Environmental lead exposure during early life alters granule cell neurogenesis and morphology in the hippocampus of young adult rats

Abstract Exposure to environmentally relevant levels of lead (Pb2+ ) during early life produces deficits in hippocampal synaptic plasticity in the form of long-term potentiation (LTP) and spatial learning in young adult rats [Nihei MK, Desmond NL, McGlothan JL, Kuhlmann AC, Guilarte TR (2000) N-meth...

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Veröffentlicht in:Neuroscience 2007-03, Vol.145 (3), p.1037-1047
Hauptverfasser: Verina, T, Rohde, C.A, Guilarte, T.R
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description Abstract Exposure to environmentally relevant levels of lead (Pb2+ ) during early life produces deficits in hippocampal synaptic plasticity in the form of long-term potentiation (LTP) and spatial learning in young adult rats [Nihei MK, Desmond NL, McGlothan JL, Kuhlmann AC, Guilarte TR (2000) N-methyl-D-aspartate receptor subunit changes are associated with lead-induced deficits of long-term potentiation and spatial learning. Neuroscience 99:233–242; Guilarte TR, Toscano CD, McGlothan JL, Weaver SA (2003) Environmental enrichment reverses cognitive and molecular deficits induced by developmental lead exposure. Ann Neurol 53:50–56]. Other evidence suggests that the performance of rats in the Morris water maze spatial learning tasks is associated with the level of granule cell neurogenesis in the dentate gyrus (DG) [ Drapeau E, Mayo W, Aurousseau C, Le Moal M, Piazza P-V, Abrous DN (2003) Spatial memory performance of aged rats in the water maze predicts level of hippocampal neurogenesis. Proc Natl Acad Sci U S A 100:14385–14390]. In this study, we examined whether continuous exposure to environmentally relevant levels of Pb2+ during early life altered granule cell neurogenesis and morphology in the rat hippocampus. Control and Pb2+ -exposed rats received bromodeoxyuridine (BrdU) injections (100 mg/kg; i.p.) for five consecutive days starting at postnatal day 45 and were killed either 1 day or 4 weeks after the last injection. The total number of newborn cells in the DG of Pb2+ -exposed rats was significantly decreased (13%; P
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Neuroscience 99:233–242; Guilarte TR, Toscano CD, McGlothan JL, Weaver SA (2003) Environmental enrichment reverses cognitive and molecular deficits induced by developmental lead exposure. Ann Neurol 53:50–56]. Other evidence suggests that the performance of rats in the Morris water maze spatial learning tasks is associated with the level of granule cell neurogenesis in the dentate gyrus (DG) [ Drapeau E, Mayo W, Aurousseau C, Le Moal M, Piazza P-V, Abrous DN (2003) Spatial memory performance of aged rats in the water maze predicts level of hippocampal neurogenesis. Proc Natl Acad Sci U S A 100:14385–14390]. In this study, we examined whether continuous exposure to environmentally relevant levels of Pb2+ during early life altered granule cell neurogenesis and morphology in the rat hippocampus. Control and Pb2+ -exposed rats received bromodeoxyuridine (BrdU) injections (100 mg/kg; i.p.) for five consecutive days starting at postnatal day 45 and were killed either 1 day or 4 weeks after the last injection. The total number of newborn cells in the DG of Pb2+ -exposed rats was significantly decreased (13%; P &lt;0.001) 1 day after BrdU injections relative to controls. Further, the survival of newborn cells in Pb2+ -exposed rats was significantly decreased by 22.7% ( P &lt;0.001) relative to control animals. Co-localization of BrdU with neuronal or astrocytic markers did not reveal a significant effect of Pb2+ exposure on cellular fate. In Pb2+ -exposed rats, immature granule cells immunolabeled with doublecortin (DCX) displayed aberrant dendritic morphology. That is, the overall length-density of the DCX-positive apical dendrites in the outer portion of the DG molecular layer was significantly reduced up to 36% in the suprapyramidal blade only. We also found that the area of Timm’s-positive staining representative of the mossy fibers terminal fields in the CA3 stratum oriens (SO) was reduced by 26% in Pb2+ -exposed rats. These findings demonstrate that exposure to environmentally relevant levels of Pb2+ during early life alters granule cell neurogenesis and morphology in the rat hippocampus. 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Psychology ; granule cell ; hippocampus ; Hippocampus - drug effects ; Hippocampus - growth &amp; development ; Lead Poisoning - physiopathology ; morphology ; Nerve Fibers - physiology ; neurogenesis ; Neurology ; Neurons - drug effects ; Neurons - physiology ; neurotoxicity ; Pb 2 ; Phenotype ; Rats ; Rats, Inbred Lew ; Vertebrates: nervous system and sense organs</subject><ispartof>Neuroscience, 2007-03, Vol.145 (3), p.1037-1047</ispartof><rights>IBRO</rights><rights>2006 IBRO</rights><rights>2007 INIST-CNRS</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c612t-a1371831f1228a736852434c8ba4f6daa4e758ff19d1cf8ff62a40e8ee5726af3</citedby><cites>FETCH-LOGICAL-c612t-a1371831f1228a736852434c8ba4f6daa4e758ff19d1cf8ff62a40e8ee5726af3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.neuroscience.2006.12.040$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&amp;idt=18674020$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/17276012$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Verina, T</creatorcontrib><creatorcontrib>Rohde, C.A</creatorcontrib><creatorcontrib>Guilarte, T.R</creatorcontrib><title>Environmental lead exposure during early life alters granule cell neurogenesis and morphology in the hippocampus of young adult rats</title><title>Neuroscience</title><addtitle>Neuroscience</addtitle><description>Abstract Exposure to environmentally relevant levels of lead (Pb2+ ) during early life produces deficits in hippocampal synaptic plasticity in the form of long-term potentiation (LTP) and spatial learning in young adult rats [Nihei MK, Desmond NL, McGlothan JL, Kuhlmann AC, Guilarte TR (2000) N-methyl-D-aspartate receptor subunit changes are associated with lead-induced deficits of long-term potentiation and spatial learning. Neuroscience 99:233–242; Guilarte TR, Toscano CD, McGlothan JL, Weaver SA (2003) Environmental enrichment reverses cognitive and molecular deficits induced by developmental lead exposure. Ann Neurol 53:50–56]. Other evidence suggests that the performance of rats in the Morris water maze spatial learning tasks is associated with the level of granule cell neurogenesis in the dentate gyrus (DG) [ Drapeau E, Mayo W, Aurousseau C, Le Moal M, Piazza P-V, Abrous DN (2003) Spatial memory performance of aged rats in the water maze predicts level of hippocampal neurogenesis. Proc Natl Acad Sci U S A 100:14385–14390]. In this study, we examined whether continuous exposure to environmentally relevant levels of Pb2+ during early life altered granule cell neurogenesis and morphology in the rat hippocampus. Control and Pb2+ -exposed rats received bromodeoxyuridine (BrdU) injections (100 mg/kg; i.p.) for five consecutive days starting at postnatal day 45 and were killed either 1 day or 4 weeks after the last injection. The total number of newborn cells in the DG of Pb2+ -exposed rats was significantly decreased (13%; P &lt;0.001) 1 day after BrdU injections relative to controls. Further, the survival of newborn cells in Pb2+ -exposed rats was significantly decreased by 22.7% ( P &lt;0.001) relative to control animals. Co-localization of BrdU with neuronal or astrocytic markers did not reveal a significant effect of Pb2+ exposure on cellular fate. In Pb2+ -exposed rats, immature granule cells immunolabeled with doublecortin (DCX) displayed aberrant dendritic morphology. That is, the overall length-density of the DCX-positive apical dendrites in the outer portion of the DG molecular layer was significantly reduced up to 36% in the suprapyramidal blade only. We also found that the area of Timm’s-positive staining representative of the mossy fibers terminal fields in the CA3 stratum oriens (SO) was reduced by 26% in Pb2+ -exposed rats. These findings demonstrate that exposure to environmentally relevant levels of Pb2+ during early life alters granule cell neurogenesis and morphology in the rat hippocampus. They provide a cellular and morphological basis for the deficits in synaptic plasticity and spatial learning documented in Pb2+ -exposed animals.</description><subject>Aging</subject><subject>Animals</subject><subject>Biological and medical sciences</subject><subject>Brain - drug effects</subject><subject>Brain - growth &amp; development</subject><subject>Brain - physiology</subject><subject>Bromodeoxyuridine - pharmacology</subject><subject>Environmental Exposure</subject><subject>Female</subject><subject>Fundamental and applied biological sciences. 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Psychology</topic><topic>granule cell</topic><topic>hippocampus</topic><topic>Hippocampus - drug effects</topic><topic>Hippocampus - growth &amp; development</topic><topic>Lead Poisoning - physiopathology</topic><topic>morphology</topic><topic>Nerve Fibers - physiology</topic><topic>neurogenesis</topic><topic>Neurology</topic><topic>Neurons - drug effects</topic><topic>Neurons - physiology</topic><topic>neurotoxicity</topic><topic>Pb 2</topic><topic>Phenotype</topic><topic>Rats</topic><topic>Rats, Inbred Lew</topic><topic>Vertebrates: nervous system and sense organs</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Verina, T</creatorcontrib><creatorcontrib>Rohde, C.A</creatorcontrib><creatorcontrib>Guilarte, T.R</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><jtitle>Neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Verina, T</au><au>Rohde, C.A</au><au>Guilarte, T.R</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Environmental lead exposure during early life alters granule cell neurogenesis and morphology in the hippocampus of young adult rats</atitle><jtitle>Neuroscience</jtitle><addtitle>Neuroscience</addtitle><date>2007-03-30</date><risdate>2007</risdate><volume>145</volume><issue>3</issue><spage>1037</spage><epage>1047</epage><pages>1037-1047</pages><issn>0306-4522</issn><eissn>1873-7544</eissn><coden>NRSCDN</coden><abstract>Abstract Exposure to environmentally relevant levels of lead (Pb2+ ) during early life produces deficits in hippocampal synaptic plasticity in the form of long-term potentiation (LTP) and spatial learning in young adult rats [Nihei MK, Desmond NL, McGlothan JL, Kuhlmann AC, Guilarte TR (2000) N-methyl-D-aspartate receptor subunit changes are associated with lead-induced deficits of long-term potentiation and spatial learning. Neuroscience 99:233–242; Guilarte TR, Toscano CD, McGlothan JL, Weaver SA (2003) Environmental enrichment reverses cognitive and molecular deficits induced by developmental lead exposure. Ann Neurol 53:50–56]. Other evidence suggests that the performance of rats in the Morris water maze spatial learning tasks is associated with the level of granule cell neurogenesis in the dentate gyrus (DG) [ Drapeau E, Mayo W, Aurousseau C, Le Moal M, Piazza P-V, Abrous DN (2003) Spatial memory performance of aged rats in the water maze predicts level of hippocampal neurogenesis. Proc Natl Acad Sci U S A 100:14385–14390]. In this study, we examined whether continuous exposure to environmentally relevant levels of Pb2+ during early life altered granule cell neurogenesis and morphology in the rat hippocampus. Control and Pb2+ -exposed rats received bromodeoxyuridine (BrdU) injections (100 mg/kg; i.p.) for five consecutive days starting at postnatal day 45 and were killed either 1 day or 4 weeks after the last injection. The total number of newborn cells in the DG of Pb2+ -exposed rats was significantly decreased (13%; P &lt;0.001) 1 day after BrdU injections relative to controls. Further, the survival of newborn cells in Pb2+ -exposed rats was significantly decreased by 22.7% ( P &lt;0.001) relative to control animals. Co-localization of BrdU with neuronal or astrocytic markers did not reveal a significant effect of Pb2+ exposure on cellular fate. In Pb2+ -exposed rats, immature granule cells immunolabeled with doublecortin (DCX) displayed aberrant dendritic morphology. That is, the overall length-density of the DCX-positive apical dendrites in the outer portion of the DG molecular layer was significantly reduced up to 36% in the suprapyramidal blade only. We also found that the area of Timm’s-positive staining representative of the mossy fibers terminal fields in the CA3 stratum oriens (SO) was reduced by 26% in Pb2+ -exposed rats. These findings demonstrate that exposure to environmentally relevant levels of Pb2+ during early life alters granule cell neurogenesis and morphology in the rat hippocampus. They provide a cellular and morphological basis for the deficits in synaptic plasticity and spatial learning documented in Pb2+ -exposed animals.</abstract><cop>Oxford</cop><pub>Elsevier Ltd</pub><pmid>17276012</pmid><doi>10.1016/j.neuroscience.2006.12.040</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record>
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subjects Aging
Animals
Biological and medical sciences
Brain - drug effects
Brain - growth & development
Brain - physiology
Bromodeoxyuridine - pharmacology
Environmental Exposure
Female
Fundamental and applied biological sciences. Psychology
granule cell
hippocampus
Hippocampus - drug effects
Hippocampus - growth & development
Lead Poisoning - physiopathology
morphology
Nerve Fibers - physiology
neurogenesis
Neurology
Neurons - drug effects
Neurons - physiology
neurotoxicity
Pb 2
Phenotype
Rats
Rats, Inbred Lew
Vertebrates: nervous system and sense organs
title Environmental lead exposure during early life alters granule cell neurogenesis and morphology in the hippocampus of young adult rats
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