Methyl-β-cyclodextrin restores the structure and function of pulmonary surfactant films impaired by cholesterol

Biochimica et Biophysica Acta - Biomembranes

Volumn 1798, Issue 5, 2010, Pages 986-994

  Gunasekara, Lasantha C ^a   Pratt, Ryan M ^a   Schoel, W Michael ^a   Gosche, Sherrie ^a   Prenner, Elmar J ^a   Amrein, Matthias Walter ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Atomic force microscopy; Bovine lipid extract surfactant; Captive bubble surfactometer; Cholesterol; Methyl cyclodextrin; Pulmonary surfactant dysfunction

Indexed keywords

BOVINE LIPID EXTRACT SURFACTANT; CHOLESTEROL; LUNG SURFACTANT; METHYL BETA CYCLODEXTRIN; SURFACTANT; UNCLASSIFIED DRUG;

AQUEOUS SOLUTION; ARTICLE; ATOMIC FORCE MICROSCOPY; CONTROLLED STUDY; LIPID MEMBRANE; MEMBRANE STRUCTURE; PRIORITY JOURNAL;

ANIMALS; BETA-CYCLODEXTRINS; CATTLE; CHOLESTEROL; MICROSCOPY, ATOMIC FORCE; PULMONARY SURFACTANTS; SURFACE PROPERTIES; SURFACE TENSION;

BOVINAE;

EID: 77649256461     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2009.12.003     Document Type: Article

References (79)

1. Pattle R.E. Properties, function and origin of the alveolar lining layer. Proc. R. Soc. Lond. 148 (1958) 217-240
2. Clements J.A. Surface tension of lung extracts. Proc. Soc. Exp. Biol. Med. 95 (1957) 170-172
3. Schurch S. Surface tension at low lung volumes: dependence on time and alveolar size. Respir. Physiol. 48 (1982) 339-355
4. Avery M.E. Surface properties in relation to atalectasis and hyaline membrane disease. Am. J. Dis. Child 97 (1959) 517-523
5. Enhorning G., and Robertson B. Lung expansion in the premature rabbit fetus after tracheal deposition of surfactant. Pediatrics 50 (1972) 58-66
6. Auten R.L., Notter R.H., Kendig J.W., Davis J.M., and Shapiro D.L. Surfactant treatment of full-term newborns with respiratory-failure. Pediatrics 87 (1991) 101-107
7. Hallman M., Merritt T.A., Jarvenpaa A.L., Boynton B., Mannino F., Gluck L., Moore T., and Edwards D. Exogenous human surfactant for treatment of severe respiratory distress syndrome: a randomized prospective clinical trial. J. Pediatr. 106 (1985) 963-969
8. Shapiro D., Notter R.H., Morin III F.C., Sinkin K.S., Weiss K.I., and Cox C. Double-blind, randomized trial of a calf lung surfactant extract administered at birth to very premature infants for prevention of respiratory distress syndrome. Pediatrics 76 (1985) 593-599
9. Hoekstra R., Jackson J.C., Myers T.F., Frantz I.D., Stern M.E., Power W.F., Maurer M., Raye J.R., Carrier S.T., and Gunkel J.H. Improved neonatal survival following multiple doses of bovine surfactant in very premature neonates at risk for respiratory distress syndrome. Pediatrics 88 (1991) 10-18
10. Schwartz R.M., Luby A.M., Scanlon J.W., and Kellogg R.J. Effect of surfactant on morbidity, mortality, and resource use in newborn infants weighing 500 to 1500 g. N. Engl. J. Med. 330 (1994) 1476-1480
11. Corbet A., Bucciarelli R., Goldman S., Mammel M., Wold D., and Long W. Decreased mortality rate among small premature infants treated at birth with a single dose of synthetic surfactant: a multicenter controlled trial. American Exosurf Pediatric Study Group 1. J. Pediatr. 118 (1991) 277-284
12. Enhorning G., Shennan A., Possmayer F., Dunn M., Chen C.P., and Milligan J. Prevention of neonatal respiratory distress syndrome by tracheal instillation of surfactant: a randomized clinical trial. Pediatrics 76 (1985) 145
13. Garber B.G., Hebert P.C., Yelle J.D., Hodder R.V., and McGowan J. Adult respiratory distress syndrome: a systemic overview of incidence and risk factors. Crit. Care. Med. 24 (1996) 687-695
14. Leaver S.K., and Evans T.W. Acute respiratory distress syndrome. Br. Med. J. 335 (2007) 389-394
15. Rubenfeld G.D., Caldwell E., Peabody E., Weaver J., Martin D.P., Neff M., Stern E.J., and Hudson L.D. Incidence and outcomes of acute lung injury. N. Engl. J. Med. 353 (2005) 1685-1693
16. Vincent J.L., and Zambon M. Why do patients who have acute lung injury/acute respiratory distress syndrome die from multiple organ dysfunction syndrome? Implications for management. Clin. Chest. Med. 27 (2006) 725-731
17. Wind J., Versteegt J., Twisk J., van der Werf T.S., Bindels A.J., Spijkstra J.J., Girbes A.R., and Groeneveld A.B. Epidemiology of acute lung injury and acute respiratory distress syndrome in The Netherlands: a survey. Respir. Med. 101 (2007) 2091-2098
18. Griese M., Essl R., Schmidt R., Rietschel E., Ratjen F., Ballmann M., and Paul K. Pulmonary surfactant, lung function, and endobronchial inflammation in cystic fibrosis. Am. J. Respir. Crit. Care. Med. 170 (2004) 1000-1005
19. Griese M., Essl R., Schmidt R., Ballmann M., Paul K., Rietschel E., and Ratjen F. Sequential analysis of surfactant, lung function and inflammation in cystic fibrosis patients. Respir. Res. 6 (2005) 133-143
20. Willson D.F., Chess P.R., and Notter R.H. Surfactant for pediatric acute lung injury. Pediatr. Clin. North Am. 55 (2008) 545-575
21. Gunasekara L., Schürch S., Schoel W.M., Nag K., Leonenko Z., Haufs M., and Amrein M. Pulmonary surfactant function is abolished by an elevated proportion of cholesterol. Biochim. Biophys. Acta 1737 (2005) 27-35
22. Gunasekara L., Schoel W.M., Schürch S., and Amrein M.W. A comparative study of mechanisms of surfactant inhibition. Biochim. Biophys. Acta, Biomembr. 1778 (2008) 433-444
23. Swendsen C.L., Skita V., and Thrall R.S. Alterations in surfactant neutral lipid composition during the development of bleomycin-induced pulmonary fibrosis. Biochim. Biophys. Acta Lipids and Lipid Metabolism 1301 (1996) 90-96
24. Markart P., Ruppert C., Wygrecka M., Colaris T., Dahal B., Walmrath D., Harbach H., Wilhelm J., Seeger W., Schmidt R., and Guenther A. Patients with ARDS show improvement but not normalisation of alveolar surface activity with surfactant treatment: putative role of neutral lipids. Thorax 62 (2007) 588-594
25. Panda A.K., Nag K., Harbottle R.R., Rodriguez-Capote K., Veldhuizen R.A., Petersen N.O., and Possmayer F. Effect of acute lung injury on structure and function of pulmonary surfactant films. Am. J. Respir. Cell Mol. Biol. 30 (2004) 641-650
26. Karagiorga G., Nakos G., Galiatsou E., and Lekka M.E. Biochemical parameters of bronchoalveolar lavage fluid in fat embolism. Intensive Care Med. 32 (2006) 116-123
27. Maruscak A.A., Vockeroth D.W., Girardi B., Sheikh T., Possmayer F., Lewis J.F., and Veldhuizen R.A. Alterations to surfactant precede physiological deterioration during high tidal volume ventilation. Am. J. Physiol. Lung Cell Mol. Physiol. 294 (2008) 974-983
28. Vockeroth D.W., Gunasekara L., Amrein M., Possmayer F., Lewis J.F., and Veldhuizen R.A. The role of cholesterol in the biophysical dysfunction of surfactant in ventilator induced lung injury. Am. J. Physiol. Lung Cell. Mol. Physiol. 298 (2009) 117-125
29. Ohtani Y., Irie T., Uekama K., Fukunaga K., and Pitha J. Differential effects of alpha-, beta- and gamma-cyclodextrins on human erythrocytes. Eur. J. Biochem. 186 (1989) 17-22
30. Bernardino de la Serna J., Perez-Gil J., Simonsen A.C., and Bagatolli L.A. Cholesterol rules: direct observation of the coexistence of two fluid phases in native pulmonary surfactant membranes at physiological temperatures. J. Biol. Chem. 279 (2004) 40715-40722
31. Yu S., Harding P.G., Smith N., and Possmayer F. Bovine pulmonary surfactant: chemical composition and physical properties. Lipids 18 (1983) 522-529
32. Schürch S., Bachofen H., and Weibel E.R. Alveolar surface tensions in excised rabbit lungs: effect of temperature. Respir. Physiol. 62 (1985) 31-45
33. Schürch S., Green F.H.Y., and Bachofen H. Formation and structure of surface films: captive bubble surfactometry. Biochim. Biophys. Acta 1408 (1998) 180-202
34. Schoel W.M., Schürch S., and Goerke J. The captive bubble method for the evaluation of pulmonary surfactant: surface tension, area, and volume calculations. Biochim. Biophys. Acta 1200 (1994) 281-290
35. Leonenko Z., Gill S., Baoukina S., Monticelli L., Doehner J., Gunasekara L., Felderer F., Rodenstein M., Eng L.M., and Amrein M. An elevated level of cholesterol impairs self-assembly of pulmonary surfactant into a functional film. Biophys. J. 93 (2007) 674-683
36. von Nahmen A., Schenk M., Sieber M., and Amrein M. The structure of a model pulmonary surfactant as revealed by scanning force microscopy. Biophys. J. 72 (1997) 463-469
37. Lipp M.M., Lee K.Y.C., Takamoto D.Y., Zasadzinski J.A., and Waring A.J. Coexistence of buckled and flat monolayers. Phys. Rev. Lett. 81 (1998) 1650-1653
38. Lopatko O.V., Orgeig S., Palmer D., Schurch S., and Daniels C.B. Alteration in pulmonary surfactant after arousal from topor in the marsupial Sminthopsis crassicaudata. J. Appl. Physiol. 86 6 (1999) 1959-1970
39. Codd J.R., Slocombe N.C., Daniels C.B., Wood P.G., and Orgeig S. Periodic fluctuations in the pulmonary surfactant system in Gould's wattled bat (Chalinolobus gouldii). Physiol. Biochem. Zool. 73 5 (2000) 605-612
40. Codd J.R., Orgeig S., Daniels C.B., and Schürch S. Alterations in surface activity of pulmonary surfactant in Gould's wattled bat during rapid arousal from torpor. Biochem. Biophys. Res. Commun. 308 3 (2003) 463-468
41. Zuo Y.Y., Veldhuizen R.A., Neumann A.W., Petersen N.O., and Possmayer F. Current perspectives in pulmonary surfactant-inhibition, enhancement and evaluation. Biochim. Biophys. Acta 1778 (2008) 1947-1977
42. Discher B.M., Maloney K.M., Grainger D.W., and Hall S.B. Effect of neutral lipids on coexisting phases in monolayers of pulmonary surfactant. Biophys. Chem. 101-102 (2002) 333-345
43. Discher B.M., Maloney K.M., Grainger D.W., Sousa C.A., and Hall S.B. Neutral lipids induce critical behaviour in interfacial monolayers of pulmonary surfactant. Biochemistry. 38 1 (1999) 374-383
44. Frerking I., Gunther A., Seeger W., and Pison U. Pulmonary surfactant: functions, abnormalities and therapeutic options. Intensive Care Med. 27 (2001) 1699-1717
45. Notter R.H. Lung surfactant: basic science and clinical applications. In: Lenfant C. (Ed). Lung Biology in Health and Disease (2000), Marcel Dekker Inc., New York 207-225
46. Gunther A., Ruppert C., Schmidt R., Markart P., Grimminger F., Walmrath D., and Seeger W. Surfactant alteration and replacement in acute respiratory distress syndrome. Respir. Res. 2 (2001) 353-364
47. Spragg R. Surfactant for acute lung injury. Am. J. Respir. Cell Mol. Biol. 37 (2007) 377-378
48. Griese M. Pulmonary surfactant in health and human lung diseases: state of the art. Eur. Resp. J. 13 (1999) 1455-1476
49. Rodriguez-Capote K., Manzanares D., Haines T., and Possmayer F. Reactive oxygen species inactivation of surfactant involves structural and functional alterations to surfactant proteins SP-B and SP-C. Biophys. J. 90 (2006) 2808-2821
50. Manzanares D., Rodriguez- Capote K., Liu S., Haines T., Ramos Y., Zhao L., Doherty-Kirby A., Lajoie G., and Possmayer F. Modification of tryptophan and methionine residues is implicated in the oxidative inactivation of surfactant protein B. Biochemistry 46 (2007) 5604-5615
51. Holm B.A., Enhorning G., and Notter R.H. A biophysical mechanism by which plasma proteins inhibit lung surfactant activity. Chem. Phys. Lipids 49 (1988) 49-55
52. Zasadzinski J.A., Aliq T.F., Alonso C., de la Serna J.B., Perez-Gil J., and Taeush H.W. Inhibition of pulmonary surfactant adsorption by serum and the mechanisms of reversal by hydrophilic polymers: theory. Biophys. J. 89 (2005) 1621-1629
53. Taeusch H.W., de la Serna J.B., Perez-Gil J., Alonso C., and Zasadzinski J.A. Inactivation of pulmonary surfactant due to serum-inhibited adsorption and reversal by hydrophilic polymers: experimental. Biophys. J. 89 (2005) 1769-1779
54. Watkins J.C. The surface properties of pure phospholipids in relation to those of lung extracts. Biochim. Biophys. Acta 152 (1968) 293-306
55. Clements J.A. Functions of the alveolar lining. Am. Rev. Respir. Dis. 115 (1977) 67-71
56. Hildebran J., Goerke J., and Clements J. Pulmonary surface film stability and composition. J. Appl. Physiol. 47 (1979) 604-611
57. Hawco M.W., Coolbear K.P., Davis P.J., and Keough K.M. Exclusion of fluid lipid during compression of monolayers of mixtures of dipalmitoylphosphatidylcholine with some other phosphatidylcholines. Biochim. Biophys. Acta 646 (1981) 185-187
58. Holm B.A., Wang Z., and Notter R.H. Multiple mechanisms of lung surfactant inhibition. Pediatr. Res. 46 (1999) 85-93
59. Putz G., Goerke J., and Clements J.A. Surface activity of rabbit pulmonary surfactant subfractions at different concentrations in a captive bubble. J. Appl. Physiol. 77 (1994) 597-605
60. Kobayashi T., Nitta K., Ganzuka M., Inui S., Grossmann G., and Robertson B. Inactivation of exogenous surfactant by pulmonary edema fluid. Pediatr. Res. 29 (1991) 353-356
61. Baldan A., Tarr P., Vales C.S., Frank J., Shimotake T.K., Hawgood S., and Edwards P.A. Deletion of the transmembrane transporter ABCG1 results in progressive pulmonary lipidosis. J. Biol. Chem. 281 (2006) 29401-29410
62. Bates S.R., Tao J.Q., Collins H.L., Francone O.L., and Rothblat G.H. Pulmonary abnormalities due to ABCA1 deficiency in mice. Am. J. Physiol. Lung Cell Mol. Physiol. 289 (2005) 980-989
63. Khovidhunkit W., Moser A.H., Shigenaga J.K., Grunfeld C., and Feingold K.R. Endotoxin down-regulates ABCG5 and ABCG8 in mouse liver and ABCA1 and ABCG1 in J774 murine macrophages: differential role of LXR. J. Lipid Res. 44 (2003) 1728-1736
64. Wojcik A.J., Skaflen M.D., Srinivasan S., and Hedrick C.C. A critical role for ABCG1 in macrophage inflammation and lung homeostasis. J. Immunol. 180 (2008) 4273-4282
65. Baldan A., Gomes A.V., Ping P., and Edwards P.A. Loss of ABCG1 results in chronic pulmonary inflammation. J. Immunol. 180 (2008) 3560-3568
66. Davidson K.G., Bersten A.D., Barr H.A., Dowling K.D., Nicholas T.E., and Doyle I.R. Lung function, permeability, and surfactant composition in oleic acid-induced acute lung injury in rats. Am. J. Physiol. Lung Cell Mol. Physiol. 279 (2000) 1091-1102
67. Ochs M., Fehrenbach H., and Richter J. Occurrence of lipid bodies in canine type II pneumocytes during hypothermic lung ischemia. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 277 (2004) 287-297
68. Davidson W., Del Dorscheid R.S., Schulzer M., Mak E., and Ayas N. Exogenous pulmonary surfactant for the treatment of adult patients with acute respiratory distress syndrome: results of a meta-analysis. Crit. Care 10 (2006) R41-R50
69. Willson D.F., Thomas N.J., Markovitz B.P., Bauman L.A., DiCarlo J.V., Pon S., Jacobs B.R., Jefferson L.S., Conaway M.R., and Egan E.A. Effect of exogenous surfactant (calfactant) in pediatric acute lung injury: a randomized controlled trial. JAMA. 293 (2005) 470-476
70. Loftsson T., Jarho P., Masson M., and Jarvinen T. Cyclodextrins in drug delivery. Expert Opin Drug Deliv. 2 (2005) 335-351
71. Stella V.J., and He Q. Cyclodextrins. Toxicol. Pathol. 36 (2008) 30-42
72. Szejtli J. Cyclodextrins. In: Tomasik P. (Ed). Chemical and Functional Properties of Food Saccharides (2004), CRC Press, Boca Raton 20045-40
73. Tewes F., Brillault J., Couet W., and Olivier J.C. Formulation of rifampicin-cyclodextrin complexes for lung nebulisation. J. Control. Release 129 (2008) 93-99
74. Evrard B., Bertholet P., Gueders M., Flament M.P., Piel G., Delattre L., Gayot A., Leterme P., Foidart J.M., and Cataldo D. Cyclodextrins as a potential carrier in drug nebulisation. J. Control. Release 96 (2004) 403-410
75. Matilainen L., Jarvinen K., Toropainen T., Nasi E., Auriola S., Jarvinen T., and Jarho P. In vitro evaluation of the effect of cyclodextrin complexation on pulmonary deposition of a peptide, cyclosporin A. Int. J. Pharm. 318 (2006) 41-48
76. Cabral Marques H.M., Hadgraft J., Kellaway I.W., and Taylor G. Studies of cyclodextrin inclusion complexes. III. The pulmonary absorption of β-, DM-β-, and HP-β-cyclodextrins in rabbits. Int. J. Pharm. 77 (1991) 297-302
77. Lambert D., O'Neill C., and Padfield P. Methyl-β-cyclodextrin increases permeability of caco-2 cell monolayers by displacing specific claudins from cholesterol rich domains associated with tight junctions. Cell. Physiol. Biochem. 20 (2007) 495-506
78. Wall D., Marcello J., Pierdomenico D., and Farid A. Administration as hydroxypropyl β-cyclodextrin complexes does not slow rates of pulmonary drug absorption in rat. STP Pharma Sciences 4 (1994) 63-68
79. Patton J.S., Fishburn C.S., and Weers J.G. The lungs as a portal of entry for systemic drug delivery. Proc. Am. Thorac. Soc. 1 (2004) 338-344