Alkaline ceramidase 3 deficiency aggravates colitis and colitis-associated tumorigenesis in mice by hyperactivating the innate immune system

Cell Death and Disease

Volumn 7, Issue 3, 2016, Pages

  Wang, K ^a,b,c   Xu, R ^a,b   Snider, A J ^a,b,d   Schrandt, J ^a   Li, Y ^a,b   Bialkowska, A B ^a   Li, M ^c   Zhou, J ^c   Hannun, Y A ^a,b   Obeid, L M ^a,b,d   Yang, V W ^a   Mao, C ^a,b  

^a STONY BROOK UNIVERSITY   (United States)

^b Stony Brook School of Dental Medicine   (United States)

^c SOUTHERN MEDICAL UNIVERSITY   (China)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE CERAMIDASE; CERAMIDE; CYTOKINE; DEXTRAN SULFATE; LIPOPOLYSACCHARIDE;

ANIMAL; C57BL MOUSE; CELL TRANSFORMATION; COLITIS; COLON; CYTOLOGY; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; ENZYME SPECIFICITY; FEMALE; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; KNOCKOUT MOUSE; MALE; METABOLISM; MONONUCLEAR CELL; MOUSE; PATHOLOGY; UPREGULATION;

ALKALINE CERAMIDASE; ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; CERAMIDES; COLITIS; COLON; CYTOKINES; DEXTRAN SULFATE; DISEASE MODELS, ANIMAL; FEMALE; IMMUNITY, INNATE; LEUKOCYTES, MONONUCLEAR; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; SUBSTRATE SPECIFICITY; UP-REGULATION;

EID: 85011074721     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2016.36     Document Type: Article

References (58)

1. Mullen TD, Hannun YA, Obeid LM. Ceramide synthases at the centre of sphingolipid metabolism and biology. Biochem J 2012; 441: 789-802.
2. Mao C, Obeid LM. Ceramidases: regulators of cellular responses mediated by ceramide, sphingosine, and sphingosine-1-phosphate. Biochim Biophys Acta 2008; 1781: 424-434.
3. Sakata A, Ochiai T, Shimeno H, Hikishima S, Yokomatsu T, Shibuya S 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.
4. Andreyev AY, Fahy E, Guan Z, Kelly S, Li X, McDonald JG et al. Subcellular organelle lipidomics in TLR-4-activated macrophages. J Lipid Res 2010; 51: 2785-2797.
5. Schilling JD, Machkovech HM, He L, Sidhu R, Fujiwara H, Weber K et al. Palmitate and lipopolysaccharide trigger synergistic ceramide production in primary macrophages. J Biol Chem 2013; 288: 2923-2932.
6. Chang ZQ, Lee SY, Kim HJ, Kim JR, Kim SJ, Hong IK et al. Endotoxin activates de novo sphingolipid biosynthesis via nuclear factor kappa B-mediated upregulation of Sptlc2. Prostaglandins Other Lipid Mediat 2011; 94: 44-52.
7. Abraham C, Cho JH. Inflammatory bowel disease. N Engl J Med 2009; 361: 2066-2078.
8. Fischbeck A, Leucht K, Frey-Wagner I, Bentz S, Pesch T, Kellermeier S et al. Sphingomyelin induces cathepsin D-mediated apoptosis in intestinal epithelial cells and increases inflammation in DSS colitis. Gut 2011; 60: 55-65.
9. Hu W, Xu R, Sun W, Szulc ZM, Bielawski J, Obeid LM et al. Alkaline ceramidase 3 (ACER3) hydrolyzes unsaturated long-chain ceramides, and its down-regulation inhibits both cell proliferation and apoptosis. J Biol Chem 2010; 285: 7964-7976.
10. Wang K, Xu R, Schrandt J, Shah P, Gong YZ, Preston C et al. Alkaline ceramidase 3 deficiency results in Purkinje cell degeneration and cerebellar ataxia due to dyshomeostasis of sphingolipids in the brain. PLoS Genet 2015; 11: e1005591.
11. Reynier F, de Vos AF, Hoogerwerf JJ, Bresser P, van der Zee JS, Paye M et al. Gene expression profiles in alveolar macrophages induced by lipopolysaccharide in humans. Mol Med 2012; 18: 1303-1311.
12. Martinez FO, Gordon S, Locati M, Mantovani A. Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J Immunol 2006; 177: 7303-7311.
13. Dower K, Ellis DK, Saraf K, Jelinsky SA, Lin LL. Innate immune responses to TREM-1 activation: overlap, divergence, and positive and negative cross-talk with bacterial lipopolysaccharide. J Immunol 2008; 180: 3520-3534.
14. Macagno A, Molteni M, Rinaldi A, Bertoni F, Lanzavecchia A, Rossetti C et al. A cyanobacterial LPS antagonist prevents endotoxin shock and blocks sustained TLR4 stimulation required for cytokine expression. J Exp Med 2006; 203: 1481-1492.
15. Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell 2006; 124: 783-801.
16. MacKichan ML, DeFranco AL. Role of ceramide in lipopolysaccharide (LPS)-induced signaling. LPS increases ceramide rather than acting as a structural homolog. J Biol Chem 1999; 274: 1767-1775.
17. Sartor RB. Microbial influences in inflammatory bowel diseases. Gastroenterology 2008; 134: 577-594.
18. Gardiner KR, Erwin PJ, Anderson NH, Barr JG, Halliday MI, Rowlands BJ. Colonic bacteria and bacterial translocation in experimental colitis. Br J Surg 1993; 80: 512-516.
19. Gabele E, Dostert K, Hofmann C, Wiest R, Scholmerich J, Hellerbrand C et al. DSS induced colitis increases portal LPS levels and enhances hepatic inflammation and fibrogenesis in experimental NASH. J Hepatol 2011; 55: 1391-1399.
20. Hudcovic T, Stepankova R, Cebra J, Tlaskalova-Hogenova H. The role of microflora in the development of intestinal inflammation: acute and chronic colitis induced by dextran sulfate in germ-free and conventionally reared immunocompetent and immunodeficient mice. Folia Microbiologica 2001; 46: 565-572.
21. Tolstanova G, Deng X, French SW, Lungo W, Paunovic B, Khomenko T et al. Early endothelial damage and increased colonic vascular permeability in the development of experimental ulcerative colitis in rats and mice. Lab Invest 2012; 92: 9-21.
22. Nakamura M, Asada M, Matsui H, Hibi N, Tsuchimoto K, Inoue J et al. Increased microvascular permeability in early stage of dextran sulfate sodium-induced colitis: its interaction with lansoprazole binding sites. Clin Hemorheol Microcirc 2006; 34: 193-199.
23. Kabashima K, Saji T, Murata T, Nagamachi M, Matsuoka T, Segi E et al. The prostaglandin receptor EP4 suppresses colitis, mucosal damage and CD4 cell activation in the gut. J Clin Invest 2002; 109: 883-893.
24. Snider AJ, Kawamori T, Bradshaw SG, Orr KA, Gilkeson GS, Hannun YA et al. A role for sphingosine kinase 1 in dextran sulfate sodium-induced colitis. FASEB J 2009; 23: 143-152.
25. Snider AJ, Wu BX, Jenkins RW, Sticca JA, Kawamori T, Hannun YA et al. Loss of neutral ceramidase increases inflammation in a mouse model of inflammatory bowel disease. Prostaglandins Other Lipid Mediat 2012; 99: 124-130.
26. Ullman TA, Itzkowitz SH. Intestinal inflammation and cancer. Gastroenterology 2011; 140: 1807-1816.
27. De Robertis M, Massi E, Poeta ML, Carotti S, Morini S, Cecchetelli L et al. The AOM/DSS murine model for the study of colon carcinogenesis: from pathways to diagnosis and therapy studies. J Carcinog 2011; 10: 9.
28. Maceyka M, Spiegel S. Sphingolipid metabolites in inflammatory disease. Nature 2014; 510: 58-67.
29. Sakata A, Yasuda K, Ochiai T, Shimeno H, Hikishima S, Yokomatsu 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 sodiuminduced colitis in mice. Cell Immunol 2007; 245: 24-31.
30. Halasiddappa LM, Koefeler H, Futerman AH, Hermetter A. Oxidized phospholipids induce ceramide accumulation in RAW 264.7 macrophages: role of ceramide synthases. PLoS One 2013; 8: e70002.
31. Schiffmann S, Ferreiros N, Birod K, Eberle M, Schreiber Y, Pfeilschifter W et al. Ceramide synthase 6 plays a critical role in the development of experimental autoimmune encephalomyelitis. J Immunol 2012; 188: 5723-5733.
32. Tong M, Longato L, Ramirez T, Zabala V, Wands JR, de la Monte SM. Therapeutic reversal of chronic alcohol-related steatohepatitis with the ceramide inhibitor myriocin. Int J Exp Pathol 2014; 95: 49-63.
33. Caretti A, Bragonzi A, Facchini M, De Fino I, Riva C, Gasco P et al. Anti-inflammatory action of lipid nanocarrier-delivered myriocin: therapeutic potential in cystic fibrosis. Biochim Biophys Acta 2014; 1840: 586-594.
34. Teichgraber V, Ulrich M, Endlich N, Riethmuller J, Wilker B, De Oliveira-Munding CC et al. Ceramide accumulation mediates inflammation, cell death and infection susceptibility in cystic fibrosis. Nat Med 2008; 14: 382-391.
35. Bauer J, Liebisch G, Hofmann C, Huy C, Schmitz G, Obermeier F et al. Lipid alterations in experimental murine colitis: role of ceramide and imipramine for matrix metalloproteinase-1 expression. PLoS One 2009; 4: e7197.
36. Jin J, Zhang X, Lu Z, Perry DM, Li Y, Russo SB et al. Acid sphingomyelinase plays a key role in palmitic acid-amplified inflammatory signaling triggered by lipopolysaccharide at low concentrations in macrophages. Am J Physiol Endocrinol Metab 2013; 305: E853-E867.
37. Mazzei JC, Zhou H, Brayfield BP, Hontecillas R, Bassaganya-Riera J, Schmelz EM. Suppression of intestinal inflammation and inflammation-driven colon cancer in mice by dietary sphingomyelin: importance of peroxisome proliferator-activated receptor gamma expression. J Nutr Biochem 2011; 22: 1160-1171.
38. von Bismarck P, Winoto-Morbach S, Herzberg M, Uhlig U, Schutze S, Lucius R et al. IKK NBD peptide inhibits LPS induced pulmonary inflammation and alters sphingolipid metabolism in a murine model. Pulmonary Pharmacol Ther 2012; 25: 228-235.
39. Santinha DR, Marques DR, Maciel EA, Simoes CS, Rosa S, Neves BM et al. Profiling changes triggered during maturation of dendritic cells: a lipidomic approach. Anal Bioanal Chem 2012; 403: 457-471.
40. Grammatikos G, Ferreiros N, Bon D, Schwalm S, Dietz J, Berkowski C et al. Variations in serum sphingolipid levels associate with liver fibrosis progression and poor treatment outcome in HCV but not HBV infection. Hepatology 2015; 61: 812-822.
41. Jozefowski S, Czerkies M, Lukasik A, Bielawska A, Bielawski J, Kwiatkowska K et al. Ceramide and ceramide 1-phosphate are negative regulators of TNF-alpha production induced by lipopolysaccharide. J Immunol 2010; 185: 6960-6973.
42. Chiba N, Masuda A, Yoshikai Y, Matsuguchi T. Ceramide inhibits LPS-induced production of IL-5, IL-10, and IL-13 from mast cells. J Cell Physiol 2007; 213: 126-136.
43. Grosch S, Schiffmann S, Geisslinger G. Chain length-specific properties of ceramides. Prog Lipid Res 2012; 51: 50-62.
44. Lu YC, Yeh WC, Ohashi PS. LPS/TLR4 signal transduction pathway. Cytokine 2008; 42: 145-151.
45. Triantafilou M, Miyake K, Golenbock DT, Triantafilou K. Mediators of innate immune recognition of bacteria concentrate in lipid rafts and facilitate lipopolysaccharide-induced cell activation. J Cell Sci 2002; 115: 2603-2611.
46. Cremesti AE, Goni FM, Kolesnick R. Role of sphingomyelinase and ceramide in modulating rafts: do biophysical properties determine biologic outcome? FEBS Lett 2002; 531: 47-53.
47. Megha, Sawatzki P, Kolter T, Bittman R, London E. Effect of ceramide N-acyl chain and polar headgroup structure on the properties of ordered lipid domains (lipid rafts). Biochim Biophys Acta 2007; 1768: 2205-2212.
48. Hailemariam TK, Huan C, Liu J, Li Z, Roman C, Kalbfeisch M et al. Sphingomyelin synthase 2 deficiency attenuates NFkappaB activation. Arterioscler Thromb Vasc Biol 2008; 28: 1519-1526.
49. Liu J, Huan C, Chakraborty M, Zhang H, Lu D, Kuo MS et al. Macrophage sphingomyelin synthase 2 deficiency decreases atherosclerosis in mice. Circ Res 2009; 105: 295-303.
50. McGuckin MA, Eri R, Simms LA, Florin TH, Radford-Smith G. Intestinal barrier dysfunction in inflammatory bowel diseases. Inflamm Bowel Dis 2009; 15: 100-113.
51. Gupta S. A decision between life and death during TNF-alpha-induced signaling. J Clin Immunol 2002; 22: 185-194.
52. Xu R, Jin J, Hu W, Sun W, Bielawski J, Szulc Z et al. Golgi alkaline ceramidase regulates cell proliferation and survival by controlling levels of sphingosine and S1P. Faseb J 2006; 20: 1813-1825.
53. Sun W, Xu R, Hu W, Jin J, Crellin HA, Bielawski J et al. Upregulation of the human alkaline ceramidase 1 and acid ceramidase mediates calcium-induced differentiation of epidermal keratinocytes. J Invest Dermatol 2008; 128: 389-397.
54. Ozaki H, Kawai T, Shuttleworth CW, Won KJ, Suzuki T, Sato K et al. Isolation and characterization of resident macrophages from the smooth muscle layers of murine small intestine. Neurogastroent Motil 2004; 16: 39-51.
55. Whitehead RH, Demmler K, Rockman SP, Watson NK. Clonogenic growth of epithelial cells from normal colonic mucosa from both mice and humans. Gastroenterology 1999; 117: 858-865.
56. Camerer E, Regard JB, Cornelissen I, Srinivasan Y, Duong DN, Palmer D et al. Sphingosine-1-phosphate in the plasma compartment regulates basal and inflammation-induced vascular leak in mice. J Clin Invest 2009; 119: 1871-1879.
57. Tolstanova G, Deng XM, French SW, Lungo W, Paunovic B, Khomenko T et al. Early endothelial damage and increased colonic vascular permeability in the development of experimental ulcerative colitis in rats and mice. Lab Invest 2012; 92: 9-21.
58. Maines LW, Fitzpatrick LR, French KJ, Zhuang Y, Xia Z, Keller SN et al. Suppression of ulcerative colitis in mice by orally available inhibitors of sphingosine kinase. Dig Dis Sci 2008; 53: 997-1012.