Fold of an oleosin targeted to cellular oil bodies

Biochimica et Biophysica Acta - Biomembranes

Volumn 1828, Issue 8, 2013, Pages 1881-1888

  Vindigni, Jean David ^a   Wien, Frank ^b   Giuliani, Alexandre ^b,c   Erpapazoglou, Zoi ^d,e   Tache, Roselyne ^a   Jagic, Franjo ^a   Chardot, Thierry ^a   Gohon, Yann ^a   Froissard, Marine ^a  

^a INSTITUT JEAN PIERRE BOURGIN   (France)

^b SYNCHROTRON SOLEIL   (France)

^c CEMAGREF   (France)

^d CNRS   (France)

^e SORBONNE UNIVERSITÉ   (France)

Author keywords

Foscholine 12; Heterologous expression; Oil body; Oleosin; Protein fold; SRCD

Indexed keywords

DETERGENT; GREEN FLUORESCENT PROTEIN; MEMBRANE PROTEIN; OLEOSIN; PHOSPHOLIPID; UNCLASSIFIED DRUG;

ALPHA HELIX; ARABIDOPSIS THALIANA; ARTICLE; BETA SHEET; CELL ORGANELLE; CIRCULAR DICHROISM; CONTROLLED STUDY; HYDROPHOBICITY; LIPID MONOLAYER; LIPID STORAGE; NONHUMAN; OIL BODY; PLANT SEED; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN TARGETING; SACCHAROMYCES CEREVISIAE; SYNCHROTRON RADIATION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL MEMBRANE; CIRCULAR DICHROISM; GREEN FLUORESCENT PROTEINS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; IMMUNOBLOTTING; MEMBRANE PROTEINS; MICROSCOPY, FLUORESCENCE; OILS; PHOSPHORYLCHOLINE; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE;

ARABIDOPSIS THALIANA; MAMMALIA; SACCHAROMYCES CEREVISIAE;

EID: 84877058110     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2013.04.009     Document Type: Article

References (59)

1. D.J. Murphy The dynamic roles of intracellular lipid droplets: from archaea to mammals Protoplasma 249 2012 541 585
2. D.L. Brasaemle, and N.E. Wolins Packaging of fat: an evolving model of lipid droplet assembly and expansion J. Biol. Chem. 287 2012 2273 2279
3. L. Yang, Y. Ding, Y. Chen, S. Zhang, C. Huo, Y. Wang, J. Yu, P. Zhang, H. Na, H. Zhang, Y. Ma, and P. Liu The proteomics of lipid droplets: structure, dynamics, and functions of the organelle conserved from bacteria to humans J. Lipid Res. 53 2012 1245 1253
4. M. Bell, H. Wang, H. Chen, J.C. McLenithan, D.W. Gong, R.Z. Yang, D. Yu, S.K. Fried, M.J. Quon, C. Londos, and C. Sztalryd Consequences of lipid droplet coat protein downregulation in liver cells: abnormal lipid droplet metabolism and induction of insulin resistance Diabetes 57 2008 2037 2045
5. D.J. Rader, and E. Pure Lipoproteins, macrophage function, and atherosclerosis: beyond the foam cell? Cell Metab. 1 2005 223 230 (Pubitemid 43960611)
6. A.H. Huang Oleosins and oil bodies in seeds and other organs Plant Physiol. 110 1996 1055 1061 (Pubitemid 126630714)
7. G. Xu, C. Sztalryd, X. Lu, J.T. Tansey, J. Gan, H. Dorward, A.R. Kimmel, and C. Londos Post-translational regulation of adipose differentiation-related protein by the ubiquitin/proteasome pathway J. Biol. Chem. 280 2005 42841 42847 (Pubitemid 43049246)
8. G. Xu, C. Sztalryd, and C. Londos Degradation of perilipin is mediated through ubiquitination-proteasome pathway Biochim. Biophys. Acta 1761 2006 83 90
9. D.L. Brasaemle 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 2007 2547 2559 (Pubitemid 350272839)
10. A. Marcinkiewicz, D. Gauthier, A. Garcia, and D.L. Brasaemle The phosphorylation of serine 492 of perilipin a directs lipid droplet fragmentation and dispersion J. Biol. Chem. 281 2006 11901 11909 (Pubitemid 43855452)
11. P. Jolivet, C. Boulard, A. Bellamy, B. Valot, S. d'Andrea, M. Zivy, N. Nesi, and T. Chardot Oil body proteins sequentially accumulate throughout seed development in Brassica napus J. Plant Physiol. 168 2011 2015 2020
12. R.M. Siloto, K. Findlay, A. Lopez-Villalobos, E.C. Yeung, C.L. Nykiforuk, and M.M. Moloney The accumulation of oleosins determines the size of seed oilbodies in arabidopsis Plant Cell 18 2006 1961 1974 (Pubitemid 44260190)
13. T.L. Shimada, T. Shimada, H. Takahashi, Y. Fukao, and I. Hara-Nishimura A novel role for oleosins in freezing tolerance of oilseeds in Arabidopsis thaliana Plant J. 55 2008 798 809
14. S.J. Hickenbottom, A.R. Kimmel, C. Londos, and J.H. Hurley Structure of a lipid droplet protein; the PAT family member TIP47 Structure 12 2004 1199 1207 (Pubitemid 38900762)
15. D.J. Lacey, N. Wellner, F. Beaudoin, J.A. Napier, and P.R. Shewry Secondary structure of oleosins in oil bodies isolated from seeds of safflower (Carthamus tinctorius L.) and sunflower (Helianthus annuus L.) Biochem. J. 334 Pt 2 1998 469 477 (Pubitemid 28448592)
16. M. Li, D.J. Murphy, K.H. Lee, R. Wilson, L.J. Smith, D.C. Clark, and J.Y. Sung Purification and structural characterization of the central hydrophobic domain of oleosin J. Biol. Chem. 277 2002 37888 37895
17. Y. Gohon, J.D. Vindigni, A. Pallier, F. Wien, H. Celia, A. Giuliani, C. Tribet, T. Chardot, and P. Briozzo High water solubility and fold in amphipols of proteins with large hydrophobic regions: oleosins and caleosin from seed lipid bodies Biochim. Biophys. Acta 1808 2011 706 716
18. B.M. Chong, T.D. Russell, J. Schaack, D.J. Orlicky, P. Reigan, M. Ladinsky, and J.L. McManaman The adipophilin C terminus is a self-folding membrane-binding domain that is important for milk lipid secretion J. Biol. Chem. 286 2011 23254 23265
19. K.B. Vargo, R. Parthasarathy, and D.A. Hammer Self-assembly of tunable protein suprastructures from recombinant oleosin Proc. Natl. Acad. Sci. U.S.A. 109 2012 11657 11662
20. J.C. Chen, and J.T. Tzen An in vitro system to examine the effective phospholipids and structural domain for protein targeting to seed oil bodies Plant Cell Physiol. 42 2001 1245 1252 (Pubitemid 34009617)
21. F. Beaudoin, and J.A. Napier Targeting and membrane-insertion of a sunflower oleosin in vitro and in Saccharomyces cerevisiae: the central hydrophobic domain contains more than one signal sequence, and directs oleosin insertion into the endoplasmic reticulum membrane using a signal anchor sequence mechanism Planta 215 2002 293 303 (Pubitemid 36064979)
22. V. Subramanian, A. Garcia, A. Sekowski, and D.L. Brasaemle Hydrophobic sequences target and anchor perilipin A to lipid droplets J. Lipid Res. 45 2004 1983 1991 (Pubitemid 40990892)
23. B.M. Abell, M. Hahn, L.A. Holbrook, and M.M. Moloney Membrane topology and sequence requirements for oil body targeting of oleosin Plant J. 37 2004 461 470 (Pubitemid 38258768)
24. P.E. Bickel, J.T. Tansey, and M.A. Welte PAT proteins, an ancient family of lipid droplet proteins that regulate cellular lipid stores Biochim. Biophys. Acta 1791 2009 419 440
25. G.I. Frandsen, J. Mundy, and J.T. Tzen Oil bodies and their associated proteins, oleosin and caleosin Physiol. Plant. 112 2001 301 307 (Pubitemid 32632602)
26. Z. Purkrtova, C. Le Bon, B. Kralova, M.H. Ropers, M. Anton, and T. Chardot Caleosin of arabidopsis thaliana: effect of calcium on functional and structural properties J. Agric. Food Chem. 56 2008 11217 11224
27. J. Tzen, Y. Cao, P. Laurent, C. Ratnayake, and A. Huang Lipids, proteins, and structure of seed oil bodies from diverse species Plant Physiol 101 1993 267 276
28. G. Kefala, C. Ahn, M. Krupa, L. Esquivies, I. Maslennikov, W. Kwiatkowski, and S. Choe Structures of the OmpF porin crystallized in the presence of foscholine-12 Protein Sci. 19 2010 1117 1125
29. M. Froissard, S. D'Andrea, C. Boulard, and T. Chardot Heterologous expression of AtClo1, a plant oil body protein, induces lipid accumulation in yeast FEMS Yeast Res. 9 2009 428 438
30. M. Froissard, N. Belgareh-Touze, N. Buisson, M. Desimone, W.B. Frommer, and R. Haguenauer-Tsapis Heterologous expression of a plant uracil transporter in yeast: improvement of plasma membrane targeting in mutants of the Rsp5p ubiquitin protein ligase Biotechnol. J. 1 2006 308 320
31. E. Roux, S. Baumberger, M.A. Axelos, and T. Chardot Oleosins of Arabidopsis thaliana: expression in Escherichia coli, purification, and functional properties J. Agric. Food Chem. 52 2004 5245 5249
32. C. Volland, D. Urban-Grimal, G. Geraud, and R. Haguenauer-Tsapis Endocytosis and degradation of the yeast uracil permease under adverse conditions J. Biol. Chem. 269 1994 9833 9841 (Pubitemid 24196592)
33. W. Yu, J. Cassara, and P.F. Weller Phosphatidylinositide 3-kinase localizes to cytoplasmic lipid bodies in human polymorphonuclear leukocytes and other myeloid-derived cells Blood 95 2000 1078 1085 (Pubitemid 30062734)
34. J. Landry, and S. Delhaye A simple and rapid procedure for hydrolyzing minute amounts of proteins with alkali Anal. Biochem. 243 1996 191 194 (Pubitemid 26418598)
35. S. D'Andrea, P. Jolivet, C. Boulard, C. Larre, M. Froissard, and T. Chardot Selective one-step extraction of arabidopsis thaliana seed oleosins using organic solvents J. Agric. Food Chem. 55 2007 10008 10015 (Pubitemid 350305189)
36. M. Refregiers, F. Wien, H.P. Ta, L. Premvardhan, S. Bac, F. Jamme, V. Rouam, B. Lagarde, F. Polack, J.L. Giorgetta, J.P. Ricaud, M. Bordessoule, and A. Giuliani DISCO synchrotron-radiation circular-dichroism endstation at SOLEIL J. Synchrotron Radiat. 19 2012 831 835
37. J.G. Lees, B.R. Smith, F. Wien, A.J. Miles, and B.A. Wallace CDtool-an integrated software package for circular dichroism spectroscopic data processing, analysis, and archiving Anal. Biochem. 332 2004 285 289 (Pubitemid 39485737)
38. L. Whitmore, and B.A. Wallace DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data Nucleic Acids Res. 32 2004 W668 W673
39. J.G. Lees, A.J. Miles, F. Wien, and B.A. Wallace A reference database for circular dichroism spectroscopy covering fold and secondary structure space Bioinformatics 22 2006 1955 1962 (Pubitemid 44283007)
40. A. Abdul-Gader, A.J. Miles, and B.A. Wallace A reference dataset for the analyses of membrane protein secondary structures and transmembrane residues using circular dichroism spectroscopy Bioinformatics 27 2011 1630 1636
41. C. Tribet, R. Audebert, and J.L. Popot Amphipols: polymers that keep membrane proteins soluble in aqueous solutions Proc. Natl. Acad. Sci. U.S.A. 93 1996 15047 15050 (Pubitemid 27009549)
42. B.A. Wallace, and R.W. Janes Synchrotron radiation circular dichroism spectroscopy of proteins: secondary structure, fold recognition and structural genomics Curr. Opin. Chem. Biol. 5 2001 567 571 (Pubitemid 32907609)
43. J.T. Ting, R.A. Balsamo, C. Ratnayake, and A.H. Huang Oleosin of plant seed oil bodies is correctly targeted to the lipid bodies in transformed yeast J. Biol. Chem. 272 1997 3699 3706 (Pubitemid 27066879)
44. F. Beaudoin, B.M. Wilkinson, C.J. Stirling, and J.A. Napier In vivo targeting of a sunflower oil body protein in yeast secretory (sec) mutants Plant J. 23 2000 159 170 (Pubitemid 30597276)
45. S.M. Kelly, T.J. Jess, and N.C. Price How to study proteins by circular dichroism Biochim. Biophys. Acta 1751 2005 119 139 (Pubitemid 41112231)
46. N. Sreerama, S.Y. Venyaminov, and R.W. Woody Estimation of the number of alpha-helical and beta-strand segments in proteins using circular dichroism spectroscopy Protein Sci. 8 1999 370 380 (Pubitemid 29072437)
47. F. Yang, L.G. Moss, and G.N. Phillips Jr. The molecular structure of green fluorescent protein Nat. Biotechnol. 14 1996 1246 1251 (Pubitemid 26332784)
48. N.V. Visser, M.A. Hink, J.W. Borst, G.N. van der Krogt, and A.J. Visser Circular dichroism spectroscopy of fluorescent proteins FEBS Lett. 521 2002 31 35 (Pubitemid 34628452)
49. W. Kabsch, and C. Sander Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features Biopolymers 22 1983 2577 2637
50. M. Li, L.J. Smith, D.C. Clark, R. Wilson, and D.J. Murphy Secondary structures of a new class of lipid body proteins from oilseeds J. Biol. Chem. 267 1992 8245 8253
51. M. Li, J.S. Keddie, L.J. Smith, D.C. Clark, and D.J. Murphy Expression and characterization of the N-terminal domain of an oleosin protein from sunflower J. Biol. Chem. 268 1993 17504 17512 (Pubitemid 23236994)
52. M. Millichip, A.S. Tatham, F. Jackson, G. Griffiths, P.R. Shewry, and A.K. Stobart Purification and characterization of oil-bodies (oleosomes) and oil-body boundary proteins (oleosins) from the developing cotyledons of sunflower (Helianthus annuus L.) Biochem. J. 314 Pt 1 1996 333 337 (Pubitemid 26063867)
53. C.C. Peng, I.P. Lin, C.K. Lin, and J.T. Tzen Size and stability of reconstituted sesame oil bodies Biotechnol. Prog. 19 2003 1623 1626 (Pubitemid 37250057)
54. L. Wang, M.T. Walsh, and D.M. Small Apolipoprotein B is conformationally flexible but anchored at a triolein/water interface: a possible model for lipoprotein surfaces Proc. Natl. Acad. Sci. U.S.A. 103 2006 6871 6876
55. A. Coronado-Gray, and R. van Antwerpen The physical state of the LDL core influences the conformation of apolipoprotein B-100 on the lipoprotein surface FEBS Lett. 533 2003 21 24 (Pubitemid 36206375)
56. V. Kumar, S.J. Butcher, K. Oorni, P. Engelhardt, J. Heikkonen, K. Kaski, M. Ala-Korpela, and P.T. Kovanen Three-dimensional cryoEM reconstruction of native LDL particles to 16A resolution at physiological body temperature PLoS One 6 2011 e18841
57. J. Hovers, M. Potschies, A. Polidori, B. Pucci, S. Raynal, F. Bonnete, M.J. Serrano-Vega, C.G. Tate, D. Picot, Y. Pierre, J.L. Popot, R. Nehme, M. Bidet, I. Mus-Veteau, H. Busskamp, K.H. Jung, A. Marx, P.A. Timmins, and W. Welte A class of mild surfactants that keep integral membrane proteins water-soluble for functional studies and crystallization Mol. Membr. Biol. 28 2011 171 181
58. J.L. Popot, T. Althoff, D. Bagnard, J.L. Baneres, P. Bazzacco, E. Billon-Denis, L.J. Catoire, P. Champeil, D. Charvolin, M.J. Cocco, G. Cremel, T. Dahmane, L.M. de la Maza, C. Ebel, F. Gabel, F. Giusti, Y. Gohon, E. Goormaghtigh, E. Guittet, J.H. Kleinschmidt, W. Kuhlbrandt, C. Le Bon, K.L. Martinez, M. Picard, B. Pucci, J.N. Sachs, C. Tribet, C. van Heijenoort, F. Wien, F. Zito, and M. Zoonens Amphipols from A to Z Annu. Rev. Biophys. 40 2011 379 408
59. L. Wang, D.D. Martin, E. Genter, J. Wang, R.S. McLeod, and D.M. Small Surface study of apoB1694-1880, a sequence that can anchor apoB to lipoproteins and make it nonexchangeable J. Lipid Res. 50 2009 1340 1352