Critical role of CFTR-dependent lipid rafts in cigarette smoke-induced lung epithelial injury

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 300, Issue 6, 2011, Pages

  Bodas, Manish ^a   Min, Taehong ^a   Vij, Neeraj ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Autophagy; Ceramide; Cystic fibrobsis transmembrane conductance regulator; Emphysema; Epithelium

Indexed keywords

CASPASE 3; CASPASE 7; CERAMIDE; CIGARETTE SMOKE; FAS ANTIGEN; GREEN FLUORESCENT PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN P62; PROTEIN ZO1; PROTEIN ZO2; TRANSMEMBRANE CONDUCTANCE REGULATOR;

APOPTOSIS; ARTICLE; AUTOPHAGY; CIGARETTE SMOKING; CONTROLLED STUDY; CORRELATIONAL STUDY; EMPHYSEMA; ENZYME ACTIVITY; HUMAN; HUMAN CELL; LIGHT CHAIN; LIPID RAFT; LUNG INJURY; MOUSE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; WILD TYPE;

ANIMALS; APOPTOSIS; AUTOPHAGY; BLOTTING, WESTERN; CASPASE 3; CASPASE 7; CELLS, CULTURED; CERAMIDES; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; FAS LIGAND PROTEIN; FLOW CYTOMETRY; GREEN FLUORESCENT PROTEINS; HUMANS; IN SITU NICK-END LABELING; LUNG INJURY; MEMBRANE MICRODOMAINS; MEMBRANE PROTEINS; MICE; MICE, INBRED CFTR; MICE, KNOCKOUT; NF-KAPPA B; PHOSPHOPROTEINS; SMOKING;

EID: 79958198426     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00408.2010     Document Type: Article

References (52)

1. Balmes JR. When smoke gets in your lungs. Proc Am Thorac Soc 7: 98-101, 2010.
2. Barnes PJ. New therapies for chronic obstructive pulmonary disease. Med Princ Pract 19: 330-338, 2010.
3. Becker KA, Riethmuller J, Luth A, Doring G, Kleuser B, Gulbins E. Acid sphingomyelinase inhibitors normalize pulmonary ceramide and inflammation in cystic fibrosis. Am J Respir Cell Mol Biol 42: 716-724,2010.
4. Bodas M, Min T, Mazur S, Vij N. Critical modifier role of membranecystic fibrosis transmembrane conductance regulator-dependent ceramide signaling in lung injury and emphysema. J Immunol 186: 602-613, 2011.
5. Bodas M, Min T, Vij N. Early-age-related changes in proteostasis augment immunopathogenesis of sepsis and acute lung injury. PLoS One 5: e15480, 2010.
6. Cantin AM, Hanrahan JW, Bilodeau G, Ellis L, Dupuis A, Liao J, Zielenski J, Durie P. Cystic fibrosis transmembrane conductance regulator function is suppressed in cigarette smokers. Am J Respir Crit Care Med 173: 1139-1144, 2006.
7. Chen ZH, Lam HC, Jin Y, Kim HP, Cao J, Lee SJ, Ifedigbo E, Parameswaran H, Ryter SW, Choi AM. Autophagy protein microtubule-associated protein 1 light chain-3B (LC3B) activates extrinsic apoptosis during cigarette smoke-induced emphysema. Proc Natl Acad Sci USA 107: 18880-18885, 2010.
8. Demedts IK, Demoor T, Bracke KR, Joos GF, Brusselle GG. Role of apoptosis in the pathogenesis of COPD and pulmonary emphysema. Respir Res 7: 53, 2006.
9. Dohm CP, Kermer P, Bahr M. Aggregopathy in neurodegenerative diseases: mechanisms and therapeutic implication. Neurodegener Dis 5: 321-338, 2008.
10. Dudez T, Borot F, Huang S, Kwak BR, Bacchetta M, Ollero M, Stanton BA, Chanson M. CFTR in a lipid raft-TNFR1 complex modulates gap junctional intercellular communication and IL-8 secretion. Biochim Biophys Acta 1783: 779-788, 2008.
11. Durieu I, Amsellem C, Paulin C, Chambe MT, Bienvenu J, Bellon G, Pacheco Y. Fas and Fas ligand expression in cystic fibrosis airway epithelium. Thorax 54: 1093-1098, 1999.
12. Filosto S, Castillo S, Danielson A, Franzi L, Khan E, Kenyon N, Last J, Pinkerton K, Tuder R, Goldkorn T. Neutral sphingomyelinase 2: a novel target in cigarette smoke-induced apoptosis and lung injury. Am J Respir Cell Mol Biol 44: 350-360, 2010.
13. Fullerton DG, Bruce N, Gordon SB. Indoor air pollution from biomass fuel smoke is a major health concern in the developing world. Trans R Soc Trop Med Hyg 102: 843-851, 2008.
14. Grassme H, Cremesti A, Kolesnick R, Gulbins E. Ceramide-mediated clustering is required for CD95-DISC formation. Oncogene 22: 5457-5470, 2003.
15. Grassme H, Jekle A, Riehle A, Schwarz H, Berger J, Sandhoff K, Kolesnick R, Gulbins E. CD95 signaling via ceramide-rich membrane rafts. J Biol Chem 276: 20589-20596, 2001.
16. Hamai H, Keyserman F, Quittell LM, Worgall TS. Defective CFTR increases synthesis and mass of sphingolipids that modulate membrane composition and lipid signaling. J Lipid Res 50: 1101-1108, 2009.
17. Henson PM, Bratton DL, Fadok VA. Apoptotic cell removal. Curr Biol 11: R795-R805, 2001.
18. Jacquot J, Tabary O, Le Rouzic P, Clement A. Airway epithelial cell inflammatory signalling in cystic fibrosis. Int J Biochem Cell Biol 40: 1703-1715, 2008.
19. Luciani A, Villella VR, Esposito S, Brunetti-Pierri N, Medina D, Settembre C, Gavina M, Pulze L, Giardino I, Pettoello-Mantovani M, D'Apolito M, Guido S, Masliah E, Spencer B, Quaratino S, Raia V, Ballabio A, Maiuri L. Defective CFTR induces aggresome formation and lung inflammation in cystic fibrosis through ROS-mediated autophagy inhibition. Nat Cell Biol 12: 863-875, 2010.
20. Luciani A, Villella VR, Esposito S, Brunetti-Pierri N, Medina DL, Settembre C, Gavina M, Raia V, Ballabio A, Maiuri L. Cystic fibrosis: a disorder with defective autophagy. Autophagy 7: 92-94, 2011.
21. Maiuri L, Raia V, De Marco G, Coletta S, de Ritis G, Londei M, Auricchio S. DNA fragmentation is a feature of cystic fibrosis epithelial cells: a disease with inappropriate apoptosis? FEBS Lett 408: 225-231,1997.
22. McKeon DJ, Condliffe AM, Cowburn AS, Cadwallader KC, Farahi N, Bilton D, Chilvers ER. Prolonged survival of neutrophils from patients with Delta F508 CFTR mutations. Thorax 63: 660-661, 2008.
23. Min T, Bodas M, Mazur S, Vij N. Critical role of proteostasis-imbalance in pathogenesis of COPD and severe emphysema. J Mol Med; http:// www.springerlink.com/content/h3077753lw797wk1/.
24. Miyaji M, Jin ZX, Yamaoka S, Amakawa R, Fukuhara S, Sato SB, Kobayashi T, Domae N, Mimori T, Bloom ET, Okazaki T, Umehara H. Role of membrane sphingomyelin and ceramide in platform formation for Fas-mediated apoptosis. J Exp Med 202: 249-259, 2005.
25. Monick MM, Powers LS, Walters K, Lovan N, Zhang M, Gerke A, Hansdottir S, Hunninghake GW. Identification of an autophagy defect in smokers' alveolar macrophages. J Immunol 185: 5425-5435, 2010.
26. Moreau K, Luo S, Rubinsztein DC. Cytoprotective roles for autophagy. Curr Opin Cell Biol 22: 206-211, 2010.
27. Moriceau S, Lenoir G, Witko-Sarsat V. In cystic fibrosis homozygotes and heterozygotes, neutrophil apoptosis is delayed and modulated by diamide or roscovitine: evidence for an innate neutrophil disturbance. J Innate Immun 2: 260-266, 2010.
28. Morissette MC, Parent J, Milot J. Alveolar epithelial and endothelial cell apoptosis in emphysema: what we know and what we need to know. Int J Chron Obstruct Pulmon Dis 4: 19-31, 2009.
29. Noe J, Petrusca D, Rush N, Deng P, VanDemark M, Berdyshev E, Gu Y, Smith P, Schweitzer K, Pilewsky J, Natarajan V, Xu Z, Obukhov AG, Petrache I. CFTR regulation of intracellular pH and ceramides is required for lung endothelial cell apoptosis. Am J Respir Cell Mol Biol 41: 314-323, 2009.
30. Park JW, Ryter SW, Choi AM. Functional significance of apoptosis in chronic obstructive pulmonary disease. Copd 4: 347-353, 2007.
31. Park MA, Zhang G, Norris J, Hylemon PB, Fisher PB, Grant S, Dent P. Regulation of autophagy by ceramide-CD95-PERK signaling. Autophagy 4: 929-931, 2008.
32. Petrache I, Natarajan V, Zhen L, Medler TR, Richter AT, Cho C, Hubbard WC, Berdyshev EV, Tuder RM. Ceramide upregulation causes pulmonary cell apoptosis and emphysema-like disease in mice. Nat Med 11: 491-498, 2005.
33. Riccardi C, Nicoletti I. Analysis of apoptosis by propidium iodide staining and flow cytometry. Nat Protoc 1: 1458-1461, 2006.
34. Rodriguez-Gonzalez A, Lin T, Ikeda AK, Simms-Waldrip T, Fu C, Sakamoto KM. Role of the aggresome pathway in cancer: targeting histone deacetylase 6-dependent protein degradation. Cancer Res 68: 2557-2560, 2008.
35. Rottner M, Freyssinet JM, Martinez MC. Mechanisms of the noxious inflammatory cycle in cystic fibrosis. Respir Res 10: 23, 2009.
36. Rottner M, Kunzelmann C, Mergey M, Freyssinet JM, Martinez MC. Exaggerated apoptosis and NF-κB activation in pancreatic and tracheal cystic fibrosis cells. FASEB J 21: 2939-2948, 2007.
37. Ryter SW, Lee SJ, Choi AM. Autophagy in cigarette smoke-induced chronic obstructive pulmonary disease. Expert Rev Respir Med 4: 573-584, 2010.
38. Tabary O, Corvol H, Boncoeur E, Chadelat K, Fitting C, Cavaillon JM, Clement A, Jacquot J. Adherence of airway neutrophils and inflammatory response are increased in CF airway epithelial cell-neutrophil interactions. Am J Physiol Lung Cell Mol Physiol 290: L588-L596, 2006.
39. Teichgraber V, Ulrich M, Endlich N, Riethmuller J, Wilker B, De Oliveira-Munding CC, van Heeckeren AM, Barr ML, von Kurthy G, Schmid KW, Weller M, Tummler B, Lang F, Grassme H, Doring G, Gulbins E. Ceramide accumulation mediates inflammation, cell death and infection susceptibility in cystic fibrosis. Nat Med 14: 382-391, 2008.
40. Uhlig S, Gulbins E. Sphingolipids in the lungs. Am J Respir Crit Care Med 178: 1100-1114, 2008.
41. van Heeckeren AM, Schluchter MD, Drumm ML, Davis PB. Role of Cftr genotype in the response to chronic Pseudomonas aeruginosa lung infection in mice. Am J Physiol Lung Cell Mol Physiol 287: L944-L952,2004.
42. van Heeckeren AM, Schluchter MD, Xue W, Davis PB. Response to acute lung infection with mucoid Pseudomonas aeruginosa in cystic fibrosis mice. Am J Respir Crit Care Med 173: 288-296, 2006.
43. Vandivier RW, Fadok VA, Hoffmann PR, Bratton DL, Penvari C, Brown KK, Brain JD, Accurso FJ, Henson PM. Elastase-mediated phosphatidylserine receptor cleavage impairs apoptotic cell clearance in cystic fibrosis and bronchiectasis. J Clin Invest 109: 661-670, 2002.
44. Vandivier RW, Fadok VA, Ogden CA, Hoffmann PR, Brain JD, Accurso FJ, Fisher JH, Greene KE, Henson PM. Impaired clearance of apoptotic cells from cystic fibrosis airways. Chest 121: 89S, 2002.
45. Vandivier RW, Richens TR, Horstmann SA, deCathelineau AM, Ghosh M, Reynolds SD, Xiao YQ, Riches DW, Plumb J, Vachon E, Downey GP, Henson PM. Dysfunctional cystic fibrosis transmembrane conductance regulator inhibits phagocytosis of apoptotic cells with proinflammatory consequences. Am J Physiol Lung Cell Mol Physiol 297: L677-L686, 2009.
46. Vij N, Mazur S, Zeitlin PL. CFTR is a negative regulator of NFκB mediated innate immune response. PLoS One 4: e4664, 2009.
47. Vij N, Roberts L, Joyce S, Chakravarti S. Lumican regulates corneal inflammatory responses by modulating Fas-Fas ligand signaling. Invest Ophthalmol Vis Sci 46: 88-95, 2005.
48. Wedzicha JA, Donaldson GC. Exacerbations of chronic obstructive pulmonary disease. Respir Care 48: 1204-1213, 2003.
49. Wright JL, Cosio M, Churg A. Animal models of chronic obstructive pulmonary disease. Am J Physiol Lung Cell Mol Physiol 295: L1-L15,2008.
50. Xu Y, Krause A, Hamai H, Harvey BG, Worgall TS, Worgall S. Proinflammatory phenotype and increased caveolin-1 in alveolar macrophages with silenced CFTR mRNA. PLoS One 5: e11004, 2010.
51. Yang SR, Chida AS, Bauter MR, Shafiq N, Seweryniak K, Maggirwar SB, Kilty I, Rahman I. Cigarette smoke induces proinflammatory cytokine release by activation of NF-κB and posttranslational modifications of histone deacetylase in macrophages. Am J Physiol Lung Cell Mol Physiol 291: L46-L57, 2006.
52. Zhang Y, Wu Y, Cheng Y, Zhao Z, Tashiro S, Onodera S, Ikejima T. Fas-mediated autophagy requires JNK activation in HeLa cells. Biochem Biophys Res Commun 377: 1205-1210, 2008.