Fat & fabulous: Bifunctional lipids in the spotlight

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1841, Issue 8, 2014, Pages 1022-1030

  Haberkant, Per ^a   Holthuis, Joost C M ^b  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b UNIVERSITY OF OSNABRÜCK   (Germany)

Author keywords

Click chemistry; Imaging; Photoaffinity labeling; Protein lipid interaction; Proteomics

Indexed keywords

CHOLESTEROL; CHOLINE PHOSPHATE CYTIDYLYLTRANSFERASE; FAT; GLYCEROLIPID; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; LIPID; LIPID BINDING PROTEIN; MEMBRANE PROTEIN; NUCLEOPHILE; PHOSPHATIDYLSERINE; PROTEIN; SPHINGOLIPID; SPHINGOMYELIN;

CELL NUCLEUS MEMBRANE; CLICK CHEMISTRY; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION; PROTEOMICS; REVIEW;

CLICK CHEMISTRY; IMAGING; PHOTOAFFINITY LABELING; PROTEIN-LIPID INTERACTION; PROTEOMICS;

LIPIDS; PHOTOCHEMICAL PROCESSES; PROTEINS;

EID: 84903316607     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2014.01.003     Document Type: Review

References (78)

1. M.R. Wenk Lipidomics: new tools and applications Cell 143 2010 888 895
2. J.C. Holthuis, and T.P. Levine Lipid traffic: floppy drives and a superhighway Nat. Rev. Mol. Cell Biol. 6 2005 209 220 (Pubitemid 40314922)
3. M.A. Lemmon Membrane recognition by phospholipid-binding domains Nat. Rev. Mol. Cell Biol. 9 2008 99 111 (Pubitemid 351158910)
4. O. Gallego, M.J. Betts, J. Gvozdenovic-Jeremic, K. Maeda, C. Matetzki, C. Aguilar-Gurrieri, P. Beltran-Alvarez, S. Bonn, C. Fernandez-Tornero, L.J. Jensen, M. Kuhn, J. Trott, V. Rybin, C.W. Muller, P. Bork, M. Kaksonen, R.B. Russell, and A.C. Gavin A systematic screen for protein-lipid interactions in Saccharomyces cerevisiae Mol. Syst. Biol. 6 2010 430
5. F.X. Contreras, A.M. Ernst, P. Haberkant, P. Bjorkholm, E. Lindahl, B. Gonen, C. Tischer, A. Elofsson, G. von Heijne, C. Thiele, R. Pepperkok, F. Wieland, and B. Brugger Molecular recognition of a single sphingolipid species by a protein's transmembrane domain Nature 481 2012 525 529
6. A. Nadler, G. Reither, S. Feng, F. Stein, S. Reither, R. Muller, and C. Schultz The fatty acid composition of diacylglycerols determines local signaling patterns Angew. Chem. Int. Ed. Engl. 52 2013 6330 6334
7. L.E. Cybulski, M. Martin, M.C. Mansilla, A. Fernandez, and D. de Mendoza Membrane thickness cue for cold sensing in a bacterium Curr. Biol. 20 2010 1539 1544
8. S. Vanni, L. Vamparys, R. Gautier, G. Drin, C. Etchebest, P.F. Fuchs, and B. Antonny Amphipathic lipid packing sensor motifs: probing bilayer defects with hydrophobic residues Biophys. J. 104 2013 575 584
9. J. Lee, S.G. Taneva, B.W. Holland, D.P. Tieleman, R.B. Cornell, Structural basis for auto-inhibition of CTP:phosphocholine cytidylyltransferase (CCT), the regulatory enzyme in phosphatidylcholine synthesis, by its membrane binding amphipathic helix, J. Biol. Chem., http://dx.doi.org/10.1074/jbc.M1113. 526970.
10. R.V. Stahelin Lipid binding domains: more than simple lipid effectors J. Lipid Res. 50 2009 S299 S304 (Suppl.)
11. T. Balla Phosphoinositides: tiny lipids with giant impact on cell regulation Physiol. Rev. 93 2013 1019 1137
12. A.G. Lee Biological membranes: the importance of molecular detail Trends Biochem. Sci. 36 2011 493 500
13. N.P. Barrera, M. Zhou, and C.V. Robinson The role of lipids in defining membrane protein interactions: insights from mass spectrometry Trends Cell Biol. 23 2013 1 8
14. K. Pfeiffer, V. Gohil, R.A. Stuart, C. Hunte, U. Brandt, M.L. Greenberg, and H. Schagger Cardiolipin stabilizes respiratory chain supercomplexes J. Biol. Chem. 278 2003 52873 52880 (Pubitemid 38035887)
15. M. Zhang, E. Mileykovskaya, and W. Dowhan Cardiolipin is essential for organization of complexes III and IV into a supercomplex in intact yeast mitochondria J. Biol. Chem. 280 2005 29403 29408 (Pubitemid 41177012)
16. H. Zhu, M. Bilgin, R. Bangham, D. Hall, A. Casamayor, P. Bertone, N. Lan, R. Jansen, S. Bidlingmaier, T. Houfek, T. Mitchell, P. Miller, R.A. Dean, M. Gerstein, and M. Snyder Global analysis of protein activities using proteome chips Science 293 2001 2101 2105 (Pubitemid 32848060)
17. M. Manifava, J.W. Thuring, Z.Y. Lim, L. Packman, A.B. Holmes, and N.T. Ktistakis Differential binding of traffic-related proteins to phosphatidic acid- or phosphatidylinositol (4,5)- bisphosphate-coupled affinity reagents J. Biol. Chem. 276 2001 8987 8994
18. A.E. Saliba, I. Vonkova, S. Ceschia, G.M. Findlay, K. Maeda, C. Tischer, S. Deghou, V. van Noort, P. Bork, T. Pawson, J. Ellenberg, A.C. Gavin, A quantitative liposome microarray to systematically characterize protein-lipid interactions, Nat. Methods, http://dx.doi.org/10.1038/nmeth.2734.
19. K. Maeda, K. Anand, A. Chiapparino, A. Kumar, M. Poletto, M. Kaksonen, and A.C. Gavin Interactome map uncovers phosphatidylserine transport by oxysterol-binding proteins Nature 501 2013 257 261
20. X. Li, T.A. Gianoulis, K.Y. Yip, M. Gerstein, and M. Snyder Extensive in vivo metabolite-protein interactions revealed by large-scale systematic analyses Cell 143 2010 639 650
21. G. Dorman, and G.D. Prestwich Benzophenone photophores in biochemistry Biochemistry 33 1994 5661 5673 (Pubitemid 24184566)
22. J. Brunner New photolabeling and crosslinking methods Annu. Rev. Biochem. 62 1993 483 514 (Pubitemid 23237879)
23. J. Das Aliphatic diazirines as photoaffinity probes for proteins: recent developments Chem. Rev. 111 2011 4405 4417
24. S.M. Korneev Valence isomerization between diazo compounds and diazirines Eur. J. Org. Chem. 2011 6153 6175
25. A. Singh, E.R. Thornton, and F.H. Westheimer The photolysis of diazoacetylchymotrypsin J. Biol. Chem. 237 1962 3006 3008
26. V. Chowdhry, and F.H. Westheimer Photoaffinity labeling of biological systems Annu. Rev. Biochem. 48 1979 293 325
27. C.M. Gupta, R. Radhakrishnan, G.E. Gerber, W.L. Olsen, S.C. Quay, and H.G. Khorana Intermolecular crosslinking of fatty acyl chains in phospholipids: use of photoactivable carbene precursors Proc. Natl. Acad. Sci. U. S. A. 76 1979 2595 2599 (Pubitemid 9213914)
28. F. Ford, T. Yuzawa, M. Platz, S. Matzinger, and M. Fülscher Rearrangement of dimethylcarbene to propene: study by laser flash photolysis and ab initio molecular orbital theory J. Am. Chem. Soc. 120 1998 4430 4438 (Pubitemid 28261204)
29. G.W. Fleet, R.R. Porter, and J.R. Knowles Affinity labelling of antibodies with aryl nitrene as reactive group Nature 224 1969 511 512
30. A. Marcinek, E. Leyva, D. Whitt, and M. Platz Evidence for stepwise nitrogen extrusion and ring expansion upon photolysis of phenyl azide J. Am. Chem. Soc. 115 1993 8609 8612
31. J. Knowles Photogenerated reagents for biological receptors-site labeling Acc. Chem. Res. 5 1972 155 160
32. R.E. Galardy, L.C. Craig, and M.P. Printz Benzophenone triplet: a new photochemical probe of biological ligand-receptor interactions Nat. New Biol. 242 1973 127 128
33. M.J. Amrich, and J.A. Bell Photoisomerization of diazirine J. Am. Chem. Soc. 86 1964 292 293
34. R. Church, and M. Weiss Diazirines. II. Synthesis and properties of small functionalized diazirine molecules. Some observations on the reaction of a diaziridine with the iodine-iodine ion system J. Org. Chem. 35 1970 2465 2471
35. R.F. Church, R.R. Maleike, and M.J. Weiss Diazirines. 3. Synthesis of a series of diazirine-containing molecules and their pharmacological evaluation J. Med. Chem. 15 1972 514 518
36. R.F.R. Church, A.S. Kende, and M.J. Weiss Diazirines. I. Some observations on the scope of the ammonia-hydroxylamine-O-sulfonic acid diaziridine synthesis. The preparation of certain steroid diaziridines and diazirines J. Am. Chem. Soc. 87 1965 2665 2671
37. M.R. Bond, H. Zhang, P.D. Vu, and J.J. Kohler Photocrosslinking of glycoconjugates using metabolically incorporated diazirine-containing sugars Nat. Protoc. 4 2009 1044 1063
38. R.A. Smith, and J.R. Knowles Letter: Aryldiazirines. Potential reagents for photolabeling of biological receptor sites J. Am. Chem. Soc. 95 1973 5072 5073
39. A.H. Ross, R. Radhakrishnan, R.J. Robson, and H.G. Khorana The transmembrane domain of glycophorin A as studied by cross-linking using photoactivatable phospholipids J. Biol. Chem. 257 1982 4152 4161
40. R.E. Offord Protection of peptides of biological origin for use as intermediates in the chemical synthesis of proteins Nature 221 1969 37 40
41. J. Brunner, H. Senn, and F.M. Richards 3-Trifluoromethyl-3- phenyldiazirine. A new carbene generating group for photolabeling reagents J. Biol. Chem. 255 1980 3313 3318
42. P. Chakrabarti, and G. Khorana A new approach to the study of phospholipid-protein interactions in biological membranes. Synthesis of fatty acids and phospholipids containing photosensitive groups Biochemistry 14 1975 5021 5033
43. P. Moonen, H.P. Haagsman, L.L. Van Deenen, and K.W. Wirtz Determination of the hydrophobic binding site of phosphatidylcholine exchange protein with photosensitive phosphatidylcholine Eur. J. Biochem. 99 1979 439 445
44. Y. Xia, and L. Peng Photoactivatable lipid probes for studying biomembranes by photoaffinity labeling Chem. Rev. 113 2013 7880 7929
45. P. Haberkant, and G. van Meer Protein-lipid interactions: paparazzi hunting for snap-shots Biol. Chem. 390 2009 795 803
46. C. Thiele, M.J. Hannah, F. Fahrenholz, and W.B. Huttner Cholesterol binds to synaptophysin and is required for biogenesis of synaptic vesicles Nat. Cell Biol. 2 2000 42 49
47. M. Simons, E.M. Kramer, C. Thiele, W. Stoffel, and J. Trotter Assembly of myelin by association of proteolipid protein with cholesterol- and galactosylceramide-rich membrane domains J. Cell Biol. 151 2000 143 154
48. V. Matyash, C. Geier, A. Henske, S. Mukherjee, D. Hirsh, C. Thiele, B. Grant, F.R. Maxfield, and T.V. Kurzchalia Distribution and transport of cholesterol in Caenorhabditis elegans Mol. Biol. Cell 12 2001 1725 1736 (Pubitemid 33049725)
49. M. Suchanek, R. Hynynen, G. Wohlfahrt, M. Lehto, M. Johansson, H. Saarinen, A. Radzikowska, C. Thiele, and V.M. Olkkonen The mammalian oxysterol-binding protein-related proteins (ORPs) bind 25-hydroxycholesterol in an evolutionarily conserved pocket Biochem. J. 405 2007 473 480 (Pubitemid 47172044)
50. P. Haberkant, O. Schmitt, F.X. Contreras, C. Thiele, K. Hanada, H. Sprong, C. Reinhard, F.T. Wieland, and B. Brügger Protein-sphingolipid interactions within cellular membranes J. Lipid Res. 49 2008 251 262
51. H.C. Kolb, M.G. Finn, and K.B. Sharpless Click Chemistry: Diverse Chemical Function from a Few Good Reactions Angew. Chem. Int. Ed. Engl. 40 2001 2004 2021
52. E. Saxon, and C.R. Bertozzi Cell surface engineering by a modified Staudinger reaction Science 287 2000 2007 2010 (Pubitemid 30158675)
53. V.V. Fokin Click imaging of biochemical processes in living systems ACS Chem. Biol. 2 2007 775 778 (Pubitemid 351166051)
54. N.J. Agard, J.A. Prescher, and C.R. Bertozzi A strain-promoted [3 + 2] azide-alkyne cycloaddition for covalent modification of biomolecules in living systems J. Am. Chem. Soc. 126 2004 15046 15047 (Pubitemid 39557262)
55. J.M. Baskin, J.A. Prescher, S.T. Laughlin, N.J. Agard, P.V. Chang, I.A. Miller, A. Lo, J.A. Codelli, and C.R. Bertozzi Copper-free click chemistry for dynamic in vivo imaging Proc. Natl. Acad. Sci. U. S. A. 104 2007 16793 16797 (Pubitemid 350210944)
56. D.C. Kennedy, C.S. McKay, M.C. Legault, D.C. Danielson, J.A. Blake, A.F. Pegoraro, A. Stolow, Z. Mester, and J.P. Pezacki Cellular consequences of copper complexes used to catalyze bioorthogonal click reactions J. Am. Chem. Soc. 133 2011 17993 18001
57. C. Thiele, C. Papan, D. Hoelper, K. Kusserow, A. Gaebler, M. Schoene, K. Piotrowitz, D. Lohmann, J. Spandl, A. Stevanovic, A. Shevchenko, and L. Kuerschner Tracing fatty acid metabolism by click chemistry ACS Chem. Biol. 7 2012 2004 2011
58. K. Hofmann, C. Thiele, H.F. Schott, A. Gaebler, M. Schoene, Y. Kiver, S. Friedrichs, D. Lutjohann, L. Kuerschner, A novel alkyne cholesterol to trace cellular cholesterol metabolism and localization, J. Lipid Res., http://dx.doi.org/10.1194/jlr.D044727.
59. S.B. Milne, K.A. Tallman, R. Serwa, C.A. Rouzer, M.D. Armstrong, L.J. Marnett, C.M. Lukehart, N.A. Porter, and H.A. Brown Capture and release of alkyne-derivatized glycerophospholipids using cobalt chemistry Nat. Chem. Biol. 6 2010 205 207
60. A. Gaebler, R. Milan, L. Straub, D. Hoelper, L. Kuerschner, and C. Thiele Alkyne lipids as substrates for click chemistry-based in vitro enzymatic assays J. Lipid Res. 54 2013 2282 2290
61. A.B. Neef, and C. Schultz Selective fluorescence labeling of lipids in living cells Angew. Chem. Int. Ed. Engl. 48 2009 1498 1500
62. R.G. R.J. Bridges The incorporation of analogues of choline into the phospholipids of the larva of the housefly, Musca domestica J. Insect Physiol. 16 1969 579 593
63. E. D.W. Hodgson The nutrition of choline, carnitine, and related compounds in the blowfly, Phormia regina Meigen J. Insect Physiol. 10 1964 1005 1008
64. C.Y. Jao, M. Roth, R. Welti, and A. Salic Metabolic labeling and direct imaging of choline phospholipids in vivo Proc. Natl. Acad. Sci. U. S. A. 106 2009 15332 15337
65. R.N. Hannoush, and J. Sun The chemical toolbox for monitoring protein fatty acylation and prenylation Nat. Chem. Biol. 6 2010 498 506
66. E.W. Tate Recent advances in chemical proteomics: exploring the post-translational proteome J. Chem. Biol. 1 2008 17 26
67. R.N. Hannoush, and N. Arenas-Ramirez Imaging the lipidome: omega-alkynyl fatty acids for detection and cellular visualization of lipid-modified proteins ACS Chem. Biol. 4 2009 581 587
68. W.P. Heal, B. Jovanovic, S. Bessin, M.H. Wright, A.I. Magee, and E.W. Tate Bioorthogonal chemical tagging of protein cholesterylation in living cells Chem. Commun. (Camb.) 47 2011 4081 4083
69. H.C. Hang, E.J. Geutjes, G. Grotenbreg, A.M. Pollington, M.J. Bijlmakers, and H.L. Ploegh Chemical probes for the rapid detection of Fatty-acylated proteins in Mammalian cells J. Am. Chem. Soc. 129 2007 2744 2745 (Pubitemid 46417937)
70. W.P. Heal, S.R. Wickramasinghe, R.J. Leatherbarrow, and E.W. Tate N-Myristoyl transferase-mediated protein labelling in vivo Org. Biomol. Chem. 6 2008 2308 2315 (Pubitemid 351852834)
71. B.R. Martin, and B.F. Cravatt Large-scale profiling of protein palmitoylation in mammalian cells Nat. Methods 6 2009 135 138
72. B.R. Martin, C. Wang, A. Adibekian, S.E. Tully, and B.F. Cravatt Global profiling of dynamic protein palmitoylation Nat. Methods 9 2011 84 89
73. T. Hosoya, T. Hiramatsu, T. Ikemoto, M. Nakanishi, H. Aoyama, A. Hosoya, T. Iwata, K. Maruyama, M. Endo, and M. Suzuki Novel bifunctional probe for radioisotope-free photoaffinity labeling: compact structure comprised of photospecific ligand ligation and detectable tag anchoring units Org. Biomol. Chem. 2 2004 637 641
74. J. Gubbens, E. Ruijter, L.E. de Fays, J.M. Damen, B. de Kruijff, M. Slijper, D.T. Rijkers, R.M. Liskamp, and A.I. de Kroon Photocrosslinking and click chemistry enable the specific detection of proteins interacting with phospholipids at the membrane interface Chem. Biol. 16 2009 3 14
75. J. Gubbens, and A.I. de Kroon Proteome-wide detection of phospholipid-protein interactions in mitochondria by photocrosslinking and click chemistry Mol. Biosyst. 6 2010 1751 1759
76. J.J. Hulce, A.B. Cognetta, M.J. Niphakis, S.E. Tully, and B.F. Cravatt Proteome-wide mapping of cholesterol-interacting proteins in mammalian cells Nat. Methods 10 2013 259 264
77. P. Haberkant, R. Raijmakers, M. Wildwater, T. Sachsenheimer, B. Brugger, K. Maeda, M. Houweling, A.C. Gavin, C. Schultz, G. van Meer, A.J. Heck, and J.C. Holthuis In vivo profiling and visualization of cellular protein-lipid interactions using bifunctional fatty acids Angew. Chem. Int. Ed. Engl. 52 2013 4033 4038
78. J.C. Cruz, M. Thomas, E. Wong, N. Ohgami, S. Sugii, T. Curphey, C.C. Chang, and T.Y. Chang Synthesis and biochemical properties of a new photoactivatable cholesterol analog 7,7-azocholestanol and its linoleate ester in Chinese hamster ovary cell lines J. Lipid Res. 43 2002 1341 1347 (Pubitemid 34988182)