Venom glands from the ectoparasitoid Nasonia vitripennis (Walker) (hymenoptera: Pteromalidae) produce a calreticulin-like protein that functions in developmental arrest and cell death in the flesh fly host, Sarcophaga bullata parker (diptera: Sarcophagidae)

Insect Physiology: New Research

Volumn , Issue , 2008, Pages 259-278

  Rivers, David B ^a   Brogan, Ashley ^a  

^a LOYOLA UNIVERSITY MARYLAND   (United States)

Author keywords

Apoptosis; Intracellular calcium; Oncosis; Signal transduction; Venom protein

Indexed keywords

EID: 84984857397     PISSN: None     EISSN: None     Source Type: Book    
DOI: None     Document Type: Chapter

References (44)

1. Abt, M., Rivers, D.B. 2007. Characterization of phenoloxidase activity in venom from the ectoparasitoid Nasonia vitripennis (Walker)(Hymenoptera: Pteromalidae). Journal of Invertebrate Pathology 94, 108-118.
2. Arnaudeau, S., Frieden, M., Nakamura, K., Castelbou, C., Michalak, M., Demaurex, N. 2002. Calreticulin differentially modulates calcium uptake and release in the endoplasmic reticulum and mitochondria. Journal of Biological Chemistry 277, 46696-46705.
3. Asgari, S., Zhang, G., Zareie, R., Schmidt, O. 2003. A serine proteinase homolog venom protein from an endoparasitoid wasp inhibits melanization of the host hemolymph. Insect Biochemostry and Molecular Biology 33, 1017-1024.
4. Beckage, N.E., Riddiford, L.M. 1978. Developmental interactions between the tobacco hornworm Manduca sexta and its braconid parasite Apanteles congregata. Entomologia Experimentalis et Applicata 23, 139-151.
5. Cerenius, L., Söderhall, K., 2004. The prophenoloxidase-activating system in invertebrates. Immunological Reviews 198, 116-126.
6. Charalambidis, N.D., Foukas, L.C., Zervas, C.G., Marmaras, V.J. 1996. Hemocyte surface phenoloxidase and immune response to lipopolysaccharide (LPS) in Ceratitis capitata. Insect Biochemistry and Molecular Biology 26, 867-874.
7. Chase, M.R., Raina, K., Bruno, J., Sugumaran, M. 2000. Purification, characterization and molecular cloning of prophenoloxidases from Sarcophaga bullata. Insect Biochemistry and Molecular Biology 30, 953-967.
8. Choi, J.Y., Whitten, M.M.A., Cho, M.Y., Lee, K.Y., Kim, M.S., Ratcliffe, N.A., Lee, B.L. 2002. Calreticulin enriched as an early-stage encapsulation protein in wax moth Galleria mellonella larvae. Developmental and Comparative Immunology 26, 335-343.
9. Davies, T.R., Wickham, T.J., McKenna, K.A., 1993. Comparative recombinant protein production of eight insect cell lines. In Vitro Cellular and Developmental Biology-Animal 29, 388.
10. Denlinger, D.L., 1972. Induction and termination of pupal diapause in Sarcophaga (Diptera: Sarcophagidae). Biological Bulletin 142, 11-24.
11. Digilio, M.C., Isidoro, N., Tremblay, E., Pennacchio, F., 2000. Host castration by Aphidius ervi venom proteins. Journal of Insect Physiology 46, 1041-1050.
12. Doury, G., Bigot, Y., Periquet, G. 1997. Physiological and biochemical analysis of factors in the female venom gland and larval salivary secretions of the ectoparasitoid wasp Eupelmus orientalis. Journal of Insect Physiology 43, 69-81.
13. Ferreira, V., Molina, M.C., Valck, C., Rojas, A., Aguilar, L., Ramirez. G. 2004. Role of calreticulin from parasites in its interaction with vertebrate hosts. Molecular Immunology 40, 1279-1291.
14. Firestone G.L., Winguth, S.D. 1990. Immunoprecipitation of proteins. In: Deutscher, M.P. (Ed.), Guide to protein purification, Academic Press, London. pp. 688-700.
15. Garfin, D.E. 1990. One-dimensional gel electrophoresis. In: Deutscher, M.P. (Ed.), Guide to protein purification, Academic Press, London. pp. 425-440.
16. Gomperts, B.D., Kramer, I.M., Tatham, P.E.R., 2002. Signal transduction. Academic Press, San Diego.
17. Himeno, M., Koyama, N., Funato, J., Komano, T., 1985. Mechanism of action of Bacillus thuringiensis insecticidal delta-endotoxins on insect cells in vitro. Agricultural Biological Chemistry 1, 1461-1468.
18. Jones, D., Sawicki, G., Wozniak, M. 1992. Sequence, structure, and expression of a wasp venom protein with a negatively charged signal peptide and a novel repeating internal structure. Journal of Biological Chemistry 267, 14871-14878.
19. Kuraishi, T., Manaka, J., Kono, M., Ishii, H., Yamamoto, N., Koizumi, K., Shiratsuchi, A., Lee, B.L., Higashida, H., Nakanishi, Y. 2007. Identification of calreticulin as a marker for phagocytosis of apoptotic cells in Drosophila. Experimental Cell Research 313, 500-510.
20. Majno, G., Joris, I., 1995. Apoptosis, oncosis, and necrosis. An overview of cell death. American Journal of Pathology 146, 3-15.
21. Marmaras, V.J., Charalambidis N.D., Zervas, C.G. 1996. Immune response in insects: the role of phenoloxidase in defense reactions in relation to melanization and sclerotization. European Journal of Biochemistry 31, 119-133.
22. Michalak, M., Corbett, E., Mesaeli, N., Nakamura, K., Opas, M. 1999. Calreticulin. Biochemical Journal 344. 281-292.
23. Nakamatsu, Y., Tanaka T., 2003. Venom of ectoparasitoid, Euplectrus sp near plathypenae (Hymenoptera: Eulophidae) regulates the physiological state of Pseudaletia separata (Lepidoptera: Noctuidae) host as a food resource. Journal of Insect Physiology 49, 149-159.
24. Ohtaki, T., 1966. On the delayed pupation of the flesh fly, Sarcophagi peregrina Robineau-Desvoiday. Japanese Journal of Medicinal Science and Biology 19, 97-104.
25. Parkinson, N.M. Richards. E.H., Conyers, C., Smith, I., Edwards, J.P. 2002. Analysis of venom constituents from the parasitoid wasp Pimpla hypochondriaca and cloning of cDNA encoding a venom protein. Insect Biochemistry and Molecular Biology 32, 729-735.
26. Parkinson, N.M., Weaver R.J., 1999. Noxious components of venom from the pupa- specific parasitoid Pimpla hypochondriaca. Journal of Invertebrate Pathology 73, 73-84.
27. Petit, P.X., Susin, S.-A., Zamzami, N., Mignotte, B., Kroemer, G., 1996. Mitochondria and programmed cell death: back to the future. FEBS Letters 396, 7-13.
28. Ratcliffe, N.A., King, P.E. 1967. The venom system of Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae). Proceedings of the Royal Entomological Society (London) 42, 49-61.
29. Rivers, D.B. 2004. Evaluation of host responses to envenomation as a means to access ectoparasitic pteromalid wasp's potential for controlling manure-breeding flies. Biological Control 30, 181-192.
30. Rivers, D.B., Crawley, T. Bauser, H. 2005. Localization of intracellular calcium release in cells injured by venom from the ectoparasitoid Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae) and dependence of calcium mobilization on G-protein activation. Journal of Insect Physiology 51, 149-160.
31. Rivers, D.B., Denlinger, D.L., 1994. Developmental fate of the flesh fly, Sarcophaga bulata(Diptera: Sarcophagidae), envenomated by the pupal extoparasitioid, Nasonia vitripennis (Hymenoptera:Pteromalidae). Journal of Insect Physiology 40, 121-127.
32. Rivers, D.B., Denlinger, D.L., 1995. Venom-induced alterations in fly lipid metabolism and its impact on larval development of the ectoparasitiod Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae. Journal of Invertebrate Pathology 66, 104-110.
33. Rivers, D.B., Genco, M., Sanchez, R.A., 1999. In vitro analysis of venom from the wasp Nasonia vitripennis: susceptibility of different cell lines and venom-induced changes in plasma membrane permeability. In Vitro Cellular and Developmental Biology- Animal 35, 102-110.
34. Rivers, D.B., Hink, W.F., Denlinger, D.L., 1993. Toxicity of the venom from Nasonia vitripennis (Hymenoptera:Pteromalidae) toward fly hosts, nontarget insects, different developmental stages, and cultured insect cells. Toxicon 31, 755-765.
35. Rivers, D.B., Pagnotta, M.A., Huntington, E.R., 1998. Reproductive strategies of 3 species of ectoparasitic wasps are modulated by the response of the fly host, Sarcophaga bullata (Diptera: Sarcophagidae) to parasitism. Annals of the Entomological Society of America 91, 458-465.
36. Rivers, D.B., Rocco, M.M., Frayha, A.R., 2002b. Venom from the ectoparasitic wasp Nasonia vitripennis increases Na+ influx and activates phospholipase C and phospholipase A2 dependent signal transduction pathways in cultured insect cells. Toxicon 40, 9-21.
37. Rivers, D.B., Ruggiero, L. Hayes, M. 2002a. The ectoparasitic wasp Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae) differentially affects cells mediating the immune response of its flesh fly host, Sarcophaga bullata Parker (Diptera: Sarcophagidae). Journal of Insect Physiology 48, 1053-1064.
38. Rivers, D.B., Uçkan, F., Ergin, E. 2006. Characterization and biochemical analyses of venom from the ectoparasitic wasp Nasonia vitripennis (Walker)(Hymenoptera: Pteromalidae). Archives of Insect Biochemistry and Physiology 61, 24-41.
39. Rivers, D.B., Zdarek, J., Denlinger, D.L., 2004. Disruption of pupariation and eclosion behavior in the flesh fly, Sarcophaga bullata Parker (Diptera: Sarcophagidae), by venom from the ectoparasitic wasp Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae). Archives of Insect Biochemistry and Physiology 57, 78-91.
40. Spiro, R.G., Zhu, Q., Bhoyroo, Söling, H-D. 1996. Definition of the lectin-like properties of the molecular chaperone, calreticulin, and demonstration of its co-purification with endomannosidase from rat liver golgi. Journal of Biological Chemistry 271, 11588-11594.
41. Trump, B.F., Berezesky, I.K., 1995. Calcium-mediated cell injury and cell death. FASEB Journal 9, 219-228.
42. Wylie, H.G., 1971. Oviposition restraint of Muscidifurax zaraptor (Hymenoptera: Pteromalidae) on parasitized housefly pupae. Canadian Entomologist 103, 1537-1544.
43. Zdarek, J., Slama, K., Fraenkel, G. 1979. Changes in internal pressure during puparium formation in flies. Journal of Experimental Zoology 207, 187-196.
44. Zhang, G., Schmidt, O., Asgari, S. 2006. A calreticulin-like protein from endoparasitoid venom fluid is involved in host hemocyte inactivation. Developmental and Comparative Immunology 30, 756-764.