Protein changes in immunodepleted cerebrospinal fluid from a transgenic mouse model of Alexander disease detected using mass spectrometry

Journal of Proteome Research

Volumn 12, Issue 2, 2013, Pages 719-728

  Cunningham, Robert ^a   Jany, Paige ^b   Messing, Albee ^b   Li, Lingjun ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Alexander disease; cerebrospinal fluid; GFAP overexpressor; immunodepletion; mass spectrometry; proteomics; spectral counting; transgenic

Indexed keywords

ACID PROTEIN; ALPHA CRYSTALLIN; BETA CRYSTALLIN; BIOLOGICAL MARKER; CATHEPSIN B; CATHEPSIN L; CATHEPSIN S; CONTACTIN 1; GLIAL FIBRILLARY ACIDIC PROTEIN; HEAT SHOCK PROTEIN 27; IMMUNOGLOBULIN Y;

ALEXANDER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE OVEREXPRESSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CEREBROSPINAL FLUID LEVEL; PROTEIN EXPRESSION; PROTEIN TARGETING; REPRODUCIBILITY; TRANSGENIC MOUSE;

ALEXANDER DISEASE; ANIMALS; CEREBROSPINAL FLUID; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; IMMUNOGLOBULINS; MALE; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; PEPTIDE FRAGMENTS; PROTEOLYSIS; TANDEM MASS SPECTROMETRY; TRYPSIN;

EID: 84873340560     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr300785h     Document Type: Article

References (57)

1. Brenner, M.; Johnson, A. B.; Boespflug-Tanguy, O.; Rodriguez, D.; Goldman, J. E.; Messing, A. Mutations in GFAP, encoding glial fibrillary acidic protein, are associated with Alexander disease Nat. Genet. 2001, 27 (1) 117-120
2. Herndon, R. M.; Rubinstein, L. J.; Freeman, J. M.; Mathieson, G. Light and electron microscopic observations on Rosenthal fibers in Alexander's disease and in multiple sclerosis J. Neuropathol. Exp. Neurol. 1970, 29 (4) 524-551
3. Alexander, W. S. Progressive fibrinoid degeneration of fibrillary astrocytes associated with mental retardation in a hydrocephalic infant Brain 1949, 72 (3) 373-381
4. Iwaki, T.; Kume-Iwaki, A.; Liem, R. K.; Goldman, J. E. Alpha B-Crystallin is expressed in non-lenticular tissues and accumulates in Alexander's disease brain Cell 1989, 57 (1) 71-78
5. Head, M. W.; Goldman, J. E. Small heat shock proteins, the cytoskeleton, and inclusion body formation Neuropathol. Appl. Neurobiol. 2000, 26 (4) 304-312
6. Messing, A.; Daniels, C. M.; Hagemann, T. L. Strategies for treatment in alexander disease Neurotherapeutics 2010, 7 (4) 507-515
7. Tang, G.; Yue, Z.; Talloczy, Z.; Hagemann, T.; Cho, W.; Messing, A.; Sulzer, D. L.; Goldman, J. E. Autophagy induced by Alexander disease-mutant GFAP accumulation is regulated by p38/MAPK and mTOR signaling pathways Hum. Mol. Genet. 2008, 17 (11) 1540-1555
8. Hagemann, T. L.; Boelens, W. C.; Wawrousek, E. F.; Messing, A. Suppression of GFAP toxicity by alphaB-Crystallin in mouse models of Alexander disease Hum. Mol. Genet. 2009, 18 (7) 1190-1199
9. Zougman, A.; Pilch, B.; Podtelejnikov, A.; Kiehntopf, M.; Schnabel, C.; Kumar, C.; Mann, M. Integrated analysis of the cerebrospinal fluid peptidome and proteome J. Proteome Res. 2008, 7 (1) 386-399
10. Sjodin, M. O.; Bergquist, J.; Wetterhall, M. Mining ventricular cerebrospinal fluid from patients with traumatic brain injury using hexapeptide ligand libraries to search for trauma biomarkers J. Chromatogr., B: Anal. Technol. Biomed. Life Sci. 2003, 878 (22) 12
11. Kyllerman, M.; Rosengren, L.; Wiklund, L. M.; Holmberg, E. Increased levels of GFAP in the cerebrospinal fluid in three subtypes of genetically confirmed Alexander disease Neuropediatrics 2005, 36 (5) 319-323
12. DeMattos, R. B.; Bales, K. R.; Parsadanian, M.; O'Dell, M. A.; Foss, E. M.; Paul, S. M.; Holtzman, D. M. Plaque-associated disruption of CSF and plasma amyloid-beta (Abeta) equilibrium in a mouse model of Alzheimer's disease J. Neurochem. 2002, 81 (2) 229-236
13. Wong, M.; Schlaggar, B. L.; Buller, R. S.; Storch, G. A.; Landt, M. Cerebrospinal fluid protein concentration in pediatric patients: defining clinically relevant reference values Arch. Pediatr. Adolesc. Med. 2000, 154 (8) 827-831
14. Roche, S.; Gabelle, A.; Lehmann, S. Clinical proteomics of the cerebrospinal fluid: Towards the discovery of new biomarkers Proteomics: Clin. Appl. 2008, 2 (3) 428-436
15. Li, C.; Lee, K. H. Affinity depletion of albumin from human cerebrospinal fluid using Cibacron-blue-3G-A-derivatized photopatterned copolymer in a microfluidic device Anal. Biochem. 2004, 333 (2) 381-388
16. Maccarrone, G.; Milfay, D.; Birg, I.; Rosenhagen, M.; Holsboer, F.; Grimm, R.; Bailey, J.; Zolotarjova, N.; Turck, C. W. Mining the human cerebrospinal fluid proteome by immunodepletion and shotgun mass spectrometry Electrophoresis 2004, 25 (14) 2402-2412
17. Huang, L.; Harvie, G.; Feitelson, J. S.; Gramatikoff, K.; Herold, D. A.; Allen, D. L.; Amunngama, R.; Hagler, R. A.; Pisano, M. R.; Zhang, W. W.; Fang, X. Immunoaffinity separation of plasma proteins by IgY microbeads: meeting the needs of proteomic sample preparation and analysis Proteomics 2005, 5 (13) 3314-3328
18. Rajic, A.; Stehmann, C.; Autelitano, D. J.; Vrkic, A. K.; Hosking, C. G.; Rice, G. E.; Ilag, L. L. Protein depletion using IgY from chickens immunised with human protein cocktails Prep. Biochem. Biotechnol. 2009, 39 (3) 221-247
19. Huang, L.; Fang, X. Immunoaffinity fractionation of plasma proteins by chicken IgY antibodies Methods Mol. Biol. 2008, 425, 41-51
20. Greunke, K.; Braren, I.; Alpers, I.; Blank, S.; Sodenkamp, J.; Bredehorst, R.; Spillner, E. Recombinant IgY for improvement of immunoglobulin-based analytical applications Clin. Biochem. 2008, 41 (14-15) 1237-1244
21. Xiao, Y.; Gao, X.; Taratula, O.; Treado, S.; Urbas, A.; Holbrook, R. D.; Cavicchi, R. E.; Avedisian, C. T.; Mitra, S.; Savla, R.; Wagner, P. D.; Srivastava, S.; He, H. Anti-HER2 IgY antibody-functionalized single-walled carbon nanotubes for detection and selective destruction of breast cancer cells BMC Cancer 2009, 9, 351
22. Liu, T.; Qian, W. J.; Mottaz, H. M.; Gritsenko, M. A.; Norbeck, A. D.; Moore, R. J.; Purvine, S. O.; Camp, D. G., 2nd; Smith, R. D. Evaluation of multiprotein immunoaffinity subtraction for plasma proteomics and candidate biomarker discovery using mass spectrometry Mol. Cell. Proteomics 2006, 5 (11) 2167-2174
23. Hinerfeld, D.; Innamorati, D.; Pirro, J.; Tam, S. W. Serum/Plasma depletion with chicken immunoglobulin Y antibodies for proteomic analysis from multiple Mammalian species J. Biomol. Tech. 2004, 15 (3) 184-190
24. Metz, T. O.; Qian, W. J.; Jacobs, J. M.; Gritsenko, M. A.; Moore, R. J.; Polpitiya, A. D.; Monroe, M. E.; Camp, D. G., 2nd; Mueller, P. W.; Smith, R. D. Application of proteomics in the discovery of candidate protein biomarkers in a diabetes autoantibody standardization program sample subset J. Proteome Res. 2008, 7 (2) 698-707
25. Ru, Q. C.; Zhu, L. A.; Silberman, J.; Shriver, C. D. Label-free semiquantitative peptide feature profiling of human breast cancer and breast disease sera via two-dimensional liquid chromatography-mass spectrometry Mol. Cell. Proteomics 2006, 5 (6) 1095-1104
26. Brechlin, P.; Jahn, O.; Steinacker, P.; Cepek, L.; Kratzin, H.; Lehnert, S.; Jesse, S.; Mollenhauer, B.; Kretzschmar, H. A.; Wiltfang, J.; Otto, M. Cerebrospinal fluid-optimized two-dimensional difference gel electrophoresis (2-D DIGE) facilitates the differential diagnosis of Creutzfeldt-Jakob disease Proteomics 2008, 8 (20) 4357-4366
27. Rao, P. V.; Reddy, A. P.; Lu, X.; Dasari, S.; Krishnaprasad, A.; Biggs, E.; Roberts, C. T.; Nagalla, S. R. Proteomic identification of salivary biomarkers of type-2 diabetes J. Proteome Res. 2009, 8 (1) 239-245
28. Yu, K. H.; Barry, C. G.; Austin, D.; Busch, C. M.; Sangar, V.; Rustgi, A. K.; Blair, I. A. Stable isotope dilution multidimensional liquid chromatography-tandem mass spectrometry for pancreatic cancer serum biomarker discovery J. Proteome Res. 2009, 8 (3) 1565-1576
29. Aebersold, R.; Mann, M. Mass spectrometry-based proteomics Nature 2003, 422 (6928) 198-207
30. Ong, S. E.; Blagoev, B.; Kratchmarova, I.; Kristensen, D. B.; Steen, H.; Pandey, A.; Mann, M. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics Mol. Cell. Proteomics 2002, 1 (5) 376-386
31. Hsu, J. L.; Huang, S. Y.; Chow, N. H.; Chen, S. H. Stable-isotope dimethyl labeling for quantitative proteomics Anal. Chem. 2003, 75 (24) 6843-6852
32. Liu, H.; Sadygov, R. G.; Yates, J. R., 3rd A model for random sampling and estimation of relative protein abundance in shotgun proteomics Anal. Chem. 2004, 76 (14) 4193-4201
33. Xiang, F.; Ye, H.; Chen, R.; Fu, Q.; Li, L. N, N -dimethyl leucines as novel isobaric tandem mass tags for quantitative proteomics and peptidomics Anal. Chem. 2010, 82 (7) 2817-2825
34. Ross, P. L.; Huang, Y. N.; Marchese, J. N.; Williamson, B.; Parker, K.; Hattan, S.; Khainovski, N.; Pillai, S.; Dey, S.; Daniels, S.; Purkayastha, S.; Juhasz, P.; Martin, S.; Bartlet-Jones, M.; He, F.; Jacobson, A.; Pappin, D. J. Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents Mol. Cell. Proteomics 2004, 3 (12) 1154-1169
35. Zybailov, B.; Coleman, M. K.; Florens, L.; Washburn, M. P. Correlation of relative abundance ratios derived from peptide ion chromatograms and spectrum counting for quantitative proteomic analysis using stable isotope labeling Anal. Chem. 2005, 77 (19) 6218-6224
36. Old, W. M.; Meyer-Arendt, K.; Aveline-Wolf, L.; Pierce, K. G.; Mendoza, A.; Sevinsky, J. R.; Resing, K. A.; Ahn, N. G. Comparison of label-free methods for quantifying human proteins by shotgun proteomics Mol. Cell. Proteomics 2005, 4 (10) 1487-1502
37. Zybailov, B.; Mosley, A. L.; Sardiu, M. E.; Coleman, M. K.; Florens, L.; Washburn, M. P. Statistical analysis of membrane proteome expression changes in Saccharomyces cerevisiae J. Proteome Res. 2006, 5 (9) 2339-2347
38. Mosley, A. L.; Florens, L.; Wen, Z.; Washburn, M. P. A label free quantitative proteomic analysis of the Saccharomyces cerevisiae nucleus J. Proteomics 2009, 72 (1) 110-120
39. Zhang, Y.; Wen, Z.; Washburn, M. P.; Florens, L. Refinements to label free proteome quantitation: how to deal with peptides shared by multiple proteins Anal. Chem. 2010, 82 (6) 2272-2281
40. Messing, A.; Head, M. W.; Galles, K.; Galbreath, E. J.; Goldman, J. E.; Brenner, M. Fatal encephalopathy with astrocyte inclusions in GFAP transgenic mice Am. J. Pathol. 1998, 152 (2) 391-398
41. Perkins, D. N.; Pappin, D. J.; Creasy, D. M.; Cottrell, J. S. Probability-based protein identification by searching sequence databases using mass spectrometry data Electrophoresis 1999, 20 (18) 3551-3567
42. Elias, J. E.; Gygi, S. P. Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry Nat. Methods 2007, 4 (3) 207-214
43. You, J. S.; Gelfanova, V.; Knierman, M. D.; Witzmann, F. A.; Wang, M.; Hale, J. E. The impact of blood contamination on the proteome of cerebrospinal fluid Proteomics 2005, 5 (1) 290-296
44. Takanashi, J.; Sugita, K.; Tanabe, Y.; Niimi, H. Adolescent case of Alexander disease: MR imaging and MR spectroscopy Pediatr. Neurol. 1998, 18 (1) 67-70
45. Hemmer, W.; Wallimann, T. Functional Aspects of Creatine Kinase in Brain Dev. Neurosci. (Basel, Switz.) 1993, 15 (3-5) 249-260
46. Hemmer, W.; Zanolla, E.; Furter-Graves, E. M.; Eppenberger, H. M.; Wallimann, T. Creatine kinase isoenzymes in chicken cerebellum: specific localization of brain-type creatine kinase in Bergmann glial cells and muscle-type creatine kinase in Purkinje neurons Eur. J. Neurosci. 1994, 6 (4) 538-549
47. Nordby, H. K.; Tveit, B.; Ruud, I. Creatine kinase and lactate dehydrogenase in the cerebrospinal fluid in patients with head injuries Acta Neurochirurgica 1975, 32 (3) 209-217
48. Bell, R. D.; Alexander, G. M.; Nguyen, T.; Albin, M. S. Quantification of cerebral infarct size by creatine kinase BB isoenzyme Stroke 1986, 17 (2) 254-260
49. Steen, C.; Wilczak, N.; Hoogduin, J. M.; Koch, M.; De Keyser, J. Reduced Creatine Kinase B Activity in Multiple Sclerosis Normal Appearing White Matter PLoS One 2010, 5 (5 e10811
50. Chwieralski, C.; Welte, T.; Bühling, F. Cathepsin-regulated apoptosis Apoptosis 2006, 11 (2) 143-149
51. Droga-Mazovec, G.; Bojic, L.; Petelin, A.; Ivanova, S.; Romih, R.; Repnik, U.; Salvesen, G. S.; Stoka, V.; Turk, V.; Turk, B. Cysteine cathepsins trigger caspase-dependent cell death through cleavage of bid and antiapoptotic Bcl-2 homologues J. Biol. Chem. 2008, 283 (27) 19140-19150
52. Duffy, M. J. Proteases as prognostic markers in cancer Clin. Cancer Res. 1996, 2 (4) 613-618
53. Guicciardi, M. E.; Deussing, J.; Miyoshi, H.; Bronk, S. F.; Svingen, P. A.; Peters, C.; Kaufmann, S. H.; Gores, G. J. Cathepsin B contributes to TNF-alpha-mediated hepatocyte apoptosis by promoting mitochondrial release of cytochrome c J. Clin. Invest. 2000, 106 (9) 1127-1137
54. Butt, A. M.; Jenkins, H. G. Morphological changes in oligodendrocytes in the intact mouse optic nerve following intravitreal injection of tumour necrosis factor J. Neuroimmunol. 1994, 51 (1) 27-33
55. Hagemann, T. L.; Gaeta, S. A.; Smith, M. A.; Johnson, D. A.; Johnson, J. A.; Messing, A. Gene expression analysis in mice with elevated glial fibrillary acidic protein and Rosenthal fibers reveals a stress response followed by glial activation and neuronal dysfunction Hum. Mol. Genet. 2005, 14 (16) 2443-2458
56. Falk, J.; Bonnon, C.; Girault, J. A.; Faivre-Sarrailh, C. F3/contactin, a neuronal cell adhesion molecule implicated in axogenesis and myelination Biol. Cell 2002, 94 (6) 327-334
57. Eckerich, C.; Zapf, S.; Ulbricht, U.; Müller, S.; Fillbrandt, R.; Westphal, M.; Lamszus, K. Contactin is expressed in human astrocytic gliomas and mediates repulsive effects Glia 2006, 53 (1) 1-12