Please use this identifier to cite or link to this item: https://doi.org/10.1038/s41467-021-23143-7
Title: Discovery of widespread transcription initiation at microsatellites predictable by sequence-based deep neural network
Authors: Grapotte, Mathys
Saraswat, Manu
Bessière, Chloé
Menichelli, Christophe
Ramilowski, Jordan A.
Severin, Jessica
Hayashizaki, Yoshihide
Itoh, Masayoshi
Tagami, Michihira
Murata, Mitsuyoshi
Kojima-Ishiyama, Miki
Noma, Shohei
Noguchi, Shuhei
Kasukawa, Takeya
Hasegawa, Akira
Suzuki, Harukazu
Nishiyori-Sueki, Hiromi
Frith, Martin C.
Abugessaisa, Imad
Aitken, Stuart
Aken, Bronwen L.
Alam, Intikhab
Alam, Tanvir
Alasiri, Rami
Alhendi, Ahmad M. N.
Alinejad-Rokny, Hamid
Alvarez, Mariano J.
Andersson, Robin
Arakawa, Takahiro
Araki, Marito
Arbel, Taly
Archer, John
Archibald, Alan L.
Arner, Erik
Arner, Peter
Asai, Kiyoshi
Ashoor, Haitham
Astrom, Gaby
Babina, M.
Baillie, J.K.
Bajic, V.B.
Bajpai, A.
Baker, S.
Baldarelli, R.M.
Balic, A.
Bansal, M.
Batagov, A.O.
Batzoglou, S.
Beckhouse, A.G.
Beltrami, A.P.
Beltrami, C.A.
Bertin, Nicolas
Bhattacharya, S.
Bickel, P.J.
Blake, J.A.
Blanchette, M.
Bodega, B.
Bonetti, A.
Bono, H.
Bornholdt, J.
Bttcher, M.
Bougouffa, S.
Boyd, M.
Breda, J.
Brombacher, F.
Brown, J.B.
Bult, C.J.
Burroughs, A.M.
Burt, D.W.
Busch, A.
Caglio, G.
Califano, A.
Cameron, C.J.
Cannistraci, C.V.
Carbone, A.
Carlisle, A.J.
Carninci, Piero
Carter, K.W.
Cesselli, D.
Chang, J.-C.
Chen, J.C.
Chen, Y.
Chierici, M.
Christodoulou, J.
Ciani, Y.
Clark, E.L.
Coskun, M.
Dalby, M.
Dalla, E.
Daub, C.O.
Davis, C.A.
de Hoom, Michiel J. L.
de Rie, D.
Denisenko, E.
Deplancke, B.
Detmar, M.
Deviatiiarov, R.
Di Bernardo, D.
Diehl, A.D.
Dieterich, L.C.
Dimont, E.
Djebali, S.
Dohi, T.
Dostie, J.
Drablos, F.
Edge, A.S.B.
Edinger, M.
Ehrlund, A.
Ekwall, K.
Elofsson, A.
Endoh, M.
Enomoto, H.
Enomoto, S.
Faghihi, M.
Fagiolini, M.
Farach-Carson, M.C.
Faulkner, G.J.
Favorov, A.
Fernandes, A.M.
Ferrai, C.
Forrest, A.R.R.
Forrester, L.M.
Forsberg, M.
Fort, A.
Francescatto, M.
Freeman, T.C.
Frith, Martin C.
Fukuda, S.
Funayama, M.
Furlanello, C.
Furuno, M.
Furusawa, C.
Gao, H.
Gazova, I.
Gebhard, C.
Geier, F.
Geijtenbeek, T.B.H.
Ghosh, S.
Ghosheh, Y.
Gingeras, T.R.
Gojobori, T.
Goldberg, T.
Goldowitz, D.
Gough, J.
Greco, D.
Gruber, A.J.
Guhl, S.
Guigo, R.
Guler, R.
Gusev, O.
Gustincich, S.
Ha, T.J.
Haberle, V.
Hale, P.
Hallstrom, B.M.
Hamada, M.
Handoko, L.
Hara, M.
Harbers, M.
Harrow, J.
Harshbarger, J.
Hase, T.
Hasegawa, Akira
Hashimoto, K.
Hatano, T.
Hattori, N.
Hayashi, R.
Hayashizaki, Yoshihide
Herlyn, M.
Hettne, K.
Heutink, P.
Hide, W.
Hitchens, K.J.
Sui, S.H.
’t Hoen, P.A.C.
Hon, C.C.
Hori, F.
Horie, M.
Horimoto, K.
Horton, P.
Hou, R.
Huang, E.
Huang, Y.
Hugues, R.
Hume, D.
Ienasescu, H.
Iida, K.
Ikawa, T.
Ikemura, T.
Ikeo, K.
Inoue, N.
Ishizu, Y.
Ito, Y.
Itoh, Masayoshi
Ivshina, A.V.
Jankovic, B.R.
Jenjaroenpun, P.
Johnson, R.
Jorgensen, M.
Jorjani, H.
Joshi, A.
Jurman, G.
Kaczkowski, B.
Kai, C.
Kaida, K.
Kajiyama, K.
Kaliyaperumal, R.
Kaminuma, E.
Kanaya, T.
Kaneda, H.
Kapranov, P.
Kasianov, A.S.
Kasukawa, Takeya
Katayama, T.
Kato, S.
Kawaguchi, S.
Kawai, J.
Kawaji, H.
Kawamoto, H.
Kawamura, Y.I.
Kawasaki, S.
Kawashima, T.
Kempfle, J.S.
Kenna, T.J.
Kere, J.
Khachigian, L.
Kiryu, H.
Kishima, M.
Kitajima, H.
Kitamura, T.
Kitano, H.
Klaric, E.
Klepper, K.
Klinken, S.P.
Kloppmann, E.
Knox, A.J.
Kodama, Y.
Kogo, Y.
Kojima, M.
Kojima, S.
Komatsu, N.
Komiyama, H.
Kono, T.
Koseki, H.
Koyasu, S.
Kratz, A.
Kukalev, A.
Kulakovskiy, I.
Kundaje, A.
Kunikata, H.
Kuo, R.
Kuo, T.
Kuraku, S.
Kuznetsov, V.A.
Kwon, T.J.
Larouche, M.
Lassmann, T.
Law, A.
Le-Cao, K.-A.
Lecellier, C.-H.
Lee, W.
Lenhard, B.
Lennartsson, A.
Li, K.
Li, R.
Lilje, B.
Lipovich, L.
Lizio, M.
Lopez, G.
Magi, S.
Mak, G.K.
Makeev, V.
Manabe, R.
Mandai, M.
Mar, J.
Maruyama, K.
Maruyama, T.
Mason, E.
Mathelier, A.
Matsuda, H.
Medvedeva, Y.A.
Meehan, T.F.
Mejhert, N.
Meynert, A.
Mikami, N.
Minoda, A.
Miura, H.
Miyagi, Y.
Miyawaki, A.
Mizuno, Y.
Morikawa, H.
Morimoto, M.
Morioka, M.
Morishita, S.
Moro, K.
Motakis, E.
Motohashi, H.
Mukarram, A.K.
Mummery, C.L.
Mungall, C.J.
Murakawa, Y.
Muramatsu, M.
Murata, Mitsuyoshi
Nagasaka, K.
Nagase, T.
Nakachi, Y.
Nakahara, F.
Nakai, K.
Nakamura, K.
Nakamura, Y.
Nakamura, Y.
Nakazawa, T.
Nason, G.P.
Nepal, C.
Nguyen, Q.H.
Nielsen, L.K.
Nishida, K.
Nishiguchi, K.M.
Nishiyori, H.
Nitta, K.
Noguchi, Shuhei
Noma, Shohei
Notredame, C.
Ogishima, S.
Ohkura, N.
Ohno, H.
Ohshima, M.
Ohtsu, T.
Okada, Y.
Okada-Hatakeyama, M.
Okazaki, Y.
Oksvold, P.
Orlando, V.
Ow, G.S.
Ozturk, M.
Pachkov, M.
Paparountas, T.
Parihar, S.P.
Park, S.-J.
Pascarella, G.
Passier, R.
Persson, H.
Philippens, I.H.
Piazza, S.
Plessy, C.
Pombo, A.
Ponten, F.
Poulain, S.
Poulsen, T.M.
Pradhan, S.
Prezioso, C.
Pridans, C.
Qin, X.-Y.
Quackenbush, J.
Rackham, O. 
Ramilowski, Jordan A.
Ravasi, T.
Rehli, M.
Rennie, S.
Rito, T.
Rizzu, P.
Robert, C.
Roos, M.
Rost, B.
Roudnicky, F.
Roy, R.
Rye, M.B.
Sachenkova, O.
Saetrom, P.
Sai, H.
Saiki, S.
Saito, M.
Saito, A.
Sakaguchi, S.
Sakai, M.
Sakaue, S.
Sakaue-Sawano, A.
Sandelin, A.
Sano, H.
Sasamoto, Y.
Sato, H.
Saxena, A.
Saya, H.
Schafferhans, A.
Schmeier, S.
Schmidl, C.
Schmocker, D.
Schneider, C.
Schueler, M.
Schultes, E.A.
Schulze-Tanzil, G.
Semple, C.A.
Seno, S.
Seo, W.
Sese, J.
Severin, Jessica
Sheng, G.
Shi, J.
Shimoni, Y.
Shin, J.W.
SimonSanchez, J.
Sivertsson, A.
Sjostedt, E.
Soderhall, C.
Laurent, G.S.
Stoiber, M.H.
Sugiyama, D.
Summers, K.M.
Suzuki, A.M.
Suzuki, Harukazu
Suzuki, K.
Suzuki, M.
Suzuki, N.
Suzuki, T.
Swanson, D.J.
Swoboda, R.K.
Tagami, Michihira
Taguchi, A.
Takahashi, H.
Takahashi, M.
Takamochi, K.
Takeda, S.
Takenaka, Y.
Tam, K.T.
Tanaka, H.
Tanaka, R.
Tanaka, Y.
Tang, D.
Taniuchi, I.
Tanzer, A.
Tarui, H.
Taylor, M.S.
Terada, A.
Terao, Y.
Testa, A.C.
Thomas, M.
Thongjuea, S.
Tomii, K.
Triglia, E.T.
Toyoda, H.
Tsang, H.G.
Tsujikawa, M.
Uhlén, M.
Valen, E.
van de Wetering, M.
van Nimwegen, E.
Velmeshev, D.
Verardo, R.
Vitezic, M.
Vitting-Seerup, K.
von Feilitzen, K.
Voolstra, C.R.
Vorontsov, I.E.
Wahlestedt, C.
Wasserman, Wyeth W.
Watanabe, K.
Watanabe, S.
Wells, C.A.
Winteringham, L.N.
Wolvetang, E.
Yabukami, H.
Yagi, K.
Yamada, T.
Yamaguchi, Y.
Yamamoto, M.
Yamamoto, Y.
Yamamoto, Y.
Yamanaka, Y.
Yano, K.
Yasuzawa, K.
Yatsuka, Y.
Yo, M.
Yokokura, S.
Yoneda, M.
Yoshida, E.
Yoshida, Y.
Yoshihara, M.
Young, R.
Young, R.S.
Yu, N.Y.
Yumoto, N.
Zabierowski, S.E.
Zhang, P.G.
Zucchelli, S.
Zwahlen, M.
Chatelain, Clement
Carninci, Piero
de Hoom, Michiel J. L.
Wasserman, Wyeth W.
Bréhélin, L.
Lecellier, C.-H.
FANTOM consortium.
Issue Date: 2-Jun-2021
Publisher: Nature Research
Citation: Grapotte, Mathys, Saraswat, Manu, Bessière, Chloé, Menichelli, Christophe, Ramilowski, Jordan A., Severin, Jessica, Hayashizaki, Yoshihide, Itoh, Masayoshi, Tagami, Michihira, Murata, Mitsuyoshi, Kojima-Ishiyama, Miki, Noma, Shohei, Noguchi, Shuhei, Kasukawa, Takeya, Hasegawa, Akira, Suzuki, Harukazu, Nishiyori-Sueki, Hiromi, Frith, Martin C., Abugessaisa, Imad, Aitken, Stuart, Aken, Bronwen L., Alam, Intikhab, Alam, Tanvir, Alasiri, Rami, Alhendi, Ahmad M. N., Alinejad-Rokny, Hamid, Alvarez, Mariano J., Andersson, Robin, Arakawa, Takahiro, Araki, Marito, Arbel, Taly, Archer, John, Archibald, Alan L., Arner, Erik, Arner, Peter, Asai, Kiyoshi, Ashoor, Haitham, Astrom, Gaby, Babina, M., Baillie, J.K., Bajic, V.B., Bajpai, A., Baker, S., Baldarelli, R.M., Balic, A., Bansal, M., Batagov, A.O., Batzoglou, S., Beckhouse, A.G., Beltrami, A.P., Beltrami, C.A., Bertin, Nicolas, Bhattacharya, S., Bickel, P.J., Blake, J.A., Blanchette, M., Bodega, B., Bonetti, A., Bono, H., Bornholdt, J., Bttcher, M., Bougouffa, S., Boyd, M., Breda, J., Brombacher, F., Brown, J.B., Bult, C.J., Burroughs, A.M., Burt, D.W., Busch, A., Caglio, G., Califano, A., Cameron, C.J., Cannistraci, C.V., Carbone, A., Carlisle, A.J., Carninci, Piero, Carter, K.W., Cesselli, D., Chang, J.-C., Chen, J.C., Chen, Y., Chierici, M., Christodoulou, J., Ciani, Y., Clark, E.L., Coskun, M., Dalby, M., Dalla, E., Daub, C.O., Davis, C.A., de Hoom, Michiel J. L., de Rie, D., Denisenko, E., Deplancke, B., Detmar, M., Deviatiiarov, R., Di Bernardo, D., Diehl, A.D., Dieterich, L.C., Dimont, E., Djebali, S., Dohi, T., Dostie, J., Drablos, F., Edge, A.S.B., Edinger, M., Ehrlund, A., Ekwall, K., Elofsson, A., Endoh, M., Enomoto, H., Enomoto, S., Faghihi, M., Fagiolini, M., Farach-Carson, M.C., Faulkner, G.J., Favorov, A., Fernandes, A.M., Ferrai, C., Forrest, A.R.R., Forrester, L.M., Forsberg, M., Fort, A., Francescatto, M., Freeman, T.C., Frith, Martin C., Fukuda, S., Funayama, M., Furlanello, C., Furuno, M., Furusawa, C., Gao, H., Gazova, I., Gebhard, C., Geier, F., Geijtenbeek, T.B.H., Ghosh, S., Ghosheh, Y., Gingeras, T.R., Gojobori, T., Goldberg, T., Goldowitz, D., Gough, J., Greco, D., Gruber, A.J., Guhl, S., Guigo, R., Guler, R., Gusev, O., Gustincich, S., Ha, T.J., Haberle, V., Hale, P., Hallstrom, B.M., Hamada, M., Handoko, L., Hara, M., Harbers, M., Harrow, J., Harshbarger, J., Hase, T., Hasegawa, Akira, Hashimoto, K., Hatano, T., Hattori, N., Hayashi, R., Hayashizaki, Yoshihide, Herlyn, M., Hettne, K., Heutink, P., Hide, W., Hitchens, K.J., Sui, S.H., ’t Hoen, P.A.C., Hon, C.C., Hori, F., Horie, M., Horimoto, K., Horton, P., Hou, R., Huang, E., Huang, Y., Hugues, R., Hume, D., Ienasescu, H., Iida, K., Ikawa, T., Ikemura, T., Ikeo, K., Inoue, N., Ishizu, Y., Ito, Y., Itoh, Masayoshi, Ivshina, A.V., Jankovic, B.R., Jenjaroenpun, P., Johnson, R., Jorgensen, M., Jorjani, H., Joshi, A., Jurman, G., Kaczkowski, B., Kai, C., Kaida, K., Kajiyama, K., Kaliyaperumal, R., Kaminuma, E., Kanaya, T., Kaneda, H., Kapranov, P., Kasianov, A.S., Kasukawa, Takeya, Katayama, T., Kato, S., Kawaguchi, S., Kawai, J., Kawaji, H., Kawamoto, H., Kawamura, Y.I., Kawasaki, S., Kawashima, T., Kempfle, J.S., Kenna, T.J., Kere, J., Khachigian, L., Kiryu, H., Kishima, M., Kitajima, H., Kitamura, T., Kitano, H., Klaric, E., Klepper, K., Klinken, S.P., Kloppmann, E., Knox, A.J., Kodama, Y., Kogo, Y., Kojima, M., Kojima, S., Komatsu, N., Komiyama, H., Kono, T., Koseki, H., Koyasu, S., Kratz, A., Kukalev, A., Kulakovskiy, I., Kundaje, A., Kunikata, H., Kuo, R., Kuo, T., Kuraku, S., Kuznetsov, V.A., Kwon, T.J., Larouche, M., Lassmann, T., Law, A., Le-Cao, K.-A., Lecellier, C.-H., Lee, W., Lenhard, B., Lennartsson, A., Li, K., Li, R., Lilje, B., Lipovich, L., Lizio, M., Lopez, G., Magi, S., Mak, G.K., Makeev, V., Manabe, R., Mandai, M., Mar, J., Maruyama, K., Maruyama, T., Mason, E., Mathelier, A., Matsuda, H., Medvedeva, Y.A., Meehan, T.F., Mejhert, N., Meynert, A., Mikami, N., Minoda, A., Miura, H., Miyagi, Y., Miyawaki, A., Mizuno, Y., Morikawa, H., Morimoto, M., Morioka, M., Morishita, S., Moro, K., Motakis, E., Motohashi, H., Mukarram, A.K., Mummery, C.L., Mungall, C.J., Murakawa, Y., Muramatsu, M., Murata, Mitsuyoshi, Nagasaka, K., Nagase, T., Nakachi, Y., Nakahara, F., Nakai, K., Nakamura, K., Nakamura, Y., Nakamura, Y., Nakazawa, T., Nason, G.P., Nepal, C., Nguyen, Q.H., Nielsen, L.K., Nishida, K., Nishiguchi, K.M., Nishiyori, H., Nitta, K., Noguchi, Shuhei, Noma, Shohei, Notredame, C., Ogishima, S., Ohkura, N., Ohno, H., Ohshima, M., Ohtsu, T., Okada, Y., Okada-Hatakeyama, M., Okazaki, Y., Oksvold, P., Orlando, V., Ow, G.S., Ozturk, M., Pachkov, M., Paparountas, T., Parihar, S.P., Park, S.-J., Pascarella, G., Passier, R., Persson, H., Philippens, I.H., Piazza, S., Plessy, C., Pombo, A., Ponten, F., Poulain, S., Poulsen, T.M., Pradhan, S., Prezioso, C., Pridans, C., Qin, X.-Y., Quackenbush, J., Rackham, O., Ramilowski, Jordan A., Ravasi, T., Rehli, M., Rennie, S., Rito, T., Rizzu, P., Robert, C., Roos, M., Rost, B., Roudnicky, F., Roy, R., Rye, M.B., Sachenkova, O., Saetrom, P., Sai, H., Saiki, S., Saito, M., Saito, A., Sakaguchi, S., Sakai, M., Sakaue, S., Sakaue-Sawano, A., Sandelin, A., Sano, H., Sasamoto, Y., Sato, H., Saxena, A., Saya, H., Schafferhans, A., Schmeier, S., Schmidl, C., Schmocker, D., Schneider, C., Schueler, M., Schultes, E.A., Schulze-Tanzil, G., Semple, C.A., Seno, S., Seo, W., Sese, J., Severin, Jessica, Sheng, G., Shi, J., Shimoni, Y., Shin, J.W., SimonSanchez, J., Sivertsson, A., Sjostedt, E., Soderhall, C., Laurent, G.S., Stoiber, M.H., Sugiyama, D., Summers, K.M., Suzuki, A.M., Suzuki, Harukazu, Suzuki, K., Suzuki, M., Suzuki, N., Suzuki, T., Swanson, D.J., Swoboda, R.K., Tagami, Michihira, Taguchi, A., Takahashi, H., Takahashi, M., Takamochi, K., Takeda, S., Takenaka, Y., Tam, K.T., Tanaka, H., Tanaka, R., Tanaka, Y., Tang, D., Taniuchi, I., Tanzer, A., Tarui, H., Taylor, M.S., Terada, A., Terao, Y., Testa, A.C., Thomas, M., Thongjuea, S., Tomii, K., Triglia, E.T., Toyoda, H., Tsang, H.G., Tsujikawa, M., Uhlén, M., Valen, E., van de Wetering, M., van Nimwegen, E., Velmeshev, D., Verardo, R., Vitezic, M., Vitting-Seerup, K., von Feilitzen, K., Voolstra, C.R., Vorontsov, I.E., Wahlestedt, C., Wasserman, Wyeth W., Watanabe, K., Watanabe, S., Wells, C.A., Winteringham, L.N., Wolvetang, E., Yabukami, H., Yagi, K., Yamada, T., Yamaguchi, Y., Yamamoto, M., Yamamoto, Y., Yamamoto, Y., Yamanaka, Y., Yano, K., Yasuzawa, K., Yatsuka, Y., Yo, M., Yokokura, S., Yoneda, M., Yoshida, E., Yoshida, Y., Yoshihara, M., Young, R., Young, R.S., Yu, N.Y., Yumoto, N., Zabierowski, S.E., Zhang, P.G., Zucchelli, S., Zwahlen, M., Chatelain, Clement, Carninci, Piero, de Hoom, Michiel J. L., Wasserman, Wyeth W., Bréhélin, L., Lecellier, C.-H., FANTOM consortium. (2021-06-02). Discovery of widespread transcription initiation at microsatellites predictable by sequence-based deep neural network. Nature Communications 12 (1) : 3297. ScholarBank@NUS Repository. https://doi.org/10.1038/s41467-021-23143-7
Rights: Attribution 4.0 International
Abstract: Using the Cap Analysis of Gene Expression (CAGE) technology, the FANTOM5 consortium provided one of the most comprehensive maps of transcription start sites (TSSs) in several species. Strikingly, ~72% of them could not be assigned to a specific gene and initiate at unconventional regions, outside promoters or enhancers. Here, we probe these unassigned TSSs and show that, in all species studied, a significant fraction of CAGE peaks initiate at microsatellites, also called short tandem repeats (STRs). To confirm this transcription, we develop Cap Trap RNA-seq, a technology which combines cap trapping and long read MinION sequencing. We train sequence-based deep learning models able to predict CAGE signal at STRs with high accuracy. These models unveil the importance of STR surrounding sequences not only to distinguish STR classes, but also to predict the level of transcription initiation. Importantly, genetic variants linked to human diseases are preferentially found at STRs with high transcription initiation level, supporting the biological and clinical relevance of transcription initiation at STRs. Together, our results extend the repertoire of non-coding transcription associated with DNA tandem repeats and complexify STR polymorphism. © 2021, The Author(s).
Source Title: Nature Communications
URI: https://scholarbank.nus.edu.sg/handle/10635/232324
ISSN: 2041-1723
DOI: 10.1038/s41467-021-23143-7
Rights: Attribution 4.0 International
Appears in Collections:Staff Publications
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