A tick mannose-binding lectin inhibitor interferes with the vertebrate complement cascade to enhance transmission of the Lyme disease agent

Cell Host and Microbe

Volumn 10, Issue 2, 2011, Pages 136-146

  Schuijt, Tim J ^a,b,c   Coumou, Jeroen ^a,b   Narasimhan, Sukanya ^a   Dai, Jianfeng ^a   Deponte, Kathleen ^a   Wouters, Diana ^d   Brouwer, Mieke ^d   Oei, Anneke ^b   Roelofs, Joris J T H ^b   Van Dam, Alje P ^e   Van Der Poll, Tom ^b   Van'T Veer, Cornelis ^b   Hovius, Joppe W ^b   Fikrig, Erol ^a,f  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^d ACADEMIC MEDICAL CENTER   (Netherlands)

^e Onze Lieve Vrouwe Gasthuis ^*  (Netherlands)

^f HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MANNOSE BINDING LECTIN; PROTEIN INHIBITOR; SALIVA PROTEIN; TICK SALIVARY LECTIN PATHWAY INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BORRELIA BURGDORFERI; COMPLEMENT ALTERNATIVE PATHWAY; COMPLEMENT LECTIN PATHWAY; CONTROLLED STUDY; DISEASE TRANSMISSION; FEMALE; HUMAN; HUMAN CELL; LYME DISEASE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; ANIMALS; BORRELIA BURGDORFERI; CELL MIGRATION ASSAYS; CLONING, MOLECULAR; COMPLEMENT MEMBRANE ATTACK COMPLEX; COMPLEMENT PATHWAY, MANNOSE-BINDING LECTIN; FEMALE; GENE SILENCING; HEMOLYSIS; HUMANS; IMMUNIZATION, PASSIVE; IMMUNOTHERAPY, ACTIVE; INSECT PROTEINS; IXODES; LARVA; LYME DISEASE; MICE; MICE, INBRED C3H; MOLECULAR SEQUENCE DATA; NEUTROPHILS; NYMPH; PHAGOCYTOSIS; RABBITS; RECOMBINANT PROTEINS; SALIVA; SALIVARY PROTEINS AND PEPTIDES; SEQUENCE ALIGNMENT;

BORRELIA; BORRELIA BURGDORFERI; IXODES; IXODIDA; MAMMALIA; MUS; VERTEBRATA;

EID: 80051863283     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2011.06.010     Document Type: Article

References (31)

1. S. Breitner-Ruddock, R. Würzner, J. Schulze, and V. Brade Heterogeneity in the complement-dependent bacteriolysis within the species of Borrelia burgdorferi Med. Microbiol. Immunol. (Berl.) 185 1997 253 260
2. C.A. Brissette, A.E. Cooley, L.H. Burns, S.P. Riley, A. Verma, M.E. Woodman, T. Bykowski, and B. Stevenson Lyme borreliosis spirochete Erp proteins, their known host ligands, and potential roles in mammalian infection Int. J. Med. Microbiol. 298 Suppl 1 2008 257 267
3. D.P. Eisen, M.M. Dean, M.A. Boermeester, K.J. Fidler, A.C. Gordon, G. Kronborg, J.F. Kun, Y.L. Lau, A. Payeras, and H. Valdimarsson Low serum mannose-binding lectin level increases the risk of death due to pneumococcal infection Clin. Infect. Dis. 47 2008 510 516
4. A. Estrada-Peña, and F. Jongejan Ticks feeding on humans: a review of records on human-biting Ixodoidea with special reference to pathogen transmission Exp. Appl. Acarol. 23 1999 685 715 (Pubitemid 29452207)
5. J. Faro, Y. Chen, P. Jhaveri, P. Oza, G.T. Spear, T.F. Lint, and H. Gewurz L-ficolin binding and lectin pathway activation by acetylated low-density lipoprotein Clin. Exp. Immunol. 151 2008 275 283
6. H.N. Fernandez, P.M. Henson, A. Otani, and T.E. Hugli Chemotactic response to human C3a and C5a anaphylatoxins. I. Evaluation of C3a and C5a leukotaxis in vitro and under stimulated in vivo conditions J. Immunol. 120 1978 109 115 (Pubitemid 8253794)
7. F. Fredslund, N.S. Laursen, P. Roversi, L. Jenner, C.L. Oliveira, J.S. Pedersen, M.A. Nunn, S.M. Lea, R. Discipio, L. Sottrup-Jensen, and G.R. Andersen Structure of and influence of a tick complement inhibitor on human complement component 5 Nat. Immunol. 9 2008 753 760 (Pubitemid 351859158)
8. M. Gadjeva, S. Thiel, and J.C. Jensenius Assays for the mannan-binding lectin pathway Curr. Protoc. Immunol. 2004 Chapter 13, 13, 6
9. N.J. Hepburn, A.S. Williams, M.A. Nunn, J.C. Chamberlain-Banoub, J. Hamer, B.P. Morgan, and C.L. Harris In vivo characterization and therapeutic efficacy of a C5-specific inhibitor from the soft tick Ornithodoros moubata J. Biol. Chem. 282 2007 8292 8299 (Pubitemid 47093564)
10. J.W. Hovius, M. Levi, and E. Fikrig Salivating for knowledge: potential pharmacological agents in tick saliva PLoS Med. 5 2008 e43
11. J.W. Hovius, M.F. Bijlsma, G.J. van der Windt, W.J. Wiersinga, B.J. Boukens, J. Coumou, A. Oei, R. de Beer, A.F. de Vos, and C. van 't Veer The urokinase receptor (uPAR) facilitates clearance of Borrelia burgdorferi PLoS Pathog. 5 2009 e1000447
12. W.K. Ip, K. Takahashi, K.J. Moore, L.M. Stuart, and R.A. Ezekowitz Mannose-binding lectin enhances Toll-like receptors 2 and 6 signaling from the phagosome J. Exp. Med. 205 2008 169 181 (Pubitemid 351185724)
13. W.K. Ip, K. Takahashi, R.A. Ezekowitz, and L.M. Stuart Mannose-binding lectin and innate immunity Immunol. Rev. 230 2009 9 21
14. U. Kishore, and K.B. Reid C1q: structure, function, and receptors Immunopharmacology 49 2000 159 170 (Pubitemid 30445227)
15. S.K. Kochi, R.C. Johnson, and A.P. Dalmasso Complement-mediated killing of the Lyme disease spirochete Borrelia burgdorferi. Role of antibody in formation of an effective membrane attack complex J. Immunol. 146 1991 3964 3970
16. K. Kurtenbach, S. De Michelis, S. Etti, S.M. Schäfer, H.S. Sewell, V. Brade, and P. Kraiczy Host association of Borrelia burgdorferi sensu lato - the key role of host complement Trends Microbiol. 10 2002 74 79 (Pubitemid 34119343)
17. M. Matsushita Ficolins: complement-activating lectins involved in innate immunity J Innate Immun 2 2009 24 32
18. S. Narasimhan, R.A. Koski, B. Beaulieu, J.F. Anderson, N. Ramamoorthi, F. Kantor, M. Cappello, and E. Fikrig A novel family of anticoagulants from the saliva of Ixodes scapularis Insect Mol. Biol. 11 2002 641 650 (Pubitemid 35450729)
19. V. Papatheodorou, and M. Brossard C3 levels in the sera of rabbits infested and reinfested with Ixodes ricinus L. and in midguts of fed ticks Exp. Appl. Acarol. 3 1987 53 59
20. M. Pausa, V. Pellis, M. Cinco, P.G. Giulianini, G. Presani, S. Perticarari, R. Murgia, and F. Tedesco Serum-resistant strains of Borrelia burgdorferi evade complement-mediated killing by expressing a CD59-like complement inhibitory molecule J. Immunol. 170 2003 3214 3222 (Pubitemid 36302199)
21. S. Ram, L.A. Lewis, and P.A. Rice Infections of people with complement deficiencies and patients who have undergone splenectomy Clin. Microbiol. Rev. 23 2010 740 780
22. J.M. Ribeiro, F. Alarcon-Chaidez, I.M. Francischetti, B.J. Mans, T.N. Mather, J.G. Valenzuela, and S.K. Wikel An annotated catalog of salivary gland transcripts from Ixodes scapularis ticks Insect Biochem. Mol. Biol. 36 2006 111 129 (Pubitemid 43129404)
23. D. Ricklin, G. Hajishengallis, K. Yang, and J.D. Lambris Complement: a key system for immune surveillance and homeostasis Nat. Immunol. 11 2010 785 797
24. T.J. Schuijt, J.W. Hovius, N.D. van Burgel, N. Ramamoorthi, E. Fikrig, and A.P. van Dam The tick salivary protein Salp15 inhibits the killing of serum-sensitive Borrelia burgdorferi sensu lato isolates Infect. Immun. 76 2008 2888 2894
25. T.J. Schuijt, J.W. Hovius, T. van der Poll, A.P. van Dam, and E. Fikrig Lyme borreliosis vaccination: the facts, the challenge, the future Trends Parasitol. 27 2011 40 47
26. T.J. Schuijt, S. Narasimhan, S. Daffre, K. DePonte, J.W. Hovius, C. Van't Veer, T. van der Poll, K. Bakhtiari, J.C. Meijers, and E.T. Boder Identification and characterization of Ixodes scapularis antigens that elicit tick immunity using yeast surface display PLoS ONE 6 2011 e15926
27. M. Takahashi, Y. Ishida, D. Iwaki, K. Kanno, T. Suzuki, Y. Endo, Y. Homma, and T. Fujita Essential role of mannose-binding lectin-associated serine protease-1 in activation of the complement factor D J. Exp. Med. 207 2010 29 37
28. K. Tyson, C. Elkins, H. Patterson, E. Fikrig, and A. de Silva Biochemical and functional characterization of Salp20, an Ixodes scapularis tick salivary protein that inhibits the complement pathway Insect Mol. Biol. 16 2007 469 479 (Pubitemid 47094275)
29. J.G. Valenzuela, R. Charlab, T.N. Mather, and J.M. Ribeiro Purification, cloning, and expression of a novel salivary anticomplement protein from the tick, Ixodes scapularis J. Biol. Chem. 275 2000 18717 18723 (Pubitemid 30422830)
30. A.P. van Dam, A. Oei, R. Jaspars, C. Fijen, B. Wilske, L. Spanjaard, and J. Dankert Complement-mediated serum sensitivity among spirochetes that cause Lyme disease Infect. Immun. 65 1997 1228 1236 (Pubitemid 27146607)
31. D. Wouters, I. Wagenaar-Bos, M. van Ham, and S. Zeerleder C1 inhibitor: just a serine protease inhibitor? New and old considerations on therapeutic applications of C1 inhibitor Expert Opin. Biol. Ther. 8 2008 1225 1240