The immunogenic properties of protozoan glycosylphosphatidylinositols in the mosquito Anopheles gambiae

Developmental and Comparative Immunology

Volumn 33, Issue 2, 2009, Pages 216-223

  Arrighi, Romanico B G ^a,d,e   Debierre Grockiego, Françoise ^b   Schwarz, Ralph T ^b,c   Faye, Ingrid ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c CNRS   (France)

^d Tumor and Cell Biology   (Sweden)

^e SWEDISH INSTITUTE FOR INFECTIOUS DISEASE CONTROL   (Sweden)

Author keywords

Anopheles gambiae; Antimicrobial peptide; Fitness cost; Glycosylphosphatidylinositol; Innate immune response; Laminarin; Lipopolysaccharide; Pathogen associated molecular pattern; Plasmodium falciparum; Toxoplasma gondii

Indexed keywords

GLYCOSYLPHOSPHATIDYLINOSITOL; PARASITE ANTIGEN;

ANIMAL EXPERIMENT; ANOPHELES GAMBIAE; ANTIGENICITY; ARTICLE; CONTROLLED STUDY; FEMALE; IMMUNE RESPONSE; IMMUNOGENICITY; INNATE IMMUNITY; NONHUMAN; PARASITE TRANSMISSION; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTOZOON; TOXOPLASMA GONDII;

ANOPHELES GAMBIAE; FUNGI; PLASMODIUM FALCIPARUM; PROTOZOA; TOXOPLASMA GONDII;

EID: 54849420045     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2008.08.009     Document Type: Article

References (52)

1. Brennan C.A., and Anderson K.V. Drosophila: the genetics of innate immune recognition and response. Annu Rev Immunol 22 (2004) 457-483
2. Christophides G.K., Vlachou D., and Kafatos F.C. Comparative and functional genomics of the innate immune system in the malaria vector Anopheles gambiae. Immunol Rev 198 (2004) 127-148
3. Osta M.A., Christophides G.K., Vlachou D., and Kafatos F.C. Innate immunity in the malaria vector Anopheles gambiae: comparative and functional genomics. J Exp Biol 207 (2004) 2551-2263
4. Whitten M.M., Shiao S.H., and Levashina E.A. Mosquito midguts and malaria: cell biology, compartmentalization and immunology. Parasite Immunol 28 (2006) 121-130
5. Ikezawa H. Glycosylphosphatidylinositol (GPI)-anchored proteins. Biol Pharm Bull 25 (2002) 409-417
6. McConville M.J., and Ferguson M.A. The structure, biosynthesis and function of glycosylated phosphatidylinositols in the parasitic protozoa and higher eukaryotes. Biochem J 294 (1993) 305-324
7. Gerold P., Dieckmann-Schuppert A., and Schwarz R.T. Glycosylphosphatidylinositols synthesized by asexual erythrocytic stages of the malarial parasite, Plasmodium falciparum. Candidates for plasmodial glycosylphosphatidylinositol membrane anchor precursors and pathogenicity factors. J Biol Chem 269 (1994) 2597-2606
8. Gowda D.C., and Davidson E.A. Protein glycosylation in the malaria parasite. Parasitol Today 15 (1999) 147-152
9. Nebl T., De Veer M.J., and Schofield L. Stimulation of innate immune responses by malarial glycosylphosphatidylinositol via pattern recognition receptors. Parasitology 130 (2005) S45-S62
10. Tachado S., Gerold P., Schwarz R., Novakovic S., McConville M., and Schofield L. Signal transduction in macrophages by glycosylphosphatidylinositols of Plasmodium, Trypanosoma, and Leishmania: activation of protein tyrosine kinases and protein kinase C by inositolglycan and diacylglycerol moieties. Proc Natl Acad Sci USA 94 (1997) 4022-4027
11. Carney C.K., Schrimpe A.C., Halfpenny K., Harry R.S., Miller C.M., Broncel M., et al. The basis of the immunomodulatory activity of malaria pigment (hemozoin). J Biol Inorg Chem 11 (2006) 917-929
12. Parroche P., Lauw F.N., Goutagny N., Latz E., Monks B.G., Visintin A., et al. Malaria hemozoin is immunologically inert but radically enhances innate responses by presenting malaria DNA to toll-like receptor 9. Proc Natl Acad Sci USA 104 (2007) 1919-1924
13. Baton L.A., and Ranford-Cartwright L.C. Do malaria ookinete surface proteins P25 and P28 mediate parasite entry into mosquito midgut epithelial cells?. Malar J 4 (2005) 15
14. Blanco A.R., Paez A., Gerold P., Dearsly A.L., Margos G., Schwarz R.T., et al. The biosynthesis and post-translational modification of Pbs21 an ookinete-surface protein of Plasmodium berghei. Mol Biochem Parasitol 98 (1999) 163-173
15. del Carmen Rodriguez M., Gerold P., Dessens J., Kurtenbach K., Schwartz R.T., Sinden R.E., et al. Characterisation and expression of pbs25, a sexual and sporogonic stage specific protein of Plasmodium berghei. Mol Biochem Parasitol 110 (2000) 147-159
16. Wang Q., Fujioka H., and Nussenzweig V. Mutational analysis of the GPI-anchor addition sequence from the circumsporozoite protein of Plasmodium. Cell Microbiol 7 (2005) 1616-1626
17. Dana A.N., Hillenmeyer M.E., Lobo N.F., Kern M.K., Romans P.A., and Collins F.H. Differential gene expression in abdomens of the malaria vector mosquito, Anopheles gambiae, after sugar feeding, blood feeding and Plasmodium berghei infection. BMC Genom. 7 (2006) 119
18. Lim J., Gowda D.C., Krishnegowda G., and Luckhart S. Induction of nitric oxide synthase in Anopheles stephensi by Plasmodium falciparum: mechanism of signaling and the role of parasite glycosylphosphatidylinositols. Infect Immun 73 (2005) 2778-2789
19. Akman-Anderson L., Olivier M., and Luckhart S. Induction of nitric oxide synthase and activation of signaling proteins in Anopheles mosquitoes by the malaria pigment, hemozoin. Infect Immun 75 (2007) 4012-4019
20. Gray E.M., and Bradley T.J. Malarial infection in Aedes aegypti: effects on feeding, fecundity and metabolic rate. Parasitology 132 (2006) 169-176
21. Hogg J.C., and Hurd H. Malaria-induced reduction of fecundity during the first gonotrophic cycle of Anopheles stephensi mosquitoes. Med Vet Entomol 9 (1995) 176-180
22. Hogg J.C., and Hurd H. The effects of natural Plasmodium falciparum infection on the fecundity and mortality of Anopheles gambiae s. l. in north east Tanzania. Parasitology 114 (1997) 325-331
23. Debierre-Grockiego F., Azzouz N., Schmidt J., Dubremetz J.F., Geyer H., Geyer R., et al. Roles of glycosylphosphatidylinositols of Toxoplasma gondii. Induction of tumor necrosis factor-alpha production in macrophages. J Biol Chem 278 (2003) 32987-32993
24. Debierre-Grockiego F., Schofield L., Azzouz N., Schmidt J., Santos de Macedo C., Ferguson M.A., et al. Fatty acids from Plasmodium falciparum down-regulate the toxic activity of malaria glycosylphosphatidylinositols. Infect Immun 74 (2006) 5487-5496
25. Luna C., Wang X., Huang Y., Zhang J., and Zheng L. Characterization of four toll related genes during development and immune responses in Anopheles gambiae. Insect Biochem Mol Biol 32 (2002) 1171-1179
26. Barillas-Mury C., Han Y.S., Seeley D., and Kafatos F.C. Anopheles gambiae Ag-STAT, a new insect member of the STAT family, is activated in response to bacterial infection. EMBO J 18 (1999) 959-967
27. Meister S., Kanzok S.M., Zheng X.L., Luna C., Li T.R., Hoa N.T., et al. Immune signaling pathways regulating bacterial and malaria parasite infection of the mosquito Anopheles gambiae. Proc Natl Acad Sci USA 102 (2005) 11420-11425
28. Vizioli J., Richman A.M., Uttenweiler-Joseph S., Blass C., and Bulet P. The defensin peptide of the malaria vector mosquito Anopheles gambiae: antimicrobial activities and expression in adult mosquitoes. Insect Biochem Mol Biol 31 (2001) 241-248
29. Vizioli J., Bulet P., Charlet M., Lowenberger C., Blass C., Muller H.M., et al. Cloning and analysis of a cecropin gene from the malaria vector mosquito, Anopheles gambiae. Insect Mol Biol 9 (2000) 75-84
30. Vizioli J., Bulet P., Hoffmann J.A., Kafatos F.C., Muller H.M., and Dimopoulos G. Gambicin: a novel immune responsive antimicrobial peptide from the malaria vector Anopheles gambiae. Proc Natl Acad Sci USA 98 (2001) 12630-12635
31. Li B., Calvo E., Marinotti O., James A.A., and Paskewitz S.M. Characterization of the c-type lysozyme gene family in Anopheles gambiae. Gene 360 (2005) 131-139
32. Riehle M.M., Markianos K., Niare O., Xu J., Li J., Toure A.M., et al. Natural malaria infection in Anopheles gambiae is regulated by a single genomic control region. Science 312 (2006) 577-579
33. Briegel H. Determination of uric acid and haematin in a single sample of excreta from blood-fed insects. Experientia 36 (1980) 1428
34. Clements A.N. Oogenesis. In: Clements A.N. (Ed). The biology of mosquitoes vol 1 (1992), Chapman and Hall, London 340-359
35. Alvarez J.I. Inhibition of toll like receptor immune responses by microbial pathogens. Front Biosci 10 (2005) 582-587
36. Blandin S., Moita L.F., Köcher T., Wilm M., Kafatos F.C., and Levashina E.A. Reverse genetics in the mosquito Anopheles gambiae: targeted disruption of the defensin gene. EMBO Rep 3 (2002) 852-856
37. Roxström-Lindquist K., Terenius O., and Faye I. Parasite-specific immune response in adult Drosophila melanogaster: a genomic study. EMBO J 5 (2004) 207-212
38. Dimopoulos G., Richman A., Muller H.M., and Kafatos F.C. Molecular immune responses of the mosquito Anopheles gambiae to bacteria and malaria parasites. Proc Natl Acad Sci USA 94 (1997) 11508-11513
39. Dimopoulos G., Christophides G.K., Meister S., Schultz J., White K.P., Barillas-Mury C., et al. Genome expression analysis of Anopheles gambiae: responses to injury, bacterial challenge, and malaria infection. Proc Natl Acad Sci USA 99 (2002) 8814-8819
40. Oduol F., Xu J., Niare O., Natarajan R., and Vernick K.D. Genes identified by an expression screen of the vector mosquito Anopheles gambiae display differential molecular immune response to malaria parasites and bacteria. Proc Natl Acad Sci USA 97 (2000) 11397-11402
41. Dong Y., Aguilar R., Xi Z., Warr E., Mongin E., and Dimopoulos G. Anopheles gambiae immune responses to human and rodent Plasmodium parasite species. PLoS Pathog 2 (2006) e52
42. Schnider D.S. How and why does a fly turn its immune system off?. PLoS Biol 5 (2007) e247
43. Debierre-Grockiego F., Campos M.A., Azzouz N., Schmidt J., Bieker U., Garcia Resende M., et al. Activation of TLR2 and TLR4 by glycosphosphatidylinositols derived from Toxoplasma gondii. J Immunol 179 (2007) 1129-1137
44. Krishnegowda G., Hajjar A.M., Zhu J., Douglass E.J., Uematsu S., Akira S., et al. Induction of proinflammatory responses in macrophages by the glycosphosphaditylinositol (GPI) structure requirement, and regulation of GPI activity. J Biol Chem 280 (2005) 8606-8616
45. Busse M.S., Arnold C.P., Towb P., Katrivesis J., and Wasserman S.A. A κB sequence code for pathway-specific innate immune responses. EMBO J 26 (2007) 3826-3835
46. Ahmed A.M., Maingon R., Romans P., and Hurd H. Effects of malaria infection on vitellogenesis in Anopheles gambiae during two gonotrophic cycles. Insect Mol Biol 10 (2001) 347-356
47. Hopwood J.A., Ahmed A.M., Polwart A., Williams G.T., and Hurd H. Malaria-induced apoptosis in mosquito ovaries: a mechanism to control vector egg production. J Exp Biol 204 (2001) 2773-2780
48. Ahmed A.M., and Hurd H. Immune stimulation and malaria infection impose reproductive costs in Anopheles gambiae via follicular apoptosis. Microbes Infect 8 (2006) 308-315
49. Ferguson H.M., Rivero A., and Read A.F. The influence of malaria parasite genetic diversity and anaemia on mosquito feeding and fecundity. Parasitology 127 (2003) 9-19
50. Hurd H., Taylor P.J., Adams D., Underhill A., and Eggleston P. Evaluating the costs of mosquito resistance to malaria parasites. Evolution Int J Org Evolution 59 (2005) 2560-2572
51. Scholte E.-J., Knols B.G.J., and Takken W. Infection of the malaria mosquito Anopheles gambiae with the entomopathogenic fungus Metarhizium anisopliae reduces blood feeding and fecundity. J Invert Pathol 91 (2006) 43-49
52. Hurd H. Manipulation of medically important insect vectors by their parasites. Annu Rev Entomol 48 (2003) 141-161