Cranial irradiation regulates CREB-BDNF signaling and variant BDNF transcript levels in the mouse hippocampus

Neurobiology of Learning and Memory

Volumn 121, Issue , 2015, Pages 12-19

  Son, Yeonghoon ^a   Yang, Miyoung ^b,c   Kang, Sohi ^a   Lee, Sueun ^a   Kim, Jinwook ^a   Kim, Juhwan ^a   Park, Seri ^a   Kim, Joong Sun ^d   Jo, Sung Kee ^e   Jung, Uhee ^e   Shin, Taekyun ^f   Kim, Sung Ho ^a   Wang, Hongbing ^b   Moon, Changjong ^a  

^a Chonnam National University   (South Korea)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c Wonkwang University   (South Korea)

^d Dongnam Institute of Radiological and Medical Science   (South Korea)

^e Jeongeup Campus of Korea Atomic Energy Research Institute (KAERI)   (South Korea)

^f Jeju National University   (South Korea)

Author keywords

BDNF; Cranial irradiation; CREB; Exon; Hippocampus; Memory deficit

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; CONDITIONING; CONTROLLED STUDY; DOWN REGULATION; EXON; FEAR; HIPPOCAMPUS; LOCOMOTION; MEMORY DISORDER; MOUSE; NONHUMAN; NOVEL OBJECT RECOGNITION TEST; OPEN FIELD TEST; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RADIATION EXPOSURE; SIGNAL TRANSDUCTION; SKULL IRRADIATION; TASK PERFORMANCE; ANIMAL; BRAIN; C57BL MOUSE; CONDITIONED REFLEX; MALE; METABOLISM; MOTOR ACTIVITY; PHOSPHORYLATION; PHYSIOLOGY; RADIATION RESPONSE; RECOGNITION;

ANIMALS; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CONDITIONING, CLASSICAL; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; FEAR; HIPPOCAMPUS; MALE; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; PHOSPHORYLATION; RECOGNITION (PSYCHOLOGY); RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 84925435294     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2015.03.002     Document Type: Article

References (50)

1. Aid T., Kazantseva A., Piirsoo M., Palm K., Timmusk T. Mouse and rat BDNF gene structure and expression revisited. Journal of Neuroscience Research 2007, 85:525-535.
2. Baj G., D'Alessandro V., Musazzi L., Mallei A., Sartori C.R., Sciancalepore M., et al. Physical exercise and antidepressants enhance BDNF targeting in hippocampal CA3 dendrites: Further evidence of a spatial code for BDNF splice variants. Neuropsychopharmacology 2012, 37:1600-1611.
3. Baj G., Del Turco D., Schlaudraff J., Torelli L., Deller T., Tongiorgi E. Regulation of the spatial code for BDNF mRNA isoforms in the rat hippocampus following pilocarpine-treatment: A systematic analysis using laser microdissection and quantitative real-time PCR. Hippocampus 2013, 23:413-423.
4. Barde Y.A. Neurotrophins: A family of proteins supporting the survival of neurons. Progress in Clinical and Biological Research 1994, 390:45-56.
5. Belarbi K., Jopson T., Arellano C., Fike J.R., Rosi S. CCR2 deficiency prevents neuronal dysfunction and cognitive impairments induced by cranial irradiation. Cancer Research 2013, 73:1201-1210.
6. 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.
7. Bender R.A., Lauterborn J.C., Gall C.M., Cariaga W., Baram T.Z. Enhanced CREB phosphorylation in immature dentate gyrus granule cells precedes neurotrophin expression and indicates a specific role of CREB in granule cell differentiation. The European Journal of Neuroscience 2001, 13:679-686.
8. Calvo W., Hopewell J.W., Reinhold H.S., Yeung T.K. Time- and dose-related changes in the white matter of the rat brain after single doses of X rays. The British Journal of Radiology 1988, 61:1043-1052.
9. Chiaruttini C., Sonego M., Baj G., Simonato M., Tongiorgi E. BDNF mRNA splice variants display activity-dependent targeting to distinct hippocampal laminae. Molecular and Cellular Neurosciences 2008, 37:11-19.
10. Cohen J. Statistical power analysis for the behavioral sciences 1988, L. Erlbaum Associates, Hillsdale, N.J. 2nd ed.
11. Conner J.M., Lauterborn J.C., Yan Q., Gall C.M., Varon S. Distribution of brain-derived neurotrophic factor (BDNF) protein and mRNA in the normal adult rat CNS: Evidence for anterograde axonal transport. The Journal of Neuroscience 1997, 17:2295-2313.
12. Dias B.G., Banerjee S.B., Duman R.S., Vaidya V.A. Differential regulation of brain derived neurotrophic factor transcripts by antidepressant treatments in the adult rat brain. Neuropharmacology 2003, 45:553-563.
13. Eichenbaum H. The hippocampus and declarative memory: Cognitive mechanisms and neural codes. Behavioural Brain Research 2001, 127:199-207.
14. Figurov A., Pozzo-Miller L.D., Olafsson P., Wang T., Lu B. Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus. Nature 1996, 381:706-709.
15. Hopewell J.W. Radiation injury to the central nervous system. Medical and Pediatric Oncology 1998, (Suppl. 1):1-9.
16. Hu Y., Russek S.J. BDNF and the diseased nervous system: A delicate balance between adaptive and pathological processes of gene regulation. Journal of Neurochemistry 2008, 105:1-17.
17. Kim J.S., Lee H.J., Kim J.C., Kang S.S., Bae C.S., Shin T., et al. Transient impairment of hippocampus-dependent learning and memory in relatively low-dose of acute radiation syndrome is associated with inhibition of hippocampal neurogenesis. Journal of Radiation Research 2008, 49:517-526.
18. Kim J., Yang M., Kim J., Song L., Lee S., Son Y., et al. Developmental and degenerative modulation of brain-derived neurotrophic factor transcript variants in the mouse hippocampus. International Journal of Developmental Neuroscience 2014, 38C:68-73.
19. Korte M., Carroll P., Wolf E., Brem G., Thoenen H., Bonhoeffer T. Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proceedings of the National Academy of Sciences of Unites States of America 1995, 92:8856-8860.
20. Licata S.C., Shinday N.M., Huizenga M.N., Darnell S.B., Sangrey G.R., Rudolph U., et al. Alterations in brain-derived neurotrophic factor in the mouse hippocampus following acute but not repeated benzodiazepine treatment. PLoS One 2013, 8:e84806.
21. Linnarsson S., Bjorklund A., Ernfors P. Learning deficit in BDNF mutant mice. The European Journal of Neuroscience 1997, 9:2581-2587.
22. Lubin F.D., Roth T.L., Sweatt J.D. Epigenetic regulation of BDNF gene transcription in the consolidation of fear memory. The Journal of Neuroscience 2008, 28:10576-10586.
23. McAllister A.K. Neurotrophins and neuronal differentiation in the central nervous system. Cellular and Molecular Life Sciences 2001, 58:1054-1060.
24. Nair A., Vadodaria K.C., Banerjee S.B., Benekareddy M., Dias B.G., Duman R.S., et al. Stressor-specific regulation of distinct brain-derived neurotrophic factor transcripts and cyclic AMP response element-binding protein expression in the postnatal and adult rat hippocampus. Neuropsychopharmacology 2007, 32:1504-1519.
25. 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. British Journal of Pharmacology 2013, 168:421-431.
26. Patterson S.L., Abel T., Deuel T.A., Martin K.C., Rose J.C., Kandel E.R. Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron 1996, 16:1137-1145.
27. Raber J., Rola R., LeFevour A., Morhardt D., Curley J., Mizumatsu S., et al. Radiation-induced cognitive impairments are associated with changes in indicators of hippocampal neurogenesis. Radiation Research 2004, 162:39-47.
28. Rattiner L.M., Davis M., Ressler K.J. Differential regulation of brain-derived neurotrophic factor transcripts during the consolidation of fear learning. Learning & Memory 2004, 11:727-731.
29. Riccio A., Ahn S., Davenport C.M., Blendy J.A., Ginty D.D. Mediation by a CREB family transcription factor of NGF-dependent survival of sympathetic neurons. Science 1999, 286:2358-2361.
30. Rola R., Raber J., Rizk A., Otsuka S., VandenBerg S.R., Morhardt D.R., et al. Radiation-induced impairment of hippocampal neurogenesis is associated with cognitive deficits in young mice. Experimental Neurology 2004, 188:316-330.
31. 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.
32. Schindler M.K., Forbes M.E., Robbins M.E., Riddle D.R. Aging-dependent changes in the radiation response of the adult rat brain. International Journal of Radiation Oncology Biology Physics 2008, 70:826-834.
33. Schmidt H.D., Sangrey G.R., Darnell S.B., Schassburger R.L., Cha J.H., Pierce R.C., et al. Increased brain-derived neurotrophic factor (BDNF) expression in the ventral tegmental area during cocaine abstinence is associated with increased histone acetylation at BDNF exon I-containing promoters. Journal of Neurochemistry 2012, 120:202-209.
34. Seo H.S., Yang M., Song M.S., Kim J.S., Kim S.H., Kim J.C., et al. Toluene inhibits hippocampal neurogenesis in adult mice. Pharmacology, Biochemistry, and Behavior 2010, 94:588-594.
35. Shieh P.B., Ghosh A. Molecular mechanisms underlying activity-dependent regulation of BDNF expression. Journal of Neurobiology 1999, 41:127-134.
36. Shieh P.B., Hu S.C., Bobb K., Timmusk T., Ghosh A. Identification of a signaling pathway involved in calcium regulation of BDNF expression. Neuron 1998, 20:727-740.
37. Simmons D.A., Rex C.S., Palmer L., Pandyarajan V., Fedulov V., Gall C.M., et al. Up-regulating BDNF with an ampakine rescues synaptic plasticity and memory in Huntington's disease knockin mice. Proceedings of the National Academy of Sciences of Unites States of America 2009, 106:4906-4911.
38. Snyder J.S., Hong N.S., McDonald R.J., Wojtowicz J.M. A role for adult neurogenesis in spatial long-term memory. Neuroscience 2005, 130:843-852.
39. Son Y., Yang M., Kim J.S., Kim J., Kim S.H., Kim J.C., et al. Hippocampal dysfunction during the chronic phase following a single exposure to cranial irradiation. Experimental Neurology 2014, 254:134-144.
40. Son Y., Yang M., Wang H., Moon C. Hippocampal dysfunctions caused by cranial irradiation: A review of the experimental evidence. Brain, Behavior, and Immunity 2015, 45C:287-296.
41. Squire L.R. Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans. Psychological Review 1992, 99:195-231.
42. Timmusk T., Palm K., Metsis M., Reintam T., Paalme V., Saarma M., et al. Multiple promoters direct tissue-specific expression of the rat BDNF gene. Neuron 1993, 10:475-489.
43. Vaynman S., Ying Z., Gomez-Pinilla F. Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. The European Journal of Neuroscience 2004, 20:2580-2590.
44. Weinreb O., Amit T., Bar-Am O., Youdim M.B. Induction of neurotrophic factors GDNF and BDNF associated with the mechanism of neurorescue action of rasagiline and ladostigil: New insights and implications for therapy. Annals of the New York Academy of Sciences 2007, 1122:155-168.
45. West A.E., Chen W.G., Dalva M.B., Dolmetsch R.E., Kornhauser J.M., Shaywitz A.J., et al. Calcium regulation of neuronal gene expression. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:11024-11031.
46. 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 Research 2010, 70:9329-9338.
47. Yang M., Kim H., Kim J., Kim S.H., Kim J.C., Bae C.S., et al. Fast neutron irradiation deteriorates hippocampus-related memory ability in adult mice. Journal of Veterinary Science 2012, 13:1-6.
48. Yang M., Kim J., Kim J.S., Kim S.H., Kim J.C., Kang M.J., et al. Hippocampal dysfunctions in tumor-bearing mice. Brain, Behavior, and Immunity 2014, 36:147-155.
49. Yang M., Kim J.S., Kim J., Kim S.H., Kim J.C., Kim J., et al. Neurotoxicity of methotrexate to hippocampal cells in vivo and in vitro. Biochemical Pharmacology 2011, 82:72-80.
50. Zheng F., Zhou X., Luo Y., Xiao H., Wayman G., Wang H. Regulation of brain-derived neurotrophic factor exon IV transcription through calcium responsive elements in cortical neurons. PLoS One 2011, 6:e28441.