Neuroglobin Expression in the Mammalian Auditory System
The energy-yielding pathways that provide the large amounts of metabolic energy required by inner ear sensorineural cells are poorly understood. Neuroglobin (Ngb) is a neuron-specific hemoprotein of the globin family, which is suggested to be involved in oxidative energy metabolism. Here, we present...
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Veröffentlicht in: | Molecular neurobiology 2016-04, Vol.53 (3), p.1461-1477 |
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creator | Reuss, Stefan Banica, Ovidiu Elgurt, Mirra Mitz, Stephanie Disque-Kaiser, Ursula Riemann, Randolf Hill, Marco Jaquish, Dawn V. Koehrn, Fred J. Burmester, Thorsten Hankeln, Thomas Woolf, Nigel K. |
description | The energy-yielding pathways that provide the large amounts of metabolic energy required by inner ear sensorineural cells are poorly understood. Neuroglobin (Ngb) is a neuron-specific hemoprotein of the globin family, which is suggested to be involved in oxidative energy metabolism. Here, we present quantitative real-time reverse transcription PCR, in situ hybridization, immunohistochemical, and Western blot evidence that neuroglobin is highly expressed in the mouse and rat cochlea. For primary cochlea neurons, Ngb expression is limited to the subpopulation of type I spiral ganglion cells, those which innervate inner hair cells, while the subpopulation of type II spiral ganglion cells which innervate the outer hair cells do not express Ngb. We further investigated Ngb distribution in rat, mouse, and human auditory brainstem centers, and found that the cochlear nuclei and superior olivary complex (SOC) also express considerable amounts of Ngb. Notably, the majority of olivocochlear neurons, those which provide efferent innervation of outer hair cells as identified by neuronal tract tracing, were Ngb-immunoreactive. We also observed that neuroglobin in the SOC frequently co-localized with neuronal nitric oxide synthase, the enzyme responsible for nitric oxide production. Our findings suggest that neuroglobin is well positioned to play an important physiologic role in the oxygen homeostasis of the peripheral and central auditory nervous system, and provides the first evidence that Ngb signal differentiates the central projections of the inner and outer hair cells. |
doi_str_mv | 10.1007/s12035-014-9082-1 |
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Neuroglobin (Ngb) is a neuron-specific hemoprotein of the globin family, which is suggested to be involved in oxidative energy metabolism. Here, we present quantitative real-time reverse transcription PCR, in situ hybridization, immunohistochemical, and Western blot evidence that neuroglobin is highly expressed in the mouse and rat cochlea. For primary cochlea neurons, Ngb expression is limited to the subpopulation of type I spiral ganglion cells, those which innervate inner hair cells, while the subpopulation of type II spiral ganglion cells which innervate the outer hair cells do not express Ngb. We further investigated Ngb distribution in rat, mouse, and human auditory brainstem centers, and found that the cochlear nuclei and superior olivary complex (SOC) also express considerable amounts of Ngb. Notably, the majority of olivocochlear neurons, those which provide efferent innervation of outer hair cells as identified by neuronal tract tracing, were Ngb-immunoreactive. We also observed that neuroglobin in the SOC frequently co-localized with neuronal nitric oxide synthase, the enzyme responsible for nitric oxide production. Our findings suggest that neuroglobin is well positioned to play an important physiologic role in the oxygen homeostasis of the peripheral and central auditory nervous system, and provides the first evidence that Ngb signal differentiates the central projections of the inner and outer hair cells.</description><identifier>ISSN: 0893-7648</identifier><identifier>EISSN: 1559-1182</identifier><identifier>DOI: 10.1007/s12035-014-9082-1</identifier><identifier>PMID: 25636685</identifier><language>eng</language><publisher>New York: Springer US</publisher><subject>Adenosine Triphosphate - metabolism ; Aged ; Animals ; Biomedical and Life Sciences ; Biomedicine ; Brain Stem - metabolism ; Cell Biology ; Cochlea - metabolism ; Ears & hearing ; Female ; Globins - biosynthesis ; Globins - genetics ; Globins - physiology ; Humans ; In Situ Hybridization ; Male ; Mice ; Mice, Inbred BALB C ; Nerve Tissue Proteins - biosynthesis ; Nerve Tissue Proteins - genetics ; Nerve Tissue Proteins - physiology ; Neurobiology ; Neurology ; Neurosciences ; Nitric Oxide Synthase Type I - analysis ; Protein expression ; Rats ; Rats, Sprague-Dawley ; Rodents ; Spiral Ganglion - metabolism ; Superior Olivary Complex - metabolism</subject><ispartof>Molecular neurobiology, 2016-04, Vol.53 (3), p.1461-1477</ispartof><rights>Springer Science+Business Media New York 2015</rights><rights>Springer Science+Business Media New York 2016</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c573t-3cf44ca94c8df4438b7fb0dec96b0522a63af77b9ba8f67f92bff2219f8ff8993</citedby><cites>FETCH-LOGICAL-c573t-3cf44ca94c8df4438b7fb0dec96b0522a63af77b9ba8f67f92bff2219f8ff8993</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s12035-014-9082-1$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s12035-014-9082-1$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>230,314,780,784,885,27924,27925,41488,42557,51319</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25636685$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Reuss, Stefan</creatorcontrib><creatorcontrib>Banica, Ovidiu</creatorcontrib><creatorcontrib>Elgurt, Mirra</creatorcontrib><creatorcontrib>Mitz, Stephanie</creatorcontrib><creatorcontrib>Disque-Kaiser, Ursula</creatorcontrib><creatorcontrib>Riemann, Randolf</creatorcontrib><creatorcontrib>Hill, Marco</creatorcontrib><creatorcontrib>Jaquish, Dawn V.</creatorcontrib><creatorcontrib>Koehrn, Fred J.</creatorcontrib><creatorcontrib>Burmester, Thorsten</creatorcontrib><creatorcontrib>Hankeln, Thomas</creatorcontrib><creatorcontrib>Woolf, Nigel K.</creatorcontrib><title>Neuroglobin Expression in the Mammalian Auditory System</title><title>Molecular neurobiology</title><addtitle>Mol Neurobiol</addtitle><addtitle>Mol Neurobiol</addtitle><description>The energy-yielding pathways that provide the large amounts of metabolic energy required by inner ear sensorineural cells are poorly understood. Neuroglobin (Ngb) is a neuron-specific hemoprotein of the globin family, which is suggested to be involved in oxidative energy metabolism. Here, we present quantitative real-time reverse transcription PCR, in situ hybridization, immunohistochemical, and Western blot evidence that neuroglobin is highly expressed in the mouse and rat cochlea. For primary cochlea neurons, Ngb expression is limited to the subpopulation of type I spiral ganglion cells, those which innervate inner hair cells, while the subpopulation of type II spiral ganglion cells which innervate the outer hair cells do not express Ngb. We further investigated Ngb distribution in rat, mouse, and human auditory brainstem centers, and found that the cochlear nuclei and superior olivary complex (SOC) also express considerable amounts of Ngb. Notably, the majority of olivocochlear neurons, those which provide efferent innervation of outer hair cells as identified by neuronal tract tracing, were Ngb-immunoreactive. We also observed that neuroglobin in the SOC frequently co-localized with neuronal nitric oxide synthase, the enzyme responsible for nitric oxide production. Our findings suggest that neuroglobin is well positioned to play an important physiologic role in the oxygen homeostasis of the peripheral and central auditory nervous system, and provides the first evidence that Ngb signal differentiates the central projections of the inner and outer hair cells.</description><subject>Adenosine Triphosphate - metabolism</subject><subject>Aged</subject><subject>Animals</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>Brain Stem - metabolism</subject><subject>Cell Biology</subject><subject>Cochlea - metabolism</subject><subject>Ears & hearing</subject><subject>Female</subject><subject>Globins - biosynthesis</subject><subject>Globins - genetics</subject><subject>Globins - physiology</subject><subject>Humans</subject><subject>In Situ Hybridization</subject><subject>Male</subject><subject>Mice</subject><subject>Mice, Inbred BALB C</subject><subject>Nerve Tissue Proteins - biosynthesis</subject><subject>Nerve Tissue Proteins - genetics</subject><subject>Nerve Tissue Proteins - physiology</subject><subject>Neurobiology</subject><subject>Neurology</subject><subject>Neurosciences</subject><subject>Nitric Oxide Synthase Type I - analysis</subject><subject>Protein expression</subject><subject>Rats</subject><subject>Rats, Sprague-Dawley</subject><subject>Rodents</subject><subject>Spiral Ganglion - metabolism</subject><subject>Superior Olivary Complex - metabolism</subject><issn>0893-7648</issn><issn>1559-1182</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNqNkctKxDAUhoMoOl4ewI0U3Lip5n7ZCDKMF_CyUNch7SQzlbYZk1actzdlVEZBcJWE850vJ_kBOETwFEEoziLCkLAcIporKHGONsAIMaZyhCTeBCMoFckFp3IH7Mb4AiHGCIptsIMZJ5xLNgLi3vbBz2pfVG02eV8EG2Pl2yydurnN7kzTmLoybXbRT6vOh2X2uIydbfbBljN1tAef6x54vpw8ja_z24erm_HFbV4yQbqclI7S0ihaymnaEVkIV8CpLRUvIMPYcGKcEIUqjHRcOIUL59KUyknnpFJkD5yvvIu-aOy0tG0XTK0XoWpMWGpvKv2z0lZzPfNvmrJkUTIJTj4Fwb_2Nna6qWJp69q01vdRIyE4Z1Rw8h-UUEyxHKzHv9AX34c2_cRAYUYUEgOFVlQZfIzBuu-5EdRDgnqVoE4J6iFBjVLP0fqDvzu-IksAXgExldqZDWtX_2n9AL_RpoA</recordid><startdate>20160401</startdate><enddate>20160401</enddate><creator>Reuss, Stefan</creator><creator>Banica, Ovidiu</creator><creator>Elgurt, Mirra</creator><creator>Mitz, Stephanie</creator><creator>Disque-Kaiser, Ursula</creator><creator>Riemann, Randolf</creator><creator>Hill, Marco</creator><creator>Jaquish, Dawn V.</creator><creator>Koehrn, Fred J.</creator><creator>Burmester, Thorsten</creator><creator>Hankeln, Thomas</creator><creator>Woolf, Nigel K.</creator><general>Springer US</general><general>Springer Nature B.V</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>3V.</scope><scope>7QR</scope><scope>7TK</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88G</scope><scope>88I</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2M</scope><scope>M2P</scope><scope>M7P</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PSYQQ</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20160401</creationdate><title>Neuroglobin Expression in the Mammalian Auditory System</title><author>Reuss, Stefan ; Banica, Ovidiu ; Elgurt, Mirra ; Mitz, Stephanie ; Disque-Kaiser, Ursula ; Riemann, Randolf ; Hill, Marco ; Jaquish, Dawn V. ; Koehrn, Fred J. ; Burmester, Thorsten ; Hankeln, Thomas ; Woolf, Nigel K.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c573t-3cf44ca94c8df4438b7fb0dec96b0522a63af77b9ba8f67f92bff2219f8ff8993</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Adenosine Triphosphate - metabolism</topic><topic>Aged</topic><topic>Animals</topic><topic>Biomedical and Life Sciences</topic><topic>Biomedicine</topic><topic>Brain Stem - metabolism</topic><topic>Cell Biology</topic><topic>Cochlea - metabolism</topic><topic>Ears & hearing</topic><topic>Female</topic><topic>Globins - biosynthesis</topic><topic>Globins - genetics</topic><topic>Globins - physiology</topic><topic>Humans</topic><topic>In Situ Hybridization</topic><topic>Male</topic><topic>Mice</topic><topic>Mice, Inbred BALB C</topic><topic>Nerve Tissue Proteins - biosynthesis</topic><topic>Nerve Tissue Proteins - genetics</topic><topic>Nerve Tissue Proteins - physiology</topic><topic>Neurobiology</topic><topic>Neurology</topic><topic>Neurosciences</topic><topic>Nitric Oxide Synthase Type I - analysis</topic><topic>Protein expression</topic><topic>Rats</topic><topic>Rats, Sprague-Dawley</topic><topic>Rodents</topic><topic>Spiral Ganglion - metabolism</topic><topic>Superior Olivary Complex - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Reuss, Stefan</creatorcontrib><creatorcontrib>Banica, Ovidiu</creatorcontrib><creatorcontrib>Elgurt, Mirra</creatorcontrib><creatorcontrib>Mitz, Stephanie</creatorcontrib><creatorcontrib>Disque-Kaiser, Ursula</creatorcontrib><creatorcontrib>Riemann, Randolf</creatorcontrib><creatorcontrib>Hill, Marco</creatorcontrib><creatorcontrib>Jaquish, Dawn V.</creatorcontrib><creatorcontrib>Koehrn, Fred J.</creatorcontrib><creatorcontrib>Burmester, Thorsten</creatorcontrib><creatorcontrib>Hankeln, Thomas</creatorcontrib><creatorcontrib>Woolf, Nigel K.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Psychology Database (Alumni)</collection><collection>Science Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech 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>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</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>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Psychology Database</collection><collection>Science Database</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest One Psychology</collection><collection>ProQuest Central Basic</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Molecular neurobiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Reuss, Stefan</au><au>Banica, Ovidiu</au><au>Elgurt, Mirra</au><au>Mitz, Stephanie</au><au>Disque-Kaiser, Ursula</au><au>Riemann, Randolf</au><au>Hill, Marco</au><au>Jaquish, Dawn V.</au><au>Koehrn, Fred J.</au><au>Burmester, Thorsten</au><au>Hankeln, Thomas</au><au>Woolf, Nigel K.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Neuroglobin Expression in the Mammalian Auditory System</atitle><jtitle>Molecular neurobiology</jtitle><stitle>Mol Neurobiol</stitle><addtitle>Mol Neurobiol</addtitle><date>2016-04-01</date><risdate>2016</risdate><volume>53</volume><issue>3</issue><spage>1461</spage><epage>1477</epage><pages>1461-1477</pages><issn>0893-7648</issn><eissn>1559-1182</eissn><abstract>The energy-yielding pathways that provide the large amounts of metabolic energy required by inner ear sensorineural cells are poorly understood. Neuroglobin (Ngb) is a neuron-specific hemoprotein of the globin family, which is suggested to be involved in oxidative energy metabolism. Here, we present quantitative real-time reverse transcription PCR, in situ hybridization, immunohistochemical, and Western blot evidence that neuroglobin is highly expressed in the mouse and rat cochlea. For primary cochlea neurons, Ngb expression is limited to the subpopulation of type I spiral ganglion cells, those which innervate inner hair cells, while the subpopulation of type II spiral ganglion cells which innervate the outer hair cells do not express Ngb. We further investigated Ngb distribution in rat, mouse, and human auditory brainstem centers, and found that the cochlear nuclei and superior olivary complex (SOC) also express considerable amounts of Ngb. Notably, the majority of olivocochlear neurons, those which provide efferent innervation of outer hair cells as identified by neuronal tract tracing, were Ngb-immunoreactive. We also observed that neuroglobin in the SOC frequently co-localized with neuronal nitric oxide synthase, the enzyme responsible for nitric oxide production. Our findings suggest that neuroglobin is well positioned to play an important physiologic role in the oxygen homeostasis of the peripheral and central auditory nervous system, and provides the first evidence that Ngb signal differentiates the central projections of the inner and outer hair cells.</abstract><cop>New York</cop><pub>Springer US</pub><pmid>25636685</pmid><doi>10.1007/s12035-014-9082-1</doi><tpages>17</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Adenosine Triphosphate - metabolism Aged Animals Biomedical and Life Sciences Biomedicine Brain Stem - metabolism Cell Biology Cochlea - metabolism Ears & hearing Female Globins - biosynthesis Globins - genetics Globins - physiology Humans In Situ Hybridization Male Mice Mice, Inbred BALB C Nerve Tissue Proteins - biosynthesis Nerve Tissue Proteins - genetics Nerve Tissue Proteins - physiology Neurobiology Neurology Neurosciences Nitric Oxide Synthase Type I - analysis Protein expression Rats Rats, Sprague-Dawley Rodents Spiral Ganglion - metabolism Superior Olivary Complex - metabolism |
title | Neuroglobin Expression in the Mammalian Auditory System |
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