Hierarchical Cluster and Region of Interest Analyses Based on Mass Spectrometry Imaging of Human Brain Tumours.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
01 04 2020
Historique:
received: 05 12 2019
accepted: 06 03 2020
entrez: 3 4 2020
pubmed: 3 4 2020
medline: 15 12 2020
Statut: epublish

Résumé

Imaging mass spectrometry (IMS) has been rarely used to examine specimens of human brain tumours. In the current study, high quality brain tumour samples were selected by tissue observation. Further, IMS analysis was combined with a new hierarchical cluster analysis (IMS-HCA) and region of interest analysis (IMS-ROI). IMS-HCA was successful in creating groups consisting of similar signal distribution images of glial fibrillary acidic protein (GFAP) and related multiple proteins in primary brain tumours. This clustering data suggested the relation of GFAP and these identified proteins in the brain tumorigenesis. Also, high levels of histone proteins, haemoglobin subunit α, tubulins, and GFAP were identified in a metastatic brain tumour using IMS-ROI. Our results show that IMS-HCA and IMS-ROI are promising techniques for identifying biomarkers using brain tumour samples.

Identifiants

pubmed: 32238824
doi: 10.1038/s41598-020-62176-8
pii: 10.1038/s41598-020-62176-8
pmc: PMC7113320
doi:

Substances chimiques

Biomarkers, Tumor 0
Peptides 0
Proteins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

5757

Références

Casadonte, R. & Caprioli, R. M. Proteomic analysis of formalin-fixed paraffin-embedded tissue by MALDI imaging mass spectrometry. Nat. Protoc. 6, 1695–1709, https://doi.org/10.1038/nprot.2011.388 (2011).
doi: 10.1038/nprot.2011.388 pubmed: 22011652 pmcid: 22011652
Kakimoto, Y. et al. Novel In Situ Pretreatment Method for Significantly Enhancing the Signal In MALDI-TOF MS of Formalin-Fixed Paraffin-Embedded Tissue Sections. PLoS One 7, e41607 (2012).
doi: 10.1371/journal.pone.0041607
Mittal, P. et al. Matrix Assisted Laser Desorption/Ionization Mass Spectrometry Imaging (MALDI MSI) for Monitoring of Drug Response in Primary Cancer Spheroids. Proteomics 19, e1900146, https://doi.org/10.1002/pmic.201900146 (2019).
doi: 10.1002/pmic.201900146 pubmed: 31474002 pmcid: 31474002
Ronci, M. et al. Protein unlocking procedures of formalin-fixed paraffin-embedded tissues: application to MALDI-TOF imaging MS investigations. Proteomics 8, 3702–3714, https://doi.org/10.1002/pmic.200701143 (2008).
doi: 10.1002/pmic.200701143 pubmed: 18704906 pmcid: 18704906
Gustafsson, J. O., Oehler, M. K., McColl, S. R. & Hoffmann, P. Citric acid antigen retrieval (CAAR) for tryptic peptide imaging directly on archived formalin-fixed paraffin-embedded tissue. J. Proteome Res. 9, 4315–4328, https://doi.org/10.1021/pr9011766 (2010).
doi: 10.1021/pr9011766 pubmed: 20597554 pmcid: 20597554
Bouschen, W., Schulz, O., Eikel, D. & Spengler, B. 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, 355–364, https://doi.org/10.1002/rcm.4401 (2010).
doi: 10.1002/rcm.4401 pubmed: 20049881 pmcid: 20049881
Yang, J. & Caprioli, R. M. Matrix sublimation/recrystallization for imaging proteins by mass spectrometry at high spatial resolution. Anal. Chem. 83, 5728–5734, https://doi.org/10.1021/ac200998a (2011).
doi: 10.1021/ac200998a pubmed: 21639088 pmcid: 21639088
Alberts, D. et al. MALDI Imaging-Guided Microproteomic Analyses of Heterogeneous Breast Tumors - A Pilot Study. Proteomics Clin Appl, https://doi.org/10.1002/prca.201700062 (2017).
Angel, P. M., Spraggins, J. M., Baldwin, H. S. & Caprioli, R. 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, https://doi.org/10.1021/ac202383m (2012).
doi: 10.1021/ac202383m pubmed: 22243218 pmcid: 22243218
El Ayed, M. et al. MALDI imaging mass spectrometry in ovarian cancer for tracking, identifying, and validating biomarkers. Med. Sci. Monit. 16, BR233–245 (2010).
pubmed: 20671603 pmcid: 20671603
Balluff, B. et al. Direct molecular tissue analysis by MALDI imaging mass spectrometry in the field of gastrointestinal disease. Gastroenterology 143, 544–549 e542, https://doi.org/10.1053/j.gastro.2012.07.022 (2012).
doi: 10.1053/j.gastro.2012.07.022 pubmed: 22820311 pmcid: 22820311
Yajima, Y. et al. Region of Interest analysis using mass spectrometry imaging of mitochondrial and sarcomeric proteins in acute cardiac infarction tissue. Sci. Rep. 8, 7493, https://doi.org/10.1038/s41598-018-25817-7 (2018).
doi: 10.1038/s41598-018-25817-7 pubmed: 29748547 pmcid: 29748547
Kakimoto, Y. et al. Sorbin and SH3 domain-containing protein 2 is released from infarcted heart in the very early phase: proteomic analysis of cardiac tissues from patients. J. Am. Heart Assoc. 2, e000565, https://doi.org/10.1161/JAHA.113.000565 (2013).
doi: 10.1161/JAHA.113.000565 pubmed: 24342996 pmcid: 24342996
Tsuruyama, T. & K. Y. Forensic Diagnosis of Acute Myocardial Infarction: Application of Mass Spectrometry. Int. J. Forensic Sci. Pathol. 2, 1–5 (2014).
Taverna, D., Pollins, A. C., Nanney, L. B., Sindona, G. & Caprioli, R. M. Histology-guided protein digestion/extraction from formalin-fixed and paraffin-embedded pressure ulcer biopsies. Exp. Dermatol. 25, 143–146, https://doi.org/10.1111/exd.12870 (2016).
doi: 10.1111/exd.12870 pubmed: 26440596 pmcid: 26440596
Judd, A. M. et al. A recommended and verified procedure for in situ tryptic digestion of formalin-fixed paraffin-embedded tissues for analysis by matrix-assisted laser desorption/ionization imaging mass spectrometry. J. Mass. Spectrom. 54, 716–727, https://doi.org/10.1002/jms.4384 (2019).
doi: 10.1002/jms.4384 pubmed: 31254303 pmcid: 31254303
Boskamp, T. et al. A new classification method for MALDI imaging mass spectrometry data acquired on formalin-fixed paraffin-embedded tissue samples. Biochim. Biophys. Acta 1865, 916–926, https://doi.org/10.1016/j.bbapap.2016.11.003 (2017).
doi: 10.1016/j.bbapap.2016.11.003
Wildburger, N. C. et al. ESI-MS/MS and MALDI-IMS Localization Reveal Alterations in Phosphatidic Acid, Diacylglycerol, and DHA in Glioma Stem Cell Xenografts. J. Proteome Res. 14, 2511–2519, https://doi.org/10.1021/acs.jproteome.5b00076 (2015).
doi: 10.1021/acs.jproteome.5b00076 pubmed: 25880480 pmcid: 25880480
Angel, P. M. et al. Mapping Extracellular Matrix Proteins in Formalin-Fixed, Paraffin-Embedded Tissues by MALDI Imaging Mass Spectrometry. J. Proteome Res. 17, 635–646, https://doi.org/10.1021/acs.jproteome.7b00713 (2018).
doi: 10.1021/acs.jproteome.7b00713 pubmed: 29161047 pmcid: 29161047
Omuro, A. & DeAngelis, L. M. Glioblastoma and other malignant gliomas: a clinical review. JAMA 310, 1842–1850, https://doi.org/10.1001/jama.2013.280319 (2013).
doi: 10.1001/jama.2013.280319 pubmed: 24193082 pmcid: 24193082
Sulman, E. P., Ismaila, N. & Chang, S. M. Radiation Therapy for Glioblastoma: American Society of Clinical Oncology Clinical Practice Guideline Endorsement of the American Society for Radiation Oncology Guideline. J. Oncol. Pract. 13, 123–127, https://doi.org/10.1200/JOP.2016.018937 (2017).
doi: 10.1200/JOP.2016.018937 pubmed: 27907278 pmcid: 27907278
Hanif, F., Muzaffar, K., Perveen, K. & Malhi, S. M. & Simjee Sh, U. Glioblastoma Multiforme: A Review of its Epidemiology and Pathogenesis through Clinical Presentation and Treatment. Asian Pac. J. Cancer Prev. 18, 3–9, https://doi.org/10.22034/APJCP.2017.18.1.3 (2017).
doi: 10.22034/APJCP.2017.18.1.3 pubmed: 28239999 pmcid: 28239999
Alifieris, C. & Trafalis, D. T. Glioblastoma multiforme: Pathogenesis and treatment. Pharmacol. Ther. 152, 63–82, https://doi.org/10.1016/j.pharmthera.2015.05.005 (2015).
doi: 10.1016/j.pharmthera.2015.05.005 pubmed: 25944528 pmcid: 25944528
Kim, D. W. et al. Brigatinib in Patients With Crizotinib-Refractory Anaplastic Lymphoma Kinase-Positive Non-Small-Cell Lung Cancer: A Randomized, Multicenter Phase II Trial. J. Clin. Oncol. 35, 2490–2498, https://doi.org/10.1200/JCO.2016.71.5904 (2017).
doi: 10.1200/JCO.2016.71.5904 pubmed: 28475456 pmcid: 28475456
Beine, B., Diehl, H. C., Meyer, H. E. & Henkel, C. Tissue MALDI Mass Spectrometry Imaging (MALDI MSI) of Peptides. Methods Mol. Biol. 1394, 129–150, https://doi.org/10.1007/978-1-4939-3341-9_10 (2016).
doi: 10.1007/978-1-4939-3341-9_10 pubmed: 26700046 pmcid: 26700046
Bag, A. K. et al. Connecting signaling and metabolic pathways in EGF receptor-mediated oncogenesis of glioblastoma. PLoS Comput. Biol. 15, e1007090, https://doi.org/10.1371/journal.pcbi.1007090 (2019).
doi: 10.1371/journal.pcbi.1007090 pubmed: 31386654 pmcid: 31386654
Gyuris, A. et al. Physical and Molecular Landscapes of Mouse Glioma Extracellular Vesicles Define Heterogeneity. Cell Rep. 27, 3972–3987 e3976, https://doi.org/10.1016/j.celrep.2019.05.089 (2019).
doi: 10.1016/j.celrep.2019.05.089 pubmed: 31242427 pmcid: 31242427
Ait-Belkacem, R. et al. MALDI imaging and in-source decay for top-down characterization of glioblastoma. Proteomics 14, 1290–1301, https://doi.org/10.1002/pmic.201300329 (2014).
doi: 10.1002/pmic.201300329 pubmed: 24376047 pmcid: 24376047
Dilillo, M. et al. Ultra-High Mass Resolution MALDI Imaging Mass Spectrometry of Proteins and Metabolites in a Mouse Model of Glioblastoma. Sci. Rep. 7, 603, https://doi.org/10.1038/s41598-017-00703-w (2017).
doi: 10.1038/s41598-017-00703-w pubmed: 28377615 pmcid: 28377615
Kaya, I. et al. Histology-Compatible MALDI Mass Spectrometry Based Imaging of Neuronal Lipids for Subsequent Immunofluorescent Staining. Anal. Chem. 89, 4685–4694, https://doi.org/10.1021/acs.analchem.7b00313 (2017).
doi: 10.1021/acs.analchem.7b00313 pubmed: 28318232 pmcid: 28318232
Ellis, S. R., Soltwisch, J., Paine, M. R. L., Dreisewerd, K. & Heeren, R. M. A. Laser post-ionisation combined with a high resolving power orbitrap mass spectrometer for enhanced MALDI-MS imaging of lipids. Chem. Commun. 53, 7246–7249, https://doi.org/10.1039/c7cc02325a (2017).
doi: 10.1039/c7cc02325a
Aichler, M. & Walch, A. MALDI Imaging mass spectrometry: current frontiers and perspectives in pathology research and practice. Lab. Invest. 95, 422–431, https://doi.org/10.1038/labinvest.2014.156 (2015).
doi: 10.1038/labinvest.2014.156 pubmed: 25621874 pmcid: 25621874
Baluya, D. L., Garrett, T. J. & Yost, R. A. Automated MALDI matrix deposition method with inkjet printing for imaging mass spectrometry. Anal. Chem. 79, 6862–6867, https://doi.org/10.1021/ac070958d (2007).
doi: 10.1021/ac070958d pubmed: 17658766 pmcid: 17658766
Batubara, A. et al. Thin-layer chromatography/matrix-assisted laser desorption/ionisation mass spectrometry and matrix-assisted laser desorption/ionisation mass spectrometry imaging for the analysis of phospholipids in LS174T colorectal adenocarcinoma xenografts treated with the vascular disrupting agent DMXAA. Rapid Commun. Mass. Spectrom. 29, 1288–1296, https://doi.org/10.1002/rcm.7223 (2015).
doi: 10.1002/rcm.7223 pubmed: 26405790 pmcid: 26405790

Auteurs

Takuya Hiratsuka (T)

Department of Drug and Discovery Medicine, Pathology Division, Kyoto University Graduate School of Medicine, Kyoto, 606-8501, Japan.

Yoshiki Arakawa (Y)

Department of Neural Surgery, Kyoto University Hospital, Kyoto, 606-8507, Japan.

Yuka Yajima (Y)

Department of Microbiology, Muroran Institute of Technology, Muroran, Hokkaido, 050-8585, Japan.

Yu Kakimoto (Y)

Department of Forensic Medicine, Graduate School of Medicine, Tokai University School of Medicine, Isehara-Shimokasuya 143, Kanagawa, 259-1193, Japan.

Keisuke Shima (K)

Kyoto Applications Development Center, Analytical & Measuring Instruments Division, Shimadzu Corporation, 1 Nishino-kyo-Kuwabara-cho, Kyoto, 604-8511, Japan.

Yuzo Yamazaki (Y)

Kyoto Applications Development Center, Analytical & Measuring Instruments Division, Shimadzu Corporation, 1 Nishino-kyo-Kuwabara-cho, Kyoto, 604-8511, Japan.

Masahiro Ikegami (M)

Kyoto Applications Development Center, Analytical & Measuring Instruments Division, Shimadzu Corporation, 1 Nishino-kyo-Kuwabara-cho, Kyoto, 604-8511, Japan.

Takushi Yamamoto (T)

Kyoto Applications Development Center, Analytical & Measuring Instruments Division, Shimadzu Corporation, 1 Nishino-kyo-Kuwabara-cho, Kyoto, 604-8511, Japan.

Hideshi Fujiwake (H)

Research Center, Shimadzu General Services, Inc., 1 Nishino-kyo-Kuwabara-cho, Kyoto, 604-8511, Japan.

Koichi Fujimoto (K)

Department of Neural Surgery, Kyoto University Hospital, Kyoto, 606-8507, Japan.

Norishige Yamada (N)

Clinical bioresource centre, Kyoto University Hospital, Kyoto, 606-8507, Japan.

Tatsuaki Tsuruyama (T)

Department of Drug and Discovery Medicine, Pathology Division, Kyoto University Graduate School of Medicine, Kyoto, 606-8501, Japan. tsuruyam@kuhp.kyoto-u.ac.jp.
Clinical bioresource centre, Kyoto University Hospital, Kyoto, 606-8507, Japan. tsuruyam@kuhp.kyoto-u.ac.jp.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH