The effect of progesterone dose on gene expression after traumatic brain injury

Journal of Neurotrauma

Volumn 28, Issue 9, 2011, Pages 1827-1843

  Anderson, Gail D ^a   Farin, Federico M ^a   Bammler, Theo K ^a   Beyer, Richard P ^a   Swan, Alicia A ^b   Wilkerson, Hui Wen ^a   Kantor, Eric D ^a   Hoane, Michael R ^b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b SOUTHERN ILLINOIS UNIVERSITY   (United States)

Author keywords

CCI injury model; gene expression; neurotrauma; progesterone

Indexed keywords

DNA; PROGESTERONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BRAIN CONTUSION; CELL PROLIFERATION; CONTROLLED STUDY; DNA DAMAGE; DRUG EFFECT; DRUG ELIMINATION; DRUG HALF LIFE; GENE EXPRESSION PROFILING; GENE ONTOLOGY; GENETIC ANALYSIS; INNATE IMMUNITY; MALE; MICROARRAY ANALYSIS; NONHUMAN; RAT; TRAUMATIC BRAIN INJURY;

ANIMALS; APOPTOSIS; BRAIN INJURIES; CEREBRAL CORTEX; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION; MALE; PROGESTERONE; PROGESTINS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 80054794856     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2011.1911     Document Type: Article

References (76)

1. Allison, D.B., Cui, X., Page, G.P., and Sabripour, M. (2006). Microarray data analysis: From disarray to consolidation and consensus. Nat. Rev. Genet. 7, 55-65.
2. Aragones, G., Ferre, R., Lazaro, I., Cabre, A., Plana, N., Merino, J., Heras, M., Girona, J., and Masana, L. (2010). Fatty acid-binding protein 4 is associated with endothelial dysfunction in patients with type 2 diabetes. Atherosclerosis 213, 329-331.
3. Bazan, N.G., Rodriguez de Turco, E.B., and Allan, G. (1995). Mediators of injury in neurotrauma: Intracellular signal transduction and gene expression. J. Neurotrauma 12, 791-814.
4. Belelli, D., Casula, A., Ling, A., and Lambert, J.J. (2002). The influence of subunit composition on the interaction of neurosteroids with GABA(A) receptors. Neuropharmacology 43, 651-661.
5. Brain, S.D., Williams, T.J., Tippins, J.R., Morris, H.R., and MacIntyre, I. (1985). Calcitonin gene-related peptide is a potent vasodilator. Nature 313, 54-56.
6. Camon, E., Magrane, M., Barrell, D., Lee, V., Dimmer, E., Maslen, J., Binns, D., Harte, N., Lopez, R., and Apweiler, R. (2004). The Gene Ontology Annotation (GOA) Database: Sharing knowledge in Uniprot with gene ontology. Nucleic Acids Res. 32, D262-266.
7. Centers for Disease Control (2011). Injury Prevention and Control: Traumatic Brain Injury. http://www.cdc.gov/traumatic braininjury/statistics/html (Last accessed August 29, 2011
8. Chesik, D., and De Keyser, J. (2010). Progesterone and dexamethasone differentially regulate the IGF-system in glial cells. Neurosci. Lett. 468, 178-182.
9. Choi, J.S., Kim, S.J., Shin, J.A., Lee, K.E., and Park, E.M. (2008). Effects of estrogen on temporal expressions of IL-1beta and IL-1ra in rat organotypic hippocampal slices exposed to oxygenglucose deprivation. Neurosci Lett. 438, 233-237.
10. Choi, S.H., Aid, S., and Bosetti, F. (2009). The distinct roles of cyclooxygenase-1 and -2 in neuroinflammation: Implications for translational research. Trends Pharmacol. Sci. 30, 174-181.
11. Cole, J.T., Yarnell, A., Kean, W.S., Gold, E., Lewis, B., Ren, M., McMullen, D.C., Jacobowitz, D.M., Pollard, H.B., O'Neill, J.T., Grunberg, N.E., Dalgard, C.L., Frank, J.A., and Watson, W.D. (2011). Craniotomy: True sham for traumatic brain injury, or a sham of a sham? J. Neurotrauma 28, 359-369.
12. Creagh, E.M., Conroy, H., and Martin, S.J. (2003). Caspase-activation pathways in apoptosis and immunity. Immunol. Rev. 193, 10-21.
13. Cui, L., Zhang, X., Yang, R., Wang, L., Liu, L., Li, M., and Du, W. (2010). Neuroprotection of early and short-time applying atorvastatin in the acute phase of cerebral ischemia: Downregulated 12/15-LOX, p38MAPK and cPLA2 expression, ameliorated BBB permeability. Brain Res. 1325, 164-173.
14. Cutler, S.M., Cekic, M., Miller, D.M., Wali, B., VanLandingham, J.W., and Stein, D.G. (2007). Progesterone improves acute recovery after traumatic brain injury in the aged rat. J. Neurotrauma 24, 1475-1486.
15. Dabney, A., and Storey, J. (2006). Bioconductor's qvalue package. Available at: Http://bioconductor.org/packages/1.8/bioc/ vignettes/qvalue/inst/ doc/qvalue.pdf (Last accessed September 2010).
16. Dash, P.K., Kobori, N., and Moore, A.N. (2004). A molecular description of brain trauma pathophysiology using microarray technology: An overview. Neurochem. Res. 29, 1275-1286.
17. Di Pietro, V., Amin, D., Pernagallo, S., Lazzarino, G., Tavazzi, B., Vagnozzi, R., Pringle, A., and Belli, A. (2010). Transcriptomics of traumatic brain injury: Gene expression and molecular pathways of different grades of insult in a rat organotypic hippocampal culture model. J. Neurotrauma 27, 349-359.
18. Djebaili, M., Hoffman, S.W., and Stein, D.G. (2004). Allopregnanolone and progesterone decrease cell death and cognitive deficits after a contusion of the rat pre-frontal cortex. Neuroscience 123, 349-359.
19. Faden, A.I., and Stoica, B. (2007). Neuroprotection: Challenges and opportunities. Arch. Neurol. 64, 794-800.
20. Fairfax, B.P., Vannberg, F.O., Radhakrishnan, J., Hakonarson, H., Keating, B.J., Hill, A.V., and Knight, J.C. (2010). An integrated expression phenotype mapping approach defines common variants in LEP, ALOX15 and CAPNS1 associated with induction of IL-6. Hum. Mol. Genet. 19, 720-730.
21. Galasko, D., and Montine, T.J. (2010). Biomarkers of oxidative damage and inflammation in Alzheimer's disease. Biomark. Med. 4, 27-36.
22. Gentleman, R., Carey, V., Bates, D., Bolstad, B., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J., Hornik, K., Hothorn, T., Huber, W., Iacus, S., Irizarry, R., Leisch, F., Li, C., Maechler, M., Rossini, A., Sawitzki, G., Smith, C., Smyth, G., Tierney, L., Yang, J., and Zhang, J. (2004). Bioconductor: Open software development for computational biology and bioinformatics,. Genome Biol. 5:R80.
23. Gentleman, R., Carey, V., Huber, W., Irizarry, R., and Dudoit, S. (2005). Iimma: Linear models for microarray data, in: Bioinformatics and Computational Biology Solutions Using R and Bioconductor, Springer Science-Business Media, Inc: New York, pps. 397-420.
24. Gibson, C.L., Gray, L.J., Bath, P.M., and Murphy, S.P. (2008). Progesterone for the treatment of experimental brain injury; a systematic review. Brain 131, 318-328.
25. Gilroy, D.W., Colville-Nash, P.R., Willis, D., Chivers, J., Paul-Clark, M.J., and Willoughby, D.A. (1999). Inducible cyclooxygenase may have anti-inflammatory properties. Nat. Med. 5, 698-701.
26. Goffus, A.M., Anderson, G.D., and Hoane, M. (2010). Sustained delivery of nicotinamide limits cortical injury and improves functional recovery following traumatic brain injury. Oxid. Med. Cell Longev. 3, 145-152.
27. Goss, C.W., Hoffman, S.W., and Stein, D.G. (2003). Behavioral effects and anatomic correlates after brain injury: A progesterone dose-response study. Pharmacol. Biochem. Behav. 76, 231-242.
28. Grossetete, M., Phelps, J., Arko, L., Yonas, H., and Rosenberg, G.A. (2009). Elevation of matrix metalloproteinases 3 and 9 in cerebrospinal fluid and blood in patients with severe traumatic brain injury. Neurosurgery 65, 702-708.
29. Halks-Miller, M, Schroeder, M.L., Haroutunian, V., Moenning, U., Rossi, M., Achim, C., Purohit, D., Mahmoudi, M., and Horuk, R. (2003). CCR1 is an early and specific marker of Alzheimer's disease. Ann. Neurol. 54, 638-646.
30. Hayashi, T., Kaneko, Y., Yu, S., Bae, E., Stahl, C.E., Kawase, T., van Loveren, H., Sanberg, P.R., and Borlongan, C.V. (2009). Quantitative analyses of matrix metalloproteinase activity after traumatic brain injury in adult rats. Brain Res. 1280, 172-177.
31. 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.
32. He, J., Evans, C.O., Hoffman, S.W., Oyesiku, N.M., and Stein, D.G. (2004). Progesterone and allopregnanolone reduce inflammatory cytokines after traumatic brain injury. Exp. Neurol. 189, 404-412.
33. Hoane, M.R., Gilbert, D.R., Holland, M.A., and Pierce, J.L. (2006). Nicotinamide reduces acute cortical neuronal death and edema in the traumatically injured brain. Neurosci. Lett. 408, 35-39.
34. Ishrat, T., Sayeed, I., Atif, F., Hua, F., and Stein, D.G. (2010). Progesterone and allopregnanolone attenuate blood-brain barrier dysfunction following permanent focal ischemia by regulating the expression of matrix metalloproteinases. Exp. Neurol. 226, 183-190.
35. Ivins, B.J. (2010). Hospitalization associated with traumatic brain injury in the active duty US Army: 2000-2006. NeuroRehabilitation 26, 199-212.
36. Jia, F., Pan, Y.H., Mao, Q., Liang, Y.M., and Jiang, J.Y. (2008). Matrix metalloproteinase-9 expression and protein levels after fluid percussion injury in rats: The effect of injury severity and brain temperature. J. Neurotrauma 27, 1059-1068.
37. Kuhn, H., and O'Donnell, V.B. (2006). Inflammation and immune regulation by 12/15-lipoxygenases. Prog. Lipid Res. 45, 334-356.
38. Langlois, J.A., Rutland-Brown, W., and Wald, M.M. (2006). The epidemiology and impact of traumatic brain injury: A brief overview. J. Head Trauma Rehabil. 21, 375-378.
39. Levy, A., Bercovich-Kinori, A., Alexandrovich, A.G., Tsenter, J., Trembovler, V., Lund, F.E., Shohami, E., Stein, R., and Mayo, L. (2009). CD38 facilitates recovery from traumatic brain injury. J. Neurotrauma 26, 1521-1533.
40. Li, J., Vause, C.V., and Durham, P.L. (2008). Calcitonin generelated peptide stimulation of nitric oxide synthesis and release from trigeminal ganglion glial cells. Brain Res. 1196, 22-32.
41. Loddick, S.A., Wong, M.L., Bongiorno, P.B., Gold, P.W., Licinio, J., and Rothwell, N.J. (1997). Endogenous interleukin-1 receptor antagonist is neuroprotective. Biochemical and biophysical research communications. 234, 211-215.
42. Majewska, M.D., Harrison, N.L., Schwartz, R.D., Barker, J.L., and Paul, S.M. (1986). Steroid hormone metabolites are barbiturate-like modulators of the GABA receptor. Science 232, 1004-1007.
43. Malavasi, F., Deaglio, S., Funaro, A., Ferrero, E., Horenstein, A.L., Ortolan, E., Vaisitti, T., and Aydin, S. (2008). Evolution and function of the ADP ribosyl cyclase/CD38 gene family in physiology and pathology. Physiol Rev. 88, 841-886.
44. Marciano, P.G., Eberwine, J.H., Ragupathi, R., Saatman, K.E., Meaney, D.F., and McIntosh, T.K. (2002). Expression profiling following traumatic brain injury: A review. Neurochem. Res. 27, 1147-1155.
45. McKallip, R.J., Do, Y., Fisher, M.T., Robertson, J.L., Nagarkatti, P.S., and Nagarkatti, M. (2002). Role of CD44 in activationinduced cell death: CD44-deficient mice exhibit enhanced T cell response to conventional and superantigens. Int. Immunol. 14, 1015-1026.
46. Narayan, R.K., Michel, M.E., Ansell, B., Baethmann, A., Biegon, A., Bracken, M.B., Bullock, M.R., Choi, S.C., Clifton, G.L., Contant, C.F., Coplin, W.M., Dietrich, W.D., Ghajar, J., Grady, S.M., Grossman, R.G., Hall, E.D., Heetderks, W., Hovda, D.A., Jallo, J., Katz, R.L., Knoller, N., Kochanek, P.M., Maas, A.I., Majde, J., Marion, D.W., Marmarou, A., Marshall, L.F., Mc-Intosh, T.K., Miller, E., Mohberg, N., Muizelaar, J.P., Pitts, L.H., Quinn, P., Riesenfeld, G., Robertson, C.S., Strauss, K.I., Teasdale, G., Temkin, N., Tuma, R., Wade, C., Walker, M.D., Weinrich, M., Whyte, J., Wilberger, J., Young, A.B., and Yurkewicz, L. (2002). Clinical trials in head injury. J. Neurotrauma 19, 503-557.
47. Natale, J.E., Ahmed, F., Cernak, I., Stoica, B., and Faden, A.I. (2003). Gene expression profile changes are commonly modulated across models and species after traumatic brain injury. J. Neurotrauma 20, 907-927.
48. Perez-Martin, M., Cifuentes, M., Grondona, J.M., Lopez-Avalos, M.D., Gomez-Pinedo, U., Garcia-Verdugo, J.M., and Fernandez-Llebrez, P. (2010). IGF-I stimulates neurogenesis in the hypothalamus of adult rats. Eur. J. Neurosci. 31, 1533-1548.
49. Quigley, A., Tan, A.A., and Hoane, M.R. (2009). The effects of hypertonic saline and nicotinamide on sensorimotor and cognitive function following cortical contusion injury in the rat. Brain Res. 1304, 138-148.
50. Raghavendra Rao, V.L., Dhodda, V.K., Song, G., Bowen, K.K., and Dempsey, R.J. (2003). Traumatic brain injury-induced acute gene expression changes in rat cerebral cortex identified by GeneChip analysis. J. Neurosci. Res. 71, 208-219.
51. Rall, J.M., Matzilevich, D.A., and Dash, P.K. (2003). Comparative analysis of mRNA levels in the frontal cortex and the hippocampus in the basal state and in response to experimental brain injury. Neuropathol. Appl. Neurobiol. 29, 118-131.
52. Roof, R.L., Duvdevani, R., and Stein, D.G. (1993). Gender influences outcome of brain injury: Progesterone plays a protective role. Brain Res. 607, 333-336.
53. Roof, R.L., Hoffman, S.W., and Stein, D.G. (1997). Progesterone protects against lipid peroxidation following traumatic brain injury in rats. Mol. Chem. Neuropathol. 31, 1-11.
54. Rubovitch, V., Edut, S., Sarfstein, R., Werner, H., and Pick, C.G. (2011). The intricate involvement of the Insulin-like growth factor receptor signaling in mild traumatic brain injury in mice. Neurobiol. Dis. 38, 299-303.
55. Sayeed, I., and Stein, D.G. (2009). Progesterone as a neuroprotective factor in traumatic and ischemic brain injury. Prog. Brain Res. 175, 219-237.
56. Schouten, J.W. (2007). Neuroprotection in traumatic brain injury: A complex struggle against the biology of nature. Curr. Opin. Crit. Care 13, 134-142.
57. Schumacher, M., Guennoun, R., Stein, D.G., and De Nicola, A.F. (2007). Progesterone: Therapeutic opportunities for neuroprotection and myelin repair. Pharmacol. Ther. 116, 77-106.
58. Smyth, G.K. (2004). Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, 1-25.
59. Sneed, T.B., Stanley, D.J., Young, L.A., and Sanderson, R.D. (1994). Interleukin-6 regulates expression of the syndecan-1 proteoglycan on B lymphoid cells. Cell Immunol. 153, 456-467.
60. Statler, K.D., Jenkins, L.W., Dixon, C.E., Clark, R.S., Marion, D.W., and Kochanek, P.M. (2001). The simple model versus the super model: Translating experimental traumatic brain injury research to the bedside. J. Neurotrauma 18, 1195-1206.
61. Stein, D.G. (2005). The case for progesterone. Ann. N. Y. Acad. Sci. 1052, 152-169.
62. Stein, D.G. (2008). Progesterone exerts neuroprotective effects after brain injury. Brain Res. Rev. 57, 386-397.
63. Stein, D.G., and Wright, D.W. (2010). Progesterone in the clinical treatment of acute traumatic brain injury. Expert Opin. Investig. Drugs. 19, 847-857.
64. Swan, A.A., Chandrashekar, R., Beare, J., and Hoane, M.R. (2011). Preclinical efficacy testing in middle-aged rats: Nicotinamide, a novel neuroprotectant, demonstrates diminished preclinical efficacy after controlled cortical impact. J. Neurotrauma 28, 431-440.
65. 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.
66. Truettner, J.S., Suzuki, T., and Dietrich, W.D. (2005). The effect of therapeutic hypothermia on the expression of inflammatory response genes following moderate traumatic brain injury in the rat. Brain Res. Mol. Brain Res. 138, 124-134.
67. Tusher, V.G., Tibshirani, R., and Chu, G. (2001). Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. U. S. A. 98, 5116-5121.
68. Van Lint, P., and Libert, C. (2006). Matrix metalloproteinase-8: Cleavage can be decisive. Cytokine Growth Factor Rev. 17, 217-223.
69. Vink, R., and Nimmo, A.J. (2009). Multifunctional drugs for head injury. Neurotherapeutics 6, 28-42.
70. Wright, D.W., Bauer, M.E., Hoffman, S.W., and Stein, D.G. (2001). Serum progesterone levels correlate with decreased cerebral edema after traumatic brain injury in male rats. J. Neurotrauma 18, 901-909.
71. Wright, D.W., Kellermann, A.L., Hertzberg, V.S., Clark, P.L., Frankel, M., Goldstein, F.C., Salomone, J.P., Dent, L.L., Harris, O.A., Ander, D.S., Lowery, D.W., Patel, M.M., Denson, D.D., Gordon, A.B., Wald, M.M., Gupta, S., Hoffman, S.W., and Stein, D.G. (2007). ProTECT: A randomized clinical trial of progesterone for acute traumatic brain injury. Ann. Emerg. Med. 49, 391-402, 402 e391-392.
72. Wright, D.W., Ritchie, J.C., Mullins, R.E., Kellermann, A.L., and Denson, D.D. (2005). Steady-state serum concentrations of progesterone following continuous intravenous infusion in patients with acute moderate to severe traumatic brain injury. J. Clin. Pharmacol. 45, 640-648.
73. Xiao, G., Wei, J., Yan, W., Wang, W., and Lu, Z. (2008). Improved outcomes from the administration of progesterone for patients with acute severe traumatic brain injury: A randomized controlled trial. Crit. Care 12:R61.
74. Yachie, A., Niida, Y., Wada, T., Igarashi, N., Kaneda, H., Toma, T., Ohta, K., Kasahara, Y., and Koizumi, S. (1999). Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J. Clin. Invest. 103, 129-135.
75. Yao, X.L., Liu, J., Lee, E., Ling, G.S., and McCabe, J.T. (2005). Progesterone differentially regulates pro-and anti-apoptotic gene expression in cerebral cortex following traumatic brain injury in rats. J. Neurotrauma 22, 656-668.
76. Yasuda, M., Nakano, K., Yasumoto, K., and Tanaka, Y. (2002). CD44: Functional relevance to inflammation and malignancy. Histol. Histopathol. 17, 945-950.