Fibroblasts from long-lived bird species are resistant to multiple forms of stress

Journal of Experimental Biology

Volumn 214, Issue 11, 2011, Pages 1902-1910

  Harper, James M ^a,b   Wang, Min ^a,b   Galecki, Andrzej T ^b   Ro, Jennifer ^c   Williams, Joseph B ^c   Miller, Richard A ^a,b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

Evolution; Fibroblast; Longevity; Oxidation; Stress

Indexed keywords

CADMIUM; HERBICIDE; HYDROGEN PEROXIDE; MESYLIC ACID METHYL ESTER; PARAQUAT;

ANIMAL; ARTICLE; BIRD; CELL CULTURE; DRUG EFFECT; FIBROBLAST; LONGEVITY; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; RADIATION EXPOSURE; ULTRAVIOLET RADIATION;

ANIMALS; BIRDS; CADMIUM; CELLS, CULTURED; FIBROBLASTS; HERBICIDES; HYDROGEN PEROXIDE; LONGEVITY; METHYL METHANESULFONATE; PARAQUAT; STRESS, PHYSIOLOGICAL; ULTRAVIOLET RAYS;

AVES; MAMMALIA; RODENTIA;

EID: 79957519364     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.054643     Document Type: Article

References (68)

1. Abouheif, E. (1999). A method for testing the assumption of phylogenetic independence in comparative data. Evol. Ecol. Res. 1, 895-909. (Pubitemid 129551969)
2. Austad, S. N. (2005). Diverse aging rates in metazoans: targets for functional genomics. Mech. Ageing Dev. 126, 43-49. (Pubitemid 40018476)
3. Austad, S. N. (2010). Methusaleh's zoo: how nature provides us with clues for extending human health span. J. Comp. Pathol. 142, S10-S21.
4. Austad, S. N. and Fischer, K. E. (1991). Mammalian aging, metabolism, and ecology: evidence from the bats and marsupials. J. Gerontol. 46, B47-B53.
5. Barja, G. and Herrero, A. (1998). Localization at complex I and mechanism of the higher free radical production of brain nonsynaptic mitochondria in the short-lived rat than in the longevous pigeon. J. Bioenerg. Biomembr. 30, 235-243. (Pubitemid 28405165)
6. Barja, G. and 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. (Pubitemid 30086068)
7. Barker, F. K., Cibois, A., Schikler, P., Feinstein, J. and Cracraft, J. (2004). Phylogeny and diversification of the largest avian radiation. Proc. Natl. Acad. Sci. USA 101, 11040-11045. (Pubitemid 38992336)
8. Blomberg, S. P., Garland, T., Jr and Ives, A. R. (2003). Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57, 717-745. (Pubitemid 36579712)
9. Brennan, R. J. and Schiestl, R. H. (1996). Cadmium is an inducer of oxidative stress in yeast. Mutat. Res. 356, 171-178. (Pubitemid 26302887)
10. Busuttil, R. A., Rubio, M., Dolle, M. E., Campisi, J. and Vijg, J. (2003). Oxygen accelerates the accumulation of mutations during the senescence and immortalization of murine cells in culture. Aging Cell 2, 287-294.
11. Buttemer, W. A., Battam, H. and Hulbert, A. J. (2008). Fowl play and the price of petrel: long-living Procellariiformes have peroxidation-resistant membrane composition compared with short-living Galliformes. Biol. Lett. 4, 351-354. (Pubitemid 351961488)
12. Charlesworth, B. (1993). Evolutionary mechanisms of senescence. Genetica 91, 11-19.
13. Diaz-Uriarte, R. and Garland, T., Jr (1996). Testing hypotheses of correlated evolution using phylogenetically independent contrasts: sensitivity to deviations from Brownian motion. Syst. Biol. 45, 27-47.
14. Donne-Goussé, C., Laudet, V. and Hänni, C. (2002). A molecular phylogeny of anseriformes based on mitochondrial DNA analysis. Mol. Phylogenet. Evol. 23, 339-356. (Pubitemid 34749754)
15. Faulks, S., Turner, N., Else, P. and Hulbert, A. (2006). Calorie restriction in mice: effects on body composition, daily activity, metabolic rate, mitochondrial reactive oxygen species production, and membrane fatty acid composition. J. Gerontol. A Biol. Sci. Med. Sci. 61, 781-794. (Pubitemid 44260160)
16. Figueiredo-Pereira, M. E., Yakushin, S. and Cohen, G. (1998). Disruption of the intracellular sulfhydryl homeostasis by cadmium-induced oxidative stress leads to protein thiolation and ubiquitination in neuronal cells. J. Biol. Chem. 273, 12703-12709. (Pubitemid 28246821)
17. Freckleton, R. P., Harvey, P. H. and Pagel, M. (2002). Phylogenetic analysis and comparative data: a test and review of evidence. Am. Nat. 160, 712-726. (Pubitemid 36035851)
18. Garland, T., Jr, Harvey, P. H. and Ives, A. R. (1992). Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst. Biol. 41, 18-32.
19. Garland, T., Jr, Bennett, A. F. and Rezende, E. L. (2005). Phylogenetic approaches in comparative physiology. J. Exp. Biol. 208, 3015-3035. (Pubitemid 41345680)
20. Harper, J. M., Durkee, S. J., Dysko, R., Austad, S. N. and Miller, R. A. (2006). Genetic modulation of hormone levels and life span in hybrids between laboratory and wild-derived mice. J. Gerontol. Biol. Med. Sci. 61, 1019-1029. (Pubitemid 44727209)
21. Harper, J. M., Salmon, A. B., Leiser, S. F., Galecki, A. T. and Miller, R. A. (2007). Skin-derived fibroblasts from long-lived species are resistant to some, but not all, lethal stresses and to the mitochondrial inhibitor rotenone. Aging Cell 6, 1-13. (Pubitemid 46140135)
22. Herrero, A. and Barja, G. (1999). 8-oxo-deoxyguanosine levels in heart and brain mitochondrial and nuclear DNA of two mammals and three birds in relation to their different rates of aging. Aging 11, 294-300.
23. Holmes, D. and Martin, K. (2009). A bird's-eye view of aging: what's in it for the ornithologist? Auk 126, 1-23.
24. Holmes, D. J. and Ottinger, M. A. (2003). Birds as long-lived animal models for the study of aging. Exp. Gerontol. 38, 365-375.
25. Hulbert, A. (2008). Explaining longevity of different animals: is membrane fatty acid composition the missing link? Age 30, 89-97.
26. Hulbert, A. J., Faulks, S. C., Harper, J. M., Miller, R. A. and Buffenstein, R. (2006). Extended longevity of wild-derived mice is associated with peroxidation-resistant membranes. Mech. Ageing Dev. 127, 653-657.
27. Hulbert, A. J., Pamplona, R., Buffenstein, R. and Buttemer, W. A. (2007). Life and death: metabolic rate, membrane composition, and life span of animals. Physiol. Rev. 87, 1175-1213. (Pubitemid 350033823)
28. Hulbert, A. J., Beard, L. A. and Grigg, G. C. (2008). The exceptional longevity of an egg-laying mammal, the short-beaked echidna (Tachyglossus aculeatus) is associated with peroxidation-resistant membrane composition. Exp. Gerontol. 43, 729-733.
29. Ives, A. R., Midford P. E. and Garland, T., Jr (2007). Within-species variation and measurement error in phylogenetic comparative methods. Syst. Biol. 56, 252-270.
30. Johnson, K. P. and Sorenson, M. D. (1999). Phylogeny and biogeography of dabbling ducks (genus: Anas): a comparison of molecular and morphological evidence. Auk 116, 792-805. (Pubitemid 29375475)
31. Kapahi, P., Boulton, M. E. and Kirkwood, T. B. (1999). Positive correlation between mammalian life span and cellular resistance to stress. Free Radic. Biol. Med. 26, 495-500. (Pubitemid 29146251)
32. Kirkwood, T. B. L. (2002). Evolution of ageing. Mech. Ageing Dev. 123, 737-745. (Pubitemid 34178486)
33. Klicka, J., Johnson, K. and Lanyon, S. (2000). New world nine-primaried oscine relationships: Constructing a mitochondrial DNA framework. Auk 117, 321-336. (Pubitemid 30231265)
34. Lambert, A. J., Boysen, H. M., Buckingham, J. A., Yang, T., Podlutsky, A., Austad, S. N., Kunz, T. H., Buffenstein, R. and Brand, M. D. (2007). Low rates of hydrogen peroxide production by isolated heart mitochondria associate with long maximum lifespan in vertebrate homeotherms. Aging Cell 6, 607-618. (Pubitemid 47400043)
35. Leiser, S. F. and Miller, R. A. (2009). Nrf2 signaling, a mechanism for cellular stress resistance in long-lived mice. Mol. Cell. Biol. 30, 871-884.
36. Leiser, S. F., Salmon, A. B. and Miller, R. A. (2006). Correlated resistance to glucose deprivation and cytotoxic agents in fibroblast cell lines from long-lived pituitary dwarf mice. Mech. Ageing Dev. 127, 821-829. (Pubitemid 44602138)
37. Lithgow, G. J. and Miller, R. A. (2008). Determination of aging rate by coordinated resistance to multiple forms of stress. In Cold Spring Harbor Monograph Archive, Vol. 51 (ed. L. P. Guarente, L. Partridge and D. C. Wallace) pp. 427-481. Cold Spring Harbor Laboratory Press: North America.
38. Lorenzini, A., Tresini, M., Austad, S. N. and Cristofalo, V. J. (2005). Cellular replicative capacity correlates primarily with species body mass not longevity. Mech. Ageing Dev. 126, 1130-1133. (Pubitemid 41253865)
39. Maddison, W. P. and Maddison, D. R. (2010). Mesquite: a modular system for evolutionary analysis. Version 2. 73 http://mesquiteproject.org.
40. Maynard, S. P. and Miller, R. A. (2006). Fibroblasts from long-lived Snell dwarf mice are resistant to oxygen-induced in vitro growth arrest. Aging Cell 5, 89-96. (Pubitemid 43348966)
41. Medawar, P. and Wolstenhilme, G. E. W. (1955). The definition and measurement of senescence. In Ciba Foundation Colloquia on Ageing, Vol. 1 (ed. G. E. W. Wolstenholme and M. P. Cameron), pp. 4-15. London: J. & A. Churchill.
42. Miller, R. A., Harper, J. M., Dysko, R., Durkee, S. J. and Austad, S. N. (2002). Longer life spans and delayed maturation in wild-derived mice. Exp. Biol. Med. 227, 500-508.
43. Miller, R. A., Williams, J. B., Kiklevich, J. V., Austad, S. and Harper, J. M. (2011). Comparative cellular biogerontology: primer and prospectus. Ageing Res. Rev. 10, 181-190.
44. Mitchell, T. W., Buffenstein, R. and Hulbert, A. J. (2007). Membrane phospholipid composition may contribute to exceptional longevity of the naked mole-rat (Heterocephalus glaber): a comparative study using shotgun lipidomics. Exp. Gerontol. 42, 1053-1062. (Pubitemid 47633462)
45. Mizumoto, K., Glascott, P. A., Jr and Farber, J. L. (1993). Roles for oxidative stress and poly(ADP-ribosyl)ation in the killing of cultured hepatocytes by methyl methanesulfonate. Biochem. Pharmacol. 46, 1811-1818. (Pubitemid 23349030)
46. Murakami, S. (2006). Stress resistance in long-lived mouse models. Exp. Gerontol. 41, 1014-1019. (Pubitemid 44821697)
47. Murakami, S., Salmon, A. B. and Miller, R. A. (2003). Multiplex stress resistance in cells from long-lived dwarf mice. FASEB J. 17, 1565-1566.
48. Ogburn, C. E., Austad, S. N., Holmes, D. J., Kiklevich, J. V., Gollahon, K., Rabinovitch, P. S. and Martin, G. M. (1998). Cultured renal epithelial cells from birds and mice: enhanced resistance of avian cells to oxidative stress and DNA damage. J. Gerontol. Biol. Med. Sci. 53, B287-B292. (Pubitemid 28354737)
49. Ogburn, C. E., Carlberg, K., Ottinger, M. A., Holmes, D. J., Martin, G. M. and Austad, S. N. (2001). Exceptional cellular resistance to oxidative damage in longlived birds requires active gene expression. J. Gerontol. Biol. Med. Sci. 56, B468-B474. (Pubitemid 33043470)
50. Pamplona, R., Portero-Otin, M., Sanz, A., Ayala, V., Vasileva, E. and Barja, G. (2005). Protein and lipid oxidative damage and complex I content are lower in the brain of budgerigar and canaries than in mice. Relation to aging rate. Age 27, 267-280. (Pubitemid 43971780)
51. Parrinello, S., Samper, E., Krtolica, A., Goldstein, J., Melov, S. and Campisi, J. (2003). Oxygen sensitivity severely limits the replicative lifespan of murine fibroblasts. Nat. Cell Biol. 5, 741-747. (Pubitemid 36986782)
52. Price, T. (1997). Correlated evolution and independent contrasts. Philos. Trans. R. Soc. Lond. B 352, 11.
53. Reznick, D. N. and Ricklefs, R. E. (2009). Darwin's bridge between microevolution and macroevolution. Nature 457, 837-842.
54. Ricklefs, R. E. (2010). Insights from comparative analyses of aging in birds and mammals. Aging Cell 9, 273-284.
55. Ricklefs, R. E. and Starck, J. M. (1996). Applications of phylogenetically independent contrasts: a mixed progress report. Oikos 77, 167-172. (Pubitemid 27088350)
56. Salmon, A. B., Murakami, S., Bartke, A., Kopchick, J., Yasumura, K. and Miller, R. A. (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. (Pubitemid 40874930)
57. Salmon, A. B., Akha, A. A. S., Buffenstein, R. and Miller, R. A. (2008a). Fibroblasts from naked mole-rats are resistant to multiple forms of cell injury, but sensitive to peroxide, ultraviolet light, and endoplasmic reticulum stress. J. Gerontol. A Biol. Sci. Med. Sci. 63, 232-241. (Pubitemid 351738427)
58. Salmon, A. B., Ljungman, M. and Miller, R. A. (2008b). Cells from long-lived mutant mice exhibit enhanced repair of ultraviolet lesions. J. Gerontol. A Biol. Sci. Med. Sci. 63, 219-231. (Pubitemid 351738426)
59. Seluanov, A., Chen, Z., Hine, C., Sasahara, T. H. C., Ribeiro, A. A. C. M., Catania, K. C., Presgraves, D. C. and Gorbunova, V. (2007). Telomerase activity coevolves with body mass not lifespan. Aging Cell 6, 45-52. (Pubitemid 46140139)
60. Seluanov, A., Hine, C., Bozzella, M., Hall, A., Sasahara, T. H., Ribeiro, A. A., Catania, K. C., Presgraves, D. C. and Gorbunova, V. (2008). Distinct tumor suppressor mechanisms evolve in rodent species that differ in size and lifespan. Aging Cell 7, 813-823. (Pubitemid 352749436)
61. Seluanov, A., Hine, C., Azpurua, J., Feigenson, M., Bozzella, M., Mao, Z., Catania, K. C. and Gorbunova, V. (2009). Hypersensitivity to contact inhibition provides a clue to cancer resistance of naked mole-rat. Proc. Natl. Acad. Sci. USA 106, 19352-19357.
62. Shukla, G. S., Shukla, A., Potts, R. J., Osier, M., Hart, B. A. and Chiu, J. F. (2000). Cadmium-mediated oxidative stress in alveolar epithelial cells induces the expression of γ-glutamylcysteine synthetase catalytic subunit and glutathione Stransferase α and π isoforms: potential role of activator protein-1. Cell Biol. Toxicol. 16, 347-362. (Pubitemid 32185001)
63. Sibley, C. G. and Ahlquist, J. E. (1990). Phylogeny and Classification of Birds. New Haven, CT: Yale University Press.
64. Strecker, V., Mai, S., Muster, B., Beneke, S., Bürkle, A., Bereiter-Hahn, J. and Jendrach, M. (2010). Aging of different avian cultured cells: lack of ROS-induced damage and quality control mechanisms. Mech. Ageing Dev. 131, 48-59.
65. Sun, L. Y., Steinbaugh, M. J., Masternak, M. M., Bartke, A. and Miller, R. A. (2009). Fibroblasts from long-lived mutant mice show diminished ERK1/2 phosphorylation but exaggerated induction of immediate early genes. Free Radic. Biol. Med. 47, 1753-1761.
66. Wilhelm, D., Bender, K., Knebel, A. and Angel, P. (1997). The level of intracellular glutathione is a key regulator for the induction of stress-activated signal transduction pathways including Jun N-terminal protein kinases and p38 kinase by alkylating agents.?Mol.?Cell. Biol. 17, 4792-4800. (Pubitemid 27318154)
67. Williams, J. B., Miller, R. A., Harper, J. M. and Wiersma, P. (2010). Functional linkages for the pace of life, life-history, and environment in birds. Integr. Comp. Biol. 50, 855-868.
68. Yuri, T. and Mindell, D. P. (2002). Molecular phylogenetic analysis of Fringillidae. New World nine-primaried oscines (Aves: Passeriformes). Mol. Phylogenet. Evol. 23, 229-243. (Pubitemid 34703378)