Malaria parasites co-opt human factor h to prevent complement-mediated lysis in the mosquito midgut

Cell Host and Microbe

Volumn 13, Issue 1, 2013, Pages 29-41

  Simon, Nina ^a   Lasonder, Edwin ^b   Scheuermayer, Matthias ^a   Kuehn, Andrea ^a   Tews, Sabrina ^a   Fischer, Rainer ^c   Zipfel, Peter F ^d   Skerka, Christine ^d   Pradel, Gabriele ^a,c  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c RWTH AACHEN UNIVERSITY   (Germany)

^d HANS KNÖLL INSTITUTE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C1Q; COMPLEMENT COMPONENT C3B; COMPLEMENT FACTOR H;

ARTICLE; COMPLEMENT SYSTEM; GAMETE; GAMETOGENESIS; IMMUNOBLOTTING; LYSIS; MOSQUITO; NONHUMAN; PARASITE TRANSMISSION; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION;

PLASMODIUM FALCIPARUM;

EID: 84872585440     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2012.11.013     Document Type: Article

References (34)

1. J. Baum, A.T. Papenfuss, B. Baum, T.P. Speed, and A.F. Cowman Regulation of apicomplexan actin-based motility Nat. Rev. Microbiol. 4 2006 621 628
2. T.K. Blackmore, J. Hellwage, T.A. Sadlon, N. Higgs, P.F. Zipfel, H.M. Ward, and D.L. Gordon Identification of the second heparin-binding domain in human complement factor H J. Immunol. 160 1998 3342 3348
3. J. Bosch, M.H. Paige, A.B. Vaidya, L.W. Bergman, and W.G. Hol Crystal structure of GAP50, the anchor of the invasion machinery in the inner membrane complex of Plasmodium falciparum J. Struct. Biol. 178 2012 61 73
4. M.K. Dearnley, J.A. Yeoman, E. Hanssen, S. Kenny, L. Turnbull, C.B. Whitchurch, L. Tilley, and M.W. Dixon Origin, composition, organization and function of the inner membrane complex of Plasmodium falciparum gametocytes J. Cell Sci. 125 2012 2053 2063
5. Y. Dong, F. Manfredini, and G. Dimopoulos Implication of the mosquito midgut microbiota in the defense against malaria parasites PLoS Pathog. 5 2009 e1000423
6. K. Frénal, V. Polonais, J.B. Marq, R. Stratmann, J. Limenitakis, and D. Soldati-Favre Functional dissection of the apicomplexan glideosome molecular architecture Cell Host Microbe 8 2010 343 357
7. C.A. Grotendorst, and R. Carter Complement effects of the infectivity of Plasmodium gallinaceum to Aedes aegypti mosquitoes. II. Changes in sensitivity to complement-like factors during zygote development J. Parasitol. 73 1987 980 984
8. C.A. Grotendorst, R. Carter, R. Rosenberg, and L.C. Koontz Complement effects on the infectivity of Plasmodium gallinaceum to Aedes aegypti mosquitoes. I. Resistance of zygotes to the alternative pathway of complement J. Immunol. 136 1986 4270 4274
9. J. Healer, D. McGuinness, P. Hopcroft, S. Haley, R. Carter, and E. Riley Complement-mediated lysis of Plasmodium falciparum gametes by malaria-immune human sera is associated with antibodies to the gamete surface antigen Pfs230 Infect. Immun. 65 1997 3017 3023
10. T.S. Jokiranta, P.F. Zipfel, J. Hakulinen, S. Kühn, M.K. Pangburn, J.D. Tamerius, and S. Meri Analysis of the recognition mechanism of the alternative pathway of complement by monoclonal anti-factor H antibodies: evidence for multiple interactions between H and surface bound C3b FEBS Lett. 393 1996 297 302
11. T.S. Jokiranta, J. Hellwage, V. Koistinen, P.F. Zipfel, and S. Meri Each of the three binding sites on complement factor H interacts with a distinct site on C3b J. Biol. Chem. 275 2000 27657 27662
12. M. Józsi, and P.F. Zipfel Factor H family proteins and human diseases Trends Immunol. 29 2008 380 387
13. M. Kono, S. Herrmann, N.B. Loughran, A. Cabrera, K. Engelberg, C. Lehmann, D. Sinha, B. Prinz, U. Ruch, and V. Heussler Evolution and architecture of the inner membrane complex in asexual and sexual stages of the malaria parasite Mol. Biol. Evol. 29 2012 2113 2132
14. S. Kühn, C. Skerka, and P.F. Zipfel Mapping of the complement regulatory domains in the human factor H-like protein 1 and in factor H1 J. Immunol. 155 1995 5663 5670
15. S. Luo, A.M. Blom, S. Rupp, U.C. Hipler, B. Hube, C. Skerka, and P.F. Zipfel The pH-regulated antigen 1 of Candida albicans binds the human complement inhibitor C4b-binding protein and mediates fungal complement evasion J. Biol. Chem. 286 2011 8021 8029
16. G. Margos, S. Navarette, G. Butcher, A. Davies, C. Willers, R.E. Sinden, and P.J. Lachmann Interaction between host complement and mosquito-midgut-stage Plasmodium berghei Infect. Immun. 69 2001 5064 5071
17. S. Meister, B. Agianian, F. Turlure, A. Relógio, I. Morlais, F.C. Kafatos, and G.K. Christophides Anopheles gambiae PGRPLC-mediated defense against bacteria modulates infections with malaria parasites PLoS Pathog. 5 2009 e1000542
18. M. Oppermann, T. Manuelian, M. Józsi, E. Brandt, T.S. Jokiranta, S. Heinen, S. Meri, C. Skerka, O. Götze, and P.F. Zipfel The C-terminus of complement regulator Factor H mediates target recognition: evidence for a compact conformation of the native protein Clin. Exp. Immunol. 144 2006 342 352
19. M.K. Pangburn Host recognition and target differentiation by factor H, a regulator of the alternative pathway of complement Immunopharmacology 49 2000 149 157
20. G. Pradel Proteins of the malaria parasite sexual stages: expression, function and potential for transmission blocking strategies Parasitology 134 2007 1911 1929
21. W.M. Prodinger, J. Hellwage, M. Spruth, M.P. Dierich, and P.F. Zipfel The C-terminus of factor H: monoclonal antibodies inhibit heparin binding and identify epitopes common to factor H and factor H-related proteins Biochem. J. 331 1998 41 47
22. S. Rodríguez de Córdoba, J. Esparza-Gordillo, E. Goicoechea de Jorge, M. Lopez-Trascasa, and P. Sánchez-Corral The human complement factor H: functional roles, genetic variations and disease associations Mol. Immunol. 41 2004 355 367
23. P.R. Sanders, G.T. Cantin, D.C. Greenbaum, P.R. Gilson, T. Nebl, R.L. Moritz, J.R. Yates 3rd, A.N. Hodder, and B.S. Crabb Identification of protein complexes in detergent-resistant membranes of Plasmodium falciparum schizonts Mol. Biochem. Parasitol. 154 2007 148 157
24. D. Serruto, R. Rappuoli, M. Scarselli, P. Gros, and J.A. van Strijp Molecular mechanisms of complement evasion: learning from staphylococci and meningococci Nat. Rev. Microbiol. 8 2010 393 399
25. R.E. Sinden Gametocytogenesis of Plasmodium falciparum in vitro: an electron microscopic study Parasitology 84 1982 1 11
26. C. Skerka, and P.F. Zipfel Complement factor H related proteins in immune diseases Vaccine 26 Suppl 8 2008 I9 I14
27. L. Sologub, A. Kuehn, S. Kern, J. Przyborski, R. Schillig, and G. Pradel Malaria proteases mediate inside-out egress of gametocytes from red blood cells following parasite transmission to the mosquito Cell. Microbiol. 13 2011 897 912
28. D. Weismann, K. Hartvigsen, N. Lauer, K.L. Bennett, H.P. Scholl, P. Charbel Issa, M. Cano, H. Brandstätter, S. Tsimikas, and C. Skerka Complement factor H binds malondialdehyde epitopes and protects from oxidative stress Nature 478 2011 76 81
29. World Malaria Report, W.H.O. (2011). http://www.who.int/malaria/world- malaria-report-2011/en/.
30. J.A. Yeoman, E. Hanssen, A.G. Maier, N. Klonis, B. Maco, J. Baum, L. Turnbull, C.B. Whitchurch, M.W. Dixon, and L. Tilley Tracking Glideosome-associated protein 50 reveals the development and organization of the inner membrane complex of Plasmodium falciparum Eukaryot. Cell 10 2011 556 564
31. P.F. Zipfel, and C. Skerka FHL-1/reconectin: a human complement and immune regulator with cell-adhesive function Immunol. Today 20 1999 135 140
32. P.F. Zipfel, and C. Skerka Complement regulators and inhibitory proteins Nat. Rev. Immunol. 9 2009 729 740
33. P.F. Zipfel, R. Würzner, and C. Skerka Complement evasion of pathogens: common strategies are shared by diverse organisms Mol. Immunol. 44 2007 3850 3857
34. P.F. Zipfel, T. Hallström, S. Hammerschmidt, and C. Skerka The complement fitness factor H: role in human diseases and for immune escape of pathogens, like pneumococci Vaccine 26 Suppl 8 2008 I67 I74