Role of enhancin in mamestra configurata nucleopolyhedrovirus virulence: Selective degradation of host peritrophic matrix proteins

Journal of General Virology

Volumn 93, Issue 4, 2012, Pages 744-753

  Toprak, Umut ^a,b,c   Harris, Stephanie ^a   Baldwin, Douglas ^a   Theilmann, David ^a   Gillott, Cedric ^b   Hegedus, Dwayne D ^a,b   Erlandson, Martin A ^a,b  

^a AGRICULTURE AND AGRI FOOD CANADA   (Canada)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

^c ANKARA UNIVERSITY   (Turkey)

Author keywords

[No Author keywords available]

Indexed keywords

EDETIC ACID; METALLOPROTEINASE; PROTEIN ENHANCIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; AUTOGRAPHA CALIFORNICA; BACULOVIRUS; INOCULATION; MAMESTRA CONFIGURATA; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYHEDROSIS VIRUS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; VIRION; VIRUS VIRULENCE; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; DIGESTIVE SYSTEM; GASTRIC MUCINS; LARVA; LEPIDOPTERA; METALLOPROTEASES; NUCLEOPOLYHEDROVIRUS; PHYLOGENY; VIRAL PROTEINS; VIRULENCE;

AUTOGRAPHA CALIFORNICA MNPV; AUTOGRAPHA CALIFORNICA NUCLEOPOLYHEDROVIRUS; HEXAPODA; MAMESTRA CONFIGURATA NUCLEOPOLYHEDROVIRUS;

EID: 84858189186     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.038117-0     Document Type: Article

References (44)

1. Bell, R. A., Owens, C. D., Shapiro, M. & Tardif, J. R. (1981). Development of mass-rearing technology. In The Gypsy Moth: Research Toward Integrated Pest Management, pp. 599-633. Edited by C. C. Doane & M. L. McManus. Washington, DC: US Department of Agriculture.
2. Bischoff, D. S. & Slavicek, J. M. (1997). Molecular analysis of an enhancin gene in the Lymantria dispar nuclear polyhedrosis virus. J Virol 71, 8133-8140.
3. Bucher, G. E. & Bracken, G. K. (1976). The bertha armyworm, Mamestra configurata (Lepidoptera: Noctuidae). Artificial diet and rearing technique. Can Entomol 108, 1327-1338.
4. Derksen, A. C. G. & Granados, R. R. (1988). Alteration of a lepidopteran peritrophic membrane by baculoviruses and enhancement of viral infectivity. Virology 167, 242-250.
5. Devenport, M., Alvarenga, P. H., Shao, L., Fujioka, H., Bianconi, M. L., Oliveira, P. L. & Jacobs-Lorena, M. (2006). Identification of the Aedes aegypti peritrophic matrix protein AeIMUCI as a heme-binding protein. Biochemistry 45, 9540-9549.
6. Dougherty, E. M., Narang, N., Loeb, M., Lynn, D. E. & Shapiro, M. (2006). Fluorescent brightener inhibits apoptosis in baculovirusinfected gypsy moth larval midgut cells in vitro. Biocontrol Sci Technol 16, 157-168.
7. Erlandson, M. (1990). Biological and biochemical comparison of Mamestra configurata and Mamestra brassica nuclear polyhedrosis virus isolates pathogenic for the bertha armyworm, Mamestra configurata (Lepidoptera: Noctuidae). J Invertebr Pathol 56, 47-56.
8. Erlandson, M., Newhouse, S., Moore, K., Janmaat, A., Myers, J. & Theilmann, D. (2007). Characterization of baculovirus isolates from Trichoplusia ni populations from vegetable greenhouses. Biol Control 41, 256-263.
9. Fang, S., Wang, L., Guo, W., Zhang, X., Peng, D., Luo, C., Yu, Z. & Sun, M. (2009). Bacillus thuringiensis bel protein enhances the toxicity of Cry1Ac protein to Helicoverpa armigera larvae by degrading insect intestinal mucin. Appl Environ Microbiol 75, 5237-5243.
10. Gallo, L. G., Corsaro, B. G., Hughes, P. R. & Granados, R. R. (1991). In vivo enhancement of baculovirus infection by the viral enhancing factor of a granulosis virus of the cabbage looper, Trichoplusia ni (Lepidoptera: Noctuidae). J Invertebr Pathol 58, 203-210.
11. Galloway, C. S., Wang, P., Winstanley, D. & Jones, I. M. (2005). Comparison of the bacterial enhancin-like proteins from Yersinia and Bacillus spp. with a baculovirus enhancin. J Invertebr Pathol 90, 134-137.
12. Gijzen, M., Roelvink, P. & Granados, R. (1995). Characterization of viral enhancing activity from Trichoplusia ni granulosis virus. J Invertebr Pathol 65, 289-294.
13. Hashimoto, Y., Corsaro, B. G. & Granados, R. R. (1991). Location and nucleotide sequence of the gene encoding the viral enhancing factor of the Trichoplusia ni granulosis virus. J Gen Virol 72, 2645-2651.
14. Hegedus, D., Erlandson, M., Gillott, C. & Toprak, U. (2009). New insights into peritrophic matrix synthesis, architecture, and function. Annu Rev Entomol 54, 285-302.
15. Hoover, K., Humphries, M. A., Gendron, A. R. & Slavicek, J. M. (2010). Impact of viral enhancin genes on potency of Lymantria dispar multiple nucleopolyhedrovirus in L. dispar following disruption of the peritrophic matrix. J Invertebr Pathol 104, 150-152.
16. Jakubowska, A. K., Peters, S. A., Ziemnicka, J., Vlak, J. M. & van Oers, M. M. (2006). Genome sequence of an enhancin gene-rich nucleopolyhedrovirus (NPV) from Agrotis segetum: collinearity with Spodoptera exigua multiple NPV. J Gen Virol 87, 537-551.
17. Jehle, J. A., Blissard, G. W., Bonning, B. C., Cory, J. S., Herniou, E. A., Rohrmann, G. F., Theilmann, D. A., Thiem, S. M. & Vlak, J. M. (2006). On the classification and nomenclature of baculoviruses: a proposal for revision. Arch Virol 151, 1257-1266.
18. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
19. Lepore, L. S., Roelvink, P. R. & Granados, R. R. (1996). Enhancin, the granulosis virus protein that facilitates nucleopolyhedrovirus (NPV) infections, is a metalloprotease. J Invertebr Pathol 68, 131-140.
20. Li, L., Donly, C., Li, Q., Willis, L. G., Keddie, B. A., Erlandson, M. A. & Theilmann, D. A. (2002a). Identification and genomic analysis of a second species of nucleopolyhedrovirus isolated from Mamestra configurata. Virology 297, 226-244.
21. Li, Q., Donly, C., Li, L., Willis, L. G., Theilmann, D. A. & Erlandson, M. (2002b). Sequence and organization of the Mamestra configurata nucleopolyhedrovirus genome. Virology 294, 106-121.
22. Li, Q., Li, L., Moore, K., Donly, C., Theilmann, D. A. & Erlandson, M. (2003). Characterization of Mamestra configurata nucleopolyhedrovirus enhancin and its functional analysis via expression in an Autographa californica M nucleopolyhedrovirus recombinant. J Gen Virol 84, 123-132.
23. Li, L., Li, Q., Willis, L. G., Erlandson, M., Theilmann, D. A. & Donly, C. (2005). Complete comparative genomic analysis of two field isolates of Mamestra configurata nucleopolyhedrovirus-A. J Gen Virol 86, 91-105.
24. Maskel, S. M. & DiCapua, R. A. (1988). Comparison of protease activity of four nuclear polyhedrosis viruses. J Invertebr Pathol 52, 447-452.
25. Peng, J., Zhong, J. & Granados, R. R. (1999). A baculovirus enhancin alters the permeability of a mucosal midgut peritrophic matrix from lepidopteran larvae. J Insect Physiol 45, 159-166.
26. Popham, H. J., Bischoff, D. S. & Slavicek, J. M. (2001). Both Lymantria dispar nucleopolyhedrovirus enhancin genes contribute to viral potency. J Virol 75, 8639-8648.
27. Roelvink, P. W., Corsaro, B. G. & Granados, R. R. (1995). Characterization of the Helicoverpa armigera and Pseudaletia unipuncta granulovirus enhancin genes. J Gen Virol 76, 2693-2705.
28. Shi, X., Chamankhah, M., Visal-Shah, S., Hemmingsen, S. M., Erlandson, M., Braun, L., Alting-Mees, M., Khachatourians, G. G., O'Grady, M. & Hegedus, D. D. (2004). Modeling the structure of the type I peritrophic matrix: characterization of a Mamestra configurata intestinal mucin and a novel peritrophin containing 19 chitin binding domains. Insect Biochem Mol Biol 34, 1101-1115.
29. Slavicek, J. M. & Popham, H. J. R. (2005). The Lymantria dispar nucleopolyhedrovirus enhancins are components of occlusionderived virus. J Virol 79, 10578-10588.
30. Tanada, Y. (1959). Synergism between two viruses of the armyworm Pseudaletia unipuncta (Haworth) (Lepidoptera, Noctuidae). J Insect Pathol 1, 215-231.
31. Tanada, Y., Inoue, H., Hess, R. T. & Omi, E. M. (1980). Site of action of a synergistic factor of a granulosis virus of the armyworm, Pseudaletia unipuncta. J Invertebr Pathol 35, 249-255.
32. Thiem, S. M. (2009). Baculovirus genes affecting host function. In Vitro Cell Dev Biol Anim 45, 111-126.
33. Toprak, U., Baldwin, D., Erlandson, M., Gillott, C., Hou, X., Coutu, C. & Hegedus, D. (2008). A chitin deacetylase and putative insect intestinal lipases are components of Mamestra configurata (Lepidoptera: Noctuidae) peritrophic matrix. Insect Mol Biol 17, 573-585.
34. Toprak, U., Baldwin, D., Erlandson, M., Gillott, C. & Hegedus, D. D. (2010a). Insect intestinal mucins and serine proteases associated with the peritrophic matrix from feeding, starved and moulting Mamestra configurata larvae. Insect Mol Biol 19, 163-175.
35. Toprak, U., Erlandson, M. & Hegedus, D. (2010b). Peritrophic matrix proteins. Trends Entomol 6, 23-51.
36. Towbin, H., Staehelin, T. & Gordon, J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A 76, 4350-4354.
37. Uchima, K., Harvey, J. P., Omi, E. M. & Tanada, Y. (1988). Binding sites on the midgut cell membrane of the synergistic factor of a granulosis virus of the armyworm (Pseudaletia unipunctata). Insect Biochem 18, 645-650.
38. Wang, P. & Granados, R. R. (1997a). An intestinal mucin is the target substrate for a baculovirus enhancin. Proc Natl Acad Sci U S A 94, 6977-6982.
39. Wang, P. & Granados, R. R. (1997b). Molecular cloning and sequencing of a novel invertebrate intestinal mucin cDNA. J Biol Chem 272, 16663-16669.
40. Wang, P. & Granados, R. R. (1998). Observations on the presence of the peritrophic membrane in larval Trichoplusia ni and its role in limiting baculovirus infection. J Invertebr Pathol 72, 57-62.
41. Wang, P., Hammer, D. A. & Granados, R. R. (1994). Interaction of Trichoplusia ni granulosis virus-encoded enhancin with the midgut epithelium and peritrophic membrane of four lepidopteran insects. J Gen Virol 75, 1961-1967.
42. Washburn, J. O., Kirkpatric, B. A., Haas-Stapleton, E. & Volkman, L. E. (1998). Evidence that the stilbene-derived optical brightener M2R enhances Autographa californica M nucleopolyhedrosis infection of Trichoplusia ni and Heliothis virescens by preventing sloughing of infected midgut epithelial cell. Biol Control 11, 58-69.
43. Yamamoto, T. & Tanada, Y. (1978). Phospholipid, an enhancing component in the synergistic factor of a granulosis virus of the armyworm, Pseudaletia unipuncta. J Invertebr Pathol 31, 48-56.
44. Zhu, Y., Hukuhara, T. & Tamura, K. (1989). Location of a synergistic factor in the capsule of a granulosis virus of the armyworm, Pseudaletia unipuncta. J Invertebr Pathol 54, 49-56.