Molecular Aspects of Moraxella catarrhalis Pathogenesis

SUMMARY In recent years, Moraxella catarrhalis has established its position as an important human mucosal pathogen, no longer being regarded as just a commensal bacterium. Further, current research in the field has led to a better understanding of the molecular mechanisms involved in M. catarrhalis pathogenesis, including mechanisms associated with cellular adherence, target cell invasion, modulation of the host's immune response, and metabolism. Additionally, in order to be successful in the host, M. catarrhalis has to be able to interact and compete with the commensal flora and overcome stressful environmental conditions, such as nutrient limitation. In this review, we provide a timely overview of the current understanding of the molecular mechanisms associated with M. catarrhalis virulence and pathogenesis.

[1]  J. Musser,et al.  Secreted bacterial phospholipase A2 enzymes: better living through phospholipolysis. , 2007, Trends in microbiology.

[2]  A. Meyer,et al.  The rise and spread of a new pathogen: seroresistant Moraxella catarrhalis. , 2007, Genome research.

[3]  E. Hansen,et al.  A hag Mutant of Moraxella catarrhalis Strain O35E Is Deficient in Hemagglutination, Autoagglutination, and Immunoglobulin D-Binding Activities , 2002, Infection and Immunity.

[4]  E. R. Lafontaine,et al.  The Moraxella catarrhalis outer membrane protein CD contains two distinct domains specifying adherence to human lung cells. , 2007, FEMS microbiology letters.

[5]  J. Heesemann,et al.  Contribution of Trimeric Autotransporter C-Terminal Domains of Oligomeric Coiled-Coil Adhesin (Oca) Family Members YadA, UspA1, EibA, and Hia to Translocation of the YadA Passenger Domain and Virulence of Yersinia enterocolitica , 2008, Journal of bacteriology.

[6]  T. Murphy,et al.  Conservation of Outer Membrane Protein E among Strains of Moraxella catarrhalis , 2001, Infection and Immunity.

[7]  A. Forsgren,et al.  Branhamella catarrhalis activates human B lymphocytes following interactions with surface IgD and class I major histocompatibility complex antigens. , 1988, Cellular immunology.

[8]  B. Clantin,et al.  Secretion signal of the filamentous haemagglutinin, a model two‐partner secretion substrate , 2006, Molecular microbiology.

[9]  Y. Tung,et al.  Relationship between nasopharyngeal colonization and the development of otitis media in children. Tonawanda/Williamsville Pediatrics. , 1997, The Journal of infectious diseases.

[10]  D. Peng,et al.  Moraxella catarrhalis Bacterium without Endotoxin, a Potential Vaccine Candidate , 2005, Infection and Immunity.

[11]  T. Sundqvist,et al.  The ability to bind albumin is correlated with nitric oxide sensitivity in Moraxella catarrhalis. , 1998, FEMS microbiology letters.

[12]  D. Metzger,et al.  Mouse models for the study of mucosal vaccination against otitis media. , 2008, Vaccine.

[13]  M. Jacques Role of lipo-oligosaccharides and lipopolysaccharides in bacterial adherence. , 1996, Trends in microbiology.

[14]  E. R. Lafontaine,et al.  Identification of a Moraxella catarrhalis Outer Membrane Protein Exhibiting Both Adhesin and Lipolytic Activities , 2003, Infection and Immunity.

[15]  Morag R. Graham,et al.  Global differential gene expression in response to growth temperature alteration in group A Streptococcus , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[16]  Paul Stoodley,et al.  Bacterial biofilms: from the Natural environment to infectious diseases , 2004, Nature Reviews Microbiology.

[17]  John A. Tainer,et al.  Type IV pilus structure and bacterial pathogenicity , 2004, Nature Reviews Microbiology.

[18]  J. Jurcisek,et al.  Contribution of Moraxella catarrhalis Type IV Pili to Nasopharyngeal Colonization and Biofilm Formation , 2007, Infection and Immunity.

[19]  A. Schryvers,et al.  The interaction between human transferrin and transferrin binding protein 2 from Moraxella (Branhamella) catarrhalis differs from that of other human pathogens. , 1993, Microbial pathogenesis.

[20]  P. Godowski,et al.  Toll-like receptor 2-mediated NF-kappa B activation requires a Rac1-dependent pathway. , 2000, Nature immunology.

[21]  Therése Nordström,et al.  The respiratory pathogen Moraxella catarrhalis adheres to epithelial cells by interacting with fibronectin through ubiquitous surface proteins A1 and A2. , 2005, The Journal of infectious diseases.

[22]  Garth D Ehrlich,et al.  Direct detection of bacterial biofilms on the middle-ear mucosa of children with chronic otitis media. , 2006, JAMA.

[23]  A. van Belkum,et al.  Complement-resistant Moraxella catarrhalis forms a genetically distinct lineage within the species. , 2000, FEMS microbiology letters.

[24]  J. Dankert,et al.  Involvement of lipooligosaccharides of Haemophilus influenzae and Neisseria meningitidis in defensin-enhanced bacterial adherence to epithelial cells. , 2003, Microbial pathogenesis.

[25]  M. Sheehan,et al.  Complement inhibition by human vitronectin involves non‐heparin binding domains , 1995, Clinical and experimental immunology.

[26]  R. Petralia,et al.  Roles of 3-Deoxy-d-manno-2-Octulosonic Acid Transferase from Moraxella catarrhalis in Lipooligosaccharide Biosynthesis and Virulence , 2005, Infection and Immunity.

[27]  A. Clarke,et al.  The Moraxella adhesin UspA1 binds to its human CEACAM1 receptor by a deformable trimeric coiled-coil , 2008, The EMBO journal.

[28]  A. S. Attia,et al.  Binding of Vitronectin by the Moraxella catarrhalis UspA2 Protein Interferes with Late Stages of the Complement Cascade , 2006, Infection and Immunity.

[29]  T. Murphy,et al.  Identification of Domains of the Hag/MID Surface Protein Recognized by Systemic and Mucosal Antibodies in Adults with Chronic Obstructive Pulmonary Disease following Clearance of Moraxella catarrhalis , 2009, Clinical and Vaccine Immunology.

[30]  S. Müller,et al.  The Moraxella IgD-binding protein MID/Hag is an oligomeric autotransporter. , 2008, Microbes and infection.

[31]  P. Jansson,et al.  The lipopolysaccharide of moraxella catarrhalis structural relationships and antigenic properties. , 1999, European journal of biochemistry.

[32]  E. R. Lafontaine,et al.  Regions important for the adhesin activity of Moraxella catarrhalis Hag , 2007, BMC microbiology.

[33]  P. Densen,et al.  Lipooligosaccharide P(k) (Galalpha1-4Galbeta1-4Glc) epitope of moraxella catarrhalis is a factor in resistance to bactericidal activity mediated by normal human serum. , 2000, Infection and immunity.

[34]  T. Murphy,et al.  Antigenic Structure of Outer Membrane Protein E ofMoraxella catarrhalis and Construction and Characterization of Mutants , 2000, Infection and Immunity.

[35]  S. E. Thomas,et al.  A protective epitope of Moraxella catarrhalis is encoded by two different genes , 1997, Infection and immunity.

[36]  A. Edwards,et al.  Carcinoembryonic antigen‐related cell adhesion molecule (CEACAM)‐binding recombinant polypeptide confers protection against infection by respiratory and urogenital pathogens , 2005, Molecular microbiology.

[37]  A. Kaser,et al.  SHP1 phosphatase-dependent T cell inhibition by CEACAM1 adhesion molecule isoforms. , 2006, Immunity.

[38]  A. Campagnari,et al.  Identification of a Novel Two-Partner Secretion Locus in Moraxella catarrhalis , 2007, Infection and Immunity.

[39]  A. Forsgren,et al.  The respiratory pathogen moraxella catarrhalis binds to laminin via ubiquitous surface proteins A1 and A2. , 2006, The Journal of infectious diseases.

[40]  A. van Belkum,et al.  Moraxella catarrhalis: from Emerging to Established Pathogen , 2002, Clinical Microbiology Reviews.

[41]  A. Ichinose,et al.  Role of Lipooligosaccharide in the Attachment of Moraxella catarrhalis to Human Pharyngeal Epithelial Cells , 2005, Microbiology and immunology.

[42]  W. Zimmermann,et al.  CEACAM1 inhibits Toll-like receptor 2–triggered antibacterial responses of human pulmonary epithelial cells , 2008, Nature Immunology.

[43]  J. S. St. Geme,et al.  Trimeric autotransporters: a distinct subfamily of autotransporter proteins. , 2005, Trends in microbiology.

[44]  J. Verhoef,et al.  Moraxella (Branhamella)catarrhalis BRO β-Lactamase: a Lipoprotein of Gram-Positive Origin? , 1999, Journal of bacteriology.

[45]  A. Forsgren,et al.  Many bacterial species bind human IgD. , 1979, Journal of immunology.

[46]  B. Pussell,et al.  Vitronectin‐mediated inhibition of complement: evidence for different binding sites for C5b‐7 and C9 , 1993, Clinical and experimental immunology.

[47]  K. Riesbeck,et al.  The UspA1 protein of Moraxella catarrhalis induces CEACAM-1-dependent apoptosis in alveolar epithelial cells. , 2007, The Journal of infectious diseases.

[48]  Christoph Dehio,et al.  Signature-tagged mutagenesis: technical advances in a negative selection method for virulence gene identification. , 2005, Current opinion in microbiology.

[49]  G. Syrogiannopoulos,et al.  The outer membrane proteins UspA1 and UspA2 of Moraxella catarrhalis are highly conserved in nasopharyngeal isolates from young children. , 2002, Vaccine.

[50]  A. Campagnari,et al.  Identification of a conserved Moraxella catarrhalis haemoglobin-utilization protein, MhuA. , 2005, Microbiology.

[51]  Middle ear mucin glycoprotein: purification and interaction with nontypable Haemophilus influenzae and Moraxella catarrhalis. , 1995, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[52]  M. Ronaghi,et al.  Phylogeny of the family Moraxellaceae by 16S rDNA sequence analysis, with special emphasis on differentiation of Moraxella species. , 1998, International journal of systematic bacteriology.

[53]  F. Mooi,et al.  Analysis of Moraxella catarrhalis by DNA typing: evidence for a distinct subpopulation associated with virulence traits. , 2000, The Journal of infectious diseases.

[54]  E. R. Lafontaine,et al.  The Hag Protein of Moraxella catarrhalis Strain O35E Is Associated with Adherence to Human Lung and Middle Ear Cells , 2003, Infection and Immunity.

[55]  N. Suttorp,et al.  Moraxella catarrhalis induces inflammatory response of bronchial epithelial cells via MAPK and NF-kappaB activation and histone deacetylase activity reduction. , 2006, American journal of physiology. Lung cellular and molecular physiology.

[56]  A. Forsgren,et al.  The Immunoglobulin D-Binding Protein MID from Moraxella catarrhalis Is Also an Adhesin , 2003, Infection and Immunity.

[57]  E. Hansen,et al.  Phenotypic Effect of Isogenic uspA1 anduspA2 Mutations on Moraxella catarrhalis 035E , 1998, Infection and Immunity.

[58]  Characterization of Moraxella(Branhamella) catarrhalis lbpB, lbpA, and Lactoferrin Receptor orf3 Isogenic Mutants , 1999, Infection and Immunity.

[59]  E. Hansen,et al.  Biofilm Formation by Moraxella catarrhalis In Vitro: Roles of the UspA1 Adhesin and the Hag Hemagglutinin , 2006, Infection and Immunity.

[60]  Therése Nordström,et al.  The Moraxella catarrhalis Immunoglobulin D-Binding Protein MID Has Conserved Sequences and Is Regulated by a Mechanism Corresponding to Phase Variation , 2003, Journal of bacteriology.

[61]  A. van Belkum,et al.  Moraxella catarrhalis is only a weak activator of the mannose-binding lectin (MBL) pathway of complement activation. , 2005, FEMS microbiology letters.

[62]  L. Schouls,et al.  Multiple-Locus Variable-Number Tandem Repeat Analysis of Neisseria meningitidis Yields Groupings Similar to Those Obtained by Multilocus Sequence Typing , 2006, Journal of Clinical Microbiology.

[63]  D. Philpott,et al.  The role of Toll-like receptors and Nod proteins in bacterial infection. , 2004, Molecular immunology.

[64]  Dexiang Chen,et al.  Isolation and Characterization of Two Proteins fromMoraxella catarrhalis That Bear a Common Epitope , 1998, Infection and Immunity.

[65]  M. Klein,et al.  The Transferrin Binding Protein B of Moraxella catarrhalis Elicits Bactericidal Antibodies and Is a Potential Vaccine Antigen , 1998, Infection and Immunity.

[66]  S. Akira,et al.  Pathogen Recognition and Innate Immunity , 2006, Cell.

[67]  A. Vergison Microbiology of otitis media: A moving target , 2008, Vaccine.

[68]  E. Hansen,et al.  Identification of Gene Products Involved in Biofilm Production by Moraxella catarrhalis ETSU-9 In Vitro , 2007, Infection and Immunity.

[69]  A. Campagnari,et al.  Construction and Characterization ofMoraxella catarrhalis Mutants Defective in Expression of Transferrin Receptors , 1999, Infection and Immunity.

[70]  J. Shao,et al.  Expression of Type IV Pili by Moraxella catarrhalis Is Essential for Natural Competence and Is Affected by Iron Limitation , 2004, Infection and Immunity.

[71]  R. M. Wooten,et al.  The Moraxella catarrhalis Autotransporter McaP Is a Conserved Surface Protein That Mediates Adherence to Human Epithelial Cells through Its N-Terminal Passenger Domain , 2006, Infection and Immunity.

[72]  T. Atkinson,et al.  Molecular evolution of bacterial cell-surface proteins. , 1993, Trends in biochemical sciences.

[73]  Song Gao,et al.  Identification of two late acyltransferase genes responsible for lipid A biosynthesis in Moraxella catarrhalis , 2008, The FEBS journal.

[74]  T. Murphy,et al.  The major heat‐modifiable outer membrane protein CD is highly conserved among strains of Branhamella catarrhalis , 1993, Molecular microbiology.

[75]  S. Gray-Owen,et al.  Bacterial transferrin and lactoferrin receptors. , 1996, Trends in microbiology.

[76]  P. Densen,et al.  Lipooligosaccharide Pk(Galα1-4Galβ1-4Glc) Epitope of Moraxella catarrhalis Is a Factor in Resistance to Bactericidal Activity Mediated by Normal Human Serum , 2000, Infection and Immunity.

[77]  J. Verhoef,et al.  Differences in complement activation between complement-resistant and complement-sensitive Moraxella (Branhamella) catarrhalis strains occur at the level of membrane attack complex formation , 1994, Infection and immunity.

[78]  J. McMichael,et al.  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 , 2007, Infection and Immunity.

[79]  M. Avery,et al.  Defined medium for Moraxella (Branhamella) catarrhalis , 1986, Applied and environmental microbiology.

[80]  J. Verhoef,et al.  Experimental evidence for Moraxella-induced penicillin neutralization in pneumococcal pneumonia. , 1994, The Journal of infectious diseases.

[81]  E. Hansen,et al.  Expression of the Moraxella catarrhalisUspA1 Protein Undergoes Phase Variation and Is Regulated at the Transcriptional Level , 2001, Journal of bacteriology.

[82]  A. Cripps,et al.  Characterization of a Novel Porin Protein from Moraxella catarrhalis and Identification of an Immunodominant Surface Loop , 2005, Journal of bacteriology.

[83]  A. S. Attia,et al.  Moraxella catarrhalis Binding to Host Cellular Receptors Is Mediated by Sequence-Specific Determinants Not Conserved among All UspA1 Protein Variants , 2008, Infection and Immunity.

[84]  A. S. Attia,et al.  A Conserved Tetranucleotide Repeat Is Necessary for Wild-Type Expression of the Moraxella catarrhalis UspA2 Protein , 2006, Journal of bacteriology.

[85]  M. Virji,et al.  A novel cell‐binding mechanism of Moraxella catarrhalis ubiquitous surface protein UspA: specific targeting of the N‐domain of carcinoembryonic antigen‐related cell adhesion molecules by UspA1 , 2003, Molecular microbiology.

[86]  E. Hansen,et al.  EXPRESSION OF THE COPB OUTER MEMBRANE PROTEIN BY MORAXELLA CATARRHALIS IS REGULATED BY IRON AND AFFECTS IRON ACQUISITION FROM TRANSFERRIN AND LACTOFERRIN. • 974 , 1996, Pediatric Research.

[87]  T. Murphy,et al.  Infection in the pathogenesis and course of chronic obstructive pulmonary disease. , 2008, The New England journal of medicine.

[88]  M. Klein,et al.  Cloning and Expression of the Moraxella catarrhalis Lactoferrin Receptor Genes , 1998, Infection and Immunity.

[89]  Zihua Hu,et al.  Mining the Moraxella catarrhalis Genome: Identification of Potential Vaccine Antigens Expressed during Human Infection , 2008, Infection and Immunity.

[90]  M. Leinonen,et al.  Human immune response against outer membrane proteins of Moraxella (Branhamella) catarrhalis determined by immunoblotting and enzyme immunoassay , 1995, Clinical and diagnostic laboratory immunology.

[91]  Ronald N. Jones,et al.  Susceptibility trends of haemophilus influenzae and Moraxella catarrhalis against orally administered antimicrobial agents: five-year report from the SENTRY Antimicrobial Surveillance Program. , 2003, Diagnostic microbiology and infectious disease.

[92]  F. Ahmad,et al.  Characterisation of Branhamella catarrhalis and differentiation from Neisseria species in a diagnostic laboratory. , 1987, Journal of clinical pathology.

[93]  A. S. Attia,et al.  Modular Arrangement of Allelic Variants Explains the Divergence in Moraxella catarrhalis UspA Protein Function , 2008, Infection and Immunity.

[94]  Shengqing Yu,et al.  Biological and Immunological Characteristics of Lipooligosaccharide-Based Conjugate Vaccines for Serotype C Moraxella catarrhalis , 2007, Infection and Immunity.

[95]  Didier Raoult,et al.  Bacterial genome sequencing and its use in infectious diseases. , 2007, The Lancet. Infectious diseases.

[96]  J. Costerton,et al.  Bacterial biofilms: a common cause of persistent infections. , 1999, Science.

[97]  A. van Belkum,et al.  Total genome polymorphism and low frequency of intra-genomic variation in the uspA1 and uspA2 genes of Moraxella catarrhalis in otitis prone and non-prone children up to 2 years of age. Consequences for vaccine design? , 2003, Vaccine.

[98]  R. Benz,et al.  Moraxella catarrhalis M35 Is a General Porin That Is Important for Growth under Nutrient-Limiting Conditions and in the Nasopharynges of Mice , 2008, Journal of bacteriology.

[99]  C. Aebi,et al.  Cold Shock Response of the UspA1 Outer Membrane Adhesin of Moraxella catarrhalis , 2005, Infection and Immunity.

[100]  B. Grant,et al.  Moraxella catarrhalis in chronic obstructive pulmonary disease: burden of disease and immune response. , 2005, American journal of respiratory and critical care medicine.

[101]  T. Logtenberg,et al.  Phage Antibodies Obtained by Competitive Selection on Complement-Resistant Moraxella (Branhamella)catarrhalis Recognize the High-Molecular-Weight Outer Membrane Protein , 1998, Infection and Immunity.

[102]  A. van Belkum,et al.  Age-related genotypic and phenotypic differences in Moraxella catarrhalis isolates from children and adults presenting with respiratory disease in 2001-2002. , 2008, Microbiology.

[103]  S. Akira,et al.  Toll-like receptors and innate immunity , 2006, Journal of Molecular Medicine.

[104]  N. Suttorp,et al.  Moraxella catarrhalis is internalized in respiratory epithelial cells by a trigger‐like mechanism and initiates a TLR2‐ and partly NOD1‐dependent inflammatory immune response , 2007, Cellular microbiology.

[105]  E. R. Lafontaine,et al.  The Moraxella catarrhalis Porin-Like Outer Membrane Protein CD Is an Adhesin for Human Lung Cells , 2004, Infection and Immunity.

[106]  T. Murphy,et al.  Bacterial Infection in Chronic Obstructive Pulmonary Disease in 2000: a State-of-the-Art Review , 2001, Clinical Microbiology Reviews.

[107]  J. Kalbfleisch,et al.  Genetic Diversity among Strains of Moraxella catarrhalis: Analysis Using Multiple DNA Probes and a Single-Locus PCR-Restriction Fragment Length Polymorphism Method , 1998, Journal of Clinical Microbiology.

[108]  Pascale Cossart,et al.  Bacterial Invasion: The Paradigms of Enteroinvasive Pathogens , 2004, Science.

[109]  E. R. Lafontaine,et al.  Hag Directly Mediates the Adherence of Moraxella catarrhalis to Human Middle Ear Cells , 2005, Infection and Immunity.

[110]  A. Campagnari,et al.  Identification of a Hemin Utilization Protein of Moraxella catarrhalis (HumA) , 2004, Infection and Immunity.

[111]  K. Riesbeck,et al.  Current progress of adhesins as vaccine candidates for Moraxella catarrhalis , 2007, Expert review of vaccines.

[112]  T. Riley,et al.  A comparison of molecular typing methods for Moraxella catarrhalis , 2007, Journal of applied microbiology.

[113]  M. Graille,et al.  Immunoglobulin-binding domains: Protein L from Peptostreptococcus magnus. , 2003, Biochemical Society transactions.

[114]  B. Grant,et al.  Airway bacterial concentrations and exacerbations of chronic obstructive pulmonary disease. , 2007, American journal of respiratory and critical care medicine.

[115]  E. Hoiczyk,et al.  Structure and sequence analysis of Yersinia YadA and Moraxella UspAs reveal a novel class of adhesins , 2000, The EMBO journal.

[116]  J. Struthers,et al.  Interaction of Streptococcus pneumoniae andMoraxella catarrhalis: Investigation of the Indirect Pathogenic Role of β-Lactamase-Producing Moraxellae by Use of a Continuous-Culture Biofilm System , 1998, Antimicrobial Agents and Chemotherapy.

[117]  A. Forsgren,et al.  The Novel IgD Binding Protein from Moraxella catarrhalis Induces Human B Lymphocyte Activation and Ig Secretion in the Presence of Th2 Cytokines1 , 2002, The Journal of Immunology.

[118]  A. S. Attia,et al.  The UspA2 Protein of Moraxella catarrhalis Is Directly Involved in the Expression of Serum Resistance , 2005, Infection and Immunity.

[119]  J. Parkhill,et al.  The Bordetellae: lessons from genomics , 2004, Nature Reviews Microbiology.

[120]  A. Campagnari,et al.  Growth of Moraxella catarrhalis with human transferrin and lactoferrin: expression of iron-repressible proteins without siderophore production , 1994, Infection and immunity.

[121]  H. Faden The microbiologic and immunologic basis for recurrent otitis media in children , 2001, European Journal of Pediatrics.

[122]  E. R. Lafontaine,et al.  Moraxella catarrhalis Strain O35E Expresses Two Filamentous Hemagglutinin-Like Proteins That Mediate Adherence to Human Epithelial Cells , 2007, Infection and Immunity.

[123]  B. Catlin Branhamella catarrhalis: an organism gaining respect as a pathogen , 1990, Clinical Microbiology Reviews.

[124]  Oscar P. Kuipers,et al.  Development of Genomic Array Footprinting for Identification of Conditionally Essential Genes in Streptococcus pneumoniae , 2007, Applied and Environmental Microbiology.

[125]  S. Gallati,et al.  Rapid typing of Moraxella catarrhalis subpopulations based on outer membrane proteins using mass spectrometry , 2006, Proteomics.

[126]  A. Forsgren,et al.  Characterization of the IgD Binding Site of Encapsulated Haemophilus influenzae Serotype b1 , 2007, The Journal of Immunology.

[127]  Patricia Siguier,et al.  Insertion sequences in prokaryotic genomes. , 2006, Current opinion in microbiology.

[128]  S. Hammarström The carcinoembryonic antigen (CEA) family: structures, suggested functions and expression in normal and malignant tissues. , 1999, Seminars in cancer biology.

[129]  E. Hansen,et al.  The UspA1 Protein and a Second Type of UspA2 Protein Mediate Adherence of Moraxella catarrhalis to Human Epithelial Cells In Vitro , 2000, Journal of bacteriology.

[130]  M. Corbel,et al.  Current progress with Moraxella catarrhalis antigens as vaccine candidates , 2009, Expert review of vaccines.

[131]  E. Hansen,et al.  A large, antigenically conserved protein on the surface of Moraxella catarrhalis is a target for protective antibodies. , 1994, The Journal of infectious diseases.

[132]  A. Wakisaka,et al.  TISSUE DISTRIBUTION OF THE PK ANTIGEN AS DETERMINED BY A MONOCLONAL ANTIBODY , 1985, Journal of immunogenetics.

[133]  B. Gibson,et al.  Identification of a 3-Deoxy-d-manno-Octulosonic Acid Biosynthetic Operon in Moraxella catarrhalis and Analysis of a KdsA-Deficient Isogenic Mutant , 2003, Infection and Immunity.

[134]  A. Forsgren,et al.  Moraxella-dependent alpha 1-antichymotrypsin neutralization: a unique virulence mechanism. , 2008, American journal of respiratory cell and molecular biology.

[135]  F. Mooi,et al.  Genesis of BRO β‐lactamase‐producing Moraxella catarrhalis: evidence for transformation‐mediated horizontal transfer , 2000, Molecular microbiology.

[136]  L. Schouls,et al.  Increase in Genetic Diversity of Haemophilus influenzae Serotype b (Hib) Strains after Introduction of Hib Vaccination in The Netherlands , 2005, Journal of Clinical Microbiology.

[137]  J. Hays,et al.  The Genus Moraxella , 2006 .

[138]  A. S. Attia,et al.  Moraxella catarrhalis Expresses an Unusual Hfq Protein , 2008, Infection and Immunity.

[139]  M. Enright,et al.  Moraxella (Branhamella) catarrhalis--clinical and molecular aspects of a rediscovered pathogen. , 1997, Journal of medical microbiology.

[140]  O. Kuipers,et al.  Search for Genes Essential for Pneumococcal Transformation: the RadA DNA Repair Protein Plays a Role in Genomic Recombination of Donor DNA , 2007, Journal of bacteriology.

[141]  G. Syrogiannopoulos,et al.  Moraxella catarrhalis strains with reduced expression of the UspA outer membrane proteins belong to a distinct subpopulation. , 2005, Vaccine.

[142]  A. Blom,et al.  The Emerging Pathogen Moraxella catarrhalis Interacts with Complement Inhibitor C4b Binding Protein through Ubiquitous Surface Proteins A1 and A21 , 2004, The Journal of Immunology.

[143]  O. Kurzai,et al.  A Functional Two-Partner Secretion System Contributes to Adhesion of Neisseria meningitidis to Epithelial Cells , 2007, Journal of bacteriology.

[144]  P. Godowski,et al.  Toll-like receptor 2–mediated NF-κB activation requires a Rac1-dependent pathway , 2000, Nature Immunology.

[145]  A. Forsgren,et al.  MID and UspA1/A2 of the human respiratory pathogen Moraxella catarrhalis, and interactions with the human host as basis for vaccine development. , 2006, Acta biochimica Polonica.

[146]  D. Rasko,et al.  Metabolic Analysis of Moraxella catarrhalis and the Effect of Selected In Vitro Growth Conditions on Global Gene Expression , 2007, Infection and Immunity.

[147]  I. Stojiljković,et al.  Iron acquisition systems in the pathogenic Neisseria , 1999, Molecular microbiology.

[148]  F. Mooi,et al.  Molecular characterization of the BRO beta-lactamase of Moraxella (Branhamella) catarrhalis , 1996, Antimicrobial agents and chemotherapy.

[149]  Wei-Gang Hu,et al.  Role of different moieties from the lipooligosaccharide molecule in biological activities of the Moraxella catarrhalis outer membrane , 2007, The FEBS journal.

[150]  E. Hansen,et al.  A mutation affecting expression of a major outer membrane protein of Moraxella catarrhalis alters serum resistance and survival in vivo. , 1993, The Journal of infectious diseases.

[151]  High-throughput amplification fragment length polymorphism (htAFLP) analysis identifies genetic lineage markers but not complement phenotype-specific markers in Moraxella catarrhalis. , 2007, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[152]  M. Vischer,et al.  A reservoir of Moraxella catarrhalis in human pharyngeal lymphoid tissue. , 2007, The Journal of infectious diseases.

[153]  C. Aebi,et al.  Outer membrane protein UspA1 and lipooligosaccharide are involved in invasion of human epithelial cells by Moraxella catarrhalis. , 2008, Microbes and infection.

[154]  Anna M. Blom,et al.  Ionic Binding of C3 to the Human Pathogen Moraxella catarrhalis Is a Unique Mechanism for Combating Innate Immunity1 , 2005, The Journal of Immunology.

[155]  C. Ratledge,et al.  Iron metabolism in pathogenic bacteria. , 2000, Annual review of microbiology.

[156]  S. Gray-Owen,et al.  CEACAM1: contact-dependent control of immunity , 2006, Nature Reviews Immunology.