XSenescence is a developmental mechanism that contributes to embryonic growth and patterning

Cell

Volumn 155, Issue 5, 2013, Pages 1119-

  Storer, Mekayla ^a   Mas, Alba ^a   Robert Moreno, Alexandre ^a   Pecoraro, Matteo ^a   Ortells, M Carmen ^a   Di Giacomo, Valeria ^a   Yosef, Reut ^b   Pilpel, Noam ^b   Krizhanovsky, Valery ^b   Sharpe, James ^a   Keyes, William M ^a  

^a CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; FIBROBLAST GROWTH FACTOR; GAMMA H2AX; H3K9ME3 PROTEIN; NUCLEAR PROTEIN; PROMYELOCYTIC LEUKEMIA PROTEIN; PROTEIN P15; PROTEIN P19; PROTEIN P21; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL AGING; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; EMBRYONIC STRUCTURES; FEMALE; FORELIMB; HOMEOBOX; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MESENCHYME; MESENCHYME CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

MUS;

EID: 84889565689     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.10.041     Document Type: Article

References (69)

1. J.C. Acosta, A. O'Loghlen, A. Banito, M.V. Guijarro, A. Augert, S. Raguz, M. Fumagalli, M. Da Costa, C. Brown, and N. Popov Chemokine signaling via the CXCR2 receptor reinforces senescence Cell 133 2008 1006 1018
2. J.C. Acosta, A. Banito, T. Wuestefeld, A. Georgilis, P. Janich, J.P. Morton, D. Athineos, T.W. Kang, F. Lasitschka, and M. Andrulis A complex secretory program orchestrated by the inflammasome controls paracrine senescence Nat. Cell Biol. 15 2013 978 990
3. D.A. Alcorta, Y. Xiong, D. Phelps, G. Hannon, D. Beach, and J.C. Barrett Involvement of the cyclin-dependent kinase inhibitor p16 (INK4a) in replicative senescence of normal human fibroblasts Proc. Natl. Acad. Sci. USA 93 1996 13742 13747
4. D.J. Baker, T. Wijshake, T. Tchkonia, N.K. LeBrasseur, B.G. Childs, B. van de Sluis, J.L. Kirkland, and J.M. van Deursen Clearance of p16Ink4a-positive senescent cells delays ageing-associated disorders Nature 479 2011 232 236
5. M. Braig, S. Lee, C. Loddenkemper, C. Rudolph, A.H. Peters, B. Schlegelberger, H. Stein, B. Dörken, T. Jenuwein, and C.A. Schmitt Oncogene-induced senescence as an initial barrier in lymphoma development Nature 436 2005 660 665
6. J. Brugarolas, C. Chandrasekaran, J.I. Gordon, D. Beach, T. Jacks, and G.J. Hannon Radiation-induced cell cycle arrest compromised by p21 deficiency Nature 377 1995 552 557
7. J. Capdevila, and J.C. Izpisúa Belmonte Patterning mechanisms controlling vertebrate limb development Annu. Rev. Cell Dev. Biol. 17 2001 87 132
8. B.D. Chang, K. Watanabe, E.V. Broude, J. Fang, J.C. Poole, T.V. Kalinichenko, and I.B. Roninson Effects of p21Waf1/Cip1/Sdi1 on cellular gene expression: implications for carcinogenesis, senescence, and age-related diseases Proc. Natl. Acad. Sci. USA 97 2000 4291 4296
9. Z. Chen, L.C. Trotman, D. Shaffer, H.K. Lin, Z.A. Dotan, M. Niki, J.A. Koutcher, H.I. Scher, T. Ludwig, and W. Gerald Crucial role of p53-dependent cellular senescence in suppression of Pten-deficient tumorigenesis Nature 436 2005 725 730
10. V.V. Chizhikov, and K.J. Millen Mechanisms of roof plate formation in the vertebrate CNS Nat. Rev. Neurosci. 5 2004 808 812
11. D. Cobrinik, M.H. Lee, G. Hannon, G. Mulligan, R.T. Bronson, N. Dyson, E. Harlow, D. Beach, R.A. Weinberg, and T. Jacks Shared role of the pRB-related p130 and p107 proteins in limb development Genes Dev. 10 1996 1633 1644
12. M.J. Cohn, J.C. Izpisúa-Belmonte, H. Abud, J.K. Heath, and C. Tickle Fibroblast growth factors induce additional limb development from the flank of chick embryos Cell 80 1995 739 746
13. M. Collado, J. Gil, A. Efeyan, C. Guerra, A.J. Schuhmacher, M. Barradas, A. Benguría, A. Zaballos, J.M. Flores, and M. Barbacid Tumour biology: senescence in premalignant tumours Nature 436 2005 642
14. J.P. Coppé, K. Kauser, J. Campisi, and C.M. Beauséjour Secretion of vascular endothelial growth factor by primary human fibroblasts at senescence J. Biol. Chem. 281 2006 29568 29574
15. J.P. Coppé, C.K. Patil, F. Rodier, Y. Sun, D.P. Muñoz, J. Goldstein, P.S. Nelson, P.Y. Desprez, and J. Campisi Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor PLoS Biol. 6 2008 2853 2868
16. J.P. Coppé, P.Y. Desprez, A. Krtolica, and J. Campisi The senescence-associated secretory phenotype: the dark side of tumor suppression Annu. Rev. Pathol. 5 2010 99 118
17. L.B. Corson, Y. Yamanaka, K.M. Lai, and J. Rossant Spatial and temporal patterns of ERK signaling during mouse embryogenesis Development 130 2003 4527 4537
18. C. Deng, P. Zhang, J.W. Harper, S.J. Elledge, and P. Leder Mice lacking p21CIP1/WAF1 undergo normal development, but are defective in G1 checkpoint control Cell 82 1995 675 684
19. V. Devgan, B.C. Nguyen, H. Oh, and G.P. Dotto p21WAF1/Cip1 suppresses keratinocyte differentiation independently of the cell cycle through transcriptional up-regulation of the IGF-I gene J. Biol. Chem. 281 2006 30463 30470
20. G.P. Dimri, X. Lee, G. Basile, M. Acosta, G. Scott, C. Roskelley, E.E. Medrano, M. Linskens, I. Rubelj, and O. Pereira-Smith A biomarker that identifies senescent human cells in culture and in aging skin in vivo Proc. Natl. Acad. Sci. USA 92 1995 9363 9367
21. A. Freund, A.V. Orjalo, P.Y. Desprez, and J. Campisi Inflammatory networks during cellular senescence: causes and consequences Trends Mol. Med. 16 2010 238 246
22. L.S. Gammill, and M. Bronner-Fraser Neural crest specification: migrating into genomics Nat. Rev. Neurosci. 4 2003 795 805
23. R.R. Gomis, C. Alarcón, C. Nadal, C. Van Poznak, and J. Massagué C/EBPbeta at the core of the TGFbeta cytostatic response and its evasion in metastatic breast cancer cells Cancer Cell 10 2006 203 214
24. Q. Guo, C. Loomis, and A.L. Joyner Fate map of mouse ventral limb ectoderm and the apical ectodermal ridge Dev. Biol. 264 2003 166 178
25. V. Hamburger, and H.L. Hamilton A series of normal stages in the development of the chick embryo. 1951 Dev. Dyn. 195 1992 231 272
26. G.J. Hannon, and D. Beach p15INK4B is a potential effector of TGF-beta-induced cell cycle arrest Nature 371 1994 257 261
27. L. Hayflick The limited in vitro lifetime of human diploid cell strains Exp. Cell Res. 37 1965 614 636
28. J.I. Jun, and L.F. Lau The matricellular protein CCN1 induces fibroblast senescence and restricts fibrosis in cutaneous wound healing Nat. Cell Biol. 12 2010 676 685
29. Y. Kanegae, A.T. Tavares, J.C. Izpisúa Belmonte, and I.M. Verma Role of Rel/NF-kappaB transcription factors during the outgrowth of the vertebrate limb Nature 392 1998 611 614
30. T.W. Kang, T. Yevsa, N. Woller, L. Hoenicke, T. Wuestefeld, D. Dauch, A. Hohmeyer, M. Gereke, R. Rudalska, and A. Potapova Senescence surveillance of pre-malignant hepatocytes limits liver cancer development Nature 479 2011 547 551
31. W.M. Keyes, Y. Wu, H. Vogel, X. Guo, S.W. Lowe, and A.A. Mills p63 deficiency activates a program of cellular senescence and leads to accelerated aging Genes Dev. 19 2005 1986 1999
32. S.H. Kim, J. Rowe, H. Fujii, R. Jones, B. Schmierer, B.W. Kong, K. Kuchler, D. Foster, D. Ish-Horowicz, and G. Peters Upregulation of chicken p15INK4b at senescence and in the developing brain J. Cell Sci. 119 2006 2435 2443
33. V. Krizhanovsky, M. Yon, R.A. Dickins, S. Hearn, J. Simon, C. Miething, H. Yee, L. Zender, and S.W. Lowe Senescence of activated stellate cells limits liver fibrosis Cell 134 2008 657 667
34. A. Krtolica, S. Parrinello, S. Lockett, P.Y. Desprez, and J. Campisi Senescent fibroblasts promote epithelial cell growth and tumorigenesis: a link between cancer and aging Proc. Natl. Acad. Sci. USA 98 2001 12072 12077
35. T. Kuilman, C. Michaloglou, L.C. Vredeveld, S. Douma, R. van Doorn, C.J. Desmet, L.A. Aarden, W.J. Mooi, and D.S. Peeper Oncogene-induced senescence relayed by an interleukin-dependent inflammatory network Cell 133 2008 1019 1031
36. T. Kuilman, C. Michaloglou, W.J. Mooi, and D.S. Peeper The essence of senescence Genes Dev. 24 2010 2463 2479
37. R.A. Lang, and J.M. Bishop Macrophages are required for cell death and tissue remodeling in the developing mouse eye Cell 74 1993 453 462
38. K.J. Lee, P. Dietrich, and T.M. Jessell Genetic ablation reveals that the roof plate is essential for dorsal interneuron specification Nature 403 2000 734 740
39. F.V. Mariani, C.P. Ahn, and G.R. Martin Genetic evidence that FGFs have an instructive role in limb proximal-distal patterning Nature 453 2008 401 405
40. C. Michaloglou, L.C. Vredeveld, M.S. Soengas, C. Denoyelle, T. Kuilman, C.M. van der Horst, D.M. Majoor, J.W. Shay, W.J. Mooi, and D.S. Peeper BRAFE600-associated senescence-like cell cycle arrest of human naevi Nature 436 2005 720 724
41. W.J. Mooi, and D.S. Peeper Oncogene-induced cell senescence - halting on the road to cancer N. Engl. J. Med. 355 2006 1037 1046
42. D. Muñoz-Espín, M. Cañamero, A. Maraver, G. Gómez-López, J. Contreras, S. Murillo-Cuesta, A. Rodríguez-Baeza, I. Varela-Nieto, J. Ruberte, and M. Collado Programmed cell senescence during mammalian embryonic development Cell 2013 10.1016/j.cell.2013.10.019 Published online November 14, 2013
43. M. Narita, S. Nũnez, E. Heard, M. Narita, A.W. Lin, S.A. Hearn, D.L. Spector, G.J. Hannon, and S.W. Lowe Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence Cell 113 2003 703 716
44. L. Niswander, C. Tickle, A. Vogel, I. Booth, and G.R. Martin FGF-4 replaces the apical ectodermal ridge and directs outgrowth and patterning of the limb Cell 75 1993 579 587
45. S.B. Parker, G. Eichele, P. Zhang, A. Rawls, A.T. Sands, A. Bradley, E.N. Olson, J.W. Harper, and S.J. Elledge p53-independent expression of p21Cip1 in muscle and other terminally differentiating cells Science 267 1995 1024 1027
46. S. Parrinello, J.P. Coppe, A. Krtolica, and J. Campisi Stromal-epithelial interactions in aging and cancer: senescent fibroblasts alter epithelial cell differentiation J. Cell Sci. 118 2005 485 496
47. B.Z. Qian, and J.W. Pollard Macrophage diversity enhances tumor progression and metastasis Cell 141 2010 39 51
48. F. Rae, K. Woods, T. Sasmono, N. Campanale, D. Taylor, D.A. Ovchinnikov, S.M. Grimmond, D.A. Hume, S.D. Ricardo, and M.H. Little Characterisation and trophic functions of murine embryonic macrophages based upon the use of a Csf1r-EGFP transgene reporter Dev. Biol. 308 2007 232 246
49. I.B. Roninson Oncogenic functions of tumour suppressor p21(Waf1/Cip1/Sdi1): association with cell senescence and tumour-promoting activities of stromal fibroblasts Cancer Lett. 179 2002 1 14
50. C.A. Schmitt, J.S. Fridman, M. Yang, S. Lee, E. Baranov, R.M. Hoffman, and S.W. Lowe A senescence program controlled by p53 and p16INK4a contributes to the outcome of cancer therapy Cell 109 2002 335 346
51. M. Serrano, A.W. Lin, M.E. McCurrach, D. Beach, and S.W. Lowe Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a Cell 88 1997 593 602
52. V. Shukla, X. Coumoul, R.H. Wang, H.S. Kim, and C.X. Deng RNA interference and inhibition of MEK-ERK signaling prevent abnormal skeletal phenotypes in a mouse model of craniosynostosis Nat. Genet. 39 2007 1145 1150
53. X. Sun, F.V. Mariani, and G.R. Martin Functions of FGF signalling from the apical ectodermal ridge in limb development Nature 418 2002 501 508
54. D.B. Vasey, C.R. Wolf, K. Brown, and C.B. Whitelaw Spatial p21 expression profile in the mid-term mouse embryo Transgenic Res. 20 2011 23 28
55. E. Wang Senescent human fibroblasts resist programmed cell death, and failure to suppress bcl2 is involved Cancer Res. 55 1995 2284 2292
56. W. Wood, M. Turmaine, R. Weber, V. Camp, R.A. Maki, S.R. McKercher, and P. Martin Mesenchymal cells engulf and clear apoptotic footplate cells in macrophageless PU.1 null mouse embryos Development 127 2000 5245 5252
57. Y. Xiong, G.J. Hannon, H. Zhang, D. Casso, R. Kobayashi, and D. Beach p21 is a universal inhibitor of cyclin kinases Nature 366 1993 701 704
58. W. Xue, L. Zender, C. Miething, R.A. Dickins, E. Hernando, V. Krizhanovsky, C. Cordon-Cardo, and S.W. Lowe Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas Nature 445 2007 656 660
59. H. Yoshida, Y.Y. Kong, R. Yoshida, A.J. Elia, A. Hakem, R. Hakem, J.M. Penninger, and T.W. Mak Apaf1 is required for mitochondrial pathways of apoptosis and brain development Cell 94 1998 739 750
60. P. Zhang, C. Wong, D. Liu, M. Finegold, J.W. Harper, and S.J. Elledge p21(CIP1) and p57(KIP2) control muscle differentiation at the myogenin step Genes Dev. 13 1999 213 224
61. Y. Benjamini, and Y. Hochberg Controlling the false discovery rate: a practical and powerful approach to multiple testing J. R. Stat. Soc. B 57 1995 289 300
62. Bolstad, B. (2001). Probe level quantile normalization of high density oligonucleotide array data. http://bmbolstad.com/stuff/qnorm.pdf.
63. J. Brugarolas, C. Chandrasekaran, J.I. Gordon, D. Beach, T. Jacks, and G.J. Hannon Radiation-induced cell cycle arrest compromised by p21 deficiency Nature 377 1995 552 557
64. J.L. de la Pompa, A. Wakeham, K.M. Correia, E. Samper, S. Brown, R.J. Aguilera, T. Nakano, T. Honjo, T.W. Mak, J. Rossant, and R.A. Conlon Conservation of the Notch signalling pathway in mammalian neurogenesis Development 124 1997 1139 1148
65. R.A. García-Fernández, P. García-Palencia, M.A. Sánchez, G. Gil-Gómez, B. Sánchez, E. Rollán, J. Martín-Caballero, and J.M. Flores Combined loss of p21(waf1/cip1) and p27(kip1) enhances tumorigenesis in mice Lab. Invest. 91 2011 1634 1642
66. R.C. Gentleman, V.J. Carey, D.M. Bates, B. Bolstad, M. Dettling, S. Dudoit, B. Ellis, L. Gautier, Y. Ge, and J. Gentry Bioconductor: open software development for computational biology and bioinformatics Genome Biol. 5 2004 R80
67. M.E. Ritchie, J. Silver, A. Oshlack, M. Holmes, D. Diyagama, A. Holloway, and G.K. Smyth A comparison of background correction methods for two-colour microarrays Bioinformatics 23 2007 2700 2707
68. J. Sharpe, U. Ahlgren, P. Perry, B. Hill, A. Ross, J. Hecksher-Sørensen, R. Baldock, and D. Davidson Optical projection tomography as a tool for 3D microscopy and gene expression studies Science 296 2002 541 545
69. G.K. Smyth Linear models and empirical bayes methods for assessing differential expression in microarray experiments Stat. Appl. Genet. Mol. Biol. 3 2004 e3