Surveying protein structure and function using bis-arsenical small molecules

Accounts of Chemical Research

Volumn 44, Issue 9, 2011, Pages 654-665

  Scheck, Rebecca A ^a   Schepartz, Alanna ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BENZOXAZINE DERIVATIVE; CYSTEINE; FLUORESCEIN; FLUORESCENT DYE; ORGANOARSENIC DERIVATIVE; PROTEIN; XANTHENE DERIVATIVE;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CHEMISTRY; FLUORESCENCE RESONANCE ENERGY TRANSFER; METABOLISM; PHYSIOLOGY;

AMINO ACID SEQUENCE; ARSENICALS; BENZOXAZINES; BINDING SITES; CYSTEINE; FLUORESCEIN; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT DYES; PROTEINS; XANTHENES;

EID: 80053015715     PISSN: 00014842     EISSN: 15204898     Source Type: Journal    
DOI: 10.1021/ar2001028     Document Type: Article

References (69)

1. Jares-Erijman, E. A.; Jovin, T. M. Imaging molecular interactions in living cells by FRET microscopy Curr. Opin. Chem. Biol. 2006, 10 (5) 409-416 (Pubitemid 44375073)
2. Medintz, I. L.; Mattoussi, H. Quantum dot-based resonance energy transfer and its growing application in biology Phys. Chem. Chem. Phys. 2009, 11 (1) 17-45
3. Nomura, D. K.; Dix, M. M.; Cravatt, B. F. Activity-based protein profiling for biochemical pathway discovery in cancer Nat. Rev. Cancer 2010, 10 (9) 630-638
4. Heal, W. P.; Dang, T. H.; Tate, E. W. Activity-based probes: discovering new biology and new drug targets Chem. Soc. Rev. 2011, 40 (1) 246-257
5. Kerppola, T. K. Visualization of molecular interactions using bimolecular fluorescence complementation analysis: characteristics of protein fragment complementation Chem. Soc. Rev. 2009, 38 (10) 2876-2886
6. Prescher, J. A.; Contag, C. H. Guided by the light: visualizing biomolecular processes in living animals with bioluminescence Curr. Opin. Chem. Biol. 2010, 14 (1) 80-89
7. Ting, A. Y.; Thyagarajan, A. Imaging Activity-Dependent Regulation of Neurexin-Neuroligin Interactions Using trans-Synaptic Enzymatic Biotinylation Cell 2010, 143 (3) 456-469
8. Johnsson, K.; O'Hare, H. M.; Gautier, A. Chemical probes shed light on protein function Curr. Opin. Struct. Biol. 2007, 17 (4) 488-494 (Pubitemid 47451768)
9. Griffin, B.; Adams, S.; Tsien, R. Specific covalent labeling of recombinant protein molecules inside live cells Science 1998, 281 (5374) 269-272 (Pubitemid 28334512)
10. Adams, S. R.; Tsien, R. Y. Preparation of the membrane-permeant biarsenicals FlAsH-EDT2 and ReAsH-EDT2 for fluorescent labeling of tetracysteine-tagged proteins Nat. Protoc. 2008, 3 (9) 1527-1534
11. Hoffmann, C.; Gaietta, G.; Zurn, A.; Adams, S. R.; Terrillon, S.; Ellisman, M. H.; Tsien, R. Y.; Lohse, M. J. Fluorescent labeling of tetracysteine-tagged proteins in intact cells Nat. Protoc. 2010, 5 (10) 1666-1677
12. Pomorski, A.; Krezel, A. Exploration of biarsenical chemistry-challenges in protein research ChemBioChem 2011, 12 (8) 1152-1167
13. Tsien, R.; Adams, S.; Griffin, B.; Kerr, R.; Li, W.; Llopis, J.; Miyawaki, A.; Schafer, W.; Zlokarnik, G. Imaging protein interactions and gene expression in live cells Mol. Biol. Cell 1998, 9, 2A-2A
14. Hinner, M. J.; Johnsson, K. How to obtain labeled proteins and what to do with them Curr. Opin. Biotechnol. 2010, 21 (6) 766-776
15. Nakanishi, J.; Takarada, T.; Yunoki, S.; Kikuchi, Y.; Maeda, M. FRET-based monitoring of conformational change of the beta2 adrenergic receptor in living cells Biochem. Biophys. Res. Commun. 2006, 343 (4) 1191-1196
16. Andresen, M.; Schmitz-Salue, R.; Jakobs, S. Short tetracysteine tags to beta-tubulin demonstrate the significance of small labels for live cell imaging Mol. Biol. Cell 2004, 15 (12) 5616-5622 (Pubitemid 39564752)
17. Rudner, L.; Nydegger, S.; Coren, L. V.; Nagashima, K.; Thali, M.; Ott, D. E. Dynamic fluorescent imaging of human immunodeficiency virus type 1 gag in live cells by biarsenical labeling J. Virol. 2005, 79 (7) 4055-4065 (Pubitemid 40392503)
18. Hoffmann, C.; Gaietta, G.; Bunemann, M.; Adams, S. R.; Oberdorff-Maass, S.; Behr, B.; Vilardaga, J. P.; Tsien, R. Y.; Ellisman, M. H.; Lohse, M. J. A FlAsH-based FRET approach to determine G protein-coupled receptor activation in living cells Nat. Methods 2005, 2 (3) 171-176 (Pubitemid 41122123)
19. Roberti, M. J.; Bertoncini, C. W.; Klement, R.; Jares-Erijman, E. A.; Jovin, T. M. Fluorescence imaging of amyloid formation in living cells by a functional, tetracysteine-tagged alpha-synuclein Nat. Methods 2007, 4 (4) 345-351 (Pubitemid 46766980)
20. Dyachok, O.; Isakov, Y.; Sagetorp, J.; Tengholm, A. Oscillations of cyclic AMP in hormone-stimulated insulin-secreting beta-cells Nature 2006, 439 (7074) 349-352 (Pubitemid 43128861)
21. Enninga, J.; Mounier, J.; Sansonetti, P.; Tran Van Nhieu, G. Secretion of type III effectors into host cells in real time Nat. Methods 2005, 2 (12) 959-965 (Pubitemid 43108733)
22. Panchal, R. G.; Ruthel, G.; Kenny, T. A.; Kallstrom, G. H.; Lane, D.; Badie, S. S.; Li, L.; Bavari, S.; Aman, M. J. In vivo oligomerization and raft localization of Ebola virus protein VP40 during vesicular budding Proc. Natl. Acad. Sci. U.S.A. 2003, 100 (26) 15936-15941 (Pubitemid 38021093)
23. Wu, L.; Huang, T.; Yang, L.; Pan, J.; Zhu, S.; Yan, X. Sensitive and Selective Bacterial Detection Using Tetracysteine-Tagged Phages in Conjunction with Biarsenical Dye. Angew. Chem., Int. Ed. 2011, DOI: 10.1002/anie.201100334.
24. Spille, J. H.; Zurn, A.; Hoffmann, C.; Lohse, M. J.; Harms, G. S. Rotational diffusion of the alpha(2a) adrenergic receptor revealed by FlAsH labeling in living cells Biophys. J. 2011, 100 (4) 1139-1148
25. Pace, C. J.; Huang, Q.; Wang, F.; Palla, K. S.; Fuller, A. A.; Gao, J. A FlAsH-Tetracysteine Assay for Quantifying the Association and Orientation of Transmembrane alpha-Helices ChemBioChem 2011, 12 (7) 1018-1022
26. Ruan, F. Q.; Chen, Y. Q.; Itoh, K.; Sasaki, T.; Hopkins, P. B. Synthesis of Peptides Containing Unnatural, Metal-Ligating Residues-Aminodiacetic Acid as a Peptide Side-Chain J. Org. Chem. 1991, 56 (14) 4347-4354
27. Ghadiri, M. R.; Choi, C. Secondary Structure Nucleation in Peptides-Transition-Metal Ion Stabilized Alpha-Helices J. Am. Chem. Soc. 1990, 112 (4) 1630-1632
28. Adams, S.; Campbell, R.; Gross, L.; Martin, B.; Walkup, G.; Yao, Y.; Llopis, J.; Tsien, R. New biarsenical Ligands and tetracysteine motifs for protein labeling in vitro and in vivo: Synthesis and biological applications J. Am. Chem. Soc. 2002, 124 (21) 6063-6076 (Pubitemid 34552852)
29. Nelson, D. L.; Cox, M. M. Lehninger Principles of Biochemistry, 4 th ed.; W. H. Freeman and Company: New York, 2005.
30. Madani, F.; Lind, J.; Damberg, P.; Adams, S. R.; Tsien, R. Y.; Graslund, A. O. Hairpin Structure of a Biarsenical-Tetracysteine Motif Determined by NMR Spectroscopy J. Am. Chem. Soc. 2009, 131 (13) 4613-4615
31. Martin, B.; Giepmans, B.; Adams, S.; Tsien, R. Mammalian cell-based optimization of the biarsenical-binding tetracysteine motif for improved fluorescence and affinity Nat. Biotechnol. 2005, 23 (10) 1308-1314 (Pubitemid 41486860)
32. Ignatova, Z.; Gierasch, L. M. Monitoring protein stability and aggregation in vivo by real-time fluorescent labeling Proc. Natl. Acad. Sci. U.S.A. 2004, 101 (2) 523-528 (Pubitemid 38084669)
33. Taguchi, Y.; Shi, Z.-D.; Ruddy, B.; Dorward, D. W.; Greene, L.; Baron, G. S. Specific Biarsenical Labeling of Cell Surface Proteins Allows Fluorescent- and Biotin-tagging of Amyloid Precursor Protein and Prion Proteins Mol. Biol. Cell 2009, 20 (1) 233-244
34. Gaspersic, J.; Hafner-Bratkovic, I.; Stephan, M.; Veranic, P.; Bencina, M.; Vorberg, I.; Jerala, R. Tetracysteine-tagged prion protein allows discrimination between the native and converted forms FEBS J. 2010, 277 (9) 2038-2050
35. Hu, Y.; Su, B.; Kim, C.-S.; Hernandez, M.; Rostagno, A.; Ghiso, J.; Kim, J. R. A Strategy for Designing a Peptide Probe for Detection of beta-Amyloid Oligomers ChemBioChem 2010, 11 (17) 2409-2418
36. Ramdzan, Y. M.; Nisbet, R. M.; Miller, J.; Finkbeiner, S.; Hill, A. F.; Hatters, D. M. Conformation Sensors that Distinguish Monomeric Proteins from Oligomers in Live Cells Chem. Biol. 2010, 17 (4) 371-379
37. Hecht, M. H.; Richardson, J. S.; Richardson, D. C.; Ogden, R. C. Denovo Design, Expression, and Characterization of Felix-a 4-Helix Bundle Protein of Native-Like Sequence Science 1990, 249 (4971) 884-891
38. Parraga, G.; Horvath, S. J.; Eisen, A.; Taylor, W. E.; Hood, L.; Young, E. T.; Klevit, R. E. Zinc-Dependent Structure of a Single-Finger Domain of Yeast Adr1 Science 1988, 241 (4872) 1489-1492
39. Luedtke, N. W.; Dexter, R. J.; Fried, D. B.; Schepartz, A. Surveying polypeptide and protein domain conformation and association with FlAsH and ReAsH Nat. Chem. Biol. 2007, 3 (12) 779-784 (Pubitemid 350126876)
40. Shaikh, T. A.; Bakus, R. C.; Parkin, S.; Atwood, D. A. Structural characteristics of 2-halo-1,3,2-dithiarsenic compounds and tris- (pentafluorophenylthio)-arsen J. Organomet. Chem. 2006, 691 (9) 1825-1833
41. Goodman, J. L.; Fried, D. B.; Schepartz, A. Bipartite Tetracysteine Display Requires Site Flexibility for ReAsH Coordination ChemBioChem 2009, 10 (10) 1644-1647
42. Krishnan, B.; Gierasch, L. M. Cross-Strand Split Tetra-Cys Motifs as Structure Sensors in a beta-Sheet Protein Chem. Biol. 2008, 15 (10) 1104-1115
43. Ray-Saha, S.; Schepartz, A. Visualizing Tyrosine Kinase Activity with Bipartite Tetracysteine Display ChemBioChem 2010, 11 (15) 2089-2091
44. 2+ based on green fluorescent proteins and calmodulin Nature 1997, 388 (6645) 882-887 (Pubitemid 27377061)
45. Ting, A. Y.; Kain, K. H.; Klemke, R. L.; Tsien, R. Y. Genetically encoded fluorescent reporters of protein tyrosine kinase activities in living cells Proc. Natl. Acad. Sci. U.S.A. 2001, 98 (26) 15003-15008 (Pubitemid 34013959)
46. Gaietta, G. M.; Giepmans, B. N.; Deerinck, T. J.; Smith, W. B.; Ngan, L.; Llopis, J.; Adams, S. R.; Tsien, R. Y.; Ellisman, M. H. Golgi twins in late mitosis revealed by genetically encoded tags for live cell imaging and correlated electron microscopy Proc. Natl. Acad. Sci. U.S.A. 2006, 103 (47) 17777-17782 (Pubitemid 44852236)
47. Dexter, R. J.; Schepartz, A. Direct Visualization of Protein Association in Living Cells with Complex-Edited Electron Microscopy Angew. Chem., Int. Ed. 2010, 49 (43) 7952-7954
48. Chen, B.; Cao, H.; Yan, P.; Mayer, M. U.; Squier, T. C. Identification of an orthogonal peptide binding motif for biarsenical multiuse affinity probes Bioconjugate Chem. 2007, 18 (4) 1259-1265 (Pubitemid 47122649)
49. Miura, T.; Urano, Y.; Tanaka, K.; Nagano, T.; Ohkubo, K.; Fukuzumi, S. Rational design principle for modulating fluorescence properties of fluorescein-based probes by photoinduced electron transfer J. Am. Chem. Soc. 2003, 125 (28) 8666-8671 (Pubitemid 36858435)
50. Spagnuolo, C. C.; Massad, W.; Miskoski, S.; Menendez, G. O.; Garcia, N. A.; Jares-Erijman, E. A. Photostability and spectral properties of fluorinated fluoresceins and their biarsenical derivatives: a combined experimental and theoretical study Photochem. Photobiol. 2009, 85 (5) 1082-1088
51. Urano, Y.; Kamiya, M.; Kanda, K.; Ueno, T.; Hirose, K.; Nagano, T. Evolution of fluorescein as a platform for finely tunable fluorescence probes J. Am. Chem. Soc. 2005, 127 (13) 4888-4894 (Pubitemid 40489642)
52. Spagnuolo, C. C.; Vermeij, R. J.; Jares-Erijman, E. A. Improved photostable FRET-competent biarsenical-tetracysteine probes based on fluorinated fluoresceins J. Am. Chem. Soc. 2006, 128 (37) 12040-12041 (Pubitemid 44413816)
53. Cao, H.; Chen, B.; Squier, T. C.; Mayer, M. U. CrAsH: a biarsenical multi-use affinity probe with low non-specific fluorescence Chem. Commun. 2006, 24, 2601-2603
54. Soh, N. Selective chemical labeling of proteins with small fluorescent molecules based on metal-chelation methodology Sensors-Basel 2008, 8 (2) 1004-1024
55. Tour, O.; Adams, S. R.; Kerr, R. A.; Meijer, R. M.; Sejnowski, T. J.; Tsien, R. W.; Tsien, R. Y. Calcium Green FlAsH as a genetically targeted small-molecule calcium indicator Nat. Chem. Biol. 2007, 3 (7) 423-431 (Pubitemid 46956323)
56. Bhunia, A. K.; Miller, S. C. Labeling tetracysteine-tagged proteins with a SplAsH of color: A modular approach to bis-arsenical fluorophores ChemBioChem 2007, 8 (14) 1642-1645 (Pubitemid 47523664)
57. Wang, T.; Yan, P.; Squier, T. C.; Mayer, M. U. Prospecting the proteome: Identification of naturally occurring binding motifs for biarsenical probes ChemBioChem 2007, 8 (16) 1937
58. Van Engelenburg, S. B.; Nahreini, T.; Palmer, A. E. FACS-Based Selection of Tandem Tetracysteine Peptides with Improved ReAsH Brightness in Live Cells ChemBioChem 2010, 489-493
59. Levitus, M.; Ranjit, S. Cyanine dyes in biophysical research: the photophysics of polymethine fluorescent dyes in biomolecular environments Q. Rev. Biophys. 2011, 44 (1) 123-151
60. Yaron, D.; Silva, G. L.; Ediz, V.; Armitage, B. A. Experimental and computational investigation of unsymmetrical cyanine dyes: Understanding torsionally responsive fluorogenic dyes J. Am. Chem. Soc. 2007, 129 (17) 5710-5718 (Pubitemid 46697662)
61. Toutchkine, A.; Nguyen, D. V.; Hahn, K. M. Simple one-pot preparation of water-soluble, cysteine-reactive cyanine and merocyanine dyes for biological imaging Bioconjugate Chem. 2007, 18 (4) 1344-1348 (Pubitemid 47122659)
62. Cao, H.; Xiong, Y.; Wang, T.; Chen, B.; Squier, T. C.; Mayer, M. U. A red Cy3-based biarsenical fluorescent probe targeted to a complementary binding peptide J. Am. Chem. Soc. 2007, 129 (28) 8672
63. Langhorst, M. F.; Genisyuerek, S.; Stuermer, C. A. O. Accumulation of FlAsH/Lumio Green in active mitochondria can be reversed by beta-mercaptoethanol for specific staining of tetracysteine-tagged proteins Histochem. Cell Biol. 2006, 125 (6) 743-747 (Pubitemid 43780180)
64. Uttamapinant, C.; White, K. A.; Baruah, H.; Thompson, S.; Fernandez-Suarez, M.; Puthenveetil, S.; Ting, A. Y. A fluorophore ligase for site-specific protein labeling inside living cells Proc. Natl. Acad. Sci. U.S.A. 2010, 107 (24) 10914-10919
65. Kuivila, H. G.; Keough, A. H.; Soboczenski, E. J. Areneboronates from Diols and Polyols J. Org. Chem. 1954, 19 (5) 780-783
66. James, T. D.; Sandanayake, K. R. A. S.; Shinkai, S. Novel Photoinduced Electron-Transfer Sensor for Saccharides Based on the Interaction of Boronic Acid and Amine J. Chem. Soc., Chem. Commun. 1994, 4, 477-478
67. Cao, H. S.; Heagy, M. D. Fluorescent chemosensors for carbohydrates: A decade's worth of bright spies for saccharides in review J. Fluoresc. 2004, 14 (5) 569-584
68. James, T. D.; Shinkai, S. Artificial receptors as chemosensors for carbohydrates Host-Guest Chem. 2002, 218, 159-200
69. Halo, T. L.; Appelbaum, J.; Hobert, E. M.; Balkin, D. M.; Schepartz, A. Selective Recognition of Protein Tetraserine Motifs with a Cell-Permeable, Pro-fluorescent Bis-boronic Acid J. Am. Chem. Soc. 2009, 131 (2) 438-439