Visualizing Metal Content and Intracellular Distribution in Primary Hippocampal Neurons with Synchrotron X-Ray Fluorescence

PLoS ONE

Volumn 11, Issue 7, 2016, Pages

  Colvin, Robert A ^a   Jin, Qiaoling ^b   Lai, Barry ^c   Kiedrowski, Lech ^d,e  

^a OHIO UNIVERSITY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c ARGONNE NATIONAL LABORATORY   (United States)

^d United States of America ^*  (United States)

^e UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; COPPER; IRON; MANGANESE; METAL; SIDEROPHORE; ZINC;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN LEVEL; BRAIN REGION; CELL LEVEL; CELL ORGANELLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSOL; DENTATE GYRUS; EMBRYO; ENDOPLASMIC RETICULUM; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL NEURONAL CULTURE; IRON PUNCTA; MITOCHONDRION; NONHUMAN; QUANTITATIVE ANALYSIS; RAT; SYNAPSE; SYNCHROTRON RADIATION; X RAY FLUORESCENCE; ZINCOSOME; ANIMAL; CELL NUCLEUS; FREEZING; MAMMALIAN EMBRYO; METABOLISM; NERVE CELL; PRIMARY CELL CULTURE; SPECTROMETRY; SYNCHROTRON; ULTRASTRUCTURE;

ANIMALS; CA1 REGION, HIPPOCAMPAL; CALCIUM; CELL NUCLEUS; CEREBRAL CORTEX; COPPER; DENTATE GYRUS; EMBRYO, MAMMALIAN; ENDOPLASMIC RETICULUM; FREEZING; IRON; MANGANESE; MITOCHONDRIA; NEURONS; PRIMARY CELL CULTURE; RATS; SPECTROMETRY, X-RAY EMISSION; SYNCHROTRONS; ZINC;

EID: 84979243377     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0159582     Document Type: Article

References (72)

1. Maret W. Zinc and human disease. In: Sigel A, Sigel H, Sigel RKO, editors. Imterrelations betwen Essential Metal Ions and Human Disease, Metal Ions in Life Sciences. 13: Springer; 2013. p. 389-414.
2. Barnham KJ, Bush AI. Biological metals and metal-targeting compounds in major neurodegenerative diseases. Chemical Society reviews. 2014; 43(19):6727-49. Epub 2014/08/08. doi: 10.1039/ c4cs00138a PMID: 25099276.
3. Bourassa MW, Miller LM. Metal imaging in neurodegenerative diseases. Metallomics. 2012; 4(8):721-38. Epub 2012/07/17. doi: 10.1039/c2mt20052j PMID: 22797194; PubMed Central PMCID: PMC4140182.
4. McRae R, Bagchi P, Sumalekshmy S, Fahrni CJ. In situ imaging of metals in cells and tissues. Chem Rev. 2009; 109(10):4780-827. Epub 2009/09/24. doi: 10.1021/cr900223a PMID: 19772288.
5. Fahrni CJ. Biological applications of X-ray fluorescence microscopy: exploring the subcellular topography and speciation of transition metals. Curr Opin Chem Biol. 2007; 11(2):121-7. Epub 2007/03/14. doi: 10.1016/j.cbpa.2007.02.039 PMID: 17353139.
6. Ortega R, Deves G, Carmona A. Bio-metals imaging and speciation in cells using proton and synchrotron radiation X-ray microspectroscopy. J R Soc Interface. 2009; 6 Suppl 5:S649-58. Epub 2009/07/17. doi: 10.1098/rsif.2009.0166.focus PMID: 19605403; PubMed Central PMCID: PMC2843977.
7. Frederickson CJ, Suh SW, Silva D, Frederickson CJ, Thompson RB. Importance of Zinc in the Central Nervous System: The Zinc-Containing Neuron. The Journal of nutrition. 2000; 130(5):1471S-83S.
8. Chwiej J, Dulinska J, Janeczko K, Appel K, Setkowicz Z. Variations in elemental compositions of rat hippocampal formation between acute and latent phases of pilocarpine-induced epilepsy: an X-ray fluorescence microscopy study. J Biol Inorg Chem. 2012; 17(5):731-9. Epub 2012/03/27. doi: 10.1007/ s00775-012-0892-1 PMID: 22447169.
9. Chwiej J, Gabrys H, Janeczko K, Kutorasinska J, Gzielo-Jurek K, Matusiak K, et al. Elemental anomalies in the hippocampal formation after repetitive electrical stimulation: an X-ray fluorescence microscopy study. J Biol Inorg Chem. 2014; 19(7):1209-20. Epub 2014/07/17. doi: 10.1007/s00775-014-1177-7 PMID: 25027680; PubMed Central PMCID: PMC4175042.
10. Robison G, Zakharova T, Fu S, Jiang W, Fulper R, Barrea R, et al. X-ray fluorescence imaging of the hippocampal formation after manganese exposure. Metallomics. 2013; 5(11):1554-65. Epub 2013/09/ 04. doi: 10.1039/c3mt00133d PMID: 23999853; PubMed Central PMCID: PMC3892963.
11. Lavenex P. Functional anatomy, development, and pathology of the hippocampus. In: Bartsch T, editor. The Clinical Neurobiology of the Hippocampus: An integrative view. United Kungdom: Oxford; 2012. p. 10-38.
12. Prasad A, S. Zinc and Neurobiology. Biochemistry of Zinc. Biochemistry of the Elements. 11. New York, New York: Plenum Press; 1993. p. 149-64.
13. Michaelis EK. Selective Neuronal Vulnerability in the Hippocampus: Relationship to Neurological Diseases and Mechanisms for Differential Sensitivity of Neurons to Stress. In: Bartsch T, editor. The Clinical Neurobiology of the Hippocampus: An integrative view. Oxford Scholarship Online: Oxford University Press; 2012. p. 55-71.
14. Pivovarova NB, Stanika RI, Kazanina G, Villanueva I, Andrews SB. The interactive roles of zinc and calcium in mitochondrial dysfunction and neurodegeneration. Journal of Neurochemistry. 2014; 128 (4):592-602. doi: 10.1111/jnc.12489 PMID: 24127746
15. Robison G, Zakharova T, Fu S, Jiang W, Fulper R, Barrea R, et al. X-ray fluorescence imaging: a new tool for studying manganese neurotoxicity. PLoS ONE. 2012; 7(11):e48899. Epub 2012/11/28. doi: 10. 1371/journal.pone.0048899 PMID: 23185282; PubMed Central PMCID: PMC3501493.
16. Robison G, Sullivan B, Cannon JR, Pushkar Y. Identification of dopaminergic neurons of the substantia nigra pars compacta as a target of manganese accumulation. Metallomics. 2015; 7(5):748-55. doi: 10. 1039/c5mt00023h PMID: 25695229
17. Colvin RA, Lai B, Holmes WR, Lee D. Understanding metal homeostasis in primary cultured neurons. Studies using single neuron subcellular and quantitative metallomics. Metallomics. 2015; 7(7):1111-23. doi: 10.1039/c5mt00084j PMID: 25894020
18. Ciccotosto GD, James SA, Altissimo M, Paterson D, Vogt S, Lai B, et al. Quantitation and localization of intracellular redox active metals by X-ray fluorescence microscopy in cortical neurons derived from APP and APLP2 knockout tissue. Metallomics. 2014; 6(10):1894-904. doi: 10.1039/c4mt00176a PMID: 25098278
19. Kiedrowski L. Neuronal acid-induced [Zn2+]i elevations calibrated using the low-affinity ratiometric probe FuraZin-1. Journal of Neurochemistry. 2015; 135(4):777-86. doi: 10.1111/jnc.13282 PMID: 26263185
20. Kiedrowski L. Proton-dependent zinc release from intracellular ligands. J Neurochem. 2014; 130 (1):87-96. Epub 2014/03/13. doi: 10.1111/jnc.12712 PMID: 24606401; PubMed Central PMCID: PMC4130388.
21. Jin Q, Vogt S, Lai B, Chen S, Finney L, Gleber SC, et al. Ultraviolet germicidal irradiation and its effects on elemental distributions in mouse embryonic fibroblast cells in x-ray fluorescence microanalysis. PLoS ONE. 2015; 10(2):e0117437. Epub 2015/02/24. doi: 10.1371/journal.pone.0117437 PMID: 25706293; PubMed Central PMCID: PMC4338249.
22. Qin Z, Toursarkissian B, Lai B. Synchroton radiation X-ray fluorescence microscopy reveals a spatial association of copper on elastic laminae in rat aortic media. Metallomics. 2011; 3:823-8. doi: 10.1039/ c1mt00033k PMID: 21589993
23. Vogt S. MAPS: A set of software tools for analysis and visualization of 3D X-ray fluorescence data sets. Journal of Physiology IV. 2003; 104:635-8.
24. Colvin RA, Stork CJ, Li YV, Lai B. Exploring the Zinc Metallome of Cultured Cortical Neurons Using Synchroton Radiation X-Ray Fluorescence Microscopy. In: Li YV, Zhang JH, editors. Metal Ion in Stroke. Springer Series in Translational Stroke Research. New York: Springer; 2012. p. 227-37.
25. Duèić T, Carboni E, Lai B, Chen S, Michalke B, Lázaro DF, et al. Alpha-Synuclein Regulates Neuronal Levels of Manganese and Calcium. ACS Chemical Neuroscience. 2015; 6(10):1769-79. doi: 10.1021/ acschemneuro.5b00093 PMID: 26284970
26. Kosior E, Bohic S, Suhonen H, Ortega R, Deves G, Carmona A, et al. Combined use of hard X-ray phase contrast imaging and X-ray fluorescence microscopy for sub-cellular metal quantification. J Struct Biol. 2012; 177(2):239-47. Epub 2011/12/21. doi: 10.1016/j.jsb.2011.12.005 PMID: 22182730.
27. Colvin RA, Bush AI, Volitakis I, Fontaine CP, Thomas D, Kikuchi K, et al. Insights into Zn2+ homeostasis in neurons from experimental and modeling studies. Am J Physiol Cell Physiol. 2008; 294(3):C726-42. Epub 2008/01/11. doi: 10.1152/ajpcell.00541.2007 PMID: 18184873.
28. Krezel A, Maret W. Zinc-buffering capacity of a eukaryotic cell at physiological pZn. J Biol Inorg Chem. 2006; 11(8):1049-62. PMID: 16924557
29. Colvin RA, Holmes WR, Fontaine CP, Maret W. Cytosolic zinc buffering and muffling: their role in intracellular zinc homeostasis. Metallomics. 2010; 2(5):306-17. Epub 2010/11/12. doi: 10.1039/b926662c PMID: 21069178.
30. Cassell MD, Brown MW. The distribution of Timm's stain in the nonsulphide-perfused human hippocampal formation. The Journal of Comparative Neurology. 1984; 222(3):461-71. doi: 10.1002/cne. 902220311 PMID: 6199383
31. Haug FM. On the normal histochemistry of trace metals in the brain. Journal fur Hirnforschung. 1975; 16(2):151-62. Epub 1975/01/01. PMID: 1214048.
32. Frederickson CJ, Kasarskis EJ, Ringo D, Frederickson RE. A quinoline fluorescence method for visualizing and assaying the histochemically reactive zinc (bouton zinc) in the brain. J Neurosci Methods. 1987; 20(2):91-103. Epub 1987/06/01. PMID: 3600033.
33. Lear J, Hare DJ, Fryer F, Adlard PA, Finkelstein DI, Doble PA. High-resolution elemental bioimaging of Ca, Mn, Fe, Co, Cu, and Zn employing LA-ICP-MS and hydrogen reaction gas. Anal Chem. 2012; 84 (15):6707-14. Epub 2012/07/04. doi: 10.1021/ac301156f PMID: 22746971.
34. Hare DJ, Lee JK, Beavis AD, van Gramberg A, George J, Adlard PA, et al. Three-dimensional atlas of iron, copper, and zinc in the mouse cerebrum and brainstem. Anal Chem. 2012; 84(9):3990-7. Epub 2012/04/03. doi: 10.1021/ac300374x PMID: 22462591.
35. Hare DJ, George JL, Grimm R, Wilkins S, Adlard PA, Cherny RA, et al. Three-dimensional elemental bio-imaging of Fe, Zn, Cu, Mn and P in a 6-hydroxydopamine lesioned mouse brain. Metallomics. 2010; 2(11):745-53. Epub 2010/11/13. doi: 10.1039/c0mt00039f PMID: 21072366.
36. Leskovjan AC, Kretlow A, Lanzirotti A, Barrea R, Vogt S, Miller LM. Increased brain iron coincides with early plaque formation in a mouse model of Alzheimer's disease. NeuroImage. 2011; 55(1):32-8. Epub 2010/12/
37. Danscher G, Jensen KB, Frederickson CJ, Kemp K, Andreasen A, Juhl S, et al. Increased amount of zinc in the hippocampus and amygdala of Alzheimer's diseased brains: a proton-induced X-ray emission spectroscopic analysis of cryostat sections from autopsy material. J Neurosci Methods. 1997; 76 (1):53-9. Epub 1997/10/23. PMID: 9334939.
38. Kemp K, Danscher G. Multi-element analysis of the rat hippocampus by proton induced X-ray emission spectroscopy (phosphorus, sulphur, chlorine, potassium, calcium, iron, zinc, copper, lead, bromine, and rubidium). Histochemistry. 1979; 59(3):167-76. PMID: 429203
39. Wegst-Uhrich S, Mullin E, Ding D, Manohar S, Salvi R, Aga D, et al. Endogenous concentrations of biologically relevant metals in rat brain and cochlea determined by inductively coupled plasma mass spectrometry. BioMetals. 2015; 28(1):187-96. doi: 10.1007/s10534-014-9814-8 PMID: 25537479
40. Cole TB, Wenzel HJ, Kafer KE, Schwartzkroin PA, Palmiter RD. Elimination of zinc from synaptic vesicles in the intact mouse brain by disruption of the ZnT3 gene. Proc Natl Acad Sci U S A. 1999; 96 (4):1716-21. PMID: 9990090
41. Palmiter RD, Cole TB, Quaife CJ, Findley SD. ZnT-3, a putative transporter of zinc into synaptic vesicles. Proceedings of the National Academy of Sciences of the United States of America. 1996; 93:14934-9. PMID: 8962159
42. Wenzel HJ, Cole TB, Born DE, Schwartzkroin PA, Palmiter RD. Ultrastructral localization of zinc transporter-3 (ZnT-3) to synaptic vesicle membranes within mossy fiber boutons in the hippocampus of mouse and monkey. Proceedings of the National Academy of Sciences of the United States of America. 1997; 94(23):12676-81. PMID: 9356509
43. Sekler I, Silverman WF. Zinc homeostasis and signaling in glia. Glia. 2012; 60(6):843-50. Epub 2012/ 02/14. doi: 10.1002/glia.22286 PMID: 22328236.
44. Hare DJ, Grubman A, Ryan TM, Lothian A, Liddell JR, Grimm R, et al. Profiling the iron, copper and zinc content in primary neuron and astrocyte cultures by rapid online quantitative size exclusion chromatography-inductively coupled plasma-mass spectrometry. Metallomics. 2013; 5(12):1656-62. Epub 2013/10/18. doi: 10.1039/c3mt00227f PMID: 24132241.
45. Cerchiaro G, Manieri TM, Bertuchi FR. Analytical methods for copper, zinc and iron quantification in mammalian cells. Metallomics. 2013; 5(10):1336-45. doi: 10.1039/c3mt00136a PMID: 23925479
46. Bozym R, Hurst TK, Westerberg N, Stoddard A, Fierke CA, Frederickson CJ, et al. Determination of zinc using carbonic anhydrase-based fluorescence biosensors. Methods Enzymol. 2008; 450:287-309. Epub 2009/01/21. doi: 10.1016/S0076-6879(08)03414-9 PMID: 19152866.
47. Frederickson CJ, Giblin LJ, Krezel A, McAdoo DJ, Muelle RN, Zeng Y, et al. Concentrations of extracellular free zinc (pZn)e in the central nervous system during simple anesthetization, ischemia and reperfusion. Exp Neurol. 2006; 198(2):285-93. PMID: 16443223
48. Ranaldi G, Perozzi G, Truong-Tran A, Zalewski P, Murgia C. Intracellular distribution of labile Zn(II) and zinc transporter expression in kidney and MDCK cells. Am J Physiol Renal Physiol. 2002; 283(6): F1365-75. PMID: 12388418
49. Colvin RA, Laskowski M, Fontaine CP. Zinquin identifies subcellular compartmentalization of zinc in cortical neurons. Relation to the trafficking of zinc and the mitochondrial compartment. Brain Res. 2006; 1085(1):1-10. Epub 2006/04/04. doi: 10.1016/j.brainres.2006.02.043 PMID: 16581038.
50. Colvin RA. pH dependence and compartmentalization of zinc transported across plasma membrane of rat cortical neurons. Am J Physiol Cell Physiol. 2002; 282(2):C317-29. Epub 2002/01/15. doi: 10.1152/ ajpcell.00143.2001 PMID: 11788343.
51. Eide DJ. Zinc transporters and the cellular trafficking of zinc. Biochim Biophys Acta. 2006; 1763 (7):711-22. PMID: 16675045
52. Burdette SC, Walkup GK, Spingler B, Tsien RY, Lippard SJ. Fluorescent sensors for Zn(2+) based on a fluorescein platform: synthesis, properties and intracellular distribution. J Am Chem Soc. 2001; 123 (32):7831-41. Epub 2001/08/09. PMID: 11493056.
53. Duèić T, Barski E, Salome M, Koch JC, Bähr M, Lingor P. X-ray fluorescence analysis of iron and manganese distribution in primary dopaminergic neurons. Journal of Neurochemistry. 2013; 124(2):250-61. doi: 10.1111/jnc.12073 PMID: 23106162
54. Ghadially FN. Siderosomes, hemosiderin, and ferritin. In: Ghadially FN, editor. Ultrastructural Pathology of the Cell and Matrix. 2. 4th ed. Boston: Butterworth-Heinemann; 1997. p. 668-74.
55. Sato S, Murphy GF, Bernhard JD, Mihm MC Jr., Fitzpatrick TB. Ultrastructural and x-ray microanalytical observations of minocycline-related hyperpigmentation of the skin. The Journal of investigative dermatology. 1981; 77(3):264-71. Epub 1981/09/01. PMID: 7264358.
56. Ortega R, Carmona A, Roudeau S, Perrin L, Duèić T, Carboni E, et al. α-Synuclein Over-Expression Induces Increased Iron Accumulation and Redistribution in Iron-Exposed Neurons. Molecular Neurobiology. 2015; 53(3):1925-34. doi: 10.1007/s12035-015-9146-x PMID: 25833099
57. Rouault TA. Iron metabolism in the CNS: implications for neurodegenerative diseases. Nat Rev Neurosci. 2013; 14(8):551-64. doi: 10.1038/nrn3453 PMID: 23820773
58. Brewer GJ. Serum-free B27/neurobasal medium supports differentiated growth of neurons from the striatum, substantia nigra, septum, cerebral cortex, cerebellum, and dentate gyrus. J Neurosci Res. 1995; 42(5):674-83. PMID: 8600300
59. Hare D, Ayton S, Bush A, Lei P. A delicate balance: Iron metabolism and diseases of the brain. Frontiers in Aging Neuroscience. 2013; 5:34. doi: 10.3389/fnagi.2013.00034 PMC3715022. PMID: 23874300
60. Dixon SJ, Stockwell BR. The role of iron and reactive oxygen species in cell death. Nat Chem Biol. 2014; 10(1):9-17. doi: 10.1038/nchembio.1416 PMID: 24346035
61. Rouault TA. Mammalian iron-sulphur proteins: novel insights into biogenesis and function. Nat Rev Mol Cell Biol. 2015; 16(1):45-55. doi: 10.1038/nrm3909 PMID: 25425402
62. Lane DJR, Merlot AM, Huang MLH, Bae DH, Jansson PJ, Sahni S, et al. Cellular iron uptake, trafficking and metabolism: Key molecules and mechanisms and their roles in disease. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research. 2015; 1853(5):1130-44. http://dx.doi.org/10.1016/j.bbamcr. 2015.01.021.
63. Antharam V, Collingwood JF, Bullivant JP, Davidson MR, Chandra S, Mikhaylova A, et al. High field magnetic resonance microscopy of the human hippocampus in Alzheimer's disease: quantitative imaging and correlation with iron. NeuroImage. 2012; 59(2):1249-60. Epub 2011/08/27. doi: 10.1016/j. neuroimage.2011.08.019 PMID: 21867761; PubMed Central PMCID: PMC3690369.
64. Andrási E, Farkas É, Scheibler H, Réffy A, Bezúr L. Al, Zn, Cu, Mn and Fe levels in brain in Alzheimer's disease. Archives of gerontology and geriatrics. 1995; 21(1):89-97. http://dx.doi.org/10.1016/0167-4943(95)00643-Y. PMID: 15374228
65. Deibel MA, Ehmann WD, Markesbery WR. Copper, iron, and zinc imbalances in severely degenerated brain regions in Alzheimer's disease: possible relation to oxidative stress. Journal of the Neurological Sciences. 1996; 143(1-2):137-42. http://dx.doi.org/10.1016/S0022-510X(96)00203-1. PMID: 8981312
66. Raven EP, Lu PH, Tishler TA, Heydari P, Bartzokis G. Increased Iron Levels and Decreased Tissue Integrity in Hippocampus of Alzheimer's Disease Detected in vivo with Magnetic Resonance Imaging. Journal of Alzheimer's Disease. 2013; 37(1):127-36. doi: 10.3233/jad-130209 PMID: 23792695
67. Schröder N, Figueiredo LS, de Lima MNM. Role of Brain Iron Accumulation in Cognitive Dysfunction: Evidence from Animal Models and Human Studies. Journal of Alzheimer's Disease. 2013; 34(4):797-812. doi: 10.3233/jad-121996 PMID: 23271321
68. de Lima MNM, Dias CP, Torres JP, Dornelles A, Garcia VA, Scalco FS, et al. Reversion of age-related recognition memory impairment by iron chelation in rats. Neurobiology of Aging. 2008; 29(7):1052-9. http://dx.doi.org/10.1016/j.neurobiolaging.2007.02.006. PMID: 17346856
69. Horning KJ, Caito SW, Tipps KG, Bowman AB, Aschner M. Manganese Is Essential for Neuronal Health. Annual Review of Nutrition. 2015; 35(1):71-108. doi: 10.1146/annurev-nutr-071714-034419 PMID: 25974698.
70. Chen P, Chakraborty S, Mukhopadhyay S, Lee E, Paoliello MMB, Bowman AB, et al. Manganese homeostasis in the nervous system. Journal of Neurochemistry. 2015; 134(4):601-10. doi: 10.1111/ jnc.13170 PMID: 25982296
71. Carmona A, Deves G, Roudeau S, Cloetens P, Bohic S, Ortega R. Manganese accumulates within golgi apparatus in dopaminergic cells as revealed by synchrotron X-ray fluorescence nanoimaging. ACS Chem Neurosci. 2010; 1(3):194-203. Epub 2010/03/17. doi: 10.1021/cn900021z PMID: 22778823; PubMed Central PMCID: PMC3368660.
72. Daoust A, Saoudi Y, Brocard J, Collomb N, Batandier C, Bisbal M, et al. Impact of manganese on primary hippocampal neurons from rodents. Hippocampus. 2014; 24(5):598-610. doi: 10.1002/hipo. 22252 PMID: 24500839