Fluorescent sterols and cholesteryl esters as probes for intracellular cholesterol transport

Lipid Insights

Volumn 2015, Issue , 2015, Pages 95-114

  Solanko, Katarzyna A ^a   Modzel, Maciej ^a   Solanko, Lukasz M ^a   Wüstner, Daniel ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

Endocytosis; Fluorescent sterols; Imaging; Metabolism; Optical microscopy; Sterol trafficking

Indexed keywords

6 DANSYLCHOLESTEROL; CHOLESTATRIENOL; CHOLESTATRIENOL LINOLEATE; CHOLESTATRIENOL OLEATE; CHOLESTEROL; CHOLESTEROL DERIVATIVE; CHOLESTEROL ESTER; DEHYDROERGOSTEROL; ERGOSTEROL; FILIPIN; LOW DENSITY LIPOPROTEIN; NYSTATIN; PARINARIC ACID; PYRENECHOLESTEROL; STEROL; UNCLASSIFIED DRUG;

ARTICLE; ARTIFICIAL MEMBRANE; CHOLESTEROL METABOLISM; CHOLESTEROL SYNTHESIS; CHOLESTEROL TRANSPORT; CLICK CHEMISTRY; DRUG SCREENING; ENDOCYTOSIS; FIBROBLAST; FLUORESCENCE; HUMAN; INTRACELLULAR TRANSPORT; NIEMANN PICK DISEASE; NONHUMAN;

EID: 85013356878     PISSN: None     EISSN: 11786353     Source Type: Journal    
DOI: 10.4137/Lpi.s31617     Document Type: Article

References (187)

1. Behrman EJ, Gopalan V. Cholesterol and plants. J Chem Educ. 2005;82:1791-1793.
2. Schroeder F, Barenholz Y, Gratton E, Thompson TE. A fluorescence study of dehydroergosterol in phosphatidylcholine bilayer vesicles. Biochemistry. 1987;26: 2441-2448.
3. Marrink SJ, de Vries AH, Harroun TA, Katsaras J, Wassall SR. Cholesterol shows preference for the interior of polyunsaturated lipid membranes. J Am Chem Soc. 2008;130:10-11.
4. Aittoniemi J, Róg T, Niemelä P, Pasenkiewicz-Gierula M, Karttunen M, Vattulainen I. Tilt: major factor in sterols' ordering capability in membranes. J Phys Chem B. 2006;110:25562-25564.
5. Mesmin B, Maxfield FR. Intracellular sterol dynamics. Biochim Biophys Acta. 2009;1791:636-645.
6. Wüstner D, Solanko KA. How cholesterol interacts with proteins and lipids during its intracellular transport. Biochim Biophys Acta. 2015;1848:2188-2199.
7. Goldstein JL, DeBose-Boyd RA, Brown MS. Protein sensors for membrane sterols. Cell. 2006;124:35-46.
8. Sharpe LJ, Cook ECL, Zelcer N, Brown AJ. The UPS and downs of cholesterol homeostasis. Trends Biochem Sci. 2014;39:527-535.
9. Lange Y, Ye J, Rigney M, Steck TL. Regulation of endoplasmic reticulum cholesterol by plasma membrane cholesterol. J Lipid Res. 1999;40:2264-2270.
10. van Meer G, Voelker DR, Feigenson GW. Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol. 2008;9:112-124.
11. Tabas I. Free cholesterol-induced cytotoxicity-a possible contributing factor to macrophage foam cell necrosis in advanced atherosclerotic lesions. Trends Cardiovasc Med. 1997;7:256-263.
12. Radhakrishnan A, Goldstein JL, McDonald JG, Brown MS. Switch-like control of SREBP-2 transport triggered by small changes in ER cholesterol: a delicate balance. Cell Metab. 2008;8:512-521.
13. Sokolov A, Radhakrishnan A. Accessibility of cholesterol in endoplasmic reticulum membranes and activation of SREBP-2 switch abruptly at a common cholesterol threshold. J Biol Chem. 2010;285:29480-29490.
14. Xu XX, Tabas I. Lipoproteins activate acyl-coenzyme A:cholesterol acyltransferase in macrophages only after cellular cholesterol pools are expanded to a critical threshold level. J Biol Chem. 1991;266:17040-17048.
15. Chang CCY, Chen J, Thomas MA, et al. Regulation and immunolocalization of Acyl-Coenzyme a-cholesterol acyltransferase in mammalian-cells as studied with specific antibodies. J Biol Chem. 1995;270:29532-29540.
16. Goldstein JL, Brown MS. The LDL receptor. Arterioscler Thromb Vasc Biol. 2009; 29:431-438.
17. Norata GD, Ballantyne CM, Catapano AL. New therapeutic principles in dyslipidaemia: focus on LDL and Lp(a) lowering drugs. Eur Heart J. 2013;34: 1783-1789.
18. Maxfield FR, Tabas I. Role of cholesterol and lipid organization in disease. Nature. 2005;438:612-621.
19. Mukherjee S, Maxfield FR. Lipid and cholesterol trafficking in NPC. Biochim Biophys Acta. 2004;1685:28-37.
20. Wang ML, Motamed M, Infante RE, et al. Identification of surface residues on Niemann-Pick C2 essential for hydrophobic handoff of cholesterol to NPC1 in lysosomes. Cell Metab. 2010;12:166-173.
21. Lloyd-Evans E, Platt FM. Lipids on trial: the search for the offending metabolite in Niemann Pick type C disease. Traffic. 2010;11:419-428.
22. Kruth HS, Comly ME, Butler JD, et al. Type C Niemann-Pick disease. Abnormal metabolism of low density lipoprotein in homozygous and heterozygous fibroblasts. J Biol Chem. 1986;261:16769-16774.
23. Pentchev PG, Comly ME, Kruth HS, et al. A defect in cholesterol esterification in Niemann-Pick disease (type C) patients. Proc Natl Acad Sci U S A. 1985; 82:8247-8251.
24. Storch J. Niemann-Pick C2 (NPC2) and intracellular cholesterol trafficking. Biochim Biophys Acta. 2009;1791:671-678.
25. Subramanian K, Balch WE. NPC1/NPC2 function as a tag team duo to mobilize cholesterol. Proc Natl Acad Sci U S A. 2008;105:15223-15224.
26. Gallala HD, Breiden B, Sandhoff K. Regulation of the NPC2 protein-mediated cholesterol trafficking by membrane lipids. J Neurochem. 2011;116:702-707.
27. McCauliff LA, Xu Z, Li R, et al. Multiple surface regions on the Niemann- Pick C2 protein facilitate intracellular cholesterol transport. J Biol Chem. 2015; 290(45):27321-27331.
28. Maekawa M, Fairn GD. Complementary probes reveal that phosphatidylserine is required for the proper transbilayer distribution of cholesterol. J Cell Sci. 2015;128:1422-1433.
29. Maxfield F, Wüstner D. Analysis of cholesterol trafficking with fluorescent probes. Methods Cell Biol. 2012;108:367-393.
30. Nagao T, Qin C, Grosheva I, Maxfield FR, Pierini LM. Elevated cholesterol levels in the plasma membranes of macrophages inhibit migration by disrupting RhoA regulation. Arterioscler Thromb Vasc Biol. 2007;27:1596-1602.
31. Pipalia NH, Huang A, Ralph H, Rujoi M, Maxfield FR. Automated microscopy screening for compounds that partially revert cholesterol accumulation in Niemann-Pick C cells. J Lipid Res. 2006;47:284-301.
32. Bartz F, Kern L, Erz D, et al. Identification of cholesterol-regulating genes by targeted RNAi screening. Cell Metab. 2009;10:63-75.
33. Ishitsuka R, Saito T, Osada H, Ohno-Iwashita Y, Kobayashi T. Fluorescence image screening for chemical compounds modifying cholesterol metabolism and distribution. J Lipid Res. 2011;52:2084-2094.
34. Möbius W, Ohno-Iwashita Y, van Donselaar EG, et al. Immunoelectron microscopic localization of cholesterol using biotinylated and non-cytolytic perfringolysin O. J Histochem Cytochem. 2002;50:43-55.
35. Orci L, Montesano R, Meda P, et al. Heterogeneous distribution of filipin- cholesterol complexes across the cisternae of the Golgi apparatus. Proc Natl Acad Sci U S A. 1981;78:293-297.
36. Severs NJ, Simons HL. Failure of filipin to detect cholesterol-rich domains in smooth muscle plasma membrane. Nature. 1983;303:637-638.
37. Behnke O, Tranum-Jensen J, van Deurs B. Filipin as a cholesterol probe. I. Morphology of filipin-cholesterol interaction in lipid model systems. Eur J Cell Biol. 1984;35:189-199.
38. Behnke O, Tranum-Jensen J, van Deurs B. Filipin as a cholesterol probe. II. Filipin-cholesterol interaction in red blood cell membranes. Eur J Cell Biol. 1984; 35:200-215.
39. Arthur JR, Heinecke KA, Seyfried TN. Filipin recognizes both GM1 and cholesterol in GM1 gangliosidosis mouse brain. J Lipid Res. 2011;52:1345-1351.
40. Smith RJ, Green C. The rate of cholesterol 'flip-flop' in lipid bilayers and its relation to membrane sterol pools. FEBS Lett. 1974;42:108-111.
41. Davenport L, Kutson JR, Brand L. Excited-state proton transfer of equilenin and dihydroequilenin: interaction with bilayer vesicles. Biochemistry. 1986;25:1186-1195.
42. Schroeder F. Fluorescent sterols-probe molecules of membrane-structure and function. Prog Lipid Res. 1984;23:97-113.
43. McIntosh AL, Atshaves BP, Huang H, Gallegos AM, Kier AB, Schroeder F. Fluorescence techniques using dehydroergosterol to study cholesterol trafficking. Lipids. 2008;43:1185-1208.
44. Ano Y, Kutsukake T, Hoshi A, Yoshida A, Nakayama H. Identification of a novel dehydroergosterol enhancing microglial anti-inflammatory activity in a dairy product fermented with Penicillium candidum. PLoS One. 2015;10:e0116598.
45. McIntosh AL, Gallegos AM, Atshaves BP, Storey SM, Kannoju D, Schroeder F. Fluorescence and multiphoton imaging resolve unique structural forms of sterol in membranes of living cells. J Biol Chem. 2003;278:6384-6403.
46. Kohut P, Wüstner D, Hronska L, Kuchler K, Hapala I, Valachovic M. The role of ABC proteins Aus1p and Pdr11p in the uptake of external sterols in yeast: dehydroergosterol fluorescence study. Biochem Biophys Res Commun. 2011;404: 233-238.
47. Georgiev AG, Sullivan DP, Kersting MC, Dittman JS, Beh CT, Menon AK. Osh proteins regulate membrane sterol organization but are not required for sterol movement between the ER and PM. Traffic. 2011;12:1341-1355.
48. Wüstner D, Mondal M, Tabas I, Maxfield FR. Direct observation of rapid internalization and intracellular transport of sterol by macrophage foam cells. Traffic. 2005;6:396-412.
49. Hölttä-Vuori M, Uronen RL, Repakova J, et al. BODIPY-cholesterol: a new tool to visualize sterol trafficking in living cells and organisms. Traffic. 2008;9: 1839-1849.
50. Liu J, Chang CC, Westover EJ, Covey DF, Chang TY. Investigating the allosterism of acyl-CoA:cholesterol acyltransferase (ACAT) by using various sterols: in vitro and intact cell studies. Biochem J. 2005;391:389-397.
51. Mesmin B, Pipalia NH, Lund FW, et al. STARD4 abundance regulates sterol transport and sensing. Mol Biol Cell. 2011;22:4004-4015.
52. Pourmousa M, Róg T, Mikkeli R, et al. Dehydroergosterol as an analogue for cholesterol: why it mimics cholesterol so well or does it? J Phys Chem. 2014;118: 7345-7357.
53. Scheidt HA, Müller P, Herrmann A, Huster D. The potential of fluorescent and spin-labeled steroid analogs to mimic natural cholesterol. J Biol Chem. 2003;278: 45563-45569.
54. Henriksen J, Rowat AC, Brief E, et al. Universal behavior of membranes with sterols. Biophys J. 2006;90:1639-1649.
55. 55. Arora A, Raghuraman H, Chattopadhyay A. Influence of cholesterol and ergosterol on membrane dynamics: a fluorescence approach. Biochem Biophys Res Commun. 2004;318:920-926.
56. Wüstner D, Herrmann A, Hao M, Maxfield FR. Rapid nonvesicular transport of sterol between the plasma membrane domains of polarized hepatic cells. J Biol Chem. 2002;277:30325-30336.
57. Smutzer G, Crawford BF, Yeagle PL. Physical properties of the fluorescent sterol probe dehydroergosterol. Biochim Biophys Acta. 1986;862:361-371.
58. Loura LM, Prieto M. Dehydroergosterol structural organization in aqueous medium and in a model system of membranes. Biophys J. 1997;72:2226-2236.
59. Harris JS, Epps DE, Davio SR, Kezdy FJ. Evidence for transbilayer, tail-to-tail cholesterol dimers in dipalmitoylglycerophosphocholine liposomes. Biochemistry. 1995;34:3851-3857.
60. Wüstner D. Fluorescent sterols as tools in membrane biophysics and cell biology. Chem Phys Lipids. 2007;146:1-25.
61. Frolov A, Petrescu A, Atshaves BP, et al. High density lipoprotein-mediated cholesterol uptake and targeting to lipid droplets in intact L-cell fibroblasts. J Biol Chem. 2000;275:12769-12780.
62. Wüstner D, Brewer JR, Bagatolli LA, Sage D. Potential of ultraviolet widefield imaging and multiphoton microscopy for analysis of dehydroergosterol in cellular membranes. Microsc Res Tech. 2011;74:92-108.
63. Wüstner D, Landt Larsen A, Færgeman NJ, Brewer JR, Sage D. Selective visualization of fluorescent sterols in Caenorhabditis elegans by bleach-rate based image segmentation. Traffic. 2010;11:440-454.
64. Zipfel WR, Williams RM, Webb WW. Nonlinear magic: multiphoton microscopy in the biosciences. Nat Biotechnol. 2003;21:1369-1377.
65. Luisier F, Vonesch C, Blu T, Unser M. Fast interscale wavelet denoising of Poisson-corrupted images. Signal Processing. 2010;90:415-427.
66. Gerstbrein B, Stamatas G, Kollias N, Driscoll M. In vivo spectrofluorimetry reveals endogenous biomarkers that report healthspan and dietary restriction in Caenorhabditis elegans. Aging Cell. 2005;4:127-137.
67. Wüstner D, Sage D. Multicolor bleach-rate imaging enlightens in vivo sterol transport. Commun Integr Biol. 2010;3:1-4.
68. Albro PW, Bilski P, Corbett JT, Schroeder JL, Chignell CF. Photochemical reactions and phototoxicity of sterols: novel self-perpetuating mechanisms for lipid photoxidation. Photochem Photobiol. 1997;66:316-325.
69. Windaus A, Deppe M, Roosen-Runge C. The pyro-vitamin D and its dehydroderivative. Liebigs Ann Chem. 1939;537:1-10.
70. Antonucci R, Bernstein S, Giancola D, Sax KJ. Delta-5, 7-steroids.7. The conversion of delta-5, 7-steroidal to delta-5, 7,9-steroidal hormones. J Org Chem. 1951; 16:1159-1164.
71. Fischer RT, Stephenson FA, Shafiee A, Schroeder F. Delta-5,7,9(11)- cholestatrien-3beta-Ol-a fluorescent cholesterol analog. Chem Phys Lipids. 1984; 36:1-14.
72. Wüstner D, Færgeman NJ. Spatiotemporal analysis of endocytosis and membrane distribution of fluorescent sterols in living cells. Histochem Cell Biol. 2008; 130:891-908.
73. Mondal M, Mesmin B, Mukherjee S, Maxfield FR. Sterols are mainly in the cytoplasmic leaflet of the plasma membrane and the endocytic recycling compartment in CHO cells. Mol Biol Cell. 2009;20:581-588.
74. Garvik O, Benediktson P, Simonsen AC, Ipsen JH, Wüstner D. The fluorescent cholesterol analog dehydroergosterol induces liquid-ordered domains in model membranes. Chem Phys Lipids. 2009;159:114-118.
75. Schroeder F, Dempsey ME, Fischer RT. Sterol and squalene carrier protein interactions with fluorescent delta-5,7,9(11)-cholestatrien-3-beta-Ol. J Biol Chem. 1985;260:2904-2911.
76. Schroeder F, Nemecz G, Gratton E, Barenholz Y, Thompson TE. Fluorescence properties of cholestatrienol in phosphatidylcholine bilayer vesicles. Biophys Chem. 1988;32:57-72.
77. Hyslop PA, Morel B, Sauerheber RD. Organization and interaction of cholesterol and phosphatidylcholine in model bilayer membranes. Biochemistry. 1990; 29:1025-1038.
78. Yeagle PL, Albert AD, Boesze-Battaglia K, Young J, Frye J. Cholesterol dynamics in membranes. Biophys J. 1990;57:413-424.
79. Robalo JR, do Canto AM, Carvalho AJ, Ramalho JP, Loura LM. Behavior of fluorescent cholesterol analogues dehydroergosterol and cholestatrienol in lipid bilayers: a molecular dynamics study. J Phys Chem B. 2013;117:5806-5819.
80. Nåbo LJ, List NH, Witzke S, Wüstner D, Khandelia H, Kongsted J. Design of new fluorescent cholesterol and ergosterol analogs: insights from theory. Biochim Biophys Acta. 2015;1848:2188-2199.
81. Yeagle PL, Bensen J, Boni L, Hui SW. Molecular packing of cholesterol in phospholipid vesicles as probed by dehydroergosterol. Biochim Biophys Acta. 1982;692: 139-146.
82. Chong PL, Thompson TE. Depolarization of dehydroergosterol in phospholipid bilayers. Biochim Biophys Acta. 1986;863:53-62.
83. Chong PL. Evidence for regular distribution of sterols in liquid crystalline phosphatidylcholine bilayers. Proc Natl Acad Sci U S A. 1994;91:10069-10073.
84. Ipsen JH, Karlstrom G, Mouritsen OG, Wennerstrom H, Zuckermann MJ. Phase equilibria in the phosphatidylcholine-cholesterol system. Biochim Biophys Acta. 1987;905:162-172.
85. Veatch SL, Keller SL. Separation of liquid phases in giant vesicles of ternary mixtures of phospholipids and cholesterol. Biophys J. 2003;85:3074-3083.
86. Baumgart T, Hunt G, Farkas ER, Webb WW, Feigenson GW. Fluorescence probe partitioning between Lo/Ld phases in lipid membranes. Biochim Biophys Acta. 2007;1768:2182-2194.
87. Sezgin E, Levental I, Grzybek M, et al. Partitioning, diffusion, and ligand binding of raft lipid analogs in model and cellular plasma membranes. Biochim Biophys Acta. 2012;1818:1777-1784.
88. Wüstner D, Solanko LM, Sokol E, et al. Quantitative assessment of sterol traffic in living cells by dual labeling with dehydroergosterol and BODIPY-cholesterol. Chem Phys Lipids. 2011;164:221-235.
89. Loura LMS, Fedorov A, Prieto M. Exclusion of a cholesterol analog from the cholesterol- rich phase in model membranes. Biochim Biophys Acta. 2001;1511:236-243.
90. Loura LMS, Fedorov A, Prieto M. Partition of membrane probes in a gel/fluid two-component lipid system: a fluorescence resonance energy transfer study. Biochim Biophys Acta. 2000;1467:101-112.
91. Wüstner D. Plasma membrane sterol distribution resembles the surface topography of living cells. Mol Biol Cell. 2007;18:211-228.
92. Wüstner D. Free-cholesterol loading does not trigger phase separation of the fluorescent sterol dehydroergosterol in the plasma membrane of macrophages. Chem Phys Lipids. 2008;154:129-136.
93. Anderton CR, Lou K, Weber PK, Hutcheon ID, Kraft ML. Correlated AFM and NanoSIMS imaging to probe cholesterol-induced changes in phase behavior and non-ideal mixing in ternary lipid membranes. Biochim Biophys Acta. 2011; 1808:307-315.
94. Frisz JF, Klitzing HA, Lou K, et al. Sphingolipid domains in the plasma membranes of fibroblasts are not enriched with cholesterol. J Biol Chem. 2013;288: 16855-16861.
95. Mayor S, Maxfield FR. Insolubility and redistribution of GPI-anchored proteins at the cell surface after detergent treatment. Mol Biol Cell. 1995;6:929-944.
96. Hao M, Mukherjee S, Maxfield FR. Cholesterol depletion induces large scale domain segregation in living cell membranes. Proc Natl Acad Sci U S A. 2001;98: 13072-13077.
97. Sezgin E, Betul Can F, Schneider F, et al. A comparative study on fluorescent cholesterol analogs as versatile cellular reporters. J Lipid Res. 2016;57(2):299-309.
98. Sezgin E, Kaiser HJ, Baumgart T, Schwille P, Simons K, Levental I. Elucidating membrane structure and protein behavior using giant plasma membrane vesicles. Nat Protoc. 2012;7:1042-1051.
99. Pagler TA, Wang M, Mondal M, et al. Deletion of ABCA1 and ABCG1 impairs macrophage migration because of increased Rac1 signaling. Circ Res. 2011;108: 194-200.
100. Wüstner D, Modzel M, Lund FW, Lomholt MA. Imaging approaches for analysis of cholesterol distribution and dynamics in the plasma membrane. Chem Phys Lipids. 2016. http://dx.doi.org/10.1016/j.chemphyslip.2016.03.003 101. Hartwig Petersen N, Færgeman NJ, Yu L, Wüstner D. Kinetic imaging of NPC1L1 and sterol trafficking between plasma membrane and recycling endosomes in hepatoma cells. J Lipid Res. 2008;49:2023-2037.
101. Xu Z, Farver W, Kodukula S, Storch J. Regulation of sterol transport between membranes and NPC2. Biochemistry. 2008;47:11134-11143.
102. Ngo M, Ridgway ND. Oxysterol binding protein-related protein 9 (ORP9) is a cholesterol transfer protein that regulates Golgi structure and function. Mol Biol Cell. 2009;20:1388-1399.
103. Iaea DB, Gale SE, Bielska AA, et al. A novel intrinsically fluorescent probe for study of uptake and trafficking of 25-hydroxycholesterol. J Lipid Res. 2015; 56(12):2408-2419.
104. Patel KM, Sklar LA, Currie R, Pownall HJ, Morrisett JD, Sparrow JT. Synthesis of saturated, unsaturated, spin-labeled, and fluorescent cholesteryl esters- acylation of cholesterol using fatty-acid anhydride and 4-pyrrolidinopyridine. Lipids. 1979;14:816-818.
105. Pattnaik NM, Montes A, Hughes LB, Zilversmit DB. Cholesteryl ester exchange protein in human-plasma isolation and characterization. Biochim Biophys Acta. 1978;530:428-438.
106. Krieger M, Brown MS, Faust JR, Goldstein JL. Replacement of endogenous cholesteryl esters of low-density lipoprotein with exogenous cholesteryl linoleate-reconstitution of a biologically-active lipoprotein particle. J Biol Chem. 1978;253:4093-4101.
107. Smith RJ, Green C. Fluorescence studies of protein-sterol relationships in human plasma lipoproteins. Biochem J. 1974;137:413-415.
108. Sklar LA, Craig IF, Pownall HJ. Induced circular-dichroism of incorporated fluorescent cholesteryl esters and polar lipids as a probe of human-serum lowdensity lipoprotein structure and melting. J Biol Chem. 1981;256:4286-4292.
109. Schroeder F, Goh EH, Heimberg M. Regulation of the surface physical properties of the very low density lipoprotein. J Biol Chem. 1979;254:2456-2463.
110. Sklar LA, Mantulin WW, Ponwall HJ. Fluorescent cholesteryl esters in the core of low density lipoprotein. Biochem Biophys Res Commun. 1982;105:674-680.
111. Riley JP. The seed fat of parinarium laurinum.1. Component acids of the seed fat. J Chem Soc. 1950:12-18.
112. Lee SJ, Gray KC, Paek JS, Burke MD. Simple, efficient, and modular syntheses of polyene natural products via iterative cross-coupling. J Am Chem Soc. 2008;130: 466-468.
113. Sklar LA, Hudson BS, Simoni RD. Conjugated polyene fatty-acids as membrane probes-preliminary characterization. Proc Natl Acad Sci U S A. 1975;72: 1649-1653.
114. Sklar LA, Hudson BS, Simoni RD. Conjugated polyene fatty-acids as fluorescentprobes- synthetic phospholipid membrane studies. Biochemistry. 1977;16: 819-828.
115. Benyashar V, Barenholz Y. Characterization of the core and surface of human plasma-lipoproteins-a study based on the use of 5 fluorophores. Chem Phys Lipids. 1991;60:1-14.
116. Sibarita JB. Deconvolution microscopy. Adv Biochem Eng Biotechnol. 2005;95: 201-243.
117. Heintzmann R. Estimating missing information by maximum likelihood deconvolution. Micron. 2007;38:136-144.
118. Kirshner H, Aguet F, Sage D, Unser M. 3-D PSF fitting for fluorescence microscopy: implementation and localization application. J Microsc. 2013;249: 13-25.
119. Bertero M, Boccacci P. Super-resolution in computational imaging. Micron. 2003;34:265-273.
120. Stelzer EHK. Contrast, resolution, pixelation, dynamic range and signal-tonoise ratio: fundamental limits to resolution in fluorescence light microscopy. J Microsc. 1998;189:15-24.
121. Wustner D, Christensen T, Solanko LM, Sage D. Photobleaching kinetics and time-integrated emission of fluorescent probes in cellular membranes. Molecules. 2014;19:11096-11130.
122. Marks DL, Bittman R, Pagano RE. Use of Bodipy-labeled sphingolipid and cholesterol analogs to examine membrane microdomains in cells. Histochem Cell Biol. 2008;130:819-832.
123. Li ZG, Mintzer E, Bittman R. First synthesis of free cholesterol-BODIPY conjugates. J Org Chem. 2006;71:1718-1721.
124. Wüstner D, Lund FW, Röhrl C, Stangl H. Potential of BODIPY-cholesterol for analysis of cholesterol transport and diffusion in living cells. Chem Phys Lipids. 2016;194:12-28.
125. Liu Z, Thacker SG, Fernandez-Castillejo S, Neufeld EB, Remaley AT, Bittman R. Synthesis of cholesterol analogues bearing BODIPY fluorophores by Suzuki or Liebeskind-Srogl cross-coupling and evaluation of their potential for visualization of cholesterol pools. Chembiochem. 2014;15:2087-2096.
126. Shaw JE, Epand RF, Epand RM, Li Z, Bittman R, Yip CM. Correlated fluorescence-atomic force microscopy of membrane domains: structure of fluorescence probes determines lipid localization. Biophys J. 2006;90:2170-2178.
127. Solanko LM, Honigmann A, Midtiby HS, et al. Membrane orientation and lateral diffusion of BODIPY-cholesterol as a function of probe structure. Biophys J. 2013;105:2082-2092.
128. Lund FW, Lomholt MA, Solanko LM, Bittman R, Wüstner D. Two-photon time-lapse microscopy of BODIPY-cholesterol reveals anomalous sterol diffusion in Chinese hamster ovary cells. BMC Biophys. 2012;5:20.
129. Hiramoto-Yamaki N, Tanaka KA, Suzuki KG, et al. Ultrafast diffusion of a fluorescent cholesterol analog in compartmentalized plasma membranes. Traffic. 2014;15(6):583-612.
130. Honigmann A, Mueller V, Ta H, et al. Scanning STED-FCS reveals spatiotemporal heterogeneity of lipid interaction in the plasma membrane of living cells. Nat Commun. 2014;5:5412.
131. Sevcsik E, Brameshuber M, Folser M, Weghuber J, Honigmann A, Schutz GJ. GPI-anchored proteins do not reside in ordered domains in the live cell plasma membrane. Nat Commun. 2015;6:6969.
132. Lee HJ, Zhang W, Zhang D, et al. Assessing cholesterol storage in live cells and C. elegans by stimulated Raman scattering imaging of phenyl-Diyne cholesterol. Sci Rep. 2015;5:7930.
133. Listenberger LL, Brown DA. Fluorescent detection of lipid droplets and associated proteins. Curr Protoc Cell Biol. 2007:24. doi: 10.1002/0471143030. cb2402s35.
134. Milles S, Meyer T, Scheidt HA, et al. Organization of fluorescent cholesterol analogs in lipid bilayers-lessons from cyclodextrin extraction. Biochim Biophys Acta. 2013;1828:1822-1828.
135. Kanerva K, Uronen RL, Blom T, et al. LDL cholesterol recycles to the plasma membrane via a Rab8a-Myosin5b-actin-dependent membrane transport route. Dev Cell. 2013;27:249-262.
136. Krieger M. Reconstitution of the hydrophobic core of low-density-lipoprotein. Methods Enzymol. 1986;128:608-613.
137. Röhrl C, Meisslitzer-Ruppitsch C, Bittman R, et al. Combined light and electron microscopy using diaminobenzidine photooxidation to monitor trafficking of lipids derived from lipoprotein particles. Curr Pharm Biotechnol. 2012;13: 331-340.
138. Silver DL, Wang N, Xiao X, Tall AR. High density lipoprotein (HDL) particle uptake mediated by scavenger receptor class B type 1 results in selective sorting of HDL cholesterol from protein and polarized cholesterol secretion. J Biol Chem. 2001;276:25287-25293.
139. Wüstner D. Mathematical analysis of hepatic high density lipoprotein transport based on quantitative imaging data. J Biol Chem. 2005;280:6766-6779.
140. Ikonen E, Blom T. Lipoprotein-mediated delivery of BODIPY-labeled sterol and sphingolipid analogs reveals lipid transport mechanisms in mammalian cells. Chem Phys Lipids. 2016;194:29-36.
141. Bernik DL, Negri RM. Local polarity at the polar head level of lipid vesicles using dansyl fluorescent probes. J Colloid Interface Sci. 1998;203:97-105.
142. Wiegand V, Chang TY, Strauss JF III, Fahrenholz F, Gimpl G. Transport of plasma membrane-derived cholesterol and the function of Niemann-Pick C1 protein. FASEB J. 2003;17:782-784.
143. Huang H, McIntosh AL, Atshaves BP, Ohno-Iwashita Y, Kier AB, Schroeder F. Use of dansyl-cholestanol as a probe of cholesterol behavior in membranes of living cells. J Lipid Res. 2010;51:1157-1172.
144. Haberland ME, Reynolds JA. Self-association of cholesterol in aqueous solution. Proc Natl Acad Sci U S A. 1973;70:2313-2318.
145. Stubbs CD, Meech SR, Lee AG, Phillips D. Solvent relaxation in lipid bilayers with dansyl probes. Biochim Biophys Acta. 1985;815:351-360.
146. Shrivastava S, Haldar S, Gimpl G, Chattopadhyay A. Orientation and dynamics of a novel fluorescent cholesterol analogue in membranes of varying phase. J Phys Chem B. 2009;113:4475-4481.
147. Chattopadhyay A, London E. Parallax method for direct measurement of membrane penetration depth utilizing fluorescence quenching by spin-labeled phospholipids. Biochemistry. 1987;26:39-45.
148. Leonard A, Escrive C, Laguerre M, et al. Location of cholesterol in DMPC membranes. A comparative study by neutron diffraction and molecular mechanics simulation. Langmuir. 2001;17:2019-2030.
149. Petrescu AD, Vespa A, Huang H, McIntosh AL, Schroeder F, Kier AB. Fluorescent sterols monitor cell penetrating peptide Pep-1 mediated uptake and intracellular targeting of cargo protein in living cells. Biochim Biophys Acta. 2009;1788: 425-441.
150. Wrenn SP, Kaler EW, Lee SP. A fluorescence energy transfer study of lecithincholesterol vesicles in the presence of phospholipase C. J Lipid Res. 1999;40: 1483-1494.
151. Wrenn SP, Gudheti M, Veleva AN, Kaler EW, Lee SP. Characterization of model bile using fluorescence energy transfer from dehydroergosterol to dansylated lecithin. J Lipid Res. 2001;42:923-934.
152. John K, Kubelt J, Muller P, Wustner D, Herrmann A. Rapid transbilayer movement of the fluorescent sterol dehydroergosterol in lipid membranes. Biophys J. 2002;83:1525-1534.
153. Benson DM, Bryan J, Plant AL, Gotto AMJ, Smith LC. Digital imaging fluorescence microscopy: spatial heterogeneity of photobleaching rate constants in individual cells. J Cell Biol. 1985;100:1309-1323.
154. Craig IF, Via DP, Mantulin WW, Pownall HJ, Gotto AM Jr, Smith LC. Low density lipoproteins reconstituted with steroids containing the nitrobenzoxadiazole fluorophore. J Lipid Res. 1981;22:687-696.
155. Gimpl G, Gehrig-Burger K. Cholesterol reporter molecules. Biosci Rep. 2007; 27:335-358.
156. Reiner S, Micolod D, Schneiter R. Saccharomyces cerevisiae, a model to study sterol uptake and transport in eukaryotes. Biochem Soc Trans. 2005;33: 1186-1188.
157. Marek M, Silvestro D, Fredslund MD, Andersen TG, Pomorski TG. Serum albumin promotes ATP-binding cassette transporter-dependent sterol uptake in yeast. FEMS Yeast Res. 2014;14:1223-1233.
158. Ishii H, Shimanouchi T, Umakoshi H, Walde P, Kuboi R. Analysis of the 22-NBD-cholesterol transfer between liposome membranes and its relation to the intermembrane exchange of 25-hydroxycholesterol. Colloids Surf B Biointerfaces. 2010;77:117-121.
159. Bar LK, Chong PL, Barenholz Y, Thompson TE. Spontaneous transfer between phospholipid bilayers of dehydroergosterol, a fluorescent cholesterol analog. Biochim Biophys Acta. 1989;983:109-112.
160. Bar LK, Barenholz Y, Thompson TE. Fraction of cholesterol undergoing spontaneous exchange between small unilamellar phosphatidylcholine vesicles. Biochemistry. 1986;25:6701-6705.
161. Ostašov P, Sỳkora J, Brejchová J, Olzynska A, Hof M, Svoboda P. FLIM studies of 22- and 25-NBD-cholesterol in living HEK293 cells: plasma membrane change induced by cholesterol depletion. Chem Phys Lipids. 2013;167-168: 62-69.
162. Mukherjee S, Zha X, Tabas I, Maxfield FR. Cholesterol distribution in living cells: fluorescence imaging using dehydroergosterol as a fluorescent cholesterol analog. Biophys J. 1998;75:1915-1925.
163. Faletrov YV, Bialevich KI, Edimecheva IP, et al. 22-NBD-cholesterol as a novel fluorescent substrate for cholesterol-converting oxidoreductases. J Steroid Biochem Mol Biol. 2013;134:59-66.
164. Faletrov YV, Frolova NS, Hlushko HV, et al. Evaluation of the fluorescent probes Nile Red and 25-NBD-cholesterol as substrates for steroid-converting oxidoreductases using pure enzymes and microorganisms. FEBS J. 2013;280:3109-3119.
165. Kheirolomoom A, Ferrara KW. Cholesterol transport from liposomal delivery vehicles. Biomaterials. 2007;28:4311-4320.
166. Sparrow CP, Patel S, Baffic J, et al. A fluorescent cholesterol analog traces cholesterol absorption in hamsters and is esterified in vivo and in vitro. J Lipid Res. 1999;40:1747-1757.
167. Lada AT, Davis M, Kent C, et al. Identification of ACAT1- and ACAT2- specific inhibitors using a novel, cell-based fluorescence assay: individual ACAT uniqueness. J Lipid Res. 2004;45:378-386.
168. Reiner S, Micolod D, Zellnig G, Schneiter R. A genomewide screen reveals a role of mitochondria in anaerobic uptake of sterols in yeast. Mol Biol Cell. 2005; 17:90-103.
169. Lusa S, Jauhiainen M, Metso J, Somerharju P, Ehnholm C. The mechanism of human plasma phospholipid transfer protein-induced enlargement of high-density lipoprotein particles: evidence for particle fusion. Biochem J. 1996;313(pt 1): 275-282.
170. Lusa S, Tanhuanpaa K, Ezra T, Somerharju P. Direct observation of lipoprotein cholesterol ester degradation in lysosomes. Biochem J. 1998;332(pt 2):451-457.
171. Le Guyader L, Le Roux C, Mazères S, et al. Changes of the membrane lipid organization characterized by means of a new cholesterol-pyrene probe. Biophys J. 2007;93:4462-4473.
172. Repáková J, Holopainen JM, Karttunen M, Vattulainen I. Influence of pyrenelabeling on fluid lipid membranes. J Phys Chem B. 2006;110:15403-15410.
173. Gaibelet G, Terce F, Bertrand-Michel J, et al. 21-Methylpyrenyl-cholesterol stably and specifically associates with lipoprotein peripheral hemi-membrane: a new labelling tool. Biochem Biophys Res Commun. 2013;440:533-538.
174. Gaibelet G, Allart S, Terce F, et al. Specific cellular incorporation of a pyrenelabelled cholesterol: lipoprotein-mediated delivery toward ordered intracellular membranes. PLoS One. 2015;10:e0121563.
175. Kolb HC, Sharpless KB. The growing impact of click chemistry on drug discovery. Drug Discov Today. 2003;8:1128-1137.
176. Gaebler A, Milan R, Straub L, Hoelper D, Kuerschner L, Thiele C. Alkyne lipids as substrates for click chemistry-based in vitro enzymatic assays. J Lipid Res. 2013;54:2282-2290.
177. Thiele C, Papan C, Hoelper D, et al. Tracing fatty acid metabolism by click chemistry. ACS Chem Biol. 2012;7:2004-2011.
178. Hofmann K, Thiele C, Schott HF, et al. A novel alkyne cholesterol to trace cellular cholesterol metabolism and localization. J Lipid Res. 2014;55:583-591.
179. Peyrot SM, Nachtergaele S, Luchetti G, et al. Tracking the subcellular fate of 20(S)-hydroxycholesterol with click chemistry reveals a transport pathway to the Golgi. J Biol Chem. 2014;289:11095-11110.
180. Yamakoshi H, Dodo K, Palonpon A, et al. Alkyne-tag Raman imaging for visualization of mobile small molecules in live cells. J Am Chem Soc. 2012;134: 20681-20689.
181. Scheidt HA, Meyer T, Nikolaus J, et al. Cholesterol's aliphatic side chain modulates membrane properties. Angew Chem Int Ed Engl. 2013;52:12848-12851.
182. Meyer T, Baek DJ, Bittman R, et al. Membrane properties of cholesterol analogs with an unbranched aliphatic side chain. Chem Phys Lipids. 2014;184:1-6.
183. Chien CH, Chen WW, Wu JT, Chang TC. Label-free imaging of Drosophila in vivo by coherent anti-Stokes Raman scattering and two-photon excitation autofluorescence microscopy. J Biomed Opt. 2011;16:016012.
184. Jao CY, Nedelcu D, Lopez LV, Samarakoon TN, Welti R, Salic A. Bioorthogonal probes for imaging sterols in cells. Chembiochem. 2015;16:611-617.
185. Sletten EM, Bertozzi CR. From mechanism to mouse: a tale of two bioorthogonal reactions. Acc Chem Res. 2011;44:666-676.
186. Baskin JM, Prescher JA, Laughlin ST, et al. Copper-free click chemistry for dynamic in vivo imaging. Proc Natl Acad Sci U S A. 2007;104:16793-16797.
187. Wüstner D, Lund FW, Solanko LM. Quantitative fluorescence studies of intracellular sterol transport and distribution. In: Mely Y, Duportail G, eds. Springer Series in Fluorescence. Properties and Functions of Biological Membranes Investigated by Fluorescence Methods. Springer Press, Berlin Heidelberg; 2012:185-213.