OXPHOS-mediated induction of NAD+ promotes complete oxidation of fatty acids and interdicts non-alcoholic fatty liver disease

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Akie, Thomas E ^a   Liu, Lijun ^a   Nam, Minwoo ^a   Lei, Shi ^a   Cooper, Marcus P ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CITRATE SYNTHASE; CYCLOOXYGENASE 1; GLUTAMATE SYNTHASE (NADH); LEUCINE RICH PENTATRICOPEPTIDE REPEAT CONTAINING; MITOCHONDRIAL DNA; NICOTINAMIDE ADENINE DINUCLEOTIDE; PROTEIN KINASE C EPSILON; REACTIVE OXYGEN METABOLITE; SIRTUIN 3; SUPEROXIDE; UNCLASSIFIED DRUG; FATTY ACID; LRPPRC PROTEIN, MOUSE; PRKCE PROTEIN, MOUSE; SIRT3 PROTEIN, MOUSE; TUMOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUGMENTATION INDEX; CELL DENSITY; CELL RESPIRATION; CONTROLLED STUDY; CRISTAE; DISEASE ASSOCIATION; ENDOPLASMIC RETICULUM STRESS; ENERGY BALANCE; ENERGY EXPENDITURE; ENZYME ACTIVITY; FATTY ACID OXIDATION; FGF21 GENE; GENE; GENE EXPRESSION; HOMOZYGOSITY; HUMAN; HUMAN CELL; IL6 GENE; INFLAMMATION; INSULIN RESISTANCE; INSULIN SENSITIVITY; IRISIN GENE; LIPID HOMEOSTASIS; LIPID STORAGE; LIVER CELL; LIVER MITOCHONDRION; LIVER PROTECTION; LRPPRC GENE; MALE; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; PHENOTYPE; POLRMT GENE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIRT3 GENE; TFAM GENE; TFB2M GENE; ANIMAL; C57BL MOUSE; DEFICIENCY; GENE EXPRESSION REGULATION; GENETICS; LIPID DIET; LIPID METABOLISM; LIVER; METABOLISM; MITOCHONDRION; NON-ALCOHOLIC FATTY LIVER DISEASE; OXIDATION REDUCTION REACTION; PATHOLOGY; PRIMARY CELL CULTURE; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ANIMALS; DIET, HIGH-FAT; FATTY ACIDS; GENE EXPRESSION REGULATION; HEPATOCYTES; HUMANS; INSULIN RESISTANCE; LIPID METABOLISM; LIVER; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MITOCHONDRIA; NAD; NEOPLASM PROTEINS; NON-ALCOHOLIC FATTY LIVER DISEASE; OXIDATION-REDUCTION; OXIDATIVE PHOSPHORYLATION; PRIMARY CELL CULTURE; PROTEIN KINASE C-EPSILON; SIGNAL TRANSDUCTION; SIRTUIN 3;

EID: 84928799067     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0125617     Document Type: Article

References (48)

1. Bellentani S, Scaglioni F, Marino M, Bedogni G. Epidemiology of non-alcoholic fatty liver disease. Dig Dis. 2010; 28(1):155-61. doi: 000282080 [pii]; doi: 10.1159/000282080 PMID: 20460905
2. Angulo P. Nonalcoholic fatty liver disease. N Engl J Med. 2002 Apr 18; 346(16):1221-31. doi: 10.1056/NEJMra011775 [doi];346/16/1221 [pii]. PMID: 11961152
3. Adams LA, Lymp JF, St SJ, Sanderson SO, Lindor KD, Feldstein A, et al. The natural history of nonalcoholic fatty liver disease: a population-based cohort study. Gastroenterology. 2005 Jul; 129(1):113-21. doi: S0016508505006943 [pii]. PMID: 16012941
4. White DL, Kanwal F, El-Serag HB. Association between nonalcoholic fatty liver disease and risk for hepatocellular cancer, based on systematic review. Clin Gastroenterol Hepatol. 2012 Dec; 10(12):1342-59. doi: S1542-3565(12)01153-6 [pii]; doi: 10.1016/j.cgh.2012.10.001 PMID: PMC3501546.
5. Bellentani S, Saccoccio G, Masutti F, Croce LS, Brandi G, Sasso F, et al. Prevalence of and risk factors for hepatic steatosis in Northern Italy. Ann Intern Med. 2000 Jan 18; 132(2):112-7. doi: 200001180-00004 [pii]. PMID: 10644271
6. Browning JD, Szczepaniak LS, Dobbins R, Nuremberg P, Horton JD, Cohen JC, et al. Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology. 2004 Dec; 40(6):1387-95. doi: 10.1002/hep.20466 PMID: 15565570
7. Michael MD, Kulkarni RN, Postic C, Previs SF, Shulman GI, Magnuson MA, et al. Loss of insulin signaling in hepatocytes leads to severe insulin resistance and progressive hepatic dysfunction. Mol Cell. 2000 Jul; 6(1):87-97. doi: S1097-2765(05)00015-8 [pii]. PMID: 10949030
8. Perez-Carreras M, Del HP, Martin MA, Rubio JC, Martin A, Castellano G, et al. Defective hepatic mitochondrial respiratory chain in patients with nonalcoholic steatohepatitis. Hepatology. 2003 Oct; 38(4):999-1007. doi: 10.1053/jhep.2003.50398 [doi];S0270913903007031 [pii]. PMID: 14512887
9. Cortez-Pinto H, Chatham J, Chacko VP, Arnold C, Rashid A, Diehl AM. Alterations in liver ATP homeostasis in human nonalcoholic steatohepatitis: a pilot study. JAMA. 1999 Nov 3; 282(17):1659-64. doi: jpc90051 [pii]. PMID: 10553793
10. Sanyal AJ, Campbell-Sargent C, Mirshahi F, Rizzo WB, Contos MJ, Sterling RK, et al. Nonalcoholic steatohepatitis: association of insulin resistance and mitochondrial abnormalities. Gastroenterology. 2001 Apr; 120(5):1183-92. doi: 10.1053/gast.2001.23256 [doi];S0016508501007491 [pii]. PMID: 11266382
11. Caldwell SH, Swerdlow RH, Khan EM, Iezzoni JC, Hespenheide EE, Parks JK, et al. Mitochondrial abnormalities in non-alcoholic steatohepatitis. J Hepatol. 1999 Sep; 31(3):430-4. doi: S0168-8278(99)80033-6 [pii]. PMID: 10488700
12. Seki S, Kitada T, Yamada T, Sakaguchi H, Nakatani K, Wakasa K. In situ detection of lipid peroxidation and oxidative DNA damage in non-alcoholic fatty liver diseases. J Hepatol. 2002 Jul; 37(1):56-62. doi: S0168827802000739 [pii]. PMID: 12076862
13. Kumashiro N, Erion DM, Zhang D, Kahn M, Beddow SA, Chu X, et al. Cellular mechanism of insulin resistance in nonalcoholic fatty liver disease. Proc Natl Acad Sci U S A. 2011 Sep 27; 108(39):16381-5. doi: 1113359108 [pii]; doi: 10.1073/pnas.1113359108 PMID: 21930939
14. Kim HJ, Kim JH, Noh S, Hur HJ, Sung MJ, Hwang JT, et al. Metabolomic analysis of livers and serum from high-fat diet induced obese mice. J Proteome Res. 2011 Feb 4; 10(2):722-31. doi: 10.1021/pr100892r PMID: 21047143
15. Kendrick AA, Choudhury M, Rahman SM, McCurdy CE, Friederich M, Vanhove JL, et al. Fatty liver is associated with reduced SIRT3 activity and mitochondrial protein hyperacetylation. Biochem J. 2010 Nov 2; doi: BJ20100791 [pii]; doi: 10.1042/BJ20100791
16. Mootha VK, Lepage P, Miller K, Bunkenborg J, Reich M, Hjerrild M, et al. Identification of a gene causing human cytochrome c oxidase deficiency by integrative genomics. Proc Natl Acad Sci U S A. 2003 Jan 21; 100(2):605-10. doi: 10.1073/pnas.242716699 [doi];242716699 [pii]. PMID: PMC141043.
17. Cooper MP, Qu L, Rohas LM, Lin J, Yang W, Erdjument-Bromage H, et al. Defects in energy homeostasis in Leigh syndrome French Canadian variant through PGC-1alpha/LRP130 complex. Genes Dev. 2006 Nov 1; 20(21):2996-3009. doi: gad.1483906 [pii]; doi: 10.1101/gad.1483906 PMID: PMC1620022.
18. Liu L, Sanosaka M, Lei S, Bestwick ML, Frey JH Jr., Surovtseva YV, et al. LRP130 protein remodels mitochondria and stimulates fatty acid oxidation. J Biol Chem. 2011 Dec 2; 286(48):41253-64. doi: M111.276121 [pii]; doi: 10.1074/jbc.M111.276121 PMID: 21971050
19. Liu L, Nam M, Fan W, Akie TE, Hoaglin DC, Gao G, et al. Nutrient sensing by the mitochondrial transcription machinery dictates oxidative phosphorylation. J Clin Invest. 2014 Feb 3; 124(2):768-84. doi: 69413 [pii]; doi: 10.1172/JCI69413 PMID: 24430182
20. Sondheimer N, Fang JK, Polyak E, Falk M, Avadhani NG. The Leucine-rich Pentatricopeptide-Repeat Containing Protein Regulates Mitochondrial Transcription. Biochemistry. 2010 Aug 2; doi: 10.1021/bi1008479
21. Mourier A, Ruzzenente B, Brandt T, Kuhlbrandt W, Larsson NG. Loss of LRPPRC causes ATP synthase deficiency. Hum Mol Genet. 2014 May 15; 23(10):2580-92. doi: ddt652 [pii]; doi: 10.1093/hmg/ddt652 PMID: PMC3990160.
22. Ruzzenente B, Metodiev MD, Wredenberg A, Bratic A, Park CB, Camara Y, et al. LRPPRC is necessary for polyadenylation and coordination of translation of mitochondrial mRNAs. EMBO J. 2012 Jan 18; 31(2):443-56. doi: emboj2011392 [pii]; doi: 10.1038/emboj.2011.392 PMID: PMC3261557.
23. Gohil VM, Nilsson R, Belcher-Timme CA, Luo B, Root DE, Mootha VK. Mitochondrial and nuclear genomic responses to loss of lrpprc expression. J Biol Chem. 2010 Mar 10; doi: M109.098400 [pii]; doi: 10.1074/jbc.M109.098400
24. Sasarman F, Brunel-Guitton C, Antonicka H, Wai T, Shoubridge EA, Consortium L. LRPPRC and SLIRP Interact in a Ribonucleoprotein Complex that Regulates Posttranscriptional Gene Expression in Mitochondria. Mol Biol Cell. 2010 Mar 3; doi: E10-01-0047 [pii]; doi: 10.1091/mbc.E10-01-0047
25. Kleiner DE, Brunt EM, Van NM, Behling C, Contos MJ, Cummings OW, et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology. 2005 Jun; 41(6):1313-21. doi: 10.1002/hep.20701 PMID: 15915461
26. Frezza C, Cipolat S, Scorrano L. Organelle isolation: functional mitochondria from mouse liver, muscle and cultured fibroblasts. Nat Protoc. 2007; 2(2):287-95. doi: nprot.2006.478 [pii]; doi: 10.1038/nprot.2006.478 PMID: 17406588
27. Goncalves LA, Vigario AM, Penha-Goncalves C. Improved isolation of murine hepatocytes for in vitro malaria liver stage studies. Malar J. 2007; 6:169. doi: 1475-2875-6-169 [pii]; doi: 10.1186/1475-2875-6-169 PMID: PMC2244635.
28. Qu X, Seale JP, Donnelly R. Tissue and isoform-selective activation of protein kinase C in insulin-resistant obese Zucker rats - effects of feeding. J Endocrinol. 1999 Aug; 162(2):207-14. doi: JOE3274 [pii]. PMID: 10425458
29. Korshunov SS, Skulachev VP, Starkov AA. High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett. 1997 Oct 13; 416(1):15-8. doi: S0014-5793(97)01159-9 [pii]. PMID: 9369223
30. Mourier A, Ruzzenente B, Brandt T, Kuhlbrandt W, Larsson NG. Loss of LRPPRC causes ATP synthase deficiency. Hum Mol Genet. 2014 May 15; 23(10):2580-92. doi: ddt652 [pii]; doi: 10.1093/hmg/ddt652 PMID: PMC3990160.
31. Samuel VT, Liu ZX, Wang A, Beddow SA, Geisler JG, Kahn M, et al. Inhibition of protein kinase Cepsilon prevents hepatic insulin resistance in nonalcoholic fatty liver disease. J Clin Invest. 2007 Mar; 117(3):739-45. doi: 10.1172/JCI30400 PMID: PMC1797607.
32. Jornayvaz FR, Shulman GI. Diacylglycerol activation of protein kinase Cepsilon and hepatic insulin resistance. Cell Metab. 2012 May 2; 15(5):574-84. doi: S1550-4131(12)00100-3 [pii]; doi: 10.1016/j.cmet.2012.03.005 PMID: PMC3353749.
33. Jornayvaz FR, Birkenfeld AL, Jurczak MJ, Kanda S, Guigni BA, Jiang DC, et al. Hepatic insulin resistance in mice with hepatic overexpression of diacylglycerol acyltransferase 2. Proc Natl Acad Sci U S A. 2011 Apr 5; 108(14):5748-52. doi: 1103451108 [pii]; doi: 10.1073/pnas.1103451108 PMID: PMC3078388.
34. Bellafante E, Murzilli S, Salvatore L, Latorre D, Villani G, Moschetta A. Hepatic-specific activation of peroxisome proliferator-activated receptor gamma coactivator-1beta protects against steatohepatitis. Hepatology. 2013 Apr; 57(4):1343-56. doi: 10.1002/hep.26222 PMID: 23299802
35. Lelliott CJ, Ljungberg A, Ahnmark A, William-Olsson L, Ekroos K, Elmgren A, et al. Hepatic PGC-1beta overexpression induces combined hyperlipidemia and modulates the response to PPARalpha activation. Arterioscler Thromb Vasc Biol. 2007 Dec; 27(12):2707-13. doi: ATVBAHA.107.155739 [pii]; doi: 10.1161/ATVBAHA.107.155739 PMID: 17932310
36. Donnelly KL, Smith CI, Schwarzenberg SJ, Jessurun J, Boldt MD, Parks EJ. Sources of fatty acids stored in liver and secreted via lipoproteins in patients with nonalcoholic fatty liver disease. J Clin Invest. 2005 May; 115(5):1343-51. doi: 10.1172/JCI23621 PMID: PMC1087172.
37. Chakravarthy MV, Pan Z, Zhu Y, Tordjman K, Schneider JG, Coleman T, et al. "New" hepatic fat activates PPARalpha to maintain glucose, lipid, and cholesterol homeostasis. Cell Metab. 2005 May; 1(5):309-22. doi: S1550-4131(05)00110-5 [pii]; doi: 10.1016/j.cmet.2005.04.002 PMID: 16054078
38. Merante F, Petrova-Benedict R, MacKay N, Mitchell G, Lambert M, Morin C, et al. A biochemically distinct form of cytochrome oxidase (COX) deficiency in the Saguenay-Lac-Saint-Jean region of Quebec. Am J Hum Genet. 1993 Aug; 53(2):481-7. PMID: PMC1682348.
39. Morin C, Mitchell G, Larochelle J, Lambert M, Ogier H, Robinson BH, et al. Clinical, metabolic, and genetic aspects of cytochrome C oxidase deficiency in Saguenay-Lac-Saint-Jean. Am J Hum Genet. 1993 Aug; 53(2):488-96. PMID: PMC1682365.
40. Eaton S, Pourfarzam M, Bartlett K. The effect of respiratory chain impairment of beta-oxidation in rat heart mitochondria. Biochem J. 1996 Oct 15; 319 (Pt 2):633-40. PMID: PMC1217814.
41. Noguchi Y, Young JD, Aleman JO, Hansen ME, Kelleher JK, Stephanopoulos G. Effect of anaplerotic fluxes and amino acid availability on hepatic lipoapoptosis. J Biol Chem. 2009 Nov 27; 284(48):33425-36. doi: M109.049478 [pii]; doi: 10.1074/jbc.M109.049478 PMID: PMC2785187.
42. Hirschey MD, Shimazu T, Goetzman E, Jing E, Schwer B, Lombard DB, et al. SIRT3 regulates mitochondrial fatty-acid oxidation by reversible enzyme deacetylation. Nature. 2010 Mar 4; 464(7285):121-5. doi: nature08778 [pii]; doi: 10.1038/nature08778 PMID: PMC2841477.
43. Karamanlidis G, Lee CF, Garcia-Menendez L, Kolwicz SC Jr., Suthammarak W, Gong G, et al. Mitochondrial complex I deficiency increases protein acetylation and accelerates heart failure. Cell Metab. 2013 Aug 6; 18(2):239-50. doi: S1550-4131(13)00291-X [pii]; doi: 10.1016/j.cmet.2013.07.002 PMID: PMC3779647.
44. Perry RJ, Kim T, Zhang XM, Lee HY, Pesta D, Popov VB, et al. Reversal of hypertriglyceridemia, fatty liver disease, and insulin resistance by a liver-targeted mitochondrial uncoupler. Cell Metab. 2013 Nov 5; 18(5):740-8. doi: S1550-4131(13)00416-6 [pii]; doi: 10.1016/j.cmet.2013.10.004 PMID: 24206666
45. Samuel VT, Liu ZX, Qu X, Elder BD, Bilz S, Befroy D, et al. Mechanism of hepatic insulin resistance in non-alcoholic fatty liver disease. J Biol Chem. 2004 Jul 30; 279(31):32345-53. doi: 10.1074/jbc.M313478200 [doi];M313478200 [pii]. PMID: 15166226
46. Ganji SH, Kukes GD, Lambrecht N, Kashyap ML, Kamanna VS. Therapeutic role of niacin in the prevention and regression of hepatic steatosis in rat model of nonalcoholic fatty liver disease. Am J Physiol Gastrointest Liver Physiol. 2014 Feb 15; 306(4):G320-G327. doi: ajpgi.00181.2013 [pii]; doi: 10.1152/ajpgi.00181.2013 PMID: 24356885
47. Canto C, Houtkooper RH, Pirinen E, Youn DY, Oosterveer MH, Cen Y, et al. The NAD(+) precursor nicotinamide riboside enhances oxidative metabolism and protects against high-fat diet-induced obesity. Cell Metab. 2012 Jun 6; 15(6):838-47. doi: S1550-4131(12)00192-1 [pii]; doi: 10.1016/j.cmet.2012.04.022 PMID: PMC3616313.
48. Pospisilik JA, Knauf C, Joza N, Benit P, Orthofer M, Cani PD, et al. Targeted deletion of AIF decreases mitochondrial oxidative phosphorylation and protects from obesity and diabetes. Cell. 2007 Nov 2; 131(3):476-91. doi: S0092-8674(07)01197-X [pii]; doi: 10.1016/j.cell.2007.08.047 PMID: 17981116