Global reorganization of the nuclear landscape in senescent cells

Cell Reports

Volumn 10, Issue 4, 2015, Pages 471-483

  Chandra, Tamir ^a,b   Ewels, Philip Andrew ^a   Schoenfelder, Stefan ^a   Furlan Magaril, Mayra ^a   Wingett, Steven William ^a   Kirschner, Kristina ^c   Thuret, Jean Yves ^d   Andrews, Simon ^a   Fraser, Peter ^a   Reik, Wolf ^a,b  

^a BABRAHAM INSTITUTE   (United Kingdom)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d DIF   (France)

Author keywords

[No Author keywords available]

Indexed keywords

LAMIN; CHROMATIN; HETEROCHROMATIN;

ARTICLE; CELL AGING; CELL DIFFERENTIATION; CELL DIVISION; CELLULAR SENESCENCE; CHROMATIN STRUCTURE; CHROMOSOME POSITIONING; CHROMOSOMES AND CHROMOSOMAL PHENOMENA; CONSTITUTIVE HETEROCHROMATIN; CONTROLLED STUDY; EMBRYONIC STEM CELL; HETEROCHROMATIN; SENESCENCE ASSOCIATED HETEROCHROMATIC FOCI; SEQUENCE ANALYSIS; SOMATIC CELL; CELL LINE; CELL PROLIFERATION; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; FLUORESCENCE IN SITU HYBRIDIZATION; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY;

CELL AGING; CELL LINE; CELL PROLIFERATION; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; HETEROCHROMATIN; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE;

EID: 84922788164     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.12.055     Document Type: Article

References (65)

1. Acosta J.C., O'Loghlen A., Banito A., Guijarro M.V., Augert A., Raguz S., Fumagalli M., Da Costa M., Brown C., Popov N., et al. Chemokine signaling via the CXCR2 receptor reinforces senescence. Cell 2008, 133:1006-1018.
2. Acosta J.C., Banito A., Wuestefeld T., Georgilis A., Janich P., Morton J.P., Athineos D., Kang T.-W., Lasitschka F., Andrulis M., et al. A complex secretory program orchestrated by the inflammasome controls paracrine senescence. Nat. Cell Biol. 2013, 15:978-990.
3. 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.
4. Banito A., Rashid S.T., Acosta J.C., Li S., Pereira C.F., Geti I., Pinho S., Silva J.C., Azuara V., Walsh M., et al. Senescence impairs successful reprogramming to pluripotent stem cells. Genes Dev. 2009, 23:2134-2139.
5. Bartkova J., Rezaei N., Liontos M., Karakaidos P., Kletsas D., Issaeva N., Vassiliou L.-V.F., Kolettas E., Niforou K., Zoumpourlis V.C., et al. Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 2006, 444:633-637.
6. Benson E.K., Lee S.W., Aaronson S.A. Role of progerin-induced telomere dysfunction in HGPS premature cellular senescence. J.Cell Sci. 2010, 123:2605-2612.
7. Bernardi G. The genome: an isochore ensemble and its evolution. Ann. N Y Acad. Sci. 2012, 1267:31-34.
8. Bolland D.J., King M.R., Reik W., Corcoran A.E., Krueger C. Robust 3D DNA FISH using directly labeled probes. J.Vis. Exp 2013, e50587.
9. Braig M., Lee S., Loddenkemper C., Rudolph C., Peters A.H.F.M., Schlegelberger B., Stein H., Dörken B., Jenuwein T., Schmitt C.A. Oncogene-induced senescence as an initial barrier in lymphoma development. Nature 2005, 436:660-665.
10. Cao K., Blair C.D., Faddah D.A., Kieckhaefer J.E., Olive M., Erdos M.R., Nabel E.G., Collins F.S. Progerin and telomere dysfunction collaborate to trigger cellular senescence in normal human fibroblasts. J.Clin. Invest. 2011, 121:2833-2844.
11. Chan H.M., Narita M., Lowe S.W., Livingston D.M. The p400 E1A-associated protein is a novel component of the p53 -> p21 senescence pathway. Genes Dev. 2005, 19:196-201.
12. Chandra T., Narita M. High-order chromatin structure and the epigenome in SAHFs. Nucleus 2013, 4:23-28.
13. Chandra T., Kirschner K., Thuret J.-Y., Pope B.D., Ryba T., Newman S., Ahmed K., Samarajiwa S.A., Salama R., Carroll T., et al. Independence of repressive histone marks and chromatin compaction during senescent heterochromatic layer formation. Mol. Cell 2012, 47:203-214.
14. Chicas A., Wang X., Zhang C., McCurrach M., Zhao Z., Mert O., Dickins R.A., Narita M., Zhang M., Lowe S.W. Dissecting the unique role of the retinoblastoma tumor suppressor during cellular senescence. Cancer Cell 2010, 17:376-387.
15. Coppé J.-P., Patil C.K., Rodier F., Sun Y., Muñoz D.P., Goldstein J., Nelson P.S., Desprez P.-Y., Campisi J. Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol. 2008, 6:2853-2868.
16. Costantini M., Clay O., Auletta F., Bernardi G. An isochore map of human chromosomes. Genome Res. 2006, 16:536-541.
17. Costantini M., Auletta F., Bernardi G. The distributions of "new" and "old" Alu sequences in the human genome: the solution of a "mystery". Mol. Biol. Evol. 2012, 29:421-427.
18. Cruickshanks H.A., McBryan T., Nelson D.M., Vanderkraats N.D., Shah P.P., van Tuyn J., Singh Rai T., Brock C., Donahue G., Dunican D.S., et al. Senescent cells harbour features of the cancer epigenome. Nat. Cell Biol. 2013, 15:1495-1506.
19. De Cecco M., Criscione S.W., Peckham E.J., Hillenmeyer S., Hamm E.A., Manivannan J., Peterson A.L., Kreiling J.A., Neretti N., Sedivy J.M. Genomes of replicatively senescent cells undergo global epigenetic changes leading to gene silencing and activation of transposable elements. Aging Cell 2013, 12:247-256.
20. Di Leonardo A., Linke S.P., Clarkin K., Wahl G.M. DNA damage triggers a prolonged p53-dependent G1 arrest and long-term induction of Cip1 in normal human fibroblasts. Genes Dev. 1994, 8:2540-2551.
21. Di Micco R., Fumagalli M., Cicalese A., Piccinin S., Gasparini P., Luise C., Schurra C., Garre' M., Nuciforo P.G., Bensimon A., et al. Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 2006, 444:638-642.
22. Di Micco R., Sulli G., Dobreva M., Liontos M., Botrugno O.A., Gargiulo G., dal Zuffo R., Matti V., d'Ario G., Montani E., et al. Interplay between oncogene-induced DNA damage response and heterochromatin in senescence and cancer. Nat. Cell Biol. 2011, 13:292-302.
23. Dixon J.R., Selvaraj S., Yue F., Kim A., Li Y., Shen Y., Hu M., Liu J.S., Ren B. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 2012, 485:376-380.
24. Eriksson M., Brown W.T., Gordon L.B., Glynn M.W., Singer J., Scott L., Erdos M.R., Robbins C.M., Moses T.Y., Berglund P., et al. Recurrent de novo point mutations in lamin A cause Hutchinson-Gilford progeria syndrome. Nature 2003, 423:293-298.
25. Funayama R., Saito M., Tanobe H., Ishikawa F. Loss of linker histone H1 in cellular senescence. J.Cell Biol. 2006, 175:869-880.
26. Haugstetter A.M., Loddenkemper C., Lenze D., Gröne J., Standfuss C., Petersen I., Dörken B., Schmitt C.A. Cellular senescence predicts treatment outcome in metastasised colorectal cancer. Br. J. Cancer 2010, 103:505-509.
27. Hayflick L., Moorhead P.S. The serial cultivation of human diploid cell strains. Exp. Cell Res. 1961, 25:585-621.
28. Heinz S., Benner C., Spann N., Bertolino E., Lin Y.C., Laslo P., Cheng J.X., Murre C., Singh H., Glass C.K. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 2010, 38:576-589.
29. Hiratani I., Leskovar A., Gilbert D.M. Differentiation-induced replication-timing changes are restricted to AT-rich/long interspersed nuclear element (LINE)-rich isochores. Proc. Natl. Acad. Sci. USA 2004, 101:16861-16866.
30. Hirosue A., Ishihara K., Tokunaga K., Watanabe T., Saitoh N., Nakamoto M., Chandra T., Narita M., Shinohara M., Nakao M. Quantitative assessment of higher-order chromatin structure of the INK4/ARF locus in human senescent cells. Aging Cell 2012, 11:553-556.
31. 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 ageing modified by the cyclin-dependent kinase inhibitor p16INK4a. Nature 2006, 443:421-426.
32. Jeanblanc M., Ragu S., Gey C., Contrepois K., Courbeyrette R., Thuret J.-Y., Mann C. Parallel pathways in RAF-induced senescence and conditions for its reversion. Oncogene 2012, 31:3072-3085.
33. Kalhor R., Tjong H., Jayathilaka N., Alber F., Chen L. Genome architectures revealed by tethered chromosome conformation capture and population-based modeling. Nat. Biotechnol. 2012, 30:90-98.
34. Kuilman T., Michaloglou C., Vredeveld L.C.W., Douma S., van Doorn R., Desmet C.J., Aarden L.A., Mooi W.J., Peeper D.S. Oncogene-induced senescence relayed by an interleukin-dependent inflammatory network. Cell 2008, 133:1019-1031.
35. Li H., Collado M., Villasante A., Strati K., Ortega S., Cañamero M., Blasco M.A., Serrano M. The Ink4/Arf locus is a barrier for iPS cell reprogramming. Nature 2009, 460:1136-1139.
36. Lieberman-Aiden E., van Berkum N.L., Williams L., Imakaev M., Ragoczy T., Telling A., Amit I., Lajoie B.R., Sabo P.J., Dorschner M.O., et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 2009, 326:289-293.
37. Lin A.W., Barradas M., Stone J.C., van Aelst L., Serrano M., Lowe S.W. Premature senescence involving p53 and p16 is activated in response to constitutive MEK/MAPK mitogenic signaling. Genes Dev. 1998, 12:3008-3019.
38. López-Otín C., Blasco M.A., Partridge L., Serrano M., Kroemer G. The hallmarks of aging. Cell 2013, 153:1194-1217.
39. Macaya G., Thiery J.P., Bernardi G. An approach to the organization of eukaryotic genomes at a macromolecular level. J.Mol. Biol. 1976, 108:237-254.
40. Manukyan M., Singh P.B. Epigenetic rejuvenation. Genes Cells 2012, 17:337-343.
41. McCord R.P., Nazario-Toole A., Zhang H., Chines P.S., Zhan Y., Erdos M.R., Collins F.S., Dekker J., Cao K. Correlated alterations in genome organization, histone methylation, and DNA-lamin A/C interactions in Hutchinson-Gilford progeria syndrome. Genome Res. 2013, 23:260-269.
42. Michaloglou C., Vredeveld L.C.W., Soengas M.S., Denoyelle C., Kuilman T., van der Horst C.M.A.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.
43. Muñoz-Espín D., Cañamero M., Maraver A., Gómez-López G., Contreras J., Murillo-Cuesta S., Rodríguez-Baeza A., Varela-Nieto I., Ruberte J., Collado M., Serrano M. Programmed cell senescence during mammalian embryonic development. Cell 2013, 155:1104-1118.
44. Narita M., Nũnez 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.
45. Narita M., Narita M., Krizhanovsky V., Nuñez S., Chicas A., Hearn S.A., Myers M.P., Lowe S.W. A novel role for high-mobility group a proteins in cellular senescence and heterochromatin formation. Cell 2006, 126:503-514.
46. Nora E.P., Lajoie B.R., Schulz E.G., Giorgetti L., Okamoto I., Servant N., Piolot T., van Berkum N.L., Meisig J., Sedat J., et al. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 2012, 485:381-385.
47. Peric-Hupkes D., Meuleman W., Pagie L., Bruggeman S.W.M., Solovei I., Brugman W., Gräf S., Flicek P., Kerkhoven R.M., van Lohuizen M., et al. Molecular maps of the reorganization of genome-nuclear lamina interactions during differentiation. Mol. Cell 2010, 38:603-613.
48. Rando T.A., Chang H.Y. Aging, rejuvenation, and epigenetic reprogramming: resetting the aging clock. Cell 2012, 148:46-57.
49. Reimann M., Lee S., Loddenkemper C., Dörr J.R., Tabor V., Aichele P., Stein H., Dörken B., Jenuwein T., Schmitt C.A. Tumor stroma-derived TGF-beta limits myc-driven lymphomagenesis via Suv39h1-dependent senescence. Cancer Cell 2010, 17:262-272.
50. Sadaie M., Salama R., Carroll T., Tomimatsu K., Chandra T., Young A.R.J., Narita M., Pérez-Mancera P.A., Bennett D.C., Chong H., et al. Redistribution of the Lamin B1 genomic binding profile affects rearrangement of heterochromatic domains and SAHF formation during senescence. Genes Dev. 2013, 27:1800-1808.
51. Scaffidi P., Misteli T. Lamin A-dependent nuclear defects in human aging. Science 2006, 312:1059-1063.
52. Serrano M., Lin A.W., McCurrach M.E., Beach D., Lowe S.W. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 1997, 88:593-602.
53. Shah P.P., Donahue G., Otte G.L., Capell B.C., Nelson D.M., Cao K., Aggarwala V., Cruickshanks H.A., Rai T.S., McBryan T., et al. Lamin B1 depletion in senescent cells triggers large-scale changes in gene expression and the chromatin landscape. Genes Dev. 2013, 27:1787-1799.
54. Shimi T., Butin-Israeli V., Adam S.A., Hamanaka R.B., Goldman A.E., Lucas C.A., Shumaker D.K., Kosak S.T., Chandel N.S., Goldman R.D. The role of nuclear lamin B1 in cell proliferation and senescence. Genes Dev. 2011, 25:2579-2593.
55. Shumaker D.K., Dechat T., Kohlmaier A., Adam S.A., Bozovsky M.R., Erdos M.R., Eriksson M., Goldman A.E., Khuon S., Collins F.S., et al. Mutant nuclear lamin A leads to progressive alterations of epigenetic control in premature aging. Proc. Natl. Acad. Sci. USA 2006, 103:8703-8708.
56. Sofueva S., Yaffe E., Chan W.-C., Georgopoulou D., Vietri Rudan M., Mira-Bontenbal H., Pollard S.M., Schroth G.P., Tanay A., Hadjur S. Cohesin-mediated interactions organize chromosomal domain architecture. EMBO J. 2013, 32:3119-3129.
57. Storer M., Mas A., Robert-Moreno A., Pecoraro M., Ortells M.C., Di Giacomo V., Yosef R., Pilpel N., Krizhanovsky V., Sharpe J., Keyes W.M. Senescence is a developmental mechanism that contributes to embryonic growth and patterning. Cell 2013, 155:1119-1130.
58. Swanson E.C., Manning B., Zhang H., Lawrence J.B. Higher-order unfolding of satellite heterochromatin is a consistent and early event in cell senescence. J.Cell Biol. 2013, 203:929-942.
59. Thiery J.P., Macaya G., Bernardi G. An analysis of eukaryotic genomes by density gradient centrifugation. J.Mol. Biol. 1976, 108:219-235.
60. Tu Z., Zhuang X., Yao Y.-G., Zhang R. BRG1 is required for formation of senescence-associated heterochromatin foci induced by oncogenic RAS or BRCA1 loss. Mol. Cell. Biol. 2013, 33:1819-1829.
61. Xue W., Zender L., Miething C., Dickins R.A., Hernando E., Krizhanovsky V., Cordon-Cardo C., Lowe S.W. Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature 2007, 445:656-660.
62. Ye X., Zerlanko B., Kennedy A., Banumathy G., Zhang R., Adams P.D. Downregulation of Wnt signaling is a trigger for formation of facultative heterochromatin and onset of cell senescence in primary human cells. Mol. Cell 2007, 27:183-196.
63. Ye X., Zerlanko B., Zhang R., Somaiah N., Lipinski M., Salomoni P., Adams P.D. Definition of pRB- and p53-dependent and -independent steps in HIRA/ASF1a-mediated formation of senescence-associated heterochromatin foci. Mol. Cell. Biol. 2007, 27:2452-2465.
64. Young A.R.J., Narita M., Ferreira M., Kirschner K., Sadaie M., Darot J.F.J., Tavaré S., Arakawa S., Shimizu S., Watt F.M., Narita M. Autophagy mediates the mitotic senescence transition. Genes Dev. 2009, 23:798-803.
65. Zhang R., Poustovoitov M.V., Ye X., Santos H.A., Chen W., Daganzo S.M., Erzberger J.P., Serebriiskii I.G., Canutescu A.A., Dunbrack R.L., et al. Formation of MacroH2A-containing senescence-associated heterochromatin foci and senescence driven by ASF1a and HIRA. Dev. Cell 2005, 8:19-30.