An olfactory-specific glutathione-S-transferase in the sphinx moth Manduca sexta

Journal of Experimental Biology

Volumn 202, Issue 12, 1999, Pages 1625-1637

  Rogers, Matthew E ^a   Jani, Mudra K ^a   Vogt, Richard G ^a  

^a UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Antennal specific mRNA; Glutathione S transferase; Manduca sexta; Odorant; Odorant degrading enzyme; Olfaction; Pheromone; Sphinx moth; Xenobiotic

Indexed keywords

CHROMATOGRAPHY; GLUTATHIONE TRANSFERASE; HEXOBARBITAL; IN SITU HYBRIDIZATION; NORTHERN BLOTTING; POLYMERASE CHAIN REACTION; SPECTROMETRY; TOBACCO HORN WORM;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; DNA PRIMERS; DNA, COMPLEMENTARY; FEMALE; GLUTATHIONE TRANSFERASE; IN SITU HYBRIDIZATION; MALE; MANDUCA; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA, MESSENGER; SEQUENCE HOMOLOGY, AMINO ACID; SMELL;

INSECTA; LEPIDOPTERA; MANDUCA SEXTA; NICOTIANA TABACUM; SPHINGIDAE;

EID: 0033153407     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (74)

1. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. and Lipman, D. J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403-410.
2. Baron, J., Voigt, J. M., Whitter, T. B., Kawabata, T., Knapp, S. A., Guengerich, P. and Jakoby, W. B. (1986). Identification of intratissue sites for xenobiotic activation and detoxification. Adv. Exp. Med. Biol. 197, 119-144.
3. Ben-Arie, N., Khen, M. and Lancet, D. (1993). Glutathione S-transferase in rat olfactory epithelium: Purification, molecular properties and odorant biotransformation. Biochem. J. 292, 379-384.
4. Boeckh, J., Kaissling, K.-E. and Schneider, D. (1965). Insect olfactory receptors. Cold Spring Harbor Symp. Quant. Biol. 30, 262-280.
5. Buetler, T. M. and Eaton, D. L. (1992). Glutathione S-transferases: Amino acid sequence comparison, classification and phylogenetic relationship. Env. Carcino. Ecotox. Rev. C10, 181-203.
6. Burchell, B. (1991). Turning on and off the sense of smell. Nature 350, 16-17.
7. Chomczynski, P. and Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocynanate-phenol-chloroform extraction. Analyt. Biochem. 162, 156-159.
8. Clark, A. G. (1990). The glutathione S-transferases and resistance to insecticides. In Glutathione S-Transferases and Drug Resistance (ed. J. D. Hayes, C. B. Picket and T. J. Mantle), pp. 369-378. London: Taylor & Francis.
9. Dahl, A. R. (1988). The effect of cytochrome P-450-dependent metabolism and other enzyme activities on olfaction. In Molecular Neurobiology of the Olfactory System (ed. F. Margolis and T. Getchel), pp. 51-70. New York: Plenum.
10. Ding, X., Porter, T. D., Peng, H.-M. and Coon, M. J. (1991). cDNA and derived amino acid sequence of a rabbit nasal cytochrome p450NMB (p450IIGI), a unique isozyme possibly involved in olfaction. Arch. Biochem. Biophys. 285, 120-125.
11. Felsenstein, J. (1985). Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39, 783-791.
12. Fournier, D., Bride, J. M., Poirie, M., Berge, J-B. and Plapp, F. W. (1992). Insect glutathione S-transferases. J. Biol. Chem. 267, 1840-1845.
13. Franciosa, H. and Berge, J. B. (1995). Glutathione S-transferases in housfly (Musca domestica): Location of GST-1 and GST-2 families. Insect Biochem. Mol. Biol. 25, 311-317.
14. Gershenzon, J. and Croteau, R. (1991). Terpenoids. In Herbivores: Their Interactions with Secondary Plant Metabolites (ed. G. A. Rosenthal and M. R. Berenbaum), pp. 165-209. San Diego, CA: Academic Press.
15. Gleeson, R. A., McDowell, L. M., Aldrich, H. C., Trapido-Rosenthal, H. G. and Carr, W. E-S. (1991). Localization of 5'-ectonuclease/phosphatase activity within the olfactory sensilla of the spiny lobster, Panulirus argus. Cell Tissue Res. 265, 385-391.
16. Gleeson, R. A., Trapido-Rosenthal, H. G., McDowell. L. M., Aldrich, H. C. and Carr, W. E.-S. (1992). Ecto-ATPase/phosphatase activity in the olfactory sensilla of the spiny lobster, Panulirus argus: localization and characterization. Cell Tissue Res. 269, 439-445.
17. Grant, D. F. and Matsumara, F. (1989). Glutathione S-transferases 1 and 2 in susceptible and insect resistant Aedes aegypti. Pestic. Biochem. Physiol. 33, 132-143.
18. Györgyi, T. K., Roby-Shemkovitz, A. J. and Lerner, M. R. (1988). Characterization and cDNA cloning of the pheromone binding protein from the tobacco hawk worm, Manduca sexta: a tissue specific, developmentally regulated protein. Proc. Natl. Acad. Sci. USA 85, 9851-9855.
19. Habig, W. H., Pabst, M. J. and Jakoby, W. B. (1974). Glutathione S-transferases: The first enzymatic step in mercapteric formation. J. Biol. Chem. 249, 7130-7139.
20. Hayes, J. D. and Pulford, D. J. (1995). The glutathione S-transferase supergene family: Regulation of GST and the contribution of the isozymes to cancer chemoprotection and drug resistance. Crit. Rev. Biochem. Mol. Biol. 30, 445-600.
21. Kaissling, K.-E. (1998). Pheromone deactivation catalyzed by receptor molecules: a quantitative kinetic model. Chem. Senses 23, 385-395.
22. Karlin, S. and Altschul, S. F. (1990). Methods for assessing the statistical significance of molecular sequence features by using general scoring schemes. Proc. Natl. Acad. Sci. USA 87, 2264-2268.
23. Keil, T. A. (1989). Fine structure of the pheromone sensitive sensilla on the antenna of the hawk moth, Manduca sexta. Tisue & Cell 21, 139-151.
24. Krieger, J. and Breer, H. (1998). Cloning of a glutathione S-transferase from the antennae of Bombyx mori. Unpublished sequence. EMBL accession number AJ006502.
25. Kumar, S., Tamura, K. and Nei, M. (1993). MEGA: Molecular Evolutionary Genetics Analysis, Version 1.0. The Pennsylvania State University, University Park, PA.
26. Lazard, D., Tal, N., Rubenstein, M., Khen, M., Lancet, D. and Zupko, K. (1990). Identification and biochemical analysis of novel olfactory-specific cytochrome P-450IIA and UDP-glucuronosyl transferase. Biochemistry 29, 7433-7440.
27. Lazard, D., Zupko, K., Poria, Y., Nef, P., Lazarovtis, S. H., Khen, M. and Lancet, D. (1991). Odorant signal termination by olfactory UDP glucuronosyl transferase. Nature 349, 790-793.
28. Lee, X.-J. and Strausfeld, N. J. (1990). Structure, distribution and the number of surface sensilla and their receptor cells on the olfactory appendage of the male moth Manduca sexta. J. Neurocytol. 19, 519-538.
29. Longo, V., Mazzaccaro, A., Naldi, F. and Gervasi, P. G. (1991). Drug-metabolizing enzymes in liver, olfactory and respiratory epithelium of cattle. J. Biochem. Toxicol. 6, 123-128.
30. Louda, S. and Mole, S. (1991). Glucosinolates: Chemistry and ecology. In Herbivores: Their Interactions with Secondary Plant Metabolites (ed. G. A. Rosenthal and M. R. Berenbaum), pp. 124-157. San Diego, CA: Academic Press.
31. Maida, R., Steinbrecht, R. A., Ziegelberger, G. and Pelosi, P. (1993). The pheromone binding protein of Bombyx mori - purification, characterization and immunolocalization. Insect Biochem. Mol. Biol. 23, 243-252.
32. Maniatis, T., Fritsch, E. F. and Sambrook, J. (1982). Molecular Cloning: A Laboratory Manual. Cold Spring Laboratory, Cold Spring Harbor, NY.
33. Mannervik, B. and Danielson, U. H. (1988). Glutathione transferases - structure and catalytic activity. CRC Crit. Rev. Biochem. 23, 283-337.
34. Nef, P., Heldman, J., Lazard, D., Margalit, T., Jaye, M., Hanukoglu, I. and Lancet, D. (1989). Olfactory-specific cytochrome P-450. J. Biol. Chem. 264, 6780-6785.
35. Nei, M., Chakraborty, R. and Fuerst, P. A. (1976). Infinite allele model with varying mutation rate. Proc. Natl. Acad. Sci. USA 89, 8948-8952.
36. Oland, L. A., Tolbert, L. P. and Mossman, K. L. (1988). Radiation-induced reduction of the glial population during development disrupts the formation of olfactory glomeruli in an insect. J. Neurosci. 8, 353-367.
37. Pearson, W. R. and Lipman, D. J. (1988). Improved tools for biological sequence analysis. Proc. Natl. Acad. Sci. USA 85, 2444-2448.
38. Pelosi, P. and Maida, R. (1995). Odorant binding proteins in insects. Comp. Biochem. Physiol. B 111, 503-514.
39. Pembe, S. E and Taylor, J. B. (1992). An evolutionary perspective on glutathione transferases inferred from class-theta glutathione transferase cDNA sequences. Biochem. J. 287, 957-963.
40. Pickett, C. B. and Lu, A. Y. H. (1989). Glutathione S-transferases: Gene structure, regulation and biological function. Annu. Rev. Biochem. 58, 743-764.
41. Prapanthadara, L., Hemingway, J. and Ketterman, A. J. (1993) Partial purification and characterization of glutathione-S-transferases involved in DTT resistance from the mosquito Anopheles gambiae. Pest. Biochem. Physiol. 47, 119-133.
42. Prapanthadara, L., Hemingway, J. and Ketterman, A. J. (1995). DDT-resistance in Anopheles gambiae (Diptera: Culicidae) from Zanzibar, Tanzania, based on increased DDT-dehydrochlorinase activity of glutathione-S-transferases. Bull. Ent. Res. 85, 267-274.
43. Prestwich, G. D. and Du, G. (1995). Pheromone binding protein, pheromone recognition and signal transduction in moth olfaction. In Pheromone Research: New Directions (ed. R. T. Cardé and A. K. Minke), pp. 131-145. New York: Chapman & Hall.
44. Rogers, M. E., Sun, M., Lerner, M. and Vogt, R. G. (1997). SNMP-1, a novel membrane protein of olfactory neurons with homology to the CD36 family of membrane proteins. J. Biol. Chem. 272, 14792-14799.
45. Rybczynski, R., Reagan, J. and Lerner, M. R. (1989). A pheromone-degrading aldehyde oxidase in the antennae of the moth Manduca sexta. J. Neurosci. 9, 1341-1353.
46. Rybczynski, R., Vogt, R. G. and Lerner, M. R. (1990). Antennal-specific pheromone-degrading aldehyde oxidases from the moths Antheraea polyphemus and Bombyx mori. J. Biol. Chem. 265, 19712-19715.
47. Saitou, N. and Nei, M. (1987). The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425.
48. Sanes, J. R. and Hildebrand, J. G. (1976). Origin and morphogenesis of sensory neurons in an insect antenna. Dev. Biol. 51, 300-319.
49. Schweitzer, E. S., Sanes, J. R. and Hildebrand, J. G. (1976). Ontogeny of electroantennogram responses in the moth, Manduca sexta. J. Insect Physiol. 22, 955-960.
50. Snyder, M. J. and Maddison, D. R. (1997). Molecular phylogeny of glutathione-S-transferases. DNA Cell Biol. 16, 1373-1384.
51. Snyder, M. J., Walding, J. K. and Feyereisen, R. (1995). Glutathione S-transferases from larval Manduca sexta midgut: Sequence of two cDNAs and enzyme induction. Insect Biochem. Mol. Biol. 25, 455-465.
52. Starratt, A. M., Dahm, K. H., Allen, N., Hildebrand, J. G., Payne, T. L. and Roller, H. (1979). Bombykal, a sex pheromone of the sphinx moth, Manduca sexta. Z. Naturforsch. 34C, 9-12.
53. Steinbrecht, R. A. (1987). Functional morphology of pheromone-sensitive sensilla. In Pheromone Biochemistry (ed. G. D. Prestwich and G. J. Blomquist), pp. 353-384. Orlando, FL: Academic Press.
54. Steinbrecht, R. A. (1996). Are odorant-binding proteins involved in odorant discrimination? Chem. Senses 21, 718-725.
55. Steinbrecht, R. A., Ozaki, M. and Ziegelberger, G. (1992). Immunological localization of pheromone-binding protein in moth antennae. Cell Tissue Res. 270, 287-302.
56. Syvanen, M., Zhou, Z.-H. and Wang, J.-Y. (1994). Glutathione transferase gene family from the housefly Musca domestica. Mol. Gen. Genet. 245, 25-31.
57. Thompson, J. D., Higgins, G. and Gibson, T. J. (1994). CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighing, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680.
58. Toung, Y.-P., Hsieh, T.-S. and Tu, C.-P. H. (1993). The glutathione S-transferase D genes. J. Biol. Chem. 268, 9737-9746.
59. Tu, C.-P. D., Chang, M. and Reddy, C. C. (1984). The major rat heart glutathione S-transferases are anionic isozymes composed of Yb size subunits. Biochem. Biophys. Res. Commun. 123, 981-988.
60. Tumlinson, J. H., Mitchell, E. R., Doolittle, R. E. and Jackson, D. M. (1994). Field tests of synthetic Manduca sexia sex pheromone. J. Chem. Ecol. 20, 579-591.
61. Uzzel, T. and Corbin, K. W. (1971). Fitting discrete probability distribution evolutionary events. Science 172, 1089-1096.
62. Vogt, R. G. (1995). Molecular genetics of moth olfaction: a model for cellular identity and temporal assembly of the nervous system. In Molecular Model Systems in the Lepidoptera (ed. M. Goldsmith and A. S. Wilkins), pp. 341-367. Cambridge: Cambridge University Press.
63. Vogt, R. G., Kohne, A. C., Dubnau, J. T. and Prestwich, G. D. (1989). Expression of pheromone binding proteins during antennal development in the gypsy moth Lymantria dispar. J. Neurosci. 9, 3332-3346.
64. Vogt, R. G., Lindsay, S. M., Byrd, C. A. and Sun, M. (1997). Spatial patterns of olfactory neurons expressing specific odor receptor genes in 48-hour-old embryos of the zebrafish Danio rerio. J. Exp. Biol. 200, 433-443.
65. Vogt, R. G., Prestwich, G. D. and Lerner, M. R. (1991a). Odorant-binding-protein subfamilies associate with distinct classes of olfactory receptor neurons in insects. J. Neurobiol. 22, 74-84.
66. Vogt, R. G. and Riddiford, L. M. (1981). Pheromone binding and inactivation by moth antennae. Nature 293, 161-163.
67. Vogt, R. G., Riddiford, L. M. and Prestwich, G. D. (1985). Kinetic properties of a sex pheromone-degrading enzyme: The sensillar esterase of Antheraea polyphemus. Proc. Natl. Acad. Sci. USA 82, 8827-8831.
68. Vogt, R. G., Rybczynski, R. and Lerner, M. R. (1991b). Molecular cloning and sequencing of general odorant binding proteins GOBP1 and GOBP2 from the tobacco hawk moth Manduca sexta: Comparisons with other insect OBPs and their signal peptides. J. Neurosci. 11, 2972-2984.
69. Wang, J.-Y., McCommas, S. and Syvanen, M. (1991). Molecular cloning of a glutathione S-transferase overproduced in an insecticide resistant strain of housefly (Musca domestica). Molec. Gen. Genet. 227, 260-266.
70. Wilce, M. C. J., Board, P. G., Feil, S. C. and Parker, M. W. (1995). Crystal structure of a theta class glutathione transferase. EMBO J. 14, 2133-2143.
71. Yu, S. J. (1983). Induction of detoxifying enzymes by allelochemicals and host plants in the fall armyworm. Pest. Biochem. Physiol. 19, 330-336.
72. Yu, S. J. (1984). Interactions of allelochemicals with detoxication enzymes of insecticide susceptible and resistant fall armyworm. Pest. Biochem. Physiol. 22, 60-68.
73. Yu, S. J. (1989). Purification and characterization of glutathione transferases from five phytophagous Lepidoptera. Pest. Biochem. Physiol. 35, 97-105.
74. Zupko, K., Poria, Y. and Lancet, D. (1991). Immunolocalization of cytochrome P-450olf1 and P-450olf2 in rat olfactory mucosa. Eur. J. Biochem. 196, 51-58.