Residue Lys57 in the collagen-like region of human L-ficolin and its counterpart Lys47 in H-ficolin play a key role in the interaction with the mannan-binding lectin-associated serine proteases and the collectin receptor calreticulin

Journal of Immunology

Volumn 182, Issue 1, 2009, Pages 456-465

  Lacroix, Monique ^a   Dumestre Pérard, Chantal ^b   Schoehn, Guy ^a,c   Houen, Gunnar ^d   Cesbron, Jean Yves ^b   Arlaud, Gérard J ^a   Thielens, Nicole M ^a  

^a INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^b UNIV GRENOBLE ALPES   (France)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

^d STATENS SERUM INSTITUT   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ARGININE; CALRETICULIN; COLLAGEN; FICOLIN; GLUTAMINE; H FICOLIN; L FICOLIN; LYSINE; MANNAN BINDING LECTIN ASSOCIATED SERINE PROTEINASE; MANNAN BINDING LECTIN ASSOCIATED SERINE PROTEINASE 1; MANNAN BINDING LECTIN ASSOCIATED SERINE PROTEINASE 3; MUTANT PROTEIN; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; COMPLEMENT 1Q RECEPTOR; COMPLEMENT RECEPTOR; LECTIN; MANNOSE BINDING LECTIN; MASP1 PROTEIN, HUMAN; MASP2 PROTEIN, HUMAN; MEMBRANE PROTEIN;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; BINDING SITE; COMPLEMENT LECTIN PATHWAY; CONTROLLED STUDY; DISSOCIATION CONSTANT; KINETICS; LIGAND BINDING; NONHUMAN; OLIGOMERIZATION; POINT MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; WILD TYPE; ANIMAL; BIOSYNTHESIS; CELL LINE; CHEMISTRY; CHO CELL; COMPARATIVE STUDY; CRICETULUS; GENETIC VARIABILITY; GENETICS; HAMSTER; HUMAN; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; SEQUENCE HOMOLOGY;

ANIMALS; BINDING SITES; CALRETICULIN; CELL LINE; CHO CELLS; COLLAGEN; CRICETINAE; CRICETULUS; GENETIC VARIATION; HUMANS; LECTINS; LYSINE; MANNOSE-BINDING LECTIN; MANNOSE-BINDING PROTEIN-ASSOCIATED SERINE PROTEASES; MEMBRANE GLYCOPROTEINS; RECEPTORS, COMPLEMENT; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 59849111369     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.182.1.456     Document Type: Article

References (56)

1. Endo, Y., M. Matsushita, and T. Fujita. 2007. Role of ficolin in innate immunity and its molecular basis. Immunobiology 212: 371-379.
2. Bohlson, S. S., D. A. Fraser, and A. J. Tenner. 2007. Complement proteins C1q and MBL are pattern recognition molecules that signal immediate and long-term protective immune functions. Mol. Immunol. 44: 33-43.
3. Ohashi, T., and H. P. Erickson. 2004. The disulfide bonding pattern in ficolin multimers. J. Biol. Chem. 279: 6534-6539.
4. Hummelshoj, T., N. M. Thielens, H. O. Madsen, G. J. Arlaud, R. B. Sim, and P. Garred. 2007. Molecular organization of human Ficolin-2. Mol. Immunol. 44: 401-411.
5. Matsushita, M., Y. Endo, S. Taira, Y. Sato, T. Fujita, N. Ichikawa, M. Nakata, and T. Mizuochi. 1996. A novel human serum lectin with collagen- and fibrinogen-like domains that functions as an opsonin. J. Biol. Chem. 271: 2448-2454.
6. Sugimoto, R., Y. Yae, M. Akaiwa, S. Kitajima, Y. Shibata, H. Sato, J. Hirata, K. Okochi, K. Izuhara, and N. Hamasaki. 1998. Cloning and characterization of the Hakata antigen, a member of the ficolin/opsonin p35 lectin family. J. Biol. Chem. 273: 20721-20727.
7. Lu, J., P. N. Tay, O. L. Kon, and K. B. Reid. 1996. 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.
8. Ichijo, H., L. Rönnstrand, K. Miyagawa, H. Ohashi, C. H. Heldin, and K. Miyazono. 1991. Purification of transforming growth factor-β1 binding proteins from porcine uterus membranes. J. Biol. Chem. 266: 22459-22464.
9. Fujimori, Y., S. Harumiya, Y. Fukumoto, Y. Miura, K. Yagasaki, H. Tachikawa, and D. Fujimoto. 1998. Molecular cloning and characterization of mouse ficolin-A. Biochem. Biophys. Res. Commun. 244: 796-800.
10. Endo, Y., Y. Liu, K. Kanno, M. Takahashi, M. Matsushita, and T. Fujita. 2004. Identification of the mouse H-ficolin gene as a pseudogene and orthology between mouse ficolins A/B and human L-/M-ficolins. Genomics 84: 737-744.
11. Thiel, S., T. Vorup-Jensen, C. M. Stover, W. Schwaeble, S. B. Laursen, K. Poulsen, A. C. Willis, P. Eggleton, S. Hansen, U. Holmskov, et al. 1997. A second serine protease associated with mannan-binding lectin that activates complement. Nature 386: 506-510.
12. Matsushita, M., and T. Fujita. 1992. 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.
13. Matsushita, M., Y. Endo, and T. Fujita. 2000. Complement-activating complex of ficolin and mannose-binding lectin-associated serine protease. J. Immunol. 164: 2281-2284.
14. Matsushita, M., M. Kuraya, N. Hamasaki, M. Tsujimura, H. Shiraki, and T. Fujita. 2002. Activation of the lectin complement pathway by H-ficolin (Hakata antigen). J. Immunol. 168: 3502-3506.
15. Dahl, M. R., S. Thiel, M. Matsushita, T. Fujita, A. C. Willis, T. Christensen, T. Vorup-Jensen, and J. C. Jensenius. 2001. MASP-3 and its association with distinct complexes of the mannan-binding lectin complement activation pathway. Immunity 15: 127-135.
16. Stover, C. M., S. Thiel, M. Thelen, N. J. Lynch, T. Vorup-Jensen, J. C. Jensenius, and W. Schwaeble. 1999. Two constituents of the initiation complex of the mannan-binding lectin activation pathway of complement are encoded by a single structural gene. J. Immunol. 162: 3481-3490.
17. Takahashi, M., Y. Endo, T. Fujita, and M. Matsushita. 1999. 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.
18. Krarup, A., K. C. Gulla, P. Gál, K. Hajela, and R. B. Sim. 2008. The action of MBL-associated serine protease 1 (MASP1) on factor XIII and fibrinogen. Biochim. Biophys. Acta 1784: 1294-1300.
19. Takahashi, M., D. Iwaki, K. Kanno, Y. Ishida, J. Xiong, M. Matsushita, Y. Endo, S. Miura, N. Ishii, K. Sugamura, and T. Fujita. 2008. Mannose-binding lectin (MBL)-associated serine protease (MASP)-1 contributes to activation of the lectin complement pathway. J. Immunol. 180: 6132-6138.
20. Rossi, V., S. Cseh, I. Bally, N. M. Thielens, J. C. Jensenius, and G. J. Arlaud. 2001. Substrate specificities of recombinant mannan-binding lectin-associated serine proteases-1 and -2. J. Biol. Chem. 276: 40880-40887.
21. Aoyagi, Y., E. E. Adderson, J. G. Min, M. Matsushita, T. Fujita, S. Takahashi, S., Y. Okuwaki, and J. F. Bohnsack. 2005. Role of L-ficolin/mannose-binding lectinassociated serine protease complexes in the opsonophagocytosis of type III group B streptococci. J. Immunol. 174: 418-425.
22. Kuraya, M., Z. Ming, X. Liu, M. Matsushita, and T. Fujita. 2005. Specific binding of L-ficolin and H-ficolin to apoptotic cells leads to complement activation. Immunobiology 209: 689-697.
23. Jensen, M. L., C. Honoré, T. Hummelshøj, B. E. Hansen, H. O. Madsen, and P. Garred. 2007. Ficolin-2 recognizes DNA and participates in the clearance of dying host cells. Mol. Immunol. 44: 856-865.
24. Honoré, C., T. Hummelshoj, B. E. Hansen, H. O. Madsen, P. Eggleton, and P. Garred. 2007. The innate immune component ficolin 3 (Hakata antigen) mediates the clearance of late apoptotic cells. Arthritis Rheum. 56: 1598-1607.
25. Stuart, G. R., N. J. Lynch, A. J. Day, W. J. Schwaeble, and R. B. Sim. 1997. The C1q and collectin binding site within C1q receptor (cell surface calreticulin). Immunopharmacology 38: 73-80.
26. Ogden, C. A., A. DeCathelineau, P. R. Hoffmann, D. Bratton, B. Ghebrehiwet, V. A. Fadok, and P. M. Henson. 2001. C1q and mannose binding lectin engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J. Exp. Med. 194: 781-795.
27. Vandivier, R. W., C. A. Ogden, V. A. Fadok, P. R. Hoffmann, K. K. Brown, M. Botto, M. J. Walport, J. H. Fisher, P. M. Henson, and K. E. Greene. 2002. Role of surfactant proteins A, D, and C1q in the clearance of apoptotic cells in vivo and in vitro: calreticulin and CD91 as a common collectin receptor complex. J. Immunol. 169: 3978-3986.
28. Wallis, R., and R. B. Dodd. 2000. Interaction of mannose-binding protein with associated serine proteases: effects of naturally occurring mutations. J. Biol. Chem. 275: 30962-30969.
29. Thielens, N. M., S. Cseh, S. Thiel, T. Vorup-Jensen, V. Rossi, J. C. Jensenius, and G. J. Arlaud. 2001. 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.
30. Cseh, S., L. Vera, M. Matsushita, T. Fujita, G. J. Arlaud, and N. M. Thielens. 2002. Characterization of the interaction between L-ficolin/p35 and mannanbinding lectin-associated serine proteases-1 and -2. J. Immunol. 169: 5735-5743.
31. Zundel, S., S. Cseh, M. Lacroix, M. R. Dahl, M. Matsushita, J.-P. Andrieu, W. J. Schwaeble, J. C. Jensenius, T. Fujita, G. J. Arlaud, and N. M. Thielens. 2004. Characterization of recombinant mannan-binding lectin-associated serine protease (MASP)-3 suggests an activation mechanism different from that of MASP-1 and MASP-2. J. Immunol. 172: 4342-4350.
32. Teillet, F., C. Gaboriaud, M. Lacroix, L. Martin, G. J. Arlaud, and N. M. Thielens. 2008. Crystal structure of the CUB1-EGF-CUB2 domain of human MASP-1/3 and identification of its interaction sites with MBL and ficolins. J. Biol. Chem. 283: 25715-25724.
33. Teillet, F., M. Lacroix, S. Thiel, D. Weilguny, T. Agger, G. J. Arlaud, and N. M. Thielens. 2007. Identification of the site of human mannan-binding lectin involved in the interaction with its partner serine proteases: the essential role of lys55. J. Immunol. 178: 5710-5716.
34. Wallis, R., J. M. Shaw, J. Uitdehaag, C. B. Chen, D. Torgersen, and K. Drickamer. 2004. Localization of the serine protease-binding sites in the collagen-like domain of mannose-binding protein. J. Biol. Chem. 279: 14065-14073.
35. Pagh, R., K. Duus, I. Laursen, P. R. Hansen, N. Thielens, G. J. Arlaud, L. Kongerslev, P. Højrup, and G. Houen. 2008. The chaperone and potential mannan-binding lectin (MBL) co-receptor calreticulin interacts with MBL through the binding site for MBL-associated serine proteases. FEBS J. 275: 515-526.
36. Girija, U. V., A. W. Dodds, S. Roscher, K. B. Reid, and R. Wallis. 2007. Localization and characterization of the mannose-binding lectin (MBL)-associatedserine protease-2 binding site in rat ficolin-A: equivalent binding sites within the collagenous domains of MBLs and ficolins. J. Immunol. 179: 455-462.
37. Krarup, A., S. Thiel, A. Hansen, T. Fujita, and J. C. Jensenius. 2004. L-ficolin is a pattern recognition molecule specific for acetyl groups. J. Biol. Chem. 279: 47513-47519.
38. Garlatti, V., N. Belloy, L. Martin, M. Lacroix, M. Matsushita, Y. Endo, T. Fujita, J. C. Fontecilla-Camps, G. J. Arlaud, N. M. Thielens, and C. Gaboriaud. 2007. Structural insights into the innate immune recognition specificities of L- and H-ficolins. EMBO J. 26: 623-633.
39. Teillet, F., B. Dublet., J.-P. Andrieu, C. Gaboriaud, G. J. Arlaud, and N. M. Thielens. 2005. The two major oligomeric forms of human mannan-binding lectin: chemical characterization, carbohydrate binding properties and interaction with MBL-associated serine proteases. J. Immunol. 174: 2870-2877.
40. Dumestre-Perard, C., D. Ponard, G. J. Arlaud, N. Monnier, R. B. Sim, and M. G. Colomb. 2002. Evaluation and clinical interest of mannan binding lectin function in human plasma. Mol. Immunol. 39: 465-473.
41. Faro, J., Y. Chen, P. Jhaveri, P. Oza, G. T. Spear, T. F. Lint, and H. Gewurz. 2008. L-ficolin binding and lectin pathway activation by acetylated low-density lipoprotein. Clin. Exp. Immunol. 151: 275-283.
42. Hummelshoj, T., L. M. Fog, H. O. Madsen, R. B. Sim, and P. Garred. 2008. Comparative study of the human ficolins reveals unique features of Ficolin-3 (Hakata antigen). Mol. Immunol. 45: 1623-1632.
43. Tsunasawa, S., S. Nakura, T. Tanigawa, and I. Kato. 1998. Pyrrolidone carboxyl peptidase from the hyperthermophilic archaeon Pyrococcus furiosus: cloning and overexpression in Escherichia coli of the gene, and its application to protein sequence analysis. J. Biochem. 124: 778-783.
44. Ohashi, T., and H. P. Erickson. 1998. Oligomeric structure and tissue distribution of ficolins from mouse, pig and human. Arch. Biochem. Biophys. 360: 223-232.
45. Ohashi, T., and H. P. Erickson. 1997. Two oligomeric forms of plasma ficolin have differential lectin activity. J. Biol. Chem. 272: 14220-14226.
46. Schoehn, G., F. Iseni, M. Mavrakis, D. Blondel, and R. W. Ruigrok. 2001. Structure of recombinant rabies virus nucleoprotein-RNA complex and identification of the phosphoprotein binding site. J. Virol. 75: 490-498.
47. Gregory, L. A., N. M. Thielens, M. Matsushita, R. Sorensen, G. J. Arlaud, J. C. Fontecilla-Camps, and C. Gaboriaud. 2004. The x-ray structure of human mannan-binding lectin-associated protein 19 (MAp19) and its interaction site with mannan-binding lectin and L-ficolin. J. Biol. Chem. 279: 29391-29397.
48. Garlatti, V., L. Martin, E. Gout, J. B. Reiser, T. Fujita, G. J. Arlaud, N. M. Thielens, and C. Gaboriaud. 2007. Structural basis for innate immune sensing by M-ficolin and its control by a pH-dependent conformational switch. J. Biol. Chem. 282: 35814-35820.
49. Tsujimura, M., C. Ishida, Y. Sagara, T. Miyazaki, K. Murakami, H. Shiraki, K. Okochi, and Y. Maeda. 2001. Detection of serum thermolabile β-2 macroglycoprotein (Hakata antigen) by enzyme-linked immunosorbent assay using polysaccharide produced by Aerococcus viridans. Clin. Diagn. Lab. Immunol. 8: 454-459.
50. Steinø, A., C. S. Jørgensen, I. Laursen, and G. Houen. 2004. Interaction of C1q with the receptor calreticulin requires a conformational change in C1q. Scand. J. Immunol. 59: 485-495.
51. Jørgensen, C. S., L. R. Ryder, A. Steinø, P. Højrup, J. Hansen, N. H. Beyer, N. H. Heegaard, and G. Houen. 2003. Dimerization and oligomerization of the chaperone calreticulin. Eur. J. Biochem. 270: 4140-4148.
52. Stuart, G. R., N. J. Lynch, J. Lu, A. Geick, B. E. Moffatt, R. B. Sim, and W. J. Schwaeble. 1996. Localisation of the C1q binding site within C1q receptor/calreticulin. FEBS Lett. 397: 245-249.
53. Schrag, J. D., J. J. Bergeron, Y. Li, S. Borisova, M. Hahn, D. Y. Thomas, and M. Cygler. 2001. The Structure of calnexin, an ER chaperone involved in quality control of protein folding. Mol. Cell 8: 633-644.
54. Feinberg, H., J. C. Uitdehaag, J. M. Davies, R. Wallis, K. Drickamer, and W. I. Weis. 2003. Crystal structure of the CUB1-EGF-CUB2 region of mannosebinding protein associated serine protease-2. EMBO J. 22: 2348-2359.
55. 2+-binding interaction domain of C1s: insights into the assembly of the C1 complex of complement. J. Biol. Chem. 278: 32157-32164.
56. Sim, R. B., S. K. Moestrup, G. R. Stuart, N. J. Lynch, J. Lu, W. J. Schwaeble, and R. Malhotra. 1998. Interaction of C1q and the collectins with the potential receptors calreticulin (cC1qR/collectin receptor) and megalin. Immunobiology 199: 208-224.