Acid sphingomyelinase plays a key role in palmitic acid-amplified inflammatory signaling triggered by lipopolysaccharide at low concentrations in macrophages

American Journal of Physiology - Endocrinology and Metabolism

Volumn 305, Issue 7, 2013, Pages

  Jin, Junfei ^b   Zhang, Xiaoming ^b   Lu, Zhongyang ^a   Perry, David M ^b   Li, Yanchun ^b   Russo, Sarah Brice ^b   Cowart, L Ashley ^a,b   Hannun, Yusuf A ^c   Huang, Yan ^a,b  

^a RALPH H JOHNSON VA MEDICAL CENTER   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^c Stony Brook Medicine   (United States)

Author keywords

Fatty acid; Inflammation; Lipopolysaccharide; Sphingomyelinase; Toll like receptor

Indexed keywords

B7 ANTIGEN; BETA INTERFERON; CCAAT ENHANCER BINDING PROTEIN; CD86 ANTIGEN; COLONY STIMULATING FACTOR; CYCLOOXYGENASE 2; FATTY ACID; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 2; INTERLEUKIN 10; INTERLEUKIN 12P35; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; LYMPHOTOXIN; MONOCYTE CHEMOTACTIC PROTEIN 1; PALMITIC ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PROTEIN C JUN; PROTEIN MD 2; SPHINGOMYELIN; SPHINGOMYELIN PHOSPHODIESTERASE; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL ISOLATION; CONTROLLED STUDY; CULTURE MEDIUM; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FATTY ACID BLOOD LEVEL; GENE AMPLIFICATION; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; HYDROLYSIS; INFLAMMATION; MACROPHAGE; MOUSE; NONHUMAN; PERIODONTAL DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; UPREGULATION;

FATTY ACID; INFLAMMATION; LIPOPOLYSACCHARIDE; SPHINGOMYELINASE; TOLL-LIKE RECEPTOR;

ANIMALS; CELL LINE; INFLAMMATION; INTERLEUKIN-1 RECEPTOR-ASSOCIATED KINASES; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; NF-KAPPA B; PALMITIC ACID; SIGNAL TRANSDUCTION; SPHINGOMYELIN PHOSPHODIESTERASE; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4;

EID: 84884949243     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00251.2013     Document Type: Article

References (54)

1. Akira S, Kishimoto T. IL-6 and NF-IL6 in acute-phase response and viral infection. Immunol Rev 127: 25-50, 1992.
2. Beutler B. TLR4 as the mammalian endotoxin sensor. Curr Top Microbiol Immunol 270: 109-120, 2002.
3. Boden G. Obesity, insulin resistance and free fatty acids. Curr Opin Endocrinol Diabetes Obes 18: 139-143, 2011.
4. Bullon P, Morillo JM, Ramirez-Tortosa MC, Quiles JL, Newman HN, Battino M. Metabolic syndrome and periodontitis: is oxidative stress a common link? J Dent Res 88: 503-518, 2009.
5. Chaffee BW, Weston SJ. Association between chronic periodontal disease and obesity: a systematic review and meta-analysis. J Periodontol 81: 1708-1724, 2010.
6. Chang ZQ, Lee SY, Kim HJ, Kim JR, Kim SJ, Hong IK, Oh BC, Choi CS, Goldberg IJ, Park TS. Endotoxin activates de novo sphingolipid biosynthesis via nuclear factor kappa B-mediated upregulation of Sptlc2. Prostaglandins Other Lipid Mediat 94: 44-52, 2011.
7. Cheng AM, Handa P, Tateya S, Schwartz J, Tang C, Mitra P, Oram JF, Chait A, Kim F. Apolipoprotein A-I attenuates palmitate-mediated NF-κB activation by reducing Toll-like receptor-4 recruitment into lipid rafts. PLoS One 7: e33917, 2012.
8. Cronin JG, Turner ML, Goetze L, Bryant CE, Sheldon IM. Toll-like receptor 4 and MYD88-dependent signaling mechanisms of the innate immune system are essential for the response to lipopolysaccharide by epithelial and stromal cells of the bovine endometrium. Biol Reprod 86: 51, 2012.
9. Cuschieri J, Bulger E, Billgrin J, Garcia I, Maier RV. Acid sphingomyelinase is required for lipid Raft TLR4 complex formation. Surg Infect (Larchmt) 8: 91-106, 2007.
10. Deshmane SL, Kremlev S, Amini S, Sawaya BE. Monocyte chemoattractant protein-1 (MCP-1): an overview. J Interferon Cytokine Res 29: 313-326, 2009.
11. Fonseca JE, Santos MJ, Canhao H, Choy E. Interleukin-6 as a key player in systemic inflammation and joint destruction. Autoimmun Rev 8: 538-542, 2009.
12. Funaki M. Saturated fatty acids and insulin resistance. J Med Invest 56: 88-92, 2009.
13. Gao D, Pararasa C, Dunston CR, Bailey CJ, Griffiths HR. Palmitate promotes monocyte atherogenicity via de novo ceramide synthesis. Free Radic Biol Med 53: 796-806, 2012.
14. García-Ruiz C, Colell A, Marí M, Morales A, Calvo M, Enrich C, Fernández-Checa JC. Defective TNF-alpha-mediated hepatocellular apoptosis and liver damage in acidic sphingomyelinase knockout mice. J Clin Invest 111: 197-208, 2003.
15. Grassme H, Cremesti A, Kolesnick R, Gulbins E. Ceramide-mediated clustering is required for CD95-DISC formation. Oncogene 22: 5457-5470, 2003.
16. Green CD, Olson LK. Modulation of palmitate-induced endoplasmic reticulum stress and apoptosis in pancreatic β-cells by stearoyl-CoA desaturase and Elovl6. Am J Physiol Endocrinol Metab 300: E640-E649, 2011.
17. Grill V, Qvigstad E. Fatty acids and insulin secretion. Br J Nutr 83, Suppl 1: S79-S84, 2000.
18. Gupta S, Knight AG, Gupta S, Keller JN, Bruce-Keller AJ. Saturated long-chain fatty acids activate inflammatory signaling in astrocytes. J Neurochem 120: 1060-1071, 2012.
19. Haimovitz-Friedman A, Cordon-Cardo C, Bayoumy S, Garzotto M, McLoughlin M, Gallily R, Edwards CK 3rd, Schuchman EH, Fuks Z, Kolesnick R. Lipopolysaccharide induces disseminated endothelial apoptosis requiring ceramide generation. J Exp Med 186: 1831-1841, 1997.
20. Hanada K. Serine palmitoyltransferase, a key enzyme of sphingolipid metabolism. Biochim Biophys Acta 1632: 16-30, 2003.
21. Harte AL, Varma MC, Tripathi G, McGee KC, Al-Daghri NM, Al-Attas OS, Sabico S, O'Hare JP, Ceriello A, Saravanan P, Kumar S, McTernan PG. High fat intake leads to acute postprandial exposure to circulating endotoxin in type 2 diabetic subjects. Diabetes Care 35: 375-382, 2012.
22. Hartung T, von Aulock S, Wendel A. Role of granulocyte colonystimulating factor in infection and inflammation. Med Microbiol Immunol 187: 61-69, 1998.
23. He Q, Wang G, Dasgupta S, Dinkins M, Zhu G, Bieberich E. Characterization of an apical ceramide-enriched compartment regulating ciliogenesis. Mol Biol Cell 23: 3156-3166, 2012.
24. Hojjati MR, Li Z, Jiang XC. Serine palmitoyl-CoA transferase (SPT) deficiency and sphingolipid levels in mice. Biochim Biophys Acta 1737: 44-51, 2005.
25. Ishihara K, Hirano T. IL-6 in autoimmune disease and chronic inflammatory proliferative disease. Cytokine Growth Factor Rev 13: 357-368, 2002.
26. Jenkins GM, Cowart LA, Signorelli P, Pettus BJ, Chalfant CE, Hannun YA. Acute activation of de novo sphingolipid biosynthesis upon heat shock causes an accumulation of ceramide and subsequent dephosphorylation of SR proteins. J Biol Chem 277: 42572-42578, 2002.
27. Kadotani A, Tsuchiya Y, Hatakeyama H, Katagiri H, Kanzaki M. Different impacts of saturated and unsaturated free fatty acids on COX-2 expression in C2C12 myotubes. Am J Physiol Endocrinol Metab 297: E1291-E1303, 2009.
28. Kelpe CL, Moore PC, Parazzoli SD, Wicksteed B, Rhodes CJ, Poitout V. Palmitate inhibition of insulin gene expression is mediated at the transcriptional level via ceramide synthesis. J Biol Chem 278: 30015-30021, 2003.
29. Kishimoto T. Interleukin-6: discovery of a pleiotropic cytokine. Arthritis Res Ther 8, Suppl 2: S2, 2006.
30. Kristiansen OP, Mandrup-Poulsen T. Interleukin-6 and diabetes: the good, the bad, or the indifferent? Diabetes 54, Suppl 2: S114-S124, 2005.
31. Lakschevitz F, Aboodi G, Tenenbaum H, Glogauer M. Diabetes and periodontal diseases: interplay and links. Curr Diabetes Rev 7: 433-439, 2011.
32. Lalla E, Lamster IB, Drury S, Fu C, Schmidt AM. Hyperglycemia, glycoxidation and receptor for advanced glycation endproducts: potential mechanisms underlying diabetic complications, including diabetes-associated periodontitis. Periodontology 2000 23: 50-62, 2000.
33. Lassenius MI, Pietiläinen KH, Kaartinen K, Pussinen PJ, Syrjänen J, Forsblom C, Pörsti I, Rissanen A, Kaprio J, Mustonen J, Groop PH, Lehto M. Bacterial endotoxin activity in human serum is associated with dyslipidemia, insulin resistance, obesity, and chronic inflammation. Diabetes Care 34: 1809-1815, 2011.
34. Li Y, Samuvel DJ, Sundararaj KP, Lopes-Virella MF, Huang Y. IL-6 and high glucose synergistically upregulate MMP-1 expression by U937 mononuclear phagocytes via ERK1/2 and JNK pathways and c-Jun. J Cell Biochem 110: 248-259, 2010.
35. 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 274: 1767-1775, 1999.
36. Mamputu JC, Renier G. Differentiation of human monocytes to monocyte-derived macrophages is associated with increased lipoprotein lipaseinduced tumor necrosis factor-alpha expression and production: a process involving cell surface proteoglycans and protein kinase C. Arterioscler Thromb Vasc Biol 19: 1405-1411, 1999.
37. Memon RA, Holleran WM, Moser AH, Seki T, Uchida Y, Fuller J, Shigenaga JK, Grunfeld C, Feingold KR. Endotoxin and cytokines increase hepatic sphingolipid biosynthesis and produce lipoproteins enriched in ceramides and sphingomyelin. Arterioscler Thromb Vasc Biol 18: 1257-1265, 1998.
38. Mullen TD, Hannun YA, Obeid LM. Ceramide synthases at the centre of sphingolipid metabolism and biology. Biochem J 441: 789-802, 2012.
39. Mullen TD, Jenkins RW, Clarke CJ, Bielawski J, Hannun YA, Obeid LM. Ceramide synthase-dependent ceramide generation and programmed cell death: involvement of salvage pathway in regulating postmitochondrial events. J Biol Chem 286: 15929-15942, 2011.
40. Page RC. The etiology and pathogenesis of periodontitis. Compend Contin Educ Dent 23: 11-14, 2002.
41. Poggi M, Bastelica D, Gual P, Iglesias MA, Gremeaux T, Knauf C, Peiretti F, Verdier M, Juhan-Vague I, Tanti JF, Burcelin R, Alessi MC. C3H/HeJ mice carrying a toll-like receptor 4 mutation are protected against the development of insulin resistance in white adipose tissue in response to a high-fat diet. Diabetologia 50: 1267-1276, 2007.
42. Qi HY, Daniels MP, Liu Y, Chen LY, Alsaaty S, Levine SJ, Shelhamer JH. A cytosolic phospholipase A2-initiated lipid mediator pathway induces autophagy in macrophages. J Immunol 187: 5286-5292, 2011.
43. Qin J, Berdyshev E, Poirer C, Schwartz NB, Dawson G. Neutral sphingomyelinase 2 deficiency increases hyaluronan synthesis by upregulation of Hyaluronan synthase 2 through decreased ceramide production and activation of Akt. J Biol Chem 287: 13620-13632, 2012.
44. Rajakariar R, Yaqoob MM, Gilroy DW. COX-2 in inflammation and resolution. Mol Interv 6: 199-207, 2006.
45. Rola-Pleszczynski M, Stankova J. Leukotriene B4 enhances interleukin-6 (IL-6) production and IL-6 messenger RNA accumulation in human monocytes in vitro: transcriptional and posttranscriptional mechanisms. Blood 80: 1004-1011, 1992.
46. Schilling JD, Machkovech HM, He L, Sidhu R, Fujiwara H, Weber K, Ory DS, Schaffer JE. Palmitate and LPS trigger synergistic ceramide production in primary macrophages. J Biol Chem 288: 2923-2932, 2012.
47. Schwartz EA, Zhang WY, Karnik SK, Borwege S, Anand VR, Laine PS, Su Y, Reaven PD. Nutrient modification of the innate immune response: a novel mechanism by which saturated fatty acids greatly amplify monocyte inflammation. Arterioscler Thromb Vasc Biol 30: 802-808, 2010.
48. Seager Danciger J, Lutz M, Hama S, Cruz D, Castrillo A, Lazaro J, Phillips R, Premack B, Berliner J. Method for large scale isolation, culture and cryopreservation of human monocytes suitable for chemotaxis, cellular adhesion assays, macrophage and dendritic cell differentiation. J Immunol Methods 288: 123-134, 2004.
49. Seong GJ, Hong S, Jung SA, Lee JJ, Lim E, Kim SJ, Lee JH. TGF-beta-induced interleukin-6 participates in transdifferentiation of human Tenon's fibroblasts to myofibroblasts. Mol Vis 15: 2123-2128, 2009.
50. Shoelson SE, Lee J, Goldfine AB. Inflammation and insulin resistance. J Clin Invest 116: 1793-1801, 2006.
51. Spector AA. Fatty acid binding to plasma albumin. J Lipid Res 16: 165-179, 1975.
52. Stahlman M, Pham HT, Adiels M, Mitchell TW, Blanksby SJ, Fagerberg B, Ekroos K, Boren J. Clinical dyslipidaemia is associated with changes in the lipid composition and inflammatory properties of apolipoprotein-B-containing lipoproteins from women with type 2 diabetes. Diabetologia 55: 1156-1166, 2012.
53. Van Veldhoven PP, Bell RM. Effect of harvesting methods, growth conditions and growth phase on diacylglycerol levels in cultured human adherent cells. Biochim Biophys Acta 959: 185-196, 1988.
54. Zeidan YH, Hannun YA. The acid sphingomyelinase/ceramide pathway: biomedical significance and mechanisms of regulation. Curr Mol Med 10: 454-466, 2010.