The protein and neutral lipid composition of lipid droplets isolated from the fission yeast, Schizosaccharomyces pombe
Abstract
Lipid droplets consist of a core of neutral lipids surrounded by a phospholipid monolayer with bound proteins. Much of the information on lipid droplet function comes from proteomic and lipodomic studies that identify the components of droplets isolated from organisms throughout the phylogenetic tree. Here, we add to that important inventory by reporting lipid droplet factors from the fission yeast, Schizosaccharomyces pombe. Unique to this study was the fact that cells were cultured in three different environments: 1) late log growth phase in glucose-based media, 2) stationary phase in glucosebased media, and 3) late log growth phase in media containing oleic acid. We confirmed colocalization of major factors with lipid droplets using live-cell fluorescent microscopy. We also analyzed droplets from each of the three conditions for sterol ester (SE) and triacylglycerol (TAG) content, along with their respective fatty acid compositions. Here, we identified a previously undiscovered lipid droplet protein, Vip1p, which affects droplet size distribution. The results provide further insight into the workings of these ubiquitous organelles.
- Authors:
-
- Univ. of Tennessee, Knoxville, TN (United States)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1545247
- Grant/Contract Number:
- AC05-00OR22725
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Microbiology
- Additional Journal Information:
- Journal Volume: 55; Journal Issue: 2; Journal ID: ISSN 1225-8873
- Publisher:
- Springer
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; lipid droplets; yeast; proteomics; lipid metabolism
Citation Formats
Meyers, Alex, Chourey, Karuna, Weiskittel, Taylor M., Pfiffner, Susan M., Dunlap, John R., Hettich, Robert L., and Dalhaimer, Paul. The protein and neutral lipid composition of lipid droplets isolated from the fission yeast, Schizosaccharomyces pombe. United States: N. p., 2017.
Web. doi:10.1007/s12275-017-6205-1.
Meyers, Alex, Chourey, Karuna, Weiskittel, Taylor M., Pfiffner, Susan M., Dunlap, John R., Hettich, Robert L., & Dalhaimer, Paul. The protein and neutral lipid composition of lipid droplets isolated from the fission yeast, Schizosaccharomyces pombe. United States. https://doi.org/10.1007/s12275-017-6205-1
Meyers, Alex, Chourey, Karuna, Weiskittel, Taylor M., Pfiffner, Susan M., Dunlap, John R., Hettich, Robert L., and Dalhaimer, Paul. Thu .
"The protein and neutral lipid composition of lipid droplets isolated from the fission yeast, Schizosaccharomyces pombe". United States. https://doi.org/10.1007/s12275-017-6205-1. https://www.osti.gov/servlets/purl/1545247.
@article{osti_1545247,
title = {The protein and neutral lipid composition of lipid droplets isolated from the fission yeast, Schizosaccharomyces pombe},
author = {Meyers, Alex and Chourey, Karuna and Weiskittel, Taylor M. and Pfiffner, Susan M. and Dunlap, John R. and Hettich, Robert L. and Dalhaimer, Paul},
abstractNote = {Lipid droplets consist of a core of neutral lipids surrounded by a phospholipid monolayer with bound proteins. Much of the information on lipid droplet function comes from proteomic and lipodomic studies that identify the components of droplets isolated from organisms throughout the phylogenetic tree. Here, we add to that important inventory by reporting lipid droplet factors from the fission yeast, Schizosaccharomyces pombe. Unique to this study was the fact that cells were cultured in three different environments: 1) late log growth phase in glucose-based media, 2) stationary phase in glucosebased media, and 3) late log growth phase in media containing oleic acid. We confirmed colocalization of major factors with lipid droplets using live-cell fluorescent microscopy. We also analyzed droplets from each of the three conditions for sterol ester (SE) and triacylglycerol (TAG) content, along with their respective fatty acid compositions. Here, we identified a previously undiscovered lipid droplet protein, Vip1p, which affects droplet size distribution. The results provide further insight into the workings of these ubiquitous organelles.},
doi = {10.1007/s12275-017-6205-1},
journal = {Journal of Microbiology},
number = 2,
volume = 55,
place = {United States},
year = {Thu Jan 26 00:00:00 EST 2017},
month = {Thu Jan 26 00:00:00 EST 2017}
}
Web of Science
Works referenced in this record:
Yeast Oxidosqualene Cyclase (Erg7p) Is a Major Component of Lipid Particles
journal, November 2001
- Milla, Paola; Athenstaedt, Karin; Viola, Franca
- Journal of Biological Chemistry, Vol. 277, Issue 4
Rab-regulated interaction of early endosomes with lipid droplets
journal, June 2007
- Liu, Pingsheng; Bartz, René; Zehmer, John K.
- Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1773, Issue 6
Proteome of Skeletal Muscle Lipid Droplet Reveals Association with Mitochondria and Apolipoprotein A-I
journal, October 2011
- Zhang, Huina; Wang, Yang; Li, Jing
- Journal of Proteome Research, Vol. 10, Issue 10
Interactions of WASp, myosin-I, and verprolin with Arp2/3 complex during actin patch assembly in fission yeast
journal, August 2005
- Sirotkin, Vladimir; Beltzner, Christopher C.; Marchand, Jean-Baptiste
- The Journal of Cell Biology, Vol. 170, Issue 4
Chinese Hamster Ovary K2 Cell Lipid Droplets Appear to Be Metabolic Organelles Involved in Membrane Traffic
journal, November 2003
- Liu, Pingsheng; Ying, Yunshu; Zhao, Yingming
- Journal of Biological Chemistry, Vol. 279, Issue 5
Characterization of the Drosophila Lipid Droplet Subproteome
journal, March 2006
- Beller, Mathias; Riedel, Dietmar; Jänsch, Lothar
- Molecular & Cellular Proteomics, Vol. 5, Issue 6
Lipid droplet autophagy in the yeast Saccharomyces cerevisiae
journal, January 2014
- van Zutphen, Tim; Todde, Virginia; de Boer, Rinse
- Molecular Biology of the Cell, Vol. 25, Issue 2
Lipid droplets are functionally connected to the endoplasmic reticulum in Saccharomyces cerevisiae
journal, June 2011
- Jacquier, N.; Choudhary, V.; Mari, M.
- Journal of Cell Science, Vol. 124, Issue 14
Biogenesis of the multifunctional lipid droplet: Lipids, proteins, and sites
journal, March 2014
- Pol, Albert; Gross, Steven P.; Parton, Robert G.
- The Journal of Cell Biology, Vol. 204, Issue 5
Protein Correlation Profiles Identify Lipid Droplet Proteins with High Confidence
journal, January 2013
- Krahmer, Natalie; Hilger, Maximiliane; Kory, Nora
- Molecular & Cellular Proteomics, Vol. 12, Issue 5
Heterologous modules for efficient and versatile PCR-based gene targeting inSchizosaccharomyces pombe
journal, July 1998
- Bähler, Jürg; Wu, Jian-Qiu; Longtine, Mark S.
- Yeast, Vol. 14, Issue 10
A lipid-based model for the creation of an escape hatch from the endoplasmic reticulum
journal, July 2007
- Ploegh, Hidde L.
- Nature, Vol. 448, Issue 7152
Triacylglycerol Synthesis Enzymes Mediate Lipid Droplet Growth by Relocalizing from the ER to Lipid Droplets
journal, February 2013
- Wilfling, Florian; Wang, Huajin; Haas, Joel T.
- Developmental Cell, Vol. 24, Issue 4
Perilipin family members preferentially sequester to either triacylglycerol-specific or cholesteryl-ester-specific intracellular lipid storage droplets
journal, June 2012
- Hsieh, Kai; Lee, Yun Kyung; Londos, Constantine
- Journal of Cell Science, Vol. 125, Issue 17
Dictyostelium Lipid Droplets Host Novel Proteins
journal, September 2013
- Du, Xiaoli; Barisch, Caroline; Paschke, Peggy
- Eukaryotic Cell, Vol. 12, Issue 11
Dipeptidyl-peptidase-IV by cleaving neuropeptide Y induces lipid accumulation and PPAR-γ expression
journal, September 2012
- Rosmaninho-Salgado, Joana; Marques, Ana Patricia; Estrada, Marta
- Peptides, Vol. 37, Issue 1
Proteomic Study and Marker Protein Identification of Caenorhabditis elegans Lipid Droplets
journal, April 2012
- Zhang, Peng; Na, Huimin; Liu, Zhenglong
- Molecular & Cellular Proteomics, Vol. 11, Issue 8
Lipid droplet-organelle interactions; sharing the fats
journal, June 2009
- Murphy, Samantha; Martin, Sally; Parton, Robert G.
- Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, Vol. 1791, Issue 6
Essential Role of Cyclophilin A for Hepatitis C Virus Replication and Virus Production and Possible Link to Polyprotein Cleavage Kinetics
journal, August 2009
- Kaul, Artur; Stauffer, Sarah; Berger, Carola
- PLoS Pathogens, Vol. 5, Issue 8
Lipid Droplet-associated Proteins Are Involved in the Biosynthesis and Hydrolysis of Triacylglycerol in Mycobacterium bovis Bacillus Calmette-Guérin
journal, May 2010
- Low, Kai Leng; Shui, Guanghou; Natter, Klaus
- Journal of Biological Chemistry, Vol. 285, Issue 28
YPR139c/LOA1 encodes a novel lysophosphatidic acid acyltransferase associated with lipid droplets and involved in TAG homeostasis
journal, January 2012
- Ayciriex, Sophie; Le Guédard, Marina; Camougrand, Nadine
- Molecular Biology of the Cell, Vol. 23, Issue 2
An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database
journal, November 1994
- Eng, Jimmy K.; McCormack, Ashley L.; Yates, John R.
- Journal of the American Society for Mass Spectrometry, Vol. 5, Issue 11
Proteomic profiling of lipid droplet-associated proteins in primary adipocytes of normal and obese mouse
journal, February 2012
- Ding, Y.; Wu, Y.; Zeng, R.
- Acta Biochimica et Biophysica Sinica, Vol. 44, Issue 5
A role for lipid droplets in inter-membrane lipid traffic
journal, February 2009
- Zehmer, John K.; Huang, Youguo; Peng, Gong
- PROTEOMICS, Vol. 9, Issue 4
Open Questions in Lipid Droplet Biology
journal, January 2014
- Ohsaki, Yuki; Suzuki, Michitaka; Fujimoto, Toyoshi
- Chemistry & Biology, Vol. 21, Issue 1
Proteomics reveal a link between the endoplasmic reticulum and lipid secretory mechanisms in mammary epithelial cells
journal, October 2000
- Wu, Christine C.; Howell, Kathryn E.; Neville, Margaret C.
- Electrophoresis, Vol. 21, Issue 16
Identification of major proteins in the lipid droplet-enriched fraction isolated from the human hepatocyte cell line HuH7
journal, February 2004
- Fujimoto, Yasuyuki; Itabe, Hiroyuki; Sakai, Jun
- Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1644, Issue 1
Expression of oleosin and perilipins in yeast promotes formation of lipid droplets from the endoplasmic reticulum
journal, September 2013
- Jacquier, N.; Mishra, S.; Choudhary, V.
- Journal of Cell Science, Vol. 126, Issue 22
Coupling a Detergent Lysis/Cleanup Methodology with Intact Protein Fractionation for Enhanced Proteome Characterization
journal, October 2012
- Sharma, Ritin; Dill, Brian D.; Chourey, Karuna
- Journal of Proteome Research, Vol. 11, Issue 12
Lipid Droplets Finally Get a Little R-E-S-P-E-C-T
journal, November 2009
- Farese, Robert V.; Walther, Tobias C.
- Cell, Vol. 139, Issue 5
Differentially localized acyl-CoA synthetase 4 isoenzymes mediate the metabolic channeling of fatty acids towards phosphatidylinositol
journal, February 2014
- Küch, Eva-Maria; Vellaramkalayil, Regina; Zhang, Ingrid
- Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, Vol. 1841, Issue 2
Efficient hepatitis C virus particle formation requires diacylglycerol acyltransferase-1
journal, October 2010
- Herker, Eva; Harris, Charles; Hernandez, Céline
- Nature Medicine, Vol. 16, Issue 11
Lipidome and proteome of lipid droplets from the methylotrophic yeast Pichia pastoris
journal, February 2013
- Ivashov, Vasyl A.; Grillitsch, Karlheinz; Koefeler, Harald
- Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, Vol. 1831, Issue 2
An intimate collaboration between peroxisomes and lipid bodies
journal, May 2006
- Binns, Derk; Januszewski, Tom; Chen, Yue
- The Journal of Cell Biology, Vol. 173, Issue 5
Lipid Droplet De Novo Formation and Fission Are Linked to the Cell Cycle in Fission Yeast: Lipid Droplet Dynamics in Fission Yeast
journal, February 2012
- Long, Allan P.; Manneschmidt, Anna K.; VerBrugge, Bobby
- Traffic, Vol. 13, Issue 5
Quantitative proteomic analysis of distinct mammalian Mediator complexes using normalized spectral abundance factors
journal, November 2006
- Paoletti, A. C.; Parmely, T. J.; Tomomori-Sato, C.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 50
Dosage-Dependent Proteome Response of Shewanella oneidensis MR-1 to Acute Chromate Challenge
journal, May 2007
- Thompson, Melissa R.; VerBerkmoes, Nathan C.; Chourey, Karuna
- Journal of Proteome Research, Vol. 6, Issue 5
Sterol-induced Dislocation of 3-Hydroxy-3-methylglutaryl Coenzyme A Reductase from Endoplasmic Reticulum Membranes into the Cytosol through a Subcellular Compartment Resembling Lipid Droplets
journal, April 2010
- Hartman, Isamu Z.; Liu, Pingsheng; Zehmer, John K.
- Journal of Biological Chemistry, Vol. 285, Issue 25
Acyl-CoA synthetase 3 promotes lipid droplet biogenesis in ER microdomains
journal, December 2013
- Kassan, Adam; Herms, Albert; Fernández-Vidal, Andrea
- The Journal of Cell Biology, Vol. 203, Issue 6
Environmental proteomics reveals early microbial community responses to biostimulation at a uranium- and nitrate-contaminated site
journal, August 2013
- Chourey, Karuna; Nissen, Silke; Vishnivetskaya, Tatiana
- PROTEOMICS
Not Just Fat: The Structure and Function of the Lipid Droplet
journal, January 2011
- Fujimoto, T.; Parton, R. G.
- Cold Spring Harbor Perspectives in Biology, Vol. 3, Issue 3
Dual Localization of Squalene Epoxidase, Erg1p, in Yeast Reflects a Relationship between the Endoplasmic Reticulum and Lipid Particles
journal, February 1998
- Leber, Regina; Landl, Karina; Zinser, Erwin
- Molecular Biology of the Cell, Vol. 9, Issue 2
Interactomic study on interaction between lipid droplets and mitochondria
journal, June 2011
- Pu, Jing; Ha, Cheol Woong; Zhang, Shuyan
- Protein & Cell, Vol. 2, Issue 6
Dynamin-Dependent Biogenesis, Cell Cycle Regulation and Mitochondrial Association of Peroxisomes in Fission Yeast
journal, March 2008
- Jourdain, Isabelle; Sontam, Dharani; Johnson, Chad
- Traffic, Vol. 9, Issue 3
Lipid particles/droplets of the yeast Saccharomyces cerevisiae revisited: Lipidome meets Proteome
journal, December 2011
- Grillitsch, Karlheinz; Connerth, Melanie; Köfeler, Harald
- Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, Vol. 1811, Issue 12
Lipid droplets: A dynamic organelle moves into focus
journal, March 2010
- Beller, Mathias; Thiel, Katharina; Thul, Peter J.
- FEBS Letters, Vol. 584, Issue 11
The life of lipid droplets
journal, June 2009
- Walther, Tobias C.; Farese, Robert V.
- Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, Vol. 1791, Issue 6
Proteomic Analysis of Proteins Associated with Lipid Droplets of Basal and Lipolytically Stimulated 3T3-L1 Adipocytes
journal, August 2004
- Brasaemle, Dawn L.; Dolios, Georgia; Shapiro, Lawrence
- Journal of Biological Chemistry, Vol. 279, Issue 45
Screening for Hydrolytic Enzymes Reveals Ayr1p as a Novel Triacylglycerol Lipase in Saccharomyces cerevisiae
journal, November 2013
- Ploier, Birgit; Scharwey, Melanie; Koch, Barbara
- Journal of Biological Chemistry, Vol. 288, Issue 50
DTASelect and Contrast: Tools for Assembling and Comparing Protein Identifications from Shotgun Proteomics
journal, February 2002
- Tabb, David L.; McDonald, W. Hayes; Yates, John R.
- Journal of Proteome Research, Vol. 1, Issue 1, p. 21-26
Biogenesis of cytoplasmic lipid droplets: From the lipid ester globule in the membrane to the visible structure
journal, June 2009
- Ohsaki, Yuki; Cheng, Jinglei; Suzuki, Michitaka
- Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, Vol. 1791, Issue 6
Association of Stomatin with Lipid Bodies
journal, March 2004
- Umlauf, Ellen; Csaszar, Edina; Moertelmaier, Manuel
- Journal of Biological Chemistry, Vol. 279, Issue 22
Analysis of Lipid Particles from Yeast
book, January 2009
- Connerth, Melanie; Grillitsch, Karlheinz; Köfeler, Harald
- Methods in Molecular Biology
Multistep and multimode cortical anchoring of tea1p at cell tips in fission yeast
journal, October 2005
- Snaith, Hilary A.; Samejima, Itaru; Sawin, Kenneth E.
- The EMBO Journal, Vol. 24, Issue 21
Microscopic Analysis of Lipid Droplet Metabolism and Dynamics in Yeast
book, January 2008
- Wolinski, Heimo; Kohlwein, Sepp D.
- Membrane Trafficking
High confidence proteomic analysis of yeast LDs identifies additional droplet proteins and reveals connections to dolichol synthesis and sterol acetylation
journal, May 2014
- Currie, Erin; Guo, Xiuling; Christiano, Romain
- Journal of Lipid Research, Vol. 55, Issue 7
Dynamics of lipid droplets induced by the hepatitis C virus core protein
journal, September 2010
- Lyn, Rodney K.; Kennedy, David C.; Stolow, Albert
- Biochemical and Biophysical Research Communications, Vol. 399, Issue 4
Molecular Dynamics of the Shewanella oneidensis Response to Chromate Stress
journal, March 2006
- Brown, Steven D.; Thompson, Melissa R.; VerBerkmoes, Nathan C.
- Molecular & Cellular Proteomics, Vol. 5, Issue 6
Lipid droplets at a glance
journal, March 2009
- Guo, Y.; Cordes, K. R.; Farese, R. V.
- Journal of Cell Science, Vol. 122, Issue 6
In vitro Formation of a Novel Type of Membrane Vesicles Containing Dpm1p: Putative Transport Vesicles for Lipid Droplets in Budding Yeast
journal, November 2007
- Takeda, Y.; Nakano, A.
- Journal of Biochemistry, Vol. 143, Issue 6
Lipid Droplets and Cellular Lipid Metabolism
journal, July 2012
- Walther, Tobias C.; Farese, Robert V.
- Annual Review of Biochemistry, Vol. 81, Issue 1
Identification and Characterization of Major Lipid Particle Proteins of the Yeast Saccharomyces cerevisiae
journal, October 1999
- Athenstaedt, Karin; Zweytick, Dagmar; Jandrositz, Anita
- Journal of Bacteriology, Vol. 181, Issue 20
Dipeptidyl Peptidase-4 Inhibition Ameliorates Western Diet–Induced Hepatic Steatosis and Insulin Resistance Through Hepatic Lipid Remodeling and Modulation of Hepatic Mitochondrial Function
journal, January 2015
- Aroor, Annayya R.; Habibi, Javad; Ford, David A.
- Diabetes, Vol. 64, Issue 6
A Block in Endoplasmic Reticulum-to-Golgi Trafficking Inhibits Phospholipid Synthesis and Induces Neutral Lipid Accumulation
journal, July 2008
- Gaspar, Maria L.; Jesch, Stephen A.; Viswanatha, Raghuvir
- Journal of Biological Chemistry, Vol. 283, Issue 37, p. 25735-25751
Conditions of endoplasmic reticulum stress stimulate lipid droplet formation in Saccharomyces cerevisiae
journal, October 2009
- Fei, Weihua; Wang, Han; Fu, Xin
- Biochemical Journal, Vol. 424, Issue 1
The size and phospholipid composition of lipid droplets can influence their proteome
journal, November 2011
- Fei, Weihua; Zhong, Ling; Ta, Minh Truong
- Biochemical and Biophysical Research Communications, Vol. 415, Issue 3
Analysis of Yeast Lipid Droplet Proteome and Lipidome
book, January 2013
- Schmidt, Claudia; Ploier, Birgit; Koch, Barbara
- Methods in Cell Biology
Hepatitis C Virus Core Protein Induces Lipid Droplet Redistribution in a Microtubule- and Dynein-Dependent Manner
journal, August 2008
- Boulant, Steeve; Douglas, Mark W.; Moody, Laura
- Traffic, Vol. 9, Issue 8
Protein composition of oil bodies in Arabidopsis thaliana ecotype WS
journal, June 2004
- Jolivet, Pascale; Roux, Emeline; d’Andrea, Sabine
- Plant Physiology and Biochemistry, Vol. 42, Issue 6
Characterization of lipid particles of the yeast,Saccharomyces cerevisiae
journal, November 1994
- Leber, Regina; Zinser, Erwin; Paltauf, Fritz
- Yeast, Vol. 10, Issue 11
Cdk1/Cdc28-Dependent Activation of the Major Triacylglycerol Lipase Tgl4 in Yeast Links Lipolysis to Cell-Cycle Progression
journal, January 2009
- Kurat, Christoph F.; Wolinski, Heimo; Petschnigg, Julia
- Molecular Cell, Vol. 33, Issue 1
Yeast Env9 is a Conserved Oxidoreductase Involved in Lipid Droplet Biogenesis
journal, April 2015
- Siddiqah, Ikha; Manandhar, Surya; Gharakhanian, Editte
- The FASEB Journal, Vol. 29, Issue S1
Works referencing / citing this record:
The New Face of the Lipid Droplet: Lipid Droplet Proteins
journal, October 2018
- Zhang, Congyan; Liu, Pingsheng
- PROTEOMICS, Vol. 19, Issue 10
Effect of Selenium on Lipid and Amino Acid Metabolism in Yeast Cells
journal, April 2018
- Kieliszek, Marek; Błażejak, Stanisław; Bzducha-Wróbel, Anna
- Biological Trace Element Research, Vol. 187, Issue 1
Correction to: Effect of Selenium on Lipid and Amino Acid Metabolism in Yeast Cells
journal, June 2018
- Kieliszek, Marek; Błażejak, Stanisław; Bzducha-Wróbel, Anna
- Biological Trace Element Research, Vol. 187, Issue 1