The CLIP-Domain Serine Protease Homolog SPCLIP1 Regulates Complement Recruitment to Microbial Surfaces in the Malaria Mosquito

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The complement C3-like protein TEP1 of the mosquito Anopheles gambiae is required for defense against malaria parasites and bacteria. Two forms of TEP1 are present in the mosquito hemolymph, the full-length TEP1-F and the proteolytically processed TEP1_cut that is part of a complex including the leucine-rich repeat proteins LRIM1 and APL1C. Here we show that the non-catalytic serine protease SPCLIP1 is a key regulator of the complement-like pathway. SPCLIP1 is required for accumulation of TEP1 on microbial surfaces, a reaction that leads to lysis of malaria parasites or triggers activation of a cascade culminating with melanization of malaria parasites and bacteria. We also demonstrate that the two forms of TEP1 have distinct roles in the complement-like pathway and provide the first evidence for a complement convertase-like cascade in insects analogous to that in vertebrates. Our findings establish that core principles of complement activation are conserved throughout the evolution of animals.

Vyšlo v časopise: The CLIP-Domain Serine Protease Homolog SPCLIP1 Regulates Complement Recruitment to Microbial Surfaces in the Malaria Mosquito. PLoS Pathog 9(9): e32767. doi:10.1371/journal.ppat.1003623
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1003623

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Zdroje

1. BlandinSA, MaroisE, LevashinaEA (2008) Antimalarial responses in Anopheles gambiae: from a complement-like protein to a complement-like pathway. Cell Host Microbe 3: 364–374.

2. BlandinS, ShiaoSH, MoitaLF, JanseCJ, WatersAP, et al. (2004) Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae. Cell 116: 661–670.

3. DongY, AguilarR, XiZ, WarrE, MonginE, et al. (2006) Anopheles gambiae immune responses to human and rodent Plasmodium parasite species. PLoS Pathog 2: e52.

4. OstaMA, ChristophidesGK, KafatosFC (2004) Effects of mosquito genes on Plasmodium development. Science 303: 2030–2032.

5. PovelonesM, WaterhouseRM, KafatosFC, ChristophidesGK (2009) Leucine-rich repeat protein complex activates mosquito complement in defense against Plasmodium parasites. Science 324: 258–261.

6. RiehleMM, MarkianosK, NiareO, XuJ, LiJ, et al. (2006) Natural malaria infection in Anopheles gambiae is regulated by a single genomic control region. Science 312: 577–579.

7. GarverLS, BahiaAC, DasS, Souza-NetoJA, ShiaoJ, et al. (2012) Anopheles Imd pathway factors and effectors in infection intensity-dependent anti-Plasmodium action. PLoS Pathog 8: e1002737.

8. Molina-CruzA, DejongRJ, OrtegaC, HaileA, AbbanE, et al. (2012) Some strains of Plasmodium falciparum, a human malaria parasite, evade the complement-like system of Anopheles gambiae mosquitoes. Proc Natl Acad Sci U S A 109: E1957–62.

9. Molina-CruzA, GarverLS, AlabasterA, BangioloL, HaileA, et al. (2013) The human malaria parasite Pfs47 gene mediates evasion of the mosquito immune system. Science 340: 984–987.

10. RottschaeferSM, RiehleMM, CoulibalyB, SackoM, NiareO, et al. (2011) Exceptional diversity, maintenance of polymorphism, and recent directional selection on the APL1 malaria resistance genes of Anopheles gambiae. PLoS biology 9: e1000600.

11. WhiteBJ, LawniczakMK, ChengC, CoulibalyMB, WilsonMD, et al. (2011) Adaptive divergence between incipient species of Anopheles gambiae increases resistance to Plasmodium. Proc Natl Acad Sci U S A 108: 244–249.

12. BlandinSA, Wang-SattlerR, LamacchiaM, GagneurJ, LycettG, et al. (2009) Dissecting the genetic basis of resistance to malaria parasites in Anopheles gambiae. Science 326: 147–150.

13. CollinsFH, SakaiRK, VernickKD, PaskewitzS, SeeleyDC, et al. (1986) Genetic selection of a Plasmodium-refractory strain of the malaria vector Anopheles gambiae. Science 234: 607–610.

14. LevashinaEA, MoitaLF, BlandinS, VriendG, LagueuxM, et al. (2001) Conserved role of a complement-like protein in phagocytosis revealed by dsRNA knockout in cultured cells of the mosquito, Anopheles gambiae. Cell 104: 709–718.

15. YassineH, KamareddineL, OstaMA (2012) The mosquito melanization response is implicated in defense against the entomopathogenic fungus Beauveria bassiana. PLoS Pathog 8: e1003029.

16. FraitureM, BaxterRH, SteinertS, ChelliahY, FroletC, et al. (2009) Two mosquito LRR proteins function as complement control factors in the TEP1-mediated killing of Plasmodium. Cell Host Microbe 5: 273–284.

17. BaxterRH, SteinertS, ChelliahY, VolohonskyG, LevashinaEA, et al. (2010) A heterodimeric complex of the LRR proteins LRIM1 and APL1C regulates complement-like immunity in Anopheles gambiae. Proc Natl Acad Sci U S A 107: 16817–22.

18. WaterhouseRM, PovelonesM, ChristophidesGK (2010) Sequence-structure-function relations of the mosquito leucine-rich repeat immune proteins. BMC Genomics 11: 531.

19. KoutsosAC, BlassC, MeisterS, SchmidtS, MacCallumRM, et al. (2007) Life cycle transcriptome of the malaria mosquito Anopheles gambiae and comparison with the fruitfly Drosophila melanogaster. Proc Natl Acad Sci U S A 104: 11304–11309.

20. PovelonesM, UptonLM, SalaKA, ChristophidesGK (2011) Structure-function analysis of the Anopheles gambiae LRIM1/APL1C complex and its interaction with complement C3-like protein TEP1. PLoS pathogens 7: e1002023.

21. SchnitgerAK, KafatosFC, OstaMA (2007) The melanization reaction is not required for survival of Anopheles gambiae mosquitoes after bacterial infections. J Biol Chem 282: 21884–21888.

22. VolzJ, MullerHM, ZdanowiczA, KafatosFC, OstaMA (2006) A genetic module regulates the melanization response of Anopheles to Plasmodium. Cell Microbiol 8: 1392–1405.

23. NurnbergerT, BrunnerF, KemmerlingB, PiaterL (2004) Innate immunity in plants and animals: striking similarities and obvious differences. Immunol Rev 198: 249–266.

24. BlandinS, LevashinaEA (2004) Thioester-containing proteins and insect immunity. Mol Immunol 40: 903–908.

25. DongY, DimopoulosG (2009) Anopheles fibrinogen-related proteins provide expanded pattern recognition capacity against bacteria and malaria parasites. J Biol Chem 284: 9835–9844.

26. DongY, TaylorHE, DimopoulosG (2006) AgDscam, a hypervariable immunoglobulin domain-containing receptor of the Anopheles gambiae innate immune system. PLoS Biol 4: e229.

27. WarrE, DasS, DongY, DimopoulosG (2008) The Gram-negative bacteria-binding protein gene family: its role in the innate immune system of anopheles gambiae and in anti-Plasmodium defence. Insect Mol Biol 17: 39–51.

28. Oliveira GdeA, LiebermanJ, Barillas-MuryC (2012) Epithelial nitration by a peroxidase/NOX5 system mediates mosquito antiplasmodial immunity. Science 335: 856–859.

29. LeBV, WilliamsM, LogarajahS, BaxterRH (2012) Molecular basis for genetic resistance of Anopheles gambiae to Plasmodium: structural analysis of TEP1 susceptible and resistant alleles. PLoS Pathog 8: e1002958.

30. KimMS, BaekMJ, LeeMH, ParkJW, LeeSY, et al. (2002) A new easter-type serine protease cleaves a masquerade-like protein during prophenoloxidase activation in Holotrichia diomphalia larvae. J Biol Chem 277: 39999–40004.

31. YuXQ, JiangH, WangY, KanostMR (2003) Nonproteolytic serine proteinase homologs are involved in prophenoloxidase activation in the tobacco hornworm, Manduca sexta. Insect Biochem Mol Biol 33: 197–208.

32. KambrisZ, BrunS, JangIH, NamHJ, RomeoY, et al. (2006) Drosophila immunity: a large-scale in vivo RNAi screen identifies five serine proteases required for Toll activation. Curr Biol 16: 808–813.

33. MoitaLF, Wang-SattlerR, MichelK, ZimmermannT, BlandinS, et al. (2005) In vivo identification of novel regulators and conserved pathways of phagocytosis in A. gambiae. Immunity 23: 65–73.

34. WaterhouseRM, KriventsevaEV, MeisterS, XiZ, AlvarezKS, et al. (2007) Evolutionary dynamics of immune-related genes and pathways in disease-vector mosquitoes. Science 316: 1738–1743.

35. HabtewoldT, PovelonesM, BlagboroughAM, ChristophidesGK (2008) Transmission blocking immunity in the malaria non-vector mosquito Anopheles quadriannulatus species A. PLoS pathogens 4: e1000070.

36. SchnitgerAK, YassineH, KafatosFC, OstaMA (2009) Two C-type lectins cooperate to defend Anopheles gambiae against Gram-negative bacteria. J Biol Chem 284: 17616–17624.