Роль MALT-системы кишечника в патогенезе IgA-нефропатии
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Guliaev SV, Strizhakov LA, Chebotareva NV, Moiseev SV. Role of the intestinal MALT in pathogenesis of the IgA-nephropathy. Terapevticheskii Arkhiv (Ter. Arkh.). 2021; 93 (6): 724–728. DOI: 10.26442/00403660.2021.06.200868
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Ключевые слова: иммуноглобулин A-нефропатия, иммуноглобулин A, дефектное гликозилирование иммуноглобулина A, кишечная проницаемость, MALT
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Modern view on pathogenesis of immunoglobulin (Ig)A-nephropathy and possible relation to intestinal MALT-system activity is presented in the article. Aberrant glycosylation of IgA and increased association of IgA-nephropathy with intestinal diseases or abnormal intestinal permeability are discussed in details. Based on supposed entero-renal pathogenesis of the disease future treatment modalities are considered. Relevant world’s literature is cited.
Keywords: immunoglobulin A-nephropathy, immunoglobulin A, аberrant glycosylation of immunoglobulin A, intestinal permeability, MALT
2. Добронравов В.А., Мужецкая Т.О., Лин Д.И., Кочоян З.Ш. Иммуноглобулин А-нефропатия в российской популяции: клинико-морфологическая презентация и отдаленный прогноз. Нефрология (Санкт-Петербург). 2019;23(6):45-60 [Dobronravov VA, Muzhetskaya TO, Lin DI, Kochoyan ZS. Immunoglobulin A-nephropathy in Russian population: clinical and morphological presentation and long-term prognosis. Nephrology (Saint-Petersburg). 2019;23(6):45-60 (in Russian)]. DOI:10.36485/1561-6274-2019-236-45-60
3. Zhang C, Zeng X, Li Z, et al. Immunoglobulin A nephropathy: current progress and future directions. Transl Res. 2015;166(2):134-44. DOI:10.1016/j.trsl.2015.02.007
4. Floege J, Feehally J. The mucosa-kidney axis in IgA nephropathy. Nat Rev Nephrol. 2016;12(3):147-56. DOI:10.1038/nrneph.2015.208
5. Novak J, Moldoveanu Z, Renfrow M, et al. IgA nephropathy and Henoch–Schoenlein purpura nephritis: aberrant glycosylation of IgA1, formation of IgA1-containing immune complexes, and activation of mesangial cells. Contrib Nephrol. 2007;157:134-8. DOI:10.1159/000102455
6. Гуляев С.В., Стрижаков Л.А., Моисеев С.В., Фомин В.В. От пурпуры Шенлейна–Геноха до IgА-васкулита: патогенетические аспекты болезни. Терапевтический архив. 2018;90(10):109-14 [Guliaev SV, Srizhakov LA, Moiseev SV, Fomin VV. From Schönlein–Henoch purpura to IgA-vasculitis: pathogenetic aspects of the disease. Terapevticheskii Arkhiv (Ter. Arkh.). 2018;90(10):109-14 (in Russian)]. DOI:10.26442/terarkh20189010109-114
7. Климович В.Б., Самойлович М.П. Иммуноглобулин А (IgA) и его рецепторы. Мед. иммунология. 2006;8(4):483-500 [Klimovich VB, Samoilovich MP. Immunoglobulin A (IgA) and its receptors. Medical Immunology. 2006;8(4):483-500 (in Russian)].DOI:10.15789/1563-0625-2006-4-483-500
8. Novak J, Julian BA, Tomana M, et al. IgA glycosylation and IgA immune complexes in the pathogenesis of IgA Nephropathy. Semin Nephrol. 2008; 28(1):78-87. DOI:10.1016/j.semnephrol.2007.10.009
9. Suzuki H, Fan R, Zhang Z, et al. Aberrantly glycosylated IgA1 in IgA nephropathy patients is recognized by IgG antibodies with restricted heterogeneity. J Clin Invest. 2009;119:1668-77. DOI:10.1172/JCI38468
10. Launay P, Grossetete B, Arcos-Fajardo M, et al. Fcα receptor (CD89) mediates the development of immunoglobulin A (IgA) nephropathy (Berger's disease). Evidence for pathogenic soluble receptor-IgA complexes in patients and CD89 transgenic mice. J Exp Med. 2000;191:1999-2009. DOI:10.1084/jem.191.11.1999
11. Van Der Helm-Van Mil AH, Smith AC, Pouria S, et al. Immunoglobulin A multiple myeloma presenting with Henoch–Schönlein purpura associated with reduced sialylation of IgA1. Br J Haematol. 2003;122(6):915-7. DOI:10.1046/j.1365-2141.2003.04539.x
12. Zhao N, Hou P, Lv J, et al. The level of galactose-deficient IgA1 in the sera of patients with IgA nephropathy is associated with disease progression. Kidney Int. 2012;82(7):790-6. DOI:10.1038/ki.2012.197
13. Smith AC, Molyneux K, Feehally J, Barratt J. O-glycosylation of serum IgA1 antibodies against mucosal and systemic antigens in IgA nephropathy. J Am Soc Nephrol. 2006;17(12):3520-8. DOI:10.1681/ASN.2006060658
14. McCarthy DD, Kujawa J, Wilson C, et al. Mice overexpressing BAFF develop a commensal flora-dependent, IgA-associated nephropathy. J Clin Investig. 2011;121(10):3991-4002. DOI:10.1172/JCI45563
15. Dong R, Bai M, Zhao J, et al. A Comparative Study of the Gut Microbiota Associated With Immunoglobulin А Nephropathy and Membranous Nephropathy. Front Cell Infect Microbiol. 2020;10:557368. DOI:10.3389/fcimb.2020.557368
16. Blaas SH, Stieber-Gunckel M, Falk W, et al. CpG-oligodeoxynucleotidesstimulate immunoglobulin A secretion in intestinal mucosal B cells. Clin Exp Immunol. 2009;155:534-40. DOI:10.1111/j.1365-2249.2008.03855.x
17. Zheng N, Fan J, Wang B, et al. Expression profile of BAFF in peripheral blood from patients of IgA nephropathy: Correlation with clinical features and Streptococcus pyogenes infection. Mol Med Rep. 2017;15(4):1925-35. DOI:10.3892/mmr.2017.6190
18. Zhai YL, Zhu L, Shi SF, et al. Increased APRIL Expression Induces IgA1 Aberrant Glycosylation in IgA Nephropathy. Medicine (Baltimore). 2016;95(11):e3099. DOI:10.1097/MD.0000000000003099
19. Davin JC, Forget P, Mahieu PR. Increased intestinal permeability to (51 Cr) EDTA is correlated with IgA immune complex-plasma levels in children with IgA-associated nephropathies. Acta Paediatr Scand. 1988;77(1):118-24. DOI: 10.1111/j.1651-2227.1988.tb10609.x
20. Davin JC, Mahieu PR. Sequential measurements of intestinal permeability to [51Cr] EDTA in children with Henoch-Schönlein purpura nephritis. Nephron. 1992;60(4):498-9. DOI: 10.1159/000186821
21. Мухин Н.А., Гуляев С.В., Кривошеев О.Г., и др. Клиническое и прогностическое значение поражения желудочно-кишечного тракта при системных сосудистых пурпурах. Терапевтический архив. 2003;75(2):50-4 [Mukhin NA, Gulyaev SV, Krivosheev ОG, et al. Clinical and prognostic implications of gastrointestinal tract lesions in systemic vascular purpuras. Terapevticheskii Arkhiv (Ter. Arkh.). 2003;75(2):50-4 (in Russian)]
22. Ambruzs JM, Walker PD, Larsen CP. The histopathologic spectrum of kidney biopsies in patients with inflammatory bowel disease. Clin J Am Soc Nephrol. 2014;9(2):265-70. DOI:10.2215/CJN.04660513
23. Elaziz MMA, Fayed A. Patterns of renal involvement in a cohort of patients with inflammatory bowel disease in Egypt. Acta Gastroenterol Belg. 2018;81(3):381-5
24. Pohjonen J, Nurmi R, Metso M, et al. Inflammatory bowel disease in patients undergoing renal biopsies. Clin Kidney J. 2019;12(5):645-51. DOI:10.1093/ckj/sfz004
25. Bjarnason I, Peters T, Veall N. A persistent defect in intestinal permeability in celiac disease demonstrated by a 51Cr-labelled EDTA absorption test. Lancet. 1983;321:323-5.
DOI:10.1016/S0140-6736(83)91628-8
26. Griffiths CE, Menzies IS, Barrison IG, et al. Intestinal permeability in dermatitis herpetiformis. Invest Dermatol. 1988;91(2):147-9. DOI:10.1111/1523-1747.ep12464390
27. Nagy J, Scott H, Brandtzaeg P. Antibodies to dietary antigens in IgA nephropathy. Clin Nephrol. 1988;29(6):275-9
28. Smerud HK, Fellström B, Hällgren R, et al. Gluten sensitivity in patients with IgA nephropathy. Nephrol Dial Transplant. 2009;24:2476-81. DOI:10.1093/ndt/gfp133
29. Coppo R, Roccatello D, Amore A, et al. Effects of a gluten-free diet in primary IgA nephropathy. Clin Nephrol. 1990;33:72-86
30. Collin P, Salmi TT, Hervonen K, et al. Dermatitis herpetiformis: a cutaneous manifestation of coeliac disease. Ann Med. 2017;49(1):23-31. DOI:10.1080/07853890.2016.1222450
31. Coppo R. The intestine-renal connection in IgA nephropathy. Nephrol Dial Transplant. 2015;30(3):360-6. DOI:10.1093/ndt/gfu343
32. Pasternack A, Collin P, Mustonen J, et al. Glomerular IgA deposits in patients with celiac disease. Clin Nephrol. 1990;34(2):56-60.
33. Tissandié E, Morelle W, Berthelot L, et al. Both IgA nephropathy and alcoholic cirrhosis feature abnormally glycosylated IgA1 and soluble CD89-IgA and IgG-IgA complexes: common mechanisms for distinct diseases. Kidney Int. 2011;80(12):1352-63. DOI:10.1038/ki.2011.276
34. van de Wiel A, Valentijn RM, Schuurman HJ, et al. Circulating IgA immune complexes and skin IgA deposits in liver disease. Relation to liver histopathology. Dig Dis Sci. 1988;33(6):679-84. DOI:10.1007/BF01540430
35. Mutlu EA, Gillevet PM, Rangwala H, et al. Colonic microbiome is altered in alcoholism. Am J Physiol Gastrointest Liver Physiol. 2012;302(9):G966-78. DOI:10.1152/ajpgi.00380.2011
36. Rao RK, Seth A, Sheth P. Recent advances in alcoholic liver disease: I. Role of intestinal permeability and endotoxemia in alcoholic liver disease. Am J Physiol Gastrointest Liver Physiol. 2004;286(6):G881-4. DOI:10.1152/ajpgi.00006.2004
37. Parlesak A, Schäfer C, Schütz T, et al. Increased intestinal permeability to macromolecules and endotoxemia in patients with chronic alcohol abuse in different stages of alcohol-induced liver disease. J Hepatol. 2000;32(5):742-7. DOI:10.1016/s0168-8278(00)80242-1
38. Chemouny JM, Gleeson PJ, Abbad L, et al. Modulation of the microbiota by oral antibiotics treats immunoglobulin A nephropathy in humanized mice. Nephrol Dial Transplant. 2019;34(7):1135-44. DOI:1093/ndt/gfy323
39. Soylu A, Berktaş S, Sarioğlu S, Erbil G. Saccharomyces boulardii prevents oral-poliovirus vaccine-induced IgA nephropathy in mice. Pediatr Nephrol. 2008;23(8):1287-91. DOI:10.1007/s00467-008-0813-2
40. Fellström BC, Barratt J, Cook H, Coppo R. Targeted-release budesonide versus placebo in patients with IgA nephropathy (NEFIGAN):
a double-blind, randomised, placebo-controlled phase 2b trial. Lancet.
2017;389(10084):2117-27. DOI:10.1016/S0140-6736(17)30550-0
41. Lafayette RA, Canetta PA, Rovin BH. A Randomized, Controlled Trial of Rituximab in IgA Nephropathy with Proteinuria and Renal Dysfunction. J Am Soc Nephrol. 2017;28(4):1306-13. DOI:10.1681/ASN.2016060640
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1. Berger J, Hinglais N. Les dépôts intercapillaires d'IgA-IgG. J Urol Nephrol. 1968;74:694-95
2. Dobronravov VA, Muzhetskaya TO, Lin DI, Kochoyan ZS. Immunoglobulin A-nephropathy in Russian population: clinical and morphological presentation and long-term prognosis. Nephrology (Saint-Petersburg). 2019;23(6):45-60 (in Russian)
DOI:10.36485/1561-6274-2019-236-45-60
3. Zhang C, Zeng X, Li Z, et al. Immunoglobulin A nephropathy: current progress and future directions. Transl Res. 2015;166(2):134-44. DOI:10.1016/j.trsl.2015.02.007
4. Floege J, Feehally J. The mucosa-kidney axis in IgA nephropathy. Nat Rev Nephrol. 2016;12(3):147-56. DOI:10.1038/nrneph.2015.208
5. Novak J, Moldoveanu Z, Renfrow M, et al. IgA nephropathy and Henoch–Schoenlein purpura nephritis: aberrant glycosylation of IgA1, formation of IgA1-containing immune complexes, and activation of mesangial cells. Contrib Nephrol. 2007;157:134-8. DOI:10.1159/000102455
6. Guliaev SV, Srizhakov LA, Moiseev SV, Fomin VV. From Schönlein–Henoch purpura to IgA-vasculitis: pathogenetic aspects of the disease. Terapevticheskii Arkhiv (Ter. Arkh.). 2018;90(10):109-14 (in Russian) DOI:10.26442/terarkh20189010109-114
7. Klimovich VB, Samoilovich MP. Immunoglobulin A (IgA) and its receptors. Medical Immunology. 2006;8(4):483-500 (in Russian) DOI:10.15789/1563-0625-2006-4-483-500
8. Novak J, Julian BA, Tomana M, et al. IgA glycosylation and IgA immune complexes in the pathogenesis of IgA Nephropathy. Semin Nephrol. 2008; 28(1):78-87. DOI:10.1016/j.semnephrol.2007.10.009
9. Suzuki H, Fan R, Zhang Z, et al. Aberrantly glycosylated IgA1 in IgA nephropathy patients is recognized by IgG antibodies with restricted heterogeneity. J Clin Invest. 2009;119:1668-77. DOI:10.1172/JCI38468
10. Launay P, Grossetete B, Arcos-Fajardo M, et al. Fcα receptor (CD89) mediates the development of immunoglobulin A (IgA) nephropathy (Berger's disease). Evidence for pathogenic soluble receptor-IgA complexes in patients and CD89 transgenic mice. J Exp Med. 2000;191:1999-2009. DOI:10.1084/jem.191.11.1999
11. Van Der Helm-Van Mil AH, Smith AC, Pouria S, et al. Immunoglobulin A multiple myeloma presenting with Henoch–Schönlein purpura associated with reduced sialylation of IgA1. Br J Haematol. 2003;122(6):915-7. DOI:10.1046/j.1365-2141.2003.04539.x
12. Zhao N, Hou P, Lv J, et al. The level of galactose-deficient IgA1 in the sera of patients with IgA nephropathy is associated with disease progression. Kidney Int. 2012;82(7):790-6. DOI:10.1038/ki.2012.197
13. Smith AC, Molyneux K, Feehally J, Barratt J. O-glycosylation of serum IgA1 antibodies against mucosal and systemic antigens in IgA nephropathy. J Am Soc Nephrol. 2006;17(12):3520-8. DOI:10.1681/ASN.2006060658
14. McCarthy DD, Kujawa J, Wilson C, et al. Mice overexpressing BAFF develop a commensal flora-dependent, IgA-associated nephropathy.
J Clin Investig. 2011;121(10):3991-4002. DOI:10.1172/JCI45563
15. Dong R, Bai M, Zhao J, et al. A Comparative Study of the Gut Microbiota Associated With Immunoglobulin А Nephropathy and Membranous Nephropathy. Front Cell Infect Microbiol. 2020;10:557368. DOI:10.3389/fcimb.2020.557368
16. Blaas SH, Stieber-Gunckel M, Falk W, et al. CpG-oligodeoxynucleotidesstimulate immunoglobulin A secretion in intestinal mucosal B cells. Clin Exp Immunol. 2009;155:534-40. DOI:10.1111/j.1365-2249.2008.03855.x
17. Zheng N, Fan J, Wang B, et al. Expression profile of BAFF in peripheral blood from patients of IgA nephropathy: Correlation with clinical features and Streptococcus pyogenes infection. Mol Med Rep. 2017;15(4):1925-35. DOI:10.3892/mmr.2017.6190
18. Zhai YL, Zhu L, Shi SF, et al. Increased APRIL Expression Induces IgA1 Aberrant Glycosylation in IgA Nephropathy. Medicine (Baltimore). 2016;95(11):e3099. DOI:10.1097/MD.0000000000003099
19. Davin JC, Forget P, Mahieu PR. Increased intestinal permeability to (51 Cr) EDTA is correlated with IgA immune complex-plasma levels in children with IgA-associated nephropathies. Acta Paediatr Scand. 1988;77(1):118-24. DOI: 10.1111/j.1651-2227.1988.tb10609.x
20. Davin JC, Mahieu PR. Sequential measurements of intestinal permeability to [51Cr] EDTA in children with Henoch-Schönlein purpura nephritis. Nephron. 1992;60(4):498-9. DOI: 10.1159/000186821
21. Mukhin NA, Gulyaev SV, Krivosheev ОG, et al. Clinical and prognostic implications of gastrointestinal tract lesions in systemic vascular purpuras. Terapevticheskii Arkhiv (Ter. Arkh.). 2003;75(2):50-4 (in Russian)
22. Ambruzs JM, Walker PD, Larsen CP. The histopathologic spectrum of kidney biopsies in patients with inflammatory bowel disease. Clin J Am Soc Nephrol. 2014;9(2):265-70. DOI:10.2215/CJN.04660513
23. Elaziz MMA, Fayed A. Patterns of renal involvement in a cohort of patients with inflammatory bowel disease in Egypt. Acta Gastroenterol Belg. 2018;81(3):381-5
24. Pohjonen J, Nurmi R, Metso M, et al. Inflammatory bowel disease in patients undergoing renal biopsies. Clin Kidney J. 2019;12(5):645-51. DOI:10.1093/ckj/sfz004
25. Bjarnason I, Peters T, Veall N. A persistent defect in intestinal permeability in celiac disease demonstrated by a 51Cr-labelled EDTA absorption test. Lancet. 1983;321:323-5.
DOI:10.1016/S0140-6736(83)91628-8
26. Griffiths CE, Menzies IS, Barrison IG, et al. Intestinal permeability in dermatitis herpetiformis. Invest Dermatol. 1988;91(2):147-9. DOI:10.1111/1523-1747.ep12464390
27. Nagy J, Scott H, Brandtzaeg P. Antibodies to dietary antigens in IgA nephropathy. Clin Nephrol. 1988;29(6):275-9
28. Smerud HK, Fellström B, Hällgren R, et al. Gluten sensitivity in patients with IgA nephropathy. Nephrol Dial Transplant. 2009;24:2476-81. DOI:10.1093/ndt/gfp133
29. Coppo R, Roccatello D, Amore A, et al. Effects of a gluten-free diet in primary IgA nephropathy. Clin Nephrol. 1990;33:72-86
30. Collin P, Salmi TT, Hervonen K, et al. Dermatitis herpetiformis: a cutaneous manifestation of coeliac disease. Ann Med. 2017;49(1):23-31. DOI:10.1080/07853890.2016.1222450
31. Coppo R. The intestine-renal connection in IgA nephropathy. Nephrol Dial Transplant. 2015;30(3):360-6. DOI:10.1093/ndt/gfu343
32. Pasternack A, Collin P, Mustonen J, et al. Glomerular IgA deposits in patients with celiac disease. Clin Nephrol. 1990;34(2):56-60.
33. Tissandié E, Morelle W, Berthelot L, et al. Both IgA nephropathy and alcoholic cirrhosis feature abnormally glycosylated IgA1 and soluble CD89-IgA and IgG-IgA complexes: common mechanisms for distinct diseases. Kidney Int. 2011;80(12):1352-63. DOI:10.1038/ki.2011.276
34. van de Wiel A, Valentijn RM, Schuurman HJ, et al. Circulating IgA immune complexes and skin IgA deposits in liver disease. Relation to liver histopathology. Dig Dis Sci. 1988;33(6):679-84. DOI:10.1007/BF01540430
35. Mutlu EA, Gillevet PM, Rangwala H, et al. Colonic microbiome is altered in alcoholism. Am J Physiol Gastrointest Liver Physiol. 2012;302(9):G966-78. DOI:10.1152/ajpgi.00380.2011
36. Rao RK, Seth A, Sheth P. Recent advances in alcoholic liver disease: I. Role of intestinal permeability and endotoxemia in alcoholic liver disease. Am J Physiol Gastrointest Liver Physiol. 2004;286(6):G881-4. DOI:10.1152/ajpgi.00006.2004
37. Parlesak A, Schäfer C, Schütz T, et al. Increased intestinal permeability to macromolecules and endotoxemia in patients with chronic alcohol abuse in different stages of alcohol-induced liver disease. J Hepatol. 2000;32(5):742-7. DOI:10.1016/s0168-8278(00)80242-1
38. Chemouny JM, Gleeson PJ, Abbad L, et al. Modulation of the microbiota by oral antibiotics treats immunoglobulin A nephropathy in humanized mice. Nephrol Dial Transplant. 2019;34(7):1135-44. DOI:1093/ndt/gfy323
39. Soylu A, Berktaş S, Sarioğlu S, Erbil G. Saccharomyces boulardii prevents oral-poliovirus vaccine-induced IgA nephropathy in mice. Pediatr Nephrol. 2008;23(8):1287-91. DOI:10.1007/s00467-008-0813-2
40. Fellström BC, Barratt J, Cook H, Coppo R. Targeted-release budesonide versus placebo in patients with IgA nephropathy (NEFIGAN):
a double-blind, randomised, placebo-controlled phase 2b trial. Lancet.
2017;389(10084):2117-27. DOI:10.1016/S0140-6736(17)30550-0
41. Lafayette RA, Canetta PA, Rovin BH. A Randomized, Controlled Trial of Rituximab in IgA Nephropathy with Proteinuria and Renal Dysfunction. J Am Soc Nephrol. 2017;28(4):1306-13. DOI:10.1681/ASN.2016060640
1 ФГАОУ ВО «Первый Московский государственный медицинский университет им. И.М. Сеченова» Минздрава России (Сеченовский Университет), Москва, Россия;
2 ФГБОУ ВО «Московский государственный университет им. М.В. Ломоносова», Москва, Россия
*guldoc@mail.ru
________________________________________________
Sergei V. Guliaev*1, Leonid A. Strizhakov1,2, Natalia V. Chebotareva1,2, Sergei V. Moiseev1,2
1 Sechenov First Moscow State Medical University (Sechenov University), Moscow, Russia;
2 Lomonosov Moscow State University, Moscow, Russia
*guldoc@mail.ru