The histone demethylase JMJD1A induces cell migration and invasion by up-regulating the expression of the long noncoding RNA MALAT1
Identifieur interne : 003431 ( Main/Exploration ); précédent : 003430; suivant : 003432The histone demethylase JMJD1A induces cell migration and invasion by up-regulating the expression of the long noncoding RNA MALAT1
Auteurs : Andrew E. Tee [Australie] ; Dora Ling [Australie] ; Charlotte Nelson [Australie] ; Bernard Atmadibrata [Australie] ; Marcel E. Dinger [Australie] ; Ning Xu [Australie] ; Tamio Mizukami [Japon] ; Pei Y. Liu [Australie] ; Bing Liu [Australie] ; Belamy Cheung [Australie] ; Eddy Pasquier [Australie, France] ; Michelle Haber [Australie] ; Murray D. Norris [Australie] ; Takayoshi Suzuki [Japon] ; Glenn M. Marshall [Australie] ; Tao Liu [Australie]Source :
- Oncotarget [ 1949-2553 ] ; 2014.
Abstract
Patients with neuroblastoma due to N-Myc oncogene amplification have a high frequency of tumor metastasis. However, it is not clear how N-Myc induces cell migration, invasion and metastasis. The histone demethylase JMJD1A activates gene transcription by demethylating the lysine 9 residue of histone H3 (H3K9) at target gene promoters. The long noncoding RNA MALAT1 induces lung cancer cell migration and plays a pivotal role in lung cancer metastasis. Here we demonstrated that N-Myc up-regulated the expression of JMJD1A in N-Myc oncogene-amplified human neuroblastoma cells by directly binding to the JMJD1A gene promoter. Affymetrix microarray studies revealed that the gene second most significantly up-regulated by JMJD1A was MALAT1. Consistent with this finding, RT-PCR and chromatin immunoprecipitation assays showed that JMJD1A bound to the MALAT1 gene promoter and demethylated histone H3K9 at the MALAT1 gene promoter. Moreover, JMJD1A and MALAT1 induced, while the small molecule JMJD1A inhibitor DMOG suppressed, neuroblastoma cell migration and invasion. Taken together, our data identify a novel pathway through which N-Myc causes neuroblastoma cell migration and invasion, and provide important evidence for further development of more potent JMJD1A/MALAT1 inhibitors for the prevention of tumor metastasis.
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PubMed: 24742640
PubMed Central: 4039110
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Tee</name><affiliation wicri:level="3"><nlm:aff id="A1"> Children's Cancer Institute Australia for Medical Research, Randwick, Sydney, Australia</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea> Children's Cancer Institute Australia for Medical Research, Randwick, Sydney</wicri:regionArea><placeName><settlement type="city">Sydney</settlement><region type="état">Nouvelle-Galles du Sud</region></placeName></affiliation></author><author><name sortKey="Ling, Dora" sort="Ling, Dora" uniqKey="Ling D" first="Dora" last="Ling">Dora Ling</name><affiliation wicri:level="3"><nlm:aff id="A1"> Children's Cancer Institute Australia for Medical Research, Randwick, Sydney, Australia</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea> Children's Cancer Institute Australia for Medical Research, Randwick, Sydney</wicri:regionArea><placeName><settlement type="city">Sydney</settlement><region type="état">Nouvelle-Galles du Sud</region></placeName></affiliation></author><author><name sortKey="Nelson, Charlotte" sort="Nelson, Charlotte" uniqKey="Nelson C" first="Charlotte" last="Nelson">Charlotte Nelson</name><affiliation wicri:level="3"><nlm:aff id="A1"> Children's Cancer Institute Australia for Medical Research, Randwick, Sydney, Australia</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea> Children's Cancer Institute Australia for Medical Research, Randwick, Sydney</wicri:regionArea><placeName><settlement type="city">Sydney</settlement><region type="état">Nouvelle-Galles du Sud</region></placeName></affiliation></author><author><name sortKey="Atmadibrata, Bernard" sort="Atmadibrata, Bernard" uniqKey="Atmadibrata B" first="Bernard" last="Atmadibrata">Bernard Atmadibrata</name><affiliation wicri:level="3"><nlm:aff id="A1"> Children's Cancer Institute Australia for Medical Research, Randwick, Sydney, Australia</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea> Children's Cancer Institute Australia for Medical Research, Randwick, Sydney</wicri:regionArea><placeName><settlement type="city">Sydney</settlement><region type="état">Nouvelle-Galles du Sud</region></placeName></affiliation></author><author><name sortKey="Dinger, Marcel E" sort="Dinger, Marcel E" uniqKey="Dinger M" first="Marcel E." last="Dinger">Marcel E. Dinger</name><affiliation wicri:level="3"><nlm:aff id="A2"> Garvan Institute of Medical Research, Darlinghurst, Sydney, Australia</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea> Garvan Institute of Medical Research, Darlinghurst, Sydney</wicri:regionArea><placeName><settlement type="city">Sydney</settlement><region type="état">Nouvelle-Galles du Sud</region></placeName></affiliation></author><author><name sortKey="Xu, Ning" sort="Xu, Ning" uniqKey="Xu N" first="Ning" last="Xu">Ning Xu</name><affiliation wicri:level="3"><nlm:aff id="A1"> Children's Cancer Institute Australia for Medical Research, Randwick, Sydney, Australia</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea> Children's Cancer Institute Australia for Medical Research, Randwick, Sydney</wicri:regionArea><placeName><settlement type="city">Sydney</settlement><region type="état">Nouvelle-Galles du Sud</region></placeName></affiliation></author><author><name sortKey="Mizukami, Tamio" sort="Mizukami, Tamio" uniqKey="Mizukami T" first="Tamio" last="Mizukami">Tamio Mizukami</name><affiliation wicri:level="1"><nlm:aff id="A3"> Graduate School of Bio-Science, Nagahama Institute of Bio-Science and Technology, Nagahama, Shiga, Japan</nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea> Graduate School of Bio-Science, Nagahama Institute of Bio-Science and Technology, Nagahama, Shiga</wicri:regionArea><wicri:noRegion>Shiga</wicri:noRegion></affiliation></author><author><name sortKey="Liu, Pei Y" sort="Liu, Pei Y" uniqKey="Liu P" first="Pei Y." last="Liu">Pei Y. Liu</name><affiliation wicri:level="3"><nlm:aff id="A1"> Children's Cancer Institute Australia for Medical Research, Randwick, Sydney, Australia</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea> Children's Cancer Institute Australia for Medical Research, Randwick, Sydney</wicri:regionArea><placeName><settlement type="city">Sydney</settlement><region type="état">Nouvelle-Galles du Sud</region></placeName></affiliation></author><author><name sortKey="Liu, Bing" sort="Liu, Bing" uniqKey="Liu B" first="Bing" last="Liu">Bing Liu</name><affiliation wicri:level="3"><nlm:aff id="A1"> Children's Cancer Institute Australia for Medical Research, Randwick, Sydney, Australia</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea> Children's Cancer Institute Australia for Medical Research, Randwick, Sydney</wicri:regionArea><placeName><settlement type="city">Sydney</settlement><region type="état">Nouvelle-Galles du Sud</region></placeName></affiliation></author><author><name sortKey="Cheung, Belamy" sort="Cheung, Belamy" uniqKey="Cheung B" first="Belamy" last="Cheung">Belamy Cheung</name><affiliation wicri:level="3"><nlm:aff id="A1"> Children's Cancer Institute Australia for Medical Research, Randwick, Sydney, Australia</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea> Children's Cancer Institute Australia for Medical Research, Randwick, Sydney</wicri:regionArea><placeName><settlement type="city">Sydney</settlement><region type="état">Nouvelle-Galles du Sud</region></placeName></affiliation></author><author><name sortKey="Pasquier, Eddy" sort="Pasquier, Eddy" uniqKey="Pasquier E" first="Eddy" last="Pasquier">Eddy Pasquier</name><affiliation wicri:level="3"><nlm:aff id="A1"> Children's Cancer Institute Australia for Medical Research, Randwick, Sydney, Australia</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea> Children's Cancer Institute Australia for Medical Research, Randwick, Sydney</wicri:regionArea><placeName><settlement type="city">Sydney</settlement><region type="état">Nouvelle-Galles du Sud</region></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="A4"> Metronomics Global Health Initiative, Marseille, France</nlm:aff><country xml:lang="fr">France</country><wicri:regionArea> Metronomics Global Health Initiative, Marseille</wicri:regionArea><placeName><region type="region">Provence-Alpes-Côte d'Azur</region><region type="old region">Provence-Alpes-Côte d'Azur</region><settlement type="city">Marseille</settlement></placeName></affiliation></author><author><name sortKey="Haber, Michelle" sort="Haber, Michelle" uniqKey="Haber M" first="Michelle" last="Haber">Michelle Haber</name><affiliation wicri:level="3"><nlm:aff id="A1"> Children's Cancer Institute Australia for Medical Research, Randwick, Sydney, Australia</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea> Children's Cancer Institute Australia for Medical Research, Randwick, Sydney</wicri:regionArea><placeName><settlement type="city">Sydney</settlement><region type="état">Nouvelle-Galles du Sud</region></placeName></affiliation></author><author><name sortKey="Norris, Murray D" sort="Norris, Murray D" uniqKey="Norris M" first="Murray D." last="Norris">Murray D. Norris</name><affiliation wicri:level="3"><nlm:aff id="A1"> Children's Cancer Institute Australia for Medical Research, Randwick, Sydney, Australia</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea> Children's Cancer Institute Australia for Medical Research, Randwick, Sydney</wicri:regionArea><placeName><settlement type="city">Sydney</settlement><region type="état">Nouvelle-Galles du Sud</region></placeName></affiliation></author><author><name sortKey="Suzuki, Takayoshi" sort="Suzuki, Takayoshi" uniqKey="Suzuki T" first="Takayoshi" last="Suzuki">Takayoshi Suzuki</name><affiliation wicri:level="1"><nlm:aff id="A5"> Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Taishogun Nishitakatsukasa-Cho, Kita-ku, Kyoto, Japan</nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea> Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Taishogun Nishitakatsukasa-Cho, Kita-ku, Kyoto</wicri:regionArea><wicri:noRegion>Kyoto</wicri:noRegion></affiliation></author><author><name sortKey="Marshall, Glenn M" sort="Marshall, Glenn M" uniqKey="Marshall G" first="Glenn M." last="Marshall">Glenn M. Marshall</name><affiliation wicri:level="3"><nlm:aff id="A1"> Children's Cancer Institute Australia for Medical Research, Randwick, Sydney, Australia</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea> Children's Cancer Institute Australia for Medical Research, Randwick, Sydney</wicri:regionArea><placeName><settlement type="city">Sydney</settlement><region type="état">Nouvelle-Galles du Sud</region></placeName></affiliation><affiliation wicri:level="1"><nlm:aff id="A6"> Kids Cancer Centre, Sydney Children's Hospital, Randwick, , Australia</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea> Kids Cancer Centre, Sydney Children's Hospital, Randwick, </wicri:regionArea><wicri:noRegion></wicri:noRegion></affiliation></author><author><name sortKey="Liu, Tao" sort="Liu, Tao" uniqKey="Liu T" first="Tao" last="Liu">Tao Liu</name><affiliation wicri:level="3"><nlm:aff id="A1"> Children's Cancer Institute Australia for Medical Research, Randwick, Sydney, Australia</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea> Children's Cancer Institute Australia for Medical Research, Randwick, Sydney</wicri:regionArea><placeName><settlement type="city">Sydney</settlement><region type="état">Nouvelle-Galles du Sud</region></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="A7"> School of Women's & Children's Health, UNSW Medicine, University of New South Wales, Randwick, Sydney, Australia</nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea> School of Women's & Children's Health, UNSW Medicine, University of New South Wales, Randwick, Sydney</wicri:regionArea><placeName><settlement type="city">Sydney</settlement><region type="état">Nouvelle-Galles du Sud</region></placeName></affiliation></author></analytic><series><title level="j">Oncotarget</title><idno type="eISSN">1949-2553</idno><imprint><date when="2014">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Patients with neuroblastoma due to N-Myc oncogene amplification have a high frequency of tumor metastasis. However, it is not clear how N-Myc induces cell migration, invasion and metastasis. The histone demethylase JMJD1A activates gene transcription by demethylating the lysine 9 residue of histone H3 (H3K9) at target gene promoters. The long noncoding RNA MALAT1 induces lung cancer cell migration and plays a pivotal role in lung cancer metastasis. Here we demonstrated that N-Myc up-regulated the expression of JMJD1A in N-Myc oncogene-amplified human neuroblastoma cells by directly binding to the JMJD1A gene promoter. Affymetrix microarray studies revealed that the gene second most significantly up-regulated by JMJD1A was MALAT1. Consistent with this finding, RT-PCR and chromatin immunoprecipitation assays showed that JMJD1A bound to the MALAT1 gene promoter and demethylated histone H3K9 at the MALAT1 gene promoter. Moreover, JMJD1A and MALAT1 induced, while the small molecule JMJD1A inhibitor DMOG suppressed, neuroblastoma cell migration and invasion. Taken together, our data identify a novel pathway through which N-Myc causes neuroblastoma cell migration and invasion, and provide important evidence for further development of more potent JMJD1A/MALAT1 inhibitors for the prevention of tumor metastasis.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Brodeur, Gm" uniqKey="Brodeur G">GM Brodeur</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Maris, Jm" uniqKey="Maris J">JM Maris</name></author><author><name sortKey="Matthay, Kk" uniqKey="Matthay K">KK Matthay</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Eilers, M" uniqKey="Eilers M">M Eilers</name></author><author><name sortKey="Eisenman, Rn" uniqKey="Eisenman R">RN Eisenman</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Meyer, N" uniqKey="Meyer N">N Meyer</name></author><author><name sortKey="Penn, Lz" uniqKey="Penn 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sortKey="Iismaa, Se" uniqKey="Iismaa S">SE Iismaa</name></author><author><name sortKey="Liu, T" uniqKey="Liu T">T Liu</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Liu, T" uniqKey="Liu T">T Liu</name></author><author><name sortKey="Liu, Py" uniqKey="Liu P">PY Liu</name></author><author><name sortKey="Tee, Ae" uniqKey="Tee A">AE Tee</name></author><author><name sortKey="Haber, M" uniqKey="Haber M">M Haber</name></author><author><name sortKey="Norris, Md" uniqKey="Norris M">MD Norris</name></author><author><name sortKey="Gleave, Me" uniqKey="Gleave M">ME Gleave</name></author><author><name sortKey="Marshall, Gm" uniqKey="Marshall G">GM Marshall</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Liu, T" uniqKey="Liu T">T Liu</name></author><author><name sortKey="Tee, Ael" uniqKey="Tee A">AEL Tee</name></author><author><name sortKey="Porro, A" uniqKey="Porro A">A Porro</name></author><author><name sortKey="Smith, Sa" uniqKey="Smith S">SA Smith</name></author><author><name sortKey="Dwarte, T" uniqKey="Dwarte T">T Dwarte</name></author><author><name sortKey="Liu, Py" uniqKey="Liu P">PY Liu</name></author><author><name sortKey="Iraci, N" uniqKey="Iraci N">N Iraci</name></author><author><name sortKey="Sekyere, E" uniqKey="Sekyere E">E Sekyere</name></author><author><name sortKey="Haber, M" uniqKey="Haber M">M Haber</name></author><author><name sortKey="Norris, Md" uniqKey="Norris M">MD Norris</name></author><author><name sortKey="Diolaiti, D" uniqKey="Diolaiti D">D Diolaiti</name></author><author><name sortKey="Della Valle, G" uniqKey="Della Valle G">G Della Valle</name></author><author><name sortKey="Perini, G" uniqKey="Perini G">G Perini</name></author><author><name sortKey="Marshall, Gm" uniqKey="Marshall G">GM Marshall</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kawamura, A" uniqKey="Kawamura A">A Kawamura</name></author><author><name sortKey="Tumber, A" uniqKey="Tumber A">A Tumber</name></author><author><name sortKey="Rose, Nr" uniqKey="Rose N">NR Rose</name></author><author><name sortKey="King, On" uniqKey="King O">ON King</name></author><author><name sortKey="Daniel, M" uniqKey="Daniel M">M Daniel</name></author><author><name sortKey="Oppermann, U" uniqKey="Oppermann U">U Oppermann</name></author><author><name sortKey="Heightman, Td" uniqKey="Heightman T">TD Heightman</name></author><author><name sortKey="Schofield, C" uniqKey="Schofield C">C Schofield</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hamada, S" uniqKey="Hamada S">S Hamada</name></author><author><name sortKey="Suzuki, T" uniqKey="Suzuki T">T Suzuki</name></author><author><name sortKey="Mino, K" uniqKey="Mino K">K Mino</name></author><author><name sortKey="Koseki, K" uniqKey="Koseki K">K Koseki</name></author><author><name sortKey="Oehme, F" uniqKey="Oehme F">F Oehme</name></author><author><name sortKey="Flamme, I" uniqKey="Flamme I">I Flamme</name></author><author><name sortKey="Ozasa, H" uniqKey="Ozasa H">H Ozasa</name></author><author><name sortKey="Itoh, Y" uniqKey="Itoh Y">Y Itoh</name></author><author><name sortKey="Ogasawara, D" uniqKey="Ogasawara D">D Ogasawara</name></author><author><name sortKey="Komaarashi, H" uniqKey="Komaarashi H">H Komaarashi</name></author><author><name sortKey="Kato, A" uniqKey="Kato A">A Kato</name></author><author><name sortKey="Tsumoto, H" uniqKey="Tsumoto H">H Tsumoto</name></author><author><name sortKey="Nakagawa, H" uniqKey="Nakagawa H">H Nakagawa</name></author><author><name sortKey="Hasegawa, M" uniqKey="Hasegawa M">M Hasegawa</name></author><author><name sortKey="Sasaki, R" uniqKey="Sasaki R">R Sasaki</name></author><author><name sortKey="Mizukami, T" uniqKey="Mizukami T">T Mizukami</name></author></analytic></biblStruct></listBibl></div1></back></TEI><affiliations><list><country><li>Australie</li><li>France</li><li>Japon</li></country><region><li>Nouvelle-Galles du Sud</li><li>Provence-Alpes-Côte d'Azur</li></region><settlement><li>Marseille</li><li>Sydney</li></settlement></list><tree><country name="Australie"><region name="Nouvelle-Galles du Sud"><name sortKey="Tee, Andrew E" sort="Tee, Andrew E" uniqKey="Tee A" first="Andrew E." last="Tee">Andrew E. Tee</name></region><name sortKey="Atmadibrata, Bernard" sort="Atmadibrata, Bernard" uniqKey="Atmadibrata B" first="Bernard" last="Atmadibrata">Bernard Atmadibrata</name><name sortKey="Cheung, Belamy" sort="Cheung, Belamy" uniqKey="Cheung B" first="Belamy" last="Cheung">Belamy Cheung</name><name sortKey="Dinger, Marcel E" sort="Dinger, Marcel E" uniqKey="Dinger M" first="Marcel E." last="Dinger">Marcel E. Dinger</name><name sortKey="Haber, Michelle" sort="Haber, Michelle" uniqKey="Haber M" first="Michelle" last="Haber">Michelle Haber</name><name sortKey="Ling, Dora" sort="Ling, Dora" uniqKey="Ling D" first="Dora" last="Ling">Dora Ling</name><name sortKey="Liu, Bing" sort="Liu, Bing" uniqKey="Liu B" first="Bing" last="Liu">Bing Liu</name><name sortKey="Liu, Pei Y" sort="Liu, Pei Y" uniqKey="Liu P" first="Pei Y." last="Liu">Pei Y. Liu</name><name sortKey="Liu, Tao" sort="Liu, Tao" uniqKey="Liu T" first="Tao" last="Liu">Tao Liu</name><name sortKey="Liu, Tao" sort="Liu, Tao" uniqKey="Liu T" first="Tao" last="Liu">Tao Liu</name><name sortKey="Marshall, Glenn M" sort="Marshall, Glenn M" uniqKey="Marshall G" first="Glenn M." last="Marshall">Glenn M. Marshall</name><name sortKey="Marshall, Glenn M" sort="Marshall, Glenn M" uniqKey="Marshall G" first="Glenn M." last="Marshall">Glenn M. Marshall</name><name sortKey="Nelson, Charlotte" sort="Nelson, Charlotte" uniqKey="Nelson C" first="Charlotte" last="Nelson">Charlotte Nelson</name><name sortKey="Norris, Murray D" sort="Norris, Murray D" uniqKey="Norris M" first="Murray D." last="Norris">Murray D. Norris</name><name sortKey="Pasquier, Eddy" sort="Pasquier, Eddy" uniqKey="Pasquier E" first="Eddy" last="Pasquier">Eddy Pasquier</name><name sortKey="Xu, Ning" sort="Xu, Ning" uniqKey="Xu N" first="Ning" last="Xu">Ning Xu</name></country><country name="Japon"><noRegion><name sortKey="Mizukami, Tamio" sort="Mizukami, Tamio" uniqKey="Mizukami T" first="Tamio" last="Mizukami">Tamio Mizukami</name></noRegion><name sortKey="Suzuki, Takayoshi" sort="Suzuki, Takayoshi" uniqKey="Suzuki T" first="Takayoshi" last="Suzuki">Takayoshi Suzuki</name></country><country name="France"><region name="Provence-Alpes-Côte d'Azur"><name sortKey="Pasquier, Eddy" sort="Pasquier, Eddy" uniqKey="Pasquier E" first="Eddy" last="Pasquier">Eddy Pasquier</name></region></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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