Evolutionary Biology

Evolutionary analysis of candidate non-coding elements regulating neurodevelopmental genes in vertebrates

10.24072/pcjournal.21 - Peer Community Journal, Volume 1 (2021), article no. e19.

Get full text PDF

Many non-coding regulatory elements conserved in vertebrates regulate the expression of genes involved in development and play an important role in the evolution of morphology through the rewiring of developmental gene networks. Available biological datasets allow the identification of non-coding regulatory elements with high confidence; furthermore, chromatin conformation data can be used to confirm enhancer-promoter interactions in specific tissue types and developmental stages. We have devised an analysis pipeline that integrates datasets about gene expression, enhancer activity, chromatin accessibility, epigenetic marks, and Hi-C contact frequencies in various brain tissues and developmental stages, leading to the identification of eight non-coding elements that might regulate the expression of three genes with important roles in brain development in vertebrates. We have then performed comparative sequence and microsynteny analyses in order to reconstruct the evolutionary history of the regulatory landscape around these genes; we observe a general pattern of ancient regulatory elements conserved across most vertebrate lineages, together with younger elements that appear to be mammal and primate innovations.

Published online:
DOI: https://doi.org/10.24072/pcjournal.21
     author = {Novo, Francisco J.},
     title = {Evolutionary analysis of candidate non-coding elements regulating neurodevelopmental genes in vertebrates},
     journal = {Peer Community Journal},
     eid = {e19},
     publisher = {Peer Community In},
     volume = {1},
     year = {2021},
     doi = {10.24072/pcjournal.21},
     url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.21/}
Novo, Francisco J. Evolutionary analysis of candidate non-coding elements regulating neurodevelopmental genes in vertebrates. Peer Community Journal, Volume 1 (2021), article  no. e19. doi : 10.24072/pcjournal.21. https://peercommunityjournal.org/articles/10.24072/pcjournal.21/

Peer reviewed and recommended by PCI : 10.24072/pci.evolbiol.100035

[1] Altschul, Stephen F.; Gish, Warren; Miller, Webb; Myers, Eugene W.; Lipman, David J. Basic local alignment search tool, Journal of Molecular Biology, Volume 215 (1990) no. 3, pp. 403-410 | Article

[2] Andersson, Robin; Gebhard, Claudia; Miguel-Escalada, Irene; Hoof, Ilka; Bornholdt, Jette; Boyd, Mette; Chen, Yun; Zhao, Xiaobei; Schmidl, Christian; Suzuki, Takahiro; Ntini, Evgenia; Arner, Erik; Valen, Eivind; Li, Kang; Schwarzfischer, Lucia; Glatz, Dagmar; Raithel, Johanna; Lilje, Berit; Rapin, Nicolas; Bagger, Frederik Otzen; Jørgensen, Mette; Andersen, Peter Refsing; Bertin, Nicolas; Rackham, Owen; Burroughs, A. Maxwell; Baillie, J. Kenneth; Ishizu, Yuri; Shimizu, Yuri; Furuhata, Erina; Maeda, Shiori; Negishi, Yutaka; Mungall, Christopher J.; Meehan, Terrence F.; Lassmann, Timo; Itoh, Masayoshi; Kawaji, Hideya; Kondo, Naoto; Kawai, Jun; Lennartsson, Andreas; Daub, Carsten O.; Heutink, Peter; Hume, David A.; Jensen, Torben Heick; Suzuki, Harukazu; Hayashizaki, Yoshihide; Müller, Ferenc; Forrest, Alistair R. R.; Carninci, Piero; Rehli, Michael; Sandelin, Albin An atlas of active enhancers across human cell types and tissues, Nature, Volume 507 (2014) no. 7493, pp. 455-461 | Article

[3] Bae, Byoung-Il; Jayaraman, Divya; Walsh, Christopher A. Genetic Changes Shaping the Human Brain, Developmental Cell, Volume 32 (2015) no. 4, pp. 423-434 | Article

[4] Bakken, Trygve E.; Miller, Jeremy A.; Ding, Song-Lin; Sunkin, Susan M.; Smith, Kimberly A.; Ng, Lydia; Szafer, Aaron; Dalley, Rachel A.; Royall, Joshua J.; Lemon, Tracy; Shapouri, Sheila; Aiona, Kaylynn; Arnold, James; Bennett, Jeffrey L.; Bertagnolli, Darren; Bickley, Kristopher; Boe, Andrew; Brouner, Krissy; Butler, Stephanie; Byrnes, Emi; Caldejon, Shiella; Carey, Anita; Cate, Shelby; Chapin, Mike; Chen, Jefferey; Dee, Nick; Desta, Tsega; Dolbeare, Tim A.; Dotson, Nadia; Ebbert, Amanda; Fulfs, Erich; Gee, Garrett; Gilbert, Terri L.; Goldy, Jeff; Gourley, Lindsey; Gregor, Ben; Gu, Guangyu; Hall, Jon; Haradon, Zeb; Haynor, David R.; Hejazinia, Nika; Hoerder-Suabedissen, Anna; Howard, Robert; Jochim, Jay; Kinnunen, Marty; Kriedberg, Ali; Kuan, Chihchau L.; Lau, Christopher; Lee, Chang-Kyu; Lee, Felix; Luong, Lon; Mastan, Naveed; May, Ryan; Melchor, Jose; Mosqueda, Nerick; Mott, Erika; Ngo, Kiet; Nyhus, Julie; Oldre, Aaron; Olson, Eric; Parente, Jody; Parker, Patrick D.; Parry, Sheana; Pendergraft, Julie; Potekhina, Lydia; Reding, Melissa; Riley, Zackery L.; Roberts, Tyson; Rogers, Brandon; Roll, Kate; Rosen, David; Sandman, David; Sarreal, Melaine; Shapovalova, Nadiya; Shi, Shu; Sjoquist, Nathan; Sodt, Andy J.; Townsend, Robbie; Velasquez, Lissette; Wagley, Udi; Wakeman, Wayne B.; White, Cassandra; Bennett, Crissa; Wu, Jennifer; Young, Rob; Youngstrom, Brian L.; Wohnoutka, Paul; Gibbs, Richard A.; Rogers, Jeffrey; Hohmann, John G.; Hawrylycz, Michael J.; Hevner, Robert F.; Molnár, Zoltán; Phillips, John W.; Dang, Chinh; Jones, Allan R.; Amaral, David G.; Bernard, Amy; Lein, Ed S. A comprehensive transcriptional map of primate brain development, Nature, Volume 535 (2016) no. 7612, pp. 367-375 | Article

[5] Bejerano, Gill; Pheasant, Michael; Makunin, Igor; Stephen, Stuart; Kent, W. James; Mattick, John S.; Haussler, David Ultraconserved Elements in the Human Genome, Science, Volume 304 (2004) no. 5675, pp. 1321-1325 | Article

[6] Bernstein, B. E.; Birney, E.; Dunham, I.; Green, E. D.; Gunter, C.; Snyder, M. An integrated encyclopedia of DNA elements in the human genome, Nature, Volume 489 (2012) no. 7414, pp. 57-74 | Article

[7] Boyd, J. Lomax; Skove, Stephanie L.; Rouanet, Jeremy P.; Pilaz, Louis-Jan; Bepler, Tristan; Gordân, Raluca; Wray, Gregory A.; Silver, Debra L. Human-Chimpanzee Differences in a FZD8 Enhancer Alter Cell-Cycle Dynamics in the Developing Neocortex, Current Biology, Volume 25 (2015) no. 6, pp. 772-779 | Article

[8] Brudno, M.; Malde, S.; Poliakov, A.; Do, C. B.; Couronne, O.; Dubchak, I.; Batzoglou, S. Glocal alignment: finding rearrangements during alignment, Bioinformatics, Volume 19 (2003) no. Suppl 1 | Article

[9] Bulchand, Sarada; Subramanian, Lakshmi; Tole, Shubha Dynamic spatiotemporal expression of LIM genes and cofactors in the embryonic and postnatal cerebral cortex, Developmental Dynamics, Volume 226 (2003) no. 3, pp. 460-469 | Article

[10] Carroll, Sean B Evolution at Two Levels: On Genes and Form, PLoS Biology, Volume 3 (2005) no. 7 | Article

[11] Cecchi, C.; Mallamaci, A.; Boncinelli, E. Otx and Emx homeobox genes in brain development, Int J Dev Biol, Volume 44 (2000) | Article

[12] Dekker, Job; Mirny, Leonid The 3D Genome as Moderator of Chromosomal Communication, Cell, Volume 164 (2016) no. 6, pp. 1110-1121 | Article

[13] Dixon, Jesse R.; Gorkin, David U.; Ren, Bing Chromatin Domains: The Unit of Chromosome Organization, Molecular Cell, Volume 62 (2016) no. 5, pp. 668-680 | Article

[14] Ernst, J.; Kellis, M. ChromHMM: automating chromatin-state discovery and characterization, Nature Methods, Volume 9 (2012) no. 3, pp. 215-216 | Article

[15] Erwin, Douglas H.; Davidson, Eric H. The evolution of hierarchical gene regulatory networks, Nature Reviews Genetics, Volume 10 (2009) no. 2, pp. 141-148 | Article

[16] Fulco, Charles P.; Munschauer, Mathias; Anyoha, Rockwell; Munson, Glen; Grossman, Sharon R.; Perez, Elizabeth M.; Kane, Michael; Cleary, Brian; Lander, Eric S.; Engreitz, Jesse M. Systematic mapping of functional enhancer–promoter connections with CRISPR interference, Science, Volume 354 (2016) no. 6313, pp. 769-773 | Article

[17] Gerstein, Mark B.; Kundaje, Anshul; Hariharan, Manoj; Landt, Stephen G.; Yan, Koon-Kiu; Cheng, Chao; Mu, Xinmeng Jasmine; Khurana, Ekta; Rozowsky, Joel; Alexander, Roger; Min, Renqiang; Alves, Pedro; Abyzov, Alexej; Addleman, Nick; Bhardwaj, Nitin; Boyle, Alan P.; Cayting, Philip; Charos, Alexandra; Chen, David Z.; Cheng, Yong; Clarke, Declan; Eastman, Catharine; Euskirchen, Ghia; Frietze, Seth; Fu, Yao; Gertz, Jason; Grubert, Fabian; Harmanci, Arif; Jain, Preti; Kasowski, Maya; Lacroute, Phil; Leng, Jing; Lian, Jin; Monahan, Hannah; O’Geen, Henriette; Ouyang, Zhengqing; Partridge, E. Christopher; Patacsil, Dorrelyn; Pauli, Florencia; Raha, Debasish; Ramirez, Lucia; Reddy, Timothy E.; Reed, Brian; Shi, Minyi; Slifer, Teri; Wang, Jing; Wu, Linfeng; Yang, Xinqiong; Yip, Kevin Y.; Zilberman-Schapira, Gili; Batzoglou, Serafim; Sidow, Arend; Farnham, Peggy J.; Myers, Richard M.; Weissman, Sherman M.; Snyder, Michael Architecture of the human regulatory network derived from ENCODE data, Nature, Volume 489 (2012) no. 7414, pp. 91-100 | Article

[18] He, Zhisong; Han, Dingding; Efimova, Olga; Guijarro, Patricia; Yu, Qianhui; Oleksiak, Anna; Jiang, Shasha; Anokhin, Konstantin; Velichkovsky, Boris; Grünewald, Stefan; Khaitovich, Philipp Comprehensive transcriptome analysis of neocortical layers in humans, chimpanzees and macaques, Nature Neuroscience, Volume 20 (2017) no. 6, pp. 886-895 | Article

[19] Hermanson, O.; Sugihara, T. M.; Andersen, B. Expression of LMO-4 in the central nervous system of the embryonic and adult mouse, . Cell Mol Biol, Volume 45 (1999)

[20] Inoue, Jun; Sato, Yukuto; Sinclair, Robert; Tsukamoto, Katsumi; Nishida, Mutsumi Rapid genome reshaping by multiple-gene loss after whole-genome duplication in teleost fish suggested by mathematical modeling, Proceedings of the National Academy of Sciences, Volume 112 (2015) no. 48, pp. 14918-14923 | Article

[21] Kundaje, Anshul; Meuleman, Wouter; Ernst, Jason; Bilenky, Misha; Yen, Angela; Heravi-Moussavi, Alireza; Kheradpour, Pouya; Zhang, Zhizhuo; Wang, Jianrong; Ziller, Michael J.; Amin, Viren; Whitaker, John W.; Schultz, Matthew D.; Ward, Lucas D.; Sarkar, Abhishek; Quon, Gerald; Sandstrom, Richard S.; Eaton, Matthew L.; Wu, Yi-Chieh; Pfenning, Andreas R.; Wang, Xinchen; Claussnitzer, Melina; Liu, Yaping; Coarfa, Cristian; Harris, R. Alan; Shoresh, Noam; Epstein, Charles B.; Gjoneska, Elizabeta; Leung, Danny; Xie, Wei; Hawkins, R. David; Lister, Ryan; Hong, Chibo; Gascard, Philippe; Mungall, Andrew J.; Moore, Richard; Chuah, Eric; Tam, Angela; Canfield, Theresa K.; Hansen, R. Scott; Kaul, Rajinder; Sabo, Peter J.; Bansal, Mukul S.; Carles, Annaick; Dixon, Jesse R.; Farh, Kai-How; Feizi, Soheil; Karlic, Rosa; Kim, Ah-Ram; Kulkarni, Ashwinikumar; Li, Daofeng; Lowdon, Rebecca; Elliott, GiNell; Mercer, Tim R.; Neph, Shane J.; Onuchic, Vitor; Polak, Paz; Rajagopal, Nisha; Ray, Pradipta; Sallari, Richard C.; Siebenthall, Kyle T.; Sinnott-Armstrong, Nicholas A.; Stevens, Michael; Thurman, Robert E.; Wu, Jie; Zhang, Bo; Zhou, Xin; Beaudet, Arthur E.; Boyer, Laurie A.; De Jager, Philip L.; Farnham, Peggy J.; Fisher, Susan J.; Haussler, David; Jones, Steven J. M.; Li, Wei; Marra, Marco A.; McManus, Michael T.; Sunyaev, Shamil; Thomson, James A.; Tlsty, Thea D.; Tsai, Li-Huei; Wang, Wei; Waterland, Robert A.; Zhang, Michael Q.; Chadwick, Lisa H.; Bernstein, Bradley E.; Costello, Joseph F.; Ecker, Joseph R.; Hirst, Martin; Meissner, Alexander; Milosavljevic, Aleksandar; Ren, Bing; Stamatoyannopoulos, John A.; Wang, Ting; Kellis, Manolis Integrative analysis of 111 reference human epigenomes, Nature, Volume 518 (2015) no. 7539, pp. 317-330 | Article

[22] Lane, Mary Ellen; Runko, Alexander P; Roy, Nicole M; Sagerström, Charles G RETRACTED: Dynamic expression and regulation by Fgf8 and Pou2 of the zebrafish LIM-only gene, lmo4, Gene Expression Patterns, Volume 2 (2002) no. 3-4, pp. 207-211 | Article

[23] Lowe, Craig B.; Kellis, Manolis; Siepel, Adam; Raney, Brian J.; Clamp, Michele; Salama, Sofie R.; Kingsley, David M.; Lindblad-Toh, Kerstin; Haussler, David Three Periods of Regulatory Innovation During Vertebrate Evolution, Science, Volume 333 (2011) no. 6045, pp. 1019-1024 | Article

[24] Lyons, Eric; Freeling, Michael How to usefully compare homologous plant genes and chromosomes as DNA sequences, The Plant Journal, Volume 53 (2008) no. 4, pp. 661-673 | Article

[25] Mariani, J.; Favaro, R.; Lancini, C.; Vaccari, G.; Ferri, A. L.; Bertolini, J.; Tonoli, D.; Latorre, E.; Caccia, R.; Ronchi, A.; Ottolenghi, S.; Miyagi, S.; Okuda, A.; Zappavigna, V.; Nicolis, S. K. Emx2 is a dose-dependent negative regulator of Sox2 telencephalic enhancers, Nucleic Acids Research, Volume 40 (2012) no. 14, pp. 6461-6476 | Article

[26] McCollum, Catherine W.; Amin, Shivas R.; Pauerstein, Philip; Lane, Mary Ellen A zebrafish LMO4 ortholog limits the size of the forebrain and eyes through negative regulation of six3b and rx3, Developmental Biology, Volume 309 (2007) no. 2, pp. 373-385 | Article

[27] McEwen, Gayle K.; Goode, Debbie K.; Parker, Hugo J.; Woolfe, Adam; Callaway, Heather; Elgar, Greg Early Evolution of Conserved Regulatory Sequences Associated with Development in Vertebrates, PLoS Genetics, Volume 5 (2009) no. 12 | Article

[28] McLean, Cory Y; Bristor, Dave; Hiller, Michael; Clarke, Shoa L; Schaar, Bruce T; Lowe, Craig B; Wenger, Aaron M; Bejerano, Gill GREAT improves functional interpretation of cis-regulatory regions, Nature Biotechnology, Volume 28 (2010) no. 5, pp. 495-501 | Article

[29] Melé, Marta; Ferreira, Pedro G.; Reverter, Ferran; DeLuca, David S.; Monlong, Jean; Sammeth, Michael; Young, Taylor R.; Goldmann, Jakob M; Pervouchine, Dmitri D.; Sullivan, Timothy J.; Johnson, Rory; Segrè, Ayellet V.; Djebali, Sarah; Niarchou, Anastasia; Consortium, The GTEx; Wright, Fred A.; Lappalainen, Tuuli; Calvo, Miquel; Getz, Gad; Dermitzakis, Emmanouil T.; Ardlie, Kristin G.; Guigó, Roderic The human transcriptome across tissues and individuals, Science, Volume 348 (2015) no. 6235, pp. 660-665 | Article

[30] Miller, Jeremy A.; Ding, Song-Lin; Sunkin, Susan M.; Smith, Kimberly A.; Ng, Lydia; Szafer, Aaron; Ebbert, Amanda; Riley, Zackery L.; Royall, Joshua J.; Aiona, Kaylynn; Arnold, James M.; Bennet, Crissa; Bertagnolli, Darren; Brouner, Krissy; Butler, Stephanie; Caldejon, Shiella; Carey, Anita; Cuhaciyan, Christine; Dalley, Rachel A.; Dee, Nick; Dolbeare, Tim A.; Facer, Benjamin A. C.; Feng, David; Fliss, Tim P.; Gee, Garrett; Goldy, Jeff; Gourley, Lindsey; Gregor, Benjamin W.; Gu, Guangyu; Howard, Robert E.; Jochim, Jayson M.; Kuan, Chihchau L.; Lau, Christopher; Lee, Chang-Kyu; Lee, Felix; Lemon, Tracy A.; Lesnar, Phil; McMurray, Bergen; Mastan, Naveed; Mosqueda, Nerick; Naluai-Cecchini, Theresa; Ngo, Nhan-Kiet; Nyhus, Julie; Oldre, Aaron; Olson, Eric; Parente, Jody; Parker, Patrick D.; Parry, Sheana E.; Stevens, Allison; Pletikos, Mihovil; Reding, Melissa; Roll, Kate; Sandman, David; Sarreal, Melaine; Shapouri, Sheila; Shapovalova, Nadiya V.; Shen, Elaine H.; Sjoquist, Nathan; Slaughterbeck, Clifford R.; Smith, Michael; Sodt, Andy J.; Williams, Derric; Zöllei, Lilla; Fischl, Bruce; Gerstein, Mark B.; Geschwind, Daniel H.; Glass, Ian A.; Hawrylycz, Michael J.; Hevner, Robert F.; Huang, Hao; Jones, Allan R.; Knowles, James A.; Levitt, Pat; Phillips, John W.; Šestan, Nenad; Wohnoutka, Paul; Dang, Chinh; Bernard, Amy; Hohmann, John G.; Lein, Ed S. Transcriptional landscape of the prenatal human brain, Nature, Volume 508 (2014) no. 7495, pp. 199-206 | Article

[31] Notwell, James H.; Chung, Tisha; Heavner, Whitney; Bejerano, Gill A family of transposable elements co-opted into developmental enhancers in the mouse neocortex, Nature Communications, Volume 6 (2015) no. 1 | Article

[32] Ocaña, Francisco M.; Suryanarayana, Shreyas M.; Saitoh, Kazuya; Kardamakis, Andreas A.; Capantini, Lorenza; Robertson, Brita; Grillner, Sten The Lamprey Pallium Provides a Blueprint of the Mammalian Motor Projections from Cortex, Current Biology, Volume 25 (2015) no. 4, pp. 413-423 | Article

[33] Okbay, Aysu; Beauchamp, Jonathan P.; Fontana, Mark Alan; Lee, James J.; Pers, Tune H.; Rietveld, Cornelius A.; Turley, Patrick; Chen, Guo-Bo; Emilsson, Valur; Meddens, S. Fleur W.; Oskarsson, Sven; Pickrell, Joseph K.; Thom, Kevin; Timshel, Pascal; de Vlaming, Ronald; Abdellaoui, Abdel; Ahluwalia, Tarunveer S.; Bacelis, Jonas; Baumbach, Clemens; Bjornsdottir, Gyda; Brandsma, Johannes H.; Pina Concas, Maria; Derringer, Jaime; Furlotte, Nicholas A.; Galesloot, Tessel E.; Girotto, Giorgia; Gupta, Richa; Hall, Leanne M.; Harris, Sarah E.; Hofer, Edith; Horikoshi, Momoko; Huffman, Jennifer E.; Kaasik, Kadri; Kalafati, Ioanna P.; Karlsson, Robert; Kong, Augustine; Lahti, Jari; Lee, Sven J. van der; deLeeuw, Christiaan; Lind, Penelope A.; Lindgren, Karl-Oskar; Liu, Tian; Mangino, Massimo; Marten, Jonathan; Mihailov, Evelin; Miller, Michael B.; van der Most, Peter J.; Oldmeadow, Christopher; Payton, Antony; Pervjakova, Natalia; Peyrot, Wouter J.; Qian, Yong; Raitakari, Olli; Rueedi, Rico; Salvi, Erika; Schmidt, Börge; Schraut, Katharina E.; Shi, Jianxin; Smith, Albert V.; Poot, Raymond A.; St Pourcain, Beate; Teumer, Alexander; Thorleifsson, Gudmar; Verweij, Niek; Vuckovic, Dragana; Wellmann, Juergen; Westra, Harm-Jan; Yang, Jingyun; Zhao, Wei; Zhu, Zhihong; Alizadeh, Behrooz Z.; Amin, Najaf; Bakshi, Andrew; Baumeister, Sebastian E.; Biino, Ginevra; Bønnelykke, Klaus; Boyle, Patricia A.; Campbell, Harry; Cappuccio, Francesco P.; Davies, Gail; De Neve, Jan-Emmanuel; Deloukas, Panos; Demuth, Ilja; Ding, Jun; Eibich, Peter; Eisele, Lewin; Eklund, Niina; Evans, David M.; Faul, Jessica D.; Feitosa, Mary F.; Forstner, Andreas J.; Gandin, Ilaria; Gunnarsson, Bjarni; Halldórsson, Bjarni V.; Harris, Tamara B.; Heath, Andrew C.; Hocking, Lynne J.; Holliday, Elizabeth G.; Homuth, Georg; Horan, Michael A.; Hottenga, Jouke-Jan; de Jager, Philip L.; Joshi, Peter K.; Jugessur, Astanand; Kaakinen, Marika A.; Kähönen, Mika; Kanoni, Stavroula; Keltigangas-Järvinen, Liisa; Kiemeney, Lambertus A. L. M.; Kolcic, Ivana; Koskinen, Seppo; Kraja, Aldi T.; Kroh, Martin; Kutalik, Zoltan; Latvala, Antti; Launer, Lenore J.; Lebreton, Maël P.; Levinson, Douglas F.; Lichtenstein, Paul; Lichtner, Peter; Liewald, David C. M.; Cohort Study, LifeLines; Loukola, Anu; Madden, Pamela A.; Mägi, Reedik; Mäki-Opas, Tomi; Marioni, Riccardo E.; Marques-Vidal, Pedro; Meddens, Gerardus A.; McMahon, George; Meisinger, Christa; Meitinger, Thomas; Milaneschi, Yusplitri; Milani, Lili; Montgomery, Grant W.; Myhre, Ronny; Nelson, Christopher P.; Nyholt, Dale R.; Ollier, William E. R.; Palotie, Aarno; Paternoster, Lavinia; Pedersen, Nancy L.; Petrovic, Katja E.; Porteous, David J.; Räikkönen, Katri; Ring, Susan M.; Robino, Antonietta; Rostapshova, Olga; Rudan, Igor; Rustichini, Aldo; Salomaa, Veikko; Sanders, Alan R.; Sarin, Antti-Pekka; Schmidt, Helena; Scott, Rodney J.; Smith, Blair H.; Smith, Jennifer A.; Staessen, Jan A.; Steinhagen-Thiessen, Elisabeth; Strauch, Konstantin; Terracciano, Antonio; Tobin, Martin D.; Ulivi, Sheila; Vaccargiu, Simona; Quaye, Lydia; van Rooij, Frank J. A.; Venturini, Cristina; Vinkhuyzen, Anna A. E.; Völker, Uwe; Völzke, Henry; Vonk, Judith M.; Vozzi, Diego; Waage, Johannes; Ware, Erin B.; Willemsen, Gonneke; Attia, John R.; Bennett, David A.; Berger, Klaus; Bertram, Lars; Bisgaard, Hans; Boomsma, Dorret I.; Borecki, Ingrid B.; Bültmann, Ute; Chabris, Christopher F.; Cucca, Francesco; Cusi, Daniele; Deary, Ian J.; Dedoussis, George V.; van Duijn, Cornelia M.; Eriksson, Johan G.; Franke, Barbara; Franke, Lude; Gasparini, Paolo; Gejman, Pablo V.; Gieger, Christian; Grabe, Hans-Jörgen; Gratten, Jacob; Groenen, Patrick J. F.; Gudnason, Vilmundur; van der Harst, Pim; Hayward, Caroline; Hinds, David A.; Hoffmann, Wolfgang; Hyppönen, Elina; Iacono, William G.; Jacobsson, Bo; Järvelin, Marjo-Riitta; Jöckel, Karl-Heinz; Kaprio, Jaakko; Kardia, Sharon L. R.; Lehtimäki, Terho; Lehrer, Steven F.; Magnusson, Patrik K. E.; Martin, Nicholas G.; McGue, Matt; Metspalu, Andres; Pendleton, Neil; Penninx, Brenda W. J. H.; Perola, Markus; Pirastu, Nicola; Pirastu, Mario; Polasek, Ozren; Posthuma, Danielle; Power, Christine; Province, Michael A.; Samani, Nilesh J.; Schlessinger, David; Schmidt, Reinhold; Sørensen, Thorkild I. A.; Spector, Tim D.; Stefansson, Kari; Thorsteinsdottir, Unnur; Thurik, A. Roy; Timpson, Nicholas J.; Tiemeier, Henning; Tung, Joyce Y.; Uitterlinden, André G.; Vitart, Veronique; Vollenweider, Peter; Weir, David R.; Wilson, James F.; Wright, Alan F.; Conley, Dalton C.; Krueger, Robert F.; Davey Smith, George; Hofman, Albert; Laibson, David I.; Medland, Sarah E.; Meyer, Michelle N.; Yang, Jian; Johannesson, Magnus; Visscher, Peter M.; Esko, Tõnu; Koellinger, Philipp D.; Cesarini, David; Benjamin, Daniel J. Genome-wide association study identifies 74 loci associated with educational attainment, Nature, Volume 533 (2016) no. 7604, pp. 539-542 | Article

[34] Pauls, Stefan; Goode, Debbie K.; Petrone, Libero; Oliveri, Paola; Elgar, Greg Evolution of lineage-specific functions in ancient cis -regulatory modules, Open Biology, Volume 5 (2015) no. 11 | Article

[35] Pennacchio, Len A.; Ahituv, Nadav; Moses, Alan M.; Prabhakar, Shyam; Nobrega, Marcelo A.; Shoukry, Malak; Minovitsky, Simon; Dubchak, Inna; Holt, Amy; Lewis, Keith D.; Plajzer-Frick, Ingrid; Akiyama, Jennifer; De Val, Sarah; Afzal, Veena; Black, Brian L.; Couronne, Olivier; Eisen, Michael B.; Visel, Axel; Rubin, Edward M. In vivo enhancer analysis of human conserved non-coding sequences, Nature, Volume 444 (2006) no. 7118, pp. 499-502 | Article

[36] Rakic, Pasko Evolution of the neocortex: a perspective from developmental biology, Nature Reviews Neuroscience, Volume 10 (2009) no. 10, pp. 724-735 | Article

[37] Reilly, Steven K.; Yin, Jun; Ayoub, Albert E.; Emera, Deena; Leng, Jing; Cotney, Justin; Sarro, Richard; Rakic, Pasko; Noonan, James P. Evolutionary changes in promoter and enhancer activity during human corticogenesis, Science, Volume 347 (2015) no. 6226, pp. 1155-1159 | Article

[38] Shlyueva, Daria; Stampfel, Gerald; Stark, Alexander Transcriptional enhancers: from properties to genome-wide predictions, Nature Reviews Genetics, Volume 15 (2014) no. 4, pp. 272-286 | Article

[39] Smemo, Scott; Tena, Juan J.; Kim, Kyoung-Han; Gamazon, Eric R.; Sakabe, Noboru J.; Gómez-Marín, Carlos; Aneas, Ivy; Credidio, Flavia L.; Sobreira, Débora R.; Wasserman, Nora F.; Lee, Ju Hee; Puviindran, Vijitha; Tam, Davis; Shen, Michael; Son, Joe Eun; Vakili, Niki Alizadeh; Sung, Hoon-Ki; Naranjo, Silvia; Acemel, Rafael D.; Manzanares, Miguel; Nagy, Andras; Cox, Nancy J.; Hui, Chi-Chung; Gomez-Skarmeta, Jose Luis; Nóbrega, Marcelo A. Obesity-associated variants within FTO form long-range functional connections with IRX3, Nature, Volume 507 (2014) no. 7492, pp. 371-375 | Article

[40] Vavouri, Tanya; Lehner, Ben Conserved noncoding elements and the evolution of animal body plans, BioEssays, Volume 31 (2009) no. 7, pp. 727-735 | Article

[41] Wang, Jie; Zhuang, Jiali; Iyer, Sowmya; Lin, XinYing; Whitfield, Troy W.; Greven, Melissa C.; Pierce, Brian G.; Dong, Xianjun; Kundaje, Anshul; Cheng, Yong; Rando, Oliver J.; Birney, Ewan; Myers, Richard M.; Noble, William S.; Snyder, Michael; Weng, Zhiping Sequence features and chromatin structure around the genomic regions bound by 119 human transcription factors, Genome Research, Volume 22 (2012) no. 9, pp. 1798-1812 | Article

[42] Wang, Yanli; Song, Fan; Zhang, Bo; Zhang, Lijun; Xu, Jie; Kuang, Da; Li, Daofeng; Choudhary, Mayank N. K.; Li, Yun; Hu, Ming; Hardison, Ross; Wang, Ting; Yue, Feng The 3D Genome Browser: a web-based browser for visualizing 3D genome organization and long-range chromatin interactions, Genome Biology, Volume 19 (2018) no. 1 | Article

[43] Wenger, Aaron M.; Clarke, Shoa L.; Notwell, James H.; Chung, Tisha; Tuteja, Geetu; Guturu, Harendra; Schaar, Bruce T.; Bejerano, Gill The Enhancer Landscape during Early Neocortical Development Reveals Patterns of Dense Regulation and Co-option, PLoS Genetics, Volume 9 (2013) no. 8 | Article

[44] Won, Hyejung; de la Torre-Ubieta, Luis; Stein, Jason L.; Parikshak, Neelroop N.; Huang, Jerry; Opland, Carli K.; Gandal, Michael J.; Sutton, Gavin J.; Hormozdiari, Farhad; Lu, Daning; Lee, Changhoon; Eskin, Eleazar; Voineagu, Irina; Ernst, Jason; Geschwind, Daniel H. Chromosome conformation elucidates regulatory relationships in developing human brain, Nature, Volume 538 (2016) no. 7626, pp. 523-527 | Article

Cited by document(s). Sources: