A pathogenic parasite interferes with phagocytosis of insect immunocompetent cells

Developmental and Comparative Immunology

Volumn 34, Issue 9, 2010, Pages 991-998

  Brivio, Maurizio F ^a   Mastore, Maristella ^a   Nappi, Anthony J ^b  

^a UNIVERSITY OF INSUBRIA   (Italy)

^b LOYOLA UNIVERSITY CHICAGO   (United States)

Author keywords

Cuticle; HIPs; Immunosuppression; Insect; Nematode; PAMPs; Phagocytosis; PRRs

Indexed keywords

ARTICLE; BACILLUS SUBTILIS; BINDING AFFINITY; BLOOD CELL; CELL ENCAPSULATION; CONTROLLED STUDY; ESCHERICHIA COLI; HEMOLYMPH; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOSURVEILLANCE; LEPIDOPTERA; NEMATODE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN BINDING; STEINERNEMA FELTIA;

GALLERIA MELLONELLA; HEXAPODA; LEPIDOPTERA; NEMATODA; STEINERNEMA FELTIAE; XENORHABDUS NEMATOPHILA;

EID: 77954083148     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2010.05.002     Document Type: Article

References (59)

1. Abu-Shakra M., Buskila D., Shoenfeld Y. Molecular mimicry between host and pathogen: examples from parasites and implication. Immunol. Lett. 1999, 67:147-152.
2. Adamo S.A., Roberts J.L., Easy R.H., Ross N.W. Competition between immune function and lipid transport for the protein apolipophorin III leads to stress-induced immunosuppression in crickets. J. Exp. Biol. 2008, 211:531-538.
3. Akhurst R.J., Dunphy G.B. Tripartite interactions between symbiotically associated entomopathogenic bacteria, nematodes, and their insect hosts. Parasites and Pathogens of Insects 1993, vol. 2:1-23. Academic Press, New York.
4. Altincicek B., Linder M., Linder D., Preissner K.T., Vilcinskas A. Microbial metalloproteinases mediate sensing of invading pathogens and activate innate immune responses in the lepidopteran model host Galleria mellonella. Infect. Immun. 2007, 75:175-183.
5. Axén A., Carlsson A., Engström Å., Bennich H. Gloverin, an antibacterial protein from the immune hemolymph of Hyalophora pupae. Eur. J. Biochem. 1997, 247:614-619.
6. Blaxter M.L., Page A.P., Rudin W., Maizels R.M. Nematode surface coats: actively evading immunity. Parasitol. Today 1992, 8(7):243-247.
7. Brivio M.F., Pagani M., Restelli S. Immune suppression of Galleria mellonella (Insecta, Lepidoptera) humoral defenses induced by Steinernema feltiae (Nematoda, Rhabditida): involvement of the parasite cuticle. Exp. Parasitol. 2002, 101:149-156.
8. Brivio M.F., Mastore M., Moro M. Role of Steinernema feltiae body-surface lipids in host-parasite immunological interactions. Mol. Biochem. Parasitol. 2004, 135:111-121.
9. Brivio M.F., Mastore M., Pagani M. Parasite-host relationship: a lesson from a professional killer. Inv. Surv. J. 2005, 2:41-53.
10. Brivio M.F., Moro M., Mastore M. Down-regulation of antibacterial peptides synthesis in an insect model induced by the body-surface of an entomoparasite (Steinernema feltiae). Dev. Comp. Immunol. 2006, 30:627-638.
11. Cerenius L., Lee B.L., Soderhall K. The proPO system: pros and cons for its role in invertebrate immunity. Trends Immunol. 2008, 29(6):264-270.
12. Chaput C., Boneca I.G. Peptidoglycan detection by mammals and flies. Microb. Infect. 2007, 9:637-647.
13. Dunphy G., Halwani A. Haemolymph proteins of larvae of Galleria mellonella detoxify endotoxins of the insect pathogenic bacteria Xenorhabdus nematophilus (Enterobacteriaceae). J. Insect Physiol. 1997, 43:1023-1029.
14. Dziarski R. Peptidoglycan recognition proteins (PGRPs). Mol. Immunol. 2004, 40:877-886.
15. Franc N.C., Heitzler P., Ezekowitz R.A., White K. Requirement for croquemort in phagocytosis of apoptotic cells in Drosophila. Science 1999, 284:1991-1994.
16. Freitak D., Wheat C.W., Heckel D.G., Vogel H. Immune system responses and fitness costs associated with consumption of bacteria in larvae of Trichoplusia ni. BMC Biol. 2007, 5(56):1-13.
17. Gillespie J.P., Kanost M.R., Trenczek T. Biological mediators of insect immunity. Annu. Rev. Entomol. 1997, 42:611-643.
18. Götz P., Matha V., Vilcinskas A. Effects of the entomopathogenic fungus Metarhizium anisopliae and its secondary metabolites on morphology and cytoskeleton of plasmatocytes isolated from the greater wax moth, Galleria mellonella. J. Insect Physiol. 1997, 43:1149-1159.
19. Halwani A.E., Dunphy G.B. Apolipophorin-III in Galleria mellonella potentiates hemolymph lytic activity. Dev. Comp. Immunol. 1999, 23:563-570.
20. Halwani A.E., Niven D.F., Dunphy G.B. Apolipophorin-III in the greater wax moth, Galleria mellonella (Lepidoptera: Pyralidae). Arch. Insect Biochem. Physiol. 2001, 48:135-143.
21. Hoffmann J.A., Reichhart J.M. Drosophila innate immunity: an evolutionary perspective. Nat. Immunol. 2002, 3(2):121-126.
22. Johnston L.A., Yoshino T.P. Analysis of lectin and snail plasma-binding glycopeptides associated with the tegumental surface of the primary sporocysts of Schistosoma mansoni. Parasitology 1996, 112:469-479.
23. Kanost M.R., Nardi J.B. Innate immune responses of Manduca sexta. Molecular Biology and Genetics of Lepidoptera 2009, 271-291. CRC Press, New York. M.R. Goldsmith, F. Marec (Eds.).
24. Kathirithamby J., Ross L.D., Johnston J.S. Masquerading as self? Endoparasitic Strepsiptera (Insecta) enclose themselves in host-derived epidermal bag. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:7655-7659.
25. Kaya H.K., Gaugler R. Entomopathogenic nematodes. Ann. Rev. Entomol. 1993, 38:181-206.
26. Koizumi N., Morozumi A., Imamura M., Tanaka E., Iwahana H., Sato R. Lipopolysaccharide-binding proteins and their involvement in the bacterial clearance from the hemolymph of the silkworm Bombyx mori. Eur. J. Biochem. 1997, 248:217-224.
27. Kurucz É., Márkus R., Zsámboki J., Folkl-Medzihradszky K., Darula Z., Vilmos P., Udvardy A., Krausz I., Lukacsovich T., Gateff E., Zettervall C.J., Hultmark D., Andó I. Nimrod, a putative phagocytosis receptor with EGF repeats in Drosophila plasmatocytes. Curr. Biol. 2007, 17:649-654.
28. Lemaitre B., Hoffmann J. The host defense of Drosophila melanogaster. Ann. Rev. Immunol. 2007, 25:697-743.
29. Levashina E.A., Moita L.F., Blandin S., Vriend G., Lagueux M., Kafatos F.C. Conserved role of a complement-like protein in phagocytosis revealed by dsRNA knockout in cultured cells of the mosquito, Anopheles gambiae. Cell 2001, 104(5):709-718.
30. Little T.J., Hultmark D., Read A.F. Invertebrate immunity and the limits of mechanistic immunology. Nat. Immunol. 2005, 6:651-654.
31. Loker E.S. On being a parasite in an invertebrate host: a short survival course. J. Parasitol. 1994, 80:728-747.
32. Maizels R.M., Blaxter M., Selkirk M.E. Forms and functions of nematode surfaces. Exp. Parasitol. 1993, 77:380-384.
33. Mastore M., Brivio M.F. Cuticular surface lipids are responsible for disguise properties of an entomoparasite against host cellular responses. Dev. Comp. Immunol. 2008, 32:1050-1062.
34. Nappi J., Vass E. Cytotoxic reactions associated with insect immunity: Signalling pathways and killing molecules. Phylogenetic Perspectives on the Vertebrate Immune System 2000, 329-348. Kluwer Academic/Plenum Publishers, New York. G. Beck, M. Sugumaran, E. Cooper (Eds.).
35. Nappi A.J., Kohler L., Mastore M. Signalling pathways implicated in the cellular innate immune responses of Drosophila. Inv. Surv. J. 2004, 1:5-33.
36. Niere M., Meisslitzer C., Dettloff M., Weise C., Ziegler M., Wiesner A. Insect immune activation by recombinant Galleria mellonella apolipophorin III. Biochem. Biophys. Acta 1999, 1433:16-26.
37. Park S.Y., Kim C.H., Jeong W.H., Lee J.H., Seo S.J., Han Y.S., Le I.H. Effects of two hemolymph proteins on humoral defense reactions in the wax moth, Galleria mellonella. Dev. Comp. Immunol. 2005, 29:43-51.
38. Politz S.M., Philipp M. Caenorhabditis elegans as a model for parasitic nematodes: a focus on the cuticle. Parasitol. Today 1992, 8:6-12.
39. Proudfoot L., Kusel J.R., Smith H.V., Kennedy M.W. Rapid changes in the surface of parasitic nematodes during transition from pre- to post-parasitic forms. Parasitology 1993, 107:107-117.
40. Ramet M., Lanot R., Zachary D., Manfruelli P. JNK signalling pathway is required for efficient wound healing in Drosophila. Dev. Biol. 2002, 241:145-156.
41. Ratner S., Vinson S.B. Encapsulation reactions in vitro by haemocytes of Heliothis virescens. J. Insect Physiol. 1983, 11:855-863.
42. Ribeiro C., Duvic B., Oliveira P., Givaudan A., Palha F., Simoes N., Brehelin M. Insect immunity: effects of factors produced by a nematobacterial complex on immunocompetent cells. J. Insect Physiol. 1999, 45:677-685.
43. Roh K.B., Kim C.H., Lee H., Kwon H.M., Park J.W., Ryu J.H., Kurokawa K., Ha N.C., Lee W.J., Lemaitre B., Söderhäll K., Lee B.L. Proteolytic cascade for the activation of the insect toll pathway induced by the fungal cell wall component. J. Biol. Chem. 2009, 284(29):19474-19481.
44. Song K.H., Jung S.J., Seo Y.R., Kang S.W., Han S.S. Identification of up-regulated proteins in the hemolymph of immunized Bombyx mori larvae. Comp. Biochem. Phys. D 2006, 1:260-266.
45. Strand M.R. The insect cellular immune response. Insect Sci. 2008, 15(1):1-14.
46. Strand M.R., Pech L.L. Immunological basis for compatibility in parasitoid-host relationship. Annu. Rev. Entomol. 1995, 40:31-56.
47. Stroschein-Stevenson S.L., Foley E., O'Farrell P.H., Johnson A.D. Identification of Drosophila gene products required for phagocytosis of Candida albicans. PLoS Biol. 2006, 4:pe4.
48. Stuart L.M., Ezekowitz R.A. Phagocytosis and comparative innate immunity: learning on the fly. Nat. Rev. Immunol. 2008, 8:131-141.
49. Takehana A., Yano T., Mita S., Kotani A., Oshima Y., Kurata S. Peptidoglycan recognition protein (PGRP)-LE and PGRP-LC act synergistically in Drosophila immunity. EMBO J. 2004, 23:4690-4700.
50. Tojo S., Naganuma F., Arakawa K., Yokoo S. Involvement of both granular cells and plasmatocytes in phagocytic reactions in the greater wax moth, Galleria mellonella. J. Insect Physiol. 2000, 46:1129-1135.
51. Van Sambeek J., Wiesner A. Successful parasitation of locusts by entomopathogenic nematodes is correlated with inhibition of insect phagocytes. J. Invertebr. Pathol. 1999, 73:154-161.
52. Vilcinskas A., Matha V., Götz P. Inhibition of phagocytic activity of plasmatocytes isolated from Galleria mellonella by entomogenous fungi and their secondary metabolites. J. Insect Physiol. 1997, 43:475-483.
53. Vinson S.D. Insect host responses against parasitoids and the parasitoid's resistance with emphasis on the lepidoptera-hymenoptera association. Comp. Pathobiol. 1977, 3:103-125.
54. Wang Y., Gaugler R. Steinernema glaseri surface coat protein suppresses the immune response of Popillia japonica (Coleoptera: Scarabaeidae) larvae. Biol. Control. 1999, 14:45-50.
55. Watson F.L., Püttmann-Holgado R., Thomas F., Lamar D.L., Hughes M., Kondo M., Rebel V.I., Schmucker D. Extensive diversity of Ig superfamily proteins in the immune system of insects. Science 2005, 309:1874-1878.
56. Weber K., Osborn M. The reliability of molecular weight determinations by dodecyl sulfate polyacrylamide gel electrophoresis. J. Biol. Chem. 1969, 244(16):4406-4412.
57. Werner T., Borge-Renberg K., Mellroth P., Steiner H., Hultmark D. Functional diversity of the Drosophila PGRP-LC gene cluster in the response to lipopolysaccharide and peptidoglycan. J. Biol. Chem. 2003, 278:26319-26322.
58. Weston D.S., Kemp W.M. Schistosoma mansoni - comparison of cloned tropomyosin antigens shared between adult parasites and Biomphalaria glabrata. Exp. Parasitol. 1993, 76:358-370.
59. Yoshino T.P., Boyle J.P., Humphries J.E. Receptor-ligand interactions and cellular signalling at the host-parasite interface. Parasitology 2001, 123:143-157.