Abstract
Despite the enormous medical and economic consequences of traumatic injury to the central nervous system (CNS), little is known about the proteins involved in the resulting pathology. Major advances in the identification of such proteins have been made in recent years through application of differential proteome analysis. Such an approach has revealed a number of novel proteins as potential regulators of the degenerative and regenerative processes that take place in the mammalian brain and spinal cord after a traumatic insult. Some of these proteins may serve as diagnostic and prognostic markers to assess the severity of tissue damage. Comparative proteome analysis of regeneration-competent vs. regeneration-deficient systems are likely to provide new insights into the cellular signals that could be targeted for therapeutic intervention to increase the repair capacity of the human CNS.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Abbreviations
- 2D PAGE:
-
Two-dimensional polyacrylamide gel electrophoresis
- CNS:
-
Central nervous system
- GFAP:
-
Glial fibrillary acidic protein
- SCI:
-
Spinal cord injury
- TBI:
-
Traumatic brain injury
References
Arvidsson, A., Collin, T., Kirik, D., Kokaia, Z., & Lindvall, O. (2002). Neuronal replacement from endogenous precursors in the adult brain after stroke. Nature Medicine, 8, 963–970.
Barnea, E., Sorkin, R., Ziv, T., Beer, I., & Admon, A. (2005). Evaluation of prefractionation methods as a preparatory step for multidimensional based chromatography of serum proteins. Proteomics, 5, 3367–3375.
Brown, M. E., & Bridgman, P. C. (2004). Myosin function in nervous and sensory systems. Journal of Neurobiology, 58, 118–130.
Burgess, J. A., Lescuyer, P., Hainard, A., Burkhard, P. R., Turck, N., Michel, P., et al. (2006). Identification of brain cell death associated proteins in human post-mortem cerebrospinal fluid. Journal of Proteome Research, 5, 1674–1681.
Busch, S. A., & Silver, J. (2007). The role of extracellular matrix in CNS regeneration. Current Opinion in Neurobiology, 17, 120–127.
Conti, A., Sanchez-Ruiz, Y., Bachi, A., Beretta, L., Grandi, E., Beltramo, M., et al. (2004). Proteome study of human cerebrospinal fluid following traumatic brain injury indicates fibrin(ogen) degradation products as trauma-associated markers. Journal of Neurotrauma, 21, 854–863.
Darling, D. L., Yingling, J., & Wynshaw-Boris, A. (2005). Role of 14-3-3 proteins in eukaryotic signaling and development. Current Topics in Developmental Biology, 68, 281–315.
Davidsson, P., Paulson, L., Hesse, C., Blennow, K., & Nilsson, C. L. (2001). Proteome studies of human cerebrospinal fluid and brain tissue using a preparative two-dimensional electrophoresis approach prior to mass spectrometry. Proteomics, 1, 444–452.
Dieringer, N. (2003). Activity-related postlesional vestibular reorganization. Annals of the New York Academy of Sciences, 1004, 50–60.
Ding, Q., Wu, Z., Guo, Y., Zhao, C., Jia, Y., Kong, F., et al. (2006). Proteome analysis of up-regulated proteins in the rat spinal cord induced by transection injury. Proteomics, 6, 505–518.
Doucet, A., & Overall, C. M. (2008). Protease proteomics: Revealing protease in vivo functions using systems biology approaches. Molecular Aspects of Medicine, 29, 339–358.
Fischer, R. S., & Fowler, V. M. (2003). Tropomodulins: Life at the slow end. Trends in Cell Biology, 13, 593–601.
Gao, Y., Thomas, J. O., Chow, R. L., Lee, G.-H., & Cowan, N. J. (1992). A cytoplasmic chaperonin that catalyzes β-actin folding. Cell, 69, 1043–1050.
Gorovits, R., Avidan, N., Avisar, N., Shaked, I., & Vardimon, L. (1997). Glutamine synthetase protects against neuronal degeneration in injured retinal tissue. Proceedings of the National Academy of Sciences of the United States of America, 94, 7024–7029.
Graeber, M. B., Raivich, G., & Kreutzberg, G. W. (1989). Increase of transferrin receptors and iron uptake in regenerating motor neurons. Journal of Neuroscience Research, 23, 342–345.
Grosche, J., Hartig, W., & Reichenbach, A. (1995). Expression of glial fibrillary acidic protein (GFAP), glutamine synthetase (GS), and Bcl-2 protooncogene protein by Müller (glial) cells in retinal light damage of rats. Neuroscience Letters, 185, 119–122.
Han, Z. G., Zhang, Q. H., Ye, M., Kan, L. X., Gu, B. W., He, K. L., et al. (1999). Molecular cloning of six novel Krüppel-like zinc finger genes from hematopoietic cells and identification of a novel transregulatory domain KRNB. Journal of Biological Chemistry, 274, 35741–35748.
Härtig, W., Grosche, J., Distler, C., Grimm, D., el-Hifnawi, E., & Reichenbach, A. (1995). Alterations of Müller (glial) cells in dystrophic retinae of RCS rats. Journal of Neurocytology, 24, 507–517.
Hattori, T., Takei, N., Mizuno, Y., Kato, K., & Kohsaka, S. (1995). Neurotrophic and neuroprotective effects of neuron-specific enolase on cultured neurons from embryonic rat brain. Neuroscience Research, 21, 191–198.
Hedgecock, E. M., Culotti, J. G., Thomson, J. N., & Perkins, L. A. (1985). Axonal guidance mutants of Caenorhabditis elegans identified by filling sensory neurons with fluorescein dyes. Developmental Biology, 111, 158–170.
Hermeking, H., & Benzinger, A. (2006). 14-3-3 proteins in cell cycle regulation. Seminars in Cancer Biology, 16, 183–192.
Hinsch, K., & Zupanc, G. K. H. (2006). Isolation, cultivation, and differentiation of neural stem cells from adult fish brain. Journal of Neuroscience Methods, 158, 75–88.
Hinsch, K., & Zupanc, G. K. H. (2007). Generation and long-term persistence of new neurons in the adult zebrafish brain: A quantitative analysis. Neuroscience, 146, 679–696.
Hitchcock, P., Ochocinska, M., Sieh, A., & Otteson, D. (2004). Persistent and injury-induced neurogenesis in the vertebrate retina. Progress in Retinal and Eye Research, 23, 183–194.
Hitchcock, P. F., & Raymond, P. A. (1992). Retinal regeneration. Trends in Neurosciences, 15, 103–108.
Horie, H., Inagaki, Y., Sohma, Y., Nozawa, R., Okawa, K., Hasegawa, M., et al. (1999). Galectin-1 regulates initial axonal growth in peripheral nerves after axotomy. Journal of Neuroscience, 19, 9964–9974.
Inagaki, Y., Sohma, Y., Horie, H., Nozawa, R., & Kadoya, T. (2000). Oxidized galectin-1 promotes axonal regeneration in peripheral nerves but does not possess lectin properties. European Journal of Biochemistry, 267, 2955–2964.
Jenkins, L. W., Peters, G. W., Dixon, C. E., Zhang, X., Clark, R. S. B., Skinner, J. C., et al. (2002). Conventional and functional proteomics using large format two-dimensional gel electrophoresis 24 hours after controlled cortical impact in postnatal day 17 rats. Journal of Neurotrauma, 19, 715–740.
Johansson, B. B. (2007). Regeneration and plasticity in the brain and spinal cord. Journal of Cerebral Blood Flow and Metabolism, 27, 1417–1430.
Kang, S. K., So, H. H., Moon, Y. S., & Kim, C. H. (2006). Proteomic analysis of injured spinal cord tissue proteins using 2-DE and MALDI-TOF MS. Proteomics, 6, 2797–2812.
Kanner, A. A., Marchi, N., Fazio, V., Mayberg, M. R., Koltz, M. T., Siomin, V., et al. (2003). Serum S100beta: A noninvasive marker of blood-brain barrier function and brain lesions. Cancer, 97, 2806–2813.
Kiang, J. G., & Tsokos, G. C. (1998). Heat shock protein 70 kDa: Molecular biology, biochemistry, and physiology. Pharmacology & Therapeutics, 80, 183–201.
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. Molecular & Cellular Proteomics, 5, 1887–1898.
Kochanek, A. R., Kline, A. E., Gao, W.-M., Chadha, M., Lai, Y., Clark, R. S. B., et al. (2006). Gel-based hippocampal proteomic analysis 2 weeks following traumatic brain injury to immature rats using controlled cortical impact. Developmental Neuroscience, 28, 410–419.
Lacour, M. (2006). Restoration of vestibular function: Basic aspects and practical advances for rehabilitation. Current Medical Research and Opinion, 22, 1651–1659.
Lai, J. C. K., Murthy, C. R. K., Cooper, A. J. L., Hertz, E., & Hertz, L. (1989). Differential effects of ammonia and β-methylene-DL-aspartate on metabolism of glutamate and related amino acids by astrocytes and neurons in primary culture. Neurochemical Research, 14, 377–389.
Lee, T. H., Lwu, S., Kim, J., & Pelletier, J. (2002). Inhibition of Wilms tumor 1 transactivation by bone marrow zinc finger 2, a novel transcriptional repressor. Journal of Biological Chemistry, 277, 44826–44837.
Leung, C. L., Zheng, M., Prater, S. M., & Liem, R. K. (2001). The BPAG1 locus: Alternative splicing produces multiple isoforms with distinct cytoskeletal linker domains, including predominant isoforms in neurons and muscles. Journal of Cell Biology, 154, 691–697.
Lewis, G. P., Erickson, P. A., Guerin, C. J., Anderson, D. H., & Fisher, S. K. (1989). Changes in the expression of specific Müller cell proteins during long-term retinal detachment. Experimental Eye Research, 49, 93–111.
Lewis, G. P., Guerin, C. J., Anderson, D. H., Matsumoto, B., & Fisher, S. K. (1994). Rapid changes in the expression of glial cell proteins caused by experimental retinal detachment. American Journal of Ophthalmology, 118, 368–376.
Li, A., Lane, W. S., Johnson, L. V., Chader, G. J., & Tombran-Tink, J. (1995). Neuron-specific enolase: A neuronal survival factor in the retinal extracellular matrix? Journal of Neuroscience, 15, 385–393.
Lifshitz, J., Sullivan, P. G., Hovda, D. A., Wieloch, T., & McIntosh, T. K. (2004). Mitochondrial damage and dysfunction in traumatic brain injury. Mitochondrion, 4, 705–713.
Lilley, K. S., Razzaq, A., & Dupree, P. (2002). Two-dimensional gel electrophoresis: Recent advances in sample preparation, detection and quantitation. Current Opinion in Chemical Biology, 6, 46–50.
Lin, R. C. S., & Matesic, D. F. (1994). Immunohistochemical demonstration of neuron-specific enolase and microtubule-associated protein 2 in reactive astrocytes after injury in the adult forebrain. Neuroscience, 60, 11–16.
Lopez, M. F., Kristal, B. S., Chernokalskaya, E., Lazarev, A., Shestopalov, A. I., Bogdanova, A., et al. (2000). High-throughput profiling of the mitochondrial proteome using affinity fractionation and automation. Electrophoresis, 21, 3427–3440.
López-Otín, C., & Overall, C. M. (2002). Protease degradomics: A new challenge for proteomics. Nature Reviews Molecular Cell Biology, 3, 509–519.
Loy, D. N., Sroufe, A. E., Pelt, J. L., Burke, D. A., Cao, Q.-L., Talbott, J. F., et al. (2005). Serum biomarkers for experimental acute spinal cord injury: Rapid elevation of neuron-specific enolase and S-100β. Neurosurgery, 56, 391–397.
Lund, L. M., Machado, V. M., & McQuarrie, I. G. (2002). Increased β-actin and tubulin polymerization in regrowing axons: Relationship to the conditioning lesion effect. Experimental Neurology, 178, 306–312.
Lund, L. M., & McQuarrie, I. G. (1996). Axonal regrowth upregulates β-actin and Jun D mRNA expression. Journal of Neurobiology, 31, 476–486.
Marouga, R., David, S., & Hawkins, E. (2005). The development of the DIGE system: 2D fluorescence difference gel analysis technology. Analytical and Bioanalytical Chemistry, 382, 669–678.
Michetti, F., & Gazzolo, D. (2002). S100B protein in biological fluids: A tool for perinatal medicine. Clinical Chemistry, 48, 2097–2104.
Michetti, F., Massaro, A., & Murazio, M. (1979). The nervous system-specific S-100 antigen in cerebrospinal fluid of multiple sclerosis patients. Neuroscience Letters, 11, 171–175.
Michetti, F., Massaro, A., Russo, G., & Rigon, G. (1980). The S-100 antigen in cerebrospinal fluid as a possible index of cell injury in the nervous system. Journal of the Neurological Sciences, 44, 259–263.
Monteoliva, L., & Albar, J. P. (2004). Differential proteomics: An overview of gel and non-gel based approaches. Briefings in Functional Genomics & Proteomics, 3, 220–239.
Nakamura, F., Kalb, R. G., & Strittmatter, S. M. (2000). Molecular basis of semaphorin-mediated axon guidance. Journal of Neurobiology, 44, 219–229.
Neuhoff, V., Arold, N., Taube, D., & Ehrhardt, W. (1988). Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis, 9, 255–262.
Nicholls, D. G., & Budd, S. L. (2000). Mitochondria and neuronal survival. Physiological Reviews, 80, 315–360.
Oliver, C. N., Starke-Reed, P. E., Stadtman, E. R., Liu, G. J., Carney, J. M., & Floyd, R. A. (1990). Oxidative damage to brain proteins, loss of glutamine synthetase activity, and production of free radicals during ischemia/reperfusion-induced injury to gerbil brain. Proceedings of the National Academy of Sciences of the United States of America, 87, 5144–5147.
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. Journal of Neurotrauma, 24, 772–789.
Ott, R., Zupanc, G. K. H., & Horschke, I. (1997). Long-term survival of postembryonically born cells in the cerebellum of gymnotiform fish, Apteronotus leptorhynchus. Neuroscience Letters, 221, 185–188.
Otteson, D. C., & Hitchcock, P. F. (2003). Stem cells in the teleost retina: Persistent neurogenesis and injury-induced regeneration. Vision Research, 43, 927–936.
Paramio, J. M., Casanova, M. L., Segrelles, C., Mittnacht, S., Lane, E. B., & Jorcano, J. L. (1999). Modulation of cell proliferation by cytokeratins K10 and K16. Molecular and Cellular Biology, 19, 3086–3094.
Paterson, J. M., Short, D., Flatman, P. W., Seckl, J. R., Aitken, A., & Dutia, M. B. (2006). Changes in protein expression in the rat medial vestibular nuclei during vestibular compensation. Journal of Physiology, 575, 777–788.
Payne, B. R., & Lomber, S. G. (2002). Plasticity of the visual cortex after injury: What’s different about the young brain? The Neuroscientist, 8, 174–185.
Pekny, M., & Nilsson, M. (2005). Astrocyte activation and reactive gliosis. Glia, 50, 427–434.
Pineda, J. A., Wang, K. K. W., & Hayes, R. L. (2004). Biomarkers of proteolytic damage following traumatic brain injury. Brain Pathology, 14, 202–209.
Porter, G. W., Khuri, F. R., & Fu, H. (2006). Dynamic 14-3-3/client protein interactions integrate survival and apoptotic pathways. Seminars in Cancer Biology, 16, 193–202.
Raivich, G., Graeber, M. B., Gehrmann, J., & Kreutzberg, G. W. (1991). Transferrin receptor expression and iron uptake in the injured and regenerating rat sciatic nerve. European Journal of Neuroscience, 3, 919–927.
Reaume, A. G., Elliott, J. L., Hoffman, E. K., Kowall, N. W., Ferrante, R. J., Siwek, D. R., et al. (1996). Motor neurons in Cu/Zn superoxide dismutase-deficient mice develop normally but exhibit enhanced cell death after axonal injury. Nature Genetics, 13, 43–47.
Rego, A. C., & Oliveira, C. R. (2003). Mitochondrial dysfunction and reactive oxygen species in excitotoxicity and apoptosis: Implications for the pathogenesis of neurodegenerative diseases. Neurochemical Research, 28, 1563–1574.
Romeo, M. J., Espina, V., Lowenthal, M., Espina, B. H., Petricoin, E. F., III, & Liotta, L. A. (2005). CSF proteome: A protein repository for potential biomarker identification. Expert Review of Proteomics, 2, 57–70.
Rowland, L. P., & Sciarra, D. (1989). Trauma. In L. P. Rowland (Ed.), Merritt’s textbook of neurology (8th ed., pp. 369–393). Philadelphia, London: Lea & Febiger.
Santos, M., Paramio, J. M., Bravo, A., Ramirez, A., & Jorcano, J. L. (2002). The expression of keratin K10 in the basal layer of the epidermis inhibits cell proliferation and prevents skin tumorigenesis. Journal of Biological Chemistry, 277, 19122–19130.
Segal, M. B. (1993). Extracellular and cerebrospinal fluids. Journal of Inherited Metabolic Disease, 16, 617–638.
Segal, M. B. (2000). The choroid plexuses and the barriers between the blood and the cerebrospinal fluid. Cellular and Molecular Neurobiology, 20, 183–196.
Serna-Sanz, A., Rairdan, G., & Peck, S. C. (2007). Preparative denaturing isoelectric focusing for enhancing sensitivity of proteomic studies. Methods of Molecular Biology, 354, 99–104.
Sickmann, A., Dormeyer, W., Wortelkamp, S., Woitalla, D., Kuhn, W., & Meyer, H. E. (2000). Identification of proteins from human cerebrospinal fluid, separated by two-dimensional polyacrylamide gel electrophoresis. Electrophoresis, 21, 2721–2728.
Sickmann, A., Dormeyer, W., Wortelkamp, S., Woitalla, D., Kuhn, W., & Meyer, H. E. (2002). Towards a high resolution separation of human cerebrospinal fluid. Journal of Chromatography B, 771, 167–196.
Siddiqui, S. S., & Culotti, J. G. (1991). Examination of neurons in wild type and mutants of Caenorhabditis elegans using antibodies to horseradish peroxidase. Journal of Neurogenetics, 7, 193–211.
Siman, R., McIntosh, T. K., Soltesz, K. M., Chen, Z., Neumar, R. W., & Roberts, V. L. (2004). Proteins released from degenerating neurons are surrogate markers for acute brain damage. Neurobiology of Disease, 16, 311–320.
Sirivatanauksorn, Y., Drury, R., Crnogorac-Jurcevic, T., Sirivatanauksorn, V., & Lemoine, N. R. (1999). Laser-assisted microdissection: Applications in molecular pathology. Journal of Pathology, 189, 150–154.
Slemmer, J. E., Weber, J. T., & De Zeeuw, C. I. (2004). Cell death, glial protein alterations and elevated S-100β release in cerebellar cell cultures following mechanically induced trauma. Neurobiology of Disease, 15, 563–572.
Smith, C. D., Carney, J. M., Starke-Reed, P. E., Oliver, C. N., Stadtman, E. R., Floyd, R. A., et al. (1991). Excess brain protein oxidation and enzyme dysfunction in normal aging and in Alzheimer disease. Proceedings of the National Academy of Sciences of the United States of America, 88, 10540–10543.
Sofroniew, M. V. (2005). Reactive astrocytes in neural repair and protection. The Neuroscientist, 11, 400–407.
Sommer, J. B., Gaul, C., Heckmann, J., Neundörfer, B., & Erbguth, F. J. (2002). Does lumbar cerebrospinal fluid reflect ventricular cerebrospinal fluid? A prospective study in patients with external ventricular drainage. European Neurology, 47, 224–232.
Sullivan, P. G., Rabchevsky, A. G., Waldmeier, P. C., & Springer, J. E. (2005). Mitochondrial permeability transition in CNS trauma: Cause or effect of neuronal cell death? Journal of Neuroscience Research, 79, 231–239.
Suzuki, M., Yakushiji, N., Nakada, Y., Satoh, A., Ide, H., & Tamura, K. (2006). Limb regeneration in Xenopus laevis froglet. ScientificWorld Journal, 6(suppl 1), 26–37.
Takei, N., Kondo, J., Nagaike, K., Ohsawa, K., Kato, K., & Kohsaka, S. (1991). Neuronal survival factor from bovine brain is identical to neuron-specific enolase. Journal of Neurochemistry, 57, 1178–1184.
Tang, H.-Y., Ali-Khan, N., Echan, L. A., Levenkova, N., Rux, J. J., & Speicher, D. W. (2005). A novel four-dimensional strategy combining protein and peptide separation methods enables detection of low-abundance proteins in human plasma and serum proteomes. Proteomics, 5, 3329–3342.
Tetzlaff, W., Alexander, S. W., Miller, F. D., & Bisby, M. A. (1991). Response of facial and rubrospinal neurons to axotomy: Changes in mRNA expression for cytoskeletal proteins and GAP-43. Journal of Neuroscience, 11, 2528–2544.
Tonge, R., Shaw, J., Middleton, B., Rowlinson, R., Rayner, S., Young, J., et al. (2001). Validation and development of fluorescence two-dimensional differential gel electrophoresis proteomics technology. Proteomics, 1, 377–396.
Tsai, M.-C., Shen, L.-F., Kuo, H.-S., Cheng, H., & Chak, K.-F. (2008). Involvement of acidic fibroblast growth factor in spinal cord injury repair processes revealed by a proteomics approach. Molecular & Cellular Proteomics, 7, 1668–1687.
Tsuchiya, D., Hong, S., Matsumori, Y., Kayama, T., Swanson, R. A., Dillman, W. H., et al. (2003). Overexpression of rat heat shock protein 70 reduces neuronal injury after transient focal ischemia, transient global ischemia, or kainic acid-induced seizures. Neurosurgery, 53, 1179–1188.
Vance, J. E., Campenot, R. B., & Vance, D. E. (2000). The synthesis and transport of lipids for axonal growth and nerve regeneration. Biochimica et Biophysica Acta, 1486, 84–96.
Weisner, B., & Bernhardt, W. (1978). Protein fractions of lumbar, cisternal, and ventricular cerebrospinal fluid: Separate areas of reference. Journal of the Neurological Sciences, 37, 205–214.
Yaffe, M. B., Farr, G. W., Miklos, D., Horwich, A. L., Sternlicht, M. L., & Sternlicht, H. (1992). TCP1 complex is a molecular chaperone in tubulin biogenesis. Nature, 358, 245–248.
Yang, Y., Dowling, J., Yu, Q.-C., Kouklis, P., Cleveland, D. W., & Fuchs, E. (1996). An essential cytoskeletal linker protein connecting actin microfilaments to intermediate filaments. Cell, 86, 655–665.
Yin, M., Wheeler, M. D., Connor, H. D., Zhong, Z., Bunzendahl, H., Dikalova, A., et al. (2001). Cu/Zn-superoxide dismutase gene attenuates ischemia-reperfusion injury in the rat kidney. Journal of the American Society of Nephrology, 12, 2691–2700.
Yoshida, M., Muneyuki, E., & Hisabori, T. (2001). ATP synthase: A marvellous rotary engine of the cell. Nature Reviews Molecular Cell Biology, 2, 669–677.
Yuan, X., & Desiderio, D. M. (2005). Proteomics analysis of prefractionated human lumbar cerebrospinal fluid. Proteomics, 5, 541–550.
Yuan, X., Russell, T., Wood, G., & Desiderio, D. M. (2002). Analysis of the human lumbar cerebrospinal fluid proteome. Electrophoresis, 23, 1185–1196.
Zappaterra, M. D., Lisgo, S. N., Lindsay, S., Gygi, S. P., Walsh, C. A., & Ballif, B. A. (2007). A comparative proteomic analysis of human and rat embryonic cerebrospinal fluid. Journal of Proteome Research, 6, 3537–3548.
Zupanc, G. K. H. (2006a). Neurogenesis and neuronal regeneration in the adult fish brain. Journal of Comparative Physiology A, 192, 649–670.
Zupanc, G. K. H. (2006b). Adult neurogenesis and neuronal regeneration in the teleost fish brain: Implications for the evolution of a primitive vertebrate trait. In T. H. Bullock & L. R. Rubenstein (Eds.), The evolution of nervous systems in non-mammalian vertebrates (pp. 485–520). Oxford: Academic.
Zupanc, G. K. H. (2008a). Adult neurogenesis in teleost fish. In F. H. Gage, G. Kempermann, & H. Song (Eds.), Adult neurogenesis (pp. 571–592). New York: Cold Spring Harbor Laboratory Press.
Zupanc, G. K. H. (2008b). Adult neurogenesis and neuronal regeneration in the brain of teleost fish. Journal of Physiology (Paris), 102, 357–373.
Zupanc, G. K. H., Clint, S. C., Takimoto, N., Hughes, A. T. L., Wellbrock, U. M., & Meissner, D. (2003). Spatio-temporal distribution of microglia/macrophages during regeneration in the cerebellum of adult teleost fish. Apteronotus leptorhynchus: A quantitative analysis. Brain Behavior and Evolution, 62, 31–42.
Zupanc, G. K. H., Hinsch, K., & Gage, F. H. (2005). Proliferation, migration, neuronal differentiation, and long-term survival of new cells in the adult zebrafish brain. Journal of Comparative Neurology, 488, 290–319.
Zupanc, G. K. H., & Horschke, I. (1995). Proliferation zones in the brain of adult gymnotiform fish: A quantitative mapping study. Journal of Comparative Neurology, 353, 213–233.
Zupanc, G. K. H., Horschke, I., Ott, R., & Rascher, G. B. (1996). Postembryonic development of the cerebellum in gymnotiform fish. Journal of Comparative Neurology, 370, 443–464.
Zupanc, G. K. H., Kompass, K. S., Horschke, I., Ott, R., & Schwarz, H. (1998). Apoptosis after injuries in the cerebellum of adult teleost fish. Experimental Neurology, 152, 221–230.
Zupanc, G. K. H., & Ott, R. (1999). Cell proliferation after lesions in the cerebellum of adult teleost fish: Time course, origin, and type of new cells produced. Experimental Neurology, 160, 78–87.
Zupanc, G. K. H., & Zupanc, M. M. (2006). New neurons for the injured brain: Mechanisms of neuronal regeneration in adult teleost fish. Regenerative Medicine, 1, 207–216.
Zupanc, M. M., Wellbrock, U. M., & Zupanc, G. K. H. (2006). Proteome analysis identifies novel protein candidates involved in regeneration of the cerebellum of teleost fish. Proteomics, 6, 577–696.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2011 Springer Science+Business Media, LLC
About this chapter
Cite this chapter
Zupanc, G.K.H., Zupanc, M.M. (2011). Proteomic Analysis of CNS Injury and Recovery. In: Clelland, J. (eds) Genomics, Proteomics, and the Nervous System. Advances in Neurobiology, vol 2. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-7197-5_20
Download citation
DOI: https://doi.org/10.1007/978-1-4419-7197-5_20
Published:
Publisher Name: Springer, New York, NY
Print ISBN: 978-1-4419-7196-8
Online ISBN: 978-1-4419-7197-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)