A new role for a classical gene: White transports cyclic GMP

Journal of Experimental Biology

Volumn 211, Issue 6, 2008, Pages 890-899

  Evans, Jennifer M ^a   Day, Jonathan P ^a   Cabrero, Pablo ^a   Dow, Julian A T ^a   Davies, Shireen Anne ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

ABCC; ABCG; Cyclic nucleotide; Functional genomics; Malpighian tubule; Transporters

Indexed keywords

ABC TRANSPORTER; BACTERIAL PROTEIN; COMPLEMENTARY DNA; CYCLIC AMP; CYCLIC GMP; DROSOPHILA PROTEIN; EYE PROTEIN; HYBRID PROTEIN; PHOTOPROTEIN; PRIMER DNA; UNCLASSIFIED DRUG; WHITE PROTEIN, DROSOPHILA; YELLOW FLUORESCENT PROTEIN, BACTERIA;

ACTIVE TRANSPORT; ANIMAL; ARTICLE; DROSOPHILA MELANOGASTER; FEMALE; GENE; GENETICS; IMMUNOHISTOCHEMISTRY; MALE; MALPIGHIAN TUBULE; METABOLISM; MUTATION; NUCLEOTIDE SEQUENCE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TISSUE DISTRIBUTION; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ATP-BINDING CASSETTE TRANSPORTERS; BACTERIAL PROTEINS; BASE SEQUENCE; BIOLOGICAL TRANSPORT, ACTIVE; CYCLIC AMP; CYCLIC GMP; DNA PRIMERS; DNA, COMPLEMENTARY; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EYE PROTEINS; FEMALE; GENES, INSECT; IMMUNOHISTOCHEMISTRY; LUMINESCENT PROTEINS; MALE; MALPIGHIAN TUBULES; MUTATION; RECOMBINANT FUSION PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TISSUE DISTRIBUTION;

EID: 42549131914     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.014837     Document Type: Article

References (46)

1. Ashman, D. F., Upton, R., Melicow, M. M. and Price, T. D. (1963). Isolation of adenosine 3′ , 5′-monophosphate and guanosine 3′ , 5′-monophosphate from rat urine. Biochem. Biophys. Res. Commun. 11, 330-334.
2. Broderick, K. E., Kean, L., Dow, J. A. T., Pyne, N. J. and Davies, S. A. (2004) Ectopic expression of bovine type 5 phosphodiesterase confers a renal phenotype in Drosophila. J. Biol. Chem. 279, 8159-8168.
3. Cabrero, P., Radford, J. C., Broderick, K. E., Veenstra, J., Spana, E., Davies, S. and Dow, J. A. T. (2002). The CRF gene of Drosophila melanogaster encodes a diuretic peptide that activates cAMP signalling. J. Exp. Biol. 205, 3799-3807.
4. Castanys-Munoz, E., Alder-Baerens, N., Pomorski, T., Gamarro, F. and Castanys, S. (2007). A novel ATP-binding cassette transporter from Leishmania is involved in transport of phosphatidylcholine analogues and resistance to alkyl-phospholipids. Mol. Microbiol. 64, 1141-1153.
5. Chintapalli, V. R., Wang, J. and Dow, J. A. (2007). Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat. Genet. 39, 715-720.
6. Coast, G. M., Webster, S. G., Schegg, K. M., Tobe, S. S. and Schooley, D. A. (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.
7. 2b, a cardioacceleratory peptide, is present in Drosophila and stimulates tubule fluid secretion via cGMP. Am. J. Physiol. 269, R1321-R1326.
8. Day, J. P., Houslay, M. D. and Davies, S. A. (2006). A novel role for a Drosophila homologue of cGMP-specific phosphodiesterase in the active transport of cGMP. Biochem. J. 393, 481-488.
9. Dazert, P., Meissner, K., Vogelgesang, S., Heydrich, B., Eckel, L., Bohm, M., Warzok, R., Kerb, R., Brinkmann, U., Schaeffeler, E. et al. (2003). Expression and localization of the multidrug resistance protein 5 (MRP5/ABCC5), a cellular export pump for cyclic nucleotides, in human heart. Am. J. Pathol. 163, 1567-1577.
10. Dow, J. A. T. and Davies, S. A. (2003). Integrative physiology, functional genomics and epithelial function in a genetic model organism. Physiol. Rev. 83, 687-729.
11. Dow, J. A. and Davies, S. A. (2005). The Malpighian tubule: rapid insights from post-genomic biology. J. Insect Physiol. 52, 365-378.
12. Dow, J. A., Maddrell, S. H., Gortz, A., Skaer, N. J., Brogan, S. and Kaiser, K. (1994a). The Malpighian tubules of Drosophila melanogaster: a novel phenotype for studies of fluid secretion and its control. J. Exp. Biol. 197, 421-428.
13. Dow, J. A. T., Maddrell, S. H., Davies, S. A., Skaer, N. J. and Kaiser, K. (1994b). A novel role for the nitric oxide-cGMP signaling pathway: the control of epithelial function in Drosophila. Am. J. Physiol. 266, R1716-R1719.
14. Doyle, L., Yang, W., Abruzzo, L., Krogmann, T., Gao, Y., Rishi, A. and Ross, D. (1998). A multidrug resistance transporter from human MCF-7 breast cancer cells. Proc. Natl. Acad. Sci. USA 95, 15665-15670.
15. Dreesen, T., Johnson, D. and Henikoff, S. (1988). The brown protein of Drosophila melanogaster is similar to the white protein and to components of active transport complexes. Mol. Cell. Biol. 8, 5206-5215.
16. Evans, J. (2007). From microarrays to renal transporter function in Drosophila melanogaster Malpighian tubules. PhD thesis, University of Glasgow, UK.
17. + channels in Drosophila melanogaster renal function. J. Exp. Biol. 208, 3771-3783.
18. Howells, A., Summers, K. and Ryall, R. (1977). Developmental patterns of 3-hydroxykynurenine accumulation in white and various other eye color mutants of Drosophila melanogaster. Biochem. Genet. 15, 1049-1059.
19. Jedlitschky, G., Tirschmann, K., Lubenow, L. E., Nieuwenhuis, H. K., Akkerman, J. W., Greinacher, A. and Kroemer, H. K. (2004). The nucleotide transporter MRP4 (ABCC4) is highly expressed in human platelets and present in dense granules, indicating a role in mediator storage. Blood 104, 3603-3610.
20. Klokouzas, A., Wu, C., van Veen, H., Barrand, M. and Hladky, S. (2003). cGMP and glutathione-conjugate transport in human erythrocytes. Eur. J. Biochem. 270, 3696-3708.
21. Koepsell, H. (2004). Polyspecific organic cation transporters: their functions and interactions with drugs. Trends Pharmacol. Sci. 25, 375-381.
22. +-ATPase to basolateral ion transport in Malpighian tubules of Drosophila melanogaster. J. Exp. Biol. 202, 1561-1570.
23. Mackenzie, S., Brooker, M., Gill, T., Cox, G., Howells, A. and Ewart, G. (1999). Mutations in the white gene of Drosophila melanogaster affecting ABC transporters that determine eye colouration. Biochem. Biophys. Acta 1419, 173-185.
24. Mackenzie, S., Howells, A., Cox, G. and Ewart, G. (2000). Sub-cellular localisation of the white/scarlet ABC transporter to pigment granule membranes within the compound eye of Drosophila melanogaster. Genetica 108, 239-252.
25. MacPherson, M. R., Pollock, V. P., Broderick, K. B., Kean, L., O'Connell, F. C., Dow, J. A. T. and Davies, S.-A. (2001). Model organisms: new insights into ion channel and transporter function: L-type calcium channels regulate epithelial fluid transport in Drosophila melanogaster. Am. J. Physiol. 280, C394-C407.
26. MacPherson, M. R., Lohmann, S. M. and Davies, S. A. (2004). Analysis of Drosophila cGMP-dependent protein kinases and assessment of their in vivo roles by targeted expression in a renal transporting epithelium. J. Biol. Chem. 279, 40026-40034.
27. 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.
28. McGettigan, J., McLennan, R. K., Broderick, K. E., Kean, L., Allan, A. K., Cabrera, 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.
29. Morgan, T. H. (1910). Sex limited inheritance in Drosophila. Science 32, 120-122.
30. O'Donnell, M. J., Dow, J. A. T., Huesmann, G. R., Tublitz, N. J. and Maddrell, S. H. P. (1996). Separate control of anion and cation transport in Malpighian tubules of Drosophila melanogaster. J. Exp. Biol. 199, 1163-1175.
31. Polgar, O., Ozvegy-Laczka, C., Robey, R., Morisaki, K., Okada, M., Tamaki, A., Koblos, G., Elkind, N., Ward, Y., Dean, M. et al. (2006). Mutational studies of G553 in TM5 of ABCG2: a residue potentially involved in dimerization. Biochemistry 45, 5251-5260.
32. Pollock, V. P., McGettigan, J., Cabrero, P., Maudlin, I. M., Dow, J. A. and Davies, S. A. (2004). Conservation of capa peptide-induced nitric oxide signalling in Diptera. J. Exp. Biol. 207, 4135-4145.
33. Riegel, J. A., Maddrell, S. H., Farndale, R. W. and Caldwell, F. M. (1998). Stimulation of fluid secretion of malpighian tubules of Drosophila melanogaster Meig. by cyclic nucleotides of inosine, cytidine, thymidine and uridine. J. Exp. Biol. 201, 3411-3418.
34. Ritter, C. A., Jedlitschky, G., Meyer zu Schwabedissen, H., Grube, M., Kock, K. and Kroemer, H. K. (2005). Cellular export of drugs and signaling molecules by the ATP-binding cassette transporters MRP4 (ABCC4) and MRP5 (ABCC5). Drug Metab. Rev. 37, 253-278.
35. Sekine, T., Cha, S. and Endou, H. (2000). The multispecific organic anion transporter (OAT) family. Pflugers Arch. 440, 337-350.
36. Shulenin, S., Schriml, L. M., Remaley, A. T., Fojo, S., Brewer, B., Allikmets, R. and Dean, M. (2001). An ATP-binding cassette gene (ABCG5) from the ABCG (White) gene subfamily maps to human chromosome 2p21 in the region of the Sitosterolemia locus. Cytogenet. Cell Genet. 92, 204-208.
37. Sullivan, D. and Sullivan, M. (1975). Transport defects as the physiological basis for eye color mutants of Drosophila melanogaster. Biochem. Genet. 13, 603-613.
38. Sullivan, D., Bell, L., Paton, D. and Sullivan, M. C. (1979). Purine transport by malpighian tubules of pteridine-deficient eye color mutants of Drosophila melanogaster. Biochem. Genet. 17, 565-573.
39. Sullivan, D., Bell, L., Paton, D. and Sullivan, M. C. (1980). Genetic and functional analysis of tryptophan transport in Malpighian tubules of Drosophila. Biochem. Genet. 18, 1109-1130.
40. Sundkvist, E., Jaeger, R. and Sager, G. (2002). Pharmacological characterization of the ATP-dependent low K(m) guanosine 3′,5′- cyclic monophosphate (cGMP) transporter in human erythrocytes. Biochem. Pharmacol. 63, 945-949.
41. van Aubel, R., Smeets, P., Peters, J., Bindels, R. and Russel, F. (2002). The MRP4/ABCC4 gene encodes a novel apical organic anion transporter in human kidney proximal tubules: putative efflux pump for urinary cAMP and cGMP. J. Am. Soc. Nephrol. 13, 595-603.
42. Volk, E. and Schneider, E. (2003). Wild-type breast cancer resistance protein (BCRP/ABCG2) is a methotrexate polyglutamate transporter. Cancer Res. 63, 5538-5543.
43. Wang, J., Kean, L., Yang, J., Allan, A. K., Davies, S. A., Herzyk, P. and Dow, J. A. (2004). Function-informed transcriptome analysis of Drosophila renal tubule. Genome Biol. 5, R69.
44. Wessing, A. and Eichelberg, D. (1968). Fluorescing substances from the Malpighian tubules of wild-type and various eye color mutants of Drosophila melanogaster. Z. Naturforsch. B 23, 376-386.
45. 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.
46. Zachar, Z. and Bingham, P. M. (1982). Regulation of white locus expression: the structure of mutant alleles at the white locus of Drosophila melanogaster. Cell 30, 529-541.