Nickel and Human Health

  • Barbara Zambelli
  • Stefano CiurliEmail author
Part of the Metal Ions in Life Sciences book series (MILS, volume 13)


This review focuses on the impact of nickel on human health. In particular, the dual nature of nickel as an essential as well as toxic element in nature is described, and the main forms of nickel that can come in contact with living systems from natural sources and anthropogenic activities are discussed. Concomitantly, the main routes of nickel uptake and transport in humans are covered, and the potential dangers that nickel exposure can represent for health are described. In particular, the insurgence of nickel-derived allergies, nickel-induced carcinogenesis as well as infectious diseases caused by human pathogens that rely on nickel-based enzymes to colonize the host are reviewed at different levels, from their macroscopic aspects on human health to the molecular mechanisms underlying these points. Finally, the importance of nickel as a beneficial element for human health, especially being essential for microorganisms that colonize the human guts, is examined.


human health nickel nickel allergy nickel carcinogenesis nickel homeostasis 


  1. 1.
    S. Ciurli, S. Mangani, in Handbook on Metalloproteins, Eds. I. Bertini, A. Sigel, H. Sigel, Marcel Dekker, New York, USA, 2001, pp. 669–708.Google Scholar
  2. 2.
    E. Merian, Toxicol. Envir. Chem. 1984, 8, 9–38.Google Scholar
  3. 3.
    R. G. Garrett, in Metal Ions in Biology and Medicine, Eds J. A. Centeno, P. Collery, G. Fernet, R. B. Finkelman, H. Gibb, J.-C. Etienne; John Libbey Eurotext, Paris, 2000, Vol. 6, pp. 508–510.Google Scholar
  4. 4.
    C. L. Coyle, E. I. Stiefel, in The Bioinorganic Chemistry of Nickel, Ed J. R. Lancaster, Jr., VCH, New York, 1988, pp. 1–28.Google Scholar
  5. 5.
    E. Denkhaus, K. Salnikow, Crit. Rev. Oncol. Hematol. 2002, 42, 35–56.PubMedGoogle Scholar
  6. 6.
    D. G. Barceloux, J. Toxicol. Clin. Toxicol. 1999, 37, 239–258.PubMedGoogle Scholar
  7. 7.
    M. Van Soestbergen, F. W. Sunderman, Jr., Clin. Chem. 1972, 18, 1478–1484.PubMedGoogle Scholar
  8. 8.
    N. Asato, M. Soestbergen, F. W. Sunderman, Jr., Clin. Chem. 1975, 21, 521–527.PubMedGoogle Scholar
  9. 9.
    J. D. Glennon, B. Sarkar, Biochem. J. 1982, 203, 15–23.PubMedCentralPubMedGoogle Scholar
  10. 10.
    F. Torres, M. das Gracas, M. Melo, A. Tosti, Clin. Cosmet. Investig. Dermatol. 2009, 2, 39–48.Google Scholar
  11. 11.
    R. B. Schiffer, F. W. Sunderman, Jr., R. B. Baggs, J. A. Moynihan, J. Neuroimmunol. 1991, 34, 229–239.PubMedGoogle Scholar
  12. 12.
    M. Freitas, P. Barcellos-de-Souza, C. Barja-Fidalgo, E. Fernandes, BioMetals 2013, 26, 13–21.PubMedGoogle Scholar
  13. 13.
    A. Au, J. Ha, M. Hernandez, A. Polotsky, D. S. Hungerford, C. G. Frondoza, J. Biomed. Mater. Res. A 2006, 79, 512–521.PubMedGoogle Scholar
  14. 14.
    M. Anke, A. Trüpschuch, G. Gunstheimer, in Trace Elements in Man and Animals 10, Eds A. M. Roussel, R. A. Anderson, A. E. Favrier, Kluwer Academic, 2002, pp. 685–686.Google Scholar
  15. 15.
    S. G. Schafer, W. Forth, Ecotoxicol. Environ. Saf. 1983, 7, 87–95.PubMedGoogle Scholar
  16. 16.
    J. Tallkvist, A. M. Wing, H. Tjalve, Pharmacol. Toxicol. 1994, 75, 244–249.PubMedGoogle Scholar
  17. 17.
    M. Muller-Fassbender, B. Elsenhans, A. T. McKie, K. Schumann, Toxicology 2003, 185, 141–153.PubMedGoogle Scholar
  18. 18.
    International Agency for Research on Cancer, "Chromium, Nickel and Welding", Proceedings of the Monographs on the Evaluation of Carcenigenic Risks to Humans, Lyon, France, 1990.Google Scholar
  19. 19.
    F. H. Nielsen, D. A. Ollerich, Fed. Proc. 1974, 33, 1767–1772.PubMedGoogle Scholar
  20. 20.
    Y. Li, D. B. Zamble, Chem. Rev. 2009, 109, 4617–4643.PubMedGoogle Scholar
  21. 21.
    M. Yusuf, Q. Fariduddin, S. Hayat, A. Ahmad, Bull. Environ. Contam. Toxicol. 2011, 86, 1–17.PubMedGoogle Scholar
  22. 22.
    EMEA, European Medicines Agency, 2008;
  23. 23.
    K. S. Kasprzak, K. Salnikow, in Nickel and Its Surprising Impact in Nature, Vol. 2 of Metal Ions in Life Sciences, Eds A. Sigel, H. Sigel, R. K. O. Sigel, Wiley, Chichester, 2007, Vol. 2, pp. 581–618.Google Scholar
  24. 24.
    K. S. Kasprzak, F. W. Sunderman, Jr., K. Salnikow, Mutat. Res. 2003, 533, 67–97.PubMedGoogle Scholar
  25. 25.
    H. M. Shen, Q. F. Zhang, Environ. Health Perspect. 1994, 102 (Suppl. 1), 275–282.PubMedCentralPubMedGoogle Scholar
  26. 26.
    A. R. Oller, M. Costa, G. Oberdorster, Toxicol. Appl. Pharmacol. 1997, 143, 152–166.PubMedGoogle Scholar
  27. 27.
    K. A. Biedermann, J. R. Landolph, Cancer Res. 1987, 47, 3815–3823.PubMedGoogle Scholar
  28. 28.
    M. Costa, T. L. Davidson, H. Chen, Q. Ke, P. Zhang, Y. Yan, C. Huang, T. Kluz, Mutat. Res. 2005, 592, 79–88.PubMedGoogle Scholar
  29. 29.
    N. W. Biggart, M. Costa, Mutat. Res. 1986, 175, 209–215.PubMedGoogle Scholar
  30. 30.
    J. B. Little, J. M. Frenial, J. Coppey, Teratog. Carcinog. Mutagen. 1988, 8, 287–292.PubMedGoogle Scholar
  31. 31.
    T. Miura, S. R. Patierno, T. Sakuramoto, J. R. Landolph, Environ. Mol. Mutagen. 1989, 14, 65–78.PubMedGoogle Scholar
  32. 32.
    F. Z. Arrouijal, H. F. Hildebrand, H. Vophi, D. Marzin, Mutagenesis 1990, 5, 583–589.PubMedGoogle Scholar
  33. 33.
    B. Kargacin, C. B. Klein, M. Costa, Mutat. Res. 1993, 300, 63–72.PubMedGoogle Scholar
  34. 34.
    M. Freitas, A. Gomes, G. Porto, E. Fernandes, J. Biol. Inorg. Chem. 2010, 15, 1275–1283.PubMedGoogle Scholar
  35. 35.
    T. J. O’Brien, S. Ceryak, S. R. Patierno, Mutat. Res. 2003, 533, 3–36.PubMedGoogle Scholar
  36. 36.
    B. Desoize, In Vivo 2003, 17, 529–539.PubMedGoogle Scholar
  37. 37.
    A. Hartwig, T. Schwerdtle, Toxicol. Lett. 2002, 127, 47–54.PubMedGoogle Scholar
  38. 38.
    W. Bal, R. Liang, J. Lukszo, S. H. Lee, M. Dizdaroglu, K. S. Kasprzak, Chem. Res. Toxicol. 2000, 13, 616–624.PubMedGoogle Scholar
  39. 39.
    L. Lande-Diner, J. Zhang, T. Hashimshony, A. Goren, I. Keshet, H. Cedar, Cold Spring Harb. Symp. Quant. Biol. 2004, 69, 131–138.PubMedGoogle Scholar
  40. 40.
    Y. W. Lee, C. B. Klein, B. Kargacin, K. Salnikow, J. Kitahara, K. Dowjat, A. Zhitkovich, N. T. Christie, M. Costa, Mol. Cell. Biol. 1995, 15, 2547–2557.PubMedCentralPubMedGoogle Scholar
  41. 41.
    B. Govindarajan, R. Klafter, M. S. Miller, C. Mansur, M. Mizesko, X. Bai, K. LaMontagne, Jr., J. L. Arbiser, Mol. Med. 2002, 8, 1–8.PubMedCentralPubMedGoogle Scholar
  42. 42.
    K. Salnikow, A. Zhitkovich, Chem. Res. Toxicol. 2008, 21, 28–44.PubMedCentralPubMedGoogle Scholar
  43. 43.
    H. Chen, Q. Ke, T. Kluz, Y. Yan, M. Costa, Mol. Cell. Biol. 2006, 26, 3728–3737.PubMedCentralPubMedGoogle Scholar
  44. 44.
    H. Chen, N. C. Giri, R. Zhang, K. Yamane, Y. Zhang, M. Maroney, M. Costa, J. Biol. Chem. 2010, 285, 7374–7383.PubMedCentralPubMedGoogle Scholar
  45. 45.
    R. Martinez-Zamudio, H. C. Ha, Epigenetics 2011, 6, 820–882.PubMedCentralPubMedGoogle Scholar
  46. 46.
    A. A. Karaczyn, F. Golebiowski, K. S. Kasprzak, Chem. Res. Toxicol. 2005, 18, 1934–1942.PubMedGoogle Scholar
  47. 47.
    Q. Zhang, K. Salnikow, T. Kluz, L. C. Chen, W. C. Su, M. Costa, Toxicol. Appl. Pharmacol. 2003, 192, 201–211.PubMedGoogle Scholar
  48. 48.
    C. B. Klein, K. Conway, X. W. Wang, R. K. Bhamra, X. H. Lin, M. D. Cohen, L. Annab, J. C. Barrett, M. Costa, Science 1991, 251, 796–799.PubMedGoogle Scholar
  49. 49.
    S. Orrenius, B. Zhivotovsky, P. Nicotera, Nat. Rev. Mol. Cell. Biol. 2003, 4, 552–565.PubMedGoogle Scholar
  50. 50.
    K. Salnikow, M. Gao, V. Voitkun, X. Huang, M. Costa, Cancer Res. 1994, 54, 6407–6412.PubMedGoogle Scholar
  51. 51.
    W. Bal, A. M. Protas, K. S. Kasprzak, in Metal Ions in Toxicology: Effects, Interactions, Interdependencies, Vol. 8 of Metal Ions in Life Sciences, Eds A. Sigel, H. Sigel, R. K. O. Sigel, Royal Society of Chemistry, Cambridge, 2011, pp. 319–373.Google Scholar
  52. 52.
    K. Salnikow, M. V. Blagosklonny, H. Ryan, R. Johnson, M. Costa, Cancer Res. 2000, 60, 38–41.PubMedGoogle Scholar
  53. 53.
    S. Salceda, J. Caro, J. Biol. Chem. 1997, 272, 22642–22647.PubMedGoogle Scholar
  54. 54.
    W. C. Hon, M. I. Wilson, K. Harlos, T. D. Claridge, C. J. Schofield, C. W. Pugh, P. H. Maxwell, P. J. Ratcliffe, D. I. Stuart, E. Y. Jones, Nature 2002, 417, 975–978.PubMedGoogle Scholar
  55. 55.
    S. J. Freedman, Z. Y. Sun, F. Poy, A. L. Kung, D. M. Livingston, G. Wagner, M. J. Eck, Proc. Natl. Acad. Sci. USA 2002, 99, 5367–5372.PubMedCentralPubMedGoogle Scholar
  56. 56.
    P. Maxwell, K. Salnikow, Cancer Biol. Ther. 2004, 3, 29–35.PubMedGoogle Scholar
  57. 57.
    K. Salnikow, S. P. Donald, R. K. Bruick, A. Zhitkovich, J. M. Phang, K. S. Kasprzak, J. Biol. Chem. 2004, 279, 40337–40344.PubMedGoogle Scholar
  58. 58.
    D. Zhou, K. Salnikow, M. Costa, Cancer Res. 1998, 58, 2182–2189.PubMedGoogle Scholar
  59. 59.
    H. Cangul, K. Salnikow, H. Yee, D. Zagzag, T. Commes, M. Costa, Cell. Biol. Toxicol. 2002, 18, 87–96.PubMedGoogle Scholar
  60. 60.
    T. P. Ellen, Q. Ke, P. Zhang, M. Costa, Carcinogenesis 2008, 29, 2–8.PubMedGoogle Scholar
  61. 61.
    M. A. Zoroddu, M. Peana, T. Kowalik-Jankowska, H. Kozlowski, M. Costa, J. Inorg. Biochem. 2004, 98, 931–939.PubMedGoogle Scholar
  62. 62.
    M. A. Zoroddu, M. Peana, S. Medici, R. Anedda, Dalton Trans. 2009, 5523–5534.Google Scholar
  63. 63.
    J. G. Burchfield, A. J. Lennard, S. Narasimhan, W. E. Hughes, V. C. Wasinger, G. L. Corthals, T. Okuda, H. Kondoh, T. J. Biden, C. Schmitz-Peiffer, J. Biol. Chem. 2004, 279, 18623–18632.PubMedGoogle Scholar
  64. 64.
    J. Hwang, Y. Kim, H. B. Kang, L. Jaroszewski, A. M. Deacon, H. Lee, W. C. Choi, K. J. Kim, C. H. Kim, B. S. Kang, J. O. Lee, T. K. Oh, J. W. Kim, I. A. Wilson, M. H. Kim, J. Biol. Chem. 2011, 286, 12450–12460.PubMedCentralPubMedGoogle Scholar
  65. 65.
    K. Kondo, T. Ozaki, Y. Nakamura, S. Sakiyama, Biochem. Biophys. Res. Commun. 1995, 216, 209–215.PubMedGoogle Scholar
  66. 66.
    K. Kanaya, A. L. Tsai, T. Kamitani, Biochem. Biophys. Res. Commun. 2002, 290, 294–299.PubMedGoogle Scholar
  67. 67.
    S. Oshiro, K. Nozawa, M. Hori, C. Zhang, Y. Hashimoto, S. Kitajima, K. Kawamura, Biochem. Biophys. Res. Commun. 2002, 290, 213–218.PubMedGoogle Scholar
  68. 68.
    C. Harford, B. Sarkar, Biochem. Biophys. Res. Commun. 1995, 209, 877–882.PubMedGoogle Scholar
  69. 69.
    S. F. Martin, P. R. Esser, F. C. Weber, T. Jakob, M. A. Freudenberg, M. Schmidt, M. Goebeler, Allergy 2011, 66, 1152–1163.PubMedGoogle Scholar
  70. 70.
    M. Schmidt, M. Goebeler, J. Mol. Med. (Berl.) 2011, 89, 961–970.Google Scholar
  71. 71.
    P. S. Friedmann, Toxicol. Lett. 2006, 162, 49–54.PubMedGoogle Scholar
  72. 72.
    K. Landsteiner, J. Jacobs, J. Exp. Med. 1935, 61, 643–656.PubMedCentralPubMedGoogle Scholar
  73. 73.
    H. J. Thierse, K. Gamerdinger, C. Junkes, N. Guerreiro, H. U. Weltzien, Toxicology 2005, 209, 101–107.PubMedGoogle Scholar
  74. 74.
    L. Lu, J. Vollmer, C. Moulon, H. U. Weltzien, P. Marrack, J. Kappler, J. Exp. Med. 2003, 197, 567–574.PubMedCentralPubMedGoogle Scholar
  75. 75.
    S. Dai, F. Crawford, P. Marrack, J. W. Kappler, Proc. Natl. Acad. Sci. USA 2008, 105, 11893–11897.PubMedCentralPubMedGoogle Scholar
  76. 76.
    F. Sinigaglia, J. Invest. Dermatol. 1994, 102, 398–401.PubMedGoogle Scholar
  77. 77.
    Y. Wang, S. Dai, Immunol. Res. 2013, 55, 83–90.PubMedGoogle Scholar
  78. 78.
    P. Griem, C. von Vultee, K. Panthel, S. L. Best, P. J. Sadler, C. F. Shaw, 3rd, Eur. J. Immunol. 1998, 28, 1941–1947.PubMedGoogle Scholar
  79. 79.
    K. Gamerdinger, C. Moulon, D. R. Karp, J. Van Bergen, F. Koning, D. Wild, U. Pflugfelder, H. U. Weltzien, J. Exp. Med. 2003, 197, 1345–1353.PubMedCentralPubMedGoogle Scholar
  80. 80.
    O. Wildner, T. Lipkow, J. Knop, Exp. Dermatol. 1992, 1, 191–198.PubMedGoogle Scholar
  81. 81.
    M. Goebeler, G. Meinardus-Hager, J. Roth, S. Goerdt, C. Sorg, J. Invest. Dermatol. 1993, 100, 759–765.PubMedGoogle Scholar
  82. 82.
    M. Goebeler, A. Trautmann, A. Voss, E. V. Brocker, A. Toksoy, R. Gillitzer, Am. J. Pathol. 2001, 158, 431–440.PubMedCentralPubMedGoogle Scholar
  83. 83.
    M. Goebeler, J. Roth, E. B. Brocker, C. Sorg, K. Schulze-Osthoff, J. Immunol. 1995, 155, 2459–2467.PubMedGoogle Scholar
  84. 84.
    M. Goebeler, R. Gillitzer, K. Kilian, K. Utzel, E. B. Brocker, U. R. Rapp, S. Ludwig, Blood 2001, 97, 46–55.PubMedGoogle Scholar
  85. 85.
    M. Schmidt, B. Raghavan, V. Muller, T. Vogl, G. Fejer, S. Tchaptchet, S. Keck, C. Kalis, P. J. Nielsen, C. Galanos, J. Roth, A. Skerra, S. F. Martin, M. A. Freudenberg, M. Goebeler, Nat. Immunol. 2010, 11, 814–819.PubMedGoogle Scholar
  86. 86.
    M. Schmidt, M. Hupe, N. Endres, B. Raghavan, S. Kavuri, P. Geserick, M. Goebeler, M. Leverkus, J. Cell. Mol. Med. 2010, 14, 1760–1776.PubMedGoogle Scholar
  87. 87.
    A. Trautmann, M. Akdis, D. Kleemann, F. Altznauer, H. U. Simon, T. Graeve, M. Noll, E. B. Brocker, K. Blaser, C. A. Akdis, J. Clin. Invest. 2000, 106, 25–35.PubMedCentralPubMedGoogle Scholar
  88. 88.
    S. Rothman, Dermatol. Wochenschr. 1930, 2, 98–99.Google Scholar
  89. 89.
    R. Spiewak, J. Pietowska, K. Curzytek, Expert Rev. Clin. Immunol. 2007, 3, 851–859.PubMedGoogle Scholar
  90. 90.
    T. Menne, K. Rasmussen, Contact Dermatitis 1990, 23, 57–58.PubMedGoogle Scholar
  91. 91.
    J. P. Thyssen, K. Ross-Hansen, T. Menne, J. D. Johansen, Contact Dermatitis 2010, 63, 102–106.PubMedGoogle Scholar
  92. 92.
    Y. Yoshihisa, T. Shimizu, Dermatol. Res. Pract. 2012, 2012, 749561.PubMedCentralPubMedGoogle Scholar
  93. 93.
    E. Mann, U. Ranft, G. Eberwein, D. Gladtke, D. Sugiri, H. Behrendt, J. Ring, T. Schafer, J. Begerow, J. Wittsiepe, U. Kramer, M. Wilhelm, Contact Dermatitis 2010, 62, 355–362.PubMedGoogle Scholar
  94. 94.
    R. Darlenski, J. Kazandjieva, K. Pramatarov, Int. J. Dermatol. 2012, 51, 523–530.PubMedGoogle Scholar
  95. 95.
    J. P. Thyssen, T. Menne, Chem. Res. Toxicol. 2010, 23, 309–318.PubMedGoogle Scholar
  96. 96.
    R. I. Nijhawan, M. Molenda, M. J. Zirwas, S. E. Jacob, Dermatol. Clin. 2009, 27, 355–364,PubMedGoogle Scholar
  97. 97.
    D. Bonamonte, A. Cristaudo, F. Nasorri, T. Carbone, O. De Pita, G. Angelini, A. Cavani, Contact Dermatitis 2011, 65, 293–301.PubMedGoogle Scholar
  98. 98.
    M. Minelli, D. Schiavino, F. Musca, M. E. Bruno, P. Falagiani, G. Mistrello, G. Riva, M. Braga, M. C. Turi, V. Di Rienzo, C. Petrarca, C. Schiavone, M. Di Gioacchino, Int. J. Immunopathol. Pharmacol. 2010, 23, 193–201.PubMedGoogle Scholar
  99. 99.
    Nickel and Its Surprising Impact in Nature, Eds A. Sigel, H. Sigel, R. K. O. Sigel, John Wiley & Sons, Chichester, Met. Ions Life Sci. 2007, 2, pp. 1–702.Google Scholar
  100. 100.
    S. W. Ragsdale, J. Biol. Chem. 2009, 284, 18571–18575.PubMedCentralPubMedGoogle Scholar
  101. 101.
    H. L. Mobley, M. D. Island, R. P. Hausinger, Microbiol. Rev. 1995, 59, 451–480.PubMedCentralPubMedGoogle Scholar
  102. 102.
    S. Wyllie, A. H. Fairlamb, Semin. Cell. Dev. Biol. 2011, 22, 271–277.PubMedCentralPubMedGoogle Scholar
  103. 103.
    N. Sukdeo, E. Daub, J. F. Honek, in Nickel and Its Surprising Impact in Nature, Vol. 2 of Metal Ions in Life Sciences, Eds A. Sigel, H. Sigel, R. K. O Sigel, John Wiley & Sons, Chichester, 2007, pp. 445–472.Google Scholar
  104. 104.
    N. Sukdeo, J. F. Honek, Biochim. Biophys. Acta 2007, 1774, 756–763.PubMedGoogle Scholar
  105. 105.
    T. C. Pochapsky, T. Ju, M. Dang, R. Beaulieu, G. M. Pagani, B. OuYang, in Nickel and Its Surprising Impact in Nature, Vol. 2 of Metal Ions in Life Sciences, Eds A. Sigel, H. Sigel, R. K. O Sigel, John Wiley & Sons, Chichester, 2007, Vol. 2, pp. 473–500.Google Scholar
  106. 106.
    Q. Xu, R. Schwarzenbacher, S. S. Krishna, D. McMullan, S. Agarwalla, K. Quijano, P. Abdubek, E. Ambing, H. Axelrod, T. Biorac, J. M. Canaves, H.-J. Chiu, M.-A. Elsliger, C. Grittini, S. K. Grzechnik, M. DiDonato, J. Hale, E. Hampton, G. W. Han, J. Haugen, M. Hornsby, L. Jaroszewski, H. E. Klock, M. W. Knuth, E. Koesema, A. Kreusch, P. Kuhn, M. D. Miller, K. Moy, E. Nigoghossian, J. Paulsen, R. Reyes, C. Rife, G. Spraggon, R. C. Stevens, H. van den Bedem, J. Velasquez, A. White, G. Wolf, K. O. Hodgson, J. Wooley, A. M. Deacon, A. Godzik, S. A. Lesley, I. A. Wilson, Proteins: Structure, Function, and Bioinformatics 2006, 64, 808–813.Google Scholar
  107. 107.
    T. Ju, R. B. Goldsmith, S. C. Chai, M. J. Maroney, S. S. Pochapsky, T. C. Pochapsky, J. Mol. Biol. 2006, 363, 823–834.PubMedCentralPubMedGoogle Scholar
  108. 108.
    S. Ciurli, in Nickel and Its Surprising Impact in Nature, Vol. 2 of Metal Ions in Life Sciences, Eds A. Sigel, H. Sigel, R. K. O Sigel, Wiley, Chichester, 2007, pp. 241–278.Google Scholar
  109. 109.
    B. Zambelli, F. Musiani, S. Benini, S. Ciurli, Acc. Chem. Res. 2011, 44, 520–530.PubMedGoogle Scholar
  110. 110.
    S. Benini, W. R. Rypniewski, K. S. Wilson, S. Miletti, S. Ciurli, S. Mangani, Structure Fold. Des. 1999, 7, 205–216.PubMedGoogle Scholar
  111. 111.
    F. Musiani, E. Arnofi, R. Casadio, S. Ciurli, J. Biol. Inorg. Chem. 2001, 3, 300–314.Google Scholar
  112. 112.
    S. Benini, W. R. Rypniewski, K. S. Wilson, S. Mangani, S. Ciurli, J. Am. Chem. Soc. 2004, 126, 3714–3715.PubMedGoogle Scholar
  113. 113.
    S. Ciurli, S. Benini, W. R. Rypniewski, K. S. Wilson, S. Miletti, S. Mangani, Coord. Chem. Rev. 1999, 190–192, 331–355.Google Scholar
  114. 114.
    W. Lubitz, M. van Gastel, W. Gartner, Nickel and Its Surprising Impact in Nature, Vol. 2 of Metal Ions in Life Sciences, Eds A. Sigel, H. Sigel, R. K. O Sigel, John Wiley & Sons, Chichester, 2007, pp. 279–322.Google Scholar
  115. 115.
    P. M. Vignais, B. Billoud, Chem. Rev. 2007, 107, 4206–4272.PubMedGoogle Scholar
  116. 116.
    R. J. Maier, Biochem. Soc. Trans. 2005, 33, 83–85.PubMedGoogle Scholar
  117. 117.
    C. Navarro, L.-F. Wu, M.-A. Mandrand-Berthelot, Mol. Microbiol. 1993, 9, 1181–1191.PubMedGoogle Scholar
  118. 118.
    H. Lebrette, M. Iannello, J. C. Fontecilla-Camps, C. Cavazza, J. Inorg. Biochem. 2013, 121, 16–18.PubMedGoogle Scholar
  119. 119.
    L. Macomber, R. P. Hausinger, Metallomics 2011, 3, 1153–1162.PubMedGoogle Scholar
  120. 120.
    D. H. Nies, FEMS Microbiol. Rev. 2003, 27, 313–339.PubMedGoogle Scholar
  121. 121.
    F. N. Stahler, S. Odenbreit, R. Haas, J. Wilrich, A. H. Van Vliet, J. G. Kusters, M. Kist, S. Bereswill, Infect. Immun. 2006, 74, 3845–3852.PubMedCentralPubMedGoogle Scholar
  122. 122.
    A. Rodrigue, G. Effantin, M. A. Mandrand-Berthelot, J. Bacteriol. 2005, 187, 2912–2916.PubMedCentralPubMedGoogle Scholar
  123. 123.
    R. Ge, Y. Zhang, X. Sun, R. M. Watt, Q. Y. He, J. D. Huang, D. E. Wilcox, H. Sun, J. Am. Chem. Soc. 2006, 128, 11330–11331.PubMedGoogle Scholar
  124. 124.
    R. J. Maier, S. L. Benoit, S. Seshadri, BioMetals 2007, 20, 655–664.PubMedCentralPubMedGoogle Scholar
  125. 125.
    Y. B. Zeng, D. M. Zhang, H. Li, H. Sun, J. Biol. Inorg. Chem. 2008, 13, 1121–1131.PubMedGoogle Scholar
  126. 126.
    F. Musiani, B. Zambelli, M. Stola, S. Ciurli, J. Inorg. Biochem. 2004, 98, 803–813.PubMedGoogle Scholar
  127. 127.
    B. Zambelli, F. Musiani, M. Savini, P. Tucker, S. Ciurli, Biochemistry 2007, 46, 3171–3182.PubMedGoogle Scholar
  128. 128.
    R. Real-Guerra, F. Staniscuaski, B. Zambelli, F. Musiani, S. Ciurli, C. R. Carlini, Plant Mol. Biol. 2012, 78, 461–475.PubMedGoogle Scholar
  129. 129.
    J. W. Olson, R. J. Maier, J. Bacteriol. 2000, 182, 1702–1705.PubMedCentralPubMedGoogle Scholar
  130. 130.
    C. Wulfing, J. Lombardero, A. Pluckthun, J. Biol. Chem. 1994, 269, 2895–2901.PubMedGoogle Scholar
  131. 131.
    R. K. Watt, P. W. Ludden, J. Biol. Chem. 1998, 273, 10019–10025.PubMedGoogle Scholar
  132. 132.
    H.-K. Song, S. B. Mulrooney, R. Huber, R. P. Hausinger, J. Biol. Chem. 2001, 276, 49359–49364.PubMedGoogle Scholar
  133. 133.
    H. Remaut, N. Safarov, S. Ciurli, J. Van Beeumen, J. Biol. Chem. 2001, 276, 49365–49370.PubMedGoogle Scholar
  134. 134.
    K. Banaszak, V. Martin-Diaconescu, M. Bellucci, B. Zambelli, W. Rypniewski, M. J. Maroney, S. Ciurli, Biochem. J. 2012, 441, 1017–1026.PubMedCentralPubMedGoogle Scholar
  135. 135.
    N. Mehta, J. W. Olson, R. J. Maier, J. Bacteriol. 2003, 185, 726–734.PubMedCentralPubMedGoogle Scholar
  136. 136.
    H. K. Loke, P. A. Lindahl, J. Inorg. Biochem. 2003, 93, 33–40.PubMedGoogle Scholar
  137. 137.
    R. L. Kerby, P. W. Ludden, G. P. Roberts, J. Bacteriol. 1997, 179, 2259–2266.PubMedCentralPubMedGoogle Scholar
  138. 138.
    P. Neyroz, B. Zambelli, S. Ciurli, Biochemistry 2006, 45, 8918–8930.PubMedGoogle Scholar
  139. 139.
    B. Zambelli, M. Stola, F. Musiani, K. De Vriendt, B. Samyn, B. Devreese, J. Van Beeumen, P. Turano, A. Dikiy, D. A. Bryant, S. Ciurli, J. Biol. Chem. 2005, 280, 4684–4695.PubMedGoogle Scholar
  140. 140.
    B. Zambelli, P. Turano, F. Musiani, P. Neyroz, S. Ciurli, Proteins 2009, 74, 222–239.PubMedGoogle Scholar
  141. 141.
    B. Zambelli, N. Cremades, P. Neyroz, P. Turano, V. N. Uversky, S. Ciurli, Mol. Biosyst. 2012, 8, 220–228.PubMedGoogle Scholar
  142. 142.
    M. Bellucci, B. Zambelli, F. Musiani, P. Turano, S. Ciurli, Biochem. J. 2009, 422, 91–100.PubMedGoogle Scholar
  143. 143.
    Y. H. Fong, H. C. Wong, C. P. Chuck, Y. W. Chen, H. Sun, K. B. Wong, J. Biol. Chem. 2011, 286, 43241–43249.PubMedCentralPubMedGoogle Scholar
  144. 144.
    B. Zambelli, F. Musiani, S. Ciurli, Met. Ions Life Sci. 2012, 10, 135–170.PubMedGoogle Scholar
  145. 145.
    Z. Ma, F. E. Jacobsen, D. P. Giedroc, Chem. Rev. 2009, 109, 4644–4681.PubMedCentralPubMedGoogle Scholar
  146. 146.
    B. Zambelli, M. Bellucci, A. Danielli, V. Scarlato, S. Ciurli, Chem. Commun. 2007, 3649–3651.Google Scholar
  147. 147.
    B. Zambelli, A. Danielli, S. Romagnoli, P. Neyroz, S. Ciurli, V. Scarlato, J. Mol. Biol. 2008, 383, 1129–1143.PubMedGoogle Scholar
  148. 148.
    F. Musiani, B. Bertosa, A. Magistrato, B. Zambelli, P. Turano, V. Losasso, C. Micheletti, S. Ciurli, P. Carloni, J. Chem. Theor. Comp. 2010, 6, 3503–3515.Google Scholar
  149. 149.
    S. Benini, M. Cianci, S. Ciurli, Dalton Trans. 2011, 40, 7831–7833.PubMedGoogle Scholar
  150. 150.
    J. G. Kusters, A. H. van Vliet, E. J. Kuipers, Clin. Microbiol. Rev. 2006, 19, 449–490.PubMedCentralPubMedGoogle Scholar
  151. 151.
    H. de Reuse, S. Bereswill, FEMS Immunol. Med. Microbiol. 2007, 50, 165–176.PubMedGoogle Scholar
  152. 152.
    A. Danielli, G. Amore, V. Scarlato, PLoS Pathog. 2010, 6, e1000938. DOI: 10.371/journal.ppat.1000938.PubMedCentralPubMedGoogle Scholar
  153. 153.
    K. A. Eaton, S. Krakowka, Infect. Immun. 1994, 62, 3604–3607.PubMedCentralPubMedGoogle Scholar
  154. 154.
    K. Muhsen, D. Cohen, Helicobacter 2008, 13, 323–340.PubMedGoogle Scholar
  155. 155.
    S. L. Benoit, E. F. Miller, R. J. Maier, Infect. Immun. 2013, 81, 580–584.PubMedCentralPubMedGoogle Scholar
  156. 156.
    M. Sousa Silva, A. E. Ferreira, R. Gomes, A. M. Tomas, A. Ponces Freire, C. Cordeiro, Int. J. Med. Microbiol. 2012, 302, 225–229.PubMedGoogle Scholar
  157. 157.
    S. C. Chauhan, P. K. Padmanabhan, R. Madhubala, Curr. Drug Targets 2008, 9, 957–965.PubMedGoogle Scholar
  158. 158.
    WHO, "Global tuberculosis control report 2011", World Health Organization, Geneva, Switzerland, 2011.Google Scholar
  159. 159.
    W. Lin, V. Mathys, E. L. Ang, V. H. Koh, J. M. Martinez Gomez, M. L. Ang, S. Z. Zainul Rahim, M. P. Tan, K. Pethe, S. Alonso, Infect. Immun. 2012, 80, 2771–2779.PubMedCentralPubMedGoogle Scholar
  160. 160.
    D. L. Clemens, B. Y. Lee, M. A. Horwitz, J. Bacteriol. 1995, 177, 5644–5652.PubMedCentralPubMedGoogle Scholar
  161. 161.
    A. H. Gordon, P. D. Hart, M. R. Young, Nature 1980, 286, 79–80.PubMedGoogle Scholar
  162. 162.
    P. D. Hart, M. R. Young, J. Exp. Med. 1991, 174, 881–889.PubMedGoogle Scholar
  163. 163.
    K. Sendide, A. E. Deghmane, J. M. Reyrat, A. Talal, Z. Hmama, Infect. Immun. 2004, 72, 4200–4209.PubMedCentralPubMedGoogle Scholar
  164. 164.
    T. Mukai, Y. Maeda, T. Tamura, Y. Miyamoto, M. Makino, FEMS Immunol. Med. Microbiol. 2008, 53, 96–106.PubMedGoogle Scholar
  165. 165.
    L. Grode, P. Seiler, S. Baumann, J. Hess, V. Brinkmann, A. Nasser Eddine, P. Mann, C. Goosmann, S. Bandermann, D. Smith, G. J. Bancroft, J. M. Reyrat, D. van Soolingen, B. Raupach, S. H. Kaufmann, J. Clin. Invest. 2005, 115, 2472–2479.PubMedCentralPubMedGoogle Scholar
  166. 166.
    D. R. Campbell, K. E. Chapman, K. J. Waldron, S. Tottey, S. Kendall, G. Cavallaro, C. Andreini, J. Hinds, N. G. Stoker, N. J. Robinson, J. S. Cavet, J. Biol. Chem. 2007, 282, 32298–32310.PubMedCentralPubMedGoogle Scholar
  167. 167.
    A. Schnegg, M. Kirchgessner, in In Trace Element Metabolism in Man and Animals-3, Ed M. Kirchgessner, Proceedings of the 3rd Intern. Symposium, Technische Universität, Munchen, Germany, 1978, pp. 236–243.Google Scholar
  168. 168.
    F. H. Nielsen, D. R. Myron, S. H. Givand, T. J. Zimmerman, D. A. Ollerich, J. Nutr. 1975, 105, 1620–1630.PubMedGoogle Scholar
  169. 169.
    M. Szilagyi, M. Anke, I. Balogh, Acta Vet. Hung. 1991, 39, 231–238.PubMedGoogle Scholar
  170. 170.
    K. Yokoi, E. O. Uthus, F. H. Nielsen, Biol. Trace Elem. Res. 2003, 93, 141–154.PubMedGoogle Scholar
  171. 171.
    F. H. Nielsen, T. R. Shuler, T. G. McLeod, T. J. Zimmerman, J. Nutr. 1984, 114, 1280–1288.PubMedGoogle Scholar
  172. 172.
    J. W. Spears, R. W. Harvey, L. J. Samsell, J. Nutr. 1986, 116, 1873–1882.PubMedGoogle Scholar
  173. 173.
    G. I. Stangl, M. Kirchgessner, J. Nutr. 1996, 126, 2466–2473.PubMedGoogle Scholar
  174. 174.
    V. Tremaroli, F. Backhed, Nature 2012, 489, 242–249.PubMedGoogle Scholar
  175. 175.
    C. Palmer, E. M. Bik, D. B. DiGiulio, D. A. Relman, P. O. Brown, PLoS Biol. 2007, 5, e177.PubMedCentralPubMedGoogle Scholar
  176. 176.
    P. B. Eckburg, E. M. Bik, C. N. Bernstein, E. Purdom, L. Dethlefsen, M. Sargent, S. R. Gill, K. E. Nelson, D. A. Relman, Science 2005, 308, 1635–1638.PubMedCentralPubMedGoogle Scholar
  177. 177.
    M. Monachese, J. P. Burton, G. Reid, Appl. Environ. Microbiol. 2012, 78, 6397–6404.PubMedCentralPubMedGoogle Scholar
  178. 178.
    K. Suzuki, Y. Benno, T. Mitsuoka, S. Takebe, K. Kobashi, J. Hase, Appl. Environ. Microbiol. 1979, 37, 379–382.PubMedCentralPubMedGoogle Scholar
  179. 179.
    F. Turroni, E. Foroni, P. Pizzetti, V. Giubellini, A. Ribbera, P. Merusi, P. Cagnasso, B. Bizzarri, G. L. de’Angelis, F. Shanahan, D. van Sinderen, M. Ventura, Appl. Environ. Microbiol. 2009, 75, 1534–1545.Google Scholar
  180. 180.
    I. S. Arvanitoyannis, M. Van Houwelingen-Koukaliaroglou, Crit. Rev. Food Sci. Nutr. 2005, 45, 385–404.PubMedGoogle Scholar
  181. 181.
    M. Pimentel, R. P. Gunsalus, S. S. Rao, H. Zhang, Am. J. Gastroenter. Suppl. 2012, 1, 28–33.Google Scholar
  182. 182.
    B. Jaun, R. K. Thauer, in Nickel and Its Surprising Impact in Nature, Vol. 2 of Metal Ions in Life Sciences, Eds A. Sigel, H. Sigel, R. K. O Sigel, John Wiley & Sons, Ltd., Chichester, UK, 2007, pp. 323–356.Google Scholar

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© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Laboratory of Bioinorganic Chemistry, Department of Pharmacy and BiotechnologyUniversity of BolognaBolognaItaly

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