Abstract
Although microbial insecticides are generally safe for vertebrates, plants and the environment, their use has been very limited, mainly because their cost of pest control is much higher than that of chemical insecticides. To expand the use of microbial insecticides, their ability to kill pests needs to be strengthened. Increased activity will reduce the amount applied per unit area and the cost of pest control. The protein fusolin that is produced by the insect viruses entomopoxviruses and baculoviruses strongly synergistically increases the infectivity of insect viruses. Recent studies further elucidated the synergistic effect of the protein on the insecticidal activity of major entomopathogenic bacterium Bacillus thuringiensis. Furthermore studies have revealed that fusolin is a lytic chitin monooxygenase, and thus the mechanism of increase in the infectivity and insecticidal activity by fusolin has been elucidated in detail. These advances have expanded the possible practical applications of this protein to pest control and suggest its potential for use in a new field, namely, the development of technologies for efficient biofuel production from biomass such as chitin.
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Aachmann FL, Sørlie M, Skjå-Bræk G, Eijsink VGH, Vaaje-Kolstad G (2012) NMR structure of a lytic polysaccharide monooxygenase provides insight into copper binding, protein dynamics, and substrate interactions. Proc Natl Acad Sci U S A 109:18779–18784
Adams JR, Wilcox TA (1968) Histopathology of the almond moth, Cadra cautella, infected with a nuclear-polyhedrosis virus. J Invertebr Pathol 12:269–274
Afonso CL, Tulman ER, Lu Z, Oma E, Kutish GF, Rock DL (1999) The genome of Melanoplus sanguinipes entomopoxvirus. J Virol 73:533–552
Bawden AL, Glassberg KJ, Diggans J, Shaw R, Farmerie W, Moyer RW (2000) Complete genomic sequence of the Amsacta moorei entomopoxvirus: analysis and comparison with other poxviruses. Virology 274:120–139
Chakraborty M, Narayanan K, Sivaprakash MK (2004) In vivo enhancement of nucleopolyhedrovirus of oriental armyworm, Mythimna separata using spindles from Helicoverpa armigera entomopoxvirus. Indian J Exp Biol 42:121–123
Chakraborty M, Narayanan K, Suryanarayana VVS, Sivaprakash MK (2005) Enhancement of nucleopolyhedrovirus of oriental armyworm, Mythimna separata (Lepidoptera: Noctuidae) using diamond shaped inclusion bodies of Galleria mellonella NPV (Lepidoptera: Pyralidae). Entomon 30:343–346
Chiu E, Coulibaly F, Metcalf P (2012) Insect virus polyhedra, infectious protein crystals that contain virus particles. Curr Opin Struct Biol 22:234–240
Chiu E, Hijnen M, Bunker R, Boudes M, Rajendran C, Aizel K, Olieric V, Schulze-Briese C, Mitsuhashi W, Young V, Ward VK, Bergoin M, Metcalf P, Coulibaly F (2015) Structural basis for the enhancement of virulence by viral spindles and their in vivo crystallization. Proc Natl Acad Sci U S A 112:3973–3978
Derksen ACG, Granados RR (1988) Alteration of a lepidopteran peritrophic membrane by baculoviruses and enhancement of viral infectivity. Virology 167:242–250
Din N, Gilkes NR, Tekant B, Miller RC, Warren AJ, Kilburn DG (1991) Non-hydrolytic disruption of cellulose fibres by the binding domain of a bacterial cellulose. Nat Biotechnol 9:1096–1099
Din N, Damude HG, Gilkes NR, Miller RC Jr, Warren RAJ, Kilburn DG (1994) C1-Cx revisited: intramolecular synergism in a cellulase. Proc Natl Acad Sci U S A 91:11383–11387
Frederiksen RF, Paspaliari DK, Larsen T, Storgaard BG, Larsen MH, Ingmer H, Palcic MM, Leisner JJ (2013) Bacterial chitinases and chitin-binding proteins as virulence factors. Microbiology 159:833–847
Furuta Y, Mitsuhashi W, Kobayashi J, Hayasaka S, Imanishi S, Chinzei Y, Sato M (2001) Peroral infectivity of non-occluded viruses of Bombyx mori nucleopolyhedrovirus and polyhedrin-negative recombinant baculoviruses to silkworm larvae is drastically enhanced when administered with Anomala cuprea entomopoxvirus spindles. J Gen Virol 82:307–312
Gelfand I, Sahajpal R, Zhang X, Izaurralde RC, Gross KL, Robertson GP (2013) Sustainable bioenergy production from marginal lands in the US Midwest. Nature 493:514–517
Goto C (1990) Enhancement of a nuclear polyhedrosis virus (NPV) infection by a granulosis virus (GV) isolated from the spotted cutworm, Xestia c-nigrum L. (Lepidoptera: Noctuidae). Appl Entomol Zool 25:135–137
Gross CH, Wolgamot GM, Russell RLQ, Pearson MN, Rohmann GF (1993) A 37-kilodalton glycoprotein from a baculovirus of Orgyia pseudotsugata is localized to cytoplasmic inclusion bodies. J Virol 67:469–475
Hayakawa T, Shitomi Y, Miyamoto K, Hori H (2004) GalNAc pretreatment inhibits trapping of Bacillus thuringiensis Cry1Ac on the peritrophic membrane of Bombyx mori. FEBS Lett 576:331–335
Hayakawa T, Xu J, Hukuhara T (1996) Cloning and sequencing of the gene for an enhancing factor from Pseudaletia separata entomopoxvirus. Gene 177:269–270
Huger AM, Krieg A (1968) On spindle-shaped cytoplasmic inclusions associated with a nuclear polyhedrosis of Choristoneura murinana. J Invertebr Pathol 12:461–462
Hukuhara T, Tamura K, Zhu Y, Abe H, Tanada Y (1987) Synergistic factor shows specificity in enhancing nuclear polyhedrosis virus infections. Appl Entomol Zool 22:235–236
Lai-Fook J, Dall DJ (2000) Spindle bodies of Heliothis armigera entomopoxvirus develop in structures associated with host cell endoplasmic reticulum. J Invertebr Pathol 75:183–192
Levasseur A, Drula E, Lombard V, Coutinho PM, Henrissart B (2013) Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes. Biotechnol Biofuels 6:41
Li X, Barrett J, Pang A, Klose RJ, Krell PJ, Arif BM (2000) Characterization of an overexpressed spindle protein during a baculovirus infection. Virology 268:56–67
Li Z, Li C, Yang K, Wang L, Yin C, Gong Y, Pang Y (2003) Characterization of a chitin-binding protein GP37 of Spodoptera litura multicapsid nucleopolyhedrovirus. Virus Res 96:113–122
Liu X, Ma X, Lei C, Xiao Y, Zhang Z, Sun X (2011) Synergistic effects of Cydia pomonella granulovirus GP37 on the infectivity of nucleopolyhedroviruses and lethality of Bacillus thuringiensis. Arch Virol 156:1707–1715
Mitsuhashi W (2002) Further evidence that spindles of an entomopoxvirus enhance its infectivity in a host insect. J Invertebr Pathol 79:59–61
Mitsuhashi W (2009) Insect virus proteins involved in the peroral infectivity of the viruses and their potential practical application in pest control. In: Insect viruses: detection, characterization and roles. Nova Science Publishers, New York, pp 1–20
Mitsuhashi W (2013) Trends in studies on insect viral proteins involved in peroral infectivity of insect viruses. Sanshi-Konchu Biotechnol 82:99–108. (in Japanese)
Mitsuhashi W, Asano S, Miyamoto K, Wada S (2014a) Further research on the biological function of inclusion bodies of Anomala cuprea entomopoxvirus, with special reference to effect on the insecticidal activity of a Bacillus thuringiensis formulation. Pest Manag Sci 70:46–54
Mitsuhashi W, Miyamoto K, Wada S (2014b) The complete genome sequence of the Alphaentomopoxvirus Anomala cuprea entomopoxvirus, including its terminal hairpin loop sequences, suggests a potentially unique mode of apoptosis inhibition and mode of DNA replication. Virology 452–453:95–116
Mitsuhashi W, Furuta Y, Sato M (1998) The spindles of an entomopoxvirus of Coleoptera (Anomala cuprea) strongly enhance the infectivity of a nucleopolyhedrovirus in Lepidoptera (Bombyx mori). J Invertebr Pathol 71:186–188
Mitsuhashi W, Kawakita H, Murakami R, Takemoto Y, Saiki T, Miyamoto K, Wada S (2007) Spindles of an entomopoxvirus facilitate its infection of the host insect by disrupting the peritrophic membrane. J Virol 81:4235–4243
Mitsuhashi W, Miyamoto K (2003) Disintegration of the peritrophic membrane of silkworm larvae due to spindles of an entomopoxvirus. J Invertebr Pathol 82:34–40
Mitsuhashi W, Murakami R, Takemoto Y, Miyamoto K, Wada S (2008) Stability of the viral-enhancing ability of entomopoxvirus spindles exposed to various abiotic factors. Appl Entomol Zool 43:483–489
Mitsuhashi W, Sato M (2000) Enhanced infection of a nucleopolyhedrovirus in a lepidopteran pest (Spilosoma imparilis) by spindles of a coleopteran entomopoxvirus (EPV) (Anomala cuprea EPV). J For Res 5:285–287
Mitsuhashi W, Sato M, Hirai Y (2000) Involvement of spindles of an entomopoxvirus (EPV) in infectivity of the EPVs to their host insect. Arch Virol 145:1465–1471
Olszewski JA, Dall DJ (2002) Assessment of foreign protein production by recombinant Heliothis (Helicoverpa) armigera entomopoxviruses in Spodoptera frugiperda cells. J Gen Virol 83:451–461
Phanis CG, Miller DP, Cassar SC, Tristem M, Thiem SM, O’Reilly DR (1999) Identification and expression of two baculovirus gp37 genes. J Gen Virol 80:1823–1831
Peng J, Zhong J, Granados RR (1999) A baculovirus enhancin alters the permeability of a mucosal midgut peritrophic matrix from lepidopteran larvae. J Insect Physiol 45:159–166
Salvador R, Ferrelli ML, Berretta MF, Mitsuhashi W, Biedma ME, Romanowski V, Sciocco-Cap A (2012) Analysis of EpapGV gp37 gene reveals a close relationship between granulovirus and entomopoxvirus. Virus Genes 45:610–613
Takemoto Y, Mitsuhashi W, Murakami R, Konishi H, Miyamoto K (2008) The N-terminal region of an entomopoxvirus fusolin is essential for the enhancement of peroral infection, whereas the C-terminal region is eliminated in digestive juice. J Virol 82:12406–12415
Tanada Y (1959) Synergism between two viruses of the armyworm, Pseudaletia unipuncta (Haworth) (Lepidoptera, Noctuidae). J Invertebr Pathol 1:215–231
Thézé J, Takatsuka J, Nakai M, Arif B, Herniou EA (2015) Gene acquisition convergence between entomopoxviruses and baculoviruses. Viruses 7:1960–1974
Vaaje-Kolstad G, Westereng B, Horn SJ, Liu Z, Zhai H, Sørlie M, Eijsink VGH (2010) An oxidative enzyme boosting the enzymatic conversion of recalcitrant polysaccharides. Science 330:219–222
Vialard JE, Yuen L, Richardson CD (1990) Identification and characterization of a baculovirus occlusion body glycoprotein which resembles spheroidin, an entomopoxvirus protein. J Virol 64:5804–5811
Wang P, Granados RR (1997) An intestinal mucin is the target substrate for a baculovirus enhancin. Proc Natl Acad Sci U S A 94:6977–6982
Wang P, Granados RR (2000) Calcofluor disrupts the midgut defense system in insects. Insect Biochem Mol Biol 30:135–143
Wang P, Granados RR (2001) Molecular structure of the peritrophic membrane (PM): identification of potential PM target sites for insect control. Arch Insect Biochem Physiol 47:110–118
Wang P, Hammer DA, Granados RR (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
Wijonarko A, Hukuhara T (1998) Detection of a virus enhancing factor in the spheroid, spindle, and virion of an entomopoxvirus. J Invertebr Pathol 72:82–86
Xu J, Hukuhara T (1992) Enhanced infection of a nuclear polyhedrosis virus in larvae of the armyworm, Pseudaletia separata, by a factor in the spheroids of an entomopoxvirus. J Invertebr Pathol 60:259–264
Yaman M, Acar KF, Radek R (2015) A nucleopolyhedrovirus from the Mediterranean flour moth, Ephestia kuehniella (Lepidoptera: Pyralidae). Appl Entomol Zool 50:355–359
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Mitsuhashi, W. (2018). Analysis of the Viral Lytic Polysaccharide Monooxygenase Fusolin and Its Potential Application to Pest Control. In: Kumar, D., Gong, C. (eds) Trends in Insect Molecular Biology and Biotechnology. Springer, Cham. https://doi.org/10.1007/978-3-319-61343-7_7
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