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Современные представления о роли системы комплемента при мембранозной нефропатии - Журнал Терапевтический архив №6 Вопросы нефрологии 2022
Современные представления о роли системы комплемента при мембранозной нефропатии
Камышова Е.С., Семерюк Т.А., Бобкова И.Н. Современные представления о роли системы комплемента при мембранозной нефропатии. Терапевтический архив. 2022;94(6):772–776.
DOI: 10.26442/00403660.2022.06.201563
DOI: 10.26442/00403660.2022.06.201563
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Аннотация
Мембранозная нефропатия (МН) – иммунологически опосредованное гломерулярное заболевание, которое является наиболее частой причиной нефротического синдрома у взрослых. Протеинурия при МН развивается в результате повреждения подоцитов, обусловленного активацией системы комплемента в ответ на отложение в субэпителиальном пространстве иммунных комплексов, содержащих различные ауто- и экзогенные антигены. Ведущую роль в реализации комплементоопосредованного подоцитарного повреждения играет мембраноатакующий комплекс (МАК), представляющий собой конечный продукт активации системы комплемента по любому из трех путей (классическому, лектиновому или альтернативному). В настоящее время основной путь активации комплемента, приводящий к формированию МАК при МН, не установлен. В статье обсуждаются современные доказательства участия в развитии МН различных путей активации комплемента, в том числе в зависимости от природы антигена и подкласса IgG, а также недавно установленные новые молекулярные механизмы повреждения подоцитов, обусловленные активацией комплемента.
Ключевые слова: мембранозная нефропатия, комплемент, мембраноатакующий комплекс, IgG4, рецептор фосфолипазы А2, PLA2R
Keywords: membranous nephropathy, complement, membrane attack complex, IgG4, phospholipase A2 receptor, PLA2R
Ключевые слова: мембранозная нефропатия, комплемент, мембраноатакующий комплекс, IgG4, рецептор фосфолипазы А2, PLA2R
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Keywords: membranous nephropathy, complement, membrane attack complex, IgG4, phospholipase A2 receptor, PLA2R
Полный текст
Список литературы
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2. Perkinson DT, Baker PJ, Couser WG, et al. Membrane attack complex deposition in experimental glomerular injury. Am J Pathol. 1985;120(1):121-8.
3. Couser WG, Johnson RJ, Young BA, et al. The effects of soluble recombinant complement receptor 1 on complement-mediated experimental glomerulonephritis. J Am Soc Nephrol. 1995;5(11):1888‑94. DOI:10.1681/ASN.V5111888
4. Petermann AT, Krofft R, Blonski M, et al. Podocytes that detach in experimental membranous nephropathy are viable. Kidney Int. 2003;64(4):1222-31.
DOI:10.1046/j.1523-1755.2003.00217.x
5. Kerjaschki D, Schulze M, Binder S, et al. Transcellular transport and membrane insertion of the C5b-9 membrane attack complex of complement by glomerular epithelial cells in experimental membranous nephropathy. J Immunol. 1989;143(2):546-52.
6. Takano T, Elimam H, Cybulsky AV. Complement-Mediated Cellular Injury. Semin Nephrol. 2013;33(6):586-601. DOI:10.1016/j.semnephrol.2013.08.009
7. Koopman JJE, van Essen MF, Rennke HG, et al. Deposition of the Membrane Attack Complex in Healthy and Diseased Human Kidneys. Front Immunol. 2021;11:599974. DOI:10.3389/fimmu.2020.599974
8. Ootaka T, Suzuki M, Sudo K, et al. Histologic localization of terminal complement complexes in renal diseases. An immunohistochemical study. Am J Clin Pathol. 1989;91(2):144-51. DOI:10.1093/ajcp/91.2.144
9. Lai KN, Lo ST, Lai FM. Immunohistochemical study of the membrane attack complex of complement and S-protein in idiopathic and secondary membranous nephropathy. Am J Pathol. 1989;135(3):469-76.
10. Papagianni AA, Alexopoulos E, Leontsini M, Papadimitriou M. C5b-9 and adhesion molecules in human idiopathic membranous nephropathy. Nephrol Dial Transplant. 2002;17(1):57-63. DOI:10.1093/ndt/17.1.57
11. Salant DJ, Belok S, Madaio MP, Couser WG. A new role for complement in experimental membranous nephropathy in rats. J Clin Invest. 1980;66(6):1339-50. DOI:10.1172/JCI109987
12. Baker PJ, Ochi RF, Schulze M, et al. Depletion of C6 prevents development of proteinuria in experimental membranous nephropathy in rats. Am J Pathol. 1989;135(1):185-94.
13. Schulze M, Donadio JV Jr, Pruchno CJ, et al. Elevated urinary excretion of the C5b-9 complex in membranous nephropathy. Kidney Int. 1991;40(3):533-8. DOI:10.1038/ki.1991.242
14. Montinaro V, Lopez A, Monno R, et al. Renal C3 synthesis in idiopathic membranous nephropathy: correlation to urinary C5b-9 excretion. Kidney Int. 2000;57(1):137-46. DOI:10.1046/j.1523-1755.2000.00812.x
15. Zhang MF, Huang J, Zhang YM, et al. Complement activation products in the circulation and urine of primary membranous nephropathy. BMC Nephrol. 2019;20(1):313. DOI:10.1186/s12882-019-1509-5
16. Kon SP, Coupes B, Short CD, et al. Urinary C5b-9 excretion and clinical course in idiopathic human membranous nephropathy. Kidney Int. 1995;48(6):1953-8. DOI:10.1038/ki.1995.496
17. Brenchley PE, Coupes B, Short CD, et al. Urinary C3dg and C5b-9 indicate active immune disease in human membranous nephropathy. Kidney Int. 1992;41(4):933-7. DOI:10.1038/ki.1992.143
18. Coupes BM, Kon SP, Brenchley PEC, et al. The temporal relationship between urinary C5b-9 and C3dg and clinical parameters in human membranous nephropathy. Nephrol Dial Transplant. 1993;8(5):397-401. DOI:10.1093/oxfordjournals.ndt.a092491
19. Leenaerts PL, Hall BM, Van Damme BJ, et al. Active Heymann nephritis in complement component C6 deficient rats. Kidney Int. 1995;47(6):1604-14. DOI:10.1038/ki.1995.224
20. Spicer ST, Tran GT, Killingsworth MC, et al. Induction of passive Heymann nephritis in complement component 6-deficient PVG rats. J Immunol. 2007;179(1):172-8. DOI:10.4049/jimmunol.179.1.172
21. Alsharhan L, Beck LH. Membranous Nephropathy: Core Curriculum 2021. Am J Kidney Dis. 2021;77(3):440-53. DOI:10.1053/j.ajkd.2020.10.009
22. Beck LH Jr, Bonegio RG, Lambeau G, et al. M-type phospholipase A2 receptor as target antigen in idiopathic membranous nephropathy. N Engl J Med. 2009;361(1):11-21. DOI:10.1056/NEJMoa0810457
23. Tomas NM, Beck LH Jr, Meyer-Schwesinger C, et al. Thrombospondin type-1 domain-containing 7A in idiopathic membranous nephropathy. N Engl J Med. 2014;371(24):2277-87. DOI:10.1056/NEJMoa1409354
24. Borza DB. Alternative Pathway Dysregulation and the Conundrum of Complement Activation by IgG4 Immune Complexes in Membranous Nephropathy. Front Immunol. 2016;7:157. DOI:10.3389/fimmu.2016.00157
25. Jennette JC, Hipp CG. Immunohistopathologic evaluation of C1q in 800 renal biopsy specimens. Am J Clin Pathol. 1985;83(4):415-20. DOI:10.1093/ajcp/83.4.415
26. Segawa Y, Hisano S, Matsushita M, et al. IgG subclasses and complement pathway in segmental and global membranous nephropathy. Pediatr Nephrol. 2010;25(6):1091-9. DOI:10.1007/s00467-009-1439-8
27. Yang Y, Wang C, Jin L, et al. IgG4 anti-phospholipase A2 receptor might activate lectin and alternative complement pathway meanwhile in idiopathic membranous nephropathy: an inspiration from a cross-sectional study. Immunol Res. 2016;64(4):919-30. DOI:10.1007/s12026-016-8790-1
28. Hayashi N, Okada K, Matsui Y, et al. G-32lomerular mannose-binding lectin deposition in intrinsic antigen-related membranous nephropathy. Nephrol Dial Transplant. 2018;33(5):832-40. DOI:10.1093/ndt/gfx235
29. Haddad G, Lorenzen JM, Ma H, et al. Altered glycosylation of IgG4 promotes lectin complement pathway activation in anti-PLA2R1-associated membranous nephropathy. J Clin Invest. 2021;131(5):e140453. DOI:10.1172/JCI140453
30. Huang CC, Lehman A, Albawardi A, et al. IgG subclass staining in renal biopsies with membranous glomerulonephritis indicates subclass switch during disease progression. Mod Pathol. 2013;26(6):799-805. DOI:10.1038/modpathol.2012.237
31. Zhang MF, Cui Z, Zhang YM, et al. Clinical and prognostic significance of glomerular C1q deposits in primary MN. Clin Chim Acta. 2018;485:152-7. DOI:10.1016/j.cca.2018.06.050
32. Wiech T, Stahl RAK, Hoxha E. Diagnostic role of renal biopsy in PLA2R1-antibody-positive patients with nephrotic syndrome. Mod Pathol. 2019;32(9):1320-8.
DOI:10.1038/s41379-019-0267-z
33. Larsen CP, Messias NC, Silva FG, et al. Determination of primary versus secondary membranous glomerulopathy utilizing phospholipase A2 receptor staining in renal biopsies. Mod Pathol. 2013;26(5):709-15. DOI:10.1038/modpathol.2012.207
34. Ravindran A, Madden B, Charlesworth MC, et al. Proteomic Analysis of Complement Proteins in Membranous Nephropathy. Kidney Int Rep. 2020;5(5):618-26. DOI:10.1016/j.ekir.2020.01.018
35. Sethi S, Madden BJ, Debiec H, et al. Exostosin 1/Exostosin 2-Associated Membranous Nephropathy. J Am Soc Nephrol. 2019;30(6):1123-36. DOI:10.1681/ASN.2018080852
36. Debiec H, Hanoy M, Francois A, et al. Recurrent membranous nephropathy in an allograft caused by IgG3κ targeting the PLA2 receptor. J Am Soc Nephrol. 2012;23(12):1949-54. DOI:10.1681/ASN.2012060577
37. Vivarelli M, Emma F, Pellé T, et al. Genetic homogeneity but IgG subclass-dependent clinical variability of alloimmune membranous nephropathy with anti-neutral endopeptidase antibodies. Kidney Int. 2015;87(3):602-9. DOI:10.1038/ki.2014.381
38. Bally S, Debiec H, Ponard D, et al. Phospholipase A2 Receptor-Related Membranous Nephropathy and Mannan-Binding Lectin Deficiency. J Am Soc Nephrol. 2016;27(12):3539-44. DOI:10.1681/ASN.2015101155
39. Luo W, Olaru F, Miner JH, et al. Alternative Pathway Is Essential for Glomerular Complement Activation and Proteinuria in a Mouse Model of Membranous Nephropathy. Front Immunol. 2018;9:1433. DOI:10.3389/fimmu.2018.01433
40. Seikrit C, Ronco P, Debiec H. Factor H Autoantibodies and Membranous Nephropathy. N Engl J Med. 2018;379(25):2479-81. DOI:10.1056/NEJMc1805857
41. Valoti E, Noris M, Remuzzi G. More about Factor H Autoantibodies in Membranous Nephropathy. N Engl J Med. 2019;381(16):1590-2. DOI:10.1056/NEJMc1905608
42. Kawata N, Kang D, Aiuchi T, et al. Proteomics of human glomerulonephritis by laser microdissection and liquid chromatography-tandem mass spectrometry. Nephrology (Carlton). 2020;25(4):351-9. DOI:10.1111/nep.13676
2. Perkinson DT, Baker PJ, Couser WG, et al. Membrane attack complex deposition in experimental glomerular injury. Am J Pathol. 1985;120(1):121-8.
3. Couser WG, Johnson RJ, Young BA, et al. The effects of soluble recombinant complement receptor 1 on complement-mediated experimental glomerulonephritis. J Am Soc Nephrol. 1995;5(11):1888‑94. DOI:10.1681/ASN.V5111888
4. Petermann AT, Krofft R, Blonski M, et al. Podocytes that detach in experimental membranous nephropathy are viable. Kidney Int. 2003;64(4):1222-31.
DOI:10.1046/j.1523-1755.2003.00217.x
5. Kerjaschki D, Schulze M, Binder S, et al. Transcellular transport and membrane insertion of the C5b-9 membrane attack complex of complement by glomerular epithelial cells in experimental membranous nephropathy. J Immunol. 1989;143(2):546-52.
6. Takano T, Elimam H, Cybulsky AV. Complement-Mediated Cellular Injury. Semin Nephrol. 2013;33(6):586-601. DOI:10.1016/j.semnephrol.2013.08.009
7. Koopman JJE, van Essen MF, Rennke HG, et al. Deposition of the Membrane Attack Complex in Healthy and Diseased Human Kidneys. Front Immunol. 2021;11:599974. DOI:10.3389/fimmu.2020.599974
8. Ootaka T, Suzuki M, Sudo K, et al. Histologic localization of terminal complement complexes in renal diseases. An immunohistochemical study. Am J Clin Pathol. 1989;91(2):144-51. DOI:10.1093/ajcp/91.2.144
9. Lai KN, Lo ST, Lai FM. Immunohistochemical study of the membrane attack complex of complement and S-protein in idiopathic and secondary membranous nephropathy. Am J Pathol. 1989;135(3):469-76.
10. Papagianni AA, Alexopoulos E, Leontsini M, Papadimitriou M. C5b-9 and adhesion molecules in human idiopathic membranous nephropathy. Nephrol Dial Transplant. 2002;17(1):57-63. DOI:10.1093/ndt/17.1.57
11. Salant DJ, Belok S, Madaio MP, Couser WG. A new role for complement in experimental membranous nephropathy in rats. J Clin Invest. 1980;66(6):1339-50. DOI:10.1172/JCI109987
12. Baker PJ, Ochi RF, Schulze M, et al. Depletion of C6 prevents development of proteinuria in experimental membranous nephropathy in rats. Am J Pathol. 1989;135(1):185-94.
13. Schulze M, Donadio JV Jr, Pruchno CJ, et al. Elevated urinary excretion of the C5b-9 complex in membranous nephropathy. Kidney Int. 1991;40(3):533-8. DOI:10.1038/ki.1991.242
14. Montinaro V, Lopez A, Monno R, et al. Renal C3 synthesis in idiopathic membranous nephropathy: correlation to urinary C5b-9 excretion. Kidney Int. 2000;57(1):137-46. DOI:10.1046/j.1523-1755.2000.00812.x
15. Zhang MF, Huang J, Zhang YM, et al. Complement activation products in the circulation and urine of primary membranous nephropathy. BMC Nephrol. 2019;20(1):313. DOI:10.1186/s12882-019-1509-5
16. Kon SP, Coupes B, Short CD, et al. Urinary C5b-9 excretion and clinical course in idiopathic human membranous nephropathy. Kidney Int. 1995;48(6):1953-8. DOI:10.1038/ki.1995.496
17. Brenchley PE, Coupes B, Short CD, et al. Urinary C3dg and C5b-9 indicate active immune disease in human membranous nephropathy. Kidney Int. 1992;41(4):933-7. DOI:10.1038/ki.1992.143
18. Coupes BM, Kon SP, Brenchley PEC, et al. The temporal relationship between urinary C5b-9 and C3dg and clinical parameters in human membranous nephropathy. Nephrol Dial Transplant. 1993;8(5):397-401. DOI:10.1093/oxfordjournals.ndt.a092491
19. Leenaerts PL, Hall BM, Van Damme BJ, et al. Active Heymann nephritis in complement component C6 deficient rats. Kidney Int. 1995;47(6):1604-14. DOI:10.1038/ki.1995.224
20. Spicer ST, Tran GT, Killingsworth MC, et al. Induction of passive Heymann nephritis in complement component 6-deficient PVG rats. J Immunol. 2007;179(1):172-8. DOI:10.4049/jimmunol.179.1.172
21. Alsharhan L, Beck LH. Membranous Nephropathy: Core Curriculum 2021. Am J Kidney Dis. 2021;77(3):440-53. DOI:10.1053/j.ajkd.2020.10.009
22. Beck LH Jr, Bonegio RG, Lambeau G, et al. M-type phospholipase A2 receptor as target antigen in idiopathic membranous nephropathy. N Engl J Med. 2009;361(1):11-21. DOI:10.1056/NEJMoa0810457
23. Tomas NM, Beck LH Jr, Meyer-Schwesinger C, et al. Thrombospondin type-1 domain-containing 7A in idiopathic membranous nephropathy. N Engl J Med. 2014;371(24):2277-87. DOI:10.1056/NEJMoa1409354
24. Borza DB. Alternative Pathway Dysregulation and the Conundrum of Complement Activation by IgG4 Immune Complexes in Membranous Nephropathy. Front Immunol. 2016;7:157. DOI:10.3389/fimmu.2016.00157
25. Jennette JC, Hipp CG. Immunohistopathologic evaluation of C1q in 800 renal biopsy specimens. Am J Clin Pathol. 1985;83(4):415-20. DOI:10.1093/ajcp/83.4.415
26. Segawa Y, Hisano S, Matsushita M, et al. IgG subclasses and complement pathway in segmental and global membranous nephropathy. Pediatr Nephrol. 2010;25(6):1091-9. DOI:10.1007/s00467-009-1439-8
27. Yang Y, Wang C, Jin L, et al. IgG4 anti-phospholipase A2 receptor might activate lectin and alternative complement pathway meanwhile in idiopathic membranous nephropathy: an inspiration from a cross-sectional study. Immunol Res. 2016;64(4):919-30. DOI:10.1007/s12026-016-8790-1
28. Hayashi N, Okada K, Matsui Y, et al. G-32lomerular mannose-binding lectin deposition in intrinsic antigen-related membranous nephropathy. Nephrol Dial Transplant. 2018;33(5):832-40. DOI:10.1093/ndt/gfx235
29. Haddad G, Lorenzen JM, Ma H, et al. Altered glycosylation of IgG4 promotes lectin complement pathway activation in anti-PLA2R1-associated membranous nephropathy. J Clin Invest. 2021;131(5):e140453. DOI:10.1172/JCI140453
30. Huang CC, Lehman A, Albawardi A, et al. IgG subclass staining in renal biopsies with membranous glomerulonephritis indicates subclass switch during disease progression. Mod Pathol. 2013;26(6):799-805. DOI:10.1038/modpathol.2012.237
31. Zhang MF, Cui Z, Zhang YM, et al. Clinical and prognostic significance of glomerular C1q deposits in primary MN. Clin Chim Acta. 2018;485:152-7. DOI:10.1016/j.cca.2018.06.050
32. Wiech T, Stahl RAK, Hoxha E. Diagnostic role of renal biopsy in PLA2R1-antibody-positive patients with nephrotic syndrome. Mod Pathol. 2019;32(9):1320-8.
DOI:10.1038/s41379-019-0267-z
33. Larsen CP, Messias NC, Silva FG, et al. Determination of primary versus secondary membranous glomerulopathy utilizing phospholipase A2 receptor staining in renal biopsies. Mod Pathol. 2013;26(5):709-15. DOI:10.1038/modpathol.2012.207
34. Ravindran A, Madden B, Charlesworth MC, et al. Proteomic Analysis of Complement Proteins in Membranous Nephropathy. Kidney Int Rep. 2020;5(5):618-26. DOI:10.1016/j.ekir.2020.01.018
35. Sethi S, Madden BJ, Debiec H, et al. Exostosin 1/Exostosin 2-Associated Membranous Nephropathy. J Am Soc Nephrol. 2019;30(6):1123-36. DOI:10.1681/ASN.2018080852
36. Debiec H, Hanoy M, Francois A, et al. Recurrent membranous nephropathy in an allograft caused by IgG3κ targeting the PLA2 receptor. J Am Soc Nephrol. 2012;23(12):1949-54. DOI:10.1681/ASN.2012060577
37. Vivarelli M, Emma F, Pellé T, et al. Genetic homogeneity but IgG subclass-dependent clinical variability of alloimmune membranous nephropathy with anti-neutral endopeptidase antibodies. Kidney Int. 2015;87(3):602-9. DOI:10.1038/ki.2014.381
38. Bally S, Debiec H, Ponard D, et al. Phospholipase A2 Receptor-Related Membranous Nephropathy and Mannan-Binding Lectin Deficiency. J Am Soc Nephrol. 2016;27(12):3539-44. DOI:10.1681/ASN.2015101155
39. Luo W, Olaru F, Miner JH, et al. Alternative Pathway Is Essential for Glomerular Complement Activation and Proteinuria in a Mouse Model of Membranous Nephropathy. Front Immunol. 2018;9:1433. DOI:10.3389/fimmu.2018.01433
40. Seikrit C, Ronco P, Debiec H. Factor H Autoantibodies and Membranous Nephropathy. N Engl J Med. 2018;379(25):2479-81. DOI:10.1056/NEJMc1805857
41. Valoti E, Noris M, Remuzzi G. More about Factor H Autoantibodies in Membranous Nephropathy. N Engl J Med. 2019;381(16):1590-2. DOI:10.1056/NEJMc1905608
42. Kawata N, Kang D, Aiuchi T, et al. Proteomics of human glomerulonephritis by laser microdissection and liquid chromatography-tandem mass spectrometry. Nephrology (Carlton). 2020;25(4):351-9. DOI:10.1111/nep.13676
2. Perkinson DT, Baker PJ, Couser WG, et al. Membrane attack complex deposition in experimental glomerular injury. Am J Pathol. 1985;120(1):121-8.
3. Couser WG, Johnson RJ, Young BA, et al. The effects of soluble recombinant complement receptor 1 on complement-mediated experimental glomerulonephritis. J Am Soc Nephrol. 1995;5(11):1888‑94. DOI:10.1681/ASN.V5111888
4. Petermann AT, Krofft R, Blonski M, et al. Podocytes that detach in experimental membranous nephropathy are viable. Kidney Int. 2003;64(4):1222-31.
DOI:10.1046/j.1523-1755.2003.00217.x
5. Kerjaschki D, Schulze M, Binder S, et al. Transcellular transport and membrane insertion of the C5b-9 membrane attack complex of complement by glomerular epithelial cells in experimental membranous nephropathy. J Immunol. 1989;143(2):546-52.
6. Takano T, Elimam H, Cybulsky AV. Complement-Mediated Cellular Injury. Semin Nephrol. 2013;33(6):586-601. DOI:10.1016/j.semnephrol.2013.08.009
7. Koopman JJE, van Essen MF, Rennke HG, et al. Deposition of the Membrane Attack Complex in Healthy and Diseased Human Kidneys. Front Immunol. 2021;11:599974. DOI:10.3389/fimmu.2020.599974
8. Ootaka T, Suzuki M, Sudo K, et al. Histologic localization of terminal complement complexes in renal diseases. An immunohistochemical study. Am J Clin Pathol. 1989;91(2):144-51. DOI:10.1093/ajcp/91.2.144
9. Lai KN, Lo ST, Lai FM. Immunohistochemical study of the membrane attack complex of complement and S-protein in idiopathic and secondary membranous nephropathy. Am J Pathol. 1989;135(3):469-76.
10. Papagianni AA, Alexopoulos E, Leontsini M, Papadimitriou M. C5b-9 and adhesion molecules in human idiopathic membranous nephropathy. Nephrol Dial Transplant. 2002;17(1):57-63. DOI:10.1093/ndt/17.1.57
11. Salant DJ, Belok S, Madaio MP, Couser WG. A new role for complement in experimental membranous nephropathy in rats. J Clin Invest. 1980;66(6):1339-50. DOI:10.1172/JCI109987
12. Baker PJ, Ochi RF, Schulze M, et al. Depletion of C6 prevents development of proteinuria in experimental membranous nephropathy in rats. Am J Pathol. 1989;135(1):185-94.
13. Schulze M, Donadio JV Jr, Pruchno CJ, et al. Elevated urinary excretion of the C5b-9 complex in membranous nephropathy. Kidney Int. 1991;40(3):533-8. DOI:10.1038/ki.1991.242
14. Montinaro V, Lopez A, Monno R, et al. Renal C3 synthesis in idiopathic membranous nephropathy: correlation to urinary C5b-9 excretion. Kidney Int. 2000;57(1):137-46. DOI:10.1046/j.1523-1755.2000.00812.x
15. Zhang MF, Huang J, Zhang YM, et al. Complement activation products in the circulation and urine of primary membranous nephropathy. BMC Nephrol. 2019;20(1):313. DOI:10.1186/s12882-019-1509-5
16. Kon SP, Coupes B, Short CD, et al. Urinary C5b-9 excretion and clinical course in idiopathic human membranous nephropathy. Kidney Int. 1995;48(6):1953-8. DOI:10.1038/ki.1995.496
17. Brenchley PE, Coupes B, Short CD, et al. Urinary C3dg and C5b-9 indicate active immune disease in human membranous nephropathy. Kidney Int. 1992;41(4):933-7. DOI:10.1038/ki.1992.143
18. Coupes BM, Kon SP, Brenchley PEC, et al. The temporal relationship between urinary C5b-9 and C3dg and clinical parameters in human membranous nephropathy. Nephrol Dial Transplant. 1993;8(5):397-401. DOI:10.1093/oxfordjournals.ndt.a092491
19. Leenaerts PL, Hall BM, Van Damme BJ, et al. Active Heymann nephritis in complement component C6 deficient rats. Kidney Int. 1995;47(6):1604-14. DOI:10.1038/ki.1995.224
20. Spicer ST, Tran GT, Killingsworth MC, et al. Induction of passive Heymann nephritis in complement component 6-deficient PVG rats. J Immunol. 2007;179(1):172-8. DOI:10.4049/jimmunol.179.1.172
21. Alsharhan L, Beck LH. Membranous Nephropathy: Core Curriculum 2021. Am J Kidney Dis. 2021;77(3):440-53. DOI:10.1053/j.ajkd.2020.10.009
22. Beck LH Jr, Bonegio RG, Lambeau G, et al. M-type phospholipase A2 receptor as target antigen in idiopathic membranous nephropathy. N Engl J Med. 2009;361(1):11-21. DOI:10.1056/NEJMoa0810457
23. Tomas NM, Beck LH Jr, Meyer-Schwesinger C, et al. Thrombospondin type-1 domain-containing 7A in idiopathic membranous nephropathy. N Engl J Med. 2014;371(24):2277-87. DOI:10.1056/NEJMoa1409354
24. Borza DB. Alternative Pathway Dysregulation and the Conundrum of Complement Activation by IgG4 Immune Complexes in Membranous Nephropathy. Front Immunol. 2016;7:157. DOI:10.3389/fimmu.2016.00157
25. Jennette JC, Hipp CG. Immunohistopathologic evaluation of C1q in 800 renal biopsy specimens. Am J Clin Pathol. 1985;83(4):415-20. DOI:10.1093/ajcp/83.4.415
26. Segawa Y, Hisano S, Matsushita M, et al. IgG subclasses and complement pathway in segmental and global membranous nephropathy. Pediatr Nephrol. 2010;25(6):1091-9. DOI:10.1007/s00467-009-1439-8
27. Yang Y, Wang C, Jin L, et al. IgG4 anti-phospholipase A2 receptor might activate lectin and alternative complement pathway meanwhile in idiopathic membranous nephropathy: an inspiration from a cross-sectional study. Immunol Res. 2016;64(4):919-30. DOI:10.1007/s12026-016-8790-1
28. Hayashi N, Okada K, Matsui Y, et al. G-32lomerular mannose-binding lectin deposition in intrinsic antigen-related membranous nephropathy. Nephrol Dial Transplant. 2018;33(5):832-40. DOI:10.1093/ndt/gfx235
29. Haddad G, Lorenzen JM, Ma H, et al. Altered glycosylation of IgG4 promotes lectin complement pathway activation in anti-PLA2R1-associated membranous nephropathy. J Clin Invest. 2021;131(5):e140453. DOI:10.1172/JCI140453
30. Huang CC, Lehman A, Albawardi A, et al. IgG subclass staining in renal biopsies with membranous glomerulonephritis indicates subclass switch during disease progression. Mod Pathol. 2013;26(6):799-805. DOI:10.1038/modpathol.2012.237
31. Zhang MF, Cui Z, Zhang YM, et al. Clinical and prognostic significance of glomerular C1q deposits in primary MN. Clin Chim Acta. 2018;485:152-7. DOI:10.1016/j.cca.2018.06.050
32. Wiech T, Stahl RAK, Hoxha E. Diagnostic role of renal biopsy in PLA2R1-antibody-positive patients with nephrotic syndrome. Mod Pathol. 2019;32(9):1320-8.
DOI:10.1038/s41379-019-0267-z
33. Larsen CP, Messias NC, Silva FG, et al. Determination of primary versus secondary membranous glomerulopathy utilizing phospholipase A2 receptor staining in renal biopsies. Mod Pathol. 2013;26(5):709-15. DOI:10.1038/modpathol.2012.207
34. Ravindran A, Madden B, Charlesworth MC, et al. Proteomic Analysis of Complement Proteins in Membranous Nephropathy. Kidney Int Rep. 2020;5(5):618-26. DOI:10.1016/j.ekir.2020.01.018
35. Sethi S, Madden BJ, Debiec H, et al. Exostosin 1/Exostosin 2-Associated Membranous Nephropathy. J Am Soc Nephrol. 2019;30(6):1123-36. DOI:10.1681/ASN.2018080852
36. Debiec H, Hanoy M, Francois A, et al. Recurrent membranous nephropathy in an allograft caused by IgG3κ targeting the PLA2 receptor. J Am Soc Nephrol. 2012;23(12):1949-54. DOI:10.1681/ASN.2012060577
37. Vivarelli M, Emma F, Pellé T, et al. Genetic homogeneity but IgG subclass-dependent clinical variability of alloimmune membranous nephropathy with anti-neutral endopeptidase antibodies. Kidney Int. 2015;87(3):602-9. DOI:10.1038/ki.2014.381
38. Bally S, Debiec H, Ponard D, et al. Phospholipase A2 Receptor-Related Membranous Nephropathy and Mannan-Binding Lectin Deficiency. J Am Soc Nephrol. 2016;27(12):3539-44. DOI:10.1681/ASN.2015101155
39. Luo W, Olaru F, Miner JH, et al. Alternative Pathway Is Essential for Glomerular Complement Activation and Proteinuria in a Mouse Model of Membranous Nephropathy. Front Immunol. 2018;9:1433. DOI:10.3389/fimmu.2018.01433
40. Seikrit C, Ronco P, Debiec H. Factor H Autoantibodies and Membranous Nephropathy. N Engl J Med. 2018;379(25):2479-81. DOI:10.1056/NEJMc1805857
41. Valoti E, Noris M, Remuzzi G. More about Factor H Autoantibodies in Membranous Nephropathy. N Engl J Med. 2019;381(16):1590-2. DOI:10.1056/NEJMc1905608
42. Kawata N, Kang D, Aiuchi T, et al. Proteomics of human glomerulonephritis by laser microdissection and liquid chromatography-tandem mass spectrometry. Nephrology (Carlton). 2020;25(4):351-9. DOI:10.1111/nep.13676
________________________________________________
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13. Schulze M, Donadio JV Jr, Pruchno CJ, et al. Elevated urinary excretion of the C5b-9 complex in membranous nephropathy. Kidney Int. 1991;40(3):533-8. DOI:10.1038/ki.1991.242
14. Montinaro V, Lopez A, Monno R, et al. Renal C3 synthesis in idiopathic membranous nephropathy: correlation to urinary C5b-9 excretion. Kidney Int. 2000;57(1):137-46. DOI:10.1046/j.1523-1755.2000.00812.x
15. Zhang MF, Huang J, Zhang YM, et al. Complement activation products in the circulation and urine of primary membranous nephropathy. BMC Nephrol. 2019;20(1):313. DOI:10.1186/s12882-019-1509-5
16. Kon SP, Coupes B, Short CD, et al. Urinary C5b-9 excretion and clinical course in idiopathic human membranous nephropathy. Kidney Int. 1995;48(6):1953-8. DOI:10.1038/ki.1995.496
17. Brenchley PE, Coupes B, Short CD, et al. Urinary C3dg and C5b-9 indicate active immune disease in human membranous nephropathy. Kidney Int. 1992;41(4):933-7. DOI:10.1038/ki.1992.143
18. Coupes BM, Kon SP, Brenchley PEC, et al. The temporal relationship between urinary C5b-9 and C3dg and clinical parameters in human membranous nephropathy. Nephrol Dial Transplant. 1993;8(5):397-401. DOI:10.1093/oxfordjournals.ndt.a092491
19. Leenaerts PL, Hall BM, Van Damme BJ, et al. Active Heymann nephritis in complement component C6 deficient rats. Kidney Int. 1995;47(6):1604-14. DOI:10.1038/ki.1995.224
20. Spicer ST, Tran GT, Killingsworth MC, et al. Induction of passive Heymann nephritis in complement component 6-deficient PVG rats. J Immunol. 2007;179(1):172-8. DOI:10.4049/jimmunol.179.1.172
21. Alsharhan L, Beck LH. Membranous Nephropathy: Core Curriculum 2021. Am J Kidney Dis. 2021;77(3):440-53. DOI:10.1053/j.ajkd.2020.10.009
22. Beck LH Jr, Bonegio RG, Lambeau G, et al. M-type phospholipase A2 receptor as target antigen in idiopathic membranous nephropathy. N Engl J Med. 2009;361(1):11-21. DOI:10.1056/NEJMoa0810457
23. Tomas NM, Beck LH Jr, Meyer-Schwesinger C, et al. Thrombospondin type-1 domain-containing 7A in idiopathic membranous nephropathy. N Engl J Med. 2014;371(24):2277-87. DOI:10.1056/NEJMoa1409354
24. Borza DB. Alternative Pathway Dysregulation and the Conundrum of Complement Activation by IgG4 Immune Complexes in Membranous Nephropathy. Front Immunol. 2016;7:157. DOI:10.3389/fimmu.2016.00157
25. Jennette JC, Hipp CG. Immunohistopathologic evaluation of C1q in 800 renal biopsy specimens. Am J Clin Pathol. 1985;83(4):415-20. DOI:10.1093/ajcp/83.4.415
26. Segawa Y, Hisano S, Matsushita M, et al. IgG subclasses and complement pathway in segmental and global membranous nephropathy. Pediatr Nephrol. 2010;25(6):1091-9. DOI:10.1007/s00467-009-1439-8
27. Yang Y, Wang C, Jin L, et al. IgG4 anti-phospholipase A2 receptor might activate lectin and alternative complement pathway meanwhile in idiopathic membranous nephropathy: an inspiration from a cross-sectional study. Immunol Res. 2016;64(4):919-30. DOI:10.1007/s12026-016-8790-1
28. Hayashi N, Okada K, Matsui Y, et al. G-32lomerular mannose-binding lectin deposition in intrinsic antigen-related membranous nephropathy. Nephrol Dial Transplant. 2018;33(5):832-40. DOI:10.1093/ndt/gfx235
29. Haddad G, Lorenzen JM, Ma H, et al. Altered glycosylation of IgG4 promotes lectin complement pathway activation in anti-PLA2R1-associated membranous nephropathy. J Clin Invest. 2021;131(5):e140453. DOI:10.1172/JCI140453
30. Huang CC, Lehman A, Albawardi A, et al. IgG subclass staining in renal biopsies with membranous glomerulonephritis indicates subclass switch during disease progression. Mod Pathol. 2013;26(6):799-805. DOI:10.1038/modpathol.2012.237
31. Zhang MF, Cui Z, Zhang YM, et al. Clinical and prognostic significance of glomerular C1q deposits in primary MN. Clin Chim Acta. 2018;485:152-7. DOI:10.1016/j.cca.2018.06.050
32. Wiech T, Stahl RAK, Hoxha E. Diagnostic role of renal biopsy in PLA2R1-antibody-positive patients with nephrotic syndrome. Mod Pathol. 2019;32(9):1320-8.
DOI:10.1038/s41379-019-0267-z
33. Larsen CP, Messias NC, Silva FG, et al. Determination of primary versus secondary membranous glomerulopathy utilizing phospholipase A2 receptor staining in renal biopsies. Mod Pathol. 2013;26(5):709-15. DOI:10.1038/modpathol.2012.207
34. Ravindran A, Madden B, Charlesworth MC, et al. Proteomic Analysis of Complement Proteins in Membranous Nephropathy. Kidney Int Rep. 2020;5(5):618-26. DOI:10.1016/j.ekir.2020.01.018
35. Sethi S, Madden BJ, Debiec H, et al. Exostosin 1/Exostosin 2-Associated Membranous Nephropathy. J Am Soc Nephrol. 2019;30(6):1123-36. DOI:10.1681/ASN.2018080852
36. Debiec H, Hanoy M, Francois A, et al. Recurrent membranous nephropathy in an allograft caused by IgG3κ targeting the PLA2 receptor. J Am Soc Nephrol. 2012;23(12):1949-54. DOI:10.1681/ASN.2012060577
37. Vivarelli M, Emma F, Pellé T, et al. Genetic homogeneity but IgG subclass-dependent clinical variability of alloimmune membranous nephropathy with anti-neutral endopeptidase antibodies. Kidney Int. 2015;87(3):602-9. DOI:10.1038/ki.2014.381
38. Bally S, Debiec H, Ponard D, et al. Phospholipase A2 Receptor-Related Membranous Nephropathy and Mannan-Binding Lectin Deficiency. J Am Soc Nephrol. 2016;27(12):3539-44. DOI:10.1681/ASN.2015101155
39. Luo W, Olaru F, Miner JH, et al. Alternative Pathway Is Essential for Glomerular Complement Activation and Proteinuria in a Mouse Model of Membranous Nephropathy. Front Immunol. 2018;9:1433. DOI:10.3389/fimmu.2018.01433
40. Seikrit C, Ronco P, Debiec H. Factor H Autoantibodies and Membranous Nephropathy. N Engl J Med. 2018;379(25):2479-81. DOI:10.1056/NEJMc1805857
41. Valoti E, Noris M, Remuzzi G. More about Factor H Autoantibodies in Membranous Nephropathy. N Engl J Med. 2019;381(16):1590-2. DOI:10.1056/NEJMc1905608
42. Kawata N, Kang D, Aiuchi T, et al. Proteomics of human glomerulonephritis by laser microdissection and liquid chromatography-tandem mass spectrometry. Nephrology (Carlton). 2020;25(4):351-9. DOI:10.1111/nep.13676
Авторы
Е.С. Камышова*, Т.А. Семерюк, И.Н. Бобкова
ФГАОУ ВО «Первый Московский государственный медицинский университет им. И.М. Сеченова» Минздрава России (Сеченовский Университет), Москва, Россия
*kamyshova_e_s@staff.sechenov.ru
Sechenov First Moscow State Medical University (Sechenov University), Moscow, Russia
*kamyshova_e_s@staff.sechenov.ru
ФГАОУ ВО «Первый Московский государственный медицинский университет им. И.М. Сеченова» Минздрава России (Сеченовский Университет), Москва, Россия
*kamyshova_e_s@staff.sechenov.ru
________________________________________________
Sechenov First Moscow State Medical University (Sechenov University), Moscow, Russia
*kamyshova_e_s@staff.sechenov.ru
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