Selective inhibition of sphingosine kinase-1 protects adipose tissue against LPS-induced inflammatory response in zucker diabetic fatty rats

American Journal of Physiology - Endocrinology and Metabolism

Volumn 307, Issue 5, 2014, Pages E437-E446

  Tous, Monica ^a   Ferrer Lorente, Raquel ^a   Badimon, Lina ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

Adipose tissue; Chemokine (C C motif) ligand 5; Inflammation; Lipopolysaccharide; Sphingosine kinase 1; Zucker diabetic fatty rats

Indexed keywords

ADIPONECTIN; CREATININE; INSULIN; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; PENTRAXIN 3; RANTES; SMALL INTERFERING RNA; SPHINGOSINE KINASE 1; ENZYME INHIBITOR; PHOSPHOTRANSFERASE; SPHINGOSINE KINASE;

3T3 CELL LINE; ADIPOCYTE; ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME LINKED IMMUNOSORBENT ASSAY; INFLAMMATION; INSULIN RESISTANCE; METABOLIC DISORDER; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PROTEIN FUNCTION; RAT; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; ZUCKER DIABETIC FATTY RAT; ANIMAL; CELL CULTURE; CELL PROTECTION; CHEMOKINE (C-C MOTIF) LIGAND 5; DRUG ANTAGONISM; DRUG EFFECT; ENZYME SPECIFICITY; EXPERIMENTAL DIABETES MELLITUS; GENETICS; MALE; METABOLISM; MOUSE; PATHOLOGY; SPHINGOSINE KINASE-1; ZUCKER DIABETIC FATTY RATS; ZUCKER RAT;

ADIPOSE TISSUE; CHEMOKINE (C-C MOTIF) LIGAND 5; INFLAMMATION; LIPOPOLYSACCHARIDE; SPHINGOSINE KINASE-1; ZUCKER DIABETIC FATTY RATS;

3T3-L1 CELLS; ADIPOSE TISSUE; ANIMALS; CELLS, CULTURED; CYTOPROTECTION; DIABETES MELLITUS, EXPERIMENTAL; ENZYME INHIBITORS; INFLAMMATION; LIPOPOLYSACCHARIDES; MALE; MICE; OBESITY; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); RATS; RATS, ZUCKER; RNA, SMALL INTERFERING; SUBSTRATE SPECIFICITY;

EID: 84907729854     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00059.2014     Document Type: Article

References (36)

1. Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, Delzenne NM, Burcelin R. Changes in gut microbiota control metabolic endotoxemiainduced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 57: 1470-1481, 2008.
2. Clark JB, Palmer CJ, Shaw WN. The diabetic Zucker fatty rat. Proc Soc Exp Biol Med 173: 68-75, 1983.
3. Creely SJ, McTernan PG, Kusminski CM, Fisher FM, Khanolkar M, Evans M, Harte AL, Kumar S. Lipopolysaccharide activates an innate immune system response in human adipose tissue in obesity and type 2 diabetes. Am J Physiol Endocrinol Metab 292: E740-E747, 2007.
4. Don AS, Martinez-Lamenca C, Webb WR, Proia RL, Roberts E, Rosen H. Essential requirement for sphingosine kinase 2 in a sphingolipid apoptosis pathway activated by FTY720 analogues. J Biol Chem 282: 15833-15842, 2007.
5. Harford KA, Reynolds CM, McGillicuddy FC, Roche HM. Fats, inflammation and insulin resistance: insights to the role of macrophage and T-cell accumulation in adipose tissue. Proc Nutr Soc 70: 408-417, 2011.
6. Hashimoto T, Igarashi J, Kosaka H. Sphingosine kinase is induced in mouse 3T3-L1 cells and promotes adipogenesis. J Lipid Res 50: 602-610, 2009.
7. Henrichot E, Juge-Aubry CE, Pernin A, Pache JC, Velebit V, Dayer JM, Meda P, Chizzolini C, Meier CA. Production of chemokines by perivascular adipose tissue: a role in the pathogenesis of atherosclerosis? Arterioscler Thromb Vasc Biol 25: 2594-2599, 2005.
8. Herder C, Haastert B, Müller-Scholze S, Koenig W, Thorand B, Holle R, Wichmann HE, Scherbaum WA, Martin S, Kolb H. Association of systemic chemokine concentrations with impaired glucose tolerance and type 2 diabetes: results from the Cooperative Health Research in the Region of Augsburg Survey S4 (KORA S4). Diabetes 54, Suppl 2: S11-S17, 2005.
9. Hotamisligil GS. Inflammation and metabolic disorders. Nature 444: 860-867, 2006.
10. Huber J, Kiefer FW, Zeyda M, Ludvik B, Silberhumer GR, Prager G, Zlabinger GJ, Stulnig TM. CC chemokine and CC chemokine receptor profiles in visceral and subcutaneous adipose tissue are altered in human obesity. J Clin Endocrinol Metab 93: 3215-3221, 2008.
11. Ibrahim FB, Pang SJ, Melendez AJ. Anaphylatoxin signaling in human neutrophils. A key role for sphingosine kinase. J Biol Chem 279: 44802-44811, 2004.
12. Karastergiou K, Evans I, Ogston N, Miheisi N, Nair D, Kaski JC, Jahangiri M, Mohamed-Ali V. Epicardial adipokines in obesity and coronary artery disease induce atherogenic changes in monocytes and endothelial cells. Arterioscler Thromb Vasc Biol 30: 1340-1346, 2010.
13. Kasper B, Winoto-Morbach S, Mittelstädt J, Brandt E, Schütze S, Petersen F. CXCL4-induced monocyte survival, cytokine expression, and oxygen radical formation is regulated by sphingosine kinase 1. Eur J Immunol 40: 1162-1173, 2010.
14. Keophiphath M, Rouault C, Divoux A, Clément K, Lacasa D. CCL5 promotes macrophage recruitment and survival in human adipose tissue. Arterioscler Thromb Vasc Biol 30: 39-45, 2010.
15. Kintscher U, Hartge M, Hess K, Foryst-Ludwig A, Clemenz M, Wabitsch M, Fischer-Posovszky P, Barth TF, Dragun D, Skurk T, Hauner H, Blüher M, Unger T, Wolf AM, Knippschild U, Hombach V, Marx N. T-lymphocyte infiltration in visceral adipose tissue: a primary event in adipose tissue inflammation and the development of obesity-mediated insulin resistance. Arterioscler Thromb Vasc Biol 28: 1304-1310, 2008.
16. Kitade H, Sawamoto K, Nagashimada M, Inoue H, Yamamoto Y, Sai Y, Takamura T, Yamamoto H, Miyamoto K, Ginsberg HN, Mukaida N, Kaneko S, Ota T. CCR5 plays a critical role in obesity-induced adipose tissue inflammation and insulin resistance by regulating both macrophage recruitment and M1/M2 status. Diabetes 61: 1680-1690, 2012.
17. Kohama T, Olivera A, Edsall L, Nagiec MM, Dickson R, Spiegel S. Molecular cloning and functional characterization of murine sphingosine kinase. J Biol Chem 273: 23722-23728, 1998.
18. Le Stunff H, Milstien S, Spiegel S. Generation and metabolism of bioactive sphingosine-1-phosphate. J Cell Biochem 92: 882-899, 2004.
19. Liu H, Sugiura M, Nava VE, Edsall LC, Kono K, Poulton S, Milstien S, Kohama T, Spiegel S. Molecular cloning and functional characterization of a novel mammalian sphingosine kinase type 2 isoform. J Biol Chem 275: 19513-19520, 2000.
20. Maceyka M, Sankala H, Hait NC, Le Stunff H, Liu H, Toman R, Collier C, Zhang M, Satin LS, Merrill AH Jr, Milstien S, Spiegel S. SphK1 and SphK2, sphingosine kinase isoenzymes with opposing functions in sphingolipid metabolism. J Biol Chem 280: 37118-37129, 2005.
21. Nishimura S, Manabe I, Nagasaki M, Eto K, Yamashita H, Ohsugi M, Otsu M, Hara K, Ueki K, Sugiura S, Yoshimura K, Kadowaki T, Nagai R. CD8 effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat Med 15: 914-920, 2009.
22. Nomura S, Shouzu A, Omoto S, Nishikawa M, Fukuhara S. Significance of chemokines and activated platelets in patients with diabetes. Clin Exp Immunol 121: 437-443, 2000.
23. Poulain-Godefroy O, Froguel P. Preadipocyte response and impairment of differentiation in an inflammatory environment. Biochem Biophys Res Commun 356: 662-667, 2007.
24. Puneet P, Yap CT, Wong L, Lam Y, Koh DR, Moochhala S, Pfeilschifter J, Huwiler A, Melendez AJ. SphK1 regulates proinflammatory responses associated with endotoxin and polymicrobial sepsis. Science 328: 1290-1294, 2010.
25. Rausch ME, Weisberg S, Vardhana P, Tortoriello DV. Obesity in C57BL/6J mice is characterized by adipose tissue hypoxia and cytotoxic T-cell infiltration. Int J Obes (Lond) 32: 451-463, 2008.
26. Rocha VZ, Folco EJ, Sukhova G, Shimizu K, Gotsman I, Vernon AH, Libby P. Interferon-gamma, a Th1 cytokine, regulates fat inflammation: a role for adaptive immunity in obesity. Circ Res 103: 467-476, 2008.
27. Ross JS, Hu W, Rosen B, Snider AJ, Obeid LM, Cowart LA. Sphingosine kinase 1 is regulated by peroxisome proliferator-activated receptor in response to free fatty acids and is essential for skeletal muscle interleukin-6 production and signaling in diet-induced obesity. J Biol Chem 288: 22193-22206, 2013.
28. Strissel KJ, DeFuria J, Shaul ME, Bennett G, Greenberg AS, Obin MS. T-cell recruitment and Th1 polarization in adipose tissue during diet-induced obesity in C57BL/6 mice. Obesity (Silver Spring) 18: 1918-1925, 2010.
29. Suganami T, Ogawa Y. Adipose tissue macrophages: their role in adipose tissue remodeling. J Leukoc Biol 88: 33-39, 2010.
30. Thomas AP, Dunn TN, Oort PJ, Grino M, Adams SH. Inflammatory phenotyping identifies CD11d as a gene markedly induced in white adipose tissue in obese rodents and women. J Nutr 141: 1172-1180, 2011.
31. Wang J, Badeanlou L, Bielawski J, Ciaraldi TP, Samad F. Sphingosine kinase 1 regulates adipose proinflammatory responses and insulin resistance. Am J Physiol Endocrinol Metab 306: E756-E768, 2014.
32. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW, Jr. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112: 1796-1808, 2003.
33. Wu H, Ghosh S, Perrard XD, Feng L, Garcia GE, Perrard JL, Sweeney JF, Peterson LE, Chan L, Smith CW, Ballantyne CM. T-cell accumulation and regulated on activation, normal T cell expressed and secreted upregulation in adipose tissue in obesity. Circulation 115: 1029-1038, 2007.
34. Xu H, Barnes GT, Yang Q, Tan G, Yang D, Chou CJ, Sole J, Nichols A, Ross JS, Tartaglia LA, Chen H. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 112: 1821-1830, 2003.
35. Zhang H, Potter BJ, Cao JM, Zhang C. Interferon-gamma induced adipose tissue inflammation is linked to endothelial dysfunction in type 2 diabetic mice. Basic Res Cardiol 106: 1135-1145, 2011.
36. Zhi L, Leung BP, Melendez AJ. Sphingosine kinase 1 regulates proinflammatory responses triggered by TNFalpha in primary human monocytes. J Cell Physiol 208: 109-115, 2006.