Fluorescence imaging of two-photon linear dichroism: Cholesterol depletion disrupts molecular orientation in cell membranes

Biophysical Journal

Volumn 88, Issue 1, 2005, Pages 609-622

  Benninger, Richard K P ^a   Önfelt, Björn ^a   Neil, Mark A A ^a   Davis, Daniel M ^a   French, Paul M W ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; NANOTUBE;

ACCURACY; ANISOTROPY; ARTICLE; CELL MEMBRANE; DIFFUSION; DYNAMICS; ENERGY TRANSFER; FLUORESCENCE; HUMAN; HUMAN CELL; HYDROPHOBICITY; IMAGING SYSTEM; LINEAR DICHROISM; MOTION; ROTATION; TIME;

EID: 11344277995     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.104.050096     Document Type: Article

References (62)

1. Ardhammar, M., N. Mikati, and B. Nordén. 1998. Chromophore orientation in liposome membranes probed with flow dichroism. J. Am. Chem. Soc. 120:9957-9958.
2. Axelrod, D. 1979. Carbocyanine dye orientation in red cell membrane studied by microscopic fluorescence polarization. Biophys. J. 26:557-574.
3. Bergström, F., P. Hagglöf, J. Karolin, T. Ny, and L. B. Å. Johansson. 1999. The use of site-directed fluorophore labeling and donor-donor energy migration to investigate solution structure and dynamics in proteins. Proc. Natl. Acad. Sci. USA. 96:12477-12481.
4. Bergström, F., I. Mikhalyov, P. Hagglöf, R. Wortmann, T. Ny, and L. B. Å. Johansson. 2002. Dimers of dipyrrometheneboron difluoride (BODIPY) with light spectroscopic applications in chemistry and biology. J. Am. Chem. Soc. 124:196-204.
5. Blackman, S. M., C. E. Cobb, A. H. Beth, and D. W. Piston. 1996. The orientation of eosin-5-maleimide on human erythrocyte band 3 measured by fluorescence polarization microscopy. Biophys. J. 71:194-208.
6. Borejdo, J., A. Shepard, D. Dumka, I. Akopova, J. Talent, A. Malka, and T. P. Burghardt. 2004. Changes in orientation of actin during contraction of muscle. Biophys. J. 86:2308-2317.
7. Brattwall, C. E. B., P. Lincoln, and B. Norde̊n. 2003. Orientation and conformation of cell-penetrating peptide penetratin in phospholipid vesicle membranes determined by polarized-light spectroscopy. J. Am. Chem. Soc. 125:14214-14215.
8. Castanho, M. A. R. B., S. Lopes, and M. Fernandes. 2003. Using UV-Vis. linear dichroism to study the orientation of molecular probes and biomolecules in lipidic membranes. Spectroscopy. 17:377-398.
9. Chen, C. S., O. C. Martin, and R. E. Pagano. 1997. Changes in the spectral properties of a plasma membrane lipid analog during the first seconds of endocytosis in living cells. Biophys. J. 72:37-50.
10. Clayton, A. H., Q. S. Hanley, D. J. Arndt-Jovin, V. Subramaniam, and T. M. Jovin. 2002. Dynamic fluorescence anisotropy imaging microscopy in the frequency domain (rFLIM). Biophys. J. 83:1631-1649.
11. Cosman, D., J. Mullberg, C. L. Sutherland, W. Chin, R. Armitage, W. Fanslow, M. Kubin, and N. J. Chalupny. 2001. ULBPs, novel MHC class I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity. 14:123-133.
12. Dahim, M., N. K. Mizuno, X. M. Li, W. E. Momsen, M. M. Momsen, and H. L. Brockman. 2002. Physical and photophysical characterization of a BODIPY phosphatidylcholine as a membrane probe. Biophys. J. 83:1511-1524.
13. Davis, D. M. 2002. Assembly of the immunological synapse for T cells and NK cells. Trends Immunol. 23:356-363.
14. Dietrich, C., B. Yang, T. Fujiwara, A. Kusumi, and K. Jacobson. 2002. Relationship of lipid rafts to transient confinement zones detected by single particle tracking. Biophys. J. 82:274-284.
15. Doucey, M. A., L. Scarpellino, J. Zimmer, P. Guillaume, I. F. Luescher, C. Bron, and W. Held. 2004. Cis association of Ly49A with MHC class I restricts natural killer cell inhibition. Nat. Immunol. 5:328-336.
16. Edidin, M. 2003. The state of lipid rafts: from model membranes to cells. Annu. Rev. Biophys. Biomol. Struct. 32:257-283.
17. Edmiston, P. L., J. E. Lee, L. L. Wood, and S. S. Saavedra. 1996. Dipole orientation distributions in Langmuir-Blodgett films by planar waveguide linear dichroism and fluorescence anisotropy. J. Phys. Chem. 100:775-784.
18. Egner, A., V. Andresen, and S. W. Hell. 2002. Comparison of the axial resolution of practical Nipkow-disk confocal fluorescence microscopy with that of multifocal multiphoton microscopy: theory and experiment. J. Microsc. 206:24-32.
19. Eleme, K., S. B. Taner, B. Önfelt, L. M. Collinson, F. E. McCann, N. J. Chalupny, D. Cosman, C. Hopkins, A. I. Magee, and D. M. Davis. 2004. Cell surface organization of stress-inducible proteins ULBP and MICA that stimulate human NK cells and T cells via NKG2D. J. Exp. Med. 199:1005-1010.
20. Farber, S. A., E. S. Olson, J. D. Clark, and M. E. Halpern. 1999. Characterization of Ca2+-dependent phospholipase A2 activity during zebrafish embryogenesis. J. Biol. Chem. 274:19338-19346.
21. Gaus, K., E. Gratton, E. P. Kable, A. S. Jones, I. Gelissen, L. Kritharides, and W. Jessup. 2003. Visualizing lipid structure and raft domains in living cells with two-photon microscopy. Proc. Natl. Acad. Sci. USA. 100:15554-15559.
22. Gomez-Mouton, C., J. L. Abad, E. Mira, R. A. Lacalle, E. Gallardo, S. Jimenez-Baranda, I. Illa, A. Bernad, S. Manes, and A. C. Martinez. 2001. Segregation of leading-edge and uropod components into specific lipid rafts during Tcell polarization. Proc. Natl. Acad. Sci. USA. 98:9642-9647.
23. Harder, T., P. Scheiffele, P. Verkade, and K. Simons. 1998. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol. 141:929-942.
24. Jin, L. W., K. A. Claborn, M. Kurimoto, M. A. Geday, I. Maezawa, F. Sohraby, M. Estrada, W. Kaminksy, and B. Kahr. 2003. Imaging linear birefringence and dichroism in cerebral amyloid pathologies. Proc. Natl. Acad. Sci. USA. 100:15294-15298.
25. Johnson, I. D., H. C. Kang, and R. P. Haugland. 1991. Fluorescent membrane probes incorporating dipyrrometheneboron difluoride fluorophores. Anal. Biochem. 198:228-237.
26. Karlsson, A., R. Karlsson, M. Karlsson, A. S. Cans, A. Strömberg, F. Ryttsen, and O. Orwar. 2001. Networks of nanotubes and containers. Nature. 409:150-152.
27. Karolin, J., L. B. Å. Johansson, L. Strandberg, and T. Ny. 1994. Fluorescence and Absorption Spectroscopic Properties of Dipyrrometheneboron Difluoride (Bodipy) Derivatives in Liquids, Lipid-Membranes, and Proteins. J. Am. Chem. Soc. 116:7801-7806.
28. Kilsdonk, E. P., P. G. Yancey, G. W. Stoudt, F. W. Bangerter, W. J. Johnson, M. C. Phillips, and G. H. Rothblat. 1995. Cellular cholesterol efflux mediated by cyclodextrins. J. Biol. Chem. 270:17250-17256.
29. Korlach, J., P. Schwille, W. W. Webb, and G. W. Feigenson. 1999. Characterization of lipid bilayer phases by confocal microscopy and fluorescence correlation spectroscopy. Proc. Natl. Acad. Sci. USA. 96:8461-8466.
30. Krishna, M. M., and N. Periasamy. 1999. Location and orientation of DODCI in lipid bilayer membranes: effects of lipid chain length and unsaturation. Biochim. Biophys. Acta. 1461:58-68.
31. Krishna, M. M. G., and N. Periasamy. 1998. Orientational distribution of linear dye molecules in bilayer membranes. Chem. Phys. Lett. 298:359-367.
32. Kusumi, A., I. Koyama-Honda, and K. Suzuki. 2004. Molecular dynamics and interactions for creation of stimulation-induced stabilized rafts from small unstable steady-state rafts. Traffic. 5:213-230.
33. Lopes, S., and M. A. R. B. Castanho. 2004. Does aliphatic chain length influence carbocyanines' orientation in supported lipid multilayers. J. Fluoresc. 14:281-287.
34. Mitra, A. K., H. Celia, G. Ren, J. G. Luz, I. A. Wilson, and L. Teyton. 2004. Supine orientation of a murine MHC class I molecule on the membrane bilayer. Curr. Biol. 14:718-724.
35. Munro, S. 2003. Lipid rafts: elusive or illusive? Cell. 115:377-388.
36. Neil, M. A. A., R. Juškaitis, and T. Wilson. 1997. Method of obtaining-optical sectioning by using structured light in a conventional microscope. Opt. Lett. 22:1905-1907.
37. Nielsen, T., M. Frick, D. Hellweg, and P. Andresen. 2001. High efficiency beam splitter for multifocal multiphoton microscopy. J. Microsc. 201:368-376.
38. Norden, B., M. Kubista, and T. Kurucsev. 1992. Linear dichroism spectroscopy of nucleic acids. Q. Rev. Biophys. 25:51-170.
39. Ohvo, H., and J. P. Slotte. 1996. Cyclodextrin-mediated removal of sterols from monolayers: effects of sterol structure and phospholipids on desorption rate. Biochemistry. 35:8018-8024.
40. Ohvo-Rekila, H., B. Ramstedt, P. Leppimaki, and J. P. Slotte. 2002. Cholesterol interactions with phospholipids in membranes. Prog. Lipid Res. 41:66-97.
41. Önfelt, B., and D. M. Davis. 2004. Can membrane nanotubes facilitate communication between immune cells? Biochem. Soc. Trans. 32:676-678.
42. Önfelt, B., S. Nedvetzki, K. Yanagi, and D. M. Davis. 2004. Cutting edge: membrane nanotubes connect immune cells. J. Immunol. 173:1511-1513.
43. Pandit, S. A., D. Bostick, and M. L. Berkowitz. 2004. Complexation of phosphatidylcholine lipids with cholesterol. Biophys. J. 86:1345-1356.
44. Parasassi, T., E. Gratton, W. M. Yu, P. Wilson, and M. Levi. 1997. Two-photon fluorescence microscopy of laurdan generalized polarization domains in model and natural membranes. Biophys. J. 72:2413-2429.
45. Pralle, A., P. Keller, E. L. Florin, K. Simons, and J. K. H. Horber. 2000. Sphingolipid-cholesterol rafts diffuse as small entities in the plasma membrane of mammalian cells. J. Cell Biol. 148:997-1007.
46. Richards, B., and E. Wolf. 1959. Electromagnetic Diffraction in Optical Systems. 2. Structure of the Image Field in an Aplanatic System. Proc. Roy. Soc. A. 253:358-379.
47. Rocheleau, J. V., M. Edidin, and D. W. Piston. 2003. Intrasequence GFP in class I MHC molecules, a rigid probe for fluorescence anisotropy measurements of the membrane environment. Biophys. J. 84:4078-4086.
48. Rustom, A., R. Saffrich, I. Markovic, P. Walther, and H. H. Gerdes. 2004. Nanotubular highways for intercellular organelle transport. Science. 303:1007-1010.
49. Schuck, S., M. Honsho, K. Ekroos, A. Shevchenko, and K. Simons. 2003. Resistance of cell membranes to different detergents. Proc. Natl. Acad. Sci. USA. 100:5795-5800.
50. Siegel, J., K. Suhling. S. Lévêque-Fort, S. E. D. Webb, D. M. Davis, D. Phillips, Y. Sabharwal, and P. M. W. French. 2003. Wide-field time-resolved fluorescence anisotropy imaging (TR- FAIM): Imaging the rotational mobility of a fluorophore. Rev. Sci. Instrum. 74:182-192.
51. Simons, K., and E. Ikonen. 1997. Functional rafts in cell membranes. Nature. 387:569-572.
52. Simons, K., and W. L. Vaz. 2004, Model systems, lipid rafts, and cell membranes. Annu. Rev. Biophys. Biomol. Struct. 33:269-295.
53. Suhling, K., J. Siegel, P. M. P. Lanigan, S. Lévêque-Fort, S. E. D. Webb. D. Phillips, D. M. Davis, and P. M. W. French. 2004. Time-resolved fluorescence anisotropy imaging applied to live cells. Opt. Lett. 29:584-586.
54. Sund, S. E., J. A. Swanson, and D. Axelrod. 1999. Cell membrane orientation visualized by polarized total internal reflection fluorescence. Biophys. J. 77:2266-2283.
55. Szabo, A. 1980. Theory of polarized fluorescent emission in uniaxial liquid crystals. J. Chem. Phys. 72:4620-4626.
56. Thulstrup, E. W., and J. Michl. 1982. Orientation and linerar dichroism of symmetrical aromatic-molecules imbedded in streched polyethylene. J. Am. Chem. Soc. 104:5594-5604.
57. Toptygin, D., and L. Brand. 1993. Fluorescence decay of DPH in lipid membranes: influence of the external refractive index. Biophys. Chem. 48:205-220.
58. Tramier, M., K. Kemnitz, C. Durieux, J. Coppey, P. Denjean, R. B. Pansu, and M. Coppey-Moisan. 2000. Restrained torsional dynamics of nuclear DNA in living proliferative mammalian cells. Biophys. J. 78:2614-2627.
59. Tronin, A., J. Strzalka, X. Chen, P. L. Dutton, and J. K. Blasie. 2000. Determination of the porphyrin orientation distribution in Langmuir monolayers by polarized epifluorescence. Langmuir. 16:9878-9886.
60. Van der meer, B. W., R. P. H. Kooyman, and Y. K. Levine. 1982. A theory of fluorescence depolarization in macroscopic ally ordered membrane systems. Chem. Phys. 66:39-50.
61. Whitesides, G. M., and B. Grzybowski. 2002. Self-assembly at all scales. Science. 295:2418-2421.
62. Xiao, M., A. Tartakowski, O. A. Andreev, and J. Borejdo. 1996. Binding of S1(A1) and S1(A2) to F-actin. Biochemistry. 35:523-530.