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Complement regulation at the molecular level: the structure of decay-accelerating factor.

Lukacik P, Roversi P, White J, Esser D, Smith GP, Billington J, Williams PA, Rudd PM, Wormald MR, Harvey DJ, Crispin MD, Radcliffe CM, Dwek RA, Evans DJ, Morgan BP, Smith RA, Lea SM
Proc Natl Acad Sci U S A 101 1279-84 (2004)
Related entries: 1ojv, 1ojw, 1ojy, 1ok1, 1ok2, 1ok9

Cited: 65 times
EuropePMC logo PMID: 14734808

Abstract

The human complement regulator CD55 is a key molecule protecting self-cells from complement-mediated lysis. X-ray diffraction and analytical ultracentrifugation data reveal a rod-like arrangement of four short consensus repeat (SCR) domains in both the crystal and solution. The stalk linking the four SCR domains to the glycosylphosphatidylinositol anchor is extended by the addition of 11 highly charged O-glycans and positions the domains an estimated 177 A above the membrane. Mutation mapping and hydrophobic potential analysis suggest that the interaction with the convertase, and thus complement regulation, depends on the burial of a hydrophobic patch centered on the linker between SCR domains 2 and 3.

Articles - 1ok3 mentioned but not cited (8)

  1. Regulators of complement activity mediate inhibitory mechanisms through a common C3b-binding mode. Forneris F, Wu J, Xue X, Ricklin D, Lin Z, Sfyroera G, Tzekou A, Volokhina E, Granneman JC, Hauhart R, Bertram P, Liszewski MK, Atkinson JP, Lambris JD, Gros P. EMBO J 35 1133-1149 (2016)
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  5. The dipeptidyl peptidase IV inhibitors vildagliptin and K-579 inhibit a phospholipase C: a case of promiscuous scaffolds in proteins. Chakraborty S, Rendón-Ramírez A, Ásgeirsson B, Dutta M, Ghosh AS, Oda M, Venkatramani R, Rao BJ, Dandekar AM, Goñi FM. F1000Res 2 286 (2013)
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  7. Switching of Receptor Binding Poses between Closely Related Enteroviruses. Zhou D, Qin L, Duyvesteyn HME, Zhao Y, Lin TY, Fry EE, Ren J, Huang KA, Stuart DI. Viruses 14 2625 (2022)
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Reviews citing this publication (16)

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Articles citing this publication (41)

  1. Structure of complement fragment C3b-factor H and implications for host protection by complement regulators. Wu J, Wu YQ, Ricklin D, Janssen BJ, Lambris JD, Gros P. Nat Immunol 10 728-733 (2009)
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  3. Structural basis for complement factor I control and its disease-associated sequence polymorphisms. Roversi P, Johnson S, Caesar JJ, McLean F, Leath KJ, Tsiftsoglou SA, Morgan BP, Harris CL, Sim RB, Lea SM. Proc Natl Acad Sci U S A 108 12839-12844 (2011)
  4. Molecular dissection of interactions between components of the alternative pathway of complement and decay accelerating factor (CD55). Harris CL, Abbott RJ, Smith RA, Morgan BP, Lea SM. J Biol Chem 280 2569-2578 (2005)
  5. Structural and functional characterization of a novel T cell receptor co-regulatory protein complex, CD97-CD55. Abbott RJ, Spendlove I, Roversi P, Fitzgibbon H, Knott V, Teriete P, McDonnell JM, Handford PA, Lea SM. J Biol Chem 282 22023-22032 (2007)
  6. Characterization of two different endo-alpha-N-acetylgalactosaminidases from probiotic and pathogenic enterobacteria, Bifidobacterium longum and Clostridium perfringens. Ashida H, Maki R, Ozawa H, Tani Y, Kiyohara M, Fujita M, Imamura A, Ishida H, Kiso M, Yamamoto K. Glycobiology 18 727-734 (2008)
  7. CD55 regulates self-renewal and cisplatin resistance in endometrioid tumors. Saygin C, Wiechert A, Rao VS, Alluri R, Connor E, Thiagarajan PS, Hale JS, Li Y, Chumakova A, Jarrar A, Parker Y, Lindner DJ, Nagaraj AB, Kim JJ, DiFeo A, Abdul-Karim FW, Michener C, Rose PG, DeBernardo R, Mahdi H, McCrae KR, Lin F, Lathia JD, Reizes O. J Exp Med 214 2715-2732 (2017)
  8. The crystal structure of a coxsackievirus B3-RD variant and a refined 9-angstrom cryo-electron microscopy reconstruction of the virus complexed with decay-accelerating factor (DAF) provide a new footprint of DAF on the virus surface. Yoder JD, Cifuente JO, Pan J, Bergelson JM, Hafenstein S. J Virol 86 12571-12581 (2012)
  9. The Kaposi's sarcoma-associated herpesvirus complement control protein (KCP) binds to heparin and cell surfaces via positively charged amino acids in CCP1-2. Mark L, Lee WH, Spiller OB, Villoutreix BO, Blom AM. Mol Immunol 43 1665-1675 (2006)
  10. Interaction of decay-accelerating factor with coxsackievirus B3. Hafenstein S, Bowman VD, Chipman PR, Bator Kelly CM, Lin F, Medof ME, Rossmann MG. J Virol 81 12927-12935 (2007)
  11. Large-scale modelling as a route to multiple surface comparisons of the CCP module family. Soares DC, Gerloff DL, Syme NR, Coulson AF, Parkinson J, Barlow PN. Protein Eng Des Sel 18 379-388 (2005)
  12. C3b deposition on human erythrocytes induces the formation of a membrane skeleton-linked protein complex. Karnchanaphanurach P, Mirchev R, Ghiran I, Asara JM, Papahadjopoulos-Sternberg B, Nicholson-Weller A, Golan DE. J Clin Invest 119 788-801 (2009)
  13. Biological activity, membrane-targeting modification, and crystallization of soluble human decay accelerating factor expressed in E. coli. White J, Lukacik P, Esser D, Steward M, Giddings N, Bright JR, Fritchley SJ, Morgan BP, Lea SM, Smith GP, Smith RA. Protein Sci 13 2406-2415 (2004)
  14. Immunophysical properties and prediction of activities for vaccinia virus complement control protein and smallpox inhibitor of complement enzymes using molecular dynamics and electrostatics. Zhang L, Morikis D. Biophys J 90 3106-3119 (2006)
  15. Decay-accelerating factor attenuates remote ischemia-reperfusion-initiated organ damage. Weeks C, Moratz C, Zacharia A, Stracener C, Egan R, Peckham R, Moore FD, Tsokos GC. Clin Immunol 124 311-327 (2007)
  16. Structure-based mapping of DAF active site residues that accelerate the decay of C3 convertases. Kuttner-Kondo L, Hourcade DE, Anderson VE, Muqim N, Mitchell L, Soares DC, Barlow PN, Medof ME. J Biol Chem 282 18552-18562 (2007)
  17. Enhanced cellular receptor usage by a bioselected variant of coxsackievirus a21. Johansson ES, Xing L, Cheng RH, Shafren DR. J Virol 78 12603-12612 (2004)
  18. Testing the Activity of Complement Convertases in Serum/Plasma for Diagnosis of C4NeF-Mediated C3 Glomerulonephritis. Blom AM, Corvillo F, Magda M, Stasiłojć G, Nozal P, Pérez-Valdivia MÁ, Cabello-Chaves V, Rodríguez de Córdoba S, López-Trascasa M, Okrój M. J Clin Immunol 36 517-527 (2016)
  19. Mutations in an Innate Immunity Pathway Are Associated with Poor Overall Survival Outcomes and Hypoxic Signaling in Cancer. Olcina MM, Balanis NG, Kim RK, Aksoy BA, Kodysh J, Thompson MJ, Hammerbacher J, Graeber TG, Giaccia AJ. Cell Rep 25 3721-3732.e6 (2018)
  20. Influence of electrostatics on the complement regulatory functions of Kaposica, the complement inhibitor of Kaposi's sarcoma-associated herpesvirus. Pyaram K, Kieslich CA, Yadav VN, Morikis D, Sahu A. J Immunol 184 1956-1967 (2010)
  21. The decay accelerating factor mutation I197V found in hemolytic uraemic syndrome does not impair complement regulation. Kavanagh D, Burgess R, Spitzer D, Richards A, Diaz-Torres ML, Goodship JA, Hourcade DE, Atkinson JP, Goodship TH. Mol Immunol 44 3162-3167 (2007)
  22. Each GPI-anchored protein species forms a specific lipid raft depending on its GPI attachment signal. Miyagawa-Yamaguchi A, Kotani N, Honke K. Glycoconj J 32 531-540 (2015)
  23. Complement therapeutics meets nanomedicine: overcoming human complement activation and leukocyte uptake of nanomedicines with soluble domains of CD55. Gifford G, Vu VP, Banda NK, Holers VM, Wang G, Groman EV, Backos D, Scheinman R, Moghimi SM, Simberg D. J Control Release 302 181-189 (2019)
  24. Comprehensive and comparative transcription analyses of the complement pathway in rainbow trout. Köbis JM, Rebl A, Kühn C, Korytář T, Köllner B, Goldammer T. Fish Shellfish Immunol 42 98-107 (2015)
  25. Order within disorder: aggrecan chondroitin sulphate-attachment region provides new structural insights into protein sequences classified as disordered. Jowitt TA, Murdoch AD, Baldock C, Berry R, Day JM, Hardingham TE. Proteins 78 3317-3327 (2010)
  26. Dissection of functional sites in herpesvirus saimiri complement control protein homolog. Reza MJ, Kamble A, Ahmad M, Krishnasastry MV, Sahu A. J Virol 87 282-295 (2013)
  27. Domain swapping reveals complement control protein modules critical for imparting cofactor and decay-accelerating activities in vaccinia virus complement control protein. Ahmad M, Raut S, Pyaram K, Kamble A, Mullick J, Sahu A. J Immunol 185 6128-6137 (2010)
  28. 1,25-Dihydroxyvitamin D3 promotes a sustained LPS-induced NF-κB-dependent expression of CD55 in human monocytic THP-1 cells. Izban MG, Nowicki BJ, Nowicki S. PLoS One 7 e49318 (2012)
  29. Structural basis for CD97 recognition of the decay-accelerating factor CD55 suggests mechanosensitive activation of adhesion GPCRs. Niu M, Xu S, Yang J, Yao D, Li N, Yan J, Zhong G, Song G. J Biol Chem 296 100776 (2021)
  30. Reduced order modeling and analysis of the human complement system. Sagar A, Dai W, Minot M, LeCover R, Varner JD. PLoS One 12 e0187373 (2017)
  31. The tag SNP rs10746463 in decay-accelerating factor is associated with the susceptibility to gastric cancer. Song Q, Zhang Z, Liu Y, Han S, Zhang X. Mol Immunol 63 473-478 (2015)
  32. Identification and characterization of TCRγ and TCRδ chains in channel catfish, Ictalurus punctatus. Moulana M, Taylor EB, Edholm ES, Quiniou SM, Wilson M, Bengtén E. Immunogenetics 66 545-561 (2014)
  33. Mapping of functional domains in herpesvirus saimiri complement control protein homolog: complement control protein domain 2 is the smallest structural unit displaying cofactor and decay-accelerating activities. Singh AK, Yadav VN, Pyaram K, Mullick J, Sahu A. J Virol 83 10299-10304 (2009)
  34. Membrane-proximal TRAIL species are incapable of inducing short circuit apoptosis signaling: Implications for drug development and basic cytokine biology. Tatzel K, Kuroki L, Dmitriev I, Kashentseva E, Curiel DT, Goedegebuure SP, Powell MA, Mutch DG, Hawkins WG, Spitzer D. Sci Rep 6 22661 (2016)
  35. Identification of a complement receptor 1 peptide for inhibition of immune hemolysis. Yu J, Heck S, Debnath A, Yazdanbakhsh K. Biochem Biophys Res Commun 353 363-368 (2007)
  36. Molecular engineering of an efficient four-domain DAF-MCP chimera reveals the presence of functional modularity in RCA proteins. Panwar HS, Ojha H, Ghosh P, Barage SH, Raut S, Sahu A. Proc Natl Acad Sci U S A 116 9953-9958 (2019)
  37. DAF in diabetic patients is subject to glycation/inactivation at its active site residues. Flückiger R, Cocuzzi E, Nagaraj RH, Shoham M, Kern TS, Medof ME. Mol Immunol 93 246-252 (2018)
  38. A desirable transgenic strategy using GGTA1 endogenous promoter-mediated knock-in for xenotransplantation model. Ko N, Shim J, Kim HJ, Lee Y, Park JK, Kwak K, Lee JW, Jin DI, Kim H, Choi K. Sci Rep 12 9611 (2022)
  39. Decay-Accelerating Factor Creates an Organ-Protective Phenotype after Hemorrhage in Conscious Rats. Simovic MO, Falabella MJ, Le TD, DalleLucca JJ, Li Y. Int J Mol Sci 23 13563 (2022)
  40. Investigating the structure of the factor B vWF-A domain/CD55 protein-protein complex using DEER spectroscopy: successes and pitfalls. Lovett JE, Abbott RJ, Roversi P, Johnson S, Caesar JJ, Doria M, Jeschke G, Timmel CR, Lea SM. Mol Phys 111 2865-2872 (2013)
  41. LifeSoaks: a tool for analyzing solvent channels in protein crystals and obstacles for soaking experiments. Pletzer-Zelgert J, Ehrt C, Fender I, Griewel A, Flachsenberg F, Klebe G, Rarey M. Acta Crystallogr D Struct Biol 79 837-856 (2023)


Related citations provided by authors (1)

  1. Biological activity, membrane-targeting modification, and crystallization of soluble human decay accelerating factor expressed in E. coli.. White J, Lukacik P, Esser D, Steward M, Giddings N, Bright JR, Fritchley SJ, Morgan BP, Lea SM, Smith GP, Smith RA Protein Sci 13 2406-15 (2004)

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