289
Views
4
CrossRef citations to date
0
Altmetric
Reviews

Ceramide in cystic fibrosis

, , , , &
Pages 681-692 | Published online: 18 Jan 2017

References

  • Kerem B, Rommens JM, Buchanan JA et al. Identification of the cystic fibrosis gene: genetic analysis. Science 245, 1073–1080 (1989).
  • Riordan JR, Rommens JM, Kerem B et al. Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 245, 1066–1073 (1989).
  • White MB, Amos J, Hsu JM et al. A frame-shift mutation in the cystic fibrosis gene. Nature 344, 665–667 (1990).
  • Pier GB, Grout M, Zaidi T et al. Salmonella typhi uses CFTR to enter intestinal epithelial cells. Nature 393, 79–82 (1998).
  • Ratjen F, Döring G. Cystic fibrosis. Lancet 361, 681–689 (2003).
  • di Sant’Agnese PA, Darling RC, Perera GA, Shea E. Abnormal electrolyte composition of sweat in cystic fibrosis of the pancreas. Clinical significance and relationship to disease. Pediatrics 12, 549–563 (1953).
  • Quinton PM. Chloride impermeability in cystic fibrosis. Nature 301, 421–422 (1983).
  • Quinton PM, Bijman J. Higher bioelectric potentials due to decreased chloride absorption in the sweat glands of patients with cystic fibrosis. N. Engl. J. Med. 308, 1185–1189 (1983).
  • Knowles MR, Stutts MJ, Spock A et al. Abnormal ion permeation through cystic fibrosis respiratory epithelium. Science 221, 1067–1070 (1983).
  • Rommens JM, Iannuzzi MC, Kerem B et al. Identification of the cystic fibrosis gene: chromosome walking and jumping. Science 245, 1059–1065 (1989).
  • Rosenstein BJ, Langbaum TS. Incidence of meconium abnormalities in newborn infants with cystic fibrosis. Am. J. Dis. Child. 134, 72–73 (1980).
  • Chase HP, Long MA, Lavin MH. Cystic fibrosis and malnutrition. J. Pediatr. 95, 337–347 (1979).
  • Park RW, Grand RJ. Gastrointestinal manifestations of cystic fibrosis: a review. Gastroenterology 81, 1143–1161 (1981).
  • Balough K, McCubbin M, Weinberger M et al. The relationship between infection and inflammation in the early stages of lung disease from cystic fibrosis. Pediatr. Pulmonol. 20, 63–70 (1995).
  • Khan TZ, Wagener JS, Bost T et al. Early pulmonary inflammation in infants with cystic fibrosis. Am. J. Respir. Crit. Care Med. 151, 1075–1082 (1995).
  • Verhaeghe C, Delbecque K, de Leval L et al. Early inflammation in the airways of a cystic fibrosis foetus. J. Cyst. Fibros. 6, 304–308 (2007).
  • Tabary O, Escotte S, Couetil JP et al. Relationship between IkBa deficiency, NFkB activity and interleukin-8 production in CF human airway epithelial cells. Pflugers Arch. 443(Suppl. 1), S40–S44 (2002).
  • Tirouvanziam R, de Bentzmann S, Hubeau C et al. Inflammation and infection in naive human cystic fibrosis airway grafts. Am. J. Respir. Cell Mol. Biol. 23, 121–127 (2000).
  • Inoue H, Massion PP, Ueki IF et al. Pseudomonas stimulates interleukin-8 mRNA expression selectively in airway epithelium, in gland ducts, and in recruited neutrophils. Am. J. Respir. Cell Mol. Biol. 11, 651–663 (1994).
  • Oceandy D, McMorran BJ, Smith SN et al. 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. 11, 1059–1067 (2002).
  • Bonfield TL, Konstan MW, Burfeind P et al. Normal bronchial epithelial cells constitutively produce the anti-inflammatory cytokine interleukin-10, which is downregulated in cystic fibrosis. Am. J. Respir. Cell Mol. Biol. 13, 257–261 (1995).
  • Venkatakrishnan A, Stecenko AA, King G et al. Exaggerated activation of nuclear factor-kappaB and altered IkappaB-beta processing in cystic fibrosis bronchial epithelial cells. Am. J. Respir. Cell Mol. Biol. 23, 396–403 (2000).
  • Teichgräber V, Ulrich M, Endlich N et al. Ceramide accumulation mediates inflammation, cell death and infection susceptibility in cystic fibrosis. Nat. Med. 14, 382–391 (2008).
  • Ziobro R, Henry B, Edwards MJ et al. Ceramide mediates lung fibrosis in cystic fibrosis. Biochem. Biophys. Res. Commun. 434(4), 705–709 (2013).
  • DiMango E, Zar HJ, Bryan R, Prince A. Diverse Pseudomonas aeruginosa gene products stimulate respiratory epithelial cells to produce interleukin-8. J. Clin. Invest. 96, 2204–2210 (1995).
  • Heeckeren A, Walenga R, Konstan MW et al. Excessive inflammatory response of cystic fibrosis mice to bronchopulmonary infection with Pseudomonas aeruginosa. J. Clin. Invest. 100, 2810–2815 (1997).
  • Schultz MJ, Rijneveld AW, Florquin S et al. Role of interleukin-1 in the pulmonary immune response during Pseudomonas aeruginosa pneumonia. Am. J. Physiol. Lung Cell. Mol. Physiol. 282, L285–L290 (2002).
  • Danel C, Erzurum SC, McElvaney NG, Crystal RG. Quantitative assessment of the epithelial and inflammatory cell populations in large airways of normals and individuals with cystic fibrosis. Am. J. Respir. Crit. CareMed. 153, 362–368 (1996).
  • Stoltz DA, Meyerholz DK, Pezzulo AA et al. Cystic fibrosis pigs develop lung disease and exhibit defective bacterial eradication at birth. Sci. Transl. Med. 28, 29ra31 (2010).
  • Pier GB, Grout M, Zaidi TS et al. Role of mutant CFTR in hypersusceptibility of cystic fibrosis patients to lung infections. Science 271, 64–67 (1996).
  • Schroeder TH, Lee MM, Yacono PW et al. CFTR is a pattern recognition molecule that extracts Pseudomonas aeruginosa LPS from the outer membrane into epithelial cells and activates NF-kappa B translocation. Proc. Natl Acad. Sci. USA 99, 6907–6912 (2002).
  • Di A, Brown ME, Deriy LV et al. CFTR regulates phagosome acidification in macrophages and alters bactericidal activity. Nat. Cell Biol. 8, 933–944 (2006).
  • Barasch J, Kiss B, Prince A et al. Defective acidification of intracellular organelles in cystic fibrosis. Nature 352, 70–73 (1991).
  • Haggie PM, Verkman AS. Cystic fibrosis transmembrane conductance regulatorindependent phagosomal acidification in macrophages. J. Biol. Chem. 282, 31422–31428 (2007).
  • Lethem MI, James SL, Marriott C, Burke JF. The origin of DNA associated with mucus glycoproteins in cystic fibrosis sputum. Eur. Respir. J. 3, 19–23 (1990).
  • Snouwaert JN, Brigman KK, Latour AM. et al. An animal model for cystic fibrosis made by gene targeting. Science 257, 1083–1088 (1992).
  • Ratcliff R, Evans MJ, Cuthbert AW et al. Production of a severe cystic fibrosis mutation in mice by gene targeting. Nat. Genet. 4, 35–41 (1993).
  • Zhou L, Dey CR, Wert SE et al. Correction of lethal intestinal defect in a mouse model of cystic fibrosis by human CFTR. Science 266, 1705–1708 (1994).
  • Dorin JR, Dickinson P, Emslie E et al. Successful targeting of the mouse cystic fibrosis transmembrane conductance regulator gene in embryonal stem cells. Transgenic Res. 1, 101–105 (1992).
  • Larbig M, Jansen S, Dorsch M et al. Residual cftr expression varies with age in cftrtm1Hgu cystic fibrosis mice: impact on morphology and physiology. Pathobiology 70, 89–97 (2002).
  • Gray MA, Winpenny JP, Porteous DJ et al. CFTR and calcium-activated chloride currents in pancreatic duct cells of a transgenic CF mouse. Am. J. Physiol. 266, C213–C221(1994).
  • Colledge WH, Abella BS, Southern KW et al. Generation and characterization of a delta F508 cystic fibrosis mouse model. Nat. Genet. 10, 445–452 (1995).
  • Zeiher BG, Eichwald E, Zabner J et al. A mouse model for the delta F508 allele of cystic fibrosis. J. Clin. Invest. 96, 2051–2064 (1995).
  • Delaney SJ, Alton EW, Smith SN et al. Cystic fibrosis mice carrying the missense mutation G551D replicate human genotype-phenotype correlations. EMBO J. 15, 955–963 (1996).
  • Dickinson P, Smith SN, Webb S et al. The severe G480C cystic fibrosis mutation, when replicated in the mouse, demonstrates mistrafficking, normal survival and organ-specific bioelectrics. Hum. Mol. Genet. 11, 243–225 (2002).
  • Hodges CA, Cotton CU, Palmert MR, Drumm ML, Generation of a conditional null allele for CFTR in mice. Genesis 46, 546–552 (2008).
  • Charizopoulou N, Jansen S, Dorsch M et al. Instability of the insertional mutation in CftrTgH(neoim)Hgu cystic fibrosis mouse model. BMC Genet. A 5, 6 (2004).
  • Charizopoulou N, Wilke M, Dorsch M et al. Spontaneous rescue from cystic fibrosis in a mouse model. BMC Genet. 7, 18 (2006).
  • Kent G, Iles R, Bear CE et al. Lung disease in mice with cystic fibrosis. J. Clin. Invest. 100, 3060–3069 (1997).
  • Kent G, Oliver M, Foskett JK et al. Phenotypic abnormalities in long-term surviving cystic fibrosis mice. Pediatr. Res. 40, 233–241 (1996).
  • Durie PR, Kent G, Phillips MJ, Ackerley CA. Characteristic multiorgan pathology of cystic fibrosis in a long-living cystic fibrosis transmembrane regulator knockout murine model. Am. J. Pathol. 164, 1481–1493 (2004).
  • Rogers CS, Stoltz DA, Meyerholz DK et al. Disruption of the CFTR gene produces a model of cystic fibrosis in newborn pigs. Science 321, 1837–1841 (2008).
  • Abu-El-Haija M, Sinkora M, Meyerholz DK et al. An activated immune and inflammatory response targets the pancreas of newborn pigs with cystic fibrosis. Pancreatology 11, 506–515 (2011).
  • Reznikov LR, Dong Q, Chen JH et al. CFTR-deficient pigs display peripheral nervous system defects at birth. Proc. Natl Acad. Sci. USA 110, 3083–3088 (2013).
  • Olivier AK, Yi Y, Sun X et al. Abnormal endocrine pancreas function at birth in cystic fibrosis ferrets. J. Clin. Invest. 122, 3755–3768 (2012).
  • Sun X, Sui H, Fisher JT et al. Disease phenotype of a ferret CFTR-knockout model of cystic fibrosis. J. Clin. Invest. 120, 3149–3160 (2010).
  • Hakomori S. Chemistry of glycosphingolipids. In: Sphingolipid Biochemistry. Kanfer JN, Hakomori S (Eds). Plenum Press, NY, USA, 1–165 (1983).
  • Barenholz Y, Thompson TE. Sphingomyelins in bilayers and biological membranes. Biochim. Biophys. Acta 604, 129–158 (1980).
  • Kolesnick RN, Goni FM, Alonso A. Compartmentalization of ceramide signaling: physical foundations and biological effects. J. Cell. Physiol. 184, 285–300 (2000).
  • Simons K, Ikonen E. Functional rafts in cell membranes. Nature 387, 569–572 (1997).
  • Brown DA, London E. Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 14, 111–136 (1998).
  • Xu X, Bittman R, Duportail G et al. Effect of the structure of natural sterols and sphingolipids on the formation of ordered sphingolipid/sterol domains (rafts). Comparison of cholesterol to plant, fungal, and disease-associated sterols and comparison of sphingomyelin, cerebrosides, and ceramide. J. Biol. Chem. 276, 33540–33546 (2001).
  • Gatt S, Herzl A, Barenholz Y. Hydrolysis of sphingomyelin liposomes by sphingomyelinase. FEBS Lett. 30, 281–285 (1973).
  • Futerman AH, Stieger B, Hubbard AL, Pagano RE. Sphingomyelin synthesis in rat liver occurs predominantly at the cis and medial cisternae of the Golgi apparatus. J. Biol. Chem. 265, 8650–8657 (1990).
  • Okino N, He X, Gatt S et al. The reverse activity of human acid ceramidase. J. Biol. Chem. 278, 29948–29953 (2003).
  • Ishibashi Y, Nakasone T, Kiyohara M et al. A novel endoglycoceramidase hydrolyzes oligogalactosylceramides to produce galactooligosaccharides and ceramides. J. Biol. Chem. 282, 11386–11396 (2007).
  • Grassmé H, Jekle A, Riehle A et al. CD95 signaling via ceramide-rich membrane rafts. J. Biol. Chem. 276, 20589–20596 (2001).
  • Gulbins E, Kolesnick RN. Raft ceramide in molecular medicine. Oncogene 22, 7070–7077 (2003).
  • Nurminen TA, Holopainen JM, Zhao H, Kinnunen PK. Observation of topical catalysis by sphingomyelinase coupled to microspheres. J. Am. Chem. Soc. 124, 12129–12134 (2002).
  • Grassmé H, Jendrossek V, Bock J et al. Ceramide-rich membrane rafts mediate CD40 clustering. J. Immunol. 168, 298–307 (2002).
  • Simarro M, Calvo J, Vilà JM et al. Signaling through CD5 involves acidic sphingomyelinase, protein kinase C-zeta, mitogen-activated protein kinase kinase, and c-Jun NH2-terminal kinase. J. Immunol. 162, 5149–5155 (1999).
  • Abdel Shakor AB, Kwiatkowska K, Sobota A. Cell surface ceramide generation precedes and controls FcgammaRII clustering and phosphorylation in rafts. J. Biol. Chem. 279, 36778–36787 (2004).
  • Goggel R, Winoto-Morbach S, Vielhaber G et al. PAF-mediated pulmonary edema: a new role for acid sphingomyelinase and ceramide. Nat. Med. 10, 155–160 (2004).
  • Pfeiffer A, Bottcher A, Orso E et al. Lipopolysaccharide and ceramide docking to CD14 provokes ligand-specific receptor clustering in rafts. Eur. J. Immunol. 31, 3153–3164 (2001).
  • Grassmé H, Jendrossek V, Riehle A et al. Host defense against Pseudomonas aeruginosa requires ceramide-rich membrane rafts. Nat. Med. 9, 322–330 (2003).
  • Esen M, Schreiner B, Jendrossek V et al. Mechanisms of Staphylococcus aureus induced apoptosis of human endothelial cells. Apoptosis 6, 431–439 (2001).
  • Grassmé H, Gulbins E, Brenner B et al. Acidic sphingomyelinase mediates entry of N. gonorrhoeae into nonphagocytic cells. Cell 91, 605–615 (1997).
  • Hauck CR, Grassmé H, Bock J et al. Acid sphingomyelinase is involved in CEACAM. receptor-mediated phagocytosis of Neisseria gonorrhoeae. FEBS Lett. 478, 260–266 (2000).
  • Gassert E, Avota E, Harms H et al. Induction of membrane ceramides: a novel strategy to interfere with T lymphocyte cytoskeletal reorganisation in viral immunosuppression. PLoS Pathog. 5, e1000623 (2009).
  • Grassmé H, Riehle A, Wilker B et al. Rhinoviruses infect human epithelial cells via ceramide-enriched membrane platforms, submitted for publication. J. Biol. Chem. 280, 26256–26262 (2005).
  • Santana P, Pena LA, Haimovitz-Friedman A et al. Acid sphingomyelinase-deficient human lymphoblasts and mice are defective in radiation-induced apoptosis. Cell 86, 189–199 (1996).
  • Rotolo JA, Zhang J, Donepudi M et al. Caspase-dependent and -independent activation of acid sphingomyelinase signaling. J. Biol. Chem. 280, 26425–26434 (2005).
  • Lacour S, Hammann A, Grazide S et al. Cisplatin-induced CD95 redistribution into membrane lipid rafts of HT29 human colon cancer cells. Cancer. Res. 64, 3593–3598 (2004).
  • Grammatikos G, Teichgräber V, Carpinteiro A et al. Over-expression of the acid sphingomyelinase sensitizes glioma cells to chemotherapy. Antioxid. Redox Signal. 9, 1449–1456 (2007).
  • Lang PA, Schenck M, Nicolay JP et al. Liver cell death and anemia in Wilson disease involve acid sphingomyelinase and ceramide. Nat. Med. 13, 164–170 (2007).
  • Scheel-Toellner D, Wang K, Craddock R et al. Reactive oxygen species limit neutrophil life span by activating death receptor signaling. Blood 104, 2557–2564 (2004).
  • Zhang Y, Li X, Grassmé H et al. Alterations in ceramide concentration and pH determine the release of reactive oxygen species by Cftr-deficient macrophages on infection. J. Immunol. 184, 5104–5111 (2010).
  • Becker KA, Riethmüller J, Lüth A et al. Acid sphingomyelinase inhibitors normalize pulmonary ceramide and inflammation in cystic fibrosis. Am. J. Respir. Cell Mol. Biol. 42, 716–724 (2010).
  • Becker KA, Henry B, Ziobro R et al. Role of CD95 in pulmonary inflammation and infection in cystic fibrosis. J. Mol. Med. 90, 1011–1023 (2012).
  • Becker KA, Tümmler B, Gulbins E, Grassmé H. Accumulation of ceramide in the trachea and intestine of cystic fibrosis mice causes inflammation and cell death. Biochem. Biophys. Res. Commun. 403, 368–374 (2010).
  • Bodas M, Min T, Mazur S, Vij N. Critical modifier role of membrane-cystic fibrosis transmembrane conductance regulatordependent ceramide signaling in lung injury and emphysema. J. Immunol. 186, 602–613 (2011).
  • Bodas M, Min T, Vij N. Critical role of CFTR-dependent lipid rafts in cigarette smoke-induced lung epithelial injury. Am. J. Physiol. Lung Cell. Mol. Physiol. 300, L811–L820 (2011).
  • Brodlie M, McKean MC, Johnson GE et al. Ceramide is increased in the lower airway epithelium of people with advanced cystic fibrosis lung disease. Am. J. Respir. Crit. Care Med. 182, 369–375 (2010).
  • Ulrich M, Worlitzsch D, Viglio S et al. Alveolar inflammation in cystic fibrosis. J. Cyst. Fibros. 9, 217–227 (2010).
  • Guilbault C, De Sanctis JB, Wojewodka G et al. Fenretinide corrects newly found ceramide deficiency in cystic fibrosis. Am. J. Respir. Cell Mol. Biol. 38, 47–56 (2008).
  • Cottart CH, Bonvin E, Rey C et al. Impact of nutrition on phenotype in CFTR-deficient mice. Pediatr. Res. 62, 528–532 (2007).
  • Borowitz D, Durie PR, Clarke LL et al. Gastrointestinal outcomes and confounders in cystic fibrosis. J. Pediatr. Gastroenterol. Nutr. 41, 273–285 (2005).
  • Bhuvaneswaran C, Venkatesan S, Mitropoulos KA. Lysosomal accumulation of cholesterol and sphingomyelin: evidence for inhibition of acid sphingomyelinase. Eur. J. Cell Biol. 73, 98–106 (1985).
  • Fuchs HJ, Borowitz DS, Christiansen DH et al. Effect of aerosolized recombinant human DNase on exacerbations of respiratory symptoms and on pulmonary function in patients with cystic fibrosis. The Pulmozyme Study Group. N. Eng. J. Med. 331, 637–642 (1994).
  • Maiuri L, Raia V, De Marco G et al. DNA fragmentation is a feature of cystic fibrosis epithelial cells: a disease with inappropriate apoptosis? FEBS Lett. 408, 225–231 (1997).
  • Li CM, Hong SB, Kopal G et al. Cloning and characterization of the full-length cDNA and genomic sequences encoding murine acid ceramidase. Genomics 50, 267–274 (1998).
  • Pezzulo AA, Tang XX, Hoegger MJ et al. Reduced airway surface pH impairs bacterial killing in the porcine cystic fibrosis lung. Nature 487, 109–113 (2013).
  • Ming Xu, Min Xia, Xiao-Xue Li et al. Requirement of translocated lysosomal V1 H+-ATPase for activation of membrane acid sphingomyelinase and raft clustering in coronary endothelial cells. Mol. Biol. Cell 23, 1546–1557 (2012).
  • Kowalski MP, Pier GB. Localization of cystic fibrosis transmembrane conductance regulator to lipid rafts of epithelial cells is required for Pseudomonas aeruginosa-induced cellular activation. J. Immunol. 172, 418–425 (2004).
  • Dudez R, Borot F, Huang S et al. CFTR in a lipid raft–TNFR1 complex modulates gap junctional intercellular communication and IL-8 secretion. Biochim. Biophys. Acta 1783, 779–788 (2008).
  • Borot F, Vieu DL, Faure G et al. Eicosanoid release is increased by membrane destabilization and CFTR inhibition in Calu-3 cell. PLoS ONE 4, e7116 (2009).
  • Wang D, Wang W, Duan et al. Functional coupling of Gs and CFTR is independent of their association with lipid rafts in epithelial cells. Pflugers Arch. 456, 929–938 (2008).
  • Bajmoczi M, Gadjeva M, Alper SL et al. Cystic fibrosis transmembrane conductance regulator and caveolin-1 regulate epithelial cell internalization of Pseudomonas aeruginosa. Am. J. Physiol. Cell Physiol. 297, C263–C277 (2009).
  • Hurwitz R, Ferlinz K, Sandhoff K. The tricyclic antidepressant desipramine causes proteolytic degradation of lysosomal sphingomyelinase in human fibroblasts. Biol. Chem. Hoppe-Seyler 375, 447–450 (1994).
  • Kornhuber J, Tripal P, Reichel M et al. Identification of new functional inhibitors of acid sphingomyelinase using a structureproperty-activity relation model. J. Med. Chem. 51, 219–237 (2008).
  • Riethmüller J, Anthonysamy J, Emilio Serra E et al. Therapeutic efficacy and safety of amitriptyline in patients with cystic fibrosis. Cell. Physiol. Biochem. 24, 65–72 (2009).
  • Nährlich L, Mainz JG, Adams C et al. Therapy of CF-patients with amitriptyline and placebo – a randomised, double-blind, placebo-controlled Phase IIb multicenter, cohort-study. Cell. Physiol. Biochem. 31, 505–512 (2013).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.