Imaging lipids with secondary ion mass spectrometry

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1841, Issue 8, 2014, Pages 1108-1119

  Kraft, Mary L ^a   Klitzing, Haley A ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Cell membrane; Lipid distribution; Model membrane; NanoSIMS; Sample preparation; TOF SIMS

Indexed keywords

LIPID;

ARTIFICIAL MEMBRANE; BIOCHEMISTRY; IMAGING; LIPID ANALYSIS; LIPID MEMBRANE; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; REVIEW; TIME OF FLIGHT MASS SPECTROMETRY;

CELL MEMBRANE; LIPID DISTRIBUTION; MODEL MEMBRANE; NANOSIMS; SAMPLE PREPARATION; TOF-SIMS;

LIPIDS; MAGNETICS; NANOTECHNOLOGY; SPECTROMETRY, MASS, SECONDARY ION;

EID: 84903270360     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2014.03.003     Document Type: Review

References (149)

1. T.-S. Park, W. Rosebury, E.K. Kindt, M.C. Kowala, and R.L. Panek Serine palmitoyltransferase inhibitor myriocin induces the regression of atherosclerotic plaques in hyperlipidemic ApoE-deficient mice Pharmacol. Res. 58 2008 45 51
2. J. Bismuth, P. Lin, Q. Yao, and C. Chen Ceramide: a common pathway for atherosclerosis? Atherosclerosis 196 2008 497 504
3. Y.H. Zeidan, R.W. Jenkins, and Y.A. Hannun Remodeling of cellular cytoskeleton by the acid sphingomyelinase/ceramide pathway J. Cell Biol. 181 2008 335 350 (Pubitemid 351574557)
4. J.W. Reagan Jr., M.L. Hubbert, and G.S. Shelness Posttranslational regulation of acid sphingomyelinase in Niemann-Pick type C1 fibroblasts and free cholesterol-enriched Chinese hamster ovary cells J. Biol. Chem. 275 2000 38104 38110 (Pubitemid 32004935)
5. T. Kolter, and K. Sandhoff Sphingolipid metabolism diseases Biochim. Biophys. Acta Biomembr. 1758 2006 2057 2079 (Pubitemid 44879358)
6. T. Kolter A view on sphingolipids and disease Chem. Phys. Lipids 164 2011 590 606
7. E. Hajduch, A. Balendran, I.H. Batty, G.J. Litherland, A.S. Blair, C.P. Downes, and H.S. Hundal Ceramide impairs the insulin-dependent membrane recruitment of protein kinase B leading to a loss in downstream signalling in L6 skeletal muscle cells Diabetologia 44 2001 173 183 (Pubitemid 32156201)
8. N. Ghosh, N. Patel, K. Jiang, J.E. Watson, J. Cheng, C.E. Chalfant, and D.R. Cooper Ceramide-activated protein phosphatase involvement in insulin resistance via Akt, serine/arginine-rich protein 40, and ribonucleic acid splicing in L6 skeletal muscle cells Endocrinology 148 2007 1359 1366
9. Y.A. Hannun, and L.M. Obeid Principles of bioactive lipid signalling: lessons from sphingolipids Nat. Rev. Mol. Cell Biol. 9 2008 139 150 (Pubitemid 351158911)
10. N.C. Lucki, and M.B. Sewer Nuclear sphingolipid metabolism Annu. Rev. Physiol. 74 2012 131 151
11. J.E. Chipuk, G.P. McStay, A. Bharti, T. Kuwana, C. Clarke, L.J. Siskind, L.M. Obeid, and D.R. Green Sphingolipid metabolism cooperates with BAK and BAX to promote the mitochondrial pathway of apoptosis Cell 148 2012 988 1000
12. N.C. Hait, J. Allegood, M. Maceyka, G.M. Strub, K.B. Harikumar, S.K. Singh, C. Luo, R. Marmorstein, T. Kordula, S. Milstien, and S. Spiegel Regulation of histone acetylation in the nucleus by sphingosine-1-phosphate Science 325 2009 1254 1257
13. E. Bieberich Ceramide in stem cell differentiation and embryo development: novel functions of a topological cell-signaling lipid and the concept of ceramide compartments J. Lipids 2011 11 ((2011) Article ID 610306)
14. + current by optical isomers of cholesterol Biophys. J. 83 2002 3211 3222 (Pubitemid 36041940)
15. P.-Y. Wang, P. Liu, J. Weng, E. Sontag, and R.G.W. Anderson A cholesterol-regulated PP2A/HePTP complex with dual specificity ERK1/2 phosphatase activity EMBO J. 22 2003 2658 2667 (Pubitemid 36712363)
16. P.-Y. Wang, J. Weng, and R.G.W. Anderson OSBP is a cholesterol-regulated scaffolding protein in control of ERK1/2 activation Science 307 2005 1472 1476 (Pubitemid 40321946)
17. P.-Y. Wang, J. Weng, S. Lee, and R.G.W. Anderson The N terminus controls sterol binding while the C terminus regulates the scaffolding function of OSBP J. Biol. Chem. 283 2008 8034 8045
18. K. Burger, G. Gimpl, and F. Fahrenholz Regulation of receptor function by cholesterol Cell. Mol. Life Sci. 57 2000 1577 1592
19. D.M. Owen, M.A.A. Neil, P.M.W. French, and A.I. Magee Optical techniques for imaging membrane lipid microdomains in living cells Semin. Cell Dev. Biol. 18 2007 591 598 (Pubitemid 350026425)
20. D. Wüstner, J.R. Brewer, L. Bagatolli, and D. Sage Potential of ultraviolet wide-field imaging and multiphoton microscopy for analysis of dehydroergosterol in cellular membranes Microsc. Res. Tech. 74 2011 92 108
21. A. Fujita, J. Cheng, and T. Fujimoto Segregation of GM1 and GM3 clusters in the cell membrane depends on the intact actin cytoskeleton Biochim. Biophys. Acta Mol. Cell. Biol. Lipids 1791 2009 388 396
22. S.J. Sahl, M. Leutenegger, M. Hilbert, S.W. Hell, and C. Eggeling Fast molecular tracking maps nanoscale dynamics of plasma membrane lipids Proc. Natl. Acad. Sci. U. S. A. 107 2010 6829 6834
23. P. Janich, and D. Corbeil GM1 and GM3 gangliosides highlight distinct lipid microdomains within the apical domain of epithelial cells FEBS Lett. 581 2007 1783 1787 (Pubitemid 46628803)
24. D. Touboul, A. Brunelle, and O. Laprévote Mass spectrometry imaging: towards a lipid microscope? Biochimie 93 2011 113 119
25. A. van Remoortere, R.J.M. van Zeijl, N. van den Oever, J. Franck, R. Longuespée, M. Wisztorski, M. Salzet, A.M. Deelder, I. Fournier, and L.A. McDonnell MALDI imaging and profiling MS of higher mass proteins from tissue J. Am. Soc. Mass Spectrom. 21 2010 1922 1929
26. R.C. Murphy, J.A. Hankin, R.M. Barkley, and K.A. Zemski Berry MALDI imaging of lipids after matrix sublimation/deposition Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1811 2011 970 975
27. D. Touboul, S. Roy, D.P. Germain, P. Chaminade, A. Brunelle, and O. Laprevote MALDI-TOF and cluster-TOF-SIMS imaging of Fabry disease biomarkers Int. J. Mass Spectrom. 260 2007 158 165
28. M.L. Reyzer, and R.M. Caprioli MALDI-MS-based imaging of small molecules and proteins in tissues Curr. Opin. Chem. Biol. 11 2007 29 35 (Pubitemid 46217921)
29. P. Chaurand, D.S. Cornett, P.M. Angel, and R.M. Caprioli From whole-body sections down to cellular level, multiscale imaging of phospholipids by MALDI mass spectrometry Mol. Cell. Proteomics 10 2011 10.1074/mcp.O110.004259
30. H. Li, and A.B. Hummon Imaging mass spectrometry of three-dimensional cell culture systems Anal. Chem. 83 2011 8794 8801
31. D. Touboul, O. Laprévote, and A. Brunelle Micrometric molecular histology of lipids by mass spectrometry imaging Curr. Opin. Chem. Biol. 15 2011 725 732
32. B. Balluff, C. Schöne, H. Höfler, and A. Walch MALDI imaging mass spectrometry for direct tissue analysis: technological advancements and recent applications Histochem. Cell Biol. 136 2011 227 244
33. N. Goto-Inoue, T. Hayasaka, N. Zaima, and M. Setou Imaging mass spectrometry for lipidomics Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1811 2011 961 969
34. P. Sigmund Theory of sputtering. I. Sputtering yield of amorphous and polycrystalline targets Phys. Rev. 184 1969 383 416
35. M.L. Yu Matrix effects in the work-function dependence of negative-secondary-ion emission Phys. Rev. B 26 1982 4731 4734
36. M.L. Yu Chemical enhancement effects in SIMS analysis Nucl. Instrum. Methods Phys. Res. Sect. B 15 1986 151 158
37. A.M. Piwowar, N.P. Lockyer, and J.C. Vickerman Salt effects on ion formation in desorption mass spectrometry: an investigation into the role of alkali chlorides on peak suppression in time-of-flight-secondary ion mass spectrometry Anal. Chem. 81 2009 1040 1048
38. E.A. Jones, N.P. Lockyer, J. Kordys, and J.C. Vickerman Suppression and enhancement of secondary ion formation due to the chemical environment in static-secondary ion mass spectrometry J. Am. Soc. Mass Spectrom. 18 2007 1559 1567 (Pubitemid 47096798)
39. A.F.M. Altelaar, J. van Minnen, R.M.A. Heeren, and S.R. Piersma The influence of the cholesterol microenvironment in tissue sections on molecular ionization efficiencies and distributions in ToF-SIMS Appl. Surf. Sci. 252 2006 6702 6705 (Pubitemid 44233829)
40. A.G. Sostarecz, D.M. Cannon Jr., C.M. McQuaw, S. Sun, A.G. Ewing, and N. Winograd Influence of molecular environment on the analysis of phospholipids by secondary ion mass spectrometry Langmuir 20 2004 4926 4932
41. S. Rangarajan, and B.J. Tyler Topography in secondary ion mass spectroscopy images J. Vac. Sci. Technol. A 24 2006 1730 1736 (Pubitemid 44370760)
42. B.J. Tyler Interpretation of TOF-SIMS images: multivariate and univariate approaches to image de-noising, image segmentation, and compound identification Appl. Surf. Sci. 203-204 2003 825 831
43. C. Prinz, J. Malm, F. Hook, and P. Sjovall Structural effects in the analysis of supported lipid bilayers by time-of-flight secondary ion mass spectrometry Langmuir 23 2007 8035 8041 (Pubitemid 47155312)
44. M.E. Kurczy, P.D. Piehowski, C.T. Van Bell, M.L. Heien, N. Winograd, and A.G. Ewing Mass spectrometry imaging of mating Tetrahymena show that changes in cell morphology relate to lipid domain formation Proc. Natl. Acad. Sci. U. S. A. 107 2010 2751 2756
45. S.G. Ostrowski, C.T. Van Bell, N. Winograd, and A.G. Ewing Mass spectrometric imaging of highly curved membranes during Tetrahymena mating Science 305 2004 71 73 (Pubitemid 38869371)
46. P.D. Piehowski, A.M. Davey, M.E. Kurczy, E.D. Sheets, N. Winograd, A.G. Ewing, and M.L. Heien Time-of-flight secondary ion mass spectrometry imaging of subcellular lipid heterogeneity: Poisson counting and spatial resolution Anal. Chem. 81 2009 5593 5602
47. A. Benninghoven Surface investigation of solids by the statical method of secondary ion mass spectroscopy (SIMS) Surf. Sci. 35 1973 427 457
48. M.K. Passarelli, and N. Winograd Lipid imaging with time-of-flight secondary ion mass spectrometry (ToF-SIMS) Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1811 2011 976 990
49. D.M. Cannon Jr., M.L. Pacholski, N. Winograd, and A.G. Ewing Molecule specific imaging of freeze-fractured, frozen-hydrated model membrane systems using mass spectrometry J. Am. Chem. Soc. 122 2000 603 610 (Pubitemid 30090497)
50. L. Zheng, C.M. McQuaw, A.G. Ewing, and N. Winograd Sphingomyelin/ phosphatidylcholine and cholesterol interaction studied by imaging mass spectrometry J. Am. Chem. Soc. 129 2007 15730 15731
51. C.M. McQuaw, L. Zheng, A.G. Ewing, and N. Winograd Localization of sphingomyelin in cholesterol domains by imaging mass spectrometry Langmuir 23 2007 5645 5650 (Pubitemid 46826517)
52. D. Touboul, F. Kollmer, E. Niehuis, A. Brunelle, and O. Laprévote Improvement of biological time-of-flight-secondary ion mass spectrometry imaging with a bismuth cluster ion source J. Am. Soc. Mass Spectrom. 16 2005 1608 1618 (Pubitemid 41345153)
53. J.S. Fletcher, and J.C. Vickerman A new SIMS paradigm for 2D and 3D molecular imaging of bio-systems Anal. Biochem. 396 2010 85 104
54. N. Winograd, and B.J. Garrison Biological cluster mass spectrometry Annu. Rev. Phys. Chem. 61 2010 305 322
55. J.S. Fletcher, N.P. Lockyer, and J.C. Vickerman Developments in molecular SIMS depth profiling and 3D imaging of biological systems using polyatomic primary ions Mass Spec. Rev. 30 2010 142 174
56. S.G. Ostrowski, C. Szakal, J. Kozole, T.P. Roddy, J. Xu, A.G. Ewing, and N. Winograd Secondary ion MS imaging of lipids in picoliter vials with a buckminsterfullerene ion source Anal. Chem. 77 2005 6190 6196 (Pubitemid 41436952)
57. H. Nygren, K. Börner, B. Hagenhoff, P. Malmberg, and J.-E. Månsson Localization of cholesterol, phosphocholine, and galactosylceramide in rat cerebellar cortel with imaging TOF-SIMS equipped with a bismuth cluster ion source Biochim. Biophys. Acta Mol. Cell. Biol. Lipids 1737 2005 102 110 (Pubitemid 41740704)
58. P. Sjovall, J. Lausmaa, and B. Johansson Mass spectrometric imaging of lipids in brain tissue Anal. Chem. 76 2004 4271 4278 (Pubitemid 39013993)
59. 3 bombardment of water ice as a function of incident kinetic energy Anal. Chem. 79 2007 4493 4498 (Pubitemid 46999562)
60. E.J. Smiley, N. Winograd, and B.J. Garrison Effect of cluster size in kiloelectronvolt cluster bombardment of solid benzene Anal. Chem. 79 2006 494 499
61. C. Szakal, J. Kozole, M.F. Russo Jr., B.J. Garrison, and N. Winograd Surface sensitivity in cluster-ion-induced sputtering Phys. Rev. Lett. 96 2006 216104
62. B.J. Garrison, and Z. Postawa Computational view of surface based organic mass spectrometry Mass Spectrom. Rev. 27 2008 289 351
63. 60) primary ions Anal. Chem. 79 2007 2199 2206 (Pubitemid 46448998)
64. J.S. Fletcher, S. Rabbani, A. Henderson, N.P. Lockyer, and J.C. Vickerman Three-dimensional mass spectral imaging of HeLa-M cells - sample preparation, data interpretation and visualisation Rapid Commun. Mass Spectrom. 25 2011 925 932
65. J. Brison, M.A. Robinson, D.S.W. Benoit, S. Muramoto, P.S. Stayton, and D.G. Castner TOF-SIMS 3D imaging of native and non-native species within HeLa cells Anal. Chem. 85 2013 10869 10877
66. K.J. Wu, and R.W. Odom Matrix-enhanced secondary ion mass spectrometry: a method for molecular analysis of solid surfaces Anal. Chem. 68 1996 873 882
67. L.A. McDonnell, S.R. Piersma, A.F.M. Altelaar, T.H. Mize, S.L. Luxembourg, P.D.E.M. Verhaert, J. van Minnen, and R.M.A. Heeren Subcellular imaging mass spectrometry of brain tissue J. Mass Spectrom. 40 2005 160 168 (Pubitemid 40330922)
68. J.J.D. Fitzgerald, P. Kunnath, and A.V. Walker Matrix-enhanced secondary ion mass spectrometry (ME SIMS) using room temperature ionic liquid matrices Anal. Chem. 82 2010 4413 4419
69. S.L. Luxembourg, L.A. McDonnell, M.C. Duursma, X. Guo, and R.M.A. Heeren Effect of local matrix crystal variations in matrix-assisted ionization techniques for mass spectrometry Anal. Chem. 75 2003 2333 2341 (Pubitemid 36582816)
70. A.F.M. Altelaar, I. Klinkert, R.P.J. de Lange, R.A.H. Adan, R.M.A. Heeren, and S.R. Piersma Gold-enhanced biomolecular surface imaging of cells and tissue by SIMS and MALDI mass spectrometry Anal. Chem. 78 2006 734 742 (Pubitemid 43228580)
71. A. Delcorte, J. Bour, F. Aubriet, J.F. Muller, and P. Bertrand Sample metallization for performance improvement in desorption/ionization of kilodalton molecules: quantitative evaluation, imaging secondary ion MS, and laser ablation Anal. Chem. 75 2003 6875 6885 (Pubitemid 37523587)
72. A. Delcorte, S. Yunus, N. Wehbe, N. Nieuwjaer, C. Poleunis, A. Felten, L. Houssiau, J.J. Pireaux, and P. Bertrand Metal-assisted secondary ion mass spectrometry using atomic (Ga +, In +) and fullerene projectiles Anal. Chem. 79 2007 3673 3689 (Pubitemid 46799063)
73. M.C. Biesinger, P.-Y. Paepegaey, N.S. McIntyre, R.R. Harbottle, and N.O. Petersen Principal component analysis of TOF-SIMS images of organic monolayers Anal. Chem. 74 2002 5711 5716 (Pubitemid 35364824)
74. M.C. Biesinger, D.J. Miller, R.R. Harbottle, F. Possmayer, N.S. McIntyre, and N.O. Petersen Imaging lipid distributions in model monolayers by ToF-SIMS with selectively deuterated components and principal components analysis Appl. Surf. Sci. 252 2006 6957 6965 (Pubitemid 44233799)
75. B. Vaezian, C.R. Anderton, and M.L. Kraft Discriminating and imaging different phosphatidylcholine species within phase-separated model membranes by principal component analysis of TOF-SIMS images Anal. Chem. 82 2010 10006 10014
76. C.R. Anderton, B. Vaezian, K. Lou, J.F. Frisz, and M.L. Kraft Identification of a lipid-related peak set to enhance the interpretation of TOF-SIMS data from model and cellular membranes Surf. Interface Anal. 44 2012 322 333
77. E.S.F. Berman, K.S. Kulp, M.G. Knize, L. Wu, E.J. Nelson, D.O. Nelson, and K.J. Wu Distinguishing monosaccharide stereo- and structural isomers with TOF-SIMS and multivariate statistical analysis Anal. Chem. 78 2006 6497 6503 (Pubitemid 44413601)
78. M.S. Wagner, M. Shen, T.A. Horbett, and D.G. Castner Quantitative analysis of binary adsorbed protein films by time of flight secondary ion mass spectrometry J. Biomed. Mater. Res. 64A 2003 1 11 (Pubitemid 37521461)
79. M.S. Wagner, B.J. Tyler, and D.G. Castner Interpretation of static time-of-flight secondary ion mass spectra of adsorbed protein films by multivariate pattern recognition Anal. Chem. 74 2002 1824 1835 (Pubitemid 34303746)
80. M.S. Wagner, M. Shen, T.A. Horbett, and D.G. Castner Quantitative time-of-flight secondary ion mass spectrometry for the characterization of multicomponent adsorbed protein films Appl. Surf. Sci. 203-204 2003 704 709
81. D.J. Graham, and B.D. Ratner Multivariate analysis of TOF-SIMS spectra from dodecanethiol SAM Assembly on gold: spectral interpretation and TOF-SIMS fragmentation patterns Langmuir 18 2002 5861 5868 (Pubitemid 35383417)
82. A.M. Belu, D.J. Graham, and D.G. Castner Time-of-flight secondary ion mass spectrometry: techniques and applications for the characterization of biomaterial surfaces Biomaterials 24 2003 3635 3653 (Pubitemid 36773600)
83. D.J. Graham, M.S. Wagner, and D.G. Castner Information from complexity: challenges of TOF-SIMS data interpretation Appl. Surf. Sci. 252 2006 6860 6868 (Pubitemid 44233837)
84. D.J. Graham, and D.G. Castner Multivariate analysis of ToF-SIMS data from multicomponent systems: the why, when, and how Biointerphases 7 2012 1 12
85. M. Mellinger Multivariate data analysis: its methods Chemom. Intell. Lab. Syst. 2 1987 29 36
86. E.R. Malinowski Factor Analysis in Chemistry 3rd ed. 2002 John Wiley and Sons, Inc. New York
87. S.J. Pachuta Enhancing and automating TOF-SIMS data interpretation using principal component analysis Appl. Surf. Sci. 231-232 2004 217 223
88. B.J. Tyler, G. Rayal, and D.G. Castner Multivariate analysis strategies for processing ToF-SIMS images of biomaterials Biomaterials 28 2007 2412 2423 (Pubitemid 46365917)
89. M.J. Baker, L. Zheng, N. Winograd, N.P. Lockyer, and J.C. Vickerman Mass spectral imaging of glycophospholipids, cholesterol, and glycophorin A in model cell membranes Langmuir 24 2008 11803 11810
90. M. Brulet, A. Seyer, A. Edelman, A. Brunelle, J. Fritsch, M. Ollero, and O. Laprévote Lipid mapping of colonic mucosa by cluster TOF-SIMS imaging and multivariate analysis in cftr knockout mice J. Lipid Res. 51 2010 3034 3045
91. J.-W. Park, H. Min, Y.-P. Kim, H.K. Shon, J. Kim, D.W. Moon, and T.G. Lee Multivariate analysis of ToF-SIMS data for biological applications Surf. Interface Anal. 41 2009 694 703
92. S.-i. Iida, N. Sanada, S.R. Bryan, and M. Suzuki Extraction of inhomogeneous chemical species from TOF-SIMS images with topographic artifacts by using correlation coefficient mapping Appl. Surf. Sci. 255 2008 1603 1605
93. X. Vanden Eynde, and P. Bertrand Quantification of polystyrene blend surfaces based on end group ToF-SIMS analysis Appl. Surf. Sci. 141 1999 1 20
94. R.L. Wilson, and M.L. Kraft Quantifying the molar percentages of cholesterol in supported lipid membranes by time-of-flight secondary ion mass spectrometry and multivariate analysis Anal. Chem. 85 2012 91 97
95. P. Williams Biological imaging using secondary ions J. Biol. 5 2006 18
96. H.A. Klitzing, P.K. Weber, and M.L. Kraft Secondary ion mass spectrometry imaging of biological membranes at high spatial resolution A.A. Sousa, M.J. Kruhlak, Methods in Molecular Biology: Nanoimaging Methods and Protocols vol. 950 2013 Humana Press Totowa, New Jersey 483 501
97. L. Zhu, C. Johnson, and M. Bakovic Stimulation of the human CTP: phosphatidylethanolamine cytidylyltransferase gene by early growth response protein 1 J. Lipid Res. 49 2008 2197 2211
98. P. Keller, and K. Simons Cholesterol is required for surface transport of influenza virus hemagglutinin J. Cell Biol. 140 1998 1357 1367 (Pubitemid 28152985)
99. S. Campbell, K. Gaus, R. Bittman, W. Jessup, S. Crowe, and J. Mak The raft-promoting property of virion-associated cholesterol, but not the presence of virion-associated Brij 98 rafts, is a determinant of human immunodeficiency virus type 1 infectivity J. Virol. 78 2004 10556 10565 (Pubitemid 39258381)
100. P. Scheiffele, T.W. Rietveld, and K. Simons Influenza viruses select ordered lipid domains during budding from the plasma membrane J. Biol. Chem. 274 1999 2038 2044
101. V. Chigorno, C. Riva, M. Valsecchi, M. Nicolini, P. Brocca, and S. Sonnino Metabolic processing of gangliosides by human fibroblasts in culture. Formation and recycling of separate pools of ganglioside Eur. J. Biochem. 250 1997 661 669 (Pubitemid 28022482)
102. V. Dolo, S. D'Ascenzo, M. Sorice, A. Pavan, M. Sciannamblo, A. Prinetti, V. Chigorno, G. Tettamanti, and S. Sonnino New approaches to the study of sphingolipid enriched membrane domains: the use of electron microscopic autoradiography to reveal metabolically tritium labeled sphingolipids in cell cultures Glycoconjugate J. 17 2000 261 268 (Pubitemid 32055914)
103. G. van Echten, R. Birk, G. Brenner-Weiss, R.R. Schmidt, and K. Sandhoff Modulation of sphingolipid biosynthesis in primary cultured neurons by long chain bases J. Biol. Chem. 265 1990 9333 9339
104. G. Schwarzmann, P. Hoffmann-Bleihauer, J. Schubert, K. Sandhoff, and D. Marsh Incorporation of ganglioside analogues into fibroblast cell membranes, a spin-label study Biochemistry 22 1983 5041 5048 (Pubitemid 14240699)
105. R. Peteranderl, and C. Lechene Measurement of carbon and nitrogen stable isotope ratios in cultured cells J. Am. Soc. Mass Spectrom. 15 2004 478 485 (Pubitemid 38407133)
106. J.F. Frisz, K. Lou, H.A. Klitzing, W.P. Hanafin, V. Lizunov, R.L. Wilson, K.J. Carpenter, R. Kim, I.D. Hutcheon, J. Zimmerberg, P.K. Weber, and M.L. Kraft Direct chemical evidence for sphingolipid domains in the plasma membranes of fibroblasts Proc. Natl. Acad. Sci. U. S. A. 110 2013 E613 E622
107. M. Edidin Lipids on the frontier: a century of cell-membrane bilayers Nat. Rev. Mol. Cell Biol. 4 2003 414 418 (Pubitemid 36565573)
108. S. Ghosal, S.J. Fallon, T.J. Leighton, K.E. Wheeler, M.J. Kristo, I.D. Hutcheon, and P.K. Weber Imaging and 3D elemental characterization of intact bacterial spores by high-resolution secondary ion mass spectrometry Anal. Chem. 80 2008 5986 5992
109. K. Simons, and W.L.C. Vaz Model systems, lipid rafts, and cell membranes Annu. Rev. Biophys. Biomol. Struct. 33 2004 269 295 (Pubitemid 38829961)
110. G.W. Feigenson Phase diagrams and lipid domains in multicomponent lipid bilayer mixtures Biochim. Biophys. Acta 1788 2009 47 52
111. S.L. Veatch, and S.L. Keller Seeing spots: complex phase behavior in simple membranes Biochim. Biophys. Acta 1746 2005 172 185 (Pubitemid 41815014)
112. M.L. Kraft, P.K. Weber, M.L. Longo, I.D. Hutcheon, and S.G. Boxer Phase separation of lipid membranes analyzed with high-resolution secondary ion mass spectrometry Science 313 2006 1948 1951 (Pubitemid 44497999)
113. S.G. Boxer, M.L. Kraft, and P.K. Weber Advances in imaging secondary ion mass spectrometry for biological samples Annu. Rev. Biophys. 38 2009 53 74
114. M.A. Hayat Principles and Techniques of Electron Microscopy: Biological Applications 4th ed. 2000 Cambridge University Press New York
115. J.F. Frisz, H.A. Klitzing, K. Lou, I.D. Hutcheon, P.K. Weber, J. Zimmerberg, and M.L. Kraft Sphingolipid domains in the plasma membranes of fibroblasts are not enriched with cholesterol J. Biol. Chem. 288 2013 16855 16861
116. J. Malm, D. Giannaras, M.O. Riehle, N. Gadegaard, and P. Sjövall Fixation and drying protocols for the preparation of cell samples for time-of-flight secondary ion mass spectrometry analysis Anal. Chem. 81 2009 7197 7205
117. D. Belazi, S. Sole-Domenech, B. Johansson, M. Schalling, and P. Sjovall Chemical analysis of osmium tetroxide staining in adipose tissue using imaging ToF-SIMS Histochem. Cell Biol. 132 2009 105 115
118. T.L. Colliver, C.L. Brummel, M.L. Pachloski, F.D. Swanek, A.G. Ewing, and N. Winograd Atomic and molecular imaging at the single-cell level with TOF-SIMS Anal. Chem. 69 1997 2225 2231
119. M.L. Pachloski, D.M. Cannon, A.G. Ewing, and N. Winograd Static time-of-flight secondary ion mass spectrometry imaging of freeze-fractured frozed-hydrated biological membranes Rapid Commun. Mass Spectrom. 12 1998 1232 1235 (Pubitemid 28422332)
120. T.P. Roddy, D.M. Cannon, S.G. Ostrowski, N. Winograd, and A.G. Ewing Identification of cellular sections with imaging mass spectrometry following freeze fracture Anal. Chem. 74 2002 4020 4026 (Pubitemid 34912899)
121. E.J. Eyring, and J. Ofengand Reaction of formaldehyde with heterocyclic imino nitrogen of purine and pyrimidine nucleosides Biochemistry 6 1967 2500 2506
122. R. Haselkorn, and P. Doty The reaction of formaldehyde with polynucleotides J. Biol. Chem. 236 1961 2738 2745
123. L. Yang, X.-Y. Yu, Z. Zhu, M.J. Iedemac, and J.P. Cowin Probing liquid surfaces under vacuum using SEM and ToF-SIMS Lab Chip 11 2011 2481 2484
124. L. Yang, X.-Y. Yu, Z. Zhu, T. Thevuthasan, and J.P. Cowin Making a hybrid microfluidic platform compatible for in situ imaging by vacuum-based techniques J. Vac. Sci. Technol. A 29 2011 061101
125. C.M. McQuaw, A.G. Sostarecz, L. Zheng, A.G. Ewing, and N. Winograd Lateral heterogeneity of dipalmitoylphosphatidylethanolamine-cholesterol Langmuir-Blodgett films investigated with imaging mass spectrometry and atomic force microscopy Langmuir 21 2005 807 813 (Pubitemid 40184772)
126. M.L. Pachloski, D.M. Cannon, A.G. Ewing, and N. Winograd Imaging of exposed headgroups and tailgroups of phospholipid membranes by mass spectrometry J. Am. Chem. Soc. 121 1999 4716 4717 (Pubitemid 29239512)
127. T.P. Roddy, D.M. Cannon, S.G. Ostrowski, A.G. Ewing, and N. Winograd Proton transfer in time-of-flight secondary ion mass spectrometry studies of frozen-hydrated dipalmitoylphosphatidylcholine Anal. Chem. 75 2003 4087 4094 (Pubitemid 37012539)
128. A.G. Sostarecz, C.M. McQuaw, A.G. Ewing, and N. Winograd Phosphatidylethanolamine-induced cholesterol domains chemically identified with mass spectrometric imaging J. Am. Chem. Soc. 126 2004 13882 13883 (Pubitemid 39447038)
129. K. Simons, and E. Ikonen Functional rafts in cell membranes Nature 387 1997 569 572 (Pubitemid 27248754)
130. D. Lingwood, and K. Simons Lipid rafts as an organizing principle Science 327 2010 46 50
131. J. Popov, D. Vobornik, O. Coban, E. Keating, D. Miller, J. Francis, N.O. Petersen, and L.J. Johnston Chemical mapping of ceramide distribution in sphingomyelin-rich domains in monolayers Langmuir 24 2008 13502 13508
132. S.G. Ostrowski, M.E. Kurczy, T.P. Roddy, N. Winograd, and A.G. Ewing Secondary ion MS imaging to relatively quantify cholesterol in the membranes of individual cells from differentially treated populations Anal. Chem. 79 2007 3554 3560 (Pubitemid 46799048)
133. I. Lanekoff, P. Sjovall, and A.G. Ewing Relative quantification of phospholipid accumulation in the PC12 cell plasma membrane following phospholipid incubation using TOF-SIMS imaging Anal. Chem. 83 2011 5337 5343
134. J.S. Fletcher, S. Rabbani, A. Henderson, P. Blenkinsopp, S.P. Thompson, N.P. Lockyer, and J.C. Vickerman A new dynamic in mass spectral imaging of single biological cells Anal. Chem. 80 2008 9058 9064
135. K.R. Amaya, E.B. Monroe, J.V. Sweedler, and D.F. Clayton Lipid imaging in the zebra finch brain with secondary ion mass spectrometry Int. J. Mass Spectrom. 260 2007 121 127
136. K. Börner, H. Nygren, B. Hagenhoff, P. Malmberg, E. Tallarek, and J.-E. Månsson Distribution of cholesterol and galactosylceramide in rat cerebellar white matter Biochim. Biophys. Acta Mol. Cell. Biol. Lipids 1761 2006 335 344
137. Z. Pernber, K. Richter, J.-E. Mansson, and H. Nygren 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 2007 202 209 (Pubitemid 46210191)
138. P. Malmberg, H. Nygren, K. Richter, Y. Chen, F. Dangardt, P. Friberg, and Y. Magnusson Imaging of lipids in human adipose tissue by cluster ion TOF-SIMS Microsc. Res. Tech. 70 2007 828 835 (Pubitemid 47509782)
139. N. Tahallah, A. Brunelle, S. De La Porte, and O. Laprévote Lipid mapping in human dystrophic muscle by cluster-time-of-flight secondary ion mass spectrometry imaging J. Lipid Res. 49 2008 438 454 (Pubitemid 351213629)
140. A. Seyer, M. Cantiello, J. Bertrand-Michel, V. Roques, M. Nauze, V. Bézirard, X. Collet, D. Touboul, A. Brunelle, and C. Coméra Lipidomic and spatio-temporal imaging of fat by mass spectrometry in mice duodenum during lipid digestion PLoS ONE 8 2013 e58224
141. P. Malmberg, K. Börner, Y. Chen, P. Friberg, B. Hagenhoff, J.-E. Månsson, and H. Nygren Localization of lipids in the aortic wall with imaging TOF-SIMS Biochim. Biophys. Acta Mol. Cell. Biol. Lipids 1771 2007 185 195 (Pubitemid 46205410)
142. A. Lazar, C. Bich, M. Panchal, N. Desbenoit, V. Petit, D. Touboul, L. Dauphinot, C. Marquer, O. Laprévote, A. Brunelle, and C. Duyckaerts Time-of-flight secondary ion mass spectrometry (TOF-SIMS) imaging reveals cholesterol overload in the cerebral cortex of Alzheimer disease patients Acta Neuropathol. 125 2013 133 144
143. C. Galli Marxer, M.L. Kraft, P.K. Weber, I.D. Hutcheon, and S.G. Boxer Supported membrane composition analysis by secondary ion mass spectrometry with high lateral resolution Biophys. J. 88 2005 2965 2975 (Pubitemid 40983845)
144. M.L. Kraft, S.F. Fishel, C. Galli Marxer, P.K. Weber, I.D. Hutcheon, and S.G. Boxer Quantitative analysis of supported membrane composition using the NanoSIMS Appl. Surf. Sci. 252 2006 6950 6956
145. C.R. Anderton, P.K. Weber, K. Lou, I.D. Hutcheon, and M.L. Kraft Correlated AFM and NanoSIMS imaging to probe cholesterol-induced changes in phase behavior and non-ideal mixing in ternary lipid membranes Biochim. Biophys. Acta 1808 2011 307 315
146. M.M. Lozano, Z. Liu, E. Sunnick, A. Janshoff, K. Kumar, and S.G. Boxer Colocalization of the ganglioside GM1 and cholesterol detected by secondary ion mass spectrometry J. Am. Chem. Soc. 135 2013 5620 5630
147. P.D. Rakowska, H. Jiang, S. Ray, A. Pyne, B. Lamarre, M. Carr, P.J. Judge, J. Ravi, U.I.M. Gerling, B. Koksch, G.J. Martyna, B.W. Hoogenboom, A. Watts, J. Crain, C.R.M. Grovenor, and M.G. Ryadnov Nanoscale imaging reveals laterally expanding antimicrobial pores in lipid bilayers Proc. Natl. Acad. Sci. U. S. A. 110 2013 8918 8923
148. 13C-oleate in adipocytes measured using multi imaging mass spectrometry J. Am. Soc. Mass Spectrom. 15 2004 1572 1580 (Pubitemid 39433851)
149. M.L. Kraft Plasma membrane organization and function: moving past lipid rafts Mol. Biol. Cell 24 2013 2765 2768