immune Suppression
Wan, Y. Y., & Flavell, R. A. (2007) · Proceedings of the American Thoracic Society · doi:10.1513/pats.200701-020aw · Cited by 90 · see citing works
Jacobo, P. V., Guazzone, V. A., Jarazo-Dietrich, S., Theas, M. S., & Lustig, L. (2009) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2009.04.005 · Cited by 90 · see citing works
T cell co-stimulation and co-inhibition in cardiovascular disease: a double-edged sword
Simons, K. H., de Jong, A., Jukema, J. W., de Vries, M. R., Arens, R., & Quax, P. H. A. (2019) · Nature Reviews Cardiology · doi:10.1038/s41569-019-0164-7 · Cited by 88 · see citing works
Hashimura, Y., Nozu, K., Kanegane, H., Miyawaki, T., Hayakawa, A., Yoshikawa, N., Nakanishi, K., Takemoto, M., Iijima, K., & Matsuo, M. (2009) · Pediatric Nephrology · doi:10.1007/s00467-009-1119-8 · Cited by 88 · see citing works
“Many autoimmune or chronic inflammatory diseases in mice that are induced by severe Treg depletion resemble, both clinically and immunologically, human autoimmune/inflammatory diseases [14, 15].”
BackgroundColeman, M. M., Ruane, D., Moran, B., Dunne, P. J., Keane, J., & Mills, K. H. G. (2013) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2012-0263oc · Cited by 86 · see citing works
Foxp3+ Treg cells in humoral immunity
Wing, J. B., & Sakaguchi, S. (2013) · International Immunology · doi:10.1093/intimm/dxt060 · Cited by 82 · see citing works
Self-citationAbnormal Tr1 differentiation in multiple sclerosis
Astier, A., & Hafler, D. A. (2007) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2007.09.018 · Cited by 81 · see citing works
“, 2007), and highlevel expression of glucocorticoid-induced TNFR family-related gene/protein (GITR) (Ono et al., 2006).”
BackgroundCell-Based Therapies with T Regulatory Cells
Gliwiński, M., Iwaszkiewicz‐Grześ, D., & Trzonkowski, P. (2017) · BioDrugs · doi:10.1007/s40259-017-0228-3 · Cited by 80 · see citing works
“Similar observations on the curative role of the adoptive transfer of Tregs were reported in animal models of multiorgan inflammation [41].”
ResultChen, J., Ellison, F. M., Eckhaus, M., Smith, A. L., Keyvanfar, K., Calado, R. T., & Young, N. S. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.178.7.4159 · Cited by 79 · see citing works
GITR+ regulatory T cells in the treatment of autoimmune diseases
Petrillo, M. G., Ronchetti, S., Ricci, E., Alunno, A., Gerli, R., Nocentini, G., & Riccardi, C. (2014) · Autoimmunity Reviews · doi:10.1016/j.autrev.2014.10.011 · Cited by 77 · see citing works
Oxidant Stress, Immune Dysregulation, and Vascular Function in Type I Diabetes
Nicolls, M. R., HASKINS, K. M., & Flores, S. C. (2007) · Antioxidants and Redox Signaling · doi:10.1089/ars.2007.1631 · Cited by 75 · see citing works
Wang, S., Xie, Y., Yang, X., Wang, X., Yan, K., Zhong, Z., Wang, X., Xu, Y., Zhang, Y., Liu, F., et al. (2016) · Parasites & Vectors · doi:10.1186/s13071-015-1288-1 · Cited by 75 · see citing works
Roles for cathepsins S, L, and B in insulitis and diabetes in the NOD mouse
Hsing, L. C., Kirk, E. A., McMillen, T. S., Hsiao, S.-H., Caldwell, M., Houston, B. A., Rudensky, A. Y., & LeBoeuf, R. C. (2009) · Journal of Autoimmunity · doi:10.1016/j.jaut.2009.07.003 · Cited by 74 · see citing works
“GITR, a member of the tumor necrosis receptor family, is highly expressed on Tr cells and its expression – in comparison to CD25 – correlates better with Foxp3 expression [29].”
Ochoa‐Repáraz, J., Rynda, A., Ascón, M. A., Yang, X., Kochetkova, I., Riccardi, C., Callis, G. M., Trunkle, T., & Pascual, D. W. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.2.954 · Cited by 73 · see citing works
Martinez, N. E., Sato, F., Kawai, E., Omura, S., Chervenak, R. P., & Tsunoda, I. (2012) · Future Virology · doi:10.2217/fvl.12.44 · Cited by 71 · see citing works
Regulatory Role of CD4+T Cells in Myocarditis
Vdovenko, D., & Eriksson, U. (2018) · Journal of Immunology Research · doi:10.1155/2018/4396351 · Cited by 69 · see citing works
Regulatory T cells inhibit Th1 cell-mediated bile duct injury in murine biliary atresia
Tucker, R. M., Feldman, A. G., Fenner, E. K., & Mack, C. L. (2013) · Journal of Hepatology · doi:10.1016/j.jhep.2013.05.010 · Cited by 68 · see citing works
“Use of other methods to remove Tregs in vivo in BA-resistant mice, such as Foxp3-DTR mice [29] or use of anti-GITR antibodies [38], may result in a more severe reconstitution of disease.”
GITR-GITRL System, A Novel Player in Shock and Inflammation
Krausz, L. T., Bianchini, R., Ronchetti, S., Fettucciari, K., Nocentini, G., & Riccardi, C. (2007) · The Scientific World JOURNAL · doi:10.1100/tsw.2007.106 · Cited by 65 · see citing works
“Downregulation of Foxp3 expression in human type 1 regulatory T cells (Tr1) causes the loss of suppressor activity together with the loss of GITR and iCTLA-4 expression but not CD25 expression[49].”
BackgroundResultInfluentialCD4 + CD25 low GITR + cells: A novel human CD4 + T‐cell population with regulatory activity
Bianchini, R., Bistoni, O., Alunno, A., Petrillo, M. G., Ronchetti, S., Sportoletti, P., Bartoloni, E., Nocentini, G., Gerli, R., & Riccardi, C. (2011) · European Journal of Immunology · doi:10.1002/eji.201040943 · Cited by 64 · see citing works
SHIP limits immunoregulatory capacity in the T-cell compartment
Collazo, M. M., Wood, D., Paraiso, K. H. T., Lund, E., Engelman, R. W., Le, C.-T., Stauch, D., Kotsch, K., & Kerr, W. G. (2009) · Blood · doi:10.1182/blood-2008-09-181164 · Cited by 61 · see citing works
Coleman, M. M., Finlay, C. M., Moran, B., Keane, J., Dunne, P. J., & Mills, K. H. G. (2011) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.2011.00927.x · Cited by 59 · see citing works
“…the lung A number of studies have reported that CD4+ T cells that lack CD25 (CD4+CD25 ) isolated from secondary lymphoid tissue have suppressive activity (Annacker et al., 2001; Lehmann et al., 2002; Ono et al., 2006); however, a functional role of such cells in the lung has yet to be determined.”
BackgroundEmerging pharmacologic targets and treatments for myocarditis
Jensen, L. D., & Marchant, D. (2016) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2016.03.006 · Cited by 59 · see citing works
Modulating Protective and Pathogenic CD4+ Subsets via CD137 in Type 1 Diabetes
Irie, J., Wu, Y., Kachapati, K., Mittler, R. S., & Ridgway, W. M. (2006) · Diabetes · doi:10.2337/db06-0793 · Cited by 56 · see citing works
“We confirmed the observation recently published by Sakaguchi and colleagues (36,37) that CD25-depleted CD4 cells transfer several autoimmune diseases.”
ResultExosomes as a novel cell‐free therapeutic approach in gastrointestinal diseases
Baghaei, K., Tokhanbigli, S., Asadzadeh, H., Nmaki, S., Zali, M. R., & Hashemi, S. M. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.27934 · Cited by 56 · see citing works
Dysregulated CD4+ T Cells and microRNAs in Myocarditis
Wang, J., & Han, B. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00539 · Cited by 53 · see citing works
“Depletion of Treg cells in nude mice by adoptive transfer of GITR-deficient CD4+ T cells led to the spontaneous development of fatal autoimmune myocarditis (19).”
BackgroundLarge functional repertoire of regulatory T-cell suppressible autoimmune T cells in scurfy mice
Sharma, R., Jarjour, W. N., Zheng, L., Gaskin, F., Fu, S. M., & Ju, S. (2007) · Journal of Autoimmunity · doi:10.1016/j.jaut.2007.04.001 · Cited by 54 · see citing works
“The prevalence and frequency of organ-specific autoimmune diseases were higher in NOD-SCID recipients transferred with T cells depleted of glucocorticoid-induced TNF receptor family-related protein (11).”
BackgroundAutoimmune Myocarditis, Old Dogs and New Tricks.
Won, T., Song, E. J., Kalinoski, H. M., Moslehi, J. J., & Čiháková, D. (2024) · Circulation Research · doi:10.1161/circresaha.124.323816 · Cited by 51 · see citing works
Yokoyama, T., Matsuda, S., Takae, Y., Wada, N. A., Nishikawa, T., Amagai, M., & Koyasu, S. (2011) · International Immunology · doi:10.1093/intimm/dxr020 · Cited by 50 · see citing works
Myosin-primed tolerogenic dendritic cells ameliorate experimental autoimmune myocarditis
Lee, J.-H., Kim, T.-H., Park, H. E., Lee, E. G., Jung, N.-C., Song, J.-Y., Seo, H. G., Seung, K.-B., Chang, K., & Lim, D.-S. (2014) · Cardiovascular Research · doi:10.1093/cvr/cvt246 · Cited by 50 · see citing works
“The aim of the present study was to generate tDCs ex vivo by exposing imDCs to TNF-a and cardiac myosin and to investigate their contribution to the regulation of myocarditis in an EAM mouse model.(30,31)”
Zhang, L., Liu, Z., Ye, J., Sha, M., Qian, H., Bu, X., Luan, Z., Xu, X., Huang, A., Yuan, D., et al. (2014) · Cell Biology International · doi:10.1002/cbin.10244 · Cited by 48 · see citing works
“Foxp3, a member of forkhead transcription factor family, is the most specific marker for Treg cells (Ono et al., 2006).”
BackgroundExpansion of regulatory GITR+CD25low/-CD4+ T cells in systemic lupus erythematosus patients
Nocentini, G., Alunno, A., Petrillo, M. G., Bistoni, O., Bartoloni, E., Caterbi, S., Ronchetti, S., Migliorati, G., Riccardi, C., & Gerli, R. (2014) · Arthritis Research & Therapy · doi:10.1186/s13075-014-0444-x · Cited by 48 · see citing works
“Moreover, regulatory functions can be exerted also by CD4CD25 cells [20,21], and in SLE patients, CD4CD25FoxP3 cells with a regulatory activity have been described [14,22].”
BackgroundImmunomodulatory effects of Trichinella spiralis-derived excretory–secretory antigens
Radovic, I., Gruden‐Movsesijan, A., Ilić, N., Cvetković, J., Mojsilović, S. B., Dević, M., & Sofronić‐Milosavljević, L. (2015) · Immunologic Research · doi:10.1007/s12026-015-8626-4 · Cited by 43 · see citing works
“CD4CD25Foxp3 T cells were found in both rodents and humans, and it was shown that they possess suppressive activity [44, 45].”
BackgroundAnti-heart autoantibodies in familial dilated cardiomyopathy
Caforio, A. L. P., Vinci, A., & Iliceto, S. (2008) · Autoimmunity · doi:10.1080/08916930802031546 · Cited by 43 · see citing works
“[82] Ono M, Shimizu J, Miyachi Y, Sakaguchi S.”
BackgroundLv, K., Xu, W., Wang, C., Niki, T., Hirashima, M., & Xiong, S. (2011) · Clinical Immunology · doi:10.1016/j.clim.2011.03.017 · Cited by 42 · see citing works
Genetically determined myocarditis: clinical presentation and immunological characteristics
Caforio, A. L. P., & Iliceto, S. (2008) · Current Opinion in Cardiology · doi:10.1097/hco.0b013e3282fbf572 · Cited by 37 · see citing works
Dendritic Cells and T Cells in the Regulation of Cutaneous Immunity
Loser, K., & Beissert, S. (2007) · Advances in Dermatology · doi:10.1016/j.yadr.2007.07.014 · Cited by 52 · see citing works
Maintaining immunological tolerance with Foxp3
Mays, L. E., & Chen, Y. H. (2007) · Cell Research · doi:10.1038/cr.2007.84 · Cited by 34 · see citing works
Haga, T., Suzuki, J., Kosuge, H., Ogawa, M., Saiki, H., Haraguchi, G., Maejima, Y., Isobe, M., & Uede, T. (2009) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2009.02.003 · Cited by 34 · see citing works
Control of inflammatory heart disease by CD4+ T cells
Barin, J. G., & Čiháková, D. (2013) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12134 · Cited by 33 · see citing works
Omokaro, S. O., Desierto, M. J., Eckhaus, M., Ellison, F. M., Chen, J., & Young, N. S. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0801430 · Cited by 33 · see citing works
Elshal, M. F., Almalki, A., Hussein, H., & Khan, J. A. (2013) · African Journal of Traditional Complementary and Alternative Medicines · doi:10.4314/ajtcam.v10i5.8 · Cited by 32 · see citing works
“Glucocorticoids are important in the management of chronic, noninfectious, inflammatory and rheumatic diseases (Goulding, 2004, Meduri et al., 2002, Ono et al., 2006).”
BackgroundNovel strategies to eliminate persistent viral infections
Martinic, M. M. A., & von Herrath, M. G. (2008) · Trends in Immunology · doi:10.1016/j.it.2007.12.002 · Cited by 32 · see citing works
Jarosch, S., Köhlen, J., Ghimire, S., Orberg, E. T., Hammel, M., Gaag, D., Evert, M., Janssen, K., Hiergeist, A., Gessner, A., et al. (2023) · Cell Reports Medicine · doi:10.1016/j.xcrm.2023.101125 · Cited by 32 · see citing works
Regulation of Th-1 T cell-dominated immunity to Neisseria meningitidis within the human mucosa
Davenport, V., Groves, E., Hobbs, C., Williams, N., & Heyderman, R. S. (2006) · Cellular Microbiology · doi:10.1111/j.1462-5822.2006.00851.x · Cited by 31 · see citing works
“Identification and depletion of mucosal cells expressing the Foxp3 gene (Lundgren et al., 2005) may have provided better discrimination but these contain both CD25+ and CD25– populations (Ono et al., 2006).”
Regulatory T Cells Control Th2-Dominant Murine Autoimmune Gastritis
Harakal, J., Rival, C. M., Qiao, H., & Tung, K. S. K. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1502344 · Cited by 31 · see citing works
“GITR and CD25 are critical for Treg costimulation (65) and survival (27, 66), and Tregs with a low level of CD25 are more prone to conversion into pathogenic effector cells”
BackgroundGuo, K. X., Sun, X., Gu, Y., Wang, Z., Huang, J., & Zhu, X. (2016) · Parasites & Vectors · doi:10.1186/s13071-016-1857-y · Cited by 29 · see citing works
Nagahama, K., Fehervari, Z. T., Oida, T., Yamaguchi, T., Ogawa, O., & Sakaguchi, S. (2009) · International Immunology · doi:10.1093/intimm/dxp005 · Cited by 28 · see citing works
Self-citationEvaluation of FoxP3 Expression in Peripheral T-Cell Lymphoma
Bonzheim, I., Geissinger, E., Tinguely, M., Roth, S., Grieb, T., Reimer, P., Wilhelm, M., Rosenwald, A., Müller‐Hermelink, H. K., & Rüdiger, T. (2008) · American Journal of Clinical Pathology · doi:10.1309/l65gweq803pp6vx1 · Cited by 27 · see citing works
Immune cell diversity contributes to the pathogenesis of myocarditis
Hua, X., & Song, J. (2019) · Heart Failure Reviews · doi:10.1007/s10741-019-09799-w · Cited by 37 · see citing works
CD4+CD25-FoxP3+T cells: a distinct subset or a heterogeneous population?
Zohouri, M., Mehdipour, F., Razmkhah, M., Faghih, Z., & Ghaderi, A. A. (2020) · International Reviews of Immunology · doi:10.1080/08830185.2020.1797005 · Cited by 26 · see citing works
Direct control of B cells by Tregs: An opportunity for long-term modulation of the humoral response
Weingartner, E., & Golding, A. (2017) · Cellular Immunology · doi:10.1016/j.cellimm.2017.05.007 · Cited by 26 · see citing works
Role of immune cells in the pathogenesis of myocarditis
Liu, K., & Han, B. (2023) · Journal of Leukocyte Biology · doi:10.1093/jleuko/qiad143 · Cited by 34 · see citing works
Antigen-specific immunotherapies in type 1 diabetes
Zhang, X., Dong, Y., Liu, D., Yang, L., Xu, J., & Wang, Q. (2022) · Journal of Trace Elements in Medicine and Biology · doi:10.1016/j.jtemb.2022.127040 · Cited by 24 · see citing works
Controversies concerning thymus‐derived regulatory T cells: fundamental issues and a new perspective
Ono, M., & Tanaka, R. J. (2015) · Immunology and Cell Biology · doi:10.1038/icb.2015.65 · Cited by 24 · see citing works
“41 .”
Self-citationFeedback loop of immune regulation by CD4+CD25+ Treg
Jung, Y.-J., & Seoh, J. (2008) · Immunobiology · doi:10.1016/j.imbio.2008.09.004 · Cited by 24 · see citing works
Yamamoto, T., Fujiwara, K., Tsubota, Y., Kageyama‐Yahara, N., Hayashi, S., & Kadowaki, M. (2016) · International Archives of Allergy and Immunology · doi:10.1159/000445433 · Cited by 24 · see citing works
Transcription factors in autoimmune diseases
Stanford, L. P. (2008) · Frontiers in bioscience · doi:10.2741/3001 · Cited by 24 · see citing works
“However, more broadly, Foxp3 likely affects the pathogenesis of multiple autoimmune diseases via its role in diseasesuppressive Tregs, including inflammatory arthritis (168, 169), inflammatory bowel disease (170, 171), multiple sclerosis (172, 173), lupus (174-176), pemphigus (177), pemphigoid (178), myasthenia gravis…”
BackgroundZhang, Y., Zhang, M., Li, X., Tang, Z., He, L., & Lv, K. (2017) · Molecular Immunology · doi:10.1016/j.molimm.2017.01.013 · Cited by 23 · see citing works
Mechanisms regulating the development and function of natural regulatory T cells
Gupta, S., Shang, W., & Sun, Z. (2008) · Archivum Immunologiae et Therapiae Experimentalis · doi:10.1007/s00005-008-0015-4 · Cited by 23 · see citing works
“Adoptive transfer of GITRhigh-depleted T cells (both CD25– and CD25+) induced autoimmune diseases which were more severe than those induced by T cells depleted of CD4+CD25+ Treg [108].”
BackgroundFujii, H., Josse, J., Tanioka, M., Miyachi, Y., Husson, F., & Ono, M. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1402695 · Cited by 22 · see citing works
Self-citationNishikubo, K., Imanaka‐Yoshida, K., Tamaki, S., Hiroe, M., Yoshida, T., Adachi, Y., & Yasutomi, Y. (2007) · Journal of Autoimmunity · doi:10.1016/j.jaut.2007.07.001 · Cited by 21 · see citing works
Dilated cardiomyopathy and severe heart failure. An update for pediatricians
Caviedes, P., Fernández, T. C., Valenzuela, M. L., & Pablo Cruces, R. (2018) · Archivos Argentinos de Pediatria · doi:10.5546/aap.2018.eng.e421 · Cited by 20 · see citing works
- Authors
- Ono, M., Shimizu, J., Miyachi, Y., & Sakaguchi, S.
- Affiliations
- Kyoto University (JP)
- Tokyo Metropolitan Institute of Gerontology (JP)
- Venue
- The Journal of Immunology
- Publisher
- Oxford University Press (OUP)
- Published
- 2006-04
- Volume
- 176
- Issue
- 8
- Pages
- 4748-4756
- ISSN
- 0022-1767 (ISSN-L)
- 1550-6606
- OpenAlex
- W2116252546
- Cited by
- 162
- References
- 52
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 6 · 2023: 5 · 2022: 4 · 2021: 1 · 2020: 9 · 2019: 3 · 2018: 6 · 2017: 8 · 2016: 14 · 2015: 9 · 2014: 7 · 2013: 9 · 2012: 4
- FWCI
- 6.88
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The Journal of Immunology (publishedVersion)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Health Sciences › Medicine › Neurology › Myasthenia Gravis and Thymoma
- Life Sciences › Immunology and Microbiology › Immunology › Psoriasis: Treatment and Pathogenesis
- Keywords
- GITR, Foxp3, regulatory T cells, CD25+ T cells, autoimmune myocarditis, type 1 diabetes, autoreactive T cells, T cell transfer, NOD mice, giant cell myocarditis
- MeSH terms
- Animals, Autoimmune Diseases, Female, Inflammation, Mice, Inbred BALB C, Mice, Nude, Myocarditis, Receptors, Interleukin-2, Gene Expression, Mice, SCID, Mice, Inbred NOD, Receptors, Nerve Growth Factor, Receptors, Tumor Necrosis Factor, Adoptive Transfer, T-Lymphocytes, Regulatory, Mice, Forkhead Transcription Factors, Glucocorticoid-Induced TNFR-Related Protein
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