Methionine restriction slows down senescence in human diploid fibroblasts

Aging Cell

Volumn 13, Issue 6, 2014, Pages 1038-1048

  Koziel, Rafal ^a   Ruckenstuhl, Christoph ^b   Albertini, Eva ^a   Neuhaus, Michael ^a   Netzberger, Christine ^b   Bust, Maria ^c   Madeo, Frank ^b   Wiesner, Rudolf J ^c,d   Jansen Dürr, Pidder ^a  

^a UNIVERSITY OF INNSBRUCK   (Austria)

^b UNIVERSITY OF GRAZ   (Austria)

^c UNIVERSITY OF COLOGNE   (Germany)

^d UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Cellular senescence; Fibroblast; Methionine; Mitochondria; Oxidative stress

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 2A; CYTOCHROME C OXIDASE; METHIONINE; MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE);

ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DIET RESTRICTION; DIPLOIDY; FIBROBLAST; HUMAN; HUMAN CELL; HUMAN DIPLOID FIBROBLAST; LIFE EXTENSION; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; NEWBORN; OXIDATIVE PHOSPHORYLATION UNCOUPLING; OXIDATIVE STRESS; PRIORITY JOURNAL; RESPIRATORY CHAIN; SENESCENCE; WESTERN BLOTTING; AGE; ANIMAL; CYTOLOGY; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; METABOLISM; PHYSIOLOGY;

AGE FACTORS; ANIMALS; DIPLOIDY; DISEASE MODELS, ANIMAL; FIBROBLASTS; HUMANS; METHIONINE; MITOCHONDRIA; OXIDATIVE STRESS;

EID: 84911990776     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/acel.12266     Document Type: Article

References (51)

1. Baker DJ, Wijshake T, Tchkonia T, LeBrasseur NK, Childs BG, van de Sluis B, Kirkland JL, van Deursen JM (2011) Clearance of p16Ink4a-positive senescent cells delays ageing-associated disorders. Nature 479, 232-236.
2. Belousov VV, Fradkov AF, Lukyanov KA, Staroverov DB, Shakhbazov KS, Terskikh AV, Lukyanov S (2006) Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nat. Methods 3, 281-286.
3. Bodnar A, Ouellette M, Holt M, Chiu C, Morin G, Harley C, Shay J, Lichtsteiner S, Wright W (1998) Extension of life-span by introduction of telomerase into normal human cells. Science 279, 349-353.
4. Brand DM, Nicholls D (2011) Assessing mitochondrial dysfunction in cells. Biochem. J. 435, 297-312.
5. Campisi J (2005) Senescent cells, tumor suppression, and organismal aging: good citizens, bad neighbors. Cell 120, 513-522.
6. Campisi J (2011) Cellular senescence: putting the paradoxes in perspective. Curr. Opin. Genet. Dev. 21, 107-112.
7. Caro P, Gomez J, Lopez-Torres M, Sanchez I, Naudi A, Jove M, Pamplona R, Barja G (2008) Forty percent and eighty percent methionine restriction decrease mitochondrial ROS generation and oxidative stress in rat liver. Biogerontology 9, 183-196.
8. Caro P, Gomez J, Sanchez I, Naudi A, Ayala V, Lopez-Torres M, Pamplona R, Barja G (2009) Forty percent methionine restriction decreases mitochondrial oxygen radical production and leak at complex I during forward electron flow and lowers oxidative damage to proteins and mitochondrial DNA in rat kidney and brain mitochondria. Rejuvenation Res. 12, 421-434.
9. Ch'ih JJ, Olszyna DM, Devlin TM (1976) Alteration in plasma and cellular enzyme and protein levels after lethal and non-lethal doses of cycloheximide in the rat. Biochem. Pharmacol. 25, 2407-2408.
10. Chomyn A (1996) In vivo labeling and analysis of human mitochondrial translation products. Methods Enzymol. 264, 197-211.
11. Cossarizza A, Baccarani-Contri M, Kalashnikova G, Franceschi C (1993) A new method for the cytofluorimetric analysis of mitochondrial membrane potential using the J-aggregate forming lipophilic cation 5, 5', 6, 6'-tetrachloro-1, 1', 3, 3'-tetraethylbenzimidazolcarbocyanine iodide (JC-1). Biochem. Biophys. Res. Commun. 197, 40-45.
12. Dufour E, Terzioglu M, Hansson FS, Sorensen L, Galter D, Olson L, Wilbertz J, Larsson NG (2008) Age-associated mosaic respiratory chain deficiency causes trans-neuronal degeneration. Hum. Mol. Genet. 17, 1418-1426.
13. Forkink M, Smeitink JA, Brock R, Willems PH, Koopman WJ (2010) Detection and manipulation of mitochondrial reactive oxygen species in mammalian cells. Biochim. Biophys. Acta 1797, 1034-1044.
14. Fornuskova D, Stiburek L, Wenchich L, Vinsova K, Hansikova H, Zeman J (2010) Novel insights into the assembly and function of human nuclear-encoded cytochrome c oxidase subunits 4, 5a, 6a, 7a and 7b. Biochem. J. 428, 363-374.
15. Galati D, Srinivasan S, Raza H, Prabu SK, Hardy M, Chandran K, Lopez M, Kalyanaraman B, Avadhani NG (2009) Role of nuclear-encoded subunit Vb in the assembly and stability of cytochrome c oxidase complex: implications in mitochondrial dysfunction and ROS production. Biochem. J. 420, 439-449.
16. Grandison RC, Piper MD, Partridge L (2009) Amino-acid imbalance explains extension of lifespan by dietary restriction in Drosophila. Nature 462, 1061-1064.
17. Hansen M, Taubert S, Crawford D, Libina N, Lee SJ, Kenyon C (2007) Lifespan extension by conditions that inhibit translation in Caenorhabditis elegans. Aging Cell 6, 95-110.
18. Hasek BE, Stewart LK, Henagan TM, Boudreau A, Lenard NR, Black C, Shin J, Huypens P, Malloy VL, Plaisance EP, Krajcik RA, Orentreich N, Gettys TW (2010) Dietary methionine restriction enhances metabolic flexibility and increases uncoupled respiration in both fed and fasted states. Am. J. Physiol. Regul. Integr. Comp. Physiol. 299, R728-R739.
19. Hayflick L (1997) Mortality and immortality at the cellular level. A review. Biochemistry (Mosc) 62, 1180-1190.
20. Hipkiss AR (2008) On methionine restriction, suppression of mitochondrial dysfunction and aging. Rejuvenation Res. 11, 685-688.
21. Holloszy JO, Oscai LB, Don IJ, Mole PA (1970) Mitochondrial citric acid cycle and related enzymes: adaptive response to exercise. Biochem. Biophys. Res. Commun. 40, 1368-1373.
22. Hornig-Do HT, Tatsuta T, Buckermann A, Bust M, Kollberg G, Rotig A, Hellmich M, Nijtmans L, Wiesner RJ (2012) Nonsense mutations in the COX1 subunit impair the stability of respiratory chain complexes rather than their assembly. EMBO J. 31, 1293-1307.
23. Hutter E, Renner K, Pfister G, Stockl P, Jansen-Durr P, Gnaiger E (2004) Senescence-associated changes in respiration and oxidative phosphorylation in primary human fibroblasts. Biochem. J. 380, 919-928.
24. Johnson JE, Johnson FB (2014) Methionine restriction activates the retrograde response and confers both stress tolerance and lifespan extension to yeast, mouse and human cells. PLoS ONE 9, e97729.
25. Koziel R, Pircher H, Kratochwil M, Lener B, Hermann M, Dencher NA, Jansen-Durr P (2013) Mitochondrial respiratory chain complex I is inactivated by NADPH oxidase Nox4. Biochem. J., 23, 1-239.
26. Kuznetsov AV, Strobl D, Ruttmann E, Konigsrainer A, Margreiter R, Gnaiger E (2002) Evaluation of mitochondrial respiratory function in small biopsies of liver. Anal. Biochem. 305, 186-194.
27. Lener B, Koziel R, Pircher H, Hutter E, Greussing R, Herndler-Brandstetter D, Hermann M, Unterluggauer H, Jansen-Durr P (2009) The NADPH oxidase Nox4 restricts the replicative lifespan of human endothelial cells. Biochem. J. 423, 363-374.
28. Lopez-Torres M, Barja G (2008) Lowered methionine ingestion as responsible for the decrease in rodent mitochondrial oxidative stress in protein and dietary restriction possible implications for humans. Biochim. Biophys. Acta 1780, 1337-1347.
29. Mailloux RJ, Harper ME (2012) Mitochondrial proticity and ROS signaling: lessons from the uncoupling proteins. Trends Endocrinol. Metab. 23, 451-458.
30. Mailloux RJ, Fu A, Robson-Doucette C, Allister EM, Wheeler MB, Screaton R, Harper ME (2012) Glutathionylation state of uncoupling protein-2 and the control of glucose-stimulated insulin secretion. J. Biol. Chem. 287, 39673-39685.
31. Malloy VL, Krajcik RA, Bailey SJ, Hristopoulos G, Plummer JD, Orentreich N (2006) Methionine restriction decreases visceral fat mass and preserves insulin action in aging male Fischer 344 rats independent of energy restriction. Aging Cell 5, 305-314.
32. Naudi A, Caro P, Jove M, Gomez J, Boada J, Ayala V, Portero-Otin M, Barja G, Pamplona R (2007) Methionine restriction decreases endogenous oxidative molecular damage and increases mitochondrial biogenesis and uncoupling protein 4 in rat brain. Rejuvenation Res. 10, 473-484.
33. Orentreich N, Matias JR, DeFelice A, Zimmerman JA (1993) Low methionine ingestion by rats extends life span. J. Nutr. 123, 269-274.
34. Pamplona R, Barja G (2006) Mitochondrial oxidative stress, aging and caloric restriction: the protein and methionine connection. Biochim. Biophys. Acta 1757, 496-508.
35. Passos JF, Saretzki G, Ahmed S, Nelson G, Richter T, Peters H, Wappler I, Birket MJ, Harold G, Schaeuble K, Birch-Machin MA, Kirkwood TB, von Zglinicki T (2007) Mitochondrial dysfunction accounts for the stochastic heterogeneity in telomere-dependent senescence. PLoS Biol. 5, e110.
36. Perrone CE, Mattocks DA, Jarvis-Morar M, Plummer JD, Orentreich N (2010) Methionine restriction effects on mitochondrial biogenesis and aerobic capacity in white adipose tissue, liver, and skeletal muscle of F344 rats. Metabolism 59, 1000-1011.
37. Plaisance EP, Henagan TM, Echlin H, Boudreau A, Hill KL, Lenard NR, Hasek BE, Orentreich N, Gettys TW (2010) Role of beta-adrenergic receptors in the hyperphagic and hypermetabolic responses to dietary methionine restriction. Am. J. Physiol. Regul. Integr. Comp. Physiol. 299, R740-R750.
38. Plaisance EP, Greenway FL, Boudreau A, Hill KL, Johnson WD, Krajcik RA, Perrone CE, Orentreich N, Cefalu WT, Gettys TW (2011) Dietary methionine restriction increases fat oxidation in obese adults with metabolic syndrome. J. Clin. Endocrinol. Metab. 96, E836-E840.
39. Rea SL, Ventura N, Johnson TE (2007) Relationship between mitochondrial electron transport chain dysfunction, development, and life extension in Caenorhabditis elegans. PLoS Biol. 5, e259.
40. Ruckenstuhl C, Netzberger C, Entfellner I, Carmona-Gutierrez D, Kickenweiz T, Stekovic S, Gleixner C, Schmid C, Klug L, Sorgo AG, Eisenberg T, Büttner S, Mariño G, Koziel R, Jansen-Dürr P, Fröhlich KU, Kroemer G, Madeo F (2014) Lifespan extension by methionine restriction requires autophagy-dependent vacuolar acidification. PLoS Genet. 10, e1004347.
41. Sanz A, Caro P, Ayala V, Portero-Otin M, Pamplona R, Barja G (2006) Methionine restriction decreases mitochondrial oxygen radical generation and leak as well as oxidative damage to mitochondrial DNA and proteins. FASEB J. 20, 1064-1073.
42. Schagger H (2002) Respiratory chain supercomplexes of mitochondria and bacteria. Biochim. Biophys. Acta 1555, 154-159.
43. Spindler SR (2010) Caloric restriction: from soup to nuts. Ageing Res. Rev. 9, 324-353.
44. Stein PK, Soare A, Meyer TE, Cangemi R, Holloszy JO, Fontana L (2012) Caloric restriction may reverse age-related autonomic decline in humans. Aging Cell 11, 644-650.
45. Stockl P, Zankl C, Hutter E, Unterluggauer H, Laun P, Heeren G, Bogengruber E, Herndler-Brandstetter D, Breitenbach M, Jansen-Durr P (2007) Partial uncoupling of oxidative phosphorylation induces premature senescence in human fibroblasts and yeast mother cells. Free Radic. Biol. Med. 43, 947-958.
46. Sun L, Sadighi Akha AA, Miller RA, Harper JM (2009) Life-span extension in mice by preweaning food restriction and by methionine restriction in middle age. J. Gerontol. A Biol. Sci. Med. Sci. 64, 711-722.
47. Syntichaki P, Troulinaki K, Tavernarakis N (2007) eIF4E function in somatic cells modulates ageing in Caenorhabditis elegans. Nature 445, 922-926.
48. Szczepanowska J, Malinska D, Wieckowski MR, Duszynski J (2012) Effect of mtDNA point mutations on cellular bioenergetics. Biochim. Biophys. Acta 1817, 1740-1746.
49. Unterluggauer H, Hampel B, Zwerschke W, Jansen-Durr P (2003) Senescence-associated cell death of human endothelial cells: the role of oxidative stress. Exp. Gerontol. 38, 1149-1160.
50. Wredenberg A, Wibom R, Wilhelmsson H, Graff C, Wiener HH, Burden SJ, Oldfors A, Westerblad H, Larsson NG (2002) Increased mitochondrial mass in mitochondrial myopathy mice. Proc. Natl. Acad. Sci. U S A 99, 15066-15071.
51. Zid BM, Rogers AN, Katewa SD, Vargas MA, Kolipinski MC, Lu TA, Benzer S, Kapahi P (2009) 4E-BP extends lifespan upon dietary restriction by enhancing mitochondrial activity in Drosophila. Cell 139, 149-160.