Perilipin 2 and lipid droplets provide reciprocal stabilization

Biophysics Reports - Tập 5 Số 3 - Trang 145-160 - 2019
Shimeng Xu1, Fei Zou2, Zhiqing Diao3, Shuyan Zhang1, Yaqin Deng1, Xiaotong Zhu1, Liujuan Cui1, Jinhai Yu4, Zhiguang Zhang5, Adekunle Toyin Bamigbade1, Hongchao Zhang6, Xuan Wei6, Xuelin Zhang7, Bin Liang8, Pingsheng Liu1
1National Laboratory of Biomacromolecules, CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing, 100101, China
2Graduate School of Anhui Medical University, Hefei, 230032, China
3School of Life Sciences, Anhui University, Hefei 230601, China
4University of Chinese Academy of Sciences, Beijing, 100049, China
5Department of Cell Biology and Genetics, School of Basic Medical Sciences, Fujian Medical University, Fuzhou, 350004, China
6General Hospital of Air Force, Beijing, 100142, China
7School of Kinesiology and Health, Capital University of Physical Education and Sports, Beijing 100191, China
8Key Laboratory of Animal Models and Human Disease Mechanisms of Chinese Academy of Science & Yunnan Province, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, 650223, China

Tóm tắt

Từ khóa


Tài liệu tham khảo

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 6:3256–3265

Bell M, Wang H, Chen H, McLenithan JC, Gong DW, Yang RZ, Yu D, Fried SK, Quon MJ, Londos C, Sztalryd C (2008) Consequences of lipid droplet coat protein downregulation in liver cells: abnormal lipid droplet metabolism and induction of insulin resistance. Diabetes 57:2037–2045

Bickel PE, Tansey JT, Welte MA (2009) PAT proteins, an ancient family of lipid droplet proteins that regulate cellular lipid stores. Biochem Biophys Acta 1791:419–440

Binns D, Januszewski T, Chen Y, Hill J, Markin VS, Zhao Y, Gilpin C, Chapman KD, Anderson RG, Goodman JM (2006) An intimate collaboration between peroxisomes and lipid bodies. J Cell Biol 173:719–731

Bosma M, Hesselink MK, Sparks LM, Timmers S, Ferraz MJ, Mattijssen F, van Beurden D, Schaart G, de Baets MH, Verheyen FK, Kersten S, Schrauwen P (2012) Perilipin 2 improves insulin sensitivity in skeletal muscle despite elevated intramuscular lipid levels. Diabetes 61:2679–2690

Brasaemle DL (2007) Thematic review series: adipocyte biology. The perilipin family of structural lipid droplet proteins: stabilization of lipid droplets and control of lipolysis. J Lipid Res 48:2547–2559

Brasaemle DL, Barber T, Wolins NE, Serrero G, Blanchette-Mackie EJ, Londos C (1997) Adipose differentiation-related protein is an ubiquitously expressed lipid storage droplet-associated protein. J Lipid Res 38:2249–2263

Brown DA (2001) Lipid droplets: proteins floating on a pool of fat. Curr Biol 11:R446–R449

Chang BH, Li L, Paul A, Taniguchi S, Nannegari V, Heird WC, Chan L (2006) Protection against fatty liver but normal adipogenesis in mice lacking adipose differentiation-related protein. Mol Cell Biol 26:1063–1076

Chang BH, Li L, Saha P, Chan L (2010) Absence of adipose differentiation related protein upregulates hepatic VLDL secretion, relieves hepatosteatosis, and improves whole body insulin resistance in leptin-deficient mice. J Lipid Res 51:2132–2142

Coll T, Eyre E, Rodriguez-Calvo R, Palomer X, Sanchez RM, Merlos M, Laguna JC, Vazquez-Carrera M (2008) Oleate reverses palmitate-induced insulin resistance and inflammation in skeletal muscle cells. J Biol Chem 283:11107–11116

Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339:819–823

de Wilde J, Smit E, Snepvangers FJ, de Wit NW, Mohren R, Hulshof MF, Mariman EC (2010) Adipophilin protein expression in muscle–a possible protective role against insulin resistance. FEBS J 277:761–773

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, Steinbüchel A, Liu P (2012) Identification of the major functional proteins of prokaryotic lipid droplets. J Lipid Res 53:399–411

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 8:43–51

Fujimoto T, Parton RG (2011) Not just fat: the structure and function of the lipid droplet. Cold Spring Harb Perspect Biol 3(3):a004838

Fukushima M, Enjoji M, Kohjima M, Sugimoto R, Ohta S, Kotoh K, Kuniyoshi M, Kobayashi K, Imamura M, Inoguchi T, Nakamuta M, Nawata H (2005) Adipose differentiation related protein induces lipid accumulation and lipid droplet formation in hepatic stellate cells. In Vitro Cell Dev Biol Anim 41:321–324

Gao D, Griffiths HR, Bailey CJ (2009) Oleate protects against palmitate-induced insulin resistance in L6 myotubes. Br J Nutr 102:1557–1563

Goodman JM (2008) The gregarious lipid droplet. J Biol Chem 283:28005–28009

Greenberg AS, Coleman RA, Kraemer FB, McManaman JL, Obin MS, Puri V, Yan QW, Miyoshi H, Mashek DG (2011) The role of lipid droplets in metabolic disease in rodents and humans. J Clin Investig 121:2102–2110

Heid HW, Moll R, Schwetlick I, Rackwitz HR, Keenan TW (1998) Adipophilin is a specific marker of lipid accumulation in diverse cell types and diseases. Cell Tissue Res 294:309–321

Kaushik S, Cuervo AM (2015) Degradation of lipid droplet-associated proteins by chaperone-mediated autophagy facilitates lipolysis. Nat Cell Biol 17:759–770

Kaushik S, Cuervo AM (2016) AMPK-dependent phosphorylation of lipid droplet protein PLIN2 triggers its degradation by CMA. Autophagy 12:432–438

Kelley DE, Goodpaster B, Wing RR, Simoneau JA (1999) Skeletal muscle fatty acid metabolism in association with insulin resistance, obesity, and weight loss. Am J Physiol 277:E1130–E1141

Kimmel AR, Brasaemle DL, McAndrews-Hill M, Sztalryd C, Londos C (2010) Adoption of PERILIPIN as a unifying nomenclature for the mammalian PAT-family of intracellular lipid storage droplet proteins. J Lipid Res 51:468–471

Koves TR, Sparks LM, Kovalik JP, Mosedale M, Arumugam R, DeBalsi KL, Everingham K, Thorne L, Phielix E, Meex RC, Kien CL, Hesselink MK, Schrauwen P, Muoio DM (2013) PPARgamma coactivator-1alpha contributes to exercise-induced regulation of intramuscular lipid droplet programming in mice and humans. J Lipid Res 54:522–534

Larigauderie G, Cuaz-Perolin C, Younes AB, Furman C, Lasselin C, Copin C, Jaye M, Fruchart JC, Rouis M (2006) Adipophilin increases triglyceride storage in human macrophages by stimulation of biosynthesis and inhibition of beta-oxidation. FEBS J 273:3498–3510

Libby AE, Bales ES, Orlicky DJ, McManaman JL (2016) Perilipin-2 deletion impairs hepatic lipid accumulation by interfering with SREBP activation and altering the hepatic lipidome. J Biol Chem 291(46):24231–24246

Listenberger LL, Ostermeyer-Fay AG, Goldberg EB, Brown WJ, Brown DA (2007) Adipocyte differentiation-related protein reduces the lipid droplet association of adipose triglyceride lipase and slows triacylglycerol turnover. J Lipid Res 48:2751–2761

Liu P, Ying Y, Zhao Y, Mundy DI, Zhu M, Anderson RG (2004) Chinese hamster ovary K2 cell lipid droplets appear to be metabolic organelles involved in membrane traffic. J Biol Chem 279:3787–3792

Liu P, Bartz R, Zehmer JK, Ying YS, Zhu M, Serrero G, Anderson RG (2007) Rab-regulated interaction of early endosomes with lipid droplets. Biochem Biophys Acta 1773:784–793

MacPherson RE, Peters SJ (2015a) Piecing together the puzzle of perilipin proteins and skeletal muscle lipolysis. Appl Physiol Nutr Metab 40(7):641–651

MacPherson REK, Peters SJ (2015b) Piecing together the puzzle of perilipin proteins and skeletal muscle lipolysis. Appl Physiol Nutr Metab 40:641–651

MacPherson RE, Herbst EA, Reynolds EJ, Vandenboom R, Roy BD, Peters SJ (2012) Subcellular localization of skeletal muscle lipid droplets and PLIN family proteins OXPAT and ADRP at rest and following contraction in rat soleus muscle. Am J Physiol Regul Integr Comp Physiol 302:R29–R36

MacPherson RE, Ramos SV, Vandenboom R, Roy BD, Peters SJ (2013) Skeletal muscle PLIN proteins, ATGL and CGI-58, interactions at rest and following stimulated contraction. Am J Physiol Regul Integr Comp Physiol 304:R644–R650

Masuda Y, Itabe H, Odaki M, Hama K, Fujimoto Y, Mori M, Sasabe N, Aoki J, Arai H, Takano T (2006) ADRP/adipophilin is degraded through the proteasome-dependent pathway during regression of lipid-storing cells. J Lipid Res 47:87–98

Mayer N, Schweiger M, Romauch M, Grabner GF, Eichmann TO, Fuchs E, Ivkovic J, Heier C, Mrak I, Lass A, Höfler G, Fledelius C, Zechner R, Zimmermann R, Breinbauer R (2013) Development of small-molecule inhibitors targeting adipose triglyceride lipase. Nat Chem Biol 9:785–787

McManaman JL, Bales ES, Orlicky DJ, Jackman M, MacLean PS, Cain S, Crunk AE, Mansur A, Graham CE, Bowman TA, Greenberg AS (2013) Perilipin-2-null mice are protected against diet-induced obesity, adipose inflammation, and fatty liver disease. J Lipid Res 54:1346–1359

Meex RC, Hoy AJ, Mason RM, Martin SD, McGee SL, Bruce CR, Watt MJ (2015) ATGL-mediated triglyceride turnover and the regulation of mitochondrial capacity in skeletal muscle. Am J Physiol Endocrinol Metab 308:E960–E970

Minnaard R, Schrauwen P, Schaart G, Jorgensen JA, Lenaers E, Mensink M, Hesselink MKC (2009) Adipocyte differentiation-related protein and OXPAT in rat and human skeletal muscle: involvement in lipid accumulation and type 2 diabetes mellitus. J Clin Endocr Metab 94:4077–4085

Murphy S, Martin S, Parton RG (2009) Lipid droplet-organelle interactions; sharing the fats. Biochem Biophys Acta 1791:441–447

Nan X, Potma EO, Xie XS (2006) Nonperturbative chemical imaging of organelle transport in living cells with coherent anti-stokes Raman scattering microscopy. Biophys J 91:728–735

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 118:2601–2611

Pan DA, Lillioja S, Kriketos AD, Milner MR, Baur LA, Bogardus C, Jenkins AB, Storlien LH (1997) Skeletal muscle triglyceride levels are inversely related to insulin action. Diabetes 46:983–988

Peng G, Li L, Liu Y, Pu J, Zhang S, Yu J, Zhao J, Liu P (2011) Oleate blocks palmitate-induced abnormal lipid distribution, endoplasmic reticulum expansion and stress, and insulin resistance in skeletal muscle. Endocrinology 152:2206–2218

Peters SJ, Samjoo IA, Devries MC, Stevic I, Robertshaw HA, Tarnopolsky MA (2012) Perilipin family (PLIN) proteins in human skeletal muscle: the effect of sex, obesity, and endurance training. Appl Physiol Nutr Me 37:724–735

Prats C, Donsmark M, Qvortrup K, Londos C, Sztalryd C, Holm C, Galbo H, Ploug T (2006) Decrease in intramuscular lipid droplets and translocation of HSL in response to muscle contraction and epinephrine. J Lipid Res 47:2392–2399

Pu J, Ha CW, Zhang S, Jung JP, Huh WK, Liu P (2011) Interactomic study on interaction between lipid droplets and mitochondria. Protein Cell 2:487–496

Robenek H, Hofnagel O, Buers I, Robenek MJ, Troyer D, Severs NJ (2006) Adipophilin-enriched domains in the ER membrane are sites of lipid droplet biogenesis. J Cell Sci 119:4215–4224

Russell TD, Palmer CA, Orlicky DJ, Bales ES, Chang BH, Chan L, McManaman JL (2008) Mammary glands of adipophilin-null mice produce an amino-terminally truncated form of adipophilin that mediates milk lipid droplet formation and secretion. J Lipid Res 49:206–216

Saltiel AR (2000) Another hormone-sensitive triglyceride lipase in fat cells? Proc Natl Acad Sci USA 97:535–537

Salvado L, Coll T, Gomez-Foix AM, Salmeron E, Barroso E, Palomer X, Vazquez-Carrera M (2013) Oleate prevents saturated-fatty-acid-induced ER stress, inflammation and insulin resistance in skeletal muscle cells through an AMPK-dependent mechanism. Diabetologia 56:1372–1382

Schrader M (2001) Tubulo-reticular clusters of peroxisomes in living COS-7 cells: dynamic behavior and association with lipid droplets. J Histochem Cytochem 49:1421–1429

Shaw C, Sherlock M, Stewart P, Wagenmakers A (2009) Adipophilin distribution and colocalisation with lipid droplets in skeletal muscle. Histochem Cell Biol 131:575–581

Sturmey RG, O’Toole PJ, Leese HJ (2006) Fluorescence resonance energy transfer analysis of mitochondrial: lipid association in the porcine oocyte. Reproduction 132:829–837

Takahashi Y, Shinoda A, Kamada H, Shimizu M, Inoue J, Sato R (2016) Perilipin2 plays a positive role in adipocytes during lipolysis by escaping proteasomal degradation. Sci Rep 6:20975

Tarnopolsky MA, Rennie CD, Robertshaw HA, Fedak-Tarnopolsky SN, Devries MC, Hamadeh MJ (2007) Influence of endurance exercise training and sex on intramyocellular lipid and mitochondrial ultrastructure, substrate use, and mitochondrial enzyme activity. Am J Physiol Regul Integr Comp Physiol 292:R1271–R1278

Thiam AR, Farese RV Jr, Walther TC (2013) The biophysics and cell biology of lipid droplets. Nat Rev Mol Cell Biol 14:775–786

Unger RH, Clark GO, Scherer PE, Orci L (2010) Lipid homeostasis, lipotoxicity and the metabolic syndrome. Biochem Biophys Acta 1801:209–214

Villena JA, Roy S, Sarkadi-Nagy E, Kim KH, Sul HS (2004) Desnutrin, an adipocyte gene encoding a novel patatin domain-containing protein, is induced by fasting and glucocorticoids. J Biol Chem 279:47066–47075

Walther TC, Farese RV Jr (2012) Lipid droplets and cellular lipid metabolism. Annu Rev Biochem 81:687–714

Xu G, Sztalryd C, Lu X, Tansey JT, Gan J, Dorward H, Kimmel AR, Londos C (2005) Post-translational regulation of adipose differentiation-related protein by the ubiquitin/proteasome pathway. J Biol Chem 280:42841–42847

Yen CL, Stone SJ, Koliwad S, Harris C, Farese RV Jr (2008) Thematic review series: glycerolipids. DGAT enzymes and triacylglycerol biosynthesis. J Lipid Res 49:2283–2301

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. Biochem Biophys Acta 1853:918–928

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 10:4757–4768

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 11:317–328

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 306:1383–1386

Zimmermann R, Lass A, Haemmerle G, Zechner R (2009) Fate of fat: the role of adipose triglyceride lipase in lipolysis. Biochim Biophys Acta 1791:494–500