Citation: | Yuwei Sun, Jian Heng, Feng Liu, Shuyan Zhang, Pingsheng Liu. Isolation and proteomic study of fish liver lipid droplets. Biophysics Reports, 2023, 9(3): 120-133. doi: 10.52601/bpr.2023.230004 |
Asaoka Y, Terai S, Sakaida I, Nishina H (2013) The expanding role of fish models in understanding non-alcoholic fatty liver disease. Dis Model Mech 6(4): 905−914
|
Bartz R, Zehmer JK, Zhu M, Chen Y, Serrero G, Zhao Y, Liu P (2007) Dynamic activity of lipid droplets: protein phosphorylation and GTP-mediated protein translocation. J Proteome Res 6(8): 3256−3265 doi: 10.1021/pr070158j
|
Beilstein F, Bouchoux J, Rousset M, Demignot S (2013) Proteomic analysis of lipid droplets from Caco-2/TC7 enterocytes identifies novel modulators of lipid secretion. PLoS One 8(1): e53017. https://doi.org/10.1371/journal.pone.0053017
|
Beller M, Riedel D, Jansch L, Dieterich G, Wehland J, Jackle H, Kuhnlein RP (2006) Characterization of the Drosophila lipid droplet subproteome. Mol Cell Proteomics 5(6): 1082−1094 doi: 10.1074/mcp.M600011-MCP200
|
Blanco AM, Unniappan S (2022) Goldfish (Carassius auratus): biology, husbandry, and research applications. In: Laboratory Fish in Biomedical Research (Eds: Angelo and Livia D'Angelo, Paolo de Girolamo) Academic Press: 373-408. https://doi.org/10.1016/B978-0-12-821099-4.00012-2
|
Bouchoux J, Beilstein F, Pauquai T, Guerrera IC, Chateau D, Ly N, Alqub M, Klein C, Chambaz J, Rousset M, Lacorte JM, Morel E, Demignot S (2011) The proteome of cytosolic lipid droplets isolated from differentiated Caco-2/TC7 enterocytes reveals cell-specific characteristics. Biol Cell 103(11): 499−517 doi: 10.1042/BC20110024
|
Brasaemle DL, Dolios G, Shapiro L, Wang R (2004) Proteomic analysis of proteins associated with lipid droplets of basal and lipolytically stimulated 3T3-L1 adipocytes. J Biol Chem 279(45): 46835−46842 doi: 10.1074/jbc.M409340200
|
Bulankina AV, Deggerich A, Wenzel D, Mutenda K, Wittmann JG, Rudolph MG, Burger KN, Honing S (2009) TIP47 functions in the biogenesis of lipid droplets. J Cell Biol 185(4): 641−655 doi: 10.1083/jcb.200812042
|
Cermelli S, Guo Y, Gross SP, Welte MA (2006) The lipid-droplet proteome reveals that droplets are a protein-storage depot. Curr Biol 16(18): 1783−1795 doi: 10.1016/j.cub.2006.07.062
|
Chen B, Zheng YM, Zhang JP (2018) Comparative study of different diets-induced NAFLD models of zebrafish. Front Endocrinol (Lausanne) 9: 366. https://doi.org/10.3389/fendo.2018.00366
|
Crunk AE, Monks J, Murakami A, Jackman M, Maclean PS, Ladinsky M, Bales ES, Cain S, Orlicky DJ, McManaman JL (2013) Dynamic regulation of hepatic lipid droplet properties by diet. PLoS One 8(7): e67631. https://doi.org/10.1371/journal.pone.0067631
|
D'Aquila T, Sirohi D, Grabowski JM, Hedrick VE, Paul LN, Greenberg AS, Kuhn RJ, Buhman KK (2015) Characterization of the proteome of cytoplasmic lipid droplets in mouse enterocytes after a dietary fat challenge. PLoS One 10(5): e0126823. https://doi.org/10.1371/journal.pone.0126823
|
Ding Y, Wu Y, Zeng R, Liao K (2012a) Proteomic profiling of lipid droplet-associated proteins in primary adipocytes of normal and obese mouse. Acta Biochim Biophys Sin (Shanghai) 44(5): 394−406 doi: 10.1093/abbs/gms008
|
Ding Y, Yang L, Zhang S, Wang Y, Du Y, Pu J, Peng G, Chen Y, Zhang H, Yu J, Hang H, Wu P, Yang F, Yang H, Steinbuchel A, Liu P (2012b) Identification of the major functional proteins of prokaryotic lipid droplets. J Lipid Res 53(3): 399−411 doi: 10.1194/jlr.M021899
|
Ding Y, Zhang S, Yang L, Na H, Zhang P, Zhang H, Wang Y, Chen Y, Yu J, Huo C, Xu S, Garaiova M, Cong Y, Liu P (2013) Isolating lipid droplets from multiple species. Nat Protoc 8(1): 43−51 doi: 10.1038/nprot.2012.142
|
Ducharme NA, Bickel PE (2008) Lipid droplets in lipogenesis and lipolysis. Endocrinology 149(3): 942−949 doi: 10.1210/en.2007-1713
|
Eichmann TO, Grumet L, Taschler U, Hartler J, Heier C, Woblistin A, Pajed L, Kollroser M, Rechberger G, Thallinger GG, Zechner R, Haemmerle G, Zimmermann R, Lass A (2015) ATGL and CGI-58 are lipid droplet proteins of the hepatic stellate cell line HSC-T6. J Lipid Res 56(10): 1972−1984 doi: 10.1194/jlr.M062372
|
Farese RV Jr., Walther TC (2009) Lipid droplets finally get a little R-E-S-P-E-C-T. Cell 139(5): 855−860 doi: 10.1016/j.cell.2009.11.005
|
Fujimoto T, Ohsaki Y, Cheng J, Suzuki M, Shinohara Y (2008) Lipid droplets: a classic organelle with new outfits. Histochem Cell Biol 130(2): 263−279 doi: 10.1007/s00418-008-0449-0
|
Fujimoto T, Parton RG (2011) Not just fat: the structure and function of the lipid droplet. Cold Spring Harb Perspect Biol 3(3): a004838. https://doi.org/10.1101/cshperspect.a004838
|
Fujimoto Y, Itabe H, Sakai J, Makita M, Noda J, Mori M, Higashi Y, Kojima S, Takano T (2004) Identification of major proteins in the lipid droplet-enriched fraction isolated from the human hepatocyte cell line HuH7. Biochim Biophys Acta 1644(1): 47−59 doi: 10.1016/j.bbamcr.2003.10.018
|
Goessling W, Sadler KC (2015) Zebrafish: an important tool for liver disease research. Gastroenterology 149(6): 1361−1377 doi: 10.1053/j.gastro.2015.08.034
|
Goodman JM (2008) The gregarious lipid droplet. J Biol Chem 283(42): 28005−28009 doi: 10.1074/jbc.R800042200
|
Goodman JM (2009) Demonstrated and inferred metabolism associated with cytosolic lipid droplets. J Lipid Res Nov 50(11): 2148−2156 doi: 10.1194/jlr.R001446
|
Grillitsch K, Connerth M, Kofeler H, Arrey TN, Rietschel B, Wagner B, Karas M, Daum G (2011) Lipid particles/droplets of the yeast Saccharomyces cerevisiae revisited: lipidome meets proteome. Biochim Biophys Acta 1811(12): 1165−1176 doi: 10.1016/j.bbalip.2011.07.015
|
Harris CA, Haas JT, Streeper RS, Stone SJ, Kumari M, Kui K, Han X, Brownell N, Gross RW, Zechner R, Farese RV Jr (2011) DGAT enzymes are required for triacylglycerol synthesis and lipid droplets in adipocytes. J Lipid Res 52(4): 657−667 doi: 10.1194/jlr.M013003
|
Jagerstrom S, Polesie S, Wickstrom Y, Johansson BR, Schroder HD, Hojlund K, Bostrom P (2009) Lipid droplets interact with mitochondria using SNAP23. Cell Biol Int 33(9): 934−940 doi: 10.1016/j.cellbi.2009.06.011
|
Kei AA, Filippatos TD, Tsimihodimos V, Elisaf MS (2012) A review of the role of apolipoprotein C-II in lipoprotein metabolism and cardiovascular disease. Metabolism 61(7): 906−921 doi: 10.1016/j.metabol.2011.12.002
|
Khor VK, Ahrends R, Lin Y, Shen WJ, Adams CM, Roseman AN, Cortez Y, Teruel MN, Azhar S, Kraemer FB (2014) The proteome of cholesteryl-ester-enriched versus triacylglycerol-enriched lipid droplets. PLoS One 9(8): e105047. https://doi.org/10.1371/journal.pone.0105047
|
Kim SC, Chen Y, Mirza S, Xu Y, Lee J, Liu P, Zhao Y (2006) A clean, more efficient method for in-solution digestion of protein mixtures without detergent or urea. J Proteome Res 5(12): 3446−3452 doi: 10.1021/pr0603396
|
Krahmer N, Farese RV Jr., Walther TC (2013a) Balancing the fat: lipid droplets and human disease. EMBO Mol Med 5(7): 973−983 doi: 10.1002/emmm.201100671
|
Krahmer N, Hilger M, Kory N, Wilfling F, Stoehr G, Mann M, Farese RV Jr., Walther TC (2013b) Protein correlation profiles identify lipid droplet proteins with high confidence. Mol Cell Proteomics 12(5): 1115−1126 doi: 10.1074/mcp.M112.020230
|
Liu P, Ying Y, Zhao Y, Mundy DI, Zhu M, Anderson RGW (2004) Chinese hamster ovary K2 cell lipid droplets appear to be metabolic organelles involved in membrane traffic. J Biol Chem 279(5): 3787−3792 doi: 10.1074/jbc.M311945200
|
Maeda K, Cao H, Kono K, Gorgun CZ, Furuhashi M, Uysal KT, Cao Q, Atsumi G, Malone H, Krishnan B, Minokoshi Y, Kahn BB, Parker RA, Hotamisligil GS (2005) Adipocyte/macrophage fatty acid binding proteins control integrated metabolic responses in obesity and diabetes. Cell Metab 1(2): 107−119 doi: 10.1016/j.cmet.2004.12.008
|
Mahmood F, Xu R, Awan MUN, Song Y, Han Q, Xia X, Zhang J (2021) PDIA3: structure, functions and its potential role in viral infections. Biomed Pharmacother 143: 112110. https://doi.org/10.1016/j.biopha.2021.112110
|
Martin S, Parton RG (2006) Lipid droplets: a unified view of a dynamic organelle. Nat Rev Mol Cell Biol 7(5): 373−378 doi: 10.1038/nrm1912
|
Mensah ET, Blanco AM, Donini A, Unniappan S (2018) Galanin decreases spontaneous resting contractions and potentiates acetyl choline-induced contractions of goldfish gut. Neuropeptides 69: 92−97 doi: 10.1016/j.npep.2018.04.010
|
Misselbeck K, Parolo S, Lorenzini F, Savoca V, Leonardelli L, Bora P, Morine MJ, Mione MC, Domenici E, Priami C (2019) A network-based approach to identify deregulated pathways and drug effects in metabolic syndrome. Nat Commun 10(1): 5215. https://doi.org/10.1038/s41467-019-13208-z
|
Murphy DJ (2001) The biogenesis and functions of lipid bodies in animals, plants and microorganisms. Prog Lipid Res 40(5): 325−438 doi: 10.1016/S0163-7827(01)00013-3
|
Murphy DJ (2012) The dynamic roles of intracellular lipid droplets: from archaea to mammals. Protoplasma 249(3): 541−585 doi: 10.1007/s00709-011-0329-7
|
Murphy S, Martin S, Parton RG (2009) Lipid droplet-organelle interactions; sharing the fats. Biochim Biophys Acta 1791(6): 441−447 doi: 10.1016/j.bbalip.2008.07.004
|
Na H, Zhang P, Chen Y, Zhu X, Liu Y, Liu Y, Xie K, Xu N, Yang F, Yu Y, Cichello S, Mak HY, Wang MC, Zhang H, Liu P (2015) Identification of lipid droplet structure-like/resident proteins in Caenorhabditis elegans. Biochim Biophys Acta 1853(10 Pt A): 2481-2491
|
Nakayama H, Hata K, Matsuoka I, Zang L, Kim Y, Chu D, Juneja LR, Nishimura N, Shimada Y (2020) Anti-obesity natural products tested in juvenile zebrafish obesogenic tests and mouse 3T3-L1 adipogenesis assays. Molecules 25(24): 5840. https://doi.org/10.3390/molecules25245840
|
Nakayama H, Shimada Y, Zang L, Terasawa M, Nishiura K, Matsuda K, Toombs C, Langdon C, Nishimura N (2018) Novel anti-obesity properties of palmaria mollis in zebrafish and mouse models. Nutrients 10(10): 1401. https://doi.org/10.3390/nu10101401
|
Ohsaki Y, Cheng J, Suzuki M, Fujita A, Fujimoto T (2008) Lipid droplets are arrested in the ER membrane by tight binding of lipidated apolipoprotein B-100. J Cell Sci 121(Pt 14): 2415-2422
|
Ozeki S, Cheng J, Tauchi-Sato K, Hatano N, Taniguchi H, Fujimoto T (2005) Rab18 localizes to lipid droplets and induces their close apposition to the endoplasmic reticulum-derived membrane. J Cell Sci 118(Pt 12): 2601-2611
|
Park JY, Seong JK, Paik YK (2004) Proteomic analysis of diet-induced hypercholesterolemic mice. Proteomics 4(2): 514−523 doi: 10.1002/pmic.200300623
|
Pereira HA, Leite Ade L, Charone S, Lobo JG, Cestari TM, Peres-Buzalaf C, Buzalaf MA (2013) Proteomic analysis of liver in rats chronically exposed to fluoride. PLoS One 8(9): e75343. https://doi.org/10.1371/journal.pone.0075343
|
Ribas L, Piferrer F (2014) The zebrafish (Danio rerio) as a model organism, with emphasis on applications for finfish aquaculture research. Rev Aquac 6(4): 209−240 doi: 10.1111/raq.12041
|
Rowe ER, Mimmack ML, Barbosa AD, Haider A, Isaac I, Ouberai MM, Thiam AR, Patel S, Saudek V, Siniossoglou S, Savage DB (2016) Conserved amphipathic helices mediate lipid droplet targeting of perilipins 1-3. J Biol Chem 291(13): 6664−6678 doi: 10.1074/jbc.M115.691048
|
Saka HA, Thompson JW, Chen YS, Dubois LG, Haas JT, Moseley A, Valdivia RH (2015) Chlamydia trachomatis infection leads to defined alterations to the lipid droplet proteome in epithelial cells. PLoS One 10(4): e0124630. https://doi.org/10.1371/journal.pone.0124630
|
Sato S, Fukasawa M, Yamakawa Y, Natsume T, Suzuki T, Shoji I, Aizaki H, Miyamura T, Nishijima M (2006) Proteomic profiling of lipid droplet proteins in hepatoma cell lines expressing hepatitis C virus core protein. J Biochem 139(5): 921−930 doi: 10.1093/jb/mvj104
|
Shi J, Feng H, Lee J, Ning Chen W (2013) Comparative proteomics profile of lipid-cumulating oleaginous yeast: an iTRAQ-coupled 2-D LC-MS/MS analysis. PLoS One 8(12): e85532. https://doi.org/10.1371/journal.pone.0085532
|
Su W, Wang Y, Jia X, Wu W, Li L, Tian X, Li S, Wang C, Xu H, Cao J, Han Q, Xu S, Chen Y, Zhong Y, Zhang X, Liu P, Gustafsson JA, Guan Y (2014) Comparative proteomic study reveals 17beta-HSD13 as a pathogenic protein in nonalcoholic fatty liver disease. Proc Natl Acad Sci USA 111(31): 11437−11442 doi: 10.1073/pnas.1410741111
|
Sztalryd C, Brasaemle DL (2017) The perilipin family of lipid droplet proteins: gatekeepers of intracellular lipolysis. Biochim Biophys Acta Mol Cell Biol Lipids 1862(10 Pt B): 1221-1232
|
Teame T, Zhang Z, Ran C, Zhang H, Yang Y, Ding Q, Xie M, Gao C, Ye Y, Duan M, Zhou Z (2019) The use of zebrafish (Danio rerio) as biomedical models. Anim Front 9(3): 68−77 doi: 10.1093/af/vfz020
|
Thiam AR, Farese RV Jr, Walther TC (2013) The biophysics and cell biology of lipid droplets. Nat Rev Mol Cell Biol 14(12): 775−786 doi: 10.1038/nrm3699
|
Tian JJ, Zhang JM, Yu EM, Sun JH, Xia Y, Zhang K, Li ZF, Gong WB, Wang GJ, Xie J (2020) Identification and analysis of lipid droplet-related proteome in the adipose tissue of grass carp (Ctenopharyngodon idella) under fed and starved conditions. Comp Biochem Physiol Part D Genomics Proteomics 36: 100710. https://doi.org/10.1016/j.cbd.2020.100710
|
Turro S, Ingelmo-Torres M, Estanyol JM, Tebar F, Fernandez MA, Albor CV, Gaus K, Grewal T, Enrich C, Pol A (2006) Identification and characterization of associated with lipid droplet protein 1: A novel membrane-associated protein that resides on hepatic lipid droplets. Traffic 7(9): 1254−1269 doi: 10.1111/j.1600-0854.2006.00465.x
|
Umlauf E, Csaszar E, Moertelmaier M, Schuetz GJ, Parton RG, Prohaska R (2004) Association of stomatin with lipid bodies. J Biol Chem 279(22): 23699−23709 doi: 10.1074/jbc.M310546200
|
Vrablik TL, Petyuk VA, Larson EM, Smith RD, Watts JL (2015) Lipidomic and proteomic analysis of Caenorhabditis elegans lipid droplets and identification of ACS-4 as a lipid droplet-associated protein. Biochim Biophys Acta 1851(10): 1337−1345 doi: 10.1016/j.bbalip.2015.06.004
|
Walther TC, Farese RV Jr. (2012) Lipid droplets and cellular lipid metabolism. Annu Rev Biochem 81: 687−714 doi: 10.1146/annurev-biochem-061009-102430
|
Welte MA, Gross SP, Postner M, Block SM, Wieschaus EF (1998) Developmental regulation of vesicle transport in Drosophila embryos: forces and kinetics. Cell 92(4): 547−557 doi: 10.1016/S0092-8674(00)80947-2
|
Westerterp M, Berbee JF, Delsing DJ, Jong MC, Gijbels MJ, Dahlmans VE, Offerman EH, Romijn JA, Havekes LM, Rensen PC (2007) Apolipoprotein C-I binds free fatty acids and reduces their intracellular esterification. J Lipid Res 48(6): 1353−1361 doi: 10.1194/jlr.M700024-JLR200
|
Wu BX, Chen Y, Chen Y, Fan J, Rohrer B, Crouch RK, Ma JX (2002) Cloning and characterization of a novel all-trans retinol short-chain dehydrogenase/reductase from the RPE. Invest Ophthalmol Vis Sci 43(11): 3365−3372
|
Xu S, Zhang X, Liu P (2018) Lipid droplet proteins and metabolic diseases. Biochim Biophys Acta Mol Basis Dis 1864(5 Pt B): 1968-1983
|
Yang L, Ding Y, Chen Y, Zhang S, Huo C, Wang Y, Yu J, Zhang P, Na H, Zhang H, Ma Y, Liu P (2012) The proteomics of lipid droplets: structure, dynamics, and functions of the organelle conserved from bacteria to humans. J Lipid Res 53(7): 1245−1253 doi: 10.1194/jlr.R024117
|
Yu J, Zhang S, Cui L, Wang W, Na H, Zhu X, Li L, Xu G, Yang F, Christian M, Liu P (2015) Lipid droplet remodeling and interaction with mitochondria in mouse brown adipose tissue during cold treatment. Biochim Biophys Acta 1853(5): 918−928 doi: 10.1016/j.bbamcr.2015.01.020
|
Yu W, Bozza PT, Tzizik DM, Gray JP, Cassara J, Dvorak AM, Weller PF (1998) Co-compartmentalization of MAP kinases and cytosolic phospholipase A2 at cytoplasmic arachidonate-rich lipid bodies. Am J Pathol 152(3): 759−769
|
Yu W, Cassara J, Weller PF (2000) Phosphatidylinositide 3-kinase localizes to cytoplasmic lipid bodies in human polymorphonuclear leukocytes and other myeloid-derived cells. Blood 95(3): 1078−1085 doi: 10.1182/blood.V95.3.1078.003k16_1078_1085
|
Zehmer JK, Huang Y, Peng G, Pu J, Anderson RG, Liu P (2009) A role for lipid droplets in inter-membrane lipid traffic. Proteomics 9(4): 914−921 doi: 10.1002/pmic.200800584
|
Zhang C, Liu P (2017) The lipid droplet: A conserved cellular organelle. Protein Cell 8(11): 796−800 doi: 10.1007/s13238-017-0467-6
|
Zhang C, Liu P (2019) The new face of the lipid droplet: lipid droplet proteins. Proteomics 19(10): e1700223. https://doi.org/10.1002/pmic.201700223
|
Zhang H, Wang Y, Li J, Yu J, Pu J, Li L, Zhang H, Zhang S, Peng G, Yang F, Liu P (2011) Proteome of skeletal muscle lipid droplet reveals association with mitochondria and apolipoprotein a-I. J Proteome Res 10(10): 4757−4768 doi: 10.1021/pr200553c
|
Zhang P, Na H, Liu Z, Zhang S, Xue P, Chen Y, Pu J, Peng G, Huang X, Yang F, Xie Z, Xu T, Xu P, Ou G, Zhang SO, Liu P (2012) Proteomic study and marker protein identification of Caenorhabditis elegans lipid droplets. Mol Cell Proteomics 11(8): 317−328 doi: 10.1074/mcp.M111.016345
|
Zhang S Du Y, Wang Y, Liu P (2010) Lipid droplet—a cellular organelle for lipid metabolism. Acta Biophys Sin 26(2): 97−105
|
Zhou X, Liao WJ, Liao JM, Liao P, Lu H (2015) Ribosomal proteins: functions beyond the ribosome. J Mol Cell Biol 7(2): 92−104 doi: 10.1093/jmcb/mjv014
|
Zimmermann R, Strauss JG, Haemmerle G, Schoiswohl G, Birner-Gruenberger R, Riederer M, Lass A, Neuberger G, Eisenhaber F, Hermetter A, Zechner R (2004) Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase. Science 306(5700): 1383−1386 doi: 10.1126/science.1100747
|
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