Stress-induced responses of human skin fibroblasts in vitro reflect human longevity

Aging Cell

Volumn 8, Issue 5, 2009, Pages 595-603

  Dekker, Pim ^a   Maier, Andrea B ^a   van Heemst, Diana ^a   de Koning Treurniet, Corine ^a   Blom, Joke ^a   Dirks, Roeland W ^a   Tanke, Hans J ^a   Westendorp, Rudi G J ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Apoptosis; Longevity; SA galactosidase; Senescence; Skin fibroblasts; Stress

Indexed keywords

BETA GALACTOSIDASE; ROTENONE; LIPOCORTIN 5;

ADULT; AGE DISTRIBUTION; AGED; APOPTOSIS; ARTICLE; CELL CYCLE; CELL GROWTH; CELL STRESS; COLONY FORMING UNIT; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN CELL; HYPERGLYCEMIA; IN VITRO STUDY; LONGEVITY; MALE; PRIORITY JOURNAL; PROGENY; SENESCENCE; SKIN FIBROBLAST; AGING; CELL AGING; CUTANEOUS PARAMETERS; DRUG EFFECT; FIBROBLAST; FUNCTIONS OF THE SKIN AND ITS APPENDAGES; GENETICS; HEALTH STATUS; METABOLISM; OXIDATIVE STRESS; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SIBLING; SMOKING;

ADULT; AGED, 80 AND OVER; AGING; ANNEXIN A5; APOPTOSIS; BETA-GALACTOSIDASE; CELL AGING; FEMALE; FIBROBLASTS; HEALTH STATUS; HUMANS; LONGEVITY; MALE; OXIDATIVE STRESS; ROTENONE; SIBLINGS; SKIN AGING; SKIN PHYSIOLOGICAL PHENOMENA; SMOKING; STRESS, PHYSIOLOGICAL;

EID: 73949143673     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/j.1474-9726.2009.00506.x     Document Type: Article

References (43)

1. Ben Porath I, Weinberg RA (2004) When cells get stressed: an integrative view of cellular senescence. J. Clin. Invest. 113, 8-13.
2. Benanti JA, Galloway DA (2004) Normal human fibroblasts are resistant to RAS-induced senescence. Mol. Cell. Biol. 24, 2842-2852.
3. Blazer S, Khankin E, Segev Y, Ofir R, Yalon-Hacohen M, Kra-Oz Z, Gottfried Y, Larisch S, Skorecki KL (2002) High glucose-induced replicative senescence: point of no return and effect of telomerase. Biochem. Biophys. Res. Commun. 296, 93-101.
4. Bootsma-van der Wiel A, Gussekloo J, de Craen AJM, van Exel E, Bloem BR, Westendorp RGJ (2002) Common chronic diseases and general impairments as determinants of walking disability in the oldest-old population. J. Am. Geriatr. Soc. 50, 1405-1410.
5. Campisi J (2003) Cancer and ageing: rival demons? Nat. Rev. Cancer 3, 339-349.
6. Cerami A (1985) Hypothesis. Glucose as a mediator of aging. J. Am. Geriatr. Soc. 33, 626-634.
7. Chintapalli J, Yang S, Opawumi D, Goyal SR, Shamsuddin N, Malhotra A, Reiss K, Meggs LG (2007) Inhibition of wild-type p66ShcA in mesangial cells prevents glycooxidant-dependent FOXO3a regulation and promotes the survival phenotype. Am. J. Physiol. Renal Physiol. 292, F523-F530.
8. Coates SS, Lehnert BE, Sharma S, Kindell SM, Gary RK (2007) Beryllium induces premature senescence in human fibroblasts. J. Pharmacol. Exp. Ther. 322, 70-79.
9. Coppe JP, Patil CK, Rodier F, Sun Y, Munoz DP, Goldstein J, Nelson PS, Desprez PY, Campisi J (2008) Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol. 6, 2853-2868.
10. Dierick JF, Eliaers F, Remacle J, Raes M, Fey SJ, Larsen PM, Toussaint O (2002) Stress-induced premature senescence and replicative senescence are different phenotypes, proteomic evidence. Biochem. Pharmacol. 64, 1011-1017.
11. Dimri GP, Lee XH, Basile G, Acosta M, Scott C, Roskelley C, Medrano EE, Linskens M, Rubelj I, Pereirasmith O, Peacocke M, Campisi J (1995) A biomarker that identifies senescent human-cells in culture and in aging skin in-vivo. Proc. Natl Acad. Sci. USA. 92, 9363-9367.
12. Donehower LA (2005) p53: guardian AND suppressor of longevity? Exp. Gerontol. 40, 7-9.
13. Duan J, Zhang Z, Tong T (2001) Senescence delay of human diploid fibroblast induced by anti-sense p16INK4a expression. J. Biol. Chem. 276, 48325-48331.
14. Francis MK, Appel S, Meyer C, Balin SJ, Balin AK, Cristofalo VJ (2004) Loss of EPC-1/PEDF expression during skin aging in vivo. J. Invest. Dermatol. 122, 1096-1105.
15. Harman D (1956) Aging: a theory based on free radical and radiation chemistry. J. Gerontol. 11, 298-300.
16. Harper JM, Salmon AB, Leiser SF, Galecki AT, Miller RA (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.
17. van Heemst D, den Reijer PM, Westendorp RG (2007) Ageing or cancer: a review on the role of caretakers and gatekeepers. Eur. J. Cancer 43, 2144-2152.
18. Herbig U, Ferreira M, Condel L, Carey D, Sedivy JM (2006) Cellular senescence in aging primates. Science 311, 1257.
19. Itahana K, Zou Y, Itahana Y, Martinez JL, Beausejour C, Jacobs JJ, Van Lohuizen M, Band V, Campisi J, Dimri GP (2003) Control of the replicative life span of human fibroblasts by p16 and the polycomb protein Bmi-1. Mol. Cell. Biol. 23, 389-401.
20. Jeyapalan JC, Ferreira M, Sedivy JA, Herbig U (2007) Accumulation of senescent cells in mitotic tissue of aging primates. Mech. Ageing Dev. 128, 36-44.
21. Kapahi P, Boulton ME, Kirkwood TBL (1999) Positive correlation between mammalian life span and cellular resistance to stress. Free Radical Biol. Med. 26, 495-500.
22. Killilea DW, Ames BN (2008) Magnesium deficiency accelerates cellular senescence in cultured human fibroblasts. Proc. Natl. Acad. Sci. USA. 105, 5768-5773.
23. Kim HJ, Kim KS, Kim SH, Baek SH, Kim HY, Lee C, Kim JR (2009) Induction of cellular senescence by secretory phospholipase A2 in human dermal fibroblasts through an ROS-mediated p53 pathway. J. Gerontol. A Biol. Sci. Med. Sci. 64, 351-362.
24. Kurz DJ, Decary S, Hong Y, Erusalimsky JD (2000) Senescence-associated beta-galactosidase reflects an increase in lysosomal mass during replicative ageing of human endothelial cells. J. Cell Sci. 113, 3613-3622.
25. Li N, Ragheb K, Lawler G, Sturgis J, Rajwa B, Melendez JA, Robinson JP (2003) Mitochondrial complex I inhibitor rotenone induces apoptosis through enhancing mitochondrial reactive oxygen species production. J. Biol. Chem. 278, 8516-8525.
26. de Magalhaes JP, Chainiaux F, Remacle J, Toussaint O (2002) Stress-induced premature senescence in BJ and hTERT-BJ1 human foreskin fibroblasts. FEBS Lett. 523, 157-162.
27. Maier AB, Westendorp RGJ (2009) Relation between replicative senescence of human fibroblasts and life history characteristics. Ageing Res. Rev. 8, 237-243.
28. Maier AB, le Cessie S, Koning-Treurniet C, Blom J, Westendorp RG, van Heemst D (2007) Persistence of high-replicative capacity in cultured fibroblasts from nonagenarians. Aging Cell 6, 27-33.
29. Noppe G, Dekker P, Koning-Treurniet C, Blom J, van Heemst D, Dirks RJ, Tanke HJ, Westendorp RG, Maier AB (2009) Rapid flow cytometric method for measuring senescence associated â-galactosidase activity in human fibroblasts. Cytometry A (in press).
30. Nyunoya T, Monick MM, Klingelhutz A, Yarovinsky TO, Cagley JR, Hunninghake GW (2006) Cigarette smoke induces cellular senescence. Am. J. Respir. Cell Mol. Biol. 35, 681-688.
31. Phillips DI, Barker DJ, Fall CH, Seckl JR, Whorwood CB, Wood PJ, Walker BR (1998) Elevated plasma cortisol concentrations: a link between low birth weight and the insulin resistance syndrome? J. Clin. Endocrinol. Metab. 1998, 757-760.
32. Piper MD, Selman C, McElwee JJ, Partridge L (2008) Separating cause from effect: how does insulin/IGF signalling control lifespan in worms, flies and mice? J. Intern. Med. 263, 179-191.
33. Ressler S, Bartkova J, Niederegger H, Bartek J, Scharffetter-Kochanek K, Jansen-Durr P, Wlaschek M (2006) p16INK4A is a robust in vivo biomarker of cellular aging in human skin. Aging Cell 5, 379-389.
34. Roobrouck VD, Ulloa-Montoya F, Verfaillie CM (2008) Self-renewal and differentiation capacity of young and aged stem cells. Exp. Cell Res. 314, 1937-1944.
35. Rubin H (2002) The disparity between human cell senescence in vitro and lifelong replication in vivo. Nat. Biotechnol. 20, 675-681.
36. 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.
37. Schoenmaker M, de Craen AJ, de Meijer PH, Beekman M, Blauw GJ, Slagboom PE, Westendorp RG (2006) Evidence of genetic enrichment for exceptional survival using a family approach: the Leiden Longevity Study. Eur. J. Hum. Genet. 14, 79-84.
38. Stockl P, Zankl C, Hutter E, Unterluggauer H, Laun P, Heeren G, Bogengruber E, Herndler-Brandstetter D, Breitenbach M, Jansen-Durr P (2007) Partial uncoupling of oxidative phosphorylation induces premature senescence in human fibroblasts and yeast mother cells. Free Radical Biol. Med. 43, 947-958.
39. Vicencio JM, Galluzzi L, Tajeddine N, Ortiz C, Criollo A, Tasdemir E, Morselli E, Ben Younes A, Maiuri MC, Lavandero S, Kroemer G (2008) Senescence, apoptosis or autophagy? When a damaged cell must decide its path - a mini-review. Gerontology 54, 92-99.
40. Warner HR, Hodes RJ, Pocinki K (1997) What does cell death have to do with aging? J. Am. Geriatr. Soc. 45, 1140-1146.
41. Westendorp RG, van Heemst D, Rozing MP, Frolich M, Mooijaart SP, Blauw GJ, Beekman M, Heijmans BT, de Craen AJ, Slagboom PE (2009) Nonagenarian siblings and their offspring display lower risk of mortality and morbidity than sporadic nonagenarians: the Leiden Longevity Study. J. Am. Geriatr. Soc. (in press).
42. Xu D, Finkel T (2002) A role for mitochondria as potential regulators of cellular life span. Biochem. Biophys. Res. Commun. 294, 245-248.
43. Yoon SO, Yun CH, Chung AS (2002) Dose effect of oxidative stress on signal transduction in aging. Mech. Ageing Dev. 123, 1597-1604.