Solvatochromic Nile Red Probes with FRET Quencher Reveal Lipid Order Heterogeneity in Living and Apoptotic Cells

ACS Chemical Biology

Volumn 10, Issue 6, 2015, Pages 1435-1442

  Kreder, Rémy ^a   Pyrshev, Kyrylo A ^a,b   Darwich, Zeinab ^a   Kucherak, Oleksandr A ^a   Mély, Yves ^a   Klymchenko, Andrey S ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b PALLADIN INSTITUTE OF BIOCHEMISTRY   (Ukraine)

Author keywords

[No Author keywords available]

Indexed keywords

FLUORESCENT DYE; LIPID; LIPOSOME; NILE RED; OXAZINE DERIVATIVE;

ABSORPTION SPECTROSCOPY; APOPTOSIS; ARTICLE; CELL HETEROGENEITY; CELL MEMBRANE; CONFOCAL MICROSCOPY; FEMALE; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENCE SPECTROSCOPY; HUMAN; HUMAN CELL; HYDROPHOBICITY; LIPID MEMBRANE; LIPID RAFT; MOLECULAR PROBE; PRIORITY JOURNAL; QUANTUM YIELD; SYNTHESIS; ANIMAL; CELL SURVIVAL; CHEMICAL PHENOMENA; CHEMISTRY; CHO CELL LINE; CRICETULUS; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; PHASE TRANSITION; ULTRASTRUCTURE;

ANIMALS; APOPTOSIS; CELL SURVIVAL; CHO CELLS; CRICETULUS; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT DYES; HEK293 CELLS; HELA CELLS; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MEMBRANE MICRODOMAINS; OXAZINES; PHASE TRANSITION; UNILAMELLAR LIPOSOMES;

EID: 84930005560     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb500922m     Document Type: Article

References (58)

1. Dietrich, C., Bagatolli, L. A., Volovyk, Z. N., Thompson, N. L., Levi, M., Jacobson, K., and Gratton, E. (2001) Lipid rafts reconstituted in model membranes Biophys. J. 80, 1417
2. Baumgart, T., Hess, S. T., and Webb, W. W. (2003) Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension Nature 425, 821-824
3. Veatch, S. L. and Keller, S. L. (2003) Separation of liquid phases in giant vesicles of ternary mixtures of phospholipids and cholesterol Biophys. J. 85, 3074-3083
4. Baumgart, T., Hammond, A. T., Sengupta, P., Hess, S. T., Holowka, D. A., Baird, B. A., and Webb, W. W. (2007) Large-scale fluid/fluid phase separation of proteins and lipids in giant plasma membrane vesicles Proc. Natl. Acad. Sci. U.S.A. 104, 3165-3170
5. Veatch, S. L., Cicuta, P., Sengupta, P., Honerkamp-Smith, A., Holowka, D., and Baird, B. (2008) Critical fluctuations in plasma membrane vesicles ACS Chem. Biol. 3, 287-293
6. Simons, K. and Ikonen, E. (1997) Functional rafts in cell membranes Nature 387, 569
7. Lingwood, D. and Simons, K. (2010) Lipid rafts as a membrane-organizing principle Science 327, 46-50
8. Brown, D. A. and London, E. (2000) Structure and function of sphingolipid- and cholesterol-rich membrane raft J. Biol. Chem. 275, 17221
9. Staubach, S. and Hanisch, F. G. (2011) Lipid rafts: Signaling and sorting platforms of cells and their roles in cancer Expert Rev. Proteomics 8, 263-277
10. Munro, S. (2003) Lipid rafts: Elusive or illusive? Cell 115, 377
11. Hancock, J. F. (2006) Lipid rafts: Contentious only from simplistic standpoints Nat. Rev. Mol. Cell Biol. 7, 456-462
12. Truong-Quang, B. A. and Lenne, P. F. (2014) Membrane microdomains: From seeing to understanding Front. Plant Sci. 5, 18
13. Lozano, M. M., Liu, Z., Sunnick, E., Janshoff, A., Kumar, K., and Boxer, S. G. (2013) Colocalization of the ganglioside GM1 and cholesterol detected by secondary ion mass spectrometry J. Am. Chem. Soc. 135, 5620-5630
14. Goksu, E. I., Vanegas, J. M., Blanchette, C. D., Lin, W. C., and Longo, M. L. (2009) AFM for structure and dynamics of biomembranes Biochim. Biophys. Acta 1788, 254-266
15. Swamy, M. J., Ciani, L., Ge, M., Smith, A. K., Holowka, D., Baird, B., and Freed, J. H. (2006) Coexisting domains in the plasma membranes of live cells characterized by spin-label ESR spectroscopy Biophys. J. 90, 4452-4465
16. Suzuki, K. G. N., Fujiwara, T. K., Sanematsu, F., Iino, R., Edidin, M., and Kusumi, A. (2007) GPI-anchored receptor clusters transiently recruit Lyn and Gα for temporary cluster immobilization and Lyn activation: Single-molecule tracking study 1 J. Cell Biol. 177, 717-730
17. Goswami, D., Gowrishankar, K., Bilgrami, S., Ghosh, S., Raghupathy, R., Chadda, R., Vishwakarma, R., Rao, M., and Mayor, S. (2008) Nanoclusters of GPI-anchored proteins are formed by cortical actin-driven activity Cell 135, 1085-1097
18. Bader, A. N., Hoetzl, S., Hofman, E. G., Voortman, J., Van Bergen En Henegouwen, P. M. P., Van Meer, G., and Gerritsen, H. C. (2011) Homo-FRET imaging as a tool to quantify protein and lipid clustering ChemPhysChem 12, 475-483
19. Kenworthy, A. K., Petranova, N., and Edidin, M. (2000) High-resolution FRET microscopy of cholera toxin B-subunit and GPI- anchored proteins in cell plasma membranes Mol. Biol. Cell 11, 1645-1655
20. Lasserre, R., Guo, X. J., Conchonaud, F., Hamon, Y., Hawchar, O., Bernard, A. M., Soudja, S. M. H., Lenne, P. F., Rigneault, H., Olive, D., Bismuth, G., Nunès, J. A., Payrastre, B., Marguet, D., and He, H. T. (2008) Raft nanodomains contribute to Akt/PKB plasma membrane recruitment and activation Nat. Chem. Biol. 4, 538-547
21. Bacia, K., Scherfeld, D., Kahya, N., and Schwille, P. (2004) Fluorescence correlation spectroscopy relates rafts in model and native membranes Biophys. J. 87, 1034-1043
22. Eggeling, C., Ringemann, C., Medda, R., Schwarzmann, G., Sandhoff, K., Polyakova, S., Belov, V. N., Hein, B., Von Middendorff, C., Schönle, A., and Hell, S. W. (2009) Direct observation of the nanoscale dynamics of membrane lipids in a living cell Nature 457, 1159-1162
23. Sengupta, P., Jovanovic-Talisman, T., Skoko, D., Renz, M., Veatch, S. L., and Lippincott-Schwartz, J. (2011) Probing protein heterogeneity in the plasma membrane using PALM and pair correlation analysis Nat. Methods 8, 969-975
24. Wilmes, S., Staufenbiel, M., Liße, D., Richter, C. P., Beutel, O., Busch, K. B., Hess, S. T., and Piehler, J. (2012) Triple-color super-resolution imaging of live cells: Resolving submicroscopic receptor organization in the plasma membrane Angew. Chem., Int. Ed. 51, 4868-4871
25. Adler, J., Shevchuk, A. I., Novak, P., Korchev, Y. E., and Parmryd, I. (2010) Plasma membrane topography and interpretation of single-particle tracks Nat. Methods 7, 170-171
26. Lillemeier, B. F., Mörtelmaier, M. A., Forstner, M. B., Huppa, J. B., Groves, J. T., and Davis, M. M. (2010) TCR and Lat are expressed on separate protein islands on T cell membranes and concatenate during activation Nat. Immunol. 11, 90-96
27. Kusumi, A., Nakada, C., Ritchie, K., Murase, K., Suzuki, K., Murakoshi, H., Kasai, R. S., Kondo, J., and Fujiwara, T. (2005) Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: High-speed single-molecule tracking of membrane molecules Annu. Rev. Biophys. Biomol. Struct. 34, 351-378
28. Sengupta, P., Holowka, D., and Baird, B. (2007) Fluorescence resonance energy transfer between lipid probes detects nanoscopic heterogeneity in the plasma membrane of live cells Biophys. J. 92, 3564-3574
29. Owen, D. M., Williamson, D. J., Magenau, A., and Gaus, K. (2012) Sub-resolution lipid domains exist in the plasma membrane and regulate protein diffusion and distribution Nat. Commun. 3, 1256
30. Brameshuber, M., Weghuber, J., Ruprecht, V., Gombos, I., Horváth, I., Vigh, L., Eckerstorfer, P., Kiss, E., Stockinger, H., and Schütz, G. J. (2010) Imaging of mobile long-lived nanoplatforms in the live cell plasma membrane J. Biol. Chem. 285, 41765-41771
31. Klymchenko, A. S. and Kreder, R. (2014) Fluorescent probes for lipid rafts: From model membranes to living cells Chem. Biol. 21, 97-113
32. Dietrich, C., Yang, B., Fujiwara, T., Kusumi, A., and Jacobson, K. (2002) Relationship of lipid rafts to transient confinement zones detected by single particle tracking Biophys. J. 82, 274-284
33. Baumgart, T., Hunt, G., Farkas, E. R., Webb, W. W., and Feigenson, G. W. (2007) Fluorescence probe partitioning between Lo/Ld phases in lipid membranes Biochim. Biophys. Acta 1768, 2182-2194
34. Sezgin, E., Levental, I., Grzybek, M., Schwarzmann, G., Mueller, V., Honigmann, A., Belov, V. N., Eggeling, C., Coskun, Ü., Simons, K., and Schwille, P. (2012) Partitioning, diffusion, and ligand binding of raft lipid analogs in model and cellular plasma membranes Biochim. Biophys. Acta 1818, 1777-1784
35. Xu, X., Bittman, R., Duportail, G., Heissler, D., Vilcheze, C., and London, E. (2001) Effect of the structure of natural sterols and sphingolipids on the formation of ordered sphingolipid/sterol domains (rafts). Comparison of cholesterol to plant, fungal, and disease-associated sterols and comparison of sphingomyelin, cerebrosides, and ceramide J. Biol. Chem. 276, 33540-33546
36. Doval, D. A., Fin, A., Takahashi-Umebayashi, M., Riezman, H., Roux, A., Sakai, N., and Matile, S. (2012) Amphiphilic dynamic NDI and PDI probes: Imaging microdomains in giant unilamellar vesicles Org. Biomol. Chem. 10, 6087-6093
37. Bagatolli, L. A. (2006) To see or not to see: Lateral organization of biological membranes and fluorescence microscopy Biochim. Biophys. Acta 1758, 1541-1556
38. Owen, D. M., Rentero, C., Magenau, A., Abu-Siniyeh, A., and Gaus, K. (2012) Quantitative imaging of membrane lipid order in cells and organisms Nat. Protoc. 7, 24-35
39. Hwan, M. K., Byeong, H. J., Hyon, J. Y., Myoung, J. A., Mun, S. S., Jin, H. H., Lee, K. J., Chul, H. K., Joo, T., Hong, S. C., and Bong, R. C. (2008) Two-photon fluorescent turn-on probe for lipid rafts in live cell and tissue J. Am. Chem. Soc. 130, 4246-4247
40. Jin, L., Millard, A. C., Wuskell, J. P., Dong, X., Wu, D., Clark, H. A., and Loew, L. M. (2006) Characterization and application of a new optical probe for membrane lipid domains Biophys. J. 90, 2563-2575
41. Oncul, S., Klymchenko, A. S., Kucherak, O. A., Demchenko, A. P., Martin, S., Dontenwill, M., Arntz, Y., Didier, P., Duportail, G., and Mely, Y. (2010) Liquid ordered phase in cell membranes evidenced by a hydration-sensitive probe: Effects of cholesterol depletion and apoptosis Biochim. Biophys. Acta 1798, 1436-1443
42. Klymchenko, A. S., Oncul, S., Didier, P., Schaub, E., Bagatolli, L., Duportail, G., and Mély, Y. (2009) Visualization of lipid domains in giant unilamellar vesicles using an environment-sensitive membrane probe based on 3-hydroxyflavone Biochim. Biophys. Acta 1788, 495-499
43. Darwich, Z., Klymchenko, A. S., Kucherak, O. A., Richert, L., and Mély, Y. (2012) Detection of apoptosis through the lipid order of the outer plasma membrane leaflet Biochim. Biophys. Acta 1818, 3048-3054
44. Kucherak, O. A., Oncul, S., Darwich, Z., Yushchenko, D. A., Arntz, Y., Didier, P., Mely, Y., and Klymchenko, A. S. (2010) Switchable nile red-based probe for cholesterol and lipid order at the outer leaflet of biomembranes J. Am. Chem. Soc. 132, 4907
45. Demchenko, A. P., Mély, Y., Duportail, G., and Klymchenko, A. S. (2009) Monitoring biophysical properties of lipid membranes by environment-sensitive fluorescent probes Biophys. J. 96, 3461-3470
46. London, E. (2002) Insights into lipid raft structure and formation from experiments in model membranes Curr. Opin. Struct. Biol. 12, 480-486
47. Loura, L. M. S. and Prieto, M. (2011) FRET in membrane biophysics: An overview. Front. Physiol. 2, art. no. 82, DOI: 10.3389/fphys.2011.00082.
48. Sapsford, K. E., Berti, L., and Medintz, I. L. (2006) Materials for fluorescence resonance energy transfer analysis: Beyond traditional donor-acceptor combinations Angew. Chem., Int. Ed. 45, 4562-4588
49. Ahmed, S. N., Brown, D. A., and London, E. (1997) On the origin of sphingolipid/cholesterol-rich detergent-insoluble cell membranes: Physiological concentrations of cholesterol and sphingolipid induce formation of a detergent-insoluble, liquid-ordered lipid phase in model membranes Biochemistry 36, 10944-10953
50. Hengartner, M. O. (2000) The biochemistry of apoptosis Nature 407, 770-776
51. Sankaram, M. B. and Thompson, T. E. (1990) Interaction of cholesterol with various glycerophospholipids and sphingomyelin Biochemistry 29, 10670-10675
52. Darwich, Z., Klymchenko, A. S., Dujardin, D., and Mély, Y. (2014) Imaging lipid order changes in endosome membranes of live cells by using a Nile Red-based membrane probe RSC Adv. 4, 8481-8488
53. Ong, C. C., Jubb, A. M., Haverty, P. M., Zhou, W., Tran, V., Truong, T., Turley, H., OBrien, T., Vucic, D., Harris, A. L., Belvin, M., Friedman, L. S., Blackwood, E. M., Koeppen, H., and Hoeflich, K. P. (2011) Targeting p21-activated kinase 1 (PAK1) to induce apoptosis of tumor cells Proc. Natl. Acad. Sci. U.S.A. 108, 7177-7182
54. Zwaal, R. F. A. and Schroit, A. J. (1997) Pathophysiologic implications of membrane phospholipid asymmetry in blood cells Blood 89, 1121-1132
55. Tepper, A. D., Ruurs, P., Wiedmer, T., Sims, P. J., Borst, J., and Van Blitterswijk, W. J. (2000) Sphingomyelin hydrolysis to ceramide during the execution phase of apoptosis results from phospholipid scrambling and alters cell-surface morphology J. Cell Biol. 150, 155-164
56. Coleman, M. L., Sahai, E. A., Yeo, M., Bosch, M., Dewar, A., and Olson, M. F. (2001) Membrane blebbing during apoptosis results from caspase-mediated activation of ROCK I Nat. Cell Biol. 3, 339-345
57. Sebbagh, M., Renvoizé, C., Hamelin, J., Riché, N., Bertoglio, J., and Bréard, J. (2001) Caspase-3-mediated cleavage of ROCK I induces MLC phosphorylation and apoptotic membrane blebbing Nat. Cell Biol. 3, 346-352
58. Krysko, D. V., Vanden Berghe, T., DHerde, K., and Vandenabeele, P. (2008) Apoptosis and necrosis: Detection, discrimination and phagocytosis Methods 44, 205-221