Human skin color is influenced by an intergenic DNA polymorphism regulating transcription of the nearby BNC2 pigmentation gene

Human Molecular Genetics

Volumn 23, Issue 21, 2014, Pages 5750-5762

  Visser, Mijke ^a   Palstra, Robert Jan ^a   Kayser, Manfred ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ALLELE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHROMATIN STRUCTURE; CONTROLLED STUDY; ENHANCER REGION; GENE; GENE EXPRESSION; GENE LINKAGE DISEQUILIBRIUM; GENETIC ASSOCIATION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; MELANOCYTE; PROMOTER REGION; SINGLE NUCLEOTIDE POLYMORPHISM; SKIN COLOR; SKIN PIGMENTATION; TRANSCRIPTION REGULATION; CELL LINE; EPIDERMIS; FEMALE; GENE EXPRESSION REGULATION; GENE LOCUS; GENETIC POLYMORPHISM; GENETIC TRANSCRIPTION; GENETICS; MALE; METABOLISM;

BNC2 PROTEIN, HUMAN; DNA BINDING PROTEIN; SPACER DNA;

ALLELES; CELL LINE; DNA, INTERGENIC; DNA-BINDING PROTEINS; ENHANCER ELEMENTS, GENETIC; EPIDERMIS; FEMALE; GENE EXPRESSION REGULATION; GENETIC LOCI; HUMANS; MALE; MELANOCYTES; POLYMORPHISM, GENETIC; POLYMORPHISM, SINGLE NUCLEOTIDE; PROMOTER REGIONS, GENETIC; SKIN PIGMENTATION; TRANSCRIPTION, GENETIC;

EID: 84911453998     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu289     Document Type: Article

References (62)

1. Sturm, R.A. (2009) Molecular genetics of human pigmentation diversity. Hum. Mol. Genet., 18, R9-R17.
2. Barsh, G.S. (2003)What controls variation in humanskin color?.PLoS Biol., 1, 19-22.
3. Han, J.L., Kraft, P., Nan, H., Guo, Q., Chen, C., Qureshi, A., Hankinson, S.E., Hu, F.B., Duffy, D.L., Zhao, Z.Z. et al. (2008) A genome-wide association selection in pigmentation candidate genes in populations of East Asian ancestry. BMC Evol. Biol., 13, 150.
4. Sturm, R.A. and Duffy, D.L. (2012) Human pigmentation genes under environmental selection. Genome Biol., 13, 248.
5. Jacobs, L.C., Wollstein, A., Lao, O., Hofman, A., Klaver, C.C., Uitterlinden, A.G., Nijsten, T., Kayser, M. and Liu, F. (2013) Comprehensive candidate gene study highlights UGT1A and BNC2 as new genes determining continuous skin color variation in Europeans. Hum. Genet., 132, 147-158.
6. Eriksson, N., Macpherson, J.M., Tung, J.Y., Hon, L.S., Naughton, B., Saxonov, S., Avey, L., Wojcicki, A., Pe'er, I. and Mountain, J. (2010) Web-based, participant-driven studies yield novel genetic associations for common traits. PLoS Genet., 6, e1000993.
7. Jablonski, N.G. and Chaplin, G. (2000) The evolution of human skin coloration. J. Hum. Evol., 39, 57-106.
8. Relethford, J.H. (1997) Hemispheric difference in human skin color. Am. J. Phys. Anthropol., 104, 449-457.
9. Lao, O., de Gruijter, J.M., van Duijn, K., Navarro, A. and Kayser, M. (2007) Signatures of positive selection in genes associated with human skin pigmentation as revealed from analyses of single nucleotide polymorphisms. Ann. Hum. Genet., 71, 354-369.
10. Parra, E.J. (2007) Human pigmentation variation: evolution, genetic basis, and implications for public health. Am. J. Phys. Anthropol., 134, 85-105.
11. Wilde, S., Timpson, A., Kirsanow, K., Kaiser, E., Kayser, M., Unterlander, M., Hollfelder, N., Potekhina, I.D., Schier, W., Thomas, M.G. et al. (2014) Direct evidence for positive selection of skin, hair, and eye pigmentation in Europeans during the last 5,000 y. Proc. Natl. Acad. Sci. USA, 111, 4832-4837.
12. Sankararaman, S., Mallick, S., Dannemann, M., Prufer, K., Kelso, J., Paabo, S., Patterson, N. and Reich, D. (2014)Thegenomiclandscape of Neanderthal ancestry in present-day humans. Nature, 507, 354-357.
13. Vernot, B. and Akey, J.M. (2014) Resurrecting surviving Neandertal lineages from modern human genomes. Science, 343, 1017-1021.
14. Romano, R.A., Li, H.X., Tummala, R., Maul, R. and Sinha, S. (2004) Identification of Basonuclin2, a DNA-binding zinc-finger protein expressed in germ tissues and skin keratinocytes. Genomics, 83, 821-833.
15. Vanhoutteghem, A. and Djian, P. (2004) Basonuclin 2: an extremely conserved homolog of the zinc finger protein basonuclin. Proc. Natl. Acad. Sci. USA, 101, 3468-3473.
16. Herve, F., Vanhoutteghem, A. and Djian, P. (2012) [Basonuclins and DISCO proteins: regulators of development in vertebrates and insects] Basonuclines et proteines DISCO: des regulateurs du developpement des vertebres et des insectes. Med. Sci. (Paris), 28, 55-61.
17. Vanhoutteghem, A. and Djian, P. (2007) The human basonuclin 2 gene has the potential to generate nearly 90,000mRNAisoforms encoding over 2000 different proteins. Genomics, 89, 44-58.
18. Vanhoutteghem, A. and Djian, P. (2006) Basonuclins 1 and 2, whose genes share a common origin, are proteins with widely different properties and functions. Proc. Natl. Acad. Sci. USA, 103, 12423-12428.
19. Smyth, I.M., Wilming, L., Lee, A.W., Taylor, M.S., Gautier, P., Barlow, K., Wallis, J., Martin, S., Glithero, R., Phillimore, B. et al. (2006) Genomic anatomy of the Tyrp1 (brown) deletion complex. Proc. Natl. Acad. Sci.USA, 103, 3704-3709.
20. Vanhoutteghem, A., Maciejewski-Duval, A., Bouche, C., Delhomme, B., Herve, F., Daubigney, F., Soubigou, G., Araki, M., Araki, K., Yamamura, K. et al. (2009) Basonuclin 2 has a function in the multiplication of embryonic craniofacial mesenchymal cells and is orthologous to disco proteins. Proc. Natl. Acad. Sci. USA, 106, 14432-14437.
21. Lang, M.R., Patterson, L.B., Gordon, T.N., Johnson, S.L. and Parichy, D.M. (2009) Basonuclin-2 requirements for zebrafish adult pigment pattern development and female fertility. PLoS Genet., 5, e1000744.
22. Patterson, L.B. and Parichy, D.M. (2013) Interactions with iridophores and the tissue environment required for patterning melanophores and xanthophores during zebrafish adult pigment stripe formation. PLoS Genet., 9, e1003561.
23. Visser, M., Kayser, M. and Palstra, R.J. (2012) HERC2 rs12913832 modulates human pigmentation by attenuating chromatin-loop formation between a long-range enhancer and the OCA2 promoter. Genome Res., 22, 446-455.
24. Praetorius, C., Grill, C., Stacey, S.N., Metcalf, A.M., Gorkin, D.U., Robinson, K.C., Van Otterloo, E., Kim, R.S.Q., Bergsteinsdottir, K., Ogmundsdottir, M.H. et al. (2013) A polymorphism in IRF4 affects human pigmentation through a tyrosinase-dependent MITF/TFAP2A pathway. Cell, 155, 1022-1033.
25. Guenther, C.A., Tasic, B., Luo, L., Bedell, M.A. and Kingsley, D.M. (2014) Amolecular basis for classic blond hair color in Europeans. Nat. Genet., doi: 10.1038/ng.2991.
26. Walsh, S., Liu, F., Wollstein, A., Kovatsi, L., Ralf, A., Kosiniak-Kamysz, A., Branicki, W. and Kayser, M. (2013) The HIrisPlex system for simultaneous prediction of hair and eye colour from DNA. Forensic Sci. Int. Genet., 7, 98-115.
27. Pritchard, J.K., Stephens, M. and Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959.
28. Lao, O., Vallone, P.M., Coble, M.D., Diegoli, T.M., van Oven, M., van der Gaag, K.J., Pijpe, J., de Knijff, P. and Kayser, M. (2010) Evaluating self-declared ancestry of US Americans with autosomal, Y-chromosomal and mitochondrial DNA. Hum. Mutat., 31, E1875-E1893.
29. Fitzpatrick, T.B. and Breathnach, A.S. (1963) [the Epidermal Melanin Unit System] Das Epidermale Melanin-Einheit-System. Dermatol. Wochenschr., 147, 481-489.
30. Praetorius, C., Sturm, R.A. and Steingrimsson, E. (2014) Sun-induced freckling: ephelides and solar lentigines. Pigment Cell Melanoma Res., 27, 339-350.
31. Shlyueva, D., Stampfel, G. and Stark, A. (2014) Transcriptional enhancers: from properties to genome-wide predictions. Nat. Rev. Genet., 15, 272-286.
32. Creyghton, M.P., Cheng, A.W., Welstead, G.G., Kooistra, T., Carey, B.W., Steine, E.J., Hanna, J., Lodato, M.A., Frampton, G.M., Sharp, P.A. et al. (2010) Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc. Natl. Acad. Sci. USA, 107, 21931-21936.
33. Rosenbloom, K.R., Sloan, C.A., Malladi, V.S., Dreszer, T.R., Learned, K., Kirkup, V.M., Wong, M.C., Maddren, M., Fang, R., Heitner, S.G. et al. (2013) ENCODE data in the UCSC Genome Browser: year 5 update. Nucleic Acids Res., 41, D56-D63.
34. Strub, T., Giuliano, S., Ye, T., Bonet, C., Keime, C., Kobi, D., Le Gras, S., Cormont, M., Ballotti, R., Bertolotto, C. et al. (2011) Essential role of microphthalmia transcription factor for DNA replication, mitosis and genomic stability in melanoma. Oncogene, 30, 2319-2332.
35. Levy, C., Khaled, M. and Fisher, D.E. (2006) MITF: master regulator of melanocyte development and melanoma oncogene. Trends Mol. Med., 12, 406-414.
36. Li, J.Y., Song, J.S., Bell, R.J.A., Tran, T.N.T., Haq, R., Liu, H.F., Love, K.T., Langer, R., Anderson, D.G., Larue, L. et al. (2012) YY1 regulates melanocyte development and function by cooperating with MITF. PLoS Genet., 8, e1002688.
37. Gorkin, D.U., Lee, D., Reed, X., Fletez-Brant, C., Bessling, S.L., Loftus, S.K., Beer, M.A., Pavan, W.J. and McCallion, A.S. (2012) Integration of ChIP-seq and machine learning reveals enhancers and a predictive regulatory sequence vocabulary in melanocytes. Genome Res., 22, 2290-2301.
38. Siepel, A., Bejerano, G., Pedersen, J.S., Hinrichs, A.S., Hou, M., Rosenbloom, K., Clawson, H., Spieth, J., Hillier, L.W., Richards, S. et al. (2005) Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res., 15, 1034-1050.
39. Genomes Project, C., Abecasis, G.R., Auton, A., Brooks, L.D., DePristo, M.A., Durbin, R.M., Handsaker, R.E., Kang, H.M., Marth, G.T. and McVean, G.A. (2012) An integrated map of genetic variation from 1,092 human genomes. Nature, 491, 56-65.
40. Eilbeck, K., Lewis, S.E., Mungall, C.J., Yandell, M., Stein, L., Durbin, R. and Ashburner, M. (2005) The sequence ontology: a tool for the unification of genome annotations. Genome Biol., 6, R44.
41. Flicek, P., Amode, M.R., Barrell, D., Beal, K., Billis, K., Brent, S., Carvalho-Silva, D., Clapham, P., Coates, G., Fitzgerald, S. et al. (2014) Ensembl 2014. Nucleic Acids Res., 42, D749-D755.
42. Felsenfeld, G. and Groudine, M. (2003) Controlling the double helix. Nature, 421, 448-453.
43. McVicker, G., van de Geijn, B., Degner, J.F., Cain, C.E., Banovich, N.E., Raj, A., Lewellen, N., Myrthil, M., Gilad, Y. and Pritchard, J.K. (2013) Identification of genetic variants that affect histone modifications in human cells. Science, 342, 747-749.
44. Smale, S.T. and Kadonaga, J.T. (2003) The RNA polymerase II core promoter. Annu. Rev. Biochem., 72, 449-479.
45. Visel, A., Rubin, E.M. and Pennacchio, L.A. (2009) Genomic views of distant-acting enhancers. Nature, 461, 199-205.
46. Zhang, X., Bailey, S.D. and Lupien, M. (2014) Laying a solid foundation for Manhattan -'setting the functional basis for the post-GWAS era'. Trends Genet., 30, 140-149.
47. Karolchik, D., Barber, G.P., Casper, J., Clawson, H., Cline, M.S., Diekhans, M., Dreszer, T.R., Fujita, P.A., Guruvadoo, L., Haeussler, M. et al. (2014) The UCSC Genome Browser database: 2014 update. Nucleic Acids Res., 42, D764-D770.
48. Marsman, J. and Horsfield, J.A. (2012) Long distance relationships: enhancer-promoter communication and dynamic gene transcription. Biochim. Biophys. Acta, 1819, 1217-1227.
49. Bhoj, E.J., Ramos, P., Baker, L.A., Cost, N., Nordenskjold, A., Elder, F.F., Bleyl, S.B., Bowles, N.E., Arrington, C.B., Delhomme, B. et al. (2011) Human balanced translocation and mouse gene inactivation implicate Basonuclin 2 in distal urethral development. Eur. J. Hum. Genet., 19, 540-546.
50. Shpak, M., Hall, A.W., Goldberg, M.M., Derryberry, D.Z., Ni, Y., Iyer, V.R. and Cowperthwaite, M.C. (2014) An eQTL analysis of the human glioblastoma multiforme genome. Genomics, 103, 252-263.
51. Song, H.L., Ramus, S.J., Tyrer, J., Bolton, K.L., Gentry-Maharaj, A., Wozniak, E., Anton-Culver, H., Chang-Claude, J., Cramer, D.W., DiCioccio,R. et al. (2009)Agenome-wide association study identifies a new ovarian cancer susceptibility locus on 9p22.2. Nat. Genet., 41, 996-1000.
52. Wentzensen, N., Black, A., Jacobs, K., Yang, H.P., Berg, C.D., Caporaso, N., Peters, U., Ragard, L., Buys, S.S., Chanock, S. et al. (2011) Genetic variation on 9p22 is associated with abnormal ovarian ultrasound results in the prostate, lung, colorectal, and ovarian cancer screening trial. PLoS ONE, 6, e21731.
53. Haraksingh, R.R. and Snyder, M.P. (2013) Impacts of variation in the human genome on gene regulation. J. Mol. Biol., 425, 3970-3977.
54. van den Boogaard, M., Barnett, P. and Christoffels, V.M. (2014) From GWAS to function: Genetic variation in sodium channel gene enhancer influences electrical patterning. Trends Cardiovasc. Med., 24, 99-104.
55. Visser, M., Kayser, M., Grosveld, F. and Palstra, R.J. (2014) Genetic variation in regulatory DNA elements: the case of OCA2 transcriptional regulation. Pigment Cell Melanoma Res., 27, 169-177.
56. Chardon, A., Cretois, I. and Hourseau, C. (1991) Skin colour typology and suntanning pathways. Int. J. Cosmet. Sci., 13, 191-208.
57. Del Bino, S., Sok, J., Bessac, E. and Bernerd, F. (2006) Relationship between skin response to ultraviolet exposure and skin color type. Pigment Cell Res., 19, 606-614.
58. Trost, A., Bauer, J.W., Lanschutzer, C., Laimer, M., Emberger, M., Hintner, H. and Onder, K. (2007) Rapid, high-quality and epidermal-specific isolation of RNA from human skin. Exp. Dermatol., 16, 185-190.
59. Soler, E., Andrieu-Soler, C., de Boer, E., Bryne, J.C., Thongjuea, S., Stadhouders, R., Palstra, R.J., Stevens, M., Kockx, C. and van IJcken, W. (2010)The genome-wide dynamics of the binding ofLdb1 complexes during erythroid differentiation. Genes Dev., 24, 277-289.
60. Thorvaldsdottir, H., Robinson, J.T. and Mesirov, J.P. (2013) Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform., 14, 178-192.
61. Johnson, A.D., Handsaker, R.E., Pulit, S.L., Nizzari, M.M., O'Donnell, C.J. and de Bakker, P.I. (2008) SNAP: a web-based tool for identification and annotation of proxy SNPs using HapMap. Bioinformatics, 24, 2938-2939.
62. Bernstein, B.E., Stamatoyannopoulos, J.A., Costello, J.F., Ren, B., Milosavljevic, A., Meissner, A., Kellis, M., Marra, M.A., Beaudet, A.L., Ecker, J.R. et al. (2010) The NIH Roadmap Epigenomics Mapping Consortium. Nat. Biotechnol., 28, 1045-1048.