Nucleotide recognition by CopA, a Cu -transporting P-type ATPase

EMBO Journal

Volumn 28, Issue 12, 2009, Pages 1782-1791

  Tsuda, Takeo ^a,b   Toyoshima, Chikashi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b GAKUSHUIN UNIVERSITY   (Japan)

Author keywords

Crystallography; Ion pump; Nucleotide binding mode; Phosphoryl transfer; Wilson disease

Indexed keywords

ADENINE; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATASE P TYPE; ADENOSINE TRIPHOSPHATE; BACTERIAL ENZYME; BETA,GAMMA METHYLENEADENOSINE TRIPHOSPHATE; COPPER EXPORTING ADENOSINE TRIPHOSPHATASE; COPPER ION; GENOMIC DNA; GLYCINE; HISTIDINE; MAGNESIUM ION; NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; ARCHAEAL PROTEIN; CATION TRANSPORT PROTEIN; COPPER TRANSPORTING ATPASES; COPPER-TRANSPORTING ATPASES; MUTANT PROTEIN; PEPTIDE; PROTEIN SUBUNIT;

ARCHAEOGLOBUS FULGIDUS; ARTICLE; BINDING SITE; CRYSTAL STRUCTURE; ENZYME CONFORMATION; HUMAN; ISOTHERMAL TITRATION CALORIMETRY; MOLECULAR CLONING; MOLECULAR RECOGNITION; NONHUMAN; NUCLEOTIDE BINDING DOMAIN; PHOSPHORYLATION DOMAIN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; AMINO ACID SUBSTITUTION; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; ION TRANSPORT; METABOLISM; PROTEIN BINDING; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

ARCHAEA;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; AMINO ACID SUBSTITUTION; ARCHAEAL PROTEINS; ARCHAEOGLOBUS FULGIDUS; BINDING SITES; CATION TRANSPORT PROTEINS; CRYSTALLOGRAPHY, X-RAY; ION TRANSPORT; MODELS, MOLECULAR; MUTANT PROTEINS; PEPTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS;

EID: 67649509594     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2009.143     Document Type: Article

References (47)

1. Argü ello JM (2003) Identification of ion-selectivity determinants in heavy-metal transport P-1B-type ATPases. J Membr Biol 195: 93-108
2. Axelsen KB, Palmgren MG (1998) Evolution of substrate specificities in the P-type ATPase superfamily. J Mol Evol 46: 84-101
3. Bèrneche S, Roux B (2000) Molecular dynamics of the KcsA K+ channel in a bilayer membrane. Biophys J 78: 2900-2917
4. Bissig KD, Wunderli-Ye H, Duda PW, Solioz M (2001) Structurefunction analysis of purified Enterococcus hirae CopB copper ATPase: effect of Menkes/Wilson disease mutation homologues. Biochem J 357: 217-223
5. Brünger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54: 905-921
6. Burroughs AM, Allen KN, Dunaway-Mariano D, Aravind L (2006) Evolutionary genomics of the HAD superfamily: understanding the structural adaptations and catalytic diversity in a superfamily of phosphoesterases and allied enzymes. J Mol Biol 361: 1003-1034
7. Cappello V, Tramontano A, Koch U (2002) Classification of proteins based on the properties of the ligand-binding site: the case of adenine-binding proteins. Proteins 47: 106-115
8. Collaborative Computational Project No. 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50: 760-763
9. Cox DW, Moore SD (2002) Copper transporting P-type ATPases and human disease. J Bioenerg Biomembr 34: 333-338
10. Das SK, Ray K (2006) Wilson's disease: an update. Nat Clin Pract Neurol 2: 482-493
11. Dmitriev O, Tsivkovskii R, Abildgaard F, Morgan CT, Markley JL, Lutsenko S (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
12. González-Guerrero M, Argü ello JM (2008) Mechanism of Cu+- transporting ATPases: soluble Cu+ chaperones directly transfer Cu+ to transmembrane transport sites. Proc Natl Acad Sci USA 105: 5992-5997
13. Hatori Y, Hirata A, Toyoshima C, Lewis D, Pilankatta R, Inesi G (2008) Intermediate phosphorylation reactions in the mechanism of ATP utilization by the copper ATPase (CopA) of Thermotoga maritima. J Biol Chem 283: 22541-22549
14. Hatori Y, Majima E, Tsuda T, Toyoshima C (2007) Domain organization and movements in heavy metal ion pumps: papain digestion of CopA, a Cu+-transporting ATPase. J Biol Chem 282: 25213-25221
15. Haupt M, Bramkamp M, Heller M, Coles M, Deckers-Hebestreit G, Herkenhoff-Hesselmann B, Altendorf K, Kessler H (2006) The holo-form of the nucleotide binding domain of the KdpFABC complex from Escherichia coli reveals a new binding mode. J Biol Chem 281: 9641-9649
16. Kraulis PJ (1991) MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J Appl Crystallogr 24: 946-950
17. Kühlbrandt W (2004) Biology, structure and mechanism of P-type ATPases. Nat Rev Mol Cell Biol 5: 282-295
18. Lübben M, Guldenhaupt J, Zoltner M, Deigwelher K, Haebel P, Urbanke C, Scheidig AJ (2007) Sulfate acts as phosphate analog on the monomeric catalytic fragment of the CPx-ATPase CopB from Suffolobus solfataricus. J Mol Biol 369: 368-385
19. Lübben M, Portmann R, Kock G, Stoll R, Young MM, Solioz M (2009) Structural model of the CopA copper ATPase of Enterococcus hirae based on chemical cross-linking. Biometals 22: 363-375
20. Mandal AK, Argü ello JM (2003) Functional roles of metal binding domains of the Archaeoglobus fulgidus Cu+-ATPase CopA. Biochemistry 42: 11040-11047
21. Marchand A, Winther AM, Holm PJ, Olesen C, Montigny C, Arnou B, Champeil P, Clausen JD, Vilsen B, Andersen JP, Nissen P, Jaxel
22. C, Møller JV, le Maire M (2008) Crystal structure of D351A and P312A mutant forms of the mammalian sarcoplasmic reticulum Ca2+-ATPase reveals key events in phosphorylation and Ca2+ release. J Biol Chem 283: 14867-14882
23. Maruyama K, Clarke DM, Fujii J, Inesi G, Loo TW, MacLennan DH (1989) Functional consequences of alterations to amino acids located in the catalytic center (Isoleucine 348 to Threonine 357) and nucleotide-binding domain of the Ca2+ -ATPase of sarcoplasmic reticulum. J Biol Chem 264: 13038-13042
24. McDonald IK, Thornton JM (1994) Satisfying hydrogen bonding potential in proteins. J Mol Biol 238: 777-793
25. McIntosh DB, Clausen JD, Woolley DG, MacLennan DH, Vilsen B, Andersen JP (2004) Roles of conserved P-domain residues and Mg2+ in ATP binding in the ground and Ca2+-activated states of sarcoplasmic reticulum Ca2+-ATPase. J Biol Chem 279: 32515-32523
26. Morgan CT, Tsivkovskii R, Kosinsky YA, Efremov RG, Lutsenko S (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
27. Morth JP, Pedersen BP, Toustrup-Jensen MS, Sørensen TL, Petersen J, Andersen JP, Vilsen B, Nissen P (2007) Crystal structure of the sodium-potassium pump. Nature 450: 1043-1049
28. Obara K, Miyashita N, Xu C, Toyoshima I, Sugita Y, Inesi G, Toyoshima C (2005) Structural role of countertransport revealed in Ca2+ pump crystal structure in the absence of Ca2+. Proc Natl Acad Sci USA 102: 14489-14496
29. 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
30. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307-325
31. Pedersen BP, Buch-Pedersen MJ, Morth JP, Palmgren MG, Nissen P (2007) Crystal structure of the plasma membrane proton pump. Nature 450: 1111-1114
32. Picard M, Jensen AM, Sørensen TL, Champeil P, Møller JV, Nissen P (2007) Ca2+ versus Mg2+ coordination at the nucleotide-binding site of the sarcoplasmic reticulum Ca2+-ATPase. J Mol Biol 368: 1-7
33. Rice WJ, Kovalishin A, Stokes DL (2006) Role of metal-binding domains of the copper pump from Archaeoglobus fulgidus. Biochem Biophys Res Commun 348: 124-131
34. Rodriguez-Granillo A, Sedlak E, Wittung-Stafshede P (2008) Stability and ATP binding of the nucleotide-binding domain of the Wilson disease protein: effect of the common H1069Q mutation. J Mol Biol 383: 1097-1111
35. Sazinsky MH, Agarwal S, Argü ello JM, Rosenzweig AC (2006a) Structure of the actuator domain from the Archaeoglobus fulgidus Cu+-ATPase. Biochemistry 45: 9949-9955
36. Sazinsky MH, Mandal AK, Argü ello JM, Rosenzweig AC (2006b) Structure of the ATP binding domain from the Archaeoglobus fulgidus Cu+-ATPase. J Biol Chem 281: 11161-11166
37. Shinoda T, Ogawa H, Cornelius F, Toyoshima C (2009) Crystal structure of the sodium-potassium pump at 2.4 A° resolution. Nature (doi:10.1038/nature07939) Thomas GR, Forbes JR, Roberts EA,Walshe JM, Cox DW(1995) The Wilson disease gene: spectrum of mutations and their consequences. Nat Genet 9: 210-217
38. Toyoshima C (2008) Structural aspects of ion pumping by Ca2+- ATPase of sarcoplasmic reticulum. Arch Biochem Biophys 476: 3-11
39. Toyoshima C, Mizutani T (2004) Crystal structure of the calcium pump with a bound ATP analogue. Nature 430: 529-535
40. Toyoshima C, Nakasako M, Nomura H, Ogawa H (2000) Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6A° resolution. Nature 405: 647-655
41. Toyoshima C, Nomura H, Tsuda T (2004) Lumenal gating mechanism revealed in calcium pump crystal structures with phosphate analogues. Nature 432: 361-368
42. 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
43. 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 copperdependent manner. J Biol Chem 276: 2234-2242
44. Walker JE, Saraste M, Runswick MJ, Gay NJ (1982) Distantly related sequences in the a- and b-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1: 945-951
45. Winn MD, Isupov MN, Murshudov GN (2001) Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr D Biol Crystallogr 57: 122-133
46. Wu CC, Rice WJ, Stokes DL (2008) Structure of a copper pump suggests a regulatory role for its metal-binding domain. Structure 16: 976-985
47. Zhou Y, Morais-Cabral JH, Kaufman A, MacKinnon R (2001) Chemistry of ion coordination and hydration revealed by a K+ channel-Fab complex at 2.0A° resolution. Nature 414: 43-48