Extreme longevity is associated with increased resistance to oxidative stress in Arctica islandica, the longest-living non-colonial animal

Journals of Gerontology - Series A Biological Sciences and Medical Sciences

Volumn 66 A, Issue 7, 2011, Pages 741-750

  Ungvari, Zoltan ^a   Ridgway, Iain ^b   Philipp, Eva E R ^c   Campbell, Courtney M ^d   McQuary, Philip ^e   Chow, Tracy ^f   Coelho, Miguel ^g   Didier, Elizabeth S ^h   Gelino, Sara ^e   Holmbeck, Marissa A ⁱ   Kim, Insil ^j   Levy, Erik ^k   Sosnowska, Danuta ^a   Sonntag, William E ^a   Austad, Steven N ^l   Csiszar, Anna ^a  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b BANGOR UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF KIEL   (Germany)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e BURNHAM INSTITUTE   (United States)

^f UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^g MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^h TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

ⁱ BROWN UNIVERSITY   (United States)

^j CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^k Tecan Group Ltd   (United States)

^l Mays Cancer Center at UT Health San Antonio   (United States)

more..

Author keywords

Comparative biology; Free radical; Oxidative stress

Indexed keywords

ANIMALIA; ARCTICA ISLANDICA; BIVALVIA; MERCENARIA; MERCENARIA MERCENARIA;

ANTIOXIDANT; HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE; TERT BUTYL HYDROPEROXIDE;

AGING; ANIMAL; APOPTOSIS; ARTICLE; COMPARATIVE STUDY; DRUG EFFECT; LONGEVITY; MERCENARIA; METABOLISM; OXIDATIVE STRESS; PHYSIOLOGY;

AGING; ANIMALS; ANTIOXIDANTS; APOPTOSIS; HYDROGEN PEROXIDE; LONGEVITY; MERCENARIA; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; TERT-BUTYLHYDROPEROXIDE;

EID: 80051504960     PISSN: 10795006     EISSN: 1758535X     Source Type: Journal    
DOI: 10.1093/gerona/glr044     Document Type: Article

References (56)

1. Harman D. The biologic clock: the mitochondria? J Am Geriatr Soc. 1972;20:145-147.
2. Harman D. Aging: a theory based on free radical and radiation chemistry. J Gerontol. 1956;11:298-300.
3. Jang YC, Perez VI, Song W, et al. Overexpression of Mn superoxide dismutase does not increase life span in mice. J Gerontol A Biol Sci Med Sci. 2009;64:1114-1125.
4. Perez VI, Van Remmen H, Bokov A, Epstein CJ, Vijg J, Richardson A. The overexpression of major antioxidant enzymes does not extend the lifespan of mice. Aging Cell. 2009;8:73-75.
5. Sentman ML, Granstrom M, Jakobson H, Reaume A, Basu S, Marklund SL. Phenotypes of mice lacking extracellular superoxide dismutase and copper- and zinc-containing superoxide dismutase. J Biol Chem. 2006;281:6904-6909. (Pubitemid 43847452)
6. Mansouri A, Muller FL, Liu Y, et al. Alterations in mitochondrial function, hydrogen peroxide release and oxidative damage in mouse hind-limb skeletal muscle during aging. Mech Ageing Dev. 2006;127:298-306. (Pubitemid 43214503)
7. Van Remmen H, Ikeno Y, Hamilton M, et al. Life-long reduction in MnSOD activity results in increased DNA damage and higher incidence of cancer but does not accelerate aging. Physiol Genomics. 2003;16:29-37. (Pubitemid 38420018)
8. Wu S, Li Q, Du M, Li SY, Ren J. Cardiac-specific overexpression of catalase prolongs lifespan and attenuates ageing-induced cardiomyocyte contractile dysfunction and protein damage. Clin Exp Pharmacol Physiol. 2007;34:81-87. (Pubitemid 46069590)
9. Mele J, Van Remmen H, Vijg J, Richardson A. Characterization of transgenic mice that overexpress both copper zinc superoxide dismutase and catalase. Antioxid Redox Signal. 2006;8:628-638. (Pubitemid 43741331)
10. Lambert AJ, Boysen HM, Buckingham JA, et al. Low rates of hydrogen peroxide production by isolated heart mitochondria associate with long maximum lifespan in vertebrate homeotherms. Aging Cell. 2007;6:607-618. (Pubitemid 47400043)
11. 2 and H2O2 production, and vascular oxidative stress resistance between the longest-living rodent, the naked mole rat, and mice. Am J Physiol. 2006;291:H2698-H2704. (Pubitemid 44904069)
12. Sohal RS, Ku HH, Agarwal S. Biochemical correlates of longevity in two closely related rodent species. Biochem Biophys Res Commun. 1993;196:7-11. (Pubitemid 23309467)
13. Ogburn CE, Carlberg K, Ottinger MA, Holmes DJ, Martin GM, Austad SN. Exceptional cellular resistance to oxidative damage in long-lived birds requires active gene expression. J Gerontol Biol Sci. 2001;56:B468-B474. (Pubitemid 33043470)
14. Perez-Campo R, Lopez-Torres M, Cadenas S, Rojas C, Barja G. The rate of free radical production as a determinant of the rate of aging: evidence from the comparative approach. J Comp Physiol B. 1998;168:149-158. (Pubitemid 28202995)
15. Wanamaker AD, Heinemeier J, Scourse JD, et al. Very long-lived molluscs confirm 17th century AD tephra-based radiocarbon reservoir ages for north Icelandic shelf waters. Radiocarbon. 2008;50:1-14.
16. Abele D, Strahl J, Brey T, Philipp EE. Imperceptible senescence: ageing in the ocean quahog Arctica islandica. Free Radic Res. 2008;42:474-480. (Pubitemid 351935161)
17. Strahl J, Philipp EE, Brey T, Broeg K, Abele D. Physiological aging in the Icelandic population of the ocean quahog Arctica islandica. Aquat Biol. 2007;1:77-84.
18. Abele D, Brey T, Philipp E. Bivalve models of aging and the determination of molluscan lifespans. Exp Gerontol. 2009;44:307-315.
19. Ridgway ID, Richardson CA. Arctica islandica: the longest lived non colonial animal known to science. Rev Fish Biol Fisheries. 2010. doi: 10.1007/s11160-11010-19171-11169.
20. Philipp EE, Abele D. Masters of longevity: lessons from long-lived bivalves-a mini-review. Gerontology. 2010;56:55-65.
21. Thórarinsdóttir GG, Einarsson ST. Distribution, abundance, population structure and meat yield of the ocean quahog, Arctica islandica, in Icelandic waters. J Mar Biol Assoc UK. 1996;76:1107-1114.
22. Peterson CH. Quantitative allometry of gamete production by Mercenaria mercenaria into old age. Mar Ecol Prog Ser. 1986;29:93-97.
23. Plisetskaya E, Kazakov VK, Soltitskaya L, Leibson LG. Insulin-producing cells in the gut of freshwater bivalve molluscs Anodonta cygnea and Unio pictorum and the role of insulin in the regulation of their carbohydrate metabolism. Gen Comp Endocrinol. 1978;35:133-145. (Pubitemid 8368816)
24. Ridgway ID, Richardson CA, Austad SN. Maximum shell size, growth rate and maturation age correlate with longevity in bivalve molluscs. J Gerontol Biol Sci. 2010;66:183-190.
25. Krug AW, Allenhofer L, Monticone R, et al. Elevated mineralocorticoid receptor activity in aged rat vascular smooth muscle cells promotes a proinflammatory phenotype via extracellular signal-regulated kinase 1/2 mitogen-activated protein kinase and epidermal growth factor receptor-dependent pathways. Hypertension. 2010;55:1476-1483.
26. Philipp E, Brey T, Portner HO, Abele D. Chronological and physiological ageing in a polar and a temperate mud clam. Mech Ageing Dev. 2005;126:598-609. (Pubitemid 40461959)
27. Strahl J, Abele D. Cell turnover in tissues of the long-lived ocean quahog Arctica islandica and the short-lived scallop Aequipecten opercularis. Mar Biol. 2010;157:1283-1290.
28. Philipp E, Heilmayer O, Brey T, Abele D, Portner HO. Physiological ageing in a polar and a temperate swimming scallop. Mar Ecol Prog Ser. 2006;307:187-198. (Pubitemid 43294009)
29. Philipp E, Portner HO, Abele D. Mitochondrial ageing of a polar and a temperate mud clam. Mech Ageing Dev. 2005;126:610-619. (Pubitemid 40461960)
30. Csiszar A, Labinskyy N, Zhao X, et al. Vascular superoxide and hydrogen peroxide production and oxidative stress resistance in two closely related rodent species with disparate longevity. Aging Cell. 2007;6:783-797. (Pubitemid 350131047)
31. Csiszar A, Labinskyy N, Orosz Z, Xiangmin Z, Buffenstein R, Ungvari Z. Vascular aging in the longest-living rodent, the naked mole rat. Am J Physiol. 2007;293:H919-H927. (Pubitemid 47254187)
32. Ungvari Z, Csiszar A, Huang A, Kaminski PM, Wolin MS, Koller A. High pressure induces superoxide production in isolated arteries via protein kinase C-dependent activation of NAD(P)H oxidase. Circulation. 2003;108:1253-1258. (Pubitemid 37099996)
33. Csiszar A, Labinskyy N, Perez V, et al. Endothelial function and vascular oxidative stress in long-lived GH/IGF-deficient Ames dwarf mice. Am J Physiol Heart Circ Physiol. 2008;295:H1882-H1894.
34. Csiszar A, Ungvari Z, Koller A, Edwards JG, Kaley G. Proinflammatory phenotype of coronary arteries promotes endothelial apoptosis in aging. Physiol Genomics. 2004;17:21-30. (Pubitemid 38924147)
35. Ungvari Z, Orosz Z, Rivera A, et al. Resveratrol increases vascular oxidative stress resistance. Am J Physiol. 2007;292:H2417-H2424. (Pubitemid 47084624)
36. Perez VI, Buffenstein R, Masamsetti V, et al. Protein stability and resistance to oxidative stress are determinants of longevity in the longest-living rodent, the naked mole-rat. Proc Natl Acad Sci U S A. 2009;106:3059-3064.
37. Brunet Rossinni AK. Testing the free radical theory of aging in bats. Ann N Y Acad Sci. 2004;1019:506-508.
38. Brunet-Rossinni AK. Reduced free-radical production and extreme longevity in the little brown bat (Myotis lucifugus) versus two non-flying mammals. Mech Ageing Dev. 2004;125:11-20. (Pubitemid 38054347)
39. Brunet-Rossinni AK, Austad SN. Ageing studies on bats: a review. Biogerontology. 2004;5:211-222. (Pubitemid 39157986)
40. Ku HH, Brunk UT, Sohal RS. Relationship between mitochondrial superoxide and hydrogen peroxide production and longevity of mammalian species. Free Radic Biol Med. 1993;15:621-627. (Pubitemid 23353411)
41. Ulrich PN, Marsh AG. Thermal sensitivity of mitochondrial respiration efficiency and protein phosphorylation in the clam Mercenaria mercenaria. Mar Biotechnol (NY). 2009;11:608-618.
42. Abele D, Heise K, Portner HO, Puntarulo S. Temperature-dependence of mitochondrial function and production of reactive oxygen species in the intertidal mud clam Mya arenaria. J Exp Biol. 2002;205:1831-1841. (Pubitemid 34853435)
43. Austad SN. An experimental paradigm for the study of slowly aging organisms. Exp Gerontol. 2001;36:599-605. (Pubitemid 32273406)
44. Kapahi P, Boulton ME, Kirkwood TB. Positive correlation between mammalian life span and cellular resistance to stress. Free Radic Biol Med. 1999;26:495-500. (Pubitemid 29146251)
45. Lithgow GJ, Walker GA. Stress resistance as a determinate of C. elegans lifespan. Mech Ageing Dev. 2002;123:765-771. (Pubitemid 34178489)
46. Harper JM, Salmon AB, Leiser SF, Galecki AT, Miller RA. Skin-derived fibroblasts from long-lived species are resistant to some, but not all, lethal stresses and to the mitochondrial inhibitor rotenone. Aging Cell. 2007;6:1-13. (Pubitemid 46140135)
47. Buttemer WA, Abele D, Constantini D. From bivalves to birds: oxidative stress and longevity. Funct Ecol. 2010;24:971-983.
48. Salmon AB, Leonard S, Masamsetti V, et al. The long lifespan of two bat species is correlated with resistance to protein oxidation and enhanced protein homeostasis. FASEB J. 2009;23:2317-2326.
49. Ferrington DA, Husom AD, Thompson LV. Altered proteasome structure, function, and oxidation in aged muscle. FASEB J. 2005;19:644-646. (Pubitemid 40471272)
50. Rodriguez KA, Gaczynska M, Osmulski PA. Molecular mechanisms of proteasome plasticity in aging. Mech Ageing Dev. 2010;131:144-155.
51. Dasuri K, Zhang L, Ebenezer P, Liu Y, Fernandez-Kim SO, Keller JN. Aging and dietary restriction alter proteasome biogenesis and composition in the brain and liver. Mech Ageing Dev. 2009;130:777-783.
52. Bulteau AL, Szweda LI, Friguet B. Age-dependent declines in proteasome activity in the heart. Arch Biochem Biophys. 2002;397:298-304. (Pubitemid 34852295)
53. Gavilan MP, Pintado C, Gavilan E, et al. Dysfunction of the unfolded protein response increases neurodegeneration in aged rat hippocampus following proteasome inhibition. Aging Cell. 2009;8:654-665.
54. Marfella R, Di Filippo C, Laieta MT, et al. Effects of ubiquitin-proteasome system deregulation on the vascular senescence and atherosclerosis process in elderly patients. J Gerontol A Biol Sci Med Sci. 2008;63:200-203. (Pubitemid 351738453)
55. Salway KD, Page MM, Faure PA, Burness G, Stuart JA. Enhanced protein repair and recycling are not correlated with longevity in 15 vertebrate endotherm species. Age (Dordr). 2010;33:33-47.
56. Ivanina A, Sokolova I, Sukhotin A. Expression of heat shock proteins in aging bivalve mollusks. FASEB J. 2008;22:1239.1231(abstract).