A translational systems biology approach in both animals and humans identifies a functionally related module of accumbal genes involved in the regulation of reward processing and binge drinking in males
Identifieur interne : 003221 ( Main/Exploration ); précédent : 003220; suivant : 003222A translational systems biology approach in both animals and humans identifies a functionally related module of accumbal genes involved in the regulation of reward processing and binge drinking in males
Auteurs : David Stacey ; Anbarasu Lourdusamy ; Barbara Ruggeri ; Matthieu Maroteaux ; Tianye Jia ; Anna Cattrell ; Charlotte Nymberg ; Tobias Banaschewski ; Sohinee Bhattacharyya ; Hamid Band ; Gareth Barker ; Arun Bokde ; Christian Buchel ; Fabiana Carvalho ; Patricia Conrod ; Sylvane Desrivieres ; Alanna Easton ; Mira Fauth-Buehler ; Alberto Fernandez-Medarde ; Herta Flor ; Vincent Frouin ; Jurgen Gallinat ; Hugh Garavanh ; Andreas Heinz ; Bernd Ittermann ; Mark Lathrop ; Claire Lawrence ; Eva Loth ; Karl Mann ; Jean-Luc Martinot ; Frauke Nees ; Tomas Paus ; Zdenka Pausova ; Marcella Rietschel ; Andrea Rotter ; Eugenio Santos ; Michael Smolka ; Wolfgang Sommer ; Manuel Mameli ; Rainer Spanagel ; Jean-Antoine Girault ; Christian Mueller ; Gunter SchumannSource :
- Journal of Psychiatry & Neuroscience : JPN [ 1180-4882 ] ; 2015.
Abstract
The mesolimbic dopamine system, composed primarily of dopaminergic neurons in the ventral tegmental area that project to striatal structures, is considered to be the key mediator of reinforcement-related mechanisms in the brain. Prompted by a genome-wide association meta-analysis implicating the Ras-specific guanine nucleotide-releasing factor 2 (
Transcriptomic data from the nucleus accumbens (NAcc) of male
The WGCNA analyses using accumbal transcriptomic data revealed 37 distinct “modules,” or functionally related groups of genes. Two of these modules were significantly associated with
It was not possible to determine the extent to which the M5 module was dysregulated in
Taken together, our findings indicate that the accumbal M5 module, initially identified as being dysregulated in male
Url:
DOI: 10.1503/jpn.150138
PubMed: 26679926
PubMed Central: 4853210
Affiliations:
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<author><name sortKey="Lourdusamy, Anbarasu" sort="Lourdusamy, Anbarasu" uniqKey="Lourdusamy A" first="Anbarasu" last="Lourdusamy">Anbarasu Lourdusamy</name>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">A translational systems biology approach in both animals and humans identifies a functionally related module of accumbal genes involved in the regulation of reward processing and binge drinking in males</title>
<author><name sortKey="Stacey, David" sort="Stacey, David" uniqKey="Stacey D" first="David" last="Stacey">David Stacey</name>
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<author><name sortKey="Lourdusamy, Anbarasu" sort="Lourdusamy, Anbarasu" uniqKey="Lourdusamy A" first="Anbarasu" last="Lourdusamy">Anbarasu Lourdusamy</name>
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<author><name sortKey="Ruggeri, Barbara" sort="Ruggeri, Barbara" uniqKey="Ruggeri B" first="Barbara" last="Ruggeri">Barbara Ruggeri</name>
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<author><name sortKey="Maroteaux, Matthieu" sort="Maroteaux, Matthieu" uniqKey="Maroteaux M" first="Matthieu" last="Maroteaux">Matthieu Maroteaux</name>
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<author><name sortKey="Jia, Tianye" sort="Jia, Tianye" uniqKey="Jia T" first="Tianye" last="Jia">Tianye Jia</name>
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<author><name sortKey="Cattrell, Anna" sort="Cattrell, Anna" uniqKey="Cattrell A" first="Anna" last="Cattrell">Anna Cattrell</name>
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<author><name sortKey="Nymberg, Charlotte" sort="Nymberg, Charlotte" uniqKey="Nymberg C" first="Charlotte" last="Nymberg">Charlotte Nymberg</name>
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<author><name sortKey="Banaschewski, Tobias" sort="Banaschewski, Tobias" uniqKey="Banaschewski T" first="Tobias" last="Banaschewski">Tobias Banaschewski</name>
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<author><name sortKey="Bhattacharyya, Sohinee" sort="Bhattacharyya, Sohinee" uniqKey="Bhattacharyya S" first="Sohinee" last="Bhattacharyya">Sohinee Bhattacharyya</name>
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<author><name sortKey="Band, Hamid" sort="Band, Hamid" uniqKey="Band H" first="Hamid" last="Band">Hamid Band</name>
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<author><name sortKey="Barker, Gareth" sort="Barker, Gareth" uniqKey="Barker G" first="Gareth" last="Barker">Gareth Barker</name>
</author>
<author><name sortKey="Bokde, Arun" sort="Bokde, Arun" uniqKey="Bokde A" first="Arun" last="Bokde">Arun Bokde</name>
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<author><name sortKey="Buchel, Christian" sort="Buchel, Christian" uniqKey="Buchel C" first="Christian" last="Buchel">Christian Buchel</name>
</author>
<author><name sortKey="Carvalho, Fabiana" sort="Carvalho, Fabiana" uniqKey="Carvalho F" first="Fabiana" last="Carvalho">Fabiana Carvalho</name>
</author>
<author><name sortKey="Conrod, Patricia" sort="Conrod, Patricia" uniqKey="Conrod P" first="Patricia" last="Conrod">Patricia Conrod</name>
</author>
<author><name sortKey="Desrivieres, Sylvane" sort="Desrivieres, Sylvane" uniqKey="Desrivieres S" first="Sylvane" last="Desrivieres">Sylvane Desrivieres</name>
</author>
<author><name sortKey="Easton, Alanna" sort="Easton, Alanna" uniqKey="Easton A" first="Alanna" last="Easton">Alanna Easton</name>
</author>
<author><name sortKey="Fauth Buehler, Mira" sort="Fauth Buehler, Mira" uniqKey="Fauth Buehler M" first="Mira" last="Fauth-Buehler">Mira Fauth-Buehler</name>
</author>
<author><name sortKey="Fernandez Medarde, Alberto" sort="Fernandez Medarde, Alberto" uniqKey="Fernandez Medarde A" first="Alberto" last="Fernandez-Medarde">Alberto Fernandez-Medarde</name>
</author>
<author><name sortKey="Flor, Herta" sort="Flor, Herta" uniqKey="Flor H" first="Herta" last="Flor">Herta Flor</name>
</author>
<author><name sortKey="Frouin, Vincent" sort="Frouin, Vincent" uniqKey="Frouin V" first="Vincent" last="Frouin">Vincent Frouin</name>
</author>
<author><name sortKey="Gallinat, Jurgen" sort="Gallinat, Jurgen" uniqKey="Gallinat J" first="Jurgen" last="Gallinat">Jurgen Gallinat</name>
</author>
<author><name sortKey="Garavanh, Hugh" sort="Garavanh, Hugh" uniqKey="Garavanh H" first="Hugh" last="Garavanh">Hugh Garavanh</name>
</author>
<author><name sortKey="Heinz, Andreas" sort="Heinz, Andreas" uniqKey="Heinz A" first="Andreas" last="Heinz">Andreas Heinz</name>
</author>
<author><name sortKey="Ittermann, Bernd" sort="Ittermann, Bernd" uniqKey="Ittermann B" first="Bernd" last="Ittermann">Bernd Ittermann</name>
</author>
<author><name sortKey="Lathrop, Mark" sort="Lathrop, Mark" uniqKey="Lathrop M" first="Mark" last="Lathrop">Mark Lathrop</name>
</author>
<author><name sortKey="Lawrence, Claire" sort="Lawrence, Claire" uniqKey="Lawrence C" first="Claire" last="Lawrence">Claire Lawrence</name>
</author>
<author><name sortKey="Loth, Eva" sort="Loth, Eva" uniqKey="Loth E" first="Eva" last="Loth">Eva Loth</name>
</author>
<author><name sortKey="Mann, Karl" sort="Mann, Karl" uniqKey="Mann K" first="Karl" last="Mann">Karl Mann</name>
</author>
<author><name sortKey="Martinot, Jean Luc" sort="Martinot, Jean Luc" uniqKey="Martinot J" first="Jean-Luc" last="Martinot">Jean-Luc Martinot</name>
</author>
<author><name sortKey="Nees, Frauke" sort="Nees, Frauke" uniqKey="Nees F" first="Frauke" last="Nees">Frauke Nees</name>
</author>
<author><name sortKey="Paus, Tomas" sort="Paus, Tomas" uniqKey="Paus T" first="Tomas" last="Paus">Tomas Paus</name>
</author>
<author><name sortKey="Pausova, Zdenka" sort="Pausova, Zdenka" uniqKey="Pausova Z" first="Zdenka" last="Pausova">Zdenka Pausova</name>
</author>
<author><name sortKey="Rietschel, Marcella" sort="Rietschel, Marcella" uniqKey="Rietschel M" first="Marcella" last="Rietschel">Marcella Rietschel</name>
</author>
<author><name sortKey="Rotter, Andrea" sort="Rotter, Andrea" uniqKey="Rotter A" first="Andrea" last="Rotter">Andrea Rotter</name>
</author>
<author><name sortKey="Santos, Eugenio" sort="Santos, Eugenio" uniqKey="Santos E" first="Eugenio" last="Santos">Eugenio Santos</name>
</author>
<author><name sortKey="Smolka, Michael" sort="Smolka, Michael" uniqKey="Smolka M" first="Michael" last="Smolka">Michael Smolka</name>
</author>
<author><name sortKey="Sommer, Wolfgang" sort="Sommer, Wolfgang" uniqKey="Sommer W" first="Wolfgang" last="Sommer">Wolfgang Sommer</name>
</author>
<author><name sortKey="Mameli, Manuel" sort="Mameli, Manuel" uniqKey="Mameli M" first="Manuel" last="Mameli">Manuel Mameli</name>
</author>
<author><name sortKey="Spanagel, Rainer" sort="Spanagel, Rainer" uniqKey="Spanagel R" first="Rainer" last="Spanagel">Rainer Spanagel</name>
</author>
<author><name sortKey="Girault, Jean Antoine" sort="Girault, Jean Antoine" uniqKey="Girault J" first="Jean-Antoine" last="Girault">Jean-Antoine Girault</name>
</author>
<author><name sortKey="Mueller, Christian" sort="Mueller, Christian" uniqKey="Mueller C" first="Christian" last="Mueller">Christian Mueller</name>
</author>
<author><name sortKey="Schumann, Gunter" sort="Schumann, Gunter" uniqKey="Schumann G" first="Gunter" last="Schumann">Gunter Schumann</name>
</author>
</analytic>
<series><title level="j">Journal of Psychiatry & Neuroscience : JPN</title>
<idno type="ISSN">1180-4882</idno>
<idno type="eISSN">1488-2434</idno>
<imprint><date when="2015">2015</date>
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<front><div type="abstract" xml:lang="en"><sec><title>Background</title>
<p>The mesolimbic dopamine system, composed primarily of dopaminergic neurons in the ventral tegmental area that project to striatal structures, is considered to be the key mediator of reinforcement-related mechanisms in the brain. Prompted by a genome-wide association meta-analysis implicating the Ras-specific guanine nucleotide-releasing factor 2 (<italic>RASGRF2</italic>
) gene in the regulation of alcohol intake in men, we have recently shown that male <italic>Rasgrf2</italic>
<sup>−/−</sup>
mice exhibit reduced ethanol intake and preference accompanied by a perturbed mesolimbic dopamine system. We therefore propose that these mice represent a valid model to further elucidate the precise genes and mechanisms regulating mesolimbic dopamine functioning.</p>
</sec>
<sec><title>Methods</title>
<p>Transcriptomic data from the nucleus accumbens (NAcc) of male <italic>Rasgrf2</italic>
<sup>−/−</sup>
mice and wild-type controls were analyzed by weighted gene coexpression network analysis (WGCNA). We performed follow-up genetic association tests in humans using a sample of male adolescents from the IMAGEN study characterized for binge drinking (<italic>n</italic>
= 905) and ventral striatal activation during an fMRI reward task (<italic>n</italic>
= 608).</p>
</sec>
<sec><title>Results</title>
<p>The WGCNA analyses using accumbal transcriptomic data revealed 37 distinct “modules,” or functionally related groups of genes. Two of these modules were significantly associated with <italic>Rasgrf2</italic>
knockout status: M5 (<italic>p</italic>
< 0.001) and M6 (<italic>p</italic>
< 0.001). In follow-up translational analyses we found that human orthologues for the M5 module were significantly (<italic>p</italic>
< 0.01) enriched with genetic association signals for binge drinking in male adolescents. Furthermore, the most significant locus, originating from the EH-domain containing 4 (<italic>EHD4</italic>
) gene (<italic>p</italic>
< 0.001), was also significantly associated with altered ventral striatal activity in male adolescents performing an fMRI reward task (<italic>p</italic>
<sub>empirical</sub>
< 0.001).</p>
</sec>
<sec><title>Limitations</title>
<p>It was not possible to determine the extent to which the M5 module was dysregulated in <italic>Rasgrf2</italic>
<sup>−/−</sup>
mice by perturbed mesolimbic dopamine signalling or by the loss of <italic>Rasgrf2</italic>
function in the NAcc.</p>
</sec>
<sec><title>Conclusion</title>
<p>Taken together, our findings indicate that the accumbal M5 module, initially identified as being dysregulated in male <italic>Rasgrf2</italic>
<sup>−/−</sup>
mice, is also relevant for human alcohol-related phenotypes potentially through the modulation of reinforcement mechanisms in the NAcc. We therefore propose that the genes comprising this module represent important candidates for further elucidation within the context of alcohol-related phenotypes.</p>
</sec>
</div>
</front>
</TEI>
<affiliations><list></list>
<tree><noCountry><name sortKey="Banaschewski, Tobias" sort="Banaschewski, Tobias" uniqKey="Banaschewski T" first="Tobias" last="Banaschewski">Tobias Banaschewski</name>
<name sortKey="Band, Hamid" sort="Band, Hamid" uniqKey="Band H" first="Hamid" last="Band">Hamid Band</name>
<name sortKey="Barker, Gareth" sort="Barker, Gareth" uniqKey="Barker G" first="Gareth" last="Barker">Gareth Barker</name>
<name sortKey="Bhattacharyya, Sohinee" sort="Bhattacharyya, Sohinee" uniqKey="Bhattacharyya S" first="Sohinee" last="Bhattacharyya">Sohinee Bhattacharyya</name>
<name sortKey="Bokde, Arun" sort="Bokde, Arun" uniqKey="Bokde A" first="Arun" last="Bokde">Arun Bokde</name>
<name sortKey="Buchel, Christian" sort="Buchel, Christian" uniqKey="Buchel C" first="Christian" last="Buchel">Christian Buchel</name>
<name sortKey="Carvalho, Fabiana" sort="Carvalho, Fabiana" uniqKey="Carvalho F" first="Fabiana" last="Carvalho">Fabiana Carvalho</name>
<name sortKey="Cattrell, Anna" sort="Cattrell, Anna" uniqKey="Cattrell A" first="Anna" last="Cattrell">Anna Cattrell</name>
<name sortKey="Conrod, Patricia" sort="Conrod, Patricia" uniqKey="Conrod P" first="Patricia" last="Conrod">Patricia Conrod</name>
<name sortKey="Desrivieres, Sylvane" sort="Desrivieres, Sylvane" uniqKey="Desrivieres S" first="Sylvane" last="Desrivieres">Sylvane Desrivieres</name>
<name sortKey="Easton, Alanna" sort="Easton, Alanna" uniqKey="Easton A" first="Alanna" last="Easton">Alanna Easton</name>
<name sortKey="Fauth Buehler, Mira" sort="Fauth Buehler, Mira" uniqKey="Fauth Buehler M" first="Mira" last="Fauth-Buehler">Mira Fauth-Buehler</name>
<name sortKey="Fernandez Medarde, Alberto" sort="Fernandez Medarde, Alberto" uniqKey="Fernandez Medarde A" first="Alberto" last="Fernandez-Medarde">Alberto Fernandez-Medarde</name>
<name sortKey="Flor, Herta" sort="Flor, Herta" uniqKey="Flor H" first="Herta" last="Flor">Herta Flor</name>
<name sortKey="Frouin, Vincent" sort="Frouin, Vincent" uniqKey="Frouin V" first="Vincent" last="Frouin">Vincent Frouin</name>
<name sortKey="Gallinat, Jurgen" sort="Gallinat, Jurgen" uniqKey="Gallinat J" first="Jurgen" last="Gallinat">Jurgen Gallinat</name>
<name sortKey="Garavanh, Hugh" sort="Garavanh, Hugh" uniqKey="Garavanh H" first="Hugh" last="Garavanh">Hugh Garavanh</name>
<name sortKey="Girault, Jean Antoine" sort="Girault, Jean Antoine" uniqKey="Girault J" first="Jean-Antoine" last="Girault">Jean-Antoine Girault</name>
<name sortKey="Heinz, Andreas" sort="Heinz, Andreas" uniqKey="Heinz A" first="Andreas" last="Heinz">Andreas Heinz</name>
<name sortKey="Ittermann, Bernd" sort="Ittermann, Bernd" uniqKey="Ittermann B" first="Bernd" last="Ittermann">Bernd Ittermann</name>
<name sortKey="Jia, Tianye" sort="Jia, Tianye" uniqKey="Jia T" first="Tianye" last="Jia">Tianye Jia</name>
<name sortKey="Lathrop, Mark" sort="Lathrop, Mark" uniqKey="Lathrop M" first="Mark" last="Lathrop">Mark Lathrop</name>
<name sortKey="Lawrence, Claire" sort="Lawrence, Claire" uniqKey="Lawrence C" first="Claire" last="Lawrence">Claire Lawrence</name>
<name sortKey="Loth, Eva" sort="Loth, Eva" uniqKey="Loth E" first="Eva" last="Loth">Eva Loth</name>
<name sortKey="Lourdusamy, Anbarasu" sort="Lourdusamy, Anbarasu" uniqKey="Lourdusamy A" first="Anbarasu" last="Lourdusamy">Anbarasu Lourdusamy</name>
<name sortKey="Mameli, Manuel" sort="Mameli, Manuel" uniqKey="Mameli M" first="Manuel" last="Mameli">Manuel Mameli</name>
<name sortKey="Mann, Karl" sort="Mann, Karl" uniqKey="Mann K" first="Karl" last="Mann">Karl Mann</name>
<name sortKey="Maroteaux, Matthieu" sort="Maroteaux, Matthieu" uniqKey="Maroteaux M" first="Matthieu" last="Maroteaux">Matthieu Maroteaux</name>
<name sortKey="Martinot, Jean Luc" sort="Martinot, Jean Luc" uniqKey="Martinot J" first="Jean-Luc" last="Martinot">Jean-Luc Martinot</name>
<name sortKey="Mueller, Christian" sort="Mueller, Christian" uniqKey="Mueller C" first="Christian" last="Mueller">Christian Mueller</name>
<name sortKey="Nees, Frauke" sort="Nees, Frauke" uniqKey="Nees F" first="Frauke" last="Nees">Frauke Nees</name>
<name sortKey="Nymberg, Charlotte" sort="Nymberg, Charlotte" uniqKey="Nymberg C" first="Charlotte" last="Nymberg">Charlotte Nymberg</name>
<name sortKey="Paus, Tomas" sort="Paus, Tomas" uniqKey="Paus T" first="Tomas" last="Paus">Tomas Paus</name>
<name sortKey="Pausova, Zdenka" sort="Pausova, Zdenka" uniqKey="Pausova Z" first="Zdenka" last="Pausova">Zdenka Pausova</name>
<name sortKey="Rietschel, Marcella" sort="Rietschel, Marcella" uniqKey="Rietschel M" first="Marcella" last="Rietschel">Marcella Rietschel</name>
<name sortKey="Rotter, Andrea" sort="Rotter, Andrea" uniqKey="Rotter A" first="Andrea" last="Rotter">Andrea Rotter</name>
<name sortKey="Ruggeri, Barbara" sort="Ruggeri, Barbara" uniqKey="Ruggeri B" first="Barbara" last="Ruggeri">Barbara Ruggeri</name>
<name sortKey="Santos, Eugenio" sort="Santos, Eugenio" uniqKey="Santos E" first="Eugenio" last="Santos">Eugenio Santos</name>
<name sortKey="Schumann, Gunter" sort="Schumann, Gunter" uniqKey="Schumann G" first="Gunter" last="Schumann">Gunter Schumann</name>
<name sortKey="Smolka, Michael" sort="Smolka, Michael" uniqKey="Smolka M" first="Michael" last="Smolka">Michael Smolka</name>
<name sortKey="Sommer, Wolfgang" sort="Sommer, Wolfgang" uniqKey="Sommer W" first="Wolfgang" last="Sommer">Wolfgang Sommer</name>
<name sortKey="Spanagel, Rainer" sort="Spanagel, Rainer" uniqKey="Spanagel R" first="Rainer" last="Spanagel">Rainer Spanagel</name>
<name sortKey="Stacey, David" sort="Stacey, David" uniqKey="Stacey D" first="David" last="Stacey">David Stacey</name>
</noCountry>
</tree>
</affiliations>
</record>
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