Synchronous protein cycling in batch cultures of the yeast Saccharomyces cerevisiae at log growth phase
The assumption that cells are temporally organized systems, i.e. showing relevant dynamics of their state variables such as gene expression or protein and metabolite concentration, while tacitly given for granted at the molecular level, is not explicitly taken into account when interpreting biologic...
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creator | Romagnoli, Gabriele Cundari, Enrico Negri, Rodolfo Crescenzi, Marco Farina, Lorenzo Giuliani, Alessandro Bianchi, Michele M. |
description | The assumption that cells are temporally organized systems,
i.e. showing relevant dynamics of their state variables such as gene expression or protein and metabolite concentration, while tacitly given for granted at the molecular level, is not explicitly taken into account when interpreting biological experimental data. This conundrum stems from the (undemonstrated) assumption that a cell culture, the actual object of biological experimentation, is a population of billions of independent oscillators (cells) randomly experiencing different phases of their cycles and thus not producing relevant coordinated dynamics at the population level. Moreover the fact of considering reproductive cycle as by far the most important cyclic process in a cell resulted in lower attention given to other rhythmic processes. Here we demonstrate that growing yeast cells show a very repeatable and robust cyclic variation of the concentration of proteins with different cellular functions. We also report experimental evidence that the mechanism governing this basic oscillator and the cellular entrainment is resistant to external chemical constraints. Finally, cell growth is accompanied by cyclic dynamics of medium pH. These cycles are observed in batch cultures, different from the usual continuous cultures in which yeast metabolic cycles are known to occur, and suggest the existence of basic, spontaneous, collective and synchronous behaviors of the cell population as a whole. |
doi_str_mv | 10.1016/j.yexcr.2011.09.007 |
format | Article |
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i.e. showing relevant dynamics of their state variables such as gene expression or protein and metabolite concentration, while tacitly given for granted at the molecular level, is not explicitly taken into account when interpreting biological experimental data. This conundrum stems from the (undemonstrated) assumption that a cell culture, the actual object of biological experimentation, is a population of billions of independent oscillators (cells) randomly experiencing different phases of their cycles and thus not producing relevant coordinated dynamics at the population level. Moreover the fact of considering reproductive cycle as by far the most important cyclic process in a cell resulted in lower attention given to other rhythmic processes. Here we demonstrate that growing yeast cells show a very repeatable and robust cyclic variation of the concentration of proteins with different cellular functions. We also report experimental evidence that the mechanism governing this basic oscillator and the cellular entrainment is resistant to external chemical constraints. Finally, cell growth is accompanied by cyclic dynamics of medium pH. These cycles are observed in batch cultures, different from the usual continuous cultures in which yeast metabolic cycles are known to occur, and suggest the existence of basic, spontaneous, collective and synchronous behaviors of the cell population as a whole.</description><identifier>ISSN: 0014-4827</identifier><identifier>EISSN: 1090-2422</identifier><identifier>DOI: 10.1016/j.yexcr.2011.09.007</identifier><identifier>PMID: 21978910</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Bacteria ; Batch Cell Culture Techniques ; Batch Cell Culture Techniques - methods ; Batch culture ; Batch processing ; Biochemistry, Molecular Biology ; Cell communication ; Cell culture ; Cell Cycle ; Cell Cycle - genetics ; Cell Proliferation ; Cells ; Continuous culture ; Cycloheximide ; Cycloheximide - pharmacology ; Data processing ; DNA Helicases ; DNA Helicases - metabolism ; Entrainment ; Expression ; Gene expression ; Hydrogen-Ion Concentration ; Life Sciences ; Metabolites ; Oscillators ; pH effects ; Population ; Population levels ; Proteins ; Reproductive status ; Rhythmic process ; Rhythms ; Ribosomal Proteins ; Ribosomal Proteins - genetics ; Ribosomal Proteins - metabolism ; Saccharomyces cerevisiae ; Saccharomyces cerevisiae - genetics ; Saccharomyces cerevisiae - growth & development ; Saccharomyces cerevisiae - metabolism ; Saccharomyces cerevisiae Proteins ; Saccharomyces cerevisiae Proteins - genetics ; Saccharomyces cerevisiae Proteins - metabolism ; Vanadates ; Vanadates - metabolism ; Yeast</subject><ispartof>Experimental cell research, 2011-12, Vol.317 (20), p.2958-2968</ispartof><rights>2011 Elsevier Inc.</rights><rights>Copyright © 2011 Elsevier Inc. All rights reserved.</rights><rights>Copyright © 2011 Elsevier B.V. All rights reserved.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c522t-e63d8cac7589662f23451252bca047372859efb29c91cee9af097899a7dda1793</citedby><cites>FETCH-LOGICAL-c522t-e63d8cac7589662f23451252bca047372859efb29c91cee9af097899a7dda1793</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0014482711003661$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>230,314,776,780,881,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21978910$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://riip.hal.science/pasteur-00978685$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Romagnoli, Gabriele</creatorcontrib><creatorcontrib>Cundari, Enrico</creatorcontrib><creatorcontrib>Negri, Rodolfo</creatorcontrib><creatorcontrib>Crescenzi, Marco</creatorcontrib><creatorcontrib>Farina, Lorenzo</creatorcontrib><creatorcontrib>Giuliani, Alessandro</creatorcontrib><creatorcontrib>Bianchi, Michele M.</creatorcontrib><title>Synchronous protein cycling in batch cultures of the yeast Saccharomyces cerevisiae at log growth phase</title><title>Experimental cell research</title><addtitle>Exp Cell Res</addtitle><description>The assumption that cells are temporally organized systems,
i.e. showing relevant dynamics of their state variables such as gene expression or protein and metabolite concentration, while tacitly given for granted at the molecular level, is not explicitly taken into account when interpreting biological experimental data. This conundrum stems from the (undemonstrated) assumption that a cell culture, the actual object of biological experimentation, is a population of billions of independent oscillators (cells) randomly experiencing different phases of their cycles and thus not producing relevant coordinated dynamics at the population level. Moreover the fact of considering reproductive cycle as by far the most important cyclic process in a cell resulted in lower attention given to other rhythmic processes. Here we demonstrate that growing yeast cells show a very repeatable and robust cyclic variation of the concentration of proteins with different cellular functions. We also report experimental evidence that the mechanism governing this basic oscillator and the cellular entrainment is resistant to external chemical constraints. Finally, cell growth is accompanied by cyclic dynamics of medium pH. These cycles are observed in batch cultures, different from the usual continuous cultures in which yeast metabolic cycles are known to occur, and suggest the existence of basic, spontaneous, collective and synchronous behaviors of the cell population as a whole.</description><subject>Bacteria</subject><subject>Batch Cell Culture Techniques</subject><subject>Batch Cell Culture Techniques - methods</subject><subject>Batch culture</subject><subject>Batch processing</subject><subject>Biochemistry, Molecular Biology</subject><subject>Cell communication</subject><subject>Cell culture</subject><subject>Cell Cycle</subject><subject>Cell Cycle - genetics</subject><subject>Cell Proliferation</subject><subject>Cells</subject><subject>Continuous culture</subject><subject>Cycloheximide</subject><subject>Cycloheximide - pharmacology</subject><subject>Data processing</subject><subject>DNA Helicases</subject><subject>DNA Helicases - metabolism</subject><subject>Entrainment</subject><subject>Expression</subject><subject>Gene expression</subject><subject>Hydrogen-Ion Concentration</subject><subject>Life Sciences</subject><subject>Metabolites</subject><subject>Oscillators</subject><subject>pH effects</subject><subject>Population</subject><subject>Population levels</subject><subject>Proteins</subject><subject>Reproductive status</subject><subject>Rhythmic process</subject><subject>Rhythms</subject><subject>Ribosomal Proteins</subject><subject>Ribosomal Proteins - genetics</subject><subject>Ribosomal Proteins - metabolism</subject><subject>Saccharomyces cerevisiae</subject><subject>Saccharomyces cerevisiae - genetics</subject><subject>Saccharomyces cerevisiae - growth & development</subject><subject>Saccharomyces cerevisiae - metabolism</subject><subject>Saccharomyces cerevisiae Proteins</subject><subject>Saccharomyces cerevisiae Proteins - genetics</subject><subject>Saccharomyces cerevisiae Proteins - metabolism</subject><subject>Vanadates</subject><subject>Vanadates - metabolism</subject><subject>Yeast</subject><issn>0014-4827</issn><issn>1090-2422</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kU9v1DAQxSMEokvhEyAhiwtcEsbOH9sHDlUFFGklDoWz5Z1MNl5l48VOtuTb4-2WHjj0ZEv-ved587LsLYeCA28-7YqF_mAoBHBegC4A5LNsxUFDLiohnmcrAF7llRLyInsV4w4AlOLNy-xCcC2V5rDKtrfLiH3wo58jOwQ_kRsZLji4ccvSdWMn7BnOwzQHisx3bOqJLWTjxG4tYm-D3y-YnpACHV10lpid2OC3bBv83dSzQ28jvc5edHaI9ObhvMx-ff3y8_omX__49v36ap1jLcSUU1O2Ci3KWummEZ0oq5qLWmzQQiVLKVStqdsIjZojkbYdnJJoK9vWcqnLyyw_-_Z2MIfg9jYsxltnbq7W5pCmpjkYOIkaVR954j-c-ZT990xxMnsXkYbBjpRWYjRUwMtaNYn8-CTJQSiQSqk6oe__Q3d-DmPKfe8nUj1VgsozhMHHGKh7HJeDORVsdua-YHMq2IBOY8ukevdgPW_21D5q_jWagM9ngNKWj46CiehoRGpdIJxM692TH_wFDXy3jA</recordid><startdate>20111210</startdate><enddate>20111210</enddate><creator>Romagnoli, Gabriele</creator><creator>Cundari, Enrico</creator><creator>Negri, Rodolfo</creator><creator>Crescenzi, Marco</creator><creator>Farina, Lorenzo</creator><creator>Giuliani, Alessandro</creator><creator>Bianchi, Michele M.</creator><general>Elsevier Inc</general><general>Elsevier BV</general><general>Elsevier</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7TK</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>M7N</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope></search><sort><creationdate>20111210</creationdate><title>Synchronous protein cycling in batch cultures of the yeast Saccharomyces cerevisiae at log growth phase</title><author>Romagnoli, Gabriele ; 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i.e. showing relevant dynamics of their state variables such as gene expression or protein and metabolite concentration, while tacitly given for granted at the molecular level, is not explicitly taken into account when interpreting biological experimental data. This conundrum stems from the (undemonstrated) assumption that a cell culture, the actual object of biological experimentation, is a population of billions of independent oscillators (cells) randomly experiencing different phases of their cycles and thus not producing relevant coordinated dynamics at the population level. Moreover the fact of considering reproductive cycle as by far the most important cyclic process in a cell resulted in lower attention given to other rhythmic processes. Here we demonstrate that growing yeast cells show a very repeatable and robust cyclic variation of the concentration of proteins with different cellular functions. We also report experimental evidence that the mechanism governing this basic oscillator and the cellular entrainment is resistant to external chemical constraints. Finally, cell growth is accompanied by cyclic dynamics of medium pH. These cycles are observed in batch cultures, different from the usual continuous cultures in which yeast metabolic cycles are known to occur, and suggest the existence of basic, spontaneous, collective and synchronous behaviors of the cell population as a whole.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>21978910</pmid><doi>10.1016/j.yexcr.2011.09.007</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Bacteria Batch Cell Culture Techniques Batch Cell Culture Techniques - methods Batch culture Batch processing Biochemistry, Molecular Biology Cell communication Cell culture Cell Cycle Cell Cycle - genetics Cell Proliferation Cells Continuous culture Cycloheximide Cycloheximide - pharmacology Data processing DNA Helicases DNA Helicases - metabolism Entrainment Expression Gene expression Hydrogen-Ion Concentration Life Sciences Metabolites Oscillators pH effects Population Population levels Proteins Reproductive status Rhythmic process Rhythms Ribosomal Proteins Ribosomal Proteins - genetics Ribosomal Proteins - metabolism Saccharomyces cerevisiae Saccharomyces cerevisiae - genetics Saccharomyces cerevisiae - growth & development Saccharomyces cerevisiae - metabolism Saccharomyces cerevisiae Proteins Saccharomyces cerevisiae Proteins - genetics Saccharomyces cerevisiae Proteins - metabolism Vanadates Vanadates - metabolism Yeast |
title | Synchronous protein cycling in batch cultures of the yeast Saccharomyces cerevisiae at log growth phase |
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