СТРУКТУРА И СВОЙСТВА ГЛОМЕРУЛЯРНОГО ФИЛЬТРА ПОЗВОНОЧНЫХ: РОЛЬ ЗАРЯДА ДЛЯ ФИЛЬТРАЦИИ БЕЛКОВ
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Ключевые слова

гломерулярный фильтр
заряд
гломерулярная базальная мембрана
подоцит
гликозаминогликан
гликокаликс
позвоночные

Аннотация

Почечный клубочек – уникальная структура, отличающая нефроны позвоночных от нефридиев беспозвоночных животных, обеспечивающая непосредственную связь кровеносной и выделительной систем и наиболее эффективный контроль состава внутренней среды за счет значительной интенсификации фильтрации. Рассмотрены современные представления о структуре гломерулярного фильтра у представителей всех основных групп позвоночных животных (круглоротые, рыбы, амфибии, рептилии и птицы, млекопитающие). Сделан акцент на роли заряда структур гломерулярного барьера для его селективных свойств, описаны подходы к изучению вклада анионных компонентов клубочка в предотвращение потери белков плазмы крови. Рассмотрены представленные в литературе основные модели работы гломерулярного фильтра. Продемонстрировано, что отрицательный заряд является отличительной чертой гломерулярного фильтра у всех позвоночных. Показано, что многократный рост скорости клубочковой фильтрации (от низших позвоночных к птицам и млекопитающим) сопровождался рядом структурных изменений, обеспечивающих прохождение значительного объема воды и растворенных низкомолекулярных веществ через гломерулярный фильтр: увеличение числа и упорядоченности фенестр в эндотелии гломерулярных капилляров, утончение гломерулярной базальной мембраны и полное исключение из нее клеточных элементов. Данные проведенного сравнительно-физиологического анализа гломерулярного барьера у разных групп позвоночных в наибольшей степени свидетельствуют о справедливости электрокинетической модели работы фильтра, так как именно она объясняет важность эволюционно консервативной структуры подоцитов и роль совокупности фиксированных отрицательных зарядов в стенке гломерулярного фильтра для предотвращения потери макромолекул (прежде всего белков) из крови при различной интенсивности ультрафильтрации.

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Литература

Natochin YV (2019) Principles of evolution of the excretory organs and the system of homeostasis. J Evol Biochem Phys 55(5): 398–410. s://doi.org/10.1134/S0022093019050077

Наточин ЮВ (2019) Почка: орган выделения или сохранения? Успехи физиологических наук 50(4): 14–25. [Natochin YV (2019) Kidney: excretion or preservation organ? Uspekhi fiziologicheskih nauk 50(4): 14–25. (In Russ)]. s://doi.org/10.1134/S0301179819040064

Yokota SD, Benyajati S, Dantzler WH (1985) Comparative aspects of glomerular filtration in vertebrates. Ren Physiol 8(4-5): 193–221. s://doi.org/10.1159/000173055

Kutina AV, Marina AS, Natochin YV (2016) Effects of exenatide on glycemia and renal water and ion excretion differ in frogs and rats. J Evol Biochem Phys 52(3): 228–237. s://doi.org/10.1134/S0022093016030054

Haraldsson B, Nystrom J, Deen WM (2008) Properties of the glomerular barrier and mechanisms of proteinuria. Physiol Rev 88(2): 451–487. s://doi.org/10.1152/physrev.00055.2006

Jarad G, Miner JH (2009) Update on the glomerular filtration barrier. Curr Opin Nephrol Hypertens 18(3): 226–232. s://doi.org/10.1097/mnh.0b013e3283296044

Riegel JA (1998) Analysis of fluid dynamics in perfused glomeruli of the hagfish eptatretus stouti (Lockington). J Exp Biol 201(Pt 22): 3097–3104. s://doi.org/10.1242/jeb.201.22.3097

Винниченко ЛН (1980) Сравнительная ультраструктура нефрона. Л. Наука. [Vinnichenko LN (1980) Sravnitel'naya ul'trastruktura nefrona [Comparative ultrastructure of the nephron]. L. Nauka. (In Russ)]

Arif E, Nihalani D (2013) Glomerular filtration barrier assembly: an insight. Postdoc J 1(4): 33–45.

Gambaryan SP (1994) Microdissectional investigation of the nephrons in some fishes, amphibians, and reptiles inhabiting different environment. J Morphol 219(3): 319–339. s://doi.org/10.1002/jmor.1052190311

Orosz SE, Echols MS (2020) The urinary and osmoregulatory systems of birds. Vet Clin North Am Exot Anim Pract 23(1): 1–19. s://doi.org/10.1016/j.cvex.2019.09.001

Kuhn K, Stolte H, Reale E (1975) The fine structure of the kidney of the hagfish (Myxine glutinosa L.): A thin section and freeze-fracture study. Cell Tissue Res 164(2): 201–213. s://doi.org/10.1007/BF00218974

Tsuji K, Suleiman H, Miner JH, Daley JM, Capen DE, Paunescu TG, Lu HAJ (2017) Ultrastructural characterization of the glomerulopathy in alport mice by helium ion scanning microscopy (HIM). Sci Rep 7(1): 11696. s://doi.org/10.1038/s41598-017-12064-5

Ballermann BJ, Nystrom J, Haraldsson B (2021) The glomerular endothelium restricts albumin filtration. Front Med (Lausanne) 8: 766689. s://doi.org/10.3389/fmed.2021.766689

Schaffner A, Rodewald R (1978) Glomerular permeability in the bullfrog Rana catesbeiana. J Cell Biol 79(2 Pt 1): 314–328. s://doi.org/10.1083/jcb.79.2.314

Mobjerg N, Jespersen A, Wilkinson M (2004) Morphology of the kidney in the West African caecilian, Geotrypetes seraphini (Amphibia, Gymnophiona, Caeciliidae). J Morphol 262(2): 583–607. s://doi.org/10.1002/jmor.10244

Tanner GA, Rippe C, Shao Y, Evan AP, Williams JC Jr (2009) Glomerular permeability to macromolecules in the Necturus kidney. Am J Physiol Renal Physiol 296(6): F1269–F1278. s://doi.org/10.1152/ajprenal.00371.2007

Gerth VE, Zhou X, Vize PD (2005) Nephrin expression and three-dimensional morphogenesis of the Xenopus pronephric glomus. Dev Dyn 233(3): 1131–1139. s://doi.org/10.1002/dvdy.20415

Mobjerg N, Larsen EH, Jespersen A (2000) Morphology of the kidney in larvae of Bufo viridis (Amphibia, Anura, Bufonidae). J Morphol 245(3): 177–195. s://doi.org/10.1002/1097-4687(200009)245:3<177::AID-JMOR1>3.0.CO;2-F

Xu CS, Yang P, Bao HJ, Bian XG, Chen QS (2013) Ultrastructure of the nephron in the soft-shelled turtle, Pelodiscus sinensis (Reptilia, Chelonia, Trionychidae). Micron 44: 451–462. s://doi.org/10.1016/j.micron.2012.10.00

Tsujii T, Inoue S, Takamiya H, Liszczynsky HR, Naora H, Seno S (1992) Morphology of the kidney of the platypus (Ornithorhynchus anatinus: Monotremata). Anat Rec 234(3): 348–358. s://doi.org/10.1002/ar.1092340306

Satchell S (2013) The role of the glomerular endothelium in albumin handling. Nat Rev Nephrol 9(12): 717–725. https://doi.org/10.1038/nrneph.2013.197

Takahashi-Iwanaga H (2015) Three-dimensional microanatomy of the pericapillary mesangial tissues in the renal glomerulus: Comparative observations in four vertebrate classes. Biomed Res 36(5): 331–341. s://doi.org/10.2220/biomedres.36.331

Squire JM, Chew M, Nneji G, Neal C, Barry J, Michel C (2001) Quasi-periodic substructure in the microvessel endothelial glycocalyx: a possible explanation for molecular filtering? J Struct Biol 136(3): 239–255. s://doi.org/10.1006/jsbi.2002.4441

Jeansson M, Haraldsson B (2006) Morphological and functional evidence for an important role of the endothelial cell glycocalyx in the glomerular barrier. Am J Physiol Renal Physiol. 290(1): F111–F116. s://doi.org/10.1152/ajprenal.00173.2005

Hegermann J, Lunsdorf H, Ochs M, Haller H (2016) Visualization of the glomerular endothelial glycocalyx by electron microscopy using cationic colloidal thorium dioxide. Histochem Cell Biol 145(1): 41–51. s://doi.org/10.1007/s00418-015-1378-3

Fan J, Sun Y, Xia Y, Tarbell JM, Fu BM (2019) Endothelial surface glycocalyx (ESG) components and ultra-structure revealed by stochastic optical reconstruction microscopy (STORM). Biorheology 56(2–3): 77–88. s://doi.org/10.3233/BIR-180204

Muller-Deile J, Gellrich F, Schenk H, Schroder P, Nystrom J, Lorenzen J, Haller H, Schiffer M (2016) Overexpression of TGF-β inducible microRNA-143 in zebrafish leads to impairment of the glomerular filtration barrier by targeting proteoglycans. Cell Physiol Biochem 40(5): 819–830. s://doi.org/10.1159/000453142

Bjornson A, Moses J, Ingemansson A, Haraldsson B, Sorensson J (2005) Primary human glomerular endothelial cells produce proteoglycans, and puromycin affects their posttranslational modification. Am J Physiol Renal Physiol 288(4): F748–F756. s://doi.org/10.1152/ajprenal.00202.2004

Melrose J (2020) Perlecan, a modular instructive proteoglycan with diverse functional properties. Int J Biochem Cell Biol 128: 105849. s://doi.org/10.1016/j.biocel.2020.105849

Jarial MS, Gattone VH, Wilkins JH (2014) Ultrastructural study of the kidney in the coelacanth Latimeria chalumnae (Rhipidistia: Coelacanthini). Zoolog Sci 31(5): 283–291. s://doi.org/10.2108/zs130192

de Ruiter AJ (1980) Changes in glomerular structure after sexual maturation and seawater adaptation in males of the euryhaline teleost Gasterosteus aculeatus L. Cell Tissue Res 206(1): 1–20. s://doi.org/10.1007/BF00233603

Brown JA, Taylor SM, Gray CJ (1983) Glomerular ultrastructure of the trout, Salmo gairdneri. Glomerular capillary epithelium and the effects of environmental salinity. Cell Tissue Res 230(1): 205–218. s://doi.org/10.1007/BF00216040

Ojeda JL, Wong WP, Ip YK, Icardo JM (2008) Renal corpuscle of the african lungfish Protopterus dolloi: structural and histochemical modifications during aestivation. Anat Rec (Hoboken) 291(9): 1156–1172. s://doi.org/10.1002/ar.20729

Reale E, Luciano L, Kühn K, Stolte H, Brod J (1981) Glomerular basement membrane and mesangial matrix: a comparative study in different vertebrates. Ren Physiol 4(2–3): 85–89. s://doi.org/10.1159/000172810

Decker B, Reale E (1991) The glomerular filtration barrier of the kidney in seven vertebrates classes. Comparative morphological and histochemical observations. Eur J Basic Appl Histochem 35(1): 15–36

Pak Poy RK, Robertson JS (1957) Electron microscopy of the avian renal glomerulus. J Biophys Biochem Cytol 3(2): 183–192. s://doi.org/10.1083/jcb.3.2.183

Lacy ER, Castellucci M, Reale E (1987) The elasmobranch renal corpuscle: fine structure of Bowman's capsule and the glomerular capillary wall. Anat Rec 218(3): 294–305. s://doi.org/10.1002/ar.1092180311

Boyd RB, DeVries AL (1983) The seasonal distribution of anionic binding sites in the basement membrane of the kidney glomerulus of the winter flounder Pseudopleuronectes americanus. Cell Tissue Res 234(2): 271–277. s://doi.org/10.1007/BF00213768

Ojeda JL, Icardo JM, Wong WP, Ip YK (2006) Microanatomy and ultrastructure of the kidney of the African lungfish Protopterus dolloi. Anat Rec A Discov Mol Cell Evol Biol 288(6): 609–625. s://doi.org/10.1002/ar.a.20333

Seliverstova EV, Prutskova NP (2017) Tubular protein uptake pattern in the frog model (Rana temporaria): The effect of previous protein loading. J Evol Biochem Physiol 53(3): 215–224. s://doi.org/10.1134/S0022093017030061

Флерова ЕА, Чуйко ГМ (2021) Сравнительная характеристика ультраструктуры клеток нефрона некоторых видов пелагических, придонных и донных рыб (бухта Карантинная, Чёрное море). Морской биологический журнал 6(2)6: 95–109. [Flerova EA, Chuyko GM (2021) Comparative characteristics of the ultrastructure of nephron cells in some species of pelagic, epibenthic, and demersal fish (the Karantinnaya bay, the Black Sea). Morskoj biologicheskij zhurnal 6(2)6: 95–109. (In Russ)]. s://doi.org/10.21072/mbj.2021.06.2.07

Elger M, Hentschel H (1981) The glomerulus of a stenohaline fresh-water teleost, Carassius auratus gibelio, adapted to saline water. A scanning and transmission electron-microscopic study. Cell Tissue Res 220(1): 73–85. s://doi.org/10.1007/BF00209967

Naylor RW, Morais MRPT, Lennon R (2021) Complexities of the glomerular basement membrane. Nat Rev Nephrol 17(2): 112–127. s://doi.org/10.1038/s41581-020-0329-y

Suh JH, Miner JH (2013) The glomerular basement membrane as a barrier to albumin. Nat Rev Nephrol 9(8): 470–477. s://doi.org/10.1038/nrneph.2013.109

Marshall CB (2016) Rethinking glomerular basement membrane thickening in diabetic nephropathy: adaptive or pathogenic? Am J Physiol Renal Physiol 311(5): F831–F843. s://doi.org/10.1152/ajprenal.00313.2016

Suleiman H, Zhang L, Roth R, Heuser JE, Miner JH, Shaw AS, Dani A (2013) Nanoscale protein architecture of the kidney glomerular basement membrane. eLife. 2: e01149. s://doi.org/10.7554/eLife.01149

Abrahamson DR (2012) Role of the podocyte (and glomerular endothelium) in building the GBM. Semin Nephrol 32(4): 342–349. s://doi.org/10.1016/j.semnephrol.2012.06.005

Bersie-Larson LM, Gyoneva L, Goodman DJ, Dorfman KD, Segal Y, Barocas VH (2020) Glomerular filtration and podocyte tensional homeostasis: importance of the minor type IV collagen network. Biomech Model Mechanobiol 19(6): 2433–2442. s://doi.org/10.1007/s10237-020-01347-y

Harvey SJ, Miner JH (2008) Revisiting the glomerular charge barrier in the molecular era. Curr Opin Nephrol Hypertens 17(4): 393–398. s://doi.org/10.1097/MNH.0b013e32830464de

Takahashi-Iwanaga H (2002) Comparative anatomy of the podocyte: A scanning electron microscopic study. Microsc Res Tech 57(4): 196–202. s://doi.org/10.1002/jemt.10073

Ichimura K, Miyazaki N, Sadayama S, Murata K, Koike M, Nakamura K, Ohta K, Sakai T (2015) Three-dimensional architecture of podocytes revealed by block-face scanning electron microscopy. Sci Rep 5: 8993. s://doi.org/10.1038/srep08993

Burghardt T, Hochapfel F, Salecker B, Meese C, Gröne HJ, Rachel R, Wanner G, Krahn MP, Witzgall R (2015) Advanced electron microscopic techniques provide a deeper insight into the peculiar features of podocytes. Am J Physiol Renal Physiol 309(12): F1082–F1089. s://doi.org/10.1152/ajprenal.00338.2015

Garg P (2018) A Review of Podocyte Biology. Am J Nephrol 47(Suppl 1): 3–13. s://doi.org/10.1159/000481633

Qu C, Roth R, Puapatanakul P, Loitman C, Hammad D, Genin GM, Miner JH, Suleiman HY (2022) Three-dimensional visualization of the podocyte actin network using integrated membrane extraction, electron microscopy, and machine learning. J Am Soc Nephrol 33(1): 155–173. s://doi.org/10.1681/ASN.2021020182

Bjornson Granqvist A, Ebefors K, Saleem MA, Mathieson PW, Haraldsson B, Nystrom JS (2006) Podocyte proteoglycan synthesis is involved in the development of nephrotic syndrome. Am J Physiol Renal Physiol 291(4): F722–F730. s://doi.org/10.1152/ajprenal.00433.2005

Salmon AH, Neal CR, Harper SJ (2009) New aspects of glomerular filtration barrier structure and function: five layers (at least) not three. Curr Opin Nephrol Hypertens 18(3): 197–205. s://doi.org/10.1097/MNH.0b013e328329f837

Janes DN, Braun EJ (1997) Urinary protein excretion in red jungle fowl (Gallus gallus). Comp Biochem Physiol a Physiol 118: 1273–1275.

Kramer-Zucker AG, Wiessner S, Jensen AM, Drummond IA (2005) Organization of the pronephric filtration apparatus in zebrafish requires Nephrin, Podocin and the FERM domain protein Mosaic eyes. Dev Biol 285(2): 316–329. s://doi.org/10.1016/j.ydbio.2005.06.038

Miner JH (2012) Life without nephrin: it's for the birds. J Am Soc Nephrol 23(3): 369–371. s://doi.org/10.1681/ASN.2012010016

Yaoita E, Nishimura H, Nameta M, Yoshida Y, Takimoto H, Fujinaka H, Kawachi H, Magdeldin S, Zhang Y, Xu B, Oyama T, Nakamura F, Yamamoto T (2016) Avian podocytes, which lack nephrin, use adherens junction proteins at intercellular junctions. J Histochem Cytochem 64(1): 67–76. s://doi.org/10.1369/0022155415611708

Lovell PV, Wirthlin M, Wilhelm L, Minx P, Lazar NH, Carbone L, Warren WC, Mello CV (2014) Conserved syntenic clusters of protein coding genes are missing in birds. Genome Biol 15(12): 565. s://doi.org/10.1186/s13059-014-0565-1

Becherucci F, Mazzinghi B, Provenzano A, Murer L, Giglio S, Romagnani P (2016) Lessons from genetics: is it time to revise the therapeutic approach to children with steroid-resistant nephrotic syndrome? J Nephrol 29(4): 543–550. s://doi.org/10.1007/s40620-016-0315-4

Wunderlich LCS, Strohl F, Strohl S, Vanderpoorten O, Mascheroni L, Kaminski CF (2021) Superresolving the kidney - a practical comparison of fluorescence nanoscopy of the glomerular filtration barrier. Anal Bioanal Chem 413(4): 1203–1214. s://doi.org/10.1007/s00216-020-03084-8

Roselli S, Gribouval O, Boute N, Sich M, Benessy F, Attie T, Gubler MC, Antignac C (2002) Podocin localizes in the kidney to the slit diaphragm area. Am J Pathol 160(1): 131–139. s://doi.org/10.1016/S0002-9440(10)64357-X

Haraldsson B, Sorensson J (2004) Why do we not all have proteinuria? An update of our current understanding of the glomerular barrier. News Physiol Sci 19: 7–10. s://doi.org/10.1152/nips.01461.2003

Tsujii T, Naito I, Ukita S, Ono T, Seno S (1984) The anionic barrier system in the mesonephric renal glomerulus of the arctic lamprey, Entosphenus japonicus (Martens) (Cyclostomata). Cell Tissue Res 235(3): 491–496. s://doi.org/10.1007/BF00226944

Tsujii T, Naito I, Ukita S, Ono T, Seno S (1984) The anionic barrier system on the mesonephric renal glomerulus of the brown hagfish, Paramyxine atami Dean (Cylostomi). Anat Rec 208(3): 337–347. s://doi.org/10.1002/ar.1092080304

Ellis LC, Youson JH (1991) The anionic charge barrier in the renal corpuscle of the pronephros in the lamprey, Petromyzon marinus L. Anat Rec 231(2): 178–184. s://doi.org/10.1002/ar.1092310205

Khalil R, Lalai RA, Wiweger MI, Avramut CM, Koster AJ, Spaink HP, Bruijn JA, Hogendoorn PCW, Baelde HJ (2019) Glomerular permeability is not affected by heparan sulfate glycosaminoglycan deficiency in zebrafish embryos. Am J Physiol Renal Physiol 317(5): F1211–F1216. s://doi.org/10.1152/ajprenal.00126.2019

More NK (1977) Mucopolysaccharide heterogeneity of the reptilian kidney basement membranes. Acta Histochem 60(2): 173–179. s://doi.org/10.1016/S0065-1281(77)80002-0

van den Hoven MJ, Wijnhoven TJ, Li JP, Zcharia E, Dijkman HB, Wismans RG, Rops AL, Lensen JF, van den Heuvel LP, van Kuppevelt TH, Vlodavsky I, Berden JH, van der Vlag J (2008) Reduction of anionic sites in the glomerular basement membrane by heparanase does not lead to proteinuria. Kidney Int 73(3): 278–287. s://doi.org/10.1038/sj.ki.5002706

Friden V, Oveland E, Tenstad O, Ebefors K, Nystrom J, Nilsson UA, Haraldsson B (2011) The glomerular endothelial cell coat is essential for glomerular filtration. Kidney Int. 79(12): 1322–1330. s://doi.org/10.1038/ki.2011.58

van den Born J, van den Heuvel LP, Bakker MA, Veerkamp JH, Assmann KJ, Berden JH (1992) A monoclonal antibody against GBM heparan sulfate induces an acute selective proteinuria in rats. Kidney Int 41(1): 115–123 s://doi.org/10.1038/ki.1992.15

Gil N, Goldberg R, Neuman T, Garsen M, Zcharia E, Rubinstein AM, van Kuppevelt T, Meirovitz A, Pisano C, Li JP, van der Vlag J, Vlodavsky I, Elkin M (2012) Heparanase is essential for the development of diabetic nephropathy in mice. Diabetes. 61(1): 208–216. s://doi.org/10.2337/db11–1024

Schenk H, Masseli A, Schroder P, Bolanos-Palmieri P, Beese M, Hegermann J, Brasen JH, Haller H (2019) Sulfatases, in particular Sulf1, are important for the integrity of the glomerular filtration barrier in zebrafish. Biomed Res Int 2019: 4508048. s://doi.org/10.1155/2019/4508048

Betteridge KB, Arkill KP, Neal CR, Harper SJ, Foster RR, Satchell SC, Bates DO, Salmon AHJ (2017) Sialic acids regulate microvessel permeability, revealed by novel in vivo studies of endothelial glycocalyx structure and function. J Physiol 595(15): 5015–5035. s://doi.org/10.1113/JP274167

Song K, Fu J, Song J, Herzog BH, Bergstrom K, Kondo Y, McDaniel JM, McGee S, Silasi-Mansat R, Lupu F, Chen H, Bagavant H, Xia L (2017) Loss of mucin-type O-glycans impairs the integrity of the glomerular filtration barrier in the mouse kidney. J Biol Chem 292(40): 16491–16497. s://doi.org/10.1074/jbc.M117.798512

Weinhold B, Sellmeier M, Schaper W, Blume L, Philippens B, Kats E, Bernard U, Galuska SP, Geyer H, Geyer R, Worthmann K, Schiffer M, Groos S, Gerardy-Schahn R, Munster-Kuhnel AK (2012) Deficits in sialylation impair podocyte maturation. J Am Soc Nephrol 23(8): 1319–1328. s://doi.org/10.1681/ASN.2011090947

Nieuwdorp M, Mooij HL, Kroon J, Atasever B, Spaan JA, Ince C, Holleman F, Diamant M, Heine RJ, Hoekstra JB, Kastelein JJ, Stroes ES, Vink H (2006) Endothelial glycocalyx damage coincides with microalbuminuria in type 1 diabetes. Diabetes. 55(4): 1127–1132. s://doi.org/10.2337/diabetes.55.04.06.db05-1619

Vehaskari VM, Root ER, Germuth FG Jr, Robson AM (1982) Glomerular charge and urinary protein excretion: effects of systemic and intrarenal polycation infusion in the rat. Kidney Int 22(2): 127–135. s://doi.org/10.1038/ki.1982.144

Kutina AV, Zakharov VV, Shahmatova EI, Natochin YV (2010) L-NAME-induced heavy proteinuria in healthy rats. Dokl Biol Sci 430(1): 26–28. s://doi.org/10.1134/s0012496610010096

Kutina AV, Shakhmatova EI, Natochin YV (2011) Effect of a blocker of nitric oxide production on albumin excretion by rat kidney. Bull Exp Biol Med 150(6): 693–695. s://doi.org/10.1007/s10517-011-1225-z

Bolton GR, Deen WM, Daniels BS (1998) Assessment of the charge selectivity of glomerular basement membrane using Ficoll sulfate. Am J Physiol 274(5): F889–F896. s://doi.org/10.1152/ajprenal.1998.274.5.F889

Salmon AH, Ferguson JK, Burford JL, Gevorgyan H, Nakano D, Harper SJ, Bates DO, Peti-Peterdi J (2012) Loss of the endothelial glycocalyx links albuminuria and vascular dysfunction. J Am Soc Nephrol 23(8): 1339–1350. s://doi.org/10.1681/ASN.2012010017

Kuwabara A, Satoh M, Tomita N, Sasaki T, Kashihara N (2010) Deterioration of glomerular endothelial surface layer induced by oxidative stress is implicated in altered permeability of macromolecules in Zucker fatty rats. Diabetologia 53(9): 2056–2065. s://doi.org/10.1007/s00125-010-1810-0

Jeansson M, Granqvist AB, Nystrom JS, Haraldsson B (2006) Functional and molecular alterations of the glomerular barrier in long-term diabetes in mice. Diabetologia 49(9): 2200–2209. s://doi.org/10.1007/s00125-006-0319-z

Jeansson M, Bjorck K, Tenstad O, Haraldsson B (2009) Adriamycin alters glomerular endothelium to induce proteinuria. J Am Soc Nephrol 20(1): 114–122. s://doi.org/10.1681/ASN.2007111205

van den Berg BM, Wang G, Boels MGS, Avramut MC, Jansen E, Sol WMPJ, Lebrin F, van Zonneveld AJ, de Koning EJP, Vink H, Grone HJ, Carmeliet P, van der Vlag J, Rabelink TJ (2019) Glomerular Function and Structural Integrity Depend on Hyaluronan Synthesis by Glomerular Endothelium. J Am Soc Nephrol 30(10): 1886–1897. s://doi.org/10.1681/ASN.2019020192

Aoki S, Saito-Hakoda A, Yoshikawa T, Shimizu K, Kisu K, Suzuki S, Takagi K, Mizumoto S, Yamada S, van Kuppevelt TH, Yokoyama A, Matsusaka T, Sato H, Ito S, Sugawara A (2018) The reduction of heparan sulphate in the glomerular basement membrane does not augment urinary albumin excretion. Nephrol Dial Transplant 33(1): 26–33. s://doi.org/10.1093/ndt/gfx218

Goldberg S, Harvey SJ, Cunningham J, Tryggvason K, Miner JH (2009) Glomerular filtration is normal in the absence of both agrin and perlecan-heparan sulfate from the glomerular basement membrane. Nephrol Dial Transplant 24(7): 2044–2051. s://doi.org/10.1093/ndt/gfn758

Harvey SJ, Jarad G, Cunningham J, Rops AL, van der Vlag J, Berden JH, Moeller MJ, Holzman LB, Burgess RW, Miner JH (2007) Disruption of glomerular basement membrane charge through podocyte-specific mutation of agrin does not alter glomerular permselectivity. Am J Pathol 171(1): 139–152. s://doi.org/10.2353/ajpath.2007.061116

Chen S, Wassenhove-McCarthy DJ, Yamaguchi Y, Holzman LB, van Kuppevelt TH, Jenniskens GJ, Wijnhoven TJ, Woods AC, McCarthy KJ (2008) Loss of heparan sulfate glycosaminoglycan assembly in podocytes does not lead to proteinuria. Kidney Int 74(3): 289–299. s://doi.org/10.1038/ki.2008.159

Sugar T, Wassenhove-McCarthy DJ, Esko JD, van Kuppevelt TH, Holzman L, McCarthy KJ (2014) Podocyte-specific deletion of NDST1, a key enzyme in the sulfation of heparan sulfate glycosaminoglycans, leads to abnormalities in podocyte organization in vivo. Kidney Int 85(2): 307–318. s://doi.org/10.1038/ki.2013.281

Rossi M, Morita H, Sormunen R, Airenne S, Kreivi M, Wang L, Fukai N, Olsen BR, Tryggvason K, Soininen R (2003) Heparan sulfate chains of perlecan are indispensable in the lens capsule but not in the kidney. EMBO J 22(2): 236–245. s://doi.org/10.1093/emboj/cdg019

van Det NF, van den Born J, Tamsma JT, Verhagen NA, Berden JH, Bruijn JA, Daha MR, van der Woude FJ (1996) Effects of high glucose on the production of heparan sulfate proteoglycan by mesangial and epithelial cells. Kidney Int 49(4): 1079–1089. s://doi.org/10.1038/ki.1996.157

Singh A, Satchell SC, Neal CR, McKenzie EA, Tooke JE, Mathieson PW (2007) Glomerular endothelial glycocalyx constitutes a barrier to protein permeability. J Am Soc Nephrol 18(11): 2885–2893. s://doi.org/10.1681/ASN.2007010119

Moeller MJ, Tenten V (2013) Renal albumin filtration: alternative models to the standard physical barriers. Nat Rev Nephrol 9(5): 266–277. s://doi.org/10.1038/nrneph.2013.58

Oberg CM, Groszek JJ, Roy S, Fissell WH, Rippe B (2018) A distributed solute model: an extended two-pore model with application to the glomerular sieving of Ficoll. Am J Physiol Renal Physiol 314(6): F1108–F1116. s://doi.org/10.1152/ajprenal.00066.2017

Ohlson M, Sorensson J, Haraldsson B (2001) A gel-membrane model of glomerular charge and size selectivity in series. Am J Physiol Renal Physiol 280(3): F396–F405. s://doi.org/10.1152/ajprenal.2001.280.3.F396

Smithies O (2003) Why the kidney glomerulus does not clog: a gel permeation/diffusion hypothesis of renal function. Proc Natl Acad Sci USA 100(7): 4108–4113. s://doi.org/10.1073/pnas.0730776100

Wolgast M, Persson AE (2011) The gel hypothesis applied to the rat renal capillary membranes: a review. Acta Physiol (Oxf) 202(4): 617–628. s://doi.org/10.1111/j.1748-1716.2011.02277.x

Fissell WH, Miner JH (2018) What Is the Glomerular Ultrafiltration Barrier? J Am Soc Nephrol 29(9): 2262–2264. s://doi.org/10.1681/ASN.2018050490

Xu Z, Yue P, Feng JJ (2023) Poroelastic modelling reveals the cooperation between two mechanisms for albuminuria. J R Soc Interface 20(198): 20220634. s://doi.org/10.1098/rsif.2022.0634

Butt L, Unnersjo-Jess D, Hohne M, Edwards A, Binz-Lotter J, Reilly D, Hahnfeldt R, Ziegler V, Fremter K, Rinschen MM, Helmstadter M, Ebert LK, Castrop H, Hackl MJ, Walz G, Brinkkoetter PT, Liebau MC, Tory K, Hoyer PF, Beck BB, Brismar H, Blom H, Schermer B, Benzing T (2020) A molecular mechanism explaining albuminuria in kidney disease. Nat Metab 2(5): 461–474. s://doi.org/10.1038/s42255-020-0204-y

Hausmann R, Grepl M, Knecht V, Moeller MJ (2012) The glomerular filtration barrier function: new concepts. Curr Opin Nephrol Hypertens 21(4): 441–449. s://doi.org/10.1097/MNH.0b013e328354a28e

Drummond IA, Davidson AJ (2010) Zebrafish kidney development. Methods Cell Biol 100: 233–260. s://doi.org/10.1016/B978-0-12-384892-5.00009-8

Zhu X, Chen Z, Zeng C, Wang L, Xu F, Hou Q, Liu Z (2016) Ultrastructural characterization of the pronephric glomerulus development in zebrafish. J Morphol 277(8): 1104–1112. s://doi.org/10.1002/jmor.20560

Endlich N, Simon O, Gopferich A, Wegner H, Moeller MJ, Rumpel E, Kotb AM, Endlich K (2014) Two-photon microscopy reveals stationary podocytes in living zebrafish larvae. J Am Soc Nephrol 25(4): 681–686. s://doi.org/10.1681/ASN.2013020178

Kourpa A, Schulz A, Mangelsen E, Kaiser-Graf D, Koppers N, Stoll M, Rothe M, Bader M, Purfürst B, Kunz S, Gladytz T, Niendorf T, Bachmann S, Mutig K, Bolbrinker J, Panakova D, Kreutz R (2023) Studies in zebrafish and rat models support dual blockade of EP2 and EP4 (prostaglandin E2 receptors type 2 and 4) for renoprotection in glomerular hyperfiltration and albuminuria. Hypertension 80(4): 771–782. s://doi.org/10.1161/HYPERTENSIONAHA.122.20392

Wiggenhauser LM, Metzger L, Bennewitz K, Soleymani S, Boger M, Tabler CT, Hausser I, Sticht C, Wohlfart P, Volk N, Heidenreich E, Buettner M, Hammes HP, Kroll J (2022) Pdx1 knockout leads to a diabetic nephropathy-like phenotype in zebrafish and identifies phosphatidylethanolamine as metabolite promoting early diabetic kidney damage. Diabetes 71(5): 1073–1080. s://doi.org/10.2337/db21-0645

Zeitler EM, Jennette JC, Flythe JE, Falk RJ, Poulton JS (2022) High-calorie diet results in reversible obesity-related glomerulopathy in adult zebrafish regardless of dietary fat. Am J Physiol Renal Physiol 322(5): F527–F539. s://doi.org/10.1152/ajprenal.00018.2022

Fukuyo Y, Nakamura T, Bubenshchikova E, Powell R, Tsuji T, Janknecht R, Obara T (2014) Nephrin and Podocin functions are highly conserved between the zebrafish pronephros and mammalian metanephrosMol Med Rep 9(2): 457–465. s://doi.org/10.3892/mmr.2013.1844

Hanke N, King BL, Vaske B, Haller H, Schiffer M (2015) A Fluorescence-based assay for proteinuria screening in larval zebrafish (Danio rerio). Zebrafish 12(5): 372–376. s://doi.org/10.1089/zeb.2015.1093

Rider SA, Bruton FA, Collins RG, Conway BR, Mullins JJ (2018) The Efficacy of puromycin and adriamycin for induction of glomerular failure in larval zebrafish validated by an assay of glomerular permeability dynamics. Zebrafish 15(3): 234–242. s://doi.org/10.1089/zeb.2017.1527

Kotb AM, Muller T, Xie J, Anand-Apte B, Endlich K, Endlich N (2014) Simultaneous assessment of glomerular filtration and barrier function in live zebrafish. Am J Physiol Renal Physiol 307(12): F1427–F1434. s://doi.org/10.1152/ajprenal.00029.2014

Siegerist F, Zhou W, Endlich K, Endlich N (2017) 4D in vivo imaging of glomerular barrier function in a zebrafish podocyte injury model. Acta Physiol (Oxf) 220(1): 167–173. s://doi.org/10.1111/apha.12754

Schindler M, Blumenthal A, Moeller MJ, Endlich K, Endlich N (2020) Adriamycin does not damage podocytes of zebrafish larvae. PLoS One 15(11): e0242436. s://doi.org/10.1371/journal.pone.0242436

Kolatsi-Joannou M, Osborn D (2020) A Technique for studying glomerular filtration integrity in the zebrafish pronephros. Methods Mol Biol 2067: 25–39. s://doi.org/10.1007/978-1-4939-9841-8_3

Sopel N, Muller-Deile J (2023) Zebrafish model to study podocyte function within the glomerular filtration barrier. Methods Mol Biol 2664: 145–157. s://doi.org/10.1007/978-1-0716-3179-9_11