Interaction of storage carbohydrates and other cyclic fluxes with central metabolism: A quantitative approach by non-stationary 13C metabolic flux analysis
13C labeling experiments in aerobic glucose limited cultures of Saccharomyces cerevisiae at four different growth rates (0.054; 0.101, 0.207, 0.307h−1) are used for calculating fluxes that include intracellular cycles (e.g., storage carbohydrate cycles, exchange fluxes with amino acids), which are r...
Saved in:
| Published in | Metabolic engineering communications Vol. 3; pp. 52 - 63 |
|---|---|
| Main Authors | , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Elsevier B.V
01.12.2016
Elsevier |
| Subjects | |
| Online Access | Get full text |
| ISSN | 2214-0301 2214-0301 |
| DOI | 10.1016/j.meteno.2016.01.001 |
Cover
Loading…
| Abstract | 13C labeling experiments in aerobic glucose limited cultures of Saccharomyces cerevisiae at four different growth rates (0.054; 0.101, 0.207, 0.307h−1) are used for calculating fluxes that include intracellular cycles (e.g., storage carbohydrate cycles, exchange fluxes with amino acids), which are rearranged depending on the growth rate. At low growth rates the impact of the storage carbohydrate recycle is relatively more significant than at high growth rates due to a higher concentration of these materials in the cell (up to 560-fold) and higher fluxes relative to the glucose uptake rate (up to 16%). Experimental observations suggest that glucose can be exported to the extracellular space, and that its source is related to storage carbohydrates, most likely via the export and subsequent extracellular breakdown of trehalose. This hypothesis is strongly supported by 13C-labeling experimental data, measured extracellular trehalose, and the corresponding flux estimations.
•Cyclic fluxes between large metabolite pools and central C-metabolism are studied.•Cyclic fluxes are rearranged depending on growth rate.•Impact of storage carbohydrate recycle is more significant at low growth rates.•Impact of exchange fluxes with amino acids is more significant at high growth rates.•Trehalose export and degradation seem to play a major role in glucose recycle. |
|---|---|
| AbstractList | 13
C labeling experiments in aerobic glucose limited cultures of
Saccharomyces cerevisiae
at four different growth rates (0.054; 0.101, 0.207, 0.307 h
−1
) are used for calculating fluxes that include intracellular cycles (e.g., storage carbohydrate cycles, exchange fluxes with amino acids), which are rearranged depending on the growth rate. At low growth rates the impact of the storage carbohydrate recycle is relatively more significant than at high growth rates due to a higher concentration of these materials in the cell (up to 560-fold) and higher fluxes relative to the glucose uptake rate (up to 16%). Experimental observations suggest that glucose can be exported to the extracellular space, and that its source is related to storage carbohydrates, most likely via the export and subsequent extracellular breakdown of trehalose. This hypothesis is strongly supported by
13
C-labeling experimental data, measured extracellular trehalose, and the corresponding flux estimations.
•
Cyclic fluxes between large metabolite pools and central C-metabolism are studied.
•
Cyclic fluxes are rearranged depending on growth rate.
•
Impact of storage carbohydrate recycle is more significant at low growth rates.
•
Impact of exchange fluxes with amino acids is more significant at high growth rates.
•
Trehalose export and degradation seem to play a major role in glucose recycle. 13C labeling experiments in aerobic glucose limited cultures of Saccharomyces cerevisiae at four different growth rates (0.054; 0.101, 0.207, 0.307 h-1) are used for calculating fluxes that include intracellular cycles (e.g., storage carbohydrate cycles, exchange fluxes with amino acids), which are rearranged depending on the growth rate. At low growth rates the impact of the storage carbohydrate recycle is relatively more significant than at high growth rates due to a higher concentration of these materials in the cell (up to 560-fold) and higher fluxes relative to the glucose uptake rate (up to 16%). Experimental observations suggest that glucose can be exported to the extracellular space, and that its source is related to storage carbohydrates, most likely via the export and subsequent extracellular breakdown of trehalose. This hypothesis is strongly supported by 13C-labeling experimental data, measured extracellular trehalose, and the corresponding flux estimations.13C labeling experiments in aerobic glucose limited cultures of Saccharomyces cerevisiae at four different growth rates (0.054; 0.101, 0.207, 0.307 h-1) are used for calculating fluxes that include intracellular cycles (e.g., storage carbohydrate cycles, exchange fluxes with amino acids), which are rearranged depending on the growth rate. At low growth rates the impact of the storage carbohydrate recycle is relatively more significant than at high growth rates due to a higher concentration of these materials in the cell (up to 560-fold) and higher fluxes relative to the glucose uptake rate (up to 16%). Experimental observations suggest that glucose can be exported to the extracellular space, and that its source is related to storage carbohydrates, most likely via the export and subsequent extracellular breakdown of trehalose. This hypothesis is strongly supported by 13C-labeling experimental data, measured extracellular trehalose, and the corresponding flux estimations. 13C labeling experiments in aerobic glucose limited cultures of Saccharomyces cerevisiae at four different growth rates (0.054; 0.101, 0.207, 0.307 h−1) are used for calculating fluxes that include intracellular cycles (e.g., storage carbohydrate cycles, exchange fluxes with amino acids), which are rearranged depending on the growth rate. At low growth rates the impact of the storage carbohydrate recycle is relatively more significant than at high growth rates due to a higher concentration of these materials in the cell (up to 560-fold) and higher fluxes relative to the glucose uptake rate (up to 16%). Experimental observations suggest that glucose can be exported to the extracellular space, and that its source is related to storage carbohydrates, most likely via the export and subsequent extracellular breakdown of trehalose. This hypothesis is strongly supported by 13C-labeling experimental data, measured extracellular trehalose, and the corresponding flux estimations. Keywords: Non-stationary 13C labeling, Flux estimation, Trehalose, Glycogen, Amino acids 13C labeling experiments in aerobic glucose limited cultures of Saccharomyces cerevisiae at four different growth rates (0.054; 0.101, 0.207, 0.307h−1) are used for calculating fluxes that include intracellular cycles (e.g., storage carbohydrate cycles, exchange fluxes with amino acids), which are rearranged depending on the growth rate. At low growth rates the impact of the storage carbohydrate recycle is relatively more significant than at high growth rates due to a higher concentration of these materials in the cell (up to 560-fold) and higher fluxes relative to the glucose uptake rate (up to 16%). Experimental observations suggest that glucose can be exported to the extracellular space, and that its source is related to storage carbohydrates, most likely via the export and subsequent extracellular breakdown of trehalose. This hypothesis is strongly supported by 13C-labeling experimental data, measured extracellular trehalose, and the corresponding flux estimations. •Cyclic fluxes between large metabolite pools and central C-metabolism are studied.•Cyclic fluxes are rearranged depending on growth rate.•Impact of storage carbohydrate recycle is more significant at low growth rates.•Impact of exchange fluxes with amino acids is more significant at high growth rates.•Trehalose export and degradation seem to play a major role in glucose recycle. ¹³C labeling experiments in aerobic glucose limited cultures of Saccharomyces cerevisiae at four different growth rates (0.054; 0.101, 0.207, 0.307h⁻¹) are used for calculating fluxes that include intracellular cycles (e.g., storage carbohydrate cycles, exchange fluxes with amino acids), which are rearranged depending on the growth rate. At low growth rates the impact of the storage carbohydrate recycle is relatively more significant than at high growth rates due to a higher concentration of these materials in the cell (up to 560-fold) and higher fluxes relative to the glucose uptake rate (up to 16%). Experimental observations suggest that glucose can be exported to the extracellular space, and that its source is related to storage carbohydrates, most likely via the export and subsequent extracellular breakdown of trehalose. This hypothesis is strongly supported by ¹³C-labeling experimental data, measured extracellular trehalose, and the corresponding flux estimations. |
| Author | Hanemaaijer, M. ten Pierick, Angela Heijnen, J.J. Suarez-Mendez, C.A. Wolters, J.C. Wahl, S.A. |
| AuthorAffiliation | c Department of Analytical Biochemistry, University of Groningen, Antonius Deusinglaan 1, 9713 AV Groningen, The Netherlands b Kluyver Centre for Genomics of Industrial Fermentation, P.O. Box 5057, 2600 GA Delft, The Netherlands a Department of Biotechnology, Delft University of Technology, Julianalaan 67 – 2628 BC Delft, The Netherlands |
| AuthorAffiliation_xml | – name: c Department of Analytical Biochemistry, University of Groningen, Antonius Deusinglaan 1, 9713 AV Groningen, The Netherlands – name: a Department of Biotechnology, Delft University of Technology, Julianalaan 67 – 2628 BC Delft, The Netherlands – name: b Kluyver Centre for Genomics of Industrial Fermentation, P.O. Box 5057, 2600 GA Delft, The Netherlands |
| Author_xml | – sequence: 1 givenname: C.A. surname: Suarez-Mendez fullname: Suarez-Mendez, C.A. email: casuarezmendez@unal.edu.co organization: Department of Biotechnology, Delft University of Technology, Julianalaan 67 – 2628 BC Delft, The Netherlands – sequence: 2 givenname: M. surname: Hanemaaijer fullname: Hanemaaijer, M. organization: Department of Biotechnology, Delft University of Technology, Julianalaan 67 – 2628 BC Delft, The Netherlands – sequence: 3 givenname: Angela surname: ten Pierick fullname: ten Pierick, Angela organization: Department of Biotechnology, Delft University of Technology, Julianalaan 67 – 2628 BC Delft, The Netherlands – sequence: 4 givenname: J.C. surname: Wolters fullname: Wolters, J.C. organization: Department of Analytical Biochemistry, University of Groningen, Antonius Deusinglaan 1, 9713 AV Groningen, The Netherlands – sequence: 5 givenname: J.J. surname: Heijnen fullname: Heijnen, J.J. organization: Department of Biotechnology, Delft University of Technology, Julianalaan 67 – 2628 BC Delft, The Netherlands – sequence: 6 givenname: S.A. surname: Wahl fullname: Wahl, S.A. email: s.a.wahl@tudelft.nl organization: Department of Biotechnology, Delft University of Technology, Julianalaan 67 – 2628 BC Delft, The Netherlands |
| BookMark | eNqNkstuUzEQho9QES2lb8DCSzYJHp-bDwukKuISqRIbWFtje07i6MRObSeQZ-FlcUgEdMfK9sz4m39G_8vqygdPVfUa-Bw4dG838y1l8mEuymvOYc45PKtuhIBmxmsOV__cr6u7lDa8VNQdNAAvqmsxNJ0EqG-qn0ufKaLJLngWRpZyiLgiZjDqsD7aiJkSQ29ZyGuKzBzN5Awbp_2PEv_u8poZ8jnixIoi1GFyafuO3bPHPfrsMmZ3IIa7XQxo1kwfWZlklk7x4DEeGdSLPz_P3NINp2Ny6VX1fMQp0d3lvK2-ffzwdfF59vDl03Jx_zCzoh-aWQ26aXUjZGu4brSUKHUvrTWkJSEAaBxNhyQktrYWqFuQo9BmgA56lFjfVssz1wbcqF102yJMBXTqdyDElcKYnZlIwTByLqUZtOma0lB2Gix1tu9th0PbF9b7M2u311uyl908gT7NeLdWq3BQbd8Pfd0UwJsLIIbHPaWsti4Zmib0FPZJCc77RvCh-69SXp-w7V9ZVPZ4cBRVMo68IesimVwGdQq4OnlLbdTZW-rkLcVBnZzzCwOCyTw |
| ContentType | Journal Article |
| Copyright | 2016 The Authors 2016 The Authors 2016 |
| Copyright_xml | – notice: 2016 The Authors – notice: 2016 The Authors 2016 |
| DBID | 6I. AAFTH 7S9 L.6 7X8 5PM DOA |
| DOI | 10.1016/j.meteno.2016.01.001 |
| DatabaseName | ScienceDirect Open Access Titles Elsevier:ScienceDirect:Open Access AGRICOLA AGRICOLA - Academic MEDLINE - Academic PubMed Central (Full Participant titles) DOAJ Directory of Open Access Journals |
| DatabaseTitle | AGRICOLA AGRICOLA - Academic MEDLINE - Academic |
| DatabaseTitleList | MEDLINE - Academic AGRICOLA |
| Database_xml | – sequence: 1 dbid: DOA name: DOAJ Open Access Full Text url: https://www.doaj.org/ sourceTypes: Open Website |
| DeliveryMethod | fulltext_linktorsrc |
| Discipline | Engineering |
| EISSN | 2214-0301 |
| EndPage | 63 |
| ExternalDocumentID | oai_doaj_org_article_19f0088c9bc6485c86b1de6d77d6a957 PMC5779734 S2214030116300025 |
| GroupedDBID | 0R~ 0SF 4.4 457 5VS 6I. AACTN AAEDT AAEDW AAFTH AAIKJ AALRI AAXUO ABMAC ACGFS ADBBV ADEZE AEXQZ AFTJW AGHFR AITUG ALMA_UNASSIGNED_HOLDINGS AMRAJ AOIJS BCNDV EBS EJD FDB GROUPED_DOAJ HYE HZ~ IPNFZ KQ8 M41 M~E NCXOZ O9- OK1 RIG ROL RPM SSZ 7S9 AAHBH AAYWO ACVFH ADCNI ADVLN AEUPX AFJKZ AFPUW AIGII AKBMS AKRWK AKYEP L.6 7X8 5PM |
| ID | FETCH-LOGICAL-d2794-31b45b4285c0b4b88a8b78ddceb8ea111bafc6ae28a5d32ab518f2bc91617a8a3 |
| IEDL.DBID | DOA |
| ISSN | 2214-0301 |
| IngestDate | Wed Aug 27 01:15:38 EDT 2025 Thu Aug 21 18:10:52 EDT 2025 Fri Jul 11 11:28:34 EDT 2025 Fri Jul 11 11:33:48 EDT 2025 Wed May 17 02:14:19 EDT 2023 |
| IsDoiOpenAccess | true |
| IsOpenAccess | true |
| IsPeerReviewed | true |
| IsScholarly | true |
| Keywords | FBA GPM GLN DO Flux estimation PRO S7P UTP GLU X5P PFK FBP GLY E4P SUC UDP F6P IDMS GAPDH&PGK G6PDH METH 2PG AK DHAP 6PG OUR OAA T6P PGI TCA CoA GAP PGM MAL SER Trehalose Ribu5P RPE G1P ENO Amino acids RPI PPP Rib5P Iso-Cit TPP α-KG TPS ASP FUM G6P FMH UDPG PYK Glycogen LYS Non-stationary 13C labeling PYR 3PG ACO PMI ALA PEP LEU |
| Language | English |
| License | This is an open access article under the CC BY-NC-ND license. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). |
| LinkModel | DirectLink |
| MergedId | FETCHMERGED-LOGICAL-d2794-31b45b4285c0b4b88a8b78ddceb8ea111bafc6ae28a5d32ab518f2bc91617a8a3 |
| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Current address: Faculty of Sciences, VU University Amsterdam, de Boelelaan 1083-1081 HV Amsterdam, The Netherlands. Current address: Departamento de Procesos y Energia, Universidad Nacional de Colombia, Carrera 80 No. 65-223, Blq. M3, Medellin, Colombia. |
| OpenAccessLink | https://doaj.org/article/19f0088c9bc6485c86b1de6d77d6a957 |
| PMID | 29468113 |
| PQID | 2000377975 |
| PQPubID | 24069 |
| PageCount | 12 |
| ParticipantIDs | doaj_primary_oai_doaj_org_article_19f0088c9bc6485c86b1de6d77d6a957 pubmedcentral_primary_oai_pubmedcentral_nih_gov_5779734 proquest_miscellaneous_2007420964 proquest_miscellaneous_2000377975 elsevier_sciencedirect_doi_10_1016_j_meteno_2016_01_001 |
| PublicationCentury | 2000 |
| PublicationDate | 20161201 |
| PublicationDateYYYYMMDD | 2016-12-01 |
| PublicationDate_xml | – month: 12 year: 2016 text: 20161201 day: 01 |
| PublicationDecade | 2010 |
| PublicationTitle | Metabolic engineering communications |
| PublicationYear | 2016 |
| Publisher | Elsevier B.V Elsevier |
| Publisher_xml | – name: Elsevier B.V – name: Elsevier |
| References | de Jonge, Buijs, ten Pierick, Deshmukh, Zhao, Kiel, Heijnen, van Gulik (bib14) 2011; 6 Murphy, Dang, Young (bib30) 2013; 15 Canelas, ten Pierick, Ras, Seifar, van Dam, van Gulik, Heijnen (bib5) 2009; 81 François, Parrou (bib16) 2001; 25 Mashego, Wu, van Dam, Ras, Vinke, Van Winden, van Gulik, Heijnen (bib28) 2004; 85 Young, Shastri, Stephanopoulos, Morgan (bib66) 2011; 13 Van Gulik, Heijnen (bib48) 1995; 48 Bruinenberg, Van Dijken, Scheffers (bib3) 1983; 129 Conte, R. L., 2011. Optimization of a Glycogen and Trehalose Determination Method for Whole Yeast Cells. TU Delft Vallino, Stephanopoulos (bib46) 1993; 41 Van Hoek, Van Dijken, Pronk (bib50) 1998; 64 Aboka, van Winden, Reginald, van Gulik, van de Berg, Oudshoorn, Heijnen (bib2) 2012; 29 Daran, Dallies, Thines-Sempoux, Paquet, Francois (bib12) 1995; 233 Noh, Wahl, Wiechert (bib33) 2006; 8 Varma, Palsson (bib54) 1994; 12 Wu, Mashego, van Dam, Proell, Vinke, Ras, Van Winden, van Gulik, Heijnen (bib65) 2005; 336 Castrillo, Zeef, Hoyle, Zhang, Hayes, Gardner, Cornell, Petty, Hakes, Wardleworth (bib6) 2007; 6 Crown, Antoniewicz (bib9) 2013; 20 Haselbeck, McAlister-Henn (bib19) 1993; 268 Paalman, Verwaal, Slofstra, Verkleij, Boonstra, Verrips (bib34) 2003; 3 Minard, McAlister-Henn (bib29) 2005; 280 Wiechert (bib60) 2001; 3 Wiechert, De Graaf (bib61) 1997; 55 Lange, Heijnen (bib23) 2001; 75 Nöh, Grönke, Luo, Takors, Oldiges, Wiechert (bib32) 2007; 129 Stambuk, De Araujo, Panek, Serrano (bib45) 1996; 237 Wahl, Seifar, ten Pierick, Ras, van Dam, Heijnen, van Gulik (bib59) 2014; vol. 1191 Jules, Beltran, François, Parrou (bib22) 2008; 74 Zhao, Kuijvenhoven, Ras, van Gulik, Heijnen, Verheijen, van Winden (bib67) 2008; 10 Parrou, Jules, Beltran, François (bib35) 2005; 5 Van der Borght, Chen, Hoflack, Van Renterghem, Desmet, Soetaert (bib47) 2011; 77 Wahl, Nöh, Wiechert (bib57) 2008; 9 Wahl, Dauner, Wiechert (bib58) 2004; 85 Dauner, Bailey, Wiechert, Witholt, Sauer (bib13) 2000 Wiechert, Nöh (bib62) 2013; 24 Peng, Trumbly, Reimann (bib37) 1990; 265 Canelas, Ras, ten Pierick, van Gulik, Heijnen (bib4) 2011; 13 Guillou, Plourde-Owobi, Parrou, Goma, François (bib18) 2004; 4 van Heerden, Wortel, Bruggeman, Heijnen, Bollen, Planqué, Hulshof, O’Toole, Wahl, Teusink (bib49) 2014; 343 Parrou, Teste, Francois (bib36) 1997; 143 Seifar, Ras, van Dam, van Gulik, Heijnen, Van Winden (bib43) 2009; 388 Daran-Lapujade, Jansen, Daran, van Gulik, de Winde, Pronk (bib11) 2004; 279 Niedenführ, ten Pierick, van Dam, Suarez-Mendez, Nöh, Wahl (bib31) 2015 van Winden, Heijnen, Verheijen (bib51) 2002; 80 Jordà, Suarez, Carnicer, ten Pierick, Heijnen, van Gulik, Ferrer, Albiol, Wahl (bib21) 2013 Verheijen (bib55) 2010 Mashego, Jansen, Vinke, van Gulik, Heijnen (bib25) 2005; 5 Pereira, Eleutherio, Panek (bib38) 2001; 1 Schuetz, Kuepfer, Sauer (bib42) 2007; 3 Mashego, van Gulik, Vinke, Visser, Heijnen (bib27) 2006; 8 Shi, Sutter, Ye, Tu (bib44) 2010; 21 Cipollina, ten Pierick, Canelas, Seifar, van Maris, van Dam, Heijnen (bib7) 2009; 877 Wilson, Roach, Montero, Baroja-Fernández, Munoz, Eydallin, Viale, Pozueta-Romero (bib64) 2010; 34 Fischer, Sauer (bib15) 2005; 37 Schmidt, Marx, de Graaf, Wiechert, Sahm, Nielsen, Villadsen (bib41) 1998; 58 Willke, Vorlop (bib63) 2004; 66 Vanrolleghem, De Jong-Gubbels, Van Gulik, Pronk, Van Dijken, Heijnen (bib53) 1996; 12 Gombert, Dos Santos, Christensen, Nielsen (bib17) 2001; 183 Van Winden, Van Dam, Ras, Kleijn, Vinke, Van Gulik, Heijnen (bib52) 2005; 5 Aboka, Heijnen, Van Winden (bib1) 2009; 9 Voit (bib56) 2003; 223 Mashego, Van Gulik, Heijnen (bib26) 2007; 7 Schick, Haltrich, Kulbe (bib40) 1995; 43 Ryu, Kim, Kim, Chung, Lee (bib39) 2011; 46 Hashem, Darwish (bib20) 2010; 34 Loftus, Hall, Anderson, McAlister-Henn (bib24) 1994; 33 van Dam, Ras, ten Pierick (bib10) 2011; 708 |
| References_xml | – volume: vol. 1191 start-page: 91 year: 2014 end-page: 105 ident: bib59 article-title: Quantitative metabolomics using ID-MS publication-title: Metabolic Flux Analysis – volume: 75 start-page: 334 year: 2001 end-page: 344 ident: bib23 article-title: Statistical reconciliation of the elemental and molecular biomass composition of Saccharomyces cerevisiae publication-title: Biotechnol. Bioeng. – year: 2015 ident: bib31 article-title: Natural isotope correction of MS/MS measurements for metabolomics and publication-title: Biotechnol. Bioeng. – volume: 9 start-page: 191 year: 2009 end-page: 201 ident: bib1 article-title: Dynamic publication-title: FEMS Yeast Res. – volume: 77 start-page: 6939 year: 2011 end-page: 6944 ident: bib47 article-title: Enzymatic properties and substrate specificity of the trehalose phosphorylase from Caldanaerobacter subterraneus publication-title: Appl. Environ. Microbiol. – volume: 388 start-page: 213 year: 2009 end-page: 219 ident: bib43 article-title: Simultaneous quantification of free nucleotides in complex biological samples using ion pair reversed phase liquid chromatography isotope dilution tandem mass spectrometry publication-title: Anal. Biochem. – volume: 3 start-page: 195 year: 2001 end-page: 206 ident: bib60 article-title: C metabolic flux analysis publication-title: Metab. Eng. – reference: Conte, R. L., 2011. Optimization of a Glycogen and Trehalose Determination Method for Whole Yeast Cells. TU Delft – volume: 237 start-page: 876 year: 1996 end-page: 881 ident: bib45 article-title: Kinetics and energetics of trehalose transport in Saccharomyces cerevisiae publication-title: Eur. J. Biochem. – year: 2000 ident: bib13 article-title: Intracellular Carbon Flux Analysis by – volume: 8 start-page: 370 year: 2006 end-page: 383 ident: bib27 article-title: In vivo kinetics with rapid perturbation experiments in Saccharomyces cerevisiae using a second-generation BioScope publication-title: Metab. Eng. – volume: 81 start-page: 7379 year: 2009 end-page: 7389 ident: bib5 article-title: Quantitative evaluation of intracellular metabolite extraction techniques for yeast metabolomics publication-title: Anal. Chem. – volume: 34 start-page: 952 year: 2010 end-page: 985 ident: bib64 article-title: Regulation of glycogen metabolism in yeast and bacteria publication-title: FEMS Microbiol. Rev. – volume: 183 start-page: 1441 year: 2001 end-page: 1451 ident: bib17 article-title: Network identification and flux quantification in the central metabolism of Saccharomyces cerevisiae under different conditions of glucose repression publication-title: J. Bacteriol. – volume: 343 start-page: 1245114 year: 2014 ident: bib49 article-title: Lost in transition: startup of glycolysis yields subpopulations of nongrowing cells publication-title: Science – volume: 877 start-page: 3231 year: 2009 end-page: 3236 ident: bib7 article-title: A comprehensive method for the quantification of the non-oxidative pentose phosphate pathway intermediates in Saccharomyces cerevisiae by GC-IDMS publication-title: J. Chromatogr. B: Anal. Technol. Biomed. Life Sci. – volume: 12 start-page: 994 year: 1994 end-page: 998 ident: bib54 article-title: Metabolic flux balancing: basic concepts, scientific and practical use publication-title: Nat. Biotechnol. – volume: 20 start-page: 42 year: 2013 end-page: 48 ident: bib9 article-title: Publishing publication-title: Metab. Eng. – volume: 129 start-page: 249 year: 2007 end-page: 267 ident: bib32 article-title: Metabolic flux analysis at ultra short time scale: isotopically non-stationary publication-title: J. Biotechnol. – volume: 5 start-page: 559 year: 2005 end-page: 568 ident: bib52 article-title: Metabolic-flux analysis of Saccharomyces cerevisiae CEN.PK113-7D based on mass isotopomer measurements of publication-title: FEMS Yeast Res. – volume: 708 start-page: 131 year: 2011 end-page: 146 ident: bib10 article-title: Analysis of glycolytic intermediates with ion chromatography- and gas chromatography-mass spectrometry publication-title: Methods Mol. Biol. – volume: 268 start-page: 12116 year: 1993 end-page: 12122 ident: bib19 article-title: Function and expression of yeast mitochondrial NAD- and NADP-specific isocitrate dehydrogenases publication-title: J. Biol. Chem. – volume: 55 start-page: 101 year: 1997 end-page: 117 ident: bib61 article-title: Bidirectional reaction steps in metabolic networks: I. Modeling and simulation of carbon isotope labeling experiments publication-title: Biotechnol. Bioeng. – volume: 64 start-page: 4226 year: 1998 ident: bib50 article-title: Effect of specific growth rate on fermentative capacity of baker’s yeast publication-title: Appl. Environ. Microbiol. – volume: 13 start-page: 656 year: 2011 end-page: 665 ident: bib66 article-title: Mapping photoautotrophic metabolism with isotopically nonstationary publication-title: Metab. Eng. – volume: 6 start-page: 4 year: 2007 ident: bib6 article-title: Growth control of the eukaryote cell: a systems biology study in yeast publication-title: J. Biol. – volume: 6 start-page: 944 year: 2011 end-page: 958 ident: bib14 article-title: Scale-down of penicillin production in Penicillium chrysogenum publication-title: Biotechnol. J – volume: 1 start-page: 11 year: 2001 ident: bib38 article-title: Acquisition of tolerance against oxidative damage in Saccharomyces cerevisiae publication-title: BMC Microbiol. – volume: 223 start-page: 55 year: 2003 end-page: 78 ident: bib56 article-title: Biochemical and genomic regulation of the trehalose cycle in yeast: Review of observations and canonical model analysis publication-title: J. Theor. Biol. – volume: 34 start-page: 953 year: 2010 end-page: 959 ident: bib20 article-title: Production of bioethanol and associated by-products from potato starch residue stream by Saccharomyces cerevisiae publication-title: Biomass Bioenergy – volume: 265 start-page: 13871 year: 1990 end-page: 13877 ident: bib37 article-title: Purification and characterization of glycogen synthase from a glycogen-deficient strain of Saccharomyces cerevisiae publication-title: J. Biol. Chem. – volume: 21 start-page: 1982 year: 2010 end-page: 1990 ident: bib44 article-title: Trehalose is a key determinant of the quiescent metabolic state that fuels cell cycle progression upon return to growth publication-title: Mol. Biol. Cell. – volume: 13 start-page: 294 year: 2011 end-page: 306 ident: bib4 article-title: An in vivo data-driven framework for classification and quantification of enzyme kinetics and determination of apparent thermodynamic data publication-title: Metab. Eng. – volume: 5 start-page: 503 year: 2005 end-page: 511 ident: bib35 article-title: Acid trehalase in yeasts and filamentous fungi: localization, regulation and physiological function publication-title: FEMS Yeast Res. – volume: 279 start-page: 9125 year: 2004 end-page: 9138 ident: bib11 article-title: Role of Transcriptional Regulation in Controlling Fluxes in Central Carbon Metabolism of Saccharomyces cerevisiae: a chemostat culture study publication-title: J. Biol. Chem. – volume: 41 start-page: 633 year: 1993 end-page: 646 ident: bib46 article-title: Metabolic flux distributions in corynebacteríum glut icum during growth and lysine overproduction publication-title: Biotechnol. Bioeng. – volume: 37 start-page: 636 year: 2005 end-page: 640 ident: bib15 article-title: Large-scale in vivo flux analysis shows rigidity and suboptimal performance of Bacillus subtilis metabolism publication-title: Nat. Genet. – start-page: 7 year: 2013 ident: bib21 article-title: Glucose-methanol co-utilization in Pichia pastoris studied by metabolomics and instationary publication-title: BMC Syst. Biol. – volume: 280 start-page: 39890 year: 2005 end-page: 39896 ident: bib29 article-title: Sources of NADPH in yeast vary with carbon source publication-title: J. Biol. Chem. – volume: 48 start-page: 681 year: 1995 end-page: 698 ident: bib48 article-title: A metabolic network stoichiometry analysis of microbial growth and product formation publication-title: Biotechnol. Bioeng. – volume: 143 start-page: 1891 year: 1997 end-page: 1900 ident: bib36 article-title: Effects of various types of stress on the metabolism of reserve carbohydrates in Saccharomyces cerevisiae: Genetic evidence for a stress-induced recycling of glycogen and trehalose publication-title: Microbiology – volume: 43 start-page: 1088 year: 1995 end-page: 1095 ident: bib40 article-title: Trehalose phosphorylase from Pichia fermentans and its role in the metabolism of trehalose publication-title: Appl. Microbiol. Biotechnol. – volume: 29 start-page: 95 year: 2012 end-page: 110 ident: bib2 article-title: Identification of informative metabolic responses using a minibioreactor: a small step change in the glucose supply rate creates a large metabolic response in Saccharomyces cerevisiae publication-title: Yeast – volume: 233 start-page: 520 year: 1995 end-page: 530 ident: bib12 article-title: Genetic and biochemical characterization of the UGP1 gene encoding the UDP-glucose pyrophosphorylase from saccharomyces cerevisiae publication-title: Eur. J. Biochem. – volume: 10 start-page: 178 year: 2008 end-page: 186 ident: bib67 article-title: Isotopic non-stationary 13C gluconate tracer method for accurate determination of the pentose phosphate pathway split-ratio in Penicillium chrysogenum publication-title: Metab. Eng. – volume: 5 start-page: 419 year: 2005 end-page: 430 ident: bib25 article-title: Changes in the metabolome of Saccharomyces cerevisiae associated with evolution in aerobic glucose-limited chemostats publication-title: FEMS Yeast Res. – volume: 85 start-page: 620 year: 2004 end-page: 628 ident: bib28 article-title: MIRACLE: mass isotopomer ratio analysis of U-13C-Labeled Extracts. A new method for accurate quantification of changes in concentrations of intracellular metabolites publication-title: Biotechnol. Bioeng. – year: 2010 ident: bib55 article-title: Data reconciliation and error detection publication-title: The Metabolic Pathway Engineering Handbook – volume: 46 start-page: 128 year: 2011 end-page: 134 ident: bib39 article-title: Catalytic reversibility of Pyrococcus horikoshii trehalose synthase: efficient synthesis of several nucleoside diphosphate glucoses with enzyme recycling publication-title: Process Biochem. – volume: 85 start-page: 259 year: 2004 end-page: 268 ident: bib58 article-title: New tools for mass isotopomer data evaluation in publication-title: Biotechnol. Bioeng. – volume: 33 start-page: 9661 year: 1994 end-page: 9667 ident: bib24 article-title: Isolation, characterization, and disruption of the yeast gene encoding cytosolic NADP-specific isocitrate dehydrogenase publication-title: Biochemistry – volume: 25 start-page: 125 year: 2001 end-page: 145 ident: bib16 article-title: Reserve carbohydrates metabolism in the yeast Saccharomyces cerevisiae publication-title: FEMS Microbiol. Rev. – volume: 129 start-page: 953 year: 1983 end-page: 964 ident: bib3 article-title: A theoretical analysis of NADPH production and consumption in yeasts publication-title: J. Gen. Microbiol. – volume: 58 start-page: 254 year: 1998 end-page: 257 ident: bib41 article-title: C tracer experiments and metabolite balancing for metabolic flux analysis: comparing two approaches publication-title: Biotechnol. Bioeng. – volume: 3 start-page: 119 year: 2007 ident: bib42 article-title: Systematic evaluation of objective functions for predicting intracellular fluxes in Escherichia coli publication-title: Mol. Syst. Biol. – volume: 3 start-page: 261 year: 2003 end-page: 268 ident: bib34 article-title: Trehalose and glycogen accumulation is related to the duration of the G1 phase of Saccharomyces cerevisiae publication-title: FEMS Yeast Res. – volume: 8 start-page: 554 year: 2006 end-page: 577 ident: bib33 article-title: Computational tools for isotopically instationary publication-title: Metabolic Eng. – volume: 12 start-page: 434 year: 1996 end-page: 448 ident: bib53 article-title: Validation of a metabolic network for Saccharomyces cerevisiae using mixed substrate studies publication-title: Biotechnol. Prog. – volume: 9 start-page: 152 year: 2008 ident: bib57 article-title: C labeling experiments at metabolic nonstationary conditions: an exploratory study publication-title: BMC Bioinformatics – volume: 7 start-page: 48 year: 2007 end-page: 66 ident: bib26 article-title: Metabolome dynamic responses of Saccharomyces cerevisiae to simultaneous rapid perturbations in external electron acceptor and electron donor publication-title: FEMS Yeast Res. – volume: 4 start-page: 773 year: 2004 end-page: 787 ident: bib18 article-title: Role of reserve carbohydrates in the growth dynamics of Saccharomyces cerevisiae publication-title: FEMS Yeast Res. – volume: 336 start-page: 164 year: 2005 end-page: 171 ident: bib65 article-title: Quantitative analysis of the microbial metabolome by isotope dilution mass spectrometry using uniformly publication-title: Anal. Biochem. – volume: 66 start-page: 131 year: 2004 end-page: 142 ident: bib63 article-title: Industrial bioconversion of renewable resources as an alternative to conventional chemistry publication-title: Appl. Microbiol. Biotechnol. – volume: 15 start-page: 206 year: 2013 end-page: 217 ident: bib30 article-title: Isotopically nonstationary publication-title: Metab. Eng. – volume: 80 start-page: 731 year: 2002 end-page: 745 ident: bib51 article-title: Cumulative bondomers: a new concept in flux analysis from 2D [13C, 1H] COSY NMR data publication-title: Biotechnol. Bioeng. – volume: 74 start-page: 605 year: 2008 end-page: 614 ident: bib22 article-title: New insights into trehalose metabolism by Saccharomyces cerevisiae: NTH2 encodes a functional cytosolic trehalase, and deletion of TPS1 reveals Ath1p-dependent trehalose mobilization publication-title: Appl. Environ. Microbiol. – volume: 24 start-page: 979 year: 2013 end-page: 986 ident: bib62 article-title: Isotopically non-stationary metabolic flux analysis: complex yet highly informative publication-title: Curr. Opin. Biotechnol. |
| SSID | ssj0001361411 |
| Score | 1.98765 |
| Snippet | 13C labeling experiments in aerobic glucose limited cultures of Saccharomyces cerevisiae at four different growth rates (0.054; 0.101, 0.207, 0.307h−1) are... ¹³C labeling experiments in aerobic glucose limited cultures of Saccharomyces cerevisiae at four different growth rates (0.054; 0.101, 0.207, 0.307h⁻¹) are... 13C labeling experiments in aerobic glucose limited cultures of Saccharomyces cerevisiae at four different growth rates (0.054; 0.101, 0.207, 0.307 h-1) are... 13 C labeling experiments in aerobic glucose limited cultures of Saccharomyces cerevisiae at four different growth rates (0.054; 0.101, 0.207, 0.307 h −1 ) are... 13C labeling experiments in aerobic glucose limited cultures of Saccharomyces cerevisiae at four different growth rates (0.054; 0.101, 0.207, 0.307 h−1) are... |
| SourceID | doaj pubmedcentral proquest elsevier |
| SourceType | Open Website Open Access Repository Aggregation Database Publisher |
| StartPage | 52 |
| SubjectTerms | Amino acids exports extracellular space Flux estimation glucose Glycogen metabolic flux analysis metabolism Non-stationary 13C labeling Saccharomyces cerevisiae Trehalose |
| Title | Interaction of storage carbohydrates and other cyclic fluxes with central metabolism: A quantitative approach by non-stationary 13C metabolic flux analysis |
| URI | https://dx.doi.org/10.1016/j.meteno.2016.01.001 https://www.proquest.com/docview/2000377975 https://www.proquest.com/docview/2007420964 https://pubmed.ncbi.nlm.nih.gov/PMC5779734 https://doaj.org/article/19f0088c9bc6485c86b1de6d77d6a957 |
| Volume | 3 |
| hasFullText | 1 |
| inHoldings | 1 |
| isFullTextHit | |
| isPrint | |
| link | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV1Lb9QwELaqcikHBBTE8qiM1GuEndiJw22pqCoqOKBW7c3yU120zcJuV2J_C3-WGTtByaVcenXi99j-xp75hpDjRnovleFFZOiSE2BJ2YrZog1BgNbMDFfonPz1W312Kb5cy-tRqC-0Ccv0wHngPvA2wjGlXGtdLZR0qrbch9o3ja9NK5MfOWvZSJlKtysVHDsp-G5ZclEg7h_85pJx1y0iUvT943Vi7cSYMImzf3ImjTDn1GJydASdPiVPeuxI57nNz8he6J6TxyNGwUPyJ93wZWcFuooUbR9hx6DOrO3qZueRGGJDTedp8ryibueWC0fjcvsb0vFSlvaVU2g8CMhysbn9SOf019Z0yR8Ndkc6EJFTu6Pdqis2-T3frHeUVyf_cuZyobbMe_KCXJ5-vjg5K_r4C4UvYZnC9myFtKCfSMessEoZZRvlYRCsCgY2SWuiq00olZG-Ko2VXMXSuhZ1JqNM9ZLsQyPCK0K9CJA7eBEBE4gIapYH7BFlrMrKN8zPyCccff0zU2xoJL1OCSAKuhcF_T9RmJFmmDvd44eMC6CohR7M2X7oPPkaJ18zjlZ9M_J-mGoNywvfTEwXVtsNRulkyMnYyHv_aQQIYS2gBRM5mfRn-qVb3CQyb4mFV-L1QwzAG3KAncrWNm_J_t16G94BZrqzR-TR_Pz71flRWiZ_AdW0Gx4 |
| 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=Interaction+of+storage+carbohydrates+and+other+cyclic+fluxes+with+central+metabolism%3A+A+quantitative+approach+by+non-stationary+13C+metabolic+flux+analysis&rft.jtitle=Metabolic+engineering+communications&rft.au=Suarez-Mendez%2C+C.A.&rft.au=Hanemaaijer%2C+M.&rft.au=ten+Pierick%2C+Angela&rft.au=Wolters%2C+J.C.&rft.date=2016-12-01&rft.pub=Elsevier&rft.eissn=2214-0301&rft.volume=3&rft.spage=52&rft.epage=63&rft_id=info:doi/10.1016%2Fj.meteno.2016.01.001&rft_id=info%3Apmid%2F29468113&rft.externalDocID=PMC5779734 |
| thumbnail_l | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=2214-0301&client=summon |
| thumbnail_m | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=2214-0301&client=summon |
| thumbnail_s | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=2214-0301&client=summon |