Pseudomonas aeruginosa protease IV degrades surfactant proteins and inhibits surfactant host defense and biophysical functions

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 288, Issue 2 32-2, 2005, Pages

  Malloy, Jaret L ^a   Veldhuizen, Ruud A W ^b   Thibodeaux, Brett A ^c   O'Callaghan, Richard J ^c   Wright, Jo Rae ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c LOUISIANA STATE UNIV MEDICAL CENTER   (United States)

Author keywords

Bacterial aggregation; Bacterial uptake; Macrophages; Surface tension; Surfactant aggregates

Indexed keywords

BACTERIAL PROTEIN; PROTEIN PROTEASE IV; SURFACTANT PROTEIN A; SURFACTANT PROTEIN B; SURFACTANT PROTEIN D; TOSYLLYSYL CHLOROMETHYL KETONE; UNCLASSIFIED DRUG;

ACUTE LUNG INJURY; AMINO ACID SEQUENCE; ARTICLE; BACTERIAL INFECTION; BACTERIAL VIRULENCE; CELL AGGREGATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DISEASE COURSE; HOST RESISTANCE; LUNG ALVEOLUS SURFACE TENSION; LUNG LAVAGE; MACROPHAGE; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN ISOLATION; PSEUDOMONAS AERUGINOSA; RAT; SEQUENCE ANALYSIS; SURFACE TENSION;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL ADHESION; BIOPHYSICS; BRONCHOALVEOLAR LAVAGE FLUID; CELL AGGREGATION; CHO CELLS; CRICETINAE; CRICETULUS; ESCHERICHIA COLI; IMMUNE SYSTEM; MACROPHAGES, ALVEOLAR; MALE; MOLECULAR SEQUENCE DATA; PEPTIDE HYDROLASES; PHOSPHOLIPIDS; PSEUDOMONAS AERUGINOSA; PULMONARY SURFACTANT-ASSOCIATED PROTEIN A; PULMONARY SURFACTANT-ASSOCIATED PROTEIN D; PULMONARY SURFACTANTS; RATS; RATS, SPRAGUE-DAWLEY; SALMONELLA TYPHIMURIUM;

EID: 12144257634     PISSN: 10400605     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajplung.00322.2004     Document Type: Article

References (42)

1. Alcorn JF and Wright JR. Degradation of pulmonary surfactant protein D by Pseudomonas aeruginosa elastase abrogates innate immune function. J Biol Chem 279: 30871-30879, 2004.
2. Cockshutt AM, Weitz J, and Possmayer F. Pulmonary surfactant-associated protein A enhances the surface activity of lipid extract surfactant and reverses inhibition by blood proteins in vitro. Biochemistry 29: 8424-8429, 1990.
3. Crouch E and Wright JR. Surfactant proteins A and D and pulmonary host defense. Annu Rev Physiol 63: 521-554, 2001.
4. Dong Q and Wright JR. Degradation of surfactant protein D by alveolar macrophages. Am J Physiol Lung Cell Mol Physiol 274: L97-L105, 1998.
5. Engel LS, Hill JM, Caballero AR, Green LC, and O'Callaghan RJ. Protease IV, a. unique extracellular protease and virulence factor from Pseudomonas aeruginosa. J Biol Chem 273: 16792-16797, 1998.
6. Engel LS, Hill JM, Moreau JM, Green LC, Hobden JA, and O'Callaghan RJ. Pseudomonas aeruginosa protease IV produces corneal damage and contributes to bacterial virulence. Invest Ophthalmol Vis Sci 39: 662-665, 1998.
7. Engel LS, Hobden JA, Moreau JM, Callegan MC, Hill JM, and O'Callaghan RJ. Pseudomonas deficient in protease IV has significantly reduced corneal virulence. Invest Ophthalmol Vis Sci 38: 1535-1542, 1997.
8. Enhorning G. Pulsating bubble technique for evaluating pulmonary surfactant. J Appl Physiol 43: 198-203, 1977.
9. Goerke J. Pulmonary surfactant: functions and molecular composition. Biochim Biophys Acta 1408: 79-89, 1998.
10. Goldberg JB and Pier GB. Pseudomonas aeruginosa lipopolysaccharides and pathogenesis. Trends Microbiol 4: 490-494, 1996.
11. Griese M, Birrer P, and Demirsoy A. Pulmonary surfactant in cystic fibrosis. Eur Respir J 10: 1983-1988, 1997.
12. Gunther A, Schmidt R, Feustel A, Meier U, Pucker C, Ermert M, and Seeger W. Surfactant subtype conversion is related to loss of surfactant apoprotein B and surface activity in large surfactant aggregates. Am J Respir Crit Care Med 159: 244-251, 1999.
13. Gunther A, Siebert C, Schmidt R, Ziegler S, Grimminger F, Yabut M, Temmesfeld B, Walmrath D, Morr H, and Seeger W. Surfactant alterations in severe pneumonia, acute respiratory distress syndrome, and cardiogenic lung edema. Am J Respir Crit Care Med 153: 176-184, 1996.
14. Gurel O, Ikegami M, Chroneos ZC, and Jobe AH. Macrophage and type II cell catabolism of SP-A and saturated phosphatidylcholine in mouse lungs. Am J Physiol Lung Cell Mol Physiol 280: L1266-L1272, 2001.
15. Hirche TO, Crouch EC, Espinola M, Brokelman TJ, Mecham RP, DeSilva N, Cooley J, Remold-O'Donnell E, and Belaaouaj A. Neutrophil serine proteinases inactivate surfactant protein D by cleaving within a conserved subregion of the carbohydrate recognition domain. J Biol Chem 279: 27688-27698, 2004.
16. Holmskov U, Thiel S, and Jensenius JC. Collections and ficolins: humoral lectins of the innate immune defense. Annu Rev Immunol 21: 547-578, 2003.
17. Kuroki Y and Akino T. Pulmonary surfactant protein A (SP-A) specifically binds dipalmitoylphosphatidylcholine. J Biol Chem 266: 3068-3073, 1991.
18. Lazdunski A, Guzzo J, Filloux A, Bally M, and Murgier M. Secretion of extracellular proteins by Pseudomonas aeruginosa. Biochimie 72: 147-156, 1990.
19. Levine AM, Elliott J, Whitsett J, Srikiatkhachorn A, Crouch E, DeSilva N, and Korfhagen T. Surfactant protein-D enhances phagocytosis and pulmonary clearance of respiratory syncytial virus. Am J Respir Cell Mol Biol 31: 193-199, 2004.
20. Levine AM, Kurak KE, Bruno MD, Stark JM, Whitsett JA, and Korfhagen TR. Surfactant protein-A-deficient mice are susceptible to Pseudomonas aeruginosa infection. Am J Respir Cell Mol Biol 19: 700-708, 1998.
21. Levine AM, Whitsett JA, Gwozdz J, Richardson TR, Fisher JH, Burhans MS, and Korfhagen TR. Distinct effects of surfactant protein A or D deficiency during bacterial infection on the lung. J Immunol 165: 3934-3940, 2000.
22. Liau DF, Yin NX, Huang J, and Ryan SF. Effects of human polymorphonuclear leukocyte elastase upon surfactant proteins in vitro. Biochim Biophys Acta 1302: 117-128, 1996.
23. Lyczak JB, Cannon CL, and Pier GB. Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect 2: 1051-1060, 2000.
24. Madsen J, Tornoe I, Nielsen O, Koch C, Steinhilber W, and Holmskov U. Expression and localization of lung surfactant protein A in human tissues. Am J Respir Cell Mol Biol 29: 591-597, 2003.
25. Mariencheck WI, Alcorn JF, Palmer SM, and Wright JR. Pseudomonas aeruginosa elastase degrades surfactant proteins A and D. Am J Respir Cell Mol Biol 28: 528-537, 2003.
26. McIntosh JC, Swyers AH, Fisher JH, and Wright JR. Surfactant proteins A and D increase in response to intratracheal lipopolysaccharide. Am J Respir Cell Mol Biol 15: 509-519, 1996.
27. Meyer KC, Sharma A, Brown R, Weatherly M, Moya FR, Lewandoski J, and Zimmerman JJ. Function and composition of pulmonary surfactant and surfactant-derived fatty acid profiles are altered in young adults with cystic fibrosis. Chest 118: 164-174, 2000.
28. O'Callaghan RJ, Engel LS, Hobden JA, Callegan MC, Green LC, and Hill JM. Pseudomonas keratitis. The role of an uncharacterized exoprotein, protease IV, in corneal virulence. Invest Ophthalmol Vis Sci 37: 534-543, 1996.
29. Ogasawara Y, Kuroki Y, and Akino T. Pulmonary surfactant protein D specifically binds to phosphatidylinositol. J Biol Chem 267: 21244-21249, 1992.
30. Pison U, Tam EK, Caughey GH, and Hawgood S. Proteolytic inactivation of dog lung surfactant-associated proteins by neutrophil elastase. Biochim Biophys Acta 992: 251-257, 1989.
31. Postle AD, Mander A, Reid KB, Wang JY, Wright SM, Moustaki M, and Warner JO. Deficient hydrophilic lung surfactant proteins A and D with normal surfactant phospholipid molecular species in cystic fibrosis. Am J Respir Cell Mol Biol 20: 90-98, 1999.
32. Putz G, Goerke J, and Clements JA. Surface activity of rabbit pulmonary surfactant subfractions at different concentrations in a captive bubble. J Appl Physiol 77: 597-605, 1994.
33. Song Z, Wu H, Ciofu O, Kong KF, Hoiby N, Rygaard J, Kharazmi A, and Mathee K. Pseudomonas aeruginosa alginate is refractory to Th1 immune response and impedes host immune clearance in a mouse model of acute lung infection. J Med Microblol 52: 731-740, 2003.
34. Stahlman MT, Gray ME, Hull WM, and Whitsett JA. Immunolocalization of surfactant protein-D (SP-D) in human fetal, newborn, and adult tissues. J Histochem Cytochem 50: 651-660, 2002.
35. Torres A, Aznar R, Gatell JM, Jimenez P, Gonzalez J, Ferrer A, Celis R, and Rodriguez-Roisin R. Incidence, risk, and prognosis factors of nosocomial pneumonia in mechanically ventilated patients. Am Rev Respir Dis 142: 523-528, 1990.
36. Veldhuizen RAW, Hearn SA, Lewis JF, and Possmayer F. Surface-area cycling of different surfactant preparations: SP-A and SP-B are essential for large-aggregate integrity. Biochem J 300: 519-524, 1994.
37. Veldhuizen RAW, Marcou J, Yao LJ, McCaig L, Ito Y, and Lewis JF. Alveolar surfactant aggregate conversion in ventilated normal and injured rabbits. Am J Physiol Lung Cell Mol Physiol 270: L152-L158, 1996.
38. Whitsett JA, Nogee LM, Weaver TE, and Horowitz AD. Human surfactant protein B: structure, function, regulation, and genetic disease. Physiol Rev 75: 749-757, 1995.
39. Wilderman PJ, Vasil AI, Johnson Z, Wilson MJ, Cunliffe HE, Lamont IL, and Vasil ML. Characterization of an endoprotease (PrpL) encoded by a PvdS-regulated gene in Pseudomonas aeruginosa. Infect Immun 69: 5385-5394, 2001.
40. Wright JR and Dobbs LG. Regulation of pulmonary surfactant secretion and clearance. Annu Rev Physiol 53: 395-414, 1991.
41. r = 26,000-36,000 enhances uptake of liposomes by type II cells. J Biol Chem 262: 2888-2894, 1987.
42. Yamada T, Ikegami M, and Jobe AH. Effects of surfactant subfractions on preterm rabbit lung function. Pediatr Res 27: 592-598, 1990.