Optimized design and synthesis of a cell-permeable biarsenical cyanine probe for imaging tagged cytosolic bacterial proteins

Bioconjugate Chemistry

Volumn 24, Issue 2, 2013, Pages 251-259

  Fu, Na ^a   Xiong, Yijia ^a   Squier, Thomas C ^a  

^a PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHESIS; ESTERS; FLUORESCENCE; IMAGE PROCESSING; PROBES; SCAFFOLDS (BIOLOGY);

ALKYL CHAIN; CAPPING REAGENTS; CELL-PERMEABLE; CYANINE DYES; CYTOSOLIC; CYTOSOLIC PROTEINS; LABELINGS; METHOXY; OPTIMIZED DESIGNS; OPTIMIZED SYNTHESIS;

PROTEINS;

ALKYL GROUP; ARSENIC; BACTERIAL PROTEIN; CARBENE; CYANINE DYE; ESTER DERIVATIVE; RNA POLYMERASE;

ARTICLE; CELL LABELING; CELL MEMBRANE PERMEABILITY; CHEMICAL STRUCTURE; CLONING; CONTROLLED STUDY; CYTOSOL; ESCHERICHIA COLI; FLUORESCENCE IMAGING; MOLECULAR PROBE; NONHUMAN; SYNTHESIS;

EID: 84874073602     PISSN: 10431802     EISSN: 15204812     Source Type: Journal    
DOI: 10.1021/bc300619m     Document Type: Article

References (50)

1. George, N., Pick, H., Vogel, H., Johnsson, N., and Johnsson, K. (2004) Specific labeling of cell surface proteins with chemically diverse compounds J. Am. Chem. Soc. 126, 8896-8897
2. Johnsson, N. and Johnsson, K. (2003) A fusion of disciplines: Chemical approaches to exploit fusion proteins for functional genomics ChemBioChem 4, 803-810
3. Juillerat, A., Gronemeyer, T., Keppler, A., Gendreizig, S., Pick, H., Vogel, H., and Johnsson, K. (2003) Directed evolution of O-6-alkylguanine-DNA alkyltransferase for efficient labeling of fusion proteins with small molecules in vivo Chem. Biol. 10, 313-317
4. Keppler, A., Pick, H., Arrivoli, C., Vogel, H., and Johnsson, K. (2004) Labeling of fusion proteins with synthetic fluorophores in live cells Proc. Natl. Acad. Sci. U.S.A. 101, 9955-9959
5. Kindermann, M., Sielaff, I., and Johnsson, K. (2004) Synthesis and characterization of bifunctional probes for the specific labeling of fusion proteins Bioorg. Med. Chem. Lett. 14, 2725-2728
6. Los, G. V., Encell, L. P., McDougall, M. G., Hartzell, D. D., Karassina, N., Zimprich, C., Wood, M. G., Learish, R., Ohana, R. F., Urh, M., Simpson, D., Mendez, J., Zimmerman, K., Otto, P., Vidugiris, G., Zhu, J., Darzins, A., Klaubert, D. H., Bulleit, R. F., and Wood, K. V. (2008) HaloTag: a novel protein labeling technology for cell imaging and protein analysis ACS Chem. Biol. 3, 373-382
7. Adams, S. R., Campbell, R. E., Gross, L. A., Martin, B. R., Walkup, G. K., Yao, Y., Llopis, J., and Tsien, R. Y. (2002) New biarsenical ligands and tetracysteine motifs for protein labeling in vitro and in vivo: synthesis and biological applications J. Am. Chem. Soc. 124, 6063-6076
8. Cao, H., Chen, B., Squier, T. C., and Mayer, M. U. (2006) CrAsH: a biarsenical multi-use affinity probe with low non-specific fluorescence Chem. Commun.(Camb) 2601-2603
9. Cao, H., Xiong, Y., Wang, T., Chen, B., Squier, T. C., and Mayer, M. U. (2007) A red cy3-based biarsenical fluorescent probe targeted to a complementary binding peptide J. Am. Chem. Soc. 129, 8672-8673
10. Griffin, B. A., Adams, S. R., and Tsien, R. Y. (1998) Specific covalent labeling of recombinant protein molecules inside live cells Science 281, 269-272
11. Pomorski, A. and Krezel, A. (2011) Exploration of biarsenical chemistry - challenges in protein research ChemBioChem 12, 1152-1167
12. Kindermann, M., George, N., Johnsson, N., and Johnsson, K. (2003) Covalent and selective immobilization of fusion proteins J. Am. Chem. Soc. 125, 7810-7811
13. Andresen, M., Schmitz-Salue, R., and Jakobs, S. (2004) Short tetracysteine tags to beta-tubulin demonstrate the significance of small labels for live cell imaging Mol. Biol. Cell 15, 5616-5622
14. Griffin, B. A., Adams, S. R., Jones, J., and Tsien, R. Y. (2000) Fluorescent labeling of recombinant proteins in living cells with FlAsH Methods Enzymol. 327, 565-578
15. Chen, B., Cao, H., Yan, P., Mayer, M. U., and Squier, T. C. (2007) Identification of an orthogonal peptide binding motif for biarsenical multiuse affinity probes Bioconjugate Chem. 18, 1259-1265
16. Zurn, A., Klenk, C., Zabel, U., Reiner, S., Lohse, M. J., and Hoffmann, C. (2010) Site-specific, orthogonal labeling of proteins in intact cells with two small biarsenical fluorophores Bioconjugate Chem. 21, 853-859
17. Verma, S., Xiong, Y., Mayer, M. U., and Squier, T. C. (2007) Remodeling of the bacterial RNA polymerase supramolecular complex in response to environmental conditions Biochemistry 46, 3023-3035
18. Jin, D. J. and Cabrera, J. E. (2006) Coupling the distribution of RNA polymerase to global gene regulation and the dynamic structure of the bacterial nucleoid in Escherichia coli J. Struct. Biol. 156, 284-291
19. Mujumdar, R. B., Ernst, L. A., Mujumdar, S. R., Lewis, C. J., and Waggoner, A. S. (1993) Cyanine dye labeling reagents: sulfoindocyanine succinimidyl esters Bioconjugate Chem. 4, 105-111
20. Kanaya, S., Koyanagi, T., and Kanaya, E. (1998) An esterase from Escherichia coli with a sequence similarity to hormone-sensitive lipase Biochem. J. 332, 75-80
21. Pacaud, M. (1982) Identification and localization of two membrane-bound esterases from Escherichia coli J. Bacteriol. 149, 6-14
22. Jung, M. E. and Kim, W. J. (2006) Practical syntheses of dyes for difference gel electrophoresis Bioorg. Med. Chem. 14, 92-97
23. Narayanan, N. and Patonay, G. (1995) A new method for the synthesis of heptamethine cyanine eyes-synthesis of new near-infrared fluorescent labels J. Org. Chem. 60, 2391-2395
24. Olah, G. A., Hashimoto, I., and Lin, H. C. (1977) Electrophilic mercuration and thallation of benzene and substituted benzenes in trifluoroacetic acid solution Proc. Natl. Acad. Sci. U.S.A. 74, 4121-4125
25. Fu, N., Xiong, Y., and Squier, T. C. (2012) Synthesis of a targeted biarsenical Cy3-Cy5 affinity probe for super-resolution fluorescence imaging J. Am. Chem. Soc. 134, 18530-18533
26. West, W. and Pearce, S. (1965) The dimeric state of cyanine dyes J. Phys. Chem. 69, 1894-1903
27. Mujumdar, R. B., Ernst, L. A., Mujumdar, S. R., Lewis, C. J., and Waggoner, A. S. (1993) Cyanine dye labeling reagents-sulfoindocyanine succinimidyl esters Bioconjugate Chem. 4, 105-111
28. Cabrera, J. E. and Jin, D. J. (2003) The distribution of RNA polymerase in Escherichia coli is dynamic and sensitive to environmental cues Mol. Microbiol. 50, 1493-1505
29. Cabrera, J. E. and Jin, D. J. (2006) Active transcription of rRNA operons is a driving force for the distribution of RNA polymerase in bacteria: effect of extrachromosomal copies of rrnB on the in vivo localization of RNA polymerase J. Bacteriol. 188, 4007-4014
30. Wang, T., Yan, P., Squier, T. C., and Mayer, M. U. (2007) Prospecting the proteome: identification of naturally occurring binding motifs for biarsenical probes ChemBioChem 8, 1937-1940
31. Johansen, C., Verheul, A., Gram, L., Gill, T., and Abee, T. (1997) Protamine-induced permeabilization of cell envelopes of gram-positive and gram-negative bacteria Appl. Environ. Microbiol. 63, 1155-1159
32. Bar-Even, A., Paulsson, J., Maheshri, N., Carmi, M., O'Shea, E., Pilpel, Y., and Barkai, N. (2006) Noise in protein expression scales with natural protein abundance Nat. Genet. 38, 636-643
33. Schmid, F. X., Mayr, L. M., Mucke, M., and Schonbrunner, E. R. (1993) Prolyl isomerases: role in protein folding Adv. Protein Chem. 44, 25-66
34. Fernandez-Suarez, M. and Ting, A. Y. (2008) Fluorescent probes for super-resolution imaging in living cells Nat. Rev. Mol. Cell Biol. 9, 929-943
35. Schepartz, A. and Gonzalez, R. L., Jr. (2011) Molecular imaging: sine labore nihil Curr. Opin. Chem. Biol. 15, 749-751
36. Genin, E., Carion, O., Mahler, B., Dubertret, B., Arhel, N., Charneau, P., Doris, E., and Mioskowski, C. (2008) CrAsH-quantum dot nanohybrids for smart targeting of proteins J. Am. Chem. Soc. 130, 8596-8597
37. Conley, N. R., Biteen, J. S., and Moerner, W. E. (2008) Cy3-Cy5 covalent heterodimers for single-molecule photoswitching J. Phys. Chem. B 112, 11878-11880
38. Bhunia, A. K. and Miller, S. C. (2007) Labeling tetracysteine-tagged proteins with a SplAsH of color: a modular approach to bis-arsenical fluorophores ChemBioChem 8, 1642-1645
39. Lukinavicius, G. and Johnsson, K. (2011) Switchable fluorophores for protein labeling in living cells Curr. Opin. Chem. Biol. 15, 768-774
40. Scheck, R. A. and Schepartz, A. (2011) Surveying protein structure and function using bis-arsenical small molecules Acc. Chem. Res. 44, 654-665
41. Chen, B., Mayer, M. U., Markillie, L. M., Stenoien, D. L., and Squier, T. C. (2005) Dynamic motion of helix A in the amino-terminal domain of calmodulin is stabilized upon calcium activation Biochemistry 44, 905-914
42. Chen, B., Mayer, M. U., and Squier, T. C. (2005) Structural uncoupling between opposing domains of oxidized calmodulin underlies the enhanced binding affinity and inhibition of the plasma membrane Ca-ATPase Biochemistry 44, 4737-4747
43. Chen, B., Mahaney, J. E., Mayer, M. U., Bigelow, D. J., and Squier, T. C. (2008) Concerted but noncooperative activation of nucleotide and actuator domains of the Ca-ATPase upon calcium binding Biochemistry 47, 12448-12456
44. Roberti, M. J., Jovin, T. M., and Jares-Erijman, E. (2011) Confocal fluorescence anisotropy and FRAP imaging of alpha-synuclein amyloid aggregates in living cells PLoS One 6, e23338
45. Halo, T. L., Appelbaum, J., Hobert, E. M., Balkin, D. M., and Schepartz, A. (2009) Selective recognition of protein tetraserine motifs with a cell-permeable, pro-fluorescent bis-boronic acid J. Am. Chem. Soc. 131, 438-439
46. Luedtke, N. W., Dexter, R. J., Fried, D. B., and Schepartz, A. (2007) Surveying polypeptide and protein domain conformation and association with FlAsH and ReAsH Nat. Chem. Biol. 3, 779-784
47. Maurel, D., Banala, S., Laroche, T., and Johnsson, K. (2010) Photoactivatable and photoconvertible fluorescent probes for protein labeling ACS Chem. Biol. 5, 507-516
48. Gautier, A., Juillerat, A., Heinis, C., Correa, I. R., Jr., Kindermann, M., Beaufils, F., and Johnsson, K. (2008) An engineered protein tag for multiprotein labeling in living cells Chem. Biol. 15, 128-136
49. Keppler, A., Gendreizig, S., Gronemeyer, T., Pick, H., Vogel, H., and Johnsson, K. (2003) A general method for the covalent labeling of fusion proteins with small molecules in vivo Nat. Biotechnol. 21, 86-89
50. Xiong, Y., Chen, B., Shi, L., Fredrickson, J. K., Bigelow, D. J., and Squier, T. C. (2011) Targeted protein degradation of outer membrane decaheme cytochrome MtrC metal reductase in Shewanella oneidensis MR-1 measured using biarsenical probe CrAsH-EDT(2) Biochemistry 50, 9738-9751