Characterization of the Particulate Methane Monooxygenase Metal Centers in Multiple Redox States by X-ray Absorption Spectroscopy

Lieberman, Raquel L.; Kondapalli, Kalyan C.; Shrestha, Deepak B.; Hakemian, Amanda S.; Smith, Stephen M.; Telser, Joshua; Kuzelka, Jane; Gupta, Rajeev; Borovik, A. S.; Lippard, Stephen J.; Hoffman, Brian M.; Rosenzweig, Amy C.; Stemmler, Timothy L.

doi:10.1021/ic060739v

Cited by 87 publications

(156 citation statements)

References 41 publications

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“…EXAFS fitting analysis was performed on raw/unfiltered data. Protein EXAFS data were fit using single scattering Feff v7 theoretical models, calculated for carbon, oxygen, sulfur, and copper coordination to simulate copper-ligand environments, with values for the scale factors (Sc) and E 0 calibrated by fitting crystallographically characterized copper model compounds, as previously outlined (37). Criteria for judging the best fit EXAFS simulations utilized both the lowest mean square deviation between data and fit corrected for the number of degrees of freedom (FЈ) (38) and reasonable Debye-Waller factors ( 2 Ͻ 0.006 Å 2 ).…”

Section: Methodsmentioning

confidence: 99%

Structure of the Two Transmembrane Cu+ Transport Sites of the Cu+-ATPases

González‐Guerrero

Eren

Rawat

et al. 2008

Journal of Biological Chemistry

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146

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Cu؉ -ATPases drive metal efflux from the cell cytoplasm. Paramount to this function is the binding of Cu ؉ within the transmembrane region and its coupled translocation across the permeability barrier. Copper is an essential micronutrient (1, 2). It has critical catalytic and electron transfer roles in a number of key proteins (tyrosinase, lysyl oxidase, ferroxidase ceruloplasmin, plastocyanin, etc.). However, when free, copper participates in the production of reactive oxygen species leading to cellular damage. Toward sustaining intracellular copper balance, transmembrane transport systems maintain the copper cell quota, Cu ϩ chaperone proteins traffic the bound metal to specific cellular targets, and metal-sensing transcription factors control copper dependent protein expression (3-5). The metal coordination geometry in these proteins is central to the efficiency of the Cu ϩ mobilization processes. In this direction, the coordination should ensure the specificity and prevent the release of free Cu ϩ to the cytoplasm. Canonical copper metalloproteins have long been characterized and classified based on spectroscopic and magnetic properties (Types I, II, and III) (6 -8). Their study has provided great detail on copper coordination in "permanent" sites where copper is bound during the functional life of the proteins. Cu ϩ linear coordination by invariant Cys residues of chaperone proteins has been described, providing insight into the mechanism of copper trafficking and exchange among similar domains (9, 10). More recently, trigonal coordination by Cys 2 -His sites has been observed, for instance, in Mycobacterium tuberculosis transcription factor CsoR (11). Alternatively, Met n His was found in several Cu ϩ -trafficking proteins located in the oxidizing periplasm of prokaryotes (12)(13)(14). Despite this progress, Cu ϩ distribution and balance cannot be understood without describing the selective coordination during compartmental transmembrane transport.In eukaryotic cells, members of the Ctr family of proteins transport Cu ϩ inside the cell (15). Ctr1 organizes as homotrimers forming transmembrane pores that facilitate Cu ϩ transmembrane translocation by an apparently energy-independent undefined mechanism (16, 17). Although relevant Cu ϩ -binding Met have been observed in the extracellular loops of Ctr1 (15); none of the invariant transmembrane residues appear to be required for transport, and no direct coordination is evident (17).As a counterpart to influx systems, Cu ϩ -ATPases are responsible for cytoplasmic Cu ϩ efflux. Mutations of the human Cu ϩ -ATPase genes, ATP7A and ATP7B, lead to Menkes syndrome and Wilson disease, respectively (18,19). Cu ϩ -ATPases are members of the superfamily of P-type ATPases (20, 21). These couple Cu ϩ transport to the hydrolysis of ATP, following a classical Post catalytic/transport cycle (19,21). In this mechanism, transmembrane metal-binding sites (TMMBSs) 4 are responsible for handling the ion during transmembrane translocation (22). These transmembrane sites are expos...

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Section: Methodsmentioning

confidence: 99%

Structure of the Two Transmembrane Cu+ Transport Sites of the Cu+-ATPases

González‐Guerrero

Eren

Rawat

et al. 2008

Journal of Biological Chemistry

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146

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“…The pMMO, in contrast, is a copper-and possibly iron-containing, membrane-associated enzyme that is associated with unusual intracytoplasmic membranes that take the form of vesicular disks in type I methanotrophs and paired peripheral layers in type II organisms (65)(66)(67)(68)(69)(70)(71)(72)(73)(74)(75). Intracytoplasmic membranes are enriched in pMMO and can be physically separated from the cytoplasmic membrane on the basis of sedimentation velocity in sucrose density gradients (76).…”

Section: Physiology and Biochemistry Of Methanotrophsmentioning

confidence: 99%

Methanobactin and the Link between Copper and Bacterial Methane Oxidation

DiSpirito

Semrau

Murrell

et al. 2016

Microbiol Mol Biol Rev

132

157

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SUMMARYMethanobactins (mbs) are low-molecular-mass (<1,200 Da) copper-binding peptides, or chalkophores, produced by many methane-oxidizing bacteria (methanotrophs). These molecules exhibit similarities to certain iron-binding siderophores but are expressed and secreted in response to copper limitation. Structurally, mbs are characterized by a pair of heterocyclic rings with associated thioamide groups that form the copper coordination site. One of the rings is always an oxazolone and the second ring an oxazolone, an imidazolone, or a pyrazinedione moiety. The mb molecule originates from a peptide precursor that undergoes a series of posttranslational modifications, including (i) ring formation, (ii) cleavage of a leader peptide sequence, and (iii) in some cases, addition of a sulfate group. Functionally, mbs represent the extracellular component of a copper acquisition system. Consistent with this role in copper acquisition, mbs have a high affinity for copper ions. Following binding, mbs rapidly reduce Cu2+to Cu1+. In addition to binding copper, mbs will bind most transition metals and near-transition metals and protect the host methanotroph as well as other bacteria from toxic metals. Several other physiological functions have been assigned to mbs, based primarily on their redox and metal-binding properties. In this review, we examine the current state of knowledge of this novel type of metal-binding peptide. We also explore its potential applications, how mbs may alter the bioavailability of multiple metals, and the many roles mbs may play in the physiology of methanotrophs.

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“…Processing methods and fitting parameters used during data analysis are described in detail elsewhere (33,36). Single scattering theoretical models were used during data simulation.…”

Section: Cloning and Purification Of Copz And The Copa N-terminal Mbdmentioning

confidence: 99%

Characterization and Structure of a Zn2+ and [2Fe-2S]-containing Copper Chaperone from Archaeoglobus fulgidus

Sazinsky

LeMoine

Orofino

et al. 2007

Journal of Biological Chemistry

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Copper is a meticulously regulated redox-active micronutrient found in a number of important enzymes, including cytochrome c oxidase and superoxide dismutase. Because free or excess intracellular copper can cause oxidative damage, both prokaryotes and eukaryotes have developed specific copper trafficking and transport pathways (1, 2). Deficiencies in these processes are linked to human diseases, including Wilson and Menkes disease. In Wilson disease, accumulation of copper in the liver and brain leads to cirrhosis and neurodegeneration, and in Menkes disease, copper transport across the small intestine is impaired, leading to copper deficiency in peripheral tissues (3, 4). Both disorders are caused by mutations in Cu ϩ -transporting P 1B -type ATPases (5-7), enzymes that are found in most organisms and function in the cellular localization and/or export of cytosolic copper (8, 9).The Cu ϩ -ATPases include eight transmembrane (TM) 4 helices, of which three (TM6, TM7, and TM8) contribute invariant residues to form the transmembrane metal-binding site, a cytosolic ATP binding domain linking TM6 and TM7, an actuator domain between TM4 and TM5, and cytosolic metal binding domains (MBDs) of ϳ60 -70 amino acids that bind Cu ϩ (8, 10). Whereas prokaryotic Cu ϩ -ATPases typically have one or two MBDs, eukaryotic homologs have up to six such domains. Each MBD contains a highly conserved CXXC consensus sequence for binding Cu ϩ and adopts a ␤␣␤␤␣␤ fold (11-14) nearly identical to that of the Atx1-like cytosolic copper chaperones, including yeast Atx1, human Atox1, and bacterial . These chaperones also contain a CXXC motif and deliver Cu ϩ to one or all of the MBDs (20 -26). It is not clear how Cu ϩ reaches the transmembrane metal-binding site and how the cytosolic chaperones participate in this process. The hyperthermophilic Cu ϩ -ATPase CopA from Archaeoglobus fulgidus is readily expressed in fully active recombinant form, is highly stable, and contains all of the essential structural elements for copper transfer, including one N-terminal and one C-terminal MBD (27)(28)(29). CopA is therefore an excellent model system both for investigating the mechanisms of P 1B -type ATPases and for studying interactions between a cytosolic chaperone and its intact partner Cu ϩ -ATPase. The only potential copper chaperone protein in the A. fulgidus genome, which we have designated A. fulgidus CopZ, differs from all other * This work was supported in part by National Institutes of Health Grant GM58518 (to A. C. R.), National Science Foundation Grant MCM-0235165 (to J. M. A.), and National Institutes of Health Grants HL13531 (to B. M. H.) and DK068139 (to T. L. S.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

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Characterization of the Particulate Methane Monooxygenase Metal Centers in Multiple Redox States by X-ray Absorption Spectroscopy

Cited by 87 publications

References 41 publications

Structure of the Two Transmembrane Cu+ Transport Sites of the Cu+-ATPases

Structure of the Two Transmembrane Cu+ Transport Sites of the Cu+-ATPases

Methanobactin and the Link between Copper and Bacterial Methane Oxidation

Characterization and Structure of a Zn2+ and [2Fe-2S]-containing Copper Chaperone from Archaeoglobus fulgidus

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