Myristic acid potentiates palmitic acid-induced lipotoxicity and steatohepatitis associated with lipodystrophy by sustaning de novo ceramide synthesis

Oncotarget

Volumn 6, Issue 39, 2015, Pages 41479-41496

  Martínez, Laura ^a,b   Torres, Sandra ^a,b   Baulies, Anna ^a,b   Alarcón Vila, Cristina ^a,b   Elena, Montserrat ^c   Fabriàs, Gemma ^d   Casas, Josefina ^d   Caballeria, Joan ^b   Fernandez Checa, Jose C ^a,b,e   García Ruiz, Carmen ^a,b,e  

^a INST D INVESTIGACIONS B   (Spain)

^b INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^c HOSPITAL CLÍNIC   (Spain)

^d DEPARTMENT OF ENVIRONMENTAL CHEMISTRY   (Spain)

^e UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Endoplasmic reticulum; FFA; Hepatocyte; NAFLD; Pathology section; Sphingolipid

Indexed keywords

CASPASE 3; CERAMIDE; CHOLESTEROL; CYTOCHROME C; MYRISTIC ACID; PALMITIC ACID; REACTIVE OXYGEN METABOLITE; TAUROURSODEOXYCHOLIC ACID; ANTHRACENE DERIVATIVE; CERS2 PROTEIN, MOUSE; DIHYDROCERAMIDE DESATURASE; MONOUNSATURATED FATTY ACID; OXIDOREDUCTASE; PROTEIN KINASE INHIBITOR; PYRAZOLANTHRONE; RUTHENIUM RED; SPHINGOSINE ACYLTRANSFERASE; STRESS ACTIVATED PROTEIN KINASE; THERMOZYMOCIDIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; HEPATITIS; HEPATOSPLENOMEGALY; IN VITRO STUDY; IN VIVO STUDY; LIPODYSTROPHY; LIPOTOXICITY; LIVER FIBROSIS; LIVER INJURY; MALE; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; SPHINGOLIPID METABOLISM; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; C57BL MOUSE; CHEMICALLY INDUCED; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; ENZYMOLOGY; GENETICS; KNOCKOUT MOUSE; LIVER; LIVER CELL; LIVER MITOCHONDRION; METABOLISM; NON-ALCOHOLIC FATTY LIVER DISEASE; OXIDATIVE STRESS; PATHOLOGY; TIME FACTOR;

ANIMALS; ANTHRACENES; APOPTOSIS; CERAMIDES; CHOLESTEROL; DISEASE MODELS, ANIMAL; ENDOPLASMIC RETICULUM STRESS; FATTY ACIDS, MONOUNSATURATED; HEPATOCYTES; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LIPODYSTROPHY; LIVER; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA, LIVER; MYRISTIC ACID; NON-ALCOHOLIC FATTY LIVER DISEASE; OXIDATIVE STRESS; OXIDOREDUCTASES; PALMITIC ACID; PROTEIN KINASE INHIBITORS; REACTIVE OXYGEN SPECIES; RUTHENIUM RED; SPHINGOSINE N-ACYLTRANSFERASE; TIME FACTORS;

EID: 84951810549     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6286     Document Type: Article

References (47)

1. Luedde T, Kaplowitz N, Schwabe RF. Cell death and cell death responses in liver disease: mechanisms and clinical relevance. Gastroenterology 2015.
2. Liang H, Zhong Y, Zhou S, Li QQ. Palmitic acid-induced apoptosis in pancreatic β-cells is increased by liver X receptor agonist and attenuated by eicosapentaenoate. in vivo (Brooklyn). 2011;25:711-8.
3. Pan Z, Wang J, Tang H, Li L, Lv J, Xia L, et al. Effects of palmitic acid on lipid metabolism homeostasis and apoptosis in goose primary hepatocytes. Mol. Cell. Biochem. 2011;350:39-46.
4. Feldstein AE, Werneburg NW, Li Z, Bronk SF, Gores GJ. Bax inhibition protects against free fatty acid-induced lysosomal permeabilization. Am. J. Physiol. Gastrointest. Liver Physiol. 2006;290:G1339-46.
5. Tanabe K, Liu Y, Hasan SD, Martinez SC, Cras-Méneur C, Welling CM, et al. Glucose and fatty acids synergize to promote B-cell apoptosis through activation of glycogen synthase kinase 3β independent of JNK activation. PLoS One. 2011;6:e18146.
6. Win S, Than TA, Le BH, García-Ruiz C, Fernandez-Checa JC, Kaplowitz N. Sab (Sh3bp5) dependence of JNK mediated inhibition of mitochondrial respiration in palmitic acid induced hepatocyte lipotoxicity. J Hepatol 2015; 62:1367-74.
7. Egnatchik RA, Leamy AK, Jacobson DA, Shiota M, Young JD. ER calcium release promotes mitochondrial dysfunction and hepatic cell lipotoxicity in response to palmitate overload. Mol Metab 2014; 3:544-553.
8. Cazanave SC, Mott JL, Bronk SF, Werneburg NW, Fingas CD, Meng XW, Finnberg N, El-Deiry WS, Kaufmann SH, Gores GJ. Death receptor 5 signaling promotes hepatocyte lipoapoptosis. J. Biol. Chem. 286:39336-48.
9. Kakisaka K, Cazanave SC, Fingas CD, Guicciardi ME, Bronk SF, Werneburg NW, Mott JL, Gores GJ. Mechanisms of lysophosphatidylcholine-induced hepatocyte lipoapoptosis. Am. J. Physiol. 302:G77-84.
10. Hannun YA, Obeid LM. Principles of bioactive lipid signalling: lessons from sphingolipids. Nat Rev Mol Cell Biol 2008; 9:139-50.
11. Morales A, Lee H, Goñi F, Kolesnick R, Fernandez-Checa JC. Sphingolipids and cell death. Apoptosis 2007; 12:923-39.
12. Garcia-Ruiz C, Morales A, Fernandez-Checa JC. Sphingolipids and cell death: one aim, many ways. Apoptosis 2015; 20: 607-20.
13. Park WJ, Park JW, Merrill AH, Storch J, Pewzner-Jung Y, Futerman AH. Hepatic fatty acid uptake is regulated by the sphingolipid acyl chain length. Biochim Biophys Acta 2014; 1841:1754-66.
14. Mizutani Y, Kihara A, Chiba H, Tojo H, Igarashi Y. 2-Hydroxy-ceramide synthesis by ceramide synthase family: enzymatic basis for the preference of FA chain length. J Lipid Res 2008; 49:2356-64.
15. García-Ruiz C, Colell A, Marí M, Morales A, Fernández-Checa JC. Direct effect of ceramide on the mitochondrial electron transport chain leads to generation of reactive oxygen species. Role of mitochondrial glutathione. J. Biol. Chem. 1997;272:11369-77.
16. Garcia-Ruiz C, Mato JM, Vance D, Kaplowitz N, Fernández-Checa JC. Acid sphingomyelinase-ceramide system in steatohepatitis: a novel target regulating multiple pathways. J Hepatol 2015; 62:219-33.
17. Ogretmen B, Hannun YA. Biologically active sphingolipids in cancer pathogenesis and treatment. Nat Rev Cancer 2004; 4:604-16.
18. Tomita K, Teratani T, Yokoyama H, Suzuki T, Irie R, Ebinuma H, Saito H, Hokari R, Miura S, Hibi T. Plasma free myristic acid proportion is a predictor of nonalcoholic steatohepatitis. Dig Dis Sci 2011; 56:3045-52.
19. Rioux V, Catheline D, Bouriel M, Legrand P. Dietary myristic acid at physiologically relevant levels increases the tissue content of C20:5 n-3 and C20:3 n-6 in the rat. Reprod Nutri Dev 2005; 45:599-612.
20. Debois D, Bralet M, Le Naour F, Brunelle A, Laprevote O. in situ lipidomic analysis of nonalcoholic fatty liver by cluster TOF-SIMS imaging. Anal Chem 2009; 81:2823-31.
21. Bauchamp E, Goenaga D, LeBloch J, Catheline D, Legrand P, Rioux V. Myristic acid increases the activity of dihydroceramide delta4-desaturase 1 through its N-terminal myriotoylation. Biochimie 2007; 89: 1553-61.
22. Russo SB, Baicu CF, Van Laer A, Geng T, Kasiganesan H, Zile MR, Cowart LA. Ceramide synthase 5 mediates lipidinduced autophagy and hypertrophy in cardiomyocytes. J Clin Invest 2012; 122:3919-30.
23. Moon JS, Lee S, Park MA, Siempos II, Haslip M, Lee PJ, Yun M, Kim CK, Howrylak J, Ryter SW, UCP2-induced fatty acid synthase promotes NLRP3 inflammasome activation during sepsis. J Clin Invest 2015, 125: 665-80.
24. Miyake Y, Kozutsumi Y, Nakamura S, Fujita T, Kawasaki T. Serine palmitoyltransferase is the primary target of a sphingosine-like immunosuppressant, ISP-1/myriocin. Biochem. Biophys. Res. Commun. 1995; 211: 396-403.
25. Malhi H, Kaufman RJ. Endoplasmic reticulum stress in liver disease. J. Hepatol. 2011;54:795-809.
26. Dara L, Ji C, Kaplowitz N. The contribution of endoplasmic reticulum stress to liver diseases. Hepatology 2011; 53:1752-63.
27. Ozcan U, Yilmaz E, Ozcan L, Furuhashi M, Vaillancourt E, Smith RO, Görgün CZ, Hotamisligil GS. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 2006; 313:1137-40.
28. Raichur S, Wang ST, Chan PW, Li Y, Ching J, Chaurasia B, Dogra S, Öhman MK, Takeda K, Sugii S, Pewzner-Jung Y, Futerman AH, Summers SA. CerS2 haploinsufficiency inhibits β-oxidation and confers susceptibility to dietinduced steatohepatitis and insulin resistance. Cell Metab 2014; 20:687-95.
29. Zigdon H, Kogot-Levin A, Park JW, Goldschmidt R, Kelly S, Merrill AH Jr, Scherz A, Pewzner-Jung Y, Saada A, Futerman AH. Ablation of ceramide synthase 2 causes chronic oxidative stress due to disruption of the mitochondrial respiratory chain. J. Biol. Chem 288:4947-56.
30. Kirichok Y, Krapivinsky G, Clapham DE. The mitochondrial calcium uniporter is a highly selective ion channel. Nature 2004; 427: 360-4.
31. Listenberger LL, Ory DS, Schaffer JE. Palmitate-induced apoptosis can occur through a ceramide-independent pathway. J. Biol. Chem. 2001;276:14890-5.
32. Wei Y, Wang D, Topczewski F, Pagliassotti MJ. Saturated fatty acids induce endoplasmic reticulum stress and apoptosis independently of ceramide in liver cells. Am. J. Physiol. Endocrinol. Metab. 2006;291:E275-81.
33. Han G, Gupta SD, Gable K, Niranjanakumari S, Moitra P, Eichler F, et al. Identification of small subunits of mammalian serine palmitoyltransferase that confer distinct acyl-CoA substrate specificities. Proc. Natl. Acad. Sci. U. S. A. 2009;106:8186-91.
34. Hornemann T, Penno A, Rütti MF, Ernst D, Kivrak-Pfiffner F, Rohrer L, von Eckardstein A. The SPTLC3 subunit of serine palmitoyltransferase generates short chain sphingoid bases. J Biol Chem 2009; 284: 26322-30.
35. Yoshimine Y, Uto H, Kumagai K, Mawatari S, Arima S, Ibusuki R, Mera K, Nosaki T, Kanmura S, Numata M, Tamai T, Moriuchi A, Tsubouchi H, Ido A. Hepatic expression of the Sptlc3 subunit of serine palmitoyltransferase is associated with the development of hepatocellular carcinoma in a mouse model of nonalcoholic steatohepatitis. Oncol Rep 2015; 33: 1657-66.
36. Senkal CE, Ponnusamy S, Bielawski J, Hannun YA, Ogretmen B. Antiapoptotic roles of ceramide-synthase-6-generated C16-ceramide via selective regulation of the ATF6/CHOP arm of ER-stress-response pathways. FASEB J 2010; 24: 296-308.
37. Fucho R, Martínez L, Baulies A, Torres S, Tarrats N, Fernandez A, Ribas V, Astudillo AM, Balsinde J, Garcia-Rovés P, Elena M, Bergheim I, Lotersztajn S, Trautwein C, Appelqvist H, Paton AW, Paton JC, Czaja MJ, Kaplowitz N, Fernandez-Checa JC, García-Ruiz C. ASMase regulates autophagy and lysosomal membrane permeabilization and its inhibition prevents early stage non-alcoholic steatohepatitis. J Hepatol 2014; 61: 1126-34.
38. Quillet-Mary A, Jaffrézou JP, Mansat V, Bordier C, Naval J, Laurent G. Implication of mitochondrial hydrogen peroxide generation in ceramide-induced apoptosis. J Biol Chem 1997; 272:21388-95.
39. Gudz TI, Tserng KY, Hoppel CL. Direct inhibition of mitochondrial respiratory chain complex III by cellpermeable ceramide. J Biol Chem 1997; 272: 24154-8.
40. Arora AS, Jones BJ, Patel TC, Bronk SF, Gores GJ. Ceramide induces hepatocyte cell death through disruption of mitochondrial function in the rat. Hepatology 1997; 25: 958-63.
41. Voss KA, Riley RT, Bacon CW, Meredith FI, Norred WP. Toxicity and sphinganine levels are correlated in rats fed fumonisin B1 (FB1) or hydrolized FB1. Environ. Toxicol. Pharmacol. 1998;5:101-104.
42. Soriano JM, González L, Catalá AI. Mechanism of action of sphingolipids and their metabolites in the toxicity of fumonisin B1. Prog. Lipid Res. 2005;44:345-56.
43. Matsuzawa N, Takamura T, Kurita S, Misu H, Ota T, Ando H, Yokoyama M, Honda M, Zen Y, Nakamura Y, Miyamoto KI, Kaneko S. Lipid-induced oxidative s tress causes steatohepatitis in mice fed an atherogenic diet. Hepatology 2007; 46: 1392-1403.
44. Chong YH, Ng TKW. Effect of palm oil on cardiovascular risk. Med J Malaysia 1991; 46:41-50.
45. Mann JP, Armstrong MJ, Sewel P, Rajwal S, McClean P. Ethnic differences in paedriatic non-alcoholic fatty liver disease (Abstract). J Hepatol 2015; 62:S823
46. Garcia-Ruiz C, Mari M, Morales A, Colell A, Ardite E, Fernandez-Checa JC. Human placenta sphingomyelinase, an exogenous acidic pH-optimum sphingomyelinase, induces oxidative stress, glutathione depletion and apoptosis in rat hepatocytes. Hepatology 2000; 32: 56-65.
47. Kleinfeld AM, Prothro D, Brown DL, Davis RC, Richieri GC, DeMaria A. Increases in serum unbound free fatty acid levels following coronary angioplasty. Am J Cardiol 1996; 78: 1350-4.