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Exploring Three-Dimensional Matrix-Assisted Laser Desorption/Ionization Imaging Mass Spectrometry Data: Three-Dimensional Spatial Segmentation of Mouse Kidney

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Steinbeis Innovation Center for Scientific Computing in Life Sciences, Bremen, Germany
Center for Industrial Mathematics, University of Bremen, Bremen, Germany
§ Bruker Daltonik GmbH, Bremen, Germany
Fraunhofer MEVIS, Institute for Medical Image Computing, Bremen, Germany
Research Unit Analytical Pathology, Institute of Pathology, Helmholtz Center Munich, Munich, Germany
MALDI Imaging Lab, University of Bremen, Bremen, Germany
*E-mail: [email protected] (P.M.); [email protected] (T.A.). Phone: +49 (0)421 21863820. Fax: +49 (0)421 218 98 63820.
Cite this: Anal. Chem. 2012, 84, 14, 6079–6087
Publication Date (Web):June 20, 2012
https://doi.org/10.1021/ac300673y
Copyright © 2012 American Chemical Society

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    Abstract

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    Three-dimensional (3D) imaging has a significant impact on many challenges of life sciences. Three-dimensional matrix-assisted laser desorption/ionization imaging mass spectrometry (MALDI-IMS) is an emerging label-free bioanalytical technique capturing the spatial distribution of hundreds of molecular compounds in 3D by providing a MALDI mass spectrum for each spatial point of a 3D sample. Currently, 3D MALDI-IMS cannot tap its full potential due to the lack efficient computational methods for constructing, processing, and visualizing large and complex 3D MALDI-IMS data. We present a new pipeline of efficient computational methods, which enables analysis and interpretation of a 3D MALDI-IMS data set. Construction of a MALDI-IMS data set was done according to the state-of-the-art protocols and involved sample preparation, spectra acquisition, spectra preprocessing, and registration of serial sections. For analysis and interpretation of 3D MALDI-IMS data, we applied the spatial segmentation approach which is well-accepted in analysis of two-dimensional (2D) MALDI-IMS data. In line with 2D data analysis, we used edge-preserving 3D image denoising prior to segmentation to reduce strong and chaotic spectrum-to-spectrum variation. For segmentation, we used an efficient clustering method, called bisecting k-means, which is optimized for hierarchical clustering of a large 3D MALDI-IMS data set. Using the proposed pipeline, we analyzed a central part of a mouse kidney using 33 serial sections of 3.5 μm thickness after the PAXgene tissue fixation and paraffin embedding. For each serial section, a 2D MALDI-IMS data set was acquired following the standard protocols with the high spatial resolution of 50 μm. Altogether, 512 495 mass spectra were acquired that corresponds to approximately 50 gigabytes of data. After registration of serial sections into a 3D data set, our computational pipeline allowed us to reveal the 3D kidney anatomical structure based on mass spectrometry data only. Finally, automated analysis discovered molecular masses colocalized with major anatomical regions. In the same way, the proposed pipeline can be used for analysis and interpretation of any 3D MALDI-IMS data set in particular of pathological cases.

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    60. Bindesh Shrestha. Data analysis and computation for imaging mass spectrometry. 2021, 129-146. https://doi.org/10.1016/B978-0-12-818998-6.00009-7
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    65. Theodore Alexandrov. Spatial Metabolomics and Imaging Mass Spectrometry in the Age of Artificial Intelligence. Annual Review of Biomedical Data Science 2020, 3 (1) , 61-87. https://doi.org/10.1146/annurev-biodatasci-011420-031537
    66. Nico Verbeeck, Richard M. Caprioli, Raf Van de Plas. Unsupervised machine learning for exploratory data analysis in imaging mass spectrometry. Mass Spectrometry Reviews 2020, 39 (3) , 245-291. https://doi.org/10.1002/mas.21602
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    71. S. Mas, A. Torro, N. Bec, L. Fernández, G. Erschov, C. Gongora, C. Larroque, P. Martineau, A. de Juan, S. Marco. Use of physiological information based on grayscale images to improve mass spectrometry imaging data analysis from biological tissues. Analytica Chimica Acta 2019, 1074 , 69-79. https://doi.org/10.1016/j.aca.2019.04.074
    72. Jiaying Han, Hjalmar Permentier, Rainer Bischoff, Geny Groothuis, Angela Casini, Péter Horvatovich. Imaging of protein distribution in tissues using mass spectrometry: An interdisciplinary challenge. TrAC Trends in Analytical Chemistry 2019, 112 , 13-28. https://doi.org/10.1016/j.trac.2018.12.016
    73. Alice Ly, Rémi Longuespée, Rita Casadonte, Petra Wandernoth, Kristina Schwamborn, Christine Bollwein, Christian Marsching, Katharina Kriegsmann, Carsten Hopf, Wilko Weichert, Jörg Kriegsmann, Peter Schirmacher, Mark Kriegsmann, Sören‐Oliver Deininger. Site‐to‐Site Reproducibility and Spatial Resolution in MALDI–MSI of Peptides from Formalin‐Fixed Paraffin‐Embedded Samples. PROTEOMICS – Clinical Applications 2019, 13 (1) https://doi.org/10.1002/prca.201800029
    74. Mathieu Fanuel, David Ropartz, Fabienne Guillon, Luc Saulnier, Hélène Rogniaux. Distribution of cell wall hemicelluloses in the wheat grain endosperm: a 3D perspective. Planta 2018, 248 (6) , 1505-1513. https://doi.org/10.1007/s00425-018-2980-0
    75. Xiang Tian, Genwei Zhang, Yihan Shao, Zhibo Yang. Towards enhanced metabolomic data analysis of mass spectrometry image: Multivariate Curve Resolution and Machine Learning. Analytica Chimica Acta 2018, 1037 , 211-219. https://doi.org/10.1016/j.aca.2018.02.031
    76. Oliver Klein, Kristin Strohschein, Grit Nebrich, Michael Fuchs, Herbert Thiele, Patrick Giavalisco, Georg N. Duda, Tobias Winkler, Jan Hendrik Kobarg, Dennis Trede, Sven Geissler. Unraveling local tissue changes within severely injured skeletal muscles in response to MSC-based intervention using MALDI Imaging mass spectrometry. Scientific Reports 2018, 8 (1) https://doi.org/10.1038/s41598-018-30990-w
    77. Jusal Quanico, Lena Hauberg-Lotte, Stephanie Devaux, Zahra Laouby, Celine Meriaux, Antonella Raffo-Romero, Melanie Rose, Leia Westerheide, Jost Vehmeyer, Franck Rodet, Peter Maass, Dasa Cizkova, Norbert Zilka, Veronika Cubinkova, Isabelle Fournier, Michel Salzet. 3D MALDI mass spectrometry imaging reveals specific localization of long-chain acylcarnitines within a 10-day time window of spinal cord injury. Scientific Reports 2018, 8 (1) https://doi.org/10.1038/s41598-018-34518-0
    78. Pere Ràfols, Dídac Vilalta, Jesús Brezmes, Nicolau Cañellas, Esteban del Castillo, Oscar Yanes, Noelia Ramírez, Xavier Correig. Signal preprocessing, multivariate analysis and software tools for MA(LDI)‐TOF mass spectrometry imaging for biological applications. Mass Spectrometry Reviews 2018, 37 (3) , 281-306. https://doi.org/10.1002/mas.21527
    79. Yu-Chuan Lin, Yeukuang Hwu, Guo-Shu Huang, Michael Hsiao, Tsung-Tse Lee, Shun-Min Yang, Ting-Kuo Lee, Nan-Yow Chen, Sung-Sen Yang, Ann Chen, Shuk-Man Ka. Differential synchrotron X-ray imaging markers based on the renal microvasculature for tubulointerstitial lesions and glomerulopathy. Scientific Reports 2017, 7 (1) https://doi.org/10.1038/s41598-017-03677-x
    80. Judith M. Lotz, Franziska Hoffmann, Johannes Lotz, Stefan Heldmann, Dennis Trede, Janina Oetjen, Michael Becker, Günther Ernst, Peter Maas, Theodore Alexandrov, Orlando Guntinas-Lichius, Herbert Thiele, Ferdinand von Eggeling. Integration of 3D multimodal imaging data of a head and neck cancer and advanced feature recognition. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics 2017, 1865 (7) , 946-956. https://doi.org/10.1016/j.bbapap.2016.08.018
    81. Peggi M. Angel, H. Scott Baldwin, Danielle Gottlieb Sen, Yan Ru Su, John E. Mayer, David Bichell, Richard R. Drake. Advances in MALDI imaging mass spectrometry of proteins in cardiac tissue, including the heart valve. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics 2017, 1865 (7) , 927-935. https://doi.org/10.1016/j.bbapap.2017.03.009
    82. J.L. Norris, D.B. Gutierrez, R.M. Caprioli. Imaging Mass Spectrometry in Clinical Pathology. 2017, 517-529. https://doi.org/10.1016/B978-0-12-800886-7.00040-6
    83. S. Giordano, L. Morosi, P. Veglianese, S. A. Licandro, R. Frapolli, M. Zucchetti, G. Cappelletti, L. Falciola, V. Pifferi, S. Visentin, M. D’Incalci, E. Davoli. 3D Mass Spectrometry Imaging Reveals a Very Heterogeneous Drug Distribution in Tumors. Scientific Reports 2016, 6 (1) https://doi.org/10.1038/srep37027
    84. Jody C. May, John A. McLean. Advanced Multidimensional Separations in Mass Spectrometry: Navigating the Big Data Deluge. Annual Review of Analytical Chemistry 2016, 9 (1) , 387-409. https://doi.org/10.1146/annurev-anchem-071015-041734
    85. Monika Pietrowska, Marta Gawin, Joanna Polańska, Piotr Widłak. Tissue fixed with formalin and processed without paraffin embedding is suitable for imaging of both peptides and lipids by MALDI‐IMS. PROTEOMICS 2016, 16 (11-12) , 1670-1677. https://doi.org/10.1002/pmic.201500424
    86. Nathan H. Patterson, Robert J. Doonan, Stella S. Daskalopoulou, Martin Dufresne, Sébastien Lenglet, Fabrizio Montecucco, Aurélien Thomas, Pierre Chaurand. Three‐dimensional imaging MS of lipids in atherosclerotic plaques: Open‐source methods for reconstruction and analysis. PROTEOMICS 2016, 16 (11-12) , 1642-1651. https://doi.org/10.1002/pmic.201500490
    87. Jin Woo Jung, Mi Suk Lee, Hyo-Jung Choi, Sunhee Jung, Yu-Jung Lee, Geum-Sook Hwang, Tae-Hwan Kwon. Mass spectrometric imaging of metabolites in kidney tissues from rats treated with furosemide. American Journal of Physiology-Renal Physiology 2016, 310 (11) , F1317-F1327. https://doi.org/10.1152/ajprenal.00524.2015
    88. Roseli F. Gonçalves, Mónica S. Ferreira, Diogo N. de Oliveira, Rafael Canevarolo, Marcos A. Achilles, Daniela L. D'Ercole, Peter E. Bols, Jose A. Visintin, Gary J. Killian, Rodrigo R. Catharino. Analysis and characterisation of bovine oocyte and embryo biomarkers by matrix-assisted desorption ionisation mass spectrometry imaging. Reproduction, Fertility and Development 2016, 28 (3) , 293. https://doi.org/10.1071/RD14047
    89. Chunxu Song, Mark Mazzola, Xu Cheng, Janina Oetjen, Theodore Alexandrov, Pieter Dorrestein, Jeramie Watrous, Menno van der Voort, Jos M. Raaijmakers. Molecular and chemical dialogues in bacteria-protozoa interactions. Scientific Reports 2015, 5 (1) https://doi.org/10.1038/srep12837
    90. Nobuhiro Zaima, Naoko Goto‐Inoue, Takahiro Hayasaka. MALDI Mass Spectrometry Imaging of Biological Structures. 2015, 1-20. https://doi.org/10.1002/9780470027318.a9417
    91. Ludovic Muller, Ajay Kailas, Shelley N. Jackson, Aurelie Roux, Damon C. Barbacci, J. Albert Schultz, Carey D. Balaban, Amina S. Woods. Lipid imaging within the normal rat kidney using silver nanoparticles by matrix-assisted laser desorption/ionization mass spectrometry. Kidney International 2015, 88 (1) , 186-192. https://doi.org/10.1038/ki.2015.3
    92. Andrew Palmer, Ekaterina Ovchinnikova, Mikael Thuné, Régis Lavigne, Blandine Guével, Andrey Dyatlov, Olga Vitek, Charles Pineau, Mats Borén, Theodore Alexandrov. Using collective expert judgements to evaluate quality measures of mass spectrometry images. Bioinformatics 2015, 31 (12) , i375-i384. https://doi.org/10.1093/bioinformatics/btv266
    93. Ingela Lanekoff, Kristin Burnum-Johnson, Mathew Thomas, Jeeyeon Cha, Sudhansu K. Dey, Pengxiang Yang, Maria C. Prieto Conaway, Julia Laskin. Three-dimensional imaging of lipids and metabolites in tissues by nanospray desorption electrospray ionization mass spectrometry. Analytical and Bioanalytical Chemistry 2015, 407 (8) , 2063-2071. https://doi.org/10.1007/s00216-014-8174-0
    94. Mark T. Bokhart, Elias Rosen, Corbin Thompson, Craig Sykes, Angela D. M. Kashuba, David C. Muddiman. Quantitative mass spectrometry imaging of emtricitabine in cervical tissue model using infrared matrix-assisted laser desorption electrospray ionization. Analytical and Bioanalytical Chemistry 2015, 407 (8) , 2073-2084. https://doi.org/10.1007/s00216-014-8220-y
    95. Ove J. R. Gustafsson, Matthew T. Briggs, Mark R. Condina, Lyron J. Winderbaum, Matthias Pelzing, Shaun R. McColl, Arun V. Everest-Dass, Nicolle H. Packer, Peter Hoffmann. MALDI imaging mass spectrometry of N-linked glycans on formalin-fixed paraffin-embedded murine kidney. Analytical and Bioanalytical Chemistry 2015, 407 (8) , 2127-2139. https://doi.org/10.1007/s00216-014-8293-7
    96. Gwendolyn Barceló-Coblijn, José A. Fernández. Mass spectrometry coupled to imaging techniques: the better the view the greater the challenge. Frontiers in Physiology 2015, 6 https://doi.org/10.3389/fphys.2015.00003
    97. Veronica Mainini, Maciej Lalowski, Athanasios Gotsopoulos, Vasiliki Bitsika, Marc Baumann, Fulvio Magni. MALDI-Imaging Mass Spectrometry on Tissues. 2015, 139-164. https://doi.org/10.1007/978-1-4939-1872-0_8
    98. Eric M. Weaver, Amanda B. Hummon, Richard B. Keithley. Chemometric analysis of MALDI mass spectrometric images of three-dimensional cell culture systems. Analytical Methods 2015, 7 (17) , 7208-7219. https://doi.org/10.1039/C5AY00293A
    99. Oliver Klein, Kristin Strohschein, Grit Nebrich, Janina Oetjen, Dennis Trede, Herbert Thiele, Theodore Alexandrov, Patrick Giavalisco, Georg N. Duda, Philipp von Roth, Sven Geissler, Joachim Klose, Tobias Winkler. MALDI imaging mass spectrometry: Discrimination of pathophysiological regions in traumatized skeletal muscle by characteristic peptide signatures. PROTEOMICS 2014, 14 (20) , 2249-2260. https://doi.org/10.1002/pmic.201400088
    100. Anna de Juan, Sara Piqueras, Marcel Maeder, Thomas Hancewicz, Ludovic Duponchel, Romà Tauler. Chemometric Tools for Image Analysis. 2014, 57-110. https://doi.org/10.1002/9783527678136.ch2
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