Unraveling the immunopathogenesis of glomerular disease

Clinical Immunology

Volumn 169, Issue , 2016, Pages 89-97

  Dickinson, Bonny L ^a  

^a WESTERN MICHIGAN UNIVERSITY HOMER STRYKER MD SCHOOL OF MEDICINE   (United States)

Author keywords

Adaptive immune system; Glomerulopathies; Immune complex diseases; Innate immune system; Nephritic syndrome; Nephrotic syndrome

Indexed keywords

FC RECEPTOR; IMMUNOGLOBULIN G;

ADAPTIVE IMMUNITY; B LYMPHOCYTE; DENDRITIC CELL; GLOMERULAR STRUCTURE; GLOMERULOPATHY; GLOMERULUS BASEMENT MEMBRANE; HUMAN; IMMUNOPATHOGENESIS; INNATE IMMUNITY; NEPHRITIS; NEPHROTIC SYNDROME; PHAGOCYTE; PODOCYTE; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; ANIMAL; BIOLOGICAL MODEL; GLOMERULONEPHRITIS; GLOMERULUS; IMMUNE SYSTEM; IMMUNOLOGY; PATHOLOGY;

ADAPTIVE IMMUNITY; ANIMALS; DENDRITIC CELLS; GLOMERULONEPHRITIS; HUMANS; IMMUNE SYSTEM; IMMUNITY, INNATE; KIDNEY GLOMERULUS; MODELS, IMMUNOLOGICAL; NEPHROTIC SYNDROME;

EID: 84977651964     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2016.06.011     Document Type: Review

References (125)

1. [1] Tryggvason, K., Wartiovaara, J., How does the kidney filter plasma?. Physiology (Bethesda) 20 (2005), 96–101.
2. [2] Haraldsson, B., Sorensson, J., Why do we not all have proteinuria? An update of our current understanding of the glomerular barrier. News Physiol. Sci. 19 (2004), 7–10.
3. [3] Ohlson, M., Sorensson, J., Haraldsson, B., A gel-membrane model of glomerular charge and size selectivity in series. Am. J. Physiol. Renal Physiol. 280 (2001), F396–F405.
4. [4] Farquhar, M.G., Wissig, S.L., Palade, G.E., Glomerular permeability. I. Ferritin transfer across the normal glomerular capillary wall. J. Exp. Med. 113 (1961), 47–66.
5. [5] Reitsma, S., Slaaf, D.W., Vink, H., van Zandvoort, M.A., oude Egbrink, M.G., The endothelial glycocalyx: composition, functions, and visualization. Pflugers Arch. 454 (2007), 345–359.
6. [6] Singh, A., Satchell, S.C., Neal, C.R., McKenzie, E.A., Tooke, J.E., Mathieson, P.W., Glomerular endothelial glycocalyx constitutes a barrier to protein permeability. J. Am. Soc. Nephrol. 18 (2007), 2885–2893.
7. [7] Schlondorff, D., Banas, B., The mesangial cell revisited: no cell is an island. J. Am. Soc. Nephrol. 20 (2009), 1179–1187.
8. [8] Scindia, Y.M., Deshmukh, U.S., Bagavant, H., Mesangial pathology in glomerular disease: targets for therapeutic intervention. Adv. Drug Deliv. Rev. 62 (2010), 1337–1343.
9. [9] Miner, J.H., Renal basement membrane components. Kidney Int. 56 (1999), 2016–2024.
10. [10] Hudson, B.G., Reeders, S.T., Tryggvason, K., Type IV collagen: structure, gene organization, and role in human diseases. Molecular basis of Goodpasture and Alport syndromes and diffuse leiomyomatosis. J. Biol. Chem. 268 (1993), 26033–26036.
11. [11] Greka, A., Mundel, P., Cell biology and pathology of podocytes. Annu. Rev. Physiol. 74 (2012), 299–323.
12. [12] Grahammer, F., Schell, C., Huber, T.B., The podocyte slit diaphragm—from a thin grey line to a complex signalling hub. Nat. Rev. Nephrol. 9 (2013), 587–598.
13. [13] Boute, N., Gribouval, O., Roselli, S., et al. NPHS2, encoding the glomerular protein podocin, is mutated in autosomal recessive steroid-resistant nephrotic syndrome. Nat. Genet. 24 (2000), 349–354.
14. [14] Roselli, S., Gribouval, O., Boute, N., et al. Podocin localizes in the kidney to the slit diaphragm area. Am. J. Pathol. 160 (2002), 131–139.
15. [15] Ciani, L., Patel, A., Allen, N.D., ffrench-Constant, C., Mice lacking the giant protocadherin mFAT1 exhibit renal slit junction abnormalities and a partially penetrant cyclopia and anophthalmia phenotype. Mol. Cell. Biol. 23 (2003), 3575–3582.
16. [16] Donoviel, D.B., Freed, D.D., Vogel, H., et al. Proteinuria and perinatal lethality in mice lacking NEPH1, a novel protein with homology to NEPHRIN. Mol. Cell. Biol. 21 (2001), 4829–4836.
17. [17] Kestila, M., Lenkkeri, U., Mannikko, M., et al. Positionally cloned gene for a novel glomerular protein—nephrin—is mutated in congenital nephrotic syndrome. Mol. Cell 1 (1998), 575–582.
18. [18] Furukawa, T., Ohno, S., Oguchi, H., Hora, K., Tokunaga, S., Furuta, S., Morphometric study of glomerular slit diaphragms fixed by rapid-freezing and freeze-substitution. Kidney Int. 40 (1991), 621–624.
19. [19] Rodewald, R., Karnovsky, M.J., Porous substructure of the glomerular slit diaphragm in the rat and mouse. J. Cell Biol. 60 (1974), 423–433.
20. [20] Pavenstadt, H., Kriz, W., Kretzler, M., Cell biology of the glomerular podocyte. Physiol. Rev. 83 (2003), 253–307.
21. [21] Wartiovaara, J., Ofverstedt, L.G., Khoshnoodi, J., et al. Nephrin strands contribute to a porous slit diaphragm scaffold as revealed by electron tomography. J. Clin. Invest. 114 (2004), 1475–1483.
22. [22] Shen, L., Rock, K.L., Priming of T cells by exogenous antigen cross-presented on MHC class I molecules. Curr. Opin. Immunol. 18 (2006), 85–91.
23. [23] Koga, T., Ichinose, K., Tsokos, G.C., T cells and IL-17 in lupus nephritis. Clin. Immunol., 2016, 10.1016/j.clim.2016.04.010.
24. [24] Liu, L.L., Qin, Y., Cai, J.F., et al. Th17/Treg imbalance in adult patients with minimal change nephrotic syndrome. Clin. Immunol. 139 (2011), 314–320.
25. [25] Ooi, J.D., Phoon, R.K., Holdsworth, S.R., Kitching, A.R., IL-23, not IL-12, directs autoimmunity to the Goodpasture antigen. J. Am. Soc. Nephrol. 20 (2009), 980–989.
26. [26] Paust, H.J., Ostmann, A., Erhardt, A., et al. Regulatory T cells control the Th1 immune response in murine crescentic glomerulonephritis. Kidney Int. 80 (2011), 154–164.
27. [27] Paust, H.J., Turner, J.E., Steinmetz, O.M., et al. The IL-23/Th17 axis contributes to renal injury in experimental glomerulonephritis. J. Am. Soc. Nephrol. 20 (2009), 969–979.
28. [28] Krebs, C.F., Turner, J.E., Paust, H.J., et al. Plasticity of Th17 cells in autoimmune kidney diseases. J. Immunol., 2016, 10.4049/jimmunol.1501831 (J Immunol 1501831; published ahead of print June 6, 2016).
29. [29] Ghali, J.R., Holdsworth, S.R., Kitching, A.R., Targeting IL-17 and IL-23 in immune mediated renal disease. Curr. Med. Chem. 22 (2015), 4341–4365.
30. [30] Ghali, J.R., Wang, Y.M., Holdsworth, S.R., Kitching, A.R., Regulatory T cells in immune-mediated renal disease. Nephrology (Carlton) 21 (2016), 86–96.
31. [31] Kurts, C., Heymann, F., Lukacs-Kornek, V., Boor, P., Floege, J., Role of T cells and dendritic cells in glomerular immunopathology. Semin. Immunopathol. 29 (2007), 317–335.
32. [32] Izui, S., Lambert, P.H., Miescher, P.A., Failure to detect circulating DNA–anti-DNA complexes by four radioimmunological methods in patients with systemic lupus erythematosus. Clin. Exp. Immunol. 30 (1977), 384–392.
33. [33] Koffler, D., Schur, P.H., Kunkel, H.G., Immunological studies concerning the nephritis of systemic lupus erythematosus. J. Exp. Med. 126 (1967), 607–624.
34. [34] Krishnan, M.R., Wang, C., Marion, T.N., Anti-DNA autoantibodies initiate experimental lupus nephritis by binding directly to the glomerular basement membrane in mice. Kidney Int. 82 (2012), 184–192.
35. [35] Garini, G., Allegri, L., Vaglio, A., Buzio, C., Hepatitis C virus-related cryoglobulinemia and glomerulonephritis: pathogenesis and therapeutic strategies. Ann. Ital. Med. Int. 20 (2005), 71–80.
36. [36] Quigg, R.J., Complement and autoimmune glomerular diseases. Curr. Dir. Autoimmun. 7 (2004), 165–180.
37. [37] Noronha, I.L., Fujihara, C.K., Zatz, R., The inflammatory component in progressive renal disease—are interventions possible?. Nephrol. Dial. Transplant. 17 (2002), 363–368.
38. [38] Mayadas, T.N., Tsokos, G.C., Tsuboi, N., Mechanisms of immune complex-mediated neutrophil recruitment and tissue injury. Circulation 120 (2009), 2012–2024.
39. [39] Belmont, H.M., Buyon, J., Giorno, R., Abramson, S., Up-regulation of endothelial cell adhesion molecules characterizes disease activity in systemic lupus erythematosus. The Shwartzman phenomenon revisited. Arthritis Rheum. 37 (1994), 376–383.
40. [40] Borza, D.B., Alternative pathway dysregulation and the conundrum of complement activation by IgG4 immune complexes in membranous nephropathy. Front. Immunol., 7, 2016, 157.
41. [41] Beck, L.H. Jr., Bonegio, R.G., Lambeau, G., et al. M-type phospholipase A2 receptor as target antigen in idiopathic membranous nephropathy. N. Engl. J. Med. 361 (2009), 11–21.
42. [42] Tomas, N.M., Beck, L.H. Jr., Meyer-Schwesinger, C., et al. Thrombospondin type-1 domain-containing 7A in idiopathic membranous nephropathy. N. Engl. J. Med. 371 (2014), 2277–2287.
43. [43] Debiec, H., Guigonis, V., Mougenot, B., et al. Antenatal membranous glomerulonephritis due to anti-neutral endopeptidase antibodies. N. Engl. J. Med. 346 (2002), 2053–2060.
44. [44] Quigg, R.J., Cybulsky, A.V., Jacobs, J.B., Salant, D.J., Anti-Fx1A produces complement-dependent cytotoxicity of glomerular epithelial cells. Kidney Int. 34 (1988), 43–52.
45. [45] Neale, T.J., Ullrich, R., Ojha, P., Poczewski, H., Verhoeven, A.J., Kerjaschki, D., Reactive oxygen species and neutrophil respiratory burst cytochrome b558 are produced by kidney glomerular cells in passive Heymann nephritis. Proc. Natl. Acad. Sci. U. S. A. 90 (1993), 3645–3649.
46. [46] Nangaku, M., Shankland, S.J., Couser, W.G., Cellular response to injury in membranous nephropathy. J. Am. Soc. Nephrol. 16 (2005), 1195–1204.
47. [47] Nangaku, M., Couser, W.G., Mechanisms of immune-deposit formation and the mediation of immune renal injury. Clin. Exp. Nephrol. 9 (2005), 183–191.
48. [48] Kerr, M.A., The structure and function of human IgA. Biochem. J. 271 (1990), 285–296.
49. [49] Lucisano Valim, Y.M., Lachmann, P.J., The effect of antibody isotype and antigenic epitope density on the complement-fixing activity of immune complexes: a systematic study using chimaeric anti-NIP antibodies with human Fc regions. Clin. Exp. Immunol. 84 (1991), 1–8.
50. [50] Reverberi, R., Reverberi, L., Factors affecting the antigen–antibody reaction. Blood Transfus. 5 (2007), 227–240.
51. [51] Steensgaard, J., Johansen, A.S., Biochemical aspects of immune complex formation and immune complex diseases. Allergy 35 (1980), 457–472.
52. [52] Caulfield, J.P., Farquhar, M.G., Distribution of annionic sites in glomerular basement membranes: their possible role in filtration and attachment. Proc. Natl. Acad. Sci. U. S. A. 73 (1976), 1646–1650.
53. [53] Ravetch, J.V., Bolland, S., IgG fc receptors. Annu. Rev. Immunol. 19 (2001), 275–290.
54. [54] Isakov, N., Immunoreceptor tyrosine-based activation motif (ITAM), a unique module linking antigen and Fc receptors to their signaling cascades. J. Leukoc. Biol. 61 (1997), 6–16.
55. [55] Underhill, D.M., Goodridge, H.S., The many faces of ITAMs. Trends Immunol. 28 (2007), 66–73.
56. [56] Nimmerjahn, F., Ravetch, J.V., Fcgamma receptors: old friends and new family members. Immunity 24 (2006), 19–28.
57. [57] Muta, T., Kurosaki, T., Misulovin, Z., Sanchez, M., Nussenzweig, M.C., Ravetch, J.V., A 13-amino-acid motif in the cytoplasmic domain of Fc gamma RIIB modulates B-cell receptor signalling. Nature, 369, 1994, 340.
58. [58] Tridandapani, S., Siefker, K., Teillaud, J.L., Carter, J.E., Wewers, M.D., Anderson, C.L., Regulated expression and inhibitory function of Fcgamma RIIb in human monocytic cells. J. Biol. Chem. 277 (2002), 5082–5089.
59. [59] Dixon, F.J., Feldman, J.D., Vazquez, J.J., Experimental glomerulonephritis. The pathogenesis of a laboratory model resembling the spectrum of human glomerulonephritis. J. Exp. Med. 113 (1961), 899–920.
60. [60] Gitlin, D., Edelhoch, H., A study of the reaction between human serum albumin and its homologous equine antibody through the medium of light scattering. J. Immunol. 66 (1951), 67–77.
61. [61] Cochrane, C.G., Dixon, F.J., Cell and tissue damage through antigen–antibody complexes. Calif. Med. 111 (1969), 99–112.
62. [62] Banchereau, J., Steinman, R.M., Dendritic cells and the control of immunity. Nature 392 (1998), 245–252.
63. [63] Mellman, I., Steinman, R.M., Dendritic cells: specialized and regulated antigen processing machines. Cell 106 (2001), 255–258.
64. [64] Soos, T.J., Sims, T.N., Barisoni, L., et al. CX3CR1 + interstitial dendritic cells form a contiguous network throughout the entire kidney. Kidney Int. 70 (2006), 591–596.
65. [65] Markovic-Lipkovski, J., Muller, C.A., Risler, T., Bohle, A., Muller, G.A., Association of glomerular and interstitial mononuclear leukocytes with different forms of glomerulonephritis. Nephrol. Dial. Transplant. 5 (1990), 10–17.
66. [66] Cuzic, S., Ritz, E., Waldherr, R., Dendritic cells in glomerulonephritis. Virchows Arch. B Cell Pathol. Incl. Mol. Pathol. 62 (1992), 357–363.
67. [67] Weisheit, C.K., Engel, D.R., Kurts, C., Dendritic cells and macrophages: sentinels in the kidney. Clin. J. Am. Soc. Nephrol. 10 (2015), 1841–1851.
68. [68] Lukacs-Kornek, V., Turley, S.J., Self-antigen presentation by dendritic cells and lymphoid stroma and its implications for autoimmunity. Curr. Opin. Immunol. 23 (2011), 138–145.
69. [69] Steinman, R.M., Cohn, Z.A., Identification of a novel cell type in peripheral lymphoid organs of mice. I. Morphology, quantitation, tissue distribution. J. Exp. Med. 137 (1973), 1142–1162.
70. + T cells. J. Exp. Med. 186 (1997), 239–245.
71. [71] Heymann, F., Meyer-Schwesinger, C., Hamilton-Williams, E.E., et al. Kidney dendritic cell activation is required for progression of renal disease in a mouse model of glomerular injury. J. Clin. Invest. 119 (2009), 1286–1297.
72. [72] Hochheiser, K., Tittel, A., Kurts, C., Kidney dendritic cells in acute and chronic renal disease. Int. J. Exp. Pathol. 92 (2011), 193–201.
73. [73] Roake, J.A., Rao, A.S., Morris, P.J., Larsen, C.P., Hankins, D.F., Austyn, J.M., Dendritic cell loss from nonlymphoid tissues after systemic administration of lipopolysaccharide, tumor necrosis factor, and interleukin 1. J. Exp. Med. 181 (1995), 2237–2247.
74. [74] Albert, M.L., Sauter, B., Bhardwaj, N., Dendritic cells acquire antigen from apoptotic cells and induce class I-restricted CTLs. Nature 392 (1998), 86–89.
75. [75] Sauter, B., Albert, M.L., Francisco, L., Larsson, M., Somersan, S., Bhardwaj, N., Consequences of cell death: exposure to necrotic tumor cells, but not primary tissue cells or apoptotic cells, induces the maturation of immunostimulatory dendritic cells. J. Exp. Med. 191 (2000), 423–434.
76. [76] Williams, C.A., Harry, R.A., McLeod, J.D., Apoptotic cells induce dendritic cell-mediated suppression via interferon-gamma-induced IDO. Immunology 124 (2008), 89–101.
77. [77] Reis e Sousa, C., Dendritic cells in a mature age. Nat. Rev. Immunol. 6 (2006), 476–483.
78. [78] Matzinger, P., Tolerance, danger, and the extended family. Annu. Rev. Immunol. 12 (1994), 991–1045.
79. [79] Darrah, E., Andrade, F., NETs: the missing link between cell death and systemic autoimmune diseases?. Front. Immunol., 3, 2013, 428.
80. [80] Renaudineau, Y., Deocharan, B., Jousse, S., Renaudineau, E., Putterman, C., Youinou, P., Anti-alpha-actinin antibodies: a new marker of lupus nephritis. Autoimmun. Rev. 6 (2007), 464–468.
81. [81] Kraaij, T., Tengstrom, F.C., Kamerling, S.W., et al. A novel method for high-throughput detection and quantification of neutrophil extracellular traps reveals ROS-independent NET release with immune complexes. Autoimmun. Rev. 15 (2016), 577–584.
82. [82] Hochheiser, K., Engel, D.R., Hammerich, L., et al. Kidney dendritic cells become pathogenic during crescentic glomerulonephritis with proteinuria. J. Am. Soc. Nephrol. 22 (2011), 306–316.
83. [83] Couser, W.G., Basic and translational concepts of immune-mediated glomerular diseases. J. Am. Soc. Nephrol. 23 (2012), 381–399.
84. + T-regulatory cells suppress anti-glomerular basement membrane nephritis. Kidney Int. 79 (2011), 977–986.
85. [85] Nolasco, F.E., Cameron, J.S., Hartley, B., Coelho, A., Hildreth, G., Reuben, R., Intraglomerular T cells and monocytes in nephritis: study with monoclonal antibodies. Kidney Int. 31 (1987), 1160–1166.
86. [86] Bolton, W.K., Innes, D.J. Jr., Sturgill, B.C., Kaiser, D.L., T-cells and macrophages in rapidly progressive glomerulonephritis: clinicopathologic correlations. Kidney Int. 32 (1987), 869–876.
87. [87] Kim, J., Bronson, C.L., Hayton, W.L., et al. Albumin turnover: FcRn-mediated recycling saves as much albumin from degradation as the liver produces. Am. J. Physiol. Gastrointest. Liver Physiol. 290 (2006), G352–G360.
88. [88] Junghans, R.P., Anderson, C.L., The protection receptor for IgG catabolism is the beta2-microglobulin-containing neonatal intestinal transport receptor. Proc. Natl. Acad. Sci. U. S. A. 93 (1996), 5512–5516.
89. [89] Mancilla-Jimenez, R., Appay, M.D., Bellon, B., Kuhn, J., Bariety, J., Druet, P., IgG Fc membrane receptor on normal human glomerular visceral epithelial cells. Virchows Arch. A Pathol. Anat. Histopathol. 404 (1984), 139–158.
90. [90] Haymann, J.P., Levraud, J.P., Bouet, S., et al. Characterization and localization of the neonatal Fc receptor in adult human kidney. J. Am. Soc. Nephrol. 11 (2000), 632–639.
91. [91] Shah, U., Dickinson, B.L., Blumberg, R.S., Simister, N.E., Lencer, W.I., Walker, W.A., Distribution of the IgG Fc receptor, FcRn, in the human fetal intestine. Pediatr. Res. 53 (2003), 295–301.
92. [92] Simister, N.E., Story, C.M., Chen, H.L., Hunt, J.S., An IgG-transporting Fc receptor expressed in the syncytiotrophoblast of human placenta. Eur. J. Immunol. 26 (1996), 1527–1531.
93. [93] Zhu, X., Meng, G., Dickinson, B.L., et al. MHC class I-related neonatal Fc receptor for IgG is functionally expressed in monocytes, intestinal macrophages, and dendritic cells. J. Immunol. 166 (2001), 3266–3276.
94. [94] Rodewald, R., Selective antibody transport in the proximal small intestine of the neonatal rat. J. Cell Biol. 45 (1970), 635–640.
95. [95] Rodewald, R., pH-dependent binding of immunoglobulins to intestinal cells of the neonatal rat. J. Cell Biol. 71 (1976), 666–669.
96. [96] Simister, N.E., Rees, A.R., Isolation and characterization of an Fc receptor from neonatal rat small intestine. Eur. J. Immunol. 15 (1985), 733–738.
97. [97] Chaudhury, C., Mehnaz, S., Robinson, J.M., et al. The major histocompatibility complex-related Fc receptor for IgG (FcRn) binds albumin and prolongs its lifespan. J. Exp. Med. 197 (2003), 315–322.
98. [98] Dickinson, B.L., Badizadegan, K., Wu, Z., et al. Bidirectional FcRn-dependent IgG transport in a polarized human intestinal epithelial cell line. J. Clin. Invest. 104 (1999), 903–911.
99. [99] Spiekermann, G.M., Finn, P.W., Ward, E.S., et al. Receptor-mediated immunoglobulin G transport across mucosal barriers in adult life: functional expression of FcRn in the mammalian lung. J. Exp. Med. 196 (2002), 303–310.
100. [100] Akilesh, S., Huber, T.B., Wu, H., et al. Podocytes use FcRn to clear IgG from the glomerular basement membrane. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 967–972.
101. [101] Kobayashi, N., Suzuki, Y., Tsuge, T., Okumura, K., Ra, C., Tomino, Y., FcRn-mediated transcytosis of immunoglobulin G in human renal proximal tubular epithelial cells. Am. J. Physiol. Renal Physiol. 282 (2002), F358–F365.
102. [102] Tenten, V., Menzel, S., Kunter, U., et al. Albumin is recycled from the primary urine by tubular transcytosis. J. Am. Soc. Nephrol. 24 (2013), 1966–1980.
103. [103] Sarav, M., Wang, Y., Hack, B.K., et al. Renal FcRn reclaims albumin but facilitates elimination of IgG. J. Am. Soc. Nephrol. 20 (2009), 1941–1952.
104. [104] Olaru, F., Luo, W., Suleiman, H., et al. Neonatal Fc receptor promotes immune complex-mediated glomerular disease. J. Am. Soc. Nephrol. 25 (2014), 918–925.
105. [105] Weflen, A.W., Baier, N., Tang, Q.J., et al. Multivalent immune complexes divert FcRn to lysosomes by exclusion from recycling sorting tubules. Mol. Biol. Cell 24 (2013), 2398–2405.
106. [106] Baker, K., Qiao, S.W., Kuo, T.T., et al. Neonatal Fc receptor for IgG (FcRn) regulates cross-presentation of IgG immune complexes by CD8-CD11b + dendritic cells. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 9927–9932.
107. [107] Hu, S.Y., Jia, X.Y., Li, J.N., et al. T cell infiltration is associated with kidney injury in patients with anti-glomerular basement membrane disease. Sci. China Life Sci., 2016, 10.1007/s11427-016-5030-9.
108. [108] Kitching, A.R., Holdsworth, S.R., Hickey, M.J., Targeting leukocytes in immune glomerular diseases. Curr. Med. Chem. 15 (2008), 448–458.
109. [109] Moroni, G., Doria, A., Ponticelli, C., Cyclosporine (CsA) in lupus nephritis: assessing the evidence. Nephrol. Dial. Transplant. 24 (2009), 15–20.
110. [110] Wada, T., Pippin, J.W., Nangaku, M., Shankland, S.J., Dexamethasone's prosurvival benefits in podocytes require extracellular signal-regulated kinase phosphorylation. Nephron Exp. Nephrol. 109 (2008), e8–19.
111. [111] Ejaz, A.A., Asmar, A., Alsabbagh, M.M., Ahsan, N., Rituximab in immunologic glomerular diseases. MAbs 4 (2012), 198–207.
112. [112] Mayo, C., Membranous Nephropathy Trial of Rituximab. 2016.
113. [113] GlaxoSmithKline, A Study of Belimumab in Idiopathic Membranous Glomerulonephropathy. 2014.
114. [114] University of I, TP10 Use in Patients With C3 Glomerulopathy (C3G). 2016.
115. [115] Omeros, C., OMS721 Treatment of Steroid-Dependent Glomerulopathies. 2017.
116. [116] Eto, N., Wada, T., Inagi, R., et al. Podocyte protection by darbepoetin: preservation of the cytoskeleton and nephrin expression. Kidney Int. 72 (2007), 455–463.
117. [117] Logar, C.M., Brinkkoetter, P.T., Krofft, R.D., Pippin, J.W., Shankland, S.J., Darbepoetin alfa protects podocytes from apoptosis in vitro and in vivo. Kidney Int. 72 (2007), 489–498.
118. [118] Alarcon-Segovia, D., Tumlin, J.A., Furie, R.A., et al. LJP 394 for the prevention of renal flare in patients with systemic lupus erythematosus: results from a randomized, double-blind, placebo-controlled study. Arthritis Rheum. 48 (2003), 442–454.
119. [119] Lutz, M.B., Therapeutic potential of semi-mature dendritic cells for tolerance induction. Front. Immunol., 3, 2012, 123.
120. [120] Hilkens, C.M., Isaacs, J.D., Thomson, A.W., Development of dendritic cell-based immunotherapy for autoimmunity. Int. Rev. Immunol. 29 (2012), 156–183.
121. [121] Apetoh, L., Locher, C., Ghiringhelli, F., Kroemer, G., Zitvogel, L., Harnessing dendritic cells in cancer. Semin. Immunol. 23 (2011), 42–49.
122. [122] Finke, L.H., Wentworth, K., Blumenstein, B., Rudolph, N.S., Levitsky, H., Hoos, A., Lessons from randomized phase III studies with active cancer immunotherapies—outcomes from the 2006 meeting of the Cancer Vaccine Consortium (CVC). Vaccine 25:Suppl. 2 (2007), B97–B109.
123. [123] Butterfield, L.H., Vujanovic, L., New approaches to the development of adenoviral dendritic cell vaccines in melanoma. Curr. Opin. Investig. Drugs 11 (2012), 1399–1408.
124. [124] Bagavant, H., Deshmukh, U.S., Wang, H., Ly, T., Fu, S.M., Role for nephritogenic T cells in lupus glomerulonephritis: progression to renal failure is accompanied by T cell activation and expansion in regional lymph nodes. J. Immunol. 177 (2006), 8258–8265.
125. [125] Tucci, M., Quatraro, C., Lombardi, L., Pellegrino, C., Dammacco, F., Silvestris, F., Glomerular accumulation of plasmacytoid dendritic cells in active lupus nephritis: role of interleukin-18. Arthritis Rheum. 58 (2008), 251–262.