Cargando…
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...
Autores principales: | , , , , , , , , , , , , , , , , , |
---|---|
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 |
_version_ | 1782305427955908608 |
---|---|
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. |
format | Online Article Text |
id | pubmed-3937096 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2014 |
publisher | The American Society for Cell Biology |
record_format | MEDLINE/PubMed |
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 |
work_keys_str_mv | AT renjihui aphosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT peichenlinconey aphosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT pathakmanishc aphosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT templebrendars aphosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT nileaaronh aphosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT mousleycarlj aphosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT duncanmarac aphosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT eckertdebram aphosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT leikerthomasj aphosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT ivanovapavlinat aphosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT myersdavids aphosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT murphyrobertc aphosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT brownhalex aphosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT verdaasdonkjolien aphosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT bloomkerrys aphosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT ortlunderica aphosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT neimanaaronm aphosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT bankaitisvytasa aphosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT renjihui phosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT peichenlinconey phosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT pathakmanishc phosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT templebrendars phosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT nileaaronh phosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT mousleycarlj phosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT duncanmarac phosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT eckertdebram phosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT leikerthomasj phosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT ivanovapavlinat phosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT myersdavids phosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT murphyrobertc phosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT brownhalex phosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT verdaasdonkjolien phosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT bloomkerrys phosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT ortlunderica phosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT neimanaaronm phosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis AT bankaitisvytasa phosphatidylinositoltransferproteinintegratesphosphoinositidesignalingwithlipiddropletmetabolismtoregulateadevelopmentalprogramofnutrientstressinducedmembranebiogenesis |