Imaging mass spectrometry-based molecular histology differentiates microscopically identical and heterogeneous tumors

Journal of Proteome Research

Volumn 12, Issue 4, 2013, Pages 1847-1855

  Jones, Emrys A ^a   Schmitz, Nicole ^a   Waaijer, Cathelijn J F ^a   Frese, Christian K ^b,c   Van Remoortere, Alexandra ^a   Van Zeijl, René J M ^a   Heck, Albert J R ^b,c   Hogendoorn, Pancras C W ^a   Deelder, André M ^a   Altelaar, A F Maarten ^b,c   Bovée, Judith V M G ^a   McDonnell, Liam A ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c NETHERLANDS PROTEOMICS CENTRE   (Netherlands)

Author keywords

chondrosarcoma; imaging mass spectrometry; intratumor heterogeneity; MALDI; molecular histology

Indexed keywords

BIOLOGICAL MARKER; PEPTIDES AND PROTEINS;

ARTICLE; BONE TUMOR; CELL HETEROGENEITY; CELL STRUCTURE; CHONDROSARCOMA; HISTOLOGY; HUMAN; HUMAN TISSUE; IMAGE ANALYSIS; MASS SPECTROMETRY; MOLECULAR IMAGING; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR CELL;

AMINO ACID SEQUENCE; BONE NEOPLASMS; CHONDROSARCOMA; HUMANS; MOLECULAR IMAGING; MOLECULAR SEQUENCE DATA; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TANDEM MASS SPECTROMETRY;

EID: 84875934361     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr301190g     Document Type: Article

References (45)

1. Schwamborn, K.; Caprioli, R. M. Molecular imaging by mass spectrometry-looking beyond classical histology Nat. Rev. Cancer 2010, 10, 639-646
2. Rubakhin, S. S.; Sweedler, J. V. A mass spectrometry primer for mass spectrometry imaging Methods Mol. Biol. 2010, 656, 21-49
3. Chughtai, K.; Heeren, R. M. A. Mass spectrometric imaging for biomedical tissue analysis Chem. Rev. 2010, 110, 3237-3277
4. Eberlin, L. S.; Norton, I.; Dill, A. L.; Golby, A. J.; Ligon, K. L.; Santagata, S.; Cooks, R. G.; Agar, N. Y. R. Classifying human brain tumors by lipid imaging with mass spectrometry Cancer Res. 2012, 72, 645-654
5. McDonnell, L. A.; Willems, S. M.; Corthals, G. L.; van Remoortere, A.; van Zeijl, R. J. M.; Deelder, A. M. Imaging mass spectrometry in cancer research: past experiences and future possibilities J. Proteomics 2010, 73, 1921-1944
6. Balluff, B.; Rauser, S.; Meding, S.; Elsner, M.; Schoene, C.; Feuchtinger, A.; Schuhmacher, C.; Novotny, A.; Juetting, U.; Maccarrone, G.; Sarioglu, H.; Ueffing, M.; Braselmann, H.; Zitzelsberger, H.; Schmid, R. M.; Hoefler, H.; Ebert, M. P.; Walch, A. MALDI imaging identifies prognostic seven-protein signature of novel tissue markers in intestinal-type gastric cancer Am. J. Pathol. 2011, 179, 2720-2729
7. Reyzer, M. L.; Caldwell, R. L.; Dugger, T. C.; Forbes, J. T.; Ritter, C. A.; Guix, M.; Arteaga, C. L.; Caprioli, R. M. Early changes in protein expression detected by mass spectrometry predict tumor response to molecular therapeutics Cancer Res. 2004, 64 (24) 9093-9100
8. Meding, S.; Nitsche, U.; Balluff, B.; Elsner, M.; Rauser, S.; Schöne, C.; Nipp, M.; Maak, M.; Feith, M.; Ebert, M. P.; Friess, H.; Langer, R.; Höfler, H.; Zitzelsberger, H.; Rosenberg, R.; Walch, A. Tumor classification of six common cancer types based on proteomic profiling by MALDI imaging J. Proteome Res. 2012, 11, 1996-2003
9. Willems, S. M.; van Remoortere, A.; van Zeijl, R.; Deelder, A. M.; McDonnell, L. A.; Hogendoorn, P. C. W. Imaging mass spectrometry of myxoid sarcomas identifies proteins and lipids specific to tumor type and grade, and reveals biochemical intratumor heterogeneity J. Pathol. 2010, 222, 400-409
10. Jones, E. A.; Dieninger, S.-O.; Hogendoorn, P. C. W.; Deelder, A. M.; McDonnell, L. A. Imaging mass spectrometry statistical analysis J. Proteomics 2012, 75, 4962-4989
11. Jones, E. A.; van Remoortere, A.; van Zeijl, R. J. M.; Hogendoorn, P. C. W.; Boveé, J. V. M. G.; Deelder, A. M.; McDonnell, L. A. Multiple statistical analysis techniques corroborate intratumor heterogeneity in imaging mass spectrometry datasets of myxofibrosarcoma PLoS ONE 2011, 6, e24913
12. Gerlinger, M.; Rowan, A. J.; Horswell, S.; Larkin, J.; Endesfelder, D.; Gronroos, E.; Martinez, P.; Matthews, N.; Stewart, A.; Tarpey, P.; Varela, I.; Phillimore, B.; Begum, S.; McDonald, N. Q.; Butler, A.; Jones, D.; Raine, K.; Latimer, C.; Santos, C. R.; Nohadani, M.; Eklund, A. C.; Spencer-Dene, B.; Clark, G.; Pickering, L.; Stamp, G.; Gore, M.; Szallasi, Z.; Downward, J.; Futreal, P. A.; Swanton, C. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing New England Journal of Medicine 2012, 366 (10) 883-892
13. Swanton, C. Intratumor heterogeneity: evolution through space and time Cancer Res. 2012, 72, 4875-4882
14. Amstalden van Hove, E. R.; Blackwell, T. R.; Klinkert, I.; Eijkel, G. B.; Heeren, R. M. A.; Glunde, K. Multimodal mass spectrometric imaging of small molecules reveals distinct spatio-molecular signatures in differentially metastatic breast tumor models Cancer Res. 2010, 70 (13) 9012-9021
15. Bertoni, F.; Bacchini, P.; Hogendoorn, P. C. W. Chondrosarcoma. In World Health Organization classification of tumours; Fletcher, C.; Unni, K.; Mertens, F., Eds.; IARC Press: Lyon, 2002; pp 247-251.
16. Bovée, J. V. M. G.; Hogendoorn, P. C. W.; Wunder, J. S.; Almin, B. A. Cartilage Tumors and Bone Development: Molecular Pathology and Possible Therapeutic targets Nat. Rev. Cancer 2010, 10, 481-488
17. de Andrea, C. E.; Reijnders, C. M. A.; Kroon, H. M.; de Jong, D.; Hogendoorn, P. C. W.; Szuhai, K.; Bovée, J. V. M. G. Secondary peripheral chondrosarcoma evolving from osteochondroma as a result of outgrowth of cells with functional EXT Oncogene 2011, 31, 1095-1104
18. Pansuriya, T. C.; van Eijk, R.; d'Adamo, P.; van Ruler, M.; Kuijjer, M. L.; Oosting, J.; Cleton-Jansen, A. M.; van Oosterwijk, J. G.; Verbeke, S. L. J.; Meijer, D.; van Wezel, T.; Nord, K. H.; Sangiorgi, L.; Toker, B.; Liegl-Atzwanger, B.; San-Julian, M.; Sciot, R.; Limaye, N.; Kindblom, L. G.; Daugaard, S.; Godfraind, C.; Boon, L. M.; Vikkula, M.; Kurek, K. C.; Szuhai, K.; French, P. J.; Bovee, J. Somatic mosaic IDH1 and IDH2 mutations are associated with enchondroma and spindle cell hemangioma in Ollier disease and Maffucci syndrome Nat. Genet. 2011, 43 (12) 1256-U124
19. Boeuf, S.; Bovée, J. V. M. G.; Lehner, B.; Hogendoorn, P. C. W.; Richter, W. Correlation of hypoxic signalling to histological grade and outcome in cartilage tumors Histopathology 2010, 56, 641-651
20. World Health Organization Cartilage Tumours; IARC Press: Lyon, 2002; pp 234-257.
21. Schwartz, S. A.; Reyzer, M. L.; Caprioli, R. M. Direct tissue analysis using matrix-assisted laser desorption/ionization mass spectrometry: practical aspects of sample preparation J. Mass Spectrom. 2003, 38, 699-708
22. Schwamborn, K.; Krieg, R. C.; Reska, M.; Jakse, G.; Knuechel, R.; Wellmann, A. Identifying prostate carcinoma by MALDI-imaging Int. J. Mol. Med. 2007, 20 (2) 155-159
23. McDonnell, L. A.; van Remoortere, A.; de Velde, N.; van Zeijl, R. J. M.; Deelder, A. Imaging mass spectrometry data reduction: automated feature identification and extraction J. Am. Soc. Mass Spectrom. 2010, 21, 1969-1978
24. Lee, D. D.; Seung, H. S. Learning the parts of objects by non-negative matrix factorization Nature 1999, 401, 788-791
25. Hanselmann, M.; Kirchner, M.; Renard, B. Y.; Amstalden, E. R.; Glunde, K.; Heeren, R. M. A.; Hamprecht, F. A. Concise representation of mass spectrometry images by probabilistic latent semantic analysis Anal. Chem. 2008, 80 (24) 9649-9658
26. Frese, C. K.; Altelaar, A. F. M.; Hennrich, M. L.; Nolting, D.; Zeller, M.; Griep-Raming, J.; Heck, A. J. R.; Mohammed, S. Improved peptide identification by targeted fragmentation using CID, HCD and ETD on an LTQ-Orbitrap velos J. Proteome Res. 2011, 10 (5) 2377-2388
27. Savitski, M. M.; Mathieson, T.; Becher, I.; Bantscheff, M. H-Score, a mass accuracy driven rescoring approach for improved peptide identification in modification rich samples J. Proteome Res. 2010, 9 (11) 5511-5516
28. van der Toorn, H. W. P.; Muñoz, J.; Mohammed, S.; Raijmakers, R.; Heck, A. J. R.; van Breukelen, B. RockerBox: analysis and filtering of massive proteomics search results J. Proteome Res. 2010, 10 (3) 1420-1424
29. Deininger, S. O.; Cornett, D. S.; Paape, R.; Becker, M.; Pineau, C.; Rauser, S.; Walch, A.; Wolski, E. Normalization in MALDI-TOF imaging datasets of proteins: practical considerations Anal. Bioanal. Chem. 2011, 401, 167-181
30. Djidja, M.-C.; Claude, E.; Snel, M. F.; Scriven, P.; Francese, S.; Carolan, V.; Clench, M. R. MALDI-ion mobility separation-mass spectrometry imaging of glucose-regulated protein 78 kDa (Grp78) in human formalin-fixed, paraffin-embedded pancreatic adenocarcinoma tissue sections J. Proteome Res. 2009, 8 (10) 4876-84
31. Leader, M.; Collins, M.; Patel, J.; Henry, K. Vimentin: an evaluation of its role as a tumour marker Histopathology 1987, 11, 63-72
32. Stoeckli, M.; Staab, D.; Schweitzer, A. Compound and metabolite distribution measured by MALDI mass spectrometric imaging in whole-body tissue sections Int. J. Mass. Spectrom. 2007, 260, 195-202
33. Lahat, G.; Zhu, Q.-S.; Huang, K.-L.; Wang, S.; Bolshakov, S.; Liu, J.; Torres, K.; Langley, R. R.; Lazar, A. J.; Hung, M. C.; Lev, D. Vimentin is a novel anti-cancer therapeutic target; insights from in vitro and in vivo mice Xenograft studies PLoS ONE 2010, 5, e10105
34. Scholz, B.; Sköld, K.; Kultima, K.; Fernandez, C.; Waldemarson, S.; Savitski, M. M.; Söderquist, M.; Borén, M.; Stella, R.; Andrén, P.; Zubarev, R.; James, P. Impact of temperature dependent sampling procedures in proteomics and peptidomics-A characterization of the liver and pancreas post mortem degradome Mol. Cell. Proteomics 2011, 10, M900229-MCP200
35. Groseclose, M. R.; Massion, P. P.; Chaurand, P.; Caprioli, R. M. High-throughput proteomic analysis of formalin-fixed paraffin-embedded tissue microarrays using MALDI imaging mass spectrometry Proteomics 2008, 8 (18) 3715-3724
36. Deininger, S.-O.; Ebert, M. P.; Fütterer, A.; Gerhard, M.; Röcken, C. MALDI imaging combined with hierarchical clustering as a new tool for the interpretation of complex human cancers J. Proteome Res. 2008, 7 (12) 5230-5236
37. van de Plas, R.; Ojeda, F.; Dewil, M.; van Den Bosch, L.; De Moor, B.; Waelkens, E. In Prospective Exploration of Biochemical Tissue Composition via Imaging Mass Spectrometry Guided by Principal Component Analysis, Proceedings of the Pacific Symposium on Biocomputing 12 (PSB), Maui, Hawaii, 2007, 2007; Maui, Hawaii, 2007; pp 458-469.
38. Tyler, B. J.; Rayal, G.; Castner, D. G. Multivariate analysis strategies for processing ToF-SIMS images of biomaterials Biomaterials 2007, 28, 2412-2423
39. McCombie, G.; Staab, D.; Stoeckli, M.; Knochenmuss, R. Spatial and Spectral Correlations in MALDI Mass Spectrometry Images by Clustering and Multivariate analysis Anal. Chem. 2005, 77 (19) 6118-6124
40. Keenan, M. R.; Kotula, P. G. Accounting for Poisson noise in the multivariate analysis of ToF-SIMS spectrum images Surf. Interface Anal. 2004, 36, 203-212
41. Djidja, M.-C.; Claude, E.; Snel, M. F.; Francese, S.; Scriven, P.; Carolan, V.; Clench, M. R. Novel molecular tumour classification using MALDI-mass spectrometry imaging of tissue micro-array Anal. Bioanal. Chem. 2010, 397, 587-601
42. Clemis, E. J.; Smith, D. S.; Camenzind, A. G.; Danell, R. M.; Parker, C. E.; Borchers, C. H. Quantitation of spatially-localized proteins in tissue samples using MALDI-MRM imaging Anal. Chem. 2012, 84 (8) 3514-3522
43. Källback, P.; Shariatgorji, M.; Nilsson, A.; Andrén, P. E. Novel mass spectrometry imaging software assisting labeled normalization and quantitation of drugs and neuropeptides directly in tissue sections J. Proteomics 2012, 75, 4941-4951
44. Elsner, M.; Rauser, S.; Maier, S.; Schone, C.; Balluff, B.; Meding, S.; Jung, G.; Nipp, M.; Sarioglu, H.; Maccarrone, G.; Aichler, M.; Ruchtinger, A.; Langer, R.; Jutting, U.; Feith, M.; Kuster, B.; Ueffing, M.; Zitzelsberger, H.; Hofler, H.; Walch, A. MALDI imaging mass spectrometry reveals COX7A2, TAGLN2 and S100-A10 as novel prognostic markers in Barrett's adenocarcinoma J. Proteomics 2012, 75 (15) 4693-4704
45. Nipp, M.; Elsner, M.; Balluff, B.; Meding, S.; Sarioglu, H.; Ueffing, M.; Rauser, S.; Unger, K.; Hofler, H.; Walch, A.; Zitzelsberger, H. S100-A10, thioredoxin, and S100-A6 as biomarkers of papillary thyroid carcinoma with lymph node metastasis identified by MALDI Imaging J. Mol. Med. 2012, 90 (2) 163-174