Skip to main content
SpringerLink
Log in
Book cover

Kidney Development and Disease pp 3–25Cite as

Drosophila Malpighian Tubules: A Model for Understanding Kidney Development, Function, and Disease

Part of the Results and Problems in Cell Differentiation book series (RESULTS,volume 60)

Abstract

The Malpighian tubules of insects are structurally simple but functionally important organs, and their integrity is important for the normal excretory process. They are functional analogs of human kidneys which are important physiological organs as they maintain water and electrolyte balance in the blood and simultaneously help the body to get rid of waste and toxic products after various metabolic activities. In addition, it receives early indications of insults to the body such as immune challenge and other toxic components and is essential for sustaining life. According to National Vital Statistics Reports 2016, renal dysfunction has been ranked as the ninth most abundant cause of death in the USA. This chapter provides detailed descriptions of Drosophila Malpighian tubule development, physiology, immune function and also presents evidences that Malpighian tubules can be used as a model organ system to address the fundamental questions in developmental and functional disorders of the kidney.

This is a preview of subscription content, access via your institution.

References

  • Agarwal SK, Gupta A (2008) Aquaporins: the renal water channels. Indian J Nephrol 18(3):95–100

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ainsworth C et al (2000) Coordinating cell fate and morphogenesis in Drosophila renal tubules. Philos Trans R Soc Lond 355:931–937

    CAS  Google Scholar 

  • Allam R et al (2012) Histones from dying renal cells aggravate kidney injury via TLR2 and TLR4. J Am Soc Nephrol 23(8):1375–1388

    CAS  PubMed  PubMed Central  Google Scholar 

  • Arikyants N et al (2007) Xanthinuria type I: a rare cause of urolithiasis. Pediatr Nephrol 22:310–314

    PubMed  Google Scholar 

  • Aronson PS, Sacktor B (1975) The Na+ gradient-dependent transport of D-glucose in renal brush border membranes. J Biol Chem 250:6032–6039

    CAS  PubMed  Google Scholar 

  • Artero RD et al (2001) The immunoglobulin-like protein Hibris functions as a dose-dependent regulator of myoblast fusion and is differentially controlled by Ras and Notch signaling. Development 128:4251–4264

    CAS  PubMed  Google Scholar 

  • Bagga HS et al (2013) New insights into the pathogenesis of renal calculi. Urol Clin North Am 40:1–12

    PubMed  Google Scholar 

  • Balda MS, Matter K (1998) Tight junctions. J Cell Sci 111:541–547

    CAS  PubMed  Google Scholar 

  • Betz B, Conway B (2016) An update on the use of animal models in diabetic nephropathy research. Curr Diab Rep 16:18

    PubMed  PubMed Central  Google Scholar 

  • Beyenbach KW et al (2010) The developmental, molecular, and transport biology of Malpighian tubules. Annu Rev Entomol 55:351–374

    CAS  PubMed  Google Scholar 

  • Bonse A (1967) Studies on the chemical nature and formation of the urinary conglomerate in the Malpighian vessels of the rosy mutant of Drosophila melanogaster. Z Naturforsch B 22:1027–1029

    CAS  PubMed  Google Scholar 

  • Breljak D et al (2016) Distribution of organic anion transporters NaDC3 and OAT1-3 along the human nephron. Am J Physiol Renal Physiol 311(1):F227–F238

    CAS  PubMed  Google Scholar 

  • Browne A, O’Donnell MJ (2016) Segment-specific Ca2+ transport by isolated Malpighian tubules of Drosophila melanogaster: a comparison of larval and adult stages. J Insect Physiol (in press)

    Google Scholar 

  • Bulet P, Stocklin R, Menin L (2004) Anti-microbial peptides: from invertebrates to vertebrates. Immunol Rev 198:169–184

    CAS  PubMed  Google Scholar 

  • Cabrero P et al (2002) The Dh gene of Drosophila melanogaster encodes a diuretic peptide that acts through cyclic AMP. J Exp Biol 205:3799–3807

    CAS  PubMed  Google Scholar 

  • Cannell E et al (2016) The corticotrophin releasing factor like diuretic hormone 44 (DH44) and kinin neuropeptides modulate desiccation and starvation tolerance in Drosophila melanogaster. Peptides 9781(16):30020–30021 (S0196)

    Google Scholar 

  • Cantaluppi V et al (2015) Endothelial progenitor cell-derived extracellular vesicles protect from complement-mediated mesangial injury in experimental anti-Thy1.1 glomerulonephritis. Nephrol Dial Transplant 30(3):410–422

    CAS  PubMed  Google Scholar 

  • Centers for Disease Control and Prevention (2014) National diabetes statistics report: estimates of diabetes and its Burden in the United States, 2014. U.S. Department of Health and Human Services, Atlanta, GA

    Google Scholar 

  • Chen et al (2011) Ethylene glycol induces calcium oxalate crystal deposition in Malpighian tubules: a Drosophila model for nephrolithiasis/urolithiasis. Kidney Int 80:369–377

    CAS  PubMed  Google Scholar 

  • Cherbas L et al (2003) EcR isoforms in Drosophila: testing tissue-specific requirements by targeted blockade and rescue. Development 130:271–284

    CAS  PubMed  Google Scholar 

  • Chi T et al (2015) A Drosophila model identifies a critical role for zinc in mineralization for kidney stone disease. PLoS One 10(5):e0124150

    PubMed  PubMed Central  Google Scholar 

  • Chintapalli VR et al (2007) Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat Genet 39:715–720

    CAS  PubMed  Google Scholar 

  • Cho E, Dressler G (2003) Formation and development of nephrons. In: Vize P, Woolf A, Bard J (eds) The kidney: from normal development to congenital disease. Academic, San Diego, pp 195–210

    Google Scholar 

  • Coast GM et al (2001) The Drosophila melanogaster homologue of an insect calcitonin-like diuretic peptide stimulates V-ATPase activity in fruit fly Malpighian tubules. J Exp Biol 204:1795–1804

    CAS  PubMed  Google Scholar 

  • Costanzo LS (1984) Comparison of calcium and sodium transport in early and late rat distal tubules: effect of amiloride. Am J Phys 246:F937–F945

    CAS  Google Scholar 

  • Curthoys NP, Moe OW (2014) Proximal tubule function and response to acidosis. Clin J Am Soc Nephrol 9(9):1627–1638

    CAS  PubMed  Google Scholar 

  • Davies SA, Dow JA (2009) Modulation of epithelial innate immunity by autocrine production of nitric oxide. Gen Comp Endocrinol 162(1):113–121

    CAS  PubMed  Google Scholar 

  • Davies MB et al (2005) Phenotypic analysis of EcR-A mutants suggests that EcR isoforms have unique functions during Drosophila development. Dev Biol 282:385–396

    Google Scholar 

  • Davies SA et al (2012) Immune and stress response ‘cross-talk’ in the Drosophila Malpighian tubule. J Insect Physiol 58(4):488–497

    CAS  PubMed  Google Scholar 

  • Day JP et al (2008) Identification of two partners from the bacterial Kef exchanger family for the apical plasma membrane VATPase of Metazoa. J Cell Sci 121:2612–2619

    CAS  PubMed  Google Scholar 

  • Delanoue R et al (2016) Drosophila insulin release is triggered by adipose Stunted ligand to brain Methuselah receptor. Science 353(6307):1553–1556

    CAS  PubMed  Google Scholar 

  • Denholm B et al (2003) Dual origin of the renal tubules in Drosophila: mesodermal cells integrate and polarize to establish secretory function. Curr Biol 13:1052–1057

    CAS  PubMed  Google Scholar 

  • Denholm B et al (2013) The tiptop/teashirt genes regulate cell differentiation and renal physiology in Drosophila. Development 40(5):1100–1110

    Google Scholar 

  • Dorwart MR et al (2008) The solute carrier 26 family of proteins in epithelial ion transport. Physiology 23:104

    CAS  PubMed  Google Scholar 

  • Dow JAT (2009) Insights into the Malpighian tubule from functional genomics. J Exp Biol 212:435–445

    CAS  PubMed  Google Scholar 

  • Dow JAT, Davies SA (2003) Integrative physiology and functional genomics of epithelial function in a genetic model organism. Physiol Rev 83:687–729

    CAS  PubMed  Google Scholar 

  • Dow JAT, Romero MF (2010) Drosophila provides rapid modeling of renal development, function, and disease. Am J Physiol Renal Physiol 299(6):F1237–F1244

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dow JAT et al (1994) The Malpighian tubules of Drosophila melanogaster, a novel phenotype for studies of fluid secretion and its control. J Exp Biol 197:421–428

    CAS  PubMed  Google Scholar 

  • Dube KA, McDonald DG, O’Donnell MJ (2000) Calcium transport by isolated anterior and posterior Malpighian tubules of Drosophila melanogaster, roles of sequestration and secretion. J Insect Physiol 46:1449–1460

    CAS  PubMed  Google Scholar 

  • Dworak HA, Sink H (2002) Myoblast fusion in Drosophila. Bioessays 24:591–601

    CAS  PubMed  Google Scholar 

  • Dworak HA et al (2001) Characterization of Drosophila hibris, a gene related to human nephrin. Development 128:4265–4276

    CAS  PubMed  Google Scholar 

  • Erickson MRS et al (1997) Drosophila myoblast city encodes a conserved protein that is essential for myoblast fusion, dorsal closure, and cytoskeletal organization. J Cell Biol 138(3):589–603

    CAS  PubMed  PubMed Central  Google Scholar 

  • Francois V et al (1994) Dorsal-ventral patterning of the Drosophila embryo depends on a putative negative growth factor encoded by the short gastrulation gene. Genes Dev 8:2602–2616

    CAS  PubMed  Google Scholar 

  • Frei R et al (2010) MHC class II molecules enhance toll-like receptor mediated innate immune responses. PLoS One 5(1):e8808

    PubMed  PubMed Central  Google Scholar 

  • Galletta BJ et al (1999) Identification of a Drosophila homologue to vertebrate Crk by interaction with MBC. Gene 228(1–2):243–252

    CAS  PubMed  Google Scholar 

  • Ganz T (2003) Microbiology: Gut defence. Nature 422(6931):478–479

    CAS  PubMed  Google Scholar 

  • Garayoa M et al (1994) Myoendocrine-like cells in invertebrates: occurrence of noncardiac striated secretory-like myocytes in the gut of the ant Formica polyctena. Gen Comp Endocrinol 95:133–142

    CAS  PubMed  Google Scholar 

  • Gaul U, Weigel D (1990) Regulation of kruppel expression in the anlage of the Malpighian tubules in Drosophila embryo. Mech Dev 33:57–67

    CAS  PubMed  Google Scholar 

  • Gautam N (2012) Studies on the role of ecdysone signaling in development and function of Malpighian tubules of Drosophila melanogaster. PhD Thesis, Banaras Hindu University, Varanasi

    Google Scholar 

  • Gautam NK, Tapadia MG (2010) Ecdysone signaling is required for proper organization and fluid secretion of stellate cells in the Malpighian tubules of Drosophila melanogaster. Int J Dev Biol 54(4):635–642

    CAS  PubMed  Google Scholar 

  • Gautam NK et al (2015) Ecdysone regulates morphogenesis and function of Malpighian tubules in Drosophila melanogaster through EcR-B2isoform. Dev Bio 398:163–176

    CAS  Google Scholar 

  • Gee et al (2015) KANK deficiency leads to podocyte dysfunction and nephrotic syndrome. J Clin Invest 125(6):2375–2384

    PubMed  PubMed Central  Google Scholar 

  • Gumbiner BM (1996) Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 84:345–357

    CAS  PubMed  Google Scholar 

  • Harbeck R, Lengyel J (1995) Genes controlling posterior gut development in the Drosophila embryo. Roux’s Arch Dev Biol 204:308–329

    Google Scholar 

  • Harbecke R, Janning W (1989) The segmentation gene Kruppel of Drosophila melanogasterhas homeotic properties. Genes Dev 3:114–122

    CAS  PubMed  Google Scholar 

  • Heron M (2016) Deaths: leading causes for 2013. Natl Vital Stat Rep 65:11

    Google Scholar 

  • Hirata T et al (2012) In vivo Drosophila genetic model for calcium oxalate nephrolithiasis. Am J Physiol Renal Physiol 303(11):F1555–F1562

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ho AW, Wong CK, Lam CW (2008) Tumor necrosis factor-alpha up-regulates the expression of CCL2 and adhesion molecules of human proximal tubular epithelial cells through MAPK signaling pathways. Immunobiology 213(7):533–544

    CAS  PubMed  Google Scholar 

  • Hoch M, Pankratz M (1996) Control of gut development by fork head and cell signaling molecules in Drosophila. Mech Dev 58:3–14

    CAS  PubMed  Google Scholar 

  • Hoch M et al (1994) Sequential fates in a single cell are established by the neurogenic cascade in the Malpighian tubules of Drosophila. Development 120:3439–3450

    CAS  PubMed  Google Scholar 

  • Hultmark D (2003) Drosophila immunity: paths and patterns. Curr Opin Immunol 15:12–19

    CAS  PubMed  Google Scholar 

  • Imig JD, Ryan MJ (2013) Immune and inflammatory role in renal disease. Compr Physiol 3(2):957–976

    PubMed  PubMed Central  Google Scholar 

  • Imler JL, Bulet P (2005) Antimicrobial peptides in Drosophila: structures, activities and gene regulation. Chem Immunol Allergy 86:1–21

    CAS  PubMed  Google Scholar 

  • Jacinto AML et al (2013) Urine concentrations of xanthine, hypoxanthine and uric acid in UK Cavalier King Charles spaniels. J Small Anim Pract 54:395–398

    CAS  PubMed  Google Scholar 

  • Janning W et al (1986) Clonal analysis of the blastoderm anlage of the Malpighain tubules in Drosophila melanogaster. Roux’s Arch Dev Biol 195:22–32

    Google Scholar 

  • Jha MK et al (2009) Defective survival of naive CD8+ T lymphocytes in the absence of the beta3 regulatory subunit of voltage-gated calcium channels. Nat Immunol 10:1275–1282

    CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson EC et al (2005) A novel diuetic hormone receptor in Drosophila: evidence for conservation of CGRP signaling. J Exp Biol 208:1239–1246

    CAS  PubMed  Google Scholar 

  • Jung CA et al (2005) Renal tubule development in Drosophila: a closer look at cellular level. J Am Soc Nephrol. 16:322–328

    CAS  PubMed  Google Scholar 

  • Kaufmann N et al (2005) Developmental expression and biophysical characterization of a Drosophila melanogaster aquaporin. Am J Physiol Cell Physiol 289:397–407

    Google Scholar 

  • Kean L et al (2002) Two nitridergic peptides are encoded by the gene capability in Drosophila melanogaster. Am J Physiol Regul Integr Comp Physiol 282:1297–1307

    Google Scholar 

  • Kerber B et al (1998) Seven-up, the Drosophila homolog of the COUP-TF orphan receptors, controls cell proliferation in the insect kidney. Genes Dev 12:1781–1786

    CAS  PubMed  PubMed Central  Google Scholar 

  • Khoshnoodi J, Tryggvason K (2001) Congenital nephritic syndromes. Curr Opin Genet Dev 11:322–327

    CAS  PubMed  Google Scholar 

  • Kim HS et al (2011) VAB-10 spectraplakin acts in cell and nuclear migration in Caenorhabditis elegans. Development 138:4013–4023

    CAS  PubMed  PubMed Central  Google Scholar 

  • King LS et al (2001) Defective urinary-concentrating ability due to a complete deficiency of aquaporin-1. N Engl J Med 345:175–179

    CAS  PubMed  Google Scholar 

  • Kirsch K et al (1999) CMS: an adapter molecule involved in cytoskeletal rearrangements. Proc Natl Acad Sci 96:6211–6216

    CAS  PubMed  Google Scholar 

  • Knier CG et al (2016) Bicaudal-C in Drosophila as a model of polycystic kidney disease (PKD) and intersection of oxalate nephrolithiasis FASEB J 30: Sup 1224.27

    Google Scholar 

  • Koelle MR et al (1991) The Drosophila EcR gene encodes an ecdysone receptor, a new member of the steroid receptor super family. Cell 67:59–77

    CAS  PubMed  Google Scholar 

  • Landry GM et al (2016) Sulfate and thiosulfate inhibit oxalate transport via a dPrestin (Slc26a6)-dependent mechanism in an insect model of calcium oxalate nephrolithiasis. Am J Physiol Renal Physiol 310(2):152–159

    Google Scholar 

  • Lanier LM, Gertler FB (2000) From Abl to actin: Abl tyrosine kinase and associated proteins in growth cone motility. Curr Opin Neurobiol 10:80–87

    CAS  PubMed  Google Scholar 

  • Lebovitz RM et al (1989) Molecular characterization and expression of the (Na+/K+)-ATPase-sub unit in Drosophila melanogaster. EMBO 8:193–202

    CAS  Google Scholar 

  • Lehmann R (1995) Cell-cell signaling, microtubules, and the loss of symmetry in the Drosophila oocyte. Cell 83:353–356

    CAS  PubMed  Google Scholar 

  • Lekven AC et al (1998) Faint sausage encode a novel extracellular protein of the immunoglobulin superfamily required for cell migration and the establishment of normal axonal pathways in the Drosophila nervous system. Development 125:2747–2758

    CAS  PubMed  Google Scholar 

  • Lemaitre B, Hoffmann J (2007) The host defense of Drosophila melanogaster. Annu Rev Immunol 25:697–743

    CAS  PubMed  Google Scholar 

  • Lemaitre B et al (1995) A recessive mutation, immune deficiency (imd), defines two distinct control pathways in the Drosophila host defense. Proc Natl Acad Sci USA 92(21):9465–9469

    CAS  PubMed  Google Scholar 

  • Li et al (2014) Further, differential Notch activity is required for homeostasis of Malpighian tubules in adult Drosophila. J Genet Genomics 41:649–652

    PubMed  Google Scholar 

  • Li et al (2015) EGFR/MAPK signaling regulates the proliferation of Drosophila renal and nephric stem cells. J Genet Genomics 42:9e20

    Google Scholar 

  • Liu X et al (1999) Identification of genes controlling malpighian tubule and other epithelial morphogenesis in Drosophila melanogaster. Genetics 151:685–695

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lothar HH (2009) Significance of zinc-related signaling pathways in immune cells. Annu Rev Nutr 29:133–152

    Google Scholar 

  • Maddrell, O’Donnell (1992) Insect Malpighian tubules: V-ATPase action in ion and fluid transport. J Exp Biol 172(1):417–429

    CAS  PubMed  Google Scholar 

  • Maddrell SHP et al (1991) 5-hydroxytryptamine: a second diuretic hormone in Rhodniusprolixus. J Exp Biol 156:557–566

    CAS  PubMed  Google Scholar 

  • Mathieson PW (2003) Immune dysregulation in minimal change nephropathy. Nephrol Dial Transplant 18(Suppl 6):vi26–vi29

    CAS  PubMed  Google Scholar 

  • McGettigan J et al (2005) Insect renal tubules constitute a cell-autonomous immune system that protects the organism against bacterial infection. Insect Biochem Mol Biol 35(7):741–754

    CAS  PubMed  Google Scholar 

  • Miller J et al (2013) Drosophila melanogaster as an emerging translational model of human nephrolithiasis. J Urol 190(5):1648–1656

    PubMed  Google Scholar 

  • Mitchison TJ, Cramer LP (1996) Actin-based cell motility and cell locomotion. Cell 9:371–379

    Google Scholar 

  • Morris SNS et al (2012) Development of diet-induced insulin resistance in adult Drosophila melanogaster. Biochim Biophys Acta 1822:1230–1237

    CAS  PubMed  PubMed Central  Google Scholar 

  • Musselman LP et al (2011) A high-sugar diet produces obesity and insulin resistance in wild-type Drosophila. Dis Model Mech 4(6):842–849

    CAS  PubMed  PubMed Central  Google Scholar 

  • Na J, Cagan RL (2013) The Drosophila nephrocyte: back on stage. J Am Soc Nephrol 24:161–163

    CAS  PubMed  Google Scholar 

  • Na et al (2015) Diet-induced podocyte dysfunction in Drosophila and Mammals. Cell Rep 12(4):636–647

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nakhoul NL, Hamm LL (2002) Vacuolar H(+)-ATPase in the kidney. J Nephrol (Suppl 5):S22–S31

    Google Scholar 

  • Nielsen S et al (1993) CHIP28 water channels are localized in constitutively water-permeable segments of the nephron. J Cell Biol 120:371–383

    CAS  PubMed  Google Scholar 

  • Nolan KM et al (1998) Myoblast city, the Drosophila homolog of DOCK180/CED-5, is required in a Rac signaling pathway utilized for multiple developmental processes. Genes Dev 12:3337–3342

    CAS  PubMed  PubMed Central  Google Scholar 

  • O’Donnell, Maddrell (1995) Fluid reabsorption and ion transport by the lower Malpighian tubules of adult female Drosophila. J Exp Biol 198:1647–1653

    PubMed  Google Scholar 

  • Oro AE et al (1990) Relationship between the product of Dosophila ultra spiracle locus and vertebrate retinoid X receptor. Nature 347:298–301

    CAS  PubMed  Google Scholar 

  • Overend G et al (2012) The receptor guanylate cyclase Gyc76C and a peptide ligand, NPLP1-VQQ, modulate the innate immune IMD pathway in response to salt stress. Peptides 34(1):209–218

    CAS  PubMed  Google Scholar 

  • Palmer LG, Schnermann J (2015) Integrated control of Na transport along the nephron. Clinical J Am Soc Nephrol 10(4):676–687

    CAS  Google Scholar 

  • Pannabecke’r T (1995) Physiology of the Malpighian tubules. Annu Rev Entomol 40:493–510

    Google Scholar 

  • Pavenstadt H, Kriz W, Kretzler M (2003) Cell biology of the glomerular podocyte. Physiol Rev 83(1):253–307

    CAS  PubMed  Google Scholar 

  • Pendse J et al (2013) A Drosophila functional evaluation of candidates from human genome-wide association studies of type 2 diabetes and related metabolic traits identifies tissue-specific roles for dHHEX. BMC Genomics 14:136–147

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pruyne D, Bretscher A (2000) Polarization of cell growth in yeast. I Establishment and maintenance of polarity states. J Cell Sci 113:365–375

    CAS  PubMed  Google Scholar 

  • Pütz M et al (2005) In Drosophila melanogaster, the rolling pebbles isoform 6 (Rols6) is essential for proper Malpighian tubule morphology. Mech Dev 122:1206–1217

    PubMed  Google Scholar 

  • Rheault MR, O’Donnell MJ (2001) Analysis of K+ transport in Malpighian tubules of Drosophila melanogaster: evidence for spatial and temporal heterogeneity. J Exp Biol 204:2289–2299

    CAS  PubMed  Google Scholar 

  • Rheault MR, O’Donnell MJ (2004) Organic cation transport by Malpighian tubules of Drosophila melanogaster: application of two novel electrophysiological methods. J Exp Biol 207:2173–2184

    CAS  PubMed  Google Scholar 

  • Robinson SW et al (2013) FlyAtlas: database of gene expression in the tissues of Drosophila melanogaster. Nucleic Acids Res 41(Database issue):D744–D750

    CAS  PubMed  Google Scholar 

  • Roy A, Al-bataineh MM, Pastor-Soler NM (2015) Collecting duct intercalated cell function and regulation. Clin J Am Soc Nephrol 10(2):305–324

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rulifson EJ et al (2002) Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes. Science 296:1118–1120

    CAS  PubMed  Google Scholar 

  • Sands JM, Layton HE (2009) The physiology of urinary concentration: an update. Semin Nephrol 29(3):178–195

    CAS  PubMed  PubMed Central  Google Scholar 

  • Saxena L (1987) Organogenesis of the kidney. Cambridge University Press, Cambridge

    Google Scholar 

  • Schubiger M et al (1998) Drosophila EcR-B ecdysone receptor isoforms required for larval molting and for neuron remodling during metamorphosis. Development 125:2053–2062

    CAS  PubMed  Google Scholar 

  • Silverman N, Maniatis T (2001) NF-kappa B signaling pathways in mammalian and insect innate immunity. Genes Dev 15(18):2321–2342

    CAS  PubMed  Google Scholar 

  • Sindić A et al (2007) Renal physiology of SLC26 anion exchangers. Curr Opin Nephrol Hypertens 16:484

    PubMed  Google Scholar 

  • Singh SR et al (2007) The adult Drosophila Malpighian tubule are maintained by pluripotent stem cells. Cell Stem Cell 16:191–203

    Google Scholar 

  • Skaer H (1989) Cell division in Malpighian tubule development in D. melanogaster is regulated by a single tip cell. Nature 342:566–569

    Google Scholar 

  • Skaer H (1993) The alimentary canal. In: Bate M, Arias AM (eds) Development of Drosophila melanogaster. Cold Spring Harbor Laboratory Press, Plain view, pp 941–1012

    Google Scholar 

  • Skaer H, Martinez A (1992) The wingless product is required for cell proliferation in the Malpighian tubules anlage of Drosophila melanogaster. Development 116:745–754

    CAS  Google Scholar 

  • Sözen MA et al (1997) Functional domains are specified to single-cell resolution in a Drosophila epithelium. Proc Natl Acad Sci USA 94(10):5207–5212

    PubMed  Google Scholar 

  • Stergiopoulos K et al (2009) Salty dog, an SLC5 symporter, modulates Drosophila response to salt stress. Physiol Genomics 37(1):1–11

    CAS  PubMed  Google Scholar 

  • Sullivan W, Theurkauf WE (1995) The cytoskeleton and morphogenesis of the early Drosophila embryo. Curr Opin Cell Biol 7:18–22

    CAS  PubMed  Google Scholar 

  • Syed KH et al (2012) Proximal renal tubular acidosis: a not so rare disorder of multiple etiologies. Nephrol Dial Transplant 27(12):4273–4287

    Google Scholar 

  • Talbot WS et al (1993) Drosophila tissues with different metamorphic responses to ecdysone express different ecdysone receptor isoforms. Cell 73(7):1323–1337

    CAS  PubMed  Google Scholar 

  • Tanji T, Ip YT (2005) Regulators of the Toll and Imd pathways in the Drosophila innate immune response. Trends Immunol 26(4):193–198

    CAS  PubMed  Google Scholar 

  • Tepass U (1996) Crumbs, a component of the apical membrane, is required for zonula adherens formation in primary epithelia of Drosophila. Dev Biol 177:217–225

    CAS  PubMed  Google Scholar 

  • Tepass U (1997) Epithelial differentiation in Drosophila. Bioessays 19:673–682

    CAS  PubMed  Google Scholar 

  • Tepass U, Hartenstein V (1994) The development of cellular junctions in the Drosophila embryo. Dev Biol 161:563–596

    CAS  PubMed  Google Scholar 

  • Terhzaz S et al (2010) Mislocalization of mitochondria and compromised renal function and oxidative stress resistance in Drosophila SesB mutants. Physiol Genomics 41(1):33–41

    CAS  PubMed  Google Scholar 

  • Thomas HE et al (1993) Heterodimerization of Drosophila ecdysone receptor with retinoid X receptor and ultra spiracle. Nature 362:471–475

    CAS  PubMed  Google Scholar 

  • Tossi A, Sandi L et al (2002) Molecular diversity in gene-encoded, cationic antimicrobial polypeptides. Curr Pharm Des 8(9):743–761

    CAS  PubMed  Google Scholar 

  • Trinh I, Boulianne GL (2013) Modeling obesity and its associated disorders in Drosophila. Physiology 28:117–124

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tzou P et al (2000) Tissue-specific inducible expression of antimicrobial peptide genes in Drosophila surface epithelia. Immunity 13(5):737–748

    CAS  PubMed  Google Scholar 

  • Van Kooten C et al (2000) Immunological function of tubular epithelial cells: the functional implications of CD40 expression. Exp Nephrol 8(4-5):203–207

    CAS  PubMed  Google Scholar 

  • Vasioukhin V et al (2000) Directed actin polymerization is the driving force for epithelial cell-cell adhesion. Cell 21:209–219

    Google Scholar 

  • Verma P, Tapadia MG (2012) Immune response and anti-microbial peptides expression in Malpighian tubules of Drosophila melanogaster is under developmental regulation. PLoS One 7(7):e40714

    PubMed  PubMed Central  Google Scholar 

  • Verma P, Tapadia MG (2014) Epithelial immune response in Drosophila malpighian tubules: interplay between Diap2 and ion channels. J Cell Physiol 229(8):1078–1095

    CAS  PubMed  Google Scholar 

  • Verma P, Tapadia MG (2015) Early gene broad complex plays a key role in regulating the immune response triggered by ecdysone in the Malpighian tubules of Drosophila melanogaster. Mol Immunol 66(2):325–339

    CAS  PubMed  Google Scholar 

  • Wan S et al (2000) Multiple signalling pathways establish cell fate and cell number inDrosophila Malpighian tubules. Dev Biol 217:153–165

    CAS  PubMed  Google Scholar 

  • Wang T et al (2001) Role of NHE isoforms in mediating bicarbonate reabsorption along the nephron. Am J Physiol 281:F1117–F1122

    CAS  Google Scholar 

  • Wang J et al (2004) Function-informed transcriptome analysis of Drosophila renal tubule. Genome Biol 5:R6

    Google Scholar 

  • Weavers H, Skaer H (2013) Tip cells act as dynamic cellular anchors in the morphogenesis of looped renal tubules in Drosophila. Dev Cell 27(3):331–344

    CAS  PubMed  PubMed Central  Google Scholar 

  • Weavers H et al (2009) The insect nephrocyte is a podocyte-like cell with a filtration slit diaphragm. Nature 15:322–326

    Google Scholar 

  • Weigel D et al (1989) Primordeum specific requirement of the homeotic gene fork head in the developing gut of the Drosophila embryo. Roux’s Arch Dev Biol 98:201–210

    Google Scholar 

  • Wessing A et al (1992) Two types of concretions in Drosophila Malpighian tubules as revealed by X-ray microanalysis: a study on urine formation. J Insect Physiol 38:543–554

    CAS  Google Scholar 

  • Wodarz A et al (1993) Crumbs is involved in the control of apical protein targeting during Drosophila epithelial development. Mech Dev 44:175–187

    CAS  PubMed  Google Scholar 

  • Wodarz et al (1995) Expression of crumbs confers apical character on plasma membrane domains of ectodermal epithelia of Drosophila. Cell 82:67–76

    CAS  PubMed  Google Scholar 

  • Woolf A, Bard J (eds) (2003) The kidney: from normal development to congenital disease. Academic Press, San Diego, pp. 165–179

    Google Scholar 

  • Wu L, Langyel J (1998) Role of caudal in hind gut specification and gastrulation suggests homology between Drosophila amnoproctodeal invagination and vertebrate blastopore. Development 125:2433–2442

    CAS  PubMed  Google Scholar 

  • Wu et al (2014) An emerging translational model to screen potential medicinal plants for nephrolithiasis, an independent risk factor for chronic kidney disease. Evid Based Complement Alternat Med. eID 972958:1–7

    Google Scholar 

  • Wu Y et al (2015) Two inwardly rectifying potassium channels, Irk1 and Irk2, play redundant roles in Drosophila renal tubule function. Am J Physiol Regul Integr Comp Physiol. 309(7):R747–R756

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yadav S, Tapadia MG (2016) Expression of polyQ aggregates in Malpighian tubules leads to degeneration in Drosophila melanogaster. Dev Biol 409(1):166–180

    CAS  PubMed  Google Scholar 

  • Yao TP et al (1992) Drosophila ultraspiracle modulates ecdysone receptor function via heterodimer formation. Cell 71:63–72

    CAS  PubMed  Google Scholar 

  • Yap AS et al (1997) Molecular and functional analysis of cadherin-based adherens junction. Annu Rev Cell Dev Biol 13:9119–9146

    Google Scholar 

  • Zeng X et al (2010) Tumor suppressors Sav/Scrib and oncogene Ras regulate stem-cell transformation in adult Drosophila malpighian tubules. J Cell Physiol 224(3):766–774

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang B et al (2008) TLR4 signaling mediates inflammation and tissue injury in nephrotoxicity. J Am Soc Nephrol. 19(5):923–932

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Embryotoxicology Laboratory, Environmental Toxicology Division, CSIR-Indian Institute of Toxicology Research (CSIR-IITR), Vishvigyan Bhavan, 31, Mahatma Gandhi Marg, Lucknow, 226001, Uttar Pradesh, India

    Naveen Kumar Gautam

  2. Department of Zoology, Cytogenetics Laboratory, Banaras Hindu University, Varanasi, 221005, Uttar Pradesh, India

    Puja Verma & Madhu G. Tapadia

Authors
  1. Naveen Kumar Gautam
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Puja Verma
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Madhu G. Tapadia
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Madhu G. Tapadia .

Editor information

Editors and Affiliations

  1. Department of Pediatrics, The University of Texas Health Science Center at Houston, Houston, TX, USA

    Ph.D. Rachel K. Miller

Rights and permissions

Reprints and Permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Gautam, N.K., Verma, P., Tapadia, M.G. (2017). Drosophila Malpighian Tubules: A Model for Understanding Kidney Development, Function, and Disease. In: Miller, R. (eds) Kidney Development and Disease. Results and Problems in Cell Differentiation, vol 60. Springer, Cham. https://doi.org/10.1007/978-3-319-51436-9_1

Download citation

search

Navigation