Kinetic properties of alternatively spliced isoforms of laccase-2 from Tribolium castaneum and Anopheles gambiae

Insect Biochemistry and Molecular Biology

Volumn 42, Issue 3, 2012, Pages 193-202

  Gorman, Maureen J ^a   Sullivan, Lucinda I ^a   Nguyen, Thi D T ^a   Dai, Huaien ^a   Arakane, Yasuyuki ^a,b   Dittmer, Neal T ^a   Syed, Lateef U ^a   Li, Jun ^a   Hua, Duy H ^a   Kanost, Michael R ^a  

^a KANSAS STATE UNIVERSITY   (United States)

^b Chonnam National University   (South Korea)

Author keywords

Cuticle; Insect; Laccase; Multicopper oxidase; Substrate

Indexed keywords

CATECHOLAMINE; INSECT PROTEIN; ISOENZYME; LACCASE; RECOMBINANT PROTEIN;

ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; ANIMAL; ANOPHELES GAMBIAE; ARTICLE; CHEMISTRY; COMPARATIVE STUDY; ENZYME SPECIFICITY; ENZYMOLOGY; FEMALE; ISOLATION AND PURIFICATION; KINETICS; MALE; METABOLISM; MOLECULAR GENETICS; OXIDATION REDUCTION REACTION; PH; TRIBOLIUM;

ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANIMALS; ANOPHELES GAMBIAE; CATECHOLAMINES; FEMALE; HYDROGEN-ION CONCENTRATION; INSECT PROTEINS; ISOENZYMES; KINETICS; LACCASE; MALE; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; RECOMBINANT PROTEINS; SUBSTRATE SPECIFICITY; TRIBOLIUM;

ANOPHELES GAMBIAE; HEXAPODA; TRIBOLIUM CASTANEUM;

EID: 84862777900     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2011.11.010     Document Type: Article

References (53)

1. Amenya D.A., Chou W., Li J., Yan G., Gershon P.D., James A.A., Marinotti O. Proteomics reveals novel components of the Anopheles gambiae eggshell. J.Insect Physiol. 2010, 56:1414-1419.
2. Andersen S.O. Characterization of a trypsin-solubilized phenoloxidase from locust cuticle. Insect Biochem. 1978, 8:143-148.
3. Andersen S.O. Insect cuticular sclerotization: a review. Insect Biochem. Mol. Biol. 2010, 40:166-178.
4. Arakane Y., Muthukrishnan S., Beeman R.W., Kanost M.R., Kramer K.J. Laccase 2 is the phenoloxidase gene required for beetle cuticle tanning. Proc. Natl. Acad. Sci. USA 2005, 102:11337-11342.
5. Arakane Y., Lomakin J., Beeman R.W., Muthukrishnan S., Gehrke S.H., Kanost M.R., Kramer K.J. Molecular and functional analyses of amino acid decarboxylases involved in cuticle tanning in Tribolium castaneum. J.Biol. Chem. 2009, 284:16584-16594.
6. Arnold K., Bordoli K., Kopp J., Schwede T. The SWISS-MODEL Workspace: a web-based environment for protein structure homology modelling. Bioinformatics 2006, 22:195-201.
7. Baez S., Segura-Aguilar J., Widersten M., Johansson A.-S., Mannervik B. Glutathione transferases catalyze the detoxication of oxidized metabolites (o-quinones) of catecholamines and may serve as an antioxidant system preventing degenerative cellular processes. Biochem. J. 1997, 324:25-28.
8. Baldrian P. Fungal laccases - occurrence and properties. FEMS Microbiol. Rev. 2006, 30:215-242.
9. Barrett F.M. Phenoloxidases from larval cuticle of the sheep blowfly, Lucilia cuprina: characterization, developmental changes, and inhibition by antiphenoloxidase antibodies. Arch. Insect Biochem. Physiol. 1987, 5:99-1118.
10. Barrett F.M. Characterization of phenoloxidases from larval cuticle of Sarcophaga bullata and a comparison with cuticular enzymes from other species. Can. J. Zool. 1987, 65:1158-1166.
11. Barrett F.M., Andersen S.O. Phenoloxidases in larval cuticle of the blowfly, Calliphora vicina. Insect Biochem. 1981, 11:17-23.
12. Bendtsen J.D., Nielsen H., von Heijne G., Brunak S. Improved prediction of signal peptides: signalP 3.0. J.Mol. Biol. 2004, 340:783-795.
13. Bertrand T., Jolivalt C., Briozzo P., Caminade E., Joly N., Madzak C., Mougin C. Crystal structure of a four-copper laccase complexed with an arylamine: insights into substrate recognition and correlation with kinetics. Biochemistry 2002, 41:7325-7333.
14. Chenna R., Sugawara H., Tadashi K., Lopez R., Gibson T.J., Higgins D.G., Thompson J.D. Multiple sequence alignment with the clustal series of programs. Nucleic Acids Res. 2003, 31:3497-3500.
15. Dittmer N.T., Kanost M.R. Insect multicopper oxidases: diversity, properties, and physiological roles. Insect Biochem. Mol. Biol. 2010, 40:179-188.
16. Dittmer N.T., Suderman R.J., Jiang H., Zhu Y.-C., Gorman M.J., Kramer K.J., Kanost M.R. Characterization of cDNAs encoding putative laccase-like multicopper oxidases and developmental expression in the tobacco hornworm, Manduca sexta, and the malaria mosquito, Anopheles gambiae. Insect Biochem. Mol. Biol. 2004, 34:29-41.
17. Dittmer N.T., Gorman M.J., Kanost M.R. Characterization of endogenous and recombinant forms of laccase-2, a multicopper oxidase from the tobacco hornworm, Manduca sexta. Insect Biochem. Mol. Biol. 2009, 39:596-606.
18. Eggert C., Temp U., Eriksson K.-E.L. The ligninolytic system of the white rot fungus Pycnoporus cinnabarinus: purification and characterization of the laccase. Appl. Environ. Microbiol. 1996, 62:1151-1158.
19. Elias-Neto M., Soares M.P.M., Simoes Z.L.P., Hartfelder K., Bitondi M.M.G. Developmental characterization, function and regulation of a Laccase2 encoding gene in the honey bee, Apis mellifera (Hymenoptera, Apinae). Insect Biochem. Mol. Biol. 2010, 40:241-251.
20. Ferraroni M., Myasoedova N.M., Schmatchenko V., Leontievsky A.A., Golovleva L.A., Scozzafava A., Briganti F. Crystal structure of a blue laccase from Lentinus tigrinus: evidences for intermediates in the molecular oxygen reductive splitting by multicopper oxidases. BMC Struct. Biol. 2007, 7:60.
21. Futahaski R., Banno Y., Fujiwara H. Caterpillar color patterns are determined by a two-phase melanin gene prepatterning process: new evidence from tan and laccase2. Evol. Dev. 2010, 12:157-167.
22. Futahashi R., Tanaka K., Matsuura Y., Tanahashi M., Kikuchi Y., Fukatsu T. Laccase2 is required for cuticular pigmentation in stinkbugs. Insect Biochem. Mol. Biol. 2011, 41:191-196.
23. Gorman M.J., An C., Kanost M.R. Characterization of tyrosine hydroxylase from Manduca sexta. Insect Biochem. Mol. Biol. 2007, 37:1327-1337.
24. Gorman M.F., Dittmer N.T., Marshall J.L., Kanost M.R. Characterization of the multicopper oxidase gene family in Anopheles gambiae. Insect Biochem. Mol. Biol. 2008, 38:817-824.
25. Gupta N., Lee N.S., Farinas E.T. Laboratory evolution of laccase for substrate specificity. J.Mol. Catal. B. Enzym. 2010, 62:230-234.
26. Hall M., Scott T., Sugumaran M., Soderhall K., Law J.H. Proenzyme of Manduca sexta phenol oxidase: purification, activation, substrate specificity of the active enzyme, and molecular cloning. Proc. Natl. Acad. Sci. USA 1995, 92:7764-7768.
27. He N., Botelho J.M.C., McNall R.J., Belozerov V., Dunn W.A., Mize T., Orlando R., Willis J.H. Proteomic analysis of cast cuticles from Anopheles gambiae by tandem mass spectrometry. Insect Biochem. Mol. Biol. 2007, 37:135-146.
28. Hopkins T.L., Kramer K.J. Insect cuticle sclerotization. Annu. Rev. Entomol. 1992, 37:273-302.
29. Kallio J.P., Auer S., Janis J., Andberg M., Kruus K., Rouvinen J., Koivula A., Hakulinen N. Structure-function studies of a Melanocarpus albomyces laccase suggest a pathway for oxidation of phenolic compounds. J.Mol. Biol. 2009, 392:895-909.
30. Kallio J.P., Gaparetti C., Andberg M., Boer H., Koivula A., Kruus K., Rouvinen J., Hakulinen N. Crystal structure of an ascomycete fungal laccase from Thielavia arenaria - common structural features of asco-laccases. FEBS J. 2011, 278:2283-2295.
31. Kiefer F., Arnold K., Kunzli M., Bordoli L., Schwede T. The SWISS-MODEL repository and associated resources. Nucleic Acids Res. 2009, 37:D387-D392.
32. Kramer K.J., Nuntnarumit C., Aso Y., Hawley M.D., Hopkins T.L. Electrochemical and enzymatic oxidation of catecholamines involved in sclerotization and melanization of insect cuticle. Insect Biochem. 1983, 13:475-479.
33. Kramer K.J., Morgan T.D., Hopkins T.L., Roseland C.R., Aso Y., Beeman R.W., Lookhart G.L. Catecholamines and β-alanine in the red flour beetle, Tribolium castaneum: roles in cuticle sclerotization and melanization. Insect Biochem. 1984, 14:293-298.
34. Kramer K.J., Kanost M.R., Hopkins T.L., Jiang H., Zhu Y.C., Xu R., Kerwin J.L., Turecek F. Oxidative conjugation of catechols with proteins in insect skeletal systems. Tetrahedron 2001, 57:385-392.
35. Matera I., Gullotto A., Tilli S., Ferraroni M., Scozzafava A., Briganti F. Crystal structure of the blue multicopper oxidase from the white-rot fungus Tramete trogii complexed with p-toluate. Inorg. Chim. Acta 2008, 361:4129-4137.
36. Mayer A.M., Staples R.C. Laccase: new functions for an old enzyme. Phytochemistry 2002, 60:551-565.
37. Murzin A.G., Brenner S.E., Hubbard T., Chothia C. SCOP: a structural classification of proteins database for the investigation of sequences and structures. J.Mol. Biol. 1995, 247:536-540.
38. Niu B.-L., Shen W.-F., Liu Y., Weng H.-B., He L.-H., Mu J.-J., Wu Z.-L., Jiang P., Tao Y.-Z., Meng Z.-Q. Cloning and RNAi-mediated functional characterization of MaLac2 of the pine sawyer, Monochamus alternatus. Insect Mol. Biol. 2008, 17:303-312.
39. Peitsch M.C. Protein modeling by e-mail. Bio/Technology 1995, 13:658-660.
40. Quintanar L., Stoj C., Taylor A.B., Hart P.J., Kosman D.J., Solomon E.I. Shall we dance? How a multicopper oxidase chooses its electron transfer partner. Acc. Chem. Res. 2007, 40:445-452.
41. Riedel F., Vorkel D., Eaton S. Megalin-dependent Yellow endocytosis restricts melanization in the Drosophila cuticle. Development 2011, 138:149-158.
42. Roseland C.R., Kramer K.J., Hopkins T.L. Cuticular strength and pigmentation of rust-red and black strains of Tribolium castaneum. Insect Biochem. 1987, 17:21-28.
43. Sakurai T., Kataoka K. Basic and applied features of multicopper oxidases, CueO, bilirubin oxidase, and laccase. Chem. Rec. 2007, 7:220-229.
44. Sugumaran M., Giglio L., Kundzicz H., Saul S., Semensi V. Studies on the enzymes involved in puparial cuticle sclerotization in Drosophila melanogaster. Arch. Insect Biochem. Physiol. 1992, 19:271-283.
45. Tadesse M.A., D'Annibale A., Galli C., Gentili P., Sergi F. An assessment of the relative contributions of redox and steric issues to laccase specificity towards putative substrates. Org. Biomol. Chem. 2008, 6:868-878.
46. Thomas B.R., Yonekura M., Morgan T.D., Czapla T.H., Hopkins T.L., Kramer K.J. Atrypsin-solubilized laccase from pharate pupal integument of the tobacco hornworm, Manduca sexta. Insect Biochem. 1989, 19:611-622.
47. Xu F. Oxidation of phenols, anilines, and benzenethiols by fungal laccases: correlation between activity and redox potentials as well as halide inhibition. Biochemistry 1996, 35:7608-7614.
48. Xu F., Shin W., Brown S.H., Wahleithner J.A., Sundaram U.M., Solomon E.I. Astudy of a series of recombinant fungal laccases and bilirubin oxidase that exhibit significant differences in redox potential, substrate specificity, and stability. Biochim. Biophys. Acta 1996, 1292:303-311.
49. Yamazaki H.I. The cuticular phenoloxidase in Drosophila virilis. J.Insect Physiol. 1969, 15:2203-2211.
50. Yamazaki H.I. Cuticular phenoloxidase from the silkworm, Bombyx mori: properties, solubilization, and purification. Insect Biochem. 1972, 2:431-444.
51. Yamazaki H.I. Laccase-type phenoloxidase in the cuticle of the silkworm, Bombyx mori. Res. J. 1989, 5:1-10. (Proceedings of the Department of General Education of Atomi Gakuen Women's University).
52. Yatsu J., Asano T. Cuticle laccase of the silkworm, Bombyx mori: purification, gene identification and presence of its inactive precursor in the cuticle. Insect Biochem. Mol. Biol. 2009, 39:254-262.
53. Zhukhlistova N.E., Zhukova Y.N., Lyashenko A.V., Zaitsev V.N., Mikhailov A.M. Three-dimensional organization of three-domain copper oxidases: a review. Crystallogr. Rep. 2008, 53:92-109.