Membrane shaping proteins, lipids, and cytoskeleton: Recipe for nascent lipid droplet formation.
endoplasmic reticulum
lipid droplets
membrane
organelle biogenesis
septin
Journal
BioEssays : news and reviews in molecular, cellular and developmental biology
ISSN: 1521-1878
Titre abrégé: Bioessays
Pays: United States
ID NLM: 8510851
Informations de publication
Date de publication:
09 2022
09 2022
Historique:
revised:
26
06
2022
received:
15
02
2022
accepted:
29
06
2022
pubmed:
15
7
2022
medline:
25
8
2022
entrez:
14
7
2022
Statut:
ppublish
Résumé
Lipid droplets (LDs) are ubiquitous, neutral lipid storage organelles that act as hubs of metabolic processes. LDs are structurally unique with a hydrophobic core that mainly consists of neutral lipids, sterol esters, and triglycerides, enclosed within a phospholipid monolayer. Nascent LD formation begins with the accumulation of neutral lipids in the endoplasmic reticulum (ER) bilayer. The ER membrane proteins such as seipin, LDAF1, FIT, and MCTPs are reported to play an important role in the formation of nascent LDs. As the LDs grow, they unmix from the highly charged ER membrane to form mature LDs. LD biogenesis is an exciting, emerging research area, and herein, we discuss the recent progress in our understanding of the formation of eukaryotic nascent LDs. We focus on the role of ER membrane shaping proteins such as reticulons and reticulon-like proteins, membrane lipids, and cytoskeleton proteins such as septin in the formation of nascent LDs.
Identifiants
pubmed: 35832014
doi: 10.1002/bies.202200038
doi:
Substances chimiques
Membrane Lipids
0
Membrane Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e2200038Informations de copyright
© 2022 Wiley Periodicals LLC.
Références
Henry, S. A., Kohlwein, S. D., & Carman, G. M. (2012). Metabolism and regulation of glycerolipids in the yeast Saccharomyces cerevisiae. Genetics, 190(2), 317-349. https://doi.org/10.1534/genetics.111.130286
Olzmann, J. A., & Carvalho, P. (2019). Dynamics and functions of lipid droplets. Nature Reviews Molecular Cell Biology, 20(3), 137-155. https://doi.org/10.1038/s41580-018-0085-z
Olarte, M.-J., Swanson, J. M. J., Walther, T. C., & Farese, R. V. (2022). The CYTOLD and ERTOLD pathways for lipid droplet-protein targeting. Trends in Biochemical Sciences, 47(1), 39-51. https://doi.org/10.1016/j.tibs.2021.08.007
Renne, M. F., & Hariri, H. (2021). Lipid droplet-organelle contact sites as hubs for fatty acid metabolism, trafficking, and metabolic channeling. Frontiers in Cell and Developmental Biology, 9, 726261. https://doi.org/10.3389/fcell.2021.726261
Choudhary, V., Ojha, N., Golden, A., & Prinz, W. A. (2015). A conserved family of proteins facilitates nascent lipid droplet budding from the ER. Journal of Cell Biology, 211(2), 261-271. https://doi.org/10.1083/jcb.201505067
Chorlay, A., Monticelli, L., Veríssimo Ferreira, J., Ben M'barek, K., Ajjaji, D., Wang, S., Johnson, E., Beck, R., Omrane, M., Beller, M., Carvalho, P., & Rachid Thiam, A. (2019). Membrane asymmetry imposes directionality on lipid droplet emergence from the ER. Developmental Cell, 50(1), 25-42.e7. https://doi.org/10.1016/j.devcel.2019.05.003
Choudhary, V., Golani, G., Joshi, A. S., Cottier, S., Schneiter, R., Prinz, W. A., & Kozlov, M. M. (2018). Architecture of lipid droplets in endoplasmic reticulum is determined by phospholipid intrinsic curvature. Current Biology, 28(6), 915-926.e9. https://doi.org/10.1016/j.cub.2018.02.020
Jacquier, N., Choudhary, V., Mari, M., Toulmay, A., Reggiori, F., & Schneiter, R. (2011). Lipid droplets are functionally connected to the endoplasmic reticulum in Saccharomyces cerevisiae. Journal of Cell Science, 124(14), 2424-2437. https://doi.org/10.1242/jcs.076836
Salo, V. T., Belevich, I., Li, S., Karhinen, L., Vihinen, H., Vigouroux, C., Magré, J., Thiele, C., Hölttä-Vuori, M., Jokitalo, E., & Ikonen, E. (2016). Seipin regulates ER - lipid droplet contacts and cargo delivery. The EMBO Journal, 35(24), 2699-2716. https://doi.org/10.15252/embj.201695170
Salo, V. T., Li, S., Vihinen, H., Hölttä-Vuori, M., Szkalisity, A., Horvath, P., Belevich, I., Peränen, J., Thiele, C., Somerharju, P., Zhao, H., Santinho, A., Thiam, A. R., Jokitalo, E., & Ikonen, E. (2019). Seipin facilitates triglyceride flow to lipid droplet and counteracts droplet ripening via endoplasmic reticulum contact. Developmental Cell, 50(4), 478-493.e9. https://doi.org/10.1016/j.devcel.2019.05.016
Wilfling, F., Thiam, A. R., Olarte, M.-J., Wang, J., Beck, R., Gould, T. J., Allgeyer, E. S., Pincet, F., Bewersdorf, J., Farese, R. V., & Walther, T. C. (2014). Arf1/COPI machinery acts directly on lipid droplets and enables their connection to the ER for protein targeting. ELife, 3, e01607. https://doi.org/10.7554/eLife.01607
Walther, T. C., Chung, J., & Farese, R. V. (2017). Lipid droplet biogenesis. Annual Review of Cell and Developmental Biology, 33, 491-510. https://doi.org/10.1146/annurev-cellbio-100616-060608
Wilfling, F., Haas, J. T., Walther, T. C., & Farese, R. V. (2014). Lipid droplet biogenesis. Current Opinion in Cell Biology, 29, 39-45. https://doi.org/10.1016/j.ceb.2014.03.008
Chung, J., Wu, X., Lambert, T. J., Lai, Z. W., Walther, T. C., & Farese, R. V. (2019). LDAF1 and seipin form a lipid droplet assembly complex. Developmental Cell, 51(5), 551-563.e7. https://doi.org/10.1016/j.devcel.2019.10.006
Chen, F., Yan, B., Ren, J., Lyu, R., Wu, Y., Guo, Y., Li, D., Zhang, H., & Hu, J. (2021). FIT2 organizes lipid droplet biogenesis with ER tubule-forming proteins and septins. The Journal of Cell Biology, 220(5), e201907183. https://doi.org/10.1083/jcb.201907183
Joshi, A. S., Ragusa, J. V., Prinz, W. A., & Cohen, S. (2021). Multiple C2 domain-containing transmembrane proteins promote lipid droplet biogenesis and growth at specialized endoplasmic reticulum subdomains. Molecular Biology of the Cell, 32(12), 1147-1157. https://doi.org/10.1091/mbc.E20-09-0590
Joshi, A. S., Nebenfuehr, B., Choudhary, V., Satpute-Krishnan, P., Levine, T. P., Golden, A., & Prinz, W. A. (2018). Lipid droplet and peroxisome biogenesis occur at the same ER subdomains. Nature Communications, 9(1), 2940. https://doi.org/10.1038/s41467-018-05277-3
Wang, H., Becuwe, M., Housden, B. E., Chitraju, C., Porras, A. J., Graham, M. M., Liu, X. N., Thiam, A. R., Savage, D. B., Agarwal, A. K., Garg, A., Olarte, M.-J., Lin, Q., Fröhlich, F., Hannibal-Bach, H. K., Upadhyayula, S., Perrimon, N., Kirchhausen, T., Ejsing, C. S., … Farese, R. V. (2016). Seipin is required for converting nascent to mature lipid droplets. ELife, 5, e16582. https://doi.org/10.7554/eLife.16582
Kassan, A., Herms, A., Fernández-Vidal, A., Bosch, M., Schieber, N. L., Reddy, B. J. N., Fajardo, A., Gelabert-Baldrich, M., Tebar, F., Enrich, C., Gross, S. P., Parton, R. G., & Pol, A. (2013). Acyl-CoA synthetase 3 promotes lipid droplet biogenesis in ER microdomains. The Journal of Cell Biology, 203(6), 985-1001. https://doi.org/10.1083/jcb.201305142
Choudhary, V., El Atab, O., Mizzon, G., Prinz, W. A., & Schneiter, R. (2020). Seipin and Nem1 establish discrete ER subdomains to initiate yeast lipid droplet biogenesis. Journal of Cell Biology, 219(7), e201910177. https://doi.org/10.1083/jcb.201910177
Zoni, V., Khaddaj, R., Campomanes, P., Thiam, A. R., Schneiter, R., & Vanni, S. (2021). Pre-existing bilayer stresses modulate triglyceride accumulation in the ER versus lipid droplets. ELife, 10, e62886. https://doi.org/10.7554/eLife.62886
Santinho, A., Salo, V. T., Chorlay, A., Li, S., Zhou, X., Omrane, M., Ikonen, E., & Thiam, A. R. (2020). Membrane curvature catalyzes lipid droplet assembly. Current Biology, 30(13), 2481-2494.e6. https://doi.org/10.1016/j.cub.2020.04.066
Ben M'barek, K., Ajjaji, D., Chorlay, A., Vanni, S., Forêt, L., & Thiam, A. R. (2017). ER membrane phospholipids and surface tension control cellular lipid droplet formation. Developmental Cell, 41(6), 591-604.e7. https://doi.org/10.1016/j.devcel.2017.05.012
Mak, H. Y., Ouyang, Q., Tumanov, S., Xu, J., Rong, P., Dong, F., Lam, S. M., Wang, X., Lukmantara, I., Du, X., Gao, M., Brown, A. J., Gong, X., Shui, G., Stocker, R., Huang, X., Chen, S., & Yang, H. (2021). AGPAT2 interaction with CDP-diacylglycerol synthases promotes the flux of fatty acids through the CDP-diacylglycerol pathway. Nature Communications, 12(1), 6877. https://doi.org/10.1038/s41467-021-27279-4
Cartwright, B. R., & Goodman, J. M. (2012). Seipin: From human disease to molecular mechanism. Journal of Lipid Research, 53(6), 1042-1055. https://doi.org/10.1194/jlr.R023754
Gross, D. A., Zhan, C., & Silver, D. L. (2011). Direct binding of triglyceride to fat storage-inducing transmembrane proteins 1 and 2 is important for lipid droplet formation. Proceedings of the National Academy of Sciences of the United States of America, 108(49), 19581-19586. https://doi.org/10.1073/pnas.1110817108
Tauchi-Sato, K., Ozeki, S., Houjou, T., Taguchi, R., & Fujimoto, T. (2002). The surface of lipid droplets is a phospholipid monolayer with a unique fatty acid composition. The Journal of Biological Chemistry, 277(46), 44507-44512. https://doi.org/10.1074/jbc.M207712200
Bartz, R., Li, W.-H., Venables, B., Zehmer, J. K., Roth, M. R., Welti, R., Anderson, R. G. W., Liu, P., & Chapman, K. D. (2007). Lipidomics reveals that adiposomes store ether lipids and mediate phospholipid traffic. Journal of Lipid Research, 48(4), 837-847. https://doi.org/10.1194/jlr.M600413-JLR200
Krahmer, N., Guo, Y., Wilfling, F., Hilger, M., Lingrell, S., Heger, K., Newman, H. W., Schmidt-Supprian, M., Vance, D. E., Mann, M., Farese, R. V., & Walther, T. C. (2011). Phosphatidylcholine synthesis for lipid droplet expansion is mediated by localized activation of CTP: Phosphocholine cytidylyltransferase. Cell Metabolism, 14(4), 504-515. https://doi.org/10.1016/j.cmet.2011.07.013
Penno, A., Hackenbroich, G., & Thiele, C. (2013). Phospholipids and lipid droplets. Biochimica et Biophysica Acta, 1831(3), 589-594. https://doi.org/10.1016/j.bbalip.2012.12.001
Voeltz, G. K., Prinz, W. A., Shibata, Y., Rist, J. M., & Rapoport, T. A. (2006). A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell, 124(3), 573-586. https://doi.org/10.1016/j.cell.2005.11.047
Klemm, R. W., Norton, J. P., Cole, R. A., Li, C. S., Park, S. H., Crane, M. M., Li, L., Jin, D., Boye-Doe, A., Liu, T. Y., Shibata, Y., Lu, H., Rapoport, T. A., Farese, R. V., Blackstone, C., Guo, Y., & Mak, H. Y. (2013). A conserved role for atlastin GTPases in regulating lipid droplet size. Cell Reports, 3(5), 1465-1475. https://doi.org/10.1016/j.celrep.2013.04.015
Renvoisé, B., Malone, B., Falgairolle, M., Munasinghe, J., Stadler, J., Sibilla, C., Park, S. H., & Blackstone, C. (2016). Reep1 null mice reveal a converging role for hereditary spastic paraplegia proteins in lipid droplet regulation. Human Molecular Genetics, 25(23), 5111-5125. https://doi.org/10.1093/hmg/ddw315
Falk, J., Rohde, M., Bekhite, M. M., Neugebauer, S., Hemmerich, P., Kiehntopf, M., Deufel, T., Hübner, C. A., & Beetz, C. (2014). Functional mutation analysis provides evidence for a role of REEP1 in lipid droplet biology. Human Mutation, 35(4), 497-504. https://doi.org/10.1002/humu.22521
Joshi, A. S., Huang, X., Choudhary, V., Levine, T. P., Hu, J., & Prinz, W. A. (2016). A family of membrane-shaping proteins at ER subdomains regulates pre-peroxisomal vesicle biogenesis. Journal of Cell Biology, 215(4), 515-529. https://doi.org/10.1083/jcb.201602064
Fei, W., Shui, G., Gaeta, B., Du, X., Kuerschner, L., Li, P., Brown, A. J., Wenk, M. R., Parton, R. G., & Yang, H. (2008). Fld1p, a functional homologue of human seipin, regulates the size of lipid droplets in yeast. Journal of Cell Biology, 180(3), 473-482. https://doi.org/10.1083/jcb.200711136
Sui, X., Arlt, H., Brock, K. P., Lai, Z. W., DiMaio, F., Marks, D. S., Liao, M., Farese, R. V., & Walther, T. C. (2018). Cryo-electron microscopy structure of the lipid droplet-formation protein seipin. Journal of Cell Biology, 217(12), 4080-4091. https://doi.org/10.1083/jcb.201809067
Yan, R., Qian, H., Lukmantara, I., Gao, M., Du, X., Yan, N., & Yang, H. (2018). Human SEIPIN binds anionic phospholipids. Developmental Cell, 47(2), 248-256.e4. https://doi.org/10.1016/j.devcel.2018.09.010
Zoni, V., Khaddaj, R., Lukmantara, I., Shinoda, W., Yang, H., Schneiter, R., & Vanni, S. (2021). Seipin accumulates and traps diacylglycerols and triglycerides in its ring-like structure. Proceedings of the National Academy of Sciences of the United States of America, 118(10), e2017205118. https://doi.org/10.1073/pnas.2017205118
Kadereit, B., Kumar, P., Wang, W.-J., Miranda, D., Snapp, E. L., Severina, N., Torregroza, I., Evans, T., & Silver, D. L. (2008). Evolutionarily conserved gene family important for fat storage. Proceedings of the National Academy of Sciences of the United States of America, 105(1), 94-99. https://doi.org/10.1073/pnas.0708579105
Becuwe, M., Bond, L. M., Pinto, A. F. M., Boland, S., Mejhert, N., Elliott, S. D., Cicconet, M., Graham, M. M., Liu, X. N., Ilkayeva, O., Saghatelian, A., Walther, T. C., & Farese, R. V. (2020). FIT2 is an acyl-coenzyme A diphosphatase crucial for endoplasmic reticulum homeostasis. The Journal of Cell Biology, 219(10), e202006111. https://doi.org/10.1083/jcb.202006111
Beber, A., Alqabandi, M., Prévost, C., Viars, F., Lévy, D., Bassereau, P., Bertin, A., & Mangenot, S. (2019). Septin-based readout of PI(4,5)P2 incorporation into membranes of giant unilamellar vesicles. Cytoskeleton, (Hoboken, N.J.), 76(1), 92-103. https://doi.org/10.1002/cm.21480
Woods, B. L., Cannon, K. S., Vogt, E. J. D., Crutchley, J. M., & Gladfelter, A. S. (2021). Interplay of septin amphipathic helices in sensing membrane-curvature and filament bundling. Molecular Biology of the Cell, 32(20), br5. https://doi.org/10.1091/mbc.E20-05-0303
Vial, A., Taveneau, C., Costa, L., Chauvin, B., Nasrallah, H., Godefroy, C., Dosset, P., Isambert, H., Ngo, K. X., Mangenot, S., Levy, D., Bertin, A., & Milhiet, P.-E. (2021). Correlative AFM and fluorescence imaging demonstrate nanoscale membrane remodeling and ring-like and tubular structure formation by septins. Nanoscale, 13(29), 12484-12493. https://doi.org/10.1039/d1nr01978c