Accelerated DNA replication in E2F1- and E2F2-deficient macrophages leads to induction of the DNA damage response and p21 CIP1-dependent senescence

Oncogene

Volumn 29, Issue 41, 2010, Pages 5579-5590

  Iglesias Ara, A ^a   Zenarruzabeitia, O ^a   Fernandez Rueda, J ^a   Sanchez Tillo E ^b   Field, S J ^c   Celada, A ^b   Zubiaga, A M ^a  

^a UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

DNA damage response; DNA hyper replication; E2F; macrophage; senescence

Indexed keywords

PROTEIN P21; TRANSCRIPTION FACTOR E2F1; TRANSCRIPTION FACTOR E2F2;

ANIMAL CELL; ARTICLE; BONE MARROW; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CONTROLLED STUDY; DNA DAMAGE; DNA REPLICATION; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; BONE MARROW CELLS; CELL AGING; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DNA DAMAGE; DNA REPLICATION; E2F1 TRANSCRIPTION FACTOR; E2F2 TRANSCRIPTION FACTOR; FLOW CYTOMETRY; IMMUNOBLOTTING; MACROPHAGES; MICE; MICE, KNOCKOUT; TIME FACTORS;

MUS;

EID: 77958014513     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2010.296     Document Type: Article

References (41)

1. Aslanian A, Iaquinta PJ, Verona R, Lees JA. (2004). Repression of the Arf tumor suppressor by E2F3 is required for normal cell cycle kinetics. Genes Dev 18: 1413-1422.
2. Balomenos D, Martn-Caballero J, Garca MI, Prieto I, Flores JM, Serrano M et al. (2000). The cell cycle inhibitor p21 controls T-cell proliferation and sex-linked lupus development. Nat Med 6: 171-176.
3. Bartkova J, Rezaei N, Liontos M, Karakaidos P, Kletsas D, Issaeva N et al. (2006). Oncogene-induced senescence is part of the tumori-genesis barrier imposed by DNA damage checkpoints. Nature 444: 633-637.
4. Brackman D, Lund-Johansen F, Aarskog D. (1995). Expression of leukocyte differentiation antigens during the differentiation of HL-60 cells induced by 1,25-dihydroxyvitamin D3: comparison with the maturation of normal monocytic and granulocytic bone marrow cells. J Leukoc Biol 58: 547-555.
5. Braun SE, Mantel C, Rosenthal M, Cooper S, Liu L, Robertson KA et al. (1998). A positive effect of p21cip1/waf1 in the colony formation from murine myeloid progenitor cells as assessed by retroviral-mediated gene transfer. Blood Cells Mol Dis 24: 138-148.
6. Campisi J. (2005). Senescent cells, tumor suppression, and organismal aging: good citizens, bad neighbors. Cell 120: 513-522.
7. Celada A, Borras FE, Soler C, Lloberas J, Klemsz M, van Beveren C et al. (1996). The transcription factor PU.1 is involved in macrophage proliferation. J Exp Med 184: 61-69.
8. Chen D, Pacal M, Wenzel P, Knoepfler PS, Leone G, Bremner R. (2009). Division and apoptosis of E2f-deficient retinal progenitors. Nature 462: 925-929.
9. Chen Z, Trotman LC, Shaffer D, Lin HK, Dotan ZA, Niki M et al. (2005). Crucial role of p53-dependent cellular senescence in suppression of Pten-deficient tumorigenesis. Nature 436: 725-730.
10. Chong JL, Wenzel PL, Saenz-Robles MT, Nair V, Ferrey A, Hagan JP et al. (2009). E2f1-3 switch from activators in progenitor cells to repressors in differentiating cells. Nature 462: 930-934.
11. Collado M, Gil J, Efeyan A, Guerra C, Schuhmacher AJ, Barradas M et al. (2005). Tumour biology: senescence in premalignant tumours. Nature 436: 642.
12. Davidson IF, Li A, Blow JJ. (2006). Deregulated replication licensing causes DNA fragmentation consistent with head-to-tail fork collision. Mol Cell 24: 433-443.
13. Di Micco R, Fumagalli M, Cicalese A, Piccinin S, Gasparini P, Luise C et al. (2006). Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 444: 638-642.
14. Dimova DK, Dyson NJ. (2005). The E2F transcriptional network: old acquaintances with new faces. Oncogene 24: 2810-2826.
15. Dirlam A, Spike BT, Macleod KF. 2007. Deregulated E2f-2 underlies cell cycle and maturation defects in retinoblastoma null erythro-blasts. Mol Cell Biol 27: 8713-8728.
16. Ekholm-Reed S, Mendez J, Tedesco D, Zetterberg A, Stillman B, Reed SI. (2004). Deregulation of cyclin E in human cells interferes with prereplication complex assembly. J Cell Biol 165: 789-800.
17. Field SJ, Tsai FY, Kuo F, Zubiaga AM, Kaelin Jr. WG, Livingston DM et al. (1996). E2F-1 functions in mice to promote apoptosis and suppress proliferation. Cell 85: 549-561.
18. Herbig U, Jobling WA, Chen BP, 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.
19. Hwang HC, Clurman BE. (2005). Cyclin E in normal and neoplastic cell cycles. Oncogene 24: 2776-2786.
20. Iglesias A, Murga M, Laresgoiti U, Skoudy A, Bernales I, Fullaondo A et al. (2004). Diabetes and exocrine pancreatic insufficiency in E2F1/E2F2 double-mutant mice. J Clin Invest 113: 1398-1407.
21. Infante A, Laresgoiti U, Fernandez-Rueda J, Fullaondo A, Galan J, Daz-Uriarte R et al. (2008). E2F2 represses cell cycle regulators to maintain quiescence. Cell Cycle 7: 3915-3927.
22. Kinross KM, Clark AJ, Iazzolino RM, Humbert PO. (2006). E2f4 regulates fetal erythropoiesis through the promotion of cellular proliferation. Blood 108: 886-895.
23. Lazzerini Denchi E, Attwooll C, Pasini D, Helin K. (2005). Deregulated E2F activity induces hyperplasia and senescence-like features in the mouse pituitary gland. Mol Cell Biol 25: 2660-2672.
24. Li FX, Zhu JW, Hogan CJ, DeGregori J. (2003). Defective gene expression, S phase progression, and maturation during hematopoi-esis in E2F1/E2F2 mutant mice. Mol Cell Biol 23: 3607-3622.
25. Liu Q, VanHoy RW, Zhou JH, Dantzer R, Freund GG, Kelley KW. (1999). Elevated cyclin E levels, inactive retinoblastoma protein, and suppression of the p27(KIP1) inhibitor characterize early development of promyeloid cells into macrophages. Mol Cell Biol 19: 6229-6239.
26. Lowe SW, Cepero E, Evan G. (2004). Intrinsic tumour suppression. Nature 432: 307-315.
27. Lukas J, Bartkova J, Bartek J. (1996). Convergence of mitogenic signalling cascades from diverse classes of receptors at the cyclin D-cyclin-dependent kinase-pRb-controlled G1 checkpoint. Mol Cell Biol 16: 6917-6925.
28. Morris EJ, Ji JY, Yang F, Di Stefano L, Herr A, Moon NS et al. (2008). E2F1 represses beta-catenin transcription and is antagonized by both pRB and CDK8. Nature 455: 552-556.
29. Murga M, Fernandez-Capetillo O, Field SJ, Moreno B, Borlado LR, Fujiwara Y et al. (2001). Mutation of E2F2 in mice causes enhanced T lymphocyte proliferation, leading to the development of autoimmunity. Immunity 15: 959-970.
30. Olsen CL, Gardie B, Yaswen P, Stampfer MR. (2002). Raf-1-induced growth arrest in human mammary epithelial cells is p16-indepen-dent and is overcome in immortal cells during conversion. Oncogene 21: 6328-6339.
31. Paulson QX, Pusapati RV, Hong S, Weaks RL, Conti CJ, Johnson DG. (2008). Transgenic expression of E2F3a causes DNA damage leading to ATM-dependent apoptosis. Oncogene 27: 4954-4961.
32. Pusapati RV, Weaks RL, Rounbehler RJ, McArthur MJ, Johnson DG. (2010). E2F2 suppresses Myc-induced proliferation and tumorigenesis. Mol Carcinogen 49: 152-156.
33. Scheijen B, Bronk M, van der Meer T, De Jong D, Bernards R. (2004). High incidence of thymic epithelial tumors in E2F2 transgenic mice. J Biol Chem 279: 10476-11083.
34. Serrano M, Lin AW, McCurrach ME, Beach D, Lowe W. (1997). Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88: 593-602.
35. Shieh SY, Ikeda M, Taya Y, Prives C. (1997). DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2. Cell 91: 325-334.
36. Timmers C, Sharma N, Opavsky R, Maiti B, Wu L, Wu J et al. (2007). E2f1, E2f2, and E2f3 control E2F target expression and cellular proliferation via a p53-dependent negative feedback loop. Mol Cell Biol 27: 65-78.
37. Wang ZM, Yang H, Livingston DM. (1998). Endogenous E2F-1 promotes timely G0 exit of resting mouse embryo fibroblasts. Proc Natl Acad Sci USA 95: 15583-15586.
38. Wu L, Timmers C, Maiti B, Saavedra HI, Sang L, Chong GT et al. (2001). The E2F1-3 transcription factors are essential for cellular proliferation. Nature 414: 457-462.
39. Xaus J, Cardo M, Valledor AF, Soler C, Lloberas J, Celada A. (1999). Interferon gamma induces the expression of p21waf-1 and arrests macrophage cell cycle, preventing induction of apoptosis. Immunity 11: 103-113.
40. Young AP, Nagarajan R, Longmore GD. (2003). Mechanisms of transcriptional regulation by Rb-E2F segregate by biological pathway. Oncogene 22: 7209-7217.
41. Zhu JW, Field SJ, Gore L, Thompson M, Yang H, Fujiwara Y et al. (2001). E2F1 and E2F2 determine thresholds for antigen-induced T-cell proliferation and suppress tumorigenesis. Mol Cell Biol 21: 8547-8564.