Skip to main content

Advertisement

SpringerLink
Log in

The structure and function of heavy metal transport P1B-ATPases

  • Published:
BioMetals Aims and scope Submit manuscript

Abstract

P1B-type ATPases transport heavy metals (Cu+, Cu2+, Zn2+, Co2+, Cd2+, Pb2+) across membranes. Present in most organisms, they are key elements for metal homeostasis. P1B-type ATPases contain 6-8 transmembrane fragments carrying signature sequences in segments flanking the large ATP binding cytoplasmic loop. These sequences made possible the differentiation of at least four P1B-ATPase subgroups with distinct metal selectivity: P1B-1: Cu+, P1B-2: Zn2+, P1B-3: Cu2+, P1B-4: Co2+. Mutagenesis of the invariant transmembrane Cys in H6, Asn and Tyr in H7 and Met and Ser in H8 of the Archaeoglobus fulgidus Cu+-ATPase has revealed that their side chains likely coordinate the metals during transport and constitute a central unique component of these enzymes. The structure of various cytoplasmic domains has been solved. The overall structure of those involved in enzyme phosphorylation (P-domain), nucleotide binding (N-domain) and energy transduction (A-domain), appears similar to those described for the SERCA Ca2+-ATPase. However, they show different features likely associated with singular functions of these proteins. Many P1B-type ATPases, but not all of them, also contain a diverse arrangement of cytoplasmic metal binding domains (MBDs). In spite of their structural differences, all N- and C-terminal MBDs appear to control the enzyme turnover rate without affecting metal binding to transmembrane transport sites. In addition, eukaryotic Cu+-ATPases have multiple N-MBD regions that participate in the metal dependent targeting and localization of these proteins. The current knowledge of structure-function relationships among the different P1B-ATPases allows for a description of selectivity, regulation and transport mechanisms. Moreover, it provides a framework to understand mutations in human Cu+-ATPases (ATP7A and ATP7B) that lead to Menkes and Wilson diseases.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Notes

  1. For simplicity P-type ATPases will be referred as P-ATPases, P1B-ATPase, etc.

References

  • Abdel-Ghany SE, Muller-Moule P, Niyogi KK et al (2005) Two P-type ATPases are required for copper delivery in Arabidopsis thaliana chloroplasts. Plant Cell 17:1233–1251

    Article  PubMed  CAS  Google Scholar 

  • Andrés-Colas N, Sancenon V, Rodríguez-Navarro S et al (2006) The Arabidopsis heavy metal P-type ATPase HMA5 interacts with metallochaperones and functions in copper detoxification of roots. Plant J 45:225–236

    Article  PubMed  CAS  Google Scholar 

  • Argüello JM (2003) Identification of ion selectivity determinants in heavy metal transport P1B-type ATPases. J Membr Biol 195:93–108

    Article  PubMed  CAS  Google Scholar 

  • Arnesano F, Banci L, Bertini I et al (2002) Metallochaperones and metal-transporting ATPases: a comparative analysis of sequences and structures. Genome Res 12:255–271

    Article  PubMed  CAS  Google Scholar 

  • Axelsen KB, Palmgren MG (1998) Evolution of substrate specificities in the P-type ATPase superfamily. J Mol Evol 46:84–101

    Article  PubMed  CAS  Google Scholar 

  • Baker-Austin C, Dopson M, Wexler M et al (2005) Molecular insight into extreme copper resistance in the extremophilic archaeon Ferroplasma acidarmanus Fer1. Microbiology 151:2637–2646

    Article  PubMed  CAS  Google Scholar 

  • Bal N, Mintz E, Guillain F et al (2001) A possible regulatory role for the metal-binding domain of CadA, the Listeria monocytogenes Cd2+-ATPase. FEBS Lett 506:249–252

    Article  PubMed  CAS  Google Scholar 

  • Banci L, Bertini I, Ciofi-Baffoni S et al (2002) A new Zinc-protein coordination site in intracellular metal trafficking: Solution structure of the apo and Zn(II) forms of ZntA(46–118). J Mol Biol 323:883–897

    Article  PubMed  CAS  Google Scholar 

  • Banci L, Bertini I, Ciofi-Baffoni S et al (2001) Solution structure of the yeast copper transporter domain Ccc2a in the apo and Cu(I)-loaded states. J Biol Chem 276:8415–8426

    Article  PubMed  CAS  Google Scholar 

  • Bissig KD, Wunderli-Ye H, Duda PW et al (2001) Structure-function analysis of purified Enterococcus hirae CopB copper ATPase: effect of Menkes/Wilson disease mutation homologues. Biochem J 357:217–223

    Article  PubMed  CAS  Google Scholar 

  • Borjigin J, Payne AS, Deng J et al (1999) A novel pineal night-specific ATPase encoded by the Wilson disease gene. J Neurosci 19:1018–1026

    PubMed  CAS  Google Scholar 

  • Bull PC, Cox DW (1994) Wilson disease and Menkes disease: new handles on heavy-metal transport. Trends Genet 10:246–252

    Article  PubMed  CAS  Google Scholar 

  • Bull PC, Thomas GR, Rommens JM et al (1993) The Wilson disease gene is a putative copper transporting P-type ATPase similar to the Menkes gene. Nat Genet 5:327–337

    Article  PubMed  CAS  Google Scholar 

  • Changela A, Chen K, Xue Y et al (2003) Molecular basis of metal-ion selectivity and zeptomolar sensitivity by CueR. Science 301:1383–1387

    Article  PubMed  CAS  Google Scholar 

  • Cox DW, Moore SD (2002) Copper transporting P-Type ATPases and human disease. J Bioenerg Biomembr 34:333–338

    Article  PubMed  CAS  Google Scholar 

  • De Hertogh B, Lantin AC, Baret PV et al (2004) The archaeal P-type ATPases. J Bioenerg Biomembr 36:135–142

    Article  PubMed  Google Scholar 

  • DiDonato M, Narindrasorasak S, Forbes JR et al (1997) Expression, 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

    Article  PubMed  CAS  Google Scholar 

  • Dmitriev O, Tsivkovskii R, Abildgaard F et al (2006) Solution structure of the N-domain of Wilson disease protein: distinct nucleotide-binding environment and effects of disease mutations. Proc Natl Acad Sci USA 103:5302–5307

    Article  PubMed  CAS  Google Scholar 

  • Dutta SJ, Liu J, Hou Z et al (2006) Conserved aspartic acid 714 in transmembrane segment 8 of the ZntA subgroup of P1B-type ATPases is a metal-binding residue. Biochemistry 45:5923–5931

    Article  PubMed  CAS  Google Scholar 

  • Eng BH, Guerinot ML, Eide D et al (1998) Sequence analyses and phylogenetic characterization of the ZIP family of metal ion transport proteins. J Membr Biol 166:1–7

    Article  PubMed  CAS  Google Scholar 

  • Eren E, Argüello JM (2004) Arabidopsis HMA2, a divalent heavy metal-transporting PIB-type ATPase, is involved in cytoplasmic Zn2+ homeostasis. Plant Physiol 136:3712–3723

    Article  PubMed  CAS  Google Scholar 

  • Fan B, Rosen BP (2002) Biochemical characterization of CopA, the Escherichia coli Cu(I)- translocating P-type ATPase. J Biol Chem 277:46987–46992

    Article  PubMed  CAS  Google Scholar 

  • Fatemi N, Sarkar B (2002) Structural and functional insights of Wilson disease copper-transporting ATPase. J Bioenerg Biomembr 34:339–349

    Article  PubMed  CAS  Google Scholar 

  • Forbes JR, Hsi G, Cox DW (1999) Role of the copper-binding domain in the copper transport function of ATP7B, the P-type ATPase defective in Wilson disease. J Biol Chem 274:12408–12413

    Article  PubMed  CAS  Google Scholar 

  • Gitschier J, Moffat B, Reilly D et al (1998) Solution structure of the fourth metal-binding domain from the Menkes copper-transporting ATPase. Nat Struct Biol 5:47–54

    Article  PubMed  CAS  Google Scholar 

  • Hamza I, Schaefer M, Klomp LW et al (1999) Interaction of the copper chaperone HAH1 with the Wilson disease protein is essential for copper homeostasis. Proc Natl Acad Sci USA 96:13363–13368

    Article  PubMed  CAS  Google Scholar 

  • Haupt M, Bramkamp M, Coles M et al (2004) Inter-domain montions of the N-domain of the KdpFABC commplex, a P-type ATPase, are not driven by ATP-induced conformational changes. J Mol Biol 342:1547–1558

    Article  PubMed  CAS  Google Scholar 

  • Hou ZJ, Narindrasorasak S, Bhushan B et al (2001) Functional analysis of chimeric proteins of the Wilson Cu(I)-ATPase (ATP7B) and ZntA, a Pb(II)/Zn(II)/Cd(II)-ATPase from Escherichia coli. J Biol Chem 276:40858–40863

    Article  PubMed  CAS  Google Scholar 

  • Huffman DL, O’Halloran TV (2000) Energetics of copper trafficking between the Atx1 metallochaperone and the intracellular copper transporter, Ccc2. J Biol Chem 275:18611–18614

    Article  PubMed  CAS  Google Scholar 

  • Hung IH, Suzuki M, Yamaguchi Y et al (1997) Biochemical characterization of the Wilson disease protein and functional expression in the yeast Saccharomyces cerevisiae. J Biol Chem 272:21461–21466

    Article  PubMed  CAS  Google Scholar 

  • Hussain D, Haydon MJ, Wang Y et al (2004) P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell 16:1327–1339

    Article  PubMed  CAS  Google Scholar 

  • Jensen PY, Bonander N, Máller LB et al (1999) Cooperative binding of copper(I) to the metal binding domains in Menkes disease protein. Biochim Biophys Acta 1434:103–113

    PubMed  CAS  Google Scholar 

  • Kahn D, David M, Domergue O et al (1989) Rhizobium meliloti fixGHI sequence predicts involvement of a specific cation pump in symbiotic nitrogen fixation. J Bacteriol 171:929–939

    PubMed  CAS  Google Scholar 

  • Kaplan JH (2002) Biochemistry of Na,K-ATPase. Annu Rev Biochem 71:511–535

    Article  PubMed  CAS  Google Scholar 

  • Larin D, Mekios C, Das K et al (1999) Characterization of the interaction between the Wilson and Menkes disease proteins and the cytoplasmic copper chaperone, HAH1p. J Biol Chem 274:28497–28504

    Article  PubMed  CAS  Google Scholar 

  • Lingrel JB, Croyle ML, Woo AL et al (1998) Ligand binding sites of Na,K-ATPase. Acta Physiol Scand Suppl 643:69–77

    PubMed  CAS  Google Scholar 

  • Liu J, Dutta SJ, Stemmler AJ et al (2006) Metal-binding affinity of the transmembrane site in ZntA: implications for metal selectivity. Biochemistry 45:763–772

    Article  PubMed  CAS  Google Scholar 

  • Liu J, Stemmler AJ, Fatima J et al (2005) Metal-binding characteristics of the amino-terminal domain of ZntA: binding of lead is different compared to cadmium and zinc. Biochemistry 44:5159–5167

    Article  PubMed  CAS  Google Scholar 

  • Loudianos G, Dessi V, Lovicu M et al (1999) Mutation analysis in patients of mediterranean descent with Wilson disease: identification of 19 novel mutations. J Med Genet 36:833–836

    PubMed  CAS  Google Scholar 

  • Lowe J, Vieyra A, Catty P et al (2004) A mutational study in the transmembrane domain of Ccc2p, the yeast Cu(I)-ATPase, shows different roles for each Cys-Pro-Cys cysteine. J Biol Chem 279:25986–25994

    Article  PubMed  CAS  Google Scholar 

  • Lutsenko S, Kaplan JH (1995) Organization of P-type ATPases: Significance of structural diversity. Biochemistry 34:15607–15613

    Article  PubMed  CAS  Google Scholar 

  • Lutsenko S, Petrukhin K, Cooper MJ et al (1997) N-terminal domains of human copper-transporting adenosine triphosphatases (the Wilson’s and Menkes disease proteins) bind copper selectively in vivo and in vitro with stoichiometry of one copper per metal-binding repeat. J Biol Chem 272:18939–18944

    Article  PubMed  CAS  Google Scholar 

  • Lutsenko S, Tsivkovskii R, Walker JM (2003) Functional properties of the human copper-transporting ATPase ATP7B (the Wilson’s disease protein) and regulation by metallochaperone Atox1. Ann N Y Acad Sci 986:204–211

    Article  PubMed  CAS  Google Scholar 

  • MacLennan DH, Rice WJ, Green NM (1997) The mechanism of Ca2+ transport by sarco(endo)plasmic reticulum Ca2+-ATPases. J Biol Chem 272:28815–28818

    Article  PubMed  CAS  Google Scholar 

  • Mana-Capelli S, Mandal AK, Argüello JM (2003) Archaeoglobus fulgidus CopB is a thermophilic Cu2+-ATPase. Functional role of its Histidine-rich N-terminal metal binding domain. J Biol Chem 278:40534–40541

    Article  PubMed  CAS  Google Scholar 

  • Mandal AK, Argüello JM (2003) Functional roles of metal binding domains of the Archaeoglobus fulgidus Cu+ ATPase CopA. Biochemistry 42:11040–11047

    Article  PubMed  CAS  Google Scholar 

  • Mandal AK, Cheung WD, Argüello JM (2002) Characterization of a thermophilic P-type Ag+/Cu+-ATPase from the extremophile Archaeoglobus fulgidus. J Biol Chem 277:7201–7208

    Article  PubMed  CAS  Google Scholar 

  • Mandal AK, Yang Y, Kertesz TM et al (2004) Identification of the transmembrane metal binding site in Cu+-transporting PIB-type ATPases. J Biol Chem 279:54802–54807

    Article  PubMed  CAS  Google Scholar 

  • Martell E, Smith R (2004) NIST Critical Stability Constants of Metal Complexes. National Institute of Standards and Technology (NIST) Standard Reference Database 46

  • Melchers K, Weitzenegger T, Buhmann A et al (1996) Cloning and membrane topology of a P type ATPase from Helicobacter pylori. J Biol Chem 271:446–457

    Article  PubMed  CAS  Google Scholar 

  • Mitra B, Sharma R (2001) The 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

    Article  PubMed  CAS  Google Scholar 

  • Morgan CT, Tsivkovskii R, Kosinsky YA et al (2004) The distinct functional properties of the nucleotide-binding domain of ATP7B, the human copper-transporting ATPase: analysis of the Wilson disease mutations E1064A, H1069Q, R1151H, and C1104F. J Biol Chem 279:36363–36371

    Article  PubMed  CAS  Google Scholar 

  • Nucifora G, Chu L, Misra TK et al (1989) Cadmium resistance from Staphylococcus aureus plasmid pI258 cadA gene results from a cadmium-efflux ATPase. Proc Natl Acad Sci USA 86:3544–3548

    Article  PubMed  CAS  Google Scholar 

  • Odermatt A, Suter H, Krapf R et al (1993) Primary structure of two P-type ATPases involved in copper homeostasis in Enterococcus hirae. J Biol Chem 268:12775–12779

    PubMed  CAS  Google Scholar 

  • Okkeri J, Haltia T (1999) Expression and mutagenesis of ZntA, a zinc-transporting P-type ATPase from Escherichia coli. Biochemistry 38:14109–14116

    Article  PubMed  CAS  Google Scholar 

  • Okkeri J, Laakkonen L, Haltia T (2004) The nucleotide-binding domain of the Zn2+-transporting P-type ATPase from Escherichia coli carries a glycine motif that may be involved in binding of ATP. Biochem J 377:95–105

    Article  PubMed  CAS  Google Scholar 

  • Olesen C, Sørensen TL, Nielsen RC et al (2004) Dephosphorylation of the calcium pump coupled to counterion occlusion. Science 306:2251–2255

    Article  PubMed  CAS  Google Scholar 

  • Outten CE, O’Halloran TV (2001) Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science 292:2488–2492

    Article  PubMed  CAS  Google Scholar 

  • Paulsen IT, Saier MH Jr (1997) A novel family of ubiquitous heavy metal ion transport proteins. J Membr Biol 156:99–103

    Article  PubMed  CAS  Google Scholar 

  • Petris MJ, Mercer JF, Culvenor JG et al (1996) Ligand-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

    PubMed  CAS  Google Scholar 

  • Phung LT, Ajlani G, Haselkorn R (1994) P-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

    Article  PubMed  CAS  Google Scholar 

  • Rensing C, Fan B, Sharma R et al (2000) CopA: An Escherichia coli Cu(I)-translocating P-type ATPase. Proc Natl Acad Sci USA 97:652–656

    Article  PubMed  CAS  Google Scholar 

  • Rensing C, Ghosh M, Rosen BP (1999) Families of soft-metal-ion-transporting ATPases. J Bacteriol 181:5891–5897

    PubMed  CAS  Google Scholar 

  • Rensing C, Mitra B, Rosen BP (1997) The zntA gene of Escherichia coli encodes a Zn(II)-translocating P-type ATPase. Proc Natl Acad Sci USA 94:14326–14331

    Article  PubMed  CAS  Google Scholar 

  • Rosenzweig AC, Huffman DL, Hou MY et al (1999) Crystal structure of the Atx1 metallochaperone protein at 1.02 A resolution. Structure 7:605–617

    Article  PubMed  CAS  Google Scholar 

  • Rutherford JC, Cavet JS, Robinson NJ (1999) Cobalt-dependent transcriptional switching by a dual-effector MerR-like protein regulates a cobalt-exporting variant CPx-type ATPase. J Biol Chem 274:25827–25832

    Article  PubMed  CAS  Google Scholar 

  • Sazinsky MH, Argüello JM, Rosenzweig AC (2006a) Structure of the actuator domain from the Archaeoglobus fulgidus Cu+-ATPase. Biochemistry 45:9949–9955

    Article  CAS  Google Scholar 

  • Sazinsky MH, Mandal AK, Argüello JM et al (2006b) Structure of the ATP Binding Domain from the Archaeoglobus fulgidus Cu+-ATPase. J Biol Chem 281:11161–11166

    Article  CAS  Google Scholar 

  • Schaefer M, Hopkins RG, Failla ML, et al (1999) Hepatocyte-specific localization and copper-dependent trafficking of the Wilson’s disease protein in the liver. Am J Physiol 276:G639–G646

    PubMed  CAS  Google Scholar 

  • Seigneurin-Berny D, Gravot A, Auroy P et al (2006) HMA1, a new Cu-ATPase of the chloroplast envelope, is essential for growth under adverse light conditions. J Biol Chem 281:2882–2892

    Article  PubMed  CAS  Google Scholar 

  • Sharma R, Rensing C, Rosen BP et al (2000) The ATP hydrolytic activity of purified ZntA, a Pb(II)/Cd(II)/Zn(II)-translocating ATPase from Escherichia coli. J Biol Chem 275:3873–3878

    Article  PubMed  CAS  Google Scholar 

  • Solioz M, Vulpe C (1996) CPx-type ATPases: a class of P-type ATPases that pump heavy metals. Trends Biochem Sci 21:237–241

    PubMed  CAS  Google Scholar 

  • Sørensen TL, Møller JV, Nissen P (2004) Phosphoryl transfer and calcium ion occlusion in the calcium pump. Science 304:1672–1675

    Article  PubMed  CAS  Google Scholar 

  • Tottey S, Rich PR, Rondet SA et al (2001) Two Menkes-type atpases supply copper for photosynthesis in Synechocystis PCC 6803. J Biol Chem 276:19999–20004

    Article  PubMed  CAS  Google Scholar 

  • Toyoshima C, Inesi G (2004) Structural basis of ion pumping by Ca2+-ATPase of the sarcoplasmic reticulum. Annu Rev Biochem 73:269–292

    Article  PubMed  CAS  Google Scholar 

  • Toyoshima C, Nakasako M, Nomura H et al (2000) Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 Å. Nature 405:647–655

    Article  PubMed  CAS  Google Scholar 

  • Toyoshima C, Nomura H (2002) Structural changes in the calcium pump accompanying the dissociation of calcium. Nature 418:605–611

    Article  PubMed  CAS  Google Scholar 

  • Toyoshima C, Nomura H, Tsuda T (2004) Lumenal gating mechanism revealed in calcium pump crystal structures with phosphate analogues. Nature 432:361–368

    Article  PubMed  CAS  Google Scholar 

  • Tsai KJ, Lin YF, Wong MD et al (2002) Membrane topology of the p1258 CadA Cd(II)/Pb(II)/Zn(II)-translocating P-type ATPase. J Bioenerg Biomembr 34:147–156

    Article  PubMed  CAS  Google Scholar 

  • Tsivkovskii R, Efremov RG, Lutsenko S (2003) The role of the invariant His-1069 in folding and function of the Wilson’s disease protein, the human copper-transporting ATPase ATP7B. J Biol Chem 278:13302–13308

    Article  PubMed  CAS  Google Scholar 

  • Tsivkovskii R, Eisses JF, Kaplan JH et al (2002) Functional properties of the copper-transporting ATPase ATP7B (the Wilson’s disease protein) expressed in insect cells. J Biol Chem 277:976–983

    Article  PubMed  CAS  Google Scholar 

  • Tsivkovskii R, MacArthur BC, Lutsenko S (2001) The Lys1010-Lys1325 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

    Article  PubMed  CAS  Google Scholar 

  • Verret F, Gravot A, Auroy P et al (2004) Overexpression of AtHMA4 enhances root-to-shoot translocation of zinc and cadmium and plant metal tolerance. FEBS Lett 576:306–312

    Article  PubMed  CAS  Google Scholar 

  • Voskoboinik I, Brooks H, Smith S et al (1998) ATP-dependent copper transport by the Menkes protein in membrane vesicles isolated from cultured Chinese hamster ovary cells. FEBS Lett 435:178–182

    Article  PubMed  CAS  Google Scholar 

  • Voskoboinik I, Mar J, Strausak D et al (2001) The 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

    Article  PubMed  CAS  Google Scholar 

  • Voskoboinik I, Strausak D, Greenough M et al (1999) Functional 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

    Article  PubMed  CAS  Google Scholar 

  • Vulpe C, Levinson B, Whitney S et al (1993) Isolation of a candidate gene for Menkes disease and evidence that it encodes a copper-transporting ATPase. Nat Genet 3:7–13

    Article  PubMed  CAS  Google Scholar 

  • Walker JM, Huster D, Ralle M et al (2004) The N-terminal metal-binding site 2 of the Wilson’s Disease Protein plays a key role in the transfer of copper from Atox1. J Biol Chem 279:15376–15384

    Article  PubMed  CAS  Google Scholar 

  • Walker JM, Tsivkovskii R, Lutsenko S (2002) Metallochaperone Atox1 transfers copper to the NH2-terminal domain of the Wilson’s disease protein and regulates its catalytic activity. J Biol Chem 277:27953–27959

    Article  PubMed  CAS  Google Scholar 

  • Wernimont AK, Huffman DL, Lamb AL et al (2000) Structural basis for copper transfer by the metallochaperone for the Menkes/Wilson disease proteins. Nature Struct Biol 7:766–771

    Article  PubMed  CAS  Google Scholar 

  • Williams LE, Mills RF (2005) P1B-ATPases–an ancient family of transition metal pumps with diverse functions in plants. Trends Plant Sci 10:491–502

    Article  PubMed  CAS  Google Scholar 

  • Wimmer R, Herrmann T, Solioz M et al (1999) NMR structure and metal interactions of the CopZ copper chaperone. J Biol Chem 274:22597–22603

    Article  PubMed  CAS  Google Scholar 

  • Woeste KE, Kieber JJ (2000) A 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

    Article  PubMed  CAS  Google Scholar 

  • Yoshimizu T, Omote H, Wakabayashi T et al (1998) Essential Cys-Pro-Cys motif of Caenorhabditis elegans copper transport ATPase. Biosci Biotechnol Biochem 62:1258–1260

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Matt Sazinsky, Danielle DeOssie, and Amy Rosenzweig for critical reading of this manuscript. This work was supported by NSF grant MCM-0235165 (J. M. A.).

Author information

Authors and Affiliations

  1. Department of Chemistry and Biochemistry, Worcester Polytechnic Institute, 100 Institute Rd., Worcester, MA, 01609, USA

    José M. Argüello, Elif Eren & Manuel González-Guerrero

Authors
  1. José M. Argüello
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elif Eren
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Manuel González-Guerrero
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to José M. Argüello.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Argüello, J.M., Eren, E. & González-Guerrero, M. The structure and function of heavy metal transport P1B-ATPases. Biometals 20, 233–248 (2007). https://doi.org/10.1007/s10534-006-9055-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10534-006-9055-6

Keywords

Search

Navigation