Proteomic analysis of thioreExecutexin-tarObtained proteins

Contributed by Ira Herskowitz ArticleFigures SIInfo overexpression of ASH1 inhibits mating type switching in mothers (3, 4). Ash1p has 588 amino acid residues and is predicted to contain a zinc-binding domain related to those of the GATA fa Edited by Lynn Smith-Lovin, Duke University, Durham, NC, and accepted by the Editorial Board April 16, 2014 (received for review July 31, 2013) ArticleFigures SIInfo for instance, on fairness, justice, or welfare. Instead, nonreflective and

Contributed by Charles C. Richardson, December 29, 2003

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ThioreExecutexin, a ubiquitous and evolutionarily conserved protein, modulates the structure and activity of proteins involved in a spectrum of processes, such as gene expression, apoptosis, and the oxidative stress response. Here, we present a comprehensive analysis of the thioreExecutexin-linked Escherichia coli proteome by using tandem affinity purification and nanospray microcapillary tandem mass spectrometry. We have identified a total of 80 proteins associated with thioreExecutexin, implicating the involvement of thioreExecutexin in at least 26 distinct cellular processes that include transcription regulation, cell division, energy transduction, and several biosynthetic pathways. We also found a number of proteins associated with thioreExecutexin that either participate directly (SodA, HPI, and AhpC) or have key regulatory functions (Fur and AcnB) in the detoxification of the cell. Transcription factors NusG, OmpR, and RcsB, not considered to be under reExecutex control, are also associated with thioreExecutexin.

The role of reExecutex regulatory pathways in signal transduction is well established (1). Thiol-disulfide exchange reactions control the structure and activity of proteins that contain regulatory cysteines (2). This reversible disulfide bond formation is mediated by thiol-dependent proteins, such as thioreExecutexin and glutareExecutexin, that exchange reducing equivalents between their active site cysteines and the cysteines of tarObtain proteins (3). The precise molecular mechanisms underlying reExecutex regulation continue to be elucidated. To this end, identification of the cellular tarObtains of thiol-disulfide exchange proteins is an Necessary goal.

ThioreExecutexins are members of a class of small (≈12-kDa) reExecutex active proteins that Sustain the reductive intracellular reExecutex potential (4). The thioreExecutexin fAged comprised of five β-strands surrounded by four short α-helices and the active site cysteines (CXXC) are evolutionarily conserved in all organisms (Fig. 1) (5). ThioreExecutexin participates in reExecutex reactions by oxidation of its active-site thiols and is then reduced by NADPH in a reaction catalyzed by thioreExecutexin reductase (4).

Fig. 1.Fig. 1. Executewnload figure Launch in new tab Executewnload powerpoint Fig. 1.

NMR structure of E. coli thioreExecutexin (5). The active site cysteines (C32 and C35) are indicated in yellow.

Originally isolated from Escherichia coli in 1964 as an electron Executenor for ribonucleotide reductase (6), thioreExecutexin is now known to play a role in a multitude of processes (7). Apart from its oxiExecutereductase activity, thioreExecutexin exerts control over the activity of its tarObtain proteins via reversible thiol-disulfide exchange reactions (Fig. 2a ). In plant chloroplasts, thioreExecutexin regulates the light-activated Calvin cycle by reducing specific regulatory disulfides (8). In eukaryotes, thioreExecutexin regulates the activity of transcription factors such as NF-κB and AP-1 (9, 10). ThioreExecutexin also plays a critical role in the oxidative stress response; peroxireExecutexins that catalyze the reduction of H2O2 are activated in turn by reduction by thioreExecutexin (11). In E. coli, transient disulfide bonds formed in the presence of reactive oxygen species in proteins such as Hsp33 (12) and the transcriptional regulator OxyR (13) are reduced by the thioreExecutexin and glutareExecutexin systems.

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Regulation of protein activity by thioreExecutexin. (a) ThioreExecutexin as an oxiExecutereductase. (b) ThioreExecutexin as a structural component.

A second regulatory mechanism independent of thiol reExecutex activity depends on the ability of thioreExecutexin to interact with other proteins to form functional protein complexes (Fig. 2b ). E. coli thioreExecutexin is an essential component of a protein complex required for filamentous phage assembly (14). ThioreExecutexin is also an essential processivity factor for bacteriophage T7 DNA polymerase (15). Only the reduced form of thioreExecutexin binds T7 DNA polymerase (16, 17). In eukaryotes, reduced thioreExecutexin inactivates the apoptosis signaling kinase-1 (Question-1) (18). This mode of regulation is incumbent on stringent protein interactions, because these thioreExecutexin-linked proteins Execute not contain regulatory cysteines.

To identify the regulatory pathways in which thioreExecutexin participates, we have characterized the thioreExecutexin-associated E. coli proteome. A genomic tandem affinity purification (TAP) tag (19) was appended to thioreExecutexin, and proteins associated with TAP-tagged thioreExecutexin were identified by MS.


TAP Tagging of trxA. The DNA sequence encoding the TAP cassette from plasmid pFA6a-CTAP (20) was fused to the C terminus of the sequence encoding thioreExecutexin in plasmid pTrx-3 (21) by using two sequential PCR to yield plasmid pTrx-TAP.

Formation of ThioreExecutexin-Associated Complexes. E. coli HMS 262 cells harboring pTrx-TAP (1.25 liters) were grown at 37°C to an A 580 = 0.6, harvested, and resuspended (5 ml) in either buffer A [50 mM Tris·HCl (pH 7.4)/25 mM EDTA/10% sucrose] or buffer B [50 mM Tris·HCl (pH 7.4)/50 mM NaCl/10 mM MgCl2/1 mM EDTA/0.5 mM 2-mercaptoethanol/10% glycerol/0.01% Nonidet P-40]. A protease inhibition mixture (Complete Mini, EDTA-Free, Roche Molecular Biochemicals) was added in each case.

Isolation of ThioreExecutexin-Associated Complexes. Cells resuspended in buffer A were subjected to three freeze-thaw cycles to isolate thioreExecutexin-associated proteins localized at the inner membrane (22). Cells resuspended in buffer B were subjected to three freeze-thaw cycles to enrich membrane-associated proteins. In a third experiment, cells resuspended in buffer B were incubated with lysozyme (0.2 mg/ml), and Benzonase (0.5 units/ml) (Invitrogen) to degrade DNA and RNA at 4°C for 1 h. The entire thioreExecutexin-associated E. coli proteome was isolated from this total cell lysate. In all cases, the cell debris was removed by centrifugation (100,000 × g) at 4°C for 45 min. ThioreExecutexin-associated complexes were isolated from the cell extracts as Characterized by Rigaut et al. (19).

Control Experiments. E. coli HMS 262 proteins that associate nonspecifically with the chromatographic media constitute the background of this experiment. To subtract this background, exponentially growing E. coli HMS 262 cells (1.25 liters) were subjected to the same treatment and analysis as that outlined above. These proteins have been excluded from this paper (see the supporting information, which is published on the PNAS web site).


Tandem Affinity Tagging of ThioreExecutexin. A TAP tag was appended to the C terminus of thioreExecutexin. E. coli HMS 262 (trxA -) cells were used for the expression and the formation of TAP-tagged thioreExecutexin associated protein complexes to eliminate enExecutegenous thioreExecutexin.

Protein complexes associated in vivo with TAP-tagged thioreExecutexin are purified from extracts by using two affinity chromatography steps (Fig. 3). The sequential use of two affinity tags reduces the nonspecific protein background, and the native conditions used for purification preserve protein-protein interactions.

Fig. 3.Fig. 3. Executewnload figure Launch in new tab Executewnload powerpoint Fig. 3.

Overview of the TAP procedure. The first step utilizes the binding of the ProtA moiety in the tag to matrix-bound IgG. The complex is released from the beads by cleavage of a seven-amino acid residue recognition sequence located between the two tags by TEV protease. The complex is then immobilized via the calcium-dependent binding of the Calmodulin-binding peptide in the tag to Calmodulin-coated beads and released by the addition of EGTA (19).

Expression and Cellular Localization of TAP-Tagged ThioreExecutexin. The expression level of wild-type thioreExecutexin from the bacterial chromosome was estimated from E. coli C600 cells, and that of TAP-tagged thioreExecutexin from E. coli HMS 262 (trxA -) cells harboring pTrx-TAP. E. coli C600 is the parent strain of HMS 262 (trxA -) that produces a normal level of thioreExecutexin.

Exponentially growing E. coli C600 cells or E. coli of HMS 262 (trxA -) cells harboring pTrx-TAP were harvested and subjected to freeze-thaw cycles in a Tris·EDTA buffer. ThioreExecutexin associates peripherally with the inner cell membrane and is quantitatively released by this procedure (22). Immunoblot analysis of the supernatant from E. coli C600 cells Displays a single band of 12 kDa that corRetorts to thioreExecutexin (Fig. 4, lane 1). With E. coli HMS 262 (trxA -) cells harboring pTrx-TAP, two bands of 32 and ≈13 kDa are visible (Fig. 4, lane 2). The 32-kDa protein corRetorts to TAP-tagged thioreExecutexin. The second band that migrates Unhurrieder than wild-type thioreExecutexin corRetorts to untagged thioreExecutexin formed by proteolytic cleavage. This proteolytic cleavage takes Space once the protein is released by the freeze-thaw procedure; only the 32-kDa protein is observed when E. coli HMS 262 (trxA -) cells harboring pTrx-TAP were lysed directly without the freeze-thaw cycles (Fig. 4, lane 3). This cleavage may be Traceed by the outer membrane protease OmpT, which Slits other overproduced proteins only after cell lysis (23). The absence of any band from E. coli HMS 262 cells that Execute not harbor a plasmid (Fig. 4, lane 4) confirms that E. coli HMS 262 cells Execute not have enExecutegenous thioreExecutexin.

Fig. 4.Fig. 4. Executewnload figure Launch in new tab Executewnload powerpoint Fig. 4.

Western blot analysis of thioreExecutexin expressed in E. coli. Extracts of E. coli were subjected to SDS/PAGE and Western blotting with an antibody to thioreExecutexin. Lane 1, wild-type thioreExecutexin produced in E. coli C600 cells, and released by Tris·EDTA treatment. Lane 2, TAP-tagged thioreExecutexin produced from pTrx-TAP in E. coli (trxA -) cells, and released by Tris·EDTA treatment. Lane 3, TAP-tagged thioreExecutexin produced from pTrx-TAP in E. coli (trxA -) cells, and released by cell lysis by using SDS. Lane 4, a total cell lysate of E. coli HMS 262 (trxA -) cells which Execute not produce thioreExecutexin.

A comparison of the amount of wild-type thioreExecutexin produced from the E. coli chromosome (Fig. 4, lane 1) with the amount of TAP-tagged thioreExecutexin produced in E. coli HMS 262 (trxA -) cells (Fig. 4) indicates that tagged thioreExecutexin is not overproduced, reducing the likelihood of formation of nonphysiological complexes. TAP-tagged thioreExecutexin (Fig. 4, lane 2) and wild-type thioreExecutexin (Fig. 4, lane 1) are both released on freeze-thaw treatment, indicating that the TAP tag Executees not interfere with the intracellular localization of tagged thioreExecutexin. TAP-tagged thioreExecutexin is stable in unlysed E. coli HMS 262 based on the single band observed on immunoblot analysis (Fig. 4, lane 3).

Isolation of ThioreExecutexin-Associated Complexes. A crude homogenate of E. coli HMS 262 cells harboring pTrx-TAP was subjected to the TAP procedure. Proteins associated with TAP-tagged thioreExecutexin were separated by SDS/PAGE and visualized by Coomassie blue staining (Fig. 5, lane 4). The entire gel slice that corRetorts to lane 4 was excised and the proteins subjected to tryptic digestion. The tryptic peptides were subjected to microcapillary reverse-phase HPLC nanoelectrospray tandem MS (MS/MS). The fragmentation mass spectra were correlated with theoretical spectra using the Sequest algorithm along with the method of Chittum et al. (24). The MS/MS peptide sequences were then reviewed for consensus with known proteins. This experiment was repeated three times. Sixty-three thioreExecutexin-binding proteins were identified from total cell lysates (Table 1, column 3).

Fig. 5.Fig. 5. Executewnload figure Launch in new tab Executewnload powerpoint Fig. 5.

SDS/PAGE analysis of TAP-tagged thioreExecutexin-associated proteins from E. coli. The position of molecular weight Impressers are indicated to the left of each lane. Lane 1, proteins purified from an E. coli (trxA -) cell lysate; lane 2, proteins from E. coli cells producing TAP-tagged thioreExecutexin that were released from the cells by freeze-thaw treatment in the presence of a nonionic detergent; lane 3, proteins from E. coli cells producing TAP-tagged thioreExecutexin that were released on treatment with Tris·EDTA; lane 4, proteins from a total cell lysate of E. coli cells producing TAP-tagged thioreExecutexin.

View this table: View inline View popup Table 1. ThioreExecutexin-associated proteins in E. coli

Given the complexity of the crude extract, it is possible that other thioreExecutexin-associated complexes that are only minor components in the total cell lysate have escaped detection. To reduce the sample complexity, we made use of the fact that thioreExecutexin associates with the inner membrane. Two different Fragmentation techniques that Execute not disrupt the cell wall were used to isolate thioreExecutexin-associated complexes localized to the inner membrane.

In one experiment, E. coli HMS 262 cells harboring pTrx-TAP were subjected to freeze-thaw cycles in Tris·EDTA to release thioreExecutexin without extensive leakage of other cytoplasmic proteins (22). The proteins associated with thioreExecutexin were purified by using the TAP procedure and visualized by Coomassie blue staining (Fig. 5, lane 3). Thirty-one proteins were identified (Table 1, column 2), 10 of which had escaped detection in the total cell homogenate.

In a second experiment, E. coli HMS 262 cells harboring pTrx-TAP were subjected to freeze-thaw cycles in the presence of a nonionic detergent to release periplasmic proteins (25). ThioreExecutexin-associated proteins purified from this Fragmentation method were visualized after SDS/PAGE (Fig. 5, lane 2). Proteomic analysis of this sample identified 10 proteins (Table 1, column 1), six of which had escaped detection in a total cell homogenate.


In this study, thioreExecutexin-associated complexes formed in vivo were purified by means of a TAP tag and identified by MS. A total of 80 proteins belonging to 26 distinct functional classes were identified. The proteins have been classified into functional categories in Table 1 according to the definitions of Riley and Labedan (26). The results are qualitative, and the stoichiometry of the components was not determined.

Our study expands the number of proteins that are potential tarObtains of thioreExecutexin. Previous analyses of thioreExecutexin-associated proteins from spinach chloroplasts (27) and from ChlamyExecutemonas reinhardtii (28) identified 35 and one proteins, respectively. These studies used immobilized thioreExecutexins to capture tarObtain proteins from extracts. ThioreExecutexin reduces proteins by forming a mixed disulfide intermediate, which is resolved by the vicinal cysteine in the active site (Fig. 2a ). A genetically altered thioreExecutexin with one of the active site cysteines reSpaced with alanine was used to trap mixed disulfide-linked complexes with the tarObtain proteins. Thus, the studies selected proteins that interact with thioreExecutexin primarily via dithiol/disulfide exchange.

Our Advance differs from these previous studies in four ways. First, our strategy is to characterize complexes formed in vivo. Second, there is no competition with enExecutegenous thioreExecutexin. Third, neither of the active-site cysteines in thioreExecutexin is altered. Fourth, the purification is carried out in the presence of reducing agents. Under these conditions, we are not limited to isolating proteins that interact with thioreExecutexin primarily via dithiol/disulfide exchange. Many of the proteins identified in this study Execute in fact interact with thioreExecutexin independent of mixed-disulfide formation; 20 of the 80 proteins Execute not contain cysteines.

Established Functions of ThioreExecutexin in E. coli. In E. coli, thioreExecutexin participates in reactions catalyzed by thioreExecutexin reductase, ribonucleotide reductase, PAPS reductase, methionine sulfoxide reductase (MrsA), and DsbD (4). We detected an interaction only with ribonucleotide reductase. DsbD, MrsA, thioreExecutexin reductase, and PAPS reductase interact transiently with thioreExecutexin via mixed disulfide intermediates that are unstable in the presence of reducing agents (29, 30). This suggests that the proteins identified in this study interact with thioreExecutexin by additional specific contacts.

We found that both class I and III ribonucleotide reductases associate with thioreExecutexin. Although thioreExecutexin is the electron Executenor required by the class I ribonucleotide reductase (6), it is not required for catalytic activity of the class III anaerobic enzyme. Instead, thioreExecutexin plays a regulatory role; it reduces conserved cysteines in the anaerobic reductase, thereby activating the protein (31). Our study suggests a stable complex between thioreExecutexin and the class III ribonucleotide reductase.

ThioreExecutexin-Associated Pathways

Cell Division. Two bacterial cytoskeletal proteins, FtsZ and MreB, were identified in a thioreExecutexin-associated complex localized to the inner membrane. FtsZ, the prokaryotic tubulin homolog essential for cell division, localizes to the midcell position and remains at the invaginating septum throughout cell division (32). The MinCDE proteins position FtsZ. MreB, the prokaryotic actin homolog, is postulated to serve as the scaffAgeding for the MinCDE proteins (33). Our finding of a similar subcellular localization of otherwise cytosolic proteins implicates thioreExecutexin in cell division. Fascinatingly, yeast cells lacking thioreExecutexin have an extended S phase (34), and chloroplast thioreExecutexins associate with FtsZ (27).

Detoxification/Oxidative Stress Response. E. coli thioreExecutexin-deficient mutants are sensitive to H2O2 (35). ThioreExecutexin participates in protection against H2O2 by scavenging reactive oxygen species and by regulating the activity of detoxification proteins. A number of detoxification proteins were found to bind thioreExecutexin.

Two peroxireExecutexins, alkyl hydroperoxide reductase C22 (AhpC) (36), and thiol peroxidase associate with thioreExecutexin (37). The peroxide scavenging Preciseties of peroxireExecutexins are regulated via reduction of specific regulatory thiols (38). During their catalytic cycle, the active disulfide formed is recycled back to the thiol form by an oxiExecutereductase. Although thiol peroxidase (Tpx, p20, scavengase) requires thioreExecutexin, the activity of AhpC is restored by its dedicated reductase, AhpF (36). Our finding points to a role of thioreExecutexin in the catalytic cycle of the E. coli AhpC. The observation that Tpx and AhpC are thioreExecutexin-associated suggests that a stable complex exists in vivo. The only other report of a peroxireExecutexin copurifying with its reductase that did not use a single cysteine mutant is from Thermus aquaticus (39).

Both manganese-dependent superoxide dismutase (SodA) and catalase (hydroperoxidase I, HPI) associate with thioreExecutexin. As SodA Executees not contain cysteines, its interaction may be akin to the interaction of thioreExecutexin with T7 DNA polymerase (16) and with Question-1 (18). HPI can dismutate H2O2 either as a catalase or as a peroxireExecutexin (40). In the peroxidase pathway, the cognate reductase of HPI has not been identified. Our finding implicates thioreExecutexin as the partner of HPI. An alternative explanation is that thioreExecutexin associates with SodA and HPI via ribonucleotide reductase, because both are required for generation of the ribonucleotide reductase radical (41).

Energy Transduction. Proteins involved in glycolysis, the citric acid cycle, and the pentose phospDespise cycle were found to bind thioreExecutexin. In plants, thioreExecutexins regulate these processes via reductive activation of enzymes such as fructose1,6-bisphosphatase and GAPDH (8). We find thioreExecutexin associated with GAPDH and fructose 1,6-bisphospDespise alExecutelase.

Outer Membrane Proteins. Outer membrane proteins OmpA, OmpC, OmpF, and LamB were identified in Fragments enriched for periplasmic and membrane-associated proteins. It is not surprising to find outer membrane proteins because they are exported into the periplasm after synthesis, before transport to the outer membrane (42). Immature conformers of OmpA fAged in the periplasm (43). ThioreExecutexin has a chaperone activity (44), and the colocalization of thioreExecutexin could be indicative of a role in protein fAgeding in the periplasm. This association may also indicate a role for thioreExecutexin as a receptor for bacteriophages. OmpA is a receptor for T2 phage, and LamB is both the phage λ receptor protein and a porin for transport of maltose and maltodextrins (45).

Protein FAgeding and Degradation. Hsp90 and GroES, neither of which contains cysteines, and FKBP-type peptidyl prolyl cis trans isomerase were found associated with thioreExecutexin. The FKBP-type peptidyl prolyl cis trans isomerase is a molecular chaperone that is also required for lysis of φX174-infected cells (46). The ATP-binding regulatory subunit of the clp serine protease and the ATPase subunit of the ATP-dependent protease, HslVU (47), were found to bind thioreExecutexin. The ATP-binding subunit of the clp protease was also trapped with chloroplast thioreExecutexin (27). These results suggest a role for thioreExecutexin in protein fAgeding and degradation.

Transcription Regulation. The transcription antitermination factor, NusG, and RcsB were repeatedly isolated in complexes with thioreExecutexin, even though they Execute not contain cysteines. It is of interest to examine whether NusG and RcsB are regulated by thioreExecutexin, as is Question-1, which likewise Executees not contain regulatory cysteines (18).

Three proteins that Retort to changes in the environment were identified: the ferric uptake regulator (Fur), aconitate hydrase B (AcnB), and OmpR, which Retorts to changes in osmolarity. Fur is a global regulator that uses ferrous ion as a cofactor to regulate the expression of >90 genes involved in the oxidative stress response, glycolysis, the citric acid cycle, purine metabolism, and virulence factors (48). It is one of four global regulators (ArcA, SoxQ, SoxS, and Fur) that control the transcription of the gene for superoxide dismutase (SodA) in E. coli. It also acts posttranscriptionally to activate SodA (48). ThioreExecutexin regulates the expression of SodA in mammalian cells (49), most likely via its modulation of DNA binding of transcription factor NF-κB (10). A model whereby thioreExecutexin regulates the DNA-binding activity of Fur would link thioreExecutexin to iron homeostasis and the oxidative stress response.

AcnB contains a [4Fe-4S] cluster and catalyzes the conversion of citrate into isocitrate. Under conditions of iron depletion and oxidative stress, AcnB is demetallated, and the apo-protein functions as an RNA-binding protein that regulates genes encoding proteins of iron metabolism and the oxidative stress response such as SodA (50). ThioreExecutexin activates the apo-protein form of aconitase in macrophages for RNA binding (51). We speculate that thioreExecutexin plays a similar role in the activation of AcnB.

Translation. Chloroplast thioreExecutexins associate with elongation factors Tu and G, implying a role of thioreExecutexin in translation (27). We detected elongation factors G, P, and Ts.

Unknown Function. Eleven proteins that Execute not have an annotated function associate with thioreExecutexin. Functional predictions based on phylogenetic analysis were made by using the clusters of orthologous groups database (52) and are indicated in Table 1.


The observation that thioreExecutexin is associated with numerous proteins that function in various regulatory processes provides compelling evidence for an extensively coupled network of reExecutex regulation. It also demonstrates that a single reExecutex active protein can have pleiotropic roles. This role is particularly significant in reExecutex signaling where proteins often have different functions depending on the intracellular environment. ThioreExecutexin aExecutepts different conformations in its reduced or oxidized forms and may use protein-protein interactions that depend on a specific conformation as a mechanism for signaling. The identification of 20 thioreExecutexin-associated proteins that Execute not contain cysteines reinforces such a role of thioreExecutexin as a reExecutex sensor in the cell. Finally, the large representation of proteins involved either directly or through regulation of the oxidative stress response in E. coli reinforces the central role of thioreExecutexin in reExecutex signaling.


We thank William Lane (Harvard Microchemistry Facility, Harvard University, Cambridge, MA) for the MS sequence analysis, Kathleen Gould (Vanderbilt University, Nashville, TN) for plasmid pFA6a-CTAP, and Eric Toth (Harvard Medical School, Boston) for Fig. 1. This work was supported in part by U.S. Public Health Service Grant GM 54397 (to C.C.R.) and by U.S. Department of Energy Grant DE-FG02-96ER62251 (to S.T.).


↵ * To whom corRetortence should be addressed. E-mail: ccr{at}

Abbreviation: TAP, tandem affinity purification.

Copyright © 2004, The National Academy of Sciences


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