Caloric restriction and intermittent fasting alter hepatic lipid droplet proteome and diacylglycerol species and prevent diabetes in NZO mice

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1851, Issue 5, 2015, Pages 566-576

  Baumeier, Christian ^a,b   Kaiser, Daniel ^a,b   Heeren, Jörg ^c   Scheja, Ludger ^c   John, Clara ^c   Weise, Christoph ^d   Eravci, Murat ^d   Lagerpusch, Merit ^a,b   Schulze, Gunnar ^a,b   Joost, Hans Georg ^a,b   Schwenk, Robert Wolfgang ^a,b   Schürmann, Annette ^a,b  

^a GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

^b GERMAN CENTER FOR DIABETES RESEARCH DZD   (Germany)

^c UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^d FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Caloric restriction; Diacylglycerol; Fatty acid oxidation; Insulin resistance; Intermittent fasting; Lipid droplet proteome

Indexed keywords

AMINOACYLASE; DIACYLGLYCEROL; FAT DROPLET; FATTY ACID BINDING PROTEIN; FATTY ACID BINDING PROTEIN 5; GLUTATHIONE TRANSFERASE A3; MACROPHAGE MIGRATION INHIBITION FACTOR; POLYPEPTIDE; POLYPEPTIDE 2; POSITIVE TRANSCRIPTION ELONGATION FACTOR B; PROTEOME; UNCLASSIFIED DRUG; FATTY ACID; GLUCOSE BLOOD LEVEL; INSULIN; PRKCE PROTEIN, MOUSE; PROTEIN KINASE C EPSILON;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALORIC RESTRICTION; CONTROLLED STUDY; HYPERGLYCEMIA; INSULIN SENSITIVITY; MALE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PREVALENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS; ANIMAL; BLOOD; COMPLICATION; DIABETES MELLITUS, TYPE 2; DIET RESTRICTION; DIET THERAPY; DISEASE MODEL; FOOD DEPRIVATION; GLUCOSE BLOOD LEVEL; INSULIN RESISTANCE; LIVER; METABOLISM; MOUSE MUTANT; OBESITY; OXIDATION REDUCTION REACTION; SKELETAL MUSCLE; TIME;

MUS;

ANIMALS; BLOOD GLUCOSE; CALORIC RESTRICTION; DIABETES MELLITUS, TYPE 2; DIGLYCERIDES; DISEASE MODELS, ANIMAL; FASTING; FATTY ACIDS; FOOD DEPRIVATION; INSULIN; INSULIN RESISTANCE; LIPID DROPLETS; LIVER; MALE; MICE, OBESE; MUSCLE, SKELETAL; OBESITY; OXIDATION-REDUCTION; PROTEIN KINASE C-EPSILON; PROTEOME; TIME FACTORS;

EID: 84922572631     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2015.01.013     Document Type: Article

References (47)

1. International Diabetes Federation IDF Diabetes Atlas 6th ed. 2013
2. S.J. Heydrick, N.B. Ruderman, T.G. Kurowski, H.B. Adams, and K.S. Chen Enhanced stimulation of diacylglycerol and lipid synthesis by insulin in denervated muscle. Altered protein kinase C activity and possible link to insulin resistance Diabetes 40 1991 1707 1711
3. F.R. Jornayvaz, and G.I. Shulman Diacylglycerol activation of protein kinase Cε and hepatic insulin resistance Cell Metab. 15 2012 574 584
4. J.M. Adams, T. Pratipanawatr, R. Berria, E. Wang, R.A. DeFronzo, M.C. Sullards, and L.J. Mandarino Ceramide content is increased in skeletal muscle from obese insulin-resistant humans Diabetes 53 2004 25 31
5. B.A. Ellis, A. Poynten, A.J. Lowy, S.M. Furler, D.J. Chisholm, E.W. Kraegen, and G.J. Cooney Long-chain acyl-CoA esters as indicators of lipid metabolism and insulin sensitivity in rat and human muscle Am. J. Physiol. Endocrinol. Metab. 279 2000 E554 E560
6. S.J. Mihalik, B.H. Goodpaster, D.E. Kelley, D.H. Chace, J. Vockley, F.G.S. Toledo, and J.P. DeLany Increased levels of plasma acylcarnitines in obesity and type 2 diabetes and identification of a marker of glucolipotoxicity Obesity (Silver Spring) 18 2010 1695 1700
7. A.S. Greenberg, R.A. Coleman, F.B. Kraemer, J.L. McManaman, M.S. Obin, V. Puri, Q.-W. Yan, H. Miyoshi, and D.G. Mashek The role of lipid droplets in metabolic disease in rodents and humans J. Clin. Invest. 121 2011 2102 2110
8. L. Liu, X. Shi, C.S. Choi, G.I. Shulman, K. Klaus, K.S. Nair, G.J. Schwartz, Y. Zhang, I.J. Goldberg, and Y.-H. Yu Paradoxical coupling of triglyceride synthesis and fatty acid oxidation in skeletal muscle overexpressing DGAT1 Diabetes 58 2009 2516 2524
9. C. Wang, Y. Zhao, X. Gao, L. Li, Y. Yuan, F. Liu, L. Zhang, J. Wu, P. Hu, X. Zhang, Y. Gu, Y. Xu, Z. Li, H. Zhang, and J. Ye Perilipin 5 improves hepatic lipotoxicity by inhibiting lipolysis Hepatology 2015 http://dx.doi.org/10.1002/hep.27409
10. M. Bell, H. Wang, H. Chen, J.C. McLenithan, D.-W. Gong, R.-Z. Yang, D. Yu, S.K. Fried, M.J. Quon, C. Londos, and C. Sztalryd Consequences of lipid droplet coat protein downregulation in liver cells: abnormal lipid droplet metabolism and induction of insulin resistance Diabetes 57 2008 2037 2045
11. J.Z. Li, J. Ye, B. Xue, J. Qi, J. Zhang, Z. Zhou, Q. Li, Z. Wen, and P. Li Cideb regulates diet-induced obesity, liver steatosis, and insulin sensitivity by controlling lipogenesis and fatty acid oxidation Diabetes 56 2007 2523 2532
12. M.K. Basantani, M.T. Sitnick, L. Cai, D.S. Brenner, N.P. Gardner, J.Z. Li, G. Schoiswohl, K. Yang, M. Kumari, R.W. Gross, R. Zechner, and E.E. Kershaw Pnpla3/Adiponutrin deficiency in mice does not contribute to fatty liver disease or metabolic syndrome J. Lipid Res. 52 2011 318 329
13. L. Fontana, L. Partridge, and V.D. Longo Extending healthy life span - from yeast to humans Science 328 2010 321 326
14. V.D. Longo, and M.P. Mattson Fasting: molecular mechanisms and clinical applications Cell Metab. 19 2014 181 192
15. J.A. Mattison, G.S. Roth, T.M. Beasley, E.M. Tilmont, A.M. Handy, R.L. Herbert, D.L. Longo, D.B. Allison, J.E. Young, M. Bryant, D. Barnard, W.F. Ward, W. Qi, D.K. Ingram, and R. de Cabo Impact of caloric restriction on health and survival in rhesus monkeys from the NIA study Nature 489 2012 318 321
16. R.M. Anderson, D. Shanmuganayagam, and R. Weindruch Caloric restriction and aging: studies in mice and monkeys Toxicol. Pathol. 37 2009 47 51
17. S.Y. Park, G.H. Choi, H.I. Choi, J. Ryu, C.Y. Jung, and W. Lee Calorie restriction improves whole-body glucose disposal and insulin resistance in association with the increased adipocyte-specific GLUT4 expression in Otsuka Long-Evans Tokushima fatty rats Arch. Biochem. Biophys. 436 2005 276 284
18. E.P. Weiss, S.B. Racette, D.T. Villareal, L. Fontana, K. Steger-May, K.B. Schechtman, S. Klein, and J.O. Holloszy Improvements in glucose tolerance and insulin action induced by increasing energy expenditure or decreasing energy intake: a randomized controlled trial Am. J. Clin. Nutr. 84 2006 1033 1042
19. L. Fontana, and S. Klein Aging, Adiposity, and Calorie Restriction 297 2007
20. R. Wan, S. Camandola, and M.P. Mattson Intermittent fasting and dietary supplementation with 2-deoxy-d-glucose improve functional and metabolic cardiovascular risk factors in rats FASEB J. 17 2003 1133 1134
21. C.R. Pedersen, I. Hagemann, T. Bock, and K. Buschard Intermittent feeding and fasting reduces diabetes incidence in BB rats Autoimmunity 30 1999 243 250
22. R.M. Anson, Z. Guo, R. de Cabo, T. Iyun, M. Rios, A. Hagepanos, D.K. Ingram, M.A. Lane, and M.P. Mattson Intermittent fasting dissociates beneficial effects of dietary restriction on glucose metabolism and neuronal resistance to injury from calorie intake Proc. Natl. Acad. Sci. U. S. A. 100 2003 6216 6220
23. R. Kluge, S. Scherneck, A. Schürmann, and H.-G. Joost Pathophysiology and genetics of obesity and diabetes in the New Zealand obese mouse: a model of the human metabolic syndrome Methods Mol. Biol. 933 2012 59 73
24. N. Schulz, H. Himmelbauer, M. Rath, M. van Weeghel, S. Houten, W. Kulik, K. Suhre, S. Scherneck, H. Vogel, R. Kluge, P. Wiedmer, H.-G. Joost, and A. Schürmann Role of medium- and short-chain l-3-hydroxyacyl-CoA dehydrogenase in the regulation of body weight and thermogenesis Endocrinology 152 2011 4641 4651
25. K.N. Frayn Calculation of substrate oxidation rates in vivo from gaseous exchange J. Appl. Physiol. Respir. Environ. Exerc. Physiol. 55 1983 628 634
26. O. Kluth, F. Mirhashemi, S. Scherneck, D. Kaiser, R. Kluge, S. Neschen, H.-G. Joost, and A. Schürmann Dissociation of lipotoxicity and glucotoxicity in a mouse model of obesity associated diabetes: role of forkhead box O1 (FOXO1) in glucose-induced beta cell failure Diabetologia 54 2011 605 616
27. K.T. Uysal, L. Scheja, S.M. Wiesbrock, S. Bonner-Weir, and G.S. Hotamisligil Improved glucose and lipid metabolism in genetically obese mice lacking aP2 Endocrinology 141 2000 3388 3396
28. A. Chadt, K. Leicht, A. Deshmukh, L.Q. Jiang, S. Scherneck, U. Bernhardt, T. Dreja, H. Vogel, K. Schmolz, R. Kluge, J.R. Zierath, C. Hultschig, R.C. Hoeben, A. Schürmann, H.-G. Joost, and H. Al-Hasani Tbc1d1 mutation in lean mouse strain confers leanness and protects from diet-induced obesity Nat. Genet. 40 2008 1354 1359
29. S. Keipert, M. Ost, A. Chadt, A. Voigt, V. Ayala, M. Portero-Otin, R. Pamplona, H. Al-Hasani, and S. Klaus Skeletal muscle uncoupling-induced longevity in mice is linked to increased substrate metabolism and induction of the endogenous antioxidant defense system Am. J. Physiol. Endocrinol. Metab. 304 2013 E495 E506
30. A.H. Merrill, M.C. Sullards, J.C. Allegood, S. Kelly, and E. Wang Sphingolipidomics: high-throughput, structure-specific, and quantitative analysis of sphingolipids by liquid chromatography tandem mass spectrometry Methods 36 2005 207 224
31. J.L. Cantley, T. Yoshimura, J.P.G. Camporez, D. Zhang, F.R. Jornayvaz, N. Kumashiro, F. Guebre-Egziabher, M.J. Jurczak, M. Kahn, B.A. Guigni, J. Serr, J. Hankin, R.C. Murphy, G.W. Cline, S. Bhanot, V.P. Manchem, J.M. Brown, V.T. Samuel, and G.I. Shulman CGI-58 knockdown sequesters diacylglycerols in lipid droplets/ER-preventing diacylglycerol-mediated hepatic insulin resistance Proc. Natl. Acad. Sci. U. S. A. 110 2013 1869 1874
32. J. Cox, N. Neuhauser, A. Michalski, R.A. Scheltema, J.V. Olsen, and M. Mann Andromeda: a peptide search engine integrated into the MaxQuant environment J. Proteome Res. 10 2011 1794 1805
33. A.S. Greenberg, R.A. Coleman, F.B. Kraemer, J.L. Mcmanaman, M.S. Obin, V. Puri, Q. Yan, H. Miyoshi, and D.G. Mashek Review Series: The Role of Lipid Droplets in Metabolic Disease in Rodents and Humans 121 2011
34. S. Turró, M. Ingelmo-Torres, J.M. Estanyol, F. Tebar, M.A. Fernández, C.V. Albor, K. Gaus, T. Grewal, C. Enrich, and A. Pol Identification and characterization of associated with lipid droplet protein 1: a novel membrane-associated protein that resides on hepatic lipid droplets Traffic 7 2006 1254 1269
35. A.E. Crunk, J. Monks, A. Murakami, M. Jackman, P.S. Maclean, M. Ladinsky, E.S. Bales, S. Cain, D.J. Orlicky, and J.L. McManaman Dynamic regulation of hepatic lipid droplet properties by diet PLoS One 8 2013 e67631
36. H. Zhang, Y. Wang, J. Li, J. Yu, J. Pu, L. Li, H. Zhang, S. Zhang, G. Peng, F. Yang, and P. Liu Proteome of skeletal muscle lipid droplet reveals association with mitochondria and apolipoprotein a-I J. Proteome Res. 10 2011 4757 4768
37. C. Gragnoli Hypercholesterolemia and a candidate gene within the 12q24 locus Cardiovasc. Diabetol. 10 2011 38
38. M.K. Thomas, S.W. Tsang, M.-L. Yeung, P.S. Leung, and K.-M. Yao The roles of the PDZ-containing proteins bridge-1 and PDZD2 in the regulation of insulin production and pancreatic beta-cell mass Curr. Protein Pept. Sci. 10 2009 30 36
39. J.L. Volinic, J.H. Lee, K. Eto, V. Kaur, and M.K. Thomas Overexpression of the coactivator bridge-1 results in insulin deficiency and diabetes Mol. Endocrinol. 20 2006 167 182
40. K. Liu, and M.J. Czaja Regulation of lipid stores and metabolism by lipophagy Cell Death Differ. 20 2013 3 11
41. I. Nikolic, M. Vujicic, T. Saksida, T. Berki, S. Stosic-Grujicic, and I. Stojanovic The role of endogenous glucocorticoids in glucose metabolism and immune status of MIF-deficient mice Eur. J. Pharmacol. 714 2013 498 506
42. H.Y. Moon, P. Song, C.S. Choi, S.H. Ryu, and P.-G. Suh Involvement of exercise-induced macrophage migration inhibitory factor in the prevention of fatty liver disease J. Endocrinol. 218 2013 339 348
43. R.A. Miller, Y. Chang, A.T. Galecki, K. Al-Regaiey, J.J. Kopchick, and A. Bartke Gene expression patterns in calorically restricted mice: partial overlap with long-lived mutant mice Mol. Endocrinol. 16 2002 2657 2666
44. E. Krízová, and V. Simek Effect of intermittent feeding with high-fat diet on changes of glycogen, protein and fat content in liver and skeletal muscle in the laboratory mouse Physiol. Res. 45 1996 379 383
45. L.K. Heilbronn, S.R. Smith, C.K. Martin, S.D. Anton, and E. Ravussin Alternate-day fasting in nonobese subjects: effects on body weight, body composition, and energy metabolism Am. J. Clin. Nutr. 81 2005 69 73
46. H.S. Jürgens, A. Schürmann, R. Kluge, S. Ortmann, S. Klaus, H.-G. Joost, and M.H. Tschöp Hyperphagia, lower body temperature, and reduced running wheel activity precede development of morbid obesity in New Zealand obese mice Physiol. Genomics 25 2006 234 241
47. M. Hatori, C. Vollmers, A. Zarrinpar, L. DiTacchio, E.A. Bushong, S. Gill, M. Leblanc, A. Chaix, M. Joens, J.A.J. Fitzpatrick, M.H. Ellisman, and S. Panda Time-restricted feeding without reducing caloric intake prevents metabolic diseases in mice fed a high-fat diet Cell Metab. 15 2012 848 860