Evolution of the lectin–complement pathway and its role in innate immunity (original) (raw)
Hoffmann, J. A., Kafatos, F. C., Janeway, C. A. & Ezekowitz, R. A. Phylogenetic perspectives in innate immunity. Science284, 1313–1318 (1999). CASPubMed Google Scholar
Medzhitov, R. & Janeway, C. Jr. Innate immune recognition: mechanisms and pathways. Immunol. Rev.173, 89–97 (2000). ArticleCASPubMed Google Scholar
Walport, M. J. Complement. Second of two parts. N. Engl. J. Med.344, 1140–1144 (2001).References3and4provide an excellent review of the complement system. They focus on recent advances in the role of complement in disease, and the interaction between innate and adaptive immunity. ArticleCASPubMed Google Scholar
Kishore, U. & Reid, K. B. C1q: structure, function and receptors. Immunopharmacology49, 159–170 (2000). ArticleCASPubMed Google Scholar
Mizuno, Y., Kozutsumi, Y., Kawasaki, T. & Yamashina, I. Isolation and characterization of a mannan-binding protein from rat liver. J. Biol. Chem.256, 4247–4252 (1981). CASPubMed Google Scholar
Drickamer, K., Dordal, M. S. & Reynolds, L. Mannose-binding proteins isolated from rat liver contain carbohydrate-recognition domains linked to collagenous tails. Complete primary structures and homology with pulmonary surfactant apoprotein. J. Biol. Chem.261, 6878–6887 (1986). CASPubMed Google Scholar
Ezekowitz, R. A., Day, L. E. & Herman, G. A. A human mannose-binding protein is an acute-phase reactant that shares sequence homology with other vertebrate lectins. J. Exp. Med.167, 1034–1046 (1988). ArticleCASPubMed Google Scholar
Turner, M. W. Mannose-binding lectin: the pluripotent molecule of the innate immune system. Immunol. Today17, 532–540 (1996). ArticleCASPubMed Google Scholar
Super, M., Thiel, S., Lu, J., Levinsky, R. J. & Turner, M. W. Association of low levels of mannan-binding protein with a common defect of opsonisation. Lancet2, 1236–1239 (1989). ArticleCASPubMed Google Scholar
Summerfield, J. A. et al. Mannose-binding protein gene mutations associated with unusual and severe infections in adults. Lancet345, 886–889 (1995). ArticleCASPubMed Google Scholar
Neth, O. et al. Mannose-binding lectin binds to a range of clinically relevant microorganisms and promotes complement deposition. Infect. Immun.68, 688–693 (2000). ArticleCASPubMedPubMed Central Google Scholar
Jack, D. L., Klein, N. J. & Turner, M. W. Mannose-binding lectin: targeting the microbial world for complement attack and opsonophagocytosis. Immunol. Rev.180, 86–99 (2001). ArticleCASPubMed Google Scholar
Holmskov, U., Malhotra, R., Sim, R. B. & Jensenius, J. C. Collectins: collagenous C-type lectins of the innate immune defense system. Immunol. Today15, 67–74 (1994). ArticleCASPubMed Google Scholar
Dahl, M. R. et al. MASP-3 and its association with distinct complexes of the mannan-binding lectin complement-activation pathway. Immunity15, 127–315 (2001).This study shows that human MBL is associated with a third serine protease termed MASP3, which is generated through alternative splicing of theMASP1/3gene. Another important finding is that different MBL oligomers have distinct MASP composition and biological activities, as shown by the association of MASP1, sMAP and C3 activation with smaller MBL oligomers. ArticleCASPubMed Google Scholar
Weis, W. I., Drickamer, K. & Hendrickson, W. A. Structure of a C-type mannose-binding protein complexed with an oligosaccharide. Nature360, 127–134 (1992). ArticleCASPubMed Google Scholar
Drickamer, K. Engineering galactose-binding activity into a C-type mannose-binding protein. Nature360, 183–186 (1992). ArticleCASPubMed Google Scholar
Sheriff, S., Chang, C. Y. & Ezekowitz, R. A. Human mannose-binding protein carbohydrate-recognition domain trimerizes through a triple α-helical coiled-coil. Nature Struct. Biol.1, 789–794 (1994). ArticleCASPubMed Google Scholar
Laursen, S. B. & Nielsen, O. L. Mannan-binding lectin (MBL) in chickens: molecular and functional aspects. Dev. Comp. Immunol.24, 85–101 (2000). ArticleCASPubMed Google Scholar
Vitved, L. et al. The homologue of mannose-binding lectin in the carp family Cyprinidae is expressed at high level in spleen, and the deduced primary structure predicts affinity for galactose. Immunogenetics51, 955–964 (2000). ArticleCASPubMed Google Scholar
Matsushita, M. & Fujita, T. Ficolins and the lectin complement pathway. Immunol. Rev.180, 78–85 (2001). ArticleCASPubMed Google Scholar
Ichijo, H. et al. Molecular cloning and characterization of ficolin, a multimeric protein with fibrinogen- and collagen-like domains. J. Biol. Chem.268, 14505–14513 (1993). CASPubMed Google Scholar
Edgar, P. F. Hucolin, a new corticosteroid-binding protein from human plasma with structural similarities to ficolins, transforming growth factor-β-1-binding proteins. FEBS Lett.375, 159–161 (1995). ArticleCASPubMed Google Scholar
Matsushita, M. et al. A novel human serum lectin with collagen- and fibrinogen-like domains that functions as an opsonin. J. Biol. Chem.271, 2448–2454 (1996). ArticleCASPubMed Google Scholar
Lu, J., Tay, P. N., Kon, O. L. & Reid, K. B. Human ficolin: cDNA cloning, demonstration of peripheral-blood leucocytes as the major site of synthesis and assignment of the gene to chromosome 9. Biochem. J.313, 473–478 (1996). ArticleCASPubMedPubMed Central Google Scholar
Endo, Y., Sato, Y., Matsushita, M. & Fujita, T. Cloning and characterization of the human lectin P35 gene and its related gene. Genomics36, 515–521 (1996). ArticleCASPubMed Google Scholar
Harumiya, S. et al. Characterization of ficolins as novel elastin-binding proteins and molecular cloning of human ficolin-1. J. Biochem. (Tokyo)120, 745–751 (1996). ArticleCAS Google Scholar
Sugimoto, R. et al. Cloning and characterization of the Hakata antigen, a member of the ficolin/opsonin p35 lectin family. J. Biol. Chem.273, 20721–20727 (1998). ArticleCASPubMed Google Scholar
Fujimori, Y. et al. Molecular cloning and characterization of mouse ficolin-A. Biochem. Biophys. Res. Commun.244, 796–800 (1998). ArticleCASPubMed Google Scholar
Ohashi, T. & Erickson, H. P. Two oligomeric forms of plasma ficolin have differential lectin activity. J. Biol. Chem.272, 14220–14226 (1997). ArticleCASPubMed Google Scholar
Omori-Satoh, T., Yamakawa, Y. & Mebs, D. The antihemorrhagic factor, erinacin, from the European hedgehog (Erinaceus europaeus), a metalloprotease inhibitor of large molecular size possessing ficolin/opsonin P35 lectin domains. Toxicon38, 1561–1580 (2000). ArticleCASPubMed Google Scholar
Kenjo, A. et al. Cloning and characterization of novel ficolins from the solitary ascidian, Halocynthia roretzi. J. Biol. Chem.276, 19959–19965 (2001).The first description of ficolins in invertebrates as GlcNAc-binding lectins, which are homologues of mammalian ficolins. The presence of ficolins in invertebrates indicates their crucial role in innate immunity. ArticleCASPubMed Google Scholar
Akaiwa, M. et al. Hakata antigen, a new member of the ficolin/opsonin p35 family, is a novel human lectin secreted into bronchus/alveolus and bile. J. Histochem. Cytochem.47, 777–786 (1999). ArticleCASPubMed Google Scholar
Teh, C., Le, Y., Lee, S. H. & Lu, J. M-ficolin is expressed on monocytes and is a lectin binding to _N_-acetyl-d-glucosamine and mediates monocyte adhesion and phagocytosis of Escherichia coli. Immunology101, 225–232 (2000). ArticleCASPubMedPubMed Central Google Scholar
Matsushita, M., Endo, Y. & Fujita, T. Cutting edge: complement-activating complex of ficolin and mannose-binding-lectin-associated serine protease. J. Immunol.164, 2281–2284 (2000).This paper describes L-ficolin/P35 as another lectin that is able to mediate complement activation through association with MASPs. ArticleCASPubMed Google Scholar
Gokudan, S. et al. Horseshoe crab acetyl-group-recognizing lectins involved in innate immunity are structurally related to fibrinogen. Proc. Natl Acad. Sci. USA96, 10086–10091 (1999). ArticleCASPubMedPubMed Central Google Scholar
Kairies, N. et al. The 2.0 Å crystal structure of tachylectin 5A provides evidence for the common origin of the innate immunity and the blood coagulation systems. Proc. Natl Acad. Sci. USA98, 13519–13524 (2001). ArticleCASPubMedPubMed Central Google Scholar
Matsushita, M. & Fujita, T. Activation of the classical complement pathway by mannose-binding protein in association with a novel C1s-like serine protease. J. Exp. Med.176, 1497–1502 (1992). ArticleCASPubMed Google Scholar
Sato, T., Endo, Y., Matsushita, M. & Fujita, T. Molecular characterization of a novel serine protease involved in activation of the complement system by mannose-binding protein. Int. Immunol.6, 665–669 (1994). ArticleCASPubMed Google Scholar
Takada, F., Takayama, Y., Hatsuse, H. & Kawakami, M. A new member of the C1s family of complement proteins found in a bactericidal factor, Ra-reactive factor, in human serum. Biochem. Biophys. Res. Commun.196, 1003–1009 (1993). ArticleCASPubMed Google Scholar
Thiel, S. et al. A second serine protease associated with mannan-binding lectin that activates complement. Nature386, 506–510 (1997). ArticleCASPubMed Google Scholar
Ji, Y. H. et al. Activation of the C4 and C2 components of complement by a proteinase in serum bactericidal factor, Ra-reactive factor. J. Immunol.150, 571–578 (1993). CASPubMed Google Scholar
Matsushita, M., Takahashi, A., Hatsuse, H., Kawakami, M. & Fujita, T. Human mannose-binding protein is identical to a component of Ra-reactive factor. Biochem. Biophys. Res. Commun.183, 645–651 (1992). ArticleCASPubMed Google Scholar
Takahashi, M., Endo, Y., Fujita, T. & Matsushita, M. A truncated form of mannose-binding lectin-associated serine protease (MASP)-2 expressed by alternative polyadenylation is a component of the lectin complement pathway. Int. Immunol.11, 859–863 (1999). ArticleCASPubMed Google Scholar
Stover, C. M., Schwaeble, W. J., Lynch, N. J., Thiel, S. & Speicher, M. R. Assignment of the gene encoding mannan-binding-lectin-associated serine protease 2 (MASP2) to human chromosome 1p36.3→p36.2 by in situ hybridization and somatic-cell hybrid analysis. Cytogenet. Cell Genet.84, 148–149 (1999). ArticleCASPubMed Google Scholar
Thiel, S. et al. Interaction of C1q and mannan-binding lectin (MBL) with C1r, C1s, MBL-associated serine proteases 1 and 2, and the MBL-associated protein MAp19. J. Immunol.165, 878–887 (2000). ArticleCASPubMed Google Scholar
Gadjeva, M., Thiel, S. & Jensenius, J. C. The mannan-binding-lectin pathway of the innate immune response. Curr. Opin. Immunol.13, 74–78 (2001). ArticleCASPubMed Google Scholar
Matsushita, M., Thiel, S., Jensenius, J. C., Terai, I. & Fujita, T. Proteolytic activities of two types of mannose-binding-lectin-associated serine protease. J. Immunol.165, 2637–2642 (2000). ArticleCASPubMed Google Scholar
Vorup-Jensen, T. et al. Distinct pathways of mannan-binding lectin (MBL)- and C1-complex autoactivation revealed by reconstitution of MBL with recombinant MBL-associated serine protease 2. J. Immunol.165, 2093–2100 (2000). ArticleCASPubMed Google Scholar
Wallis, R. & Dodd, R. B. Interaction of mannose-binding protein with associated serine proteases: effects of naturally occurring mutations. J. Biol. Chem.275, 30962–30969 (2000). ArticleCASPubMed Google Scholar
Chen, C. B. & Wallis, R. Stoichiometry of complexes between mannose-binding protein and its associated serine proteases. Defining functional units for complement activation. J. Biol. Chem.276, 25894–25902 (2001). ArticleCASPubMed Google Scholar
Thielens, N. M. et al. Interaction properties of human mannan-binding lectin (MBL)-associated serine proteases 1 and 2, MBL-associated protein 19 and MBL. J. Immunol.166, 5068–5077 (2001).References49–52describe the molecular interactions between MASP1, MASP2 and sMAP/MAp19 in association with MBL. ArticleCASPubMed Google Scholar
Matsushita, M. & Fujita, T. Cleavage of the third component of complement (C3) by mannose-binding-protein-associated serine protease (MASP) with subsequent complement activation. Immunobiology194, 443–448 (1995). ArticleCASPubMed Google Scholar
Rossi, V. et al. Substrate specificities of recombinant mannan-binding-lectin-associated serine proteases 1 and 2. J. Biol. Chem.276, 40880–40887 (2001). ArticleCASPubMed Google Scholar
Endo, Y., Sato, T., Matsushita, M. & Fujita, T. Exon structure of the gene encoding the human mannose-binding-protein-associated serine protease light chain: comparison with complement C1r and C1s genes. Int. Immunol.8, 1355–1358 (1996). ArticleCASPubMed Google Scholar
Endo, Y. et al. Two lineages of mannose-binding-lectin-associated serine protease (MASP) in vertebrates. J. Immunol.161, 4924–4930 (1998). CASPubMed Google Scholar
Matsushita, M., Endo, Y., Nonaka, M. & Fujita, T. Complement-related serine proteases in tunicates and vertebrates. Curr. Opin. Immunol.10, 29–35 (1998). ArticleCASPubMed Google Scholar
Smith, L. C., Chang, L., Britten, R. J. & Davidson, E. H. Sea urchin genes expressed in activated coelomocytes are identified by expressed sequence tags. Complement homologues and other putative immune response genes suggest immune system homology within the deuterostomes. J. Immunol.156, 593–602 (1996). CASPubMed Google Scholar
Smith, L. C., Shih, C. S. & Dachenhausen, S. G. Coelomocytes express SpBf, a homologue of factor B, the second component in the sea urchin complement system. J. Immunol.161, 6784–6793 (1998). CASPubMed Google Scholar
Smith, L. C., Clow, L. A. & Terwilliger, D. P. The ancestral complement system in sea urchins. Immunol. Rev.180, 16–34 (2001). ArticleCASPubMed Google Scholar
Nonaka, M. Evolution of the complement system. Curr. Opin. Immunol.13, 69–73 (2001).An excellent, recent review of the molecular evolution of the complement system. ArticleCASPubMed Google Scholar
Sekine, H. et al. An ancient lectin-dependent complement system in an ascidian: novel lectin isolated from the plasma of the solitary ascidian, Halocynthia roretzi. J. Immunol.167, 4504–4510 (2001).This study describes the presence of glucose-binding lectin (GBL) in the plasma of the solitary ascidian, which has a carbohydrate-recognition domain but lacks a collagen-like domain. The important finding is that the GBL–MASPs complex activates C3, leading to C3-dependent phagocytosis, which indicates that the primitive complement system consists of the lectin–proteases complex and C3. ArticleCASPubMed Google Scholar
Ji, X., Azumi, K., Sasaki, M. & Nonaka, M. Ancient origin of the complement lectin pathway revealed by molecular cloning of mannan-binding-protein-associated serine protease from a urochordate, the Japanese ascidian, Halocynthia roretzi. Proc. Natl Acad. Sci. USA94, 6340–6345 (1997). ArticleCASPubMedPubMed Central Google Scholar
Nonaka, M. et al. Opsonic complement component C3 in the solitary ascidian, Halocynthia roretzi. J. Immunol.162, 387–391 (1999). CASPubMed Google Scholar
Miyazawa, S., Azumi, K. & Nonaka, M. Cloning and characterization of integrin α-subunits from the solitary ascidian, Halocynthia roretzi. J. Immunol.166, 1710–1715 (2001).This study describes the presence of C3 receptor in the ascidian — which is homologous to human C3 receptor, CR3 or CR4 — and that this receptor is involved in the phagocytosis of yeast by ascidian haemocytes. ArticleCASPubMed Google Scholar
Nair, S. V. et al. A collectin-like protein from tunicates. Comp. Biochem. Physiol. B Biochem. Mol. Biol.125, 279–289 (2000). ArticleCASPubMed Google Scholar
Vasta, G. R., Quesenberry, M., Ahmed, H. & O'Leary, N. C-type lectins and galectins mediate innate and adaptive immune functions: their roles in the complement activation pathway. Dev. Comp. Immunol.23, 401–420 (1999). ArticleCASPubMed Google Scholar
Bulgakov, A. A. et al. Isolation and properties of a mannan-binding lectin from the coelomic fluid of the holothurian Cucumaria japonica. Biochemistry (Moscow)65, 933–939 (2000). CAS Google Scholar
Horstmann, R. D., Pangburn, M. K. & Muller-Eberhard, H. J. Species specificity of recognition by the alternative pathway of complement. J. Immunol.134, 1101–1104 (1985). CASPubMed Google Scholar
Kuhlman, M., Joiner, K. & Ezekowitz, R. A. The human mannose-binding protein functions as an opsonin. J. Exp. Med.169, 1733–1745 (1989). ArticleCASPubMed Google Scholar