A conserved family of proteins facilitates nascent lipid droplet budding from the ER

Journal of Cell Biology

Volumn 211, Issue 2, 2015, Pages 261-271

  Choudhary, Vineet ^a   Ojha, Namrata ^a   Golden, Andy ^a   Prinz, William A ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FAT DROPLET; FIT2 PROTEIN, MOUSE; MEMBRANE PROTEIN; SMALL INTERFERING RNA;

ARTICLE; BIOGENESIS; BUDDING; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM MEMBRANE; LIPID STORAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN STRUCTURE; 3T3 CELL LINE; ANIMAL; CELL LINE; GENETICS; LETHAL GENE; LIPID METABOLISM; METABOLISM; MOUSE; PHYSIOLOGY; RNA INTERFERENCE;

3T3 CELLS; ANIMALS; CAENORHABDITIS ELEGANS; CELL LINE; ENDOPLASMIC RETICULUM; GENES, LETHAL; LIPID DROPLETS; LIPID METABOLISM; MEMBRANE PROTEINS; MICE; MICROSCOPY, ELECTRON; RNA INTERFERENCE; RNA, SMALL INTERFERING;

EID: 84971299729     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201505067     Document Type: Article

References (67)

1. Adeyo, O., P.J. Horn, S. Lee, D.D. Binns, A. Chandrahas, K.D. Chapman, and J.M. Goodman. 2011. The yeast lipin orthologue Pah1p is important for biogenesis of lipid droplets. J. Cell Biol. 192:1043-1055. http://dx.doi.org/10.1083/jcb.201010111
2. Agarwal, A.K., and A. Garg. 2004. Seipin: a mysterious protein. Trends Mol. Med. 10:440-444. http://dx.doi.org/10.1016/j.molmed.2004.07.009
3. Andersson, L., P. Boström, J. Ericson, M. Rutberg, B. Magnusson, D. Marchesan, M. Ruiz, L. Asp, P. Huang, M.A. Frohman, et al. 2006. PLD1 and ERK2 regulate cytosolic lipid droplet formation. J. Cell Sci. 119:2246-2257. http://dx.doi.org/10.1242/jcs.02941
4. Arribere, J.A., R.T. Bell, B.X. Fu, K.L. Artiles, P.S. Hartman, and A.Z. Fire. 2014. Efficient marker-free recovery of custom genetic modifications with CRI SPR/Cas9 in Caenorhabditis elegans. Genetics. 198:837-846. http://dx.doi.org/10.1534/genetics.114.169730
5. Athenstaedt, K., and G. Daum. 2003. YMR313c/TGL3 encodes a novel triacylglycerol lipase located in lipid particles of Saccharomyces cerevisiae. J. Biol. Chem. 278:23317-23323. http://dx.doi.org/10.1074/jbc.M302577200
6. Athenstaedt, K., and G. Daum. 2005. Tgl4p and Tgl5p, two triacylglycerol lipases of the yeast Saccharomyces cerevisiae are localized to lipid particles. J. Biol. Chem. 280:37301-37309. http://dx.doi.org/10.1074/jbc.M507261200
7. Bernales, S., K.L. McDonald, and P. Walter. 2006. Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biol. 4:e423. http://dx.doi.org/10.1371/journal.pbio.0040423
8. Binns, D., T. Januszewski, Y. Chen, J. Hill, V.S. Markin, Y. Zhao, C. Gilpin, K.D. Chapman, R.G. Anderson, and J.M. Goodman. 2006. An intimate collaboration between peroxisomes and lipid bodies. J. Cell Biol. 173:719-731. http://dx.doi.org/10.1083/jcb.200511125
9. Branicky, R., D. Desjardins, J.L. Liu, and S. Hekimi. 2010. Lipid transport and signaling in Caenorhabditis elegans. Dev. Dyn. 239:1365-1377.
10. Brasaemle, D.L., and N.E. Wolins. 2012. Packaging of fat: an evolving model of lipid droplet assembly and expansion. J. Biol. Chem. 287:2273-2279. http://dx.doi.org/10.1074/jbc.R111.309088
11. Carman, G.M., and G.S. Han. 2009. Phosphatidic acid phosphatase, a key enzyme in the regulation of lipid synthesis. J. Biol. Chem. 284:2593-2597. http://dx.doi.org/10.1074/jbc.R800059200
12. Cartwright, B.R., D.D. Binns, C.L. Hilton, S. Han, Q. Gao, and J.M. Goodman. 2015. Seipin performs dissectible functions in promoting lipid droplet biogenesis and regulating droplet morphology. Mol. Biol. Cell. 26:726-739. http://dx.doi.org/10.1091/mbc.E14-08-1303
13. Choudhary, V., N. Jacquier, and R. Schneiter. 2011. The topology of the triacylglycerol synthesizing enzyme Lro1 indicates that neutral lipids can be produced within the luminal compartment of the endoplasmatic reticulum: implications for the biogenesis of lipid droplets. Commun. Integr. Biol. 4:781-784. http://dx.doi.org/10.4161/cib.17830
14. Czabany, T., K. Athenstaedt, and G. Daum. 2007. Synthesis, storage and degradation of neutral lipids in yeast. Biochim. Biophys. Acta. 1771:299-309. http://dx.doi.org/10.1016/j.bbalip.2006.07.001
15. Dickinson, D.J., J.D. Ward, D.J. Reiner, and B. Goldstein. 2013. Engineering the Caenorhabditis elegans genome using Cas9-triggered homologous recombination. Nat. Methods. 10:1028-1034. http://dx.doi.org/10.1038/nmeth.2641
16. Fei, W., G. Shui, B. Gaeta, X. Du, L. Kuerschner, P. Li, A.J. Brown, M.R. Wenk, R.G. Parton, and H. Yang. 2008. Fld1p, a functional homologue of human seipin, regulates the size of lipid droplets in yeast. J. Cell Biol. 180:473-482. http://dx.doi.org/10.1083/jcb.200711136
17. Fei, W., H. Wang, X. Fu, C. Bielby, and H. Yang. 2009. Conditions of endoplasmic reticulum stress stimulate lipid droplet formation in Saccharomyces cerevisiae. Biochem. J. 424:61-67.
18. Goh, V.J., and D.L. Silver. 2013. The lipid droplet as a potential therapeutic target in NAF LD. Semin. Liver Dis. 33:312-320. http://dx.doi.org/10.1055/s-0033-1358521
19. Goh, V.J., J.S. Tan, B.C. Tan, C. Seow, W.Y. Ong, Y.C. Lim, L. Sun, S. Ghosh, and D.L. Silver. 2015. Postnatal deletion of Fat storage-inducing Transmembrane Protein 2 (FIT2/FITM2) causes lethal enteropathy. J. Biol. Chem. http://dx.doi.org/10.1074/jbc.M115.676700
20. Gross, D.A., and D.L. Silver. 2014. Cytosolic lipid droplets: from mechanisms of fat storage to disease. Crit. Rev. Biochem. Mol. Biol. 49:304-326. http://dx.doi.org/10.3109/10409238.2014.931337.
21. Gross, D.A., C. Zhan, and D.L. Silver. 2011. Direct binding of triglyceride to fat storage-inducing transmembrane proteins 1 and 2 is important for lipid droplet formation. Proc. Natl. Acad. Sci. USA. 108:19581-19586. http://dx.doi.org/10.1073/pnas.1110817108
22. Guo, Y., T.C. Walther, M. Rao, N. Stuurman, G. Goshima, K. Terayama, J.S. Wong, R.D. Vale, P. Walter, and R.V. Farese. 2008. Functional genomic screen reveals genes involved in lipid-droplet formation and utilization. Nature. 453:657-661. http://dx.doi.org/10.1038/nature06928
23. Hartman, I.Z., P. Liu, J.K. Zehmer, K. Luby-Phelps, Y. Jo, R.G. Anderson, and R.A. DeBose-Boyd. 2010. 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. J. Biol. Chem. 285:19288-19298. http://dx.doi.org/10.1074/jbc.M110.134213
24. Henry, S.A., S.D. Kohlwein, and G.M. Carman. 2012. Metabolism and regulation of glycerolipids in the yeast Saccharomyces cerevisiae. Genetics. 190:317-349. http://dx.doi.org/10.1534/genetics.111.130286
25. Hosaka, K., J. Nikawa, T. Kodaki, H. Ishizu, and S. Yamashita. 1994. Cloning and sequence of the SCS3 gene which is required for inositol prototrophy in Saccharomyces cerevisiae. J. Biochem. 116:1317-1321.
26. Jacquier, N., V. Choudhary, M. Mari, A. Toulmay, F. Reggiori, and R. Schneiter. 2011. Lipid droplets are functionally connected to the endoplasmic reticulum in Saccharomyces cerevisiae. J. Cell Sci. 124:2424-2437. http://dx.doi.org/10.1242/jcs.076836
27. Jacquier, N., S. Mishra, V. Choudhary, and R. Schneiter. 2013. Expression of oleosin and perilipins in yeast promotes formation of lipid droplets from the endoplasmic reticulum. J. Cell Sci. 126:5198-5209. http://dx.doi.org/10.1242/jcs.131896
28. Kadereit, B., P. Kumar, W.J. Wang, D. Miranda, E.L. Snapp, N. Severina, I. Torregroza, T. Evans, and D.L. Silver. 2008. Evolutionarily conserved gene family important for fat storage. Proc. Natl. Acad. Sci. USA. 105:94-99. http://dx.doi.org/10.1073/pnas.0708579105
29. Karanasios, E., A.D. Barbosa, H. Sembongi, M. Mari, G.S. Han, F. Reggiori, G.M. Carman, and S. Siniossoglou. 2013. Regulation of lipid droplet and membrane biogenesis by the acidic tail of the phosphatidate phosphatase Pah1p. Mol. Biol. Cell. 24:2124-2133. http://dx.doi.org/10.1091/mbc.E13-01-0021
30. Khandelia, H., L. Duelund, K.I. Pakkanen, and J.H. Ipsen. 2010. Triglyceride blisters in lipid bilayers: implications for lipid droplet biogenesis and the mobile lipid signal in cancer cell membranes. PLoS ONE. 5:e12811. http://dx.doi.org/10.1371/journal.pone.0012811
31. Köffel, R., R. Tiwari, L. Falquet, and R. Schneiter. 2005. The Saccharomyces cerevisiae YLL012/YEH1, YLR020/YEH2, and TGL1 genes encode a novel family of membrane-anchored lipases that are required for steryl ester hydrolysis. Mol. Cell. Biol. 25:1655-1668. http://dx.doi.org/10.1128/MCB.25.5.1655-1668.2005
32. Kohlwein, S.D. 2010. Triacylglycerol homeostasis: insights from yeast. J. Biol. Chem. 285:15663-15667. http://dx.doi.org/10.1074/jbc.R110.118356
33. Lahiri, S., J.T. Chao, S. Tavassoli, A.K. Wong, V. Choudhary, B.P. Young, C.J. Loewen, and W.A. Prinz. 2014. A conserved endoplasmic reticulum membrane protein complex (EMC) facilitates phospholipid transfer from the ER to mitochondria. PLoS Biol. 12:e1001969. http://dx.doi.org/10.1371/journal.pbio.1001969
34. Listenberger, L.L., X. Han, S.E. Lewis, S. Cases, R.V. Farese Jr., D.S. Ory, and J.E. Schaffer. 2003. Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proc. Natl. Acad. Sci. USA. 100:3077-3082. http://dx.doi.org/10.1073/pnas.0630588100
35. Magré, J., M. Delépine, E. Khallouf, T. Gedde-Dahl Jr., L. Van Maldergem, E. Sobel, J. Papp, M. Meier, A. Mégarbané, A. Bachy, et al. BSCL Working Group. 2001. Identification of the gene altered in Berardinelli-Seip congenital lipodystrophy on chromosome 11q13. Nat. Genet. 28:365-370. http://dx.doi.org/10.1038/ng585
36. Martin, S., and R.G. Parton. 2006. Lipid droplets: a unified view of a dynamic organelle. Nat. Rev. Mol. Cell Biol. 7:373-378. http://dx.doi.org/10.1038/nrm1912
37. Miranda, D.A., J.H. Kim, L.N. Nguyen, W. Cheng, B.C. Tan, V.J. Goh, J.S. Tan, J. Yaligar, B.P. Kn, S.S. Velan, et al. 2014. Fat storage-inducing transmembrane protein 2 is required for normal fat storage in adipose tissue. J. Biol. Chem. 289:9560-9572. http://dx.doi.org/10.1074/jbc.M114.547687
38. Miyanari, Y., K. Atsuzawa, N. Usuda, K. Watashi, T. Hishiki, M. Zayas, R. Bartenschlager, T. Wakita, M. Hijikata, and K. Shimotohno. 2007. The lipid droplet is an important organelle for hepatitis C virus production. Nat. Cell Biol. 9:1089-1097. http://dx.doi.org/10.1038/ncb1631
39. Moir, R.D., D.A. Gross, D.L. Silver, and I.M. Willis. 2012. SCS3 and YFT2 link transcription of phospholipid biosynthetic genes to ER stress and the UPR. PLoS Genet. 8:e1002890. http://dx.doi.org/10.1371/journal.pgen.1002890
40. Murphy, D.J. 2001. The biogenesis and functions of lipid bodies in animals, plants and microorganisms. Prog. Lipid Res. 40:325-438. http://dx.doi.org/10.1016/S0163-7827(01)00013-3
41. Murphy, D.J., and J. Vance. 1999. Mechanisms of lipid-body formation. Trends Biochem. Sci. 24:109-115. http://dx.doi.org/10.1016/S0968-0004(98)01349-8
42. Ohsaki, Y., J. Cheng, M. Suzuki, Y. Shinohara, A. Fujita, and T. Fujimoto. 2009. Biogenesis of cytoplasmic lipid droplets: from the lipid ester globule in the membrane to the visible structure. Biochim. Biophys. Acta. 1791:399-407. http://dx.doi.org/10.1016/j.bbalip.2008.10.002
43. Ohsaki, Y., M. Suzuki, and T. Fujimoto. 2014. Open questions in lipid droplet biology. Chem. Biol. 21:86-96. http://dx.doi.org/10.1016/j.chembiol.2013.08.009
44. Olzmann, J.A., C.M. Richter, and R.R. Kopito. 2013. Spatial regulation of UBXD8 and p97/VCP controls ATGL-mediated lipid droplet turnover. Proc. Natl. Acad. Sci. USA. 110:1345-1350. http://dx.doi.org/10.1073/pnas.1213738110
45. Paix, A., Y. Wang, H.E. Smith, C.Y. Lee, D. Calidas, T. Lu, J. Smith, H. Schmidt, M.W. Krause, and G. Seydoux. 2014. Scalable and versatile genome editing using linear DNAs with microhomology to Cas9 Sites in Caenorhabditis elegans. Genetics. 198:1347-1356. http://dx.doi.org/10.1534/genetics.114.170423.
46. Parks, L.W., C.D. Bottema, R.J. Rodriguez, and T.A. Lewis. 1985. Yeast sterols: yeast mutants as tools for the study of sterol metabolism. Methods Enzymol. 111:333-346. http://dx.doi.org/10.1016/S0076-6879(85)11020-7
47. Ploegh, H.L. 2007. A lipid-based model for the creation of an escape hatch from the endoplasmic reticulum. Nature. 448:435-438. http://dx.doi.org/10.1038/nature06004
48. Pol, A., S.P. Gross, and R.G. Parton. 2014. Review: biogenesis of the multifunctional lipid droplet: lipids, proteins, and sites. J. Cell Biol. 204:635-646.
49. Prinz, W.A., L. Grzyb, M. Veenhuis, J.A. Kahana, P.A. Silver, and T.A. Rapoport. 2000. Mutants affecting the structure of the cortical endoplasmic reticulum in Saccharomyces cerevisiae. J. Cell Biol. 150:461-474. http://dx.doi.org/10.1083/jcb.150.3.461.
50. Robenek, H., I. Buers, O. Hofnagel, M.J. Robenek, D. Troyer, and N.J. Severs. 2009. Compartmentalization of proteins in lipid droplet biogenesis. Biochim. Biophys. Acta. 1791:408-418. http://dx.doi.org/10.1016/j.bbalip.2008.12.001
51. Sandager, L., M.H. Gustavsson, U. Ståhl, A. Dahlqvist, E. Wiberg, A. Banas, M. Lenman, H. Ronne, and S. Stymne. 2002. Storage lipid synthesis is non-essential in yeast. J. Biol. Chem. 277:6478-6482. http://dx.doi.org/10.1074/jbc.M109109200
52. Siniossoglou, S. 2013. Phospholipid metabolism and nuclear function: roles of the lipin family of phosphatidic acid phosphatases. Biochim. Biophys. Acta. 1831:575-581. http://dx.doi.org/10.1016/j.bbalip.2012.09.014
53. Skinner, J.R., T.M. Shew, D.M. Schwartz, A. Tzekov, C.M. Lepus, N.A. Abumrad, and N.E. Wolins. 2009. Diacylglycerol enrichment of endoplasmic reticulum or lipid droplets recruits perilipin 3/TIP47 during lipid storage and mobilization. J. Biol. Chem. 284:30941-30948. http://dx.doi.org/10.1074/jbc.M109.013995
54. Studer, D., B.M. Humbel, and M. Chiquet. 2008. Electron microscopy of high pressure frozen samples: bridging the gap between cellular ultrastructure and atomic resolution. Histochem. Cell Biol. 130:877-889. http://dx.doi.org/10.1007/s00418-008-0500-1
55. Szymanski, K.M., D. Binns, R. Bartz, N.V. Grishin, W.P. Li, A.K. Agarwal, A. Garg, R.G. Anderson, and J.M. Goodman. 2007. The lipodystrophy protein seipin is found at endoplasmic reticulum lipid droplet junctions and is important for droplet morphology. Proc. Natl. Acad. Sci. USA. 104:20890-20895. http://dx.doi.org/10.1073/pnas.0704154104
56. Unger, R.H., and P.E. Scherer. 2010. Gluttony, sloth and the metabolic syndrome: a roadmap to lipotoxicity. Trends Endocrinol. Metab. 21:345-352. http://dx.doi.org/10.1016/j.tem.2010.01.009
57. Vaden, D.L., V.M. Gohil, Z. Gu, and M.L. Greenberg. 2005. Separation of yeast phospholipids using one-dimensional thin-layer chromatography. Anal. Biochem. 338:162-164. http://dx.doi.org/10.1016/j.ab.2004.11.020
58. van Zutphen, T., V. Todde, R. de Boer, M. Kreim, H.F. Hofbauer, H. Wolinski, M. Veenhuis, I.J. van der Klei, and S.D. Kohlwein. 2014. Lipid droplet autophagy in the yeast Saccharomyces cerevisiae. Mol. Biol. Cell. 25:290-301. http://dx.doi.org/10.1091/mbc.E13-08-0448
59. Wältermann, M., A. Hinz, H. Robenek, D. Troyer, R. Reichelt, U. Malkus, H.J. Galla, R. Kalscheuer, T. Stöveken, P. von Landenberg, and A. Steinbüchel. 2005. Mechanism of lipid-body formation in prokaryotes: how bacteria fatten up. Mol. Microbiol. 55:750-763. http://dx.doi.org/10.1111/j.1365-2958.2004.04441.x
60. Walther, P., and A. Ziegler. 2002. Freeze substitution of high-pressure frozen samples: the visibility of biological membranes is improved when the substitution medium contains water. J. Microsc. 208:3-10. http://dx.doi.org/10.1046/j.1365-2818.2002.01064.x
61. Walther, T.C., and R.V. Farese Jr. 2009. The life of lipid droplets. Biochim. Biophys. Acta. 1791:459-466. http://dx.doi.org/10.1016/j.bbalip.2008.10.009
62. Wilfling, F., J.T. Haas, T.C. Walther, and R.V. Farese Jr. 2014. Lipid droplet biogenesis. Curr. Opin. Cell Biol. 29:39-45. http://dx.doi.org/10.1016/j.ceb.2014.03.008
63. Wolins, N.E., D.L. Brasaemle, and P.E. Bickel. 2006. A proposed model of fat packaging by exchangeable lipid droplet proteins. FEBS Lett. 580:5484-5491. http://dx.doi.org/10.1016/j.febslet.2006.08.040
64. Wright, R. 2000. Transmission electron microscopy of yeast. Microsc. Res. Tech. 51:496-510. http://dx.doi.org/10.1002/1097-0029(20001215)51:6<496::AID-JEMT2>3.0.CO;2-9
65. Yang, L., Y. Ding, Y. Chen, S. Zhang, C. Huo, Y. Wang, J. Yu, P. Zhang, H. Na, H. Zhang, et al. 2012. The proteomics of lipid droplets: structure, dynamics, and functions of the organelle conserved from bacteria to humans. J. Lipid Res. 53:1245-1253. http://dx.doi.org/10.1194/jlr.R024117
66. Zhang, J., S. Hashmi, F. Cheema, N. Al-Nasser, R. Bakheet, R.S. Parhar, F. Al-Mohanna, R. Gaugler, M.M. Hussain, and S. Hashmi. 2013. Regulation of lipoprotein assembly, secretion and fatty acid ß-oxidation by Krüppellike transcription factor, klf-3. J. Mol. Biol. 425:2641-2655. http://dx.doi.org/10.1016/j.jmb.2013.04.020
67. Zhou, M., H. Yu, X. Yin, P.M. Sabour, W. Chen, and J. Gong. 2014. Lactobacillus zeae protects Caenorhabditis elegans from enterotoxigenic Escherichia coli-caused death by inhibiting enterotoxin gene expression of the pathogen. PLoS One. 9:e89004. http://dx.doi.org/10.1371/journal.pone.0089004