218
Views
14
CrossRef citations to date
0
Altmetric
Articles

Non-specificity and synergy at the binding site of the carboplatin-induced DNA adduct via molecular dynamics simulations of the MutSα–DNA recognition complex

&
Pages 969-992 | Received 19 Mar 2013, Accepted 23 Apr 2013, Published online: 25 Jun 2013

References

  • Andrews, P., & Howell, S. (1990). Cellular pharmacology of cisplatin: Perspectives on mechanisms of acquired resistance. Cancer Cells, 2, 35–43.
  • Auffinger, P., & Westhof, E. (1997). Three ns of multiple molecular dynamics simulations of solvated tRNA(ASP) anticodon hairpin. Journal of Molecular Biology, 269, 326–341.
  • Barlow, D. J., & Thornton, J. M. (1983). Ion-pairs in proteins. Journal of Molecular Biology, 168, 867–885.
  • Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., DiNola, A., & Haak, J. R. (1984). Molecular dynamics with coupling to an external bath. Journal of Chemical Physics, 81, 3684–3690.
  • Brooks, B. R., Bruccoleri, R. E., Olafson, B. D., States, D. J., Swaminatan, S., & Karplus, M. (1983). CHARMM: A program for macromolecular energy, minimization, and dynamics calculations. Journal of Computational Chemistry, 4, 187–217.
  • Cannavo, E., Gerrits, B., Marra, G., Schlapbach, R., & Jiricny, J. (2007). Characterization of the interactome of the human MutL homologues MLH1, PMS1, and PMS2. Journal of Biological Chemistry, 282, 2976–2986.
  • Caves, L. S. D., Evanseck, J. D., & Karplus, M. (1998). Locally accessible conformations of proteins: Multiple molecular dynamics simulations of crambin. Protein Science, 7, 649–666.
  • Darden, T., York, D., & Pedersen, L. (1993). Particle Mesh Ewald: An N Log(N) method for Ewald sums in large systems. Journal of Chemical Physics, 98, 10089–10092.
  • Deans, A. J., & West, S. C. (2011). DNA interstrand crosslink repair and cancer. Nature Reviews, 11, 467–480.
  • Desiraju, G. R., & Steiner, T. (1999). The weak hydrogen bond in structural chemistry and biology. New York, NY: Oxford University Press.
  • Drotschmann, K., Topping, R. P., Clodfelter, J. E., & Salsbury, F. R., Jr (2004). Mutations in the nucleotide-binding domain of MutS homologs uncouple cell death from cell survival. DNA Repair (Amsterdam), 3, 729–742.
  • Duckett, D. R., Drummond, J. T., Alastair, I. H., Murchie, A. I. H., Reardon, J. T., Joyce, T., … Modrich, P. (1996). Human MutSα recognizes damaged DNA base pairs containing 06-methylguanine, 04-methylthymine, or the cisplatin-d(GpG) adduct. Proceedings of the National Academy of Sciences USA, 93, 6443–6447.
  • Dutta, S. (2011). Studying the interaction of cancer and thrombosis therapeutics with protein and DNA (Doctoral dissertation). Wake Forest University, USA.
  • Eisen, M. B., Spellman, P. T., Brown, P. O., & Botstein, D. (1998). Cluster analysis and display of genome-wide expression patterns. Proceedings of the National Academy of Sciences USA, 95, 14863–14868.
  • Elizondo-Riojas, M. A., & Kozelka, J. (2001). Unrestrained 5 ns molecular dynamics simulation of a cisplatin–DNA 1,2-GG adduct provides a rationale for the NMR features and reveals increased conformational flexibility at the platinum binding site. Journal of Molecular Biology, 314, 1227–1243.
  • Fink, D., Nebel, S., Aebi, S., Zheng, H., Cenni, B., Nehme, A., … Howell, S. B. (1996). The role of DNA mismatch repair in platinum drug resistance. Cancer Research, 56, 4881–4886.
  • Gelasco, A., & Lippard, S. J. (1998). NMR solution structure of a DNA dodecamer duplex containing a cis-diammineplatinum(ii) d(GpG) intrastrand cross-link, the major adduct of the anticancer drug cisplatin. Biochemistry, 37, 9230–9239.
  • Ghosh, S., Salsbury, F. R., Jr, Horita, D. A., & Gmeiner, W. H. (2011). Zn2+ selectively stabilizes FdU-substituted DNA through a unique major groove binding motif. Nucleic Acids Research, 39, 4490–4498.
  • Ginsburg, G. S., & Willard, H. F. (2009). Genomic and personalized medicine: Foundations and applications. Translational Research, 154, 277–287.
  • Glusker, J. P. (1998). Directional aspects of intermolecular interactions. Berlin: Springer-Verlag.
  • Harrap, K. R. (1985). Preclinical studies identifying carboplatin as a viable cisplatin alternative. Cancer Treatment Reviews, 12, 21–33.
  • Horita, D. A., Zhang, W., Smithgall, T. E., Gmeiner, W. H., & Byrd, R. A. (2000). Dynamics of the Hck-SH3 domain: Comparison of experiment with multiple molecular dynamics simulations. Protein Science, 9, 95–103.
  • Horowitz, S., & Trievel, R. C. (2012). Carbon–oxygen hydrogen bonding in biological structure and function. Journal of Biological Chemistry, 287, 41576–41582.
  • Huang, H., Dooley, P. A., Harris, C. M., Harris, T. M., & Stone, M. P. (2009). Differential base stacking interactions induced by trimethylene interstrand DNA cross-links in the 5′-CpG-3′ and 5′-GpC-3′ sequence contexts. Chemical Research in Toxicology, 22, 1810–1816.
  • Huang, J.-C., Zamble, D. B., Reardon, J. T., Lippard, S. J., & Sancar, A. (1994). HMG-domain proteins specifically inhibit the repair of the major DNA adduct of the anticancer drug cisplatin by human excision nuclease. Proceedings of the National Academy of Sciences USA, 91, 10394–10398.
  • Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics, 14, 33–38.
  • Hunenberger, P. H., Mark, A. E., & van Gunsteren, W. F. (1995). Fluctuation and cross-correlation analysis of protein motions observed in nanosecond molecular dynamics simulations. Journal of Molecular Biology, 252, 492–503.
  • Iyer, R. R., Pluciennik, A., Burdett, V., & Modrich, P. L. (2006). DNA mismatch repair: Functions and mechanisms. Chemical Reviews, 106, 302–323.
  • Jamieson, E. R., & Lippard, S. J. (1999). Structure, recognition, and processing of cisplatin–DNA adducts. Chemical Reviews, 99, 2467–2498.
  • Janin, J. (1999). Wet and dry interfaces: The role of solvent in protein–protein and protein–DNA recognition. Structure, 7, R277–R279.
  • Jeffrey, G. A., & Saenger, W. (1991). Hydrogen bonding in biological structures. Heidelberg: Springer Verlag.
  • Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., & Klein, M. L. (1983). Comparison of simple potential functions for simulated liquid water. Journal of Chemical Physics, 79, 926–935.
  • Kale, L., Skeel, R., Bhandarkar, M., Brunner, R., Gursoy, A., Krawetz, N., … Schulten, K. (1999). NAMD2: Greater scalability for parallel molecular dynamics. Journal of Computational Physics, 15, 1283–1312.
  • Kartalou, M., & Essigmann, J. M. (2001). Recognition of cisplatin adducts by cellular proteins. Mutation Research, 478, 1–21.
  • Kelland, L. (2007). The resurgence of platinum-based cancer chemotherapy. Nature, 7, 573–584.
  • Knaggs, M. H., Salsbury, F. R., Jr, Edgell, M. H., & Fetrow, J. S. (2007). Insights into correlated motions and long-range interactions in CheY derived from molecular dynamics simulations. Biophysical Journal, 15, 2062–2079.
  • Kuman, S., & Nussinov, R. (2002). Close-range electrostatic interactions in proteins. ChemBioChem, 3, 604–617.
  • Kuzmanic, A., & Zagrovic, B. (2010). Determination of ensemble-average pairwise root mean-square deviation from experimental B-factors. Biophysical Journal, 98, 861–871.
  • Livesay, D. R., Huynh, D. H., Dallakyan, S., & Jacobs, D. J. (2008). Hydrogen bond networks determine emergent mechanical and thermodynamic properties across a protein family. Chemistry Central Journal, 2.
  • Loccisano, A. E., Acevedo, O., DeChancie, J., Schulze, B. G., & Evanseck, J. D. (2004). Enhanced sampling by multiple molecular dynamics trajectories: Carbonmonoxy myoglobin 10 micros A0–>A(1–3 transition from ten 400 picosecond simulations. Journal of Molecular Graphics and Modelling, 22, 369–376.
  • MacKerell, A. D., Jr, Banavali, N., & Foloppe, N. (2001). Development and current status of the CHARMM force field for nucleic acids. Biopolymers, 56, 257–265.
  • MacKerell, A. D., Jr, Bashford, D., Bellot, M., Dunbrack, R. L., Evanseck, J. D., Field, M. J., … Karplus, M. (1998). All-atom empirical potential for molecular modeling and studies of proteins. Journal of Physical Chemistry B, 102, 3586–3616.
  • Marzilli, G. L., Saad, J. S., Kuklenyik, Z., Keating, K. A., & Xu, Y. (2001). Relationship of solution and protein-bound structures of DNA duplexes with the major intrastrand cross-link lesions formed on cisplatin binding to DNA. Journal of the American Chemical Society, 123, 2764–2770.
  • Matlab (7.10.0). (2010). Natick, MA: The MathWorks.
  • Mello, J. A., Acharya, S., Fishel, R., & Essigmann, J. M. (1996). The mismatch-repair protein hMSH2 binds selectively to DNA adducts of the anticancer drug cisplatin. Chemistry and Biology, 3, 579–589.
  • Mills, J. B., & Hagerman, P. J. (2004). Origin of the intrinsic rigidity of DNA. Nucleic Acids Research, 32, 4055–4059.
  • Negureanu, L., & Salsbury, F. R., Jr (2012a). Insights into protein–DNA interactions, stability and allosteric communications: A computational study of MutSα–DNA recognition complexes. Journal of Biomolecular Structure and Dynamics, 29, 757–776.
  • Negureanu, L., & Salsbury, F. R., Jr (2012b). The molecular origin of the MMR-dependent apoptosis pathway from dynamics analysis of MutSα–DNA complexes. Journal of Biomolecular Structure and Dynamics, 30, 347–361.
  • Panigrahi, S. K., & Desiraju, G. R. (2007a). Strong and weak hydrogen bonds in drug–DNA complexes: A statistical analysis. Journal of Biosciences, 32, 677–691.
  • Panigrahi, S. K., & Desiraju, G. R. (2007b). Strong and weak hydrogen bonds in the protein–ligand interface. Proteins, 67, 128–142.
  • Panigrahi, S. K., & Desiraju, G. R. (2008). Strong and weak hydrogen bonds in protein–ligand complexes of kinases: A comparative study. Amino Acids, 34, 617–633.
  • Peltomaki, P. (2003). Role of DNA mismatch repair defects in the pathogenesis of human cancer. Journal of Clinical Oncology, 21, 1174–1179.
  • Rajeswaran, A., Trojan, A., Burnand, B., & Giannelli, M. (2008). Efficacy and side effects of cisplatin- and carboplatin-based doublet chemotherapeutic regimens versus non-platinum-based doublet chemotherapeutic regimens as first line treatment of metastatic non-small cell lung carcinoma: a systematic review of randomized controlled trials. Lung Cancer, 59, 1–11.
  • Rosenberg, B., Van Camp, L., & Krigas, T. (1965). Inhibition of cell division in Escherichia coli by electrolysis products from a platinum electrode. Nature, 205, 698–699.
  • Salsbury, F. R., Jr (2010a). Effects of cisplatin binding to DNA on the dynamics of the E. coli MutS Dimer. Protein and Peptide Letters, 17, 744–750.
  • Salsbury, F. R., Jr (2010b). Molecular dynamics simulations of protein dynamics and their relevance to drug discovery. Current Opinion in Phamacology, 10, 738–744.
  • Salsbury, F. R., Jr, Clodfelter, J. E., Gentry, M. B., Hollis, T., & Scarpinato, D. K. (2006). The molecular mechanism of DNA damage recognition by MutS homologs and its consequences for cell death response. Nucleic Acids Research, 34, 2173–2185.
  • Salsbury, F. R., Jr, Crowder, M. W., Kingsmore, S. F., & Huntley, J. J. A. (2009). Molecular dynamics simulations of the metallo-beta-lactamase from Bacteroides fragilis in the presence and absence of a tight-binding inhibitor. Journal of Molecular Modeling, 15, 133–145.
  • Salsbury, F. R., Jr, Crowley, M. F., & Brooks, C. L. (2001). Modeling of the metallo-beta-lactamase from B-fragilis: Structural and dynamic effects of inhibitor binding. Proteins, 44, 448–459.
  • Sarkhel, S., & Desiraju, G. R. (2004). N–HO, O–HO, and C–HO hydrogen bonds in protein–ligand complexes: Strong and weak interactions in molecular recognition. Proteins, 54, 247–259.
  • Scheeff, E. D., Briggs, J. M., & Hawell, S. B. (1999). Molecular modeling of the intrastrand guanine–guanine DNA addcuts produced by cisplatin and oxaliplatin. Molecular Pharmacology, 56, 633–643.
  • Schonlau, M. (2002). The clustergram: A graph for visualizing hierarchical and non-hierarchical cluster analysis. The Stata Journal, 3, 316–327.
  • Sharma, S., Gong, P., Temple, B., Bhattacharyya, D., Dokholyan, N. V., & Chaney, S. G. (2007). Molecular dynamics simulations of cisplatin- and oxaliplatin-d(GG) intrastrand cross-links reveal differences in their conformational dynamics. Journal of Molecular Biology, 373, 1123–1140.
  • Sharma, R., Graham, J., Blagden, S., & Gabra, H. (2011). Sustained platelet-sparing effect of weekly low dose paclitaxel allows effective, tolerable delivery of extended dose dense weekly carboplatin in platinum resistant/refractory epithelial ovarian cancer. BMC Cancer, 11, 289.
  • Spiegel, K., & Magistrato, A. (2006). Modeling anticancer drug-DNA interactions via mixed QM/MM molecular dynamics simulations. Organic and Biomolecular Chemistry, 4, 2507–2517.
  • Steinbach, P. J., & Brooks, B. R. (1994). New spherical-cutoff methods for long-range forces in macromolecular simulations. Journal of Computational Chemistry, 15, 667–683.
  • Straub, J. E., Rashkin, A. B., & Thirumalai, D. (1994). Dynamics in rugged energy landscapes with applications to the S-peptide and ribonuclease. Journal of the American Chemical Society, 116, 2049–2063.
  • Takahara, P. M., Rosenzweig, A. C., Frederick, C. A., & Lippard, S. J. (1995). Crystal structure of double-stranded DNA containing the major adduct of the anticancer drug cisplatin. Nature, 377, 649–652.
  • Taylor, A., & Kennard, O. (1982). Crystallographic evidence for the existence of C–HO, C-HN and C-HCl hydrogen bonds. Journal of the America Chemical Society, 104, 5063–5070.
  • Teuben, J. M., Bauer, C., Wang, A. H. J., & Reedijk, J. (1999). Solution structure of a DNA duplex containing a cis-diammineplatinum(II) 1,3-d(GTG) intrastrand cross-link, a major adduct in cells treated with the anticancer drug carboplatin. Biochemistry, 38, 12305–12312.
  • Tiwari, A., & Panigrahi, S. K. (2007). HBAT: A complete package for analyzing strong and weak hydrogen bonds in macromolecular crystal structures. In Silico Biology, 7, 651–661.
  • Todd, R. C., & Lippard, S. J. (2010). Structure of duplex DNA containing the cisplatin 1,2-Pt(NH3)2–2+-d(GpG) cross-link at 1.77 A resolution. Journal of Inorganic Biochemistry, 104, 902–908.
  • Travers, A. A. (2004). The structural basis for DNA flexibility. The Philosophical Transactions of the Royal Society London, 362, 1423–1438.
  • van Gunsteren, W. F., & Berendsen, H. J. C. (1977). Algorithms for macromolecular dynamics and constraint dynamics. Molecular Physics, 34, 1311–1327.
  • Vasilyeva, A., Clodfelter, J. E., Gorczynski, M. J., Gerardi, A. R., King, S. B., Salsbury Jr, F. R., & Scarpinato, K. D. (2010). Parameters of reserpine analogs that induce MSH2/MSH6-dependent cytotoxic response. Journal of Nucleic Acids, Article I D 162018, 13 pages. doi:10.4061/2010/162018.
  • Vasilyeva, A., Clodfelter, J. E., Reactor, B., Hollis, T., Scarpinato, K. D., & Salsbury, F. R., Jr (2009). Small molecule induction of MSH2-dependent cell death suggests a vital role of mismatch repair proteins in cell death. DNA Repair, 8, 103–113.
  • Wang, D., & Lippard, S. J. (2005). Cellular processing of platinum anticancer drugs. Nature, 4, 307–321.
  • Wang, H., Yang, Y., Schofield, M. J., Du, C., Fridman, Y., Lee, S. D., & Erie, D. A. (2003). DNA bending and unbending by MutS govern mismatch recognition and specificity. Proceedings of the National Academy of Sciences USA, 100, 14822–14827.
  • Waozniak, K., & Blasiak, J. (2002). Recognition and repair of DNA–cisplatin adducts. Acta Biochimica Polonica, 49, 583–596.
  • Warren, J. J., Pohlhaus, T. J., Changele, A., Iyer, R. R., Modrich, P. L., & Beese, L. S. (2007). Structure of the human MutS DNA lesion recognition complex. Molecular Cell, 26, 579–592.
  • Wheate, N. J., Walker, S., Craig, G. E., & Onun, R. (2010). The status of platinum anticancer drugs in the clinic and in clinical trials. Dalton Transactions, 39, 813–827.
  • Williams, T., & Kelley, C. (2011). Gnuplot 4.5: An interactive plotting program. http://gnuplot.info
  • Wolfe, K. C., Hastings, W. A., Dutta, S., Long, A., Shapiro, B. A., Woolf, T. B., Guthold, M., & Chirijian, G. S. (2012). Multiscale modeling of double-helical DNA and RNA: A unification through lie groups. Journal Physical Chemistry B,dx.doi.org/10.1021/jp2126015 |.
  • Wu, Y., Pradhan, P., Havener, J., Boysen, G., Swenberg, J. A., Campbell, S. L., & Chaney, S. G. (2004). NMR solution structure of an oxaliplatin 1,2-d(GG) intrastrand cross-link in a DNA dodecamer duplex. Journal of Molecular Biology, 341, 1251–1269.
  • Yang, W. (2008). Structure and mechanism for DNA lesion recognition. Cell Research, 18, 184–197.
  • Young, L. C., Peters, A. C., Maeda, T., Edelmann, W., Kucherlapati, R., Andrew, S. E., & Tron, V. A. (2003). DNA mismatch repair protein Msh6 is required for optimal levels of ultraviolet-B-induced apoptosis in primary mouse fibroblasts. Journal of Investigative Dermatology, 121, 876–880.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.