Pulmonary collectins selectively permeabilize model bacterial membranes containing rough lipopolysaccharide

Biochemistry

Volumn 45, Issue 8, 2006, Pages 2679-2685

  Kuzmenko, Alexander I ^a   Wu, Huixing ^a   McCormack, Francis X ^a,b  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF CINCINNATI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; CELL MEMBRANES; LIPIDS; PROTEINS; PULMONARY DISEASES; QUENCHING; SUGARS; SURFACE ACTIVE AGENTS;

BACTERIAL MEMBRANES; LIPOSOMES; PERMEABILIZE MODEL; PULMONARY COLLECTINS;

BACTERIOLOGY;

2 OLEOYL 1 PALMITOYLGLYCEROPHOSPHORYLETHANOLAMINE; BACTERIUM LIPOPOLYSACCHARIDE; CALCIUM; CARBONYL DERIVATIVE; CHOLESTEROL; COLLECTIN; LIPOSOME; MELITTIN; PHOSPHOLIPID; SURFACTANT PROTEIN A; SURFACTANT PROTEIN D; UNCLASSIFIED DRUG;

ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL MEMBRANE; ESCHERICHIA COLI; FLUORESCENCE MICROSCOPY; HAEMOPHILUS INFLUENZAE; LIPID PEROXIDATION; MEMBRANE PERMEABILITY; MEMBRANE STRUCTURE; MEMBRANE VESICLE; NONHUMAN; OPSONIZATION; PHOSPHOLIPID MEMBRANE; PRIORITY JOURNAL; PROTEIN PURIFICATION; STATISTICAL ANALYSIS;

ANIMALS; CALCIUM; CELL MEMBRANE PERMEABILITY; CHOLESTEROL; COLLECTINS; ESCHERICHIA COLI; FLUORESCENT DYES; HUMANS; LIPID PEROXIDATION; LIPOPOLYSACCHARIDES; LIPOSOMES; LUNG; MODELS, BIOLOGICAL; O ANTIGENS; PHOSPHATIDYLETHANOLAMINES; PULMONARY SURFACTANT-ASSOCIATED PROTEIN A; PULMONARY SURFACTANT-ASSOCIATED PROTEIN D; RATS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; HAEMOPHILUS INFLUENZAE; NEGIBACTERIA;

EID: 33644503860     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0522652     Document Type: Article

References (36)

1. McCormack, F. X., and Whitsett, J. A. (2002) The pulmonary collectins, SP-A and SP-D, orchestrate innate immunity in the lung, J. Clin. Invest. 109, 707-712.
2. McCormack, F. X., Gibbons, R., Ward, S. R., Kuzmenko, A., Wu, H., and Deepe, G. S., Jr. (2003) Macrophage-independent fungicidal action of the pulmonary collectins, J. Biol. Chem. 278, 36250-36256.
3. Wu, H., Kuzmenko, A., Wan, S., Schaffer, L., Weiss, A., Fisher, J. H., Kim, K. S., and McCormack, F. X. (2003) Surfactant proteins A and D inhibit the growth of Gram-negative bacteria by increasing membrane permeability, J. Clin. Invest. 111, 1589-1602.
4. Weiss, J., Beckerdite-Quagliata, S., and Elsbach, P. (1980) Resistance of Gram-negative bacteria to purified bactericidal leukocyte proteins: Relation to binding and bacterial lipopolysaccharide structure, J. Clin. Invest. 65, 619-628.
5. Kuzmenko, A. I., Wu, H., Wan, S., and McCormack, F. X. (2005) Surfactant protein A is a principal and oxidation-sensitive microbial permeabilizing factor in the alveolar lining fluid, J. Biol. Chem. 280, 25913-25919.
6. Yeaman, M. R., and Yount, N. Y. (2003) Mechanisms of antimicrobial peptide action and resistance, Pharmacol. Rev. 55, 27-55.
7. Lohner, K., and Blondelle, S. E. (2005) Molecular mechanisms of membrane perturbation by antimicrobial peptides and the use of biophysical studies in the design of novel peptide antibiotics, Comb. Chem. High Throughput Screening 8, 241-256.
8. Palaniyar, N., Ridsdale, R. A., Holterman, C. E., Inchley, K., Possmayer, F., and Harauz, G. (1998) Structural changes of surfactant protein A induced by cations reorient the protein on lipid bilayers, J. Struct. Biol. 122, 297-310.
9. Kabha, K., Schmegner, J., Keisari, Y., Parolis, H., Schlepper-Schaeffer, J., and Ofek, I. (1997) SP-A enhances phagocytosis of Klebsiella by interaction with capsular polysaccharides and alveolar macrophages, Am. J. Physiol. 272, L344-L352.
10. Kuroki, Y., and Akino, T. (1991) Pulmonary surfactant protein A (SP-A) specifically binds dipalmitoylphosphatidylcholine, J. Biol. Chem. 266, 3068-3073.
11. Petsson, A. V., Gibbons, B. J., Shoemaker, J. D., Moxley, M. A., and Longmore, W. J. (1992) The major glycolipid recognized by SP-D in surfactant is phosphatidylinositol, Biochemistry 31, 12183-12189.
12. McNeely, T. B., and Coonrod, J. D. (1994) Aggregation and opsonization of type A but not type B Haemophilus influenzae by surfactant protein A, Am. J. Respir. Cell Mol. Biol. 11, 114-122.
13. Watson, R. W., Redmond, H. P., and Bouchier-Hayes, D. (1994) Role of endotoxin in mononuclear phagocyte-mediated inflammatory responses, J. Leukocyte Biol. 56, 95-103.
14. van Iwaarden, J. F., Pikaar, J. C., Storm, J., Brouwer, E., Verhoef, J., Oosting, R. S., van Golde, L. M., and Van Strijp, J. A. (1994) Binding of surfactant protein A to the lipid A moiety of bacterial lipopolysaccharides, Biochem. J. 303 (Part 2), 407-411.
15. Kuan, S. F., Rust, K., and Crouch, E. (1992) Interactions of surfactant protein D with bacterial lipopolysaccharides. Surfactant protein D is an Escherichia coli-binding protein in bronchoalveolar lavage, J. Clin. Invest. 90, 97-106.
16. Hattori, A., Kuroki, Y., Katoh, T., Takahashi, H., Shen, H. Q., Suzuki, Y., and Akino, T. (1996) Surfactant protein A accumulating in the alveoli of patients with pulmonary alveolar proteinosis: Oligomeric structure and interaction with lipids, Am. J. Respir. Cell Mol. Biol. 14, 608-619.
17. Suwabe, A., Mason, R. J., and Voelker, D. R. (1991) Temporal segregation of surfactant secretion and lamellar body biogenesis in primary cultures of rat alveolar type II cells, Am. J. Respir. Cell Mol. Biol. 5, 80-86.
18. Kuzmenko, A. I., Wu, H., Bridges, J. P., and McCormack, F. X. (2004) Surfactant lipid peroxidation damages surfactant protein A and inhibits interactions with phospholipid vesicles, J. Lipid Res. 45, 1061-1068.
19. Gregoriadis, G., and Ryman, B. E. (1972) Lysosomal localization of β-fructofuranosidase-containing liposomes injected into rats, Biochem. J. 129, 123-133.
20. Ofek, I., Mesika, A., Kalina, M., Keisari, Y., Podschun, R., Sahly, H., Chang, D., McGregor, D., and Crouch, E. (2001) Surfactant protein D enhances phagocytosis and killing of unencapsulated phase variants of Klebsiella pneumoniae, Infect. Immun. 69, 24-33.
21. Yong, S. J., Vuk-Pavlovic, Z., Standing, J. E., Crouch, E. C., and Limper, A. H. (2003) Surfactant protein D-mediated aggregation of Pneumocystis carinii impairs phagocytosis by alveolar macrophages, Infect. Immun. 71, 1662-1671.
22. Portlock, S. H., Clague, M. J., and Cherry, R. J. (1990) Leakage of internal markers from erythrocytes and lipid vesicles induced by melittin, gramicidin S and alamethicin: A comparative study, Biochim. Biophys. Acta 1030, 1-10.
23. Fatouros, D. G., Bouropoulos, N., Ioannou, P. V., and Antimisiaris, S. G. (2005) Stability and aggregation studies of non-sonicated arsonolipid- containing vesicles, Cell. Mol. Biol. Lett. 10, 173-183.
24. McIntosh, T. J. (2004) The 2004 Biophysical Society-Avanti Award in Lipids address: Roles of bilayer structure and elastic properties in peptide localization in membranes, Chem. Phys. Lipids 130, 83-98.
25. Schaeffer, L. M., McCormack, F. X., Wu, H., and Weiss, A. A. (2004) Interactions of pulmonary collectins with Bordetella bronchiseptica and Bordetella pertussis lipopolysaccharide elucidate the structural basis of their antimicrobial activities, Infect. Immun. 72, 7124-7130.
26. Sahly, H., Ofek, I., Podschun, R., Brade, H., He, Y., Ullmann, U., and Crouch, E. (2002) Surfactant protein D binds selectively to Klebsiella pneumoniae lipopolysaccharides containing mannoserich O-antigens, J. Immunol. 169, 3267-3274.
27. Dowhan, W. (1997) Molecular basis for membrane phospholipid diversity: Why are there so many lipids? Annu. Rev. Biochem. 66, 199-232.
28. Meyboom, A., Maretzki, D., Stevens, P. A., and Hofmann, K. P. (1999) Interaction of pulmonary surfactant protein A with phospholipid liposomes: A kinetic study on head group and fatty acid specificity, Biochim. Biophys. Acta 1441, 23-35.
29. Kishore, U., Greenhough, T. J., Waters, P., Shrive, A. K., Ghai, R., Kamran, M. F., Bernal, A. L., Reid, K. B., Madan, T., and Chakraborty, T. (2005) Surfactant proteins SP-A and SP-D: Structure, function and receptors, Mol. Immunol. (in press).
30. Head, J. F., Mealy, T. R., McCormack, F. X., and Seaton, B. A. (2003) Crystal structure of trimeric carbohydrate recognition and neck domains of surfactant protein A, J. Biol. Chem. 278, 43254-43260.
31. Kokkona, M., Kallinteri, P., Fatouros, D., and Antimisiaris, S. G. (2000) Stability of SUV liposomes in the presence of cholate salts and pancreatic lipases: Effect of lipid composition, Eur. J. Pharm. Sd. 9, 245-252.
32. Wieslander, A., Christiansson, A., Rilfors, L., Khan, A., Johansson, L. B., and Lindblom, G. (1982) Lipid phase structure in the regulation of lipid composition in Acholeplasma laidlawii membranes, Rev. Infect. Dis. 4 (Suppl), S43-S49.
33. Banemann, A., Deppisch, H., and Gross, R. (1998) The lipopolysaccharide of Bordetella bronchiseptica acts as a protective shield against antimicrobial peptides, Infect. Immun. 66, 5607-5612.
34. Schwarz, G., Zong, R. T., and Popescu, T. (1992) Kinetics of melittin induced pore formation in the membrane of lipid vesicles, Biochim. Biophys. Acta 1110, 97-104.
35. Smith, R., Separovic, F., Milne, T. J., Whittaker, A., Bennett, F. M., Cornell, B. A., and Makriyannis, A. (1994) Structure and orientation of the pore-forming peptide, melittin, in lipid bilayers, J. Mol. Biol. 241, 456-466.
36. Davis, I. C., Zhu, S., Sampson, J. B., Crow, J. P., and Matalon, S. (2002) Inhibition of human surfactant protein A function by oxidation intermediates of nitrite, Free Radical Biol. Med. 33, 1703-1713.