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Prediction and verification of the influence of the rs367781716 SNP on the interaction of the ТАТА-binding protein with the promoter of the human АВСА9 gene

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Russian Journal of Genetics: Applied Research

Abstract

The high-throughput sequencing project 1000 Genomes made it possible to catalog and utilize genetic loci and single nucleotide polymorphisms (SNPs) in medicine. The analysis of SNP markers allows physicians to optimize treatment. However, tens of millions of unannotated SNPs correspond to a gigantic number of false positive (false negative) candidate SNP markers that are selected by computer methods for comparing their frequency in patients with that in healthy people. This approach contributes to the undervaluation of clinically relevant SNPs and to unnecessary computational expenses for the verification of neutral SNPs. The preclinical empirical verification of possible candidate SNP markers may eliminate neutral SNPs from the dataset. In the present study, using the SNP_TATA_Comparator web service, we found the unannotated SNP rs367781716: the substitution of ancestral T (health) with a minor C at position–37 before the transcription initiation site of the ABCA9 gene. This SNP significantly reduces the affinity of TATA-binding protein (TBP) for this gene’s promoter and corresponds to the deficiency (low protein level) of the ABCA9 gene product (the transporter ATP-binding cassette A9) in patients with the–37C allele. For preclinical empirical verification of rs367781716, we used an electrophoretic mobility shift assay (EMSA) to measure the rates of association (k a) and dissociation (k d) of the complexes of TBP with an oligonucleotide matching either allele–37C or–37T of the ABCA9 gene. We found that the rate of association (k a) of the TBP/TATA complex for the minor allele is lower by a factor of 2.4 than that for the ancestral allele. We calculated the empirical value of the change in the equilibrium constant of dissociation (K D = k d/k a), which characterizes the binding affinity of TBP for a promoter containing the TATA box. This empirical value matched the value predicted by the SNP_TATA_Comparator within the allowable margin of error of the measurements and calculations. We also determined the half-life and Gibbs free energy of the complex of TBP with the ABCA9 promoter. Possible phenotypic manifestations of the candidate SNP marker rs367781716 are discussed.

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References

  • Arkova, O.V., Kuznetsov, N.A., Fedorova, O.S., Kolchanov, N.A., and Savinkova, L.K., Interaction of TBP with the TATA box of human triose phosphate isomerase gene promoter in health and pathology, as defined in real time, Acta Naturae, 2014, vol. 6, no. 2, pp. 40–44.

    Google Scholar 

  • Baecklund, F., Foo, J.N., Bracci, P., Darabi, H., Karlsson, R., Hjalgrim, H., Rosenquist, R., Adami, H.-O., Glimelius, B., Melbye, M., Conde, L., Liu, J., Humphreys, K., Skibola, C.F., and Smedby, K.E., A comprehensive evaluation of the role of genetic variation in follicular lymphoma survival, BMC Med. Genet., 2014, vol. 15, no. 113. doi 10.1186/s12881-014-0113-6

    Google Scholar 

  • Calpe-Berdiel, L., Zhao, Y., de Graauw, M., Ye, D., van Santbrink, P.J., Mommaas, A.M., Foks, A., Bot, M., Meurs, I., Kuiper, J., Mack, J.T., Van Eck, M., Tew, K.D., and van Berkel, T.J., Macrophage ABCA2 deletion modulates intracellular cholesterol deposition, affects macrophage apoptosis, and decreases early atherosclerosis in LDL receptor knockout mice, Atherosclerosis, 2012, vol. 223, no. 2, pp. 332–341. doi 10.1016/j.atherosclerosis.2012.05.039

    Article  CAS  PubMed  Google Scholar 

  • Colonna, V., Ayub, Q., Chen, Y., Pagani, L., Luisi, P., Pybus, M., Garrison, E., Xue, Y., Tyler-Smith, C., Abecasis, G.R., Auton, A., Brooks, L.D., Depristo, M.A., Durbin, R.M., et al., Human genomic regions with exceptionally high levels of population differentiation identified from 911 wholegenome sequences, Genome Biol., 2014, vol. 15, no. 6, doi 10.1186/gb-2014-15-6-r88

    Google Scholar 

  • Dean, M., Hamon, Y., and Chimini, G., The human ATPbinding cassette (ABC) transporter superfamily, J. Lipid Res., 2001, vol. 42, no. 7, pp. 1007–1017.

    CAS  PubMed  Google Scholar 

  • Dean, M. and Allikmets, R., Complete characterization of the human ABC gene family, J. Bioenerg. Biomembr., 2001, vol. 33, no. 6, pp. 475–479. doi 10.1023/A:1012823120935

    Article  CAS  PubMed  Google Scholar 

  • Drachkova, I.A., Arshinova, T.V., Ponomarenko, P.M., Merkulova, T.I., Kolchanov, N.A., and Savinkova, L.K., Effect of TATA Box polymorphisms in human ß-globin gene promoter aßsociated with ß-thalassemia on interaction with TATA-binding protein, Russ. J. Genet., Appl. Res., 2011, vol. 1, no. 3, pp. 183–188.

    Article  Google Scholar 

  • Drachkova, I.A., Shekhovtsov, S.V., Pel’tek, S.E., Ponomarenko, P.M., Arshinova, T.V., Ponomarenko, M.P., Merkulova, T.I., Savinkova, L.K., and Kolchanov, N.A., Study of the interaction of the human TATA binding protein with the TATA element of the NOS2A gene promoter using surface plasmon resonance, Vavilovskii Zh. Genet. Sel., 2012, vol. 16, no. 2, pp. 391–396.

    Google Scholar 

  • Drachkova, I., Savinkova, L., Arshinova, T., Ponomarenko, M., Peltek, S., and Kolchanov, N., The mechanism by which TATA-box polymorphisms associated with human hereditary diseases influence interactions with the TATAbinding protein, Hum. Mutat., 2014, vol. 35, no. 5, pp. 601–608. doi 10.1002/humu.22535

    Article  CAS  PubMed  Google Scholar 

  • Dreos, R., Ambrosini, G., Perier, R.C., and Bucher, P., The eukaryotic promoter database: Expansion of EPDnew and new promoter analysis tools, Nucleic Acids Res., 2015, vol. 43, pp. D92–D96. doi 10.1093/nar/gku1111

    Article  PubMed  Google Scholar 

  • Dreszer, T.R., Karolchik, D., Zweig, A.S., Hinrichs, A.S., Raney, B.J., Kuhn, R.M., Meyer, L.R., Wong, M., Sloan, C.A., Rosenbloom, K.R., Roe, G., Rhead, B., Pohl, A., Malladi, V.S., Li, C.H., et al., The UCSC genome browser database: Extensions and updates 2011, Nucleic Acids Res., 2012, no. 40, pp. D918–D923. doi 10.1093/nar/gkr1055

    Article  CAS  PubMed  Google Scholar 

  • Harrow, J., Frankish, A., Gonzalez, J.M., Tapanari, E., Diekhans, M., Kokocinski, F., Aken, B.L., Barrell, D., Zadissa, A., Searle, S., Barnes, I., Bignell, A., Boychenko, V., Hunt, T., Kay, M., et al., GENCODE: The reference human genome annotation for the ENCODE project, Genome Res, 2012, vol. 22, no. 9, pp. 1760–1774. doi 10.1101/gr.135350.111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hedditch, E.L., Gao, B., Russell, A.J., Lu, Y., Emmanuel, C., Beesley, J., Johnatty, S.E., Chen, X., Harnett, P., George, J., Australian Ovarian Cancer Study Group, Williams, R.T., Flemming, C., Lambrechts, D., Despierre E., et al., ABCA transporter gene expression and poor outcome in epithelial ovarian cancer, J. Natl. Cancer Inst., 2014, vol. 106, no. 7. doi 10.1093/jnci/dju149

    Google Scholar 

  • Hendig, D., Langmann, T., Kocken, S., Zarbock, R., Szliska, C., Schmitz, G., and Kleesiek, K., Götting, C., Gene expression profiling of ABC transporters in dermal fibroblasts of pseudoxanthoma elasticum patients identifies new candidates involved in PXE pathogenesis, Lab. Invest., 2008, vol. 88, no. 12, pp. 1303–1315. doi 10.1038/labinvest.2008.96

    Article  CAS  PubMed  Google Scholar 

  • International HapMap 3 Consortium, Altshuler, D.M., Gibbs, R.A., Peltonen, L., Dermitzakis, E., Schaffner, S.F., Yu, F., Peltonen, L., Dermitzakis, E., Bonnen, P.E., Altshuler, D.M., Gibbs, R.A., de Bakker, P.I., Deloukas, P., et al., Integrating common and rare genetic variation in diverse human populations, Nature, 2010, vol. 467, no. 7311, pp. 52–58. doi doi 10.1038/nature09298

    Article  Google Scholar 

  • Kaniwa, N., Kurose, K., Jinno, H., Tanaka-Kagawa, T., Saito, Y., Saeki, M., Sawada, J., Tohkin, M., and Hasegawa, R., Racial variability in haplotype frequencies of UGT1A1 and glucuronidation activity of a novel single nucleotide polymorphism 686C>T (P229L) found in an African-American, Drug Metab. Dispos., 2005, vol. 33, no. 3, pp. 458–465.

    Article  CAS  PubMed  Google Scholar 

  • Liu, C. and Xuan, Z., Prioritization of cancer-related genomic variants by SNP association network, Cancer Inf., 2015, vol. 14, no. 2, pp. 57–70. doi 10.4137/CIN.S17288

    Google Scholar 

  • Mallal, S., Nolan, D., Witt, C., Masel, G., Martin, A.M., Moore, C., Sayer, D., Castley, A., Mamotte, C., Maxwell, D., James, I., and Christiansen, F.T., Association between presence of HLA-B*5701, HLA-DR7, and HLA-DQ3 and hypersensitivity to HIV-1 reverse-transcriptase inhibitor abacavir, Lancet, 2002, vol. 359, no. 9308, pp. 727–732. doi 10.1016/S0140-6736(02)07873-X

    Article  CAS  PubMed  Google Scholar 

  • Mironova, V.V., Omelyanchuk, N.A., Ponomarenko, P.M., Ponomarenko, M.P., and Kolchanov, N.A., Specific/nonspecific binding of TBP to promoter DNA of the auxin response factor genes in plants correlated with ARFs function on gene transcription (activator/repressor), Dokl. Biochem. Biophys., 2010, vol. 433, no. 1, pp. 191–196.

    Article  CAS  PubMed  Google Scholar 

  • Mogno, I., Vallania, F., Mitra, R.D., and Cohen, B., TATA is a modular component of synthetic promoters, Genome Res., 2010, vol. 20, no. 10, pp. 1391–1397. doi 10.1101/gr.106732.110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oram, J. and Vaughan, A., ATP-binding cassette cholesterol transporters and cardiovascular disease, Circ. Res., 2006, vol. 99, no. 10, pp. 1031–1043. doi 0.1161/01.res. 0000250171.54048.5c

    Article  CAS  PubMed  Google Scholar 

  • Piehler, A., Kaminski, W.E., Wenzel, J., Langmann, T., and Schmitzg, G., Molecular structure of a novel cholesterol-responsive A subclass ABC transporter, ABCA9, Biochem. Biophys. Res. Commun., 2002, vol. 295, no. 2, pp. 408–416. doi doi 10.1016/S0006-291X(02)00659-9

    Article  CAS  PubMed  Google Scholar 

  • Ponomarenko, P.M., Savinkova, L.K., Drachkova, I.A., Lysova, M.V., Arshinova, T.V., Ponomarenko, M.P., and Kolchanov, N.A., A step-by-step model of TBP/TATA box binding allows predicting human hereditary diseases by single nucleotide polymorphism, Dokl. Biochem. Biophys., 2008, vol. 419, no. 1, pp. 88–92.

    Article  CAS  PubMed  Google Scholar 

  • Ponomarenko, P.M., Ponomarenko, M.P., Drachkova, I.A., Lysova, M.V., Arshinova, T.V., Savinkova, L.K., and Kolchanov, N.A., Prediction of the affinity of the TATA-binding protein to TATA boxes with single nucleotide polymorphisms, Mol. Biol. (Moscow), 2009, vol. 43, no. 3, pp. 472–479.

    Article  CAS  Google Scholar 

  • Ponomarenko, P.M., Suslov, V.V., Savinkova, L.K., Ponomarenko, M.P., and Kolchanov, N.A., A precise equation of equilibrium of four steps of TBP binding with the TATA box for prognosis of phenotypic manifestation of mutations, Biophysics, 2010, vol. 55, no. 3, pp. 358–369.

    Article  Google Scholar 

  • Ponomarenko, M., Mironova, V., Gunbin, K., and Savinkova, L., Hogness Box, in Brenner’s Encyclopedia of Genetics, Maloy, S. and Hughes, K., Eds., San Diego: Acad. Press, Elsevier Inc, 2013a, vol. 3, pp. 491–494. doi 10.1016/B978-0-12-374984-0.00720-8

    Article  Google Scholar 

  • Ponomarenko, M., Savinkova, L., and Kolchanov, N., Initiation Factors, in Brenner’s Encyclopedia of Genetics, Maloy, S. and Hughes, K., Eds., San Diego: Acad. Press, Elsevier Inc, 2013b, vol. 4, pp. 83–85. doi 10.1016/B978-0-12-374984-0.00798-1

    Article  Google Scholar 

  • Ponomarenko, M.P., Suslov, V.V., Gunbin, K.V., Ponomarenko, P.M., Vishnevskii, O.V., and Kolchanov, N.A., Identification of the relationship between the variability of the expression of signaling pathway genes in the human brain and the affinity of TATA-binding protein to their promoters, Russ. J. Genet., Appl. Res., 2015, vol. 5, no. 6, pp. 626–634.

    Article  CAS  Google Scholar 

  • Ponomarenko, P.M. and Ponomarenko, M.P., Sequencebased prediction of transcription upregulation by auxin in plants, J. Bioinform. Comput. Biol., 2015, vol. 13, no. 1. doi 10.1142/S0219720015400090

    Google Scholar 

  • Pugh, B.F., Control of gene expression through regulation of the TATA-binding protein, Gene, 2000, vol. 255, no. 1, pp. 1–14. doi 10.1016/S0378-1119(00)00288-2

    Article  CAS  PubMed  Google Scholar 

  • Rasskazov, D.A., Gunbin, K.V., Ponomarenko, P.M., Vishnevskii, O.V., Ponomarenko, M.P., and Afonnikov, D.A., SNP_TATA_Comparator: Web-service for comparing SNPs within the gene promoters associated with human diseases, using the equation of equilibrium binding of the TBP/TATA complex, Vavilovskii Zh. Genet. Sel., 2013, vol. 17, no. 4/1, pp. 599–606.

    Google Scholar 

  • Savinkova, L.K., Drachkova, I.A., Arshinova, T.V., Ponomarenko, P.M., Ponomarenko, M.P., and Kolchanov, N.A., An experimental verification of the predicted effects of promoter TATA-box polymorphisms associated with human diseases on interactions between the TATA boxes and TATA-binding protein, PLoS One, 2013, vol. 8, no. 2. doi 10.1371/journal.pone.0054626

    Google Scholar 

  • Stewart, J.J. and Stargell, L.A., The stability of the TFIIATBP-DNA complex is dependent on the sequence of the TATAAA element, J. Biol. Chem., 2001, vol. 276, no. 32, pp. 30078–30084. doi 10.1074/jbc.M105276200

    Article  CAS  PubMed  Google Scholar 

  • Suslov, V.V., Ponomarenko, P.M., Ponomarenko, M.P., Drachkova, I.A., Arshinova, T.V., Savinkova, L.K., and Kolchanov, N.A., TATA box polymorphisms in genes of commercial and laboratory animals and plants associated with selectively valuable traits, Russ. J. Genet., 2010, vol. 46, no. 4, pp. 448–457.

    Article  CAS  Google Scholar 

  • Suslov, V.V., Ponomarenko, P.M., Efimov, V.M., Savinkova, L.K., Ponomarenko, M.P., and Kolchanov, N.A., SNPs in the HIV-1 TATA box and the AIDS pandemic, J. Bioinf. Comput. Biol., 2010, vol. 8, no. 3, pp. 607–625. doi 10.1142/S0219720010004677

    Article  CAS  Google Scholar 

  • Trovato, G.M., Sustainable medical research by effective and comprehensive medical skills: Overcoming the frontiers by predictive, preventive and personalized medicine, EPMA J., 2014, vol. 5, no. 1, p. 14. doi 10.1186/1878-5085-5-14

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang, X., Collins, H.L., Ranalletta, M., Fuki, I.V., Billheimer, J.T., Rothblat, G.H., Tall, A.R., and Rader, D.J., Macrophage ABCA1 and ABCG1, but not SR-BI, promote macrophage reverse cholesterol transport in vivo, J. Clin. Invest., 2007, vol. 117, no. 8, pp. 2216–2224.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Welter, D., MacArthur, J., Morales, J., Burdett, T., Hall, P., Junkins, H., Klemm, A., Flicek, P., Manolio, T., Hindorff, L., and Parkinson, H., The NH-GRI-GWAS Catalog, a curated resource of SNP-trait associations, Nucleic Acids Res., 2014, vol. 42, pp. D1001–1006. doi 10.1093/nar/gkt1229

    Article  CAS  PubMed  Google Scholar 

  • Ye, D., Hoekstra, M., Out, R., Meurs, I., Kruijt, J.K., Hildebrand, R.B., Van Berkel, T.J.C., and Van Eck, M., Hepatic cell-specific ATP-binding cassette (ABC) transporter profiling identifies putative novel candidates for lipid homeostasis in mice, Atherosclerosis, 2008, vol. 196, no. 2, pp. 650–658.

    Article  CAS  PubMed  Google Scholar 

  • Yoo, S.S., Jin, C., Jung, D., Choi, Y., Choi, J.E., Lee, W.K., Lee, S.Y., Lee, J., Cha, S.I., Kim, C.H., Seok, Y., Lee, E., and Park, J.Y., Putative functional variants of XRCC1 identified by RegulomeDB were not associated with lung cancer risk in a Korean population, Cancer Genet., 2015, vol. 208, nos. 1/2, pp. 19–24. doi 10.1016/j.cancergen.2014.11.004

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Institute of Cytology and Genetics, Siberian Branch, Russian Academy of Sciences, Novosibirsk, Russia

    O. V. Arkova, I. A. Drachkova, T. V. Arshinova, D. A. Rasskazov, V. V. Suslov, M. P. Ponomarenko, N. A. Kolchanov & L. K. Savinkova

  2. Children’s Hospital Los Angeles, University of Southern California, Los Angeles, CA, 90027, United States

    P. M. Ponomarenko

  3. Novosibirsk State University, Novosibirsk, Russia

    M. P. Ponomarenko & N. A. Kolchanov

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  1. O. V. Arkova
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  2. I. A. Drachkova
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  3. T. V. Arshinova
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  4. D. A. Rasskazov
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  5. V. V. Suslov
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  6. P. M. Ponomarenko
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  7. M. P. Ponomarenko
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  8. N. A. Kolchanov
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  9. L. K. Savinkova
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Correspondence to L. K. Savinkova.

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Original Russian Text © O.V. Arkova, I.A. Drachkova, T.V. Arshinova, D.A. Rasskazov, V.V. Suslov, P.M. Ponomarenko, M.P. Ponomarenko, N.A. Kolchanov, L.K. Savinkova, 2015, published in Vavilovskii Zhurnal Genetiki i Selektsii, 2015, Vol. 19, No. 6, pp. 675–681.

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Arkova, O.V., Drachkova, I.A., Arshinova, T.V. et al. Prediction and verification of the influence of the rs367781716 SNP on the interaction of the ТАТА-binding protein with the promoter of the human АВСА9 gene. Russ J Genet Appl Res 6, 785–791 (2016). https://doi.org/10.1134/S2079059716070029

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