Formation of disulfide bonds in insect prophenoloxidase enhances immunity through improving enzyme activity and stability

Developmental and Comparative Immunology

Volumn 44, Issue 2, 2014, Pages 351-358

  Lu, Anrui ^a   Peng, Qin ^a   Ling, Erjun ^a  

^a INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

Author keywords

Disulfide bonds; Immunity; Insect; Prophenoloxidase

Indexed keywords

ENZYME PRECURSOR; MONOPHENOL MONOOXYGENASE; PROPHENOL OXIDASE; UNCLASSIFIED DRUG; CATECHOL OXIDASE; COPPER; INSECT PROTEIN; PRO-PHENOLOXIDASE; RECOMBINANT PROTEIN;

ANIMAL CELL; ANTIBACTERIAL ACTIVITY; ARTICLE; BACILLUS SUBTILIS; CONTROLLED STUDY; DISULFIDE BOND; DROSOPHILA MELANOGASTER; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME STABILITY; ENZYME STRUCTURE; ESCHERICHIA COLI; IMMUNITY; IMMUNOSTIMULATION; INNATE IMMUNITY; INSECT IMMUNITY; MUTANT DROSOPHILA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STRUCTURE ANALYSIS; THERMOSTABILITY; ANIMAL; CELL CULTURE; CHEMICAL STRUCTURE; CHEMISTRY; COMPARATIVE STUDY; ESCHERICHIA COLI INFECTION; GENETICS; GRAM POSITIVE INFECTION; IMMUNOLOGY; METABOLISM; MUTATION; WASP;

ANIMALS; BACILLUS SUBTILIS; CATECHOL OXIDASE; CELLS, CULTURED; COPPER; DROSOPHILA MELANOGASTER; ENZYME ACTIVATION; ENZYME PRECURSORS; ENZYME STABILITY; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; GRAM-POSITIVE BACTERIAL INFECTIONS; IMMUNITY; INSECT PROTEINS; MOLECULAR STRUCTURE; MUTATION; RECOMBINANT PROTEINS; WASPS;

EID: 84896736186     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2014.01.011     Document Type: Article

References (42)

1. Aguilera F., McDougall C., Degnan B.M. Origin, evolution and classification of type-3 copper proteins: lineage-specific gene expansions and losses across the Metazoa. BMC Evol. Biol. 2013, 13:96.
2. Amparyup P., Charoensapsri W., Tassanakajon A. Two prophenoloxidases are important for the survival of Vibrio harveyi challenged shrimp Penaeus monodon. Dev. Comp. Immunol. 2009, 33:247-256.
3. Asano T., Takebuchi K. Identification of the gene encoding pro-phenoloxidase A(3) in the fruitfly Drosophila melanogaster. Insect Mol. Biol. 2009, 18:223-232.
4. Ashida M. Purification and characterization of pre-phenoloxidase from hemolymph of the silkworm Bombyx mori. Arch. Biochem. Biophys. 1971, 144:749-762.
5. Ashida M., Brey P. Recent advances on the research of the insect prophenoloxidase cascade. Molecular Mechanisms of Immune Responses in Insects 1998, 135-172. Chapman & Hall, London. P. Brey, D. Hultmark (Eds.).
6. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
7. Burmester T. Origin and evolution of arthropod hemocyanins and related proteins. J. Comp. Physiol. B 2002, 172:95-107.
8. Cerenius L., Lee B.L., Söderhäll K. The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immunol. 2008, 29:263-271.
9. Chase M.R., Raina K., Bruno J., Sugumaran M. Purification, characterization and molecular cloning of prophenoloxidases from Sarcophaga bullata. Insect Biochem. Mol. Biol. 2000, 30:953-967.
10. Claus H., Decker H. Bacterial tyrosinases. Syst. Appl. Microbiol. 2006, 29:3-14.
11. Decker H., Schweikardt T., Tuczek F. The first crystal structure of tyrosinase: all questions answered?. Angew. Chem. Int. Ed. Engl. 2006, 45:4546-4550.
12. Decker H., Tuczek F. Tyrosinase/catecholoxidase activity of hemocyanins: structural basis and molecular mechanism. Trends Biochem. Sci. 2000, 25:392-397.
13. Fujimoto K., Masuda K., Asada N., Ohnishi E. Purification and characterization of prophenoloxidases from pupae of Drosophila melanogaster. J. Biochem. 1993, 113:285-291.
14. González-Santoyo I., Córdoba-Aguilar A. Phenoloxidase: a key component of the insect immune system. Entomol. Exp. Appl. 2012, 142:1-16.
15. Hillyer J.F., Schmidt S.L., Christensen B.M. Hemocyte-mediated phagocytosis and melanization in the mosquito Armigeres subalbatus following immune challenge by bacteria. Cell Tissue Res. 2003, 313:117-127.
16. Kadokura H., Katzen F., Beckwith J. Protein disulfide bond formation in prokaryotes. Annu. Rev. Biochem. 2003, 72:111-135.
17. Kanost M.R., Jiang H., Yu X.Q. Innate immune responses of a lepidopteran insect, Manduca sexta. Immunol. Rev. 2004, 198:97-105.
18. Klabunde T., Eicken C., Sacchettini J.C., Krebs B. Crystal structure of a plant catechol oxidase containing a dicopper center. Nat. Struct. Mol. Biol. 1998, 5:1084-1090.
19. Lazcano A., Díaz-Villagómez E., Mills T., Oró J. On the levels of enzymatic substrate specificity: implications for the early evolution of metabolic pathways. Adv. Space Res. 1995, 15:345-356.
20. Lemaitre B., Hoffmann J. The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 2007, 25:697-743.
21. Lemaitre B., Miguel-Aliaga I. The digestive tract of Drosophila melanogaster. Annu. Rev. Genet. 2013, 47:377-404.
22. Li X., Ma M., Liu F., Chen Y., Lu A., Ling Q.-Z., Li J., Beerntsen B.T., Yu X.-Q., Liu C., Ling E. Properties of Drosophila melanogaster prophenoloxidases expressed in Escherichia coli. Dev. Comp. Immunol. 2012, 36:648-656.
23. Li Y., Wang Y., Jiang H., Deng J. Crystal structure of Manduca sexta prophenoloxidase provides insights into the mechanism of type 3 copper enzymes. Proc. Natl. Acad. Sci. USA 2009, 106:17002-17006.
24. 2+ and have different activity in vitro. Dev. Comp. Immunol. 2012, 36:619-628.
25. Liu H., Jiravanichpaisal P., Cerenius L., Lee B.L., Soderhall I., Soderhall K. Phenoloxidase is an important component of the defense against Aeromonas hydrophila infection in a crustacean, Pacifastacus leniusculus. J. Biol. Chem. 2007, 282:33593-33598.
26. Magnus K.A., Hazes B., Ton-That H., Bonaventura C., Bonaventura J., Hol W.G. Crystallographic analysis of oxygenated and deoxygenated states of arthropod hemocyanin shows unusual differences. Proteins 1994, 19:302-309.
27. Marusek C.M., Trobaugh N.M., Flurkey W.H., Inlow J.K. Comparative analysis of polyphenol oxidase from plant and fungal species. J. Inorg. Biochem. 2006, 100:108-123.
28. Nam H.J., Jang I.H., You H., Lee K.A., Lee W.J. Genetic evidence of a redox-dependent systemic wound response via Hayan protease-phenoloxidase system in Drosophila. EMBO J. 2012, 31:1253-1265.
29. Paria A., Greeshma S.S., Chaudhari A., Makesh M., Purushothaman C.S., Rajendran K.V. Nonspecific effect of double-stranded (ds) RNA on prophenoloxidase (proPO) expression in Penaeus monodon. Appl. Biochem. Biotechnol. 2013, 169:281-289.
30. Parkinson N., Smith I., Weaver R., Edwards J.P. A new form of arthropod phenoloxidase is abundant in venom of the parasitoid wasp Pimpla hypochondriaca. Insect Biochem. Mol. Biol. 2001, 31:57-63.
31. Plaisance K.L., Gronwald J.W. Enhanced catalytic constant for glutathioneS-transferase (Atrazine) activity in an Atrazine-resistant Abutilon theophrasti biotype. Pestic. Biochem. Physiol. 1999, 63:34-49.
32. Ramet M., Lanot R., Zachary D., Manfruelli P. JNK signaling pathway is required for efficient wound healing in Drosophila. Dev. Biol. 2002, 241:145-156.
33. Rock F.L., Li X., Chong P., Ida N., Klein M. Roles of disulfide bonds in recombinant human interleukin 6 conformation. Biochemistry 1994, 33:5146-5154.
34. Sendovski M., Kanteev M., Ben-Yosef V.S., Adir N., Fishman A. First structures of an active bacterial tyrosinase reveal copper plasticity. J. Mol. Biol. 2011, 405:227-237.
35. Sevier C.S., Kaiser C.A. Formation and transfer of disulphide bonds in living cells. Nat. Rev. Mol. Cell Biol. 2002, 3:836-847.
36. Seybold W.D., Meltzer P.S., Mitchell H.K. Phenol oxidase activation in Drosophila: a cascase of reactions. Biochem. Genet. 1975, 13:85-108.
37. Starr C., Taggart R. Biology: The Unity and Diversity of Life 2009, Wadsworth Publishing Company, Belmont, California, USA. 12th ed.
38. Strand M.R. The insect cellular immune response. Insect Sci. 2008, 15:1-14.
39. Wang N., Hebert D.N. Tyrosinase maturation through the mammalian secretory pathway: bringing color to life. Pigment Cell Res. 2006, 19:3-18.
40. Wang Z., Lu A., Li X., Shao Q., Beerntsen B.T., Liu C., Ma Y., Huang Y., Zhu H., Ling E. A systematic study on hemocyte identification and plasma prophenoloxidase from Culex pipiens quinquefasciatus at different developmental stages. Exp. Parasitol. 2011, 127:135-141.
41. Yang B., Lu A., Peng Q., Ling Q.-Z., Ling E. Activity of fusion prophenoloxidase-GFP and its potential applications for innate immunity study. PLoS ONE 2013, 8:e64106.
42. Zhao P., Li J., Wang Y., Jiang H. Broad-spectrum antimicrobial activity of the reactive compounds generated in vitro by Manduca sexta phenoloxidase. Insect Biochem. Mol. Biol. 2007, 37:952-959.