Biomarkers of aging in Drosophila

Aging Cell

Volumn 9, Issue 4, 2010, Pages 466-477

  Jacobson, Jake ^a,b   Lambert, Adrian J ^c   Portero Otín, Manuel ^d   Pamplona, Reinald ^d   Magwere, Tapiwanashe ^a,e   Miwa, Satomi ^c,f   Driege, Yasmine ^a   Brand, Martin D ^c,g   Partridge, Linda ^a,b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b MAX PLANCK INSTITUTE FOR BIOLOGY OF AGEING   (Germany)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d UNIVERSITY OF LLEIDA   (Spain)

^e ST JAMES S UNIVERSITY HOSPITAL   (United Kingdom)

^f NEWCASTLE UNIVERSITY   (United Kingdom)

^g BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

Author keywords

Biomarkers of aging; Demography of aging; Drosophila

Indexed keywords

ADVANCED GLYCATION END PRODUCT; BIOLOGICAL MARKER; INSECT PROTEIN;

AGING; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DIET RESTRICTION; DROSOPHILA; ENVIRONMENTAL TEMPERATURE; FEMALE; LIFESPAN; MALE; MOLECULAR MECHANICS; MORTALITY; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN MODIFICATION; RISK FACTOR; TEMPERATURE SENSITIVITY; ANIMAL; CALORIC RESTRICTION; DIET; DROSOPHILA MELANOGASTER; FLUORESCENCE; GROWTH, DEVELOPMENT AND AGING; METABOLISM; OXIDATION REDUCTION REACTION; SURVIVAL; TEMPERATURE;

AGING; ANIMALS; BIOLOGICAL MARKERS; CALORIC RESTRICTION; DIET; DROSOPHILA MELANOGASTER; FEMALE; FLUORESCENCE; GLYCOSYLATION END PRODUCTS, ADVANCED; INSECT PROTEINS; MALE; OXIDATION-REDUCTION; SURVIVAL ANALYSIS; TEMPERATURE;

EID: 78049438124     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/j.1474-9726.2010.00573.x     Document Type: Article

References (68)

1. Adachi H, Ishii N (2000) Effects of tocotrienols on life span and protein carbonylation in Caenorhabditis elegans. J. Gerontol. Ser. A-Biol. Sci. Med. Sci. 55, B280-B285.
2. Agarwal S, Sohal RS (1994a) Aging and proteolysis of oxidized proteins. Arch. Biochem. Biophys. 309, 24-28.
3. Agarwal S, Sohal RS (1994b) DNA oxidative damage and life expectancy in houseflies. Proc. Natl. Acad. Sci. USA 91, 12332-12335.
4. Ahmed N, Thornalley PJ (2007) Advanced glycation endproducts: what is their relevance to diabetic complications? Diabetes Obes. Metab. 9, 233-245.
5. Bass TM, Grandison RC, Wong R, Martinez P, Partridge L, Piper MDW (2007) Optimization of dietary restriction protocols in Drosophila. J. Gerontol. Ser. A-Biol. Sci. Med. Sci. 62, 1071-1081.
6. Baynes JW (2001) The role of AGEs in aging: causation or correlation. Exp. Gerontol. 36, 1527-1537.
7. Chapman T, Partridge L (1996) Female fitness in Drosophila melanogaster: an interaction between the effect of nutrition and of encounter rate with males. Proc. R. Soc. Lond. B Biol. Sci. 263, 755-759.
8. Colantoni A, Idilman R, de Maria N, Duffner LA, Van Thiel DH, Witte PL, Kovacs EJ (2001) Evidence of oxidative injury during aging of the liver in a mouse model. J. Am. Aging Assoc. 24, 51-57.
9. 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.
10. Dunlop RA, Brunk UT, Rodgers KJ (2009) Oxidized proteins: mechanisms of removal and consequences of accumulation. IUBMB Life 61, 522-527.
11. Fu MX, Requena JR, Jenkins AJ, Lyons TJ, Baynes JW, Thorpe SR (1996) The advanced glycation end product, N-(epsilon)(carboxym-ethyl)lysine, is a product of both lipid peroxidation and glycoxidation reactions. J. Biol. Chem. 271, 9982-9986.
12. Gerstbrein B, Stamatas G, Kollias N, Driscoll M (2005) In vivo spectrofluorimetry reveals endogenous biomarkers that report healthspan and dietary restriction in Caenorhabditis elegans. Aging Cell 4, 127-137.
13. Grzelak A, Macierzynska E, Bartosz G (2006) Accumulation of oxidative damage during replicative aging of the yeast Saccharomyces cerevisiae. Exp. Gerontol. 41, 813-818.
14. Harman D (1956) Aging: a theory based on free radical and radiation chemistry. J. Gerontol. 2, 298-300.
15. Houthoofd K, Braeckman BP, Johnson TE, Vanfleteren JR (2003) Life extension via dietary restriction is independent of the Ins/IGF-1 signalling pathway in Caenorhabditis elegans. Exp. Gerontol. 38, 947-954.
16. 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.
17. Hursting SD, Lavigne JA, Berrigan D, Perkins SN, Barrett JC (2003) Calorie restriction, aging, and cancer prevention: mechanisms of action and a applicability to humans. Annu. Rev. Med. 54, 131-152.
18. Jakubowski W, Bilinski T, Bartosz G (2000) Oxidative stress during aging of stationary cultures of the yeast Saccharomyces cerevisiae. Free Radic. Biol. Med. 28, 659-664.
19. Jiang JC, Jaruga E, Repnevskaya MV, Jazwinski SM (2000) An intervention resembling caloric restriction prolongs life span and retards aging in yeast. FASEB J. 14, 2135-2137.
20. Kirkwood TBL (2005) Understanding the odd science of aging. Cell 120, 437-447.
21. Kishi S, Bayliss PE, Uchiyama J, Koshimizu E, Qi J, Nanjappa P, Imamura S, Islam A, Neuberg D, Amsterdam A, Roberts TM (2008) The identification of Zebrafish mutants showing alterations in senescence-associated biomarkers. Plos Genet. 4, 18.
22. Klass MR (1977) Aging in nematode Caenorhabditis-elegans -major biological and environmental-factors influencing life-span. Mech. Ageing Dev. 6, 413-429.
23. Lee ET (1992) Statistical Methods for Survival Data Analysis. New York: Wiley. Lee JH, Park JW (2004) Role of thioredoxin peroxidase in aging of stationary cultures of Saccharomyces cerevisiae. Free Radic. Res. 38, 225-231.
24. Levine RL, Stadtman ER (2001) Oxidative modification of proteins during aging. Exp. Gerontol. 36, 1495-1502.
25. Li SY, Du M, Dolence EK, Fang CX, Mayer GE, Ceylan-Isik AF, LaCour KH, Yang XP, Wilbert CJ, Sreejayan N, Ren J (2005) Aging induces cardiac diastolic dysfunction, oxidative stress, accumulation of advanced glycation endproducts and protein modification. Aging Cell 4, 57-64.
26. Lin SJ, Ford E, Haigis M, Liszt G, Guarente L (2004) Calorie restriction extends yeast life span by lowering the level of NADH. Genes Dev. 18, 12-16.
27. Loeb J, Northrop J (1917) On the influence of food and temperature upon the duration of life. J. Biol. Chem. 32, 103-121.
28. Lu CY, He JC, Cai WJ, Liu HX, Zhu L, Vlassara H (2004) Advanced glycation endproduct (AGE) receptor 1 is a negative regulator of the inflammatory response to AGE in mesangial cells. Proc. Natl. Acad. Sci. USA. 101, 11767-11772.
29. Mair W, Goymer P, Pletcher SD, Partridge L (2003) Demography of dietary restriction and death in Drosophila. Science 301, 1731-1733.
30. Masoro EJ (2009) Caloric restriction-induced life extension of rats and mice: a critique of proposed mechanisms. Biochim. Biophys. Acta 1790, 1040-1048.
31. McKay CM, Maynard LA, Sperling G, Barnes LL (1935) The effect of retarded growth upon the length of life span and upon the ultimate body size. J. Nutr. 10, 63-79.
32. Miquel J, Tappel AL, Dillard CJ, Herman MM, Bensch KG (1974) Fluorescent products and lysosomal components in aging Drosophilamelanogaster. J. Gerontol. 29, 622-637.
33. Miquel J, Lundgren PR, Bensch KG, Atlan H (1976) Effects of temperature on life-span, vitality and fine-structure of Drosophila-melanogaster. Mech. Ageing Dev. 5, 347-370.
34. Mockett RJ, Sohal RS, Orr WC (1999) Overexpression of glutathione reductase extends survival in transgenic Drosophila melanogaster under hyperoxia but not normoxia. FASEB J. 13, 1733-1742.
35. Navarro A, Boveris A (2004) Rat brain and liver mitochondria develop oxidative stress and lose enzymatic activities on aging. Am. J. Physiol. Regul. Integr. Comp. Physiol. 287, R1244-R1249.
36. Oudes AJ, Herr CM, Olsen Y, Fleming JE (1998) Age-dependent accumulation of advanced glycation end-products in adult Drosophila melanogaster. Mech. Ageing Dev. 100, 221-229.
37. Pamplona R, Barja G (2007) Highly resistant macromolecular components and low rate of generation of endogenous damage: two key traits of longevity. Ageing Res. Rev. 6, 189-210.
38. Pamplona R, Portero-Otin M, Bellmunt MJ, Gredilla R, Barja G (2002) Aging increases N-epsilon-(Carboxymethyl)lysine and caloric restriction decreases N-epsilon-(Carboxyethyl)lysine and N-epsilon-(Malondialdehyde) lysine in rat heart mitochondrial proteins (vol 36, pg 47, 2002). Free Radic. Res. 36, U3-U3.
39. Pamplona R, Portero-Otin 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.
40. Pamplona R, Dalfo E, Ayala VR, Bellmunt MJ, Prat J, Ferrer I, Portero-Otin M (2005) Proteins in human brain cortex are modified by oxidation, glycoxidation, and lipoxidation -effects of Alzheimer disease and identification of lipoxidation targets. J. Biol. Chem. 280, 21522-21530.
41. Pansarasa O, Castagna L, Colombi B, Vecchiet J, Felzani G, Marzatico F (2000) Age and sex differences in human skeletal muscle: role of reactive oxygen species. Free Radic. Res. 33, 287-293.
42. Partridge L, Gems D (2002) Mechanisms of ageing: public or private? Nat. Rev. Genet. 3, 165-175.
43. Partridge L, Pletcher SD, Mair W (2005) Dietary restriction, mortality trajectories, risk and damage. Mech. Ageing Dev. 126, 35-41.
44. Pearl R (1928) The Rate of Living. New York: Knopf.
45. Pletcher SD (1999) Model fitting and hypothesis testing for age-specific mortality data. J. Evol. Biol. 12, 430-439.
46. Pletcher SD, Khazaeli AA, Curtsinger JW (2000) Why do life spans differ? Partitioning mean longevity differences in terms of age-specific mortality parameters. J. Gerontol. Ser. A-Biol. Sci. Med. Sci. 55, B381-B389.
47. Pletcher SD, Macdonald SJ, Marguerie R, Certa U, Stearns SC, Goldstein DB, Partridge L (2002) Genome-wide transcript profiles in aging and calorically restricted Drosophila melanogaster. Curr. Biol. 12, 712-723.
48. Portero-Otin M, Requena JR, Bellmunt MJ, Ayala V, Pamplona R (2004) Protein nonenzymatic modifications and proteasome activity in skeletal muscle from the short-lived rat and long-lived pigeon. Exp. Gerontol. 39, 1527-1535.
49. Requena JR, Fu MX, Ahmed MU, Jenkins AJ, Lyons TJ, Baynes JW, Thorpe SR (1997) Quantification of malondialdehyde and 4-hydroxynonenal adducts to lysine residues in native and oxidized human low-density lipoprotein. Biochem. J. 322, 317-325.
50. Reverter-Branchat G, Cabiscol E, Tamarit J, Ros J (2004) Oxidative damage to specific proteins in replicative and chronological-aged Saccharomyces cerevisiae -common targets and prevention by calorie restriction. J. Biol. Chem. 279, 31983-31989.
51. Sohal RS, Dubey A (1994) Mitochondrial oxidative damage, hydrogenperoxide release, and aging. Free Radic. Biol. Med. 16, 621-626.
52. Sohal RS, Sohal BH, Orr WC (1995) Mitochondrial superoxide and hydrogen-peroxide generation, protein oxidative damage, and longevity in different species of flies. Free Radic. Biol. Med. 19, 499-504.
53. Spindler SR (2005) Rapid and reversible induction of the longevity, anticancer and genomic effects of caloric restriction. Mech. Ageing Dev. 126, 960-966.
54. Stehouwer CDA, Gall MA, Twisk JWR, Knudsen E, Emeis JJ, Parving HH (2002) Increased urinary albumin excretion, endothelial dysfunction, and chronic low-grade inflammation in type 2 diabetes -progressive, interrelated, and independently associated with risk of death. Diabetes 51, 1157-1165.
55. Terman A, Brunk UT (2004) Aging as a catabolic malfunction. Int. J. Biochem. Cell Biol. 36, 2365-2375.
56. Thornalley PJ (1998) Cell activation by glycated proteins. AGE receptors, receptor recognition factors and functional classification of AGEs. Cell. Mol. Biol. 44, 1013-1023.
57. Traverso N, Patriarca S, Balbis E, Furfaro AL, Cottalasso D, Pronzato MA, Carlier P, Botta F, Marinari UM, Fontana L (2003) Anti malondialdehyde-adduct immunological response as a possible marker of successful aging. Exp. Gerontol. 38, 1129-1135.
58. Turturro A, Duffy P, Hass B, Kodell R, Hart R (2002) Survival characteristics and age-adjusted disease incidences in C57BL/6 mice fed a commonly used cereal-based diet modulated by dietary restriction. J. Gerontol. Ser. A-Biol. Sci. Med. Sci. 57, B379-B389.
59. Vijg J, Campisi J (2008) Puzzles, promises and a cure for ageing. Nature 454, 1065-1071.
60. Vittorini S, Paradiso C, Donati A, Cavallini G, Masini M, Gori Z, Pollera M, Bergamini E (1999) The age-related accumulation of protein carbonyl in rat liver correlates with the age-related decline in liver proteolytic activities. J. Gerontol. Ser. A-Biol. Sci. Med. Sci. 54, B318-B323.
61. Warner HR (2004) Current status of efforts to measure and modulate the biological rate of aging. J. Gerontol. Ser. A-Biol. Sci. Med. Sci. 59, 692-696.
62. Weindruch R, Walford RL (1982) Dietary restriction in mice beginning at 1 year of age -effect on life-span and spontaneous cancer incidence. Science 215, 1415-1418.
63. Weindruch R, Walford RL, Fligiel S, Guthrie D (1986) The retardation of aging in mice by dietary restriction -longevity, cancer, immunity and lifetime energy-intake. J. Nutr. 116, 641-654.
64. Wong R, Piper MDW, Blanc E, Partridge L (2008) Pitfalls of measuring feeding rate in the fruit fly Drosophila melanogaster. Nat. Methods 5, 214-215.
65. Wong R, Piper MDW, Wertheim B, Partridge L (2009) Quantification of food intake in Drosophila. PLoS ONE 4, e6063.
66. Yanase S, Yasuda K, Ishii N (2002) Adaptive responses to oxidative, damage in three mutants of Caenorhabditis elegans (age-1, mev-1 and daf-16) that affect life span. Mech. Ageing Dev. 123, 1579-1587.
67. Yasuda K, Adachi H, Fujiwara Y, Ishii N (1999) Protein carbonyl accumulation in aging Dauer formation-defective (daf) mutants of Caenorhabditis elegans. J. Gerontol. Ser. A-Biol. Sci. Med. Sci. 54, B47-B51.
68. Yin DZ (1996) Biochemical basis of lipofuscin, ceroid, and age pigment-like fluorophores. Free Radic. Biol. Med. 21, 871-888.