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A phosphatidylinositol transfer protein integrates phosphoinositide signaling with lipid droplet metabolism to regulate a developmental program of nutrient stress–induced membrane biogenesis

Lipid droplet (LD) utilization is an important cellular activity that regulates energy balance and release of lipid second messengers. Because fatty acids exhibit both beneficial and toxic properties, their release from LDs must be controlled. Here we demonstrate that yeast Sfh3, an unusual Sec14-li...

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Autores principales: Ren, Jihui, Pei-Chen Lin, Coney, Pathak, Manish C., Temple, Brenda R. S., Nile, Aaron H., Mousley, Carl J., Duncan, Mara C., Eckert, Debra M., Leiker, Thomas J., Ivanova, Pavlina T., Myers, David S., Murphy, Robert C., Brown, H. Alex, Verdaasdonk, Jolien, Bloom, Kerry S., Ortlund, Eric A., Neiman, Aaron M., Bankaitis, Vytas A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3937096/
https://www.ncbi.nlm.nih.gov/pubmed/24403601
http://dx.doi.org/10.1091/mbc.E13-11-0634
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author Ren, Jihui
Pei-Chen Lin, Coney
Pathak, Manish C.
Temple, Brenda R. S.
Nile, Aaron H.
Mousley, Carl J.
Duncan, Mara C.
Eckert, Debra M.
Leiker, Thomas J.
Ivanova, Pavlina T.
Myers, David S.
Murphy, Robert C.
Brown, H. Alex
Verdaasdonk, Jolien
Bloom, Kerry S.
Ortlund, Eric A.
Neiman, Aaron M.
Bankaitis, Vytas A.
author_facet Ren, Jihui
Pei-Chen Lin, Coney
Pathak, Manish C.
Temple, Brenda R. S.
Nile, Aaron H.
Mousley, Carl J.
Duncan, Mara C.
Eckert, Debra M.
Leiker, Thomas J.
Ivanova, Pavlina T.
Myers, David S.
Murphy, Robert C.
Brown, H. Alex
Verdaasdonk, Jolien
Bloom, Kerry S.
Ortlund, Eric A.
Neiman, Aaron M.
Bankaitis, Vytas A.
author_sort Ren, Jihui
collection PubMed
description Lipid droplet (LD) utilization is an important cellular activity that regulates energy balance and release of lipid second messengers. Because fatty acids exhibit both beneficial and toxic properties, their release from LDs must be controlled. Here we demonstrate that yeast Sfh3, an unusual Sec14-like phosphatidylinositol transfer protein, is an LD-associated protein that inhibits lipid mobilization from these particles. We further document a complex biochemical diversification of LDs during sporulation in which Sfh3 and select other LD proteins redistribute into discrete LD subpopulations. The data show that Sfh3 modulates the efficiency with which a neutral lipid hydrolase-rich LD subclass is consumed during biogenesis of specialized membrane envelopes that package replicated haploid meiotic genomes. These results present novel insights into the interface between phosphoinositide signaling and developmental regulation of LD metabolism and unveil meiosis-specific aspects of Sfh3 (and phosphoinositide) biology that are invisible to contemporary haploid-centric cell biological, proteomic, and functional genomics approaches.
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spelling pubmed-39370962014-05-16 A phosphatidylinositol transfer protein integrates phosphoinositide signaling with lipid droplet metabolism to regulate a developmental program of nutrient stress–induced membrane biogenesis Ren, Jihui Pei-Chen Lin, Coney Pathak, Manish C. Temple, Brenda R. S. Nile, Aaron H. Mousley, Carl J. Duncan, Mara C. Eckert, Debra M. Leiker, Thomas J. Ivanova, Pavlina T. Myers, David S. Murphy, Robert C. Brown, H. Alex Verdaasdonk, Jolien Bloom, Kerry S. Ortlund, Eric A. Neiman, Aaron M. Bankaitis, Vytas A. Mol Biol Cell Articles Lipid droplet (LD) utilization is an important cellular activity that regulates energy balance and release of lipid second messengers. Because fatty acids exhibit both beneficial and toxic properties, their release from LDs must be controlled. Here we demonstrate that yeast Sfh3, an unusual Sec14-like phosphatidylinositol transfer protein, is an LD-associated protein that inhibits lipid mobilization from these particles. We further document a complex biochemical diversification of LDs during sporulation in which Sfh3 and select other LD proteins redistribute into discrete LD subpopulations. The data show that Sfh3 modulates the efficiency with which a neutral lipid hydrolase-rich LD subclass is consumed during biogenesis of specialized membrane envelopes that package replicated haploid meiotic genomes. These results present novel insights into the interface between phosphoinositide signaling and developmental regulation of LD metabolism and unveil meiosis-specific aspects of Sfh3 (and phosphoinositide) biology that are invisible to contemporary haploid-centric cell biological, proteomic, and functional genomics approaches. The American Society for Cell Biology 2014-03-01 /pmc/articles/PMC3937096/ /pubmed/24403601 http://dx.doi.org/10.1091/mbc.E13-11-0634 Text en © 2014 Ren et al. This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License (http://creativecommons.org/licenses/by-nc-sa/3.0). “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society of Cell Biology.
spellingShingle Articles
Ren, Jihui
Pei-Chen Lin, Coney
Pathak, Manish C.
Temple, Brenda R. S.
Nile, Aaron H.
Mousley, Carl J.
Duncan, Mara C.
Eckert, Debra M.
Leiker, Thomas J.
Ivanova, Pavlina T.
Myers, David S.
Murphy, Robert C.
Brown, H. Alex
Verdaasdonk, Jolien
Bloom, Kerry S.
Ortlund, Eric A.
Neiman, Aaron M.
Bankaitis, Vytas A.
A phosphatidylinositol transfer protein integrates phosphoinositide signaling with lipid droplet metabolism to regulate a developmental program of nutrient stress–induced membrane biogenesis
title A phosphatidylinositol transfer protein integrates phosphoinositide signaling with lipid droplet metabolism to regulate a developmental program of nutrient stress–induced membrane biogenesis
title_full A phosphatidylinositol transfer protein integrates phosphoinositide signaling with lipid droplet metabolism to regulate a developmental program of nutrient stress–induced membrane biogenesis
title_fullStr A phosphatidylinositol transfer protein integrates phosphoinositide signaling with lipid droplet metabolism to regulate a developmental program of nutrient stress–induced membrane biogenesis
title_full_unstemmed A phosphatidylinositol transfer protein integrates phosphoinositide signaling with lipid droplet metabolism to regulate a developmental program of nutrient stress–induced membrane biogenesis
title_short A phosphatidylinositol transfer protein integrates phosphoinositide signaling with lipid droplet metabolism to regulate a developmental program of nutrient stress–induced membrane biogenesis
title_sort phosphatidylinositol transfer protein integrates phosphoinositide signaling with lipid droplet metabolism to regulate a developmental program of nutrient stress–induced membrane biogenesis
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3937096/
https://www.ncbi.nlm.nih.gov/pubmed/24403601
http://dx.doi.org/10.1091/mbc.E13-11-0634
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