Mass spectrometry imaging, an emerging technology in neuropsychopharmacology

Neuropsychopharmacology

Volumn 39, Issue 1, 2014, Pages 34-39

  Shariatgorji, Mohammadreza ^a   Svenningsson, Per ^b   Andrén, Per E ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

lipid; mass spectrometry imaging; neuropeptide; neurotransmitter; protein

Indexed keywords

8 CHLORO 2,3,4,5 TETRAHYDRO 3 METHYL 5 PHENYL 1H 3 BENZAZEPIN 7 OL HYDROGEN MALEATE; ADENOSINE PHOSPHATE; CLOZAPINE; ION; LIPID; NEUROPEPTIDE; NEUROTRANSMITTER; PEPTIDES AND PROTEINS; RACLOPRIDE;

ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; CEREBROVASCULAR ACCIDENT; EPILEPSY; HUMAN; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MENTAL DISEASE; MOLECULAR IMAGING; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PSYCHOPHARMACOLOGY; REVIEW; TANDEM MASS SPECTROMETRY; FUNCTIONAL NEUROIMAGING; MULTIMODAL IMAGING; NEUROPHARMACOLOGY; PROCEDURES;

FUNCTIONAL NEUROIMAGING; HUMANS; MASS SPECTROMETRY; MOLECULAR IMAGING; MULTIMODAL IMAGING; NEUROPHARMACOLOGY; PSYCHOPHARMACOLOGY;

EID: 84890523368     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2013.215     Document Type: Review

References (148)

1. Ageta H, Asai S, Sugiura Y, Goto-Inoue N, Zaima N, Setou M (2009). Layer-specific sulfatide localization in rat hippocampus middle molecular layer is revealed by nanoparticle-Assisted laser desorption/ionization imaging mass spectrometry. Med Mol Morphol 42: 16-23
2. Angel PM, Spraggins JM, Baldwin HS, Caprioli R (2012). Enhanced sensitivity for high spatial resolution lipid analysis by negative ion mode matrix assisted laser desorption ionization imaging mass spectrometry. Anal Chem 84: 1557-1564
3. Astigarraga E, Barreda-Gomez G, Lombardero L, Fresnedo O, Castano F, Giralt MT et al. (2008). Profiling and imaging of lipids on brain and liver tissue by matrixassisted laser desorption/ionization mass spectrometry using 2-mercaptobenzothiazole as a matrix. Anal Chem 80: 9105-9114
4. Barrett PJ, Song Y, Van Horn WD, Hustedt EJ, Schafer JM, Hadziselimovic A et al. (2012). The amyloid precursor protein has a flexible transmembrane domain and binds cholesterol. Science 336: 1168-1171
5. Bayes A, Grant SG (2009). Neuroproteomics: Understanding the molecular organization and complexity of the brain. Nat Rev Neurosci 10: 635-646
6. Becker JS, Dobrowolska J, Zoriy M, Matusch A (2008). Imaging of uranium on rat brain sections using laser ablation inductively coupled plasma mass spectrometry: A new tool for the study of critical substructures affined to heavy metals in tissues. Rapid Commun Mass Spectrom 22: 2768-2772
7. Becker JS, Zoriy M, Becker JS, Dobrowolska J, Dehnhardt M, Matusch A (2007). Elemental imaging mass spectrometry of thin sections of tissues and analysis of brain proteins in gels by laser ablation inductively coupled plasma mass spectrometry. Phys Status Solidi C 4: 1775-1784
8. Becker JS, Zoriy MV, Pickhardt C, Palomero-Gallagher N, Zilles K (2005). Imaging of copper, zinc, and other elements in thin section of human brain samples (Hippocampus) by laser ablation inductively coupled plasma mass spectrometry. Anal Chem 77: 3208-3216
9. Benabdellah F, Seyer A, Quinton L, Touboul D, Brunelle A, Laprevote O (2010). Mass spectrometry imaging of rat brain sections: Nanomolar sensitivity with MALDI versus nanometer resolution by TOF-SIMS. Anal Bioanal Chem 396: 151-162
10. Benabdellah F, Touboul D, Brunelle A, Laprevote O (2009). In situ primary metabolites localization on a rat brain section by chemical mass spectrometry imaging. Anal Chem 81: 5557-5560
11. Bezard E, Brotchie JM, Gross CE (2001). Pathophysiology of levodopa-induced dyskinesia: Potential for new therapies. Nat Rev Neurosci 2: 577-588
12. Bonnel D, Longuespee R, Franck J, Roudbaraki M, Gosset P, Day R et al. (2011). Multivariate analyses for biomarkers hunting and validation through on-Tissue bottom-up or in-source decay in MALDI-MSI: Application to prostate cancer. Anal Bioanal Chem 401: 149-165
13. Borner K, Nygren H, Hagenhoff B, Malmberg P, Tallarek E, Mansson JE (2006). Distribution of cholesterol and galactosylceramide in rat cerebellar white matter. Biochim Biophys Acta 1761: 335-344
14. Burnum KE, Frappier SL, Caprioli RM (2008). Matrix-Assisted laser desorption/ ionization imaging mass spectrometry for the investigation of proteins and peptides. Annu Rev Anal Chem 1: 689-705
15. Calligaris D, Longuespee R, Debois D, Asakawa D, Turtoi A, Castronovo V et al. (2013). Selected protein monitoring in histological sections by targeted MALDIFTICR in-source decay imaging. Anal Chem 85: 2117-2126
16. Candy JM, Oakley AE, Mountfort SA, Taylor GA, Morris CM, Bishop HE et al. (1992). The imaging and quantification of aluminum in the human brain using dynamic secondary ion mass-spectrometry (SIMS). Biol Cell 74: 109-118
17. Caprioli RM, Farmer TB, Gile J (1997). Molecular imaging of biological samples: Localization of peptides and proteins using MALDI-TOF MS. Anal Chem 69: 4751-4760
18. Carter CL, McLeod CW, Bunch J (2011). Imaging of phospholipids in formalin fixed rat brain sections by matrix assisted laser desorption/ionization mass spectrometry. J Am Soc Mass Spectrom 22: 1991-1998
19. Castaing R, Slodzian G (1962). Microanalyse par é mission ionique secondaire. J Microsc 1: 395-410
20. Cerruti CD, Benabdellah F, Laprevote O, Touboul D, Brunelle A (2012). MALDI imaging and structural analysis of rat brain lipid negative ions with 9-Aminoacridine matrix. Anal Chem 84: 2164-2171
21. Cerruti CD, Touboul D, Guerineau V, Petit VW, Laprevote O, Brunelle A (2011). MALDI imaging mass spectrometry of lipids by adding lithium salts to the matrix solution. Anal Bioanal Chem 401: 75-87
22. Chacon A, Zagol-Ikapitte I, Amarnath V, Reyzer ML, Oates JA, Caprioli RM et al. (2011). On-Tissue chemical derivatization of 3-methoxysalicylamine for MALDIimaging mass spectrometry. J Mass Spectrom 46: 840-846
23. Chan K, Lanthier P, Liu X, Sandhu JK, Stanimirovic D, Li JJ (2009). MALDI mass spectrometry imaging of gangliosides in mouse brain using ionic liquid matrix. Anal Chim Acta 639: 57-61
24. Chaurand P, Schwartz SA, Caprioli RM (2002). Imaging mass spectrometry: A new tool to investigate the spatial organization of peptides and proteins in mammalian tissue sections. Curr Opin Chem Biol 6: 676-681
25. Chen YF, Allegood J, Liu Y, Wang E, Cachon-Gonzalez B, Cox TM et al. (2008). Imaging MALDI mass spectrometry using an oscillating capillary nebulizer matrix coating system and its application to analysis of lipids in brain from a mouse model of Tay-Sachs/Sandhoff disease. Anal Chem 80: 2780-2788
26. Chochina SV, Avdulov NA, Igbavboa U, Cleary JP, O'Hare EO, Wood WG (2001). Amyloid beta-peptide1-40 increases neuronal membrane fluidity: Role of cholesterol and brain region. J Lipid Res 42: 1292-1297
27. Cohen LH, Gusev AI (2002). Small molecule analysis by MALDI mass spectrometry. Anal Bioanal Chem 373: 571-586
28. Colsch B, Woods AS (2010). Localization and imaging of sialylated glycosphingolipids in brain tissue sections by MALDI mass spectrometry. Glycobiology 20: 661-667
29. Cossec JC, Marquer C, Panchal M, Lazar AN, Duyckaerts C, Potier MC (2010). Cholesterol changes in Alzheimer's disease: Methods of analysis and impact on the formation of enlarged endosomes. Biochim Biophys Acta 1801: 839-845
30. Debois D, Bertrand V, Quinton L, De Pauw-Gillet MC, De Pauw E (2010). MALDI-in source decay applied to mass spectrometry imaging: A new tool for protein identification. Anal Chem 82: 4036-4045
31. Debois D, Brunelle A, Laprevote O (2007). Attempts for molecular depth profiling directly on a rat brain tissue section using fullerene and bismuth cluster ion beams. Int J Mass Spectrom 260: 115-120
32. Delvolve AM, Woods AS (2011). Optimization of automated matrix deposition for biomolecular mapping using a spotter. J Mass Spectrom 46: 1046-1050
33. Dill AL, Eberlin LS, Costa AB, Ifa DR, Cooks RG (2011). Data quality in tissue analysis using desorption electrospray ionization. Anal Bioanal Chem 401: 1949-1961
34. Dobrowolska J, Dehnhardt M, Matusch A, Zoriy M, Palomero-Gallagher N, Koscielniak P et al. (2008). Quantitative imaging of zinc, copper and lead in three distinct regions of the human brain by laser ablation inductively coupled plasma mass spectrometry. Talanta 74: 717-723
35. Double KL, Gerlach M, Schunemann V, Trautwein AX, Zecca L, Gallorini M et al. (2003). Iron-binding characteristics of neuromelanin of the human substantia nigra. Biochem Pharmacol 66: 489-494
36. Eberlin LS, Dill AL, Golby AJ, Ligon KL, Wiseman JM, Cooks RG et al. (2010a). Discrimination of human astrocytoma subtypes by lipid analysis using desorption electrospray ionization imaging mass spectrometry. Angew Chem Int Ed Engl 49: 5953-5956
37. Eberlin LS, Ifa DR, Wu C, Cooks RG (2010b). Three-dimensional vizualization of mouse brain by lipid analysis using ambient ionization mass spectrometry. Angew Chem Int Ed Engl 49: 873-876
38. Ferguson CN, Benchaar SA, Miao Z, Loo JA, Chen H (2011). Direct ionization of large proteins and protein complexes by desorption electrospray ionization-mass spectrometry. Anal Chem 83: 6468-6473
39. Franck J, Arafah K, Barnes A, Wisztorski M, Salzet M, Fournier I (2009). Improving tissue preparation for matrix-Assisted laser desorption ionization mass spectrometry imaging. Part 1: Using microspotting. Anal Chem 81: 8193-8202
40. Goodwin RJ, Dungworth JC, Cobb SR, Pitt AR (2008). Time-dependent evolution of tissue markers by MALDI-MS imaging. Proteomics 8: 3801-3808
41. Goodwin RJ, Iverson SL, Andren PE (2012). The significance of ambienttemperature on pharmaceutical and endogenous compound abundance and distribution in tissues sections when analyzed by matrix-Assisted laser desorption/ionization mass spectrometry imaging. Rapid Commun Mass Spectrom 26: 494-498
42. Goodwin RJ, Lang AM, Allingham H, Boren M, Pitt AR (2010). Stopping the clock on proteomic degradation by heat treatment at the point of tissue excision. Proteomics 10: 1751-1761
43. Goodwin RJ, Mackay CL, Nilsson A, Harrison DJ, Farde L, Andren PE et al. (2011). Qualitative and quantitative MALDI imaging of the positron emission tomography ligands raclopride (a D2 dopamine antagonist) and SCH 23390 (a D1 dopamine antagonist) in rat brain tissue sections using a solvent-free dry matrix application method. Anal Chem 83: 9694-9701
44. Goto-Inoue N, Hayasaka T, Zaima N, Kashiwagi Y, Yamamoto M, Nakamoto M et al. (2010). The detection of glycosphingolipids in brain tissue sections by imaging mass spectrometry using gold nanoparticles. J Am Soc Mass Spectrom 21: 1940-1943
45. Groseclose MR, Andersson M, Hardesty WM, Caprioli RM (2007). Identification of proteins directly from tissue: In situ tryptic digestions coupled with imaging mass spectrometry. J Mass Spectrom 42: 254-262
46. Han XL, Holtzman DM, McKeel DW, Kelley J, Morris JC (2002). Substantial sulfatide deficiency and ceramide elevation in very early Alzheimer's disease: Potential role in disease pathogenesis. J Neurochem 82: 809-818
47. Hankin JA, Barkley RM, Murphy RC (2007). Sublimation as a method of matrix application for mass spectrometric imaging. J Am Soc Mass Spectrom 18: 1646-1652
48. Hankin JA, Farias SE, Barkley R, Heidenreich K, Frey LC, Hamazaki K et al. (2011). MALDI mass spectrometric imaging of lipids in rat brain injury models. J Am Soc Mass Spectrom 22: 1014-1021
49. Hanrieder J, Ekegren T, Andersson M, Bergquist J (2013). MALDI imaging of postmortem human spinal cord in amyotrophic lateral sclerosis. J Neurochem 124: 695-707
50. Hanrieder J, Ljungdahl A, Falth M, Mammo SE, Bergquist J, Andersson M (2011). L-DOPA-induced dyskinesia is associated with regional increase of striatal dynorphin peptides as elucidated by imaging mass spectrometry. Mol Cell Proteomics 10: M111.009308
51. Hardiman O, van den Berg LH, Kiernan MC (2011). Clinical diagnosis and management of amyotrophic lateral sclerosis. Nat Rev Neurol 7: 639-649
52. Hardy J, Allsop D (1991). Amyloid deposition as the central event in the aetiology of Alzheimer's disease. Trends Pharmacol Sci 12: 383-388
53. Hardy J, Selkoe DJ (2002). The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics. Science 297: 353-356
54. Hare D, Reedy B, Grimm R, Wilkins S, Volitakis I, George JL et al. (2009). Quantitative elemental bio-imaging of Mn, Fe, Cu and Zn in 6-hydroxydopamine induced Parkinsonism mouse models. Metallomics 1: 53-58
55. Hattori K, Kajimura M, Hishiki T, Nakanishi T, Kubo A, Nagahata Y et al. (2010). Paradoxical ATP elevation in ischemic penumbra revealed by quantitative imaging mass spectrometry. Antioxid Redox Signal 13: 1157-1167
56. Hirsch-Reinshagen V, Burgess BL, Wellington CL (2009). Why lipids are important for Alzheimer disease? Mol Cell Biochem 326: 121-129
57. Hsieh Y, Casale R, Fukuda E, Chen J, Knemeyer I, Wingate J et al. (2006). Matrixassisted laser desorption/ionization imaging mass spectrometry for direct measurement of clozapine in rat brain tissue. Rapid Commun Mass Spectrom 20: 965-972
58. Ifa DR, Wiseman JM, Song QY, Cooks RG (2007). Development of capabilities for imaging mass spectrometry under ambient conditions with desorption electrospray ionization (DESI). Int J Mass Spectrom 259: 8-15
59. Jehl B, Bauer R, Dorge A, Rick R (1981). The use of propane/isopentane mixtures for rapid freezing of biological specimens. J Microsc 123: 307-309
60. Kallback P, Shariatgorji M, Nilsson A, Andren PE (2012). Novel mass spectrometry imaging software assisting labeled normalization and quantitation of drugs and neuropeptides directly in tissue sections. J Proteomics 75: 4941-4951
61. Kim JH, Kim JH, Ahn BJ, Park JH, Shon HK, Yu YS et al. (2008). Label-free calcium imaging in ischemic retinal tissue by TOF-SIMS. Biophys J 94: 4095-4102
62. Koizumi S, Yamamoto S, Hayasaka T, Konishi Y, Yamaguchi-Okada M, Goto-Inoue N et al. (2010). Imaging mass spectrometry revealed the production of lysophosphatidylcholine in the injured ischemic rat brain. Neuroscience 168: 219-225
63. Komatsu M, Murayama Y, Hashimoto H (2008). Protein fragment imaging using ink jet printing digestion technique. Appl Surf Sci 255: 1162-1164
64. Laskin J, Heath BS, Roach PJ, Cazares L, Semmes OJ (2012). Tissue imaging using nanospray desorption electrospray ionization mass spectrometry. Anal Chem 84: 141-148
65. Lazar AN, Bich C, Panchal M, Desbenoit N, Petit VW, Touboul D et al. (2013). Time-of-flight secondary ion mass spectrometry (TOF-SIMS) imaging reveals cholesterol overload in the cerebral cortex of Alzheimer disease patients. Acta Neuropathol 125: 133-144
66. Lees AJ, Hardy J, Revesz T (2009). Parkinson's disease. Lancet 373: 2055-2066
67. Lemaire R, Wisztorski M, Desmons A, Tabet JC, Day R, Salzet M et al. (2006). MALDI-MS direct tissue analysis of proteins: Improving signal sensitivity using organic treatments. Anal Chem 78: 7145-7153
68. Liebl H (1967). Ion microprobe mass analyzer. J Appl Phys 38: 5277-5283
69. Ljungdahl A, Hanrieder J, Falth M, Bergquist J, Andersson M (2011). Imaging mass spectrometry reveals elevated nigral levels of dynorphin neuropeptides in L-DOPA-induced dyskinesia in rat model of Parkinson's disease. PLoS ONE 6: E25653
70. MacAleese L, Stauber J, Heeren RM (2009). Perspectives for imaging mass spectrometry in the proteomics landscape. Proteomics 9: 819-834
71. Manicke NE, Wiseman JM, Ifa DR, Cooks RG (2008). Desorption electrospray ionization (DESI) mass Spectrometry and tandem mass spectrometry (MS/MS) of phospholipids and sphingolipids: Ionization, adduct formation, and fragmentation. J Am Soc Mass Spectrom 19: 531-543
72. Matsumoto J, Sugiura Y, Yuki D, Hayasaka T, Goto-Inoue N, Zaima N et al. (2011). Abnormal phospholipids distribution in the prefrontal cortex from a patient with schizophrenia revealed by matrix-Assisted laser desorption/ionization imaging mass spectrometry. Anal Bioanal Chem 400: 1933-1943
73. Matusch A, Depboylu C, Palm C, Wu B, Hoglinger GU, Schafer MKH et al. (2010). Cerebral bioimaging of Cu, Fe, Zn, and Mn in the MPTP mouse model of Parkinson's disease using laser ablation inductively coupled plasma mass spectrometry (LA-ICP-MS). J Am Soc Mass Spectrom 21: 161-171
74. McLean JA, Ridenour WB, Caprioli RM (2007). Profiling and imaging of tissues by imaging ion mobility-mass spectrometry. J Mass Spectrom 42: 1099-1105
75. Meriaux C, Franck J, Wisztorski M, Salzet M, Fournier I (2010). Liquid ionic matrixes for MALDI mass spectrometry imaging of lipids. J Proteomics 73: 1204-1218
76. Monnot AD, Behl M, Ho SN, Zheng W (2011). Regulation of brain copper homeostasis by the brain barrier systems: Effects of Fe-overload and Fedeficiency. Toxicol Appl Pharm 256: 249-257
77. Nilsson A, Fehniger TE, Gustavsson L, Andersson M, Kenne K, Marko-Varga G et al. (2010). Fine mapping the spatial distribution and concentration of unlabeled drugs within tissue micro-compartments using imaging mass spectrometry. PloS One 5: E11411
78. Nilsson A, Skold K, Sjogren B, Svensson M, Pierson J, Zhang X et al. (2007). Increased striatal mRNA and protein levels of the immunophilin FKBP-12 in experimental Parkinson's disease and identification of FKBP-12-binding proteins. J Proteome Res 6: 3952-3961
79. Norris JL, Caprioli RM (2013). Analysis of tissue specimens by matrix-Assisted laser desorption/ionization imaging mass spectrometry in biological and clinical research. Chem Rev 113: 2309-2342
80. Nygren H, Borner K, Hagenhoff B, Malmberg P, Mansson JE (2005). Localization of cholesterol, phosphocholine and galactosylceramide in rat cerebellar cortex with imaging TOF-SIMS equipped with a bismuth cluster ion source. Biochim Biophys Acta 1737: 102-110
81. Nygren H, Malmberg P (2010). High-resolution imaging and proteomics of peptide fragments by TOF-SIMS. Proteomics 10: 1694-1698
82. Pan N, Liu PY, Cui WD, Tang B, Shi JM, Chen H (2013). Highly efficient ionization of phosphopeptides at low pH by desorption electrospray ionization mass spectrometry. Analyst 138: 1321-1324
83. Passarelli MK, Winograd N (2011). Characterizing in situ Glycerophospholipids with SIMS and MALDI Methodologies. Surf Interface Anal 43: 269-271
84. Pernber Z, Richter K, Mansson JE, Nygren H (2007). Sulfatide with different fatty acids has unique distributions in cerebellum as imaged by time-of-flight secondary ion mass spectrometry (TOF-SIMS). Biochim Biophys Acta 1771: 202-209
85. Perrin RJ, Fagan AM, Holtzman DM (2009). Multimodal techniques for diagnosis and prognosis of Alzheimer's disease. Nature 461: 916-922
86. Pierson J, Norris JL, Aerni HR, Svenningsson P, Caprioli RM, Andren PE (2004). Molecular profiling of experimental Parkinson's disease: Direct analysis of peptides and proteins on brain tissue sections by MALDI mass spectrometry. J Proteome Res 3: 289-295
87. Pierson J, Svenningsson P, Caprioli RM, Andren PE (2005). Increased levels of ubiquitin in the 6-OHDA-lesioned striatum of rats. J Proteome Res 4: 223-226
88. Pirman DA, Reich RF, Kiss A, Heeren RMA, Yost RA (2013). Quantitative MALDI tandem mass spectrometric imaging of cocaine from brain tissue with a deuterated internal standard. Anal Chem 85: 1081-1089
89. Pol J, Vidova V, Kruppa G, Kobliha V, Novak P, Lemr K et al. (2009). Automated ambient desorption-ionization platform for surface imaging integrated with a commercial fourier transform ion cyclotron resonance mass spectrometer. Anal Chem 81: 8479-8487
90. Przybylski C, Gonnet F, Hersant Y, Bonnaffe D, Lortat-Jacob H, Daniel R (2010). Desorption electrospray ionization mass spectrometry of glycosaminoglycans and their protein noncovalent complex. Anal Chem 82: 9225-9233
91. Puglielli L, Tanzi RE, Kovacs DM (2003). Alzheimer's disease: The cholesterol connection. Nat Neurosci 6: 345-351
92. Puolitaival SM, Burnum KE, Cornett DS, Caprioli RM (2008). Solvent-free matrix dry-coating for MALDI Imaging of phospholipids. J Am Soc Mass Spectrom 19: 882-886
93. Qin ZY, Caruso JA, Lai B, Matusch A, Becker JS (2011). Trace metal imaging with high spatial resolution: Applications in biomedicine. Metallomics 3: 28-37
94. Rasia RM, Bertoncini CW, Marsh D, Hoyer W, Cherny D, Zweckstetter M et al. (2005). Structural characterization of copper(II) binding to alpha-synuclein: Insights into the bioinorganic chemistry of Parkinson's disease. Proc Natl Acad Sci USA 102: 4294-4299
95. Rohner TC, Staab D, Stoeckli M (2005). MALDI mass spectrometric imaging of biological tissue sections. Mech Ageing Dev 126: 177-185
96. Schober Y, Schramm T, Spengler B, Rompp A (2011). Protein identification by accurate mass matrix-Assisted laser desorption/ionization imaging of tryptic peptides. Rapid Commun Mass Spectrom 25: 2475-2483
97. Seeley EH, Oppenheimer SR, Mi D, Chaurand P, Caprioli RM (2008). Enhancement of protein sensitivity for MALDI imaging mass spectrometry after chemical treatment of tissue sections. J Am Soc Mass Spectrom 19: 1069-1077
98. Sensi SL, Paoletti P, Koh JY, Aizenman E, Bush AI, Hershfinkel M (2011). The Neurophysiology and pathology of Brain Zinc. J Neurosci 31: 16076-16085
99. Shanta SR, Zhou LH, Park YS, Kim YH, Kim Y, Kim KP (2011). Binary matrix for MALDI imaging mass spectrometry of phospholipids in both ion modes. Anal Chem 83: 1252-1259
100. Shariatgorji M, Amini N, Ilag LL (2009). Silicon nitride nanoparticles for surfaceassisted laser desorption/ionization of small molecules. J Nanopart Res 11: 1509-1512
101. Shariatgorji M, Kallback P, Gustavsson L, Schintu N, Svenningsson P, Goodwin RJA et al. (2012a). Controlled-pH tissue cleanup protocol for signal enhancement of small molecule drugs analyzed by MALDI-MS imaging. Anal Chem 84: 4603-4607
102. Shariatgorji M, Nilsson A, Goodwin RJA, Svenningsson P, Schintu N, Banka Z et al. (2012b). Deuterated matrix-Assisted laser desorption ionization matrix uncovers masked mass spectrometry imaging signals of small molecules. Anal Chem 84: 7152-7157
103. Shiea J, Yuan CH, Huang MZ, Cheng SC, Ma YL, Tseng WL et al. (2008). Detection of native protein ions in aqueous solution under ambient conditions by electrospray laser desorption/ionization mass spectrometry. Anal Chem 80: 4845-4852
104. Shimma S, Sugiura Y, Hayasaka T, Zaima N, Matsumoto M, Setou M (2008). Mass imaging and identification of biomolecules with MALDI-QIT-TOF-based system. Anal Chem 80: 878-885
105. Shrivas K, Hayasaka T, Goto-Inoue N, Sugiura Y, Zaima N, Setou M (2010). Ionic matrix for enhanced MALDI imaging mass spectrometry for identification of phospholipids in mouse liver and cerebellum tissue sections. Anal Chem 82: 8800-8806
106. Shrivas K, Hayasaka T, Sugiura Y, Setou M (2011). Method for simultaneous imaging of endogenous low molecular weight metabolites in mouse brain using TiO2 nanoparticles in nanoparticle-Assisted laser desorption/ionization-imaging mass spectrometry. Anal Chem 83: 7283-7289
107. Sjovall P, Johansson B, Lausmaa J (2006). Localization of lipids in freeze-dried mouse brain sections by imaging TOF-SIMS. Appl Surf Sci 252: 6966-6974
108. Sjovall P, Lausmaa J, Johansson B (2004). Mass spectrometric imaging of lipids in brain tissue. Anal Chem 76: 4271-4278
109. Sjovall P, Lausmaa J, Nygren H, Carlsson L, Malmberg P (2003). Imaging of membrane lipids in single cells by imprint-imaging time-of-flight secondary ion mass spectrometry. Anal Chem 75: 3429-3434
110. Skold K, Svensson M, Nilsson A, Zhang XQ, Nydahl K, Caprioli RM et al. (2006). Decreased striatal levels of PEP-19 following MPTP lesion in the mouse. J Proteome Res 5: 262-269
111. Skold K, Svensson M, Norrman M, Sjogren B, Svenningsson P, Andren PE (2007). The significance of biochemical and molecular sample integrity in brain proteomics and peptidomics: Stathmin 2-20 and peptides as sample quality indicators. Proteomics 7: 4445-4456
112. Sloot WN, Gramsbergen JB (1994). Axonal transport of manganese and its relevance to selective n eurotoxicity in the rat basal ganglia. Brain Res 657: 124-132
113. Sole-Domenech S, Sjovall P, Vukojevic V, Fernando R, Codita A, Salve S et al. (2013). Localization of cholesterol, amyloid and glia in Alzheimer's disease transgenic mouse brain tissue using time-of-flight secondary ion mass spectrometry (ToF-SIMS) and immunofluorescence imaging. Acta Neuropathol 125: 145-157
114. Stauber J, MacAleese L, Franck J, Claude E, Snel M, Kaletas BK et al. (2010). Ontissue protein identification and imaging by MALDI-ion mobility mass spectrometry. J Am Soc Mass Spectrom 21: 338-347
115. Stoeckli M, Chaurand P, Hallahan DE, Caprioli RM (2001). Imaging mass spectrometry: A new technology for the analysis of protein expression in mammalian tissues. Nat Med 7: 493-496
116. Stoeckli M, Knochenmuss R, McCombie G, Mueller D, Rohner T, Staab D et al. (2006). MALDI MS imaging of amyloid. Methods Enzymol 412: 94-106
117. Stoeckli M, Staab D, Staufenbiel M, Wiederhold KH, Signor L (2002). Molecular imaging of amyloid beta peptides in mouse brain sections using mass spectrometry. Anal Biochem 311: 33-39
118. Sugiura Y, Konishi Y, Zaima N, Kajihara S, Nakanishi H, Taguchi R et al. (2009a). Visualization of the cell-selective distribution of PUFA-containing phosphatidylcholines in mouse brain by imaging mass spectrometry. J Lipid Res 50: 1776-1788
119. Sugiura Y, Setou M (2009b). Selective imaging of positively charged polar and nonpolar lipids by optimizing matrix solution composition. Rapid Commun Mass Spectrom 23: 3269-3278
120. Sugiura Y, Taguchi R, Setou M (2011). Visualization of spatiotemporal energy dynamics of hippocampal neurons by mass spectrometry during a kainateinduced seizure. PLoS ONE 6: E17952
121. Sugiura Y, Zaima N, Setou M, Ito S, Yao I (2012). Visualization of acetylcholine distribution in central nervous system tissue sections by tandem imaging mass spectrometry. Anal Bioanal Chem 403: 1851-1861
122. Svensson M, Boren M, Skold K, Falth M, Sjogren B, Andersson M et al. (2009). Heat stabilization of the tissue proteome: A new technology for improved proteomics. J Proteome Res 8: 974-981
123. Svensson M, Skold K, Nilsson A, Falth M, Nydahl K, Svenningsson P et al. (2007). Neuropeptidomics: MS applied to the discovery of novel peptides from the brain. Anal Chem 79: 15-16, 18-21
124. Svensson M, Skold K, Svenningsson P, Andren PE (2003). Peptidomics-based discovery of novel neuropeptides. J Proteome Res 2: 213-219
125. Takats Z, Wiseman JM, Gologan B, Cooks RG (2004). Mass spectrometry sampling under ambient conditions with desorption electrospray ionization. Science 306: 471-473
126. Thomas A, Charbonneau JL, Fournaise E, Chaurand P (2012). Sublimation of new matrix candidates for high spatial resolution imaging mass spectrometry of lipids: Enhanced information in both positive and negative polarities after 1,5-diaminonapthalene deposition. Anal Chem 84: 2048-2054
127. Touboul D, Halgand F, Brunelle A, Kersting R, Tallarek E, Hagenhoff B et al. (2004). Tissue molecular ion imaging by gold cluster ion bombardment. Anal Chem 76: 1550-1559
128. Trim PJ, Atkinson SJ, Princivalle AP, Marshall PS, West A, Clench MR (2008). Matrix-Assisted laser desorption/ionisation mass spectrometry imaging of lipids in rat brain tissue with integrated unsupervised and supervised multivariant statistical analysis. Rapid Commun Mass Spectrom 22: 1503-1509
129. Trim PJ, Djidja MC, Atkinson SJ, Oakes K, Cole LM, Anderson DM et al. (2010). Introduction of a 20 kHz Nd:YVO4 laser into a hybrid quadrupole timeof-flight mass spectrometer for MALDI-MS imaging. Anal Bioanal Chem 397: 3409-3419
130. Trimpin S, Herath TN, Inutan ED, Wager-Miller J, Kowalski P, Claude E et al. (2010). Automated solvent-free matrix deposition for tissue imaging by mass spectrometry. Anal Chem 82: 359-367
131. Uys JD, Grey AC, Wiggins A, Schwacke JH, Schey KL, Kalivas PW (2010). Matrix-Assisted laser desorption/ionization tissue profiling of secretoneurin in the nucleus accumbens shell from cocaine-sensitized rats. J Mass Spectrom 45: 97-103
132. Wang HYJ, Liu CB, Wu HW, Kuo S (2010). Direct profiling of phospholipids and lysophospholipids in rat brain sections after ischemic stroke. Rapid Commun Mass Spectrom 24: 2057-2064
133. Wang HYJ, SNJJ Post, Woods AS (2008). A minimalist approach to MALDI imaging of glycerophospholipids and sphingolipids in rat brain sections. Int J Mass Spectrom 278: 143-149
134. Wei J, Buriak JM, Siuzdak G (1999). Desorption-ionization mass spectrometry on porous silicon. Nature 399: 243-246
135. Wenk GL (2003). Neuropathologic changes in Alzheimer's disease. J Clin Psychiatry 64(Suppl 9): 7-10
136. Whitehead SN, Chan KH, Gangaraju S, Slinn J, Li J, Hou ST (2011). Imaging mass spectrometry detection of gangliosides species in the mouse brain following transient focal cerebral ischemia and long-Term recovery. PLoS ONE 6: E20808
137. Wiseman JM, Ifa DR, Song QY, Cooks RG (2006). Tissue imaging at atmospheric pressure using desorption electrospray ionization (DESI) mass spectrometry. Angew Chem Int Ed Engl 45: 7188-7192
138. Wiseman JM, Ifa DR, Zhu Y, Kissinger CB, Manicke NE, Kissinger PT et al. (2008). Desorption electrospray ionization mass spectrometry: Imaging drugs and metabolites in tissues. Proc Natl Acad Sci USA 105: 18120-18125
139. Wu CP, Ifa DR, Manicke NE, Cooks RG (2009). Rapid, direct analysis of cholesterol by charge labeling in reactive desorption electrospray ionization. Anal Chem 81: 7618-7624
140. Wu CP, Ifa DR, Manicke NE, Cooks RG (2010). Molecular imaging of adrenal gland by desorption electrospray ionization mass spectrometry. Analyst 135: 28-32
141. Yang HJ, Ishizaki I, Sanada N, Zaima N, Sugiura Y, Yao I et al. (2010a). Detection of characteristic distributions of phospholipid head groups and fatty acids on neurite surface by time-of-flight secondary ion mass spectrometry. Med Mol Morphol 43: 158-164
142. Yang HJ, Sugiura Y, Ishizaki I, Sanada N, Ikegami K, Zaima N et al. (2010b). Imaging of lipids in cultured mammalian neurons by matrix assisted laser/ desorption ionization and secondary ion mass spectrometry. Surf Interface Anal 42: 1606-1611
143. Yang J, Caprioli RM (2013). Matrix precoated targets for direct lipid analysis and imaging of tissue. Anal Chem 85: 2907-2912
144. Yuki D, Sugiura Y, Zaima N, Akatsu H, Hashizume Y, Yamamoto T et al. (2011). Hydroxylated and non-hydroxylated sulfatide are distinctly distributed in the human cerebral cortex. Neuroscience 193: 44-53
145. Zecca L, Youdim MBH, Riederer P, Connor JR, Crichton RR (2004). Iron, brain ageing and neurodegenerative disorders. Nat Rev Neurosci 5: 863-873
146. Zoriy MV, Becker JS (2007). Imaging of elements in thin cross sections of human brain samples by LA-ICP-MS: A study on reproducibility. Int J Mass Spectrom 264: 175-180
147. Zoriy MV, Dehnhardt M, Matusch A, Becker JS (2008). Comparative imaging of P, S, Fe, Cu, Zn and C in thin sections of rat brain tumor as well as control tissues by laser ablation inductively coupled plasma mass spectrometry. Spectrochim Acta B 63: 375-382
148. Zoriy MV, Dehnhardt M, Reifenberger G, Zilles K, Becker JS (2006). Imaging of Cu, Zn, Pb and U in human brain tumor resections by laser ablation inductively coupled plasma mass spectrometry. Int J Mass Spectrom 257: 27-33