Abstract
The complement system is a potent innate immune mechanism consisting of cascades of proteins which are designed to fight against and annul intrusion of all the foreign pathogens. Although viruses are smaller in size and have relatively simple structure, they are not immune to complement attack. Thus, activation of the complement system can lead to neutralization of cell-free viruses, phagocytosis of C3b-coated viral particles, lysis of virus-infected cells, and generation of inflammatory and specific immune responses. However, to combat host responses and succeed as pathogens, viruses not only have developed/adopted mechanisms to control complement, but also have turned these interactions to their own advantage. Important examples include poxviruses, herpesviruses, retroviruses, paramyxoviruses and picornaviruses. In this review, we provide information on the various complement evasion strategies that viruses have developed to thwart the complement attack of the host. A special emphasis is given on the interactions between the viral proteins that are involved in molecular mimicry and the complement system.
Keywords: Complement system, herpesviruses, paramyxoviruses, picornaviruses, poxviruses, retroviruses, viral mimicry
Abbreviations used
- CCP
Complement control protein
- CCPH
complement control protein homolog
- CV
coxsackieviruses;
- DAF
decay-accelerating factor
- EBV
Epstein-Barr virus
- EEV
extracellular enveloped virus
- gC-2
glycoprotein C-2
- HCMV
human cytomegalovirus
- HSV-1
herpes simplex virus-1
- HTLV-1
human T-cell leukemia virus type-1
- MAC
membrane attack complex
- MBL
mannose-binding lectin
- MCP
membrane cofactor protein
- MV
measles virus
- ORF
open reading frame
- RCA
regulators of complement activation
- HVS
herpesvirus saimiri
- SCR
short consensus repeat
- VCP
vaccinia virus complement control protein
- VV
vaccinia virus
References
- Albrecht J C, Fleckenstein B. New member of the multigene family of complement control proteins in herpesvirus saimiri. J. Virol. 1992;66:3937–3940. doi: 10.1128/jvi.66.6.3937-3940.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Albrecht J C, Nicholas J, Cameron K R, Newman C, Fleckenstein B, Honess R W. Herpesvirus saimiri has a gene specifying a homologue of the cellular membrane glycoprotein CD59. Virology. 1992;190:527–530. doi: 10.1016/0042-6822(92)91247-R. [DOI] [PubMed] [Google Scholar]
- Alsenz J, Lambris J D, Schulz T F, Dierich M P. Localization of the complement-component-C3b-binding site and the cofactor activity for factor I in the 38 kDa tryptic fragment of factor H. Biochem. J. 1984;224:389–398. doi: 10.1042/bj2240389. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Al-Sharif W Z, Sunyer J O, Lambris J D, Smith L C. Sea urchin coelomocytes specifically express a homologue of the complement component C3. J. Immunol. 1997;160:2983–2997. [PubMed] [Google Scholar]
- Bartholomew R M, Esser A F, Muller-Eberhard H J. Lysis of oncornaviruses by human serum. Isolation of the viral complement (C1) receptor and identification as p15E. J. Exp. Med. 1978;147:844–853. doi: 10.1084/jem.147.3.844. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Beebe D P, Cooper N R. Neutralization of vesicular stomatitis virus (VSV) by human complement requires a natural IgM antibody present in human serum. J. Immunol. 1981;126:1562–1568. [PubMed] [Google Scholar]
- Beebe D P, Schreiber R D, Cooper N R. Neutralization of influenza virus by normal human sera: mechanisms involving antibody and complement. J. Immunol. 1983;130:1317–1322. [PubMed] [Google Scholar]
- Bergelson J M, Chan M, Solomon K R, Stjohn N F, Lin H M, Finberg R W. Decay-accelerating factor (CD55), a glycosylphosphatidylinositol-anchored complement regulatory protein, is a receptor for several echoviruses. Proc. Natl. Acad. Sci. USA. 1994;91:6245–6249. doi: 10.1073/pnas.91.13.6245. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bergelson J M, Mohanty J G, Crowell R L, John NFS, Lublin D M, Finberg R W. Coxsackievirus B3 adapted to growth in RD cells binds to decay-accelerating factor (CD55) J. Virol. 1995;69:1903–1906. doi: 10.1128/jvi.69.3.1903-1906.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Buchholz C J, Koller D, Devaux P, Mumenthaler C, Schneider-Schaulies J, Braun W, Gerlier D, Cattaneo R. Mapping of the primary binding site of measles virus to its receptor CD46. J. Biol. Chem. 1997;272:22072–22079. doi: 10.1074/jbc.272.35.22072. [DOI] [PubMed] [Google Scholar]
- Casasnovas J M, Larvie M, Stehle T. Crystal structure of two CD46 domains reveals an extended measles virus-binding surface. EMBO J. 1999;18:2911–2922. doi: 10.1093/emboj/18.11.2911. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Clarkson N A, Kaufman R, Lublin D M, Ward T, Pipkin P A, Minor P D, Evans D J, Almond J W. Characterization of the echovirus 7 receptor: domains of CD55 critical for virus binding. J. Virol. 1995;69:5497–5501. doi: 10.1128/jvi.69.9.5497-5501.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cooper N R. Complement and viruses. In: Volanakis J E, Frank M M, editors. The human complement system in health and disease. New York: Marcel Dekker; 1998. pp. 393–407. [Google Scholar]
- Cooper N R, Nemerow G R. Complement, viruses, and virus-infected cells. Springer Semin. Immunopathol. 1983;6:327–347. doi: 10.1007/BF02116278. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dall’Olio F, Malagolini N, Speziali V, Campadelli-Fiume G, Serafini-Cessi F. Sialylated oligosaccharides O-glycosidically linked to glycoprotein C from herpes simplex virus type 1. J. Virol. 1985;56:127–134. doi: 10.1128/jvi.56.1.127-134.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dempsey P W, Allison MED, Akkaraju S, Goodnow C C, Fearon D T. C3d of complement as a molecular adjuvant: bridging innate and acquired immunity. Science. 1996;271:348–350. doi: 10.1126/science.271.5247.348. [DOI] [PubMed] [Google Scholar]
- Devaux P, Loveland B, Christiansen D, Milland J, Gerlier D. Interactions between the ectodomains of haemagglutinin and CD46 as a primary step in measles virus entry. J. Gen. Virol. 1996;77:1477–1481. doi: 10.1099/0022-1317-77-7-1477. [DOI] [PubMed] [Google Scholar]
- Dorig R E, Marcil A, Chopra A, Richardson C D. The human CD46 molecule is a receptor for measles virus (Edmonston strain) Cell. 1993;75:295–305. doi: 10.1016/0092-8674(93)80071-L. [DOI] [PubMed] [Google Scholar]
- Ebenbichler C F, Thielens N M, Vornhagen R, Marschang P, Arlaud G J, Dierich M P. Human immunodeficiency virus type 1 activates the classical pathway of complement by direct C1 binding through specific sites in the transmembrane glycoprotein gp41. J. Exp. Med. 1991;174:1417–1424. doi: 10.1084/jem.174.6.1417. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Eisenberg R J, Ponce de Leon P, Friedman H M, Fries L F, Frank M M, Hastings J C, Cohen G H. Complement component C3b binds directly to purified glycoprotein C of herpes simplex virus types 1 and 2. Microbial Path. 1987;3:423–435. doi: 10.1016/0882-4010(87)90012-X. [DOI] [PubMed] [Google Scholar]
- Engelstad M, Howard S T, Smith G L. A constitutively expressed vaccinia gene encodes a 42-kDa glycoprotein related to complement control factors that forms part of the extracellular virus envelope. Virology. 1992;188:801–810. doi: 10.1016/0042-6822(92)90535-W. [DOI] [PubMed] [Google Scholar]
- Ezekowitz R A, Kuhlman M, Groopman J E, Byrn R A. A human serum mannose-binding protein inhibits in vitro infection by the human immunodeficiency virus. J. Exp. Med. 1989;169:185–196. doi: 10.1084/jem.169.1.185. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fingeroth J D, Weis J J, Tedder T F, Strominger J L, Biro P A, Fearon D T. Epstein-Barr virus receptor of human B lymphocytes is the C3d receptor CR2. Proc. Natl. Acad. Sci. USA. 1984;81:4510–4514. doi: 10.1073/pnas.81.14.4510. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fodor W L, Rollins S A, Biancocaron S, Rother R P, Guilmette E R, Burton W V, Albrecht J C, Fleckenstein B, Squinto S P. The complement control protein homolog of herpesvirus saimiri regulates serum complement by inhibiting C3 convertase activity. J. Virol. 1995;69:3889–3892. doi: 10.1128/jvi.69.6.3889-3892.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Friedman H M, Cohen G H, Eisenberg R J, Seidel C A, Cines D B. Glycoprotein C of herpes simplex virus 1 acts as a receptor for the C3b complement component on infected cells. Nature (London) 1984;309:633–635. doi: 10.1038/309633a0. [DOI] [PubMed] [Google Scholar]
- Friedman H M, Wang L, Fishman N O, Lambris J D, Eisenberg R J, Cohen G H, Lubinsky J. Immune evasion properties of herpes simplex virus type 1 glycoprotein gC. J. Virol. 1996;70:4253–4260. doi: 10.1128/jvi.70.7.4253-4260.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Friedman H M, Wang L, Pangburn M K, Lambris J D, Lubinski J. Novel mechanism of antibody-independent complement neutralization of herpes simplex virus type 1. J. Immunol. 2000;165:4528–4536. doi: 10.4049/jimmunol.165.8.4528. [DOI] [PubMed] [Google Scholar]
- Fries L F, Friedman H M, Cohen G H, Eisenberg R J, Hammer C H, Frank M M. Glycoprotein C of herpes simplex virus 1 is an inhibitor of the complement cascade. J. Immunol. 1986;137:1636–1641. [PubMed] [Google Scholar]
- Frink R J, Eisenberg R, Cohen G, Wagner E K. Detailed analysis of the portion of the herpes simplex virus type 1 genome encoding glycoprotein C. J. Virol. 1983;45:634–647. doi: 10.1128/jvi.45.2.634-647.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goebel S J, Johnson G P, Perkus M E, Davis S W, Winslow J P, Paoletti E. The complete DNA sequence of vaccinia virus. Virology. 1990;179:247–263. doi: 10.1016/0042-6822(90)90294-2. [DOI] [PubMed] [Google Scholar]
- Gordon D L, Kaufman R M, Blackmore T K, Kwong J, Lublin D M. Identification of complement regulatory domains in human factor H. J. Immunol. 1995;155:348–356. [PubMed] [Google Scholar]
- Henderson C E, Bromek K, Mullin N P, Smith B O, Uhrin D, Barlow P N. Solution structure and dynamics of the central CCP module pair of a poxvirus complement control protein. J. Mol. Biol. 2001;307:323–339. doi: 10.1006/jmbi.2000.4477. [DOI] [PubMed] [Google Scholar]
- Hidaka Y, Sakai Y, Toh Y, Mori R. Glycoprotein C of herpes simplex virus type 1 is essential for the virus to evade antibody-independent complement-mediated virus inactivation and lysis of virus-infected cells. J. Gen. Virol. 1991;72:915–921. doi: 10.1099/0022-1317-72-4-915. [DOI] [PubMed] [Google Scholar]
- Hidaka Y, Sakuma S, Kumano Y, Minagawa H, Mori R. Characterization of glycoprotein C-negative mutants of herpes simplex virus type 1 isolated from a patient with keratitis. Arch. Virol. 1990;113:195–207. doi: 10.1007/BF01316673. [DOI] [PubMed] [Google Scholar]
- Hirsch R L, Winkelstein J A, Griffin D E. The role of complement in viral infections. III. Activation of the classical and alternative complement pathways by Sindbis virus. J. Immunol. 1980;124:2507–2510. [PubMed] [Google Scholar]
- Hung S L, Peng C, Kostavasili I, Friedman H M, Lambris J D, Eisenberg R J, Cohen G H. The interaction of glycoprotein C of herpes simplex virus types 1 and 2 with the alternative complement pathway. Virology. 1994;203:299–312. doi: 10.1006/viro.1994.1488. [DOI] [PubMed] [Google Scholar]
- Hung S L, Srinivasan S, Friedman H M, Eisenberg R J, Cohen G H. Structural basis of C3b binding by glycoprotein-C of herpes simplex virus. J. Virol. 1992;66:4013–4027. doi: 10.1128/jvi.66.7.4013-4027.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Isaacs S N, Kotwal G J, Moss B. Vaccinia virus complement-control protein prevents antibody-dependent complement-enhanced neutralization of infectivity and contributes to virulence. Proc. Natl. Acad. Sci. USA. 1992a;89:628–632. doi: 10.1073/pnas.89.2.628. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Isaacs S N, Wolffe E J, Payne L G, Moss B. Characterization of a vaccinia virus-encoded 42-kilodalton class I membrane glycoprotein component of the extracellular virus envelope. J. Virol. 1992b;66:7217–7224. doi: 10.1128/jvi.66.12.7217-7224.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ishii Y, Shimomura H, Itoh M, Miyake M, Ikeda F, Miyaike J, Fujioka S, Iwasaki Y, Tsuji H, Tsuji T. Cold activation of serum complement in patients with chronic hepatitis C: study on activating pathway and involvement of IgG. Acta Med. Okayama. 2001;55:229–235. doi: 10.18926/AMO/31989. [DOI] [PubMed] [Google Scholar]
- Iwata K, Seya T, Yanagi Y, Pesando J M, Johnson P M, Okabe M, Ueda S, Ariga H, Nagasawa S. Diversity of sites for measles virus binding and for inactivation of complement C3b and C4b on membrane cofactor protein CD46. J. Biol. Chem. 1995;270:15148–15152. doi: 10.1074/jbc.270.25.15148. [DOI] [PubMed] [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 49. Proc. Natl. Acad. Sci. USA. 1997;94:6340–6345. doi: 10.1073/pnas.94.12.6340. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Johnson D C, Spear P G. O-linked oligosaccharides are acquired by herpes simplex virus glycoproteins in the Golgi apparatus. Cell. 1983;32:987–997. doi: 10.1016/0092-8674(83)90083-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kelkar S D, Gogate S S. Macrophage-virus interaction during Con A-induced protection against Japanese encephalitis virus in infant mice. Acta Virol. 1987;31:103–108. [PubMed] [Google Scholar]
- Kim Y U, Carroll M C, Isenman D E, Nonaka M, Pramoonjago P, Takeda J, Inoue K, Kinoshita T. Covalent binding of C3b to C4b within the classical complement pathway C5 convertase: Determination of amino acid residues involved in ester linkage formation. J. Biol. Chem. 1992;267:4171–4176. [PubMed] [Google Scholar]
- Kinoshita T, Takata Y, Kozono H, Takeda J, Hong K, Inoue K. C5 convertase of the alternative complement path-way: covalent linkage between two C3b molecules within the trimolecular complex enzyme. J. Immunol. 1988;141:3895–3901. [PubMed] [Google Scholar]
- Klickstein L B, Bartow T J, Miletic V, Rabson L D, Smith J A, Fearon D T. Identification of distinct C3b and C4b recognition sites in the human C3b/C4b receptor (CR1, CD35) by deletion mutagenesis. J. Exp. Med. 1988;168:1699–1717. doi: 10.1084/jem.168.5.1699. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kostavasil I, Sahu A, Friedman H M, Eisenberg R J, Cohen G H, Lambris J D. Mechanism of complement inactivation by glycoprotein C of herpes simplex virus. J. Immunol. 1997;158:1763–1771. [PubMed] [Google Scholar]
- Kotwal G J, Isaacs S N, Mckenzie R, Frank M M, Moss B. Inhibition of the complement cascade by the major secretory protein of vaccinia virus. Science. 1990;250:827–830. doi: 10.1126/science.2237434. [DOI] [PubMed] [Google Scholar]
- Kotwal G J, Moss B. Vaccinia virus encodes a secretory polypeptide structurally related to complement control proteins. Nature (London) 1988;335:176–178. doi: 10.1038/335176a0. [DOI] [PubMed] [Google Scholar]
- Krych M, Hourcade D, Atkinson J P. Sites within the complement C3b C4b receptor important for the specificity of ligand binding. Proc. Natl. Acad. Sci. USA. 1991;88:4353–4357. doi: 10.1073/pnas.88.10.4353. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lambris J D, Ganu V S, Hirani S, Müller-Eberhard H J. Mapping of the C3d receptor (CR2)-binding site and a neoantigenic site in the C3d domain of the third component of complement. Proc. Natl. Acad. Sci. USA. 1985;82:4235–4239. doi: 10.1073/pnas.82.12.4235. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lambris J D, Sahu A, Wetsel R. The chemistry and biology of C3,C4, and C5. In: Volanakis J E, Frank M, editors. The human complement systemin health and disease. New York: Marcel Dekker; 1998. pp. 83–118. [Google Scholar]
- Lea S M, Powell R M, Mckee T, Evans D J, Brown D, Stuart D I, van der Merwe P A. Determination of the affinity and kinetic constants for the interaction between the human virus echovirus 11 and its cellular receptor, CD55. J. Biol. Chem. 1998;273:30443–30447. doi: 10.1074/jbc.273.46.30443. [DOI] [PubMed] [Google Scholar]
- Levashina E A, Moita L F, Blandin S, Vriend G, Lagueux M, Kafatos F C. Conserved role of a complement-like protein in phagocytosis revealed by dsRNA knockout in cultured cells of the mosquito. Anopheles gambiae; Cell. 2001;104:709–718. doi: 10.1016/S0092-8674(01)00267-7. [DOI] [PubMed] [Google Scholar]
- Lowell C A, Klickstein L B, Carter R H, Mitchell J A, Fearon D T, Ahearn J M. Mapping of the Epstein-Barr virus and C3dg binding sites to a common domain on complement receptor type 2. J. Exp. Med. 1989;170:1931–1946. doi: 10.1084/jem.170.6.1931. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lubinski J, Wang L, Mastellos D, Sahu A, Lambris J D, Friedman H M. In vivo role of complement-interacting domains of herpes simplex virus type 1 glycoprotein gC. J. Exp. Med. 1999;190:1637–1646. doi: 10.1084/jem.190.11.1637. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maisner A, Alvarez J, Liszewski M K, Atkinson D J, Atkinson J P, Herrler G. The N-glycan of the SCR 2 region is essential for membrane cofactor protein (CD46) to function as a measles virus receptor. J. Virol. 1996;70:4973–4977. doi: 10.1128/jvi.70.8.4973-4977.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Manchester M, Gairin J E, Patterson J B, Alvarez J, Liszewski M K, Eto D S, Atkinson J P, Oldstone M B. Measles virus recognizes its receptor, CD46, via two distinct binding domains within SCR1-2. Virology. 1997;233:174–184. doi: 10.1006/viro.1997.8581. [DOI] [PubMed] [Google Scholar]
- Manchester M, Liszewski M K, Atkinson J P, Oldstone M B. Multiple isoforms of CD46 (membrane cofactor protein) serve as receptors for measles virus. Proc. Natl. Acad. Sci. USA. 1994;91:2161–2165. doi: 10.1073/pnas.91.6.2161. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Manchester M, Rall G F. Model Systems: transgenic mouse models for measles pathogenesis. Trends Microbiol. 2001;9:19–23. doi: 10.1016/S0966-842X(00)01903-X. [DOI] [PubMed] [Google Scholar]
- Manchester M, Valsamakis A, Kaufman R, Liszewski M K, Alvarez J, Atkinson J P, Lublin D M, Oldstone MBA. Measles virus and C3 binding sites are distinct on membrane cofactor protein (CD46) Proc. Natl. Acad. Sci. USA. 1995;92:2303–2307. doi: 10.1073/pnas.92.6.2303. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Marschang P, Sodroski J, Wurzner R, Dierich M P. Decay-accelerating factor (CD55) protects human immuno-deficiency virus type 1 from inactivation by human complement. Eur. J. Immunol. 1995;25:285–290. doi: 10.1002/eji.1830250147. [DOI] [PubMed] [Google Scholar]
- Martinezpomares L, Thompson J P, Moyer R W. Mapping and investigation of the role in pathogenesis of the major unique secreted 35-kDa protein of rabbitpox virus. Virology. 1995;206:591–600. doi: 10.1016/S0042-6822(95)80076-X. [DOI] [PubMed] [Google Scholar]
- Mckenzie R, Kotwal G J, Moss B, Hammer C H, Frank M M. Regulation of complement activity by vaccinia virus complement-control protein. J. Infect. Dis. 1992;166:1245–1250. doi: 10.1093/infdis/166.6.1245. [DOI] [PubMed] [Google Scholar]
- McNearney T A, Odell C, Holers V M, Spear P G, Atkinson J P. Herpes simplex virus glycoproteins gC-1 and gC-2 bind to the third component of complement and provide protection against complement-mediated neutralization of viral infectivity. J. Exp. Med. 1987;166:1525–1535. doi: 10.1084/jem.166.5.1525. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McSharry J J, Pickering R J, Caliguiri L A. Activation of the alternative complement pathway by enveloped viruses containing limited amounts of sialic acid. Virology. 1981;114:507–515. doi: 10.1016/0042-6822(81)90230-0. [DOI] [PubMed] [Google Scholar]
- Miller C G, Shchelkunov S N, Kotwal G J. The cow-pox virus-encoded homolog of the vaccinia virus complement control protein is an inflammation modulatory protein. Virology. 1997;229:126–133. doi: 10.1006/viro.1996.8396. [DOI] [PubMed] [Google Scholar]
- Mold C, Bradt B M, Nemerow G R, Cooper N R. Activation of the alternative complement pathway by EBV and the viral envelope glycoprotein, gp350. J. Immunol. 1988a;140:3867–3874. [PubMed] [Google Scholar]
- Mold C, Bradt B M, Nemerow G R, Cooper N R. Epstein-Barr virus regulates activation and processing of the third component of complement. J. Exp. Med. 1988b;168:949–969. doi: 10.1084/jem.168.3.949. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Molina H, Brenner C, Jacobi S, Gorka J, Carel J C, Kinoshita T, Holers V M. Analysis of Epstein-Barr virus-binding sites on complement receptor 2 (CR2/CD21) using human-mouse chimeras and peptides. At least two distinct sites are necessary for ligand-receptor interaction. J. Biol. Chem. 1991;266:12173–12179. [PubMed] [Google Scholar]
- Montefiori D C, Cornell R J, Zhou J Y, Zhou J T, Hirsch V M, Johnson P R. Complement control proteins, CD46, CD55, and CD59, as common surface constituents of human and simian immunodeficiency viruses and possible targets for vaccine protection. Virology. 1994;205:82–92. doi: 10.1006/viro.1994.1622. [DOI] [PubMed] [Google Scholar]
- Morgan B P. Regulation of the complement membrane attack pathway. Crit. Rev. Immunol. 1999;19:173–198. doi: 10.1615/CritRevImmunol.v19.i3.10. [DOI] [PubMed] [Google Scholar]
- Murthy K H, Smith S A, Ganesh V K, Judge K W, Mullin N, Barlow P N, Ogata C M, Kotwal G J. Crystal structure of a complement control protein that regulates both pathways of complement activation and binds heparan sulfate proteoglycans. Cell. 2001;104:301–311. doi: 10.1016/S0092-8674(01)00214-8. [DOI] [PubMed] [Google Scholar]
- Naniche D, Variorkrishnan G, Cervoni F, Wild T F, Rossi B, Rabourdincombe C, Gerlier D. Human membrane cofactor protein (CD46) acts as a cellular receptor for measles virus. J. Virol. 1993;67:6025–6032. doi: 10.1128/jvi.67.10.6025-6032.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nemerow G R, Cooper N R. Isolation of Epstein Barr-virus and studies of its neutralization by human IgG and complement. J. Immunol. 1981;127:272–278. [PubMed] [Google Scholar]
- Nemerow G R, Houghten R A, Moore M D, Cooper N R. Identification of an epitope in the major envelope protein of Epstein-Barr virus that mediates viral binding to the B lymphocyte EBV receptor (CR2) Cell. 1989;56:369–377. doi: 10.1016/0092-8674(89)90240-7. [DOI] [PubMed] [Google Scholar]
- Nemerow G R, Mold C, Schwend V K, Tollefson V, Cooper N R. Identification of gp350 as the viral glycoprotein mediating attachment of Epstein-Barr virus (EBV) to the EBV/C3d receptor of B cells: sequence homology of gp350 and C3 complement fragment C3d. J. Virol. 1987;61:1416–1420. doi: 10.1128/jvi.61.5.1416-1420.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nonaka M, Azumi K, Ji X, Namikawa-Yamada C, Sasaki M, Saiga H, Dodds A W, Sekine H, Homma M K, Matsushita M, Endo Y, Fujita T. Opsonic complement component C3 in the solitary ascidian,Halocynthia roretzi. J. Immunol. 1999;162:387–391. [PubMed] [Google Scholar]
- Nussbaum O, Broder C C, Moss B, Stern L B, Rozenblatt S, Berger E A. Functional and structural interactions between measles virus hemagglutinin and CD46. J. Virol. 1995;69:3341–3349. doi: 10.1128/jvi.69.6.3341-3349.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Oldstone M B, Cooper N R, Larson D L. Formation and biologic role of polyoma virus-antibody complexes. A critical role for complement. J. Exp. Med. 1974;140:549–565. doi: 10.1084/jem.140.2.549. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pinter C, Siccardi A G, Longhi R, Clivio A. Direct interaction of complement factor H with the C1 domain of HIV type 1 glycoprotein 120. AIDS Res. Hum. Retroviruses. 1995a;11:577–588. doi: 10.1089/aid.1995.11.577. [DOI] [PubMed] [Google Scholar]
- Pinter C, Siccardi A G, Lopalco L, Longhi R, Clivio A. HIV glycoprotein 41 and complement factor H interact with each other and share functional as well as antigenic homology. AIDS Res. Hum. Retroviruses. 1995b;11:971–980. doi: 10.1089/aid.1995.11.971. [DOI] [PubMed] [Google Scholar]
- Powell R M, Ward T, Evans D J, Almond J W. Interaction between echovirus 7 and its receptor, decay-accelerating factor (CD55): evidence for a secondary cellular factor in A-particle formation. J. Virol. 1997;71:9306–9312. doi: 10.1128/jvi.71.12.9306-9312.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Prodeus A P, Goerg S, Shen L M, Pozdnyakova O O, Chu L, Alicot E M, Goodnow C C, Carroll M C. A critical role for complement in maintenance of self-tolerance. Immunity. 1998;9:721–731. doi: 10.1016/S1074-7613(00)80669-X. [DOI] [PubMed] [Google Scholar]
- Robinson W E Jr, Montefiori D C, Mitchell W M. Antibody-dependent enhancement of human immunodeficiency virus type 1 infection. Lancet. 1988;1:790–794. doi: 10.1016/S0140-6736(88)91657-1. [DOI] [PubMed] [Google Scholar]
- Rosengard A M, Ahearn J M. Creation and functional characterization of spice, the small pox inhibitor of complement enzymes. Mol. Immunol. 1998;35:397–397. doi: 10.1016/S0161-5890(98)90799-4. [DOI] [Google Scholar]
- Rosengard A M, Alonso L C, Korb L C, Baldwin W M, Sanfilippo F, Turka L A, Ahearn J M. Functional characterization of soluble and membrane-bound forms of vaccinia virus complement control protein (VCP) Mol. Immunol. 1999;36:685–697. doi: 10.1016/S0161-5890(99)00081-4. [DOI] [PubMed] [Google Scholar]
- Rother R P, Rollins S A, Fodor W L, Albrecht J C, Setter E, Fleckenstein B, Squinto S P. Inhibition of complement-mediated cytolysis by the terminal complement inhibitor of herpesvirus saimiri. J. Virol. 1994;68:730–737. doi: 10.1128/jvi.68.2.730-737.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Russo J J, Bohenzky R A, Chien M C, Chen J, Yan M, Maddalena D, Parry J P, Peruzzi D, Edelman I S, Chang Y, Moore P S. Nucleotide sequence of the Kaposi sarcoma-associated herpesvirus (HHV8) Proc. Natl. Acad. Sci. USA. 1996;93:14862–14867. doi: 10.1073/pnas.93.25.14862. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rux A H, Moore W T, Lambris J D, Abrams W R, Peng C, Friedman H M, Cohen G H, Eisenberg R J. Disulfide bond structure determination and biochemical analysis of glycoprotein C from herpes simplex virus. J. Virol. 1996;70:5455–5465. doi: 10.1128/jvi.70.8.5455-5465.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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. 1998b;160:5596–5604. [PubMed] [Google Scholar]
- Sahu A, Kozel T R, Pangburn M K. Specificity of the thioester-containing reactive site of human C3 and its significance to complement activation. Biochem. J. 1994;302:429–436. doi: 10.1042/bj3020429. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sahu A, Lambris J D. Complement inhibitors: a resurgent concept in anti-inflammatory therapeutics. Immunopharmacology. 2000;49:133–148. doi: 10.1016/S0162-3109(00)80299-4. [DOI] [PubMed] [Google Scholar]
- Sahu A, Lambris J D. Structure and biology of complement protein C3, a connecting link between innate and acquired immunity. Immunol. Rev. 2001;180:35–48. doi: 10.1034/j.1600-065X.2001.1800103.x. [DOI] [PubMed] [Google Scholar]
- Sahu A, Morikis D, Lambris J D. Complement inhibitors targeting C3, C4, and C5. In: Lambris J D, Holers V M, editors. Therapeutic interventions in the complement system. Totowa: Humana Press; 2000. pp. 75–112. [Google Scholar]
- Sahu A, Pangburn M K. Identification of multiple sites of interaction between heparin and the complement system. Mol. Immunol. 1993;30:679–684. doi: 10.1016/0161-5890(93)90079-Q. [DOI] [PubMed] [Google Scholar]
- Sahu A, Pangburn M K. Covalent attachment of human complement C3 to IgG: Identification of the amino acid residue involved in ester linkage formation. J. Biol. Chem. 1994;269:28997–29002. [PubMed] [Google Scholar]
- Sahu A, Pangburn M K. Tyrosine is a potential site for covalent attachment of activated commplement component C3. Mol. Immunol. 1995;32:711–716. doi: 10.1016/0161-5890(95)98933-F. [DOI] [PubMed] [Google Scholar]
- Sahu A, Sunyer J O, Moore W T, Sarrias M R, Soulika A M, Lambris J D. Structure, functions, and evolution of the third complement component and viral molecular mimicry. Immunol. Res. 1998a;17:109–121. doi: 10.1007/BF02786436. [DOI] [PubMed] [Google Scholar]
- Saifuddin M, Hart M L, Gewurz H, Zhang Y, Spear G T. Interaction of mannose-binding lectin with primary isolates of human immunodeficiency virus type 1. J. Gen. Virol. 2000;81:949–955. doi: 10.1099/0022-1317-81-4-949. [DOI] [PubMed] [Google Scholar]
- Saifuddin M, Parker C J, Peeples M E, Gorny M K, Zolla-Pazner S, Ghassemi M, Rooney I A, Atkinson J P, Spear G T. Role of virion-associated glycosylphosphatidy-linositol-linked proteins CD55 and CD59 in complement resistance of cell line-derived and primary isolates of HIV-1. J. Exp. Med. 1995;182:501–509. doi: 10.1084/jem.182.2.501. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Santoro F, Kennedy P E, Locatelli G, Malnati M S, Berger E A, Lusso P. CD46 is a cellular receptor for human herpesvirus 6. Cell. 1999;99:817–827. doi: 10.1016/S0092-8674(00)81678-5. [DOI] [PubMed] [Google Scholar]
- Sarrias M R, Franchini S, Canziani G, Argyropoulos E, Moore W T, Sahu A, Lambris J D. Kinetic analysis of the interactions of complement receptor 2 (CR2, CD21) with its ligands C3d, iC3b, and the EBV glycoprotein gp350/220. J. Immunol. 2001;167:1490–1499. doi: 10.4049/jimmunol.167.3.1490. [DOI] [PubMed] [Google Scholar]
- Schmitz J, Zimmer J P, Kluxen B, Aries S, Bogel M, Gigli I, Schmitz H. Antibody-dependent complement-mediated cytotoxicity in sera from patients with HIV-1 infection is controlled by CD55 and CD59. J. Clin. Invest. 1995;96:1520–1526. doi: 10.1172/JCI118190. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schwarting R, Stein H, Wang C Y. The monoclonal antibodies αS-HCL 1 (αLeu-14) and αS-HCL 3 (αLeu-M5) allow the diagnosis of hairy cell leukemia. Blood. 1985;65:974–983. [PubMed] [Google Scholar]
- Seidel-Dugan C, Ponce de Leon M, Friedman H M, Eisenberg R J, Cohen G H. Identification of C3b-binding regions on herpes simplex virus type 2 glycoprotein C. J. Virol. 1990;64:1897–1906. doi: 10.1128/jvi.64.5.1897-1906.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sekine H, Kenjo A, Azumi K, Ohi G, Takahashi M, Kasukawa R, Ichikawa N, Nakata M, Mizuochi T, Matsushita M, Endo Y, Fujita T. An ancient lectin-dependent complement system in an ascidian: novel lectin isolated from the plasma of the solitary ascidian,Halocynthia roretzi. J. Immunol. 2001;167:4504–4510. doi: 10.4049/jimmunol.167.8.4504. [DOI] [PubMed] [Google Scholar]
- Shafren D R, Bates R C, Agrez M V, Herd R L, Burns G F, Barry R D. Coxsackieviruses B1, B3, and B5 use decay accelerating factor as a receptor for cell attachment. J. Virol. 1995;69:3873–3877. doi: 10.1128/jvi.69.6.3873-3877.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shafren D R, Dorahy D J, Ingham R A, Burns G F, Barry R D. Coxsackievirus A21 binds to decay-accelerating factor but requires intercellular adhesion molecule 1 for cell entry. J. Virol. 1997a;71:4736–4743. doi: 10.1128/jvi.71.6.4736-4743.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shafren D R, Williams D T, Barry R D. A decayaccelerating factor-binding strain of coxsackievirus B3 requires the coxsackievirus-adenovirus receptor protein to mediate lytic infection of rhabdomyosarcoma cells. J. Virol. 1997b;71:9844–9848. doi: 10.1128/jvi.71.12.9844-9848.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sharma A K, Pangburn M K. Identification of three physically and functionally distinct binding sites for C3b in human complement factor H by deletion mutagenesis. Proc. Natl. Acad. Sci. USA. 1996;93:10996–11001. doi: 10.1073/pnas.93.20.10996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Spear G T, Hart M, Olinger G G, Hashemi F B, Saifuddin M. The role of the complement system in virus infections. Curr. Top. Microbiol. Immunol. 2001;260:229–245. doi: 10.1007/978-3-662-05783-4_12. [DOI] [PubMed] [Google Scholar]
- Spear G T, Lurain N S, Parker C J, Ghassemi M, Payne G H, Saifuddin M. Host cell-derived complement control proteins CD55 and CD59 are incorporated into the virions of two unrelated enveloped viruses. Human T cell leukemia/lymphoma virus type I (HTLV-I) and human cytomegalovirus (HCMV) J. Immunol. 1995;155:4376–4381. [PubMed] [Google Scholar]
- Spear G T, Sullivan B L, Takefman D M, Landay A L, Lint T F. Human immunodeficiency virus (HIV)-infected cells and free virus directly activate the classical complement pathway in rabbit, mouse and guinea-pig sera; activation results in virus neutralization by virolysis. Immunology. 1991;73:377–382. [PMC free article] [PubMed] [Google Scholar]
- Spear P G. Antigenic structure of herpes simplex viruses. In: Regenmortel M V H van, Neurath A R., editors. Immunochemistry of viruses. The basis for serodiagnosis and vaccines. Amsterdam: Elsevier Science Publishers; 1985. pp. 425–446. [Google Scholar]
- Stoiber H, Clivio A, Dierich M P. Role of complement in HIV infection. Annu. Rev. Immunol. 1997;15:649–674. doi: 10.1146/annurev.immunol.15.1.649. [DOI] [PubMed] [Google Scholar]
- Stoiber H, Kacani L, Speth C, Wurzner R, Dierich M P. The supportive role of complement in HIV pathogenesis. Immunol. Rev. 2001;180:168–176. doi: 10.1034/j.1600-065X.2001.1800115.x. [DOI] [PubMed] [Google Scholar]
- Stoiber H, Pinter C, Siccardi A G, Clivio A, Dierich M P. Efficient destruction of human immunodeficiency virus in human serum by inhibiting the protective action of complement factor H and decay accelerating factor (DAF, CD55) J. Exp. Med. 1996;183:307–310. doi: 10.1084/jem.183.1.307. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stoiber H, Schneider R, Janatova J, Dierich M P. Human complement proteins C3b, C4b, factor H and properdin react with specific sites in gp120 and gp41, the envelope proteins of HIV-1. Immunobiology. 1995;193:98–113. doi: 10.1016/S0171-2985(11)80158-0. [DOI] [PubMed] [Google Scholar]
- Sullivan B L, Takefman D M, Spear G T. Complement can neutralize HIV-1 plasma virus by a C5-independent mechanism. Virology. 1998;248:173–181. doi: 10.1006/viro.1998.9289. [DOI] [PubMed] [Google Scholar]
- Sun X, Funk C D, Deng C, Sahu A, Lambris J D, Song W C. Role of decay-accelerating factor in regulating complement activation on the erythrocyte surface as revealed by gene targeting. Proc. Natl. Acad. Sci. USA. 1999;96:628–633. doi: 10.1073/pnas.96.2.628. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Susal C, Kirschfink M, Kropelin M, Daniel V, Opelz G. Complement activation by recombinant HIV-1 glycoprotein gp120. J. Immunol. 1994;152:6028–6034. [PubMed] [Google Scholar]
- Swain M A, Peet R W, Galloway D A. Characterization of the gene encoding herpes simplex virus type 2 glycoprotein C and comparison with the type 1 counterpart. J. Virol. 1985;53:561–569. doi: 10.1128/jvi.53.2.561-569.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Takahashi-Nishimaki F, Funahashi S, Miki K, Hashizume S, Sugimoto M. Regulation of plaque size and host range by a vaccinia virus gene related to complement system proteins. Virology. 1991;181:158–164. doi: 10.1016/0042-6822(91)90480-Y. [DOI] [PubMed] [Google Scholar]
- Tanner J, Weis J, Fearon D, Whang Y, Kieff E. Epstein-Barr virus gp350/220 binding to the B lymphocyte C3d receptor mediates adsorption, capping, and endocytosis. Cell. 1987;50:203–213. doi: 10.1016/0092-8674(87)90216-9. [DOI] [PubMed] [Google Scholar]
- Tanner J, Whang Y, Sample J, Sears A, Kieff E. Soluble gp350/220 and deletion mutant glycoprotein block Epstein-Barr virus adsorption to lymphocytes. J. Virol. 1988;62:4452–4464. doi: 10.1128/jvi.62.12.4452-4464.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Van Strijp J A, Miltenburg L A, vander Tol M E, Van Kessel K P, Fluit A C, Verhoef J. Degradation of herpes simplex virions by human polymorphonuclear leukocytes and monocytes. J. Gen. Virol. 1990;71:1205–1209. doi: 10.1099/0022-1317-71-5-1205. [DOI] [PubMed] [Google Scholar]
- Vanderplasschen A, Mathew E, Hollinshead M, Sim R B, Smith G L. Extracellular enveloped vaccinia virus is resistant to complement because of incorporation of host complement control proteins into its envelope. Proc. Natl. Acad. Sci. USA. 1998;95:7544–7549. doi: 10.1073/pnas.95.13.7544. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Virgin H W, Latreille P, Wamsley P, Hallsworth K, Weck K E, DalCanto A J, Speck S H. Complete sequence and genomic analysis of murine gammaherpesvirus 68. J. Virol. 1997;71:5894–5904. doi: 10.1128/jvi.71.8.5894-5904.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wakimoto H, Ikeda K, Abe T, Ichikawa T, Hochberg F H, Ezekowitz R A, Pasternack M S, Chiocca E A. The complement response against an oncolytic virus is speciesspecific in its activation pathways. Mol. Ther. 2002;5:275–282. doi: 10.1006/mthe.2002.0547. [DOI] [PubMed] [Google Scholar]
- Wedgewood R J, Ginsberg H S, Pillemer H. The properdin system and immunity. VI. The inactivation of Newcastle disease virus by the properdin system. J. Exp. Med. 1956;104:707–725. doi: 10.1084/jem.104.5.707. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Welsh R M, Lampert P W, Burner P A, Oldstone M B. Antibody-complement interactions with purified lymphocytic choriomeningitis virus. Virology. 1976;73:59–71. doi: 10.1016/0042-6822(76)90060-X. [DOI] [PubMed] [Google Scholar]
- Wiles A P, Shaw G, Bright J, Perczel A, Campbell I D, Barlow P N. NMR studies of a viral protein that mimics the regulators of complement activation. J. Mol. Biol. 1997;272:253–265. doi: 10.1006/jmbi.1997.1241. [DOI] [PubMed] [Google Scholar]
- Zezulak K M, Spear P G. Mapping of the structural gene for the herpes simplex virus type 2 counterpart of herpes simplex virus type 1 glycoprotein C and identification of a type 2 mutant which does not express this glycoprotein. J. Virol. 1984;49:741–747. doi: 10.1128/jvi.49.3.741-747.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
