期刊论文详细信息
BMC Genomics
Abundance, arrangement, and function of sequence motifs in the chicken promoters
Neil J Gemmell1  Hideaki Abe2 
[1]Allan Wilson Centre for Molecular Ecology and Evolution, University of Otago, Dunedin, New Zealand
[2]Department of Anatomy, University of Otago, Dunedin, New Zealand
关键词: Cis-regulatory element;    Selection;    GC content;    Transcription;    Gene ontology;    G-quadruplex;    CpG island;    Short tandem repeat;    Transcription factor binding site;    Promoter;   
Others  :  1128456
DOI  :  10.1186/1471-2164-15-900
 received in 2014-04-04, accepted in 2014-10-08,  发布年份 2014
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【 摘 要 】

Background

Eukaryotic promoters are regions containing various sequence motifs necessary to control gene transcription. Much evidence has emerged showing that structural and/or contextual changes in regulatory elements can critically affect cis-regulatory activity. As sequence motifs can be key factors in maintaining complex promoter architectures, one effective approach to further understand the evolution of promoter regions in vertebrates is to compare the abundance and distribution patterns of sequence motifs in these regions between divergent species. When compared with mammals, the chicken (Gallus gallus) has a very different genome composition and sufficient genomic information to make it a good model for the exploration of promoter structure and evolution.

Results

More than 10% of chicken genes contained short tandem repeat (STR) in the region 2 kb upstream of promoters, but the total number of STRs observed in chicken is approximately half of that detected in human promoters. In terms of the STR motif frequencies, chicken promoter regions were more similar to other avian and mammalian promoters than these were to the entire chicken genome. Unlike other STRs, nearly half of the trinucleotide repeats found in promoters partly or entirely overlapped with CpG islands, indicating potential association with nucleosome positions. Moreover, the chicken promoters are abundant with sequence motifs such as poly-A, poly-G and G-quadruplexes, especially in the core region, that are otherwise rare in the genome. Most of sequence motifs showed strong functional enrichment for particular gene ontology (GO) categories, indicating roles in regulation of transcription and gene expression, as well as immune response and cognition.

Conclusions

Chicken promoter regions share some, but not all, of the structural features observed in mammalian promoters. The findings presented here provide empirical evidence suggesting that the frequencies and locations of STR motifs have been conserved through promoter evolution in a lineage-specific manner. Correlation analysis between GO categories and sequence motifs suggests motif-specific constraints acting on gene function.

【 授权许可】

   
2014 Abe and Gemmell; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Wray GA, Hahn MW, Abouheif E, Balhoff JP, Pizer M, Rockman MV, Romano LA: The evolution of transcriptional regulation in eukaryotes. Mol Biol Evol 2003, 20(9):1377-1419.
  • [2]Halees AS: PromoSer: a large-scale mammalian promoter and transcription start site identification service. Nucleic Acids Res 2003, 31(13):3554-3559.
  • [3]Wittkopp PJ, Kalay G: Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nat Rev Genet 2012, 13(1):59-69.
  • [4]Gemayel R, Vinces MD, Legendre M, Verstrepen KJ: Variable tandem repeats accelerate evolution of coding and regulatory sequences. Annu Rev Genet 2010, 44:445-477.
  • [5]Horton BM, Hudson WH, Ortlund EA, Shirk S, Thomas JW, Young ER, Zinzow-Kramer WM, Maney DL: Estrogen receptor alpha polymorphism in a species with alternative behavioral phenotypes. Proc Natl Acad Sci U S A 2014, 111(4):1443-1448.
  • [6]Andersson L: Genome-wide association analysis in domestic animals: a powerful approach for genetic dissection of trait loci. Genetica 2009, 136(2):341-349.
  • [7]Xu Y, He B, Li R, Pan Y, Gao T, Deng Q, Sun H, Song G, Wang S: Association of the polymorphisms in the Fas/FasL promoter regions with cancer susceptibility: a systematic review and meta-analysis of 52 studies. PLoS One 2014, 9(3):e90090.
  • [8]Vinces MD, Legendre M, Caldara M, Hagihara M, Verstrepen KJ: Unstable tandem repeats in promoters confer transcriptional evolvability. Science 2009, 324(5931):1213-1216.
  • [9]Bolton KA, Ross JP, Grice DM, Bowden NA, Holliday EG, Avery-Kiejda KA, Scott RJ: STaRRRT: a table of short tandem repeats in regulatory regions of the human genome. BMC Genomics 2013, 14(1):795. BioMed Central Full Text
  • [10]Valipour E, Kowsari A, Bayat H, Banan M, Kazeminasab S, Mohammadparast S, Ohadi M: Polymorphic core promoter GA-repeats alter gene expression of the early embryonic developmental genes. Gene 2013, 531(2):175-179.
  • [11]Morris EE, Amria MY, Kistner-Griffin E, Svenson JL, Kamen DL, Gilkeson GS, Nowling TK: A GA microsatellite in the Fli1 promoter modulates gene expression and is associated with systemic lupus erythematosus patients without nephritis. Arthritis Res Ther 2010, 12(6):R212. BioMed Central Full Text
  • [12]Luo W, Gangwal K, Sankar S, Boucher KM, Thomas D, Lessnick SL: GSTM4 is a microsatellite-containing EWS/FLI target involved in Ewing’s sarcoma oncogenesis and therapeutic resistance. Oncogene 2009, 28(46):4126-4132.
  • [13]Kovar H: Downstream EWS/FLI1 - upstream Ewing’s sarcoma. Genome Med 2010, 2:8. BioMed Central Full Text
  • [14]Guillon N, Tirode F, Boeva V, Zynovyev A, Barillot E, Delattre O: The oncogenic EWS-FLI1 protein binds in vivo GGAA microsatellite sequences with potential transcriptional activation function. PLoS One 2009, 4(3):e4932.
  • [15]Sawaya S, Bagshaw A, Buschiazzo E, Kumar P, Chowdhury S, Black MA, Gemmell N: Microsatellite tandem repeats are abundant in human promoters and are associated with regulatory elements. PLoS One 2013, 8(2):e54710.
  • [16]Lipps HJ, Rhodes D: G-quadruplex structures: in vivo evidence and function. Trends Cell Biol 2009, 19(8):414-422.
  • [17]Zhang C, Liu HH, Zheng KW, Hao YH, Tan Z: DNA G-quadruplex formation in response to remote downstream transcription activity: long-range sensing and signal transducing in DNA double helix. Nucleic Acids Res 2013, 41(14):7144-7152.
  • [18]Siddiqui-Jain A, Grand CL, Bearss DJ, Hurley LH: Direct evidence for a G-quadruplex in a promoter region and its targeting with a small molecule to repress c-MYC transcription. Proc Natl Acad Sci U S A 2002, 99(18):11593-11598.
  • [19]Ambrus A, Chen D, Dai J, Jones RA, Yang D: Solution structure of the biologically relevant G-quadruplex element in the human c-MYC promoter. Implications for G-quadruplex stabilization. Biochemistry 2005, 44(6):2048-2058.
  • [20]Akan P, Deloukas P: DNA sequence and structural properties as predictors of human and mouse promoters. Gene 2008, 410(1):165-176.
  • [21]Elango N, Yi SV: Functional relevance of CpG island length for regulation of gene expression. Genetics 2011, 187(4):1077-1083.
  • [22]Sharif J, Endo TA, Toyoda T, Koseki H: Divergence of CpG island promoters: a consequence or cause of evolution? Dev Growth Differ 2010, 52(6):545-554.
  • [23]Robertson KD: DNA methylation and chromatin - unraveling the tangled web. Oncogene 2002, 21(35):5361-5379.
  • [24]Li Q, Li N, Hu X, Li J, Du Z, Chen L, Yin G, Duan J, Zhang H, Zhao Y, Wang J, Li N: Genome-wide mapping of DNA methylation in chicken. PLoS One 2011, 6(5):e19428.
  • [25]Vavouri T, Lehner B: Human genes with CpG island promoters have a distinct transcription-associated chromatin organization. Genome Biol 2012, 13(11):R110. BioMed Central Full Text
  • [26]Furlong RF: Insights into vertebrate evolution from the chicken genome sequence. Genome Biol 2005, 6(2):207. BioMed Central Full Text
  • [27]Rao YS, Chai XW, Wang ZF, Nie QH, Zhang XQ: Impact of GC content on gene expression pattern in chicken. Genet Sel Evol 2013, 45:9. BioMed Central Full Text
  • [28]Warren WC, Hillier LW, Marshall Graves JA, Birney E, Ponting CP, Grutzner F, Belov K, Miller W, Clarke L, Chinwalla AT, Yang SP, Heger A, Locke DP, Miethke P, Waters PD, Veyrunes F, Fulton L, Fulton B, Graves T, Wallis J, Puente XS, Lopez-Otin C, Ordonez GR, Eichler EE, Chen L, Cheng Z, Deakin JE, Alsop A, Thompson K, Kirby P, et al.: Genome analysis of the platypus reveals unique signatures of evolution. Nature 2008, 453(7192):175-183.
  • [29]Du Z, Kong P, Gao Y, Li N: Enrichment of G4 DNA motif in transcriptional regulatory region of chicken genome. Biochem Biophys Res Commun 2007, 354(4):1067-1070.
  • [30]Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS: MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 2009, 37(Web Server issue):W202-W208.
  • [31]Portales-Casamar E, Thongjuea S, Kwon AT, Arenillas D, Zhao X, Valen E, Yusuf D, Lenhard B, Wasserman WW, Sandelin A: JASPAR 2010: the greatly expanded open-access database of transcription factor binding profiles. Nucleic Acids Res 2010, 38(Database issue):D105-D110.
  • [32]Newburger DE, Bulyk ML: UniPROBE: an online database of protein binding microarray data on protein-DNA interactions. Nucleic Acids Res 2009, 37(Database issue):D77-D82.
  • [33]Gupta S, Stamatoyannopoulos JA, Bailey TL, Noble WS: Quantifying similarity between motifs. Genome Biol 2007, 8(2):R24. BioMed Central Full Text
  • [34]Carninci P, Sandelin A, Lenhard B, Katayama S, Shimokawa K, Ponjavic J, Semple CA, Taylor MS, Engstrom PG, Frith MC, Forrest AR, Alkema WB, Tan SL, Plessy C, Kodzius R, Ravasi T, Kasukawa T, Fukuda S, Kanamori-Katayama M, Kitazume Y, Kawaji H, Kai C, Nakamura M, Konno H, Nakano K, Mottagui-Tabar S, Arner P, Chesi A, Gustincich S, Persichetti F, et al.: Genome-wide analysis of mammalian promoter architecture and evolution. Nat Genet 2006, 38(6):626-635.
  • [35]da Huang W, Sherman BT, Lempicki RA: Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 2009, 37(1):1-13.
  • [36]Lawson MJ, Zhang L: Housekeeping and tissue-specific genes differ in simple sequence repeats in the 5′-UTR region. Gene 2008, 407(1–2):54-62.
  • [37]Sawaya SM, Bagshaw AT, Buschiazzo E, Gemmell NJ: Promoter microsatellites as modulators of human gene expression. In Tandem Repeat Polymorphisms: Genetic Plasticity, Neural Diversity and Disease. Edited by Hannan AJ. Austin/New York: Landes Bioscience and Springer Science + Business Media; 2012:41-54.
  • [38]Rich A, Nordheim A, Wang AH: The chemistry and biology of left-handed Z-DNA. Annu Rev Plant Physiol Plant Mol Biol 1984, 53:791-846.
  • [39]Bayele HK, Peyssonnaux C, Giatromanolaki A, Arrais-Silva WW, Mohamed HS, Collins H, Giorgio S, Koukourakis M, Johnson RS, Blackwell JM, Nizet V, Srai SK: HIF-1 regulates heritable variation and allele expression phenotypes of the macrophage immune response gene SLC11A1 from a Z-DNA forming microsatellite. Blood 2007, 110(8):3039-3048.
  • [40]Bacolla A, Larson JE, Collins JR, Li J, Milosavljevic A, Stenson PD, Cooper DN, Wells RD: Abundance and length of simple repeats in vertebrate genomes are determined by their structural properties. Genome Res 2008, 18(10):1545-1553.
  • [41]Martin P, Makepeace K, Hill SA, Hood DW, Moxon ER: Microsatellite instability regulates transcription factor binding and gene expression. Proc Natl Acad Sci U S A 2005, 102(10):3800-3804.
  • [42]Zhou W, Chen Z, Hu W, Shen M, Zhang X, Li C, Wen Z, Wu X, Hu Y, Zhang X, Duan X, Han X, Tao Z: Association of short tandem repeat polymorphism in the promoter of prostate cancer antigen 3 gene with the risk of prostate cancer. PLoS One 2011, 6(5):e20378.
  • [43]Primmer CR, Raudsepp T, Chowdhary BP, Moller AP, Ellegren H: Low frequency of microsatellites in the avian genome. Genome Res 1997, 7(5):471-482.
  • [44]Mayer C, Leese F, Tollrian R: Genome-wide analysis of tandem repeats in daphnia pulex–a comparative approach. BMC Genomics 2010, 11:277. BioMed Central Full Text
  • [45]Kruglyak S, Durrett RT, Schug MD, Aquadro CF: Equilibrium distributions of microsatellite repeat length resulting from a balance between slippage events and point mutations. Proc Natl Acad Sci U S A 1998, 95(18):10774-10778.
  • [46]McQueen HA, Fantes J, Cross SH, Clark VH, Archibald AL, Bird AP: CpG islands of chicken are concentrated on microchromosomes. Nat Genet 1996, 12(3):321-324.
  • [47]Hughes AL, Hughes MK: Small genomes for better flyers. Nature 1995, 377(6548):391.
  • [48]Vardhanabhuti S, Wang J, Hannenhalli S: Position and distance specificity are important determinants of cis-regulatory motifs in addition to evolutionary conservation. Nucleic Acids Res 2007, 35(10):3203-3213.
  • [49]Moses AM, Chiang DY, Kellis M, Lander ES, Eisen MB: Position specific variation in the rate of evolution in transcription factor binding sites. BMC Evol Biol 2003, 3:19. BioMed Central Full Text
  • [50]Brandström M, Ellegren H: Genome-wide analysis of microsatellite polymorphism in chicken circumventing the ascertainment bias. Genome Res 2008, 18(6):881-887.
  • [51]Beilina A, Tassone F, Schwartz PH, Sahota P, Hagerman PJ: Redistribution of transcription start sites within the FMR1 promoter region with expansion of the downstream CGG-repeat element. Hum Mol Genet 2004, 13(5):543-549.
  • [52]Tomita N, Fujita R, Kurihara D, Shindo H, Wells RD, Shimizu M: Effects of triplet repeat sequences on nucleosome positioning and gene expression in yeast minichromosomes. Nucleic Acids Res Suppl 2002, 2:231-232.
  • [53]Bansal M, Kumar A, Yella VR: Role of DNA sequence based structural features of promoters in transcription initiation and gene expression. Curr Opin Struct Biol 2014, 25C:77-85.
  • [54]Brukner I, Sanchez R, Suck D, Pongor S: Sequence-dependent bending propensity of DNA as revealed by DNase I: parameters for trinucleotides. EMBO J 1995, 14(8):1812-1818.
  • [55]Anderson JD, Widom J: Poly(dA-dT) promoter elements increase the equilibrium accessibility of nucleosomal DNA target sites. Mol Cell Biol 2001, 21(11):3830-3839.
  • [56]Shimizu M, Mori T, Sakurai T, Shindo H: Destabilization of nucleosomes by an unusual DNA conformation adopted by poly(dA) small middle dotpoly(dT) tracts in vivo. EMBO J 2000, 19(13):3358-3365.
  • [57]Finkenzeller G, Sparacio A, Technau A, Marme D, Siemeister G: Sp1 recognition sites in the proximal promoter of the human vascular endothelial growth factor gene are essential for platelet-derived growth factor-induced gene expression. Oncogene 1997, 15(6):669-676.
  • [58]Cooper SJ, Trinklein ND, Anton ED, Nguyen L, Myers RM: Comprehensive analysis of transcriptional promoter structure and function in 1% of the human genome. Genome Res 2006, 16(1):1-10.
  • [59]Deaton AM, Bird A: CpG islands and the regulation of transcription. Genes Dev 2011, 25(10):1010-1022.
  • [60]Chan ET, Quon GT, Chua G, Babak T, Trochesset M, Zirngibl RA, Aubin J, Ratcliffe MJ, Wilde A, Brudno M, Morris QD, Hughes TR: Conservation of core gene expression in vertebrate tissues. J Biol 2009, 8(3):33. BioMed Central Full Text
  • [61]Kumar P, Yadav VK, Baral A, Kumar P, Saha D, Chowdhury S: Zinc-finger transcription factors are associated with guanine quadruplex motifs in human, chimpanzee, mouse and rat promoters genome-wide. Nucleic Acids Res 2011, 39(18):8005-8016.
  • [62]Chen Y, Cunningham F, Rios D, McLaren WM, Smith J, Pritchard B, Spudich GM, Brent S, Kulesha E, Marin-Garcia P, Smedley D, Birney E, Flicek P: Ensembl variation resources. BMC Genomics 2010, 11:293. BioMed Central Full Text
  • [63]The UCSC genome browser http://genome.ucsc.edu webcite
  • [64]International Chicken Genome Sequencing Consortium (ICGSC): Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 2004, 432(7018):695-716.
  • [65]Medvedeva YA, Fridman MV, Oparina NJ, Malko DB, Ermakova EO, Kulakovskiy IV, Heinzel A, Makeev VJ: Intergenic, gene terminal, and intragenic CpG islands in the human genome. BMC Genomics 2010, 11:48. BioMed Central Full Text
  • [66]The European bioinformatics institute http://www.ebi.ac.uk webcite
  • [67]Gardiner-Garden M, Frommer M: CpG islands in vertebrate genomes. J Mol Biol 1987, 196(2):261-282.
  • [68]Martins WS, Lucas DCS, Neves KFS, Bertioli DJ: WebSat–a web software for microsatellite marker development. Bioinformation 2009, 3(6):282-283.
  • [69]Phobos 3.3.11 http://www.ruhr-uni-bochum.de/spezzoo/cm/cm_phobos.htm webcite
  • [70]Kraemer L, Beszteri B, Gabler-Schwarz S, Held C, Leese F, Mayer C, Pohlmann K, Frickenhaus S: STAMP: Extensions to the STADEN sequence analysis package for high throughput interactive microsatellite marker design. BMC Bioinformatics 2009, 10:41. BioMed Central Full Text
  • [71]Kikin O, D’Antonio L, Bagga PS: QGRS Mapper: a web-based server for predicting G-quadruplexes in nucleotide sequences. Nucleic Acids Res 2006, 34(Web Server issue):W676-W682.
  • [72]da Huang W, Sherman BT, Lempicki RA: Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4(1):44-57.
  • [73]Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G: Gene ontology: tool for the unification of biology. The gene ontology consortium. Nat Genet 2000, 25(1):25-29.
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