Near-infrared fluorescent sensor for in vivo copper imaging in a murine Wilson disease model

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 7, 2012, Pages 2228-2233

  Hirayama, Tasuku ^a   Van De Bittner, Genevieve C ^a   Gray, Lawrence W ^b   Lutsenko, Svetlana ^b   Chang, Christopher J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Diagnostic; Metal homeostasis; Molecular imaging; Near infrared fluorophore

Indexed keywords

COPPER; CYANINE DYE; SULFUR; WILSON DISEASE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; COPPER DEFICIENCY; FLUORESCENCE; IN VIVO STUDY; MASS SPECTROMETRY; MOLECULAR IMAGING; MOUSE; NEAR INFRARED FLUORESCENT SENSOR; NONHUMAN; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTUM YIELD; SENSOR; SYNTHESIS; WILSON DISEASE;

ANIMALS; COPPER; DISEASE MODELS, ANIMAL; FLUORESCENT DYES; HEPATOLENTICULAR DEGENERATION; MICE;

ANIMALIA; MURINAE; MUS;

EID: 84863178523     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1113729109     Document Type: Article

References (61)

1. Lippard S, Berg JM (1994) Principles of Bioinorganic Chemistry (University Science Books, Mill Valley, CA).
2. Gray H, Stiefel EI, Valentine JS, Bertini I (2007) Biological Inorganic Chemistry: Structure and Reactivity (University Science Books, Mill Valley, CA).
3. Prohaska J, Gybina AA (2004) Intracellular copper transport in mammals. J Nutr 134:1003-1006. (Pubitemid 38619931)
4. Que E, Domaille DW, Chang CJ (2008) Metals in neurobiology: Probing their chemistry and biology with molecular imaging. Chem Rev 108:1517-1549. (Pubitemid 351796396)
5. Thiele DJ, Gitlin JD (2008) Assembling the pieces. Nat Chem Biol 4:145-147. (Pubitemid 351264132)
6. Davis AV, O'Halloran TV (2008) A place for thioether chemistry in cellular copper ion recognition and trafficking. Nat Chem Biol 4:148-151. (Pubitemid 351265328)
7. Robinson NJ, Winge DR (2010) Assembling the pieces. Annu Rev Biochem 79:537-562.
8. Finkel T, Serrano M, Blasco MA (2007) The common biology of cancer and ageing. Nature 448:767-774. (Pubitemid 47266334)
9. Looi YH, et al. (2008) Involvement of Nox2 NADPH oxidase in adverse cardiac remodeling after myocardial infarction. Hypertension 51:319-325. (Pubitemid 351159945)
10. Kim BE, et al. (2010) Cardiac copper deficiency activates a systemic signaling mechanism that communicates with the copper acquisition and storage organs. Cell Metab 11:353-363.
11. Kang YJ (2011) Copper and homocysteine in cardiovascular diseases. Pharmacol Ther 129:321-331.
12. Barnham KJ, Masters CL, Bush AI (2004) Neurodegenerative diseases and oxidative stress. Nat Rev Drug Discov 3:205-214.
13. Gaggelli E, Kozlowski H, Valensin D, Valensin G (2006) Copper homeostasis and neurodegenerative disorders (Alzheimer's, prion, and Parkinson's diseases and amyotrophic lateral sclerosis). Chem Rev 106:1995-2044.
14. Lutsenko S, Gupta A, Burkhead JL, Zuzel V (2008) Cellular multitasking: The dual role of human Cu-ATPases in cofactor delivery and intracellular copper balance. Arch Biochem Biophys 476:22-32.
15. Beckman J, Estevez AG, Crow JP, Barbeito L (2001) Superoxide dismutase and the death of motoneurons in ALS. Trends Neurosci 24:S15-S20.
16. Valentine J, Hart PJ (2003) Bioinorganic chemistry special feature: Misfolded CuZnSOD and amyotrophic lateral sclerosis. Proc Natl Acad Sci USA 100:3617-3622. (Pubitemid 36418082)
17. Brown D, Kozlowski H (2004) Biological inorganic and bioinorganic chemistry of neurodegeneration based on prion and Alzheimer diseases. Dalton Trans 1907-1917.
18. Millhauser G (2004) Copper binding in the prion protein. Acc Chem Res 37:79-85.
19. Camakaris J, Voskoboinik I, Mercer JF (1999) Molecular mechanisms of copper homeostasis. Biochem Biophys Res Commun 261:225-232. (Pubitemid 29392460)
20. Bertini I, Rosato A (2008) Menkes disease. Cell Mol Life Sci 65:89-91.
21. Kaler SG (2011) ATP7A-related copper transport diseases - emerging concepts and future trends. Nat Rev Neurol 7:15-29.
22. Cox D, Moore SD (2002) Copper transporting P-type ATPases and human disease. J Bioenerg Biomembr 34:333-338. (Pubitemid 36055727)
23. Leary S, et al. (2007) The human cytochrome c oxidase assembly factors SCO1 and SCO2 have regulatory roles in the maintenance of cellular copper homeostasis. Cell Metab 5:9-20. (Pubitemid 44933111)
24. Domaille D, Que EL, Chang CJ (2008) Synthetic fluorescent sensors for studying the cell biology of metals. Nat Chem Biol 4:168-175. (Pubitemid 351265326)
25. McRae R, Bagchi P, Sumalekshmy S, Fahrni CJ (2009) In situ imaging of metals in cells and tissues. Chem Rev 109:4780-4827.
26. Haas K, Franz KJ (2009) Application of metal coordination chemistry to explore and manipulate cell biology. Chem Rev 109:4921-4960.
27. Yang L, et al. (2005) Imaging of the intracellular topography of copper with a fluorescent sensor and by synchrotron X-ray fluorescence microscopy. Proc Natl Acad Sci USA 102:11179-11184. (Pubitemid 41153794)
28. Zeng L, et al. (2006) A selective turn-on fluorescent sensor for imaging copper in living cells. J Am Chem Soc 128:10-11. (Pubitemid 43100825)
29. Miller E, Zeng L, Domaille DW, Chang CJ (2006) Preparation and use of Coppersensor- 1, a synthetic fluorophore for live-cell copper imaging. Nat Protoc 1:824-827.
30. Taki M, et al. (2010) Development of highly sensitive fluorescent probes for detection of intracellular copper(I) in living systems. J Am Chem Soc 132:5938-5939.
31. Domaille D, Zeng L, Chang CJ (2010) Visualizing ascorbate-triggered release of labile copper within living cells using a ratiometric fluorescent sensor. J Am Chem Soc 132:1194-1195.
32. Dodani S, et al. (2011) Calcium-dependent copper redistributions in neuronal cells revealed by a fluorescent copper sensor and X-ray fluorescence microscopy. Proc Natl Acad Sci USA 108:5980-5985.
33. Dodani S, et al. (2011) A targetable fluorescent sensor reveals that copper-deficient SCO1 and SCO2 patient cells prioritize mitochondrial copper homeostasis. J Am Chem Soc 133:8606-8616.
34. Lim CS, et al. (2011) A copper(I)-ion selective two-photon fluorescent probe for in vivo imaging. Chem Commun 47:7146-7148.
35. You Y, et al. (2011) Phosphorescent sensor for robust quantification of copper(II) ion. J Am Chem Soc 133:11488-11491.
36. Wegner S, et al. (2010) Dynamic copper(I) imaging in mammalian cells with a genetically encoded fluorescent copper(I) sensor. J Am Chem Soc 132:2567-2569.
37. Wegner S, Sun F, Hernandez N, He C (2011) The tightly regulated copper window in yeast. Chem Commun 47:2571-2573.
38. 2+ ions in aqueous solution with high sensitivity and selectivity. J Am Chem Soc 129:9838-9839.
39. 2+ detection with a ligation DNAzyme and nanoparticles. Chem Commun 4872-4874.
40. Quaranta D, et al. (2011) Mechanisms of contact-mediated killing of yeast cells on dry metallic copper surfaces. Appl Environ Microbiol 77:416-426.
41. Santo C, et al. (2011) Bacterial killing by dry metallic copper surfaces. Appl Environ Microbiol 77:794-802.
42. Weissleder R, Ntziachristos V (2003) Shedding light onto live molecular targets. Nat Med 9:123-128. (Pubitemid 36098273)
43. Frangioni J (2003) In vivo near-infrared fluorescence imaging. Curr Opin Chem Biol 7:626-634.
44. Sasaki E, et al. (2005) Highly sensitive near-infrared fluorescent probes for nitric oxide and their application to isolated organs. J Am Chem Soc 127:3684-3685. (Pubitemid 40411394)
45. Peng X, et al. (2005) Heptamethine cyanine dyes with a large stokes shift and strong fluorescence: A paradigm for excited-state intramolecular charge transfer. J Am Chem Soc 127:4170-4171. (Pubitemid 40463032)
46. Zhang Z, Achilefu S (2005) Design, synthesis and evaluation of near-infrared fluorescent pH indicators in a physiologically relevant range. Chem Commun 5887-5889. (Pubitemid 43021906)
47. Hilderbrand S, Weissleder R (2007) Optimized pH-responsive cyanine fluorochromes for detection of acidic environments. Chem Commun 2747-2749. (Pubitemid 47000802)
48. Hilderbrand S, Kelly KA, Niedre M, Weissleder R (2008) Near infrared fluorescence-based bacteriophage particles for ratiometric pH imaging. Bioconjug Chem 19:1635-1639.
49. Myochin T, et al. (2011) Rational design of ratiometric near-infrared fluorescent pH probes with various pKa values, based on aminocyanine. J Am Chem Soc 133:3401-3409.
50. Chaudhry A, et al. (2010) Kinetically controlled photoinduced electron transfer switching in Cu(I)-responsive fluorescent probes. J Am Chem Soc 132:737-747.
51. Chaudhry A, Mandal S, Hardcastle KI, Fahrni CJ (2011) High-contrast Cu(I)-selective fluorescent probes based on synergistic electronic and conformational switching. Chem Sci 2:1016-1024.
52. Tsien R (1981) A non-disruptive technique for loading calcium buffers and indicators into cells. Nature 290:527-528.
53. i in perfused hearts. Critical evaluation of the 5F-BAPTA and nuclear magnetic resonance method as applied to the study of ischemia and reperfusion. Circ Res 66:1255-1267.
54. Meyer L, Durley AP, Prohaska JR, Harris ZL (2001) Copper transport and metabolism are normal in aceruloplasminemic mice. J Biol Chem 276:36857-36861.
55. Lee V, Schulman JM, Stiefel EI, Lee CC (2007) Reversible precipitation of bovine serum albumin by metal ions and synthesis, structure and reactivity of new tetrathiometallate chelating agents. J Inorg Biochem 101:1707-1718. (Pubitemid 47576218)
56. Buiakova O, et al. (1999) Null mutation of the murine ATP7B (Wilson disease) gene results in intracellular copper accumulation and late-onset hepatic nodular transformation. Hum Mol Genet 8:1665-1671. (Pubitemid 29423875)
57. -/- (Wilson disease gene) knockout mice. Am J Pathol 168:423-434.
58. -/- mice as a model for studies of Wilson's disease. Biochem Soc Trans 36:1233-1238.
59. Brewer GJ (2009) Zinc and tetrathiomolybdate for the treatment of Wilson's disease and the potential efficacy of anticopper therapy in a wide variety of diseases. Metallomics 1:199-206.
60. Smith SV (2004) Molecular imaging with copper-64. J Inorg Biochem 98:1874-1901.
61. -/- knock-out mouse model of Wilson's disease. Mol Imaging Biol, DOI: 10.1007/s11307-011-0476-4.