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International Journal of Radiation Biology Volume 77, 2001 - Issue 5
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Research Article

Neuron loss during early adulthood following prenatal low-dose X-irradiation in the mouse brain

H. Korr, H. Thorsten Rohde, J. Benders, M. Dafotakis, N. Grolms, C. Schmitz RWTH University of Aachen, Department of Anatomy and Cell Biology, Pauwelsstrasse/Wendlingweg 2, D-52057 Aachen, Germany
Pages 567-580 | Published online: 03 Jul 2009

  • AHMAD, A. and SPEAR, P. D., 1993, Effects of aging on the size, density, and number of rhesus monkey lateral geniculate neurons. Journal of Comparative Neurology, 334, 631-643.
  • AMES, B. N., SHIGENAGA, M. K. and HAGEN, T. M., 1993, Oxidants, antioxidants, and the degenerative diseases of aging. Proceedings of the National Academy of Sciences of the United States of America, 90, 7915-7922.
  • ANSON, R. M. and BOHR, V. A., 1999, Gene-specific and mitochondrial repair of oxidative DNA damage. Methods in Molecular Biology, 113, 257-279.
  • ASPINWALL, R., ROTOWELL, D. G., ROLDAN-ARJONA, T., ANSELMINO, C., WARD, C. J., CHEADLE, J. P., SAMPSON, J. R., LINDAHL, T., HARRIS, P. C. and HICKSON, I. D., 1997, Cloning and characterization of a functional human homolog of Escherichia coli endonuclease III. Proceedings of the National Academy of Sciences of the United States of America, 94, 109-114.
  • ASHWELL, M. and WORK, T. S., 1970, The biogenesis of mitochondria. Annual Review of Biochemistry, 39, 251-290.
  • BAKALIAN, A., DELHAYE-BOUCHAUD, N. and MARIANI, J., 1995, Quantitative analysis of the Purkinje cell and the granule cell populations in the cerebellum of the nude mice. Journal of Neurogenetics, 9, 207-218.
  • BANDY, B. and DAVISON, A. J., 1990, Mitochondrial mutations may increase oxidative stress: implications for carcinogenesis and aging? Free Radical Biology and Medicine, 8, 523-539.
  • BOHR, V. A. and HANAWALT, P. C., 1988, DNA repair in genes. Pharmacology and Therapeutics, 38, 305-319.
  • Boss, B. D., TURLEJSKI, K., STANHELD, B. B. and COWAN, W. M., 1987, On the numbers of neurons in fields CAl and CA3 of the hippocampus of Sprague-Dawley and Wistar rats. Brain Research, 406, 280-287.
  • BRENT, R. L., 1980, Radiation teratogenesis. Teratology, 21, 281-298.
  • BRIZZEE, K. R., ORDY, J. M., KAACK, M. B. and BEAVERS, T., 1980, Effect of prenatal ionizing radiation on the visual cortex and hippocampus of newborn squirrel monkeys. Journal of Neuropathology and Experimental Neurology, 39, 523-540.
  • BRUNI, J. E., PERSAUD, T. V. N., HUANG, W. and FROESE, G., 1993, Postnatal development of the rat CNS following in utero exposure to a low dose of ionizing radiation. Experimental and Toxicologie Pathology, 45, 223-231.
  • BUNCH, R. T., GEWIRTZ, D. A. and POVIRK, L. F., 1995, Ionizing radiation-induced DNA strand breakage and rejoining in specific genomic regions as determined by an alkaline unwinding/Southern blotting method. International Journal of Radiation Biology, 68, 553-562.
  • CAVALIERI, B., 1635, Geometria Indivisiblibus Continuorum. Bononiae: Typis Clementis Ferronij (reprinted 1966 as Geometria Degli Indivisibili. Torino: Unione Tipografico-Editrice Torinese).
  • CLAYTON, D. A., 1982, Replication of animal mitochondrial DNA. Cell, 28, 693-705.
  • CROTEAU, D. L., RHYS, C. M., HUDSON, E. K., DIANOV, G. L., HANSFORD, R. G. and BOHR, V. A., 1997, An oxidative damage-specific endonuclease from rat liver mitochondria. Journal of Biological Chemistry, 272, 27338-27344.
  • DE GREY, A. D. N. J., 1997, A proposed refinement of the mitochondrial free radical theory of aging. Bioessays, 19, 161-166.
  • DIKOMEY, E. and FRANZKE, J., 1986a, DNA repair kinetics after exposure to X-irradiation and to internal ß-rays in CHO cells. Radiation and Environmental Biophysics, 25, 189-194.
  • DIKOMEY, E. and FRANZKE, J., 1986b, Three classes of DNA strand breaks induced by X-irradiation and internal ß-rays. International Journal of Radiation Biology, 50, 893-908.
  • ESPOSITO, L. A., MELOV, S., PANOV, A., COTTRELL, B. A. and WALLACE, D. C., 1999, Mitochondrial disease in mouse results in increased oxidative stress. Proceedings of the National Academy of Sciences of the United States of America, 96, 4820-4825.
  • FERRER, I., 1993, Experimentally induced cortical malformations in rats. Childs Nervous System, 9, 403-407.
  • FLOR-HENRY, P., 1983, Cerebral Basis of Psychopathology (Boston: John Wright, PSG Inc.).
  • GILMORE, E. C., NOWAKOWSI, R. S., CAVINESS, V. S. and HERRUP, K., 2000, Cell birth, cell death, cell diversity and DNA breaks: how do they all fit together? Trends in Neurosciences, 23, 100-105.
  • GIUFFRIDA, A. M., GADALETA, M. N., SERRA, I., REMIS, M., GEREMIA, E., DEL PRETE, G. and SACCONE, C., 1979, Mitochondrial DNA, RNA and protein synthesis in different regions of developing rat brain. Naurochemical Research, 4, 37-52.
  • GOODHEAD, D. T., 1994, Initial events in the cellular effects of ionizing radiations: clustered damage in DNA. International Journal of Radiation Biology, 65, 7-17.
  • GROSS, N. J., GETZ, G. S. and RABINOWITZ, M., 1969, Apparent turnover of mitochondrial deoxyribonucleic acid and mitochondrial phospholipids in the tissues of the rat. Journal of Biological Chemistry, 244, 1552-1562.
  • GRUZELIER, J. H. and HAMMOND, N., 1976, Schizophrenia: a dominant hemisphere temporal-limbic disorder? Research Communications in Psychology, Psychiatry and Behavior, 1, 33-72.
  • GUNDERSEN, H. J. G., 1986, Stereology of arbitrary particles. Journal of Microscopy, 143, 3-45.
  • GUNDERSEN, H. J. G. and JENSEN, E. B., 1987, The efficiency of systematic sampling in Stereology and its prediction. Journal of Microscopy, 147, 229-263.
  • GUR, R. E., 1978, Left hemisphere dysfunction and left hemisphere overactivation in schizophrenia. Journal of Abnormal Psychology, 2, 226-238.
  • HEINSEN, H. and HEINSEN, Y. L., 1991, Serial thick, frozen, gallocyanin stained sections of human central nervous system. Journal of Histotechnology, 14, 167-173.
  • HEINSEN, H., RÜB, U., BAUER, M., ULMAR, G., BETHKE, B., SCHÜLER, M., BÖCKER, F., EISENMENGER, W., GÖTZ, M., KORR, H. and SCHMITZ, C., 1999. Nerve cell loss in the thalamic mediodorsal nucleus in Huntington's disease. Acta Neuropathologica, 97, 613-622.
  • HERGUIDO, M. J., CARCELLER, F., RODA, J. M. and AVENDANO, C., 1999, Hippocampal cell loss in transient global cerebral ischemia in rats: a critical assessment. Neuroscience, 93, 71-80.
  • HlCKS, S. P. and D'AMATO, C. J., 1966, Effects of ionizing radiation on mammalian development. In Advances in Teratology, edited by D. H. M. Woollam (London: Logos Press), pp. 195-243.
  • HOSHIND, K. and KAMEYAMA, Y., 1988, Developmental-stage-dependent radiosensitivity of neural cells in the ventricular zone of telencephalon in mouse and rat fetuses. Teratology, 37, 257-262.
  • HULTCRANTZ, M., ANNIKO, M. and BORG, E., 1989, The influence of prenatal gamma irradiation on the ageing of the cochlea. Acta Otolaryngologica, 108, 414-423.
  • INSAUSTI, A. M., MEGIAS, M., CRESPO, D., CRUZ-ORIVE, L. M., DIERSSEN, M., VALLINA, I. F., INSAUSTI, R., FLOREZ, J. and VALLINA, T. F., 1998, Hippocampal volume and neuronal number in Ts65Dn mice: a murine model of Down syndrome. Neuroscience Letters, 253, 175-178.
  • KAMEYAMA, Y., HOSHINO, K. and HAYASHI, Y., 1978, Effects of low-dose X-radiation on the matrix cells in the telencephalon of mouse embryos. In Developmental Toxicology of Energy-related Pollutants, edited by D. D. Mahlum, M. R. Sikow, P. L. Hackett and F. D. Andrew (Oak Ridge: US DOE Technical Information Center), pp. 228-236.
  • KlMLER, B. F., 1998, Prenatal irradiation: a major concern for the developing brain. International Journal of Radiation Biology, 73, 423-434.
  • KIMLER, B. F. and NORTON, S., 1988, Behavioral changes and structural defects in rats irradiated in utero. International Journal of Radiation Oncology, Biology, Physics, 15,1171 -1177.
  • KONERMANN, G., 1989, Postnatal brain maturation damage induced by prenatal irradiation: modes of effect manifestations and dose--response relations. In Low Dose Radiation: Biological Basis of Risk Assessment, edited by K. F. Baverstock and J. W. Slather (London: Taylor & Francis), pp. 364-376.
  • KORR, H., BAUER, K., BUNZECK, A. S., NACKEN, M. and KARBACH, F. T., 1997b, Correction factors of 3H-ß-self-absorption for quantitative autoradiography of different cell types in the brain of pre- and postnatal mice. Histochemistry and Cell Biololgy, 108, 537-541.
  • KORR, H., KOESER, S., OLDENKOTT, S., SCHMIDT, H. and SCHULTZE, B., 1989, X-ray dose-effect relationship on unscheduled DNA synthesis and spontaneous unscheduled DNA synthesis in mouse brain cells studied in moo. Radiation and Environmental Biophysics, 28, 13-26.
  • KORR, H., KURZ, C., SEIDLER, T. O., SOMMER, D. and SCHMITZ, C., 1998, Mitochondrial DNA synthesis studied autoradiographically in various cell types in moo. Brazilian Journal of Medical and Biological Research, 31, 289-298.
  • KORR, H., PHILIPPI, V., HELG, C., SCHIEFER, J., GRABBER, M. B. and KREUTZBERG, G. W., 1997a, Unscheduled DNA synthesis and mitochondrial DNA synthetic rate following injuring of the facial nerve. Acta Neuropathologica, 94, 557-566.
  • KORR, H. and SCHMIDT, H., 1988, An improved procedure for background correction in autoradiography. Histochemistry, 88, 407-410.
  • KOWALD, A., 1999, The mitochondrial theory of aging: do damaged mitochondria accumulate by delayed degradation? Experimental Gerontology, 34, 605-612.
  • KOWALD, A. and KIRKWOOD, T. B., 1996, A network theory of ageing: the interactions of defective mitochondria, aberrant proteins, free radicals and scavengers in the ageing process. Mutation Research, 316, 209-236.
  • KOWALD, A. and KIRKWOOD, T. B., 2000, Accumulation of defective mitochondria through delayed degradation of damaged organelles and its possible role in the ageing of post-mitotic and dividing cells. Journal of Theoretical Biology, 202, 145-160.
  • LAENG, H., SCHNEIDER, R., BOLLI, A., ZIMMERMANN, T., SCHAFFNER, R. and SCHINDLER, R., 1988, Participation of mitochondrial proliferation in morphological differentiation of murine mastocytoma cells. Experimental Cell Research, 179, 222-232.
  • LEE, H. C., YIN, P. H., Lu, C. Y., CHI, C. W. and WEI, Y. H., 2000, Increase of mitochondria and mitochondrial DNA in response to oxidative stress in human cells. Biochemical Journal, 348, 425-432.
  • LIEBERMAN, J. A., 1999, Is schizophrenia a neurodegenerative disorder? A clinical and neurobiological perspective. Biological Psychiatry, 46, 729-739.
  • LJUNGMAN, M., 1999, Repair of radiation-induced DNA strand breaks does not occur preferentially in transcriptionally active DNA. Radiation Research, 152, 444-449.
  • LOHR, J. B., 1991, Oxygen radicals and neuropsychiatrie illness. Some speculations. Archives of General Psychiatry, 48, 1097-1106.
  • LONGLEY, M. J., PRASAD, R., SRIVASTAVA, D. K., WILSON, S. H. and COPELAND, W. C., 1998, Identification of 5'-deoxyribose phosphate lyase activity in human DNA polymerase gamma and its role in mitochondrial base excision repair in vitro. Proceedings of the National Academy of Sciences of the United States of America, 95, 12244-12248.
  • MAEHARA, Y., ANAI, H., KUSUMOTO, T., SAKAGUCHI, Y. and SUGIMACHI, K., 1989, Nick translation detection in situ of cellular DNA strand break induced by radiation. American Journal of Pathology, 134, 7-10.
  • MARGOLIS, R. L., CHUANG, D. M. and POST, R. M., 1994, Programmed cell death: implications for neuropsychiatrie disorders. Biological Psychiatry, 35, 946-956.
  • MARTIN, L. J., SIEBER, F. E. and TRAYSTMAN, R. J., 2000, Apoptosis and necrosis occur in separate neuronal populations in hippocampus and cerebellum after ischemia and are associated with differential alterations in metabotropic glutamate receptor signaling pathways. Journal of Cerebral Blood Flow and Metabolism, 20, 153-167.
  • MAY, A. and BOHR, V. A., 2000, Gene-specific repair of gamma-ray-induced DNA strand breaks in colon cancer cells: no coupling to transcription and no removal from the mitochondrial genome. Biochemical and Biophysical Research Communications, 269, 433-437.
  • MELOV, S., SCHNEIDER, J. A., COSKUN, P. E., BENNETT, D. A. and WALLACE, D. C., 1999, Mitochondrial DNA rearrangements in aging human brain and in situ PCR of mtDNA. Neurobiology of Aging, 20, 565-571.
  • MENZIES, R. A. and GOLD, P. H., 1971, The turnover of mitochondria in a variety of tissues of young adult and aged rats. Journal of Biological Chemistry, 246, 2425-2429.
  • MIKI, T., SAWADA, K., SUN, X. Z., HISANO, S., TAKEUCHI, Y. and FUKUI, Y., 1999, Abnormal distribution of hippocampal mossy fibers in rats exposed to X-irradiation in utero. Developmental Brain Research, 112, 275-280.
  • MITRA, S., HAZRA, T. K., ROY, R., IKEDA, S., BISWAS, T., LOCK, J., BOLDOGH, I. and IZUMI, T., 1997, Complexities of DNA base excision repair in mammalian cells. Molecules and Cells, 7, 305-312.
  • MORALES, A., MIRANDA, M., SANCHEZ-REYES, A., BIETE, A. and FERNANDEZ-CHECA, J. C., 1998, Oxidative damage of mitochondrial and nuclear DNA induced by ionizing radiation in human hepatoblastoma cells. International Journal of Radiation Oncology, Biology, Physics, 42, 191-203.
  • NORTON, S., 1979, Development of rat telencephalic neurons after prenatal x-irradiation. Journal of Environmental Science and Health, 13, 121-134.
  • NORTON, S. and KIMLER, B. F., 1988, Comparison of functional and morphological deficits in the rat after gestational exposure to ionizing radiation. Neurotoxicolcy and Teratology, 10, 363-371.
  • NYAGU, A. I., LOGANOVSKY, K. N. and LOGANOVSKAJA, T. K., 1998, Psychophysiologic after effects of prenatal irradiation. International Journal of Psychophysiology, 30, 303-311.
  • PLOSKONOSOVA, 1.1., BARANOV, V. I. and GAZIEV, A. I., 1999a, PCR assay of DNA damage and repair at the gene level in brain and spleen of ?-irradiated young and old rats. Mutation Research, 434, 109-117.
  • PLOSKONOSOVA, 1.1., BARANOV, V. I. and GAZIEV, A. L, 1999b, Estimation of DNA damage and repair in tissues of ?-irradiated animals using the polymerase chain reaction. Biochemistry (Moscow), 64, 1320-1325.
  • REYNERS, H., GIANFELICI DE REYNERS, E., POORTMANS, F., CRAMETZ, A., COFFIGNY, H. and MAISIN, J.-R., 1992, Brain atrophy after foetal exposure to very low doses of ionizing radiation. International Journal of Radiation Biology, 62, 619-626.
  • SADOWSKI, M., WISMEWSKI, H. M., JAKUBOWSKA-SADOWSKA, K., TARNAWSKI, M., LAZAREWICZ, J. W. and MOSSAKOWSKI, M. J., 1999, Pattern of neuronal loss in the rat hippocampus following experimental cardiac arrest-induced ischemia. Journal of the Neurological Sciences, 168, 13-20.
  • SAMBROOK, J., FRITSCH, E. F. and MANIATIS, T., 1989, Molecular Cloning. A Laboratory Manual, 2nd edition (Cold Spring Harbor: Cold Spring Harbor Laboratory Press).
  • SANCAR, A., 1996, DNA excision repair. Annual Review of Biochemistry, 65, 43-81.
  • SCHMITZ, C., 1994, Spontane DNA-Reparatur-Syntheserate verschiedener Zellarten in Cortex und Hippocampus der Maus als Funktion des Lebensalters [MD thesis]. RWTH University of Aachen.
  • SCHMITZ, C., 1998, Variation of fractionator estimates and its prediction. Anatomy and Embryology, 198, 371-397.
  • SCHMITZ, C. and HOF, P. R., 2000, Recommendations for straightforward and rigorous methods of counting neurons based on a computer simulation approach. Journal of Chemical Neuroanatomy, 20, 93-114.
  • SCHMITZ, C., AXMACHER, B., ZUNKER, U. and KORR, H., 1999a, Age-related changes of DNA repair and mitochondrial DNA synthesis in the mouse brain. Acta Neuropathologica, 97, 71-81.
  • SCHMITZ, C., BÜLTMANN, E., CUBE, M. and KORR, H., 1999c, Neuron loss in the mouse hippocampus following prenatal injection of tritiated thymidine or saline. International Journal of Developmental Neuroscience, 17, 185-190.
  • SCHMITZ, C., HEINSEN, H. and KORR, H., 1999d, Design-based counting techniques: the real problems. Trends in Neurosciences, 22, 345.
  • SCHMITZ, C., MATERNE, S. and KORR, H., 1999b, Cell-type-specific differences in age-related changes of DNA repair in the mouse brain-molecular basis for a new approach to understand the selective neuronal vulnerability in Alzheimer's disease. Journal of Alzhcimer's Disease, 1, 387-407.
  • SCHMITZ, C., OTTO, U. and KORR, H., 2000, More cerebellar granule cells following prenatal low-dose X-irradiation. Brain Research, 872, 250-253.
  • SCHMITZ, C., RUB, U., KORR, H. and HEINSEN, H., 1999e, Nerve cell loss in the thalamic mediodorsal nucleus in Huntington's disease. II. Optimization of a stereological estimation procedure. Acta Neuropathologica, 97, 623-628.
  • SCHULTZE, B., RABBANI, B. and MAURER, W., 1972, Blood-brain-barrier and placental-barrier for different amino acids in the mouse. Beiträge zur Pathologie, 147, 352-365.
  • SCHWEITZER, D. J., BENJAMIN, S. A. and LEE, A. C., 1987, Retinal dysplasia and progressive atrophy in dogs irradiated during ocular development. Radiation Research, 111, 340-353.
  • SINGH, G., HAUSWIRTH, W. W., Ross, W. E. and NEIMS, A. H., 1985, A method for assessing damage to mitochondrial DNA caused by radiation and epichlorohydrin. Molecular Pharmacology, 27, 167-170.
  • STUMPF, W. E., SAR, M., ZUBER, T. J., SOINI, E. and TUOHIMAA, P., 1981, Quantitative assessment of steroid hormone binding sites by thaw-mount autoradiography. Journal of Histochemistry and Cytochemistry, 29 (1A Suppl), 201-206.
  • STURROCK, R. R., 1991, Stability of neuron number in the subthalamic and entopeduncular nuclei of the ageing mouse brain. Journal of Anatomy, 179, 67-73.
  • TAKAO, M., ABURATANI, H., KOBAYASHI, K. and YASUI, A., 1998, Mitochondria! targeting of human DNA glycosylases for repair of oxidative DNA damage. Nucleic Acids Research, 26, 2917-2922.
  • TANG, J. T., YAMAZAKI, H., INDUE, T., KOIZUMI, M., YOSHIDA, K., OZEKI, S. and INDUE, T., 1999, MITOCHONDRIALDNA INFLUENCES RADIATION SENSITIVITY AND INDUCTIONOF APOPTOSIS IN HUMAN FIBROBLASTS. Anticancer Research, 19, 4959-4964.
  • TSUANG, M., 2000, Schizophrenia: genes and environment. Biological Psychiatry, 47, 210-220.
  • WALLACE, S. S., 1998, Enzymatic processing of radiation-induced free radical damage in DNA. Radiation Research, 150, S60-S79.
  • WANG, H., HIATT, W., BARSTOW, T. J. and BRASS, E. P., 1999, Relationships between muscle mitochondrial DNA content, mitochondrial enzyme activity and oxidative capacity in man: alterations with disease. European Journal of Applied Physiology, 80, 22-27.
  • WANG, R. Y., HSU, T. C., BROCK, W. A. and LIANG, J., 1995, DNA fragility and repair capability are separate genetic phenotypes: studies on in situ nick translation and chromosome breakage. International Journal of Oncology, 6, 51-54.
  • WEI, Y. H., LU, C. Y., LEE, H. C., PANG, C. Y. and MA, Y. S., 1998, Oxidative damage and mutation to mitochondrial DNA and age-dependent decline of mitochondrial respiratory function. Annals of the New York Academy of Sciences, 854, 155-170.
  • WIESNER, R. J., HORNUNG, T. V., CARMAN, J. D., CLAYTON, D. A., O'GORMAN, E. and WALLIMANN, T., 1999, Stimulation of mitochondrial gene expression and proliferation of mitochondria following impairment of cellular energy transfer by inhibition of the phosphocreatine circuit in rat hearts. Journal of Bioenergetics and Biomembranes, 31, 559-567.
  • YAMAZAKI, J. N., 1966, 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, 877-903.
  • ZANJANI, H. S., VOGEL, M. W., DELHAYE-BOUCHAUD, N., MARTINOU, J. C. and MARIANI, J., 1996, Increased cerebellar Purkinje cell numbers in mice overexpressing a human Bcl-2 transgene. Journal of Comparative Neurology, 374, 332-341.

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