Perinatal exposure to bisphenol-A impairs spatial memory through upregulation of neurexin1 and neuroligin3 expression in male mouse brain
Bisphenol-A (BPA), a well known endocrine disruptor, impairs learning and memory in rodents. However, the underlying molecular mechanism of BPA induced impairment in learning and memory is not well known. As synaptic plasticity is the cellular basis of memory, the present study investigated the effe...
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| description | Bisphenol-A (BPA), a well known endocrine disruptor, impairs learning and memory in rodents. However, the underlying molecular mechanism of BPA induced impairment in learning and memory is not well known. As synaptic plasticity is the cellular basis of memory, the present study investigated the effect of perinatal exposure to BPA on the expression of synaptic proteins neurexin1 (Nrxn1) and neuroligin3 (Nlgn3), dendritic spine density and spatial memory in postnatal male mice. The pregnant mice were orally administered BPA (50 µg/kgbw/d) from gestation day (GD) 7 to postnatal day (PND) 21 and sesame oil was used as a vehicle control. In Morris water maze (MWM) test, BPA extended the escape latency time to locate the hidden platform in 8 weeks male mice. RT-PCR and Immunoblotting results showed significant upregulation of Nrxn1 and Nlgn3 expression in both cerebral cortex and hippocampus of 3 and 8 weeks male mice. This was further substantiated by in-situ hybridization and immunofluorescence techniques. BPA also significantly increased the density of dendritic spines in both regions, as analyzed by rapid Golgi staining. Thus our data suggest that perinatal exposure to BPA impairs spatial memory through upregulation of expression of synaptic proteins Nrxn1 and Nlgn3 and increased dendritic spine density in cerebral cortex and hippocampus of postnatal male mice. |
| doi_str_mv | 10.1371/journal.pone.0110482 |
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However, the underlying molecular mechanism of BPA induced impairment in learning and memory is not well known. As synaptic plasticity is the cellular basis of memory, the present study investigated the effect of perinatal exposure to BPA on the expression of synaptic proteins neurexin1 (Nrxn1) and neuroligin3 (Nlgn3), dendritic spine density and spatial memory in postnatal male mice. The pregnant mice were orally administered BPA (50 µg/kgbw/d) from gestation day (GD) 7 to postnatal day (PND) 21 and sesame oil was used as a vehicle control. In Morris water maze (MWM) test, BPA extended the escape latency time to locate the hidden platform in 8 weeks male mice. RT-PCR and Immunoblotting results showed significant upregulation of Nrxn1 and Nlgn3 expression in both cerebral cortex and hippocampus of 3 and 8 weeks male mice. This was further substantiated by in-situ hybridization and immunofluorescence techniques. BPA also significantly increased the density of dendritic spines in both regions, as analyzed by rapid Golgi staining. Thus our data suggest that perinatal exposure to BPA impairs spatial memory through upregulation of expression of synaptic proteins Nrxn1 and Nlgn3 and increased dendritic spine density in cerebral cortex and hippocampus of postnatal male mice.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0110482</identifier><identifier>PMID: 25330104</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Autism ; Behavior ; Benzhydryl Compounds - administration & dosage ; Biochemistry ; Biology and Life Sciences ; Bisphenol A ; Brain ; Brain research ; Cell Adhesion Molecules, Neuronal - biosynthesis ; Cell Adhesion Molecules, Neuronal - genetics ; Cerebral cortex ; Cerebral Cortex - drug effects ; Dendritic spines ; Dendritic Spines - drug effects ; Dendritic Spines - genetics ; Dendritic structure ; Density ; Epoxy resins ; Exposure ; Female ; Gene Expression Regulation, Developmental - drug effects ; Gestation ; Hippocampus ; Hippocampus - drug effects ; Hormones ; Immunoblotting ; Immunofluorescence ; Laboratories ; Latency ; Learning ; Male ; Maze Learning - drug effects ; Membrane Proteins - biosynthesis ; Membrane Proteins - genetics ; Memory ; Memory tasks ; Mice ; Molecular biology ; Mutation ; Nerve Tissue Proteins - biosynthesis ; Nerve Tissue Proteins - genetics ; Nervous system ; Neural Cell Adhesion Molecules - biosynthesis ; Neural Cell Adhesion Molecules - genetics ; Neuronal Plasticity - drug effects ; Neuronal Plasticity - genetics ; Neurons ; Oral administration ; Perinatal exposure ; Phenols ; Phenols - administration & dosage ; Plastic foam ; Polymerase chain reaction ; Pregnancy ; Prenatal Exposure Delayed Effects - genetics ; Prenatal Exposure Delayed Effects - pathology ; Proteins ; Rodents ; Sesame oil ; Spatial analysis ; Spatial memory ; Spatial Memory - drug effects ; Spine ; Synaptic plasticity ; Up-regulation ; Zoology</subject><ispartof>PloS one, 2014-10, Vol.9 (10), p.e110482</ispartof><rights>COPYRIGHT 2014 Public Library of Science</rights><rights>2014 Kumar, Thakur. This is an open-access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2014 Kumar, Thakur 2014 Kumar, Thakur</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c758t-3d4f1f640793b6aa884c0941d14dd1c875845186514e367bf383994aac78c0593</citedby><cites>FETCH-LOGICAL-c758t-3d4f1f640793b6aa884c0941d14dd1c875845186514e367bf383994aac78c0593</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4201550/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4201550/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79569,79570</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25330104$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kumar, Dhiraj</creatorcontrib><creatorcontrib>Thakur, Mahendra Kumar</creatorcontrib><title>Perinatal exposure to bisphenol-A impairs spatial memory through upregulation of neurexin1 and neuroligin3 expression in male mouse brain</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Bisphenol-A (BPA), a well known endocrine disruptor, impairs learning and memory in rodents. However, the underlying molecular mechanism of BPA induced impairment in learning and memory is not well known. As synaptic plasticity is the cellular basis of memory, the present study investigated the effect of perinatal exposure to BPA on the expression of synaptic proteins neurexin1 (Nrxn1) and neuroligin3 (Nlgn3), dendritic spine density and spatial memory in postnatal male mice. The pregnant mice were orally administered BPA (50 µg/kgbw/d) from gestation day (GD) 7 to postnatal day (PND) 21 and sesame oil was used as a vehicle control. In Morris water maze (MWM) test, BPA extended the escape latency time to locate the hidden platform in 8 weeks male mice. RT-PCR and Immunoblotting results showed significant upregulation of Nrxn1 and Nlgn3 expression in both cerebral cortex and hippocampus of 3 and 8 weeks male mice. This was further substantiated by in-situ hybridization and immunofluorescence techniques. BPA also significantly increased the density of dendritic spines in both regions, as analyzed by rapid Golgi staining. Thus our data suggest that perinatal exposure to BPA impairs spatial memory through upregulation of expression of synaptic proteins Nrxn1 and Nlgn3 and increased dendritic spine density in cerebral cortex and hippocampus of postnatal male mice.</description><subject>Animals</subject><subject>Autism</subject><subject>Behavior</subject><subject>Benzhydryl Compounds - administration & dosage</subject><subject>Biochemistry</subject><subject>Biology and Life Sciences</subject><subject>Bisphenol A</subject><subject>Brain</subject><subject>Brain research</subject><subject>Cell Adhesion Molecules, Neuronal - biosynthesis</subject><subject>Cell Adhesion Molecules, Neuronal - genetics</subject><subject>Cerebral cortex</subject><subject>Cerebral Cortex - drug effects</subject><subject>Dendritic spines</subject><subject>Dendritic Spines - drug effects</subject><subject>Dendritic Spines - genetics</subject><subject>Dendritic structure</subject><subject>Density</subject><subject>Epoxy resins</subject><subject>Exposure</subject><subject>Female</subject><subject>Gene Expression Regulation, Developmental - drug effects</subject><subject>Gestation</subject><subject>Hippocampus</subject><subject>Hippocampus - drug effects</subject><subject>Hormones</subject><subject>Immunoblotting</subject><subject>Immunofluorescence</subject><subject>Laboratories</subject><subject>Latency</subject><subject>Learning</subject><subject>Male</subject><subject>Maze Learning - drug effects</subject><subject>Membrane Proteins - biosynthesis</subject><subject>Membrane Proteins - genetics</subject><subject>Memory</subject><subject>Memory tasks</subject><subject>Mice</subject><subject>Molecular biology</subject><subject>Mutation</subject><subject>Nerve Tissue Proteins - biosynthesis</subject><subject>Nerve Tissue Proteins - genetics</subject><subject>Nervous system</subject><subject>Neural Cell Adhesion Molecules - biosynthesis</subject><subject>Neural Cell Adhesion Molecules - genetics</subject><subject>Neuronal Plasticity - drug effects</subject><subject>Neuronal Plasticity - genetics</subject><subject>Neurons</subject><subject>Oral administration</subject><subject>Perinatal exposure</subject><subject>Phenols</subject><subject>Phenols - administration & dosage</subject><subject>Plastic foam</subject><subject>Polymerase chain reaction</subject><subject>Pregnancy</subject><subject>Prenatal Exposure Delayed Effects - genetics</subject><subject>Prenatal Exposure Delayed Effects - pathology</subject><subject>Proteins</subject><subject>Rodents</subject><subject>Sesame oil</subject><subject>Spatial analysis</subject><subject>Spatial memory</subject><subject>Spatial Memory - drug effects</subject><subject>Spine</subject><subject>Synaptic plasticity</subject><subject>Up-regulation</subject><subject>Zoology</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqNk12L1DAUhoso7rr6D0QDguDFjEmTtumNMCx-DCys-HUbTtO0kyFNatLK7E_wX5vudJcpKEgu8vW8b8LLOUnynOA1oQV5u3ejt2DWvbNqjQnBjKcPknNS0nSVp5g-PFmfJU9C2GOcUZ7nj5OzNKMUR8V58vuz8trCAAapQ-_C6BUaHKp06HfKOrPaIN31oH1AoYdBR65TnfM3aNh5N7Y7NPZetaOJd84i1yCrosdBW4LA1rc7Z3SrLZ0e8CqEidMWdWAU6twYFKo8aPs0edSACerZPF8k3z-8_3b5aXV1_XF7ublaySLjw4rWrCFNznBR0ioH4JxJXDJSE1bXRPIIsYzwPCNM0byoGsppWTIAWXCJs5JeJC-Pvr1xQcwpBkFyQlnKGKeR2B6J2sFe9F534G-EAy1uD5xvBfhBS6NEkTclAYUxlBVjkJYAWQ4yj3-RBeU4er2bXxurTtVS2cGDWZgub6zeidb9EizFJMsmg1ezgXc_RxWGf3x5ptqYqtC2cdFMdjpIsWGERypLWaTWf6HiqFWnZayjRsfzheDNQhCZQR2GFsYQxPbrl_9nr38s2dcn7E6BGXbBmXGqobAE2RGU3oXgVXOfHMFiaoO7NMTUBmJugyh7cZr6veiu7ukfRPIEOQ</recordid><startdate>20141017</startdate><enddate>20141017</enddate><creator>Kumar, Dhiraj</creator><creator>Thakur, Mahendra Kumar</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20141017</creationdate><title>Perinatal exposure to bisphenol-A impairs spatial memory through upregulation of neurexin1 and neuroligin3 expression in male mouse brain</title><author>Kumar, Dhiraj ; Thakur, Mahendra Kumar</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c758t-3d4f1f640793b6aa884c0941d14dd1c875845186514e367bf383994aac78c0593</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Animals</topic><topic>Autism</topic><topic>Behavior</topic><topic>Benzhydryl Compounds - administration & dosage</topic><topic>Biochemistry</topic><topic>Biology and Life Sciences</topic><topic>Bisphenol A</topic><topic>Brain</topic><topic>Brain research</topic><topic>Cell Adhesion Molecules, Neuronal - biosynthesis</topic><topic>Cell Adhesion Molecules, Neuronal - genetics</topic><topic>Cerebral cortex</topic><topic>Cerebral Cortex - drug effects</topic><topic>Dendritic spines</topic><topic>Dendritic Spines - drug effects</topic><topic>Dendritic Spines - genetics</topic><topic>Dendritic structure</topic><topic>Density</topic><topic>Epoxy resins</topic><topic>Exposure</topic><topic>Female</topic><topic>Gene Expression Regulation, Developmental - drug effects</topic><topic>Gestation</topic><topic>Hippocampus</topic><topic>Hippocampus - drug effects</topic><topic>Hormones</topic><topic>Immunoblotting</topic><topic>Immunofluorescence</topic><topic>Laboratories</topic><topic>Latency</topic><topic>Learning</topic><topic>Male</topic><topic>Maze Learning - drug effects</topic><topic>Membrane Proteins - biosynthesis</topic><topic>Membrane Proteins - genetics</topic><topic>Memory</topic><topic>Memory tasks</topic><topic>Mice</topic><topic>Molecular biology</topic><topic>Mutation</topic><topic>Nerve Tissue Proteins - biosynthesis</topic><topic>Nerve Tissue Proteins - genetics</topic><topic>Nervous system</topic><topic>Neural Cell Adhesion Molecules - biosynthesis</topic><topic>Neural Cell Adhesion Molecules - genetics</topic><topic>Neuronal Plasticity - drug effects</topic><topic>Neuronal Plasticity - genetics</topic><topic>Neurons</topic><topic>Oral administration</topic><topic>Perinatal exposure</topic><topic>Phenols</topic><topic>Phenols - administration & dosage</topic><topic>Plastic foam</topic><topic>Polymerase chain reaction</topic><topic>Pregnancy</topic><topic>Prenatal Exposure Delayed Effects - genetics</topic><topic>Prenatal Exposure Delayed Effects - pathology</topic><topic>Proteins</topic><topic>Rodents</topic><topic>Sesame oil</topic><topic>Spatial analysis</topic><topic>Spatial memory</topic><topic>Spatial Memory - drug effects</topic><topic>Spine</topic><topic>Synaptic plasticity</topic><topic>Up-regulation</topic><topic>Zoology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kumar, Dhiraj</creatorcontrib><creatorcontrib>Thakur, Mahendra Kumar</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - 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However, the underlying molecular mechanism of BPA induced impairment in learning and memory is not well known. As synaptic plasticity is the cellular basis of memory, the present study investigated the effect of perinatal exposure to BPA on the expression of synaptic proteins neurexin1 (Nrxn1) and neuroligin3 (Nlgn3), dendritic spine density and spatial memory in postnatal male mice. The pregnant mice were orally administered BPA (50 µg/kgbw/d) from gestation day (GD) 7 to postnatal day (PND) 21 and sesame oil was used as a vehicle control. In Morris water maze (MWM) test, BPA extended the escape latency time to locate the hidden platform in 8 weeks male mice. RT-PCR and Immunoblotting results showed significant upregulation of Nrxn1 and Nlgn3 expression in both cerebral cortex and hippocampus of 3 and 8 weeks male mice. This was further substantiated by in-situ hybridization and immunofluorescence techniques. BPA also significantly increased the density of dendritic spines in both regions, as analyzed by rapid Golgi staining. Thus our data suggest that perinatal exposure to BPA impairs spatial memory through upregulation of expression of synaptic proteins Nrxn1 and Nlgn3 and increased dendritic spine density in cerebral cortex and hippocampus of postnatal male mice.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25330104</pmid><doi>10.1371/journal.pone.0110482</doi><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Autism Behavior Benzhydryl Compounds - administration & dosage Biochemistry Biology and Life Sciences Bisphenol A Brain Brain research Cell Adhesion Molecules, Neuronal - biosynthesis Cell Adhesion Molecules, Neuronal - genetics Cerebral cortex Cerebral Cortex - drug effects Dendritic spines Dendritic Spines - drug effects Dendritic Spines - genetics Dendritic structure Density Epoxy resins Exposure Female Gene Expression Regulation, Developmental - drug effects Gestation Hippocampus Hippocampus - drug effects Hormones Immunoblotting Immunofluorescence Laboratories Latency Learning Male Maze Learning - drug effects Membrane Proteins - biosynthesis Membrane Proteins - genetics Memory Memory tasks Mice Molecular biology Mutation Nerve Tissue Proteins - biosynthesis Nerve Tissue Proteins - genetics Nervous system Neural Cell Adhesion Molecules - biosynthesis Neural Cell Adhesion Molecules - genetics Neuronal Plasticity - drug effects Neuronal Plasticity - genetics Neurons Oral administration Perinatal exposure Phenols Phenols - administration & dosage Plastic foam Polymerase chain reaction Pregnancy Prenatal Exposure Delayed Effects - genetics Prenatal Exposure Delayed Effects - pathology Proteins Rodents Sesame oil Spatial analysis Spatial memory Spatial Memory - drug effects Spine Synaptic plasticity Up-regulation Zoology |
| title | Perinatal exposure to bisphenol-A impairs spatial memory through upregulation of neurexin1 and neuroligin3 expression in male mouse brain |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-13T16%3A19%3A31IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Perinatal%20exposure%20to%20bisphenol-A%20impairs%20spatial%20memory%20through%20upregulation%20of%20neurexin1%20and%20neuroligin3%20expression%20in%20male%20mouse%20brain&rft.jtitle=PloS%20one&rft.au=Kumar,%20Dhiraj&rft.date=2014-10-17&rft.volume=9&rft.issue=10&rft.spage=e110482&rft.pages=e110482-&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0110482&rft_dat=%3Cgale_plos_%3EA418424524%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1613424483&rft_id=info:pmid/25330104&rft_galeid=A418424524&rft_doaj_id=oai_doaj_org_article_76f91ae00a9b44a29aa56ac64ddc7380&rfr_iscdi=true |