A virus essential for insect host-parasite interactions encodes cystatins

Journal of Virology

Volumn 79, Issue 15, 2005, Pages 9765-9776

  Espagne, E ^a,f   Douris, V ^b   Lalmanach, G ^c   Provost, B ^a   Cattolico, L ^d   Lesobre, J ^a   Kurata, S ^e   Iatrou, K ^b   Drezen, J M ^a   Huguet, E ^a  

^a UFR des Sciences et Techniques   (France)

^b INSTITUTE OF NANOSCIENCE AND NANOTECHNOLOGY   (Greece)

^c UNIVERSITÉ DE TOURS   (France)

^d CENTRE NATIONAL DE SÉQUENÇAGE   (France)

^e TOHOKU UNIVERSITY   (Japan)

^f UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CATHEPSIN B; CATHEPSIN L; CYSTATIN; CYSTEINE PROTEINASE INHIBITOR;

ANIMAL CELL; ARTICLE; GENETIC CODE; HEMOLYMPH; HOST PARASITE INTERACTION; IMMUNE RESPONSE; INSECT CELL; LEPIDOPTERA; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; VIRUS CHARACTERIZATION; VIRUS GENE; VIRUS GENOME; WASP;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CATHEPSINS; CYSTATINS; DIPTERA; GENES, VIRAL; HOST-PARASITE RELATIONS; HUMANS; MANDUCA; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; OVUM; PAPAIN; POLYDNAVIRIDAE; SEQUENCE ALIGNMENT; WASPS;

BRACOVIRUS; COTESIA CONGREGATA; EUKARYOTA; INSECTA; MANDUCA SEXTA; VESPOIDEA;

EID: 22544453620     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.15.9765-9776.2005     Document Type: Article

References (78)

1. Abe, K., Y. Emori, H. Kondo, K. Suzuki, and S. Araic. 1987. Molecular cloning of a cysteine proteinase inhibitor of rice (oryzacystatin). Homology with animal cystatins and transient expression in the ripening process of rice seeds. J. Biol. Chem. 262:16793-16797.
2. Abrahamson, M., M. Alvarez-Fernandez, and C. M. Nathanson. 2003. Cystatins. Biochem. Soc. Symp. 2003:179-199.
3. Albrecht, U., T. Wyler, R. Pfister-Wilhelm, A. Gruber, P. Stettler, P. Heiniger, F. Kurt, D. Schümperli, and B. Lanzrein. 1994. Polydnavirus of the parasitic wasp Chelonus inanitus (Braconidae): characterization, genome organization and time point of replication. J. Gen. Virol. 75:3353-3363.
4. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
5. Anastasi, A., M. A. Brown, A. A. Kembhavi, M. J. Nicklin, C. A. Sayers, D. C. Sunter, and A. J. Barrett. 1983. Cystatin, a protein inhibitor of cysteine proteinases. Improved purification from egg white, characterization, and detection in chicken serum. Biochem. J. 211:129-138.
6. Barrett, A. J., A. A. Kembhavi, M. A. Brown, H. Kirschke, C. G. Knight, M. Tamai, and K. Hanada. 1982. L1-trans-Epoxysuccinyl-leucylamido(4-guanidino) butane (E-64) and its analogues as inhibitors of cysteine proteinases including cathepsins B, H and L. Biochem. J. 201:189-198.
7. Beckage, N. E. 1998. Modulation of immune responses to parasitoids by polydnaviruses. Parasitology 116:57-64.
8. Beckage, N. E., and D. B. Gelman. 2004. Wasp parasitoid disruption of host development: implications for new biologically based strategies for insect control. Annu. Rev. Entomol. 49:299-330.
9. Beckage, N. E., D. B. Gelman, M. A. Chappell, and M. Alleyne. 1997. Effects of parasitism by the braconid wasp Cotesia congregata on metabolic rate in host larvae of the tobacco hornworm, Manduca sexta. J. Insect. Physiol. 43:143-154.
10. Beckage, N. E., F. F. Tan, K. W. Schleifer, R. D. Lane, and L. L. Cherubin. 1994. Characterisation and biological effects of Cotesia congregate polydnavirus on host larvae of the tobacco hornworm, Manduca sexta. Arch. Insect Biochem. Physiol. 26:165-195.
11. Beliveau, C., M. Laforge, M. Cusson, and G. Bellemare. 2000. Expression of a Tranosema rostrale polydnavirus gene in the spruce budworm, Choristoneura fumiferana. J. Gen. Virol. 81:1871-1880.
12. Belle, E., N. E. Beckage, J. Rousselet, M. Poirié, F. Lemeunier, and J.-M. Drezen. 2002. Visualization of polydnavirus sequences in a parasitoid wasp chromosome. J. Virol. 76:5793-5796.
13. Bode, W., R. Engh, D. Musil, U. Thiele, R. Huber, A. Karshikov, J. Brzin, J. Kos, and V. Turk. 1988. The 2.0 A X-ray crystal structure of chicken egg white cystatin and its possible mode of interaction with cysteine proteinases. EMBO J. 7:2593-2599.
14. Brillard-Bourdet, M., V. Nguyen, M. Ferrer-di Martino, F. Gauthier, and T. Moreau. 1998. Purification and characterization of a new cystatin inhibitor from Taiwan cobra (Naja naja atra) venom. Biochem. J. 331:239-244.
15. Brown, W. M., and K. M. Dziegielewska. 1997. Friends and relations of the cystatin superfamily-new members and their evolution. Protein Sci. 6:5-12.
16. Clem, R. J. 2001. Baculoviruses and apoptosis: the good, the bad, and the ugly. Cell Death Differ. 8:137-143.
17. Cole, T. J., N. E. Beckage, F. F. Tan, A. Srinivasan, and S. B. Ramaswamy. 2002. Parasitoid-host endocrine relations: self-reliance or co-optation? Insect Biochem. Mol. Biol. 32:1673-1679.
18. Cui, L., and B. A. Webb. 1996. Isolation and characterization of a member of the cysteine-rich gene family from Campoletis sonorensis polydnavirus. J. Gen. Virol. 77:797-809.
19. Delbridge, M. L., and L. E. Kelly. 1990. Sequence analysis, and chromosomal localization of a gene encoding a cystatin-like protein from Drosophila melanogaster. FEBS Lett. 274:141-145.
20. Esnard, A., F. Esnard, F. Guillou, and F. Gauthier. 1992. Production of the cysteine proteinase inhibitor cystatin C by rat Sertoli cells. FEBS Lett. 300:131-135.
21. Esnault, C., J. Maestre, and T. Heidmann. 2000. Human LINE retrotransposons generate processed pseudogenes. Nat. Genet. 24:363-367.
22. Espagne, E., C. Dupuy, E. Huguet, L. Cattolico, B. Provost, N. Martins, M. Poirie, G. Periquet, and J. M. Drezen. 2004. Genome sequence of a polydnavirus: insights into symbiotic virus evolution. Science 306:286-289.
23. Farrell, P. J., M. Lu, J. Prevost, C. Brown, L. Behie, and K. Iatrou. 1998. High-level expression of secreted glycoproteins in transformed lepidopteran insect cells using a novel expression vector. Biotechnol. Bioeng. 60:656-663.
24. Fleming, J. A. G. W., and P. J. Krell. 1993. Polydnavirus genome organization, p. 189-225. In N. Beckage, S. Thompson, and B. Federici (ed.), Parasites and pathogens of insects, vol. 1. Academic Press, New York, N.Y.
25. Fleming, J. A. G. W., and M. D. Summers. 1991. Polydnavirus DNA is integrated in the DNA of its parasitoid wasp host. Proc. Natl. Acad. Sci. USA 88:9770-9774.
26. Fujimoto, Y., A. Kobayashi, S. Kurata, and S. Natori. 1999. Two subunits of the insect 26/29-kDa proteinase are probably derived from a common precursor protein. J. Biochem. (Tokyo) 125:566-573.
27. Gelman, D. B., D. A. Reed, and N. E. Beckage. 1998. Manipulation of fifth-instar host (Manduca sexta) ecdysteroid levels by the parastoid wasp Cotesia congregata. J. Insect Physiol. 44:833-843.
28. Goto, S. G., and D. L. Denlinger. 2002. Genes encoding two cystatins in the flesh fly Sarcophaga crassipalpis and their distinct expression patterns in relation to pupal diapause. Gene 292:121-127.
29. Gruber, A., P. Stettler, P. Heiniger, D. Schumperli, and B. Lanzrein. 1996. Polydnavirus DNA of the braconid wasp Chelonus inanitus is integrated in the wasp genome and excised only in later pupal and adult stages of the female. J. Gen. Virol. 77:2873-2879.
30. Hartmann, S., B. Kyewski, B. Sonnenburg, and R. Lucius. 1997. A filarial cysteine protease inhibitor down-regulates T cell proliferation and enhances interleukin-10 production. Eur. J. Immunol. 27:2253-2260.
31. Harwood, S. H., and N. E. Beckage. 1994. Purification and characterization of an early-expressed polynavirus induced protein from the hemolymph of Manduca sexta larvae parasitized by Cotesia congregata. Insect Biochem. Mol. Biol. 24:685-698.
32. Homma, K., S. Kurata, and S. Natori. 1994. Purification, characterization, and cDNA cloning of procathepsin L from the culture medium of NIH-Sape-4, an embryonic cell line of Sarcophaga peregrina (flesh fly), and its involvement in the differentiation of imaginal discs. J. Biol. Chem. 269:15258-15264.
33. Huang, Q., Q. L. Deveraux, S. Maeda, G. S. Salvesen, H. R. Stennicke, B. D. Hammock, and J. C. Reed. 2000. Evolutionary conservation of apoptosis mechanisms: lepidopteran and baculoviral inhibitor of apoptosis proteins are inhibitors of mammalian caspase-9. Proc. Natl. Acad. Sci. USA 97:1427-1432.
34. Jaattela, M., and J. Tschopp. 2003. Caspase-independent cell death in T lymphocytes. Nat. Immunol. 4:416-423.
35. Johner, A., and B. Lanzrein. 2002. Characterization of two genes of the polydnavirus of Chelonus inanitus and their stage-specific expression in the host Spodoptera littoralis. J. Gen. Virol. 83:1075-1085.
36. Keith, M. B., P. J. Farrell, K. Iatrou, and L. A. Behie. 2000. Use of flow cytometry to rapidly optimize the transfection of animal cells. BioTechniques 28:148-154.
37. Kroemer, J. A., and B. A. Webb. 2004. Polydnavirus genes and genomes: emerging gene families and new insights into polydnavirus replication. Annu. Rev. Entomol. 49:431-456.
38. Kurata, S., H. Saito, and S. Natori. 1992. The 29-kDa hemocyte proteinase dissociates fat body at metamorphosis of Sarcophaga. Dev. Biol. 153:115-121.
39. Kurata, S., H. Saito, and S. Natori. 1992. Purification of a 29-kDa hemocyte proteinase of Sarcophaga peregrina. Eur. J. Biochem. 204:911-914.
40. Laber, B., K. Krieglstein, A. Henschen, J. Kos, V. Turk, R. Huber, and W. Bode. 1989. The cysteine proteinase inhibitor chicken cystatin is a phosphoprotein. FEBS Lett. 248:162-168.
41. Lapointe, R., R. Wilson, L. Vilaplana, D. R. O'Reilly, P. Falabella, V. Douris, M. Bernier-Cardou, F. Pennacchio, K. Iatrou, C. Malva, and J. A. Olszewski. 2005. Expression of a Toxoneuron nigriceps polydnavirus (TnBV) encoded protein, causes apoptosis-like programmed cell death in lepidopteran insect cells. J. Gen. Virol. 86:963-971.
42. Lavine, M. D., and N. E. Beckage. 1996. Temporal pattern of parasitism-induced immunosuppression in Manduca sexta larvae parasitized by Cotesia congregata. J. Insect Physiol. 42:41-51.
43. Le, N. T., S. Asgari, K. Amaya, F. F. Tan, and N. E. Beckage. 2003. Persistence and expression of Cotesia congregata polydnavirus in host larvae of the tobacco hornworm, Manduca sexta. J. Insect Physiol. 49:533-543.
44. Lecaille, F., E. Weidauer, M. A. Juliano, D. Bromme, and G. Lalmanach. 2003. Probing cathepsin K activity with a selective substrate spanning its active site. Biochem. J. 375:307-312.
45. Lu, M., P. J. Farrell, R. Johnson, and K. Iatrou. 1997. A baculovirus (Bombyx mori nuclear polyhedrosis virus) repeat element functions as a powerful constitutive enhancer in transfected insect cells. J. Biol. Chem. 272:30724-30728.
46. Lustigman, S., J. H. McKerrow, K. Shah, J. Lui, T. Huima, M. Hough, and B. Brotman. 1996. Cloning of a cysteine protease required for the molting of Onchocerca volvulus third stage larvae. J. Biol. Chem. 271:30181-30189.
47. Maizels, R. M., M. L. Blaxter, and A. L. Scott. 2001. Immunological genomics of Brugia malayi: filarial genes implicated in immune evasion and protective immunity. Parasite Immunol. 23:327-344.
48. Muir, A., A. Lever, and A. Moffet. 2004. Expression and functions of human endogenous retroviruses in the placenta: an update. Placenta 25 (Suppl. A):S16-S25.
49. Nielsen, H., J. Engelbrecht, S. Brunak, and G. von Heijne. 1997. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10:1-6.
50. Pasquier-Barre, F., C. Dupuy, E. Huguet, F. Monteiro, A. Moreau, M. Poirie, and J. M. Drezen. 2002. Polydnavirus replication: the EP1 segment of the parasitoid wasp Cotesia congregata is amplified within a larger precursor molecule. J. Gen. Virol. 83:2035-2045.
51. Provost, B., P. Varricchio, E. Arana, E. Espagne, P. Falabella, E. Huguet, R. La Scaleia, L. Cattolico, M. Poirie, C. Malva, J. A. Olszewski, F. Pennacchio, and J. M. Drezen. 2004. Bracoviruses contain a large multigene family coding for protein tyrosine phosphatases. J. Virol. 78:13090-13103.
52. Quicke, D. L. J. 1997. Parasitic wasps. Chapman & Hall, London, United Kingdom.
53. Rawlings, N. D., D. P. Tolle, and A. J. Barrett. 2004. Evolutionary families of peptidase inhibitors. Biochem. J. 378:705-716.
54. Saito, H., S. Kurata, and S. Natori. 1992. Purification and characterization of a hemocyte proteinase of Sarcophaga, possibly participating in elimination of foreign substances. Eur. J. Biochem. 209:939-944.
55. Saito, H., T. Suzuki, K. Ueno, T. Kubo, and S. Natori. 1989. Molecular cloning of cDNA for sarcocystatin A and analysis of the expression of the sarcocystatin A gene during development of Sarcophaga peregrina. Biochemistry 28:1749-1755.
56. Sali, A., and V. Turk. 1987. Prediction of the secondary structures of stefins and cystatins, the low-molecular mass protein inhibitors of cysteine proteinases. Biol. Chem. Hoppe Seyler 368:493-499.
57. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
58. Savary, S., N. E. Beckage, F. Tan, G. Periquet, and J. M. Drezen. 1997. Excision of the polydnavirus chromosomal integrated EP1 sequence of the parasitoid wasp Cotesia congregata (Braconidae, Microgastrinae) at potential recombinase binding sites. J. Gen. Virol. 78:3125-3134.
59. Schierack, P., R. Lucius, B. Sonnenburg, K. Schilling, and S. Hartmann. 2003. Parasite-specific immunomodulatory functions of filarial cystatin. Infect. Immun. 71:2422-2429.
60. Shiba, H., D. Uchida, H. Kobayashi, and M. Natori. 2001. Involvement of cathepsin B- and L-like proteinases in silk gland histolysis during metamorphosis of Bombyx mori. Arch. Biochem. Biophys. 390:28-34.
61. Stoka, V., B. Turk, S. L. Schendel, T. H. Kim, T. Cirman, S. J. Snipas, L. M. Ellerby, D. Bredesen, H. Freeze, M. Abrahamson, D. Bromme, S. Krajewski, J. C. Reed, X. M. Yin, V. Turk, and G. S. Salvesen. 2001. Lysosomal protease pathways to apoptosis. Cleavage of bid, not pro-caspases, is the most likely route. J. Biol. Chem. 276:3149-3157.
62. Stoltz, D. B., P. J. Krell, M. D. Summers, and S. B. Vinson. 1984. Polydnaviridae-a proposed family of insect viruses with segmented, double-stranded, circular DNA genomes. Intervirology 21:1-4.
63. Strand, M. R., and L. L. Pech. 1995. Microplitis demolitor polydnavirus induces apoptosis of a specific haemocyte morphotype in Pseudoplusia includens. J. Gen. Virol. 76:283-291.
64. Suzuki, T., and S. Natori. 1986. Changes in the amount of sarcocystatin A, a new cysteine protease inhibitor, during the development of adult Sarcophaga peregrina. Insect Biochem. Mol. Biol. 16:589-595.
65. Suzuki, T., and S. Natori. 1985. Purification and characterization of an inhibitor of the cysteine protease from the hemolymph of Sarcophaga peregrina larvae. J. Biol. Chem. 260:5115-5120.
66. Takahashi, N., S. Kurata, and S. Natori. 1993. Molecular cloning of cDNA for the 29 kDa proteinase participating in decomposition of the larval fat body during metamorphosis of Sarcophaga peregrina (flesh fly). FEBS Lett. 334:153-157.
67. Teramoto, T., and T. Tanaka. 2004. Mechanism of reduction in the number of the circulating hemocytes in the Pseudaletia separata host parasitized by Cotesia kariyai. J. Insect Physiol. 50:1103-1111.
68. Turnbull, M., and B. Webb. 2002. Perspectives on polydnavirus origins and evolution. Adv. Virus Res. 58:203-254.
69. Verdot, L., G. Lalmanach, V. Vercruysse, J. Hoebeke, F. Gauthier, and B. Vray. 1999. Chicken cystatin stimulates nitric oxide release from interferon-gamma-activated mouse peritoneal macrophages via cytokine synthesis. Eur. J. Biochem. 266:1111-1117.
70. Volkoff, A. N., P. Cerutti, J. Rocher, M. C. Ohresser, G. Devauchelle, and M. Duonor-Cerutti. 1999. Related RNAs in lepidopteran cells after in vitro infection with Hyposoter didymator virus define a new polydnavirus gene family. Virology 263:349-363.
71. Vray, B., S. Hartmann, and J. Hoebeke. 2002. Immunomodulatory properties of cystatins. Cell Mol. Life Sci. 59:1503-1512.
72. Webb, B. A. 1998. Polydnavirus biology, genome structure, and evolution, p. 105-139. In L. K. Miller and L. A. Balls (ed.), The insect viruses. Plenum Publishing Corporation, New York, N.Y.
73. Whitfield, J. B. 2002. Estimating the age of the polydnavirus/braconid wasp symbiosis. Proc. Natl. Acad. Sci. USA 99:7508-7513.
74. Whitfield, J. B. 1990. Parasitoids, polydnaviruses and endosymbiosis. Parasitol. Today 6:381-384.
75. Whitfield, J. B. 1998. Phylogeny and evolution of host-parasitoid interactions in hymenoptera. Annu. Rev. Entomol. 43:129-151.
76. Whitfield, J. B., and S. Asgari. 2003. Virus or not? Phylogenetics of polydnaviruses and their wasp carriers. J. Insect Physiol. 49:397-405.
77. Xu, D., and D. B. Stoltz. 1991. Evidence for a chromosomal location of polydnavirus DNA in the ichneumonid parasitoid Hyposoter fugitivus. J. Virol. 65:6693-6704.
78. Xu, Y., and H. Kawasaki. 2001. Isolation and expression of cathepsin B cDNA in hemocytes during metamorphosis of Bombyx mori. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 130:393-399.