Calcium-dependent copper redistributions in neuronal cells revealed by a fluorescent copper sensor and X-ray fluorescence microscopy

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

Volumn 108, Issue 15, 2011, Pages 5980-5985

  Dodani, Sheel C ^a   Domaille, Dylan W ^a   Nam, Christine I ^a   Miller, Evan W ^a   Finney, Lydia A ^b   Vogt, Stefan ^b   Chang, Christopher J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b ARGONNE NATIONAL LABORATORY   (United States)

Author keywords

Fluorescent sensor; Mobile metals; Molecular imaging; Transition metal signaling

Indexed keywords

CALCIUM; COPPER; FLUORESCENT DYE; IRON; TRANSITION ELEMENT;

BIOSENSOR; CALCIUM TRANSPORT; CELL ACTIVATION; CELLULAR DISTRIBUTION; CONFERENCE PAPER; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; FLUORESCENT COPPER SENSOR; HUMAN; HUMAN CELL; MOLECULAR PROBE; NERVE CELL; PERIKARYON; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SYNCHROTRON; X RAY FLUORESCENCE MICROSCOPY;

EID: 79955003399     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1009932108     Document Type: Article

References (54)

1. Tsien RW, Tsien RY (1990) Calcium channels, stores, and oscillations. Annu Rev Cell Biol 6:715-760.
2. Debanne D (2004) Information processing in the axon. Nat Rev Neurosci 5:304-316. (Pubitemid 38478657)
3. Clapham DE (2007) Calcium signaling. Cell 131:1047-1058. (Pubitemid 350258556)
4. Lippard SJ, Berg JM (1994) Principles of Bioinorganic Chemistry (University Science Books, Mill Valley, CA).
5. Gray HB, Stiefel EI, Valentine JS, Bertini I (2007) Biological Inorganic Chemistry (University Science Books, Mill Valley, CA).
6. Cvetkovic A, et al. (2010) Microbial metalloproteomes are largely uncharacterized. Nature 466:779-782.
7. Berridge MJ, Bootman MD, Lipp P (1998) Calcium-A life and death signal. Nature 395:645-648.
8. Atwood CS, et al. (1999) Metal Ions in Biological Systems: Interrelations Betwen Free Radicals and Metal Ions in Life Processes (CRC, New York).
9. Bush AI (2000) Metals and neuroscience. Curr Opin Chem Biol 4:184-191. (Pubitemid 30189310)
10. Burdette SC, Lippard SJ (2003) Bioinorganic Chemistry Special Feature: Meeting of the minds: Metalloneurochemistry. Proc Natl Acad Sci USA 100:3605-3610.
11. Prohaska JR, Gybina AA (2004) Intracellular copper transport in mammals. J Nutr 134:1003-1006. (Pubitemid 38619931)
12. Que EL, Domaille DW, Chang CJ (2008) Metals in neurobiology: Probing their chemistry and biology with molecular imaging. Chem Rev 108:1517-1549. (Pubitemid 351796396)
13. Camakaris J, Voskoboinik I, Mercer JF (1999) Molecular mechanisms of copper homeostasis. Biochem Biophys Res Commun 261:225-232. (Pubitemid 29392460)
14. Bertini I, Rosato A (2008) Menkes disease. Cell Mol Life Sci 65:89-91.
15. Barnham KJ, Masters CL, Bush AI (2004) Neurodegenerative diseases and oxidative stress. Nat Rev Drug Discov 3:205-214.
16. 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.
17. 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.
18. Beckman JS, Estevez AG, Crow JP, Barbeito L (2001) Superoxide dismutase and the death of motoneurons in ALS. Trends Neurosci 24:S15-S20.
19. Valentine JS, Hart PJ (2003) Bioinorganic Chemistry Special Feature: Misfolded CuZn- SOD and amyotrophic lateral sclerosis. Proc Natl Acad Sci USA 100:3617-3622.
20. Brown DR, Kozlowski H (2004) Biological inorganic and bioinorganic chemistry of neurodegeneration based on prion and Alzheimer diseases. Dalton Trans 1907-1917.
21. Millhauser GL (2004) Copper binding in the prion protein. Acc Chem Res 37:79-85.
22. Hartter DE, Barnea A (1988) Evidence for release of copper in the brain: Depolarization- induced release of newly taken up copper. Synapse 2:412-415.
23. Schlief ML, Craig AM, Gitlin JD (2005) NMDA receptor activation mediates copper homeostasis in hippocampal neurons. J Neurosci 25:239-246. (Pubitemid 40110786)
24. Hopt A, et al. (2003) Methods for studying synaptosomal copper release. J Neurosci Methods 128:159-172. (Pubitemid 37013560)
25. Schlief ML, et al. (2006) Role of the Menkes copper-transporting ATPase in NMDA receptor-mediated neuronal toxicity. Proc Natl Acad Sci USA 103:14919-14924. (Pubitemid 44527829)
26. Domaille DW, Que EL, Chang CJ (2008) Synthetic fluorescent sensors for studying the cell biology of metals. Nat Chem Biol 4:168-175. (Pubitemid 351265326)
27. McRae R, Bagchi P, Sumalekshmy S, Fahrni CJ (2009) In situ imaging of metals in cells and tissues. Chem Rev 109:4780-4827.
28. Haas KL, Franz KJ (2009) Application of metal coordination chemistry to explore and manipulate cell biology. Chem Rev 109:4921-4960.
29. Yang LC (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.
30. 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)
31. Miller EW, 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.
32. Domaille DW, 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.
33. Wegner SV, 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.
34. Wegner SV, Sun F, Hernandez N, He C (2011) The tightly regulated copper window in yeast. Chem Commun 47:2571-2573.
35. Gabe Y (2006) Tunable design strategy for fluorescence probes based on 4-substituted BODIPY chromophore: Improvement of highly sensitive fluorescence probe for nitric oxide. Anal Bioanal Chem 386:621-626. (Pubitemid 44450942)
36. Hamza I, Prohaska J, Gitlin JD (2003) Essential role for Atox1 in the copper-mediated intracellular trafficking of the Menkes ATPase. Proc Natl Acad Sci USA 100:1215-1220. (Pubitemid 36183982)
37. Glesne D, et al. (2006) Regulatory properties and cellular redistribution of zinc during macrophage differentiation of human leukemia cells. J Struct Biol 155:2-11. (Pubitemid 43867315)
38. Finney L, et al. (2007) X-ray fluorescencemicroscopy reveals large-scale relocalization and extracellular translocation of cellular copper during angiogenesis. Proc Natl Acad Sci USA 104:2247-2252. (Pubitemid 46391383)
39. Fahrni CJ (2007) Biological applications of X-ray fluorescence microscopy: Exploring the subcellular topography and speciation of transition metals. Curr Opin Chem Biol 11:121-127. (Pubitemid 46528374)
40. Finney L, et al. (2010) Imaging metals in proteins by combining electrophoresis with rapid X-ray fluorescence mapping. ACS Chem Biol 5:577-587.
41. Twining BS, et al. (2003) Quantifying trace elements in individual aquatic protist cells with a synchrotron X-ray fluorescence microprobe. Anal Chem 75:3806-3816. (Pubitemid 36962115)
42. Tsien RY (1980) A non-disruptive technique for loading calcium buffers and indicators into cells. Nature 290:527-528. (Pubitemid 11159085)
43. Balkowiec A, Katz DM (2002) Cellular mechanisms regulating activity-dependent release of native brain-derived neurotrophic factor from hippocampal neurons. J Neurosci 22:10399-10407. (Pubitemid 35416877)
44. 2+ oscillation in cultured rat frontal cortical neurons. J Neural Transm 104:811-824. (Pubitemid 27507329)
45. Herd SM (1987) Uptake and efflux of copper-64 in Menkes'-disease and normal continuous lymphoid cell lines. Biochem J 247:341-347. (Pubitemid 17153342)
46. O'Halloran TV, Culotta VC (2000) Metallochaperones, an intracellular shuttle service for metal ions. J Biol Chem 275:25057-25060.
47. Rosenzweig AC, O'Halloran TV (2000) Structure and chemistry of the copper chaperone proteins. Curr Opin Chem Biol 4:140-147. (Pubitemid 30189303)
48. Cobine PA, Pierrel F, Winge DR (2006) Copper trafficking to the mitochondrion and assembly of copper metalloenzymes. Biochim Biophys Acta 1763:759-772. (Pubitemid 44189537)
49. Kim B-E, Nevitt T, Thiele DJ (2008) Mechanisms for copper acquisition, distribution and regulation. Nat Chem Biol 4:176-185. (Pubitemid 351264130)
50. 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)
51. Ma Z, Jacobsen FE, Giedroc DP (2009) Coordination chemistry of bacterial metal transport and sensing. Chem Rev 109:4644-4681.
52. Li Z, Okamoto K-I, Hayashi Y, Sheng M (2004) The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell 119:873-887. (Pubitemid 40017692)
53. El Meskini R, Cline LB, Eipper BA, Ronnett GV (2005) The developmentally regulated expression of Menkes protein ATP7A suggests a role in axon extension and synaptogenesis. Dev Neurosci Basel 27:333-348. (Pubitemid 41243221)
54. El Meskini R, et al. (2007) ATP7A (Menkes protein) functions in axonal targeting and synaptogenesis. Mol Cell Neurosci 34:409-421. (Pubitemid 46330045)