Subversion of complement by hematophagous parasites

Developmental and Comparative Immunology

Volumn 33, Issue 1, 2009, Pages 5-13

  Schroeder, Hélène ^a   Skelly, Patrick J ^b   Zipfel, Peter F ^c,d   Losson, Bertrand ^a   Vanderplasschen, Alain ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b TUFTS UNIVERSITY   (United States)

^c HANS KNÖLL INSTITUTE   (Germany)

^d FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

Complement system; Darwinian evolution; Hematophagous parasites; Immune evasion

Indexed keywords

CALRETICULIN; CD59 ANTIGEN; COMPLEMENT COMPONENT C1Q; COMPLEMENT COMPONENT C2; COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT C5; COMPLEMENT INHIBITOR; PARAMYOSIN; PROPERDIN;

ADAPTIVE IMMUNITY; COMPLEMENT INHIBITION; COMPLEMENT SYSTEM; HOST PARASITE INTERACTION; HUMAN; INNATE IMMUNITY; NONHUMAN; PARASITE SURVIVAL; PARASITE VIRULENCE; PRIORITY JOURNAL; PROTEIN BINDING; REVIEW; SCHISTOSOMA; TICK;

METAZOA;

ANIMALS; CALRETICULIN; COMPLEMENT ACTIVATION; COMPLEMENT SYSTEM PROTEINS; HOST-PARASITE INTERACTIONS; IMMUNITY, INNATE; PARASITES; SCHISTOSOMA; TICKS;

EID: 54049088084     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2008.07.010     Document Type: Review

References (77)

1. Nonaka M., and Yoshizaki F. Evolution of the complement system. Mol Immunol 40 12 (2004) 897-902
2. Rother K., Till G.O., and Hänsch G.M. The complement system (1998), Springer, Berlin
3. Houle J., and Hoffmann E. Evidence for restriction of the ability of complement to lyse homologous erythrocytes. J Immunol 133 3 (1984) 1444-1452
4. Yamamoto H., Blaas P., Nicholson-Weller A., and Hansch G.M. Homologous species restriction of the complement-mediated killing of nucleated cells. Immunology 70 4 (1990) 422-426
5. Meri S., and Jarva H. Complement regulation. Vox Sang 74 Suppl. 2 (1998) 291-302
6. Rodriguez de Cordoba S., Lublin D., Rubinstein P., and Atkinson J. Human genes for three complement components that regulate the activation of C3 are tightly linked. J Exp Med 161 5 (1985) 1189-1195
7. Krushkal J., Bat O., and Gigli I. Evolutionary relationships among proteins encoded by the regulator of complement activation gene cluster. Mol Biol Evol 17 11 (2000) 1718-1730
8. Perkins S.J., Gilbert H.E., Aslam M., Hannan J., Holers V.M., and Goodship T.H. Solution structures of complement components by X-ray and neutron scattering and analytical ultracentrifugation. Biochem Soc Trans 30 Pt 6 (2002) 996-1001
9. Cooper N.R. Complement evasion strategies of microorganisms. Immunol Today 12 9 (1991) 327-331
10. Blom A.M. Strategies developed by bacteria and virus for protection from the human complement system. Scand J Clin Lab Invest 64 5 (2004) 479-496
11. Thern A., Stenberg L., Dahlback B., and Lindahl G. Ig-binding surface proteins of Streptococcus pyogenes also bind human C4b-binding protein (C4BP), a regulatory component of the complement system. J Immunol 154 1 (1995) 375-386
12. Vanderplasschen A., Mathew E., Hollinshead M., Sim R.B., and Smith G.L. Extracellular enveloped vaccinia virus is resistant to complement because of incorporation of host complement control proteins into its envelope. Proc Natl Acad Sci USA 95 13 (1998) 7544-7549
13. Hellwage J., Meri T., Heikkila T., Alitalo A., Panelius J., Lahdenne P., et al. The complement regulator factor H binds to the surface protein OspE of Borrelia burgdorferi. J Biol Chem 276 11 (2001) 8427-8435
14. Kraiczy P., Skerka C., Kirschfink M., Brade V., and Zipfel P.F. Immune evasion of Borrelia burgdorferi by acquisition of human complement regulators FHL-1/reconectin and factor H. Eur J Immunol 31 6 (2001) 1674-1684
15. Kotwal G.J., and Moss B. Vaccinia virus encodes a secretory polypeptide structurally related to complement control proteins. Nature 335 6186 (1988) 176-178
16. Bernet J., Mullick J., Singh A.K., and Sahu A. Viral mimicry of the complement system. J Biosci 28 3 (2003) 249-264
17. Favoreel H.W., Van de Walle G.R., Nauwynck H.J., and Pensaert M.B. Virus complement evasion strategies. J Gen Virol 84 1 (2003) 1-15
18. Inal J.M. Parasite interaction with host complement: beyond attack regulation. Trends Parasitol 20 9 (2004) 407-412
19. Finlay B.B., and McFadden G. Anti-immunology: evasion of the host immune system by bacterial and viral pathogens. Cell 124 4 (2006) 767-782
20. Kraiczy P., and Wurzner R. Complement escape of human pathogenic bacteria by acquisition of complement regulators. Mol Immunol 43 1-2 (2006) 31-44
21. Rooijakkers S.H.M., and van Strijp J.A.G. Bacterial complement evasion. Molecular immunology. XXI international complement workshop Beijing. China, October 22-26, 44 (1-3), 2006 (2007) 23-32
22. Zipfel P.F., Wurzner R., and Skerka C. Complement evasion of pathogens: common strategies are shared by diverse organisms. Mol Immunol 44 16 (2007) 3850-3857
23. Samuelson J.C., and Caulfield J.P. Cercarial glycocalyx of Schistosoma mansoni activates human complement. Infect Immun 51 1 (1986) 181-186
24. Skelly P.J., and Wilson A.R. Making sense of the schistosome surface. In: Baker J.R., Muller R., and Rollinson D. (Eds). Advances in parasitology (2006), Academic Press, UK 185-284
25. Dessein A., Samuelson J.C., Butterworth A.E., Hogan M., Sherry B.A., Vadas M.A., et al. Immune evasion by Schistosoma mansoni: loss of susceptibility to antibody or complement-dependent eosinophil attack by schistosomula cultured in medium free of macromolecules. Parasitology 82 Pt 3 (1981) 357-374
26. Keating J.H., Wilson R.A., and Skelly P.J. No overt cellular inflammation around intravascular schistosomes in vivo. J Parasitol 92 6 (2006) 1365-1369
27. Vignali D.A., Bickle Q.D., Taylor M.G., Tennent G., and Pepys M.B. Comparison of the role of complement in immunity to Schistosoma mansoni in rats and mice. Immunology 63 1 (1988) 55-61
28. Skelly P.J. Intravascular schistosomes and complement. Trends Parasitol 20 8 (2004) 370-374
29. Inal J. Complement C2 receptor inhibitor trispanning: from man to schistosome. Springer Semin Immunopathol 27 4 (2006) 509-510
30. Deng J., Gold D., LoVerde P.T., and Fishelson Z. Mapping of the complement C9 binding domain in paramyosin of the blood fluke Schistosoma mansoni. Int J Parasitol 37 1 (2007) 67-75
31. Silva E.E., Clarke M.W., and Podesta R.B. Characterization of a C3 receptor on the envelope of Schistosoma mansoni. J Immunol 151 12 (1993) 7057-7066
32. Braschi S., and Wilson R.A. Proteins Exposed at the adult schistosome surface revealed by biotinylation. Mol Cell Proteomics 5 2 (2006) 347-356
33. Loukas A., Jones M.K., King L.T., Brindley P.J., and McManus D.P. Receptor for Fc on the surfaces of schistosomes. Infect Immun 69 6 (2001) 3646-3651
34. Pearce E.J., Hall B.F., and Sher A. Host-specific evasion of the alternative complement pathway by schistosomes correlates with the presence of a phospholipase C-sensitive surface molecule resembling human decay-accelerating factor. J Immunol 144 7 (1990) 2751-2756
35. La Flamme A.C., MacDonald A.S., Huxtable C.R., Carroll M., and Pearce E.J. Lack of C3 affects Th2 response development and the sequelae of chemotherapy in schistosomiasis. J Immunol 170 1 (2003) 470-476
36. Ruppel A., Rother U., and Diesfeld H.J. Schistosoma mansoni: development of primary infections in mice genetically deficient or intact in the fifth component of complement. Parasitology 85 2 (1982) 315-323
37. Ribeiro J.M., Makoul G.T., Levine J., Robinson D.R., and Spielman A. Antihemostatic, antiinflammatory, and immunosuppressive properties of the saliva of a tick, Ixodes dammini. J Exp Med 161 2 (1985) 332-344
38. Ribeiro J.M., and Spielman A. Ixodes dammini: salivary anaphylatoxin inactivating activity. Exp Parasitol 62 2 (1986) 292-297
39. Ribeiro J.M. Ixodes dammini: salivary anti-complement activity. Exp Parasitol 64 3 (1987) 347-353
40. Wikel S.K., and Allen J.R. Acquired resistance to ticks. III. Cobra venom factor and the resistance response. Immunology 32 4 (1977) 457-465
41. Wikel S.K. Acquired resistance to ticks: expression of resistance by C4-deficient guinea pigs. Am J Trop Med Hyg 28 3 (1979) 586-590
42. Papatheodorou V., and Brossard M. C3 levels in the sera of rabbits infested and reinfested with Ixodes ricinus L. and in midguts of fed ticks. Exp Appl Acarol 3 1 (1987) 53-59
43. Nunn M.A., Sharma A., Paesen G.C., Adamson S., Lissina O., Willis A.C., et al. Complement inhibitor of C5 activation from the soft tick Ornithodoros moubata. J Immunol 174 4 (2005) 2084-2091
44. Keirans J.E., Needham G.R., and Oliver J.H.J. The Ixodes (Ixodes) ricinus complex worldwide: diagnosis of the species in the complex, hosts and distribution. In: Needham G.R., Michell R., Horn D.J., and Welborn W.C. (Eds). Symposium proceedings IX international congress of acarology. Ohio Biological Survey, Colombus, OH (1999) 341-347
45. Xu G., Fang Q.Q., Keirans J.E., and Durden L.A. Molecular phylogenetic analyses indicate that the Ixodes ricinus complex is a paraphyletic group. J Parasitol 89 3 (2003) 452-457
46. Lawrie C.H., Randolph S.E., and Nuttall P.A. Ixodes ticks: serum species sensitivity of anticomplement activity. Exp Parasitol 93 4 (1999) 207-214
47. Valenzuela J.G., Charlab R., Mather T.N., and Ribeiro J.M. Purification, cloning, and expression of a novel salivary anticomplement protein from the tick, Ixodes scapularis. J Biol Chem 275 25 (2000) 18717-18723
48. Soares C.A., Lima C.M., Dolan M.C., Piesman J., Beard C.B., and Zeidner N.S. Capillary feeding of specific dsRNA induces silencing of the Isac gene in nymphal Ixodes scapularis ticks. Insect Mol Biol 14 4 (2005) 443-452
49. Das S., Banerjee G., DePonte K., Marcantonio N., Kantor F.S., and Fikrig E. Salp25D, an Ixodes scapularis antioxidant, is 1 of 14 immunodominant antigens in engorged tick salivary glands. J Infect Dis 184 8 (2001) 1056-1064
50. Ribeiro J.M., Alarcon-Chaidez F., Francischetti I.M., Mans B.J., Mather T.N., Valenzuela J.G., et al. An annotated catalog of salivary gland transcripts from Ixodes scapularis ticks. Insect Biochem Mol Biol 36 2 (2006) 111-129
51. Tyson K., Elkins C., Patterson H., Fikrig E., and de Silva A. Biochemical and functional characterization of Salp20, an Ixodes scapularis tick salivary protein that inhibits the complement pathway. Insect Mol Biol 16 4 (2007) 469-479
52. Francischetti I.M.B., My Pham V., Mans B.J., Andersen J.F., Mather T.N., Lane R.S., et al. The transcriptome of the salivary glands of the female western black-legged tick Ixodes pacificus (Acari: Ixodidae). Insect Biochem Mol Biol 35 10 (2005) 1142-1161
53. Couvreur B., Beaufays Jr. M., and Charon C.D. Variability and action mechanism of a family of anticomplement proteins in Ixodes ricinus. PLoS ONE 3 1 (2008) e1400
54. Daix V., Schroeder H., Praet N., Georgin J.P., Chiappino I., Gillet L., et al. Ixodes ticks belonging to the Ixodes ricinus complex encode a family of anticomplement proteins. Insect Mol Biol 16 2 (2007) 155-166
55. Tyson K.R., Elkins C., and de Silva A.M. A novel mechanism of complement inhibition unmasked by a tick salivary protein that binds to properdin. J Immunol 180 6 (2008) 3964-3968
56. Fearon D., and Austen K. Properdin: binding to C3b and stabilization of the C3b-dependent C3 convertase. J Exp Med 142 4 (1975) 856-863
57. Hourcade D.E. The role of properdin in the assembly of the alternative pathway C3 convertases of complement. J Biol Chem 281 4 (2006) 2128-2132
58. Schroeder H., Daix V., Gillet L., Renauld J.C., and Vanderplasschen A. The paralogous salivary anti-complement proteins IRAC I and IRAC II encoded by Ixodes ricinus ticks have broad and complementary inhibitory activities against the complement of different host species. Microbes Infect 9 2 (2007) 247-250
59. Johnson S., Michalak M., Opas M., and Eggleton P. The ins and outs of calreticulin: from the ER lumen to the extracellular space. Trends Cell Biol 11 3 (2001) 122-129
60. Eggleton P., Lieu T.S., Zappi E.G., Sastry K., Coburn J., Zaner K.S., et al. Calreticulin is released from activated neutrophils and binds to C1q- and mannan-binding protein. Clin Immunol Immunopathol 72 3 (1994) 405-409
61. Kishore U., Sontheimer R.D., Sastry K.N., Zaner K.S., Zappi E.G., Hughes G.R., et al. Release of calreticulin from neutrophils may alter C1q-mediated immune functions. Biochem J 322 Pt 2 (1997) 543-550
62. Kovacs H., Campbell I.D., Strong P., Johnson S., Ward F.J., Reid K.B., et al. Evidence that C1q binds specifically to CH2-like immunoglobulin gamma motifs present in the autoantigen calreticulin and interferes with complement activation. Biochemistry 37 51 (1998) 17865-17874
63. Coppolino M.G., and Dedhar S. Calreticulin Int J Biochem Cell Biol 30 5 (1998) 553-558
64. Stuart G.R., Lynch N.J., Lu J., Geick A., Moffatt B.E., Sim R.B., et al. Localisation of the C1q-binding site within C1q receptor/calreticulin. FEBS Lett 397 2-3 (1996) 245-249
65. Pritchard D.I., Brown A., Kasper G., McElroy P., Loukas A., Hewitt C., et al. A hookworm allergen which strongly resembles calreticulin. Parasite Immunol 21 9 (1999) 439-450
66. Suchitra S., and Joshi P. Characterization of Haemonchus contortus calreticulin suggests its role in feeding and immune evasion by the parasite. Biochim Biophys Acta 1722 3 (2005) 293-303
67. Kasper G., Brown A., Eberl M., Vallar L., Kieffer N., Berry C., et al. A calreticulin-like molecule from the human hookworm Necator americanus interacts with C1q and the cytoplasmic signalling domains of some integrins. Parasite Immunol 23 3 (2001) 141-152
68. Jaworski D., Simmen F., Lamoreaux W., Coons L., Muller M., and Needham G. A secreted calreticulin protein in ixodid tick (Amblyomma americanum) saliva. J Insect Physiol 41 (1995) 369-375
69. Ferreira C.A., Da Silva Vaz I., da Silva S.S., Haag K.L., Valenzuela J.G., and Masuda A. Cloning and partial characterization of a Boophilus microplus (Acari: Ixodidae) calreticulin. Exp Parasitol 101 1 (2002) 25-34
70. Sanders M.L., Glass G.E., Nadelman R.B., Wormser G.P., Scott A.L., Raha S., et al. Antibody levels to recombinant tick calreticulin increase in humans after exposure to Ixodes scapularis (Say) and are correlated with tick engorgement indices. Am J Epidemiol 149 8 (1999) 777-784
71. Sanders M.L., Jaworski D.C., Sanchez J.L., DeFraites R.F., Glass G.E., Scott A.L., et al. Antibody to a cDNA-derived calreticulin protein from Amblyomma americanum as a biomarker of tick exposure in humans. Am J Trop Med Hyg 59 2 (1998) 279-285
72. Alarcon-Chaidez F., Ryan R., Wikel S., Dardick K., Lawler C., Foppa I.M., et al. Confirmation of tick bite by detection of antibody to ixodes calreticulin salivary protein. Clin Vaccine Immunol 13 11 (2006) 1217-1222
73. Gao J., Luo J., Fan R., Fingerle V., Guan G., Liu Z., et al. Cloning and characterization of a cDNA clone encoding calreticulin from Haemaphysalis qinghaiensis (Acari: Ixodidae). Parasitol Res 102 4 (2008) 737-746
74. Valenzuela J.G., Pham V.M., Garfield M.K., Francischetti I.M., and Ribeiro J.M. Toward a description of the sialome of the adult female mosquito Aedes aegypti. Insect Biochem Mol Biol 32 9 (2002) 1101-1122
75. Francischetti I.M., Valenzuela J.G., Pham V.M., Garfield M.K., and Ribeiro J.M. Toward a catalog for the transcripts and proteins (sialome) from the salivary gland of the malaria vector Anopheles gambiae. J Exp Biol 205 Pt 16 (2002) 2429-2451
76. Jaworski D.C., Higgins J.A., Radulovic S., Vaughan J.A., and Azad A.F. Presence of calreticulin in vector fleas (Siphonaptera). J Med Entomol 33 3 (1996) 482-489
77. Cavalcante R.R., Pereira M.H., and Gontijo N.F. Anti-complement activity in the saliva of phlebotomine sand flies and other haematophagous insects. Parasitology 127 Pt 1 (2003) 87-93