Mitochondrial ultrastructure and markers of dynamics in hepatocytes from aged, calorie restricted mice fed with different dietary fats

Experimental Gerontology

Volumn 56, Issue , 2014, Pages 77-88

  Khraiwesh, Husam ^a   López Domínguez, José A ^a,b   Fernández del Río, Lucía ^a   Gutierrez Casado, Elena ^a   López Lluch, Guillermo ^c   Navas, Plácido ^c   de Cabo, Rafael ^d   Ramsey, Jon J ^b   Burón, María I ^a   Villalba, José M ^a   González Reyes, José A ^a  

^a UNIVERSITY OF CÓRDOBA   (Spain)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

^d NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

Calorie restriction; Dietary fat; Hepatocyte; Mature old aged mice; Mitochondria

Indexed keywords

FISH OIL; HYBRID PROTEIN; LARD; NUCLEAR RESPIRATORY FACTOR 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; SOYBEAN OIL; BIOLOGICAL MARKER; FAT INTAKE; LIPID PEROXIDE; NRF1 PROTEIN, MOUSE; PPARGC1A PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOGENESIS; CALORIC RESTRICTION; CELL SIZE; CELL ULTRASTRUCTURE; CONTROLLED STUDY; FAT INTAKE; LIPID PEROXIDATION; LIVER CELL; LIVER HOMOGENATE; LIVER MITOCHONDRION; MALE; MICROSCOPY; MOUSE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEREOLOGY; WESTERN BLOTTING; ADMINISTRATION AND DOSAGE; AGE; AGING; ANIMAL; C57BL MOUSE; COMPARATIVE STUDY; METABOLISM; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL VOLUME; PATHOLOGY; TIME; ULTRASTRUCTURE;

ANIMALIA; GLYCINE MAX; MUS;

AGE FACTORS; AGING; ANIMALS; BIOLOGICAL MARKERS; CALORIC RESTRICTION; CELL SIZE; DIETARY FATS; FISH OILS; HEPATOCYTES; LIPID PEROXIDES; MALE; MICE, INBRED C57BL; MITOCHONDRIA, LIVER; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL SIZE; MITOCHONDRIAL TURNOVER; NUCLEAR RESPIRATORY FACTOR 1; SOYBEAN OIL; TIME FACTORS; TRANSCRIPTION FACTORS;

EID: 84901856057     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2014.03.023     Document Type: Article

References (49)

1. Barja G. Updating the mitochondrial free radical theory of aging: an integrated view, key aspects, and confounding concepts. Antioxid. Redox Signal. 2013, 19:1420-1445.
2. Baur J.A., Pearson K.J., Price N.L., Jamieson H.A., Lerin C., Kalra A., Prabhu V.V., Allard J.S., Lopez-Lluch G., Lewis K., Pistell P.J., Poosala S., Becker K.G., Boss O., Gwinn D., Wang M., Ramaswamy S., Fishbein K.W., Spencer R.G., Lakatta E.G., Le Couteur D., Shaw R.J., Navas P., Puigserver P., Ingram D.K., de Cabo R., Sinclair D.A. Resveratrol improves health and survival of mice on a high-calorie diet. Nature 2006, 444:337-342.
3. Bello R.I., Alcaín F.J., Gómez-Díaz C., López-Lluch G., Navas P., Villalba J.M. Hydrogen peroxide- and cell-density-regulated expression of NADH-cytochrome b5 reductase in HeLa cells. J. Bioenerg. Biomembr. 2003, 35:169-179.
4. Bevilacqua L., Ramsey J.J., Hagopian K., Weindruch R., Harper M.E. Effects of short- and medium-term calorie restriction on muscle mitochondrial proton leak and reactive oxygen species production. Am. J. Physiol. Endocrinol. Metab. 2004, 286:E852-E861.
5. Bratic A., Larsson N.G. The role of mitochondria in aging. J. Clin. Invest. 2013, 123:951-957.
6. Campisi J. Aging, cellular senescence, and cancer. Annu. Rev. Physiol. 2013, 75:685-705.
7. Chan D.C. Fusion and fission: interlinked processes critical for mitochondrial health. Annu. Rev. Genet. 2012, 46:265-287.
8. Chen Y., Hagopian K., McDonald R.B., Bibus D., López-Lluch G., Villalba J.M., Navas P., Ramsey J.J. The influence of dietary lipid composition on skeletal muscle mitochondria from mice following 1month of calorie restriction. J. Gerontol. A Biol. Sci. Med. Sci. 2012, 67:1121-1131.
9. Chen Y., Hagopian K., Bibus D., Villalba J.M., López-Lluch G., Navas P., Kim K., McDonald R.B., Ramsey J.J. The influence of dietary lipid composition on liver mitochondria from mice following 1month of calorie restriction. Biosci. Rep. 2013, 33:83-95.
10. Chung K.W., Kima D.H., Parka M.H., Choia Y.J., Kima N.D., Leea J., Yub B.P., Chung H.Y. Recent advances in calorie restriction research on aging. Exp. Gerontol. 2013, 48:1049-1053.
11. Cogger V.C., Svistounov D., Warren A., Zykova S., Melvin R.G., Solon-Biet S.M., O'Reilly J.N., McMahon A.C., Ballard J.W., De Cabo R., Le Couteur D.G., Lebel M. Liver aging and pseudocapillarization in a Werner syndrome mouse model. J. Gerontol. A Biol. Sci. Med. Sci. 2013, (Oct 22, Epub ahead of print). 10.1093/gerona/glt169.
12. Colman R.J., Anderson R.M., Johnson S.C., Kastman E.K., Kosmatka K.J., Beasley T.M., Allison D.B., Cruzen C., Simmons H.A., Kemnitz J.W., Weindruch R. Caloric restriction delays disease onset and mortality in rhesus monkeys. Science 2009, 325:201-204.
13. Gomes L.C., Di Benedetto G., Scorrano L. During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Nat. Cell Biol. 2011, 13:589-598.
14. Gregg S.Q., Gutiérrez V., Robinson A.R., Woodell T., Nakao A., Ross M.A., Michalopoulos G.K., Rigatti L., Rothermel C.E., Kamileri I., Garinis G.A., Stolz D.B., Niedernhofer L.J. A mouse model of accelerated liver aging caused by a defect in DNA repair. Hepatology 2012, 55:609-621.
15. Hagopian K., Harper M.E., Ram J.J., Humble S.J., Weindruch R., Ramsey J.J. Long-term calorie restriction reduces proton leak and hydrogen peroxide production in liver mitochondria. Am. J. Physiol. Endocrinol. Metab. 2005, 288:E674-E684.
16. Hagopian K., Weber K.L., Hwee D.T., Van Eenennaam A.L., López-Lluch G., Villalva J.M., Burón I., Navas P., German J.B., Watkins S.M., Chen Y., Wei A., McDonald R.B., Ramsey J.J. 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 2010, 5(9):e12696. 10.1371/journal.pone.0012696.
17. Harman D. The biological clock: the mitochondria?. J. Am. Geriatr. Soc. 1972, 20:145-147.
18. Hekimi S., Lapointe J., Wen Y. Taking a "good" look at free radicals in the aging process. Trends Cell Biol. 2011, 21:569-576.
19. Hulbert A.J. Life, death and membrane bilayers. J. Exp. Biol. 2003, 206:2303-2311.
20. Jiang Z.Y., Woollard A.C., Wolff S.P. Lipid hydroperoxide measurement by oxidation of Fe2+ in the presence of xylenol orange. Comparison with the TBA assay and an iodometric method. Lipids 1991, 26:853-856.
21. Kaneko T., Tahara S., Matsuo M. Retarding effect of dietary restriction on the accumulation of 8-hydroxy-2'-deoxyguanosine in organs of Fischer 344 rats during aging. Free Radic. Biol. Med. 1997, 23:76-81.
22. Khraiwesh H., López-Domínguez J.A., López-Lluch G., Navas P., de Cabo R., Ramsey J.J., Villalba J.M., González-Reyes J.A. 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. 2013, 68:1023-1034.
23. Le Couteur D.G., Sinclair D.A., Cogger V.C. The aging liver and the effect of longterm caloric restriction. Calorie Restriction, Aging and Longevity 2010, 191-216. Springer Press, Dordrecht, Netherlands. A.V. Everitt, S.I.S. Rattan, D.G. Le Couteur, R. de Cabo (Eds.).
24. Liesa M., Shirihai O.S. Mitochondrial dynamics in the regulation of nutrient utilization and energy expenditure. Cell Metab. 2013, 17:491-506.
25. López-Domínguez J.A., Khraiwesh H., González-Reyes J.A., López-Lluch G., Navas P., Ramsey J.J., de Cabo R., Burón M.I., Villalba J.M. Dietary fat modifies mitochondrial and plasma membrane apoptotic signaling in skeletal muscle of calorie restricted mice. Age 2013, 35:2027-2044.
26. López-Domínguez J.A., Khraiwesh H., González-Reyes J.A., López-Lluch G., Navas P., Ramsey J.J., de Cabo R., Buron I., Villalba J.M. Dietary fat and aging modulate apoptotic signaling in liver of calorie-restricted mice. J. Gerontol. A Biol. Sci. Med. Sci. 2014, (in press). 10.1093/gerona/glu045.
27. López-Lluch G., Hunt N., Jones B., Zhu M., Jamieson H., Hilmer S., Cascajo M.V., Allard J., Ingram D.K., Navas P., de Cabo R. Calorie restriction induces mitochondrial biogenesis and bioenergetic efficiency. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:1768-1773.
28. López-Otín C., Blasco M.A., Partridge L., Serrano M., Kroemer G. The hallmarks of aging. Cell 2013, 153:1194-1217.
29. Mattison J.A., Roth G.S., Beasley T.M., Tilmont E.M., Handy A.M., Herbert R.L., Longo D.L., Allison B., Young J.E., Bryant M., Barnard D., Ward W.F., Qi W., Ingram D.K., de Cabo R. Impact of caloric restriction on health and survival in rhesus monkeys from the NIA study. Nature 2012, 489:318-321.
30. Miquel J., Economos A.C., Fleming J., Johnson J.E. Mitochondrial role in cell aging. Exp. Gerontol. 1980, 15:575-591.
31. Nisoli E., Tonello C., Cardile A., Cozzi V., Bracale R., Tedesco L., Falcone S., Valerio A., Cantoni O., Clementi E., Moncada S., Carruba M.O. Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science 2005, 310:314-317.
32. Pamplona R., Barja G., Portero-Otin M. Membrane fatty acid unsaturation, protection against oxidative stress, and maximum life span: a homeoviscous-longevity adaptation?. Ann. N. Y. Acad. Sci. 2002, 959:475-490.
33. Pieri C., Giuli C., Del Moro M., Piantanelli L. Electron-microscopic morphometric analysis of mouse liver. II. Effect of ageing and thymus transplantation in old animals. Mech. Ageing Dev. 1980, 13:275-283.
34. Sastre J., Pallardo F.V., Plá R., Pellín A., Juan G., O'Connor J.E., Estrela J.M., Miquel J., Viña J. Aging of the liver: age-associated mitochondrial damage in intact hepatocytes. Hepatology 1996, 24:1199-1205.
35. Sato T. A modified method for lead staining of thin sections. J. Electron Microsc. (Tokyo) 1968, 17:158-159.
36. Schmucker D.L. Hepatocyte fine structure during maturation and senescence. J. Electron Microsc. Tech. 1990, 14:106-125.
37. Schmucker D.L. Aging and the liver: an update. J. Gerontol. Biol. Sci. 1998, 53A:B315-B320.
38. Schmucker D.L. Age-related changes in liver structure and function: implications for disease?. Exp. Gerontol. 2005, 40:650-659.
39. Schmucker D.L., Sanchez H. Liver regeneration and aging: a current perspective. Curr. Gerontol. Geriatr. Res. 2011, 2011. (Article ID 526379, 8 pages). 10.1155/2011/526379.
40. Schmucker D.L., Mooney J.S., Jones A.L. Stereological analysis of hepatic fine structure in the Fischer 344 rat. Influence of sublobular location and animal age. J. Cell Biol. 1978, 78:319-337.
41. Shiozaki M., Hayakawa N., Shibata M., Koike M., Uchiyama Y., Gotow T. Closer association of mitochondria with lipid droplets in hepatocytes and activation of Kupffer cells in resveratrol-treated senescence-accelerated mice. Histochem. Cell Biol. 2011, 136:475-489.
42. Sohal R.S., Weindruch R. Oxidative stress, caloric restriction, and aging. Science 1996, 273:59-63.
43. Sohal R.S., Agarwal S., Candas M., Forster M.J., Lal H. Effect of age and caloric restriction on DNA oxidative damage in different tissues of C57BL/6 mice. Mech. Ageing Dev. 1994, 76:215-224.
44. Weibel E.R. Stereological Methods. Practical Methods for Biological Morphometry 1979, vol. 1. Academic Press, New York, NY.
45. Weindruch R., Sohal R.S. Seminars in medicine of the Beth Israel Deaconess Medical Center. Caloric intake and aging. N. Engl. J. Med. 1997, 337:986-994.
46. Weindruch R.H., Walford R.L. The Retardation of Aging and Disease by Dietary Restriction 1988, Charles C. Thomas, Springfield, IL.
47. Youngman L.D., Park J.Y., Ames B.N. Protein oxidation associated with aging is reduced by dietary restriction of protein or calories. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:9112-9116.
48. Yu B.P., Lim B.O., Sugano M. Dietary restriction downregulates free radical and lipid peroxide production: plausible mechanism for elongation of life span. J. Nutr. Sci. Vitaminol. 2002, 48:257-264.
49. Zs.-Nagy I. A membrane hypothesis of aging. J. Theor. Biol. 1978, 75:189-195.