Regulator-dependent mechanisms of C3b processing by factor i allow differentiation of immune responses

Nature Structural and Molecular Biology

Volumn 24, Issue 8, 2017, Pages 643-651

  Xue, Xiaoguang ^a   Wu, Jin ^a   Ricklin, Daniel ^b,e   Forneris, Federico ^a,f   Di Crescenzio, Patrizia ^b   Schmidt, Christoph Q ^b,c   Granneman, Joke ^a   Sharp, Thomas H ^d   Lambris, John D ^b   Gros, Piet ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF ULM   (Germany)

^d LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^e UNIVERSITY OF PAVIA   (Italy)

^f UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C3B; COMPLEMENT FACTOR H; COMPLEMENT FACTOR I; OPSONIN; OPSONIN C3DG; OPSONIN IC3B; UNCLASSIFIED DRUG; PROTEIN BINDING;

ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; COMPARATIVE STUDY; COMPLEMENT SYSTEM; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME SUBSTRATE COMPLEX; HUMAN; HYDROGEN BOND; IMMUNE RESPONSE; IMMUNOREGULATION; MOLECULAR DOCKING; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REGULATORY MECHANISM; THIOESTER CONTAINING DOMAIN; X RAY CRYSTALLOGRAPHY; CHEMISTRY; METABOLISM; MOLECULAR MODEL;

COMPLEMENT C3B; COMPLEMENT FACTOR H; COMPLEMENT FACTOR I; CRYSTALLOGRAPHY, X-RAY; HUMANS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEOLYSIS;

EID: 85026919046     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.3427     Document Type: Article

References (66)

1. Ricklin, D., Hajishengallis, G., Yang, K. & Lambris, J.D. Complement: A key system for immune surveillance and homeostasis. Nat. Immunol. 11, 785-797 (2010).
2. Stephan, A.H., Barres, B.A. & Stevens, B. The complement system: An unexpected role in synaptic pruning during development and disease. Annu. Rev. Neurosci. 35, 369-389 (2012).
3. Walport, M.J. Complement. First of two parts. N. Engl. J. Med. 344, 1058-1066 (2001).
4. Merle, N.S., Church, S.E., Fremeaux-Bacchi, V. & Roumenina, L.T. Complement system part I-molecular mechanisms of activation and regulation. Front. Immunol. 6, 262 (2015).
5. Merle, N.S., Noe, R., Halbwachs-Mecarelli, L., Fremeaux-Bacchi, V. & Roumenina, L.T. Complement system part II: role in immunity. Front. Immunol. 6, 257 (2015).
6. Zipfel, P.F., Lauer, N. & Skerka, C. in Inflammation and Retinal Disease: Complement Biology and Pathology Vol. 703 (eds. Lambris, J.D. & Adamis, A.P.) 9-24 (Springer New York, 2010).
7. Lambert, J.-C. et al. Genome-wide association study identifies variants at CLU and CR1 associated with Alzheimer's disease. Nat. Genet. 41, 1094-1099 (2009).
8. Brouwers, N. et al. Alzheimer risk associated with a copy number variation in the complement receptor 1 increasing C3b/C4b binding sites. Mol. Psychiatry 17, 223-233 (2012).
9. Zipfel, P.F. & Skerka, C. Complement regulators and inhibitory proteins. Nat. Rev. Immunol. 9, 729-740 (2009).
10. Ricklin, D., Reis, E.S. & Lambris, J.D. Complement in disease: A defence system turning offensive. Nat. Rev. Nephrol. 12, 383-401 (2016).
11. Lin, Z. et al. Complement C3dg-mediated erythrophagocytosis: implications for paroxysmal nocturnal hemoglobinuria. Blood 126, 891-894 (2015).
12. Ramaglia, V. et al. C3-dependent mechanism of microglial priming relevant to multiple sclerosis. Proc. Natl. Acad. Sci. USA 109, 965-970 (2012).
13. Carroll, M.C. The complement system in regulation of adaptive immunity. Nat. Immunol. 5, 981-986 (2004).
14. Kemper, C. & Atkinson, J.P. T-cell regulation: with complements from innate immunity. Nat. Rev. Immunol. 7, 9-18 (2007).
15. Roversi, P. et al. Structural basis for complement factor I control and its disease-associated sequence polymorphisms. Proc. Natl. Acad. Sci. USA 108, 12839-12844 (2011).
16. Tsiftsoglou, S.A. et al. The catalytically active serine protease domain of human complement factor I. Biochemistry 44, 6239-6249 (2005).
17. Lechtenberg, B.C., Johnson, D.J.D., Freund, S.M.V. & Huntington, J.A. NMR resonance assignments of thrombin reveal the conformational and dynamic effects of ligation. Proc. Natl. Acad. Sci. USA 107, 14087-14092 (2010).
18. Nilsson, S.C. et al. Analysis of binding sites on complement factor I that are required for its activity. J. Biol. Chem. 285, 6235-6245 (2010).
19. Wu, J. et al. Structure of complement fragment C3b-factor H and implications for host protection by complement regulators. Nat. Immunol. 10, 728-733 (2009).
20. Forneris, F. et al. Regulators of complement activity mediate inhibitory mechanisms through a common C3b-binding mode. EMBO J. 35, 1133-1149 (2016).
21. Morgan, H.P. et al. Structural basis for engagement by complement factor H of C3b on a self surface. Nat. Struct. Mol. Biol. 18, 463-470 (2011).
22. Kajander, T. et al. Dual interaction of factor H with C3d and glycosaminoglycans in host-nonhost discrimination by complement. Proc. Natl. Acad. Sci. USA 108, 2897-2902 (2011).
23. Lambris, J.D. et al. Dissection of CR1, factor H, membrane cofactor protein, and factor B binding and functional sites in the third complement component. J. Immunol. 156, 4821-4832 (1996).
24. Sahu, A., Isaacs, S.N., Soulika, A.M. & Lambris, J.D. Interaction of vaccinia virus complement control protein with human complement proteins: factor I-mediated degradation of C3b to iC3b1 inactivates the alternative complement pathway. J. Immunol. 160, 5596-5604 (1998).
25. Yadav, V.N., Pyaram, K., Mullick, J. & Sahu, A. Identification of hot spots in the variola virus complement inhibitor (SPICE) for human complement regulation. J. Virol. 82, 3283-3294 (2008).
26. Mortensen, S. et al. Structural basis for the function of complement component C4 within the classical and lectin pathways of complement. J. Immunol. 194, 5488-5496 (2015).
27. Janssen, B.J.C., Christodoulidou, A., McCarthy, A., Lambris, J.D. & Gros, P. Structure of C3b reveals conformational changes that underlie complement activity. Nature 444, 213-216 (2006).
28. Ross, G.D. et al. Generation of three different fragments of bound C3 with purified factor I or serum. II. Location of binding sites in the C3 fragments for factors B and H, complement receptors, and bovine conglutinin. J. Exp. Med. 158, 334-352 (1983).
29. Hocking, H.G. et al. Structure of the N-terminal region of complement factor H and conformational implications of disease-linked sequence variations. J. Biol. Chem. 283, 9475-9487 (2008).
30. Pechtl, I.C., Kavanagh, D., McIntosh, N., Harris, C.L. & Barlow, P.N. Disease-associated N-terminal complement factor H mutations perturb cofactor and decay-accelerating activities. J. Biol. Chem. 286, 11082-11090 (2011).
31. Gautam, A.K. et al. Mutational analysis of Kaposica reveals that bridging of MG2 and CUB domains of target protein is crucial for the cofactor activity of RCA proteins. Proc. Natl. Acad. Sci. USA 112, 12794-12799 (2015).
32. Forneris, F. et al. Structures of C3b in complex with factors B and D give insight into complement convertase formation. Science 330, 1816-1820 (2010).
33. Nishida, N., Walz, T. & Springer, T.A. Structural transitions of complement component C3 and its activation products. Proc. Natl. Acad. Sci. USA 103, 19737-19742 (2006).
34. Papanastasiou, M. et al. Structural implications for the formation and function of the complement effector protein iC3b. J. Immunol. 198, 3326-3335 (2017).
35. Alcorlo, M. et al. Unique structure of iC3b resolved at a resolution of 24 A by 3D-electron microscopy. Proc. Natl. Acad. Sci. USA 108, 13236-13240 (2011).
36. Schmidt, C.Q. et al. Rational engineering of a minimized immune inhibitor with unique triple-targeting properties. J. Immunol. 190, 5712-5721 (2013).
37. McCoy, A.J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
38. Nilsson, S.C. et al. Analysis of binding sites on complement factor I that are required for its activity. J. Biol. Chem. 285, 6235-6245 (2010).
39. Sartz, L. et al. A novel C3 mutation causing increased formation of the C3 convertase in familial atypical hemolytic uremic syndrome. J. Immunol. 188, 2030-2037 (2012).
40. Rodriguez, E., Rallapalli, P.M., Osborne, A.J. & Perkins, S.J. New functional and structural insights from updated mutational databases for complement factor H, Factor I, membrane cofactor protein and C3. Biosci. Rep. 34, 635-649 (2014).
41. Dragon-Durey, M.-A. et al. Heterozygous and homozygous factor h deficiencies associated with hemolytic uremic syndrome or membranoproliferative glomerulonephritis: report and genetic analysis of 16 cases. J. Am. Soc. Nephrol. 15, 787-795 (2004).
42. Moore, I. et al. Association of factor H autoantibodies with deletions of CFHR1, CFHR3, CFHR4, and with mutations in CFH, CFI, CD46, and C3 in patients with atypical hemolytic uremic syndrome. Blood 115, 379-387 (2010).
43. Kavanagh, D., Goodship, T.H. & Richards, A. Atypical hemolytic uremic syndrome. Semin. Nephrol. 33, 508-530 (2013).
44. Ahmad, M. et al. Domain swapping reveals complement control protein modules critical for imparting cofactor and decay-accelerating activities in vaccinia virus complement control protein. J. Immunol. 185, 6128-6137 (2010).
45. Ricklin, D., Reis, E.S., Mastellos, D.C., Gros, P. & Lambris, J.D. Complement component C3-The "Swiss Army Knife" of innate immunity and host defense. Immunol. Rev. 274, 33-58 (2016).
46. Janssen, B.J.C. et al. Insights into complement convertase formation based on the structure of the factor B-cobra venom factor complex. EMBO J. 28, 2469-2478 (2009).
47. Hart, S.P., Ross, J.A., Ross, K., Haslett, C. & Dransfield, I. Molecular characterization of the surface of apoptotic neutrophils: implications for functional downregulation and recognition by phagocytes. Cell Death Differ. 7, 493-503 (2000).
48. Gershov, D., Kim, S., Brot, N. & Elkon, K.B. C-Reactive protein binds to apoptotic cells, protects the cells from assembly of the terminal complement components, and sustains an antiinflammatory innate immune response: implications for systemic autoimmunity. J. Exp. Med. 192, 1353-1364 (2000).
49. Verbovetski, I. et al. Opsonization of apoptotic cells by autologous iC3b facilitates clearance by immature dendritic cells, down-regulates DR and CD86, and up-regulates CC chemokine receptor 7. J. Exp. Med. 196, 1553-1561 (2002).
50. Trouw, L.A. et al. C4b-binding protein and factor H compensate for the loss of membrane-bound complement inhibitors to protect apoptotic cells against excessive complement attack. J. Biol. Chem. 282, 28540-28548 (2007).
51. Kang, Y.-H., Urban, B.C., Sim, R.B. & Kishore, U. Human complement Factor H modulates C1q-mediated phagocytosis of apoptotic cells. Immunobiology 217, 455-464 (2012).
52. Verschoor, A. et al. A platelet-mediated system for shuttling blood-borne bacteria to CD8+ dendritic cells depends on glycoprotein GPIb and complement C3. Nat. Immunol. 12, 1194-1201 (2011).
53. Broadley, S.P. et al. Dual-track clearance of circulating bacteria balances rapid restoration of blood sterility with induction of adaptive immunity. Cell Host Microbe 20, 36-48 (2016).
54. Kabsch, W. XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132 (2010).
55. Evans, P.R. & Murshudov, G.N. How good are my data and what is the resolution Acta Crystallogr. D Biol. Crystallogr. 69, 1204-1214 (2013).
56. Strong, M. et al. Toward the structural genomics of complexes: crystal structure of a PE/PPE protein complex from Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 103, 8060-8065 (2006).
57. Adams, P.D. et al. PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).
58. Joosten, R.P., Long, F., Murshudov, G.N. & Perrakis, A. The PDBREDO server for macromolecular structure model optimization. IUCrJ 1, 213-220 (2014).
59. Tang, G. et al. EMAN2: An extensible image processing suite for electron microscopy. J. Struct. Biol. 157, 38-46 (2007).
60. de la Rosa-Trevín, J.M. et al. Xmipp 3.0: An improved software suite for image processing in electron microscopy. J. Struct. Biol. 184, 321-328 (2013).
61. Scheres, S.H.W., Núñez-Ramírez, R., Sorzano, C.O.S., Carazo, J.M. & Marabini, R. Image processing for electron microscopy single-particle analysis using XMIPP. Nat. Protoc. 3, 977-990 (2008).
62. Hutin, S., Brennich, M., Maillot, B. & Round, A. Online ion-exchange chromatography for small-angle X-ray scattering. Acta Crystallographica D Structural Biology 72, 1090-1099 (2016).
63. Shkumatov, A.V. & Strelkov, S.V. DATASW, a tool for HPLC-SAXS data analysis. Acta Crystallogr. D Biol. Crystallogr. 71, 1347-1350 (2015).
64. Petoukhov, M.V. et al. New developments in the ATSAS program package for small-angle scattering data analysis. J. Appl. Crystallogr. 45, 342-350 (2012).
65. The PyMOL Molecular Graphics System, V 1.8. (Schrödinger, LLC, 2015).
66. Notredame, C., Higgins, D.G. & Heringa, J. T-Coffee: A novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302, 205-217 (2000).