Recognition- and Reactivity-Based Fluorescent Probes for Studying Transition Metal Signaling in Living Systems

Accounts of Chemical Research

Volumn 48, Issue 8, 2015, Pages 2434-2442

  Aron, Allegra T ^a   Ramos Torres, Karla M ^a   Cotruvo, Joseph A ^a   Chang, Christopher J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; FLUORESCENT DYE; TRANSITION ELEMENT;

CHEMISTRY; CHLAMYDOMONAS REINHARDTII; FLUORESCENCE MICROSCOPY; HEK293 CELL LINE; HUMAN; METABOLISM; SIGNAL TRANSDUCTION; SYNAPSE; TUMOR CELL LINE;

CELL LINE, TUMOR; CHLAMYDOMONAS REINHARDTII; FLUORESCENT DYES; HEK293 CELLS; HUMANS; MICROSCOPY, FLUORESCENCE; NEUROTRANSMITTER AGENTS; SIGNAL TRANSDUCTION; SYNAPSES; TRANSITION ELEMENTS;

EID: 84939523702     PISSN: 00014842     EISSN: 15204898     Source Type: Journal    
DOI: 10.1021/acs.accounts.5b00221     Document Type: Article

References (66)

1. Lippard, S. J.; Berg, J. M. Principles of Bioinorganic Chemistry; University Science Books: Mill Valley, CA, 1994.
2. Winterbourn, C. C. Toxicity of iron and hydrogen peroxide: the Fenton reaction Toxicol. Lett. 1995, 82-83, 969-974 10.1016/0378-4274(95)03532-X
3. Maryon, E. B.; Molloy, S. A.; Kaplan, J. H. Cellular glutathione plays a key role in copper uptake mediated by human copper transporter 1 Am. J. Physiol. Cell. Physiol. 2013, 304, C768-C779 10.1152/ajpcell.00417.2012
4. Brissot, P.; Ropert, M.; Le Lan, C.; Loréal, O. Non-transferrin bound iron: A key role in iron overload and iron toxicity Biochim. Biophys. Acta, Gen. Subj. 2012, 1820, 403-410 10.1016/j.bbagen.2011.07.014
5. Banci, L.; Bertini, I.; Ciofi-Baffoni, S.; Kozyreva, T.; Zovo, K.; Palumaa, P. Affinity gradients drive copper to cellular destinations Nature 2010, 465, 645-8 10.1038/nature09018
6. Kemlo, J. A.; Shepherd, T. M. Quenching of Excited Singlet States by Metal Ions Chem. Phys. Lett. 1977, 47, 158-162 10.1016/0009-2614(77)85329-3
7. Varnes, A. W.; Dodson, R. B.; Wehry, E. L. Interactions of transition-metal ions with photoexcited states of flavins. Fluorescence quenching studies J. Am. Chem. Soc. 1972, 94, 946-950 10.1021/ja00758a037
8. Tsien, R. Y. Monitoring Cell Calcium. In Calcium as a Cellular Regulator; Carafoli, E.; Klee, C., Eds.; Oxford University Press: New York, 1999; pp 28-54.
9. Que, E. L.; Domaille, D. W.; Chang, C. J. Metals in neurobiology: probing their chemistry and biology with molecular imaging Chem. Rev. 2008, 108, 1517-49 10.1021/cr078203u
10. Carter, K. P.; Young, A. M.; Palmer, A. E. Fluorescent sensors for measuring metal ions in living systems Chem. Rev. 2014, 114, 4564-4601 10.1021/cr400546e
11. Cotruvo, J. A., Jr.; Aron, A. T.; Ramos-Torres, K. M.; Chang, C. J. Synthetic fluorescent probes for studying copper in biological systems Chem. Soc. Rev. 2015, 44, 4400-4414 10.1039/C4CS00346B
12. Domaille, D. W.; Que, E. L.; Chang, C. J. Synthetic fluorescent sensors for studying the cell biology of metals Nat. Chem. Biol. 2008, 4, 168-175 10.1038/nchembio.69
13. Lippert, A. R.; Van de Bittner, G. C.; Chang, C. J. Boronate Oxidation as a Bioorthogonal Reaction Approach for Studying the Chemistry of Hydrogen Peroxide in Living Systems Acc. Chem. Res. 2011, 44, 793-804 10.1021/ar200126t
14. Michel, B. W.; Lippert, A. R.; Chang, C. J. A Reaction-Based Fluorescent Probe for Selective Imaging of Carbon Monoxide in Living Cells Using a Palladium-Mediated Carbonylation J. Am. Chem. Soc. 2012, 134, 15668-15671 10.1021/ja307017b
15. Lin, V. S.; Chen, W.; Xian, M.; Chang, C. J. Chemical probes for molecular imaging and detection of hydrogen sulfide and reactive sulfur species in biological systems Chem. Soc. Rev. 2015, 10.1039/C4CS00298A
16. Chan, J.; Dodani, S. C.; Chang, C. J. Reaction-based small-molecule fluorescent probes for chemoselective bioimaging Nat. Chem. 2012, 4, 973-984 10.1038/nchem.1500
17. Robinson, N. J.; Winge, D. R. Copper metallochaperones Annu. Rev. Biochem. 2010, 79, 537-62 10.1146/annurev-biochem-030409-143539
18. Ferguson-Miller, S.; Babcock, G. T. Heme/copper terminal oxidases Chem. Rev. 1996, 96, 2889-2908 10.1021/cr950051s
19. Kohen, A.; Klinman, J. P. Enzyme Catalysis: Beyond Classical Paradigms Acc. Chem. Res. 1998, 31, 397-404 10.1021/ar9701225
20. Setty, S. R.; Tenza, D.; Sviderskaya, E. V.; Bennett, D. C.; Raposo, G.; Marks, M. S. Cell-specific ATP7A transport sustains copper-dependent tyrosinase activity in melanosomes Nature 2008, 454, 1142-1146 10.1038/nature07163
21. McCord, J. M.; Fridovich, I. Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein) J. Biol. Chem. 1969, 244, 6049-6055
22. Herranz, N.; Dave, N.; Millanes-Romero, A.; Morey, L.; Diaz, V. M.; Lorenz-Fonfria, V.; Gutierrez-Gallego, R.; Jeronimo, C.; Di Croce, L.; de Herreros, A. G.; Peiro, S. Lysyl oxidase-like 2 deaminates lysine 4 in histone H3 Mol. Cell 2012, 46, 369-376 10.1016/j.molcel.2012.03.002
23. Brady, D. C.; Crowe, M. S.; Turski, M. L.; Hobbs, G. A.; Yao, X.; Chaikuad, A.; Knapp, S.; Xiao, K.; Campbell, S. L.; Thiele, D. J.; Counter, C. M. Copper is required for oncogenic BRAF signalling and tumorigenesis Nature 2014, 509, 492-496 10.1038/nature13180
24. Turski, M. L.; Brady, D. C.; Kim, H. J.; Kim, B. E.; Nose, Y.; Counter, C. M.; Winge, D. R.; Thiele, D. J. A novel role for copper in Ras/mitogen-activated protein kinase signaling Mol. Cell. Biol. 2012, 32, 1284-1295 10.1128/MCB.05722-11
25. Burkhead, J. L.; Lutsenko, S. The role of copper as a modifier of lipid metabolism. In Lipid Metabolism; Baez, R. V., Ed.; InTech, 2013; DOI: 10.5772/51819.
26. Bernardo, M. M.; Heeg, M. J.; Schroeder, R. R.; Ochrymowycz, L. A.; Rorabacher, D. B. Comparison of the influence of saturated nitrogen and sulfur donor atoms on the properties of copper(II/I)-macrocyclic polyamino polythiaether ligand complexes: redox potentials and protonation and stability constants of CuIL species and new structural data Inorg. Chem. 1992, 31, 191-198 10.1021/ic00028a013
27. Davis, A. V.; O'Halloran, T. V. A place for thioether chemistry in cellular copper ion recognition and trafficking Nat. Chem. Biol. 2008, 4, 148-151 10.1038/nchembio0308-148
28. de Silva, A. P.; Gunaratne, H. Q. N.; Gunnlaugsson, T.; Huxley, A. J. M.; McCoy, C. P.; Rademacher, J. T.; Rice, T. E. Signaling Recognition Events with Fluorescent Sensors and Switches Chem. Rev. 1997, 97, 1515-1566 10.1021/cr960386p
29. Zeng, L.; Miller, E. W.; Pralle, A.; Isacoff, E. Y.; Chang, C. J. A selective turn-on fluorescent sensor for imaging copper in living cells J. Am. Chem. Soc. 2006, 128, 10-11 10.1021/ja055064u
30. Miller, E. W.; Zeng, L.; Domaille, D. W.; Chang, C. J. Preparation and use of Coppersensor-1, a synthetic fluorophore for live-cell copper imaging Nat. Protoc. 2006, 1, 824-827 10.1038/nprot.2006.140
31. Kowada, T.; Maedab, H.; Kikuchi, K. BODIPY-based probes for the fluorescence imaging of biomolecules in living cells Chem. Soc. Rev. 2015, 10.1039/C5CS00030K
32. Yang, L.; McRae, R.; Henary, M. M.; Patel, R.; Lai, B.; Vogt, S.; Fahrni, C. J. Imaging of the intracellular topography of copper with a fluorescent sensor and by synchrotron x-ray fluorescence microscopy Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 11179-84 10.1073/pnas.0406547102
33. Price, K. A.; Hickey, J. L.; Xiao, Z.; Wedd, A. G.; James, S. A.; Liddell, J. R.; Crouch, P. J.; White, A. R.; Donnelly, P. S. The challenges of using a copper fluorescent sensor (CS1) to track intracellular distributions of copper in neuronal and glial cells Chem. Sci. 2012, 3, 2748-2759 10.1039/c2sc20397a
34. Santo, C. E.; Lam, E. W.; Elowsky, C. G.; Quaranta, D.; Domaille, D. W.; Chang, C. J.; Grass, G. Bacterial killing by dry metallic copper surfaces Appl. Environ. Microbiol. 2011, 77, 794-802 10.1128/AEM.01599-10
35. Bernal, M.; Casero, D.; Singh, V.; Wilson, G. T.; Grande, A.; Yang, H.; Connolly, E. L.; Huijser, P.; Pellegrini, M.; Merchant, S. S.; Krämer, U. Plant Cell 2012, 24, 738-761 10.1105/tpc.111.090431
36. Beaudoin, J.; Ioannoni, R.; López-Maury, L.; Bähler, J.; Ait-Mohand, S.; Guérin, B.; Dodani, S. C.; Chang, C. J.; Labbé, S. Mfc1 is a novel forespore membrane copper transporter in meiotic and sporulating cells J. Biol. Chem. 2011, 286, 34356-34372 10.1074/jbc.M111.280396
37. Cusick, K. D.; Minkin, S. C.; Dodani, S. C.; Chang, C. J.; Wilhelm, S. W.; Sayler, G. S. Inhibition of copper uptake in yeast reveals the copper transporter Ctr1p as a potential molecular target of saxitoxin Environ. Sci. Technol. 2012, 46, 2959-2966 10.1021/es204027m
38. Quaranta, D.; Krans, T.; Santo, C. E.; Elowsky, C. G.; Domaille, D. W.; Chang, C. J.; Grass, G. Mechanisms of contact-mediated killing of yeast cells on dry metallic copper surfaces Appl. Environ. Microbiol. 2011, 77, 416-426 10.1128/AEM.01704-10
39. Dodani, S. C.; Domaille, D. W.; Nam, C. I.; Miller, E. W.; Finney, L. A.; Vogt, S.; Chang, C. J. Calcium-dependent copper redistributions in neuronal cells revealed by a fluorescent copper sensor and X-ray fluorescence microscopy Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 5980-5 10.1073/pnas.1009932108
40. Corazza, A.; Harvey, I.; Sadler, P. J. 1H, 13C-NMR and X-ray absorption studies of copper(I) glutathione complexes Eur. J. Biochem. 1996, 236, 697-705 10.1111/j.1432-1033.1996.0697d.x
41. de Jonge, M. D.; Vogt, S. Hard X-ray fluorescence tomography - an emerging tool for structural visualization Curr. Opin. Struct. Biol. 2010, 20, 606-14 10.1016/j.sbi.2010.09.002
42. Domaille, D. W.; Zeng, L.; Chang, C. J. Visualizing ascorbate-triggered release of labile copper within living cells using a ratiometric fluorescent sensor J. Am. Chem. Soc. 2010, 132, 1194-1195 10.1021/ja907778b
43. Dodani, S. C.; Leary, S. C.; Cobine, P. A.; Winge, D. R.; Chang, C. J. A targetable fluorescent sensor reveals that copper-deficient SCO1 and SCO2 patient cells prioritize mitochondrial copper homeostasis J. Am. Chem. Soc. 2011, 133, 8606-16 10.1021/ja2004158
44. Murphy, M. P.; Smith, R. A. Annu. Rev. Pharmacol. Toxicol. 2007, 47, 629-656 10.1146/annurev.pharmtox.47.120505.105110
45. Hong-Hermesdorf, A.; Miethke, M.; Gallaher, S. D.; Kropat, J.; Dodani, S. C.; Chan, J.; Barupala, D.; Domaille, D. W.; Shirasaki, D. I.; Loo, J. A.; Weber, P. K.; Pett-Ridge, J.; Stemmler, T. L.; Chang, C. J.; Merchant, S. S. Sub-cellular metal imaging identifies dynamic sites of Cu accumulation in Chlamydomonas Nat. Chem. Biol. 2014, 10, 1034-1042 10.1038/nchembio.1662
46. Dodani, S. C.; Firl, A.; Chan, J.; Nam, C. I.; Aron, A. T.; Onak, C. S.; Ramos-Torres, K. M.; Paek, J.; Webster, C. M.; Feller, M. B.; Chang, C. J. Copper is an endogenous modulator of neural circuit spontaneous activity Proc. Natl. Acad. Sci. U. S. A. 2014, 111, 16280-16285 10.1073/pnas.1409796111
47. Whitaker, J. E.; Haugland, R. P.; Ryan, D.; Hewitt, P. C.; Haugland, R. P.; Prendergast, F. G. Fluorescent rhodol derivatives: versatile, photostable labels and tracers Anal. Biochem. 1992, 207, 267-79 10.1016/0003-2697(92)90011-U
48. 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, 4888-94 10.1021/ja043919h
49. Hirayama, T.; Van de Bittner, G. C.; Gray, L. W.; Lutsenko, S.; Chang, C. J. Near-infrared fluorescent sensor for in vivo copper imaging in a murine Wilson disease model Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 2228-33 10.1073/pnas.1113729109
50. Tsien, R. Y. A non-disruptive technique for loading calcium buffers and indicators into cells Nature 1981, 290, 527-528 10.1038/290527a0
51. Dodani, S. C.; He, Q.; Chang, C. J. A Turn-On Fluorescent Sensor for Detecting Nickel in Living Cells J. Am. Chem. Soc. 2009, 131, 18020-18021 10.1021/ja906500m
52. Yoon, S.; Albers, A. E.; Wong, A. P.; Chang, C. J. Screening Mercury Levels in Fish with a Selective Fluorescent Chemosensor J. Am. Chem. Soc. 2005, 127, 16030-16031 10.1021/ja0557987
53. Yoon, S.; Miller, E. W.; He, Q.; Do, P. H.; Chang, C. J. A Bright and Specific Fluorescent Sensor for Mercury in Water, Cells, and Tissue Angew. Chem., Int. Ed. 2007, 46, 6658-6661 10.1002/anie.200701785
54. Miller, E. W.; He, Q.; Chang, C. J. Preparation and Use of Leadfluor-1, a Synthetic Fluorophore for Live-Cell Lead Imaging Nat. Protoc. 2008, 3, 777-783 10.1038/nprot.2008.43
55. He, Q.; Miller, E. W.; Wong, A. P.; Chang, C. J. A Selective Fluorescent Sensor for Detecting Lead in Living Cells J. Am. Chem. Soc. 2006, 128, 9316-9317 10.1021/ja063029x
56. Breuer, W.; Epsztejn, S.; Millgram, P.; Cabantchik, I. Z. Transport of iron and other transition metals into cells as revealed by a fluorescent probe Am. J. Physiol. 1995, 268, C1354-C1361
57. Irving, H.; Williams, R. J. P. The Stability of Transition-Metal Complexes J. Chem. Soc. 1953, 3192-3210 10.1039/jr9530003192
58. Vad, M. S.; Nielsen, A.; Lennartson, A.; Bond, A. D.; McGrady, J. E.; McKenzie, C. J. Switching on oxygen activation by cobalt complexes of pentadentate ligands Dalton Trans. 2011, 40, 10698-10707 10.1039/c1dt10594a
59. Taki, M.; Iyoshi, S.; Ojida, A.; Hamachi, I.; Yamamoto, Y. Development of highly sensitive fluorescent probes for detection of intracellular copper(I) in living systems J. Am. Chem. Soc. 2010, 132, 5938-5939 10.1021/ja100714p
60. Au-Yeung, H. Y.; New, E. J.; Chang, C. J. A selective reaction-based fluorescent probe for detecting cobalt in living cells Chem. Commun. 2012, 48, 5268-5270 10.1039/c2cc31681a
61. Que, L., Jr.; Ho, R. Y. N. Dioxygen Activation by Enzymes with Mononuclear Non-Heme Iron Active Sites Chem. Rev. 1996, 96, 2607-2624 10.1021/cr960039f
62. Au-Yeung, H. Y.; Chan, J.; Chantarojsiri, T.; Chang, C. J. Molecular imaging of labile iron(II) pools in living cells with a turn-on fluorescent probe J. Am. Chem. Soc. 2013, 135, 15165-73 10.1021/ja4072964
63. Huang, C. P.; Fofana, M.; Chan, J.; Chang, C. J.; Howell, S. B. Copper transporter 2 regulates intracellular copper and sensitivity to cisplatin Metallomics 2014, 6, 654-661 10.1039/c3mt00331k
64. Polishchuk, E. V.; Concilli, M.; Iacobacci, S.; Chesi, G.; Pastore, N.; Piccolo, P.; Paladino, S.; Baldantoni, D.; van, I. S. C.; Chan, J.; Chang, C. J.; Amoresano, A.; Pane, F.; Pucci, P.; Tarallo, A.; Parenti, G.; Brunetti-Pierri, N.; Settembre, C.; Ballabio, A.; Polishchuk, R. S. Wilson disease protein ATP7B utilizes lysosomal exocytosis to maintain copper homeostasis Dev. Cell 2014, 29, 686-700 10.1016/j.devcel.2014.04.033
65. Ohrvik, H.; Nose, Y.; Wood, L. K.; Kim, B. E.; Gleber, S. C.; Ralle, M.; Thiele, D. J. Ctr2 regulates biogenesis of a cleaved form of mammalian Ctr1 metal transporter lacking the copper- and cisplatin-binding ecto-domain Proc. Natl. Acad. Sci. U. S. A. 2013, 110, E4279-E4288 10.1073/pnas.1311749110
66. Ding, X.; Xie, H.; Kang, Y. J. The significance of copper chelators in clinical and experimental application J. Nutr. Biochem. 2011, 22, 301-310 10.1016/j.jnutbio.2010.06.010