Exogenous sphingomyelinase causes impaired intestinal epithelial barrier function

World Journal of Gastroenterology

Volumn 13, Issue 39, 2007, Pages 5217-5225

  Bock, Jürgen ^a   Liebisch, Gerhard ^a   Schweimer, Joachim ^a   Schmitz, Gerd ^a   Rogler, Gerhard ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

Caco 2 cells; Ceramide; Cholesterol; Inflammatory bowel disease; Permeability; Tight junction

Indexed keywords

CERAMIDE; CHOLESTEROL; CLAUDIN 4; OCCLUDIN; SPHINGOLIPID; SPHINGOMYELIN; SPHINGOMYELIN PHOSPHODIESTERASE; THROMBOCYTE ACTIVATING FACTOR;

ARTICLE; CELL INTERACTION; CELL MEMBRANE PERMEABILITY; CELL STRAIN CACO 2; CONTROLLED STUDY; ENTERITIS; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IN VITRO STUDY; INTESTINE EPITHELIUM; INTESTINE MUCOSA PERMEABILITY; LIPID ANALYSIS; LIPID HYDROLYSIS; LIPID STORAGE; TANDEM MASS SPECTROMETRY; TIGHT JUNCTION; WESTERN BLOTTING;

EID: 34948885187     PISSN: 10079327     EISSN: None     Source Type: Journal    
DOI: 10.3748/wjg.v13.i39.5217     Document Type: Article

References (44)

1. Hollander D. Intestinal permeability, leaky gut, and intestinal disorders. Curr Gastroenterol Rep 1999; 1:410-416
2. Playford RJ, Ghosh S. Cytokines and growth factor modulators in intestinal inflammation and repair. J Pathol 2005; 205:417-425
3. Kim MY, Linardic C, Obeid L, Hannun Y. Identification of sphingomyelin turnover as an effector mechanism for the action of tumor necrosis factor alpha and gamma-interferon. Specific role in cell differentiation. J Biol Chem 1991; 266: 484-489
4. Schutze S, Potthoff K, Machleidt T, Berkovic D, Wiegmann K, Kronke M. TNF activates NF-kappa B by phosphatidylcholine-specific phospholipase C-induced "acidic" sphingomyelin breakdown. Cell 1992; 71:765-776
5. Schissel SL, Keesler GA, Schuchman EH, Williams KJ, Tabas I. The cellular trafficking and zinc dependence of secretory and lysosomal sphingomyelinase, two products of the acid sphingomyelinase gene. J Biol Chem 1998; 273:18250-18259
6. Gulbins E, Kolesnick R. Raft ceramide in molecular medicine. Oncogene 2003; 22:7070-7077
7. Grassme H, Jendrossek V, Bock J, Riehle A, Gulbins E. Ceramide-rich membrane rafts mediate CD40 clustering. J Immunol 2002; 168:298-307
8. 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 2001; 276:20589-20596
9. Cremesti A, Paris F, Grassme H, Holler N, Tschopp J, Fuks Z, Gulbins E, Kolesrtick R. Ceramide enables fas to cap and kill. J Biol Chem 2001; 276:23954-23961
10. Garcia-Ruiz C, Colell A, Mari M, Morales A, Calvo M, Enrich C, Fernandez-Checa JC. Defective TNF-alpha-mediated hepatocellular apoptosis and liver damage in acidic sphingomyelinase knockout mice. J Clin Invest 2003; 111: 197-208
11. Santana P, Pena LA, Haimovitz-Friedman A, Martin S, Green D, McLoughlin M, Cordon-Cardo C, Schuchman EH, Fuks Z, Kolesnick R. Acid sphingomyelinase-deficient human lymphoblasts and mice are defective in radiation-induced apoptosis. Cell 1996; 86:189-199
12. Morita Y, Perez GI, Paris F, Miranda SR, Ehleiter D, Haimovitz-Friedman A, Fuks Z, Xie Z, Reed JC, Schuchman EH, Kolesnick RN, Tilly JL. Oocyte apoptosis is suppressed by disruption of the acid sphingomyelinase gene or by sphingosine-1-phosphate therapy. Nat Med 2000; 6:1109-1114
13. Garcia-Barros M, Paris F, Cordon-Cardo C, Lyden D, Rafii S, Haimovitz-Friedman A, Fuks Z, Kolesnick R. Tumor response to radiotherapy regulated by endothelial cell apoptosis. Science 2003; 300:1155-1159
14. Yu ZF, Nikolova-Karakashian M, Zhou D, Cheng G, Schuchman EH, Mattson MP. Pivotal role for acidic sphingomyelinase in cerebral ischemia-induced ceramide and cytokine production, and neuronal apoptosis. J Mol Neurosci 2000; 15:85-97
15. Grassme H, Gulbins E, Brenner B, Ferlinz K, Sandhoff K, Harzer K, Lang F, Meyer TF. Acidic sphingomyelinase mediates entry of N. gonorrhoeae into nonphagocytic cells. Cell 1997; 91:605-615
16. Hauck CR, Grassme H, Bock J, Jendrossek V, Ferlinz K, Meyer TF, Gulbins E. Acid sphingomyelinase is involved in CEACAM receptor-mediated phagocytosis of Neisseria gonorrhoeae. FEBS Lett 2000; 478:260-266
17. Grassme H, Jendrossek V, Riehle A, von Kurthy G, Berger J, Schwarz H, Weller M, Kolesnick R, Gulbins E. Host defense against Pseudomonas aeruginosa requires ceramide-rich membrane rafts. Nat Med 2003; 9:322-330
18. Jan JT, Chatterjee S, Griffin DE. Sindbis virus entry into cells triggers apoptosis by activating sphingomyelinase, leading to the release of ceramide. J Virol 2000; 74:6425-6432
19. Grassme H, Riehle A, Wilker B, Gulbins E. Rhinoviruses infect human epithelial cells via ceramide-enriched membrane platforms. J Biol Chem 2005; 280:26256-26262
20. Megha, London E. Ceramide selectively displaces cholesterol from ordered lipid domains (rafts): implications for lipid raft structure and function. J Biol Chem 2004; 279:9997-10004
21. Montes LR, Ruiz-Arguello MB, Goni FM, Alonso A. Membrane restructuring via ceramide results in enhanced solute effiux. J Biol Chem 2002; 277:11788-11794
22. Brown DA, London E. Structure and function of sphingolipid-and cholesterol-rich membrane rafts. J Biol Chem 2000; 275: 17221-17224
23. Simons K, Ikonen E. Functional rafts in cell membranes. Nature 1997; 387:569-572
24. Rosella O, Sinclair A, Gibson PR. Polyunsaturated fatty acids reduce non-receptor-mediated transcellular permeation of protein across a model of intestinal epithelium in vitro. J Gastroenterol Hepatol 2000; 15:626-631
25. Usami M, Komurasaki T, Hanada A, Kinoshita K, Ohata A. Effect of gamma-linolenic acid or docosahexaenoic acid on tight junction permeability in intestinal monolayer cells and their mechanism by protein kinase C activation and/or eicosanoid formation. Nutrition 2003; 19:150-156
26. Shoda R, Matsueda K, Yamato S, Umeda N. Therapeutic efficacy of N-3 polyunsaturated fatty acid in experimental Crohn's disease. J Gastroenterol 1995; 30 Suppl 8:98-101
27. Belluzzi A, Brignola C, Campieri M, Pera A, Boschi S, Miglioli M. Effect of an enteric-coated fish-oil preparation on relapses in Crohn's disease. N Engl J Med 1996; 334:1557-1560
28. Nusrat A, Parkos CA, Verkade P, Foley CS, Liang TW, Innis-Whitehouse W, Eastburn KK, Madara JL. Tight junctions are membrane microdomains. J Cell Sci 2000; 113 (Pt 10): 1771-1781
29. Leung LW, Contreras RG, Flores-Maldonado C, Cereijido M, Rodriguez-Boulan E. Inhibitors of glycosphingolipid biosynthesis reduce transepithelial electrical resistance in MDCK I and FRT cells. Am J Physiol Cell Physiol 2003; 284: C1021-C1030
30. Lambert D, O'Neill CA, Padfield PJ. Depletion of Caco-2 cell cholesterol disrupts barrier function by altering the detergent solubility and distribution of specific tight-junction proteins. Biochem J 2005; 387:553-560
31. Bruewer M, Luegering A, Kucharzik T, Parkos CA, Madara JL, Hopkins AM, Nusrat A. Proinflammatory cytokines disrupt epithelial barrier function by apoptosis-independent mechanisms. J Immunol 2003; 171:6164-6172
32. Brugger B, Erben G, Sandhoff R, Wieland FT, Lehmann WD. Quantitative analysis of biological membrane lipids at the low picomole level by nano-electrospray ionization tandem mass spectrometry. Proc Natl Acad Sci USA 1997; 94:2339-2344
33. Liebisch G, Drobnik W, Lieser B, Schmitz G. High-throughput quantification of lysophosphatidylcholine by electrospray ionization tandem mass spectrometry. Clin Chem 2002; 48: 2217-2224
34. Liebisch G, Lieser B, Rathenberg J, Drobnik W, Schmitz G. High-throughput quantification of phosphatidylcholine and sphingomyelin by electrospray ionization tandem mass spectrometry coupled with isotope correction algorithm. Biochim Biophys Acta 2004; 1686:108-117
35. Liebisch G, Drobnik W, Reil M, Trumbach B, Arnecke R, Olgemoller B, Roscher A, Schmitz G. Quantitative measurement of different ceramide species from crude cellular extracts by electrospray ionization tandem mass spectrometry (ESI-MS/MS). J Lipid Res 1999; 40:1539-1546
36. Liebisch G, Binder M, Schifferer R, Langmann T, Schulz B, Schmitz G. High throughput quantification of cholesterol and cholesteryl ester by electrospray ionization tandem mass spectrometry (ESI-MS/MS). Biochim Biophys Acta 2006; 1761: 121-128
37. Hidalgo IJ, Raub TJ, Borchardt RT. Characterization of the human colon carcinoma cell line (Caco-2) as a model system for intestinal epithelial permeability. Gastroenterology 1989; 96: 736-749
38. Wong ML, Xie B, Beatini N, Phu P, Marathe S, Johns A, Gold PW, Hirsch E, Williams KJ, Licinio J, Tabas I. Acute systemic inflammation up-regulates secretory sphingomyelinase in vivo: a possible link between inflammatory cytokines and atherogenesis. Proc Natl Acad Sci USA 2000; 97:8681-8686
39. Goggel R, Winoto-Morbach S, Vielhaber G, Imai Y, Lindner K, Brade L, Brade H, Ehlers S, Slutsky AS, Schutze S, Gulbins E, Uhlig S. PAF-mediated pulmonary edema: a new role for acid sphingomyelinase and ceramide. Nat Med 2004; 10:155-160
40. Holopainen JM, Subramanian M, Kinnunen PK. Sphingomyelinase induces lipid microdomain formation in a fluid phosphatidylcholine/ sphingomyelin membrane. Biochemistry 1998; 37:17562-17570
41. Nurminen TA, Holopainen JM, Zhao H, Kinnunen PK. Observation of topical catalysis by sphingomyelinase coupled to microspheres. J Am Chem Soc 2002; 124:12129-12134
42. Ruiz-Arguello MB, Basanez G, Goni FM, Alonso A. Different effects of enzyme-generated ceramides and diacylglycerols in phospholipid membrane fusion and leakage. J Biol Chem 1996; 271:26616-26621
43. Siskind LJ, Colombini M. The lipids C2- and C16-ceramide form large stable channels. Implications for apoptosis. J Biol Chem 2000; 275:38640-38644
44. Stremmel W, Merle U, Zahn A, Autschbach F, Hinz U, Ehehalt R. Retarded release phosphatidylcholine benefits patients with chronic active ulcerative colitis. Gut 2005; 54:966-971