This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Akkari, Y. M. N.
Right arrow Articles by Grompe, M.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Akkari, Y. M. N.
Right arrow Articles by Grompe, M.

 Previous Article  |  Next Article 

Molecular and Cellular Biology, November 2000, p. 8283-8289, Vol. 20, No. 21
0270-7306/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

DNA Replication Is Required To Elicit Cellular Responses to Psoralen-Induced DNA Interstrand Cross-Links

Yassmine M. N. Akkari,* Raynard L. Bateman, Carol A. Reifsteck, Susan B. Olson, and Markus Grompe

Department of Molecular and Medical Genetics, Oregon Health Sciences University, Portland, Oregon 97201

Received 24 November 1999/Returned for modification 7 February 2000/Accepted 21 July 2000

Following introduction of DNA interstrand cross-links (ICLs), mammalian cells display chromosome breakage or cell cycle delay with a 4N DNA content. To further understand the nature of the delay, previously described as a G2/M arrest, we developed a protocol to generate ICLs during specific intervals of the cell cycle. Synchronous populations of G1, S, and G2 cells were treated with photoactivated 4'-hydroxymethyl-4,5',8-trimethylpsoralen (HMT) and scored for normal passage into mitosis. In contrast to what was found for ionizing radiation, ICLs introduced during G2 did not result in a G2/M arrest, mitotic arrest, or chromosome breakage. Rather, subsequent passage through S phase was required to trigger both chromosome breakage and arrest in the next cell cycle. Similarly, ICLs introduced during G1 did not cause a G1/S arrest. We conclude that DNA replication is required to elicit the cellular responses of cell cycle arrest and genomic instability after psoralen-induced ICLs. In primary human fibroblasts, the 4N DNA content cell cycle arrest triggered by ICLs was long lasting but reversible. Kinetic analysis suggested that these cells could remove up to ~2,500 ICLs/genome at an average rate of 11 ICLs/genome/h.

* Corresponding author. Mailing address: Oregon Health Sciences University, 3181 SW Sam Jackson Park Rd., L103, Portland, OR 97201. Phone: (503) 494-6206. Fax: (503) 494-6886. E-mail: akkariy{at}ohsu.edu.

Molecular and Cellular Biology, November 2000, p. 8283-8289, Vol. 20, No. 21
0270-7306/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Howlett, N. G., Harney, J. A., Rego, M. A., Kolling, F. W. IV, Glover, T. W. (2009). Functional Interaction between the Fanconi Anemia D2 Protein and Proliferating Cell Nuclear Antigen (PCNA) via a Conserved Putative PCNA Interaction Motif. J. Biol. Chem. 284: 28935-28942 [Abstract] [Full Text]  
  • Muniandy, P. A., Thapa, D., Thazhathveetil, A. K., Liu, S.-t., Seidman, M. M. (2009). Repair of Laser-localized DNA Interstrand Cross-links in G1 Phase Mammalian Cells. J. Biol. Chem. 284: 27908-27917 [Abstract] [Full Text]  
  • Al-Minawi, A. Z., Lee, Y.-F., Hakansson, D., Johansson, F., Lundin, C., Saleh-Gohari, N., Schultz, N., Jenssen, D., Bryant, H. E., Meuth, M., Hinz, J. M., Helleday, T. (2009). The ERCC1/XPF endonuclease is required for completion of homologous recombination at DNA replication forks stalled by inter-strand cross-links. Nucleic Acids Res 37: 6400-6413 [Abstract] [Full Text]  
  • Zhao, J., Jain, A., Iyer, R. R., Modrich, P. L., Vasquez, K. M. (2009). Mismatch repair and nucleotide excision repair proteins cooperate in the recognition of DNA interstrand crosslinks. Nucleic Acids Res 37: 4420-4429 [Abstract] [Full Text]  
  • Cui, B., Johnson, S. P., Bullock, N., Ali-Osman, F., Bigner, D. D., Friedman, H. S. (2009). Bifunctional DNA Alkylator 1,3-Bis(2-chloroethyl)-1-nitrosourea Activates the ATR-Chk1 Pathway Independently of the Mismatch Repair Pathway. Mol. Pharmacol. 75: 1356-1363 [Abstract] [Full Text]  
  • Razidlo, G. L., Johnson, H. J., Stoeger, S. M., Cowan, K. H., Bessho, T., Lewis, R. E. (2009). KSR1 Is Required for Cell Cycle Reinitiation Following DNA Damage. J. Biol. Chem. 284: 6705-6715 [Abstract] [Full Text]  
  • Collins, N. B., Wilson, J. B., Bush, T., Thomashevski, A., Roberts, K. J., Jones, N. J., Kupfer, G. M. (2009). ATR-dependent phosphorylation of FANCA on serine 1449 after DNA damage is important for FA pathway function. Blood 113: 2181-2190 [Abstract] [Full Text]  
  • Derheimer, F. A., Hicks, J. K., Paulsen, M. T., Canman, C. E., Ljungman, M. (2009). Psoralen-Induced DNA Interstrand Cross-Links Block Transcription and Induce p53 in an Ataxia-Telangiectasia and Rad3-Related-Dependent Manner. Mol. Pharmacol. 75: 599-607 [Abstract] [Full Text]  
  • Gari, K., Decaillet, C., Delannoy, M., Wu, L., Constantinou, A. (2008). Remodeling of DNA replication structures by the branch point translocase FANCM. Proc. Natl. Acad. Sci. USA 105: 16107-16112 [Abstract] [Full Text]  
  • Fisher, L. A., Bessho, M., Bessho, T. (2008). Processing of a Psoralen DNA Interstrand Cross-link by XPF-ERCC1 Complex in Vitro. J. Biol. Chem. 283: 1275-1281 [Abstract] [Full Text]  
  • Grillari, J., Katinger, H., Voglauer, R. (2007). Contributions of DNA interstrand cross-links to aging of cells and organisms. Nucleic Acids Res 0: gkm1065v1-gkm1065 [Abstract] [Full Text]  
  • Otterlei, M., Bruheim, P., Ahn, B., Bussen, W., Karmakar, P., Baynton, K., Bohr, V. A. (2006). Werner syndrome protein participates in a complex with RAD51, RAD54, RAD54B and ATR in response to ICL-induced replication arrest. J. Cell Sci. 119: 5137-5146 [Abstract] [Full Text]  
  • Arnould, S., Spanswick, V. J., Macpherson, J. S., Hartley, J. A., Thurston, D. E., Jodrell, D. I., Guichard, S. M. (2006). Time-dependent cytotoxicity induced by SJG-136 (NSC 694501): influence of the rate of interstrand cross-link formation on DNA damage signaling.. Molecular Cancer Therapeutics 5: 1602-1609 [Abstract] [Full Text]  
  • Andreassen, P. R., Ho, G. P.H., D'Andrea, A. D. (2006). DNA damage responses and their many interactions with the replication fork. Carcinogenesis 27: 883-892 [Abstract] [Full Text]  
  • Hovest, M. G., Bruggenolte, N., Hosseini, K. S., Krieg, T., Herrmann, G. (2006). Senescence of Human Fibroblasts after Psoralen Photoactivation Is Mediated by ATR Kinase and Persistent DNA Damage Foci at Telomeres. Mol. Biol. Cell 17: 1758-1767 [Abstract] [Full Text]  
  • Zhang, N., Kaur, R., Lu, X., Shen, X., Li, L., Legerski, R. J. (2005). The Pso4 mRNA Splicing and DNA Repair Complex Interacts with WRN for Processing of DNA Interstrand Cross-links. J. Biol. Chem. 280: 40559-40567 [Abstract] [Full Text]  
  • Houghtaling, S., Newell, A., Akkari, Y., Taniguchi, T., Olson, S., Grompe, M. (2005). Fancd2 functions in a double strand break repair pathway that is distinct from non-homologous end joining. Hum Mol Genet 14: 3027-3033 [Abstract] [Full Text]  
  • Yang, Y.-G., Herceg, Z., Nakanishi, K., Demuth, I., Piccoli, C., Michelon, J., Hildebrand, G., Jasin, M., Digweed, M., Wang, Z.-Q. (2005). The Fanconi anemia group A protein modulates homologous repair of DNA double-strand breaks in mammalian cells. Carcinogenesis 26: 1731-1740 [Abstract] [Full Text]  
  • Richards, S., Liu, S.-T., Majumdar, A., Liu, J.-L., Nairn, R. S., Bernier, M., Maher, V., Seidman, M. M. (2005). Triplex targeted genomic crosslinks enter separable deletion and base substitution pathways. Nucleic Acids Res 33: 5382-5393 [Abstract] [Full Text]  
  • Dendouga, N., Gao, H., Moechars, D., Janicot, M., Vialard, J., McGowan, C. H. (2005). Disruption of Murine Mus81 Increases Genomic Instability and DNA Damage Sensitivity but Does Not Promote Tumorigenesis. Mol. Cell. Biol. 25: 7569-7579 [Abstract] [Full Text]  
  • Barber, L. J., Ward, T. A., Hartley, J. A., McHugh, P. J. (2005). DNA Interstrand Cross-Link Repair in the Saccharomyces cerevisiae Cell Cycle: Overlapping Roles for PSO2 (SNM1) with MutS Factors and EXO1 during S Phase. Mol. Cell. Biol. 25: 2297-2309 [Abstract] [Full Text]  
  • Mi, J., Kupfer, G. M. (2005). The Fanconi anemia core complex associates with chromatin during S phase. Blood 105: 759-766 [Abstract] [Full Text]  
  • Houghtaling, S., Granville, L., Akkari, Y., Torimaru, Y., Olson, S., Finegold, M., Grompe, M. (2005). Heterozygosity for p53 (Trp53+/-) Accelerates Epithelial Tumor Formation in Fanconi Anemia Complementation Group D2 (Fancd2) Knockout Mice. Cancer Res. 65: 85-91 [Abstract] [Full Text]  
  • Clerici, M., Baldo, V., Mantiero, D., Lottersberger, F., Lucchini, G., Longhese, M. P. (2004). A Tel1/MRX-Dependent Checkpoint Inhibits the Metaphase-to-Anaphase Transition after UV Irradiation in the Absence of Mec1. Mol. Cell. Biol. 24: 10126-10144 [Abstract] [Full Text]  
  • Qiao, F., Mi, J., Wilson, J. B., Zhi, G., Bucheimer, N. R., Jones, N. J., Kupfer, G. M. (2004). Phosphorylation of Fanconi Anemia (FA) Complementation Group G Protein, FANCG, at Serine 7 Is Important for Function of the FA Pathway. J. Biol. Chem. 279: 46035-46045 [Abstract] [Full Text]  
  • Mi, J., Qiao, F., Wilson, J. B., High, A. A., Schroeder, M. J., Stukenberg, P. T., Moss, A., Shabanowitz, J., Hunt, D. F., Jones, N. J., Kupfer, G. M. (2004). FANCG Is Phosphorylated at Serines 383 and 387 during Mitosis. Mol. Cell. Biol. 24: 8576-8585 [Abstract] [Full Text]  
  • Saffran, W. A., Ahmed, S., Bellevue, S., Pereira, G., Patrick, T., Sanchez, W., Thomas, S., Alberti, M., Hearst, J. E. (2004). DNA Repair Defects Channel Interstrand DNA Cross-links into Alternate Recombinational and Error-prone Repair Pathways. J. Biol. Chem. 279: 36462-36469 [Abstract] [Full Text]  
  • Niedernhofer, L. J., Odijk, H., Budzowska, M., van Drunen, E., Maas, A., Theil, A. F., de Wit, J., Jaspers, N. G. J., Beverloo, H. B., Hoeijmakers, J. H. J., Kanaar, R. (2004). The Structure-Specific Endonuclease Ercc1-Xpf Is Required To Resolve DNA Interstrand Cross-Link-Induced Double-Strand Breaks. Mol. Cell. Biol. 24: 5776-5787 [Abstract] [Full Text]  
  • Rothfuss, A., Grompe, M. (2004). Repair Kinetics of Genomic Interstrand DNA Cross-Links: Evidence for DNA Double-Strand Break-Dependent Activation of the Fanconi Anemia/BRCA Pathway. Mol. Cell. Biol. 24: 123-134 [Abstract] [Full Text]  
  • Houghtaling, S., Timmers, C., Noll, M., Finegold, M. J., Jones, S. N., Meyn, M. S., Grompe, M. (2003). Epithelial cancer in Fanconi anemia complementation group D2 (Fancd2) knockout mice. Genes Dev. 17: 2021-2035 [Abstract] [Full Text]  
  • Lambert, S., Mason, S. J., Barber, L. J., Hartley, J. A., Pearce, J. A., Carr, A. M., McHugh, P. J. (2003). Schizosaccharomyces pombe Checkpoint Response to DNA Interstrand Cross-Links. Mol. Cell. Biol. 23: 4728-4737 [Abstract] [Full Text]  
  • Bessho, T. (2003). Induction of DNA Replication-mediated Double Strand Breaks by Psoralen DNA Interstrand Cross-links. J. Biol. Chem. 278: 5250-5254 [Abstract] [Full Text]  
  • Weiss, R. S., Leder, P., Vaziri, C. (2003). Critical Role for Mouse Hus1 in an S-Phase DNA Damage Cell Cycle Checkpoint. Mol. Cell. Biol. 23: 791-803 [Abstract] [Full Text]  
  • Zheng, H., Wang, X., Warren, A. J., Legerski, R. J., Nairn, R. S., Hamilton, J. W., Li, L. (2003). Nucleotide Excision Repair- and Polymerase {eta}-Mediated Error-Prone Removal of Mitomycin C Interstrand Cross-Links. Mol. Cell. Biol. 23: 754-761 [Abstract] [Full Text]  
  • Richie, C. T., Peterson, C., Lu, T., Hittelman, W. N., Carpenter, P. B., Legerski, R. J. (2002). hSnm1 Colocalizes and Physically Associates with 53BP1 before and after DNA Damage. Mol. Cell. Biol. 22: 8635-8647 [Abstract] [Full Text]  
  • De Silva, I. U., McHugh, P. J., Clingen, P. H., Hartley, J. A. (2002). Defects in interstrand cross-link uncoupling do not account for the extreme sensitivity of ERCC1 and XPF cells to cisplatin. Nucleic Acids Res 30: 3848-3856 [Abstract] [Full Text]  
  • Digweed, M., Rothe, S., Demuth, I., Scholz, R., Schindler, D., Stumm, M., Grompe, M., Jordan, A., Sperling, K. (2002). Attenuation of the formation of DNA-repair foci containing RAD51 in Fanconi anaemia. Carcinogenesis 23: 1121-1126 [Abstract] [Full Text]  
  • Zhang, N., Lu, X., Zhang, X., Peterson, C. A., Legerski, R. J. (2002). hMutS{beta} Is Required for the Recognition and Uncoupling of Psoralen Interstrand Cross-Links In Vitro. Mol. Cell. Biol. 22: 2388-2397 [Abstract] [Full Text]  
  • Grompe, M., D'Andrea, A. (2001). Fanconi anemia and DNA repair. Hum Mol Genet 10: 2253-2259 [Abstract] [Full Text]  
  • Vasquez, K. M., Marburger, K., Intody, Z., Wilson, J. H. (2001). Manipulating the mammalian genome by homologous recombination. Proc. Natl. Acad. Sci. USA 98: 8403-8410 [Abstract] [Full Text]  
  • Qiao, F., Moss, A., Kupfer, G. M. (2001). Fanconi Anemia Proteins Localize to Chromatin and the Nuclear Matrix in a DNA Damage- and Cell Cycle-regulated Manner. J. Biol. Chem. 276: 23391-23396 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»