Current progress with Moraxella catarrhalis antigens as vaccine candidates

Expert Review of Vaccines

Volumn 8, Issue 1, 2009, Pages 77-90

  Mawas, Fatme ^a   Mei, Mei Ho ^a   Corbel, Michael J ^a  

^a NATIONAL INSTITUTE FOR BIOLOGICAL STANDARDS AND CONTROL   (United Kingdom)

Author keywords

Antigen; Moraxella catarrhalis; Vaccine candidate

Indexed keywords

BACTERIAL ANTIGEN; BACTERIAL VACCINE; MORAXELLA CATARRHALIS VACCINE; OUTER MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

CLINICAL TRIAL; HAEMOPHILUS INFLUENZAE; HUMAN; INFECTION PREVENTION; MORAXELLACEAE INFECTION; NONHUMAN; OTITIS MEDIA; PRIORITY JOURNAL; QUALITY CONTROL; RESPIRATORY TRACT INFECTION; REVIEW; VACCINATION; VACCINE PRODUCTION;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL VACCINES; HUMANS; MORAXELLA (BRANHAMELLA) CATARRHALIS; MORAXELLACEAE INFECTIONS; OTITIS MEDIA;

EID: 58149380347     PISSN: 14760584     EISSN: 17448395     Source Type: Journal    
DOI: 10.1586/14760584.8.1.77     Document Type: Review

References (132)

1. Catlin BW. Branhamella catarrhalis: an organism gaining respect as a pathogen. Clin. Microbiol. Rev. 3(4), 293-320 (1990).
2. Enright MC, McKenzie H. Moraxella (Branhamella) catarrhalis - clinical and molecular aspects of a rediscovered pathogen. J. Med. Microbiol. 46(5), 360-371 (1997).
3. Faden H, Harabuchi Y, Hong JJ. Epidemiology of Moraxella catarrhalis in children during the first 2 years of life: relationship to otitis media. J. Infect. Dis. 169(6), 1312-1317 (1994).
4. Murphy TF. Branhamella catarrhalis: epidemiology, surface antigenic structure, and immune response. Microbiol. Rev. 60(2), 267-279 (1996).
5. Sethi S, Murphy TF. Bacterial infection in chronic obstructive pulmonary disease in 2000: a state-of-the-art review. Clin. Microbiol. Rev. 14(2), 336-363 (2001).
6. Meyer GA, Shope TR, Waecker NJ Jr, Lanningham FH. Moraxella (Branhamella) catarrhalis bacteremia in children. A report of two patients and review of the literature. Clin. Pediatr. (Phila.) 34(3), 146-150 (1995).
7. Daoud A, Abuekteish F, Masaadeh H. Neonatal meningitis due to Moraxella catarrhalis and review of the literature. Ann. Trop. Paediatr. 16(3), 199-201 (1996).
8. Verjano SF, Calvo RC, Nebreda PV. Moraxella catarrhalis as a cause of osteomyelitis in the infant. An. Esp. Pediatr. 56(2), 190-191 (2002).
9. Abbott M, Nageswaran A. Bacteremia and septic arthritis caused by Moraxella catarrhalis. Clin. Infect. Dis. 14(1), 368-369 (1992).
10. Richards SJ, Greening AP, Enright MC, Morgan MG, McKenzie H. Outbreak of Moraxella catarrhalis in a respiratory unit. Thorax 48(1), 91-92 (1993).
11. Picard B, Goullet P, Denamur E, Suermondt G. Esterase electrophoresis: a molecular tool for studying the epidemiology of Branhamella catarrhalis nosocomial infection. Epidemiol. Infect. 103(3), 547-554 (1989).
12. Patterson JE, Patterson TF, Farrel P, Hierholzer WJ Jr, Zervos MJ. Evaluation of restriction endonuclease analysis as an epidemiologic typing system for Branhamella catarrhalis. J. Clin. Microbiol. 27(5), 944-946 (1989).
13. Patterson TF, Patterson JE, Masecar BL, Barden GE, Hierholzer WJ Jr, Zervos MJ. A nosocomial outbreak of Branhamella catarrhalis confirmed by restriction endonuclease analysis. J. Infect. Dis. 157(5), 996-1001 (1988).
14. Abdolrasouli A, Amin A, Baharsefat M, Roushan A, Hemmati Y. Moraxella catarrhalis associated with acute urethritis imitating gonorrhoea acquired by oral-genital contact. Int. J. STD AIDS 18(8), 579-580 (2007).
15. Del Beccaro MA, Mendelman PM, Inglis AF et al. Bacteriology of acute otitis media: a new perspective. J. Pediatr. 120(1), 81-84 (1992).
16. Faden H, Bernstein J, Brodsky L, Stanievich J, Ogra PL. Effect of prior antibiotic treatment on middle ear disease in children. Ann. Otol. Rhinol. Laryngol. 101(1), 87-91 (1992).
17. Faden H, Hong J, Murphy T. Immune response to outer membrane antigens of Moraxella catarrhalis in children with otitis media. Infect. Immun. 60(9), 3824-3829 (1992).
18. Faden H, Waz MJ, Bernstein JM, Brodsky L, Stanievich J, Ogra PL. Nasopharyngeal flora in the first three years of life in normal and otitis-prone children. Ann. Otol. Rhinol. Laryngol. 100(8), 612-615 (1991).
19. Gan VN, Kusmiesz H, Shelton S, Nelson JD. Comparative evaluation of loracarbef and amoxicillin-clavulanate for acute otitis media. Antimicrob. Agents Chemother. 35(5), 967-971 (1991).
20. Bennett KE, Haggard MP, Silva PA, Stewart IA. Behaviour and developmental effects of otitis media with effusion into the teens. Arch. Dis. Child 85(2), 91-95 (2001).
21. Klein JO. Otitis media. Clin. Infect. Dis. 19(5), 823-833 (1994).
22. Verduin CM, Hol C, Fleer A, van Dijk H, van Belkum A. Moraxella catarrhalis: from emerging to established pathogen. Clin. Microbiol. Rev. 15(1), 125-144 (2002).
23. Kaieda S, Yano H, Okitsu N et al. In vitro investigation of the indirect pathogenicity of ?-lactamase-producing microorganisms in the nasopharyngeal microflora. Int. J. Pediatr. Otorhinolaryngol. 69(4), 479-485 (2005).
24. Wardle JK. Branhamella catarrhalis as an indirect pathogen. Drugs 31(Suppl. 3), 93-96 (1986).
25. Ejlertsen T, Thisted E, Ostergaard PA, Renneberg J. Maternal antibodies and acquired serological response to Moraxella catarrhalis in children determined by an enzyme-linked immunosorbent assay. Clin. Diagn. Lab. Immunol. 1(4), 464-468 (1994).
26. Ejlertsen T, Thisted E, Ebbesen F, Olesen B, Renneberg J. Branhamella catarrhalis in children and adults. A study of prevalence, time of colonisation, and association with upper and lower respiratory tract infections. J. Infect. 29(1), 23-31 (1994).
27. Van Hare GF, Shurin PA, Marchant CD et al. Acute otitis media caused by Branhamella catarrhalis: biology and therapy. Rev. Infect. Dis. 9(1), 16-27 (1987).
28. Verhaegh SJ, Streefland A, Dewnarain JK, Farrell DJ, van Belkum A, Hays JP. Age-related genotypic and phenotypic differences in Moraxella catarrhalis isolates from children and adults presenting with respiratory disease in 2001-2002. Microbiology 154(Pt 4), 1178-1184 (2008).
29. Prymula R, Peeters P, Chrobok V et al. Pneumococcal capsular polysaccharides conjugated to protein D for prevention of acute otitis media caused by both Streptococcus pneumoniae and non-typable Haemophilus influenzae: a randomised double-blind efficacy study. Lancet 367(9512), 740-748 (2006).
30. Eskola J, Kilpi T, Palmu A et al. Efficacy of a pneumococcal conjugate vaccine against acute otitis media. N. Engl. J. Med. 344(6), 403-409 (2001).
31. Veenhoven R, Bogaert D, Uiterwaal C et al. Effect of conjugate pneumococcal vaccine followed by polysaccharide pneumococcal vaccine on recurrent acute otitis media: a randomised study. Lancet 361(9376), 2189-2195 (2003).
32. McMichael JC, Green BA. Vaccines for Moraxella catarrhalis and non-typeable Haemophilus influenzae. Curr. Opin. Investig. Drugs 4(8), 953-958 (2003).
33. Murphy TF. Vaccine development for non-typeable Haemophilus influenzae and Moraxella catarrhalis: progress and challenges. Expert Rev. Vaccines 4(6), 843-853 (2005).
34. Cripps AW, Otczyk DC. Prospects for a vaccine against otitis media. Expert Rev. Vaccines 5(4), 517-534 (2006).
35. Tan TT, Riesbeck K. Current progress of adhesins as vaccine candidates for Moraxella catarrhalis. Expert Rev. Vaccines 6(6), 949-956 (2007).
36. Aebi C, Maciver I, Latimer JL et al. A protective epitope of Moraxella catarrhalis is encoded by two different genes. Infect. Immun. 65(11), 4367-4377 (1997).
37. Lafontaine ER, Wagner NJ, Hansen EJ. Expression of the Moraxella catarrhalis UspA1 protein undergoes phase variation and is regulated at the transcriptional level. J. Bacteriol. 183(5), 1540-1551 (2001).
38. Meier PS, Troller R, Grivea IN, Syrogiannopoulos GA, Aebi C. The outer membrane proteins UspA1 and UspA2 of Moraxella catarrhalis are highly conserved in nasopharyngeal isolates from young children. Vaccine 20(13-14), 1754-1760 (2002).
39. McMichael JC, Fiske MJ, Fredenburg RA et al. Isolation and characterization of two proteins from Moraxella catarrhalis that bear a common epitope. Infect. Immun. 66(9), 4374-4381 (1998).
40. Chen D, McMichael JC, VanDerMeid KR et al. Evaluation of purified UspA from Moraxella catarrhalis as a vaccine in a murine model after active immunization. Infect. Immun. 64(6), 1900-1905 (1996).
41. Helminen ME, Maciver I, Latimer JL et al. A large, antigenically conserved protein on the surface of Moraxella catarrhalis is a target for protective antibodies. J. Infect. Dis. 170(4), 867-872 (1994).
42. Klingman KL, Murphy TF. Purification and characterization of a high-molecular-weight outer membrane protein of Moraxella (Branhamella) catarrhalis. Infect. Immun. 62(4), 1150-1155 (1994).
43. Brooks MJ, Sedillo JL, Wagner N et al. Modular arrangement of allelic variants explains divergence in Moraxella catarrhalis UspA protein function. Infect. Immun. (2008).
44. Brooks MJ, Sedillo JL, Wagner N et al. Moraxella catarrhalis binding to host cellular receptors is mediated by sequence-specific determinants not conserved among all UspA1 protein variants. Infect. Immun. 76(11), 5322-5329 (2008).
45. Cope LD, Lafontaine ER, Slaughter CA et al. Characterization of the Moraxella catarrhalis uspA1 and uspA2 genes and their encoded products. J. Bacteriol. 181(13), 4026-4034 (1999).
46. Hoiczyk E, Roggenkamp A, Reichenbecher M, Lupas A, Heesemann J. Structure and sequence analysis of Yersinia YadA and Moraxella UspAs reveal a novel class of adhesins. EMBO J. 19(22), 5989-5999 (2000).
47. Lafontaine ER, Cope LD, Aebi C, Latimer JL, McCracken GH Jr, Hansen EJ. The UspA1 protein and a second type of UspA2 protein mediate adherence of Moraxella catarrhalis to human epithelial cells in vitro. J. Bacteriol. 182(5), 1364-1373 (2000).
48. Tan TT, Nordstrom T, Forsgren A, Riesbeck K. The respiratory pathogen Moraxella catarrhalis adheres to epithelial cells by interacting with fibronectin through ubiquitous surface proteins A1 and A2. J. Infect. Dis. 192(6), 1029-1038 (2005).
49. Tan TT, Forsgren A, Riesbeck K. The respiratory pathogen Moraxella catarrhalis binds to laminin via ubiquitous surface proteins A1 and A2. J. Infect. Dis. 194(4), 493-497 (2006).
50. Riesbeck K, Tan TT, Forsgren A. MID and UspA1/A2 of the human respiratory pathogen Moraxella catarrhalis, and interactions with the human host as basis for vaccine development. Acta Biochim. Pol. 53(3), 445-456 (2006).
51. Heiniger N, Troller R, Meier PS, Aebi C. Cold shock response of the UspA1 outer membrane adhesin of Moraxella catarrhalis. Infect. Immun. 73(12), 8247-8255 (2005).
52. Attia AS, Hansen EJ. A conserved tetranucleotide repeat is necessary for wild-type expression of the Moraxella catarrhalis UspA2 protein. J. Bacteriol. 188(22), 7840-7852 (2006).
53. Attia AS, Lafontaine ER, Latimer JL, Aebi C, Syrogiannopoulos GA, Hansen EJ. The UspA2 protein of Moraxella catarrhalis is directly involved in the expression of serum resistance. Infect. Immun. 73(4), 2400-2410 (2005).
54. Bootsma HJ, van der Heide HG, van de Pas S, Schouls LM, Mooi FR. Analysis of Moraxella catarrhalis by DNA typing: evidence for a distinct subpopulation associated with virulence traits. J. Infect. Dis. 181(4), 1376-1387 (2000).
55. Meier PS, Troller R, Heiniger N, Grivea IN, Syrogiannopoulos GA, Aebi C. Moraxella catarrhalis strains with reduced expression of the UspA outer membrane proteins belong to a distinct subpopulation. Vaccine 23(16), 2000-2008 (2005).
56. Chen D, Barniak V, VanDerMeid KR, McMichael JC. The levels and bactericidal capacity of antibodies directed against the UspA1 and UspA2 outer membrane proteins of Moraxella (Branhamella) catarrhalis in adults and children. Infect. Immun. 67(3), 1310-1316 (1999).
57. Murphy TF, Brauer AL, Aebi C, Sethi S. Identification of surface antigens of Moraxella catarrhalis as targets of human serum antibody responses in chronic obstructive pulmonary disease. Infect. Immun. 73(6), 3471-3478 (2005).
58. Murphy TF, Brauer AL, Aebi C, Sethi S. Antigenic specificity of the mucosal antibody response to Moraxella catarrhalis in chronic obstructive pulmonary disease. Infect. Immun. 73(12), 8161-8166 (2005).
59. McMichael JC, Fiske MJ, Fredenburg RA et al. Isolation and characterization of two proteins from Moraxella catarrhalis that bear a common epitope. Infect. Immun. 66(9), 4374-4381 (1998).
60. Mason KW, Zhu D, Scheuer CA, McMichael JC, Zlotnick GW, Green BA. Reduction of nasal colonization of nontypeable Haemophilus influenzae following intranasal immunization with rLP4/rLP6/UspA2 proteins combined with aqueous formulation of RC529. Vaccine 22(25-26), 3449-3456 (2004).
61. Mawas F, Ho MM, Huskisson R, Saydam M, Corbel MJ. Physico-chemical characterisation and immunogenicity of a multi-valent candidate vaccine against non-typeable Haemophilus influenzae and Moraxella catarrhalis. Vaccine 25(25), 4801-4808 (2007).
62. Forsgren A, Brant M, Mollenkvist A et al. Isolation and characterization of a novel IgD-binding protein from Moraxella catarrhalis. J. Immunol. 167(4), 2112-2120 (2001).
63. Bullard B, Lipski SL, Lafontaine ER. Hag directly mediates the adherence of Moraxella catarrhalis to human middle ear cells. Infect. Immun. 73(8), 5127-5136 (2005).
64. Riesbeck K, Nordstrom T. Structure and immunological action of the human pathogen Moraxella catarrhalis IgD-binding protein. Crit. Rev. Immunol. 26(4), 353-376 (2006).
65. Mollenkvist A, Nordstrom T, Hallden C, Christensen JJ, Forsgren A, Riesbeck K. The Moraxella catarrhalis immunoglobulin D-binding protein MID has conserved sequences and is regulated by a mechanism corresponding to phase variation. J. Bacteriol. 185(7), 2285-2295 (2003).
66. Meier PS, Freiburghaus S, Martin A, Heiniger N, Troller R, Aebi C. Mucosal immune response to specific outer membrane proteins of Moraxella catarrhalis in young children. Pediatr. Infect. Dis. J. 22(3), 256-262 (2003).
67. Forsgren A, Brant M, Riesbeck K. Immunization with the truncated adhesin Moraxella catarrhalis immunoglobulin D-binding protein (MID764-913) is protective against M. catarrhalis in a mouse model of pulmonary clearance. J. Infect. Dis. 190(2), 352-355 (2004).
68. Lipski SL, Akimana C, Timpe JM, Wooten RM, Lafontaine ER. The Moraxella catarrhalis autotransporter McaP is a conserved surface protein that mediates adherence to human epithelial cells through its N-terminal passenger domain. Infect. Immun. 75(1), 314-324 (2007).
69. Timpe JM, Holm MM, Vanlerberg SL, Basrur V, Lafontaine ER. Identification of a Moraxella catarrhalis outer membrane protein exhibiting both adhesin and lipolytic activities. Infect. Immun. 71(8), 4341-4350 (2003).
70. Sarwar J, Campagnari AA, Kirkham C, Murphy TF. Characterization of an antigenically conserved heat-modifiable major outer membrane protein of Branhamella catarrhalis. Infect. Immun. 60(3), 804-809 (1992).
71. Holm MM, Vanlerberg SL, Foley IM, Sledjeski DD, Lafontaine ER. The Moraxella catarrhalis porin-like outer membrane protein CD is an adhesin for human lung cells. Infect. Immun. 72(4), 1906-1913 (2004).
72. Murphy TF, Kirkham C, Lesse AJ. The major heat-modifiable outer membrane protein CD is highly conserved among strains of Branhamella catarrhalis. Mol. Microbiol. 10(1), 87-97 (1993).
73. Hsiao CB, Sethi S, Murphy TF. Outer membrane protein CD of Branhamella catarrhalis: sequence conservation in strains recovered from the human respiratory tract. Microb. Pathog. 19(4), 215-225 (1995).
74. Murphy TF, Kirkham C, Liu DF, Sethi S. Human immune response to outer membrane protein CD of Moraxella catarrhalis in adults with chronic obstructive pulmonary disease. Infect. Immun. 71(3), 1288-1294 (2003).
75. Murphy TF, Brauer AL, Grant BJ, Sethi S. Moraxella catarrhalis in chronic obstructive pulmonary disease: burden of disease and immune response. Am. J. Respir. Crit. Care Med. 172(2), 195-199 (2005).
76. Harabuchi Y, Murakata H, Goh M et al. Serum antibodies specific to CD outer membrane protein of Moraxella catarrhalis, P6 outer membrane protein of non-typeable Haemophilus influenzae and capsular polysaccharides of Streptococcus pneumoniae in children with otitis media with effusion. Acta Otolaryngol. 118(6), 826-832 (1998).
77. Becker PD, Bertot GM, Souss D, Ebensen T, Guzman CA, Grinstein S. Intranasal vaccination with recombinant outer membrane protein CD and adamantylamide dipeptide as the mucosal adjuvant enhances pulmonary clearance of Moraxella catarrhalis in an experimental murine model. Infect. Immun. 75(4), 1778-1784 (2007).
78. Murphy TF, Kyd JM, John A, Kirkham C, Cripps AW. Enhancement of pulmonary clearance of Moraxella (Branhamella) catarrhalis following immunization with outer membrane protein CD in a mouse model. J. Infect. Dis. 178(6), 1667-1675 (1998).
79. Yang YP, Myers LE, McGuinness U et al. The major outer membrane protein, CD, extracted from Moraxella (Branhamella) catarrhalis is a potential vaccine antigen that induces bactericidal antibodies. FEMS Immunol. Med. Microbiol. 17(3), 187-199 (1997).
80. Liu DF, McMichael JC, Baker SM. Moraxella catarrhalis outer membrane protein CD elicits antibodies that inhibit CD binding to human mucin and enhance pulmonary clearance of M. catarrhalis in a mouse model. Infect. Immun. 75(6), 2818-2825 (2007).
81. Easton DM, Smith A, Gallego SG, Foxwell AR, Cripps AW, Kyd JM. Characterization of a novel porin protein from Moraxella catarrhalis and identification of an immunodominant surface loop. J. Bacteriol. 187(18), 6528-6535 (2005).
82. Balder R, Hassel J, Lipski S, Lafontaine ER. Moraxella catarrhalis strain O35E expresses two filamentous hemagglutinin-like proteins that mediate adherence to human epithelial cells. Infect. Immun. 75(6), 2765-2775 (2007).
83. Plamondon P, Luke NR, Campagnari AA. Identification of a novel two-partner secretion locus in Moraxella catarrhalis. Infect. Immun. 75(6), 2929-2936 (2007).
84. Guedin S, Willery E, Tommassen J et al. Novel topological features of FhaC, the outer membrane transporter involved in the secretion of the Bordetella pertussis filamentous hemagglutinin. J. Biol. Chem. 275(39), 30202-30210 (2000).
85. Brooks MJ, Laurence CA, Hansen EJ, Gray-Owen SD. Characterization of the Moraxella catarrhalis opa-like protein, OlpA, reveals a phylogenetically conserved family of outer membrane proteins. J. Bacteriol. 189(1), 76-82 (2007).
86. Gray-Owen SD, Schryvers AB. Bacterial transferrin and lactoferrin receptors. Trends Microbiol. 4(5), 185-191 (1996).
87. Myers LE, Yang YP, Du RP et al. The transferrin binding protein B of Moraxella catarrhalis elicits bactericidal antibodies and is a potential vaccine antigen. Infect. Immun. 66(9), 4183-4192 (1998).
88. Alcantara J, Padda JS, Schryvers AB. The N-linked oligosaccharides of human lactoferrin are not required for binding to bacterial lactoferrin receptors. Can. J. Microbiol. 38(11), 1202-1205 (1992).
89. Luke NR, Russo TA, Luther N, Campagnari AA. Use of an isogenic mutant constructed in Moraxella catarrhalis to identify a protective epitope of outer membrane protein B1 defined by monoclonal antibody 11C6. Infect. Immun. 67(2), 681-687 (1999).
90. Luke NR, Campagnari AA. Construction and characterization of Moraxella catarrhalis mutants defective in expression of transferrin receptors. Infect. Immun. 67(11), 5815-5819 (1999).
91. Campagnari AA, Ducey TF, Rebmann CA. Outer membrane protein B1, an iron-repressible protein conserved in the outer membrane of Moraxella (Branhamella) catarrhalis, binds human transferrin. Infect. Immun. 64(9), 3920-3924 (1996).
92. Sethi S, Hill SL, Murphy TF. Serum antibodies to outer membrane proteins (OMPs) of Moraxella (Branhamella) catarrhalis in patients with bronchiectasis: identification of OMP B1 as an important antigen. Infect. Immun. 63(4), 1516-1520 (1995).
93. Yu RH, Bonnah RA, Ainsworth S, Schryvers AB. Analysis of the immunological responses to transferrin and lactoferrin receptor proteins from Moraxella catarrhalis. Infect. Immun. 67(8), 3793-3799 (1999).
94. Du RP, Wang Q, Yang YP et al. Cloning and expression of the Moraxella catarrhalis lactoferrin receptor genes. Infect. Immun. 66(8), 3656-3665 (1998).
95. Schryvers AB, Bonnah R, Yu RH, Wong H, Retzer M. Bacterial lactoferrin receptors. Adv. Exp. Med. Biol. 443, 123-133 (1998).
96. Bonnah RA, Wong H, Loosmore SM, Schryvers AB. Characterization of Moraxella (Branhamella) catarrhalis lbpB, lbpA, and lactoferrin receptor orf3 isogenic mutants. Infect. Immun. 67(3), 1517-1520 (1999).
97. Helminen ME, Maciver I, Latimer JL, Cope LD, McCracken GH Jr, Hansen EJ. A major outer membrane protein of Moraxella catarrhalis is a target for antibodies that enhance pulmonary clearance of the pathogen in an animal model. Infect. Immun. 61(5), 2003-2010 (1993).
98. Campagnari AA, Shanks KL, Dyer DW. Growth of Moraxella catarrhalis with human transferrin and lactoferrin: expression of iron-repressible proteins without siderophore production. Infect. Immun. 62(11), 4909-4914 (1994).
99. Aebi C, Stone B, Beucher M et al. Expression of the CopB outer membrane protein by Moraxella catarrhalis is regulated by iron and affects iron acquisition from transferrin and lactoferrin. Infect. Immun. 64(6), 2024-2030 (1996).
100. Liu DF, Xie X, Mastri MG et al. Polymorphism of the major surface epitope of the CopB outer membrane protein of Moraxella catarrhalis. FEMS Immunol. Med. Microbiol. 47(3), 343-350 (2006).
101. Helminen ME, Maciver I, Paris M et al. A mutation affecting expression of a major outer membrane protein of Moraxella catarrhalis alters serum resistance and survival in vivo. J. Infect. Dis. 168(5), 1194-1201 (1993).
102. Mathers K, Leinonen M, Goldblatt D. Antibody response to outer membrane proteins of Moraxella catarrhalis in children with otitis media. Pediatr. Infect. Dis. J. 18(11), 982-988 (1999).
103. Helminen ME, Beach R, Maciver I, Jarosik G, Hansen EJ, Leinonen M. Human immune response against outer membrane proteins of Moraxella (Branhamella) catarrhalis determined by immunoblotting and enzyme immunoassay. Clin. Diagn. Lab. Immunol. 2(1), 35-39 (1995).
104. Murphy TF, Brauer AL, Yuskiw N, Hiltke TJ. Antigenic structure of outer membrane protein E of Moraxella catarrhalis and construction and characterization of mutants. Infect. Immun. 68(11), 6250-6256 (2000).
105. Murphy TF. Branhamella catarrhalis: epidemiology, surface antigenic structure, and immune response. Microbiol. Rev. 60(2), 267-279 (1996).
106. Bhushan R, Craigie R, Murphy TF. Molecular cloning and characterization of outer membrane protein E of Moraxella (Branhamella) catarrhalis. J. Bacteriol. 176(21), 6636-6643 (1994).
107. Bhushan R, Kirkham C, Sethi S, Murphy TF. Antigenic characterization and analysis of the human immune response to outer membrane protein E of Branhamella catarrhalis. Infect. Immun. 65(7), 2668-2675 (1997).
108. Murphy TF, Bartos LC. Surface-exposed and antigenically conserved determinants of outer membrane proteins of Branhamella catarrhalis. Infect. Immun. 57(10), 2938-2941 (1989).
109. Murphy TF, Brauer AL, Yuskiw N, McNamara ER, Kirkham C. Conservation of outer membrane protein E among strains of Moraxella catarrhalis. Infect. Immun. 69(6), 3576-3580 (2001).
110. Bartos LC, Murphy TF. Comparison of the outer membrane proteins of 50 strains of Branhamella catarrhalis. J. Infect. Dis. 158(4), 761-765 (1988).
111. Adlowitz DG, Hiltke T, Lesse AJ, Murphy TF. Identification and characterization of outer membrane proteins G1a and G1b of Moraxella catarrhalis. Vaccine 22(20), 2533-2540 (2004).
112. Adlowitz DG, Sethi S, Cullen P, Adler B, Murphy TF. Human antibody response to outer membrane protein G1a, a lipoprotein of Moraxella catarrhalis. Infect. Immun. 73(10), 6601-6607 (2005).
113. Hays JP, van Selm S, Hoogenboezem T et al. Identification and characterization of a novel outer membrane protein (OMP J) of Moraxella catarrhalis that exists in two major forms. J. Bacteriol. 187(23), 7977-7984 (2005).
114. Ruckdeschel EA, Kirkham C, Lesse AJ, Hu Z, Murphy TF. Mining the Moraxella catarrhalis genome: identification of potential vaccine antigens expressed during human infection. Infect. Immun. 76(4), 1599-1607 (2008).
115. Fomsgaard JS, Fomsgaard A, Hoiby N, Bruun B, Galanos C. Comparative immunochemistry of lipopolysaccharides from Branhamella catarrhalis strains. Infect. Immun. 59(9), 3346-3349 (1991).
116. Vaneechoutte M, Verschraegen G, Claeys G, Van den Abeele AM. Serological typing of Branhamella catarrhalis strains on the basis of lipopolysaccharide antigens. J. Clin. Microbiol. 28(2), 182-187 (1990).
117. Edebrink P, Jansson PE, Rahman MM et al. Structural studies of the O-polysaccharide from the lipopolysaccharide of Moraxella (Branhamella) catarrhalis serotype A (strain ATCC 25238). Carbohydr. Res. 257(2), 269-284 (1994).
118. Verduin CM, Hol C, Fleer A, van Dijk H, van Belkum A. Moraxella catarrhalis: from emerging to established pathogen. Clin. Microbiol. Rev. 15(1), 125-144 (2002).
119. Rahman M, Holme T, Jonsson I, Krook A. Lack of serotype-specific antibody response to lipopolysaccharide antigens of Moraxella catarrhalis during lower respiratory tract infection. Eur. J. Clin. Microbiol. Infect. Dis. 14(4), 297-304 (1995).
120. Gergova RT, Iankov ID, Haralambieva IH, Mitov IG. Bactericidal monoclonal antibody against Moraxella catarrhalis lipooligosaccharide cross-reacts with Haemophilus spp. Curr. Microbiol. 54(2), 85-90 (2007).
121. Gu XX, Chen J, Barenkamp SJ et al. Synthesis and characterization of lipooligosaccharide-based conjugates as vaccine candidates for Moraxella (Branhamella) catarrhalis. Infect. Immun. 66(5), 1891-1897 (1998).
122. Jiao X, Hirano T, Hou Y, Gu XX. Specific immune responses and enhancement of murine pulmonary clearance of Moraxella catarrhalis by intranasal immunization with a detoxified lipooligosaccharide conjugate vaccine. Infect. Immun. 70(11), 5982-5989 (2002).
123. Yu S, Gu XX. Synthesis and characterization of lipooligosaccharide-based conjugate vaccines for serotype B Moraxella catarrhalis. Infect. Immun. 73(5), 2790-2796 (2005).
124. Yu S, Gu XX. Biological and immunological characteristics of lipooligosaccharide-based conjugate vaccines for serotype C Moraxella catarrhalis. Infect. Immun. 75(6), 2974-2980 (2007).
125. Hu WG, Chen J, Battey JF, Gu XX. Enhancement of clearance of bacteria from murine lungs by immunization with detoxified lipooligosaccharide from Moraxella catarrhalis conjugated to proteins. Infect. Immun. 68(9), 4980-4985 (2000).
126. Hu WG, Berry J, Chen J, Gu XX. Exploration of Moraxella catarrhalis outer membrane proteins, CD and UspA, as new carriers for lipooligosaccharide-based conjugates. FEMS Immunol. Med. Microbiol. 41(2), 109-115 (2004).
127. Peng D, Hong W, Choudhury BP, Carlson RW, Gu XX. Moraxella catarrhalis bacterium without endotoxin, a potential vaccine candidate. Infect. Immun. 73(11), 7569-7577 (2005).
128. Gu XX, Rudy SF, Chu C et al. Phase I study of a lipooligosaccharide-based conjugate vaccine against nontypeable Haemophilus influenzae. Vaccine 21(17-18), 2107-2114 (2003).
129. Bakaletz LO, Murwin DM, Billy JM. Adenovirus serotype 1 does not act synergistically with Moraxella (Branhamella) catarrhalis to induce otitis media in the chinchilla. Infect. Immun. 63(10), 4188-4190 (1995).
130. Luke NR, Jurcisek JA, Bakaletz LO, Campagnari AA. Contribution of Moraxella catarrhalis type IV pili to nasopharyngeal colonization and biofilm formation. Infect. Immun. 75(12), 5559-5564 (2007).
131. Ahmed A, Broides A, Givon-Lavi N, Peled N, Dagan R, Greenberg D. Clinical and laboratory aspects of Moraxella catarrhalis bacteremia in children. Pediatr. Infect. Dis. J. 27(5), 459-461 (2008).
132. Heyderman RS, Ison CA, Peakman M, Levin M, Klein NJ. Neutrophil response to Neisseria meningitidis: inhibition of adhesion molecule expression and phagocytosis by recombinant bactericidal/permeability-increasing protein (rBPI21). J. Infect. Dis. 179(5), 1288-1292 (1999).