Targeted Induction of Ceramide Degradation Leads to Improved Systemic Metabolism and Reduced Hepatic Steatosis

Cell Metabolism

Volumn 22, Issue 2, 2015, Pages 266-278

  Xia, Jonathan Y ^a   Holland, William L ^a   Kusminski, Christine M ^a   Sun, Kai ^a   Sharma, Ankit X ^a   Pearson, Mackenzie J ^a   Sifuentes, Angelica J ^a   McDonald, Jeffrey G ^a   Gordillo, Ruth ^a   Scherer, Philipp E ^a,b  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACID CERAMIDASE; CERAMIDE; GLUCOSE; INSULIN; PROTEIN KINASE C ZETA; SPHINGOLIPID; TRIACYLGLYCEROL; ASAH1 PROTEIN, MOUSE; PRKCE PROTEIN, MOUSE; PROTEIN KINASE C EPSILON;

ADIPOCYTE; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEGRADATION; ENZYME ACTIVATION; ENZYME INDUCTION; FATTY LIVER; GLUCOSE HOMEOSTASIS; GLUCOSE METABOLISM; HORMONE ACTION; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID DEGRADATION; LIPID DIET; LIPID TRANSPORT; LIPOTOXICITY; MALE; METABOLIC REGULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; WHITE ADIPOSE TISSUE; ADIPOSE TISSUE; ANIMAL; BIOSYNTHESIS; GENETICS; LIVER; METABOLISM; PATHOLOGY; TRANSGENIC MOUSE;

MUS MUSCULUS;

ACID CERAMIDASE; ADIPOSE TISSUE; ANIMALS; CERAMIDES; ENZYME INDUCTION; FATTY LIVER; LIVER; MICE; MICE, TRANSGENIC; PROTEIN KINASE C-EPSILON;

EID: 84938569966     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2015.06.007     Document Type: Article

References (40)

1. C. Bedia, L. Camacho, J.L. Abad, G. Fabriàs, and T. Levade A simple fluorogenic method for determination of acid ceramidase activity and diagnosis of Farber disease J. Lipid Res. 51 2010 3542 3547
2. A.L. Birkenfeld, and G.I. Shulman Nonalcoholic fatty liver disease, hepatic insulin resistance, and type 2 diabetes Hepatology 59 2014 713 723
3. L.T. Boni, and R.R. Rando The nature of protein kinase C activation by physically defined phospholipid vesicles and diacylglycerols J. Biol. Chem. 260 1985 10819 10825
4. J. Boon, A.J. Hoy, R. Stark, R.D. Brown, R.C. Meex, D.C. Henstridge, S. Schenk, P.J. Meikle, J.F. Horowitz, B.A. Kingwell, and et al. Ceramides contained in LDL are elevated in type 2 diabetes and promote inflammation and skeletal muscle insulin resistance Diabetes 62 2013 401 410
5. J.M. Brown, J.L. Betters, C. Lord, Y. Ma, X. Han, K. Yang, H.M. Alger, J. Melchior, J. Sawyer, R. Shah, and et al. CGI-58 knockdown in mice causes hepatic steatosis but prevents diet-induced obesity and glucose intolerance J. Lipid Res. 51 2010 3306 3315
6. J.A. Chavez, T.A. Knotts, L.P. Wang, G. Li, R.T. Dobrowsky, G.L. Florant, and S.A. Summers A role for ceramide, but not diacylglycerol, in the antagonism of insulin signal transduction by saturated fatty acids J. Biol. Chem. 278 2003 10297 10303
7. M.M. Chou, W. Hou, J. Johnson, L.K. Graham, M.H. Lee, C.S. Chen, A.C. Newton, B.S. Schaffhausen, and A. Toker Regulation of protein kinase C zeta by PI 3-kinase and PDK-1 Curr. Biol. 8 1998 1069 1077
8. R.V. Farese Jr., R. Zechner, C.B. Newgard, and T.C. Walther The problem of establishing relationships between hepatic steatosis and hepatic insulin resistance Cell Metab. 15 2012 570 573
9. T.E. Fox, K.L. Houck, S.M. O'Neill, M. Nagarajan, T.C. Stover, P.T. Pomianowski, O. Unal, J.K. Yun, S.J. Naides, and M. Kester Ceramide recruits and activates protein kinase C zeta (PKC zeta) within structured membrane microdomains J. Biol. Chem. 282 2007 12450 12457
10. J.M. Haus, S.R. Kashyap, T. Kasumov, R. Zhang, K.R. Kelly, R.A. Defronzo, and J.P. Kirwan Plasma ceramides are elevated in obese subjects with type 2 diabetes and correlate with the severity of insulin resistance Diabetes 58 2009 337 343
11. W.L. Holland, J.T. Brozinick, L.P. Wang, E.D. Hawkins, K.M. Sargent, Y. Liu, K. Narra, K.L. Hoehn, T.A. Knotts, A. Siesky, and et al. Inhibition of ceramide synthesis ameliorates glucocorticoid-, saturated-fat-, and obesity-induced insulin resistance Cell Metab. 5 2007 167 179
12. W.L. Holland, R.A. Miller, Z.V. Wang, K. Sun, B.M. Barth, H.H. Bui, K.E. Davis, B.T. Bikman, N. Halberg, J.M. Rutkowski, and et al. Receptor-mediated activation of ceramidase activity initiates the pleiotropic actions of adiponectin Nat. Med. 17 2011 55 63
13. A.J. Hoy, C.R. Bruce, S.M. Turpin, A.J. Morris, M.A. Febbraio, and M.J. Watt Adipose triglyceride lipase-null mice are resistant to high-fat diet-induced insulin resistance despite reduced energy expenditure and ectopic lipid accumulation Endocrinology 152 2011 48 58
14. I. Ichi, K. Nakahara, K. Fujii, C. Iida, Y. Miyashita, and S. Kojo Increase of ceramide in the liver and plasma after carbon tetrachloride intoxication in the rat J. Nutr. Sci. Vitaminol. (Tokyo) 53 2007 53 56
15. X. Lopez, A.B. Goldfine, W.L. Holland, R. Gordillo, and P.E. Scherer Plasma ceramides are elevated in female children and adolescents with type 2 diabetes J. Pediatr. Endocrinol. Metab. 26 2013 995 998
16. J.J. Luiken, D.M. Ouwens, D.D. Habets, G.C. van der Zon, W.A. Coumans, R.W. Schwenk, A. Bonen, and J.F. Glatz Permissive action of protein kinase C-zeta in insulin-induced CD36- and GLUT4 translocation in cardiac myocytes J. Endocrinol. 201 2009 199 209
17. K. Minehira, S.G. Young, C.J. Villanueva, L. Yetukuri, M. Oresic, M.K. Hellerstein, R.V. Farese Jr., J.D. Horton, F. Preitner, B. Thorens, and L. Tappy Blocking VLDL secretion causes hepatic steatosis but does not affect peripheral lipid stores or insulin sensitivity in mice J. Lipid Res. 49 2008 2038 2044
18. M. Monetti, M.C. Levin, M.J. Watt, M.P. Sajan, S. Marmor, B.K. Hubbard, R.D. Stevens, J.R. Bain, C.B. Newgard, R.V. Farese Sr., and et al. Dissociation of hepatic steatosis and insulin resistance in mice overexpressing DGAT in the liver Cell Metab. 6 2007 69 78
19. J. Monsénégo, A. Mansouri, M. Akkaoui, V. Lenoir, C. Esnous, V. Fauveau, V. Tavernier, J. Girard, and C. Prip-Buus Enhancing liver mitochondrial fatty acid oxidation capacity in obese mice improves insulin sensitivity independently of hepatic steatosis J. Hepatol. 56 2012 632 639
20. G. Müller, M. Ayoub, P. Storz, J. Rennecke, D. Fabbro, and K. Pfizenmaier PKC zeta is a molecular switch in signal transduction of TNF-alpha, bifunctionally regulated by ceramide and arachidonic acid EMBO J. 14 1995 1961 1969
21. D.J. Powell, E. Hajduch, G. Kular, and H.S. Hundal Ceramide disables 3-phosphoinositide binding to the pleckstrin homology domain of protein kinase B (PKB)/Akt by a PKCzeta-dependent mechanism Mol. Cell. Biol. 23 2003 7794 7808
22. S. Raichur, S.T. Wang, P.W. Chan, Y. Li, J. Ching, B. Chaurasia, S. Dogra, M.K. Öhman, K. Takeda, S. Sugii, and et al. CerS2 haploinsufficiency inhibits β-oxidation and confers susceptibility to diet-induced steatohepatitis and insulin resistance Cell Metab. 20 2014 687 695
23. M.P. Sajan, M.L. Standaert, A. Miura, C.R. Kahn, and R.V. Farese Tissue-specific differences in activation of atypical protein kinase C and protein kinase B in muscle, liver, and adipocytes of insulin receptor substrate-1 knockout mice Mol. Endocrinol. 18 2004 2513 2521
24. M.P. Sajan, M.L. Standaert, J. Rivas, A. Miura, Y. Kanoh, J. Soto, C.M. Taniguchi, C.R. Kahn, and R.V. Farese Role of atypical protein kinase C in activation of sterol regulatory element binding protein-1c and nuclear factor kappa B (NFkappaB) in liver of rodents used as a model of diabetes, and relationships to hyperlipidaemia and insulin resistance Diabetologia 52 2009 1197 1207
25. M.P. Sajan, M.E. Acevedo-Duncan, M.L. Standaert, R.A. Ivey, M. Lee, and R.V. Farese Akt-dependent phosphorylation of hepatic FoxO1 is compartmentalized on a WD40/ProF scaffold and is selectively inhibited by aPKC in early phases of diet-induced obesity Diabetes 63 2014 2690 2701
26. M.P. Sajan, R.A. Ivey, M.C. Lee, and R.V. Farese Hepatic insulin resistance in ob/ob mice involves increases in ceramide, aPKC activity, and selective impairment of Akt-dependent FoxO1 phosphorylation J. Lipid Res. 56 2015 70 80
27. E.H. Schuchman, and I. Galanin Development of enzyme replacement therapy for Farber disease and other disorders with ceramide storage Mol. Genet. Metab. 111 2014 S94
28. I. Shimomura, Y. Bashmakov, and J.D. Horton Increased levels of nuclear SREBP-1c associated with fatty livers in two mouse models of diabetes mellitus J. Biol. Chem. 274 1999 30028 30032
29. I. Shimomura, Y. Bashmakov, S. Ikemoto, J.D. Horton, M.S. Brown, and J.L. Goldstein Insulin selectively increases SREBP-1c mRNA in the livers of rats with streptozotocin-induced diabetes Proc. Natl. Acad. Sci. USA 96 1999 13656 13661
30. G.I. Shulman Ectopic fat in insulin resistance, dyslipidemia, and cardiometabolic disease N. Engl. J. Med. 371 2014 1131 1141
31. J.W. Soh, and I.B. Weinstein Roles of specific isoforms of protein kinase C in the transcriptional control of cyclin D1 and related genes J. Biol. Chem. 278 2003 34709 34716
32. C.M. Taniguchi, K. Ueki, and R. Kahn Complementary roles of IRS-1 and IRS-2 in the hepatic regulation of metabolism J. Clin. Invest. 115 2005 718 727
33. C.M. Taniguchi, T. Kondo, M. Sajan, J. Luo, R. Bronson, T. Asano, R. Farese, L.C. Cantley, and C.R. Kahn Divergent regulation of hepatic glucose and lipid metabolism by phosphoinositide 3-kinase via Akt and PKClambda/zeta Cell Metab. 3 2006 343 353
34. A.T. Turer, J.D. Browning, C.R. Ayers, S.R. Das, A. Khera, G.L. Vega, S.M. Grundy, and P.E. Scherer Adiponectin as an independent predictor of the presence and degree of hepatic steatosis in the Dallas Heart Study J. Clin. Endocrinol. Metab. 97 2012 E982 E986
35. S.M. Turpin, H.T. Nicholls, D.M. Willmes, A. Mourier, S. Brodesser, C.M. Wunderlich, J. Mauer, E. Xu, P. Hammerschmidt, H.S. Brönneke, and et al. Obesity-induced CerS6-dependent C16:0 ceramide production promotes weight gain and glucose intolerance Cell Metab. 20 2014 678 686
36. P.J. Voshol, G. Haemmerle, D.M. Ouwens, R. Zimmermann, R. Zechner, B. Teusink, J.A. Maassen, L.M. Havekes, and J.A. Romijn Increased hepatic insulin sensitivity together with decreased hepatic triglyceride stores in hormone-sensitive lipase-deficient mice Endocrinology 144 2003 3456 3462
37. J.Y. Xia, T.S. Morley, and P.E. Scherer The adipokine/ceramide axis: key aspects of insulin sensitization Biochimie 96 2014 130 139
38. R. Ye, W.L. Holland, R. Gordillo, M. Wang, Q.A. Wang, M. Shao, T.S. Morley, R.K. Gupta, A. Stahl, and P.E. Scherer Adiponectin is essential for lipid homeostasis and survival under insulin deficiency and promotes β-cell regeneration eLife 3 2014 3
39. L. Yetukuri, M. Katajamaa, G. Medina-Gomez, T. Seppänen-Laakso, A. Vidal-Puig, and M. Oresic Bioinformatics strategies for lipidomics analysis: characterization of obesity related hepatic steatosis BMC Syst. Biol. 1 2007 12
40. X.X. Yu, S.F. Murray, S.K. Pandey, S.L. Booten, D. Bao, X.Z. Song, S. Kelly, S. Chen, R. McKay, B.P. Monia, and S. Bhanot Antisense oligonucleotide reduction of DGAT2 expression improves hepatic steatosis and hyperlipidemia in obese mice Hepatology 42 2005 362 371