A comparative study on fluorescent cholesterol analogs as versatile cellular reporters

Journal of Lipid Research

Volumn 57, Issue 2, 2016, Pages 299-309

  Sezgin, Erdinc ^a   Can, Fatma Betul ^a   Schneider, Falk ^a   Clausen, Mathias P ^a,b   Galiani, Silvia ^a   Stanly, Tess A ^a   Waithe, Dominic ^a   Colaco, Alexandria ^c   Honigmann, Alf ^d   Wüstner, Daniel ^b   Platt, Frances ^c   Eggeling, Christian ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

Author keywords

Cholesterol metabolism; Cholesterol trafficking; Fluorescence correlation spectroscopy; Fluorescence microscopy; Giant plasma membrane vesicles; Giant unilamellar vesicles; Lipid rafts; Membranes model; Niemann Pick type C disease; Stimulated emission depletion

Indexed keywords

CHOLESTEROL DERIVATIVE; FLUORESCENT DYE; CHOLESTEROL; LIPID BILAYER; LIPOSOME;

ARTICLE; CELL INTERACTION; CELL MEMBRANE; CELL MIGRATION; CELLULAR DISTRIBUTION; CHOLESTEROL TRANSPORT; COMPARATIVE STUDY; CONTROLLED STUDY; DIFFUSION; FLUORESCENCE CORRELATION SPECTROSCOPY; MEMBRANE VESICLE; NIEMANN PICK DISEASE; PRIORITY JOURNAL; ANALOGS AND DERIVATIVES; CHEMISTRY; FLUORESCENCE; HUMAN; LIPID BILAYER; METABOLISM; SPECTROFLUOROMETRY;

CELL MEMBRANE; CHOLESTEROL; FLUORESCENCE; FLUORESCENT DYES; HUMANS; LIPID BILAYERS; SPECTROMETRY, FLUORESCENCE; UNILAMELLAR LIPOSOMES;

EID: 84964780777     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M065326     Document Type: Article

References (80)

1. Maxfield , F. R. , and I. Tabas . 2005 . Role of cholesterol and lipid organization in disease. Nature . 438 : 612 - 621 .
2. Simons , K. , and E. Ikonen . 1997 . Functional rafts in cell membranes. Nature . 387 : 569 - 572 .
3. Edwards , P. A. , and J. Ericsson . 1999 . Sterols and isoprenoids: signaling molecules derived from the cholesterol biosynthetic pathway. Annu. Rev. Biochem. 68 : 157 - 185 .
4. Furuchi , T. , and R. G. W. Anderson . 1998 . Cholesterol depletion of caveolae causes hyperactivation of extracellular signal-related kinase (ERK). J. Biol. Chem. 273 : 21099 - 21104 .
5. Lewis , P. M. , M. P. Dunn , J. A. McMahon , M. Logan , J. F. Martin , B. St-Jacques , and A. P. McMahon . 2001 . Cholesterol modification of sonic hedgehog is required for long-range signaling activity and effective modulation of signaling by Ptc1. Cell . 105 : 599 - 612 .
6. Porter , J. A. , K. E. Young , and P. A. Beachy . 1996 . Cholesterol modification of hedgehog signaling proteins in animal development. Science . 274 : 255 - 259 .
7. Silvius , J. R. 2003 . Role of cholesterol in lipid raft formation: lessons from lipid model systems. Biochim. Biophys. Acta . 1610 : 174 - 183 .
8. Schroeder , F., H. Huang A. L. McIntosh , B. P. Atshaves , G. G. Martin , and A. B. Kier . 2010 . Caveolin, sterol carrier protein-2, membrane cholesterol-rich microdomains and intracellular cholesterol trafficking. Subcell. Biochem. 51: 279 - 318 .
9. Mizuno , H. , M. Abe , P. Dedecker , A. Makino , S. Rocha , Y. Ohno-Iwashita , J. Hofkens , T. Kobayashi , and A. Miyawaki . 2011 . Fluorescent probes for superresolution imaging of lipid domains on the plasma membrane. Chem. Sci. 2 : 1548 - 1553 .
10. Pourmousa , M. , T. Rog , R. Mikkeli , I. Vattulainen , L. M. Solanko , D. Wustner , N. H. List , J. Kongsted , and M. Karttunen . 2014 . Dehydroergosterol as an analogue for cholesterol: why it mimics cholesterol so well-or does it? J. Phys. Chem. B . 118 : 7345 - 7357 .
11. Robalo , J. R. , A. M. T. Martins do Canto , A. J. Palace Carvalho , J. P. Prates Ramalho , and L. M. S. Loura . 2013 . Behavior of fluorescent cholesterol analogues dehydroergosterol and cholestatrienol in lipid bilayers: a molecular dynamics study. J. Phys. Chem. B . 117 : 5806 - 5819 .
12. Gimpl , G. , and K. Gehrig-Burger . 2007 . Cholesterol reporter molecules. Biosci. Rep. 27 : 335 - 358 .
13. Arthur , J. R. , K. A. Heinecke , and T. N. Seyfried . 2011 . Filipin recognizes both GM1 and cholesterol in GM1 gangliosidosis mouse brain. J. Lipid Res. 52 : 1345 - 1351 .
14. Tserentsoodol , N. , J. Sztein , M. Campos , N. V. Gordiyenko , R. N. Fariss , J. W. Lee , S. J. Fliesler , and I. R. Rodriguez . 2006 . Uptake of cholesterol by the retina occurs primarily via a low density lipoprotein receptor-mediated process. Mol. Vis. 12 : 1306 - 1318 .
15. Albert , A. D. , J. E. Young , and P. L. Yeagle . 1996 . Rhodopsincholesterol interactions in bovine rod outer segment disk membranes. Biochim. Biophys. Acta . 1285 : 47 - 55 .
16. Yeagle , P. L. , A. D. Albert , K. Boeszebattaglia , J. Young , and J. Frye . 1990 . Cholesterol dynamics in membranes. Biophys. J. 57 : 413 - 424 .
17. John , K. , J. Kubelt , P. Muller , D. Wustner , and A. Herrmann . 2002 . Rapid transbilayer movement of the fluorescent sterol dehydroergosterol in lipid membranes. Biophys. J. 83 : 1525 - 1534 .
18. Mukherjee , S. , X. H. Zha , I. Tabas , and F. R. Maxfield . 1998 . Cholesterol distribution in living cells: Fluorescence imaging using dehydroergosterol as a fluorescent cholesterol analog. Biophys. J. 75 : 1915 - 1925 .
19. Garvik , O. , P. Benediktson , A. C. Simonsen , J. H. Ipsen , and D. Wustner . 2009 . The fluorescent cholesterol analog dehydroergosterol induces liquid-ordered domains in model membranes. Chem. Phys. Lipids . 159 : 114 - 118 .
20. Wüstner , D. 2008 . Free-cholesterol loading does not trigger phase separation of the fluorescent sterol dehydroergosterol in the plasma membrane of macrophages. Chem. Phys. Lipids . 154 : 129 - 136 .
21. Wüstner , D. , L. Solanko , E. Sokol , O. Garvik , Z. Li , R. Bittman , T. Korte , and A. Herrmann . 2011 . Quantitative assessment of sterol traffic in living cells by dual labeling with dehydroergosterol and BODIPY-cholesterol. Chem. Phys. Lipids . 164 : 221 - 235 .
22. Wüstner , D. , and K. Solanko . 2015 . How cholesterol interacts with proteins and lipids during its intracellular transport. Biochim. Biophys. Acta . 1848 : 1908 - 1926 .
23. Wüstner , D. 2007 . Fluorescent sterols as tools in membrane biophysics and cell biology. Chem. Phys. Lipids . 146 : 1 - 25 .
24. Boldyrev , I. A. , X. H. Zhai , M. M. Momsen , H. L. Brockman , R. E. Brown , and J. G. Molotkovsky . 2007 . New BODIPY lipid probes for fluorescence studies of membranes. J. Lipid Res. 48 : 1518 - 1532 .
25. Ramirez , D. M. , W. W. Ogilvie , and L. J. Johnston . 2010 . NBDcholesterol probes to track cholesterol distribution in model membranes. Biochim. Biophys. Acta . 1798 : 558 - 568 .
26. Ariola , F. S. , Z. Li , C. Cornejo , R. Bittman , and A. A. Heikal . 2009 . Membrane fluidity and lipid order in ternary giant unilamellar vesicles using a new bodipy-cholesterol derivative. Biophys. J. 96 : 2696 - 2708 .
27. Honigmann , A. , V. Mueller , S. W. Hell , and C. Eggeling . 2013 . STED microscopy detects and quantifies liquid phase separation in lipid membranes using a new far-red emitting fluorescent phosphoglycerolipid analogue. Faraday Discuss. 161 : 77 - 89 .
28. Sezgin , E. , I. Levental , M. Grzybek , G. Schwarzmann , V. Mueller , A. Honigmann , V. N. Belov , C. Eggeling , U. Coskun , K. Simons , et al . 2012 . Partitioning, diffusion, and ligand binding of raft lipid analogs in model and cellular plasma membranes. Biochim. Biophys. Acta . 1818 : 1777 - 1784 .
29. García-Sáez , A. J. , D. C. Carrer , and P. Schwille . 2010 . Fluorescence correlation spectroscopy for the study of membrane dynamics and organization in giant unilamellar vesicles. Methods Mol. Biol . 606 : 493 - 508 .
30. Clausen , M. P. , E. Sezgin , J. Bernardino de la Serna , D. Waithe , B. C. Lagerholm , and C. Eggeling . 2015 . A straightforward approach for gated STED-FCS to investigate lipid membrane dynamics. Methods . 88 : 67 - 75 .
31. Sezgin , E. , H-J. Kaiser , T. Baumgart , P. Schwille , K. Simons , and I. Levental . 2012 . Elucidating membrane structure and protein behavior using giant plasma membrane vesicles. Nat. Protoc. 7 : 1042 - 1051 .
32. Levental , I. , D. Lingwood , M. Grzybek , U. Coskun , and K. Simons . 2010 . Palmitoylation regulates raft affinity for the majority of integral raft proteins. Proc. Natl. Acad. Sci. USA . 107 : 22050 - 22054 .
33. Adler , J. , and I. Parmryd . 2010 . Quantifying colocalization by correlation: the Pearson correlation coefficient is superior to the Mander's overlap coefficient. Cytometry A . 77 : 733 - 742 .
34. Clausen , M. P. , S. Galiani , J. B. de la Serna , M. Fritzsche , J. Chojnacki , K. Gehmlich , B. C. Lagerholm , and C. Eggeling . 2013 . Pathways to optical STED microscopy. NanoBioImaging . 1 : 1 - 12 .
35. Waithe , D. , M. P. Clausen , E. Sezgin , and C. Eggeling . FoCuS-point: software for STED fluorescence correlation and time-gated single photon counting. Bioinformatics . Epub ahead of print. November 20, 2015; doi:10.1093/bioinformatics/btv687.
36. Sezgin , E. , and P. Schwille . 2011 . Fluorescence techniques to study lipid dynamics. Cold Spring Harb. Perspect. Biol. 3 : a009803 .
37. Eggeling , C. , C. Ringemann , R. Medda , G. Schwarzmann , K. Sandhoff , S. Polyakova , V. N. Belov , B. Hein , C. von Middendorff , A. Schonle , et al . 2009 . Direct observation of the nanoscale dynamics of membrane lipids in a living cell. Nature . 457 : 1159 - 1162 .
38. Ringemann , C. , B. Harke , C. von Middendorff , R. Medda , A. Honigmann , R. Wagner , M. Leutenegger , A. Schönle , S. Hell , and C. Eggeling . 2009 . Exploring single-molecule dynamics with fluorescence nanoscopy. New J. Phys. 11 : 103054 .
39. Gimpl , G. , and K. Gehrig-Burger . 2011 . Probes for studying cholesterol binding and cell biology. Steroids . 76 : 216 - 231 .
40. Huang , H. , A. L. McIntosh , B. P. Atshaves , Y. Ohno-Iwashita , A. B. Kier , and F. Schroeder . 2010 . Use of dansyl-cholestanol as a probe of cholesterol behavior in membranes of living cells. J. Lipid Res. 51 : 1157 - 1172 .
41. Ohvo-Rekilä , H. , B. Akerlund , and J. P. Slotte . 2000 . Cyclodextrincatalyzed extraction of fluorescent sterols from monolayer membranes and small unilamellar vesicles. Chem. Phys. Lipids . 105 : 167 - 178 .
42. Honigmann , A. , V. Mueller , H. Ta , A. Schoenle , E. Sezgin , S. W. Hell , and C. Eggeling . 2014 . Scanning STED-FCS reveals spatiotemporal heterogeneity of lipid interaction in the plasma membrane of living cells. Nat. Commun. 5 : 5412 .
43. Sheng , R. , Y. Chen , H. Yung Gee , E. Stec , H. R. Melowic , N. R. Blatner , M. P. Tun , Y. Kim , M. Kallberg , T. K. Fujiwara , et al . 2012 . Cholesterol modulates cell signaling and protein networking by specifically interacting with PDZ domain-containing scaffold proteins. Nat. Commun. 3 : 1249 .
44. Bagatolli , L. A. , S. A. Sanchez , T. Hazlett , and E. Gratton . 2003 . Giant vesicles, Laurdan, and two-photon fluorescence microscopy: evidence of lipid lateral separation in bilayers. Methods Enzymol. 360 : 481 - 500 .
45. Dietrich , C. , L. A. Bagatolli , Z. N. Volovyk , N. L. Thompson , M. Levi , K. Jacobson , and E. Gratton . 2001 . Lipid rafts reconstituted in model membranes. Biophys. J. 80 : 1417 - 1428 .
46. Sezgin , E. , and P. Schwille . 2012 . Model membrane platforms to study protein-membrane interactions. Mol. Membr. Biol. 29 : 144 - 154 .
47. Klotzsch , E. , and G. J. Schuetz . 2013 . A critical survey of methods to detect plasma membrane rafts. Philos. Trans. R. Soc. Lond. B Biol. Sci. 368 : 20120033 .
48. Lozano , M. M. , Z. Liu , E. Sunnick , A. Janshoff , K. Kumar , and S. G. Boxer . 2013 . Colocalization of the ganglioside G(M1) and cholesterol detected by secondary ion mass spectrometry. J. Am. Chem. Soc. 135 : 5620 - 5630 .
49. Frisz , J. F. , H. A. Klitzing , K. Lou , I. D. Hutcheon , P. K. Weber , J. Zimmerberg , and M. L. Kraft . 2013 . Sphingolipid domains in the plasma membranes of fibroblasts are not enriched with cholesterol. J. Biol. Chem. 288 : 16855 - 16861 .
50. Sezgin , E. , T. Sadowski , and K. Simons . 2014 . Measuring lipid packing of model and cellular membranes with environment sensitive probes. Langmuir . 30 : 8160 - 8166 .
51. Sezgin , E. , T. Gutmann , T. Buhl , R. Dirkx , M. Grzybek , U. Coskun , M. Solimena , K. Simons , I. Levental , and P. Schwille . 2015 . Adaptive lipid packing and bioactivity in membrane domains. PLoS One . 10 : e0123930 .
52. Baumgart , T. , G. Hunt , E. R. Farkas , W. W. Webb , and G. W. Feigenson . 2007 . Fluorescence probe partitioning between L-o/L-d phases in lipid membranes. Biochim. Biophys. Acta . 1768 : 2182 - 2194 .
53. Kaiser , H. J. , D. Lingwood , I. Levental , J. L. Sampaio , L. Kalvodova , L. Rajendran , and K. Simons . 2009 . Order of lipid phases in model and plasma membranes. Proc. Natl. Acad. Sci. USA . 106 : 16645 - 16650 .
54. Loura , L. M. S. , A. Fedorov , and M. Prieto . 2001 . Exclusion of a cholesterol analog from the cholesterol-rich phase in model membranes. Biochim. Biophys. Acta . 1511 : 236 - 243 .
55. Sevcsik , E. , M. Brameshuber , M. Folser , J. Weghuber , A. Honigmann , and G. J. Schutz . 2015 . GPI-anchored proteins do not reside in ordered domains in the live cell plasma membrane. Nat. Commun. 6 : 6969 .
56. Scheidt , H. A. , P. Muller , A. Herrmann , and D. Huster . 2003 . The potential of fluorescent and spin-labeled steroid analogs to mimic natural cholesterol. J. Biol. Chem. 278 : 45563 - 45569 .
57. Kaiser , R. D. , and E. London . 1998 . Determination of the depth of BODIPY probes in model membranes by parallax analysis of fluorescence quenching. Biochim. Biophys. Acta . 1375 : 13 - 22 .
58. Vanier , M. T. 2015 . Complex lipid trafficking in Niemann-Pick disease type C. J. Inherit. Metab. Dis. 38 : 187 - 199 .
59. Platt , F. M. , C. Wassif , A. Colaco , A. Dardis , E. Lloyd-Evans , B. Bembi , and F. D. Porter . 2014 . Disorders of cholesterol metabolism and their unanticipated convergent mechanisms of disease. Annu. Rev. Genomics Hum. Genet. 15 : 173 - 194 .
60. Peake , K. B. , and J. E. Vance . 2010 . Defective cholesterol trafficking in Niemann-Pick C-deficient cells. FEBS Lett. 584 : 2731 - 2739 .
61. Cruz , J. C. , and T. Y. Chang . 2000 . Fate of endogenously synthesized cholesterol in Niemann-Pick type C1 cells. J. Biol. Chem. 275 : 41309 - 41316 .
62. Pipalia , N. H. , M. Hao , S. Mukherjee , and F. R. Maxfield . 2007 . Sterol, protein and lipid trafficking in Chinese hamster ovary cells with Niemann-Pick type C1 defect. Traffic . 8 : 130 - 141 .
63. Hölttä-Vuori , M. , R. L. Uronen , J. Repakova , E. Salonen , I. Vattulainen , P. Panula , Z. G. Li , R. Bittman , and E. Ikonen . 2008 . BODIPY-cholesterol: a new tool to visualize sterol trafficking in living cells and organisms. Traffic . 9 : 1839 - 1849 .
64. Manson , M. E. , D. A. Corey , I. Bederman , J. D. Burgess , and T. J. Kelley . 2012 . Regulatory role of beta-arrestin-2 in cholesterol processing in cystic fibrosis epithelial cells. J. Lipid Res. 53 : 1268 - 1276 .
65. Du , X. , J. Kumar , C. Ferguson , T. A. Schulz , Y. S. Ong , W. Hong , W. A. Prinz , R. G. Parton , A. J. Brown , and H. Yang . 2011 . A role for oxysterol-binding protein-related protein 5 in endosomal cholesterol trafficking. J. Cell Biol. 192 : 121 - 135 .
66. Lee , H. J. , W. Zhang , D. Zhang , Y. Yang , B. Liu , E. L. Barker , K. K. Buhman , L. V. Slipchenko , M. Dai , and J-X. Cheng . 2015 . Assessing cholesterol storage in live cells and C. elegans by stimulated Raman scattering imaging of phenyl-diyne cholesterol. Sci. Rep. 5 : 7930 .
67. Hao , M. , S. X. Lin , O. J. Karylowski , D. Wüstner , T. E. McGraw , and F. R. Maxfield . 2002 . Vesicular and non-vesicular sterol transport in living cells - The endocytic recycling compartment is a major sterol storage organelle. J. Biol. Chem. 277 : 609 - 617 .
68. Wüstner , D. , F. W. Lund , C. Röhrl , and H. Stangl . Potential of BODIPY-cholesterol for analysis of cholesterol transport and diffusion in living cells. Chem. Phys. Lipids . Epub ahead of print. August 17, 2015; doi:10.1016/j.chemphyslip.2015.08.007.
69. Mondal , M. , B. Mesmin , S. Mukherjee , and F. R. Maxfield . 2009 . Sterols are mainly in the cytoplasmic leaflet of the plasma membrane and the endocytic recycling compartment in CHO cells. Mol. Biol. Cell . 20 : 581 - 588 .
70. Milles , S. , T. Meyer , H. A. Scheidt , R. Schwarzer , L. Thomas , M. Marek , L. Szente , R. Bittman , A. Herrmann , T. G. Pomorski , et al . 2013 . Organization of fluorescent cholesterol analogs in lipid bilayers - Lessons from cyclodextrin extraction. Biochim. Biophys. Acta . 1828 : 1822 - 1828 .
71. Bacia , K. , D. Scherfeld , N. Kahya , and P. Schwille . 2004 . Fluorescence correlation spectroscopy relates rafts in model and native membranes. Biophys. J. 87 : 1034 - 1043 .
72. Mueller , V. , C. Ringemann , A. Honigmann , G. Schwarzmann , R. Medda , M. Leutenegger , S. Polyakova , V. N. Belov , S. W. Hell , and C. Eggeling . 2011 . STED nanoscopy reveals molecular details of cholesterol- and cytoskeleton-modulated lipid interactions in living cells. Biophys. J. 101 : 1651 - 1660 .
73. Vicidomini , G. , H. Ta , A. Honigmann , V. Mueller , M. P. Clausen , D. Waithe , S. Galiani , E. Sezgin , A. Diaspro , S. W. Hell , et al . 2015 . STED-FLCS: an advanced tool to reveal spatiotemporal heterogeneity of molecular membrane dynamics. Nano Lett. 15 : 5912 - 5918 .
74. Magde , D. , E. L. Elson , and W. W. Webb . 1974 . Fluorescence correlation spectroscopy. II. An experimental realization. Biopolymers . 13 : 29 - 61 .
75. Eggeling , C. , J. Widengren , R. Rigler , and C. A. Seidel . 1998 . Photobleaching of fluorescent dyes under conditions used for single-molecule detection: evidence of two-step photolysis. Anal. Chem. 70 : 2651 - 2659 .
76. Solanko , L. M. , A. Honigmann , H. S. Midtiby , F. W. Lund , J. R. Brewer , V. Dekaris , R. Bittman , C. Eggeling , and D. Wustner . 2013 . Membrane orientation and lateral diffusion of BODIPY-cholesterol as a function of probe structure. Biophys. J. 105 : 2082 - 2092 .
77. Hell , S. W. , and J. Wichmann . 1994 . Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy. Opt. Lett. 19 : 780 - 782 .
78. Eggeling , C. 2015 . Super-resolution optical microscopy of lipid plasma membrane dynamics. Essays Biochem. 57 : 69 - 80 .
79. Eggeling , C. , K. I. Willig , S. J. Sahl , and S. W. Hell . 2015 . Lens-based fluorescence nanoscopy. Q. Rev. Biophys. 48 : 178 - 243 .
80. Maxfield , F. R. , and D. Wüstner . 2012 . Analysis of cholesterol trafficking with fluorescent probes. In Lipids. Vol. 108. G. DiPaolo and M. R. Wenk, editors. 367-393.