Lipid metabolism and signaling in cardiac lipotoxicity

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1861, Issue 10, 2016, Pages 1513-1524

  D'Souza, Kenneth ^a   Nzirorera, Carine ^a   Kienesberger, Petra C ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Cardiomyopathy; Diabetes; Heart; Lipids; Lipotoxicity; Obesity

Indexed keywords

ACYL COENZYME A; ACYLCARNITINE; ADENOSINE TRIPHOSPHATE; CERAMIDE; DIACYLGLYCEROL; FAT DROPLET; PHOSPHOLIPID; SPHINGOLIPID; TRIACYLGLYCEROL; LIPID;

AGING; CARDIAC MUSCLE CELL; CARDIOMYOPATHY; DIABETES MELLITUS; FATTY ACID OXIDATION; LIPID METABOLISM; LIPID TRANSPORT; LIPOGENESIS; LIPOTOXICITY; NONHUMAN; OBESITY; PHOSPHOLIPID METABOLISM; PRIORITY JOURNAL; REPERFUSION INJURY; REVIEW; SIGNAL TRANSDUCTION; SPHINGOLIPID METABOLISM; ANIMAL; BIOLOGICAL MODEL; CARDIAC MUSCLE; DRUG EFFECTS; HUMAN; METABOLISM; MITOCHONDRION;

ANIMALS; HUMANS; LIPID METABOLISM; LIPIDS; MITOCHONDRIA; MODELS, BIOLOGICAL; MYOCARDIUM; SIGNAL TRANSDUCTION;

EID: 84959454587     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2016.02.016     Document Type: Review

References (173)

1. [1] Unger, R.H., Orci, L., Lipoapoptosis: its mechanism and its diseases. Biochim. Biophys. Acta 1585 (2002), 202–212.
2. [2] Chiu, H.C., Kovacs, A., Ford, D.A., Hsu, F.F., Garcia, R., Herrero, P., Saffitz, J.E., Schaffer, J.E., A novel mouse model of lipotoxic cardiomyopathy. J. Clin. Invest. 107 (2001), 813–822.
3. [3] Goldberg, I.J., Trent, C.M., Schulze, P.C., Lipid metabolism and toxicity in the heart. Cell Metab. 15 (2012), 805–812.
4. [4] Birse, R.T., Bodmer, R., Lipotoxicity and cardiac dysfunction in mammals and Drosophila. Crit. Rev. Biochem. Mol. Biol. 46 (2011), 376–385.
5. [5] Brindley, D.N., Kok, B.P., Kienesberger, P.C., Lehner, R., Dyck, J.R., Shedding light on the enigma of myocardial lipotoxicity: the involvement of known and putative regulators of fatty acid storage and mobilization. Am. J. Physiol. Endocrinol. Metab. 298 (2010), E897–E908.
6. [6] Wende, A.R., Abel, E.D., Lipotoxicity in the heart. Biochim. Biophys. Acta 1801 (2010), 311–319.
7. [7] Perman, J.C., Bostrom, P., Lindbom, M., Lidberg, U., StAhlman, M., Hagg, D., Lindskog, H., Scharin Tang, M., Omerovic, E., Mattsson Hulten, L., Jeppsson, A., Petursson, P., Herlitz, J., Olivecrona, G., Strickland, D.K., Ekroos, K., Olofsson, S.O., Boren, J., The VLDL receptor promotes lipotoxicity and increases mortality in mice following an acute myocardial infarction. J. Clin. Invest. 121 (2011), 2625–2640.
8. [8] Koonen, D.P., Febbraio, M., Bonnet, S., Nagendran, J., Young, M.E., Michelakis, E.D., Dyck, J.R., CD36 expression contributes to age-induced cardiomyopathy in mice. Circulation 116 (2007), 2139–2147.
9. [9] Dewald, O., Sharma, S., Adrogue, J., Salazar, R., Duerr, G.D., Crapo, J.D., Entman, M.L., Taegtmeyer, H., Downregulation of peroxisome proliferator-activated receptor-alpha gene expression in a mouse model of ischemic cardiomyopathy is dependent on reactive oxygen species and prevents lipotoxicity. Circulation 112 (2005), 407–415.
10. [10] Girousse, A., Tavernier, G., Valle, C., Moro, C., Mejhert, N., Dinel, A.L., Houssier, M., Roussel, B., Besse-Patin, A., Combes, M., Mir, L., Monbrun, L., Bezaire, V., Prunet-Marcassus, B., Waget, A., Vila, I., Caspar-Bauguil, S., Louche, K., Marques, M.A., Mairal, A., Renoud, M.L., Galitzky, J., Holm, C., Mouisel, E., Thalamas, C., Viguerie, N., Sulpice, T., Burcelin, R., Arner, P., Langin, D., Partial inhibition of adipose tissue lipolysis improves glucose metabolism and insulin sensitivity without alteration of fat mass. PLoS Biol., 11, 2013, e1001485.
11. [11] Gray, S., Kim, J.K., New insights into insulin resistance in the diabetic heart. Trends Endocrinol. Metab. 22 (2011), 394–403.
12. [12] Borradaile, N.M., Schaffer, J.E., Lipotoxicity in the heart. Curr. Hypertens. Rep. 7 (2005), 412–417.
13. [13] Abel, E.D., O'Shea, K.M., Ramasamy, R., Insulin resistance: metabolic mechanisms and consequences in the heart. Arterioscler. Thromb. Vasc. Biol. 32 (2012), 2068–2076.
14. [14] Kienesberger, P.C., Pulinilkunnil, T., Nagendran, J., Dyck, J.R., Myocardial triacylglycerol metabolism. J. Mol. Cell. Cardiol. 55 (2013), 101–110.
15. [15] Heather, L.C., Pates, K.M., Atherton, H.J., Cole, M.A., Ball, D.R., Evans, R.D., Glatz, J.F., Luiken, J.J., Griffin, J.L., Clarke, K., Differential translocation of the fatty acid transporter, FAT/CD36, and the glucose transporter, GLUT4, coordinates changes in cardiac substrate metabolism during ischemia and reperfusion. Circ. Heart Fail. 6 (2013), 1058–1066.
16. [16] Nagendran, J., Pulinilkunnil, T., Kienesberger, P.C., Sung, M.M., Fung, D., Febbraio, M., Dyck, J.R., Cardiomyocyte-specific ablation of CD36 improves post-ischemic functional recovery. J. Mol. Cell. Cardiol. 63C (2013), 180–188.
17. [17] Augustus, A.S., Buchanan, J., Park, T.S., Hirata, K., Noh, H.L., Sun, J., Homma, S., D'Armiento, J., Abel, E.D., Goldberg, I.J., Loss of lipoprotein lipase-derived fatty acids leads to increased cardiac glucose metabolism and heart dysfunction. J. Biol. Chem. 281 (2006), 8716–8723.
18. [18] Lopaschuk, G.D., Ussher, J.R., Folmes, C.D., Jaswal, J.S., Stanley, W.C., Myocardial fatty acid metabolism in health and disease. Physiol. Rev. 90 (2010), 207–258.
19. [19] Kolwicz, S.C. Jr., Purohit, S., Tian, R., Cardiac metabolism and its interactions with contraction, growth, and survival of cardiomyocytes. Circ. Res. 113 (2013), 603–616.
20. [20] Iozzo, P., Metabolic toxicity of the heart: insights from molecular imaging. Nutr. Metab. Cardiovasc. Dis. 20 (2010), 147–156.
21. [21] Taegtmeyer, H., Golfman, L., Sharma, S., Razeghi, P., van Arsdall, M., Linking gene expression to function: metabolic flexibility in the normal and diseased heart. Ann. N. Y. Acad. Sci. 1015 (2004), 202–213.
22. [22] Birse, R.T., Choi, J., Reardon, K., Rodriguez, J., Graham, S., Diop, S., Ocorr, K., Bodmer, R., Oldham, S., High-fat-diet-induced obesity and heart dysfunction are regulated by the TOR pathway in Drosophila. Cell Metab. 12 (2010), 533–544.
23. [23] Drosatos, K., Schulze, P.C., Cardiac lipotoxicity: molecular pathways and therapeutic implications. Curr. Heart Fail. Rep. 10 (2013), 109–121.
24. [24] Szczepaniak, L.S., Dobbins, R.L., Metzger, G.J., Sartoni-D'Ambrosia, G., Arbique, D., Vongpatanasin, W., Unger, R., Victor, R.G., Myocardial triglycerides and systolic function in humans: in vivo evaluation by localized proton spectroscopy and cardiac imaging. Magn. Reson. Med. 49 (2003), 417–423.
25. [25] Utz, W., Engeli, S., Haufe, S., Kast, P., Hermsdorf, M., Wiesner, S., Pofahl, M., Traber, J., Luft, F.C., Boschmann, M., Schulz-Menger, J., Jordan, J., Myocardial steatosis, cardiac remodelling and fitness in insulin-sensitive and insulin-resistant obese women. Heart 97 (2011), 1585–1589.
26. [26] Hammer, S., van der Meer, R.W., Lamb, H.J., Schar, M., de Roos, A., Smit, J.W., Romijn, J.A., Progressive caloric restriction induces dose-dependent changes in myocardial triglyceride content and diastolic function in healthy men. J. Clin. Endocrinol. Metab. 93 (2008), 497–503.
27. [27] Schrauwen-Hinderling, V.B., Hesselink, M.K., Meex, R., van der Made, S., Schar, M., Lamb, H., Wildberger, J.E., Glatz, J., Snoep, G., Kooi, M.E., Schrauwen, P., Improved ejection fraction after exercise training in obesity is accompanied by reduced cardiac lipid content. J. Clin. Endocrinol. Metab. 95 (2010), 1932–1938.
28. [28] McGavock, J.M., Lingvay, I., Zib, I., Tillery, T., Salas, N., Unger, R., Levine, B.D., Raskin, P., Victor, R.G., Szczepaniak, L.S., Cardiac steatosis in diabetes mellitus: a 1H-magnetic resonance spectroscopy study. Circulation 116 (2007), 1170–1175.
29. [29] McGavock, J.M., Victor, R.G., Unger, R.H., Szczepaniak, L.S., Adiposity of the heart, revisited. Ann. Intern. Med. 144 (2006), 517–524.
30. [30] Szczepaniak, L.S., Victor, R.G., Orci, L., Unger, R.H., Forgotten but not gone: the rediscovery of fatty heart, the most common unrecognized disease in America. Circ. Res. 101 (2007), 759–767.
31. [31] Labbe, S.M., Grenier-Larouche, T., Noll, C., Phoenix, S., Guerin, B., Turcotte, E.E., Carpentier, A.C., Increased myocardial uptake of dietary fatty acids linked to cardiac dysfunction in glucose-intolerant humans. Diabetes 61 (2012), 2701–2710.
32. [32] Chiu, H.C., Kovacs, A., Blanton, R.M., Han, X., Courtois, M., Weinheimer, C.J., Yamada, K.A., Brunet, S., Xu, H., Nerbonne, J.M., Welch, M.J., Fettig, N.M., Sharp, T.L., Sambandam, N., Olson, K.M., Ory, D.S., Schaffer, J.E., Transgenic expression of fatty acid transport protein 1 in the heart causes lipotoxic cardiomyopathy. Circ. Res. 96 (2005), 225–233.
33. [33] Finck, B.N., Lehman, J.J., Leone, T.C., Welch, M.J., Bennett, M.J., Kovacs, A., Han, X., Gross, R.W., Kozak, R., Lopaschuk, G.D., Kelly, D.P., The cardiac phenotype induced by PPARalpha overexpression mimics that caused by diabetes mellitus. J. Clin. Invest. 109 (2002), 121–130.
34. [34] Yagyu, H., Chen, G., Yokoyama, M., Hirata, K., Augustus, A., Kako, Y., Seo, T., Hu, Y., Lutz, E.P., Merkel, M., Bensadoun, A., Homma, S., Goldberg, I.J., Lipoprotein lipase (LpL) on the surface of cardiomyocytes increases lipid uptake and produces a cardiomyopathy. J. Clin. Invest. 111 (2003), 419–426.
35. [35] Luiken, J.J., Arumugam, Y., Dyck, D.J., Bell, R.C., Pelsers, M.M., Turcotte, L.P., Tandon, N.N., Glatz, J.F., Bonen, A., Increased rates of fatty acid uptake and plasmalemmal fatty acid transporters in obese Zucker rats. J. Biol. Chem. 276 (2001), 40567–40573.
36. [36] Coort, S.L., Luiken, J.J., van der Vusse, G.J., Bonen, A., Glatz, J.F., Increased FAT (fatty acid translocase)/CD36-mediated long-chain fatty acid uptake in cardiac myocytes from obese Zucker rats. Biochem. Soc. Trans. 32 (2004), 83–85.
37. [37] Coort, S.L., Hasselbaink, D.M., Koonen, D.P., Willems, J., Coumans, W.A., Chabowski, A., van der Vusse, G.J., Bonen, A., Glatz, J.F., Luiken, J.J., Enhanced sarcolemmal FAT/CD36 content and triacylglycerol storage in cardiac myocytes from obese Zucker rats. Diabetes 53 (2004), 1655–1663.
38. [38] Angin, Y., Steinbusch, L.K., Simons, P.J., Greulich, S., Hoebers, N.T., Douma, K., van Zandvoort, M.A., Coumans, W.A., Wijnen, W., Diamant, M., Ouwens, D.M., Glatz, J.F., Luiken, J.J., CD36 inhibition prevents lipid accumulation and contractile dysfunction in rat cardiomyocytes. Biochem. J. 448 (2012), 43–53.
39. [39] Yang, J., Sambandam, N., Han, X., Gross, R.W., Courtois, M., Kovacs, A., Febbraio, M., Finck, B.N., Kelly, D.P., CD36 deficiency rescues lipotoxic cardiomyopathy. Circ. Res. 100 (2007), 1208–1217.
40. [40] Finck, B.N., Han, X., Courtois, M., Aimond, F., Nerbonne, J.M., Kovacs, A., Gross, R.W., Kelly, D.P., A critical role for PPARalpha-mediated lipotoxicity in the pathogenesis of diabetic cardiomyopathy: modulation by dietary fat content. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 1226–1231.
41. [41] Glatz, J.F., Angin, Y., Steinbusch, L.K., Schwenk, R.W., Luiken, J.J., CD36 as a target to prevent cardiac lipotoxicity and insulin resistance. Prostaglandins Leukot. Essent. Fat. Acids 88 (2013), 71–77.
42. [42] Duncan, J.G., Bharadwaj, K.G., Fong, J.L., Mitra, R., Sambandam, N., Courtois, M.R., Lavine, K.J., Goldberg, I.J., Kelly, D.P., Rescue of cardiomyopathy in peroxisome proliferator-activated receptor-alpha transgenic mice by deletion of lipoprotein lipase identifies sources of cardiac lipids and peroxisome proliferator-activated receptor-alpha activators. Circulation 121 (2010), 426–435.
43. [43] Banke, N.H., Wende, A.R., Leone, T.C., O'Donnell, J.M., Abel, E.D., Kelly, D.P., Lewandowski, E.D., Preferential oxidation of triacylglyceride-derived fatty acids in heart is augmented by the nuclear receptor PPARalpha. Circ. Res. 107 (2010), 233–241.
44. [44] Listenberger, L.L., Han, X., Lewis, S.E., Cases, S., Farese, R.V. Jr., Ory, D.S., Schaffer, J.E., Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 3077–3082.
45. [45] Bosma, M., Dapito, D.H., Drosatos-Tampakaki, Z., Huiping-Son, N., Huang, L.S., Kersten, S., Drosatos, K., Goldberg, I.J., Sequestration of fatty acids in triglycerides prevents endoplasmic reticulum stress in an in vitro model of cardiomyocyte lipotoxicity. Biochim. Biophys. Acta 1841 (2014), 1648–1655.
46. [46] Liu, L., Shi, X., Bharadwaj, K.G., Ikeda, S., Yamashita, H., Yagyu, H., Schaffer, J.E., Yu, Y.H., Goldberg, I.J., DGAT1 expression increases heart triglyceride content but ameliorates lipotoxicity. J. Biol. Chem. 284 (2009), 36312–36323.
47. [47] Liu, L., Yu, S., Khan, R.S., Homma, S., Schulze, P.C., Blaner, W.S., Yin, Y., Goldberg, I.J., Diacylglycerol acyl transferase 1 overexpression detoxifies cardiac lipids in PPARgamma transgenic mice. J. Lipid Res. 53 (2012), 1482–1492.
48. [48] Glenn, D.J., Wang, F., Nishimoto, M., Cruz, M.C., Uchida, Y., Holleran, W.M., Zhang, Y., Yeghiazarians, Y., Gardner, D.G., A murine model of isolated cardiac steatosis leads to cardiomyopathy. Hypertension 57 (2011), 216–222.
49. [49] Liu, L., Trent, C.M., Fang, X., Son, N.H., Jiang, H., Blaner, W.S., Hu, Y., Yin, Y.X., Farese, R.V. Jr., Homma, S., Turnbull, A.V., Eriksson, J.W., Hu, S.L., Ginsberg, H.N., Huang, L.S., Goldberg, I.J., Cardiomyocyte-specific loss of diacylglycerol acyltransferase 1 (DGAT1) reproduces the abnormalities in lipids found in severe heart failure. J. Biol. Chem. 289 (2014), 29881–29891.
50. [50] Liu, L., Yu, S., Khan, R.S., Ables, G.P., Bharadwaj, K.G., Hu, Y., Huggins, L.A., Eriksson, J.W., Buckett, L.K., Turnbull, A.V., Ginsberg, H.N., Blaner, W.S., Huang, L.S., Goldberg, I.J., DGAT1 deficiency decreases PPAR expression and does not lead to lipotoxicity in cardiac and skeletal muscle. J. Lipid Res. 52 (2011), 732–744.
51. [51] Lee, B., Fast, A.M., Zhu, J., Cheng, J.X., Buhman, K.K., Intestine-specific expression of acyl CoA:diacylglycerol acyltransferase 1 reverses resistance to diet-induced hepatic steatosis and obesity in Dgat1 −/− mice. J. Lipid Res. 51 (2010), 1770–1780.
52. [52] Chokshi, A., Drosatos, K., Cheema, F.H., Ji, R., Khawaja, T., Yu, S., Kato, T., Khan, R., Takayama, H., Knoll, R., Milting, H., Chung, C.S., Jorde, U., Naka, Y., Mancini, D.M., Goldberg, I.J., Schulze, P.C., Ventricular assist device implantation corrects myocardial lipotoxicity, reverses insulin resistance, and normalizes cardiac metabolism in patients with advanced heart failure. Circulation 125 (2012), 2844–2853.
53. [53] Lewin, T.M., de Jong, H., Schwerbrock, N.J., Hammond, L.E., Watkins, S.M., Combs, T.P., Coleman, R.A., Mice deficient in mitochondrial glycerol-3-phosphate acyltransferase-1 have diminished myocardial triacylglycerol accumulation during lipogenic diet and altered phospholipid fatty acid composition. Biochim. Biophys. Acta 1781 (2008), 352–358.
54. [54] Kok, B.P., Kienesberger, P.C., Dyck, J.R., Brindley, D.N., Relationship of glucose and oleate metabolism to cardiac function in lipin-1 deficient (fld) mice. J. Lipid Res. 53 (2012), 105–118.
55. [55] Mitra, M.S., Schilling, J.D., Wang, X., Jay, P.Y., Huss, J.M., Su, X., Finck, B.N., Cardiac lipin 1 expression is regulated by the peroxisome proliferator activated receptor gamma coactivator 1alpha/estrogen related receptor axis. J. Mol. Cell. Cardiol. 51 (2011), 120–128.
56. [56] Burgdorf, C., Hansel, L., Heidbreder, M., Johren, O., Schutte, F., Schunkert, H., Kurz, T., Suppression of cardiac phosphatidate phosphohydrolase 1 activity and lipin mRNA expression in Zucker diabetic fatty rats and humans with type 2 diabetes mellitus. Biochem. Biophys. Res. Commun. 390 (2009), 165–170.
57. [57] Jamal, Z., Martin, A., Gomez-Munoz, A., Hales, P., Chang, E., Russell, J.C., Brindley, D.N., Phosphatidate phosphohydrolases in liver, heart and adipose tissue of the JCR:LA corpulent rat and the lean genotypes: implications for glycerolipid synthesis and signal transduction. Int. J. Obes. Relat. Metab. Disord. 16 (1992), 789–799.
58. [58] Haemmerle, G., Moustafa, T., Woelkart, G., Buttner, S., Schmidt, A., van de Weijer, T., Hesselink, M., Jaeger, D., Kienesberger, P.C., Zierler, K., Schreiber, R., Eichmann, T., Kolb, D., Kotzbeck, P., Schweiger, M., Kumari, M., Eder, S., Schoiswohl, G., Wongsiriroj, N., Pollak, N.M., Radner, F.P., Preiss-Landl, K., Kolbe, T., Rulicke, T., Pieske, B., Trauner, M., Lass, A., Zimmermann, R., Hoefler, G., Cinti, S., Kershaw, E.E., Schrauwen, P., Madeo, F., Mayer, B., Zechner, R., ATGL-mediated fat catabolism regulates cardiac mitochondrial function via PPAR-alpha and PGC-1. Nat. Med. 17 (2011), 1076–1085.
59. [59] Kienesberger, P.C., Pulinilkunnil, T., Nagendran, J., Young, M.E., Bogner-Strauss, J.G., Hackl, H., Khadour, R., Heydari, E., Haemmerle, G., Zechner, R., Kershaw, E.E., Dyck, J.R., Early structural and metabolic cardiac remodelling in response to inducible adipose triglyceride lipase ablation. Cardiovasc. Res. 99 (2013), 442–451.
60. [60] Zierler, K.A., Jaeger, D., Pollak, N.M., Eder, S., Rechberger, G.N., Radner, F.P., Woelkart, G., Kolb, D., Schmidt, A., Kumari, M., Preiss-Landl, K., Pieske, B., Mayer, B., Zimmermann, R., Lass, A., Zechner, R., Haemmerle, G., Functional cardiac lipolysis in mice critically depends on comparative gene identification-58. J. Biol. Chem. 288 (2013), 9892–9904.
61. [61] Hirano, K., Ikeda, Y., Zaima, N., Sakata, Y., Matsumiya, G., Triglyceride deposit cardiomyovasculopathy. N. Engl. J. Med. 359 (2008), 2396–2398.
62. [62] Hirano, K., Tanaka, T., Ikeda, Y., Yamaguchi, S., Zaima, N., Kobayashi, K., Suzuki, A., Sakata, Y., Sakata, Y., Kobayashi, K., Toda, T., Fukushima, N., Ishibashi-Ueda, H., Tavian, D., Nagasaka, H., Hui, S.P., Chiba, H., Sawa, Y., Hori, M., Genetic mutations in adipose triglyceride lipase and myocardial up-regulation of peroxisome proliferated activated receptor-gamma in patients with triglyceride deposit cardiomyovasculopathy. Biochem. Biophys. Res. Commun. 443 (2014), 574–579.
63. [63] Pulinilkunnil, T., Kienesberger, P.C., Nagendran, J., Waller, T.J., Young, M.E., Kershaw, E.E., Korbutt, G., Haemmerle, G., Zechner, R., Dyck, J.R., Myocardial adipose triglyceride lipase overexpression protects diabetic mice from the development of lipotoxic cardiomyopathy. Diabetes 62 (2013), 1464–1477.
64. [64] Kienesberger, P.C., Pulinilkunnil, T., Sung, M.M., Nagendran, J., Haemmerle, G., Kershaw, E.E., Young, M.E., Light, P.E., Oudit, G.Y., Zechner, R., Dyck, J.R., Myocardial ATGL overexpression decreases the reliance on fatty acid oxidation and protects against pressure overload-induced cardiac dysfunction. Mol. Cell. Biol. 32 (2012), 740–750.
65. [65] Pulinilkunnil, T., Kienesberger, P.C., Nagendran, J., Sharma, N., Young, M.E., Dyck, J.R., Cardiac-specific adipose triglyceride lipase overexpression protects from cardiac steatosis and dilated cardiomyopathy following diet-induced obesity. Int. J. Obes. 38 (2013), 205–215.
66. [66] Ueno, M., Suzuki, J., Zenimaru, Y., Takahashi, S., Koizumi, T., Noriki, S., Yamaguchi, O., Otsu, K., Shen, W.J., Kraemer, F.B., Miyamori, I., Cardiac overexpression of hormone-sensitive lipase inhibits myocardial steatosis and fibrosis in streptozotocin diabetic mice. Am. J. Physiol. Endocrinol. Metab. 294 (2008), E1109–E1118.
67. [67] Pollak, N.M., Schweiger, M., Jaeger, D., Kolb, D., Kumari, M., Schreiber, R., Kolleritsch, S., Markolin, P., Grabner, G.F., Heier, C., Zierler, K.A., Ruelicke, T., Zimmermann, R., Lass, A., Zechner, R., Haemmerle, G., Cardiac-specific overexpression of perilipin 5 provokes severe cardiac steatosis via the formation of a lipolytic barrier. J. Lipid Res. 54 (2013), 1092–1102.
68. [68] Wang, H., Sreenivasan, U., Gong, D.W., O'Connell, K.A., Dabkowski, E.R., Hecker, P.A., Ionica, N., Konig, M., Mahurkar, A., Sun, Y., Stanley, W.C., Sztalryd, C., Cardiomyocyte specific perilipin 5 over expression leads to myocardial steatosis, and modest cardiac dysfunction. J. Lipid Res. 54 (2013), 953–965.
69. [69] Pollak, N.M., Jaeger, D., Kolleritsch, S., Zimmermann, R., Zechner, R., Lass, A., Haemmerle, G., The interplay of protein kinase A and perilipin 5 regulates cardiac lipolysis. J. Biol. Chem. 290 (2015), 1295–1306.
70. [70] Kuramoto, K., Okamura, T., Yamaguchi, T., Nakamura, T.Y., Wakabayashi, S., Morinaga, H., Nomura, M., Yanase, T., Otsu, K., Usuda, N., Matsumura, S., Inoue, K., Fushiki, T., Kojima, Y., Hashimoto, T., Sakai, F., Hirose, F., Osumi, T., Perilipin 5, a lipid droplet-binding protein, protects the heart from oxidative burden by sequestering fatty acid from excessive oxidation. J. Biol. Chem. 287 (2012), 23852–23863.
71. [71] Bartels, E.D., Nielsen, J.M., Hellgren, L.I., Ploug, T., Nielsen, L.B., Cardiac expression of microsomal triglyceride transfer protein is increased in obesity and serves to attenuate cardiac triglyceride accumulation. PLoS One, 4, 2009, e5300.
72. [72] Nielsen, L.B., Bartels, E.D., Bollano, E., Overexpression of apolipoprotein B in the heart impedes cardiac triglyceride accumulation and development of cardiac dysfunction in diabetic mice. J. Biol. Chem. 277 (2002), 27014–27020.
73. [73] Yokoyama, M., Yagyu, H., Hu, Y., Seo, T., Hirata, K., Homma, S., Goldberg, I.J., Apolipoprotein B production reduces lipotoxic cardiomyopathy: studies in heart-specific lipoprotein lipase transgenic mouse. J. Biol. Chem. 279 (2004), 4204–4211.
74. [74] He, L., Kim, T., Long, Q., Liu, J., Wang, P., Zhou, Y., Ding, Y., Prasain, J., Wood, P.A., Yang, Q., Carnitine palmitoyltransferase-1b deficiency aggravates pressure overload-induced cardiac hypertrophy caused by lipotoxicity. Circulation 126 (2012), 1705–1716.
75. [75] Haynie, K.R., Vandanmagsar, B., Wicks, S.E., Zhang, J., Mynatt, R.L., Inhibition of carnitine palymitoyltransferase1b induces cardiac hypertrophy and mortality in mice. Diabetes Obes. Metab. 16 (2014), 757–760.
76. [76] Lee, L., Campbell, R., Scheuermann-Freestone, M., Taylor, R., Gunaruwan, P., Williams, L., Ashrafian, H., Horowitz, J., Fraser, A.G., Clarke, K., Frenneaux, M., Metabolic modulation with perhexiline in chronic heart failure: a randomized, controlled trial of short-term use of a novel treatment. Circulation 112 (2005), 3280–3288.
77. [77] Luiken, J.J., Niessen, H.E., Coort, S.L., Hoebers, N., Coumans, W.A., Schwenk, R.W., Bonen, A., Glatz, J.F., Etomoxir-induced partial carnitine palmitoyltransferase-I (CPT-I) inhibition in vivo does not alter cardiac long-chain fatty acid uptake and oxidation rates. Biochem. J. 419 (2009), 447–455.
78. [78] Cabrero, A., Merlos, M., Laguna, J.C., Carrera, M.V., Down-regulation of acyl-CoA oxidase gene expression and increased NF-kappaB activity in etomoxir-induced cardiac hypertrophy. J. Lipid Res. 44 (2003), 388–398.
79. [79] Cheng, L., Ding, G., Qin, Q., Huang, Y., Lewis, W., He, N., Evans, R.M., Schneider, M.D., Brako, F.A., Xiao, Y., Chen, Y.E., Yang, Q., Cardiomyocyte-restricted peroxisome proliferator-activated receptor-delta deletion perturbs myocardial fatty acid oxidation and leads to cardiomyopathy. Nat. Med. 10 (2004), 1245–1250.
80. [80] Bakermans, A.J., Geraedts, T.R., van Weeghel, M., Denis, S., Joao Ferraz, M., Aerts, J.M., Aten, J., Nicolay, K., Houten, S.M., Prompers, J.J., Fasting-induced myocardial lipid accumulation in long-chain acyl-CoA dehydrogenase knockout mice is accompanied by impaired left ventricular function. Circ. Cardiovasc. Imaging 4 (2011), 558–565.
81. [81] Chambers, K.T., Leone, T.C., Sambandam, N., Kovacs, A., Wagg, C.S., Lopaschuk, G.D., Finck, B.N., Kelly, D.P., Chronic inhibition of pyruvate dehydrogenase in heart triggers an adaptive metabolic response. J. Biol. Chem. 286 (2011), 11155–11162.
82. [82] Ford, D.A., Han, X., Horner, C.C., Gross, R.W., Accumulation of unsaturated acylcarnitine molecular species during acute myocardial ischemia: metabolic compartmentalization of products of fatty acyl chain elongation in the acylcarnitine pool. Biochemistry 35 (1996), 7903–7909.
83. [83] Su, X., Han, X., Mancuso, D.J., Abendschein, D.R., Gross, R.W., Accumulation of long-chain acylcarnitine and 3-hydroxy acylcarnitine molecular species in diabetic myocardium: identification of alterations in mitochondrial fatty acid processing in diabetic myocardium by shotgun lipidomics. Biochemistry 44 (2005), 5234–5245.
84. [84] Koves, T.R., Ussher, J.R., Noland, R.C., Slentz, D., Mosedale, M., Ilkayeva, O., Bain, J., Stevens, R., Dyck, J.R., Newgard, C.B., Lopaschuk, G.D., Muoio, D.M., Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab. 7 (2008), 45–56.
85. [85] Idell-Wenger, J.A., Grotyohann, L.W., Neely, J.R., Coenzyme A and carnitine distribution in normal and ischemic hearts. J. Biol. Chem. 253 (1978), 4310–4318.
86. [86] Thyfault, J.P., Cree, M.G., Zheng, D., Zwetsloot, J.J., Tapscott, E.B., Koves, T.R., Ilkayeva, O., Wolfe, R.R., Muoio, D.M., Dohm, G.L., Contraction of insulin-resistant muscle normalizes insulin action in association with increased mitochondrial activity and fatty acid catabolism. Am. J. Physiol. Cell Physiol. 292 (2007), C729–C739.
87. [87] Ussher, J.R., Koves, T.R., Jaswal, J.S., Zhang, L., Ilkayeva, O., Dyck, J.R., Muoio, D.M., Lopaschuk, G.D., Insulin-stimulated cardiac glucose oxidation is increased in high-fat diet-induced obese mice lacking malonyl CoA decarboxylase. Diabetes 58 (2009), 1766–1775.
88. [88] Son, N.H., Yu, S., Tuinei, J., Arai, K., Hamai, H., Homma, S., Shulman, G.I., Abel, E.D., Goldberg, I.J., PPARgamma-induced cardiolipotoxicity in mice is ameliorated by PPARalpha deficiency despite increases in fatty acid oxidation. J. Clin. Invest. 120 (2010), 3443–3454.
89. [89] Battiprolu, P.K., Hojayev, B., Jiang, N., Wang, Z.V., Luo, X., Iglewski, M., Shelton, J.M., Gerard, R.D., Rothermel, B.A., Gillette, T.G., Lavandero, S., Hill, J.A., Metabolic stress-induced activation of FoxO1 triggers diabetic cardiomyopathy in mice. J. Clin. Invest. 122 (2012), 1109–1118.
90. [90] Anderson, E.J., Katunga, L.A., Willis, M.S., Mitochondria as a source and target of lipid peroxidation products in healthy and diseased heart. Clin. Exp. Pharmacol. Physiol. 39 (2012), 179–193.
91. [91] Lesnefsky, E.J., Minkler, P., Hoppel, C.L., Enhanced modification of cardiolipin during ischemia in the aged heart. J. Mol. Cell. Cardiol. 46 (2009), 1008–1015.
92. [92] Lim, H.Y., Bodmer, R., Phospholipid homeostasis and lipotoxic cardiomyopathy: a matter of balance. Fly 5 (2011), 234–236 (Austin).
93. [93] Gurung, I.S., Medina-Gomez, G., Kis, A., Baker, M., Velagapudi, V., Neogi, S.G., Campbell, M., Rodriguez-Cuenca, S., Lelliott, C., McFarlane, I., Oresic, M., Grace, A.A., Vidal-Puig, A., Huang, C.L., Deletion of the metabolic transcriptional coactivator PGC1beta induces cardiac arrhythmia. Cardiovasc. Res. 92 (2011), 29–38.
94. [94] Ovide-Bordeaux, S., Bescond-Jacquet, A., Grynberg, A., Cardiac mitochondrial alterations induced by insulin deficiency and hyperinsulinaemia in rats: targeting membrane homeostasis with trimetazidine. Clin. Exp. Pharmacol. Physiol. 32 (2005), 1061–1070.
95. [95] Cedars, A., Jenkins, C.M., Mancuso, D.J., Gross, R.W., Calcium-independent phospholipases in the heart: mediators of cellular signaling, bioenergetics, and ischemia-induced electrophysiologic dysfunction. J. Cardiovasc. Pharmacol. 53 (2009), 277–289.
96. [96] Lim, H.Y., Wang, W., Wessells, R.J., Ocorr, K., Bodmer, R., Phospholipid homeostasis regulates lipid metabolism and cardiac function through SREBP signaling in Drosophila. Genes Dev. 25 (2011), 189–200.
97. [97] Schmitz, G., Ruebsaamen, K., Metabolism and atherogenic disease association of lysophosphatidylcholine. Atherosclerosis 208 (2010), 10–18.
98. [98] Sobel, B.E., Corr, P.B., Robison, A.K., Goldstein, R.A., Witkowski, F.X., Klein, M.S., Accumulation of lysophosphoglycerides with arrhythmogenic properties in ischemic myocardium. J. Clin. Invest. 62 (1978), 546–553.
99. [99] Mancuso, D.J., Abendschein, D.R., Jenkins, C.M., Han, X., Saffitz, J.E., Schuessler, R.B., Gross, R.W., Cardiac ischemia activates calcium-independent phospholipase A2beta, precipitating ventricular tachyarrhythmias in transgenic mice: rescue of the lethal electrophysiologic phenotype by mechanism-based inhibition. J. Biol. Chem. 278 (2003), 22231–22236.
100. [100] Mancuso, D.J., Han, X., Jenkins, C.M., Lehman, J.J., Sambandam, N., Sims, H.F., Yang, J., Yan, W., Yang, K., Green, K., Abendschein, D.R., Saffitz, J.E., Gross, R.W., Dramatic accumulation of triglycerides and precipitation of cardiac hemodynamic dysfunction during brief caloric restriction in transgenic myocardium expressing human calcium-independent phospholipase A2gamma. J. Biol. Chem. 282 (2007), 9216–9227.
101. [101] Jenkins, C.M., Cedars, A., Gross, R.W., Eicosanoid signalling pathways in the heart. Cardiovasc. Res. 82 (2009), 240–249.
102. [102] Bikman, B.T., Summers, S.A., Ceramides as modulators of cellular and whole-body metabolism. J. Clin. Invest. 121 (2011), 4222–4230.
103. [103] Novgorodov, S.A., Riley, C.L., Keffler, J.A., Yu, J., Kindy, M.S., Macklin, W.B., Lombard, D.B., Gudz, T.I., SIRT3 deacetylates ceramide synthases: implications for mitochondrial dysfunction and brain injury. J. Biol. Chem., 2015 (ahead of print).
104. [104] Park, T.S., Hu, Y., Noh, H.L., Drosatos, K., Okajima, K., Buchanan, J., Tuinei, J., Homma, S., Jiang, X.C., Abel, E.D., Goldberg, I.J., Ceramide is a cardiotoxin in lipotoxic cardiomyopathy. J. Lipid Res. 49 (2008), 2101–2112.
105. [105] Russo, S.B., Baicu, C.F., Van Laer, A., Geng, T., Kasiganesan, H., Zile, M.R., Cowart, L.A., Ceramide synthase 5 mediates lipid-induced autophagy and hypertrophy in cardiomyocytes. J. Clin. Invest. 122 (2012), 3919–3930.
106. [106] Russo, S.B., Tidhar, R., Futerman, A.H., Cowart, L.A., Myristate-derived d16:0 sphingolipids constitute a cardiac sphingolipid pool with distinct synthetic routes and functional properties. J. Biol. Chem. 288 (2013), 13397–13409.
107. [107] Holland, W.L., Miller, R.A., Wang, Z.V., Sun, K., Barth, B.M., Bui, H.H., Davis, K.E., Bikman, B.T., Halberg, N., Rutkowski, J.M., Wade, M.R., Tenorio, V.M., Kuo, M.S., Brozinick, J.T., Zhang, B.B., Birnbaum, M.J., Summers, S.A., Scherer, P.E., Receptor-mediated activation of ceramidase activity initiates the pleiotropic actions of adiponectin. Nat. Med. 17 (2011), 55–63.
108. [108] Abel, E.D., Litwin, S.E., Sweeney, G., Cardiac remodeling in obesity. Physiol. Rev. 88 (2008), 389–419.
109. [109] Park, M., Sweeney, G., Direct effects of adipokines on the heart: focus on adiponectin. Heart Fail. Rev. 18 (2013), 631–644.
110. [110] Lee, S.Y., Kim, J.R., Hu, Y., Khan, R., Kim, S.J., Bharadwaj, K.G., Davidson, M.M., Choi, C.S., Shin, K.O., Lee, Y.M., Park, W.J., Park, I.S., Jiang, X.C., Goldberg, I.J., Park, T.S., Cardiomyocyte specific deficiency of serine palmitoyltransferase subunit 2 reduces ceramide but leads to cardiac dysfunction. J. Biol. Chem. 287 (2012), 18429–18439.
111. [111] Baranowski, M., Blachnio-Zabielska, A., Hirnle, T., Harasiuk, D., Matlak, K., Knapp, M., Zabielski, P., Gorski, J., Myocardium of type 2 diabetic and obese patients is characterized by alterations in sphingolipid metabolic enzymes but not by accumulation of ceramide. J. Lipid Res. 51 (2010), 74–80.
112. [112] Karliner, J.S., Honbo, N., Summers, K., Gray, M.O., Goetzl, E.J., The lysophospholipids sphingosine-1-phosphate and lysophosphatidic acid enhance survival during hypoxia in neonatal rat cardiac myocytes. J. Mol. Cell. Cardiol. 33 (2001), 1713–1717.
113. [113] Hilal-Dandan, R., Means, C.K., Gustafsson, A.B., Morissette, M.R., Adams, J.W., Brunton, L.L., Heller Brown, J., Lysophosphatidic acid induces hypertrophy of neonatal cardiac myocytes via activation of Gi and rho. J. Mol. Cell. Cardiol. 36 (2004), 481–493.
114. [114] Ishii, I., Fukushima, N., Ye, X., Chun, J., Lysophospholipid receptors: signaling and biology. Annu. Rev. Biochem. 73 (2004), 321–354.
115. [115] Means, C.K., Brown, J.H., Sphingosine-1-phosphate receptor signalling in the heart. Cardiovasc. Res. 82 (2009), 193–200.
116. [116] Hofmann, U., Burkard, N., Vogt, C., Thoma, A., Frantz, S., Ertl, G., Ritter, O., Bonz, A., Protective effects of sphingosine-1-phosphate receptor agonist treatment after myocardial ischaemia–reperfusion. Cardiovasc. Res. 83 (2009), 285–293.
117. [117] Holland, W.L., Bikman, B.T., Wang, L.P., Yuguang, G., Sargent, K.M., Bulchand, S., Knotts, T.A., Shui, G., Clegg, D.J., Wenk, M.R., Pagliassotti, M.J., Scherer, P.E., Summers, S.A., Lipid-induced insulin resistance mediated by the proinflammatory receptor TLR4 requires saturated fatty acid-induced ceramide biosynthesis in mice. J. Clin. Invest. 121 (2011), 1858–1870.
118. [118] Dong, B., Qi, D., Yang, L., Huang, Y., Xiao, X., Tai, N., Wen, L., Wong, F.S., TLR4 regulates cardiac lipid accumulation and diabetic heart disease in the nonobese diabetic mouse model of type 1 diabetes. Am. J. Physiol. Heart Circ. Physiol. 303 (2012), H732–H742.
119. [119] Shi, H., Kokoeva, M.V., Inouye, K., Tzameli, I., Yin, H., Flier, J.S., TLR4 links innate immunity and fatty acid-induced insulin resistance. J. Clin. Invest. 116 (2006), 3015–3025.
120. [120] Pal, D., Dasgupta, S., Kundu, R., Maitra, S., Das, G., Mukhopadhyay, S., Ray, S., Majumdar, S.S., Bhattacharya, S., Fetuin-A acts as an endogenous ligand of TLR4 to promote lipid-induced insulin resistance. Nat. Med. 18 (2012), 1279–1285.
121. [121] Huang, S., Rutkowsky, J.M., Snodgrass, R.G., Ono-Moore, K.D., Schneider, D.A., Newman, J.W., Adams, S.H., Hwang, D.H., Saturated fatty acids activate TLR-mediated proinflammatory signaling pathways. J. Lipid Res. 53 (2012), 2002–2013.
122. [122] Wong, S.W., Kwon, M.J., Choi, A.M., Kim, H.P., Nakahira, K., Hwang, D.H., Fatty acids modulate toll-like receptor 4 activation through regulation of receptor dimerization and recruitment into lipid rafts in a reactive oxygen species-dependent manner. J. Biol. Chem. 284 (2009), 27384–27392.
123. [123] Lin, M.E., Herr, D.R., Chun, J., Lysophosphatidic acid (LPA) receptors: signaling properties and disease relevance. Prostaglandins Other Lipid Mediat. 91 (2010), 130–138.
124. [124] Cremers, B., Flesch, M., Kostenis, E., Maack, C., Niedernberg, A., Stoff, A., Sudkamp, M., Wendler, O., Bohm, M., Modulation of myocardial contractility by lysophosphatidic acid (LPA). J. Mol. Cell. Cardiol. 35 (2003), 71–80.
125. [125] Pulinilkunnil, T., An, D., Ghosh, S., Qi, D., Kewalramani, G., Yuen, G., Virk, N., Abrahani, A., Rodrigues, B., Lysophosphatidic acid-mediated augmentation of cardiomyocyte lipoprotein lipase involves actin cytoskeleton reorganization. Am. J. Physiol. Heart Circ. Physiol. 288 (2005), H2802–H2810.
126. [126] Chen, J., Chen, Y., Zhu, W., Han, Y., Han, B., Xu, R., Deng, L., Cai, Y., Cong, X., Yang, Y., Hu, S., Chen, X., Specific LPA receptor subtype mediation of LPA-induced hypertrophy of cardiac myocytes and involvement of Akt and NFkappaB signal pathways. J. Cell. Biochem. 103 (2008), 1718–1731.
127. [127] Yang, J., Nie, Y., Wang, F., Hou, J., Cong, X., Hu, S., Chen, X., Reciprocal regulation of miR-23a and lysophosphatidic acid receptor signaling in cardiomyocyte hypertrophy. Biochim. Biophys. Acta 1831 (2013), 1386–1394.
128. [128] Lin, Z., Murtaza, I., Wang, K., Jiao, J., Gao, J., Li, P.F., miR-23a functions downstream of NFATc3 to regulate cardiac hypertrophy. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 12103–12108.
129. [129] Wang, K., Lin, Z.Q., Long, B., Li, J.H., Zhou, J., Li, P.F., Cardiac hypertrophy is positively regulated by microRNA miR-23a. J. Biol. Chem. 287 (2012), 589–599.
130. [130] Rachakonda, V.P., Reeves, V.L., Aljammal, J., Wills, R.C., Trybula, J.S., DeLany, J.P., Kienesberger, P.C., Kershaw, E.E., Serum autotaxin is independently associated with hepatic steatosis in women with severe obesity. Obesity (Silver Spring) 23 (2015), 965–972.
131. [131] Reeves, V.L., Trybula, J.S., R. C., W., Goodpaster, B.H., J. J., D., Kienesberger, P.C., Kershaw, E.E., Serum autotaxin/ENPP2 correlates with insulin resistance in older humans with obesity. Obesity 23 (2015), 2371–2376.
132. [132] Nishimura, S., Nagasaki, M., Okudaira, S., Aoki, J., Ohmori, T., Ohkawa, R., Nakamura, K., Igarashi, K., Yamashita, H., Eto, K., Uno, K., Hayashi, N., Kadowaki, T., Komuro, I., Yatomi, Y., Nagai, R., ENPP2 contributes to adipose tissue expansion in diet-induced obesity. Diabetes 63 (2014), 4154–4164.
133. [133] Rancoule, C., Dusaulcy, R., Treguer, K., Gres, S., Attane, C., Saulnier-Blache, J.S., Involvement of autotaxin/lysophosphatidic acid signaling in obesity and impaired glucose homeostasis. Biochimie 96 (2013), 140–143.
134. [134] Unger, R.H., Scherer, P.E., Holland, W.L., Dichotomous roles of leptin and adiponectin as enforcers against lipotoxicity during feast and famine. Mol. Biol. Cell 24 (2013), 3011–3015.
135. [135] Atkinson, L.L., Fischer, M.A., Lopaschuk, G.D., Leptin activates cardiac fatty acid oxidation independent of changes in the AMP-activated protein kinase-acetyl-CoA carboxylase-malonyl-CoA axis. J. Biol. Chem. 277 (2002), 29424–29430.
136. [136] Lee, Y., Naseem, R.H., Duplomb, L., Park, B.H., Garry, D.J., Richardson, J.A., Schaffer, J.E., Unger, R.H., Hyperleptinemia prevents lipotoxic cardiomyopathy in acyl CoA synthase transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 101 (2004), 13624–13629.
137. [137] Myers, M.G. Jr., Leibel, R.L., Seeley, R.J., Schwartz, M.W., Obesity and leptin resistance: distinguishing cause from effect. Trends Endocrinol. Metab. 21 (2010), 643–651.
138. [138] Churchill, E., Budas, G., Vallentin, A., Koyanagi, T., Mochly-Rosen, D., PKC isozymes in chronic cardiac disease: possible therapeutic targets?. Annu. Rev. Pharmacol. Toxicol. 48 (2008), 569–599.
139. [139] Way, K.J., Isshiki, K., Suzuma, K., Yokota, T., Zvagelsky, D., Schoen, F.J., Sandusky, G.E., Pechous, P.A., Vlahos, C.J., Wakasaki, H., King, G.L., Expression of connective tissue growth factor is increased in injured myocardium associated with protein kinase C beta2 activation and diabetes. Diabetes 51 (2002), 2709–2718.
140. [140] Xia, Z., Kuo, K.H., Nagareddy, P.R., Wang, F., Guo, Z., Guo, T., Jiang, J., McNeill, J.H., N-acetylcysteine attenuates PKCbeta2 overexpression and myocardial hypertrophy in streptozotocin-induced diabetic rats. Cardiovasc. Res. 73 (2007), 770–782.
141. [141] Lei, S., Li, H., Xu, J., Liu, Y., Gao, X., Wang, J., Ng, K.F., Lau, W.B., Ma, X.L., Rodrigues, B., Irwin, M.G., Xia, Z., Hyperglycemia-induced protein kinase C beta2 activation induces diastolic cardiac dysfunction in diabetic rats by impairing caveolin-3 expression and Akt/eNOS signaling. Diabetes 62 (2013), 2318–2328.
142. [142] Ferreira, J.C., Brum, P.C., Mochly-Rosen, D., betaIIPKC and epsilonPKC isozymes as potential pharmacological targets in cardiac hypertrophy and heart failure. J. Mol. Cell. Cardiol. 51 (2011), 479–484.
143. [143] Guo, M., Wu, M.H., Korompai, F., Yuan, S.Y., Upregulation of PKC genes and isozymes in cardiovascular tissues during early stages of experimental diabetes. Physiol. Genomics 12 (2003), 139–146.
144. +-sensitive isoforms in the failing human heart. Circulation 99 (1999), 384–391.
145. [145] Wakasaki, H., Koya, D., Schoen, F.J., Jirousek, M.R., Ways, D.K., Hoit, B.D., Walsh, R.A., King, G.L., Targeted overexpression of protein kinase C beta2 isoform in myocardium causes cardiomyopathy. Proc. Natl. Acad. Sci. U. S. A. 94 (1997), 9320–9325.
146. [146] Bowman, J.C., Steinberg, S.F., Jiang, T., Geenen, D.L., Fishman, G.I., Buttrick, P.M., Expression of protein kinase C beta in the heart causes hypertrophy in adult mice and sudden death in neonates. J. Clin. Invest. 100 (1997), 2189–2195.
147. [147] Min, W., Bin, Z.W., Quan, Z.B., Hui, Z.J., Sheng, F.G., The signal transduction pathway of PKC/NF-kappa B/c-fos may be involved in the influence of high glucose on the cardiomyocytes of neonatal rats. Cardiovasc. Diabetol., 8, 2009, 8.
148. [148] Kawamura, N., Kubota, T., Kawano, S., Monden, Y., Feldman, A.M., Tsutsui, H., Takeshita, A., Sunagawa, K., Blockade of NF-kappaB improves cardiac function and survival without affecting inflammation in TNF-alpha-induced cardiomyopathy. Cardiovasc. Res. 66 (2005), 520–529.
149. [149] Higuchi, Y., Chan, T.O., Brown, M.A., Zhang, J., DeGeorge, B.R. Jr., Funakoshi, H., Gibson, G., McTiernan, C.F., Kubota, T., Jones, W.K., Feldman, A.M., Cardioprotection afforded by NF-kappaB ablation is associated with activation of Akt in mice overexpressing TNF-alpha. Am. J. Physiol. Heart Circ. Physiol. 290 (2006), H590–H598.
150. [150] Itani, S.I., Ruderman, N.B., Schmieder, F., Boden, G., Lipid-induced insulin resistance in human muscle is associated with changes in diacylglycerol, protein kinase C, and IkappaB-alpha. Diabetes 51 (2002), 2005–2011.
151. [151] Ghosh, S., Baltimore, D., Activation in vitro of NF-kappa B by phosphorylation of its inhibitor I kappa B. Nature 344 (1990), 678–682.
152. [152] Yu, C., Chen, Y., Cline, G.W., Zhang, D., Zong, H., Wang, Y., Bergeron, R., Kim, J.K., Cushman, S.W., Cooney, G.J., Atcheson, B., White, M.F., Kraegen, E.W., Shulman, G.I., Mechanism by which fatty acids inhibit insulin activation of insulin receptor substrate-1 (IRS-1)-associated phosphatidylinositol 3-kinase activity in muscle. J. Biol. Chem. 277 (2002), 50230–50236.
153. [153] Kang, N., Alexander, G., Park, J.K., Maasch, C., Buchwalow, I., Luft, F.C., Haller, H., Differential expression of protein kinase C isoforms in streptozotocin-induced diabetic rats. Kidney Int. 56 (1999), 1737–1750.
154. [154] Galbo, T., Perry, R.J., Jurczak, M.J., Camporez, J.P., Alves, T.C., Kahn, M., Guigni, B.A., Serr, J., Zhang, D., Bhanot, S., Samuel, V.T., Shulman, G.I., Saturated and unsaturated fat induce hepatic insulin resistance independently of TLR-4 signaling and ceramide synthesis in vivo. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 12780–12785.
155. [155] Eichmann, T.O., Kumari, M., Haas, J.T., Farese, R.V. Jr., Zimmermann, R., Lass, A., Zechner, R., Studies on the substrate and stereo/regioselectivity of adipose triglyceride lipase, hormone-sensitive lipase, and diacylglycerol-O-acyltransferases. J. Biol. Chem. 287 (2012), 41446–41457.
156. [156] Pettitt, T.R., Martin, A., Horton, T., Liossis, C., Lord, J.M., Wakelam, M.J., Diacylglycerol and phosphatidate generated by phospholipases C and D, respectively, have distinct fatty acid compositions and functions. phospholipase D-derived diacylglycerol does not activate protein kinase C in porcine aortic endothelial cells. J. Biol. Chem. 272 (1997), 17354–17359.
157. [157] Madani, S., Hichami, A., Legrand, A., Belleville, J., Khan, N.A., Implication of acyl chain of diacylglycerols in activation of different isoforms of protein kinase C. FASEB J. 15 (2001), 2595–2601.
158. [158] Cuschieri, J., Bulger, E., Billgrin, J., Garcia, I., Maier, R.V., Acid sphingomyelinase is required for lipid raft TLR4 complex formation. Surg. Infect. 8 (2007), 91–106.
159. [159] Stratford, S., Hoehn, K.L., Liu, F., Summers, S.A., Regulation of insulin action by ceramide: dual mechanisms linking ceramide accumulation to the inhibition of Akt/protein kinase B. J. Biol. Chem. 279 (2004), 36608–36615.
160. [160] Powell, D.J., Hajduch, E., Kular, G., Hundal, H.S., 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.
161. [161] Miura, A., Kajita, K., Ishizawa, M., Kanoh, Y., Kawai, Y., Natsume, Y., Sakuma, H., Yamamoto, Y., Yasuda, K., Ishizuka, T., Inhibitory effect of ceramide on insulin-induced protein kinase Czeta translocation in rat adipocytes. Metabolism 52 (2003), 19–24.
162. [162] Jaeschke, A., Davis, R.J., Metabolic stress signaling mediated by mixed-lineage kinases. Mol. Cell 27 (2007), 498–508.
163. [163] Galadari, S., Rahman, A., Pallichankandy, S., Galadari, A., Thayyullathil, F., Role of ceramide in diabetes mellitus: evidence and mechanisms. Lipids Health Dis., 12, 2013, 98.
164. [164] Sathyanarayana, P., Barthwal, M.K., Kundu, C.N., Lane, M.E., Bergmann, A., Tzivion, G., Rana, A., Activation of the Drosophila MLK by ceramide reveals TNF-alpha and ceramide as agonists of mammalian MLK3. Mol. Cell 10 (2002), 1527–1533.
165. [165] Xu, Z., Maroney, A.C., Dobrzanski, P., Kukekov, N.V., Greene, L.A., The MLK family mediates c-Jun N-terminal kinase activation in neuronal apoptosis. Mol. Cell. Biol. 21 (2001), 4713–4724.
166. [166] Kanety, H., Hemi, R., Papa, M.Z., Karasik, A., Sphingomyelinase and ceramide suppress insulin-induced tyrosine phosphorylation of the insulin receptor substrate-1. J. Biol. Chem. 271 (1996), 9895–9897.
167. [167] Ola, A., Kerkela, R., Tokola, H., Pikkarainen, S., Skoumal, R., Vuolteenaho, O., Ruskoaho, H., The mixed-lineage kinase 1-3 signalling pathway regulates stress response in cardiac myocytes via GATA-4 and AP-1 transcription factors. Br. J. Pharmacol. 159 (2010), 717–725.
168. [168] Chen, C.L., Lin, C.F., Chang, W.T., Huang, W.C., Teng, C.F., Lin, Y.S., Ceramide induces p38 MAPK and JNK activation through a mechanism involving a thioredoxin-interacting protein-mediated pathway. Blood 111 (2008), 4365–4374.
169. [169] Hreniuk, D., Garay, M., Gaarde, W., Monia, B.P., McKay, R.A., Cioffi, C.L., Inhibition of c-Jun N-terminal kinase 1, but not c-Jun N-terminal kinase 2, suppresses apoptosis induced by ischemia/reoxygenation in rat cardiac myocytes. Mol. Pharmacol. 59 (2001), 867–874.
170. [170] Liang, Q., Molkentin, J.D., Redefining the roles of p38 and JNK signaling in cardiac hypertrophy: dichotomy between cultured myocytes and animal models. J. Mol. Cell. Cardiol. 35 (2003), 1385–1394.
171. [171] Aoki, H., Kang, P.M., Hampe, J., Yoshimura, K., Noma, T., Matsuzaki, M., Izumo, S., Direct activation of mitochondrial apoptosis machinery by c-Jun N-terminal kinase in adult cardiac myocytes. J. Biol. Chem. 277 (2002), 10244–10250.
172. [172] Wang, J., Zhen, L., Klug, M.G., Wood, D., Wu, X., Mizrahi, J., Involvement of caspase 3- and 8-like proteases in ceramide-induced apoptosis of cardiomyocytes. J. Card. Fail. 6 (2000), 243–249.
173. [173] Dyntar, D., Eppenberger-Eberhardt, M., Maedler, K., Pruschy, M., Eppenberger, H.M., Spinas, G.A., Donath, M.Y., Glucose and palmitic acid induce degeneration of myofibrils and modulate apoptosis in rat adult cardiomyocytes. Diabetes 50 (2001), 2105–2113.