Hydrophobic and basic domains target proteins to lipid droplets

Traffic

Volumn 10, Issue 12, 2009, Pages 1785-1801

  Ingelmo Torres, Mercedes ^a,b   González Moreno, Elena ^a   Kassan, Adam ^b   Hanzal Bayer, Michael ^c   Tebar, Francesc ^a   Herms, Albert ^b   Grewal, Thomas ^d   Hancock, John F ^c   Enrich, Carlos ^a,b   Bosch, Marta ^b   Gross, Steven P ^e   Parton, Robert G ^c   Pol, Albert ^b,f  

^a UNIVERSITY OF BARCELONA   (Spain)

^b INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d UNIVERSITY OF SYDNEY   (Australia)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f Estudis Avançats ^*  (Spain)

Author keywords

ALDI; Caveolin; Endoplasmic reticulum; Lipid droplets; Sorting signal

Indexed keywords

CAVEOLIN; FAT DROPLET;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; HYDROPHOBICITY; MITOCHONDRIAL MEMBRANE; MUTATIONAL ANALYSIS; NONHUMAN; PEROXISOME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; LIPIDS; MOLECULAR SEQUENCE DATA; PROTEINS;

EID: 70749126722     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2009.00994.x     Document Type: Article

References (58)

1. Murphy S, Martin S, Parton RG. Lipid droplet-organelle interactions; sharing the fats. Biochim Biophys Acta 2009, 1791:441-447.
2. Ohsaki Y, Cheng J, Suzuki M, Shinohara Y, Fujita A, Fujimoto T. Biogenesis of cytoplasmic lipid droplets: from the lipid ester globule in the membrane to the visible structure. Biochim Biophys Acta 2009, 1791:399-407.
3. Tauchi-Sato K, Ozeki S, Houjou T, Taguchi R, Fujimoto T. The surface of lipid droplets is a phospholipid monolayer with a unique fatty acid composition. J Biol Chem 2002, 277:44507-44512.
4. Leber R, Zinser E, Zellnig G, Paltauf F, Daum G. Characterization of lipid particles of the yeast, Saccharomyces cerevisiae. Yeast 1994, 10:1421-1428.
5. Bartz R, Li WH, Venables B, Zehmer JK, Roth MR, Welti R, Anderson RG, Liu P, Chapman KD. Lipidomics reveals that adiposomes store ether lipids and mediate phospholipid traffic. J Lipid Res 2007, 48:837-847.
6. Guo Y, Walther TC, Rao M, Stuurman N, Goshima G, Terayama K, Wong JS, Vale RD, Walter P, Farese RV. Functional genomic screen reveals genes involved in lipid-droplet formation and utilization. Nature 2008, 453:657-661.
7. Fujimoto Y, Itabe H, Sakai J, Makita M, Noda J, Mori M, Higashi Y, Kojima S, Takano T. Identification of major proteins in the lipid droplet-enriched fraction isolated from the human hepatocyte cell line HuH7. Biochim Biophys Acta 2004, 1644:47-59.
8. Liu P, Ying Y, Zhao Y, Mundy DI, Zhu M, Anderson RG. Chinese hamster ovary K2 cell lipid droplets appear to be metabolic organelles involved in membrane traffic. J Biol Chem 2004, 279:3787-3792.
9. Brasaemle DL, Dolios G, Shapiro L, Wang R. Proteomic analysis of proteins associated with lipid droplets of basal and lipolytically stimulated 3T3-L1 adipocytes. J Biol Chem 2004, 279:46835-46842.
10. Cermelli S, Guo Y, Gross SP, Welte MA. The lipid-droplet proteome reveals that droplets are a protein-storage depot. Curr Biol 2006, 16:1783-1795.
11. Turro S, Ingelmo-Torres M, Estanyol JM, Tebar F, Fernandez MA, Albor CV, Gaus K, Grewal T, Enrich C, Pol A. Identification and characterization of associated with lipid droplet protein 1: a novel membrane-associated protein that resides on hepatic lipid droplets. Traffic 2006, 7:1254-1269.
12. Umlauf E, Csaszar E, Moertelmaier M, Schuetz GJ, Parton RG, Prohaska R. Association of stomatin with lipid bodies. J Biol Chem 2004, 279:23699-23709.
13. Beller M, Riedel D, Jansch L, Dieterich G, Wehland J, Jackle H, Kuhnlein RP. Characterization of the Drosophila lipid droplet subproteome. Mol Cell Proteomics 2006, 5:1082-1094.
14. Bartz R, Zehmer JK, Zhu M, Chen Y, Serrero G, Zhao Y, Liu P. Dynamic activity of lipid droplets: protein phosphorylation and GTP-mediated protein translocation. J Proteome Res 2007, 6:3256-3265.
15. Sato S, Fukasawa M, Yamakawa Y, Natsume T, Suzuki T, Shoji I, Aizaki H, Miyamura T, Nishijima M. Proteomic profiling of lipid droplet proteins in hepatoma cell lines expressing hepatitis C virus core protein. J Biochem (Tokyo) 2006, 139:921-930.
16. Wu CC, Howell KE, Neville MC, Yates JR, McManaman JL. Proteomics reveal a link between the endoplasmic reticulum and lipid secretory mechanisms in mammary epithelial cells. Electrophoresis 2000, 21:3470-3482.
17. Wan HC, Melo RC, Jin Z, Dvorak AM, Weller PF. Roles and origins of leukocyte lipid bodies: proteomic and ultrastructural studies. Faseb J 2007, 21:167-178.
18. Robenek H, Hofnagel O, Buers I, Robenek MJ, Troyer D, Severs NJ. Adipophilin-enriched domains in the ER membrane are sites of lipid droplet biogenesis. J Cell Sci 2006, 119:4215-4224.
19. Greenberg AS, Egan JJ, Wek SA, Garty NB, Blanchette-Mackie EJ, Londos C. Perilipin, a major hormonally regulated adipocyte-specific phosphoprotein associated with the periphery of lipid storage droplets. J Biol Chem 1991, 266:11341-11346.
20. Brasaemle DL, Barber T, Wolins NE, Serrero G, Blanchette-Mackie EJ, Londos C. Adipose differentiation-related protein is an ubiquitously expressed lipid storage droplet-associated protein. J Lipid Res 1997, 38:2249-2263.
21. Martin S, Parton RG. Caveolin, cholesterol, and lipid bodies. Semin Cell Dev Biol 2005, 16:163-174.
22. Ozeki S, Cheng J, Tauchi-Sato K, Hatano N, Taniguchi H, Fujimoto T. Rab18 localizes to lipid droplets and induces their close apposition to the endoplasmic reticulum-derived membrane. J Cell Sci 2005, 118:2601-2611.
23. Chen JC, Tsai CC, Tzen JT. Cloning and secondary structure analysis of caleosin, a unique calcium-binding protein in oil bodies of plant seeds. Plant Cell Physiol 1999, 40:1079-1086.
24. Qu RD, Huang AH. Oleosin KD 18 on the surface of oil bodies in maize. Genomic and cDNA sequences and the deduced protein structure. J Biol Chem 1990, 265:2238-2243.
25. Barba G, Harper F, Harada T, Kohara M, Goulinet S, Matsuura Y, Eder G, Schaff Z, Chapman MJ, Miyamura T, Brechot C. Hepatitis C virus core protein shows a cytoplasmic localization and associates to cellular lipid storage droplets. Proc Natl Acad Sci U S A 1997, 94:1200-1205.
26. Hope RG, Murphy DJ, McLauchlan J. The domains required to direct core proteins of hepatitis C virus and GB virus-B to lipid droplets share common features with plant oleosin proteins. J Biol Chem 2002, 277:4261-4270.
27. Fujimoto T, Kogo H, Ishiguro K, Tauchi K, Nomura R. Caveolin-2 is targeted to lipid droplets, a new " membrane domain" in the cell. J Cell Biol 2001, 152:1079-1085.
28. Ostermeyer AG, Paci JM, Zeng Y, Lublin DM, Munro S, Brown DA. Accumulation of caveolin in the endoplasmic reticulum redirects the protein to lipid storage droplets. J Cell Biol 2001, 152:1071-1078.
29. Pol A, Luetterforst R, Lindsay M, Heino S, Ikonen E, Parton RG. A caveolin dominant negative mutant associates with lipid bodies and induces intracellular cholesterol imbalance. J Cell Biol 2001, 152:1057-1070.
30. Athenstaedt K, Zweytick D, Jandrositz A, Kohlwein SD, Daum G. Identification and characterization of major lipid particle proteins of the yeast Saccharomyces cerevisiae. J Bacteriol 1999, 181:6441-6448.
31. Zehmer JK, Bartz R, Liu P, Anderson RG. Identification of a novel N-terminal hydrophobic sequence that targets proteins to lipid droplets. J Cell Sci 2008, 121:1852-1860.
32. Le Lay S, Hajduch E, Lindsay MR, Le Liepvre X, Thiele C, Ferre P, Parton RG, Kurzchalia T, Simons K, Dugail I. Cholesterol-induced caveolin targeting to lipid droplets in adipocytes: a role for caveolar endocytosis. Traffic 2006, 7:549-561.
33. Martin S, Driessen K, Nixon SJ, Zerial M, Parton RG. Regulated localization of Rab18 to lipid droplets: effects of lipolytic stimulation and inhibition of lipid droplet catabolism. J Biol Chem 2005, 280:42325-42335.
34. Parton RG, Simons K. The multiple faces of caveolae. Nat Rev Mol Cell Biol 2007, 8:185-194.
35. Ostermeyer AG, Ramcharan LT, Zeng Y, Lublin DM, Brown DA. Role of the hydrophobic domain in targeting caveolin-1 to lipid droplets. J Cell Biol 2004, 164:69-78.
36. Pol A, Martin S, Fernandez MA, Ferguson C, Carozzi A, Luetterforst R, Enrich C, Parton RG. Dynamic and regulated association of caveolin with lipid bodies: modulation of lipid body motility and function by a dominant negative mutant. Mol Biol Cell 2004, 15:99-110.
37. Pol A, Martin S, Fernandez MA, Ingelmo-Torres M, Ferguson C, Enrich C, Parton RG. Cholesterol and fatty acids regulate dynamic caveolin trafficking through the Golgi complex and between the cell surface and lipid bodies. Mol Biol Cell 2005, 16:2091-2105.
38. Fernandez MA, Albor C, Ingelmo-Torres M, Nixon SJ, Ferguson C, Kurzchalia T, Tebar F, Enrich C, Parton RG, Pol A. Caveolin-1 is essential for liver regeneration. Science 2006, 313:1628-1632.
39. Roy S, Luetterforst R, Harding A, Apolloni A, Etheridge M, Stang E, Rolls B, Hancock JF, Parton RG. Dominant-negative caveolin inhibits H-Ras function by disrupting cholesterol-rich plasma membrane domains. Nat Cell Biol 1999, 1:98-105.
40. Hope RG, McLauchlan J. Sequence motifs required for lipid droplet association and protein stability are unique to the hepatitis C virus core protein. J Gen Virol 2000, 81:1913-1925.
41. Luetterforst R, Stang E, Zorzi N, Carozzi A, Way M, Parton RG. Molecular characterization of caveolin association with the Golgi complex: identification of a cis-Golgi targeting domain in the caveolin molecule. J Cell Biol 1999, 145:1443-1459.
42. Borgese N, Francolini M, Snapp E. Endoplasmic reticulum architecture: structures in flux. Curr Opin Cell Biol 2006, 18:358-364.
43. Listenberger LL, Brown DA. Lipid droplets. Curr Biol 2008, 18:R237-238.
44. Boulant S, Montserret R, Hope RG, Ratinier M, Targett-Adams P, Lavergne JP, Penin F, McLauchlan J. Structural determinants that target the hepatitis C virus core protein to lipid droplets. J Biol Chem 2006, 281:22236-22247.
45. Subramanian V, Garcia A, Sekowski A, Brasaemle DL. Hydrophobic sequences target and anchor perilipin A to lipid droplets. J Lipid Res 2004, 45:1983-1991.
46. Ohsaki Y, Maeda T, Maeda M, Tauchi-Sato K, Fujimoto T. Recruitment of TIP47 to lipid droplets is controlled by the putative hydrophobic cleft. Biochem Biophys Res Commun 2006, 347:279-287.
47. Abell BM, High S, Moloney MM. Membrane protein topology of oleosin is constrained by its long hydrophobic domain. J Biol Chem 2002, 277:8602-8610.
48. Nakamura N, Fujimoto T. Adipose differentiation-related protein has two independent domains for targeting to lipid droplets. Biochem Biophys Res Commun 2003, 306:333-338.
49. Cho SY, Park PJ, Lee JH, Kim JJ, Lee TR. Identification of the domains required for the localization of Prp19p to lipid droplets or the nucleus. Biochem Biophys Res Commun 2007, 364:844-849.
50. Yamaguchi T, Matsushita S, Motojima K, Hirose F, Osumi T. MLDP, a novel PAT family protein localized to lipid droplets and enriched in the heart, is regulated by peroxisome proliferator-activated receptor alpha. J Biol Chem 2006, 281:14232-14240.
51. Shu X, Ryan RO, Forte TM. Intracellular lipid droplet targeting by apolipoprotein A-V requires the C-terminal and signal peptide segments. 2008, 49:1670-1676.
52. Borgese N, Brambillasca S, Colombo S. How tails guide tail-anchored proteins to their destinations. Curr Opin Cell Biol 2007, 19:368-375.
53. Rapaport D. Finding the right organelle. Targeting signals in mitochondrial outer-membrane proteins. EMBO Rep 2003, 4:948-952.
54. Kaufmann T, Schlipf S, Sanz J, Neubert K, Stein R, Borner C. Characterization of the signal that directs Bcl-x(L), but not Bcl-2, to the mitochondrial outer membrane. J Cell Biol 2003, 160:53-64.
55. Suzuki R, Sakamoto S, Tsutsumi T, Rikimaru A, Tanaka K, Shimoike T, Moriishi K, Iwasaki T, Mizumoto K, Matsuura Y, Miyamura T, Suzuki T. Molecular determinants for subcellular localization of hepatitis C virus core protein. J Virol 2005, 79:1271-1281.
56. Nufer O, Guldbrandsen S, Degen M, Kappeler F, Paccaud JP, Tani K, Hauri HP. Role of cytoplasmic C-terminal amino acids of membrane proteins in ER export. J Cell Sci 2002, 115:619-628.
57. Wendeler MW, Paccaud JP, Hauri HP. Role of Sec24 isoforms in selective export of membrane proteins from the endoplasmic reticulum. EMBO Rep 2007, 8:258-264.
58. Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A, Walker JM. The Proteomics Protocols Handbook 2005, In:, editor., Humana Press, New Jersey, USA