Absence of replicative senescence in cultured cells from the short-lived killifish Nothobranchius furzeri

Experimental Gerontology

Volumn 48, Issue 1, 2013, Pages 17-28

  Graf, Michael ^a,b   Hartmann, Nils ^a   Reichwald, Kathrin ^a   Englert, Christoph ^a  

^a FRITZ LIPMANN INSTITUTE   (Germany)

^b CARL ZEISS SMT AG   (Germany)

Author keywords

Ageing; Cellular senescence; Killifish; Nothobranchius furzeri; Primary cells

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1A; CYCLIN DEPENDENT KINASE INHIBITOR 2A; CYCLIN DEPENDENT KINASE INHIBITOR 2B; PROTEIN P53; TELOMERASE;

ANIMAL CELL; ARTICLE; CDKN1A GENE; CDKN2A GENE; CDKN2B GENE; CELL AGING; CELL CULTURE; CELL DIVISION; CELL PROLIFERATION; CONTROLLED STUDY; CYPRINODONTIFORMES; ENZYME ACTIVITY; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; LIFESPAN; NONHUMAN; NOTHOBRANCHIUS FURZERI; PRIORITY JOURNAL; REPLICATIVE SENESCENCE; SENESCENCE; STRAIN DIFFERENCE; TELOMERE; TP53 GENE;

AMINO ACID SEQUENCE; ANIMALS; CELL AGING; CELL CYCLE CHECKPOINTS; CELL CYCLE PROTEINS; CELL PROLIFERATION; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE INHIBITOR P15; CYCLIN-DEPENDENT KINASE INHIBITOR P16; CYCLIN-DEPENDENT KINASE INHIBITOR P21; GAMMA RAYS; GENE EXPRESSION REGULATION; HISTONES; KILLIFISHES; LONGEVITY; MOLECULAR SEQUENCE DATA; SEQUENCE ALIGNMENT; SKIN; SPECIES SPECIFICITY; TELOMERASE; TELOMERE HOMEOSTASIS;

CYPRINODONTOIDEI; NOTHOBRANCHIUS FURZERI; VERTEBRATA;

EID: 84872014500     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2012.02.012     Document Type: Article

References (67)

1. Baker D.J., Wijshake T., Tchkonia T., LeBrasseur N.K., Childs B.G., van de Sluis B., Kirkland J.L., van Deursen J.M. Clearance of p16Ink4a-positive senescent cells delays ageing-associated disorders. Nature 2011, 479:232-236.
2. Bodnar A.G., Ouellette M., Frolkis M., Holt S.E., Chiu C.-P., Morin G.B., Harley C.B., Shay J.W., Lichtsteiner S., Wright W.E. Extension of life-span by introduction of telomerase into normal human cells. Science 1998, 279:349-352.
3. Braig M., Lee S., Loddenkemper C., Rudolph C., Peters A.H., Schlegelberger B., Stein H., Dorken B., Jenuwein T., Schmitt C.A. Oncogene-induced senescence as an initial barrier in lymphoma development. Nature 2005, 436:660-665.
4. Campisi J. The biology of replicative senescence. Eur. J. Cancer 1997, 33:703-709.
5. Collado M., Blasco M.A., Serrano M. Cellular senescence in cancer and aging. Cell 2007, 130:223-233.
6. Counter C.M., Hahn W.C., Wei W., Caddle S.D., Beijersbergen R.L., Lansdorp P.M., Sedivy J.M., Weinberg R.A. Dissociation among in vitro telomerase activity, telomere maintenance, and cellular immortalization. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:14723-14728.
7. d'Adda di Fagagna F., Reaper P.M., Clay-Farrace L., Fiegler H., Carr P., Von Zglinicki T., Saretzki G., Carter N.P., Jackson S.P. A DNA damage checkpoint response in telomere-initiated senescence. Nature 2003, 426:194-198.
8. Deng Q., Liao R., Wu B.L., Sun P. High intensity ras signaling induces premature senescence by activating p38 pathway in primary human fibroblasts. J. Biol. Chem. 2004, 279:1050-1059.
9. Di Cicco E., Tozzini E.T., Rossi G., Cellerino A. The short-lived annual fish Nothobranchius furzeri shows a typical teleost aging process reinforced by high incidence of age-dependent neoplasias. Exp. Gerontol. 2011, 46:249-256.
10. Dierick J.-F., Eliaers F., Remacle J., Raes M., Fey S.J., Larsen P.M., Toussaint O. Stress-induced premature senescence and replicative senescence are different phenotypes, proteomic evidence. Biochem. Pharmacol. 2002, 64:1011-1017.
11. Dierick J.-F., Kalume D.E., Wenders F., Salmon M., Dieu M., Raes M., Roepstorff P., Toussaint O. Identification of 30 protein species involved in replicative senescence and stress-induced premature senescence. FEBS Lett. 2002, 531:499-504.
12. Dimri G.P., Lee X., Basile G., Acosta M., Scott G., Roskelley C., Medrano E.E., Linskens M., Rubelj I., Pereira-Smith O., et al. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:9363-9367.
13. Elmore L.W., Norris M.W., Sircar S., Bright A.T., McChesney P.A., Winn R.N., Holt S.E. Upregulation of telomerase function during tissue regeneration. Exp. Biol. Med. (Maywood) 2008, 233:958-967.
14. Fagagna F.d.A.d., Reaper P.M., Clay-Farrace L., Fiegler H., Carr P., von Zglinicki T., Saretzki G., Carter N.P., Jackson S.P. A DNA damage checkpoint response in telomere-initiated senescence. Nature 2003, 426:194-198.
15. Feldser D.M., Greider C.W. Short telomeres limit tumor progression in vivo by inducing senescence. Cancer Cell 2007, 11:461-469.
16. Fryer J.L., Lannan C.N. Three decades of fish cell culture: a current listing of cell lines derived from fishes. Methods Cell Sci. 1994, 16:87-94.
17. Genade T., Benedetti M., Terzibasi E., Roncaglia P., Valenzano D.R., Cattaneo A., Cellerino A. Annual fishes of the genus Nothobranchius as a model system for aging research. Aging Cell 2005, 4:223-233.
18. Gilley J., Fried M. One INK4 gene and no ARF at the Fugu equivalent of the human INK4A/ARF/INK4B tumor suppressor locus. Oncogene 2001, 20:7447-7452.
19. Gomes N.M., Shay J.W., Wright W.E. Telomere biology in Metazoa. FEBS Lett. 2010, 584:3741-3751.
20. Graf M., Cellerino A., Englert C. Gender separation increases somatic growth in females but does not affect lifespan in Nothobranchius furzeri. PLoS One 2010, 5:e11958.
21. Hammer Ø., Harper D.A.T., Ryan P.D. Past: paleontological statistics software package for education and data analysis. Palaeontol. Electron. 2001, 4(1):9.
22. Hara E., Smith R., Parry D., Tahara H., Stone S., Peters G. Regulation of p16CDKN2 expression and its implications for cell immortalization and senescence. Mol. Cell. Biol. 1996, 16:859-867.
23. Harley C.B., Futcher A.B., Greider C.W. Telomeres shorten during ageing of human fibroblasts. Nature 1990, 345:458-460.
24. Hartmann N., Reichwald K., Lechel A., Graf M., Kirschner J., Dorn A., Terzibasi E., Wellner J., Platzer M., Rudolph K.L., Cellerino A., Englert C. Telomeres shorten while Tert expression increases during aging of the short-lived fish Nothobranchius furzeri. Mech. Ageing Dev. 2009, 130:290-296.
25. Hayflick L., Moorhead P.S. The serial cultivation of human diploid cell strains. Exp. Cell Res. 1961, 25:585-621.
26. Hemann M.T., Strong M.A., Hao L.-Y., Greider C.W. The shortest telomere, not average telomere length, is critical for cell viability and chromosome stability. Cell 2001, 107:67-77.
27. Herbig U., Jobling W.A., Chen B.P.C., Chen D.J., Sedivy J.M. Telomere shortening triggers senescence of human cells through a pathway involving ATM, p53, and p21CIP1, but not p16INK4a. Mol. Cell 2004, 14:501-513.
28. Janzen V., Forkert R., Fleming H.E., Saito Y., Waring M.T., Dombkowski D.M., Cheng T., DePinho R.A., Sharpless N.E., Scadden D.T. Stem-cell aging modified by the cyclin-dependent kinase inhibitor p16INK4a. Nature 2006, 443:421-426.
29. Kazianis S., Khanolkar V.A., Nairn R.S., Rains J.D., Trono D., Garcia R., Williams E.L., Walter R.B. Structural organization, mapping, characterization and evolutionary relationships of CDKN2 gene family members in Xiphophorus fishes. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2004, 138:291-299.
30. Kirschner J., Weber D., Neuschl C., Franke A., Zielke L., Powalsky E., Menzel U., Groth M., Shagin D., Petzold A., Felder M., Hartmann N., Graf M., Englert C., Brockmann G.A., Platzer M., Cellerino A., Reichwald K. Mapping of quantitative trait loci affecting lifespan in the short-lived teleost fish Nothobranchius furzeri. Aging Cell 2012, 11:252-261.
31. Klapper W., Heidorn K., Kuhne K., Parwaresch R., Krupp G. Telomerase activity in 'immortal' fish. FEBS Lett. 1998, 434:409-412.
32. Komura J.-I., Mitani H., Shima A. Fish cell culture: establishment of two fibroblast-like cell lines (OL-17 and OL-32) from fins of the medaka, Oryzias latipes. In Vitro Cell. Dev. Biol. - Plant 1988, 24:294-298.
33. Krishnamurthy J., Torrice C., Ramsey M.R., Kovalev G.I., Al-Regaiey K., Su L., Sharpless N.E. Ink4a/Arf expression is a biomarker of aging. J. Clin. Invest. 2004, 114:1299-1307.
34. Lakra W.S., Swaminathan T.R., Joy K.P. Development, characterization, conservation and storage of fish cell lines: a review. Fish Physiol. Biochem. 2011, 37:1-20.
35. Lepilina, A., Coon, A.N., Kikuchi, K., Holdway, J.E., Roberts, R.W., Burns, C.G., Poss, K.D., 2006. A Dynamic Epicardial Injury Response Supports Progenitor Cell Activity during Zebrafish Heart Regeneration. Cell 127, 607-619.
36. Liu Y., Sanoff H.K., Cho H., Burd C.E., Torrice C., Ibrahim J.G., Thomas N.E., Sharpless N.E. Expression of p16(INK4a) in peripheral blood T-cells is a biomarker of human aging. Aging Cell 2009, 8:439-448.
37. Lloyd A.C. Limits to lifespan. Nat. Cell Biol. 2002, 4:E25-E27.
38. Michaloglou C., Vredeveld L.C., Soengas M.S., Denoyelle C., Kuilman T., van der Horst C.M., Majoor D.M., Shay J.W., Mooi W.J., Peeper D.S. BRAFE600-associated senescence-like cell cycle arrest of human naevi. Nature 2005, 436:720-724.
39. Nakayama J., Tahara H., Tahara E., Saito M., Ito K., Nakamura H., Nakanishi T., Ide T., Ishikawa F. Telomerase activation by hTRT in human normal fibroblasts and hepatocellular carcinomas. Nat. Genet. 1998, 18:65-68.
40. Narita M., Nuñez S., Heard E., Narita M., Lin A.W., Hearn S.A., Spector D.L., Hannon G.J., Lowe S.W. Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell 2003, 113:703-716.
41. Noda A., Ning Y., Venable S.F., Pereira-Smith O.M., Smith J.R. Cloning of senescent cell-derived inhibitors of DNA synthesis using an expression screen. Exp. Cell Res. 1994, 211:90-98.
42. Parrinello S., Samper E., Krtolica A., Goldstein J., Melov S., Campisi J. Oxygen sensitivity severely limits the replicative lifespan of murine fibroblasts. Nat. Cell Biol. 2003, 5:741-747.
43. Pascal T., Debacq-Chainiaux F., Chrétien A., Bastin C., Dabée A.-F., Bertholet V., Remacle J., Toussaint O. Comparison of replicative senescence and stress-induced premature senescence combining differential display and low-density DNA arrays. FEBS Lett. 2005, 579:3651-3659.
44. Pfaffl M.W., Horgan G.W., Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 2002, 30:e36.
45. Poss K.D., Keating M.T., Nechiporuk A. Tales of regeneration in zebrafish. Dev. Dyn. 2003, 226:202-210.
46. Reichwald K., Lauber C., Nanda I., Kirschner J., Hartmann N., Schories S., Gausmann U., Taudien S., Schilhabel M.B., Szafranski K., Glockner G., Schmid M., Cellerino A., Schartl M., Englert C., Platzer M. High tandem repeat content in the genome of the short-lived annual fish Nothobranchius furzeri: a new vertebrate model for aging research. Genome Biol. 2009, 10:R16.
47. Reimschuessel R. A fish model of renal regeneration and development. ILAR J. 2001, 42:285-291.
48. Ressler S., Bartkova J., Niederegger H., Bartek J., Scharffetter-Kochanek K., Jansen-Durr P., Wlaschek M. p16INK4A is a robust in vivo biomarker of cellular aging in human skin. Aging Cell 2006, 5:379-389.
49. Rodier F., Campisi J. Four faces of cellular senescence. J. Cell Biol. 2011, 192:547-556.
50. Rogakou E.P., Pilch D.R., Orr A.H., Ivanova V.S., Bonner W.M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 1998, 273:5858-5868.
51. Seluanov A., Chen Z., Hine C., Sasahara T.H., Ribeiro A.A., Catania K.C., Presgraves D.C., Gorbunova V. Telomerase activity coevolves with body mass not lifespan. Aging Cell 2007, 6:45-52.
52. Seluanov A., Hine C., Bozzella M., Hall A., Sasahara T.H., Ribeiro A.A., Catania K.C., Presgraves D.C., Gorbunova V. Distinct tumor suppressor mechanisms evolve in rodent species that differ in size and lifespan. Aging Cell 2008, 7:813-823.
53. Severino J., Allen R.G., Balin S., Balin A., Cristofalo V.J. Is beta-galactosidase staining a marker of senescence in vitro and in vivo?. Exp. Cell Res. 2000, 257:162-171.
54. Shima A., Nikaido O., Shinohara S., Egami N. Continued in vitro growth of fibroblast-like cells (RBCF-1) derived from the caudal fin of the fish, Carassius auratus. Exp. Gerontol. 1980, 15:305-314.
55. Stein G., Beeson M., Gordon L. Failure to phosphorylate the retinoblastoma gene product in senescent human fibroblasts. Science 1990, 249:666-669.
56. Takahashi A., Ohtani N., Yamakoshi K., Iida S., Tahara H., Nakayama K., Nakayama K.I., Ide T., Saya H., Hara E. Mitogenic signalling and the p16INK4a-Rb pathway cooperate to enforce irreversible cellular senescence. Nat. Cell Biol. 2006, 8:1291-1297.
57. Terzibasi E., Valenzano D.R., Cellerino A. The short-lived fish Nothobranchius furzeri as a new model system for aging studies. Exp. Gerontol. 2007, 42:81-89.
58. Terzibasi E., Valenzano D.R., Benedetti M., Roncaglia P., Cattaneo A., Domenici L., Cellerino A. Large differences in aging phenotype between strains of the short-lived annual fish Nothobranchius furzeri. PLoS One 2008, 3:e3866.
59. Terzibasi E., Lefrancois C., Domenici P., Hartmann N., Graf M., Cellerino A. Effects of dietary restriction on mortality and age-related phenotypes in the short-lived fish Nothobranchius furzeri. Aging Cell 2009, 8:88-99.
60. Valdesalici S., Cellerino A. Extremely short lifespan in the annual fish Nothobranchius furzeri. Proc. Biol. Sci. 2003, 270(Suppl. 2):S189-S191.
61. Valenzano D.R., Terzibasi E., Cattaneo A., Domenici L., Cellerino A. Temperature affects longevity and age-related locomotor and cognitive decay in the short-lived fish Nothobranchius furzeri. Aging Cell 2006, 5:275-278.
62. Valenzano D.R., Terzibasi E., Genade T., Cattaneo A., Domenici L., Cellerino A. Resveratrol prolongs lifespan and retards the onset of age-related markers in a short-lived vertebrate. Curr. Biol. 2006, 16:296-300.
63. Vaziri H., Benchimol S. Reconstitution of telomerase activity in normal human cells leads to elongation of telomeres and extended replicative life span. Curr. Biol. 1998, 8:279-282.
64. Ventura A., Kirsch D.G., McLaughlin M.E., Tuveson D.A., Grimm J., Lintault L., Newman J., Reczek E.E., Weissleder R., Jacks T. Restoration of p53 function leads to tumor regression in vivo. Nature 2007, 445:661-665.
65. Weinrich S.L., Pruzan R., Ma L., Ouellette M., Tesmer V.M., Holt S.E., Bodnar A.G., Lichtsteiner S., Kim N.W., Trager J.B., Taylor R.D., Carlos R., Andrews W.H., Wright W.E., Shay J.W., Harley C.B., Morin G.B. Reconstitution of human telomerase with the template RNA component hTR and the catalytic protein subunit hTRT. Nat. Genet. 1997, 17:498-502.
66. Woodhead A.D., Setlow R.B., Grist E. DNA repair and longevity in three species of cold-blooded vertebrates. Exp. Gerontol. 1980, 15:301-304.
67. Zglinicki T.v., Saretzki G., Ladhoff J., Fagagna F.d.A.d., Jackson S.P. Human cell senescence as a DNA damage response. Mech. Ageing Dev. 2005, 126:111-117.