Insights into the Malpighian tubule from functional genomics

Journal of Experimental Biology

Volumn 212, Issue 3, 2009, Pages 435-445

  Dow, Julian A T ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Cell signalling; Detoxification; Drosophila melanogaster; FlyAtlas; Ion transport; Malpighian tubule

Indexed keywords

XANTHINE OXIDASE;

ANIMAL; BIOLOGICAL MODEL; CHEMICAL STRUCTURE; CYTOLOGY; DROSOPHILA MELANOGASTER; GENETICS; GENOMICS; IMMUNOLOGY; INNATE IMMUNITY; MALPIGHIAN TUBULE; METHODOLOGY; MICROARRAY ANALYSIS; MUTATION; PHYSIOLOGY; REVIEW;

ANIMALS; DROSOPHILA MELANOGASTER; GENOMICS; IMMUNITY, INNATE; MALPIGHIAN TUBULES; MICROARRAY ANALYSIS; MODELS, BIOLOGICAL; MOLECULAR STRUCTURE; MUTATION; XANTHINE OXIDASE;

BACTERIA (MICROORGANISMS); DROSOPHILA MELANOGASTER; HEXAPODA; MAMMALIA;

EID: 59149100787     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.024224     Document Type: Review

References (82)

1. Allan, A. K., Du, J., Davies, S. A. and Dow, J. A. T. (2005). Genome-wide survey of V-ATPase genes in Drosophila reveals a conserved renal phenotype for lethal alleles. Physiol. Genomics 22, 128-138.
2. Ashburner, M. (1971). Induction of puffs in polytene chromosomes of in vitro cultured salivary glands of Drosophila melanogaster by ecdysone and echysone analogues. Nat. New Biol. 230, 222-224.
3. Ashburner, M. and Drysdale, R. (1994). FlyBase-the Drosophila genetic database. Development 120, 2077-2079.
4. + antiport helps to explain extracellular pH 11 in a model epithelium. FEBS Lett. 361, 153-156.
5. Bellen, H. J., Levis, R. W., Liao, G., He, Y., Carlson, J. W., Tsang, G., Evans-Holm, M., Hiesinger, P. R., Schulze, K. L., Rubin, G. M. et al. (2004). The BDGP gene disruption project: single transposon insertions associated with 40% of Drosophila genes. Genetics 167, 761-781.
6. Berridge, M. J. and Oschman, J. L. (1969). A structural basis for fluid secretion by Malpighian tubules. Tissue Cell 1, 247-272.
7. Beyenbach, K. W. (2003). Transport mechanisms of diuresis in Malpighian tubules of insects. J. Exp. Biol. 206, 3845-3856.
8. Bingham, P. M., Kidwell, M. G. and Rubin, G. M. (1982). The molecular basis of P-M hybrid dysgenesis: the role of the P element, a P-strain-specific transposon family. Cell 29, 995-1004.
9. Blumenthal, E. M. (2003). Regulation of chloride permeability by endogenously produced tyramine in the Drosophila Malpighian tubule. Am. J. Physiol. Cell Physiol. 284, C718-C728.
10. Brand, A. H. and Perrimon, N. (1993). Targetted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
11. Brett, C. L., Donowitz, M. and Rao, R. (2005). Evolutionary origins of eukaryotic sodium/proton exchangers. Am. J. Physiol. Cell Physiol. 288, C223-C239.
12. Chien, S., Reiter, L. T., Bier, E. and Gribskov, M. (2002). Homophila: human disease gene cognates in Drosophila. Nucleic Acids Res. 30, 149-151.
13. Chintapalli, V. R., Wang, J., Davies, S. A. and Dow, J. A. T. (2007). Using FlyAtlas to identify better Drosophila models of human disease. Nat. Genetics 39, 715-720.
14. Coast, G. M., Orchard, I., Phillips, J. E. and Schooley, D. A. (2002). Insect diuretic and antidiuretic hormones. Adv. Insect Physiol. 29, 279-409.
15. Daborn, P. J., Yen, J. L., Bogwitz, M. R., Le Goff, G., Feil, E., Jeffers, S., Tijet, N., Perry, T., Heckel, D., Batterham, P. et al. (2002). A single P450 allele associated with insecticide resistance in Drosophila. Science 297, 2253-2256.
16. Davies, S. A. and Terhzaz, S. (2009). Organellar calcium signalling mechanisms in Drosophila epithelial function. J. Exp. Biol. 212, 387-400.
17. Davies, S. A., Kelly, D. C., Goodwin, S. F., Wang, S.-Z., Kaiser, K. and Dow, J. A. T. (1996). Analysis and inactivation of vha55, the gene encoding the V-ATPase B-subunit in Drosophila melanogaster, reveals a larval lethal phenotype. J. Biol. Chem. 271, 30677-30684.
18. Day, J. P., Allan, A. K., Wan, S., Kean, L., Davies, S. A. and Dow, J. A. T. (2008). Two partners for the apical plasma membrane V-ATPase of Metazoa from the bacterial kef exchanger family. J. Cell Sci. 121, 2612-2619.
19. Dent, C. E. and Philpot, G. R. (1954). Xanthinuria: an inborn error of metabolism. Lancet I, 182-185.
20. Dietzl, G., Chen, D., Schnorrer, F., Su, K. C., Barinova, Y., Fellner, M., Gasser, B., Kinsey, K., Oppel, S., Scheiblauer, S. et al. (2007). A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448, 151-156.
21. Dow, J. A. T. (1984). Extremely high pH in biological systems: a model for carbonate transport. Am. J. Physiol. 246, R633-R635.
22. Dow, J. A. T. (2007). Integrative physiology, functional genomics and the phenotype gap: a guide for comparative physiologists. J. Exp. Biol. 210, 1632-1640.
23. Dow, J. A. T. and Davies, S. A. (2001). The Drosophila melanogaster Malpighian tubule. Adv. Insect Physiol. 28, 1-83.
24. Dow, J. A. T. and Davies, S. A. (2003). Integrative physiology and functional genomics of epithelial function in a genetic model organism. Physiol. Rev. 83, 687-729.
25. Drysdale, R. (2008). FlyBase: a database for the Drosophila research community. Methods Mol. Biol. 420, 45-59.
26. + channels in Drosophila melanogaster renal function. J. Exp. Biol. 208, 3771-3783.
27. Evans, J. M., Day, J. P., Cabrero, P., Dow, J. A. and Davies, S. A. (2008). A new role for a classical gene: white transports cyclic GMP. J. Exp. Biol. 211, 890-899.
28. Gaertner, L. S. and Morris, C. E. (1999). Accumulation of daunomycin and fluorescent dyes by drug-transporting Malpighian tubule cells of the tobacco hornworn, Manduca sexta. Tissue Cell 31, 185-194.
29. Gaertner, L. S., Murray, C. L. and Morris, C. E. (1998). Transepithelial transport of nicotine and vinblastine in isolated malpighian tubules of the tobacco hornworm (Manduca sexta) suggests a P-glycoprotein-like mechanism. J. Exp. Biol. 201, 2637-2645.
30. Giannakou, M. E. and Dow, J. A. T. (2001). Characterization of the Drosophila melanogaster alkali-metal/proton exchanger (NHE) gene family. J. Exp. Biol. 204, 3703-3716.
31. + V-ATPases. J. Exp. Biol. 200, 203-216.
32. Harvey, W. R., Cioffi, M. and Wolfersberger, M. G. (1981). Portasomes as coupling factors in active ion transport and oxidative phosphorylation. Am. Zool. 21, 775-791.
33. Harvey, W. R., Cioffi, M., Dow, J. A. T. and Wolfersberger, M. G. (1983). Potassium ion transport ATPase in insect epithelia. J. Exp. Biol. 106, 91-117.
34. Hilliker, A., Duyf, B., Evans, D. and Phillips, J. (1992). Urate-null rosy mutants of Drosophila melanogaster are hypersensitive to oxygen stress. Proc. Natl. Acad. Sci. USA 89, 4343-4347.
35. Hoffmann, J. A. (1995). Innate immunity of insects. Curr. Opin. Immunol. 7, 4-10.
36. - conductance. J. Exp. Biol. 207, 2599-2609.
37. Kamleh, M. A., Hobani, Y., Dow, J. A. and Watson, D. G. (2008). Metabolomic profiling of Drosophila using liquid chromatography Fourier transform mass spectrometry. FEBS Lett. 582, 2916-2922.
38. +-ATPase cause renal tubular acidosis with sensorineural deafness. Nat. Genetics 21, 84-90.
39. Kell, D. B. (2004). Metabolomics and systems biology: making sense of the soup. Curr. Opin. Microbiol. 7, 296-307.
40. Kerr, M., Davies, S. A. and Dow, J. A. T. (2004). Cell-specific manipulation of second messengers; a toolbox for integrative physiology in Drosophila. Curr. Biol. 14, 1468-1474.
41. Kidwell, M. G., Kidwell, J. F. and Sved, J. A. (1977). Hybrid dysgenesis in Drosophila melanogaster: a syndrome of aberrant traits including mutation, sterility and male recombination. Genetics 86, 813-833.
42. +-ATPase to basolateral ion transport in Malpighian tubules of Drosophila melanogaster. J. Exp. Biol. 202, 1561-1570.
43. Linton, S. M. and O'Donnell, M. J. (2000). Novel aspects of the transport of organic anions by the malpighian tubules of Drosophila melanogaster. J. Exp. Biol. 203, 3575-3584.
44. Maddrell, S. H. P. (1971). The mechanisms of insect excretory systems. Adv. Insect Physiol. 8, 199-331.
45. Maddrell, S. H. P. and O'Donnell, M. J. (1993). Gramicidin switches transport in insect epithelia from potassium to sodium. J. Exp. Biol. 177, 287-292.
46. Maddrell, S. H. P. and Overton, J. A. (1988). Stimulation of sodium transport and fluid secretion by ouabain in an insect Malpighian tubule. J. Exp. Biol. 137, 265-276.
47. Maddrell, S. H. P., Gardiner, B. O. C., Pilcher, D. E. M. and Reynolds, S. E. (1974). Active transport by insect Malpighian tubules of acidic dyes and of acylamides. J. Exp. Biol. 61, 357-377.
48. McCarron, M., O'Donnell, J., Chovnick, A., Bhullar, B. S., Hewitt, J. and Candido, E. P. (1979). Organization of the rosy locus in Drosophila melanogaster: further evidence in support of a cis-acting control element adjacent to the xanthine dehydrogenase structural element. Genetics 91, 275-293.
49. McGettigan, J., McLennan, R. K., Broderick, K. E., Kean, L., Allan, A. K., Cabrero, P., Regulski, M. R., Pollock, V. P., Gould, G. W., Davies, S. A. et al. (2005). Insect renal tubules constitute a cell-autonomous immune system that protects the organism against bacterial infection. Insect Biochem. Mol. Biol. 35, 741-754.
50. Meredith, J., Moore, L. and Scudder, G. G. (1984). Excretion of ouabain by Malpighian tubules of Oncopeltus fasciatus. Am. J. Physiol. 246, R705-R715.
51. Mitchell, H. K. and Glassman, E. (1959). Hypoxanthine in rosy and maroon-like mutants of Drosophila melanogaster. Science 129, 268.
52. Moe, O. W. (2006). Uric acid nephrolithiasis: proton titration of an essential molecule? Curr. Opin. Nephrol. Hypertens. 15, 366-373.
53. Noe, B., Hagenbuch, B., Stieger, B. and Meier, P. (1997). Isolation of a multispecific organic anion and cardiac glycoside transporter from rat brain. Proc. Natl. Acad. Sci. USA 94, 10346-10350.
54. O'Donnell, M. J. and Rheault, M. R. (2005). Ion-selective microelectrode analysis of salicylate transport by the Malpighian tubules and gut of Drosophila melanogaster. J. Exp. Biol. 208, 93-104.
55. O'Donnell, M. J. and Spring, J. H. (2000). Modes of control of insect Malpighian tubules: synergism, antagonism, cooperation and autonomous regulation. J. Insect Physiol. 46, 107-117.
56. Okech, B. A., Boudko, D. Y., Linser, P. J. and Harvey, W. R. (2008). Cationic pathway of pH regulation in larvae of Anopheles gambiae. J. Exp. Biol. 211, 957-968.
57. Quinlan, M. C. and O'Donnell, M. J. (1998). Anti-diuresis in the blood-feeding insect Rhodnius prolixus Stal: antagonistic actions of cAMP and cGMP and the role of organic acid transport. J. Insect Physiol. 44, 561-568.
58. Radford, J. C., Davies, S. A. and Dow, J. A. T. (2002). Systematic GPCR analysis in Drosophila melanogaster identifies a leucokinin receptor with novel roles. J. Biol. Chem. 277, 38810-38817.
59. Rheault, M. R., Plaumann, J. S. and O'Donnell, M. J. (2006). Tetraethylammonium and nicotine transport by the Malpighian tubules of insects. J. Insect Physiol. 52, 487-498.
60. + antiporter (NHA) from a metazoan, Anopheles gambiae. J. Exp. Biol. 210, 3848-3861.
61. Rodriguez-Soriano, J. (1998). Bartter and related syndromes: the puzzle is almost solved. Pediatr. Nephrol. 12, 315-327.
62. Rosay, P., Davies, S. A., Yu, Y., Sozen, M. A., Kaiser, K. and Dow, J. A. T. (1997). Cell-type specific calcium signalling in a Drosophila epithelium. J. Cell Sci. 110, 1683-1692.
63. Rosenstiel, P., Jacobs, G., Till, A. and Schreiber, S. (2008). NOD-like receptors: Ancient sentinels of the innate immune system. Cell. Mol. Life Sci. 65, 1361-1377.
64. Rubin, G. M. and Lewis, E. B. (2000). A brief history of Drosophila's contributions to genome research. Science 287, 2216-2218.
65. Rubin, G. M. and Spradling, A. C. (1983). Vectors for P element-mediated gene transfer in Drosophila. Nucleic Acids Res. 11, 6341-6351.
66. Ruiz-Sanchez, E., Van Walderveen, M. C., Livingston, A. and O'Donnell, M. J. (2007). Transepithelial transport of salicylate by the Malpighian tubules of insects from different orders. J. Insect Physiol. 53, 1034-1045.
67. Sanders, H. R., Evans, A. M., Ross, L. S. and Gill, S. S. (2003). Blood meal induces global changes in midgut gene expression in the disease vector, Aedes aegypti. Insect Biochem. Mol. Biol. 33, 1105-1122.
68. Schweikl, H., Klein, U., Schindlebeck, M. and Wieczorek, H. (1989). A vacuolar-type ATPase, partially purified from potassium transporting plasma membranes of tobacco hornworm midgut. J. Biol. Chem. 264, 11136-11142.
69. Shafer, O. T., Kim, D. J., Dunbar-Yaffe, R., Nikolaev, V. O., Lohse, M. J. and Taghert, P. H. (2008). Widespread receptivity to neuropeptide PDF throughout the neuronal circadian clock network of Drosophila revealed by real-time cyclic AMP imaging. Neuron 58, 223-237.
70. Sözen, M. A., Armstrong, J. D., Yang, M. Y., Kaiser, K. and Dow, J. A. T. (1997). Functional domains are specified to single-cell resolution in a Drosophila epithelium. Proc. Natl. Acad. Sci. USA 94, 5207-5212.
71. Spradling, A. C., Stern, D., Kiss, I., Roote, J., Laverty, T. and Rubin, G. M. (1995). Gene disruptions using P transposable elements: an integral component of the Drosophila genome project. Proc. Natl. Acad. Sci. USA 92, 10824-10830.
72. Terhzaz, S., Southall, T. D., Lilley, K. S., Kean, L., Allan, A. K., Davies, S. A. and Dow, J. A. T. (2006). Differential gel electrophoresis and transgenic mitochondrial calcium reporters demonstrate spatiotemporal filtering in calcium control of mitochondria. J. Biol. Chem. 281, 18849-18858.
73. Torrie, L. S., Radford, J. C., Southall, T. D., Kean, L., Dinsmore, A. J., Davies, S. A. and Dow, J. A. T. (2004). Resolution of the insect ouabain paradox. Proc. Natl. Acad. Sci. USA 101, 13689-13693.
74. Tzou, P., Ohresser, S., Ferrandon, D., Capovilla, M., Reichhart, J. M., Lemaitre, B., Hoffmann, J. A. and Imler, J. L. (2000). Tissue-specific inducible expression of antimicrobial peptide genes in Drosophila surface epithelia. Immunity 13, 737-748.
75. Wang, J., Kean, L., Yang, J., Allan, A. K., Davies, S. A., Herzyk, P. and Dow, J. A. T. (2004). Function-informed transcriptome analysis of Drosophila renal tubule. Genome Biol. 5, R69.
76. Wessing, A. and Eichelberg, D. (1978). Malpighian tubules, rectal papillae and excretion. In The Genetics and Biology of Drosophila, vol. 2c (ed. A. Ashburner and T. R. F. Wright), pp. 1-42. London: Academic Press.
77. Wieczorek, H. and Harvey, W. R. (1995). Energization of animal plasma membranes by the proton-motive force. Physiol. Zool. 68, 15-23.
78. + antiport in an animal plasma membrane. J. Biol. Chem. 266, 15340-15347.
79. Wieczorek, H., Brown, D., Grinstein, S., Ehrenfeld, J. and Harvey, W. R. (1999). Animal plasma membrane energization by proton motive V-ATPases. BioEssays 21, 637-648.
80. Worcester, E. M. and Coe, F. L. (2008). Nephrolithiasis. Prim. Care. 35, 369-391.
81. Xu, W. and Marshall, A. T. (1999). X-ray microanalysis of the Malpighian tubules of the black field cricket Teleogryllus oceanicus: the roles of NaK ATPase and the NaK2Cl cotransporter. J. Insect Physiol. 45, 885-893.
82. Yang, J., McCart, C., Woods, D. J., Terhzaz, S., Greenwood, K. G., ffrench-Constant, R. H. and Dow, J. A. T. (2007). A Drosophila systems approach to xenobiotic metabolism. Physiol. Genomics 30, 223-231.