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Dynamic balance between vesicle transport and microtubule growth enables neurite outgrowth
Whole cell responses involve multiple subcellular processes (SCPs). To understand how balance between SCPs controls the dynamics of whole cell responses we studied neurite outgrowth in rat primary cortical neurons in culture. We used a combination of dynamical models and experiments to understand th...
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Published in: | PLoS computational biology 2019-05, Vol.15 (5), p.e1006877-e1006877 |
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description | Whole cell responses involve multiple subcellular processes (SCPs). To understand how balance between SCPs controls the dynamics of whole cell responses we studied neurite outgrowth in rat primary cortical neurons in culture. We used a combination of dynamical models and experiments to understand the conditions that permitted growth at a specified velocity and when aberrant growth could lead to the formation of dystrophic bulbs. We hypothesized that dystrophic bulb formation is due to quantitative imbalances between SCPs. Simulations predict redundancies between lower level sibling SCPs within each type of high level SCP. In contrast, higher level SCPs, such as vesicle transport and exocytosis or microtubule growth characteristic of each type need to be strictly coordinated with each other and imbalances result in stalling of neurite outgrowth. From these simulations, we predicted the effect of changing the activities of SCPs involved in vesicle exocytosis or microtubule growth could lead to formation of dystrophic bulbs. siRNA ablation experiments verified these predictions. We conclude that whole cell dynamics requires balance between the higher-level SCPs involved and imbalances can terminate whole cell responses such as neurite outgrowth. |
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To understand how balance between SCPs controls the dynamics of whole cell responses we studied neurite outgrowth in rat primary cortical neurons in culture. We used a combination of dynamical models and experiments to understand the conditions that permitted growth at a specified velocity and when aberrant growth could lead to the formation of dystrophic bulbs. We hypothesized that dystrophic bulb formation is due to quantitative imbalances between SCPs. Simulations predict redundancies between lower level sibling SCPs within each type of high level SCP. In contrast, higher level SCPs, such as vesicle transport and exocytosis or microtubule growth characteristic of each type need to be strictly coordinated with each other and imbalances result in stalling of neurite outgrowth. From these simulations, we predicted the effect of changing the activities of SCPs involved in vesicle exocytosis or microtubule growth could lead to formation of dystrophic bulbs. siRNA ablation experiments verified these predictions. We conclude that whole cell dynamics requires balance between the higher-level SCPs involved and imbalances can terminate whole cell responses such as neurite outgrowth.</description><identifier>ISSN: 1553-7358</identifier><identifier>ISSN: 1553-734X</identifier><identifier>EISSN: 1553-7358</identifier><identifier>DOI: 10.1371/journal.pcbi.1006877</identifier><identifier>PMID: 31042702</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Ablation ; Animals ; Axonogenesis ; Biological Transport - physiology ; Biology ; Biology and Life Sciences ; Brain ; Bulbs ; Cell culture ; Cell Physiological Phenomena ; Cells, Cultured ; Computer simulation ; Exocytosis ; Growth models ; Mathematical models ; Medicine ; Microtubules ; Microtubules - metabolism ; Microtubules - physiology ; Models, Neurological ; Neural circuitry ; Neurites - metabolism ; Neurites - physiology ; Neuronal Outgrowth - physiology ; Neurons ; Neurons - physiology ; Neurosciences ; Ordinary differential equations ; Physiological aspects ; Predictions ; Protein Binding ; Rats ; siRNA ; Stalling ; Transport</subject><ispartof>PLoS computational biology, 2019-05, Vol.15 (5), p.e1006877-e1006877</ispartof><rights>COPYRIGHT 2019 Public Library of Science</rights><rights>2019 Yadaw et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://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>2019 Yadaw et al 2019 Yadaw et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c633t-cb4e82cced497a8da6aac2cd13cc509eb78d828857ebfcb2e95106b40bace1223</citedby><cites>FETCH-LOGICAL-c633t-cb4e82cced497a8da6aac2cd13cc509eb78d828857ebfcb2e95106b40bace1223</cites><orcidid>0000-0002-7814-0180 ; 0000-0002-1362-6534 ; 0000-0002-8597-7376 ; 0000-0002-4261-3230</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2250647342/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2250647342?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31042702$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Maini, Philip K.</contributor><creatorcontrib>Yadaw, Arjun Singh</creatorcontrib><creatorcontrib>Siddiq, Mustafa M</creatorcontrib><creatorcontrib>Rabinovich, Vera</creatorcontrib><creatorcontrib>Tolentino, Rosa</creatorcontrib><creatorcontrib>Hansen, Jens</creatorcontrib><creatorcontrib>Iyengar, Ravi</creatorcontrib><title>Dynamic balance between vesicle transport and microtubule growth enables neurite outgrowth</title><title>PLoS computational biology</title><addtitle>PLoS Comput Biol</addtitle><description>Whole cell responses involve multiple subcellular processes (SCPs). To understand how balance between SCPs controls the dynamics of whole cell responses we studied neurite outgrowth in rat primary cortical neurons in culture. We used a combination of dynamical models and experiments to understand the conditions that permitted growth at a specified velocity and when aberrant growth could lead to the formation of dystrophic bulbs. We hypothesized that dystrophic bulb formation is due to quantitative imbalances between SCPs. Simulations predict redundancies between lower level sibling SCPs within each type of high level SCP. In contrast, higher level SCPs, such as vesicle transport and exocytosis or microtubule growth characteristic of each type need to be strictly coordinated with each other and imbalances result in stalling of neurite outgrowth. From these simulations, we predicted the effect of changing the activities of SCPs involved in vesicle exocytosis or microtubule growth could lead to formation of dystrophic bulbs. siRNA ablation experiments verified these predictions. 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To understand how balance between SCPs controls the dynamics of whole cell responses we studied neurite outgrowth in rat primary cortical neurons in culture. We used a combination of dynamical models and experiments to understand the conditions that permitted growth at a specified velocity and when aberrant growth could lead to the formation of dystrophic bulbs. We hypothesized that dystrophic bulb formation is due to quantitative imbalances between SCPs. Simulations predict redundancies between lower level sibling SCPs within each type of high level SCP. In contrast, higher level SCPs, such as vesicle transport and exocytosis or microtubule growth characteristic of each type need to be strictly coordinated with each other and imbalances result in stalling of neurite outgrowth. From these simulations, we predicted the effect of changing the activities of SCPs involved in vesicle exocytosis or microtubule growth could lead to formation of dystrophic bulbs. siRNA ablation experiments verified these predictions. We conclude that whole cell dynamics requires balance between the higher-level SCPs involved and imbalances can terminate whole cell responses such as neurite outgrowth.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>31042702</pmid><doi>10.1371/journal.pcbi.1006877</doi><orcidid>https://orcid.org/0000-0002-7814-0180</orcidid><orcidid>https://orcid.org/0000-0002-1362-6534</orcidid><orcidid>https://orcid.org/0000-0002-8597-7376</orcidid><orcidid>https://orcid.org/0000-0002-4261-3230</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Ablation Animals Axonogenesis Biological Transport - physiology Biology Biology and Life Sciences Brain Bulbs Cell culture Cell Physiological Phenomena Cells, Cultured Computer simulation Exocytosis Growth models Mathematical models Medicine Microtubules Microtubules - metabolism Microtubules - physiology Models, Neurological Neural circuitry Neurites - metabolism Neurites - physiology Neuronal Outgrowth - physiology Neurons Neurons - physiology Neurosciences Ordinary differential equations Physiological aspects Predictions Protein Binding Rats siRNA Stalling Transport |
title | Dynamic balance between vesicle transport and microtubule growth enables neurite outgrowth |
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