Laser ablation-inductively coupled plasma-mass spectrometry imaging of white and gray matter iron distribution in Alzheimer's disease frontal cortex

NeuroImage

Volumn 137, Issue , 2016, Pages 124-131

  Hare, Dominic J ^a,b   Raven, Erika P ^c,d   Roberts, Blaine R ^b   Bogeski, Mirjana ^b   Portbury, Stuart D ^b   McLean, Catriona A ^e,f   Masters, Colin L ^b   Connor, James R ^g   Bush, Ashley I ^b   Crouch, Peter J ^b   Doble, Philip A ^a  

^a UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

^d NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^e ALFRED HOSPITAL   (Australia)

^f MONASH UNIVERSITY   (Australia)

^g PENN STATE MILTON S HERSHEY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IRON; BIOLOGICAL MARKER;

ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; CASE REPORT; CONTROLLED STUDY; FEMALE; FRONTAL CORTEX; GRAY MATTER; HUMAN; HUMAN TISSUE; IRON STORAGE; LASER ABLATION INDUCTIVELY COUPLED PLASMA MASS SPECTROMETRY; MALE; MASS SPECTROMETRY; MIDDLE AGED; NERVE DEGENERATION; PILOT STUDY; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; TISSUE DISTRIBUTION; VERY ELDERLY; WHITE MATTER; ATOMIC ABSORPTION SPECTROMETRY; FRONTAL LOBE; IN VITRO STUDY; LOW LEVEL LASER THERAPY; METABOLISM; MOLECULAR IMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PROCEDURES; REPRODUCIBILITY; SENSITIVITY AND SPECIFICITY;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; BIOMARKERS; FEMALE; FRONTAL LOBE; GRAY MATTER; HUMANS; IN VITRO TECHNIQUES; IRON; LASER THERAPY; MAGNETIC RESONANCE IMAGING; MALE; MOLECULAR IMAGING; PILOT PROJECTS; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; SPECTROPHOTOMETRY, ATOMIC; TISSUE DISTRIBUTION; WHITE MATTER;

EID: 84973535647     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2016.05.057     Document Type: Article

References (74)

1. Austin C., Fryer F., Lear J., Bishop D., Hare D.J., Rawling T., Doble P. Factors affecting internal standard selection for quantitative elemental bio-imaging of soft tissues by LA-ICP-MS. J. Anal. At. Spectrom. 2011, 26:1494-1501.
2. Bartzokis G., Cummings J.L., Sultzer D., Henderson V.W., Nuechterlein K.H., Mintz J. White matter structural integrity in healthy aging adults and patients with Alzheimer disease: a magnetic resonance imaging study. Arch. Neurol. 2003, 60:393-398.
3. Bartzokis G., Sultzer D., Cummings J., Holt L.E., Hance D.B., Henderson V.W., Mintz J. In vivo evaluation of brain iron in Alzheimer disease using magnetic resonance imaging. Arch. Gen. Psychiatry 2000, 57:47-53.
4. Beilby J.P., Prins A.W., Swanson N.R. Determination of hepatic iron concentration in fresh and paraffin-embedded tissue. Clin. Chem. 1999, 45:573-574.
5. Belaidi A.A., Bush A.I. Iron neurochemistry in Alzheimer's disease and Parkinson' disease: targets for therapeutics. J. Neurochem. 2015.
6. Bilgic B., Pfefferbaum A., Rohlfing T., Sullivan E.V., Adalsteinsson E. MRI estimates of brain iron concentration in normal aging using quantitative susceptibility mapping. NeuroImage 2012, 59:2625-2635.
7. Bishop D.P., Clases D., Fryer F., Williams E., Wilkins S., Hare D.J., Cole N., Karst U., Doble P.A. Elemental bio-imaging using laser ablation-triple quadrupole-ICP-MS. J. Anal. At. Spectrom. 2015.
8. Blasko I., Stampfer Kountchev M., Robatscher P., Veerhuis R., Eikelenboom P., Grubeck Loebenstein B. How chronic inflammation can affect the brain and support the development of Alzheimer's disease in old age: the role of microglia and astrocytes. Aging Cell 2004, 3:169-176.
9. Chen L., Hambright W.S., Na R., Ran Q. Ablation of the ferroptosis inhibitor glutathione peroxidase 4 in neurons results in rapid motor neuron degeneration and paralysis. J. Biol. Chem. 2015, 290:28097-28106.
10. Chételat G., Desgranges B., Landeau B., Mézenge F., Poline J.B., de la Sayette V., Viader F., Eustache F., Baron J.C. Direct voxel-based comparison between grey matter hypometabolism and atrophy in Alzheimer's disease. Brain 2008, 131:60-71.
11. Connor J.R., Menzies S.L. Cellular management of iron in the brain. J. Neurol. Sci. 1995, 134(Suppl.):33-44.
12. Connor J.R., Menzies S.L., St Martin S.M., Mufson E.J. A histochemical study of iron, transferrin, and ferritin in Alzheimer's diseased brains. J. Neurosci. Res. 1992, 31:75-83.
13. Connor J.R., Snyder B.S., Arosio P., Loeffler D.A., LeWitt P. A quantitative analysis of isoferritins in select regions of aged, parkinsonian, and Alzheimer's diseased brains. J. Neurochem. 1995, 65:717-724.
14. Connor J.R., Snyder B.S., Beard J.L., Fine R.E., Mufson E.J. Regional distribution of iron and iron-regulatory proteins in the brain in aging and Alzheimer's disease. J. Neurosci. Res. 1992, 31:327-335.
15. Crespo A.C., Silva B., Marques L., Marcelino E., Maruta C., Costa S., Timóteo A., Vilares A., Couto F.S., Faustino P., Correia A.P., Verdelho A., Porto G., Guerreiro M., Herrero A., Costa C., de Mendonça A., Costa L., Martins M. Genetic and biochemical markers in patients with Alzheimer's disease support a concerted systemic iron homeostasis dysregulation. Neurobiol. Aging 2014, 35:777-785.
16. Daugherty A.M., Raz N. Appraising the role of iron in brain aging and cognition: promises and limitations of MRI methods. Neuropsychol. Rev. 2015, 25:272-287.
17. De Lucia C., Rinchon A., Olmos-Alonso A., Riecken K., Fehse B., Boche D., Perry V.H., Gomez-Nicola D. Microglia regulate hippocampal neurogenesis during chronic neurodegeneration. Brain Behav. Immun. 2015.
18. Dixon S.J., Lemberg K.M., Lamprecht M.R., Skouta R., Zaitsev E.M., Gleason C.E., Patel D.N., Bauer A.J., Cantley A.M., Yang W.S., Morrison B., Stockwell B.R. Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell 2012, 149:1060-1072.
19. Drayer B., Burger P., Darwin R., Riederer S., Herfkens R., Johnson G.A. MRI of brain iron. Am. J. Roentgenol. 1986, 147:103-110.
20. Duce J.A., Tsatsanis A., Cater M.A., James S.A., Robb E., Wikhe K., Leong S.L., Perez K., Johanssen T., Greenough M.A., Cho H.-H., Galatis D., Moir R.D., Masters C.L., McLean C., Tanzi R.E., Cappai R., Barnham K.J., Ciccotosto G.D., Rogers J.T., Bush A.I. Iron-export ferroxidase activity of β-amyloid precursor protein is inhibited by zinc in Alzheimer's disease. Cell 2010, 142:857-867.
21. Duyn J.H., van Gelderen P., Li T.-Q., de Zwart J.A., Koretsky A.P., Fukunaga M. High-field MRI of brain cortical substructure based on signal phase. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:11796-11801.
22. Fukunaga M., Li T.-Q., van Gelderen P., de Zwart J.A., Shmueli K., Yao B., Lee J., Maric D., Aronova M.A., Zhang G., Leapman R.D., Schenck J.F., Merkle H., Duyn J.H. Layer-specific variation of iron content in cerebral cortex as a source of MRI contrast. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:3834-3839.
23. Gellein K., Flaten T.P., Erikson K.M., Aschner M., Syversen T. Leaching of trace elements from biological tissue by formalin fixation. Biol. Trace Elem. Res. 2007, 121:221-225.
24. Gomez-Nicola D., Boche D. Post-mortem analysis of neuroinflammatory changes in human Alzheimer's disease. Alzheimers Res. Ther. 2015, 7:1.
25. Gunning-Dixon F.M., Brickman A.M., Cheng J.C., Alexopoulos G.S. Aging of cerebral white matter: a review of MRI findings. Int. J. Geriatr. Psychiatry 2009, 24:109-117.
26. Hackett M.J., McQuillan J.A., El-Assaad F., Aitken J.B., Levina A., Cohen D.D., Siegele R., Carter E.A., Grau G.E., Hunt N.H., Lay P.A. Chemical alterations to murine brain tissue induced by formalin fixation: implications for biospectroscopic imaging and mapping studies of disease pathogenesis. Analyst 2011, 136:2941.
27. Hallgren B., Sourander P. The effect of age on the non-haemin iron in the human brain. J. Neurochem. 1958, 3:41-51.
28. Hallgren B., Sourander P. The non-haemin iron in the cerebral cortex in Alzheimer's disease. J. Neurochem. 1960, 5:307-310.
29. Hare D.J., Austin C., Doble P. Quantification strategies for elemental imaging of biological samples using laser ablation-inductively coupled plasma-mass spectrometry. Analyst 2012, 137:1527-1537.
30. Hare D.J., Ayton S., Bush A., Lei P. A delicate balance: iron metabolism and diseases of the brain. Front. Aging Neurosci. 2013, 5.
31. Hare D.J., George J.L., Bray L., Volitakis I., Vais A., Ryan T.M., Cherny R.A., Bush A.I., Masters C.L., Adlard P.A. The effect of paraformaldehyde fixation and sucrose cryoprotection on metal concentration in murine neurological tissue. J. Anal. At. Spectrom. 2014.
32. Hare D.J., Gerlach M., Riederer P. Considerations for measuring iron in post-mortem tissue of Parkinson's disease patients. J. Neural Transm. 2012, 119:1515-1521.
33. Hare D.J., Lear J., Bishop D., Beavis A., Doble P.A. Protocol for production of matrix-matched brain tissue standards for imaging by laser ablation-inductively coupled plasma-mass spectrometry. Anal. Methods 2013, 5:1915-1921.
34. Hare D.J., Lei P., Ayton S., Roberts B.R., Grimm R., George J.L., Bishop D.P., Beavis A.D., Donovan S.J., McColl G., Volitakis I., Masters C.L., Adlard P.A., Cherny R.A., Bush A.I., Finkelstein D.I., Doble P.A. An iron-dopamine index predicts risk of parkinsonian neurodegeneration in the substantia nigra pars compacta. Chem. Sci. 2014, 5:2160-2169.
35. Hare D.J., New E.J., de Jonge M.D., McColl G. Imaging metals in biology: balancing sensitivity, selectivity and spatial resolution. Chem. Soc. Rev. 2015, 44:5941-5958.
36. Hebbrecht G., Maenhaut W., Reuck J.D. Brain trace elements and aging. Nucl. Instrum. Methods Phys. Res., Sect. B 1999, 150:208-213.
37. James S.A., Hare D.J., Jenkins N.L., de Jonge M.D., Bush A.I., McColl G. φXANES: in vivo imaging of metal-protein coordination environments. Sci. Rep. 2016, 6:20350.
38. Keep R.F., Hua Y., Xi G. Brain water content: a misunderstood measurement?. Transl. Stroke Res. 2012, 3:263-265.
39. Krebs N., Langkammer C., Goessler W., Ropele S., Fazekas F., Yen K., Scheurer E. Assessment of trace elements in human brain using inductively coupled plasma mass spectrometry. - PubMed - NCBI. J. Trace Elem. Med. Biol. 2014, 28:1-7.
40. Langkammer C., Krebs N., Goessler W., Scheurer E., Ebner F., Yen K., Fazekas F., Ropele S. Quantitative MR imaging of brain iron: a postmortem validation study. Radiology 2010, 257:455-462.
41. Langkammer C., Krebs N., Goessler W., Scheurer E., Yen K., Fazekas F., Ropele S. Susceptibility induced gray-white matter MRI contrast in the human brain. NeuroImage 2012, 59:1413-1419.
42. Langkammer C., Ropele S., Pirpamer L., Fazekas F., Schmidt R. MRI for iron mapping in Alzheimer's disease. Neurodegener. Dis. 2014, 13:189-191.
43. Langkammer C., Schweser F., Krebs N., Deistung A., Goessler W., Scheurer E., Sommer K., Reishofer G., Yen K., Fazekas F., Ropele S., Reichenbach J.R. Quantitative susceptibility mapping (QSM) as a means to measure brain iron? A postmortem validation study. NeuroImage 2012, 62:1593-1599.
44. Lear J., Hare D.J., Fryer F., Adlard P.A., Finkelstein D.I., Doble P.A. High-resolution elemental bioimaging of Ca, Mn, Fe, Co, Cu, and Zn employing LA-ICP-MS and hydrogen reaction gas. Anal. Chem. 2012, 84:6707-6714.
45. Leskovjan A.C., Kretlow A., Lanzirotti A., Barrea R., Vogt S., Miller L.M. Increased brain iron coincides with early plaque formation in a mouse model of Alzheimer's disease. NeuroImage 2011, 55:32-38.
46. Lodygensky G.A., Marques J.P., Maddage R., Perroud E., Sizonenko S.V., Hüppi P.S., Gruetter R. In vivo assessment of myelination by phase imaging at high magnetic field. NeuroImage 2012, 59:1979-1987.
47. Lovell M.A., Robertson J.D., Teesdale W.J., Campbell J.L., Markesbery W.R. Copper, iron and zinc in Alzheimer's disease senile plaques. J. Neurol. Sci. 1998, 158:47-52.
48. Medina D., deToledo-Morrell L., Urresta F., Gabrieli J.D.E., Moseley M., Fleischman D., Bennett D.A., Leurgans S., Turner D.A., Stebbins G.T. White matter changes in mild cognitive impairment and AD: a diffusion tensor imaging study. Neurobiol. Aging 2006, 27:663-672.
49. Miliszkiewicz N., Walas S., Tobiasz A. Current approaches to calibration of LA-ICP-MS analysis. J. Anal. At. Spectrom. 2015, 30:327-338.
50. Miyajima H., Takahashi Y., Kono S., Sugimoto M., Suzuki Y., Hishida A., Sakamoto M., Oucm Y. Glucose and oxygen hypometabolism in Aceruloplasminemia brains. Intern. Med. 2002, 41:186-190.
51. Olmos-Alonso A., Schetters S.T.T., Sri S., Askew K., Mancuso R., Vargas-Caballero M., Holscher C., Perry V.H., Gomez-Nicola D. Pharmacological targeting of CSF1R inhibits microglial proliferation and prevents the progression of Alzheimer's-like pathology. Brain 2016.
52. Ong W.-Y., Farooqui A.A. Iron, neuroinflammation, and Alzheimer's disease. J. Alzheimers Dis. 2005, 8:183-200.
53. O'Reilly J., Douglas D., Braybrook J., So P.W., Vergucht E., Garrevoet J., Vekemans B., Vincze L., Goenaga-Infante H. A novel calibration strategy for the quantitative imaging of iron in biological tissues by LA-ICP-MS using matrix-matched standards and internal standardisation. J. Anal. At. Spectrom. 2014, 29.
54. Peters D.G., Connor J.R., Meadowcroft M.D. The relationship between iron dyshomeostasis and amyloidogenesis in Alzheimer's disease: two sides of the same coin. Neurobiol. Dis. 2015, 81:49-65.
55. Ramos P., Santos A., Pinto N.R., Mendes R., Magalhães T., Almeida A. Iron levels in the human brain: a post-mortem study of anatomical region differences and age-related changes. J. Trace Elem. Med. Biol. 2014, 28:13-17.
56. Raven E.P., Lu P.H., Tishler T.A., Heydari P., Bartzokis G. Increased iron levels and decreased tissue integrity in hippocampus of Alzheimer's disease detected in vivo with magnetic resonance imaging. J. Alzheimers Dis. 2013, 37:127-136.
57. Rembach A., Hare D.J., Lind M., Fowler C.J., Cherny R.A., McLean C., Bush A.I., Masters C.L., Roberts B.R. Decreased copper in Alzheimer's disease brain is predominantly in the soluble extractable fraction. Int. J. Alzheimers Dis. 2013, 2013:1-7.
58. Riederer P., Sofic E., Rausch W.-D., Schmidt B., Reynolds G.P., Jellinger K., Youdim M.B.H. Transition metals, ferritin, glutathione, and ascorbic acid in parkinsonian brains. J. Neurochem. 1989, 52:515-520.
59. Roberts B.R., Ryan T.M., Bush A.I., Masters C.L., Duce J.A. The role of metallobiology and amyloid-β peptides in Alzheimer's disease. J. Neurochem. 2011, 120:149-166.
60. Rossi M., Ruottinen H., Soimakallio S., Elovaara I., Dastidar P. Clinical MRI for iron detection in Parkinson's disease. Clin. Imaging 2013, 37:631-636.
61. Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., Preibisch S., Rueden C., Saalfeld S., Schmid B., Tinevez J.-Y., White D.J., Hartenstein V., Eliceiri K., Tomancak P., Cardona A. Fiji: an open-source platform for biological-image analysis. Nat. Methods 2012, 9:676-682.
62. Schipper H.M. Brain iron deposition and the free radical-mitochondrial theory of ageing. Ageing Res. Rev. 2004, 3:265-301.
63. Schrag M., Dickson A., Jiffry A., Kirsch D., Vinters H.V., Kirsch W. The effect of formalin fixation on the levels of brain transition metals in archived samples. Biometals 2010, 23:1123-1127.
64. Schrag M., Mueller C., Oyoyo U., Smith M.A., Kirsch W.M. Iron, zinc and copper in the Alzheimer's disease brain: a quantitative meta-analysis. Some insight on the influence of citation bias on scientific opinion. Prog. Neurobiol. 2011, 94:296-306.
65. Snedecor G., Cochran W. Statistical Methods 1986, Iowa State University Press. eighth ed.
66. Stüber C., Morawski M., Schäfer A., Labadie C., Wähnert M., Leuze C., Streicher M., Barapatre N., Reimann K., Geyer S., Spemann D., Turner R. Myelin and iron concentration in the human brain: a quantitative study of MRI contrast. NeuroImage 2014, 93:95-106.
67. van Duijn S., Nabuurs R.J.A., van Duinen S.G., Natte R. Comparison of histological techniques to visualize iron in paraffin-embedded brain tissue of patients with Alzheimer's disease. J. Histochem. Cytochem. 2013, 61:785-792.
68. Ward R.R., Zucca F.A., Duyn J.H., Crichton R.R., Zecca L. The role of iron in brain ageing and neurodegenerative disorders. Lancet Neurol. 2014, 13:1045-1060.
69. Wong B.X., Tsatsanis A., Lim L.Q., Adlard P.A., Bush A.I., Duce J.A. β-amyloid precursor protein does not possess ferroxidase activity but does stabilize the cell surface ferrous iron exporter ferroportin. PLoS One 2014, 9:e114174.
70. Yeatman J.D., Wandell B.A., Mezer A.A. Lifespan maturation and degeneration of human brain white matter. Nat. Commun. 2014, 5:4932.
71. Zecca L., Pietra R., Goj C., Mecacci C., Radice D., Sabbioni E. Iron and other metals in neuromelanin, substantia nigra, and putamen of human brain. J. Neurochem. 1994, 62:1097-1101.
72. Zecca L., Stroppolo A., Gatti A., Tampellini D., Toscani M., Gallorini M., Giaveri G., Arosio P., Santambrogio P., Fariello R.G. The role of iron and copper molecules in the neuronal vulnerability of locus coeruleus and substantia nigra during aging. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:9843.
73. Zeineh M.M., Chen Y., Kitzler H.H., Hammond R., Vogel H., Rutt B.K. Activated iron-containing microglia in the human hippocampus identified by magnetic resonance imaging in Alzheimer disease. Neurobiol. Aging 2015, 36:2483-2500.
74. Zhu W.-z., Zhong W.-d., Wang W., Zhan C.-j., Wang C.-y., Qi J.-p., Wang J.-z., Lei T. Quantitative MR phase-corrected imaging to investigate increased brain iron deposition of patients with Alzheimer disease. Radiology 2009, 253:497-504.