Human SOD1-G93A specific distribution evidenced in murine brain of a transgenic model for amyotrophic lateral sclerosis by MALDI imaging mass spectrometry

Journal of Proteome Research

Volumn 13, Issue 4, 2014, Pages 1800-1809

  Acquadro, Elena ^a   Caron, Ilaria ^b   Tortarolo, Massimo ^b   Bucci, Enrico M ^a,c   Bendotti, Caterina ^b   Corpillo, Davide ^a  

^a Bioindustry Park Silvano Fumero SpA   (Italy)

^b MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^c BioDigitalValley Srl   (Italy)

Author keywords

amyotrophic lateral sclerosis; hSOD1G93A; imaging; MALDI TOF; mouse

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; RIBOSOME PROTEIN; TRYPSIN; SUPEROXIDE DISMUTASE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; BRAIN REGION; BRAIN SLICE; CONTROLLED STUDY; FACIAL NERVE NUCLEUS; FEMALE; FRACTIONATION; GLIA CELL; MASS SPECTROMETRY; MOUSE; MSOD1 MOUSE; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN ISOLATION; PROTEIN LOCALIZATION; PROTEOMICS; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; TRIGEMINAL NUCLEUS; UPREGULATION; WILD TYPE; ANIMAL; BRAIN; C57BL MOUSE; CHEMISTRY; DISEASE MODEL; GENETICS; HUMAN; METABOLISM; MOLECULAR IMAGING; PROCEDURES; TISSUE DISTRIBUTION; TRANSGENIC MOUSE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; BRAIN; BRAIN CHEMISTRY; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOLECULAR IMAGING; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SUPEROXIDE DISMUTASE; TISSUE DISTRIBUTION;

EID: 84898716762     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr400942n     Document Type: Article

References (52)

1. Ryberg, H.; Bowser, R. Protein biomarkers for amyotrophic lateral sclerosis Expert. Rev. Proteomics 2008, 5, 249-262
2. Bruijn, L. I.; Miller, T. M.; Cleveland, D. W. Unraveling the mechanisms involved in motor neuron degeneration in ALS Annu. Rev. Neurosci. 2004, 27, 723-749
3. Gurney, M. E.; Pu, H.; Chiu, A. Y.; Dal Canto, M. C.; Polchow, C. Y.; Alexander, D. D.; Caliendo, J.; Hentati, A.; Kwon, Y. W.; Deng, H. X. Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation Science 1994, 264, 1772-1775
4. Ripps, M. E.; Huntley, G. W.; Hof, P. R.; Morrison, J. H.; Gordon, J. W. Transgenic mice expressing an altered murine superoxide dismutase gene provide an animal model of amyotrophic lateral sclerosis Proc. Natl. Acad. Sci. U.S.A. 1995, 92, 689-693
5. Gurney, M. E. The use of transgenic mouse models of amyotrophic lateral sclerosis in preclinical drug studies J. Neurol. Sci. 1997, 152, S67-73
6. Bendotti, C.; Carrì, M. T. Lessons from models of SOD1-linked familial ALS Trends Mol. Med. 2004, 10, 393-400
7. Zhou, J. Y.; Afjehi-Sadat, L.; Asress, S.; Duong, D. M.; Cudkowicz, M.; Glass, J. D.; Peng, J. Galectin-3 is a candidate biomarker for amyotrophic lateral sclerosis: discovery by a proteomics approach J. Proteome Res. 2010, 9, 5133-5141
8. Staunton, L.; Jockusch, H.; Ohlendieck, K. Proteomic analysis of muscle affected by motor neuron degeneration: the wobbler mouse model of amyotrophic lateral sclerosis Biochem. Biophys. Res. Commun. 2011, 406, 595-600
9. Casoni, F.; Basso, M.; Massignan, T.; Gianazza, E.; Cheroni, C.; Salmona, M.; Bendotti, C.; Sonetto, V. Protein nitration in a mouse model of familial amyotrophic lateral sclerosis: possible multifunctional role in the pathogenesis J. Biol. Chem. 2005, 280, 16295-16304
10. Basso, M.; Samengo, G.; Nardo, G.; Massignan, T.; D'Alessandro, G.; Tartari, S.; Cantoni, L.; Marino, M.; Cheroni, C.; De Biasi, S.; Giordana, M. T.; Strong, M. J.; Estevez, A. G.; Salmona, M.; Bendotti, C.; Bonetto, V. Characterization of detergent-insoluble proteins in ALS indicates a causal link between nitrative stress and aggregation in pathogenesis PLoS One 2009, 4, e8130
11. Caprioli, R. M.; Farmer, T. B.; Gile, J. Molecular imaging of biological samples: localization of peptides and proteins using MALDI-TOF MS Anal. Chem. 1997, 69, 4751-4760
12. Fournier, I.; Day, R.; Salzet, M. Direct analysis of neuropeptides by in situ MALDI-TOF mass spectrometry in the rat brain Neuroendocrinol. Lett. 2003, 24, 9-14
13. Walch, A.; Rauser, S.; Deininger, S. O.; Höfler, H. MALDI imaging mass spectrometry for direct tissue analysis: a new frontier for molecular histology Histochem. Cell. Biol. 2008, 130, 421-434
14. Seeley, E. H.; Schwamborn, K.; Caprioli, R. M. Imaging of intact tissue sections: moving beyond the microscope J. Biol. Chem. 2011, 286, 25459-25466
15. Acquadro, E.; Cabella, C.; Ghiani, S.; Miragoli, L.; Bucci, E. M.; Corpillo, D. Matrix-assisted laser desorption ionization imaging mass spectrometry detection of a magnetic resonance imaging contrast agent in mouse liver Anal. Chem. 2009, 81, 2779-2784
16. Reyzer, M. L.; Caprioli, R. M. MALDI-MS-based imaging of small molecules and proteins in tissues Curr. Opin. Chem. Biol. 2007, 11, 29-35
17. Nilsson, A.; Fehniger, T. E.; Gustavsson, L.; Andrén, P. E. Fine mapping the spatial distribution and concentration of unlabeled drugs within tissue micro-compartments using imaging mass spectrometry PLoS One 2010, 5, e11411
18. El Ayed, M.; Bonnel, D.; Longuespée, R.; Castelier, C.; Franck, J.; Vergara, D.; Desmons, A.; Tasiemski, A.; Kenani, A.; Vinatier, D.; Day, R.; Fournier, I.; Salzet, M. MALDI imaging mass spectrometry in ovarian cancer for tracking, identifying, and validating biomarkers Med. Sci. Monit. 2010, 16, BR233-BR245
19. Gustafsson, J. O.; Oehler, M. K.; Ruszkiewicz, A.; McColl, S. R.; Hoffmann, P. MALDI imaging mass spectrometry (MALDI-IMS)-application of spatial proteomics for ovarian cancer classification and diagnosis Int. J. Mol. Sci. 2011, 12, 773-794
20. Pierson, J.; Norris, J. L.; Aerni, H. R.; Svenningsson, P.; Caprioli, R. M.; Andrén, P. E. Molecular profiling of experimental Parkinson's disease: direct analysis of peptides and proteins on brain tissue sections by MALDI mass spectrometry Proteome Res. 2004, 3, 289-295
21. Stoeckli, M.; Knochenmuss, R.; McCombie, G.; Mueller, D.; Rohner, T.; Staab, D.; Wiederhold, K. H. MALDI MS imaging of amyloid Methods Enzymol. 2006, 412, 94-106
22. Hanrieder, J.; Ekegren, T.; Andersson, M.; Bergquist, J. MALDI imaging of post-mortem human spinal cord in amyotrophic lateral sclerosis J. Neurochem. 2013, 124, 695-707
23. Ferrucci, M.; Spalloni, A.; Bartalucci, A.; Cantafora, E.; Fulceri, F.; Nutini, M.; Longone, P.; Paparelli, A.; Fornai, F. A systematic study of brainstem motor nuclei in a mouse model of ALS, the effects of lithium Neurobiol. Dis. 2010, 37, 370-383
24. Paxinos, G.; Franklin, K. B. J. The Mouse Brain in Stereotaxic Coordinates, 2 nd ed.; Academic Press: San Diego, 2001.
25. Dal Canto, M. C.; Gurney, M. E. Neuropathological changes in two lines of mice carrying a transgene for mutant human Cu,Zn SOD, and in mice overexpressing wild type human SOD: a model of familial amyotrophic lateral sclerosis (FALS) Brain Res. 1995, 676, 25-40
26. Haenggeli, C.; Kato, A. C. Differential vulnerability of cranial motoneurons in mouse models with motor neuron degeneration Neurosci. Lett. 2002, 335, 39-43
27. Bucher, S.; Braunstein, K. E.; Niessen, H. G.; Kaulisch, T.; Neumaier, M.; Boeckers, T. M.; Stiller, D.; Ludolph, A. C. Vacuolization correlates with spin-spin relaxation time in motor brainstem nuclei and behavioural tests in the transgenic G93A-SOD1 mouse model of ALS Eur. J. Neurosci. 2007, 26, 1895-1901
28. Bruijn, L. I.; Houseweart, M. K.; Kato, S.; Anderson, K. L.; Anderson, S. D.; Ohama, E.; Reaume, A. G.; Scott, R. W.; Cleveland, D. W. Aggregation and motor neuron toxicity of an ALS-linked SOD1 mutant independent from wild-type SOD1 Science 1998, 281, 1851-1854
29. Deng, H. X.; Shi, Y.; Furukawa, Y.; Zhai, H.; Fu, R.; Liu, E.; Gorrie, G. H.; Khan, M. S.; Hung, W. Y.; Bigio, E. H.; Lukas, T.; Dal Canto, M. C.; O'Halloran, T. V.; Siddique, T. Conversion to the amyotrophic lateral sclerosis phenotype is associated with intermolecular linked insoluble aggregates of SOD1 in mitochondria Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 7142-7147
30. Hardesty, W. M.; Kelley, M. C.; Mi, D.; Low, R. L.; Caprioli, R. M. Protein signatures for survival and recurrence in metastatic melanoma J. Proteomics 2011, 74, 1002-1014
31. Chaurand, P.; Sanders, M. E.; Jensen, R. A.; Caprioli, R. M. Proteomics in diagnostic pathology. Profiling and imaging proteins directly in tissue sections Am. J. Pathol. 2004, 165, 1057-1068
32. Wisztorski, M.; Croix, D.; Macagno, E.; Fournier, I.; Salzet, M. Molecular MALDI imaging: an emerging technology for neuroscience studies Dev. Neurobiol. 2008, 68, 845-858
33. Massignan, T.; Casoni, F.; Basso, M.; Stefanazzi, P.; Biasimi, E.; Tortarolo, M.; Salmona, M.; Gianazza, E.; Bendotti, C.; Sonetto, V. Proteomic analysis of spinal cord of presymptomatic amyotrophic lateral sclerosis G93A SOD1 mouse Biochem. Biophys. Res. Commun. 2007, 353, 719-725
34. Freibaum, B. D.; Chitta, R. K.; High, A. A.; Taylor, J. P. Global analysis of TDP-43 interacting proteins reveals strong association with RNA splicing and translation machinery J. Proteome Res. 2010, 9, 1104-1120
35. Nardo, G.; Pozzi, S.; Mantovani, S.; Gabelli, S.; Marinou, K.; Basso, M.; Mora, G.; Bendotti, C.; Bonetto, V. Nitroproteomics of peripheral blood mononuclear cells from patients and a rat model of ALS Antioxid. Redox Signaling 2009, 11, 1559-1567
36. Antinone, S. E.; Ghadge, G. D.; Lam, T. T.; Wang, L.; Roos, R. P.; Green, W. N. Palmitoylation of superoxide dismutase 1 (SOD1) is increased for familial amyotrophic lateral sclerosis-linked SOD1 mutants J. Biol. Chem. 2013, 288, 21606-21617
37. Basso, M.; Massignan, T.; Samengo, G.; Cheroni, C.; De Biasi, S.; Salmona, M.; Bendotti, C.; Bonetto, V. Insoluble mutant SOD1 is partly oligoubiquitinated in amyotrophic lateral sclerosis mice J. Biol. Chem. 2006, 281, 33325-33335
38. Cheroni, C.; Marino, M.; Tortarolo, M.; Veglianese, P.; De Biasi, S.; Fontana, E.; Zuccarello, L. V.; Maynard, C. J.; Dantuma, N. P.; Bendotti, C. Functional alterations of the ubiquitin-proteasome system in motor neurons of a mouse model of familial amyotrophic lateral sclerosis Hum. Mol. Genet. 2009, 18, 82-96
39. Bendotti, C.; Marino, M.; Cheroni, C.; Fontana, E.; Crippa, V.; Poletti, A.; De Biasi, S. Dysfunction of constitutive and inducible ubiquitin-proteasome system in amyotrophic lateral sclerosis: implication for protein aggregation and immune response Prog. Neurobiol 2012, 97, 101-126
40. Soulet, F.; Al Saati, T.; Roga, S.; Amalric, F.; Bouche, G. Fibroblast growth factor-2 interacts with free ribosomal protein S19 Biochem. Biophys. Res. Commun. 2001, 289, 591-596
41. Orrù, S.; Aspesi, A.; Armiraglio, M.; Caterino, M.; Loreni, F.; Ruoppolo, M.; Santoro, C.; Dianzani, I. Analysis of the ribosomal protein S19 interactome Mol. Cell. Proteomics 2007, 6, 382-393
42. Jordan, P. M.; Ojeda, L. D.; Thonhoff, J. R.; Gao, J.; Boehning, D.; Yu, Y.; Wu, P. Generation of spinal motor neurons from human fetal brain-derived neural stem cells: role of basic fibroblast growth factor J. Neurosci. Res. 2009, 87, 318-332
43. De Oliveira, G. P.; Duobles, T.; Castelucci, P.; Chadi, G. Differential regulation of FGF-2 in neurons and reactive astrocytes of axotomized rat hypoglossal nucleus. A possible therapeutic target for neuroprotection in peripheral nerve pathology Acta Histochem. 2010, 112, 604-617
44. Yamamoto, T. Molecular mechanism of monocyte predominant infiltration in chronic inflammation: mediation by a novel monocyte chemotactic factor, S19 ribosomal protein dimer Pathol. Int. 2000, 50, 863-871
45. Yamamoto, T. Roles of the ribosomal protein S19 dimer and the C5a receptor in pathophysiological functions of phagocytic leukocytes Pathol. Int. 2007, 57, 1-11
46. Mariotti, R.; Bentivoglio, M. Activation and response to axotomy of microglia in the facial motor nuclei of G93A superoxide dismutase transgenic mice Neurosci. Lett. 2000, 285, 87-90
47. Filip, A. M.; Klug, J.; Cayli, S.; Fröhlich, S.; Henke, T.; Lacher, P.; Eickhoff, R.; Bulau, P.; Linder, M.; Carlsson-Skwirut, C.; Leng, L.; Bucala, R.; Kraemer, S.; Bernhagen, J.; Meinhardt, A. Ribosomal protein S19 interacts with macrophage migration inhibitory factor and attenuates its pro-inflammatory function J. Biol. Chem. 2009, 284, 7977-85
48. Lv, J.; Huang, X. R.; Klug, J.; Fröhlich, S.; Lacher, P.; Xu, A.; Meinhardt, A.; Lan, H. Y. Ribosomal protein S19 is a novel therapeutic agent in inflammatory kidney disease Clin. Sci. 2013, 124, 627-37
49. Cherepkova, O. A.; Lyutova, E. M.; Eronina, T. B.; Gurvits, B. Y. Accelerated protein aggregation induced by macrophage migration inhibitory factor under heat stress conditions Biochemistry 2006, 71, 140-145
50. Schwamborn, K.; Caprioli, R. M. MALDI imaging mass spectrometry-painting molecular pictures Mol. Oncol. 2010, 4, 529-538
51. 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, 254-262
52. 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, 9093-9100