Posttraumatic hypothermia increases doublecortin expressing neurons in the dentate gyrus after traumatic brain injury in the rat

Experimental Neurology

Volumn 233, Issue 2, 2012, Pages 821-828

  Bregy, Amade ^a   Nixon, Ryan ^a   Lotocki, George ^a   Alonso, Ofelia F ^a   Atkins, Coleen M ^a   Tsoulfas, Pantelis ^a   Bramlett, Helen M ^a   Dietrich, W Dalton ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

Dentate gyrus; Doublecortin; Fluid percussion; Hypothermia; Neurogenesis; Traumatic brain injury

Indexed keywords

DEOXYURIDINE; DOUBLECORTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN PERFUSION; CELL COUNT; CELL PROLIFERATION; CONTROLLED STUDY; DENTATE GYRUS; DISEASE ACTIVITY; DISEASE ASSOCIATION; HYPOTHERMIA; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MITOSIS; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; RAT; TRAUMATIC BRAIN INJURY;

ANIMALS; BRAIN INJURIES; DENTATE GYRUS; GENE EXPRESSION REGULATION; HYPOTHERMIA, INDUCED; IMMUNOHISTOCHEMISTRY; MALE; MICROTUBULE-ASSOCIATED PROTEINS; NEUROGENESIS; NEURONS; NEUROPEPTIDES; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84856535947     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2011.12.008     Document Type: Article

References (117)

1. Arvidsson A., Collin T., Kirik D., Kokaia Z., Lindvall O. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat. Med. 2002, 8:963-970.
2. Atkins C.M., Oliva A.A., Alonso O.F., Chen S., Bramlett H.M., Hu B.R., Dietrich W.D. Hypothermia treatment potentiates ERK1/2 activation after traumatic brain injury. Eur. J. Neurosci. 2007, 26:810-819.
3. Atkins C.M., Truettner J.S., Lotocki L., Sanchez-Molano J., Kang Y., Alonso O.F., Sick T.J., Dietrich W.D., Bramlett H.M. Post-traumatic seizure susceptibility is attenuated by hypothermia therapy. Eur. J. Neurosci. 2010, 28:35-42.
4. Back S.A., Han B.H., Luo N.L., Chricton C.A., Xanthoudakis S., Tam J., Arvin K.L., Holtzman D.M. Selective vulnerability of late oligodendrocyte progenitors to hypoxia-ischemia. J. Neurosci. 2002, 22:455-463.
5. Bao Y.H., Bramlett H.M., Atkins C.M., Truettner J.S., Lotocki G., Alonso O.F., Dietrich W.D. Post-traumatic seizures exacerbate histopathological damage after fluid-percussion brain injury. J. Neurotrauma 2011, 28:35-42.
6. Barha C.K., Ishrat T., Epp J.R., Galea L.A., Stein D.G. Progesterone treatment normalizes the levels of cell proliferation and cell death in the dentate gyrus of the hippocampus after traumatic brain injury. Exp. Neurol. 2011, 231:72-81.
7. Bernard S.A., Gray T.W., Buist M.D., Jones B.M., Silvester W., Gutteridge G., Smith K. Treatment of comatose survivors of out-of-hospital cardiac arrest with induced hypothermia. N. Engl. J. Med. 2002, 346:557-563.
8. Bigler E.D., Maxwell W.L. Neuroimaging and neuropathology of TBI. NeuroRehabilitation 2011, 28:63-74.
9. Blaiss C.A., Yu T.S., Zhang G., Chen J., Dimchev G., Parada L.F., Powell C.M., Kernie S.G. Temporally specified genetic ablation of neurogenesis impairs cognitive recovery after traumatic brain injury. J. Neurosci. 2011, 31:4906-4916.
10. Bonde S., Ekdahl C.T., Lindvall O. Long-term neuronal replacement in adult rat hippocampus after status epilepticus despite chronic inflammation. Eur. J. Neurosci. 2006, 23:965-974.
11. Bramlett H.M., Dietrich W.D. Pathophysiology of cerebral ischemia and brain trauma: similarities and differences. J. Cereb. Blood Flow Metab. 2004, 24:133-150.
12. Bramlett H.M., Dietrich W.D., Green E.J., Busto R. Chronic histopathological consequences of fluid-percussion brain injury in rats: effects of post-traumatic hypothermia. Acta Neuropathol. (Berl) 1997, 93:190-199.
13. Bramlett H.M., Green E.J., Dietrich W.D. Hippocampally dependent and independent chronic spatial navigational deficits following parasagittal fluid percussion brain injury in the rat. Brain Res. 1997, 762:195-202.
14. Bratton S.L., Chestnut R.M., Ghajar J., McConnell Hammond F.F., Harris O.A., Hartl R., Manley G.T., Nemecek A., Newell D.W., Rosenthal G., Schouten J., Shutter L., et al. Guidelines for the management of severe traumatic brain injury. III. Prophylactic hypothermia. J. Neurotrauma 2007, 24(Suppl 1):S21-S25.
15. Braun H., Schafer K., Hollt V. bIII tubulin-expressing neurons reveal enhanced neurogenesis in hippocampal and cortical structures after a contusion trauma in rats. J. Neurotrauma 2002, 19:975-983.
16. Brown J.P., Couillard-Despres S., Cooper-Kuhn C.M., Winkler J., Aigner L., Kuhn H.G. Transient expression of doublecortin during adult neurogenesis. J. Comp. Neurol. 2003, 467:1-10.
17. Chatzipanteli K., Alonso O.F., Kraydieh S., Dietrich W.D. Importance of posttraumatic hypothermia and hyperthermia on the inflammatory response after fluid percussion brain injury: biochemical and immunocytochemical studies. J. Cereb. Blood Flow Metab. 2000, 20:531-542.
18. Chen X.H., Iwata A., Nonaka M., Browne K.D., Smith D.H. Neurogenesis and glial proliferation persist for at least one year in the subventricular zone following brain trauma in rats. J. Neurotrauma 2003, 20:623-631.
19. Chirumamilla S., Sun D., Bullock M.R., Colello R.J. Traumatic brain injury induced cell proliferation in the adult mammalian central nervous system. J. Neurotrauma 2002, 19:693-703.
20. Clifton G.L., Valadka A., Zygun D., Coffey C.S., Drever P., Fourwinds S., Janis L.S., Wilde E., Taylor P., Harshman K., Conley A., Puccio A., et al. Very early hypothermia induction in patients with severe brain injury (the National Acute Brain Injury Study: Hypothermia II): a randomised trial. Lancet Neurol. 2011, 10:131-139.
21. Corbett D., Hamilton M., Colbourne F. Persistent neuroprotection with prolonged postischemic hypothermia in adult rats subjected to transient middle cerebral artery occlusion. Exp. Neurol. 2000, 163:200-206.
22. Couillard-Despres S., Winner B., Schaubeck S., Aigner R., Vroemen M., Weidner N., Bogdahn U., Winkler J., Kuhn H.G., Aigner L. Doublecortin expression levels in adult brain reflect neurogenesis. Eur. J. Neurosci. 2005, 21:1-14.
23. Covolan L., Ribeiro L.T., Longo B.M., Mello L.E. Cell damage and neurogenesis in the dentate granule cell layer of adult rats after pilocarpine- or kainate-induced status epilepticus. Hippocampus 2000, 10:169-180.
24. Dash P.K., Moore A.N., Dixon C.E. Spatial memory deficits, increased phosphorylation of the transcription factor CREB, and induction of the AP-1 complex following experimental brain injury. J. Neurosci. 1995, 15:2030-2039.
25. Dash P.K., Mach S.A., Moore A.N. Enhanced neurogenesis in the rodent hippocampus following traumatic brain injury. J. Neurosci. Res. 2001, 63:313-319.
26. Deng W., Aimone J.B., Gage F.H. New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory?. Nat. Rev. Neurosci. 2010, 11:339-350.
27. Dietrich W.D., Bramlett H.M. The evidence for hypothermia as a neuroprotectant in traumatic brain injury. Neurotherapeutics 2010, 7:43-50.
28. Dietrich W.D., Busto R., Alonso O., Globus M.Y., Ginsberg M.D. Intraischemic but not postischemic brain hypothermia protects chronically following global forebrain ischemia in rats. J. Cereb. Blood Flow Metab. 1993, 13:541-549.
29. Dietrich W.D., Alonso O., Busto R., Globus M.Y., Ginsberg M.D. Post-traumatic brain hypothermia reduces histopathological damage following concussive brain injury in the rat. Acta Neuropathol. (Berl) 1994, 87:250-258.
30. Dietrich W.D., Atkins C.M., Bramlett H.M. Protection in animal models of brain and spinal cord injury with mild to moderate hypothermia. J. Neurotrauma 2009, 26:301-312.
31. Dixon C.E., Kochanek P.M., Yan H.Q., Schiding J.K., Griffith R.G., Baum E., Marion D.W., DeKosky S.T. One-year study of spatial memory performance, brain morphology, and cholinergic markers after moderate controlled cortical impact in rats. J. Neurotrauma 1999, 16:109-122.
32. Doetsch F., Garcia-Verdugo J.M., Alvarez-Buylla A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J. Neurosci. 1997, 17:5046-5061.
33. Doetsch F., Garcia-Verdugo J.M., Alvarez-Buylla A. Regeneration of a germinal layer in the adult mammalian brain. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:11619-11624.
34. Eicher D.J., Wagner C.L., Katikaneni L.P., Hulsey T.C., Bass W.T., Kaufman D.A., Horgan M.J., Languani S., Bhatia J.J., Givelichian L.M., Sankaran K., Yager J.Y. Moderate hypothermia in neonatal encephalopathy: efficacy outcomes. Pediatr. Neurol. 2005, 32:11-17.
35. Ekdahl C.T., Claasen J.H., Bonde S., Kokaia Z., Lindvall O. Inflammation is detrimental for neurogenesis in adult brain. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:13632-13637.
36. Emery D.L., Fulp C.T., Saatman K.E., Schutz C., Neugebauer E., McIntosh T.K. Newly born granule cells in the dentate gyrus rapidly extend axons into the hippocampal CA3 region following experimental brain injury. J. Neurotrauma 2005, 22:978-988.
37. Emsley J.G., Mitchell B.D., Kempermann G., Macklis J.D. Adult neurogenesis and repair of the adult CNS with neural progenitors, precursors, and stem cells. Prog. Neurobiol. 2005, 75:321-341.
38. Eriksson P.S., Perfilieva E., Bjork-Eriksson T., Alborn A.M., Nordborg C., Peterson D.A., Gage F.H. Neurogenesis in the adult human hippocampus. Nat. Med. 1998, 4:1313-1317.
39. Faul M., Xu L., Wald M.M., Coronado V.G. Traumatic brain injury in the United States: emergency department visits, hospitalizations and deaths 2010, Centers for Disease Control and Prevention, National Center for Injury Prevention and Control Atlanta, GA.
40. Felling R.J., Levison S.W. Enhanced neurogenesis following stroke. J. Neurosci. Res. 2003, 73:277-283.
41. Francis F., Koulakoff A., Boucher D., Chafey P., Schaar B., Vinet M.C., Friocourt G., McDonnell N., Reiner O., Kahn A., McConnell S.K., Berwald-Netter Y., et al. Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron 1999, 23:247-256.
42. Gage F.H., Kempermann G., Palmer T.D., Peterson D.A., Ray J. Multipotent progenitor cells in the adult dentate gyrus. J. Neurobiol. 1998, 36:249-266.
43. Gao X., Deng-Bryant Y., Cho W., Carrico K.M., Hall E.D., Chen J. Selective death of newborn neurons in hippocampal dentate gyrus following moderate experimental traumatic brain injury. J. Neurosci. Res. 2008, 86:2258-2270.
44. Gaulke L.J., Horner P.J., Fink A.J., McNamara C.L., Hicks R.R. Environmental enrichment increases progenitor cell survival in the dentate gyrus following lateral fluid percussion injury. Brain Res. Mol. Brain Res. 2005, 141:138-150.
45. Gleeson J.G., Lin P.T., Flanagan L.A., Walsh C.A. Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 1999, 23:257-271.
46. Globus M.Y., Alonso O., Dietrich W.D., Busto R., Ginsberg M.D. Glutamate release and free radical production following brain injury: effects of posttraumatic hypothermia. J. Neurochem. 1995, 65:1704-1711.
47. Goss J.R., Styren S.D., Miller P.D., Kochanek P.M., Palmer A.M., Marion D.W., DeKosky S.T. Hypothermia attenuates the normal increase in interleukin 1 beta RNA and nerve growth factor following traumatic brain injury in the rat. J. Neurotrauma 1995, 12:159-167.
48. Gould E., Reeves A.J., Graziano M.S., Gross C.G. Neurogenesis in the neocortex of adult primates. Science 1999, 286:548-552.
49. Gratzner H.G. Monoclonal antibody to 5-bromo- and 5-iododeoxyuridine: a new reagent for detection of DNA replication. Science 1982, 218:474-475.
50. Hallbergson A.F., Gnatenco C., Peterson D.A. Neurogenesis and brain injury: managing a renewable resource for repair. J. Clin. Invest. 2003, 112:1128-1133.
51. Holzer M., Bernard S.A., Hachimi-Idrissi S., Roine R.O., Sterz F., Mullner M. Hypothermia for neuroprotection after cardiac arrest: systematic review and individual patient data meta-analysis. Crit. Care Med. 2005, 33:414-418.
52. Jessberger S., Zhao C., Toni N., Clemenson G.D., Li Y., Gage F.H. Seizure-associated, aberrant neurogenesis in adult rats characterized with retrovirus-mediated cell labeling. J. Neurosci. 2007, 27:9400-9407.
53. Jiang J.Y., Xu W., Li W.P., Gao G.Y., Bao Y.H., Liang Y.M., Luo Q.Z. Effect of long-term mild hypothermia or short-term mild hypothermia on outcome of patients with severe traumatic brain injury. J. Cereb. Blood Flow Metab. 2006, 26:771-776.
54. Jin K., Minami M., Lan J.Q., Mao X.O., Batteur S., Simon R.P., Greenberg D.A. Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:4710-4715.
55. Johansson C.B., Momma S., Clarke D.L., Risling M., Lendahl U., Frisen J. Identification of a neural stem cell in the adult mammalian central nervous system. Cell 1999, 96:25-34.
56. Kalluri H.S., Vemuganti R., Dempsey R.J. Mechanism of insulin-like growth factor I-mediated proliferation of adult neural progenitor cells: role of Akt. Eur. J. Neurosci. 2007, 25:1041-1048.
57. Kee N.J., Preston E., Wojtowicz J.M. Enhanced neurogenesis after transient global ischemia in the dentate gyrus of the rat. Exp. Brain Res. 2001, 136:313-320.
58. Kempermann G., Kuhn H.G., Gage F.H. More hippocampal neurons in adult mice living in an enriched environment. Nature 1997, 386:493-495.
59. Kempermann G., Jessberger S., Steiner B., Kronenberg G. Milestones of neuronal development in the adult hippocampus. Trends Neurosci. 2004, 27:447-452.
60. Kernie S.G., Erwin T.M., Parada L.F. Brain remodeling due to neuronal and astrocytic proliferation after controlled cortical injury in mice. J. Neurosci. Res. 2001, 66:317-326.
61. Kinoshita K., Chatzipanteli K., Vitarbo E., Truettner J.S., Alonso O.F., Dietrich W.D. Interleukin-1b messenger ribonucleic acid and protein levels after fluid-percussion brain injury in rats: importance of injury severity and brain temperature. Neurosurgery 2002, 51:195-203.
62. Kirschenbaum B., Goldman S.A. Brain-derived neurotrophic factor promotes the survival of neurons arising from the adult rat forebrain subependymal zone. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:210-214.
63. Kitamura T., Saitoh Y., Takashima N., Murayama A., Niibori Y., Ageta H., Sekiguchi M., Sugiyama H., Inokuchi K. Adult neurogenesis modulates the hippocampus-dependent period of associative fear memory. Cell 2009, 139:814-827.
64. Koch J.D., Miles D.K., Gilley J.A., Yang C.P., Kernie S.G. Brief exposure to hyperoxia depletes the glial progenitor pool and impairs functional recovery after hypoxic-ischemic brain injury. J. Cereb. Blood Flow Metab. 2008, 28:1294-1306.
65. Komitova M., Mattsson B., Johansson B.B., Eriksson P.S. Enriched environment increases neural stem/progenitor cell proliferation and neurogenesis in the subventricular zone of stroke-lesioned adult rats. Stroke 2005, 36:1278-1282.
66. Lasarzik I., Winkelheide U., Thal S.C., Benz N., Lorscher M., Jahn-Eimermacher A., Werner C., Engelhard K. Mild hypothermia has no long-term impact on postischemic neurogenesis in rats. Anesth. Analg. 2009, 109:1632-1639.
67. Lau B.W., Yau S.Y., Lee T.M., Ching Y.P., Tang S.W., So K.F. Intracerebroventricular infusion of cytosine-arabinoside causes prepulse inhibition disruption. Neuroreport 2009, 20:371-377.
68. Lee J., Duan W., Long J.M., Ingram D.K., Mattson M.P. Dietary restriction increases the number of newly generated neural cells, and induces BDNF expression, in the dentate gyrus of rats. J. Mol. Neurosci. 2000, 15:99-108.
69. Leventhal C., Rafii S., Rafii D., Shahar A., Goldman S.A. Endothelial trophic support of neuronal production and recruitment from the adult mammalian subependyma. Mol. Cell. Neurosci. 1999, 13:450-464.
70. Liu J., Solway K., Messing R.O., Sharp F.R. Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils. J. Neurosci. 1998, 18:7768-7778.
71. Liu Y.P., Lin H.I., Tzeng S.F. Tumor necrosis factor-alpha and interleukin-18 modulate neuronal cell fate in embryonic neural progenitor culture. Brain Res. 2005, 1054:152-158.
72. Lotocki G., de Rivero Vaccari J.P., Perez E.R., Alonso O.F., Curbelo K., Keane R.W., Dietrich W.D. Therapeutic hypothermia modulates TNFR1 signaling in the traumatized brain via early transient activation of the JNK pathway and suppression of XIAP cleavage. Eur. J. Neurosci. 2006, 24:2283-2290.
73. Lotocki G., Vaccari Jde R., Alonso O., Molano J.S., Nixon R., Safavi P., Dietrich W.D., Bramlett H.M. Oligodendrocyte vulnerability following traumatic brain injury in rats. Neurosci. Lett. 2011, 499:143-148.
74. Lotocki G., de Rivero Vaccari J.P., Perez E., Sanchez J., Alonso O., Bramlett H.M., Dietrich W.D. Alterations in blood-brain barrier permeability to large and small molecules and leukocyte accumulation after traumatic brain injury: effects of posttraumatic hypothermia. J. Neurotrauma 2009, 26:1123-1134.
75. Lu K.T., Sun C.L., Wo P.Y., Yen H.H., Tang T.H., Ng M.C., Huang M.L., Yang Y.L. Hippocampal neurogenesis after traumatic brain injury is mediated by vascular endothelial growth factor receptor-2 and the Raf/MEK/ERK cascade. J. Neurotrauma 2011, 28:441-450.
76. Maas A.I., Stocchetti N., Bullock R. Moderate and severe traumatic brain injury in adults. Lancet Neurol. 2008, 7:728-741.
77. Maas A.I., Roozenbeek B., Manley G.T. Clinical trials in traumatic brain injury: past experience and current developments. Neurotherapeutics 2010, 7:115-126.
78. Marion D., Bullock M.R. Current and future role of therapeutic hypothermia. J. Neurotrauma 2009, 26:455-467.
79. Martin E.M., Lu W.C., Helmick K., French L., Warden D.L. Traumatic brain injuries sustained in the Afghanistan and Iraq wars. Am. J. Nurs. 2008, 108:40-47.
80. Miller M.W., Nowakowski R.S. Use of bromodeoxyuridine-immunohistochemistry to examine the proliferation, migration and time of origin of cells in the central nervous system. Brain Res. 1988, 457:44-52.
81. Moreno-Lopez B., Romero-Grimaldi C., Noval J.A., Murillo-Carretero M., Matarredona E.R., Estrada C. Nitric oxide is a physiological inhibitor of neurogenesis in the adult mouse subventricular zone and olfactory bulb. J. Neurosci. 2004, 24:85-95.
82. Noonan M.A., Bulin S.E., Fuller D.C., Eisch A.J. Reduction of adult hippocampal neurogenesis confers vulnerability in an animal model of cocaine addiction. J. Neurosci. 2010, 30:304-315.
83. Packer M.A., Stasiv Y., Benraiss A., Chmielnicki E., Grinberg A., Westphal H., Goldman S.A., Enikolopov G. Nitric oxide negatively regulates mammalian adult neurogenesis. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:9566-9571.
84. Parent J.M., Yu T.W., Leibowitz R.T., Geschwind D.H., Sloviter R.S., Lowenstein D.H. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J. Neurosci. 1997, 17:3727-3738.
85. Passineau M.J., Green E.J., Dietrich W.D. Therapeutic effects of environmental enrichment on cognitive function and tissue integrity following severe traumatic brain injury in rats. Exp. Neurol. 2001, 168:373-384.
86. Pedersen M.O., Larsen A., Pedersen D.S., Stoltenberg M., Penkova M. Metallic gold treatment reduces proliferation of inflammatory cells, increases expression of VEGF and FGF, and stimulates cell proliferation in the subventricular zone following experimental traumatic brain injury. Histol. Histopathol. 2009, 24:573-586.
87. Peng H., Whitney N., Wu Y., Tian C., Dou H., Zhou Y., Zheng J. HIV-1-infected and/or immune-activated macrophage-secreted TNF-alpha affects human fetal cortical neural progenitor cell proliferation and differentiation. Glia 2008, 56:903-916.
88. Picard-Riera N., Nait-Oumesmar B., Baron-Van Evercooren A. Endogenous adult neural stem cells: limits and potential to repair the injured central nervous system. J. Neurosci. Res. 2004, 76:223-231.
89. Pieper A.A., Xie S., Capota E., Estill S.J., Zhong J., Long J.M., Becker G.L., Huntington P., Goldman S.E., Shen C.H., Capota M., Britt J.K., et al. Discovery of a proneurogenic, neuroprotective chemical. Cell 2011, 142:39-51.
90. Pierce J.E., Smith D.H., Trojanowski J.Q., McIntosh T.K. Enduring cognitive, neurobehavioral and histopathological changes persist for up to one year following severe experimental brain injury in rats. Neuroscience 1998, 87:359-369.
91. Polderman K.H. Induced hypothermia and fever control for prevention and treatment of neurological injuries. Lancet 2008, 371:1955-1969.
92. Potts M.B., Rola R., Claus C.P., Ferriero D.M., Fike J.R., Noble-Haeusslein L.J. Glutathione peroxidase overexpression does not rescue impaired neurogenesis in the injured immature brain. J. Neurosci. Res. 2009, 87:1848-1857.
93. Qiu W., Zhang Y., Sheng H., Zhang J., Wang W., Liu W., Chen K., Zhou J., Xu Z. Effects of therapeutic mild hypothermia on patients with severe traumatic brain injury after craniotomy. J. Crit. Care 2007, 22:229-235.
94. Raghupathi R., McIntosh T.K. Pharmacotherapy for traumatic brain injury: a review. Proc. West. Pharmacol. Soc. 1998, 41:241-246.
95. Ramaswamy S., Goings G.E., Soderstrom K.E., Szele F.G., Kozlowski D.A. Cellular proliferation and migration following a controlled cortical impact in the mouse. Brain Res. 2005, 1053:38-53.
96. Rao M.S., Shetty A.K. Efficacy of doublecortin as a marker to analyse the absolute number and dendritic growth of newly generated neurons in the adult dentate gyrus. Eur. J. Neurosci. 2004, 19:234-246.
97. Richardson R.M., Sun D., Bullock M.R. Neurogenesis after traumatic brain injury. Neurosurg. Clin. N. Am. 2007, 18:169-181. xi.
98. Rola R., Mizumatsu S., Otsuka S., Morhardt D.R., Noble-Haeusslein L.J., Fishman K., Potts M.B., Fike J.R. Alterations in hippocampal neurogenesis following traumatic brain injury in mice. Exp. Neurol. 2006, 202:189-199.
99. Rossi C., Angelucci A., Costantin L., Braschi C., Mazzantini M., Babbini F., Fabbri M.E., Tessarollo L., Maffei L., Berardi N., Caleo M. Brain-derived neurotrophic factor (BDNF) is required for the enhancement of hippocampal neurogenesis following environmental enrichment. Eur. J. Neurosci. 2006, 24:1850-1856.
100. Russo-Neustadt A.A., Alejandre H., Garcia C., Ivy A.S., Chen M.J. Hippocampal brain-derived neurotrophic factor expression following treatment with reboxetine, citalopram, and physical exercise. Neuropsychopharmacology 2004, 29:2189-2199.
101. Scharfman H., Goodman J., Macleod A., Phani S., Antonelli C., Croll S. Increased neurogenesis and the ectopic granule cells after intrahippocampal BDNF infusion in adult rats. Exp. Neurol. 2005, 192:348-356.
102. Scott B.W., Wojtowicz J.M., Burnham W.M. Neurogenesis in the dentate gyrus of the rat following electroconvulsive shock seizures. Exp. Neurol. 2000, 165:231-236.
103. Shankaran S., Laptook A.R., Ehrenkranz R.A., Tyson J.E., McDonald S.A., Donovan E.F., Fanaroff A.A., Poole W.K., Wright L.L., Higgins R.D., Finer N.N., Carlo W.A., et al. Whole-body hypothermia for neonates with hypoxic-ischemic encephalopathy. N. Engl. J. Med. 2005, 353:1574-1584.
104. Silasi G., Colbourne F. Therapeutic hypothermia influences cell genesis and survival in the rat hippocampus following global ischemia. J. Cereb. Blood Flow Metab. 2011, 31:1725-1735.
105. Smith D.H., Okiyama K., Thomas M.J., Claussen B., McIntosh T.K. Evaluation of memory dysfunction following experimental brain injury using the Morris water maze. J. Neurotrauma 1991, 8:259-269.
106. Smith D.H., Chen X.H., Pierce J.E., Wolf J.A., Trojanowski J.Q., Graham D.I., McIntosh T.K. Progressive atrophy and neuron death for one year following brain trauma in the rat. J. Neurotrauma 1997, 14:715-727.
107. Suh H., Deng W., Gage F.H. Signaling in adult neurogenesis. Annu. Rev. Cell Dev. Biol. 2009, 25:253-275.
108. Sun D., Colello R.J., Daugherty W.P., Kwon T.H., McGinn M.J., Harvey H.B., Bullock M.R. Cell proliferation and neuronal differentiation in the dentate gyrus in juvenile and adult rats following traumatic brain injury. J. Neurotrauma 2005, 22:95-105.
109. Takasawa K., Kitagawa K., Yagita Y., Sasaki T., Tanaka S., Matsushita K., Ohstuki T., Miyata T., Okano H., Hori M., Matsumoto M. Increased proliferation of neural progenitor cells but reduced survival of newborn cells in the contralateral hippocampus after focal cerebral ischemia in rats. J. Cereb. Blood Flow Metab. 2002, 22:299-307.
110. Urrea C., Castellanos D.A., Sagen J., Tsoulfas P., Bramlett H.M., Dietrich W.D. Widespread cellular proliferation and focal neurogenesis after traumatic brain injury in the rat. Restor. Neurol. Neurosci. 2007, 25:65-76.
111. Vallieres L., Campbell I.L., Gage F.H., Sawchenko P.E. Reduced hippocampal neurogenesis in adult transgenic mice with chronic astrocytic production of interleukin-6. J. Neurosci. 2002, 22:486-492.
112. Verwer R.W., Sluiter A.A., Balesar R.A., Baayen J.C., Noske D.P., Dirven C.M., Wouda J., van Dam A.M., Lucassen P.J., Swaab D.F. Mature astrocytes in the adult human neocortex express the early neuronal marker doublecortin. Brain 2007, 130:3321-3335.
113. Vespa P.M., McArthur D.L., Xu Y., Eliseo M., Etchepare M., Dinov I., Alger J., Glenn T.P., Hovda D. Nonconvulsive seizures after traumatic brain injury are associated with hippocampal atrophy. Neurology 2010, 75:792-798.
114. Vitarbo E.A., Chatzipanteli K., Kinoshita K., Truettner J.S., Alonso O.F., Dietrich W.D. Tumor necrosis factor a expression and protein levels after fluid percussion injury in rats: the effect of injury severity and brain temperature. Neurosurgery 2004, 55:416-424.
115. Whalen M.J., Carlos T.M., Clark R.S., Marion D.W., DeKosky S.T., Heineman S., Schiding J.K., Memarzadeh F., Kochanek P.M. The effect of brain temperature on acute inflammation after traumatic brain injury in rats. J. Neurotrauma 1997, 14:561-572.
116. Whitney N.P., Eidem T.M., Peng H., Huang Y., Zheng J.C. Inflammation mediates varying effects in neurogenesis: relevance to the pathogenesis of brain injury and neurodegenerative disorders. J. Neurochem. 2009, 108:1343-1359.
117. Yu T.S., Zhang G., Liebl D.J., Kernie S.G. Traumatic brain injury-induced hippocampal neurogenesis requires activation of early nestin-expressing progenitors. J. Neurosci. 2008, 28:12901-12912.