Determining the Control Circuitry of Redox Metabolism at the Genome-Scale
Determining how facultative anaerobic organisms sense and direct cellular responses to electron acceptor availability has been a subject of intense study. However, even in the model organism Escherichia coli, established mechanisms only explain a small fraction of the hundreds of genes that are regu...
Saved in:
| Published in | PLoS genetics Vol. 10; no. 4; p. e1004264 |
|---|---|
| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
01.04.2014
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1553-7404 1553-7390 1553-7404 |
| DOI | 10.1371/journal.pgen.1004264 |
Cover
Loading…
| Abstract | Determining how facultative anaerobic organisms sense and direct cellular responses to electron acceptor availability has been a subject of intense study. However, even in the model organism Escherichia coli, established mechanisms only explain a small fraction of the hundreds of genes that are regulated during electron acceptor shifts. Here we propose a qualitative model that accounts for the full breadth of regulated genes by detailing how two global transcription factors (TFs), ArcA and Fnr of E. coli, sense key metabolic redox ratios and act on a genome-wide basis to regulate anabolic, catabolic, and energy generation pathways. We first fill gaps in our knowledge of this transcriptional regulatory network by carrying out ChIP-chip and gene expression experiments to identify 463 regulatory events. We then interfaced this reconstructed regulatory network with a highly curated genome-scale metabolic model to show that ArcA and Fnr regulate >80% of total metabolic flux and 96% of differential gene expression across fermentative and nitrate respiratory conditions. Based on the data, we propose a feedforward with feedback trim regulatory scheme, given the extensive repression of catabolic genes by ArcA and extensive activation of chemiosmotic genes by Fnr. We further corroborated this regulatory scheme by showing a 0.71 r(2) (p<1e-6) correlation between changes in metabolic flux and changes in regulatory activity across fermentative and nitrate respiratory conditions. Finally, we are able to relate the proposed model to a wealth of previously generated data by contextualizing the existing transcriptional regulatory network. |
|---|---|
| AbstractList | Determining how facultative anaerobic organisms sense and direct cellular responses to electron acceptor availability has been a subject of intense study. However, even in the model organism Escherichia coli, established mechanisms only explain a small fraction of the hundreds of genes that are regulated during electron acceptor shifts. Here we propose a qualitative model that accounts for the full breadth of regulated genes by detailing how two global transcription factors (TFs), ArcA and Fnr of E. coli, sense key metabolic redox ratios and act on a genome-wide basis to regulate anabolic, catabolic, and energy generation pathways. We first fill gaps in our knowledge of this transcriptional regulatory network by carrying out ChIP-chip and gene expression experiments to identify 463 regulatory events. We then interfaced this reconstructed regulatory network with a highly curated genome-scale metabolic model to show that ArcA and Fnr regulate >80% of total metabolic flux and 96% of differential gene expression across fermentative and nitrate respiratory conditions. Based on the data, we propose a feedforward with feedback trim regulatory scheme, given the extensive repression of catabolic genes by ArcA and extensive activation of chemiosmotic genes by Fnr. We further corroborated this regulatory scheme by showing a 0.71 r(2) (p<1e-6) correlation between changes in metabolic flux and changes in regulatory activity across fermentative and nitrate respiratory conditions. Finally, we are able to relate the proposed model to a wealth of previously generated data by contextualizing the existing transcriptional regulatory network. Determining how facultative anaerobic organisms sense and direct cellular responses to electron acceptor availability has been a subject of intense study. However, even in the model organism Escherichia coli, established mechanisms only explain a small fraction of the hundreds of genes that are regulated during electron acceptor shifts. Here we propose a qualitative model that accounts for the full breadth of regulated genes by detailing how two global transcription factors (TFs), ArcA and Fnr of E. coli, sense key metabolic redox ratios and act on a genome-wide basis to regulate anabolic, catabolic, and energy generation pathways. We first fill gaps in our knowledge of this transcriptional regulatory network by carrying out ChIP-chip and gene expression experiments to identify 463 regulatory events. We then interfaced this reconstructed regulatory network with a highly curated genome-scale metabolic model to show that ArcA and Fnr regulate >80% of total metabolic flux and 96% of differential gene expression across fermentative and nitrate respiratory conditions. Based on the data, we propose a feedforward with feedback trim regulatory scheme, given the extensive repression of catabolic genes by ArcA and extensive activation of chemiosmotic genes by Fnr. We further corroborated this regulatory scheme by showing a 0.71 r(2) (p<1e-6) correlation between changes in metabolic flux and changes in regulatory activity across fermentative and nitrate respiratory conditions. Finally, we are able to relate the proposed model to a wealth of previously generated data by contextualizing the existing transcriptional regulatory network.Determining how facultative anaerobic organisms sense and direct cellular responses to electron acceptor availability has been a subject of intense study. However, even in the model organism Escherichia coli, established mechanisms only explain a small fraction of the hundreds of genes that are regulated during electron acceptor shifts. Here we propose a qualitative model that accounts for the full breadth of regulated genes by detailing how two global transcription factors (TFs), ArcA and Fnr of E. coli, sense key metabolic redox ratios and act on a genome-wide basis to regulate anabolic, catabolic, and energy generation pathways. We first fill gaps in our knowledge of this transcriptional regulatory network by carrying out ChIP-chip and gene expression experiments to identify 463 regulatory events. We then interfaced this reconstructed regulatory network with a highly curated genome-scale metabolic model to show that ArcA and Fnr regulate >80% of total metabolic flux and 96% of differential gene expression across fermentative and nitrate respiratory conditions. Based on the data, we propose a feedforward with feedback trim regulatory scheme, given the extensive repression of catabolic genes by ArcA and extensive activation of chemiosmotic genes by Fnr. We further corroborated this regulatory scheme by showing a 0.71 r(2) (p<1e-6) correlation between changes in metabolic flux and changes in regulatory activity across fermentative and nitrate respiratory conditions. Finally, we are able to relate the proposed model to a wealth of previously generated data by contextualizing the existing transcriptional regulatory network. Determining how facultative anaerobic organisms sense and direct cellular responses to electron acceptor availability has been a subject of intense study. However, even in the model organism Escherichia coli, established mechanisms only explain a small fraction of the hundreds of genes that are regulated during electron acceptor shifts. Here we propose a qualitative model that accounts for the full breadth of regulated genes by detailing how two global transcription factors (TFs), ArcA and Fnr of E. coli, sense key metabolic redox ratios and act on a genome-wide basis to regulate anabolic, catabolic, and energy generation pathways. We first fill gaps in our knowledge of this transcriptional regulatory network by carrying out ChIP-chip and gene expression experiments to identify 463 regulatory events. We then interfaced this reconstructed regulatory network with a highly curated genome-scale metabolic model to show that ArcA and Fnr regulate >80% of total metabolic flux and 96% of differential gene expression across fermentative and nitrate respiratory conditions. Based on the data, we propose a feedforward with feedback trim regulatory scheme, given the extensive repression of catabolic genes by ArcA and extensive activation of chemiosmotic genes by Fnr. We further corroborated this regulatory scheme by showing a 0.71 r2 (p<1e-6) correlation between changes in metabolic flux and changes in regulatory activity across fermentative and nitrate respiratory conditions. Finally, we are able to relate the proposed model to a wealth of previously generated data by contextualizing the existing transcriptional regulatory network. Determining how facultative anaerobic organisms sense and direct cellular responses to electron acceptor availability has been a subject of intense study. However, even in the model organism Escherichia coli , established mechanisms only explain a small fraction of the hundreds of genes that are regulated during electron acceptor shifts. Here we propose a qualitative model that accounts for the full breadth of regulated genes by detailing how two global transcription factors (TFs), ArcA and Fnr of E. coli , sense key metabolic redox ratios and act on a genome-wide basis to regulate anabolic, catabolic, and energy generation pathways. We first fill gaps in our knowledge of this transcriptional regulatory network by carrying out ChIP-chip and gene expression experiments to identify 463 regulatory events. We then interfaced this reconstructed regulatory network with a highly curated genome-scale metabolic model to show that ArcA and Fnr regulate >80% of total metabolic flux and 96% of differential gene expression across fermentative and nitrate respiratory conditions. Based on the data, we propose a feedforward with feedback trim regulatory scheme, given the extensive repression of catabolic genes by ArcA and extensive activation of chemiosmotic genes by Fnr. We further corroborated this regulatory scheme by showing a 0.71 r 2 (p<1e-6) correlation between changes in metabolic flux and changes in regulatory activity across fermentative and nitrate respiratory conditions. Finally, we are able to relate the proposed model to a wealth of previously generated data by contextualizing the existing transcriptional regulatory network. All heterotrophic organisms must balance the deployment of consumed carbon compounds between growth and the generation of energy. These two competing objectives have been shown, both computationally and experimentally, to exist as the principal dimensions of the function of metabolic networks. Each of these dimensions can also be thought of as the familiar metabolic functions of catabolism, anabolism, and generation of energy. Here we detail how two global transcription factors (TFs), ArcA and Fnr of Escherichia coli that sense redox ratios, act on a genome-wide basis to coordinately regulate these global metabolic functions through transcriptional control of enzyme and transporter levels in changing environments. A model results from the study that shows how global transcription factors regulate global dimensions of metabolism and form a regulatory hierarchy that reflects the structural hierarchy of the metabolic network. Determining how facultative anaerobic organisms sense and direct cellular responses to electron acceptor availability has been a subject of intense study. However, even in the model organism Escherichia coli, established mechanisms only explain a small fraction of the hundreds of genes that are regulated during electron acceptor shifts. Here we propose a qualitative model that accounts for the full breadth of regulated genes by detailing how two global transcription factors (TFs), ArcA and Fnr of E. coli, sense key metabolic redox ratios and act on a genome-wide basis to regulate anabolic, catabolic, and energy generation pathways. We first fill gaps in our knowledge of this transcriptional regulatory network by carrying out ChIP-chip and gene expression experiments to identify 463 regulatory events. We then interfaced this reconstructed regulatory network with a highly curated genome-scale metabolic model to show that ArcA and Fnr regulate >80% of total metabolic flux and 96% of differential gene expression across fermentative and nitrate respiratory conditions. Based on the data, we propose a feedforward with feedback trim regulatory scheme, given the extensive repression of catabolic genes by ArcA and extensive activation of chemiosmotic genes by Fnr. We further corroborated this regulatory scheme by showing a 0.71 [r.sup.2] (p < 1e 6) correlation between changes in metabolic flux and changes in regulatory activity across fermentative and nitrate respiratory conditions. Finally, we are able to relate the proposed model to a wealth of previously generated data by contextualizing the existing transcriptional regulatory network. Determining how facultative anaerobic organisms sense and direct cellular responses to electron acceptor availability has been a subject of intense study. However, even in the model organism Escherichia coli, established mechanisms only explain a small fraction of the hundreds of genes that are regulated during electron acceptor shifts. Here we propose a qualitative model that accounts for the full breadth of regulated genes by detailing how two global transcription factors (TFs), ArcA and Fnr of E. coli, sense key metabolic redox ratios and act on a genome-wide basis to regulate anabolic, catabolic, and energy generation pathways. We first fill gaps in our knowledge of this transcriptional regulatory network by carrying out ChIP-chip and gene expression experiments to identify 463 regulatory events. We then interfaced this reconstructed regulatory network with a highly curated genome-scale metabolic model to show that ArcA and Fnr regulate .80% of total metabolic flux and 96% of differential gene expression across fermentative and nitrate respiratory conditions. Based on the data, we propose a feedforward with feedback trim regulatory scheme, given the extensive repression of catabolic genes by ArcA and extensive activation of chemiosmotic genes by Fnr. We further corroborated this regulatory scheme by showing a 0.71 r2 (p,1e-6) correlation between changes in metabolic flux and changes in regulatory activity across fermentative and nitrate respiratory conditions. Finally, we are able to relate the proposed model to a wealth of previously generated data by contextualizing the existing transcriptional regulatory network. |
| Audience | Academic |
| Author | Zengler, Karsten Palsson, Bernhard Nagarajan, Harish Kim, Donghyuk Federowicz, Stephen Ebrahim, Ali Cho, Byung-kwan Lerman, Joshua |
| AuthorAffiliation | 1 Department of Bioengineering, University of California San Diego, La Jolla, California, United States of America 3 Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, Lyngby, Denmark 2 Bioinformatics and Systems Biology Program, University of California San Diego, La Jolla, California, United States of America Institute of Molecular and Cell Biology (IMCB), ASTAR, Singapore |
| AuthorAffiliation_xml | – name: Institute of Molecular and Cell Biology (IMCB), ASTAR, Singapore – name: 3 Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, Lyngby, Denmark – name: 1 Department of Bioengineering, University of California San Diego, La Jolla, California, United States of America – name: 2 Bioinformatics and Systems Biology Program, University of California San Diego, La Jolla, California, United States of America |
| Author_xml | – sequence: 1 givenname: Stephen surname: Federowicz fullname: Federowicz, Stephen – sequence: 2 givenname: Donghyuk surname: Kim fullname: Kim, Donghyuk – sequence: 3 givenname: Ali surname: Ebrahim fullname: Ebrahim, Ali – sequence: 4 givenname: Joshua surname: Lerman fullname: Lerman, Joshua – sequence: 5 givenname: Harish surname: Nagarajan fullname: Nagarajan, Harish – sequence: 6 givenname: Byung-kwan surname: Cho fullname: Cho, Byung-kwan – sequence: 7 givenname: Karsten surname: Zengler fullname: Zengler, Karsten – sequence: 8 givenname: Bernhard surname: Palsson fullname: Palsson, Bernhard |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24699140$$D View this record in MEDLINE/PubMed https://www.osti.gov/servlets/purl/1904015$$D View this record in Osti.gov |
| BookMark | eNqVk11v0zAUhiM0xLbCP0AQDQnBRYs_88EF0lRgVBpM2oBby3VOWleOXWwHbf8ed-2mBiEE8kUs53nfNznH5zg7sM5Clj3FaIJpid-sXO-tNJP1AuwEI8RIwR5kR5hzOi4ZYgd7-8PsOIQVQpRXdfkoOySsqGvM0FE2ew8RfKettos8LiGfOhu9M_lUe9Xr6G9y1-aX0Ljr_DNEOXdGhy6X8RY-A-s6GF8paeBx9rCVJsCT3XOUffv44ev00_j84mw2PT0fq5LwOAbUAqlAlpQpUtSc8prNm7pqSCFrQMBJQxlQUFwqWqsCtRQSKQlvkZQE01H2fOu7Ni6IXRWCwJxwiigrUSJmW6JxciXWXnfS3wgntbg9cH4hpI9aGUgqKlFVAiZqznCB5lULlCAuG1RhyVXyerdL6-cdNApSdaQZmA7fWL0UC_dT0LpkBSXJ4GRr4ELUIigdQS2VsxZUFLhGDKVvGGWvdine_eghRNHpoMAYacH1m5_DFHFMaJnQF1t0kWoutG1dilUbXJzSoiIVI7hK1OQPVFoNdDqlQ6vT-UDweiBITITruJB9CGJ2dfkf7Jd_Zy--D9mXe-wSpInL4EwftbNhCD7bb8p9N-6udQLYFlDeheChvUcwEpvpubs3YjM9Yjc9Sfb2N1lql9zEp-pp83fxL8UZHYs |
| CitedBy_id | crossref_primary_10_1016_j_copbio_2014_12_017 crossref_primary_10_1016_j_jmb_2016_12_008 crossref_primary_10_1016_j_copbio_2014_12_016 crossref_primary_10_1128_spectrum_02101_22 crossref_primary_10_1128_mbio_03298_22 crossref_primary_10_1371_journal_pgen_1006590 crossref_primary_10_1038_s41467_018_06219_9 crossref_primary_10_1002_pmic_201600316 crossref_primary_10_1128_msystems_00001_21 crossref_primary_10_1038_s41598_017_02110_7 crossref_primary_10_1534_g3_116_029785 crossref_primary_10_1074_jbc_M117_789164 crossref_primary_10_1371_journal_pcbi_1011824 crossref_primary_10_1016_j_celrep_2023_113105 crossref_primary_10_1016_j_celrep_2015_07_043 crossref_primary_10_1128_mmbr_00110_21 crossref_primary_10_1093_nargab_lqad006 crossref_primary_10_1128_jb_00545_21 crossref_primary_10_1371_journal_pcbi_1008647 crossref_primary_10_1016_j_jia_2024_02_014 crossref_primary_10_1038_s41598_020_77927_w crossref_primary_10_3389_fmicb_2021_711077 crossref_primary_10_1016_j_biortech_2025_132061 crossref_primary_10_1016_j_vetmic_2016_10_011 crossref_primary_10_1371_journal_pgen_1005007 crossref_primary_10_1128_mbio_01448_23 crossref_primary_10_1093_nar_gkad253 crossref_primary_10_1089_ars_2017_7365 crossref_primary_10_1016_j_biotechadv_2019_107441 crossref_primary_10_1128_AEM_00823_18 crossref_primary_10_15252_msb_202010064 crossref_primary_10_1371_journal_pone_0197272 crossref_primary_10_1128_mSphere_00443_21 crossref_primary_10_1007_s12257_020_0030_9 crossref_primary_10_1016_j_coche_2014_08_003 crossref_primary_10_1093_nar_gky069 crossref_primary_10_1371_journal_pone_0147651 crossref_primary_10_1371_journal_pone_0152917 crossref_primary_10_1073_pnas_1702581114 crossref_primary_10_3390_biom12081019 crossref_primary_10_1099_mic_0_000346 crossref_primary_10_1016_j_bbamcr_2014_11_018 crossref_primary_10_1186_s12915_018_0555_y crossref_primary_10_3390_genes9110565 crossref_primary_10_1016_j_jbc_2022_102304 crossref_primary_10_1093_nar_gky752 crossref_primary_10_1021_jacs_7b13292 crossref_primary_10_1111_mmi_14795 crossref_primary_10_1186_s12934_017_0744_3 crossref_primary_10_3390_microorganisms10030647 crossref_primary_10_1038_s41598_019_42768_9 crossref_primary_10_1128_msystems_00784_24 |
| Cites_doi | 10.1074/jbc.M311657200 10.1046/j.1365-2958.2000.01972.x 10.1073/pnas.0406811102 10.1074/jbc.M512312200 10.1073/pnas.0403064101 10.1016/j.tibs.2009.12.001 10.1128/ecosalplus.3.4.4 10.1093/nar/gkq1143 10.1128/MMBR.52.3.318-326.1988 10.1073/pnas.1202582110 10.1016/j.cell.2012.01.021 10.1002/bit.10812 10.1093/nar/gkq780 10.1016/0092-8674(91)90130-Q 10.1111/j.1365-2958.1993.tb01664.x 10.1038/nrmicro787 10.1046/j.1365-2958.1999.01347.x 10.1002/bit.20381 10.1002/bit.20044 10.1006/jmbi.1998.2160 10.1073/pnas.0807227105 10.1371/journal.pone.0025501 10.1073/pnas.0609023104 10.1128/JB.185.1.204-209.2003 10.1371/journal.pgen.1003839 10.1038/nrmicro1022 10.1038/msb.2010.47 10.2144/000112039 10.1038/nrmicro2549 10.1074/jbc.M603450200 10.1038/nbt.2205 10.1074/jbc.M110.211144 10.1093/nar/gkq1110 10.1109/MCSE.2007.53 10.1101/gad.13.16.2134 10.1038/nprot.2011.308 10.1371/journal.pgen.1003565 10.1111/j.1742-4658.2005.04840.x 10.1126/science.1216882 10.1074/jbc.M700728200 10.1093/oxfordjournals.jbchem.a021519 10.1038/ncomms1928 10.1093/nar/gkp335 10.1016/j.molcel.2010.08.031 |
| ContentType | Journal Article |
| Copyright | COPYRIGHT 2014 Public Library of Science 2014 Federowicz et al 2014 Federowicz et al 2014 Federowicz et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Federowicz S, Kim D, Ebrahim A, Lerman J, Nagarajan H, et al. (2014) Determining the Control Circuitry of Redox Metabolism at the Genome-Scale. PLoS Genet 10(4): e1004264. doi:10.1371/journal.pgen.1004264 |
| Copyright_xml | – notice: COPYRIGHT 2014 Public Library of Science – notice: 2014 Federowicz et al 2014 Federowicz et al – notice: 2014 Federowicz et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Federowicz S, Kim D, Ebrahim A, Lerman J, Nagarajan H, et al. (2014) Determining the Control Circuitry of Redox Metabolism at the Genome-Scale. PLoS Genet 10(4): e1004264. doi:10.1371/journal.pgen.1004264 |
| CorporateAuthor | University of California San Diego, La Jolla, CA (United States) |
| CorporateAuthor_xml | – name: University of California San Diego, La Jolla, CA (United States) |
| DBID | AAYXX CITATION CGR CUY CVF ECM EIF NPM IOV ISN ISR 7X8 OIOZB OTOTI 5PM DOA |
| DOI | 10.1371/journal.pgen.1004264 |
| DatabaseName | CrossRef Medline MEDLINE MEDLINE (Ovid) MEDLINE MEDLINE PubMed Gale In Context: Opposing Viewpoints Gale In Context: Canada Gale In Context: Science MEDLINE - Academic OSTI.GOV - Hybrid OSTI.GOV PubMed Central (Full Participant titles) DOAJ Directory of Open Access Journals (ND) |
| DatabaseTitle | CrossRef MEDLINE Medline Complete MEDLINE with Full Text PubMed MEDLINE (Ovid) MEDLINE - Academic |
| DatabaseTitleList | MEDLINE MEDLINE - Academic |
| Database_xml | – sequence: 1 dbid: DOA name: Directory of Open Access Journals (DOAJ) url: https://www.doaj.org/ sourceTypes: Open Website – sequence: 2 dbid: NPM name: PubMed url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed sourceTypes: Index Database – sequence: 3 dbid: EIF name: MEDLINE url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search sourceTypes: Index Database |
| DeliveryMethod | fulltext_linktorsrc |
| Discipline | Biology |
| DocumentTitleAlternate | Genome-Scale Control Circuitry of Redox Metabolism |
| EISSN | 1553-7404 |
| ExternalDocumentID | 1525303470 oai_doaj_org_article_153a087e12cb4160b8fe3205ad081a5c PMC3974632 1904015 A368284218 24699140 10_1371_journal_pgen_1004264 |
| Genre | Research Support, U.S. Gov't, Non-P.H.S Journal Article Research Support, N.I.H., Extramural |
| GeographicLocations | United States |
| GeographicLocations_xml | – name: United States |
| GrantInformation_xml | – fundername: NIGMS NIH HHS grantid: R01 GM062791 – fundername: NIGMS NIH HHS grantid: GM062791 |
| GroupedDBID | --- 123 29O 2WC 53G 5VS 7X7 88E 8FE 8FH 8FI 8FJ AAFWJ AAUCC AAWOE AAYXX ABDBF ABUWG ACGFO ACIHN ACIWK ACPRK ACUHS ADBBV ADRAZ AEAQA AENEX AFKRA AFPKN AHMBA ALIPV ALMA_UNASSIGNED_HOLDINGS AOIJS B0M BAWUL BBNVY BCNDV BENPR BHPHI BPHCQ BVXVI BWKFM CCPQU CITATION CS3 DIK DU5 E3Z EAP EAS EBD EBS EJD EMK EMOBN ESX F5P FPL FYUFA GROUPED_DOAJ GX1 HCIFZ HMCUK HYE IAO IGS IHR IHW INH INR IOV ISN ISR ITC KQ8 LK8 M1P M48 M7P O5R O5S OK1 OVT P2P PHGZM PHGZT PIMPY PQQKQ PROAC PSQYO QF4 QN7 RNS RPM SV3 TR2 TUS UKHRP WOW XSB ~8M C1A CGR CUY CVF ECM EIF H13 IPNFZ NPM PJZUB PPXIY PQGLB PV9 RIG RZL WOQ PMFND 7X8 3V. AAPBV ABPTK M~E OIOZB OTOTI PQEST PQUKI 5PM PUEGO - ADACO BBAFP PRINS |
| ID | FETCH-LOGICAL-c725t-e0fe28ea734c26953594bd98d26a9e0e52d34e3ec5ac39c60f3e4c2a25f0aa213 |
| IEDL.DBID | DOA |
| ISSN | 1553-7404 1553-7390 |
| IngestDate | Fri Nov 26 17:13:36 EST 2021 Wed Aug 27 01:19:09 EDT 2025 Thu Aug 21 14:05:37 EDT 2025 Mon Jul 17 03:59:00 EDT 2023 Fri Jul 11 10:01:11 EDT 2025 Tue Jun 17 21:11:51 EDT 2025 Tue Jun 10 20:32:48 EDT 2025 Fri Jun 27 04:12:46 EDT 2025 Fri Jun 27 05:03:57 EDT 2025 Fri Jun 27 04:41:42 EDT 2025 Thu May 22 21:15:41 EDT 2025 Mon Jul 21 05:42:40 EDT 2025 Tue Jul 01 04:24:05 EDT 2025 Thu Apr 24 22:53:45 EDT 2025 |
| IsDoiOpenAccess | true |
| IsOpenAccess | true |
| IsPeerReviewed | true |
| IsScholarly | true |
| Issue | 4 |
| Language | English |
| License | This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited. Creative Commons Attribution License |
| LinkModel | DirectLink |
| MergedId | FETCHMERGED-LOGICAL-c725t-e0fe28ea734c26953594bd98d26a9e0e52d34e3ec5ac39c60f3e4c2a25f0aa213 |
| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 FOA-0000143; GM062791 National Institutes of Health (NIH) USDOE Office of Science (SC), Biological and Environmental Research (BER) Current address: Department of Biological Sciences, Korea Advanced Institute of Science and Technology, Daejoen, Korea. Conceived and designed the experiments: SF BP BkC. Performed the experiments: BkC DK. Analyzed the data: SF BkC JL KZ. Contributed reagents/materials/analysis tools: SF AE HN. Wrote the paper: SF JL KZ BP. Current address: Genomatica, Inc., San Diego, California, United States of America. The authors have declared that no competing interests exist. |
| OpenAccessLink | https://doaj.org/article/153a087e12cb4160b8fe3205ad081a5c |
| PMID | 24699140 |
| PQID | 1513051237 |
| PQPubID | 23479 |
| ParticipantIDs | plos_journals_1525303470 doaj_primary_oai_doaj_org_article_153a087e12cb4160b8fe3205ad081a5c pubmedcentral_primary_oai_pubmedcentral_nih_gov_3974632 osti_scitechconnect_1904015 proquest_miscellaneous_1513051237 gale_infotracmisc_A368284218 gale_infotracacademiconefile_A368284218 gale_incontextgauss_ISR_A368284218 gale_incontextgauss_ISN_A368284218 gale_incontextgauss_IOV_A368284218 gale_healthsolutions_A368284218 pubmed_primary_24699140 crossref_primary_10_1371_journal_pgen_1004264 crossref_citationtrail_10_1371_journal_pgen_1004264 |
| ProviderPackageCode | CITATION AAYXX |
| PublicationCentury | 2000 |
| PublicationDate | 2014-04-01 |
| PublicationDateYYYYMMDD | 2014-04-01 |
| PublicationDate_xml | – month: 04 year: 2014 text: 2014-04-01 day: 01 |
| PublicationDecade | 2010 |
| PublicationPlace | United States |
| PublicationPlace_xml | – name: United States – name: San Francisco, USA |
| PublicationTitle | PLoS genetics |
| PublicationTitleAlternate | PLoS Genet |
| PublicationYear | 2014 |
| Publisher | Public Library of Science Public Library of Science (PLoS) |
| Publisher_xml | – name: Public Library of Science – name: Public Library of Science (PLoS) |
| References | G Unden (ref4) 2008; 79 DF Browning (ref39) 2004; 2 K Kochanowski (ref33) 2013; 110 P Kiley (ref13) 1998 JD Partridge (ref34) 2007; 282 K Patil (ref41) 2005; 102 B-K Cho (ref44) 2006; 40 J Green (ref1) 2004; 2 MD Rolfe (ref3) 2011; 286 DP Clark (ref30) 2005 R Carlson (ref20) 2004; 86 E Noor (ref19) 2010; 39 EW Trotter (ref6) 2011; 6 C Constantinidou (ref5) 2006; 281 JA Lerman (ref36) 2012; 3 R Gourse (ref47) 2000; 37 S Iuchi (ref8) 1996; 120 U Sauer (ref32) 2003; 279 S Estrem (ref27) 1999; 13 BK Cho (ref45) 2008; 105 S Iuchi (ref7) 1993; 9 NE Lewis (ref49) 2010; 6 O Chumsakul (ref29) 2011; 39 R Malpica (ref12) 2004; 101 J Schellenberger (ref50) 2011; 6 ref40 G Semenza (ref43) 2012; 148 S Gama-Castro (ref24) 2010; 39 RBH van Rijsewijk Bart (ref35) 2011; 7 M Cosentino Lagomarsino (ref38) 2007; 104 K Robison (ref22) 1998; 284 S Iuchi (ref2) 1991; 66 S Achebach (ref15) 2005; 272 G Unden (ref14) 2002; 4 E Sharon (ref48) 2012; 30 M Bostock (ref46) 2011 JD Orth (ref31) 2011; 7 IM Keseler (ref26) 2010; 39 JD Partridge (ref11) 2006; 281 DM Park (ref16) 2013; 9 CF Beck (ref28) 1988; 52 S Alexeeva (ref9) 2003; 185 R Carlson (ref17) 2003; 85 TA Krulwich (ref37) 2011; 9 R Schuetz (ref18) 2012; 336 TL Bailey (ref21) 2009; 37 KS Myers (ref25) 2013; 9 S Shalel Levanon (ref10) 2005; 89 N-M Gruning (ref42) 2010; 35 F Perez (ref51) 2007; 9 AM McGuire (ref23) 1999; 32 |
| References_xml | – volume: 279 start-page: 6613 year: 2003 ident: ref32 article-title: The Soluble and Membrane-bound Transhydrogenases UdhA and PntAB Have Divergent Functions in NADPH Metabolism of Escherichia coli publication-title: Journal of Biological Chemistry doi: 10.1074/jbc.M311657200 – volume: 7 start-page: 1 year: 2011 ident: ref35 article-title: Large-scale 13C-flux analysis reveals distinct transcriptional control of respiratory and fermentative metabolism in Escherichia coli publication-title: Mol Syst Biol – volume: 37 start-page: 687 issue: 4 year: 2000 ident: ref47 article-title: UPs and downs in bacterial transcription initiation: the role of the alpha subunit of RNA polymerase in promoter recognition publication-title: Mol Microbiol doi: 10.1046/j.1365-2958.2000.01972.x – year: 1998 ident: ref13 article-title: Oxygen sensing by the global regulator, FNR: the role of the iron-sulfur cluster publication-title: FEMS Microbiology Reviews – volume: 102 start-page: 2685 year: 2005 ident: ref41 article-title: Uncovering transcriptional regulation of metabolism by using metabolic network topology publication-title: Proceedings of the National Academy of Sciences doi: 10.1073/pnas.0406811102 – volume: 281 start-page: 4802 year: 2006 ident: ref5 article-title: A reassessment of the FNR regulon and transcriptomic analysis of the effects of nitrate, nitrite, NarXL, and NarQP as Escherichia coli K12 adapts from aerobic to nitrate respiration publication-title: The Journal of biological chemistry doi: 10.1074/jbc.M512312200 – volume: 101 start-page: 13318 year: 2004 ident: ref12 article-title: Identification of a quinone-sensitive redox switch in the ArcB sensor kinase publication-title: Proceedings of the National Academy of Sciences doi: 10.1073/pnas.0403064101 – volume: 35 start-page: 220 year: 2010 ident: ref42 article-title: Regulatory crosstalk of the metabolic network publication-title: Trends in Biochemical Sciences doi: 10.1016/j.tibs.2009.12.001 – year: 2005 ident: ref30 article-title: Two-carbon compounds and fatty acids as carbon sources doi: 10.1128/ecosalplus.3.4.4 – volume: 39 start-page: D583 year: 2010 ident: ref26 article-title: EcoCyc: a comprehensive database of Escherichia coli biology publication-title: Nucleic acids research doi: 10.1093/nar/gkq1143 – volume: 52 start-page: 318 year: 1988 ident: ref28 article-title: Divergent Promoters, a Common Form of Gene Organization publication-title: Microbiological reviews doi: 10.1128/MMBR.52.3.318-326.1988 – volume: 110 start-page: 1130 year: 2013 ident: ref33 article-title: Functioning of a metabolic flux sensor in Escherichia coli publication-title: Proceedings of the National Academy of Sciences doi: 10.1073/pnas.1202582110 – volume: 148 start-page: 399 year: 2012 ident: ref43 article-title: Hypoxia-Inducible Factors in Physiology and Medicine publication-title: Cell doi: 10.1016/j.cell.2012.01.021 – volume: 4 start-page: 263 issue: 3 year: 2002 ident: ref14 article-title: Control of FNR Function of Escherichia coli by O2 and Reducing Conditions publication-title: Journal of molecular microbiolog – volume: 85 start-page: 1 year: 2003 ident: ref17 article-title: Fundamental Escherichia coli biochemical pathways for biomass and energy production: Identification of reactions publication-title: Biotechnol Bioeng doi: 10.1002/bit.10812 – volume: 39 start-page: 414 issue: 2 year: 2011 ident: ref29 article-title: Genome-wide binding profiles of the Bacillus subtilis transition state regulator AbrB and its homolog Abh reveals their interactive role in transcriptional regulation publication-title: Nucleic acids Research doi: 10.1093/nar/gkq780 – ident: ref40 – volume: 66 start-page: 5 year: 1991 ident: ref2 article-title: Adaptation of Escherichia coli to respiratory conditions: regulation of gene expression publication-title: Cell doi: 10.1016/0092-8674(91)90130-Q – volume: 7 year: 2011 ident: ref31 article-title: A comprehensive genome-scale reconstruction of Escherichia coli metabolism—2011 publication-title: Mol Syst Biol – volume: 9 start-page: 9 year: 1993 ident: ref7 article-title: Adaptation of Escherichia coli to redox environments by gene expression publication-title: Mol Microbiol doi: 10.1111/j.1365-2958.1993.tb01664.x – volume: 2 start-page: 57 year: 2004 ident: ref39 article-title: The regulation of bacterial transcription initiation publication-title: Nat Rev Micro doi: 10.1038/nrmicro787 – volume: 32 start-page: 219 year: 1999 ident: ref23 article-title: A weight matrix for binding recognition by the redox-response regulator ArcA-P of Escherichia coli publication-title: Mol Microbiol doi: 10.1046/j.1365-2958.1999.01347.x – volume: 89 start-page: 556 year: 2005 ident: ref10 article-title: Effect of oxygen on the Escherichia coli ArcA and FNR regulation systems and metabolic responses publication-title: Biotechnol Bioeng doi: 10.1002/bit.20381 – volume: 86 start-page: 149 year: 2004 ident: ref20 article-title: Fundamental Escherichia coli biochemical pathways for biomass and energy production: creation of overall flux states publication-title: Biotechnol Bioeng doi: 10.1002/bit.20044 – volume: 284 start-page: 241 year: 1998 ident: ref22 article-title: A comprehensive library of DNA-binding site matrices for 55 proteins applied to the complete Escherichia coli K-12 genome publication-title: J Mol Biol doi: 10.1006/jmbi.1998.2160 – volume: 105 start-page: 19462 year: 2008 ident: ref45 article-title: Genome-scale reconstruction of the Lrp regulatory network in Escherichia coli publication-title: Proceedings of the National Academy of Sciences doi: 10.1073/pnas.0807227105 – volume: 6 start-page: e25501 year: 2011 ident: ref6 article-title: Reprogramming of Escherichia coli K-12 Metabolism during the Initial Phase of Transition from an Anaerobic to a Micro-Aerobic Environment publication-title: PLoS ONE doi: 10.1371/journal.pone.0025501 – volume: 104 start-page: 5516 year: 2007 ident: ref38 article-title: Hierarchy and feedback in the evolution of the Escherichia coli transcription network publication-title: Proceedings of the National Academy of Sciences doi: 10.1073/pnas.0609023104 – volume: 185 start-page: 204 issue: 1 year: 2003 ident: ref9 article-title: Requirement of ArcA for Redox Regulation in Escherichia coli under Microaerobic but Not Anaerobic or Aerobic Conditions publication-title: Journal of Bacteriology doi: 10.1128/JB.185.1.204-209.2003 – volume: 9 start-page: e1003839 year: 2013 ident: ref16 article-title: The Bacterial Response Regulator ArcA Uses a Diverse Binding Site Architecture to Regulate Carbon Oxidation Globally publication-title: PLoS Genet doi: 10.1371/journal.pgen.1003839 – volume: 2 start-page: 954 year: 2004 ident: ref1 article-title: Bacterial redox sensors publication-title: Nat Rev Micro doi: 10.1038/nrmicro1022 – volume: 6 start-page: 390 year: 2010 ident: ref49 article-title: Omic data from evolved E. coli are consistent with computed optimal growth from genome-scale models publication-title: Mol Syst Biol doi: 10.1038/msb.2010.47 – volume: 40 start-page: 67 issue: 1 year: 2006 ident: ref44 article-title: PCR-based tandem epitope tagging system for Escherichia coli genome engineering publication-title: Biotechniques doi: 10.2144/000112039 – volume: 9 start-page: 330 year: 2011 ident: ref37 article-title: Molecular aspects of bacterial pH sensing and homeostasis publication-title: Nat Rev Micro doi: 10.1038/nrmicro2549 – volume: 281 start-page: 27806 year: 2006 ident: ref11 article-title: Escherichia coli transcriptome dynamics during the transition from anaerobic to aerobic conditions publication-title: The Journal of biological chemistry doi: 10.1074/jbc.M603450200 – volume: 30 start-page: 521 year: 2012 ident: ref48 article-title: Inferring gene regulatory logic from high-throughput measurements of thousands of systematically designed promoters publication-title: Nat Biotechnol doi: 10.1038/nbt.2205 – volume: 286 start-page: 10147 year: 2011 ident: ref3 article-title: Transcript Profiling and Inference of Escherichia coli K-12 ArcA Activity across the Range of Physiologically Relevant Oxygen Concentrations publication-title: Journal of Biological Chemistry doi: 10.1074/jbc.M110.211144 – volume: 39 start-page: D98 year: 2010 ident: ref24 article-title: RegulonDB version 7.0: transcriptional regulation of Escherichia coli K-12 integrated within genetic sensory response units (Gensor Units) publication-title: Nucleic acids research doi: 10.1093/nar/gkq1110 – volume: 9 start-page: 21 year: 2007 ident: ref51 article-title: IPython: A System for Interactive Scientific Computing publication-title: Comput Sci Eng doi: 10.1109/MCSE.2007.53 – volume: 13 start-page: 2134 year: 1999 ident: ref27 article-title: Bacterial promoter architecture: subsite structure of UP elements and interactions with the carboxy-terminal domain of the RNA polymerase α subunit publication-title: Genes & Development doi: 10.1101/gad.13.16.2134 – volume: 6 start-page: 1290 year: 2011 ident: ref50 article-title: Quantitative prediction of cellular metabolism with constraint-based models: the COBRA Toolbox v2.0 publication-title: Nat Protoc doi: 10.1038/nprot.2011.308 – volume: 9 start-page: e1003565 year: 2013 ident: ref25 article-title: Genome-scale Analysis of Escherichia coli FNR Reveals Complex Features of Transcription Factor Binding publication-title: PLoS Genet doi: 10.1371/journal.pgen.1003565 – volume: 272 start-page: 4260 year: 2005 ident: ref15 article-title: Properties and significance of apoFNR as a second form of air-inactivated [4Fe-4S]·FNR of Escherichia coli publication-title: FEBS Journal doi: 10.1111/j.1742-4658.2005.04840.x – volume: 336 start-page: 597 year: 2012 ident: ref18 article-title: Multidimensional Optimality of Microbial Metabolism publication-title: Science doi: 10.1126/science.1216882 – volume: 282 start-page: 11230 year: 2007 ident: ref34 article-title: Transition of Escherichia coli from Aerobic to Micro-aerobic Conditions Involves Fast and Slow Reacting Regulatory Components publication-title: Journal of Biological Chemistry doi: 10.1074/jbc.M700728200 – start-page: 1 year: 2011 ident: ref46 article-title: Data-Driven Documents publication-title: Data-Driven Documents – volume: 120 start-page: 1055 year: 1996 ident: ref8 article-title: Cellular and molecular physiology of Escherichia coli in the adaptation to aerobic environments publication-title: J Biochem doi: 10.1093/oxfordjournals.jbchem.a021519 – volume: 3 start-page: 929 year: 2012 ident: ref36 article-title: In silico method for modelling metabolism and gene product expression at genome scale publication-title: Nat Comms doi: 10.1038/ncomms1928 – volume: 37 start-page: W202 year: 2009 ident: ref21 article-title: MEME SUITE: tools for motif discovery and searching publication-title: Nucleic acids research doi: 10.1093/nar/gkp335 – volume: 39 start-page: 809 year: 2010 ident: ref19 article-title: Central Carbon Metabolism as a Minimal Biochemical Walk between Precursors for Biomass and Energy publication-title: Molecular Cell doi: 10.1016/j.molcel.2010.08.031 – volume: 79 start-page: 4218 year: 2008 ident: ref4 article-title: The Aerobic and Anaerobic Respiratory Chain of Escherichia coli and Salmonella enterica: Enzymes and Energetics publication-title: Ecosal |
| SSID | ssj0035897 |
| Score | 2.3522744 |
| Snippet | Determining how facultative anaerobic organisms sense and direct cellular responses to electron acceptor availability has been a subject of intense study.... Determining how facultative anaerobic organisms sense and direct cellular responses to electron acceptor availability has been a subject of intense study.... |
| SourceID | plos doaj pubmedcentral osti proquest gale pubmed crossref |
| SourceType | Open Website Open Access Repository Aggregation Database Index Database Enrichment Source |
| StartPage | e1004264 |
| SubjectTerms | Anaerobiosis - genetics BASIC BIOLOGICAL SCIENCES Biology and Life Sciences Computer and Information Sciences E coli Electron Transport - genetics Electrons Energy Metabolism - genetics enzyme regulation Enzymes Escherichia coli - genetics Escherichia coli Proteins - genetics Experiments Gene expression Gene Expression Regulation, Bacterial - genetics gene regulation Gene Regulatory Networks - genetics Genetic aspects Genetic research Genomes genomics metabolic networks Metabolism Metabolism - genetics Metabolites Neural circuitry Neurological research Nitrates Oxidation-Reduction oxidation-reduction reactions Transcription factors Transcription Factors - genetics Transcription, Genetic - genetics transcriptional control |
| SummonAdditionalLinks | – databaseName: Scholars Portal Journals: Open Access dbid: M48 link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV1Lb9QwELbKIiQuqDwbWiAgJE6pEj-TA0LlUbVILRKwqDfLcZyy0m5SNlmp--87k3gjgorogcseNp9zGM94vlHG3xDyushUrnhqoTYxEn-SKCsLqFJsLhg1mcm78W0np_Joyj-fibMtspnZ6g3YXFva4Typ6XK-f_lr_Q4C_m03tUElm0X7F2By_OqPSf4WuQ25SWGonvDhuwITaT9uRQgWKSj3_WW6v71llKw6Tf_h5J7UEIKoiDqvm-vY6Z9Nlr9lrcNtcs_TzfCg94_7ZMtVD8idfgDl-iE5_ui7YSCBhUAFQ9-5HtrZ0q5m7XId1mWImqKX4cK14DDzWbMITduBUd914aIGttk9ItPDT98_HEV-uEJkFRVt5OLS0dQZxbilMhNMZDwvsrSg0mQudoIWjDvmrDCWZVbGJXOANFSUsTE0YY_JpKort0NCWqQylyaNuY0h1zksioA5JjLHm7eOBoRtrKitVx7HARhz3X1OU1CB9NbQaHvtbR-QaFh10Stv_AP_HjdowKJudvdHvTzXPgw1nO8mTpVLqM2BisZ5WjpGY2EKoEZG2IC8wO3V_SXUIfr1AZNQmnLgQwF51SFQO6PC5pxzs2oaffzlxw1A305vAvo6Ar3xoLIGm1njb02A5VG4a4TcGyHhmLCjx7vosRqIFaoDW2yjsq0GPggVtgjIDjryxrCNxrFYwG64igPycuPcGt-JTXmVq1eIAQIEhJGpgDzpnX2wPuUSKg8Oq9UoDEbbM35SzX528ubAkLlk9On_2M9dchcYrm-12iOTdrlyz4BFtvnz7mC4Ao-Ibg8 priority: 102 providerName: Scholars Portal |
| Title | Determining the Control Circuitry of Redox Metabolism at the Genome-Scale |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/24699140 https://www.proquest.com/docview/1513051237 https://www.osti.gov/servlets/purl/1904015 https://pubmed.ncbi.nlm.nih.gov/PMC3974632 https://doaj.org/article/153a087e12cb4160b8fe3205ad081a5c http://dx.doi.org/10.1371/journal.pgen.1004264 |
| Volume | 10 |
| hasFullText | 1 |
| inHoldings | 1 |
| isFullTextHit | |
| isPrint | |
| link | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV3fa9RAEF70RPBF_N3YekYRfIpN9mfy2GpLK_SUauXels1mowd3SbnkwP73ziR7oRGhffAlD5cvgczM7nzDzX5DyLsiU7niqYXaxEi8JFFWFlCl2FwwajKTd-Pbzmby5IJ_nov5tVFf2BPWywP3htuHFWniVLmE2hzIQ5ynpWM0FqaAZGaExd0Xct62mOr3YCbSfqyKECxSUNb7Q3NMJfveRx8uwUHYI4CUYJSUOu3-YYee1LDUUPl0WTf_YqF_N1Ney07Hj8hDTyvDg_5zHpM7rnpC7veDJq-ektNPvusFElUIlC_0HeqhXaztZtGur8K6DFE79He4ci0ExnLRrELTdmDUcV25qAF3umfk4vjo-8eTyA9RiKyioo1cXDqaOqMYt1RmgomM50WWFlSazMVO0IJxx5wVxrLMyrhkDpCGijI2hibsOZlUdeV2SEiLVObSpDG3MeQ0h8UPMMRE5njC1tGAsK0VtfUK4zjoYqm7v80UVBq9NTTaXnvbByQanrrsFTZuwB-igwYs6mN3P0DUaB81-qaoCchrdK_uD5sOq1wfMAklKAfeE5C3HQI1MipswvlpNk2jT7_8uAXo2-w2oPMR6L0HlTXYzBp_OgIsjwJdI-TeCAnbgR3d3sWI1UCgUAXYYruUbTXwPqikRUB2MJC3hm00jr8CFsNVHJA32-DW-E5svqtcvUEMEB0ghkwF5EUf7IP1KZdQYXB4Wo2Wwcg94zvV4lcnYw5MmEtGX_4Pf-6SB8BkfUvVHpm06417BWyxzafkrpqrKbl3eDT7ej7ttgm4nvH0D3jFZuY |
| linkProvider | Directory of Open Access Journals |
| openUrl | ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Determining+the+control+circuitry+of+redox+metabolism+at+the+genome-scale&rft.jtitle=PLoS+genetics&rft.au=Stephen+Federowicz&rft.au=Donghyuk+Kim&rft.au=Ali+Ebrahim&rft.au=Joshua+Lerman&rft.date=2014-04-01&rft.pub=Public+Library+of+Science+%28PLoS%29&rft.issn=1553-7390&rft.eissn=1553-7404&rft.volume=10&rft.issue=4&rft.spage=e1004264&rft_id=info:doi/10.1371%2Fjournal.pgen.1004264&rft.externalDBID=DOA&rft.externalDocID=oai_doaj_org_article_153a087e12cb4160b8fe3205ad081a5c |
| thumbnail_l | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1553-7404&client=summon |
| thumbnail_m | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1553-7404&client=summon |
| thumbnail_s | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1553-7404&client=summon |