Efficiency of organelle capture by microtubules as a function of centrosome nucleation capacity: general theory and the special case of polyspermia
Transport of organelles along microtubules is essential for the cell metabolism and morphogenesis. The presented analysis derives the probability that an organelle of a given size comes in contact with the microtubule aster. The question is asked how this measure of functionality of the microtubule...
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| description | Transport of organelles along microtubules is essential for the cell metabolism and morphogenesis. The presented analysis derives the probability that an organelle of a given size comes in contact with the microtubule aster. The question is asked how this measure of functionality of the microtubule aster is controlled by the centrosome. A quantitative model is developed to address this question. It is shown that for the given set of cellular parameters, such as size and total tubulin content, a centrosome nucleation capacity exists that maximizes the probability of the organelle capture. The developed general model is then applied to the capture of the female pronucleus by microtubules assembled on the sperm centrosome, following physiologically polyspermic fertilization. This application highlights an unintuitive reflection of nonlinearity of the nucleated polymerization of the cellular pool of tubulin. The prediction that the sperm centrosome should lower its nucleation capacity in the face of the competition from the other sperm is a stark illustration of the new optimality principle. Overall, the model calls attention to the capabilities of the centrosomal pathway of regulation of the transport-related functionality of the microtubule cytoskeleton. It establishes a quantitative and conceptual framework that can guide experiment design and interpretation. |
| doi_str_mv | 10.1371/journal.pone.0037675 |
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The presented analysis derives the probability that an organelle of a given size comes in contact with the microtubule aster. The question is asked how this measure of functionality of the microtubule aster is controlled by the centrosome. A quantitative model is developed to address this question. It is shown that for the given set of cellular parameters, such as size and total tubulin content, a centrosome nucleation capacity exists that maximizes the probability of the organelle capture. The developed general model is then applied to the capture of the female pronucleus by microtubules assembled on the sperm centrosome, following physiologically polyspermic fertilization. This application highlights an unintuitive reflection of nonlinearity of the nucleated polymerization of the cellular pool of tubulin. The prediction that the sperm centrosome should lower its nucleation capacity in the face of the competition from the other sperm is a stark illustration of the new optimality principle. Overall, the model calls attention to the capabilities of the centrosomal pathway of regulation of the transport-related functionality of the microtubule cytoskeleton. It establishes a quantitative and conceptual framework that can guide experiment design and interpretation.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0037675</identifier><identifier>PMID: 22662187</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Algorithms ; Analysis ; Beroe ovata ; Biology ; Cell cycle ; Centrosome - metabolism ; Computer Science ; Cytoskeleton ; Design of experiments ; Eggs ; Female ; Fertilization ; Fertilization - physiology ; Humans ; Male ; Metabolism ; Microscopy ; Microsurgery ; Microtubules ; Microtubules - metabolism ; Models, Biological ; Morphogenesis ; Nonlinear systems ; Nucleation ; Organelles ; Organelles - metabolism ; Physics ; Physiological aspects ; Polymerization ; Pronucleus ; Proteins ; Sperm ; Spermatozoa - metabolism ; Stochastic models ; Transport ; Tubulin ; Xenopus ; Zygote - metabolism</subject><ispartof>PloS one, 2012-05, Vol.7 (5), p.e37675-e37675</ispartof><rights>COPYRIGHT 2012 Public Library of Science</rights><rights>2012 Ivan V. Maly. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Ivan V. Maly. 2012</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c641t-fedfe0311ea74aa6ee6438353f4eb0658af56b191ce5d25e778a305939e629103</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3360769/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3360769/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2100,2926,23864,27922,27923,53789,53791,79370,79371</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22662187$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Yang, Yanmin</contributor><creatorcontrib>Maly, Ivan V</creatorcontrib><title>Efficiency of organelle capture by microtubules as a function of centrosome nucleation capacity: general theory and the special case of polyspermia</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Transport of organelles along microtubules is essential for the cell metabolism and morphogenesis. The presented analysis derives the probability that an organelle of a given size comes in contact with the microtubule aster. The question is asked how this measure of functionality of the microtubule aster is controlled by the centrosome. A quantitative model is developed to address this question. It is shown that for the given set of cellular parameters, such as size and total tubulin content, a centrosome nucleation capacity exists that maximizes the probability of the organelle capture. The developed general model is then applied to the capture of the female pronucleus by microtubules assembled on the sperm centrosome, following physiologically polyspermic fertilization. This application highlights an unintuitive reflection of nonlinearity of the nucleated polymerization of the cellular pool of tubulin. 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It establishes a quantitative and conceptual framework that can guide experiment design and interpretation.</description><subject>Algorithms</subject><subject>Analysis</subject><subject>Beroe ovata</subject><subject>Biology</subject><subject>Cell cycle</subject><subject>Centrosome - metabolism</subject><subject>Computer Science</subject><subject>Cytoskeleton</subject><subject>Design of experiments</subject><subject>Eggs</subject><subject>Female</subject><subject>Fertilization</subject><subject>Fertilization - physiology</subject><subject>Humans</subject><subject>Male</subject><subject>Metabolism</subject><subject>Microscopy</subject><subject>Microsurgery</subject><subject>Microtubules</subject><subject>Microtubules - metabolism</subject><subject>Models, Biological</subject><subject>Morphogenesis</subject><subject>Nonlinear systems</subject><subject>Nucleation</subject><subject>Organelles</subject><subject>Organelles - metabolism</subject><subject>Physics</subject><subject>Physiological aspects</subject><subject>Polymerization</subject><subject>Pronucleus</subject><subject>Proteins</subject><subject>Sperm</subject><subject>Spermatozoa - metabolism</subject><subject>Stochastic models</subject><subject>Transport</subject><subject>Tubulin</subject><subject>Xenopus</subject><subject>Zygote - metabolism</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk9-K1DAUxoso7rr6BqIFQfRixqRp0tYLYVlWHVhY8N9tOE1PZrK0TU1asc_hC5vOdJep7IW00HDy-770nJwTRc8pWVOW0Xc3dnAt1OvOtrgmhGUi4w-iU1qwZCUSwh4erU-iJ97fEMJZLsTj6CRJhEhonp1Gfy61Nspgq8bY6ti6LbRY1xgr6PrBYVyOcWOUs_1QDjX6GMIb66FVvbHtJFHY9s5622DcDqpG2G8EOSjTj-_jLbbooI77HVo3xtBW0zL2HSoTwgo8TjadrccQc42Bp9EjDbXHZ_P3LPr-8fLbxefV1fWnzcX51UqJlPYrjZVGwihFyFIAgShSljPOdIolETwHzUVJC6qQVwnHLMuBEV6wAkVSUMLOopcH3662Xs719JKyhBOSB6tAbA5EZeFGds404EZpwch9IFRLgutNyFryLKW6oGmh8jSt8rJgHFSJCdVKqZLr4PVhPm0oG6z2ZYN6Ybrcac1Obu0vyZggmSiCwZvZwNmfA_peNsarcFnhxuwQ_pvQXDBKiiSgr_5B789uprYQEjCttuFcNZnK8zTLSEoFE4Fa30OFp8LQGKH5tAnxheDtQhCYHn_3Wxi8l5uvX_6fvf6xZF8fsTuEut95Ww9Tv_klmB7A0LbeO9R3RaZETrNzWw05zY6cZyfIXhxf0J3odljYX7yGFrE</recordid><startdate>20120525</startdate><enddate>20120525</enddate><creator>Maly, Ivan V</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20120525</creationdate><title>Efficiency of organelle capture by microtubules as a function of centrosome nucleation capacity: general theory and the special case of polyspermia</title><author>Maly, Ivan V</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c641t-fedfe0311ea74aa6ee6438353f4eb0658af56b191ce5d25e778a305939e629103</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Algorithms</topic><topic>Analysis</topic><topic>Beroe ovata</topic><topic>Biology</topic><topic>Cell cycle</topic><topic>Centrosome - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Maly, Ivan V</au><au>Yang, Yanmin</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Efficiency of organelle capture by microtubules as a function of centrosome nucleation capacity: general theory and the special case of polyspermia</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2012-05-25</date><risdate>2012</risdate><volume>7</volume><issue>5</issue><spage>e37675</spage><epage>e37675</epage><pages>e37675-e37675</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Transport of organelles along microtubules is essential for the cell metabolism and morphogenesis. The presented analysis derives the probability that an organelle of a given size comes in contact with the microtubule aster. The question is asked how this measure of functionality of the microtubule aster is controlled by the centrosome. A quantitative model is developed to address this question. It is shown that for the given set of cellular parameters, such as size and total tubulin content, a centrosome nucleation capacity exists that maximizes the probability of the organelle capture. The developed general model is then applied to the capture of the female pronucleus by microtubules assembled on the sperm centrosome, following physiologically polyspermic fertilization. This application highlights an unintuitive reflection of nonlinearity of the nucleated polymerization of the cellular pool of tubulin. The prediction that the sperm centrosome should lower its nucleation capacity in the face of the competition from the other sperm is a stark illustration of the new optimality principle. Overall, the model calls attention to the capabilities of the centrosomal pathway of regulation of the transport-related functionality of the microtubule cytoskeleton. It establishes a quantitative and conceptual framework that can guide experiment design and interpretation.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>22662187</pmid><doi>10.1371/journal.pone.0037675</doi><tpages>e37675</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Algorithms Analysis Beroe ovata Biology Cell cycle Centrosome - metabolism Computer Science Cytoskeleton Design of experiments Eggs Female Fertilization Fertilization - physiology Humans Male Metabolism Microscopy Microsurgery Microtubules Microtubules - metabolism Models, Biological Morphogenesis Nonlinear systems Nucleation Organelles Organelles - metabolism Physics Physiological aspects Polymerization Pronucleus Proteins Sperm Spermatozoa - metabolism Stochastic models Transport Tubulin Xenopus Zygote - metabolism |
| title | Efficiency of organelle capture by microtubules as a function of centrosome nucleation capacity: general theory and the special case of polyspermia |
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