1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Analytical Chemistry
  4. Volume 12, 2019
  5. Article

Annual Review of Analytical Chemistry

Volume 12, 2019

Metabolic Imaging at the Single-Cell Scale: Recent Advances in Mass Spectrometry Imaging

Abstract

There is an increasing appreciation that every cell, even of the same type, is different. This complexity, when additionally combined with the variety of different cell types in tissue, is driving the need for spatially resolved omics at the single-cell scale. Rapid advances are being made in genomics and transcriptomics, but progress in metabolomics lags. This is partly because amplification and tagging strategies are not suited to dynamically created metabolite molecules. Mass spectrometry imaging has excellent potential for metabolic imaging. This review summarizes the recent advances in two of these techniques: matrix-assisted laser desorption ionization (MALDI) and secondary ion mass spectrometry (SIMS) and their convergence in subcellular spatial resolution and molecular information. The barriers that have held back progress such as lack of sensitivity and the breakthroughs that have been made including laser-postionization are highlighted as well as the future challenges and opportunities for metabolic imaging at the single-cell scale.

Keyword(s): MALDI, mass spectrometry imaging, matrix-assisted laser desorption ionization, metabolite, postionization, secondary ion mass spectrometry, SIMS, single-cell
Loading

Article metrics loading...

/content/journals/10.1146/annurev-anchem-061318-115516
2019-06-12
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/ac/12/1/annurev-anchem-061318-115516.html?itemId=/content/journals/10.1146/annurev-anchem-061318-115516&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Hayden EC. 2014. The $1,000 genome. Nature 507:294–95
     [Google Scholar]
  2. 2.
    Gawad C, Koh W, Quake SR 2016. Single-cell genome sequencing: current state of the science. Nat. Rev. Genet 17:175–88
     [Google Scholar]
  3. 3.
    Svensson V, Vento-Tormo R, Teichmann SA 2018. Exponential scaling of single-cell RNA-seq in the past decade. Nat. Protoc 13:599–604
     [Google Scholar]
  4. 4.
    Lee JH. 2017. Quantitative approaches for investigating the spatial context of gene expression. Wiley Interdiscip. Rev. Syst. Biol. Med 9:e1369
     [Google Scholar]
  5. 5.
    Angelo M, Bendall SC, Finck R, Hale MB, Hitzman C et al. 2014. Multiplexed ion beam imaging of human breast tumors. Nat. Med 20:436–42
     [Google Scholar]
  6. 6.
    Zenobi R. 2013. Single-cell metabolomics: analytical and biological perspectives. Science 342:1243259
     [Google Scholar]
  7. 7.
    Fessenden M. 2016. Metabolomics: small molecules, single cells. Nature 540:153–55
     [Google Scholar]
  8. 8.
    Doerr A. 2018. Mass spectrometry imaging takes off. Nat. Methods 15:32
     [Google Scholar]
  9. 9.
    Linwen Z, Akos V. 2018. Single-cell mass spectrometry approaches to explore cellular heterogeneity. Angew. Chem. Int. Ed 57:4466–77
     [Google Scholar]
  10. 10.
    Fujii T, Matsuda S, Tejedor ML, Esaki T, Sakane I et al. 2015. Direct metabolomics for plant cells by live single-cell mass spectrometry. Nat. Protoc 10:1445–56
     [Google Scholar]
  11. 11.
    Kalluri R. 2016. The biology and function of fibroblasts in cancer. Nat. Rev. Cancer 16:582–98
     [Google Scholar]
  12. 12.
    Gilmore IS. 2013. SIMS of organics—advances in 2D and 3D imaging and future outlook. J. Vac. Sci. Technol. A 31:050819
     [Google Scholar]
  13. 13.
    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
     [Google Scholar]
  14. 14.
    Castellino S, Groseclose MR, Wagner D 2011. MALDI imaging mass spectrometry: bridging biology and chemistry in drug development. Bioanalysis 3:2427–41
     [Google Scholar]
  15. 15.
    Römpp A, Spengler B. 2013. Mass spectrometry imaging with high resolution in mass and space. Histochem. Cell Biol 139:759–83
     [Google Scholar]
  16. 16.
    Feigl P, Schueler B, Hillenkamp F 1983. LAMMA 1000, a new instrument for bulk microprobe mass analysis by pulsed laser irradiation. Int. J. Mass Spectrom. Ion Phys 47:15–18
     [Google Scholar]
  17. 17.
    Karas M, Bachmann D, Hillenkamp F 1985. Influence of the wavelength in high-irradiance ultraviolet laser desorption mass spectrometry of organic molecules. Anal. Chem 57:2935–39
     [Google Scholar]
  18. 18.
    Spengler B, Hubert M. 2002. Scanning microprobe matrix-assisted laser desorption ionization (SMALDI) mass spectrometry: instrumentation for sub-micrometer resolved LDI and MALDI surface analysis. J. Am. Soc. Mass Spectrom 13:735–48
     [Google Scholar]
  19. 19.
    Zavalin A, Todd EM, Rawhouser PD, Yang J, Norris JL, Caprioli RM 2012. Direct imaging of single cells and tissue at sub-cellular spatial resolution using transmission geometry MALDI MS. J. Mass Spectrom 47:1473–81
     [Google Scholar]
  20. 20.
    Spengler B, Hubert M, Kaufmann R 1994. MALDI ion imaging and biological ion imaging with a new scanning UV-laser microprobe. Proceedings of the 42nd Annual Conference on Mass Spectrometry and Allied Topics1041 Chicago: ASMS
     [Google Scholar]
  21. 21.
    Makarov A. 2000. Electrostatic axially harmonic orbital trapping: a high-performance technique of mass analysis. Anal. Chem 72:1156–62
     [Google Scholar]
  22. 22.
    Potočnik NO, Porta T, Becker M, Heeren RMA, Ellis SR 2015. Use of advantageous, volatile matrices enabled by next-generation high-speed matrix-assisted laser desorption/ionization time-of-flight imaging employing a scanning laser beam. Rapid Commun. Mass Spectrom 29:2195–203
     [Google Scholar]
  23. 23.
    Kettling H, Vens-Cappell S, Soltwisch J, Pirkl A, Haier J et al. 2014. MALDI mass spectrometry imaging of bioactive lipids in mouse brain with a Synapt G2-S mass spectrometer operated at elevated pressure: improving the analytical sensitivity and the lateral resolution to ten micrometers. Anal. Chem 86:7798–805
     [Google Scholar]
  24. 24.
    Korte AR, Yandeau-Nelson MD, Nikolau BJ, Lee YJ 2015. Subcellular-level resolution MALDI-MS imaging of maize leaf metabolites by MALDI-linear ion trap-Orbitrap mass spectrometer. Anal. Bioanal. Chem 407:2301–9
     [Google Scholar]
  25. 25.
    Takahashi K, Kozuka T, Anegawa A, Nagatani A, Mimura T 2015. Development and application of a high-resolution imaging mass spectrometer for the study of plant tissues. Plant Cell Physiol 56:1329–38
     [Google Scholar]
  26. 26.
    Feenstra AD, Dueñas ME, Lee YJ 2017. Five micron high resolution MALDI mass spectrometry imaging with simple, interchangeable, multi-resolution optical system. J. Am. Soc. Mass Spectrom 28:434–42
     [Google Scholar]
  27. 27.
    Belov ME, Ellis SR, Dilillo M, Paine MRL, Danielson WF et al. 2017. Design and performance of a novel interface for combined matrix-assisted laser desorption ionization at elevated pressure and electrospray ionization with Orbitrap mass spectrometry. Anal. Chem 89:7493–501
     [Google Scholar]
  28. 28.
    Laiko VV, Moyer SC, Cotter RJ 2000. Atmospheric pressure MALDI/ion trap mass spectrometry. Anal. Chem 72:5239–43
     [Google Scholar]
  29. 29.
    Koestler M, Kirsch D, Hester A, Leisner A, Guenther S, Spengler B 2008. A high-resolution scanning microprobe matrix-assisted laser desorption/ionization ion source for imaging analysis on an ion trap/Fourier transform ion cyclotron resonance mass spectrometer. Rapid Commun. Mass Spectrom 22:3275–85
     [Google Scholar]
  30. 30.
    Spengler B, Bökelmann V. 1993. Angular and time resolved intensity distributions of laser-desorbed matrix ions. Nuclear Inst. Methods Phys. Res. B 82:379–85
     [Google Scholar]
  31. 31.
    Kompauer M, Heiles S, Spengler B 2016. Atmospheric pressure MALDI mass spectrometry imaging of tissues and cells at 1.4-μm lateral resolution. Nat. Methods 14:90–96
     [Google Scholar]
  32. 32.
    Briggs D. 1983. Analysis of polymer surfaces by SIMS, 3—preliminary results from molecular imaging and microanalysis experiments. Surf. Interface Anal 5:113–18
     [Google Scholar]
  33. 33.
    Winograd N. 2005. The magic of cluster SIMS. Anal. Chem 77:143A–49A
     [Google Scholar]
  34. 34.
    Seah MP, Havelund R, Gilmore IS 2014. Universal equation for argon cluster size-dependence of secondary ion spectra in SIMS of organic materials. J. Phys. Chem. C 118:12862–72
     [Google Scholar]
  35. 35.
    Winograd N. 2018. Gas cluster ion beams for secondary ion mass spectrometry. Annu. Rev. Anal. Chem 11:29–48
     [Google Scholar]
  36. 36.
    Gilmore IS, Seah MP. 2000. Ion detection efficiency in SIMS: dependencies on energy, mass and composition for microchannel plates used in mass spectrometry. Int. J. Mass Spectrom 202:217–29
     [Google Scholar]
  37. 37.
    Lee JLS, Ninomiya S, Matsuo J, Gilmore IS, Seah MP, Shard AG 2010. Organic depth profiling of a nanostructured delta layer reference material using large argon cluster ions. Anal. Chem 82:98–105
     [Google Scholar]
  38. 38.
    Matsuo J, Torii S, Yamauchi K, Wakamoto K, Kusakari M et al. 2014. Novel SIMS system with focused massive cluster ion source for mass imaging spectrometry with high lateral resolution. Appl. Phys. Express 7:056602
     [Google Scholar]
  39. 39.
    Ninomiya S, Ichiki K, Yamada H, Nakata Y, Seki T et al. 2009. Precise and fast secondary ion mass spectrometry depth profiling of polymer materials with large Ar cluster ion beams. Rapid Commun. Mass Spectrom 23:1601–6
     [Google Scholar]
  40. 40.
    Ninomiya S, Nakata Y, Ichiki K, Seki T, Aoki T, Matsuo J 2007. Measurements of secondary ions emitted from organic compounds bombarded with large gas cluster ions. Nuclear Instrum. Methods Phys. B 256:493–96
     [Google Scholar]
  41. 41.
    Passarelli MK, Pirkl A, Moellers R, Grinfeld D, Kollmer F et al. 2017. The 3D OrbiSIMS-label-free metabolic imaging with subcellular lateral resolution and high mass-resolving power. Nat. Methods 14:1175–83
     [Google Scholar]
  42. 42.
    Phan NTN, Munem M, Ewing AG, Fletcher JS 2017. MS/MS analysis and imaging of lipids across Drosophila brain using secondary ion mass spectrometry. Anal. Bioanal. Chem 409:3923–32
     [Google Scholar]
  43. 43.
    Rabbani S, Barber AM, Fletcher JS, Lockyer NP, Vickerman JC 2011. TOF-SIMS with argon gas cluster ion beams: a comparison with C60+. Anal. Chem 83:3793–800
     [Google Scholar]
  44. 44.
    Tian H, Maciążek D, Postawa Z, Garrison BJ, Winograd N 2016. CO2 cluster ion beam, an alternative projectile for secondary ion mass spectrometry. J. Am. Soc. Mass Spectrom 27:1476–82
     [Google Scholar]
  45. 45.
    Ichiki K, Tamura J, Seki T, Aoki T, Matsuo J 2013. Development of gas cluster ion beam irradiation system with an orthogonal acceleration TOF instrument. Surf. Interface Anal 45:522–24
     [Google Scholar]
  46. 46.
    Satoshi N, Kazuya I, Hideaki Y, Yoshihiko N, Toshio S et al. 2011. The effect of incident energy on molecular depth profiling of polymers with large Ar cluster ion beams. Surf. Interface Anal 43:221–24
     [Google Scholar]
  47. 47.
    Sheraz née Rabbani S, Barber A, Fletcher JS, Lockyer NP, Vickerman JC 2013. Enhancing secondary ion yields in time of flight-secondary ion mass spectrometry using water cluster primary beams. Anal. Chem 85:5654–58
     [Google Scholar]
  48. 48.
    Rabbani SS, Berrueta Razo I, Kohn T, Lockyer NP, Vickerman JC 2015. Enhancing ion yields in time-of-flight-secondary ion mass spectrometry: a comparative study of argon and water cluster primary beams. Anal. Chem 87:2367–74
     [Google Scholar]
  49. 49.
    Gilmore IS, Green FM, Seah MP 2007. Static TOF-SIMS. A VAMAS interlaboratory study. Part II—accuracy of the mass scale and G-SIMS compatibility. Surf. Interface Anal 39:817–25
     [Google Scholar]
  50. 50.
    Bristow AWT, Webb KS. 2003. Intercomparison study on accurate mass measurement of small molecules in mass spectrometry. J. Am. Soc. Mass Spectrom 14:1086–98
     [Google Scholar]
  51. 51.
    Green FM, Gilmore IS, Seah MP 2006. TOF-SIMS: accurate mass scale calibration. J. Am. Soc. Mass Spectrom 17:514–23
     [Google Scholar]
  52. 52.
    Carado A, Passarelli MK, Kozole J, Wingate JE, Winograd N, Loboda AV 2008. C60 secondary ion mass spectrometry with a hybrid-quadrupole orthogonal time-of-flight mass spectrometer. Anal. Chem 80:7921–29
     [Google Scholar]
  53. 53.
    Fletcher JS, Rabbani S, Henderson A, Blenkinsopp P, Thompson SP et al. 2008. A new dynamic in mass spectral imaging of single biological cells. Anal. Chem 80:9058–64
     [Google Scholar]
  54. 54.
    Fisher GL, Bruinen AL, Potocnik NO, Hammond JS, Bryan SR et al. 2016. A new method and mass spectrometer design for TOF-SIMS parallel imaging MS/MS. Anal. Chem 88:6433–40
     [Google Scholar]
  55. 55.
    Scheltema RA, Hauschild JP, Lange O, Hornburg D, Denisov E et al. 2014. The Q Exactive HF, a benchtop mass spectrometer with a pre-filter, high-performance quadrupole and an ultra-high-field Orbitrap analyzer. Mol. Cell. Proteom 13:3698–708
     [Google Scholar]
  56. 56.
    Dreisewerd K, Yew JY. 2017. Mass spectrometry imaging goes three dimensional. Nat. Methods 14:1139–40
     [Google Scholar]
  57. 57.
    Dong Y, Li B, Malitsky S, Rogachev I, Aharoni A et al. 2016. Sample preparation for mass spectrometry imaging of plant tissues: a review. Front. Plant Sci 7:60
     [Google Scholar]
  58. 58.
    Amstalden van Hove ER, Smith DF, Heeren RMA 2010. A concise review of mass spectrometry imaging. J. Chromatogr. A 1217:3946–54
     [Google Scholar]
  59. 59.
    Jaskolla TW, Lehmann W-D, Karas M 2008. 4-Chloro-α-cyanocinnamic acid is an advanced, rationally designed MALDI matrix. PNAS 105:12200–5
     [Google Scholar]
  60. 60.
    Knochenmuss R. 2016. The coupled chemical and physical dynamics model of MALDI. Annu. Rev. Anal. Chem 9:365–85
     [Google Scholar]
  61. 61.
    Strupat K, Kampmeier J, Horneffer V 1997. Investigations of 2,5-DHB and succinic acid as matrices for UV and IR MALDI. Part II: crystallographic and mass spectrometric analysis. Int. J. Mass Spectrom. Ion Process 169–170:43–50
     [Google Scholar]
  62. 62.
    Beavist RC, Chait BT. 1989. Cinnamic acid derivatives as matrices for ultraviolet laser desorption mass spectrometry of proteins. Rapid Commun. Mass Spectrom 3:432–35
     [Google Scholar]
  63. 63.
    Le CH, Han J, Borchers CH 2012. Dithranol as a MALDI matrix for tissue imaging of lipids by Fourier transform ion cyclotron resonance mass spectrometry. Anal. Chem 84:8391–98
     [Google Scholar]
  64. 64.
    Wang J, Qiu S, Chen S, Xiong C, Liu H et al. 2015. MALDI-TOF MS imaging of metabolites with a N-(1-naphthyl) ethylenediamine dihydrochloride matrix and its application to colorectal cancer liver metastasis. Anal. Chem 87:422–30
     [Google Scholar]
  65. 65.
    Ibrahim H, Jurcic K, Wang JSH, Whitehead SN, Yeung KKC 2017. 1,6-Diphenyl-1,3,5-hexatriene (DPH) as a novel matrix for MALDI MS imaging of fatty acids, phospholipids, and sulfatides in brain tissues. Anal. Chem 89:12828–36
     [Google Scholar]
  66. 66.
    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 84:2048–54
     [Google Scholar]
  67. 67.
    Calvano CD, Monopoli A, Cataldi TRI, Palmisano F 2018. MALDI matrices for low molecular weight compounds: an endless story?. Anal. Bioanal. Chem 410:4015–38
     [Google Scholar]
  68. 68.
    Dai Y, Whittal RM, Li L 1996. Confocal fluorescence microscopic imaging for investigating the analyte distribution in MALDI matrices. Anal. Chem 68:2494–500
     [Google Scholar]
  69. 69.
    Bouschen W, Spengler B. 2007. Artifacts of MALDI sample preparation investigated by high-resolution scanning microprobe matrix-assisted laser desorption/ionization (SMALDI) imaging mass spectrometry. Int. J. Mass Spectrom 266:129–37
     [Google Scholar]
  70. 70.
    Körsgen M, Pelster A, Dreisewerd K, Arlinghaus HF 2016. 3D ToF-SIMS analysis of peptide incorporation into MALDI matrix crystals with sub-micrometer resolution. J. Am. Soc. Mass Spectrom 27:277–84
     [Google Scholar]
  71. 71.
    Dreisewerd K. 2003. The desorption process in MALDI. Chem. Rev 103:395–426
     [Google Scholar]
  72. 72.
    Van Nuffel S, Elie N, Yang E, Nouet J, Touboul D et al. 2018. Insights into the MALDI process after matrix deposition by sublimation using 3D ToF-SIMS imaging. Anal. Chem 90:1907–14
     [Google Scholar]
  73. 73.
    Hankin JA, Barkley RM, Murphy RC 2007. Sublimation as a method of matrix application for mass spectrometric imaging. J. Am. Soc. Mass Spectrom 18:1646–52
     [Google Scholar]
  74. 74.
    Dueñas ME, Carlucci L, Lee YJ 2016. Matrix recrystallization for MALDI-MS imaging of maize lipids at high-spatial resolution. J. Am. Soc. Mass Spectrom 27:1575–78
     [Google Scholar]
  75. 75.
    Li S, Zhang Y, Liu JA, Han J, Guan M et al. 2016. Electrospray deposition device used to precisely control the matrix crystal to improve the performance of MALDI MSI. Sci. Rep 6:37903
     [Google Scholar]
  76. 76.
    Bouschen W, Schulz O, Eikel D, Spengler B 2010. Matrix vapor deposition/recrystallization and dedicated spray preparation for high-resolution scanning microprobe matrix-assisted laser desorption/ionization imaging mass spectrometry (SMALDI-MS) of tissue and single cells. Rapid Commun. Mass Spectrom 24:355–64
     [Google Scholar]
  77. 77.
    Schwartz SA, Reyzer ML, Caprioli RM 2003. Direct tissue analysis using matrix-assisted laser desorption/ionization mass spectrometry: practical aspects of sample preparation. J. Mass Spectrom 38:699–708
     [Google Scholar]
  78. 78.
    Gemperline E, Rawson S, Li L 2014. Optimization and comparison of multiple MALDI matrix application methods for small molecule mass spectrometric imaging. Anal. Chem 86:10030–35
     [Google Scholar]
  79. 79.
    Jones EA, Lockyer NP, Vickerman JC 2008. Depth profiling brain tissue sections with a 40 keV C60+ primary ion beam. Anal. Chem 80:2125–32
     [Google Scholar]
  80. 80.
    Sjövall P, Johansson B, Lausmaa J 2006. Localization of lipids in freeze-dried mouse brain sections by imaging TOF-SIMS. Appl. Surf. Sci 252:6966–74
     [Google Scholar]
  81. 81.
    Vickerman JC. 2011. Molecular imaging and depth profiling by mass spectrometry—SIMS, MALDI or DESI?. Analyst 136:2199–217
     [Google Scholar]
  82. 82.
    Newman CF, Havelund R, Passarelli MK, Marshall PS, Francis I et al. 2017. Intracellular drug uptake—a comparison of single cell measurements using ToF-SIMS imaging and quantification from cell populations with LC/MS/MS. Anal. Chem 89:11944–53
     [Google Scholar]
  83. 83.
    Li B, Bhandari DR, Janfelt C, Römpp A, Spengler B 2014. Natural products in Glycyrrhiza glabra (licorice) rhizome imaged at the cellular level by atmospheric pressure matrix-assisted laser desorption/ionization tandem mass spectrometry imaging. Plant J 80:161–71
     [Google Scholar]
  84. 84.
    Yamamoto K, Takahashi K, Mizuno H, Anegawa A, Ishizaki K et al. 2016. Cell-specific localization of alkaloids in Catharanthus roseus stem tissue measured with imaging MS and single-cell MS. PNAS 113:3891–96
     [Google Scholar]
  85. 85.
    Schober Y, Guenther S, Spengler B, Römpp A 2012. Single cell matrix-assisted laser desorption/ionization mass spectrometry imaging. Anal. Chem 84:6293–97
     [Google Scholar]
  86. 86.
    Grove KJ, Voziyan PA, Spraggins JM, Wang S, Paueksakon P et al. 2014. Diabetic nephropathy induces alterations in the glomerular and tubule lipid profiles. J. Lipid Res 55:1375–85
     [Google Scholar]
  87. 87.
    Römpp A, Guenther S, Takats Z, Spengler B 2011. Mass spectrometry imaging with high resolution in mass and space (HR2 MSI) for reliable investigation of drug compound distributions on the cellular level. Anal. Bioanal. Chem 401:65–73
     [Google Scholar]
  88. 88.
    Sørensen IS, Janfelt C, Nielsen MMB, Mortensen RW, Knudsen N et al. 2017. Combination of MALDI-MSI and cassette dosing for evaluation of drug distribution in human skin explant. Anal. Bioanal. Chem 409:4993–5005
     [Google Scholar]
  89. 89.
    Guenther S, Römpp A, Kummer W, Spengler B 2011. AP-MALDI imaging of neuropeptides in mouse pituitary gland with 5 μm spatial resolution and high mass accuracy. Int. J. Mass Spectrom 305:228–37
     [Google Scholar]
  90. 90.
    Passarelli MK, Newman CF, Marshall PS, West A, Gilmore IS et al. 2015. Single-cell analysis: visualizing pharmaceutical and metabolite uptake in cells with label-free 3D mass spectrometry imaging. Anal. Chem 87:6696–702
     [Google Scholar]
  91. 91.
    Rutkowska A, Thomson DW, Vappiani J, Werner T, Mueller KM et al. 2016. A modular probe strategy for drug localization, target identification and target occupancy measurement on single cell level. ACS Chem. Biol 11:2541–50
     [Google Scholar]
  92. 92.
    Tian H, Six DA, Krucker T, Leeds JA, Winograd N 2017. Subcellular chemical imaging of antibiotics in single bacteria using C60-secondary ion mass spectrometry. Anal. Chem 89:5050–57
     [Google Scholar]
  93. 93.
    Jones EA, Lockyer NP, Vickerman JC 2007. Mass spectral analysis and imaging of tissue by ToF-SIMS—the role of buckminsterfullerene, C60+, primary ions. Int. J. Mass Spectrom 260:146–57
     [Google Scholar]
  94. 94.
    Takado Y, Knott G, Humbel BM, Masoodi M, Escrig S et al. 2015. Imaging the time-integrated cerebral metabolic activity with subcellular resolution through nanometer-scale detection of biosynthetic products deriving from 13C-glucose. J. Chem. Neuroanat 69:7–12
     [Google Scholar]
  95. 95.
    Benabdellah F, Seyer A, Quinton L, Touboul D, Brunelle A, Laprévote O 2010. Mass spectrometry imaging of rat brain sections: nanomolar sensitivity with MALDI versus nanometer resolution by TOF-SIMS. Anal. Bioanal. Chem 396:151–62
     [Google Scholar]
  96. 96.
    Hsu C-C, Chou P-T, Zare RN 2015. Imaging of proteins in tissue samples using nanospray desorption electrospray ionization mass spectrometry. Anal. Chem 87:11171–75
     [Google Scholar]
  97. 97.
    Kompauer M, Heiles S, Spengler B 2017. Autofocusing MALDI mass spectrometry imaging of tissue sections and 3D chemical topography of nonflat surfaces. Nat. Methods 14:1156–58
     [Google Scholar]
  98. 98.
    Bartels B, Kulkarni P, Danz N, Böcker S, Saluz HP, Svatoš A 2017. Mapping metabolites from rough terrain: laser ablation electrospray ionization on non-flat samples. RSC Adv 7:9045–50
     [Google Scholar]
  99. 99.
    Dilillo M, Pellegrini D, Ait-Belkacem R, De Graaf EL, Caleo M, McDonnell LA 2017. Mass spectrometry imaging, laser capture microdissection, and LC-MS/MS of the same tissue section. J. Proteome Res 16:2993–3001
     [Google Scholar]
  100. 100.
    Palmer A, Phapale P, Chernyavsky I, Lavigne R, Fay D et al. 2016. FDR-controlled metabolite annotation for high-resolution imaging mass spectrometry. Nat. Methods 14:57–60
     [Google Scholar]
  101. 101.
    Ellis SR, Paine MRL, Eijkel GB, Pauling JK, Husen P et al. 2018. Automated, parallel mass spectrometry imaging and structural identification of lipids. Nat. Methods 15:515–18
     [Google Scholar]
  102. 102.
    Hansen RL, Lee YJ. 2017. Overlapping MALDI-mass spectrometry imaging for in-parallel MS and MS/MS data acquisition without sacrificing spatial resolution. J. Am. Soc. Mass Spectrom 28:1910–18
     [Google Scholar]
  103. 103.
    Paine MRL, Poad BLJ, Eijkel GB, Marshall DL, Blanksby SJ et al. 2018. Mass spectrometry imaging with isomeric resolution enabled by ozone-induced dissociation. Angew. Chem 130:10690–94
     [Google Scholar]
  104. 104.
    Bednařík A, Bölsker S, Soltwisch J, Dreisewerd K 2018. On-tissue Paternò-Büchi reaction for localization of carbon-carbon double bonds in phospho- and glycolipids by matrix-assisted laser desorption ionization mass spectrometry imaging. Angew. Chem. Int. Ed 57:12092–96
     [Google Scholar]
  105. 105.
    Soltwisch J, Jaskolla TW, Hillenkamp F, Karas M, Dreisewerd K 2012. Ion yields in UV-MALDI mass spectrometry as a function of excitation laser wavelength and optical and physico-chemical properties of classical and halogen-substituted MALDI matrixes. Anal. Chem 84:6567–76
     [Google Scholar]
  106. 106.
    Niehaus M, Schnapp A, Koch A, Soltwisch J, Dreisewerd K 2017. New insights into the wavelength dependence of MALDI mass spectrometry. Anal. Chem 89:7734–41
     [Google Scholar]
  107. 107.
    Shariatgorji M, Nilsson A, Goodwin RJA, Källback P, Schintu N et al. 2014. Direct targeted quantitative molecular imaging of neurotransmitters in brain tissue sections. Neuron 84:697–707
     [Google Scholar]
  108. 108.
    Winograd N, Baxter JP, Kimock FM 1982. Multiphoton resonance ionization of sputtered neutrals: a novel approach to materials characterization. Chem. Phys. Lett 88:581–84
     [Google Scholar]
  109. 109.
    Becker CH, Gillen KT. 1984. Surface analysis by nonresonant multiphoton ionization of desorbed or sputtered species. Anal. Chem 56:1671–74
     [Google Scholar]
  110. 110.
    Kimock FM, Baxter JP, Pappas DL, Korbin PH, Winograd N 1984. Solids analysis using energetic ion bombardment and multiphoton resonance ionization with time-of-flight detection. Anal. Chem 56:2782–91
     [Google Scholar]
  111. 111.
    Tembreull R, Lubman DM. 1986. Pulsed laser desorption with resonant two-photon ionization detection in supersonic beam mass spectrometry. Anal. Chem 58:1299–303
     [Google Scholar]
  112. 112.
    Engelke F, Hahn JH, Henke W, Zare RN 1987. Determination of phenylthiohydantoin-amino acids by two-step laser desorption/multiphoton ionization. Anal. Chem 59:909–12
     [Google Scholar]
  113. 113.
    Köster C, Grotemeyer J. 1992. Single-photon and multi-photon ionization of infrared laser-desorbed biomolecules. Organ. Mass Spectrom 27:463–71
     [Google Scholar]
  114. 114.
    Akhmetov A, Moore JF, Gasper GL, Koin PJ, Hanley L 2010. Laser desorption postionization for imaging MS of biological material. J. Mass Spectrom 45:137–45
     [Google Scholar]
  115. 115.
    Hanley L, Zimmermann R. 2009. Light and molecular ions: the emergence of vacuum UV single-photon ionization in MS. Anal. Chem 81:4174–82
     [Google Scholar]
  116. 116.
    Grotemeyer J, Schlag EW. 1988. Multiphoton-ionization-mass spectrometry (MUPI-MS). Angew. Chem. Int. Ed 27:447–59
     [Google Scholar]
  117. 117.
    Zare RN. 1984. Laser chemical analysis. Science 226:298–303
     [Google Scholar]
  118. 118.
    Boesl U. 2000. Laser mass spectrometry for environmental and industrial chemical trace analysis. J. Mass Spectrom 35:289–304
     [Google Scholar]
  119. 119.
    Hanley L, Kornienko O, Ada ET, Fuoco E, Trevor JL 1999. Surface mass spectrometry of molecular species. J. Mass Spectrom 34:705–23
     [Google Scholar]
  120. 120.
    Lezius M, Blanchet V, Rayner DM, Villeneuve DM, Stolow A, Ivanov MY 2001. Nonadiabatic multielectron dynamics in strong field molecular ionization. Phys. Rev. Lett 86:51–54
     [Google Scholar]
  121. 121.
    Kucher A, Wucher A, Winograd N 2014. Strong field ionization of β-estradiol in the IR: strategies to optimize molecular postionization in secondary neutral mass spectrometry. J. Phys. Chem. C 118:25534–44
     [Google Scholar]
  122. 122.
    Huang Z, Ossenbrüggen T, Rubinsky I, Schust M, Horke DA, Küpper J 2018. Development and characterization of a laser-induced acoustic desorption source. Anal. Chem 90:3920–27
     [Google Scholar]
  123. 123.
    Cui Y, Bhardwaj C, Milasinovic S, Carlson RP, Gordon RJ, Hanley L 2013. Molecular imaging and depth profiling of biomaterials interfaces by femtosecond laser desorption postionization mass spectrometry. ACS Appl. Mater. Interfaces 5:9269–75
     [Google Scholar]
  124. 124.
    Soltwisch J, Kettling H, Vens-Cappell S, Wiegelmann M, Muthing J, Dreisewerd K 2015. Mass spectrometry imaging with laser-induced postionization. Science 348:211–15
     [Google Scholar]
  125. 125.
    Pelster A, Körsgen M, Kurosawa T, Morita H, Arlinghaus HF 2016. ToF-SIMS and laser-SNMS imaging of heterogeneous topographically complex polymer systems. Anal. Chem 88:9638–46
     [Google Scholar]
  126. 126.
    Heeger M, Tyler BJ, Körsgen M, Arlinghaus HF 2018. Laser postionization of neutral molecules sputtered using bismuth and argon cluster primary ions. Biointerphases 13:03B412
     [Google Scholar]
  127. 127.
    Finch JW, Toerne KA, Schram KH, Denton MB 2005. Evaluation of a hydrogen laser vacuum ultraviolet source for photoionization mass spectrometry of pharmaceuticals. Rapid Commun. Mass Spectrom 19:15–22
     [Google Scholar]
  128. 128.
    Adam T, Zimmermann R. 2007. Determination of single photon ionization cross sections for quantitative analysis of complex organic mixtures. Anal. Bioanal. Chem 389:1941–51
     [Google Scholar]
  129. 129.
    Edirisinghe PD, Moore JF, Calaway WF, Veryovkin IV, Pellin MJ, Hanley L 2006. Vacuum ultraviolet postionization of aromatic groups covalently bound to peptides. Anal. Chem 78:5876–83
     [Google Scholar]
  130. 130.
    Bari S, Gonzalez-Magaña O, Reitsma G, Werner J, Schippers S et al. 2011. Photodissociation of protonated leucine-enkephalin in the VUV range of 8–40 eV. J. Chem. Phys 134:024314
     [Google Scholar]
  131. 131.
    Schlathölter T, Reitsma G, Egorov D, Gonzalez-Magaña O, Bari S et al. 2016. Multiple ionization of free ubiquitin molecular ions in extreme ultraviolet free-electron laser pulses. Angew. Chem. Int. Ed 55:10741–45
     [Google Scholar]
  132. 132.
    Takahashi LK, Zhou J, Wilson KR, Leone SR, Ahmed M 2009. Imaging with mass spectrometry: a secondary ion and VUV-photoionization study of ion-sputtered atoms and clusters from GaAs and Au. J. Phys. Chem. A 113:4035–44
     [Google Scholar]
  133. 133.
    Gasper GL, Takahashi LK, Zhou J, Ahmed M, Moore JF, Hanley L 2010. Laser desorption postionization mass spectrometry of antibiotic-treated bacterial biofilms using tunable vacuum ultraviolet radiation. Anal. Chem 82:7472–78
     [Google Scholar]
  134. 134.
    Luo G, Marginean I, Vertes A 2002. Internal energy of ions generated by matrix-assisted laser desorption/ionization. Anal. Chem 74:6185–90
     [Google Scholar]
  135. 135.
    Zhou J, Takahashi LK, Wilson KR, Leone SR, Ahmed M 2010. Internal energies of ion-sputtered neutral tryptophan and thymine molecules determined by vacuum ultraviolet photoionization. Anal. Chem 82:3905–13
     [Google Scholar]
  136. 136.
    Nir E, Hunziker HE, de Vries MS 1999. Fragment-free mass spectrometric analysis with jet cooling/VUV photoionization. Anal. Chem 71:1674–78
     [Google Scholar]
  137. 137.
    Milasinovic S, Cui Y, Gordon RJ, Hanley L 2014. Internal energy of thermometer ions formed by femtosecond laser desorption: implications for mass spectrometric imaging. J. Phys. Chem. C 118:28938–47
     [Google Scholar]
  138. 138.
    Wahl M, Koch D, Berthold W, Wucher A 1995. Relative elemental sensitivity factors in non-resonant laser-SNMS. Fresenius' J. Anal. Chem 353:354–59
     [Google Scholar]
  139. 139.
    Jia L, Le Brech Y, Mauviel G, Qi F, Bente-von Frowein M et al. 2016. Online analysis of biomass pyrolysis tar by photoionization mass spectrometry. Energy Fuels 30:1555–63
     [Google Scholar]
  140. 140.
    Wu Q, Pomerantz AE, Mullins OC, Zare RN 2013. Minimization of fragmentation and aggregation by laser desorption laser ionization mass spectrometry. J. Am. Soc. Mass Spectrom 24:1116–22
     [Google Scholar]
  141. 141.
    Möllers R, Terhorst M, Niehuis E, Benninghoven A 1992. Resonant photoionization of sputtered organic molecules by femtosecond UV laser pulses. Org. Mass Spectrom 27:1393–95
     [Google Scholar]
  142. 142.
    Brummel CL, Willey KF, Vickerman JC, Winograd N 1995. Ion beam induced desorption with postionization using high repetition femtosecond lasers. Int. J. Mass Spectrom. Ion Process 143:257–70
     [Google Scholar]
  143. 143.
    Weinkauf R, Aicher P, Wesley G, Grotemeyer J, Schlag EW 1994. Femtosecond versus nanosecond multiphoton ionization and dissociation of large molecules. J. Phys. Chem 98:8381–91
     [Google Scholar]
  144. 144.
    Willey KF, Vorsa V, Braun RM, Winograd N 1998. Postionization of molecules desorbed from surfaces by keV ion bombardment with femtosecond laser pulses. Rapid Commun. Mass Spectrom 12:1253–60
     [Google Scholar]
  145. 145.
    Tian H, Sparvero LJ, Blenkinsopp P, Amoscato AA, Watkins SC et al. 2019. Secondary-ion mass spectrometry images cardiolipins and phosphatidylethanolamines at the subcellular level. Angew. Chem. Int. Ed. 58:3156–61
     [Google Scholar]
/content/journals/10.1146/annurev-anchem-061318-115516
Loading
Metabolic Imaging at the Single-Cell Scale: Recent Advances in Mass Spectrometry Imaging
Annual Review of Analytical Chemistry 12, 201 (2019); https://doi.org/10.1146/annurev-anchem-061318-115516
/content/journals/10.1146/annurev-anchem-061318-115516
/content/journals/10.1146/annurev-anchem-061318-115516
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error