Crystal structure of a SLC11 (NRAMP) transporter reveals the basis for transition-metal ion transport (original) (raw)

References

  1. Nevo, Y. & Nelson, N. The NRAMP family of metal-ion transporters. Biochim. Biophys. Acta 1763, 609–620 (2006).
    Article CAS Google Scholar
  2. Montalbetti, N., Simonin, A., Kovacs, G. & Hediger, M.A. Mammalian iron transporters: families SLC11 and SLC40. Mol. Aspects Med. 34, 270–287 (2013).
    Article CAS Google Scholar
  3. Cellier, M.F., Bergevin, I., Boyer, E. & Richer, E. Polyphyletic origins of bacterial Nramp transporters. Trends Genet. 17, 365–370 (2001).
    Article CAS Google Scholar
  4. Vidal, S.M., Malo, D., Vogan, K., Skamene, E. & Gros, P. Natural resistance to infection with intracellular parasites: isolation of a candidate for Bcg. Cell 73, 469–485 (1993).
    Article CAS Google Scholar
  5. Illing, A.C., Shawki, A., Cunningham, C.L. & Mackenzie, B. Substrate profile and metal-ion selectivity of human divalent metal-ion transporter-1. J. Biol. Chem. 287, 30485–30496 (2012).
    Article CAS Google Scholar
  6. Vidal, S.M., Pinner, E., Lepage, P., Gauthier, S. & Gros, P. Natural resistance to intracellular infections: Nramp1 encodes a membrane phosphoglycoprotein absent in macrophages from susceptible (Nramp1 D169) mouse strains. J. Immunol. 157, 3559–3568 (1996).
    CAS PubMed Google Scholar
  7. Gunshin, H. et al. Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 388, 482–488 (1997).
    Article CAS Google Scholar
  8. Beaumont, C. et al. Two new human DMT1 gene mutations in a patient with microcytic anemia, low ferritinemia, and liver iron overload. Blood 107, 4168–4170 (2006).
    Article CAS Google Scholar
  9. Johnson, E.E. & Wessling-Resnick, M. Iron metabolism and the innate immune response to infection. Microbes Infect. 14, 207–216 (2012).
    Article CAS Google Scholar
  10. Shawki, A., Knight, P.B., Maliken, B.D., Niespodzany, E.J. & Mackenzie, B.H. H+-coupled divalent metal-ion transporter-1: functional properties, physiological roles and therapeutics. Curr. Top. Membr. 70, 169–214 (2012).
    Article CAS Google Scholar
  11. Mackenzie, B., Ujwal, M.L., Chang, M.H., Romero, M.F. & Hediger, M.A. Divalent metal-ion transporter DMT1 mediates both H+ -coupled Fe2+ transport and uncoupled fluxes. Pflugers Arch. 451, 544–558 (2006).
    Article CAS Google Scholar
  12. Shawki, A. & Mackenzie, B. Interaction of calcium with the human divalent metal-ion transporter-1. Biochem. Biophys. Res. Commun. 393, 471–475 (2010).
    Article CAS Google Scholar
  13. Au, C., Benedetto, A. & Aschner, M. Manganese transport in eukaryotes: the role of DMT1. Neurotoxicology 29, 569–576 (2008).
    Article CAS Google Scholar
  14. Bressler, J.P., Olivi, L., Cheong, J.H., Kim, Y. & Bannona, D. Divalent metal transporter 1 in lead and cadmium transport. Ann. NY Acad. Sci. 1012, 142–152 (2004).
    Article CAS Google Scholar
  15. Guerinot, M.L. Microbial iron transport. Annu. Rev. Microbiol. 48, 743–772 (1994).
    Article CAS Google Scholar
  16. Makui, H. et al. Identification of the Escherichia coli K-12 Nramp orthologue (MntH) as a selective divalent metal ion transporter. Mol. Microbiol. 35, 1065–1078 (2000).
    Article CAS Google Scholar
  17. Czachorowski, M., Lam-Yuk-Tseung, S., Cellier, M. & Gros, P. Transmembrane topology of the mammalian Slc11a2 iron transporter. Biochemistry 48, 8422–8434 (2009).
    Article CAS Google Scholar
  18. Yamashita, A., Singh, S.K., Kawate, T., Jin, Y. & Gouaux, E. Crystal structure of a bacterial homologue of Na+/Cl−-dependent neurotransmitter transporters. Nature 437, 215–223 (2005).
    Article CAS Google Scholar
  19. Cellier, M.F. Nramp: from sequence to structure and mechanism of divalent metal import. Curr. Top. Membr. 69, 249–293 (2012).
    Article CAS Google Scholar
  20. Cellier, M.F. Nutritional immunity: homology modeling of Nramp metal import. Adv. Exp. Med. Biol. 946, 335–351 (2012).
    Article CAS Google Scholar
  21. Geertsma, E.R. & Dutzler, R. A versatile and efficient high-throughput cloning tool for structural biology. Biochemistry 50, 3272–3278 (2011).
    Article CAS Google Scholar
  22. Pardon, E. et al. A general protocol for the generation of Nanobodies for structural biology. Nat. Protoc. 9, 674–693 (2014).
    Article CAS Google Scholar
  23. Schulze, S., Koster, S., Geldmacher, U., Terwisscha van Scheltinga, A.C. & Kuhlbrandt, W. Structural basis of Na+-independent and cooperative substrate/product antiport in CaiT. Nature 467, 233–236 (2010).
    Article CAS Google Scholar
  24. Ressl, S., Terwisscha van Scheltinga, A.C., Vonrhein, C., Ott, V. & Ziegler, C. Molecular basis of transport and regulation in the Na+/betaine symporter BetP. Nature 458, 47–52 (2009).
    Article CAS Google Scholar
  25. Weyand, S. et al. Structure and molecular mechanism of a nucleobase-cation-symport-1 family transporter. Science 322, 709–713 (2008).
    Article CAS Google Scholar
  26. Faham, S. et al. The crystal structure of a sodium galactose transporter reveals mechanistic insights into Na+/sugar symport. Science 321, 810–814 (2008).
    Article CAS Google Scholar
  27. Gao, X. et al. Structure and mechanism of an amino acid antiporter. Science 324, 1565–1568 (2009).
    Article CAS Google Scholar
  28. Fang, Y. et al. Structure of a prokaryotic virtual proton pump at 3.2 Å resolution. Nature 460, 1040–1043 (2009).
    Article CAS Google Scholar
  29. Krishnamurthy, H. & Gouaux, E. X-ray structures of LeuT in substrate-free outward-open and apo inward-open states. Nature 481, 469–474 (2012).
    Article CAS Google Scholar
  30. Lam-Yuk-Tseung, S., Govoni, G., Forbes, J. & Gros, P. Iron transport by Nramp2/DMT1: pH regulation of transport by 2 histidines in transmembrane domain 6. Blood 101, 3699–3707 (2003).
    Article CAS Google Scholar
  31. Edward, R.A., Whittaker, M.M., Whittaker, J.W., Jameson, G.B. & Baker, E.N. Distinct metal environment in Fe-substituted manganese superoxide dismutatse provides a structural basis of metal specificity. J. Am. Chem. Soc. 120, 9684–9685 (1998).
    Article CAS Google Scholar
  32. Qi, W. & Cowan, J.A. Structural, mechanistic and coordination chemistry of relevance to the biosynthesis of iron-sulfur and related iron cofactors. Coord. Chem. Rev. 255, 688–699 (2011).
    Article CAS Google Scholar
  33. Freisinger, E. & Vasak, M. Cadmium in metallothioneins. Met. Ions. Life Sci. 11, 339–371 (2013).
    Article CAS Google Scholar
  34. Hoch, E. et al. Histidine pairing at the metal transport site of mammalian ZnT transporters controls Zn2+ over Cd2+ selectivity. Proc. Natl. Acad. Sci. USA 109, 7202–7207 (2012).
    Article CAS Google Scholar
  35. Cellier, M. et al. Nramp defines a family of membrane proteins. Proc. Natl. Acad. Sci. USA 92, 10089–10093 (1995).
    Article CAS Google Scholar
  36. Courville, P. et al. Solute carrier 11 cation symport requires distinct residues in transmembrane helices 1 and 6. J. Biol. Chem. 283, 9651–9658 (2008).
    Article CAS Google Scholar
  37. Haemig, H.A. & Brooker, R.J. Importance of conserved acidic residues in mntH, the Nramp homolog of Escherichia coli. J. Membr. Biol. 201, 97–107 (2004).
    Article CAS Google Scholar
  38. Haemig, H.A., Moen, P.J. & Brooker, R.J. Evidence that highly conserved residues of transmembrane segment 6 of Escherichia coli MntH are important for transport activity. Biochemistry 49, 4662–4671 (2010).
    Article CAS Google Scholar
  39. Xu, H., Jin, J., DeFelice, L.J., Andrews, N.C. & Clapham, D.E. A spontaneous, recurrent mutation in divalent metal transporter-1 exposes a calcium entry pathway. PLoS Biol. 2, E50 (2004).
    Article Google Scholar
  40. Iolascon, A. & De Falco, L. Mutations in the gene encoding DMT1: clinical presentation and treatment. Semin. Hematol. 46, 358–370 (2009).
    Article CAS Google Scholar
  41. Courville, P., Chaloupka, R. & Cellier, M.F. Recent progress in structure-function analyses of Nramp proton-dependent metal-ion transporters. Biochem. Cell Biol. 84, 960–978 (2006).
    Article CAS Google Scholar
  42. Forrest, L.R. et al. Mechanism for alternating access in neurotransmitter transporters. Proc. Natl. Acad. Sci. USA 105, 10338–10343 (2008).
    Article CAS Google Scholar
  43. Casadaban, M.J. & Cohen, S.N. Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J. Mol. Biol. 138, 179–207 (1980).
    Article CAS Google Scholar
  44. Kawate, T. & Gouaux, E. Fluorescence-detection size-exclusion chromatography for precrystallization screening of integral membrane proteins. Structure 14, 673–681 2006).
    Article CAS Google Scholar
  45. Van Duyne, G.D., Standaert, R.F., Karplus, P.A., Schreiber, S.L. & Clardy, J. Atomic structures of the human immunophilin FKBP-12 complexes with FK506 and rapamycin. J. Mol. Biol. 229, 105–124 (1993).
    Article CAS Google Scholar
  46. Kabsch, W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 26, 795–800 (1993).
    Article CAS Google Scholar
  47. Collaborative Computational Project, Number 4. The CCP4 Suite: programs for X-ray crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760–763 (1994).
  48. Schneider, T.R. & Sheldrick, G.M. Substructure solution with SHELXD. Acta Crystallogr. D Biol. Crystallogr. 58, 1772–1779 (2002).
    Article Google Scholar
  49. Pape, T. & Schneider, T.R. HKL2MAP: a graphical user interface for phasing with SHELX programs. J. Appl. Crystallogr. 37, 843–844 (2004).
    Article CAS Google Scholar
  50. De La Fortelle, E. & Bricogne, G. Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. Methods Enzymol. 276, 472–494 (1997).
    Article CAS Google Scholar
  51. Cowtan, K. dm: an automated procedure for phase improvement by density modification. Joint CCP4 and ESF-EACBM Newslett. Protein Crystallogr. 31, 34–38 (1994).
    Google Scholar
  52. Jones, T.A., Zou, J.Y., Cowan, S.W. & Kjeldgaard, M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47, 110–119 (1991).
    Article Google Scholar
  53. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126–2132 (2004).
    Article Google Scholar
  54. Brünger, A.T. et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905–921 (1998).
    Article Google Scholar
  55. Adams, P.D. et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr. 58, 1948–1954 (2002).
    Article Google Scholar
  56. McCoy, A.J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658–674 (2007).
    Article CAS Google Scholar
  57. Geertsma, E.R., Nik Mahmood, N.A., Schuurman-Wolters, G.K. & Poolman, B. Membrane reconstitution of ABC transporters and assays of translocator function. Nat. Protoc. 3, 256–266 (2008).
    Article CAS Google Scholar
  58. Keller, S. et al. High-precision isothermal titration calorimetry with automated peak-shape analysis. Anal. Chem. 84, 5066–5073 (2012).
    Article CAS Google Scholar
  59. Lorenz, C., Pusch, M. & Jentsch, T.J. Heteromultimeric CLC chloride channels with novel properties. Proc. Natl. Acad. Sci. USA 93, 13362–13366 (1996).
    Article CAS Google Scholar

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