Egf1.5 is a second phenoloxidase cascade inhibitor encoded by Microplitis demolitor bracovirus

Insect Biochemistry and Molecular Biology

Volumn 40, Issue 7, 2010, Pages 497-505

  Lu, Zhiqiang ^a   Beck, Markus H ^a   Strand, Michael R ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

Immunity; Insect; Melanization; Virulence; Virus

Indexed keywords

INSECT PROTEIN; MONOPHENOL MONOOXYGENASE; PEPTIDE HYDROLASE; PROTEINASE INHIBITOR; VIRUS PROTEIN;

ANIMAL; ARTICLE; CHEMISTRY; ENZYME ACTIVATION; ENZYMOLOGY; GENETICS; HEMOLYMPH; LEPIDOPTERA; METABOLISM; MULTIGENE FAMILY; PHYSIOLOGY; POLYDNAVIRIDAE; PROTEIN MOTIF; VIROLOGY; MANDUCA;

AMINO ACID MOTIFS; ANIMALS; ENZYME ACTIVATION; HEMOLYMPH; INSECT PROTEINS; MANDUCA; MONOPHENOL MONOOXYGENASE; MULTIGENE FAMILY; PEPTIDE HYDROLASES; POLYDNAVIRIDAE; PROTEASE INHIBITORS; VIRAL PROTEINS;

BOMBYX MORI; HELICOVERPA ZEA; HEXAPODA; LEPIDOPTERA; MANDUCA SEXTA; MICROPLITIS DEMOLITOR BRACOVIRUS; PSEUDOPLUSIA INCLUDENS;

EID: 77953916901     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2010.04.009     Document Type: Article

References (54)

1. An C.J., Ishibashi J., Ragan E.J., Jiang H.B., Kanost M.R. Functions of Manduca sexta hemolymph proteinases HP6 and HP8 in two innate immune pathways. J. Biol. Chem. 2009, 284:19716-19726.
2. Beck M.H., Strand M.R. A novel protein from a polydnavirus inhibits the insect prophenoloxidase activation pathway. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:19267-19272.
3. Bezier A., Herbiniere J., Lanzrein B., Drezen J.-M. Polydnavirus hidden face: the genes producing virus particles of parasitic wasps. J. Invertebr. Pathol. 2009, 101:194-203.
4. Blankenship J.R., Mitchell A.P. The fungal frontier. Genome Biol. 2007, 8:305.
5. Buchon N., Poidevin M., Kwon M., Guillou A., Sottas V., Lee B.L., Lemaitre B. A single modular serine protease integrates signals from pattern-recognition receptors upstream of the Drosophila toll pathway. Proc. Natl. Acad. Sci. U. S. A. 2009, 95:12220-12225.
6. Cerenius L., Lee B.L., Soderhall K. The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immunol. 2008, 29:263-271.
7. Clark A.G. Invasion and maintenance of gene duplication. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:2950-2954.
8. Dupuy C., Huguet E., Drezen J.M. Unfolding the evolutionary history of polydnaviruses. Virus Res. 2006, 117:81-89.
9. Espagne E., Dupuy C., Huguet E., Cattolico L., Provost B., Martins N., Poirie M., Periquet G., Drezen J.-M. Genome sequence of a polydnavirus: insights into symbiotic virus evolution. Science 2004, 306:286-289.
10. Francino M.P. An adaptive radiation model for the origin of new gene functions. Nat. Genet. 2005, 573-577.
11. Friedman R., Hughes A.L. Pattern of gene duplication in the Cotesia congregata bracovirus. Infect. Genet. Evol. 2006, 6:315-322.
12. Gorman M.J., Wang Y., Jiang H., Kanost M.R. Manduca sexta hemolymph proteinase 21 activates prophenoloxidase activating proteinase 3 in an insect innate immune response proteinase cascade. J. Biol. Chem. 2007, 282:11742-11749.
13. Greer J.M., Puetz J., Thomas K.R., Capecchi M.R. Maintenance of functional equivalence during paralogous Hox gene evolution. Nature 2000, 403:661-665.
14. Gupta S., Wang Y., Jiang H. Purification and characterization of Manduca sexta prophenoloxidase-activating proteinase-1, an enzyme involved in insect immune responses. Protein Expr. Purif. 2005, 39:261-268.
15. Hileman L.C., Baum D.A. Why do paralogs exists? Molecular evolution of Cycloidea and related floral symmetry genes in Antirrhinaeae (Veronicaceae). Mol. Biol. Evol. 2003, 20:591-600.
16. Hughes A.L. The evolution of functionally novel proteins after gene duplication. Proc. R. Soc. Lond. B 1994, 256:119-124.
17. Jiang H., Wang Y., Ma C., Kanost M.R. Subunit composition of pro-phenol oxidase from Manduca sexta: molecular cloning of subunit ProPO-P1. Insect Biochem. Mol. Biol. 1997, 27:835-850.
18. Jiang H., Wang Y., Kanost M.R. Pro-phenol oxidase activating proteinase from an insect, Manduca sexta: a bacteria-inducible protein similar to Drosophila easter. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:12220-12225.
19. Jiang H., Wang Y., Yu X.-Q., Zhu Y., Kanost M.R. Prophenoloxidase-activating proteinase-3 (PAP-3) from Manduca sexta hemolymph: a clip-domain serine proteinase regulated by serpin-1J and serine proteinase homologs. Insect Biochem. Mol. Biol. 2003, 33:1049-1060.
20. Jiang H., Wang Y., Yu X.-Q., Kanost M.R. Prophenoloxidase-activating proteinase-2 (PAP-2) from hemolymph of Manduca sexta: a bacteria-inducible serine proteinase containing two clip domains. J. Biol. Chem. 2003, 278:3552-3561.
21. Kan H., Kim C.H., Kwo H.M., Park J.W., Roh K.B., Lee H., Park B.J., Zhang R., Zhang J., Soderhall K., Ha N.C., Lee B.L. Molecular control of phenoloxidase-induced melanin synthesis in an insect. J. Biol. Chem. 2009, 283:25316-25323.
22. Kanost, M.R., Gorman, M., 2008. Phenoloxidases in insect immunity. In: Beckage, N.E. (Ed.), Insect Immunity. Academic Press, San Diego, pp. 69-96.
23. Krakauer D.C., Nowak M.A. Evolutionary preservation of redundant duplicated genes. Semin. Cell Dev. Biol. 1999, 10:555-559.
24. Leclerc V., Perte N., Chamy L., Martinelli C., Ligoxygakis P., Hoffmann J.A., Reichart J.M. Prophenoloxidase activation is not required for survival to microbial infections in Drosophila. EMBO Rep. 2006, 7:231-235.
25. Lee S.Y., Cho M.Y., Hyun J.H., Lee K.M., Homma K.I., Natori S., Kawabata S.I., Iwanaga S., Lee B.L. Molecular cloning of cDNA for prophenoloxidase activating factor I, a serine protease is induced by lipopolysaccharide or 1, 3-beta glucan in coleopteran insect, Holotrichia diomphalia larvae. Eur. J. Biochem. 1998, 257:615-621.
26. Lu Z., Jiang H. Expression of Manduca sexta serine proteinase homolog precursors in insect cells and their proteolytic processing. Insect Biochem. Mol. Biol. 2008, 38:89-98.
27. Lu Z., Beck M.H., Jiang H., Wang Y., Strand M.R. The viral protein Egf1.0 is a dual activity inhibitor of prophenoloxidase activating proteinases 1 and 3 from Manduca sexta. J. Biol. Chem. 2008, 283:21325-21333.
28. Luo D., Carpenter R., Copsey L., Vincent C., Clark J., Coen E. Control of organ asymmetry in flowers of Antirrhinum. Cell 1999, 99:367-376.
29. Lynch M., O'Hely M., Walsh B., Force A. The probability of preservation of a newly arisen gene duplicate. Genetics 2001, 159:1789-1804.
30. Ohno S. Evolution by Gene Duplication 1970, Springer-Verlag, Heidelberg, Germany.
31. Paskewitz S.M., Andreev O., Shi L. Gene silencing of serine proteases affects melanization of Sephadex beads in Anopheles gambiae. Insect Biochem. Mol. Biol. 2006, 36:701-711.
32. Satoh D., Horii A., Ochiai M., Ashida M. Prophenoloxidase - activating enzyme of the silkworm, Bombyx mori - purification, characterization, and cDNA cloning. J. Biol. Chem. 1999, 274:7441-7453.
33. Schmidt O., Theopold U., Strand M. Innate immunity and evasion by insect parasitoids. BioEssays 2001, 23:344-351.
34. Serbielle C., Chowdhury S., Pichon S., Dupas S., Lesobre J., Purisma E.A., Drezen J.-M., Huguet E. Viral cystatin evolution and three-dimensional structure modelling: a case for directional selection acting on a viral protein involved in a host-parasitoid interaction. BMC Biol. 2008, 6:38.
35. Strand M.R. The interactions between polydnavirus-carrying parasitoids and their lepidopteran hosts. Molecular Biology and Genetics of the Lepidoptera 2009, 321-336. CRC Press, Boca Raton, USA. M.R. Goldsmith, F. Marec (Eds.).
36. Strand, M.R. Polydnaviruses. In: Asgari, S., Johnson, K. (Eds.), Insect Virology. Caister Academic Press, Norwich, UK, in press.
37. Strand M.R., Dover B.A. Developmental disruption of Pseudoplusia includens and Heliothis virescens larvae by the polydnavirus and venom of Microplitis demolitor. Arch. Insect Biochem. Physiol. 1991, 18:131-145.
38. Strand M.R., Noda T. Alterations in the haemocytes of Pseudoplusia includens after parasitism by Microplitis demolitor. J. Insect Physiol. 1991, 37:839-850.
39. Strand M.R., Johnson J.A., Culin J.D. Developmental interactions between the parasitoid Microplitis demolitor (Hymenoptera: Braconidae) and its host Heliothis virescens (Lepidoptera: Noctuidae). Ann. Entomol. Soc. Am. 1988, 81:822-830.
40. Strand M.R., Witherell S.A., Trudeau D. Two related Microplitis demolitor polydnavirus mRNAs expressed in hemocytes of Pseudoplusia includens contain a common cysteine-rich domain. J. Virol. 1997, 71:2146-2156.
41. Tang H., Kambris Z., Lemaitre B., Hashimoto C. Two proteases defining a melanization cascade in the immune system of Drosophila. J. Biol. Chem. 2006, 281:28097-28104.
42. Thoetkiattikul L., Beck M.H., Strand M.R. IkB-like proteins from a polydnavirus function as suppressors of the insect immune response. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:11426-11431.
43. Trudeau D., Witherell A.R., Strand M.R. Characterization of two novel Microplitis demolitor polydnavirus mRNAs expressed in Pseudoplusia includens haemocytes. J. Gen. Virol. 2000, 81:3049-3058.
44. Volz J., Muller H.M., Zdanowicz A., Kafatos F.C., Osta M.A. A genetic module regulates the melanization response of Anopheles to Plasmodium. Cell. Microbiol. 2006, 8:1392-1405.
45. Wagner A. Selection and gene duplication: a view from the genome. Genome Biol. 2002, 3:1012.1-1012.3.
46. Walsh J.B. How often do duplicated genes evolve new functions. Genetics 1995, 139:421-428.
47. Wang Y., Jiang H. Prophenoloxidase (PPO) activation in Manduca sexta: an initial analysis of molecular interactions among PPO, PPO-activating proteinase-3 (PAP-3), and a cofactor. Insect Biochem. Mol. Biol. 2004, 34:731-742.
48. Wang Y., Jiang H. Interaction of β-1,3-glucan with its recognition protein activates hemolymph proteinase 14, an initiation enzyme of the prophenoloxidase activation system in Manduca sexta. J. Biol. Chem. 2006, 281:9271-9278.
49. Wang Y., Jiang H. Reconstitution of a branch of the Manduca sexta prophenoloxidase activation cascade in vitro: snake-like hemolymph proteinase 21 (HP21) cleaved by HP14 activates prophenoloxidase-activating proteinase-2 precursor. Insect Biochem. Mol. Biol. 2007, 37:1015-1025.
50. Watterson G.A. On the time for gene silencing at duplicate loci. Genetics 1983, 105:745-766.
51. Webb B.A., Strand M.R. The biology and genomics of polydnaviruses. Comprehensive Molecular Insect Science 2005, vol. 6:323-360. Elsevier, San Diego. L.I. Gilbert, K. Iatrou, S.S. Gill (Eds.).
52. Webb B.A., Strand M.R., Deborde S.E., Beck M., Hilgarth R.S., Kadash K., Kroemer J.A., Lindstrom K.G., Rattanadechakul W., Shelby K.S., Thoetkiattikul L., Turnbull M.W., Barney W.E., Witherell R.A. Polydnavirus genomes reflect their dual roles as mutualists and pathogens. Virology 2006, 347:160-174.
53. Yu X.-Q., Jiang H., Wang Y., Kanost M.R. Nonproteolytic serine proteinase homologs involved in the tobacco hornworm, Manduca sexta. Insect Biochem. Mol. Biol. 2003, 33:197-208.
54. Zhu Y., Wang Y., Gorman M.J., Jiang H., Kanost M.R. Manduca sexta serpin-3 regulates prophenoloxidase activation in response to infection by inhibiting prophenoloxidase-activating proteinases. J. Biol. Chem. 2003, 278:46556-46564.