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<article article-type="research-article" dtd-version="1.3" xmlns:mml="http://www.w3.org/1998/Math/MathML" xmlns:xlink="http://www.w3.org/1999/xlink" xmlns:xsi="http://www.w3.org/2001/XMLSchema-instance" xml:lang="ru"><front><journal-meta><journal-id journal-id-type="publisher-id">vavilov</journal-id><journal-title-group><journal-title xml:lang="ru">Вавиловский журнал генетики и селекции</journal-title><trans-title-group xml:lang="en"><trans-title>Vavilov Journal of Genetics and Breeding</trans-title></trans-title-group></journal-title-group><issn pub-type="epub">2500-3259</issn><publisher><publisher-name>Institute of Cytology and Genetics of Siberian Branch of the RAS</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="doi">10.18699/VJ19.477</article-id><article-id custom-type="elpub" pub-id-type="custom">vavilov-1929</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="section-heading" xml:lang="ru"><subject>ЭПИГЕНЕТИКА</subject></subj-group><subj-group subj-group-type="section-heading" xml:lang="en"><subject>EPIGENETICS</subject></subj-group></article-categories><title-group><article-title>Функциональные свойства Su(Hw)-зависимого комплекса определяются его регуляторным окружением  и множественными взаимодействиями  на белковой платформе Su(Hw)</article-title><trans-title-group xml:lang="en"><trans-title>Functional properties of the Su(Hw) complex  are determined by its regulatory environment  and multiple interactions on the Su(Hw) protein platform</trans-title></trans-title-group></title-group><contrib-group><contrib contrib-type="author" corresp="yes"><name-alternatives><name name-style="eastern" xml:lang="ru"><surname>Мельникова</surname><given-names>Л. С.</given-names></name><name name-style="western" xml:lang="en"><surname>Melnikova</surname><given-names>L. S.</given-names></name></name-alternatives><bio xml:lang="ru"><p>Москва.</p></bio><bio xml:lang="en"><p>Moscow.</p></bio><email xlink:type="simple">lsm73@mail.ru</email><xref ref-type="aff" rid="aff-1"/></contrib><contrib contrib-type="author" corresp="yes"><name-alternatives><name name-style="eastern" xml:lang="ru"><surname>Костюченко</surname><given-names>М. В.</given-names></name><name name-style="western" xml:lang="en"><surname>Kostyuchenko</surname><given-names>M. V.</given-names></name></name-alternatives><bio xml:lang="ru"><p>Москва.</p></bio><bio xml:lang="en"><p>Moscow.</p></bio><xref ref-type="aff" rid="aff-1"/></contrib><contrib contrib-type="author" corresp="yes"><name-alternatives><name name-style="eastern" xml:lang="ru"><surname>Молодина</surname><given-names>В. В.</given-names></name><name name-style="western" xml:lang="en"><surname>Molodina</surname><given-names>V. V.</given-names></name></name-alternatives><bio xml:lang="ru"><p>Москва.</p></bio><bio xml:lang="en"><p>Moscow.</p></bio><xref ref-type="aff" rid="aff-1"/></contrib><contrib contrib-type="author" corresp="yes"><name-alternatives><name name-style="eastern" xml:lang="ru"><surname>Георгиев</surname><given-names>П. Г.</given-names></name><name name-style="western" xml:lang="en"><surname>Georgiev</surname><given-names>P. G.</given-names></name></name-alternatives><bio xml:lang="ru"><p>Москва.</p></bio><bio xml:lang="en"><p>Moscow.</p></bio><xref ref-type="aff" rid="aff-1"/></contrib><contrib contrib-type="author" corresp="yes"><name-alternatives><name name-style="eastern" xml:lang="ru"><surname>Головнин</surname><given-names>А. К.</given-names></name><name name-style="western" xml:lang="en"><surname>Golovnin</surname><given-names>A. K.</given-names></name></name-alternatives><bio xml:lang="ru"><p>Москва.</p></bio><bio xml:lang="en"><p>Moscow.</p></bio><xref ref-type="aff" rid="aff-1"/></contrib></contrib-group><aff-alternatives id="aff-1"><aff xml:lang="ru">Институт биологии гена Российской академии наук.<country>Россия</country></aff><aff xml:lang="en">Institute of Gene Biology, RAS.<country>Russian Federation</country></aff></aff-alternatives><pub-date pub-type="collection"><year>2019</year></pub-date><pub-date pub-type="epub"><day>28</day><month>03</month><year>2019</year></pub-date><volume>23</volume><issue>2</issue><fpage>168</fpage><lpage>173</lpage><permissions><copyright-statement>Copyright &amp;#x00A9; Мельникова Л.С., Костюченко М.В., Молодина В.В., Георгиев П.Г., Головнин А.К., 2019</copyright-statement><copyright-year>2019</copyright-year><copyright-holder xml:lang="ru">Мельникова Л.С., Костюченко М.В., Молодина В.В., Георгиев П.Г., Головнин А.К.</copyright-holder><copyright-holder xml:lang="en">Melnikova L.S., Kostyuchenko M.V., Molodina V.V., Georgiev P.G., Golovnin A.K.</copyright-holder><license license-type="creative-commons-attribution" xlink:href="https://creativecommons.org/licenses/by/4.0/" xlink:type="simple"><license-p>This work is licensed under a Creative Commons Attribution 4.0 License.</license-p></license></permissions><self-uri xlink:href="https://vavilov.elpub.ru/jour/article/view/1929">https://vavilov.elpub.ru/jour/article/view/1929</self-uri><abstract><p>Белок Su(Hw) был впервые идентифицирован как ДНК-связывающий компонент инсуляторного комплекса. Инсуляторы представляют собой регуляторные элементы, которые могут блокировать энхансер-промоторные взаимодействия и работать как границы между активным и репрессивным хроматином. Su(Hw)-зави симый белковый комплекс – уникальная модель для изучения инсуляторов, поскольку основные структурные компоненты, влияющие на его активность, уже известны. Однако механизмы, вовлекающие этот комплекс в различные регуляторные процессы, и детали взаимодействий между компонентами Su(Hw) инсуляторов остаются недостаточно изученными. Наши недавние работы выявили детальный механизм формирования и функционирования инсулятора Su(Hw). В представленном обзоре мы демонстрируем, как множественные взаимодействия между основными компонентами Su(Hw)-зависимого комплекса (Su(Hw)/ Mod(mdg4)-67.2/CP190) влияют на его активность. Показываем, что Su(Hw) может регулировать энхансерпромоторные взаимодействия через новый механизм нейтрализации инсулятора и, корме того, участвует в прямой регуляции активности близлежащих промоторов. Наконец, мы описываем механизм формирования «инсуляторных телец» и предлагаем модель, объясняющую их роль в рекрутировании Su(Hw)-зависимого комплекса на хроматин.</p></abstract><trans-abstract xml:lang="en"><p>The Su(Hw) protein was first identified as a DNA-binding component of an insulator complex in Drosophila. Insulators are regulatory elements that can block the enhancer-promoter communication and exhibit boundary activity. Some insulator complexes contribute to the higher-order organization of chromatin in topologically associated domains that are fundamental elements of the eukaryotic genomic structure. The Su(Hw)-dependent protein complex is a unique model for studying the insulator, since its basic structural components affecting its activity are already known. However, the mechanisms involving this complex in various regulatory processes and the precise interaction between the components of the Su(Hw) insulators remain poorly understood. Our recent studies reveal the fine mechanism of formation and function of the Su(Hw) insulator. Our results provide, for the first time, an example of a high complexity of interactions between the insulator proteins that are required to form the (Su(Hw)/Mod(mdg4)-67.2/CP190) complex. All interactions between the proteins are to a greater or lesser extent redundant, which increases the reliability of the complex formation. We conclude that both association with CP190 and Mod(mdg4)-67.2 partners and the proper organization of the DNA binding site are essential for the efficient recruitment of the Su(Hw) complex to chromatin insulators. In this review, we demonstrate the role of multiple interactions between the major components of the Su(Hw) insulator complex (Su(Hw)/Mod(mdg4)-67.2/CP190) in its activity. It was shown that Su(Hw) may regulate the enhancer–promoter communication via the newly described insulator neutralization mechanism. Moreover, Su(Hw) participates in direct regulation of activity of vicinity promoters. Finally, we demonstrate the mechanism of organization of “insulator bodies” and suggest a model describing their role in proper binding of the Su(Hw) complex to chromatin.</p></trans-abstract><kwd-group xml:lang="ru"><kwd>Su(Hw)</kwd><kwd>Mod(mdg4)-67.2</kwd><kwd>CP190</kwd><kwd>регуляция транскрипции</kwd><kwd>инсуляция</kwd><kwd>инсуляторные тельца</kwd><kwd>белок-белковые взаимодействия</kwd></kwd-group><kwd-group xml:lang="en"><kwd>Su(Hw)</kwd><kwd>Mod(mdg4)-67.2</kwd><kwd>CP190</kwd><kwd>transcription regulation</kwd><kwd>insulation</kwd><kwd>insulator bodies</kwd><kwd>protein-protein interactions.</kwd></kwd-group></article-meta></front><back><ref-list><title>References</title><ref id="cit1"><label>1</label><citation-alternatives><mixed-citation xml:lang="ru">Baxley R.M., Bullard J.D., Klein M.W., Fell A.G., Morales-Rosa- do J.A., Duan T., Geyer P.K. Deciphering the DNA code for the function of the Drosophila polydactyl zinc finger protein Suppres-sor of Hairy-wing. Nucleic Acids Res. 2017;45(8):4463-4478. DOI 10.1093/nar/gkx040.</mixed-citation><mixed-citation xml:lang="en">Baxley R.M., Bullard J.D., Klein M.W., Fell A.G., Morales-Rosa- do J.A., Duan T., Geyer P.K. Deciphering the DNA code for the function of the Drosophila polydactyl zinc finger protein Suppres-sor of Hairy-wing. Nucleic Acids Res. 2017;45(8):4463-4478. DOI 10.1093/nar/gkx040.</mixed-citation></citation-alternatives></ref><ref id="cit2"><label>2</label><citation-alternatives><mixed-citation xml:lang="ru">Bonchuk A., Denisov S., Georgiev P., Maksimenko O. Drosophila BTB/POZ domains of “ttk group” can form multimers and selec-tively interact with each other. J. Mol. Biol. 2011;412(3):423-436. DOI 10.1016/jjmb.2011.07.052.</mixed-citation><mixed-citation xml:lang="en">Bonchuk A., Denisov S., Georgiev P., Maksimenko O. Drosophila BTB/POZ domains of “ttk group” can form multimers and selec-tively interact with each other. J. Mol. Biol. 2011;412(3):423-436. DOI 10.1016/jjmb.2011.07.052.</mixed-citation></citation-alternatives></ref><ref id="cit3"><label>3</label><citation-alternatives><mixed-citation xml:lang="ru">Bonchuk A., Maksimenko O., Kyrchanova O., Ivlieva T., Mogila V, Deshpande G., Wolle D., Schedl P., Georgiev P. Functional role of dimerization and CP190 interacting domains of CTCF protein in Drosophila melanogaster. BMC Biol. 2015; 13:63. DOI 10.1186/ s12915-015-0168-7.</mixed-citation><mixed-citation xml:lang="en">Bonchuk A., Maksimenko O., Kyrchanova O., Ivlieva T., Mogila V, Deshpande G., Wolle D., Schedl P., Georgiev P. Functional role of dimerization and CP190 interacting domains of CTCF protein in Drosophila melanogaster. BMC Biol. 2015; 13:63. DOI 10.1186/ s12915-015-0168-7.</mixed-citation></citation-alternatives></ref><ref id="cit4"><label>4</label><citation-alternatives><mixed-citation xml:lang="ru">Dorn R., Krauss V The modifier of mdg4 locus in Drosophila: function¬al complexity is resolved by trans splicing. Genetica. 2003;117(2-3): 165-177.</mixed-citation><mixed-citation xml:lang="en">Dorn R., Krauss V The modifier of mdg4 locus in Drosophila: function¬al complexity is resolved by trans splicing. Genetica. 2003;117(2-3): 165-177.</mixed-citation></citation-alternatives></ref><ref id="cit5"><label>5</label><citation-alternatives><mixed-citation xml:lang="ru">Gerasimova T.I., Gdula D.A., Gerasimov D.V., Simonova O., Cor- ces V.G. A Drosophila protein that imparts directionality on a chro¬matin insulator is an enhancer of position-effect variegation. Cell. 1995;82(4):587-597.</mixed-citation><mixed-citation xml:lang="en">Gerasimova T.I., Gdula D.A., Gerasimov D.V., Simonova O., Cor- ces V.G. A Drosophila protein that imparts directionality on a chro¬matin insulator is an enhancer of position-effect variegation. Cell. 1995;82(4):587-597.</mixed-citation></citation-alternatives></ref><ref id="cit6"><label>6</label><citation-alternatives><mixed-citation xml:lang="ru">Golovnin A., Biryukova I., Romanova O., Silicheva M., Parshikov A., Savitskaya E., Pirrotta V, Georgiev P. An endogenous Su(Hw) insu-lator separates the yellow gene from the Achaete-scute gene com¬plex in Drosophila. Development. 2003;130(14):3249-3258. Golovnin A., Gause M., Georgieva S., Gracheva E., Georgiev P. The su(Hw) insulator can disrupt enhancer-promoter interactions when located more than 20 kilobases away from the Drosophila achaete- scute complex. Mol Cell. Biol. 1999;19(5):3443-3456.</mixed-citation><mixed-citation xml:lang="en">Golovnin A., Biryukova I., Romanova O., Silicheva M., Parshikov A., Savitskaya E., Pirrotta V, Georgiev P. An endogenous Su(Hw) insu-lator separates the yellow gene from the Achaete-scute gene com¬plex in Drosophila. Development. 2003;130(14):3249-3258. Golovnin A., Gause M., Georgieva S., Gracheva E., Georgiev P. The su(Hw) insulator can disrupt enhancer-promoter interactions when located more than 20 kilobases away from the Drosophila achaete- scute complex. Mol Cell. Biol. 1999;19(5):3443-3456.</mixed-citation></citation-alternatives></ref><ref id="cit7"><label>7</label><citation-alternatives><mixed-citation xml:lang="ru">Golovnin A., Mazur A., Kopantseva M., Kurshakova M., Gulak P.V., Gilmore B., Whitfield W.G., Geyer P, Pirrotta V., Georgiev P. Integ¬rity of the Mod(mdg4)-67.2 BTB domain is critical to insulator func¬tion in Drosophila melanogaster. Mol. Cell. Biol. 2007;27(3):963- 974. DOI 10.1128/MCB.00795-06.</mixed-citation><mixed-citation xml:lang="en">Golovnin A., Mazur A., Kopantseva M., Kurshakova M., Gulak P.V., Gilmore B., Whitfield W.G., Geyer P, Pirrotta V., Georgiev P. Integ¬rity of the Mod(mdg4)-67.2 BTB domain is critical to insulator func¬tion in Drosophila melanogaster. Mol. Cell. Biol. 2007;27(3):963- 974. DOI 10.1128/MCB.00795-06.</mixed-citation></citation-alternatives></ref><ref id="cit8"><label>8</label><citation-alternatives><mixed-citation xml:lang="ru">Golovnin A., Melnick E., Mazur A., Georgiev P. Drosophila Su(Hw) insulator can stimulate transcription of a weakened yellow promoter over a distance. Genetics. 2005; 170(3): 1133-1142. DOI 10.1534/ genetics.104.034587.</mixed-citation><mixed-citation xml:lang="en">Golovnin A., Melnick E., Mazur A., Georgiev P. Drosophila Su(Hw) insulator can stimulate transcription of a weakened yellow promoter over a distance. Genetics. 2005; 170(3): 1133-1142. DOI 10.1534/ genetics.104.034587.</mixed-citation></citation-alternatives></ref><ref id="cit9"><label>9</label><citation-alternatives><mixed-citation xml:lang="ru">Golovnin A., Melnikova L., Shapovalov I., Kostyuchenko M., Geor-giev P. EAST organizes Drosophila insulator proteins in the inter-chromosomal nuclear compartment and modulates CP190 binding to chromatin. PLoS One. 2015;10(10):e0140991. DOI 10.1371/ journal.pone.0140991.</mixed-citation><mixed-citation xml:lang="en">Golovnin A., Melnikova L., Shapovalov I., Kostyuchenko M., Geor-giev P. EAST organizes Drosophila insulator proteins in the inter-chromosomal nuclear compartment and modulates CP190 binding to chromatin. PLoS One. 2015;10(10):e0140991. DOI 10.1371/ journal.pone.0140991.</mixed-citation></citation-alternatives></ref><ref id="cit10"><label>10</label><citation-alternatives><mixed-citation xml:lang="ru">Golovnin A., Melnikova L., Volkov I., Kostuchenko M., Galkin A.V., Georgiev P. ‘Insulator bodies’ are aggregates of proteins but not of insulators. EMBO Rep. 2008;9(5):440-445. DOI 10.1038/embor. 2008.32.</mixed-citation><mixed-citation xml:lang="en">Golovnin A., Melnikova L., Volkov I., Kostuchenko M., Galkin A.V., Georgiev P. ‘Insulator bodies’ are aggregates of proteins but not of insulators. EMBO Rep. 2008;9(5):440-445. DOI 10.1038/embor. 2008.32.</mixed-citation></citation-alternatives></ref><ref id="cit11"><label>11</label><citation-alternatives><mixed-citation xml:lang="ru">Golovnin A., Volkov I., Georgiev P. SUMO conjugation is required for the assembly of Drosophila Su(Hw) and Mod(mdg4) into insula¬tor bodies that facilitate insulator complex formation. J. Cell Sci. 2012;125:2064-2074. DOI 10.1242/jcs.100172.</mixed-citation><mixed-citation xml:lang="en">Golovnin A., Volkov I., Georgiev P. SUMO conjugation is required for the assembly of Drosophila Su(Hw) and Mod(mdg4) into insula¬tor bodies that facilitate insulator complex formation. J. Cell Sci. 2012;125:2064-2074. DOI 10.1242/jcs.100172.</mixed-citation></citation-alternatives></ref><ref id="cit12"><label>12</label><citation-alternatives><mixed-citation xml:lang="ru">Harrison D.A., Gdula D.A., Coyne R.S., Corces V.G. A leucine zip¬per domain of the suppressor of Hairy-wing protein mediates its re-pressive effect on enhancer function. Genes Dev. 1993;7(10):1966- 1978.</mixed-citation><mixed-citation xml:lang="en">Harrison D.A., Gdula D.A., Coyne R.S., Corces V.G. A leucine zip¬per domain of the suppressor of Hairy-wing protein mediates its re-pressive effect on enhancer function. Genes Dev. 1993;7(10):1966- 1978.</mixed-citation></citation-alternatives></ref><ref id="cit13"><label>13</label><citation-alternatives><mixed-citation xml:lang="ru">Kim J., Shen B., Rosen C., Dorsett D. The DNA-binding and enhancer¬blocking domains of the Drosophila suppressor of Hairy-wing pro¬tein. Mol. Cell. Biol. 1996;16(7):3381-3392.</mixed-citation><mixed-citation xml:lang="en">Kim J., Shen B., Rosen C., Dorsett D. The DNA-binding and enhancer¬blocking domains of the Drosophila suppressor of Hairy-wing pro¬tein. Mol. Cell. Biol. 1996;16(7):3381-3392.</mixed-citation></citation-alternatives></ref><ref id="cit14"><label>14</label><citation-alternatives><mixed-citation xml:lang="ru">Krivega M., Savitskaya E., Krivega I., Karakozova M., Parshikov A., Golovnin A., Georgiev P. Interaction between a pair of gypsy in-sulators or between heterologous gypsy and Wari insulators modu¬lates Flp site-specific recombination in Drosophila melanogaster. Chromosoma. 2010;119(4):425-434. DOI 10.1007/s00412-010- 0268-7.</mixed-citation><mixed-citation xml:lang="en">Krivega M., Savitskaya E., Krivega I., Karakozova M., Parshikov A., Golovnin A., Georgiev P. Interaction between a pair of gypsy in-sulators or between heterologous gypsy and Wari insulators modu¬lates Flp site-specific recombination in Drosophila melanogaster. Chromosoma. 2010;119(4):425-434. DOI 10.1007/s00412-010- 0268-7.</mixed-citation></citation-alternatives></ref><ref id="cit15"><label>15</label><citation-alternatives><mixed-citation xml:lang="ru">Kuhn-Parnell E.J., Helou C., Marion D.J., Gilmore B.L., Parnell T.J., Wold M.S., Geyer P.K. Investigation of the properties of non-gypsy suppressor of hairy-wing-binding sites. Genetics. 2008;179(3):1263- 1273. DOI 10.1534/genetics.108.087254.</mixed-citation><mixed-citation xml:lang="en">Kuhn-Parnell E.J., Helou C., Marion D.J., Gilmore B.L., Parnell T.J., Wold M.S., Geyer P.K. Investigation of the properties of non-gypsy suppressor of hairy-wing-binding sites. Genetics. 2008;179(3):1263- 1273. DOI 10.1534/genetics.108.087254.</mixed-citation></citation-alternatives></ref><ref id="cit16"><label>16</label><citation-alternatives><mixed-citation xml:lang="ru">Kyrchanova O., Chetverina D., Maksimenko O., Kullyev A., Geor- giev P. Orientation-dependent interaction between Drosophila in-sulators is a property of this class of regulatory elements. Nucleic Acids Res. 2008;36(22):7019-7028. DOI 10.1093/nar/gkn781.</mixed-citation><mixed-citation xml:lang="en">Kyrchanova O., Chetverina D., Maksimenko O., Kullyev A., Geor- giev P. Orientation-dependent interaction between Drosophila in-sulators is a property of this class of regulatory elements. Nucleic Acids Res. 2008;36(22):7019-7028. DOI 10.1093/nar/gkn781.</mixed-citation></citation-alternatives></ref><ref id="cit17"><label>17</label><citation-alternatives><mixed-citation xml:lang="ru">Lei E.P., Corces V.G. RNA interference machinery influences the nuc¬lear organization of a chromatin insulator. Nat. Genet. 2006;38(8): 936-941. DOI 10.1038/ng1850.</mixed-citation><mixed-citation xml:lang="en">Lei E.P., Corces V.G. RNA interference machinery influences the nuc¬lear organization of a chromatin insulator. Nat. Genet. 2006;38(8): 936-941. DOI 10.1038/ng1850.</mixed-citation></citation-alternatives></ref><ref id="cit18"><label>18</label><citation-alternatives><mixed-citation xml:lang="ru">Maksimenko O., Bartkuhn M., Stakhov V., Herold M., Zolotarev N., Jox T., Buxa M.K., Kirsch R., Bonchuk A., Fedotova A., Kyrcha-nova O., Renkawitz R., Georgiev P. Two new insulator proteins, Pita and ZIPIC, target CP190 to chromatin. Genome Res. 2015;25(1): 89-99. DOI 10.1101/gr.174169.114.</mixed-citation><mixed-citation xml:lang="en">Maksimenko O., Bartkuhn M., Stakhov V., Herold M., Zolotarev N., Jox T., Buxa M.K., Kirsch R., Bonchuk A., Fedotova A., Kyrcha-nova O., Renkawitz R., Georgiev P. Two new insulator proteins, Pita and ZIPIC, target CP190 to chromatin. Genome Res. 2015;25(1): 89-99. DOI 10.1101/gr.174169.114.</mixed-citation></citation-alternatives></ref><ref id="cit19"><label>19</label><citation-alternatives><mixed-citation xml:lang="ru">Melnikova L., Kostyuchenko M., Molodina V., Parshikov A., Geor-giev P., Golovnin A. Multiple interactions are involved in a high¬ly specific association of the Mod(mdg4)-67.2 isoform with the Su(Hw) sites in Drosophila. Open Biol. 2017a;7(10):pii: 170150. DOI 10.1098/rsob.170150.</mixed-citation><mixed-citation xml:lang="en">Melnikova L., Kostyuchenko M., Molodina V., Parshikov A., Geor-giev P., Golovnin A. Multiple interactions are involved in a high¬ly specific association of the Mod(mdg4)-67.2 isoform with the Su(Hw) sites in Drosophila. Open Biol. 2017a;7(10):pii: 170150. DOI 10.1098/rsob.170150.</mixed-citation></citation-alternatives></ref><ref id="cit20"><label>20</label><citation-alternatives><mixed-citation xml:lang="ru">Melnikova L., Kostyuchenko M., Molodina V., Parshikov A., Geor-giev P., Golovnin A. Interactions between BTB domain of CP190 and two adjacent regions in Su(Hw) are required for the insula¬tor complex formation. Chromosoma. 2018a;127(1):59-71. DOI 10.1007/s00412-017-0645-6.</mixed-citation><mixed-citation xml:lang="en">Melnikova L., Kostyuchenko M., Molodina V., Parshikov A., Geor-giev P., Golovnin A. Interactions between BTB domain of CP190 and two adjacent regions in Su(Hw) are required for the insula¬tor complex formation. Chromosoma. 2018a;127(1):59-71. DOI 10.1007/s00412-017-0645-6.</mixed-citation></citation-alternatives></ref><ref id="cit21"><label>21</label><citation-alternatives><mixed-citation xml:lang="ru">Melnikova L., Kostyuchenko M., Parshikov A., Georgiev P., Golov-nin A. Role of Su(Hw) zinc finger 10 and interaction with CP190 and Mod(mdg4) proteins in recruiting the Su(Hw) complex to chro¬matin sites in Drosophila. PLoS One. 2018b;13(2):e0193497. DOI 10.1371/journal.pone.0193497.</mixed-citation><mixed-citation xml:lang="en">Melnikova L., Kostyuchenko M., Parshikov A., Georgiev P., Golov-nin A. Role of Su(Hw) zinc finger 10 and interaction with CP190 and Mod(mdg4) proteins in recruiting the Su(Hw) complex to chro¬matin sites in Drosophila. PLoS One. 2018b;13(2):e0193497. DOI 10.1371/journal.pone.0193497.</mixed-citation></citation-alternatives></ref><ref id="cit22"><label>22</label><citation-alternatives><mixed-citation xml:lang="ru">Melnikova L., Shapovalov I., Kostyuchenko M., Georgiev P., Golov-nin A. EAST affects the activity of Su(Hw) insulators by two differ¬ent mechanisms in Drosophila melanogaster. Chromosoma. 2017b; 126(2):299-311. DOI 10.1007/s00412-016-0596-3.</mixed-citation><mixed-citation xml:lang="en">Melnikova L., Shapovalov I., Kostyuchenko M., Georgiev P., Golov-nin A. EAST affects the activity of Su(Hw) insulators by two differ¬ent mechanisms in Drosophila melanogaster. Chromosoma. 2017b; 126(2):299-311. DOI 10.1007/s00412-016-0596-3.</mixed-citation></citation-alternatives></ref><ref id="cit23"><label>23</label><citation-alternatives><mixed-citation xml:lang="ru">Muravyova E., Golovnin A., Gracheva E., Parshikov A., Belenkaya T., Pirrotta V., Georgiev P. Loss of insulator activity by paired Su(Hw) chromatin insulators. Science. 2001;291(5503):495-498. DOI 10.1126/science.291.5503.495.</mixed-citation><mixed-citation xml:lang="en">Muravyova E., Golovnin A., Gracheva E., Parshikov A., Belenkaya T., Pirrotta V., Georgiev P. Loss of insulator activity by paired Su(Hw) chromatin insulators. Science. 2001;291(5503):495-498. DOI 10.1126/science.291.5503.495.</mixed-citation></citation-alternatives></ref><ref id="cit24"><label>24</label><citation-alternatives><mixed-citation xml:lang="ru">Parkhurst S.M., Corces V.G. Mutations at the suppressor of forked lo¬cus increase the accumulation of gypsy-encoded transcripts in Drosophila melanogaster. Mol. Cell. Biol. 1986;6(6):2271-2274.</mixed-citation><mixed-citation xml:lang="en">Parkhurst S.M., Corces V.G. Mutations at the suppressor of forked lo¬cus increase the accumulation of gypsy-encoded transcripts in Drosophila melanogaster. Mol. Cell. Biol. 1986;6(6):2271-2274.</mixed-citation></citation-alternatives></ref><ref id="cit25"><label>25</label><citation-alternatives><mixed-citation xml:lang="ru">Parkhurst S.M., Harrison D.A., Remington M.P., Spana C., Kelley R.L., Coyne R.S., Corces V.G. The Drosophila su(Hw) gene, which con¬trols the phenotypic effect of the gypsy transposable element, en¬codes a putative DNA-binding protein. Genes Dev. 1988;2(10): 1205-1215.</mixed-citation><mixed-citation xml:lang="en">Parkhurst S.M., Harrison D.A., Remington M.P., Spana C., Kelley R.L., Coyne R.S., Corces V.G. The Drosophila su(Hw) gene, which con¬trols the phenotypic effect of the gypsy transposable element, en¬codes a putative DNA-binding protein. Genes Dev. 1988;2(10): 1205-1215.</mixed-citation></citation-alternatives></ref><ref id="cit26"><label>26</label><citation-alternatives><mixed-citation xml:lang="ru">Parnell T.J., Kuhn E.J., Gilmore B.L., Helou C., Wold M.S., Geyer P.K. Identification of genomic sites that bind the Drosophila suppressor of Hairy-wing insulator protein. Mol. Cell. Biol. 2006;26(16):5983- 5993. DOI 10.1128/MCB.00698-06.</mixed-citation><mixed-citation xml:lang="en">Parnell T.J., Kuhn E.J., Gilmore B.L., Helou C., Wold M.S., Geyer P.K. Identification of genomic sites that bind the Drosophila suppressor of Hairy-wing insulator protein. Mol. Cell. Biol. 2006;26(16):5983- 5993. DOI 10.1128/MCB.00698-06.</mixed-citation></citation-alternatives></ref><ref id="cit27"><label>27</label><citation-alternatives><mixed-citation xml:lang="ru">Parnell T.J., Viering M.M., Skjesol A., Helou C., Kuhn E.J., Geyer P.K. An endogenous suppressor of hairy-wing insulator separates regu¬latory domains in Drosophila. Proc. Natl. Acad. Sci. USA. 2003; 100(23):13436-13441. DOI 10.1073/pnas.2333111100.</mixed-citation><mixed-citation xml:lang="en">Parnell T.J., Viering M.M., Skjesol A., Helou C., Kuhn E.J., Geyer P.K. An endogenous suppressor of hairy-wing insulator separates regu¬latory domains in Drosophila. Proc. Natl. Acad. Sci. USA. 2003; 100(23):13436-13441. DOI 10.1073/pnas.2333111100.</mixed-citation></citation-alternatives></ref><ref id="cit28"><label>28</label><citation-alternatives><mixed-citation xml:lang="ru">Plevock K.M., Galletta B.J., Slep K.C., Rusan N.M. Newly charac-terized region of CP190 associates with microtubules and mediates proper spindle morphology in Drosophila stem cells. PLoS One. 2015;10(12):e0144174. DOI 10.1371/journal.pone.0144174.</mixed-citation><mixed-citation xml:lang="en">Plevock K.M., Galletta B.J., Slep K.C., Rusan N.M. Newly charac-terized region of CP190 associates with microtubules and mediates proper spindle morphology in Drosophila stem cells. PLoS One. 2015;10(12):e0144174. DOI 10.1371/journal.pone.0144174.</mixed-citation></citation-alternatives></ref><ref id="cit29"><label>29</label><citation-alternatives><mixed-citation xml:lang="ru">Schwartz Y.B., Linder-Basso D., Kharchenko P.V., Tolstorukov M.Y., Kim M., Li H.B., Gorchakov A.A., Minoda A., Shanower G., Alekseyenko A.A., Riddle N.C., Jung Y.L., Gu T., Plachetka A., Elgin S.C.R., Kuroda M.I., Park P.J., Savitsky M., Karpen G.H., Pirrotta V. Nature and function of insulator protein binding sites in the Drosophila genome. Genome Res. 2012;22(11):2188-2198. DOI 10.1101/gr.138156.112.</mixed-citation><mixed-citation xml:lang="en">Schwartz Y.B., Linder-Basso D., Kharchenko P.V., Tolstorukov M.Y., Kim M., Li H.B., Gorchakov A.A., Minoda A., Shanower G., Alekseyenko A.A., Riddle N.C., Jung Y.L., Gu T., Plachetka A., Elgin S.C.R., Kuroda M.I., Park P.J., Savitsky M., Karpen G.H., Pirrotta V. Nature and function of insulator protein binding sites in the Drosophila genome. Genome Res. 2012;22(11):2188-2198. DOI 10.1101/gr.138156.112.</mixed-citation></citation-alternatives></ref><ref id="cit30"><label>30</label><citation-alternatives><mixed-citation xml:lang="ru">Scott K.C., Taubman A.D., Geyer P.K. Enhancer blocking by the Dro-sophila gypsy insulator depends upon insulator anatomy and enhan¬cer strength. Genetics. 1999;153(2):787-798.</mixed-citation><mixed-citation xml:lang="en">Scott K.C., Taubman A.D., Geyer P.K. Enhancer blocking by the Dro-sophila gypsy insulator depends upon insulator anatomy and enhan¬cer strength. Genetics. 1999;153(2):787-798.</mixed-citation></citation-alternatives></ref><ref id="cit31"><label>31</label><citation-alternatives><mixed-citation xml:lang="ru">Smith P.A., Corces V.G. The suppressor of Hairy-wing protein regulates the tissue-specific expression of the Drosophila gypsy retrotranspo- son. Genetics. 1995;139(1):215-228.</mixed-citation><mixed-citation xml:lang="en">Smith P.A., Corces V.G. The suppressor of Hairy-wing protein regulates the tissue-specific expression of the Drosophila gypsy retrotranspo- son. Genetics. 1995;139(1):215-228.</mixed-citation></citation-alternatives></ref><ref id="cit32"><label>32</label><citation-alternatives><mixed-citation xml:lang="ru">Soshnev A.A., Baxley R.M., Manak J.R., Tan K., Geyer P.K. The insulator protein Suppressor of Hairy-wing is an essential tran-scriptional repressor in the Drosophila ovary. Development. 2013; 140(17):3613-3623. DOI 10.1242/dev.094953.</mixed-citation><mixed-citation xml:lang="en">Soshnev A.A., Baxley R.M., Manak J.R., Tan K., Geyer P.K. The insulator protein Suppressor of Hairy-wing is an essential tran-scriptional repressor in the Drosophila ovary. Development. 2013; 140(17):3613-3623. DOI 10.1242/dev.094953.</mixed-citation></citation-alternatives></ref><ref id="cit33"><label>33</label><citation-alternatives><mixed-citation xml:lang="ru">Soshnev A.A., Ishimoto H., McAllister B.F., Li X., Wehling M.D., Kitamoto T., Geyer P.K. A conserved long noncoding RNA affects sleep behavior in Drosophila. Genetics. 2011;189(2):455-468. DOI 10.1534/genetics.111.131706.</mixed-citation><mixed-citation xml:lang="en">Soshnev A.A., Ishimoto H., McAllister B.F., Li X., Wehling M.D., Kitamoto T., Geyer P.K. A conserved long noncoding RNA affects sleep behavior in Drosophila. Genetics. 2011;189(2):455-468. DOI 10.1534/genetics.111.131706.</mixed-citation></citation-alternatives></ref><ref id="cit34"><label>34</label><citation-alternatives><mixed-citation xml:lang="ru">Wasser M., Chia W. The EAST protein of Drosophila controls an ex-pandable nuclear endoskeleton. Nat. Cell Biol. 2000;2(5):268-275. DOI 10.1038/35010535.</mixed-citation><mixed-citation xml:lang="en">Wasser M., Chia W. The EAST protein of Drosophila controls an ex-pandable nuclear endoskeleton. Nat. Cell Biol. 2000;2(5):268-275. DOI 10.1038/35010535.</mixed-citation></citation-alternatives></ref><ref id="cit35"><label>35</label><citation-alternatives><mixed-citation xml:lang="ru">Wei W., Brennan M.D. The gypsy insulator can act as a promoter-spe-cific transcriptional stimulator. Mol. Cell. Biol. 2001;21(22):7714- 7720. DOI 10.1128/MCB.21.22.7714-7720.2001</mixed-citation><mixed-citation xml:lang="en">Wei W., Brennan M.D. The gypsy insulator can act as a promoter-spe-cific transcriptional stimulator. Mol. Cell. Biol. 2001;21(22):7714- 7720. DOI 10.1128/MCB.21.22.7714-7720.2001</mixed-citation></citation-alternatives></ref></ref-list><fn-group><fn fn-type="conflict"><p>The authors declare that there are no conflicts of interest present.</p></fn></fn-group></back></article>
