Whole brain radiation-induced impairments in learning and memory are time-sensitive and reversible by systemic hypoxia

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Warrington, Junie P ^a,b   Csiszar, Anna ^b   Mitschelen, Matthew ^b   Lee, Yong Woo ^c   Sonntag, William E ^a,b  

^a UNIVERSITY OF OKLAHOMA HEALTH SCIENCES CENTER   (United States)

^b UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^c VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AVOIDANCE BEHAVIOR; BRAIN BLOOD VESSEL; BRAIN RADIATION; COGNITIVE DEFECT; CONTEXTUAL LEARNING; CONTROLLED STUDY; HIPPOCAMPUS; HYPOXIA; LEARNING DISORDER; MALE; MAZE TEST; MEMORY CONSOLIDATION; MEMORY DISORDER; MOUSE; NONHUMAN; SPATIAL LEARNING; SPATIAL MEMORY; WORKING MEMORY; ANIMAL; ANOXIA; BRAIN; C57BL MOUSE; MEMORY; PATHOPHYSIOLOGY; PHYSIOLOGY; RADIATION EXPOSURE; RADIATION INJURY; TIME;

MUS;

ANIMALS; ANOXIA; BRAIN; COGNITION DISORDERS; HIPPOCAMPUS; LEARNING DISORDERS; MALE; MAZE LEARNING; MEMORY; MEMORY DISORDERS; MICE; MICE, INBRED C57BL; RADIATION INJURIES, EXPERIMENTAL; TIME FACTORS;

EID: 84862908289     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0030444     Document Type: Article

References (60)

1. American Cancer Society (2011) Cancer Facts & Figures 2011. Atlanta American Cancer Society.
2. American Brain Tumor Association (2011) Facts & Statistics, 2011.
3. Khuntia D, Brown P, Li J, Mehta M, (2006) Whole-brain radiotherapy in the management of brain metastasis. J Clin Oncol 24: 1295-1304.
4. Li J, Bentzen S, Renschler M, Mehta M, (2008) Relationship between neurocognitive function and quality of life after whole-brain radiotherapy in patients with brain metastasis. Int J Radiat Oncol Biol Phys 71: 64-70.
5. Welzel G, Fleckenstein K, Mai S, Hermann B, Kraus-Tiefenbacher U, et al. (2008) Acute neurocognitive impairment during cranial radiation therapy in patients with intracranial tumors. Strahlenther Onkol 184: 647-654.
6. Welzel G, Fleckenstein K, Schaefer J, Hermann B, Kraus-Tiefenbacher U, et al. (2008) Memory function before and after whole brain radiotherapy in patients with and without brain metastases. Int J Radiat Oncol Biol Phys 72: 1311-1318.
7. Brown W, Blair R, Moody D, Thore C, Ahmed S, et al. (2007) Capillary loss precedes the cognitive impairment induced by fractionated whole-brain irradiation: a potential rat model of vascular dementia. J Neurol Sci 257: 67-71.
8. Shi L, Adams MM, Long A, Carter CC, Bennett C, et al. (2006) Spatial learning and memory deficits after whole-brain irradiation are associated with changes in NMDA receptor subunits in the hippocampus. Radiat Res 166: 892-899.
9. Rola R, Raber J, Rizk A, Otsuka S, VandenBerg SR, et al. (2004) Radiation-induced impairment of hippocampal neurogenesis is associated with cognitive deficits in young mice. Exp Neurol 188: 316-330.
10. Lee WH, Sonntag WE, Mitschelen M, Yan H, Lee YW, (2010) Irradiation induces regionally specific alterations in pro-inflammatory environments in rat brain. Int J Radiat Biol 86: 132-144.
11. Lee WH, Warrington JP, Sonntag WE, Lee YW, (2011) Irradiation alters MMP-2/TIMP- 2 system and collagen type IV degradation in brain. International Journal of Radiation Oncology Biology Physics.
12. Li Y, Chen P, Haimovitz-Friedman A, Reilly R, Wong C, (2003) Endothelial apoptosis initiates acute blood-brain barrier disruption after ionizing radiation. Cancer Res 63: 5950-5956.
13. Li Y, Chen P, Jain V, Reilly R, Wong C, (2004) Early radiation-induced endothelial cell loss and blood-spinal cord barrier breakdown in the rat spinal cord. Radiat Res 161: 143-152.
14. Kamiryo T, Lopes M, Kassell N, Steiner L, Lee K, (2001) Radiosurgery-induced microvascular alterations precede necrosis of the brain neuropil. Neurosurgery 49: 409-414; discussion 414-405.
15. Brown W, Thore C, Moody D, Robbins M, Wheeler K, (2005) Vascular damage after fractionated whole-brain irradiation in rats. Radiat Res 164: 662-668.
16. Warrington JP, Csiszar A, Johnson DA, Herman TS, Ahmad S, et al. (2011) Cerebral microvascular rarefaction induced by whole brain radiation is reversible by systemic hypoxia in mice. Am J Physiol Heart Circ Physiol 300: H736-744.
17. Chang E, Wefel J, Hess K, Allen P, Lang F, et al. (2009) Neurocognition in patients with brain metastases treated with radiosurgery or radiosurgery plus whole-brain irradiation: a randomised controlled trial. Lancet Oncol 10: 1037-1044.
18. DeAngelis LM, Delattre JY, Posner JB, (1989) Radiation-induced dementia in patients cured of brain metastases. Neurology 39: 789-796.
19. Silber J, Radcliffe J, Peckham V, Perilongo G, Kishnani P, et al. (1992) Whole-brain irradiation and decline in intelligence: the influence of dose and age on IQ score. J Clin Oncol 10: 1390-1396.
20. Liu Y, Xiao S, Liu J, Zhou H, Liu Z, et al. (2010) An experimental study of acute radiation-induced cognitive dysfunction in a young rat model. AJNR Am J Neuroradiol 31: 383-387.
21. Akiyama K, Tanaka R, Sato M, Takeda N, (2001) Cognitive dysfunction and histological findings in adult rats one year after whole brain irradiation. Neurol Med Chir (Tokyo) 41: 590-598.
22. Raber J, Rola R, LeFevour A, Morhardt D, Curley J, et al. (2004) Radiation-induced cognitive impairments are associated with changes in indicators of hippocampal neurogenesis. Radiat Res 162: 39-47.
23. Fisher M, (2009) Pericyte signaling in the neurovascular unit. Stroke 40: S13-15.
24. Udagawa T, Birsner A, Wood M, D'Amato R, (2007) Chronic suppression of angiogenesis following radiation exposure is independent of hematopoietic reconstitution. Cancer Res 67: 2040-2045.
25. Troen AM, Shea-Budgell M, Shukitt-Hale B, Smith DE, Selhub J, et al. (2008) B-vitamin deficiency causes hyperhomocysteinemia and vascular cognitive impairment in mice. Proc Natl Acad Sci U S A 105: 12474-12479.
26. Clark PJ, Brzezinska WJ, Puchalski EK, Krone DA, Rhodes JS, (2009) Functional analysis of neurovascular adaptations to exercise in the dentate gyrus of young adult mice associated with cognitive gain. Hippocampus 19: 937-950.
27. Cao R, Jensen L, Söll I, Hauptmann G, Cao Y, (2008) Hypoxia-induced retinal angiogenesis in zebrafish as a model to study retinopathy. PLoS One 3: e2748.
28. Ingraham JP, Forbes ME, Riddle DR, Sonntag WE, (2008) Aging reduces hypoxia-induced microvascular growth in the rodent hippocampus. J Gerontol A Biol Sci Med Sci 63: 12-20.
29. Vilar J, Waeckel L, Bonnin P, Cochain C, Loinard C, et al. (2008) Chronic hypoxia-induced angiogenesis normalizes blood pressure in spontaneously hypertensive rats. Circ Res 103: 761-769.
30. Conway E, Collen D, Carmeliet P, (2001) Molecular mechanisms of blood vessel growth. Cardiovasc Res 49: 507-521.
31. Liao D, Johnson R, (2007) Hypoxia: a key regulator of angiogenesis in cancer. Cancer Metastasis Rev 26: 281-290.
32. Denko N, (2008) Hypoxia, HIF1 and glucose metabolism in the solid tumour. Nat Rev Cancer.
33. Pugh C, Ratcliffe P, (2003) Regulation of angiogenesis by hypoxia: role of the HIF system. Nat Med 9: 677-684.
34. Kang SG, Shinojima N, Hossain A, Gumin J, Yong RL, et al. (2010) Isolation and perivascular localization of mesenchymal stem cells from mouse brain. Neurosurgery 67: 711-720.
35. Shi L, Molina D, Robbins M, Wheeler K, Brunso-Bechtold J, (2008) Hippocampal neuron number is unchanged 1 year after fractionated whole-brain irradiation at middle age. Int J Radiat Oncol Biol Phys 71: 526-532.
36. Fagel DM, Ganat Y, Silbereis J, Ebbitt T, Stewart W, et al. (2006) Cortical neurogenesis enhanced by chronic perinatal hypoxia. Exp Neurol 199: 77-91.
37. Jin K, Mao XO, Sun Y, Xie L, Greenberg DA, (2002) Stem cell factor stimulates neurogenesis in vitro and in vivo. J Clin Invest 110: 311-319.
38. Zhu X, Yan H, Zhang J, Qu H, Qiu X, et al. (2010) Intermittent hypoxia promotes hippocampal neurogenesis and produces antidepressant-like effects in adult rats. J Neurosci 30: 12653-12663.
39. Cengiz P, Uluc K, Kendigelen P, Akture E, Hutchinson E, et al. (2011) Chronic neurological deficits in mice after perinatal hypoxia and ischemia correlate with hemispheric tissue loss and white matter injury detected by MRI. Dev Neurosci 33: 270-279.
40. Muthuraju S, Maiti P, Solanki P, Sharma AK, Singh SB, et al. (2010) Cholinesterase inhibitors ameliorate spatial learning deficits in rats following hypobaric hypoxia. Exp Brain Res 203: 583-592.
41. Titus AD, Shankaranarayana Rao BS, Harsha HN, Ramkumar K, Srikumar BN, et al. (2007) Hypobaric hypoxia-induced dendritic atrophy of hippocampal neurons is associated with cognitive impairment in adult rats. Neuroscience 145: 265-278.
42. Muthuraju S, Maiti P, Solanki P, Sharma AK, Pati S, et al. (2011) Possible role of cholinesterase inhibitors on memory consolidation following hypobaric hypoxia of rats. Int J Neurosci 121: 279-288.
43. Muthuraju S, Maiti P, Pati S, Solanki P, Sharma AK, et al. (2011) Role of cholinergic markers on memory function of rats exposed to hypobaric hypoxia. Eur J Pharmacol.
44. Palmer T, Willhoite A, Gage F, (2000) Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 425: 479-494.
45. Acharya M, Christie L, Lan M, Donovan P, Cotman C, et al. (2009) Rescue of radiation-induced cognitive impairment through cranial transplantation of human embryonic stem cells. Proc Natl Acad Sci U S A 106: 19150-19155.
46. Noguès X, Corsini MM, Marighetto A, Abrous DN, (2011) Functions for adult neurogenesis in memory: An introduction to the neurocomputational approach and to its contribution. Behav Brain Res.
47. Marín-Burgin A, Schinder AF, (2011) Requirement of adult-born neurons for hippocampus-dependent learning. Behav Brain Res.
48. Ming GL, Song H, (2011) Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70: 687-702.
49. Zhu C, Huang Z, Gao J, Zhang Y, Wang X, et al. (2009) Irradiation to the immature brain attenuates neurogenesis and exacerbates subsequent hypoxic-ischemic brain injury in the adult. J Neurochem 111: 1447-1456.
50. Jahanshahi M, Khoshbin Khoshnazar A, Azami NS, Heidari M, (2011) Radiation-induced lowered neurogenesis associated with shortened latency of inhibitory avoidance memory response. Folia Neuropathol 49: 103-108.
51. Kim S, Jang BS, Jung U, Jo SK, (2011) Gamma-irradiation is more efficient at depleting hippocampal neurogenesis than D-galactose/NaNO2. Neurosci Lett 498: 47-51.
52. Achanta P, Fuss M, Martinez JL, (2009) Ionizing radiation impairs the formation of trace fear memories and reduces hippocampal neurogenesis. Behav Neurosci 123: 1036-1045.
53. Fishman K, Baure J, Zou Y, Huang TT, Andres-Mach M, et al. (2009) Radiation-induced reductions in neurogenesis are ameliorated in mice deficient in CuZnSOD or MnSOD. Free Radic Biol Med 47: 1459-1467.
54. Monje M, (2008) Cranial radiation therapy and damage to hippocampal neurogenesis. Dev Disabil Res Rev 14: 238-242.
55. Manda K, Ueno M, Anzai K, (2009) Cranial irradiation-induced inhibition of neurogenesis in hippocampal dentate gyrus of adult mice: attenuation by melatonin pretreatment. J Pineal Res 46: 71-78.
56. Coremans V, Ahmed T, Balschun D, D'Hooge R, DeVriese A, et al. (2010) Impaired neurogenesis, learning and memory and low seizure threshold associated with loss of neural precursor cell survivin. BMC Neurosci 11: 2.
57. Barnes CA, (1979) Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. J Comp Physiol Psychol 93: 74-104.
58. Berta S, Gert L, Harald H, Sudarshan P, (2007) Barnes maze, a useful task to assess spatial reference memory in the mice. Protocol Exchange.
59. Koopmans G, Blokland A, van Nieuwenhuijzen P, Prickaerts J, (2003) Assessment of spatial learning abilities of mice in a new circular maze. Physiol Behav 79: 683-693.
60. Hof PR, Young WC, Bloom FE, Belichenko PV, Celio MR, (2000) Comparative Cytoachitectonic Atlas of the C57BL/6 and 129/Sv Mouse Brains: Elsevier.