Lipid Droplets Embedded in a Model Cell Membrane Create a Phospholipid Diffusion Barrier.
lipid bilayers
lipid diffusion
lipid droplets
monotopic membrane proteins
phospholipid monolayers
wetting
Journal
Small (Weinheim an der Bergstrasse, Germany)
ISSN: 1613-6829
Titre abrégé: Small
Pays: Germany
ID NLM: 101235338
Informations de publication
Date de publication:
03 2022
03 2022
Historique:
revised:
09
12
2021
received:
26
10
2021
pubmed:
25
1
2022
medline:
5
4
2022
entrez:
24
1
2022
Statut:
ppublish
Résumé
Lipid droplets (LDs) are ubiquitous, cytoplasmic fat storage organelles that originate from the endoplasmic reticulum (ER) membrane. They are composed of a core of neutral lipids surrounded by a phospholipid monolayer. Proteins embedded into this monolayer membrane adopt a monotopic topology and are crucial for regulated lipid storage and consumption. A key question is, which collective properties of protein-intrinsic and lipid-mediated features determine spatio-temporal protein partitioning between phospholipid bilayer and LD monolayer membranes. To address this question, a freestanding phospholipid bilayer with physiological lipidic composition is produced using microfluidics and micrometer-sized LDs are dispersed around the bilayer that spontaneously insert into the bilayer. Using confocal microscopy, the 3D geometry of the reconstituted LDs is determined with high spatial resolution. The micrometer-sized bilayer-embedded LDs present a characteristic lens shape that obeys predictions from equilibrium wetting theory. Fluorescence recovery after photobleaching measurements reveals the existence of a phospholipid diffusion barrier at the monolayer-bilayer interface. Coarse-grained molecular dynamics simulation reveals lipid specific density distributions along the pore rim, which may rationalize the diffusion barrier. The lipid diffusion barrier between the LD covering monolayer and the bilayer may be a key phenomenon influencing protein partitioning between the ER membrane and LDs in living cells.
Identifiants
pubmed: 35072348
doi: 10.1002/smll.202106524
doi:
Substances chimiques
Phospholipids
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e2106524Informations de copyright
© 2022 The Authors. Small published by Wiley-VCH GmbH.
Références
M. A. Welte, A. P. Gould, Biochim. Biophys. Acta, Mol. Cell Biol. Lipids 2017, 1862, 1260.
Y. Guo, T. C. Walther, M. Rao, N. Stuurman, G. Goshima, K. Terayama, J. S. Wong, R. D. Vale, P. Walter, R. V. Farese, Nature 2008, 453, 657.
T. C. Walther, J. Chung, R. V. Farese, Ann. Rev. Cell Dev. Biol. 2017, 33, 491.
J. A. Olzmann, P. Carvalho, Nat. Rev. Mol. Cell Biol. 2019, 20, 137.
H. Khandelia, L. Duelund, K. I. Pakkanen, J. H. Ipsen, PLoS ONE 2010, 5, e12811.
M. J. Greenall, C. M. Marques, Soft Matter 2012, 8, 3308.
V. Zoni, V. Nieto, L. J. Endter, H. J. Risselada, L. Monticelli, S. Vanni, Front. Mol. Biosci. 2019, 6, 2017.
A. Masedunskas, Y. Chen, R. Stussman, R. Weigert, I. H. Mather, MBoC 2017, 28, 935.
K. D. Chapman, J. M. Dyer, R. T. Mullen, J. Lipid Res. 2012, 53, 215.
V. Choudhary, N. Ojha, A. Golden, W. A. Prinz, J. Cell Biol. 2015, 211, 261.
R. Dhiman, S. Caesar, A. R. Thiam, B. Schrul, Semin. Cell Dev. Biol. 2020, 108, 4.
K. Bersuker, J. A. Olzmann, Biochim. Biophys. Acta 2017, 1862, 1166.
A. L. S. Cruz, E. d. A. Barreto, N. P. B. Fazolini, J. P. B. Viola, P. T. Bozza, Cell Death Dis. 2020, 11, 105.
T. Fujimoto, R. G. Parton, Cold Spring Harb. Perspect. Biol. 2011, 3, 3.
R. Bartz, W.-H. Li, B. Venables, J. K. Zehmer, M. R. Roth, R. Welti, R. G. W. Anderson, P. Liu, K. D. Chapman, J. Lipid Res. 2007, 48, 837.
K. Tauchi-Sato, S. Ozeki, T. Houjou, R. Taguchi, T. Fujimoto, J. Biol. Chem. 2002, 277, 44507.
P. J. Horn, N. R. Ledbetter, C. N. James, W. D. Hoffman, C. R. Case, G. F. Verbeck, K. D. Chapman, J. Biol. Chem. 2011, 286, 3298.
G. Onal, O. Kutlu, D. Gozuacik, S. Dokmeci Emre, Lipids Health Dis. 2017, 16, 128.
T. Fujii, Microelectron. Eng. 2002, 61-62, 907.
P. Heo, S. Ramakrishnan, J. Coleman, J. E. Rothman, J.-B. Fleury, F. Pincet, Small 2019, 15, 1900725.
H. Kusumaatmaja, R. Lipowsky, Soft Matter 2011, 7, 6914.
B. Winckler, P. Forscher, I. Mellman, Nature 1999, 397, 698.
H. Tawfik, S. Puza, R. Seemann, J.-B. Fleury, Front. Cell Dev. Biol. 2020, 8, 531229.
J.-B. Fleury, M. Werner, X. L. Guével, V. A. Baulin, J. Colloid Interface Sci. 2021, 603, 550.
K. Triantafilou, M. Triantafilou, S. Ladha, A. Mackie, R. L. Dedrick, N. Fernandez, R. Cherry, J. Cell Sci. 2001, 114, 2535.
M. Garten, L. D. Mosgaard, T. Bornschlögl, S. Dieudonné, P. Bassereau, G. E. S. Toombes, Proc. Natl. Acad. Sci. U. S. A. 2017, 114, 328.
L. Fouillen, L. Maneta-Peyret, P. Moreau, Methods Mol. Biol. 2018, 1691, 125.
T. K. Fam, A. S. Klymchenko, M. Collot, Materials (Basel) 2018, 11, 9.
P. A. Ferrari, S. Goldstein, J. L. Lebowitz, in,Statistical Physics and Dynamical Systems: Rigorous Results (Eds: J. Fritz, A. Jaffe, D. Szász), Progress in Physics, Birkhäuser, Boston, MA 1985, pp. 405-441.
V. Choudhary, G. Golani, A. S. Joshi, S. Cottier, R. Schneiter, W. A. Prinz, M. M. Kozlov, Curr. Biol. 2018, 28, 915.
L. V. Chernomordik, M. M. Kozlov, Nat. Struct. Mol. Biol. 2008, 15, 675.
C. S. Poojari, K. C. Scherer, J. S. Hub, Free energies of stalk formation in the lipidomics era, Technical report, 2021, https://www.biorxiv.org/content/10.1101/2021.06.02.446700v1, Company: Cold Spring Harbor Laboratory Distributor: Cold Spring Harbor Laboratory Label: Cold Spring Harbor Laboratory Section: New Results Type: article.
P. G. de Gennes, Rev. Mod. Phys. 1985, 57, 827.
N. Khangholi, R. Seemann, J.-B. Fleury, Biomicrofluidics 2020, 14, 024117.
A. Chorlay, A. R. Thiam, Biophys. J. 2018, 114, 631.
A. Chorlay, L. Monticelli, J. V. Ferreira, K. B. M'barek, D. Ajjaji, S. Wang, E. Johnson, R. Beck, M. Omrane, M. Beller, P. Carvalho, A. R. Thiam, Develop. Cell 2019, 50, 25.
T. Takei, T. Yaguchi, T. Fujii, T. Nomoto, T. Toyota, M. Fujinami, Soft Matter 2015, 11, 8641.
D. M. Soumpasis, Biophys. J. 1983, 41, 95.
T. Wang, C. Ingram, J. C. Weisshaar, Langmuir 2010, 26, 11157.
M. Przybylo, J. Sýkora, J. Humpolíckova, A. Benda, A. Zan, M. Hof, Langmuir 2006, 22, 9096.
S. J. Marrink, H. J. Risselada, S. Yefimov, D. P. Tieleman, A. H. de Vries, J. Phys. Chem. B 2007, 111, 7812.
V. Zoni, R. Khaddaj, P. Campomanes, A. R. Thiam, R. Schneiter, S. Vanni, eLife 2021, 10, e62886.
L. Caillon, V. Nieto, P. Gehan, M. Omrane, N. Rodriguez, L. Monticelli, A. R. Thiam, Nat. Comm. 2020, 11, 3944.
N. Malmstadt, M. A. Nash, R. F. Purnell, J. J. Schmidt, Nano Lett. 2006, 6, 1961.
M. J. Abraham, T. Murtola, R. Schulz, S. Páll, J. C. Smith, B. Hess, E. Lindahl, SoftwareX 2015, 1-2, 19.
G. Bussi, D. Donadio, M. Parrinello, J. Chem. Phys. 2007, 126, 014101.
H. J. C. Berendsen, J. P. M. Postma, W. F. van Gunsteren, A. DiNola, J. R. Haak, J. Chem. Phys. 1984, 81, 3684.
B. Hess, J. Chem. Theory Comput. 2008, 4, 116.
T. A. Wassenaar, H. I. Ingólfsson, R. A. Böckmann, D. P. Tieleman, S. J. Marrink, J. Chem. Theory Comput. 2015, 11, 2144.