Skip to main content
SpringerLink
Log in

The DNA helical biopolymer: A template for the binding, assembly, and reactivity of metal ions and complexes

  • Published:
Journal of Inorganic and Organometallic Polymers Aims and scope Submit manuscript

Abstract

The helical DNA polymer provides many structural features that facilitate the binding of metal ions or complexes. DNA binding inorganic agents have proven invaluable, with demonstrated applications ranging from chemotherapeutic agents to probes of DNA structure. This broad range of applications attests to the utility of inorganic agents in the design of compounds which interact with the DNA helix and is due, in part, to the ability of inorganic species to define a particular ligand geometry complementary to the DNA structure, bind, or chemically react along the polymer strand. While a diverse array of novel inorganic compounds that interact with DNA have already been studied, many opportunities still exist to exploit inorganic agents in the design of new molecules that will interact uniquely with the DNA polymer. This review examines the structure of the DNA polymer, emphasizing aspects which promote the binding of inorganic agents. Along with a structural overview, the binding modes available to an inorganic element or complex are reviewed, in combination with a discussion of the ability of the DNA to act as a template for the organized binding of inorganic agents. In addition, chemical alteration of the DNA polymer structure by inorganic agents is discussed, along with the potential utility of such modifications.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. C. R. Cantor and P. R. Schimmel,Biophysical Chemistry (W. H. Freeman, New York, 1980).

    Google Scholar 

  2. T. D. Tullius (ed.),Metal-DNA Chemistry ACS Symposium Series 402 (American Chemical Society, Washington, D.C., 1989).

    Google Scholar 

  3. A. M. Pyle and J. K. Barton,Prog. Inorg. Chem. 38, 413 (1990).

    Google Scholar 

  4. S. L. Bruhn, J. H. Toney, and S. J. Lippard,Prog. Inorg. Chem. 38, 413 (1990).

    Google Scholar 

  5. M. J. Gait (ed.),Oligonucleotide Synthesis. A Practical Approach (IRL Press, Washington, D.C., 1985).

    Google Scholar 

  6. R. E. Dickerson, H. R. Drew, B. N. Conner, R. M. Wing, A. V. Fratini, and M. L. Kopka,Science 216, 475 (1982).

    Google Scholar 

  7. W. Saenger,Principles of Nucleic Acid Structure (Springer-Verlag, New York, 1988).

    Google Scholar 

  8. A. Rich, A. Nordheim, and A. H.-J. Wang,Annu. Rev. Biochem. 53, 791 (1984).

    Google Scholar 

  9. R. D. Wells, D. B. Collier, J. C. Hanvey, M. Shimizu, and F. Wohlrab,FASEB J. 2, 2939 (1988); R. D. Wells and S. C. Harvey (eds.),Unusual DNA Structures (Springer-Verlag, New York, 1988); D. M. J. Lilley,Chem. Soc. Rev. 18, 53 (1989).

    Google Scholar 

  10. C. R. Calladine,J. Mol. Biol. 161, 343 (1982); R. E. Dickerson,J. Mol. Biol. 166, 419 (1983).

    Google Scholar 

  11. R. B. Martin,Acc. Chem. Res. 18, 32 (1985); H. Pezzano and F. Podo,Chem. Rev. 80, 365 (1980).

    Google Scholar 

  12. S. B. Zimmerman,Annu. Rev. Biochem. 51, 395 (1982); E. Rowatt and R. J. P. Williams,J. Inorg. Biochem. 46, 87 (1992).

    Google Scholar 

  13. P. Aich, R. Sen, and D. Dasgupta,Biochemistry 31, 2988 (1992).

    Google Scholar 

  14. V. Thielking, U. Selent, E. Kohler, A. Landgraf, H. Wolfes, J. Alves, and A. Pingoud,Biochemistry 31, 3727 (1992).

    Google Scholar 

  15. T. F. Kagawa, B. H. Geierstanger, A. H.-J. Wang, and P. S. Ho,J. Biol. Chem. 266, 20175 (1991).

    Google Scholar 

  16. B. H. Geierstanger, T. F. Kagawa, S.-L. Chen, G. J. Quigley, and P. S. Ho,J. Biol. Chem. 266, 20185 (1991).

    Google Scholar 

  17. C. E. Lepre and S. J. Lippard,Nucleic Acids Mol. Biol. 4, 9 (1990); W. I. Sundquist and S. J. Lippard,Coord. Chem. Rev. 110, 293 (1990).

    Google Scholar 

  18. S. E. Sherman and S. J. Lippard,Chem. Rev. 87, 1153 (1987).

    Google Scholar 

  19. A. L. Pinto and S. J. Lippard,Proc. Natl. Acad. Sci. USA 82, 4616 (1985); R. B. Ciccarelli, M. J. Solomon, A. Varshavsky, and S. J. Lippard,Biochemistry 24, 7533 (1985); W. J. Heiger-Bernays, J. M. Essigmann, and S. J. Lippard,Biochemistry 29, 8461 (1990); K. M. Comess, C. E. Costello, and S. J. Lippard,Biochemistry 29, 2102 (1990).

    Google Scholar 

  20. S. J. Berners-Price, T. A. Frenkiel, V. Frey, J. D. Ranford, and P. J. Sadler,J. Chem. Soc. Chem. Commun. 789 (1992).

  21. J. F. Hartwig and S. J. Lippard,J. Am. Chem. Soc. 114, 5646 (1992).

    Google Scholar 

  22. F. Herman, J. Kozelka, V. Stoven, E. Guittet, J.-P. Girault, H. D. Tam, J. Igolen, J. Y. Lallemand, and J. C. Chottard,Eur. J. Biochem. 194, 119 (1990).

    Google Scholar 

  23. S. F. Bellon, J. H. Coleman, and S. J. Lippard,Biochemistry 30, 8026 (1991); S. F. Bellon and S. J. Lippard,Biophys. Chem. 35, 179 (1990).

    Google Scholar 

  24. P. M. Pil and S. J. Lippard,Science 256, 234 (1992).

    Google Scholar 

  25. K. M. Comess, J. N. Burstyn, J. M. Essigmann, and S. J. Lippard,Biochemistry 31, 3975 (1992).

    Google Scholar 

  26. Y. Qu and N. Farrell,J. Am. Chem. Soc. 113, 4851 (1991).

    Google Scholar 

  27. E. C. Long and J. K. Barton,Acc. Chem. Res. 23, 271 (1990), and references therein.

    Google Scholar 

  28. E. F. Gale, E. Cundliffe, P. E. Reynolds, M. H. Richmond, and M. J. Waring,The Molecular Basis of Antibiotic Action (Wiley, London, 1972).

    Google Scholar 

  29. H. M. Berman and P. R. Young,Annu. Rev. Biophys. Bioeng. 10, 87 (1981); S. Neidle,Prog. Med. Chem. 16, 151 (1979).

    Google Scholar 

  30. K. W. Jennette, S. J. Lippard, G. A. Vassiliades, and W. R. Bauer,Proc. Natl. Acad. Sci. USA 71, 3839 (1974); M. Howe-Grant, K. Wu, W. R. Bauer, and S. J. Lippard,Biochemistry 15, 4339 (1976); S. J. Lippard,Acc. Chem. Res. 11, 211 (1978).

    Google Scholar 

  31. S. J. Lippard, P. J. Bond, K. C. Wu, and W. R. Bauer,Science 194, 726 (1976).

    Google Scholar 

  32. P. J. Bond, R. Langridge, K. W. Jennette, and S. J. Lippard,Proc. Natl. Acad. Sci. USA 72, 4825 (1975).

    Google Scholar 

  33. J. Cairns,Cold Spring Harbor Symp. Quant. Biol. 27, 311 (1962); D. M. Crothers,Biopolymers 6, 595 (1968).

    Google Scholar 

  34. A. H. J. Wang, J. Nathans, G. van der Marel, J. H. van Boom, and A. Rich,Nature 276, 471 (1978).

    Google Scholar 

  35. J. K. Barton, J. J. Dannenberg, and A. L. Raphael,J. Am. Chem. Soc. 104, 4967 (1982).

    Google Scholar 

  36. J. K. Barton,Science 233, 727 (1986).

    Google Scholar 

  37. J. K. Barton, A. T. Danishefsky, and J. M. Goldberg,J. Am. Chem. Soc. 106, 2172 (1984); C. V. Kumar, J. K. Barton, and N. J. Turro,J. Am. Chem. Soc. 107, 5518 (1985); J. K. Barton, J. M. Goldberg, C. V. Kumar, and N. J. Turro,J. Am. Chem. Soc. 108, 2081 (1986); J. K. Barton,J. Biomol. Struct. Dyn. 1, 621 (1983).

    Google Scholar 

  38. A. Yamagishi,J. Chem. Soc. Chem. Commun. 572 (1983).

  39. J. P. Rehmann and J. K. Barton,Biochemistry 29, 1701 (1990); J. P. Rehmann and J. K. Barton,Biochemistry 29, 1710 (1990).

    Google Scholar 

  40. C. Hiort, B. Norden, and A. Rodger,J. Am. Chem. Soc. 112, 1971 (1990).

    Google Scholar 

  41. M. Ericksson, M. Leijon, C. Hiort, B. Norden, and A. Graslund,J. Am. Chem. Soc. 114, 4933 (1992).

    Google Scholar 

  42. A. M. Pyle, E. C. Long, and J. K. Barton,J. Am. Chem. Soc. 111, 4520 (1989).

    Google Scholar 

  43. A. Sitlani, E. C. Long, A. M. Pyle, and J. K. Barton,J. Am. Chem. Soc. 114, 2303 (1992).

    Google Scholar 

  44. M. B. Fleisher, H.-Y. Mei, and J. K. Barton,Nucleic Acids Mol. Biol. 2, 65 (1988).

    Google Scholar 

  45. S.-F. Chan, M. Chou, C. Creutz, T. Matsubara, and N. Sutin,J. Am. Chem. Soc. 103, 369 (1981); G. M. Brown, S.-F. Chan, C. Creutz, H. A. Schwartz, and N. Sutin,J. Am. Chem. Soc. 101, 7639 (1979); M. T. Indelli, A. Carioli, and F. Scandola,J. Phys. Chem. 88, 2685 (1984); R. Ballardini, G. Varani, and V. Balzani,J. Am. Chem. Soc. 102, 1719 (1980); M. E. Frink, S. D. Sprouse, H. A. Goodwin, R. J. Watts, and P. C. Ford,Inorg. Chem. 27, 1283 (1988).

    Google Scholar 

  46. P. Huber, T. Morii, H.-Y. Mei, and J. K. Barton,Proc. Natl. Acad. Sci. USA 88, 10801 (1991); K. Uchida, A. M. Pyle, T. Morii, and J. K. Barton,Nucleic Acids Res. 17, 10259 (1989).

    Google Scholar 

  47. A. M. Pyle, T. Morii, and J. K. Barton,J. Am. Chem. Soc. 112, 9432 (1990).

    Google Scholar 

  48. P. B. Dervan,Science 238, 645 (1987).

    Google Scholar 

  49. H. C. M. Nelson, J. T. Finch, B. F. Luisi, and A. Klug,Nature 330, 221 (1987); S. C. Satchwell, H. R. Drew, and A. A. Travers,J. Mol. Biol. 191, 659 (1986).

    Google Scholar 

  50. Z. Otwinowski, R. W. Schevitz, R.-G. Zhang, C. L. Lawson, A. Joachimiak, R. Q. Marmorstein, B. F. Luisi, and P. B. Sigler,Nature 335, 321 (1988).

    Google Scholar 

  51. T. A. Steitz,Q. Rev. Biophys. 23, 205 (1990).

    Google Scholar 

  52. R. V. Gessner, G. J. Quigley, A. H.-J. Wang, G. A. van der Marel, J. H. van Boom, and A. Rich,Biochemistry 24, 237 (1985).

    Google Scholar 

  53. M. B. Fleisher, K. C. Waterman, N. J. Turro, and J. K. Barton,Inorg. Chem. 25, 3551 (1986).

    Google Scholar 

  54. S. M. Hecht,Acc. Chem. Res. 19, 383 (1986).

    Google Scholar 

  55. J. Stubbe and J. W. Kozarich,Chem. Rev. 87, 1107 (1987).

    Google Scholar 

  56. B. J. Carter, V. S. Murty, K. S. Reddy, S.-N. Wang, and S. M. Hecht,J. Biol. Chem. 265, 4193 (1990).

    Google Scholar 

  57. N. Hamamichi, A. Natrajan, and S. M. Hecht,J. Am. Chem. Soc. 114, 6278 (1992).

    Google Scholar 

  58. J. Miller, A. D. McLachlan, and A. Klug,EMBO J. 4, 1609 (1985); A. D. Frankel, J. M. Berg, and C. O. Pabo,Proc. Natl. Acad. Sci. USA 84, 4841 (1987); J. M. Berg,J. Biol. Chem. 265, 6513 (1990).

    Google Scholar 

  59. N. P. Pavletich and C. O. Pabo,Science 252, 809 (1991); G. Parraga, S. J. Horvath, A. Eisen, W. E. Taylor, L. Hood, E. T. Young, and R. E. Klevit,Science 241, 1489 (1988); M. S. Lee, G. P. Gippert, K. V. Soman, D. A. Case, and P. E. Wright,Science 245, 635 (1989).

    Google Scholar 

  60. R. Marmorstein, M. Carey, M. Ptashne, and S. C. Harrison,Nature 356, 408 (1992); P. J. Kraulis, A. R. C. Raine, P. L. Gadhavi, and E. D. Laue,Nature 356, 448 (1992); J. D. Baleja, R. Marmorstein, S. C. Harrison, and G. Wagner,Nature 356, 450 (1992).

    Google Scholar 

  61. D. S. Sigman,Acc. Chem. Res. 19, 180 (1986); D. S. Sigman and C. B. Chen, in Ref. 2.

    Google Scholar 

  62. R. F. Pasternack and E. J. Gibbs, in Ref. 2.

    Google Scholar 

  63. M. D. Purugganan, C. V. Kumar, N. J. Turro, and J. K. Barton,Science 241, 1645 (1988).

    Google Scholar 

  64. A. M. Brun and A. Harriman,J. Am. Chem. Soc. 114, 3656 (1992).

    Google Scholar 

  65. A. K.-D. Mesmaker, G. Orellana, J. K. Barton, and N. J. Turro,Photochem. Photobiol. 52, 461 (1990).

    Google Scholar 

  66. R. F. Pasternack, E. J. Gibbs, R. Santucci, S. Schaertel, R. Ellinas, and S. C. Mah,J. Chem. Soc. Chem. Commun. 1771 (1987).

  67. R. F. Pasternack, A. Giannetto, P. Pagano, and E. J. Gibbs,J. Am. Chem. Soc. 113, 7799 (1991).

    Google Scholar 

  68. E. J. Gibbs, I. Tinoco Jr., M. Maestre, P. A. Ellinas, and R. F. Pasternack,Biochem. Biophys. Res. Commun. 157, 350 (1988); R. F. Pasternack, R. A. Brigandi, M. J. Abrams, A. P. Williams, and E. J. Gibbs,Inorg. Chem. 29, 4483 (1990).

    Google Scholar 

  69. J. Malinge and M. Leng,Proc. Natl. Acad. Sci. USA 83, 6317 (1986); J. Malinge, A. Schwartz, and M. Leng,Nucleic Acids Res. 15, 1779 (1987); J. Malinge and M. Leng,Nucleic Acids Res. 16, 7663 (1988).

    Google Scholar 

  70. W. I. Sundquist, D. P. Bancroft, L. Chassot, and S. J. Lippard,J. Am. Chem. Soc. 110, 8559 (1988).

    Google Scholar 

  71. L. A. Basile and J. K. Barton, inMetal Ions in Biological Systems, H. Sigel, ed. (Marcel Dekker, New York, 1989).

    Google Scholar 

  72. R. P. Herzberg and P. B. Dervan,J. Am. Chem. Soc. 104, 313 (1982); R. P. Herzberg and P. B. Dervan,Biochemistry 23, 3934 (1984).

    Google Scholar 

  73. T. D. Tullius, B. A. Dombroski, M. E. A. Churchill, and L. Kam,Methods Enzymol. 155, 537 (1987); T. D. Tullius,Annu. Rev. Biophys. Biophys. Chem. 1, 213 (1989).

    Google Scholar 

  74. K. Yamamoto and S. Kawanishi,J. Biol. Chem. 264, 15435 (1989); J.-L. Sagripanti and K. H. Kraemer,J. Biol. Chem. 264, 1729 (1989).

    Google Scholar 

  75. X. Chen, S. E. Rokita, and C. J. Burrows,J. Am. Chem. Soc. 113, 5884 (1991); X. Chen, C. J. Burrows, and S. E. Rokita,J. Am. Chem. Soc. 114, 322 (1992).

    Google Scholar 

  76. R. B. Van Atta, J. Bernadou, B. Meunier, and S. M. Hecht,Biochemistry 29, 4783 (1990); B. Ward, A. Skorobogaty, and J. C. Dabrowiak,Biochemistry 25, 6875 (1986); G. Raner, J. Goodisman, and J. C. Dabrowiak, in Ref. 2; J. T. Groves and T. P. Farrell,J. Am. Chem. Soc. 111, 4998 (1989).

    Google Scholar 

  77. M. K. Stern, J. K. Bashkin, and E. D. Sall,J. Am. Chem. Soc. 112, 5357 (1990); J. Chin and M. Banaszczyk,J. Am. Chem. Soc. 111, 4103 (1989); J. R. Morrow, L. A. Buttrey, V. M. Shelton, and K. A. Berback,J. Am. Chem. Soc. 114, 1903 (1992); M. Komiyama, K. Matsumura, and Y. Matsumoto,J. Chem. Soc. Chem. Commun. 640 (1992).

    Google Scholar 

  78. L. A. Basile and J. K. Barton,J. Am. Chem. Soc. 109, 7548 (1987); L. A. Basile, A. L. Raphael, and J. K. Barton,J. Am. Chem. Soc. 109, 7550 (1987).

    Google Scholar 

  79. J. P. Sluka, S. J. Horvath, M. F. Bruist, M. I. Simon, and P. B. Dervan,Science 238, 1129 (1987); D. P. Mack, B. L. Iverson, and P. B. Dervan,J. Am. Chem. Soc. 110, 7572 (1988); D. P. Mack and P. B. Dervan,J. Am. Chem. Soc. 112, 4604 (1990); C.-H. B. Chen and D. S. Sigman,Science 237, 1197 (1987).

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Chemistry, Indiana University-Purdue University at Indianapolis, 402 North Blackford Street, 46202-3274, Indianapolis, Indiana

    Eric C. Long

Authors
  1. Eric C. Long
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Long, E.C. The DNA helical biopolymer: A template for the binding, assembly, and reactivity of metal ions and complexes. J Inorg Organomet Polym 3, 3–39 (1993). https://doi.org/10.1007/BF00696751

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00696751

Key words

Search

Navigation