The response to DNA damage during differentiation: Pathways and consequences
Abstract
Damage to genomic DNA triggers a prompt set of signaling events known as the DNA damage response (DDR) which coordinates DNA repair, cell cycle arrest and ultimately cell death or senescence. Although activation of adequate DNA damage signaling and repair systems depends on the type of lesion and the cell-cycle phase in which it occurs, emerging evidence indicates that DNA repair and DDR function differently in different cellular contexts. Depending on the time maintenance and function of a specific cell type the risk of accumulating DNA damage may vary. For instance, damage to stem cells if not repaired can lead to mutation amplification or propagation through the processes of self-renewal and differentiation, respectively, whereas damage to post-mitotic cells can affect mostly tissue homeostasis. Stem cells are therefore expected to address DNA damage differently from their somatic counterparts. In this review the information available on the common and distinct mechanisms of control of genome integrity utilized by different cell types along the self-renewal/differentiation program will be reviewed, with special emphasis on their roles in the prevention of aging and disease.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
DDR pathways that safeguard genomic integrity may show reduced activity in stem cells with age.
“These observations suggest that DDR pathways, evolved to safeguard genomic integrity and maximize survival of the organism13,44–46, may show reduced activity in stem cells with age.”
From Stem cell aging: mechanisms, regulators and therapeutic opportunities (2014) · cites this paper as [45]
Cites
1 retracted
Wenz, T., Rossi, S. G., Rotundo, R. L., Spiegelman, B. M., & Moraes, C. T. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0911570106 · Cited by 600 · see citing works
RetractedLong non-coding RNAs: insights into functions
Mercer, T. R., Dinger, M. E., & Mattick, J. S. (2009) · Nature Reviews Genetics · doi:10.1038/nrg2521 · Cited by 5,654 · see citing works
The DNA Damage Response: Making It Safe to Play with Knives
Ciccia, A., & Elledge, S. J. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.09.019 · Cited by 4,368 · see citing works
Regulation mechanisms and signaling pathways of autophagy
He, C., & Klionsky, D. J. (2009) · Annual Review of Genetics · doi:10.1146/annurev-genet-102808-114910 · Cited by 3,609 · see citing works
The DNA damage response: putting checkpoints in perspective
Zhou, B.-B. S., & Elledge, S. J. (2000) · Nature · doi:10.1038/35044005 · Cited by 3,213 · see citing works
A Long Noncoding RNA Controls Muscle Differentiation by Functioning as a Competing Endogenous RNA
Cesana, M., Cacchiarelli, D., Legnini, I., Santini, T., Sthandier, O., Chinappi, M., Tramontano, A., & Bozzoni, I. (2011) · Cell · doi:10.1016/j.cell.2011.09.028 · Cited by 2,554 · see citing works
Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-γ
Picard, F., Kurtev, M. V., Chung, N., Topark‐Ngarm, A., Senawong, T., de Oliveira, R. M., Leid, M. E., McBurney, M. W., & Guarente, L. (2004) · Nature · doi:10.1038/nature02583 · Cited by 1,943 · see citing works
The pathways of mitophagy for quality control and clearance of mitochondria
Ashrafi, G., & Schwarz, T. L. (2013) · Cell Death & Differentiation · doi:10.1038/cdd.2012.81 · Cited by 1,900 · see citing works
Autophagy in mammalian development and differentiation
Mizushima, N., & Levine, B. (2010) · Nature Cell Biology · doi:10.1038/ncb0910-823 · Cited by 1,555 · see citing works
The multifaceted mismatch-repair system
Jiricny, J. (2006) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1907 · Cited by 1,375 · see citing works
Reactive oxygen species act through p38 MAPK to limit the lifespan of hematopoietic stem cells
Ito, K., Hirao, A., Arai, F., Takubo, K., Matsuoka, S., Miyamoto, K., Ohmura, M., Naka, K., Hosokawa, K., Ikeda, Y., et al. (2006) · Nature Medicine · doi:10.1038/nm1388 · Cited by 1,362 · see citing works
Essential role for Nix in autophagic maturation of erythroid cells
Sandoval, H., Thiagarajan, P., Dasgupta, S. K., Schumacher, A., Prchal, J. T., Chen, M., & Wang, J. (2008) · Nature · doi:10.1038/nature07006 · Cited by 1,185 · see citing works
Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells
Ito, K., Hirao, A., Arai, F., Matsuoka, S., Takubo, K., Hamaguchi, I., Nomiyama, K., Hosokawa, K., Sakurada, K., Nakagata, N., et al. (2004) · Nature · doi:10.1038/nature02989 · Cited by 1,175 · see citing works
Deficiencies in DNA damage repair limit the function of haematopoietic stem cells with age
Rossi, D. J., Bryder, D., Seita, J., Nussenzweig, A., Hoeijmakers, J., & Weissman, I. L. (2007) · Nature · doi:10.1038/nature05862 · Cited by 1,115 · see citing works
Mitophagy: mechanisms, pathophysiological roles, and analysis
Ding, W.-X., & Yin, X.-M. (2012) · bchm · doi:10.1515/hsz-2012-0119 · Cited by 1,032 · see citing works
Sandri, M., Lin, J., Handschin, C., Yang, W., Arany, Z. P., Lecker, S. H., Goldberg, A. L., & Spiegelman, B. M. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0607795103 · Cited by 974 · see citing works
p53 induces differentiation of mouse embryonic stem cells by suppressing Nanog expression
Lin, T., Chao, C., Saito, S., Mazur, S. J., Murphy, M. E., Appella, E., & Xu, Y. (2004) · Nature Cell Biology · doi:10.1038/ncb1211 · Cited by 859 · see citing works
p53 and Pten control neural and glioma stem/progenitor cell renewal and differentiation
Zheng, H., Ying, H., Yan, H., Kimmelman, A. C., Hiller, D. J., Chen, A.-J., Perry, S. R., Tonon, G., Chu, G. C., Ding, Z., et al. (2008) · Nature · doi:10.1038/nature07443 · Cited by 767 · see citing works
Autophagy regulates adipose mass and differentiation in mice
Singh, R., Xiang, Y., Wang, Y., Baikati, K., Cuervo, A. M., Luu, Y. K., Tang, Y., Pessin, J. E., Schwartz, G. J., & Czaja, M. J. (2009) · Journal of Clinical Investigation · doi:10.1172/jci39228 · Cited by 748 · see citing works
Chen, C., Liu, Y., Liu, R., Ikenoue, T., Guan, K.-L., Liu, Y., & Zheng, P. (2008) · The Journal of Experimental Medicine · doi:10.1084/jem.20081297 · Cited by 682 · see citing works
The autophagy protein Atg7 is essential for hematopoietic stem cell maintenance
Mortensen, M., Soilleux, E. J., Djordjevic, G., Tripp, R., Lutteropp, M., Sadighi-Akha, E., Stranks, A. J., Glanville, J., Knight, S., W. Jacobsen, S.-E., et al. (2011) · Journal of Experimental Medicine · doi:10.1084/jem.20101145 · Cited by 657 · see citing works
Robertson, A. B., Klungland, A., Rognes, T., & Leiros, I. (2009) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-009-8736-z · Cited by 652 · see citing works
Bentzinger, C. F., Romanino, K., Cloëtta, D., Lin, S., Mascarenhas, J. B., Oliveri, F., Xia, J., Casanova, E., Costa, C. F., Brink, M., et al. (2008) · Cell Metabolism · doi:10.1016/j.cmet.2008.10.002 · Cited by 640 · see citing works
Zhang, Y., Goldman, S., Baerga, R., Zhao, Y., Komatsu, M., & Jin, S. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0906048106 · Cited by 634 · see citing works
Hematopoietic Stem Cell Quiescence Promotes Error-Prone DNA Repair and Mutagenesis
Mohrin, M., Bourke, E., Alexander, D., Warr, M. R., Barry-Holson, K., Le Beau, M. M., Morrison, C. G., & Passegué, E. (2010) · Cell Stem Cell · doi:10.1016/j.stem.2010.06.014 · Cited by 599 · see citing works
Sir2 Regulates Skeletal Muscle Differentiation as a Potential Sensor of the Redox State
Fulco, M., Schiltz, R. L., Iezzi, S., King, M. T., Zhao, P., Kashiwaya, Y., Hoffman, E. P., Veech, R. L., & Sartorelli, V. (2003) · Molecular Cell · doi:10.1016/s1097-2765(03)00226-0 · Cited by 590 · see citing works
Hwang, B. J., Ford, J. M., Hanawalt, P. C., & Chu, G. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.2.424 · Cited by 581 · see citing works
Kundu, M., Lindsten, T., Yang, C.-Y., Wu, J., Zhao, F., Zhang, J., Selak, M. A., Ney, P. A., & Thompson, C. B. (2008) · Blood · doi:10.1182/blood-2008-02-137398 · Cited by 571 · see citing works
ATM and Artemis promote homologous recombination of radiation‐induced DNA double‐strand breaks in G2
Beucher, A., Birraux, J., Tchouandong, L., Barton, O., Shibata, A., Conrad, S., Goodarzi, A. A., Krempler, A., Jeggo, P. A., & Löbrich, M. (2009) · The EMBO Journal · doi:10.1038/emboj.2009.276 · Cited by 548 · see citing works
Site-specific DICER and DROSHA RNA products control the DNA-damage response
Francia, S., Michelini, F., Saxena, A., Tang, D. T. P., de Hoon, M., Anelli, V., Mione, M., Carninci, P., & di Fagagna, F. D. (2012) · Nature · doi:10.1038/nature11179 · Cited by 533 · see citing works
DNA repair is limiting for haematopoietic stem cells during ageing
Nijnik, A., Woodbine, L., Marchetti, C., Dawson, S., Lambe, T., Liu, C., Rodrigues, N. P., Crockford, T. L., Cabuy, E., Vindigni, A., et al. (2007) · Nature · doi:10.1038/nature05875 · Cited by 518 · see citing works
Self‐renewal of human embryonic stem cells is supported by a shortened G1 cell cycle phase
Becker, K. A., Ghule, P. N., Therrien, J. A., Lian, J. B., Stein, J. L., van Wijnen, A. J., & Stein, G. S. (2006) · Journal of Cellular Physiology · doi:10.1002/jcp.20776 · Cited by 460 · see citing works
Wilson-Fritch, L., Burkart, A., Bell, G., Mendelson, K., Leszyk, J., Nicoloro, S., Czech, M., & Corvera, S. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.3.1085-1094.2003 · Cited by 459 · see citing works
Aladjem, M. I., Spike, B. T., Rodewald, L. W., Hope, T. J., Klemm, M., Jaenisch, R., & Wahl, G. M. (1998) · Current Biology · doi:10.1016/s0960-9822(98)70061-2 · Cited by 442 · see citing works
HDACs link the DNA damage response, processing of double-strand breaks and autophagy
Robert, T., Vanoli, F., Chiolo, I., Shubassi, G., Bernstein, K. A., Rothstein, R. J., Botrugno, O. A., Parazzoli, D., Oldani, A., Minucci, S., et al. (2011) · Nature · doi:10.1038/nature09803 · Cited by 412 · see citing works
Mitochondria removal by autophagy
Wang, K., & Klionsky, D. J. (2011) · Autophagy · doi:10.4161/auto.7.3.14502 · Cited by 407 · see citing works
Moving toward System Genetics through Multiple Trait Analysis in Genome-Wide Association Studies
Shriner, D. (2012) · Frontiers in Genetics · doi:10.3389/fgene.2012.00001 · Cited by 390 · see citing works
Mortensen, M., Ferguson, D. J. P., Edelmann, M. J., Kessler, B. M., Morten, K., Komatsu, M., & Simon, A. K. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0913170107 · Cited by 388 · see citing works
Cell Cycle Activation Linked to Neuronal Cell Death Initiated by DNA Damage
Kruman, I. I., Wersto, R. P., Cardozo‐Pelaez, F., Smilenov, L. B., Chan, S. L., Chrest, F. J., Emokpae, R., Gorospe, M., & Mattson, M. P. (2004) · Neuron · doi:10.1016/s0896-6273(04)00017-0 · Cited by 365 · see citing works
Mitochondrial dysfunction in ataxia-telangiectasia
Valentin-Vega, Y. A., MacLean, K. H., Tait-Mulder, J., Milasta, S., Steeves, M., Dorsey, F. C., Cleveland, J. L., Green, D. R., & Kastan, M. B. (2012) · Blood · doi:10.1182/blood-2011-08-373639 · Cited by 365 · see citing works
A role for p53 in base excision repair
Zhou, J., Ahn, J., Wilson, S. H., & Prives, C. (2001) · The EMBO Journal · doi:10.1093/emboj/20.4.914 · Cited by 333 · see citing works
DNA Repair in Mammalian Cells: Nucleotide excision repair: variations on versatility
Nouspikel, T. (2009) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-009-8737-y · Cited by 330 · see citing works
Embryonic stem cells and somatic cells differ in mutation frequency and type
Cervantes, R. B., Stringer, J. R., Shao, C., Tischfield, J. A., & Stambrook, P. J. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.062527199 · Cited by 317 · see citing works
Baerga, R., Zhang, Y., Chen, P.-H., Goldman, S., & Jin, S. V. (2009) · Autophagy · doi:10.4161/auto.5.8.9991 · Cited by 304 · see citing works
Histone deacetylase SIRT1 modulates neuronal differentiation by its nuclear translocation
Hisahara, S., Chiba, S., Matsumoto, H., Tanno, M., Yagi, H., Shimohama, S., Sato, M., & Horio, Y. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0800612105 · Cited by 281 · see citing works
Milyavsky, M., Gan, O. I., Trottier, M., Komosa, M., Tabach, O., Notta, F., Lechman, E. R., Hermans, K. G., Eppert, K., Konovalova, Z., et al. (2010) · Cell stem cell · doi:10.1016/j.stem.2010.05.016 · Cited by 280 · see citing works
Hong, Y., & Stambrook, P. J. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0401346101 · Cited by 248 · see citing works
Sotiropoulou, P. A., Candi, A., Mascré, G., Clercq, S. D., Youssef, K. K., Lapouge, G., Dahl, E., Semeraro, C., Denecker, G., Marine, J., et al. (2010) · Nature Cell Biology · doi:10.1038/ncb2059 · Cited by 245 · see citing works
Zhang, J., Randall, M. S., Loyd, M. R., Dorsey, F. C., Kundu, M., Cleveland, J. L., & Ney, P. A. (2009) · Blood · doi:10.1182/blood-2008-04-151639 · Cited by 231 · see citing works
Human Embryonic Stem Cells Have Enhanced Repair of Multiple Forms of DNA Damage
Maynard, S., Swistowska, A. M., Lee, J. W., Liu, Y., Liu, S.-T., Da Cruz, A. B., Rao, M., de Souza-Pinto, N. C., Zeng, X., & Bohr, V. A. (2008) · Stem Cells · doi:10.1634/stemcells.2007-1041 · Cited by 220 · see citing works
Cancer predisposition and hematopoietic failure in <i> Rad50 <sup>S/S</sup> </i> mice
Bender, C. F., Sikes, M. L., Sullivan, R., Huye, L. E., Le Beau, M. M., Roth, D. B., Mirzoeva, O. K., Oltz, E. M., & Petrini, J. H. J. (2002) · Genes & Development · doi:10.1101/gad.1007902 · Cited by 213 · see citing works
Scheibye‐Knudsen, M., Ramamoorthy, M., Sýkora, P., Maynard, S., Lin, P., Minor, R. K., Wilson, D. M., Cooper, M. P., Spencer, R. G. S., de Cabo, R., et al. (2012) · The Journal of Experimental Medicine · doi:10.1084/jem.20111721 · Cited by 203 · see citing works
Autophagy for tissue homeostasis and neuroprotection
Mariño, G., Madeo, F., & Kroemer, G. (2011) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2010.10.001 · Cited by 195 · see citing works
Orii, K. E., Lee, Y., Kondo, N., & McKinnon, P. J. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0602436103 · Cited by 181 · see citing works
DNA Damage Responses in Human Induced Pluripotent Stem Cells and Embryonic Stem Cells
Momčilović, O., Knobloch, L., Fornsaglio, J. L., Varum, S., Easley, C. A., & Schatten, G. P. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013410 · Cited by 174 · see citing works
Atg7 Induces Basal Autophagy and Rescues Autophagic Deficiency in CryAB R120G Cardiomyocytes
Pattison, J. S., Osińska, H. E., & Robbins, J. M. (2011) · Circulation Research · doi:10.1161/circresaha.110.237339 · Cited by 172 · see citing works
Atg5 and Ambra1 differentially modulate neurogenesis in neural stem cells
Vázquez, P., Arroba, A. I., Cecconi, F., de la Rosa, E. J., Boya, P., & De Pablo, F. (2012) · Autophagy · doi:10.4161/auto.8.2.18535 · Cited by 171 · see citing works
Bai, L., Pang, W.-J., Yang, Y., & Yang, G.-S. (2007) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-007-9592-5 · Cited by 158 · see citing works
Tichy, E. D., Pillai, R., Deng, L., Liang, L., Tischfield, J., Schwemberger, S. J., Babcock, G. F., & Stambrook, P. J. (2010) · Stem Cells and Development · doi:10.1089/scd.2010.0058 · Cited by 152 · see citing works
The role of DNA damage repair in aging of adult stem cells
Kenyon, J. D., & Gerson, S. L. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm1064 · Cited by 152 · see citing works
DNA double-strand breaks activate a multi-functional genetic program in developing lymphocytes
Bredemeyer, A. L., Helmink, B. A., Innes, C. L., Calderón, B., McGinnis, L. M., Mahowald, G. K., Gapud, E. J., Walker, L. M., Collins, J. B., Weaver, B. K., et al. (2008) · Nature · doi:10.1038/nature07392 · Cited by 147 · see citing works
DNA repair in murine embryonic stem cells and differentiated cells
Tichy, E. D., & Stambrook, P. J. (2008) · Experimental Cell Research · doi:10.1016/j.yexcr.2008.02.007 · Cited by 143 · see citing works
Momčilović, O., Choi, S., Varum, S., Bakkenist, C. J., Schatten, G. P., & Navara, C. S. (2009) · Stem Cells · doi:10.1002/stem.123 · Cited by 142 · see citing works
Reduced hematopoietic reserves in DNA interstrand crosslink repair‐deficient Ercc1−/− mice
Prasher, J. M., Lalai, A. S., Heijmans‐Antonissen, C., Ploemacher, R., Hoeijmakers, J. H. J., Touw, I. P., & Niedernhofer, L. J. (2005) · The EMBO Journal · doi:10.1038/sj.emboj.7600542 · Cited by 135 · see citing works
SIRT1 Promotes Differentiation of Normal Human Keratinocytes
Blander, G., Bhimavarapu, A., Mammone, T., Maes, D. H., Elliston, K. O., Reich, C., Matsui, M. S., Guarente, L., & Loureiro, J. (2008) · Journal of Investigative Dermatology · doi:10.1038/jid.2008.179 · Cited by 128 · see citing works
Narciso, L., Fortini, P., Pajalunga, D., Franchitto, A., Liu, P., Degan, P., Fréchet, M., Demple, B., Crescenzi, M., & Eugenia Dogliotti, Y. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0701743104 · Cited by 117 · see citing works
Self-citationA myogenic differentiation checkpoint activated by genotoxic stress
Puri, P., Bhakta, K. S., Wood, L. D., Costanzo, A., Zhu, J., & Wang, J. Y. J. (2002) · Nature Genetics · doi:10.1038/ng1023 · Cited by 117 · see citing works
The genesis of cerebellar interneurons and the prevention of neural DNA damage require XRCC1
Lee, Y., Katyal, S., Li, Y., El‐Khamisy, S. F., Russell, H. R., Caldecott, K. W., & McKinnon, P. J. (2009) · Nature Neuroscience · doi:10.1038/nn.2375 · Cited by 114 · see citing works
Adams, B. R., Golding, S. E., Rao, R. R., & Valerie, K. C. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010001 · Cited by 113 · see citing works
Zaky, A., Busso, C., Izumi, T., Chattopadhyay, R., Bassiouny, A., Mitra, S., & Bhakat, K. K. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkm1173 · Cited by 111 · see citing works
DNA repair in differentiated cells: Some new answers to old questions
Nouspikel, T. P. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.07.006 · Cited by 107 · see citing works
At Loose Ends: Resecting a Double-Strand Break
Bernstein, K. A., & Rothstein, R. J. (2009) · Cell · doi:10.1016/j.cell.2009.05.007 · Cited by 103 · see citing works
Sloun, P. P. H. V., Jansen, J. G., Weeda, G., Mullenders, L. H. F., van Zeeland, A. A., Lohman, P. H. M., & Vrieling, H. (1999) · Nucleic Acids Research · doi:10.1093/nar/27.16.3276 · Cited by 93 · see citing works
Repopulating defect of mismatch repair–deficient hematopoietic stem cells
Reese, J., Liu, L., & Gerson, S. L. (2003) · Blood · doi:10.1182/blood-2002-10-3035 · Cited by 89 · see citing works
Autophagy in human keratinocytes: an early step of the differentiation?
Aymard, E., Barruche, V., Naves, T., Bordes, S., Closs, B., Verdier, M., & Ratinaud, M. (2010) · Experimental Dermatology · doi:10.1111/j.1600-0625.2010.01157.x · Cited by 86 · see citing works
Sherman, M. H., Kuraishy, A. I., Deshpande, C., Hong, J. S., Cacalano, N. A., Gatti, R. A., Manis, J. P., Damore, M. A., Pellegrini, M. A., & Teitell, M. A. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.08.019 · Cited by 84 · see citing works
Groth, P., Orta, M. L., Elvers, I., Majumder, M. M., Lagerqvist, A., & Helleday, T. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks315 · Cited by 75 · see citing works
Biton, S., Dar, I., Mittelman, L. A., Pereg, Y., Barzilai, A., & Shiloh, Y. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m601895200 · Cited by 74 · see citing works
Schneider, L. X., Fumagalli, M., & di Fagagna, F. D. (2011) · Cell Death and Differentiation · doi:10.1038/cdd.2011.129 · Cited by 69 · see citing works
Differentiation-Induced Radioresistance in Muscle Cells
Latella, L., Lukas, J., Simone, C., Puri, P., & Bártek, J. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.14.6350-6361.2004 · Cited by 69 · see citing works
Maintenance of genomic integrity in hematopoietic stem cells
Naka, K., & Hirao, A. (2011) · International Journal of Hematology · doi:10.1007/s12185-011-0793-z · Cited by 64 · see citing works
DEWAARD, H., Sonneveld, E., DEWIT, J., LANGE, R., Hoeijmakers, J. H. J., Vrieling, H., & van der Horst, G. T. J. (2008) · DNA repair · doi:10.1016/j.dnarep.2008.06.009 · Cited by 63 · see citing works
ATM-independent, high-fidelity nonhomologous end joining predominates in human embryonic stem cells
Adams, B. R., Hawkins, A. J., Povirk, L. F., & Valerie, K. C. (2010) · Aging · doi:10.18632/aging.100197 · Cited by 60 · see citing works
The Chk1/Cdc25A Pathway as Activators of the Cell Cycle in Neuronal Death Induced by Camptothecin
Zhang, Y. Q., Qu, D., Morris, E. J., O’Hare, M. J., Callaghan, S. M., Slack, R. S., Geller, H. M., & Park, D. S. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2593-06.2006 · Cited by 59 · see citing works
Tomashevski, A., Webster, D. R., Grammas, P., Gorospe, M., & Kruman, I. I. (2010) · Cell Death and Differentiation · doi:10.1038/cdd.2009.221 · Cited by 57 · see citing works
Briegert, M., & Kaina, B. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-3712 · Cited by 53 · see citing works
Meulle, A., Salles, B., Daviaud, D., Valet, P., & Muller, C. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003345 · Cited by 52 · see citing works
Mouse models of DNA double-strand break repair and neurological disease
Frappart, P., & McKinnon, P. J. (2008) · DNA repair · doi:10.1016/j.dnarep.2008.03.007 · Cited by 52 · see citing works
Green, M. H. L., Waugh, A. P. W., Lowe, J. E., Harcourt, S. A., Cole, J., & Arlett, C. F. (1994) · Mutation Research/DNA Repair · doi:10.1016/0921-8777(94)90024-8 · Cited by 51 · see citing works
ATM-mediated response to DNA double strand breaks in human neurons derived from stem cells
Biton, S., Gropp, M., Itsykson, P., Pereg, Y., Mittelman, L. A., Johe, K. K., Reubinoff, B. E., & Shiloh, Y. (2006) · DNA repair · doi:10.1016/j.dnarep.2006.10.019 · Cited by 47 · see citing works
Acetylation: A Novel Link between Double-Strand Break Repair and Autophagy
Shubassi, G., Robert, T., Vanoli, F., Minucci, S., & Foiani, M. (2012) · Cancer Research · doi:10.1158/0008-5472.can-11-3172 · Cited by 44 · see citing works
Nouspikel, T., & Hanawalt, P. C. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0607769103 · Cited by 43 · see citing works
Fortini, P., Ferretti, C., Pascucci, B., Narciso, L., Pajalunga, D., Puggioni, E. M. R., Castino, R., Isidoro, C., Crescenzi, M., & Eugenia Dogliotti, Y. (2012) · Cell Death and Differentiation · doi:10.1038/cdd.2012.53 · Cited by 42 · see citing works
Self-citationSkeletal Muscle Differentiation Evokes Endogenous XIAP to Restrict the Apoptotic Pathway
Smith, M. I., Huang, Y. Y., & Deshmukh, M. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005097 · Cited by 42 · see citing works
Botrugno, O. A., Robert, T., Vanoli, F., et al. (2012) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-11-0767 · Cited by 40 · see citing works
Error-prone nonhomologous end joining repair operates in human pluripotent stem cells during late G2
Bogomazova, A. N., Lagarkova, M. A., Lv, T., Shutova, M. V., & Киселев, С. Л. (2011) · Aging · doi:10.18632/aging.100336 · Cited by 40 · see citing works
Mismatch and base excision repair proficiency in murine embryonic stem cells
Tichy, E. D., Liang, L., Deng, L., Tischfield, J. A., Schwemberger, S. J., Babcock, G. F., & Stambrook, P. J. (2011) · DNA repair · doi:10.1016/j.dnarep.2011.01.008 · Cited by 38 · see citing works
Bouças, J., Riabinska, A., Jokić, M., Herter-Sprie, G. S., Chen, S., Höpker, K., & Reinhardt, H. C. (2012) · Frontiers in Genetics · doi:10.3389/fgene.2012.00159 · Cited by 38 · see citing works
Essential postmitochondrial function of p53 uncovered in DNA damage-induced apoptosis in neurons
Vaughn, A. E., & Deshmukh, M. (2007) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4402084 · Cited by 37 · see citing works
XRCC1 protects against the lethality of induced oxidative DNA damage in nondividing neural cells
Kulkarni, A., McNeill, D. R., Gleichmann, M., Mattson, M. P., & Wilson, D. M. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn480 · Cited by 36 · see citing works
Nucleotide excision repair in differentiated cells
van der Wees, C. G. C., Jansen, J. G., Vrieling, H., van der Laarse, A., van Zeeland, A., & Mullenders, L. H. F. (2006) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2006.06.005 · Cited by 35 · see citing works
Tanida, I., Wakabayashi, M., Kanematsu, T., et al. (2006) · Autophagy · doi:10.4161/auto.2871 · Cited by 34 · see citing works
A putative role for cell cycle‐related proteins in microtubule‐based neuroplasticity
Schmetsdorf, S., Arnold, E., Holzer, M., Arendt, T., & Gärtner, U. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06661.x · Cited by 30 · see citing works
Photosensitivity syndrome brings to light a new transcription-coupled DNA repair cofactor
Cleaver, J. (2012) · Nature Genetics · doi:10.1038/ng.2255 · Cited by 26 · see citing works
Hyka‐Nouspikel, N., Lemonidis, K., Lu, W.-T., & Nouspikel, T. P. (2011) · Blood · doi:10.1182/blood-2010-12-326637 · Cited by 22 · see citing works
Mitophagy and Disease: New Avenues for Pharmacological Intervention
Taylor, R., & Goldman, S. J. (2011) · Current Pharmaceutical Design · doi:10.2174/138161211796904768 · Cited by 20 · see citing works
Nouspikel, T. (2009) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-009-8734-1 · Cited by 17 · see citing works
Simonatto, M., Giordani, L., Marullo, F., Minetti, G., Puri, P., & Latella, L. (2011) · Cell Cycle · doi:10.4161/cc.10.14.15948 · Cited by 13 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Stem cell aging: mechanisms, regulators and therapeutic opportunities
Oh, J., Lee, Y. D., & Wagers, A. J. (2014) · Nature Medicine · doi:10.1038/nm.3651 · Cited by 796 · see citing works
Maintaining genome stability in the nervous system
McKinnon, P. J. (2013) · Nature Neuroscience · doi:10.1038/nn.3537 · Cited by 229 · see citing works
- Authors
- Fortini, P., Ferretti, C., & Dogliotti, E.
- Affiliations
- Istituto Superiore di Sanità (IT)
- ORCID
- Fortini, Paola
- Venue
- Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis
- Publisher
- Elsevier BV
- Published
- 2013-03
- Volume
- 743-744
- Pages
- 160-168
- ISSN
- 0027-5107 (ISSN-L)
- 1386-1964
- OpenAlex
- W2006305985
- Cited by
- 45
- References
- 108
- Citations by year
- 2025: 1 · 2024: 4 · 2023: 5 · 2022: 2 · 2021: 2 · 2020: 2 · 2019: 4 · 2018: 4 · 2017: 3 · 2016: 5 · 2015: 8 · 2014: 4 · 2013: 1
- FWCI
- 0.56
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- Locations
- Mutation research. Fundamental and molecular mechanisms of mutagenesis (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Associazione Italiana per la Ricerca sul Cancro
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Keywords
- DNA damage response, DNA repair, cell differentiation, stem cells, self-renewal, genome stability, cell cycle arrest, cell death, senescence, mutation accumulation, tissue homeostasis, aging, postmitotic cells
- MeSH terms
- Animals, Cell Differentiation, DNA Damage, DNA Repair, Humans, Signal Transduction, Cell Death
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review