Cytokines and T Helper Cells in Diabetic Nephropathy Pathogenesis — Oak Academic Publishing
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Cytokines and T Helper Cells in Diabetic Nephropathy Pathogenesis
General Pathology and Nephropathology Service, Institute of Biological and Natural Sciences of Federal University of Triangulo Mineiro, Uberaba, Brazil
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Immunology, Institute of Biological and Natural Sciences of Federal University of Triangulo Mineiro, Uberaba, Brazil
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General Pathology and Nephropathology Service, Institute of Biological and Natural Sciences of Federal University of Triangulo Mineiro, Uberaba, Brazil
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General Pathology and Nephropathology Service, Institute of Biological and Natural Sciences of Federal University of Triangulo Mineiro, Uberaba, Brazil
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General Pathology and Nephropathology Service, Institute of Biological and Natural Sciences of Federal University of Triangulo Mineiro, Uberaba, Brazil
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General Pathology and Nephropathology Service, Institute of Biological and Natural Sciences of Federal University of Triangulo Mineiro, Uberaba, Brazil
,
General Pathology and Nephropathology Service, Institute of Biological and Natural Sciences of Federal University of Triangulo Mineiro, Uberaba, Brazil
,
General Pathology and Nephropathology Service, Institute of Biological and Natural Sciences of Federal University of Triangulo Mineiro, Uberaba, Brazil
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General Pathology and Nephropathology Service, Institute of Biological and Natural Sciences of Federal University of Triangulo Mineiro, Uberaba, Brazil
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General Pathology, Institute of Tropical Pathology and Public Health of Federal University of Goiás, Goiania, Brazil
1 General Pathology and Nephropathology Service, Institute of Biological and Natural Sciences of Federal University of Triangulo Mineiro, Uberaba, Brazil
2 Immunology, Institute of Biological and Natural Sciences of Federal University of Triangulo Mineiro, Uberaba, Brazil
3 General Pathology and Nephropathology Service, Institute of Biological and Natural Sciences of Federal University of Triangulo Mineiro, Uberaba, Brazil
4 General Pathology and Nephropathology Service, Institute of Biological and Natural Sciences of Federal University of Triangulo Mineiro, Uberaba, Brazil
5 General Pathology and Nephropathology Service, Institute of Biological and Natural Sciences of Federal University of Triangulo Mineiro, Uberaba, Brazil
6 General Pathology and Nephropathology Service, Institute of Biological and Natural Sciences of Federal University of Triangulo Mineiro, Uberaba, Brazil
7 General Pathology and Nephropathology Service, Institute of Biological and Natural Sciences of Federal University of Triangulo Mineiro, Uberaba, Brazil
8 General Pathology and Nephropathology Service, Institute of Biological and Natural Sciences of Federal University of Triangulo Mineiro, Uberaba, Brazil
9 General Pathology and Nephropathology Service, Institute of Biological and Natural Sciences of Federal University of Triangulo Mineiro, Uberaba, Brazil
10 General Pathology, Institute of Tropical Pathology and Public Health of Federal University of Goiás, Goiania, Brazil
Diabetic Nephropathy (DN) is considered the main cause of end stage kidney disease around the world. However, its pathogenesis is not completely established. More than just a direct consequence of chronic glycemic changes, recent studies had suggested Diabetic Nephropathy could be considered an inflammatory disease. It has been shown that concentrations of pro-inflammatory cytokines, as IL-1, IL-6, IL-18, IL-33, IFN- γ and TNF- α actively participate in development and progression of DN, and thus, are involved in pathogenesis. Besides, changes in acquired immune response, especially the presence of cellular immune response profiles of pro-inflammatory and effector nature, mainly Th1 and Th17, as the imbalance between interaction of cytokines and T regulatory cells, foment the onset and progression of DN. Here we summarize the main evidences that support the critical role of the immune system in this condition. These new conceptual advances in DN understanding are essential for development of new the rapeutical strategies and prognostic factors, which could be protagonists or adjuvants to the current ones, leading ultimately to a better clinical management of DN patients.
Association, A.D. (2014) Standards of Medical Care in Diabetes: 2014. Diabetes Care, 37, S14-S80. http://dx.doi.org/10.2337/dc14-S014
Andersen, A.R., Christiansen, J.S., Andersen, J.K., Kreiner, S. and Deckert, T. (1983) Diabetic Nephropathy in Type 1 (Insulin-Dependent) Diabetes: An Epidemiological Study. Diabetologia, 25, 496-501. http://dx.doi.org/10.1007/BF00284458
Murussi, M., Baglio, P., Gross, J.L. and Silveiro, S.P. (2002) Risk Factors for Microalbuminuria and Macroalbuminuria in Type 2 Diabetic Patients: A 9-Year Follow-Up Study. Diabetes Care, 25, 1101-1103. http://dx.doi.org/10.2337/diacare.25.6.1101
Forsblom, C.M., Groop, P.H., Ekstrand, A., Totterman, K.J., Sane, T., Saloranta, C. and Groop, L. (1998) Predictors of Progression from Normoalbuminuria to Microalbuminuria in NIDDM. Diabetes Care, 21, 1932-1938. http://dx.doi.org/10.2337/diacare.21.11.1932
Ravid, M., Brosh, D., Ravid-Safran, D., Levy, Z. and Rachmani, R. (1998) Main Risk Factors for Nephropathy in Type 2 Diabetes Mellitus Are Plasma Cholesterol Levels, Mean Blood Pressure, and Hyperglycemia. Archives of Internal Medicine, 158, 998-1004. http://dx.doi.org/10.1001/archinte.158.9.998
Adler, A.I., Stevens, R.J., Manley, S.E., Bilous, R.W., Cull, C.A., Holman, R.R. and UKPDS Group (2003) Development and Progression of Nephropathy in Type 2 Diabetes: The United Kingdom Prospective Diabetes Study (UKPDS 64). Kidney International, 63, 225-232. http://dx.doi.org/10.1046/j.1523-1755.2003.00712.x
Hayashi, H., Karasawa, R., Inn, H., Saitou, T., Ueno, M., Nishi, S., Suzuki, Y., Ogino, S., Maruyama, Y. and Kouda, Y. (1992) An Electron Microscopic Study of Glomeruli in Japanese Patients with Non-Insulin Dependent Diabetes Mellitus. Kidney International, 41, 749-757. http://dx.doi.org/10.1038/ki.1992.117
Dronavalli, S., Duka, I. and Bakris, G.L. (2008) The Pathogenesis of Diabetic Nephropathy. Nature Clinical Practice Endocrinology & Metabolism, 4, 444-452. http://dx.doi.org/10.1038/ncpendmet0894
Kanwar, Y.S., Wada, J., Sun, L., Xie, P., Wallner, E.I., Chen, S., Chugh, S. and Danesh, F.R. (2008) Diabetic Nephropathy: Mechanisms of Renal Disease Progression. Experimental Biology and Medicine (Maywood), 233, 4-11. http://dx.doi.org/10.3181/0705-MR-134
Mauer, S.M., Steffes, M.W., Ellis, E.N., Sutherland, D.E., Brown, D.M. and Goetz, F.C. (1984) Structural-Functional Relationships in Diabetic Nephropathy. Journal of Clinical Investigation, 74, 1143-1155. http://dx.doi.org/10.1172/JCI111523
Dalla Vestra, M., Saller, A., Bortoloso, E., Mauer, M. and Fioretto, P. (2000) Structural Involvement in Type 1 and Type 2 Diabetic Nephropathy. Diabetes & Metabolism, 26, 8-14.
Ziyadeh, F.N. (1993) The Extracellular Matrix in Diabetic Nephropathy. American Journal of Kidney Diseases, 22, 736-744. http://dx.doi.org/10.1016/S0272-6386(12)80440-9
Mason, R.M. and Wahab, N.A. (2003) Extracellular Matrix Metabolism in Diabetic Nephropathy. Journal of the American Society of Nephrology, 14, 1358-1373. http://dx.doi.org/10.1097/01.ASN.0000065640.77499.D7
Matheson, A., Willcox, M.D., Flanagan, J. and Walsh, B.J. (2010) Urinary Biomarkers Involved in Type 2 Diabetes: A Review. Diabetes/Metabolism Research and Reviews, 26, 150-171. http://dx.doi.org/10.1002/dmrr.1068
Ponchiardi, C., Mauer, M. and Najafian, B. (2013) Temporal Profile of Diabetic Nephropathy Pathologic Changes. Current Diabetes Reports, 13, 592-599. http://dx.doi.org/10.1007/s11892-013-0395-7
Wada, J. and Makino, H. (2013) Inflammation and the Pathogenesis of Diabetic Nephropathy. Clinical Science, 124, 139-152. http://dx.doi.org/10.1042/CS20120198
Rivero, A., Mora, C., Muros, M., García, J., Herrera, H. and Navarro-González, J.F. (2009) Pathogenic Perspectives for the Role of Inflammation in Diabetic Nephropathy. Clinical Science, 116, 479-492. http://dx.doi.org/10.1042/CS20080394
Navarro-González, J.F., Mora-Fernández, C., Muros de Fuentes, M. and García-Pérez, J. (2011) Inflammatory Molecules and Pathways in the Pathogenesis of Diabetic Nephropathy. Nature Reviews Nephrology, 7, 327-340. http://dx.doi.org/10.1038/nrneph.2011.51
Hickey, F.B. and Martin, F. (2013) Diabetic Kidney Disease and Immune Modulation. Curr Current Opinion in Pharmacology, 13, 602-612. http://dx.doi.org/10.1016/j.coph.2013.05.002
Barutta, F., Bruno, G., Grimaldi, S. and Gruden, G. (2014) Inflammation in Diabetic Nephropathy: Moving toward Clinical Biomarkers and Targets for Treatment. Endocrine, 48, 730-742. http://dx.doi.org/10.1007/s12020-014-0437-1
Schmidt, M.I., Duncan, B.B., Sharrett, A.R., Lindberg, G., Savage, P.J., Offenbacher, S., Azambuja, M.I., Tracy, R.P. and Heiss, G. (1999) Markers of Inflammation and Prediction of Diabetes Mellitus in Adults (Atherosclerosis Risk in Communities Study): A Cohort Study. The Lancet, 353, 1649-1652. http://dx.doi.org/10.1016/S0140-6736(99)01046-6
Pradhan, A.D., Manson, J.E., Rifai, N., Buring, J.E. and Ridker, P.M. (2001) C-Reactive Protein, Interleukin 6, and Risk of Developing Type 2 Diabetes Mellitus. JAMA, 286, 327-334. http://dx.doi.org/10.1001/jama.286.3.327
Spranger, J., Kroke, A., Mohlig, M., Hoffmann, K., Bergmann, M.M., Ristow, M., Boeing, H. and Pfeiffer, A.F. (2003) Inflammatory Cytokines and the Risk to Develop Type 2 Diabetes: Results of the Prospective Population-Based European Prospective Investigation into Cancer and Nutrition (EPIC)-Potsdam Study. Diabetes, 52, 812-817. http://dx.doi.org/10.2337/diabetes.52.3.812
Dalla Vestra, M., Mussap, M., Gallina, P., Bruseghin, M., Cernigoi, A.M., Saller, A., Plebani, M. and Fioretto, P. (2005) Acute-Phase Markers of Inflammation and Glomerular Structure in Patients with Type 2 Diabetes. Journal of the American Society of Nephrology, 16, S78-S82. http://dx.doi.org/10.1681/ASN.2004110961
Hasegawa, G., Nakano, K., Sawada, M., Uno, K., Shibayama, Y., Ienaga, K. and Kondo, M. (1991) Possible Role of Tumor Necrosis Factor and Interleukin-1 in the Development of Diabetic Nephropathy. Kidney International, 40, 1007-1012. http://dx.doi.org/10.1038/ki.1991.308
Harjutsalo, V. and Groop, P.H. (2014) Epidemiology and Risk Factors for Diabetic Kidney Disease. Advances in Chronic Kidney Disease, 21, 260-266. http://dx.doi.org/10.1053/j.ackd.2014.03.009
Pickup, J.C., Chusney, G.D., Thomas, S.M. and Burt, D. (2000) Plasma Interleukin-6, Tumour Necrosis Factor Alpha and Blood Cytokine Production in Type 2 Diabetes. Life Sciences, 67, 291-300. http://dx.doi.org/10.1016/S0024-3205(00)00622-6
Festa, A., D’Agostino, R., Howard, G., Mykkanen, L., Tracy, R.P. and Haffner, S.M. (2000) Inflammation and Microalbuminuria in Nondiabetic and Type 2 Diabetic Subjects: The Insulin Resistance Atherosclerosis Study. Kidney International, 58, 1703-1710. http://dx.doi.org/10.1046/j.1523-1755.2000.00331.x
Bruno, G., Merletti, F., Biggeri, A., Bargero, G., Ferrero, S., Pagano, G., Cavallo Perin, P. and Study, C.M. (2003) Progression to Overt Nephropathy in Type 2 Diabetes: The Casale Monferrato Study. Diabetes Care, 26, 2150-2155. http://dx.doi.org/10.2337/diacare.26.7.2150
Navarro, J.F., Mora, C., Maca, M. and Garca, J. (2003) Inflammatory Parameters Are Independently Associated with Urinary Albumin in Type 2 Diabetes Mellitus. American Journal of Kidney Diseases, 42, 53-61. http://dx.doi.org/10.1016/S0272-6386(03)00408-6
Awad, A.S., Kinsey, G.R., Khutsishvili, K., Gao, T., Bolton, W.K. and Okusa, M.D. (2011) Monocyte/Macrophage Chemokine Receptor CCR2 Mediates Diabetic Renal Injury. American Journal of Physiology-Renal Physiology, 301, F1358-F1366. http://dx.doi.org/10.1152/ajprenal.00332.2011
Chow, F.Y., Nikolic-Paterson, D.J., Ozols, E., Atkins, R.C. and Tesch, G.H. (2005) Intercellular Adhesion Molecule-1 Deficiency Is Protective against Nephropathy in Type 2 Diabetic db/db Mice. Journal of the American Society of Nephrology, 16, 1711-1722. http://dx.doi.org/10.1681/ASN.2004070612
Ostendorf, T., Burg, M. and Floege, J. (1996) Cytokines and Glomerular Injury. Kidney and Blood Pressure Research, 19, 281-289. http://dx.doi.org/10.1159/000174088
Noronha, I.L., Niemir, Z., Stein, H. and Waldherr, R. (1995) Cytokines and Growth Factors in Renal Disease. Nephrology Dialysis Transplantation, 10, 775-786.
Navarro-González, J.F. and Mora-Fernández, C. (2008) The Role of Inflammatory Cytokines in Diabetic Nephropathy. Journal of the American Society of Nephrology, 19, 433-442. http://dx.doi.org/10.1681/ASN.2007091048
Sassy-Prigent, C., Heudes, D., Mandet, C., Bélair, M.F., Michel, O., Perdereau, B., Bariéty, J. and Bruneval, P. (2000) Early Glomerular Macrophage Recruitment in Streptozotocin-Induced Diabetic Rats. Diabetes, 49, 466-475. http://dx.doi.org/10.2337/diabetes.49.3.466
Navarro, J.F., Milena, F.J., Mora, C., León, C. and García, J. (2006) Renal Pro-Inflammatory Cytokine Gene Expression in Diabetic Nephropathy: Effect of Angiotensin-Converting Enzyme Inhibition and Pentoxifylline Administration. American Journal of Nephrology, 26, 562-570. http://dx.doi.org/10.1159/000098004
Park, C.W., Kim, J.H., Lee, J.H., Kim, Y.S., Ahn, H.J., Shin, Y.S., Kim, S.Y., Choi, E.J., Chang, Y.S., Bang, B.K. and Lee, J.W. (2000) High Glucose-Induced Intercellular Adhesion Molecule-1 (ICAM-1) Expression through an Osmotic Effect in Rat Mesangial Cells Is PKC-NF-κB-Dependent. Diabetologia, 43, 1544-1553. http://dx.doi.org/10.1007/s001250051567
Pfeilschifter, J., Pignat, W., Vosbeck, K. and Marki, F. (1989) Interleukin 1 and Tumor Necrosis Factor Synergistically Stimulate Prostaglandin Synthesis and Phospholipase A2 Release from Rat Renal Mesangial Cells. Biochemical and Biophysical Research Communications, 159, 385-394. http://dx.doi.org/10.1016/0006-291X(89)90003-X
Royall, J.A., Berkow, R.L., Beckman, J.S., Cunningham, M.K., Matalon, S. and Freeman, B.A. (1989) Tumor Necrosis Factor and Interleukin 1 Alpha Increase Vascular Endothelial Permeability. American Journal of Physiology, 257, L399-L410.
Schiering, C., Krausgruber, T., Chomka, A., Frohlich, A., Adelmann, K., Wohlfert, E.A., Pott, J., Griseri, T., Bollrath, J., Hegazy, A.N., Harrison, O.J., Owens, B.M., Lohning, M., Belkaid, Y., Fallon, P.G. and Powrie, F. (2014) The Alarmin IL-33 Promotes Regulatory T-Cell Function in the Intestine. Nature, 513, 564-568. http://dx.doi.org/10.1038/nature13577
Sattler, S., Ling, G.S., Xu, D., Hussaarts, L., Romaine, A., Zhao, H., Fossati-Jimack, L., Malik, T., Cook, H.T., Botto, M., Lau, Y.L., Smits, H.H., Liew, F.Y. and Huang, F.P. (2014) IL-10-Producing Regulatory B Cells Induced by IL-33 (BregIL-33) Effectively Attenuate Mucosal Inflammatory Responses in the Gut. Journal of Autoimmunity, 50, 107-122. http://dx.doi.org/10.1016/j.jaut.2014.01.032
Schmitz, J., Owyang, A., Oldham, E., Song, Y., Murphy, E., McClanahan, T.K., Zurawski, G., Moshrefi, M., Qin, J., Li, X., Gorman, D.M., Bazan, J.F. and Kastelein, R.A. (2005) IL-33, an Interleukin-1-Like Cytokine That Signals via the IL-1 Receptor-Related Protein ST2 and Induces T Helper Type 2-Associated Cytokines. Immunity, 23, 479-490. http://dx.doi.org/10.1016/j.immuni.2005.09.015
Anand, G., Vasanthakumar, R., Mohan, V., Babu, S. and Aravindhan, V. (2014) Increased IL-12 and Decreased IL-33 Serum Levels Are Associated with Increased Th1 and Suppressed Th2 Cytokine Profile in Patients with Diabetic Nephropathy (CURES-134). International Journal of Clinical and Experimental Pathology, 7, 8008-8015.
Demirtas, L., Turkmen, K., Kandemir, F.M., Ozkaraca, M., Kucukler, S., Gürbüzel, M. and Comakli, S. (2016) The Possible Role of Interleukin-33 as a New Player in the Pathogenesis of Contrast-Induced Nephropathy in Diabetic Rats. Renal Failure, 38, 952-960. http://dx.doi.org/10.3109/0886022X.2016.1165034
Onk, D., Onk, O.A., Turkmen, K., Erol, H.S., Ayazoglu, T.A., Keles, O.N., Halici, M. and Topal, E. (2016) Melatonin Attenuates Contrast-Induced Nephropathy in Diabetic Rats: The Role of Interleukin-33 and Oxidative Stress. Mediators of Inflammation, 2016, Article ID: 9050828.
Caner, S., Usluogullari, C.A., Balkan, F., Büyükcam, F., Kaya, C., Sacikara, M., Koca, C., Ersoy, R. and Cakir, B. (2014) Is IL-33 Useful to Detect Early Stage of Renal Failure? Renal Failure, 36, 78-80. http://dx.doi.org/10.3109/0886022X.2013.832313
Moriwaki, Y., Yamamoto, T., Shibutani, Y., Aoki, E., Tsutsumi, Z., Takahashi, S., Okamura, H., Koga, M., Fukuchi, M. and Hada, T. (2003) Elevated Levels of Interleukin-18 and Tumor Necrosis Factor-Alpha in Serum of Patients with Type 2 Diabetes Mellitus: Relationship with Diabetic Nephropathy. Metabolism, 52, 605-608. http://dx.doi.org/10.1053/meta.2003.50096
Nakamura, A., Shikata, K., Hiramatsu, M., Nakatou, T., Kitamura, T., Wada, J., Itoshima, T. and Makino, H. (2005) Serum Interleukin-18 Levels Are Associated with Nephropathy and Atherosclerosis in Japanese Patients with Type 2 Diabetes. Diabetes Care, 28, 2890-2895. http://dx.doi.org/10.2337/diacare.28.12.2890
Uciechowski, P., Schwarz, M., Gessner, J.E., Schmidt, R.E., Resch, K. and Radeke, H.H. (1998) IFN-γ Induces the High-Affinity Fc Receptor I for IgG (CD64) on Human Glomerular Mesangial Cells. European Journal of Immunology, 28, 2928-2935. http://dx.doi.org/10.1002/(SICI)1521-4141(199809)28:09 3.0.CO;2-8
Dai, S.M., Matsuno, H., Nakamura, H., Nishioka, K. and Yudoh, K. (2004) Interleukin-18 Enhances Monocyte Tumor Necrosis Factor α and Interleukin-1β Production Induced by Direct Contact with T Lymphocytes: Implications in Rheumatoid Arthritis. Arthritis & Rheumatology, 50, 432-443. http://dx.doi.org/10.1002/art.20064
Marino, E. and Cardier, J.E. (2003) Differential Effect of IL-18 on Endothelial Cell Apoptosis Mediated by TNF-α and Fas (CD95). Cytokine, 22, 142-148. http://dx.doi.org/10.1016/S1043-4666(03)00150-9
Stuyt, R.J., Netea, M.G., Geijtenbeek, T.B., Kullberg, B.J., Dinarello, C.A. and van der Meer, J.W. (2003) Selective Regulation of Intercellular Adhesion Molecule-1 Expression by Interleukin-18 and Interleukin-12 on Human Monocytes. Immunology, 110, 329-334. http://dx.doi.org/10.1046/j.1365-2567.2003.01747.x
Forbes, J.M. and Cooper, M.E. (2013) Mechanisms of Diabetic Complications. Physiological Reviews, 93, 137-188. http://dx.doi.org/10.1152/physrev.00045.2011
Mahadevan, P., Larkins, R.G., Fraser, J.R., Fosang, A.J. and Dunlop, M.E. (1995) Increased Hyaluronan Production in the Glomeruli from Diabetic Rats: A Link between Glucose-Induced Prostaglandin Production and Reduced Sulphated Proteoglycan. Diabetologia, 38, 298-305. http://dx.doi.org/10.1007/BF00400634
Suzuki, D., Miyazaki, M., Naka, R., Koji, T., Yagame, M., Jinde, K., Endoh, M., Nomoto, Y. and Sakai, H. (1995) In Situ Hybridization of Interleukin 6 in Diabetic Nephropathy. Diabetes, 44, 1233-1238. http://dx.doi.org/10.2337/diab.44.10.1233
Coleman, D.L. and Ruef, C. (1992) Interleukin-6: An Autocrine Regulator of Mesangial Cell Growth. Kidney International, 41, 604-606. http://dx.doi.org/10.1038/ki.1992.91
Dong, X., Swaminathan, S., Bachman, L.A., Croatt, A.J., Nath, K.A. and Griffin, M.D. (2007) Resident Dendritic Cells Are the Predominant TNF-Secreting Cell in Early Renal Ischemia-Reperfusion Injury. Kidney International, 71, 619-628. http://dx.doi.org/10.1038/sj.ki.5002132
Navarro, J.F., Mora, C., Muros, M. and García, J. (2006) Urinary Tumour Necrosis Factor-Alpha Excretion Independently Correlates with Clinical Markers of Glomerular and Tubulointerstitial Injury in Type 2 Diabetic Patients. Nephrology Dialysis Transplantation, 21, 3428-3434. http://dx.doi.org/10.1093/ndt/gfl469
Pestana, R.M., Domingueti, C.P., Duarte, R.C., Fóscolo, R.B., Reis, J.S., Rodrigues, A.M., Martins, L.B., Sousa, L.P., Lage, D.P., Ferreira, C.N., Ferreira, A.V., Fernandes, A.P. and Gomes, K.B. (2016) Cytokines Profile and Its Correlation with Endothelial Damage and Oxidative Stress in Patients with Type 1 Diabetes Mellitus and Nephropathy. Immunologic Research, 64, 951-960. http://dx.doi.org/10.1007/s12026-016-8806-x
Nguyen, D.V., Shaw, L.C. and Grant, M.B. (2012) Inflammation in the Pathogenesis of Microvascular Complications in Diabetes. Frontiers in Endocrinology, 3, 170. http://dx.doi.org/10.3389/fendo.2012.00170
Xiao, X., Ma, B., Dong, B., Zhao, P., Tai, N., Chen, L., Wong, F.S. and Wen, L. (2009) Cellular and Humoral Immune Responses in the Early Stages of Diabetic Nephropathy in NOD Mice. Journal of Autoimmunity, 32, 85-93. http://dx.doi.org/10.1016/j.jaut.2008.12.003
Moon, J.Y., Jeong, K.H., Lee, T.W., Ihm, C.G., Lim, S.J. and Lee, S.H. (2012) Aberrant Recruitment and Activation of T Cells in Diabetic Nephropathy. American Journal of Nephrology, 35, 164-174. http://dx.doi.org/10.1159/000334928
Lim, A.K., Ma, F.Y., Nikolic-Paterson, D.J., Kitching, A.R., Thomas, M.C. and Tesch, G.H. (2010) Lymphocytes Promote Albuminuria, but Not Renal Dysfunction or Histological Damage in a Mouse Model of Diabetic Renal Injury. Diabetologia, 53, 1772-1782. http://dx.doi.org/10.1007/s00125-010-1757-1
van Belle, T.L., Coppieters, K.T. and von Herrath, M.G. (2011) Type 1 Diabetes: Etiology, Immunology, and Therapeutic Strategies. Physiological Reviews, 91, 79-118. http://dx.doi.org/10.1152/physrev.00003.2010
Heurtier, A.H. and Boitard, C. (1997) T-Cell Regulation in Murine and Human Autoimmune Diabetes: The Role of TH1 and TH2 Cells. Diabetes & Metabolism, 23, 377-385.
Nikolajczyk, B.S., Jagannathan-Bogdan, M., Shin, H. and Gyurko, R. (2011) State of the Union between Metabolism and the Immune System in Type 2 Diabetes. Genes and Immunity, 12, 239-250. http://dx.doi.org/10.1038/gene.2011.14
Lei, L., Mao, Y., Meng, D., Zhang, X., Cui, L., Huo, Y. and Wang, Y. (2014) Percentage of Circulating CD8+ T Lymphocytes Is Associated with Albuminuria in Type 2 Diabetes Mellitus. Experimental and Clinical Endocrinology & Diabetes, 122, 27-30.
Mensah-Brown, E.P., Obineche, E.N., Galadari, S., Chandranath, E., Shahin, A., Ahmed, I., Patel, S.M. and Adem, A. (2005) Streptozotocin-Induced Diabetic Nephropathy in Rats: The Role of Inflammatory Cytokines. Cytokine, 31, 180-190. http://dx.doi.org/10.1016/j.cyto.2005.04.006
Moriya, R., Manivel, J.C. and Mauer, M. (2004) Juxtaglomerular Apparatus T-Cell Infiltration Affects Glomerular Structure in Type 1 Diabetic Patients. Diabetologia, 47, 82-88. http://dx.doi.org/10.1007/s00125-003-1253-y
Bending, J.J., Lobo-Yeo, A., Vergani, D. and Viberti, G.C. (1988) Proteinuria and Activated T-Lymphocytes in Diabetic Nephropathy. Diabetes, 37, 507-511. http://dx.doi.org/10.2337/diab.37.5.507
Abbas, A.K., Murphy, K.M. and Sher, A. (1996) Functional Diversity of Helper T Lymphocytes. Nature, 383, 787-793. http://dx.doi.org/10.1038/383787a0
Mosmann, T.R. and Sad, S. (1996) The Expanding Universe of T-Cell Subsets: Th1, Th2 and More. Immunology Today, 17, 138-146. http://dx.doi.org/10.1016/0167-5699(96)80606-2
Mosmann, T.R., Cherwinski, H., Bond, M.W., Giedlin, M.A. and Coffman, R.L. (1986) Two Types of Murine Helper T Cell Clone. I. Definition According to Profiles of Lymphokine Activities and Secreted Proteins. The Journal of Immunology, 136, 2348-2357.
Adkins, B., Leclerc, C. and Marshall-Clarke, S. (2004) Neonatal Adaptive Immunity Comes of Age. Nature Reviews Immunology, 4, 553-564. http://dx.doi.org/10.1038/nri1394
Bettelli, E., Oukka, M. and Kuchroo, V.K. (2007) TH-17 Cells in the Circle of Immunity and Autoimmunity. Nature Immunology, 8, 345-350. http://dx.doi.org/10.1038/ni0407-345
Yang, X.P., Ghoreschi, K., Steward-Tharp, S.M., Rodriguez-Canales, J., Zhu, J., Grainger, J.R., Hirahara, K., Sun, H.W., Wei, L., Vahedi, G., Kanno, Y., O’Shea, J.J. and Laurence, A. (2011) Opposing Regulation of the Locus Encoding IL-17 through Direct, Reciprocal Actions of STAT3 and STAT5. Nature Immunology, 12, 247-254. http://dx.doi.org/10.1038/ni.1995
Josefowicz, S.Z., Lu, L.F. and Rudensky, A.Y. (2012) Regulatory T Cells: Mechanisms of Differentiation and Function. Annual Review of Immunology, 30, 531-564. http://dx.doi.org/10.1146/annurev.immunol.25.022106.141623
Nunes-Alves, C., Booty, M.G., Carpenter, S.M., Jayaraman, P., Rothchild, A.C. and Behar, S.M. (2014) In Search of a New Paradigm for Protective Immunity to TB. Nature Reviews Microbiology, 12, 289-299. http://dx.doi.org/10.1038/nrmicro3230
Boissier, M.C., Assier, E., Falgarone, G. and Bessis, N. (2008) Shifting the Imbalance from Th1/Th2 to Th17/Treg: The Changing Rheumatoid Arthritis Paradigm. Joint Bone Spine, 75, 373-375. http://dx.doi.org/10.1016/j.jbspin.2008.04.005
Cheng, X., Yu, X., Ding, Y.J., Fu, Q.Q., Xie, J.J., Tang, T.T., Yao, R., Chen, Y. and Liao, Y.H. (2008) The Th17/Treg Imbalance in Patients with Acute Coronary Syndrome. Clinical Immunology, 127, 89-97. http://dx.doi.org/10.1016/j.clim.2008.01.009
Zeng, C., Shi, X., Zhang, B., Liu, H., Zhang, L., Ding, W. and Zhao, Y. (2012) The Imbalance of Th17/Th1/Tregs in Patients with Type 2 Diabetes: Relationship with Metabolic Factors and Complications. Journal of Molecular Medicine, 90, 175-186. http://dx.doi.org/10.1007/s00109-011-0816-5
Ryba-Stanislawowska, M., Skrzypkowska, M., Mysliwiec, M. and Mysliwska, J. (2013) Loss of the Balance between CD4+Foxp3+ Regulatory T Cells and CD4+IL17A+ Th17 Cells in Patients with Type 1 Diabetes. Human Immunology, 74, 701-707. http://dx.doi.org/10.1016/j.humimm.2013.01.024
Odobasic, D., Kitching, A.R., Tipping, P.G. and Holdsworth, S.R. (2005) CD80 and CD86 Costimulatory Molecules Regulate Crescentic Glomerulonephritis by Different Mechanisms. Kidney International, 68, 584-594. http://dx.doi.org/10.1111/j.1523-1755.2005.00436.x
Wu, C.C., Chen, J.S., Lu, K.C., Chen, C.C., Lin, S.H., Chu, P., Sytwu, H.K. and Lin, Y.F. (2010) Aberrant Cytokines/Chemokines Production Correlate with Proteinuria in Patients with Overt Diabetic Nephropathy. Clinica Chimica Acta, 411, 700-704. http://dx.doi.org/10.1016/j.cca.2010.01.036
Bending, D., De la Pena, H., Veldhoen, M., Phillips, J.M., Uyttenhove, C., Stockinger, B. and Cooke, A. (2009) Highly Purified Th17 Cells from BDC2.5NOD Mice Convert into Th1-Like Cells in NOD/SCID Recipient Mice. Journal of Clinical Investigation, 119, 565-572. http://dx.doi.org/10.1172/JCI37865
Bradshaw, E.M., Raddassi, K., Elyaman, W., Orban, T., Gottlieb, P.A., Kent, S.C. and Hafler, D.A. (2009) Monocytes from Patients with Type 1 Diabetes Spontaneously Secrete Proinflammatory Cytokines Inducing Th17 Cells. The Journal of Immunology, 183, 4432-4439. http://dx.doi.org/10.4049/jimmunol.0900576
Honkanen, J., Nieminen, J.K., Gao, R., Luopajarvi, K., Salo, H.M., Ilonen, J., Knip, M., Otonkoski, T. and Vaarala, O. (2010) IL-17 Immunity in Human Type 1 Diabetes. The Journal of Immunology, 185, 1959-1967. http://dx.doi.org/10.4049/jimmunol.1000788
Jagannathan-Bogdan, M., McDonnell, M.E., Shin, H., Rehman, Q., Hasturk, H., Apovian, C.M. and Nikolajczyk, B.S. (2011) Elevated Proinflammatory Cytokine Production by a Skewed T Cell Compartment Requires Monocytes and Promotes Inflammation in Type 2 Diabetes. The Journal of Immunology, 186, 1162-1172. http://dx.doi.org/10.4049/jimmunol.1002615
Galvan, D.L. and Danesh, F.R. (2016) Paradoxical Role of IL-17 in Progression of Diabetic Nephropathy. Journal of the American Society of Nephrology, 27, 657-658. http://dx.doi.org/10.1681/ASN.2015070813
Mohamed, R., Jayakumar, C., Chen, F., Fulton, D., Stepp, D., Gansevoort, R.T. and Ramesh, G. (2016) Low-Dose IL-17 Therapy Prevents and Reverses Diabetic Nephropathy, Metabolic Syndrome, and Associated Organ Fibrosis. Journal of the American Society of Nephrology, 27, 745-765. http://dx.doi.org/10.1681/ASN.2014111136
Arababadi, M.K., Nosratabadi, R., Hassanshahi, G., Yaghini, N., Pooladvand, V., Shamsizadeh, A., Hakimi, H. and Derakhshan, R. (2010) Nephropathic Complication of Type-2 Diabetes Is Following Pattern of Autoimmune Diseases? Diabetes Research and Clinical Practice, 87, 33-37. http://dx.doi.org/10.1016/j.diabres.2009.09.027
Sakaguchi, S., Ono, M., Setoguchi, R., Yagi, H., Hori, S., Fehervari, Z., Shimizu, J., Takahashi, T. and Nomura, T. (2006) Foxp3+CD25+CD4+ Natural Regulatory T Cells in Dominant Self-Tolerance and Autoimmune Disease. Immunological Reviews, 212, 8-27. http://dx.doi.org/10.1111/j.0105-2896.2006.00427.x
Xu, J., Su, H.L., Wang, J.H. and Zhang, C.H. (2009) [Role of CD4+CD25+Foxp3+ Regulatory T Cells in Type 2 Diabetic Nephropathy]. Journal of Southern Medical University, 29, 137-139.
Eller, K., Kirsch, A., Wolf, A.M., Sopper, S., Tagwerker, A., Stanzl, U., Wolf, D., Patsch, W., Rosenkranz, A.R. and Eller, P. (2011) Potential Role of Regulatory T Cells in Reversing Obesity-Linked Insulin Resistance and Diabetic Nephropathy. Diabetes, 60, 2954-2962. http://dx.doi.org/10.2337/db11-0358
Wu, C.C., Sytwu, H.K., Lu, K.C. and Lin, Y.F. (2011) Role of T Cells in Type 2 Diabetic Nephropathy. Experimental Diabetes Research, 2011, Article ID: 514738.
Singh, K., Kadesjo, E., Lindroos, J., Hjort, M., Lundberg, M., Espes, D., Carlsson, P.O., Sandler, S. and Thorvaldson, L. (2015) Interleukin-35 Administration Counteracts Established Murine Type 1 Diabetes—Possible Involvement of Regulatory T Cells. Scientific Reports, 5, Article No. 12633. http://dx.doi.org/10.1038/srep12633
Lalani, I., Bhol, K. and Ahmed, A.R. (1997) Interleukin-10: Biology, Role in Inflammation and Autoimmunity. Annals of Allergy, Asthma & Immunology, 79, 469-484. http://dx.doi.org/10.1016/S1081-1206(10)63052-9
van Exel, E., Gussekloo, J., de Craen, A.J., Frolich, M., Bootsma-Van Der Wiel, A., Westendorp, R.G. and Study, L.P. (2002) Low Production Capacity of Interleukin-10 Associates with the Metabolic Syndrome and Type 2 Diabetes : The Leiden 85-Plus Study. Diabetes, 51, 1088-1092. http://dx.doi.org/10.2337/diabetes.51.4.1088
Mysliwska, J., Zorena, K., Semetkowska-Jurkiewicz, E., Rachoń, D., Suchanek, H. and Mysliwski, A. (2005) High Levels of Circulating Interleukin-10 in Diabetic Nephropathy Patients. European Cytokine Network, 16, 117-122.
Wong, C.K., Ho, A.W., Tong, P.C., Yeung, C.Y., Kong, A.P., Lun, S.W., Chan, J.C. and Lam, C.W. (2007) Aberrant Activation Profile of Cytokines and Mitogen-Activated Protein Kinases in Type 2 Diabetic Patients with Nephropathy. Clinical & Experimental Immunology, 149, 123-131. http://dx.doi.org/10.1111/j.1365-2249.2007.03389.x
Zamauskaite, A., Yaqoob, M.M., Madrigal, J.A. and Cohen, S.B. (1999) The Frequency of Th2 Type Cells Increases with Time on Peritoneal Dialysis in Patients with Diabetic Nephropathy. European Cytokine Network, 10, 219-226.
Xu, X., Zheng, S., Yang, F., Shi, Y., Gu, Y., Chen, H., Zhang, M. and Yang, T. (2014) Increased Th22 Cells Are Independently Associated with Th17 Cells in Type 1 Diabetes. Endocrine, 46, 90-98. http://dx.doi.org/10.1007/s12020-013-0030-z
Veldhoen, M., Uyttenhove, C., van Snick, J., Helmby, H., Westendorf, A., Buer, J., Martin, B., Wilhelm, C. and Stockinger, B. (2008) Transforming Growth Factor-Bold Beta “reprograms” the Differentiation of T Helper 2 Cells and Promotes an Interleukin 9-Producing Subset. Nature Immunology, 9, 1341-1346. http://dx.doi.org/10.1038/ni.1659
Dardalhon, V., Awasthi, A., Kwon, H., Galileos, G., Gao, W., Sobel, R.A., Mitsdoerffer, M., Strom, T.B., Elyaman, W., Ho, I.C., Khoury, S., Oukka, M. and Kuchroo, V.K. (2008) IL-4 Inhibits TGF-Bold Beta-Induced Foxp3+ T Cells and, Together with TGF-Bold Beta, Generates IL-9+ IL-10+ Foxp3- Effector T Cells. Nature Immunology, 9, 1347-1355. http://dx.doi.org/10.1038/ni.1677
Mantel, P.Y. and Schmidt-Weber, C.B. (2011) Transforming Growth Factor-Beta: Recent Advances on Its Role in Immune Tolerance. In: Cuturi, M.C. and Anegon, I., Eds., Suppression and Regulation of Immune Responses, Methods in Molecular Biology, Vol. 677, Humana Press, 303-338. http://dx.doi.org/10.1007/978-1-60761-869-0_21
Beriou, G., Bradshaw, E.M., Lozano, E., Costantino, C.M., Hastings, W.D., Orban, T., Elyaman, W., Khoury, S.J., Kuchroo, V.K., Baecher-Allan, C. and Hafler, D.A. (2010) TGF-Beta Induces IL-9 Production from Human Th17 Cells. The Journal of Immunology, 185, 46-54. http://dx.doi.org/10.4049/jimmunol.1000356
Vasanthakumar, R., Mohan, V., Anand, G., Deepa, M., Babu, S. and Aravindhan, V. (2015) Serum IL-9, IL-17, and TGF-β Levels in Subjects with Diabetic Kidney Disease (CURES-134). Cytokine, 72, 109-112. http://dx.doi.org/10.1016/j.cyto.2014.10.009
Zhang, L., Li, Y.G., Li, Y.H., Qi, L., Liu, X.G., Yuan, C.Z., Hu, N.W., Ma, D.X., Li, Z.F., Yang, Q., Li, W. and Li, J.M. (2012) Increased Frequencies of Th22 Cells as Well as Th17 Cells in the Peripheral Blood of Patients with Ankylosing Spondylitis and Rheumatoid Arthritis. PLoS ONE, 7, e31000. http://dx.doi.org/10.1371/journal.pone.0031000
Kagami, S., Rizzo, H.L., Lee, J.J., Koguchi, Y. and Blauvelt, A. (2010) Circulating Th17, Th22, and Th1 Cells Are Increased in Psoriasis. Journal of Investigative Dermatology, 130, 1373-1383. http://dx.doi.org/10.1038/jid.2009.399
Ryba-Stanislawowska, M., Werner, P., Brandt, A., Mysliwiec, M. and Mysliwska, J. (2016) Th9 and Th22 Immune Response in Young Patients with Type 1 Diabetes. Immunologic Research, 64, 730-735. http://dx.doi.org/10.1007/s12026-015-8765-7