Sphingomyelin induces cathepsin D-mediated apoptosis in intestinal epithelial cells and increases inflammation in DSS colitis

Gut

Volumn 60, Issue 1, 2011, Pages 55-65

  Fischbeck, Anne ^a   Leucht, Katharina ^b   Frey Wagner, Isabelle ^b   Bentz, Susanne ^b   Pesch, Theresa ^b   Kellermeier, Silvia ^b   Krebs, Michaela ^b   Fried, Michael ^b   Rogler, Gerhard ^b   Hausmann, Martin ^b   Humpf, Hans Ulrich ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CASPASE 9; CATHEPSIN D; CERAMIDE; DEXTRAN SULFATE; INTERLEUKIN 10; SPHINGOMYELIN;

ACUTE DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; C57BL 6 MOUSE; COLITIS; CONTROLLED STUDY; DIETARY INTAKE; ENZYME ACTIVATION; FEMALE; FLUORESCENCE ACTIVATED CELL SORTER; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INTESTINE EPITHELIUM CELL; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; WEIGHT REDUCTION; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; CATHEPSIN D; COLITIS; COLONOSCOPY; DEXTRAN SULFATE; DIETARY FATS; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; FECES; FEMALE; INTESTINAL MUCOSA; MICE; MICE, INBRED C57BL; SIGNAL TRANSDUCTION; SPHINGOMYELINS; WEIGHT LOSS;

EID: 78651245288     PISSN: 00175749     EISSN: 14683288     Source Type: Journal    
DOI: 10.1136/gut.2009.201988     Document Type: Article

References (33)

1. Stremmel W, Merle U, Zahn A, et al. Retarded release phosphatidylcholine benefits patients with chronic active ulcerative colitis. Gut 2005;54:966-71. (Pubitemid 40873911)
2. Nixon GF. Sphingolipids in inflammation: pathological implications and potential therapeutic targets. Br J Pharmacol 2009;158:982-93.
3. McCole DF, Barrett KE. Varied role of the gut epithelium in mucosal homeostasis. Curr Opin Gastroenterol 2007;23:647-54.
4. Strater J, Wellisch I, Riedl S, et al. CD95 (APO-1/Fas)-mediated apoptosis in colon epithelial cells: a possible role in ulcerative colitis. Gastroenterology 1997;113:160-7.
5. Huwiler A, Kolter T, Pfeilschifter J, et al. Physiology and pathophysiology of sphingolipid metabolism and signaling. Biochim Biophys Acta 2000;1485:63-99.
6. Hannun YA, Obeid LM. Principles of bioactive lipid signalling: lessons from sphingolipids. Nat Rev Mol Cell Biol 2008;9:139-50.
7. Mizushima N, Koike R, Kohsaka H, et al. Ceramide induces apoptosis via CPP32 activation. FEBS Lett 1996;395:267-71.
8. Ruvolo PP, Deng X, Ito T, et al. Ceramide induces Bcl2 dephosphorylation via a mechanism involving mitochondrial PP2A. J Biol Chem 1999;274:20296-300. (Pubitemid 29340382)
9. Ghafourifar P, Klein SD, Schucht O, et al. Ceramide induces cytochrome c release from isolated mitochondria. Importance of mitochondrial redox state. J Biol Chem 1999;274:6080-4.
10. Heinrich M, Wickel M, Schneider-Brachert W, et al. Cathepsin D targeted by acid sphingomyelinase-derived ceramide. EMBO J 1999;18:5252-63.
11. Heinrich M, Neumeyer J, Jakob M, et al. Cathepsin D links TNF-induced acid sphingomyelinase to Bid-mediated caspase-9 and -3 activation. Cell Death Differ 2004;11:550-63.
12. Dobrowsky RT, Kamibayashi C, Mumby MC, et al. Ceramide activates heterotrimeric protein phosphatase 2A. J Biol Chem 1993;268:15523-30.
13. Levade T, Jaffrezou JP. Signalling sphingomyelinases: which, where, how and why? Biochim Biophys Acta 1999;1438:1-17.
14. Schmelz EM, Crall KJ, Larocque R, et al. Uptake and metabolism of sphingolipids in isolated intestinal loops of mice. J Nutr 1994;124:702-12. (Pubitemid 24157291)
15. Nilsson A. The presence of spingomyelin- and ceramide-cleaving enzymes in the small intestinal tract. Biochim Biophys Acta 1969;176:339-47.
16. Fischbeck A, Kruger M, Blaas N, et al. Analysis of sphingomyelin in meat based on hydrophilic interaction liquid chromatography coupled to electrospray ionization-tandem mass spectrometry (HILIC-HPLC-ESI-MS/MS). J Agric Food Chem 2009;57:9469-74.
17. Vesper H, Schmelz EM, Nikolova-Karakashian MN, et al. Sphingolipids in food and the emerging importance of sphingolipids to nutrition. J Nutr 1999;129:1239-50.
18. Duan RD, Nilsson A. Metabolism of sphingolipids in the gut and its relation to inflammation and cancer development. Prog Lipid Res 2009;48:62-72.
19. Obermeier F, Kojouharoff G, Hans W, et al. Interferon-gamma (IFN-gamma)-and tumour necrosis factor (TNF)-induced nitric oxide as toxic effector molecule in chronic dextran sulphate sodium (DSS)-induced colitis in mice. Clin Exp Immunol 1999;116:238-45.
20. Becker C, Fantini MC, Neurath MF. High resolution colonoscopy in live mice. Nat Protoc 2006;1:2900-4.
21. Hausmann M, Obermeier F, Paper DH, et al. In vivo treatment with the herbal phenylethanoid acteoside ameliorates intestinal inflammation in dextran sulphate sodium-induced colitis. Clin Exp Immunol 2007;148:373-81.
22. Grossmann J, Walther K, Artinger M, et al. Progress on isolation and short-term ex-vivo culture of highly purified non-apoptotic human intestinal epithelial cells (IEC). Eur J Cell Biol 2003;82:262-70.
23. Sakata A, Ochiai T, Shimeno H, et al. Acid sphingomyelinase inhibition suppresses lipopolysaccharide-mediated release of inflammatory cytokines from macrophages and protects against disease pathology in dextran sulphate sodium-induced colitis in mice. Immunology 2007;122:54-64.
24. Cifone MG, Roncaioli P, De Maria R, et al. Multiple pathways originate at the Fas/APO-1 (CD95) receptor: sequential involvement of phosphatidylcholine- specific phospholipase C and acidic sphingomyelinase in the propagation of the apoptotic signal. EMBO J 1995;14:5859-68.
25. Zareie M, McKay DM, Kovarik GG, et al. Monocytes/macrophages evoke epithelial dysfunction: indirect role of tumor necrosis factor-alpha. Am J Physiol 1998;275:C932-9.
26. Sakata A, Yasuda K, Ochiai T, et al. Inhibition of lipopolysaccharide- induced release of interleukin-8 from intestinal epithelial cells by SMA, a novel inhibitor of sphingomyelinase and its therapeutic effect on dextran sulphate sodium-induced colitis in mice. Cell Immunol 2007;245:24-31. (Pubitemid 46776639)
27. Ahn EH, Schroeder JJ. Sphingoid bases and ceramide induce apoptosis in HT-29 and HCT-116 human colon cancer cells. Exp Biol Med (Maywood) 2002;227:345-53.
28. Furuya H, Ohkawara S, Nagashima K, et al. Dietary sphingomyelin alleviates experimental inflammatory bowel disease in mice. Int J Vitam Nutr Res 2008;78:41-9.
29. Reunanen N, Westermarck J, Hakkinen L, et al. Enhancement of fibroblast collagenase (matrix metalloproteinase-1) gene expression by ceramide is mediated by extracellular signal-regulated and stress-activated protein kinase pathways. J Biol Chem 1998;273:5137-45.
30. Meijer MJ, Mieremet-Ooms MA, van Hogezand RA, et al. Role of matrix metalloproteinase, tissue inhibitor of metalloproteinase and tumor necrosis factor-alpha single nucleotide gene polymorphisms in inflammatory bowel disease. World J Gastroenterol 2007;13:2960-6.
31. Bauer J, Huy C, Brenmoehl J, et al. Matrix metalloproteinase-1 expression induced by IL-1beta requires acid sphingomyelinase. FEBS Lett 2009;583:915-20.
32. Bauer J, Liebisch G, Hofmann C, et al. Lipid alterations in experimental murine colitis: role of ceramide and imipramine for matrix metalloproteinase-1 expression. PLoS One 2009;4:e7197.
33. Schutze S, Potthoff K, Machleidt T, et al. TNF activates NF-kappa B by phosphatidylcholine-specific phospholipase C-induced "acidic" sphingomyelin breakdown. Cell 1992;71:765-76.