MALDI Imaging of Formalin-Fixed Paraffin-Embedded Tissues: Application to Model Animals of Parkinson Disease for Biomarker Hunting

  • Isabelle Fournier
  • Julien Franck
  • Céline Meriaux
  • Michel Salzet
Part of the Advances in Neurobiology book series (NEUROBIOL, volume 2)


After 10 years of important technical developments, MALDI Imaging Mass Spectrometry appears to be a sufficiently mature technology to be introduced in laboratories as a practical approach to exploring tissue properties at the molecular level, particularly in the comparison of normal vs. pathological states to study neurological diseases such as Parkinson’s. In this report, we will present the technology and the development to enable the use of formalin fixed and paraffin embedded tissue (FFPE) tissue in order to examine banked hospital clinical samples.


MALDI imaging Pathologies Developments Proteomics 



Supported by grants from Centre National de la Recherche Scientifique (CNRS), Ministère de L’Education Nationale, de L’Enseignement Supérieur et de la Recherche, Agence Nationale de la Recherche (ANR to I.F.).


  1. Arafah, K., Wisztorski, M., Croix, D., Fournier, I., & Salzet, M. (2009). Dye-Assisted Laser Desorption Ionisation (DALDI): Introduction to a new field of investigation in lipid mass spectrometry imaging. Proceedings of the 18th International Mass Spectrometry Conference, Bremen, Germany.Google Scholar
  2. Barzilai, A., Zilkha-Falb, R., Daily, D., Stern, N., Offen, D., Ziv, I., et al. (2000). The molecular mechanism of dopamine-induced apoptosis: Identification and characterization of genes that mediate dopamine toxicity. Journal of Neural Transmission. Supplementum, 60, 59–76.PubMedGoogle Scholar
  3. Basso, M., Giraudo, S., Corpillo, D., Bergamasco, B., Lopiano, L., & Fasano, M. (2004). Proteome analysis of human substantia nigra in Parkinson’s disease. Proteomics, 4(12), 3943–3952.CrossRefPubMedGoogle Scholar
  4. Basso, M., Giraudo, S., Lopiano, L., Bergamasco, B., Bosticco, E., Cinquepalmi, A., et al. (2003). Proteome analysis of mesencephalic tissues: Evidence for Parkinson’s disease. Neurological Sciences, 24(3), 155–156.CrossRefPubMedGoogle Scholar
  5. Beal, M. F., & Hantraye, P. (2001). Novel therapies in the search for a cure for Huntington’s disease. Proceedings of the National Academy of Sciences of the United States of America, 98(1), 3–4.CrossRefPubMedGoogle Scholar
  6. Bonnel, D., Franck, J., Wisztorski, M., El ayed, M., Salzet, M., & Fournier, I. (2008). On tissue fractionation: Unmasking difficult proteins for MALDI profiling. 56th Annual Conference on Mass Spectrometry and Allied Topics, Denver, Colorado.Google Scholar
  7. Bretin, S., Reibel, S., Charrier, E., Maus-Moatti, M., Auvergnon, N., Thevenoux, A., et al. (2005). Differential expression of CRMP1, CRMP2A, CRMP2B, and CRMP5 in axons or dendrites of distinct neurons in the mouse brain. The Journal of Comparative Neurology, 486(1), 1–17.CrossRefPubMedGoogle Scholar
  8. Caprioli, R. M., Farmer, T. B., & Gile, J. (1997). Molecular imaging of biological samples: Localization of peptides and proteins using MALDI-TOF MS. Analytical Chemistry, 69(23), 4751–4760.CrossRefPubMedGoogle Scholar
  9. Charrier, E., Reibel, S., Rogemond, V., Aguera, M., Thomasset, N., & Honnorat, J. (2003). Collapsin response mediator proteins (CRMPs): Involvement in nervous system development and adult neurodegenerative disorders. Molecular Neurobiology, 28(1), 51–64.CrossRefPubMedGoogle Scholar
  10. Chaurand, P., Schwartz, S. A., Billheimer, D., Xu, B. J., Crecelius, A., & Caprioli, R. M. (2004). Integrating histology and imaging mass spectrometry. Analytical Chemistry, 76(4), 1145–1155.CrossRefPubMedGoogle Scholar
  11. Chaurand, P., Stoeckli, M., & Caprioli, R. M. (1999). Direct profiling of proteins in biological tissue sections by MALDI mass spectrometry. Analytical Chemistry, 71(23), 5263–5270.CrossRefPubMedGoogle Scholar
  12. Dani, F. R., Francese, S., Mastrobuoni, G., Felicioli, A., Caputo, B., Simard, F., et al. (2008). Exploring proteins in Anopheles gambiae male and female antennae through MALDI mass spectrometry profiling. PLoS ONE, 3(7), 2822.CrossRefGoogle Scholar
  13. Daniel, R., He, Z., Carmichael, K. P., Halper, J., & Bateman, A. (2000). Cellular localization of gene expression for progranulin. The Journal of Histochemistry and Cytochemistry, 48(7), 999–1009.CrossRefPubMedGoogle Scholar
  14. De Iuliis, A., Grigoletto, J., Recchia, A., Giusti, P., & Arslan, P. (2005). A proteomic approach in the study of an animal model of Parkinson’s disease. Clinica Chimica Acta, 357(2), 202–209.CrossRefGoogle Scholar
  15. DeKeyser, S. S., Kutz-Naber, K. K., Schmidt, J. J., Barrett-Wilt, G. A., & Li, L. (2007). Imaging mass spectrometry of neuropeptides in decapod crustacean neuronal tissues. Journal of Proteome Research, 6(5), 1782–1791.CrossRefPubMedGoogle Scholar
  16. Djidja, M. C., Claude, E., Snel, M., Scriven, P., Francese, S., Carolan, V. A., et al. (2009). MALDI-ion mobility separation-mass spectrometry imaging of glucose-regulated protein 78 kDa (Grp78) in human formalin fixed paraffin embedded pancreatic adenocarcinoma tissue sections. Journal of Proteome Research, 8, 4876–4884.CrossRefPubMedGoogle Scholar
  17. Djidja, M. C., Francese, S., Loadman, P. M., Sutton, C. W., Scriven, P., Claude, E., et al. (2009). 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.CrossRefPubMedGoogle Scholar
  18. Dreisewerd, K., Kingston, R., Geraerts, W. P., & Li, K. W. (1997). Direct mass spectrometric peptide profiling and sequencing of nervous tissues to identify peptides involved in male copulatory behavior in Lymnaea stagnalis. International Journal of Mass Spectrometry, 169, 291–299.CrossRefGoogle Scholar
  19. Fournier, I., Day, R., & Salzet, M. (2003). Direct analysis of neuropeptides by in situ MALDI-TOF mass spectrometry in the rat brain. Neuro Endocrinology Letters, 24(1–2), 9–14.PubMedGoogle Scholar
  20. Fournier, I., Wisztorski, M., & Salzet, M. (2008). Tissue imaging using MALDI-MS: A new frontier of histopathology proteomics. Expert Review of Proteomics, 5(3), 413–424.CrossRefPubMedGoogle Scholar
  21. Franck, J., Arafah, K., Barnes, A., Wisztorski, M., Salzet, M., & Fournier, I. (2009). Improving tissue preparation for matrix-assisted laser desorption ionization mass spectrometry imaging. Part 1: Using microspotting. Analytical Chemistry, 81(19), 8193–8202.CrossRefPubMedGoogle Scholar
  22. Franck, J., El Ayed, M., Wisztorski, M., Salzet, M., & Fournier, I. (2009). On-tissue N-terminal peptide derivatizations for enhancing protein identification in MALDI mass spectrometric imaging strategies. Analytical Chemistry, 81(20), 8305–8317.CrossRefPubMedGoogle Scholar
  23. Franck, J., Longuespée, R., Wisztorski, M., van Remoortere, A., van Zeijl, R., Deelder, A., et al. (2010). MALDI mass spectrometry imaging of proteins exceeding 30,000 daltons. Medical Science Monitor, 16(9), BR293–BR299.Google Scholar
  24. Furukawa, Y., Nakamaru, K., Wakayama, H., Fujisawa, Y., Minakata, H., Ohta, S., et al. (2001). The enterins: A novel family of neuropeptides isolated from the enteric nervous system and CNS of Aplysia. The Journal of Neuroscience, 21(20), 8247–8261.PubMedGoogle Scholar
  25. Garden, R. W., Shippy, S. A., Li, L., Moroz, T. P., & Sweedler, J. V. (1998). Proteolytic processing of the Aplysia egg-laying hormone prohormone. Proceedings of the National Academy of Sciences of the United States of America, 95(7), 3972–3977.CrossRefPubMedGoogle Scholar
  26. Giasson, B. I., & Lee, V. M. (2003). Are ubiquitination pathways central to Parkinson’s disease? Cell, 114(1), 1–8.CrossRefPubMedGoogle Scholar
  27. Good, P. F., Alapat, D., Hsu, A., Chu, C., Perl, D., Wen, X., et al. (2004). A role for semaphorin 3A signaling in the degeneration of hippocampal neurons during Alzheimer’s disease. Journal of Neurochemistry, 91(3), 716–736.CrossRefPubMedGoogle Scholar
  28. Groseclose, M. R., Massion, P. P., Chaurand, P., & Caprioli, R. M. (2008). High-throughput proteomic analysis of formalin-fixed paraffin-embedded tissue microarrays using MALDI imaging mass spectrometry. Proteomics, 8(18), 3715–3724.CrossRefPubMedGoogle Scholar
  29. Grunblatt, E., Mandel, S., & Youdim, M. B. (2000). MPTP and 6-hydroxydopamine-induced neurodegeneration as models for Parkinson’s disease: Neuroprotective strategies. Journal of Neurology, 247(suppl 2), II95–II102.PubMedGoogle Scholar
  30. Gu, Y., Hamajima, N., & Ihara, Y. (2000). Neurofibrillary tangle-associated collapsin response mediator protein-2 (CRMP-2) is highly phosphorylated on Thr-509, Ser-518, and Ser-522. Biochemistry, 39(15), 4267–4275.CrossRefPubMedGoogle Scholar
  31. Herceg, Z., & Wang, Z. Q. (2001). Functions of poly(ADP-ribose) polymerase (PARP) in DNA repair, genomic integrity and cell death. Mutation Research, 477(1–2), 97–110.CrossRefPubMedGoogle Scholar
  32. Hofer, S., Dircksen, H., Tollback, P., & Homberg, U. (2005). Novel insect orcokinins: Characterization and neuronal distribution in the brains of selected dicondylian insects. The Journal of Comparative Neurology, 490(1), 57–71.CrossRefPubMedGoogle Scholar
  33. Hummon, A. B., Amare, A., & Sweedler, J. V. (2006). Discovering new invertebrate neuropeptides using mass spectrometry. Mass Spectrometry Reviews, 25(1), 77–98.CrossRefPubMedGoogle Scholar
  34. Jardin-Mathe, O., Bonnel, D., Franck, J., Wisztorski, M., Macagno, E., Fournier, I., et al. (2008).MITICS (MALDI Imaging Team Imaging Computing System): A new open source mass spectrometry imaging software. Journal of Proteomics, 71(3), 332–345.CrossRefPubMedGoogle Scholar
  35. Jespersen, S., Chaurand, P., van Strien, F. J., Spengler, B., & van der Greef, J. (1999). Direct sequencing of neuropeptides in biological tissue by MALDI-PSD mass spectrometry. Analytical Chemistry, 71(3), 660–666.CrossRefPubMedGoogle Scholar
  36. Jimenez, C. R., Li, K. W., Dreisewerd, K., Spijker, S., Kingston, R., Bateman, R. H., et al. (1998). Direct mass spectrometric peptide profiling and sequencing of single neurons reveals differential peptide patterns in a small neuronal network. Biochemistry, 37(7), 2070–2076.CrossRefPubMedGoogle Scholar
  37. Kruse, R. A., Rubakhin, S. S., Romanova, E. V., Bohn, P. W., & Sweedler, J. V. (2001). Direct assay of Aplysia tissues and cells with laser desorption/ionization mass spectrometry on porous silicon. Journal of Mass Spectrometry, 36(12), 1317–1322.CrossRefPubMedGoogle Scholar
  38. Kruse, R., & Sweedler, J. V. (2003). Spatial profiling invertebrate ganglia using MALDI MS. Journal of the American Society for Mass Spectrometry, 14(7), 752–759.CrossRefPubMedGoogle Scholar
  39. Langstrom, B., Andren, P. E., Lindhe, O., Svedberg, M., & Hall, H. (2007). In vitro imaging techniques in neurodegenerative diseases. Molecular Imaging and Biology, 9(4), 161–175.CrossRefPubMedGoogle Scholar
  40. Lemaire, R., Desmons, A., Ducoroy, P., Tabet, J. C., Salzet, M., & Fournier, I. (2006) Direct analysis and MALDI imaging on formalin fixed paraffin embedded tissue (FFPE): Application to Parkinson disease. Proceedings of the 54th American Society for Mass Spectrometry Conference, Seattle, Washington.Google Scholar
  41. Lemaire, R., Desmons, A., Tabet, J. C., Day, R., Salzet, M., & Fournier, I. (2007). Direct analysis and MALDI imaging of formalin-fixed, paraffin-embedded tissue sections. Journal of Proteome Research, 6(4), 1295–1305.CrossRefPubMedGoogle Scholar
  42. Lemaire, R., Stauber, J., Wisztorski, M., Van Camp, C., Desmons, A., Deschamps, M., et al. (2007). Tag-mass: Specific molecular imaging of transcriptome and proteome by mass spectrometry based on photocleavable tag. Journal of Proteome Research, 6(6), 2057–2067.CrossRefPubMedGoogle Scholar
  43. Lemaire, R., Tabet, J. C., Ducoroy, P., Hendra, J. B., Salzet, M., & Fournier, I. (2006). Solid ionic matrixes for direct tissue analysis and MALDI imaging. Analytical Chemistry, 78(3), 809–819.CrossRefPubMedGoogle Scholar
  44. Lemaire, R., Wisztorski, M., Desmons, A., Tabet, J. C., Day, R., Salzet, M., et al. (2006). MALDI-MS direct tissue analysis of proteins: Improving signal sensitivity using organic treatments. Analytical Chemistry, 78(20), 7145–7153.CrossRefPubMedGoogle Scholar
  45. Leroy, E., Boyer, R., Auburger, G., Leube, B., Ulm, G., Mezey, E., et al. (1998). The ubiquitin pathway in Parkinson’s disease. Nature, 395(6701), 451–452.CrossRefPubMedGoogle Scholar
  46. Li, L., Garden, R. W., Romanova, E. V., & Sweedler, J. V. (1999). In situ sequencing of peptides from biological tissues and single cells using MALDI-PSD/CID analysis. Analytical Chemistry, 71(24), 5451–5458.CrossRefPubMedGoogle Scholar
  47. Li, K. W., Hoek, R. M., Smith, F., Jimenez, C. R., van der Schors, R. C., van Veelen, P. A., et al. (1994). Direct peptide profiling by mass spectrometry of single identified neurons reveals complex neuropeptide-processing pattern. The Journal of Biological Chemistry, 269(48), 30288–30292.PubMedGoogle Scholar
  48. Li, L., Moroz, T. P., Garden, R. W., Floyd, P. D., Weiss, K. R., & Sweedler, J. V. (1998). Mass spectrometric survey of interganglionically transported peptides in Aplysia. Peptides, 19(8), 1425–1433.CrossRefPubMedGoogle Scholar
  49. Li, L., Romanova, E. V., Rubakhin, S. S., Alexeeva, V., Weiss, K. R., Vilim, F. S., et al. (2000). Peptide profiling of cells with multiple gene products: Combining immunochemistry and MALDI mass spectrometry with on-plate microextraction. Analytical Chemistry, 72(16), 3867–3874.CrossRefPubMedGoogle Scholar
  50. Liu, Q., Xie, F., Siedlak, S. L., Nunomura, A., Honda, K., Moreira, P. I., et al. (2004). Neurofilament proteins in neurodegenerative diseases. Cellular and Molecular Life Sciences, 61(24), 3057–3075.CrossRefPubMedGoogle Scholar
  51. McDonnell, L. A., & Heeren, R. M. (2007). Imaging mass spectrometry. Mass Spectrometry Reviews, 26(4), 606–643.CrossRefPubMedGoogle Scholar
  52. Murphy, R. C., Hankin, J. A., & Barkley, R. M. (2009). Imaging of lipid species by MALDI mass spectrometry. Journal of Lipid Research, 50(suppl), S317–S322.CrossRefPubMedGoogle Scholar
  53. Painter, S. D., Clough, B., Garden, R. W., Sweedler, J. V., & Nagle, G. T. (1998). Characterization of Aplysia attractin, the first water-borne peptide pheromone in invertebrates. The Biological Bulletin, 194(2), 120–131.CrossRefPubMedGoogle Scholar
  54. Palacino, J. J., Sagi, D., Goldberg, M. S., Krauss, S., Motz, C., Wacker, M., et al. (2004). Mitochondrial dysfunction and oxidative damage in parkin-deficient mice. The Journal of Biological Chemistry, 279(18), 18614–18622.CrossRefPubMedGoogle Scholar
  55. Pierson, J., Norris, J. L., Aerni, H. R., Svenningsson, P., Caprioli, R. M., & Andren, P. E. (2004). Molecular profiling of experimental Parkinson’s disease: Direct analysis of peptides and proteins on brain tissue sections by MALDI mass spectrometry. Journal of Proteome Research, 3(2), 289–295.CrossRefPubMedGoogle Scholar
  56. Pierson, J., Svenningsson, P., Caprioli, R. M., & Andren, P. E. (2005). Increased levels of ubiquitin in the 6-OHDA-lesioned striatum of rats. Journal of Proteome Research, 4(2), 223–226.CrossRefPubMedGoogle Scholar
  57. Reyzer, M. L., & Caprioli, R. M. (2007). MALDI-MS-based imaging of small molecules and proteins in tissues. Current Opinion in Chemical Biology, 11(1), 29–35.CrossRefPubMedGoogle Scholar
  58. Ricard, D., Stankoff, B., Bagnard, D., Aguera, M., Rogemond, V., Antoine, J. C., et al. (2000). Differential expression of collapsin response mediator proteins (CRMP/ULIP) in subsets of oligodendrocytes in the postnatal rodent brain. Molecular and Cellular Neurosciences, 16(4), 324–337.CrossRefPubMedGoogle Scholar
  59. Ronci, M., Bonanno, E., Colantoni, A., Pieroni, L., Di Ilio, C., Spagnoli, L. G., et al. (2008). Protein unlocking procedures of formalin-fixed paraffin-embedded tissues: Application to MALDI-TOF imaging MS investigations. Proteomics, 8(18), 3702–3714.CrossRefPubMedGoogle Scholar
  60. Rubakhin, S. S., Garden, R. W., Fuller, R. R., & Sweedler, J. V. (2000). Measuring the peptides in individual organelles with mass spectrometry. Nature Biotechnology, 18(2), 172–175.CrossRefPubMedGoogle Scholar
  61. Rubakhin, S. S., Greenough, W. T., & Sweedler, J. V. (2003). Spatial profiling with MALDI MS: Distribution of neuropeptides within single neurons. Analytical Chemistry, 75(20), 5374–5380.CrossRefPubMedGoogle Scholar
  62. Rubakhin, S. S., Jurchen, J. C., Monroe, E. B., & Sweedler, J. V. (2005). Imaging mass spectrometry: Fundamentals and applications to drug discovery. Drug Discovery Today, 10(12), 823–837.CrossRefPubMedGoogle Scholar
  63. Rubakhin, S. S., Li, L., Moroz, T. P., & Sweedler, J. V. (1999). Characterization of the Aplysia californica cerebral ganglion F cluster. Journal of Neurophysiology, 81(3), 1251–1260.PubMedGoogle Scholar
  64. Schein, C. H., Nagle, G. T., Page, J. S., Sweedler, J. V., Xu, Y., Painter, S. D., et al. (2001). Aplysia attractin: Biophysical characterization and modeling of a water-borne pheromone. Biophysical Journal, 81(1), 463–472.CrossRefPubMedGoogle Scholar
  65. Seo, B. B., Nakamaru-Ogiso, E., Cruz, P., Flotte, T. R., Yagi, T., & Matsuno-Yagi, A. (2004). Functional expression of the single subunit NADH dehydrogenase in mitochondria in vivo:A potential therapy for complex I deficiencies. Human Gene Therapy, 15(9), 887–895.CrossRefPubMedGoogle Scholar
  66. Shi, S. R., Imam, S. A., Young, L., Cote, R. J., & Taylor, C. R. (1995). Antigen retrieval immunohistochemistry under the influence of pH using monoclonal antibodies. The Journal of Histochemistry and Cytochemistry, 43(2), 193–201.CrossRefPubMedGoogle Scholar
  67. Spengler, B. (1994). Ion imaging and confocal microscopy with a new scanning UV-laser microprobe. In 42nd Annual Conference on Mass Spectrometry and Allied Topics, Chicago, IL.Google Scholar
  68. Stauber, J., Lemaire, R., Franck, J., Bonnel, D., Croix, D., Day, R., et al. (2008). MALDI imaging of formalin-fixed paraffin-embedded tissues: Application to model animals of Parkinson disease for biomarker hunting. Journal of Proteome Research, 7(3), 969–978.CrossRefPubMedGoogle Scholar
  69. Stoeckli, M., Chaurand, P., Hallahan, D. E., & Caprioli, R. M. (2001). Imaging mass spectrometry: A new technology for the analysis of protein expression in mammalian tissues. Natural Medicines, 7(4), 493–496.CrossRefGoogle Scholar
  70. Stoeckli, M., Farmer, T. B., & Caprioli, R. M. (1999). Automated mass spectrometry imaging with a matrix-assisted laser desorption ionization time-of-flight instrument. Journal of the American Society for Mass Spectrometry, 10(1), 67–71.CrossRefPubMedGoogle Scholar
  71. Strey, C. W., Spellman, D., Stieber, A., Gonatas, J. O., Wang, X., Lambris, J. D., et al. (2004). Dysregulation of stathmin, a microtubule-destabilizing protein, and up-regulation of Hsp25, Hsp27, and the antioxidant peroxiredoxin 6 in a mouse model of familial amyotrophic lateral sclerosis. The American Journal of Pathology, 165(5), 1701–1718.CrossRefPubMedGoogle Scholar
  72. Sweedler, J. V., Li, L., Floyd, P., & Gilly, W. (2000). Mass spectrometric survey of peptides in cephalopods with an emphasis on the FMRFamide-related peptides. The Journal of Experimental Biology, 203(Pt 23), 3565–3573.PubMedGoogle Scholar
  73. Sweedler, J. V., Li, L., Rubakhin, S. S., Alexeeva, V., Dembrow, N. C., Dowling, O., et al. (2002). Identification and characterization of the feeding circuit-activating peptides, a novel neuropeptide family of aplysia. The Journal of Neuroscience, 22(17), 7797–7808.PubMedGoogle Scholar
  74. Ungerstedt, U., Ljungberg, T., & Steg, G. (1974). Behavioral, physiological, and neurochemical changes after 6-hydroxydopamine-induced degeneration of the nigro-striatal dopamine neurons. Advances in Neurology, 5, 421–426.PubMedGoogle Scholar
  75. van Remoortere, A., van Zeijl, R. J., van den Oever, N., Franck, J., Longuespee, R., Wisztorski, M., et al. (2010). MALDI imaging and profiling MS of higher mass proteins from tissue. Journal of American Society for Mass Spectrometry.Google Scholar
  76. Wisztorski, M., Brunet, L., Dreisewerd, K., Hillenkamp, F., Berkenkamp, S., Salzet, M., et al. (2006). Effect of metals coating for UV MALDI-a-TOF mass spectrometry imaging (MALDI MSI) and direct tissue analysis in UV/IR MALDI-o-TOF mass spectrometry. Proceedings of the 54th American Society for Mass Spectrometry Conference, Seattle, Washington.Google Scholar
  77. Wisztorski, M., Croix, D., Macagno, E., Fournier, I., & Salzet, M. (2008). Molecular MALDI imaging: An emerging technology for neuroscience studies. Developmental Neurobiology, 68(6), 845–858.CrossRefPubMedGoogle Scholar
  78. Wisztorski, M., Lemaire, R., Stauber, J., Ait Menguellet, S., Jardin-Mathe, O., Day, R., et al. (2007). MALDI imaging: A new technology to discover and validate new biomarkers. Medical Science (Paris), 23(Spec no. 1), 31–36.CrossRefGoogle Scholar
  79. Wisztorski, M., Lemaire, R., Stauber, J., Menguelet, S. A., Croix, D., Mathe, O. J., et al. (2007). New developments in MALDI imaging for pathology proteomic studies. Current Pharmaceutical Design, 13(32), 3317–3324.CrossRefPubMedGoogle Scholar
  80. Woods, A. S., & Jackson, S. N. (2006). Brain tissue lipidomics: Direct probing using matrix-assisted laser desorption/ionization mass spectrometry. The AAPS Journal, 8(2), E391–E395.PubMedGoogle Scholar
  81. Yuasa-Kawada, J., Suzuki, R., Kano, F., Ohkawara, T., Murata, M., & Noda, M. (2003). Axonal morphogenesis controlled by antagonistic roles of two CRMP subtypes in microtubule organization. The European Journal of Neuroscience, 17(11), 2329–2343.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Isabelle Fournier
  • Julien Franck
  • Céline Meriaux
  • Michel Salzet
    • 1
  1. 1.Laboratoire de Neuroimmunologie et Neurochimie Evolutives, FRE CNRS 3249, MALDI Imaging TeamUniversité Lille Nord de FranceVilleneuve d’Ascq CedexFrance

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