Antimicrobial activity of the complement system
- Authors: Egorova E.V.1,2, Krenev I.A.1, Oborin N.N.1,2, Berlov M.N.1
-
Affiliations:
- Institute of Experimental Medicine
- Saint Petersburg State University
- Issue: Vol 23, No 2 (2023)
- Pages: 31-45
- Section: Analytical reviews
- URL: https://bakhtiniada.ru/MAJ/article/view/253866
- DOI: https://doi.org/10.17816/MAJ322841
- ID: 253866
Cite item
Abstract
The complement system plays a key role in homeostasis and defense against pathogens. The antimicrobial activity of serum against Gram-negative bacteria is usually attributed to the action of the membrane attack complex. However, there is increasing evidence that some other components of the complement system and the products of its activation are also capable of direct killing of both Gram-negative and Gram-positive bacteria. In the course of complement activation, anaphylatoxins C3a, C4a, C5a are produced, which, in addition to their main function, can exhibit a bactericidal effect and disrupt the bacterial membrane. Recent studies have shown that in fish, complement factors D, I, as well as a Ba fragment of factor B, are able to neutralize pathogens. The triggering and amplification of complement usually occurs on the surface of pathogen cells, so the local production of antimicrobial components can potentially make a significant contribution to their elimination. The aim of this review is to outline the role of individual complement members in the elimination of pathogens through direct antibiotic action. The problem of antimicrobial protection in the context of therapeutic complement inhibition is considered.
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##article.viewOnOriginalSite##About the authors
Ekaterina V. Egorova
Institute of Experimental Medicine; Saint Petersburg State University
Email: egorova.ekaterina@internet.ru
Trainee in the General Pathology Laboratory, Department of General Pathology and Pathological Physiology; Undergraduate student in the Faculty of Biology
Russian Federation, Saint Petersburg; Saint PetersburgIlia A. Krenev
Institute of Experimental Medicine
Email: il.krenevv13@yandex.ru
Junior Research Associate in the General Pathology Laboratory, Department of General Pathology and Pathological Physiology, PhD student
Russian Federation, Saint PetersburgNikita N. Oborin
Institute of Experimental Medicine; Saint Petersburg State University
Email: obnn29@gmail.com
Laboratory Technician, Laboratory of Antitumour Peptide Drugs, Department of General Pathology and Pathological Physiology; Master’s student in the Faculty of Biology
Russian Federation, Saint Petersburg; Saint PetersburgMikhail N. Berlov
Institute of Experimental Medicine
Author for correspondence.
Email: berlov.mn@iemspb.ru
ORCID iD: 0000-0001-5191-0467
SPIN-code: 9006-6127
Scopus Author ID: 6505880084
ResearcherId: O-1283-2014
Cand. Sci. (Biol.), Senior Research Associate in the General Pathology Laboratory, Department of General Pathology and Pathological Physiology
Russian Federation, Saint PetersburgReferences
- Merle NS, Church SE, Fremeaux-Bacchi V, Roumenina LT. Complement system part I: Molecular mechanisms of activation and regulation. Front Immunol. 2015;6;262. doi: 10.3389/fimmu.2015.00262
- Merle NS, Noe R, Halbwachs-Mecarelli L, et al. Complement system part II: Role in immunity. Front Immunol. 2015;6;257. doi: 10.3389/fimmu.2015.00257
- Xie CB, Jane-Wit D, Pober JS. Complement membrane attack complex: new roles, mechanisms of action, and therapeutic targets. Am J Pathol. 2020;190(6):1138–1150. doi: 10.1016/j.ajpath.2020.02.006
- Venkatraman Girija U, Gingras AR, Marshall JE, et al. Structural basis of the C1q/C1s interaction and its central role in assembly of the C1 complex of complement activation. Proc Natl Acad Sci USA. 2013;110(34):13916–13920. doi: 10.1073/pnas.1311113110
- Goldberg BS, Ackerman ME. Antibody-mediated complement activation in pathology and protection. Immunol Cell Biol. 2020;98(4):305–317. doi: 10.1111/imcb.12324
- Matsushita M, Endo Y, Fujita T. Structural and functional overview of the lectin complement pathway: its molecular basis and physiological implication. Arch Immunol Ther Exp (Warsz). 2013;61(4):273–283. doi: 10.1007/s00005-013-0229-y
- Harrison RA. The properdin pathway: an “alternative activation pathway” or a “critical amplification loop” for C3 and C5 activation? Semin Immunopathol. 2018;40(1):15–35. doi: 10.1007/s00281-017-0661-x
- Windfuhr JP, Alsenz J, Loos M. The critical concentration of C1-esterase inhibitor (C1-INH) in human serum preventing auto-activation of the first component of complement (C1). Mol Immunol. 2005;42(6):657–663. doi: 10.1016/j.molimm.2004.09.025
- Paréj K, Dobó J, Závodszky P, Gál P. The control of the complement lectin pathway activation revisited: both C1-inhibitor and antithrombin are likely physiological inhibitors, while α2-macroglobulin is not. Mol Immunol. 2013;54(3–4):415–422. doi: 10.1016/j.molimm.2013.01.009
- Noris M, Remuzzi G. Overview of complement activation and regulation. Semin Nephrol. 2013;33(6):479–492. doi: 10.1016/j.semnephrol.2013.08.001
- Bayly-Jones C, Bubeck D, Dunstone MA. The mystery behind membrane insertion: a review of the complement membrane attack complex. Philos Trans R Soc Lond B Biol Sci. 2017;372(1726):20160221. doi: 10.1098/rstb.2016.0221
- Kokryakov VN. Essays on innate immunity. Saint Petersburg: Nauka; 2006. (In Russ.)
- Luo Y, Song Y. Mechanism of antimicrobial peptides: antimicrobial, anti-inflammatory and antibiofilm activities. Int J Mol Sci. 2021;22(21):11401. doi: 10.3390/ijms222111401
- Stapels DA, Geisbrecht BV, Rooijakkers SH. Neutrophil serine proteases in antibacterial defense. Curr Opin Microbiol. 2015;23:42–48. doi: 10.1016/j.mib.2014.11.002
- Korkmaz B, Horwitz MS, Jenne DE, Gauthier F. Neutrophil elastase, proteinase 3, and cathepsin G as therapeutic targets in human diseases. Pharmacol Rev. 2010;62(4):726–759. doi: 10.1124/pr.110.002733
- Ram S, Lewis LA, Rice PA. Infections of people with complement deficiencies and patients who have undergone splenectomy. Clin Microbiol Rev. 2010;23(4):740–780. doi: 10.1128/CMR.00048-09
- Nagata M, Hara T, Aoki T, et al. Inherited deficiency of ninth component of complement: an increased risk of meningococcal meningitis. J Pediatr. 1989;114(2):260–264. doi: 10.1016/s0022-3476(89)80793-0
- Joiner KA, Warren KA, Hammer C, Frank MM. Bactericidal but not nonbactericidal C5b-9 is associated with distinctive outer membrane proteins in Neisseria gonorrhoeae. J Immunol. 1985;134(3):1920–1925. doi: 10.4049/jimmunol.134.3.1920
- Harriman GR, Esser AF, Podack ER, et al. The role of C9 in complement-mediated killing of Neisseria. J Immunol. 1981;127(6):2386–2390. doi: 10.4049/jimmunol.127.6.2386
- Niculescu F, Rus H. Mechanisms of signal transduction activated by sublytic assembly of terminal complement complexes on nucleated cells. Immunol Res. 2001;24(2):191–199. doi: 10.1385/ir:24:2:191
- Heesterbeek DA, Bardoel BW, Parsons ES, et al. Bacterial killing by complement requires membrane attack complex formation via surface-bound C5 convertases. EMBO J. 2019;38(4):e99852. doi: 10.15252/embj.201899852
- Hadders MA, Bubeck D, Roversi P, et al. Assembly and regulation of the membrane attack complex based on structures of C5b6 and sC5b9. Cell Rep. 2012;1(3):200–207. doi: 10.1016/j.celrep.2012.02.003
- Parsons ES, Stanley GJ, Pyne ALB, et al. Single-molecule kinetics of pore assembly by the membrane attack complex. Nat Commun. 2019;10(1):2066. doi: 10.1038/s41467-019-10058-7
- Bhakdi S, Tranum-Jensen J. C5b-9 assembly: average binding of one C9 molecule to C5b-8 without poly-C9 formation generates a stable transmembrane pore. J Immunol. 1986;136(8):2999–3005. doi: 10.4049/jimmunol.136.8.2999
- Sharp TH, Koster AJ, Gros P. Heterogeneous MAC initiator and pore structures in a lipid bilayer by phase-plate cryo-electron tomography. Cell Rep. 2016;15(1):1–8. doi: 10.1016/j.celrep.2016.03.002
- Menny A, Serna M, Boyd CM, et al. CryoEM reveals how the complement membrane attack complex ruptures lipid bilayers. Nat Commun. 2018;9(1):5316. doi: 10.1038/s41467-018-07653-5
- Franc V, Yang Y, Heck AJ. Proteoform profile mapping of the human serum complement component C9 revealing unexpected new features of N-, O-, and C-Glycosylation. Anal Chem. 2017;89(6):3483–3491. doi: 10.1021/acs.analchem.6b04527
- Doorduijn DJ, Rooijakkers SHM, Heesterbeek DAC. How the membrane attack complex damages the bacterial cell envelope and kills gram-negative bacteria. Bioessays. 2019;41(10):e1900074. doi: 10.1002/bies.201900074
- Hoover DL, Berger M, Nacy CA, et al. Killing of Leishmania tropica amastigotes by factors in normal human serum. J Immunol. 1984;132(2):893–897. doi: 10.4049/jimmunol.132.2.893
- Berends ET, Dekkers JF, Nijland R, et al. Distinct localization of the complement C5b-9 complex on Gram-positive bacteria. Cell Microbiol. 2013;15(12):1955–1968. doi: 10.1111/cmi.12170
- Nakamura M, Okada H, Sasaki H, et al. Quantification of the CD55 and CD59, membrane inhibitors of complement on HIV-1 particles as a function of complement-mediated virolysis. Microbiol Immunol. 1996;40(8):561–567. doi: 10.1111/j.1348-0421.1996.tb01109.x
- Kim SH, Carney DF, Hammer CH, Shin ML. Nucleated cell killing by complement: effects of C5b-9 channel size and extracellular Ca2+ on the lytic process. J Immunol. 1987;138(5):1530–1536. doi: 10.4049/jimmunol.138.5.1530
- Nauta AJ, Daha MR, Tijsma O, et al. The membrane attack complex of complement induces caspase activation and apoptosis. Eur J Immunol. 2002;32(3):783–792. doi: 10.1002/1521-4141(200203)32:3<783::AID-IMMU783>3.0.CO;2-Q
- Kim SH, Carney DF, Papadimitriou JC, Shin ML. Effect of osmotic protection on nucleated cell killing by C5b-9: cell death is not affected by the prevention of cell swelling. Mol Immunol. 1989;26(3):323–331. doi: 10.1016/0161-5890(89)90087-4
- Pilzer D, Fishelson Z. Mortalin/GRP75 promotes release of membrane vesicles from immune attacked cells and protection from complement-mediated lysis. Int Immunol. 2005;17(9):1239–1248. doi: 10.1093/intimm/dxh300
- Brown EJ. Interaction of gram-positive microorganisms with complement. Curr Top Microbiol Immunol. 1985;121:159–187. doi: 10.1007/978-3-642-45604-6_8
- Berends ET, Kuipers A, Ravesloot MM, et al. Bacteria under stress by complement and coagulation. FEMS Microbiol Rev. 2014;38(6):1146–1171. doi: 10.1111/1574-6976.12080
- Morgan BP, Boyd C, Bubeck D. Molecular cell biology of complement membrane attack. Semin Cell Dev Biol. 2017;72:124–132. doi: 10.1016/j.semcdb.2017.06.009
- O’Hara AM, Moran AP, Würzner R, Orren A. Complement-mediated lipopolysaccharide release and outer membrane damage in Escherichia coli J5: requirement for C9. Immunology. 2001;102(3):365–372. doi: 10.1046/j.1365-2567.2001.01198.x
- Wang Y, Bjes ES, Esser AF. Molecular aspects of complement-mediated bacterial killing. Periplasmic conversion of C9 from a protoxin to a toxin. J Biol Chem. 2000;275(7):4687–4692. doi: 10.1074/jbc.275.7.4687
- Dankert JR, Esser AF. Complement-mediated killing of Escherichia coli: dissipation of membrane potential by a C9-derived peptide. Biochemistry. 1986;25(5):1094–1100. doi: 10.1021/bi00353a023
- Dankert JR, Esser AF. Bacterial killing by complement. C9-mediated killing in the absence of C5b-8. Biochem J. 1987;244(2):393–399. doi: 10.1042/bj2440393
- Doorduijn DJ, Heesterbeek DAC, Ruyken M, et al. Polymerization of C9 enhances bacterial cell envelope damage and killing by membrane attack complex pores. PLoS Pathog. 2021;17(11):e1010051. doi: 10.1371/journal.ppat.1010051
- Heesterbeek DAC, Martin NI, Velthuizen A, et al. Complement-dependent outer membrane perturbation sensitizes Gram-negative bacteria to Gram-positive specific antibiotics. Sci Rep. 2019;9(1):3074. doi: 10.1038/s41598-019-38577-9
- Murray GL, Attridge SR, Morona R. Inducible serum resistance in Salmonella typhimurium is dependent on wzz(fepE)-regulated very long O antigen chains. Microbes Infect. 2005;7(13):1296–1304. doi: 10.1016/j.micinf.2005.04.015
- Grossman N, Schmetz MA, Foulds J, et al. Lipopolysaccharide size and distribution determine serum resistance in Salmonella montevideo. J Bacteriol. 1987;169(2):856–863. doi: 10.1128/jb.169.2.856-863.1987
- Schneider MC, Exley RM, Ram S, et al. Interactions between Neisseria meningitidis and the complement system. Trends Microbiol. 2007;15(5):233–240. doi: 10.1016/j.tim.2007.03.005
- Pramoonjago P, Kaneko M, Kinoshita T, et al. Role of TraT protein, an anticomplementary protein produced in Escherichia coli by R100 factor, in serum resistance. J Immunol. 1992;148(3):827–836. doi: 10.4049/jimmunol.148.3.827
- Hallström T, Siegel C, Mörgelin M, et al. CspA from Borrelia burgdorferi inhibits the terminal complement pathway. mBio. 2013;4(4):e00481–13. doi: 10.1128/mBio.00481-13
- Sjölinder H, Eriksson J, Maudsdotter L, et al. Meningococcal outer membrane protein NhhA is essential for colonization and disease by preventing phagocytosis and complement attack. Infect Immun. 2008;76(11):5412–5420. doi: 10.1128/IAI.00478-08
- Blom AM, Hallström T, Riesbeck K. Complement evasion strategies of pathogens-acquisition of inhibitors and beyond. Mol Immunol. 2009;46(14):2808–2817. doi: 10.1016/j.molimm.2009.04.025
- Singh B, Su YC, Riesbeck K. Vitronectin in bacterial pathogenesis: a host protein used in complement escape and cellular invasion. Mol Microbiol. 2010;78(3):545–560. doi: 10.1111/j.1365-2958.2010.07373.x
- Wat JM, Foley JH, Krisinger MJ, et al. Polyphosphate suppresses complement via the terminal pathway. Blood. 2014;123(5):768–776. doi: 10.1182/blood-2013-07-515726
- Zhang Q, Li Y, Tang CM. The role of the exopolyphosphatase PPX in avoidance by Neisseria meningitidis of complement-mediated killing. J Biol Chem. 2010;285(44):34259–34268. doi: 10.1074/jbc.M110.154393
- Umnyakova ES, Pashinskaya LD, Krenev IA, et al. Diseases associated with complement system dysregulation and the prospects of their treatment. Medical Academic Journal. 2018;18(3):7–16. (In Russ.) doi: 10.17816/MAJ1837-16
- Alper CA. A history of complement genetics. Exp Clin Immunogenet. 1998;15(4):203–212. doi: 10.1159/000019074
- Wessels MR, Butko P, Ma M, et al. Studies of group B streptococcal infection in mice deficient in complement component C3 or C4 demonstrate an essential role for complement in both innate and acquired immunity. Proc Natl Acad Sci USA. 1995;92(25):11490–11494. doi: 10.1073/pnas.92.25.11490
- Xu Y, Yu Y, Zhang X, et al. Molecular characterization and expression analysis of complement component 3 in dojo loach (Misgurnus anguillicaudatus). Fish Shellfish Immunol. 2018;72:484–493. doi: 10.1016/j.fsi.2017.11.022
- Kerr AR, Paterson GK, Riboldi-Tunnicliffe A, Mitchell TJ. Innate immune defense against pneumococcal pneumonia requires pulmonary complement component C3. Infect Immun. 2005;73(7):4245–4252. doi: 10.1128/IAI.73.7.4245-4252.2005
- Shokal U, Eleftherianos I. Evolution and function role of complement in cnidarian-dinoflagellate symbiosis and immune challenge in the sea anemone aiptasia pallida of thioester-containing proteins and the complement system in the innate immune response. Front Immunol. 2017;8:759. doi: 10.3389/fimmu.2017.00759
- Najafpour B, Cardoso JCR, Canário AVM, Power DM. Specific evolution and gene family expansion of complement 3 and regulatory factor H in fish. Front Immunol. 2020;11:568631. doi: 10.3389/fimmu.2020.568631
- Poole AZ, Kitchen SA, Weis VM. The role of complement in cnidarian-dinoflagellate symbiosis and immune challenge in the sea anemone aiptasia pallida. Front Microbiol. 2016;7:519. doi: 10.3389/fmicb.2016.00519
- Wang Z, Liang X, Li G, et al. Molecular characterization of complement component 3 (c3) in the pearl oyster pinctada fucata improves our understanding of the primitive complement system in bivalve. Front Immunol. 2021;12:652805. doi: 10.3389/fimmu.2021.652805
- Peronato A, Drago L, Rothbächer U, et al. Complement system and phagocytosis in a colonial protochordate. Dev Comp Immunol. 2020;103:103530. doi: 10.1016/j.dci.2019.103530
- Elvington M, Liszewski MK, Atkinson JP. Evolution of the complement system: from defense of the single cell to guardian of the intravascular space. Immunol Rev. 2016;274(1):9–15. doi: 10.1111/imr.12474
- Nordahl EA, Rydengård V, Nyberg P, et al. Activation of the complement system generates antibacterial peptides. Proc Natl Acad Sci USA. 2004;101(48):16879–16884. doi: 10.1073/pnas.0406678101
- Wu M, Jia BB, Li MF. Complement C3 and activated fragment C3a are involved in complement activation and anti-bacterial immunity. Front Immunol. 2022;13:813173. doi: 10.3389/fimmu.2022.813173
- Hugli TE. Human anaphylatoxin (C3a) from the third component of complement. Primary structure. J Biol Chem. 1975;250(21):829–8301. doi: 10.1016/s0021-9258(19)40758-8
- Klos A, Tenner AJ, Johswich KO, et al. The role of the anaphylatoxins in health and disease. Mol Immunol. 2009;46(14):2753–2766. doi: 10.1016/j.molimm.2009.04.027
- Peng Q, Li K, Sacks SH, Zhou W. The role of anaphylatoxins C3a and C5a in regulating innate and adaptive immune responses. Inflamm Allergy Drug Targets. 2009;8(3):236–246. doi: 10.2174/187152809788681038
- Zipfel PF, Reuter M. Complement activation products C3a and C4a as endogenous antimicrobial peptides. Int J Pept Res Ther. 2009;15:87–95. doi: 10.1007/s10989-009-9180-5
- Zhang XJ, Zhong YQ, Ma ZY, et al. Insights into the antibacterial properties of complement peptides C3a, C4a, and C5a across vertebrates. J Immunol. 2022;209(12):2330–2340. doi: 10.4049/jimmunol.2101019
- Pasupuleti M, Walse B, Nordahl EA, et al. Preservation of antimicrobial properties of complement peptide C3a, from invertebrates to humans. J Biol Chem. 2007;282(4):2520–2528. doi: 10.1074/jbc.M607848200
- Sonesson A, Ringstad L, Nordahl EA, et al. Antifungal activity of C3a and C3a-derivedpeptides against Candida. Biochim Biophys Acta. 2007;1768(2):346–353. doi: 10.1016/j.bbamem.2006.10.017
- Pasupuleti M, Walse B, Svensson B, et al. Rational design of antimicrobial C3a analogues with enhanced effects against Staphylococci using an integrated structure and function-based approach. Biochemistry. 2008;47(35):9057–9070. doi: 10.1021/bi800991e
- Ringstad L, Andersson Nordahl E, Schmidtchen A, Malmsten M. Composition effect on peptide interaction with lipids and bacteria: variants of C3a peptide CNY21. Biophys J. 2007;92(1):87–98. doi: 10.1529/biophysj.106.088161
- Gao S, Cui Z, Zhao MH. The complement C3a and C3a receptor pathway in kidney diseases. Front Immunol. 2020;11:1875. doi: 10.3389/fimmu.2020.01875
- Ganu VS, Müller-Eberhard HJ, Hugli TE. Factor C3f is a spasmogenic fragment released from C3b by factors I and H: the heptadeca-peptide C3f was synthesized and characterized. Mol Immunol. 1989;26(10):939–948. doi: 10.1016/0161-5890(89)90112-0
- Pozolotin VA, Umnyakova ES, Kopeykin PM, et al. Evaluation of antimicrobial activity of the C3f peptide, a derivative of human C3 protein. Russian Journal of Bioorganic Chemistry. 2021;47(3):741–748. doi: 10.1134/S1068162021030158
- Wang H, Liu M. Complement C4, infections, and autoimmune diseases. Front Immunol. 2021;12:694928. doi: 10.3389/fimmu.2021.694928
- Coss SL, Zhou D, Chua GT, et al. The complement system and human autoimmune diseases. J Autoimmun. 2022;102979. doi: 10.1016/j.jaut.2022.102979
- Zhou D, King EH, Rothwell S, et al. Low copy numbers of complement C4 and C4A deficiency are risk factors for myositis, its subgroups and autoantibodies. Ann Rheum Dis. 2023;82(2):235–245. doi: 10.1136/ard-2022-222935
- Yang Y, Chung EK, Zhou B, et al. The intricate role of complement component C4 in human systemic lupus erythematosus. Curr Dir Autoimmun. 2004;7:98–132. doi: 10.1159/000075689
- Nonaka M, Kimura A. Genomic view of the evolution of the complement system. Immunogenetics. 2006;58(9):701–713. doi: 10.1007/s00251-006-0142-1
- Gorski JP, Hugli TE, Müller-Eberhard HJ. C4a: the third anaphylatoxin of the human complement system. Proc Natl Acad Sci USA. 1979;76(10):5299–5302. doi: 10.1073/pnas.76.10.5299
- Barnum SR. C4a: An anaphylatoxin in name only. J Innate Immun. 2015;7(4):333–339. doi: 10.1159/000371423
- Laursen NS, Magnani F, Gottfredsen RH, et al. Structure, function and control of complement C5 and its proteolytic fragments. Curr Mol Med. 2012;12(8):1083–1097. doi: 10.2174/156652412802480925
- Schatz-Jakobsen JA, Yatime L, Larsen C, et al. Structural and functional characterization of human and murine C5a anaphylatoxins. Acta Crystallogr D Biol Crystallogr. 2014;70(Pt6):1704–1717. doi: 10.1107/S139900471400844X
- Hughes AL. Phylogeny of the C3/C4/C5 complement-component gene family indicates that C5 diverged first. Mol Biol Evol. 1994;11(3):417–425. doi: 10.1093/oxfordjournals.molbev.a040123
- Xu Y, Narayana SV, Volanakis JE. Structural biology of the alternative pathway convertase. Immunol Rev. 2001;180:123–135. doi: 10.1034/j.1600-065x.2001.1800111.x
- Li X, Sun L. A teleost complement factor Ba possesses antimicrobial activity and inhibits bacterial infection in fish. Dev Comp Immunol. 2017;71:49–58. doi: 10.1016/j.dci.2017.01.021
- Volanakis JE, Narayana SV. Complement factor D, a novel serine protease. Protein Sci. 1996;5(4):553–564. doi: 10.1002/pro.5560050401
- Fishelson Z, Pangburn MK, Müller-Eberhard HJ. C3 convertase of the alternative complement pathway. Demonstration of an active, stable C3b, Bb (Ni) complex. J Biol Chem. 1983;258(12):7411–7415. doi: 10.1016/s0021-9258(18)32194-x
- Ding M, Fan J, Wang W, et al. Molecular characterization, expression and antimicrobial activity of complement factor D in Megalobrama amblycephala. Fish Shellfish Immunol. 2019;89:43–51. doi: 10.1016/j.fsi.2019.03.031
- Lachmann PJ. The story of complement factor I. Immunobiology. 2019;224(4):511–517. doi: 10.1016/j.imbio.2019.05.003
- Lachmann PJ, Müller-Eberhard HJ. The demonstration in human serum of “conglutinogen-activating factor” and its effect on the third component of complement. J Immunol. 1968;100(4):691–698. doi: 10.4049/jimmunol.100.4.691
- Nakao M, Hisamatsu S, Nakahara M, et al. Molecular cloning of the complement regulatory factor I isotypes from the common carp (Cyprinus carpio). Immunogenetics. 2003;54(11):801–806. doi: 10.1007/s00251-002-0518-9
- Xiang J, Li X, Chen Y, et al. Complement factor I from flatfish half-smooth tongue (Cynoglossus semilaevis) exhibited anti-microbial activities. Dev Comp Immunol. 2015;53(1):199–209. doi: 10.1016/j.dci.2015.06.010
- Jia BB, Jin CD, Li MF. The trypsin-like serine protease domain of paralichthys olivaceus complement factor I regulates complement activation and inhibits bacterial growth. Fish Shellfish Immunol. 2020;97:18–26. doi: 10.1016/j.fsi.2019.12.019
- Rother RP, Rollins SA, Mojcik CF, et al. Discovery and development of the complement inhibitor eculizumab for the treatment of paroxysmal nocturnal hemoglobinuria. Nat Biotechnol. 2007;25(11):1256–1264. doi: 10.1038/nbt1344
- Konar M, Granoff DM. Eculizumab treatment and impaired opsonophagocytic killing of meningococci by whole blood from immunized adults. Blood. 2017;130(7):891–899. doi: 10.1182/blood-2017-05-781450
- McNamara LA, Topaz N, Wang X, et al. High risk for invasive meningococcal disease among patients receiving eculizumab (soliris) despite receipt of meningococcal vaccine. MMWR Morb Mortal Wkly Rep. 2017;66(27):734–737. doi: 10.15585/mmwr.mm6627e1
- Barnum SR. Therapeutic inhibition of complement: well worth the risk. Trends Pharmacol Sci. 2017;38(6):503–505. doi: 10.1016/j.tips.2017.03.009
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