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Abstract:

The maintenance of genomic integrity is of main importance to the survival and health of organisms which are continuously exposed to genotoxic stress. Cells respond to DNA damage by activating survival pathways consisting of cell cycle checkpoints and repair mechanisms. However, the signal that triggers the DNA damage response is not necessarily a direct detection of the primary DNA lesion. In fact, chromatin defects may serve as initiating signals to activate those mechanisms. If the modulation of chromatin structure could initiate a checkpoint response in a direct manner, this supposes the existence of specific chromatin sensors. p19INK4d, a member of the INK4 cell cycle inhibitors, plays a crucial role in regulating genomic stability and cell viability by enhancing DNA repair. Its expression is induced in cells injured by one of several genotoxic treatments like cis-platin, UV light or neocarzinostatin. Nevertheless, when exogenous DNA damaged molecules are introduced into the cell, this induction is not observed. Here, we show that p19INK4d is enhanced after chromatin relaxation even in the absence of DNA damage. This induction was shown to depend upon ATM/ATR, Chk1/Chk2 and E2F activity, as is the case of p19INK4d induction by endogenous DNA damage. Interestingly, p19INK4d improves DNA repair when the genotoxic damage is caused in a relaxed-chromatin context. These results suggest that changes in chromatin structure, and not DNA damage itself, is the actual trigger of p19INK4d induction. We propose that, in addition to its role as a cell cycle inhibitor, p19INK4d could participate in a signaling network directed to detecting and eventually responding to chromatin anomalies. © 2013 Ogara et al.

Registro:

Documento: Artículo
Título:Chromatin Relaxation-Mediated Induction of p19INK4d Increases the Ability of Cells to Repair Damaged DNA
Autor:Ogara, M.F.; Sirkin, P.F.; Carcagno, A.L.; Marazita, M.C.; Sonzogni, S.V.; Ceruti, J.M.; Cánepa, E.T.
Filiación:Laboratorio de Biología Molecular, Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria Pabellón II, Buenos Aires, Argentina
Palabras clave:ATM protein; ATR protein; checkpoint kinase 1; checkpoint kinase 2; cyclin dependent kinase inhibitor 2D; transcription factor E2F; article; cell cycle regulation; cell function; chromatin; chromatin relaxation; chromatin structure; controlled study; DNA repair; enzyme activity; genotoxicity; human; human cell; protein induction; signal transduction; Cell Cycle Proteins; Cell Line; Chloroquine; Chromatin; Cyclin-Dependent Kinase Inhibitor p19; DNA Damage; DNA Repair; DNA-Binding Proteins; E2F1 Transcription Factor; Humans; Models, Biological; Mutagens; Protein Kinases; Protein-Serine-Threonine Kinases; Signal Transduction; Tumor Suppressor Proteins; Ultraviolet Rays
Año:2013
Volumen:8
Número:4
DOI: http://dx.doi.org/10.1371/journal.pone.0061143
Título revista:PLoS ONE
Título revista abreviado:PLoS ONE
ISSN:19326203
CAS:checkpoint kinase 2, 244634-79-5; ATR protein, human, 2.7.1.-; Cell Cycle Proteins; Checkpoint kinase 1, 2.7.11.1; Chloroquine, 54-05-7; Chromatin; Cyclin-Dependent Kinase Inhibitor p19; DNA-Binding Proteins; E2F1 Transcription Factor; E2F1 protein, human; Mutagens; Protein Kinases, 2.7.-; Protein-Serine-Threonine Kinases, 2.7.11.1; Tumor Suppressor Proteins; ataxia telangiectasia mutated protein, 2.7.11.1; checkpoint kinase 2, 2.7.1.11
PDF:https://bibliotecadigital.exactas.uba.ar/download/paper/paper_19326203_v8_n4_p_Ogara.pdf
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_19326203_v8_n4_p_Ogara

Referencias:

  • Groth, A., Rocha, W., Verreault, A., Almouzni, G., Chromatin challenges during DNA replication and repair (2007) Cell, 128, pp. 721-733
  • Loizou, J.I., Murr, R., Finkbeiner, M.G., Sawan, C., Wang, Z.Q., Epigenetic information in chromatin: the code of entry for DNA repair (2006) Cell Cycle, 5, pp. 696-701
  • Celeste, A., Fernandez-Capetillo, O., Kruhlak, M.J., Pilch, D.R., Staudt, D.W., Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks (2003) Nat Cell Biol, 5, pp. 675-679
  • Fernandez-Capetillo, O., Celeste, A., Nussenzweig, A., Focusing on foci: H2AX and the recruitment of DNA-damage response factors (2003) Cell Cycle, 2, pp. 426-427
  • Matsuoka, S., Ballif, B.A., Smogorzewska, A., McDonald 3rd, E.R., Hurov, K.E., ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage (2007) Science, 316, pp. 1160-1166
  • Bartek, J., Lukas, J., Chk1 and Chk2 kinases in checkpoint control and cancer (2003) Cancer Cell, 3, pp. 421-429
  • Kastan, M.B., Bartek, J., Cell-cycle checkpoints and cancer (2004) Nature, 432, pp. 316-323
  • Helleday, T., Petermann, E., Lundin, C., Hodgson, B., Sharma, R.A., DNA repair pathways as targets for cancer therapy (2008) Nat Rev Cancer, 8, pp. 193-204
  • Fernandez-Capetillo, O., Allis, C.D., Nussenzweig, A., Phosphorylation of histone H2B at DNA double-strand breaks (2004) J Exp Med, 199, pp. 1671-1677
  • Bilsland, E., Downs, J.A., Tails of histones in DNA double-strand break repair (2005) Mutagenesis, 20, pp. 153-163
  • Downs, J.A., Allard, S., Jobin-Robitaille, O., Javaheri, A., Auger, A., Binding of chromatin-modifying activities to phosphorylated histone H2A at DNA damage sites (2004) Mol Cell, 16, pp. 979-990
  • Shroff, R., Arbel-Eden, A., Pilch, D., Ira, G., Bonner, W.M., Distribution and dynamics of chromatin modification induced by a defined DNA double-strand break (2004) Curr Biol, 14, pp. 1703-1711
  • Rubbi, C.P., Milner, J., p53 is a chromatin accessibility factor for nucleotide excision repair of DNA damage (2003) Embo J, 22, pp. 975-986
  • Bakkenist, C.J., Kastan, M.B., DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation (2003) Nature, 421, pp. 499-506
  • Downs, J.A., Cote, J., Dynamics of chromatin during the repair of DNA double-strand breaks (2005) Cell Cycle, 4, pp. 1373-1376
  • Ortega, S., Malumbres, M., Barbacid, M., Cyclin D-dependent kinases, INK4 inhibitors and cancer (2002) Biochim Biophys Acta, 1602, pp. 73-87
  • Roussel, M.F., The INK4 family of cell cycle inhibitors in cancer (1999) Oncogene, 18, pp. 5311-5317
  • Canepa, E.T., Scassa, M.E., Ceruti, J.M., Marazita, M.C., Carcagno, A.L., INK4 proteins, a family of mammalian CDK inhibitors with novel biological functions (2007) IUBMB Life, 59, pp. 419-426
  • Ceruti, J.M., Scassa, M.E., Flo, J.M., Varone, C.L., Canepa, E.T., Induction of p19INK4d in response to ultraviolet light improves DNA repair and confers resistance to apoptosis in neuroblastoma cells (2005) Oncogene, 24, pp. 4065-4080
  • Scassa, M.E., Marazita, M.C., Ceruti, J.M., Carcagno, A.L., Sirkin, P.F., Cell cycle inhibitor, p19INK4d, promotes cell survival and decreases chromosomal aberrations after genotoxic insult due to enhanced DNA repair (2007) DNA Repair (Amst), 6, pp. 626-638
  • Ceruti, J.M., Scassa, M.E., Marazita, M.C., Carcagno, A.C., Sirkin, P.F., Transcriptional upregulation of p19INK4d upon diverse genotoxic stress is critical for optimal DNA damage response (2009) Int J Biochem Cell Biol, 41, pp. 1344-1353
  • Eller, M.S., Maeda, T., Magnoni, C., Atwal, D., Gilchrest, B.A., Enhancement of DNA repair in human skin cells by thymidine dinucleotides: evidence for a p53-mediated mammalian SOS response (1997) Proc Natl Acad Sci U S A, 94, pp. 12627-12632
  • Murr, R., Loizou, J.I., Yang, Y.G., Cuenin, C., Li, H., Histone acetylation by Trrap-Tip60 modulates loading of repair proteins and repair of DNA double-strand breaks (2006) Nat Cell Biol, 8, pp. 91-99
  • Kuo, L.J., Yang, L.X., Gamma-H2AX - a novel biomarker for DNA double-strand breaks (2008) In Vivo, 22, pp. 305-309
  • Avemann, K., Knippers, R., Koller, T., Sogo, J.M., Camptothecin, a specific inhibitor of type I DNA topoisomerase, induces DNA breakage at replication forks (1988) Mol Cell Biol, 8, pp. 3026-3034
  • Forget, A., Ayrault, O., den Besten, W., Kuo, M.L., Sherr, C.J., Differential post-transcriptional regulation of two Ink4 proteins, p18 Ink4c and p19 Ink4d (2008) Cell Cycle, 7, pp. 3737-3746
  • Kongruttanachok, N., Phuangphairoj, C., Thongnak, A., Ponyeam, W., Rattanatanyong, P., Replication independent DNA double-strand break retention may prevent genomic instability Mol Cancer, 9, p. 70
  • Lee, J.S., Activation of ATM-dependent DNA damage signal pathway by a histone deacetylase inhibitor, trichostatin A (2007) Cancer Res Treat, 39, pp. 125-130
  • Toth, K.F., Knoch, T.A., Wachsmuth, M., Frank-Stohr, M., Stohr, M., Trichostatin A-induced histone acetylation causes decondensation of interphase chromatin (2004) J Cell Sci, 117, pp. 4277-4287
  • Baure, J., Izadi, A., Suarez, V., Giedzinski, E., Cleaver, J.E., Histone H2AX phosphorylation in response to changes in chromatin structure induced by altered osmolarity (2009) Mutagenesis, 24, pp. 161-167
  • Hickson, I., Zhao, Y., Richardson, C.J., Green, S.J., Martin, N.M., Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM (2004) Cancer Res, 64, pp. 9152-9159
  • Sarkaria, J.N., Busby, E.C., Tibbetts, R.S., Roos, P., Taya, Y., Inhibition of ATM and ATR kinase activities by the radiosensitizing agent, caffeine (1999) Cancer Res, 59, pp. 4375-4382
  • Alderton, G.K., Joenje, H., Varon, R., Borglum, A.D., Jeggo, P.A., Seckel syndrome exhibits cellular features demonstrating defects in the ATR-signalling pathway (2004) Hum Mol Genet, 13, pp. 3127-3138
  • Yokota, T., Matsuzaki, Y., Miyazawa, K., Zindy, F., Roussel, M.F., Histone deacetylase inhibitors activate INK4d gene through Sp1 site in its promoter (2004) Oncogene, 23, pp. 5340-5349
  • Di Micco, R., Sulli, G., Dobreva, M., Liontos, M., Botrugno, O.A., Interplay between oncogene-induced DNA damage response and heterochromatin in senescence and cancer (2011) Nat Cell Biol, 13, pp. 292-302
  • Hunt, C.R., Pandita, R.K., Laszlo, A., Higashikubo, R., Agarwal, M., Hyperthermia activates a subset of ataxia-telangiectasia mutated effectors independent of DNA strand breaks and heat shock protein 70 status (2007) Cancer Res, 67, pp. 3010-3017
  • Fuse, T., Yamada, K., Asai, K., Kato, T., Nakanishi, M., Heat shock-mediated cell cycle arrest is accompanied by induction of p21 CKI (1996) Biochem Biophys Res Commun, 225, pp. 759-763
  • Weizman, N., Shiloh, Y., Barzilai, A., Contribution of the Atm protein to maintaining cellular homeostasis evidenced by continuous activation of the AP-1 pathway in Atm-deficient brains (2003) J Biol Chem, 278, pp. 6741-6747
  • Carcagno, A.L., Marazita, M.C., Ogara, M.F., Ceruti, J.M., Sonzogni, S.V., E2F1-mediated upregulation of p19INK4d determines its periodic expression during cell cycle and regulates cellular proliferation (2011) PLoS One, 6, pp. e21938
  • Foiani, M., Pellicioli, A., Lopes, M., Lucca, C., Ferrari, M., DNA damage checkpoints and DNA replication controls in Saccharomyces cerevisiae (2000) Mutat Res, 451, pp. 187-196
  • Koundrioukoff, S., Polo, S., Almouzni, G., Interplay between chromatin and cell cycle checkpoints in the context of ATR/ATM-dependent checkpoints (2004) DNA Repair (Amst), 3, pp. 969-978
  • Zhang, Y.W., Jones, T.L., Martin, S.E., Caplen, N.J., Pommier, Y., Implication of checkpoint kinase-dependent up-regulation of ribonucleotide reductase R2 in DNA damage response (2009) J Biol Chem, 284, pp. 18085-18095
  • Stevens, C., Smith, L., La Thangue, N.B., Chk2 activates E2F-1 in response to DNA damage (2003) Nat Cell Biol, 5, pp. 401-409
  • Lin, W.C., Lin, F.T., Nevins, J.R., Selective induction of E2F1 in response to DNA damage, mediated by ATM-dependent phosphorylation (2001) Genes Dev, 15, pp. 1833-1844
  • Stevens, C., La Thangue, N.B., The emerging role of E2F-1 in the DNA damage response and checkpoint control (2004) DNA Repair (Amst), 3, pp. 1071-1079
  • Niedernhofer, L.J., Garinis, G.A., Raams, A., Lalai, A.S., Robinson, A.R., A new progeroid syndrome reveals that genotoxic stress suppresses the somatotroph axis (2006) Nature, 444, pp. 1038-1043
  • Misri, S., Pandita, S., Pandita, T.K., Detecting ATM-dependent chromatin modification in DNA damage and heat shock response (2009) Methods Mol Biol, 523, pp. 395-410
  • Chomczynski, P., Sacchi, N., Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction (1987) Anal Biochem, 162, pp. 156-159
  • Loeken, M.R., Brady, J., The adenovirus EIIA enhancer. Analysis of regulatory sequences and changes in binding activity of ATF and EIIF following adenovirus infection (1989) J Biol Chem, 264, pp. 6572-6579
  • Varone, C.L., Giono, L.E., Ochoa, A., Zakin, M.M., Canepa, E.T., Transcriptional regulation of 5-aminolevulinate synthase by phenobarbital and cAMP-dependent protein kinase (1999) Arch Biochem Biophys, 372, pp. 261-270
  • You, Y.H., Lee, D.H., Yoon, J.H., Nakajima, S., Yasui, A., Cyclobutane pyrimidine dimers are responsible for the vast majority of mutations induced by UVB irradiation in mammalian cells (2001) The Journal of Biological Chemistry, 276, pp. 44688-44694
  • Koberle, B., Roginskaya, V., Wood, R.D., XPA protein as a limiting factor for nucleotide excision repair and UV sensitivity in human cells (2006) DNA Repair, 5, pp. 641-648

Citas:

---------- APA ----------
Ogara, M.F., Sirkin, P.F., Carcagno, A.L., Marazita, M.C., Sonzogni, S.V., Ceruti, J.M. & Cánepa, E.T. (2013) . Chromatin Relaxation-Mediated Induction of p19INK4d Increases the Ability of Cells to Repair Damaged DNA. PLoS ONE, 8(4).
http://dx.doi.org/10.1371/journal.pone.0061143
---------- CHICAGO ----------
Ogara, M.F., Sirkin, P.F., Carcagno, A.L., Marazita, M.C., Sonzogni, S.V., Ceruti, J.M., et al. "Chromatin Relaxation-Mediated Induction of p19INK4d Increases the Ability of Cells to Repair Damaged DNA" . PLoS ONE 8, no. 4 (2013).
http://dx.doi.org/10.1371/journal.pone.0061143
---------- MLA ----------
Ogara, M.F., Sirkin, P.F., Carcagno, A.L., Marazita, M.C., Sonzogni, S.V., Ceruti, J.M., et al. "Chromatin Relaxation-Mediated Induction of p19INK4d Increases the Ability of Cells to Repair Damaged DNA" . PLoS ONE, vol. 8, no. 4, 2013.
http://dx.doi.org/10.1371/journal.pone.0061143
---------- VANCOUVER ----------
Ogara, M.F., Sirkin, P.F., Carcagno, A.L., Marazita, M.C., Sonzogni, S.V., Ceruti, J.M., et al. Chromatin Relaxation-Mediated Induction of p19INK4d Increases the Ability of Cells to Repair Damaged DNA. PLoS ONE. 2013;8(4).
http://dx.doi.org/10.1371/journal.pone.0061143