Fluorescence and Bioluminescence Genetically Encoded Probes for Imaging Protein Conformational Changes and Interactions in Living Cells and Animals

JALA - Journal of the Association for Laboratory Automation

Volumn 15, Issue 5, 2010, Pages 396-404

  Awais, Muhammad ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Bioluminescence; Fluorescence resonance energy transfer; Protein conformational changes; Protein fragment complementation; Single living cells

Indexed keywords

CELL BIOLOGISTS; CONFORMATIONAL CHANGE; FLUORESCENCE AND LUMINESCENCE; FLUORESCENCE RESONANCE ENERGY TRANSFER; HIGH-THROUGHPUT ASSAYS; LIVE CELL; LIVING CELL; MOLECULAR EVENTS; POTENTIAL DRUG; PROTEIN LOCALIZATION; PROTEIN-PROTEIN INTERACTIONS; RAPID ADVANCEMENT; REAL TIME; SMALL MOLECULES; TEMPORAL RESOLUTION;

ANIMALS; BIOLUMINESCENCE; CONFORMATIONS; ENERGY TRANSFER; PHOSPHORESCENCE; PROBES; RESONANCE;

FLUORESCENCE;

CELL NUCLEUS RECEPTOR; DEXAMETHASONE; ENDOCRINE DISRUPTOR; ESTRADIOL; GREEN FLUORESCENT PROTEIN; HYDROCORTISONE; LUCIFERASE; MIFEPRISTONE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROGESTERONE; STEROID RECEPTOR; TESTOSTERONE;

ACETYLATION; ARTICLE; BIOLUMINESCENCE; CYTOLOGY; FLUORESCENCE IMAGING; FLUORESCENCE MICROSCOPE; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE EXPRESSION; GENETIC VARIABILITY; HIGH THROUGHPUT SCREENING; HYDROPHOBICITY; MOLECULAR DYNAMICS; MOLECULAR PROBE; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; SIGNAL TRANSDUCTION;

EID: 77956884648     PISSN: 15355535     EISSN: 15402452     Source Type: Journal    
DOI: 10.1016/j.jala.2010.04.001     Document Type: Article

References (64)

1. Simamura O., Johnson F.H., Saiga Y. Extraction, purification and properties of aequorin, a bioluminescent protein from the luminous hydromedusan, Aequorea. J. Cell. Comp. Physiol. 1962, 59:223-239.
2. Cody C.W., Prasher D.C., Westler W.M., Prendergast F.G., Ward W.W. Chemical structure of the hexapeptide chromophore of the Aequorea green-fluorescent protein. Biochemistry 1993, 32:1212-1218.
3. Prasher D.C., Eckenrode V.K., Ward W.W., Prendergast F.G., Cormier M.J. Primary structure of the Aequorea victoria green-fluorescent protein. Gene 1992, 11:229-233.
4. Chalfie M., Tu Y., Euskirchen G., Ward W.W., Prasher D.C. Green fluorescent protein as a marker for gene expression. Science 1994, 263:802-805.
5. Heim R., Prasher D.C., Tsien R.Y. Wavelength mutations and posttranslational autoxidation of green fluorescent protein. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:12501-12504.
6. Matz M.V., Fradkov A.F., Labas Y.A., Savitasky A.P., Zaraissky A.G., Markelov M.L., Lukyanov S.A. Fluorescent proteins from nonbioluminescent Anthozoa species. Nat. Biotechnol. 1999, 17:969-973.
7. Lukyanov K.A., Fradkov A.F., Gurskaya N.G., Matz M.V., Labas Y.A., Savitasky A.P., Markelov M.L., Zaraisky A.G., Zhao X., Fang Y., Tan W., Lukyanov S.A. Natural animal coloration can be determined by a nonfluorescent green fluorescent protein homolog. J. Biol. Chem. 2000, 275:25879-25882.
8. Nagai T., Ibata K., Park E.S., Kubata M., Mikoshiba K., Miyawaki A. A variant of yellow fluorescent protein with fast and efficient maturation for cell-biology application. Nat. Biotechnol. 2002, 20:87-90.
9. Shaner N.C., Campbell R.E., Steinbach P.A., Giepmans B.N.G., Palmer A.E., Tsien R.Y. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. 2004, 22:1567-1572.
10. Kredel S., Oswald F., Nienhaus K., Deuschle K., Roecker C., Wolff M., Heilker R., Nienhaus G.U., Wiedenmann J. mRuby, a bright monomeric red fluorescent protein for labeling of subcellular structures. PLoS ONE 2009, 4. e4391.
11. Shu X., Royant A., Lin M.Z., Aguilera T.A., Lev-Ram V., Steinbach P.A., Tsien R.Y. Mammalian expression of infrared fluorescent proteins engineered from a bacterial phytochrome. Science 2009, 324:804-807.
12. Lukyanov K.A., Chudakov D.M., Lukyanov S., Verkhusha V.V. Photoactivatable fluorescent proteins. Nat. Rev. Mol. Cell Biol. 2005, 6:885-891.
13. Sample V., Newman R.H., Zhang J. The structure and function of fluorescent proteins. Chem. Soc. Rev. 2009, 38:2852-2864.
14. Frommer W.B., Davidson M.W., Campbell R.E. Genetically encoded biosensors based on engineering fluorescent proteins. Chem. Soc. Rev. 2009, 38:2833-2841.
15. Ciruela F. Fluorescence-based methods in the study of protein-protein interactions in living cells. Curr. Opin. Biotechnol. 2008, 19:338-343.
16. Piston D.W., Kremers G.J. Fluorescent protein FRET: the good, the bad and the ugly. Trends Biochem. Sci. 2007, 32:407-414.
17. Truong K., Ikura M. The use of FRET imaging microscopy to detect protein-protein interactions and protein conformational changes in vivo. Curr. Opin. Struct. Biol. 2001, 11:573-578.
18. Romoser V.A., Hinkle P.M., Persechini A. Detection in living cells of Ca2+-dependent changes in the fluorescence emission of an indicator composed of two green fluorescent protein variants linked by a calmodulin-binding sequence. A new class of fluorescent indicators. J. Biol. Chem. 1997, 272:13270-13274.
19. Miyawaki A., Llopis J., Heim R., McCaffery J.M., Adams J.A., Ikura M., Tsien R.Y. Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 1997, 388:882-887.
20. Kuner T., Augustine G.J. A genetically encoded ratiometric indicator for chloride: capturing chloride transients in cultured hippocampal neurons. Neuron 2000, 27:447-459.
21. Nikolaev V.O., Bünemann M., Hein L., Hannawacker A., Lohse M.J. Novel single chain cAMP sensors for receptor-induced signal propagation. J. Biol. Sci. 2004, 279:37215-37218.
22. Sato M., Hida N., Ozawa T., Umezawa Y. Fluorescent indicators for cyclic GMP based on cyclic GMP-dependent protein kinase Iα and green fluorescent proteins. Anal. Chem. 2000, 72:5918-5924.
23. Nagai Y., Miyazaki M., Aoki R., Zama T., Inouye S., Hirose K., Iino M., Hagiwara M. A fluorescent indicator for visualizing cAMP-induced phosphorylation in vivo. Nat. Biotechnol. 2000, 18:313-316.
24. Sato M., Ozawa T., Inukai K., Asano T., Umezawa Y. Fluorescent indicators for imaging protein phosphorylation in single living cells. Nat. Biotechnol. 2002, 20:287-294.
25. Sasaki K., Sato M., Umezawa Y. Fluorescent indicator for Akt/protein kinase B and dynamics of Akt activity visualized in living cells. J. Biol. Chem. 2003, 278:30945-30951.
26. Sasaki K., Ito T., Nishino N., Khochbin S., Yoshida M. Real-time imaging of histone H4 hyperacetylation in living cells. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:16257-16262.
27. Newman R.H., Zhang J. Visualization of phosphatase activity in living cells with a FRET-based calcineurin activity sensor. Mol. Biosyst. 2008, 4:496-501.
28. Tsutsui H., Karasawa S., Okamura Y., Miyawaki A. Improving membrane voltage measurements using FRET with new fluorescent proteins. Nat. Methods 2008, 5:683-685.
29. Zhang X., Lanter J.C., Sui Z. Recent advances in the development of selective androgen receptor modulators. Expert Opin. Ther. Pat. 2009, 19:1239-1258.
30. Narayanan R., Yepuru M., Szafran A.T., Szwarc M., Bohl C.E., Young N.L., Miller D.D., Mancini M.A., Dalton J.T. Discovery and mechanistic characterization of a novel selective nuclear androgen receptor exporter for the treatment of prostate cancer. Cancer Res. 2010, 70:842-851.
31. Biggadike K., Bledsoe R.K., Coe D.M., Cooper T.W.J., House D., Iannone M.A., Macdonal S.J.F., Madauss K.P., McLay I.M., Shipley T.J., Taylor S.J., Tran T.B., Uings I.J., Weller V., Williams S.P. Design and X-ray crystal structures of high-potency nonsteroidal glucocorticoid agonists exploiting a novel binding site on the receptor. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:18114-18119.
32. Smith C.L., O'Malley B.W. Coregulator function: a key to understanding tissue specificity of selective receptor modulator. Endocr. Rev. 2004, 25:45-71.
33. Gronemeyer H., Gustafsson J., Laudet V. Principles for modulation of the nuclear receptor superfamily. Nat. Rev. Drug Discov. 2004, 3:950-964.
34. Greschik H., Moras D. Structure-activity relationship of nuclear receptor-ligand interactions. Curr. Top. Med. Chem. 2003, 3:1573-1599.
35. Heery D.M., Kalkhoven E., Hoare S., Parker M.G. A signature motif in transcriptional co-activators mediates binding to nuclear receptors. Nature 1997, 387:733-736.
36. Shiau A.K., Barstad D., Loria P.M., Cheng L., Kushner P.J., Agard D.A., Greene G.L. The structural basis of estrogen receptor/coactivator recognition and antagonism of this interaction by tamoxifen. Cell 1998, 95:927-937.
37. Bourguet W., Vivat V., Wurtz J.M., Chambon P., Gronemeyer H., Moras D. Crystal structure of a heterodimeric complex of RAR and RXR ligand-binding domains. Mol. Cell 2000, 5:289-298.
38. Nagy L., Kao H.Y., Love J.D., Li C., Banayo E., Gooch J.T., Krishna V., Chatterjee K., Evans R.M., Schwabe J.W.R. Mechanism of corepressor binding and release from nuclear hormone receptors. Genes Dev. 1999, 13:3209-3216.
39. Xu H.E., Stanley T.B., Montana V.G., Lambert M.H., Shearer B.G., Cobb J.E., Mckee D.D., Galardi C.M., Plunket K.D., Nolte R.T., Parks D.J., Moore J.T., Kliewer S.A., Willson T.M., Stimmel J.B. Structural basis for antagonist-mediated recruitment of nuclear corepressors by PPARα. Nature 2002, 415:813-817.
40. Wang Q., Blackford J.A., Song L.N., Huang Y., Cho S., Simons S.S. Equilibrium interactions of corepressors and coactivators with agonist and antagonist complexes of glucocorticoid receptors. Mol. Endocrinol. 2004, 18:1376-1395.
41. Liu Z., Auboeuf D., Wong J., Chen J.D., Tsai S.Y., Tsai M.J., O'Malley B.W. Coactivator/corepressor ratios modulate PR-mediated transcription by the selective receptor modulator RU486. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:7040-7944.
42. Awais M., Sato M., Umezawa Y. Imaging of selective nuclear receptor modulator-induced conformational changes in the nuclear receptor to interact with coactivator and corepressor proteins in living cells. Chembiochem 2007, 8:737-743.
43. Awais M., Sato M., Lee X., Umezawa Y. A fluorescent indicator to visualize activities of the androgen receptor ligands in single living cells. Angew. Chem. Int. Ed. Engl. 2006, 45:2707-2712.
44. Awais M., Sato M., Sasaki K., Umezawa Y. A genetically encoded fluorescent indicator capable of discriminating estrogen agonists from antagonists in living cells. Anal. Chem. 2004, 76:2181-2186.
45. Awais M., Sato M., Umezawa Y. Optical probes to identify the glucocorticoid receptor ligands in living cells. Steroids 2007, 72:949-954.
46. Awais M., Sato M., Umezawa Y. A fluorescent indicator to visualize ligand-induced receptor/coactivator interactions for screening of peroxisome proliferator-activated receptor γ ligands in living cells. Biosen. Bioelect. 2007, 22:2564-2569.
47. Gaido K.W., Leonard L.S., Lovell S., Gould J.C., Babia D., Portier C.J., McDonnell D.P. Evaluation of chemicals with endocrine modulating activity in a yeast-based steroid hormones receptor gene transcription assay. Toxicol. Appl. Pharmacol. 1997, 143:205-212.
48. Korach K.S. Surprising places of estrogenic activity. Endocrinology 1993, 132:2277-2278.
49. Shelby M.D., Newbold R.R., Tully D.B., Chae K., Davis V.L. Assessing environmental chemicals for estrogenicity using a combination of in vitro and in vivo assays. Environ. Health Perspect. 1996, 104:1296-1300.
50. Oosterkamp A.J., Hock B., Seifert M., Irth H. Novel monitoring strategies for xenoestrogens. Trends Analyt. Chem. 1997, 16:544-553.
51. Sonnenschein C., Soto A.M. An updated review of environmental estrogen and androgen mimics and antagonists. J. Steroid Biochem. Mol. Biol. 1998, 65:143-150.
52. Colborn T. Environmental estrogens: health implications for humans and wildlife. Environ. Health Perspect. 1995, 103:135-136.
53. Neubert D. Vulnerability of the endocrine system to xenobiotic influence. Regul. Toxicol. Pharmacol. 1997, 26:9-29.
54. Daston G.P., Gooch J.W., Berslin W.J., Shuey D.L., Nikiforov A.I., Fico T.A., Gorsuch J.W. Environmental estrogens and reproductive health: a discussion of the human and environmental data. Reprod. Toxicol. 1997, 11:465-481.
55. Furukawa T., Bai C.X., Kaihara A., Ozaki E., Kawano T., Nakaya Y., Awais M., Sato M., Umezawa Y., Furukawa J. Ginsenoside Re, a main phytosterol of Panax ginseng, activates cardiac potassium channels via a non-genomic pathway of sex hormones. Mol. Pharmacol. 2006, 70:1916-1924.
56. Michnick S.W., Ear P.H., Manderson E.N., Remy I., Stefan E. Universal strategies in research and drug discovery based on protein-fragment complementation assays. Nat. Rev. Drug Discov. 2007, 6:569-582.
57. Binkowski B., Fan F., Wood K. Engineered luciferases for molecular sensing in living cells. Curr. Opin. Biotechnol. 2009, 20:14-18.
58. Ozawa T. Designing split reporter proteins for analytical tools. Anal. Chem. Acta 2006, 556:58-68.
59. Ozawa T., Natori Y., Sato M., Umezawa Y. Imaging dynamics of endogenous mitochondrial RNA in single living cells. Nat. Methods 2007, 4:413-419.
60. Hida N., Awais M., Takeuchi M., Ueno N., Tashiro M., Takagi C., Ozawa T. High-sensitivity real-time imaging of dual protein-protein interactions in living subjects using multicolor luciferases. PLoS ONE 2009, 4. e5868.
61. Kanno A., Yamanaka Y., Hirano H., Umezawa Y., Ozawa T. Cyclic luciferases for real-time sensing of caspase-3 activities in living mice. Angew. Chem. Int. Ed. Engl. 2007, 46:7595-7599.
62. Kim S.B., Ozawa T., Watanabe S., Umezawa Y. High-throughput sensing and noninvasive imaging of protein nuclear transport by using reconstitution of split Renilla luciferase. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:11542-11547.
63. Paulmurugan R., Gambhir S.S. An intramolecular folding sensor for imaging estrogen receptor-ligand interactions. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:15883-15888.
64. Kim S.B., Awais M., Sato M., Umezawa Y., Tao H. Integrated molecule-format bioluminescence probe for visualizing androgenicity of ligands based on the intramolecular association of androgen receptor with its recognition peptide. Anal. Chem. 2007, 79:1874-1880.