FANCD2–FANCI is a clamp stabilized on DNA by monoubiquitination of FANCD2 during DNA repair (original) (raw)

• Kottemann, M. C. & Smogorzewska, A. Fanconi anaemia and the repair of Watson and Crick DNA crosslinks. Nature 493, 356–363 (2013).
  CAS PubMed PubMed Central Google Scholar
• Crossan, G. P. & Patel, K. J. The Fanconi anaemia pathway orchestrates incisions at sites of crosslinked DNA. J. Pathol. 226, 326–337 (2012).
  CAS PubMed Google Scholar
• Walden, H. & Deans, A. J. The Fanconi anemia DNA repair pathway: structural and functional insights into a complex disorder. Annu. Rev. Biophys. 43, 257–278 (2014).
  CAS PubMed Google Scholar
• Knipscheer, P., Raschle, M., Scharer, O. D. & Walter, J. C. Replication-coupled, DNA interstrand cross-link repair in Xenopus egg extracts. Methods Mol. Biol. 920, 221–243 (2012).
  CAS PubMed PubMed Central Google Scholar
• Alpi, A. et al. UBE2T, the Fanconi anemia core complex, and FANCD2 are recruited independently to chromatin: a basis for the regulation of FANCD2 monoubiquitination. Mol. Cell Biol. 27, 8421–8430 (2007).
  CAS PubMed PubMed Central Google Scholar
• Garcia-Higuera, I. et al. Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol. Cell 7, 249–262 (2001).
  CAS PubMed Google Scholar
• Meetei, A. R. et al. A multiprotein nuclear complex connects Fanconi anemia and Bloom syndrome. Mol. Cell. Biol. 23, 3417–3426 (2003).
  CAS PubMed PubMed Central Google Scholar
• Rajendra, E. et al. The genetic and biochemical basis of FANCD2 monoubiquitination. Mol. Cell 54, 858–869 (2014).
  CAS PubMed PubMed Central Google Scholar
• van Twest, S. et al. Mechanism of ubiquitination and deubiquitination in the Fanconi anemia pathway. Mol. Cell 65, 247–259 (2017).
  CAS PubMed Google Scholar
• Knipscheer, P. et al. The Fanconi anemia pathway promotes replication-dependent DNA interstrand cross-link repair. Science 326, 1698–1701 (2009).
  CAS PubMed PubMed Central Google Scholar
• Sims, A. E. et al. FANCI is a second monoubiquitinated member of the Fanconi anemia pathway. Nat. Struct. Mol. Biol. 14, 564–567 (2007).
  CAS PubMed Google Scholar
• Smogorzewska, A. et al. Identification of the FANCI protein, a monoubiquitinated FANCD2 paralog required for DNA repair. Cell 129, 289–301 (2007).
  CAS PubMed PubMed Central Google Scholar
• Montes de Oca, R. et al. Regulated interaction of the Fanconi anemia protein, FANCD2, with chromatin. Blood 105, 1003–1009 (2005).
  PubMed Google Scholar
• MacKay, C. et al. Identification of KIAA1018/FAN1, a DNA repair nuclease recruited to DNA damage by monoubiquitinated FANCD2. Cell 142, 65–76 (2010).
  CAS PubMed PubMed Central Google Scholar
• Liu, T., Ghosal, G., Yuan, J., Chen, J. & Huang, J. FAN1 acts with FANCI-FANCD2 to promote DNA interstrand cross-link repair. Science 329, 693–696 (2010).
  CAS PubMed Google Scholar
• Smogorzewska, A. et al. A genetic screen identifies FAN1, a Fanconi anemia-associated nuclease necessary for DNA interstrand crosslink repair. Mol. Cell 39, 36–47 (2010).
  CAS PubMed PubMed Central Google Scholar
• Kratz, K. et al. Deficiency of FANCD2-associated nuclease KIAA1018/FAN1 sensitizes cells to interstrand crosslinking agents. Cell 142, 77–88 (2010).
  CAS PubMed Google Scholar
• Klein Douwel, D. et al. XPF-ERCC1 acts in unhooking DNA interstrand crosslinks in cooperation with FANCD2 and FANCP/SLX4. Mol. Cell 54, 460–471 (2014).
  CAS PubMed Google Scholar
• Hodskinson, M. R. et al. Mouse SLX4 is a tumor suppressor that stimulates the activity of the nuclease XPF-ERCC1 in DNA crosslink repair. Mol. Cell 54, 472–484 (2014).
  CAS PubMed PubMed Central Google Scholar
• Yamamoto, K. N. et al. Involvement of SLX4 in interstrand cross-link repair is regulated by the Fanconi anemia pathway. Proc. Natl Acad. Sci. USA 108, 6492–6496 (2011).
  CAS PubMed PubMed Central Google Scholar
• Oestergaard, V. H. et al. Deubiquitination of FANCD2 is required for DNA crosslink repair. Mol. Cell 28, 798–809 (2007).
  CAS PubMed PubMed Central Google Scholar
• Kim, J. M. et al. Inactivation of murine Usp1 results in genomic instability and a Fanconi anemia phenotype. Dev. Cell 16, 314–320 (2009).
  CAS PubMed PubMed Central Google Scholar
• Nijman, S. M. et al. The deubiquitinating enzyme USP1 regulates the Fanconi anemia pathway. Mol. Cell 17, 331–339 (2005).
  CAS PubMed Google Scholar
• Tan, W. & Deans, A. J. A defined role for multiple Fanconi anemia gene products in DNA-damage-associated ubiquitination. Exp. Hematol. 50, 27–32 (2017).
  CAS PubMed Google Scholar
• Ishiai, M. et al. FANCI phosphorylation functions as a molecular switch to turn on the Fanconi anemia pathway. Nat. Struct. Mol. Biol. 15, 1138–1146 (2008).
  CAS PubMed PubMed Central Google Scholar
• Cheung, R. S. et al. Ubiquitination-linked phosphorylation of the FANCI S/TQ cluster contributes to activation of the Fanconi anemia I/D2 complex. Cell Reports 19, 2432–2440 (2017).
  CAS PubMed Google Scholar
• Lopez-Martinez, D. et al. Phosphorylation of FANCD2 inhibits the FANCD2/FANCI complex and suppresses the Fanconi anemia pathway in the absence of DNA damage. Cell Reports 27, 2990–3005.e5 (2019).
  CAS PubMed Google Scholar
• Sato, K., Toda, K., Ishiai, M., Takata, M. & Kurumizaka, H. DNA robustly stimulates FANCD2 monoubiquitylation in the complex with FANCI. Nucleic Acids Res. 40, 4553–4561 (2012).
  CAS PubMed PubMed Central Google Scholar
• Shakeel, S. et al. Structure of the Fanconi anaemia monoubiquitin ligase complex. Nature 575, 234–237 (2019).
  CAS PubMed PubMed Central Google Scholar
• Liang, C. C. & Cohn, M. A. UHRF1 is a sensor for DNA interstrand crosslinks. Oncotarget 7, 3–4 (2016).
  PubMed Google Scholar
• Joo, W. et al. Structure of the FANCI-FANCD2 complex: insights into the Fanconi anemia DNA repair pathway. Science 333, 312–316 (2011).
  CAS PubMed PubMed Central Google Scholar
• Swuec, P. et al. The FA core complex contains a homo-dimeric catalytic module for the symmetric mono-ubiquitination of FANCI-FANCD2. Cell Reports 18, 611–623 (2017).
  CAS PubMed Google Scholar
• Liang, C. C. et al. The FANCD2–FANCI complex is recruited to DNA interstrand crosslinks before monoubiquitination of FANCD2. Nat. Commun. 7, 12124 (2016).
  CAS PubMed PubMed Central Google Scholar
• Chaugule, V. K., Arkinson, C., Toth, R. & Walden, H. Enzymatic preparation of monoubiquitinated FANCD2 and FANCI proteins. Methods Enzymol. 618, 73–104 (2019).
  PubMed Google Scholar
• Zhi, G. et al. Purification of FANCD2 sub-complexes. Br. J. Haematol. 150, 88–92 (2010).
  CAS PubMed PubMed Central Google Scholar
• Thompson, E. L. et al. FANCI and FANCD2 have common as well as independent functions during the cellular replication stress response. Nucleic Acids Res. 45, 11837–11857 (2017).
  CAS PubMed PubMed Central Google Scholar
• Dubois, E. L. et al. A Fanci knockout mouse model reveals common and distinct functions for FANCI and FANCD2. Nucleic Acids Res. 47, 7532–7547 (2019).
  PubMed PubMed Central Google Scholar
• Longerich, S. et al. Regulation of FANCD2 and FANCI monoubiquitination by their interaction and by DNA. Nucleic Acids Res. 42, 5657–5670 (2014).
  CAS PubMed PubMed Central Google Scholar
• Raschle, M. et al. Mechanism of replication-coupled DNA interstrand crosslink repair. Cell 134, 969–980 (2008).
  CAS PubMed PubMed Central Google Scholar
• Crossan, G. P. et al. Disruption of mouse Slx4, a regulator of structure-specific nucleases, phenocopies Fanconi anemia. Nat. Genet. 43, 147–152 (2011).
  CAS PubMed PubMed Central Google Scholar
• Parmar, K. et al. Hematopoietic stem cell defects in mice with deficiency of Fancd2 or Usp1. Stem Cells 28, 1186–1195 (2010).
  CAS PubMed PubMed Central Google Scholar
• Weissmann, F. et al. biGBac enables rapid gene assembly for the expression of large multisubunit protein complexes. Proc. Natl Acad. Sci. USA 113, E2564–E2569 (2016).
  CAS PubMed PubMed Central Google Scholar
• Hill, C. H. et al. Activation of the Endonuclease that Defines mRNA 3′ Ends Requires Incorporation into an 8-Subunit Core Cleavage and Polyadenylation Factor Complex. Mol. Cell 73, 1217–1231.e11 (2019).
  CAS PubMed PubMed Central Google Scholar
• Rueden, C. T. et al. ImageJ2: ImageJ for the next generation of scientific image data. BMC Bioinf. 18, 529 (2017).
  Google Scholar
• Russo, C. J. & Passmore, L. A. Electron microscopy: ultrastable gold substrates for electron cryomicroscopy. Science 346, 1377–1380 (2014).
  CAS PubMed PubMed Central Google Scholar
• Zivanov, J. et al. New tools for automated high-resolution cryo-EM structure determination in RELION-3. Elife 7, e42166 (2018).
  PubMed PubMed Central Google Scholar
• Zheng, S. Q. et al. MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14, 331–332 (2017).
  CAS PubMed PubMed Central Google Scholar
• Rohou, A. & Grigorieff, N. CTFFIND4: fast and accurate defocus estimation from electron micrographs. J. Struct. Biol. 192, 216–221 (2015).
  PubMed PubMed Central Google Scholar
• Nakane, T., Kimanius, D., Lindahl, E. & Scheres, S. H. Characterisation of molecular motions in cryo-EM single-particle data by multi-body refinement in RELION. Elife 7, e36861 (2018).
  PubMed PubMed Central Google Scholar
• Yang, J. et al. The I-TASSER Suite: protein structure and function prediction. Nat. Methods 12, 7–8 (2015).
  CAS PubMed PubMed Central Google Scholar
• Pettersen, E. F. et al. UCSF Chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).
  CAS PubMed Google Scholar
• Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486–501 (2010).
  CAS PubMed PubMed Central Google Scholar
• Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126–2132 (2004).
  PubMed Google Scholar
• Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213–221 (2010).
  CAS PubMed PubMed Central Google Scholar
• Vijay-Kumar, S., Bugg, C. E. & Cook, W. J. Structure of ubiquitin refined at 1.8 Å resolution. J. Mol. Biol. 194, 531–544 (1987).
  CAS PubMed Google Scholar
• Shevchenko, A., Wilm, M., Vorm, O. & Mann, M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850–858 (1996).
  CAS PubMed Google Scholar
• Rappsilber, J., Ishihama, Y. & Mann, M. Stop and Go Extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal. Chem. 75, 663–670 (2003).
  CAS PubMed Google Scholar
• Kolbowski, L., Mendes, M. L. & Rappsilber, J. Optimizing the parameters governing the fragmentation of cross-linked peptides in a Tribrid mass spectrometer. Anal. Chem. 89, 5311–5318 (2017).
  CAS PubMed PubMed Central Google Scholar
• Mendes, M. L. et al. An integrated workflow for crosslinking mass spectrometry. Mol. Syst. Biol. 15, e8994 (2019).
  CAS PubMed PubMed Central Google Scholar
• Lenz, S., Giese, S. H., Fischer, L. & Rappsilber, J. In-search assignment of monoisotopic peaks improves the identification of cross-linked peptides. J. Proteome Res. 17, 3923–3931 (2018).
  CAS PubMed PubMed Central Google Scholar
• Perez-Riverol, Y. The PRIDE database and related tools and resources in 2019: improving support for quantification data. Nucleic Acids Res. 47, D442–D450 (2019).
  CAS PubMed Google Scholar
• Krissinel, E. & Henrick, K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. D Biol Crystallogr. 60, 2256–2268 (2004).
  CAS PubMed Google Scholar
• Naydenova, K. & Russo, C. J. Measuring the effects of particle orientation to improve the efficiency of electron cryomicroscopy. Nat. Commun. 8, 629 (2017).
  PubMed PubMed Central Google Scholar
• Kucukelbir, A., Sigworth, F. J. & Tagare, H. D. Quantifying the local resolution of cryo-EM density maps. Nat. Methods 11, 63–65 (2014).
  CAS PubMed Google Scholar