Skip to main content

Modeling the Metal Binding Sites in Core Histones: Interactions of Carcinogenic Ni(II) with the -CAIH- Motif of Histone H3

  • Chapter
Cytotoxic, Mutagenic and Carcinogenic Potential of Heavy Metals Related to Human Environment

Part of the book series: NATO ASI Series ((ASEN2,volume 26))

Abstract

This paper presents results of studies on interactions of carcinogenic nickel with -CAIH-, a potential metal binding motif in nuclear chromatin. Structural and mechanistic results are discussed in the perspective of various concepts in nickel carcinogenesis. Evidence is presented for a major role of oxidative mechanism of damage caused by Ni(II) binding and reactivity on both genotoxic (DNA) and epigenetic (core histones) levels. Preliminary results of a study of (H3-H4)2 histone tetramer supporting the validity of CAIH model are also shown.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 39.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 54.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. IARC (1990) IARC Monographs on the Evaluation of Carcinogenic Risk to Humans. Vol. 49. Chromium, Nickel and Welding, IARC, Lyon

    Google Scholar 

  2. Lee, J.E., Ciccarelli, R.B., and Wetterhahn-Jeanette, K. (1982) Solubilization of the carcinogen nickel subsulfide and its interaction with deoxynucleic acid and protein, Biochemistry 21, 771–778.

    Article  CAS  Google Scholar 

  3. Kasprzak, K.S., Waalkes, M.P., and Poirier, L.A. (1986) Antagonism by essential divalent metals and amino acids of nickel(II)-DNA binding in vitro, Toxicol. Appl. Pharmacol. 82, 336–343.

    Article  CAS  Google Scholar 

  4. Kasprzak, K. S. (1995) Possible role of oxidative damage in metal-induced carcinogenesis, Cancer Invest. 13, 411–430.

    Article  CAS  Google Scholar 

  5. Kasprzak, K.S. (1996) The oxidative damage hypothesis of metal-induced genotoxicity and carcinogenesis, this volume.

    Google Scholar 

  6. Tkeshelashvili, L.K., Reid, T.M., McBnde, T.J., and Loeb, L.A. (1993) Nickel induces a signature mutation for oxygen free radicals, Cancer Res. 53, 4172–4174.

    CAS  Google Scholar 

  7. Wallmg, C. (1975) Fenton’s reagent revisited, Acc. Chem. Res. 8, 125–131.

    Article  Google Scholar 

  8. Eickbush, T.H., and Moudrianakis, E.N. (1978) The histone core complex: An octamer assembled by two sets of protein-protein interactions, Biochemistry 17, 4955–4964.

    Article  CAS  Google Scholar 

  9. Arents, G., and Moudrianakis, E.N., (1993) Topography of the histone octamer surface: Repeating structural motifs utilized in the docking of nucleosomal DNA, Proc. Natl. Acad. Sci. USA 90, 10489–10493.

    Article  CAS  Google Scholar 

  10. Zlatanova, J., and van Holde, K. (1996) The linker histones and chromatin structure: new twists, in W.E. Cohn, and K. Moldave (eds.), Nucleic Acid Research and Molecular Biology, vol. 52, Academic Press,San Diego, pp. 217–2

    Google Scholar 

  11. Hsiung, N. and Kucherlapati, R. (1980) Histone gene expression and chromatin structure in mammalian cell hybrids, J. Cell. Biol. 87, 227–236.

    Article  CAS  Google Scholar 

  12. Alberts, D., Bray, D., Lewis, J., Raff, M., Roberts, K., and Watson, J.D. (1994) Molecular Biology of the Cell, 3rd ed., Garland, New York, pp. 335–399.

    Google Scholar 

  13. Cook, P.R. (1995) A chromomenc model for nuclear and chromosome structure, J. Cell. Sci. 108, 2927–2935.

    CAS  Google Scholar 

  14. Costa, M. (1991) Molecular mechanisms of nickel carcinogenesis, Annu. Rev. Pharmacol. Toxicol. 31, 321–337.

    Article  CAS  Google Scholar 

  15. Salnikov, K., Cosentino, S., Klein, C., and Costa, M. (1994) Loss of thrombospondin transcriptional activity in nickel-transformed cells, Mol. Cell. Biol. 14, 851–858.

    Google Scholar 

  16. Lee, Y.-W., Klein, C.B., Kargacin, B., Salnikov, K., Kitahara, J., Dowjat, K., Zhitkovich, A., and Costa, M. (1995) Carcinogenic nickel silences gene expression by chromatin condensation and DNA methylation: a new model for epigenetic carcinogen, Mol. Cell. Biol. 15, 2547–2557.

    CAS  Google Scholar 

  17. Huang, X., Kitahara, J., Zhitkovich, A., Dowjat, K., and Costa, M. (1995) Heterochromatic proteins specifically enhance nickel-induced 8-oxo-dG formation, Carcinogenesis 16, 1753–1759.

    Article  CAS  Google Scholar 

  18. Hartwig, A. (1995) Current aspects in metal genotoxicity, BioMetals 8, 3–11.

    Article  CAS  Google Scholar 

  19. Hartwig, A., Mullenders, L.H.F., Schlepegrell, R., Kasten, U., and Beyersmann, D. (1994) Nickel(II) interferes with the incision step in nucleotide excision repair in mammalian cells, Cancer Res. 54, 4045–4051.

    CAS  Google Scholar 

  20. Porter, D.W., Nelson, V.C., Fivash, Jr., M.J., and Kasprzak, K.S. (1996) Mechanistic studies on the inhibition by Ni(II) of 8-oxo-2′-deoxyguanosine-5′-triphosphatase (MutT), a nucleotide pool-sanitizing enzyme, in P. Collery (ed.), Metal Ions in Biology and Medicine, Vol. 4, John Libbey Eurotext, Montrouge, in press.

    Google Scholar 

  21. Datta, A.K., Shi, X., and Kasprzak, K.S. (1993) Effect of carnosine, homocamosine, and anserine on hydroxylarion of the guanine moiety in 2′-deoxyguanosine, DNA and nucleohistone with hydrogen peroxide in the presence of nickel (II), Carcinogenesis 14, 417–422.

    Article  CAS  Google Scholar 

  22. Halcrow, MA. and Chnstou, G. (1994) Biomimetic chemistry of nickel, Chem. Rev. 94, 2421–2481.

    Article  CAS  Google Scholar 

  23. Pettit, L.D., Gregor, J.E., and Kozlowski, H., (1991) Complex formation between metal ions and peptides, in R.W. Hay, JR. Dillworth, and K.B. Nolan (eds.) Perspectives on Bioinorganic Chemistry Vol. 1 JAI Press,Greenwich, pp. 1–

    Google Scholar 

  24. IUPAC Stability Constants Database, Release 2, (1995) IUPAC and Academic Software

    Google Scholar 

  25. GenPept (GenBank Gene Products) Database distributed by National Cancer Institute Frederick Biomedical Supercomputing Center. For GenBank, cf. Burks, C, Cassidy, M., Cinkosky, M.J., Cumella, K.E., Gilna, P., Hayden, J. E-D., Kelley, T.A., Kelly, M., Kristofferson, D., and Ryals, J. (1991) GenBank, Nucl. Acids Res. 19 (Suppl.) 2221–2225.

    Article  Google Scholar 

  26. von Holt, C., Brandt, W.F., Greyling, HJ., Lindsey, G.G., Retief, J.D., Rodrigues, J. de A., Schwager, S., and Sewell, B.T. (1989) Isolation and characterization of histones. Appendix: Histone sequences, in P. M. Wassarman and R. D. Kornberg (eds.) Methods in Enzymology, Vol. 170, Nucleosomes, Academic Press, San Diego, pp. 503–523.

    Google Scholar 

  27. Arents, G., Burlingame, R.W., Wang, B.-C, Love, WE., and Moudnanakis, E.N. (1991) The nucleosomal core histone octamer at 3.1 A resolution: a tripartite protein assembly and a left-handed superhelix, Proc. Natl. Acad. Sci. USA 88, 10148–10152.

    Article  CAS  Google Scholar 

  28. Arents, G. and Moudrianakis, E.N. (1994) DNA protein interactions in chromatin and the structure of the histone octamer, in R.H. Sarma and M.H. Sarma (eds.), Structural Biology: The State of the Art, Proceedings of the Eighth Conversation, State University of New York, Albany, NY, 1993, Adenine Press, New York, pp. 93–108

    Google Scholar 

  29. Arents, G. and Moudnanakis, E.N. (1995) The histone fold: a ubiquitous architectural motif utilized in DNA compaction and protein dimerization, Proc. Natl. Acad. Sci. USA 92, 11170–11174.

    Article  CAS  Google Scholar 

  30. Wang, B.-C, `Rose, J., Arents, G., and Moudrianakis, E.N. (1994) The octameric histone core of the nucleosome. Structural issues resolved, J. Mol. Biol. 236, 179–188.

    Article  CAS  Google Scholar 

  31. Camenni-Otero, R.D., and Felsenfeld, G. (1977) Histone H3 disulfide dimers and nucleosome structure, Proc. Natl. Acad. Sci. USA 74, 5519–5523.

    Article  Google Scholar 

  32. Daban, J.-R., and Cantor, C.R. (1989) Use of fluorescent probes to study nucleosomes, in P. M. Wassarman and R. D Kornberg (eds.) Methods in Enzymology, Vol. 170, Nucleosomes., Academic Press, San Diego, pp. 192–214.

    Google Scholar 

  33. Bal, W., Chmurny, G.N., Hilton, B.D., Sadler, P.J., and Tucker, A. (1996) Axial hydrophobic fence in highly-stable Ni(II) complex of des-angiotensinogen N-terminal peptide, J. Am. Chem. Soc. in press.

    Google Scholar 

  34. Yamashita, M.M., Wesson, L., Eisenman, G., and Eisenberg, D.(1990) Where metal ions bind in proteins, Proc. Natl. Acad. Sci. USA 87, 5648–5652.

    Article  CAS  Google Scholar 

  35. Regan, L. (1993) The design of metal-binding sites in proteins, Annu. Rev. Biophys. Biomol. Struct. 22, 257–281.

    Article  CAS  Google Scholar 

  36. Saavedra, R.A. (1986) Histones and metal-binding domains. Science 232, 1589, and response from Berg, J.M. therein.

    Google Scholar 

  37. Bal, W., Lukszo, J., Jezowska-Bojczuk, M., and Kasprzak, K.S. (1995) Interactions of nickel(II) with histones. Stability and solution structure of complexes with CH3CO-Cys-Ala-Ile-His-NH2, a putative metal binding sequence of histone H3, Chem. Res. Toxicol. 8, 683–692.

    Article  CAS  Google Scholar 

  38. Sigel, H., and Martin, R.B. (1982) Coordinating properties of the amide bond. Stability and structure of metal ion complexes of peptides and related ligands, Chem. Rev. 82, 385–426.

    Article  CAS  Google Scholar 

  39. Chang, J.W., and Martin, R.B., (1969) Visible circular dichroism of planar nickel ion. Complexes of peptides and cysteine and derivatives, J. Phys. Chem. 73, 4277–4283.

    Article  CAS  Google Scholar 

  40. Kozlowski, H., Decock Le Reverend, B., Ficheux, D., Loucheux, C., and Sovago, I., (1987) Nickel(II) complexes with sulfhydryl containing peptides. Potentiometric and spectroscopic studies, J. Inorg. Biochem. 29, 187–197.

    Article  CAS  Google Scholar 

  41. Cherifi, K., Decock Le Reverend, B., Varnagy, K., Kiss, T., Sovago, I., Loucheux, C., and Kozlowski, H. (1990) Transition metal complexes of L-cysteine containing di-and tripeptides. J. Inorg. Biochem. 38, 69–80.

    Article  CAS  Google Scholar 

  42. Margerum, D.W., and Dukes, G.R. (1974) Kinetics and mechanism of metal-ion and proton-transfer reactions of oligopeptide complexes, in H. Sigel (ed.), Metal Ions in Biological Systems Vol.1, Simple Complexes, Marcel Dekker Inc., New York, pp. 158–212.

    Google Scholar 

  43. Bal, W., Kozlowski, H., Robbins, R., and Pettit, L.D. (1995) Competition between the terminal amino and imidazole nitrogen donors for co-ordination to Ni(II) ions in oligopeptides. Inorg. Chim. Acta 231, 7–12.

    Article  CAS  Google Scholar 

  44. Pettit, L.D., Pyburn, S., Bal, W., Kozlowski, H., and Bataille, M. (1990) A study of the comparative donor properties of the terminal amino and imidazole nitrogens in peptides, J. Chem. Soc, Dalton Trans. 3565–3570.

    Google Scholar 

  45. Bal, W., Jezowska-Bojczuk, M., Kozlowski, H., Chruscinski, L., Kupryszewski, G., and Mackiewicz, Z. (1995) Cu(II) binding by Asp-Arg-Val-Tyr-Ile-His and Arg-Val-Tyr-Ile-His, essential peptide fragments of angiotensin II, J. Inorg. Biochem. 57, 235–247.

    Article  CAS  Google Scholar 

  46. Bal, W., Lukszo, J., and Kasprzak, K.S. (1996) Interactions of nickel(II) with histones: Enhancement of 2′-deoxyguanosine oxidation by Ni(II) complexes with CH3CO-Cys-Ala-Ile-His-NH2, a putative metal binding sequence of histone H3, Chem. Res. Toxicol. 9, 535–5

    Article  CAS  Google Scholar 

  47. Cotton, F.A., and Wilkinson, G. (1988) Advanced inorganic chemistry, 5th ed. Wiley-Interscience, New York, pp. 748–752.

    Google Scholar 

  48. Saha, N., and Sigel, H. (1982) Ternary complexes in solution as models for enzyme-metal ion-substrate complexes. Comparison of the coordination tendency of imidazole and ammonia toward the binary complexes of Mn(II), Co(II), Ni(II), Cu(II), Zn(II), or Cd(II) and uridine 5′-triphosphate or adenosine 5′-triphosphate, J. Am.Chem. Soc. 104, 4100–4105.

    Article  CAS  Google Scholar 

  49. Kasprzak, K.S., and Hernandez, L. (1989) Enhancement of hydroxylation and deglycosylation of 2′-deoxyguanosine by carcinogenic nickel compounds, Cancer Res. 49, 5964–5968.

    CAS  Google Scholar 

  50. Datta, A.K., Riggs, C.W., Fivash, Jr., M.J., and Kasprzak, K.S. (1991) Mechanisms of nickel carcinogenesis. Interaction of Ni(II) with 2′-deoxynucleosides and 2′-deoxynucleotides, Chem.-Biol. Interact. 79, 323–334.

    Article  CAS  Google Scholar 

  51. Datta, A.K., North, S.L., and Kasprzak, K.S. (1994) Effect of nickel(II) and tetraglycine on hydroxylation of the guanine moiety in 2′-deoxyguanosine, DNA, and nucleohistone by hydrogen peroxide, Sci. Total Environ. 148, 207–216.

    Article  CAS  Google Scholar 

  52. Kasprzak, K.S., North, S.L., Datta, A.K., and Bal, W. (1995) Enhancement by cysteine and some other natural amino acid ligands of nickel(II)-mediated oxidation of free 2′-deoxyguanosine with H2O2, The Toxicologist 15, 28.

    Google Scholar 

  53. Nackerdien, Z., Kasprzak, K.S., Rao, G., Halliwell, B., and Dizdaroglu, M. (1991) Nickel(II)-and cobalt(II)-dependent damage by hydrogen peroxide to the DNA bases in isolated human chromatin, Cancer Res. 51, 5837–5842.

    CAS  Google Scholar 

  54. Munday, R. (1994) Bioactivation of thiols by one-electron oxidation. Adv. Pharmacol. 27, 237–270.

    Article  CAS  Google Scholar 

  55. Cotelle, N., Tremolieres, E., Bernier, J.L., Catteau, J.P., and Henichart, J.P. (1992) Redox chemistry of complexes of nickel(II) with some biologically important peptides in the presence of reduced oxygen species: an ESR study. J. Inorg. Biochem. 46, 7–15.

    Article  CAS  Google Scholar 

  56. Bal, W., Djuran, M.I., Margerum, D.W., Gray, Jr., E.T., Mazid, M.A., Tom, R.T., Nieboer, E., and Sadler, P.J. (1994) Dioxygen-induced decarboxylation and hydroxylation of [NiII(Glycyl-Glycyl-L-Histidine)] occurs via NiIII: X-ray crystal structure of [NiII(Glycyl-Glycyl-α-hydroxy-D, L-Histamine)]3H2O, J. Chem. Soc, Chem. Comm. 1889–1890.

    Google Scholar 

  57. Datta, A.K., Misra, M., North, S.L., and Kasprzak, K.S. (1992) Enhancement by nickel(II) and L-histidine of 2′-deoxyguanosine oxidation with hydrogen peroxide, Carcinogenesis 13, 283–287

    Article  CAS  Google Scholar 

  58. Bal, W. and Kasprzak, K.S., unpublished results.

    Google Scholar 

  59. Mirza, S.A., Pressler, M.A., Kumar, M., Day, R.O., and Maroney, M.J. (1993) Oxidation of nickel thiolate ligands by dioxygen, Inorg. Chem. 32, 977–987.

    Article  CAS  Google Scholar 

  60. Buonomo, R.M., Font, I., Maguire, M.J., Reibenspies, J.H., Tuntulani, T., and Darensbourg, M.Y. (1995) Study of sulfinate and sulfenate complexes derived from the oxygenation of thiolate sulfur in [l, 5-bis(2-mercapto-2-methylpropyl)-l, 5-diazacyclooctanato(2-)nickel(II), J. Am. Chem. Soc, 117, 963–973.

    Article  CAS  Google Scholar 

  61. Bal, W., Moudrianakis, E.N, and Kasprzak, K.S., unpublished results.

    Google Scholar 

  62. Thatcher, T.H., MacGaffey, J., Bowen, J., Horowitz, S., Shapiro, D.L., and Gorovsky, M. (1994) Independent evolutionary origin of histone H3.3-like variants of animals and Tetrahymena, Nucl. Acid Res. 22, 180–186.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1997 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Bal, W., Kasprzak, K.S. (1997). Modeling the Metal Binding Sites in Core Histones: Interactions of Carcinogenic Ni(II) with the -CAIH- Motif of Histone H3. In: Hadjiliadis, N.D. (eds) Cytotoxic, Mutagenic and Carcinogenic Potential of Heavy Metals Related to Human Environment. NATO ASI Series, vol 26. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-5780-3_7

Download citation

  • DOI: https://doi.org/10.1007/978-94-011-5780-3_7

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-94-010-6440-8

  • Online ISBN: 978-94-011-5780-3

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics