Shaping up for action: The path to physiological maturation in the renal tubules of Drosophila

Organogenesis

Volumn 9, Issue 1, 2013, Pages 40-54

  Denholm, Barry ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Convergent extension; Drosophila; Insect excretory system; Malpighian tubule; Morphogenesis; Organogenesis; Physiological differentiation; Renal tubule; Tubulogenesis

Indexed keywords

KRUPPEL LIKE FACTOR; MYOSIN II; PROTEIN CDC42; RAC PROTEIN; RHO FACTOR; SYNAPTOPHYSIN; SYNAPTOTAGMIN; TRANSCRIPTION FACTOR GAL4; TRANSCRIPTION FACTOR ONECUT;

APICAL MEMBRANE; BASOLATERAL MEMBRANE; CELL DIFFERENTIATION; CELL FUNCTION; CELL JUNCTION; CELL LINEAGE; CELL SHAPE; CELLULAR DISTRIBUTION; CYTOSKELETON; DROSOPHILA; EMBRYO DEVELOPMENT; ENDOREDUPLICATION; EXTRACELLULAR MATRIX; GENE EXPRESSION; GENE INACTIVATION; GENE SILENCING; HEMOLYMPH; KIDNEY TUBULE; LARVAL STAGE; MALPIGHIAN TUBULE; MESODERM; NONHUMAN; NOTOCHORD; OSMOREGULATION; PRIMORDIUM; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; STELLATE CELL; TRANSCRIPTION INITIATION; ANIMAL; CONVERGENT-EXTENSION; DROSOPHILA MELANOGASTER; GROWTH, DEVELOPMENT AND AGING; INSECT EXCRETORY SYSTEM; MORPHOGENESIS; ORGANOGENESIS; PHYSIOLOGICAL DIFFERENTIATION; PHYSIOLOGY; TUBULOGENESIS;

CONVERGENT-EXTENSION; DROSOPHILA; INSECT EXCRETORY SYSTEM; MALPIGHIAN TUBULE; MORPHOGENESIS; ORGANOGENESIS; PHYSIOLOGICAL DIFFERENTIATION; RENAL TUBULE; TUBULOGENESIS;

ANIMALS; BODY PATTERNING; DROSOPHILA MELANOGASTER; KIDNEY TUBULES; MALPIGHIAN TUBULES; ORGANOGENESIS;

EID: 84876583038     PISSN: 15476278     EISSN: 15558592     Source Type: Journal    
DOI: 10.4161/org.24107     Document Type: Review

References (136)

1. Maddrell SHP. The Fastest Fluid-secreting Cell Known: The Upper Malpighian Tubule Cell of Rhodnius. Bioessays 1991; 13:357-62; http://dx.doi.org/10.1002/bies.950130710. (Pubitemid 121000579)
2. Bertsch A. Foraging in male bumblebess (Bombus lucorum L.): maximizing energy or minimizing water load? Oecologia 1984; 62:325-36; http://dx.doi.org/ 10.1007/BF00384264. (Pubitemid 16277122)
3. Malpighi M. Dissertatio Epistolica De Bombyce. London, 1669.
4. Cobb M. Malpighi, Swammerdam and the colourful silkworm: replication and visual representation in early modern science. Ann Sci 2002; 59:111-7; PMID:12068908; http://dx.doi.org/10.1080/00033790110050759.
5. McGettigan J, McLennan RK, Broderick KE, Kean L, Allan AK, Cabrero P, et al. Insect renal tubules constitute a cell-autonomous immune system that protects the organism against bacterial infection. Insect Biochem Mol Biol 2005; 35:741-54; PMID:15894191; http://dx.doi.org/10.1016/j.ibmb.2005.02.017. (Pubitemid 40707637)
6. Davies SA, Overend G, Sebastian S, Cundall M, Cabrero P, Dow JA, et al. Immune and stress response 'cross-talk' in the Drosophila Malpighian tubule. J Insect Physiol 2012; 58:488-97; PMID:22306292; http://dx.doi.org/10.1016/j. jinsphys.2012.01.008.
7. Craig CL. Evolution of arthropod silks. Annu Rev Entomol 1997; 42:231-67; PMID:15012314; http://dx.doi.org/10.1146/annurev.ento.42.1.231. (Pubitemid 27169549)
8. Green L F. The fine structure of the light organ of the New Zealand glow-worm Arachnocampa luminosa (Diptera: Mycetophilidae). Tissue Cell 1979; 11:457-65; PMID:494236; http://dx.doi.org/10.1016/0040-8166(79)90056-9. (Pubitemid 9258187)
9. Sutherland TD, Young JH, Weisman S, Hayashi CY, Merritt DJ. Insect silk: one name, many materials. Annu Rev Entomol 2010; 55:171-88; PMID:19728833; http://dx.doi.org/10.1146/annurev-ento-112408-085401.
10. Denholm B, Skaer H. Development of Malpighian tubules in Insects. Oxford, UK: Elseveir, 2005.
11. Beyenbach KW, Skaer H, Dow JA. The developmental, molecular, and transport biology of Malpighian tubules. Annu Rev Entomol 2010; 55:351-74; PMID:19961332; http://dx.doi.org/10.1146/annurev-ento-112408-085512.
12. Hatton-Ellis E, Ainsworth C, Sushama Y, Wan S, VijayRaghavan K, Skaer H. Genetic regulation of patterned tubular branching in Drosophila. Proc Natl Acad Sci U S A 2007; 104:169-74; PMID:17190812; http://dx.doi.org/10.1073/pnas. 0606933104. (Pubitemid 46068003)
13. Skaer H, Martinez Arias A. The wingless product is required for cell proliferation in the Malpighian tubule anlage of Drosophila melanogaster. Development 1992; 116:745-54.
14. Wan S, Cato AM, Skaer H. Multiple signalling pathways establish cell fate and cell number in Drosophila malpighian tubules. Dev Biol 2000; 217:153-65; PMID:10625542; http://dx.doi.org/10.1006/dbio.1999.9499. (Pubitemid 30046806)
15. Sudarsan V, Pasalodos-Sanchez S, Wan S, Gampel A, Skaer H. A genetic hierarchy establishes mito-genic signalling and mitotic competence in the renal tubules of Drosophila. Development 2002; 129:935-44; PMID:11861476. (Pubitemid 34874117)
16. Kerber B, Fellert S, Hoch M. Seven-up, the Drosophila homolog of the COUP-TF orphan receptors, controls cell proliferation in the insect kidney. Genes Dev 1998; 12:1781-6; PMID:9637680; http://dx.doi.org/10.1101/gad.12.12. 1781. (Pubitemid 28304331)
17. Denholm B, Sudarsan V, Pasalodos-Sanchez S, Artero R, Lawrence P, Maddrell S, et al. Dual origin of the renal tubules in Drosophila: mesodermal cells integrate and polarize to establish secretory function. Curr Biol 2003; 13:1052-7; PMID:12814552; http://dx.doi.org/10.1016/S0960-9822(03)00375-0. (Pubitemid 36726042)
18. Campbell K, Casanova J, Skaer H. Mesenchymal-to-epithelial transition of intercalating cells in Drosophila renal tubules depends on polarity cues from epithelial neighbours. Mech Dev 2010; 127:345-57; PMID:20382220; http://dx.doi.org/10.1016/j. mod.2010.04.002.
19. O'Donnell MJ, Maddrell SH. Fluid reabsorption and ion transport by the lower Malpighian tubules of adult female Drosophila. J Exp Biol 1995; 198:1647-53; PMID:7636442.
20. Wessing A, Eichelberg D. Malpighian tubules, rectal papillae and excretion. London: Academic Press, 1978.
21. Piersol GM. Polycystic Disease of the Kidney. Trans Am Climatol Clin Assoc 1927; 43:221-31; PMID:21408945.
22. Keller R. Shaping the vertebrate body plan by polarized embryonic cell movements. Science 2002; 298:1950-4; PMID:12471247; http://dx.doi.org/10.1126/ sci-ence.1079478. (Pubitemid 35425243)
23. Keller R. Mechanisms of elongation in embryogenesis. Development 2006; 133:2291-302; PMID:16720874; http://dx.doi.org/10.1242/dev.02406. (Pubitemid 44044551)
24. Skaer H. Cell division in Malpighian tubule development in D. melanogaster is regulated by a single tip cell. Nature 1989; 342:566-9; http://dx.doi.org/10.1038/342566a0.
25. Broadie K, Skaer H, Bate M. Whole-embryo culture of Drosophila: development of embryonic tissues in vitro. Rouxs Arch Dev Biol 1992; 201:364-75; http://dx.doi.org/10.1007/BF00365124.
26. Denholm B, Brown S, Ray R P, Ruiz-Gómez M, Skaer H, Hombría JC. crossveinless-c is a RhoGAP required for actin reorganisation during morphogenesis. Development 2005; 132:2389-400; PMID:15843408; http://dx.doi.org/10.1242/dev.01829. (Pubitemid 40872808)
27. Blake KJ, Myette G, Jack J. The products of ribbon and raw are necessary for proper cell shape and cellular localization of nonmuscle myosin in Drosophila. Dev Biol 1998; 203:177-88; PMID:9806782; http://dx.doi.org/10.1006/ dbio.1998.9036. (Pubitemid 28506672)
28. Blake KJ, Myette G, Jack J. ribbon, raw, and zipper have distinct functions in reshaping the Drosophila cytoskeleton. Dev Genes Evol 1999; 209:555-9; PMID:10502112; http://dx.doi.org/10.1007/s004270050288. (Pubitemid 29452700)
29. Jack J, Myette G. The genes raw and ribbon are required for proper shape of tubular epithelial tissues in Drosophila. Genetics 1997; 147:243-53; PMID:9286684. (Pubitemid 27385552)
30. Simões S, Denholm B, Azevedo D, Sotillos S, Martin P, Skaer H, et al. Compartmentalisation of Rho regulators directs cell invagination during tissue morphogenesis. Development 2006; 133:4257-67; PMID:17021037; http://dx.doi.org/10.1242/dev.02588. (Pubitemid 44830669)
31. Bertet C, Sulak L, Lecuit T. Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature 2004; 429:667-71; PMID:15190355; http://dx.doi.org/10.1038/nature02590. (Pubitemid 38812319)
32. Blankenship J T, Backovic ST, Sanny JS, Weitz O, Zallen JA. Multicellular rosette formation links planar cell polarity to tissue morphogenesis. Dev Cell 2006; 11:459-70; PMID:17011486; http://dx.doi.org/10.1016/j.devcel.2006.09.007. (Pubitemid 44430903)
33. Shih J, Keller R. Patterns of cell motility in the organizer and dorsal mesoderm of Xenopus laevis. Development 1992; 116:915-30; PMID:1295744. (Pubitemid 23042433)
34. Shih J, Keller R. Cell motility driving mediolateral intercalation in explants of Xenopus laevis. Development 1992; 116:901-14; PMID:1295743. (Pubitemid 23042432)
35. Keller R, Tibbetts P. Mediolateral cell intercalation in the dorsal, axial mesoderm of Xenopus laevis. Dev Biol 1989; 131:539-49; PMID:2463948; http://dx.doi.org/10.1016/S0012-1606(89)80024-7. (Pubitemid 19054786)
36. Munro EM, Odell GM. Polarized basolateral cell motility underlies invagination and convergent extension of the ascidian notochord. Development 2002; 129:13-24; PMID:11782397. (Pubitemid 34863772)
37. Williams-Masson EM, Heid PJ, Lavin CA, Hardin J. The cellular mechanism of epithelial rearrangement during morphogenesis of the Caenorhabditis elegans dorsal hypodermis. Dev Biol 1998; 204:263-76; PMID:9851858; http://dx.doi.org/ 10.1006/dbio.1998.9048. (Pubitemid 28563880)
38. Bunt S, Hooley C, Hu N, Scahill C, Weavers H, Skaer H. Hemocyte-secreted type IV collagen enhances BMP signaling to guide renal tubule morphogenesis in Drosophila. Dev Cell 2010; 19:296-306; PMID:20708591; http://dx.doi.org/10.1016/ j.dev-cel.2010.07.019.
39. Vasilyev A, Liu Y, Mudumana S, Mangos S, Lam PY, Majumdar A, et al. Collective cell migration drives morphogenesis of the kidney nephron. PLoS Biol 2009; 7:e9; PMID:19127979; http://dx.doi.org/10.1371/journal.pbio.1000009.
40. Haigo SL, Bilder D. Global tissue revolutions in a mor-phogenetic movement controlling elongation. Science 2011; 331:1071-4; PMID:21212324; http://dx.doi.org/10.1126/science.1199424.
41. Harbecke R, Lengyel JA. Genes controlling posterior gut development in the Drosophila embryo. Rouxs Arch Dev Biol 1995; 204:308-29; http://dx.doi.org/10.1007/BF02179500.
42. Jack J, Myette G. Mutations that alter the morphology of the malpighian tubules in Drosophila. Dev Genes Evol 1999; 209:546-54; PMID:10502111; http://dx.doi.org/10.1007/s004270050287. (Pubitemid 29452699)
43. Araújo SJ, Aslam H, Tear G, Casanova J. mummy/cystic encodes an enzyme required for chitin and glycan synthesis, involved in trachea, embryonic cuticle and CNS development-analysis of its role in Drosophila tracheal morphogenesis. Dev Biol 2005; 288:179-93; PMID:16277981; http://dx.doi.org/10. 1016/j. ydbio.2005.09.031. (Pubitemid 41713162)
44. Tonning A, Hemphälä J, Tång E, Nannmark U, Samakovlis C, Uv A. A transient luminal chitinous matrix is required to model epithelial tube diameter in the Drosophila trachea. Dev Cell 2005; 9:423-30; PMID:16139230; http://dx.doi.org/10.1016/j.dev-cel.2005.07.012. (Pubitemid 41235811)
45. Devine W P, Lubarsky B, Shaw K, Luschnig S, Messina L, Krasnow MA. Requirement for chitin biosynthesis in epithelial tube morphogenesis. Proc Natl Acad Sci U S A 2005; 102:17014-9; PMID:16287975; http://dx.doi.org/10.1073/pnas. 0506676102. (Pubitemid 41692675)
46. Tonning A, Helms S, Schwarz H, Uv AE, Moussian B. Hormonal regulation of mummy is needed for apical extracellular matrix formation and epithelial morphogenesis in Drosophila. Development 2006; 133:331-41; PMID:16368930; http://dx.doi.org/10.1242/dev.02206. (Pubitemid 43210721)
47. Fernandes I, Chanut-Delalande H, Ferrer P, Latapie Y, Waltzer L, Affolter M, et al. Zona pellucida domain proteins remodel the apical compartment for localized cell shape changes. Dev Cell 2010; 18:64-76; PMID:20152178; http://dx.doi.org/10.1016/j.dev-cel.2009.11.009.
48. Luschnig S, Bätz T, Armbruster K, Krasnow MA. serpentine and vermiform encode matrix proteins with chitin binding and deacetylation domains that limit tracheal tube length in Drosophila. Curr Biol 2006; 16:186-94; PMID:16431371; http://dx.doi.org/10.1016/j.cub.2005.11.072. (Pubitemid 43117434)
49. Bökel C, Prokop A, Brown NH. Papillote and Piopio: Drosophila ZP-domain proteins required for cell adhesion to the apical extracellular matrix and microtubule organization. J Cell Sci 2005; 118:633-42; PMID:15657084; http://dx.doi.org/10.1242/jcs.01619. (Pubitemid 40310129)
50. Jazwinska A, Ribeiro C, Affolter M. Epithelial tube morphogenesis during Drosophila tracheal development requires Piopio, a luminal ZP protein. Nat Cell Biol 2003; 5:895-901; PMID:12973360; http://dx.doi.org/10.1038/ncb1049. (Pubitemid 37220695)
51. Wang S, Jayaram SA, Hemphälä J, Senti KA, Tsarouhas V, Jin H, et al. Septate-junction-dependent lumi-nal deposition of chitin deacetylases restricts tube elongation in the Drosophila trachea. Curr Biol 2006; 16:180-5; PMID:16431370; http://dx.doi.org/10.1016/j.cub.2005.11.074. (Pubitemid 43117433)
52. Tepass U, Hartenstein V. The development of cellular junctions in the Drosophila embryo. Dev Biol 1994; 161:563-96; PMID:8314002; http://dx.doi.org/ 10.1006/dbio.1994.1054.
53. Zallen JA, Wieschaus E. Patterned gene expression directs bipolar planar polarity in Drosophila. Dev Cell 2004; 6:343-55; PMID:15030758; http://dx.doi.org/10.1016/S1534-5807(04)00060-7. (Pubitemid 38364567)
54. Ninomiya H, Elinson R P, Winklbauer R. Antero-posterior tissue polarity links mesoderm convergent extension to axial patterning. Nature 2004; 430:364-7; PMID:15254540; http://dx.doi.org/10.1038/nature02620. (Pubitemid 38937745)
55. Wallingford JB. Planar cell polarity and the developmental control of cell behavior in vertebrate embryos. Annu Rev Cell Dev Biol 2012; 28:627-53; PMID:22905955; http://dx.doi.org/10.1146/annurev-cellbio-092910-154208.
56. Chung S, Vining MS, Bradley PL, Chan CC, Wharton KA Jr., Andrew DJ. Serrano (sano) functions with the planar cell polarity genes to control tracheal tube length. PLoS Genet 2009; 5:e1000746; PMID:19956736; http://dx.doi.org/10. 1371/journal.pgen.1000746.
57. Lekven AC, Tepass U, Keshmeshian M, Hartenstein V. faint sausage encodes 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 1998; 125:2747-58; PMID:9636088. (Pubitemid 28396171)
58. Brodu V, Casanova J. The RhoGAP crossveinless-c links trachealess and EGFR signaling to cell shape remodeling in Drosophila tracheal invagination. Genes Dev 2006; 20:1817-28; PMID:16818611; http://dx.doi.org/10.1101/gad.375706. (Pubitemid 43992889)
59. Sözen MA, Armstrong JD, Yang M, Kaiser K, Dow JA. Functional domains are specified to single-cell resolution in a Drosophila epithelium. Proc Natl Acad Sci U S A 1997; 94:5207-12; PMID:9144216; http://dx.doi.org/10.1073/pnas. 94.10.5207. (Pubitemid 27214762)
60. Maddrell SHP. The Functional Design of the Insect Excretory System. J Exp Biol 1981; 90:1-15.
61. Du J, Kean L, Allan AK, Southall TD, Davies SA, McInerny CJ, et al. The SzA mutations of the B subunit of the Drosophila vacuolar H+ ATPase identify conserved residues essential for function in fly and yeast. J Cell Sci 2006; 119:2542-51; PMID:16735441; http://dx.doi.org/10.1242/jcs.02983. (Pubitemid 44070435)
62. Weng XH, Huss M, Wieczorek H, Beyenbach KW. The V-type H(+)-ATPase in Malpighian tubules of Aedes aegypti: localization and activity. J Exp Biol 2003; 206:2211-9; PMID:12771170; http://dx.doi.org/10.1242/jeb.00385. (Pubitemid 36821517)
63. Davies SA, Goodwin S F, Kelly DC, Wang Z, Sözen MA, Kaiser K, et al. Analysis and inactivation of vha55, the gene encoding the vacuolar ATPase B-subunit in Drosophila melanogaster reveals a larval lethal phenotype. J Biol Chem 1996; 271:30677-84; PMID:8940044; http://dx.doi.org/10.1074/jbc.271.48. 30677. (Pubitemid 26404084)
64. Bertram G, Shleithoff L, Zimmermann P, Wessing A. Bafilomycin A1 is a potent inhibitor of urine formation by Malpighian tubules of Drosophila hydei-is a vacuolar-type ATPase involved in ion and fluid secretion? J Insect Physiol 1991; 37:201-9; http://dx.doi.org/10.1016/0022-1910(91)90070-G.
65. Rheault MR, Okech BA, Keen SB, Miller MM, Meleshkevitch EA, Linser PJ, et al. Molecular cloning, phylogeny and localization of AgNHA1: the first Na+/H+ antiporter (NHA) from a metazoan, Anopheles gambiae. J Exp Biol 2007; 210:3848-61; PMID:17951426; http://dx.doi.org/10.1242/jeb.007872. (Pubitemid 350206253)
66. Day J P, Wan S, Allan AK, Kean L, Davies SA, Gray JV, et al. Identification of two partners from the bacterial Kef exchanger family for the apical plasma membrane V-ATPase of Metazoa. J Cell Sci 2008; 121:2612-9; PMID:18628302; http://dx.doi.org/10.1242/jcs.033084.
67. Scott BN, Yu MJ, Lee LW, Beyenbach KW. Mechanisms of K+ transport across basolateral membranes of principal cells in Malpighian tubules of the yellow fever mosquito, Aedes aegypti. J Exp Biol 2004; 207:1655-63; PMID:15073198; http://dx.doi.org/10.1242/jeb.00932. (Pubitemid 38630495)
68. Evans JM, Allan AK, Davies SA, Dow JA. Sulphonylurea sensitivity and enriched expression implicate inward rectifier K+ channels in Drosophila melanogas-ter renal function. J Exp Biol 2005; 208:3771-83; PMID:16169954; http://dx.doi.org/10.1242/jeb.01829. (Pubitemid 41571757)
69. Piermarini PM, Rouhier M F, Schepel M, Kosse C, Beyenbach KW. Cloning and functional characterization of inward-rectifying potassium (Kir) channels from Malpighian tubules of the mosquito Aedes aegypti. Insect Biochem Mol Biol 2013; 43:75-90; PMID:23085358; http://dx.doi.org/10.1016/j. ibmb.2012.09.009.
70. Pullikuth AK, Aimanova K, Kang'ethe W, Sanders HR, Gill SS. Molecular characterization of sodium/proton exchanger 3 (NHE3) from the yellow fever vector, Aedes aegypti. J Exp Biol 2006; 209:3529-44; PMID:16943493; http://dx.doi.org/10.1242/jeb.02419. (Pubitemid 44606609)
71. Coast GM, Webster SG, Schegg KM, Tobe SS, Schooley DA. The Drosophila melanogaster homologue of an insect calcitonin-like diuretic peptide stimulates V-ATPase activity in fruit fly Malpighian tubules. J Exp Biol 2001; 204:1795-804; PMID:11316500. (Pubitemid 34861425)
72. Johnson EC, Shafer OT, Trigg JS, Park J, Schooley DA, Dow JA, et al. A novel diuretic hormone receptor in Drosophila: evidence for conservation of CGRP signaling. J Exp Biol 2005; 208:1239-46; PMID:15781884; http://dx.doi.org/10. 1242/jeb.01529. (Pubitemid 40564558)
73. Kean L, Cazenave W, Costes L, Broderick KE, Graham S, Pollock V P, et al. Tw o nitridergic peptides are encoded by the gene capability in Drosophila melano-gaster. Am J Physiol Regul Integr Comp Physiol 2002; 282:R1297-307; PMID:11959669.
74. Cabrero P, Radford JC, Broderick KE, Costes L, Veenstra JA, Spana E P, et al. The Dh gene of Drosophila melanogaster encodes a diuretic peptide that acts through cyclic AMP. J Exp Biol 2002; 205:3799-807; PMID:12432004. (Pubitemid 36059033)
75. Dow JA. The versatile stellate cell-more than just a space-filler. J Insect Physiol 2012; 58:467-72; PMID:22202730; http://dx.doi.org/10.1016/j.jins- phys.2011.12.003.
76. O'Donnell MJ, Rheault MR, Davies SA, Rosay P, Harvey BJ, Maddrell SH, et al. Hormonally controlled chloride movement across Drosophila tubules is via ion channels in stellate cells. Am J Physiol 1998; 274:R1039-49; PMID:9575967.
77. Piermarini PM, Grogan LF, Lau K, Wang L, Beyenbach KWA. A SLC4-like anion exchanger from renal tubules of the mosquito (Aedes aegypti): evidence for a novel role of stellate cells in diuretic fluid secretion. Am J Physiol Regul Integr Comp Physiol 2010; 298:R642-60; PMID:20042685; http://dx.doi.org/10.1152/ ajp-regu.00729.2009.
78. Linser PJ, Neira Oviedo M, Hirata T, Seron TJ, Smith KE, Piermarini PM, et al. Slc4-like anion transporters of the larval mosquito alimentary canal. J Insect Physiol 2012; 58:551-62; PMID:22251674; http://dx.doi.org/10.1016/j. jinsphys.2012.01.002.
79. O'Connor KR, Beyenbach KW. Chloride channels in apical membrane patches of stellate cells of Malpighian tubules of Aedes aegypti. J Exp Biol 2001; 204:367-78; PMID:11136622. (Pubitemid 32116912)
80. Wang J, Kean L, Yang J, Allan AK, Davies SA, Herzyk P, et al. Function-informed transcriptome analysis of Drosophila renal tubule. Genome Biol 2004; 5:R69; PMID:15345053; http://dx.doi.org/10.1186/gb-2004-5-9-r69.
81. Denholm B, Hu N, Fauquier T, Caubit X, Fasano L, Skaer H. The tiptop/teashirt genes regulate cell differentiation and renal physiology in Drosophila. Development 2013; 140:1100-10; PMID:23404107; http://dx.doi.org/10. 1242/dev.088989.
82. Pannabecker TL, Hayes TK, Beyenbach KW. Regulation of epithelial shunt conductance by the peptide leucokinin. J Membr Biol 1993; 132:63-76; PMID:8459448; http://dx.doi.org/10.1007/BF00233052. (Pubitemid 23071927)
83. Skaer HB, Maddrell SH, Harrison JB. The permeability properties of septate junctions in Malpighian tubules of Rhodnius. J Cell Sci 1987; 88:251-65; PMID:3320067.
84. Beyenbach K W. A dynamic paracellular pathway serves diuresis in mosquito Malpighian tubules. Ann N Y Acad Sci 2012; 1258:166-76; PMID:22731730; http://dx.doi.org/10.1111/j.1749-6632.2012.06527.x.
85. Beyenbach KW, Baumgart S, Lau K, Piermarini PM, Zhang S. Signaling to the apical membrane and to the paracellular pathway: changes in the cyto-solic proteome of Aedes Malpighian tubules. J Exp Biol 2009; 212:329-40; PMID:19151207; http://dx.doi.org/10.1242/jeb.024646.
86. Miyauchi J T, Piermarini PM, Yang JD, Gilligan DM, Beyenbach KW. Roles of PKC and phospho-adducin in transepithelial fluid secretion by Malpighian tubules of the yellow fever mosquito. Tissue Barriers 2013; 11:1-14.
87. Kaufmann N, Mathai JC, Hill WG, Dow JA, Zeidel ML, Brodsky JL. Developmental expression and biophysical characterization of a Drosophila melanogaster aquaporin. Am J Physiol Cell Physiol 2005; 289:C397-407; PMID:15800049; http://dx.doi.org/10.1152/ajp-cell.00612.2004.
88. O'Donnell MJ, Maddrell SH. Paracellular and tran-scellular routes for water and solute movements across insect epithelia. J Exp Biol 1983; 106:231-53; PMID:6361206. (Pubitemid 14200314)
89. O'Donnell MJ, Aldis GK, Maddrell SHP. Measurements of osmotic permeability in the Malpighian tubules of an insect Rhodnius prolixus. Proc R Soc Lond B Biol Sci 1982; 216:267-78; http://dx.doi.org/10.1098/rspb.1982.0074.
90. Sofía Hernández C, González E, Whittembury G. The paracellular channel for water secretion in the upper segment of the Malpighian tubule of Rhodnius prolix-us. J Membr Biol 1995; 148:233-42; PMID:8747555. (Pubitemid 26017799)
91. Spring JH, Robichaux SR, Kaufmann N, Brodsky JL. Localization of a Drosophila DRIP-like aquaporin in the Malpighian tubules of the house cricket, Acheta domesticus. Comp Biochem Physiol A Mol Integr Physiol 2007; 148:92-100; PMID:17267256; http://dx.doi.org/10.1016/j.cbpa.2006.12.022. (Pubitemid 47077659)
92. Echevarría M, Ramírez-Lorca R, Hernández CS, Gutiérrez A, Méndez-Ferrer S, González E, et al. Identification of a new water channel (Rp-MIP) in the Malpighian tubules of the insect Rhodnius prolixus. Pflugers Arch 2001; 442:27-34; PMID:11374065; http://dx.doi.org/10.1007/s004240000494. (Pubitemid 32336822)
93. Martini SV, Goldenberg RC, Fortes FS, Campos-de-Carvalho AC, Falkenstein D, Morales MM. Rhodnius prolixus Malpighian tubule's aquaporin expression is modulated by 5-hydroxytryptamine. Arch Insect Biochem Physiol 2004; 57:133-41; PMID:15484262; http://dx.doi.org/10.1002/arch.20017. (Pubitemid 39520770)
94. Liu K, Tsujimoto H, Cha SJ, Agre P, Rasgon JL. Aquaporin water channel AgAQP1 in the malaria vector mosquito Anopheles gambiae during blood feeding and humidity adaptation. Proc Natl Acad Sci U S A 2011; 108:6062-6; PMID:21444767; http://dx.doi.org/10.1073/pnas.1102629108.
95. Cabrero P, Pollock V P, Davies SA, Dow JA. A conserved domain of alkaline phosphatase expression in the Malpighian tubules of dipteran insects. J Exp Biol 2004; 207:3299-305; PMID:15326206; http://dx.doi.org/10.1242/jeb.01156. (Pubitemid 39348332)
96. Shippy TD, Tomoyasu Y, Nie W, Brown SJ, Denell RE. Do teashirt family genes specify trunk identity? Insights from the single tiptop/teashirt homolog of Tribolium castaneum. Dev Genes Evol 2008; 218:141-52; PMID:18392876; http://dx.doi.org/10.1007/s00427-008-0212-5. (Pubitemid 351513914)
97. Gloor H. Schädigungsmuster eines Letalfaktors (Kr) in Drosophila melanogaster. Arch Julius Klaus-Stift Vererb Sozialanhropol Rassenhyg 1950; 25:38-44.
98. Liu S, Jack J. Regulatory interactions and role in cell type specification of the Malpighian tubules by the cut, Krüppel, and caudal genes of Drosophila. Dev Biol 1992; 150:133-43; PMID:1537429; http://dx.doi.org/10.1016/0012-1606(92)90013-7.
99. Dube K, McDonald DG, O'Donnell MJ. Calcium transport by isolated anterior and posterior Malpighian tubules of Drosophila melanogaster: roles of sequestration and secretion. J Insect Physiol 2000; 46:1449-60; PMID:10891573; http://dx.doi.org/10.1016/S0022-1910(00)00069-X.
100. Chintapalli VR, Terhzaz S, Wang J, Al Bratty M, Watson DG, Herzyk P, et al. Functional correlates of positional and gender-specific renal asymmetry in Drosophila. PLoS One 2012; 7:e32577; PMID:22496733; http://dx.doi.org/10.1371/ journal.pone.0032577.
101. Hoch M, Broadie K, Jäckle H, Skaer H. Sequential fates in a single cell are established by the neuro-genic cascade in the Malpighian tubules of Drosophila. Development 1994; 120:3439-50; PMID:7821213. (Pubitemid 24366989)
102. Isshiki T, Pearson B, Holbrook S, Doe CQ. Drosophila neuroblasts sequentially express transcription factors which specify the temporal identity of their neuronal progeny. Cell 2001; 106:511-21; PMID:11525736; http://dx.doi.org/10.1016/S0092-8674(01)00465-2. (Pubitemid 32786994)
103. Skaer H. Cell proliferation and development of the Malpighian tubules in Drosophila melanogaster. Exp Nephrol 1996; 4:119-26; PMID:8673441. (Pubitemid 26094912)
104. Skaer H, Harrison JB, Maddrell SHP. Physiological and structural maturation of a polarised epithelium: the malpighian tubules of a blood sucking insect, Rhodnius prolixus. J Cell Sci 1990; 96:537-47.
105. O'donnell MJ, Maddrell SH, le B Skaer H, Harrison JB. Elaborations of the basal surface of the cells of the Malpighian tubules of an insect. Tissue Cell 1985; 17: 865-81 PMID:18620151. http://dx.doi.org/10.1016/0040-8166(85)90042-4. (Pubitemid 16175261)
106. Schepel SA, Fox AJ, Miyauchi JT, Sou T, Yang JD, Lau K, et al. The single kinin receptor signals to separate and independent physiological pathways in Malpighian tubules of the yellow fever mosquito. Am J Physiol Regul Integr Comp Physiol 2010; 299:R612-22; PMID:20538895; http://dx.doi.org/10.1152/ajp-regu. 00068.2010.
107. Choksi S P, Southall TD, Bossing T, Edoff K, de Wit E, Fischer BE, et al. Prospero acts as a binary switch between self-renewal and differentiation in Drosophila neural stem cells. Dev Cell 2006; 11:775-89; PMID:17141154; http://dx.doi.org/10.1016/j. devcel.2006.09.015. (Pubitemid 44804272)
108. Sirodot S. Malpighian tubules: anatomy and chemistry. Ann Sci Nat Zool 1858; 10:141-89.
109. Wang X, Harris RE, Bayston LJ, Ashe HL. Type IV collagens regulate BMP signalling in Drosophila. Nature 2008; 455:72-7; PMID:18701888; http://dx.doi.org/10.1038/nature07214.
110. Ainsworth C, Wan S, Skaer H. Coordinating cell fate and morphogenesis in Drosophila renal tubules. Philos Trans R Soc Lond B Biol Sci 2000; 355:931-7; PMID:11128986; http://dx.doi.org/10.1098/rstb.2000.0628. (Pubitemid 30613317)
111. Ishimori AC. Relation of Malpighian tubes to rectum: Lepidoptera larvae. Ann Entomol Soc Am 1924; 17:75-86.
112. Ramsay JA. The rectal complex of the mealworm Tenebrio molitor, L. (Coleoptera, Tenebrionidae). Philosophical Transactions of the Royal Society B. Biological Sciences 1964; 248:279-314; http://dx.doi.org/10.1098/rstb.1964.0013.
113. Talsma AD, Christov C P, Terriente-Felix A, Linneweber GA, Perea D, Wayland M, et al. Remote control of renal physiology by the intestinal neuropeptide pigment-dispersing factor in Drosophila. Proc Natl Acad Sci U S A 2012; 109:12177-82; PMID:22778427; http://dx.doi.org/10.1073/pnas.1200247109.
114. Cantera R, Nässel DR. Segmental peptidergic innervation of abdominal targets in larval and adult dipteran insects revealed with an antiserum against leucokinin I. Cell Tissue Res 1992; 269:459-71; PMID:1423512; http://dx.doi.org/10.1007/BF00353901.
115. Dow JA, Maddrell SH, Görtz A, Skaer NJ, Brogan S, Kaiser K. The malpighian tubules of Drosophila melanogaster: a novel phenotype for studies of fluid secretion and its control. J Exp Biol 1994; 197:421-8; PMID:7852912.
116. Brand AH, Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993; 118:401-15; PMID:8223268. (Pubitemid 23214028)
117. McGuire SE, Le PT, Osborn AJ, Matsumoto K, Davis RL. Spatiotemporal rescue of memory dysfunction in Drosophila. Science 2003; 302:1765-8; PMID:14657498; http://dx.doi.org/10.1126/sci-ence.1089035. (Pubitemid 37505740)
118. McGuire SE, Mao Z, Davis RL. Spatiotemporal gene expression targeting with the TARGET and gene-switch systems in Drosophila. Sci STKE 2004; 2004:pl6; PMID:14970377; http://dx.doi.org/10.1126/stke.2202004pl6.
119. Dietzl G, Chen D, Schnorrer F, Su KC, Barinova Y, Fellner M, et al. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 2007; 448:151-6; PMID:17625558; http://dx.doi.org/10.1038/ nature05954. (Pubitemid 47067374)
120. Chintapalli VR, Wang J, Dow JA. Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat Genet 2007; 39:715-20; PMID:17534367; http://dx.doi.org/10.1038/ng2049. (Pubitemid 46848596)
121. Dow JA, Romero M F. Drosophila provides rapid modeling of renal development, function, and disease. Am J Physiol Renal Physiol 2010; 299:F1237-44; PMID:20926630; http://dx.doi.org/10.1152/ajpre-nal.00521.2010.
122. Hirata T, Cabrero P, Berkholz DS, Bondeson D P, Ritman EL, Thompson JR, et al. In vivo Drosophilia genetic model for calcium oxalate nephrolithiasis. Am J Physiol Renal Physiol 2012; 303:F1555-62; PMID:22993075; http://dx.doi.org/ 10.1152/ajpre-nal.00074.2012.
123. Ramsay JA. Active transport of water by the Malpighian tubules of the stick insect, Dixippus morosus (Orthoptera, Phasmidae). J Exp Biol 1954; 31:104-13.
124. Grobstein C. Trans-filter induction of tubules in mouse metanephrogenic mesenchyme. Exp Cell Res 1956; 10:424-40; PMID:13317909; http://dx.doi.org/10. 1016/0014-4827(56)90016-7.
125. Saxén L, Lehtonen E. Transfilter induction of kidney tubules as a function of the extent and duration of intercellular contacts. J Embryol Exp Morphol 1978; 47:97-109; PMID:722235. (Pubitemid 9037417)
126. Saxen L. Organogenesis of the kidney. Cambridge: Cambridge University Press, 1987.
127. Srinivas S, Goldberg MR, Watanabe T, D'Agati V, al-Awqati Q, Costantini F. Expression of green fluorescent protein in the ureteric bud of transgenic mice: a new tool for the analysis of ureteric bud morphogenesis. Dev Genet 1999; 24:241-51; PMID:10322632; http://dx.doi.org/10.1002/(SICI)1520-6408(1999)24:3/ 4241::AID-DVG73.0.CO;2-R. (Pubitemid 29211788)
128. Watanabe T, Costantini F. Real-time analysis of ure-teric bud branching morphogenesis in vitro. Dev Biol 2004; 271:98-108; PMID:15196953; http://dx.doi.org/10.1016/j.ydbio.2004.03.025. (Pubitemid 38757778)
129. Costantini F, Watanabe T, Lu B, Chi X, Srinivas S. Imaging kidney development. Cold Spring Harbor protocols 2011; 2011:109.
130. Chi X, Michos O, Shakya R, Riccio P, Enomoto H, Licht JD, et al. Ret-dependent cell rearrangements in the Wolffian duct epithelium initiate ure-teric bud morphogenesis. Dev Cell 2009; 17:199-209; PMID:19686681; http://dx.doi.org/10.1016/j. devcel.2009.07.013.
131. Li X, Hyink D P, Polgar K, Gusella GL, Wilson PD, Burrow CR. Protein kinase X activates ureteric bud branching morphogenesis in developing mouse meta-nephric kidney. J Am Soc Nephrol 2005; 16:3543-52; PMID:16236808; http://dx.doi.org/10.1681/ASN.2005030240. (Pubitemid 46211275)
132. Polgar K, Burrow CR, Hyink D P, Fernandez H, Thornton K, Li X, et al. Disruption of polycystin-1 function interferes with branching morphogenesis of the ureteric bud in developing mouse kidneys. Dev Biol 2005; 286:16-30; PMID:16122726; http://dx.doi.org/10.1016/j.ydbio.2005.06.034. (Pubitemid 41394044)
133. Davies JA, Ladomery M, Hohenstein P, Michael L, Shafe A, Spraggon L, et al. Development of an siRNA-based method for repressing specific genes in renal organ culture and its use to show that the Wt1 tumour suppressor is required for nephron differentiation. Hum Mol Genet 2004; 13:235-46; PMID:14645201; http://dx.doi.org/10.1093/hmg/ddh015. (Pubitemid 38111361)
134. Maeshima A, Vaughn DA, Choi Y, Nigam SK. Activin A is an endogenous inhibitor of ureteric bud outgrowth from the Wolffian duct. Dev Biol 2006; 295:473-85; PMID:16643884; http://dx.doi.org/10.1016/j. ydbio.2006.03.011. (Pubitemid 43927690)
135. Lienkamp SS, Liu K, Karner CM, Carroll TJ, Ronneberger O, Wallingford JB, et al. Vertebrate kidney tubules elongate using a planar cell polarity-dependent, rosette-based mechanism of convergent extension. Nat Genet 2012; 44:1382-7; PMID:23143599; http://dx.doi.org/10.1038/ng.2452.
136. Caubit X, Lye CM, Martin E, Coré N, Long DA, Vola C, et al. Teashirt 3 is necessary for ureteral smooth muscle differentiation downstream of SHH and BMP4. Development 2008; 135:3301-10; PMID:18776146; http://dx.doi.org/10.1242/dev.022442.