Enhanced protein repair and recycling are not correlated with longevity in 15 vertebrate endotherm species
Tóm tắt
Previous studies have shown that longevity is associated with enhanced cellular stress resistance. This observation supports the disposable soma theory of aging, which suggests that the investment made in cellular maintenance will be proportional to selective pressures to extend lifespan. Maintenance of protein homeostasis is a critical component of cellular maintenance and stress resistance. To test the hypothesis that enhanced protein repair and recycling activities underlie longevity, we measured the activities of the 20S/26S proteasome and two protein repair enzymes in liver, heart and brain tissues of 15 different mammalian and avian species with maximum lifespans (MLSP) ranging from 3 to 30 years. The data set included Snell dwarf mice, in which lifespan is increased by ∼50% compared to their normal littermates. None of these activities in any of the three tissues correlated positively with MLSP. In liver, 20S/26S proteasome and thioredoxin reductase (TrxR) activities correlated negatively with body mass. In brain tissue, TrxR was also negatively correlated with body mass. Glutaredoxin (Grx) activity in brain was negatively correlated with MLSP and this correlation remained after residual analysis to remove the effects of body mass, but was lost when the data were analysed using Felsenstein’s independent contrasts. Snell dwarf mice had marginally lower 20S proteasome, TrxR and Grx activities than normal controls in brain, but not heart tissue. Thus, increased longevity is not associated with increased protein repair or proteasomal degradation capacities in vertebrate endotherms.
Tài liệu tham khảo
Arner ESJ (2009) Focus on mammalian thioredoxin reductases—important selenoproteins with versatile functions. Biochim Biophys Acta 1790:495–526
Arner ES, Zhong L, Holmgren A (1999) Preparation and assay of mammalian thioredoxin and thioredoxin reductase. Meth Enzymol 300:226–239
Bader M, Steller H (2009) Regulation of cell death by the ubiquitin–proteasome system. Curr Opin Cell Biol 21:878–884
Barja G, Herrero A (2000) Oxidative damage to mitochondrial DNA is inversely related to maximum life span in the heart and brain of mammals. FASEB J 14:312–318
Boffoli D, Scacco SC, Vergari R, Solarino G, Santacroce G, Papa S (1994) Decline with age of the respiratory chain activity in human skeletal muscle. Biochim Biophys Acta 1226:73–82
Bokov A, Lindsey M, Khodr C, Sabia M, Richardson A (2009) Long-lived Ames dwarf mice are resistant to chemical stressors. J Gerontol A Biol Sci Med Sci 64A:819–827
Daulney A, Tansey WP (2009) Damage control: DNA repair, transcription, and the ubiquitin–proteasome system. DNA Repair 8:444–448
Davies KJ (2001) Degradation of oxidized proteins by the 20S proteasome. Biochimie 83:301–310
de Magalhães JP, Costa J, Toussaint O (2005) HAGR: the human ageing genomic resources. Nucleic Acids Res 33:D537–D543
Divald A, Powell SR (2006) Proteasome mediates removal of proteins oxidized during myocardial ischemia. Free Radic Biol Med 40:156–164
Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15
Ghazi A, Henis-Korenblit S, Kenyon C (2007) Regulation of Caenorhabditis elegans lifespan by a proteasomal E3 ligase complex. PNAS 104:5947–5952
Gorbunova V, Bozzella MJ, Seluanov A (2008) Rodents for comparative aging studies: from mice to beavers. Age 30:111–119
Grune T, Blasig IE, Sitte N, Roloff B, Haseloff R, Davies KJ (1998) Peroxynitrite increases the degradation of aconitase and other cellular proteins by proteasome. J Biol Chem 273:10857–10862
Grune T, Jung T, Merker K, Davies KJ (2004) Decreased proteolysis caused by protein aggregates, inclusion bodies, plaques, lipofuscin, ceroid, and ‘aggresomes’ during oxidative stress, aging, and disease. Int J Biochem Cell Biol 36:2519–2530
Hackett SJ, Kimball RT, Reddy S, Bowie RCK, Braun EL, Braun MJ, Chojnowski JL, Cox WA, Han K-L, Harshman J, Huddleston CJ, Marks BD, Miglia KJ, Moore WS, Sheldon FH, Steadman DW, Witt CC, Yuri T (2008) A phylogenomic study of birds reveals their evolutionary history. Science 320:1763–1768
Hershko A, Ciechanover A (1998) The ubiquitin system. Annu Rev Biochem 67:425–479
Holzenberger M, Dupont J, Ducos B, Leneuve P, Geloen A, Even PC, Cervera P, Le Bouc Y (2003) IGF-1 receptor regulates lifespan and resistance to oxidative stress in mice. Nature 421:182–187
Ideker T, Thorsson V, Ranish J, Christmas R, Buhler J, Eng J, Bumgarner R, Goodlett D, Aebersold R, Hood L (2001) Integrated genomic and proteomic analyses of a systematically perturbed metabolic network. Science 292:929–934
Jung T, Catalgol B, Grune T (2009) The proteasomal system. Mol Aspects Med 30:191–296
Kapahi P, Boulton ME, Kirkwood TBL (1999) Positive correlation between mammalian life span and cellular resistance to stress. Free Radic Biol Med 26:495–500
Kirkwood T, Kapahi P, Shanley D (2000) Evolution, stress and longevity. J Anat 197:587–590
Kumar S, Holmgren A (1999) Induction of thioredoxin, thioredoxin reductase and glutaredoxin activity in mouse skin by TPA, a calcium ionophore and other tumor promoters. Carcinogenesis 22:1761–1767
Le Naour F, Hohenkirk L, Grolleau A, Misek D, Lescure P, Geiger J, Hanash S, Beretta L (2001) Profiling changes in gene expression during differentiation and maturation of monocyte-derived dendritic cells using both oligonucleotide microarrays and proteomics. J Biol Chem 276:17920–17931
Lofgren S, Fernando MR, Xing KY, Wang Y, Kuszynski CA, Ho YS, Lou MF (2008) Effect of thioltransferase (glutaredoxin) deletion on cellular sensitivity to oxidative stress and cell proliferation in lens epithelial cells of thioltransferase knockout mice. IOVS 49:4497–4505
Martinez A, Portero-Otin M, Pamplona R, Ferrer I (2008) Protein targets of oxidative damage in human neurodegenerative diseases with abnormal protein aggregates. Brain Pathol 20:281–297
Maynard S, Miller R (2006) Fibroblasts from long-lived Snell dwarf mice are resistant to oxygen-induced in vitro growth arrest. Aging Cell 5:89–96
Miller RA, Williams J, Kiklevich JV, Austad S, Harper JM (2010) Comparative cellular biogerontology: primer and prospectus. Ageing Res Rev (in press). doi:10.1016/j.arr.2010.01.002
Miranda-Vizuete A, Gonzalez J, Gahmon G, Burghoorn J, Navas P, Swoboda P (2005) Lifespan decrease in Caenorhabditis elegans mutant lacking TRX-1, a thioredoxin expressed in ASJ sensory neurons. FEBS Lett 580:484–490
Moosmann B, Behl C (2008) Mitochondrially encoded cysteine predicts animal lifespan. Aging Cell 7:32–46
Morimoto RI (2008) Proteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging. Genes Dev 22:1427–1438
Navarro A, Boveris A (2007) The mitochondrial energy transduction system and the aging process. Am J Physiol Cell Physiol 292:C670–C686
Ngo J, Davies K (2009) Mitochondrial Lon protease is a human stress protein. Free Radic Biol Med 46:1042–1048
Ogburn C, Carlberg K, Ottinger MA, Holmes D, Martin GM, Austad SN (2001) Exceptional cellular resistance to oxidative damage in long-lived birds requires active gene expression. J Gerontol (Bio Sci) 56A:B468–B474
Page MM, Peters CW, Staples JF, Stuart JA (2009) Intracellular superoxide dismutases are not altered during hibernation in the 13-lined ground squirrel Spermophilus tridecemlineatus. Comp Biochem Physiol A Mol Integr Physiol 152:115–122
Page M, Richardson J, Wiens B, Tiedtke E, Peters C, Faure P, Burness G, Stuart JA (2010a) Antioxidant enzyme activities are not broadly correlated with longevity in 14 vertebrate endotherm species. Age (Dordr) 32(2):255–270
Page M, Robb E, Salway K, Stuart J (2010b) Mitochondrial redox metabolism: aging, longevity and dietary effects. Mech Ageing Dev 131:242–252
Perez V, Buffenstein R, Masamsetti V, Leonard S, Salmon AB, Mele J, Andziak B, Yang T, Edrey Y, Friguet B, Ward W, Richardson A, Chaudhuri A (2009a) Protein stability and resistance to oxidative stress are determinants of longevity in the longest-living rodent, naked mole-rat. Proc Natl Acad Sci U S A 106:3059–3064
Perez V, Bokov A, Van Remmen H, Mele J, Ran Q, Ikeno Y, Richardson A (2009b) Is the oxidative stress theory of aging dead? Biochim Biophys Acta 1790:1005–1014
Prasad AB, Allard MW, Green ED, NISC Comparative Sequencing Program (2008) Confirming the phylogeny of mammals by use of large comparative sequence data sets. Mol Biol Evol 25:1795–1808
Price T (1997) Correlated evolution and independent contrasts. Philos Trans R Soc Lond B Bio Sci 352:519–529
Reinheckel T, Sitte N, Ullrich O, Kuckelkorn U, Davies KJ, Grune T (1998) Comparative resistance of the 20S and 26S proteasome to oxidative stress. Biochem J 335:637–642
Robb E, Page M, Stuart J (2009) Mitochondria, cellular stress resistance, somatic cell depletion and lifespan. Curr Ageing Sci 16:12–27
Rodgers KJ, Dean RT (2003) Assessment of proteasome activity in cell lysates and tissue homogenates using peptide substrates. Int J Biochem Cell Biol 35:716–727
Salmon AB, Murakami S, Bartke A, Kopchick J, Yasumura K, Miller RA (2005) Fibroblast cell lines from young adult mice of long-lived mutant strains are resistant to multiple forms of stress. Am J Physiol Endocrinol Metab 289:E23–E29
Salmon AB, Leonard S, Masamsetti V, Pierce A, Podlutsky A, Podlutskaya N, Richardson A, Austad S, Chaudhuri A (2009) The long lifespan of two bat species is correlated with resistance to protein oxidation and enhanced protein oxidation. FASEB J 23:2317–2326
Speakman JR (2005) Correlations between physiology and lifespan—two widely ignored problems with comparative studies. Aging Cell 4:167–175
Springer MS, Murphy WJ (2007) Mammalian evolution and biomedicine: new views from phylogeny. Biol Rev 82:375–392
Stuart GW, Moffett K, Leader JJ (2002) A comprehensive vertebrate phylogeny using vector representations of protein sequences from whole genomes. Mol Biol Evol 19:554–562
Swindell W, Masternak M, Kopchick J, Conover C, Bartke A, Miller R (2009) Endocrine regulation of heat shock protein mRNA levels in long-lived dwarf mice. Mech Ageing Dev 130:393–400
Torres CA, Perez VI (2008) Proteasome modulates mitochondrial function during cellular senescence. Free Radic Biol Med 44:403–414