Top

Published in:

01-01-2014 | Review

The role of the immune system in idiopathic nephrotic syndrome: a review of clinical and experimental studies

Authors: Wagner de Fátima Pereira, Gustavo Eustáquio Alvim Brito-Melo, Fábio Tadeu Lourenço Guimarães, Thiago Guimarães Rosa Carvalho, Elvis Cueva Mateo, Ana Cristina Simões e Silva

Published in: Inflammation Research | Issue 1/2014

Abstract

Idiopathic nephrotic syndrome (INS) is a multifactorial disease, characterized by proteinuria, hypoalbuminemia, edema and hyperlipidemia. Studies in humans and animal models have associated INS with changes in the immune response. The purpose of this article is to review clinical and experimental findings showing the involvement of the immune response in the pathogenesis of INS. The role of the immune system in INS has been shown by clinical and experimental studies. However, the pattern of immune response in patients with INS is still not clearly defined. Many studies show changes in the dynamics of T lymphocytes, especially the regulatory T cells. Alternatively, there are other reports regarding the involvement of the complement system and B lymphocytes in the pathophysiology of INS. Indeed, none of the immunological biomarkers evaluated were undeniably linked to changes in glomerular permeability and proteinuria. On the other hand, some studies suggest a link between urinary chemokines, such as IL-8/CXCL8 and MCP-1/CCL2, and changes in glomerular permeability and/or the deterioration of glomerulopathies. To understand the pathophysiology of INS, longitudinal studies are clearly needed. The characterization of the profile of the immune response might help the development of specific and individualized therapies, leading to clinical improvement and better prognosis.

Schachter AD. The pediatric nephrotic syndrome spectrum: clinical homogeneity and molecular heterogeneity. Pediatr Transpl. 2004;8:344–8.

D’Agati VD, Kaskel FJ, Falk RJ. Focal segmental glomerulosclerosis. N Engl J Med. 2011;365:2398–411.PubMed

Souto MFO, Teixeira MM, Penido MGMG, Simões e Silva AC. Fisiopatologia da Síndrome Nefrótica em crianças e adolescentes. Arch Latin Nefr Ped. 2008;8:1–10.

Fodor P, Saitúa MT, Rodriguez E, González B, Schlesinger L. T-cell dysfunction in minimal-change nephrotic syndrome of childhood. Am J Dis Child. 1982;136:713–7.PubMed

Araya C, Diaz L, Wasserfall C, Atkinson M, Mu W, Johnson R, et al. T regulatory cell function in idiopathic minimal lesion nephrotic syndrome. Pediatr Nephrol. 2009;24:1691–8.PubMedCentralPubMed

Araya CE, Wasserfall CH, Brusko TM, Mu W, Segal MS, Johnson RJ, et al. A case of unfulfilled expectations cytokines in idiopathic minimal lesion nephrotic syndrome. Pediatr Nephrol. 2006;21(603–610):3.

Shalboub RJ. Pathogenesis of lipoid nephritis: a disorder of T cell function. Lancet. 1974;304:556–60.

Savin VJ, Sharma R, Sharma M, McCarthy ET, Swan SK, Ellis E, et al. Circulating fator associated with increased glomerular permeability to albumin in recurrent focal segmental glomerulosclerosis. N Engl J Med. 1996;334:878–83.PubMed

Gitlin D, Janeway CA, Farr LE. Studies of the metabolism of plasma proteins in the nephrotic syndrome. I. Albumin, γ-globulin and immunoglobulin. J Clin Invest. 1956;35:44–56.PubMedCentralPubMed

10.

Lagrue G, Branellec A, Blanc C, Xheneumont S, Beaudoux F, Sobel A, et al. A vascular permeability factor in lymphocyte culture supernatants from patients with nephrotic syndrome II: pharmacological and physicochemical properties. Biomedicine. 1975;23:73–5.PubMed

11.

Giangiacomo J, Cleary TG, Cole BR, Hoffstein P, Robson AM. Serum immunoglobulins in the nephrotic syndrome. A possible cause of minimal change nephrotic syndrome. N Engl J Med. 1975;293:08–12.

12.

Herrod HG, Stapleton FB, Trouy RL, Roy S. Evaluation of T lymphocyte subpopulations in children with nephrotic syndrome. Clin Exp Immunol. 1983;52:581–5.PubMedCentralPubMed

13.

Boulton JJM, Tulloch I, Dore B, Mclay A. Changes in the glomerular capillary wall induced by lymphocyte products and serum of nephrotic patients. Clin Nephrol. 1983;20:72–7.

14.

Yokoyama H, Kida H, Tani Y, Abe T, Tomosugi N, Koshino Y, et al. Immunodynamics of minimal change nephrotic syndrome in adults T and B lymphocyte subsets and serum immunoglobulin levels. Clin Exp Immunol. 1985;61:601–7.PubMedCentralPubMed

15.

Beaman M, Oldfield S, Maclennan ICM, Michael J, Adu D. Hypogammaglobulinaemia in nephrotic rats is attributable to hypercatabolism of IgG. Clin Exp Immunol. 1988;74:425–30.PubMedCentralPubMed

16.

Moorthy AV, Zimmerman SW, Burkholder PM. Inhibition of lymphocyte blastogenesis by plasma of patients with minimal change nephrotic syndrome. Lancet. 1976;1:1160–2.PubMed

17.

Kausman JY, Kitching AR. A new approach to idiopathic nephrotic syndrome. J Am Soc Nephrol. 2007;18:2621–2.PubMed

18.

Hashimura Y, Nozu K, Kanegane H, Miyawaki T, Hayakawa A, Yoshikawa N, et al. Minimal change nephrotic syndrome associated with immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome. Pediatr Nephrol. 2009;24:1181–6.PubMed

19.

Lagrue G, Branellec A, Xheneumont S, Weil B. Lymphokine ‘skin reactive factor’ (SRF) and the nephrotic syndrome. Bibl Anat. 1975;13:331–4.PubMed

20.

Tanaka R, Yoshikawa N, Nakamura H, Ito H. Infusion of peripheral blood mononuclear cell products from nephrotic children increases albuminuria in rats. Nephron. 1992;60:35–41.PubMed

21.

Riyuzo MC, Soares V. Revisão: Papel do infiltrado inflamatório na fibrose túbulo-intersticial e evolução das glomerulopatias. J Bras Nefrol. 2002;24:40–7.

22.

Le Berre L, Herve C, Buzelin F, Usal C, Soulillou JP, Dantal J. Renal macrophage activation and Th2 polarization precedes the development of nephrotic syndrome in Buffalo/Mna rats. Kidney Int. 2005;68:2079–90.PubMed

23.

Cao Q, Wang Y, Zheng D, Sun Y, Wang YA, et al. IL-10/TGF-β-modified macrophages induce regulatory t cells and protect against adriamycin nephrosis. J Am Soc Nephrol. 2010;21:933–42.PubMed

24.

Kuncio GS, Neilson EG, Haverty T. Mechanisms of tubulointerstitial fibrosis. Kidney Int. 1991;39:550–6.PubMed

25.

Benz K, Büttner M, Dittrich K, Campean V, Dötsch J, Amann K. Characterization of renal immune cell infiltrates in children with nephrotic syndrome. Pediatr Nephrol. 2010;25:1291–8.PubMed

26.

Lai K-W, Wei Ch-L, Tan L-K, Tan P-H, Chiang GSC, Lee CGL, et al. Overexpression of interleukin 13 induces minimal-change-like nephropathy in rats. J Am Soc Nephrol. 2007;18:1476–85.PubMed

27.

Lee VWS, Wang Y, Qin X, Wang Y, Zheng G, Mahajan D, et al. Adriamycin nephropathy in severe combined immunodeficient (SCID) mice. Nephrol Dial Transpl. 2006;21:3293–8.

28.

Vielhauer V, Berning E, Eis V, Kretzler M, Segerer S, Strutz F, et al. CCR1 blockade reduces interstitial inflammation and fibrosis in mice with glomerulosclerosis and nephrotic syndrome. Kidney Int. 2004;66:2264–78.PubMed

29.

Wu H, Wang Y, Tay Y-C, Zheng G, Shang C, Alexander S, et al. DNA vaccination with naked DNA encoding MCP-1 and RANTES protects against renal injury in Adriamycin nephropathy. Kidney Int. 2005;67:2178–86.PubMed

30.

Wang Y, Wang YP, Tay Y-C, Harris DCH. Progressive adriamycin nephropathy in mice: sequence of histologic and immunohistochemical events. Kidney Int. 2000;58:1797–804.PubMed

31.

Rossmann P, Matousovic K, Bohdanecká M. Experimental adriamycin nephropathy: fine structure, morphometry, glomerular polyanion and cell membrane antigens. J Pathol. 1993;169:99–108.PubMed

32.

Muñoz M, Rincón J, Pedreañez A, Viera N, Hernández-Fonseca JP, Mosquera J. Proinflammatory role of angiotensin II in a rat nephrosis model induced by Adriamycin. J Renin Angiotensin Aldosterone Syst. 2001; doi:10.1177/14703203114100922011.

33.

Van Goor H, Van Der Horst MLC, Atmosoerodjo J, Joles JA, Van To A, Grond J. Renal apolipoproteins in nephrotic rats. Am J Pathol. 1993;142:1804–12.PubMed

34.

Erwig LP, Kluth DC, Rees AJ. Macrophage heterogeneity in renal inflammation. Nephrol Dial Transpl. 2003;18:1962–5.

35.

Eardley KS, Cockwell P. Macrophages and progressive tubulointerstitial disease. Kidney Int. 2005;68:437–55.

36.

Wang Y, Wang YP, Zheng G, Lee VWS, Ouyang L, Chang DHH, et al. Ex vivo programmed macrophages ameliorate experimental chronic inflammatory renal disease. Kidney Int. 2007;72:290–9.PubMed

37.

Schnaper HW, Aune TM. Identification of the lymphokine soluble immune response suppressor in urine of nephrotic children. J Clin Invest. 1985;76:341–9.PubMedCentralPubMed

38.

Sasdelli M, Rovinetti C, Cagnoli L, Beltrandi E, Barboni F, Zucchelli P. Lymphocyte subpopulations in minimal-change nephropathy. Nephron. 1980;25:72–6.PubMed

39.

Fiser RT, Arnold WC, Charlton RK, Steele RW, Childress SH, Shirkey B. T-lymphocyte subsets in nephrotic syndrome. Kidney Int. 1991;40:913–6.PubMed

40.

Lama G, Luongo I, Tirino G, Borriello A, Carangio C, Salsano ME. T-lymphocyte populations and cytokines in childhood nephrotic syndrome. Am J Kidney Dis. 2002;39:958–65.PubMed

41.

Wang Y, Wang Y, Feng X, Bao S, Yi S, Kairaitis L, et al. Depletion of CD4 T cells aggravates glomerular and interstitial injury in murine adriamycin nephropathy. Kidney Int. 2001;59:975–84.PubMed

42.

Wang Y, Wang YP, Tay Y-C, Harris DCH. Role of CD8 cells in the progression of murine adriamycin nephropathy. Kidney Int. 2001;59:941–9.PubMed

43.

Tejani AT, Butt K, Trachtman H, Suthanthiran M, Rosenthal CJ, Khawar MR. Cyclosporine-A induced remission of relapsing nephrotic syndrome in children. Kidney Int. 1988;33:729–34.PubMed

44.

Okuyama S, Komatsuda A, Wakui H, Aiba N, Fujishima N, Iwamoto K, et al. Up-regulation of TRAIL mRNA expression in peripheral blood mononuclear cells from patients with minimal-change nephrotic syndrome. Nephrol Dial Transpl. 2005;20:539–44.

45.

Musial K, Ciszak L, Kosmaczewska A, Szteblich A, Frydecka I, Zwolińska D. Zeta chain expression in T and NK cells in peripheral blood of children with nephrotic syndrome. Pediatr Nephrol. 2010;25:119–27.PubMed

46.

Wu H, Wang YM, Wang Y, Hu M, Zhang GY, Knight JF, et al. Depletion of gama–delta T cells exacerbates murine adriamycin nephropathy. J Am Soc Nephrol. 2007;18:1180–9.PubMed

47.

Wang YM, Hu M, Wang Y, Polhill T, Zhang GY, Wang Y, et al. Regulatory T cells in renal disease. Int J Clin Exp Med. 2008;1:294–304.PubMedCentralPubMed

48.

Rubio-Cabezas O, Minton JA, Caswell R, Shield JP, Deiss D, Sumnik Z, et al. Clinical heterogeneity in patients with FOXP3 mutations presenting with permanent neonatal diabetes. Diabetes Care. 2009;32:111–6.PubMed

49.

Apostolou I, Von Boehmer H. In vivo instruction of suppressor commitment in naive T cells. J Exp Med. 2004;199:1401–8.PubMedCentralPubMed

50.

Chen W, Jin W, Hardegen N, Lei KJ, Li L, Marinos N, et al. Conversion of peripheral CD4⁺CD25⁻ naïve T cells to CD4⁺CD25⁺ regulatory T cells by TGF-beta induction of transcription factor FOXP3. J Exp Med. 2003;198:1875–86.PubMedCentralPubMed

51.

Le NT, Chao N. Regulating regulatory T cells. Bone Marrow Transpl. 2007;39:01–9.

52.

Wang YM, Zhang GY, Wang Y, Hu M, Wu H, Watson D, et al. Foxp3-transduced polyclonal regulatory T cells protect against chronic renal injury from adriamycin. J Am Soc Nephrol. 2006;17:697–706.PubMed

53.

Mahajan D, Wang Y, Qin X, Wang Y, Zheng G, Wang YM, et al. CD4⁺CD25⁺ regulatory T cells protect against injury in an innate murine model of chronic kidney disease. J Am Soc Nephrol. 2006;17:2731–41.PubMed

54.

Shao XS, Yang XQ, Zhao XD, Li Q, Xie YY, Wang XG, et al. The prevalence of Th17 cells and FOXP3 regulate T cells (Treg) in children with primary nephrotic syndrome. Pediatr Nephrol. 2009;24:1683–90.PubMed

55.

Pereira RL, Reis VO, Semedo P, Buscariollo BN, Donizetti-Oliveira C, Cenedeze MA, et al. Invariant natural killer T cell agonist modulates experimental focal and segmental glomerulosclerosis. PLoS One. 2012;. doi:10.1371/journal.pone.0032454.

56.

Sellier-Leclerc AL, Duval A, Riveron S, Macher MA, Deschenes G, Loirat C, et al. A humanized mouse model of idiopathic nephrotic syndrome suggests a pathogenic role for immature cells. J Am Soc Nephrol. 2007;18:2732–9.PubMed

57.

Garin EH, Blanchard DK, Matsushima K, Djeu JY. IL-8 production by peripheral blood mononuclear cells in nephrotic patients. Kidney Int. 1994;45:1311–7.PubMed

58.

Neuhaus TJ, Wadhwa M, Callard R, Barratt TM. Increased IL-2, IL-4 and interferon-gamma (IFN-γ) in steroid-sensitive nephrotic syndrome. Clin Exp Immunol. 1995;100:475–9.PubMedCentralPubMed

59.

Yap HK, Cheung W, Murugasu B, Sim SK, Seah CC, Jordan SC. Th1 and Th2 cytokine mRNA profiles in childhood nephrotic syndrome: evidence for increased IL-13 mRNA expression in relapse. J Am Soc Nephrol. 1999;10:529–37.PubMed

60.

Kemper MJ, Meyer-Jark T, Lilova M, Müller-Wiefel DE. Combined T- and B-cell activation in childhood steroid-sensitive nephrotic syndrome. Clin Nephrol. 2003;60:242–7.PubMed

61.

Valanciuté A, Le SG, Solhonne B, Pawlak A, Grimbert P, Lyonnet L, et al. NF-kappa-B p65 antagonizes IL-4 induction by c-maf in minimal change nephrotic syndrome. J Immunol. 2004;172:688–98.PubMed

62.

Kanai T, Yamagata T, Momoi MY. Macrophage inflammatory protein-1b and interleukin-8 associated with idiopathic steroid sensitive nephrotic syndrome. Pediatr Int. 2009;51:443–7.PubMed

63.

Bricio T, Molina A, Egido J, Gonzalez E, Mampaso F. IL-1-like production in adriamycin-induced nephrotic syndrome in the rat. Clin Exp Immunol. 1992;87:117–21.PubMedCentralPubMed

64.

Wang Y, Chen J, Chen L, Tay Y-C, Rangan GK, Harris DCH. Induction of monocyte chemoattractant protein-1 in proximal tubule cells by urinary protein. J Am Soc Nephrol. 1997;8:1537–45.PubMed

65.

Rangan GK, Wang Y, Tay YC, Harris DCH. Inhibition of nuclear factor-κB activation reduces cortical tubulointerstitial injury in proteinuric rats. Kidney Int. 1999;56:118–34.PubMed

66.

Wang LM, Chi HJ, Wang LN, Nie L, Zou YH, Zhao TN, et al. Expression of interleukin 6 in rat model of doxorubicin induced nephropathy. Chin J Contemp Pediatr. 2010;12:912–4.

67.

Kerpen HO, Bhat JG, Kantor R, Gauthier B, Rai KR, Schacht RG, et al. Lymphocyte subpopulations in minimal change nephrotic syndrome. Clin Immunol Immunopathol. 1979;14:130–6.PubMed

68.

Pescovitz MD, Book BK, Sidner RA. Resolution of recurrent focal segmental glomerulosclerosis proteinuria after rituximab treatment. N Engl J Med. 2006;354:1961–3.PubMed

69.

Ahmed MS, Wong CF. Rituximab and nephrotic syndrome: a new therapeutic hope? Nephrol Dial Transpl. 2008;23:11–7.

70.

Takei T, Nitta K. Rituximab and minimal change nephrotic syndrome: a therapeutic option. Clin Exp Nephrol. 2011;15:641–7.PubMed

71.

Sarma JV, Ward PA. The complement system. Cell Tissue Res. 2011; doi:10.1007/s00441-010-1034-0.PubMedCentralPubMed

72.

David S, Biancone L, Caserta C, Bussolati B, Cambi V, Camussi G. Alternative pathway complement activation induces proinflammatory activity in human proximal tubular epithelial cells. Nephrol Dial Transpl. 1997;12:51–6.

73.

Rangan GK, Pippin JW, Couser WG. C5b-9 regulates peritubular myofibroblast accumulation in experimental focal segmental glomerulosclerosis. Kidney Int. 2004;66:1838–48.PubMed

74.

He C, Imai M, Song H, Quigg RJ, Tomlinson S. Complement inhibitors targeted to the proximal tubule prevent injury in experimental nephrotic syndrome and demonstrate a key role for C5b-91. J Immunol. 2005;174:5750–7.PubMed

75.

Rangan GK, Pippin JW, Coombes JD, Couser WG. C5b-9 does not mediate chronic tubulointerstitial disease in the absence of proteinuria. Kidney Int. 2005;67:492–503.PubMed

76.

Eddy AA. Interstitial nephritis induced by protein overload proteinuria. Am J Pathol. 1989;135:719–73.PubMed

77.

Bao L, Haas M, Pippin J, Wang Y, Miwa T, Chang A, et al. Focal and segmental glomerulosclerosis induced in mice lacking decay-accelerating factor in T cells. J Clin Invest. 2009;119:1264–74.PubMedCentralPubMed

78.

Turnberg D, Lewis M, Moss J, Xu Y, Botto MH, Cook T. Complement activation contributes to both glomerular and tubulointerstitial damage in adriamycin nephropathy in mice. J Immunol. 2006;177:4094–102.PubMed

79.

Matsuo S, Nishikage H, Yoshida F, Nomura A, Piddlesden SJ, Morgan BP. Role of CD59 in experimental glomerulonephritis in rats. Kidney Int. 1994;46:191–200.PubMed

80.

Turnberg D, Botto M, Warren J, Morgan BP, Walport MJ, Cook HT. CD59a deficiency exacerbates accelerated nephrotoxic nephritis in mice. J Am Soc Nephrol. 2003;14:2271–9.PubMed

81.

Ransohoff RM. Chemokines and chemokine receptors: standing at the crossroads of immunobiology and neurobiology. Immunity. 2009;31(5):711–21.PubMedCentralPubMed

82.

Vianna HR, Bouissou CMMS, Tavares MS, Teixeira MM, Simões e Silva AC. Inflamação na doença renal crônica: papel de citocinas. J Bras Nefrol. 2011;33:351–64.PubMed

83.

Pereira AB, Rezende NA, Teixeira Junior AL, Teixeira MM, Simões e Silva AC. Citocinas e quimiocinas no transplante renal. J Bras Nefrol. 2009;31:286–96.

84.

Vianna HR, Soares CMBM, Silveira KD, Elmiro GS, Mendes PM, Tavares MS, et al. Cytokines in chronic kidney disease: potential link of MCP-1 and dyslipidemia in glomerular diseases. Pediatr Nephrol. 2013;28:463–9.PubMed

85.

Pereira AB, Teixeira AL, Rezende NA, Pereira RM, Miranda DM, Oliveira EA, et al. Urinary chemokines and anti-inflammatory molecules in renal transplanted patients as potential biomarkers of graft function: a prospective study. Int Urol Nephrol. 2012;44:1539–48.PubMed

86.

Garin EH, Laflam P, Chandler L. Anti-interleukin 8 antibody abolishes effects of lipoid nephrosis cytokine. Pediatr Nephrol. 1998;12:381–5.PubMed

87.

Souto MFO, Teixeira AL, Russo RC, Penido M-GMG, Silveira KD, Teixeira MM, Simões e Silva AC. Immune mediators in idiopathic nephrotic syndrome: evidence for a relation between interleukin 8 and proteinuria. Pediatr Res. 2008;64:637–42.PubMed

88.

Roberts WG, Palade GE. Increased microvascular permeability and endothelial fenestration induced by vascular endothelial growth factor. J Cell Sci. 1995;108:2369–79.PubMed

89.

Simon M, Gröne HJ, Jöhren O, Kullmer J, Plate KH, Risau W. Expression of vascular endothelial growth factor and its receptors in human renal ontogenesis and in adult kidney. Am J Physiol. 1995;268:240–50.

90.

Webb NJA, Watson CJ, Roberts ISD, Bottomley MJ, Jones CA, Lewis MA, et al. Circulating vascular endothelial growth factor is not increased during relapses of steroid-sensitive nephrotic syndrome. Kidney Int. 1999;55:1063–71.PubMed

91.

Laflam PF, Garin EH. Effect of tumor necrosis factor-α and vascular permeability growth factor on albuminuria in rats. Pediatr Nephrol. 2005;21:177–81.PubMed

92.

Strehlau J, Schachter AD, Pavlakis M, Singh A, Tejani A, Strom TB. Activated intrarenal transcription of CTL-effectors and TGF-1 in children with focal segmental glomerulosclerosis. Kidney Int. 2002;61:90–5.PubMed

93.

Ruiz-Ortega M, Lorenzo Ó, Rupérez M, Blanco J, Egido J. Systemic infusion of angiotensin II into normal rats activates nuclear factor-κB and AP-1 in the kidney role of AT1 and AT2 receptors. Am J Pathol. 2001;158:1743–56.PubMed

94.

Wei C, El Hindi S, Li J, Fornoni A, Goes N, Sageshima J, et al. Circulating urokinase receptor (suPAR) as a cause of focal segmenter glomerulosclerosis. Nat Med. 2011;17:952–60.PubMed

95.

Maas RJ, Deegens JK, Wetzels JF. Serum suPAR in patients with FSGS: trash or treasure? Pediatr Nephrol. 2013;28:1041–8.PubMed

96.

Mosmann TR, Cherwinski H, Bond MW, Giedlin MA, Coffman RL. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J Immunol. 1986;175:05–14.

97.

Del Prete GF, De Carli M, Mastromauro C, Biagiotti R, Macchia D, Falagiani P, Ricci M, Romagnani S. Purified protein derivative of Mycobacterium tuberculosis and excretory-secretory antigen(s) of Toxocara canis expand in vitro human T cells with stable and opposite (type 1 T helper or type 2 T helper) profile of cytokine production. J Clin Invest. 1991;88:346–50.PubMedCentralPubMed

98.

Abbas AK, Murphy KM, Sher A. Functional diversity of helper T lymphocytes. Nature. 1986;383:787–93.

99.

Hurtado A, Johnson RJ. Hygiene hypothesis and prevalence of glomerulonephritis. Kidney Int. 2005;68 (Supplement):62–7.

100.

Odobasic D, Kitching AR, Tipping PG, Holdsworth SR. CD80 and CD86 costimulatory molecules regulate crescentic glomerulonephritis by different mechanisms. Kidney Int. 2005;68:584–94.PubMed

101.

Lee VWS, Harris DCH. Adriamycin nephropathy: a model of focal segmental glomerulosclerosis. Nephrology. 2011;16:30–8.PubMed

102.

Tovar AR, Murguía F, Cruz C, Hernández-Pando R, Aguilar-Salinas CA, Pedraza-Chaverri J, et al. A soy protein diet alters hepatic lipid metabolism gene expression and reduces serum lipids and renal fibrogenic cytokines in rats with chronic nephrotic syndrome. J Nutr. 2002;132:2562–9.PubMed

103.

Kim SY, Lim AY, Jeon SK, Lee IS, Choue R. Effects of dietary protein and fat contents on renal function and inflammatory cytokines in rats with adriamycin-induced nephrotic syndrome. Mediat Inflamm. 2011; doi:10.1155/2011/945123.

Title: The role of the immune system in idiopathic nephrotic syndrome: a review of clinical and experimental studies
Authors: Wagner de Fátima Pereira
Gustavo Eustáquio Alvim Brito-Melo
Fábio Tadeu Lourenço Guimarães
Thiago Guimarães Rosa Carvalho
Elvis Cueva Mateo
Ana Cristina Simões e Silva
Publication date: 01-01-2014
Publisher: Springer Basel
Published in: Inflammation Research / Issue 1/2014
Print ISSN: 1023-3830
Electronic ISSN: 1420-908X
DOI: https://doi.org/10.1007/s00011-013-0672-6

Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Reserve your place

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin

Prof. Florian Limbourg

Prof. Anoop Chauhan

Developed by: Springer Medicine

Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2014

Role of Angptl4 in vascular permeability and inflammation

OxLDL-induced IL-1beta secretion promoting foam cells formation was mainly via CD36 mediated ROS production leading to NLRP3 inflammasome activation

Flavones derived from nature attenuate the immediate and late-phase asthmatic responses to aerosolized-ovalbumin exposure in conscious guinea pigs

Microgravity inhibition of lipopolysaccharide-induced tumor necrosis factor-α expression in macrophage cells

Associations between PTPN2 polymorphisms and susceptibility to ulcerative colitis and Crohn’s disease: a meta-analysis

Interleukin-4 deficiency protects mice from acetaminophen-induced liver injury and inflammation by prevention of glutathione depletion

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

At a glance: The STEP trials