Biological applications of X-ray fluorescence microscopy: exploring the subcellular topography and speciation of transition metals

Current Opinion in Chemical Biology

Volumn 11, Issue 2, 2007, Pages 121-127

  Fahrni, Christoph J ^a  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; CHROMIUM; CISPLATIN; COPPER; HEAVY METAL; IRON; METAL ION; TRANSITION ELEMENT; ZINC;

ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; BRAIN TISSUE; CELLULAR DISTRIBUTION; DEGENERATIVE DISEASE; DIAGNOSTIC IMAGING; DRUG ABSORPTION; DRUG METABOLISM; ESCHERICHIA COLI; FLUORESCENCE MICROSCOPY; HUMAN; INFECTION; INTOXICATION; NERVE CELL; NONHUMAN; PARKINSON DISEASE; PHYTOPLANKTON; PSEUDOMONAS FLUORESCENS; REVIEW; TISSUE SECTION; WHOLE CELL; WILSON DISEASE; X RAY FLUORESCENCE;

ANIMALS; BACTERIA; CHROMIUM; CISPLATIN; COPPER; ELECTRON PROBE MICROANALYSIS; HUMANS; MICROSCOPY, FLUORESCENCE; NANOPARTICLES; NEURODEGENERATIVE DISEASES; SYNCHROTRONS; TRANSITION ELEMENTS;

EID: 34047112462     PISSN: 13675931     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpa.2007.02.039     Document Type: Review

References (48)

1. Finney L.A., and O'Halloran T.V. Transition metal speciation in the cell: insights from the chemistry of metal ion receptors. Science 300 (2003) 931-936
2. Kikuchi K., Komatsu K., and Nagano T. Zinc sensing for cellular application. Curr Opin Chem Biol 8 (2004) 182-191
3. Yang L.C., McRae R., Henary M.M., Patel R., Lai B., Vogt S., and 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 USA 102 (2005) 11179-11184. Correlative optical fluorescence and SXRF microscopy studies with Cu-loaded mouse fibroblast cells suggest the presence of a kinetically labile intracellular Cu pool that is localized in the Golgi apparatus and mitochondria. Micro-XANES spectra acquired at various subcellular locations indicate the presence of low-coordinate monovalent Cu.
4. Zeng L., Miller E.W., Pralle A., Isacoff E.Y., and Chang C.J. A selective turn-on fluorescent sensor for imaging copper in living cells. J Am Chem Soc 128 (2006) 10-11
5. Ortega R. Chemical elements distribution in cells. Nucl Inst Meth Phys Res B 231 (2005) 218-223
6. Paunesku T., Vogt S., Maser J., Lai B., and Woloschak G. X-ray fluorescence microprobe imaging in biology and medicine. J Cell Biochem 99 (2006) 1489-1502. A comprehensive overview of recent applications of X-ray fluorescence microscopy in biology and medicine.
7. Dillon C.T., Kennedy B.J., Lay P.A., Lai B., Cai Z., Stampfl A.P.J., Ilinski P., Legnini D., Maser J., Rodrigues W., et al. Implementation of X-ray microscopy and micro-XANES analysis for investigations of the cellular uptake and cellular metabolism of transition metals. J Phys IV 104 (2003) 293-296
8. Bertsch P.M., and Hunter D.B. Applications of synchrotron-based X-ray microprobes. Chem Rev 101 (2001) 1809-1842
9. Matsuyama S., Mimura H., Yumoto H., Sano Y., Yamamura K., Yabashi M., Nishino Y., Tamasaku K., Ishikawa T., and Yamauchi K. Development of scanning X-ray fluorescence microscope with spatial resolution of 30 nm using Kirkpatrick-Baez mirror optics. Rev Sci Instrum 77 (2006) 103102
10. Ortega R., Bohic S., Tucoulou R., Somogyi A., and Devès G. Microchemical element imaging of yeast and human cells using synchrotron X-ray microprobe with Kirkpatrick-Baez optics. Anal Chem 76 (2004) 309-314
11. Snigirev A., Kohn V., Snigireva I., and Lengeler B. A compound refractive lens for focusing high-energy X-rays. Nature 384 (1996) 49-51
12. Di Fabrizio E., Romanato F., Gentili M., Cabrini S., Kaulich B., Susini J., and Barrett R. High-efficiency multilevel zone plates for keV X-rays. Nature 401 (1999) 895-898
13. Twining B.S., Baines S.B., Fisher N.S., Maser J., Vogt S., Jacobsen C., Tovar-Sanchez A., and Sañudo-Wilhelmy S.A. Quantifying trace elements in individual aquatic protist cells with a synchrotron X-ray fluorescence microprobe. Anal Chem 75 (2003) 3806-3816
14. Kemner K.M., Kelly S.D., Lai B., Maser J., O'Loughlin E.J., Sholto-Douglas D., Cai Z.H., Schneegurt M.A., Kulpa Jr. C.F., and Nealson K.H. Elemental and redox analysis of single bacterial cells by X-ray microbeam analysis. Science 306 (2004) 686-687. The authors used SXRF microscopy to map the intracellular elemental distribution of individual Pseudomonas fluorescens microbes at spatial scales of 150 nm. The study revealed compelling differences in Cr uptake for planktonic compared with attached cells.
15. Ide-Ektessabi A., Fujisawa S., and Yoshida S. Chemical state imaging of iron in nerve cells from a patient with Parkinsonism-dementia complex. J Appl Phys 91 (2002) 1613-1617
16. Ide-Ektessabi A., and Rabionet M. The role of trace metallic elements in neurodegenerative disorders: quantitative analysis using XRF and XANES spectroscopy. Anal Sci 21 (2005) 885-892
17. Miller L.M., Wang Q., Telivala T.P., Smith R.J., Lanzirotti A., and Miklossy J. Synchrotron-based infrared and X-ray imaging shows focalized accumulation of Cu and Zn co-localized with β-amyloid deposits in Alzheimer's disease. J Struct Biol 155 (2006) 30-37. Brain tissue of Alzheimer's disease patients was analyzed by means of correlative synchrotron Fourier transform infrared micro-spectroscopy (FTIRM) and SXRF microscopy. The study demonstrated for the first time a strong spatial correlation between elevated β-sheet content in Aβ plaques and accumulations of metal ions in these areas.
18. Szczerbowska-Boruchowska M., Chwiej J., Lankosz M., Adamek D., Wojcik S., Krygowska-Wajs A., Tomik B., Bohic S., Susini J., Simionovici A., et al. Intraneuronal investigations of organic components and trace elements with the use of synchrotron radiation. X-Ray Spectrom 34 (2005) 514-520
19. Szczerbowska-Boruchowska M., Lankosz M., Ostachowicz J., Adamek D., Krygowska-Wajs A., Tomik B., Szczudlik A., Simionovici A., and Bohic S. Topographic and quantitative microanalysis of human central nervous system tissue using synchrotron radiation. X-Ray Spectrom 33 (2004) 3-11
20. Tomik B., Chwiej J., Szczerbowska-Boruchowska M., Lankosz M., Wojcik S., Adamek D., Falkenberg G., Bohic S., Simionovici A., Stegowski Z., et al. Implementation of X-ray fluorescence microscopy for investigation of elemental abnormalities in amyotrophic lateral sclerosis. Neurochem Res 31 (2006) 321-331
21. Yoshida S., Ide-Ektessabi A., and Fujisawa S. Application of synchrotron radiation in neuromicrobiology: role of iron in Parkinson's disease. Struct Chem 14 (2003) 85-95
22. Rae T.D., Schmidt P.J., Pufahl R.A., Culotta V.C., and O'Halloran T.V. Undetectable intracellular free copper: the requirement of a copper chaperone for superoxide dismutase. Science 284 (1999) 805-808
23. Ralle M., Blackburn N.J., and Lutsenko S. Using XAS and SXRF to study copper in Wilson disease at the molecular and tissue level. AIP Conference Proceedings 882, 13th International Conference on X-ray Absorption Fine Structure, XAFS13 (2006) 328-330
24. Wagner D., Maser J., Lai B., Cai Z.H., Barry III C.E., Höner zu Bentrup K., Russell D.G., and Bermudez L.E. Elemental analysis of Mycobacterium avium-, Mycobacterium tuberculosis-, and Mycobacterium smegmatis-containing phagosomes indicates pathogen-induced microenvironments within the host cell's endosomal system. J Immunol 174 (2005) 1491-1500. The authors studied changes of the elemental composition in phagosome of macrophages when they were infected with various mycobacteria strains. SXRF elemental maps revealed a significant increase of the phagosomal Fe concentration in macrophages that were infected with pathogenic mycobacteria.
25. Levina A., and Lay P.A. Mechanistic studies of relevance to the biological activities of chromium. Coord Chem Rev 249 (2005) 281-298
26. Dillon C.T., Lay P.A., Kennedy B.J., Stampfl A.P.J., Cai Z.H., Ilinski P., Rodrigues W., Legnini D.G., Lai B., and Maser J. Hard X-ray microprobe studies of chromium(VI)-treated V79 Chinese hamster lung cells: intracellular mapping of the biotransformation products of a chromium carcinogen. J Biol Inorg Chem 7 (2002) 640-645
27. Harris H.H., Levina A., Dillon C.T., Mulyani I., Lai B., Cai Z.H., and Lay P.A. Time-dependent uptake, distribution and biotransformation of chromium(VI) in individual and bulk human lung cells: application of synchrotron radiation techniques. J Biol Inorg Chem 10 (2005) 105-118. SXRF microscopy studies on Cr(VI)-treated human lung cells revealed intriguing time-dependent differences of the subcellular Cr distribution. Detailed X-ray spectroscopic analyses of bulk cell samples provided insights into the chemical speciation of intracellular Cr.
28. Ortega R., Fayard B., Salomé M., Devès G., and Susini J. Chromium oxidation state imaging in mammalian cells exposed in vitro to soluble or particulate chromate compounds. Chem Res Toxicol 18 (2005) 1512-1519. The authors used SXRF microscopy to gain insights into the toxicology of sparingly soluble Cr(VI) complexes. The studies indicated that intracellular Cr(III) originates from extracellular dissolution followed by uptake and subsequent reduction rather than from phagocytosed Cr(VI) particles.
29. Connett P.H., and Wetterhahn K.E. Metabolism of the carcinogen chromate by cellular-constituents. Struct Bond 54 (1983) 93-124
30. Wise J.P., Orenstein J.M., and Patierno S.R. Inhibition of lead chromate clastogenesis by ascorbate - relationship to particle dissolution and uptake. Carcinogenesis 14 (1993) 429-434
31. Xie H., Holmes A.L., Wise S.S., Gordon N., and Wise J.P. Lead chromate-induced chromosome damage requires extracellular dissolution to liberate chromium ions but does not require particle internalization or intracellular dissolution. Chem Res Toxicol 17 (2004) 1362-1367
32. Farrell N. Biomedical uses and applications of inorganic chemistry. An overview. Coord Chem Rev 232 (2002) 1-4
33. Zhang C.X., and Lippard S.J. New metal complexes as potential therapeutics. Curr Opin Chem Biol 7 (2003) 481-489
34. Storr T., Thompson K.H., and Orvig C. Design of targeting ligands in medicinal inorganic chemistry. Chem Soc Rev 35 (2006) 534-544
35. Hall M.D., Alderden R.A., Zhang M., Beale P.J., Cai Z.H., Lai B., Stampfl A.P.J., and Hambley T.W. The fate of platinum(II) and platinum(IV) anti-cancer agents in cancer cells and tumours. J Struct Biol 155 (2006) 38-44
36. Hall M.D., Dillon C.T., Zhang M., Beale P., Cai Z.H., Lai B., Stampfl A.P.J., and Hambley T.W. The cellular distribution and oxidation state of platinum(II) and platinum(IV) antitumour complexes in cancer cells. J Biol Inorg Chem 8 (2003) 726-732
37. Wong E., and Giandomenico C.M. Current status of platinum-based antitumor drugs. Chem Rev 99 (1999) 2451-2466
38. Hall M.D., Foran G.J., Zhang M., Beale P.J., and Hambley T.W. XANES determination of the platinum oxidation state distribution in cancer cells treated with platinum(IV) anticancer agents. J Am Chem Soc 125 (2003) 7524-7525
39. Shimura M., Saito A., Matsuyama S., Sakuma T., Terui Y., Ueno K., Yumoto H., Yamauchi K., Yamamura K., Mimura H., et al. Element array by scanning X-ray fluorescence microscopy after cis-diamminedichloro-platinum(II) treatment. Cancer Res 65 (2005) 4998-5002
40. Chen K.G., Valencia J.C., Lai B., Zhang G.F., Paterson J.K., Rouzaud F., Berens W., Wincovitch S.M., Garfield S.H., Leapman R.D., et al. Melanosomal sequestration of cytotoxic drugs contributes to the intractability of malignant melanomas. Proc Natl Acad Sci USA 103 (2006) 9903-9907. The authors investigated in this study possible mechanisms for the multidrug resistance of malignant melanomas. SXRF microscopy demonstrated that cisplatin, a cytotoxic drug, is sequestered in melanosomes, a process that significantly reduced nuclear localization of the drug when compared with nonmelanoma cells.
41. Clarke M.J., Zhu F.C., and Frasca D.R. Non-platinum chemotherapeutic metallopharmaceuticals. Chem Rev 99 (1999) 2511-2533
42. Waern J.B., Harris H.H., Lai B., Cai Z.H., Harding M.M., and Dillon C.T. Intracellular mapping of the distribution of metals derived from the antitumor metallocenes. J Biol Inorg Chem 10 (2005) 443-452
43. Harding M.M., and Mokdsi G. Antitumour metallocenes: structure-activity studies and interactions with biomolecules. Curr Med Chem 7 (2000) 1289-1303
44. Moghimi S.M., Hunter A.C., and Murray J.C. Nanomedicine: current status and future prospects. FASEB J 19 (2005) 311-330
45. 2-oligonucleotide nanocomposites. Nat Mater 2 (2003) 343-346
46. McRae R., Lai B., Vogt S., and Fahrni C.J. Correlative microXRF and optical immunofluorescence microscopy of adherent cells labeled with ultrasmall gold particles. J Struct Biol 155 (2006) 22-29. The authors demonstrated the utility of ultrasmall gold particles conjugated to a secondary antibody and a small organic fluorophore as label for correlative SXRF and optical immunofluorescence microscopy.
47. Endres P.J., MacRenaris K.W., Vogt S., Allen M.J., and Meade T.J. Quantitative imaging of cell-permeable magnetic resonance contrast agents using X-ray fluorescence. Mol Imaging 5 (2006) 485-497
48. Finney L., Mandava S., Ursos L., Zhang W., Rodi D., Vogt S., Legnini D., Maser J., Ikpatt F., Olopade O.I., and Glesne D. X-ray fluorescence microscopy reveals large-scale relocalization and extracellular translocation of cellular copper during angiogenesis. Proc Natl Acad Sci USA 104 (2007) 2247-2252. High-resolution elemental SXRF imaging of human microvascular endothelial cells revealed a dramatic relocalization of endogenous copper stores from intracellular compartments towards the tips of extended filopodia, thus underscoring the importance of endogenous copper during angiogenesis.