Quantitative model of cell cycle arrest and cellular senescence in primary human fibroblasts

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Schäuble, Sascha ^a   Klement, Karolin ^b,c   Marthandan, Shiva ^b   Münch, Sandra ^b,d   Heiland, Ines ^a   Schuster, Stefan ^a   Hemmerich, Peter ^b   Diekmann, Stephan ^b  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^b FLI   (Germany)

^c UNIVERSITY OF CALGARY   (Canada)

^d UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANALYTIC METHOD; ANIMAL CELL; APOPTOSIS; ARTICLE; CALCULATION; CELL AGING; CELL CYCLE ARREST; CELL DIFFERENTIATION; CELL GROWTH; CELL PROLIFERATION; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; DNA DAMAGE; FEMALE; FIBROBLAST; GROWTH RATE; HUMAN; HUMAN CELL; MALE; NONHUMAN; RAT;

ANIMALS; BIOLOGICAL MARKERS; CELL AGING; CELL CYCLE CHECKPOINTS; CELL PROLIFERATION; CELLS, CULTURED; COMPUTER SIMULATION; FEMALE; FIBROBLASTS; GAMMA RAYS; HUMANS; MALE; MODELS, BIOLOGICAL; RATS; STRESS, PHYSIOLOGICAL;

EID: 84864654179     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042150     Document Type: Article

References (78)

1. Campisi J, Sedivy J, (2009) How does proliferative homeostasis change with age? What causes it and how does it contribute to aging? J Gerontol A Biol Sci Med Sci 64: 164-166.
2. Baker DJ, Wijshake T, Tchkonia T, LeBrasseur NK, Childs BG, et al. (2011) Clearance of p16Ink4a-positive senescent cells delays ageing-associated disorders. Nature 479: 232-236.
3. Hayflick L, Moorhead PS, (1961) The serial cultivation of human diploid cell strains. Exp Cell Res 25: 585-621.
4. Krizhanovsky V, Xue W, Zender L, Yon M, Hernando E, et al. (2008) Implications of cellular senescence in tissue damage response, tumor suppression, and stem cell biology. Cold Spring Harb Symp Quant Biol 73: 513-522.
5. Chaturvedi V, Qin JZ, Denning MF, Choubey D, Diaz MO, et al. (1999) Apoptosis in proliferating, senescent, and immortalized keratinocytes. J Biol Chem 274: 23358-23367.
6. Marcotte R, Lacelle C, Wang E, (2004) Senescent fibroblasts resist apoptosis by downregulating caspase-3. Mech Ageing Dev 125: 777-783.
7. Narita M, Nũnez S, Heard E, Narita M, Lin AW, et al. (2003) Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell 113: 703-716.
8. Dimri GP, Lee X, Basile G, Acosta M, Scott G, et al. (1995) A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci U S A 92: 9363-9367.
9. Kuilman T, Michaloglou C, Mooi WJ, Peeper DS, (2010) The essence of senescence. Genes Dev 24: 2463-2479.
10. Sikora E, Arendt T, Bennett M, Narita M, (2011) Impact of cellular senescence signature on ageing research. Ageing Res Rev 10: 146-152.
11. Cristofalo VJ, Lorenzini A, Allen RG, Torres C, Tresini M, (2004) Replicative senescence: a critical review. Mech Ageing Dev 125: 827-848.
12. Herbig U, Jobling WA, Chen BPC, Chen DJ, Sedivy JM, (2004) Telomere shortening triggers senescence of human cells through a pathway involving ATM, p53, and p21(CIP1), but not p16(INK4a). Mol Cell 14: 501-513.
13. Jeyapalan JC, Ferreira M, Sedivy JM, Herbig U, (2007) Accumulation of senescent cells in mitotic tissue of aging primates. Mech Ageing Dev 128: 36-44.
14. Ressler S, Bartkova J, Niederegger H, Bartek J, Scharffetter-Kochanek K, et al. (2006) p16INK4A is a robust in vivo biomarker of cellular aging in human skin. Aging Cell 5: 379-389.
15. Robles SJ, Adami GR, (1998) Agents that cause DNA double strand breaks lead to p16INK4a enrichment and the premature senescence of normal fibroblasts. Oncogene 16: 1113-1123.
16. Kosar M, Bartkova J, Hubackova S, Hodny Z, Lukas J, et al. (2011) Senescence-associated heterochromatin foci are dispensable for cellular senescence, occur in a cell type- and insult-dependent manner and follow expression of p16(ink4a). Cell Cycle 10: 457-468.
17. Coppé J-P, Desprez P-Y, Krtolica A, Campisi J, (2010) The senescence-associated secretory phenotype: the dark side of tumor suppression. Annu Rev Pathol 5: 99-118.
18. Kuilman T, Peeper DS, (2009) Senescence-messaging secretome: SMS-ing cellular stress. Nat Rev Cancer 9: 81-94.
19. Shelton DN, Chang E, Whittier PS, Choi D, Funk WD, (1999) Microarray analysis of replicative senescence. Curr Biol 9: 939-945.
20. Acosta JC, O'Loghlen A, Banito A, Guijarro MV, Augert A, et al. (2008) Chemokine signaling via the CXCR2 receptor reinforces senescence. Cell 133: 1006-1018.
21. Wajapeyee N, Serra RW, Zhu X, Mahalingam M, Green MR, (2008) Oncogenic BRAF induces senescence and apoptosis through pathways mediated by the secreted protein IGFBP7. Cell 132: 363-374.
22. d'Adda di Fagagna F, Reaper PM, Clay-Farrace L, Fiegler H, Carr P, et al. (2003) A DNA damage checkpoint response in telomere-initiated senescence. Nature 426: 194-198.
23. Takai H, Smogorzewska A, de Lange T, (2003) DNA damage foci at dysfunctional telomeres. Curr Biol 13: 1549-1556.
24. Nakamura AJ, Redon CE, Bonner WM, Sedelnikova OA, (2009) Telomere-dependent and telomere-independent origins of endogenous DNA damage in tumor cells. Aging (Albany NY) 1: 212-218.
25. Gire V, Roux P, Wynford-Thomas D, Brondello J-M, Dulic V, (2004) DNA damage checkpoint kinase Chk2 triggers replicative senescence. EMBO J 23: 2554-2563.
26. Goodarzi AA, Noon AT, Deckbar D, Ziv Y, Shiloh Y, et al. (2008) ATM signaling facilitates repair of DNA double-strand breaks associated with heterochromatin. Mol Cell 31: 167-177.
27. Ben-Porath I, Weinberg RA, (2004) When cells get stressed: an integrative view of cellular senescence. J Clin Invest 113: 8-13.
28. Ben-Porath I, Weinberg RA, (2005) The signals and pathways activating cellular senescence. Int J Biochem Cell Biol 37: 961-976.
29. Shay JW, Wright WE, (2005) Senescence and immortalization: role of telomeres and telomerase. Carcinogenesis 26: 867-874.
30. Cosme-Blanco W, Chang S, (2008) Dual roles of telomere dysfunction in initiation and suppression of tumorigenesis. Exp Cell Res 314: 1973-1979.
31. Hwang ES, (2002) Replicative senescence and senescence-like state induced in cancer-derived cells. Mech Ageing Dev 123: 1681-1694.
32. Zhao W, Lin ZX, Zhang ZQ, (2004) Cisplatin-induced premature senescence with concomitant reduction of gap junctions in human fibroblasts. Cell Res 14: 60-66.
33. Havelka AM, Berndtsson M, Olofsson MH, Shoshan MC, Linder S, (2007) Mechanisms of action of DNA-damaging anticancer drugs in treatment of carcinomas: is acute apoptosis an "off-target" effect? Mini Rev Med Chem 7: 1035-1039.
34. Di Leonardo A, Linke SP, Clarkin K, Wahl GM, (1994) DNA damage triggers a prolonged p53-dependent G1 arrest and long-term induction of Cip1 in normal human fibroblasts. Genes Dev 8: 2540-2551.
35. Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW, (1997) Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88: 593-602.
36. Toussaint O, Medrano EE, von Zglinicki T, (2000) Cellular and molecular mechanisms of stress-induced premature senescence (SIPS) of human diploid fibroblasts and melanocytes. Exp Gerontol 35: 927-945.
37. Debacq-Chainiaux F, Borlon C, Pascal T, Royer V, Eliaers F, et al. (2005) Repeated exposure of human skin fibroblasts to UVB at subcytotoxic level triggers premature senescence through the TGF-beta1 signaling pathway. J Cell Sci 118: 743-758.
38. Mallette FA, Gaumont-Leclerc M-F, Ferbeyre G, (2007) The DNA damage signaling pathway is a critical mediator of oncogene-induced senescence. Genes Dev 21: 43-48.
39. Maslov AY, Vijg J, (2009) Genome instability, cancer and aging. Biochim Biophys Acta 1790: 963-969.
40. Dimri GP, Itahana K, Acosta M, Campisi J, (2000) Regulation of a senescence checkpoint response by the E2F1 transcription factor and p14(ARF) tumor suppressor. Mol Cell Biol 20: 273-285.
41. Pearson M, Carbone R, Sebastiani C, Cioce M, Fagioli M, et al. (2000) PML regulates p53 acetylation and premature senescence induced by oncogenic Ras. Nature 406: 207-210.
42. Bartkova J, Rezaei N, Liontos M, Karakaidos P, Kletsas D, et al. (2006) Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 444: 633-637.
43. Lee AC, Fenster BE, Ito H, Takeda K, Bae NS, et al. (1999) Ras proteins induce senescence by altering the intracellular levels of reactive oxygen species. J Biol Chem 274: 7936-7940.
44. Di Micco R, Fumagalli M, Cicalese A, Piccinin S, Gasparini P, et al. (2006) Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 444: 638-642.
45. Pantoja C, Serrano M, (1999) Murine fibroblasts lacking p21 undergo senescence and are resistant to transformation by oncogenic Ras. Oncogene 18: 4974-4982.
46. Benanti JA, Galloway DA, (2004) Normal human fibroblasts are resistant to RAS-induced senescence. Mol Cell Biol 24: 2842-2852.
47. Rodier F, Campisi J, (2011) Four faces of cellular senescence. J Cell Biol 192: 547-556.
48. Lawless C, Wang C, Jurk D, Merz A, von Zglinicki T, et al. (2010) Quantitative assessment of markers for cell senescence. Exp Gerontol 45: 772-778.
49. Klement K, Melle C, Murzik U, Diekmann S, Norgauer J, et al. (2012) Accumulation of annexin A5 at the nuclear envelope is a biomarker of cellular aging. Mech Ageing Dev: in press.
50. Kill IR, Faragher RG, Lawrence K, Shall S, (1994) The expression of proliferation-dependent antigens during the lifespan of normal and progeroid human fibroblasts in culture. J Cell Sci 107 (Pt 2): 571-579.
51. Faragher RG, Kill IR, Hunter JA, Pope FM, Tannock C, et al. (1993) The gene responsible for Werner syndrome may be a cell division "counting" gene. Proc Natl Acad Sci U S A 90: 12030-12034.
52. Kronschnabl M, Stamminger T, (2003) Synergistic induction of intercellular adhesion molecule-1 by the human cytomegalovirus transactivators IE2p86 and pp71 is mediated via an Sp1-binding site. J Gen Virol 84: 61-73.
53. Seluanov A, Hine C, Bozzella M, Hall A, Sasahara THC, et al. (2008) Distinct tumor suppressor mechanisms evolve in rodent species that differ in size and lifespan. Aging Cell 7: 813-823.
54. Thornley JH, (1970) Respiration, growth and maintenance in plants. Nature 227: 304-305.
55. Penning de Vries FWT, (1975) The Cost of Maintenance Processes in Plant Cells. Annals of Botany 39: 77-92.
56. Pirt SJ, (1965) The maintenance energy of bacteria in growing cultures. Proc R Soc Lond B Biol Sci 163: 224-231.
57. Kim CS, Kim JK, Nam SY, Yang KH, Jeong M, et al. (2007) Low-dose radiation stimulates the proliferation of normal human lung fibroblasts via a transient activation of Raf and Akt. Mol Cells 24: 424-430.
58. Fumagalli M, Rossiello F, Clerici M, Barozzi S, Cittaro D, et al. (2012) Telomeric DNA damage is irreparable and causes persistent DNA-damage-response activation. Nat Cell Biol 14: 355-365.
59. Ludwig D, Jones DD, Holling CS, (1978) Qualitative analysis of Insect Outbreak Systems: Spruce Budworm and Forest. The Journal of Animal Ecology 47: 315-332.
60. Itahana K, Zou Y, Itahana Y, Martinez J-L, Beausejour C, et al. (2003) Control of the replicative life span of human fibroblasts by p16 and the polycomb protein Bmi-1. Mol Cell Biol 23: 389-401.
61. Münch S (2011) Die Rolle der PML-Kernkörperchen in der DNA-Schadensanwort [Dissertation]: Friedrich Schiller University.
62. Kuilman T, Michaloglou C, Vredeveld LCW, Douma S, van Doorn R, et al. (2008) Oncogene-induced senescence relayed by an interleukin-dependent inflammatory network. Cell 133: 1019-1031.
63. Coppé J-P, Kauser K, Campisi J, Beauséjour CM, (2006) Secretion of vascular endothelial growth factor by primary human fibroblasts at senescence. J Biol Chem 281: 29568-29574.
64. Rodier F, Coppé J-P, Patil CK, Hoeijmakers WAM, Muñoz DP, et al. (2009) Persistent DNA damage signalling triggers senescence-associated inflammatory cytokine secretion. Nat Cell Biol 11: 973-979.
65. Shin J-S, Hong A, Solomon MJ, Lee CS, (2006) The role of telomeres and telomerase in the pathology of human cancer and aging. Pathology 38: 103-113.
66. Lee BY, Han JA, Im JS, Morrone A, Johung K, et al. (2006) Senescence-associated beta-galactosidase is lysosomal beta-galactosidase. Aging Cell 5: 187-195.
67. Chen Q, Fischer A, Reagan JD, Yan LJ, Ames BN, (1995) Oxidative DNA damage and senescence of human diploid fibroblast cells. Proc Natl Acad Sci U S A 92: 4337-4341.
68. Toussaint O, Remacle J, Dierick J-F, Pascal T, Frippiat C, et al. (2002) Stress-induced premature senescence: from biomarkers to likeliness of in vivo occurrence. Biogerontology 3: 13-17.
69. Toussaint O, Weemaels G, Debacq-Chainiaux F, Scharffetter-Kochanek K, Wlaschek M, (2011) Artefactual effects of oxygen on cell culture models of cellular senescence and stem cell biology. J Cell Physiol 226: 315-321.
70. Tan Z, (1999) Intramitotic and intraclonal variation in proliferative potential of human diploid cells: explained by telomere shortening. J Theor Biol 198: 259-268.
71. Rubelj I, Vondracek Z, (1999) Stochastic mechanism of cellular aging-abrupt telomere shortening as a model for stochastic nature of cellular aging. J Theor Biol 197: 425-438.
72. Sozou PD, Kirkwood TB, (2001) A stochastic model of cell replicative senescence based on telomere shortening, oxidative stress, and somatic mutations in nuclear and mitochondrial DNA. J Theor Biol 213: 573-586.
73. Golubev A, Khrustalev S, Butov A, (2003) An in silico investigation into the causes of telomere length heterogeneity and its implications for the Hayflick limit. J Theor Biol 225: 153-170.
74. Portugal RD, Land MGP, Svaiter BF, (2008) A computational model for telomere-dependent cell-replicative aging. Biosystems 91: 262-267.
75. Smith JR, Whitney RG, (1980) Intraclonal variation in proliferative potential of human diploid fibroblasts: stochastic mechanism for cellular aging. Science 207: 82-84.
76. Csikász-Nagy A, Battogtokh D, Chen KC, Novák B, Tyson JJ, (2006) Analysis of a generic model of eukaryotic cell-cycle regulation. Biophys J 90: 4361-4379.
77. Tyson JJ, Novak B, (2008) Temporal organization of the cell cycle. Curr Biol 18: R759-R768.
78. Passos JF, Nelson G, Wang C, Richter T, Simillion C, et al. (2010) Feedback between p21 and reactive oxygen production is necessary for cell senescence. Mol Syst Biol 6: 347.