Biochemical Genetics

, Volume 29, Issue 7–8, pp 365–388

Biochemical and physiological studies of soluble esterases fromDrosophila melanogaster

  • Marion J. Healy
  • Mira M. Dumancic
  • John G. Oakeshott


Twenty-two soluble esterases have been identified inD. melanogaster by combining the techniques of native polyacrylamide gel electrophoresis and isoelectric focusing. The sensitivity of each isozyme to three types of inhibitors (organophosphates, eserine sulfate, and sulfydryl reagents) identified 10 as carboxylesterases, 6 as cholinesterases, and 3 as acetylesterases. Three isozymes could not be classified and no arylesterases were identified. The carboxyl- and cholinesterases could each be further divided into two subclasses on the basis of inhibition by organophosphates and sulfhydryl reagents, respectively. Cholineand acetylesterases have characteristic substrate preferences but both subclasses of carboxylesterases are heterogeneous in substrate utilization. Subclass 2 carboxylesterases exhibit diverse temporal expression patterns, with subclass 1 carboxylesterases generally found in larvae and subclass 1 cholinesterases and acetylesterases more characteristic of pupae and adults. Tissues showing the greatest number of isozymes are larval body wall (eight) and digestive tract (six in larvae, six in adults). Carboxylesterases are distributed across a wide range of tissues, but subclass 1 cholinesterases are generally associated with neural or neurosecretory tissues and subclass 2 cholinesterases with digestive tissues.

Key words

Drosophila melanogaster esterases biochemical properties expression pattern 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Ahmad, S. (1976). Larval and adult housefly carboxylesterase: Isozymic composition and tissue pattern.Insect Biochem. 6541.Google Scholar
  2. Akam, M. E., Roberts, D. B., Richards, G. P., and Ashburner, M. (1978).Drosophila: the genetics of two major larval proteins.Cell 13215.Google Scholar
  3. Aldridge, W. N. (1953). Serum esterases. 1. Two types of esterase (A and B) hydrolysing p-nitrophenyl acetate, propionate and butyrate, and a method for their determination.Biochemistry 53110.Google Scholar
  4. Arpagaus, M., Fournier, D., and Toutant, J. P. (1988). Analysis of acetylcholinesterase molecular forms during the development ofDrosophila melanogaster. Evidence for the existence of an amphiphilic monomer.Insect Biochem. 18539.Google Scholar
  5. Ashour, M. A., Harshman, L. G., and Hammock, B. D. (1987). Malathion toxicity and carboxylesterase activity inDrosophila melanogaster.Pestic. Biochem. Physiol. 2997.Google Scholar
  6. Augustinsson, K. B. (1968). The evolution of esterases in vertebrates. In Their, N. V., and Roche, J. (eds.),Homologous Enzymes and Biochemical Evolution Gordon and Breach, New York, p. 299.Google Scholar
  7. Beckman, L., and Johnson, F. M. (1964). Esterase variation inDrosophila melanogaster.Hereditas 51212.Google Scholar
  8. Brady, J. P., Richmond, R. C., and Oakeshott, J. G. (1990). Cloning of the esterase-5 locus fromDrosophila pseudoobscura and comparison with the homologous locus inD. melanogaster.Mol. Biol. Evol. 7525.Google Scholar
  9. Cavener, D., Otteson, D. C., and Kaufman, T. C. (1986). A rehabilitation of the genetic map of the 84B-D region ofDrosophila melanogaster.Genetics 114111.Google Scholar
  10. Chatonnet, A., and Lockridge, O. (1989). Comparison of butyrylcholinesterase and acetylcholinesterase.Biochem. J. 260625.Google Scholar
  11. Coates, P. M., Mestriner, M. A., and Hopkinson, D. A. (1975). A preliminary genetic interpretation of the esterase isozymes of human tissue.Ann. Hum. Genet. 391.Google Scholar
  12. Collet, C., Nielsen, K. M., Russell, R. J., Karl, M., Oakeshott, J. G., and Richmond, R. C. (1990). Molecular analysis of duplicated esterase genes inDrosophila melanogaster.Mol. Biol. Evol. 79.Google Scholar
  13. Cooke, P. H., Richmond, R. C., and Oakeshott, J. G. (1987). High resolution electrophoretic variation at the esterase-6 locus in a natural population ofDrosophila melanogaster.Heredity 59259.Google Scholar
  14. Dewhurst, S. A., McCaman, R. E., and Kaplan, W. P. (1970). The time course of development of acetylcholinesterase and choline acetyltransferase inDrosophila melanogaster.Biochem. Genet. 4499.Google Scholar
  15. Foster, G. G., Whitten, M. J., Konovalov, C., Arnold, J. T. A., and Maffi, G. (1981). Autosomal genetic maps of the Australian sheep blowfly,Lucilia cuprina dorsalis R.D. (Diptera: Calliphoridae), and possible correlations with the linkage maps ofMusca domestica L. andDrosophila melanogaster (Mg).Genet. Res. 3755.Google Scholar
  16. Hall, L., and Spierer, P. (1986). TheAce locus ofDrosophila melanogaster: Structural gene for acetylcholinesterase with an unusual 5′ leader.EMBO J. 52949.Google Scholar
  17. Hammock, B. D. (1985). Regulation of juvenile hormone titer: degradation. In Kerkut, G. A., and Gilbert, L. I. (eds.),Comprehensive Insect Physiology, Biochemistry and Pharmacology Pergamon Press, Oxford, Vol. 7, p. 431.Google Scholar
  18. Hammock, B. D., Abdel-Aal, Y. A. I., Mullin, C. A., Hanzlik, T. N., and Roe, R. M. (1984). Substituted thiotrifluoropropanones as potent selective inhibitors of juvenile hormone esterase.Pestic. Biochem. Physiol. 22209.Google Scholar
  19. Hanzlik, T. N., Abdel-Aal, Y. A. I., Harshman, L. G., and Hammock, B. D. (1989). Isolation and sequencing of cDNA clones coding for juvenile hormone esterase fromHeliothis virescens. J. Biol. Chem. 26412419.Google Scholar
  20. Hedrich, H. J., and von Deimling, O. (1987). Re-evaluation of LG V of the rat and assignment of 12 carboxylesterases to two gene clusters.J. Hered. 7892.Google Scholar
  21. Hedrich, H. J., von Deimling, O., and Kluge, R. (1987). Biochemical genetics ofEs-14 (formerly Es-Si) and a new esterase variation,Es-15, of the laboratory rat (Rattus norvegicus): Biochemistry, tissue expression and linkage toEs-1 in linkage group V.Biochem. Genet. 2579.Google Scholar
  22. Heymann, E. (1980). Carboxylesterase and amidases. In Jakoby, W. (ed.),Enzymatic Basis of Detoxication Academic Press, New York, Vol II, p. 291.Google Scholar
  23. Hughes, P. B., and Raftos, D. A. (1985). Genetics of an esterase associated with resistance to organophosphorus insecticides in the sheep blowfly,Lucilia cuprina (Wiedemann) (Diptera: Calliphoridae).Bull. Entomol. Res. 75535.Google Scholar
  24. Kissel, J. A., Fontaine, R. N., Turck, C. W., Brockman, H. L., and Hui, D. Y. (1989). Molecular cloning and expression of cDNA for rat pancreatic cholesterol esterase.Biochim. Biophys. Acta 1006227.Google Scholar
  25. Krisch, K. (1971). Carboxylic ester hydrolases. In Boyer, P. D. (ed.),The Enzymes Academic Press, New York, p. 43.Google Scholar
  26. Mane, S. D., Tepper, C. S., and Richmond, R. C. (1983). Studies of esterase 6 inDrosophila melanogaster. XIII. Purification and characterisation of the two major isozymes.Biochem. Genet. 211019.Google Scholar
  27. Markwell, M. A., Haas, S. M., Bieber, L. L., and Tolbert, N. E. (1978). A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples.Anal. Biochem. 87206.Google Scholar
  28. Mitchell, H. K., and Mitchell, A. (1964). Mass culture and age selection inDrosophila.Dros. Info. Serv. 39135.Google Scholar
  29. Morton, R. A., and Singh, R. S. (1980). Variation inDrosophila acetylcholinesterase.Biochem. Genet. 18439.Google Scholar
  30. Myers, M., Richmond, R. C., and Oakeshott, J. G. (1988). On the origins of esterases.Mol. Biol. Evol. 5113.Google Scholar
  31. Oakeshott, J. G., Collet, C., Phillis, R. W., Nielsen, K. M., Russell, R. J. Chambers, G. K., Ross, V., and Richmond, R. C. (1987). Molecular cloning and characterisation of esterase-6, a serine hydrolase ofDrosophila.Proc. Natl. Acad. Sci. USA 843359.Google Scholar
  32. Oakeshott, J. G., Healy, M. J., and Game, A. Y. (1990). Regulatory evolution of β-carboxyl esterases inDrosophila. In Barker, J. S. F., Starmer, W. T., and MacIntyre, R. J. (eds.),Ecological and Evolutionary Genetics of Drosophila Plenum, New York, p. 359.Google Scholar
  33. O'Brien, S. J., and MacIntyre, R. J. (1978). Genetics and biochemistry of enzymes and specific proteins ofDrosophila. In Ashburner, M., and Wright, T. R. F. (eds.),The Genetics and Biology of Drosophila Academic Press, London, Vol. 2a, p. 395.Google Scholar
  34. Ogita, Z., and Kasai, T. (1965). Genetic control of multiple esterases inMusca domestica. Japan.J. Genet. 401.Google Scholar
  35. Olson, P. F., Fessler, L. I., Nelson, R. E., Sterne, R. E., Campbell, A. G., and Fessler, J. H. (1990). Glutactin, a novelDrosophila basement membrane-related glycoprotein with sequence similarity to serine esterases.EMBO J. 91219.Google Scholar
  36. Parker, A. G., Russell, R. J., Delves, A. C., and Oakeshott, J. G. (1991). Biochemistry and physiology of esterases in organophosphate suspectible and resistant strains of the Australian sheep blowfly,Lucilia cuprina. Pestic Biochem. Physiol. (in press).Google Scholar
  37. Peters, J. (1982). Nonspecific esterases ofMus musculus.Biochem. Genet. 20585.Google Scholar
  38. Rauschenbach, I. Y., Lukashina, N. S., and Korochkin, L. I. (1984). The genetics of esterases inDrosophila. VIII. The gene regulating the activity of JH-esterase inD. virilis.Biochem. Genet. 2265.Google Scholar
  39. Richmond, R. C., Nielsen, K. M., Brady, J. P., and Snella, E. M. (1990). Physiology, biochemistry and molecular biology of theEst-6 locus inDrosophila melanogaster. In Barker, J. S. F., Starmer, W. T., and MacIntyre, R. J. (eds.),Ecological and Evolutionary Genetics of Drosophila Plenum, New York. p. 273.Google Scholar
  40. Russell, R. J., Dumancic, M. M., Foster, G. G., Weller, G. L., Healy, M. J., and Oakeshott, J. G. (1990). Insecticide resistance as a model system for studying molecular evolution. In Barker, J. S. F., Starmer, W. T., and MacIntyre, R. J. (eds.),Ecological and Evolutionary Genetics of Drosophila Plenum, New York, p. 293.Google Scholar
  41. Sheehan, K., Richmond, R. C., and Cochrane, B. J. (1979). Studies of esterase 6 inDrosophila melanogaster. III. The developmental pattern and tissue distribution.Insect Biochem. 9443.Google Scholar
  42. Small, D. H. (1990). Non-cholinergic actions of acetylcholinesterases: proteases regulating cell growth and development?TIBS 15213.Google Scholar
  43. van Zutphen, L. F. M., den Bieman, M. G. C., von Deimling, O., and Fox, R. R. (1987). Genetics of a tissue esterase polymorphism (Est-6) in the rabbit (Oryctolagus cuniculus).Biochem. Genet. 25335.Google Scholar
  44. Vernick, K. D., Collins, F. H., Seeley, D. C., Gwadz, R. W., and Miller, L. H. (1988). The genetics and expression of an esterase locus inAnopheles gambiae.Biochem. Genet. 26367.Google Scholar
  45. Vogt, R. G., and Riddiford, L. M. (1981). Pheromone binding and inactivation by moth antennae.Nature 293161.Google Scholar
  46. Vogt, R. G., and Riddiford, L. M. (1986). Scale esterase: A pheromone-degrading enzyme from scales of silk mothAntheraea polyphemus.J. Chem. Ecol. 12469.Google Scholar
  47. von Deimling, O. H. (1984). Esterase-23 (Es-23): Characterization of a new carboxylesterase isozyme (EC of the house mouse, genetically linked toES-2 on chromosome 8.Biochem. Genet. 22769.Google Scholar
  48. von Deimling, O. H., Gaa, A., and Simon, G. G. (1988). Esterase-18 (ES-18) of the house mouse (Mus musculus): Biochemical characterization and genetics of an allozyme linked to chromosome 19.Biochem. Genet. 26617.Google Scholar
  49. Waterhouse, W. J. (1981). An esterase of bacterial origin inDrosophila montana.Biochem. Genet. 19227.Google Scholar
  50. Wright, T. R. F. (1963). The genetics of an esterase inDrosophila melanogaster.Genetics 48787.Google Scholar
  51. Zador, E., Gausz, J., and Maroy, P. (1986). Tissue-specific expression of the acetylcholinesterase gene inDrosophila melanogaster embryos.Mol. Gen. Genet. 204469.Google Scholar
  52. Zador, E., and Maroy, P. (1987). Subcellular localization of isozyme variants of acetylcholinesterase during the life cycle ofDrosophila melanogaster.Biochem. Genet. 25779.Google Scholar
  53. Ziegler, R., Whyard, S., Downe, A. E. R., Wyatt, G. R., and Walker, V. K. (1987). General esterase, malathion carboxylesterase and malathion resistance inCulex tarsails.Pest. Biochem. Physiol. 28279.Google Scholar
  54. Zingde, S., Rodrigues, V., Joshi, S. M., and Krishnan, K. S. (1983). Molecular properties ofDrosophila acetylcholinesterase.J. Neurochem. 411243.Google Scholar

Copyright information

© Plenum Publishing Corporation 1991

Authors and Affiliations

  • Marion J. Healy
    • 1
  • Mira M. Dumancic
    • 1
  • John G. Oakeshott
    • 1
  1. 1.CSIRO Division of EntomologyCanberra ACTAustralia

Personalised recommendations