A genome-wide association scan in admixed Latin Americans identifies loci influencing facial and scalp hair features

Nature Communications

Volumn 7, Issue , 2016, Pages

  Adhikari, Kaustubh ^a   Fontanil, Tania ^b   Cal, Santiago ^b   Mendoza Revilla, Javier ^a,c   Fuentes Guajardo, Macarena ^a,d   Chacón Duque, Juan Camilo ^a   Al Saadi, Farah ^a   Johansson, Jeanette A ^e   Quinto Sanchez, Mirsha ^f   Acuña Alonzo, Victor ^a,g   Jaramillo, Claudia ^h   Arias, William ^h   Lozano, Rodrigo Barquera ^g,i   Pérez, Gastón Macín ^g,i   Gómez Valdés, Jorge ^j   Villamil Ramírez, Hugo ⁱ   Hunemeier, Tábita ^k,n   Ramallo, Virginia ^f,k   De Cerqueira, Caio C Silva ^f,k   Hurtado, Malena ^c   Villegas, Valeria ^c   Granja, Vanessa ^c   Gallo, Carla ^c   Poletti, Giovanni ^c   Schuler Faccini, Lavinia ^k   Salzano, Francisco M ^k   Bortolini, Maria Cátira ^k   Canizales Quinteros, Samuel ⁱ   Rothhammer, Francisco ^d   Bedoya, Gabriel ^h   Gonzalez José, Rolando ^f   Headon, Denis ^e   López Otín, Carlos ^b   Tobin, Desmond J ^l   Balding, David ^a,m   Ruiz Linares, Andrés ^a   more..

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b DEPARTAMENTO DE BIOQUÍMICA Y BIOLOGÍA MOLECULAR   (Spain)

^c UNIVERSIDAD PERUANA CAYETANO HEREDIA   (Peru)

^d UNIVERSIDAD DE TARAPACÁ   (Chile)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

^f Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^g National Institute of Anthropology and History   (Mexico)

^h UNIVERSIDAD DE ANTIOQUIA   (Colombia)

ⁱ UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^j UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^k FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^l UNIVERSITY OF BRADFORD   (United Kingdom)

^m UNIVERSITY OF MELBOURNE   (Australia)

ⁿ UNIVERSITY OF SÃO PAULO   (Brazil)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; INTERFERON REGULATORY FACTOR 4; PROLYL ENDOPEPTIDASE; PROTEASE SERINE S1 FAMILY MEMBER 53 PROTEIN; SERINE PROTEINASE; TRANSCRIPTION FACTOR FOXP2; TRANSCRIPTION FACTOR GATA 3; UNCLASSIFIED DRUG; XEDAR RECEPTOR;

ENZYME; EVOLUTION; GENE EXPRESSION; GENOME; GENOMICS; HAIR; ROOT; ROOT ARCHITECTURE; SHAPE; SIGNAL;

ADULT; ALOPECIA; AMERICAN INDIAN; AMINO ACID SUBSTITUTION; ARTICLE; BRAZIL; CHILE; COLOMBIA; EUROPEAN; EYEBROW; FACIES; FEMALE; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENETIC ASSOCIATION; GENETIC VARIABILITY; HAIR; HAIR COLOR; HAIR FOLLICLE; HAIR GROWTH; HUMAN; HUMAN GENOME; IN VITRO STUDY; MALE; MEXICO; NORMAL HUMAN; PERU; PHENOTYPIC VARIATION; PROTEIN EXPRESSION; SCALP HAIR; SINGLE NUCLEOTIDE POLYMORPHISM; STATISTICAL SIGNIFICANCE; THICKNESS; ANCESTRY GROUP; FACE; GENE EXPRESSION REGULATION; GENETIC VARIATION; GENOME-WIDE ASSOCIATION STUDY; GROWTH, DEVELOPMENT AND AGING; PHYSIOLOGY; SCALP;

CONTINENTAL POPULATION GROUPS; FACE; FEMALE; GENE EXPRESSION REGULATION; GENETIC VARIATION; GENOME-WIDE ASSOCIATION STUDY; HAIR; HUMANS; MALE; SCALP;

EID: 84959515522     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms10815     Document Type: Article

References (69)

1. Bradley, B. J. M., N.I. The primate palette: the evolution of primate coloration. Evol. Anthropol. 17, 97-111 (2008).
2. Jablonski, N. G. Skin: A Natural History (Univ. of California Press, 2006).
3. Jablonski, N. G. The naked truth. Sci. Am. 302, 42-49 (2010).
4. Loussouarn, G. et al. Worldwide diversity of hair curliness: a new method of assessment. Int. J. Dermatol. 46(Suppl 1): 2-6 (2007).
5. Panhard, S., Lozano, I. & Loussouarn, G. Greying of the human hair: a worldwide survey, revisiting the '50' rule of thumb. Br. J. Dermatol. 167, 865-873 (2012).
6. Westgate, G. E., Botchkareva, N. V. & Tobin, D. J. The biology of hair diversity. Int. J. Cosmet. Sci. 35, 329-336 (2013).
7. Nyholt, D. R., Gillespie, N. A., Heath, A. C. & Martin, N. G. Genetic basis of male pattern baldness. J. Invest. Dermatol. 121, 1561-1564 (2003).
8. Gunn, D. A. et al. Why some women look young for their age. PLoS ONE 4, e8021 (2009).
9. Medland, S. E., Zhu, G. & Martin, N. G. Estimating the heritability of hair curliness in twins of European ancestry. Twin. Res. Hum. Genet. 12, 514-518 (2009).
10. Lin, B. D. et al. Heritability and Genome-Wide Association Studies for Hair Color in a Dutch Twin Family Based Sample. Genes (Basel) 6, 559-576 (2015).
11. Frost, P. The Puzzle of European Hair, Eye, and Skin Color. Adv. Anthropol. 4, 78-88 (2014).
12. Li, R. et al. Six novel susceptibility Loci for early-onset androgenetic alopecia and their unexpected association with common diseases. PLoS Genet. 8, e1002746 (2012).
13. Liu, F., Wen, B. & Kayser, M. Colorful DNA polymorphisms in humans. Semin. Cell Dev. Biol. 24, 562-575 (2013).
14. Medland, S. E. et al. Common variants in the trichohyalin gene are associated with straight hair in Europeans. Am. J. Hum. Genet. 85, 750-755 (2009).
15. Eriksson, N. et al. Web-based, participant-driven studies yield novel genetic associations for common traits. PLoS Genet. 6, e1000993 (2010).
16. Tan, J. et al. The adaptive variant EDARV370A is associated with straight hair in East Asians. Hum. Genet. 132, 1187-1191 (2013).
17. Ruiz-Linares, A. et al. Admixture in latin america: geographic structure, phenotypic diversity and self-perception of ancestry based on 7,342 individuals. PLoS Genet. 10, e1004572 (2014).
18. Adhikari, K. et al. A genome-wide association study identifies multiple loci for variation in human ear morphology. Nat. Commun. 6, 7500 (2015).
19. Speed, D., Hemani, G., Johnson, M. R. & Balding, D. J. Improved heritability estimation from genome-wide SNPs. Am. J. Hum. Genet. 91, 1011-1021 (2012).
20. Yang, J., Lee, S. H., Goddard, M. E. & Visscher, P. M. GCTA: a tool for genomewide complex trait analysis. Am. J. Hum. Genet. 88, 76-82 (2011).
21. Purcell, S. et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559-575 (2007).
22. Willer, C. J., Li, Y. & Abecasis, G. R. METAL: fast and efficient meta-analysis of genomewide association scans. Bioinformatics 26, 2190-2191 (2010).
23. Mikkola, M. L. Molecular aspects of hypohidrotic ectodermal dysplasia. Am. J. Med. Genet. A 149A, 2031-2036 (2009).
24. Fujimoto, A. et al. A scan for genetic determinants of human hair morphology: EDAR is associated with Asian hair thickness. Hum. Mol. Genet. 17, 835-843 (2008).
25. Fujimoto, A. et al. A replication study confirmed the EDAR gene to be a major contributor to population differentiation regarding head hair thickness in Asia. Hum. Genet. 124, 179-185 (2008).
26. Mou, C. et al. Enhanced ectodysplasin-A receptor (EDAR) signaling alters multiple fiber characteristics to produce the East Asian hair form. Hum. Mutat. 29, 1405-1411 (2008).
27. Kamberov, Y. G. et al. Modeling recent human evolution in mice by expression of a selected EDAR variant. Cell 152, 691-702 (2013).
28. Bhogal, R. K., Mouser, P. E., Higgins, C. A. & Turner, G. A. Protease activity, localization and inhibition in the human hair follicle. Int. J. Cosmet. Sci. 36, 46-53 (2014).
29. Spacek, D. V. et al. The mouse frizzy (fr) and rat 'hairless' (frCR) mutations are natural variants of protease serine S1 family member 8 (Prss8). Exp. Dermatol. 19, 527-532 (2010).
30. Leyvraz, C. et al. The epidermal barrier function is dependent on the serine protease CAP1/Prss8. J. Cell Biol. 170, 487-496 (2005).
31. Mlitz, V. et al. Trichohyalin-like proteins have evolutionarily conserved roles in the morphogenesis of skin appendages. J. Invest. Dermatol. 134, 2685-2692 (2014).
32. Kaufman, C. K. et al. GATA-3: an unexpected regulator of cell lineage determination in skin. Genes Dev. 17, 2108-2122 (2003).
33. Kurek, D., Garinis, G. A., van Doorninck, J. H., van der Wees, J. & Grosveld, F. G. Transcriptome and phenotypic analysis reveals Gata3-dependent signalling pathways in murine hair follicles. Development 134, 261-272 (2007).
34. D'Haene, B. et al. Disease-causing 7.4kb cis-regulatory deletion disrupting conserved non-coding sequences and their interaction with the FOXL2 promotor: implications for mutation screening. PLoS Genet. 5, e1000522 (2009).
35. Heude, E. et al. Etiology of craniofacial malformations in mouse models of blepharophimosis, ptosis, and epicanthus inversus syndrome. Hum. Mol. Genet. 24, 1670-1681 (2015).
36. Shi, F. et al. A piggyBac insertion disrupts Foxl2 expression that mimics BPES syndrome in mice. Hum. Mol. Genet. 23, 3792-3800 (2014).
37. Pingault, V. et al. Review and update of mutations causing Waardenburg syndrome. Hum. Mutat. 31, 391-406 (2010).
38. Liu, F. et al. A genome-wide association study identifies five loci influencing facial morphology in Europeans. PLoS Genet. 8, e1002932 (2012).
39. Paternoster, L. et al. Genome-wide association study of three-dimensional facial morphology identifies a variant in PAX3 associated with nasion position. Am. J. Hum. Genet. 90, 478-485 (2012).
40. Monsoro-Burq, A. H. PAX transcription factors in neural crest development. Semin. Cell Dev. Biol. 44, 87-96 (2015).
41. Praetorius, C. et al. A polymorphism in IRF4 affects human pigmentation through a tyrosinase-dependent MITF/TFAP2A pathway. Cell 155, 1022-1033 (2013).
42. Steinert, P. M., Parry, D. A. & Marekov, L. N. Trichohyalin mechanically strengthens the hair follicle: multiple cross-bridging roles in the inner root shealth. J. Biol. Chem. 278, 41409-41419 (2003).
43. Fischer, H. et al. Essential role of the keratinocyte-specific endonuclease DNase1L2 in the removal of nuclear DNA from hair and nails. J. Invest. Dermatol. 131, 1208-1215 (2011).
44. Wagner, R. & Joekes, I. Hair medulla morphology and mechanical properties. J. Cosmet. Sci. 58, 359-368 (2007).
45. Tsuji, A. et al. Engineering of alpha I-antitrypsin variants selective for subtilisin-like proprotein convertases PACE4 and PC6: importance of the P2′ residue in stable complex formation of the serpin with proprotein convertase. Protein Engin. Des. Sel. 20, 163-170 (2007).
46. Grossman, S. R. et al. Identifying recent adaptations in large-scale genomic data. Cell 152, 703-713 (2013).
47. Grossman, S. R. et al. A composite of multiple signals distinguishes causal variants in regions of positive selection. Science 327, 883-886 (2010).
48. Medland, S. E. et al. Common variants in the trichohyalin gene are associated with straight hair in Europeans. Am. J. Hum. Genet. 85, 750-755 (2009).
49. Tobin, D. J. et al. The lysosomal protease cathepsin L is an important regulator of keratinocyte and melanocyte differentiation during hair follicle morphogenesis and cycling. Am. J. Pathol. 160, 1807-1821 (2002).
50. Eissa, A. & Diamandis, E. P. Human tissue kallikreins as promiscuous modulators of homeostatic skin barrier functions. Biol. Chem. 389, 669-680 (2008).
51. Le, N. A. et al. Regulation of serine protease inhibitor Kazal type-5 (SPINK5) gene expression in the keratinocytes. Environ Health Prev. Med. 19, 307-313 (2014).
52. Johansson, J. A. & Headon, D. J. Regionalisation of the skin. Semin. Cell Dev. Biol. 25-26, 3-10 (2014).
53. Mou, C., Jackson, B., Schneider, P., Overbeek, P. A. & Headon, D. J. Generation of the primary hair follicle pattern. Proc. Natl Acad. Sci. USA 103, 9075-9080 (2006).
54. Held, L. I. The evo-devo puzzle of human hair patterning. Evol. Biol. 37, 113-122 (2010).
55. Matama, T., Gomes, A. C. & Cavaco-Paulo, A. Hair coloration by gene regulation: fact or fiction? Trends Biotechnol. 33, 707-711 (2015).
56. Pospiech, E. et al. Evaluation of the predictive capacity of DNA variants associated with straight hair in Europeans. Forensic Sci. Int. Genet. 19, 280-288 (2015).
57. Chang, C. C. et al. Second-generation PLINK: rising to the challenge of larger and richer datasets. Gigascience 4, 7 (2015).
58. Alexander, D. H., Novembre, J. & Lange, K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19, 1655-1664 (2009).
59. O'Connell, J. et al. A general approach for haplotype phasing across the full spectrum of relatedness. PLoS Genet. 10, e1004234 (2014).
60. Howie, B., Fuchsberger, C., Stephens, M., Marchini, J. & Abecasis, G. R. Fast and accurate genotype imputation in genome-wide association studies through pre-phasing. Nature Genet. 44, 955-959 (2012).
61. Genomes Project Consortium et al. An integrated map of genetic variation from 1,092 human genomes. Nature 491, 56-65 (2012).
62. Marchini, J. & Howie, B. Genotype imputation for genome-wide association studies. Nat. Rev. Genet. 11, 499-511 (2010).
63. Higgins, J. P. & Thompson, S. G. Quantifying heterogeneity in a meta-analysis. Stat. Med. 21, 1539-1558 (2002).
64. Hastie, T., Tibshirani, R. & Friedman, J. H. The Elements of Statistical Learning: Data Mining, Inference, and Prediction, xxii 745 (Springer, 2009).
65. Narhi, K. et al. Sostdc1 defines the size and number of skin appendage placodes. Dev. Biol. 364, 149-161 (2012).
66. Cal, S. et al. Identification and characterization of human polyserase-3, a novel protein with tandem serine-protease domains in the same polypeptide chain. BMC Biochem 7, 9 (2006).
67. Incorporated, A. S. Adobe Photoshop CS6 (San Jose, 2012).
68. Pruim, R. J. et al. LocusZoom: regional visualization of genome-wide association scan results. Bioinformatics 26, 2336-2337 (2010).
69. Barrett, J. C., Fry, B., Maller, J. & Daly, M. J. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21, 263-265 (2005).