Immune evasion of Moraxella catarrhalis involves ubiquitous surface protein A-dependent C3d binding

Journal of Immunology

Volumn 186, Issue 5, 2011, Pages 3120-3129

  Hallström, Teresia ^a,b   Nordström, Therése ^a   Tan, Thuan Tong ^a   Manolov, Taras ^a   Lambris, John D ^c   Isenman, David E ^d   Zipfel, Peter F ^b   Blom, Anna M ^a   Riesbeck, Kristian ^a  

^a LUND UNIVERSITY   (Sweden)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C3A; COMPLEMENT COMPONENT C3B; COMPLEMENT COMPONENT C3D; MEMBRANE PROTEIN; UBIQUITOUS SURFACE PROTEIN A1; UBIQUITOUS SURFACE PROTEIN A2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING SITE; COMPLEMENT ACTIVATION; CONTROLLED STUDY; IMMUNE EVASION; IMMUNITY; MORAXELLA CATARRHALIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION;

ADULT; ANIMALS; ANTIGENS, BACTERIAL; ANTIGENS, SURFACE; BACTERIAL OUTER MEMBRANE PROTEINS; CHILD; COMPLEMENT ACTIVATION; COMPLEMENT C3A; COMPLEMENT C3D; COMPLEMENT INACTIVATOR PROTEINS; COMPLEMENT PATHWAY, ALTERNATIVE; HUMANS; IMMUNE EVASION; INFLAMMATION; MICE; MORAXELLA (BRANHAMELLA) CATARRHALIS; MORAXELLACEAE INFECTIONS; PROTEIN BINDING; RABBITS; SHEEP;

EID: 79952773851     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1002621     Document Type: Article

References (83)

1. Perez Vidakovics, M. L., and K. Riesbeck. 2009. Virulence mechanisms of Moraxella in the pathogenesis of infection. Curr. Opin. Infect. Dis. 22: 279-285.
2. Yamanaka, N., M. Hotomi, and D. S. Billal. 2008. Clinical bacteriology and immunology in acute otitis media in children. J. Infect. Chemother. 14: 180-187.
3. Catlin, B. W. 1990. Branhamella catarrhalis: an organism gaining respect as a pathogen. Clin. Microbiol. Rev. 3: 293-320.
4. Murphy, T. F., and G. I. Parameswaran. 2009. Moraxella catarrhalis, a human respiratory tract pathogen. Clin. Infect. Dis. 49: 124-131.
5. Sethi, S., and T. F. Murphy. 2001. Bacterial infection in chronic obstructive pulmonary disease in 2000: a state-of-the-art review. Clin. Microbiol. Rev. 14: 336-363.
6. Murphy, T. F., A. L. Brauer, B. J. Grant, and S. Sethi. 2005. Moraxella catarrhalis in chronic obstructive pulmonary disease: burden of disease and immune response. Am. J. Respir. Crit. Care Med. 172: 195-199.
7. de Vries, S. P., H. J. Bootsma, J. P. Hays, and P. W. Hermans. 2009. Molecular aspects of Moraxella catarrhalis pathogenesis. Microbiol. Mol. Biol. Rev. 73: 389-406.
8. McMichael, J. C. 2000. Vaccines for Moraxella catarrhalis. Vaccine 19(Suppl. 1): S101-S107. (Pubitemid 32121729)
9. Tan, T. T., and K. Riesbeck. 2007. Current progress of adhesins as vaccine candidates for Moraxella catarrhalis. Expert Rev. Vaccines 6: 949-956. (Pubitemid 350260658)
10. Aebi, C., E. R. Lafontaine, L. D. Cope, J. L. Latimer, S. L. Lumbley, G. H. McCracken, Jr., and E. J. Hansen. 1998. Phenotypic effect of isogenic uspA1 and uspA2 mutations on Moraxella catarrhalis 035E. Infect. Immun. 66: 3113-3119.
11. Forsgren, A., M. Brant, M. Karamehmedovic, and K. Riesbeck. 2003. The immunoglobulin D-binding protein MID from Moraxella catarrhalis is also an adhesin. Infect. Immun. 71: 3302-3309.
12. Forsgren, A., M. Brant, A. Möllenkvist, A. Muyombwe, H. Janson, N. Woin, and K. Riesbeck. 2001. Isolation and characterization of a novel IgD-binding protein from Moraxella catarrhalis. J. Immunol. 167: 2112-2120. (Pubitemid 32747520)
13. Holm, M. M., S. L. Vanlerberg, I. M. Foley, D. D. Sledjeski, and E. R. Lafontaine. 2004. The Moraxella catarrhalis porin-like outer membrane protein CD is an adhesin for human lung cells. Infect. Immun. 72: 1906-1913.
14. Pearson, M. M., E. R. Lafontaine, N. J. Wagner, J. W. St Geme, III, and E. J. Hansen. 2002. A hag mutant of Moraxella catarrhalis strain O35E is deficient in hemagglutination, autoagglutination, and immunoglobulin D-binding activities. Infect. Immun. 70: 4523-4533.
15. Timpe, J. M., M. M. Holm, S. L. Vanlerberg, V. Basrur, and E. R. Lafontaine. 2003. Identification of a Moraxella catarrhalis outer membrane protein exhibiting both adhesin and lipolytic activities. Infect. Immun. 71: 4341-4350.
16. Aebi, C., I. Maciver, J. L. Latimer, L. D. Cope, M. K. Stevens, S. E. Thomas, G. H. McCracken, Jr., and E. J. Hansen. 1997. A protective epitope of Moraxella catarrhalis is encoded by two different genes. Infect. Immun. 65: 4367-4377.
17. Lafontaine, E. R., L. D. Cope, C. Aebi, J. L. Latimer, G. H. McCracken, Jr., and E. J. Hansen. 2000. The UspA1 protein and a second type of UspA2 protein mediate adherence of Moraxella catarrhalis to human epithelial cells in vitro. J. Bacteriol. 182: 1364-1373.
18. Karalus, R., and A. Campagnari. 2000. Moraxella catarrhalis: a review of an important human mucosal pathogen. Microbes Infect. 2: 547-559. (Pubitemid 30387209)
19. Brooks, M. J., J. L. Sedillo, N. Wagner, C. A. Laurence, W. Wang, A. S. Attia, E. J. Hansen, and S. D. Gray-Owen. 2008. Modular arrangement of allelic variants explains the divergence in Moraxella catarrhalis UspA protein function. Infect. Immun. 76: 5330-5340.
20. Hoiczyk, E., A. Roggenkamp, M. Reichenbecher, A. Lupas, and J. Heesemann. 2000. Structure and sequence analysis of Yersinia YadA and Moraxella UspAs reveal a novel class of adhesins. EMBO J. 19: 5989-5999.
21. Cope, L. D., E. R. Lafontaine, C. A. Slaughter, C. A. Hasemann, Jr., C. Aebi, F. W. Henderson, G. H. McCracken, Jr., and E. J. Hansen. 1999. Characterization of the Moraxella catarrhalis uspA1 and uspA2 genes and their encoded products. J. Bacteriol. 181: 4026-4034.
22. McMichael, J. C., M. J. Fiske, R. A. Fredenburg, D. N. Chakravarti, K. R. VanDerMeid, V. Barniak, J. Caplan, E. Bortell, S. Baker, R. Arumugham, and D. Chen. 1998. Isolation and characterization of two proteins from Moraxella catarrhalis that bear a common epitope. Infect. Immun. 66: 4374-4381.
23. Tan, T. T., A. Forsgren, and K. Riesbeck. 2006. The respiratory pathogen moraxella catarrhalis binds to laminin via ubiquitous surface proteins A1 and A2. J. Infect. Dis. 194: 493-497.
24. Tan, T. T., T. Nordström, A. Forsgren, and K. Riesbeck. 2005. The respiratory pathogen Moraxella catarrhalis adheres to epithelial cells by interacting with fibronectin through ubiquitous surface proteins A1 and A2. J. Infect. Dis. 192: 1029-1038.
25. Attia, A. S., S. Ram, P. A. Rice, and E. J. Hansen. 2006. Binding of vitronectin by the Moraxella catarrhalis UspA2 protein interferes with late stages of the complement cascade. Infect. Immun. 74: 1597-1611.
26. Nordström, T., A. M. Blom, A. Forsgren, and K. Riesbeck. 2004. The emerging pathogen Moraxella catarrhalis interacts with complement inhibitor C4b binding protein through ubiquitous surface proteins A1 and A2. J. Immunol. 173: 4598-4606. (Pubitemid 39280693)
27. Nordström, T., A. M. Blom, T. T. Tan, A. Forsgren, and K. Riesbeck. 2005. Ionic binding of C3 to the human pathogen Moraxella catarrhalis is a unique mechanism for combating innate immunity. J. Immunol. 175: 3628-3636. (Pubitemid 41292022)
28. Singh, B., A. M. Blom, C. Unal, B. Nilson, M. Mörgelin, and K. Riesbeck. 2010. Vitronectin binds to the head region of Moraxella catarrhalis ubiquitous surface protein A2 and confers complement-inhibitory activity. Mol. Microbiol. 75: 1426-1444.
29. Chen, D., V. Barniak, K. R. VanDerMeid, and J. C. McMichael. 1999. 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: 1310-1316.
30. Tan, T. T., J. J. Christensen, M. H. Dziegiel, A. Forsgren, and K. Riesbeck. 2006. Comparison of the serological responses to Moraxella catarrhalis immunoglobulin D-binding outer membrane protein and the ubiquitous surface proteins A1 and A2. Infect. Immun. 74: 6377-6386.
31. Volanakis, J. E. 2001. Human C-reactive protein: expression, structure, and function. Mol. Immunol. 38: 189-197.
32. Walport, M. J. 2001. Complement: first of two parts. N. Engl. J. Med. 344: 1058-1066.
33. Lambris, J. D. 1988. The multifunctional role of C3, the third component of complement. Immunol. Today 9: 387-393.
34. Gros, P., F. J. Milder, and B. J. Janssen. 2008. Complement driven by conformational changes. Nat. Rev. Immunol. 8: 48-58.
35. Sahu, A., and J. D. Lambris. 2001. Structure and biology of complement protein C3, a connecting link between innate and acquired immunity. Immunol. Rev. 180: 35-48.
36. S. Reis, E., D. A. Falcão, and L. Isaac. 2006. Clinical aspects and molecular basis of primary deficiencies of complement component C3 and its regulatory proteins factor I and factor H. Scand. J. Immunol. 63: 155-168.
37. Zipfel, P. F., and C. Skerka. 2009. Complement regulators and inhibitory proteins. Nat. Rev. Immunol. 9: 729-740.
38. Blom, A. M., T. Hallström, and K. Riesbeck. 2009. Complement evasion strategies of pathogens: acquisition of inhibitors and beyond. Mol. Immunol. 46: 2808-2817.
39. Lambris, J. D., D. Ricklin, and B. V. Geisbrecht. 2008. Complement evasion by human pathogens. Nat. Rev. Microbiol. 6: 132-142.
40. Rooijakkers, S. H., and J. A. van Strijp. 2007. Bacterial complement evasion. Mol. Immunol. 44: 23-32.
41. Zipfel, P. F., R. Würzner, and C. Skerka. 2007. Complement evasion of pathogens: common strategies are shared by diverse organisms. Mol. Immunol. 44: 3850-3857.
42. Dieudonné-Vatran, A., S. Krentz, A. M. Blom, S. Meri, B. Henriques-Normark, K. Riesbeck, and B. Albiger. 2009. Clinical isolates of Streptococcus pneumoniae bind the complement inhibitor C4b-binding protein in a PspC alleledependent fashion. J. Immunol. 182: 7865-7877.
43. Hallström, T., H. Jarva, K. Riesbeck, and A. M. Blom. 2007. Interaction with C4b-binding protein contributes to nontypeable Haemophilus influenzae serum resistance. J. Immunol. 178: 6359-6366.
44. Hallström, T., P. F. Zipfel, A. M. Blom, N. Lauer, A. Forsgren, and K. Riesbeck. 2008. Haemophilus influenzae interacts with the human complement inhibitor factor H. J. Immunol. 181: 537-545.
45. Horstmann, R. D., H. J. Sievertsen, J. Knobloch, and V. A. Fischetti. 1988. Antiphagocytic activity of streptococcal M protein: selective binding of complement control protein factor H. Proc. Natl. Acad. Sci. USA 85: 1657-1661.
46. Jarva, H., R. Janulczyk, J. Hellwage, P. F. Zipfel, L. Björck, and S. Meri. 2002. Streptococcus pneumoniae evades complement attack and opsonophagocytosis by expressing the pspC locus-encoded Hic protein that binds to short consensus repeats 8-11 of factor H. J. Immunol. 168: 1886-1894. (Pubitemid 34135790)
47. Jarva, H., S. Ram, U. Vogel, A. M. Blom, and S. Meri. 2005. Binding of the complement inhibitor C4bp to serogroup B Neisseria meningitidis. J. Immunol. 174: 6299-6307. (Pubitemid 40663822)
48. Madico, G., J. A. Welsch, L. A. Lewis, A. McNaughton, D. H. Perlman, C. E. Costello, J. Ngampasutadol, U. Vogel, D. M. Granoff, and S. Ram. 2006. The meningococcal vaccine candidate GNA1870 binds the complement regulatory protein factor H and enhances serum resistance. J. Immunol. 177: 501-510. (Pubitemid 43939163)
49. Thern, A., L. Stenberg, B. Dahlbäck, and G. Lindahl. 1995. Ig-binding surface proteins of Streptococcus pyogenes also bind human C4b-binding protein (C4BP), a regulatory component of the complement system. J. Immunol. 154: 375-386.
50. Laarman, A., F. Milder, J. van Strijp, and S. Rooijakkers. 2010. Complement inhibition by Gram-positive pathogens: molecular mechanisms and therapeutic implications. J. Mol. Med. 88: 115-120.
51. Lee, L. Y., X. Liang, M. Höök, and E. L. Brown. 2004. Identification and characterization of the C3 binding domain of the Staphylococcus aureus extracellular fibrinogen-binding protein (Efb). J. Biol. Chem. 279: 50710-50716.
52. Luo, S., A. Hartmann, H. M. Dahse, C. Skerka, and P. F. Zipfel. 2010. Secreted pH-regulated antigen 1 of Candida albicans blocks activation and conversion of complement C3. J. Immunol. 185: 2164-2173.
53. Schenkein, H. A., H. M. Fletcher, M. Bodnar, and F. L. Macrina. 1995. Increased opsonization of a prtH-defective mutant of Porphyromonas gingivalis W83 is caused by reduced degradation of complement-derived opsonins. J. Immunol. 154: 5331-5337.
54. Stover, C. K., X. Q. Pham, A. L. Erwin, S. D. Mizoguchi, P. Warrener, M. J. Hickey, F. S. Brinkman, W. O. Hufnagle, D. J. Kowalik, M. Lagrou, et al. 2000. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406: 959-964.
55. Burman, J. D., E. Leung, K. L. Atkins, M. N. O'Seaghdha, L. Lango, P. Bernadó, S. Bagby, D. I. Svergun, T. J. Foster, D. E. Isenman, and J. M. van den Elsen. 2008. Interaction of human complement with Sbi, a staphylococcal immunoglobulin-binding protein: indications of a novel mechanism of complement evasion by Staphylococcus aureus. J. Biol. Chem. 283: 17579-17593.
56. Hammel, M., G. Sfyroera, S. Pyrpassopoulos, D. Ricklin, K. X. Ramyar, M. Pop, Z. Jin, J. D. Lambris, and B. V. Geisbrecht. 2007. Characterization of Ehp, a secreted complement inhibitory protein from Staphylococcus aureus. J. Biol. Chem. 282: 30051-30061.
57. Hammel, M., G. Sfyroera, D. Ricklin, P. Magotti, J. D. Lambris, and B. V. Geisbrecht. 2007. A structural basis for complement inhibition by Staphylococcus aureus. Nat. Immunol. 8: 430-437.
58. Rooijakkers, S. H., M. Ruyken, A. Roos, M. R. Daha, J. S. Presanis, R. B. Sim, W. J. van Wamel, K. P. van Kessel, and J. A. van Strijp. 2005. Immune evasion by a staphylococcal complement inhibitor that acts on C3 convertases. Nat. Immunol. 6: 920-927.
59. Rooijakkers, S. H., J. Wu, M. Ruyken, R. van Domselaar, K. L. Planken, A. Tzekou, D. Ricklin, J. D. Lambris, B. J. Janssen, J. A. van Strijp, and P. Gros. 2009. Structural and functional implications of the alternative complement pathway C3 convertase stabilized by a staphylococcal inhibitor. Nat. Immunol. 10: 721-727.
60. Potempa, M., J. Potempa, T. Kantyka, K. A. Nguyen, K. Wawrzonek, S. P. Manandhar, K. Popadiak, K. Riesbeck, S. Eick, and A. M. Blom. 2009. Interpain A, a cysteine proteinase from Prevotella intermedia, inhibits complement by degrading complement factor C3. PLoS Pathog. 5: e1000316.
61. Möllenkvist, A., T. Nordström, C. Halldén, J. J. Christensen, A. Forsgren, and K. Riesbeck. 2003. The Moraxella catarrhalis immunoglobulin D-binding protein MID has conserved sequences and is regulated by a mechanism corresponding to phase variation. J. Bacteriol. 185: 2285-2295. (Pubitemid 36363190)
62. de Vries, S. P., S. A. van Hijum, W. Schueler, K. Riesbeck, J. P. Hays, P. W. Hermans, and H. J. Bootsma. 2010. Genome analysis of Moraxella catarrhalis strain RH4, a human respiratory tract pathogen. J. Bacteriol. 192: 3574-3583.
63. Nagar, B., R. G. Jones, R. J. Diefenbach, D. E. Isenman, and J. M. Rini. 1998. X-ray crystal structure of C3d: a C3 fragment and ligand for complement receptor 2. Science 280: 1277-1281.
64. Giclas, P. C. 2001. Classical pathway evaluation. Curr. Protoc. Immunol. Chapter 13: Unit13.1.
65. Roos, A., L. H. Bouwman, J. Munoz, T. Zuiverloon, M. C. Faber-Krol, F. C. Fallaux-van den Houten, N. Klar-Mohamad, C. E. Hack, M. G. Tilanus, and M. R. Daha. 2003. Functional characterization of the lectin pathway of complement in human serum. Mol. Immunol. 39: 655-668.
66. 131I-labelled human growth hormone of high specific radioactivity. Biochem. J. 89: 114-123.
67. Rautemaa, R., and S. Meri. 1999. Complement-resistance mechanisms of bacteria. Microbes Infect. 1: 785-794.
68. Hol, C., C. M. Verduin, E. E. Van Dijke, J. Verhoef, A. Fleer, and H. van Dijk. 1995. Complement resistance is a virulence factor of Branhamella (Moraxella) catarrhalis. FEMS Immunol. Med. Microbiol. 11: 207-211.
69. Greiff, L., M. Andersson, J. S. Erjefält, C. G. Persson, and P. Wollmer. 2003. Airway microvascular extravasation and luminal entry of plasma. Clin. Physiol. Funct. Imaging 23: 301-306.
70. Greiff, L., I. Erjefält, C. Svensson, P. Wollmer, U. Alkner, M. Andersson, and C. G. Persson. 1993. Plasma exudation and solute absorption across the airway mucosa. Clin. Physiol. 13: 219-233.
71. Persson, C. G., I. Erjefält, U. Alkner, C. Baumgarten, L. Greiff, B. Gustafsson, A. Luts, U. Pipkorn, F. Sundler, C. Svensson, et al. 1991. Plasma exudation as a first line respiratory mucosal defence. Clin. Exp. Allergy 21: 17-24.
72. Aebi, C., L. D. Cope, J. L. Latimer, S. E. Thomas, C. A. Slaughter, G. H. McCracken, Jr., and E. J. Hansen. 1998. Mapping of a protective epitope of the CopB outer membrane protein of Moraxella catarrhalis. Infect. Immun. 66: 540-548.
73. Bhushan, R., R. Craigie, and T. F. Murphy. 1994. Molecular cloning and characterization of outer membrane protein E of Moraxella (Branhamella) catarrhalis. J. Bacteriol. 176: 6636-6643.
74. Frank, M. M., and L. F. Fries. 1991. The role of complement in inflammation and phagocytosis. Immunol. Today 12: 322-326.
75. Vogt, W. 1974. Activation, activities and pharmacologically active products of complement. Pharmacol. Rev. 26: 125-169.
76. Carroll, M. C. 2004. The complement system in regulation of adaptive immunity. Nat. Immunol. 5: 981-986.
77. Cheng, Q., D. Finkel, and M. K. Hostetter. 2000. Novel purification scheme and functions for a C3-binding protein from Streptococcus pneumoniae. Biochemistry 39: 5450-5457.
78. Heidenreich, F., and M. P. Dierich. 1985. Candida albicans and Candida stellatoidea, in contrast to other Candida species, bind iC3b and C3d but not C3b. Infect. Immun. 50: 598-600.
79. Lee, L. Y., M. Höök, D. Haviland, R. A. Wetsel, E. O. Yonter, P. Syribeys, J. Vernachio, and E. L. Brown. 2004. Inhibition of complement activation by a secreted Staphylococcus aureus protein. J. Infect. Dis. 190: 571-579.
80. Upadhyay, A., J. D. Burman, E. A. Clark, E. Leung, D. E. Isenman, J. M. van den Elsen, and S. Bagby. 2008. Structure-function analysis of the C3 binding region of Staphylococcus aureus immune subversion protein Sbi. J. Biol. Chem. 283: 22113-22120.
81. Isenman, D. E., E. Leung, J. D. Mackay, S. Bagby, and J. M. van den Elsen. 2010. Mutational analyses reveal that the staphylococcal immune evasion molecule Sbi and complement receptor 2 (CR2) share overlapping contact residues on C3d: implications for the controversy regarding the CR2/C3d cocrystal structure. J. Immunol. 184: 1946-1955.
82. Ricklin, D., S. K. Ricklin-Lichtsteiner, M. M. Markiewski, B. V. Geisbrecht, and J. D. Lambris. 2008. Cutting edge: members of the Staphylococcus aureus extracellular fibrinogen-binding protein family inhibit the interaction of C3d with complement receptor 2. J. Immunol. 181: 7463-7467.
83. Helminen, M. E., I. Maciver, J. L. Latimer, J. Klesney-Tait, L. D. Cope, M. Paris, G. H. McCracken, Jr., and E. J. Hansen. 1994. A large, antigenically conserved protein on the surface of Moraxella catarrhalis is a target for protective antibodies. J. Infect. Dis. 170: 867-872.