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Fish Physiology and Biochemistry

, Volume 43, Issue 2, pp 309–319 | Cite as

Aging asymmetry: systematic survey of changes in age-related biomarkers in the annual fish Nothobranchius guentheri

  • Yuan Dong
  • Pengfei Cui
  • Zhijian Li
  • Shicui Zhang
Article

Abstract

Aging asymmetry is the observation that different tissues age in different ways and at different rates. This has not been assessed in a single organism using multiple biomarkers of aging. Here we clearly demonstrated that the levels of protein oxidation and lipid peroxidation as well as CAT, SOD and GPX activities all showed a tissue-dependent change with advancing age; and DNA repair ability, as revealed by the expression of ercc1 and its protein levels, also exhibited a tissue-specific variation with age. We also found that protein oxidation and lipid peroxidation levels remained relatively stable in the liver, intestine, skin and testis as well as in the brain, eye and heart of young, adult and aged fishes; SOD and GPX activities displayed little variation in the intestine, eye and skin as well as in the brain and skin of young, adult and aged fishes; and low and stable expression of ercc1 was observed in the spleen, eye and heart of young, adult and aged fishes. Collectively, these results indicate that aging is tissue specific and asymmetric in N. guentheri. The observation of aging asymmetry may have practical implications for the application of non-intrusion intervention approaches to prolong lifespan.

Keywords

Aging asymmetry Age-related markers Annual fish Nothobranchius Reactive oxygen species ercc1 

Notes

Acknowledgments

This work was supported by the grants of Natural Science Foundation of China (31372505; U1401211). No competing financial interests exist. S.C. Zhang designed the research and wrote the manuscript; Y. Dong performed the research, analyzed the data and wrote the manuscript; P.F. Cui and Z.J. Li participated in the research.

Supplementary material

10695_2016_288_MOESM1_ESM.doc (1.2 mb)
Supplementary material 1 (DOC 1243 kb)

References

  1. Akintola AD, Crislip ZL, Catania JM, Chen G, Zimmer WE, Burghardt RC, Parrish AR (2008) Promoter methylation is associated with the age-dependent loss of N-cadherin in the rat kidney. Am J Physiol Renal Physiol 294:F170–F176. doi: 10.1152/ajprenal.00285.2007 CrossRefPubMedGoogle Scholar
  2. Almeida M (2012) Aging mechanisms in bone. Bonekey Rep 1:102. doi: 10.1038/bonekey.2012.102 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Anson RM, Bohr VA (2000) Mitochondria, oxidative DNA damage, and aging. J Am Aging Assoc 23:199–218. doi: 10.1007/s11357-000-0020-y PubMedPubMedCentralGoogle Scholar
  4. Berlett BS, Stadtman ER (1997) Protein oxidation in aging, disease, and oxidative stress. J Biol Chem 272:20313–20316. doi: 10.1074/jbc.272.33.20313 CrossRefPubMedGoogle Scholar
  5. Cakatay U, Telci A, Kayali R, Tekeli F, Akçay T, Sivas A (2003) Relation of aging with oxidative protein damage parameters in the rat skeletal muscle. Clin Biochem 36:51–55. doi: 10.1016/S0009-9120(02)00407-1 CrossRefPubMedGoogle Scholar
  6. Cellerino A, Valenzano DR, Reichard M (2016) From the bush to the bench: the annual Nothobranchius fishes as a new model system in biology. Biol Rev Camb Philos Soc 91:511–533. doi: 10.1111/brv.12183 CrossRefPubMedGoogle Scholar
  7. Di Cicco E, Tozzini ET, Rossi G, Cellerino A (2011) The short-lived annual fish Nothobranchius furzeri shows a typical teleost aging process reinforced by high incidence of age-dependent neoplasias. Exp Gerontol 46:249–256. doi: 10.1016/j.exger.2010.10.011 CrossRefPubMedGoogle Scholar
  8. Facista A, Nguyen H, Lewis C, Prasad AR, Ramsey L, Zaitlin B, Nfonsam V, Krouse RS, Bernstein H, Payne CM, Stern S, Oatman N, Banerjee B, Bernstein C (2012) Deficient expression of DNA repair enzymes in early progression to sporadic colon cancer. Genome Integr 3:3. doi: 10.1186/2041-9414-3-3 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Genade T, Benedetti M, Terzibasi E, Roncaglia P, Valenzano DR, Cattaneo A, Cellerino A (2005) Annual fishes of the genus Nothobranchius as a model system for aging research. Aging Cell 4:223–233CrossRefPubMedGoogle Scholar
  10. Gensler HL, Bernstein H (1981) DNA damage as the primary cause of aging. Q Rev Biol 56:279–303CrossRefPubMedGoogle Scholar
  11. Gregg SQ, Robinson AR, Niedernhofer LJ (2011) Physiological consequences of defects in ERCC1-XPF DNA repair endonuclease. DNA Repair (Amst). 10:781–791. doi: 10.1016/j.dnarep.2011.04.026 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Harman D (1965) The free radical theory of aging: effect of age on serum copper levels. J Gerontol 20:151–153. doi: 10.1016/0921-8734(92)90030-S CrossRefPubMedGoogle Scholar
  13. Harman D (1981) The aging process. Proc Natl Acad Sci USA 78:7124–7128CrossRefPubMedPubMedCentralGoogle Scholar
  14. Hayflick L, Moorhead PS (1961) The serial cultivation of human diploid cell strains. Exp Cell Res 25:585–621CrossRefPubMedGoogle Scholar
  15. Helen O, Norman S (2003) Cardiovascular aging and heart failure. Eur J Heart Fail 5:427–434. doi: 10.1016/S1388-9842(03)00011-4 CrossRefGoogle Scholar
  16. Hsu CY, Chiu YC, Hsu WL, Chan YP (2008) Age-related markers assayed at different developmental stages of the annual fish Nothobranchius rachovii. J Gerontol A Biol Sci Med Sci 63:1267–1276CrossRefPubMedGoogle Scholar
  17. Jin J, Wang GL, Timchenko L, Timchenko NA (2009) GSK3beta and aging liver. Aging 1:582–585CrossRefPubMedPubMedCentralGoogle Scholar
  18. Kazachkova N, Ramos A, Santos C, Lima M (2013) Mitochondrial DNA damage patterns and aging: revising the evidences for humans and mice. Aging Dis 4:337–350. doi: 10.14336/AD.2013.0400337 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Klass MR (1983) A method for the isolation of longevity mutants in the nematode Caenorhabditis elegans and initial results. Mech Ageing Dev 22:279–286. doi: 10.1016/0047-6374(83)90082-9 CrossRefPubMedGoogle Scholar
  20. Koutsouleris N, Davatzikos C, Borgwardt S, Gaser C, Bottlender R, Frodl T, Falkai P, Riecher-Rössler A, Möller HJ, Reiser M, Pantelis C, Meisenzahl E (2014) Accelerated brain aging in schizophrenia and beyond: a neuroanatomical marker of psychiatric disorders. Schizophr Bull 40:1140–1153. doi: 10.1093/schbul/sbt142 CrossRefPubMedGoogle Scholar
  21. Latimer CS, Searcy JL, Bridges MT, Brewer LD, Popović J, Blalock EM, Landfield PW, Thibault O, Porter NM (2011) Reversal of glial and neurovascular markers of unhealthy brain aging by exercise in middle-aged female mice. PLoS One 6:e26812. doi: 10.1371/journal.pone.0026812 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Li XL, Khanna A, Li N, Wang E (2011) Circulatory miR-34a as an RNA-based, noninvasive biomarker for brain aging. Aging 3:985–1002CrossRefPubMedPubMedCentralGoogle Scholar
  23. Liu CS, Wang X, Feng WR, Li GR, Su F, Zhang SC (2012) Differential expression of aging biomarkers at different life stages of the annual fish Nothobranchius guentheri. Biogerontology 13:501–510. doi: 10.1007/s10522-012-9395-2 CrossRefPubMedGoogle Scholar
  24. López-Otín C, Blasco MA, Partridge L, Serrano M, Kroemer G (2013) The hallmarks of aging. Cell 153:1194–1217. doi: 10.1016/j.cell.2013.05.039 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Lucas-Sánchez A, Almaida-Pagan PF, Mendiola P, de Costa J (2014) Nothobranchius as a model for aging studies. A review. Aging Dis 5:281–291. doi: 10.14336/AD.2014.0500281 PubMedGoogle Scholar
  26. Markofsky J, Perlmutter A (1972) Age at sexual maturity and its relationship to longevity in the male annual cyprinodont fish, Nothobranchius guentheri. Exp Gerontol 7:131–135. doi: 10.1016/0531-5565(72)90007-1 CrossRefPubMedGoogle Scholar
  27. Masuyama M, Iida R, Takatsuka H, Yasuda T, Matsuk IT (2005) Quantitative change in mitochondrial DNA content in various mouse tissues during aging. Biochim Biophys Acta 1723:302–308. doi: 10.1016/j.bbagen.2005.03.001 CrossRefPubMedGoogle Scholar
  28. Montine TJ, Neely MD, Quinn JF, Beal MF, Markesbery WR, Roberts LJ, Morrow JD (2002) Lipid peroxidation in aging brain and Alzheimer’s disease. Free Radic Biol Med 33:620–626. doi: 10.1016/S0891-5849(02)00807-9 CrossRefPubMedGoogle Scholar
  29. Ng’oma E, Reichwald K, Dorn A, Wittig M, Balschun T, Franke A, Platzer M, Cellerino A (2014) The age related markers lipofuscin and apoptosis show different genetic architecture by QTL mapping in short-lived Nothobranchius fish. Aging (Albany NY) 6:468–480CrossRefGoogle Scholar
  30. Olovnikow AM (1996) Telomeres, telomerase, and aging: origin of the theory. Exp Gerontol 31:443–448. doi: 10.1016/0531-5565(96)00005-8 CrossRefGoogle Scholar
  31. Schisler NJ, Singh SM (1987) Inheritance and expression of tissue-specific catalase activity during development and aging in mice. Genome 29:748–760CrossRefPubMedGoogle Scholar
  32. Sohal RS (2002) Role of oxidative stress and protein oxidation in the aging process. Free Radic Biol Med 33:37–44. doi: 10.1016/S0891-5849(02)00856-0 CrossRefPubMedGoogle Scholar
  33. Sohal RS, Agarwal S, Dubey A, William CO (1993) Protein oxidative damage is associated with life expectancy of houseflies. Proc Natl Acad Sci USA 90:7255–7259CrossRefPubMedPubMedCentralGoogle Scholar
  34. Spitz DR, Oberley LW (1989) An assay for superoxide dismutase activity in mammalian tissue homogenates. Anal Biochem 179:8–18. doi: 10.1016/0003-2697(89)90192-9 CrossRefPubMedGoogle Scholar
  35. Ursini F, Maiorino M, Gregolin C (1985) The selenoenzyme phospholipid hydroperoxide glutathione peroxidase. Biochim Biophys Acta 839:62–70. doi: 10.1016/0304-4165(85)90182-5 CrossRefPubMedGoogle Scholar
  36. Valenzano DR, Terzibasi E, Cattaneo A, Domenici L, Cellerino A (2006) Temperature affects longevity and age-related locomotor and cognitive decay in the short-lived fish Nothobranchius furzeri. Aging Cell 5:275–278CrossRefPubMedGoogle Scholar
  37. Van Manen R, de Priester W, Knook DL (1983) Lysosomal activity in aging rat liver: I. Variation in enzyme activity within the liver lobule. Mech Ageing Dev 22:159–165. doi: 10.1016/0047-6374(83)90109-4 CrossRefPubMedGoogle Scholar
  38. Van Voorhies WA (2002) The influence of metabolic rate on longevity in the nematode Caenorhabditis elegans. Aging Cell 1:91–101. doi: 10.1046/j.1474-9728.2002.00022.x CrossRefPubMedGoogle Scholar
  39. Wang G, Zhang S, Wang Z (2009) Responses of alternative complement expression to challenge with different combinations of Vibrio anguillarum, Escherichia coli and Staphylococcus aureus: evidence for specific immune priming in amphioxus Branchiostoma belcheri. Fish Shellfish Immunol 26:33–39. doi: 10.1016/j.fsi.2008.09.018 CrossRefPubMedGoogle Scholar
  40. Weglicki WB, Luna Z, Nair PP (1969) Sex and tissue specific differences in concentrations of alpha-tocopherol in mature and senescent rats. Nature 221:185–186CrossRefPubMedGoogle Scholar
  41. Weisleder N, Ma JJ (2008) Altered Ca2+ sparks in aging skeletal and cardiac muscle. Ageing Res Rev 7:177–188. doi: 10.1016/j.arr.2007.12.003 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Wilkinson JE, Burmeister L, Brooks SV, Chan CC, Friedline S, Harrison DE, Hejtmancik JF, Nadon N, Strong R, Wood LK, Woodward MA, Miller RA (2012) Rapamycin slows aging in mice. Aging Cell 11:675–682. doi: 10.1111/j.1474-9726.2012.00832.x CrossRefPubMedPubMedCentralGoogle Scholar
  43. Wu JJ, Liu J, Chen EB, Wang JJ, Cao L, Narayan N, Fergusson MM, Rovira II, Allen M, Springer DA, Lago CU, Zhang S, DuBois W, Ward T, deCabo R, Gavrilova O, Mock B, Finkel T (2013) Increased mammalian lifespan and a segmental and tissue-specific slowing of aging after genetic reduction of mTOR expression. Cell Rep 4:913–920. doi: 10.1016/j.celrep.2013.07.030 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Zhu Y, Carvey PM, Ling Z (2006) Age-related changes in glutathione and glutathione-related enzymes in rat brain. Brain Res 1090:35–44. doi: 10.1016/j.brainres.2006.03.063 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Yuan Dong
    • 1
  • Pengfei Cui
    • 1
  • Zhijian Li
    • 1
  • Shicui Zhang
    • 1
  1. 1.Laboratory for Evolution and Development, Department of Marine Biology, Institute of Evolution and Marine BiodiversityOcean University of ChinaQingdaoChina

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