Structural analysis of sterol distributions in the plasma membrane of living cells

Biochemistry

Volumn 44, Issue 8, 2005, Pages 2864-2884

  Zhang, Weimin ^a   McIntosh, Avery L ^b   Xu, Hai ^a   Wu, Di ^a   Gruninger, Todd ^a   Atshaves, Barbara ^b   Liu, J C Steve ^a   Schroeder, Friedhelm ^b  

^a Texas AandM University   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOLOGICAL MEMBRANES; BIOMARKERS; CELLS; CYTOLOGY; IMAGE PROCESSING; MATHEMATICAL MODELS; PROTEINS; RANDOM PROCESSES; STATISTICAL METHODS;

DEHYDROERGOSTEROL (DHE); LIVING CELLS; MULTIPHOTON LASER SCANNING MICROSCOPY (MLSM); PLASMA MEMBRANES;

CHOLESTEROL;

3' DIOCTADECYLOXACARBOCYANINE PERCHLORATE; CARBOCYANINE; CYAN FLUORESCENT PROTEIN; DEHYDROERGOSTEROL; STEROL DERIVATIVE; UNCLASSIFIED DRUG;

ALGORITHM; ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; IMAGE PROCESSING; LASER MICROSCOPY; MOUSE; NONHUMAN; POISSON DISTRIBUTION; PRIORITY JOURNAL; STEROL ANALYSIS; STRUCTURE ANALYSIS;

ANIMALS; CELL MEMBRANE; ERGOSTEROL; FIBROBLASTS; L CELLS (CELL LINE); MEMBRANE LIPIDS; MICE; MICROSCOPY, CONFOCAL; MONTE CARLO METHOD; STEROLS;

EID: 14344265621     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048172m     Document Type: Article

References (70)

1. Brown, M. S., and Goldstein, J. L. (1986) A receptor-mediated pathway for cholesterol homeostasis, Science 232, 34-47.
2. Small, D. M. (1988) Progression and regression of atherosclerotic lesions. Insights from lipid physical chemistry, Arteriosclerosis 8, 103-129.
3. Tabas, I. (1997) Free cholesterol-induced cytotoxicity, Trends Cardiovasc. Med. 7, 256-263.
4. Sokol, J., Blanchette-Mackie, E. J., Kruth, H. S., Dwyer, N. K., Amende, L. M., Butler, J. D., Robinson, E., Patel, S., Brady, R. O., Comly, M. E., Vanier, M. T., and Pentchev, P. (1988) Type C Niemann-Pick disease: lysosomal accumulation and defective intracellular mobilization of LDL cholesterol, J. Biol. Chem. 263, 3411-3417.
5. Fielding, C. J., and Fielding, P. E. (1997) Intracellular cholesterol transport, J. Lipid Res. 38, 1503-1521.
6. Schroeder, F., Gallegos, A. M., Atshaves, B. P., Storey, S. M., McIntosh, A., Petrescu, A. D., Huang, H., Starodub, O., Chao, H., Yang, H., Frolov, A., and Kier, A. B. (2001) Recent advances in membrane microdomains: rafts, caveolae, and intracellular cholesterol trafficking, Exp. Biol. Med. 226, 873-890.
7. Anderson, R. (1998) The caveolae membrane system, Annu. Rev. Biochem. 67, 199-225.
8. Brown, D. A., and London, E. (2000) Structure and function of sphingolipid- and cholesterol-rich membrane rafts, J. Biol. Chem. 275, 17221-17224.
9. Hooper, N. M. (1999) Detergent-insoluble glycosphingolipid/cholesterol rich membrane domains, lipid rafts, and caveolae, Mol. Membr. Biol. 16, 145-156.
10. Simons, K., and Ikonen, E. (1997) Functional rafts in cell membranes, Nature 387, 569-572.
11. Fielding, C. J., and Fielding, P. E. (2000) Cholesterol and caveolae: structural and functional relationships, Biochim. Biophys. Acta 1529, 210-222.
12. Samsonov, A. V., Mihalyov, I., and Cohen, F. S. (2001) Characterization of cholesterol-sphingomyelin domains and their dynamics in bilayer membranes, Biophys. J. 81, 1486-1500.
13. Ikonen, E., and Parton, R. G. (2000) Caveolins and cellular cholesterol balance, Traffic 1, 212-217.
14. Kurzchalia, T. V., and Parton, R. G. (1999) Membrane microdomains and caveolae, Curr. Opin. Cell Biol. 11, 424-431.
15. Lundbaek, J. A., Andersen, O. S., Werge, T., and Nielsen, C. (2003) Cholesterol-induced protein sorting: an analysis of energetic feasibility Biophys. J. 84, 2080-2089.
16. Stahlhut, M., Sandvig, K., and van Deurs, B. (2000) Caveolae: Uniform Structures with Multiple Functions in Signaling, Cell Growth, and Cancer, Exp. Cell Res. 261, 111-118.
17. Pierini, L. M., and Maxfield, F. R. (2001) Commentary flotillas of lipid rafts fore and aft, Proc. Natl. Acad. Sci. U.S.A. 98, 9471-9473.
18. Anderson, R. G. W., and Jacobson, K. (2002) A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains, Science 296, 1821-1825.
19. Smart, E. J., Ying, Y., Mineo, C., and Anderson, R. G. W. (1995) A detergent-free method for purifying caveolae membrane from tissue culture cells, Proc. Natl. Acad. Sci. U.S.A. 92, 10404-10408.
20. Schroeder, R., London, E., and Brown, D. (1994) Interactions between saturated acyl chains confer detergent resistance on lipids and glycosylphosphatidylinositol (GPI)-anchored proteins: GPI-anchored proteins in liposomes and cells show similar behavior, Proc. Natl. Acad. Sci. U.S.A. 91, 12130-12134.
21. Brown, D. A., and London, E. (1998) Structure and origin of ordered lipid domains in biological membranes, J. Membr. Biol. 164, 103-114.
22. Pike, L. J., Han, X., Chung, K.-N., and Gross, R. W. (2002) Lipid rafts are enriched in arachidonic acid and plasmenylethanolamine and their composition is independent of caveolin-1 expression: a quantitative electrospray ionization/mass spectrometric analysis, Biochemistry 41, 2075-2088.
23. McIntosh, A., Gallegos, A., Atshaves, B. P., Storey, S., Kannoju, D., and Schroeder, F. (2003) Fluorescence and multiphoton imaging resolve unique structural forms of sterol in membranes of living cells, J. Biol. Chem. 278, 6384-6403.
24. Eckert, G. P., Igbavboa, U., Muller, W., and Wood, W. G. (2003) Lipid rafts of purified mouse brain synaptosomes prepared with or without detergent reveal different lipid and protein domains, Brain Res. 962, 144-150.
25. London, E., and Brown, D. A. (2000) Insolubility of lipids in Trition X-100: physical origin and relationship to sphingolipid/cholesterol membrane domains (rafts), Biochim. Biophys. Acta 1508, 182-195.
26. Hale, J. E., and Schroeder, F. (1982) Asymmetric transbilayer distribution of sterol across plasma membranes determined by fluorescence quenching of dehydroergosterol, Eur. J. Biochem. 122, 649-661.
27. Schroeder, F., and Nemecz, G. (1990) in Advances in Cholesterol Research (Esfahami, M., and Swaney, J., Eds.) pp 47-87, Telford Press, Caldwell, NJ.
28. Schroeder, F. (1984) Fluorescent sterols: probe molecules of membrane structure and function, Prog. Lipid Res. 23, 97-113.
29. Schroeder, F., Jefferson, J. R., Kier, A. B., Knittell, J., Scallen, T. J., Wood, W. G., and Hapala, I. (1991) Membrane cholesterol dynamics: cholesterol domains and kinetic pools, Proc. Soc. Exp. Biol. Med. 196, 235-252.
30. Gimpl, G., Burger, K., and Fahrenholz, F. (1997) Cholesterol as modulator of receptor function, Biochemistry 36, 10959-10974.
31. Schroeder, F., Frolov, A., Schoer, J., Gallegos, A., Atshaves, B. P., Stolowich, N. J., Scott, A. I., and Kier, A. B. (1998) in Intracellular Cholesterol Trafficking (Chang, T. Y., and Freeman, D. A., Eds.) pp 213-234, Kluwer Academic Publishers, Boston, MA.
32. Frolov, A., Petrescu, A., Atshaves, B. P., So, P. T. C., Gratton, E., Serrero, G., and Schroeder, F. (2000) High-density lipoprotein mediated cholesterol uptake and targeting to lipid droplets in intact L-cell fibroblasts, J. Biol. Chem. 275, 12769-12780.
33. Mukherjee, S., Zha, X., Tabas, I., and Maxfield, F. R. (1998) Cholesterol distribution in living cells: fluorescence imaging using dehydroergosterol as a fluorescent cholesterol analog, Biophys. J. 75, 1915-1925.
34. Wustner, D., Herrmann, A., Hao, M., and Maxfield, F. R. (2002) Rapid nonvesicular transport of sterol between the plasma membrane domains of polarized hepatic cells, J. Biol. Chem. 277, 30325-30336.
35. Williams, R. M., Zipfel, W. R., and Webb, W. W. (2001) Multiphoton microscopy in biological research, Curr. Opin. Chem. Biol. 5, 603-608.
36. Xu, C., Zipfel, W. R., Shear, J. B., Williams, R. M., and Webb, W. W. (1996) Multiphoton fluorescence excitation: new spectral windows for biological nonlinear spectroscopy, Proc. Natl. Acad. Sci. U.S.A. 93, 10763-10768.
37. Huang, H., Starodub, O., McIntosh, A., Kier, A. B., and Schroeder, F. (2002) Liver fatty acid binding protein targets fatty acids to the nucleus: real-time confocal and multiphoton fluorescence imaging in living cells, J. Biol. Chem. 277, 29139-29151.
38. Rocheleau, J. V., Wiseman, P. W., and Petersen, N. O. (2003) Isolation of bright aggregate fluctuations in a multipopulation image correlation spectroscopy system using intensity subtraction, Biophys. J. 84, 4011-4022.
39. Petersen, N. O., Hoddelius, P. L., Wiseman, P. W., Seger, O., and Magnusson, K. E. (1993) Quantitation of membrane receptor distributions by image correlation spectroscopy: concept and application, Biophys. J. 65, 1135-1146.
40. Elson, E. L., and Webb, W. W. (1975) Concentration correlation spectroscopy: a new biophysical probe based on occupation number fluctuations, Annu. Rev. Biophys. Bioeng. 4, 311-334.
41. Magde, D., Elson, E. L., and Webb, W. W. (1974) Fluorescence correlation spectroscopy. II. An experimental realization, Biopolymers 13, 29-61.
42. McCaughan, L., and Krimm, S. (1980) X-ray and neutron scattering density profiles of the intact human red blood cell membrane, Science 207, 1481-1483.
43. Kaplan, M. R., and Simoni, R. D. (1985) Transport of cholesterol from the endoplasmic reticulum to the plasma membrane, J. Cell Biol. 101, 446-453.
44. Fischer, R. T., Stephenson, F. A., Shafiee, A., and Schroeder, F. (1985) Structure and dynamic properties of dehydroergosterol, Δ5,7,9(11),22- ergostatetraen-3β-ol, J. Biol. Phys. 13, 13-24.
45. Ruthazer, E. S., and Cline, H. T. (2002) Multiphoton imaging of neurons in living tissue: acquisition and analysis of time-lapse morphological data, Real-Time Imaging 8, 175-188.
46. Hollander, M., and Wolfe, D. A. (1999) Nonparametric Statistical Methods, John Wiley & Sons, New York.
47. Mukundan, R., and Ramakrishnan, K. R. (1998) Moment Function in Image Analysis: Theory and Applications, World Scientific, River Edge, NJ.
48. Diggle, P. J. (1983) Statistical Analysis of Spatial Point Patterns, Academic Press, New York.
49. Baddeley, A. J., and Gill, R. D. (1997) Kaplan-Meier estimators of interpoint distance distributions for spatial point processes, Ann. Stat. 25, 263-292.
50. Bernard, G. A. (1963) Contribution to the discussion of Professor Bartlett's paper, J. R. Stat. Soc. B25, 294.
51. A project for statistical computing, http://www.r-project.org/index.html.
52. Atshaves, B. P., Gallegos, A., McIntosh, A. L., Kier, A. B., and Schroeder, F. (2003) Sterol carrier protein-2 selectively alters lipid composition and cholesterol dynamics of caveolae/lipid raft vs non-raft domains in L-cell fibroblast plasma membranes, Biochemistry 42, 14583-14598.
53. Schroeder, F., Fontaine, R. N., and Kinden, D. A. (1982) LM fibroblast plasma membrane subfractionation by affinity chromatography on ConA-sepharose, Biochim. Biophys. Acta 690, 231-242.
54. Schroeder, F., and Kinden, D. A. (1983) Measurement of phagocytosis using fluorescent latex beads, J. Biochem. Biophys. Methods 8, 15-27.
55. Yonemura, S., Tsukita, S., and Tsukita, S. (1999) Direct involvement of ezrin/radixin/moesin (ERM)-binding membrane proteins in the organization of microvilli in collaboration with activated ERM proteins, J. Cell Biol. 145, 1497-1509.
56. Puri, V., Watanabe, R., Singh, R. D., Dominguez, M., Brown, J. C., Wheatley, C. L., Marks, D. L., and Pagano, R. E. (2001) Clathrin-dependent and -independent internalization of plasma membrane sphingolipids initiates two Golgi targeting pathways, J. Cell Biol. 154, 535-547.
57. Roper, K., Corbeil, D., and Huttner, W. B. (2000) Retention of prominin in microvilli reveals distinct cholesterol-based lipid microdomains in the apical plasma membrane, Nat. Cell Biol. 2, 582-592.
58. Spink, C. H., Yeager, M., and Feigenson, G. W. (1990) Partitioning behavior of indocarbocyanine probes between coexisting gel and fluid phases in model membranes, Biochim. Biophys. Acta 1023, 25-33.
59. Pearse, B. M. F. (1976) Clathrin: a unique protein associated with intracellular transfer of membrane by coated vesicles, Proc. Natl. Acad. Sci. U.S.A. 73, 1255-1259.
60. Mukherjee, S., Ghosh, R. N., and Maxfield, F. R. (1997) Endocytosis, Physiol Rev. 77, 759-803.
61. Hao, M., and Maxfield, F. R. (2000) Characterization of rapid membrane internalization and recycling, J. Biol. Chem. 275, 15279-15286.
62. Hao, M., Lin, S. X., Karylowski, O. J., Wustner, D., McGraw, T. E., and Maxfield, F. R. (2002) Vesicular and non-vesicular sterol transport in living cells: the endoytic recycling compartment is a major sterol storage organelle, J. Biol. Chem. 277, 609-617.
63. Schutz, G. J., Kada, G., Pastushenko, V. Ph., and Schindler, H. (2000) Properties of lipid microdomains in a muscle cell membrane visualized by single molecule microscopy, EMBO J. 19, 892-901.
64. Wachtler, V., Rajagopalan, S., and Balasubramanian, M. K. (2003) Sterol-rich plasma membrane domains in the fission yeast Schizosaccharomyces pombe, J. Cell Sci. 116, 867-874.
65. Prior, I. A., Muncke, C., Parton, R. G., and Hancock, J. F. (2003) Direct visualization of Ras proteins in spatially distinct surface microdomains, J. Cell Biol. 160, 165-170.
66. Thomsen, P., Roepstorff, K., Stahlhut, M., and van Deurs, B. (2002) Caveolae are highly immobile plasma membrane microdomains, which are not involved in constitutive endocytic trafficking, Mol. Biol. Cell 13, 238-250.
67. Kuehl, R. O. (2000) Design of Experiments, Statistical Principles of Research Design and Analysis, Duxbury/Thomson Learning, Pacific Grove, CA.
68. Hu, M. K. (1961) Pattern recognition by moment invariants, Proc. Inst. Radio Eng. 49, 1428.
69. Sluzek, A. (1995) Identification and inspection of 2-D objects using new moment-based shape descriptors, Pattern Recognit. Lett. 16, 687-697.
70. Gentle, J. E. (2002) Elements of Computational Statistics, Springer-Verlag, New York.