Detection of structural and metabolic changes in traumatically injured hippocampus by quantitative differential proteomics

Journal of Neurotrauma

Volumn 30, Issue 9, 2013, Pages 775-788

  Wu, Ping ^a   Zhao, Yingxin ^a,b   Haidacher, Sigmund J ^a,b   Wang, Enyin ^a   Parsley, Margaret O ^a   Gao, Junling ^a   Sadygov, Rovshan G ^a,b   Starkey, Jonathan M ^a   Luxon, Bruce A ^a,b   Spratt, Heidi ^a,b   Dewitt, Douglas S ^a   Prough, Donald S ^a   Denner, Larry ^a,b  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

Animal models; Bioinformatics; Mass spectrometry; Proteomics; Traumatic brain injury

Indexed keywords

CALCINEURIN B1; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALMODULIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLOSPORIN; OXYGEN 18; PHOSPHATASE; RHO KINASE; TACROLIMUS; UNCLASSIFIED DRUG; VIMENTIN;

ACTIN FILAMENT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AXONAL INJURY; BIOINFORMATICS; BRAIN METABOLISM; CALCIUM SIGNALING; CELL FUNCTION; CELL STRUCTURE; CITRIC ACID CYCLE; COGNITIVE DEFECT; CONTROLLED STUDY; DOWN REGULATION; DRUG HALF LIFE; DYNAMICS; ENERGY METABOLISM; GLUCONEOGENESIS; GLYCOLYSIS; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; HOMEOSTASIS; ISOTOPE LABELING; LIQUID CHROMATOGRAPHY; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE PHOSPHORYLATION; PROTEIN EXPRESSION; PROTEOMICS; RAT; RESPIRATORY CHAIN; TANDEM MASS SPECTROMETRY; TRAUMATIC BRAIN INJURY; UNINDEXED SEQUENCE; UPREGULATION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; BRAIN INJURIES; CALCINEURIN; CHROMATOGRAPHY, LIQUID; DISEASE MODELS, ANIMAL; HIPPOCAMPUS; MALE; PROTEOMICS; RATS; RATS, SPRAGUE-DAWLEY; TANDEM MASS SPECTROMETRY;

EID: 84877853679     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2012.2391     Document Type: Article

References (83)

1. Asai, A., Qiu, J., Narita, Y., Chi, S., Saito, N., Shinoura, N., Hamada, H., Kuchino, Y., and Kirino, T. (1999). High level calcineurin activity predisposes neuronal cells to apoptosis. J. Biol. Chem. 274, 34450-34458. (Pubitemid 129511792)
2. Bales, J.W.,Ma, X., Yan, H.Q., Jenkins, L.W., and Dixon, C.E. (2010a). Expression of protein phosphatase 2B (calcineurin) subunit A isoforms in rat hippocampus after traumatic brain injury. J. Neurotrauma 27, 109-120.
3. Bales, J.W., Ma, X., Yan, H.Q., Jenkins, L.W., and Dixon, C.E. (2010b). Regional calcineurin subunit B isoform expression in rat hippocampus following a traumatic brain injury. Brain Res. 1358, 211-220.
4. Bedell, E.A., DeWitt, D.S., Uchida, T., and Prough, D.S. (2004). Cerebral pressure autoregulation is intact and is not influenced by hypothermia after traumatic brain injury in rats. J. Neurotrauma 21, 1212-1222. (Pubitemid 39280848)
5. Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. Royal Statistical Soc. Series B (Methodological) 57, 289-300.
6. Blanchet, S., Paradis-Giroux, A.A., Pepin, M., and McKerral, M. (2009). Impact of divided attention during verbal learning in young adults following mild traumatic brain injury. Brain Inj. 23, 111-122.
7. Burgess, J.A., Lescuyer, P., Hainard, A., Burkhard, P.R., Turck, N., Michel, P., Rossier, J.S., Reymond, F., Hochstrasser, D.F., and Sanchez, J.C. (2006). Identification of brain cell death associated proteins in human post-mortem cerebrospinal fluid. J. Proteome Res. 5, 1674-1681. (Pubitemid 44036141)
8. Chaichana, K.L., Pradilla, G., Huang, J., and Tamargo, R.J. (2010). Role of inflammation (leukocyte-endothelial cell interactions) in vasospasm after subarachnoid hemorrhage. World Neurosurg. 73, 22-41.
9. Chew, E., and Zafonte, R.D. (2009). Pharmacological management of neurobehavioral disorders following traumatic brain injury - a stateof-the-art review. J. Rehabil. Res. Dev. 46, 851-879.
10. Consales, C., Volpicelli, F., Greco, D., Leone, L., Colucci-D'Amato, L., Perrone-Capano, C., and di Porzio, U. (2007). GDNF signaling in embryonic midbrain neurons in vitro. Brain Res. 1159, 28-39. (Pubitemid 47058026)
11. Conti, A., Sanchez-Ruiz, Y., Bachi, A., Beretta, L., Grandi, E., Beltramo, M., and Alessio, M. (2004). Proteome study of human cerebrospinal fluid following traumatic brain injury indicates fibrin(ogen) degradation products as trauma-associated markers. J. Neurotrauma 21, 854-863. (Pubitemid 38998913)
12. Corso, P., Finkelstein, E., Miller, T., Fiebelkorn, I., and Zaloshnja, E. (2006). Incidence and lifetime costs of injuries in the United States. Inj. Prev. 12, 212-218. (Pubitemid 44265190)
13. Dayon, L., Hainard, A., Licker, V., Turck, N., Kuhn, K., Hochstrasser, D.F., Burkhard, P.R., and Sanchez, J.C. (2008). Relative quantification of proteins in human cerebrospinal fluids by MS/MS using 6-plex isobaric tags. Anal. Chem. 80, 2921-2931. (Pubitemid 351556457)
14. De Beaumont, L., Theoret, H., Mongeon, D., Messier, J., Leclerc, S., Tremblay, S., Ellemberg, D., and Lassonde, M. (2009). Brain function decline in healthy retired athletes who sustained their last sports concussion in early adulthood. Brain 132, 695-708.
15. De Monte, V.E., Geffen, G.M., and Massavelli, B.M. (2006). The effects of post-traumatic amnesia on information processing following mild traumatic brain injury. Brain Inj. 20, 1345-1354.
16. DeWitt, D.S., Smith, T.G., Deyo, D.J., Miller, K.R., Uchida, T., and Prough, D.S. (1997). L-arginine and superoxide dismutase prevent or reverse cerebral hypoperfusion after fluid-percussion traumatic brain injury. J. Neurotrauma 14, 223-233. (Pubitemid 27205070)
17. Fukura, H., Komiya, Y., and Igarashi, M. (1996). Signaling pathway downstream of GABAA receptor in the growth cone. J. Neurochem. 67, 1426-1434. (Pubitemid 26314197)
18. Gao, J., Prough, D.S., McAdoo, D.J., Grady, J.J., Parsley, M.O., Ma, L., Tarensenko, Y.I., and Wu, P. (2006). Transplantation of primed human fetal neural stem cells improves cognitive function in rats after traumatic brain injury. Exp. Neurol. 201, 281-292. (Pubitemid 44344239)
19. Gao, W.M., Chadha, M.S., Berger, R.P., Omenn, G.S., Allen, D.L., Pisano, M., Adelson, P.D., Clark, R.S., Jenkins, L.W., and Kochanek, P.M. (2007). A gel-based proteomic comparison of human cerebrospinal fluid between inflicted and non-inflicted pediatric traumatic brain injury. J. Neurotrauma 24, 43-53. (Pubitemid 46214411)
20. Goshe, M.B., and Smith, R.D. (2003). Stable isotope-coded proteomic mass spectrometry. Curr. Opin. Biotechnol. 14, 101-109. (Pubitemid 36151850)
21. Gygi, S.P., Rist, B., Gerber, S.A., Turecek, F., Gelb, M.H., and Aebersold, R. (1999). Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat. Biotechnol. 17, 994-999. (Pubitemid 29474856)
22. Hall, E.D., Vaishnav, R.A., and Mustafa, A.G. (2010). Antioxidant therapies for traumatic brain injury. Neurotherapeutics 7, 51-61.
23. 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.
24. Haqqani, A.S., Hutchison, J.S., Ward, R., and Stanimirovic, D.B. (2007). 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. (Pubitemid 46214412)
25. Hardingham, G.E. (2009). Coupling of the NMDA receptor to neuroprotective and neurodestructive events. Biochem. Soc. Trans. 37, 1147-1160.
26. Haskins, W.E., Kobeissy, F.H., Wolper, R.A., Ottens, A.K., Kitlen, J.W., McClung, S.H., O'Steen, B.E., Chow, M.M., Pineda, J.A., Denslow, N.D., Hayes, R.L., and Wang, K.K. (2005). Rapid discovery of putative protein biomarkers of traumatic brain injury by SDSPAGE-capillary liquid chromatography-tandem mass spectrometry. J. Neurotrauma 22, 629-644. (Pubitemid 40840379)
27. Heller, M., Mattou, H., Menzel, C., and Yao, X. (2003). Trypsin catalyzed 16O-to-18O exchange for comparative proteomics: Tandem mass spectrometry comparison using MALDI-TOF, ESI-QTOF, and ESI-ion trap mass spectrometers. J. Am. Soc. Mass Spectrom. 14, 704-718. (Pubitemid 36870953)
28. Hoffrogge, R., Beyer, S., Hubner, R., Mikkat, S., Mix, E., Scharf, C., Schmitz, U., Pauleweit, S., Berth, M., Zubrzycki, I.Z., Christoph, H., Pahnke, J., Wolkenhauer, O., Uhrmacher, A., Volker, U., and Rolfs, A. (2007). 2-DE profiling of GDNF overexpression-related proteome changes in differentiating ST14A rat progenitor cells. Proteomics 7, 33-46. (Pubitemid 46173714)
29. Hong, Z., Liu, J., Xia, L., Pan, J., Xiao, Q., Lu, G., Liang, L., and Chen, S.D. (2009). Identification of glial-cell-line-derived neurotrophic factor-regulated proteins of striatum in mouse model of Parkinson disease. Proteomics Clin. Appl. 3, 1072-1083.
30. Hovda, D.A., Becker, D.P., and Katayama, Y. (1992). Secondary injury and acidosis. J. Neurotrauma 9 Suppl. 1, S47- S60.
31. Hovda, D.A., Yoshino, A., Kawamata, T., Katayama, Y., and Becker, D.P. (1991). Diffuse prolonged depression of cerebral oxidative metabolism following concussive brain injury in the rat: A cytochrome oxidase histochemistry study. Brain Res. 567, 1-10.
32. Huang, R.Q., and Dillon, G.H. (1998). Maintenance of recombinant type A gamma-aminobutyric acid receptor function: Role of protein tyrosine phosphorylation and calcineurin. J. Pharmacol. Exp. Ther. 286, 243-255. (Pubitemid 28317997)
33. Jenkins, L.W., Peters, G.W., Dixon, C.E., Zhang, X., Clark, R.S., Skinner, J.C., Marion, D.W., Adelson, P.D., and Kochanek, P.M. (2002). 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. (Pubitemid 34761335)
34. Jiang, X.B., Ohno, K., Qian, L., Tominaga, B., Kuroiwa, T., Nariai, T., and Hirakawa, K. (2000). Changes in local cerebral blood flow, glucose utilization, and mitochondrial function following traumatic brain injury in rats. Neurol. Med. Chir. (Tokyo) 40, 16-28; discussion 28-19.
35. Kim, B.T., Rao, V.L., Sailor, K.A., Bowen, K.K., and Dempsey, R.J. (2001). Protective effects of glial cell line-derived neurotrophic factor on hippocampal neurons after traumatic brain injury in rats. J. Neurosurg. 95, 674-679. (Pubitemid 33031429)
36. Klee, C.B., Crouch, T.H., and Krinks, M.H. (1979). Calcineurin: A calcium- and calmodulin-binding protein of the nervous system. Proc. Natl. Acad. Sci. USA 76, 6270-6273. (Pubitemid 10163382)
37. Kobeissy, F.H., Ottens, A.K., Zhang, Z., Liu, M.C., Denslow, N.D., Dave, J.R., Tortella, F.C., Hayes, R.L., and Wang, K.K. (2006). Novel differential neuroproteomics analysis of traumatic brain injury in rats. Mol. Cell Proteomics 5, 1887-1898. (Pubitemid 44688197)
38. Kochanek, A.R., Kline, A.E., Gao, W.M., Chadha, M., Lai, Y., Clark, R.S., Dixon, C.E., and Jenkins, L.W. (2006). Gel-based hippocampal proteomic analysis 2 weeks following traumatic brain injury to immature rats using controlled cortical impact. Dev. Neurosci. 28, 410-419. (Pubitemid 44310507)
39. Kochanek, P.M. (1993). Ischemic and traumatic brain injury: Pathobiology and cellular mechanisms. Crit. Care Med. 21, S333- S335. (Pubitemid 23270533)
40. Laird, M.D., Vender, J.R., and Dhandapani, K.M. (2008). Opposing roles for reactive astrocytes following traumatic brain injury. Neurosignals 16, 154-164. (Pubitemid 351263222)
41. Lehninger, A.L. (1970). Biochemistry: The Molecular Basis of Cell Structure and Function. Worth Publishers: New York.
42. Lowenstein, D.H., Thomas, M.J., Smith, D.H., and McIntosh, T.K. (1992). Selective vulnerability of dentate hilar neurons following traumatic brain injury: A potential mechanistic link between head trauma and disorders of the hippocampus. J. Neurosci. 12, 4846-4853.
43. Lu, D., Goussev, A., Chen, J., Pannu, P., Li, Y., Mahmood, A., and Chopp, M. (2004). Atorvastatin reduces neurological deficit and increases synaptogenesis, angiogenesis, and neuronal survival in rats subjected to traumatic brain injury. J. Neurotrauma 21, 21-32. (Pubitemid 38141799)
44. Marmarou, C.R., and Povlishock, J.T. (2006). Administration of the immunophilin ligand FK506 differentially attenuates neurofilament compaction and impaired axonal transport in injured axons following diffuse traumatic brain injury. Exp. Neurol. 197, 353-362. (Pubitemid 43077143)
45. Matser, E.J., Kessels, A.G., Lezak, M.D., Jordan, B.D., and Troost, J. (1999). Neuropsychological impairment in amateur soccer players. JAMA 282, 971-973. (Pubitemid 29420317)
46. McNamara, R.K., Hussain, R.J., Simon, E.J., Stumpo, D.J., Blackshear, P.J., Abel, T., and Lenox, R.H. (2005). Effect of myristoylated alanine-rich C kinase substrate (MARCKS) overexpression on hippocampus-dependent learning and hippocampal synaptic plasticity in MARCKS transgenic mice. Hippocampus 15, 675-683. (Pubitemid 41149588)
47. Ohmitsu, M., Fukunaga, K., Yamamoto, H., and Miyamoto, E. (1999). Phosphorylation of myristoylated alanine-rich protein kinase C substrate by mitogen-activated protein kinase in cultured rat hippocampal neurons following stimulation of glutamate receptors. J. Biol. Chem. 274, 408-417. (Pubitemid 29035076)
48. Okonkwo, D.O., Melon, D.E., Pellicane, A.J., Mutlu, L.K., Rubin, D.G., Stone, J.R., and Helm, G.A. (2003). Dose-response of cyclosporin A in attenuating traumatic axonal injury in rat. Neuroreport 14, 463-466. (Pubitemid 36337951)
49. Ong, S.E., and Mann, M. (2005). Mass spectrometry-based proteomics turns quantitative. Nat. Chem. Biol. 1, 252-262.
50. Ong, S.E., Blagoev, B., Kratchmarova, I., Kristensen, D.B., Steen, H., Pandey, A., and Mann, M. (2002). Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell Proteomics 1, 376-386.
51. Ong, S.E., Foster, L.J., and Mann, M. (2003). Mass spectrometricbased approaches in quantitative proteomics. Methods 29, 124-130. (Pubitemid 36269199)
52. Oshima, T., Lee, S., Sato, A., Oda, S., Hirasawa, H., and Yamashita, T. (2009). TNF-alpha contributes to axonal sprouting and functional recovery following traumatic brain injury. Brain Res. 1290, 102-110.
53. Ottens, A.K., Kobeissy, F.H., Fuller, B.F., Liu, M.C., Oli, M.W., Hayes, R.L. and Wang, K.K. (2007). Novel neuroproteomic approaches to studying traumatic brain injury. Prog. Brain Res. 161, 401-418. (Pubitemid 47017418)
54. Palop, J.J., Mucke, L., and Roberson, E.D. (2011). Quantifying biomarkers of cognitive dysfunction and neuronal network hyperexcitability in mouse models of Alzheimer's disease: Depletion of calcium-dependent proteins and inhibitory hippocampal remodeling. Methods Mol. Biol. 670, 245-262.
55. Robel, S., Berninger, B., and Gotz, M. (2011). The stem cell potential of glia: Lessons from reactive gliosis. Nat. Rev. Neurosci. 12, 88-104.
56. Rusnak, F., and Mertz, P. (2000). Calcineurin: Form and function. Physiol. Rev. 80, 1483-1521.
57. Sadygov, R.G., Zhao, Y., Haidacher, S.J., Starkey, J.M., Tilton, R.G., and Denner, L. (2010). Using power spectrum analysis to evaluate (18)O-water labeling data acquired from low resolution mass spectrometers. J. Proteome Res. 9, 4306-4312.
58. Scheff, S.W., Price, D.A., Hicks, R.R., Baldwin, S.A., Robinson, S., and Brackney, C. (2005). Synaptogenesis in the hippocampal CA1 field following traumatic brain injury. J. Neurotrauma 22, 719-732. (Pubitemid 40995305)
59. Shapira, Y., Yadid, G., Cotev, S., and Shohami, E. (1989). Accumulation of calcium in the brain following head trauma. Neurol. Res. 11, 169-172. (Pubitemid 19274857)
60. Soares, H.D., Hicks, R.R., Smith, D., and McIntosh, T.K. (1995). Inflammatory leukocytic recruitment and diffuse neuronal degeneration are separate pathological processes resulting from traumatic brain injury. J. Neurosci. 15, 8223-8233. (Pubitemid 26006925)
61. Sosin, D.M., Sniezek, J.E., and Waxweiler, R.J. (1995). Trends in death associated with traumatic brain injury, 1979 through 1992. Success and failure. JAMA 273, 1778-1780.
62. Starkey, J.M., Zhao, Y., Sadygov, R.G., Haidacher, S.J., Lejeune, W.S., Dey, N., Luxon, B.A., Kane, M.A., Napoli, J.L., Denner, L., and Tilton, R.G. (2010). Altered retinoic acid metabolism in diabetic mouse kidney identified by O isotopic labeling and 2D mass spectrometry. PLoS One 5, e11095.
63. Stoica, B.A., and Faden, A.I. (2010). Cell death mechanisms and modulation in traumatic brain injury. Neurotherapeutics 7, 3-12.
64. Tan, S.E., Wenthold, R.J., and Soderling, T.R. (1994). Phosphorylation of AMPA-type glutamate receptors by calcium/calmodulindependent protein kinase II and protein kinase C in cultured hippocampal neurons. J. Neurosci. 14, 1123-1129.
65. Tao, W.A., and Aebersold, R. (2003). Advances in quantitative proteomics via stable isotope tagging and mass spectrometry. Curr. Opin. Biotechnol. 14, 110-118. (Pubitemid 36151851)
66. Tarasenko, Y.I., Yu, Y., Jordan, P.M., Bottenstein, J., and Wu, P. (2004). Effect of growth factors on proliferation and phenotypic differentiation of human fetal neural stem cells. J. Neurosci. Res. 78, 625-636. (Pubitemid 39657580)
67. Tilton, R.G., Haidacher, S.J., Lejeune, W.S., Zhang, X., Zhao, Y., Kurosky, A., Brasier, A.R., and Denner, L. (2007). Diabetes-induced changes in the renal cortical proteome assessed with two-dimensional gel electrophoresis and mass spectrometry. Proteomics 7, 1729-1742. (Pubitemid 46841832)
68. Tong, G., Shepherd, D., and Jahr, C.E. (1995). Synaptic desensitization of NMDA receptors by calcineurin. Science 267, 1510-1512.
69. Venkataramanan, R., Warty, V.S., Zemaitis, M.A., Sanghvi, A.T., Burckart, G.J., Seltman, H., Todo, S., Makowka, L., and Starzl, T.E. (1987). Biopharmaceutical aspects of FK-506. Transplant. Proc. 19, 30-35. (Pubitemid 17157075)
70. Wang, E., Gao, J., Yang, Q., Parsley, M., Dunn, T., Zhang, L., Dewitt, D., Denner, L., Prough, D.S., and Wu, P. (2011). Molecular mechanisms underlying effects of neural stem cells against traumatic axonal injury. J. Neurotrauma 29, 295-312.
71. Wang, K.K., Ottens, A., Haskins, W., Liu, M.C., Kobeissy, F., Denslow, N., Chen, S., and Hayes, R.L. (2004). Proteomics studies of traumatic brain injury. Int. Rev. Neurobiol. 61, 215-240. (Pubitemid 39752437)
72. Wang, Y., Shibasaki, F., and Mizuno, K. (2005). Calcium signalinduced cofilin dephosphorylation is mediated by Slingshot via calcineurin. J. Biol. Chem. 280, 12683-12689.
73. Whiteman, I.T., Gervasio, O.L., Cullen, K.M., Guillemin, G.J., Jeong, E.V., Witting, P.K., Antao, S.T., Minamide, L.S., Bamburg, J.R., and Goldsbury, C. (2009). Activated actin-depolymerizing factor/cofilin sequesters phosphorylated microtubule-associated protein during the assembly of alzheimer-like neuritic cytoskeletal striations. J. Neurosci. 29, 12994-13005.
74. Xiong, Y., Mahmood, A., and Chopp, M. (2010a). Angiogenesis, neurogenesis and brain recovery of function following injury. Curr. Opin. Investig. Drugs 11, 298-308.
75. Xiong, Y., Mahmood, A., and Chopp, M. (2010b). Neurorestorative treatments for traumatic brain injury. Discov. Med. 10, 434-442.
76. Yang, S.A., and Klee, C.B. (2000). Low affinity Ca2 + binding sites of calcineurin B mediate conformational changes in calcineurin A. Biochemistry (Mosc.) 39, 16147-16154. (Pubitemid 32038277)
77. Yang, X., Yang, S., Wang, J., Zhang, X., Wang, C., and Hong, G. (2009). Expressive proteomics profile changes of injured human brain cortex due to acute brain trauma. Brain Inj. 23, 830-840.
78. Yao, X., Freas, A., Ramirez, J., Demirev, P.A., and Fenselau, C. (2001). Proteolytic 18O labeling for comparative proteomics: Model studies with two serotypes of adenovirus. Anal. Chem. 73, 2836-2842. (Pubitemid 32868136)
79. Yi, J.H., and Hazell, A.S. (2006). Excitotoxic mechanisms and the role of astrocytic glutamate transporters in traumatic brain injury. Neurochem. Int. 48, 394-403. (Pubitemid 43327279)
80. Yoong, L.F., Wan, G., and Too, H.P. (2009). GDNF-induced cell signaling and neurite outgrowths are differentially mediated by GFRalpha1 isoforms. Mol. Cell. Neurosci. 41, 464-473.
81. Zhao, Y., Denner, L., Haidacher, S.J., LeJeune, W.S., and Tilton, R.G. (2008). Comprehensive analysis of the mouse renal cortex using twodimensional HPLC-tandem mass spectrometry. Proteome Sci. 6, 15.
82. Zhu, W.L., Shi, H.S., Wang, S.J., Wu, P., Ding, Z.B., and Lu, L. (2011). Hippocampal CA3 calcineurin activity participates in depressive-like behavior in rats. J. Neurochem. 117, 1075-1086.
83. Zuberovic, A., Wetterhall, M., Hanrieder, J., and Bergquist, J. (2009). CE MALDI-TOF/TOF MS for multiplexed quantification of proteins in human ventricular cerebrospinal fluid. Electrophoresis 30, 1836-1843.