Immunopathogenesis of membranous nephropathy: An update

Seminars in Immunopathology

Volumn 36, Issue 4, 2014, Pages 381-397

  Debiec, Hanna ^a,b,c   Ronco, Pierre ^a,b,c  

^a SORBONNE UNIVERSITÉ   (France)

^b Urgences Néphrologiques et Transplantation Rénale Hôpital Tenon 4   (France)

^c HÔPITAL TENON   (France)

Author keywords

Antigens; Autoimmunity; Complement; Membranous nephropathy; Podocyte; Stress response

Indexed keywords

ANTIGEN; AUTOANTIBODY; BOVINE SERUM ALBUMIN; COMPLEMENT COMPONENT C5B; COMPLEMENT COMPONENT C9; EPITOPE; IMMUNOGLOBULIN G ANTIBODY; MEMBRANE METALLOENDOPEPTIDASE; NEPHRIN; PHOSPHATIDYLCHOLINE STEROL ACYLTRANSFERASE; PHOSPHOLIPASE A2 RECEPTOR; PLASMINOGEN ACTIVATOR INHIBITOR 1; REGULATOR PROTEIN; COMPLEMENT;

ALLOIMMUNITY; ANTIGENICITY; COMPLEMENT ACTIVATION; COMPLEMENT SYSTEM; ENZYME REPLACEMENT; GENETIC PREDISPOSITION; GENETIC VARIABILITY; GENOTYPE; HEYMANN NEPHRITIS; HUMAN; IMMUNOPATHOGENESIS; IMMUNOSTIMULATION; KIDNEY FUNCTION; MEMBRANOUS GLOMERULONEPHRITIS; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN TARGETING; REVIEW; ADULT; CHILD; GLOMERULONEPHRITIS, MEMBRANOUS; GLOMERULUS BASEMENT MEMBRANE; IMMUNOLOGY; PATHOLOGY; PODOCYTE; PRESCHOOL CHILD; PROTEINURIA;

ADULT; CHILD; CHILD, PRESCHOOL; COMPLEMENT SYSTEM PROTEINS; GLOMERULAR BASEMENT MEMBRANE; GLOMERULONEPHRITIS, MEMBRANOUS; HUMANS; PODOCYTES; PROTEINURIA;

EID: 84905859130     PISSN: 18632297     EISSN: 18632300     Source Type: Journal    
DOI: 10.1007/s00281-014-0423-y     Document Type: Review

References (169)

1. Kerjaschki D (2000) Pathogenetic concepts of membranous glomerulopathy (MGN). J Nephrol 13:S96-S100
2. Glassock RJ (2010) The pathogenesis of idiopathic membranous nephropathy: a 50-year odyssey. Am J Kidney Dis 56:157-167
3. Ronco P, Debiec H (2010) Antigen identification in membranous nephropathy moves toward targeted monitoring and new therapy. J Am Soc Nephrol 21:564-569
4. Simon P, Ramée MP, Autuly V, Laruelle E, Charasse C, Cam G, Ang KS (1994) Epidemiology of primary glomerular diseases in a French region. Variations according to period and age. Kidney Int 46:1192-1198
5. Maisonneuve P, Agodoa L, Gellert R, Stewart JH, Buccianti G, Lowenfels AB, Wolfe RA, Jones E, Disney AP, Briggs D, McCredie M, Boyle P (2000) Distribution of primary renal diseases leading to end-stage renal failure in the United States, Europe, and Australia/New Zealand: results from an international comparative study. Am J Kidney Dis 35:157-165 (Pubitemid 30027256)
6. Eddy AA, Symons JM (2003) Nephrotic syndrome in childhood. Lancet 362:629-639 (Pubitemid 37013306)
7. Chen A, Frank R, Vento S, Crosby V, Chandra M, Gauthier B, Valderrama E, Trachtman H (2007) Idiopathic membranous nephropathy in pediatric patients: presentation, response to therapy, and long-term outcome. BMC Nephrol 6:8-11
8. Polanco N, Gutiérrez E, Covarsí A, Ariza F, Carreño A, Vigil A, Baltar J, Fernández-Fresnedo G, Martín C, Pons S, Lorenzo D, Bernis C, Arrizabalaga P, Fernández-Juárez G, Barrio V, Sierra M, Castellanos I, Espinosa M, Rivera F, Oliet A, Fernández-Vega F, Praga M (2010) Spontaneous remission of nephrotic syndrome in idiopathic membranous nephropathy. J Am Soc Nephrol 21:697-704
9. Polanco N, Gutiérrez E, Rivera F, Castellanos I, Baltar J, Lorenzo D, Praga M (2012) Spontaneous remission of nephrotic syndrome in membranous nephropathy with chronic renal impairment. Nephrol Dial Transplant 27:231-234
10. Glassock RJ (2003) Diagnosis and natural course of membranous nephropathy. Semin Nephrol 23:324-332
11. Glassock RJ (2004) The treatment of idiopathic membranous nephropathy: a dilemma or a conundrum? Am J Kidney Dis 44:562-566
12. Hofstra JM, Fervenza FC, Wetzels JF (2013) Treatment of idiopathic membranous nephropathy. Nat Rev Nephrol 9:443-458
13. Waldman M, Austin HAIII (2009) Controversies in the treatment of idiopathic membranous nephropathy. Nat Rev Nephrol 5:469-479
14. Heymann W, Hackel DB, Harwood S, Wilson SGF, Hunter JL (1959) Production of nephrotic syndrome in rats by Freund's adjuvants and rat kidney suspension. Proc Soc Exp Biol Med 100:660-664
15. Van Damme BJ, Fleuren GJ, BakkerWW, Vernier RL, Hoedemaeker PJ (1978) Experimental glomerulonephritis in the rat induced by antibodies directed against tubular antigens. V. Fixed glomerular antigens in the pathogenesis of heterologous immune complex glomerulonephritis. Lab Investig 38:502-510 (Pubitemid 8338244)
16. Couser WG, Steinmuller DR, Stilmant MM, Salant DJ, Lowenstein LM (1978) Experimental glomerulonephritis in the isolated perfused rat kidney. J Clin Invest 62:1275-1287 (Pubitemid 9075757)
17. Kerjaschki D, Farquhar MG (1982) The pathogenic antigen of Heymann nephritis is a membrane glycoprotein of the renal proximal tubule brush border. Proc Natl Acad Sci 79:5557-5561 (Pubitemid 13197683)
18. Kerjaschki D, Farquhar MG (1983) Immunocytochemical localization of the Heymann nephritis antigen (gp330) in glomerular epithelial cells of normal Lewis rats. J Exp Med 157:667-686 (Pubitemid 13145068)
19. Shah P, Tramontano A, Makker SP (2007) Intramolecular spreading in Heymann nephritis. J Am Soc Nephrol 18:3060-3066
20. Prabakaran T, Nielsen R, Larsen JV, Sørensen SS, Feldt-Rasmussen U, Saleem MA, Petersen CM, Verroust PJ, Christensen EI (2011) Receptor-mediated endocytosis of α-galactosidase A in human podocytes in Fabry disease. PLoS One 6:e25065
21. Border WA, Ward HJ, Kamil ES, Cohen AH (1982) Induction of membranous nephropathy in rabbits by administration of an exogenous cationic antigen. J Clin Invest 69:451-461
22. Adler SG, Wang H, Ward HJ, Cohen AH, Border WA (1983) Electrical charge. Its role in the pathogenesis and prevention of experimental membranous nephropathy in the rabbit. J Clin Invest 71:487-499 (Pubitemid 13160794)
23. Koyama A, Inage H, Kobayashi M, Nakamura H, NaritaM, Tojo S (1986) Effect of chemical cationization of antigen on glomerular localization of immune complexes in active models of serum sickness nephritis in rabbits. Immunology 58:529-534 (Pubitemid 16068124)
24. Bass PS, Drake AF, Wang Y, Thomas JH, Davies DR (1990) Cationization of bovine serum albumin alters its conformation as well as its charge. Lab Investig 62:185-188 (Pubitemid 20108294)
25. Wright NG, Mohammed NA, Eckersall PD, Nash AS (1985) Experimental immune complex glomerulonephritis in dogs receiving cationized bovine serum albumin. Res Vet Sci 38:322-328 (Pubitemid 15091867)
26. Koyama A, Inage H, Kobayashi M, Ohta Y, Narita M, Tojo S, Cameron JS (1986) Role of antigenic charge and antibody avidity on the glomerular immune complex localization in serum sickness of mice. Clin Exp Immunol 64:606-614 (Pubitemid 16122399)
27. Kobayashi M, Muro K, Yoh K, Kondoh M, Iwabuchi S, Hirayama K, Ishizu (1998) Effects of FK506 on experimental membranous glomerulonephritis induced by cationized bovine serum albumin in rats. Nephrol Dial Transplant 13:2501-2508 (Pubitemid 28445862)
28. Debiec H, Guigonis V, Mougenot B, Decobert F, Haymann JP, Bensman A, Deschênes G, Ronco PM (2002) Antenatal membranous glomerulonephritis due to anti-neutral endopeptidase antibodies. N Engl J Med 346:2053-2060 (Pubitemid 34680597)
29. Ronco P, Debiec H, Guigonis V (2006) Mechanisms of disease: alloimmunization in renal diseases. Nat Clin Pract Nephrol 2:388-397 (Pubitemid 44034189)
30. Platt JL, Tucker WL, Michael AF (1983) Stages of renal ontogenesis identified by monoclonal antibodies reactive with lymphohematopoietic differentiation antigens. J Exp Med 157:155-172 (Pubitemid 13176181)
31. Appay MD, Mounier F, Gubler MC, Rouchon M, Beziau A, Kazatchkine MD (1985) Ontogenesis of the glomerular C3b receptor (CR1) in fetal human kidney. Clin Immunol Immunopathol 37:103-113 (Pubitemid 16242009)
32. Debiec H, Nauta J, Coulet F, van der Burg M, Guigonis V, Schurmans T, de Heer E, Soubrier F, Janssen F, Ronco P (2004) Role of truncating mutations in MME gene in feto-maternal allo-immunization and neonatal glomerulopathies. Lancet 364:1252-1259 (Pubitemid 39311346)
33. Ronco P, Debiec H (2005) Molecular pathomechanisms of membranous nephropathy: from Heymann nephritis to alloimmunization. J Am Soc Nephrol 16:1205-1213 (Pubitemid 41716505)
34. Vivarelli M, Gerken C, Pelle T, Pedicelli S, Diomedi F, Klaus G, Waldegger S, Emma F, Ronco P, Debiec H (2013) Alloimmune membranous nephropathywith anti-neutral endopeptidase antibodies: genetic homogeneity but IgG subclass-dependent clinical variability. Nephrol Dial Transplant 28 (suppl 1). ERA-EDTA congress in Istanbul 2013.
35. Nortier JL, Debiec H, Tournay Y, Mougenot B, Nöel JC, Deschodt-Lanckman MM, Janssen F, Ronco P (2006) Neonatal disease in neutral endopeptidase alloimmunization: lessons for immunological monitoring. Pediatr Nephrol 1:1399-1405 (Pubitemid 44283471)
36. Beck LH Jr, Bonegio RG, Lambeau G, Beck DM, Powell DW, Cummins TD, Klein JB, Salant DJ (2009) M-type phospholipase A2 receptor as target antigen in idiopathic MN. N Engl J Med 361:11-21
37. Stahl R, Hoxha E, Fechner K (2010) PLA2R autoantibodies and recurrent membranous nephropathy after transplantation. N Engl J Med 363:496-498
38. Blosser CD, Ayalon R, Nair R, Thomas C, Beck LH Jr (2012) Very early recurrence of anti-phospholipase A2 receptor-positive membranous nephropathy after transplantation. Am J Transplant 12:1637-1642
39. Debiec H, Martin L, Jouanneau C, Dautin G, Mesnard L, Rondeau E, Mousson C, Ronco P (2011) Autoantibodies specific for the phospholipase A(2) receptor in recurrent and de novo membranous nephropathy. Am J Transplant 11:2144-2152
40. Debiec H, Hanoy M, Francois A, Guerrot D, Ferlicot S, Johanet C, Aucouturier P, Godin M, Ronco P (2012) Recurrent membranous nephropathy in an allograft caused by IgG3κ targeting the PLA2 receptor. J Am Soc Nephrol 23:1949-1954
41. East L, Isacke CM (2002) The mannose receptor family. Biochim Biophys Acta 1572:364-386 (Pubitemid 35246355)
42. Llorca O (2008) Extended and bent conformations of the mannose receptor family. Cell Mol Life Sci 65:1302-1310
43. Behnert A, Fritzler MJ, Teng B, Zhang M, Bollig F, Haller H, Skoberne A, Mahler M, Schiffer M (2013) An anti-phospholipase A2 receptor quantitative immunoassay and epitope analysis in membranous nephropathy reveals different antigenic domains of the receptor. PLoS One 8(4):e61669
44. Vangelista A, Tazzari R, Bonomini V (1988) Idiopathic membranous nephropathy in twin brothers. Nephron 50:79-80
45. Bockenhauer D, Debiec H, Sebire N, Barratt M, Warwicker P, Ronco P, Kleta R (2008) Familial membranous nephropathy: an X-linked genetic susceptibility? Nephron Clin Pract 108:10-15
46. Short CD, Feehally J, Gokal R, Mallick NP (1984) Familial membranous nephropathy. Br Med J (Clin Res Ed) 289:1500 (Pubitemid 15219280)
47. Vasmant D, Murnaghan K, Bensman A, Muller JY, Mougenot B (1984) Familial idiopathic membranous glomerulonephritis. Int J Pediatr Nephrol 5:193-196 (Pubitemid 15124479)
48. Sato K, Oguchi H, Hora K, Furukawa T, Furuta S, Shigematsu H, Yoshizawa S (1987) Idiopathic membranous nephropathy in two brothers. Nephron 46:174-178 (Pubitemid 17074316)
49. Elshihabi I, Kaye CI, Brzowski A (1993) Membranous nephropathy in two human leukocyte antigen-identical brothers. J Pediatr 123:940-942 (Pubitemid 23353258)
50. Chen JS, Chen A, Chang LC, Chang WS, Lee HS, Lin SH, Lin YF (2004) Mouse model of membranous nephropathy induced by cationic bovine serum albumin: antigen dose-response relations and strain differences. Nephrol Dial Transplant 19:2721-2728 (Pubitemid 39480964)
51. Bagchus WM, Hoedemaeker PJ, Vos JT, Bakker WW (1989) Thymocytes reacting with heterologous antibodies against GP 330 in autologous immune complex glomerulopathy (AICG) in the rat. The relation between susceptibility for AICG and anti-GP 330-binding thymocytes. Immunobiology 179:432-444 (Pubitemid 19268317)
52. Klouda PT, Manos J, Acheson EJ, Dyer PA, Goldby FS, Harris R, Lawler W, Mallick NP, Williams G (1979) Strong association between idiopathic membranous nephropathy and HLA-DRW3. Lancet 2:770-771 (Pubitemid 10213789)
53. Le Petit JC, Laurent B, Berthoux FC (1982) HLA-DR3 and idiopathic membranous nephritis (IMN) association. Tissue Antigens 20:227-228
54. Berthoux FC, Alamartine E, Laurent B, Berthoux P, Vacherot C, Lambert C, Le Petit JC (1984) Immunogenetics and immunopathology of human primary membranous glomerulonephritis: HLA-A, B, DR antigens functional activity of splenic macrophage Fc-receptors and peripheral blood T-lymphocyte subpopulations. Clin Nephrol 22:15-20 (Pubitemid 14089426)
55. Vaughan RW, Demaine AG, Welsh KI (1989) A DQA1 allele is strongly associated with idiopathic membranous nephropathy. Tissue Antigens 34:261-269 (Pubitemid 20051630)
56. Dyer PA, Short CD, Clarke EA, Mallick NP (1992) HLA antigen and gene polymorphisms and haplotypes established by family studies in membranous nephropathy. Nephrol Dial Transplant 7(Suppl 1):42-47 (Pubitemid 23016766)
57. Sacks SH, Warner C, Campbell RD, Dunham I (1993) Molecular mapping of the HLA class II region in HLA-DR3 associated idiopathic membranous nephropathy. Kidney Int Suppl 39:S13-S19
58. Chevrier D, Giral M, Perrichot R, Latinne D, Coville P, Muller JY, Soulillou JP, Bignon JD (1997) Idiopathic and secondary membranous nephropathy and polymorphism at TAP1 and HLA-DMA loci. Tissue Antigens 50:164-169 (Pubitemid 27326282)
59. Stanescu HC, Arcos-Burgos M, Medlar A, Bockenhauer D, Kottgen A, Dragomirescu L, Voinescu C, Patel N, Pearce K, Hubank M, Stephens HA, Laundy V, Padmanabhan S, Zawadzka A, Hofstra JM, Coenen MJ, den Heijer M, Kiemeney LA, Bacq-Daian D, Stengel B, Powis SH, Brenchley P, Feehally J, Rees AJ, Debiec H, Wetzels JF, Ronco P, Mathieson PW, Kleta R (2011) Risk HLA-DQA1 and PLA(2)R1 alleles in idiopathic membranous nephropathy. N Engl J Med 364:616-626
60. Kanigicherla D, Gummadova J, McKenzie EA, Roberts SA, Harris S, Nikam M, Poulton K, McWilliam L, Short CD, Venning M, Brenchley PE (2013) Anti-PLA2R antibodies measured by ELISA predict long-term outcome in a prevalent population of patients with idiopathic membranous nephropathy. Kidney Int 83:940-948
61. Bullich G, Ballarín J, Oliver A, Ayasreh N, Silva I, Santín S, Díaz-Encarnación MM, Torra R, Ars E (2014) HLA-DQA1 and PLA2R1 polymorphisms and risk of idiopathic membranous nephropathy. Clin J Am Soc Nephrol 9:335-343
62. Liu YH, Chen CH, Chen SY, Lin YJ, Liao WL, Tsai CH, Wan L, Tsai FJ (2010) Association of phospholipase A2 receptor 1 polymorphisms with idiopathic membranous nephropathy in Chinese patients in Taiwan. J Biomed Sci 17:81-88
63. Kim S, Chin HJ, Na KY, Kim S, Oh J, ChungW, Noh JW, Lee YK, Cho JT, Lee EK, Chae DW (2011) Single nucleotide polymorphisms in the phospholipase A2 receptor gene are associated with genetic susceptibility to idiopathic membranous nephropathy. Nephron Clin Pract 117:c253-c258
64. Lv J, Hou W, Zhou X, Liu G, Zhou F, Zhao N, Hou P, Zhao M, Zhang H (2013) Interaction between PLA2R1 and HLA-DQA1 variants associates with anti-PLA2R antibodies and membranous nephropathy. J Am Soc Nephrol 24:1323-1329
65. Coenen MJ, Hofstra JM, Debiec H, Stanescu HC, Medlar AJ, Stengel B, Boland-Augé A, Groothuismink JM, Bockenhauer D, Powis SH, Mathieson PW, Brenchley PE, Kleta R, Wetzels JF, Ronco P (2013) Phospholipase A2 receptor (PLA2R1) sequence variants in idiopathic membranous nephropathy. J Am Soc Nephrol 24:677-683
66. Bantis C, Heering PJ, Aker S, Siekierka M, Kuhr N, Grabensee B, Ivens K (2006) Tumor necrosis factor-alpha gene G-308A polymorphism is a risk factor for the development of membranous glomerulonephritis. Am Nephrol 26:12-15
67. Thibaudin D, Thibaudin L, Berthoux P, Mariat C, Filippis JP, Laurent B, Alamartine E, Berthoux F (2007) TNFA2 and d2 alleles of the tumor necrosis factor alpha gene polymorphism are associated with onset/occurrence of idiopathic membranous nephropathy. Kidney Int 71:431-437
68. Honkanen E, vonWillebrand E, Teppo AM, Törnroth T, Grönhagen-Riska C (1998) Adhesion molecules and urinary tumor necrosis factor-alpha in idiopathic membranous glomerulonephritis. Kidney Int 53:909-917 (Pubitemid 28155663)
69. Neale TJ, Rüger BM, Macaulay H, Dunbar PR, Hasan Q, Bourke A, Murray-McIntosh RP, Kitching AR (1995) Tumor necrosis factor-alpha is expressed by glomerular visceral epithelial cells in human membranous nephropathy. Am J Pathol 146:1444-1454
70. Tabibzadeh S, Kong QF, Kapur S et al (1995) TNF-alpha induces dyscohesion of epithelial cells-association with disassembly of actin filaments. Endocrine 3:549-556
71. Huber TB, Benzing T (2005) The slit diaphragm: a signaling platform to regulate podocyte function. Curr Opin Nephrol Hypertens 14:211-216 (Pubitemid 40685631)
72. Lo WY, Chen SY, Wang HJ, Shih HC, Chen CH, Tsai CH, Tsai FJ (2010) Association between genetic polymorphisms of the NPHS1 gene and membranous in the Taiwanese population. Clin Chim Acta 411:714-718
73. Chen CH, Shu KH, Wen MC, Chen KJ, Cheng CH, Lian JD, Wu MJ, Yu TM, Tsai FJ (2008) Impact of plasminogen activator inhibitor-1 gene polymorphisms on primary membranous nephropathy. Nephrol Dial Transplant 23:3166-3173
74. Luo Y, Wang C, Tu H (2014) Impact of the 4G/5G polymorphismin the plasminogen activator inhibitor-1 gene on primary nephrotic syndrome. Mol Med Rep 9:894-898
75. Chen SY, Chen CH, Huang YC, Chuang HM, Lo MM, Tsai FJ (2010) Effect of IL-6C-572G polymorphism on idiopathic membranous nephropathy risk in a Han Chinese population. Ren Fail 32:1172-1176
76. Chen SY, Chen CH, Huang YC, Chan CJ, Hsieh YY, Yu MC, Tsai CH, Tsai FJ (2011) Association of STAT4 polymorphisms with susceptibility to primary membranous glomerulonephritis and renal failure. Clin Chim Acta 412:1899-1904
77. Chen YT, Wei CC, Ng KL, Chen CH, Chan CJ, Chen XX, Chang YY, Chen SY, Tsai FJ (2013) Toll-like receptor 9 SNPs are susceptible to the development and progression of membranous glomerulonephritis: 27 years follow-up in Taiwan. Ren Fail 35:1370-1375
78. Debiec H, Ronco P (2011) Nephrotic syndrome: a new specific test for idiopathic membranous nephropathy. Nat Rev Nephrol 7:496-498
79. Hoxha E, Harendza S, Zahner G, Panzer U, Steinmetz O, Fechner K, Helmchen U, Stahl RA (2011) An immunofluorescence test for phospholipase-A2-receptor antibodies and its clinical usefulness in patients with membranous glomerulonephritis. Nephrol Dial Transplant 26:2526-2532
80. Dähnrich C, Komorowski L, Probst C, Seitz-Polski B, Esnault V, Wetzels JF, Hofstra JM, Hoxha E, Stahl RA, Lambeau G, Stöcker W, Schlumberger W (2013) Development of a standardized ELISA for the determination of autoantibodies against human M-type phospholipase A2 receptor in primary membranous nephropathy. Clin Chim Acta 421:213-218
81. Qin W, Beck LH Jr, Zeng C, Chen Z, Li S, Zuo K, Salant DJ, Liu Z (2011) Anti-phospholipase A2 receptor antibody in membranous nephropathy. J Am Soc Nephrol 22:1137-1143
82. Knehtl M, Debiec H, Kamgang P, Callard P, Cadranel J, Ronco P, Boffa JJ (2011) A case of phospholipase A2 receptor-positive membranous nephropathy preceding sarcoid-associated granulomatous tubulointerstitial nephritis. Am J Kidney Dis 57:140-143
83. Nawaz FA, Larsen CP, Troxell ML (2013) Membranous nephropathy and nonsteroidal anti-inflammatory agents. Am J Kidney Dis 62:1012-1017
84. Huang X, Qin W, Zhang M, Zheng C, Zeng C, Liu Z (2013) Detection of anti-PLA2R autoantibodies and IgG subclasses in post-allogeneic hematopoietic stem cell transplantation membranous nephropathy. Am J Med Sci 346:32-37
85. Svobodova B, Honsova E, Ronco P, Tesar V, Debiec H (2013) Kidney biopsy is a sensitive tool for retrospective diagnosis of PLA2R-related membranous nephropathy. Nephrol Dial Transplant 28:1839-1844
86. Larsen CP, Messias NC, Silva FG, Messias E, Walker PD (2013) Determination of primary versus secondary membranous glomerulopathy utilizing phospholipaseA2 receptor staining in renal biopsies. Mod Pathol 26:709-715
87. Debiec H, Ronco P (2011) PLA2R autoantibodies and PLA2R glomerular deposits in membranous nephropathy. N Engl J Med 364:689-690
88. Hoxha E, Kneißler U, Stege G, Zahner G, Thiele I, Panzer U, Harendza S, Helmchen UM, Stahl RA (2012) Enhanced expression of the M-type phospholipase A2 receptor in glomeruli correlates with serum receptor antibodies in primary membranous nephropathy. Kidney Int 82:797-804
89. Kuroki A, Shibata T, Honda H, Totsuka D, Kobayashi K, Sugisaki T (2002) Glomerular and serum IgG subclasses in diffuse proliferative lupus nephritis, membranous lupus nephritis, and idiopathic membranous nephropathy. Intern Med 41:936-942 (Pubitemid 35423073)
90. Ohtani H, Wakui H, Komatsuda A, Okuyama S, Masai R, Maki N, Kigawa A, Sawada K, Imai H (2004) Distribution of glomerular IgG subclass deposits in malignancy-associated membranous nephropathy. Nephrol Dial Transplant 19:574-579 (Pubitemid 38263115)
91. Segawa Y, Hisano S, Matsushita M, Fujita T, Hirose S, Takeshita M, Iwasaki H (2010) IgG subclasses and complement pathway in segmental and global membranous nephropathy. Pediatr Nephrol 25:1091-1099
92. Qu Z, Liu G, Li J, Wu LH, Tan Y, Zheng X, Ao J, Zhao MH (2012) Absence of glomerular IgG4 deposition in patients with membranous nephropathy may indicate malignancy. Nephrol Dial Transplant 27:1931-1937
93. Hofstra JM, Beck LH Jr, Beck DM, Wetzels JF, Salant DJ (2011) Anti-phospholipase A2 receptor antibodies correlate with clinical status in idiopathic membranous nephropathy. Clin J Am Soc Nephrol 6:1286-1291
94. Beck LH Jr, Fervenza FC, Beck DM, Bonegio RG, Malik FA, Erickson SB, Cosio FG, Cattran DC, Salant DJ (2011) Rituximab-induced depletion of anti-PLA2R autoantibodies predicts response in membranous nephropathy. J Am Soc Nephrol 22:1543-1550
95. Hofstra JM, Debiec H, Short CD, Pellé T, Kleta R, Mathieson PW, Ronco P, Brenchley PE, Wetzels JF (2012) Antiphospholipase A2 receptor antibody titer and subclass in idiopathic membranous nephropathy. J Am Soc Nephrol 23:1735-1743
96. Oh YJ, Yang SH, Kim DK, Kang SW, Kim YS (2013) Autoantibodies against phospholipase A2 receptor in Korean patients with membranous nephropathy. PLoS One 8:e62151
97. Hofstra J, Bech A, Brenchley P, Wetzels J (2013) Measurement of anti PLA2R antibodies predicts relapse rate after immunosuppressive therapy in patients with idiopathic membranous nephropathy, abstract [OR049] ASN meeting Atlanta 2013
98. Hu SL, Wang D, Gou WJ, Lei QF, Ma TA, Cheng JZ (2014) Diagnostic value of phospholipase A(2) receptor in idiopathic membranous nephropathy: a systematic review and meta-analysis. J Nephrol 27:111-116
99. Briganti EM, Russ GR, McNeil JJ, Atkins RC, Chadban SJ (2002) Risk of renal allograft loss from recurrent glomerulonephritis. N Engl J Med 347:103-109 (Pubitemid 34753480)
100. Dabade TS, Grande JP, Norby SM, Fervenza FC, Cosio FG (2008) Recurrent idiopathic membranous nephropathy after kidney transplantation: a surveillance biopsy study.AmJ Transplant 8:1318-1322 (Pubitemid 351763689)
101. Larsen CP, Walker PD (2013) Phospholipase A2 receptor (PLA2R) staining is useful in the determination of de novo versus recurrent membranous glomerulopathy. Transplantation 95:1259-1262
102. Takahashi S, Hiromura K, Tsukida M, Ohishi Y, Hamatani H, Sakurai N, Sakairi T, Ikeuchi H, Kaneko Y, Maeshima A, Kuroiwa T, Yokoo H, Aoki T, Nagata M, Nojima Y (2013) Nephrotic syndrome caused by immune-mediated acquired LCAT deficiency. J Am Soc Nephrol 24:1305-1312
103. Prunotto M, Carnevali ML, Candiano G, Murtas C, Bruschi M, Corradini E, Trivelli A, Magnasco A, Petretto A, Santucci L, Mattei S, Gatti R, Scolari F, Kador P, Allegri L, Ghiggeri GM (2010) Autoimmunity in membranous nephropathy targets aldose reductase and SOD2. J Am Soc Nephrol 21:507-519
104. Bruschi M, Carnevali ML, Murtas C, Candiano G, Petretto A, Prunotto M, Gatti R, Argentiero L, Magistroni R, Garibotto G, Scolari F, Ravani P, Gesualdo L, Allegri L, Ghiggeri GM (2011) Direct characterization of target podocyte antigens and autoantibodies in human membranous glomerulonephritis: alfa-enolase and borderline antigens. J Proteomics 74:2008-2017
105. Murtas C, Bruschi M, Candiano G, Moroni G, Magistroni R, Magnano A, Bruno F, Radice A, Furci L, Argentiero L, Carnevali ML, Messa P, Scolari F, Sinico RA, Gesualdo L, Fervenza FC, Allegri L, Ravani P, Ghiggeri GM (2012) Coexistence of different circulating anti-podocyte antibodies in membranous nephropathy. Clin J Am Soc Nephrol 7:1394-1400
106. Ronco P, Debiec H, Imai H (2013) Circulating antipodocyte antibodies in membranous nephropathy: pathophysiologic and clinical relevance. Am J Kidney Dis 62:16-19
107. Debiec H, Lefeu F, Kemper MJ, Niaudet P, Deschênes G, Remuzzi G, Ulinski T, Ronco P (2011) Early childhood membranous nephropathy due to cationic bovine serum albumin. N Engl J Med 364:2101-2110
108. Sathe SK, Teuber SS, Roux KH (2005) Effects of food processing on the stability of food allergens. Biotechnol Adv 23:423-429 (Pubitemid 40984979)
109. Sanchez C, Fremont S (2003) Consequences of heat treatment and processing of food on the structure and allergenicity of component proteins. Rev Fr Allergol Immunol Clin 43:13-20 (Pubitemid 36188390)
110. van Elburg RM, Fetter WP, Bunkers CM, Heymans HS (2003) Intestinal permeability in relation to birth weight and gestational and postnatal age. Arch Dis Child Fetal Neonatal Ed 88:F52-F55 (Pubitemid 36084209)
111. Sreedharan R, Mehta DI (2004) Gastrointestinal tract. Pediatrics 113:1044-1050 (Pubitemid 38437357)
112. Torente F, Murch S (2004) Food allergic enteropathy. In: Walker AW, Goulet O, Kleinman RE et al (eds) Pediatric gastrointestinal disease, 4th edn. BC Decker, Hamilton, pp 944-958
113. Richards SM (2002) Immunologic considerations for enzyme replacement therapy in the treatment of lysosomal storage disorders. Clin Appl Immunol Rev 2:241-253
114. Brooks DA (1999) Immune response to enzyme replacement therapy in lysosomal storage disorder patients and animal models. Mol Genet Metab 68:268-275
115. Koren E, Zuckerman LA,Mire-Sluis AR (2002) Immune responses to therapeutic proteins in humans - clinical significance, assessment and prediction. Curr Pharm Biotechnol 3:349-360 (Pubitemid 35364009)
116. Hunley TE, Corzo D, Dudek M, Kishnani P, Amalfitano A, Chen YT, Richards SM, Phillips JA 3rd, Fogo AB, Tiller GE (2004) Nephrotic syndrome complicating alpha-glucosidase replacement therapy for Pompe disease. Pediatrics 114:e532-e535 (Pubitemid 41529751)
117. Debiec H, Valayannopoulos V, Boyer O, Nöel LH, Callard P, Sarda H, de Lonlay P, Niaudet P, Ronco P (2013) Allo-immune membranous nephropathy and recombinant aryl sulfatase replacement therapy: a need for tolerance induction therapy. J Am Soc Nephrol 25:675-680
118. Jordan SC, Buckingham B, Sakai R, Olson D (1981) Studies of immune-complex glomerulonephritis mediated by human thyroglobulin. N Engl J Med 304:1212-1215 (Pubitemid 11102801)
119. Hörl WH, Kerjaschki D (2000) Membranous glomerulonephritis (MGN). J Nephrol 13:291-316
120. Bhimma R, Coovadia HM (2004) Hepatitis B virus-associated nephropathy. Am J Nephrol 24:198-211 (Pubitemid 38456630)
121. Nakahara K, Takahashi H, Okuse C, Shigefuku R, Yamada N, Murao M, Matsunaga K, Koike J, Yotsuyanagi H, Suzuki M, Kimura K, Itoh F (2010)Membranous nephropathy associated with chronic hepatitis B occurring in a short period after acute hepatitis B virus infection. Intern Med 49:383-388
122. Guiard E, Karras A, Plaisier E, Duong Van Huyen JP, Fakhouri F, Rougier JP, Noel LH, Callard P, Delahousse M, Ronco P (2011) Patterns of noncryoglobulinemic glomerulonephritis with monoclonal Ig deposits: correlation with IgG subclass and response to rituximab. Clin J Am Soc Nephrol 6:1609-1616
123. de Seigneux S, Bindi P, Debiec H, Alyanakian MA, Aymard B, Callard P, Ronco P, Aucouturier P (2010) Immunoglobulin deposition disease with a membranous pattern and a circulating monoclonal immunoglobulin G with charge-dependent aggregation properties. Am J Kidney Dis 56:117-121
124. Lundberg K, Venables PJ (2008) Epitope spreading in animal models: array of hope in rheumatoid arthritis and multiple sclerosis. Arthritis Res Ther 10:122
125. Chen L, Hellmark T, Pedchenko V, Hudson BG, Pusey CD, Fox JW, Bolton WK (2006) A nephritogenic peptide induces intermolecular epitope spreading on collagen IV in experimental autoimmune glomerulonephritis. J Am Soc Nephrol 17:3076-3081 (Pubitemid 44707768)
126. Adler S, Chen X (1992) Anti-Fx1A antibody recognizes a beta 1-integrin on glomerular epithelial cells and inhibits adhesion and growth. Am J Physiol 262:F770-F776
127. Binstadt BA, Patel PR, Alencar H, Nigrovic PA, Lee DM,Mahmood U, Weissleder R, Mathis D, Benoist C (2006) Particularities of the vasculature can promote the organ specificity of autoimmune attack. Nat Immunol 7:284-292
128. Spicer ST, Tran GT, KillingsworthMC, Carter N, Power DA, Paizis K, Boyd R, Hodgkinson SJ, Hall BM (2007) Induction of passive Heymann nephritis in complement component 6-deficient PVG rats. J Immunol 179:172-178 (Pubitemid 46986531)
129. Leenaerts PL, Hall BM, Van Damme BJ, DahaMR, Vanrenterghem YF (1995) Active Heymann nephritis in complement component C6 deficient rats. Kidney Int 47:1604-1614
130. Kerjaschki D, Exner M, Ullrich R, Susani M, Curtiss LK, Witztum JL, Farquhar MG, Orlando RA (1997) Pathogenic antibodies inhibit the binding of apolipoproteins to megalin/gp330 in passive Heymann nephritis. J Clin Invest 100:2303-2309 (Pubitemid 27500153)
131. Turner AJ, Isaac RE, Coates D (2001) The neprilysin (NEP) family of zinc metalloendopeptidases: genomics and function. Bioessays 23:261-269 (Pubitemid 32192145)
132. Ancian P, Lambeau G, LazdunskiM(1995)Multifunctional activity of the extracellular domain of the M-type (180 kDa) membrane receptor for secretory phospholipases A2. Biochemistry 34:13146-13151
133. Zvaritch E, Lambeau G, Lazdunski M (1996) Endocytic properties of the M-type 180-kDa receptor for secretory phospholipases A2. J Biol Chem 271:250-257 (Pubitemid 26026586)
134. Hanasaki K, Arita H (2002) Phospholipase A2 receptor: a regulator of biological functions of secretory phospholipase A2. Prostaglandins Other Lipid Mediat 69:71-82 (Pubitemid 35247388)
135. Lambeau G, Gelb MH (2008) Biochemistry and physiology of mammalian secreted phospholipases A2. Annu Rev Biochem 77:495-520
136. Augert A, Payré C, de Launoit Y, Gil J, Lambeau G, Bernard D (2009) The M-type receptor PLA2R regulates senescence through the p53 pathway. EMBO Rep 10:271-217
137. Sis B, Tasanarong A, Khoshjou F, Dadras F, Solez K, Halloran PF (2007) Accelerated expression of senescence associated cell cycle inhibitor p16INK4A in kidneys with glomerular disease. Kidney Int 71:218-226 (Pubitemid 46160922)
138. Cybulsky AV, Quigg RJ, Salant DJ (2005) Experimental membranous nephropathy redux. Am J Physiol Renal Physiol 289:F660-F671 (Pubitemid 41324186)
139. Sarma JV, Ward PA (2011) The complement system. Cell Tissue Res 343:227-235
140. Morgan BP, Haris CL (1999) Regulation in the activation pathways. In: Complement regulatory proteins. Academic, San Diego, pp 41-136
141. Naik A, Sharma S, Quigg RJ (2013) Complement regulation in renal disease models. Semin Nephrol 33:575-585
142. Loirat C, Frémeaux-Bacchi V (2011) Atypical hemolytic uremic syndrome. Orphanet J Rare Dis 6:60-90
143. Hughes AE, Orr N, Esfandiary H, Diaz-Torres M, Goodship T, Chakravarthy U (2006) A common CFH haplotype, with deletion of CFHR1 and CFHR3, is associated with lower risk of age-related macular degeneration. Nat Genet 38:1173-1177 (Pubitemid 44470363)
144. Gold B, Merriam JE, Zernant J, Hancox LS, Taiber AJ, Gehrs K, Cramer K, Neel J, Bergeron J, Barile GR, Smith RT, AMD Genetics Clinical Study Group, Hageman GS, Dean M, Allikmets R (2006) Variation in factor B (BF) and complement component 2 (C2) genes is associated with age-related macular degeneration. Nat Genet 38:458-462
145. van der Zee JS, van Swieten P, Aalberse RC (1986) Inhibition of complement activation by IgG4 antibodies. Clin Exp Immunol 64:415-422
146. Aalberse RC, Schuurman J (2002) IgG4 breaking the rules. Immunology 105:9-19 (Pubitemid 34128035)
147. Huang CC, Lehman A, Albawardi A, Satoskar A, Brodsky S, Nadasdy G, Hebert L, Rovin B, Nadasdy T (2013) IgG subclass staining in renal biopsies with membranous glomerulonephritis indicates subclass switch during disease progression. Mod Pathol 26:799-805
148. Lhotta K, Würzner R, König P (1999) Glomerular deposition of mannose-binding lectin in human glomerulonephritis. Nephrol Dial Transplant 14:881-886
149. Espinosa-Hernández M, Ortega-Salas R, López-Andreu M, Gómez-Carrasco JM, Pérez-Sáez MJ, Pérez-Seoane C, Aljama-García P (2012) C4d as a diagnostic tool in membranous nephropathy. Nefrologia 32:295-299
150. Thiel S, GadjevaM (2009) Humoral pattern recognition molecules: mannan-binding lectin and ficolins. Adv Exp Med Biol 653:58-73
151. Malhotra R, Wormald MR, Rudd PM, Fischer PB, Dwek RA, Sim RB (1995) Glycosylation changes of IgG associated with rheumatoid arthritis can activate complement via the mannose-binding protein. Nat Med 1:237-243
152. Bond A, Alavi A, Axford JS, Bourke BE, Bruckner FE, Kerr MA, Maxwell JD, Tweed KJ, Weldon MJ, Youinou P, Hay FC (1997) A detailed lectin analysis of IgG glycosylation, demonstrating disease specific changes in terminal galactose and N-acetylglucosamine. J Autoimmun 10:77-85 (Pubitemid 27110310)
153. Parekh R, Isenberg D, Rook G, Roitt I, Dwek R, Rademacher T (1989) A comparative analysis of disease-associated changes in the galactosylation of serum IgG. J Autoimmun 2:101-114
154. Ma H, Beck LH Jr, Salant D (2011) J Am Soc Nephrol 22:62A, abstr. ASN congress in 2013.
155. Rispens T, Ooievaar-De Heer P, Vermeulen E, Schuurman J, van der Neut Kolfschoten M, Aalberse RC (2009) Human IgG4 binds to IgG4 and conformationally altered IgG1 via Fc-Fc interactions. J Immunol 182:4275-4281
156. Ito T, Kitahara K, Umemura T, Ota M, Shimozuru Y, Kawa S, Bahram S (2010) A novel heterophilic antibody interaction involves IgG4. Scand J Immunol 71:109-114
157. Nangaku M, Shankland SJ, Couser WG (2005) Cellular response to injury in membranous nephropathy. J Am Soc Nephrol 16:1195-1204 (Pubitemid 41716504)
158. Cunningham PN, Quigg RJ (2005) Contrasting roles of complement activation and its regulation in membranous nephropathy. J Am Soc Nephrol 16:1214-1222 (Pubitemid 41716506)
159. Tegla CA, Cudrici C, Patel S, Trippe R 3rd, Rus V, Niculescu F, Rus H (2011) Membrane attack by complement: the assembly and biology of terminal complement complexes. Immunol Res 51:45-60
160. Bohana-Kashtan O, Ziporen L, Donin N, Kraus S, Fishelson Z (2004) Cell signals transduced by complement. Mol Immunol 41:583-597 (Pubitemid 38824616)
161. Moskovich O, Fishelson Z (2000) Live cell imaging of outward and inward vesiculation induced by the complement c5b-9 complex. J Biol Chem 28:29977-29986
162. Kerjaschki D, Schulze M, Binder S, Kain R, Ojha PP, Susani M, Horvat R, Baker PJ, CouserWG (1989) Transcellular transport and membrane insertion of the C5b-9 membrane attack complex of complement by glomerular epithelial cells in experimental membranous nephropathy. J Immunol 143:546-552 (Pubitemid 19191550)
163. Kon SP, Coupes B, Short CD, Solomon LR, Raftery MJ, Mallick NP, Brenchley PE (1995) Urinary C5b-9 excretion and clinical course in idiopathic human membranous nephropathy. Kidney Int 48:1953-1958
164. Cybulsky AV (2010) Endoplasmic reticulum stress in proteinuric kidney disease. Kidney Int 7:187-193
165. Cybulsky AV (2013) The intersecting roles of endoplasmic reticulum stress, ubiquitin- proteasome system, and autophagy in the pathogenesis of proteinuric kidney disease. Kidney Int 84:25-33
166. Wang L, Hong Q, Lv Y, Feng Z, Zhang X, Wu L, Cui S, Hou K, Su H, Huang Z, Wu D, Chen X (2012) Autophagy can repair endoplasmic reticulum stress damage of the passive Heymann nephritis model as revealed by proteomics analysis. J Proteomics 75:3866-3876
167. Meyer-Schwesinger C, Meyer TN, Sievert H, Hoxha E, Sachs M, Klupp EM, Münster S, Balabanov S, Carrier L, Helmchen U, Thaiss F, Stahl RA (2011) Ubiquitin C-terminal hydrolase-l1 activity induces polyubiquitin accumulation in podocytes and increases proteinuria in rat membranous nephropathy. Am J Pathol 178:2044-2057
168. Meyer-Schwesinger C, Meyer TN, Münster S, Klug P, Saleem M, Helmchen U, Stahl RA (2009) A new role for the neuronal ubiquitin C-terminal hydrolase-L1 (UCH-L1) in podocyte process formation and podocyte injury in human glomerulopathies. J Pathol 217:452-464
169. Hetz C (2012) The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol 13:89-102