Effects of Lipopolysaccharide on 56Fe-Particle Radiation-Induced Impairment of Synaptic Plasticity in the Mouse Hippocampus

Abstract Vlkolinský, R., Krucker, T., Smith, A. L., Lamp, T. C., Nelson, G. A. and Obenaus, A. Effects of Lipopolysaccharide on 56Fe-Particle Radiation-Induced Impairment of Synaptic Plasticity in the Mouse Hippocampus. Radiat. Res. 168, 462–470 (2007). Space radiation, including high-mass, high-Z, high-energy particles (HZE; e.g. 56Fe), represents a significant health risk for astronauts, and the central nervous system (CNS) may be a vulnerable target. HZE-particle radiation may directly affect neuronal function, or during immunological challenge, it may alter immune system-to-CNS communication. To test these hypotheses, we exposed mice to accelerated iron particles (56Fe; 600 MeV/nucleon; 1, 2, 4 Gy; brain only) and 1 month later prepared hippocampal slices to measure the effects of radiation on neurotransmission and synaptic plasticity in CA1 neurons. In a model of immune system-to-CNS communication, these electrophysiological parameters were measured in irradiated mice additionally challenged with the peripheral immunological stressor lipopolysaccharide (LPS) injected intraperitoneally 4 h before the slice preparation. Exposure to 56Fe particles alone increased dendritic excitability and inhibited plasticity. In control mice (0 Gy), LPS treatment also inhibited synaptic plasticity. Paradoxically, in mice exposed to 2 Gy, the LPS treatment restored synaptic plasticity to levels similar to those found in controls (0 Gy, no LPS). Our results indicate that HZE-particle radiation alters normal electrophysiological properties of the CNS and the hippocampal response to LPS.

[1]  M. Pickering,et al.  Interleukin-18 mediated inhibition of LTP in the rat dentate gyrus is attenuated in the presence of mGluR antagonists , 2007, Neuroscience Letters.

[2]  G. Collingridge,et al.  Presynaptic mechanisms involved in the expression of STP and LTP at CA1 synapses in the hippocampus , 2007, Neuropharmacology.

[3]  Marco Durante,et al.  Cancer risk from exposure to galactic cosmic rays: implications for space exploration by human beings. , 2006, The Lancet. Oncology.

[4]  C. Biddle The neurobiology of the human febrile response. , 2006, AANA journal.

[5]  J. Wojtowicz Irradiation as an experimental tool in studies of adult neurogenesis , 2006, Hippocampus.

[6]  M. Pecaut,et al.  Acute Effects of Iron-Particle Radiation on Immunity. Part I: Population Distributions , 2006, Radiation research.

[7]  E. Miyamoto Molecular mechanism of neuronal plasticity: induction and maintenance of long-term potentiation in the hippocampus. , 2006, Journal of pharmacological sciences.

[8]  M. Pecaut,et al.  Acute Effects of Iron-Particle Radiation on Immunity. Part II: Leukocyte Activation, Cytokines and Adhesion , 2006, Radiation research.

[9]  R. Malinow,et al.  AMPA receptor phosphorylation during synaptic plasticity. , 2005, Biochemical Society transactions.

[10]  J. Fike,et al.  High-LET Radiation Induces Inflammation and Persistent Changes in Markers of Hippocampal Neurogenesis , 2005, Radiation research.

[11]  M. Danik,et al.  Chronic LPS exposure produces changes in intrinsic membrane properties and a sustained IL‐β‐dependent increase in GABAergic inhibition in hippocampal CA1 pyramidal neurons , 2005, Hippocampus.

[12]  D. Balschun,et al.  Interleukin‐6: a cytokine to forget , 2004, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[13]  M. Bear,et al.  LTP and LTD An Embarrassment of Riches , 2004, Neuron.

[14]  B. Bilgiç,et al.  Effects of lipopolysaccharide on the radiation-induced changes in the blood–brain barrier and the astrocytes , 2004, Brain Research.

[15]  Jacob Raber,et al.  Radiation-Induced Cognitive Impairments are Associated with Changes in Indicators of Hippocampal Neurogenesis , 2004, Radiation research.

[16]  G. Siggins,et al.  Acute exposure to CXC chemokine ligand 10, but not its chronic astroglial production, alters synaptic plasticity in mouse hippocampal slices , 2004, Journal of Neuroimmunology.

[17]  M. Lynch,et al.  Lipopolysaccharide‐induced increase in signalling in hippocampus is abrogated by IL‐10 – a role for IL‐1β? , 2004, Journal of neurochemistry.

[18]  Wickliffe C Abraham,et al.  Properties and Mechanisms of LTP Maintenance , 2003, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[19]  G. Nelson,et al.  Fundamental space radiobiology. , 2003, Gravitational and space biology bulletin : publication of the American Society for Gravitational and Space Biology.

[20]  Ashutosh Kumar Singh,et al.  Lipopolysaccharide (LPS) induced activation of the immune system in control rats and rats chronically exposed to a low level of the organothiophosphate insecticide, acephate , 2003, Toxicology and industrial health.

[21]  B. Shukitt-Hale,et al.  Long-term changes in amphetamine-induced reinforcement and aversion in rats following exposure to 56Fe particle. , 2003, Advances in space research : the official journal of the Committee on Space Research.

[22]  B. Shukitt-Hale,et al.  Cognitive deficits induced by 56Fe radiation exposure. , 2003, Advances in space research : the official journal of the Committee on Space Research.

[23]  B. Shukitt-Hale,et al.  Brain Signaling and Behavioral Responses Induced by Exposure to 56Fe-Particle Radiation , 2002, Radiation research.

[24]  B. Hauss-Wegrzyniak,et al.  Chronic Brain Inflammation Results in Cell Loss in the Entorhinal Cortex and Impaired LTP in Perforant Path-Granule Cell Synapses , 2002, Experimental Neurology.

[25]  W Budach,et al.  Radiation induced CNS toxicity – molecular and cellular mechanisms , 2001, British Journal of Cancer.

[26]  C. Culmsee,et al.  Adaptive Plasticity in Tachykinin and Tachykinin Receptor Expression after Focal Cerebral Ischemia Is Differentially Linked to GABAergic and Glutamatergic Cerebrocortical Circuits and Cerebrovenular Endothelium , 2001, The Journal of Neuroscience.

[27]  Eleanor A. Blakely,et al.  Biological Effects of Cosmic Radiation: Deterministic and Stochastic , 2000, Health physics.

[28]  C. Pavlides,et al.  Long-term potentiation/depotentiation are accompanied by complex changes in spontaneous unit activity in the hippocampus. , 2000, Journal of neurophysiology.

[29]  M. Lynch,et al.  Lipopolysaccharide Inhibits Long Term Potentiation in the Rat Dentate Gyrus by Activating Caspase-1* , 2000, The Journal of Biological Chemistry.

[30]  B. Shukitt-Hale,et al.  Spatial Learning and Memory Deficits Induced by Exposure to Iron-56-Particle Radiation , 2000, Radiation research.

[31]  B. Shukitt-Hale,et al.  Effects of exposure to heavy particles on a behavior mediated by the dopaminergic system. , 2000, Advances in space research : the official journal of the Committee on Space Research.

[32]  S. Akhondzadeh Hippocampal synaptic plasticity and cognition , 1999, Journal of clinical pharmacy and therapeutics.

[33]  L. Mucke,et al.  Transgenic mice with cerebral expression of human immunodeficiency virus type-1 coat protein gp120 show divergent changes in short- and long-term potentiation in CA1 hippocampus , 1998, Neuroscience.

[34]  P. Schulz,et al.  Differing mechanisms of expression for short- and long-term potentiation. , 1997, Journal of neurophysiology.

[35]  J. J. O'Connor,et al.  Interleukin-1β (IL-1β) and tumour necrosis factor (TNF) inhibit long-term potentiation in the rat dentate gyrus in vitro , 1996, Neuroscience Letters.

[36]  M. Lynch,et al.  Interleukin-1 beta (IL-1 beta) and tumour necrosis factor (TNF) inhibit long-term potentiation in the rat dentate gyrus in vitro. , 1996, Neuroscience letters.

[37]  Steven F. Maier,et al.  Immune activation: the role of pro-inflammatory cytokines in inflammation, illness responses and pathological pain states , 1995, Pain.

[38]  G. Siggins,et al.  Reduced long-term potentiation in the dentate gyrus of transgenic mice with cerebral overexpression of interleukin-6 , 1995, Neuroscience Letters.

[39]  M. T. Brewer,et al.  Mechanisms of tumor necrosis factor-α (TNF-α) hyperalgesia , 1995, Brain Research.

[40]  S. Maier,et al.  Blockade of cytokine induced conditioned taste aversion by subdiaphragmatic vagotomy: further evidence for vagal mediation of immune-brain communication , 1995, Neuroscience Letters.

[41]  Steven F. Maier,et al.  Blockade of interleukin-1 induced hyperthermia by subdiaphragmatic vagotomy: evidence for vagal mediation of immune-brain communication , 1995, Neuroscience Letters.

[42]  M. Gilbert,et al.  Hippocampal Field Potentials: A Model System to Characterize Neurotoxicity , 1995 .

[43]  M. T. Brewer,et al.  Mechanisms of tumor necrosis factor-alpha (TNF-alpha) hyperalgesia. , 1995, Brain research.

[44]  R. Dantzer,et al.  Peripheral administration of lipopolysaccharide induces the expression of cytokine transcripts in the brain and pituitary of mice. , 1994, Brain research. Molecular brain research.

[45]  J. Joseph,et al.  Behavioral endpoints for radiation injury. , 1994, Advances in space research : the official journal of the Committee on Space Research.

[46]  G. Siggins,et al.  Interleukin 1β inhibits synaptic strength and long-term potentiation in the rat CA1 hippocampus , 1993, Brain Research.

[47]  T. Pellmar,et al.  Gamma radiation (5-10 Gy) impairs neuronal function in the guinea pig hippocampus. , 1993, Radiation research.

[48]  E. D. De Souza,et al.  Reciprocal modulation of interleukin-1 beta (IL-1 beta) and IL-1 receptors by lipopolysaccharide (endotoxin) treatment in the mouse brain-endocrine-immune axis. , 1993, Endocrinology.

[49]  G. Zeman,et al.  Time- and dose-dependent changes in neuronal activity produced by X radiation in brain slices. , 1990, Radiation research.

[50]  T. Pellmar,et al.  Ionizing radiation alters neuronal excitability in hippocampal slices of the guinea pig. , 1987, Radiation research.

[51]  D. Philpott,et al.  The effect of high energy (HZE) particle radiation (40Ar) on aging parameters of mouse hippocampus and retina. , 1985, Scanning electron microscopy.

[52]  I. C. Wiseman An Embarrassment of Riches or a Richness of Embarrassments. , 1984 .

[53]  J. Miquel,et al.  Ultrastructural findings in the brain of fruit flies (Drosophila melanogaster) and mice exposed to high-energy particle radiation. , 1984, Scanning electron microscopy.

[54]  T. Teyler,et al.  Long-term and short-term plasticity in the CA1, CA3, and dentate regions of the rat hippocampal slice , 1976, Brain Research.