Yıl: 2022 Cilt: 31 Sayı: 2 Sayfa Aralığı: 93 - 102 Metin Dili: İngilizce DOI: 10.5152/turkjnephrol.2022.21253 İndeks Tarihi: 06-07-2022

Primary Glomerular Diseases and Novel Biomarkers

Öz:
Glomerulonephritis is the third most common cause of end-stage kidney disease. The presentation, clinical course, and outcome of glomerular diseases are highly variable. A kidney biopsy is always needed to clarify the diagnosis; however, performing a kidney biopsy is limited by several factors such as bleeding disorders, obesity, and other comorbid conditions. There is a need for less invasive, simple, and reproducible tests, especially by using blood and urine samples, which could replace kidney biopsy. Our review focuses on the novel clinical, histopathological, blood, and urine biomarkers to make an accurate diagnosis and predict the prognosis of primary glomerular diseases including immunoglobulin A nephropathy, membranous nephropathy, focal segmental glomerulosclerosis, and membranoproliferative glomerulonephritis. Overall, although there are promising biomarkers for glomerulonephritis, long-term evaluation of these biomarkers is still needed.
Anahtar Kelime:

Belge Türü: Makale Makale Türü: Derleme Erişim Türü: Erişime Açık
  • 1. Ali AA, Sharif DA, Almukhtar SE, Abd KH, Saleem ZSM, Hughson MD. Incidence of glomerulonephritis and non-diabetic endstage renal disease in a developing middle-east region near armed conflict. BMC Nephrol. 2018;19(1):257. [CrossRef]
  • 2. Varghese SA, Powell TB, Budisavljevic MN, et al. Urine biomarkers predict the cause of glomerular disease. J Am Soc Nephrol. 2007;18(3):913-922. [CrossRef]
  • 3. Caliskan Y, Kiryluk K. Novel biomarkers in glomerular disease. Adv Chronic Kidney Dis. 2014;21(2):205-216. [CrossRef]
  • 4. Hassler JR. IgA nephropathy: a brief review. Semin Diagn Pathol. 2020;37(3):143-147. [CrossRef]
  • 5. Selvaskandan H, Shi S, Twaij S, Cheung CK, Barratt J. Monitoring immune responses in IgA nephropathy: biomarkers to guide management. Front Immunol. 2020;11:572754. [CrossRef]
  • 6. Kim JS, Hwang HS, Lee SH, et al. Clinical relevance of serum galactose deficient IgA1 in patients with IgA nephropathy. J Clin Med. 2020;9(11). [CrossRef]
  • 7. Tomana M, Novak J, Julian BA, Matousovic K, Konecny K, Mestecky J. Circulating immune complexes in IgA nephropathy consist of IgA1 with galactose-deficient hinge region and antiglycan antibodies. J Clin Invest. 1999;104(1):73-81. [CrossRef]
  • 8. Maixnerova D, Reily C, Bian Q, Neprasova M, Novak J, Tesar V. Markers for the progression of IgA nephropathy. J Nephrol. 2016;29(4):535-541. [CrossRef]
  • 9. Tortajada A, Gutierrez E, Pickering MC, Praga Terente M, Medjeral- Thomas N. The role of complement in IgA nephropathy. Mol Immunol. 2019;114:123-132. [CrossRef]
  • 10. Moriyama T. Clinical and histological features and therapeutic strategies for IgA nephropathy. Clin Exp Nephrol. 2019;23(9):1089- 1099. [CrossRef]
  • 11. Radford MG, Jr, Donadio JV, Jr, Bergstralh EJ, Grande JP. Predicting renal outcome in IgA nephropathy. J Am Soc Nephrol. 1997;8(2):199-207. [CrossRef]
  • 12. Li PK, Ho KK, Szeto CC, Yu L, Lai FM. Prognostic indicators of IgA nephropathy in the Chinese--clinical and pathological perspectives. Nephrol Dial Transplant. 2002;17(1):64-69. [CrossRef]
  • 13. Lv J, Zhang H, Zhou Y, Li G, Zou W, Wang H. Natural history of immunoglobulin A nephropathy and predictive factors of prognosis: a long-term follow up of 204 cases in China. Nephrology. 2008;13(3):242-246. [CrossRef]
  • 14. Goto M, Wakai K, Kawamura T, Ando M, Endoh M, Tomino Y. A scoring system to predict renal outcome in IgA nephropathy: a nationwide 10-year prospective cohort study. Nephrol Dial Transplant. 2009;24(10):3068-3074. [CrossRef]
  • 15. Berthoux F, Mohey H, Laurent B, Mariat C, Afiani A, Thibaudin L. Predicting the risk for dialysis or death in IgA nephropathy. J Am Soc Nephrol. 2011;22(4):752-761. [CrossRef]
  • 16. Donadio JV, Bergstralh EJ, Grande JP, Rademcher DM. Proteinuria patterns and their association with subsequent end-stage renal disease in IgA nephropathy. Nephrol Dial Transplant. 2002;17(7):1197-1203. [CrossRef]
  • 17. Reich HN, Troyanov S, Scholey JW, Cattran DC, Toronto Glomerulonephritis Registry. Remission of proteinuria improves prognosis in IgA nephropathy. J Am Soc Nephrol. 2007;18(12):3177-3183. [CrossRef]
  • 18. Okabayashi Y, Tsuboi N, Haruhara K, et al. Reduction of proteinuria by therapeutic intervention improves the renal outcome of elderly patients with IgA nephropathy. Clin Exp Nephrol. 2016;20(6):910- 917. [CrossRef]
  • 19. Alamartine E, Sabatier JC, Guerin C, Berliet JM, Berthoux F. Prognostic factors in mesangial IgA glomerulonephritis: an extensive study with univariate and multivariate analyses. Am J Kidney Dis. 1991;18(1):12-19. [CrossRef]
  • 20. Gorriz JL, Martinez-Castelao A. Proteinuria: detection and role in native renal disease progression. Transplant Rev. 2012;26(1):3-13. [CrossRef]
  • 21. Cravedi P, Remuzzi G. Pathophysiology of proteinuria and its value as an outcome measure in chronic kidney disease. Br J Clin Pharmacol. 2013;76(4):516-523. [CrossRef]
  • 22. Szeto CC, Lai FM, To KF, et al. The natural history of immunoglobulin A nephropathy among patients with hematuria and minimal proteinuria. Am J Med. 2001;110(6):434-437. [CrossRef]
  • 23. Moriyama T, Tanaka K, Iwasaki C, et al. Prognosis in IgA nephropathy: 30-year analysis of 1,012 patients at a single center in Japan. PLoS ONE. 2014;9(3):e91756. [CrossRef]
  • 24. Wakai K, Kawamura T, Endoh M, et al. A scoring system to predict renal outcome in IgA nephropathy: from a nationwide prospective study. Nephrol Dial Transplant. 2006;21(10):2800-2808. [CrossRef] 25. Lee H, Kim DK, Oh KH, et al. Mortality of IgA nephropathy patients: a single center experience over 30 years. PLoS ONE. 2012;7(12):e51225. [CrossRef]
  • 26. Syrjänen J, Mustonen J, Pasternack A. Hypertriglyceridaemia and hyperuricaemia are risk factors for progression of IgA nephropathy. Nephrol Dial Transplant. 2000;15(1):34-42. [CrossRef]
  • 27. Shimamoto M, Ohsawa I, Suzuki H, et al. Impact of body mass index on progression of IgA nephropathy among Japanese patients. J Clin Lab Anal. 2015;29(5):353-360. [CrossRef] 28. Berger J. IgA glomerular deposits in renal disease. Transplant Proc. 1969;1(4):939-944.
  • 29. Hastings MC, Moldoveanu Z, Suzuki H, et al. Biomarkers in IgA nephropathy: relationship to pathogenetic hits. Expert Opin Med Diagn. 2013;7(6):615-627. [CrossRef]
  • 30. Trimarchi H, Barratt J, Cattran DC, et al. Oxford classification of IgA nephropathy 2016: an update from the IgA Nephropathy Classification Working Group. Kidney Int. 2017;91(5):1014-1021. [CrossRef]
  • 31. Caliskan Y, Demir E, Karatay E, et al. Oxidative stress and macrophage infiltration in IgA nephropathy. J Nephrol. 2021. [CrossRef] 32. Becker JU, Mayerich D, Padmanabhan M, et al. Artificial intelligence and machine learning in nephropathology. Kidney Int. 2020;98(1):65-75. [CrossRef]
  • 33. Caliskan Y, Ozluk Y, Celik D, et al. The clinical significance of uric acid and complement activation in the progression of IgA nephropathy. Kidney Blood Press Res. 2016;41(2):148-157. [CrossRef]
  • 34. Kim SJ, Koo HM, Lim BJ, et al. Decreased circulating C3 levels and mesangial C3 deposition predict renal outcome in patients with IgA nephropathy. PLoS ONE. 2012;7(7):e40495. [CrossRef]
  • 35. Roos A, Rastaldi MP, Calvaresi N, et al. Glomerular activation of the lectin pathway of complement in IgA nephropathy is associated with more severe renal disease. J Am Soc Nephrol. 2006;17(6):1724- 1734. [CrossRef]
  • 36. Espinosa M, Ortega R, Sánchez M, et al. Association of C4d deposition with clinical outcomes in IgA nephropathy. Clin J Am Soc Nephrol. 2014;9(5):897-904. [CrossRef]
  • 37. Yanagawa H, Suzuki H, Suzuki Y, et al. A panel of serum biomarkers differentiates IgA nephropathy from other renal diseases. PLoS ONE. 2014;9(5):e98081. [CrossRef]
  • 38. Zhang L, Wang Y, Shi X, Zou H, Jiang Y. A higher frequency of CD4(+) CXCR5(+) T follicular helper cells in patients with newly diagnosed IgA nephropathy. Immunol Lett. 2014;158(1-2):101-108. [CrossRef]
  • 39. Bagchi S, Lingaiah R, Mani K, et al. Significance of serum galactose deficient IgA1 as a potential biomarker for IgA nephropathy: a case control study. PLoS ONE. 2019;14(3):e0214256. [CrossRef]
  • 40. Shimozato S, Hiki Y, Odani H, Takahashi K, Yamamoto K, Sugiyama S. Serum under-galactosylated IgA1 is increased in Japanese patients with IgA nephropathy. Nephrol Dial Transplant. 2008;23(6):1931-1939. [CrossRef]
  • 41. Berthoux F, Suzuki H, Thibaudin L, et al. Autoantibodies targeting galactose-deficient IgA1 associate with progression of IgA nephropathy. J Am Soc Nephrol. 2012;23(9):1579-1587. [CrossRef]
  • 42. 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(6):1668-1677. [CrossRef]
  • 43. Kiryluk K, Li Y, Sanna-Cherchi S, et al. Geographic differences in genetic susceptibility to IgA nephropathy: GWAS replication study and geospatial risk analysis. PLoS Genet. 2012;8(6):e1002765. [CrossRef]
  • 44. Gharavi AG, Kiryluk K, Choi M, et al. Genome-wide association study identifies susceptibility loci for IgA nephropathy. Nat Genet. 2011;43(4):321-327. [CrossRef]
  • 45. Kiryluk K, Li Y, Scolari F, et al. Discovery of new risk loci for IgA nephropathy implicates genes involved in immunity against intestinal pathogens. Nat Genet. 2014;46(11):1187-1196. [CrossRef]
  • 46. Selvaskandan H, Pawluczyk I, Barratt J. MicroRNAs: a new avenue to understand, investigate and treat immunoglobulin A nephropathy? Clin Kidney J. 2018;11(1):29-37. [CrossRef]
  • 47. Serino G, Sallustio F, Cox SN, Pesce F, Schena FP. Abnormal miR- 148b expression promotes aberrant glycosylation of IgA1 in IgA nephropathy. J Am Soc Nephrol. 2012;23(5):814-824. [CrossRef]
  • 48. Szeto CC, Ching-Ha KB, Ka-Bik L, et al. Micro-RNA expression in the urinary sediment of patients with chronic kidney diseases. Dis Markers. 2012;33(3):137-144. [CrossRef]
  • 49. Bao H, Chen H, Zhu X, et al. MiR-223 downregulation promotes glomerular endothelial cell activation by upregulating importin alpha4 and alpha5 in IgA nephropathy. Kidney Int. 2014;85(3):624- 635. [CrossRef]
  • 50. Serino G, Pesce F, Sallustio F, et al. In a retrospective international study, circulating miR-148b and let-7b were found to be serum markers for detecting primary IgA nephropathy. Kidney Int. 2016;89(3):683-692. [CrossRef]
  • 51. Ghiggeri GM, Seitz-Polski B, Justino J, et al. Multi-autoantibody signature and clinical outcome in membranous nephropathy. Clin J Am Soc Nephrol. 2020;15(12):1762-1776. [CrossRef]
  • 52. Cavanaugh C, Okusa MD. The evolving role of novel biomarkers in glomerular disease: a review. Am J Kidney Dis. 2021;77(1):122-131. [CrossRef]
  • 53. Maifata SM, Hod R, Zakaria F, Abd Ghani F. Primary membranous glomerulonephritis: the role of serum and urine biomarkers in patient management. Biomedicines. 2019;7(4). [CrossRef]
  • 54. Salant DJ. Genetic variants in membranous nephropathy: perhaps a perfect storm rather than a straightforward conformeropathy? J Am Soc Nephrol. 2013;24(4):525-528. [CrossRef]
  • 55. Rodriguez EF, Nasr SH, Larsen CP, Sethi S, Fidler ME, Cornell LD. Membranous nephropathy with crescents: a series of 19 cases. Am J Kidney Dis. 2014;64(1):66-73. [CrossRef]
  • 56. De Vriese AS, Glassock RJ, Nath KA, Sethi S, Fervenza FC. A proposal for a serology-based approach to membranous nephropathy. J Am Soc Nephrol. 2017;28(2):421-430. [CrossRef]
  • 57. van den Brand JA, Hofstra JM, Wetzels JF. Prognostic value of risk score and urinary markers in idiopathic membranous nephropathy. Clin J Am Soc Nephrol. 2012;7(8):1242-1248. [CrossRef]
  • 58. Parker SE. Use and abuse of volatile substances in industry. Hum Toxicol. 1989;8(4):271-275. [CrossRef]
  • 59. An C, Akankwasa G, Liu J, et al. Urine markers of renal tubular injury in idiopathic membranous nephropathy: a cross sectional study. Clin Chim Acta. 2019;492:7-11. [CrossRef]
  • 60. Sprangers B, Bomback AS, Cohen SD, et al. Idiopathic membranous nephropathy: clinical and histologic prognostic features and treatment patterns over time at a tertiary referral center. Am J Nephrol. 2012;36(1):78-89. [CrossRef]
  • 61. Val-Bernal JF, Garijo MF, Val D, Rodrigo E, Arias M. C4d as a diagnostic tool in membranous nephropathy. Nefrologia. 2012;32(4):536; author reply 537. [CrossRef]
  • 62. Sethi S, Madden BJ, Debiec H, et al. Exostosin 1/exostosin 2-associated membranous nephropathy. J Am Soc Nephrol. 2019;30(6):1123-1136. [CrossRef]
  • 63. Mahmud M, Pinnschmidt HO, Reinhard L, et al. Role of phospholipase A2 receptor 1 antibody level at diagnosis for long-term renal outcome in membranous nephropathy. PLoS ONE. 2019;14(9):e0221293. [CrossRef]
  • 64. Timmermans SA, Ayalon R, van Paassen P, et al. Anti-phospholipase A2 receptor antibodies and malignancy in membranous nephropathy. Am J Kidney Dis. 2013;62(6):1223-1225. [CrossRef]
  • 65. Hoxha E, Harendza S, Pinnschmidt H, Panzer U, Stahl RA. PLA2R antibody levels and clinical outcome in patients with membranous nephropathy and non-nephrotic range proteinuria under treatment with inhibitors of the renin-angiotensin system. PLoS ONE. 2014;9(10):e110681. [CrossRef]
  • 66. Caza TN, Hassen SI, Dvanajscak Z, et al. NELL1 is a target antigen in malignancy-associated membranous nephropathy. Kidney Int. 2021;99(4):967-976. [CrossRef]
  • 67. Sharma SG, Larsen CP. Tissue staining for THSD7A in glomeruli correlates with serum antibodies in primary membranous nephropathy: a clinicopathological sudy. Mod Pathol. 2018;31(4):616-622. [CrossRef]
  • 68. Al-Rabadi LF, Caza T, Trivin-Avillach C, et al. Serine protease HTRA1 as a novel target antigen in primary membranous nephropathy. J Am Soc Nephrol. 2021;32(7):1666-1681. [CrossRef]
  • 69. Le Quintrec M, Teisseyre M, Bec N, et al. Contactin-1 is a novel target antigen in membranous nephropathy associated with chronic inflammatory demyelinating polyneuropathy. Kidney Int. 2021;100(6):1240-1249. [CrossRef]
  • 70. D’Agati VD, Kaskel FJ, Falk RJ. Focal segmental glomerulosclerosis. N Engl J Med. 2011;365(25):2398-2411. [CrossRef]
  • 71. Rosenberg AZ, Kopp JB. Focal segmental glomerulosclerosis. Clin J Am Soc Nephrol. 2017;12(3):502-517. [CrossRef]
  • 72. Sprangers B, Meijers B, Appel G. FSGS: diagnosis and diagnostic work-up. BioMed Res Int. 2016;2016:4632768. [CrossRef]
  • 73. Maas RJ, Deegens JK, Smeets B, Moeller MJ, Wetzels JF. Minimal change disease and idiopathic FSGS: manifestations of the same disease. Nat Rev Nephrol. 2016;12(12):768-776. [CrossRef]
  • 74. Jacobs-Cachá C, Vergara A, García-Carro C, et al. Challenges in primary focal segmental glomerulosclerosis diagnosis: from the diagnostic algorithm to novel biomarkers. Clin Kidney J. 2021;14(2):482-491. [CrossRef]
  • 75. Praga M, Morales E, Herrero JC, et al. Absence of hypoalbuminemia despite massive proteinuria in focal segmental glomerulosclerosis secondary to hyperfiltration. Am J Kidney Dis. 1999;33(1):52-58. [CrossRef]
  • 76. Trautmann A, Schnaidt S, Lipska-Ziętkiewicz BS, et al. Long-term outcome of steroid-resistant nephrotic syndrome in children. J Am Soc Nephrol. 2017;28(10):3055-3065. [CrossRef]
  • 77. D’Agati VD, Fogo AB, Bruijn JA, Jennette JC. Pathologic classification of focal segmental glomerulosclerosis: a working proposal. Am J Kidney Dis. 2004;43(2):368-382. [CrossRef]
  • 78. Gipson DS, Trachtman H, Kaskel FJ, et al. Clinical trial of focal segmental glomerulosclerosis in children and young adults. Kidney Int. 2011;80(8):868-878. [CrossRef]
  • 79. Thomas DB, Franceschini N, Hogan SL, et al. Clinical and pathologic characteristics of focal segmental glomerulosclerosis pathologic variants. Kidney Int. 2006;69(5):920-926. [CrossRef]
  • 80. Sethi S, Zand L, Nasr SH, Glassock RJ, Fervenza FC. Focal and segmental glomerulosclerosis: clinical and kidney biopsy correlations. Clin Kidney J. 2014;7(6):531-537. [CrossRef]
  • 81. Fatima H, Moeller MJ, Smeets B, et al. Parietal epithelial cell activation marker in early recurrence of FSGS in the transplant. Clin J Am Soc Nephrol. 2012;7(11):1852-1858. [CrossRef]
  • 82. Zhang J, Pippin JW, Krofft RD, Naito S, Liu ZH, Shankland SJ. Podocyte repopulation by renal progenitor cells following glucocorticoids treatment in experimental FSGS. Am J Physiol Ren Physiol. 2013;304(11):F1375-F1389. [CrossRef]
  • 83. Froes BP, de Almeida Araújo S, Bambirra EA, Oliveira EA, Simões E Silva AC, Pinheiro SVB. Is CD44 in glomerular parietal epithelial cells a pathological marker of renal function deterioration in primary focal segmental glomerulosclerosis? Pediatr Nephrol. 2017;32(11):2165-2169. [CrossRef]
  • 84. Harel E, Shoji J, Abraham V, et al. Identifying a potential biomarker for primary focal segmental glomerulosclerosis and its association with recurrence after transplantation. Clin Transplant. 2019;33(3):e13487. [CrossRef]
  • 85. Wei C, Trachtman H, Li J, et al. Circulating suPAR in two cohorts of primary FSGS. J Am Soc Nephrol. 2012;23(12):2051-2059. [CrossRef]
  • 86. Wei C, El Hindi S, Li J, et al. Circulating urokinase receptor as a cause of focal segmental glomerulosclerosis. Nat Med. 2011;17(8):952-960. [CrossRef]
  • 87. Hayek SS, Sever S, Ko YA, et al. Soluble urokinase receptor and chronic kidney disease. N Engl J Med. 2015;373(20):1916-1925. [CrossRef]
  • 88. Peev V, Hahm E, Reiser J. Unwinding focal segmental glomerulosclerosis. F1000Res. 2017;6:466. [CrossRef]
  • 89. Delville M, Sigdel TK, Wei C, et al. A circulating antibody panel for pretransplant prediction of FSGS recurrence after kidney transplantation. Sci Transl Med. 2014;6(256):256ra136. [CrossRef]
  • 90. Srivastava P, Solanki AK, Arif E, et al. Development of a novel cellbased assay to diagnose recurrent focal segmental glomerulosclerosis patients. Kidney Int. 2019;95(3):708-716. [CrossRef]
  • 91. Nafar M, Kalantari S, Samavat S, Rezaei-Tavirani M, Rutishuser D, Zubarev RA. The novel diagnostic biomarkers for focal segmental glomerulosclerosis. Int J Nephrol. 2014;2014:574261. [CrossRef]
  • 92. Clark AJ, Jabs K, Hunley TE, et al. Urinary apolipoprotein AI in children with kidney disease. Pediatr Nephrol. 2019;34(11):2351- 2360. [CrossRef]
  • 93. Kaysen GA, de Sain-van der Velden MG. New insights into lipid metabolism in the nephrotic syndrome. Kidney Int Suppl. 1999;71:S18-S21. [CrossRef]
  • 94. Lopez-Hellin J, Cantarell C, Jimeno L, et al. A form of apolipoprotein a-I is found specifically in relapses of focal segmental glomerulosclerosis following transplantation. Am J Transplant. 2013;13(2):493-500. [CrossRef]
  • 95. Schena FP, Esposito P, Rossini M. A narrative review on C3 glomerulopathy: a rare renal disease. Int J Mol Sci. 2020;21(2). [CrossRef]
  • 96. Pickering MC, D’Agati VD, Nester CM, et al. C3 glomerulopathy: consensus report. Kidney Int. 2013;84(6):1079-1089. [CrossRef] 97. Cook HT, Pickering MC. Clusters not classifications: making sense of complement-mediated kidney injury. J Am Soc Nephrol. 2018;29(1):9-12. [CrossRef]
  • 98. Merle NS, Noe R, Halbwachs-Mecarelli L, Fremeaux-Bacchi V, Roumenina LT. Complement system part II: role in immunity. Front Immunol. 2015;6:257. [CrossRef]
  • 99. Medjeral-Thomas NR, Pickering MC, Cook HT. Complement and kidney disease, new insights. Curr Opin Nephrol Hypertens. 2021;30(3):310-316. [CrossRef]
  • 100. Fakhouri F, Frémeaux-Bacchi V, Noël LH, Cook HT, Pickering MC. C3 glomerulopathy: a new classification. Nat Rev Nephrol. 2010;6(8):494-499. [CrossRef]
  • 101. Sethi S, Vrana JA, Fervenza FC, et al. Characterization of C3 in C3 glomerulopathy. Nephrol Dial Transplant. 2017;32(3):459-465. [CrossRef]
  • 102. D’Agati VD, Bomback AS. In search of C3G tissue biomarkers. Kidney Int Rep. 2019;4(10):1359-1361. [CrossRef]
  • 103. Medjeral-Thomas NR, Moffitt H, Lomax-Browne HJ, et al. Glomerular complement factor H-related protein 5 (FHR5) is highly prevalent in C3 glomerulopathy and associated with renal impairment. Kidney Int Rep. 2019;4(10):1387-1400. [CrossRef]
  • 104. Servais A, Noël LH, Roumenina LT, et al. Acquired and genetic complement abnormalities play a critical role in dense deposit disease and other C3 glomerulopathies. Kidney Int. 2012;82(4):454-464. [CrossRef]
  • 105. Dalili N, Behnam B, Vali F, et al. C3 glomerulonephritis with multiple mutations in complement factor H. Iran J Kidney Dis. 2018;12(6):376-381.
  • 106. Garam N, Cserhalmi M, Prohászka Z, et al. FHR-5 serum levels and CFHR5 genetic variations in patients with immune complex-mediated membranoproliferative glomerulonephritis and C3-glomerulopathy. Front Immunol. 2021;12:720183. [CrossRef]
  • 107. Athanasiou Y, Voskarides K, Gale DP, et al. Familial C3 glomerulopathy associated with CFHR5 mutations: clinical characteristics of 91 patients in 16 pedigrees. Clin J Am Soc Nephrol. 2011;6(6):1436- 1446. [CrossRef]
  • 108. Malik TH, Gitterman DP, Lavin DP, et al. Gain-of-function factor H-related 5 protein impairs glomerular complement regulation resulting in kidney damage. Proc Natl Acad Sci USA. 2021;118(13). [CrossRef]
APA şafak s, Caliskan Y (2022). Primary Glomerular Diseases and Novel Biomarkers. , 93 - 102. 10.5152/turkjnephrol.2022.21253
Chicago şafak seda,Caliskan Yasar Primary Glomerular Diseases and Novel Biomarkers. (2022): 93 - 102. 10.5152/turkjnephrol.2022.21253
MLA şafak seda,Caliskan Yasar Primary Glomerular Diseases and Novel Biomarkers. , 2022, ss.93 - 102. 10.5152/turkjnephrol.2022.21253
AMA şafak s,Caliskan Y Primary Glomerular Diseases and Novel Biomarkers. . 2022; 93 - 102. 10.5152/turkjnephrol.2022.21253
Vancouver şafak s,Caliskan Y Primary Glomerular Diseases and Novel Biomarkers. . 2022; 93 - 102. 10.5152/turkjnephrol.2022.21253
IEEE şafak s,Caliskan Y "Primary Glomerular Diseases and Novel Biomarkers." , ss.93 - 102, 2022. 10.5152/turkjnephrol.2022.21253
ISNAD şafak, seda - Caliskan, Yasar. "Primary Glomerular Diseases and Novel Biomarkers". (2022), 93-102. https://doi.org/10.5152/turkjnephrol.2022.21253
APA şafak s, Caliskan Y (2022). Primary Glomerular Diseases and Novel Biomarkers. Turkish journal of nephrology (Online), 31(2), 93 - 102. 10.5152/turkjnephrol.2022.21253
Chicago şafak seda,Caliskan Yasar Primary Glomerular Diseases and Novel Biomarkers. Turkish journal of nephrology (Online) 31, no.2 (2022): 93 - 102. 10.5152/turkjnephrol.2022.21253
MLA şafak seda,Caliskan Yasar Primary Glomerular Diseases and Novel Biomarkers. Turkish journal of nephrology (Online), vol.31, no.2, 2022, ss.93 - 102. 10.5152/turkjnephrol.2022.21253
AMA şafak s,Caliskan Y Primary Glomerular Diseases and Novel Biomarkers. Turkish journal of nephrology (Online). 2022; 31(2): 93 - 102. 10.5152/turkjnephrol.2022.21253
Vancouver şafak s,Caliskan Y Primary Glomerular Diseases and Novel Biomarkers. Turkish journal of nephrology (Online). 2022; 31(2): 93 - 102. 10.5152/turkjnephrol.2022.21253
IEEE şafak s,Caliskan Y "Primary Glomerular Diseases and Novel Biomarkers." Turkish journal of nephrology (Online), 31, ss.93 - 102, 2022. 10.5152/turkjnephrol.2022.21253
ISNAD şafak, seda - Caliskan, Yasar. "Primary Glomerular Diseases and Novel Biomarkers". Turkish journal of nephrology (Online) 31/2 (2022), 93-102. https://doi.org/10.5152/turkjnephrol.2022.21253