Current frontiers in clinical research application of MALDI imaging mass spectrometry

References

• Castain R, Slodzian G. [Optique corpusculaire – premiers essais de microanalyse par emission ionique secondaire]. Comptes Rendus Hebdomadaires Des Seances De L Academie Des Sciences 255, 1893–1895 (1962).
   Google Scholar
• Galle P. Sur une nouvelle methode d’analyse cellulaire utilisant le phenomene d’emission ionique secondaire. Ann. Phys. Biol. Med. 42, 83–94 (1970).
   Google Scholar
• Morrison GH, Slodzian G. Ion microscopy. Anal. Chem. 47, 932–943 (1975).
   Web of Science ®Google Scholar
• Karas M, Bachmann D, Hillenkamp F. Influence of the wavelength in high-irradiance ultraviolet laser desorption mass spectrometry of organic molecules. Anal. Chem. 57, 2935–2939 (1985).
   Web of Science ®Google Scholar
• Caprioli RM, Farmer TB, Gile J. Molecular imaging of biological samples: localization of peptides and proteins using MALDI-TOF MS. Anal. Chem. 69(23), 4751–4760 (1997).
   PubMed Web of Science ®Google Scholar
• Takáts Z, Wiseman JM, Gologan B, Cooks RG. Mass spectrometry sampling under ambient conditions with desorption electrospray ionization. Science 306(5695), 471–473 (2004).
   PubMed Web of Science ®Google Scholar
• Eberlin LS, Norton I, Orringer D et al. Ambient mass spectrometry for the intraoperative molecular diagnosis of human brain tumors. Proc. Natl Acad. Sci. USA 110(5), 1611–1616 (2013).
   PubMed Web of Science ®Google Scholar
• Schober Y, Guenther S, Spengler B, Römpp A. Single cell matrix-assisted laser desorption/ionization mass spectrometry imaging. Anal. Chem. 84(15), 6293–6297 (2012).
   PubMed Web of Science ®Google Scholar
• Schober Y, Guenther S, Spengler B, Römpp A. High-resolution matrix-assisted laser desorption/ionization imaging of tryptic peptides from tissue. Rapid Commun. Mass Spectrom. 26(9), 1141–1146 (2012).
   Google Scholar
• Spraggins JM, Caprioli RM. High-speed MALDI-TOF imaging mass spectrometry: rapid ion image acquisition and considerations for next generation instrumentation. J. Am. Soc. Mass Spectrom. 22(6), 1022–1031 (2011).
   PubMed Web of Science ®Google Scholar
• Pól J, Strohalm M, Havlícek V, Volný M. Molecular mass spectrometry imaging in biomedical and life science research. Histochem. Cell Biol. 134(5), 423–443 (2010).
   Google Scholar
• Goodwin RJ. Sample preparation for mass spectrometry imaging: small mistakes can lead to big consequences. J. Proteomics 75(16), 4893–4911 (2012).
   PubMed Web of Science ®Google Scholar
• Jones EA, Deininger SO, Hogendoorn PC, Deelder AM, McDonnell LA. Imaging mass spectrometry statistical analysis. J. Proteomics 75(16), 4962–4989 (2012).
   PubMed Web of Science ®Google Scholar
• Deininger SO, Cornett DS, Paape R et al. Normalization in MALDI-TOF imaging datasets of proteins: practical considerations. Anal. Bioanal. Chem. 401(1), 167–181 (2011).
   PubMed Web of Science ®Google Scholar
• Murphy AJ, Axt JR, de Caestecker C et al. Molecular characterization of Wilms’ tumor from a resource-constrained region of sub-Saharan Africa. Int. J. Cancer 131(6), E983–E994 (2012).
   Google Scholar
• Schwamborn K. Imaging mass spectrometry in biomarker discovery and validation. J. Proteomics 75(16), 4990–4998 (2012).
   PubMed Web of Science ®Google Scholar
• Rauser S, Deininger SO, Suckau D, Höfler H, Walch A. Approaching MALDI molecular imaging for clinical proteomic research: current state and fields of application. Expert Rev. Proteomics 7(6), 927–941 (2010).
   PubMed Web of Science ®Google Scholar
• Jones EA, Deininger SO, Hogendoorn PC, Deelder AM, McDonnell LA. Imaging mass spectrometry statistical analysis. J. Proteomics 75(16), 4962–4989 (2012).
   PubMed Web of Science ®Google Scholar
• Baker SG, Kramer BS, Srivastava S. Markers for early detection of cancer: statistical guidelines for nested case-control studies. BMC Med. Res. Methodol. 2, 4 (2002).
   Google Scholar
• Seeley EH, Caprioli RM. MALDI imaging mass spectrometry of human tissue: method challenges and clinical perspectives. Trends Biotechnol. 29(3), 136–143 (2011).
   PubMed Web of Science ®Google Scholar
• Balluff B, Elsner M, Kowarsch A et al. Classification of HER2/neu status in gastric cancer using a breast-cancer derived proteome classifier. J. Proteome Res. 9(12), 6317–6322 (2010).
   PubMed Web of Science ®Google Scholar
• Djidja MC, Claude E, Snel MF et al. Novel molecular tumour classification using MALDI-mass spectrometry imaging of tissue micro-array. Anal. Bioanal. Chem. 397(2), 587–601 (2010).
   PubMed Web of Science ®Google Scholar
• Hardesty WM, Kelley MC, Mi D, Low RL, Caprioli RM. Protein signatures for survival and recurrence in metastatic melanoma. J. Proteomics 74(7), 1002–1014 (2011).
   PubMed Web of Science ®Google Scholar
• Hood BL, Conrads TP, Veenstra TD. Mass spectrometric analysis of formalin-fixed paraffin-embedded tissue: unlocking the proteome within. Proteomics 6(14), 4106–4114 (2006).
   PubMed Web of Science ®Google Scholar
• Schwartz SA, Reyzer ML, Caprioli RM. Direct tissue analysis using matrix-assisted laser desorption/ionization mass spectrometry: practical aspects of sample preparation. J. Mass Spectrom. 38(7), 699–708 (2003).
   PubMed Web of Science ®Google Scholar
• Strohalm M, Strohalm J, Kaftan F et al. Poly[N-(2-hydroxypropyl)methacrylamide]-based tissue-embedding medium compatible with MALDI mass spectrometry imaging experiments. Anal. Chem. 83(13), 5458–5462 (2011).
   Google Scholar
• Balluff B, Schöne C, Höfler H, Walch A. MALDI imaging mass spectrometry for direct tissue analysis: technological advancements and recent applications. Histochem. Cell Biol. 136(3), 227–244 (2011).
   PubMed Web of Science ®Google Scholar
• Walch A, Rauser S, Deininger SO, Höfler H. MALDI imaging mass spectrometry for direct tissue analysis: a new frontier for molecular histology. Histochem. Cell Biol. 130(3), 421–434 (2008).
   PubMed Web of Science ®Google Scholar
• McDonnell LA, Corthals GL, Willems SM, van Remoortere A, van Zeijl RJ, Deelder AM. Peptide and protein imaging mass spectrometry in cancer research. J. Proteomics 73(10), 1921–1944 (2010).
   PubMed Web of Science ®Google Scholar
• Chaurand P, Schwartz SA, Billheimer D, Xu BJ, Crecelius A, Caprioli RM. Integrating histology and imaging mass spectrometry. Anal. Chem. 76(4), 1145–1155 (2004).
   PubMed Web of Science ®Google Scholar
• Cornett DS, Mobley JA, Dias EC et al. A novel histology-directed strategy for MALDI-MS tissue profiling that improves throughput and cellular specificity in human breast cancer. Mol. Cell Proteomics 5(10), 1975–1983 (2006).
   PubMed Web of Science ®Google Scholar
• Seeley EH, Oppenheimer SR, Mi D, Chaurand P, Caprioli RM. Enhancement of protein sensitivity for MALDI imaging mass spectrometry after chemical treatment of tissue sections. J. Am. Soc. Mass Spectrom. 19(8), 1069–1077 (2008).
   PubMed Web of Science ®Google Scholar
• Thomas A, Patterson NH, Laveaux Charbonneau J, Chaurand P. Orthogonal organic and aqueous-based washes of tissue sections to enhance protein sensitivity by MALDI imaging mass spectrometry. J. Mass Spectrom. 48(1), 42–48 (2013).
   Google Scholar
• Mainini V, Angel PM, Magni F, Caprioli RM. Detergent enhancement of on-tissue protein analysis by matrix-assisted laser desorption/ionization imaging mass spectrometry. Rapid Commun. Mass Spectrom. 25(1), 199–204 (2011).
   PubMed Web of Science ®Google Scholar
• Shariatgorji M, Källback P, Gustavsson L et al. Controlled-pH tissue cleanup protocol for signal enhancement of small molecule drugs analyzed by MALDI-MS imaging. Anal. Chem. 84(10), 4603–4607 (2012).
   Google Scholar
• Meriaux C, Franck J, Wisztorski M, Salzet M, Fournier I. Liquid ionic matrixes for MALDI mass spectrometry imaging of lipids. J. Proteomics 73(6), 1204–1218 (2010).
   PubMed Web of Science ®Google Scholar
• Gross JH. Mass Spectrometry: A Textbook (2nd Edition). Gross JH (Ed.). Springer Verlag, Heidelberg, Germany (2011).
   Google Scholar
• Goodwin RJ. Sample preparation for mass spectrometry imaging: small mistakes can lead to big consequences. J. Proteomics 75(16), 4893–4911 (2012).
   PubMed Web of Science ®Google Scholar
• Shanta SR, Zhou LH, Park YS, Kim YH, Kim Y, Kim KP. Binary matrix for MALDI imaging mass spectrometry of phospholipids in both ion modes. Anal. Chem. 83(4), 1252–1259 (2011).
   Google Scholar
• García MC. The effect of the mobile phase additives on sensitivity in the analysis of peptides and proteins by high-performance liquid chromatography-electrospray mass spectrometry. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 825(2), 111–123 (2005).
   PubMed Web of Science ®Google Scholar
• Amstalden van Hove ER, Smith DF, Heeren RM. A concise review of mass spectrometry imaging. J. Chromatogr. A 1217(25), 3946–3954 (2010).
   PubMed Web of Science ®Google Scholar
• Hankin JA, Barkley RM, Murphy RC. Sublimation as a method of matrix application for mass spectrometric imaging. J. Am. Soc. Mass Spectrom. 18(9), 1646–1652 (2007).
   PubMed Web of Science ®Google Scholar
• Jaskolla TW, Karas M, Roth U, Steinert K, Menzel C, Reihs K. Comparison between vacuum sublimed matrices and conventional dried droplet preparation in MALDI-TOF mass spectrometry. J. Am. Soc. Mass Spectrom. 20(6), 1104–1114 (2009).
   PubMed Web of Science ®Google Scholar
• Thomas A, Charbonneau JL, Fournaise E, Chaurand P. 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(4), 2048–2054 (2012).
   PubMed Web of Science ®Google Scholar
• Goodwin RJ, Macintyre L, Watson DG, Scullion SP, Pitt AR. A solvent-free matrix application method for matrix-assisted laser desorption/ionization imaging of small molecules. Rapid Commun. Mass Spectrom. 24(11), 1682–1686 (2010).
   Google Scholar
• Goodwin RJ, Scullion P, Macintyre L, Watson DG, Pitt AR. Use of a solvent-free dry matrix coating for quantitative matrix-assisted laser desorption ionization imaging of 4-bromophenyl-1,4-diazabicyclo(3.2.2)nonane-4-carboxylate in rat brain and quantitative analysis of the drug from laser microdissected tissue regions. Anal. Chem. 82(9), 3868–3873 (2010).
   PubMed Web of Science ®Google Scholar
• Casadonte R, Caprioli RM. Proteomic analysis of formalin-fixed paraffin-embedded tissue by MALDI imaging mass spectrometry. Nat. Protoc. 6(11), 1695–1709 (2011).
   PubMed Web of Science ®Google Scholar
• McDonnell LA, van Remoortere A, de Velde N, van Zeijl RJ, Deelder AM. Imaging mass spectrometry data reduction: automated feature identification and extraction. J. Am. Soc. Mass Spectrom. 21(12), 1969–1978 (2010).
   Google Scholar
• Deininger SO, Becker M, Suckau D. Tutorial: multivariate statistical treatment of imaging data for clinical biomarker discovery. Methods Mol. Biol. 656, 385–403 (2010).
   Google Scholar
• Deininger SO, Ebert MP, 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. 7(12), 5230–5236 (2008).
   PubMed Web of Science ®Google Scholar
• Liu NQ, Braakman RB, Stingl C et al. Proteomics pipeline for biomarker discovery of laser capture microdissected breast cancer tissue. J. Mammary Gland Biol. Neoplasia 17(2), 155–164 (2012).
   PubMed Web of Science ®Google Scholar
• Umar A, Luider TM, Foekens JA, Pasa-Tolic L. NanoLC-FT-ICR MS improves proteome coverage attainable for approximately 3000 laser-microdissected breast carcinoma cells. Proteomics 7(2), 323–329 (2007).
   PubMed Web of Science ®Google Scholar
• Imanishi SY, Kouvonen P, Smått JH et al. Phosphopeptide enrichment with stable spatial coordination on a titanium dioxide coated glass slide. Rapid Commun. Mass Spectrom. 23(23), 3661–3667 (2009).
   Google Scholar
• Reyzer ML, Caldwell RL, Dugger TC et al. Early changes in protein expression detected by mass spectrometry predict tumor response to molecular therapeutics. Cancer Res. 64(24), 9093–9100 (2004).
   PubMed Web of Science ®Google Scholar
• Pierson J, Norris JL, Aerni HR, Svenningsson P, Caprioli RM, Andrén PE. Molecular profiling of experimental Parkinson’s disease: direct analysis of peptides and proteins on brain tissue sections by MALDI mass spectrometry. J. Proteome Res. 3(2), 289–295 (2004).
   PubMed Web of Science ®Google Scholar
• Reiber DC, Grover TA, Brown RS. Identifying proteins using matrix-assisted laser desorption/ionization in-source fragmentation data combined with database searching. Anal. Chem. 70(4), 673–683 (1998).
   PubMed Web of Science ®Google Scholar
• Suckau D, Resemann A. T3-sequencing: targeted characterization of the N- and C-termini of undigested proteins by mass spectrometry. Anal. Chem. 75(21), 5817–5824 (2003).
   PubMed Web of Science ®Google Scholar
• Suckau D, Resemann A. MALDI top-down sequencing: calling N- and C-terminal protein sequences with high confidence and speed. J. Biomol. Tech. 20(5), 258–262 (2009).
   Google Scholar
• Demeure K, Quinton L, Gabelica V, De Pauw E. Rational selection of the optimum MALDI matrix for top-down proteomics by in-source decay. Anal. Chem. 79(22), 8678–8685 (2007).
   PubMedGoogle Scholar
• Calligaris D, Longuespée R, Debois D et al. Selected protein monitoring in histological sections by targeted MALDI-FTICR in-source decay imaging. Anal. Chem. 85(4), 2117–2126 (2013).
   PubMed Web of Science ®Google Scholar
• Bonnel D, Longuespee R, Franck J et al. Multivariate analyses for biomarkers hunting and validation through on-tissue bottom-up or in-source decay in MALDI-MSI: application to prostate cancer. Anal. Bioanal. Chem. 401(1), 149–165 (2011).
   PubMed Web of Science ®Google Scholar
• Debois D, Bertrand V, Quinton L, De Pauw-Gillet MC, De Pauw E. MALDI-in source decay applied to mass spectrometry imaging: a new tool for protein identification. Anal. Chem. 82(10), 4036–4045 (2010).
   PubMed Web of Science ®Google Scholar
• Rauser S, Marquardt C, Balluff B et al. Classification of HER2 receptor status in breast cancer tissues by MALDI imaging mass spectrometry. J. Proteome Res. 9(4), 1854–1863 (2010).
   PubMed Web of Science ®Google Scholar
• Meding S, Martin K, Gustafsson OJ et al. Tryptic peptide reference data sets for MALDI imaging mass spectrometry on formalin-fixed ovarian cancer tissues. J. Proteome Res. 12(1), 308–315 (2013).
   Google Scholar
• Gustafsson JO, Eddes JS, Meding S et al. Internal calibrants allow high accuracy peptide matching between MALDI imaging MS and LC-MS/MS. J. Proteomics 75(16), 5093–5105 (2012).
   Google Scholar
• Djidja MC, Claude E, Snel MF et al. 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. 8(10), 4876–4884 (2009).
   PubMed Web of Science ®Google Scholar
• Groseclose MR, Massion PP, Chaurand P, Caprioli RM. High-throughput proteomic analysis of formalin-fixed paraffin-embedded tissue microarrays using MALDI imaging mass spectrometry. Proteomics 8(18), 3715–3724 (2008).
   PubMed Web of Science ®Google Scholar
• Djidja MC, Francese S, Loadman PM et al. Detergent addition to tryptic digests and ion mobility separation prior to MS/MS improves peptide yield and protein identification for in situ proteomic investigation of frozen and formalin-fixed paraffin-embedded adenocarcinoma tissue sections. Proteomics 9(10), 2750–2763 (2009).
   PubMed Web of Science ®Google Scholar
• Stauber J, MacAleese L, Franck J et al. On-tissue protein identification and imaging by MALDI-ion mobility mass spectrometry. J. Am. Soc. Mass Spectrom. 21(3), 338–347 (2010).
   PubMed Web of Science ®Google Scholar
• Grüner BM, Hahne H, Mazur PK et al. MALDI imaging mass spectrometry for in situ proteomic analysis of preneoplastic lesions in pancreatic cancer. PLoS ONE 7(6), e39424 (2012).
   PubMed Web of Science ®Google Scholar
• Quanico J, Franck J, Dauly C et al. Development of liquid microjunction extraction strategy for improving protein identification from tissue sections. J. Proteomics 79, 200–218 (2013).
   Google Scholar
• Hamm G, Bonnel D, Legouffe R et al. Quantitative mass spectrometry imaging of propranolol and olanzapine using tissue extinction calculation as normalization factor. J. Proteomics 75(16), 4952–4961 (2012).
   PubMed Web of Science ®Google Scholar
• Stoeckli M, Staab D, Schweitzer A, Gardiner J, Seebach D. Imaging of a beta-peptide distribution in whole-body mice sections by MALDI mass spectrometry. J. Am. Soc. Mass Spectrom. 18(11), 1921–1924 (2007).
   PubMed Web of Science ®Google Scholar
• Sugiura Y, Konishi Y, Zaima N et al. Visualization of the cell-selective distribution of PUFA-containing phosphatidylcholines in mouse brain by imaging mass spectrometry. J. Lipid Res. 50(9), 1776–1788 (2009).
   PubMed Web of Science ®Google Scholar
• Takai N, Tanaka Y, Inazawa K, Saji H. Quantitative analysis of pharmaceutical drug distribution in multiple organs by imaging mass spectrometry. Rapid Commun. Mass Spectrom. 26(13), 1549–1556 (2012).
   PubMed Web of Science ®Google Scholar
• Reich RF, Cudzilo K, Levisky JA, Yost RA. Quantitative MALDI-MS(n) analysis of cocaine in the autopsied brain of a human cocaine user employing a wide isolation window and internal standards. J. Am. Soc. Mass Spectrom. 21(4), 564–571 (2010).
   Google Scholar
• Castellino S. MALDI imaging MS analysis of drug distribution in tissue: the right time!(?). Bioanalysis 4(21), 2549–2551 (2012).
   PubMed Web of Science ®Google Scholar
• Trede D, Schiffler S, Becker M et al. Exploring three-dimensional matrix-assisted laser desorption/ionization imaging mass spectrometry data: three-dimensional spatial segmentation of mouse kidney. Anal. Chem. 84(14), 6079–6087 (2012).
   Google Scholar
• Sinha TK, Khatib-Shahidi S, Yankeelov TE et al. Integrating spatially resolved three-dimensional MALDI IMS with in vivo magnetic resonance imaging. Nat. Methods 5(1), 57–59 (2008).
   PubMed Web of Science ®Google Scholar
• Andersson M, Groseclose MR, Deutch AY, Caprioli RM. Imaging mass spectrometry of proteins and peptides: 3D volume reconstruction. Nat. Methods 5(1), 101–108 (2008).
   PubMed Web of Science ®Google Scholar
• Chughtai K, Jiang L, Greenwood TR et al. Fiducial markers for combined 3-dimensional mass spectrometric and optical tissue imaging. Anal. Chem. 84(4), 1817–1823 (2012).
   PubMed Web of Science ®Google Scholar
• Seeley EH, Caprioli RM. 3D imaging by mass spectrometry: a new frontier. Anal. Chem. 84(5), 2105–2110 (2012).
   PubMed Web of Science ®Google Scholar
• Crecelius AC, Cornett DS, Caprioli RM, Williams B, Dawant BM, Bodenheimer B. Three-dimensional visualization of protein expression in mouse brain structures using imaging mass spectrometry. J. Am. Soc. Mass Spectrom. 16(7), 1093–1099 (2005).
   PubMed Web of Science ®Google Scholar
• McKinley ET, Smith RA, Zhao P et al. 3′-deoxy-3′-18F-fluorothymidine PET predicts response to V600EBRAF-targeted therapy in preclinical models of colorectal cancer. J. Nucl. Med. 54(3), 424–430 (2013).
   Google Scholar
• Goodwin RJ, Mackay CL, Nilsson A et al. Qualitative and quantitative MALDI imaging of the positron emission tomography ligands raclopride (a D2 dopamine antagonist) and SCH 23390 (a D1 dopamine antagonist) in rat brain tissue sections using a solvent-free dry matrix application method. Anal. Chem. 83(24), 9694–9701 (2011).
   PubMed Web of Science ®Google Scholar
• Scheuer W, van Dam GM, Dobosz M, Schwaiger M, Ntziachristos V. Drug-based optical agents: infiltrating clinics at lower risk. Sci. Transl. Med. 4(134), 134ps11 (2012).
   Google Scholar
• Schwartz SA, Weil RJ, Thompson RC et al. Proteomic-based prognosis of brain tumor patients using direct-tissue matrix-assisted laser desorption ionization mass spectrometry. Cancer Res. 65(17), 7674–7681 (2005).
   PubMed Web of Science ®Google Scholar
• Schwartz SA, Weil RJ, Johnson MD, Toms SA, Caprioli RM. Protein profiling in brain tumors using mass spectrometry: feasibility of a new technique for the analysis of protein expression. Clin. Cancer Res. 10(3), 981–987 (2004).
   PubMed Web of Science ®Google Scholar
• Lemaire R, Menguellet SA, Stauber J et al. Specific MALDI imaging and profiling for biomarker hunting and validation: fragment of the 11S proteasome activator complex, Reg alpha fragment, is a new potential ovary cancer biomarker. J. Proteome Res. 6(11), 4127–4134 (2007).
   PubMed Web of Science ®Google Scholar
• Cazares LH, Troyer D, Mendrinos S et al. Imaging mass spectrometry of a specific fragment of mitogen-activated protein kinase/extracellular signal-regulated kinase kinase kinase 2 discriminates cancer from uninvolved prostate tissue. Clin. Cancer Res. 15(17), 5541–5551 (2009).
   PubMed Web of Science ®Google Scholar
• Chaurand P, DaGue BB, Pearsall RS, Threadgill DW, Caprioli RM. Profiling proteins from azoxymethane-induced colon tumors at the molecular level by matrix-assisted laser desorption/ionization mass spectrometry. Proteomics 1(10), 1320–1326 (2001).
   PubMed Web of Science ®Google Scholar
• Balluff B, Rauser S, Ebert MP, Siveke JT, Höfler H, Walch A. Direct molecular tissue analysis by MALDI imaging mass spectrometry in the field of gastrointestinal disease. Gastroenterology 143(3), 544–549.e1 (2012).
   Google Scholar
• Elsner M, Rauser S, Maier S et al. MALDI imaging mass spectrometry reveals COX7A2, TAGLN2 and S100-A10 as novel prognostic markers in Barrett’s adenocarcinoma. J. Proteomics 75(15), 4693–4704 (2012).
   PubMed Web of Science ®Google Scholar
• Balluff B, Rauser S, Meding S et al. MALDI imaging identifies prognostic seven-protein signature of novel tissue markers in intestinal-type gastric cancer. Am. J. Pathol. 179(6), 2720–2729 (2011).
   PubMed Web of Science ®Google Scholar
• Stoeckli M, Staab D, Staufenbiel M, Wiederhold KH, Signor L. Molecular imaging of amyloid beta peptides in mouse brain sections using mass spectrometry. Anal. Biochem. 311(1), 33–39 (2002).
   PubMed Web of Science ®Google Scholar
• Senyo SE, Steinhauser ML, Pizzimenti CL et al. Mammalian heart renewal by pre-existing cardiomyocytes. Nature 493(7432), 433–436 (2013).
   PubMed Web of Science ®Google Scholar
• Yanagisawa K, Shyr Y, Xu BJ et al. Proteomic patterns of tumour subsets in non-small-cell lung cancer. Lancet 362(9382), 433–439 (2003).
   PubMed Web of Science ®Google Scholar
• Nipp M, Elsner M, Balluff B et al. S100-A10, thioredoxin, and S100-A6 as biomarkers of papillary thyroid carcinoma with lymph node metastasis identified by MALDI imaging. J. Mol. Med. 90(2), 163–174 (2012).
   PubMed Web of Science ®Google Scholar
• Meding S, Balluff B, Elsner M et al. Tissue-based proteomics reveals FXYD3, S100A11 and GSTM3 as novel markers for regional lymph node metastasis in colon cancer. J. Pathol. 228(4), 459–470 (2012).
   PubMed Web of Science ®Google Scholar
• Bauer JA, Chakravarthy AB, Rosenbluth JM et al. Identification of markers of taxane sensitivity using proteomic and genomic analyses of breast tumors from patients receiving neoadjuvant paclitaxel and radiation. Clin. Cancer Res. 16(2), 681–690 (2010).
   PubMed Web of Science ®Google Scholar
• Cole LM, Djidja MC, Bluff J et al. Investigation of protein induction in tumour vascular targeted strategies by MALDI MSI. Methods 54(4), 442–453 (2011).
   Google Scholar
• Meding S, Nitsche U, Balluff B et al. Tumor classification of six common cancer types based on proteomic profiling by MALDI imaging. J. Proteome Res. 11(3), 1996–2003 (2012).
   PubMed Web of Science ®Google Scholar
• Kim HK, Reyzer ML, Choi IJ et al. Gastric cancer-specific protein profile identified using endoscopic biopsy samples via MALDI mass spectrometry. J. Proteome Res. 9(8), 4123–4130 (2010).
   PubMed Web of Science ®Google Scholar
• Oezdemir RF, Gaisa NT, Lindemann-Docter K et al. Proteomic tissue profiling for the improvement of grading of noninvasive papillary urothelial neoplasia. Clin. Biochem. 45(1–2), 7–11 (2012).
   PubMedGoogle Scholar
• Schwamborn K, Krieg RC, Jirak P et al. Application of MALDI imaging for the diagnosis of classical Hodgkin lymphoma. J. Cancer Res. Clin. Oncol. 136(11), 1651–1655 (2010).
   Google Scholar
• Morita Y, Ikegami K, Goto-Inoue N et al. Imaging mass spectrometry of gastric carcinoma in formalin-fixed paraffin-embedded tissue microarray. Cancer Sci. 101(1), 267–273 (2010).
   PubMed Web of Science ®Google Scholar
• Willems SM, van Remoortere A, van Zeijl R, Deelder AM, McDonnell LA, Hogendoorn PC. Imaging mass spectrometry of myxoid sarcomas identifies proteins and lipids specific to tumour type and grade, and reveals biochemical intratumour heterogeneity. J. Pathol. 222(4), 400–409 (2010).
   PubMed Web of Science ®Google Scholar
• Jones EA, van Remoortere A, van Zeijl RJ et al. Multiple statistical analysis techniques corroborate intratumor heterogeneity in imaging mass spectrometry datasets of myxofibrosarcoma. PLoS ONE 6(9), e24913 (2011).
   Google Scholar
• Gerlinger M, Rowan AJ, Horswell S et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N. Engl. J. Med. 366, 883–892 (2012).
   PubMed Web of Science ®Google Scholar
• Prideaux B, Stoeckli M. Mass spectrometry imaging for drug distribution studies. J. Proteomics 75(16), 4999–5013 (2012).
   PubMed Web of Science ®Google Scholar
• Castellino S, Groseclose MR, Wagner D. MALDI imaging mass spectrometry: bridging biology and chemistry in drug development. Bioanalysis 3(21), 2427–2441 (2011).
   PubMed Web of Science ®Google Scholar
• Ait-Belkacem R, Sellami L, Villard C, DePauw E, Calligaris D, Lafitte D. Mass spectrometry imaging is moving toward drug protein co-localization. Trends Biotechnol. 30(9), 466–474 (2012).
   PubMed Web of Science ®Google Scholar