Accumulation of ceramide in the trachea and intestine of cystic fibrosis mice causes inflammation and cell death

Biochemical and Biophysical Research Communications

Volumn 403, Issue 3-4, 2010, Pages 368-374

  Becker, Katrin Anne ^a   Tümmler, Burkhard ^b   Gulbins, Erich ^a   Grassmé, Heike ^a  

^a UNIVERSITY OF DUISBURG ESSEN   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Cell death; Ceramide; Cystic fibrosis; Inflammation; Intestine; Sphingomyelinase; Trachea

Indexed keywords

AMITRIPTYLINE; CERAMIDE; INTERLEUKIN 8; SPHINGOMYELIN PHOSPHODIESTERASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CONTROLLED STUDY; CYSTIC FIBROSIS; CYTOKINE RELEASE; ENZYME ACTIVITY; ENZYME INHIBITION; HETEROZYGOSITY; INFLAMMATION; INTESTINE EPITHELIUM CELL; LIPID STORAGE; MOUSE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; TRACHEA;

ANIMALS; CELL DEATH; CERAMIDES; CYSTIC FIBROSIS; CYTOKINES; INFLAMMATION; INTESTINES; MICE; MICE, CONGENIC; MICE, INBRED CFTR; TRACHEA;

MUS;

EID: 78650177234     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2010.11.038     Document Type: Article

References (33)

1. Riordan J.R., Rommens J.M., Kerem B., Alon N., Rozmahel R., Grzelczak Z., Zielenski J., Lok S., Plavsic N., Chou J.L., et al. Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 1989, 245:1066-1073.
2. Rommens J.M., Iannuzzi M.C., Kerem B., Drumm M.L., Melmer G., Dean M., Rozmahel R., Cole J.L., Kennedy D., Hidaka N., et al. Identification of the cystic fibrosis gene: chromosome walking and jumping. Science 1989, 245:1059-1065.
3. Kerem B., Rommens J.M., Buchanan J.A., Markiewicz D., Cox T.K., Chakravarti A., Buchwald M., Tsui L.C. Identification of the cystic fibrosis gene: genetic analysis. Science 1989, 245:1073-1080.
4. Cystic Fibrosis Foundation, Patient Registry 2004 Annual Report, Cystic Fibrosis Foundation, Bethesda, MD, USA, 2005.
5. Durie P.R., Kent G., Phillips M.J., Ackerley C.A. Characteristic multiorgan pathology of cystic fibrosis in a long-living cystic fibrosis transmembrane regulator knockout murine model. Am. J. Pathol. 2004, 164:1481-1493.
6. 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. 1997, 408:225-231.
7. Tümmler B., Kiewitz C. Cystic fibrosis: an inherited susceptibility to bacterial respiratory infections. Mol. Med. Today 1999, 5:351-358.
8. Döring G., Gulbins E. Cystic fibrosis and innate immunity: how chloride channel mutations provoke lung disease. Cell. Microbiol. 2009, 11:208-216.
9. Bonfield T.L., Konstan M.W., Burfeind P., Panuska J.R., Hilliard J.B., Berger M. Normal bronchial epithelial cells constitutively produce the anti-inflammatory cytokine interleukin-10, which is downregulated in cystic fibrosis. Am. J. Respir. Cell Mol. Biol. 1995, 13:257-261.
10. Goldman M.J., Anderson G.M., Stolzenberg E.D., Kari U.P., Zasloff M., Wilson J.M. Human beta-defensin-1 is a salt-sensitive antibiotic in lung that is inactivated in cystic fibrosis. Cell 1997, 88:553-560.
11. Oceandy D., McMorran B.J., Smith S.N., Schreiber R., Kunzelmann K., Alton E.W., Hume D.A., Wainwright B.J. Gene complementation of airway epithelium in the cystic fibrosis mouse is necessary and sufficient to correct the pathogen clearance and inflammatory abnormalities. Hum. Mol. Genet. 2002, 11:1059-1067.
12. Tabary O., Escotte S., Couetil J.P., Hubert D., Dusser D., Puchelle E., Jacquot J. Genistein inhibits constitutive and inducible NFkappaB activation and decreases IL-8 production by human cystic fibrosis bronchial gland cells. Am. J. Pathol. 1999, 155:473-481.
13. Tirouvanziam R., de Bentzmann S., Hubeau C., Hinnrasky J., Jacquot J., Péault B., Puchelle E. Inflammation and infection in naive human cystic fibrosis airway grafts. Am. J. Respir. Cell Mol. Biol. 2000, 23:121-127.
14. Teichgräber V., Ulrich M., Endlich N., Riethmüller J., Wilker B., De Oliveira-Munding C.C., van Heeckeren A.M., Barr M.L., von Kürthy G., Schmid K.W., Weller M., Tümmler B., Lang F., Grassmé H., Döring G., Gulbins E. Ceramide accumulation mediates inflammation, cell death and infection susceptibility in cystic fibrosis. Nat. Med. 2008, 14:382-391.
15. Becker K.A., Riethmüller J., Lüth A., Döring G., Kleuser B., Gulbins E. Acid sphingomyelinase inhibitors normalize pulmonary ceramide and inflammation in cystic fibrosis. Am. J. Respir. Cell Mol. Biol. 2009, 42:716-724.
16. Venkatakrishnan A., Stecenko A.A., King G., Blackwell T.R., Brigham K.L., Christman J.W., Blackwell T.S. Exaggerated activation of nuclear factor-kappaB and altered IkappaB-beta processing in cystic fibrosis bronchial epithelial cells. Am. J. Respir. Cell Mol. Biol. 2000, 23:396-403.
17. Khan T.Z., Wagener J.S., Bost T., Martinez J., Accurso F.J., Riches D.W. Early pulmonary inflammation in infants with cystic fibrosis. Am. J. Respir. Crit. Care Med. 1995, 151:1075-1082.
18. Verhaeghe C., Delbecque K., de Leval L., Oury C., Bours V. Early inflammation in the airways of a cystic fibrosis foetus. J. Cyst. Fibros. 2007, 6:304-308.
19. Vij N., Mazur S., Zeitlin P.L. CFTR is a negative regulator of NFκB mediated innate immune response. PLoS ONE 2009, 4:e4664.
20. Boucher R.C. Airway surface dehydration in cystic fibrosis: pathogenesis and therapy. Annu. Rev. Med. 2007, 58:157-170.
21. Matsui H., Verghese M.W., Kesimer M., Schwab U.E., Randell S.H., Sheehan J.K., Grubb B.R., Boucher R.C. Reduced three-dimensional motility in dehydrated airway mucus prevents neutrophil capture and killing bacteria on airway epithelial surfaces. J. Immunol. 2005, 175:1090-1099.
22. Barasch J., Kiss B., Prince A., Saiman L., Gruenert D., al-Awqati Q. Defective acidification of intracellular organelles in cystic fibrosis. Nature 1991, 352:70-73.
23. Di A., Brown M.E., Deriy L.V., Li C., Szeto F.L., Chen Y., Huang P., Tong J., Naren A.P., Bindokas V., Palfrey H.C., Nelson D.J. CFTR regulates phagosome acidification in macrophages and alters bactericidal activity. Nat. Cell Biol. 2006, 8:933-944.
24. Zhang Y., Li X., Grassmé H., Döring G., Gulbins E. Alterations in ceramide concentration and pH determine the release of reactive oxygen species by Cftr-deficient macrophages on infection. J. Immunol. 2010, 184:5104-5111.
25. Pier G.B., Grout M., Zaidi T.S., Olsen J.C., Johnson L.G., Yankaskas J.R., Goldberg J.B. Role of mutant CFTR in hypersusceptibility of cystic fibrosis patients to lung infections. Science 1996, 271:64-67.
26. Brodlie M., McKean M.C., Johnson G.E., Gray J., Fisher A.J., Corris P.A., Lordan J.L., Ward C. Ceramide is increased in the lower airway epithelium of people with advanced cystic fibrosis lung disease. Am. J. Respir. Crit. Care Med. 2010, 182:369-375.
27. Charizopoulou N., Jansen S., Dorsch M., Stanke F., Dorin J.R., Hedrich H.J., Tümmler B. Instability of the insertional mutation in CftrTgH(neoim)Hgu cystic fibrosis mouse model. BMC Genet. 2004, 5:6.
28. Wölbeling F., Munder A., Stanke F., Tümmler B., Baumann U. Head-out spirometry accurately monitors the course of Pseudomonas aeruginosa lung infection in mice. Respiration 2010, 80:340-346.
29. Uhlig S., Gulbins E. Sphingolipids in the lungs. Am. J. Respir. Crit. Care Med. 2008, 178:1100-1114.
30. Kornhuber J., Tripal P., Reichel M., Terfloth L., Bleich S., Wiltfang J., Gulbins E. Identification of new functional inhibitors of acid sphingomyelinase using a structure-property-activity relation model. J. Med. Chem. 2008, 51:219-237.
31. Hurwitz R., Ferlinz K., Sandhoff K. The tricyclic antidepressant desipramine causes proteolytic degradation of lysosomal sphingomyelinase in human fibroblasts. Biol. Chem. Hoppe Seyler 1994, 375:447-450.
32. Ulrich M., Worlitzsch D., Viglio S., Siegmann N., Ladarola P., Shute J.K., Geiser M., Pier G.B., Friedel G., Barr M.L., Schuster A., Meyer K.C., Ratjen F., Bjarnsholt T., Gulbins E., Döring G. Alveolar inflammation in cystic fibrosis. J. Cyst. Fibros. 2010, 9:217-227.
33. Riethmüller J., Anthonysamy J., Serra E., Schwab M., Döring G., Gulbins E. Therapeutic efficacy and safety of amitriptyline in patients with cystic fibrosis. Cell. Physiol. Biochem. 2009, 24:65-72.