Development of potent fluorescent polyamine toxins and application in labeling of ionotropic glutamate receptors in hippocampal neurons

ACS Chemical Biology

Volumn 8, Issue 9, 2013, Pages 2033-2041

  Nørager, Niels G ^a   Jensen, Christel B ^a   Rathje, Mette ^a   Andersen, Jacob ^a   Madsen, Kenneth L ^a   Kristensen, Anders S ^a   Strømgaard, Kristian ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; ARGIOTOXIN 48; ARGIOTOXIN 636; ARGIOTOXIN 75; GLUTAMATE RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; POLYAMINE DERIVATIVE; TOXIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; DRUG RECEPTOR BINDING; DRUG STRUCTURE; DRUG SYNTHESIS; FLUORESCENCE ANALYSIS; HIPPOCAMPUS; IC 50; NONHUMAN; PRIORITY JOURNAL; RAT; TOXIN ANALYSIS;

ANIMALS; FLUORESCENT DYES; HIPPOCAMPUS; INDOLEACETIC ACIDS; LIGANDS; MODELS, MOLECULAR; NEURONS; POLYAMINES; RATS; RECEPTORS, IONOTROPIC GLUTAMATE; STAINING AND LABELING;

EID: 84884646164     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb400272m     Document Type: Article

References (51)

1. Lichtman, J. and Conchello, J.-A. (2005) Fluorescence microscopy Nat. Methods 2, 910-919
2. Qian, X., Xiao, Y., Xu, Y., Guo, X., Qian, J., and Zhu, W. (2010) 'Alive' dyes as fluorescent sensors: Fluorophore, mechanism, receptor, and images in living cells Chem. Commun. 46, 6418-6436
3. Leopoldo, M., Lacivita, E., Berardi, F., and Perrone, R. (2009) Developments in fluorescent probes for receptor research Drug Discov. Today 14, 706-712
4. Hern, J. A., Baig, A. H., Mashanov, G. I., Birdsall, B., Corrie, J. E. T., Lazareno, S., Molloy, J. E., and Birdsall, N. J. M. (2010) Formation and dissociation of M1 muscarinic receptor dimers seen by total internal reflection fluorescence imaging of single molecules Proc. Natl. Acad. Sci. U.S.A. 107, 2693-2698
5. Bach, A., Clausen, B. H., Møller, M., Vestergaard, B., Chi, C. N., Round, A., Sørensen, P. L., Nissen, K. B., Kastrup, J. S., Gajhede, M., Jemth, P., Kristensen, A. S., Lundström, P., Lambertsen, K. L., and Strømgaard, K. (2012) A high-affinity, dimeric inhibitor of PSD-95 bivalently interacts with PDZ1-2 and protects against ischemic brain damage Proc. Natl. Acad. Sci. U.S.A. 109, 3317-3322
6. Roy, R., Hohng, S., and Ha, T. (2008) A practical guide to single-molecule FRET Nat. Methods 5, 507-516
7. Briddon, S. J. and Hill, S. J. (2007) Pharmacology under the microscope: the use of fluorescence correlation spectroscopy to determine the properties of ligand-receptor complexes Trends Pharmacol. Sci. 28, 637-645
8. Wu, B., Piatkevich, K. D., Lionnet, T., Singer, R. H., and Verkhusha, V. V. (2011) Modern fluorescent proteins and imaging technologies to study gene expression, nuclear localization, and dynamics Curr. Opin. Cell Biol. 23, 310-317
9. 3 receptor in plasma membranes of live biological cells Biochemistry 42, 877-884
10. Daigle, T. L., Kwok, M. L., and Mackie, K. (2008) Regulation of CB1 cannabinoid receptor internalization by a promiscuous phosphorylation-dependent mechanism J. Neurochem. 106, 70-82
11. Maurel, D., Comps-Agrar, L., Brock, C., Rives, M.-L., Bourrier, E., Ayoub, M. A., Bazin, H., Tinel, N., Durroux, T., Prezeau, L., Trinquet, E., and Pin, J.-P. (2008) Cell-surface protein-protein interaction analysis with time-resolved FRET and snap-tag technologies: Application to GPCR oligomerization Nat. Methods 5, 561-567
12. Bohme, I. and Beck-Sickinger, A. (2009) Illuminating the life of GPCRs Cell Commun. Signal. 7, 16
13. Traynelis, S., Wollmuth, L., McBain, C., Menniti, F., Vance, K., Ogden, K., Hansen, K., Yuan, H., Myers, S., and Dingledine, R. (2010) Glutamate receptor ion channels: Structure, regulation, and function Pharmacol. Rev. 62, 405-496
14. Pinheiro, P. S. and Mulle, C. (2008) Presynaptic glutamate receptors: Physiological functions and mechanisms of action Nat. Rev. Neurosci. 9, 423-436
15. Ogden, K. and Traynelis, S. (2011) New advances in NMDA receptor pharmacology Trends Pharmacol. Sci. 32, 726-733
16. Stawski, P., Janovjak, H., and Trauner, D. (2010) Pharmacology of ionotropic glutamate receptors: A structural perspective Bioorg. Med. Chem. 18, 7759-7772
17. Sobolevsky, A., Rosconi, M., and Gouaux, E. (2009) X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor Nature 462, 745-756
18. Ramanoudjame, G., Du, M., Mankiewicz, K. A., and Jayaraman, V. (2006) Allosteric mechanism in AMPA receptors: A FRET-based investigation of conformational changes Proc. Natl. Acad. Sci. U.S.A. 103, 10473-10478
19. Rambhadran, A., Gonzalez, J., and Jayaraman, V. (2010) Subunit arrangement in N -methyl-D-aspartate (NMDA) receptors J. Biol. Chem. 285, 15296-15301
20. Henley, J. M., Barker, E. A., and Glebov, O. O. (2011) Routes, destinations and delays: Recent advances in AMPA receptor trafficking Trends Neurosci. 34, 258-268
21. Marchand, P., Becerril-Ortega, J., Mony, L., Bouteiller, C., Paoletti, P., Nicole, O., Barré, L., Buisson, A., and Perrio, C. (2011) Confocal microscopy imaging of NR2B-containing NMDA receptors based on fluorescent Ifenprodil-like conjugates Bioconjugate Chem. 23, 21-26
22. Joubert, J., Dyk, S. v., Green, I. R., and Malan, S. F. (2011) Synthesis and evaluation of fluorescent heterocyclic aminoadamantanes as multifunctional neuroprotective agents Bioorg. Med. Chem. 19, 3935-3944
23. Nishimaru, T., Sano, M., Yamaguchi, Y., and Wakamiya, T. (2009) Syntheses and biological activities of fluorescent-labeled analogs of acylpolyamine toxin NPTX-594 isolated from the venom of Madagascar Joro spider Bioorg. Med. Chem. 17, 57-63
24. Vytla, D., Combs-Bachmann, R. E., Hussey, A. M., Hafez, I., and Chambers, J. J. (2011) Silent, fluorescent labeling of native neuronal receptors Org. Biomol. Chem. 9, 7151-7161
25. Kwak, S. and Weiss, J. (2006) Calcium-permeable AMPA channels in neurodegenerative disease and ischemia Curr. Opin. Neurobiol. 16, 281-287
26. Man, H.-Y. (2011) GluA2-lacking, calcium-permeable AMPA receptors-inducers of plasticity Curr. Opin. Neurobiol. 21, 291-298
27. Green, A., Nakanishi, K., and Usherwood, P. (1996) Polyamine amides are neuroprotective in cerebellar granule cell cultures challenged with excitatory amino acids Brain Res. 717, 135-146
28. + channel voltage sensor measured with luminescence energy transfer Nature 436, 848-851
29. Olsen, C. A., Kristensen, A. S., and Strømgaard, K. (2011) Small molecules from spiders used as chemical probes Angew. Chem., Int. Ed. 50, 11296-11311
30. Nelson, J. K., Frølund, S. U., Tikhonov, D. B., Kristensen, A. S., and Strømgaard, K. (2009) Synthesis and biological activity of argiotoxin 636 and analogues: Selective antagonists for ionotropic glutamate receptors Angew. Chem., Int. Ed. 48, 3087-3091
31. Poulsen, M. H., Lucas, S., Bach, T. B., Barslund, A. F., Wenzler, C., Jensen, C. B., Kristensen, A. S., and Strømgaard, K. (2013) Structure-activity relationship studies of argiotoxins: Selective and potent inhibitors of ionotropic glutamate receptors J. Med. Chem. 56, 1171-1181
32. Briddon, S. J., Kellam, B., and Kill, S. J. (2011) In Methods in Molecular Biology: Receptor Signal Transduction Protocols (Willars, G. B. and Challiss, J., Eds.) 3rd ed., Vol. 746, pp 211-236, Springer Science-Business Media, New York.
33. Baker, J. G., Middleton, R., Adams, L., May, L. T., Briddon, S. J., Kellam, B., and Hill, S. J. (2010) Influence of fluorophore and linker composition on the pharmacology of fluorescent adenosine A1 receptor ligands Br. J. Pharmacol. 159, 772-786
34. Andersen, T. F., Tikhonov, D. B., Bølcho, U., Bolshakov, K., Nelson, J. K., Pluteanu, F., Mellor, I. R., Egebjerg, J., and Strømgaard, K. (2006) Uncompetitive antagonism of AMPA receptors: Mechanistic insights from studies of polyamine toxin derivatives J. Med. Chem. 49, 5414-5423
35. Wysocki, L. M. and Lavis, L. D. (2011) Advances in the chemistry of small molecule fluorescent probes Curr. Opin. Chem. Biol. 15, 752-759
36. Johnson, I. and Spence, M. T. Z. (Eds.) Molecular Probes Handbook, A Guide to Fluorescent Probes and Labeling Technologies (2010) 11 th ed., Molecular Probes, Eugene, OR.
37. Loudet, A. and Burgess, K. (2007) BODIPY dyes and their derivatives: Syntheses and spectroscopic properties Chem. Rev. 107, 4891-4932
38. Bryantseva, N. G., Sokolova, I. V., Tsyrenzhapova, A. B., Selivanov, N. I., Khilya, V. P., and Garazd, Y. L. (2008) Fluorescent characteristics of coumarin photosensitizers J. Appl. Spectrosc. 75, 700-705
39. Sun, W.-C., Gee, K. R., Klaubert, D. H., and Haugland, R. P. (1997) Synthesis of fluorinated fluoresceins J. Org. Chem. 62, 6469-6475
40. Jensen, K. J., Alsina, J., Songster, M. F., Vágner, J., Albericio, F., and Barany, G. (1998) Backbone amide linker (BAL) strategy for solid-phase synthesis of C-terminal-modified and cyclic peptides J. Am. Chem. Soc. 120, 5441-5452
41. Olsen, C. A., Witt, M., Hansen, S. H., Jaroszewski, J. W., and Franzyk, H. (2005) Fukuyama-Mitsunobu alkylation in amine synthesis on solid phase revisited: N-alkylation with secondary alcohols and synthesis of curtatoxins Tetrahedron 61, 6046-6055
42. Tornøe, C. W., Christensen, C., and Meldal, M. (2002) Peptidotriazoles on solid phase: [1,2,3]-triazoles by regiospecific copper(I)-catalyzed 1,3-dipolar cycloadditions of terminal alkynes to azides J. Org. Chem. 67, 3057-3064
43. Bock, V. D., Speijer, D., Hiemstra, H., and van Maarseveen, J. H. (2007) 1,2,3-Triazoles as peptide bond isosteres: Synthesis and biological evaluation of cyclotetrapeptide mimics Org. Biomol. Chem. 5, 971-975
44. 2 complexes as laser dyes: 1 Heteroat. Chem. 1, 389-399
45. Bräse, S., Gil, C., Knepper, K., and Zimmermann, V. (2005) Organic azides: An exploding diversity of a unique class OFC Angew. Chem., Int. Ed. 44, 5188-5240
46. Nicolaou, K. C., Winssinger, N., Vourloumis, D., Ohshima, T., Kim, S., Pfefferkorn, J., Xu, J. Y., and Li, T. (1998) Solid and solution phase synthesis and biological evaluation of combinatorial sarcodictyin libraries J. Am. Chem. Soc. 120, 10814-10826
47. Lee, C. E., Kick, E. K., and Ellman, J. A. (1998) General solid-phase synthesis approach to prepare mechanism-based aspartyl protease inhibitor libraries. Identification of potent cathepsin D inhibitors J. Am. Chem. Soc. 120, 9735-9747
48. Goddard-Borger, E. D. and Stick, R. V. (2007) An efficient, inexpensive, and shelf-stable diazotransfer reagent: Imidazole-1-sulfonyl azide hydrochloride Org. Lett. 9, 3797-3800
49. Burnashev, N., Villarroel, A., and Sakmann, B. (1996) Dimensions and ion selectivity of recombinant AMPA and kainate receptor channels and their dependence on Q/R site residues The J. Physiol. 496, 165-173
50. Villarroel, A., Burnashev, N., and Sakmann, B. (1995) Dimensions of the narrow portion of a recombinant NMDA receptor channel Biophys. J. 68, 866-875
51. Barria, A. and Malinow, R. (2002) Subunit-specific NMDA receptor trafficking to synapses Neuron 35, 345-353