Absence of perilipin 2 prevents hepatic steatosis, glucose intolerance and ceramide accumulation in alcohol-fed mice

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Carr, Rotonya M ^a   Peralta, Giselle ^a   Yin, Xiaoyan ^a   Ahima, Rexford S ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; CERAMIDE; PERILIPIN; PERILIPIN 2; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; MEMBRANE PROTEIN;

ALCOHOL CONSUMPTION; ALCOHOL LIVER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY COMPOSITION; BODY WEIGHT; CALORIC INTAKE; CARBON DIOXIDE EXCRETION; CONTROLLED STUDY; DISEASE MODEL; DOWN REGULATION; ENERGY BALANCE; ENERGY EXPENDITURE; FATTY LIVER; GENE CONTROL; GENOTYPE; GLUCOSE HOMEOSTASIS; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE; GLUCOSE TOLERANCE TEST; HISTOPATHOLOGY; IN VIVO STUDY; KNOCKOUT MOUSE; LIPID ANALYSIS; LIPID HOMEOSTASIS; LIPID STORAGE; LIPOGENESIS; MALE; MOUSE; NONHUMAN; OXYGEN CONSUMPTION; PROTEIN FUNCTION; WILD TYPE; ANIMAL; C57BL MOUSE; GENETICS; HOMEOSTASIS; LIPID METABOLISM; LIVER; METABOLISM; PATHOLOGY; PHYSIOLOGY; TIME;

ANIMALS; BODY COMPOSITION; BODY WEIGHT; CERAMIDES; DOWN-REGULATION; ETHANOL; FATTY LIVER; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE TEST; HOMEOSTASIS; LIPID METABOLISM; LIVER; LIVER DISEASES, ALCOHOLIC; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OXYGEN CONSUMPTION; TIME FACTORS; TRIGLYCERIDES;

EID: 84901302133     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0097118     Document Type: Article

References (60)

1. O'Shea RS, Dasarathy S, McCullough AJ (2010) Alcoholic liver disease. Hepatology 51: 307-328.
2. National Institute on Alcohol Abuse and Alcoholism (U.S.) (2005) Alcohol alert. Rockville, Md. National Institute on Alcohol Abuse and Alcoholism.
3. Watson CG (1987) Recidivism in "controlled drinker" alcoholics: a longitudinal study. Journal of clinical psychology 43: 404-412.
4. Wanless IR, Lentz JS (1990) Fatty liver hepatitis (steatohepatitis) and obesity: an autopsy study with analysis of risk factors. Hepatology 12: 1106-1110.
5. Raynard B, Balian A, Fallik D, Capron F, Bedossa P, et al. (2002) Risk factors of fibrosis in alcohol-induced liver disease. Hepatology 35: 635-638. (Pubitemid 34183969)
6. de la Monte SM, Yeon JE, Tong M, Longato L, Chaudhry R, et al. (2008) Insulin resistance in experimental alcohol-induced liver disease. Journal of gastroenterology and hepatology 23: e477-486.
7. de la Monte SM, Pang M, Chaudhry R, Duan K, Longato L, et al. (2011) Peroxisome proliferator-activated receptor agonist treatment of alcohol-induced hepatic insulin resistance. Hepatology research: the official journal of the Japan Society of Hepatology 41: 386-398.
8. Ramirez T, Tong M, Chen WC, Nguyen QG, Wands JR, et al. (2013) Chronic alcohol-induced hepatic insulin resistance and endoplasmic reticulum stress ameliorated by peroxisome-proliferator activated receptor-delta agonist treatment. Journal of gastroenterology and hepatology 28: 179-187.
9. Carr RM, Dhir R, Yin X, Agarwal B, Ahima RS (2013) Temporal effects of ethanol consumption on energy homeostasis, hepatic steatosis, and insulin sensitivity in mice. Alcoholism, clinical and experimental research 37: 1091-1099.
10. You M, Matsumoto M, Pacold CM, Cho WK, Crabb DW (2004) The role of AMP-activated protein kinase in the action of ethanol in the liver. Gastroenterology 127: 1798-1808. (Pubitemid 39575858)
11. Nakajima T, Kamijo Y, Tanaka N, Sugiyama E, Tanaka E, et al. (2004) Peroxisome proliferator-activated receptor alpha protects against alcohol-induced liver damage. Hepatology 40: 972-980. (Pubitemid 39288131)
12. Clugston RD, Jiang H, Lee MX, Piantedosi R, Yuen JJ, et al. (2011) Altered hepatic lipid metabolism in C57BL/6 mice fed alcohol: a targeted lipidomic and gene expression study. Journal of lipid research 52: 2021-2031.
13. Altamirano J, Bataller R (2011) Alcoholic liver disease: pathogenesis and new targets for therapy. Nature reviews Gastroenterology & hepatology 8: 491-501.
14. Brasaemle DL, Wolins NE (2012) Packaging of fat: an evolving model of lipid droplet assembly and expansion. The Journal of biological chemistry 287: 2273-2279.
15. Gross DA, Zhan C, Silver DL (2011) Direct binding of triglyceride to fat storage-inducing transmembrane proteins 1 and 2 is important for lipid droplet formation. Proceedings of the National Academy of Sciences of the United States of America 108: 19581-19586.
16. Bickel PE, Tansey JT, Welte MA (2009) PAT proteins, an ancient family of lipid droplet proteins that regulate cellular lipid stores. Biochim Biophys Acta 1791: 419-440.
17. McIntosh AL, Storey SM, Atshaves BP (2010) Intracellular lipid droplets contain dynamic pools of sphingomyelin: ADRP binds phospholipids with high affinity. Lipids 45: 465-477.
18. Crunk AE, Monks J, Murakami A, Jackman M, Maclean PS, et al. (2013) Dynamic regulation of hepatic lipid droplet properties by diet. PloS one 8: e67631.
19. Carr RM, Patel RT, Rao V, Dhir R, Graham MJ, et al. (2012) Reduction of TIP47 improves hepatic steatosis and glucose homeostasis in mice. American journal of physiology Regulatory, integrative and comparative physiology 302: R996-1003.
20. Chang BH, Li L, Paul A, Taniguchi S, Nannegari V, et al. (2006) Protection against fatty liver but normal adipogenesis in mice lacking adipose differentiation-related protein. Molecular and cellular biology 26: 1063-1076. (Pubitemid 43146498)
21. Imai Y, Varela GM, Jackson MB, Graham MJ, Crooke RM, et al. (2007) Reduction of hepatosteatosis and lipid levels by an adipose differentiation- related protein antisense oligonucleotide. Gastroenterology 132: 1947-1954. (Pubitemid 46677941)
22. Varela GM, Antwi DA, Dhir R, Yin X, Singhal NS, et al. (2008) Inhibition of ADRP prevents diet-induced insulin resistance. American journal of physiology Gastrointestinal and liver physiology 295: G621-628.
23. Dalen KT, Ulven SM, Arntsen BM, Solaas K, Nebb HI (2006) PPARalpha activators and fasting induce the expression of adipose differentiation-related protein in liver. Journal of lipid research 47: 931-943. (Pubitemid 43778694)
24. Imai Y, Boyle S, Varela GM, Caron E, Yin X, et al. (2012) Effects of perilipin 2 antisense oligonucleotide treatment on hepatic lipid metabolism and gene expression. Physiological genomics 44: 1125-1131.
25. Straub BK, Stoeffel P, Heid H, Zimbelmann R, Schirmacher P (2008) Differential pattern of lipid droplet-associated proteins and de novo perilipin expression in hepatocyte steatogenesis. Hepatology 47: 1936-1946. (Pubitemid 351945561)
26. Straub BK, Gyoengyoesi B, Koenig M, Hashani M, Pawella LM, et al. (2013) Adipophilin/perilipin-2 as a lipid droplet-specific marker for metabolically active cells and diseases associated with metabolic dysregulation. Histopathology 62: 617-631.
27. Listenberger LL, Ostermeyer-Fay AG, Goldberg EB, Brown WJ, Brown DA (2007) Adipocyte differentiation-related protein reduces the lipid droplet association of adipose triglyceride lipase and slows triacylglycerol turnover. Journal of lipid research 48: 2751-2761. (Pubitemid 350272859)
28. Chang BH, Li L, Saha P, Chan L (2010) Absence of adipose differentiation related protein upregulates hepatic VLDL secretion, relieves hepatosteatosis, and improves whole body insulin resistance in leptin-deficient mice. Journal of lipid research 51: 2132-2142.
29. McManaman JL, Bales ES, Orlicky DJ, Jackman M, MacLean PS, et al. (2013) Perilipin-2-null mice are protected against diet-induced obesity, adipose inflammation, and fatty liver disease. Journal of lipid research 54: 1346-1359.
30. Mak KM, Ren C, Ponomarenko A, Cao Q, Lieber CS (2008) Adipose differentiation-related protein is a reliable lipid droplet marker in alcoholic fatty liver of rats. Alcoholism, clinical and experimental research 32: 683-689. (Pubitemid 351430433)
31. Orlicky DJ, Roede JR, Bales E, Greenwood C, Greenberg A, et al. (2011) Chronic ethanol consumption in mice alters hepatocyte lipid droplet properties. Alcoholism, clinical and experimental research 35: 1020-1033.
32. Imanishi Y, Sun W, Maeda T, Maeda A, Palczewski K (2008) Retinyl ester homeostasis in the adipose differentiation-related protein-deficient retina. The Journal of biological chemistry 283: 25091-25102.
33. Matyash V, Liebisch G, Kurzchalia TV, Shevchenko A, Schwudke D (2008) Lipid extraction by methyl-tert-butyl ether for high-throughput lipidomics. Journal of lipid research 49: 1137-1146.
34. Chen J, Narayan SB, Edinger AL, Bennett MJ (2012) Flow injection tandem mass spectrometric measurement of ceramides of multiple chain lengths in biological samples. Journal of chromatography B, Analytical technologies in the biomedical and life sciences 883-884: 136-140.
35. Deaciuc IV, Nikolova-Karakashian M, Fortunato F, Lee EY, Hill DB, et al. (2000) Apoptosis and dysregulated ceramide metabolism in a murine model of alcohol-enhanced lipopolysaccharide hepatotoxicity. Alcoholism, clinical and experimental research 24: 1557-1565.
36. Liangpunsakul S, Sozio MS, Shin E, Zhao Z, Xu Y, et al. (2010) Inhibitory effect of ethanol on AMPK phosphorylation is mediated in part through elevated ceramide levels. American journal of physiology Gastrointestinal and liver physiology 298: G1004-1012.
37. Zhao Z, Yu M, Crabb D, Xu Y, Liangpunsakul S (2011) Ethanol-induced alterations in fatty acid-related lipids in serum and tissues in mice. Alcoholism, clinical and experimental research 35: 229-234.
38. Longato L, Ripp K, Setshedi M, Dostalek M, Akhlaghi F, et al. (2012) Insulin resistance, ceramide accumulation, and endoplasmic reticulum stress in human chronic alcohol-related liver disease. Oxidative medicine and cellular longevity 2012: 479348.
39. Hannun YA, Obeid LM (2008) Principles of bioactive lipid signalling: lessons from sphingolipids. Nature reviews Molecular cell biology 9: 139-150. (Pubitemid 351158911)
40. Mandrekar P, Ambade A, Lim A, Szabo G, Catalano D (2011) An essential role for monocyte chemoattractant protein-1 in alcoholic liver injury: regulation of proinflammatory cytokines and hepatic steatosis in mice. Hepatology 54: 2185-2197.
41. Miller AM, Horiguchi N, Jeong WI, Radaeva S, Gao B (2011) Molecular mechanisms of alcoholic liver disease: innate immunity and cytokines. Alcoholism, clinical and experimental research 35: 787-793.
42. Pastorino JG, Hoek JB (2000) Ethanol potentiates tumor necrosis factor-alpha cytotoxicity in hepatoma cells and primary rat hepatocytes by promoting induction of the mitochondrial permeability transition. Hepatology 31: 1141-1152. (Pubitemid 30233240)
43. Cahill A, Stabley GJ, Wang X, Hoek JB (1999) Chronic ethanol consumption causes alterations in the structural integrity of mitochondrial DNA in aged rats. Hepatology 30: 881-888. (Pubitemid 29458275)
44. Ji C, Chan C, Kaplowitz N (2006) Predominant role of sterol response element binding proteins (SREBP) lipogenic pathways in hepatic steatosis in the murine intragastric ethanol feeding model. Journal of hepatology 45: 717-724. (Pubitemid 44479875)
45. McVicker BL, Rasineni K, Tuma DJ, McNiven MA, Casey CA (2012) Lipid droplet accumulation and impaired fat efflux in polarized hepatic cells: consequences of ethanol metabolism. International journal of hepatology 2012: 978136.
46. Sztalryd C, Bell M, Lu X, Mertz P, Hickenbottom S, et al. (2006) Functional compensation for adipose differentiation-related protein (ADFP) by Tip47 in an ADFP null embryonic cell line. The Journal of biological chemistry 281: 34341-34348. (Pubitemid 46043256)
47. Magne J, Aminoff A, Perman Sundelin J, Mannila MN, Gustafsson P, et al. (2013) The minor allele of the missense polymorphism Ser251Pro in perilipin 2 (PLIN2) disrupts an alpha-helix, affects lipolysis, and is associated with reduced plasma triglyceride concentration in humans. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 27: 3090-3099.
48. Bulankina AV, Deggerich A, Wenzel D, Mutenda K, Wittmann JG, et al. (2009) TIP47 functions in the biogenesis of lipid droplets. J Cell Biol 185: 641-655.
49. Buers I, Robenek H, Lorkowski S, Nitschke Y, Severs NJ, et al. (2009) TIP47, a lipid cargo protein involved in macrophage triglyceride metabolism. Arteriosclerosis, thrombosis, and vascular biology 29: 767-773.
50. Denucci SM, Tong M, Longato L, Lawton M, Setshedi M, et al. (2010) Rat strain differences in susceptibility to alcohol-induced chronic liver injury and hepatic insulin resistance. Gastroenterology research and practice 2010.
51. Lieber CS, DeCarli LM (1982) The feeding of alcohol in liquid diets: two decades of applications and 1982 update. Alcoholism, clinical and experimental research 6: 523-531. (Pubitemid 13201236)
52. Holley DC, Bagby GJ, Curry DL (1981) Ethanol-insulin interrelationships in the rat studied in vitro and in vivo: evidence for direct ethanol inhibition of biphasic glucose-induced insulin secretion. Metabolism: clinical and experimental 30: 894-899. (Pubitemid 11057489)
53. Tiengo A, Valerio A, Molinari M, Meneghel A, Lapolla A (1981) Effect of ethanol, acetaldehyde, and acetate on insulin and glucagon secretion in the perfused rat pancreas. Diabetes 30: 705-709. (Pubitemid 11022654)
54. Liangpunsakul S, Rahmini Y, Ross RA, Zhao Z, Xu Y, et al. (2012) Imipramine blocks ethanol-induced ASMase activation, ceramide generation, and PP2A activation, and ameliorates hepatic steatosis in ethanol-fed mice. American journal of physiology Gastrointestinal and liver physiology 302: G515-523.
55. Dobrowsky RT, Kamibayashi C, Mumby MC, Hannun YA (1993) Ceramide activates heterotrimeric protein phosphatase 2A. The Journal of Biological Chemistry 268: 15523-15530. (Pubitemid 23222045)
56. Grosch S, Schiffmann S, Geisslinger G (2012) Chain length-specific properties of ceramides. Progress in lipid research 51: 50-62.
57. Karahatay S, Thomas K, Koybasi S, Senkal CE, Elojeimy S, et al. (2007) Clinical relevance of ceramide metabolism in the pathogenesis of human head and neck squamous cell carcinoma (HNSCC): attenuation of C(18)-ceramide in HNSCC tumors correlates with lymphovascular invasion and nodal metastasis. Cancer letters 256: 101-111. (Pubitemid 47333333)
58. Siskind LJ, Colombini M (2000) The lipids C2- and C16-ceramide form large stable channels. Implications for apoptosis. The Journal of biological chemistry 275: 38640-38644. (Pubitemid 32009194)
59. Hannun YA, Obeid LM (2011) Many ceramides. The Journal of biological chemistry 286: 27855-27862.
60. Lizarazo D, Zabala V, Tong M, Longato L, de la Monte SM (2013) Ceramide inhibitor myriocin restores insulin/insulin growth factor signaling for liver remodeling in experimental alcohol-related steatohepatitis. Journal of gastroenterology and hepatology 28: 1660-1668.