Moraxella-dependent α1-antichymotrypsin neutralization: A unique virulence mechanism

American Journal of Respiratory Cell and Molecular Biology

Volumn 38, Issue 5, 2008, Pages 609-617

  Manolov, Taras ^a   Thuan, Tong Tan ^a,b   Forsgren, Arne ^a   Riesbeck, Kristian ^a  

^a LUND UNIVERSITY   (Sweden)

^b SINGAPORE GENERAL HOSPITAL   (Singapore)

Author keywords

Bacteria; Inflammation; Protease inhibitor

Indexed keywords

ALPHA 1 ANTICHYMOTRYPSIN; MEMBRANE PROTEIN; OUTER MEMBRANE PROTEIN; USPA PROTEIN, MORAXELLA CATARRHALIS;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL VIRULENCE; CONTROLLED STUDY; FLOW CYTOMETRY; HAEMOPHILUS INFLUENZAE; LUNG LAVAGE; MORAXELLA CATARRHALIS; NONHUMAN; PROTEIN BINDING; STREPTOCOCCUS PNEUMONIAE; AMINO ACID SEQUENCE; BACTERIUM ADHERENCE; BINDING SITE; CELL SEPARATION; CHEMISTRY; COMPARATIVE STUDY; GENETICS; HUMAN; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; MORAXELLACEAE INFECTION; PATHOGENICITY; PHYSIOLOGY; VIRULENCE;

BACTERIA (MICROORGANISMS); HAEMOPHILUS INFLUENZAE; MORAXELLA CATARRHALIS; STREPTOCOCCUS PNEUMONIAE;

ALPHA 1-ANTICHYMOTRYPSIN; AMINO ACID SEQUENCE; BACTERIAL ADHESION; BACTERIAL OUTER MEMBRANE PROTEINS; BINDING SITES; BRONCHOALVEOLAR LAVAGE FLUID; CELL SEPARATION; FLOW CYTOMETRY; HAEMOPHILUS INFLUENZAE; HUMANS; MOLECULAR SEQUENCE DATA; MORAXELLA (BRANHAMELLA) CATARRHALIS; MORAXELLACEAE INFECTIONS; PROTEIN BINDING; STREPTOCOCCUS PNEUMONIAE; VIRULENCE;

EID: 42949175646     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2007-0289OC     Document Type: Article

References (61)

1. Beatty K, Bieth J, Travis J. Kinetics of association of serine proteinases with native and oxidized alpha-1-proteinase inhibitor and alpha-1-antichymotrypsin. J Biol Chem 1980;255:3931-3934.
2. Cichy J, Potempa J, Chawla RK, Travis J. Stimulatory effect of inflammatory cytokines on alpha 1-antichymotrypsin expression in human lung-derived epithelial cells. J Clin Invest 1995;95:2729-2733.
3. Potempa J, Fedak D, Dubin A, Mast A, Travis J. Proteolytic inactivation of alpha-1-anti-chymotrypsin. Sites of cleavage and generation of chemotactic activity. J Biol Chem 1991;266:21482-21487.
4. Lomas DA, Stone SR, Llewellyn-Jones C, Keogan MT, Wang ZM, Rubin H, Carrell RW, Stockley RA. The control of neutrophil chemotaxis by inhibitors of cathepsin G and chymotrypsin. J Biol Chem 1995;270:23437-23443.
5. Kilpatrick L, Johnson JL, Nickbarg EB, Wang ZM, Clifford TF, Banach M, Cooperman BS, Douglas SD, Rubin H. Inhibition of human neutrophil superoxide generation by alpha 1-antichymotrypsin. J Immunol 1991;146:2388-2393.
6. Camussi G, Tetta C, Bussolino F, Baglioni C. Synthesis and release of platelet-activating factor is inhibited by plasma alpha 1-proteinase inhibitor or alpha 1-antichymotrypsin and is stimulated by proteinases. J Exp Med 1988;168:1293-1306.
7. Eriksson S. Studies in alpha 1-antitrypsin deficiency. Acta Med Scand Suppl 1965;432:1-85.
8. Ishii T, Matsuse T, Teramoto S, Matsui H, Hosoi T, Fukuchi Y, Ouchi Y. Association between alpha-1-antichymotrypsin polymorphism and susceptibility to chronic obstructive pulmonary disease. Eur J Clin Invest 2000;30:543-548.
9. Verduin CM, Hol C, Fleer A, van Dijk H, van Belkum A. Moraxella catarrhalis: from Emerging to Established Pathogen. Clin Microbiol Rev 2002;15:125-144.
10. 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 2006;53:445-456.
11. Pearson MM, Lafontaine ER, Wagner NJ, St. Geme Iii JW, Hansen EJ. A hag mutant of Moraxella catarrhalis strain O35E is deficient in hemagglutination, autoagglutination, and immunoglobulin D-binding activities. Infect Immun 2002;70:4523-4533.
12. Hill DJ, Edwards AM, Rowe HA, Virji M. Carcinoembryonic antigen-related cell adhesion molecule (CEACAM)-binding recombinant polypeptide confers protection against infection by respiratory and urogenital pathogens. Mol Microbiol 2005;55:1515-1527.
13. Tan TT, Forsgren A, Riesbeck K. The respiratory pathogen Moraxella catarrhalis binds to laminin via ubiquitous surface proteins A1 and A2. J Infect Dis 2006;194:493-497.
14. Nordström T, Blom AM, Tan TT, Forsgren A, Riesbeck K. Ionic binding of C3 to the human pathogen Moraxella catarrhalis is a unique mechanism for combating innate immunity. J Immunol 2005;175:3628-3636.
15. Siafakas NM, Tzortzaki EG. Few smokers develop COPD. Why? Respir Med 2002;96:615-624.
16. Nordström T, Blom AM, Forsgren A, Riesbeck K. The emerging pathogen Moraxella catarrhalis interacts with complement inhibitor C4b binding protein through ubiquitous surface proteins A1 and A2. J Immunol 2004;173:4598-4606.
17. McMichael JC, Fiske MJ, Fredenburg RA, Chakravarti DN, VanDerMeid KR, Barniak V, Caplan J, Bortell E, Baker S, Arumugham R, et al. Isolation and characterization of two proteins from Moraxella catarrhalis that bear a common epitope. Infect Immun 1998;66:4374-4381.
18. Tan TT, Nordström 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 2005;192:1029-1038.
19. Aebi C, Lafontaine ER, Cope LD, Latimer JL, Lumbley SL, McCracken GH Jr, Hansen EJ. Phenotypic effect of isogenic uspA1 and uspA2 mutations on Moraxella catarrhalis 035E. Infect Immun 1998;66:3113-3119.
20. 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 2005;73:2400-2410.
21. 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 2000;182:1364-1373.
22. Möllenkvist A, Nordström T, Halldén 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 2003;185:2285-2295.
23. Cope LD, Lafontaine ER, Slaughter CA, Hasemann CA Jr, Aebi C, Henderson FW, McCracken GH Jr, Hansen EJ. Characterization of the Moraxella catarrhalis uspA1 and uspA2 genes and their encoded products. J Bacteriol 1999;181:4026-4034.
24. Johnsson E, Thern A, Dahlback B, Heden LO, Wikstrom M, Lindahl G. A highly variable region in members of the streptococcal M protein family binds the human complement regulator C4BP. J Immunol 1996;157:3021-3029.
25. Travis J. Structure, function, and control of neutrophil proteinases. Am J Med 1988;84:37-42.
26. Chertov O, Ueda H, Xu LL, Tani K, Murphy WJ, Wang JM, Howard OM, Sayers TJ, Oppenheim JJ. Identification of human neutrophilderived cathepsin G and azurocidin/CAP37 as chemoattractants for mononuclear cells and neutrophils. J Exp Med 1997;186:739-747.
27. Muller HE. Proteolytic action of Legionella pneumophila on human serum proteins. Infect Immun 1980;27:51-53.
28. Catanese J, Kress LF. Enzymatic inactivation of human plasma C1-inhibitor and alpha 1-antichymotrypsin by Pseudomonas aeruginosa proteinase and elastase. Biochim Biophys Acta 1984;789:37-43.
29. Kress LF. Inactivation of human plasma serine proteinase inhibitors (serpins) by limited proteolysis of the reactive site loop with snake venom and bacterial metalloproteinases. J Cell Biochem 1986;32:51-58.
30. Grenier D. Degradation of host protease inhibitors and activation of plasminogen by proteolytic enzymes from Porphyromonas gingivalis and Treponema denticola. Microbiology 1996;142:955-961.
31. Fernie-King BA, Seilly DJ, Davies A, Lachmann PJ. Streptococcal inhibitor of complement inhibits two additional components of the mucosal innate immune system: secretory leukocyte proteinase inhibitor and lysozyme. Infect Immun 2002;70:4908-4916.
32. Rasmussen M, Muller HP, Bjorck L. Protein GRAB of streptococcus pyogenes regulates proteolysis at the bacterial surface by binding alpha2-macroglobulin. J Biol Chem 1999;274:15336-15344.
33. Toppel AW, Rasmussen M, Rohde M, Medina E, Chhatwal GS. Contribution of protein G-related alpha2-macroglobulin-binding protein to bacterial virulence in a mouse skin model of group A streptococcal infection. J Infect Dis 2003;187:1694-1703.
34. Heusipp G, Spekker K, Brast S, Falker S, Schmidt MA. YopM of Yersinia enterocolitica specifically interacts with alpha1-antitrypsin without affecting the anti-protease activity. Microbiology 2006;152:1327-1335.
35. Knappstein S, Ide T, Schmidt MA, Heusipp G. falphag1-Antitrypsin binds to and interferes with functionality of EspB from atypical and typical enteropathogenic Escherichia coli strains. Infect Immun 2004;72:4344-4350.
36. 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 1994;169:1312-1317.
37. Aniansson G, Alm B, Andersson B, Larsson P, Nylen O, Peterson H, Rigner P, Svanborg M, Svanborg C. Nasopharyngeal colonization during the first year of life. J Infect Dis 1992;165:S38-S42.
38. Leach AJ, Boswell JB, Asche V, Nienhuys TG, Mathews JD. Bacterial colonization of the nasopharynx predicts very early onset and persistence of otitis media in Australian aboriginal infants. Pediatr Infect Dis J 1994;13:983-989.
39. Faden H, Duffy L, Wasielewski R, Wolf J, Krystofik D, Tung Y. Relationship between nasopharyngeal colonization and the development of otitis media in children. Tonawanda/Williamsville Pediatrics. J Infect Dis 1997;175:1440-1445.
40. Vives M, Garcia ME, Saenz P, Mora MA, Mata L, Sabharwal H, Svanborg C. Nasopharyngeal colonization in Costa Rican children during the first year of life. Pediatr Infect Dis J 1997;16:852-858.
41. MacIvor DM, Shapiro SD, Pham CT, Belaaouaj A, Abraham SN, Ley TJ. Normal neutrophil function in cathepsin G-deficient mice. Blood 1999;94:4282-4293.
42. Sedor J, Hogue L, Akers K, Boslaugh S, Schreiber J, Ferkol T. Cathepsin-G interferes with clearance of Pseudomonas aeruginosa from mouse lungs. Pediatr Res 2007;61:26-31.
43. Fick RB Jr, Naegel GP, Squier SU, Wood RE, Gee JB, Reynolds HY. Proteins of the cystic fibrosis respiratory tract. Fragmented immunoglobulin G opsonic antibody causing defective opsonophagocytosis. J Clin Invest 1984;74:236-248.
44. Tosi MF, Zakem H, Berger M. Neutrophil elastase cleaves C3bi on opsonized pseudomonas as well as CR1 on neutrophils to create a functionally important opsonin receptor mismatch. J Clin Invest 1990;86:300-308.
45. Tkalcevic J, Novelli M, Phylactides M, Iredale JP, Segal AW, Roes J. Impaired immunity and enhanced resistance to endotoxin in the absence of neutrophil elastase and cathepsin G. Immunity 2000;12:201-210.
46. Shafer WM, Onunka VC, Martin LE. Antigonococcal activity of human neutrophil cathepsin G. Infect Immun 1986;54:184-188.
47. Papi A, Bellettato CM, Braccioni F, Romagnoli M, Casolari P, Caramori G, Fabbri LM, Johnston SL. Infections and airway inflammation in chronic obstructive pulmonary disease severe exacerbations. Am J Respir Crit Care Med 2006;173:1114-1121.
48. Sethi S, Muscarella K, Evans N, Klingman KL, Grant BJ, Murphy TF. Airway inflammation and etiology of acute exacerbations of chronic bronchitis. Chest 2000;118:1557-1565.
49. Wedzicha JA. Role of viruses in exacerbations of chronic obstructive pulmonary disease. Proc Am Thorac Soc 2004;1:115-120.
50. Wright JL, Churg A. Advances in the pathology of COPD. Histopathology 2006;49:1-9.
51. Larsson C. Natural history and life expectancy in severe alpha1-antitrypsin deficiency, Pi Z. Acta Med Scand 1978;204:345-351.
52. Demeo DL, Mariani TJ, Lange C, Srisuma S, Litonjua AA, Celedon JC, Lake SL, Reilly JJ, Chapman HA, Mecham BH, et al. The SERPINE2 gene is associated with chronic obstructive pulmonary disease. Am J Hum Genet 2006;78:253-264.
53. Poller W, Faber JP, Weidinger S, Tief K, Scholz S, Fischer M, Olek K, Kirchgesser M, Heidtmann HH. A leucine-to-proline substitution causes a defective alpha 1-antichymotrypsin allele associated with familial obstructive lung disease. Genomics 1993;17:740-743.
54. Sandford AJ, Chagani T, Weir TD, Pare PD. Alpha 1-antichymotrypsin mutations in patients with chronic obstructive pulmonary disease. Dis Markers 1998;13:257-260.
55. Samilchuk EI, Chuchalin AG. Mis-sense mutation of alpha 1-antichymotrypsin gene and chronic lung disease. Lancet 1993;342:624.
56. Smith CE, Stack MS, Johnson DA. Ozone effects on inhibitors of human neutrophil proteinases. Arch Biochem Biophys 1987;253:146-155.
57. Chang WS, Lomas DA. Latent alpha1-antichymotrypsin: a molecular explanation for the inactivation of alpha1-antichymotrypsin in chronic bronchitis and emphysema. J Biol Chem 1998;273:3695-3701.
58. Korkmaz B, Poutrain P, Hazouard E, de Monte M, Attucci S, Gauthier FL. Competition between elastase and related proteases from human neutrophil for binding to alpha1-protease inhibitor. Am J Respir Cell Mol Biol 2005;32:553-559.
59. Liou TG, Campbell EJ. Nonisotropic enzyme-inhibitor interactions: a novel nonoxidative mechanism for quantum proteolysis by human neutrophils. Biochemistry 1995;34:16171-16177.
60. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994;22:4673-4680.
61. Hallström T, Trajkovska E, Forsgren A, Riesbeck K. Haemophilus influenzae surface fibrils contribute to serum resistance by interacting with vitronectin. J Immunol 2006;177:430-436.