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Identification of Ion-Selectivity Determinants in Heavy-Metal Transport P1B-type ATPases

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Abstract

P1B-type ATPases transport a variety of metals (Cd2+, Zn2+, Pb2+, Co2+, Cu2+, Ag+, Cu+) across biomembranes. Characteristic sequences CP[C/H/S] in transmembrane fragment H6 were observed in the putative transporting metal site of the founding members of this subfamily (initially named CPx-ATPases). In spite of their importance for metal homeostasis and biotolerance, their mechanisms of ion selectivity are not understood. Studies of better-characterized PII-type ATPases (Ca-ATPase and Na,K-ATPase) have identified three transmembrane segments that participate in ion binding and transport. Testing the hypothesis that metal specificity is determined by conserved amino acids located in the equivalent transmembrane segments of P1B-type ATPases (H6, H7, and H8), 234 P1B-ATPase protein sequences were analyzed. This showed that although H6 contains characteristic CPX or XPC sequences, conserved amino acids in H7 and H8 provide signature sequences that predict the metal selectivity in each of five P1B-ATPase subgroups identified. These invariant amino acids contain diverse side chains (thiol, hydroxyl, carbonyl, amide, imidazolium) that can participate in transient metal coordination during transport and consequently determine the particular metal selectivity of each enzyme. Each subgroup shares additional structural characteristics such as the presence (or absence) of particular amino-terminal metal-binding domains and the number of putative transmembrane segments. These differences suggest unique functional characteristics for each subgroup in addition to their particular metal specificity.

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References

  1. S.F. Altschul W. Gish W. Miller E.W. Myers D.J. Lipman (1990) ArticleTitleBasic local alignment search tool. J. Mol. Biol. 215 403–410 Occurrence Handle10.1006/jmbi.1990.9999 Occurrence Handle1:CAS:528:DyaK3MXitVGmsA%3D%3D Occurrence Handle2231712

    Article  CAS  PubMed  Google Scholar 

  2. A. Anton C. Grosse J. Reissmann T. Pribyl D.H. Nies (1999) ArticleTitleCzcD is a heavy metal ion transporter involved in regulation of heavy metal resistance in Ralstonia sp strain CH34. J. Bacteriol. 181 6876–6881 Occurrence Handle1:CAS:528:DyaK1MXnsFSrtLc%3D Occurrence Handle10559151

    CAS  PubMed  Google Scholar 

  3. J.M. Argüello J.H. Kaplan (1994) ArticleTitleGlutamate 779, an intramembrane carboxyl, is essential for monovalent cation binding by the Na,K-ATPase. J. Biol. Chem. 269 6892–6899 Occurrence Handle7907096

    PubMed  Google Scholar 

  4. J.M. Argüello J.B. Lingrel (1995) ArticleTitleSubstitutions of serine 775 in the alpha subunit of the Na,K-ATPase selectively disrupt K+ high affinity activation without affecting Na+ interaction. J. Biol. Chem. 270 22764–22771 Occurrence Handle10.1074/jbc.270.39.22764 Occurrence Handle7559403

    Article  PubMed  Google Scholar 

  5. J.M. Argüello A.K. Mandal S. Mana-Capelli (2003) Heavy metal transport CPx-ATPases from the thermophile Archaeoglobus fulgidus. P.L. Jørgensen S.J.D. Karlish A.B. Maunsbach (Eds) Na,K-ATPase and Related Cation Pumps: Structure, Function, and Regulatory Mechanisms. Annals of New York Academy of Sciences NY 212–218

    Google Scholar 

  6. J.M. Argüello R.D. Peluffo J. Feng J.B. Lingrel J.R. Berlin (1996) ArticleTitleSubstitution of glutamic 779 with alanine in the Na,K-ATPase alpha subunit removes voltage dependence of ion transport. J. Biol. Chem. 271 24610–24616 Occurrence Handle10.1074/jbc.271.40.24610 Occurrence Handle8798726

    Article  PubMed  Google Scholar 

  7. J.M. Argüello J. Whitis M.C. Cheung J.B. Lingrel et al. (1999) ArticleTitleFunctional role of oxygen-containing residues in the fifth transmembrane segment of the Na,K-ATPase alpha subunit. Arch. Biochem. Biophys. 364 254–263 Occurrence Handle10.1006/abbi.1999.1124 Occurrence Handle10190982

    Article  PubMed  Google Scholar 

  8. F. Arnesano L. Banci I. Bertini S. Ciofi-Baffoni E. Molteni D.L. Huffman T.V. O’Halloran (2002) ArticleTitleMetallochaperones and metal-transporting ATPases: a comparative analysis of sequences and structures. Genome Res. 12 255–271 Occurrence Handle10.1101/gr.196802 Occurrence Handle1:CAS:528:DC%2BD38XhtlKksrY%3D Occurrence Handle11827945

    Article  CAS  PubMed  Google Scholar 

  9. K.B. Axelsen M.G. Palmgren (1998) ArticleTitleEvolution of substrate specificities in the P-type ATPase superfamily. J. Mol. Evol. 46 84–101 Occurrence Handle1:CAS:528:DyaK1cXks1aqsw%3D%3D Occurrence Handle9419228

    CAS  PubMed  Google Scholar 

  10. K.B. Axelsen M.G. Palmgren (2001) ArticleTitleInventory of the superfamily of P-type ion pumps in Arabidopsis. Plant Physiol. 126 696–706 Occurrence Handle10.1104/pp.126.2.696 Occurrence Handle1:CAS:528:DC%2BD3MXks1Gmsrc%3D Occurrence Handle11402198

    Article  CAS  PubMed  Google Scholar 

  11. N. Bal E. Mintz F. Guillain P. Catty (2001) ArticleTitleA possible regulatory role for the metal-binding domain of CadA, the Listeria monocytogenes Cd2+-ATPase. FEBS Lett. 506 249–252 Occurrence Handle10.1016/S0014-5793(01)02927-1 Occurrence Handle1:CAS:528:DC%2BD3MXnsF2gu7s%3D Occurrence Handle11602255

    Article  CAS  PubMed  Google Scholar 

  12. K.D. Bissig H. Wunderli-Ye P.W. Duda M. Solioz (2001) ArticleTitleStructure-function analysis of purified Enterococcus hirae CopB copper ATPase: effect of Menkes/Wilson disease mutation homologues. Biochem. J. 357 217–223 Occurrence Handle10.1042/0264-6021:3570217 Occurrence Handle1:CAS:528:DC%2BD3MXlt1Ojurg%3D Occurrence Handle11415452

    Article  CAS  PubMed  Google Scholar 

  13. N.L. Brown J. Camakaris B.T. Lee T. Williams A.P. Morby J. Parkhill D.A. Rouch (1991) ArticleTitleBacterial resistances to mercury and copper. J. Cell. Biochem. 46 106–114 Occurrence Handle1:CAS:528:DyaK3MXks1yjt7o%3D Occurrence Handle1717500

    CAS  PubMed  Google Scholar 

  14. P.C. Bull D.W. Cox (1994) ArticleTitleWilson disease and Menkes disease: new handles on heavy-metal transport. Trends Genet. 10 246–252 Occurrence Handle10.1016/0168-9525(94)90172-4 Occurrence Handle1:CAS:528:DyaK2cXltlWjs7g%3D Occurrence Handle8091505

    Article  CAS  PubMed  Google Scholar 

  15. P.C. Bull G.R. Thomas J.M. Rommens J.R. Forbes D.W. Cox (1993) ArticleTitleThe Wilson disease gene is a putative copper transporting P-type ATPase similar to the Menkes gene [published erratum appears in Nat. Genet. 1994. 6:214]. Nat. Genet. 5 327–337 Occurrence Handle1:CAS:528:DyaK2cXht1Kns7Y%3D Occurrence Handle8298639

    CAS  PubMed  Google Scholar 

  16. J. Camakaris M.J. Petris L. Bailey P. Shen P. Lockhart T.W. Glover C. Barcroft J. Patton J.F. Mercer (1995) ArticleTitleGene amplification of the Menkes (MNK; ATP7A) P-type ATPase gene of CHO cells is associated with copper resistance and enhanced copper efflux. Hum. Mol. Genet. 4 2117–2123 Occurrence Handle1:CAS:528:DyaK2MXpt1Oqur8%3D Occurrence Handle8589689

    CAS  PubMed  Google Scholar 

  17. J.A. Cowan (1996) Inorganic Biochemistry. An Introduction. Wiley-VCH, Inc. New York, NY

    Google Scholar 

  18. M. DiDonato S. Narindrasorasak J.R. Forbes D.W. Cox B. Sarkar (1997) ArticleTitleExpression, purification, and metal binding properties of the N-terminal domain from the Wilson disease putative copper-transporting ATPase (ATP7B). J. Biol Chem. 272 33279–33282 Occurrence Handle10.1074/jbc.272.52.33279 Occurrence Handle1:CAS:528:DyaK1cXpvVSj Occurrence Handle9407118

    Article  CAS  PubMed  Google Scholar 

  19. T. Dudev Y.L. Lin M. Dudev C. Lim (2003) ArticleTitleFirst-second shell interactions in metal binding sites in proteins: A PDB survey and DFT/CDM calculations. J. Am. Chem. Soc. 125 3168–3180 Occurrence Handle10.1021/ja0209722 Occurrence Handle1:CAS:528:DC%2BD3sXht1Sgt7w%3D Occurrence Handle12617685

    Article  CAS  PubMed  Google Scholar 

  20. R. Dutzler E.B. Campbell M. Cadene B.T. Chait R. MacKinnon (2002) ArticleTitleX-ray structure of a ClC chloride channel at 3.0 A reveals the molecular basis of anion selectivity. Nature 415 287–294 Occurrence Handle10.1038/415287a Occurrence Handle1:CAS:528:DC%2BD38XptlWksA%3D%3D Occurrence Handle11796999

    Article  CAS  PubMed  Google Scholar 

  21. B.H. Eng M.L. Guerinot D. Eide M.H. Saier Jr. (1998) ArticleTitleSequence analyses and phylogenetic characterization of the ZIP family of metal ion transport proteins. J. Membrane Biol. 166 1–7 Occurrence Handle10.1007/s002329900442 Occurrence Handle1:CAS:528:DyaK1cXnsFOls7k%3D

    Article  CAS  Google Scholar 

  22. B. Fan B.P. Rosen (2002) ArticleTitleBiochemical characterization of CopA, the Escherichia coli Cu(I)-translocating P-type ATPase. J. Biol. Chem. 277 46987–46992 Occurrence Handle10.1074/jbc.M208490200 Occurrence Handle1:CAS:528:DC%2BD38XptFSksb0%3D Occurrence Handle12351646

    Article  CAS  PubMed  Google Scholar 

  23. J. Felsenstein (1989) ArticleTitlePHYLIP—Phylogeny Inference Package (Version 3.2). Cladistics 5 164–166

    Google Scholar 

  24. J.J.R. Fraústro da Silva R.J.P. Williams (2001) The Biological Chemistry of the Elements. Oxford University Press New York

    Google Scholar 

  25. A. Gattiker E. Gasteiger A. Bairoch (2002) ArticleTitleScanProsite: a reference implementation of a PROSITE scanning tool. Applied Bioinformatics 1 107–108

    Google Scholar 

  26. J. Gitschier B. Moffat D. Reilly W.I. Wood W.J. Fairbrother (1998) ArticleTitleSolution structure of the fourth metal-binding domain from the Menkes copper-transporting ATPase. Nat. Struct. Biol. 5 47–54 Occurrence Handle1:CAS:528:DyaK1cXjvFKqtw%3D%3D Occurrence Handle9437429

    CAS  PubMed  Google Scholar 

  27. I. Glynn (1985) The Na+,K+-transporting adenosine triphosphatase. A. Martonosi (Eds) Enzymes of Biological Membranes. Plenum PL New York 35–114

    Google Scholar 

  28. L. Herrmann D. Schwan R. Garner H.L. Mobley R. Haas K.P. Schafer K. Melchers (1999) ArticleTitle Helicobacter pylori cadA encodes an essential Cd(II)-Zn(II)-Co(II) resistance factor influencing urease activity. Mol. Microbiol. 33 524–536 Occurrence Handle10.1046/j.1365-2958.1999.01496.x Occurrence Handle1:CAS:528:DyaK1MXlslSjtbg%3D Occurrence Handle10417643

    Article  CAS  PubMed  Google Scholar 

  29. T. Hirayama J.J. Kieber N. Hirayama M. Kogan P. Guzman S. Nourizadeh J.M. Alonso W.P. Dailey A. Dancis J.R. Ecker (1999) ArticleTitleRESPONSIVE-TO-ANTAGONIST1, a Menkes/Wilson disease-related copper transporter, is required for ethylene signaling in Arabidopsis. Cell 97 383–393 Occurrence Handle1:CAS:528:DyaK1MXjtVKltbo%3D Occurrence Handle10319818

    CAS  PubMed  Google Scholar 

  30. D.L. Huffman T.V. O’Halloran (2000) ArticleTitleEnergetics of copper trafficking between the Atx1 metallochaperone and the intracellular copper transporter, Ccc2. J. Biol. Chem. 275 18611–18614 Occurrence Handle10.1074/jbc.C000172200 Occurrence Handle1:CAS:528:DC%2BD3cXksVGksL8%3D Occurrence Handle10764731

    Article  CAS  PubMed  Google Scholar 

  31. M.N. Hughes (1988) The Inorganic Chemistry of Biological Processes. John Wiley & Sons Ltd. London

    Google Scholar 

  32. I.K. Jordan D.A. Natale E.V. Koonin M.Y. Galperin (2001) ArticleTitleIndependent evolution of heavy metal-associated domains in copper chaperones and copper-transporting atpases. J. Mol. Evol. 53 622–633 Occurrence Handle10.1007/s002390010249 Occurrence Handle1:CAS:528:DC%2BD3MXnvFOltrg%3D Occurrence Handle11677622

    Article  CAS  PubMed  Google Scholar 

  33. T.A. Kuntzweiler J.M. Argüello J.B. Lingrel (1996) ArticleTitleAsp804 and Asp808 in the transmembrane domain of the Na,K-ATPase alpha subunit are cation coordinating residues. J. Biol. Chem. 271 29682–29687 Occurrence Handle10.1074/jbc.271.24.14176 Occurrence Handle1:CAS:528:DyaK28XntFKltLk%3D Occurrence Handle8939901

    Article  CAS  PubMed  Google Scholar 

  34. S. La Fontaine S.D. Firth P.J. Lockhart H. Brooks J. Camakaris J.F. Mercer (1999.) ArticleTitleFunctional analysis of the Menkes protein (MNK) expressed from a cDNA construct. Adv. Exp. Med. Biol. 448 67–82 Occurrence Handle1:CAS:528:DC%2BD3cXitVGmtbc%3D Occurrence Handle10079816

    CAS  PubMed  Google Scholar 

  35. S. Lutsenko J.H. Kaplan (1995) ArticleTitleOrganization of P-type ATPases: Significance of structural diversity. Biochemistry 34 15607–15613 Occurrence Handle1:CAS:528:DyaK2MXpt12rtL4%3D Occurrence Handle7495787

    CAS  PubMed  Google Scholar 

  36. D.H. MacLennan W.J. Rice A. Odermatt N.M. Green (1998) ArticleTitleStructure-function relationships in the Ca2+-binding and translocation domain of SERCA1: physiological correlates in Body disease. Acta Physiol. Scand. Suppl. 643 55–67 Occurrence Handle1:STN:280:DyaK1M%2FgsF2ktA%3D%3D Occurrence Handle9789547

    CAS  PubMed  Google Scholar 

  37. A.K. Mandal W.D. Cheung J.M. Argüello (2002) ArticleTitleCharacterization of a thermophilic P-type Ag+/Cu+-ATPase from the extremophile Archaeoglobus fulgidus. J. Biol. Chem. 277 7201–7208 Occurrence Handle10.1074/jbc.M109964200 Occurrence Handle1:CAS:528:DC%2BD38XitV2lsr4%3D Occurrence Handle11756450

    Article  CAS  PubMed  Google Scholar 

  38. K. Melchers T. Weitzenegger A. Buhmann W. Steinhilber G. Sachs K.P. Schofer (1996) ArticleTitleCloning and membrane topology of a P type ATPase from Helicobacter pylori. J. Biol. Chem. 271 446–457 Occurrence Handle10.1074/jbc.271.1.446 Occurrence Handle1:CAS:528:DyaK28XktFKjtw%3D%3D Occurrence Handle8550601

    Article  CAS  PubMed  Google Scholar 

  39. B. Mitra R. Sharma (2001) ArticleTitleThe cysteine-rich amino-terminal domain of ZntA, a Pb(II)/Zn(II)/Cd(II)-translocating ATPase from Escherichia coli, is not essential for its function. Biochemistry 40 7694–7699 Occurrence Handle10.1021/bi010529o Occurrence Handle1:CAS:528:DC%2BD3MXjvVOhtbg%3D Occurrence Handle11412123

    Article  CAS  PubMed  Google Scholar 

  40. A. Odermatt H. Suter R. Krapf M. Solioz (1993) ArticleTitlePrimary structure of two P-type ATPases involved in copper homeostasis in Enterococcus hirae. J. Biol. Chem. 268 12775–12779 Occurrence Handle1:CAS:528:DyaK3sXltFaitLs%3D Occurrence Handle8048974

    CAS  PubMed  Google Scholar 

  41. H. Ogawa C. Toyoshima (2002) ArticleTitleHomology modeling of the cation binding sites of Na+,K+-ATPase. Proc. Natl. Acad. Sci. USA 99 15977–15982 Occurrence Handle10.1073/pnas.202622299 Occurrence Handle1:CAS:528:DC%2BD38Xps1egu7o%3D Occurrence Handle12461183

    Article  CAS  PubMed  Google Scholar 

  42. J. Okkeri T. Haltia (1999) ArticleTitleExpression and mutagenesis of ZntA, a zinc-transporting P-type ATPase from Escherichia coli. Biochemistry 38 14109–14116 Occurrence Handle10.1021/bi9913956 Occurrence Handle1:CAS:528:DyaK1MXmslClur8%3D Occurrence Handle10529259

    Article  CAS  PubMed  Google Scholar 

  43. M.G. Palmgren K.B. Axelsen (1998) ArticleTitleEvolution of P-type ATPases. Biochim. Biophys. Acta 1365 37–45 Occurrence Handle10.1016/S0005-2728(98)00041-3 Occurrence Handle1:CAS:528:DyaK1cXksFGrtr0%3D Occurrence Handle9693719

    Article  CAS  PubMed  Google Scholar 

  44. I.T. Paulsen M.H. Saier Jr. (1997) ArticleTitleA novel family of ubiquitous heavy metal ion transport proteins. J. Membrane Biol. 156 99–103 Occurrence Handle10.1007/s002329900192 Occurrence Handle1:CAS:528:DyaK2sXitFKqu7g%3D

    Article  CAS  Google Scholar 

  45. R.G. Pearson (1963) ArticleTitleHard and soft acids and bases. J. Am. Chem. Soc. 85 3533–3539 Occurrence Handle1:CAS:528:DyaF2cXksV0%3D

    CAS  Google Scholar 

  46. P.A. Pedersen J.M. Nielsen J.H. Rasmussen P.L. Jorgensen (1998) ArticleTitleContribution to Tl+, K+, and Na+ binding of Asn776, Ser775, Thr774, Thr772, and Tyr771 in cytoplasmic part of fifth transmembrane segment in alpha-subunit of renal Na,K-ATPase. Biochemistry 37 17818–17827 Occurrence Handle10.1021/bi981898w Occurrence Handle1:CAS:528:DyaK1cXns1Cktrc%3D Occurrence Handle9922148

    Article  CAS  PubMed  Google Scholar 

  47. P.A. Pedersen J.H. Rasmussen J.M. Nielsen P.L. Jorgensen (1997) ArticleTitleIdentification of Asp804 and Asp808 as Na+ and K+ coordinating residues in alpha-subunit of renal Na,K-ATPase. FEBS Lett. 400 206–210 Occurrence Handle10.1016/S0014-5793(96)01381-6 Occurrence Handle1:CAS:528:DyaK2sXhs12rtQ%3D%3D Occurrence Handle9001399

    Article  CAS  PubMed  Google Scholar 

  48. P.L. Pedersen E. Carafoli (1987) ArticleTitleIon motive ATPases: I. Ubiquity, properties, and significance to cell function. Trends Biochem. Sci. 12 146–150 Occurrence Handle10.1016/0968-0004(87)90071-5 Occurrence Handle1:CAS:528:DyaL2sXkvFagtr8%3D

    Article  CAS  Google Scholar 

  49. M.J. Petris J.F. Mercer J.G. Culvenor P. Lockhart P.A. Gleeson J. Camakaris (1996) ArticleTitleLigand-regulated transport of the Menkes copper P-type ATPase efflux pump from the Golgi apparatus to the plasma membrane: a novel mechanism of regulated trafficking. Embo J. 15 6084–6095 Occurrence Handle1:CAS:528:DyaK28XnsFKktL0%3D Occurrence Handle8947031

    CAS  PubMed  Google Scholar 

  50. K. Petrukhin S. Lutsenko I. Chernov B.M. Ross J.H. Kaplan T.C. Gilliam (1994) ArticleTitleCharacterization of the Wilson disease gene encoding a P-type copper transporting ATPase: genomic organization, alternative splicing, and structure/function predictions. Hum. Mol. Genet. 3 1647–1656 Occurrence Handle1:CAS:528:DyaK2cXmvFCitLk%3D Occurrence Handle7833924

    CAS  PubMed  Google Scholar 

  51. L.T. Phung G. Ajlani R. Haselkorn (1994) ArticleTitleP-Type Atpase from the cyanobacterium Synechococcus-7942 related to the human Menkes and Wilson disease gene-products. Proc. Natl. Acad. Sci. USA 91 9651–9654 Occurrence Handle1:CAS:528:DyaK2cXmvFCitbk%3D Occurrence Handle7937823

    CAS  PubMed  Google Scholar 

  52. C. Rensing B. Fan R. Sharma B. Mitra B.P. Rosen (2000) ArticleTitleCopA: An Escherichia coli Cu(I)-translocating P-type ATPase. Proc. Natl. Acad. Sci. USA 97 652–656 Occurrence Handle10.1073/pnas.97.2.652 Occurrence Handle1:CAS:528:DC%2BD3cXot1aiuw%3D%3D Occurrence Handle10639134

    Article  CAS  PubMed  Google Scholar 

  53. C. Rensing M. Ghosh B.P. Rosen (1999) ArticleTitleFamilies of soft-metal-ion-transporting ATPases. J. Bacteriol. 181 5891–5897 Occurrence Handle1:CAS:528:DyaK1MXmsVOrtrs%3D Occurrence Handle10498699

    CAS  PubMed  Google Scholar 

  54. C. Rensing B. Mitra B.P. Rosen (1997) ArticleTitleThe zntA gene of Escherichia coli encodes a Zn(II)-translocating P-type ATPase. Proc. Natl. Acad. Sci. USA 94 14326–14331 Occurrence Handle10.1073/pnas.94.26.14326 Occurrence Handle1:CAS:528:DyaK1cXis1OrtA%3D%3D Occurrence Handle9405611

    Article  CAS  PubMed  Google Scholar 

  55. C. Rensing Y. Sun B. Mitra B.P. Rosen (1998) ArticleTitlePb(II)-translocating P-type ATPases. J. Biol. Chem. 273 32614–32617 Occurrence Handle10.1074/jbc.273.49.32614 Occurrence Handle1:CAS:528:DyaK1cXnvFOntLo%3D Occurrence Handle9830000

    Article  CAS  PubMed  Google Scholar 

  56. J.C. Rutherford J.S. Cavet N.J. Robinson (1999) ArticleTitleCobalt-dependent transcriptional switching by a dual-effector MerR-like protein regulates a cobalt-exporting variant CPx-type ATPase. J. Biol. Chem. 274 25827–25832 Occurrence Handle10.1074/jbc.274.36.25827 Occurrence Handle1:CAS:528:DyaK1MXmtVWhsbk%3D Occurrence Handle10464323

    Article  CAS  PubMed  Google Scholar 

  57. M. Schaefer R.G. Hopkins M.L. Failla J.D. Gitlin (1999) ArticleTitleHepatocyte-specific localization and copper-dependent trafficking of the Wilson’s disease protein in the liver. Am. J. Physiol. 276 G639–G646 Occurrence Handle1:CAS:528:DyaK1MXit1Sqs7g%3D Occurrence Handle10070040

    CAS  PubMed  Google Scholar 

  58. R. Sharma C. Rensing B.P. Rosen B. Mitra (2000) ArticleTitleThe ATP hydrolytic activity of purified ZntA, a Pb(II)/Cd(II)/Zn(II)-translocating ATPase from Escherichia coli. J. Biol. Chem. 275 3873–3878 Occurrence Handle10.1074/jbc.275.6.3873 Occurrence Handle1:CAS:528:DC%2BD3cXht12gsrY%3D Occurrence Handle10660539

    Article  CAS  PubMed  Google Scholar 

  59. S. Silver L.T. Phung (1996) ArticleTitleBacterial heavy metal resistance: new surprises. Ann. Rev. Microbiol. 50 753–789 Occurrence Handle10.1146/annurev.micro.50.1.753 Occurrence Handle1:CAS:528:DyaK28XmtFGht78%3D

    Article  CAS  Google Scholar 

  60. M. Solioz J. Camakaris (1997) ArticleTitleAcylphosphate formation by the Menkes copper ATPase. FEBS Lett. 412 165–168 Occurrence Handle10.1016/S0014-5793(97)00770-9 Occurrence Handle1:CAS:528:DyaK2sXks12muro%3D Occurrence Handle9257713

    Article  CAS  PubMed  Google Scholar 

  61. M. Solioz A. Odermatt (1995) ArticleTitleCopper and silver transport by CopB-ATPase in membrane vesicles of Enterococcus hirae. J. Biol. Chem. 270 9217–9221 Occurrence Handle10.1074/jbc.270.9.4349 Occurrence Handle1:CAS:528:DyaK2MXlt1ajtrw%3D Occurrence Handle7721839

    Article  CAS  PubMed  Google Scholar 

  62. M. Solioz C. Vulpe (1996) ArticleTitleCPx-type ATPases: a class of P-type ATPases that pump heavy metals. Trends Biochem. Sci. 21 237–241 Occurrence Handle10.1016/0968-0004(96)20016-7 Occurrence Handle1:CAS:528:DyaK28XksVymsb0%3D Occurrence Handle8755241

    Article  CAS  PubMed  Google Scholar 

  63. E.L.L. Sonnhammer G. von Heijne A. Krogh (2003) A hidden Markov model for predicting transmembrane helices in protein sequences. J. Glasgow T. Littlejohn F. Major R. Lathrop D. Sankoff C. Sensen (Eds) Proc. of Sixth Int. Conf. on Intelligent Systems for Molecular Biology. AAAI Press Menlo Park, CA 175–182

    Google Scholar 

  64. K.J. Sweadner C. Donnet (2001) ArticleTitleStructural similarities of Na,K-ATPase and SERCA, the Ca2+-ATPase of the sarcoplasmic reticulum. Biochem. J. 356 685–704 Occurrence Handle10.1042/0264-6021:3560685 Occurrence Handle1:CAS:528:DC%2BD3MXkvVaqt7k%3D Occurrence Handle11389677

    Article  CAS  PubMed  Google Scholar 

  65. C. Thelwell N.J. Robinson J.S. Turner-Cavet (1998) ArticleTitleAn SmtB-like repressor from Synechocystis PCC 6803 regulates a zinc exporter. Proc. Natl. Acad. Sci. USA. 95 10728–107033 Occurrence Handle10.1073/pnas.95.18.10728 Occurrence Handle1:CAS:528:DyaK1cXlvFWgsbg%3D Occurrence Handle9724772

    Article  CAS  PubMed  Google Scholar 

  66. J.D. Thompson D.G. Higgins T.J. Gibson (1994) ArticleTitleCLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22 4673–4680 Occurrence Handle1:CAS:528:DyaK2MXitlSgu74%3D Occurrence Handle7984417

    CAS  PubMed  Google Scholar 

  67. C. Toyoshima M. Nakasako H. Nomura H. Ogawa (2000) ArticleTitleCrystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 Å resolution. Nature 405 647–655 Occurrence Handle10.1038/35015017 Occurrence Handle1:CAS:528:DC%2BD3cXktlCis74%3D Occurrence Handle10864315

    Article  CAS  PubMed  Google Scholar 

  68. C. Toyoshima H. Nomura (2002) ArticleTitleStructural changes in the calcium pump accompanying the dissociation of calcium. Nature 418 605–611 Occurrence Handle10.1038/nature00944 Occurrence Handle1:CAS:528:DC%2BD38XlvVyltLg%3D Occurrence Handle12167852

    Article  CAS  PubMed  Google Scholar 

  69. K.J. Tsai Y.F. Lin M.D. Wong H.H. Yang H.L. Fu B.P. Rosen (2002) ArticleTitleMembrane topology of the p1258 CadA Cd(II)/Pb(II)/Zn(II)-translocating P-type ATPase. J. Bioenerg. Biomembr. 34 147–156 Occurrence Handle10.1023/A:1016085301323 Occurrence Handle1:CAS:528:DC%2BD38XkvFejs78%3D Occurrence Handle12171064

    Article  CAS  PubMed  Google Scholar 

  70. K.J. Tsai A.L. Linet (1993) ArticleTitleFormation of a phosphorylated enzyme intermediate by the cadA Cd(2+)-ATPase. Arch. Biochem. Biophys. 305 267–270 Occurrence Handle10.1006/abbi.1993.1421 Occurrence Handle1:CAS:528:DyaK3sXmsVChsbg%3D Occurrence Handle8373163

    Article  CAS  PubMed  Google Scholar 

  71. K.J. Tsai K.P. Yoon A.R. Lynn (1992) ArticleTitleATP-dependent cadmium transport by the cadA cadmium resistance determinant in everted membrane vesicles of Bacillus subtilis. J. Bacteriol. 174 116–121 Occurrence Handle1:CAS:528:DyaK38XnvVSmsw%3D%3D Occurrence Handle1530844

    CAS  PubMed  Google Scholar 

  72. R. Tsivkovskii B. MacArthurs S. Lutsenko (2001) ArticleTitleThe Lys(1010)-Lys(1325) fragment of the Wilson’s disease protein binds nucleotides and interacts with the N-terminal domain of this protein in a copper-dependent manner. J. Biol. Chem. 276 2234–2242 Occurrence Handle10.1074/jbc.M003238200 Occurrence Handle1:CAS:528:DC%2BD3MXotVCltQ%3D%3D Occurrence Handle11053407

    Article  CAS  PubMed  Google Scholar 

  73. B. Vilsen J.P. Andersen (1998) ArticleTitleMutation to the glutamate in the fourth membrane segment of Na+,K+-ATPase and Ca2+-ATPase affects cation binding from both sides of the membrane and destabilizes the occluded enzyme forms. Biochemistry 37 10961–10971 Occurrence Handle10.1021/bi9802925 Occurrence Handle1:CAS:528:DyaK1cXkvVylsro%3D Occurrence Handle9692989

    Article  CAS  PubMed  Google Scholar 

  74. I. Voskoboinik H. Brooks S. Smith P. Shen J. Camakaris (1998) ArticleTitleATP-dependent copper transport by the Menkes protein in membrane vesicles isolated from cultured Chinese hamster ovary cells. FEBS Lett. 435 178–182 Occurrence Handle10.1016/S0014-5793(98)01059-X Occurrence Handle1:CAS:528:DyaK1cXmt1emtL8%3D Occurrence Handle9762903

    Article  CAS  PubMed  Google Scholar 

  75. I. Voskoboinik J. Mar D. Strausak J. Camakaris (2001) ArticleTitleThe regulation of catalytic activity of the menkes copper-translocating P-type ATPase. Role of high affinity copper-binding sites. J. Biol. Chem. 276 28620–28627 Occurrence Handle10.1074/jbc.M103532200 Occurrence Handle1:CAS:528:DC%2BD3MXls1Sruro%3D Occurrence Handle11373292

    Article  CAS  PubMed  Google Scholar 

  76. I. Voskoboinik D. Strausak M. Greenough H. Brooks M. Petris S. Smith J.F. Mercer J. Camakaris (1999) ArticleTitleFunctional analysis of the N-terminal CXXC metal-binding motifs in the human Menkes copper-transporting P-type ATPase expressed in cultured mammalian cells. J. Biol. Chem. 274 22008–22012 Occurrence Handle10.1074/jbc.274.31.22008 Occurrence Handle1:CAS:528:DyaK1MXltVymtbw%3D Occurrence Handle10419525

    Article  CAS  PubMed  Google Scholar 

  77. C.D. Vulpe S. Packman (1995) ArticleTitleCellular copper transport. Ann. Rev. Nutr. 10 293–322

    Google Scholar 

  78. L.E. Williams J.K. Pittman J.L. Hall (2000) ArticleTitleEmerging mechanisms for heavy metal transport in plants. Biochim. Biophys. Acta 1465 104–126 Occurrence Handle10.1016/S0005-2736(00)00133-4 Occurrence Handle1:CAS:528:DC%2BD3cXit1Wgtr0%3D Occurrence Handle10748249

    Article  CAS  PubMed  Google Scholar 

  79. K.E. Woeste J.J. Kieber (2000) ArticleTitleA strong loss-of-function mutation in RAN1 results in constitutive activation of the ethylene response pathway as well as a rosette-lethal phenotype. Plant Cell 12 443–455 Occurrence Handle10.1105/tpc.12.3.443 Occurrence Handle1:CAS:528:DC%2BD3cXktFWju7g%3D Occurrence Handle10715329

    Article  CAS  PubMed  Google Scholar 

  80. T. Yoshimizu H. Omote T. Wakabayashi Y. Sambongi M. Futai (1998) ArticleTitleEssential Cys-Pro-Cys motif of Caenorhabditis elegans copper transport ATPase. Biosci. Biotechnol. Biochem. 62 1258–1260 Occurrence Handle1:CAS:528:DyaK1cXksFCisLo%3D Occurrence Handle9692213

    CAS  PubMed  Google Scholar 

  81. Y. Zhou J.H. Morais-Cabral A. Kaufman R. MacKinnon (2001) ArticleTitleChemistry of ion coordination and hydration revealed by a K+ channel-Fab complex at 2.0 A resolution. Nature 414 43–48 Occurrence Handle10.1038/35102009 Occurrence Handle1:CAS:528:DC%2BD3MXot1Wqsbg%3D Occurrence Handle11689936

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

I thank Kristin Wobbe and Atin Mandal for helpful discussions and critical review of the manuscript, and Win Cheung and Melinda Palma for their assistance with sequence download, file organization and listing. This work was supported by the National Institute of Health Grant R15 GM64419 and American Chemical Society—The Petroleum Research Fund Grant #36628-AC.

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Argüello, J. Identification of Ion-Selectivity Determinants in Heavy-Metal Transport P1B-type ATPases . J. Membrane Biol. 195, 93–108 (2003). https://doi.org/10.1007/s00232-003-2048-2

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