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Определение мочевых маркеров фокального сегментарного гломерулосклероза с помощью протеомного анализа
Определение мочевых маркеров фокального сегментарного гломерулосклероза с помощью протеомного анализа
Виноградов А.А., Чеботарева Н.В., Бугрова А.Е., Бржозовский А.Г., Краснова Т.Н., Насибуллина К.З., Кононихин А.С., Моисеев С.В. Определение мочевых маркеров фокального сегментарного гломерулосклероза с помощью протеомного анализа. Терапевтический архив. 2023;95(6):457–461.
DOI: 10.26442/00403660.2023.06.202266
© ООО «КОНСИЛИУМ МЕДИКУМ», 2023 г.
DOI: 10.26442/00403660.2023.06.202266
© ООО «КОНСИЛИУМ МЕДИКУМ», 2023 г.
________________________________________________
Материалы доступны только для специалистов сферы здравоохранения. Авторизуйтесь или зарегистрируйтесь.
Аннотация
Обоснование. Фокальный сегментарный гломерулосклероз (ФСГС) относится к первичным подоцитопатиям, которые характеризуются первичным повреждением подоцитов и высокой протеинурией. Поиск биомаркеров и факторов, участвующих в прогрессировании этого заболевания почек, является актуальной задачей в настоящее время.
Цель. Оценить протеомный профиль мочи у больных с ФСГС и выделить мочевые биомаркеры подоцитопатий.
Материалы и методы. В исследование включен 41 пациент с диагнозом хронического гломерулонефрита – 27 мужчин и 14 женщин. По данным морфологического исследования у 28 пациентов диагностирован ФСГС, у 9 – со стероид-чувствительным нефротическим синдромом и 14 – со стероид-резистентным (СР) нефротическим синдромом. В группу сравнения вошли 13 больных с мембранозной нефропатией. Исследование протеома мочи проводилось методом таргетной хромато-масс-спектрометрии в режиме мониторинга множественных реакций с использованием синтетических изотопно-меченых пептидных стандартов.
Результаты. Наибольшие различия по белковому составу мочи выявлены в подгруппах стероид-чувствительного и СР ФСГС. В группе СР ФСГС в дебюте заболевания отмечалось высокое содержание белков, отражающих повреждение гломерулярного фильтра (аполипопротеин А-IV, орозомукоид, кадгерин, гемопексин, витронектин), а также белков, связанных с тубулоинтерстициальным воспалением и накоплением экстрацеллюлярного матрикса (ретинол- и витамин-D-связывающие белки, кининоген-1, люмикан и нейрофилин-2). По сравнению с группой мембранозной нефропатии у больных с ФСГС отмечена достоверно более высокая концентрация в моче карнозиназы, орозомукоида, кадгерина-13, тенасцина X, остеопонтина, цинк-α-2-гликопротеина.
Заключение. Таким образом, у больных со СР ФСГС протеомный профиль мочи включает большее количество белков в повышенных концентрациях, что отражает тяжелое повреждение различных отделов нефрона по сравнению с больными со стероид-чувствительным ФСГС и мембранозной нефропатией.
Ключевые слова: подоцитопатии, фокальный сегментарный гломерулосклероз, нефротический синдром, стероид-чувствительный, стероид-резистентный, протеом мочи, масс-спектрометрия
Aim. To assess the proteomic profile of urine in patients with FSGS and to isolate urinary biomarkers of podocytopathies.
Materials and methods. The study included 41 patients diagnosed with chronic glomerulonephritis, 27 men and 14 women. According to the morphological study, 28 patients were diagnosed with FSGS, 9 with steroid-sensitive nephrotic syndrome and 14 with steroid-resistant nephrotic syndrome. The comparison group included 13 patients with membranous nephropathy. The study of the urinary proteome was carried out by targeted liquid chromatography-mass spectrometry using multiple reaction monitoring with synthetic stable isotope labelled peptide standards.
Results. The main differences in the protein profile of urine were found in the subgroups of steroid-sensitive (SS) and steroid-resistant (SR) FSGS. In the FSGS SR group, at the onset of the disease, there was a high concentration of proteins reflecting damage to the glomerular filter (apo-lipoprotein A-IV, orosomucoid, cadherin, hemopexin, vitronectin), as well as proteins associated with tubulo-interstitial inflammation and accumulation of extracellular matrix (retinol- and vitamin D-binding proteins, kininogen-1, lumican and neurophilin-2). Compared with the membranous nephropathy group, FSGS patients had significantly higher urinary concentrations of carnosinase, orosomucoid, cadherin-13, tenascin X, osteopontin, and zinc-alpha-2-glycoprotein.
Conclusion. Thus, in patients with SR FSGS, the proteomic profile of urine includes more proteins at elevated concentrations, which reflects severe damage to various parts of the nephron compared with patients with SS FSGS and membranous nephropathy.
Keywords: podocytopathies, focal segmental glomerulosclerosis, nephrotic syndrome, steroid-sensitive, steroid-resistant, urinary proteome, mass spectrometry
Цель. Оценить протеомный профиль мочи у больных с ФСГС и выделить мочевые биомаркеры подоцитопатий.
Материалы и методы. В исследование включен 41 пациент с диагнозом хронического гломерулонефрита – 27 мужчин и 14 женщин. По данным морфологического исследования у 28 пациентов диагностирован ФСГС, у 9 – со стероид-чувствительным нефротическим синдромом и 14 – со стероид-резистентным (СР) нефротическим синдромом. В группу сравнения вошли 13 больных с мембранозной нефропатией. Исследование протеома мочи проводилось методом таргетной хромато-масс-спектрометрии в режиме мониторинга множественных реакций с использованием синтетических изотопно-меченых пептидных стандартов.
Результаты. Наибольшие различия по белковому составу мочи выявлены в подгруппах стероид-чувствительного и СР ФСГС. В группе СР ФСГС в дебюте заболевания отмечалось высокое содержание белков, отражающих повреждение гломерулярного фильтра (аполипопротеин А-IV, орозомукоид, кадгерин, гемопексин, витронектин), а также белков, связанных с тубулоинтерстициальным воспалением и накоплением экстрацеллюлярного матрикса (ретинол- и витамин-D-связывающие белки, кининоген-1, люмикан и нейрофилин-2). По сравнению с группой мембранозной нефропатии у больных с ФСГС отмечена достоверно более высокая концентрация в моче карнозиназы, орозомукоида, кадгерина-13, тенасцина X, остеопонтина, цинк-α-2-гликопротеина.
Заключение. Таким образом, у больных со СР ФСГС протеомный профиль мочи включает большее количество белков в повышенных концентрациях, что отражает тяжелое повреждение различных отделов нефрона по сравнению с больными со стероид-чувствительным ФСГС и мембранозной нефропатией.
Ключевые слова: подоцитопатии, фокальный сегментарный гломерулосклероз, нефротический синдром, стероид-чувствительный, стероид-резистентный, протеом мочи, масс-спектрометрия
________________________________________________
Aim. To assess the proteomic profile of urine in patients with FSGS and to isolate urinary biomarkers of podocytopathies.
Materials and methods. The study included 41 patients diagnosed with chronic glomerulonephritis, 27 men and 14 women. According to the morphological study, 28 patients were diagnosed with FSGS, 9 with steroid-sensitive nephrotic syndrome and 14 with steroid-resistant nephrotic syndrome. The comparison group included 13 patients with membranous nephropathy. The study of the urinary proteome was carried out by targeted liquid chromatography-mass spectrometry using multiple reaction monitoring with synthetic stable isotope labelled peptide standards.
Results. The main differences in the protein profile of urine were found in the subgroups of steroid-sensitive (SS) and steroid-resistant (SR) FSGS. In the FSGS SR group, at the onset of the disease, there was a high concentration of proteins reflecting damage to the glomerular filter (apo-lipoprotein A-IV, orosomucoid, cadherin, hemopexin, vitronectin), as well as proteins associated with tubulo-interstitial inflammation and accumulation of extracellular matrix (retinol- and vitamin D-binding proteins, kininogen-1, lumican and neurophilin-2). Compared with the membranous nephropathy group, FSGS patients had significantly higher urinary concentrations of carnosinase, orosomucoid, cadherin-13, tenascin X, osteopontin, and zinc-alpha-2-glycoprotein.
Conclusion. Thus, in patients with SR FSGS, the proteomic profile of urine includes more proteins at elevated concentrations, which reflects severe damage to various parts of the nephron compared with patients with SS FSGS and membranous nephropathy.
Keywords: podocytopathies, focal segmental glomerulosclerosis, nephrotic syndrome, steroid-sensitive, steroid-resistant, urinary proteome, mass spectrometry
Полный текст
Список литературы
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2. Rydel JJ, Korbet SM, Borok RZ, Schwartz MM. Focal segmental glomerular sclerosis in adults: presentation, course, and response to treatment. Am J Kidney Dis. 1995;25(4):534-42. DOI:10.1016/0272-6386(95)90120-5
3. Sim JJ, Batech M, Hever A, et al. Distribution of biopsy-proven presumed primary glomerulonephropathies in 2000–2011 among a racially and ethnically diverse US population. Am J Kidney Dis. 2006;68:533-44. DOI:10.1053/j.ajkd.2016.03.416
4. Kitiyakara C, Eggers P, Kopp JB. Twenty-one-year trend in ESRD due to focal segmental glomerulosclerosis in the United States. Am J Kidney Dis. 2004;44(5):815-25. DOI:10.1053/j.ajkd.2004.07.008
5. Coon JJ, Zürbig P, Dakna M, et al. CE-MS analysis of the human urinary proteome for biomarker discovery and disease diagnostics. Proteomics Clin Appl. 2008;2:964-73. DOI:10.1002/prca.200800024
6. Kalantari S, Nafar M, Samavat S, et al. Urinary prognostic biomarkers in patients with focal segmental glomerulosclerosis. Nephrourol Mon. 2014;6(2):e16806. DOI:10.5812/numonthly.16806
7. Pérez V, López D, Boixadera E, et al. Comparative differential proteomic analysis of minimal change disease and focal segmental glomerulosclerosis. BMC Nephrol. 2017;18(1):49. DOI:10.1186/s12882-017-0452-6
8. Medyńska A, Chrzanowska J, Kościelska-Kasprzak K, et al. Alpha-1 Acid Glycoprotein and Podocin mRNA as Novel Biomarkers for Early Glomerular Injury in Obese Children. J Clin Med. 2021;10(18):4129. DOI:10.3390/jcm10184129
9. Christiansen MS, Iversen K, Larsen CT, et al. Increased urinary orosomucoid excretion: A proposed marker for inflammation and endothelial dysfunction in patients with type 2 diabetes. Scand J Clin Lab Investig. 2009;69:272-81. DOI:10.1080/00365510802531100
10. Kalantari S, Nafar M, Rutishauser D, et al. Predictive urinary biomarkers for steroid-resistant and steroid-sensitive focal segmental glomerulosclerosis using high resolution mass spectrometry and multivariate statistical analysis. BMC Nephrol. 2014;15:141. DOI:10.1186/1471-2369-15-141
11. Lingenhel A, Lhotta K, Neyer U, et al. Role of the kidney in the metabolism of apolipoprotein A-IV: influence of the type of proteinuria. J Lipid Res. 2006;47(9):2071-9. DOI:10.1194/jlr.M600178-JLR200
12. Kretzler M. Regulation of adhesive interaction between podocytes and glomerular basement membrane. Microsc Res Tech. 2002;57(4):247-53. DOI:10.1002/jemt.10083
13. Yu CJ, Damaiyanti DW, Yan SJ, et al. The Pathophysiologic Role of Gelsolin in Chronic Kidney Disease: Focus on Podocytes. Int J Mol Sci. 2021;22(24):13281.
DOI:10.3390/ ijms222413281
14. Kapojos JJ, Poelstra K, Borghuis T, et al. Regulation of plasma hemopexin activity by stimulated endothelial or mesangial cells. Nephron Physiol. 2004;96(1):1-10. DOI:10.1159/000075574
15. Pukajło-Marczyk A, Zwolińska D. Involvement of Hemopexin in the Pathogenesis of Proteinuria in Children with Idiopathic Nephrotic Syndrome. J Clin Med. 2021;10(14):3160. DOI:10.3390/jcm10143160
16. Lennon R, Singh A, Welsh GI, et al. Hemopexin induces nephrin-dependent reorganization of the actin cytoskeleton in podocytes. J Am Soc Nephrol. 2008;19(11):2140-9. DOI:10.1681/ASN.2007080940
17. Shen J, Zhu Y, Zhang S, et al. Vitronectin-activated αvβ3 and αvβ5 integrin signalling specifies haematopoietic fate in human pluripotent stem cells. Cell Prolif. 2021;54(4):e13012. DOI:10.1111/cpr.13012
18. Choudhary A, Mohanraj PS, Krishnamurthy S, Rajappa M. Association of Urinary Vitamin D Binding Protein and Neutrophil Gelatinase-Associated Lipocalin with Steroid Responsiveness in Idiopathic Nephrotic Syndrome of Childhood. Saudi J Kidney Dis Transpl. 2020;31(5):946-56. DOI:10.4103/1319-2442.301201
19. Mirković K, Doorenbos CR, Dam WA, et al. Urinary vitamin D binding protein: a potential novel marker of renal interstitial inflammation and fibrosis. PLoS One. 2013;8(2):e55887. DOI:10.1371/journal.pone.0055887
20. Bennett MR, Pordal A, Haffner C, et al. Urinary Vitamin D-Binding Protein as a Biomarker of Steroid-Resistant Nephrotic Syndrome. Biomark Insights. 2016;11:1-6. DOI:10.4137/BMI.S31633
21. Gonzalez-Calero L, Martin-Lorenzo M, Ramos-Barron A, et al. Urinary Kininogen-1 and Retinol binding protein-4 respond to Acute Kidney Injury: predictors of patient prognosis? Sci Rep. 2016;6:19667. DOI:10.1038/srep19667
22. Mastroianni Kirsztajn G, Nishida SK, Silva MS, et al. Urinary retinol-binding protein as a prognostic marker in the treatment of nephrotic syndrome. Nephron. 2000;86(2):109-14. DOI:10.1159/000045727
23. Krishnan A, Li X, Kao WY, Viker K, et al. Lumican, an extracellular matrix proteoglycan, is a novel requisite for hepatic fibrosis. Lab Invest. 2012;92(12):1712-25. DOI:10.1038/labinvest.2012.121
24. Schramek H, Sarközi R, Lauterberg C, et al. Neuropilin-1 and neuropilin-2 are differentially expressed in human proteinuric nephropathies and cytokine-stimulated proximal tubular cells. Lab Invest. 2009;89(11):1304-16. DOI:10.1038/labinvest.2009.96
25. Xie Q, Zhang M, Mao X, et al. Matrix protein Tenascin-C promotes kidney fibrosis via STAT3 activation in response to tubular injury. Cell Death Dis. 2022;13(12):1044. DOI:10.1038/s41419-022-05496-z
26. Steinbrenner I, Sekula P, Kotsis F, el al. Association of osteopontin with kidney function and kidney failure in chronic kidney disease patients: the GCKD study. Nephrol Dial Transplant. 2022:gfac173. DOI:10.1093/ndt/gfac173
27. Riedl E, Pfister F, Braunagel M, et al. Carnosine prevents apoptosis of glomerular cells and podocyte loss in STZ diabetic rats. Cell Physiol Biochem. 2011;28(2):279-88. DOI:10.1159/000331740
2. Rydel JJ, Korbet SM, Borok RZ, Schwartz MM. Focal segmental glomerular sclerosis in adults: presentation, course, and response to treatment. Am J Kidney Dis. 1995;25(4):534-42. DOI:10.1016/0272-6386(95)90120-5
3. Sim JJ, Batech M, Hever A, et al. Distribution of biopsy-proven presumed primary glomerulonephropathies in 2000–2011 among a racially and ethnically diverse US population. Am J Kidney Dis. 2006;68:533-44. DOI:10.1053/j.ajkd.2016.03.416
4. Kitiyakara C, Eggers P, Kopp JB. Twenty-one-year trend in ESRD due to focal segmental glomerulosclerosis in the United States. Am J Kidney Dis. 2004;44(5):815-25. DOI:10.1053/j.ajkd.2004.07.008
5. Coon JJ, Zürbig P, Dakna M, et al. CE-MS analysis of the human urinary proteome for biomarker discovery and disease diagnostics. Proteomics Clin Appl. 2008;2:964-73. DOI:10.1002/prca.200800024
6. Kalantari S, Nafar M, Samavat S, et al. Urinary prognostic biomarkers in patients with focal segmental glomerulosclerosis. Nephrourol Mon. 2014;6(2):e16806. DOI:10.5812/numonthly.16806
7. Pérez V, López D, Boixadera E, et al. Comparative differential proteomic analysis of minimal change disease and focal segmental glomerulosclerosis. BMC Nephrol. 2017;18(1):49. DOI:10.1186/s12882-017-0452-6
8. Medyńska A, Chrzanowska J, Kościelska-Kasprzak K, et al. Alpha-1 Acid Glycoprotein and Podocin mRNA as Novel Biomarkers for Early Glomerular Injury in Obese Children. J Clin Med. 2021;10(18):4129. DOI:10.3390/jcm10184129
9. Christiansen MS, Iversen K, Larsen CT, et al. Increased urinary orosomucoid excretion: A proposed marker for inflammation and endothelial dysfunction in patients with type 2 diabetes. Scand J Clin Lab Investig. 2009;69:272-81. DOI:10.1080/00365510802531100
10. Kalantari S, Nafar M, Rutishauser D, et al. Predictive urinary biomarkers for steroid-resistant and steroid-sensitive focal segmental glomerulosclerosis using high resolution mass spectrometry and multivariate statistical analysis. BMC Nephrol. 2014;15:141. DOI:10.1186/1471-2369-15-141
11. Lingenhel A, Lhotta K, Neyer U, et al. Role of the kidney in the metabolism of apolipoprotein A-IV: influence of the type of proteinuria. J Lipid Res. 2006;47(9):2071-9. DOI:10.1194/jlr.M600178-JLR200
12. Kretzler M. Regulation of adhesive interaction between podocytes and glomerular basement membrane. Microsc Res Tech. 2002;57(4):247-53. DOI:10.1002/jemt.10083
13. Yu CJ, Damaiyanti DW, Yan SJ, et al. The Pathophysiologic Role of Gelsolin in Chronic Kidney Disease: Focus on Podocytes. Int J Mol Sci. 2021;22(24):13281.
DOI:10.3390/ ijms222413281
14. Kapojos JJ, Poelstra K, Borghuis T, et al. Regulation of plasma hemopexin activity by stimulated endothelial or mesangial cells. Nephron Physiol. 2004;96(1):1-10. DOI:10.1159/000075574
15. Pukajło-Marczyk A, Zwolińska D. Involvement of Hemopexin in the Pathogenesis of Proteinuria in Children with Idiopathic Nephrotic Syndrome. J Clin Med. 2021;10(14):3160. DOI:10.3390/jcm10143160
16. Lennon R, Singh A, Welsh GI, et al. Hemopexin induces nephrin-dependent reorganization of the actin cytoskeleton in podocytes. J Am Soc Nephrol. 2008;19(11):2140-9. DOI:10.1681/ASN.2007080940
17. Shen J, Zhu Y, Zhang S, et al. Vitronectin-activated αvβ3 and αvβ5 integrin signalling specifies haematopoietic fate in human pluripotent stem cells. Cell Prolif. 2021;54(4):e13012. DOI:10.1111/cpr.13012
18. Choudhary A, Mohanraj PS, Krishnamurthy S, Rajappa M. Association of Urinary Vitamin D Binding Protein and Neutrophil Gelatinase-Associated Lipocalin with Steroid Responsiveness in Idiopathic Nephrotic Syndrome of Childhood. Saudi J Kidney Dis Transpl. 2020;31(5):946-56. DOI:10.4103/1319-2442.301201
19. Mirković K, Doorenbos CR, Dam WA, et al. Urinary vitamin D binding protein: a potential novel marker of renal interstitial inflammation and fibrosis. PLoS One. 2013;8(2):e55887. DOI:10.1371/journal.pone.0055887
20. Bennett MR, Pordal A, Haffner C, et al. Urinary Vitamin D-Binding Protein as a Biomarker of Steroid-Resistant Nephrotic Syndrome. Biomark Insights. 2016;11:1-6. DOI:10.4137/BMI.S31633
21. Gonzalez-Calero L, Martin-Lorenzo M, Ramos-Barron A, et al. Urinary Kininogen-1 and Retinol binding protein-4 respond to Acute Kidney Injury: predictors of patient prognosis? Sci Rep. 2016;6:19667. DOI:10.1038/srep19667
22. Mastroianni Kirsztajn G, Nishida SK, Silva MS, et al. Urinary retinol-binding protein as a prognostic marker in the treatment of nephrotic syndrome. Nephron. 2000;86(2):109-14. DOI:10.1159/000045727
23. Krishnan A, Li X, Kao WY, Viker K, et al. Lumican, an extracellular matrix proteoglycan, is a novel requisite for hepatic fibrosis. Lab Invest. 2012;92(12):1712-25. DOI:10.1038/labinvest.2012.121
24. Schramek H, Sarközi R, Lauterberg C, et al. Neuropilin-1 and neuropilin-2 are differentially expressed in human proteinuric nephropathies and cytokine-stimulated proximal tubular cells. Lab Invest. 2009;89(11):1304-16. DOI:10.1038/labinvest.2009.96
25. Xie Q, Zhang M, Mao X, et al. Matrix protein Tenascin-C promotes kidney fibrosis via STAT3 activation in response to tubular injury. Cell Death Dis. 2022;13(12):1044. DOI:10.1038/s41419-022-05496-z
26. Steinbrenner I, Sekula P, Kotsis F, el al. Association of osteopontin with kidney function and kidney failure in chronic kidney disease patients: the GCKD study. Nephrol Dial Transplant. 2022:gfac173. DOI:10.1093/ndt/gfac173
27. Riedl E, Pfister F, Braunagel M, et al. Carnosine prevents apoptosis of glomerular cells and podocyte loss in STZ diabetic rats. Cell Physiol Biochem. 2011;28(2):279-88. DOI:10.1159/000331740
2. Rydel JJ, Korbet SM, Borok RZ, Schwartz MM. Focal segmental glomerular sclerosis in adults: presentation, course, and response to treatment. Am J Kidney Dis. 1995;25(4):534-42. DOI:10.1016/0272-6386(95)90120-5
3. Sim JJ, Batech M, Hever A, et al. Distribution of biopsy-proven presumed primary glomerulonephropathies in 2000–2011 among a racially and ethnically diverse US population. Am J Kidney Dis. 2006;68:533-44. DOI:10.1053/j.ajkd.2016.03.416
4. Kitiyakara C, Eggers P, Kopp JB. Twenty-one-year trend in ESRD due to focal segmental glomerulosclerosis in the United States. Am J Kidney Dis. 2004;44(5):815-25. DOI:10.1053/j.ajkd.2004.07.008
5. Coon JJ, Zürbig P, Dakna M, et al. CE-MS analysis of the human urinary proteome for biomarker discovery and disease diagnostics. Proteomics Clin Appl. 2008;2:964-73. DOI:10.1002/prca.200800024
6. Kalantari S, Nafar M, Samavat S, et al. Urinary prognostic biomarkers in patients with focal segmental glomerulosclerosis. Nephrourol Mon. 2014;6(2):e16806. DOI:10.5812/numonthly.16806
7. Pérez V, López D, Boixadera E, et al. Comparative differential proteomic analysis of minimal change disease and focal segmental glomerulosclerosis. BMC Nephrol. 2017;18(1):49. DOI:10.1186/s12882-017-0452-6
8. Medyńska A, Chrzanowska J, Kościelska-Kasprzak K, et al. Alpha-1 Acid Glycoprotein and Podocin mRNA as Novel Biomarkers for Early Glomerular Injury in Obese Children. J Clin Med. 2021;10(18):4129. DOI:10.3390/jcm10184129
9. Christiansen MS, Iversen K, Larsen CT, et al. Increased urinary orosomucoid excretion: A proposed marker for inflammation and endothelial dysfunction in patients with type 2 diabetes. Scand J Clin Lab Investig. 2009;69:272-81. DOI:10.1080/00365510802531100
10. Kalantari S, Nafar M, Rutishauser D, et al. Predictive urinary biomarkers for steroid-resistant and steroid-sensitive focal segmental glomerulosclerosis using high resolution mass spectrometry and multivariate statistical analysis. BMC Nephrol. 2014;15:141. DOI:10.1186/1471-2369-15-141
11. Lingenhel A, Lhotta K, Neyer U, et al. Role of the kidney in the metabolism of apolipoprotein A-IV: influence of the type of proteinuria. J Lipid Res. 2006;47(9):2071-9. DOI:10.1194/jlr.M600178-JLR200
12. Kretzler M. Regulation of adhesive interaction between podocytes and glomerular basement membrane. Microsc Res Tech. 2002;57(4):247-53. DOI:10.1002/jemt.10083
13. Yu CJ, Damaiyanti DW, Yan SJ, et al. The Pathophysiologic Role of Gelsolin in Chronic Kidney Disease: Focus on Podocytes. Int J Mol Sci. 2021;22(24):13281.
DOI:10.3390/ ijms222413281
14. Kapojos JJ, Poelstra K, Borghuis T, et al. Regulation of plasma hemopexin activity by stimulated endothelial or mesangial cells. Nephron Physiol. 2004;96(1):1-10. DOI:10.1159/000075574
15. Pukajło-Marczyk A, Zwolińska D. Involvement of Hemopexin in the Pathogenesis of Proteinuria in Children with Idiopathic Nephrotic Syndrome. J Clin Med. 2021;10(14):3160. DOI:10.3390/jcm10143160
16. Lennon R, Singh A, Welsh GI, et al. Hemopexin induces nephrin-dependent reorganization of the actin cytoskeleton in podocytes. J Am Soc Nephrol. 2008;19(11):2140-9. DOI:10.1681/ASN.2007080940
17. Shen J, Zhu Y, Zhang S, et al. Vitronectin-activated αvβ3 and αvβ5 integrin signalling specifies haematopoietic fate in human pluripotent stem cells. Cell Prolif. 2021;54(4):e13012. DOI:10.1111/cpr.13012
18. Choudhary A, Mohanraj PS, Krishnamurthy S, Rajappa M. Association of Urinary Vitamin D Binding Protein and Neutrophil Gelatinase-Associated Lipocalin with Steroid Responsiveness in Idiopathic Nephrotic Syndrome of Childhood. Saudi J Kidney Dis Transpl. 2020;31(5):946-56. DOI:10.4103/1319-2442.301201
19. Mirković K, Doorenbos CR, Dam WA, et al. Urinary vitamin D binding protein: a potential novel marker of renal interstitial inflammation and fibrosis. PLoS One. 2013;8(2):e55887. DOI:10.1371/journal.pone.0055887
20. Bennett MR, Pordal A, Haffner C, et al. Urinary Vitamin D-Binding Protein as a Biomarker of Steroid-Resistant Nephrotic Syndrome. Biomark Insights. 2016;11:1-6. DOI:10.4137/BMI.S31633
21. Gonzalez-Calero L, Martin-Lorenzo M, Ramos-Barron A, et al. Urinary Kininogen-1 and Retinol binding protein-4 respond to Acute Kidney Injury: predictors of patient prognosis? Sci Rep. 2016;6:19667. DOI:10.1038/srep19667
22. Mastroianni Kirsztajn G, Nishida SK, Silva MS, et al. Urinary retinol-binding protein as a prognostic marker in the treatment of nephrotic syndrome. Nephron. 2000;86(2):109-14. DOI:10.1159/000045727
23. Krishnan A, Li X, Kao WY, Viker K, et al. Lumican, an extracellular matrix proteoglycan, is a novel requisite for hepatic fibrosis. Lab Invest. 2012;92(12):1712-25. DOI:10.1038/labinvest.2012.121
24. Schramek H, Sarközi R, Lauterberg C, et al. Neuropilin-1 and neuropilin-2 are differentially expressed in human proteinuric nephropathies and cytokine-stimulated proximal tubular cells. Lab Invest. 2009;89(11):1304-16. DOI:10.1038/labinvest.2009.96
25. Xie Q, Zhang M, Mao X, et al. Matrix protein Tenascin-C promotes kidney fibrosis via STAT3 activation in response to tubular injury. Cell Death Dis. 2022;13(12):1044. DOI:10.1038/s41419-022-05496-z
26. Steinbrenner I, Sekula P, Kotsis F, el al. Association of osteopontin with kidney function and kidney failure in chronic kidney disease patients: the GCKD study. Nephrol Dial Transplant. 2022:gfac173. DOI:10.1093/ndt/gfac173
27. Riedl E, Pfister F, Braunagel M, et al. Carnosine prevents apoptosis of glomerular cells and podocyte loss in STZ diabetic rats. Cell Physiol Biochem. 2011;28(2):279-88. DOI:10.1159/000331740
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2. Rydel JJ, Korbet SM, Borok RZ, Schwartz MM. Focal segmental glomerular sclerosis in adults: presentation, course, and response to treatment. Am J Kidney Dis. 1995;25(4):534-42. DOI:10.1016/0272-6386(95)90120-5
3. Sim JJ, Batech M, Hever A, et al. Distribution of biopsy-proven presumed primary glomerulonephropathies in 2000–2011 among a racially and ethnically diverse US population. Am J Kidney Dis. 2006;68:533-44. DOI:10.1053/j.ajkd.2016.03.416
4. Kitiyakara C, Eggers P, Kopp JB. Twenty-one-year trend in ESRD due to focal segmental glomerulosclerosis in the United States. Am J Kidney Dis. 2004;44(5):815-25. DOI:10.1053/j.ajkd.2004.07.008
5. Coon JJ, Zürbig P, Dakna M, et al. CE-MS analysis of the human urinary proteome for biomarker discovery and disease diagnostics. Proteomics Clin Appl. 2008;2:964-73. DOI:10.1002/prca.200800024
6. Kalantari S, Nafar M, Samavat S, et al. Urinary prognostic biomarkers in patients with focal segmental glomerulosclerosis. Nephrourol Mon. 2014;6(2):e16806. DOI:10.5812/numonthly.16806
7. Pérez V, López D, Boixadera E, et al. Comparative differential proteomic analysis of minimal change disease and focal segmental glomerulosclerosis. BMC Nephrol. 2017;18(1):49. DOI:10.1186/s12882-017-0452-6
8. Medyńska A, Chrzanowska J, Kościelska-Kasprzak K, et al. Alpha-1 Acid Glycoprotein and Podocin mRNA as Novel Biomarkers for Early Glomerular Injury in Obese Children. J Clin Med. 2021;10(18):4129. DOI:10.3390/jcm10184129
9. Christiansen MS, Iversen K, Larsen CT, et al. Increased urinary orosomucoid excretion: A proposed marker for inflammation and endothelial dysfunction in patients with type 2 diabetes. Scand J Clin Lab Investig. 2009;69:272-81. DOI:10.1080/00365510802531100
10. Kalantari S, Nafar M, Rutishauser D, et al. Predictive urinary biomarkers for steroid-resistant and steroid-sensitive focal segmental glomerulosclerosis using high resolution mass spectrometry and multivariate statistical analysis. BMC Nephrol. 2014;15:141. DOI:10.1186/1471-2369-15-141
11. Lingenhel A, Lhotta K, Neyer U, et al. Role of the kidney in the metabolism of apolipoprotein A-IV: influence of the type of proteinuria. J Lipid Res. 2006;47(9):2071-9. DOI:10.1194/jlr.M600178-JLR200
12. Kretzler M. Regulation of adhesive interaction between podocytes and glomerular basement membrane. Microsc Res Tech. 2002;57(4):247-53. DOI:10.1002/jemt.10083
13. Yu CJ, Damaiyanti DW, Yan SJ, et al. The Pathophysiologic Role of Gelsolin in Chronic Kidney Disease: Focus on Podocytes. Int J Mol Sci. 2021;22(24):13281.
DOI:10.3390/ ijms222413281
14. Kapojos JJ, Poelstra K, Borghuis T, et al. Regulation of plasma hemopexin activity by stimulated endothelial or mesangial cells. Nephron Physiol. 2004;96(1):1-10. DOI:10.1159/000075574
15. Pukajło-Marczyk A, Zwolińska D. Involvement of Hemopexin in the Pathogenesis of Proteinuria in Children with Idiopathic Nephrotic Syndrome. J Clin Med. 2021;10(14):3160. DOI:10.3390/jcm10143160
16. Lennon R, Singh A, Welsh GI, et al. Hemopexin induces nephrin-dependent reorganization of the actin cytoskeleton in podocytes. J Am Soc Nephrol. 2008;19(11):2140-9. DOI:10.1681/ASN.2007080940
17. Shen J, Zhu Y, Zhang S, et al. Vitronectin-activated αvβ3 and αvβ5 integrin signalling specifies haematopoietic fate in human pluripotent stem cells. Cell Prolif. 2021;54(4):e13012. DOI:10.1111/cpr.13012
18. Choudhary A, Mohanraj PS, Krishnamurthy S, Rajappa M. Association of Urinary Vitamin D Binding Protein and Neutrophil Gelatinase-Associated Lipocalin with Steroid Responsiveness in Idiopathic Nephrotic Syndrome of Childhood. Saudi J Kidney Dis Transpl. 2020;31(5):946-56. DOI:10.4103/1319-2442.301201
19. Mirković K, Doorenbos CR, Dam WA, et al. Urinary vitamin D binding protein: a potential novel marker of renal interstitial inflammation and fibrosis. PLoS One. 2013;8(2):e55887. DOI:10.1371/journal.pone.0055887
20. Bennett MR, Pordal A, Haffner C, et al. Urinary Vitamin D-Binding Protein as a Biomarker of Steroid-Resistant Nephrotic Syndrome. Biomark Insights. 2016;11:1-6. DOI:10.4137/BMI.S31633
21. Gonzalez-Calero L, Martin-Lorenzo M, Ramos-Barron A, et al. Urinary Kininogen-1 and Retinol binding protein-4 respond to Acute Kidney Injury: predictors of patient prognosis? Sci Rep. 2016;6:19667. DOI:10.1038/srep19667
22. Mastroianni Kirsztajn G, Nishida SK, Silva MS, et al. Urinary retinol-binding protein as a prognostic marker in the treatment of nephrotic syndrome. Nephron. 2000;86(2):109-14. DOI:10.1159/000045727
23. Krishnan A, Li X, Kao WY, Viker K, et al. Lumican, an extracellular matrix proteoglycan, is a novel requisite for hepatic fibrosis. Lab Invest. 2012;92(12):1712-25. DOI:10.1038/labinvest.2012.121
24. Schramek H, Sarközi R, Lauterberg C, et al. Neuropilin-1 and neuropilin-2 are differentially expressed in human proteinuric nephropathies and cytokine-stimulated proximal tubular cells. Lab Invest. 2009;89(11):1304-16. DOI:10.1038/labinvest.2009.96
25. Xie Q, Zhang M, Mao X, et al. Matrix protein Tenascin-C promotes kidney fibrosis via STAT3 activation in response to tubular injury. Cell Death Dis. 2022;13(12):1044. DOI:10.1038/s41419-022-05496-z
26. Steinbrenner I, Sekula P, Kotsis F, el al. Association of osteopontin with kidney function and kidney failure in chronic kidney disease patients: the GCKD study. Nephrol Dial Transplant. 2022:gfac173. DOI:10.1093/ndt/gfac173
27. Riedl E, Pfister F, Braunagel M, et al. Carnosine prevents apoptosis of glomerular cells and podocyte loss in STZ diabetic rats. Cell Physiol Biochem. 2011;28(2):279-88. DOI:10.1159/000331740
Авторы
А.А. Виноградов*1, Н.В. Чеботарева2, А.Е. Бугрова3, А.Г. Бржозовский4, Т.Н. Краснова1,2, К.З. Насибуллина2, А.С. Кононихин4, С.В. Моисеев2
1 ФГБОУ ВО «Московский государственный университет им. М.В. Ломоносова», Москва, Россия;
2 ФГАОУ ВО «Первый Московский государственный медицинский университет им. И.М. Сеченова» Минздрава России (Сеченовский Университет), Москва, Россия;
3 ФГБУН «Институт биохимической физики им. Н.М. Эмануэля» РАН, Москва, Россия;
4 АНОО ВО «Сколковский институт науки и технологии», Москва, Россия
*anatoliy_vinogradov@list.ru
1 Lomonosov Moscow State University, Moscow, Russia;
2 Sechenov First Moscow State Medical University (Sechenov University), Moscow, Russia;
3 Emanuel Institute for Biochemical Physics, Moscow, Russia;
4 Skolkovo Institute of Science and Technology, Moscow, Russia
*anatoliy_vinogradov@list.ru
1 ФГБОУ ВО «Московский государственный университет им. М.В. Ломоносова», Москва, Россия;
2 ФГАОУ ВО «Первый Московский государственный медицинский университет им. И.М. Сеченова» Минздрава России (Сеченовский Университет), Москва, Россия;
3 ФГБУН «Институт биохимической физики им. Н.М. Эмануэля» РАН, Москва, Россия;
4 АНОО ВО «Сколковский институт науки и технологии», Москва, Россия
*anatoliy_vinogradov@list.ru
________________________________________________
1 Lomonosov Moscow State University, Moscow, Russia;
2 Sechenov First Moscow State Medical University (Sechenov University), Moscow, Russia;
3 Emanuel Institute for Biochemical Physics, Moscow, Russia;
4 Skolkovo Institute of Science and Technology, Moscow, Russia
*anatoliy_vinogradov@list.ru
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