Molecular signatures of selection on the human GLI3 associated central nervous system specific enhancers.
Central nervous system
Gli3
Human populations
Positive selection
SNPs
Transcription factors
Journal
Development genes and evolution
ISSN: 1432-041X
Titre abrégé: Dev Genes Evol
Pays: Germany
ID NLM: 9613264
Informations de publication
Date de publication:
03 2021
03 2021
Historique:
received:
24
09
2020
accepted:
09
02
2021
pubmed:
4
3
2021
medline:
21
9
2021
entrez:
3
3
2021
Statut:
ppublish
Résumé
The zinc finger-containing transcription factor Gli3 is a key mediator of Hedgehog (Hh) signaling pathway. In vertebrates, Gli3 has widespread expression pattern during early embryonic development. Along the anteroposterior axes of the central nervous system (CNS), dorsoventral neural pattern elaboration is achieved through Hh mediated spatio-temporal deployment of Gli3 transcripts. Previously, we and others uncovered a set of enhancers that mediate many of the known aspects of Gli3 expression during neurogenesis. However, the potential role of Gli3 associated enhancers in trait evolution has not yet received any significant attention. Here, we investigate the evolutionary patterns of Gli3 associated CNS-specific enhancers that have been reported so far. A subset of these enhancers has undergone an accelerated rate of molecular evolution in the human lineage in comparison to other primates/mammals. These fast-evolving enhancers have acquired human-specific changes in transcription factor binding sites (TFBSs). These human-unique changes within subset of Gli3 associated CNS-specific enhancers were further validated as single nucleotide polymorphisms through 1000 Genome Project Phase 3 data. This work not only infers the molecular evolutionary patterns of Gli3 associated enhancers but also provides clues for putative genetic basis of the population-specificity of gene expression regulation.
Identifiants
pubmed: 33655411
doi: 10.1007/s00427-021-00672-1
pii: 10.1007/s00427-021-00672-1
doi:
Substances chimiques
GLI3 protein, human
0
Nerve Tissue Proteins
0
Zinc Finger Protein Gli3
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
21-32Subventions
Organisme : Higher Education Commission (HEC) of Pakistan
ID : 315-4672-2BS3-053
Références
Abbasi AA, Paparidis Z, Malik S, Goode DK, Callaway H, Elgar G, Grzeschik KH (2007) Human GLI3 intragenic conserved non-coding sequences are tissue-specific enhancers. PLoS One 2:e366. https://doi.org/10.1371/journal.pone.0000366
doi: 10.1371/journal.pone.0000366
pubmed: 17426814
pmcid: 1838922
Abbasi AA, Goode DK, Amir S, Grzeschik K-H (2009) Evolution and functional diversification of the GLI family of transcription factors in vertebrates. Evol Bioinformatics Online 5:5–13. https://doi.org/10.4137/ebo.s2322
doi: 10.4137/ebo.s2322
Abbasi AA, Paparidis Z, Malik S, Bangs F, Schmidt A, Koch S, Lopez-Rios J, Grzeschik KH (2010) Human intronic enhancers control distinct sub-domains of Gli3 expression during mouse CNS and limb development. BMC Dev Biol 10:44. https://doi.org/10.1186/1471-213X-10-44
doi: 10.1186/1471-213X-10-44
pubmed: 20426846
pmcid: 2875213
Abbasi AA, Minhas R, Schmidt A, Koch S, Grzeschik KH (2013) Cis-regulatory underpinnings of human GLI3 expression in embryonic craniofacial structures and internal organs. Develop Growth Differ 55:699–709. https://doi.org/10.1111/dgd.12076
doi: 10.1111/dgd.12076
Ali S, Amina B, Anwar S, Minhas R, Parveen N, Nawaz U, Azam SS, Abbasi AA (2016) Genomic features of human limb specific enhancers. Genomics 108:143–150. https://doi.org/10.1016/j.ygeno.2016.08.003
doi: 10.1016/j.ygeno.2016.08.003
pubmed: 27580967
Allahyari RV, Clark KL, Shepard KA, Garcia ADR (2019) Sonic Hedgehog signaling is negatively regulated in reactive astrocytes after forebrain stab injury. Sci Rep 9:565. https://doi.org/10.1038/s41598-018-37555-x
doi: 10.1038/s41598-018-37555-x
pubmed: 30679745
pmcid: 6345977
Al-Qattan MM, Al Abdulkareem I, Al Haidan Y, Al Balwi M (2012) A novel mutation in the SHH long-range regulator (ZRS) is associated with preaxial polydactyly, triphalangeal thumb, and severe radial ray deficiency. Am J Med Genet A 158A:2610–2615. https://doi.org/10.1002/ajmg.a.35584
doi: 10.1002/ajmg.a.35584
pubmed: 22903933
Alvarez-Medina R, Cayuso J, Okubo T, Takada S, Marti E (2008) Wnt canonical pathway restricts graded Shh/Gli patterning activity through the regulation of Gli3 expression. Dev Camb Engl 135:237–247. https://doi.org/10.1242/dev.012054
doi: 10.1242/dev.012054
Antao T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G (2008) LOSITAN: A workbench to detect molecular adaptation based on a Fst-outlier method. BMC Bioinformatics 9:323. https://doi.org/10.1186/1471-2105-9-323
doi: 10.1186/1471-2105-9-323
pubmed: 18662398
pmcid: 2515854
Anwar S, Minhas R, Ali S, Lambert N, Kawakami Y, Elgar G, Azam SS, Abbasi AA (2015) Identification and functional characterization of novel transcriptional enhancers involved in regulating human GLI3 expression during early development. Develop Growth Differ 57:570–580. https://doi.org/10.1111/dgd.12239
doi: 10.1111/dgd.12239
Aoto K, Nishimura T, Eto K, Motoyama J (2002) Mouse GLI3 regulates Fgf8 expression and apoptosis in the developing neural tube, face, and limb bud. Dev Biol 251:320–332. https://doi.org/10.1006/dbio.2002.0811
doi: 10.1006/dbio.2002.0811
pubmed: 12435361
Auton A, Abecasis GR, Altshuler DM et al (2015) A global reference for human genetic variation. Nature 526:68–74. https://doi.org/10.1038/nature15393
doi: 10.1038/nature15393
Bai CB, Stephen D, Joyner AL (2004) All mouse ventral spinal cord patterning by Hedgehog is Gli dependent and involves an activator function of Gli3. Dev Cell 6:103–115
doi: 10.1016/S1534-5807(03)00394-0
Biesecker LG (2006) What you can learn from one gene: GLI3. J Med Genet 43:465–469. https://doi.org/10.1136/jmg.2004.029181
doi: 10.1136/jmg.2004.029181
pubmed: 16740916
pmcid: 2564530
Bonhomme M, Chevalet C, Servin B, Boitard S, Abdallah J, Blott S, SanCristobal M (2010) Detecting selection in population trees: the Lewontin and Krakauer test extended. Genetics 186:241–262. https://doi.org/10.1534/genetics.110.117275
doi: 10.1534/genetics.110.117275
pubmed: 20855576
pmcid: 2940290
Boyd JL, Skove SL, Rouanet JP, Pilaz LJ, Bepler T, Gordân R, Wray GA, Silver DL (2015) Human-chimpanzee differences in a FZD8 enhancer alter cell-cycle dynamics in the developing neocortex. Curr Biol CB 25:772–779. https://doi.org/10.1016/j.cub.2015.01.041
doi: 10.1016/j.cub.2015.01.041
pubmed: 25702574
Böse J, Grotewold L, Rüther U, (2002) Pallister-Hall syndrome phenotype in mice mutant for Gli3. Hum Mol Genet 11:1129–1135. https://doi.org/10.1093/hmg/11.9.1129
doi: 10.1093/hmg/11.9.1129
Burgess DJ (2016) Regulatory elements: putting enhancers into context. Nat Rev Genet 17:377. https://doi.org/10.1038/nrg.2016.74
doi: 10.1038/nrg.2016.74
pubmed: 27240812
Cao T, Wang C, Yang M, Wu C, Wang B (2013) Mouse limbs expressing only the Gli3 repressor resemble those of Sonic Hedgehog mutants. Dev Biol 379:221–228. https://doi.org/10.1016/j.ydbio.2013.04.025
doi: 10.1016/j.ydbio.2013.04.025
pubmed: 23644062
pmcid: 3707282
Capellini TD, Chen H, Cao J, Doxey AC, Kiapour AM, Schoor M, Kingsley DM (2017) Ancient selection for derived alleles at a GDF5 enhancer influencing human growth and osteoarthritis risk. Nat Genet 49:1202–1210. https://doi.org/10.1038/ng.3911
doi: 10.1038/ng.3911
pubmed: 28671685
pmcid: 6556117
Carullo NVN, Day JJ (2019) Genomic enhancers in brain health and disease. Genes 10. https://doi.org/10.3390/genes10010043
Chan YF, Marks ME, Jones FC, Villarreal G, Shapiro MD, Brady SD, Southwick AM, Absher DM, Grimwood J, Schmutz J, Myers RM, Petrov D, Jonsson B, Schluter D, Bell MA, Kingsley DM (2010) Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327:302–305. https://doi.org/10.1126/science.1182213
doi: 10.1126/science.1182213
pubmed: 20007865
Chuang J-Y, Kao T-J, Lin S-H, Wu AC, Lee PT, Su TP, Yeh SH, Lee YC, Wu CC, Chang WC (2016) Specificity protein 1-zinc finger protein 179 pathway is involved in the attenuation of oxidative stress following brain injury. Redox Biol 11:135–143. https://doi.org/10.1016/j.redox.2016.11.012
doi: 10.1016/j.redox.2016.11.012
pubmed: 27918959
pmcid: 5144757
Coy S, Caamaño JH, Carvajal J et al (2011) A novel Gli3 enhancer controls the Gli3 spatiotemporal expression pattern through a TALE homeodomain protein binding site▿. Mol Cell Biol 31:1432–1443. https://doi.org/10.1128/MCB.00451-10
doi: 10.1128/MCB.00451-10
pubmed: 21262763
pmcid: 3135294
Coyle SM, Huntingford FA, Peichel CL (2007) Parallel evolution of Pitx1 underlies pelvic reduction in Scottish threespine stickleback (Gasterosteus aculeatus). J Hered 98:581–586. https://doi.org/10.1093/jhered/esm066
doi: 10.1093/jhered/esm066
pubmed: 17693397
Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST, McVean G, Durbin R, 1000 Genomes Project Analysis Group (2011) The variant call format and VCFtools. Bioinformatics 27:2156–2158. https://doi.org/10.1093/bioinformatics/btr330
doi: 10.1093/bioinformatics/btr330
pubmed: 21653522
pmcid: 21653522
Davis A, Reubens MC, Stellwag EJ (2016) Functional and comparative genomics of Hoxa2 gene cis-regulatory elements: evidence for evolutionary modification of ancestral core element activity. J Dev Biol 4:15
doi: 10.3390/jdb4020015
Démurger F, Ichkou A, Mougou-Zerelli S, Le Merrer M, Goudefroye G, Delezoide AL et al (2015) New insights into genotype-phenotype correlation for GLI3 mutations. Eur J Hum Genet 23:92–102. https://doi.org/10.1038/ejhg.2014.62
doi: 10.1038/ejhg.2014.62
pubmed: 24736735
Deng L, Xu S (2017) Adaptation of human skin color in various populations. Hereditas 155:1. https://doi.org/10.1186/s41065-017-0036-2
doi: 10.1186/s41065-017-0036-2
pubmed: 28701907
pmcid: 5502412
Douglas AT, Hill RD (2014) Variation in vertebrate cis-regulatory elements in evolution and disease. Transcription 5:e28848. https://doi.org/10.4161/trns.28848
doi: 10.4161/trns.28848
pubmed: 25764334
pmcid: 4215174
Eppig JT, Richardson JE, Kadin JA, Ringwald M, Blake JA, Bult CJ (2015) Mouse Genome Informatics (MGI): reflecting on 25 years. Mamm Genome 26:272–284. https://doi.org/10.1007/s00335-015-9589-4
doi: 10.1007/s00335-015-9589-4
pubmed: 26238262
pmcid: 4534491
Fariello MI, Boitard S, Naya H, SanCristobal M, Servin B (2013) Detecting signatures of selection through haplotype differentiation among hierarchically structured populations. Genetics 193:929–941. https://doi.org/10.1534/genetics.112.147231
doi: 10.1534/genetics.112.147231
pubmed: 23307896
pmcid: 3584007
Fischer MC, Foll M, Excoffier L, Heckel G (2011) Enhanced AFLP genome scans detect local adaptation in high-altitude populations of a small rodent (Microtus arvalis). Mol Ecol 20:1450–1462. https://doi.org/10.1111/j.1365-294X.2011.05015.x
doi: 10.1111/j.1365-294X.2011.05015.x
pubmed: 21352386
Foll M (2012) BayeScan v2. 1 User manual. Ecology 20:1450–1462
Gautier M, Vitalis R (2012) rehh: an R package to detect footprints of selection in genome-wide SNP data from haplotype structure. Bioinformatics 28:1176–1177. https://doi.org/10.1093/bioinformatics/bts115
doi: 10.1093/bioinformatics/bts115
pubmed: 22402612
Grabe N (2002) AliBaba2: context specific identification of transcription factor binding sites. In Silico Biol 2:S1–S15
pubmed: 11808873
Haddad-Tóvolli R, Paul FA, Zhang Y et al (2015) Differential requirements for Gli2 and Gli3 in the regional specification of the mouse hypothalamus. Front Neuroanat 9. https://doi.org/10.3389/fnana.2015.00034
Hancock AM, Alkorta-Aranburu G, Witonsky DB, Di Rienzo A (2010) Adaptations to new environments in humans: the role of subtle allele frequency shifts. Philos Trans R Soc Lond B Biol Sci 365:2459–2468. https://doi.org/10.1098/rstb.2010.0032
doi: 10.1098/rstb.2010.0032
pubmed: 20643735
pmcid: 2935101
Hata J, Matsuda K, Ninomiya T, Yonemoto K, Matsushita T, Ohnishi Y, Saito S, Kitazono T, Ibayashi S, Iida M, Kiyohara Y, Nakamura Y, Kubo M (2007) Functional SNP in an Sp1-binding site of AGTRL1 gene is associated with susceptibility to brain infarction. Hum Mol Genet 16:630–639. https://doi.org/10.1093/hmg/ddm005
doi: 10.1093/hmg/ddm005
pubmed: 17309882
Hu MC, Mo R, Bhella S, Wilson CW, Chuang PT, Hui CC, Rosenblum ND (2006) GLI3-dependent transcriptional repression of Gli1, Gli2 and kidney patterning genes disrupts renal morphogenesis. Development 133:569–578. https://doi.org/10.1242/dev.02220
doi: 10.1242/dev.02220
pubmed: 16396903
Johnson EJ, Neely DM, Dunn IC, Davey MG (2014) Direct functional consequences of ZRS enhancer mutation combine with secondary long range SHH signalling effects to cause preaxial polydactyly. Dev Biol 392:209–220. https://doi.org/10.1016/j.ydbio.2014.05.025
doi: 10.1016/j.ydbio.2014.05.025
pubmed: 24907417
pmcid: 4111902
Kalff-Suske M, Wild A, Topp J, Wessling M, Jacobsen E-M, Bornholdt D et al (1999) Point Mutations Throughout the GLI3 Gene Cause Greig Cephalopolysyndactyly Syndrome. Hum Mol Genet 8:1769–1777. https://doi.org/10.1093/hmg/8.9.1769
doi: 10.1093/hmg/8.9.1769
pubmed: 10441342
Karlstrom RO, Tyurina OV, Kawakami A, Nishioka N, Talbot WS, Sasaki H, Schier AF (2003) Genetic analysis of zebrafish gli1 and gli2 reveals divergent requirements for gli genes in vertebrate development. Development 130:1549–1564. https://doi.org/10.1242/dev.00364
doi: 10.1242/dev.00364
pubmed: 12620981
Korneliussen TS, Moltke I, Albrechtsen A, Nielsen R (2013) Calculation of Tajima’s D and other neutrality test statistics from low depth next-generation sequencing data. BMC Bioinformatics 14:289. https://doi.org/10.1186/1471-2105-14-289
doi: 10.1186/1471-2105-14-289
pubmed: 24088262
pmcid: 4015034
Kvon EZ, Zhu Y, Kelman G et al (2020) Comprehensive in vivo interrogation reveals phenotypic impact of human enhancer variants. Cell 180:1262–1271.e15. https://doi.org/10.1016/j.cell.2020.02.031
doi: 10.1016/j.cell.2020.02.031
pubmed: 32169219
pmcid: 7179509
Leal F, Cohn MJ (2017) Developmental, genetic, and genomic insights into the evolutionary loss of limbs in snakes. Genesis 56(1). https://doi.org/10.1002/dvg.23077
Levchenko A, Kanapin A, Samsonova A, Gainetdinov RR (2018) Human accelerated regions and other human-specific sequence variations in the context of evolution and their relevance for brain development. Genome Biol Evol 10:166–188. https://doi.org/10.1093/gbe/evx240
doi: 10.1093/gbe/evx240
pubmed: 29149249
Long HK, Prescott SL, Wysocka J (2016) Ever-changing landscapes: transcriptional enhancers in development and evolution. Cell 167:1170–1187. https://doi.org/10.1016/j.cell.2016.09.018
doi: 10.1016/j.cell.2016.09.018
pubmed: 27863239
pmcid: 5123704
Malomane DK, Reimer C, Weigend S, Weigend A, Sharifi AR, Simianer H (2018) Efficiency of different strategies to mitigate ascertainment bias when using SNP panels in diversity studies. BMC Genomics 19:22. https://doi.org/10.1186/s12864-017-4416-9
doi: 10.1186/s12864-017-4416-9
pubmed: 29304727
pmcid: 5756397
Matissek SJ, Elsawa SF (2020) GLI3: a mediator of genetic diseases, development and cancer. Cell Commun Signal 18:54. https://doi.org/10.1186/s12964-020-00540-x
doi: 10.1186/s12964-020-00540-x
pubmed: 32245491
pmcid: 7119169
Memi F, Zecevic N, Radonjić N (2018) Multiple roles of Sonic Hedgehog in the developing human cortex are suggested by its widespread distribution. Brain Struct Funct 223:2361–2375. https://doi.org/10.1007/s00429-018-1621-5
doi: 10.1007/s00429-018-1621-5
pubmed: 29492654
pmcid: 5968052
Methot N, Basler K (2001) An absolute requirement for Cubitus interruptus in Hedgehog signaling. Development 128:733–742
pubmed: 11171398
Mill P, Mo R, Fu H, Grachtchouk M, Kim PC, Dlugosz AA, Hui CC (2003) Sonic Hedgehog-dependent activation of Gli2 is essential for embryonic hair follicle development. Genes Dev 17:282–294. https://doi.org/10.1101/gad.1038103
doi: 10.1101/gad.1038103
pubmed: 12533516
pmcid: 195973
Moon JM, Capra JA, Abbot P, Rokas A (2019) Signatures of recent positive selection in enhancers across 41 human tissues. G3 Genes Genomes Genetics 9:2761–2774. https://doi.org/10.1534/g3.119.400186
doi: 10.1534/g3.119.400186
pubmed: 31213516
pmcid: 6686946
Nielsen ES, Henriques R, Toonen RJ, Knapp ISS, Guo B, von der Heyden S (2018) Complex signatures of genomic variation of two non-model marine species in a homogeneous environment. BMC Genomics 19:347. https://doi.org/10.1186/s12864-018-4721-y
doi: 10.1186/s12864-018-4721-y
pubmed: 29743012
pmcid: 5944137
Nishizaki SS, Ng N, Dong S et al (2019) Predicting the effects of SNPs on transcription factor binding affinity. Bioinformatics. https://doi.org/10.1093/bioinformatics/btz612
O’Connor L, Gilmour J, Bonifer C (2016) The role of the ubiquitously expressed transcription factor Sp1 in tissue-specific transcriptional regulation and in disease. Yale J Biol Med 89:513–525
pubmed: 28018142
pmcid: 5168829
Onat OE, Tez M, Ozçelik T, Törüner GA (2006) MDM2 T309G polymorphism is associated with bladder cancer. Anticancer Res 26:3473–3475
pubmed: 17094469
Osterwalder M, Barozzi I, Tissières V, Fukuda-Yuzawa Y, Mannion BJ, Afzal SY, Lee EA, Zhu Y, Plajzer-Frick I, Pickle CS, Kato M, Garvin TH, Pham QT, Harrington AN, Akiyama JA, Afzal V, Lopez-Rios J, Dickel DE, Visel A, Pennacchio LA (2018) Enhancer redundancy allows for phenotypic robustness in mammalian development. Nature 554:239–243. https://doi.org/10.1038/nature25461
doi: 10.1038/nature25461
pubmed: 29420474
pmcid: 5808607
Pearson AG, Curtis MA, Waldvogel HJ, Faull RLM, Dragunow M (2005) Activating transcription factor 2 expression in the adult human brain: association with both neurodegeneration and neurogenesis. Neuroscience 133:437–451. https://doi.org/10.1016/j.neuroscience.2005.02.029
doi: 10.1016/j.neuroscience.2005.02.029
pubmed: 15878807
Pfeifer B, Wittelsbürger U, Ramos-Onsins SE, Lercher MJ (2014) PopGenome: an efficient Swiss army knife for population genomic analyses in R. Mol Biol Evol 31:1929–1936. https://doi.org/10.1093/molbev/msu136
doi: 10.1093/molbev/msu136
pubmed: 24739305
pmcid: 4069620
Prabhakar S, Noonan JP, Pääbo S, Rubin EM (2006) Accelerated evolution of conserved noncoding sequences in humans. Science 314:786. https://doi.org/10.1126/science.1130738
doi: 10.1126/science.1130738
pubmed: 17082449
Ryu H, Lee J, Zaman K, Kubilis J, Ferrante RJ, Ross BD, Neve R, Rattan RR (2003) Sp1 and Sp3 Are Oxidative Stress-Inducible, Antideath Transcription Factors in Cortical Neurons. J Neurosci 23:3597–3606. https://doi.org/10.1523/jneurosci.23-09-03597.2003
doi: 10.1523/jneurosci.23-09-03597.2003
pubmed: 12736330
pmcid: 6742168
Sabeti PC, Reich DE, Higgins JM, Levine HZP, Richter DJ, Schaffner SF, Gabriel SB, Platko JV, Patterson NJ, McDonald GJ, Ackerman HC, Campbell SJ, Altshuler D, Cooper R, Kwiatkowski D, Ward R, Lander ES (2002) Detecting recent positive selection in the human genome from haplotype structure. Nature 419:832–837. https://doi.org/10.1038/nature01140
doi: 10.1038/nature01140
pubmed: 12397357
Schaschl H, Huber S, Schaefer K, Windhager S, Wallner B, Fieder M (2015) Signatures of positive selection in the cis -regulatory sequences of the human oxytocin receptor (OXTR) and arginine vasopressin receptor 1a (AVPR1A) genes. BMC Evol Biol 15:1–12. https://doi.org/10.1186/s12862-015-0372-7
doi: 10.1186/s12862-015-0372-7
Scheet P, Stephens M (2006) A fast and flexible statistical model for large-scale population genotype data: applications to inferring missing genotypes and haplotypic phase. Am J Hum Genet 78:629–644
doi: 10.1086/502802
Symmons O, Pan L, Remeseiro S, Aktas T, Klein F, Huber W, Spitz F (2016) The Shh topological domain facilitates the action of remote enhancers by reducing the effects of genomic distances. Dev Cell 39:529–543
doi: 10.1016/j.devcel.2016.10.015
Tickle C, Towers M (2017) Sonic Hedgehog signaling in limb development. Front Cell Dev Biol 5. https://doi.org/10.3389/fcell.2017.00014
Tyurina OV, Guner B, Popova E, Feng J, Schier AF, Kohtz JD, Karlstrom RO (2005) Zebrafish Gli3 functions as both an activator and a repressor in Hedgehog signaling. Dev Biol 277:537–556. https://doi.org/10.1016/j.ydbio.2004.10.003
doi: 10.1016/j.ydbio.2004.10.003
pubmed: 15617692
Veistinen L, Takatalo M, Kesper DA et al (2012) Deletion of Gli3 in mice causes abnormal frontal bone morphology and premature synostosis of the interfrontal suture. Front Physiol 3. https://doi.org/10.3389/fphys.2012.00121
Visel A, Minovitsky S, Dubchak I, Pennacchio LA (2007) VISTA Enhancer Browser—a database of tissue-specific human enhancers. Nucleic Acids Res 35:D88–D92. https://doi.org/10.1093/nar/gkl822
doi: 10.1093/nar/gkl822
pubmed: 17130149
Vortkamp A, Franz T, Gessler M, Grzeschik KH (1992) Deletion of GLI3 supports the homology of the human Greig cephalopolysyndactyly syndrome (GCPS) and the mouse mutant extra toes (Xt). Mamm Genome 3:461–463. https://doi.org/10.1007/bf00356157
doi: 10.1007/bf00356157
pubmed: 1322743
Ward LD, Kellis M (2016) HaploReg v4: systematic mining of putative causal variants, cell types, regulators and target genes for human complex traits and disease. Nucleic Acids Res 44:D877–D881. https://doi.org/10.1093/nar/gkv1340
doi: 10.1093/nar/gkv1340
pubmed: 26657631
pmcid: 26657631
Watson G, Ronai ZA, Lau E (2017) ATF2, a paradigm of the multifaceted regulation of transcription factors in biology and disease. Pharmacol Res 119:347–357. https://doi.org/10.1016/j.phrs.2017.02.004
doi: 10.1016/j.phrs.2017.02.004
pubmed: 28212892
pmcid: 5457671
Wong ES, Schmitt BM, Kazachenka A, Thybert D, Redmond A, Connor F, Rayner TF, Feig C, Ferguson-Smith AC, Marioni JC, Odom DT, Flicek P (2017) Interplay of cis and trans mechanisms driving transcription factor binding and gene expression evolution. Nat Commun 8:1–13. https://doi.org/10.1038/s41467-017-01037-x
doi: 10.1038/s41467-017-01037-x
Xu F-L, Yao J, Wu X, Xia X, Xing JX, Xuan JF, Liu YP, Wang BJ (2020) Association analysis between SNPs in the promoter region of RGS4 and schizophrenia in the Northern Chinese Han population. Neuropsychiatr Dis Treat 16:985–992. https://doi.org/10.2147/NDT.S250282
doi: 10.2147/NDT.S250282
pubmed: 32346293
pmcid: 7169994
Yang S-C, Liu J-J, Wang C-K, Lin YT, Tsai SY, Chen WJ, Huang WK, Tu PWA, Lin YC, Chang CF, Cheng CL, Lin H, Lai CY, Lin CY, Lee YH, Chiu YC, Hsu CC, Hsu SC, Hsiao M, Schuyler SC, Lu FL, Lu J (2019) Down-regulation of ATF1 leads to early neuroectoderm differentiation of human embryonic stem cells by increasing the expression level of SOX2. FASEB J Off Publ Fed Am Soc Exp Biol 33:10577–10592. https://doi.org/10.1096/fj.201800220RR
doi: 10.1096/fj.201800220RR
Zehra R, Abbasi AA (2018) Homo sapiens-specific binding site variants within brain exclusive enhancers are subject to accelerated divergence across human population. Genome Biol Evol 10:956–966. https://doi.org/10.1093/gbe/evy052
doi: 10.1093/gbe/evy052
pubmed: 29608725
pmcid: 5952923
Zhang D, Ma J, Brismar K, Efendic S, Gu HF (2009) A single nucleotide polymorphism alters the sequence of SP1 binding site in the adiponectin promoter region and is associated with diabetic nephropathy among type 1 diabetic patients in the Genetics of Kidneys in Diabetes Study. J Diabetes Complicat 23:265–272. https://doi.org/10.1016/j.jdiacomp.2008.05.004
doi: 10.1016/j.jdiacomp.2008.05.004