Seipin is required for converting nascent to mature lipid droplets

eLife

Volumn 5, Issue AUGUST, 2016, Pages

  Wang, Huajin ^a,b,c   Becuwe, Michel ^b,c   Housden, Benjamin E ^c   Chitraju, Chandramohan ^b,c   Porras, Ashley J ^b,c   Graham, Morven M ^d   Liu, Xinran N ^d   Thiam, Abdou Rachid ^e   Savage, David B ^f   Agarwal, Anil K ^g   Garg, Abhimanyu ^g   Olarte, Maria Jesus ^b,c   Lin, Qingqing ^b,c   Frohlich, Florian ^b,c,h   Hannibal Bach, Hans Kristian ⁱ   Upadhyayula, Srigokul ^c,j   Perrimon, Norbert ^c,k   Kirchhausen, Tomas ^c,j   Ejsing, Christer S ⁱ   Walther, Tobias C ^b,c,k,l   Farese, Robert V ^b,c,l   more..

^a CARNEGIE MELLON UNIVERSITY   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e ECOLE NORMALE SUPÉRIEURE   (France)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^g UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^h UNIVERSITY OF OSNABRÜCK   (Germany)

ⁱ UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^j BOSTON CHILDREN S HOSPITAL   (United States)

^k HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^l BROAD INSTITUTE OF MIT AND HARVARD   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

FAT DROPLET; MEMBRANE PROTEIN; SEIPIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL FRACTIONATION; CONTROLLED STUDY; DROSOPHILA; ELECTRON TOMOGRAPHY; ENDOPLASMIC RETICULUM; FLUORESCENCE; GENE SEQUENCE; HUMAN; HUMAN CELL; IMAGE PROCESSING; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; LIPID ANALYSIS; LIPID METABOLISM; LIPIDOMICS; MICROSCOPY; MOLECULAR BIOLOGY; NONHUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; REAL TIME POLYMERASE CHAIN REACTION; TRANSMISSION ELECTRON MICROSCOPY;

EID: 84988807217     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.16582     Document Type: Article

References (45)

1. Agarwal AK, Garg A. 2004. Seipin: a mysterious protein. Trends in Molecular Medicine 10:440-444. doi: 10.1016/j.molmed.2004.07.009
2. Agarwal AK, Simha V, Oral EA, Moran SA, Gorden P, O’Rahilly S, Zaidi Z, Gurakan F, Arslanian SA, Klar A, Ricker A, White NH, Bindl L, Herbst K, Kennel K, Patel SB, Al-Gazali L, Garg A. 2003. Phenotypic and genetic heterogeneity in congenital generalized lipodystrophy. The Journal of Clinical Endocrinology & Metabolism 88: 4840-4847. doi: 10.1210/jc.2003-030855
3. Almeida R, Pauling JK, Sokol E, Hannibal-Bach HK, Ejsing CS. 2015. Comprehensive lipidome analysis by shotgun lipidomics on a hybrid quadrupole-orbitrap-linear ion trap mass spectrometer. Journal of the American Society for Mass Spectrometry 26:133-148. doi: 10.1007/s13361-014-1013-x
4. Bi J, Wang W, Liu Z, Huang X, Jiang Q, Liu G, Wang Y, Huang X. 2014. Seipin promotes adipose tissue fat storage through the ER Ca2+-ATPase SERCA. Cell Metabolism 19:861-871. doi: 10.1016/j.cmet.2014.03.028
5. Binns D, Lee S, Hilton CL, Jiang QX, Goodman JM. 2010. Seipin is a discrete homooligomer. Biochemistry 49: 10747-10755. doi: 10.1021/bi1013003
6. Boutet E, El Mourabit H, Prot M, Nemani M, Khallouf E, Colard O, Maurice M, Durand-Schneider AM, Chrétien Y, Grès S, Wolf C, Saulnier-Blache JS, Capeau J, Magré J. 2009. Seipin deficiency alters fatty acid Delta9 desaturation and lipid droplet formation in Berardinelli-Seip congenital lipodystrophy. Biochimie 91:796-803. doi: 10.1016/j.biochi.2009.01.011
7. Cartwright BR, Binns DD, Hilton CL, Han S, Gao Q, Goodman JM. 2015. Seipin performs dissectible functions in promoting lipid droplet biogenesis and regulating droplet morphology. Molecular Biology of the Cell 26:726-739. doi: 10.1091/mbc.E14-08-1303
8. Cartwright BR, Goodman JM. 2012. Seipin: from human disease to molecular mechanism. The Journal of Lipid Research 53:1042-1055. doi: 10.1194/jlr.R023754
9. Chen B-C, Legant WR, Wang K, Shao L, Milkie DE, Davidson MW, Janetopoulos C, Wu XS, Hammer JA, Liu Z, English BP, Mimori-Kiyosue Y, Romero DP, Ritter AT, Lippincott-Schwartz J, Fritz-Laylin L, Mullins RD, Mitchell DM, Bembenek JN, Reymann A-C, et al. 2014. Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution. Science 346:1257998. doi: 10.1126/science.1257998
10. Dayel MJ, Hom EF, Verkman AS. 1999. Diffusion of green fluorescent protein in the aqueous-phase lumen of endoplasmic reticulum. Biophysical Journal 76:2843-2851. doi: 10.1016/S0006-3495(99)77438-2
11. Ejsing CS, Sampaio JL, Surendranath V, Duchoslav E, Ekroos K, Klemm RW, Simons K, Shevchenko A. 2009. Global analysis of the yeast lipidome by quantitative shotgun mass spectrometry. PNAS 106:2136-2141. doi: 10.1073/pnas.0811700106
12. Fei W, Du X, Yang H. 2011a. Seipin, adipogenesis and lipid droplets. Trends in Endocrinology and Metabolism 22:204-210. doi: 10.1016/j.tem.2011.02.004
13. Fei W, Li H, Shui G, Kapterian TS, Bielby C, Du X, Brown AJ, Li P, Wenk MR, Liu P, Yang H. 2011b. Molecular characterization of seipin and its mutants: implications for seipin in triacylglycerol synthesis. The Journal of Lipid Research 52:2136-2147. doi: 10.1194/jlr.M017566
14. Fei W, Shui G, Gaeta B, Du X, Kuerschner L, Li P, Brown AJ, Wenk MR, Parton RG, Yang H. 2008. Fld1p, a functional homologue of human seipin, regulates the size of lipid droplets in yeast. The Journal of Cell Biology 180:473-482. doi: 10.1083/jcb.200711136
15. Fei W, Shui G, Zhang Y, Krahmer N, Ferguson C, Kapterian TS, Lin RC, Dawes IW, Brown AJ, Li P, Huang X, Parton RG, Wenk MR, Walther TC, Yang H. 2011c. A role for phosphatidic acid in the formation of “supersized” lipid droplets. PLoS Genetics 7:e1002201. doi: 10.1371/journal.pgen.1002201
16. Folch J, Lees M, Sloane Stanley GH. 1957. A simple method for the isolation and purification of total lipides from animal tissues. The Journal of Biological Chemistry 226:497-509.
17. Grippa A, Buxó L, Mora G, Funaya C, Idrissi FZ, Mancuso F, Gomez R, Muntanyà J, Sabidó E, Carvalho P. 2015. The seipin complex Fld1/Ldb16 stabilizes ER-lipid droplet contact sites. The Journal of Cell Biology 211:829-844. doi: 10.1083/jcb.201502070
18. Gross DA, Silver DL. 2014. Cytosolic lipid droplets: from mechanisms of fat storage to disease. Critical Reviews in Biochemistry and Molecular Biology 49:304-326. doi: 10.3109/10409238.2014.931337
19. Hashemi HF, Goodman JM. 2015. The life cycle of lipid droplets. Current Opinion in Cell Biology 33:119-124. doi: 10.1016/j.ceb.2015.02.002
20. Horchani H, de Saint-Jean M, Barelli H, Antonny B. 2014. Interaction of the Spo20 membrane-sensor motif with phosphatidic acid and other anionic lipids, and influence of the membrane environment. PLoS ONE 9:e113484. doi: 10.1371/journal.pone.0113484
21. Housden BE, Lin S, Perrimon N. 2014. Cas9-based genome editing in Drosophila. Methods in Enzymology 546: 415-439. doi: 10.1016/B978-0-12-801185-0.00019-2
22. Housden BE, Valvezan AJ, Kelley C, Sopko R, Hu Y, Roesel C, Lin S, Buckner M, Tao R, Yilmazel B, Mohr SE, Manning BD, Perrimon N. 2015. Identification of potential drug targets for tuberous sclerosis complex by synthetic screens combining CRISPR-based knockouts with RNAi. Science Signaling 8:rs9. doi: 10.1126/scisignal.aab3729
23. Kory N, Thiam AR, Farese RV, Walther TC. 2015. Protein crowding Is a determinant of lipid droplet protein composition. Developmental Cell 34:351-363. doi: 10.1016/j.devcel.2015.06.007
24. Krahmer N, Guo Y, Wilfling F, Hilger M, Lingrell S, Heger K, Newman HW, Schmidt-Supprian M, Vance DE, Mann M, Farese RV, Walther TC. 2011. Phosphatidylcholine synthesis for lipid droplet expansion is mediated by localized activation of CTP:phosphocholine cytidylyltransferase. Cell Metabolism 14:504-515. doi: 10.1016/j.cmet.2011.07.013
25. Lu M, Tay LW, He J, Du G. 2016. Monitoring Phosphatidic Acid Signaling in Breast Cancer Cells Using Genetically Encoded Biosensors. Methods in Molecular Biology 1406:225-237. doi: 10.1007/978-1-4939-3444-7_20
26. Lundin C, Nordstrom R, Wagner K, Windpassinger C, Andersson H, von Heijne G, Nilsson I. 2006. Membrane topology of the human seipin protein. FEBS Letters 580:2281-2284. doi: 10.1016/j.febslet.2006.03.040
27. Magré J, Delépine M, Khallouf E, Gedde-Dahl T, Van Maldergem L, Sobel E, Papp J, Meier M, Mégarbané A, Bachy A, Verloes A, d’Abronzo FH, Seemanova E, Assan R, Baudic N, Bourut C, Czernichow P, Huet F, Grigorescu F, de Kerdanet M, et al. 2001. Identification of the gene altered in Berardinelli-Seip congenital lipodystrophy on chromosome 11q13. Nature Genetics 28:365-370. doi: 10.1038/ng585
28. Mastronarde DN. 2008. Correction for non-perpendicularity of beam and tilt axis in tomographic reconstructions with the IMOD package. Journal of Microscopy 230:212-217. doi: 10.1111/j.1365-2818.2008.01977.x
29. Pol A, Gross SP, Parton RG. 2014. Review: biogenesis of the multifunctional lipid droplet: lipids, proteins, and sites. The Journal of Cell Biology 204:635-646. doi: 10.1083/jcb.201311051
30. Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F. 2013. Genome engineering using the CRISPR-Cas9 system. Nature Protocols 8:2281-2308. doi: 10.1038/nprot.2013.143
31. Sim MF, Dennis RJ, Aubry EM, Ramanathan N, Sembongi H, Saudek V, Ito D, O’Rahilly S, Siniossoglou S, Rochford JJ. 2012. The human lipodystrophy protein seipin is an ER membrane adaptor for the adipogenic PA phosphatase lipin 1. Molecular Metabolism 2:38-46. doi: 10.1016/j.molmet.2012.11.002
32. Sim MF, Talukder MM, Dennis RJ, O’Rahilly S, Edwardson JM, Rochford JJ. 2013. Analysis of naturally occurring mutations in the human lipodystrophy protein seipin reveals multiple potential pathogenic mechanisms. Diabetologia 56:2498-2506. doi: 10.1007/s00125-013-3029-3
33. Szymanski KM, Binns D, Bartz R, Grishin NV, Li W-P, Agarwal AK, Garg A, Anderson RGW, Goodman JM. 2007. The lipodystrophy protein seipin is found at endoplasmic reticulum lipid droplet junctions and is important for droplet morphology. PNAS 104:20890-20895. doi: 10.1073/pnas.0704154104
34. Thiam AR, Antonny B, Wang J, Delacotte J, Wilfling F, Walther TC, Beck R, Rothman JE, Pincet F. 2013a. COPI buds 60-nm lipid droplets from reconstituted water-phospholipid-triacylglyceride interfaces, suggesting a tension clamp function. PNAS 110:13244-13249. doi: 10.1073/pnas.1307685110
35. Thiam AR, Bremond N, Bibette J. 2012. From stability to permeability of adhesive emulsion bilayers. Langmuir 28:6291-6298. doi: 10.1021/la3003349
36. Thiam AR, Farese RV Jr, Walther TC. 2013b. The biophysics and cell biology of lipid droplets. Nature Reviews Molecular Cell Biology 14:775-786. doi: 10.1038/nrm3699
37. Tian Y, Bi J, Shui G, Liu Z, Xiang Y, Liu Y, Wenk MR, Yang H, Huang X. 2011. Tissue-autonomous function of Drosophila seipin in preventing ectopic lipid droplet formation. PLoS Genetics 7:e1001364. doi: 10.1371/journal.pgen.1001364
38. Walther TC, Farese RV. 2012. Lipid droplets and cellular lipid metabolism. Annual Review of Biochemistry 81: 687-714. doi: 10.1146/annurev-biochem-061009-102430
39. Wang CW, Miao YH, Chang YS. 2014. Control of lipid droplet size in budding yeast requires the collaboration between Fld1 and Ldb16. Journal of Cell Science 127:1214-1228. doi: 10.1242/jcs.137737
40. Welte MA. 2015. Expanding roles for lipid droplets. Current Biology 25:R470-481. doi: 10.1016/j.cub.2015.04.004
41. Wilfling F, Haas JT, Walther TC, Farese RV. 2014. Lipid droplet biogenesis. Current Opinion in Cell Biology 29: 39-45. doi: 10.1016/j.ceb.2014.03.008
42. Wilfling F, Thiam AR, Olarte MJ, Wang J, Beck R, Gould TJ, Allgeyer ES, Pincet F, Bewersdorf J, Farese RV, Walther TC. 2014b. Arf1/COPI machinery acts directly on lipid droplets and enables their connection to the ER for protein targeting. eLife 3:e01607. doi: 10.7554/eLife.01607
43. Wilfling F, Wang H, Haas JT, Krahmer N, Gould TJ, Uchida A, Cheng JX, Graham M, Christiano R, Frohlich F, Liu X, Buhman KK, Coleman RA, Bewersdorf J, Farese RV, Walther TC. 2013. Triacylglycerol synthesis enzymes mediate lipid droplet growth by relocalizing from the ER to lipid droplets. Developmental Cell 24:384-399. doi: 10.1016/j.devcel.2013.01.013
44. Wolinski H, Hofbauer HF, Hellauer K, Cristobal-Sarramian A, Kolb D, Radulovic M, Knittelfelder OL, Rechberger GN, Kohlwein SD. 2015. Seipin is involved in the regulation of phosphatidic acid metabolism at a subdomain of the nuclear envelope in yeast. Biochimica Et Biophysica Acta 1851:1450-1464. doi: 10.1016/j.bbalip.2015.08.003
45. Yen CL, Stone SJ, Koliwad S, Harris C, Farese RV. 2008. Thematic review series: glycerolipids. DGAT enzymes and triacylglycerol biosynthesis. The Journal of Lipid Research 49:2283-2301. doi: 10.1194/jlr.R800018-JLR200