Skip to main content
SpringerLink
Log in

Expression Profiling Following Traumatic Brain Injury: A Review

  • Published:
Neurochemical Research Aims and scope Submit manuscript

Abstract

Traumatic brain injury (TBI) elicits a complex sequence of putative autodestructive and neuroprotective cellular cascades. It is hypothesized that the genomic responses of cells in the injured brain serve as the basis for these cascades. Traditional methods for analyzing differential gene expression following brain trauma demonstrate that immediate early genes, cytokines, transcription factors, and neurotrophic factors can all participate in the brain's active and directed response to injury, and may do so concurrently. It is this complexity and multiplicity of interrelated molecular mechanisms that has demanded new methods for comprehensive and parallel evaluation of putative as well as novel gene targets. Recent advances in DNA microarray technology have enabled the simultaneous evaluation of thousands of genes and the subsequent generation of massive amounts of biological data relevant to CNS injury. This emerging technology can serve to further current knowledge regarding recognized molecular cascades as well as to identify novel molecular mechanisms that occur throughout the post-traumatic period. The elucidation of the complex alterations in gene expression underlying the pathological sequelae following TBI is of central importance in the design of future therapeutic agents.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

REFERENCES

  1. Raghupathi, R., McIntosh, T. K., and Smith, D. H. 1995. Cellular responses to experimental brain injury. Brain Pathol. 5:437-442.

    Google Scholar 

  2. Hayes, R. L., Yang, K., Raghupathi, R., and McIntosh, T. K. 1995. Changes in gene expression following traumatic brain injury in the rat. J. Neurotrauma 12:779-790.

    Google Scholar 

  3. McIntosh, T. K., Saatman, K. E., Raghupathi, R., Graham, D. I., Smith, D. H., Lee, V. M., and Trojanowski, J. Q. 1998. The Dorothy Russell Memorial Lecture. The molecular and cellular sequelae of experimental traumatic brain injury: Pathogenetic mechanisms. Neuropathol. Appl. Neurobiol. 24:251-267.

    Google Scholar 

  4. Lobenhofer, E. K., Bushel, P. R., Afshari, C. A., and Hamadeh, H. K. 2001. Progress in the application of DNA microarrays. Environ. Health Perspect. 109:881-891.

    Google Scholar 

  5. Noordewier, M. O. and Warren, P. V. 2001. Gene expression microarrays and the integration of biological knowledge. Trends Biotechnol. 19:412-415.

    Google Scholar 

  6. Eberwine, J., Yeh, H., Miyashiro, K., Cao, Y., Nair, S., Finnell, R., Zettel, M., and Coleman, P. 1992. Analysis of gene expression in single live neurons. Proc. Natl. Acad. Sci. USA 89:3010-3014.

    Google Scholar 

  7. Eberwine, J. 1996. Amplification of mRNA populations using aRNA generated from immobilized oligo(dT)-T7 primed cDNA. Biotechniques 20:584-591.

    Google Scholar 

  8. O'Dell, D. M., Raghupathi, R., Crino, P. B., Morrison, B., Eberwine, J. H., and McIntosh, T. K. 1998. Amplification of mRNAs from single, fixed, TUNEL-positive cells. Biotechniques 25:566-568.

    Google Scholar 

  9. Alwine, J. C., Kemp, D. J., and Stark, G. R. 1977. Method for detection of specific RNAs in agarose gels by transfer to diazobenzyloxymethyl-paper and hybridization with DNA probes. Proc. Natl. Acad. Sci. USA 74:5350-5354.

    Google Scholar 

  10. Melton, D. A., Krieg, P. A., Rebagliati, M. R., Maniatis, T., Zinn, K., and Green, M. R. 1984. Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Res. 12:7035-7056.

    Google Scholar 

  11. Hansen, J. N., Pheiffer, B. H., and Hough, C. J. 1974. Hybrid isolation by recovery of RNA-DNA hybrids from agar using S1 nuclease. Nucleic Acids Res. 1:787-801.

    Google Scholar 

  12. Kuang, W. W., Thompson, D. A., Hoch, R. V., and Weigel, R. J. 1998. Differential screening and suppression subtractive hybridization identified genes differentially expressed in an estrogen receptor-positive breast carcinoma cell line. Nucleic Acids Res. 26:1116-1123.

    Google Scholar 

  13. Bustin, S. A. 2000. Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J. Mol. Endocrinol. 25:169-193.

    Google Scholar 

  14. Prediger, E. A. 2001. Detection and quantitation of mRNAs using ribonuclease protection assays. Methods Mol. Biol. 160:495-505.

    Google Scholar 

  15. Porchet, N. and Aubert, J. P. 2000. Northern blot analysis of large mRNAs. Methods Mol. Biol. 125:305-312.

    Google Scholar 

  16. Larsson, L. G., Gray, H. E., Totterman, T., Pettersson, U., and Nilsson, K. 1987. Drastically increased expression of MYC and FOS protooncogenes during in vitro differentiation of chronic lymphocytic leukemia cells. Proc. Natl. Acad. Sci. USA 84:223-227.

    Google Scholar 

  17. Sheng, M. and Greenberg, M. E. 1990. The regulation and function of c-fos and other immediate early genes in the nervous system. Neuron 4:477-485.

    Google Scholar 

  18. Angel, P. and Karin, M. 1991. The role of Jun, Fos and the AP-1 complex in cell-proliferation and transformation. Biochim. Biophys. Acta 1072:129-157.

    Google Scholar 

  19. D'Mello, S. R. and Heinrich, G. 1991. Multiple signalling pathways interact in the regulation of nerve growth factor production in L929 fibroblasts. J. Neurochem. 57:1570-1576.

    Google Scholar 

  20. Quitschke, W. W. and Goldgaber, D. 1992. The amyloid beta-protein precursor promoter. A region essential for transcriptional activity contains a nuclear factor binding domain. J. Biol. Chem. 267:17362-17368.

    Google Scholar 

  21. Morgan, J. L. and Curran, T. 1991. Stimulus-transcription coupling in the nervous system: Involvement of the inducible protooncogenes fos and jun. Annu. Rev. Neurosci. 14:421-451.

    Google Scholar 

  22. Dragunow, M., Young, D., Hughes, P., MacGibbon, G., Lawlor, P., Singleton, K., Sirimanne, E., Beilharz, E., and Gluckman, P. 1993. Is c-Jun involved in nerve cell death following status epilepticus and hypoxic-ischaemic brain injury? Brain Res. Mol. Brain Res. 18:347-352.

    Google Scholar 

  23. Smeyne, R. J., Vendrell, M., Hayward, M., Baker, S. J., Miao, G. G., Schilling, K., Robertson, L. M., Curran, T., and Morgan, J. I. 1993. Continuous c-fos expression precedes programmed cell death in vivo. Nature 363:166-169.

    Google Scholar 

  24. An, G., Lin, T. N., Liu, J. S., Xue, J. J., He, Y. Y., and Hsu, C. Y. 1993. Expression of c-fos and c-jun family genes after focal cerebral ischemia. Ann. Neurol. 33:457-464.

    Google Scholar 

  25. Dragunow, M. and Robertson, H. A. 1987. Kindling stimulation induces c-fos protein(s) in granule cells of the rat dentate gyrus. Nature 329:441-442.

    Google Scholar 

  26. Phillips, L. L. and Belardo, E. T. 1992. Expression of c-fos in the hippocampus following mild and moderate fluid percussion brain injury. J. Neurotrauma 9:323-333.

    Google Scholar 

  27. Ruzdijic, S., Pekovic, S., Kanazir, S., Ivkovic, S., Stojiljkovic, M., and Rakic, L. 1993. Temporal and spatial preferences of c-fos mRNA expression in the rat brain following cortical lesion. Brain Res. 601:230-240.

    Google Scholar 

  28. Raghupathi, R., Welsh, F. A., Lowenstein, D. H., Gennarelli, T. A., and McIntosh, T. K. 1995. Regional induction of c-fos and heat shock protein-72 mRNA following fluid-percussion brain injury in the rat. J. Cereb. Blood. Flow Metab. 15:467-473.

    Google Scholar 

  29. Yang, K., Mu, X. S., Xue, J. J., Whitson, J., Salminen, A., Dixon, C. E., Liu, P. K., and Hayes, R. L. 1994. Increased expression of c-fos mRNA and AP-1 transcription factors after cortical impact injury in rats. Brain Res. 664:141-147.

    Google Scholar 

  30. Raghupathi, R. and McIntosh, T. K. 1996. Regionally and temporally distinct patterns of induction of c-fos, c-jun and junB mRNAs following experimental brain injury in the rat. Brain Res. Mol. Brain Res. 37:134-144.

    Google Scholar 

  31. McIntosh, T. K. 1994. Neurochemical sequelae of traumatic brain injury: Therapeutic implications. Cerebrovasc. Brain Metab. Rev. 6:109-162.

    Google Scholar 

  32. Sharp, F. R. and Sagar, S. M. 1994. Alterations in gene expression as an index of neuronal injury: Heat shock and the immediate early gene response. Neurotoxicology 15:51-59.

    Google Scholar 

  33. Kinouchi, H., Sharp, F. R., Chan, P. H., Koistinaho, J., Sagar, S. M., and Yoshimoto, T. 1994. Induction of c-fos, junB, c-jun, and hsp70 mRNA in cortex, thalamus, basal ganglia, and hippocampus following middle cerebral artery occlusion. J. Cereb. Blood Flow Metab. 14:808-817.

    Google Scholar 

  34. Nowak, T. S., Jr., Bond, U., and Schlesinger, M. J. 1990. Heat shock RNA levels in brain and other tissues after hyperthermia and transient ischemia. J. Neurochem. 54:451-458.

    Google Scholar 

  35. Welsh, F. A., Moyer, D. J., and Harris, V. A. 1992. Regional expression of heat shock protein-70 mRNA and c-fos mRNA following focal ischemia in rat brain. J. Cereb. Blood Flow Metab. 12:204-212.

    Google Scholar 

  36. Lowenstein, D. H., Simon, R. P., and Sharp, F. R. 1990. The pattern of 72-kDa heat shock protein-like immunoreactivity in the rat brain following flurothyl-induced status epilepticus. Brain Res. 531:173-182.

    Google Scholar 

  37. Brown, I. R., Rush, S., and Ivy, G. O. 1989. Induction of a heat shock gene at the site of tissue injury in the rat brain. Neuron 2:1559-1564.

    Google Scholar 

  38. Schiaffonati, L., Rappocciolo, E., Tacchini, L., Cairo, G., and Bernelli-Zazzera, A. 1990. Reprogramming of gene expression in postischemic rat liver: Induction of proto-oncogenes and hsp 70 gene family. J. Cell Physiol. 143:79-87.

    Google Scholar 

  39. Pelham, H. R. 1986. Speculations on the functions of the major heat shock and glucose-regulated proteins. Cell 46:959-961.

    Google Scholar 

  40. Beckmann, R. P., Mizzen, L. E., and Welch, W. J. 1990. Interaction of Hsp 70 with newly synthesized proteins: Implications for protein folding and assembly. Science 248:850-854.

    Google Scholar 

  41. Hightower, L. E. 1991. Heat shock, stress proteins, chaperones, and proteotoxicity. Cell 66:191-197.

    Google Scholar 

  42. Burdon, R. H. 1986. Heat shock and the heat shock proteins. Biochem. J. 240:313-324.

    Google Scholar 

  43. Rordorf, G., Koroshetz, W. J., and Bonventre, J. V. 1991. Heat shock protects cultured neurons from glutamate toxicity. Neuron 7:1043-1051.

    Google Scholar 

  44. Tanno, H., Nockels, R. P., Pitts, L. H., and Noble, L. J. 1993. Immunolocalization of heat shock protein after fluid percussive brain injury and relationship to breakdown of the blood-brain barrier. J. Cereb. Blood Flow Metab. 13:116-124.

    Google Scholar 

  45. Lowenstein, D. H., Gwinn, R. P., Seren, M. S., Simon, R. P., and McIntosh, T. K. 1994. Increased expression of mRNA encoding calbindin-D28K, the glucose-regulated proteins, or the 72 kDa heat-shock protein in three models of acute CNS injury. Brain Res. Mol. Brain Res. 22:299-308.

    Google Scholar 

  46. Gonzalez, M. F., Shiraishi, K., Hisanaga, K., Sagar, S. M., Mandabach, M., and Sharp, F. R. 1989. Heat shock proteins as markers of neural injury. Brain Res. Mol. Brain Res. 6:93-100.

    Google Scholar 

  47. 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.

    Google Scholar 

  48. McIntosh, T. K., Smith, D. H., Meaney, D. F., Kotapka, M. J., Gennarelli, T. A., and Graham, D. I. 1996. Neuropathological sequelae of traumatic brain injury: Relationship to neurochemical and biomechanical mechanisms. Lab. Invest. 74:315-342.

    Google Scholar 

  49. Holmin, S., Soderlund, J., Biberfeld, P., and Mathiesen, T. 1998. Intracerebral inflammation after human brain contusion. Neurosurgery 42:291-298.

    Google Scholar 

  50. Thomas, W. E. 1992. Brain macrophages: Evaluation of microglia and their functions. Brain Res. Brain Res. Rev. 17:61-74.

    Google Scholar 

  51. Woodroofe, M. N., Sarna, G. S., Wadhwa, M., Hayes, G. M., Loughlin, A. J., Tinker, A., and Cuzner, M. L. 1991. Detection of interleukin-1 and interleukin-6 in adult rat brain, following mechanical injury, by in vivo microdialysis: Evidence of a role for microglia in cytokine production. J. Neuroimmunol. 33:227-236.

    Google Scholar 

  52. Benveniste, E. N. 1992. Cytokines: Influence on glial cell gene expression and function. Chem. Immunol. 52:106-153.

    Google Scholar 

  53. Giulian, D., Li, J., Bartel, S., Broker, J., Li, X., and Kirkpatrick, J. B. 1995. Cell surface morphology identifies microglia as a distinct class of mononuclear phagocyte. J. Neurosci. 15:7712-7726.

    Google Scholar 

  54. Thery, C. and Mallat, M. 1993. Influence of interleukin-1 and tumor necrosis factor alpha on the growth of microglial cells in primary cultures of mouse cerebral cortex: Involvement of colony-stimulating factor 1. Neurosci Lett. 150:195-199.

    Google Scholar 

  55. Norris, J. G., Tang, L. P., Sparacio, S. M., and Benveniste, E. N. 1994. Signal transduction pathways mediating astrocyte IL-6 induction by IL-1 beta and tumor necrosis factor-alpha. J. Immunol. 152:841-850.

    Google Scholar 

  56. Young, B., Ott, L., Yingling, B., and McClain, C. 1992. Nutrition and brain injury. J. Neurotrauma. 9 (Suppl 1):S375-S383.

    Google Scholar 

  57. Ott, L., McClain, C. J., Gillespie, M., and Young, B. 1994. Cytokines and metabolic dysfunction after severe head injury. J. Neurotrauma 11:447-472.

    Google Scholar 

  58. Gourin, C. G. and Shackford, S. R. 1997. Production of tumor necrosis factor-alpha and interleukin-1beta by human cerebral microvascular endothelium after percussive trauma. J. Trauma 42:1101-1107.

    Google Scholar 

  59. Shohami, E., Novikov, M., Bass, R., Yamin, A., and Gallily, R. 1994. Closed head injury triggers early production of TNF alpha and IL-6 by brain tissue. J. Cereb. Blood Flow Metab. 14:615-619.

    Google Scholar 

  60. Taupin, V., Toulmond, S., Serrano, A., Benavides, J., and Zavala, F. 1993. Increase in IL-6, IL-1 and TNF levels in rat brain following traumatic lesion. Influence of pre-and post-traumatic treatment with Ro5 4864, a peripheral-type (p site) benzodiazepine ligand. J. Neuroimmunol. 42:177-185.

    Google Scholar 

  61. Fan, L., Young, P. R., Barone, F. C., Feuerstein, G. Z., Smith, D. H., and McIntosh, T. K. 1995. Experimental brain injury induces expression of interleukin-1 beta mRNA in the rat brain. Brain Res. Mol. Brain Res. 30:125-130.

    Google Scholar 

  62. Fan, L., Young, P. R., Barone, F. C., Feuerstein, G. Z., Smith, D. H., and McIntosh, T. K. 1996. Experimental brain injury induces differential expression of tumor necrosis factor-alpha mRNA in the CNS. Brain Res. Mol. Brain Res. 36:287-291.

    Google Scholar 

  63. Rothwell, N. J. and Relton, J. K. 1993. Involvement of cytokines in acute neurodegeneration in the CNS. Neurosci. Bio behav. Rev. 17:217-227.

    Google Scholar 

  64. Toulmond, S. and Rothwell, N. J. 1995. Interleukin-1 receptor antagonist inhibits neuronal damage caused by fluid percussion injury in the rat. Brain Res. 671:261-266.

    Google Scholar 

  65. Sanderson, K. L., Raghupathi, R., Saatman, K. E., Martin, D., Miller, G., and McIntosh, T. K. 1999. Interleukin-1 receptor antagonist attenuates regional neuronal cell death and cognitive dysfunction after experimental brain injury. J. Cereb. Blood Flow Metab. 19:1118-1125.

    Google Scholar 

  66. Scherbel, U., Raghupathi, R., Nakamura, M., Saatman, K. E., Trojanowski, J. Q., Neugebauer, E., Marino, M. W., and McIntosh, T. K. 1999. Differential acute and chronic responses of tumor necrosis factor-deficient mice to experimental brain injury. Proc. Natl. Acad. Sci. USA 96:8721-8726.

    Google Scholar 

  67. Thoenen, H. 1991. The changing scene of neurotrophic factors. Trends Neurosci. 14:165-170.

    Google Scholar 

  68. Williams, L. R., Varon, S., Peterson, G. M., Wictorin, K., Fischer, W., Bjorklund, A., and Gage, F. H. 1986. Continuous infusion of nerve growth factor prevents basal forebrain neuronal death after fimbria fornix transection. Proc. Natl. Acad. Sci. USA 83:9231-9235.

    Google Scholar 

  69. Kromer, L. F. 1987. Nerve growth factor treatment after brain injury prevents neuronal death. Science 235:214-216.

    Google Scholar 

  70. Oyesiku, N. M. and Wigston, D. J. 1996. Ciliary neurotrophic factor stimulates neurite outgrowth from spinal cord neurons. J. Comp. Neurol. 364:68-77.

    Google Scholar 

  71. Levi-Montalcini, R. 1987. The nerve growth factor 35 years later. Science 237:1154-1162.

    Google Scholar 

  72. Leibrock, J., Lottspeich, F., Hohn, A., Hofer, M., Hengerer, B., Masiakowski, P., Thoenen, H., and Barde, Y. A. 1989. Molecular cloning and expression of brain-derived neurotrophic factor. Nature 341:149-152.

    Google Scholar 

  73. Hohn, A., Leibrock, J., Bailey, K., and Barde, Y. A. 1990. Identification and characterization of a novel member of the nerve growth factor/brain-derived neurotrophic factor family. Nature 344:339-341.

    Google Scholar 

  74. Kaplan, D. R., Martin-Zanca, D., and Parada, L. F. 1991. Tyrosine phosphorylation and tyrosine kinase activity of the trk proto-oncogene product induced by NGF. Nature 350:158-160.

    Google Scholar 

  75. Klein, R., Nanduri, V., Jing, S. A., Lamballe, F., Tapley, P., Bryant, S., Cordon-Cardo, C., Jones, K. R., Reichardt, L. F., and Barbacid, M. 1991. The trkB tyrosine protein kinase is a receptor for brain-derived neurotrophic factor and neurotrophin-3. Cell 66:395-403.

    Google Scholar 

  76. Lamballe, F., Klein, R., and Barbacid, M. 1991. trkC, a new member of the trk family of tyrosine protein kinases, is a receptor for neurotrophin-3. Cell 66:967-979.

    Google Scholar 

  77. DeKosky, S. T., Goss, J. R., Miller, P. D., Styren, S. D., Kochanek, P. M., and Marion, D. 1994. Upregulation of nerve growth factor following cortical trauma. Exp. Neurol. 130:173-177.

    Google Scholar 

  78. Goss, J. R., O'Malley, M. E., Zou, L., Styren, S. D., Kochanek, P. M., and DeKosky, S. T. 1998. Astrocytes are the major source of nerve growth factor upregulation following traumatic brain injury in the rat. Exp. Neurol. 149:301-309.

    Google Scholar 

  79. Yang, K., Mu, X. S., Xue, J. J., Perez-Polo, J. R., and Hayes, R. L. 1995. Regional and temporal profiles of c-fos and nerve growth factor mRNA expression in rat brain after lateral cortical impact injury. J. Neurosci. Res. 42:571-578.

    Google Scholar 

  80. Goss, J. R., Taffe, K. M., Kochanek, P. M., and DeKosky, S. T. 1997. The antioxidant enzymes glutathione peroxidase and catalase increase following traumatic brain injury in the rat. Exp. Neurol. 146:291-294.

    Google Scholar 

  81. Longo, F. M., Selak, I., Zovickian, J., Manthorpe, M., and Varon, S. 1984. Neuronotrophic activities in cerebrospinal fluid of head trauma patients. Exp. Neurol. 84:207-218.

    Google Scholar 

  82. Patterson, S. L., Grady, M. S., and Bothwell, M. 1993. Nerve growth factor and a fibroblast growth factor-like neurotrophic activity in cerebrospinal fluid of brain injured human patients. Brain Res. 605:43-49.

    Google Scholar 

  83. Hicks, R. R., Numan, S., Dhillon, H. S., Prasad, M. R., and Seroogy, K. B. 1997. Alterations in BDNF and NT-3 mRNAs in rat hippocampus after experimental brain trauma. Brain Res. Mol. Brain Res. 48:401-406.

    Google Scholar 

  84. Oyesiku, N. M., Evans, C. O., Houston, S., Darrell, R. S., Smith, J. S., Fulop, Z. L., Dixon, C. E., and Stein, D. G. 1999. Regional changes in the expression of neurotrophic factors and their receptors following acute traumatic brain injury in the adult rat brain. Brain Res. 833:161-172.

    Google Scholar 

  85. Sinson, G., Voddi, M., and McIntosh, T. K. 1995. Nerve growth factor administration attenuates cognitive but not neurobehavioral motor dysfunction or hippocampal cell loss following fluid-percussion brain injury in rats. J. Neurochem. 65:2209-2216.

    Google Scholar 

  86. Dixon, C. E., Flinn, P., Bao, J., Venya, R., and Hayes, R. L. 1997. Nerve growth factor attenuates cholinergic deficits following traumatic brain injury in rats. Exp. Neurol. 146:479-490.

    Google Scholar 

  87. Sinson, G., Perri, B. R., Trojanowski, J. Q., Flamm, E. S., and McIntosh, T. K. 1997. Improvement of cognitive deficits and decreased cholinergic neuronal cell loss and apoptotic cell death following neurotrophin infusion after experimental traumatic brain injury. J. Neurosurg. 86:511-518.

    Google Scholar 

  88. Morrison, B., Eberwine, J. H., Meaney, D. F., and McIntosh, T. K. 2000. Traumatic injury induces differential expression of cell death genes in organotypic brain slice cultures determined by complementary DNA array hybridization. Neuroscience 96:131-139.

    Google Scholar 

  89. Matzilevich, D. A., Rall, J. M., Moore, A. N., Grill, R. J., and Dash, P. K. 2002. High-density microarray analysis of hippocampal gene expression following experimental brain injury. J. Neurosci. Res. 67:646-663.

    Google Scholar 

  90. Eisen, M. B., Spellman, P. T., Brown, P. O., and Botstein, D. 1998. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. USA 95:14863-14868.

    Google Scholar 

  91. O'Dell, D. M., Raghupathi, R., Crino, P. B., Eberwine, J. H., and McIntosh, T. K. 2000. Traumatic brain injury alters the molecular fingerprint of TUNEL-positive cortical neurons in vivo: A single-cell analysis. J. Neurosci. 20:4821-4828.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Neuroscience, University of Pennsylvania, Philadelphia, PA

    Paolo G. Marciano

  2. Department of Pharmacology, University of Pennsylvania, Philadelphia, PA

    James H. Eberwine

  3. Department of Neurosurgery, University of Pennsylvania, Philadelphia, PA

    Ramesh Ragupathi, Kathryn E. Saatman & Tracy K. McIntosh

  4. Department of Bioengineering, University of Pennsylvania, Philadelphia, PA

    David F. Meaney

  5. Veterans Administration Medical Center, Philadelphia, PA

    Tracy K. McIntosh

Authors
  1. Paolo G. Marciano
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. James H. Eberwine
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ramesh Ragupathi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kathryn E. Saatman
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. David F. Meaney
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tracy K. McIntosh
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Marciano, P.G., Eberwine, J.H., Ragupathi, R. et al. Expression Profiling Following Traumatic Brain Injury: A Review. Neurochem Res 27, 1147–1155 (2002). https://doi.org/10.1023/A:1020973308941

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1020973308941

Search

Navigation