Voluntary running rescues adult hippocampal neurogenesis after irradiation of the young mouse brain

Proceedings of the National Academy of Sciences of the United States of America

Volumn 105, Issue 38, 2008, Pages 14632-14637

  Naylor, Andrew S ^a,b   Bull, Cecilia ^a   Nilsson, Marie K L ^a   Zhu, Changlian ^a   Björk Eriksson, Thomas ^c,e   Eriksson, Peter S ^a   Blomgren, Klas ^a,d,f   Kuhn, H Georg ^a,f  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

^c SAHLGRENSKA UNIVERSITY HOSPITAL   (Sweden)

^d QUEEN SILVIA CHILDREN'S HOSPITAL   (Sweden)

^e Rigshospitalet   (Denmark)

^f UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Exercise; Juvenile; Open field; Radiotherapy; Stem cell

Indexed keywords

DOUBLECORTIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; BRAIN INJURY; CANCER RADIOTHERAPY; CHILDHOOD CANCER; CONTROLLED STUDY; DENTATE GYRUS; EXERCISE; HIPPOCAMPUS; HISTOPATHOLOGY; IRRADIATION; MALE; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OPEN FIELD TEST; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RADIATION DOSE; REHABILITATION CARE; RUNNING; STEM CELL; VOLUNTARY MOVEMENT;

ANIMALS; BEHAVIOR, ANIMAL; CELL PROLIFERATION; CRANIAL IRRADIATION; DENTATE GYRUS; GENE EXPRESSION REGULATION; HIPPOCAMPUS; MALE; MICE; MICE, INBRED C57BL; MICROTUBULE-ASSOCIATED PROTEINS; NEURONS; NEUROPEPTIDES; RUNNING; STEM CELLS;

MUS;

EID: 55749088804     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0711128105     Document Type: Article

References (62)

1. Lannering B, Marky I, Lundberg A, Olsson E (1990) Long-term sequelae after pediatric brain tumors: Their effect on disability and quality of life. Med Pediatr Oncol 18:304-310.
2. Crossen JR, Garwood D, Glatstein E, Neuwelt EA (1994) Neurobehavioral sequelae of cranial irradiation in adults: A review of radiation-induced encephalopathy. J Clin Oncol 12:627-642.
3. Schultheiss TE, Kun LE, Ang KK, Stephens LC (1995) Radiation response of the central nervous system. Int J Radiat Oncol Biol Phys 31:1093-1112.
4. Correa DD, et al. (2004) Cognitive functions in survivors of primary central nervous system lymphoma. Neurology 62:548-555.
5. Spiegler BJ, Bouffet E, Greenberg ML, Rutka JT, Mabbott DJ (2004) Change in neurocognitive functioning after treatment with cranial radiation in childhood. J Clin Oncol 22:706-713.
6. Shors TJ, Townsend DA, Zhao M, Kozorovitskiy Y, Gould E (2002) Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 12:578-584.
7. Kempermann G., Wiskott L, Gage FH (2004) Functional significance of adult neurogenesis. Curr Opin Neurobiol 2:186-191.
8. Eriksson PS, et al. (1998) Neurogenesis in the adult human hippocampus. Nat Med 4:1313-1317.
9. Kuhn HG, Dickinson-Anson H, Gage FH (1996) Neurogenesis in the dentate gyrus of the adult rat: Age-related decrease of neuronal progenitor proliferation. J Neurosci 16:2027-2033.
10. Monje ML, Mizumatsu S, Fike JR, Palmer TD (2002) Irradiation induces neural precursor-cell dysfunction. Nat Med 8:955-962.
11. Madsen TM, Kristjansen PE, Bolwig TG, Wortwein G (2003) Arrested neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat. Neuroscience 119:635-642.
12. Mizumatsu S, et al. (2003) Extreme sensitivity of adult neurogenesis to low doses of x-irradiation. Cancer Res 63:4021-4027.
13. Tada E, Parent JM, Lowenstein DH, Fike JR (2000) X-irradiation causes a prolonged reduction in cell proliferation in the dentate gyrus of adult rats. Neuroscience 99:33-41.
14. Fukuda H, et al. (2004) Irradiation-induced progenitor cell death in the developing brain is resistant to erythropoietin treatment and caspase inhibition. Cell Death Differ 11:1166-1178.
15. Monje ML, et al. (2007) Impaired human hippocampal neurogenesis after treatment for central nervous system malignancies. Ann Neurol 62:515-520.
16. Raber J, et al. (2004) Radiation-induced cognitive impairments are associated with changes in indicators of hippocampal neurogenesis. Radiat Res 162:39-47.
17. Winocur G, Wojtowicz JM, Sekeres M, Snyder JS, Wang S (2006) Inhibition of neurogenesis interferes with hippocampus-dependent memory function. Hippocampus 16:296-304.
18. Snyder JS, Hong NS, McDonald RJ, Wojtowicz JM (2005) A role for adult neurogenesis in spatial long-term memory. Neuroscience 130:843-852.
19. Altman J (1987) Morphological and behavioral markers of environmentally induced retardation of brain development: An animal model. Environ Health Perspect 74:153-168.
20. Van Praag H, Kempermann G, Gage FH (1999) Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2:266-270.
21. Naylor AS, Persson AI, Eriksson PS, Jonsdottir IH, Thorlin T (2005) Extended voluntary running inhibits exercise-induced adult hippocampal progenitor proliferation in the spontaneously hypertensive rat. J Neurophysiol 93:2406-2414.
22. Holmes MM, Galea LA, Mistlberger RE, Kempermann G (2004) Adult hippocampal neurogenesis and voluntary running activity: Circadian and dose-dependent effects. J Neurosci Res 76:216-222.
23. Van Praag H, Christie BR, Sejnowski TJ, Gage FH (1999) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci USA 96:13427-13431.
24. Anderson BJ, et al. (2000) Exercise influences spatial learning in the radial arm maze. Physiol Behav 70:425-429.
25. Vaynman S, Ying Z, Gomez-Pinilla F (2004) Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur J Neurosci 20:2580-2590.
26. Fabel K, et al. (2003) VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur J Neurosci 18:2803-2812.
27. Neeper SA, Gomez-Pinilla F, Choi J, Cotman CW (1996) Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain. Brain Res 726:49-56.
28. Farmer J, et al. (2004) Effects of voluntary exercise on synaptic plasticity and gene expression in the dentate gyrus of adult male Sprague-Dawley rats in vivo. Neuroscience 124:71-79.
29. Ding Q, Vaynman S, Souda P, Whitelegge JP, Gomez-Pinilla F (2006) Exercise affects energy metabolism and neural plasticity-related proteins in the hippocampus as revealed by proteomic analysis. Eur J Neurosci 24:1265-1276.
30. Rogers RL, Meyer JS, Mortel KF (1990) After reaching retirement age physical activity sustains cerebral perfusion and cognition. J Am Geriatr Soc 38:123-128.
31. Colcombe S, Kramer AF (2003) Fitness effects on the cognitive function of older adults: A meta-analytic study. Psychol Sci 14:125-130.
32. Kramer AF, Erickson KI, Colcombe SJ (2006) Exercise, cognition, and the aging brain. J Appl Physiol 101:1237-1242.
33. Pereira AC, et al. (2007) An in vivo correlate of exercise-induced neurogenesis in the adult dentate gyrus. Proc Natl Acad Sci USA 104:5638-5643.
34. Fukuda A, et al. (2005) Age-dependent sensitivity of the developing brain to irradiation is correlated with the number and vulnerability of progenitor cells. J Neurochem 92:569-584.
35. Steiner B, et al. (2004) Differential regulation of gliogenesis in the context of adult hippocampal neurogenesis in mice. Glia 46:41-52.
36. Steiner B, et al. (2006) Type 2 cells as link between glial and neuronal lineage in adult hippocampal neurogenesis. Glia 54:805-814.
37. Brown JP, et al. (2003) Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467:1-10.
38. Couillard-Despres S, et al. (2005) Doublecortin expression levels in adult brain reflect neurogenesis. Eur J Neurosci 21:1-14.
39. Gleeson JG, et al. (1998) Doublecortin, a brain-specific gene mutated in human X-linked lissencephaly and double cortex syndrome, encodes a putative signaling protein. Cell 92:63-72.
40. Lemaire V, Koehl M, Le Moal M, Abrous DN (2000) Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci USA 97:11032-11037.
41. Bick-Sander A, Steiner B, Wolf SA, Babu H, Kempermann G (2006) Running in pregnancy transiently increases postnatal hippocampal neurogenesis in the offspring. Proc Natl Acad Sci USA 103:3852-3857.
42. Redila VA, et al. (2006) Hippocampal cell proliferation is reduced following prenatal ethanol exposure but can be rescued with voluntary exercise. Hippocampus 16:305-311.
43. Faverjon S, et al. (2002) Beneficial effects of enriched environment following status epilepticus in immature rats. Neurology 59:1356-1364.
44. Fowler JF (1989) The linear-quadratic formula and progress in fractionated radiotherapy. Br J Radiol 62:679-694.
45. Ben Abdallah NM, Slomianka L, Lipp HP (2007) Reversible effect of x-irradiation on proliferation, neurogenesis, and cell death in the dentate gyrus of adult mice. Hippocampus 17:1230-1240.
46. Stranahan AM, Khalil D, Gould E (2006) Social isolation delays the positive effects of running on adult neurogenesis. Nat Neurosci 9:526-533.
47. Plumpe T, et al. (2006) Variability of doublecortin-associated dendrite maturation in adult hippocampal neurogenesis is independent of the regulation of precursor cell proliferation. BMC Neurosci 7:77-91.
48. Oomen CA, Mayer JL, de Kloet ER, Joels M, Lucassen PJ (2007) Brief treatment with the glucocorticoid receptor antagonist mifepristone normalizes the reduction in neurogenesis after chronic stress. Eur J Neurosci 26:3395-3401.
49. Walker TL, Yasuda T, Adams DJ, Bartlett PF (2007) The doublecortin-expressing population in the developing and adult brain contains multipotential precursors in addition to neuronal-lineage cells. J Neurosci 27:3734-3742.
50. Doetsch F, Hen R (2005) Young and excitable: The function of new neurons in the adult mammalian brain. Curr Opin Neurobiol 15:121-128.
51. Deisseroth K, et al. (2004) Excitation-neurogenesis coupling in adult neural stem/progenitor cells. Neuron 42:535-552.
52. van Praag H, et al. (2002) Functional neurogenesis in the adult hippocampus. Nature 415:1030-1034.
53. Dayer AG, Ford AA, Cleaver KM, Yassaee M, Cameron HA (2003) Short-term and long-term survival of new neurons in the rat dentate gyrus. J Comp Neurol 460:563-572.
54. Kuhn HG, et al. (2005) Increased generation of granule cells in adult Bcl-2-overexpressing mice: A role for cell death during continued hippocampal neurogenesis. Eur J Neurosci 22:1907-1915.
55. Mickley GA, Ferguson JL, Mulvihill MA, Nemeth TJ (1989) Progressive behavioral changes during the maturation of rats with early radiation-induced hypoplasia of fascia dentata granule cells. Neurotoxicol Teratol 11:385-393.
56. Mickley GA, Ferguson JL, Nemeth TJ, Mulvihill MA, Alderks CE (1989) Spontaneous perseverative turning in rats with radiation-induced hippocampal damage. Behav Neurosci 103:722-730.
57. Meshi D, et al. (2006) Hippocampal neurogenesis is not required for behavioral effects of environmental enrichment. Nat Neurosci 9:729-731.
58. Highfield DA, Hu D, Amsel A (1998) Alleviation of x-irradiation-based deficit in memory-based learning by D-amphetamine: Suggestions for attention deficit-hyperactivity disorder. Proc Natl Acad Sci USA 95:5785-5788.
59. Mickley GA, Ferguson JL, Nemeth TJ (1992) Serial injections of MK 801 (dizocilpine) in neonatal rats reduce behavioral deficits associated with x-ray-induced hippocampal granule cell hypoplasia. Pharmacol Biochem Behav 43:785-793.
60. Roman DD, Sperduto PW (1995) Neuropsychological effects of cranial radiation: Current knowledge and future directions. Int J Radiat Oncol Biol Phys 31:983-998.
61. Mulhern RK, Merchant TE, Gajjar A, Reddick WE, Kun LE (2004) Late neurocognitive sequelae in survivors of brain tumours in childhood. Lancet Oncol 5:399-408.
62. Nilsson M, Markinhuhta KR, Carlsson ML (2006) Differential effects of classical neuroleptics and a newer generation antipsychotics on the MK-801-induced behavioural primitivization in mouse. Prog Neuropsychopharmacol Biol Psychiatry 30:521-530.