Prenatal protracted irradiation at very low dose rate induces severe neuronal loss in rat hippocampus and cerebellum

Neuroscience

Volumn 130, Issue 4, 2005, Pages 935-948

  Schmitz, C ^a,b,c   Born, M ^b   Dolezel, P ^b   Rutten, B P F ^a,b,c   De Saint Georges, L ^d   Hof, P R ^e   Korr, H ^b,c  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b RWTH AACHEN UNIVERSITY   (Germany)

^c European Graduate School of Neuroscience   (Netherlands)

^d BELGIAN NUCLEAR RESEARCH CENTRE   (Belgium)

^e MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

brain; development; prenatal low dose irradiation; stereology

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CELL DENSITY; CELL LOSS; CELL STRUCTURE; CELL SUBPOPULATION; CEREBELLUM; CONTROLLED STUDY; EXPERIMENTAL DESIGN; FEMALE; GAMMA IRRADIATION; GRANULE CELL; HIPPOCAMPUS; INTERMETHOD COMPARISON; MALE; NERVE CELL; NONHUMAN; PRENATAL PERIOD; PRIORITY JOURNAL; PROGENY; PURKINJE CELL; PYRAMIDAL NERVE CELL; RADIATION DOSE; RADIATION INJURY; RANDOMIZATION; RAT; STATISTICAL SIGNIFICANCE; STEREOLOGY;

ANIMALS; CELL COUNT; CELL DEATH; CEREBELLUM; FEMALE; GAMMA RAYS; HIPPOCAMPUS; MALE; NERVE DEGENERATION; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PURKINJE CELLS; PYRAMIDAL CELLS; RADIATION DOSAGE; RATS; RATS, WISTAR;

EID: 11844287572     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2004.08.034     Document Type: Article

References (93)

1. A. Ahmad, P.D. Spear Effects of aging on the size, density, and number of rhesus monkey lateral geniculate neurons J Comp Neurol 334 1993 631 643
2. J. Alder, N.K. Cho, M.E. Hatten Embryonic precursor cells from the rhombic lip are specified to a cerebellar granule neuron identity Neuron 17 1996 389 399
3. J. Alder, K.J. Lee, T.M. Jessell, M.E. Hatten Generation of cerebellar granule neurons in vivo by transplantation of BMP-treated neural progenitor cells Nat Neurosci 2 1999 535 540
4. J. Altman Postnatal development of the cerebellar cortex in the rat. 3: Maturation of the components of the granular layer J Comp Neurol 145 1972 465 513
5. J. Altman, G.D. Das Post-natal origin of microneurones in the rat brain Nature 207 1965 953 956
6. J. Altman, S.A. Bayer Prenatal development of the cerebellar system in the rat. I: Cytogenesis and histogenesis of the deep nuclei and the cortex of the cerebellum J Comp Neurol 179 1978 23 48
7. D.E. Barnes, D.W. Walker Prenatal ethanol exposure permanently reduces the number of pyramidal neurons in rat hippocampus Brain Res 227 1981 333 340
8. S.A. Bayer Development of the hippocampal region in the rat. I: Neurogenesis examined with 3H-thymidine autoradiography J Comp Neurol 190 1980 87 114
9. A. Benekou, S. Bolaris, E. Kazanis, E. Bozas, H. Philippidis, F. Stylianopoulou In utero radiation-induced changes in growth factor levels in the developing rat brain Int J Radiat Biol 77 2001 83 93
10. S. Bolaris, E. Bozas, A. Benekou, H. Philippidis, F. Stylianopoulou In utero radiation-induced apoptosis and p53 gene expression in the developing rat brain Int J Radiat Biol 77 2001 71 81
11. B.D. Boss, G.M. Peterson, W.M. Cowan On the number of neurons in the dentate gyrus of the rat Brain Res 338 1985 144 150
12. B.D. Boss, K. Turlejski, B.B. Stanfield, W.M. Cowan On the numbers of neurons in fields CA1 and CA3 of the hippocampus of Sprague-Dawley and Wistar rats Brain Res 406 1987 280 287
13. D.J. Brenner, R. Doll, D.T. Goodhead, E.J. Hall, C.E. Land, J.B. Little, J.H. Lubin, D.L. Preston, R.J. Preston, J.S. Puskin, E. Ron, R.K. Sachs, J.M. Samet, R.B. Setlow, M. Zaider Cancer risks attributable to low doses of ionizing radiation assessing what we really know Proc Natl Acad Sci USA 100 2003 13761 13766
14. R.L. Brent The response of the 9 and one-half-day-old-rat embryo to variations in exposure rate of 150 R x-irradiation Radiat Res 45 1971 127 136
15. K.R. Brizzee Effects of single and fractionated doses of total body X-irradiation in utero on growth of the brain and its parts Nature 202 1964 262 264
16. K.R. Brizzee, L.A. Jacobs, X. Kharetchki Effects of total body x-irradiation in utero on early postnatal changes in neuron volumetric relationships and packing density in cerebral cortex Radiat Res 14 1961 96 103
17. K.R. Brizzee, L.A. Jacobs, C.J. Bench Histologic effects of total-body x-irradiation in various dose fractionation patterns on fetal cerebral hemisphere Radiat Res 31 1967 415 429
18. J.E. Bruni, T.V.N. Persaud, W. Huang, G. Froese Postnatal development of the rat CNS following in utero exposure to a low dose of ionizing radiation Exp Toxicol Pathol 45 1993 223 231
19. D.F. Cahill, C.L. Yuile Tritium some effects of continuous exposure in utero on mammalian development Radiat Res 44 1970 727 737
20. B.A. Carnes, N. Gavrilova, D. Grahn Pathology effects at radiation doses below those causing increased mortality Radiat Res 158 2002 187 194
21. B. Cavalieri Geometria indivisibilibus continuorum Bononiae Typis Clementis Ferronij 1635 (reprinted 1966 as Geometria Degli Indivisibilii. Torino: Unione Tipografico-Editrice Torinese).
22. D. Charytoniuk, B. Porcel, J. Rodriguez Gomez, H. Faure, M. Ruat, E. Traiffort Sonic hedgehog signalling in the developing and adult brain J Physiol 96 2002 9 16
23. S. Chen, D.E. Hillman Regulation of granule cell number by a predetermined number of Purkinje cells in development Dev Brain Res 45 1989 137 147
24. Y. Cheng, I.B. Black, E. DiCicco-Bloom Hippocampal granule neuron production and population size are regulated by levels of bFGF Eur J Neurosci 15 2002 3 12
25. N. Dahmane, A. Ruiz-I-Altaba Sonic hedgehog regulates the growth and patterning of the cerebellum Development 126 1999 3089 3100
26. B. Djordjevic, W. Szybalski Genetics of human cell lines. III: Incorporation of 5-bromodeoxyuridine and 5-iododeoxyuridine into deoxyribonucleic acid of human cells and its effect on radiation sensitivity J Exp Med 112 1960 509 531
27. M. Doulazmi, F. Frederic, Y. Lemaigre-Dubreuil, N. Hadj-Sahraoui, N. Delhaye-Bouchaud, J. Mariani Cerebellar Purkinje cell loss during life span of the heterozygous staggerer mouse (Rora(+)/Rora(sg)) is gender-related J Comp Neurol 411 1999 267 273
28. I. Ferrer Experimentally induced cortical malformations in rats Childs Nerv Syst 9 1993 403 407
29. I. Ferrer, S. Alcantara, E. Marti A four-layered 'lissencephalic' cortex induced by prenatal X-irradiation in the rat Neuropathol Appl Neurobiol 19 1993 74 81
30. W.M. Gao, B. Wang, X.Y. Zhou Effects of prenatal low-dose beta radiation from tritiated water on learning and memory in rats and their possible mechanisms Radiat Res 152 1999 265 272
31. M. Garcia-Finana, L.M. Cruz-Orive, C.E. Mackay, B. Pakkenberg, N. Roberts Comparison of MR imaging against physical sectioning to estimate the volume of human cerebral compartments Neuroimage 18 2003 505 516
32. J. Glaser, E.M. Glaser Stereology, morphometry, and mapping the whole is greater than the sum of its parts J Chem Neuroanat 20 2000 115 126
33. D. Goldowitz, K. Hamre The cells and molecules that make a cerebellum Trends Neurosci 21 1998 375 382
34. H.J.G. Gundersen, E.B. Jensen The efficiency of systematic sampling in stereology and its prediction J Microsc 147 1987 229 263
35. O. Guntinas-Lichius, W.F. Neiss Comparison of empirical and estimated efficiency in neuron counting by the fractionator method and in volume measurement by Cavalieri's method Acta Stereol 15 1996 131 139
36. N. Hadj-Sahraoui, F. Frederic, H. Zanjani, K. Herrup, N. Delhaye-Bouchaud, J. Mariani Purkinje cell loss in heterozygous staggerer mutant mice during aging Dev Brain Res 98 1997 1 8
37. R.J. Harvey, R.M.A. Napper Quantitative study of granule and Purkinje cells in the cerebellar cortex of the rat J Comp Neurol 274 1988 151 157
38. R.B. Hawkins A microdosimetric-kinetic model for the sensitization of V79 cells to radiation by incorporation of bromodeoxyuridine Radiat Res 155 2001 698 702
39. S.P. Hicks, C.J. D'Amato Effects of ionizing radiation on mammalian development D.H.M. Woollam Advances in teratology 1966 Logos Press London 195 243
40. D.E. Hillman, S. Chen Vulnerability of cerebellar development in malnutrition. I: Quantitation of layer volume and neuron numbers Neuroscience 6 1981 1249 1262
41. K. Hoshino Histogenetic abnormalities of the brain caused by environmental factors sensitive period for microcephaly Cong Anom 23 1983 415 423
42. Y. Hyodo-Taguchi, S. Fushiki, C. Kinoshita, Y. Ishikawa, T. Hirobe Effects of continuous low-dose prenatal irradiation on neuronal migration in mouse cerebral cortex J Radiat Res 38 1997 87 94
43. G. Iliakis, S. Kurtzman, G. Pantelias, R. Okayasu Mechanism of radiosensitization by halogenated pyrimidines effect of BrdU on radiation induction of DNA and chromosome damage and its correlation with cell killing Radiat Res 119 1989 286 304
44. M. Inouye Cerebellar malformations in prenatally X-irradiated rats quantitative analysis and detailed description Teratology 20 1979 353 364
45. R.P. Jensh, L.M. Eisenman, R.L. Brent Postnatal neurophysiologic effects of prenatal X-irradiation Int J Radiat Biol 67 1995 217 227
46. Y. Kameyama Low-dose radiation as an environmental agent affecting intrauterine development Environ Med 26 1982 1 15
47. Y. Kameyama Factors in manifestation of developmental abnormalities of the central nervous system by environmental agents J Toxicol Sci 8 1983 91 103
48. B.F. Kimler Prenatal irradiation a major concern for the developing brain Int J Radiat Biol 73 1998 423 434
49. L. Korbo, B.B. Andersen, O. Ladefoged, A. Møller Total numbers of various cell types in rat cerebellar cortex estimated using an unbiased stereological method Brain Res 609 1993 262 268
50. H. Korr, H.T. Rohde, J. Benders, M. Dafotakis, N. Grolms, C. Schmitz Neuron loss during early adulthood following prenatal low-dose X-irradiation in the mouse brain Int J Radiat Biol 77 2001 567 580
51. K. Lai, B.K. Kaspar, F.H. Gage, D.V. Schaffer Sonic hedgehog regulates adult neural progenitor proliferation in vitro and in vivo Nat Neurosci 6 2003 21 27
52. J.O. Larsen, T. Tandrup, H. Braendgaard The volume of Purkinje cells decreases in the cerebellum of acrylamide-intoxicated rats, but no cells are lost Acta Neuropathol 88 1994 307 312
53. E.R. Lewis, C.W. Cotman Factors specifying the development of synapse number in the rat dentate gyrus effects of partial target loss Brain Res 191 1980 35 52
54. H.P. Li, T. Miki, H. Gu, I. Satriotomo, Y. Mastumoto, H. Kuma, D. Gonzalez, K.S. Bedi, H. Suwaki, Y. Takeuchi The effect of the timing of prenatal X-irradiation on Purkinje cell numbers in rat cerebellum Dev Brain Res 139 2002 159 166
55. R. Machold, S. Hayashi, M. Rutlin, M.D. Muzumdar, S. Nery, J.G. Corbin, A. Gritli-Linde, T. Dellovade, J.A. Porter, L.L. Rubin, H. Dudek, A.P. McMahon, G. Fishell Sonic hedgehog is required for progenitor cell maintenance in telencephalic stem cell niches Neuron 39 2003 937 950
56. J.H. Millonig, K.J. Millen, M.E. Hatten The mouse Dreher gene Lmx1a controls formation of the roof plate in the vertebrate CNS Nature 403 2000 720 721
57. S. Momosaki, X.Z. Sun, N. Takai, R. Hosoi, O. Inoue, S. Takahashi Changes in histological construction and decrease in 3H-QNB binding in the rat brain after prenatal X-irradiation J Radiat Res 43 2002 277 282
58. S. Norton Development of rat telencephalic neurons after prenatal X-irradiation J Environ Sci Health C 13 1979 121 134
59. T. Ohnishi, A. Takahashi, K. Ohnishi, M. Yonezawa Tumor suppressor p53 response is blunted by low-dose-rate radiation Phys Med 17 Suppl. 1 2001 215 216
60. T.A. Ralcewicz, T.V. Persaud Effects of prenatal exposure to low dose ionizing radiation on the development of the cerebellar cortex in the rat Histol Histopathol 10 1995 371 383
61. P.R. Rapp, M. Gallagher Preserved neuron number in the hippocampus of aged rats with spatial learning deficits Proc Natl Acad Sci USA 93 1996 9926 9930
62. T. Rasmussen, T. Schliemann, J.C. Sørensen, J. Zimmer, M.J. West Memory impaired aged rats no loss of principal hippocampal and subicular neurons Neurobiol Aging 17 1996 143 147
63. H. Reyners, E. Gianfelici de Reyners, F. Poortmans, A. Crametz, H. Coffigny, J.R. Maisin Brain atrophy after foetal exposure to very low doses of ionizing radiation Int J Radiat Biol 62 1992 619 626
64. B. Roozendaal, W.A. van Gool, D.F. Swaab, J.E. Hoogendijk, M. Mirmiran Changes in vasopressin cells of the rat suprachiasmatic nucleus with aging Brain Res 409 1987 259 264
65. B.P.F. Rutten, H. Korr, O.H.M. Gerlach, H. Oyen, H.W.M. Steinbusch, C. Schmitz The aging brain: less neurons could be better: the cerebellum Soc Neurosci Abstr 735 2003 16
66. J. Satorre, J. Cano, F. Reinoso-Suarez Stability of the neuronal population of the dorsal lateral geniculate nucleus (LGNd) of aged rats Brain Res 339 1985 375 377
67. A.R. Schlessinger, W.M. Cowan, D.I. Gottlieb An autoradiographic study of the time of origin and the pattern of granule cell migration in the dentate gyrus of the rat J Comp Neurol 159 1975 149 175
68. C. Schmitz Variation of fractionator estimates and its prediction Anat Embryol 198 1998 371 397
69. C. Schmitz, P.R. Hof Recommendations for straightforward and rigorous methods of counting neurons based on a computer simulation approach J Chem Neuroanat 20 2000 93 114
70. C. Schmitz, P.R. Hof Design-based stereology in neuroscience Neuroscience 2005 in press.
71. C. Schmitz, E. Bültmann, M. Gube, H. Korr Neuron loss in the mouse hippocampus following prenatal injection of tritiated thymidine or saline Int J Dev Neurosci 17 1999 185 190
72. C. Schmitz, M. Dafotakis, H. Heinsen, K. Mugrauer, A. Niesel, G.J. Popken, M. Stephan, W.D. Van de Berg, S. von Horsten, H. Korr Use of cryostat sections from snap-frozen nervous tissue for combining stereological estimates with histological, cellular, or molecular analyses on adjacent sections J Chem Neuroanat 20 2000 21 29
73. C. Schmitz, N. Grolms, P. Hof, R. Boehringer, J. Glaser, H. Korr Altered spatial arrangement of layer V pyramidal cells in the mouse brain following prenatal low-dose X-irradiation a stereological study using a novel three-dimensional analysis method to estimate the nearest neighbor distance distributions of cells in thick sections Cereb Cortex 12 2002 954 960
74. C. Schmitz, M.E. Rhodes, M. Bludau, S. Kaplan, P. Ong, I. Ueffing, J. Vehoff, H. Korr, C.A. Frye Depression reduced number of granule cells in the hippocampus of female, but not male, rats due to prenatal restraint stress Mol Psychiatry 7 2002 810 813
75. T.M. Seed, C. Inal, M.E. Dobson, S. Ghose, E. Hilyard, D. Tolle, T.E. Fritz Accommodative responses to chronic irradiation effects of dose, dose rate, and pharmacological response modifiers Mil Med 167 2 Suppl 2002 82 86
76. C. Streffer, R. Shore, G. Konermann, A. Meadows, P. Uma Devi, J. Preston Withers, L.E. Holm, J. Stather, K. Mabuchi Biological effects after prenatal irradiation (embryo and fetus) a report of the International Commission on Radiological Protection Ann ICRP 33 2003 5 206
77. R.R. Sturrock Changes in neuron number in the cerebellar cortex of the ageing mouse J Hirnforsch 30 1989 499 503
78. R.R. Sturrock Stability of neuron number in the subthalamic and entopeduncular nuclei of the ageing mouse brain J Anat 179 1991 67 73
79. X.Z. Sun, M. Inouye, S. Hayasaka, Y. Takagishi, H. Yamamura Effects of different doses of gamma-radiation on the developing brain of mice Environ Med 39 1995 113 116
80. X.Z. Sun, M. Inouye, H. Yamamura, Y. Fukui Effects of prenatal treatment with tritiated water on the developing brain in mouse Int J Radiat Biol 71 1997 309 313
81. G.M. Vidal-Pergola, B.F. Kimler, S. Norton Effect of in utero irradiation on the postnatal development, behavior, and brain structure of rats dose fractionation with a 6-h interval Radiat Res 134 1993 369 374
82. M.W. Vogel, K. Sunter, K. Herrup Numerical matching between granule and Purkinje cells in lurcher chimeric mice a hypothesis for the trophic rescue of granule cells from target-related cell death J Neurosci 9 1989 3454 3462
83. V.A. Wallace Purkinje-cell-derived sonic hedgehog regulates granule neuron precursor cell proliferation in the developing mouse cerebellum Curr Biol 9 1999 445 448
84. H. Wang, D. Chen, C. Gao, X. Zhou Effects of low level prenatal 60Co gamma-irradiation on postnatal growth and behavior in mice Teratology 48 1993 451 457
85. B. Wang, H. Takeda, W.M. Gao, X.Y. Zhou, T. Odaka, H. Ohyama, T. Yamada, I. Hayata Induction of apoptosis by beta radiation from tritium compounds in mouse embryonic brain cells Health Phys 77 1999 16 23
86. R.J. Wechsler-Reya, M.P. Scott Control of neuronal precursor proliferation in the cerebellum by sonic hedgehog Neuron 22 1999 103 114
87. M.J. West New stereological methods for counting neurons Neurobiol Aging 14 1993 275 285
88. M.J. West Stereological methods for estimating the total number of neurons and synapses issues of precision and bias Trends Neurosci 22 1999 51 61
89. M.J. West, L. Slomianka, H.J. Gundersen Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator Anat Rec 231 1991 482 497
90. R. Wetts, K. Herrup Direct correlation between Purkinje and granule cell number in the cerebella of lurcher chimeras and wild-type mice Brain Res 312 1983 41 47
91. R.E. Wimer, C.C. Wimer, J.E. Vaughn, R.P. Barber, B.A. Balvanz, C.R. Chernow The genetic organization of neuron number in Ammon's horns of house mice Brain Res 118 1976 219 243
92. T. Yabe, I. Samuels, J.P. Schwartz Bone morphogenetic proteins BMP-6 and BMP-7 have differential effects on survival and neurite outgrowth of cerebellar granule cell neurons J Neurosci Res 68 2002 161 168
93. J.N. Yamazaki A review of the literature on the radiation dosage required to cause manifest central nervous system disturbances from in utero and postnatal exposure Pediatrics 37 1966 877 903