Browse by volumes Browse by section

Evolutionary Biology

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

Novo, Francisco J.1  
1 Department of Biochemistry and Genetics. University of Navarra. c/ Irunlarrea, 1. 31008. Pamplona, Spain

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

Get full text PDF Peer reviewed and recommended by PCI

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: 10.24072/pcjournal.21
Novo, Francisco J. 1

1 Department of Biochemistry and Genetics. University of Navarra. c/ Irunlarrea, 1. 31008. Pamplona, Spain
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights 
@article{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/}
}
TY  - JOUR
AU  - Novo, Francisco J.
TI  - Evolutionary analysis of candidate non-coding elements regulating neurodevelopmental genes in vertebrates
JO  - Peer Community Journal
PY  - 2021
VL  - 1
PB  - Peer Community In
UR  - https://peercommunityjournal.org/articles/10.24072/pcjournal.21/
UR  - https://doi.org/10.24072/pcjournal.21
DO  - 10.24072/pcjournal.21
ID  - 10_24072_pcjournal_21
ER  - 
%0 Journal Article
%A Novo, Francisco J.
%T Evolutionary analysis of candidate non-coding elements regulating neurodevelopmental genes in vertebrates
%J Peer Community Journal
%D 2021
%V 1
%I Peer Community In
%U https://doi.org/10.24072/pcjournal.21
%R 10.24072/pcjournal.21
%F 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

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Altschul, S. F.; Gish, W.; Miller, W.; Myers, E. W.; Lipman, D. J. Basic local alignment search tool, Journal of Molecular Biology, Volume 215 (1990) no. 3, pp. 403-410 | DOI

[2] Andersson, R.; Gebhard, C.; Miguel-Escalada, I.; Hoof, I.; Bornholdt, J.; Boyd, M.; Chen, Y.; Zhao, X.; Schmidl, C.; Suzuki, T.; Ntini, E.; Arner, E.; Valen, E.; Li, K.; Schwarzfischer, L.; Glatz, D.; Raithel, J.; Lilje, B.; Rapin, N.; Bagger, F. O.; Jørgensen, M.; Andersen, P. R.; Bertin, N.; Rackham, O.; Burroughs, A. M.; Baillie, J. K.; Ishizu, Y.; Shimizu, Y.; Furuhata, E.; Maeda, S.; Negishi, Y.; Mungall, C. J.; Meehan, T. F.; Lassmann, T.; Itoh, M.; Kawaji, H.; Kondo, N.; Kawai, J.; Lennartsson, A.; Daub, C. O.; Heutink, P.; Hume, D. A.; Jensen, T. H.; Suzuki, H.; Hayashizaki, Y.; Müller, F.; Forrest, A. R. R.; Carninci, P.; Rehli, M.; Sandelin, A. An atlas of active enhancers across human cell types and tissues, Nature, Volume 507 (2014) no. 7493, pp. 455-461 | DOI

[3] Bae, B.-I.; Jayaraman, D.; Walsh, C. A. Genetic Changes Shaping the Human Brain, Developmental Cell, Volume 32 (2015) no. 4, pp. 423-434 | DOI

[4] Bakken, T. E.; Miller, J. A.; Ding, S.-L.; Sunkin, S. M.; Smith, K. A.; Ng, L.; Szafer, A.; Dalley, R. A.; Royall, J. J.; Lemon, T.; Shapouri, S.; Aiona, K.; Arnold, J.; Bennett, J. L.; Bertagnolli, D.; Bickley, K.; Boe, A.; Brouner, K.; Butler, S.; Byrnes, E.; Caldejon, S.; Carey, A.; Cate, S.; Chapin, M.; Chen, J.; Dee, N.; Desta, T.; Dolbeare, T. A.; Dotson, N.; Ebbert, A.; Fulfs, E.; Gee, G.; Gilbert, T. L.; Goldy, J.; Gourley, L.; Gregor, B.; Gu, G.; Hall, J.; Haradon, Z.; Haynor, D. R.; Hejazinia, N.; Hoerder-Suabedissen, A.; Howard, R.; Jochim, J.; Kinnunen, M.; Kriedberg, A.; Kuan, C. L.; Lau, C.; Lee, C.-K.; Lee, F.; Luong, L.; Mastan, N.; May, R.; Melchor, J.; Mosqueda, N.; Mott, E.; Ngo, K.; Nyhus, J.; Oldre, A.; Olson, E.; Parente, J.; Parker, P. D.; Parry, S.; Pendergraft, J.; Potekhina, L.; Reding, M.; Riley, Z. L.; Roberts, T.; Rogers, B.; Roll, K.; Rosen, D.; Sandman, D.; Sarreal, M.; Shapovalova, N.; Shi, S.; Sjoquist, N.; Sodt, A. J.; Townsend, R.; Velasquez, L.; Wagley, U.; Wakeman, W. B.; White, C.; Bennett, C.; Wu, J.; Young, R.; Youngstrom, B. L.; Wohnoutka, P.; Gibbs, R. A.; Rogers, J.; Hohmann, J. G.; Hawrylycz, M. J.; Hevner, R. F.; Molnár, Z.; Phillips, J. W.; Dang, C.; Jones, A. R.; Amaral, D. G.; Bernard, A.; Lein, E. S. A comprehensive transcriptional map of primate brain development, Nature, Volume 535 (2016) no. 7612, pp. 367-375 | DOI

[5] Bejerano, G.; Pheasant, M.; Makunin, I.; Stephen, S.; Kent, W. J.; Mattick, J. S.; Haussler, D. Ultraconserved Elements in the Human Genome, Science, Volume 304 (2004) no. 5675, pp. 1321-1325 | DOI

[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 | DOI

[7] Boyd, J. L.; Skove, S. L.; Rouanet, J. P.; Pilaz, L.-J.; Bepler, T.; Gordân, R.; Wray, G. A.; Silver, D. 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 | DOI

[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 | DOI

[9] Bulchand, S.; Subramanian, L.; Tole, S. 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 | DOI

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

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

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

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

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

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

[16] Fulco, C. P.; Munschauer, M.; Anyoha, R.; Munson, G.; Grossman, S. R.; Perez, E. M.; Kane, M.; Cleary, B.; Lander, E. S.; Engreitz, J. M. Systematic mapping of functional enhancer–promoter connections with CRISPR interference, Science, Volume 354 (2016) no. 6313, pp. 769-773 | DOI

[17] Gerstein, M. B.; Kundaje, A.; Hariharan, M.; Landt, S. G.; Yan, K.-K.; Cheng, C.; Mu, X. J.; Khurana, E.; Rozowsky, J.; Alexander, R.; Min, R.; Alves, P.; Abyzov, A.; Addleman, N.; Bhardwaj, N.; Boyle, A. P.; Cayting, P.; Charos, A.; Chen, D. Z.; Cheng, Y.; Clarke, D.; Eastman, C.; Euskirchen, G.; Frietze, S.; Fu, Y.; Gertz, J.; Grubert, F.; Harmanci, A.; Jain, P.; Kasowski, M.; Lacroute, P.; Leng, J.; Lian, J.; Monahan, H.; O’Geen, H.; Ouyang, Z.; Partridge, E. C.; Patacsil, D.; Pauli, F.; Raha, D.; Ramirez, L.; Reddy, T. E.; Reed, B.; Shi, M.; Slifer, T.; Wang, J.; Wu, L.; Yang, X.; Yip, K. Y.; Zilberman-Schapira, G.; Batzoglou, S.; Sidow, A.; Farnham, P. J.; Myers, R. M.; Weissman, S. M.; Snyder, M. Architecture of the human regulatory network derived from ENCODE data, Nature, Volume 489 (2012) no. 7414, pp. 91-100 | DOI

[18] He, Z.; Han, D.; Efimova, O.; Guijarro, P.; Yu, Q.; Oleksiak, A.; Jiang, S.; Anokhin, K.; Velichkovsky, B.; Grünewald, S.; Khaitovich, P. Comprehensive transcriptome analysis of neocortical layers in humans, chimpanzees and macaques, Nature Neuroscience, Volume 20 (2017) no. 6, pp. 886-895 | DOI

[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, J.; Sato, Y.; Sinclair, R.; Tsukamoto, K.; Nishida, M. 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 | DOI

[21] Kundaje, A.; Meuleman, W.; Ernst, J.; Bilenky, M.; Yen, A.; Heravi-Moussavi, A.; Kheradpour, P.; Zhang, Z.; Wang, J.; Ziller, M. J.; Amin, V.; Whitaker, J. W.; Schultz, M. D.; Ward, L. D.; Sarkar, A.; Quon, G.; Sandstrom, R. S.; Eaton, M. L.; Wu, Y.-C.; Pfenning, A. R.; Wang, X.; Claussnitzer, M.; Liu, Y.; Coarfa, C.; Harris, R. A.; Shoresh, N.; Epstein, C. B.; Gjoneska, E.; Leung, D.; Xie, W.; Hawkins, R. D.; Lister, R.; Hong, C.; Gascard, P.; Mungall, A. J.; Moore, R.; Chuah, E.; Tam, A.; Canfield, T. K.; Hansen, R. S.; Kaul, R.; Sabo, P. J.; Bansal, M. S.; Carles, A.; Dixon, J. R.; Farh, K.-H.; Feizi, S.; Karlic, R.; Kim, A.-R.; Kulkarni, A.; Li, D.; Lowdon, R.; Elliott, G.; Mercer, T. R.; Neph, S. J.; Onuchic, V.; Polak, P.; Rajagopal, N.; Ray, P.; Sallari, R. C.; Siebenthall, K. T.; Sinnott-Armstrong, N. A.; Stevens, M.; Thurman, R. E.; Wu, J.; Zhang, B.; Zhou, X.; Beaudet, A. E.; Boyer, L. A.; De Jager, P. L.; Farnham, P. J.; Fisher, S. J.; Haussler, D.; Jones, S. J. M.; Li, W.; Marra, M. A.; McManus, M. T.; Sunyaev, S.; Thomson, J. A.; Tlsty, T. D.; Tsai, L.-H.; Wang, W.; Waterland, R. A.; Zhang, M. Q.; Chadwick, L. H.; Bernstein, B. E.; Costello, J. F.; Ecker, J. R.; Hirst, M.; Meissner, A.; Milosavljevic, A.; Ren, B.; Stamatoyannopoulos, J. A.; Wang, T.; Kellis, M. Integrative analysis of 111 reference human epigenomes, Nature, Volume 518 (2015) no. 7539, pp. 317-330 | DOI

[22] Lane, M. E.; Runko, A. P.; Roy, N. M.; Sagerström, C. 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 | DOI

[23] Lowe, C. B.; Kellis, M.; Siepel, A.; Raney, B. J.; Clamp, M.; Salama, S. R.; Kingsley, D. M.; Lindblad-Toh, K.; Haussler, D. Three Periods of Regulatory Innovation During Vertebrate Evolution, Science, Volume 333 (2011) no. 6045, pp. 1019-1024 | DOI

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

[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 | DOI

[26] McCollum, C. W.; Amin, S. R.; Pauerstein, P.; Lane, M. E. 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 | DOI

[27] McEwen, G. K.; Goode, D. K.; Parker, H. J.; Woolfe, A.; Callaway, H.; Elgar, G. Early Evolution of Conserved Regulatory Sequences Associated with Development in Vertebrates, PLoS Genetics, Volume 5 (2009) no. 12 | DOI

[28] McLean, C. Y.; Bristor, D.; Hiller, M.; Clarke, S. L.; Schaar, B. T.; Lowe, C. B.; Wenger, A. M.; Bejerano, G. GREAT improves functional interpretation of cis-regulatory regions, Nature Biotechnology, Volume 28 (2010) no. 5, pp. 495-501 | DOI

[29] Melé, M.; Ferreira, P. G.; Reverter, F.; DeLuca, D. S.; Monlong, J.; Sammeth, M.; Young, T. R.; Goldmann, J. M.; Pervouchine, D. D.; Sullivan, T. J.; Johnson, R.; Segrè, A. V.; Djebali, S.; Niarchou, A.; Consortium, T. G.; Wright, F. A.; Lappalainen, T.; Calvo, M.; Getz, G.; Dermitzakis, E. T.; Ardlie, K. G.; Guigó, R. The human transcriptome across tissues and individuals, Science, Volume 348 (2015) no. 6235, pp. 660-665 | DOI

[30] Miller, J. A.; Ding, S.-L.; Sunkin, S. M.; Smith, K. A.; Ng, L.; Szafer, A.; Ebbert, A.; Riley, Z. L.; Royall, J. J.; Aiona, K.; Arnold, J. M.; Bennet, C.; Bertagnolli, D.; Brouner, K.; Butler, S.; Caldejon, S.; Carey, A.; Cuhaciyan, C.; Dalley, R. A.; Dee, N.; Dolbeare, T. A.; Facer, B. A. C.; Feng, D.; Fliss, T. P.; Gee, G.; Goldy, J.; Gourley, L.; Gregor, B. W.; Gu, G.; Howard, R. E.; Jochim, J. M.; Kuan, C. L.; Lau, C.; Lee, C.-K.; Lee, F.; Lemon, T. A.; Lesnar, P.; McMurray, B.; Mastan, N.; Mosqueda, N.; Naluai-Cecchini, T.; Ngo, N.-K.; Nyhus, J.; Oldre, A.; Olson, E.; Parente, J.; Parker, P. D.; Parry, S. E.; Stevens, A.; Pletikos, M.; Reding, M.; Roll, K.; Sandman, D.; Sarreal, M.; Shapouri, S.; Shapovalova, N. V.; Shen, E. H.; Sjoquist, N.; Slaughterbeck, C. R.; Smith, M.; Sodt, A. J.; Williams, D.; Zöllei, L.; Fischl, B.; Gerstein, M. B.; Geschwind, D. H.; Glass, I. A.; Hawrylycz, M. J.; Hevner, R. F.; Huang, H.; Jones, A. R.; Knowles, J. A.; Levitt, P.; Phillips, J. W.; Šestan, N.; Wohnoutka, P.; Dang, C.; Bernard, A.; Hohmann, J. G.; Lein, E. S. Transcriptional landscape of the prenatal human brain, Nature, Volume 508 (2014) no. 7495, pp. 199-206 | DOI

[31] Notwell, J. H.; Chung, T.; Heavner, W.; Bejerano, G. A family of transposable elements co-opted into developmental enhancers in the mouse neocortex, Nature Communications, Volume 6 (2015) no. 1 | DOI

[32] Ocaña, F. M.; Suryanarayana, S. M.; Saitoh, K.; Kardamakis, A. A.; Capantini, L.; Robertson, B.; Grillner, S. The Lamprey Pallium Provides a Blueprint of the Mammalian Motor Projections from Cortex, Current Biology, Volume 25 (2015) no. 4, pp. 413-423 | DOI

[33] Okbay, A.; Beauchamp, J. P.; Fontana, M. A.; Lee, J. J.; Pers, T. H.; Rietveld, C. A.; Turley, P.; Chen, G.-B.; Emilsson, V.; Meddens, S. F. W.; Oskarsson, S.; Pickrell, J. K.; Thom, K.; Timshel, P.; de Vlaming, R.; Abdellaoui, A.; Ahluwalia, T. S.; Bacelis, J.; Baumbach, C.; Bjornsdottir, G.; Brandsma, J. H.; Pina Concas, M.; Derringer, J.; Furlotte, N. A.; Galesloot, T. E.; Girotto, G.; Gupta, R.; Hall, L. M.; Harris, S. E.; Hofer, E.; Horikoshi, M.; Huffman, J. E.; Kaasik, K.; Kalafati, I. P.; Karlsson, R.; Kong, A.; Lahti, J.; Lee, S. J. v. d.; deLeeuw, C.; Lind, P. A.; Lindgren, K.-O.; Liu, T.; Mangino, M.; Marten, J.; Mihailov, E.; Miller, M. B.; van der Most, P. J.; Oldmeadow, C.; Payton, A.; Pervjakova, N.; Peyrot, W. J.; Qian, Y.; Raitakari, O.; Rueedi, R.; Salvi, E.; Schmidt, B.; Schraut, K. E.; Shi, J.; Smith, A. V.; Poot, R. A.; St Pourcain, B.; Teumer, A.; Thorleifsson, G.; Verweij, N.; Vuckovic, D.; Wellmann, J.; Westra, H.-J.; Yang, J.; Zhao, W.; Zhu, Z.; Alizadeh, B. Z.; Amin, N.; Bakshi, A.; Baumeister, S. E.; Biino, G.; Bønnelykke, K.; Boyle, P. A.; Campbell, H.; Cappuccio, F. P.; Davies, G.; De Neve, J.-E.; Deloukas, P.; Demuth, I.; Ding, J.; Eibich, P.; Eisele, L.; Eklund, N.; Evans, D. M.; Faul, J. D.; Feitosa, M. F.; Forstner, A. J.; Gandin, I.; Gunnarsson, B.; Halldórsson, B. V.; Harris, T. B.; Heath, A. C.; Hocking, L. J.; Holliday, E. G.; Homuth, G.; Horan, M. A.; Hottenga, J.-J.; de Jager, P. L.; Joshi, P. K.; Jugessur, A.; Kaakinen, M. A.; Kähönen, M.; Kanoni, S.; Keltigangas-Järvinen, L.; Kiemeney, L. A. L. M.; Kolcic, I.; Koskinen, S.; Kraja, A. T.; Kroh, M.; Kutalik, Z.; Latvala, A.; Launer, L. J.; Lebreton, M. P.; Levinson, D. F.; Lichtenstein, P.; Lichtner, P.; Liewald, D. C. M.; Cohort Study, L.; Loukola, A.; Madden, P. A.; Mägi, R.; Mäki-Opas, T.; Marioni, R. E.; Marques-Vidal, P.; Meddens, G. A.; McMahon, G.; Meisinger, C.; Meitinger, T.; Milaneschi, Y.; Milani, L.; Montgomery, G. W.; Myhre, R.; Nelson, C. P.; Nyholt, D. R.; Ollier, W. E. R.; Palotie, A.; Paternoster, L.; Pedersen, N. L.; Petrovic, K. E.; Porteous, D. J.; Räikkönen, K.; Ring, S. M.; Robino, A.; Rostapshova, O.; Rudan, I.; Rustichini, A.; Salomaa, V.; Sanders, A. R.; Sarin, A.-P.; Schmidt, H.; Scott, R. J.; Smith, B. H.; Smith, J. A.; Staessen, J. A.; Steinhagen-Thiessen, E.; Strauch, K.; Terracciano, A.; Tobin, M. D.; Ulivi, S.; Vaccargiu, S.; Quaye, L.; van Rooij, F. J. A.; Venturini, C.; Vinkhuyzen, A. A. E.; Völker, U.; Völzke, H.; Vonk, J. M.; Vozzi, D.; Waage, J.; Ware, E. B.; Willemsen, G.; Attia, J. R.; Bennett, D. A.; Berger, K.; Bertram, L.; Bisgaard, H.; Boomsma, D. I.; Borecki, I. B.; Bültmann, U.; Chabris, C. F.; Cucca, F.; Cusi, D.; Deary, I. J.; Dedoussis, G. V.; van Duijn, C. M.; Eriksson, J. G.; Franke, B.; Franke, L.; Gasparini, P.; Gejman, P. V.; Gieger, C.; Grabe, H.-J.; Gratten, J.; Groenen, P. J. F.; Gudnason, V.; van der Harst, P.; Hayward, C.; Hinds, D. A.; Hoffmann, W.; Hyppönen, E.; Iacono, W. G.; Jacobsson, B.; Järvelin, M.-R.; Jöckel, K.-H.; Kaprio, J.; Kardia, S. L. R.; Lehtimäki, T.; Lehrer, S. F.; Magnusson, P. K. E.; Martin, N. G.; McGue, M.; Metspalu, A.; Pendleton, N.; Penninx, B. W. J. H.; Perola, M.; Pirastu, N.; Pirastu, M.; Polasek, O.; Posthuma, D.; Power, C.; Province, M. A.; Samani, N. J.; Schlessinger, D.; Schmidt, R.; Sørensen, T. I. A.; Spector, T. D.; Stefansson, K.; Thorsteinsdottir, U.; Thurik, A. R.; Timpson, N. J.; Tiemeier, H.; Tung, J. Y.; Uitterlinden, A. G.; Vitart, V.; Vollenweider, P.; Weir, D. R.; Wilson, J. F.; Wright, A. F.; Conley, D. C.; Krueger, R. F.; Davey Smith, G.; Hofman, A.; Laibson, D. I.; Medland, S. E.; Meyer, M. N.; Yang, J.; Johannesson, M.; Visscher, P. M.; Esko, T.; Koellinger, P. D.; Cesarini, D.; Benjamin, D. J. Genome-wide association study identifies 74 loci associated with educational attainment, Nature, Volume 533 (2016) no. 7604, pp. 539-542 | DOI

[34] Pauls, S.; Goode, D. K.; Petrone, L.; Oliveri, P.; Elgar, G. Evolution of lineage-specific functions in ancient cis -regulatory modules, Open Biology, Volume 5 (2015) no. 11 | DOI

[35] Pennacchio, L. A.; Ahituv, N.; Moses, A. M.; Prabhakar, S.; Nobrega, M. A.; Shoukry, M.; Minovitsky, S.; Dubchak, I.; Holt, A.; Lewis, K. D.; Plajzer-Frick, I.; Akiyama, J.; De Val, S.; Afzal, V.; Black, B. L.; Couronne, O.; Eisen, M. B.; Visel, A.; Rubin, E. M. In vivo enhancer analysis of human conserved non-coding sequences, Nature, Volume 444 (2006) no. 7118, pp. 499-502 | DOI

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

[37] Reilly, S. K.; Yin, J.; Ayoub, A. E.; Emera, D.; Leng, J.; Cotney, J.; Sarro, R.; Rakic, P.; Noonan, J. P. Evolutionary changes in promoter and enhancer activity during human corticogenesis, Science, Volume 347 (2015) no. 6226, pp. 1155-1159 | DOI

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

[39] Smemo, S.; Tena, J. J.; Kim, K.-H.; Gamazon, E. R.; Sakabe, N. J.; Gómez-Marín, C.; Aneas, I.; Credidio, F. L.; Sobreira, D. R.; Wasserman, N. F.; Lee, J. H.; Puviindran, V.; Tam, D.; Shen, M.; Son, J. E.; Vakili, N. A.; Sung, H.-K.; Naranjo, S.; Acemel, R. D.; Manzanares, M.; Nagy, A.; Cox, N. J.; Hui, C.-C.; Gomez-Skarmeta, J. L.; Nóbrega, M. A. Obesity-associated variants within FTO form long-range functional connections with IRX3, Nature, Volume 507 (2014) no. 7492, pp. 371-375 | DOI

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

[41] Wang, J.; Zhuang, J.; Iyer, S.; Lin, X.; Whitfield, T. W.; Greven, M. C.; Pierce, B. G.; Dong, X.; Kundaje, A.; Cheng, Y.; Rando, O. J.; Birney, E.; Myers, R. M.; Noble, W. S.; Snyder, M.; Weng, Z. 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 | DOI

[42] Wang, Y.; Song, F.; Zhang, B.; Zhang, L.; Xu, J.; Kuang, D.; Li, D.; Choudhary, M. N. K.; Li, Y.; Hu, M.; Hardison, R.; Wang, T.; Yue, F. 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 | DOI

[43] Wenger, A. M.; Clarke, S. L.; Notwell, J. H.; Chung, T.; Tuteja, G.; Guturu, H.; Schaar, B. T.; Bejerano, G. The Enhancer Landscape during Early Neocortical Development Reveals Patterns of Dense Regulation and Co-option, PLoS Genetics, Volume 9 (2013) no. 8 | DOI

[44] Won, H.; de la Torre-Ubieta, L.; Stein, J. L.; Parikshak, N. N.; Huang, J.; Opland, C. K.; Gandal, M. J.; Sutton, G. J.; Hormozdiari, F.; Lu, D.; Lee, C.; Eskin, E.; Voineagu, I.; Ernst, J.; Geschwind, D. H. Chromosome conformation elucidates regulatory relationships in developing human brain, Nature, Volume 538 (2016) no. 7626, pp. 523-527 | DOI

Cited by Sources: