Abstract
The Membrane Theory of Aging proposes that lifespan is inversely related to the level of unsaturation in membrane phospholipids. Calorie restriction (CR) without malnutrition extends lifespan in many model organisms, which may be related to alterations in membrane phospholipids fatty acids. During the last few years our research focused on studying how altering the predominant fat source affects the outcome of CR in mice. We have established four dietary groups: one control group fed 95 % of a pre-determined ad libitum intake (in order to prevent obesity), and three CR groups fed 40 % less than ad libitum intake. Lipid source for the control and one of the CR groups was soybean oil (high in n-6 PUFA) whereas the two remaining CR groups were fed diets containing fish oil (high in n-3 PUFA), or lard (high in saturated and monounsaturated fatty acids). Dietary intervention periods ranged from 1 to 18 months. We performed a longitudinal lifespan study and a cross-sectional study set up to evaluate several mitochondrial parameters which included fatty acid composition, H+ leak, activities of electron transport chain enzymes, ROS generation, lipid peroxidation, mitochondrial ultrastructure, and mitochondrial apoptotic signaling in liver and skeletal muscle. These approaches applied to different cohorts of mice have independently indicated that lard as a fat source often maximizes the effects of 40 % CR on mice. These effects could be due to significant increases of monounsaturated fatty acids levels, in accordance with the Membrane Theory of Aging.
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Adams JM, Cory S (2007) The Bcl-2 apoptotic switch in cancer development and therapy. Oncogene 26:1324–1337. doi:10.1038/sj.onc.1210220
Agarwal B, Baur JA (2011) Resveratrol and life extension. Ann N Y Acad Sci 1215:138–143. doi:10.1111/j.1749-6632.2010.05850.x
Asami DK, McDonald RB, Hagopian K, Horwitz BA, Warman D, Hsiao A, Warden C (2008) Ramsey JJ (2008) Effect of aging, caloric restriction, and uncoupling protein 3 (UCP3) on mitochondrial proton leak in mice. Exp Gerontol 43(12):1069–1076. doi:10.1016/j.exger.2008.09.010
Baillie RA, Takada R, Nakamura M, Clarke SD (1999) Coordinate induction of peroxisomal acyl-CoA oxidase and UCP-3 by dietary fish oil: a mechanism for decreased body fat deposition. Prostaglandins Leukot Essent Fatty Acids 60:351–356. doi:10.1016/S0952-3278(99)80011-8
Barja G (2013) Updating the mitochondrial free radical theory of aging: an integrated view, key aspects, and confounding concepts. Antioxid Redox Signal 20:1420–1445. doi:10.1089/ars.2012.5148
Barja G (2014) The mitochondrial free radical theory of aging. Prog Mol Biol Transl Sci 127:1–27. doi:10.1016/B978-0-12-394625-6.00001-5
Barzanti V, Battino M, Baracca A, Cavazzoni M, Cocchi M, Noble R, Maranesi M, Turchetto E, Lenaz G (1994) The effect of dietary lipid changes on the fatty acid composition and function of liver, heart and brain mitochondria in the rat at different ages. Br J Nutr 71:193–202. doi:http://dx.doi.org/10.1079/BJN19940126
Baur JA, Pearson KJ, Price NL, Jamieson HA, Lerin C, Kalra A, Prabhu VV, Allard JS, Lopez-Lluch G, Lewis K, Pistell PJ, Poosala S, Becker KG, Boss O, Gwinn D, Wang M, Ramaswamy S, Fishbein KW, Spencer RG, Lakatta EG, Le Couteur D, Shaw RJ, Navas P, Puigserver P, Ingram DK, de Cabo R, Sinclair DA (2006) Resveratrol improves health and survival of mice on a high-calorie diet. Nature 444:337–342. doi:10.1038/nature05354
Berdanier CD, Johnson B, Hartle DK, Crowell W (1992) Life span is shortened in BHE/cdb rats fed a diet containing 9% menhaden oil and 1% corn oil. J Nutr 122:1309–1317
Bevilacqua L, Ramsey JJ, Hagopian K, Weindruch R, Harper ME (2004) Effects of short- and medium-term calorie restriction on muscle mitochondrial proton leak and reactive oxygen species production. Am J Physiol Endocrinol Metab 286:E852–E861. doi:10.1152/ajpendo.00367.2003
Bevilacqua L, Ramsey JJ, Hagopian K, Weindruch R, Harper ME (2005) Long-term caloric restriction increases UCP3 content but decreases proton leak and reactive oxygen species production in rat skeletal muscle mitochondria. Am J Physiol Endocrinol Metab 289:E429–E438. doi:10.1152/ajpendo.00435.2004
Brand MD, Couture P, Hulbert AJ (1994) Liposomes from mammalian liver mitochondria are more polyunsaturated and leakier to protons than those from reptiles. Comp Biochem Physiol Biochem Mol Biol 108:181–188. doi:10.1016/0305-0491(94)90064-7
Bronnikov GE, Kulagina TP, Aripovsky AV (2010) Dietary supplementation of old rats with hydrogenated peanut oil restores activities of mitochondrial respiratory complexes in skeletal muscles. Biochemistry (Mosc) 75:1491–1497. doi:10.1134/S0006297910120102
Brookes PS (2005) Mitochondrial H(+) leak and ROS generation: an odd couple. Free Radic Biol Med 38:12–23. doi:10.1016/j.freeradbiomed.2004.10.016
Brookes PS, Rolfe DF, Brand MD (1997) The proton permeability of liposomes made from mitochondrial inner membrane phospholipids: comparison with isolated mitochondria. J Membre Biol 155:167–174. doi:10.1007/s002329900168
Brookes PS, Buckingham JA, Tenreiro AM, Hulbert AJ, Brand MD (1998) The proton permeability of the inner membrane of liver mitochondria from ectothermic and endothermic vertebrates and from obese rats: correlations with standard metabolic rate and phospholipid fatty acid composition. Comp Biochem Physiol B: Biochem Mol Biol 119:325–334. doi:10.1016/S0305-0491(97)00357-X
Bruss MD, Khambatta CF, Ruby MA, Aggarwal I, Hellerstein MK (2009) Calorie restriction increases fatty acid synthesis and whole body fat oxidation rates. Am J Physiol Endocrinol Metab 298:E108–E116. doi:10.1152/ajpendo.00524.2009
Calder PC (2004) N-3 polyunsaturated fatty acids and inflammation: from molecular biology to the clinic. Lipids 38:343–352. doi:10.1007/s11745-003-1068-y
Calder PC (2007) Immunomodulation by omega-3 fatty acids. Prostaglandins Leukot Essent Fatty Acids 77:327–335. doi:10.1016/j.plefa.2007.10.015
Calder PC (2012) Mechanisms of action of (n-3) fatty acids. J Nutr 142:592S–599S. doi:10.3945/jn.111.155259
Cava E, Fontana L (2013) Will calorie restriction work in humans? Aging (Albany NY) 5:507–514
Cha MC, Jones PJ (2000) Energy restriction dilutes the changes related to dietary fat type in membrane phospholipid fatty acid composition in rats. Metabolism 49:977–983. doi:10.1053/meta.2000.7725
Chen BK, Seligman B, Farquhar JW, Goldhaber-Fiebert JD (2011) Multi-Country analysis of palm oil consumption and cardiovascular disease mortality for countries at different stages of economic development: 1980–1997. Global Health 7:45. doi:10.1186/1744-8603-7-45
Chen Y, Hagopian K, McDonald RB, Bibus D, López-Lluch G, Villalba JM, Navas P, Ramsey JJ (2012) The influence of dietary lipid composition on skeletal muscle mitochondria from mice following 1 month of calorie restriction. J Gerontol A Biol Sci Med Sci 67:1121–1131. doi:10.1093/gerona/gls113
Chen Y, Hagopian K, Bibus D, Villalba JM, López-Lluch G, Navas P, Kim K, McDonald RB, Ramsey JJ (2013) The influence of dietary lipid composition on liver mitochondria from mice following 1 month of calorie restriction. Biosci Rep 33:83–95. doi:10.1042/BSR20120060
Chen Y, Hagopian K, Bibus D, Villalba JM, López-Lluch G, Navas P, Kim K, Ramsey JJ (2014) The influence of dietary lipid composition on skeletal muscle mitochondria from mice following eight months of calorie restriction. Physiol Res 63:57–71
Chung L, Ng Y-C (2006) Age-related alterations in expression of apoptosis regulatory proteins and heat shock proteins in rat skeletal muscle. Biochim Biophys Acta 1762:103–109. doi:10.1016/j.bbadis.2005.08.003
Chung HY, Kim HJ, Kim JW, Yu BP (2001) The inflammation hypothesis of aging: molecular modulation by calorie restriction. Ann N Y Acad Sci 928:327–335. doi:10.1111/j.1749-6632.2001.tb05662.x
Civitarese AE, Carling S, Heilbronn LK, Hulver MH, Ukropcova B, Deutsch WA, Smith SR, Ravussin E, Pennington Team CALERIE (2007) Calorie restriction increases muscle mitochondrial biogenesis in healthy humans. PLoS Med 4(3):e76. doi:10.1371/journal.pmed.0040076
Colman RJ, Anderson RM, Johnson SC, Kastman EK, Kosmatka KJ, Beasley TM, Allison DB, Cruzen C, Simmons HA, Kemnitz JW, Weindruch R (2009) Caloric restriction delays disease onset and mortality in rhesus monkeys. Science 325:201–204. doi:10.1126/science.1173635
Colman RJ, Beasley TM, Kemnitz JW, Johnson SC, Weindruch R, Anderson RM (2014) Caloric restriction reduces age-related and all-cause mortality in rhesus monkeys. Nat Commun 5:3557. doi:10.1038/ncomms4557
Couet C, Delarue J, Ritz P, Antoine JM, Lamisse F (1997) Effect of dietary fish oil on body fat mass and basal fat oxidation in healthy adults. Int J Obes Relat Metab Disord 21:637–643. doi:10.1038/sj.ijo.0800451
Crockett EL (2008) The cold but not hard fats in ectotherms: consequences of lipid restructuring on susceptibility of biological membranes to peroxidation, a review. J Comp Physiol B 178:795–809. doi:10.1007/s00360-008-0275-7
Daum G (1985) Lipids of mitochondria. Biochim Biophys Acta 822:1–42
Deckelbaum RJ, Torrejon C (2012) The omega-3 fatty acid nutritional landscape: health benefits and sources. J Nutr 142:587S–5591S. doi:10.3945/jn.111.148080
Desai VG, Weindruch R, Hart RW, Feuers RJ (1996) Influences of age and dietary restriction on gastrocnemius electron transport system activities in mice. Arch Biochem Biophys 1333:145–151. doi:10.1006/abbi.1996.0375
Dirks A, Leeuwenburgh C (2002) Apoptosis in skeletal muscle with aging. Am J Physiol Regul Integr Comp Physiol 282:R519–R527. doi:10.1152/ajpregu.00458.2001
Dirks AJ, Leeuwenburgh C (2004) Aging and lifelong calorie restriction result in adaptations of skeletal muscle apoptosis repressors, apoptosis-inducing factor, X-linked inhibitor of apoptosis, caspase-3, and caspase-12. Free Radic Biol Med 36:27–39. doi:10.1016/j.freeradbiomed.2003.10.003
Dowhan W, Mileykovskaya E, Bogdanov M (2004) Diversity and versatility of lipid-protein interactions revealed by molecular genetic approaches. Biochim Biophys Acta 1666:19–39. doi:10.1016/j.bbamem.2004.04.010
Drew B, Phaneuf S, Dirks A, Selman C, Gredilla R, Lezza A, Barja G, Leeuwenburgh C (2003) Effects of aging and caloric restriction on mitochondrial energy production in gastrocnemius muscle and heart. Am J Physiol Regul Integr Comp Physiol 284:R474–R480. doi:10.1152/ajpregu.00455.2002
Evan G, Littlewood T (1998) A matter of life and cell death. Science 281:1317–1322. doi:10.1126/science.281.5381.1317
Faulks SC, Turner N, Else PL, Hulbert AJ (2006) Calorie restriction in mice: effects on body composition, daily activity, metabolic rate, mitochondrial reactive oxygen species production, and membrane fatty acid composition. J Gerontol A Biol Sci Med Sci 61:781–794
Flachs P, Horakova O, Brauner P, Rossmeisl M, Pecina P, Franssen-van Hal N, Ruzickova J, Sponarova J, Drahota Z, Vlcek C, Keijer J, Houstek J, Kopecky J (2005) Polyunsaturated fatty acids of marine origin upregulate mitochondrial biogenesis and induce beta-oxidation in white fat. Diabetologia 48:2365–2375. doi:10.1007/s00125-005-1944-7
Fontana L (2009) Neuroendocrine factors in the regulation of inflammation: excessive adiposity and calorie restriction. Exp Gerontol 44:41–45. doi:10.1016/j.exger.2008.04.005
Gómez J, Caro P, Naudí A, Portero-Otin M, Pamplona R, Barja G (2007) Effect of 8.5% and 25% caloric restriction on mitochondrial free radical production and oxidative stress in rat liver. Biogerontology 8:555–566. doi:10.1007/s10522-007-9099-1
Gómez A, Sánchez-Roman I, Gomez J, Cruces J, Mate I, Lopez-Torres M, Naudi A, Portero-Otin M, Pamplona R, De la Fuente M, Barja G (2014) Lifelong treatment with atenolol decreases membrane fatty acid unsaturation and oxidative stress in heart and skeletal muscle mitochondria and improves immunity and behavior, without changing mice longevity. Aging Cell 13:551–560. doi:10.1111/acel.12205
Gopinath B, Buyken AE, Flood VM, Empson M, Rochtchina E, Mitchell P (2011) Consumption of polyunsaturated fatty acids, fish, and nuts and risk of inflammatory disease mortality. Am J Clin Nutr 93:1073–1079. doi:10.3945/ajcn.110.009977
Gredilla R, Barja G (2005) Minireview: the role of oxidative stress in relation to caloric restriction and longevity. Endocrinology 146:3713–3717. doi:http://dx.doi.org/10.1210/en.2005-0378
Gredilla R, Barja G, López-Torres M (2001) Effect of short-term caloric restriction on H2O2 production and oxidative DNA damage in rat liver mitochondria and location of the free radical source. J Bioenerg Biomembr 33:279–287. doi:10.1023/A:1010603206190
Gredilla R, Phaneuf S, Selman C, Kendaiah S, Leeuwenburgh C, Barja G (2004) Short-term caloric restriction and sites of oxygen radical generation in kidney and skeletal muscle mitochondria. Ann N Y Acad Sci 1019:333–432. doi:10.1196/annals.1297.057
Hagen TM, Yowe DL, Bartholomew JC, Wehr CM, Do KL, Park JY, Ames BN (1997) Mitochondrial decay in hepatocytes from old rats: membrane potential declines, heterogeneity and oxidants increase. Proc Natl Acad Sci U S A 94:3064–3069
Hagopian K, Harper ME, Ram JJ, Humble SJ, Weindruch R, Ramsey JJ (2005) Long-term calorie restriction reduces proton leak and hydrogen peroxide production in liver mitochondria. Am J Physiol Endocrinol Metab 288:E674–E684. doi:10.1152/ajpendo.00382.2004
Hagopian K, Weber KL, Hwee DT, Van Eenennaam AL, López-Lluch G, Villalba JM, Burón I, Navas P, German JB, Watkins SM, Chen Y, Wei A, McDonald RB, Ramsey JJ (2010) Complex I-associated hydrogen peroxide production is decreased and electron transport chain enzyme activities are altered in n-3 enriched fat-1 mice. PLoS ONE 5(9):e12696. doi:10.1371/journal.pone.0012696
Halade GV, Rahman MM, Bhattacharya A, Barnes JL, Chandrasekar B, Fernandes G (2010) Docosahexaenoic acid-enriched fish oil attenuates kidney disease and prolongs median and maximal life span of autoimmune lupus-prone mice. J Immunol 184:5280–5286. doi:10.4049/jimmunol.0903282
Halminski MA, Marsh JB, Harrison EH (1991) Differential effects of fish oil, safflower oil and palm oil on fatty acid oxidation and glycerolipid synthesis in rat liver. J Nutr 121:1554–1561
Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144:646–674. doi:10.1016/j.cell.2011.02.013
Harman DJ (1956) Aging: a theory based on free radical and radiation chemistry. J Gerontol 11:298–300
Harper ME, Monemdjou S, Ramsey JJ, Weindruch R (1998) Age-related increase in mitochondrial proton leak and decrease in ATP turnover reactions in mouse hepatocytes. Am J Physiol 275:E197–E206
Hepple RT, Baker DJ, McConkey M, Murynka T, Norris R (2006) Caloric restriction protects mitochondrial function with aging in skeletal and cardiac muscles. Rejuvenation Res 9:219–222. doi:10.1089/rej.2006.9.219
Herrero A, Portero-Otín M, Bellmunt MJ, Pamplona R, Barja G (2001) Effect of the degree of fatty acid unsaturation of rat heart mitochondria on their rates of H2O2 production and lipid and protein oxidative damage. Mech Ageing Dev 122:427–443. doi:10.1016/S0047-6374(01)00214-7
Hill JO, Peters JC, Lin D, Yakubu F, Greene H, Swift L (1993) Lipid accumulation and body fat distribution is influenced by type of dietary fat fed to rats. Int J Obes Relat Metab Disord 17:223–236
Hong DD, Takahashi Y, Kushiro M, Ide T (2003) Divergent effects of eicosapentaenoic and docosahexaenoic acid ethyl esters, and fish oil on hepatic fatty acid oxidation in the rat. Biochim Biophys Acta 1635:29–36. doi:10.1016/j.bbalip.2003.10.003
Huertas JR, Martinez-Velasco E, Ibáñez S, López-Frias M, Ochoa JJ, Quiles J, Parenti Castelli G, Mataix J, Lenaz G (1999) Virgin olive oil and coenzyme Q10 protect heart mitochondria from peroxidative damage during aging. BioFactors 9:337–343
Hulbert AJ (2008) The links between membrane composition, metabolic rate and lifespan. Comp Biochem Physiol A: Mol Integr Physiol 150:196–203. doi:10.1016/j.cbpa.2006.05.014
Hulbert AJ, Pamplona R, Buffenstein R, Buttemer WA (2007) Life and death: metabolic rate, membrane composition, and life span of animals. Physiol Rev 87:1175–1213. doi:10.1152/physrev.00047.2006
Ide T, Kobayashi H, Ashakumary L, Rouyer IA, Takahashi Y, Aoyama T, Hashimoto T, Mizugaki M (2000) Comparative effects of perilla and fish oils on the activity and gene expression of fatty acid oxidation enzymes in rat liver. Biochim Biophys Acta 1485:23–35. doi:10.1016/S1388-1981(00)00026-3
Infante JP, Kirwan RC, Brenna JT (2001) High levels of docosahexaenoic acid (22:6n-3)-containing phospholipids in high-frequency contraction muscles of hummingbirds and rattlesnakes. Comp Biochem Physiol B: Biochem Mol Biol 130:291–298. doi:10.1016/S1096-4959(01)00443-2
Innis SM, Clandinin MT (1981) Dynamic modulation of mitochondrial membrane physical properties and ATPase activity by diet lipid. Biochem J 198:167–175
Jolly CA, Muthukumar A, Avula CP, Troyer D, Fernandes G (2001) Life span is prolonged in food-restricted autoimmune-prone (NZB x NZW)F(1) mice fed a diet enriched with (n-3) fatty acids. J Nutr 131:2753–2760
Jones PJ (1989) Effect of fatty acid composition of dietary fat on energy balance and expenditure in hamsters. Can J Physiol Pharmacol 67:994–998
Jové M, Naudí A, Ramírez-Núñez O, Portero-Otín M, Selman C, Withers DJ, Pamplona R (2014) Caloric restriction reveals a metabolomic and lipidomic signature in liver of male mice. Aging Cell 13:828–837. doi:10.1111/acel.12241
Jurk D, Wilson C, Passos JF, Oakley F, Correia-Melo C, Greaves L, Saretzki G, Fox C, Lawless C, Anderson R, Hewitt G, Pender SL, Fullard N, Nelson G, Mann J, van de Sluis B, Mann DA, von Zglinicki T (2014) Chronic inflammation induces telomere dysfunction and accelerates ageing in mice. Nat Commun 2:4172. doi:10.1038/ncomms5172
Kanzler S, Galle PR (2000) Apoptosis and the liver. Semin Cancer Biol 10:173–184. doi:10.1006/scbi.2000.0318
Khraiwesh H, López-Domínguez JA, López-Lluch G, Navas P, de Cabo R, Ramsey JJ, Villalba JM, González-Reyes JA (2013) Alterations of ultrastructural and fission/fusion markers in hepatocyte mitochondria from mice following calorie restriction with different dietary fats. J Gerontol A Biol Sci Med Sci 68:1023–1034. doi:10.1093/gerona/glt006
Khraiwesh H, López-Domínguez JA, Fernández del Río L, Gutierrez-Casado E, López-Lluch G, Navas P, de Cabo R, Ramsey JJ, Burón MI, Villalba JM, González-Reyes JA (2014) Mitochondrial ultrastructure and markers of dynamics in hepatocytes from aged, calorie restricted mice fed with different dietary fats. Exp Gerontol 56:77–88. doi:10.1016/j.exger.2014.03.023
König A, Bouzan C, Cohen JT, Connor WE, Kris-Etherton PM, Gray GM, Lawrence RS, Savitz DA, Teutsch SM (2005) A quantitative analysis of fish consumption and coronary heart disease mortality. Am J Prev Med 29:335–346. doi:10.1016/j.amepre.2005.07.001
Kromhout D, Bloemberg B, Feskens E, Menotti A, Nissinen A (2000) Saturated fat, vitamin C and smoking predict long-term population all-cause mortality rates in the Seven Countries Study. Int J Epidemiol 29:260–265. doi:10.1093/ije/29.2.260
Laganiere S, Yu BP (1989) Effect of chronic food restriction in aging rats. II. Liver cytosolic antioxidants and related enzymes. Mech Ageing Dev 48:221–230. doi:10.1016/0047-6374(89)90084-5
Laganiere S, Yu BP (1993) Modulation of membrane phospholipid fatty acid composition by age and food restriction. Gerontology 39:7–18. doi:10.1159/000213509
Lal SB, Ramsey JJ, Monemdjou S, Weindruch R, Harper ME (2001) Effects of caloric restriction on skeletal muscle mitochondrial proton leak in aging rats. J Gerontol A Biol Sci Med Sci 56:B116–B122. doi:10.1093/gerona/56.3.B116
Lambert AJ, Merry BJ (2004) Effect of caloric restriction on mitochondrial reactive oxygen species production and bioenergetics: reversal by insulin. Am J Physiol Regul Integr Comp Physiol 286:R71–R79. doi:10.1152/ajpregu.00341.2003
Lambert AJ, Merry BJ (2005) Lack of effect of caloric restriction on bioenergetics and reactive oxygen species production in intact rat hepatocytes. J Gerontol A Biol Sci Med Sci 60:175–180. doi:10.1093/gerona/60.2.175
Lands B (2014) Historical perspectives on the impact of n-3 and n-6 nutrients on health. Prog Lipid Res 55:17–29. doi:10.1016/j.plipres.2014.04.002
Lee AG (2004) How lipids affect the activities of integral membrane proteins. Biochim Biophys Acta 1666:62–87. doi:10.1016/j.bbamem.2004.05.012
León H, Shibata MC, Sivakumaran S, Dorgan M, Chatterley T, Tsuyuki RT (2008) Effect of fish oil on arrhythmias and mortality: systematic review. BMJ 23(337):a2931. doi:10.1136/bmj.a2931
Leosdottir M, Nilsson PM, Nilsson JA, Månsson H, Berglund G (2005) Dietary fat intake and early mortality patterns–data from The Malmö Diet and Cancer Study. J Intern Med 258:153–165. doi:10.1111/j.1365-2796.2005.01520.x
Li M, Izpisua-Belmonte JC (2014) Ageing: genetic rejuvenation of old muscle Nature 506: 304–305. doi: 10.1038/nature13058
López-Domínguez JA, Khraiwesh H, González-Reyes JA, López-Lluch G, Navas P, Ramsey JJ, de Cabo R, Burón MI, Villalba JM (2013) Dietary fat modifies mitochondrial and plasma membrane apoptotic signaling in skeletal muscle of calorie-restricted mice. Age (Dordr) 35:2027–2044. doi:10.1007/s11357-012-9492-9
López-Domínguez JA, Khraiwesh H, González-Reyes JA, López-Lluch G, Navas P, Ramsey JJ, de Cabo R, Burón MI, Villalba JM (2014a) Dietary fat and aging modulate apoptotic signaling in liver of calorie-restricted mice. J Gerontol A Biol Sci Med Sci doi:10.1093/gerona/glu045
López-Domínguez JA, Ramsey JJ, Tran D, Imai DM, Koehne A, Laing ST, Griffey SM, Kim K, Taylor SL, Hagopian K, Villalba JM, López-Lluch G, Navas P, McDonald RB (2014b) The influence of dietary fat source on life span in calorie restricted mice. J Gerontol A Biol Sci Med Sci doi:10.1093/gerona/glu177
López-Lluch G, Hunt N, Jones B, Zhu M, Jamieson H, Hilmer S, Cascajo MV, Allard J, Ingram DK, Navas P, de Cabo R (2006) Calorie restriction induces mitochondrial biogenesis and bioenergetic efficiency. Proc Natl Acad Sci U S A. 103:1768–1773. doi:10.1073/pnas.0510452103
López-Otín C, Blasco MA, Partridge L, Serrano M, Kroemer G (2013) The hallmarks of aging. Cell 153:1194–1217. doi:10.1016/j.cell.2013.05.039
Marsh D (2008) Protein modulation of lipids, and vice versa, in membranes. Biochim Biophys Acta 1778:1545–1575. doi:10.1016/j.bbamem.2008.01.015
Marzetti E, Lawler JM, Hiona A, Manini T, Seo AY, Leeuwenburgh C (2008a) Modulation of age-induced apoptotic signaling and cellular remodeling by exercise and calorie restriction in skeletal muscle. Free Radic Biol Med 44:160–168. doi:10.1016/j.freeradbiomed.2007.05.028
Marzetti E, Wohlgemuth SE, Lees HA, Chung H-Y, Giovannini S, Leeuwenburgh C (2008b) Age-related activation of mitochondrial caspase-independent apoptotic signaling in rat gastrocnemius muscle. Mech Ageing Dev 129:542–549. doi:10.1016/j.mad.2008.05.005
Marzetti E, Carter CS, Wohlgemuth SE, Lees HA, Giovannini S, Anderson B, Quinn LS, Leeuwenburgh C (2009) Changes in IL-15 expression and death-receptor apoptotic signaling in rat gastrocnemius muscle with aging and lifelong calorie restriction. Mech Ageing Dev 130:272–280. doi:10.1016/j.mad.2008.12.008
Masoro EJ (2006) Caloric restriction and aging: controversial issues. J Gerontol A Biol Sci Med Sci 61:14–19
Masoro EJ, Iwasaki K, Gleiser CA, McMahan CA, Seo EJ, Yu BP (1989) Dietary modulation of the progression of nephropathy in aging rats: an evaluation of the importance of protein. Am J Clin Nutr 49:1217–1227
Mataix J, Ochoa JJ, Quiles JL (2006) Olive oil and mitochondrial oxidative stress. Int J Vitam Nutr Res 76:178–183
Mattison JA, Roth GS, Beasley TM, Tilmont EM, Handy AM, Herbert RL, Longo DL, Allison DB, Young JE, Bryant M, Barnard D, Ward WF, Qi W, Ingram DK, de Cabo R (2012) Impact of caloric restriction on health and survival in rhesus monkeys from the NIA study. Nature 489:318–321. doi:10.1038/nature11432
McMillin JB, Bick RJ, Benedict CR (1992) Influence of dietary fish oil on mitochondrial function and response to ischemia. Am J Physiol 263:H1479–H1485
Meagher EA, Fitzgerald GA (2000) Indices of lipid peroxidation in vivo: strengths and limitations. Free Radic Biol Med 28:1745–1750. doi:10.1016/S0891-5849(00)00232-X
Mujahid A, Akiba Y, Toyomizu M (2009) Olive oil-supplemented diet alleviates acute heat stress-induced mitochondrial ROS production in chicken skeletal muscle. Am J Physiol Regul Integr Comp Physiol 297:R690–R698. doi:10.1152/ajpregu.90974.2008
Murtagh-Mark CM, Reiser KM, Harris R Jr, McDonald RB (1995) Source of dietary carbohydrate affects life span of Fischer 344 rats independent of caloric restriction. J Gerontol A Biol Sci Med Sci 50:B148–B154. doi:10.1093/gerona/50A.3.B148
Nakamura MT, Yudell BE, Loor JJ (2014) Regulation of energy metabolism by long-chain fatty acids. Prog Lipid Res 53:124–144. doi:10.1016/j.plipres.2013.12.001
Nisoli E, Tonello C, Cardile A, Cozzi V, Bracale R, Tedesco L, Falcone S, Valerio A, Cantoni O, Clementi E, Moncada S, Carruba MO (2005) Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science 310:314–317. doi:10.1126/science.1117728
Noreen EE, Sass MJ, Crowe ML, Pabon VA, Brandauer J, Averill LK (2010) Effects of supplemental fish oil on resting metabolic rate, body composition, and salivary cortisol in healthy adults. J Int Soc Sports Nutr 7:31. doi:10.1186/1550-2783-7-31
Pamplona R, Barja G (2011) An evolutionary comparative scan for longevity-related oxidative stress resistance mechanisms in homeotherms. Biogerontology 12:409–435. doi:10.1007/s10522-011-9348-1
Pamplona R, Portero-Otín M, Riba D, Ruiz C, Prat J, Bellmunt MJ, Barja G (1998) Mitochondrial membrane peroxidizability index is inversely related to maximum life span in mammals. J Lipid Res 39:1989–1994
Pamplona R, Barja G, Portero-Otín M (2002) Membrane fatty acid unsaturation, protection against oxidative stress, and maximum life span: a homeoviscous-longevity adaptation? Ann N Y Acad Sci 959:475–490. doi:10.1111/j.1749-6632.2002.tb02118.x
Pamplona R, Portero-Otín M, Sanz A, Requena J, Barja G (2004) Modification of the longevity-related degree of fatty acid unsaturation modulates oxidative damage to proteins and mitochondrial DNA in liver and brain. Exp Gerontol 39:725–733. doi:10.1016/j.exger.2004.01.006
Phillips T, Leeuwenburgh C (2005) Muscle fiber specific apoptosis and TNF-alpha signaling in sarcopenia are attenuated by life-long calorie restriction. FASEB J 19:668–670. doi:10.1096/fj.04-2870fje
Porter RK, Hulbert AJ, Brand MD (1996) Allometry of mitochondrial proton leak: influence of membrane surface area and fatty acid composition. Am J Physiol 271:R1550–R1560
Power GW, Newsholme EA (1997) Dietary fatty acids influence the activity and metabolic control of mitochondrial carnitine palmitoyltransferase I in rat heart and skeletal muscle. J Nutr 127:2142–2150
Power GW, Yaqoob P, Harvey DJ, Newsholme EA, Calder PC (1994) The effect of dietary lipid manipulation on hepatic mitochondrial phospholipid fatty acid composition and carnitine palmitoyltransferase I activity. Biochem Mol Biol Int 34:671–684
Pugh TD, Klopp RG, Weindruch R (1999) Controlling caloric consumption: protocols for rodents and rhesus monkeys. Neurobiol Aging 20:157–165. doi:10.1016/S0197-4580(99)00043-3
Quiles JL, Martínez E, Ibáñez S, Ochoa JJ, Martín Y, López-Frías M, Huertas JR, Mataix J (2002) Ageing-related tissue-specific alterations in mitochondrial composition and function are modulated by dietary fat type in the rat. J Bioenerg Biomembr 34:517–524. doi:10.1023/A:1022530512096
Ramsey JJ, Hagopian K (2006) Energy expenditure and restriction of energy intake: could energy restriction alter energy expenditure in companion animals? J Nutr 136:1958S–1966S
Ramsey JJ, Harper ME, Weindruch R (2000) Restriction of energy intake, energy expenditure, and aging. Free Radic Biol Med 29:946–968. doi:10.1016/S0891-5849(00)00417-2
Ramsey JJ, Hagopian K, Kenny TM, Koomson EK, Bevilacqua L, Weindruch R, Harper ME (2004) Proton leak and hydrogen peroxide production in liver mitochondria from energy-restricted rats. Am J Physiol Endocrinol Metab 286:E31–E40. doi:10.1152/ajpendo.00283.2003
Ramsey JJ, Harper ME, Humble SJ, Koomson EK, Ram JJ, Bevilacqua L, Hagopian K (2005) Influence of mitochondrial membrane fatty acid composition on proton leak and H2O2 production in liver. Comp Biochem Physiol B: Biochem Mol Biol 140:99–108. doi:10.1016/j.cbpc.2004.09.016
Sanchez-Roman I, Gomez J, Naudi A, Ayala V, Portero-Otín M, Lopez-Torres M, Pamplona R, Barja G (2010) The β-blocker atenolol lowers the longevity-related degree of fatty acid unsaturation, decreases protein oxidative damage, and increases extracellular signal-regulated kinase signaling in the heart of C57BL/6 mice. Rejuvenation Res 13:683–693. doi:10.1089/rej.2010.1062
Sanchez-Roman I, Gomez A, Naudí A, Jove M, Gómez J, Lopez-Torres M, Pamplona R, Barja G (2014) Independent and additive effects of atenolol and methionine restriction on lowering rat heart mitochondria oxidative stress. J Bioenerg Biomembr 46:159–172. doi:10.1007/s10863-013-9535-7
Schmitz G, Ecker J (2008) The opposing effects of n-3 and n-6 fatty acids. Prog Lipid Res 47:147–155. doi:10.1016/j.plipres.2007.12.004
Seo AY, Xu J, Servais S, Hofer T, Marzetti E, Wohlgemuth SE, Knutson MD, Chung HY, Leeuwenburgh C (2008) Mitochondrial iron accumulation with age and functional consequences. Aging Cell 7:706–716. doi:10.1111/j.1474-9726.2008.00418.x
Sohal RS, Weindruch R (1996) Oxidative stress, caloric restriction, and aging. Science 273:59–63. doi:10.1126/science.273.5271.59
Sousa-Victor P, Gutarra S, García-Prat L, Rodriguez-Ubreva J, Ortet L, Ruiz-Bonilla V, Jardí M, Ballestar E, González S, Serrano AL, Perdiguero E, Muñoz-Cánoves P (2014) Geriatric muscle stem cells switch reversible quiescence into senescence. Nature 506:316–321. doi:10.1038/nature13013
Speakman JR, Mitchell SE (2011) Caloric restriction. Mol Aspects Med 32:159–221. doi:10.1016/j.mam.2011.07.001
Spindler SR, Mote PL, Flegal JM (2014) Dietary supplementation with Lovaza and krill oil shortens the life span of long-lived F1 mice. Age 36:1345–1352. doi:10.1007/s11357-014-9659-7
Staessen L, De Bacquer D, De Henauw S, De Backer G, Van Peteghem C (1997) Relation between fat intake and mortality: an ecological analysis in Belgium. Eur J Cancer Prev 6:374–381
Su W, Jones PJ (1993) Dietary fatty acid composition influences energy accretion in rats. J Nutr 123:2109–2114
Tahin QS, Blum M, Carafoli E (1981) The fatty acid composition of subcellular membranes of rat liver, heart, and brain: diet-induced modifications. Eur J Biochem 121:5–13. doi:10.1111/j.1432-1033.1981.tb06421.x
Tsuboyama-Kasaoka N, Sano K, Shozawa C, Osaka T, Ezaki O (2008) Studies of UCP2 transgenic and knockout mice reveal that liver UCP2 is not essential for the antiobesity effects of fish oil. Am J Physiol Endocrinol Metab 294:E600–E606. doi:10.1152/ajpendo.00551.2007
Tsuduki T, Honma T, Nakagawa K, Ikeda I, Miyazawa T (2011) Long-term intake of fish oil increases oxidative stress and decreases lifespan in senescence-accelerated mice. Nutrition 27:334–337. doi:10.1016/j.nut.2010.05.017
Tucker KL, Hallfrisch J, Qiao N, Muller D, Andres R, Fleg JL, Baltimore Longitudinal Study of Aging (2005) The combination of high fruit and vegetable and low saturated fat intakes is more protective against mortality in aging men than is either alone: the Baltimore Longitudinal Study of aging. J Nutr 135:556–561
Umezawa M, Takeda T, Kogishi K, Higuchi K, Matushita T, Wang J, Chiba T, Hosokawa M (2000) Serum lipid concentrations and mean life span are modulated by dietary polyunsaturated fatty acids in the senescence-accelerated mouse. J Nutr 130:221–227
Villalba JM, Alcaín FJ (2012) Sirtuin activators and inhibitors. BioFactors 38:349–359. doi:10.1002/biof.1032
Wohlgemuth SE, Seo AY, Marzetti E, Lees HA, Leeuwenburgh C (2010) Skeletal muscle autophagy and apoptosis during aging: effects of calorie restriction and life-long exercise. Exp Gerontol 45:138–148. doi:10.1016/j.exger.2009.11.002
Yamagishi K, Iso H, Date C, Fukui M, Wakai K, Kikuchi S, Inaba Y, Tanabe N, Tamakoshi A, Japan Collaborative Cohort Study for Evaluation of Cancer Risk Study Group (2008) Fish, omega-3 polyunsaturated fatty acids, and mortality from cardiovascular diseases in a nationwide community-based cohort of Japanese men and women the JACC (Japan Collaborative Cohort Study for Evaluation of Cancer Risk) Study. J Am Coll Cardiol 52:988–996. doi:10.1016/j.jacc.2008.06.018
Yamaoka S, Urade R, Kito M (1988) Mitochondrial function in rats is affected by modification of membrane phospholipids with dietary sardine oil. J Nutr 118:290–296
Yu BP, Lim BO, Sugano M (2002) Dietary restriction downregulates free radical and lipid peroxide production: plausible mechanism for elongation of life span. J Nutr Sci Vitaminol (Tokyo) 48:257–264
Acknowledgments
Supported by NIH grant 1R01AG028125 (to JJR, PN and JMV), Ministerio de Economía y Competitividad BFU2011-23578 (to JMV), Junta de Andalucía Proyectos de Excelencia grant P09-CVI-4887 (to JMV), Junta de Andalucía Proyectos Internacionales grant (to JMV), and BIO-276 (Junta de Andalucía and the University of Córdoba, to JMV). RdC is funded by the Intramural Research program of the NIA/NIH. JALD, JA, LFdR and EGC were funded by a predoctoral fellowship of the Spanish Ministerio de Educación and BIO-276. HK was funded by a predoctoral fellowship of the Agencia Española de Cooperación Internacional al Desarrollo and BIO-276. MCR and MdR were supported by BIO-276.
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Villalba, J.M., López-Domínguez, J.A., Chen, Y. et al. The influence of dietary fat source on liver and skeletal muscle mitochondrial modifications and lifespan changes in calorie-restricted mice. Biogerontology 16, 655–670 (2015). https://doi.org/10.1007/s10522-015-9572-1
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DOI: https://doi.org/10.1007/s10522-015-9572-1