Integration of proteomics, bioinformatics, and systems biology in traumatic brain injury biomarker discovery

Frontiers in Neurology

Volumn 4 MAY, Issue , 2013, Pages

  Guingab Cagmat, J D ^a   Cagmat, E B ^a   Hayes, R L ^a   Anagli, J ^a  

^a BANYAN BIOMARKERS INC   (United States)

Author keywords

Bioinformatics; Biomarkers; Proteomics; Systems biology; Traumatic brain injury

Indexed keywords

ALPHAII SPECTRIN; BIOLOGICAL MARKER; C REACTIVE PROTEIN; CALPAIN; CASPASE 3; COLLAPSIN RESPONSE MEDIATOR PROTEIN 2; GLIAL FIBRILLARY ACIDIC PROTEIN; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HEXOKINASE; MICROTUBULE ASSOCIATED PROTEIN 2; MICROTUBULE ASSOCIATED PROTEIN 2A; MICROTUBULE ASSOCIATED PROTEIN 2B; NEURON SPECIFIC ENOLASE; PROTEIN S 100BETA; SPECTRIN; SYNAPTOTAGMIN; SYNTAXIN 6; TRANSFERRIN; TYROSINE 3 MONOOXYGENASE; UBIQUITIN CARBOXYL TERMINAL HYDROLASE L1 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BIOINFORMATICS; CEREBROSPINAL FLUID; COLLISIONALLY ACTIVATED DISSOCIATION; COMPUTER PROGRAM; DIAGNOSTIC ACCURACY; ELECTROPHORESIS; ELECTROSPRAY; FALSE DETECTION RATE; FUNCTIONAL ASSESSMENT; HUMAN; INTRACRANIAL PRESSURE; ION CYCLOTRON RESONANCE MASS SPECTROMETRY; ISOBARIC TAGGING FOR RELATIVE AND ABSOLUTE QUANTIFICATION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; ONE DIMENSIONAL ELECTROPHORESIS; PATHOGENESIS; PEPTIDE MASS FINGERPRINTING; PROGNOSIS; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN PROCESSING; PROTEOMICS; SENSITIVITY AND SPECIFICITY; TANDEM MASS SPECTROMETRY; TRAUMATIC BRAIN INJURY; TWO DIMENSIONAL ELECTROPHORESIS; TWO DIMENSIONAL LIQUID CHROMATOGRAPHY; WORKFLOW;

EID: 84878802221     PISSN: None     EISSN: 16642295     Source Type: Journal    
DOI: 10.3389/fneur.2013.00061     Document Type: Article

References (143)

1. Agoston, D. V., Gyorgy, A., Eidelman, O., and Pollard, H. B. (2009). Proteomic biomarkers for blast neurotrauma: targeting cerebral edema, inflammation, and neuronal death cascades. J. Neurotrauma 26, 901-911. doi:10.1089/neu.2008.0724
2. Alexander, M. P. (1995). Mild traumatic brain injury: pathophysiology, natural history, and clinical management. Neurology 45, 1253-1260. doi:10.1212/WNL.45.7.1253
3. Alzate, O.. (ed.). (2010). "Neuroproteomics," in Neuroproteomics, Chap. 1. Boca Raton: CRC Press.
4. Appella, E., Padlan, E. A., and Hunt, D. F. (1995). Analysis of the structure of naturally processed peptides bound by class I and class II major histocompatibility complex molecules. EXS 73, 105-119.
5. Arciniegas, D. B., and Silver, J. M. (2001). Regarding the search for a unified definition of mild traumatic brain injury. Brain Inj. 15, 649-652. doi:10.1080/02699050010019800
6. Bairoch, A., and Apweiler, R. (1997). The SWISS-PROT protein sequence database: its relevance to human molecular medical research. J. Mol. Med. 75, 312-316.
7. Bairoch, A., and Boeckmann, B. (1991). The SWISS-PROT protein sequence data bank. Nucleic Acids Res. 19, 2247-2249. doi:10.1093/nar/19.suppl.2247
8. Bayes, A., and Grant, S. G. (2009). Neuroproteomics: understanding the molecular organization and complexity of the brain. Nat. Rev. Neurosci. 10, 635-646. doi:10.1038/nrn2701
9. Bencsath, F. A., and Field, F. H. (1988). Ion retardation and collision-induced dissociation in the thermospray ion source. Anal. Chem. 60, 1323-1329. doi:10.1021/ac00164a016
10. Benzinger, T. L., Brody, D., Cardin, S., Curley, K. C., Mintun, M. A., Mun, S. K., et al. (2009). Blast-related brain injury: imaging for clinical and research applications: report of the 2008 St. Louis workshop. J. Neurotrauma 26, 2127-2144. doi:10.1089/neu.2009-0885
11. Berger, R. P., Adelson, P. D., Pierce, M. C., Dulani, T., Cassidy, L. D., and Kochanek, P. M. (2005). Serum neuron-specific enolase, S100B, and myelin basic protein concentrations after inflicted and noninflicted traumatic brain injury in children. J. Neurosurg. 103, 61-68.
12. Binder, L. M. (1997). A review of mild head trauma. Part II: clinical implications. J. Clin. Exp. Neuropsychol. 19, 432-457. doi:10.1080/01688639708403871
13. Bissonnette, L., and Bergeron, M. G. (2006). Next revolution in the molecular theranostics of infectious diseases: microfabricated systems for personalized medicine. Expert Rev. Mol. Diagn. 6, 433-450. doi:10.1586/14737159.6.3.433
14. Blackstock, W. P., and Weir, M. P. (1999). Proteomics: quantitative and physical mapping of cellular proteins. Trends Biotechnol. 17, 121-127. doi:10.1016/S0167-7799(98)01245-1
15. Boutté, A. M., Yao, C., Kobeissy, F., May, L. uX. C., Zhang, Z., Wang, K. K., et al. (2012). Proteomic analysis and brain-specific systems biology in a rodent model of penetrating ballistic-like brain injury. Electrophoresis 33, 3693-3704. doi:10.1002/elps.201200196
16. Brophy, G. M., Mondello, S., Papa, L., Robicsek, S. A., Gabrielli, A., Tepas, J. III, et al. (2011). Biokinetic analysis of ubiquitin C-terminal hydrolase-L1 (UCH-L1) in severe traumatic brain injury patient biofluids. J. Neurotrauma 28, 861-870. doi:10.1089/neu.2010.1564
17. Büki, A., Siman, R., Trojanowski, J. Q., and Povlishock, J. T. (1999). The role of calpain-mediated spectrin proteolysis in traumatically induced axonal injury. J. Neuropathol. Exp. Neurol. 58, 365-375. doi:10.1097/00005072-199904000-00007
18. Carey, M. E. (1996). Analysis of wounds incurred by U.S. Army Seventh Corps personnel treated in Corps hospitals during Operation Desert Storm, February 20 to March 10, 1991. J. Trauma 40, S165-S169. doi:10.1097/00005373-199603001-00036
19. Chen, X., Yu, L., Steill, J. D., Oomens, J., and Polfer, N. C. (2009). Effect of peptide fragment size on the propensity of cyclization in collision-induced dissociation: oligoglycine b(2)-b(8). J. Am. Chem. Soc. 131, 18272-18282. doi:10.1021/ja9030837
20. Cheng, J., Gu, J., Ma, Y., Yang, T., Kuang, Y., Li, B., et al. (2010). Development of a rat model for studying blast-induced traumatic brain injury. J. Neurol. Sci. 294, 23-28. doi:10.1016/j.jns.2010.04.010
21. Choudhary, J., and Grant, S. G. (2004). Proteomics in postgenomic neuroscience: the end of the beginning. Nat. Neurosci. 7, 6. doi:10.1038/nn1240
22. Chuang, H. Y., Hofree, M., and Ideker, T. (2010). A decade of systems biology. Annu. Rev. Cell Dev. Biol. 26, 721-744. doi:10.1146/annurev-cellbio-100109-104122
23. Colinge, J., and Bennett, K. L. (2007). Introduction to computational proteomics. PLoS Comput. Biol. 3:e114. doi:10.1371/journal.pcbi.0030114
24. Crawford, F., Crynen, G., Reed, J., Mouzon, B., Bishop, A., Katz, B., et al. (2012). Identification of plasma biomarkers of TBI outcome using proteomic approaches in an APOE mouse model. J. Neurotrauma 29, 246-260. doi:10.1089/neu.2011.1789
25. Dixon, C. E., Clifton, G. L., Lighthall, J. W., Yaghmai, A. A., and Hayes, R. L. (1991). A controlled cortical impact model of traumatic brain injury in the rat. J. Neurosci. Methods 39, 253-262. doi:10.1016/0165-0270(91)90104-8
26. Donato, R. (1986). S-100 proteins. Cell Calcium 7, 123-145. doi:10.1016/0143-4160(86)90017-5
27. Donato, R., Battaglia, F., and Cocchia, D. (1986a). Effects of S-100 proteins on assembly of brain microtubule proteins: correlation between kinetic and ultrastructural data. J. Neurochem. 47, 350-354. doi:10.1111/j.1471-4159.1986.tb04508.x
28. Donato, R., Prestagiovanni, B., and Zelano, G. (1986b). Identity between cytoplasmic and membrane-bound S-100 proteins purified from bovine and rat brain. J. Neurochem. 46, 1333-1337. doi:10.1111/j.1471-4159.1986.tb01743.x
29. Egea-Guerrero, J. J., Revuelto-Rey, J., Murillo-Cabezas, F., Muñoz-Sánchez, M. A., Vilches-Arenas, A., Sánchez-Linares, P., et al. (2012). Accuracy of the S100beta protein as a marker of brain damage in traumatic brain injury. Brain Inj. 26, 76-82. doi:10.3109/02699052.2011.635360
30. Elias, J. E., and Gygi, S. P. (2010). Target-decoy search strategy for mass spectrometry-based proteomics. Methods Mol. Biol. 604, 55-71. doi:10.1007/978-1-60761-444-9_5
31. Eng, L. F., Vanderhaeghen, J. J., Bignami, A., and Gerstl, B. (1971). An acidic protein isolated from fibrous astrocytes. Brain Res. 28, 351-354. doi:10.1016/0006-8993(71)90668-8
32. Farkas, O., Polgár, B., Szekeres-Barthó, J., Dóczi, T., Povlishock, J. T., and Büki, A. (2005). Spectrin breakdown products in the cerebrospinal fluid in severe head injury - preliminary observations. Acta Neurochir. (Wien) 147, 855-861. doi:10.1007/s00701-005-0559-6
33. Fenn, J. B., Mann, M., Meng, C. K., Wong, S. F., and Whitehouse, C. M. (1989). Electrospray ionization for mass spectrometry of large biomolecules. Science 246, 64-71. doi:10.1126/science.2675315
34. Frank, A., and Pevzner, P. (2005). PepNovo: de novo peptide sequencing via probabilistic network modeling. Anal. Chem. 77, 964-973. doi:10.1021/ac048788h
35. Fraser, D., and Powell, R. E. (1950). The kinetics of trypsin digestion. J. Biol. Chem. 187, 803-820.
36. Galea, E., Dupouey, P., and Feinstein, D. L. (1995). Glial fibrillary acidic protein mRNA isotypes: expression in vitro and in vivo. J. Neurosci. Res. 41, 452-461. doi:10.1002/jnr.490410404
37. Gerberding, J. (2003). Report to Congress on Mild Traumatic Brain Injury in the Ubited States: Steps to Prevent a Serious Public Health Problem. Atlanta: National Center for Injury Prevention and Control.
38. Guingab-Cagmat, J. D., Newsom, K., Vakulenko, A., Cagmat, E. B., Kobeissy, F. H., Zoltewicz, S., et al. (2012). An in vitro mass spectrometry-based proteomic analysis and absolute quantification of neuronal-glial injury biomarkers in cell culture system. Electrophoresis 33, 3786-3797. doi:10.1002/elps.201200326
39. Hagen, J. B. (2000). The origins of bioinformatics. Nat. Rev. Genet. 1, 231-236. doi:10.1038/35042090
40. Hamm, R. J., Lyeth, B. G., Jenkins, L. W., O'Dell, D. M., and Pike, B. R. (1993). Selective cognitive impairment following traumatic brain injury in rats. Behav. Brain Res. 59, 169-173. doi:10.1016/0166-4328(93)90164-L
41. Hanrieder, J., Wetterhall, M., Enblad, P., Hillered, L., and Bergquist, J. (2009). Temporally resolved differential proteomic analysis of human ventricular CSF for monitoring traumatic brain injury biomarker candidates. J. Neurosci. Methods 177, 469-478. doi:10.1016/j.jneumeth.2008.10.038
42. Haqqani, A. S., Hutchison, J. S., Ward, R., and Stanimirovic, D. B. (2007a). Biomarkers and diagnosis; protein biomarkers in serum of pediatric patients with severe traumatic brain injury identified by ICAT-LC-MS/MS. J. Neurotrauma 24, 54-74. doi:10.1089/neu.2006.0079
43. Haqqani, A. S., Kelly, J., Baumann, E., Haseloff, R. F., Blasig, I. E., and Stanimirovic, D. B. (2007b). Protein markers of ischemic insult in brain endothelial cells identified using 2D gel electrophoresis and ICAT-based quantitative proteomics. J. Proteome Res. 6, 226-239. doi:10.1021/pr0603811
44. Heizmann, C. W., Fritz, G., and Schafer, B. W. (2002). S100 proteins: structure, functions and pathology. Front. Biosci. 7:d1356-d1368. doi:10.2741/heizmann
45. Hergenroeder, G., Redell, J. B., Moore, A. N., Dubinsky, W. P., Funk, R. T., Crommett, J., et al. (2008). Identification of serum biomarkers in brain-injured adults: potential for predicting elevated intracranial pressure. J. Neurotrauma 25, 79-93. doi:10.1089/neu.2007.0386
46. Herrmann, M., Jost, S., Kutz, S., Ebert, A. D., Kratz, T., Wunderlich, M. T., et al. (2000). Temporal profile of release of neurobiochemical markers of brain damage after traumatic brain injury is associated with intracranial pathology as demonstrated in cranial computerized tomography. J. Neurotrauma 17, 113-122. doi:10.1089/neu.2000.17.113
47. Hinman, L. M., Huang, S. M., Hackett, J., Koch, W. H., Love, P. Y., Pennello, G., et al. (2006). The drug diagnostic co-development concept paper: commentary from the 3rd FDA-DIA-PWG-PhRMA-BIO Pharmacogenomics Workshop. Pharmacogenomics J. 6, 375-380. doi:10.1038/sj.tpj.6500392
48. Hooper, J. W. (2006). The genetic map to theranostics. MLO Med. Lab. Obs. 38, 22-23.
49. Ideker, T., Galitski, T., and Hood, L. (2001). A new approach to decoding life: systems biology. Annu. Rev. Genomics Hum. Genet. 2, 343-372. doi:10.1146/annurev.genom.2.1.343
50. Inglese, M., Makani, S., Johnson, G., Cohen, B. A., Silver, J. A., Gonen, O., et al. (2005). Diffuse axonal injury in mild traumatic brain injury: a diffusion tensor imaging study. J. Neurosurg. 103, 298-303. doi:10.3171/jns.2005.103.2.0298
51. Jackson, R. G., Samra, G. S., Radcliffe, J., Clark, G. H., and Price, C. P. (2000). The early fall in levels of S-100 beta in traumatic brain injury. Clin. Chem. Lab. Med. 38, 1165-1167. doi:10.1515/CCLM.2000.179
52. Jager, T. E., Weiss, H. B., Coben, J. H., and Pepe, P. E. (2000). Traumatic brain injuries evaluated in U.S. emergency departments, 1992-1994. Acad. Emerg. Med. 7, 134-140. doi:10.1111/j.1553-2712.2000.tb00515.x
53. Jenkins, L. W., Peters, G. W., Dixon, C. E., Zhang, X., Clark, R. S., Skinner, J. C., et al. (2012). Conventional and functional proteomics using large format two-dimensional gel electrophoresis 24 hours after controlled cortical impact in postnatal day 17 rats. J. Neurotrauma 19, 715-740. doi:10.1089/08977150260139101
54. Johnson, E. A., Svetlov, S. I., Pike, B. R., Tolentino, P. J., Shaw, G., Wang, K. K., et al. (2004). Cell-specific upregulation of survivin after experimental traumatic brain injury in rats. J. Neurotrauma 21, 1183-1195. doi:10.1089/neu.2004.21.1183
55. Karas, M., and Hillenkamp, F. (1988). Laser desorption ionization of proteins with molecular masses exceeding 10,000 daltons. Anal. Chem. 60, 2299-2301. doi:10.1021/ac00171a028
56. Kibby, M. Y., and Long, C. J. (1996). Minor head injury: attempts at clarifying the confusion. Brain Inj. 10, 159-186. doi:10.1080/026990596124494
57. Kitano, H. (2002a). Systems biology: a brief overview. Science 295, 1662-1664. doi:10.1126/science.1069492
58. Kitano, H. (2002b). Computational systems biology. Nature 420, 206-210. doi:10.1038/nature01254
59. Kleindienst, A., Hesse, F., Bullock, M. R., and Buchfelder, M. (2007). "The neurotrophic protein S100B: value as a marker of brain damage and possible therapeutic implications," in Progress in Brain Research, eds T. W. John, and I. R. M. Andrew (Amsterdam: Elsevier), 161, 317-325.
60. Klose, J., and Feller, M. (1981). Genetic variability of proteins from plasma membranes and cytosols of mouse organs. Biochem. Genet. 19, 859-870. doi:10.1007/BF00504251
61. Kobeissy, F. H., Ottens, A. K., Zhang, Z., Liu, M. C., Denslow, N. D., Dave, J. R., et al. (2006). Novel differential neuroproteomics analysis of traumatic brain injury in rats. Mol. Cell Proteomics 5, 1887-1898. doi:10.1074/mcp.M600157-MCP200
62. Kobeissy, F. H., Sadasivan, S., Oli, M. W., Robinson, G., Larner, S. F., Zhang, Z., et al. (2008). Neuroproteomics and systems biology-based discovery of protein biomarkers for traumatic brain injury and clinical validation. Proteomics. Clin. Appl. 2, 1467-1483. doi:10.1002/prca.200800011
63. Kumar, C., and Mann, M. (2009). Bioinformatics analysis of mass spectrometry-based proteomics data sets. FEBS Lett. 583, 1703-1712. doi:10.1016/j.febslet.2009.03.035
64. Kushner, D. (1998). Mild traumatic brain injury: toward understanding manifestations and treatment. Arch. Intern. Med. 158, 1617-1624. doi:10.1001/archinte.158.15.1617
65. Kwon, S. K., Kovesdi, E., Gyorgy, A. B., Wingo, D., Kamnaksh, A., Walker, J., et al. (2011). Stress and traumatic brain injury: a behavioral, proteomics, and histological study. Front. Neurol. 2:12. doi:10.3389/fneur.2011.00012
66. Lesko, L. J., and Atkinson, A. J. Jr. (2001). Use of biomarkers and surrogate endpoints in drug development and regulatory decision making: criteria, validation, strategies. Annu. Rev. Pharmacol. Toxicol. 41, 347-366. doi:10.1146/annurev.pharmtox.41.1.347
67. Lew, H. L. (2005). Rehabilitation needs of an increasing population of patients: traumatic brain injury, polytrauma, and blast-related injuries. J. Rehabil. Res. Dev. 42, xiii-xvi. doi:10.1682/JRRD.2005.07.0124
68. Lighthall, J. W. (1988). Controlled cortical impact: a new experimental brain injury model. J. Neurotrauma 5, 1-15. doi:10.1089/neu.1988.5.1
69. Liu, Z., and Schey, K. L. (2008). Fragmentation of multiply-charged intact protein ions using MALDI TOF-TOF mass spectrometry. J. Am. Soc. Mass Spectrom. 19, 231-238. doi:10.1016/j.jasms.2007.06.006
70. Lyeth, B. G., Jenkins, L. W., Hamm, R. J., Dixon, C. E., Phillips, L. L., Clifton, G. L., et al. (1990). Prolonged memory impairment in the absence of hippocampal cell death following traumatic brain injury in the rat. Brain Res. 526, 249-258. doi:10.1016/0006-8993(90)91229-A
71. Ma, B., Zhang, K., Hendrie, C., Liang, C., Li, M., Doherty-Kirby, A., et al. (2003). PEAKS: powerful software for peptide de novo sequencing by tandem mass spectrometry. Rapid Commun. Mass Spectrom. 17, 2337-2342. doi:10.1002/rcm.1196
72. Maggio, E. T., and Ramnarayan, K. (2001). Recent developments in computational proteomics. Drug Discov. Today 6, 996-1004. doi:10.1016/S1359-6446(01)02003-7
73. Management of Concussion/mTBI Working Group. (2009). VA/DoD clinical practice guideline for management of concussion/mild traumatic brain injury. J. Rehabil. Res. Dev. 46, C1-68. doi:10.1682/JRRD.2008.03.0038
74. Mann, M., and Wilm, M. (1994). Error-tolerant identification of peptides in sequence databases by peptide sequence tags. Anal. Chem. 66, 4390-4399. doi:10.1021/ac00096a002
75. Margulies, S. (2000). The postconcussion syndrome after mild head trauma part II: is migraine underdiagnosed? J. Clin. Neurosci. 7, 495-499. doi:10.1054/jocn.1999.0773
76. Marion, D. W., Curley, K. C., Schwab, K., and Hicks, R. R. mTBI Diagnostics Workgroup. (2011). Proceedings of the military mTBI Diagnostics Workshop, St. Pete Beach, August 2010. J. Neurotrauma 28, 517-526. doi:10.1089/neu.2010.1638
77. Marshall, A. G., Hendrickson, C. L., and Jackson, G. S. (1998). Fourier transform ion cyclotron resonance mass spectrometry: a primer. Mass Spectrom. Rev. 17, 1-35. doi:10.1002/(SICI)1098-2787(1998)17:1<1::AID-MAS1>3.0.CO;2-K
78. Mathers, C. D., and Loncar, D. (2006). Projections of global mortality and burden of disease from 2002 to 2030. PLoS Med. 3:e442. doi:10.1371/journal.pmed.0030442
79. Matthiesen, R. (2007). Methods, algorithms and tools in computational proteomics: a practical point of view. Proteomics 7, 2815-2832. doi:10.1002/pmic.200700116
80. McDonald, W. H., and Yates, J. R. III. (2002). Shotgun proteomics and biomarker discovery. Dis. Markers 18, 99-105.
81. McDonald, W. H., and Yates, J. R. III. (2003). Shotgun proteomics: integrating technologies to answer biological questions. Curr. Opin. Mol. Ther. 5, 302-309. doi:10.1016/S0076-6879(83)96021-4
82. Merril, C. R., Goldman, D., and Van Keuren, M. L. (1983). Silver staining methods for polyacrylamide gel electrophoresis. Meth. Enzymol. 96, 230-239. doi:10.1016/S0076-6879(83)96021-4
83. Mondello, S., Jeromin, A., Buki, A., Bullock, R., Czeiter, E., Kovacs, N., et al. (2012a). Glial neuronal ratio: a novel index for differentiating injury type in patients with severe traumatic brain injury. J. Neurotrauma 29, 1096-1104. doi:10.1089/neu.2011.2092
84. Mondello, S., Linnet, A., Buki, A., Robicsek, S., Gabrielli, A., Tepas, J., et al. (2012b). Clinical utility of serum levels of ubiquitin C-terminal hydrolase as a biomarker for severe traumatic brain injury. Neurosurgery 70, 666-675. doi:10.1227/NEU.0b013e318236a809
85. Mondello, S., Robicsek, S. A., Gabrielli, A., Brophy, G. M., Papa, L., Tepas, J., et al. (2010). AlphaII-spectrin breakdown products (SBDPs): diagnosis and outcome in severe traumatic brain injury patients. J. Neurotrauma 27, 1203-1213. doi:10.1089/neu.2010.1278
86. Niogi, S. N., and Mukherjee, P. (2010). Diffusion tensor imaging of mild traumatic brain injury. J. Head Trauma Rehabil. 25, 241-255. doi:10.1097/HTR.0b013e3181e52c2a
87. Nylén, K., Ost, M., Csajbok, L. Z., Nilsson, I., Blennow, K., Nellgård, B., et al. (2006). Increased serum-GFAP in patients with severe traumatic brain injury is related to outcome. J. Neurol. Sci. 240, 85-91. doi:10.1016/j.jns.2005.09.007
88. O'Farrell, P. H. (1975). High resolution two-dimensional electrophoresis of proteins. J. Biol. Chem. 250, 4007-4021.
89. Okie, S. (2005). Traumatic brain injury in the war zone. N. Engl. J. Med. 352, 2043-2047. doi:10.1056/NEJMp058102
90. Opii, W. O., Nukala, V. N., Sultana, R., Pandya, J. D., Day, K. M., Merchant, M. L., et al. (2007). Proteomic identification of oxidized mitochondrial proteins following experimental traumatic brain injury. J. Neurotrauma 24, 772-789. doi:10.1089/neu.2006.0229
91. Ottens, A. K., Bustamante, L., Golden, E. C., Yao, C., Hayes, R. L., Wang, K. K., et al. (2010). Neuroproteomics: a biochemical means to discriminate the extent and modality of brain injury. J. Neurotrauma 27, 1837-1852. doi:10.1089/neu.2010.1374
92. Ottens, A. K., Kobeissy, F. H., Fuller, B. F., Liu, M. C., Oli, M. W., Hayes, R. L., et al. (2007). Novel neuroproteomic approaches to studying traumatic brain injury. Prog. Brain Res. 161, 401-418. doi:10.1016/S0079-6123(06)61029-7
93. Ottens, A. K., Kobeissy, F. H., Golden, E. C., Zhang, Z., Haskins, W. E., Chen, S. S., et al. (2006). Neuroproteomics in neurotrauma. Mass Spectrom. Rev. 25, 380-408. doi:10.1002/mas.20073
94. Paizs, B., and Mann, M. (2012). 23rd Sanibel Conference on mass spectrometry: from fragmentation mechanisms to sequencing: Tandem Mass Spectrometry based peptide and protein identification. J. Am. Soc. Mass Spectrom. 23, 575-576. doi:10.1007/s13361-012-0358-2
95. Peitsch, M. C., Wilkins, M. R., Tonella, L., Sanchez, J. C., Appel, R. D., and Hochstrasser, D. F. (1997). Large-scale protein modelling and integration with the SWISS-PROT and SWISS-2DPAGE databases: the example of Escherichia coli. Electrophoresis 18, 498-501. doi:10.1002/elps.1150180326
96. Pelinka, L. E., Kroepfl, A., Leixnering, M., Buchinger, W., Raabe, A., and Redl, H. (2004a). GFAP versus S100B in serum after traumatic brain injury: relationship to brain damage and outcome. J. Neurotrauma 21, 1553-1561. doi:10.1089/neu.2004.21.1553
97. Pelinka, L. E., Kroepfl, A., Schmidhammer, R., Krenn, M., Buchinger, W., Redl, H., et al. (2004b). Glial fibrillary acidic protein in serum after traumatic brain injury and multiple trauma. J. Trauma 57, 1006-1012. doi:10.1097/01.TA.0000108998.48026.C3
98. Pelinka, L. E., Toegel, E., Mauritz, W., and Redl, H. (2003a). Serum S 100 B: a marker of brain damage in traumatic brain injury with and without multiple trauma. Shock 19, 195-200. doi:10.1097/00024382-200303000-00001
99. Pelinka, L. E., Szalay, L., Jafarmadar, M., Schmidhammer, R., Redl, H., and Bahrami, S. (2003b). Circulating S100B is increased after bilateral femur fracture without brain injury in the rat. Br. J. Anaesth. 91, 595-597. doi:10.1093/bja/aeg225
100. Pelinka, L. E., Bahrami, S., Szalay, L., Umar, F., and Redl, H. (2003c). Hemorrhagic shock induces an S 100 B increase associated with shock severity. Shock 19, 422-426. doi:10.1097/01.shk.0000055345.58165.52
101. Perkins, D. N., Pappin, D. J., Creasy, D. M., and Cottrell, J. S. (1999). Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567. doi:10.1002/(SICI)1522-2683(19991201)20:18<3551::AID-ELPS3551>3.0.CO;2-2
102. Pineda, J. A., Lewis, S. B., Valadka, A. B., Papa, L., Hannay, H. J., Heaton, S. C., et al. (2007). Clinical significance of alphaII-spectrin breakdown products in cerebrospinal fluid after severe traumatic brain injury. J. Neurotrauma 24, 354-366. doi:10.1089/neu.2006.003789
103. Polfer, N. C., Oomens, J., Suhai, S., and Paizs, B. (2005). Spectroscopic and theoretical evidence for oxazolone ring formation in collision-induced dissociation of peptides. J. Am. Chem. Soc. 127, 17154-17155. doi:10.1021/ja056553x
104. Riederer, B. M., Zagon, I. S., and Goodman, S. R. (1986). Brain spectrin(240/235) and brain spectrin(240/235E): two distinct spectrin subtypes with different locations within mammalian neural cells. J. Cell Biol. 102, 2088-2097. doi:10.1083/jcb.102.6.2088
105. Rifai, N., Gillette, M. A., and Carr, S. A. (2006). Protein biomarker discovery and validation: the long and uncertain path to clinical utility. Nat. Biotechnol. 24, 971-983. doi:10.1038/nbt1235
106. Ringger, N. C., O'Steen, B. E., Brabham, J. G., Silver, X., Pineda, J., Wang, K. K., et al. (2004). A novel marker for traumatic brain injury: CSF alphaII-spectrin breakdown product levels. J. Neurotrauma 21, 1443-1456. doi:10.1089/neu.2004.21.1443
107. Risdall, J. E., and Menon, D. K. (2011). Traumatic brain injury. Philos. Trans. R. Soc. Lond. B Biol. Sci. 366, 241-250. doi:10.1098/rstb.2010.0230
108. Risling, M., Plantman, S., Angeria, M., Rostami, E., Bellander, B. M., Kirkegaard, M., et al. (2011). Mechanisms of blast induced brain injuries, experimental studies in rats. Neuroimage 54, S89-97. doi:10.1016/j.neuroimage.2010.05.031
109. Roepstorff, P., and Fohlman, J. (1984). Proposal for a common nomenclature for sequence ions in mass spectra of peptides. Biomed. Mass Spectrom. 11, 601. doi:10.1002/bms.1200111109
110. Ross, S. A., Cunningham, R. T., Johnston, C. F., and Rowlands, B. J. (1996). Neuron-specific enolase as an aid to outcome prediction in head injury. Br. J. Neurosurg. 10, 471-476. doi:10.1080/02688699647104
111. Rothoerl, R. D., and Woertgen, C. (2001). High serum S100B levels for trauma patients without head injuries. Neurosurgery 49, 1490-1491. doi:10.1097/00006123-200112000-00053
112. Ruff, R. M., and Jurica, P. (1999). In search of a unified definition for mild traumatic brain injury. Brain Inj. 13, 943-952. doi:10.1080/026990599120963
113. Selakovic, V., Raicevic, R., and Radenovic, L. (2005). The increase of neuron-specific enolase in cerebrospinal fluid and plasma as a marker of neuronal damage in patients with acute brain infarction. J. Clin. Neurosci. 12, 542-547. doi:10.1016/j.jocn.2004.07.019
114. Setsuie, R., and Wada, K. (2007). The functions of UCH-L1 and its relation to neurodegenerative diseases. Neurochem. Int. 51, 105-111. doi:10.1016/j.neuint.2007.05.007
115. Shadforth, I., Crowther, D., and Bessant, C. (2005). Protein and peptide identification algorithms using MS for use in high-throughput, automated pipelines. Proteomics 5, 4082-4095. doi:10.1002/pmic.200402091
116. Shenton, M. E., Hamoda, H. M., Schneiderman, J. S., Bouix, S., Pasternak, O., Rathi, Y., et al. (2012). A review of magnetic resonance imaging and diffusion tensor imaging findings in mild traumatic brain injury. Brain Imaging Behav. 6, 137-192. doi:10.1007/s11682-012-9156-5
117. Shevchenko, A., Sunyaev, S., Loboda, A., Shevchenko, A., Bork, P., Ens, W., et al. (2001). Charting the proteomes of organisms with unsequenced genomes by MALDI-quadrupole time-of-flight mass spectrometry and BLAST homology searching. Anal. Chem. 73, 1917-1926. doi:10.1021/ac0013709
118. Shi, S. D., Hendrickson, C. L., and Marshall, A. G. (1998). Counting individual sulfur atoms in a protein by ultrahigh-resolution Fourier transform ion cyclotron resonance mass spectrometry: experimental resolution of isotopic fine structure in proteins. Proc. Natl. Acad. Sci. U.S.A. 95, 11532-11537. doi:10.1073/pnas.95.20.11532
119. Shoemaker, L. D., Achrol, A. S., Sethu, P., Steinberg, G. K., and Chang, S. D. (2012). Clinical neuroproteomics and biomarkers: from basic research to clinical decision making. Neurosurgery 70, 518-525. doi:10.1227/NEU.0b013e3182333a26
120. Siman, R., McIntosh, T. K., Soltesz, K. M., Chen, Z., Neumar, R. W., and Roberts, V. L. (2004). Proteins released from degenerating neurons are surrogate markers for acute brain damage. Neurobiol. Dis. 16, 311-320. doi:10.1016/j.nbd.2004.03.016
121. Smith, D. H., Uryu, K., Saatman, K. E., Trojanowski, J. Q., and McIntosh, T. K. (2003). Protein accumulation in traumatic brain injury. Neuromolecular Med. 4, 59-72. doi:10.1385/NMM:4:1-2:59
122. Stults, J. T., and Arnott, D. (2005). Proteomics. Meth. Enzymol. 402, 245-289. doi:10.1016/S0076-6879(05)02008-2
123. Svetlov, S. I., Larner, S. F., Kirk, D. R., Atkinson, J., Hayes, R. L., and Wang, K. K. (2009). Biomarkers of blast-induced neurotrauma: profiling molecular and cellular mechanisms of blast brain injury. J. Neurotrauma 26, 913-921. doi:10.1089/neu.2008.0609
124. Svetlov, S. I., Prima, V., Kirk, D. R., Gutierrez, H., Curley, K. C., Hayes, R. L., et al. (2010). Morphologic and biochemical characterization of brain injury in a model of controlled blast overpressure exposure. J. Trauma 69, 795-804. doi:10.1097/TA.0b013e3181bbd885
125. Szczygielski, J., Mautes, A., Steudel, W. I., Falkai, P., Bayer, T. A., and Wirths, O. (2005). Traumatic brain injury: cause or risk of Alzheimer's disease? A review of experimental studies. J. Neural Transm. 112, 1547-1564. doi:10.1007/s00702-005-0326-0
126. Townend, W., Dibble, C., Abid, K., Vail, A., Sherwood, R., and Lecky, F. (2006). Rapid elimination of protein S-100B from serum after minor head trauma. J. Neurotrauma 23, 149-155. doi:10.1089/neu.2006.23.149
127. Vos, P. E., Jacobs, B., Andriessen, T. M., Lamers, K. J., Borm, G. F., Beems, T., et al. (2010). GFAP and S100B are biomarkers of traumatic brain injury: an observational cohort study. Neurology 75, 1786-1793. doi:10.1212/WNL.0b013e3181fd62d2
128. Vos, P. E., Lamers, K. J., Hendriks, J. C., van, H., aaren, M., Beems, T., Zimmerman, C., et al. (2004). Glial and neuronal proteins in serum predict outcome after severe traumatic brain injury. Neurology 62, 1303-1310. doi:10.1212/01.WNL.0000120550.00643.DC
129. Wang, K. K. W., Ottens, A. K., Liu, M. C., Lewis, S. B., Meegan, C., Oli, M. W., et al. (2005). Proteomic identification of biomarkers of traumatic brain injury. Expert Rev. Proteomics, 2, 603-614. doi:10.1586/14789450.2.4.603
130. Wang, H., Qian, W. J., Chin, M. H., Petyuk, V. A., Barry, R. C., Liu, T., et al. (2006). Characterization of the mouse brain proteome using global proteomic analysis complemented with cysteinyl-peptide enrichment. J. Proteome Res. 5, 361-369. doi:10.1021/pr0503681
131. Warden, D. (2006). Military TBI during the Iraq and Afghanistan wars. J. Head Trauma Rehabil. 21, 398-402. doi:10.1097/00001199-200609000-00004
132. Wasinger, V. C., Cordwell, S. J., Cerpa-Poljak, A., Yan, J. X., Gooley, A. A., Wilkins, M. R., et al. (1995). Progress with gene-product mapping of the Mollicutes: Mycoplasma genitalium. Electrophoresis 16, 1090-1094. doi:10.1002/elps.11501601185
133. Webb-Robertson, B. J., and Cannon, W. R. (2007). Current trends in computational inference from mass spectrometry-based proteomics. Brief. Bioinformatics 8, 304-317. doi:10.1093/bib/bbm023
134. Williams, A. J., Hartings, J. A., Lu, X. C., Rolli, M. L., Dave, J. R., and Tortella, F. C. (2005). Characterization of a new rat model of penetrating ballistic brain injury. J. Neurotrauma 22, 313-331. doi:10.1089/neu.2005.22.313
135. Wolters, D. A., Washburn, M. P., and Yates, J. R. III. (2001). An automated multidimensional protein identification technology for shotgun proteomics. Anal. Chem. 73, 5683-5690. doi:10.1021/ac010617e
136. Wu, C. C., and MacCoss, M. J. (2002). Shotgun proteomics: tools for the analysis of complex biological systems. Curr. Opin. Mol. Ther. 4, 242-250.
137. Xenarios, I., Fernandez, E., Salwinski, L., Duan, X. J., Thompson, M. J., Marcotte, E. M., et al. (2001). DIP: the database of interacting proteins: 2001 update. Nucleic Acids Res. 29, 239-241. doi:10.1093/nar/29.1.239
138. Xiong, Y., Mahmood, A., and Chopp, M. (2013). Animal models of traumatic brain injury. Nat. Rev. Neurosci. 14, 128-142. doi:10.1038/nrn3407
139. Xu, C., and Ma, B. (2006). Software for computational peptide identification from MS-MS data. Drug Discov. Today 11, 595-600. doi:10.1016/j.drudis.2006.05.011
140. Yates, J. R. 3rd, Eng, J. K., McCormack, A. L., and Schieltz, D. (1995). Method to correlate tandem mass spectra of modified peptides to amino acid sequences in the protein database. Anal. Chem. 67, 1426-1436. doi:10.1021/ac00104a020
141. Zhang, Z., Larner, S. F., Kobeissy, F., Hayes, R. L., and Wang, K. K. (2010). Systems biology and theranostic approach to drug discovery and development to treat traumatic brain injury. Methods Mol. Biol. 662, 317-329. doi:10.1007/978-1-60761-800-3_16
142. Zimmer, D. B., Cornwall, E. H., Landar, A., and Song, W. (1995). The S100 protein family: history, function, and expression. Brain Res. Bull. 37, 417-429. doi:10.1016/0361-9230(95)00040-2
143. Zurek, J., and Fedora, M. (2012). The usefulness of S100B, NSE, GFAP, NF-H, secretagogin and Hsp70 as a predictive biomarker of outcome in children with traumatic brain injury. Acta Neurochir. (Wien) 154, 93-103. doi:10.1007/s00701-011-1175-2