New analysis workflow for MALDI imaging mass spectrometry: Application to the discovery and identification of potential markers of childhood absence epilepsy

Journal of Proteome Research

Volumn 11, Issue 11, 2012, Pages 5453-5463

  Lagarrigue, Mélanie ^a   Alexandrov, Theodore ^b,e   Dieuset, Gabriel ^c   Perrin, Aline ^d   Lavigne, Régis ^a   Baulac, Stéphanie ^d   Thiele, Herbert ^e   Martin, Benoit ^c   Pineau, Charles ^a,b  

^a UNIVERSITY OF BREMEN   (Germany)

^b UNIVERSITÉ DE RENNES 1   (France)

^c UNIVERSITÉ DE RENNES 1   (France)

^d PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^e Steinbeis Innovation Center SCiLS   (Germany)

Author keywords

absence epilepsy; classification method; imaging mass spectrometry; MALDI time of flight mass spectrometry; protein markers

Indexed keywords

SYNAPSIN I;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHILDHOOD ABSENCE EPILEPSY; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SUPPORT VECTOR MACHINE; WAVELET ANALYSIS; WESTERN BLOTTING;

ANIMALS; BIOLOGICAL MARKERS; BLOTTING, WESTERN; CHILD; EPILEPSY, ABSENCE; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

MUS;

EID: 84868316135     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr3006974     Document Type: Article

References (58)

1. Panayiotopoulos, C. P.; Koutroumanidis, M.; Giannakodimos, S.; Agathonikou, A. Idiopathic generalised epilepsy in adults manifested by phantom absences, generalised tonic-clonic seizures, and frequent absence status J. Neurol. Neurosurg. Psychiatry 1997, 63 (5) 622-7
2. Vega, C.; Guo, J.; Killory, B.; Danielson, N.; Vestal, M.; Berman, R.; Martin, L.; Gonzalez, J. L.; Blumenfeld, H.; Spann, M. N. Symptoms of anxiety and depression in childhood absence epilepsy Epilepsia 2011, 52 (8) E70-4
3. Yalcin, O. Genes and molecular mechanisms involved in the epileptogenesis of idiopathic absence epilepsies Seizure 2012, 21 (2) 79-86
4. Chapouthier, G.; Launay, J.-M.; Venault, P.; Breton, C.; Roubertoux, P. L.; Crusio, W. E. Genetic selection of mouse lines differing in sensitivity to a benzodiazepine receptor inverse agonist Brain Res. 1998, 787, 85-90
5. Balluff, B.; Elsner, M.; Kowarsch, A.; Rauser, S.; Meding, S.; Schuhmacher, C.; Feith, M.; Herrmann, K.; Rocken, C.; Schmid, R. M.; Hofler, H.; Walch, A.; Ebert, M. P. Classification of HER2/neu Status in Gastric Cancer Using a Breast-Cancer Derived Proteome Classifier J. Proteome Res. 2010, 9 (12) 6317-22
6. Balluff, B.; Rauser, S.; Meding, S.; Elsner, M.; Schone, C.; Feuchtinger, A.; Schuhmacher, C.; Novotny, A.; Juttingaaaa, U.; Maccarrone, G.; Sarioglu, H.; Ueffing, M.; Braselmann, H.; Zitzelsberger, H.; Schmid, R. M.; Hofler, 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 (6) 2720-29
7. 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 (2) 587-601
8. Seeley, E. H.; Caprioli, R. M. MALDI imaging mass spectrometry of human tissue: method challenges and clinical perspectives Trends Biotechnol. 2011, 29 (3) 136-43
9. MacAleese, L.; Stauber, J.; Heeren, R. M. Perspectives for imaging mass spectrometry in the proteomics landscape Proteomics 2009, 9 (4) 819-34
10. Chaurand, P. Imaging mass spectrometry of thin tissue sections: A decade of collective efforts J. Proteomics 2012, 75 (16) 4883-92
11. Lagarrigue, M.; Becker, M.; Lavigne, R.; Deininger, S. O.; Walch, A.; Aubry, F.; Suckau, D.; Pineau, C. Revisiting rat spermatogenesis with MALDI imaging at 20 μm resolution Mol. Cell. Proteomics 2011, 10 (3) M110.005991
12. Watrous, J. D.; Alexandrov, T.; Dorrestein, P. C. The evolving field of imaging mass spectrometry and its impact on future biological research J. Mass Spectrom. 2011, 46 (2) 209-22
13. Meeren, H.; van Luijtelaar, G.; Lopes da Silva, F.; Coenen, A. Evolving concepts on the pathophysiology of absence seizures: the cortical focus theory Arch. Neurol. 2005, 62 (3) 371-6
14. Zamdborg, L.; LeDuc, R. D.; Glowacz, K. J.; Kim, Y. B.; Viswanathan, V.; Spaulding, I. T.; Early, B. P.; Bluhm, E. J.; Babai, S.; Kelleher, N. L. ProSight PTM 2.0: improved protein identification and characterization for top down mass spectrometry Nucleic Acids Res. 2007, 35 (Web Server issue) W701-6
15. Alexandrov, T.; Decker, J.; Mertens, B.; Deelder, A. M.; Tollenaar, R. A.; Maass, P.; Thiele, H. Biomarker discovery in MALDI-TOF serum protein profiles using discrete wavelet transformation Bioinformatics 2009, 25 (5) 643-9
16. Groseclose, M. R.; Andersson, M.; Hardesty, W. M.; Caprioli, R. M. Identification of proteins directly from tissue: in situ tryptic digestions coupled with imaging mass spectrometry J Mass Spectrom 2007, 42 (2) 254-62
17. Andersson, M.; Andren, P.; Caprioli, R. M. MALDI Imaging and Profiling Mass Spectrometry. In Neuroproteomics; Alzate, O., Ed.; CRC Press: Boca Raton, USA, 2010; Chapter 7.
18. Chin, L. S.; Li, L.; Ferreira, A.; Kosik, K. S.; Greengard, P. Impairment of axonal development and of synaptogenesis in hippocampal neurons of synapsin I-deficient mice Proc. Natl. Acad. Sci. U.S.A. 1995, 92 (20) 9230-4
19. Farisello, P.; Boido, D.; Nieus, T.; Medrihan, L.; Cesca, F.; Valtorta, F.; Baldelli, P.; Benfenati, F. Synaptic and extrasynaptic origin of the excitation/inhibition imbalance in the hippocampus of synapsin I/II/III knockout mice. Cereb. Cortex [Online early access]. DOI:10.1093/cercor/bhs041. Published Online: Apr 24, 2012.
20. Murrey, H. E.; Gama, C. I.; Kalovidouris, S. A.; Luo, W. I.; Driggers, E. M.; Porton, B.; Hsieh-Wilson, L. C. Protein fucosylation regulates synapsin Ia/Ib expression and neuronal morphology in primary hippocampal neurons Proc. Natl. Acad. Sci. U.S.A. 2006, 103 (1) 21-6
21. Paulussen, M.; Landuyt, B.; Schoofs, L.; Luyten, W.; Arckens, L. Thymosin beta 4 mRNA and peptide expression in phagocytic cells of different mouse tissues Peptides 2009, 30 (10) 1822-32
22. Ryu, M.-J.; Kim, D.; Kang, U.-B.; Kim, J.; Shin, H.-S.; Lee, C.; Yu, M.-H. Proteomic analysis of gamma-butyrolactone-treated mouse thalamus reveals dysregulated proteins upon absence seizure J. Neurochem. 2007, 102 (3) 646-56
23. Ryu, M.-J.; Lee, C.; Kim, J.; Shin, H.-S.; Yu, M.-H. Proteomic analysis of stargazer mutant mouse neuronal proteins involved in absence seizure J. Neurochem. 2008, 104 (5) 1260-70
24. Danis, O.; Demir, S.; Gunel, A.; Aker, R. G.; Gulcebi, M.; Onat, F.; Ogan, A. Changes in intracellular protein expression in cortex., thalamus and hippocampus in a genetic rat model of absence epilepsy Brain Res. Bull. 2011, 84 (6) 381-8
25. Marescaux, C.; Vergnes, M.; Depaulis, A. Genetic absence epilepsy in rats from Strasbourg - a review J. Neural Transm. Suppl. 1992, 35, 37-69
26. Schwamborn, K.; Caprioli, R. M. Molecular imaging by mass spectrometry - looking beyond classical histology Nat. Rev. Cancer 2010, 10 (9) 639-46
27. Trede, D.; Kobarg, J. H.; Oetjen, J.; Thiele, H.; Maass, P.; Alexandrov, T. On the importance of mathematical methods for analysis of MALDI-imaging mass spectrometry data J. Integr. Bioinform. 2012, 9 (1) 189
28. Lemaire, R.; Menguellet, S. A.; Stauber, J.; Marchaudon, V.; Lucot, J. P.; Collinet, P.; Farine, M. O.; Vinatier, D.; Day, R.; Ducoroy, P.; Salzet, M.; Fournier, I. 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. 2007, 6 (11) 4127-34
29. 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) 3715-24
30. Cazares, L. H.; Troyer, D.; Mendrinos, S.; Lance, R. A.; Nyalwidhe, J. O.; Beydoun, H. A.; Clements, M. A.; Drake, R. R.; Semmes, O. J. 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. 2009, 15 (17) 5541-51
31. Rauser, S.; Marquardt, C.; Balluff, B.; Deininger, S. O.; Albers, C.; Belau, E.; Hartmer, R.; Suckau, D.; Specht, K.; Ebert, M. P.; Schmitt, M.; Aubele, M.; Hofler, H.; Walch, A. Classification of HER2 receptor status in breast cancer tissues by MALDI imaging mass spectrometry J. Proteome Res. 2010, 9 (4) 1854-63
32. Debois, D.; Bertrand, V.; Quinton, L.; De Pauw-Gillet, M. C.; De Pauw, E. MALDI-in source decay applied to mass spectrometry imaging: a new tool for protein identification Anal. Chem. 2010, 82 (10) 4036-45
33. Le Faouder, J.; Laouirem, S.; Chapelle, M.; Albuquerque, M.; Belghiti, J.; Degos, F.; Paradis, V.; Camadro, J.-M.; Bedossa, P. Imaging Mass Spectrometry Provides Fingerprints for Distinguishing Hepatocellular Carcinoma from Cirrhosis J. Proteome Res. 2011, 10 (8) 3755-65
34. Bonnel, D.; Longuespee, R.; Franck, J.; Roudbaraki, M.; Gosset, P.; Day, R.; Salzet, M.; Fournier, I. 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. 2011, 401 (1) 149-65
35. Calligaris, D.; Villard, C.; Terras, L.; Braguer, D.; Verdier-Pinard, P.; Lafitte, D. MALDI in-source decay of high mass protein isoforms: application to alpha- and beta-tubulin variants Anal. Chem. 2010, 82 (14) 6176-84
36. Zimmerman, T. A.; Debois, D.; Mazzucchelli, G.; Bertrand, V.; De Pauw-Gillet, M. C.; De Pauw, E. An analytical pipeline for MALDI in-source decay mass spectrometry imaging Anal. Chem. 2011, 83 (15) 6090-7
37. Schober, Y.; Schramm, T.; Spengler, B.; Rompp, A. Protein identification by accurate mass matrix-assisted laser desorption/ionization imaging of tryptic peptides Rapid Commun. Mass Spectrom. 2011, 25 (17) 2475-83
38. LeDuc, R. D.; Taylor, G. K.; Kim, Y. B.; Januszyk, T. E.; Bynum, L. H.; Sola, J. V.; Garavelli, J. S.; Kelleher, N. L. ProSight PTM: an integrated environment for protein identification and characterization by top-down mass spectrometry Nucleic Acids Res. 2004, 32 (Web Server issue) W340-5
39. Taylor, G. K.; Kim, Y. B.; Forbes, A. J.; Meng, F.; McCarthy, R.; Kelleher, N. L. Web and database software for identification of intact proteins using top down mass spectrometry Anal. Chem. 2003, 75 (16) 4081-6
40. Durbin, K. R.; Tran, J. C.; Zamdborg, L.; Sweet, S. M.; Catherman, A. D.; Lee, J. E.; Li, M.; Kellie, J. F.; Kelleher, N. L. Intact mass detection, interpretation, and visualization to automate Top-Down proteomics on a large scale Proteomics 2010, 10 (20) 3589-97
41. Meier, S. M.; Tsybin, Y. O.; Dyson, P. J.; Keppler, B. K.; Hartinger, C. G. Fragmentation methods on the balance: unambiguous top-down mass spectrometric characterization of oxaliplatin-ubiquitin binding sites Anal. Bioanal. Chem. 2011, 402 (8) 2655-62
42. Michalski, A.; Damoc, E.; Lange, O.; Denisov, E.; Nolting, D.; Mueller, M.; Viner, R.; Schwartz, J.; Remes, P.; Belford, M.; Dunyach, J. J.; Cox, J.; Horning, S.; Mann, M.; Makarov, A. Ultra high resolution linear ion trap Orbitrap mass spectrometer (Orbitrap Elite) facilitates top down LC MS/MS and versatile peptide fragmentation modes Mol. Cell. Proteomics 2011, 11 (3) O111.013698
43. Bushee, J. L.; Argikar, U. A. An experimental approach to enhance precursor ion fragmentation for metabolite identification studies: application of dual collision cells in an orbital trap Rapid Commun. Mass Spectrom. 2011, 25 (10) 1356-62
44. Frese, C. K.; Altelaar, A. F.; Hennrich, M. L.; Nolting, D.; Zeller, M.; Griep-Raming, J.; Heck, A. J. Mohammed, S. Improved peptide identification by targeted fragmentation using CID, HCD and ETD on an LTQ-Orbitrap Velos J Proteome Res 2011, 10 (5) 2377-88
45. Olsen, J. V.; Macek, B.; Lange, O.; Makarov, A.; Horning, S.; Mann, M. Higher-energy C-trap dissociation for peptide modification analysis Nat. Methods 2007, 4 (9) 709-12
46. Segu, Z. M.; Mechref, Y. Characterizing protein glycosylation sites through higher-energy C-trap dissociation Rapid Commun. Mass Spectrom. 2010, 24 (9) 1217-25
47. Liu, X.; Sirotkin, Y.; Shen, Y.; Anderson, G.; Tsai, Y. S.; Ting, Y. S.; Goodlett, D. R.; Smith, R. D.; Bafna, V.; Pevzner, P. A. Protein identification using top-down spectra Mol. Cell. Proteomics 2011, 11 (6) M111.008524
48. Fricker, L. D. Analysis of mouse brain peptides using mass spectrometry-based peptidomics: implications for novel functions ranging from non-classical neuropeptides to microproteins Mol. Biosyst. 2010, 6 (8) 1355-65
49. Li, L.; Chin, L. S.; Shupliakov, O.; Brodin, L.; Sihra, T. S.; Hvalby, O.; Jensen, V.; Zheng, D.; McNamara, J. O.; Greengard, P. Impairment of synaptic vesicle clustering and of synaptic transmission, and increased seizure propensity, in synapsin I-deficient mice Proc. Natl. Acad. Sci. U.S.A. 1995, 92 (20) 9235-9
50. Rosahl, T. W.; Spillane, D.; Missler, M.; Herz, J.; Selig, D. K.; Wolff, J. R.; Hammer, R. E.; Malenka, R. C.; Sudhof, T. C. Essential functions of synapsins I and II in synaptic vesicle regulation Nature 1995, 375 (6531) 488-93
51. Fassio, A.; Patry, L.; Congia, S.; Onofri, F.; Piton, A.; Gauthier, J.; Pozzi, D.; Messa, M.; Defranchi, E.; Fadda, M.; Corradi, A.; Baldelli, P.; Lapointe, L.; St-Onge, J.; Meloche, C.; Mottron, L.; Valtorta, F.; Khoa Nguyen, D.; Rouleau, G. A.; Benfenati, F.; Cossette, P. SYN1 loss-of-function mutations in autism and partial epilepsy cause impaired synaptic function Hum. Mol. Genet. 2011, 20 (12) 2297-307
52. Garcia, C. C.; Blair, H. J.; Seager, M.; Coulthard, A.; Tennant, S.; Buddles, M.; Curtis, A.; Goodship, J. A. Identification of a mutation in synapsin I, a synaptic vesicle protein, in a family with epilepsy J. Med. Genet. 2004, 41 (3) 183-6
53. Henderson, N. D. Spurious associations in unreplicated selected lines Behavior Genetics 1997, 27 (2) 145-54
54. Wu, L.; Peng, J.; Wei, C.; Liu, G.; Wang, G.; Li, K.; Yin, F. Characterization, using comparative proteomics, of differentially expressed proteins in the hippocampus of the mesial temporal lobe of epileptic rats following treatment with valproate Amino Acids 2011, 40 (1) 221-38
55. Wei, P.; Blundon, J. A.; Rong, Y.; Zakharenko, S. S.; Morgan, J. I. Impaired locomotor learning and altered cerebellar synaptic plasticity in pep-19/PCP4-null mice Mol. Cell. Biol. 2011, 31 (14) 2838-44
56. Chen, P. C.; Bhattacharyya, B. J.; Hanna, J.; Minkel, H.; Wilson, J. A.; Finley, D.; Miller, R. J.; Wilson, S. M. Ubiquitin homeostasis is critical for synaptic development and function J. Neurosci. 2011, 31 (48) 17505-13
57. Olsen, R. W. Combining Ubiquitin Deficiency and GABA-Mediated Inhibition Equals Seizures? Epilepsy Curr. 2011, 11 (3) 96-8
58. Goldstein, A. L.; Hannappel, E.; Sosne, G.; Kleinman, H. K. Thymosin beta4: a multi-functional regenerative peptide. Basic properties and clinical applications Expert Opin. Biol. Ther. 2012, 12 (1) 37-51