Skip to main content
Log in

Sub-cellular Localisation of the White/Scarlet ABC Transporter to Pigment Granule Membranes Within the Compound Eye of Drosophila Melanogaster

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

The white, scarlet, and browngenes of Drosophila melanogasterencode ABC transporters involved with the uptake and storage of metabolic precursors to the red and brown eye colour pigments. It has generally been assumed that these proteins are localised in the plasma membrane and transport precursor molecules from the heamolymph into the eye pigment cells. However, the immuno-electron microscopy experiments in this study reveal that the White and Scarlet proteins are located in the membranes of pigment granules within pigment cells and retinula cells of the compound eye. No evidence of their presence in the plasma membrane was observed. This result suggests that, rather than tranporting tryptophan into the cell across the plasma membrane, the White/Scarlet complex transports a metabolic intermediate (such as 3-hydroxy kynurenine) from the cytoplasm into the pigment granules. Other functional implications of this new finding are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bingham, P.M., R. Levis & G.M. Rubin, 1981. Cloning of DNA sequences from the whitelocus of Drosophila melanogasterby a novel and general method. Cell 25: 693–704.

    Article  PubMed  CAS  Google Scholar 

  • Cagan, R.L. & D.F. Ready, 1989. The emergence of order in the Drosophilapupal retina. Develop. Biol. 136: 346–362.

    Article  PubMed  CAS  Google Scholar 

  • Castagna, M., C. Shayakul, D. Trotti, V.F. Sacchi, W.R. Harvey & M.A. Hediger, 1997. Molecular characteristics of mammalian and insect amino acid transporters: implications for amino acid homeostasis. J. Exp. Biol. 200: 269–286.

    PubMed  CAS  Google Scholar 

  • Chen, H., C. Rossier, M.D. Lalioti, A. Lynn, A. Chakravarti, G. Perrin & S.E. Antonarakis, 1996. Cloning of the cDNA for a human homologue of the DrosophilaWhite gene and mapping to chromosome 21q22.3. Amer. J. Hum. Genet. 59: 66–75.

    PubMed  CAS  Google Scholar 

  • Croop, J.M., 1998. Evolutionary relationships among ABC transporters. Meth. Enzymol. 292: 101–116.

    PubMed  CAS  Google Scholar 

  • Dreeson, T.D., D.H. Johnson & S. Henikoff, 1988. The Brown protein of Drosophila melanogasteris similar to the White protein and to components of active transport complexes. Mol. Cell. Biol. 8: 5206–5215.

    Google Scholar 

  • Ewart, G.D., D. Cannell, G.B. Cox & A.J. Howells, 1994. Mutational analysis of the traffic ATPase (ABC) transporters involved in uptake of eye pigment precursors in Drosophila melanogaster. J. Biol. Chem. 269: 10370–10377.

    PubMed  CAS  Google Scholar 

  • Ewart, G.D. & A.J. Howells, 1998. ABC transporters involved in transport of eye pigment precursors in Drosophila melanogaster. Meth. Enzymol. 292: 213–224.

    PubMed  CAS  Google Scholar 

  • Fjose, A., L.C. Polito, U. Weber & W.J. Gehring 1984. Developmental expression of the whitelocus of Drosophila melanogaster. EMBO J. 3: 2087–2094.

    PubMed  CAS  Google Scholar 

  • Forrest, H.S., 1957. Pigment Cell Biology. Academic Press, New York.

    Google Scholar 

  • Harlow, E. & D. Lane, 1988. Antibodies, A Laboratory Manual. Cold Spring Harbour Laboratory, New York.

    Google Scholar 

  • Higgins, C.F., 1992. ABC transporters: frommicrooganisms toman. Ann. Rev. Cell Biol. 8: 67–113.

    PubMed  CAS  Google Scholar 

  • Höning, S., I.V. Sandoval & Figura, K.V., 1998. A di-leucine-based motif in the cytoplasmic tail of LIMP-II and tyrosinase mediates selective binding of AP-3. EMBO J. 17: 1304–1314.

    Article  PubMed  Google Scholar 

  • Howells, A.J. & R.L. Ryall, 1975. A biochemical study of the Scarleteye-color mutant of Drosophila melanogaster. Bioch Genet. 13: 273–282.

    Article  CAS  Google Scholar 

  • Howells, A.J., K.M. Summers & R.L. Ryall, 1977. Developmental patterns of 3-hydroxykynurenine accumulation in whiteand various other eye color mutants of Drosophila melanogaster. Biochem. Genetics 15: 1049–1059.

    Article  CAS  Google Scholar 

  • King, L.A. & R.D. Possee, 1992. The Baculovirus Expresssion System, A laboratory Guide. Chapman & Hall, London.

    Google Scholar 

  • Kurkulos, M., J.M. Weinberg, M.E. Pepling & S.M. Mount, 1991. Polyadenylation in copiarequires unusually distant upstream sequences. Proc. Nat. Acad. Sci. USA 88: 3038–3042.

    Article  PubMed  CAS  Google Scholar 

  • Laemmli, U.K., 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680–685.

    Article  PubMed  CAS  Google Scholar 

  • Levis, R., T. Hazelrigg & G.M. Rubin, 1985a. Effects of genomic position on the expression of transduced copies of the whitegene of Drosophila. Science 229: 558–561.

    PubMed  CAS  Google Scholar 

  • Levis, R., T. Hazelrigg & G.M. Rubin, 1985b. Separable cis-acting control elements for expression of theWhite gene of Drosophila. EMBO J. 4: 3489–3499.

    PubMed  CAS  Google Scholar 

  • Linzen, B., 1974. The tryptophan to ommochrome pathway in insects. Adv. Insect Physiol. 10: 117–245.

    CAS  Google Scholar 

  • Lloyd, V., M. Ramaswami & Krämer, H. 1998. Not just pretty eyes: Drosophilaeye-colour mutations and lysosomal delivery. Trends Cell Biol. 8: 257–259.

    Article  PubMed  CAS  Google Scholar 

  • Lu, Y.-A., P. Clavijo, M. Galantino, Z.-Y. Shen, W. Liu & J.P. Tam, 1991. Chemically unambiguous peptide immunogen: preparation, orientation and antigenicity of purified peptide conjugated to the multiple antigen peptide system. Mol. Immunol. 28: 623–630.

    Article  PubMed  CAS  Google Scholar 

  • Mackenzie, S., M.R. Brooker, T.R. Gill, G.B. Cox, A.J. Howells & G.D. Ewart, 1999. Mutations in the whitegene of Drosophila melanogasteraffecting ABC transporters that determine eye colouration. Biochim. et Biophys. Acta 1419: 173–185.

    Article  CAS  Google Scholar 

  • McGivan, J.D. & M. Pastor-Anglada, 1994. Regulatory and molecular aspects of mammalian amino acid transport. Biochem. J. 299: 321–334.

    PubMed  CAS  Google Scholar 

  • Odorizzi, G., C.R. Cowles & S.D. Emr, 1998. The AP-3 complex: a coat of many colours. Trends Cell Biol. 8: 282–288.

    Article  PubMed  CAS  Google Scholar 

  • O'Hare, K., C. Murphy, R. Levis & G.M. Rubin, 1984. DNA Sequence of the whitelocus of Drosophila melanogaster. J. Mol. Biol. 180: 437–455.

    Article  PubMed  Google Scholar 

  • Ooi, C.E., J.E. Moreira, E.C. Dell'Angelica, G. Poy, D.A. Wassarman & J.S. Bonifacino, 1997. Altered expression of a novel adaptin leads to defective pigment granule biogenesis in the Drosophilaeye colour mutant garnet. EMBO J. 16: 4508–4518.

    Article  PubMed  CAS  Google Scholar 

  • Pepling, M. & S.M. Mount, 1990. Sequence of a cDNA from the Drosophila melanogaster whitegene. Nucleic Acids Res. 18: 1633.

    PubMed  CAS  Google Scholar 

  • Phillips, J.P. & H.S. Forrest, 1980. Ommochromes and pteridines pp. 542–611, in The Genetics and Biology of Drosophila, edited by M. Ashburner & T.R.F. Wright. Vol. 2d, Academic Press, New York and London.

    Google Scholar 

  • Potterf, S.B., J. Muler, I. Bernardini, F. Tietze, T. Kobayashi, V.J. Hearing & W.A. Gahl, 1996. Characterization of a melanosomal transport system in murine melanocytes mediating entry of the melanogenic substrate tyrosine. J. Biol. Chem. 271: 4002–4008.

    Article  PubMed  CAS  Google Scholar 

  • Refranz, P. & S. Benzer, 1989. Monoclonal antibody probes discriminate early and late mutant defects in development of the Drosophilaretina. Develop. Biol. 136: 411–429.

    Article  Google Scholar 

  • Roberts, D.B., 1986. Drosophila: A Practical Approach. IRL Press Limited, Oxford.

    Google Scholar 

  • Ryall, R.L. & A.J. Howells, 1974. Ommochrome biosynthetic pathway of Drosophila melanogaster: Variations in the levels of enzyme activities and intermediates during adult development. Insect Biochem. 6: 135–142.

    Article  Google Scholar 

  • Sambrook, J., E.F. Fritsch & T. Maniatis, 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.

    Google Scholar 

  • Savary, S., F. Denizot, M.-F. Luciani, M.-G. Mattei & G. Chimini, 1996. Molecular cloning of a mammalian ABC transporter homologous to Drosophila whitegene. Mammal. Genome 7: 673–676.

    CAS  Google Scholar 

  • Schraermeyer, U. & M. Dohms, 1993. Atypical granules in the eyes of whitemutant Drosophila melanogasterare lysosome-related organelles. Pigment Cell Res. 6: 73–84.

    PubMed  CAS  Google Scholar 

  • Shotwell, M.A. & D.L. Oxender, 1983. The regulation of neutral amino acid transport by amino acid availability in animal cells. Trends Biochem. Sci. 8: 314–316.

    Article  CAS  Google Scholar 

  • Shoup, J.R., 1966. The development of pigment granules in the eyes of wild type and mutant Drosophila melanogaster. J. Cell Biol. 29: 223–249.

    Article  PubMed  CAS  Google Scholar 

  • Simpson, F., A.A. Peden, L. Christopoulou & M.S. Robinson, 1997. Characterisation of the Adaptor-related protein complex, AP-3. J. Cell Biol. 137: 835–845.

    Article  PubMed  CAS  Google Scholar 

  • Stark, W.S. & R. Sapp, 1988. Eye color pigment granules in wildtype and mutant Drosophila melanogaster. Canadian J. Zool. 66: 1301–1308.

    Article  Google Scholar 

  • Sullivan, D.T., L.A. Bell, D.R. Paton & M.C. Sullivan, 1979. Purine transport by malpighian tubules of pteridine-deficient eye color mutants of Drosophila melanogaster. Biochem. Genet. 17: 565–573.

    Article  PubMed  CAS  Google Scholar 

  • Sullivan, D.T., L.A. Bell, D.R. Paton & M.C. Sullivan, 1980. Genetic and functional analysis of tryptophan transport in malpighian tubules of Drosophila. Biochem. Genet. 18: 1109–1131.

    Article  PubMed  CAS  Google Scholar 

  • Sullivan, D.T. & M.C. Sullivan, 1975. Transport defects as the physiological basis for eye color mutants of Drosophila melanogaster. Biochem. Genet. 13: 603–613.

    Article  PubMed  CAS  Google Scholar 

  • Summers, K.M., A.J. Howells & N.A. Pyliotis, 1982. Biology of eye pigmentation in insects. Adv. Insect Physiol. 16: 119–166.

    Article  CAS  Google Scholar 

  • Tearle, R.G., J.M. Belote, M. McKeown, B.S. Baker & A.J. Howells, 1989. Cloning and characterisation of the Scarletgene of Drosophila melanogaster. Genet. 122: 595–606.

    CAS  Google Scholar 

  • Towbin, H., T. Staehelin & J. Gordon, 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Nat. Acad. Sci. USA 76: 4350–4354.

    Article  PubMed  CAS  Google Scholar 

  • Venkateswaran, A., J.J. Repa, J.A. Lobaccaro, A. Bronson, D.J. Mangelsdorf & P.A. Edwards, 2000. Human White/murine ABC8 mRNA levels are highly induced in lipid-loaded macrophages. J. Biol. Chem. 275: 14700–14707.

    Article  PubMed  CAS  Google Scholar 

  • Wiley, K. & H.S. Forrest, 1981. Terminal synthesis of xanthommatin in Drosophila melanogaster. IV. enzymatic and nonenzymatic catalysis. Biochem. Genet. 19: 1211–1221.

    Article  PubMed  CAS  Google Scholar 

  • Yagi, S. & H. Ogawa, 1996. Effect of tryptophan metabolites on fluorescent granules in the malpighian tubules of eye color mutants of Drosophila melanogaster. Zool. Sci. 13: 97–104.

    Article  PubMed  CAS  Google Scholar 

  • Zwiebel, L.J., G. Saccone, A. Zacharopoulou, N.J. Besansky, G. Favia, F.H. Collins, C. Louis & F.C. Kafatos, 1995. The whitegene of Ceratitis capitata: a phenotypic marker for germline transformation. Science 270: 2005–2007.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mackenzie, S.M., Howells, A.J., Cox, G.B. et al. Sub-cellular Localisation of the White/Scarlet ABC Transporter to Pigment Granule Membranes Within the Compound Eye of Drosophila Melanogaster. Genetica 108, 239–252 (2000). https://doi.org/10.1023/A:1004115718597

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1004115718597

Navigation