Progressive adaptation of hepatic ketogenesis in mice fed a high-fat diet

American Journal of Physiology - Endocrinology and Metabolism

Volumn 298, Issue 6, 2010, Pages

  Sunny, Nishanth E ^a   Satapati, Santhosh ^a,b   Fu, Xiaorong ^a   He, TianTeng ^a   Mehdibeigi, Roshi ^a   Spring Robinson, Chandra ^a   Duarte, Joao ^a   Potthoff, Matthew J ^c   Browning, Jeffrey D ^a   Burgess, Shawn C ^a,b,c  

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

^b UNIVERSITY OF TEXAS AT DALLAS   (United States)

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

Author keywords

Hepatic insulin resistance; Liquid chromatography tandem mass spectrometry; Nuclear magnetic resonance

Indexed keywords

ACYLCARNITINE; KETONE; KETONE BODY;

ADAPTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; C57BL 6 MOUSE; CONTROLLED STUDY; INSULIN RESISTANCE; KETOGENESIS; LIPID DIET; LIPID OXIDATION; LIVER MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; CHROMATOGRAPHY, LIQUID; DIETARY FATS; FEMALE; INSULIN RESISTANCE; KETONE BODIES; LIVER; MAGNETIC RESONANCE SPECTROSCOPY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; POLYMERASE CHAIN REACTION; PPAR ALPHA; REGRESSION ANALYSIS; RNA, MESSENGER; TANDEM MASS SPECTROMETRY;

EID: 77952618580     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00033.2010     Document Type: Article

References (55)

1. An J, Muoio DM, Shiota M, Fujimoto Y, Cline GW, Shulman GI, Koves TR, Stevens R, Millington D, Newgard CB. Hepatic expression of malonyl-CoA decarboxylase reverses muscle, liver and whole-animal insulin resistance. Nat Med 10: 268-274, 2004.
2. Badman MK, Pissios P, Kennedy AR, Koukos G, Flier JS, Maratos-Flier E. Hepatic fibroblast growth factor 21 is regulated by PPARalpha and is a key mediator of hepatic lipid metabolism in ketotic states. Cell Metab 5: 426-437, 2007. (Pubitemid 46825495)
3. Bailey JW, Haymond MW, Miles JM. Validation of two-pool model for in vivo ketone body kinetics. Am J Physiol Endocrinol Metab 258: E850-E855, 1990.
4. Balasse EO, Neef MA. Inhibition of ketogenesis by ketone bodies in fasting humans. Metabolism 24: 999-1007, 1975.
5. Berglund ED, Li CY, Bina HA, Lynes SE, Michael MD, Shanafelt AB, Kharitonenkov A, Wasserman DH. Fibroblast growth factor 21 controls glycemia via regulation of hepatic glucose flux and insulin sensitivity. Endocrinology 150: 4084-4093, 2009.
6. Beuers U, Beckh K, Jungermann K. Control of ketogenesis in the perfused rat liver by the sympathetic innervation. Eur J Biochem 158: 19-24, 1986. (Pubitemid 16066505)
7. Beylot M, Beaufrere B, Normand S, Riou JP, Cohen R, Mornex R. Determination of human ketone body kinetics using stable-isotope labelled tracers. Diabetologia 29: 90-96, 1986. (Pubitemid 16162749)
8. 3 tracers. Am J Physiol Endocrinol Metab 253: E496-E502, 1987.
9. Burgess SC, He T, Yan Z, Lindner J, Sherry AD, Malloy CR, Browning JD, Magnuson MA. Cytosolic phosphoenolpyruvate carboxykinase does not solely control the rate of hepatic gluconeogenesis in the intact mouse liver. Cell Metab 5: 313-320, 2007. (Pubitemid 46477858)
10. Burgess SC, Jeffrey FM, Storey C, Milde A, Hausler N, Merritt ME, Mulder H, Holm C, Sherry AD, Malloy CR. Effect of murine strain on metabolic pathways of glucose production after brief or prolonged fasting. Am J Physiol Endocrinol Metab 289: E53-E61, 2005.
11. Chambrier C, Laville M, Rhzioual Berrada K, Odeon M, Boulétreau P, Beylot M. Insulin sensitivity of glucose and fat metabolism in severe sepsis. Clin Sci (Lond) 99: 321-328, 2000.
12. Chan MY, Zhao Y, Heng CK. Sequential responses to high-fat and high-calorie feeding in an obese mouse model. Obesity (Silver Spring) 16: 972-978, 2008.
13. Choi CS, Savage DB, Abu-Elheiga L, Liu ZX, Kim S, Kulkarni A, Distefano A, Hwang YJ, Reznick RM, Codella R, Zhang D, Cline GW, Wakil SJ, Shulman GI. Continuous fat oxidation in acetyl-CoA carboxylase 2 knockout mice increases total energy expenditure, reduces fat mass, and improves insulin sensitivity. Proc Natl Acad Sci USA 104: 16480-16485, 2007.
14. DeFronzo RA. Lilly lecture 1987. The triumvirate: beta-cell, muscle, liver. A collusion responsible for NIDDM. Diabetes 37: 667-687, 1988.
15. Des Rosiers C, Montgomery JA, Desrochers S, Garneau M, David F, Mamer OA, Brunengraber H. Interference of 3-hydroxyisobutyrate with measurements of ketone body concentration and isotopic enrichment by gas chromatography-mass spectrometry. Anal Biochem 173: 96-105, 1988.
16. Des Rosiers C, Montgomery JA, Garneau M, David F, Mamer OA, Daloze P, Toffolo G, Cobelli C, Landau BR, Brunengraber H. Pseudoketogenesis in hepatectomized dogs. Am J Physiol Endocrinol Metab 258: E519-E528, 1990.
17. Fink G, Desrochers S, Des Rosiers C, Garneau M, David F, Daloze T, Landau BR, Brunengraber H. Pseudoketogenesis in the perfused rat heart. J Biol Chem 263: 18036-18042, 1988.
18. Foster DW. Studies in the Ketosis of Fasting. J Clin Invest 46: 1283-1296, 1967.
19. Hachey DL, Patterson BW, Reeds PJ, Elsas LJ. Isotopic determination of organic keto acid pentafluorobenzyl esters in biological fluids by negative chemical ionization gas chromatography/mass spectrometry. Anal Chem 63: 919-923, 1991.
20. Keller U, Cherrington AD, Liljenquist JE. Ketone body turnover and net hepatic ketone production in fasted and diabetic dogs. Am J Physiol Endocrinol Metab Gastrointest Physiol 235: E238-E247, 1978.
21. Kelley DE, He J, Menshikova EV, Ritov VB. Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51: 2944-2950, 2002.
22. Kennedy EP, Lehninger AL. Oxidation of fatty acids and tricarboxylic acid cycle intermediates by isolated rat liver mitochondria. J Biol Chem 179: 957-972, 1949.
23. Kersten S, Seydoux J, Peters JM, Gonzalez FJ, Desvergne B, Wahli W. Peroxisome proliferator-activated receptor alpha mediates the adaptive response to fasting. J Clin Invest 103: 1489-1498, 1999.
24. Koves TR, Ussher JR, Noland RC, Slentz D, Mosedale M, Ilkayeva O, Bain J, Stevens R, Dyck JR, Newgard CB, Lopaschuk GD, Muoio DM. Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab 7: 45-56, 2008.
25. Lam TK, Yoshii H, Haber CA, Bogdanovic E, Lam L, Fantus IG, Giacca A. Free fatty acid-induced hepatic insulin resistance: a potential role for protein kinase C-δ. Am J Physiol Endocrinol Metab 283: E682-E691, 2002.
26. Lieber CS. Alcoholic fatty liver: its pathogenesis and mechanism of progression to inflammation and fibrosis. Alcohol 34: 9-19, 2004.
27. Matsuda M, DeFronzo RA. Insulin sensitivity indices obtained from oral glucose tolerance testing: comparison with the euglycemic insulin clamp. Diabetes Care 22: 1462-1470, 1999. (Pubitemid 29418240)
28. McGarry J. What if Minkowski had been ageusic? An alternative angle on diabetes. Science 258: 766-770, 1992.
29. McGarry JD. Banting lecture 2001: dysregulation of fatty acid metabolism in the etiology of type 2 diabetes. Diabetes 51: 7-18, 2002.
30. McGarry JD, Foster DW. Regulation of hepatic fatty acid oxidation and ketone body production. Annu Rev Biochem 49: 395-420, 1980.
31. Miles JM, Schwenk WF, McClean KL, Haymond MW. A dual-isotope technique for determination of in vivo ketone body kinetics. Am J Physiol Endocrinol Metab 251: E185-E191, 1986.
32. Millington DS, Kodo N, Norwood DL, Roe CR. Tandem mass spectrometry: a new method for acylcarnitine profiling with potential for neonatal screening for inborn errors of metabolism. J Inherit Metab Dis 13: 321-324, 1990. (Pubitemid 20338872)
33. Moreau NM, Goupry SM, Antignac JP, Monteau FJ, Le Bizec BJ, Champ MM, Martin LJ, Dumon HJ. Simultaneous measurement of plasma concentrations and 13C-enrichment of short-chain fatty acids, lactic acid and ketone bodies by gas chromatography coupled to mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 784: 395-403, 2003.
34. Muoio DM, Newgard CB. Mechanisms of disease: molecular and metabolic mechanisms of insulin resistance and beta-cell failure in type 2 diabetes. Nat Rev Mol Cell Biol 9: 193-205, 2008.
35. Neufeld HA, Pace JG, Kaminski MV, George DT, Jahrling PB, Wannemacher RW Jr, Beisel WR. A probable endocrine basis for the depression of ketone bodies during infectious or inflammatory state in rats. Endocrinology 107: 596-601, 1980.
36. Noland RC, Koves TR, Seiler SE, Lum H, Lust RM, Ilkayeva O, Stevens RD, Hegardt FG, Muoio DM. Carnitine insufficiency caused by aging and overnutrition compromises mitochondrial performance and metabolic control. J Biol Chem 284: 22840-22852, 2009.
37. Owen OE, Reichard GA Jr, Markus H, Boden G, Mozzoli MA, Shuman CR. Rapid intravenous sodium acetoacetate infusion in man. Metabolic and kinetic responses. J Clin Invest 52: 2606-2616, 1973.
38. Parekh PI, Petro AE, Tiller JM, Feinglos MN, Surwit RS. Reversal of diet-induced obesity and diabetes in C57BL/6J mice. Metabolism 47: 1089-1096, 1998.
39. Pérez-Carreras M, Del Hoyo P, Martín MA, Rubio JC, Martín A, Castellano G, Colina F, Arenas J, Solis-Herruzo JA. Defective hepatic mitochondrial respiratory chain in patients with nonalcoholic steatohepatitis. Hepatology 38: 999-1007, 2003. (Pubitemid 37221683)
40. Petersen KF, Dufour S, Befroy D, Garcia R, Shulman GI. Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med 350: 664-671, 2004. (Pubitemid 38364625)
41. Petersen KF, Shulman GI. Etiology of insulin resistance. Am J Med 119, 5 Suppl 1: S10-S16, 2006.
42. Potthoff MJ, Inagaki T, Satapati S, Ding X, He T, Goetz R, Mohammadi M, Finck BN, Mangelsdorf DJ, Kliewer SA, Burgess SC. FGF21 induces PGC-1alpha and regulates carbohydrate and fatty acid metabolism during the adaptive starvation response. Proc Natl Acad Sci USA 106: 10853-10858, 2009.
43. Riou JP, Beylot M, Laville M, De Parscau L, Delinger J, Sautot G, Mornex R. Antiketogenic effect of glucose per se in vivo in man and in vitro in isolated rat liver cells. Metabolism 35: 608-613, 1986.
44. Samuel VT, Liu ZX, Qu X, Elder BD, Bilz S, Befroy D, Romanelli AJ, Shulman GI. Mechanism of hepatic insulin resistance in non-alcoholic fatty liver disease. J Biol Chem 279: 32345-32353, 2004. (Pubitemid 39014687)
45. Sanyal AJ, Campbell-Sargent C, Mirshahi F, Rizzo WB, Contos MJ, Sterling RK, Luketic VA, Shiffman ML, Clore JN. Nonalcoholic steatohepatitis: association of insulin resistance and mitochondrial abnormalities. Gastroenterology 120: 1183-1192, 2001.
46. Satapati S, He T, Inagaki T, Potthoff M, Merritt ME, Esser V, Mangelsdorf DJ, Kliewer SA, Browning JD, Burgess SC. Partial resistance to peroxisome proliferator-activated receptor-alpha agonists in ZDF rats is associated with defective hepatic mitochondrial metabolism. Diabetes 57: 2012-2021, 2008.
47. Shulman GI. Cellular mechanisms of insulin resistance. J Clin Invest 106: 171-176, 2000.
48. Sparks LM, Xie H, Koza RA, Mynatt R, Hulver MW, Bray GA, Smith SR. A high-fat diet coordinately downregulates genes required for mitochondrial oxidative phosphorylation in skeletal muscle. Diabetes 54: 1926-1933, 2005.
49. Stanley CA. New genetic defects in mitochondrial fatty acid oxidation and carnitine deficiency. Adv Pediatr 34: 59-88, 1987.
50. Steele R, Winkler B, Rathgeb I, Bjerknes C, Altszuler N. Plasma glucose and free fatty acid metabolism in normal and long-fasted dogs. Am J Physiol 214: 313-319, 1968.
51. Szendroedi J, Chmelik M, Schmid AI, Nowotny P, Brehm A, Krssak M, Moser E, Roden M. Abnormal hepatic energy homeostasis in type 2 diabetes. Hepatology 50: 1079-1086, 2009.
52. Triscari J, Greenwood MR, Sullivan AC. Oxidation and ketogenesis in hepatocytes of lean and obese Zucker rats. Metabolism 31: 223-228, 1982.
53. Wright JJ, Kim J, Buchanan J, Boudina S, Sena S, Bakirtzi K, Ilkun O, Theobald HA, Cooksey RC, Kandror KV, Abel ED. Mechanisms for increased myocardial fatty acid utilization following short-term high-fat feeding. Cardiovasc Res 82: 351-360, 2009.
54. Ye JM, Doyle PJ, Iglesias MA, Watson DG, Cooney GJ, Kraegen EW. Peroxisome proliferator-activated receptor (PPAR)-alpha activation lowers muscle lipids and improves insulin sensitivity in high fat-fed rats: comparison with PPAR-gamma activation. Diabetes 50: 411-417, 2001.
55. Zhang D, Liu ZX, Choi CS, Tian L, Kibbey R, Dong J, Cline GW, Wood PA, Shulman GI. Mitochondrial dysfunction due to long-chain Acyl-CoA dehydrogenase deficiency causes hepatic steatosis and hepatic insulin resistance. Proc Natl Acad Sci USA 104: 17075-17080, 2007. (Pubitemid 350210994)