The OmpA family of proteins: Roles in bacterial pathogenesis and immunity

Veterinary Microbiology - Tập 163 - Trang 207-222 - 2013
Anthony W. Confer1, Sahlu Ayalew1
1Department of Veterinary Pathobiology, Oklahoma State University, McFarland & Farm Road, Stillwater, OK 74078-2007, USA

Tài liệu tham khảo

Abbott, 2010, Structure and function of the blood–brain barrier, Neurobiol. Dis., 37, 13, 10.1016/j.nbd.2009.07.030 Andrew, 2011, Partial protection against chlamydial reproductive tract infection by a recombinant major outer membrane protein/CpG/cholera toxin intranasal vaccine in the guinea pig Chlamydia caviae model, J. Reprod. Immunol., 91, 9, 10.1016/j.jri.2011.06.100 Arnold, 2004, Enhanced immunogenicity in the murine airway mucosa with an attenuated Salmonella live vaccine expressing OprF–OprI from Pseudomonas aeruginosa, Infect. Immun., 72, 6546, 10.1128/IAI.72.11.6546-6553.2004 Avadhanula, 2006, Nontypeable Haemophilus influenzae adheres to intercellular adhesion molecule 1 (ICAM-1) on respiratory epithelial cells and upregulates ICAM-1 expression, Infect. Immun., 74, 830, 10.1128/IAI.74.2.830-838.2006 Ayalew, 2010, Immunoproteomic analyses of outer membrane proteins of Mannheimia haemolytica and identification of potential vaccine candidates, Proteomics, 10, 2151, 10.1002/pmic.200900557 Ayalew, 2011, Immunogenicity of Mannheimia haemolytica recombinant outer membrane proteins serotype 1-specific antigen, OmpA, OmpP2, and OmpD15, Clin. Vaccine Immunol., 18, 2067, 10.1128/CVI.05332-11 Azghani, 2002, Pseudomonas aeruginosa outer membrane protein F is an adhesin in bacterial binding to lung epithelial cells in culture, Microb. Pathog., 33, 109, 10.1006/mpat.2002.0514 Bagos, 2004, PRED-TMBB: a web server for predicting the topology of beta-barrel outer membrane proteins, Nucleic Acids Res, 32, W400, 10.1093/nar/gkh417 Bartra, 2012, The outer membrane protein A (OmpA) of Yersinia pestis promotes intracellular survival and virulence in mice, Microb. Pathog., 52, 41, 10.1016/j.micpath.2011.09.009 Baumann, 2004, Recombinant OprF–OprI as a vaccine against Pseudomonas aeruginosa infections, Vaccine, 22, 840, 10.1016/j.vaccine.2003.11.029 Belaaouaj, 2000, Degradation of outer membrane protein A in Escherichia coli killing by neutrophil elastase, Science, 289, 1185, 10.1126/science.289.5482.1185 Bermudez-Fajardo, 2011, The effect of Chlamydophila pneumoniae major outer membrane protein (MOMP) on macrophage and T cell-mediated immune responses, Immunobiology, 216, 152, 10.1016/j.imbio.2010.06.004 Bertot, 2007, Nasal immunization with Burkholderia multivorans outer membrane proteins and the mucosal adjuvant adamantylamide dipeptide confers efficient protection against experimental lung infections with B. multivorans and B. cenocepacia, Infect. Immun., 75, 2740, 10.1128/IAI.01668-06 Bosshart, 2012, The transmembrane protein KpOmpA anchoring the outer membrane of Klebsiella pneumoniae unfolds and refolds in response to tensile load, Structure, 20, 121, 10.1016/j.str.2011.11.002 Brennan, 1999, Pseudomonas aeruginosa outer-membrane protein F epitopes are highly immunogenic in mice when expressed on a plant virus, Microbiology, 145, 211, 10.1099/13500872-145-1-211 Brown, 1989, The antibody response to salmonellae in mice and humans studied by immunoblots and ELISA, Microb. Pathog., 6, 445, 10.1016/0882-4010(89)90086-7 Cai, 2009, Biophysical and stabilization studies of the Chlamydia trachomatis mouse pneumonitis major outer membrane protein, Mol. Pharm., 6, 1553, 10.1021/mp900110q Calderwood, 2006, Heat shock proteins in cancer: chaperones of tumorigenesis, Trends Biochem. Sci., 31, 164, 10.1016/j.tibs.2006.01.006 Chai, 1977, Purification of protein A, an outer membrane component missing in Escherichia coli K-12 ompA mutants, Biochim. Biophys. Acta, 493, 210, 10.1016/0005-2795(77)90274-4 Chalifour, 2004, Direct bacterial protein PAMP recognition by human NK cells involves TLRs and triggers alpha-defensin production, Blood, 104, 1778, 10.1182/blood-2003-08-2820 Chart, 1991, Antibodies to lipopolysaccharide and outer membrane proteins of Salmonella enteritidis PT4 are not involved in protection from experimental infection, FEMS Microbiol. Lett., 68, 345, 10.1111/j.1574-6968.1991.tb04621.x Chenu, 2009, Cronobacter (‘Enterobacter sakazakii’): current status and future prospects, Lett. Appl. Microbiol., 49, 153, 10.1111/j.1472-765X.2009.02651.x Choi, 2005, Outer membrane protein 38 of Acinetobacter baumannii localizes to the mitochondria and induces apoptosis of epithelial cells, Cell. Microbiol., 7, 1127, 10.1111/j.1462-5822.2005.00538.x Cripps, 1995, Immunity to Pseudomonas aeruginosa induced by OprF following intestinal immunization, Adv. Exp. Med. Biol., 371B, 761 Dabo, 2008, Vaccination with Pasteurella multocida recombinant OmpA induces strong but non-protective and deleterious Th2-type immune response in mice, Vaccine, 26, 4345, 10.1016/j.vaccine.2008.06.029 Dabo, 1997, Outer membrane proteins of bovine Pasteurella multocida serogroup A isolates, Vet. Microbiol., 54, 167, 10.1016/S0378-1135(96)01274-6 Dabo, 2003, Molecular and immunological characterization of Pasteurella multocida serotype A:3 OmpA: evidence of its role in P. multocida interaction with extracellular matrix molecules, Microb. Pathog., 35, 147, 10.1016/S0882-4010(03)00098-6 Dabo, 1994, Expression, purification and immunologic analysis of three Pasteurella haemolytica A1 28–30kDa lipoproteins, Microb. Pathog., 17, 149, 10.1006/mpat.1994.1061 Danoff, 2011, The soluble, periplasmic domain of OmpA folds as an independent unit and displays chaperone activity by reducing the self-association propensity of the unfolded OmpA transmembrane beta-barrel, Biophys. Chem., 159, 194, 10.1016/j.bpc.2011.06.013 Datta, 2003, Interaction of E. coli outer-membrane protein A with sugars on the receptors of the brain microvascular endothelial cells, Proteins, 50, 213, 10.1002/prot.10257 Davies, 1993, The expression of the adhesion molecules ICAM-1, VCAM-1, PECAM, and E-selectin in human atherosclerosis, J. Pathol., 171, 223, 10.1002/path.1711710311 Dhakal, 2008, Mechanisms and consequences of bladder cell invasion by uropathogenic Escherichia coli, Eur. J. Clin. Invest., 38, 2, 10.1111/j.1365-2362.2008.01986.x Dumetz, 2007, The Flavobacterium psychrophilum OmpA, an outer membrane glycoprotein, induces a humoral response in rainbow trout, J. Appl. Microbiol., 103, 1461, 10.1111/j.1365-2672.2007.03359.x Ewers, 2007, Avian pathogenic, uropathogenic, and newborn meningitis-causing Escherichia coli: how closely related are they?, Int. J. Med. Microbiol., 297, 163, 10.1016/j.ijmm.2007.01.003 Farina, 2007, Astrocytes are active players in cerebral innate immunity, Trends Immunol., 28, 138, 10.1016/j.it.2007.01.005 Farris, 2011, Vaccination against Chlamydia genital infection utilizing the murine C. muridarum model, Infect. Immun., 79, 986, 10.1128/IAI.00881-10 Farris, 2010, CD4+ T cells and antibody are required for optimal major outer membrane protein vaccine-induced immunity to Chlamydia muridarum genital infection, Infect. Immun., 78, 4374, 10.1128/IAI.00622-10 Findlay, 2005, Surface expression, single-channel analysis and membrane topology of recombinant Chlamydia trachomatis major outer membrane protein, BMC Microbiol., 5, 5, 10.1186/1471-2180-5-5 Foulds, 1978, Defeat of colicin tolerance in Escherichia coli ompA mutants: evidence for interaction between colicin L-JF246 and the cytoplasmic membrane, J. Bacteriol., 133, 158, 10.1128/JB.133.1.158-164.1978 Freudl, 1986, Cell surface exposure of the outer membrane protein OmpA of Escherichia coli K-12, J. Mol. Biol., 188, 491, 10.1016/0022-2836(86)90171-3 Fu, 2003, Outer membrane protein A deficient Escherichia coli activates neutrophils to produce superoxide and shows increased susceptibility to antibacterial peptides, Microbes Infect., 5, 781, 10.1016/S1286-4579(03)00145-X Fuller, 2000, Identification of Actinobacillus pleuropneumoniae virulence genes using signature-tagged mutagenesis in a swine infection model, Microb. Pathog., 29, 39, 10.1006/mpat.2000.0364 Gatto, 2002, Characterization of, and immune responses of mice to, the purified OmpA-equivalent outer membrane protein of Pasteurella multocida serotype A:3 (Omp28), Vet. Microbiol., 87, 221, 10.1016/S0378-1135(02)00068-8 Gilleland, 1993, Vaccine efficacies of elastase, exotoxin A, and outer-membrane protein F in preventing chronic pulmonary infection by Pseudomonas aeruginosa in a rat model, J. Med. Microbiol., 38, 79, 10.1099/00222615-38-2-79 Gilleland, 1988, Outer membrane protein F preparation of Pseudomonas aeruginosa as a vaccine against chronic pulmonary infection with heterologous immunotype strains in a rat model, Infect. Immun., 56, 1017, 10.1128/IAI.56.5.1017-1022.1988 Gilleland, 1984, Use of a purified outer membrane protein F (porin) preparation of Pseudomonas aeruginosa as a protective vaccine in mice, Infect. Immun., 44, 49, 10.1128/IAI.44.1.49-54.1984 Gophna, 2004, OmpA of a septicemic Escherichia coli O78—secretion and convergent evolution, Int. J. Med. Microbiol., 294, 373, 10.1016/j.ijmm.2004.08.004 Grizot, 2004, Structure of the OmpA-like domain of RmpM from Neisseria meningitidis, Mol. Microbiol., 51, 1027, 10.1111/j.1365-2958.2003.03903.x Gruenheid, 2012, Resistance to antimicrobial peptides in Gram-negative bacteria, FEMS Microbiol. Lett., 330, 81, 10.1111/j.1574-6968.2012.02528.x Hari-Dass, 2005, Serum amyloid A protein binds to outer membrane protein A of Gram-negative bacteria, J. Biol. Chem., 280, 18562, 10.1074/jbc.M500490200 Harkinezhad, 2009, Protection of budgerigars (Melopsittacus undulatus) against Chlamydophila psittaci challenge by DNA vaccination, Vet. Res., 40, 61, 10.1051/vetres/2009044 Hickey, 2004, Intranasal immunization with C. muridarum major outer membrane protein (MOMP) and cholera toxin elicits local production of neutralising IgA in the prostate, Vaccine, 22, 4306, 10.1016/j.vaccine.2004.04.021 Hong, 2006, Electrostatic couplings in OmpA ion-channel gating suggest a mechanism for pore opening, Nat. Chem. Biol., 2, 627, 10.1038/nchembio827 Hounsome, 2011, Outer membrane protein A of bovine and ovine isolates of Mannheimia haemolytica is surface exposed and contains host species-specific epitopes, Infect. Immun., 79, 4332, 10.1128/IAI.05469-11 Hu, 2012, Immunoproteomics analysis of whole cell bacterial proteins of Riemerella anatipestifer, Vet. Microbiol., 157, 428, 10.1016/j.vetmic.2012.01.009 Huang, 2002, Vaccination of ducks with recombinant outer membrane protein (OmpA) and a 41kDa partial protein (P45N′) of Riemerella anatipestifer, Vet. Microbiol., 84, 219, 10.1016/S0378-1135(01)00456-4 Hughes, 1995, Ability of synthetic peptides representing epitopes of outer membrane protein F of Pseudomonas aeruginosa to afford protection against P. aeruginosa infection in a murine acute pneumonia model, Vaccine, 13, 1750, 10.1016/0264-410X(95)00166-X Igietseme, 2000, Induction of protective immunity against Chlamydia trachomatis genital infection by a vaccine based on major outer membrane protein-lipophilic immune response-stimulating complexes, Infect. Immun., 68, 6798, 10.1128/IAI.68.12.6798-6806.2000 Jang, 2011, Dendritic cells stimulated with outer membrane protein A (OmpA) of Salmonella typhimurium generate effective anti-tumor immunity, Vaccine, 29, 2400, 10.1016/j.vaccine.2011.01.036 Jin, 2000, Intestinal receptors for adhesive fimbriae of enterotoxigenic Escherichia coli (ETEC) K88 in swine—a review, Appl. Microbiol. Biotechnol., 54, 311, 10.1007/s002530000404 Kajiya, 2011, Aggregatibacter actinomycetemcomitans Omp29 is associated with bacterial entry to gingival epithelial cells by F-actin rearrangement, PLoS ONE, 6, e18287, 10.1371/journal.pone.0018287 Kari, 2009, Chlamydia trachomatis native major outer membrane protein induces partial protection in nonhuman primates: implication for a trachoma transmission-blocking vaccine, J. Immunol., 182, 8063, 10.4049/jimmunol.0804375 Kennedy, 2000, Passive transfer of antiserum specific for immunogens derived from a nontypeable Haemophilus influenzae adhesin and lipoprotein D prevents otitis media after heterologous challenge, Infect. Immun., 68, 2756, 10.1128/IAI.68.5.2756-2765.2000 Kese, 2011, Genotyping of Chlamydia trachomatis directly from urogenital and conjunctiva samples using an ompA gene pyrosequencing-based assay, FEMS Immunol. Med. Microbiol., 63, 210, 10.1111/j.1574-695X.2011.00843.x Khalid, 2008, OmpA: gating and dynamics via molecular dynamics simulations, Biochim. Biophys. Acta, 1778, 1871, 10.1016/j.bbamem.2007.05.024 Kim, 2010, Outer membrane proteins A (OmpA) and X (OmpX) are essential for basolateral invasion of Cronobacter sakazakii, Appl. Environ. Microbiol., 76, 5188, 10.1128/AEM.02498-09 Kim, 2003, The K1 capsule modulates trafficking of E. coli-containing vacuoles and enhances intracellular bacterial survival in human brain microvascular endothelial cells, Cell. Microbiol., 5, 245, 10.1046/j.1462-5822.2003.t01-1-00271.x Kim, 2009, Serum resistance of Acinetobacter baumannii through the binding of factor H to outer membrane proteins, FEMS Microbiol. Lett., 301, 224, 10.1111/j.1574-6968.2009.01820.x Kisiela, 2009, Identification of Mannheimia haemolytica adhesins involved in binding to bovine bronchial epithelial cells, Infect. Immun., 77, 446, 10.1128/IAI.00312-08 Kleinschmidt, 2003, Membrane protein folding on the example of outer membrane protein A of Escherichia coli, Cell. Mol. Life Sci., 60, 1547, 10.1007/s00018-003-3170-0 Klimke, 2005, The mating pair stabilization protein, TraN, of the F plasmid is an outer-membrane protein with two regions that are important for its function in conjugation, Microbiology, 151, 3527, 10.1099/mic.0.28025-0 Koebnik, 1999, Membrane assembly of the Escherichia coli outer membrane protein OmpA: exploring sequence constraints on transmembrane beta-strands, J. Mol. Biol., 285, 1801, 10.1006/jmbi.1998.2405 Koebnik, 1999, Structural and functional roles of the surface-exposed loops of the beta-barrel membrane protein OmpA from Escherichia coli, J. Bacteriol., 181, 3688, 10.1128/JB.181.12.3688-3694.1999 Koebnik, 2000, Structure and function of bacterial outer membrane proteins: barrels in a nutshell, Mol. Microbiol., 37, 239, 10.1046/j.1365-2958.2000.01983.x Krause, 2011, Protective anti-Pseudomonas aeruginosa humoral and cellular mucosal immunity by AdC7-mediated expression of the P. aeruginosa protein OprF, Vaccine, 29, 2131, 10.1016/j.vaccine.2010.12.087 Krishnan, 2012, Outer membrane protein A and OprF – versatile roles in Gram-negative bacterial infections, FEBS J., 279, 919, 10.1111/j.1742-4658.2012.08482.x Krull, 2006, Mechanisms of Chlamydophila pneumoniae-mediated GM-CSF release in human bronchial epithelial cells, Am. J. Respir. Cell Mol. Biol., 34, 375, 10.1165/rcmb.2004-0157OC Kurupati, 2011, Protective efficacy of DNA vaccines encoding outer membrane protein A and OmpK36 of Klebsiella pneumoniae in mice, Clin. Vac. Immunol., 18, 82, 10.1128/CVI.00275-10 Kyd, 2003, Efficacy of the 26-kilodalton outer membrane protein and two P5 fimbrin-derived immunogens to induce clearance of nontypeable Haemophilus influenzae from the rat middle ear and lungs as well as from the chinchilla middle ear and nasopharynx, Infect. Immun., 71, 4691, 10.1128/IAI.71.8.4691-4699.2003 Lee, 2010, Outer membrane protein a of Salmonella enterica serovar Typhimurium activates dendritic cells and enhances Th1 polarization, BMC Microbiol., 10, 263, 10.1186/1471-2180-10-263 Liebner, 2011, Current concepts of blood–brain barrier development, Int. J. Dev. Biol., 55, 467, 10.1387/ijdb.103224sl Llobet, 2009, Klebsiella pneumoniae OmpA confers resistance to antimicrobial peptides, Antimicrob. Agents Chemother., 53, 298, 10.1128/AAC.00657-08 Lo, 2007, The outer membrane protein OmpA of Mannheimia haemolytica A1 is involved in the binding of fibronectin, FEMS Microbiol. Lett., 274, 226, 10.1111/j.1574-6968.2007.00830.x Mahasreshti, 1997, Purification and partial characterization of the OmpA family of proteins of Pasteurella haemolytica, Infect. Immun., 65, 211, 10.1128/IAI.65.1.211-218.1997 Makidon, 2010, Induction of immune response to the 17 kDa OMPA Burkholderia cenocepacia polypeptide and protection against pulmonary infection in mice after nasal vaccination with an OMP nanoemulsion-based vaccine, Med. Microbiol. Immunol. (Berl), 199, 81, 10.1007/s00430-009-0137-2 Mansouri, 2003, Clinical study to assess the immunogenicity and safety of a recombinant Pseudomonas aeruginosa OprF-OprI vaccine in burn patients, FEMS Immunol. Med. Microbiol., 37, 161, 10.1016/S0928-8244(03)00072-5 March, 2011, Klebsiella pneumoniae outer membrane protein A is required to prevent the activation of airway epithelial cells, J. Biol. Chem., 286, 9956, 10.1074/jbc.M110.181008 Masuda, 2006, Effects of various growth conditions in a chemostat on expression of virulence factors in Porphyromonas gingivalis, Appl. Environ. Microbiol., 72, 3458, 10.1128/AEM.72.5.3458-3467.2006 McConnell, 2012, Acinetobacter baumannii: human infections, factors contributing to pathogenesis and animal models, FEMS Microbiol. Rev., 10.1111/j.1574-6976.2012.00344.x Meier, 1996, Ability of Escherichia coli isolates that cause meningitis in newborns to invade epithelial and endothelial cells, Infect. Immun., 64, 2391, 10.1128/IAI.64.7.2391-2399.1996 Meyer-Hoffert, 2011, Neutrophil serine proteases: mediators of innate immune responses, Curr. Opin. Hematol., 18, 19, 10.1097/MOH.0b013e32834115d1 Mittal, 2009, Enterobacter sakazakii targets DC-SIGN to induce immunosuppressive responses in dendritic cells by modulating MAPKs, J. Immunol., 183, 6588, 10.4049/jimmunol.0902029 Mittal, 2009, Brain damage in newborn rat model of meningitis by Enterobacter sakazakii: a role for outer membrane protein A, Lab. Invest., 89, 263, 10.1038/labinvest.2008.164 Miyamoto, 1996, Selective adherence of non-typeable Haemophilus influenzae (NTHi) to mucus or epithelial cells in the chinchilla eustachian tube and middle ear, Microb. Pathog., 21, 343, 10.1006/mpat.1996.0067 Munkley, 1991, Blocking of bactericidal killing of Neisseria meningitidis by antibodies directed against class 4 outer membrane protein, Microb. Pathog., 11, 447, 10.1016/0882-4010(91)90041-8 Munson, 1993, Molecular cloning and sequence of the gene for outer membrane protein P5 of Haemophilus influenzae, Infect. Immun., 61, 4017, 10.1128/IAI.61.9.4017-4020.1993 Murphy, 2002, Biofilm formation by nontypeable Haemophilus influenzae: strain variability, outer membrane antigen expression and role of pili, BMC Microbiol., 2, 7, 10.1186/1471-2180-2-7 Nair, 2009, Outer membrane protein A (OmpA) of Cronobacter sakazakii binds fibronectin and contributes to invasion of human brain microvascular endothelial cells, Foodborne Pathog. Dis., 6, 495, 10.1089/fpd.2008.0228 Nicholson, 2009, OmpA of uropathogenic Escherichia coli promotes postinvasion pathogenesis of cystitis, Infect. Immun., 77, 5245, 10.1128/IAI.00670-09 Novotny, 2003, The fourth surface-exposed region of the outer membrane protein P5-homologous adhesin of nontypable Haemophilus influenzae is an immunodominant but nonprotective decoying epitope, J. Immunol., 171, 1978, 10.4049/jimmunol.171.4.1978 Novotny, 2000, Epitope mapping of the outer membrane protein P5-homologous fimbrin adhesin of nontypeable Haemophilus influenzae, Infect. Immun., 68, 2119, 10.1128/IAI.68.4.2119-2128.2000 Novotny, 2008, Differential uptake and processing of a Haemophilus influenzae P5-derived immunogen by chinchilla dendritic cells, Infect. Immun., 76, 967, 10.1128/IAI.01395-07 Ojha, 2010, Characterization of colonization-deficient mutants of Actinobacillus suis, Vet. Microbiol., 140, 122, 10.1016/j.vetmic.2009.07.014 Oldfield, 2008, Identification and characterization of novel antigenic vaccine candidates of Actinobacillus pleuropneumoniae, Vaccine, 26, 1942, 10.1016/j.vaccine.2008.02.022 Orme, 2006, Proteomic analysis of Escherichia coli biofilms reveals the overexpression of the outer membrane protein OmpA, Proteomics, 6, 4269, 10.1002/pmic.200600193 Ortiz, 1996, Chlamydia trachomatis major outer membrane protein (MOMP) epitopes that activate HLA class II-restricted T cells from infected humans, J. Immunol., 157, 4554, 10.4049/jimmunol.157.10.4554 Pal, 1997, Immunization with an acellular vaccine consisting of the outer membrane complex of Chlamydia trachomatis induces protection against a genital challenge, Infect. Immun., 65, 3361, 10.1128/IAI.65.8.3361-3369.1997 Pal, 1997, Monoclonal immunoglobulin A antibody to the major outer membrane protein of the Chlamydia trachomatis mouse pneumonitis biovar protects mice against a chlamydial genital challenge, Vaccine, 15, 575, 10.1016/S0264-410X(97)00206-5 Park, 2012, Mechanism of anchoring of OmpA protein to the cell wall peptidoglycan of the gram-negative bacterial outer membrane, FASEB J., 26, 219, 10.1096/fj.11-188425 Patel, 2009, The periplasmic chaperone Skp facilitates targeting, insertion, and folding of OmpA into lipid membranes with a negative membrane surface potential, Biochemistry, 48, 10235, 10.1021/bi901403c Penttila, 2000, Immunity to Chlamydia pneumoniae induced by vaccination with DNA vectors expressing a cytoplasmic protein (Hsp60) or outer membrane proteins (MOMP and Omp2), Vaccine, 19, 1256, 10.1016/S0264-410X(00)00237-1 Pichavant, 2003, Outer membrane protein A from Klebsiella pneumoniae activates bronchial epithelial cells: implication in neutrophil recruitment, J. Immunol., 171, 6697, 10.4049/jimmunol.171.12.6697 Prasadarao, 2002, A novel interaction of outer membrane protein A with C4b binding protein mediates serum resistance of Escherichia coli K1, J. Immunol., 169, 6352, 10.4049/jimmunol.169.11.6352 Prasadarao, 2003, Cloning and expression of the Escherichia coli K1 outer membrane protein A receptor, a gp96 homologue, Infect. Immun., 71, 1680, 10.1128/IAI.71.4.1680-1688.2003 Prasadarao, 1996, Endothelial cell GlcNAc beta 1–4GlcNAc epitopes for outer membrane protein A enhance traversal of Escherichia coli across the blood–brain barrier, Infect. Immun., 64, 154, 10.1128/IAI.64.1.154-160.1996 Prasadarao, 1999, Outer membrane protein A-promoted actin condensation of brain microvascular endothelial cells is required for Escherichia coli invasion, Infect. Immun., 67, 5775, 10.1128/IAI.67.11.5775-5783.1999 Prasadarao, 1996, Outer membrane protein A of Escherichia coli contributes to invasion of brain microvascular endothelial cells, Infect. Immun., 64, 146, 10.1128/IAI.64.1.146-153.1996 Price, 2002, Enhancement of the protective efficacy of an oprF DNA vaccine against Pseudomonas aeruginosa, FEMS Immunol. Med. Microbiol., 33, 89, 10.1111/j.1574-695X.2002.tb00577.x Price, 2001, Protection against Pseudomonas aeruginosa chronic lung infection in mice by genetic immunization against outer membrane protein F (OprF) of P. aeruginosa, Infect. Immun., 69, 3510, 10.1128/IAI.69.5.3510-3515.2001 Qu, 2009, Binding regions of outer membrane protein A in complexes with the periplasmic chaperone Skp. A site-directed fluorescence study, Biochemistry, 48, 4926, 10.1021/bi9004039 Reusch, 2012, Biogenesis and functions of model integral outer membrane proteins: Escherichia coli OmpA and Pseudomonas aeruginosa OprF, FEBS J., 10.1111/j.1742-4658.2012.08486.x Reusch, 2012, Insights into the structure and assembly of Escherichia coli outer membrane protein A, FEBS J., 10.1111/j.1742-4658.2012.08484.x Rice, 1994, Serum resistance of Neisseria gonorrhoeae. Does it thwart the inflammatory response and facilitate the transmission of infection?, Ann. N.Y. Acad. Sci., 730, 7, 10.1111/j.1749-6632.1994.tb44234.x Ried, 1994, Membrane topology and assembly of the outer membrane protein OmpA of Escherichia coli K12, Mol. Gen. Genet., 243, 127, 10.1007/BF00280309 Ristow, 2007, The OmpA-like protein Loa22 is essential for leptospiral virulence, PLoS Pathog., 3, e97, 10.1371/journal.ppat.0030097 Rosenqvist, 1999, Functional activities and epitope specificity of human and murine antibodies against the class 4 outer membrane protein (Rmp) of Neisseria meningitidis, Infect. Immun., 67, 1267, 10.1128/IAI.67.3.1267-1276.1999 Seder, 2000, Vaccines against intracellular infections requiring cellular immunity, Nature, 406, 793, 10.1038/35021239 Selvaraj, 2007, Outer membrane protein A of Escherichia coli K1 selectively enhances the expression of intercellular adhesion molecule-1 in brain microvascular endothelial cells, Microbes. Infect., 9, 547, 10.1016/j.micinf.2007.01.020 Selvaraj, 2005, Escherichia coli K1 inhibits proinflammatory cytokine induction in monocytes by preventing NF-kappaB activation, J. Leukoc. Biol., 78, 544, 10.1189/jlb.0904516 Serino, 2007, Identification of a new OmpA-like protein in Neisseria gonorrhoeae involved in the binding to human epithelial cells and in vivo colonization, Mol. Microbiol., 64, 1391, 10.1111/j.1365-2958.2007.05745.x Shah, 2006, Serum amyloid A is an innate immune opsonin for Gram-negative bacteria, Blood, 108, 1751, 10.1182/blood-2005-11-011932 Shin, 2005, Escherichia coli outer membrane protein A adheres to human brain microvascular endothelial cells, Biochem. Biophys. Res. Commun., 330, 1199, 10.1016/j.bbrc.2005.03.097 Singamsetty, 2008, Outer membrane protein A expression in Enterobacter sakazakii is required to induce microtubule condensation in human brain microvascular endothelial cells for invasion, Microb. Pathog., 45, 181, 10.1016/j.micpath.2008.05.006 Singh, 2003, The C-terminal domain of Salmonella enterica serovar typhimurium OmpA is an immunodominant antigen in mice but appears to be only partially exposed on the bacterial cell surface, Infect. Immun., 71, 3937, 10.1128/IAI.71.7.3937-3946.2003 Singh, 2006, Mucosal immunization with recombinant MOMP genetically linked with modified cholera toxin confers protection against Chlamydia trachomatis infection, Vaccine, 24, 1213, 10.1016/j.vaccine.2005.08.097 Smith, 2007, A molecular Swiss army knife: OmpA structure, function and expression, FEMS Microbiol. Lett., 273, 1, 10.1111/j.1574-6968.2007.00778.x Staczek, 1998, A chimeric influenza virus expressing an epitope of outer membrane protein F of Pseudomonas aeruginosa affords protection against challenge with P. aeruginosa in a murine model of chronic pulmonary infection, Infect. Immun., 66, 3990, 10.1128/IAI.66.8.3990-3994.1998 Staczek, 2003, DNA vaccines against chronic lung infections by Pseudomonas aeruginosa, FEMS Immunol. Med. Microbiol., 37, 147, 10.1016/S0928-8244(03)00075-0 Starnino, 2010, Molecular analysis of two novel Neisseria gonorrhoeae virulent components: the macrophage infectivity potentiator and the outer membrane protein A, New Microbiol., 33, 167 Su, 1990, Chlamydia trachomatis–host cell interactions: role of the chlamydial major outer membrane protein as an adhesin, Infect. Immun., 58, 1017, 10.1128/IAI.58.4.1017-1025.1990 Subramaniam, 2000, Characterization of a predominant immunogenic outer membrane protein of Riemerella anatipestifer, Clin. Diagn. Lab. Immunol., 7, 168, 10.1128/CDLI.7.2.168-174.2000 Sukumaran, 2002, Escherichia coli K1 internalization via caveolae requires caveolin-1 and protein kinase Calpha interaction in human brain microvascular endothelial cells, J. Biol. Chem., 277, 50716, 10.1074/jbc.M208830200 Sukumaran, 2004, Inhibition of apoptosis by Escherichia coli K1 is accompanied by increased expression of BclXL and blockade of mitochondrial cytochrome c release in macrophages, Infect. Immun., 72, 6012, 10.1128/IAI.72.10.6012-6022.2004 Sukumaran, 2003, Entry and intracellular replication of Escherichia coli K1 in macrophages require expression of outer membrane protein A, Infect. Immun., 71, 5951, 10.1128/IAI.71.10.5951-5961.2003 Tadjine, 2004, Production and characterization of murine monoclonal antibodies against Haemophilus parasuis and study of their protective role in mice, Microbiology, 150, 3935, 10.1099/mic.0.27443-0 Tagawa, 1993, Characterization of a heat-modifiable outer membrane protein of Haemophilus somnus, Infect. Immun., 61, 1750, 10.1128/IAI.61.5.1750-1755.1993 Teng, 2006, Effects of ompA deletion on expression of type 1 fimbriae in Escherichia coli K1 strain RS218 and on the association of E. coli with human brain microvascular endothelial cells, Infect. Immun., 74, 5609, 10.1128/IAI.00321-06 Thanavala, 2011, Role of nontypeable Haemophilus influenzae in otitis media and chronic obstructive pulmonary disease, Adv. Otorhinolaryngol., 72, 170 Tian, 2011, Identification of the immunogenic outer membrane protein A antigen of Haemophilus parasuis by a proteomics approach and passive immunization with monoclonal antibodies in mice, Clin. Vaccine Immunol., 18, 1695, 10.1128/CVI.05223-11 Torres, 2005, Differential binding of Escherichia coli O157:H7 to alfalfa, human epithelial cells, and plastic is mediated by a variety of surface structures, Appl. Environ. Microbiol., 71, 8008, 10.1128/AEM.71.12.8008-8015.2005 Torres, 2003, Multiple elements controlling adherence of enterohemorrhagic Escherichia coli O157:H7 to HeLa cells, Infect. Immun., 71, 4985, 10.1128/IAI.71.9.4985-4995.2003 Torres, 2006, Outer membrane protein A of Escherichia coli O157:H7 stimulates dendritic cell activation, Infect. Immun., 74, 2676, 10.1128/IAI.74.5.2676-2685.2006 Vanrompay, 1999, Protection of turkeys against Chlamydia psittaci challenge by gene gun-based DNA immunizations, Vaccine, 17, 2628, 10.1016/S0264-410X(99)00053-5 von Specht, 1996, Outer membrane proteins of Pseudomonas aeruginosa as vaccine candidates, J. Biotechnol., 44, 145, 10.1016/0168-1656(95)00161-1 Wang, 2006, Identification of surface-exposed components of MOMP of Chlamydia trachomatis serovar F, Protein Sci., 15, 122, 10.1110/ps.051616206 Weimer, 2009, Immunization of young African green monkeys with OprF epitope 8-OprI-type A- and B-flagellin fusion proteins promotes the production of protective antibodies against nonmucoid Pseudomonas aeruginosa, Vaccine, 27, 6762, 10.1016/j.vaccine.2009.08.080 Weimer, 2009, A fusion protein vaccine containing OprF epitope 8, OprI, and type A and B flagellins promotes enhanced clearance of nonmucoid Pseudomonas aeruginosa, Infect. Immun., 77, 2356, 10.1128/IAI.00054-09 Weiser, 1991, Outer membrane protein A (OmpA) contributes to serum resistance and pathogenicity of Escherichia coli K-1, Infect. Immun., 59, 2252, 10.1128/IAI.59.7.2252-2258.1991 Worgall, 2007, Protective immunity to Pseudomonas aeruginosa induced with a capsid-modified adenovirus expressing P. aeruginosa OprF, J. Virol., 81, 13801, 10.1128/JVI.01246-07 Wu, 2003, Surfactant proteins A and D inhibit the growth of Gram-negative bacteria by increasing membrane permeability, J. Clin. Invest., 111, 1589, 10.1172/JCI16889 Wu, 2009, OmpA is the critical component for Escherichia coli invasion-induced astrocyte activation, J. Neuropathol. Exp. Neurol., 68, 677, 10.1097/NEN.0b013e3181a77d1e Xie, 2004, Current concepts on Escherichia coli K1 translocation of the blood–brain barrier, FEMS Immunol. Med. Microbiol., 42, 271, 10.1016/j.femsim.2004.09.001 Yan, 2010, Identification and characterization of OmpA-like proteins as novel vaccine candidates for Leptospirosis, Vaccine, 28, 2277, 10.1016/j.vaccine.2009.12.071 Yao, 2012, Molecular structure and peptidoglycan recognition of Mycobacterium tuberculosis ArfA (Rv0899), J. Mol. Biol., 416, 208, 10.1016/j.jmb.2011.12.030 Yu, 2012, Chlamydia muridarum T cell antigens and adjuvants that induce protective immunity in mice, Infect. Immun., 80, 1510, 10.1128/IAI.06338-11 Zeng, 1999, Molecular cloning of the Pasteurella haemolytica pomA gene and identification of bovine antibodies against PomA surface domains, Infect. Immun., 67, 4968, 10.1128/IAI.67.9.4968-4973.1999 Zhang, 2012, Comparative proteomic analysis of a Haemophilus parasuis SC096 mutant deficient in the outer membrane protein P5, Microb. Pathog., 52, 117, 10.1016/j.micpath.2011.11.002 Zhang, 1997, DNA vaccination with the major outer-membrane protein gene induces acquired immunity to Chlamydia trachomatis (mouse pneumonitis) infection, J. Infect. Dis., 176, 1035, 10.1086/516545 Zhang, 2011, Characterization of outer membrane proteins of Escherichia coli in response to phenol stress, Curr. Microbiol., 62, 777, 10.1007/s00284-010-9786-z Zhang, 1999, Characterization of immune responses following intramuscular DNA immunization with the MOMP gene of Chlamydia trachomatis mouse pneumonitis strain, Immunology, 96, 314, 10.1046/j.1365-2567.1999.00682.x Zhang, 2010, OmpA-like protein Loa22 from Leptospira interrogans serovar Lai is cytotoxic to cultured rat renal cells and promotes inflammatory responses, Acta Biochim. Biophys. Sin., 42, 70, 10.1093/abbs/gmp109