Distinct cellular responses to replication stress leading to apoptosis or senescence

. 2019 May ; 9 (5) : 870-890. [epub] 20190413

Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid30982228

Replication stress (RS) is a major driver of genomic instability and tumorigenesis. Here, we investigated whether RS induced by the nucleotide analog fludarabine and specific kinase inhibitors [e.g. targeting checkpoint kinase 1 (Chk1) or ataxia telangiectasia and Rad3-related (ATR)] led to apoptosis or senescence in four cancer cell lines differing in TP53 mutation status and expression of lamin A/C (LA/C). RS resulted in uneven chromatin condensation in all cell types, as evidenced by the presence of metaphasic chromosomes with unrepaired DNA damage, as well as detection of less condensed chromatin in the same nucleus, frequent ultrafine anaphase bridges, and micronuclei. We observed that responses to these chromatin changes may be distinct in individual cell types, suggesting that expression of lamin A/C and lamin B1 (LB1) may play an important role in the transition of damaged cells to senescence. MCF7 mammary carcinoma cells harboring wild-type p53 (WT-p53) and LA/C responded to RS by transition to senescence with a significant reduction of lamin B receptor and LB1 proteins. In contrast, a lymphoid cancer cell line WSU-NHL (WT-p53) lacking LA/C and expressing low levels of LB1 died after several hours, while lines MEC-1 and SU-DHL-4, both with mutated p53, and SU-DHL-4 with mutations in LA/C, died at different rates by apoptosis. Our results show that, in addition to being influenced by p53 mutation status, the response to RS (apoptosis or senescence) may also be influenced by lamin A/C and LB1 status.

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Zeman MK and Ciprich KA (2014) Causes and consequences of replication stress. Nat Cell Biol 16, 2–9. PubMed PMC

Cimprich KA and Cortez D (2000) ATR: an essential regulator of genome integrity. Nat Rev Mol Cell Biol 9, 612–627. PubMed PMC

Lukas C, Savic V, Bekker‐Jensen S, Doil C, Neumann B, Pedersen RS, Grofte M, Chan KL, Hickson ID, Bartek J et al (2011) 53BP1 nuclear bodies form around DNA lesions generated by mitotic transmission of chromosomes under replication stress. Nat Cell Biol 13, 243–253. PubMed

Liu Q, Guntuku S, Ciu XS, Matsuoka S, Cortez D, Tamai K, Luo G, Carattini‐Rivera S, DeMayo F, Bradley A et al (2000) Chk1 is an essential kinase that is regulated by ATR and required for the G(2)M DNA damage checkpoint. Genes Dev 1, 1448–1459. PubMed PMC

Zou L and Elledge SJ (2003) Sensing DNA damage through ATRIP recognition of RPA‐ssDNA complexes. Science 300, 1542–1548. PubMed

Syljuasen RG, Sorensen CS, Hansen LT, Fugger K, Lundin C, Johansson F, Helleday T, Sehested M, Lukas J and Bartek J (2005) Inhibition of human Chk1 causes increased initiation of DNA replication, phosphorylation of ATR targets and DNA breakage. Mol Cell Biol 25, 3553–3562. PubMed PMC

Branzei D and Foiani M (2010) Maintaining genome stability at the replication fork. Nat Rev Mol Cell Biol 11, 208–219. PubMed

Debatisse M, Le Tallec B, Letessier A, Dutrillaux B and Brison O (2012) Common fragile sites: mechanisms of instability revisited. Trends Genet 28, 22–32. PubMed

Mankouri HW, Huttner D and Hickson ID (2013) How unfinished business from S‐phase affects mitosis and beyond. EMBO J 32, 2661–2671. PubMed PMC

Mackay DR and Ullman KS (2015) ATR and Chk1‐Aurora B pathway coordinate postmitotic surveillance with cytokinetic abscission. Mol Biol Cell 26, 2217–2226. PubMed PMC

Pedersen RS, Karemore G, Gudjonsson T, Rask MB, Neumann B, Hériché JK, Papperkok R, Ellenberg J, Gerlich DW, Lukas J et al (2016) Profiling DNA damage response following mitotic perturbations. Nat Commun 7, 13887. PubMed PMC

Brough R, Frankum JR, Costa‐Cabral S, Lord CJ and Ashworth A (2011) Searching for synthetic lethality in cancer. Curr Opin Genet Dev 21, 34–41. PubMed

Garrett MD and Collins I (2011) Anticancer therapy with checkpoint inhibitors: what, where and when? Trends Pharmacol Sci 32, 308–316. PubMed

Hirao A, Kong YY, Matsuoka S, Wakeham A, Ruland J, Yoshida H, Liu D, Elledge SJ and Mak TW (2008) DNA damage‐induced activation of p53 by the checkpoint kinase Chk2. Science 287, 1824–1827. PubMed

Jackson SP and Bartek J (2009) The DNA‐damage response in human biology and disease. Nature 461, 1071–1078. PubMed PMC

Toledo LI, Murga M and Fernandez‐Capetillo O (2011a) Targeting ATR and Chk1 kinases for cancer treatment: a new model for new (and old) drugs. Mol Oncol 5, 368–373. PubMed PMC

Cuadrano M, Martinez‐Pastor B, Murga M, Toledo IL, Gutierrez‐Martinez P, Lopez E and Fernandez‐Capetillo O (2006) ATM regulates ATR chromatin loading in response to DNA double‐strand breaks. J Exp Med 203, 297–303. PubMed PMC

Jazayeri A, Falck J, Lukas C, Bartek J, Smith GC, Lukas J and Jackson SP (2006) ATM and cell cycle dependent regulation of ATR in response to DNA double‐strand breaks. Nat Cell Biol 8, 37–45. PubMed

Bartkova J, Rezaei N, Liontos M, Karakaidos P, Kletsas D, Issaeva N, Vassiliu LV, Kolettas E, Niforou K, Zoumpourlis VC et al (2006) Oncogene‐induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 444, 633–637. PubMed

Colado M and Serano M (2006) The power and the promise of oncogene‐induced senescence marker. Nat Rev Cancer 6, 472–476. PubMed

Di Micco R, Fumagalli M, Cicalese A, Piccinin S, Gasparini P, Luise C, Schurra C, Garre' M, Nuciforo PG, Bensimon A et al (2006) Oncogene‐induced senescence is a DNA damage response triggered by DNA hyper‐replication. Nature 444, 638–642. PubMed

Campisi J and d′Adda di Fagagna F (2007) Cellular senescence: when bad things happen to good cells. Nat Rev Mol Cell Biol 8, 729–740. PubMed

D′Adda di Fagagna F (2008) Living on a break: cellular senescence as a DNA‐damage response. Nat Rev Cancer 8, 512–522. PubMed

Kosar M, Bartkova J, Hubackova S, Hodny Z, Lukas J and Bartek J (2011) Senescence associated heterochromatin foci are dispensable for cellular senescence, occur in cell type‐ and insult‐dependent manner, and follow expression of p16ink4a . Cell Cycle 10, 457–468. PubMed

Lukasova E, Kovařík A, Bačíková A, Falk M and Kozubek S (2017) Loss of lamin B receptor is necessary to induce cellular senescence. Biochem J 474, 281–300. PubMed

Shimi T, Butin‐Israeli V, Adam SA, Hamanaka RB, Goldman AE, Lucas CA, Shumaker DKS, Chandel NS and Goldman RD (2011) The role of nuclear lamin B1 in cell proliferation and senescence. Genes Dev 25, 2579–2593. PubMed PMC

Freund A, Laberge RM, Demaria M and Campisi J (2012) Lamin B1 loss is a senescence‐associated biomarker. Mol Biol Cell 23, 2066–2074. PubMed PMC

Sadaie M, Salama R, Carroll T, Tomimatsu K, Chandra T, Young AR, Narita M, Pérez‐Mancera PA, Bennett DC, Chong H et al (2013) Redistribution of the lamin B1 genomic binding profile affects rearrangement of heterochromatic domains and SAHF formation during senescence. Genes Dev 27, 1800–1808. PubMed PMC

Chandra T, Ewels PA, Schoenfelder S, Furlan‐Magaril M, Wingett SW, Kirschner K, Thuret JY, Andrews S, Fraser P and Reik W (2015) Global reorganization of the nuclear landscape in senescent cells. Cell Rep 10, 471–483. PubMed PMC

Shah PP, Donahue G, Otte GL, Capell BC, Nelson DM, Cao K, Aggarwala V, Cruickshanks HA, Rai TS, McBryan T et al (2013) Lamin B1 depletion in senescent cells triggers large‐scale changes in gene expression and the chromatin landscape. Genes Dev 27, 1787–1799. PubMed PMC

Rai KR, Peterson BL, Appelbaum FR, Kolitz J, Elias L, Shepherd L, Hines J, Threatte GA, Larson RA, Cheson BD et al (2000) Fludarabine compared with chlorambucil as primary therapy for chronic lymphocytic leukemia. N Engl J Med 343, 1750–1757. PubMed

Dwyer MP, Keertikar K, Paruch K, Alvarez C, Labroli M, Poker C, Fischmann TO, Mayer‐Ezell R, Bond R, Wang Y et al (2013) Discovery of pyrazolo[1,5‐a] pyrimidine‐based Pim inhibitors: a template based approach. Bioorg Med Chem Lett 23, 6178–6182. PubMed

Labroli M, Paruch K, Dwyer MP, Alvarez C, Keertikar K, Poker C, Rossman R, Duca JS, Fischmann TO, Madison V et al (2011) Discovery of pyrazolo [1,5a]pyrimidine based Chk1 inhibitors: a template‐based approach‐part 2. Bioorg Med Chem Lett 21, 471–474. PubMed

Reaper PM, Griffiths MR, Long JM, Charrier JD, Maccormick S, Charlton PA, Golec JM and Pollard JR (2011) Selective killing of ATM‐ or p53‐deficient cancer cells through inhibition of ATR. Nat Chem Biol 13, 428–430. PubMed

Toledo IL, Murga M, Zur R, Soria R, Rodriguez A, Martinez S, Oyarzabal J, Pastor J, Bischoff JR and Fernandez‐Capetillo O (2011) A cell‐based screen identifies ATR inhibitors with synthetic lethal properties for cancer associated mutations. Nat Struct Mol Biol 18, 721–727. PubMed PMC

Malcikova J, Stano‐Kozubík K, Tichy B, Kantorova B, Pavlova S, Tom N, Radova L, Smardova J, Pardy D, Doubek M et al (2015) Detailed analysis of therapy‐driven clonal evolution of TP53 mutations in chronic lymphocytic leukemia. Leukemia 29, 877–885. PubMed PMC

Matula PA, Danek O, Maska M, Vinkler M and Kozubek M (2009) Acquiarium: free software for acquisition and analysis of 3D images of cells in fluorescence microscopy In IEEE International Symposium on Biomedical Imaging. pp. 1138–1141. IEEE, Boston, MA. ISBN 978‐1‐4244‐3932‐4.

Dimri GP, Lee X, Basile G, Acosta M, Scott G, Roskelley C, Medrano EE, Linskens M, Rubelj I, Pereira‐Smith O et al (1995) A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci USA 92, 9363–9367. PubMed PMC

Singh M, Hunt CR, Pandita RK, Kumar R, Yang C‐R, Horokoshi N, Bachoo R, Serag S, Story MD, Shay JW et al (2013) Lamin A/C depletion enhances DNA damage‐induced stalled replication fork arrest. Mol Cell Biol 33, 1210–1222. PubMed PMC

Gagou ME, Zuazua‐Villar P and Meuth M (2010) Enhanced H2AX phosphorylation, DNA replication fork arrest, and cell death in the absence of Chk1. Mol Biol Cell 21, 739–752. PubMed PMC

Guzi T, Paruch K, Dwyer MP, Labroli M, Shanahan F, Davis N, Taricani L, Wisswell D, Seghezzi W, Penaflor E et al (2011) Targeting the replication checkpoint using SCH900776, a potent and functionally selective Chk1 inhibitor identified via high content screening. Mol Cancer Ther 10, 591–602. PubMed

Xiao Y, Ramiscal J, Kowanetz K, Del Nagro C, Malek S, Evangelista M, Blackwood E, Jackson PK and O′Brien T (2013) Identification of preferred chemotherapeutics for combining with a Chk1 inhibitor. Mol Cancer Ther 12, 2285–2295. PubMed

Qian Y and Chen X (2010) Tumor suppression by p53: making cells senescent. Histol Histopathol 25, 515–526. PubMed PMC

Guelen L, Pagie l, Brasset E, Meuleman W, Faza MB, Talhout W, Eussen BH, de Klein A, Wessels L, de Laat W et al (2008) Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions in single human cells. Nature 453, 948–951. PubMed

Andrés V and González JM (2009) Role of A‐type lamins in signaling, transcription, and chromatin organization. J Cell Biol 187, 945–957. PubMed PMC

Solovei I, Wang AS, Thanisch K, Schmidt CS, Krebs S, Zwerger M, Cohen TV, Devys D, Foisner R, Peichl L et al (2013) LBR and lamin A/C sequentially tether peripheral heterochromatin and inversely regulate differentiation. Cell 152, 584–598. PubMed

Schreiber KH and Kennedy BK (2013) When lamins go bad: nuclear structure and disease. Cell 152, 1365–1372. PubMed PMC

Zemanova J, Hylse O, Collakova J, Vesely P, Oltova A, Borsky M, Zaprazna K, Kasparkova M, Janovska P, Verner J et al (2016) Chk1 inhibition significantly potentiates activity of nucleoside analogs in TP53‐mutated B‐lymphoid cells. Oncotarget 7, 62091–62106. PubMed PMC

Vitale I, Galluzzi L, Castedo M and Kroemer G (2011) Mitotic catastrophe: a mechanism for avoiding genomic instability. Nat Rev Mol Cell Biol 12, 385–392. PubMed

Fragkos M and Naim V (2017) Rescue from replication stress during mitosis. Cell Cycle 16, 613–633. PubMed PMC

Wang Q, Fan S, Eastman A, Worland PJ, Seussville EA and O′Connor PM (1996) UCN‐01: a potent abrogator of G2 checkpoint function in cancer cells with disrupted p53. J Natl Cancer Inst 88, 956–965. PubMed

Toledo IL, Altmeyer M, Rask MM, Lukas C, Larsen DH, Povlsen LK, Bekker‐Jensen S, Mailand N, Bartek J and Lukas J (2013) ATR prohibits replication catastrophe preventing global exhaustion of RPA. Cell 15, 1088–1103. PubMed

Toledo LI, Neelsen KJ and Lukas J (2017) Replication catastrophe: when a checkpoint fails because of exhaustion. Mol Cell 66, 735–749. PubMed

Buisson R, Boisvert JL, Benes CH and Zou L (2015) Distinct but concerted roles of ATR, DNA‐PK, and Chk1 in countering replication stress during S phase. Mol Cell 59, 1011–1024. PubMed PMC

Nikolov I and Tadei A (2015) Linking replication stress with heterochromatin formation. Chromosoma 125, 523–533. PubMed PMC

Tittel‐Elmer M, Lengronne A, Davidson MB, Bacal J, Francois P, Hohl M, Petrini JH, Pasero P and Cobb JA (2012) Cohesin association to replication sits depends on rad50 and promotes fork restart. Mol Cell 48, 98–108. PubMed PMC

Wu CS, Chen YF and Gartenberg MR (2011) Targeted sister chromatid cohesin by Sir2. PLoS Genet 7, e10020000. PubMed PMC

Rogakou EP, Pilch DR, Orr AH, Ivanova VS and Bohner WM (1998) DNA double‐strand breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273, 5858–5868. PubMed

Kar A, Jones N, Arat NO, Fishel R and Griffith JD (2018) Long repeating (TTAGGG)n single stranded DNA self‐condenses into compact beaded filaments stabilized by G‐quadruplex formation. J Biol Chem 293, 9473–9485. PubMed PMC

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