Hippocampal dysfunctions caused by cranial irradiation: A review of the experimental evidence

Brain, Behavior, and Immunity

Volumn 45, Issue , 2015, Pages 287-296

  Son, Yeonghoon ^a   Yang, Miyoung ^b   Wang, Hongbing ^b   Moon, Changjong ^a  

^a Chonnam National University   (South Korea)

^b MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Cranial radiation; Hippocampal dysfunction; Neurogenesis; Neuroinflammation; Neurotrophin

Indexed keywords

2 ETHYL 5,7 DIMETHYL 3 [4 [2 (2H TETRAZOL 5 YL)PHENYL]BENZYL]IMIDAZO[4,5 B]PYRIDINE; BAICALEIN; BRAIN DERIVED NEUROTROPHIC FACTOR; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; INDOMETACIN; LITHIUM; NEUROTROPHIN; [4 [2 (3 FLUORO 4 TRIFLUOROMETHYLPHENYL) 4 METHYL 5 THIAZOLYLMETHYLTHIO] 2 METHYLPHENOXY]ACETIC ACID;

ASTROCYTE; BRAIN DYSFUNCTION; HIPPOCAMPAL DYSFUNCTION; HUMAN; IONIZING RADIATION; MICROGLIA; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; REVIEW; RUNNING; SKULL IRRADIATION; STEM CELL; ADVERSE EFFECTS; ANIMAL; ANIMAL BEHAVIOR; BRAIN NEOPLASMS; COGNITION; COGNITION DISORDERS; DEPRESSION; HIPPOCAMPUS; INJURIES; MAZE TEST; MEMORY; MEMORY DISORDERS; PATHOPHYSIOLOGY; PSYCHOLOGY; RADIATION INJURIES; RADIATION RESPONSE;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN NEOPLASMS; COGNITION; COGNITION DISORDERS; CRANIAL IRRADIATION; DEPRESSION; HIPPOCAMPUS; HUMANS; MAZE LEARNING; MEMORY; MEMORY DISORDERS; NEUROGENESIS; RADIATION INJURIES;

EID: 84924026049     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2015.01.007     Document Type: Review

References (121)

1. Acharya M.M., Christie L.A., Lan M.L., Giedzinski E., Fike J.R., Rosi S., Limoli C.L. Human neural stem cell transplantation ameliorates radiation-induced cognitive dysfunction. Cancer Res. 2011, 71:4834-4845.
2. Airaksinen M.S., Saarma M. The GDNF family: signalling, biological functions and therapeutic value. Nat. Rev. Neurosci. 2002, 3:383-394.
3. Altman J., Das G.D. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J. Comp. Neurol. 1965, 124:319-335.
4. Andre C., Dinel A.L., Ferreira G., Laye S., Castanon N. Diet-induced obesity progressively alters cognition, anxiety-like behavior and lipopolysaccharide-induced depressive-like behavior: focus on brain indoleamine 2,3-dioxygenase activation. Brain Behav. Immun. 2014, 41:10-21.
5. Barde Y.A. Neurotrophins: a family of proteins supporting the survival of neurons. Prog. Clin. Biol. Res. 1994, 390:45-56.
6. Batchelor P.E., Liberatore G.T., Wong J.Y., Porritt M.J., Frerichs F., Donnan G.A., Howells D.W. Activated macrophages and microglia induce dopaminergic sprouting in the injured striatum and express brain-derived neurotrophic factor and glial cell line-derived neurotrophic factor. J. Neurosci. 1999, 19:1708-1716.
7. Beck K.D., Valverde J., Alexi T., Poulsen K., Moffat B., Vandlen R.A., Rosenthal A., Hefti F. Mesencephalic dopaminergic neurons protected by GDNF from axotomy-induced degeneration in the adult brain. Nature 1995, 373:339-341.
8. Ben Abdallah N.M., Slomianka L., Lipp H.P. Reversible effect of X-irradiation on proliferation, neurogenesis, and cell death in the dentate gyrus of adult mice. Hippocampus 2007, 17:1230-1240.
9. Bjorklund A., Rosenblad C., Winkler C., Kirik D. Studies on neuroprotective and regenerative effects of GDNF in a partial lesion model of Parkinson's disease. Neurobiol. Dis. 1997, 4:186-200.
10. Bramham C.R., Messaoudi E. BDNF function in adult synaptic plasticity: the synaptic consolidation hypothesis. Prog. Neurobiol. 2005, 76:99-125.
11. Bremner J.D., Narayan M., Anderson E.R., Staib L.H., Miller H.L., Charney D.S. Hippocampal volume reduction in major depression. Am. J. Psychiatry 2000, 157:115-118.
12. Case M., Soltesz I. Discreet charm of the GABAergic bourgeoisie: superconnected cells conduct developmental symphonies. Neuron 2009, 64:780-782.
13. Chakraborti A., Allen A., Allen B., Rosi S., Fike J.R. Cranial irradiation alters dendritic spine density and morphology in the hippocampus. PLoS One 2012, 7:e40844.
14. Chang E.L., Wefel J.S., Hess K.R., Allen P.K., Lang F.F., Kornguth D.G., Arbuckle R.B., Swint J.M., Shiu A.S., Maor M.H., Meyers C.A. Neurocognition in patients with brain metastases treated with radiosurgery or radiosurgery plus whole-brain irradiation: a randomised controlled trial. Lancet Oncol. 2009, 10:1037-1044.
15. Chen P.S., Peng G.S., Li G., Yang S., Wu X., Wang C.C., Wilson B., Lu R.B., Gean P.W., Chuang D.M., Hong J.S. Valproate protects dopaminergic neurons in midbrain neuron/glia cultures by stimulating the release of neurotrophic factors from astrocytes. Mol. Psychiatry 2006, 11:1116-1125.
16. Chiang C.S., McBride W.H., Withers H.R. Radiation-induced astrocytic and microglial responses in mouse brain. Radiother. Oncol. 1993, 29:60-68.
17. Chiew K.S., Braver T.S. Positive affect versus reward: emotional and motivational influences on cognitive control. Front. Psychol. 2011, 2:279.
18. Conner K.R., Payne V.S., Forbes M.E., Robbins M.E., Riddle D.R. Effects of the AT1 receptor antagonist L-158,809 on microglia and neurogenesis after fractionated whole-brain irradiation. Radiat. Res. 2010, 173:49-61.
19. Crocker L.D., Heller W., Warren S.L., O'Hare A.J., Infantolino Z.P., Miller G.A. Relationships among cognition, emotion, and motivation: implications for intervention and neuroplasticity in psychopathology. Front. Hum. Neurosci. 2013, 7:261.
20. Crossen J.R., Garwood D., Glatstein E., Neuwelt E.A. Neurobehavioral sequelae of cranial irradiation in adults: a review of radiation-induced encephalopathy. J. Clin. Oncol. 1994, 12:627-642.
21. David D.J., Samuels B.A., Rainer Q., Wang J.W., Marsteller D., Mendez I., Drew M., Craig D.A., Guiard B.P., Guilloux J.P., Artymyshyn R.P., Gardier A.M., Gerald C., Antonijevic I.A., Leonardo E.D., Hen R. Neurogenesis-dependent and -independent effects of fluoxetine in an animal model of anxiety/depression. Neuron 2009, 62:479-493.
22. Dietrich J., Monje M., Wefel J., Meyers C. Clinical patterns and biological correlates of cognitive dysfunction associated with cancer therapy. Oncologist 2008, 13:1285-1295.
23. Dimberg Y., Vazquez M., Soderstrom S., Ebendal T. Effects of X-irradiation on nerve growth factor in the developing mouse brain. Toxicol. Lett. 1997, 90:35-43.
24. Dulcich M.S., Hartman R.E. Pomegranate supplementation improves affective and motor behavior in mice after radiation exposure. Evid. Based Complement. Alternat. Med. 2013, 2013:940830.
25. Eichenbaum H., Dudchenko P., Wood E., Shapiro M., Tanila H. The hippocampus, memory, and place cells: is it spatial memory or a memory space?. Neuron 1999, 23:209-226.
26. Ewend M.G., Elbabaa S., Carey L.A. Current treatment paradigms for the management of patients with brain metastases. Neurosurgery 2005, 57:S66-S77. (discussion S61-64).
27. Fan Y., Liu Z., Weinstein P.R., Fike J.R., Liu J. Environmental enrichment enhances neurogenesis and improves functional outcome after cranial irradiation. Eur. J. Neurosci. 2007, 25:38-46.
28. Gill S.S., Patel N.K., Hotton G.R., O'Sullivan K., McCarter R., Bunnage M., Brooks D.J., Svendsen C.N., Heywood P. Direct brain infusion of glial cell line-derived neurotrophic factor in Parkinson disease. Nat. Med. 2003, 9:589-595.
29. Greene-Schloesser D., Robbins M.E., Peiffer A.M., Shaw E.G., Wheeler K.T., Chan M.D. Radiation-induced brain injury: a review. Front. Oncol. 2012, 2:73.
30. Guillemin G.J., Brew B.J., Noonan C.E., Takikawa O., Cullen K.M. Indoleamine 2,3 dioxygenase and quinolinic acid immunoreactivity in Alzheimer's disease hippocampus. Neuropathol. Appl. Neurobiol. 2005, 31:395-404.
31. Guzowski J.F., McNaughton B.L., Barnes C.A., Worley P.F. Imaging neural activity with temporal and cellular resolution using FISH. Curr. Opin. Neurobiol. 2001, 11:579-584.
32. Hensley K., Mhatre M., Mou S., Pye Q.N., Stewart C., West M., Williamson K.S. On the relation of oxidative stress to neuroinflammation: lessons learned from the G93A-SOD1 mouse model of amyotrophic lateral sclerosis. Antioxid. Redox Signal. 2006, 8:2075-2087.
33. Heyser C.J., Masliah E., Samimi A., Campbell I.L., Gold L.H. Progressive decline in avoidance learning paralleled by inflammatory neurodegeneration in transgenic mice expressing interleukin 6 in the brain. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:1500-1505.
34. Hodges H., Katzung N., Sowinski P., Hopewell J.W., Wilkinson J.H., Bywaters T., Rezvani M. Late behavioural and neuropathological effects of local brain irradiation in the rat. Behav. Brain Res. 1998, 91:99-114.
35. Hong J.H., Chiang C.S., Campbell I.L., Sun J.R., Withers H.R., McBride W.H. Induction of acute phase gene expression by brain irradiation. Int. J. Radiat. Oncol. Biol. Phys. 1995, 33:619-626.
36. Hua K., Schindler M.K., McQuail J.A., Forbes M.E., Riddle D.R. Regionally distinct responses of microglia and glial progenitor cells to whole brain irradiation in adult and aging rats. PLoS One 2012, 7:e52728.
37. Hwang S.Y., Jung J.S., Kim T.H., Lim S.J., Oh E.S., Kim J.Y., Ji K.A., Joe E.H., Cho K.H., Han I.O. Ionizing radiation induces astrocyte gliosis through microglia activation. Neurobiol. Dis. 2006, 21:457-467.
38. Janzer R.C., Raff M.C. Astrocytes induce blood-brain barrier properties in endothelial cells. Nature 1987, 325:253-257.
39. Jenrow K.A., Brown S.L., Lapanowski K., Naei H., Kolozsvary A., Kim J.H. Selective inhibition of microglia-mediated neuroinflammation mitigates radiation-induced cognitive impairment. Radiat. Res. 2013, 179:549-556.
40. Jenrow K.A., Brown S.L., Liu J., Kolozsvary A., Lapanowski K., Kim J.H. Ramipril mitigates radiation-induced impairment of neurogenesis in the rat dentate gyrus. Radiat. Oncol. 2010, 5:6.
41. Ji J.F., Ji S.J., Sun R., Li K., Zhang Y., Zhang L.Y., Tian Y. Forced running exercise attenuates hippocampal neurogenesis impairment and the neurocognitive deficits induced by whole-brain irradiation via the BDNF-mediated pathway. Biochem. Biophys. Res. Commun. 2014, 443:646-651.
42. Johannesen T.B., Lien H.H., Hole K.H., Lote K. Radiological and clinical assessment of long-term brain tumour survivors after radiotherapy. Radiother. Oncol. 2003, 69:169-176.
43. Kalm M., Lannering B., Bjork-Eriksson T., Blomgren K. Irradiation-induced loss of microglia in the young brain. J. Neuroimmunol. 2009, 206:70-75.
44. Kanoski S.E., Meisel R.L., Mullins A.J., Davidson T.L. The effects of energy-rich diets on discrimination reversal learning and on BDNF in the hippocampus and prefrontal cortex of the rat. Behav. Brain Res. 2007, 182:57-66.
45. Kataoka T. Study of antioxidative effects and anti-inflammatory effects in mice due to low-dose X-irradiation or radon inhalation. J. Radiat. Res. 2013, 54:587-596.
46. Klein M., Heimans J.J., Aaronson N.K., van der Ploeg H.M., Grit J., Muller M., Postma T.J., Mooij J.J., Boerman R.H., Beute G.N., Ossenkoppele G.J., van Imhoff G.W., Dekker A.W., Jolles J., Slotman B.J., Struikmans H., Taphoorn M.J. Effect of radiotherapy and other treatment-related factors on mid-term to long-term cognitive sequelae in low-grade gliomas: a comparative study. Lancet 2002, 360:1361-1368.
47. Kocher M., Wittig A., Piroth M.D., Treuer H., Seegenschmiedt H., Ruge M., Grosu A.L., Guckenberger M. Stereotactic radiosurgery for treatment of brain metastases. A report of the DEGRO Working Group on Stereotactic Radiotherapy. Strahlenther. Onkol. 2014, 190:521-532.
48. Kyrkanides S., Moore A.H., Olschowka J.A., Daeschner J.C., Williams J.P., Hansen J.T., Kerry O'Banion M. Cyclooxygenase-2 modulates brain inflammation-related gene expression in central nervous system radiation injury. Brain Res. Mol. Brain Res. 2002, 104:159-169.
49. Laack N.N., Brown P.D. Cognitive sequelae of brain radiation in adults. Semin. Oncol. 2004, 31:702-713.
50. Lagace D.C., Whitman M.C., Noonan M.A., Ables J.L., DeCarolis N.A., Arguello A.A., Donovan M.H., Fischer S.J., Farnbauch L.A., Beech R.D., DiLeone R.J., Greer C.A., Mandyam C.D., Eisch A.J. Dynamic contribution of nestin-expressing stem cells to adult neurogenesis. J. Neurosci. 2007, 27:12623-12629.
51. Lamproglou I., Chen Q.M., Boisserie G., Mazeron J.J., Poisson M., Baillet F., Le Poncin M., Delattre J.Y. Radiation-induced cognitive dysfunction: an experimental model in the old rat. Int. J. Radiat. Oncol. Biol. Phys. 1995, 31:65-70.
52. Lee E., Son H. Adult hippocampal neurogenesis and related neurotrophic factors. BMB Rep. 2009, 42:239-244.
53. Lee W.H., Sonntag W.E., Lee Y.W. Aging attenuates radiation-induced expression of pro-inflammatory mediators in rat brain. Neurosci. Lett. 2010, 476:89-93.
54. Lipsky R.H., Marini A.M. Brain-derived neurotrophic factor in neuronal survival and behavior-related plasticity. Ann. N. Y. Acad. Sci. 2007, 1122:130-143.
55. Liu J.L., Tian D.S., Li Z.W., Qu W.S., Zhan Y., Xie M.J., Yu Z.Y., Wang W., Wu G. Tamoxifen alleviates irradiation-induced brain injury by attenuating microglial inflammatory response in vitro and in vivo. Brain Res. 2010, 1316:101-111.
56. Liu Q., Zhu H.Y., Li B., Wang Y.Q., Yu J., Wu G.C. Chronic clomipramine treatment restores hippocampal expression of glial cell line-derived neurotrophic factor in a rat model of depression. J. Affect. Disord. 2012, 141:367-372.
57. Malaterre J., McPherson C.S., Denoyer D., Lai E., Hagekyriakou J., Lightowler S., Shudo K., Ernst M., Ashley D.M., Short J.L., Wheeler G., Ramsay R.G. Enhanced lithium-induced brain recovery following cranial irradiation is not impeded by inflammation. Stem Cells Transl. Med. 2012, 1:469-479.
58. Masi G., Brovedani P. The hippocampus, neurotrophic factors and depression: possible implications for the pharmacotherapy of depression. CNS Drugs 2011, 25:913-931.
59. Massie M.J. Prevalence of depression in patients with cancer. J. Natl. Cancer Inst. Monogr. 2004, 57-71.
60. McAllister A.K. Neurotrophins and neuronal differentiation in the central nervous system. Cell. Mol. Life Sci. 2001, 58:1054-1060.
61. McTyre E., Scott J., Chinnaiyan P. Whole brain radiotherapy for brain metastasis. Surg. Neurol. Int. 2013, 4:S236-244.
62. Meshi D., Drew M.R., Saxe M., Ansorge M.S., David D., Santarelli L., Malapani C., Moore H., Hen R. Hippocampal neurogenesis is not required for behavioral effects of environmental enrichment. Nat. Neurosci. 2006, 9:729-731.
63. Messaoudi E., Ying S.W., Kanhema T., Croll S.D., Bramham C.R. Brain-derived neurotrophic factor triggers transcription-dependent, late phase long-term potentiation in vivo. J. Neurosci. 2002, 22:7453-7461.
64. Mizumatsu S., Monje M.L., Morhardt D.R., Rola R., Palmer T.D., Fike J.R. Extreme sensitivity of adult neurogenesis to low doses of X-irradiation. Cancer Res. 2003, 63:4021-4027.
65. Monje M.L., Mizumatsu S., Fike J.R., Palmer T.D. Irradiation induces neural precursor-cell dysfunction. Nat. Med. 2002, 8:955-962.
66. Monje M.L., Palmer T. Radiation injury and neurogenesis. Curr. Opin. Neurol. 2003, 16:129-134.
67. Monje M.L., Toda H., Palmer T.D. Inflammatory blockade restores adult hippocampal neurogenesis. Science 2003, 302:1760-1765.
68. Moravan M.J., Olschowka J.A., Williams J.P., O'Banion M.K. Cranial irradiation leads to acute and persistent neuroinflammation with delayed increases in T-cell infiltration and CD11c expression in C57BL/6 mouse brain. Radiat. Res. 2011, 176:459-473.
69. Nakatsukasa H., Tsukimoto M., Ohshima Y., Tago F., Masada A., Kojima S. Suppressing effect of low-dose gamma-ray irradiation on collagen-induced arthritis. J. Radiat. Res. 2008, 49:381-389.
70. Naylor A.S., Bull C., Nilsson M.K., Zhu C., Bjork-Eriksson T., Eriksson P.S., Blomgren K., Kuhn H.G. Voluntary running rescues adult hippocampal neurogenesis after irradiation of the young mouse brain. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:14632-14637.
71. Nielsen J., Gotfryd K., Li S., Kulahin N., Soroka V., Rasmussen K.K., Bock E., Berezin V. Role of glial cell line-derived neurotrophic factor (GDNF)-neural cell adhesion molecule (NCAM) interactions in induction of neurite outgrowth and identification of a binding site for NCAM in the heel region of GDNF. J. Neurosci. 2009, 29:11360-11376.
72. Oh S.B., Park H.R., Jang Y.J., Choi S.Y., Son T.G., Lee J. Baicalein attenuates impaired hippocampal neurogenesis and the neurocognitive deficits induced by gamma-ray radiation. Br. J. Pharmacol. 2013, 168:421-431.
73. Parihar V.K., Limoli C.L. Cranial irradiation compromises neuronal architecture in the hippocampus. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:12822-12827.
74. Patel N.K., Gill S.S. GDNF delivery for Parkinson's disease. Acta Neurochir Suppl. 2007, 97:135-154.
75. Peacock K.H., Lesser G.J. Current therapeutic approaches in patients with brain metastases. Curr. Treat. Options Oncol. 2006, 7:479-489.
76. Pereira Dias G., Hollywood R., Bevilaqua M.C., da Luz A.C., Hindges R., Nardi A.E., Thuret S. Consequences of cancer treatments on adult hippocampal neurogenesis: implications for cognitive function and depressive symptoms. Neuro. Oncol. 2014, 16:476-492.
77. Pessoa L., Engelmann J.B. Embedding reward signals into perception and cognition. Front. Neurosci. 2010, 4.
78. Phelps E.A. Emotion and cognition: insights from studies of the human amygdala. Annu. Rev. Psychol. 2006, 57:27-53.
79. Raber J., Allen A.R., Rosi S., Sharma S., Dayger C., Davis M.J., Fike J.R. Effects of whole body (56)Fe radiation on contextual freezing and Arc-positive cells in the dentate gyrus. Behav. Brain Res. 2013, 246:162-167.
80. Raber J., Rola R., LeFevour A., Morhardt D., Curley J., Mizumatsu S., VandenBerg S.R., Fike J.R. Radiation-induced cognitive impairments are associated with changes in indicators of hippocampal neurogenesis. Radiat. Res. 2004, 162:39-47.
81. Rao A.A., Ye H., Decker P.A., Howe C.L., Wetmore C. Therapeutic doses of cranial irradiation induce hippocampus-dependent cognitive deficits in young mice. J. Neurooncol. 2011, 105:191-198.
82. Rasmusson A.M., Shi L., Duman R. Downregulation of BDNF mRNA in the hippocampal dentate gyrus after re-exposure to cues previously associated with footshock. Neuropsychopharmacology 2002, 27:133-142.
83. Rivera P.D., Shih H.Y., Leblanc J.A., Cole M.G., Amaral W.Z., Mukherjee S., Zhang S., Lucero M.J., Decarolis N.A., Chen B.P., Eisch A.J. Acute and fractionated exposure to high-LET (56)Fe HZE-particle radiation both result in similar long-term deficits in adult hippocampal neurogenesis. Radiat. Res. 2013, 180:658-667.
84. Rohde B.H., Rea M.A., Simon J.R., McBride W.J. Effects of X-irradiation induced loss of cerebellar granule cells on the synaptosomal levels and the high affinity uptake of amino acids. J. Neurochem. 1979, 32:1431-1435.
85. Rola R., Raber J., Rizk A., Otsuka S., VandenBerg S.R., Morhardt D.R., Fike J.R. Radiation-induced impairment of hippocampal neurogenesis is associated with cognitive deficits in young mice. Exp. Neurol. 2004, 188:316-330.
86. Rosi S., Andres-Mach M., Fishman K.M., Levy W., Ferguson R.A., Fike J.R. Cranial irradiation alters the behaviorally induced immediate-early gene arc (activity-regulated cytoskeleton-associated protein). Cancer Res. 2008, 68:9763-9770.
87. Rylett R.J., Williams L.R. Role of neurotrophins in cholinergic-neurone function in the adult and aged CNS. Trends Neurosci. 1994, 17:486-490.
88. Sahay A., Hen R. Adult hippocampal neurogenesis in depression. Nat. Neurosci. 2007, 10:1110-1115.
89. Schindler M.K., Forbes M.E., Robbins M.E., Riddle D.R. Aging-dependent changes in the radiation response of the adult rat brain. Int. J. Radiat. Oncol. Biol. Phys. 2008, 70:826-834.
90. Schnegg C.I., Greene-Schloesser D., Kooshki M., Payne V.S., Hsu F.C., Robbins M.E. The PPARδ agonist GW0742 inhibits neuroinflammation, but does not restore neurogenesis or prevent early delayed hippocampal-dependent cognitive impairment after whole-brain irradiation. Free Radical Bio. Med. 2013, 61:1-9.
91. Shekelle R.B., Raynor W.J., Ostfeld A.M., Garron D.C., Bieliauskas L.A., Liu S.C., Maliza C., Paul O. Psychological depression and 17-year risk of death from cancer. Psychosom. Med. 1981, 43:117-125.
92. Sheng M., McFadden G., Greenberg M.E. Membrane depolarization and calcium induce c-fos transcription via phosphorylation of transcription factor CREB. Neuron 1990, 4:571-582.
93. Shi L., Adams M.M., Long A., Carter C.C., Bennett C., Sonntag W.E., Nicolle M.M., Robbins M., D'Agostino R., Brunso-Bechtold J.K. Spatial learning and memory deficits after whole-brain irradiation are associated with changes in NMDA receptor subunits in the hippocampus. Radiat. Res. 2006, 166:892-899.
94. Shirayama Y., Chen A.C., Nakagawa S., Russell D.S., Duman R.S. Brain-derived neurotrophic factor produces antidepressant effects in behavioral models of depression. J. Neurosci. 2002, 22:3251-3261.
95. Silver J., Miller J.H. Regeneration beyond the glial scar. Nat. Rev. Neurosci. 2004, 5:146-156.
96. Slotman B., Faivre-Finn C., Kramer G., Rankin E., Snee M., Hatton M., Postmus P., Collette L., Musat E., Senan S. Prophylactic cranial irradiation in extensive small-cell lung cancer. N. Engl. J. Med. 2007, 357:664-672. Group E.R.O., Lung Cancer G.Lung Cancer G.
97. Snyder J.S., Kee N., Wojtowicz J.M. Effects of adult neurogenesis on synaptic plasticity in the rat dentate gyrus. J. Neurophysiol. 2001, 85:2423-2431.
98. Snyder J.S., Soumier A., Brewer M., Pickel J., Cameron H.A. Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature 2011, 476:458-461.
99. Son Y., Yang M., Kim J.S., Kim J., Kim S.H., Kim J.C., Shin T., Wang H., Jo S.K., Jung U., Moon C. Hippocampal dysfunction during the chronic phase following a single exposure to cranial irradiation. Exp. Neurol. 2014, 254:134-144.
100. Stoll G., Jander S. The role of microglia and macrophages in the pathophysiology of the CNS. Prog. Neurobiol. 1999, 58:233-247.
101. Stranahan A.M. Physiological variability in brain-derived neurotrophic factor expression predicts dendritic spine density in the mouse dentate gyrus. Neurosci. Lett. 2011, 495:60-62.
102. Taliaz D., Stall N., Dar D.E., Zangen A. Knockdown of brain-derived neurotrophic factor in specific brain sites precipitates behaviors associated with depression and reduces neurogenesis. Mol. Psychiatry 2010, 15:80-92.
103. Taphoorn M.J., Klein M. Cognitive deficits in adult patients with brain tumours. Lancet Neurol. 2004, 3:159-168.
104. Thomas R.M., Hotsenpiller G., Peterson D.A. Acute psychosocial stress reduces cell survival in adult hippocampal neurogenesis without altering proliferation. J. Neurosci. 2007, 27:2734-2743.
105. Tofilon P.J., Fike J.R. The radioresponse of the central nervous system: a dynamic process. Radiat. Res. 2000, 153:357-370.
106. Vaidya V.A., Fernandes K., Jha S. Regulation of adult hippocampal neurogenesis: relevance to depression. Expert Rev. Neurother. 2007, 7:853-864.
107. van't Spijker A., Trijsburg R.W., Duivenvoorden H.J. Psychological sequelae of cancer diagnosis: a meta-analytical review of 58 studies after 1980. Psychosom. Med. 1997, 59:280-293.
108. Voloboueva L.A., Giffard R.G. Inflammation, mitochondria, and the inhibition of adult neurogenesis. J. Neurosci. Res. 2011, 89:1989-1996.
109. Waltereit R., Dammermann B., Wulff P., Scafidi J., Staubli U., Kauselmann G., Bundman M., Kuhl D. Arg3.1/Arc mRNA induction by Ca2+ and cAMP requires protein kinase A and mitogen-activated protein kinase/extracellular regulated kinase activation. J. Neurosci. 2001, 21:5484-5493.
110. Wan X.S., Ware J.H., Zhou Z., Donahue J.J., Guan J., Kennedy A.R. Protection against radiation-induced oxidative stress in cultured human epithelial cells by treatment with antioxidant agents. Int. J. Radiat. Oncol. Biol. Phys. 2006, 64:1475-1481.
111. Winocur G., Wojtowicz J.M., Sekeres M., Snyder J.S., Wang S. Inhibition of neurogenesis interferes with hippocampus-dependent memory function. Hippocampus 2006, 16:296-304.
112. Wojtowicz J.M. Irradiation as an experimental tool in studies of adult neurogenesis. Hippocampus 2006, 16:261-266.
113. Wojtowicz J.M., Askew M.L., Winocur G. The effects of running and of inhibiting adult neurogenesis on learning and memory in rats. Eur. J. Neurosci. 2008, 27:1494-1502.
114. Wong-Goodrich S.J., Pfau M.L., Flores C.T., Fraser J.A., Williams C.L., Jones L.W. Voluntary running prevents progressive memory decline and increases adult hippocampal neurogenesis and growth factor expression after whole-brain irradiation. Cancer Res. 2010, 70:9329-9338.
115. Yang M., Kim J., Kim J.S., Kim S.H., Kim J.C., Kang M.J., Jung U., Shin T., Wang H., Moon C. Hippocampal dysfunctions in tumor-bearing mice. Brain Behav. Immun. 2014, 36:147-155.
116. Yang M., Kim J., Kim S.H., Kim J.S., Shin T., Moon C. Temporal profiles of synaptic plasticity-related signals in adult mouse hippocampus with methotrexate treatment. Neural. Regen. Res. 2012, 7:1651-1658.
117. Yang M., Kim J.S., Kim J., Jang S., Kim S.H., Kim J.C., Shin T., Wang H.B., Moon C. Acute treatment with methotrexate induces hippocampal dysfunction in a mouse model of breast cancer. Brain Res. Bull. 2012, 89:50-56.
118. Yang M., Kim J.S., Kim J., Kim S.H., Kim J.C., Kim J., Wang H.B., Shin T., Moon C. Neurotoxicity of methotrexate to hippocampal cells in vivo and in vitro. Biochem. Pharmacol. 2011, 82:72-80.
119. Yang M., Kim J.S., Song M.S., Kim S.H., Kang S.S., Bae C.S., Kim J.C., Wang H.B., Shin T., Moon C. Cyclophosphamide impairs hippocampus-dependent learning and memory in adult mice: Possible involvement of hippocampal neurogenesis in chemotherapy-induced memory deficits. Neurobiol. Learn. Mem. 2010, 93:487-494.
120. Yang M., Moon C. Neurotoxicity of cancer chemotherapy. Neural Regen. Res. 2013, 8:1606-1614.
121. Yazlovitskaya E.M., Edwards E., Thotala D., Fu A., Osusky K.L., Whetsell W.O., Boone B., Shinohara E.T., Hallahan D.E. Lithium treatment prevents neurocognitive deficit resulting from cranial irradiation. Cancer Res. 2006, 66:11179-11186.