Combined activities of secretory phospholipases and eosinophil lysophospholipases induce pulmonary surfactant dysfunction by phospholipid hydrolysis

Journal of Allergy and Clinical Immunology

Volumn 119, Issue 4, 2007, Pages 838-847

  Kwatia, Mark A ^a   Doyle, Christine B ^a   Cho, Wonwha ^b   Enhorning, Goran ^c   Ackerman, Steven J ^a  

^a Department of Biochemistry and Molecular Genetics ^*  (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c UNIVERSITY AT BUFFALO   (United States)

Author keywords

asthma; capillary surfactometer; Eosinophil; lysophospholipases; phosphatidylcholine; phospholipases; pulmonary surfactant

Indexed keywords

HYDROLASE; LUNG SURFACTANT; LYSOPHOSPHOLIPASE; PHOSPHATIDYLCHOLINE; PHOSPHOLIPASE; PHOSPHOLIPID;

ANIMAL CELL; ARTICLE; CELL LYSATE; CONTROLLED STUDY; CORRELATION ANALYSIS; DOSE RESPONSE; ENZYME ACTIVITY; EOSINOPHIL; HUMAN; HUMAN CELL; HYDROLYSIS; LIPOLYSIS; MASS SPECTROMETRY; MOUSE; NONHUMAN; NORMAL HUMAN; PRIORITY JOURNAL; THIN LAYER CHROMATOGRAPHY;

ANIMALS; CATALYSIS; CELL LINE, TUMOR; CELLS, CULTURED; DRUG SYNERGISM; ENZYME ACTIVATION; EOSINOPHILS; GLYCOPROTEINS; HUMANS; HYDROLYSIS; LYSOPHOSPHOLIPASE; MICE; PHOSPHOLIPASES A; PHOSPHOLIPIDS; PULMONARY SURFACTANTS;

EID: 34047126774     PISSN: 00916749     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jaci.2006.12.614     Document Type: Article

References (52)

1. Van Golde L.M., Batenburg J.J., and Robertson B. The pulmonary surfactant system: biochemical aspects and functional significance. Physiol Rev 68 (1988) 374-455
2. Jarjour N.N., and Enhorning G. Antigen-induced airway inflammation in atopic subjects generates dysfunction of pulmonary surfactant. Am J Respir Crit Care Med 160 (1999) 336-341
3. Hohlfeld J.M. The role of surfactant in asthma. Respir Res 3 (2002) 4
4. Baritussio A. Lung surfactant, asthma, and allergens: a story in evolution. Am J Respir Crit Care Med 169 (2004) 550-551
5. Kurashima K., Fujimura M., Matsuda T., and Kobayashi T. Surface activity of sputum from acute asthmatic patients. Am J Respir Crit Care Med 155 (1997) 1254-1259
6. Wright S.M., Hockey P.M., Enhorning G., Strong P., Reid K.B., Holgate S.T., et al. Altered airway surfactant phospholipid composition and reduced lung function in asthma. J Appl Physiol 89 (2000) 1283-1292
7. Kurashima K., Ogawa H., Ohka T., Fujimura M., Matsuda T., and Kobayashi T. A pilot study of surfactant inhalation in the treatment of asthmatic attack. Arerugi 40 (1991) 160-163
8. Babu K.S., Woodcock D.A., Smith S.E., Staniforth J.N., Holgate S.T., and Conway J.H. Inhaled synthetic surfactant abolishes the early allergen-induced response in asthma. Eur Respir J 21 (2003) 1046-1049
9. Hohlfeld J.M., Ahlf K., Enhorning G., Balke K., Erpenbeck V.J., Petschallies J., et al. Dysfunction of pulmonary surfactant in asthmatics after segmental allergen challenge. Am J Respir Crit Care Med 159 (1999) 1803-1809
10. Hite R.D., Seeds M.C., Safta A.M., Jacinto R.B., Gyves J.I., Bass D.A., et al. Lysophospholipid generation and phosphatidylglycerol depletion in phospholipase A(2)-mediated surfactant dysfunction. Am J Physiol Lung Cell Mol Physiol 288 (2005) L618-L624
11. Hite R.D., Seeds M.C., Bowton D.L., Grier B.L., Safta A.M., Balkrishnan R., et al. Surfactant phospholipid changes after antigen challenge: a role for phosphatidylglycerol in dysfunction. Am J Physiol Lung Cell Mol Physiol 288 (2005) L610-L617
12. Bowton D.L., Seeds M.C., Fasano M.B., Goldsmith B., and Bass D.A. Phospholipase A2 and arachidonate increase in bronchoalveolar lavage fluid after inhaled antigen challenge in asthmatics. Am J Respir Crit Care Med 155 (1997) 421-425
13. Chilton F.H., Averill F.J., Hubbard W.C., Fonteh A.N., Triggiani M., and Liu M.C. Antigen-induced generation of lyso-phospholipids in human airways. J Exp Med 183 (1996) 2235-2245
14. Ackerman S.J., Zhou Z.-Q., Tenen D.G., Clark M.A., Tu Y.-P., and Irvin C.G. Human eosinophil lysophospholipase (Charcot-Leyden crystal protein): molecular cloning, expression, and potential functions in asthma. In: Gleich G.J., and Kay A.B. (Eds). Eosinophils in allergy and inflammation (1994), Marcel Dekker, New York 21-54
15. Ackerman S.J., Kwatia M.A., Doyle C.B., and Enhorning G. Hydrolysis of surfactant phospholipids catalyzed by phospholipase A2 and eosinophil lysophospholipases causes surfactant dysfunction: a mechanism for small airway closure in asthma. Chest 123 (2003) 355S
16. Lee J.J., Dimina D., Macias M.P., Ochkur S.I., McGarry M.P., O'Neill K.R., et al. Defining a link with asthma in mice congenitally deficient in eosinophils. Science 305 (2004) 1773-1776
17. Kay A.B. The role of eosinophils in the pathogenesis of asthma. Trends Mol Med 11 (2005) 148-152
18. Humbles A.A., Lloyd C.M., McMillan S.J., Friend D.S., Xanthou G., McKenna E.E., et al. A critical role for eosinophils in allergic airways remodeling. Science 305 (2004) 1776-1779
19. Weller P.F., Wasserman S.I., and Austen K.F. In: Mahmoud A.A.F., and Austen K.F. (Eds). The eosinophil in health and disease (1980), Grune and Stratton, New York 115-128
20. Blom M., Tool A.T., Wever P.C., Wolbink G.J., Brouwer M.C., Calafat J., et al. Human eosinophils express, relative to other circulating leukocytes, large amounts of secretory 14-kD phospholipase A2. Blood 91 (1998) 3037-3043
21. Furue S., Kuwabara K., Mikawa K., Nishina K., Shiga M., Maekawa N., et al. Crucial role of group IIA phospholipase A(2) in oleic acid-induced acute lung injury in rabbits. Am J Respir Crit Care Med 160 (1999) 1292-1302
22. Arbibe L., Koumanov K., Vial D., Rougeot C., Faure G., Havet N., et al. Generation of lyso-phospholipids from surfactant in acute lung injury is mediated by type-II phospholipase A2 and inhibited by a direct surfactant protein A-phospholipase A2 protein interaction. J Clin Invest 102 (1998) 1152-1160
23. Touqui L., and Wu Y.Z. Interaction of secreted phospholipase A2 and pulmonary surfactant and its pathophysiological relevance in acute respiratory distress syndrome. Acta Pharmacol Sin 24 (2003) 1292-1296
24. Ackerman S.J., Liu L., Kwatia M.A., Savage M.P., Leonidas D.D., Swaminathan G.J., et al. Charcot-Leyden crystal protein (galectin-10) is not a dual function galectin with lysophospholipase activity but binds a lysophospholipase inhibitor in a novel structural fashion. J Biol Chem 277 (2002) 14859-14868
25. Holtsberg F.W., Ozgur L.E., Garsetti D.E., Myers J., Egan R.W., and Clark M.A. Presence in human eosinophils of a lysophospholipase similar to that found in the pancreas. Biochem J 309 (1995) 141-144
26. Van Schaik S.M., Vargas I., Welliver R.C., and Enhorning G. Surfactant dysfunction develops in BALB/c mice infected with respiratory syncytial virus. Pediatr Res 42 (1997) 169-173
27. Du J., Alsayed Y.M., Xin F., Ackerman S.J., and Platanias L.C. Engagement of the CrkL adapter in interleukin-5 signaling in eosinophils. J Biol Chem 275 (2000) 33167-33175
28. Lee J.J., McGarry M.P., Farmer S.C., Denzler K.L., Larson K.A., Carrigan P.E., et al. Interleukin-5 expression in the lung epithelium of transgenic mice leads to pulmonary changes pathognomonic of asthma. J Exp Med 185 (1997) 2143-2156
29. Borchers M.T., Ansay T., DeSalle R., Daugherty B.L., Shen H., Metzger M., et al. In vitro assessment of chemokine receptor-ligand interactions mediating mouse eosinophil migration. J Leukoc Biol 71 (2002) 1033-1041
30. Baumann M.A., and Paul C.C. The AML14 and AML14.3D10 cell lines: a long-overdue model for the study of eosinophils and more. Stem Cells 16 (1998) 16-24
31. Gomes I., Mathur S.K., Espenshade B.M., Mori Y., Varga J., and Ackerman S.J. Eosinophil-fibroblast interactions induce fibroblast IL-6 secretion and extracellular matrix gene expression: implications in fibrogenesis. J Allergy Clin Immunol 116 (2005) 796-804
32. Wang A., Loo R., Chen Z., and Dennis E.A. Regiospecificity and catalytic triad of lysophospholipase I. J Biol Chem 272 (1997) 22030-22036
33. Snitko Y., Yoon E.T., and Cho W. High specificity of human secretory class II phospholipase A2 for phosphatidic acid. Biochem J 321 (1997) 737-741
34. Wang A., Yang H.C., Friedman P., Johnson C.A., and Dennis E.A. A specific human lysophospholipase: cDNA cloning, tissue distribution and kinetic characterization. Biochim Biophys Acta 1437 (1999) 157-169
35. Enhorning G. Pulmonary surfactant function studied with the pulsating bubble surfactometer (PBS) and the capillary surfactometer (CS). Comp Biochem Physiol A Mol Integr Physiol 129 (2001) 221-226
36. Touchstone J. Advances in thin layer chromatography (1982), Wiley, New York
37. Weller P.F., Goetzl E.J., and Austen K.F. Identification of human eosinophil lysophospholipase as the constituent of Charcot-Leyden crystals. Proc Natl Acad Sci U S A 77 (1980) 7440-7443
38. Heeley E.L., Hohlfeld J.M., Krug N., and Postle A.D. Phospholipid molecular species of bronchoalveolar lavage fluid after local allergen challenge in asthma. Am J Physiol Lung Cell Mol Physiol 278 (2000) L305-L311
39. Hite R.D., Seeds M.C., Jacinto R.B., Balasubramanian R., Waite M., and Bass D. Hydrolysis of surfactant-associated phosphatidylcholine by mammalian secretory phospholipases A2. Am J Physiol 275 (1998) L740-L747
40. Lema G., and Enhorning G. Surface properties after a simulated PLA2 hydrolysis of pulmonary surfactant's main component, DPPC. Biochim Biophys Acta 1345 (1997) 86-92
41. Kahn M.C., Anderson G.J., Anyan W.R., and Hall S.B. Phosphatidylcholine molecular species of calf lung surfactant. Am J Physiol 269 (1995) L567-L573
42. Holm B.A., Wang Z., Egan E.A., and Notter R.H. Content of dipalmitoyl phosphatidylcholine in lung surfactant: ramifications for surface activity. Pediatr Res 39 (1996) 805-811
43. Hallman M., Enhorning G., and Possmayer F. Composition and surface activity of normal and phosphatidylglycerol-deficient lung surfactant. Pediatr Res 19 (1985) 286-292
44. Hohlfeld J.M., Schmiedl A., Erpenbeck V.J., Venge P., and Krug N. Eosinophil cationic protein alters pulmonary surfactant structure and function in asthma. J Allergy Clin Immunol 113 (2004) 496-502
45. Kim C.K., Kim S.W., Kim Y.K., Kang H., Yu J., Yoo Y., et al. Bronchoalveolar lavage eosinophil cationic protein and interleukin-8 levels in acute asthma and acute bronchiolitis. Clin Exp Allergy 35 (2005) 591-597
46. Wagers S.S., Norton R.J., Rinaldi L.M., Bates J.H., Sobel B.E., and Irvin C.G. Extravascular fibrin, plasminogen activator, plasminogen activator inhibitors, and airway hyperresponsiveness. J Clin Invest 114 (2004) 104-111
47. Dunnill M.S. The pathology of asthma. Ciba Found Study Group 38 (1971) 35-46
48. Macklem P.T. Airway obstruction and collateral ventilation. Physiol Rev 51 (1971) 368-436
49. Samee S., Altes T., Powers P., de Lange E.E., Knight-Scott J., Rakes G., et al. Imaging the lungs in asthmatic patients by using hyperpolarized helium-3 magnetic resonance: assessment of response to methacholine and exercise challenge. J Allergy Clin Immunol 111 (2003) 1205-1211
50. Erjefalt J.S., Greiff L., Andersson M., Matsson E., Petersen H., Linden M., et al. Allergen-induced eosinophil cytolysis is a primary mechanism for granule protein release in human upper airways. Am J Respir Crit Care Med 160 (1999) 304-312
51. Erjefalt J.S., Andersson M., Greiff L., Korsgren M., Gizycki M., Jeffery P.K., et al. Cytolysis and piecemeal degranulation as distinct modes of activation of airway mucosal eosinophils. J Allergy Clin Immunol 102 (1998) 286-294
52. Masuda S., Murakami M., Mitsuishi M., Komiyama K., Ishikawa Y., Ishii T., et al. Expression of secretory phospholipase A2 enzymes in lungs of humans with pneumonia and their potential prostaglandin-synthetic function in human lung-derived cells. Biochem J 387 (2005) 27-38