Venom proteins from endoparasitoid wasps and their role in host-parasite interactions

Annual Review of Entomology

Volumn 56, Issue , 2011, Pages 313-335

  Asgari, Sassan ^a   Rivers, David B ^b  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b LOYOLA UNIVERSITY MARYLAND   (United States)

Author keywords

development; host manipulation; immunity; koinobiont

Indexed keywords

INSECT PROTEIN; VENOM;

ANIMAL; ARTICLE; CHEMISTRY; HOST PARASITE INTERACTION; IMMUNOLOGY; PHYSIOLOGY; WASP;

ANIMALS; HOST-PARASITE INTERACTIONS; INSECT PROTEINS; VENOMS; WASPS;

HEXAPODA;

EID: 77958472770     PISSN: 00664170     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev-ento-120709-144849     Document Type: Article

References (116)

1. Abt M, Rivers DB. 2007. Characterization of phenoloxidase activity in venom from the ectoparasitoid Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae). J. Invertebr. Pathol. 94:108-18
2. Andersen SO. 2005. Cuticular sclerotization and tanning. In Comprehensive Molecular Insect Science, ed. LI Gilbert, K Iatrou, S Gill, pp. 145-70. Oxford, UK: Elsevier
3. Asgari S, Schmidt O. 2003. Is cell surface calreticulin involved in phagocytosis by insect hemocytes? J. Insect Physiol. 49:545-50
4. Asgari S, Zareie R, Zhang G, Schmidt O. 2003. Isolation and characterization of a novel venom protein from an endoparasitoid, Cotesia rubecula (Hym: Braconidae). Arch. Insect Biochem. Physiol. 53:92-100
5. 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 Biochem. Mol. Biol. 33:1017-24
6. Askew RR, Shaw MR. 1986. Parasitoid communities: their size, structure and development. In Insect Parasitoids, ed. J Waage, D Greathead, pp. 225-63. London: Academic
7. Bai S, Cai D, Li X. 2009. Parasitic castration of Plutella xylostella larvae induced by polydnaviruses and venom of Cotesia vestalis and Diadegma semiclausum polydnaviruses and venom of Cotesia vestalis and Diadegma semiclausum. Arch. Insect Biochem. Physiol. 70:30-43
8. Beck M, Theopold U, Schmidt O. 2000. Evidence for serine protease inhibitor activity in the ovarian calyx fluid of the endoparasitoid Venturia canescens. J. Insect Physiol. 46:1275-83
9. Beck MH, Strand MR. 2007. Anovel polydnavirus protein inhibits the insect prophenoloxidase activation pathway. Proc. Natl. Acad. Sci. USA 104:19267-72
10. Beliveau C, Levasseur A, Stoltz D, Cusson M. 2003. Three related TrIV genes: comparative sequence analysis and expression in host larvae and Cf-124T cells. J. Insect Physiol. 49:501-11
11. Besson MT, Soustelle L, Birman S. 2000. Selective high-affinity transport of aspartate by a Drosophila homologue of the excitatory amino acid transporters. Curr. Biol. 10:207-10
12. Bourne HR, Sanders DA, McCormick F. 1991. The GTPase superfamily: conserved structure and molecular mechanisms. Nature 349:117-27
13. Bull H, Murray PG, Thomas D, Fraser AM, Nelson PN. 2002. Acid phosphatases. Mol. Pathol. 55:65-72
14. Cai J, Ye G-y, Hu C. 2004. Parasitism of Pieris rapae (Lepidoptera: Pieridae) by a pupal endopara-sitoid, Pteromalus puparum (Hymenoptera: Pteromalidae): effects of parasitization and venom on host hemocytes. J. Insect Physiol. 50:315-22
15. Cerenius L, Lee BL, Söderhäll K. 2008. The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immunol. 29:263-71
16. Chen YF, Shi M, Huang F, Chen X-x. 2007. Characterization of two genes of Cotesia vestalis polydnavirus and their expression patterns in the host Plutella xylostella. J. Gen. Viol. 88:3317-22
17. Choi JY, Whitten MMA, Cho MY, Lee KY, Kim MS, et al. 2002. Calreticulin enriched as an early-stage encapsulation protein in wax moth Galleria mellonella larvae. Dev. Comp. Immunol. 26:335-43
18. Christensen BM, Li JY, Chen CC, Nappi AJ. 2005. Melanization immune responses in mosquito vectors. Trends Parasitol. 21:192-99
19. Colinet D, Dubuffet A, Cazes D, Moreau S, Drezen JM, Poirié M. 2009. A serpin from the parasitoid wasp Leptopilina boulardi targets the Drosophila phenoloxidase cascade. Dev. Comp. Immunol. 33:681-89
20. Coudron TA, Kelly TJ, Puttler B. 1990. Developmental responses of Trichoplusia ni (Lepidoptera: Noc-tuidae) to parasitism by the ectoparasite Euplectrus plathypenae (Hymenoptera: Eulophidae). Arch. Insect Biochem. Physiol. 13:83-94
21. Crawford AM, Brauning R, Smolenski G, Ferguson C, Barton D, et al. 2008. The constituents of Microctonus sp. parasitoid venoms. Insect Mol. Biol. 17:313-24
22. Dani MP, Edwards JP, Richards EH. 2005. Hydrolase activity in the venom of the pupal endoparasitic wasp, Pimpla hypochondriaca. Comp. Biochem. Physiol. B 141:373-81
23. Dani MP, Richards EH. 2009. Cloning and expression of the gene for an insect haemocyte anti-aggregation protein (VPr3), from the venom of the endoparasitic wasp, Pimpla hypochondriaca. Arch. Insect Biochem. Physiol. 71:191-204
24. Dani MP, Richards EH, Edwards JP. 2004. Venom from the pupal endoparasitoid, Pimpla hypochondriaca, increases the susceptibility of larval Lacanobia oleracea to the entomopathogens Bacillus cereus and Beauveria bassiana. J. Invertebr. Pathol. 86:19-25
25. de Graaf DC, Brunain M, Scharlaken B, Peiren N, Devreese B, et al. 2010. Two novel proteins expressed by the venom glands of Apis mellifera and Nasonia vitripennis share an ancient C1q-like domain. Insect Mol. Biol. 19:11-26
26. Desneux N, Barta RJ, Delebecque CJ, Heimpel GE. 2009. Transient host paralysis as a means of reducing self-superparasitism in koinobiont endoparasitoids. J. Insect Physiol. 55:321-27
27. Digilio MC, Isidoro N, Tremblay E, Pennacchio F. 2000. Host castration by Aphidius ervi venom proteins. J. Insect Physiol. 46:1041-50
28. Dubuffeta A, Douryb G, Labroussea C, Drezena JM, Cartonc Y, Poirié M. 2008. Variation of success of Leptopilina boulardi in Drosophila yakuba: the mechanisms explored. Dev. Comp. Immunol. 32:597-602
29. Dubuffeta A, Dupas S, Frey F, Drezena J-M, Poirié M, Cartonc Y. 2007. Genetic interactions between the parasitoid wasp Leptopilina boulardi and its Drosophila hosts. Heredity 98:21-27
30. Dupas S, Brehelin M, Frey F, Carton Y. 1996. Immune suppressive virus-like particles in a Drosophila parasitoid: significance of their intraspecific morphological variations. Parasitology 113:207-12
31. Dupas S, Gitau GW, Branca A, Le Ru BP, Silvain JF. 2008. Evolution of a polydnavirus gene in relation to parasitoid-host species immune resistance. J. Hered. 99:491-99
32. Ergin E, Uckan F, Rivers DB, Sak O. 2006. In vivo and in vitro activity of venom from the endoparasitic wasp Pimpla turionellae (L.) (Hymenoptera: Ichneumonidae). Arch. Insect Biochem. Physiol. 61:87-97
33. Falabella P, Perugino G, Caccialupi P, Riviello L, Varricchio P, et al. 2005. A novel fatty acid binding protein produced by teratocytes of the aphid parasitoid Aphidius ervi. Insect Mol. Biol. 14:195-205
34. Falabella P, Riviello L, Caccialupi P, Rossodivita T, Valente MT, et al. 2007. A g-glutamyl transpeptidase of Aphidius ervi venom induces apoptosis in the ovaries of host aphids. Insect Biochem. Mol. Biol. 37:453-65
35. Ferreira V, Molina MC, Valck C, Rojas A, Aguilar L, et al. 2004. Role of calreticulin from parasites in its interaction with vertebrate hosts. Mol. Immunol. 40:1279-91
36. Fry BG, Roelants J, Norman JA. 2009. Tentacles of venom: toxic protein convergence in the kingdom Animalia. J. Mol. Evol. 68:311-21
37. Furihata SX, Kimura MT. 2009. Effects of Asobara japonica venom on larval survival of host and nonhost Drosophila species. Physiol. Entomol. 34:292-95
38. Gillespie JP, Kanost MR, Trenczek T. 1997. Biological mediators of insect immunity. Annu. Rev. Entomol. 42:611-43
39. Giordana B, Milani A, Grimaldi A, Farneti R, Casartelli M, et al. 2003. Absorption of sugars and amino acids by the epidermis of Aphidius ervi larvae. J. Insect Physiol. 49:1115-24
40. Jiang H, Kanost MR. 2000. The clip-domain family of serine proteinases in arthropods. Insect Biochem. Mol. Biol. 30:95-105
41. Jones D. 1996. Biochemical interaction between chelonine wasps and their lepidopteran hosts: After a decade of research-the parasite is in control. Insect Biochem. Mol. Biol. 26:981-96
42. 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. J. Biol. Chem. 267:14871-78
43. Jones D, Wache S, Chhokar V. 1996. Toxins produced by arthropod parasites: salivary gland proteins of human body lice and venom proteins of chelonine wasps. Toxicon 34:1421-29
44. Keenan B, Uckan F, Ergin E, Rivers DB. 2007. Morphological and biochemical changes in cultured cells induced by venom from the endoparasitoid, Pimpla turionellae. See Ref. 87a, pp. 75-92
45. Kitano H. 1986. The role of Apanteles glomeratus venom in the defensive response of its host, Pieris rapae crucivora. J. Insect Physiol. 32:369-75
46. Kohler LJ, Carton Y, Mastore M, Nappi AJ. 2007. Parasite suppression of the oxidations of eumelanin precursors in Drosophila melanogaster. Arch. Insect Biochem. Physiol. 66:64-75
47. Krishnan A, Nair PN, Jones D. 1994. Isolation, cloning and characterization of new chitinase stored in active form in chitin-lined venom reservoir. J. Biol. Chem. 269:20971-76
48. Kroemer JA, Webb BA. 2004. Polydnavirus genes and genomes: emerging gene families and new insights into polydnavirus replication. Annu. Rev. Entomol. 49:431-56
49. Labrosse C, Carton Y, Dubuffet A, Drezen JM, Poirie M. 2003. Active suppression of D. melanogaster immune response by long gland products of the parasitic wasp Leptopilina boulardi. J. Insect Physiol. 49:513-22
50. Labrosse C, Eslin P, Doury G, Drezen JM, Poirie M. 2005. Haemocyte changes in D. melanogaster in response to long gland components of the parasitoid wasp Leptopilina boulardi: a Rho-GAP protein as an important factor. J. Insect Physiol. 51:161-70
51. Labrosse C, Stasiak K, Lesobre J, Grangeia A, Huguet E, et al. 2005. A RhoGAP protein as a main immune suppressive factor in the Leptopilina boulardi (Hymenoptera, Figitidae)-Drosophila melanogaster interaction. Insect Biochem. Mol. Biol. 35:93-103
52. Lawrence PO. 2002. Purification and partial characterization of an entomopoxvirus (DlEPV) from a parasitic wasp of tephritid fruit flies. J. Insect Sci. 2:10
53. Lawrence PO. 2005. Morphogenesis and cytopathic effects of the Diachasmimorpha longicaudata ento-mopoxvirus in host haemocytes. J. Insect Physiol. 51:221-33
54. Leluk J, Jones D. 1989. Chelonus sp. near curvimaculatus venom proteins: analysis of their potential role and processing during development of host Trichoplusia ni. Arch. Insect Biochem. Physiol. 10:1-12
55. Leluk J, Schmidt J, Jones D. 1989. Comparative studies on the protein composition of hymenopteran venom reservoirs. Toxicon 27:105-14
56. Lewis RJ. 2004. Conotoxins as selective inhibitors of neuronal ion channels, receptors and transporters. IUBMB Life 56:89-93
57. Lu Z, Beck MH, Wang Y, Jiang H, Strand MR. 2008. The viral protein Egf1.0 is a dual activity inhibitor of prophenoloxidase-activating proteinases 1 and 3 from Manduca sexta. J. Biol. Chem. 283:21325-33
58. Mabiala-Moundoungou ADN, Doury G, Eslin P, Cherqui A, Prevost G. 2010. Deadly venom of Asobara japonica parasitoid needs ovarian antidote to regulate host physiology. J. Insect Physiol. 56:35-41
59. Marris GC, Weaver RJ, Edwards JP. 2001. Endocrine interactions of the ectoparasitoid wasps with their hosts: an overview. In Endocrine Interactions of Insects Parasites and Pathogens, ed. JP Edwards, RJ Weaver, pp. 133-51. Oxford: Bios
60. Michalak M, Milner RE, Burns K, Opas M. 1992. Calreticulin. Biochem. J. 285:681-92
61. Morales J, Chiu H, Oo T, Plaza R, Hoskins S, Govind S. 2005. Biogenesis, structure, and immune-suppressive effects of virus-like particles of a Drosophila parasitoid, Leptopilina victoriae. J. Insect Physiol. 51:181-95
62. Moreau A, Guillot S. 2005. Advances and prospects on biosynthesis, structures and functions of venom proteins from parasitic wasps. Insect Biochem. Mol. Biol. 35:1209-23
63. Moreau SJM, Cherqui A, Doury G, Dubois F, Fourdrain Y, et al. 2004. Identification of an spartylglucosaminidase-like protein in the venom of the parasitic wasp Asobara tabida (Hymenoptera: Braconidae). Insect Biochem. Mol. Biol. 34:485-92
64. Moreau SJM, Dingremont A, Doury G, Giordanengo P. 2002. Effects of parasitism by Asobara tabida (Hymenoptera: Braconidae) on the development, survival and activity of Drosophila melanogaster larvae. J. Insect Physiol. 48:337-47
65. Nakamatsu Y, Suzuki M, Harvey JA, Tanaka T. 2007. Regulation of the host nutritional milieu by ecto-and endoparasitoid venom. See Ref. 87a, pp. 37-56
66. Nakhasi HL, Pogue GP, Duncan RC, Joshi M, Atreya CD, et al. 1998. Implication of calreticulin function in parasite biology. Parasitol. Today 14:157-60
67. Nappi AJ, Christensen BM. 2005. Melanogenesis and associated cytotoxic reactions: applications to insect innate immunity. Insect Biochem. Mol. Biol. 35:443-59
68. Nappi AJ, Vass E. 1993. Melanogenesis and the generation of cytotoxic molecules during insect cellular immune reactions. Pigment Cell Res. 6:117-26
69. Parkinson N, Conyers C, Smith I. 2002. A venom protein from the endoparasitoid wasp Pimpla hypochon-driaca is similar to snake venom reprolysin-type metalloproteases. J. Invertebr. Pathol. 79:129-31
70. Parkinson N, Richards EH, Conyers C, Smith I, Edwards JP. 2002. Analysis of venom constituents from the parasitoid wasp Pimpla hypochondriaca and cloning of a cDNA encoding a venom protein. Insect Biochem. Mol. Biol. 32:729-35
71. Parkinson N, Smith I, Audsley N, Edwards JP. 2002. Purification of pimplin, a paralytic heterodimeric polypeptide from venom of the parasitoid wasp Pimpla hypochondriaca, and cloning of the cDNA encoding one of the subunits. Insect Biochem. Mol. Biol. 32:1769-73
72. Parkinson N, Smith I, Weaver R, Edwards JP. 2001. A new form of arthropod phenoloxidase is abundant in venom of the parasitoid wasp Pimpla hypochondriaca. Insect Biochem. Mol. Biol. 31:57-63
73. Parkinson NM, Conyers C, Keen J, MacNicoll A, Smith I, et al. 2004. Towards a comprehensive view of the primary structure of venom proteins from the parasitoid wasp Pimpla hypochondriaca. Insect Biochem. Mol. Biol. 34:565-71
74. Parkinson NM, Conyers C, Keen JN, MacNicoll AD, Weaver ISR. 2003. cDNAs encoding large venom proteins from the parasitoid wasp Pimpla hypochondriaca identified by random sequence analysis. Comp. Biochem. Physiol. C 134:513-20
75. Parkinson NM, Weaver RJ. 1999. Noxious components of venom from the pupa-specific para-sitoid Pimpla hypochondriaca. J. Invertebr. Pathol. 73:74-83
76. Pennacchio F, Strand MR. 2006. Evolution of developmental strategies in parasitic Hymenoptera. Annu. Rev. Entomol. 51:233-58
77. Pfister-Wilhelm R, Lanzrein B. 2009. Stage dependent influences of polydnaviruses and the parasitoid larvae on host ecdysteroids. J. Insect Physiol. 55:707-15
78. Price DRG,Bell HA, Hinchliffe G,Fitches E, Weaver R, Gatehouse JA. 2009. A venom metalloproteinase from the parasitic wasp Eulophus pennicornis is toxic towards its host, tomato moth (Lacanobia oleracae). Insect Mol. Biol. 18:195-202
79. Pruijssers AJ, Falabella P, Eum JH, Pennacchio F, Brown MR, Strand MR. 2009. Infection by a symbiotic polydnavirus induces wasting and inhibits metamorphosis of the moth Pseudoplusia includens. J. Exp. Biol. 212:2998-3006
80. Quicke DLJ. 1997. Parasitic Wasps. London: Chapman & Hall
81. Richards EH, Dani MP. 2007. Venom-induced apoptosis of insect hemocytes. See Ref. 87a, pp. 19-36
82. Richards EH, Dani MP. 2008. Biochemical isolation of an insect haemocyte anti-aggregation protein from the venom of the endoparasitic wasp, Pimpla hypochondriaca, and identification of its gene. J. Insect Physiol. 54:1041-19
83. Richards EH, Edwards JP. 2000. Parasitism of Lacanobia oleracea (Lepidoptera) by the ectoparasitoid, Eulophus pennicornis, is associated with a reduction in host haemolymph phenoloxidase activity. Comp. Biochem. Physiol. B 127:289-98
84. Richards EH, Parkinson NM. 2000. Venom from the endoparasitic wasp Pimpla hypochondriaca adversely affects the morphology, viability, and immune function of hemocytes from larvae of the tomato moth, Lacanobia oleracea. J. Invertebr. Pathol. 76:33-42
85. Rivers DB, Brogan A. 2008. Venom glands from the ectoparasitoid Nasonia vitripennis (Walker) (Hy-menoptera: Pteromalidae) produce a calreticulin-like protein that functions in developmental arrest and cell death in the flesh fly host, Sarcophaga bullata Parker (Diptera: Sarcophagidae). In Insect Physiology: New Research, ed. RP Maes, pp. 259-78. New York: Nova Sci.
86. +2-dependent cell death pathways. Arch. Insect Biochem. Physiol. 71:173-90
87. Rivers DB, Ruggiero L, Hayes M. 2002. 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). J. Insect Physiol. 48:1053-64
88. Rivers DB, Yoder JA, eds. 2007. Recent Advances in the Biochemistry, Toxicity, and Mode of Action of Parasitic Wasp Venoms. Kerala, India: Res. Signpost
89. Rizki RM, Rizki TM. 1990. Encapsulation of parasitoid eggs in phenoloxidase-deficient mutants of Drosophila melanogaster. J. Insect Physiol. 36:523-29
90. Rizki RM, Rizki TM. 1990. Parasitoid virus-like particles destroy Drosophila cellular immunity. Proc. Natl. Acad. Sci. USA 87:8388-92
91. Schmidt JO, Blum MS, Overall WL. 1986. Comparative enzymology of venoms from stinging hy-menoptera. Toxicon 24:907-21
92. Seals DF, Courtneidge SA. 2003. The ADAMs family of metalloproteases: multidomain proteins with multiple functions. Genes Dev. 17:7-30
93. Serrano SMT, Kim J, Wang DY, Dragulev B, Shannon JD, et al. 2006. The cysteine-rich domain of snake venom metalloproteinases is a ligand for von Willebrand factor A domains-Role in substrate targeting. J. Biol. Chem. 281:39746-56
94. Sotillos S, Roch F, Campuzano S. 1997. The metalloprotease-disintegrin Kuzbanian participates in Notch activation during growth and patterning of Drosophila imaginal discs. Development 124:4769-79
95. Stoltz DB, Guzo D, Belland ER, Lucarotti CJ, MacKinnon EA. 1988. Venom promotes uncoating in vitro and persistence in vivo of DNA from a braconid polydnavirus. J. Gen. Virol. 69:903-7
96. Suzuki M, Miura K, Tanaka T. 2008. The virus-like particles of a braconid endoparasitoid wasp, Meteorus pulchricornis, inhibit hemocyte spreading in its noctuid host, Pseudaletia separata. J. Insect Physiol. 54:1015-22
97. Suzuki M, Miura K, Tanaka T. 2009. Effects of the virus-like particles of a braconid endoparasitoid, Meteorus pulchricornis, on hemocytes and hematopoietic organs of its noctuid host, Pseudaletia separata. Appl. Entomol. Zool. 44:115-25
98. Suzuki M, Tanaka T. 2006. Virus-like particles in venom of Meteorus pulchricornis induce host hemocyte apoptosis. J. Insect Physiol. 52:602-13
99. Tanaka T. 1987. Effect of the venom of the endoparasitoid Apanteles kariyai Watanabe, on the cellular defence reaction of the host, Pseudaletia separata Walker. J. Insect Physiol. 33:413-20
100. Teramoto T, Tanaka T. 2004. Mechanism of reduction in the number of the circulating hemocytes in the Pseudaletia separata host parasitized by Cotesia kariyai. J. Insect Physiol. 50:1103-11
101. Thomas P, Yamada R, Johnson KN, Asgari S. 2010. Ectopic expression of an endoparasitic wasp venom protein in Drosophila melanogaster affects immune function, larval development and oviposition. Insect Mol. Biol. 19:473-80
102. Thompson SN. 1993. Redirection of host metabolism and effects on parasites nutrition. In Parasites and Pathogens of Insects, ed. NE Beckage, SN Thompson, BA Federici, pp. 125-44. San Diego: Academic
103. Uçkan F, Ergin E, Rivers DB, Gençer N. 2006. Age and diet influence the composition of venom from the endoparasitic wasp Pimpla turionellae L. (Hymenoptera: Ichneumonidae). Arch. Insect Biochem. Physiol. 63:177-87
104. UçkanF,SinanS,SavasciS,ErginE.2004. Determinationofvenom components from the endoparasitoid wasp Pimpla turionellae L. (Hymenoptera: Ichneumonidae). Ann. Entomol. Soc. Am. 97:775-80
105. Vinson SB. 1990. How parasitoids deal with the immune system of their host: an overview. Arch. Insect Biochem. Physiol. 13:3-27
106. Vinson SB, Iwantsch GF. 1980. Host regulation by insect parasitoids. Q. Rev. Biol. 55:143-65
107. Webb BA, Luckhart S. 1994. Evidence for an early immunosuppressive role for related Campoletis sonoren-sis venom and ovarian proteins in Heliothis virescens. Arch. Insect Biochem. Physiol. 26:147-63
108. Webb BA, Summers MD. 1990. Venom and viral expression products of the endoparasitic wasp Campoletis sonorensis share epitopes and related sequences. Proc. Natl. Acad. Sci. USA 87:4961-65
109. Wu M-L, Ye G-y, Zhu Jy, Chen X-X, Hu C. 2008. Isolation and characterization of an immunosup-pressive protein from venom of the pupa-specific endoparasitoid Pteromalus puparum. J. Invertebr. Pathol. 99:186-91
110. Yao L, Pike SE, Tosato G. 2002. Laminin binding to the calreticulin fragment vasostatin regulates endothelial cell function. J. Leukoc. Biol. 71:47-53
111. Ye G-Y, Zhu J, Zhang Z, Fang Q, Cai J, Hu C. 2007. Venom from the endoparasitoid Pteromalus puparum (Hymenoptera: Pteromalidae) adversely affects host hemocytes: differential toxicity and microstructural and ultrastructural changes in plasmatocytes and granular cells. See Ref. 87a, pp. 115-28
112. Zhang G, Lu Z-Q, Jiang H, Asgari S. 2004. Negative regulation of prophenoloxidase (proPO) activation by a clip-domain serine proteinase homolog (SPH) from endoparasitoid venom. Insect Biochem. Mol. Biol. 34:477-83
113. Zhang G, Schmidt O, Asgari S. 2004. A novel venom peptide from an endoparasitoid wasp is required for expression of polydnavirus genes in host hemocytes. J. Biol. Chem. 279:41580-85
114. Zhang G, Schmidt O, Asgari S. 2006. A calreticulin-like protein from endoparasitoid venom fluid is involved in host hemocyte inactivation. Dev. Comp. Immunol. 30:756-64
115. Zhang H, Forman HJ, Choi J. 2005. Gamma-glutamyl transpeptidase in glutathione biosynthesis. Methods Enzymol. 401:468-83
116. Zhu J-Y, Ye GY, Hu C. 2008. Molecular cloning and characterization of acid phosphatase in venom of the endoparasitoid wasp Pteromalus puparum (Hymenoptera: Pteromalidae). Toxicon 51:1391-99