Src regulates cigarette smoke-induced ceramide generation via neutral sphingomyelinase 2 in the airway epithelium

American Journal of Respiratory Cell and Molecular Biology

Volumn 52, Issue 6, 2015, Pages 738-748

  Chung, Samuel ^a   Vu, Simon ^a   Filosto, Simone ^a   Goldkorn, Tzipora ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Ceramide; Neutral sphingomyelinase 2; Sphingolipids; Src

Indexed keywords

CERAMIDE; CIGARETTE SMOKE; DASATINIB; HEAT SHOCK PROTEIN 27; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN TYROSINE KINASE; SMALL INTERFERING RNA; SPHINGOMYELIN PHOSPHODIESTERASE; SPHINGOMYELIN PHOSPHODIESTERASE 2; UNCLASSIFIED DRUG; SMPD3 PROTEIN, MOUSE;

A549 CELL LINE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL FREE SYSTEM; CHRONIC OBSTRUCTIVE LUNG DISEASE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; LIQUID CHROMATOGRAPHY; LUNG CANCER; LUNG INJURY; MODULATION; MOUSE; NONHUMAN; ONCOGENE SRC; OXIDATIVE STRESS; POLYACRYLAMIDE GEL ELECTROPHORESIS; REGULATORY MECHANISM; RESPIRATORY EPITHELIUM; SUPERNATANT; TANDEM MASS SPECTROMETRY; TISSUE SECTION; TUNEL ASSAY; 129 MOUSE; ADVERSE EFFECTS; ANIMAL; BIOSYNTHESIS; ENZYMOLOGY; EPITHELIUM; LUNG DISEASES; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN PROCESSING; RESPIRATORY TRACT MUCOSA; SMOKING; TUMOR CELL LINE;

MUS;

ANIMALS; APOPTOSIS; CELL LINE, TUMOR; CERAMIDES; ENZYME ACTIVATION; EPITHELIUM; HUMANS; LUNG DISEASES; MICE, 129 STRAIN; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RESPIRATORY MUCOSA; SMOKING; SPHINGOMYELIN PHOSPHODIESTERASE; SRC-FAMILY KINASES;

EID: 84930401005     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2014-0122OC     Document Type: Article

References (47)

1. Lee JT, Xu J, Lee JM, Ku G, Han X, Yang DI, Chen S, Hsu CY. Amyloid-beta peptide induces oligodendrocyte death by activating the neutral sphingomyelinase-ceramide pathway. J Cell Biol 2004;164:123-131.
2. Clarke CJ, Cloessner EA, Roddy PL, Hannun YA. Neutral sphingomyelinase 2 (nSMase2) is the primary neutral sphingomyelinase isoform activated by tumour necrosis factor-alpha in MCF-7 cells. Biochem J 2011;435:381-390.
3. Marchesini N, Osta W, Bielawski J, Luberto C, Obeid LM, Hannun YA. Role for mammalian neutral sphingomyelinase 2 in confluence-induced growth arrest of MCF7 cells. J Biol Chem 2004;279:25101-25111.
4. 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 2011;44:350-360.
5. Levy M, Khan E, Careaga M, Goldkorn T. Neutral sphingomyelinase 2 is activated by cigarette smoke to augment ceramide-induced apoptosis in lung cell death. Am J Physiol Lung Cell Mol Physiol 2009;297:125-133.
6. Ravid T, Tsaba A, Gee P, Rasooly R, Medina EA, Goldkorn T. Ceramide accumulation precedes caspase-3 activation during apoptosis of A549 human lung adenocarcinoma cells. Am J Physiol Lung Cell Mol Physiol 2003;284:L1082-L1092.
7. Filosto S, Fry W, Knowlton AA, Goldkorn T. Neutral sphingomyelinase 2 (nSMase2) is a phosphoprotein regulated by calcineurin (PP2B). J Biol Chem 2010;285:10213-10222.
8. Zhang J, Kalyankrishna S, Wislez M, Thilaganathan N, Saigal B, Wei W, Ma L, Wistuba II, Johnson FM, Kurie JM. Src-family kinases are activated in non-small cell lung cancer and promote the survival of epidermal growth factor receptor-dependent cell lines. Am J Pathol 2007;170:366-376.
9. Masaki T, Igarashi K, Tokuda M, Yukimasa S, Han F, Jin YJ, Li JQ, Yoneyama H, Uchida N, Fujita J, et al. PP60C-Src activation in lung adenocarcinoma. Eur J Cancer 2003;39:1447-1455.
10. Giaccone G, Zucali PA. Src as a potential therapeutic target in non-small-cell lung cancer. Ann Oncol 2008;19:1219-1223.
11. Leung EL, Tam IY, Tin VP, Chua DT, Sihoe AD, Cheng LC, Ho JC, Chung LP, Wong MP. Src promotes survival and invasion of lung cancers with epidermal growth factor receptor abnormalities and is a potential candidate for molecular-targeted therapy. Mol Cancer Res 2009;7:923-932.
12. Filosto S, Baston DS, Chung S, Becker CR, Goldkorn T. Src mediates cigarette smoke-induced resistance to tyrosine kinase inhibitors in NSCLC cells. Mol Cancer Ther 2013;12:1579-1590.
13. Geraghty P, Hardigan A, Foronjy RF. Cigarette smoke activates the proto-oncogene c-Src to promote airway inflammation and lung tissue destruction. Am J Respir Cell Mol Biol 2013;50:559-570.
14. Filosto S, Becker CR, Goldkorn T. Cigarette smoke induces aberrant EGF receptor activation that mediates lung cancer development and resistance to tyrosine kinase inhibitors. Mol Cancer Ther 2012;11:795-804.
15. Zhang H, Liu H, Borok Z, Davies KJ, Ursini F, Forman HJ. Cigarette smoke extract stimulates epithelial-mesenchymal transition through src activation. Free Radic Biol Med 2012;52:1437-1442.
16. Chen Y, Zhao YH, Di YP, Wu R. Characterization of human mucin 5B gene expression in airway epithelium and the genomic clone of the amino-terminal and 59-flanking region. Am J Respir Cell Mol Biol 2001;25:542-553.
17. Robinson CB, Wu R. Culture of airway epithelial cells in serum-free medium. Methods Cell Sci 1991;13:95-102.
18. Khan EM, Lanir R, Danielson AR, Goldkorn T. EGF receptor exposed to cigarette smoke is aberrantly activated and undergoes perinuclear trafficking. FASEB J 2008;22:910-917.
19. Bielawski J, Szulc ZM, Hannun YA, Bielawska A. Simultaneous quantitative analysis of bioactive sphingolipids by high-performance liquid chromatography-tandem mass spectrometry. Methods 2006;39:82-91.
20. Okazaki T, Bielawska A, Domae N, Bell RM, Hannun YA. Characteristics and partial purification of a novel cytosolic, magnesium-independent, neutral sphingomyelinase activated in the early signal transduction of 1 alpha,25-dihydroxyvitamin d3-induced hl-60 cell differentiation. J Biol Chem 1994;269:4070-4077. [Published erratum appears in J Biol Chem 1994 269:16518.]
21. Lawler JF Jr, Yin M, Diehl AM, Roberts E, Chatterjee S. Tumor necrosis factor-alpha stimulates the maturation of sterol regulatory element binding protein-1 in human hepatocytes through the action of neutral sphingomyelinase. J Biol Chem 1998;273:5053-5059.
22. Chan C, Goldkorn T. Ceramide path in human lung cell death. Am J Respir Cell Mol Biol 2000;22:460-468.
23. Filosto S, Ashfaq M, Chung S, Fry W, Goldkorn T. Neutral sphingomyelinase 2 activity and protein stability are modulated by phosphorylation of five conserved serines. JBiolChem2012;287:514-522.
24. Yokouchi M, Kondo T, Sanjay A, Houghton A, Yoshimura A, Komiya S, Zhang H, Baron R. Src-catalyzed phosphorylation of c-Cbl leads to the interdependent ubiquitination of both proteins. J Biol Chem 2001;276:35185-35193.
25. Kim M, Tezuka T, Tanaka K, Yamamoto T. Cbl-c suppresses V-Src-induced transformation through ubiquitin-dependent protein degradation. Oncogene 2004;23:1645-1655.
26. Filosto S, Khan E, Tognon E, Becker C, Ashfaq M, Ravid T, Goldkorn T. EGF receptor exposed to oxidative stress acquires abnormal phosphorylation and aberrant activated conformation that impairs canonical dimerization. PloS One 2011;6:e23240.
27. Khan E, Heidinger J, Levy M, Lisanti M, Ravid T, Goldkorn T. EGF receptor exposed to oxidative stress undergoes Src- and caveolin-1-dependent perinuclear trafficking. J Biol Chem 2006;281:14486-14493.
28. Raingeaud J, Gupta S, Rogers JS, Dickens M, Han J, Ulevitch RJ, Davis RJ. Pro-inflammatory cytokines and environmental stress cause p38 mitogen-activated protein kinase activation by dual phosphorylation on tyrosine and threonine. J Biol Chem 1995;270:7420-7426.
29. Zhang YY, Mei ZQ, Wu JW, Wang ZX. Enzymatic activity and substrate specificity of mitogen-activated protein kinase p38alpha in different phosphorylation states. J Biol Chem 2008;283:26591-26601.
30. Larsen JK, Yamboliev IA, Weber LA, Gerthoffer WT. Phosphorylation of the 27-kda heat shock protein via p38 MAP kinase and MAPKAP kinase in smooth muscle. Am J Physiol 1997;273:L930-L940.
31. Wang T, Chiang ET, Moreno-Vinasco L, Lang GD, Pendyala S, Samet JM, Geyh AS, Breysse PN, Chillrud SN, Natarajan V, et al. Particulate matter disrupts human lung endothelial barrier integrity via ROS- and p38 MAPK-dependent pathways. Am J Respir Cell Mol Biol 2010;42:442-449.
32. Cinq-Frais C, Coatrieux C, Grazide MH, Hannun YA, Negre-Salvayre A, Salvayre R, Auge N. A signaling cascade mediated by ceramide, Src and PDGFRbeta coordinates the activation of the redox-sensitive neutral sphingomyelinase-2 and sphingosine kinase-1. Biochim Biophys Acta 2013;1831:1344-1356.
33. 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 2005;11:491-498.
34. de Torres JP, Bastarrika G, Wisnivesky JP, Alcaide AB, Campo A, Seijo LM, Pueyo JC, Villanueva A, Lozano MD, Montes U, et al. Assessing the relationship between lung cancer risk and emphysema detected on low-dose CT of the chest. Chest 2007;132:1932-1938.
35. Houghton AM. Mechanistic links between COPD and lung cancer. Nat Rev Cancer 2013;13:233-245.
36. Paschall AV, Zimmerman MA, Torres CM, Yang D, Chen MR, Li X, Bieberich E, Bai A, Bielawski J, Bielawska A, et al. Ceramide targets XIAP and CIAP1 to sensitize metastatic colon and breast cancer cells to apoptosis induction to suppress tumor progression. BMC Cancer 2014;14:24.
37. Kurinna SM, Tsao CC, Nica AF, Jiffar T, Ruvolo PP. Ceramide promotes apoptosis in lung cancer-derived A549 cells by a mechanism involving c-Jun NH2-terminal kinase. Cancer Res 2004;64:7852-7856.
38. Goldkorn T, Chung S, Filosto S. Lung cancer and lung injury: the dual role of ceramide. Handbook Exp Pharmacol 2013; (216):93-113.
39. Saddoughi SA, Ogretmen B. Diverse functions of ceramide in cancer cell death and proliferation. Adv Cancer Res 2013;117:37-58.
40. Mitra P, Maceyka M, Payne SG, Lamour N, Milstien S, Chalfant CE, Spiegel S. Ceramide kinase regulates growth and survival of a549 human lung adenocarcinoma cells. FEBS Lett 2007;581:735-740.
41. Bundy RE, Hoare GS, Kite A, Beach J, Yacoub M, Marczin N. Redox regulation of p38 MAPK activation and expression of ICAM-1 and Heme oxygenase-1 in human alveolar epithelial (A549) cells. Antioxid Redox Signal 2005;7:14-24.
42. Schweitzer KS, Hatoum H, Brown MB, Gupta M, Justice MJ, Beteck B, Van Demark M, Gu Y, Presson RG Jr, Hubbard WC, et al. Mechanisms of lung endothelial barrier disruption induced by cigarette smoke: role of oxidative stress and ceramides. Am J Physiol Lung Cell Mol Physiol 2011;301:L836-L846.
43. Medicherla S, Fitzgerald MF, Spicer D, Woodman P, Ma JY, Kapoun AM, Chakravarty S, Dugar S, Protter AA, Higgins LS. P38alpha-selective mitogen-activated protein kinase inhibitor SD-282 reduces inflammation in a subchronic model of tobacco smoke-induced airway inflammation. J Pharmacol Exp Ther 2008;324:921-929.
44. Kim MJ, Byun JY, Yun CH, Park IC, Lee KH, Lee SJ. C-Src-p38 mitogen-activated protein kinase signaling is required for Akt activation in response to ionizing radiation. Mol Cancer Res 2008;6:1872-1880.
45. Lim MJ, Seo YH, Choi KJ, Cho CH, Kim BS, Kim YH, Lee J, Lee H, Jung CY, Ha J, et al. Suppression of c-Src activity stimulates muscle differentiation via p38 MAPK activation. Arch Biochem Biophys 2007;465:197-208.
46. Clarke CJ, Truong TG, Hannun YA. Role for neutral sphingomyelinase-2 in tumor necrosis factor alpha-stimulated expression of vascular cell adhesion molecule-1 (VCAM) and intercellular adhesion molecule-1 (ICAM) in lung epithelial cells: P38 MAPK is an upstream regulator of nSMase2. J Biol Chem 2007;282:1384-1396.
47. Gaffey K, Reynolds S, Plumb J, Kaur M, Singh D. Increased phosphorylated p38 mitogen activated protein kinase in COPD lungs. Eur Respir J 2012;42:28-41.