Top

Published in:

Open Access 12-05-2023 | Review

Insights into human kidney function from the study of Drosophila

Authors: Sybille Koehler, Tobias B. Huber

Published in: Pediatric Nephrology | Issue 12/2023

Abstract

Biological and biomedical research using Drosophila melanogaster as a model organism has gained recognition through several Nobel prizes within the last 100 years. Drosophila exhibits several advantages when compared to other in vivo models such as mice and rats, as its life cycle is very short, animal maintenance is easy and inexpensive and a huge variety of transgenic strains and tools are publicly available. Moreover, more than 70% of human disease-causing genes are highly conserved in the fruit fly. Here, we explain the use of Drosophila in nephrology research and describe two kidney tissues, Malpighian tubules and the nephrocytes. The latter are the homologous cells to mammalian glomerular podocytes and helped to provide insights into a variety of signaling pathways due to the high morphological similarities and the conserved molecular make-up between nephrocytes and podocytes. In recent years, nephrocytes have also been used to study inter-organ communication as links between nephrocytes and the heart, the immune system and the muscles have been described. In addition, other tissues such as the eye and the reproductive system can be used to study the functional role of proteins being part of the kidney filtration barrier.

Li H, Janssens J, De Waegeneer M et al (2022) Fly Cell Atlas: a single-nucleus transcriptomic atlas of the adult fruit fly. Science 375:eabk2432. https://doi.org/10.1126/science.abk2432CrossRefPubMedPubMedCentral

Hughes CS, Foehr S, Garfield DA et al (2014) Ultrasensitive proteome analysis using paramagnetic bead technology. Mol Syst Biol 10:757CrossRefPubMed

Wang M, Hu Q, Lv T et al (2022) High-resolution 3D spatiotemporal transcriptomic maps of developing Drosophila embryos and larvae. Dev Cell 57:1271-1283.e4. https://doi.org/10.1016/j.devcel.2022.04.006CrossRefPubMed

Pende M, Becker K, Wanis M et al (2018) High-resolution ultramicroscopy of the developing and adult nervous system in optically cleared Drosophila melanogaster. Nat Commun 9:4731. https://doi.org/10.1038/s41467-018-07192-zCrossRefPubMedPubMedCentral

Ugur B, Chen K, Bellen HJ (2016) Drosophila tools and assays for the study of human diseases. Dis Model Mech 9:235–244. https://doi.org/10.1242/dmm.023762CrossRefPubMedPubMedCentral

Wolf MJ, Rockman HA (2011) Drosophila, Genetic Screens, and Cardiac Function. Circ Res 109:794–806. https://doi.org/10.1161/CIRCRESAHA.111.244897CrossRefPubMedPubMedCentral

Yu L, Daniels JP, Wolf MJ (2013) Vascular and cardiac studies in drosophila. In: Bolli R, Losordo DW, Ardehali H (eds) Manual of Research Techniques in Cardiovascular Medicine. Wiley-Blackwell, Hoboken NJ, pp 432–439

Cammarato A, Ahrens CH, Alayari NN et al (2011) A mighty small heart: the cardiac proteome of adult Drosophila melanogaster. PLoS One 6:e18497. https://doi.org/10.1371/journal.pone.0018497CrossRefPubMedPubMedCentral

Zheng H, Yang X, Xi Y (2016) Fat body remodeling and homeostasis control in Drosophila. Life Sci 167:22–31. https://doi.org/10.1016/j.lfs.2016.10.019CrossRefPubMed

10.

Scheffer LK, Xu CS, Januszewski M et al (2020) A connectome and analysis of the adult Drosophila central brain. eLife 9:e57443. https://doi.org/10.7554/eLife.57443CrossRefPubMedPubMedCentral

11.

Wood W, Jacinto A (2007) Drosophila melanogaster embryonic haemocytes: masters of multitasking. Nat Rev Mol Cell Biol 8:542–551. https://doi.org/10.1038/nrm2202CrossRefPubMed

12.

Denholm B, Sudarsan V, Pasalodos-Sanchez S et al (2003) Dual origin of the renal tubules in Drosophila. Curr Biol 13:1052–1057. https://doi.org/10.1016/S0960-9822(03)00375-0CrossRefPubMed

13.

Weavers H, Skaer H (2013) Tip cells act as dynamic cellular anchors in the morphogenesis of looped renal tubules in Drosophila. Dev Cell 27:331–344. https://doi.org/10.1016/j.devcel.2013.09.020CrossRefPubMedPubMedCentral

14.

Xu J, Liu Y, Li H et al (2022) Transcriptional and functional motifs defining renal function revealed by single-nucleus RNA sequencing. Proc Natl Acad Sci 119:e2203179119. https://doi.org/10.1073/pnas.2203179119CrossRefPubMedPubMedCentral

15.

Rodan AR (2019) The Drosophila Malpighian tubule as a model for mammalian tubule function. Curr Opin Nephrol Hypertens 28:455–464. https://doi.org/10.1097/MNH.0000000000000521CrossRefPubMedPubMedCentral

16.

Denholm B, Hu N, Fauquier T et al (2013) The tiptop / teashirt genes regulate cell differentiation and renal physiology in Drosophila. Development 140:1100–1110. https://doi.org/10.1242/dev.088989CrossRefPubMedPubMedCentral

17.

Beaven R, Denholm B (2022) Early patterning followed by tissue growth establishes proximo-distal identity in Drosophila Malpighian tubules. Front Cell Dev Biol 10:947376CrossRefPubMedPubMedCentral

18.

Beaven R, Denholm B (2018) Release and spread of wingless is required to pattern the proximo-distal axis of Drosophila renal tubules. eLife 7:e35373. https://doi.org/10.7554/eLife.35373CrossRefPubMedPubMedCentral

19.

Saxena A, Denholm B, Bunt S et al (2014) Epidermal growth factor signalling controls myosin II planar polarity to orchestrate convergent extension movements during Drosophila tubulogenesis. PLoS Biol 12:e1002013. https://doi.org/10.1371/journal.pbio.1002013CrossRefPubMedPubMedCentral

20.

Weavers H, Prieto-Sánchez S, Grawe F et al (2009) The insect nephrocyte is a podocyte-like cell with a filtration slit diaphragm. Nature 457:322–326. https://doi.org/10.1038/nature07526CrossRefPubMed

21.

Feng X, Hong X, Fan Q et al (2021) dCubilin- or dAMN-mediated protein reabsorption in Drosophila nephrocytes modulates longevity. Dis Model Mech 14:dmm047464. https://doi.org/10.1242/dmm.047464CrossRefPubMedPubMedCentral

22.

Zhang F, Zhao Y, Chao Y et al (2013) Cubilin and amnionless mediate protein reabsorption in Drosophila nephrocytes. J Am Soc Nephrol 24:209–216. https://doi.org/10.1681/ASN.2012080795CrossRefPubMed

23.

Zhuang S, Shao H, Guo F et al (2009) Sns and Kirre, the Drosophila orthologs of Nephrin and Neph1, direct adhesion, fusion and formation of a slit diaphragm-like structure in insect nephrocytes. Development 136:2335–2344. https://doi.org/10.1242/dev.031609CrossRefPubMedPubMedCentral

24.

Koehler S, Kuczkowski A, Kuehne L et al (2020) Proteome analysis of isolated podocytes reveals stress responses in glomerular sclerosis. J Am Soc Nephrol 31:544–559. https://doi.org/10.1681/ASN.2019030312CrossRefPubMedPubMedCentral

25.

Lang K, Milosavljevic J, Heinkele H et al (2022) Selective endocytosis controls slit diaphragm maintenance and dynamics in Drosophila nephrocytes. eLife 11:e79037. https://doi.org/10.7554/eLife.79037CrossRefPubMedPubMedCentral

26.

Helmstädter M, Lüthy K, Gödel M et al (2012) Functional study of mammalian Neph proteins in Drosophila melanogaster. PloS One 7:e40300. https://doi.org/10.1371/journal.pone.0040300CrossRefPubMedPubMedCentral

27.

Fu Y, Zhu J-Y, Richman A et al (2017) A Drosophila model system to assess the function of human monogenic podocyte mutations that cause nephrotic syndrome. Hum Mol Genet 26:768–780. https://doi.org/10.1093/hmg/ddw428CrossRefPubMedPubMedCentral

28.

Carrasco-Rando M, Prieto-Sánchez S, Culi J et al (2019) A specific isoform of Pyd/ZO-1 mediates junctional remodeling and formation of slit diaphragms. J Cell Biol 218:2294–2308. https://doi.org/10.1083/jcb.201810171CrossRefPubMedPubMedCentral

29.

Tutor AS, Prieto-Sánchez S, Ruiz-Gómez M (2014) Src64B phosphorylates Dumbfounded and regulates slit diaphragm dynamics: Drosophila as a model to study nephropathies. Development 141:367–376. https://doi.org/10.1242/dev.099408CrossRefPubMed

30.

Na J, Sweetwyne MT, Park ASD et al (2015) Diet-induced podocyte dysfunction in drosophila and mammals. Cell Rep 12:636–647. https://doi.org/10.1016/j.celrep.2015.06.056CrossRefPubMedPubMedCentral

31.

Ivy JR, Drechsler M, Catterson JH et al (2015) Klf15 is critical for the development and differentiation of Drosophila nephrocytes. PLoS One 10:e0134620. https://doi.org/10.1371/journal.pone.0134620CrossRefPubMedPubMedCentral

32.

Bierzynska A, Bull K, Miellet S et al (2022) Exploring the relevance of NUP93 variants in steroid-resistant nephrotic syndrome using next generation sequencing and a fly kidney model. Pediatr Nephrol 37:2643–2656. https://doi.org/10.1007/s00467-022-05440-5CrossRefPubMedPubMedCentral

33.

Zhao F, Zhu J, Richman A et al (2019) Mutations in nup160 are implicated in steroid-resistant nephrotic syndrome. J Am Soc Nephrol 30:840–853. https://doi.org/10.1681/ASN.2018080786CrossRefPubMedPubMedCentral

34.

Hochapfel F, Denk L, Mendl G et al (2017) Distinct functions of crumbs regulating slit diaphragms and endocytosis in Drosophila nephrocytes. Cell Mol Life Sci 74:4573–4586. https://doi.org/10.1007/s00018-017-2593-yCrossRefPubMed

35.

Hermle T, Braun DA, Helmstädter M et al (2017) Modeling monogenic human nephrotic syndrome in the drosophila garland cell nephrocyte. J Am Soc Nephrol 28:1521–1533. https://doi.org/10.1681/ASN.2016050517CrossRefPubMed

36.

Odenthal J, Dittrich S, Ludwig V et al (2023) Modeling of ACTN4-based podocytopathy using Drosophila nephrocytes. Kidney Int Rep 8:317–329. https://doi.org/10.1016/j.ekir.2022.10.024CrossRefPubMed

37.

Akilesh S, Suleiman H, Yu H et al (2011) Arhgap24 inactivates Rac1 in mouse podocytes, and a mutant form is associated with familial focal segmental glomerulosclerosis. J Clin Invest 121:4127–4137. https://doi.org/10.1172/JCI46458CrossRefPubMedPubMedCentral

38.

Kopp JB, Smith MW, Nelson GW et al (2008) MYH9 is a major-effect risk gene for focal segmental glomerulosclerosis. Nat Genet 40:1175–1184. https://doi.org/10.1038/ng.226CrossRefPubMedPubMedCentral

39.

Koehler S, Odenthal J, Ludwig V et al (2021) Scaffold polarity proteins Par3A and Par3B share redundant functions while Par3B acts independent of atypical protein kinase C/Par6 in podocytes to maintain the kidney filtration barrier. Kidney Int 101:733–751. https://doi.org/10.1016/j.kint.2021.11.030CrossRefPubMed

40.

Bayraktar S, Nehrig J, Menis E et al (2020) A Deregulated Stress Response Underlies Distinct INF2-Associated Disease Profiles. J Am Soc Nephrol 31:1296–1313. https://doi.org/10.1681/ASN.2019111174CrossRefPubMedPubMedCentral

41.

Lepa C, Möller-Kerutt A, Stölting M et al (2020) LIM and SH3 protein 1 (LASP-1): A novel link between the slit membrane and actin cytoskeleton dynamics in podocytes. FASEB J 34:5453–5464. https://doi.org/10.1096/fj.201901443RCrossRefPubMed

42.

Durand A, Winkler CA, Vince N et al (2023) Identification of novel genetic risk factors for focal segmental glomerulosclerosis in children: results from the Chronic Kidney Disease in Children (CKiD) Cohort. Am J Kidney Dis. https://doi.org/10.1053/j.ajkd.2022.11.003CrossRefPubMed

43.

Heiden S, Siwek R, Lotz M-L et al (2021) Apical-basal polarity regulators are essential for slit diaphragm assembly and endocytosis in Drosophila nephrocytes. Cell Mol Life Sci 78:3657–3672. https://doi.org/10.1007/s00018-021-03769-yCrossRefPubMedPubMedCentral

44.

Mysh M, Poulton JS (2021) The basolateral polarity module promotes slit diaphragm formation in Drosophila nephrocytes, a model of vertebrate Podocytes. J Am Soc Nephrol 32:1409–1424. https://doi.org/10.1681/ASN.2020071050CrossRefPubMedPubMedCentral

45.

Bechtel W, Helmstädter M, Balica J et al (2013) Vps34 deficiency reveals the importance of endocytosis for podocyte homeostasis. J Am Soc Nephrol 24:727–743. https://doi.org/10.1681/ASN.2012070700CrossRefPubMedPubMedCentral

46.

Selma-Soriano E, Llamusi B, Fernández-Costa JM et al (2020) Rabphilin involvement in filtration and molecular uptake in Drosophila nephrocytes suggests a similar role in human podocytes. Dis Model Mech 13:dmm041509. https://doi.org/10.1242/dmm.041509CrossRefPubMedPubMedCentral

47.

Wang L, Wen P, van de Leemput J et al (2021) Slit diaphragm maintenance requires dynamic clathrin-mediated endocytosis facilitated by AP-2, Lap, Aux and Hsc70-4 in nephrocytes. Cell Biosci 11:83. https://doi.org/10.1186/s13578-021-00595-4CrossRefPubMedPubMedCentral

48.

Atienza-Manuel A, Castillo-Mancho V, De Renzis S et al (2021) Endocytosis mediated by an atypical CUBAM complex modulates slit diaphragm dynamics in nephrocytes. Development 148:dev199894. https://doi.org/10.1242/dev.199894CrossRefPubMedPubMedCentral

49.

Yang J, Xu Y, Deng L et al (2022) CUBN gene mutations may cause focal segmental glomerulosclerosis (FSGS) in children. BMC Nephrol 23:15. https://doi.org/10.1186/s12882-021-02654-xCrossRefPubMedPubMedCentral

50.

Fu Y, Zhu J, Zhang F et al (2017) Comprehensive functional analysis of Rab GTPases in Drosophila nephrocytes. Cell Tissue Res 368:615–627. https://doi.org/10.1007/s00441-017-2575-2CrossRefPubMedPubMedCentral

51.

Lakatos Z, Benkő P, Juhász G, Lőrincz P (2021) Drosophila rab39 attenuates lysosomal degradation. Int J Mol Sci 22:10635. https://doi.org/10.3390/ijms221910635CrossRefPubMedPubMedCentral

52.

Hermle T, Schneider R, Schapiro D et al (2018) GAPVD1 and ANKFY1 mutations implicate RAB5 regulation in nephrotic syndrome. J Am Soc Nephrol 29:2123–2138. https://doi.org/10.1681/ASN.2017121312CrossRefPubMedPubMedCentral

53.

Lakatos Z, Lőrincz P, Szabó Z, Benkő P, Kenéz LA, Csizmadia T, Juhász G (2019) Sec20 is required for autophagic and endocytic degradation independent of Golgi-ER retrograde transport. Cells 8:768. https://doi.org/10.3390/cells8080768CrossRefPubMedPubMedCentral

54.

Spitz D, Comas M, Gerstner L et al (2022) mTOR-dependent autophagy regulates slit diaphragm density in podocyte-like Drosophila nephrocytes. Cells 11:2103. https://doi.org/10.3390/cells11132103CrossRefPubMedPubMedCentral

55.

Koehler S, Huber TB, Denholm B (2022) A protective role for Drosophila filamin in nephrocytes via Yorkie mediated hypertrophy. Life Sci Alliance 5:281CrossRef

56.

Hurcombe JA, Hartley P, Lay AC et al (2019) Podocyte GSK3 is an evolutionarily conserved critical regulator of kidney function. Nat Commun 10:403. https://doi.org/10.1038/s41467-018-08235-1CrossRefPubMedPubMedCentral

57.

Schütte-Nütgen K, Edeling M, Mendl G et al (2019) Getting a Notch closer to renal dysfunction: activated Notch suppresses expression of the adaptor protein Disabled-2 in tubular epithelial cells. FASEB J 33:821–832. https://doi.org/10.1096/fj.201800392RRCrossRefPubMed

58.

Koehler S, Edenhofer I, Lindenmeyer M et al (2021) The mechano-sensitive ion channel Piezo mediates Rho activation and actin stress fibre formation in Drosophila nephrocytes. Cell Biology. https://doi.org/10.1101/2021.10.23.465463CrossRef

59.

Gass MM, Borkowsky S, Lotz M-L et al (2022) PI(4,5)P2 controls slit diaphragm formation and endocytosis in Drosophila nephrocytes. Cell Mol Life Sci 79:248. https://doi.org/10.1007/s00018-022-04273-7CrossRefPubMedPubMedCentral

60.

Lovric S, Goncalves S, Gee HY et al (2017) Mutations in sphingosine-1-phosphate lyase cause nephrosis with ichthyosis and adrenal insufficiency. J Clin Invest 127:912–928. https://doi.org/10.1172/JCI89626CrossRefPubMedPubMedCentral

61.

Fu Y, Zhu J, Richman A et al (2017) APOL1-G1 in nephrocytes induces hypertrophy and accelerates cell death. J Am Soc Nephrol 28:1106–1116. https://doi.org/10.1681/ASN.2016050550CrossRefPubMed

62.

Kruzel-Davila E, Shemer R, Ofir A et al (2017) APOL1–mediated cell injury involves disruption of conserved trafficking processes. J Am Soc Nephrol 28:1117–1130. https://doi.org/10.1681/ASN.2016050546CrossRefPubMed

63.

Gerstner L, Chen M, Kampf LL et al (2022) Inhibition of endoplasmic reticulum stress signaling rescues cytotoxicity of human apolipoprotein-L1 risk variants in Drosophila. Kidney Int 101:1216–1231. https://doi.org/10.1016/j.kint.2021.12.031CrossRefPubMedPubMedCentral

64.

Lubojemska A, Stefana MI, Sorge S et al (2021) Adipose triglyceride lipase protects renal cell endocytosis in a Drosophila dietary model of chronic kidney disease. PLoS Biol 19:30. https://doi.org/10.1371/journal.pbio.3001230CrossRef

65.

Marchesin V, Pérez-Martí A, Le Meur G et al (2019) Molecular basis for autosomal-dominant renal fanconi syndrome caused by HNF4A. Cell Rep 29:4407-4421.e5. https://doi.org/10.1016/j.celrep.2019.11.066CrossRefPubMedPubMedCentral

66.

Kampf LL, Schneider R, Gerstner L et al (2019) TBC1D8B mutations implicate RAB11-dependent vesicular trafficking in the pathogenesis of nephrotic syndrome. J Am Soc Nephrol 30:2338–2353. https://doi.org/10.1681/ASN.2019040414CrossRefPubMedPubMedCentral

67.

Milosavljevic J, Lempicki C, Lang K et al (2022) Nephrotic syndrome gene TBC1D8B is required for endosomal maturation and nephrin endocytosis in Drosophila. J Am Soc Nephrol 33:2174–2193. https://doi.org/10.1681/ASN.2022030275CrossRefPubMed

68.

Muraleedharan S, Sam A, Skaer H, Inamdar MS (2018) Networks that link cytoskeletal regulators and diaphragm proteins underpin filtration function in Drosophila nephrocytes. Exp Cell Res 364:234–242. https://doi.org/10.1016/j.yexcr.2018.02.015CrossRefPubMedPubMedCentral

69.

Maywald M-L, Picciotto C, Lepa C et al (2022) Rap1 activity is essential for focal adhesion and slit diaphragm integrity. Front Cell Dev Biol 10:790365. https://doi.org/10.3389/fcell.2022.790365CrossRefPubMedPubMedCentral

70.

Dlugos CP, Picciotto C, Lepa C et al (2019) Nephrin signaling results in integrin β 1 activation. J Am Soc Nephrol 30:1006–1019. https://doi.org/10.1681/ASN.2018040362CrossRefPubMedPubMedCentral

71.

Krausel V, Pund L, Nüsse H et al (2023) The transcription factor ATF4 mediates endoplasmic reticulum stress-related podocyte injury and slit diaphragm defects. Kidney Int 103:872–885. https://doi.org/10.1016/j.kint.2022.11.024CrossRefPubMed

72.

Sivakumar S, Miellet S, Clarke C, Hartley PS (2022) Insect nephrocyte function is regulated by a store operated calcium entry mechanism controlling endocytosis and Amnionless turnover. J Insect Physiol 143:104453. https://doi.org/10.1016/j.jinsphys.2022.104453CrossRefPubMed

73.

Cagan R (2009) Principles of Drosophila eye differentiation. Curr Top Dev Biol 89:115–135. https://doi.org/10.1016/S0070-2153(09)89005-4CrossRefPubMedPubMedCentral

74.

Bao S, Cagan R (2005) Preferential adhesion mediated by Hibris and Roughest regulates morphogenesis and patterning in the Drosophila eye. Dev Cell 8:925–935. https://doi.org/10.1016/j.devcel.2005.03.011CrossRefPubMed

75.

Höhne M, Lorscheider J, von Bardeleben A et al (2011) The BAR domain protein PICK1 regulates cell recognition and morphogenesis by interacting with Neph proteins. Mol Cell Biol 31:3241–3251. https://doi.org/10.1128/MCB.05286-11CrossRefPubMedPubMedCentral

76.

Hayashi T, Carthew RW (2004) Surface mechanics mediate pattern formation in the developing retina. Nature 431:647–652. https://doi.org/10.1038/nature02952CrossRefPubMed

77.

Ramos RG, Igloi GL, Lichte B et al (1993) The irregular chiasm C-roughest locus of Drosophila, which affects axonal projections and programmed cell death, encodes a novel immunoglobulin-like protein. Genes Dev 7:2533–2547. https://doi.org/10.1101/gad.7.12b.2533CrossRefPubMed

78.

Kuckwa J, Fritzen K, Buttgereit D et al (2016) A new level of plasticity: Drosophila smooth-like testes muscles compensate failure of myoblast fusion. Development 143:329–338. https://doi.org/10.1242/dev.126730CrossRefPubMedPubMedCentral

79.

Valer FB, Machado MCR, Silva-Junior RMP, Ramos RGP (2018) Expression of Hbs, Kirre, and Rst during Drosophila ovarian development. Genesis 56:e23242. https://doi.org/10.1002/dvg.23242CrossRefPubMed

80.

Gnanaraj J, Radhakrishnan J (2016) Cardio-renal syndrome. F1000Res 5:F1000. https://doi.org/10.12688/f1000research.8004.1CrossRefPubMedPubMedCentral

81.

Kurts C, Panzer U, Anders H-J, Rees AJ (2013) The immune system and kidney disease: basic concepts and clinical implications. Nat Rev Immunol 13:738–753. https://doi.org/10.1038/nri3523CrossRefPubMed

82.

Solagna F, Tezze C, Lindenmeyer MT et al (2021) Pro-cachectic factors link experimental and human chronic kidney disease to skeletal muscle wasting programs. J Clin Invest 131:135821. https://doi.org/10.1172/JCI135821CrossRef

83.

Bright R (no. II vol. I) Cases and observations, illustrative of renal disease accompanied with the secretion of albuminous urine.

84.

Janani R, Vivek B, Blair John EA et al (2019) Cardiorenal syndrome: classification, pathophysiology, diagnosis, and treatment strategies: a scientific statement from the American Heart Association. Circulation 139:e840–e878. https://doi.org/10.1161/CIR.0000000000000664CrossRef

85.

Jemtel THL, Rajapreyar I, Selby MG et al (2015) Direct evidence of podocyte damage in cardiorenal syndrome type 2: preliminary evidence. Cardiorenal Med 5:125–134. https://doi.org/10.1159/000375130CrossRefPubMedPubMedCentral

86.

Hartley PS, Motamedchaboki K, Bodmer R, Ocorr K (2016) SPARC–dependent cardiomyopathy in Drosophila. Circ Cardiovasc Genet 9:119–129. https://doi.org/10.1161/CIRCGENETICS.115.001254CrossRefPubMedPubMedCentral

87.

Mulderrig L, Garaycoechea JI, Tuong ZK et al (2021) Aldehyde-driven transcriptional stress triggers an anorexic DNA damage response. Nature 600:158–163. https://doi.org/10.1038/s41586-021-04133-7CrossRefPubMed

88.

Troha K, Nagy P, Pivovar A et al (2019) Nephrocytes remove microbiota-derived peptidoglycan from systemic circulation to maintain immune homeostasis. Immunity 51:625-637.e3. https://doi.org/10.1016/j.immuni.2019.08.020CrossRefPubMed

89.

Bier E (2005) Drosophila, the golden bug, emerges as a tool for human genetics. Nat Rev Genet 6:9–23. https://doi.org/10.1038/nrg1503CrossRefPubMed

90.

Verheyen EM (2022) The power of Drosophila in modeling human disease mechanisms. Dis Model Mech 15:dmm049549. https://doi.org/10.1242/dmm.049549CrossRefPubMedPubMedCentral

Title: Insights into human kidney function from the study of Drosophila
Authors: Sybille Koehler
Tobias B. Huber
Publication date: 12-05-2023
Publisher: Springer Berlin Heidelberg
Published in: Pediatric Nephrology / Issue 12/2023
Print ISSN: 0931-041X
Electronic ISSN: 1432-198X
DOI: https://doi.org/10.1007/s00467-023-05996-w

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Insights into human kidney function from the study of Drosophila

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 12/2023

Chronic, severe abdominal pain in a girl with a renal anomaly: Answers

Tubulointerstitial nephritis and uveitis syndrome and SARS-CoV-2 infection in an adolescent: just a coincidence in time?

The efficacy and safety of corticosteroids in pediatric kidney scar prevention after urinary tract infection: a systematic review and meta-analysis of randomized clinical trials

Metabolic acidosis in pediatric kidney transplant recipients

Quality of life in pediatric chronic kidney disease: expectations and responsibilities

Drugs in treating paediatric acute kidney injury